Tubulin- and actin-associating GIMAP4 is required for IFN-γ secretion during Th cell differentiation

Immunology and Cell Biology

Volumn 93, Issue 2, 2015, Pages 158-166

  Heinonen, Mirkka T ^a,b   Kanduri, Kartiek ^a   Lähdesmäki, Harri J ^c   Lahesmaa, Riitta ^a   Henttinen, Tiina A ^a  

^a UNIVERSITY OF TURKU   (Finland)

^b UNIVERSITY OF TURKU   (Finland)

^c AALTO UNIVERSITY   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; CHAPERONE; CHAPERONE VMA21; GAMMA INTERFERON; GTPASE OF THE IMMUNITY ASSOCIATED PROTEIN 4; GUANOSINE TRIPHOSPHATASE; TUBULIN; UNCLASSIFIED DRUG; GIMAP4 PROTEIN, HUMAN; GUANINE NUCLEOTIDE BINDING PROTEIN; LYMPHOCYTE ANTIGEN RECEPTOR; PROTEIN BINDING; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; VMA21 PROTEIN, HUMAN;

APOPTOSIS; ARTICLE; B LYMPHOCYTE; CELL MATURATION; CELL TRANSPORT; CELL VIABILITY; CONTROLLED STUDY; CYTOKINE RELEASE; DOWN REGULATION; ENDOPLASMIC RETICULUM; FEMALE; HELA CELL LINE; HELPER CELL; HUMAN; HUMAN CELL; LYMPHOCYTE DIFFERENTIATION; PHENOTYPE; PROTEIN DEPLETION; PROTEIN LOCALIZATION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TH1 CELL; TRANS GOLGI NETWORK; CELL CYCLE; CELL DIFFERENTIATION; CELL SURVIVAL; CYTOLOGY; GENETIC TRANSCRIPTION; IMMUNOLOGY; METABOLISM; MICROTUBULE; SECRETION (PROCESS);

ACTINS; CELL CYCLE; CELL DIFFERENTIATION; CELL SURVIVAL; DOWN-REGULATION; ENDOPLASMIC RETICULUM; GTP-BINDING PROTEINS; HELA CELLS; HUMANS; INTERFERON-GAMMA; MICROTUBULES; PROTEIN BINDING; RECEPTORS, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION; T-LYMPHOCYTES, HELPER-INDUCER; TRANS-GOLGI NETWORK; TRANSCRIPTION, GENETIC; TUBULIN; VACUOLAR PROTON-TRANSLOCATING ATPASES;

EID: 84922658842     PISSN: 08189641     EISSN: 14401711     Source Type: Journal    
DOI: 10.1038/icb.2014.86     Document Type: Article

References (52)

1. Krucken J, Schroetel RM, Muller IU, Saidani N, Marinovski P, Benten WP et al. Comparative analysis of the human gimap gene cluster encoding a novel GTPase family. Gene 2004; 27: 291-304
2. Liu C, Wang T, Zhang W, Li X. Computational identification and analysis of immuneassociated nucleotide gene family in arabidopsis thaliana. J Plant Physiol 2008; 5: 777-787
3. Poirier GM, Anderson G, Huvar A, Wagaman PC, Shuttleworth J, Jenkinson E et al. Immune-associated nucleotide-1 (IAN-1) is a thymic selection marker and defines a novel gene family conserved in plants. J Immunol 1999; 163: 4960-4969
4. Nitta T, Takahama Y. The lymphocyte guard-IANs: regulation of lymphocyte survival by IAN/GIMAP family proteins. Trends Immunol 2007; 28: 58-65
5. Filen S, Lahesmaa R. GIMAP proteins in T-lymphocytes. J Signal Transd 2010; 2010: 268589
6. Filen JJ, Filen S, Moulder R, Tuomela S, Ahlfors H, West A et al. Quantitative proteomics reveals GIMAP family proteins 1 and 4 to be differentially regulated during human T helper cell differentiation. Mol Cell Proteomics 2009; 8: 32-44
7. Baldwin TA, Hogquist KA. Transcriptional analysis of clonal deletion in vivo. J Immunol 2007; 179: 837-844
8. Nitta T, Nasreen M, Seike T, Goji A, Ohigashi I, Miyazaki T et al. IAN family critically regulates survival and development of T lymphocytes. PLoS Biol 2006; 4: e103
9. Dion C, Carter C, Hepburn L, Coadwell WJ, Morgan G, Graham M et al. Expression of the ian family of putative GTPases during T cell development and description of an ian with three sets of GTP/GDP-binding motifs. Int Immunol 2005; 17: 1257-1268
10. Pandarpurkar M, Wilson-Fritch L, Corvera S, Markholst H, Hornum L, Greiner DL et al. Ian4 is required for mitochondrial integrity and T cell survival. Proc Natl Acad Sci USA 2003; 100: 10382-10387
11. Saunders A, Webb LM, Janas ML, Hutchings A, Pascall J, Carter C et al. Putative GTPase GIMAP1 is critical for the development of mature B and T lymphocytes. Blood 2010; 115: 3249-3257.
12. Schulteis RD, Chu H, Dai X, Chen Y, Edwards B, Haribhai D et al. Impaired survival of peripheral T cells, disrupted NK/NKT cell development, and liver failure in mice lacking Gimap5. Blood 2008; 112: 4905-4914
13. MacMurray AJ, Moralejo DH, Kwitek AE, Rutledge EA, Van Yserloo B, Gohlke P et al. 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 2002; 12: 1029-1039
14. Shin JH, Janer M, McNeney B, Blay S, Deutsch K, Sanjeevi CB et al. IA-2 autoantibodies in incident type I diabetes patients are associated with a polyadenylation signal polymorphism in GIMAP5. Genes Immun 2007; 8: 503-512
15. Hellquist A, Zucchelli M, Kivinen K, Saarialho-Kere U, Koskenmies S, Widen E et al. The human GIMAP5 gene has a common polyadenylation polymorphism increasing risk to systemic lupus erythematosus. J Med Genet 2007; 44: 314-321
16. Taniwaki M, Daigo Y, Ishikawa N, Takano A, Tsunoda T, Yasui W et al. Gene expression profiles of small-cell lung cancers: molecular signatures of lung cancer. Int J Oncol 2006; 29: 567-575
17. Leipe DD, Wolf YI, Koonin EV, Aravind L. Classification and evolution of P-loop GTPases and related ATPases. J Mol Biol 2002; 317: 41-72
18. Schwefel D, Frohlich C, Eichhorst J, Wiesner B, Behlke J, Aravind L et al. Structural basis of oligomerization in septin-like GTPase of immunity-associated protein 2 (GIMAP2). Proc Natl Acad Sci USA 2010; 107: 20299-20304
19. Kinoshita M. Diversity of septin scaffolds. Curr Opin Cell Biol 2006; 18: 54-60
20. Stamm O, Krucken J, Schmitt-Wrede HP, Benten WP, Wunderlich F. Human ortholog to mouse gene imap38 encoding an ER-localizable G-protein belongs to a gene family clustered on chromosome 7q32-36. Gene 2002; 282: 159-167
21. Chen XL, Serrano D, Mayhue M, Wieden HJ, Stankova J, Boulay G et al. GTPase of the immune-associated nucleotide-binding protein 5 (GIMAP5) regulates calcium influx in T lymphocytes by promoting mitochondrial calcium accumulation. Biochem J 2013; 449: 353-364
22. Quintana A, Schwindling C, Wenning AS, Becherer U, Rettig J, Schwarz EC et al. T cell activation requires mitochondrial translocation to the immunological synapse. Proc Natl Acad Sci USA 2007; 104: 14418-14423
23. Simpson JC, Joggerst B, Laketa V, Verissimo F, Cetin C, Erfle H et al. Genome-wide RNAi screening identifies human proteins with a regulatory function in the early secretory pathway. Nat Cell Biol 2012; 14: 764-774
24. Pascall JC, Rotondo S, Mukadam AS, Oxley D, Webster J, Walker SA et al. The immune system GTPase GIMAP6 interacts with the Atg8 homologue GABARAPL2 and is recruited to autophagosomes. PLoS ONE 2013; 8: e77782
25. Weiss Y, Forêt S, Hayward DC, Ainsworth T, King R, Ball EE et al. The acute transcriptional response of the coral Acropora millepora to immune challenge: expression of GiMAP/IAN genes links the innate immune responses of corals with those of mammals and plants. BMC Genomics 2013; 14: 400
26. Jokinen R, Marttinen P, Sandell HK, Manninen T, Teerenhovi H, Wai T et al. Gimap3 regulates tissue-specific mitochondrial DNA segregation. PLoS Genet 2010; 6: e1001161
27. Jokinen R, Junnila H, Battersby BJ. Gimap3: A foot-in-The-door to tissue-specific regulation of mitochondrial DNA genetics. Small GTPases 2011; 2: 31-35
28. Cambot M, Aresta S, Kahn-Perles B, de Gunzburg J, Romeo PH. Human immune associated nucleotide 1: A member of a new guanosine triphosphatase family expressed in resting T and B cells. Blood 2002; 99: 3293-3301
29. Schnell S, Demolliere C, van den Berk P, Jacobs H. Gimap4 accelerates T-cell death. Blood 2006; 108: 591-599
30. Sugiura R, Sio SO, Shuntoh H, Kuno T. Molecular genetic analysis of the calcineurin signaling pathways. Cell Mol Life Sci 2001; 58: 278-288
31. Hacker G, Bauer A, Villunger A. Apoptosis in activated T cells: what are the triggers, and what the signal transducers? Cell Cycle 2006; 5: 2421-2424
32. Bock JB, Klumperman J, Davanger S, Scheller RH. Syntaxin 6 functions in trans-golgi network vesicle trafficking. Mol Biol Cell 1997; 8: 1261-1271
33. Peterson EA, Petty EM. Conquering the complex world of human septins: implications for health and disease. Clin Genet 2010; 77: 511-524
34. Scheele JS, Marks RE, Boss GR. Signaling by small GTPases in the immune system. Immunol Rev 2007; 218: 92-101
35. Hill KJ, Stevens TH. Vma21p is a yeast membrane protein retained in the endoplasmic reticulum by a di-lysine motif and is required for the assembly of the vacuolar H (+)-ATPase complex. Mol Biol Cell 1994; 5: 1039-1050
36. Welsh LM, Tong AH, Boone C, Jensen ON, Otte S. Genetic and molecular interactions of the Erv41p-Erv46p complex involved in transport between the endoplasmic reticulum and Golgi complex. J Cell Sci 2006; 119: 4730-4740
37. Huse M, Lillemeier BF, Kuhns MS, Chen DS, Davis MM. T cells use two directionally distinct pathways for cytokine secretion. Nat Immunol 2006; 7: 247-255
38. Wen Z, Zhong Z, Darnell JE Jr. Maximal activation of transcription by Stat1 and Stat3 requires both tyrosine and serine phosphorylation. Cell 1995; 82: 241-250
39. Decker T, Kovarik P, Meinke A. GAS elements: A few nucleotides with a major impact on cytokine-induced gene expression. J Interferon Cytokine Res 1997; 17: 121-134
40. Afkarian M, Sedy JR, Yang J, Jacobson NG, Cereb N, Yang SY et al. T-bet is a STAT1-induced regulator of IL-12R expression in naive CD4+ T cells. Nat Immunol 2002; 3: 549-557
41. Chang JT, Shevach EM, Segal BM. Regulation of interleukin (IL)-12 receptor beta2 subunit expression by endogenous IL-12: A critical step in the differentiation of pathogenic autoreactive T cells. J Exp Med 1999; 189: 969-978
42. Szabo SJ, Dighe AS, Gubler U, Murphy KM. Regulation of the interleukin (IL)-12R beta 2 subunit expression in developing T helper 1 (Th1) and Th2 cells. J Exp Med 1997; 185: 817-824
43. Carter C, Dion C, Schnell S, Coadwell WJ, Graham M, Hepburn L et al. A natural hypomorphic variant of the apoptosis regulator Gimap4/IAN1. J Immunol 2007; 179: 1784-1795
44. Hernandez-Hoyos G, Joseph S, Miller NG, Butcher GW. The lymphopenia mutation of the BB rat causes inappropriate apoptosis of mature thymocytes. Eur J Immunol 1999; 29: 1832-1841
45. Zenz T, Roessner A, Thomas A, Frohling S, Dohner H, Calabretta B, Daheron L. 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 2004; 5: 109-116
46. Barnes MJ, Aksoylar H, Krebs P, Bourdeau T, Arnold CN, Xia Y et al. 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 2010; 184: 3743-3754
47. Keita M, Leblanc C, Andrews D, Ramanathan S. GIMAP5 regulates mitochondrial integrity from a distinct subcellular compartment. Biochem Biophys Res Commun 2007; 361: 481-486
48. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U et al. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 2003; 4: 249-264
49. Gentleman R, Carey V, Huber W, Hahne F. Genefilter: Methods for filtering genes from microarray experiments. R package version 1.38.0. online manual. Available from http://www.bioconductor.org/packages/release/bioc/html/genefilter.html.
50. Benaglia T, Chaveau D, Hunter DR, Young DS. Mixtools: An R package for analyzing mixture Models. J Stat Softw 2009; 32: 1-29
51. Lee HJ, Suk JE, Patrick C, Bae EJ, Cho JH, Rho S et al. Direct transfer of alphasynuclein from neuron to astroglia causes inflammatory responses in synucleinopathies. J Biol Chem 2010; 285: 9262-9272
52. Smyth GK. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 2004; 3: Article3