GTPase of the immune-associated nucleotide-binding protein 5 (GIMAP5) regulates calcium influx in T-lymphocytes by promoting mitochondrial calcium accumulation

Biochemical Journal

Volumn 449, Issue 2, 2013, Pages 353-364

  Chen, Xi Lin ^a   Serrano, Daniel ^a   Mayhue, Marian ^a   Wieden, Hans Joachim ^b   Stankova, Jana ^a   Boulay, Guylain ^c   Ilangumaran, Subburaj ^a   Ramanathan, Sheela ^d  

^a UNIVERSITÉ DE SHERBROOKE   (Canada)

^b UNIVERSITY OF LETHBRIDGE   (Canada)

^c UNIVERSITY OF SHERBROOKE   (Canada)

^d Centre Hospitalier Universitaire de Sherbrooke   (Canada)

Author keywords

Calcium flux; GTPase of the immune associated nucleotide binding protein 5 (GIMAP5); Microtubule; Mitochondrion; T lymphocyte

Indexed keywords

CALCIUM; GTPASE OF THE IMMUNE ASSOCIATED NUCLEOTIDE BINDING PROTEIN 5; PROTEIN; TUBULIN; UNCLASSIFIED DRUG;

ACTIN FILAMENT; ARTICLE; CALCIUM TRANSPORT; CELL DISRUPTION; CELL MEMBRANE; CELL STRAIN HEK293; CONTROLLED STUDY; HUMAN; HUMAN CELL; MICROTUBULE; MITOCHONDRION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; T LYMPHOCYTE;

ANIMALS; BLOTTING, WESTERN; CALCIUM; CELL MEMBRANE; CELLS, CULTURED; CYTOSKELETON; GTP-BINDING PROTEINS; HEK293 CELLS; HUMANS; ION TRANSPORT; MICROSCOPY, CONFOCAL; MITOCHONDRIA; MUTATION; RATS; RECEPTORS, ANTIGEN, T-CELL; T-LYMPHOCYTES; TUBULIN;

RATTUS;

EID: 84871411835     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20120516     Document Type: Article

References (72)

1. Jackson, R., Rassi, N., Crump, T., Haynes, B. and Eisenbarth, G. S. (1981) The BB diabetic rat. Profound T-cell lymphocytopenia. Diabetes 30, 887-889 (Pubitemid 11020067)
2. Poussier, P., Nakhooda, A. F., Falk, J. A., Lee, C. and Marliss, E. B. (1982) Lymphopenia and abnormal lymphocyte subsets in the "BB" rat: relationship to the diabetic syndrome. Endocrinology 110, 1825-1827
3. Elder, M. E. and Maclaren, N. K. (1983) Identification of profound peripheral T lymphocyte immunodeficiencies in the spontaneously diabetic BB rat. J. Immunol. 130, 1723-1731 (Pubitemid 13091624)
4. Groen, H., Klatter, F. A., Brons, N. H., Wubbena, A. S., Nieuwenhuis, P. and Kampinga, J. (1995) High-frequency, but reduced absolute numbers of recent thymic migrants among peripheral blood T lymphocytes in diabetes-prone BB rats. Cell. Immunol. 163, 113-119
5. Zadeh, H. H., Greiner, D. L., Wu, D. Y., Tausche, F. and Goldschneider, I. (1996) Abnormalities in the export and fate of recent thymic emigrants in diabetes-prone BB/W rats. Autoimmunity 24, 35-46 (Pubitemid 26379165)
6. Ramanathan, S., Norwich, K. and Poussier, P. (1998) Antigen activation rescues recent thymic emigrants from programmed cell death in the BB rat. J. Immunol. 160, 5757-5764 (Pubitemid 28298032)
7. Hernandez-Hoyos, G., Joseph, S., Miller, N. G. and Butcher, G. W. (1999) The lymphopenia mutation of the BB rat causes inappropriate apoptosis of mature thymocytes. Eur. J. Immunol. 29, 1832-1841 (Pubitemid 29265538)
8. Ramanathan, S. and Poussier, P. (2001) BB rat lyp mutation and Type 1 diabetes. Immunol. Rev. 184, 161-171 (Pubitemid 34123773)
9. Hornum, L., Romer, J. and Markholst, H. (2002) The diabetes-prone BB rat carries a frameshift mutation in Ian4, a positional candidate of Iddm1. Diabetes 51, 1972-1979 (Pubitemid 34564313)
10. MacMurray, A. J., Moralejo, D. H., Kwitek, A. E., Rutledge, E. A., Van Yserloo, B., Gohlke, P., Speros, S. J., Snyder, B., Schaefer, J., Bieg, S. 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 (Pubitemid 34785195)
11. Krucken, J., Schroetel, R. M., Muller, I. U., Saidani, N., Marinovski, P., Benten, W. P., Stamm, O. and Wunderlich, F. (2004) Comparative analysis of the human gimap gene cluster encoding a novel GTPase family. Gene 341, 291-304 (Pubitemid 39335904)
12. Liu, C., Wang, T., Zhang, W. and Li, X. (2008) Computational identification and analysis of immune-associated nucleotide gene family in Arabidopsis thaliana . J. Plant Physiol. 165, 777-787 (Pubitemid 351467000)
13. Nitta, T., Nasreen, M., Seike, T., Goji, A., Ohigashi, I., Miyazaki, T., Ohta, T., Kanno, M. and Takahama, Y. (2006) IAN family critically regulates survival and development of T lymphocytes. PLoS Biol. 4, e103
14. Zenz, T., Roessner, A., Thomas, A., Frohling, S., Dohner, H., Calabretta, B. and Daheron, L. (2004) hIan5: the human ortholog to the rat Ian4/Iddm1/lyp is a new member of the Ian family that is overexpressed in B-cell lymphoid malignancies. Genes Immun. 5, 109-116 (Pubitemid 38967639)
15. Barnes, M. J., Aksoylar, H., Krebs, P., Bourdeau, T., Arnold, C. N., Xia, Y., Khovananth, K., Engel, I., Sovath, S., Lampe, K. et al. (2010) Loss of T cell and B cell quiescence precedes the onset of microbial flora-dependent wasting disease and intestinal inflammation in Gimap5-deficient mice. J. Immunol. 184, 3743-3754
16. Chen, Y., Yu, M., Dai, X., Zogg, M., Wen, R., Weiler, H. and Wang, D. (2011) Critical role for Gimap5 in the survival of mouse hematopoietic stem and progenitor cells. J. Exp. Med. 208, 923-935
17. Pino, S. C., O'Sullivan-Murphy, B., Lidstone, E. A., Yang, C., Lipson, K. L., Jurczyk, A., diIorio, P., Brehm, M. A., Mordes, J. P., Greiner, D. L. et al. (2009) CHOP mediates endoplasmic reticulum stress-induced apoptosis in Gimap5-deficient T cells. PLoS ONE 4, e5468
18. Keita, M., Leblanc, C., Andrews, D. and Ramanathan, S. (2007) GIMAP5 regulates mitochondrial integrity from a distinct subcellular compartment. Biochem. Biophys. Res. Commun. 361, 481-486 (Pubitemid 47187283)
19. Pandarpurkar, M., Wilson-Fritch, L., Corvera, S., Markholst, H., Hornum, L., Greiner, D. L., Mordes, J. P., Rossini, A. A. and Bortell, R. (2003) Ian4 is required for mitochondrial integrity and T cell survival. Proc. Natl. Acad. Sci. U.S.A. 100, 10382-10387 (Pubitemid 37071887)
20. Wong, V. W. Y., Saunders, A. E., Hutchings, A., Pascall, J. C., Carter, C., Bright, N. A., Walker, S. A., Ktistakis, N. T. and Butcher, G. W. (2010) The autoimmunity-related GIMAP5 GTPase is a lysosome-associated protein. Self/nonself 1, 259-268
21. Schulteis, R. D., Chu, H., Dai, X., Chen, Y., Edwards, B., Haribhai, D., Williams, C. B., Malarkannan, S., Hessner, M. J., Glisic-Milosavljevic, S. et al. (2008) Impaired survival of peripheral T cells, disrupted NK/NKT cell development, and liver failure in mice lacking Gimap5. Blood 112, 4905-4914
22. Lee, K. U. (1994) Nitric oxide produced by macrophages mediates suppression of ConA-induced proliferative responses of splenic leukocytes in the diabetes-prone BB rat. Diabetes 43, 1218-1220
23. Lau, A., Ramanathan, S. and Poussier, P. (1998) Excessive production of nitric oxide by macrophages from DP-BB rats is secondary to the T-lymphopenic state of these animals. Diabetes 47, 197-205 (Pubitemid 28079974)
24. Takada, K. and Jameson, S. C. (2009) Naive T cell homeostasis: from awareness of space to a sense of place. Nat. Rev. Immunol. 9, 823-832
25. Seddon, B. and Zamoyska, R. (2002) TCR and IL-7 receptor signals can operate independently or synergize to promote lymphopenia-induced expansion of naive T cells. J. Immunol. 169, 3752-3759
26. 2+ influx. Curr. Biol. 15, 1235-1241
27. Roos, J., DiGregorio, P. J., Yeromin, A. V., Ohlsen, K., Lioudyno, M., Zhang, S., Safrina, O., Kozak, J. A., Wagner, S. L., Cahalan, M. D. et al. (2005) STIM1, an essential and conserved component of store-operated Ca2+ channel function. J. Cell Biol. 169, 435-445 (Pubitemid 40686694)
28. Berridge, M. J. (1993) Inositol trisphosphate and calcium signalling. Nature 361, 315-325
29. Hogan, P. G., Lewis, R. S. and Rao, A. (2010) Molecular basis of calcium signaling in lymphocytes: STIM and ORAI. Annu. Rev. Immunol. 28, 491-533
30. Valitutti, S., Dessing, M., Aktories, K., Gallati, H. and Lanzavecchia, A. (1995) Sustained signaling leading to T cell activation results from prolonged T cell receptor occupancy. Role of T cell actin cytoskeleton. J. Exp. Med. 181, 577-584
31. Takeda, S., Rodewald, H. R., Arakawa, H., Bluethmann, H. and Shimizu, T. (1996) MHC class II molecules are not required for survival of newly generated CD4 + T cells, but affect their long-term life span. Immunity 5, 217-228 (Pubitemid 26341365)
32. Kondo, T., Cortese, I., Markovic-Plese, S., Wandinger, K. P., Carter, C., Brown, M., Leitman, S. and Martin, R. (2001) Dendritic cells signal T cells in the absence of exogenous antigen. Nat. Immunol. 2, 932-938 (Pubitemid 32976165)
33. Revy, P., Sospedra, M., Barbour, B. and Trautmann, A. (2001) Functional antigen-independent synapses formed between T cells and dendritic cells. Nat. Immunol. 2, 925-931 (Pubitemid 32976164)
34. 2+ signals in CD4+ T cells during early contacts with antigen-bearing dendritic cells in lymph node. J. Immunol. 179, 1586-1594
35. Ilangumaran, S., Forand-Boulerice, M., Bousquet, S. M., Savard, A., Rocheleau, P., Chen, X. L., Dupuis, G., Poussier, P., Boulay, G. and Ramanathan, S. (2009) Loss of GIMAP5 (GTPase of immunity-associated nucleotide binding protein 5) impairs calcium signaling in rat T lymphocytes. Mol. Immunol. 46, 1256-1259
36. Spat, A., Szanda, G., Csordas, G. and Hajnoczky, G. (2008) High- and low-calcium-dependent mechanisms of mitochondrial calcium signalling. Cell Calcium 44, 51-63
37. Contreras, L., Drago, I., Zampese, E. and Pozzan, T. (2010) Mitochondria: the calcium connection. Biochim. Biophys. Acta 1797, 607-618
38. 2+ from mitochondria via the saturable mechanisms and the permeability transition. IUBMB Life 52, 205-212
39. Hoth, M., Fanger, C. M. and Lewis, R. S. (1997) Mitochondrial regulation of store-operated calcium signaling in T lymphocytes. J. Cell Biol. 137, 633-648 (Pubitemid 27200666)
40. Hajnoczky, G., Csordas, G. and Yi, M. (2002) Old players in a new role: mitochondria-associated membranes, VDAC, and ryanodine receptors as contributors to calcium signal propagation from endoplasmic reticulum to the mitochondria. Cell Calcium 32, 363-377 (Pubitemid 36175757)
41. 2+-dependent regulation of mitochondrial dynamics by the Miro-Milton complex. Int. J. Biochem. Cell Biol. 41, 1972-1976
42. Colle, E., Fuks, A., Poussier, P., Edouard, P. and Guttmann, R. D. (1992) Polygenic nature of spontaneous diabetes in the rat. Permissive MHC haplotype and presence of the lymphopenic trait of the BB rat are not sufficient to produce susceptibility. Diabetes 41, 1617-1623
43. Manders, E. M., Verbeek, M. F. J. and Aten, J. A. (1993) Measurement of optics in dual-color confocal images. J. Microsc. 169, 375-382 (Pubitemid 23119681)
44. Arguin, G., Regimbald-Dumas, Y., Fregeau, M. O., Caron, A. Z. and Guillemette, G. (2007) Protein kinase C phosphorylates the inositol 1,4,5-trisphosphate receptor type 2 and decreases the mobilization of Ca2+ in pancreatoma AR4-2J cells. J. Endocrinol. 192, 659-668 (Pubitemid 46455968)
45. Adler, J. and Parmryd, I. (2010) Quantifying colocalization by correlation: the Pearson correlation coefficient is superior to the Mander's overlap coefficient. Cytometry, Part A 77, 733-742
46. Dalberg, U., Markholst, H. and Hornum, L. (2007) Both Gimap5 and the diabetogenic BBDP allele of Gimap5 induce apoptosis in T cells. Int. Immunol. 19, 447-453 (Pubitemid 46523392)
47. 2+ in sea urchin sperm. Biochim. Biophys. Acta 1787, 15-24
48. Szalai, G., Csordas, G., Hantash, B. M., Thomas, A. P. and Hajnoczky, G. (2000) Calcium signal transmission between ryanodine receptors and mitochondria. J. Biol. Chem. 275, 15305-15313 (Pubitemid 30337257)
49. Quintana, A., Schwarz, E. C., Schwindling, C., Lipp, P., Kaestner, L. and Hoth, M. (2006) Sustained activity of calcium release-activated calcium channels requires translocation of mitochondria to the plasma membrane. J. Biol. Chem. 281, 40302-40309 (Pubitemid 46041835)
50. Quintana, A., Schwindling, C., Wenning, A. S., Becherer, U., Rettig, J., Schwarz, E. C. and Hoth, M. (2007) T cell activation requires mitochondrial translocation to the immunological synapse. Proc. Natl. Acad. Sci. U.S.A. 104, 14418-14423 (Pubitemid 350003276)
51. Schwindling, C., Quintana, A., Krause, E. and Hoth, M. (2010) Mitochondria positioning controls local calcium influx in T cells. J. Immunol. 184, 184-190
52. Kupfer, A., Swain, S. L. and Singer, S. J. (1987) The specific direct interaction of helper T cells and antigen-presenting B cells. II. Reorientation of the microtubule organizing center and reorganization of the membrane-associated cytoskeleton inside the bound helper T cells. J. Exp. Med. 165, 1565-1580 (Pubitemid 17087908)
53. Burkhardt, J. K., Carrizosa, E. and Shaffer, M. H. (2008) The actin cytoskeleton in T cell activation. Annu. Rev. Immunol. 26, 233-259 (Pubitemid 351600376)
54. Gomez, T. S. and Billadeau, D. D. (2008) T cell activation and the cytoskeleton: you can't have one without the other. Adv. Immunol. 97, 1-64 (Pubitemid 351711631)
55. Holsinger, L. J., Graef, I. A., Swat, W., Chi, T., Bautista, D. M., Davidson, L., Lewis, R. S., Alt, F. W. and Crabtree, G. R. (1998) Defects in actin-cap formation in Vav-deficient mice implicate an actin requirement for lymphocyte signal transduction. Curr. Biol. 8, 563-572 (Pubitemid 28222890)
56. Martin-Cofreces, N. B., Robles-Valero, J., Cabrero, J. R., Mittelbrunn, M., Gordon-Alonso, M., Sung, C. H., Alarcon, B., Vazquez, J. and Sanchez-Madrid, F. (2008) MTOC translocation modulates IS formation and controls sustained T cell signaling. J. Cell Biol. 182, 951-962
57. Delon, J., Bercovici, N., Liblau, R. and Trautmann, A. (1998) Imaging antigen recognition by naive CD4 + T cells: compulsory cytoskeletal alterations for the triggering of an intracellular calcium response. Eur. J. Immunol. 28, 716-729 (Pubitemid 28101749)
58. Frederick, R. L. and Shaw, J. M. (2007) Moving mitochondria: establishing distribution of an essential organelle. Traffic 8, 1668-1675 (Pubitemid 350066679)
59. Hollenbeck, P. J. and Saxton, W. M. (2005) The axonal transport of mitochondria. J. Cell Sci. 118, 5411-5419 (Pubitemid 43079283)
60. Yi, M., Weaver, D. and Hajnoczky, G. (2004) Control of mitochondrial motility and distribution by the calcium signal: a homeostatic circuit. J. Cell Biol. 167, 661-672 (Pubitemid 39565147)
61. Maraskovsky, E., Teepe, M., Morrissey, P. J., Braddy, S., Miller, R. E., Lynch, D. H. and Peschon, J. J. (1996) Impaired survival and proliferation in IL-7 receptor-deficient peripheral T cells. J. Immunol. 157, 5315-5323 (Pubitemid 126448949)
62. Maraskovsky, E., O'Reilly, L. A., Teepe, M., Corcoran, L. M., Peschon, J. J. and Strasser, A. (1997) Bcl-2 can rescue T lymphocyte development in interleukin-7 receptor-deficient mice but not in mutant rag-1-/- mice. Cell 89, 1011-1019 (Pubitemid 127678735)
63. Schluns, K. S., Kieper, W. C., Jameson, S. C. and Lefrancois, L. (2000) Interleukin-7 mediates the homeostasis of naive and memory CD8 T cells in vivo. Nat. Immunol. 1, 426-432
64. Tan, J. T., Dudl, E., LeRoy, E., Murray, R., Sprent, J., Weinberg, K. I. and Surh, C. D. (2001) IL-7 is critical for homeostatic proliferation and survival of naive T cells. Proc. Natl. Acad. Sci. U.S.A. 98, 8732-8737 (Pubitemid 32678096)
65. Jameson, S. C. (2002) Maintaining the norm: T-cell homeostasis. Nat. Rev. Immunol. 2, 547-556
66. Schluns, K. S. and Lefrancois, L. (2003) Cytokine control of memory T-cell development and survival. Nat. Rev. Immunol. 3, 269-279 (Pubitemid 37328680)
67. Kuo, C. T., Veselits, M. L. and Leiden, J. M. (1997) LKLF: a transcriptional regulator of single-positive T cell quiescence and survival. Science 277, 1986-1990 (Pubitemid 27449139)
68. Ouyang, W. and Li, M. O. (2011) Foxo: in command of T lymphocyte homeostasis and tolerance. Trends Immunol. 32, 26-33
69. Plamondon, C., Kottis, V., Brideau, C., Metroz-Dayer, M. D. and Poussier, P. (1990) Abnormal thymocyte maturation in spontaneously diabetic BB rats involves the deletion of CD4-8+ cells. J. Immunol. 144, 923-928 (Pubitemid 20065032)
70. Omilusik, K., Priatel, J. J., Chen, X., Wang, Y. T., Xu, H., Choi, K. B., Gopaul, R., McIntyre-Smith, A., Teh, H. S., Tan, R. et al. (2011) The Ca(v)1.4 calcium channel is a critical regulator of T cell receptor signaling and naive T cell homeostasis. Immunity 35, 349-360
71. Fooksman, D. R., Vardhana, S., Vasiliver-Shamis, G., Liese, J., Blair, D. A., Waite, J., Sacristan, C., Victora, G. D., Zanin-Zhorov, A. and Dustin, M. L. (2010) Functional anatomy of T cell activation and synapse formation. Annu. Rev. Immunol. 28, 79-105
72. 2+ responses triggered in T cells by dendritic cells compared with B cells. J. Exp. Med. 188, 1473-1484