The unfolded protein response selectively targets active smoothened mutants

Molecular and Cellular Biology

Volumn 33, Issue 12, 2013, Pages 2375-2387

  Marada, Suresh ^a   Stewart, Daniel P ^a   Bodeen, William J ^a,b   Han, Young Goo ^a   Ogden, Stacey K ^a  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^b UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

THAPSIGARGIN;

ARTICLE; CONFORMATION; DEGRADATION; DROSOPHILA MELANOGASTER; ENDOPLASMIC RETICULUM; IN VIVO STUDY; MODULATION; MUTANT; MUTATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; UNFOLDED PROTEIN RESPONSE; WILD TYPE;

3T3 CELLS; ANIMALS; ANTINEOPLASTIC AGENTS; BENZOQUINONES; BORONIC ACIDS; CARCINOMA, BASAL CELL; CELL LINE; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; ENZYME INHIBITORS; GREEN FLUORESCENT PROTEINS; HEDGEHOG PROTEINS; HETEROCYCLIC COMPOUNDS WITH 4 OR MORE RINGS; HSP90 HEAT-SHOCK PROTEINS; LACTAMS, MACROCYCLIC; MEDULLOBLASTOMA; MICE; MUTANT PROTEINS; PYRAZINES; RECEPTORS, G-PROTEIN-COUPLED; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; THAPSIGARGIN; UBIQUITIN-PROTEIN LIGASES; UNFOLDED PROTEIN RESPONSE;

DROSOPHILA MELANOGASTER; ERINACEIDAE;

EID: 84878997806     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.01445-12     Document Type: Article

References (56)

1. Jiang J, Hui CC. 2008. Hedgehog signaling in development and cancer. Dev. Cell 15:801-812.
2. Barakat MT, Humke EW, Scott MP. 2010. Learning from Jekyll to control Hyde: Hedgehog signaling in development and cancer. Trends Mol. Med. 16:337-348.
3. Xie J, Murone M, Luoh SM, Ryan A, Gu Q, Zhang C, Bonifas JM, Lam CW, Hynes M, Goddard A, Rosenthal A, Epstein EH, Jr, de Sauvage FJ. 1998. Activating Smoothened mutations in sporadic basal-cell carcinoma. Nature 391:90 -92.
4. Fan H, Oro AE, Scott MP, Khavari PA. 1997. Induction of basal cell carcinoma features in transgenic human skin expressing Sonic Hedgehog. Nat. Med. 3:788 -792.
5. Goodrich LV, Milenkovic L, Higgins KM, Scott MP. 1997. Altered neural cell fates and medulloblastoma in mouse patched mutants. Science 277:1109 -1113.
6. Karhadkar SS, Bova GS, Abdallah N, Dhara S, Gardner D, Maitra A, Isaacs JT, Berman DM, Beachy PA. 2004. Hedgehog signalling in prostate regeneration, neoplasia and metastasis. Nature 431:707-712.
7. Watkins DN, Berman DM, Burkholder SG, Wang B, Beachy PA, Baylin SB. 2003. Hedgehog signalling within airway epithelial progenitors and in small-cell lung cancer. Nature 422:313-317.
8. Yuan Z, Goetz JA, Singh S, Ogden SK, Petty WJ, Black CC, Memoli VA, Dmitrovsky E, Robbins DJ. 2007. Frequent requirement of hedgehog signaling in non-small cell lung carcinoma. Oncogene 26:1046 -1055.
9. Berman DM, Karhadkar SS, Maitra A, Montes De Oca R, Gerstenblith MR, Briggs K, Parker AR, Shimada Y, Eshleman JR, Watkins DN, Beachy PA. 2003. Widespread requirement for Hedgehog ligand stimulation in growth of digestive tract tumours. Nature 425:846-851.
10. van den Heuvel M, Ingham PW. 1996. smoothened encodes a receptorlike serpentine protein required for Hedgehog signalling. Nature 382:547-551.
11. Alcedo J, Ayzenzon M, Von Ohlen T, Noll M, Hooper JE. 1996. The Drosophila smoothened gene encodes a seven-pass membrane protein, a putative receptor for the hedgehog signal. Cell 86:221-232.
12. Carroll CE, Marada S, Stewart DP, Ouyang JX, Ogden SK. 2012. The extracellular loops of Smoothened play a regulatory role in control of Hedgehog pathway activation. Development 139:612-621.
13. Karnik SS, Sakmar TP, Chen HB, Khorana HG. 1988. Cysteine residues 110 and 187 are essential for the formation of correct structure in bovine rhodopsin. Proc. Natl. Acad. Sci. U. S. A. 85:8459-8463.
14. Incardona JP, Gruenberg J, Roelink H. 2002. Sonic hedgehog induces the segregation of patched and smoothened in endosomes. Curr. Biol. 12: 983-995.
15. Chen JK, Taipale J, Cooper MK, Beachy PA. 2002. Inhibition of Hedgehog signaling by direct binding of cyclopamine to Smoothened. Genes Dev. 16:2743-2748.
16. Wong SY, Seol AD, So PL, Ermilov AN, Bichakjian CK, Epstein EH, Jr, Dlugosz AA, Reiter JF. 2009. Primary cilia can both mediate and suppress Hedgehog pathway-dependent tumorigenesis. Nat. Med. 15:1055-1061.
17. Hoffmeister H, Babinger K, Gurster S, Cedzich A, Meese C, Schadendorf K, Osten L, de Vries U, Rascle A, Witzgall R. 2011. Polycystin-2 takes different routes to the somatic and ciliary plasma membrane. J. Cell Biol. 192:631-645.
18. Han YG, Spassky N, Romaguera-Ros M, Garcia-Verdugo JM, Aguilar A, Schneider-Maunoury S, Alvarez-Buylla A. 2008. Hedgehog signaling and primary cilia are required for the formation of adult neural stem cells. Nat. Neurosci. 11:277-284.
19. Gardner BM, Walter P. 2011. Unfolded proteins are Ire1-activating ligands that directly induce the unfolded protein response. Science 333: 1891-1894.
20. Walter P, Ron D. 2011. The unfolded protein response: from stress pathway to homeostatic regulation. Science 334:1081-1086.
21. Hetz C. 2012. The unfolded protein response: controlling cell fate decisions under ER stress and beyond. Nat. Rev. Mol. Cell Biol. 13:89 -102.
22. Harding HP, Zhang Y, Ron D. 1999. Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397:271-274.
23. Yoshida H, Haze K, Yanagi H, Yura T, Mori K. 1998. Identification of the cis-acting endoplasmic reticulum stress response element responsible for transcriptional induction of mammalian glucose-regulated proteins. Involvement of basic leucine zipper transcription factors. J. Biol. Chem. 273:33741-33749.
24. Tirasophon W, Lee K, Callaghan B, Welihinda A, Kaufman RJ. 2000. The endoribonuclease activity of mammalian IRE1 autoregulates its mRNA and is required for the unfolded protein response. Genes Dev. 14:2725-2736.
25. McCracken AA, Brodsky JL. 1996. Assembly of ER-associated protein degradation in vitro: dependence on cytosol, calnexin, and ATP. J. Cell Biol. 132:291-298.
26. Liu Y, Ye Y. 2011. Proteostasis regulation at the endoplasmic reticulum: a new perturbation site for targeted cancer therapy. Cell Res. 21:867-883.
27. Li X, Zhang K, Li Z. 2011. Unfolded protein response in cancer: the physician's perspective. J. Hematol. Oncol. 4:8.
28. Taipale J, Chen JK, Cooper MK, Wang B, Mann RK, Milenkovic L, Scott MP, Beachy PA. 2000. Effects of oncogenic mutations in Smoothened and Patched can be reversed by cyclopamine. Nature 406: 1005-1009.
29. Rudin CM, Hann CL, Laterra J, Yauch RL, Callahan CA, Fu L, Holcomb T, Stinson J, Gould SE, Coleman B, LoRusso PM, Von Hoff DD, de Sauvage FJ, Low JA. 2009. Treatment of medulloblastoma with hedgehog pathway inhibitor GDC-0449. N. Engl. J. Med. 361:1173-1178.
30. Yauch RL, Dijkgraaf GJ, Alicke B, Januario T, Ahn CP, Holcomb T, Pujara K, Stinson J, Callahan CA, Tang T, Bazan JF, Kan Z, Seshagiri S, Hann CL, Gould SE, Low JA, Rudin CM, de Sauvage FJ. 2009. Smoothened mutation confers resistance to a Hedgehog pathway inhibitor in medulloblastoma. Science 326:572-574.
31. Wang Y, Davidow L, Arvanites AC, Blanchard J, Lam K, Xu K, Oza V, Yoo JW, Ng JM, Curran T, Rubin LL, McMahon AP. 2012. Glucocorticoid compounds modify smoothened localization and hedgehog pathway activity. Chem. Biol. 19:972-982.
32. Ogden SK, Casso DJ, Ascano M, Jr, Yore MM, Kornberg TB, Robbins DJ. 2006. Smoothened regulates activator and repressor functions of Hedgehog signaling via two distinct mechanisms. J. Biol. Chem. 281: 7237-7243.
33. Chen CH, von Kessler DP, Park W, Wang B, Ma Y, Beachy PA. 1999. Nuclear trafficking of Cubitus interruptus in the transcriptional regulation of Hedgehog target gene expression. Cell 98:305-316.
34. Nachtergaele S, Mydock LK, Krishnan K, Rammohan J, Schlesinger PH, Covey DF, Rohatgi R. 2012. Oxysterols are allosteric activators of the oncoprotein Smoothened. Nat. Chem. Biol. 8:211-220.
35. -δδCT method. Methods 25: 402-408.
36. Ryoo HD, Domingos PM, Kang MJ, Steller H. 2007. Unfolded protein response in a Drosophila model for retinal degeneration.EMBOJ. 26:242-252.
37. Shen Y, Meunier L, Hendershot LM. 2002. Identification and characterization of a novel endoplasmic reticulum (ER) DnaJ homologue, which stimulates ATPase activity of BiP in vitro and is induced by ER stress. J. Biol. Chem. 277:15947-15956.
38. Iwawaki T, Akai R, Kohno K, Miura M. 2004. A transgenic mouse model for monitoring endoplasmic reticulum stress. Nat. Med. 10:98 -102.
39. Duffy JB. 2002. GAL4 system in Drosophila: a fly geneticist's Swiss army knife. Genesis 34:1-15.
40. Aza-Blanc P, Ramirez-Weber FA, Laget MP, Schwartz C, Kornberg TB. 1997. Proteolysis that is inhibited by hedgehog targets Cubitus interruptus protein to the nucleus and converts it to a repressor. Cell 89:1043-1053.
41. Denef N, Neubuser D, Perez L, Cohen SM. 2000. Hedgehog induces opposite changes in turnover and subcellular localization of patched and smoothened. Cell 102:521-531.
42. Ingham PW, Nystedt S, Nakano Y, Brown W, Stark D, van den Heuvel M, Taylor AM. 2000. Patched represses the Hedgehog signalling pathway by promoting modification of the Smoothened protein. Curr. Biol. 10: 1315-1318.
43. Casso DJ, Tanda S, Biehs B, Martoglio B, Kornberg TB. 2005. Drosophila signal peptide peptidase is an essential protease for larval development. Genetics 170:139 -148.
44. Rendie D, Wilson IB, Paschinger K. 2008. The glycosylation capacity of insect cells. Croat. Chem. Acta 81:7-21.
45. Schiller B, Hykollari A, Yan S, Paschinger K, Wilson IB. 2012. Complicated N-linked glycans in simple organisms. Biol. Chem. 393:661-673. 46. Xu X, Gupta S, Hu W, McGrath BC, Cavener DR. 2011. Hyperthermiainduces the ER stress pathway. PLoS One 6:e23740. doi:10.1371/journal .pone.0023740.
46. Xu X, Gupta S, Hu W, McGrath BC, Cavener DR. 2011. Hyperthermiainduces the ER stress pathway. PLoS One 6:e23740. doi:10.1371/journal .pone.0023740.
47. Li M, Baumeister P, Roy B, Phan T, Foti D, Luo S, Lee AS. 2000. ATF6 as a transcription activator of the endoplasmic reticulum stress element: thapsigargin stress-induced changes and synergistic interactions with NF-Y and YY1. Mol. Cell. Biol. 20:5096 -5106.
48. de Celis JF, Ruiz-Gomez M. 1995. groucho and hedgehog regulate engrailed expression in the anterior compartment of the Drosophila wing. Development 121:3467-3476.
49. Tabata T, Kornberg TB. 1994. Hedgehog is a signaling protein with a key role in patterning Drosophila imaginal discs. Cell 76:89 -102.
50. Mas C, Ruiz i Altaba A. 2010. Small molecule modulation of HH-GLI signaling: current leads, trials and tribulations. Biochem. Pharmacol. 80: 712-723.
51. Robbins DJ, Goetz JA, Yuan Z, Stegman MA. 2005. Inhibitors of the Hedgehog signal transduction pathway. Curr. Cancer Ther. Rev. 1:227-288.
52. Scales SJ, de Sauvage FJ. 2009. Mechanisms of Hedgehog pathway activation in cancer and implications for therapy. Trends Pharmacol. Sci. 30:303-312.
53. Kang MJ, Ryoo HD. 2009. Suppression of retinal degeneration in Drosophila by stimulation of ER-associated degradation. Proc. Natl. Acad. Sci. U. S. A. 106:17043-17048.
54. Mendes CS, Levet C, Chatelain G, Dourlen P, Fouillet A, Dichtel-Danjoy ML, Gambis A, Ryoo HD, Steller H, Mollereau B. 2009. ER stress protects from retinal degeneration. EMBO J. 28:1296 -1307.
55. Fouillet A, Levet C, Virgone A, Robin M, Dourlen P, Rieusset J, Belaidi E, Ovize M, Touret M, Nataf S, Mollereau B. 2012. ER stress inhibits neuronal death by promoting autophagy. Autophagy 8:915-926.
56. Denmeade SR, Mhaka AM, Rosen DM, Brennen WN, Dalrymple S, Dach I, Olesen C, Gurel B, Demarzo AM, Wilding G, Carducci MA, Dionne CA, Moller JV, Nissen P, Christensen SB, Isaacs JT. 2012. Engineering a prostate-specific membrane antigen-activated tumor endothelial cell prodrug for cancer therapy. Sci. Transl. Med. 4:140ra186. doi: 10.1126/scitranslmed.3003886.