The Dependence Receptor UNC5H2/B Triggers Apoptosis via PP2A-Mediated Dephosphorylation of DAP Kinase

Molecular Cell

Volumn 40, Issue 6, 2010, Pages 863-876

  Guenebeaud, Céline ^a   Goldschneider, David ^a   Castets, Marie ^a   Guix, Catherine ^a   Chazot, Guillaume ^a   Delloye Bourgeois, Céline ^a   Eisenberg Lerner, Avital ^b   Shohat, Galit ^b   Zhang, Mingjie ^c   Laudet, Vincent ^d   Kimchi, Adi ^b   Bernet, Agnès ^a   Mehlen, Patrick ^a  

^a UNIVERSITÉ DE LYON   (France)

^b WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^c HONG KONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Hong Kong)

^d University Lyon i   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SURFACE RECEPTOR; DEATH ASSOCIATED PROTEIN KINASE; NETRIN 1; PHOSPHATASE; PHOSPHATASE 2A; PROTEIN UNC5H2; UNCLASSIFIED DRUG;

ANGIOGENESIS; APOPTOSIS; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; DEPHOSPHORYLATION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME STRUCTURE; HUMAN; HUMAN CELL; PROTEIN BINDING; PROTEIN INTERACTION;

APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASES; HUMANS; PHOSPHORYLATION; PROTEIN PHOSPHATASE 2; RECEPTORS, CELL SURFACE; TUMOR CELLS, CULTURED;

EID: 78650251694     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2010.11.021     Document Type: Article

References (60)

1. Ackerman S.L., Kozak L.P., Przyborski S.A., Rund L.A., Boyer B.B., Knowles B.B. The mouse rostral cerebellar malformation gene encodes an UNC-5-like protein. Nature 1997, 386:838-842.
2. Arroyo J.D., Hahn W.C. Involvement of PP2A in viral and cellular transformation. Oncogene 2005, 24:7746-7755.
3. Bernet A., Mazelin L., Coissieux M.M., Gadot N., Ackerman S.L., Scoazec J.Y., Mehlen P. Inactivation of the UNC5C Netrin-1 receptor is associated with tumor progression in colorectal malignancies. Gastroenterology 2007, 133:1840-1848.
4. Bialik S., Kimchi A. The death-associated protein kinases: structure, function, and beyond. Annu. Rev. Biochem. 2006, 75:189-210.
5. Bordeaux M.C., Forcet C., Granger L., Corset V., Bidaud C., Billaud M., Bredesen D.E., Edery P., Mehlen P. The RET proto-oncogene induces apoptosis: a novel mechanism for Hirschsprung disease. EMBO J. 2000, 19:4056-4063.
6. Castets M., Coissieux M.M., Delloye-Bourgeois C., Bernard L., Delcros J.G., Bernet A., Laudet V., Mehlen P. Inhibition of endothelial cell apoptosis by netrin-1 during angiogenesis. Dev. Cell 2009, 16:614-620.
7. Chatfield K., Eastman A. Inhibitors of protein phosphatases 1 and 2A differentially prevent intrinsic and extrinsic apoptosis pathways. Biochem. Biophys. Res. Commun. 2004, 323:1313-1320.
8. Chen C.H., Wang W.J., Kuo J.C., Tsai H.C., Lin J.R., Chang Z.F., Chen R.H. Bidirectional signals transduced by DAPK-ERK interaction promote the apoptotic effect of DAPK. EMBO J. 2005, 24:294-304.
9. Cirulli V., Yebra M. Netrins: beyond the brain. Nat. Rev. Mol. Cell Biol. 2007, 8:296-306.
10. Cohen O., Feinstein E., Kimchi A. DAP-kinase is a Ca2+/calmodulin-dependent, cytoskeletal-associated protein kinase, with cell death-inducing functions that depend on its catalytic activity. EMBO J. 1997, 16:998-1008.
11. Cohen O., Inbal B., Kissil J.L., Raveh T., Berissi H., Spivak-Kroizaman T., Feinstein E., Kimchi A. DAP-kinase participates in TNF-alpha- and Fas-induced apoptosis and its function requires the death domain. J. Cell Biol. 1999, 146:141-148.
12. Deiss L.P., Feinstein E., Berissi H., Cohen O., Kimchi A. Identification of a novel serine/threonine kinase and a novel 15-kD protein as potential mediators of the gamma interferon-induced cell death. Genes Dev. 1995, 9:15-30.
13. Delloye-Bourgeois C., Brambilla E., Coissieux M.M., Guenebeaud C., Pedeux R., Firlej V., Cabon F., Brambilla C., Mehlen P., Bernet A. Interference with netrin-1 and tumor cell death in non-small cell lung cancer. J. Natl. Cancer Inst. 2009, 101:237-247.
14. Delloye-Bourgeois C., Fitamant J., Paradisi A., Cappellen D., Douc-Rasy S., Raquin M.A., Stupack D., Nakagawara A., Rousseau R., Combaret V., et al. Netrin-1 acts as a survival factor for aggressive neuroblastoma. J. Exp. Med. 2009, 206:833-847.
15. Deng X., Gao F., May W.S. Protein phosphatase 2A inactivates Bcl2's antiapoptotic function by dephosphorylation and up-regulation of Bcl2-p53 binding. Blood 2009, 113:422-428.
16. Eichhorn P.J., Creyghton M.P., Bernards R. Protein phosphatase 2A regulatory subunits and cancer. Biochim. Biophys. Acta 2009, 1795:1-15.
17. Eisenberg-Lerner A., Kimchi A. DAP kinase regulates JNK signaling by binding and activating protein kinase D under oxidative stress. Cell Death Differ. 2007, 14:1908-1915.
18. Feinstein E., Kimchi A., Wallach D., Boldin M., Varfolomeev E. The death domain: a module shared by proteins with diverse cellular functions. Trends Biochem. Sci. 1995, 20:342-344.
19. Fitamant J., Guenebeaud C., Coissieux M.M., Guix C., Treilleux I., Scoazec J.Y., Bachelot T., Bernet A., Mehlen P. Netrin-1 expression confers a selective advantage for tumor cell survival in metastatic breast cancer. Proc. Natl. Acad. Sci. USA 2008, 105:4850-4855.
20. Forcet C., Stein E., Pays L., Corset V., Llambi F., Tessier-Lavigne M., Mehlen P. Netrin-1-mediated axon outgrowth requires deleted in colorectal cancer-dependent MAPK activation. Nature 2002, 417:443-447.
21. Fujita Y., Taniguchi J., Uchikawa M., Endo M., Hata K., Kubo T., Mueller B.K., Yamashita T. Neogenin regulates neuronal survival through DAP kinase. Cell Death Differ. 2008, 15:1593-1608.
22. Furne C., Rama N., Corset V., Chédotal A., Mehlen P. Netrin-1 is a survival factor during commissural neuron navigation. Proc. Natl. Acad. Sci. USA 2008, 105:14465-14470.
23. Furne C., Ricard J., Cabrera J.R., Pays L., Bethea J.R., Mehlen P., Liebl D.J. EphrinB3 is an anti-apoptotic ligand that inhibits the dependence receptor functions of EphA4 receptors during adult neurogenesis. Biochim. Biophys. Acta 2009, 1793:231-238.
24. Garcia A., Cayla X., Guergnon J., Dessauge F., Hospital V., Rebollo M.P., Fleischer A., Rebollo A. Serine/threonine protein phosphatases PP1 and PP2A are key players in apoptosis. Biochimie 2003, 85:721-726.
25. Goldschneider D., Mehlen P. Dependence receptors: a new paradigm in cell signaling and cancer therapy. Oncogene 2010, 29:1865-1882.
26. Gozuacik D., Kimchi A. DAPk protein family and cancer. Autophagy 2006, 2:74-79.
27. Gozuacik D., Bialik S., Raveh T., Mitou G., Shohat G., Sabanay H., Mizushima N., Yoshimori T., Kimchi A. DAP-kinase is a mediator of endoplasmic reticulum stress-induced caspase activation and autophagic cell death. Cell Death Differ. 2008, 15:1875-1886.
28. Hong K., Hinck L., Nishiyama M., Poo M.M., Tessier-Lavigne M., Stein E. A ligand-gated association between cytoplasmic domains of UNC5 and DCC family receptors converts netrin-induced growth cone attraction to repulsion. Cell 1999, 97:927-941.
29. Inbal B., Cohen O., Polak-Charcon S., Kopolovic J., Vadai E., Eisenbach L., Kimchi A. DAP kinase links the control of apoptosis to metastasis. Nature 1997, 390:180-184.
30. Janssens V., Goris J. Protein phosphatase 2A: a highly regulated family of serine/threonine phosphatases implicated in cell growth and signalling. Biochem. J. 2001, 353:417-439.
31. Junttila M.R., Puustinen P., Niemelä M., Ahola R., Arnold H., Böttzauw T., Ala-aho R., Nielsen C., Ivaska J., Taya Y., et al. CIP2A inhibits PP2A in human malignancies. Cell 2007, 130:51-62.
32. Kawaguchi K., Oda Y., Saito T., Yamamoto H., Takahira T., Tamiya S., Iwamoto Y., Tsuneyoshi M. Death-associated protein kinase (DAP kinase) alteration in soft tissue leiomyosarcoma: Promoter methylation or homozygous deletion is associated with a loss of DAP kinase expression. Hum. Pathol. 2004, 35:1266-1271.
33. Keino-Masu K., Masu M., Hinck L., Leonardo E.D., Chan S.S., Culotti J.G., Tessier-Lavigne M. Deleted in Colorectal Cancer (DCC) encodes a netrin receptor. Cell 1996, 87:175-185.
34. Kong M., Fox C.J., Mu J., Solt L., Xu A., Cinalli R.M., Birnbaum M.J., Lindsten T., Thompson C.B. The PP2A-associated protein alpha4 is an essential inhibitor of apoptosis. Science 2004, 306:695-698.
35. Lawson N.D., Weinstein B.M. In vivo imaging of embryonic vascular development using transgenic zebrafish. Dev. Biol. 2002, 248:307-318.
36. Li X., Scuderi A., Letsou A., Virshup D.M. B56-associated protein phosphatase 2A is required for survival and protects from apoptosis in Drosophila melanogaster. Mol. Cell. Biol. 2002, 22:3674-3684.
37. Llambi F., Causeret F., Bloch-Gallego E., Mehlen P. Netrin-1 acts as a survival factor via its receptors UNC5H and DCC. EMBO J. 2001, 20:2715-2722.
38. Llambi F., Lourenço F.C., Gozuacik D., Guix C., Pays L., Del Rio G., Kimchi A., Mehlen P. The dependence receptor UNC5H2 mediates apoptosis through DAP-kinase. EMBO J. 2005, 24:1192-1201.
39. Lu X., Le Noble F., Yuan L., Jiang Q., De Lafarge B., Sugiyama D., Bréant C., Claes F., De Smet F., Thomas J.L., et al. The netrin receptor UNC5B mediates guidance events controlling morphogenesis of the vascular system. Nature 2004, 432:179-186.
40. Maisse C., Rossin A., Cahuzac N., Paradisi A., Klein C., Haillot M.L., Hérincs Z., Mehlen P., Hueber A.O. Lipid raft localization and palmitoylation: identification of two requirements for cell death induction by the tumor suppressors UNC5H. Exp. Cell Res. 2008, 314:2544-2552.
41. Mazelin L., Bernet A., Bonod-Bidaud C., Pays L., Arnaud S., Gespach C., Bredesen D.E., Scoazec J.Y., Mehlen P. Netrin-1 controls colorectal tumorigenesis by regulating apoptosis. Nature 2004, 431:80-84.
42. Mehlen P., Bredesen D.E. The dependence receptor hypothesis. Apoptosis 2004, 9:37-49.
43. Mehlen P., Furne C. Netrin-1: when a neuronal guidance cue turns out to be a regulator of tumorigenesis. Cell. Mol. Life Sci. 2005, 62:2599-2616.
44. Mehlen P., Puisieux A. Metastasis: a question of life or death. Nat. Rev. Cancer 2006, 6:449-458.
45. Mehlen P., Rabizadeh S., Snipas S.J., Assa-Munt N., Salvesen G.S., Bredesen D.E. The DCC gene product induces apoptosis by a mechanism requiring receptor proteolysis. Nature 1998, 395:801-804.
46. Mille F., Llambi F., Guix C., Delloye-Bourgeois C., Guenebeaud C., Castro-Obregon S., Bredesen D.E., Thibert C., Mehlen P. Interfering with multimerization of netrin-1 receptors triggers tumor cell death. Cell Death Differ. 2009, 16:1344-1351.
47. Mille F., Thibert C., Fombonne J., Rama N., Guix C., Hayashi H., Corset V., Reed J.C., Mehlen P. The Patched dependence receptor triggers apoptosis through a DRAL-caspase-9 complex. Nat. Cell Biol. 2009, 11:739-746.
48. Raveh T., Kimchi A. DAP kinase-a proapoptotic gene that functions as a tumor suppressor. Exp. Cell Res. 2001, 264:185-192.
49. Sablina A.A., Chen W., Arroyo J.D., Corral L., Hector M., Bulmer S.E., DeCaprio J.A., Hahn W.C. The tumor suppressor PP2A Abeta regulates the RalA GTPase. Cell 2007, 129:969-982.
50. Serafini T., Colamarino S.A., Leonardo E.D., Wang H., Beddington R., Skarnes W.C., Tessier-Lavigne M. Netrin-1 is required for commissural axon guidance in the developing vertebrate nervous system. Cell 1996, 87:1001-1014.
51. Shohat G., Spivak-Kroizman T., Cohen O., Bialik S., Shani G., Berrisi H., Eisenstein M., Kimchi A. The pro-apoptotic function of death-associated protein kinase is controlled by a unique inhibitory autophosphorylation-based mechanism. J. Biol. Chem. 2001, 276:47460-47467.
52. Silverstein A.M., Barrow C.A., Davis A.J., Mumby M.C. Actions of PP2A on the MAP kinase pathway and apoptosis are mediated by distinct regulatory subunits. Proc. Natl. Acad. Sci. USA 2002, 99:4221-4226.
53. Strack S., Cribbs J.T., Gomez L. Critical role for protein phosphatase 2A heterotrimers in mammalian cell survival. J. Biol. Chem. 2004, 279:47732-47739.
54. Tang X., Jang S.W., Okada M., Chan C.B., Feng Y., Liu Y., Luo S.W., Hong Y., Rama N., Xiong W.C., et al. Netrin-1 mediates neuronal survival through PIKE-L interaction with the dependence receptor UNC5B. Nat. Cell Biol. 2008, 10:698-706.
55. Tanikawa C., Matsuda K., Fukuda S., Nakamura Y., Arakawa H. p53RDL1 regulates p53-dependent apoptosis. Nat. Cell Biol. 2003, 5:216-223.
56. Tauszig-Delamasure S., Yu L.Y., Cabrera J.R., Bouzas-Rodriguez J., Mermet-Bouvier C., Guix C., Bordeaux M.C., Arumäe U., Mehlen P. The TrkC receptor induces apoptosis when the dependence receptor notion meets the neurotrophin paradigm. Proc. Natl. Acad. Sci. USA 2007, 104:13361-13366.
57. Thibert C., Teillet M.A., Lapointe F., Mazelin L., Le Douarin N.M., Mehlen P. Inhibition of neuroepithelial patched-induced apoptosis by sonic hedgehog. Science 2003, 301:843-846.
58. Wang H., Ozaki T., Shamim Hossain M., Nakamura Y., Kamijo T., Xue X., Nakagawara A. A newly identified dependence receptor UNC5H4 is induced during DNA damage-mediated apoptosis and transcriptional target of tumor suppressor p53. Biochem. Biophys. Res. Commun. 2008, 370:594-598.
59. Wang R., Wei Z., Jin H., Wu H., Yu C., Wen W., Chan L.N., Wen Z., Zhang M. Autoinhibition of UNC5b revealed by the cytoplasmic domain structure of the receptor. Mol. Cell 2009, 33:692-703.
60. Wilson B.D., Ii M., Park K.W., Suli A., Sorensen L.K., Larrieu-Lahargue F., Urness L.D., Suh W., Asai J., Kock G.A., et al. Netrins promote developmental and therapeutic angiogenesis. Science 2006, 313:640-644.