The unique hypusine modification of eIF5A promotes islet β cell inflammation and dysfunction in mice

Journal of Clinical Investigation

Volumn 120, Issue 6, 2010, Pages 2156-2170

  Maier, Bernhard ^a   Ogihara, Takeshi ^a   Trace, Anthony P ^b   Tersey, Sarah A ^a   Robbins, Reiesha D ^a,b   Chakrabarti, Swarup K ^c   Nunemaker, Craig S ^b   Stull, Natalie D ^a   Taylor, Catherine A ^d   Thompson, John E ^d,e   Dondero, Richard S ^e   Lewis, Eli C ^f   Dinarello, Charles A ^f   Nadler, Jerry L ^c   Mirmira, Raghavendra G ^a  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

^c EASTERN VIRGINIA MEDICAL SCHOOL   (United States)

^d UNIVERSITY OF WATERLOO   (Canada)

^e Senesco Technologies Inc   (United States)

^f UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EXPORTIN 1; HYPUSINE; INDUCIBLE NITRIC OXIDE SYNTHASE; INITIATION FACTOR 5A; STREPTOZOCIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL CYCLE PROGRESSION; CELL VIABILITY; CONTROLLED STUDY; GLUCOSE INTOLERANCE; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PANCREAS ISLET CELL FUNCTION; PRIORITY JOURNAL; STREPTOZOCIN DIABETES;

ANIMALS; ISLETS OF LANGERHANS; LYSINE; MICE; MICE, INBRED C57BL; MICE, INBRED NOD; MICE, SCID; PEPTIDE INITIATION FACTORS; RNA-BINDING PROTEINS;

EID: 77953186469     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI38924     Document Type: Article

References (81)

1. Prentki M, Nolan CJ. Islet beta cell failure in type 2 diabetes. J Clin Invest. 2006;116(7):1802-1812. (Pubitemid 44033300)
2. Mathis D, Vence L, Benoist C. beta-Cell death during progression to diabetes. Nature. 2001; 414(6865):792-798. (Pubitemid 34000782)
3. Spranger J, et al. Inflammatory cytokines and the risk to develop type 2 diabetes: results of the prospective population-based European Prospective Investigation into Cancer and Nutrition (EPIC)-Potsdam Study. Diabetes. 2003;52(3):812-817. (Pubitemid 36323590)
4. Sauter NS, Schulthess FT, Galasso R, Castellani LW, Maedler K. The antiinflammatory cytokine interleukin-1 receptor antagonist protects from high-fat diet-induced hyperglycemia. Endocrinology. 2008;149(5):2208-2218. (Pubitemid 351574505)
5. Larsen CM. Interleukin-1-receptor antagonist in type 2 diabetes mellitus. N Engl J Med. 2007; 356(15):1517-1526. (Pubitemid 46588416)
6. Eizirik DL, Mandrup-Poulsen T. A choice of death - the signal-transduction of immune-mediated betacell apoptosis. Diabetologia. 2001;44(12):2115-2133. (Pubitemid 34015464)
7. Leist M, et al. Inhibition of mitochondrial ATP generation by nitric oxide switches apoptosis to necrosis. Exp Cell Res. 1999;249(2):396-403. (Pubitemid 29397947)
8. Koster JC, Marshall BA, Ensor N, Corbett JA, Nichols CG. Targeted overactivity of beta cell K(ATP) channels induces profound neonatal diabetes. Cell. 2000;100(6):645-654.
9. Chambers KT, Unverferth JA, Weber SM, Wek RC, Urano F, Corbett JA. The role of nitric oxide and the unfolded protein response in cytokine-induced beta-cell death. Diabetes. 2008;57(1):124-132.
10. Collier JJ, Fueger PT, Hohmeier HE, Newgard CB. Pro- and antiapoptotic proteins regulate apoptosis but do not protect against cytokine-mediated cytotoxicity in rat islets and beta-cell lines. Diabetes. 2006;55(5):1398-1406.
11. Larsen L, et al. Inhibition of histone deacetylases prevents cytokine-induced toxicity in beta cells. Diabetologia. 2007;50(4):779-789. (Pubitemid 46355819)
12. Steer SA, Scarim AL, Chambers KT, Corbett JA. Interleukin-1 stimulates beta-cell necrosis and release of the immunological adjuvant HMGB1. PLoS Med. 2006;3(2):e17.
13. Facchiano AM, et al. Homology modelling of the human eukaryotic initiation factor 5A (eIF-5A). Protein Eng. 2001;14(11):881-890.
14. Cooper HL, Park MH, Folk JE, Safer B, Braverman R. Identification of the hypusine-containing protein hy+ as translation initiation factor eIF-4D. Proc Natl Acad Sci U S A. 1983;80(7):1854-1857.
15. Park MH, Nishimura K, Zanelli CF, Valentini SR. Functional significance of eIF5A and its hypusine modification in eukaryotes. Amino Acids. 2010; 38(2):491-500.
16. Park MH, Wolff EC, Lee YB, Folk JE. Antiproliferative effects of inhibitors of deoxyhypusine synthase. Inhibition of growth of Chinese hamster ovary cells by guanyl diamines. J Biol Chem. 1994;269(45):27827-27832. (Pubitemid 24982988)
17. Caraglia M, et al. The eukaryotic initiation factor 5A is involved in the regulation of proliferation and apoptosis induced by interferon-alpha and EGF in human cancer cells. J Biochem. 2003;133(6):757-765. (Pubitemid 36898647)
18. Taylor CA, et al. Role of eIF5A in TNF-alpha-mediated apoptosis of lamina cribrosa cells. Invest Ophthalmol Vis Sci. 2004;45(10):3568-3576.
19. Taylor CA, et al. Eukaryotic translation initiation factor 5A induces apoptosis in colon cancer cells and associates with the nucleus in response to tumour necrosis factor alpha signalling. Exp Cell Res. 2007;313(3):437-449.
20. Li AL, et al. A novel eIF5A complex functions as a regulator of p53 and p53-dependent apoptosis. J Biol Chem. 2004;279(47):49251-49258.
21. Moore CC, et al. Eukaryotic translation initiation factor 5a small interference rna-liposome complexes reduce inflammation and increase survival in murine models of severe sepsis and acute lung injury. J Infect Dis. 2008;198(9):1407-1414.
22. Maier LM, Wicker LS. Genetic susceptibility to type 1 diabetes. Curr Opin Immunol. 2005;17(6):601-608.
23. Grattan M, Mi QS, Meagher C, Delovitch TL. Congenic mapping of the diabetogenic locus Idd4 to a 5.2-cM region of chromosome 11 in NOD mice: identification of two potential candidate subloci. Diabetes. 2002;51(1):215-223. (Pubitemid 34518001)
24. Kruse M, et al. Inhibition of CD83 cell surface expression during dendritic cell maturation by interference with nuclear export of CD83 mRNA. J Exp Med. 2000;191(9):1581-1590. (Pubitemid 30257354)
25. Clement PM, Johansson HE, Wolff EC, Park MH. Differential expression of eIF5A-1 and eIF5A-2 in human cancer cells. FEBS J. 2006;273(6):1102-1114. (Pubitemid 43345032)
26. Jenkins ZA, Haag PG, Johansson HE. Human eIF5A2 on chromosome 3q25-q27 is a phylogenetically conserved vertebrate variant of eukaryotic translation initiation factor 5A with tissue-specific expression. Genomics. 2001;71(1):101-109.
27. Lukic ML, Stosic-Grujicic S, Shahin A. Effector mechanisms in low-dose streptozotocin-induced diabetes. Dev Immunol. 1998;6(1-2):119-128. (Pubitemid 28409872)
28. Calderon B, Suri A, Miller MJ, Unanue ER. Dendritic cells in islets of Langerhans constitutively present beta cell-derived peptides bound to their class II MHC molecules. Proc Natl Acad Sci U S A. 2008;105(16):6121-6126. (Pubitemid 351758409)
29. Lenzen S. The mechanisms of alloxan- and streptozotocin-induced diabetes. Diabetologia. 2008;51(2):216-226.
30. Flodstrom M, Tyrberg B, Eizirik DL, Sandler S. Reduced sensitivity of inducible nitric oxide synthase-deficient mice to multiple low-dose streptozotocin-induced diabetes. Diabetes. 1999;48(4):706-713. (Pubitemid 29153068)
31. Henquin JC, Nenquin M, Stiernet P, Ahren B. In vivo and in vitro glucose-induced biphasic insulin secretion in the mouse: pattern and role of cytoplasmic Ca2+ and amplification signals in betacells. Diabetes. 2006;55(2):441-451. (Pubitemid 43343275)
32. Kolb H, Mandrup-Poulsen T. An immune origin of type 2 diabetes? Diabetologia. 2005;48(6):1038-1050. (Pubitemid 40909636)
33. Corbett JA, McDaniel ML. Intraislet release of interleukin 1 inhibits beta cell function by inducing beta cell expression of inducible nitric oxide synthase. J Exp Med. 1995;181(2):559-568.
34. Chen KY, Liu AY. Biochemistry and function of hypusine formation on eukaryotic initiation factor 5A. Biol Signals. 1997;6(3):105-109.
35. Dong Z, et al. Modulation of differentiation-related gene 1 expression by cell cycle blocker mimosine, revealed by proteomic analysis. Mol Cell Proteomics. 2005;4(7):993-1001. (Pubitemid 41309156)
36. Nishimura K, Murozumi K, Shirahata A, Park MH, Kashiwagi K, Igarashi K. Independent roles of eIF5A and polyamines in cell proliferation. Biochem J. 2005;385(pt 3):779-785. (Pubitemid 40208839)
37. Landau G, Bercovich Z, Park MH, Kahana C. The role of polyamines in supporting growth of mammalian cells is mediated through their requirement for translation initiation and elongation. J Biol Chem. 2010;285(17):12474-12481.
38. Herbst M, Sasse P, Greger R, Yu H, Hescheler J, Ullrich S. Membrane potential dependent modulations of calcium oscillations in insulin-secreting INS-1 cells. Cell Calcium. 2002;31(3):115-126. (Pubitemid 34752895)
39. Corbett JA, McDaniel ML. The use of aminoguanidine, a selective inos inhibitor, to evaluate the role of nitric oxide in the development of autoimmune diabetes. Methods. 1996;10(1):21-30.
40. Duncan RF, Hershey JW. Changes in eIF-4D hypusine modification or abundance are not correlated with translational repression in HeLa cells. J Biol Chem. 1986;261(27):12903-12906.
41. Gerner EW, Mamont PS, Bernhardt A, Siat M. Post-translational modification of the protein-synthesis initiation factor eIF-4D by spermidine in rat hepatoma cells. Biochem J. 1986;239(2):379-386. (Pubitemid 16008458)
42. Parker R, Sheth U. P bodies and the control of mRNA translation and degradation. Mol Cell. 2007; 2007;25(5):635-646. (Pubitemid 46341926)
43. Jao DL, Yu Chen K. Subcellular localization of the hypusine-containing eukaryotic initiation factor 5A by immunofluorescent staining and green fluorescent protein tagging. J Cell Biochem. 2002;86(3):590-600.
44. Shi XP, Yin KC, Zimolo ZA, Stern AM, Waxman L. The subcellular distribution of eukaryotic translation initiation factor, eIF-5A, in cultured cells. Exp Cell Res. 1996;225(2):348-356. (Pubitemid 26183952)
45. Rosorius O, Reichart B, Kratzer F, Heger P, Dabauvalle MC, Hauber J. Nuclear pore localization and nucleocytoplasmic transport of eIF-5A: evidence for direct interaction with the export receptor CRM1. J Cell Sci. 1999;112(pt 14):2369-2380. (Pubitemid 29381027)
46. Lipowsky G, et al. Exportin 4: a mediator of a novel nuclear export pathway in higher eukaryotes. EMBO J. 2000;19(16):4362-4371. (Pubitemid 30623747)
47. Jin BF, et al. Proteomic analysis of ubiquitin-proteasome effects: insight into the function of eukaryotic initiation factor 5A. Oncogene. 2003;22(31):4819-4830.
48. Lee SB, Park JH, Kaevel J, Sramkova M, Weigert R, Park MH. The effect of hypusine modification on the intracellular localization of eIF5A. Biochem Biophys Res Commun. 2009;383(4):497-502.
49. Xu A, Chen KY. Hypusine is required for a sequence-specific interaction of eukaryotic initiation factor 5A with postsystematic evolution of ligands by exponential enrichment RNA. J Biol Chem. 2001;276(4):2555-2561. (Pubitemid 37376629)
50. Chow JC, Young DW, Golenbock DT, Christ WJ, Gusovsky F. Toll-like receptor-4 mediates lipopolysaccharide-induced signal transduction. J Biol Chem. 1999;274(16):10689-10692. (Pubitemid 129528264)
51. Schulthess FT, et al. CXCL10 impairs beta cell function and viability in diabetes through TLR4 signaling. Cell Metab. 2009;9(2):125-139.
52. Kemper WM, Berry KW, Merrick WC. Purification and properties of rabbit reticulocyte protein synthesis initiation factors M2Balpha and M2Bbeta. J Biol Chem. 1976;251(18):5551-5557.
53. Saini P, Eyler DE, Green R, Dever TE. Hypusine-containing protein eIF5A promotes translation elongation. Nature. 2009;459(7243):118-121.
54. Kang HA, Hershey JW. Effect of initiation factor eIF-5A depletion on protein synthesis and proliferation of Saccharomyces cerevisiae. J Biol Chem. 1994;269(6):3934-3940.
55. Chatterjee I, Gross SR, Kinzy TG, Chen KY. Rapid depletion of mutant eukaryotic initiation factor 5A at restrictive temperature reveals connections to actin cytoskeleton and cell cycle progression. Mol Genet Genomics. 2006;275(3):264-276. (Pubitemid 43357663)
56. Rahman-Roblick R, et al. p53 targets identified by protein expression profiling. Proc Natl Acad Sci U S A. 2007;104(13):5401-5406.
57. Bevec D, et al. Inhibition of HIV-1 replication in lymphocytes by mutants of the Rev cofactor eIF-5A. Science. 1996;271(5257):1858-1860.
58. Kroncke KD, Fehsel K, Suschek C, Kolb-Bachofen V. Inducible nitric oxide synthase-derived nitric oxide in gene regulation, cell death and cell survival. Int Immunopharmacol. 2001;1(8):1407-1420.
59. Park MH. The post-translational synthesis of a polyamine-derived amino acid, hypusine, in the eukaryotic translation initiation factor 5A (eIF5A). J Biochem. 2006;139(2):161-169.
60. Gosslau A, Jao DL, Butler R, Liu AY, Chen KY. Thermal killing of human colon cancer cells is associated with the loss of eukaryotic initiation factor 5A. J Cell Physiol. 2009;219(2):485-493.
61. Takeuchi K, Nakamura K, Fujimoto M, Kaino S, Kondoh S, Okita K. Heat stress-induced loss of eukaryotic initiation factor 5A (eIF-5A) in a human pancreatic cancer cell line, MIA PaCa-2, analyzed by two-dimensional gel electrophoresis. Electrophoresis. 2002;23(4):662-669.
62. Elfgang C, Rosorius O, Hofer L, Jaksche H, Hauber J, Bevec D. Evidence for specific nucleocytoplasmic transport pathways used by leucine-rich nuclear export signals. Proc Natl Acad Sci U S A. 1999;96(11):6229-6234.
63. Hofmann W, et al. Cofactor requirements for nuclear export of Rev response element (RRE)- and constitutive transport element (CTE)-containing retroviral RNAs. An unexpected role for actin. J Cell Biol. 2001;152(5):895-910.
64. Schutz S, Chemnitz J, Spillner C, Frohme M, Hauber J, Kehlenbach RH. Stimulated expression of mRNAs in activated T cells depends on a functional CRM1 nuclear export pathway. J Mol Biol. 2006;358(4):997-1009.
65. Jang BC, et al. Leptomycin B, a metabolite of Streptomyces, inhibits the expression of inducible nitric oxide synthase in BV2 microglial cells. Int J Oncol. 2006;29(6):1509-1515.
66. Zanelli CF, et al. eIF5A binds to translational machinery components and affects translation in yeast. Biochem Biophys Res Commun. 2006;348(4):1358-1366.
67. Bleich D, Chen S, Zipser B, Sun D, Funk CD, Nadler JL. Resistance to type 1 diabetes induction in 12-lipoxygenase knockout mice. J Clin Invest. 1999;103(10):1431-1436.
68. McDuffie M, et al. Nonobese diabetic (NOD) mice congenic for a targeted deletion of 12/15-lipoxygenase are protected from autoimmune diabetes. Diabetes. 2008;57(1):199-208.
69. Hyon SH, Tracey KJ, Kaufman DB. Specific inhibition of macrophage-derived proinflammatory cytokine synthesis with a tetravalent guanylhydrazone CNI-1493 accelerates early islet graft function posttransplant. Transplant Proc. 1998;30(2):409-410.
70. Hohmeier HE, Mulder H, Chen G, Henkel-Rieger R, Prentki M, Newgard CB. Isolation of INS-1-derived cell lines with robust ATP-sensitive K+ channel-dependent and -independent glucose-stimulated insulin secretion. Diabetes. 2000;49(3):424-430. (Pubitemid 30131788)
71. Gotoh M, Ohzato H, Porter J, Maki T, Monaco AP. Crucial role of pancreatic ductal collagenase injection for isolation of pancreatic islets. Horm Metab Res Suppl. 1990;25:10-16.
72. Yang Z, Chen M, Ellett JD, Fialkow LB, Carter JD, Nadler JL. The novel anti-inflammatory agent lisofylline prevents autoimmune diabetic recurrence after islet transplantation. Transplantation. 2004;77(1):55-60. (Pubitemid 38116872)
73. Parreiras-E-Silva LT, Gomes MD, Oliveira EB, Costa-Neto CM. The N-terminal region of eukaryotic translation initiation factor 5A signals to nuclear localization of the protein. Biochem Biophys Res Commun. 2007;362(2):393-398.
74. Evans-Molina C, et al. PPAR-{gamma} activation restores islet function in diabetic mice through reduction of er stress and maintenance of euchromatin structure. Mol Cell Biol. 2009;29(8):2053-2067.
75. Kulkarni RN, Jhala US, Winnay JN, Krajewski S, Montminy M, Kahn CR. PDX-1 haploinsufficiency limits the compensatory islet hyperplasia that occurs in response to insulin resistance. J Clin Invest. 2004;114(6):828-836. (Pubitemid 39578742)
76. Francis J, Chakrabarti SK, Garmey JC, Mirmira RG. Pdx-1 links histone H3-Lys-4 methylation to RNA polymerase II Elongation during activation of insulin transcription. J Biol Chem. 2005;280(43):36244-36253. (Pubitemid 41633897)
77. Sun BK, Deaton AM, Lee JT. A transient heterochromatic state in Xist preempts X inactivation choice without RNA stabilization. Mol Cell. 2006;21(5):617-628.
78. Dignam JD, Lebovitz RM, Roeder RG. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 1983;11(5):1475-1489.
79. Evans-Molina C, Garmey JC, Ketchum RJ, Brayman K, Deng S, Mirmira RG. Glucose regulation of insulin gene transcription and pre-mRNA processing in human islets. Diabetes. 2007;56(3):827-835. (Pubitemid 46348457)
80. Iype T, et al. Mechanism of insulin gene regulation by the pancreatic transcription factor Pdx-1: application of pre-mRNA analysis and chromatin immunoprecipitation to assess formation of functional transcriptional complexes. J Biol Chem. 2005;280(17):16798-16807. (Pubitemid 41389138)
81. Deering TG, Ogihara T, Trace AP, Maier B, Mirmira RG. Methyltransferase Set7/9 maintains transcription and euchromatin structure at islet-enriched genes. Diabetes. 2009;58(1):185-193.