Patched-1 proapoptotic activity is downregulated by modification of K1413 by the E3 ubiquitin-protein ligase Itchy homolog

Molecular and Cellular Biology

Volumn 34, Issue 20, 2014, Pages 3855-3866

  Chen, Xiaole L ^a   Chinchilla, Pilar ^a,d   Fombonne, Joanna ^b   Ho, Lan ^a   Guix, Catherine ^b   Keen, James H ^a,c   Mehlen, Patrick ^b   Riobo, Natalia A ^a,c  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b UNIVERSITÉ DE LYON   (France)

^c THOMAS JEFFERSON UNIVERSITY   (United States)

^d PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 9; ITCHY HOMOLOG; PROTEIN PATCHED 1; REGULATOR PROTEIN; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR GLI1; UBIQUITIN PROTEIN LIGASE E3; UBIQUITIN PROTEIN LIGASE NEDD4; UNCLASSIFIED DRUG; WW DOMAIN CONTAINING PROTEIN 2; CELL SURFACE RECEPTOR; G PROTEIN COUPLED RECEPTOR; ITCH PROTEIN, HUMAN; LYSINE; PATCHED RECEPTORS; REPRESSOR PROTEIN; SHH PROTEIN, HUMAN; SMO PROTEIN, HUMAN; UBIQUITIN PROTEIN LIGASE; WWP2 PROTEIN, HUMAN;

ANIMAL CELL; APOPTOSIS; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; ENZYME ACTIVATION; ENZYME ACTIVE SITE; GENE MUTATION; GENE SILENCING; HALF LIFE TIME; HUMAN; HUMAN CELL; INTERNALIZATION; MOUSE; NONHUMAN; PROTEIN AGGREGATION; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; TRANSACTIVATION; UBIQUITINATION; ANIMAL; CHEMISTRY; CHLOROCEBUS AETHIOPS; COS 1 CELL LINE; ENDOCYTOSIS; ENZYME SPECIFICITY; HEK293 CELL LINE; METABOLISM; PHYSIOLOGY; PROTEIN TRANSPORT;

ANIMALS; APOPTOSIS; CERCOPITHECUS AETHIOPS; COS CELLS; DOWN-REGULATION; ENDOCYTOSIS; HEDGEHOG PROTEINS; HEK293 CELLS; HUMANS; LYSINE; MICE; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN TRANSPORT; PROTEOLYSIS; RECEPTORS, CELL SURFACE; RECEPTORS, G-PROTEIN-COUPLED; REPRESSOR PROTEINS; SUBSTRATE SPECIFICITY; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 84907153851     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00960-14     Document Type: Article

References (42)

1. Carpenter D, Stone DM, Brush J, Ryan A, Armanini M, Frantz G, Rosenthal A, de Sauvage FJ. 1998. Characterization of two patched receptors for the vertebrate Hedgehog protein family. Proc. Natl. Acad. Sci. U. S. A. 95:13630 -13634. http://dx.doi.org/10.1073/pnas.95.23.13630.
2. Robbins DJ, Fei DL, Riobo NA. 2012. The Hedgehog signal transduction network. Sci. Signal. 5:re6. http://dx.doi.org/10.1126/scisignal.2002906.
3. Yang C, Chen W, Chen Y, Jiang J. 2012. Smoothened transduces Hedgehog signal by forming a complex with Evc/Evc2. Cell Res. 22:1593-1604. http://dx.doi.org/10.1038/cr.2012.134.
4. Gailani MR, Stahle-Backdahl M, Leffell DJ, Glynn M, Zaphiropoulos PG, Pressman C, Unde´n AB, Dean M, Brash DE, Bale AE, Toftga˚rd R. 1996. The role of the human homologue of Drosophila patched in sporadic basal cell carcinomas. Nat. Genet. 14:78-81. http://dx.doi.org/10.1038/ng0996-78.
5. Hahn H, Christiansen J, Wicking C, Zaphiropoulos PG, Chidambaram A, Gerrard B, Vorechovsky I, Bale AE, Toftgard R, Dean M, Wainwright B. 1996. A mammalian Patched homolog is expressed in target tissues of Sonic Hedgehog and maps to a region associated with developmental abnormalities. J. Biol. Chem. 271:12125-12128. http://dx.doi.org/10.1074/jbc.271.21.12125.
6. Johnson RL, Rothman AL, Xie J, Goodrich LV, Bare JW, Bonifas JM, Quinn AG, Myers RM, Cox DR, Epstein EH, Jr, Scott MP. 1996. Human homolog of Patched, a candidate gene for the basal cell nevus syndrome. Science 272:1668 -1671. http://dx.doi.org/10.1126/science.272.5268.1668.
7. Xie J, Johnson RL, Zhang X, Bare JW, Waldman FM, Cogen PH, Menon AG, Warren RS, Chen LC, Scott MP, Epstein EH, Jr. 1997. Mutations of the Patched gene in several types of sporadic extracutaneous tumors. Cancer Res. 57:2369-2372.
8. Goodrich LV, Milenkovic L, Higgins KM, Scott MP. 1997. Altered neural cell fates and medulloblastoma in mouse patched mutants. Science 277:1109-1113. http://dx.doi.org/10.1126/science.277.5329.1109.
9. Belyea B, Kephart JG, Blum J, Kirsch DG, Linardic CM. 2012. Embryonic signaling pathways and rhabdomyosarcoma: contributions to cancer development and opportunities for therapeutic targeting. Sarcoma 2012: 406239. http://dx.doi.org/10.1155/2012/406239.
10. Lee Y, Miller HL, Russell HR, Boyd K, Curran T, McKinnon PJ. 2006. Patched2 modulates tumorigenesis in Patched1 heterozygous mice. Cancer Res. 66:6964-6971. http://dx.doi.org/10.1158/0008-5472.CAN-06-0505.
11. Thibert C, Teillet MA, Lapointe F, Mazelin L, Le Douarin NM, Mehlen P. 2003. Inhibition of neuroepithelial Patched-induced apoptosis by Sonic Hedgehog. Science 301:843- 846. http://dx.doi.org/10.1126/science.1085405.
12. Mille F, Thibert C, Fombonne J, Rama N, Guix C, Hayashi H, Corset V, Reed JC, Mehlen P. 2009. The Patched dependence receptor triggers apoptosis through a DRAL-caspase-9 complex. Nat. Cell Biol. 11:739- 746. http://dx.doi.org/10.1038/ncb1880.
13. Mehlen P. 2003. Patched is a dependence receptor. Med. Sci. (Paris) 19:1062. http://dx.doi.org/10.1051/medsci/200319111062.
14. Chinchilla P, Xiao L, Kazanietz MG, Riobo NA. 2010. Hedgehog proteins activate pro-angiogenic responses in endothelial cells through noncanonical signaling pathways. Cell Cycle 9:570-579. http://dx.doi.org/10.4161/cc.9.3.10591.
15. Brennan D, Chen X, Cheng L, Mahoney M, Riobo NA. 2012. Noncanonical Hedgehog signaling. Vitam. Horm. 88:55-72. http://dx.doi.org/10.1016/B978-0-12-394622-5.00003-1.
16. Nieuwenhuis E, Barnfield PC, Makino S, Hui CC. 2007. Epidermal hyperplasia and expansion of the interfollicular stem cell compartment in mutant mice with a C-terminal truncation of Patched1. Dev. Biol. 308: 547-560. http://dx.doi.org/10.1016/j.ydbio.2007.06.016.
17. Makino S, Masuya H, Ishijima J, Yada Y, Shiroishi T. 2001. A spontaneous mouse mutation, mesenchymal dysplasia (mes), is caused by a deletion of the most C-terminal cytoplasmic domain of Patched (Ptc). Dev. Biol. 239:95-106. http://dx.doi.org/10.1006/dbio.2001.0419.
18. Acconcia F, Sigismund S, Polo S. 2009. Ubiquitin in trafficking: the network at work. Exp. Cell Res. 315:1610-1618. http://dx.doi.org/10.1016/j.yexcr.2008.10.014.
19. Metzger MB, Hristova VA, Weissman AM. 2012. HECT and RING finger families of E3 ubiquitin ligases at a glance. J. Cell Sci. 125:531-537. http://dx.doi.org/10.1242/jcs.091777.
20. Rotin D, Kumar S. 2009. Physiological functions of the HECT family of ubiquitin ligases. Nat. Rev. Mol. Cell Biol. 10:398-409. http://dx.doi.org/10.1038/nrm2690.
21. Bernassola F, Karin M, Ciechanover A, Melino G. 2008. The HECT family of E3 ubiquitin ligases: multiple players in cancer development. Cancer Cell 14:10-21. http://dx.doi.org/10.1016/j.ccr.2008.06.001.
22. Maddika S, Kavela S, Rani N, Palicharla VR, Pokorny JL, Sarkaria JN, Chen J. 2011. WWP2 is an E3 ubiquitin ligase for PTEN. Nat. Cell Biol. 13:728-733. http://dx.doi.org/10.1038/ncb2240.
23. Chen C, Matesic LE. 2007. The Nedd4-like family of E3 ubiquitin ligases and cancer. Cancer Metastasis Rev. 26:587-604. http://dx.doi.org/10.1007/s10555-007-9091-x.
24. Marchese A, Raiborg C, Santini F, Keen JH, Stenmark H, Benovic JL. 2003. The E3 ubiquitin ligase AIP4 mediates ubiquitination and sorting of the G protein-coupled receptor CXCR4. Dev. Cell 5:709-722. http://dx.doi.org/10.1016/S1534-5807(03)00321-6.
25. Martinez-Chinchilla P, Riobo NA. 2008. Purification and bioassay of Hedgehog ligands for the study of cell death and survival. Methods Enzymol. 446:189-204. http://dx.doi.org/10.1016/S0076-6879(08)01611-X.
26. Yue S, Tang LY, Tang Y, Tang Y, Shen QH, Ding J, Chen Y, Zhang Z, Yu TT, Zhang YE, Cheng SY. 2014. Requirement of Smurf-mediated endocytosis of Patched1 in Sonic Hedgehog signal reception. eLife 12: e02555. http://dx.doi.org/10.7554/eLife.02555.
27. Kay BK, Williamson MP, Sudol M. 2000. The importance of being proline: the interaction of proline-rich motifs in signaling proteins with their cognate domains. FASEB J. 14:231-241. http://dx.doi.org/10.1096/fj.1530-6860.
28. Mouchantaf R, Azakir BA, McPherson PS, Millard SM, Wood SA, Angers A. 2006. The ubiquitin ligase Itch is auto-ubiquitylated in vivo and in vitro but is protected from degradation by interacting with the deubiquitylating enzyme FAM/USP9X. J. Biol. Chem. 281:38738-38747. http://dx.doi.org/10.1074/jbc.M605959200.
29. Lu X, Liu S, Kornberg TB. 2006. The C-terminal tail of the Hedgehog receptor Patched regulates both localization and turnover. Genes Dev. 20:2539-2551. http://dx.doi.org/10.1101/gad.1461306.
30. Bailey EC, Milenkovic L, Scott MP, Collawn JF, Johnson RL. 2002. Several Patched1 missense mutations display activity in Patched1-deficient fibroblasts. J. Biol. Chem. 277:33632-33640. http://dx.doi.org/10.1074/jbc.M202203200.
31. Di Marcotullio L, Ferretti E, Greco A, De Smaele E, Po A, Sico MA, Alimandi M, Giannini G, Maroder M, Screpanti I, Gulino A. 2006. Numb is a suppressor of Hedgehog signalling and targets Gli1 for Itchdependent ubiquitination. Nat. Cell Biol. 8:1415-1423. http://dx.doi.org/10.1038/ncb1510.
32. Fombonne J, Bissey PA, Guix C, Sadoul R, Thibert C, Mehlen P. 2012. Patched dependence receptor triggers apoptosis through ubiquitination of caspase-9. Proc. Natl. Acad. Sci. U. S. A. 109:10510-10515. http://dx.doi.org/10.1073/pnas.1200094109.
33. Rohatgi R, Milenkovic L, Scott MP. 2007. Patched1 regulates Hedgehog signaling at the primary cilium. Science 317:372-376. http://dx.doi.org/10.1126/science.1139740.
34. Corbit KC, Aanstad P, Singla V, Norman AR, Stainier DY, Reiter JF. 2005. Vertebrate Smoothened functions at the primary cilium. Nature 437:1018-1021. http://dx.doi.org/10.1038/nature04117.
35. Wang Y, Zhou Z, Walsh CT, McMahon AP. 2009. Selective translocation of intracellular Smoothened to the primary cilium in response to Hedgehog pathway modulation. Proc. Natl. Acad. Sci. U. S. A. 106:2623- 2628. http://dx.doi.org/10.1073/pnas.0812110106.
36. Molla-Herman A, Ghossoub R, Blisnick T, Meunier A, Serres C, Silbermann F, Emmerson C, Romeo K, Bourdoncle P, Schmitt A, Saunier S, Spassky N, Bastin P, Benmerah A. 2010. The ciliary pocket: an endocytic membrane domain at the base of primary and motile cilia. J. Cell Sci. 123:1785-1795. http://dx.doi.org/10.1242/jcs.059519.
37. Li S, Chen Y, Shi Q, Yue T, Wang B, Jiang J. 2012. Hedgehog-regulated ubiquitination controls Smoothened trafficking and cell surface expression in Drosophila. PLoS Biol. 10:e1001239. http://dx.doi.org/10.1371/journal.pbio.1001239.
38. Xia R, Jia H, Fan J, Liu Y, Jia J. 2012. Usp8 promotes Smoothened signaling by preventing its ubiquitination and changing its subcellular localization. PLoS Biol. 10:e1001238. http://dx.doi.org/10.1371/journal.pbio.1001238.
39. Jimenez-Sanchez M, Menzies FM, Chang YY, Simecek N, Neufeld TP, Rubinsztein DC. 2012. The Hedgehog signalling pathway regulates autophagy. Nat. Commun. 3:1200. http://dx.doi.org/10.1038/ncomms2212.
40. Huang S, Zhang Z, Zhang C, Lv X, Zheng X, Chen Z, Sun L, Wang H, Zhu Y, Zhang J, Yang S, Lu Y, Sun Q, Tao Y, Liu F, Zhao Y, Chen D. 2013. Activation of Smurf E3 ligase promoted by smoothened regulates Hedgehog signaling through targeting Patched turnover. PLoS Biol. 11: e1001721. http://dx.doi.org/10.1371/journal.pbio.1001721.
41. Ingham RJ, Gish G, Pawson T. 2004. The Nedd4 family of E3 ubiquitin ligases: functional diversity within a common modular architecture. Oncogene 23:1972-1984. http://dx.doi.org/10.1038/sj.onc.1207436.
42. Melino G, Gallagher E, Aqeilan RI, Knight R, Peschiaroli A, Rossi M, Scialpi F, Malatesta M, Zocchi L, Browne G, Ciechanover A, Bernassola F. 2008. Itch: a HECT-type E3 ligase regulating immunity, skin and cancer. Cell Death Differ. 15:1103-1112. http://dx.doi.org/10.1038/cdd.2008.60.