Proteomics analysis of cytokine-induced dysfunction and death in insulin-producing INS-1E cells: New insights into the pathways involved

Molecular and Cellular Proteomics

Volumn 6, Issue 12, 2007, Pages 2180-2199

  D'Hertog, Wannes ^a   Overbergh, Lut ^a   Lage, Kasper ^b   Ferreira, Gabriela Bonfim ^a   Maris, Michael ^a   Gysemans, Conny ^a   Flamez, Daisy ^c   Cardozo, Alessandra Kupper ^c,d   Van den Bergh, Gert ^e   Schoofs, Liliane ^a,e   Arckens, Lut ^a,e   Moreau, Yves ^e   Hansen, Daniel Aaen ^b   Eizirik, Decio Laks ^c   Waelke, Ettienne ^a   Mathieu, Chantal ^a  

^a UNIVERSITY HOSPITALS LEUVEN   (Belgium)

^b TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^c UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^d FNRS   (Belgium)

^e UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; INSULIN;

AMINO ACID SEQUENCE; ANIMAL CELL; APOPTOSIS; ARTICLE; CELL VIABILITY; DIABETOGENESIS; ENDOPLASMIC RETICULUM; HUMAN; HUMAN CELL; INSULIN DEPENDENT DIABETES MELLITUS; INSULIN RELEASE; INSULIN SYNTHESIS; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN METABOLISM; PROTEOMICS; REGULATORY MECHANISM; RNA METABOLISM; UNINDEXED SEQUENCE;

EID: 38349025873     PISSN: 15359476     EISSN: None     Source Type: Journal    
DOI: 10.1074/mcp.M700085-MCP200     Document Type: Article

References (62)

1. Mathis, D., Vence, L., and Benoist, C. (2001) β-Cell death during progression to diabetes. Nature 414, 792-798
2. Eizirik, D. L., and Mandrup-Poulsen, T. (2001) A choice of death - the signal-transduction of immune-mediated beta-cell apoptosis. Diabetologia 44, 2115-2133
3. Cnop, M., Welsh, N., Jonas, J. C., Jorns, A., Lenzen, S., and Eizirik, D. L. (2005) Mechanisms of pancreatic β-cell death in type 1 and type 2 diabetes: many differences, few similarities. Diabetes 54, Suppl. 2, S97-S107
4. Hostens, K., Pavlovic, D., Zambre, Y., Ling, Z., Van Schravendijk, C., Eizirik, D. L., and Pipeleers, D. G. (1999) Exposure of human islets to cytokines can result in disproportionately elevated proinsulin release. J. Clin. Investig. 104, 67-72
5. Ohara-Imaizumi, M., Cardozo, A. K., Kikuta, T., Eizirik, D. L., and Nagamatsu, S. (2004) The cytokine interleukin-1β reduces the docking and fusion of insulin granules in pancreatic β-cells, preferentially decreasing the first phase of exocytosis. J. Biol. Chem. 279, 41271-41274
6. Borjesson, A., and Carlsson, C. (2007) Altered proinsulin conversion in rat pancreatic islets exposed long-term to various glucose concentrations or interleukin-1β. J. Endocrinol. 192, 381-387
7. Cardozo, A. K., Heimberg, H., Heremans, Y., Leeman, R., Kutlu, B., Kruhoffer, M., Omtoft, T., and Eizirik, D. L. (2001) A comprehensive analysis of cytokine-induced and nuclear factor-κB-dependent genes in primary rat pancreatic β-cells. J. Biol. Chem. 276, 48879-48886
8. Delaney, C. A., Pavlovic, D., Hoorens, A., Pipeleers, D. G., and Eizirik, D. L. (1997) Cytokines induce deoxyribonucleic acid strand breaks and apoptosis in human pancreatic islet cells. Endocrinology 138, 2610-2614
9. Kutlu, B., Cardozo, A. K., Darville, M. I., Kruhoffer, M., Magnusson, N., Orntoft, T., and Eizirik, D. L. (2003) Discovery of gene networks regulating cytokine-induced dysfunction and apoptosis in insulin-producing INS-1 cells. Diabetes 52, 2701-2719
10. Papaccio, G., Graziano, A., D'Aquino, R., Valiante, S., and Naro, F. (2005) A biphasic role of nuclear transcription factor (NF)-κB in the islet β-cell apoptosis induced by interleukin (IL)-1β. J. Cell Physiol. 204, 124-130
11. Gysemans, C. A., Ladriere, L., Callewaert, H., Rasschaert, J., Flamez, D., Levy, D. E., Matthys, P., Eizirik, D. L., and Mathieu, C. (2005) Disruption of the γ-interferon signaling pathway at the level of signal transducer and activator of transcription-1 prevents immune destruction of β-cells. Diabetes 54, 2396-2403
12. Gygi, S. P., Rochon, Y., Franza, B. R., and Aebersold, R. (1999) Correlation between protein and mRNA abundance in yeast. Mol. Cell. Biol. 19, 1720-1730
13. Apweiler, R., Hermjakob, H., and Sharon, N. (1999) On the frequency of protein glycosylation, as deduced from analysis of the SWISS-PROT database. Biochim. Biophys. Acta 1473, 4-8
14. Mann, M., and Jensen, O. N. (2003) Proteomic analysis of post-translational modifications. Nat. Biotechnol. 21, 255-261
15. Sparre, T., Christensen, U. B., Mose, L. P., Fey, S. J., Wrzesinski, K., Roepstorff, P., Mandrup-Poulsen, T., Pociot, F., Karlsen, A. E., and Nerup, J. (2002) IL-1β induced protein changes in diabetes prone BB rat islets of Langerhans identified by proteome analysis. Diabetologia 45, 1550-1561
16. Sparre, T., Christensen, U. B., Gotfredsen, C. F., Larsen, P. M., Fey, S. J., Hjemo, K., Roepstorff, P., Pociot, F., Karlsen, A. E., and Nerup, J. (2004) Changes in expression of IL-1β influenced proteins in transplanted islets during development of diabetes in diabetes-prone BB rats. Diabetologia 47, 892-908
17. Sparre, T., Larsen, M. R., Heding, P. E., Karlsen, A. E., Jensen, O. N., and Pociot, F. (2005) Unraveling the pathogenesis of type 1 diabetes with proteomics: present and future directions. Mol. Cell. Proteomics 4, 441-457
18. Marouga, R., David, S., and Hawkins, E. (2005) The development of the DIGE system: 2D fluorescence difference gel analysis technology. Anal. Bioanal. Chem. 382, 669-678
19. D'Hertog, W., Mathieu, C., and Overbergh, L. (2006) Type 1 diabetes: entering the proteomic era. Expert Rev. Proteomics 3, 223-236
20. Tonge, R., Shaw, J., Middleton, B., Rowlinson, R., Rayner, S., Young, J., Pognan, F., Hawkins, E., Currie, I., and Davison, M. (2001) Validation and development of fluorescence two-dimensional differential gel electro-phoresis proteomics technology. Proteomics 1, 377-396
21. Merglen, A., Theander, S., Rubi, B., Chaffard, G., Wollheim, C. B., and Maechler, P. (2004) Glucose sensitivity and metabolism-secretion coupling studied during two-year continuous culture in INS-1E insulinoma cells. Endocrinology 145, 667-678
22. Ortis, F., Cardozo, A. K., Crispim, D., Storling, J., Mandrup-Poulsen, T., and Eizirik, D. L. (2006) Cytokine-induced proapoptotic gene expression in insulin-producing cells is related to rapid, sustained, and nonoscillatory nuclear factor-κB activation. Mol. Endocrinol. 20, 1867-1879
23. Hoorens, A., Van de Casteele, M., Kloppel, G., and Pipeleers, D. (1996) Glucose promotes survival of rat pancreatic β cells by activating synthesis of proteins which suppress a constitutive apoptotic program. J. Clin. Investig. 98, 1568-1574
24. 15N]nitrate in biological fluids. Anal. Biochem. 126, 131-138
25. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254
26. Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D. J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402
27. Hinsby, A. M., Kiemer, L., Karlberg, E. O., Lage, K., Fausboll, A., Juncker, A. S., Andersen, J. S., Mann, M., and Brunak, S. (2006) A wiring of the human nucleolus. Mol. Cell 22, 285-295
28. Lage, K., Karlberg, E. O., Storling, Z. M., Olason, P. I., Pedersen, A. G., Rigina, O., Hinsby, A. M., Turner, Z., Pociot, F., Tommerup, N., Moreau, Y., and Brunak, S. (2007) A human phenome-interactome network of protein complexes implicated in genetic disorders. Nat. Biotechnol. 25, 309-316
29. Li, D., and Roberts, R. (2001) WD-repeat proteins: structure characteristics, biological function, and their involvement in human diseases. CMLS Cell. Mol. Life Sci. 58, 2085-2097
30. DesMarais, V., Ghosh, M., Eddy, R., and Condeelis, J. (2005) Cofilin takes the lead. J. Cell Sci. 118, 19-26
31. Dan, C., Kelly, A., Bernard, O., and Minden, A. (2001) Cytoskeletal changes regulated by the PAK4 serine/threonine kinase are mediated by LIM kinase 1 and cofilin. J. Biol. Chem. 276, 32115-32121
32. Grantham, J., Ruddock, L. W., Roobol, A., and Carden, M. J. (2002) Eukaryotic chaperonin containing T-complex polypeptide 1 interacts with filamentous actin and reduces the initial rate of actin polymerization in vitro. Cell Stress Chaperones 7, 235-242
33. Verboven, C., Bogaerts, I., Waelkens, E., Rabijns, A., Van Baelen, H., Bouillon, R., and De Ranter, C. (2003) Actin-DBP: the perfect structural fit? Acta Crystallogr. Sect. D Biol. Crystallogr. 59, 263-273
34. Hansen, B. S., Nielsen, J. H., Linde, S., Spines, G. A., Welinder, B. S., Mandrup-Poulsen, T., and Nerup, J. (1988) Effect of interleukin-1 on the biosynthesis of proinsulin and insulin in isolated rat pancreatic islets. Biomed. Biochim. Acta 47, 305-309
35. Lee, K. K., Murakawa, M., Takahashi, S., Tsubuki, S., Kawashima, S., Sakamaki, K., and Yonehara, S. (1998) Purification, molecular cloning, and characterization of TRP32, a novel thloredoxin-related mammalian protein of 32 kDa. J. Biol. Chem. 273, 19160-19166
36. Laybutt, D. R., Preston, A. M., Akerfeldt, M. C., Kench, J. G., Busch, A. K., Biankin, A. V., and Biden, T. J. (2007) Endoplasmic reticulum stress contributes to beta cell apoptosis in type 2 diabetes. Diabetologia 50, 752-763
37. Nagano, K., Masters, J. R., Akpan, A., Yang, A., Corless, S., Wood, C., Hestia, C., Zvelebil, M., Cramer, R., and Naaby-Hansen, S. (2004) Differential protein synthesis and expression levels in normal and neoplastic human prostate cells and their regulation by type I and II interferons. Oncogene 23, 1693-1703
38. Pirot, P., Eizirik, D. L., and Cardozo, A. K. (2006) Interferon-γ potentiates encloplasmic reticulum stress-induced death by reducing pancreatic beta cell defence mechanisms. Diabetologia 49, 1229-1236
39. Freiden, P. J., Gaut, J. R., and Hendershot, L. M. (1992) Interconversion of three differentially modified and assembled forms of BiP. EMBO J. 11, 63-70
40. Hendershot, L. M., Ting, J., and Lee, A. S. (1988) Identity of the immunoglobulin heavy-chain-binding protein with the 78,000-dafton glucose-regulated protein and the role of posttranslational modifications in its binding function. Mol. Cell. Biol. 8, 4250-4256
41. Hendershot, L. M. (2004) The ER function BiP is a master regulator of ER function. Mt. Sinai J. Med. 71, 289-297
42. Nakatani, Y., Kaneto, H., Kawamori, D., Yoshiuchi, K, Hatazaki, M., Matsuoka, T. A., Ozawa, K., Ogawa, S., Hori, M., Yamasaki, Y., and Matsuhisa, M. (2005) Involvement of encloplasmic reticulum stress in insulin resistance and diabetes. J. Biol. Chem. 280, 847-851
43. Wu, S. J., Liu, F. H., Hu, S. M., and Wang, C. (2001) Different combinations of the heat-shock cognate protein 70 (hsc70) C-terminal functional groups are utilized to interact with distinct tetratricopeptide repeat-containing proteins. Biochem. J. 359, 419-426
44. Lasunskaia, E. B., Fridlianskaia, I. I., Guzhova, I. V., Bozhkov, V. M., and Margulis, B. A. (1997) Accumulation of major stress protein 70kDa protects myeloid and lymphoid cells from death by apoptosis. Apoptosis 2, 156-163
45. John, N. E., Andersen, H. U., Fey, S. J., Larsen, P. M., Roepstorff, P., Larsen, M. R., Pociot, F., Karlsen, A. E., Nerup, J., Green, I. C., and Mandrup-Poulsen, T. (2000) Cytokine- or chemically derived nitric oxide alters the expression of proteins detected by two-dimensional gel electrophoresis in neonatal rat islets of Langerhans. Diabetes 49, 1819-1829
46. Jolly, C., and Morimoto, R. I. (2000) Role of the heat shock response and molecular chaperones in oncogenesis and cell death. J. Natl. Cancer Inst. 92, 1564-1572
47. Wadhwa, R., Takano, S., Kaur, K., Deocaris, C. C., Pereira-Smith, O. M., Reddel, R. R., and Kaul, S. C. (2006) Upregulation of mortalin/mthsp70/ Grp75 contributes to human carcinogenesis. Int. J. Cancer 118, 2973-2980
48. Bast, A., Wolf, G., Oberbaumer, I., and Walther, R. (2002) Oxidative and nitrosative stress induces peroxiredoxins in pancreatic beta cells. Diabetologia 45, 867-876
49. Kang, S. W., Chae, H. Z., Sao, M. S., Kim, K., Baines, I. C., and Rhee, S. G. (1998) Mammalian peroxiredoxin isoforms can reduce hydrogen peroxide generated in response to growth factors and tumor necrosis factor-α. J. Biol. Chem. 273, 6297-6302
50. Thiede, B., Siejak, F., Dimmler, C., and Rudel, T. (2002) Prediction of translocation and cleavage of heterogeneous ribonuclear proteins and Rho guanine nucleotide dissociation inhibitor 2 during apoptosis by subcellular proteome analysis. Proteomics 2, 996-1006
51. Bomsztyk, K., Van Seuningen, I., Suzuki, H., Denisenko, O., and Ostrowski, J. (1997) Diverse molecular interactions of the hnRNP K protein. FEBS Lett. 403, 113-115
52. Chang, P. C., Chi, C. W., Chau, G. Y., Li, F. Y., Tsai, Y. H., Wu, J. C., and Wu Lee, Y. H. (2006) DDX3, a DEAD box RNA helicase, is deregulated in hepatitis virus-associated hepatocellular carcinoma and is involved in cell growth control. Oncogrene 25, 1991-2003
53. Cardozo, A. K., Kruhoffer, M., Leeman, R., Orntoft, T., and Eizirik, D. L. (2001) Identification of novel cytokine-induced genes in pancreatic β-cells by high-density oligonucleotide arrays. Diabetes 50, 909-920
54. Eizirik, D. L., Kutlu, B., Rasschaert, J., Darville, M., and Cardozo, A. K. (2003) Use of microarray analysis to unveil transcription factor and gene networks contributing to β cell dysfunction and apoptosis. Ann. N. Y. Acad. Sci. 1005, 55-74
55. Rasschaert, J., Liu, D., Kutlu, B., Cardozo, A. K., Kruhoffer, M., Orntoft, T. F., and Eizirik, D. L. (2003) Global profiling of double stranded RNA-and IFN-γ-induced genes in rat pancreatic beta cells. Diabetologia 46, 1641-1657
56. Ylipaasto, P., Kutlu, B., Rasilainen, S., Rasschaert, J., Salmela, K., Teerijoki, H., Korsgren, O., Lahesmaa, R., Hovi, T., Eizirik, D. L., Otonkoski, T., and Roivainen, M. (2005) Global profiling of coxsackievirus- and cytokine-induced gene expression in human pancreatic islets. Diabetologia 48, 1510-1522
57. Cardozo, A. K., Proost, P., Gysemans, C., Chen, M. C., Mathieu, C., and Eizirik, D. L. (2003) IL-10 and IFN-γ induce the expression of diverse chemokines and IL-15 in human and rat pancreatic islet cells, and in islets from pre-diabetic NOD mice. Diabetologia 46, 255-266
58. Rasschaert, J., Ladriere, L., Urbain, M., Dogusan, Z., Katabua, B., Sato, S., Akira, S., Gysemans, C., Mathieu, C., and Eizirik, D. L. (2005) Toll-like receptor 3 and STAT-1 contribute to double-stranded RNA+ interferon-γ-induced apoptosis in primary pancreatic β-cells. J. Biol. Chem. 280, 33984-33991
59. Larsen, C. M., Faulenbach, M., Vaag, A., Volund, A., Ehses, J. A., Seifert, B., Mandrup-Poulsen, T., and Donath, M. Y. (2007) Interleukin-1-receptor antagonist in type 2 diabetes mellitus. N. Engl. J. Med. 356, 1517-1526
60. Maedler, K., Schumann, D. M., Sauter, N., Ellingsgaard, H., Bosco, D., Baertschiger, R., Iwakura, Y., Oberholzer, J., Wollheim, C. B., Gauthier, B. R., and Donath, M. Y. (2006) Low concentration of interieukin-1β induces FLICE-inhibitory protein-mediated β-cell proliferation in human pancreatic islets. Diabetes 55, 2713-2722
61. Welsh, N., Cnop, M., Kharroubi, I., Bugliani, M., Lupi, R., Marchetti, P., and Eizirik, D. L. (2005) Is there a role for locally produced interleukin-1 in the deleterious effects of high glucose or the type 2 diabetes milieu to human pancreatic islets? Diabetes 54, 3238-3244
62. Hoorens, A., Stange, G., Pavlovic, D., and Pipeleers, D. (2001) Distinction between interleukin-1-induced necrosis and apoptosis of islet cells. Diabetes 50, 551-557