CHOP mediates endoplasmic reticulum stress-induced apoptosis in Gimap5-deficient T cells

PLoS ONE

Volumn 4, Issue 5, 2009, Pages

  Pino, Steven C ^a   O'Sullivan Murphy, Bryan ^a   Lidstone, Erich A ^a   Yang, Chaoxing ^a   Lipson, Kathryn L ^a   Jurczyk, Agata ^a   Dilorio, Philip ^a   Brehm, Michael A ^a   Mordes, John P ^a   Greiner, Dale L ^a   Rossini, Aldo A ^a   Bortell, Rita ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; CCAAT ENHANCER BINDING PROTEIN; GIMAP5 PROTEIN; GLUCOSE REGULATED PROTEIN 78; UNCLASSIFIED DRUG; CHAPERONE; GIMAP5 PROTEIN, RAT; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; GUANINE NUCLEOTIDE BINDING PROTEIN; HEAT SHOCK PROTEIN; HSPA5 PROTEIN, RAT;

ANIMAL CELL; APOPTOSIS; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL SURVIVAL; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; LYMPHOCYTOPENIA; NONHUMAN; PROTEIN EXPRESSION; RAT; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; ANIMAL; CYTOLOGY; ENDOPLASMIC RETICULUM; EXPERIMENTAL DIABETES MELLITUS; GENE SILENCING; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; PATHOLOGY; PHYSIOLOGICAL STRESS; SIGNAL TRANSDUCTION; THYMUS;

RATTUS;

ANIMALS; APOPTOSIS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL SURVIVAL; DIABETES MELLITUS, EXPERIMENTAL; ENDOPLASMIC RETICULUM; GENE KNOCKDOWN TECHNIQUES; GTP-BINDING PROTEINS; HEAT-SHOCK PROTEINS; LYMPHOCYTE ACTIVATION; MOLECULAR CHAPERONES; RATS; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; T-LYMPHOCYTES; THYMUS GLAND; TRANSCRIPTION FACTOR CHOP;

EID: 65549143673     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0005468     Document Type: Article

References (52)

1. Nitta T, Nasreen M, Seike T, Goji A, Ohigashi I, et al. (2006) IAN family critically regulates survival and development of T lymphocytes. PLoS Biol 4: 593-605.
2. Nitta T, Takahama Y (2007) The lymphocyte guard-IANs: regulation of lymphocyte survival by IAN/GIMAP family proteins. Trends Immunol 28: 58-65.
3. Hellquist A, Zucchelli M, Kivinen K, Saarialho-Kere U, Koskenmies S, et al. (2007) The human GIMAP5 gene has a common polyadenylation polymorphism increasing risk to systemic lupus erythematosus. J Med Genet 44: 314-321.
4. Shin JH, Janer M, McNeney B, Blay S, Deutsch K, et al. (2007) IA-2 autoantibodies in incident type I diabetes patients are associated with a polyadenylation signal polymorphism in GIMAP5. Genes Immun 8: 503-512.
5. Schulteis RD, Chu H, Dai X, Chen Y, Edwards B, et al. (2008) Impaired survival of peripheral T cells, disrupted NK/NKT cell development, and liver failure in mice lacking gimap5. Blood 112: 4905-4915.
6. Krucken J, Schroetel RM, Muller IU, Saidani N, Marinovski P, et al. (2004) Comparative analysis of the human gimap gene cluster encoding a novel GTPase family. Gene 341: 291-304.
7. Ramanathan S, Norwich K, Poussier P (1998) Antigen activation rescues recent thymic emigrants from programmed cell death in the BB rat. J Immunol 160: 5757-5764.
8. Schnell S, Demolliere C, van den BP, Jacobs H (2006) Gimap4 accelerates T-cell death. Blood 108: 591-599.
9. Hornum L, Romer J, Markholst H (2002) The diabetes-prone BB rat carries a frameshift mutation in Ian4, a positional candidate of Iddm1. Diabetes 51: 1972-1979.
10. MacMurray AJ, Moralejo DH, Kwitek AE, Rutledge EA, Van Yserloo B, et al. (2002) Lymphopenia in the BB rat model of type 1 diabetes is due to a mutation in a novel immune-associated nucleotide (Ian)-related gene. Genome Res 12: 1029-1039.
11. Pandarpurkar M, Wilson-Fritch L, Corvera S, Markholst H, Hornum L, et al. (2003) Ian4 is required for mitochondrial integrity and T cell survival. Proc Natl Acad Sci U S A 100: 10382-10387.
12. Dalberg U, Markholst H, Hornum L (2007) Both Gimap5 and the diabetogenic BBDP allele of Gimap5 induce apoptosis in T cells. Int Immunol 19: 447-453.
13. Sandal T, Aumo L, Hedin L, Gjertsen BT, Doskeland SO (2003) Irod/Ian5: an inhibitor of gamma-radiation- and okadaic acid-induced apoptosis. Mol Biol Cell 14: 3292-3304.
14. Daheron L, Zenz T, Siracusa LD, Brenner C, Calabretta B (2001) Molecular cloning of Ian4: a BCR/ABL-induced gene that encodes an outer membrane mitochondrial protein with GTP-binding activity. Nucleic Acids Res 29: 1308-1316.
15. Kaneko M, Nomura Y (2003) ER signaling in unfolded protein response. Life Sci 74: 199-205.
16. Kaufman RJ (2002) Orchestrating the unfolded protein response in health and disease. J Clin Invest 110: 1389-1398.
17. Borgese N, Francolini M, Snapp E (2006) Endoplasmic reticulum architecture: structures in flux. Curr Opin Cell Biol 18: 358-364.
18. Boyce M, Yuan J (2006) Cellular response to endoplasmic reticulum stress: a matter of life or death. Cell Death Differ 13: 363-373.
19. Ron D (2002) Translational control in the endoplasmic reticulum stress response. J Clin Invest 110: 1383-1388.
20. Rao RV, Peel A, Logvinova A, Del Rio G, Hermel E, et al. (2002) Coupling endoplasmic reticulum stress to the cell death program: role of the ER chaperone GRP78. FEBS Lett 514: 122-128.
21. Harding HP, Calfon M, Urano F, Novoa I, Ron D (2002) Transcriptional and translational control in the Mammalian unfolded protein response. Annu Rev Cell Dev Biol 18: 575-599.
22. Yoshida H, Oku M, Suzuki M, Mori K (2006) pXBP1(U) encoded in XBP1 pre-mRNA negatively regulates unfolded protein response activator pXBP1(S) in mammalian ER stress response. J Cell Biol 172: 565-575.
23. Zhang K, Kaufman RJ (2004) Signaling the unfolded protein response from the endoplasmic reticulum. J Biol Chem 279: 25935-25938.
24. Lee AS (2005) The ER chaperone and signaling regulator GRP78/BiP as a monitor of endoplasmic reticulum stress. Methods 35: 373-381.
25. Sato N, Urano F, Yoon LJ, Kim SH, Li M, et al. (2000) Upregulation of BiP and CHOP by the unfolded-protein response is independent of presenilin expression. Nat Cell Biol 2: 863-870.
26. Puthalakath H, O'Reilly LA, Gunn P, Lee L, Kelly PN, et al. (2007) ER stress triggers apoptosis by activating BH3-only protein Bim. Cell 129: 1337-1349.
27. Wang XZ, Lawson B, Brewer JW, Zinszner H, Sanjay A, et al. (1996) Signals from the stressed endoplasmic reticulum induce C/EBP-homologous protein (CHOP/GADD153). Mol Cell Biol 16: 4273-4280.
28. Medigeshi GR, Lancaster AM, Hirsch AJ, Briese T, Lipkin WI, et al. (2007) West Nile virus infection activates the unfolded protein response, leading to CHOP induction and apoptosis. J Virol 81: 10849-10860.
29. Michalkiewicz M, Michalkiewicz T, Ettinger RA, Rutledge EA, Fuller JM, et al. (2004) Transgenic rescue demonstrates involvement of the Ian5 gene in T cell development in the rat. Physiol Genomics 19: 228-232.
30. Jung CG, Kamiyama T, Agui T (1999) Elevated apoptosis of peripheral T lymphocytes in diabetic BB rats. Immunology 98: 590-594.
31. Lang JA, Kominski D, Bellgrau D, Scheinman RI (2004) Partial activation precedes apoptotic death in T cells harboring an IAN gene mutation. Eur J Immunol 34: 2396-2406.
32. Pino SC, O'Sullivan-Murphy B, Lidstone EA, Thornley TB, Jurczyk A, et al. (2008) Protein kinase C signaling during T cell activation induces the endoplasmic reticulum stress response. Cell Stress Chaperones 13: 421-434.
33. Scheu S, Stetson DB, Reinhardt RL, Leber JH, Mohrs M, et al. (2006) Activation of the integrated stress response during T helper cell differentiation. Nat Immunol 7: 644-651.
34. Mordes JP, Bortell R, Blankenhorn EP, Rossini AA, Greiner DL (2004) Rat models of type 1 diabetes: genetics, environment, and autoimmunity. ILAR J 45: 278-291.
35. Gallegos AM, Bevan MJ (2006) Central tolerance: good but imperfect. Immunol Rev 209: 290-296.
36. Kisielow P, von Boehmer H (1995) Development and selection of T cells: facts and puzzles. Adv Immunol 58: 87-209.
37. Willerford DM, Swat W, Alt FW (1996) Developmental regulation of V(D)J recombination and lymphocyte differentiation. Curr Opin Genet Dev 6: 603-609.
38. Iwakoshi NN, Goldschneider I, Tausche F, Mordes JP, Rossini AA, et al. (1998) High frequency apoptosis of recent thymic emigrants in the liver of lymphopenic diabetes-prone BioBreeding rats. J Immunol 160: 5838-5850.
39. Gass JN, Gifford NM, Brewer JW (2002) Activation of an unfolded protein response during differentiation of antibody-secreting B cells. J Biol Chem 277: 49047-49054.
40. Nakanishi K, Sudo T, Morishima N (2005) Endoplasmic reticulum stress signaling transmitted by ATF6 mediates apoptosis during muscle development. J Cell Biol 169: 555-560.
41. Oyadomari S, Araki E, Mori M (2002) Endoplasmic reticulum stress-mediated apoptosis in pancreatic beta-cells. Apoptosis 7: 335-345.
42. Keita M, Leblanc C, Andrews D, Ramanathan S (2007) GIMAP5 regulates mitochondrial integrity from a distinct subcellular compartment. Biochem Biophys Res Commun 361: 481-486.
43. Kim R, Emi M, Tanabe K, Murakami S (2006) Role of the unfolded protein response in cell death. Apoptosis 11: 5-13.
44. Faitova J, Krekac D, Hrstka R, Vojtesek B (2006) Endoplasmic reticulum stress and apoptosis. Cell Mol Biol Lett 11: 488-505.
45. Kim I, Xu W, Reed JC (2008) Cell death and endoplasmic reticulum stress: disease relevance and therapeutic opportunities. Nat Rev Drug Discov 7: 1013-1030.
46. Araki E, Oyadomari S, Mori M (2003) Impact of endoplasmic reticulum stress pathway on pancreatic beta-cells and diabetes mellitus. Exp Biol Med 228: 1213-1217.
47. Rossini AA (2004) Autoimmune diabetes and the circle of tolerance. Diabetes 53: 267-275.
48. Kaaba SA, Al-Harbi SA (1995) Abnormal lymphocyte subsets in Kuwaiti patients with type-1 insulin-dependent diabetes mellitus and their first-degree relatives. Immunol Lett 47: 209-213.
49. Mordes JP, Cort L, Norowski E, Leif J, Fuller JM, et al. (2009) Analysis of the rat Iddm14 diabetes susceptibility locus in multiple rat strains: identification of a susceptibility haplotype in the Tcrb-V locus. Mamm Genome, In press.
50. Mordes JP, Leif J, Novak S, DeScipio C, Greiner DL, et al. (2002) The iddm4 locus segregates with diabetes susceptibility in congenic WF.iddm4 rats. Diabetes 51: 3254-3262.
51. Blankenhorn EP, Rodemich L, Martin-Fernandez C, Leif J, Greiner DL, et al. (2005) The rat diabetes susceptibility locus Iddm4 and at least one additional gene are required for autoimmune diabetes induced by viral infection. Diabetes 54: 1233-1237.
52. Rigby MR, Bortell R, Greiner DL, Czech MP, Klarlund JK, et al. (1996) The rat T-cell surface protein RT6 is associated with src family tyrosine kinases and generates an activation signal. Diabetes 45: 1419-1426.