Postnatal β-cell maturation is associated with islet-specific microRNA changes induced by nutrient shifts at weaning

Nature Communications

Volumn 6, Issue , 2015, Pages

  Jacovetti, Cécile ^a   Matkovich, Scot J ^b   Rodriguez Trejo, Adriana ^a   Guay, Claudiane ^a   Regazzi, Romano ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE; INSULIN; MICRORNA; MICRORNA 106B; MICRORNA 106B 5P; MICRORNA 129 5P; MICRORNA 130B; MICRORNA 130B 3P; MICRORNA 17 5P; MICRORNA 181B; MICRORNA 181B 5P; MICRORNA 18A; MICRORNA 18A 5P; MICRORNA 192; MICRORNA 192 5P; MICRORNA 194; MICRORNA 194 5P; MICRORNA 19B 3P; MICRORNA 203; MICRORNA 203A 3P; MICRORNA 204; MICRORNA 204 5P; MICRORNA 20A 5P; MICRORNA 215; MICRORNA 29B; MICRORNA 29B 3P; MICRORNA 92A 3P; MICRORNA 93 5P; PHOSPHORUS 31; PROTEIN P23; UNCLASSIFIED DRUG;

CELLS AND CELL COMPONENTS; DIABETES; ENZYME ACTIVITY; GENE EXPRESSION; GLUCOSE; MATURATION; NUTRIENT; RNA; WEANING;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL MATURATION; CONTROLLED STUDY; DIABETES MELLITUS; GENE EXPRESSION; INSULIN RELEASE; METABOLIC DISORDER; MOUSE; NONHUMAN; NUTRIENT CONTENT; NUTRIENT SUPPLY; NUTRITIONAL REQUIREMENT; PANCREAS ISLET BETA CELL; POSTNATAL CARE; POSTNATAL DEVELOPMENT; PROTEIN MODIFICATION; RAT; WEANING; ANIMAL; CELL CULTURE; CELL DIFFERENTIATION; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; GENETICS; IMMUNOHISTOCHEMISTRY; METABOLISM; NON INSULIN DEPENDENT DIABETES MELLITUS; PANCREAS ISLET; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SECRETION (PROCESS); SPRAGUE DAWLEY RAT;

ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; DIABETES MELLITUS, TYPE 2; FLOW CYTOMETRY; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IMMUNOHISTOCHEMISTRY; INSULIN; INSULIN-SECRETING CELLS; ISLETS OF LANGERHANS; MICRORNAS; RATS; RATS, SPRAGUE-DAWLEY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; WEANING;

EID: 84940831580     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms9084     Document Type: Article

References (68)

1. Prentki, M., Matschinsky, F. M. & Madiraju, S. R. Metabolic signaling in fuel-induced insulin secretion. Cell. Metab. 18, 162-185 (2013).
2. Nolan, C. J. & Prentki, M. The islet beta-cell: fuel responsive and vulnerable. Trends Endocrinol. Metab. 19, 285-291 (2008).
3. Grasso, S., Messina, A., Saporito, N. & Reitano, G. Serum-insulin response to glucose and aminoacids in the premature infant. Lancet 2, 755-756 (1968).
4. Pildes, R. S., Hart, R. J., Warrner, R. & Cornblath, M. Plasma insulin response during oral glucose tolerance tests in newborns of normal and gestational diabetic mothers. Pediatrics 44, 76-83 (1969).
5. Rozzo, A., Meneghel-Rozzo, T., Delakorda, S. L., Yang, S. B. & Rupnik, M. Exocytosis of insulin: in vivo maturation of mouse endocrine pancreas. Ann. N. Y. Acad. Sci. 1152, 53-62 (2009).
6. Rorsman, P. et al. Failure of glucose to elicit a normal secretory response in fetal pancreatic beta cells results from glucose insensitivity of the ATPregulated K+ channels. Proc. Natl Acad. Sci. USA 86, 4505-4509 (1989).
7. Dixit, P. K., Lowe, I. P., Heggestad, C. B. & Lazarow, A. Insulin content of microdissected fetal islets obtained from diabetic and normal rats. Diabetes 13, 71-77 (1964).
8. Blum, B. et al. Functional beta-cell maturation is marked by an increased glucose threshold and by expression of urocortin 3. Nat. Biotechnol. 30, 261-264 (2012).
9. Aguayo-Mazzucato, C., Sanchez-Soto, C., Godinez-Puig, V., Gutierrez-Ospina, G. & Hiriart, M. Restructuring of pancreatic islets and insulin secretion in a postnatal critical window. PLoS ONE 1, e35 (2006).
10. Jermendy, A. et al. Rat neonatal beta cells lack the specialised metabolic phenotype of mature beta cells. Diabetologia 54, 594-604 (2011).
11. Martens, G. A. et al. Functional characteristics of neonatal rat beta cells with distinct markers. J. Mol. Endocrinol. 52, 11-28 (2014).
12. Tan, C., Tuch, B. E., Tu, J. & Brown, S. A. Role of NADH shuttles in glucoseinduced insulin secretion from fetal beta-cells. Diabetes 51, 2989-2996 (2002).
13. Thorrez, L. et al. Tissue-specific disallowance of housekeeping genes: the other face of cell differentiation. Genome Res. 21, 95-105 (2011).
14. Mezza, T. & Kulkarni, R. N. The regulation of pre-And post-maturational plasticity of mammalian islet cell mass. Diabetologia 57, 1291-1303 (2014).
15. Meier, J. J. et al. Beta-cell replication is the primary mechanism subserving the postnatal expansion of beta-cell mass in humans. Diabetes 57, 1584-1594 (2008).
16. Gregg, B. E. et al. Formation of a human beta-cell population within pancreatic islets is set early in life. J. Clin. Endocrinol. Metab. 97, 3197-3206 (2012).
17. Devlieger, R., Casteels, K. & Van Assche, F. A. Reduced adaptation of the pancreatic B cells during pregnancy is the major causal factor for gestational diabetes: current knowledge and metabolic effects on the offspring. Acta. Obstet. Gynecol. Scand. 87, 1266-1270 (2008).
18. Yessoufou, A. & Moutairou, K. Maternal diabetes in pregnancy: early and longterm outcomes on the offspring and the concept of "metabolic memory". Exp. Diabetes Res. 2011, 218598 (2011).
19. Henning, S. J. Postnatal development: coordination of feeding, digestion, and metabolism. Am. J. Physiol. 241, G199-G214 (1981).
20. Girard, J., Ferre, P., Pegorier, J. P. & Duee, P. H. Adaptations of glucose and fatty acid metabolism during perinatal period and suckling-weaning transition. Physiol. Rev. 72, 507-562 (1992).
21. Tarussio, D. et al. Nervous glucose sensing regulates postnatal beta cell proliferation and glucose homeostasis. J. Clin. Invest. 124, 413-424 (2014).
22. Srinivasan, M., Laychock, S. G., Hill, D. J. & Patel, M. S. Neonatal nutrition: metabolic programming of pancreatic islets and obesity. Exp. Biol. Med. (Maywood) 228, 15-23 (2003).
23. Bringhenti, I. et al. Maternal obesity during the preconception and early life periods alters pancreatic development in early and adult life in male mouse offspring. PLoS ONE 8, e55711 (2013).
24. Stolovich-Rain, M. et al. Weaning triggers a maturation step of pancreatic beta cells. Dev. Cell. 32, 535-545 (2015).
25. Guay, C. et al. Emerging roles of non-coding RNAs in pancreatic beta-cell function and dysfunction. Diabetes. Obes. Metab. 14, 12-21 (2012).
26. Dumortier, O., Hinault, C. & Van Obberghen, E. MicroRNAs and metabolism crosstalk in energy homeostasis. Cell. Metab. 18, 312-324 (2013).
27. Lynn, F. C. et al. MicroRNA expression is required for pancreatic islet cell genesis in the mouse. Diabetes 56, 2938-2945 (2007).
28. Melkman-Zehavi, T. et al. miRNAs control insulin content in pancreatic beta-cells via downregulation of transcriptional repressors. EMBO J. 30, 835-845 (2011).
29. Kalis, M. et al. Beta-cell specific deletion of dicer1 leads to defective insulin secretion and diabetes mellitus. PLoS ONE 6, e29166 (2011).
30. Mandelbaum, A. D. et al. Dysregulation of Dicer1 in beta cells impairs islet architecture and glucose metabolism. Exp. Diabetes Res. 2012, 470302 (2012).
31. Kanji, M. S., Martin, M. G. & Bhushan, A. Dicer1 is required to repress neuronal fate during endocrine cell maturation. Diabetes 62, 1602-1611 (2013).
32. Lu, T. P. et al. miRSystem: an integrated system for characterizing enriched functions and pathways of MicroRNA Targets. PLoS ONE 7, e42390 (2012).
33. Dweep, H., Sticht, C., Pandey, P. & Gretz, N. miRWalk-database: prediction of possible miRNA binding sites by "walking" the genes of three genomes. J. Biomed. Inform. 44, 839-847 (2011).
34. Pullen, T. J., da Silva Xavier, G., Kelsey, G. & Rutter, G. A. miR-29a and miR-29b contribute to pancreatic beta-cell-specific silencing of monocarboxylate transporter 1 (Mct1). Mol. Cell. Biol. 31, 3182-3194 (2011).
35. Matkovich, S. J. & Dorn, 2nd G. W. Deep sequencing of cardiac MicroRNAmRNA interactomes in clinical and experimental cardiomyopathy. Methods Mol. Biol. 1299, 27-49 (2015).
36. Joglekar, M. V., Parekh, V. S. & Hardikar, A. A. New pancreas from old: microregulators of pancreas regeneration. Trends. Endocrinol. Metab. 18, 393-400 (2007).
37. Carvalho, C. P., Martins, J. C., da Cunha, D. A., Boschero, A. C. & Collares-Buzato, C. B. Histomorphology and ultrastructure of pancreatic islet tissue during in vivo maturation of rat pancreas. Ann. Anat. 188, 221-234 (2006).
38. Miller, K. et al. Islet formation during the neonatal development in mice. PLoS ONE 4, e7739 (2009).
39. Fox, J. E. et al. Functional plasticity of the human infant beta-cell exocytotic phenotype. Endocrinology 154, 1392-1399 (2013).
40. Gu, C. et al. Pancreatic beta cells require NeuroD to achieve and maintain functional maturity. Cell. Metab. 11, 298-310 (2010).
41. Hang, Y. et al. The MafA transcription factor becomes essential to islet betacells soon after birth. Diabetes 63, 1994-2005 (2014).
42. Piccand, J. et al. Rfx6 maintains the functional identity of adult pancreatic beta cells. Cell Rep. 9, 2219-2232 (2014).
43. Girard, J., Perdereau, D., Foufelle, F., Prip-Buus, C. & Ferre, P. Regulation of lipogenic enzyme gene expression by nutrients and hormones. FASEB J. 8, 36-42 (1994).
44. Kirchner, G., Harbers, M., Bunsch, A., Seitz, H. J. & Hoppner, W. Zonation of glucokinase in rat liver changes during postnatal development. FEBS Lett. 328, 119-124 (1993).
45. Montanya, E., Nacher, V., Biarnes, M. & Soler, J. Linear correlation between beta-cell mass and body weight throughout the lifespan in Lewis rats: role of beta-cell hyperplasia and hypertrophy. Diabetes 49, 1341-1346 (2000).
46. Finegood, D. T., Scaglia, L. & Bonner-Weir, S. Dynamics of beta-cell mass in the growing rat pancreas. Estimation with a simple mathematical model. Diabetes 44, 249-256 (1995).
47. Setyowati Karolina, D., Sepramaniam, S., Tan, H. Z., Armugam, A. & Jeyaseelan, K. miR-25 and miR-92a regulate insulin I biosynthesis in rats. RNA Biol. 10, 1365-1378 (2013).
48. Tan, W., Li, Y., Lim, S. G. & Tan, T. M. Clusters: polycistrons with oncogenic roles in hepatocellular carcinoma. World J. Gastroenterol. 20, 5962-5972 (2014).
49. Wang, B. et al. miR-181b promotes hepatic stellate cells proliferation by targeting p27 and is elevated in the serum of cirrhosis patients. Biochem. Biophys. Res. Commun. 421, 4-8 (2012).
50. Kaspi, H., Pasvolsky, R. & Hornstein, E. Could microRNAs contribute to the maintenance of beta cell identity? Trends Endocrinol. Metab. 25, 285-292 (2014).
51. Aguayo-Mazzucato, C. et al. Mafa expression enhances glucose-responsive insulin secretion in neonatal rat beta cells. Diabetologia 54, 583-593 (2011).
52. MacDonald, M. J. et al. Decreased levels of metabolic enzymes in pancreatic islets of patients with type 2 diabetes. Diabetologia 52, 1087-1091 (2009).
53. Gunton, J. E. et al. Loss of ARNT/HIF1beta mediates altered gene expression and pancreatic-islet dysfunction in human type 2 diabetes. Cell 122, 337-349 (2005).
54. Marselli, L. et al. Gene expression profiles of Beta-cell enriched tissue obtained by laser capture microdissection from subjects with type 2 diabetes. PLoS ONE 5, e11499 (2010).
55. Kelley, D. E., Mokan, M. & Mandarino, L. J. Intracellular defects in glucose metabolism in obese patients with NIDDM. Diabetes 41, 698-706 (1992).
56. Bravo-Egana, V. et al. Quantitative differential expression analysis reveals miR-7 as major islet microRNA. Biochem. Biophys. Res. Commun. 366, 922-926 (2008).
57. Atouf, F., Czernichow, P. & Scharfmann, R. Expression of neuronal traits in pancreatic beta cells. Implication of neuron-restrictive silencing factor/repressor element silencing transcription factor, a neuron-restrictive silencer. J. Biol. Chem. 272, 1929-1934 (1997).
58. Schuit, F. et al. beta-cell-specific gene repression: a mechanism to protect against inappropriate or maladjusted insulin secretion? Diabetes 61, 969-975 (2012).
59. Chen, H. et al. PDGF signalling controls age-dependent proliferation in pancreatic beta-cells. Nature 478, 349-355 (2011).
60. Cerf, M. E. High fat programming of beta cell compensation, exhaustion, death and dysfunction. Pediatr. Diabetes 16, 71-78 (2015).
61. Hu, Y. et al. Epitranscriptional orchestration of genetic reprogramming is an emergent property of stress-regulated cardiac microRNAs. Proc. Natl Acad. Sci. USA 109, 19864-19869 (2012).
62. Matkovich, S. J., Hu, Y. & Dorn, 2nd G. W. Regulation of cardiac microRNAs by cardiac microRNAs. Circ. Res. 113, 62-71 (2013).
63. Huang, da, W., Sherman, B. T. & Lempicki, R. A. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 37, 1-13 (2009).
64. Gotoh, M. et al. Reproducible high yield of rat islets by stationary in vitro digestion following pancreatic ductal or portal venous collagenase injection. Transplantation 43, 725-730 (1987).
65. Jacovetti, C. et al. MicroRNAs contribute to compensatory beta cell expansion during pregnancy and obesity. J. Clin. Invest. 122, 3541-3551 (2012).
66. Kohler, M. et al. One-step purification of functional human and rat pancreatic alpha cells. Integr. Biol. (Camb.) 4, 209-219 (2012).
67. Matkovich, S. J., Hu, Y., Eschenbacher, W. H., Dorn, L. E. & Dorn, 2nd G. W. Direct and indirect involvement of microRNA-499 in clinical and experimental cardiomyopathy. Circ. Res. 111, 521-531 (2012).
68. Anders, S. & Huber, W. Differential expression analysis for sequence count data. Genome. Biol. 11, R106 (2010).