Differentially expressed microRNA-483 confers distinct functions in pancreatic β- and α-cells

Journal of Biological Chemistry

Volumn 290, Issue 32, 2015, Pages 19955-19966

  Mohan, Ramkumar ^a   Mao, Yiping ^a   Zhang, Shungang ^a   Zhang, Yu Wei ^b   Xu, Cheng Ran ^b   Gradwohl, Gérard ^c   Tang, Xiaoqing ^a  

^a MICHIGAN TECHNOLOGICAL UNIVERSITY   (United States)

^b Tsinghua University   (China)

^c UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CELL DEATH; CELLS; CYTOLOGY; DRUG PRODUCTS; GENE EXPRESSION; INSULIN; PHYSIOLOGY; RNA; TRANSCRIPTION;

DIFFERENTIAL EXPRESSIONS; EXPRESSION LEVELS; GLUCOSE HOMEOSTASIS; INDUCED APOPTOSIS; OVER-EXPRESSION; PANCREATIC BETA CELLS; PROINFLAMMATORY CYTOKINES; SUPPRESSOR OF CYTOKINE SIGNALING;

CELL SIGNALING;

GLUCAGON; INSULIN; MICRORNA; MICRORNA 483; SUPPRESSOR OF CYTOKINE SIGNALING 3; UNCLASSIFIED DRUG; GAMMA INTERFERON; INTERLEUKIN 1BETA; LEPTIN RECEPTOR; LEPTIN RECEPTOR, MOUSE; MIRN483 MICRORNA, MOUSE; SOCS3 PROTEIN, MOUSE; SUPPRESSOR OF CYTOKINE SIGNALING; TUMOR NECROSIS FACTOR ALPHA;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL FUNCTION; CONTROLLED STUDY; GENE EXPRESSION PROFILING; GENE IDENTIFICATION; GENETIC TRANSCRIPTION; INSULIN RELEASE; MOUSE; NONHUMAN; PANCREAS ISLET ALPHA CELL; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN SECRETION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; ANIMAL; ANTIBODY SPECIFICITY; BIOSYNTHESIS; C57BL MOUSE; CELL LINE; CYTOLOGY; DEFICIENCY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; HOMEOSTASIS; IMPAIRED GLUCOSE TOLERANCE; KNOCKOUT MOUSE; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PATHOLOGY; SECRETION (PROCESS);

MUS;

ANIMALS; APOPTOSIS; BASE SEQUENCE; CELL LINE; GENE EXPRESSION REGULATION; GLUCAGON; GLUCAGON-SECRETING CELLS; HOMEOSTASIS; INSULIN; INSULIN-SECRETING CELLS; INTERFERON-GAMMA; INTERLEUKIN-1BETA; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICRORNAS; MOLECULAR SEQUENCE DATA; ORGAN SPECIFICITY; PREDIABETIC STATE; RECEPTORS, LEPTIN; SIGNAL TRANSDUCTION; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS; TRANSCRIPTION, GENETIC; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84939131576     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.650705     Document Type: Article

References (67)

1. Cabrera, O., Berman, D. M., Kenyon, N. S., Ricordi, C., Berggren, P. O., and Caicedo, A. (2006) The unique cytoarchitecture of human pancreatic islets has implications for islet cell function. Proc. Natl. Acad. Sci. U.S.A. 103, 2334-2339
2. Breckenridge, S. M., Cooperberg, B. A., Arbelaez, A. M., Patterson, B. W., and Cryer, P. E. (2007) Glucagon, in concert with insulin, supports the postabsorptive plasma glucose concentration in humans. Diabetes 56, 2442-2448
3. Cooperberg, B. A., and Cryer, P. E. (2010) Insulin reciprocally regulates glucagon secretion in humans. Diabetes 59, 2936-2940
4. Porte, D., Jr., and Kahn, S. E. (2001) β-Cell dysfunction and failure in type 2 diabetes: potential mechanisms. Diabetes 50, Suppl. 1, S160-S163, 10.2337/diabetes.50.2007.S160
5. Butler, A. E., Janson, J., Bonner-Weir, S., Ritzel, R., Rizza, R. A., and Butler, P. C. (2003) β-Cell deficit and increased β-cell apoptosis in humans with type 2 diabetes. Diabetes 52, 102-110
6. D'Alessio, D. (2011) The role of dysregulated glucagon secretion in type 2 diabetes. Diabetes Obes. Metab. 13, Suppl. 1, 126-132, 10.1111/j.1463-1326.2011.01449.x
7. Yoon, K. H., Ko, S. H., Cho, J. H., Lee, J. M., Ahn, Y. B., Song, K. H., Yoo, S. J., Kang, M. I., Cha, B. Y., Lee, K. W., Son, H. Y., Kang, S. K., Kim, H. S., Lee, I. K., and Bonner-Weir, S. (2003) Selective β-cell loss and α-cell expansion in patients with type 2 diabetes mellitus in Korea. J. Clin. Endocrinol. Metab. 88, 2300-2308
8. Deng, S., Vatamaniuk, M., Huang, X., Doliba, N., Lian, M. M., Frank, A., Velidedeoglu, E., Desai, N. M., Koeberlein, B., Wolf, B., Barker, C. F., Naji, A., Matschinsky, F. M., and Markmann, J. F. (2004) Structural and functional abnormalities in the islets isolated from type 2 diabetic subjects. Diabetes 53, 624-632
9. Montanya, E., and Téllez, N. (2009) Pancreatic remodeling: β-cell apoptosis, proliferation and neogenesis, and the measurement of β-cell mass and of individual β-cell size. Methods Mol. Biol. 560, 137-158
10. Kassem, S. A., Ariel, I., Thornton, P. S., Scheimberg, I., and Glaser, B. (2000) β-Cell proliferation and apoptosis in the developing normal human pancreas and in hyperinsulinism of infancy. Diabetes 49, 1325-1333
11. Heit, J. J., Karnik, S. K., and Kim, S. K. (2006) Intrinsic regulators of pancreatic β-cell proliferation. Annu. Rev. Cell Dev. Biol. 22, 311-338
12. Kulkarni, R. N. (2005) New insights into the roles of insulin/IGF-I in the development and maintenance of β-cell mass. Rev. Endocr. Metab. Disord. 6, 199-210
13. Kulkarni, R. N., Mizrachi, E. B., Ocana, A. G., and Stewart, A. F. (2012) Human β-cell proliferation and intracellular signaling: driving in the dark without a road map. Diabetes 61, 2205-2213
14. Bernal-Mizrachi, E., Kulkarni, R. N., Scott, D. K., Mauvais-Jarvis, F., Stewart, A. F., and Garcia-Ocaña, A. (2014) Human β-cell proliferation and intracellular signaling part 2: still driving in the dark without a road map. Diabetes 63, 819-831
15. Mandrup-Poulsen, T. (2001) β-Cell apoptosis: stimuli and signaling. Diabetes 50, Suppl. 1, S58-S63, 10.2337/diabetes.50.2007.S58
16. Ravier, M. A., and Rutter, G. A. (2005) Glucose or insulin, but not zinc ions, inhibit glucagon secretion from mouse pancreatic α-cells. Diabetes 54, 1789-1797
17. Diao, J., Asghar, Z., Chan, C. B., and Wheeler, M. B. (2005) Glucose-regulated glucagon secretion requires insulin receptor expression in pancreatic α-cells. J. Biol. Chem. 280, 33487-33496
18. Zhou, H., Tran, P. O., Yang, S., Zhang, T., LeRoy, E., Oseid, E., and Robertson, R. P. (2004) Regulation of α-cell function by the β-cell during hypoglycemia in Wistar rats: the "switch-off" hypothesis. Diabetes 53, 1482-1487
19. Hope, K. M., Tran, P. O., Zhou, H., Oseid, E., Leroy, E., and Robertson, R. P. (2004) Regulation of α-cell function by the β-cell in isolated human and rat islets deprived of glucose: the "switch-off" hypothesis. Diabetes 53, 1488-1495
20. Cantley, J., Choudhury, A. I., Asare-Anane, H., Selman, C., Lingard, S., Heffron, H., Herrera, P., Persaud, S. J., and Withers, D. J. (2007) Pancreatic deletion of insulin receptor substrate 2 reduces β and α cell mass and impairs glucose homeostasis in mice. Diabetologia 50, 1248-1256
21. Kawamori, D., Kurpad, A. J., Hu, J., Liew, C. W., Shih, J. L., Ford, E. L., Herrera, P. L., Polonsky, K. S., McGuinness, O. P., and Kulkarni, R. N. (2009) Insulin signaling in α cells modulates glucagon secretion in vivo. Cell Metab. 9, 350-361
22. Liu, Z., Kim, W., Chen, Z., Shin, Y. K., Carlson, O. D., Fiori, J. L., Xin, L., Napora, J. K., Short, R., Odetunde, J. O., Lao, Q., and Egan, J. M. (2011) Insulin and glucagon regulate pancreatic α-cell proliferation. PLoS One 6, e16096
23. Bartel, D. P. (2009) MicroRNAs: target recognition and regulatory functions. Cell 136, 215-233
24. Broderick, J. A., and Zamore, P. D. (2011) MicroRNA therapeutics. Gene. Ther. 18, 1104-1110
25. Guay, C., Roggli, E., Nesca, V., Jacovetti, C., and Regazzi, R. (2011) Diabetes mellitus, a microRNA-related disease? Transl. Res. 157, 253-264
26. Mao, Y., Mohan, R., Zhang, S., and Tang, X. (2013) MicroRNAs as pharmacological targets in diabetes. Pharmacol. Res. 75, 37-47
27. Poy, M. N., Hausser, J., Trajkovski, M., Braun, M., Collins, S., Rorsman, P., Zavolan, M., and Stoffel, M. (2009) miR-375 maintains normal pancreatic α- and β-cell mass. Proc. Natl. Acad. Sci. U.S.A. 106, 5813-5818
28. Wang, Y., Liu, J., Liu, C., Naji, A., and Stoffers, D. A. (2013) MicroRNA-7 regulates the mTOR pathway and proliferation in adult pancreatic β-cells. Diabetes 62, 887-895
29. Latreille, M., Hausser, J., Stützer, I., Zhang, Q., Hastoy, B., Gargani, S., Kerr-Conte, J., Pattou, F., Zavolan, M., Esguerra, J. L., Eliasson, L., Rülicke, T., Rorsman, P., and Stoffel, M. (2014) MicroRNA-7a regulates pancreatic β cell function. J. Clin. Invest. 124, 2722-2735
30. Klein, D., Misawa, R., Bravo-Egana, V., Vargas, N., Rosero, S., Piroso, J., Ichii, H., Umland, O., Zhijie, J., Tsinoremas, N., Ricordi, C., Inverardi, L., Domínguez-Bendala, J., and Pastori, R. L. (2013) MicroRNA expression in α and β cells of human pancreatic islets. PLoS One 8, e55064
31. Miyazaki, J., Araki, K., Yamato, E., Ikegami, H., Asano, T., Shibasaki, Y., Oka, Y., and Yamamura, K. (1990) Establishment of a pancreatic β cell line that retains glucose-inducible insulin secretion: special reference to expression of glucose transporter isoforms. Endocrinology 127, 126-132
32. Tang, X., Muniappan, L., Tang, G., and Ozcan, S. (2009) Identification of glucose-regulated miRNAs from pancreatic β cells reveals a role for miR-30d in insulin transcription. RNA 15, 287-293
33. Brissova, M., Fowler, M., Wiebe, P., Shostak, A., Shiota, M., Radhika, A., Lin, P. C., Gannon, M., and Powers, A. C. (2004) Intraislet endothelial cells contribute to revascularization of transplanted pancreatic islets. Diabetes 53, 1318-1325
34. Piccand, J., Meunier, A., Merle, C., Jia, Z., Barnier, J. V., and Gradwohl, G. (2014) Pak3 promotes cell cycle exit and differentiation of β-cells in the embryonic pancreas and is necessary to maintain glucose homeostasis in adult mice. Diabetes 63, 203-215
35. Herrera, P. L. (2000) Adult insulin- and glucagon-producing cells differentiate from two independent cell lineages. Development 127, 2317-2322
36. Xu, C. R., Li, L. C., Donahue, G., Ying, L., Zhang, Y. W., Gadue, P., and Zaret, K. S. (2014) Dynamics of genomic H3K27me3 domains and role of EZH2 during pancreatic endocrine specification. EMBO J. 33, 2157-2170
37. Tang, X., Gal, J., Zhuang, X., Wang, W., Zhu, H., and Tang, G. (2007) A simple array platform for microRNA analysis and its application in mouse tissues. RNA 13, 1803-1822
38. de Hoon, M. J., Imoto, S., Nolan, J., and Miyano, S. (2004) Open source clustering software. Bioinformatics 20, 1453-1454
39. Saldanha, A. J. (2004) Java Treeview: extensible visualization of microarray data. Bioinformatics 20, 3246-3248
40. Wang, W. X., Rajeev, B. W., Stromberg, A. J., Ren, N., Tang, G., Huang, Q., Rigoutsos, I., and Nelson, P. T. (2008) The expression of microRNA miR-107 decreases early in Alzheimer's disease and may accelerate disease progression through regulation of β-site amyloid precursor protein-cleaving enzyme 1. J. Neurosci. 28, 1213-1223
41. Liu, M., Roth, A., Yu, M., Morris, R., Bersani, F., Rivera, M. N., Lu, J., Shioda, T., Vasudevan, S., Ramaswamy, S., Maheswaran, S., Diederichs, S., and Haber, D. A. (2013) The IGF2 intronic miR-483 selectively enhances transcription from IGF2 fetal promoters and enhances tumorigenesis. Genes Dev. 27, 2543-2548
42. Ma, N., Wang, X., Qiao, Y., Li, F., Hui, Y., Zou, C., Jin, J., Lv, G., Peng, Y., Wang, L., Huang, H., Zhou, L., Zheng, X., and Gao, X. (2011) Coexpression of an intronic microRNA and its host gene reveals a potential role for miR-483-5p as an IGF2 partner. Mol. Cell Endocrinol. 333, 96-101
43. Rui, L., Yuan, M., Frantz, D., Shoelson, S., and White, M. F. (2002) SOCS-1 and SOCS-3 block insulin signaling by ubiquitin-mediated degradation of IRS1 and IRS2. J. Biol. Chem. 277, 42394-42398
44. Shi, H., Tzameli, I., Bjørbaek, C., and Flier, J. S. (2004) Suppressor of cytokine signaling 3 is a physiological regulator of adipocyte insulin signaling. J. Biol. Chem. 279, 34733-34740
45. Ueki, K., Kondo, T., and Kahn, C. R. (2004) Suppressor of cytokine signaling 1 (SOCS-1) and SOCS-3 cause insulin resistance through inhibition of tyrosine phosphorylation of insulin receptor substrate proteins by discrete mechanisms. Mol. Cell. Biol. 24, 5434-5446
46. Ueki, K., Kondo, T., Tseng, Y. H., and Kahn, C. R. (2004) Central role of suppressors of cytokine signaling proteins in hepatic steatosis, insulin resistance, and the metabolic syndrome in the mouse. Proc. Natl. Acad. Sci. U.S.A. 101, 10422-10427
47. Rønn, S. G., Hansen, J. A., Lindberg, K., Karlsen, A. E., and Billestrup, N. (2002) The effect of suppressor of cytokine signaling 3 on GH signaling in β-cells. Mol. Endocrinol. 16, 2124-2134
48. Laubner, K., Kieffer, T. J., Lam, N. T., Niu, X., Jakob, F., and Seufert, J. (2005) Inhibition of preproinsulin gene expression by leptin induction of suppressor of cytokine signaling 3 in pancreatic β-cells. Diabetes 54, 3410-3417
49. Lindberg, K., Rønn, S. G., Tornehave, D., Richter, H., Hansen, J. A., Rømer, J., Jackerott, M., and Billestrup, N. (2005) Regulation of pancreatic β-cell mass and proliferation by SOCS-3. J. Mol. Endocrinol. 35, 231-243
50. Emanuelli, B., Peraldi, P., Filloux, C., Chavey, C., Freidinger, K., Hilton, D. J., Hotamisligil, G. S., and Van Obberghen, E. (2001) SOCS-3 inhibits insulin signaling and is up-regulated in response to tumor necrosis factor-α in the adipose tissue of obese mice. J. Biol. Chem. 276, 47944-47949
51. Karlsen, A. E., Rønn, S. G., Lindberg, K., Johannesen, J., Galsgaard, E. D., Pociot, F., Nielsen, J. H., Mandrup-Poulsen, T., Nerup, J., and Billestrup, N. (2001) Suppressor of cytokine signaling 3 (SOCS-3) protects β-cells against interleukin-1β- and interferon-γ-mediated toxicity. Proc. Natl. Acad. Sci. U.S.A. 98, 12191-12196
52. Emanuelli, B., Glondu, M., Filloux, C., Peraldi, P., and Van Obberghen, E. (2004) The potential role of SOCS-3 in the interleukin-1β-induced desensitization of insulin signaling in pancreatic β-cells. Diabetes 53, Suppl. 3, S97-S103, 10.2337/diabetes.53.suppl-3.S97
53. Wang, Q., and Brubaker, P. L. (2002) Glucagon-like peptide-1 treatment delays the onset of diabetes in 8 week-old db/db mice. Diabetologia 45, 1263-1273
54. Grimson, A., Farh, K. K., Johnston, W. K., Garrett-Engele, P., Lim, L. P., and Bartel, D. P. (2007) MicroRNA targeting specificity in mammals: determinants beyond seed pairing. Mol. Cell 27, 91-105
55. Shin, C., Nam, J. W., Farh, K. K., Chiang, H. R., Shkumatava, A., and Bartel, D. P. (2010) Expanding the microRNA targeting code: functional sites with centered pairing. Mol. Cell 38, 789-802
56. Jorgensen, S. B., O'Neill, H. M., Sylow, L., Honeyman, J., Hewitt, K. A., Palanivel, R., Fullerton, M. D., Öberg, L., Balendran, A., Galic, S., van der Poel, C., Trounce, I. A., Lynch, G. S., Schertzer, J. D., and Steinberg, G. R. (2013) Deletion of skeletal muscle SOCS3 prevents insulin resistance in obesity. Diabetes 62, 56-64
57. Monteys, A. M., Spengler, R. M., Wan, J., Tecedor, L., Lennox, K. A., Xing, Y., and Davidson, B. L. (2010) Structure and activity of putative intronic miRNA promoters. RNA 16, 495-505
58. Cornu, M., Yang, J. Y., Jaccard, E., Poussin, C., Widmann, C., and Thorens, B. (2009) Glucagon-like peptide-1 protects β-cells against apoptosis by increasing the activity of an IGF-2/IGF-1 receptor autocrine loop. Diabetes 58, 1816-1825
59. Devedjian, J. C., George, M., Casellas, A., Pujol, A., Visa, J., Pelegrín, M., Gros, L., and Bosch, F. (2000) Transgenic mice overexpressing insulin-like growth factor-II in β cells develop type 2 diabetes. J. Clin. Invest. 105, 731-740
60. Petrik, J., Arany, E., McDonald, T. J., and Hill, D. J. (1998) Apoptosis in the pancreatic islet cells of the neonatal rat is associated with a reduced expression of insulin-like growth factor II that may act as a survival factor. Endocrinology 139, 2994-3004
61. Hill, D. J., Strutt, B., Arany, E., Zaina, S., Coukell, S., and Graham, C. F. (2000) Increased and persistent circulating insulin-like growth factor II in neonatal transgenic mice suppresses developmental apoptosis in the pancreatic islets. Endocrinology 141, 1151-1157
62. Place, R. F., Li, L. C., Pookot, D., Noonan, E. J., and Dahiya, R. (2008) MicroRNA-373 induces expression of genes with complementary promoter sequences. Proc. Natl. Acad. Sci. U.S.A. 105, 1608-1613
63. Kim, D. H., Saetrom, P., Snøve, O., Jr., and Rossi, J. J. (2008) MicroRNA-directed transcriptional gene silencing in mammalian cells. Proc. Natl. Acad. Sci. U.S.A. 105, 16230-16235
64. Barbagallo, D., Piro, S., Condorelli, A. G., Mascali, L. G., Urbano, F., Parrinello, N., Monello, A., Statello, L., Ragusa, M., Rabuazzo, A. M., Di Pietro, C., Purrello, F., and Purrello, M. (2013) miR-296-3p, miR-298-5p and their downstream networks are causally involved in the higher resistance of mammalian pancreatic α cells to cytokine-induced apoptosis as compared to β cells. BMC Genomics 14, 62
65. Baroukh, N., Ravier, M. A., Loder, M. K., Hill, E. V., Bounacer, A., Scharfmann, R., Rutter, G. A., and Van Obberghen, E. (2007) MicroRNA-124a regulates Foxa2 expression and intracellular signaling in pancreatic β-cell lines. J. Biol. Chem. 282, 19575-19588
66. Lovis, P., Gattesco, S., and Regazzi, R. (2008) Regulation of the expression of components of the exocytotic machinery of insulin-secreting cells by microRNAs. Biol. Chem. 389, 305-312
67. Trajkovski, M., Hausser, J., Soutschek, J., Bhat, B., Akin, A., Zavolan, M., Heim, M. H., and Stoffel, M. (2011) MicroRNAs 103 and 107 regulate insulin sensitivity. Nature 474, 649-653