Jund/ap-1-mediated gene expression promotes lymphocyte growth dependent on interleukin-7 signal transduction

PLoS ONE

Volumn 7, Issue 2, 2012, Pages

  Ruppert, Shannon M ^a   Chehtane, Mounir ^a   Zhang, Ge ^a   Hu, Haiyan ^b   Li, Xiaoman ^a   Khaled, Annette R ^a  

^a UNIVERSITY OF CENTRAL FLORIDA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF CENTRAL FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD8 ANTIGEN; GLUCOSE; GLYCOLYTIC ENZYME; HEXOKINASE; HEXOKINASE ISOENZYME; INTERLEUKIN 7; INTERLEUKIN 7 RECEPTOR; PROTEIN C FOS; PROTEIN C JUN; PROTEIN KINASE PIM 1; STAT5 PROTEIN; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR JUND; UNCLASSIFIED DRUG; MITOGEN ACTIVATED PROTEIN KINASE; PIM1 MAP KINASE;

ANIMAL CELL; ARTICLE; BIOINFORMATICS; CD8+ T LYMPHOCYTE; CELL GROWTH; CELL METABOLISM; CELL SURVIVAL; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVITY; GENE EXPRESSION REGULATION; GLUCOSE TRANSPORT; HUMAN; HUMAN CELL; LYMPHOCYTE PROLIFERATION; LYMPHOID CELL LINE; MOUSE; NONHUMAN; SIGNAL TRANSDUCTION; ANIMAL; BIOLOGY; C57BL MOUSE; CELL PROLIFERATION; CYTOLOGY; GENE EXPRESSION; LYMPHOCYTE; METABOLISM; METHODOLOGY;

ANIMALS; CELL PROLIFERATION; COMPUTATIONAL BIOLOGY; GENE EXPRESSION; GENE EXPRESSION REGULATION; GLUCOSE; HEXOKINASE; HUMANS; INTERLEUKIN-7; LYMPHOCYTES; MICE; MICE, INBRED C57BL; MITOGEN-ACTIVATED PROTEIN KINASES; PROTO-ONCOGENE PROTEINS C-FOS; PROTO-ONCOGENE PROTEINS C-JUN; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTOR AP-1;

EID: 84863164126     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0032262     Document Type: Article

References (67)

1. Kittipatarin C, Khaled AR, (2007) Interlinking interleukin-7. Cytokine 39: 75-83.
2. Sportes C, Hakim FT, Memon SA, Zhang H, Chua KS, et al. (2008) Administration of rhIL-7 in humans increases in vivo TCR repertoire diversity by preferential expansion of naive T cell subsets. J Exp Med 205: 1701-1714.
3. Alpdogan O, Muriglan SJ, Eng JM, Willis LM, Greenberg AS, et al. (2003) IL-7 enhances peripheral T cell reconstitution after allogeneic hematopoietic stem cell transplantation. J Clin Invest 112: 1095-1107.
4. Unsinger J, McGlynn M, Kasten KR, Hoekzema AS, Watanabe E, et al. (2010) IL-7 promotes T cell viability, trafficking, and functionality and improves survival in sepsis. J Immunol 184: 3768-3779.
5. Sereti I, Dunham RM, Spritzler J, Aga E, Proschan MA, et al. (2009) IL-7 administration drives T cell-cycle entry and expansion in HIV-1 infection. Blood 113: 6304-6314.
6. Sakata T, Iwagami S, Tsuruta Y, Teraoka H, Tatsumi Y, et al. (1990) Constitutive expression of interleukin-7 mRNA and production of IL-7 by a cloned murine thymic stromal cell line. J Leukoc Biol 48: 205-212.
7. Mazzucchelli RI, Warming S, Lawrence SM, Ishii M, Abshari M, et al. (2009) Visualization and identification of IL-7 producing cells in reporter mice. PLoS One 4: e7637.
8. Repass JF, Laurent MN, Carter C, Reizis B, Bedford MT, et al. (2009) IL7-hCD25 and IL7-Cre BAC transgenic mouse lines: New tools for analysis of IL-7 expressing cells. Genesis.
9. Sawa Y, Arima Y, Ogura H, Kitabayashi C, Jiang JJ, et al. (2009) Hepatic interleukin-7 expression regulates T cell responses. Immunity 30: 447-457.
10. Kovanen PE, Leonard WJ, (2004) Cytokines and immunodeficiency diseases: critical roles of the gamma(c)-dependent cytokines interleukins 2, 4, 7, 9, 15, and 21, and their signaling pathways. Immunol Rev 202: 67-83.
11. Venkitaraman AR, Cowling RJ, (1992) Interleukin 7 receptor functions by recruiting the tyrosine kinase p59fyn through a segment of its cytoplasmic tail. Proc Natl Acad Sci U S A 89: 12083-12087.
12. Seckinger P, Fougereau M, (1994) Activation of src family kinases in human pre-B cells by IL-7. J Immunol 153: 97-109.
13. Crawley JB, Willcocks J, Foxwell BM, (1996) Interleukin-7 induces T cell proliferation in the absence of Erk/MAP kinase activity. Eur J Immunol 26: 2717-2723.
14. Crawley JB, Rawlinson L, Lali FV, Page TH, Saklatvala J, et al. (1997) T cell proliferation in response to interleukins 2 and 7 requires p38MAP kinase activation. J Biol Chem 272: 15023-15027.
15. Seddon B, 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.
16. Kittipatarin C, Tschammer N, Khaled AR, (2010) The interaction of LCK and the CD4 co-receptor alters the dose response of T-cells to interleukin-7. Immunol Lett 131: 170-181.
17. Rajnavolgyi E, Benbernou N, Muegge K, Durum SK, (2000) IL-7 Withdrawal Induces a Stress Pathway Activating p38 Map Kinase and JNK.
18. Khaled AR, Moor AN, Li A, Kim K, Ferris DK, et al. (2001) Trophic Factor Withdrawal: p38 Mitogen-Activated Protein Kinase Activates NHE1, Which Induces Intracellular Alkalinization. Mol Cell Biol 21: 7545-7557.
19. Khaled AR, Bulavin DV, Kittipatarin C, Li WQ, Alvarez M, et al. (2005) Cytokine-driven cell cycling is mediated through Cdc25A. J Cell Biol 169: 755-763.
20. Shaulian E, (2010) AP-1-The Jun proteins: Oncogenes or tumor suppressors in disguise? Cell Signal 22: 894-899.
21. Eychene A, Rocques N, Pouponnot C, (2008) A new MAFia in cancer. Nat Rev Cancer 8: 683-693.
22. Hess J, Angel P, Schorpp-Kistner M, (2004) AP-1 subunits: quarrel and harmony among siblings. J Cell Sci 117: 5965-5973.
23. Gao Y, Tao J, Li MO, Zhang D, Chi H, et al. (2005) JNK1 is essential for CD8+ T cell-mediated tumor immune surveillance. J Immunol 175: 5783-5789.
24. Kallunki T, Deng T, Hibi M, Karin M, (1996) c-Jun can recruit JNK to phosphorylate dimerization partners via specific docking interactions. Cell 87: 929-939.
25. Short JD, Pfarr CM, (2002) Translational regulation of the JunD messenger RNA. J Biol Chem 277: 32697-32705.
26. Ryseck RP, Hirai SI, Yaniv M, Bravo R, (1988) Transcriptional activation of c-jun during the G0/G1 transition in mouse fibroblasts. Nature 334: 535-537.
27. Ryder K, Lau LF, Nathans D, (1988) A gene activated by growth factors is related to the oncogene v-jun. Proc Natl Acad Sci U S A 85: 1487-1491.
28. Schutte J, Minna JD, Birrer MJ, (1989) Deregulated expression of human c-jun transforms primary rat embryo cells in cooperation with an activated c-Ha-ras gene and transforms rat-1a cells as a single gene. Proc Natl Acad Sci U S A 86: 2257-2261.
29. Castellazzi M, Spyrou G, La VN, Dangy JP, Piu F, et al. (1991) Overexpression of c-jun, junB, or junD affects cell growth differently. Proc Natl Acad Sci U S A 88: 8890-8894.
30. Pfarr CM, Mechta F, Spyrou G, Lallemand D, Carillo S, et al. (1994) Mouse JunD negatively regulates fibroblast growth and antagonizes transformation by ras. Cell 76: 747-760.
31. Kim K, Khaled AR, Reynolds D, Young HA, Lee CK, et al. (2003) Characterization of an interleukin-7-dependent thymic cell line derived from a p53(-/-) mouse. J Immunol Methods 274: 177-184.
32. von-Freeden-Jeffry U, Solvason N, Howard M, Murray R, (1997) The earliest T lineage-committed cells depend on IL-7 for Bcl-2 expression and normal cell cycle progression. Immunity 7: 147-154.
33. Khaled AR, Kim K, Hofmeister R, Muegge K, Durum SK, (1999) Withdrawal of IL-7 induces Bax translocation from cytosol to mitochondria through a rise in intracellular pH. Proc Natl Acad Sci U S A 96: 14476-14481.
34. Khaled AR, Durum SK, (2003) Death and Baxes: mechanisms of lymphotrophic cytokines. Immunol Rev 193: 48-57.
35. Pellegrini M, Bouillet P, Robati M, Belz GT, Davey GM, et al. (2004) Loss of Bim increases T cell production and function in interleukin 7 receptor-deficient mice. J Exp Med 200: 1189-1195.
36. Li WQ, Jiang Q, Khaled AR, Keller JR, Durum SK, (2004) Interleukin-7 inactivates the pro-apoptotic protein bad promoting T cell survival. J Biol Chem 279: 29160-29166.
37. Li WQ, Jiang Q, Aleem E, Kaldis P, Khaled AR, et al. (2006) IL-7 promotes T cell proliferation through destabilization of p27Kip1. J Exp Med 203: 573-582.
38. Wofford JA, Wieman HL, Jacobs SR, Zhao Y, Rathmell JC, (2008) IL-7 promotes Glut1 trafficking and glucose uptake via STAT5-mediated activation of Akt to support T-cell survival. Blood 111: 2101-2111.
39. Chehtane M, Khaled AR, (2010) Interleukin-7 Mediates Glucose Utilization in Lymphocytes through Transcriptional Regulation of the Hexokinase II Gene. Am J Physiol Cell Physiol.
40. Heikkinen S, Suppola S, Malkki M, Deeb SS, Janne J, et al. (2000) Mouse hexokinase II gene: structure, cDNA, promoter analysis, and expression pattern. Mamm Genome 11: 91-96.
41. Khaled AR, Li WQ, Huang J, Fry TJ, Khaled AS, et al. (2002) Bax deficiency partially corrects IL-7 receptor alpha deficiency. Immunity 17: 561-573.
42. Li WQ, Guszczynski T, Hixon JA, Durum SK, (2010) Interleukin-7 regulates Bim proapoptotic activity in peripheral T-cell survival. Mol Cell Biol 30: 590-600.
43. Kittipatarin C, Khaled AR, (2009) Ex vivo expansion of memory CD8 T cells from lymph nodes or spleen through in vitro culture with interleukin-7. J Immunol Methods 344: 45-57.
44. Kang J, DiBenedetto B, Narayan K, Zhao H, Der SD, et al. (2004) STAT5 is required for thymopoiesis in a development stage-specific manner. J Immunol 173: 2307-2314.
45. Morcinek JC, Weisser C, Geissinger E, Schartl M, Wellbrock C, (2002) Activation of STAT5 triggers proliferation and contributes to anti-apoptotic signalling mediated by the oncogenic Xmrk kinase. Oncogene 21: 1668-1678.
46. Goetz CA, Harmon IR, O'Neil JJ, Burchill MA, Farrar MA, (2004) STAT5 activation underlies IL7 receptor-dependent B cell development. J Immunol 172: 4770-4778.
47. Mochizuki T, Kitanaka C, Noguchi K, Muramatsu T, Asai A, et al. (1999) Physical and functional interactions between Pim-1 kinase and Cdc25A phosphatase. Implications for the Pim-1-mediated activation of the c-Myc signaling pathway. J Biol Chem 274: 18659-18666.
48. Cen B, Mahajan S, Zemskova M, Beharry Z, Lin YW, et al. (2010) Regulation of Skp2 levels by the Pim-1 protein kinase. J Biol Chem 285: 29128-29137.
49. Jacobs H, Krimpenfort P, Haks M, Allen J, Blom B, et al. (1999) PIM1 reconstitutes thymus cellularity in interleukin 7- and common gamma chain-mutant mice and permits thymocyte maturation in Rag- but not CD3gamma-deficient mice. J Exp Med 190: 1059-1068.
50. Mikkers H, Nawijn M, Allen J, Brouwers C, Verhoeven E, et al. (2004) Mice deficient for all PIM kinases display reduced body size and impaired responses to hematopoietic growth factors. Mol Cell Biol 24: 6104-6115.
51. Weitzman JB, Fiette L, Matsuo K, Yaniv M, (2000) JunD protects cells from p53-dependent senescence and apoptosis. Mol Cell 6: 1109-1119.
52. Lamb JA, Ventura JJ, Hess P, Flavell RA, Davis RJ, (2003) JunD mediates survival signaling by the JNK signal transduction pathway. Mol Cell 11: 1479-1489.
53. Meixner A, Karreth F, Kenner L, Wagner EF, (2004) JunD regulates lymphocyte proliferation and T helper cell cytokine expression. EMBO J 23: 1325-1335.
54. Xiao L, Rao JN, Zou T, Liu L, Marasa BS, et al. (2007) Induced JunD in intestinal epithelial cells represses CDK4 transcription through its proximal promoter region following polyamine depletion. Biochem J 403: 573-581.
55. Hernandez JM, Floyd DH, Weilbaecher KN, Green PL, Boris-Lawrie K, (2008) Multiple facets of junD gene expression are atypical among AP-1 family members. Oncogene 27: 4757-4767.
56. Hartman TR, Qian S, Bolinger C, Fernandez S, Schoenberg DR, et al. (2006) RNA helicase A is necessary for translation of selected messenger RNAs. Nat Struct Mol Biol 13: 509-516.
57. Musti AM, Treier M, Peverali FA, Bohmann D, (1996) Differential regulation of c-Jun and JunD by ubiquitin-dependent protein degradation. Biol Chem 377: 619-624.
58. Yazgan O, Pfarr CM, (2002) Regulation of two JunD isoforms by Jun N-terminal kinases. J Biol Chem 277: 29710-29718.
59. Sasson SC, Zaunders JJ, Kelleher AD, (2006) The IL-7/IL-7 receptor axis: understanding its central role in T-cell homeostasis and the challenges facing its utilization as a novel therapy. Curr Drug Targets 7: 1571-1582.
60. Jiang Q, Li WQ, Hofmeister RR, Young HA, Hodge DR, et al. (2004) Distinct regions of the interleukin-7 receptor regulate different Bcl2 family members. Mol Cell Biol 24: 6501-6513.
61. Rahman Z, Yoshikawa H, Nakajima Y, Tasaka K, (2001) Down-regulation of Pim-1 and Bcl-2 is accompanied with apoptosis of interleukin-6-depleted mouse B-cell hybridoma 7TD1 cells. Immunol Lett 75: 199-208.
62. Zou T, Rao JN, Liu L, Xiao L, Yu TX, et al. (2010) Polyamines regulate the stability of JunD mRNA by modulating the competitive binding of its 3′ untranslated region to HuR and AUF1. Mol Cell Biol 30: 5021-5032.
63. Azfer A, Niu J, Rogers LM, Adamski FM, Kolattukudy PE, (2006) Activation of endoplasmic reticulum stress response during the development of ischemic heart disease. Am J Physiol Heart Circ Physiol 291: H1411-H1420.
64. Jaganathan S, Yue P, Turkson J, (2010) Enhanced sensitivity of pancreatic cancer cells to concurrent inhibition of aberrant signal transducer and activator of transcription 3 and epidermal growth factor receptor or Src. J Pharmacol Exp Ther 333: 373-381.
65. Dignam JD, Lebovitz RM, Roeder RG, (1983) Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res 11: 1475-1489.
66. Storey JD, Tibshirani R, (2003) Statistical significance for genomewide studies. Proc Natl Acad Sci U S A 100: 9440-9445.
67. Boyle EI, Weng S, Gollub J, Jin H, Botstein D, et al. (2004) GO::TermFinder-open source software for accessing Gene Ontology information and finding significantly enriched Gene Ontology terms associated with a list of genes. Bioinformatics 20: 3710-3715.