Hedgehog 'on' state (Homo sapiens)

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54, 75, 97, 12711, 32, 35, 107, 1143, 16, 20, 24, 49...9, 11, 26, 28, 32...6, 17, 48, 64, 75...14, 53, 75, 89, 9211, 14, 19, 21, 22, 32...23, 62, 8315, 33, 36, 70, 73...945, 72, 75, 82, 103...9, 11, 32, 35, 37...14, 21, 22, 53, 55...12, 36, 77, 86, 94...4, 6, 17, 34, 64...82, 103, 1282, 11, 18, 29, 38...23, 62, 8330, 82, 97, 103, 12831, 47, 57, 69, 7836, 77, 86, 94, 12311, 18, 75, 91, 107...12, 16, 31, 41, 47...5, 72, 82, 103, 124...7, 27, 52, 59, 60, 66...16, 49, 7349, 7361, 12131, 47, 57, 781, 8, 10, 13, 35...77, 94, 12323, 62, 8311, 18, 35, 43, 47...16, 49, 50, 63, 73...16, 38, 76, 87, 107...62, 8351, 1006, 25, 64, 67, 71...endocytic vesicle lumennucleoplasmcytosolciliumPSMB9 HHIP gene UBB(77-152) PSMB7 PSMD5 PSMD8 2p-GLI1 SPOPL UBC(77-152) UBB(1-76) UBB(153-228) ub-PTCH1ub-GLI1 CSNK1A1 UBC(381-456) ADPADRBK1SMO NUMB:ITCHPSMD13 UBC(77-152) UBC(153-228) KIF7p6S, T-SMO dimerEVC2 GLI:SUFUCDC73:2p-GLIPSMC5 PSMB10 RPS27A(1-76) PTCH1:SMURFKIF3APTCH1 2p-GLI3 PSMD6 PSMB2 GLI2 p6S,T-SMOdimer:CSNK1A1:ADRBK1EFCAB7 PSMA7 HHIP RBX1 PSME1 PSME2 IHH UBC(609-684) BOC GLI3 IQCE PSMA6 pS588, S590, T593, S595, S611, S615, S616-SMO PTCH1 RBX1 EFCAB7 Ub2p-GLI:GLI1 geneUBC(609-684) PSMA4 DZIP1ITCH EVC2 2p-GLI2 PSMD7 PSMA1 2p-GLI3 UBC(457-532) UBC(229-304) SMO dimer:ARRB:KIF3ACDON2p-GLI2 PSMC2 PTCH2 gene PSMF1 26S proteasomeNUMB PSMC3 SUFU Hh-Npp:CDON:PTCHp6S, T-SMOdimer:EVC2:EVCITCHADRBK1 UBC(533-608) PSMB7 SPOP CSNK1A1 2p-GLI:PTCH1 genePSMD11 GPR161ub-PTCH1:SMURF2p-GLI1 2p-GLI2 PSMC2 UBC(305-380) UBC(381-456) SMO DHH(33-?) PSMC5 26S proteasomeCDON PSMC4 Hh-Npp:GAS1:PTCHGLI1 IQCE:EFCAB7:EVC2:EVC2p-GLI3 PSMD2 SUFUPSMD4 PSMD3 p-GLI3 ULK3:SUFUHHIP gene,PTCH2gene,BOC geneGLI2 ITCH ATPPSMB5 pS588, S590, T593, S595-SMO PSMC3 2p-GLI1 2p-GLI2 PSMB4 UbCSNK1A1 p-GLI1 ADPDHH(33-?) BOC PSMA3 CUL3 EVC2 UBC(1-76) PSMB11 EVC UBC(305-380) PSMA5 PSMD4 ub-PTCH1GPR161CSNK1A1ADRBK1 Hh-Npp2p-GLI2 PSMB6 CUL3 NUMB PSMA2 SMURF1 PSMB5 GLI3 PSMC1 EFCAB7:IQCE2p-GLI1,2,3SHFM1 GLI1,2,3PSMB6 PSME1 ub-2p-GLI2 GLI1 gene EVC UBA52(1-76) UBB(153-228) CDC73 PTCH12p-GLI1 Hh-Npp:BOC:PTCH1UBC(229-304) PTCH1 gene p-GLI1,2,3SMO dimerPSMB8 UBC(609-684) IHH RPS27A(1-76) UBB(153-228) PTCH1 PSMD9 SMURFGLI1 SPOP:CUL3:RBX1pS588, S590, T593, S595, S611, S615, S616-SMO PSMD7 CSNK1A1 2p-GLI:SPOP:CUL3:RBX1GLI2 SHH(34-?) NUMB SPOPL GLI1 p-GLI1 PSMF1 PSMB4 DHH(33-?) PSMD3 PSME4 PSMD5 CUL3 PSMD10 DHH(33-?) UBA52(1-76) UBC(153-228) UBC(533-608) 2p-GLI1SUFU ITCH PSMB8 SMURF2 PSMD1 PSMD14 ub-GLI1:NUMB:ITCHSUFU 2p-GLI2 PSMD8 GAS1ARRB2 HHIPpS588, S590, T593, S595, S611, S615, S616-SMO PSMA7 PSMA1 PSMD6 ub-2p-GLI2,3:SPOP:CUL3:RBX1p-GLI2 UBC(533-608) PSME3 ATPPTCH1 SHH(34-?) 2p-GLI3 PSMD11 NUMBEVC2:EVCPSMD13 GLI1 pS588, S590, T593, S595-SMO GLI1 SHH(34-?) UbGLI1,2,3ATPBOC gene PSMB10 ATPCDC73PSMA2 2p-GLI3 GAS1 IHH 2p-GLI1 PSMC6 HHIP gene PSMB3 UBC(457-532) UBC(77-152) PSMC1 PSMA3 SHH(34-?) PTCH1 geneSMURF1 PSME2 SPOP SMO dimer:CSNK1A1PSMD12 ARRB1 PTCH2 gene PSMD1 RPS27A(1-76) ARRBGLI2 SHFM1 2p-GLI2,3DHH(33-?) PSMB3 IHH ARRB2 p-GLI3 BOC:PTCH1PSMB1 PSMD14 UBC(457-532) GLI3 SMURF2 GLI:SUFUBOC gene UBC(153-228) PSME3 SMO dimerPSMB9 PSMD2 SMO UBA52(1-76) pS588,S590, T593,S595-SMOdimer:CSNK1A1PSMA5 SMURF1 EVC IQCE ub-2p-GLI3 GLI1 geneUBB(1-76) UBC(305-380) PSMC4 PSMD12 SPOP SUFU2p-GLI1:HHIPgene,PTCH2 gene,BOCgeneRBX1 PTCH1 UBB(77-152) UBC(1-76) PSMA6 SHH(34-?) GLI1:NUMB:ITCHGLI1UBC(229-304) UBC(1-76) PSMA4 PSMD10 ADPUBB(1-76) UBC(381-456) ARRB1 p-GLI2 KIF3A ULK3PSMB1 pS588,S590,T593,S595-SMOdimer:CSNK1A1:ADRBK1PSMC6 ADPub-PTCH1 PSMA8 p-GLI1,2,3PSMD9 SMURF2 SPOPL PSMB2 SMO UBB(77-152) ULK3 GLI3 Hh-Npp:HHIPGAS82p-GLI3 unknown kinaseIHH 77111454444, 11645100121474544, 1164457


Description

Hedgehog is a secreted morphogen that has evolutionarily conserved roles in body organization by regulating the activity of the Ci/Gli transcription factor family. In Drosophila in the absence of Hh signaling, full-length Ci is partially degraded by the proteasome to generate a truncated repressor form that translocates to the nucleus to represses Hh-responsive genes. Binding of Hh ligand to the Patched (PTC) receptor allows the 7-pass transmembrane protein Smoothened (SMO) to be activated in an unknown manner, disrupting the partial proteolysis of Ci and allowing the full length activator form to accumulate (reviewed in Ingham et al, 2011; Briscoe and Therond, 2013).
While many of the core components of Hh signaling are conserved from flies to humans, the pathways do show points of significant divergence. Notably, the human genome encodes three Ci homologues, GLI1, 2 and 3 that each play slightly different roles in regulating Hh responsive genes. GLI3 is the primary repressor of Hh signaling in vertebrates, and is converted to the truncated GLI3R repressor form in the absence of Hh. GLI2 is a potent activator of transcription in the presence of Hh but contributes only minimally to the repression function. While a minor fraction of GLI2 protein is processed into the repressor form in the absence of Hh, the majority is either fully degraded by the proteasome or sequestered in the full-length form in the cytosol by protein-protein interactions. GLI1 lacks the repression domain and appears to be an obligate transcriptional activator (reviewed in Briscoe and Therond, 2013).
Vertebrate but not fly Hh signaling also depends on the movement of pathway components through the primary cilium. The primary cilium is a non-motile microtubule based structure whose construction and maintenance depends on intraflagellar transport (IFT). Anterograde IFT moves molecules from the ciliary base along the axoneme to the ciliary tip in a manner that requires the microtubule-plus-end directed kinesin KIF3 motor complex and the IFT-B protein complex, while retrograde IFT back to the ciliary base depends on the minus-end directed dynein motor and the IFT-A complex. Genetic screens have identified a number of cilia-related proteins that are required both to maintain Hh in the 'off' state and to transduce the signal when the pathway is activated (reviewed in Hui and Angers, 2011; Goetz and Anderson, 2010). View original pathway at Reactome.

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Pathway is converted from Reactome ID: 5632684
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Reactome version: 75
Reactome Author 
Reactome Author: Rothfels, Karen

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Bibliography

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  89. Maloverjan A, Piirsoo M.; ''Mammalian homologues of Drosophila fused kinase.''; PubMed Europe PMC Scholia
  90. Kim HR, Richardson J, van Eeden F, Ingham PW.; ''Gli2a protein localization reveals a role for Iguana/DZIP1 in primary ciliogenesis and a dependence of Hedgehog signal transduction on primary cilia in the zebrafish.''; PubMed Europe PMC Scholia
  91. Kim J, Kato M, Beachy PA.; ''Gli2 trafficking links Hedgehog-dependent activation of Smoothened in the primary cilium to transcriptional activation in the nucleus.''; PubMed Europe PMC Scholia
  92. Wilson CW, Nguyen CT, Chen MH, Yang JH, Gacayan R, Huang J, Chen JN, Chuang PT.; ''Fused has evolved divergent roles in vertebrate Hedgehog signalling and motile ciliogenesis.''; PubMed Europe PMC Scholia
  93. Svärd J, Heby-Henricson K, Persson-Lek M, Rozell B, Lauth M, Bergström A, Ericson J, Toftgård R, Teglund S.; ''Genetic elimination of Suppressor of fused reveals an essential repressor function in the mammalian Hedgehog signaling pathway.''; PubMed Europe PMC Scholia
  94. Chen Y, Sasai N, Ma G, Yue T, Jia J, Briscoe J, Jiang J.; ''Sonic Hedgehog dependent phosphorylation by CK1α and GRK2 is required for ciliary accumulation and activation of smoothened.''; PubMed Europe PMC Scholia
  95. Bishop B, Aricescu AR, Harlos K, O'Callaghan CA, Jones EY, Siebold C.; ''Structural insights into hedgehog ligand sequestration by the human hedgehog-interacting protein HHIP.''; PubMed Europe PMC Scholia
  96. Paces-Fessy M, Boucher D, Petit E, Paute-Briand S, Blanchet-Tournier MF.; ''The negative regulator of Gli, Suppressor of fused (Sufu), interacts with SAP18, Galectin3 and other nuclear proteins.''; PubMed Europe PMC Scholia
  97. Hui CC, Angers S.; ''Gli proteins in development and disease.''; PubMed Europe PMC Scholia
  98. Lum L, Zhang C, Oh S, Mann RK, von Kessler DP, Taipale J, Weis-Garcia F, Gong R, Wang B, Beachy PA.; ''Hedgehog signal transduction via Smoothened association with a cytoplasmic complex scaffolded by the atypical kinesin, Costal-2.''; PubMed Europe PMC Scholia
  99. Sekimizu K, Nishioka N, Sasaki H, Takeda H, Karlstrom RO, Kawakami A.; ''The zebrafish iguana locus encodes Dzip1, a novel zinc-finger protein required for proper regulation of Hedgehog signaling.''; PubMed Europe PMC Scholia
  100. Kovacs JJ, Whalen EJ, Liu R, Xiao K, Kim J, Chen M, Wang J, Chen W, Lefkowitz RJ.; ''Beta-arrestin-mediated localization of smoothened to the primary cilium.''; PubMed Europe PMC Scholia
  101. Cheng SY, Bishop JM.; ''Suppressor of Fused represses Gli-mediated transcription by recruiting the SAP18-mSin3 corepressor complex.''; PubMed Europe PMC Scholia
  102. Bae GU, Domené S, Roessler E, Schachter K, Kang JS, Muenke M, Krauss RS.; ''Mutations in CDON, encoding a hedgehog receptor, result in holoprosencephaly and defective interactions with other hedgehog receptors.''; PubMed Europe PMC Scholia
  103. Lee EY, Ji H, Ouyang Z, Zhou B, Ma W, Vokes SA, McMahon AP, Wong WH, Scott MP.; ''Hedgehog pathway-regulated gene networks in cerebellum development and tumorigenesis.''; PubMed Europe PMC Scholia
  104. Stone DM, Murone M, Luoh S, Ye W, Armanini MP, Gurney A, Phillips H, Brush J, Goddard A, de Sauvage FJ, Rosenthal A.; ''Characterization of the human suppressor of fused, a negative regulator of the zinc-finger transcription factor Gli.''; PubMed Europe PMC Scholia
  105. McLellan JS, Zheng X, Hauk G, Ghirlando R, Beachy PA, Leahy DJ.; ''The mode of Hedgehog binding to Ihog homologues is not conserved across different phyla.''; PubMed Europe PMC Scholia
  106. Tay SY, Yu X, Wong KN, Panse P, Ng CP, Roy S.; ''The iguana/DZIP1 protein is a novel component of the ciliogenic pathway essential for axonemal biogenesis.''; PubMed Europe PMC Scholia
  107. Humke EW, Dorn KV, Milenkovic L, Scott MP, Rohatgi R.; ''The output of Hedgehog signaling is controlled by the dynamic association between Suppressor of Fused and the Gli proteins.''; PubMed Europe PMC Scholia
  108. Stone DM, Hynes M, Armanini M, Swanson TA, Gu Q, Johnson RL, Scott MP, Pennica D, Goddard A, Phillips H, Noll M, Hooper JE, de Sauvage F, Rosenthal A.; ''The tumour-suppressor gene patched encodes a candidate receptor for Sonic hedgehog.''; PubMed Europe PMC Scholia
  109. Olsen CL, Hsu PP, Glienke J, Rubanyi GM, Brooks AR.; ''Hedgehog-interacting protein is highly expressed in endothelial cells but down-regulated during angiogenesis and in several human tumors.''; PubMed Europe PMC Scholia
  110. Taylor MD, Liu L, Raffel C, Hui CC, Mainprize TG, Zhang X, Agatep R, Chiappa S, Gao L, Lowrance A, Hao A, Goldstein AM, Stavrou T, Scherer SW, Dura WT, Wainwright B, Squire JA, Rutka JT, Hogg D.; ''Mutations in SUFU predispose to medulloblastoma.''; PubMed Europe PMC Scholia
  111. Zhuang M, Calabrese MF, Liu J, Waddell MB, Nourse A, Hammel M, Miller DJ, Walden H, Duda DM, Seyedin SN, Hoggard T, Harper JW, White KP, Schulman BA.; ''Structures of SPOP-substrate complexes: insights into molecular architectures of BTB-Cul3 ubiquitin ligases.''; PubMed Europe PMC Scholia
  112. Marigo V, Davey RA, Zuo Y, Cunningham JM, Tabin CJ.; ''Biochemical evidence that patched is the Hedgehog receptor.''; PubMed Europe PMC Scholia
  113. Jin Z, Mei W, Strack S, Jia J, Yang J.; ''The antagonistic action of B56-containing protein phosphatase 2As and casein kinase 2 controls the phosphorylation and Gli turnover function of Daz interacting protein 1.''; PubMed Europe PMC Scholia
  114. Tukachinsky H, Lopez LV, Salic A.; ''A mechanism for vertebrate Hedgehog signaling: recruitment to cilia and dissociation of SuFu-Gli protein complexes.''; PubMed Europe PMC Scholia
  115. Evron T, Daigle TL, Caron MG.; ''GRK2: multiple roles beyond G protein-coupled receptor desensitization.''; PubMed Europe PMC Scholia
  116. Voges D, Zwickl P, Baumeister W.; ''The 26S proteasome: a molecular machine designed for controlled proteolysis.''; PubMed Europe PMC Scholia
  117. Evangelista M, Lim TY, Lee J, Parker L, Ashique A, Peterson AS, Ye W, Davis DP, de Sauvage FJ.; ''Kinome siRNA screen identifies regulators of ciliogenesis and hedgehog signal transduction.''; PubMed Europe PMC Scholia
  118. Incardona JP, Lee JH, Robertson CP, Enga K, Kapur RP, Roelink H.; ''Receptor-mediated endocytosis of soluble and membrane-tethered Sonic hedgehog by Patched-1.''; PubMed Europe PMC Scholia
  119. Furukawa M, He YJ, Borchers C, Xiong Y.; ''Targeting of protein ubiquitination by BTB-Cullin 3-Roc1 ubiquitin ligases.''; PubMed Europe PMC Scholia
  120. Glazer AM, Wilkinson AW, Backer CB, Lapan SW, Gutzman JH, Cheeseman IM, Reddien PW.; ''The Zn finger protein Iguana impacts Hedgehog signaling by promoting ciliogenesis.''; PubMed Europe PMC Scholia
  121. Mosimann C, Hausmann G, Basler K.; ''The role of Parafibromin/Hyrax as a nuclear Gli/Ci-interacting protein in Hedgehog target gene control.''; PubMed Europe PMC Scholia
  122. Lu X, Liu S, Kornberg TB.; ''The C-terminal tail of the Hedgehog receptor Patched regulates both localization and turnover.''; PubMed Europe PMC Scholia
  123. Chen Y, Li S, Tong C, Zhao Y, Wang B, Liu Y, Jia J, Jiang J.; ''G protein-coupled receptor kinase 2 promotes high-level Hedgehog signaling by regulating the active state of Smo through kinase-dependent and kinase-independent mechanisms in Drosophila.''; PubMed Europe PMC Scholia
  124. Dai P, Akimaru H, Tanaka Y, Maekawa T, Nakafuku M, Ishii S.; ''Sonic Hedgehog-induced activation of the Gli1 promoter is mediated by GLI3.''; PubMed Europe PMC Scholia
  125. Evron T, Philipp M, Lu J, Meloni AR, Burkhalter M, Chen W, Caron MG.; ''Growth Arrest Specific 8 (Gas8) and G protein-coupled receptor kinase 2 (GRK2) cooperate in the control of Smoothened signaling.''; PubMed Europe PMC Scholia
  126. Varjosalo M, Li SP, Taipale J.; ''Divergence of hedgehog signal transduction mechanism between Drosophila and mammals.''; PubMed Europe PMC Scholia
  127. Ingham PW, Nakano Y, Seger C.; ''Mechanisms and functions of Hedgehog signalling across the metazoa.''; PubMed Europe PMC Scholia
  128. Vokes SA, Ji H, McCuine S, Tenzen T, Giles S, Zhong S, Longabaugh WJ, Davidson EH, Wong WH, McMahon AP.; ''Genomic characterization of Gli-activator targets in sonic hedgehog-mediated neural patterning.''; PubMed Europe PMC Scholia

History

View all...
CompareRevisionActionTimeUserComment
114890view16:40, 25 January 2021ReactomeTeamReactome version 75
113336view11:40, 2 November 2020ReactomeTeamReactome version 74
112547view15:51, 9 October 2020ReactomeTeamReactome version 73
101461view11:32, 1 November 2018ReactomeTeamreactome version 66
100999view21:11, 31 October 2018ReactomeTeamreactome version 65
100535view19:45, 31 October 2018ReactomeTeamreactome version 64
100082view16:30, 31 October 2018ReactomeTeamreactome version 63
99633view15:02, 31 October 2018ReactomeTeamreactome version 62 (2nd attempt)
99239view12:44, 31 October 2018ReactomeTeamreactome version 62
94028view13:52, 16 August 2017ReactomeTeamreactome version 61
93650view11:29, 9 August 2017ReactomeTeamreactome version 61
87140view18:52, 18 July 2016MkutmonOntology Term : 'Hedgehog signaling pathway' added !
86766view09:25, 11 July 2016ReactomeTeamreactome version 56
85681view02:23, 5 June 2016AlexanderPicoQuick edit to datanode annotation or property
83588view07:53, 26 November 2015EgonwAdded missing ENSG parts of the Ensembl IDs.
83259view10:34, 18 November 2015ReactomeTeamVersion54
81371view12:54, 21 August 2015ReactomeTeamNew pathway

External references

DataNodes

View all...
NameTypeDatabase referenceComment
26S proteasomeComplexR-HSA-177750 (Reactome)
26S proteasomeComplexR-HSA-68819 (Reactome)
2p-GLI1 ProteinP08151 (Uniprot-TrEMBL)
2p-GLI1,2,3ComplexR-HSA-5635077 (Reactome)
2p-GLI1:HHIP

gene,PTCH2 gene,BOC

gene
ComplexR-HSA-5635078 (Reactome)
2p-GLI1ProteinP08151 (Uniprot-TrEMBL)
2p-GLI2 ProteinP10070 (Uniprot-TrEMBL)
2p-GLI2,3ComplexR-HSA-5635080 (Reactome)
2p-GLI3 ProteinP10071 (Uniprot-TrEMBL)
2p-GLI:GLI1 geneComplexR-HSA-5635082 (Reactome)
2p-GLI:PTCH1 geneComplexR-HSA-5635085 (Reactome)
2p-GLI:SPOP:CUL3:RBX1ComplexR-HSA-5635087 (Reactome)
ADPMetaboliteCHEBI:456216 (ChEBI)
ADRBK1 ProteinP25098 (Uniprot-TrEMBL)
ADRBK1ProteinP25098 (Uniprot-TrEMBL)
ARRB1 ProteinP49407 (Uniprot-TrEMBL)
ARRB2 ProteinP32121 (Uniprot-TrEMBL)
ARRBComplexR-HSA-1911410 (Reactome)
ATPMetaboliteCHEBI:30616 (ChEBI)
BOC ProteinQ9BWV1 (Uniprot-TrEMBL)
BOC gene ProteinENSG00000144857 (Ensembl)
BOC:PTCH1ComplexR-HSA-5632584 (Reactome)
CDC73 ProteinQ6P1J9 (Uniprot-TrEMBL)
CDC73:2p-GLIComplexR-HSA-5635076 (Reactome)
CDC73ProteinQ6P1J9 (Uniprot-TrEMBL)
CDON ProteinQ4KMG0 (Uniprot-TrEMBL)
CDONProteinQ4KMG0 (Uniprot-TrEMBL)
CSNK1A1 ProteinP48729 (Uniprot-TrEMBL)
CSNK1A1ProteinP48729 (Uniprot-TrEMBL)
CUL3 ProteinQ13618 (Uniprot-TrEMBL)
DHH(33-?) ProteinO43323 (Uniprot-TrEMBL)
DZIP1ProteinQ86YF9 (Uniprot-TrEMBL)
EFCAB7 ProteinA8K855 (Uniprot-TrEMBL)
EFCAB7:IQCEComplexR-HSA-5633045 (Reactome)
EVC ProteinP57679 (Uniprot-TrEMBL)
EVC2 ProteinQ86UK5 (Uniprot-TrEMBL)
EVC2:EVCComplexR-HSA-5633041 (Reactome)
GAS1 ProteinP54826 (Uniprot-TrEMBL)
GAS1ProteinP54826 (Uniprot-TrEMBL)
GAS8ProteinO95995 (Uniprot-TrEMBL)
GLI1 ProteinP08151 (Uniprot-TrEMBL)
GLI1 gene ProteinENSG00000111087 (Ensembl)
GLI1 geneGeneProductENSG00000111087 (Ensembl)
GLI1,2,3ComplexR-HSA-5610616 (Reactome)
GLI1,2,3ComplexR-HSA-5621782 (Reactome)
GLI1:NUMB:ITCHComplexR-HSA-5635832 (Reactome)
GLI1ProteinP08151 (Uniprot-TrEMBL)
GLI2 ProteinP10070 (Uniprot-TrEMBL)
GLI3 ProteinP10071 (Uniprot-TrEMBL)
GLI:SUFUComplexR-HSA-5621780 (Reactome)
GLI:SUFUComplexR-HSA-5621783 (Reactome)
GPR161ProteinQ8N6U8 (Uniprot-TrEMBL)
HHIP ProteinQ96QV1 (Uniprot-TrEMBL)
HHIP gene ProteinENSG00000164161 (Ensembl)
HHIP gene,PTCH2 gene,BOC geneComplexR-HSA-5635070 (Reactome)
HHIPProteinQ96QV1 (Uniprot-TrEMBL)
Hh-Npp:BOC:PTCH1ComplexR-HSA-5632588 (Reactome)
Hh-Npp:CDON:PTCHComplexR-HSA-5632590 (Reactome)
Hh-Npp:GAS1:PTCHComplexR-HSA-5632592 (Reactome)
Hh-Npp:HHIPComplexR-HSA-445447 (Reactome)
Hh-NppComplexR-HSA-5362783 (Reactome)
IHH ProteinQ14623 (Uniprot-TrEMBL)
IQCE ProteinQ6IPM2 (Uniprot-TrEMBL)
IQCE:EFCAB7:EVC2:EVCComplexR-HSA-5633050 (Reactome)
ITCH ProteinQ96J02 (Uniprot-TrEMBL)
ITCHProteinQ96J02 (Uniprot-TrEMBL)
KIF3A ProteinQ9Y496 (Uniprot-TrEMBL)
KIF3AProteinQ9Y496 (Uniprot-TrEMBL)
KIF7ProteinQ2M1P5 (Uniprot-TrEMBL)
NUMB ProteinP49757 (Uniprot-TrEMBL)
NUMB:ITCHComplexR-HSA-5610562 (Reactome)
NUMBProteinP49757 (Uniprot-TrEMBL)
PSMA1 ProteinP25786 (Uniprot-TrEMBL)
PSMA2 ProteinP25787 (Uniprot-TrEMBL)
PSMA3 ProteinP25788 (Uniprot-TrEMBL)
PSMA4 ProteinP25789 (Uniprot-TrEMBL)
PSMA5 ProteinP28066 (Uniprot-TrEMBL)
PSMA6 ProteinP60900 (Uniprot-TrEMBL)
PSMA7 ProteinO14818 (Uniprot-TrEMBL)
PSMA8 ProteinQ8TAA3 (Uniprot-TrEMBL)
PSMB1 ProteinP20618 (Uniprot-TrEMBL)
PSMB10 ProteinP40306 (Uniprot-TrEMBL)
PSMB11 ProteinA5LHX3 (Uniprot-TrEMBL)
PSMB2 ProteinP49721 (Uniprot-TrEMBL)
PSMB3 ProteinP49720 (Uniprot-TrEMBL)
PSMB4 ProteinP28070 (Uniprot-TrEMBL)
PSMB5 ProteinP28074 (Uniprot-TrEMBL)
PSMB6 ProteinP28072 (Uniprot-TrEMBL)
PSMB7 ProteinQ99436 (Uniprot-TrEMBL)
PSMB8 ProteinP28062 (Uniprot-TrEMBL)
PSMB9 ProteinP28065 (Uniprot-TrEMBL)
PSMC1 ProteinP62191 (Uniprot-TrEMBL)
PSMC2 ProteinP35998 (Uniprot-TrEMBL)
PSMC3 ProteinP17980 (Uniprot-TrEMBL)
PSMC4 ProteinP43686 (Uniprot-TrEMBL)
PSMC5 ProteinP62195 (Uniprot-TrEMBL)
PSMC6 ProteinP62333 (Uniprot-TrEMBL)
PSMD1 ProteinQ99460 (Uniprot-TrEMBL)
PSMD10 ProteinO75832 (Uniprot-TrEMBL)
PSMD11 ProteinO00231 (Uniprot-TrEMBL)
PSMD12 ProteinO00232 (Uniprot-TrEMBL)
PSMD13 ProteinQ9UNM6 (Uniprot-TrEMBL)
PSMD14 ProteinO00487 (Uniprot-TrEMBL)
PSMD2 ProteinQ13200 (Uniprot-TrEMBL)
PSMD3 ProteinO43242 (Uniprot-TrEMBL)
PSMD4 ProteinP55036 (Uniprot-TrEMBL)
PSMD5 ProteinQ16401 (Uniprot-TrEMBL)
PSMD6 ProteinQ15008 (Uniprot-TrEMBL)
PSMD7 ProteinP51665 (Uniprot-TrEMBL)
PSMD8 ProteinP48556 (Uniprot-TrEMBL)
PSMD9 ProteinO00233 (Uniprot-TrEMBL)
PSME1 ProteinQ06323 (Uniprot-TrEMBL)
PSME2 ProteinQ9UL46 (Uniprot-TrEMBL)
PSME3 ProteinP61289 (Uniprot-TrEMBL)
PSME4 ProteinQ14997 (Uniprot-TrEMBL)
PSMF1 ProteinQ92530 (Uniprot-TrEMBL)
PTCH1 ProteinQ13635 (Uniprot-TrEMBL)
PTCH1 gene ProteinENSG00000185920 (Ensembl)
PTCH1 geneGeneProductENSG00000185920 (Ensembl)
PTCH1:SMURFComplexR-HSA-5632594 (Reactome)
PTCH1ProteinQ13635 (Uniprot-TrEMBL)
PTCH2 gene ProteinENSG00000117425 (Ensembl)
RBX1 ProteinP62877 (Uniprot-TrEMBL)
RPS27A(1-76) ProteinP62979 (Uniprot-TrEMBL)
SHFM1 ProteinP60896 (Uniprot-TrEMBL)
SHH(34-?) ProteinQ15465 (Uniprot-TrEMBL)
SMO ProteinQ99835 (Uniprot-TrEMBL)
SMO dimer:ARRB:KIF3AComplexR-HSA-5632599 (Reactome)
SMO dimer:CSNK1A1ComplexR-HSA-5632602 (Reactome)
SMO dimerComplexR-HSA-5610574 (Reactome)
SMO dimerComplexR-HSA-5632597 (Reactome)
SMURF1 ProteinQ9HCE7 (Uniprot-TrEMBL)
SMURF2 ProteinQ9HAU4 (Uniprot-TrEMBL)
SMURFComplexR-HSA-173533 (Reactome)
SPOP ProteinO43791 (Uniprot-TrEMBL)
SPOP:CUL3:RBX1ComplexR-HSA-5635071 (Reactome)
SPOPL ProteinQ6IQ16 (Uniprot-TrEMBL)
SUFU ProteinQ9UMX1 (Uniprot-TrEMBL)
SUFUProteinQ9UMX1 (Uniprot-TrEMBL)
UBA52(1-76) ProteinP62987 (Uniprot-TrEMBL)
UBB(1-76) ProteinP0CG47 (Uniprot-TrEMBL)
UBB(153-228) ProteinP0CG47 (Uniprot-TrEMBL)
UBB(77-152) ProteinP0CG47 (Uniprot-TrEMBL)
UBC(1-76) ProteinP0CG48 (Uniprot-TrEMBL)
UBC(153-228) ProteinP0CG48 (Uniprot-TrEMBL)
UBC(229-304) ProteinP0CG48 (Uniprot-TrEMBL)
UBC(305-380) ProteinP0CG48 (Uniprot-TrEMBL)
UBC(381-456) ProteinP0CG48 (Uniprot-TrEMBL)
UBC(457-532) ProteinP0CG48 (Uniprot-TrEMBL)
UBC(533-608) ProteinP0CG48 (Uniprot-TrEMBL)
UBC(609-684) ProteinP0CG48 (Uniprot-TrEMBL)
UBC(77-152) ProteinP0CG48 (Uniprot-TrEMBL)
ULK3 ProteinQ6PHR2 (Uniprot-TrEMBL)
ULK3:SUFUComplexR-HSA-5635073 (Reactome)
ULK3ProteinQ6PHR2 (Uniprot-TrEMBL)
UbComplexR-HSA-113595 (Reactome)
UbComplexR-HSA-68524 (Reactome)
p-GLI1 ProteinP08151 (Uniprot-TrEMBL)
p-GLI1,2,3ComplexR-HSA-5635089 (Reactome)
p-GLI1,2,3ComplexR-HSA-5635090 (Reactome)
p-GLI2 ProteinP10070 (Uniprot-TrEMBL)
p-GLI3 ProteinP10071 (Uniprot-TrEMBL)
p6S,

T-SMO

dimer:CSNK1A1:ADRBK1
ComplexR-HSA-5632615 (Reactome)
p6S, T-SMO dimer:EVC2:EVCComplexR-HSA-5633039 (Reactome)
p6S, T-SMO dimerComplexR-HSA-5632614 (Reactome)
pS588,

S590, T593, S595-SMO

dimer:CSNK1A1:ADRBK1
ComplexR-HSA-5632622 (Reactome)
pS588, S590, T593, S595, S611, S615, S616-SMO ProteinQ99835 (Uniprot-TrEMBL)
pS588, S590, T593, S595-SMO ProteinQ99835 (Uniprot-TrEMBL)
pS588,S590, T593,

S595-SMO

dimer:CSNK1A1
ComplexR-HSA-5632624 (Reactome)
ub-2p-GLI2 ProteinP10070 (Uniprot-TrEMBL)
ub-2p-GLI2,3:SPOP:CUL3:RBX1ComplexR-HSA-5635095 (Reactome)
ub-2p-GLI3 ProteinP10071 (Uniprot-TrEMBL)
ub-GLI1 ProteinP08151 (Uniprot-TrEMBL)
ub-GLI1:NUMB:ITCHComplexR-HSA-5635836 (Reactome)
ub-PTCH1 ProteinQ13635 (Uniprot-TrEMBL)
ub-PTCH1:SMURFComplexR-HSA-5632582 (Reactome)
ub-PTCH1ProteinQ13635 (Uniprot-TrEMBL)
unknown kinaseR-HSA-5635063 (Reactome)

Annotated Interactions

View all...
SourceTargetTypeDatabase referenceComment
26S proteasomemim-catalysisR-HSA-5635854 (Reactome)
26S proteasomemim-catalysisR-HSA-5635868 (Reactome)
2p-GLI1,2,3ArrowR-HSA-5635841 (Reactome)
2p-GLI1,2,3R-HSA-5635845 (Reactome)
2p-GLI1,2,3R-HSA-5635846 (Reactome)
2p-GLI1,2,3R-HSA-5635848 (Reactome)
2p-GLI1:HHIP

gene,PTCH2 gene,BOC

gene
ArrowR-HSA-5635850 (Reactome)
2p-GLI1R-HSA-5635850 (Reactome)
2p-GLI2,3R-HSA-5635855 (Reactome)
2p-GLI:GLI1 geneArrowR-HSA-5635846 (Reactome)
2p-GLI:GLI1 geneArrowR-HSA-5635853 (Reactome)
2p-GLI:PTCH1 geneArrowR-HSA-5635848 (Reactome)
2p-GLI:SPOP:CUL3:RBX1ArrowR-HSA-5635855 (Reactome)
2p-GLI:SPOP:CUL3:RBX1R-HSA-5635856 (Reactome)
2p-GLI:SPOP:CUL3:RBX1mim-catalysisR-HSA-5635856 (Reactome)
ADPArrowR-HSA-5632670 (Reactome)
ADPArrowR-HSA-5632672 (Reactome)
ADPArrowR-HSA-5635841 (Reactome)
ADPArrowR-HSA-5635842 (Reactome)
ADRBK1ArrowR-HSA-5633040 (Reactome)
ADRBK1R-HSA-5632674 (Reactome)
ARRBR-HSA-5632667 (Reactome)
ATPR-HSA-5632670 (Reactome)
ATPR-HSA-5632672 (Reactome)
ATPR-HSA-5635841 (Reactome)
ATPR-HSA-5635842 (Reactome)
ArrowR-HSA-5632668 (Reactome)
BOC:PTCH1R-HSA-5632653 (Reactome)
CDC73:2p-GLIArrowR-HSA-5635845 (Reactome)
CDC73R-HSA-5635845 (Reactome)
CDONR-HSA-5632652 (Reactome)
CSNK1A1ArrowR-HSA-5633040 (Reactome)
CSNK1A1R-HSA-5632671 (Reactome)
DZIP1ArrowR-HSA-5635855 (Reactome)
EFCAB7:IQCER-HSA-5633051 (Reactome)
EVC2:EVCR-HSA-5632679 (Reactome)
EVC2:EVCR-HSA-5633051 (Reactome)
GAS1R-HSA-5632649 (Reactome)
GAS8ArrowR-HSA-5632668 (Reactome)
GLI1 geneR-HSA-5635846 (Reactome)
GLI1 geneR-HSA-5635853 (Reactome)
GLI1,2,3ArrowR-HSA-5635859 (Reactome)
GLI1,2,3R-HSA-5610723 (Reactome)
GLI1,2,3R-HSA-5635842 (Reactome)
GLI1:NUMB:ITCHArrowR-HSA-5635861 (Reactome)
GLI1:NUMB:ITCHR-HSA-5635864 (Reactome)
GLI1:NUMB:ITCHmim-catalysisR-HSA-5635864 (Reactome)
GLI1ArrowR-HSA-5635853 (Reactome)
GLI1R-HSA-5635861 (Reactome)
GLI:SUFUArrowR-HSA-5610723 (Reactome)
GLI:SUFUArrowR-HSA-5635860 (Reactome)
GLI:SUFUR-HSA-5635859 (Reactome)
GLI:SUFUR-HSA-5635860 (Reactome)
GPR161ArrowR-HSA-5635102 (Reactome)
GPR161R-HSA-5635102 (Reactome)
HHIP gene,PTCH2 gene,BOC geneR-HSA-5635850 (Reactome)
HHIPR-HSA-445448 (Reactome)
Hh-Npp:BOC:PTCH1ArrowR-HSA-5632653 (Reactome)
Hh-Npp:CDON:PTCHArrowR-HSA-5632652 (Reactome)
Hh-Npp:GAS1:PTCHArrowR-HSA-5632649 (Reactome)
Hh-Npp:HHIPArrowR-HSA-445448 (Reactome)
Hh-NppArrowR-HSA-5632646 (Reactome)
Hh-NppR-HSA-445448 (Reactome)
Hh-NppR-HSA-5632649 (Reactome)
Hh-NppR-HSA-5632652 (Reactome)
Hh-NppR-HSA-5632653 (Reactome)
IQCE:EFCAB7:EVC2:EVCArrowR-HSA-5633051 (Reactome)
ITCHR-HSA-5610735 (Reactome)
KIF3AR-HSA-5632667 (Reactome)
KIF7ArrowR-HSA-5635860 (Reactome)
NUMB:ITCHArrowR-HSA-5610735 (Reactome)
NUMB:ITCHArrowR-HSA-5635868 (Reactome)
NUMB:ITCHR-HSA-5635861 (Reactome)
NUMBR-HSA-5610735 (Reactome)
PTCH1 geneR-HSA-5635848 (Reactome)
PTCH1:SMURFArrowR-HSA-5632646 (Reactome)
PTCH1:SMURFR-HSA-5632648 (Reactome)
PTCH1:SMURFmim-catalysisR-HSA-5632648 (Reactome)
PTCH1R-HSA-5632646 (Reactome)
PTCH1R-HSA-5632649 (Reactome)
PTCH1R-HSA-5632652 (Reactome)
R-HSA-445448 (Reactome) HHIP is a Hh-binding transmembrane protein that antagonizes Hh signaling by sequestering the ligand away from PTCH. HHIP is also a downstream target gene of Hh signaling, establishing a negative feedback loop that limits the extent of signaling (Chuang et al, 1999; Chuang et al, 2003; Bosanac et al, 2009; Bishop et al, 2009: Holtz et al, 2013). HHIP binds to all three Hh ligands, and also exists in a secreted form, which also sequesters ligand (Chuang et al, 1999; Coulombe et al, 2004). HHIP expression is altered in some cancers that show upregulated Hh signaling (Olsen et al, 2004; Tada et al, 2008; Tojo et al, 2002).
R-HSA-5610723 (Reactome) Vertebrate SUFU plays a critical role in the negative regulation of Hh signaling in the absence of ligand. Disruption of SUFU causes constitutive activation of the pathway, and is associated with the development of medulloblastoma in humans (Cooper et al, 2005; Svard et al, 2006; Taylor et al, 2002; Pastorino et al, 2009). SUFU binds directly to all three GLI proteins (Pearse et al, 1999; Stone et al, 1999; Jia et al, 2009; Svard et al, 2006). Formation of a SUFU:GLI complex is required for the processing of GLI3 to the GLI3R repressor form, and the processing depends on transit through the primary cilia (Kise et al, 2009; Humke et al, 2010; Huangfu and Anderson, 2005). Despite this, primary cilia are not required for SUFU to inhibit GLI activity; SUFU may also serve in a cilia-independent manner to sequester the full-length protein in the cytoplasm in the absence of Hh signal (Chen et al, 2009; Humke et al, 2010; Jia et al, 2009; Tukachinsky et al, 2010). After processing, GLI3R dissociates from SUFU and its activity is SUFU-independent (Humke et al, 2010; Tukachinsky et al, 2010). Nuclear SUFU may also play a direct role as a transcriptional co-repressor through interaction with the N-terminal DNA-binding domain of GLI proteins, though this remains to be fully elaborated (Monnier et al, 1998; Pearse et al, 1999; Cheng and Bishop, 2002; Paces-Fessy et al, 2004; Dunaeva et al, 2003; Szczepny et al, 2014).
R-HSA-5610735 (Reactome) NUMB is a negative regulator of Hh signaling that acts by promoting the ITCH-dependent ubiquitination of GLI1. ITCH is an E3 ligase that is kept in an inactive conformation by an intramolecular interaction between the HECT domain and a WW motif. Binding of the adaptor protein NUMB to the WW region of ITCH displaces the HECT domain and promotes the catalytic activity of the E3 ligase (di Marcotullio et al, 2006; 2011).
R-HSA-5632646 (Reactome) Hh stimulation promotes PTCH1 clearance from the primary cilium to endocytic compartments (Rohatgi et al, 2007; reviewed in Nowaza et al, 2013). Receptor internalization is required for pathway activation, and additionally limits the duration and range of Hh signaling by sequestering the ligand inside the cell (Rohatgi et al, 2007; Incardona et al, 2000; Incardona et al, 2002; Denef et al, 2000; Huang et al, 2013; Yue et al, 2014). Upon Hh pathway activation, the E3 ligases SMURF1 and SMURF2 bind to two PPXY motifs in the C-terminal tail of PTCH1 to promote its ubiquination, endocytosis and degradation. In Drosophila, SMURF-mediated ubiquitination of PTCH is depends on an interaction between SMURF and activated SMO, but this does not appear to be true in vertebrates where PTCH1 turnover is SMO-independent (Yue et al, 2014; Huang et al, 2013; Lu et al, 2006). In flies, SMURF-dependent ubiquitination preferentially downregulates ligand-unbound receptor and is thus believed to regulate downstream signaling by altering the ratio of bound to unbound receptor on the cell surface; this aspect of PTCH1 downregulation has not been examined in detail in vertebrate cells (Huang et al, 2013; Casali and Struhl, 2004; Yue et al, 2014).
R-HSA-5632648 (Reactome) SMURF 1 and 2 are required in a redundant manner for the ligand-dependent ubiquitination of the C-terminal tail of PTCH. Ubiquitination is required for PTCH1 clearance from the primary cilium to endocytic compartments for degradation, allowing downstream pathway activation (Rohatgi et al, 2007; Yue et al, 2014; Huang et al, 2013).
R-HSA-5632649 (Reactome) GAS1 is a vertebrate-specific Hh coreceptor that binds directly to Hh ligand to promote signaling (Martinelli and Fan, 2007; McLellan et al, 2008; Izzi et al, 2011; Pineda-Alvarez et al, 2012). GAS1 interacts directly with PTCH as well as BOC and CDON and contributes in an unclearly defined manner to Hh signal transduction (Martinelli and Fan, 2007; Allen et al, 2007; Izzi et al, 2011; Allen et al, 2011; reviewed in Sanchez-Arrones et al, 2012).
R-HSA-5632652 (Reactome) CDON is a transmembrane glycoprotein that binds directly to Hh ligand and is required in conjunction with PTCH, BOC and GAS1 to promote Hh signaling (Tenzen et al, 2006; McLellan et al, 2008; Kavran et al, 2010; Bae et al, 2011; reviewed in Beachy et al, 2010; Sanchez-Arrones et al, 2012). Conserved fibronectin type III repeats in the extracellular region of CDON and BOC are required for interaction with both Hh ligand and the PTCH receptor and also for interactions between BOC, CDON and GAS1 (Okada et al, 2006; Izzi et al, 2011; Bae et al, 2011). The manner in which each of these co-receptors interact and contribute to Hh signaling is not fully elucidated, but knockout of all three is required to abrogate Hh signaling in mice (Allen et al, 2007; Allen et al, 2011; Izzi et al, 2011; reviewed in Sanchez-Arrones et al, 2012).
R-HSA-5632653 (Reactome) Hh pathway activation depends upon the binding of Hh ligand to the PTCH transmembrane receptor (Chen and Struhl, 1996; Marigo et al, 1996; Stone et al, 1996). Ligand binding relieves the PTCH-dependent inhibition of SMO, allowing SMO to concentrate in the primary cilium and promoting the accumulation of the full-length form of the GLI transcriptional proteins (reviewed in Briscoe and Therond, 2013). PTCH also binds constitutively to the transmembrane protein BOC (brother of CDO), one of three vertebrate co-receptors required for Hh signaling in mice (Izzi et al, 2011; Allen et al, 2011; reviewed in Sanchez-Arrones et al, 2012). BOC interacts with PTCH through the first and second of the BOC fibronectin type 3 (FNIII) repeats, and with SHH through the third FNIII repeat, suggesting the formation of a ternary complex in the presence of ligand (Okada et al, 2006; Izzi et al, 2011). Although GAS1 similarly binds to both PTCH and Hh, it is not co-immunoprecipitated with BOC, suggesting the formation of separate receptor:co-receptor complexes (Izzi et al, 2011; Allen et al, 2011; reviewed in Briscoe and Therond, 2013).
R-HSA-5632667 (Reactome) Beta-arrestin 1 and 2 (ARRB1 and 2) and the anterograde motor protein KIF3A bind to SMO and may be required for its ciliary accumulation after Hh stimulation (Kovacs et al, 2008; Barakat et al, 2013).
R-HSA-5632668 (Reactome) Binding of ligand to the PTCH receptor activates the Hh signaling pathway and results in the accumulation of SMO in the primary cilium (Denef et al, 2000; Corbit et al, 2005; Rohatgi et al, 2007; Milenkovic et al, 2009; Wang et al, 2009; Wilson et al, 2009; reviewed in Briscoe and Therond, 2013). Neither the mechanism for how PTCH represses SMO in the absence of ligand nor how this relief is lifted upon pathway activation are fully understood, however SMO translocation to the cilium appears to depend upon complex formation with beta-arrestin proteins and the anterograde motor protein KIF3A (Chen et al, 2004; Kovacs et al, 2008). GAS8, a SMO- and microtubule-binding protein, is also required for the ciliary localization of SMO, although the mechanism is not clear (Evron et al, 2011; reviewed in Evron et al, 2012). In response to pathway activation, SMO is phosphorylated in a CKI- and ADRBK1/GRK2-dependent fashion and undergoes a conformational change, both of which are required for downstream pathway activation; accumulation of SMO in the cilium is in itself not sufficient (Chen et al, 2011; Zhao et al, 2007; Chen et al, 2010; Rohatgi et al, 2009). In the primary cilium, SMO interacts with the Ellis-van Creveld syndrome proteins 1 and 2 (EVC1 and 2) in a SMO phosphorylation-dependent manner, and the interaction with EVC1 and 2 is required for downstream signal propagation (Yang et al, 2012; Dorn et al, 2012; Capparos-Martin et al, 2013; Pusapati et al, 2014; Yang et al, 2012). SMO activation results in the concentration of SUFU and the GLI proteins in the cilium, the dissociation of the SUFU:GLI complex and the nuclear accumulation of the full length activator form of the GLI proteins (reviewed in Briscoe and Therond, 2013).
R-HSA-5632670 (Reactome) Initial activation of SMO in response to HH occurs with the CSNK1A1-mediated phosphorylation of serine and threonine residues in the C-terminal tail. While many potential CSNK1A1 target residues have been identified in in vitro assays, residues S588, S590, T593 and S595 in the S0 region appear to be the most critical for function (Chen et al, 2011). Initial phosphorylation increases the affinity of the C-terminal tail for both CSNK1A1 and ADRBK1/GRK2, establishing a positive feedback mechanism that promotes further phosphorylation. CSNK1A1 and ADRBK1-mediated phosphorylation is thought to promote an open, activated conformation of the C-terminal tails, analogous to that in Drosophila Smo upon pathway activation (Chen et al, 2011; Chen et al, 2010; Zhao et al, 2007).
R-HSA-5632671 (Reactome) Activation of SMO in vertebrate cells depends upon its sequential phosphorylation by CSNK1A1/CK1alpha and ADRBK1/GRK2 kinases. Phosphorylation is thought to promote a conformational change in the SMO C-terminal tails, destabilizing an intramolecular interaction within the tail and promoting a more open conformation that brings the two tails of the SMO dimer into closer proximity (Chen et al, 2010; Chen et al, 2011; Wilson et al, 2009). This mechanism parallels the activation of Smo in Drosophila, where phosphorylation of consensus PKA and CK1 sites in the C-terminus promotes conformational change (Zhao et al, 2007). In both Drosophila and vertebrates, the kinases interact with SMO as assessed by co-precipitation (Zhao et al, 2007; Chen et al, 2010; Chen et al, 2011). In vertebrate cells, SHH stimulation appears to promote a 2-step activation of SMO. In the first step, CSNK1A1 binds to the C-terminal tails in the closed conformation. Initial CSNK1A1-mediated phosphorylation promotes the open conformation and increases the binding affinity of both CSNK1A1 and ADRBK1/GRK2 for the SMO tail, establishing a positive feedback loop to enhance SMO phosphorylation (Chen et al, 2010; Chen et al, 2011; Meloni et al 2006; Philipp et al, 2008). CSNK1A1 accumulates in the primary cilium in an SHH-dependent manner, and the kinetics of SMO phosphorylation are faster there than in the whole cell. Phosphorylation also depends on the kinesin II ciliary motor KIF3A, and promotes the ciliary accumulation of SMO, possibly in a ARRB-dependent manner (Chen et al, 2011; Meloni et al, 2006).
R-HSA-5632672 (Reactome) ADRBK1 phosphorylates the SMO C-terminal tail after initial phosphorylation by CSNK1A1. Phosphorylation promotes an open, activated conformation of the C-terminal tails, allowing an intramolecular interaction between tails of adjacent monomers in the SMO dimer. This Hh-dependent conformational change is required for downstream signal propagation (Chen et al, 2011; Chen et al, 2010; Zhao et al, 2007; Meloni et al, 2006; Philipp et al, 2008; reviewed in Briscoe and Therond, 2013). In Drosophila, Smo C-terminal tail phosphorylation promotes an association with the Hedgehog signaling complex (HSC) through interaction with the scaffolding kinesin-2 like protein Cos2, and ultimately results in the release of full-length Ci from the complex (Zhang et al, 2005; Ogden et al, 2003; Lum et al, 2003; reviewed in Mukhopadhyay and Rohatgi, 2014). How Hh signal is transmitted from activated SMO to downstream components in vertebrate cells is not fully established
R-HSA-5632674 (Reactome) Initial binding and phosphorylation of the SMO C-terminal tail by CSNK1A1 increases the affinity of the tail for ADRBK1/GRK2. Like CSNK1A1, ADRBK1 phosphorylates multiple sites in the SMO tail in a Hh-dependent manner, and this phosphorylation is required for a conformational change that promotes closer association of the two tails in the SMO dimer, analogous to what is seen in Drosophila (Chen et al, 2011; Chen et al, 2010; Zhao et al, 2007; Meloni et al, 2006; Philipp et al, 2008).
R-HSA-5632677 (Reactome) After SMURF-dependent ubiquitination, PTCH1 is internalized to endocytic vesicles for degradation (Rohatgi et al, 2007; Huang et al, 2013; Yue et al, 2014). PTCH1 and SMO show reciprocal changes in localization upon Hh pathway activation, with PTCH moving from the primary cilium to internal vesicles while SMO becomes enriched in the primary cilium after ligand binding (Denef et al, 2000; Rohatgi et al, 2007; Corbit et al, 2005; Kovacs et al, 2008; reviewed in Goetz and Anderson). In mice, internalization of PTCH1 appears to be independent of SMO, while in flies, activated SMO is required to promote the SMURF-dependent downregulation of PTCH (Yue et al, 2014; Huang et al, 2013).
R-HSA-5632679 (Reactome) EVC2 and EVC are components of a complex that localizes to the base of the cilium in a so-called EvC zone just distal to the transition zone. Mutations in the genes for EVC2 and EVC are associated with the ciliopathy Ellis van Creveld syndrome and result in an abrogated response to stimulation by Hh, making EVC2 and EVC positive regulators of Hh signaling (Blair et al, 2011; Dorn et al, 2012; Caparros-Martin et al, 2013). The EVC2:EVC complex interacts with SMO in the cilium after Hh stimulation and restricts SMO localization to the EvC zone (Dorn et al, 2012; Yang et al, 2012; Caparros-Martin et al, 2013). Disruption of the EVC2:EVC complex does not interfere with SMO ciliary localization or its activation by CSNK1A1 and ADRBK1, but prevents the Hh-dependent localization of the GLI transcription factors to the tip of the cilium and abrogates the dissociation of the GLI:SUFU complex (Dorn et al, 2012; Yang et al, 2012; Caparros-Martin et al, 2013). These events are required for the activation of the GLI transcription factors in response to ligand stimulation. Localization of the EVC2:EVC complex to the EVC zone depends on an interaction between the EVC2 W peptide (a stretch of 43 amino-acids in the C-terminal tail that is missing in a disease associated EVC2-variant), and the IQCE:EFCAB7 complex. Abrogation of this interaction causes the EVC2:EVC complex to localize along the length of the cilium and disrupts production and nuclear translocation of the full length GLI2 transcriptional activator (Pusapati et al, 2014). How the Hh signal is transmitted from the SMO:EVC2:EVC complex to downstream components is not known.
R-HSA-5633040 (Reactome) After phosphorylating the SMO dimer, CSNK1A1 and ADRBK1 presumably dissociate, although this has not been demonstrated explicitly (Chen et al, 2011).
R-HSA-5633051 (Reactome) IQCE and EFCAB7 are ciliary proteins that are required to restrict the EVC2:EVC complex to the 'EVC region' at the base of the cilium, just distal to the transition zone (Pusapati et al, 2014). EVC2 and EVC are transmembrane proteins that form a ciliary-localized complex that is a positive regulator of Hh signal transduction. The EVC2:EVC complex appears to act downstream of both SMO ciliary localization and its activation by CSNK1A1 and ADRBK1, and is required for the dissociation of the GLI:SUFU complex at the ciliary tip, although the mechanism for this is not known (Blair et al, 2011; Dorn et al, 2012; Capparos-Martin et al, 2013; Pusapati et al, 2014). EVC2 interacts with the IQCE:EFCAB7 subcomplex through the so called 'W-peptide', a stretch of amino acids in the intracellular tail that is deleted in the ciliopathy Weyers Acrofacial Dysostosis. Deletion of the W-peptide results in mislocalization of EVC2 throughout the length of the cilium, rather than being concentrated in the 'EVC zone' (Pusapati et al, 2014; Dorn et al, 2012; Capparos-Martin et al, 2011). EVC2:EVC localization to the EVC region, mediated by the IQCE:EFCAB7 complex and the W-peptide, is required for the Hh-dependent activation of full-length GLI2, but does not appear to critical for the regulation of GLI3R levels, suggesting a bifurcation of the pathway (Pusapati et al, 2014).
R-HSA-5635102 (Reactome) Hh signaling promotes the removal of the orphan G protein coupled receptor GPR161 from the cilium (Rohatgi et al, 2007). GPR161 is a negative regulator of Hh signaling that is recruited to the cilium through interaction with TULP3 (Mukhopadhyay et al, 2010; Mukhopadhyay et al, 2013). GPR161 thought to act by locally increasing the cAMP levels, promoting PKA activity and thereby favouring the production of the repressor form of the GLI proteins in the absence of Hh ligand. Consistent with this, deletion of GPR161 results in ectopic pathway activation (Mukhopadhyay et al, 2013). The decrease in PKA activity in the cilium after clearance of GPR161 from the ciliary membrane may contribute to the dissociation of the GLI:SUFU complex upon pathway activation, although this remains to formally demonstrated (Humke et al, 2010; Tukachinsky et al, 2010; reviewed in Mukhopadhyay et al, 2014).
R-HSA-5635839 (Reactome) ULK3 is a serine-threonine kinase that was identified as a positive regulator of Hh signaling that regulates GLI activity by phosphorylating the full-length form (Maloverjan et al, 2010a). In the absence of Hh ligand, ULK3 forms a complex with SUFU that restricts its kinase activity (Maloverjan et al, 2010b). Upon Hh stimulation, the ULK3:SUFU complex dissociates, allowing ULK3 to phosphorylate the full-length GLI proteins and promoting their activation and nuclear localization (Maloverjan et al, 2010a; Maloverjan et al, 2010b). ULK3 is related by sequence to the vertebrate kinase STK36, homologue to Drosophila Fused (Fu). While Fu plays a critical role in propagating Hh signal and is part of the Hedgehog signaling complex (HSC), STK36 is not required for Hh signaling in vertebrate cells but instead contributes to the formation of motile cilia (Wilson et al, 2009; reviewed in Briscoe and Therond, 2013; Maloverjan and Piirsoo, 2012).
R-HSA-5635841 (Reactome) Hh signaling induces phosphorylation of full-length GLI that coincides with its nuclear localization and transcription factor activity (Humke et al, 2010; reviewed in Hui and Angers, 2011). Although this is depicted as occuring in the nucleus, the identity and location of the kinase(s) is not definitively known, nor is the ordering of the phosphorylation and translocation events (Wen et al, 2010; Humke et al, 2010; reviewed in Hui and Angers, 2011). Both cytoplasmic/ciliary and nuclear full-length GLI proteins are likely subject to phosphorylation, and the interaction between the numerous regulatory events is not clear. CDC2L1 was identified as a kinase that positively regulates Hh pathway activity, and it was shown to bind SUFU and promote the dissociation of the GLI1:SUFU complex in a kinase-dependent manner in mouse, but it has not been implicated in the phosphorylation of the GLI transcription factors themselves (Evangelista et al, 2008). ULK3 is another kinase that positively regulates Hh signaling and has been proposed to phosphorylate GLI proteins to promote their transcriptional activity (Maloverjan et al, 2010a; Maloverjan et al, 2010b; reviewed in Maloverjan and Piirsoo, 2012). DYRK family kinases are also implicated in the post-transcriptional regulation of the GLI proteins in both a positive and a negative manner (Mao et al, 2002; Lauth et al, 2010; Varjosalo et al, 2008).
Once in the nucleus, phosphorylated GLI transcription factors bind to promoters of Hh-responsive genes such as PTCH1, PTCH2, GLI1 and HHIP to activate transcription (Vokes et al, 2007; Vokes et al 2007; Lee et al, 2010; reviewed in Briscoe and Therond, 2013). The full-length transcriptionally active GLI proteins are labile and subject to SPOP-dependent proteolysis (Chen et al, 2009; Zhang et al, 2009; Wen et al, 2010).
R-HSA-5635842 (Reactome) Dissociation from SUFU allows the STK36/dFu homologue ULK3 to phosphorylate full-length GLI proteins. Phosphorylation promotes the nuclear translocation of the proteins and stimulates the transcription factor activity as assessed by a GLI-responsive reporter gene. In vitro, ULK3 phosphorylates GLI2 with the highest efficiency, but the kinase is also able to phosphorylate GLI1 and GLI3 (Maloverjan et al, 2010a; Maloverjan et al, 2010b). ULK3 is only one of a number of kinases that have been implicated in the regulation of GLI proteins in response to pathway stimulation, and how all the putative regulators interact to control GLI transcriptional activity remains to be elucidated (Evangelista et al, 2008; Mao et al, 2002; Varjosalo et al, 2008; reviewed in Marjosalo and Piirsoo, 2012).
R-HSA-5635843 (Reactome) Activation of SMO downstream of Hh ligand binding results in the dissociation of the SUFU:GLI complex and the translocation of the full-length GLI proteins to the nucleus where it is converted to a short-lived transcriptionally active form (Pan et al, 2006; Kim et al, 2009; Wen et al, 2010; Humke et al, 2010; Tukachinsky et al, 2010; reviewed in Briscoe and Therond, 2013).
R-HSA-5635845 (Reactome) Each of the GLI proteins can form a complex in the nucleus with CDC73, also known as Parafibromin, a component of the PAF complex (Mosimann et al, 2009). PAF1 is a conserved protein complex that affects aspects of RNA polymerase II transcription including histone modification, transcription elongation and RNA 3' end formation, among others. In humans, the PAF1 complex consists of CDC73, PAF1, LEO1, CTR9, RTF1 and WDR61 (reviewed in Tomson and Arndt, 2013). Knockdown of CDC73 in mammalian cell culture compromises GLI1- and GLI2-dependent transcriptional activation and has been shown to abrogate expression of endogenous targets in Drosophila. CDC73 interacts with the GLI proteins through the SUFU-interacting domain in region 1 of the N-terminal (Mosimann et al, 2009). Direct binding of a CDC73:GLI complex on an endogenous human target gene has not yet been demonstrated.
R-HSA-5635846 (Reactome) GLI1 is a direct target of the GLI transcription factors and its expression is absolutely dependent on Hh pathway activation (Dai et al, 1999; Bai et al, 2002; Bai et al, 2004; Vokes et al, 2007; Vokes et al, 2008; Lee et al, 2010). GLI1 is an obligate transcriptional activator and its expression downstream of Hh stimulation establishes a positive feedback loop (reviewed in Briscoe and Therond, 2013).
R-HSA-5635848 (Reactome) PTCH1 has been identified as a Hh-responsive target in a number of genome-wide ChIP-based screens and each of the GLI proteins enhances transcription through a consensus GLI-binding site in a ligand-dependent manner (Vokes et al, 2007; Vokes et al, 2008; Lee et al, 2010; Agren et al, 2004). Expression of PTCH1 in response to Hh stimulation establishes a negative feedback loop that limits the duration of pathway activation (reviewed in Hui and Angers, 2011).
R-HSA-5635850 (Reactome) Genome-wide ChIP studies have identified Hh pathway members HHIP, PTCH2 and BOC as direct targets of GLI1 downstream of pathway activation (Vokes et al, 2007; Vokes et al, 2008; Lee et al, 2010).
R-HSA-5635853 (Reactome) GLI1 expression is promoted by the binding of the full-length GLI transcription factors to consensus GLI sites in the promoter in response to Hh signaling (Dai et al, 1999; Bai et al, 2002; Bai et al, 2004; Vokes et al, 2007; Vokes et al, 2008; Lee et al, 2010).
R-HSA-5635854 (Reactome) SPOP:CUL3:RBX1-mediated ubiquitination of the transcriptionally active GLI proteins attenuates Hh-dependent signaling by promoting their degradation by the proteasome (Zhang et al, 2009; Chen et al, 2009; Humke et al, 2010; Tukachinsky et al, 2010; Wen et al, 2010).
R-HSA-5635855 (Reactome) Full-length GLI proteins are labile transcription factors that are rapidly degraded after ubiquitination by the SPOP:CUL3:RBX1 E3 ligase (Ohlmeyer et al, 1998; Humke et al, 2010; Tukachinsky et al, 2010; Chen et al, 2009; Zhang et al, 2009; Wen et al, 2010). SPOP (Speckle-type POZ protein) is the vertebrate homologue of Drosophila Hib/Roadkill, which was identified as a negative regulator of Hh signaling (Ohlmeyer et al, 1998; Zhang et al, 2006; Kent et al, 2006). SPOP/Hib proteins contain BTB and MATH domains and function as the substrate-binding component of the E3 ligase complex, where they promote oligomerization (Zhang et al, 2009; Furukawa et al, 2003; Zhuang et al, 2009). SPOP has been shown to bind to GLI2 and GLI3 through multiple serine and threonine rich motifs in the transcription factors, but direct binding to GLI1 has not been demonstrated (Cheng et al, 2009; Zhang et al, 2009).
The stability of SPOP itself is regulated in an unknown manner by DZIP1, a regulator of Hh signaling best characterized in zebrafish for its positive role in promoting ciliogenesis (Sekimizu et al, 2004; Wolff et al, 2004; Glazer et al, 2010; Kim et al, 2010; Tay et al, 2010; Wang et al, 2013). More recently, DZIP1 has also been shown to act as a negative regulator of Hh signaling by preventing the ubiquitin- and proteasome-dependent degradation of SPOP, and in this way increasing the turnover of activated GLI proteins (Jin et al, 2011; Schwend et al, 2013).
R-HSA-5635856 (Reactome) The transcriptional activity of full-length activated Ci/GLI proteins is restricted by their rapid ubiquitin-mediated degradation after initiation of Hh signaling (Ohlmeyer et al, 1998; Humke et al, 2010; Tukachinsky et al, 2010; Wen et al, 2010). Ubiquitination of Ci, GLI2 and GLI3 is mediated by the E3 ligase complex SPOP:CUL3:RBX1, which ubiquitinates the transcription factors in a Hh-dependent manner (Zhang et al, 2006; Kent et al, 2006; Zhang et al, 2009; Chen et al, 2009).
R-HSA-5635859 (Reactome) Hh signaling promotes the dissociation of the GLI:SUFU complex in the cilium downstream of SMO activation (Humke et al, 2010; Tukachinsky et al, 2010). This appears to divert the transcription factors away from the partial processing/degradation pathway and allow the full-length forms to translocate to the nucleus where they are converted to labile transcriptional activators (Humke et al, 2010; Tukachinsky et al, 2010; Pan et al, 2006; Kim et al, 2009). How the Hh signal is transmited from SMO to promote the dissociation of the GLI:SUFU complex is not clear, however it may involve changes in PKA activity as a result of lowered cAMP levels upon pathway stimulation. (Tukachinsky et al, 2010; Wen et al, 2010; Tuson et al, 2011; Barzi et al, 2010; reviewed in Briscoe and Therond, 2013). GPR161, which localizes to the cilium in a TULP3-dependent manner and which increases cAMP levels in the absence of ligand, is cleared from the cilium upon pathway activation, and deletion of GPR161 increases Hh-dependent signaling (Mukhopadhyay et al, 2010; Mukhopadhyay et al, 2013). These data suggest that removal of ciliary GPR161 upon Hh stimulation may contribute to pathway activity by downregulating PKA activity through cAMP levels (reviewed in Mukhopadhyay and Rohatgi, 2014).
R-HSA-5635860 (Reactome) Activation of the Hh pathway causes the GLI:SUFU complex to concentrate in the primary cilium (Humke et al, 2010; Tukachinsky et al, 2010; Kim et al, 2009). The net movement of the GLI:SUFU complex into the cilium occurs downstream of SMO phosphorylation and activation, and requires the Cos2 homologue KIF7, but how the signal is transmitted from the SMO:EVC complex is not clear (Chen et al, 2009; Chen et al, 2010; Pusapati et al, 2013; Endoh-Yamagami et al, 2009; Liem et al, 2009; Cheung et al, 2009). SUFU appears to be a major regulator of the ratio of full length:repressor forms of GLI proteins in vertebrate cells, and the GLI:SUFU interaction is required for the production of GLIR. Dissociation of the GLI:SUFU complex after ligand stimulation diverts GLI from the degradation pathway and allows the full-length form to be activated (Humke et al, 2010; Tukachinsky et al, 2010; Pan et al, 2006; Kim et al, 209; Wen et al, 2010; Chen et al, 2009; reviewed in Briscoe and Therond, 2013). This represents another major point of divergence between the fly and the vertebrate Hh pathways. In Drosophila, absence of SUFU has no effect on Hh signaling, and the scaffolding protein Cos2 may play the key inhibitory role (Varjosalo et al, 2006; reviewed in Briscoe and Therond, 2013).
R-HSA-5635861 (Reactome) GLI1 is recruited to the NUMB:ITCH complex through a direct interaction with both proteins. Once recruited, GLI1 is ubiquitinated by ITCH and subsequently degraded by the proteasome. ITCH-mediated degradation of GLI1 does not depend on the Dc or Dn degrons required for interaction with beta-TrCP, but instead relies on a novel PPXYs/pSP degron of GLI1 (di Marcotullio et al, 2006, 2011; Huntzicker et al, 2006).
R-HSA-5635864 (Reactome) GLI1 is ubiquitinated by ITCH and subsequently degraded by the proteasome. ITCH-mediated degradation of GLI1 does not depend on the Dc or Dn degrons required for interaction with beta-TrCP, but instead relies on a novel PPXYs/pSP degron of GLI1 (di Marcotullio et al, 2006, 2011; Huntzicker et al, 2006).
R-HSA-5635865 (Reactome) After ubiquitinating PTCH1, the SMURF E3 ligase presumably dissociates, although this has not been studied in detail (Huang et al, 2013; Yue et al, 2014).
R-HSA-5635868 (Reactome) After NUMB:ITCH-mediated ubiquitination, GLI1 is degraded by the proteasome. This degradation limits the extent and duration of the response to Hh signaling (di Marcotullio et al, 2006; Huntzicker et al, 2006; di Marcotullio et al, 2011).
SMO dimer:ARRB:KIF3AArrowR-HSA-5632667 (Reactome)
SMO dimer:ARRB:KIF3AArrowR-HSA-5632668 (Reactome)
SMO dimer:CSNK1A1ArrowR-HSA-5632671 (Reactome)
SMO dimer:CSNK1A1R-HSA-5632670 (Reactome)
SMO dimer:CSNK1A1mim-catalysisR-HSA-5632670 (Reactome)
SMO dimerArrowR-HSA-5632668 (Reactome)
SMO dimerR-HSA-5632667 (Reactome)
SMO dimerR-HSA-5632668 (Reactome)
SMO dimerR-HSA-5632671 (Reactome)
SMURFArrowR-HSA-5635865 (Reactome)
SMURFR-HSA-5632646 (Reactome)
SPOP:CUL3:RBX1ArrowR-HSA-5635854 (Reactome)
SPOP:CUL3:RBX1R-HSA-5635855 (Reactome)
SUFUArrowR-HSA-5635839 (Reactome)
SUFUArrowR-HSA-5635859 (Reactome)
SUFUR-HSA-5610723 (Reactome)
ULK3:SUFUR-HSA-5635839 (Reactome)
ULK3ArrowR-HSA-5635839 (Reactome)
ULK3mim-catalysisR-HSA-5635842 (Reactome)
UbArrowR-HSA-5635854 (Reactome)
UbArrowR-HSA-5635868 (Reactome)
UbR-HSA-5632648 (Reactome)
UbR-HSA-5635856 (Reactome)
UbR-HSA-5635864 (Reactome)
p-GLI1,2,3ArrowR-HSA-5635842 (Reactome)
p-GLI1,2,3ArrowR-HSA-5635843 (Reactome)
p-GLI1,2,3R-HSA-5635841 (Reactome)
p-GLI1,2,3R-HSA-5635843 (Reactome)
p6S,

T-SMO

dimer:CSNK1A1:ADRBK1
ArrowR-HSA-5632672 (Reactome)
p6S,

T-SMO

dimer:CSNK1A1:ADRBK1
R-HSA-5633040 (Reactome)
p6S, T-SMO dimer:EVC2:EVCArrowR-HSA-5632679 (Reactome)
p6S, T-SMO dimer:EVC2:EVCArrowR-HSA-5635859 (Reactome)
p6S, T-SMO dimerArrowR-HSA-5633040 (Reactome)
p6S, T-SMO dimerR-HSA-5632679 (Reactome)
pS588,

S590, T593, S595-SMO

dimer:CSNK1A1:ADRBK1
ArrowR-HSA-5632674 (Reactome)
pS588,

S590, T593, S595-SMO

dimer:CSNK1A1:ADRBK1
R-HSA-5632672 (Reactome)
pS588,

S590, T593, S595-SMO

dimer:CSNK1A1:ADRBK1
mim-catalysisR-HSA-5632672 (Reactome)
pS588,S590, T593,

S595-SMO

dimer:CSNK1A1
ArrowR-HSA-5632670 (Reactome)
pS588,S590, T593,

S595-SMO

dimer:CSNK1A1
R-HSA-5632674 (Reactome)
ub-2p-GLI2,3:SPOP:CUL3:RBX1ArrowR-HSA-5635856 (Reactome)
ub-2p-GLI2,3:SPOP:CUL3:RBX1R-HSA-5635854 (Reactome)
ub-GLI1:NUMB:ITCHArrowR-HSA-5635864 (Reactome)
ub-GLI1:NUMB:ITCHR-HSA-5635868 (Reactome)
ub-PTCH1:SMURFArrowR-HSA-5632648 (Reactome)
ub-PTCH1:SMURFR-HSA-5635865 (Reactome)
ub-PTCH1ArrowR-HSA-5632677 (Reactome)
ub-PTCH1ArrowR-HSA-5635865 (Reactome)
ub-PTCH1R-HSA-5632677 (Reactome)
unknown kinasemim-catalysisR-HSA-5635841 (Reactome)
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