Knockdown of prolactin receptors in a pancreatic beta cell line: Effects on DNA synthesis, apoptosis, and gene expression

Endocrine

Volumn 46, Issue 3, 2014, Pages 568-576

  Arumugam, Ramamani ^a   Fleenor, Don ^a   Freemark, Michael ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

BCL6; Cyclin; FoxM1; IRS 2; Lactogen; PTTG1

Indexed keywords

CYCLIN A; CYCLIN B; CYCLIN B2; CYCLIN D2; INSULIN RECEPTOR SUBSTRATE 2; MESSENGER RNA; PROLACTIN; PROLACTIN RECEPTOR; PROTEIN BCL 6; PROTEIN BCL XL; PROTEIN P21; SECURIN; SMALL INTERFERING RNA; CYCLINE; DNA;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; DNA SYNTHESIS; DOWN REGULATION; GENE EXPRESSION; GENE IDENTIFICATION; GENE SILENCING; INSULINOMA CELL LINE; NONHUMAN; NUCLEOTIDE SEQUENCE; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN INDUCTION; RAT; SIGNAL TRANSDUCTION; ANIMAL; BIOSYNTHESIS; CELL COUNT; GENETICS; INSULINOMA; METABOLISM; PANCREAS TUMOR; PATHOLOGY; TUMOR CELL LINE;

ANIMALS; APOPTOSIS; CELL COUNT; CELL LINE, TUMOR; CYCLINS; DNA; DOWN-REGULATION; GENE EXPRESSION; INSULIN-SECRETING CELLS; INSULINOMA; PANCREATIC NEOPLASMS; RATS; RECEPTORS, PROLACTIN; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

EID: 84904510245     PISSN: 1355008X     EISSN: 15590100     Source Type: Journal    
DOI: 10.1007/s12020-013-0073-1     Document Type: Article

References (42)

1. P.C. Butler, J.J. Meier, A.E. Butler, A. Bhushan, The replication of beta cells in normal physiology, in disease and for therapy. Nat. Clin. Pract. Endocrinol. Metab. 3, 758-768 (2007)
2. J.J. Meier, A.E. Butler, Y. Saisho et al., Beta-cell replication is the primary mechanism subserving the postnatal expansion of beta-cell mass in humans. Diabetes 57, 1584-1594 (2008)
3. F.A. Van Assche, Quantitative morphologic and histoenzymatic study of the endocrine pancreas in nonpregnant and pregnant rats. Am. J. Obstet. Gynecol. 118, 39-41 (1974)
4. A.E. Butler, L. Cao-Minh, R. Galasso et al., Adaptive changes in pancreatic beta cell fractional area and beta cell turnover in human pregnancy. Diabetologia 53, 2167-2176 (2010)
5. P.H. Whincup, S.J. Kaye, C.G. Owen et al., Birth weight and risk of type 2 diabetes: a systematic review. JAMA 300, 2886-2897 (2008)
6. M. Freemark, Placental hormones and the control of fetal growth. J. Clin. Endocrinol. Metab. 95, 2054-2057 (2010)
7. D. Newbern, M. Freemark, Placental hormones and the control of maternal metabolism and fetal growth. Curr. Opin. Endocrinol. Diabetes Obes. 18, 409-416 (2011)
8. M. Freemark, Regulation of maternal metabolism by pituitary and placental hormones: roles in fetal development and metabolic programming. Horm. Res. 65(Suppl 3), 41-49 (2006)
9. M. Freemark, K. Kirk, C. Pihoker, M.C. Robertson, R.P. Shiu, P. Driscoll, Pregnancy lactogens in the rat conceptus and fetus: circulating levels, distribution of binding, and expression of receptor messenger ribonucleic acid. Endocrinology 133, 1830-1842 (1993)
10. R. Arumugam, D. Fleenor, D. Lu, M. Freemark, Differential and complementary effects of glucose and prolactin on islet DNA synthesis and gene expression. Endocrinology 152, 856-868 (2011)
11. R. Arumugam, E. Horowitz, D. Lu et al., The interplay of prolactin and the glucocorticoids in the regulation of beta-cell gene expression, fatty acid oxidation, and glucose-stimulated insulin secretion: implications for carbohydrate metabolism in pregnancy. Endocrinology 149, 5401-5414 (2008)
12. R. Arumugam, E. Horowitz, R.C. Noland, D. Lu, D. Fleenor, M. Freemark, Regulation of islet beta-cell pyruvate metabolism: interactions of prolactin, glucose, and dexamethasone. Endocrinology 151, 3074-3083 (2010)
13. T.C. Brelje, D.W. Scharp, P.E. Lacy et al., Effect of homologous placental lactogens, prolactins, and growth hormones on islet B-cell division and insulin secretion in rat, mouse, and human islets: implication for placental lactogen regulation of islet function during pregnancy. Endocrinology 132, 879-887 (1993)
14. M. Freemark, Ontogenesis of prolactin receptors in the human fetus: roles in fetal development. Biochem. Soc. Trans. 29, 38-41 (2001)
15. L. Labriola, W.R. Montor, K. Krogh et al., Beneficial effects of prolactin and laminin on human pancreatic islet-cell cultures. Mol. Cell. Endocrinol. 263, 120-133 (2007)
16. A. Petryk, D. Fleenor, P. Driscoll, M. Freemark, Prolactin induction of insulin gene expression: the roles of glucose and glucose transporter-2. J. Endocrinol. 164, 277-286 (2000)
17. T. Yamamoto, C. Ricordi, A. Mita et al., beta-Cell specific cytoprotection by prolactin on human islets. Transpl. Proc. 40, 382-383 (2008)
18. D. Fleenor, A. Petryk, P. Driscoll, M. Freemark, Constitutive expression of placental lactogen in pancreatic beta cells: effects on cell morphology, growth, and gene expression. Pediatr. Res. 47, 136-142 (2000)
19. R.C. Vasavada, A. Garcia-Ocana, W.S. Zawalich et al., Targeted expression of placental lactogen in the beta cells of transgenic mice results in beta cell proliferation, islet mass augmentation, and hypoglycemia. J. Biol. Chem. 275, 15399-15406 (2000)
20. M. Freemark, I. Avril, D. Fleenor et al., Targeted deletion of the PRL receptor: effects on islet development, insulin production, and glucose tolerance. Endocrinology 143, 1378-1385 (2002)
21. C. Huang, F. Snider, J.C. Cross, Prolactin receptor is required for normal glucose homeostasis and modulation of beta-cell mass during pregnancy. Endocrinology 150, 1618-1626 (2009)
22. S.K. Karnik, H. Chen, G.W. McLean et al., Menin controls growth of pancreatic beta-cells in pregnant mice and promotes gestational diabetes mellitus. Science 318, 806-809 (2007)
23. H. Kim, Y. Toyofuku, F.C. Lynn, Serotonin regulates pancreatic beta cell mass during pregnancy. Nat. Med. 16, 804-808 (2010)
24. A. Schraenen, K. Lemaire, G. de Faudeur et al., Placental lactogens induce serotonin biosynthesis in a subset of mouse beta cells during pregnancy. Diabetologia 53, 2589-2599 (2010)
25. T.C. Becker, R.J. Noel, W.S. Coats et al., Use of recombinant adenovirus for metabolic engineering of mammalian cells. Methods Cell Biol. 43, 161-189 (1994)
26. H.E. Hohmeier, H. Mulder, G. Chen, R. Henkel-Rieger, M. Prentki, C.B. Newgard, Isolation of INS-1-derived cell lines with robust ATP-sensitive K? channel-dependent and -independent glucose-stimulated insulin secretion. Diabetes 49, 424-430 (2000)
27. M.D. Holland, K.L. Hossner, S.E. Williams, C.R. Wallace, G.D. Niswender, K.G. Odde, Serum concentrations of insulin-like growth factors and placental lactogen during gestation in cattle. I. Fetal profiles. Domest. Anim. Endocrinol. 14, 231-239 (1997)
28. B.N. Friedrichsen, H.E. Richter, J.A. Hansen et al., Signal transducer and activator of transcription 5 activation is sufficient to drive transcriptional induction of cyclin D2 gene and proliferation of rat pancreatic beta-cells. Mol. Endocrinol. 17, 945-958 (2003)
29. S. Georgia, A. Bhushan, Beta cell replication is the primary mechanism for maintaining postnatal beta cell mass. J. Clin. Invest. 114, 963-968 (2004)
30. J.A. Kushner, M.A. Ciemerych, E. Sicinska et al., Cyclins D2 and D1 are essential for postnatal pancreatic beta-cell growth. Mol. Cell. Biol. 25, 3752-3762 (2005)
31. S. Rieck, P. White, J. Schug et al., The transcriptional response of the islet to pregnancy in mice. Mol. Endocrinol. 23, 1702-1712 (2009)
32. H. Zhang, J. Zhang, C.F. Pope et al., Gestational diabetes mellitus resulting from impaired beta-cell compensation in the absence of FoxM1, a novel downstream effector of placental lactogen. Diabetes 59, 143-152 (2010)
33. N. Kubota, K. Tobe, Y. Terauchi et al., Disruption of insulin receptor substrate 2 causes type 2 diabetes because of liver insulin resistance and lack of compensatory beta-cell hyperplasia. Diabetes 49, 1880-1889 (2000)
34. Y. Fujinaka, K. Takane, H. Yamashita, R.C. Vasavada, Lactogens promote beta cell survival through JAK2/STAT5 activation and Bcl-XL upregulation. J. Biol. Chem. 282, 30707-30717 (2007)
35. N.G. Kondegowda, A. Mozar, C. Chin, A. Otero, A. Garcia-Ocana, R.C. Vasavada, Lactogens protect rodent and human beta cells against glucolipotoxicity-induced cell death through Janus kinase-2 (JAK2)/signal transducer and activator of transcription-5 (STAT5) signalling. Diabetologia 55, 1721-1732 (2012)
36. V. Chesnokova, C. Wong, S. Zonis et al., Diminished pancreatic beta-cell mass in securin-null mice is caused by beta-cell apoptosis and senescence. Endocrinology 150, 2603-2610 (2009)
37. R. Yu, M. Cruz-Soto, S. Li Calzi, H. Hui, S. Melmed, Murine pituitary tumor-transforming gene functions as a securin protein in insulin-secreting cells. J. Endocrinol. 191, 45-53 (2006)
38. T.H. Tran, F.E. Utama, J. Lin et al., Prolactin inhibits BCL6 expression in breast cancer through a Stat5a-dependent mechanism. Cancer Res. 70, 1711-1721 (2010)
39. S.R. Walker, E.A. Nelson, D.A. Frank, STAT5 represses BCL6 expression by binding to a regulatory region frequently mutated in lymphomas. Oncogene 26, 224-233 (2007)
40. H. Xiong, W.Y. Su, Q.C. Liang et al., Inhibition of STAT5 induces G1 cell cycle arrest and reduces tumor cell invasion in human colorectal cancer cells. Lab. Invest. 89, 717-725 (2009)
41. R.D. Meyer, E.V. Laz, T. Su, D.J. Waxman, Male-specific hepatic Bcl6: growth hormone-induced block of transcription elongation in females and binding to target genes inversely coordinated with STAT5. Mol. Endocrinol. 23, 1914-1926 (2009)
42. S.C. Martinez, C. Cras-Meneur, E. Bernal-Mizrachi, M.A. Permutt, Glucose regulates FoxO1 through insulin receptor signaling in the pancreatic islet beta-cell. Diabetes 55, 1581-1591 (2006)