Coordinate changes in histone modifications, mRNA levels, and metabolite profiles in clonal INS-1 832/13 β-cells accompany functional adaptations to lipotoxicity

Journal of Biological Chemistry

Volumn 288, Issue 17, 2013, Pages 11973-11987

  Malmgren, Siri ^a   Spégel, Peter ^a   Danielsson, Anders P H ^a   Nagorny, Cecilia L ^a   Andersson, Lotta E ^a   Nitert, Marloes Dekker ^b   Ridderstrale, Martin ^a   Mulder, Hindrik ^a   Ling, Charlotte ^a  

^a LUND UNIVERSITY HOSPITAL   (Sweden)

^b UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

DIFFERENTIALLY EXPRESSED GENE; EPIGENETIC REGULATION; FATTY ACID METABOLISM; FUNCTIONAL ADAPTATION; GLUCOSE-STIMULATED INSULIN SECRETIONS; HISTONE MODIFICATION; METABOLITE PROFILING; TRICARBOXYLIC ACID CYCLE;

BIOCHEMISTRY; BIOMOLECULES; BIOSYNTHESIS; CYTOLOGY; GENE EXPRESSION; GLUCOSE; INSULIN; LIPIDS; METABOLITES; NUCLEIC ACIDS; PALMITIC ACID; PHYSIOLOGY; UNSATURATED FATTY ACIDS;

CLONE CELLS;

AMINOACYL TRANSFER RNA; MESSENGER RNA;

ARTICLE; CASR GENE; CELL VIABILITY; CHROMATIN IMMUNOPRECIPITATION; CLONAL VARIATION; CONTROLLED STUDY; DNA REPLICATION; DOWN REGULATION; EPIGENETICS; FATTY ACID METABOLISM; GENE; GENE EXPRESSION; GLUCOSE UTILIZATION; HISTONE MODIFICATION; HMGCS1 GENE; HUMAN; HUMAN CELL; IDI1 GENE; INSIG1 GENE; INSULIN RELEASE; LIPOTOXICITY; LSS GENE; MICROARRAY ANALYSIS; NON INSULIN DEPENDENT DIABETES MELLITUS; PANCREAS ISLET BETA CELL; PECI GENE; PRIORITY JOURNAL; STEROIDOGENESIS; UPREGULATION;

ANIMALS; CELL LINE, TUMOR; CITRIC ACID CYCLE; ENZYME INHIBITORS; EPIGENESIS, GENETIC; HISTONES; HUMANS; INSULIN; INSULIN-SECRETING CELLS; OXYGEN CONSUMPTION; PALMITIC ACID; PROTEIN PROCESSING, POST-TRANSLATIONAL; RATS; RNA, MESSENGER;

EID: 84876934840     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.422527     Document Type: Article

References (79)

1. Ferrannini, E., Gastaldelli, A., Miyazaki, Y., Matsuda, M., Pettiti, M., Natali, A., Mari, A., and DeFronzo, R. A. (2003) Predominant role of reducedβ-cell sensitivity to glucose over insulin resistance in impaired glucose tolerance. Diabetologia 46, 1211-1219
2. Jensen, M. V., Joseph, J. W., Ronnebaum, S. M., Burgess, S. C., Sherry, A. D., and Newgard, C. B. (2008) Metabolic cycling in control of glucosestimulated insulin secretion. Am. J. Physiol. Endocrinol. Metab. 295, E1287-1297
3. Kelly, R. P., Sutton, R., and Ashcroft, F. M. (1991) Voltage-activated calcium and potassium currents in human pancreaticβ-cells. J. Physiol. 443, 175-192
4. Lee, Y., Hirose, H., Ohneda, M., Johnson, J. H., McGarry, J. D., and Unger, R. H. (1994) β-Cell lipotoxicity in the pathogenesis of non-insulin-dependent diabetes mellitus of obese rats. Impairment in adipocyte-β-cell relationships. Proc. Natl. Acad. Sci. U. S. A. 91, 10878-10882
5. Prentki, M., Vischer, S., Glennon, M. C., Regazzi, R., Deeney, J. T., and Corkey, B. E. (1992) Malonyl-CoA and long chain acyl-CoA esters as metabolic coupling factors in nutrient-induced insulin secretion. J. Biol. Chem. 267, 5802-5810
6. Sako, Y., and Grill, V. E. (1990) A 48-hour lipid infusion in the rat timedependently inhibits glucose-induced insulin secretion and B cell oxidation through a process likely coupled to fatty acid oxidation. Endocrinology 127, 1580-1589
7. Carlsson, C., Borg, L. A., and Welsh, N. (1999) Sodium palmitate induces partial mitochondrial uncoupling and reactive oxygen species in rat pancreatic islets in vitro. Endocrinology 140, 3422-3428
8. Karaskov, E., Scott, C., Zhang, L., Teodoro, T., Ravazzola, M., and Volchuk, A. (2006) Chronic palmitate but not oleate exposure induces endoplasmic reticulum stress, which may contribute to INS-1 pancreaticβ-cell apoptosis. Endocrinology 147, 3398-3407
9. Kharroubi, I., Ladrière, L., Cardozo, A. K., Dogusan, Z., Cnop, M., and Eizirik, D. L. (2004) Free fatty acids and cytokines induce pancreaticβ-cell apoptosis by different mechanisms. Role of nuclear factor-κB and endoplasmic reticulum stress. Endocrinology 145, 5087-5096
10. Lupi, R., Dotta, F., Marselli, L., Del Guerra, S., Masini, M., Santangelo, C., Patané, G., Boggi, U., Piro, S., Anello, M., Bergamini, E., Mosca, F., Di Mario, U., Del Prato, S., and Marchetti, P. (2002) Prolonged exposure to free fatty acids has cytostatic and pro-apoptotic effects on human pancreatic islets. Evidence thatβ-cell death is caspase mediated, partially dependent on ceramide pathway, and Bcl-2 regulated. Diabetes 51, 1437-1442
11. Giacca, A., Xiao, C., Oprescu, A. I., Carpentier, A. C., and Lewis, G. F. (2011) Lipid-induced pancreaticβ-cell dysfunction. Focus on in vivo studies. Am. J. Physiol. Endocrinol. Metab. 300, E255-262
12. Poitout, V., and Robertson, R. P. (2008) Glucolipotoxicity. Fuel excess andβ-cell dysfunction. Endocr. Rev. 29, 351-366
13. Prentki, M., Joly, E., El-Assaad, W., and Roduit, R. (2002) Malonyl-CoA signaling, lipid partitioning, and glucolipotoxicity. Role inβ-cell adaptation and failure in the etiology of diabetes. Diabetes 51, S405-413
14. Biden, T. J., Robinson, D., Cordery, D., Hughes, W. E., and Busch, A. K. (2004) Chronic effects of fatty acids on pancreaticβ-cell function. New insights from functional genomics. Diabetes 53, S159-165
15. Nolan, C. J., Madiraju, M. S., Delghingaro-Augusto, V., Peyot, M. L., and Prentki, M. (2006) Fatty acid signaling in theβ-cell and insulin secretion. Diabetes 55, S16-23
16. Randle, P. J., Garland, P. B., Hales, C. N, and Newsholme, E. A. (1963) The glucose fatty-acid cycle. Its role in insulin sensitivity and the metabolic disturbances of diabetes mellitus. Lancet 1, 785-789
17. Weinberg, J. M. (2006) Lipotoxicity. Kidney Int. 70, 1560-1566
18. Eto, K., Yamashita, T., Matsui, J., Terauchi, Y., Noda, M., and Kadowaki, T. (2002) Genetic manipulations of fatty acid metabolism inβ-cells are associated with dysregulated insulin secretion. Diabetes 51, S414-420
19. Boucher, A., Lu, D., Burgess, S. C., Telemaque-Potts, S., Jensen, M. V., Mulder, H., Wang, M. Y., Unger, R. H., Sherry, A. D., and Newgard, C. B. (2004) Biochemical mechanism of lipid-induced impairment of glucosestimulated insulin secretion and reversal with a malate analogue. J. Biol. Chem. 279, 27263-27271
20. Keating, S. T., and El-Osta, A. (2012) Chromatin modifications associated with diabetes. J. Cardiovasc. Transl. Res. 5, 399-412
21. LeRoith, D., Fonseca, V., and Vinik, A. (2005) Metabolic memory in diabetes. Focus on insulin. Diabetes Metab. Res. Rev. 21, 85-90
22. El-Osta, A. (2012) Glycemic memory. Curr. Opin. Lipidol. 23, 24-29
23. Ling, C., and Groop, L. (2009) Epigenetics. A molecular link between environmental factors and type 2 diabetes. Diabetes 58, 2718-2725
24. Ling, C., Del Guerra, S., Lupi, R., Rönn, T., Granhall, C., Luthman, H., Masiello, P., Marchetti, P., Groop, L., and Del Prato, S. (2008) Epigenetic regulation of PPARGC1A in human type 2 diabetic islets and effect on insulin secretion. Diabetologia 51, 615-622
25. Yang, B. T., Dayeh, T. A., Volkov, P. A., Kirkpatrick, C. L., Malmgren, S., Jing, X., Renström, E., Wollheim, C. B., Nitert, M. D., and Ling, C. (2012) Increased DNA methylation and decreased expression of PDX-1 in pancreatic islets from patients with type 2 diabetes. Mol. Endocrinol. 26, 1203-1212
26. Yang, B. T., Dayeh, T. A., Kirkpatrick, C L., Taneera, J., Kumar, R., Groop, L., Wollheim, C. B., Nitert, M. D., and Ling, C. (2011) Insulin promoter DNA methylation correlates negatively with insulin gene expression and positively with HbA (1c) levels in human pancreatic islets. Diabetologia 54, 360-367
27. Volkmar, M., Dedeurwaerder, S., Cunha, D. A., Ndlovu, M. N., Defrance, M., Deplus, R., Calonne, E., Volkmar, U., Igoillo-Esteve, M., Naamane, N., Del Guerra, S., Masini, M., Bugliani, M., Marchetti, P., Cnop, M., Eizirik, D. L., and Fuks, F. (2012) DNA methylation profiling identifies epigenetic dysregulation in pancreatic islets from type 2 diabetic patients. EMBO J. 31, 1405-1426
28. Peterson, C L., and Laniel, M. A. (2004) Histones and histone modifications. Curr. Biol. 14, R546-551
29. Cedar, H., and Bergman, Y. (2009) Linking DNA methylation and histone modification. Patterns and paradigms. Nat. Rev. Genet. 10, 295-304
30. Kouzarides, T. (2007) Chromatin modifications and their function. Cell 128, 693-705
31. Martin, C., and Zhang, Y. (2005) The diverse functions of histone lysine methylation. Nat. Rev. Mol. Cell Biol. 6, 838-849
32. Ogihara, T., Vanderford, N. L., Maier, B., Stein, R. W., and Mirmira, R. G. (2009) Expression and function of Set7/9 in pancreatic islets. Islets 1, 269-272
33. Deering, T. G., Ogihara, T., Trace, A. P., Maier, B., and Mirmira, R. G. (2009) Methyltransferase Set7/9 maintains transcription and euchromatin structure at islet-enriched genes. Diabetes 58, 185-193
34. Danielsson, A. P. H., Moritz, T., Mulder, H., and Spégel, P. (2012) Development of a gas chromatography/mass spectrometry based metabolomics protocol by means of statistical experimental design. Metabolomics 8, 50-63
35. + channel-dependent and -independent glucose-stimulated insulin secretion. Diabetes 49, 424-430
36. Malmgren, S., Nicholls, D. G., Taneera, J., Bacos, K., Koeck, T., Tamaddon, A., Wibom, R., Groop, L., Ling, C., Mulder, H., and Sharoyko, V. V. (2009) Tight coupling between glucose and mitochondrial metabolism in clonalβ-cells is required for robust insulin secretion. J. Biol. Chem. 284, 32395-32404
37. Fex, M., Olofsson, C. S., Fransson, U., Bacos, K., Lindvall, H., Sörhede-Winzell, M., Rorsman, P., Holm, C., and Mulder, H. (2004) Hormonesensitive lipase deficiency in mouse islets abolishes neutral cholesterol ester hydrolase activity but leaves lipolysis, acylglycerides, fat oxidation, and insulin secretion intact. Endocrinology 145, 3746-3753
38. Brand, M. D., and Nicholls, D. G. (2011) Assessing mitochondrial dysfunction in cells. Biochem. J. 435, 297-312
39. Danielsson, A. P., Moritz, T., Mulder, H., and Spégel, P. (2010) Development and optimization of a metabolomic method for analysis of adherent cell cultures. Anal. Biochem. 404, 30-39
40. Spégel, P., Malmgren, S., Sharoyko, V. V., Newsholme, P., Koeck, T., and Mulder, H. (2011) Metabolomic analyses reveal profound differences in glycolytic and tricarboxylic acid cycle metabolism in glucose-responsive and -unresponsive clonalβ-cell lines. Biochem. J. 435, 277-284
41. Irizarry, R. A., Hobbs, B., Collin, F., Beazer-Barclay, Y. D., Antonellis, K. J., Scherf, U., and Speed, T. P. (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4, 249-264
42. Andersen, C. L., Jensen, J. L., and Ørntoft, T. F. (2004) Normalization of real-time quantitative reverse transcription-PCR data. A model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res. 64, 5245-5250
43. Weishaupt, H., and Attema, J. L. (2010) A method to study the epigenetic chromatin states of rare hematopoietic stem and progenitor cells. MiniChIP-Chip. Biol. Proced Online 12, 1-17
44. Schneider, C. A., Rasband, W. S., and Eliceiri, K. W. (2012) NIH Image to ImageJ. 25 years of image analysis. Nat Methods 9, 671-675
45. Saeed, A. I., Bhagabati, N. K., Braisted, J. C., Liang, W., Sharov, V., Howe, E. A., Li, J., Thiagarajan, M., White, J. A., and Quackenbush, J. (2006) TM4 microarray software suite. MethodsEnzymol. 411, 134-193
46. Dennis, G., Jr., Sherman, B. T., Hosack, D. A., Yang, J., Gao, W., Lane, H. C., and Lempicki, R. A. (2003) DAVID, database for annotation, visualization, and integrated discovery. Genome Biol. 4, P3
47. Suganuma, T., and Workman, J. L. (2011) Signals and combinatorial functions of histone modifications. Annu. Rev. Biochem. 80, 473-499
48. Zhang, Y., and Reinberg, D. (2001) Transcription regulation by histone methylation. Interplay between different covalent modifications of the core histone tails. Genes Dev. 15, 2343-2360
49. Quintens, R., Hendrickx, N., Lemaire, K., and Schuit, F. (2008) Why expression of some genes is disallowed inβ-cells. Biochem. Soc. Trans. 36, 300-305
50. Barski, A., Cuddapah, S., Cui, K., Roh, T. Y., Schones, D. E., Wang, Z., Wei, G., Chepelev, I., and Zhao, K. (2007) High-resolution profiling of histone methylations in the human genome. Cell 129, 823-837
51. Bernstein, B. E., Kamal, M., Lindblad-Toh, K., Bekiranov, S., Bailey, D. K., Huebert, D. J., McMahon, S., Karlsson, E. K., Kulbokas, E. J., 3rd, Gingeras, T. R., Schreiber, S. L., and Lander, E. S. (2005) Genomic maps and comparative analysis of histone modifications in human and mouse. Cell 120, 169-181
52. Bhandare, R., Schug, J., Le Lay, J., Fox, A., Smirnova, O., Liu, C, Naji, A., and Kaestner, K. H. (2010) Genome-wide analysis of histone modifications in human pancreatic islets. Genome research 20, 428-433
53. Heintzman, N. D., Stuart, R. K., Hon, G., Fu, Y., Ching, C. W., Hawkins, R. D., Barrera, L. O., Van Calcar, S., Qu, C, Ching, K. A., Wang, W., Weng, Z., Green, R. D., Crawford, G. E., and Ren, B. (2007) Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat. Genet. 39, 311-318
54. Porte, D., Jr. (1991) Banting lecture 1990. β-Cells in type II diabetes mellitus. Diabetes 40, 166-180
55. Zhou, Y. P., and Grill, V. E. (1994) Long-term exposure of rat pancreatic islets to fatty acids inhibits glucose-induced insulin secretion and biosynthesis through a glucose fatty acid cycle. J. Clin. Invest. 93, 870-876
56. Liang, Y., Buettger, C., Berner, D. K., and Matschinsky, F. M. (1997) Chronic effect of fatty acids on insulin release is not through the alteration of glucose metabolism in a pancreaticβ-cell line (βHC9). Diabetologia 40, 1018-1027
57. Segall, L., Lameloise, N., Assimacopoulos-Jeannet, F., Roche, E., Corkey, P., Thumelin, S., Corkey, B. E., and Prentki, M. (1999) Lipid rather than glucose metabolism is implicated in altered insulin secretion caused by oleate in INS-1 cells. Am. J. Physiol. 277, E521-528
58. Koshkin, V., Dai, F. F., Robson-Doucette, C. A., Chan, C. B., and Wheeler, M. B. (2008) Limited mitochondrial permeabilization is an early manifestation of palmitate-induced lipotoxicity in pancreaticβ-cells. J. Biol. Chem. 283, 7936-7948
59. Henquin, J. C. (2009) Regulation of insulin secretion. A matter of phase control and amplitude modulation. Diabetologia 52, 739-751
60. Ivarsson, R., Quintens, R., Dejonghe, S., Tsukamoto, K., in 't Veld, P., Renström, E., and Schuit, F. C. (2005) Redox control of exocytosis. Regulatory role of NADPH, thioredoxin, and glutaredoxin. Diabetes 54, 2132-2142
61. Gu, X. H., Kurose, T., Kato, S., Masuda, K., Tsuda, K., Ishida, H., and Seino, Y. (1993) Suppressive effect of GABA on insulin secretion from the pancreaticβ-cells in the rat. Life Sci. 52, 687-694
62. Gilon, P., Bertrand, G., Loubatières-Mariani, M. M., Remacle, C., and Henquin, J. C. (1991) The influence of 7-aminobutyric acid on hormone release by the mouse and rat endocrine pancreas. Endocrinology 129, 2521-2529
63. Shi, Y., Kanaani, J., Menard-Rose, V., Ma, Y. H., Chang, P. Y., Hanahan, D., Tobin, A., Grodsky, G., and Baekkeskov, S. (2000) Increased expression of GAD65 and GABA in pancreaticβ-cells impairs first-phase insulin secretion. Am. J. Physiol. Endocrinol. Metab. 279, E684-694
64. Maechler, P., and Wollheim, C. B. (1999) Mitochondrial glutamate acts as a messenger in glucose-induced insulin exocytosis. Nature 402, 685-689
65. MacDonald, M. J., and Fahien, L. A. (2000) Glutamate is not a messenger in insulin secretion. J. Biol. Chem. 275, 34025-34027
66. Rubi, B., del Arco, A., Bartley, C., Satrustegui, J., and Maechler, P. (2004) The malate-aspartate NADH shuttle member Aralar1 determines glucose metabolic fate, mitochondrial activity, and insulin secretion in beta cells. J. Biol. Chem. 279, 55659-55666
67. Casimir, M., Rubi, B., Frigerio, F., Chaffard, G., and Maechler, P. (2009) Silencing of the mitochondrial NADH shuttle component aspartate-glutamate carrier AGC1/Aralar1 in INS-1E cells and rat islets. Biochem. J. 424, 459-466
68. Busch, A. K., Cordery, D., Denyer, G. S., and Biden, T. J. (2002) Expression profiling of palmitate-and oleate-regulated genes provides novel insights into the effects of chronic lipid exposure on pancreaticβ-cell function. Diabetes 51, 977-987
69. El-Assaad, W., Joly, E., Barbeau, A., Sladek, R., Buteau, J., Maestre, I., Pepin, E., Zhao, S., Iglesias, J., Roche, E., and Prentki, M. (2010) Glucolipotoxicity alters lipid partitioning and causes mitochondrial dysfunction, cholesterol, and ceramide deposition and reactive oxygen species production in INS832/13 ss-cells. Endocrinology 151, 3061-3073
70. Brunham, L. R., Kruit, J. K., Pape, T. D., Timmins, J. M., Reuwer, A. Q., Vasanji, Z., Marsh, B. J., Rodrigues, B., Johnson, J. D., Parks, J. S., Verchere, C. B., and Hayden, M. R. (2007) β-Cell ABCA1 influences insulin secretion, glucose homeostasis and response to thiazolidinedione treatment. Nat. Med. 13, 340-347
71. Ishikawa, M., Iwasaki, Y., Yatoh, S., Kato, T., Kumadaki, S., Inoue, N., Yamamoto, T., Matsuzaka, T., Nakagawa, Y., Yahagi, N., Kobayashi, K., Takahashi, A., Yamada, N., and Shimano, H. (2008) Cholesterol accumulation and diabetes in pancreaticβ-cell-specific SREBP-2 transgenic mice. A new model for lipotoxicity. J. Lipid Res. 49, 2524-2534
72. Kanehisa, M., and Goto, S. (2000) KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acid Res. 28, 27-30
73. Barrès, R., Osler, M. E., Yan, J., Rune, A., Fritz, T., Caidahl, K., Krook, A., and Zierath, J. R. (2009) Non-CpG methylation of the PGC-1α promoter through DNMT3B controls mitochondrial density. CellMetab. 10, 189-198
74. Chen, K., Jin, P., He, H. H., Xie, Y. H., Xie, X. Y., and Mo, Z. H. (2011) Overexpression of Insig-1 protectsβ cell against glucolipotoxicity via SREBP-1c. J. Biomed. Sci. 18, 57
75. Vock, C., Döring, F., and Nitz, I. (2008) Transcriptional regulation of HMG-CoA synthase and HMG-CoA reductase genes by human ACBP. Cell Physiol. Biochem. 22, 515-524
76. van Weeghel, M., te Brinke, H., van Lenthe, H., Kulik, W., Minkler, P. E., Stoll, M. S., Sass, J. O., Janssen, U., Stoffel, W., Schwab, K. O., Wanders, R. J., Hoppel, C. L., and Houten, S. M. (2012) Functional redundancy of mitochondrial enoyl-CoA isomerases in the oxidation of unsaturated fatty acids. FASEBJ. 26, 4316-4326
77. Falchetti, A., Gozzini, A., Terranegra, A., Soldati, L., Vezzoli, G., Leoncini, G., Giusti, F., Franceschelli, F., Masi, L., Tanini, A., Cavalli, L., and Brandi, M. L. (2012) A novel germline inactivating mutation in the CASR gene in an Italian kindred affected by familial hypocalciuric hypercalcemia. Eur. J. Endocrinol. 166, 933-940
78. Moran, A., Zhang, H. J., Olson, L. K., Harmon, J. S., Poitout, V., and Robertson, R. P. (1997) Differentiation of glucose toxicity fromβ cell exhaustion during the evolution of defective insulin gene expression in the pancreatic islet cell line, HIT-T15. J. Clin. Invest. 99, 534-539
79. Olson, L. K., Qian, J., and Poitout, V. (1998) Glucose rapidly and reversibly decreases INS-1 cell insulin gene transcription via decrements in STF-1 and C1 activator transcription factor activity. Mol. Endocrinol. 12, 207-219