Augmented STAT5 signaling bypasses multiple impediments to lactogen-mediated proliferation in human β-cells

Diabetes

Volumn 64, Issue 11, 2015, Pages 3784-3797

  Chen, Hainan ^a   Kleinberger, Jeffrey W ^b   Takane, Karen K ^a   Salim, Fatimah ^c   Fiaschi Taesch, Nathalie ^a   Pappas, Kyrie ^a   Parsons, Ramon ^a   Jiang, Jing ^d   Zhang, Yue ^d   Liu, Hongtao ^a   Wang, Peng ^a   Bender, Aaron S ^a   Frank, Stuart J ^d,e   Stewart, Andrew F ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^c DUQUESNE UNIVERSITY   (United States)

^d UNIVERSITY OF ALABAMA SCHOOL OF MEDICINE   (United States)

^e BIRMINGHAM VA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN D1; CYCLIN D2; CYCLIN D3; CYCLIN DEPENDENT KINASE 4; CYCLIN DEPENDENT KINASE INHIBITOR; JANUS KINASE 2; MESSENGER RNA; PLACENTA LACTOGEN; PROLACTIN; PROLACTIN RECEPTOR; PROTEIN INHIBITOR OF ACTIVATED STAT; STAT5 PROTEIN; STAT5A PROTEIN; CYCLIN D;

ADULT; AGED; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL CYCLE; CELL EXPANSION; CELL FUNCTION; CELL PROLIFERATION; CELL SIZE; CELL SURVIVAL; CONTROLLED STUDY; FEMALE; HISTOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOCYTOCHEMISTRY; MALE; MCF 7 CELL LINE; NONHUMAN; PANCREAS ISLET; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; ANIMAL; CELL LINE; CYTOLOGY; DRUG EFFECTS; GENETICS; METABOLISM; MOUSE; PHOSPHORYLATION; PHYSIOLOGY; UPREGULATION;

ANIMALS; CELL LINE; CELL PROLIFERATION; CYCLIN D; CYCLIN-DEPENDENT KINASE 4; HUMANS; INSULIN-SECRETING CELLS; MICE; PHOSPHORYLATION; PROLACTIN; RECEPTORS, PROLACTIN; SIGNAL TRANSDUCTION; STAT5 TRANSCRIPTION FACTOR; UP-REGULATION;

EID: 84962170665     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db15-0083     Document Type: Article

References (49)

1. Gregg BE, Moore PC, Demozay D, et al. Formation of a human β-cell population within pancreatic islets is set early in life. J Clin Endocrinol Metab 2012;97:3197-3206
2. Butler AE, Janson J, Bonner-Weir S, Ritzel R, Rizza RA, Butler PC. Beta-cell deficit and increased beta-cell apoptosis in humans with type 2 diabetes. Diabetes 2003;52:102-110
3. Rahier J, Guiot Y, Goebbels RM, Sempoux C, Henquin JC. Pancreatic betacell mass in European subjects with type 2 diabetes. Diabetes Obes Metab 2008;10(Suppl 4):32-42
4. Menge BA, Tannapfel A, Belyaev O, et al. Partial pancreatectomy in adult humans does not provoke beta-cell regeneration. Diabetes 2008;57:142-149
5. Parnaud G, Bosco D, Berney T, et al. Proliferation of sorted human and rat beta cells. Diabetologia 2008;51:91-100
6. Levitt HE, Cyphert TJ, Pascoe JL, et al. Glucose stimulates human beta cell replication in vivo in human islets transplanted into NOD-severe combined immunodeficiency (SCID) mice. Diabetologia 2011;54:572-582
7. Maedler K, Schumann DM, Schulthess F, et al. Aging correlates with decreased beta-cell proliferative capacity and enhanced sensitivity to apoptosis: a potential role for Fas and pancreatic duodenal homeobox-1. Diabetes 2006;55:2455-2462
8. Butler AE, Cao-Minh L, Galasso R, et al. Adaptive changes in pancreatic beta cell fractional area and beta cell turnover in human pregnancy. Diabetologia 2010;53:2167-2176
9. Wang P, Fiaschi-Taesch NM, Vasavada RC, Scott DK, Garcia-Ocaña A, Stewart AF. Diabetes mellitus-advances and challenges in human β-cell proliferation. Nat Rev Endocrinol 2015;11:201-212
10. Stewart AF, Hussain MA, Garcia-Ocaña A, et al. Human β-cell proliferation and intracellular signaling: part 3. Diabetes 2015;64:1872-1885
11. Fiaschi-Taesch NM, Kleinberger JW, Salim FG, et al. Human pancreatic β-cell G1/S molecule cell cycle atlas. Diabetes 2013;62:2450-2459
12. Fiaschi-Taesch NM, Kleinberger JW, Salim FG, et al. Cytoplasmic-nuclear trafficking of G1/S cell cycle molecules and adult human β-cell replication: a revised model of human β-cell G1/S control. Diabetes 2013;62:2460-2470
13. Alonso LC, Yokoe T, Zhang P, et al. Glucose infusion in mice: a new model to induce beta-cell replication. Diabetes 2007;56:1792-1801
14. Kushner JA, Ciemerych MA, Sicinska E, et al. Cyclins D2 and D1 are essential for postnatal pancreatic beta-cell growth. Mol Cell Biol 2005;25:3752-3762
15. Georgia S, Hinault C, Kawamori D, et al. Cyclin D2 is essential for the compensatory β-cell hyperplastic response to insulin resistance in rodents. Diabetes 2010;59:987-996
16. Fiaschi-Taesch N, Bigatel TA, Sicari B, et al. Survey of the human pancreatic beta-cell G1/S proteome reveals a potential therapeutic role for cdk-6 and cyclin D1 in enhancing human beta-cell replication and function in vivo. Diabetes 2009;58:882-893
17. Fiaschi-Taesch NM, Salim F, Kleinberger J, et al. Induction of human betacell proliferation and engraftment using a single G1/S regulatory molecule, cdk6. Diabetes 2010;59:1926-1936
18. Lavine JA, Raess PW, Davis DB, et al. Overexpression of pre-procholecystokinin stimulates beta-cell proliferation in mouse and human islets with retention of islet function [retracted in: Mol Endocrinol 2010;24:472]. Mol Endocrinol 2008;22:2716-2728
19. Davis DB, Lavine JA, Suhonen JI, et al. FoxM1 is up-regulated by obesity and stimulates beta-cell proliferation. Mol Endocrinol 2010;24:1822-1834
20. Metzger BE, Phelps RL. Diabetes mellitus and pregnancy. In Endocrinology. 6th ed. DeGroot L, Jameson L, Eds. Philadelphia, Saunders Elsevier, 2010, p. 2644-2661
21. Sorenson RL, Brelje TC. Adaptation of islets of Langerhans to pregnancy: beta-cell growth, enhanced insulin secretion and the role of lactogenic hormones. Horm Metab Res 1997;29:301-307
22. Brelje TC, Scharp DW, Lacy PE, 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 1993;132:879-887
23. Sorenson RL, Stout LE. Prolactin receptors and JAK2 in islets of Langerhans: an immunohistochemical analysis. Endocrinology 1995;136:4092-4098
24. Stout LE, Svensson AM, Sorenson RL. Prolactin regulation of islet-derived INS-1 cells: characteristics and immunocytochemical analysis of STAT5 translocation. Endocrinology 1997;138:1592-1603
25. Jackerott M, Møldrup A, Thams P, et al. STAT5 activity in pancreatic betacells influences the severity of diabetes in animal models of type 1 and 2 diabetes. Diabetes 2006;55:2705-2712
26. Friedrichsen BN, Richter HE, Hansen JA, 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 2003;17:945-958
27. Vasavada RC, Garcia-Ocaña A, Zawalich WS, 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 2000;275:15399-15406
28. Kondegowda GN, Mozar A, Otero A, Chin C, Garcia-Ocaña A, Vasavada RC. 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 2012;55:1721-1732
29. Schraenen A, Lemaire K, De Faudeur G, et al. Placental lactogens induce serotonin biosynthesis in a subset of mouse beta cells during pregnancy. Diabetologia 2010;53:2589-2599
30. Zhang H, Zhang J, Pope CF, et al. Gestational diabetes mellitus resulting from impaired β-cell compensation in the absence of FoxM1, a novel downstream effector of placental lactogen. Diabetes 2010;59:143-152
31. Freemark M, Avril I, Fleenor D, et al. Targeted deletion of the PRL receptor: effects on islet development, insulin production, and glucose tolerance. Endocrinology 2002;143:1378-1385
32. Arumugam R, Fleenor D, Freemark M. Knockdown of prolactin receptors in a pancreatic cell line: effects on DNA synthesis, apoptosis, and gene expression. Endocrine 2014;46:568-576,. 2011.
33. Demirci C, Ernst S, Alvarez-Perez JC, et al. Loss of HGF/c-Met signaling in pancreatic β-cells leads to incomplete maternal β-cell adaptation and gestational diabetes. Diabetes 2012;61:1143-1152
34. Karnik SK, Chen H, McLean GW, et al. Menin controls growth of pancreatic beta-cells in pregnant mice and promotes gestational diabetes mellitus. Science 2007;318:806-809
35. Kim H, Toyofuku Y, Lynn FC, et al. Serotonin regulates pancreatic beta cell mass during pregnancy. Nat Med 2010;16:804-808
36. Rieck S, Kaestner KH. Expansion of beta-cell mass in response to pregnancy. Trends Endocrinol Metab 2010;21:151-158
37. Johansson M, Olerud J, Jansson L, Carlsson PO. Prolactin treatment improves engraftment and function of transplanted pancreatic islets. Endocrinology 2009;150:1646-1653
38. Nyga R, Pecquet C, Harir N, et al. Activated STAT5 proteins induce activation of the PI 3-kinase/Akt and Ras/MAPK pathways via the Gab2 scaffolding adapter. Biochem J 2005;390:359-366
39. Le TN, Elsea SH, Romero R, Chaiworapongsa T, Francis GL. Prolactin receptor gene polymorphisms are associated with gestational diabetes. Genet Test Mol Biomarkers 2013;17:567-571
40. Cozar-Castellano I, Takane KK, Bottino R, Balamurugan AN, Stewart AF. Induction of beta-cell proliferation and retinoblastoma protein phosphorylation in rat and human islets using adenovirus-mediated transfer of cyclin-dependent kinase-4 and cyclin D1. Diabetes 2004;53:149-159
41. Rao P, Roccisana J, Takane KK, et al. Gene transfer of constitutively active Akt markedly improves human islet transplant outcomes in diabetic severe combined immunodeficient mice. Diabetes 2005;54:1664-1675
42. Karslioglu E, Kleinberger JW, Salim FG, et al. cMyc is a principal upstream driver of beta-cell proliferation in rat insulinoma cell lines and is an effective mediator of human beta-cell replication. Mol Endocrinol 2011;25:1760-1772
43. Chen H, Gu X, Liu Y, et al. PDGF signalling controls age-dependent proliferation in pancreatic β-cells. Nature 2011;478:349-355
44. Benner C, Van Der Meulen T, Cacéres E, Tigyi K, Donaldson CJ, Huising MO. The transcriptional landscape of mouse beta cells compared to human beta cells reveals notable species differences in long non-coding RNA and protein-coding gene expression. BMC Genomics 2014;15:620
45. Nica AC, Ongen H, Irminger J-C, et al. Cell-type, allelic, and genetic signatures in the human pancreatic beta cell transcriptome. Genome Res 2013;23:1554-1562
46. Blodgett DM, Nowosielska A, Afik S, et al. Novel observations from next generation RNA sequencing of highly purified human adult and fetal islet cell subsets. Diabetes 30 April 2015 [Epub ahead of print]
47. Jiao Y, Rieck S, Le Lay J, Kaestner KH. CISH has no non-redundant functions in glucose homeostasis or beta cell proliferation during pregnancy in mice. Diabetologia 2013;56:2435-2445
48. Agarwal SK, Mateo CM, Marx SJ. Rare germline mutations in cyclindependent kinase inhibitor genes in multiple endocrine neoplasia type 1 and related states. J Clin Endocrinol Metab 2009;94:1826-1834
49. Brouwers B, De Faudeur G, Osipovich AB, et al. Impaired islet function in commonly used transgenic mouse lines due to human growth hormone minigene expression. Cell Metab 2014;20:979-990