Prolactin-stimulated survivin induction is required for beta cell mass expansion during pregnancy in mice

Diabetologia

Volumn 58, Issue 9, 2015, Pages 2064-2073

  Xu, Yili ^a   Wang, Xiaojing ^a   Gao, Li ^a   Zhu, Jiayu ^a   Zhang, Hui ^a   Shi, Houxia ^a   Woo, Minna ^b   Wu, Xiaohong ^a  

^a THE FIRST AFFILIATED HOSPITAL OF NANJING MEDICAL UNIVERSITY   (China)

^b UNIVERSITY HEALTH NETWORK   (Canada)

Author keywords

Beta cell mass; Pregnancy; Prolactin; Signalling pathway; Survivin

Indexed keywords

CYCLIN B1; CYCLIN D1; CYCLIN DEPENDENT KINASE 1; CYCLIN DEPENDENT KINASE 2; CYCLIN DEPENDENT KINASE 4; CYCLIN E; CYCLIN E1; INSULIN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; PROLACTIN; PROLACTIN RECEPTOR; PROTEIN KINASE B INHIBITOR; PROTEIN P16; PROTEIN P21; PROTEIN P53; STAT5 PROTEIN; SURVIVIN; TRANSCRIPTION FACTOR E2F1; UNCLASSIFIED DRUG; BIRC5 PROTEIN, MOUSE; GLUCOSE; INHIBITOR OF APOPTOSIS PROTEIN; REPRESSOR PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE PROGRESSION; CELL CYCLE S PHASE; CELL EXPANSION; CELL PROLIFERATION; CELL SIZE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVATION; FEMALE; G1 PHASE CELL CYCLE CHECKPOINT; GENE DELETION; GENETIC TRANSFECTION; GLUCOSE HOMEOSTASIS; GLUCOSE INTOLERANCE; GLUCOSE TOLERANCE; INS 1 CELL LINE; INSULIN BLOOD LEVEL; MOLECULAR WEIGHT; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PREGNANCY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN LOCALIZATION; S PHASE CELL CYCLE CHECKPOINT; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; APOPTOSIS; C57BL MOUSE; CELL LINE; CYTOLOGY; GENOTYPE; GLUCOSE TOLERANCE TEST; INSULINOMA; KNOCKOUT MOUSE; METABOLISM;

ANIMALS; APOPTOSIS; CELL LINE; CELL PROLIFERATION; FEMALE; GENOTYPE; GLUCOSE; GLUCOSE TOLERANCE TEST; INHIBITOR OF APOPTOSIS PROTEINS; INSULIN-SECRETING CELLS; INSULINOMA; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PREGNANCY; PROLACTIN; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION; STAT5 TRANSCRIPTION FACTOR;

EID: 84938749434     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-015-3670-0     Document Type: Article

References (44)

1. Sorenson RL, Brelje TC (1997) Adaptation of islets of Langerhans to pregnancy: beta-cell growth, enhanced insulin secretion and the role of lactogenic hormones. Horm Metab Res 29:301–307
2. Parsons JA, Brelje TC, Sorenson RL (1992) Adaptation of islets of Langerhans to pregnancy: increased islet cell proliferation and insulin secretion correlates with the onset of placental lactogen secretion. Endocrinology 130:1459–1466
3. Van Assche FA, Aerts L, De Prins F (1978) A morphological study of the endocrine pancreas in human pregnancy. Br J Obstet Gynaecol 85:818–820
4. Butler AE, Cao-Minh L, Galasso R et al (2010) Adaptive changes in pancreatic beta cell fractional area and beta cell turnover in human pregnancy. Diabetologia 53:2167–2176
5. Kim C, Newton KM, Knopp RH (2002) Gestational diabetes and the incidence of type 2 diabetes: a systematic review. Diabetes Care 25:1862–1868
6. Brelje TC, Stout LE, Bhagroo NV, Sorenson RL (2004) Distinctive roles for prolactin and growth hormone in the activation of signal transducer and activator of transcription 5 in pancreatic islets of Langerhans. Endocrinology 145:4162–4175
7. Amaral ME, Cunha DA, Anhe GF et al (2004) Participation of prolactin receptors and phosphatidylinositol 3-kinase and MAP kinase pathways in the increase in pancreatic islet mass and sensitivity to glucose during pregnancy. J Endocrinol 183:469–476
8. Amaral ME, Ueno M, Carvalheira JB et al (2003) Prolactin-signal transduction in neonatal rat pancreatic islets and interaction with the insulin-signaling pathway. Horm Metab Res 35:282–289
9. Hugl SR, Merger M (2007) Prolactin stimulates proliferation of the glucose-dependent beta-cell line INS-1 via different IRS-proteins. JOP 8:739–752
10. Friedrichsen BN, Galsgaard ED, Nielsen JH, Moldrup A (2001) Growth hormone- and prolactin-induced proliferation of insulinoma cells, INS-1, depends on activation of STAT5 (signal transducer and activator of transcription 5). Mol Endocrinol 15:136–148
11. Mita AC, Mita MM, Nawrocki ST, Giles FJ (2008) Survivin: key regulator of mitosis and apoptosis and novel target for cancer therapeutics. Clin Cancer Res 14:5000–5005
12. Altieri DC (2008) Survivin, cancer networks and pathway-directed drug discovery. Nat Rev Cancer 8:61–70
13. Altieri DC (2008) New wirings in the survivin networks. Oncogene 27:6276–6284
14. Wu X, Wang L, Schroer S et al (2009) Perinatal survivin is essential for the establishment of pancreatic beta cell mass in mice. Diabetologia 52:2130–2141
15. Jiang Y, Nishimura W, Devor-Henneman D et al (2008) Postnatal expansion of the pancreatic beta-cell mass is dependent on survivin. Diabetes 57:2718–2727
16. Wu X, Zhang Q, Wang X et al (2012) Survivin is required for beta-cell mass expansion in the pancreatic duct-ligated mouse model. Plos One 7:e41976
17. Rieck S, White P, Schug J et al (2009) The transcriptional response of the islet to pregnancy in mice. Mol Endocrinol 23:1702–1712
18. Hakonen E, Ustinov J, Palgi J, Miettinen PJ, Otonkoski T (2014) EGFR signaling promotes beta-cell proliferation and survivin expression during pregnancy. Plos One 9:e93651
19. Nguyen KT, Tajmir P, Lin CH et al (2006) Essential role of Pten in body size determination and pancreatic beta-cell homeostasis in vivo. Mol Cell Biol 26:4511–4518
20. Liadis N, Murakami K, Eweida M et al (2005) Caspase-3-dependent beta-cell apoptosis in the initiation of autoimmune diabetes mellitus. Mol Cell Biol 25:3620–3629
21. Xue Y, Liu C, Xu Y et al (2010) Study on pancreatic islet adaptation and gene expression during pregnancy in rats. Endocrine 37:83–97
22. Wang H, Gambosova K, Cooper ZA et al (2010) EGF regulates survivin stability through the Raf-1/ERK pathway in insulin-secreting pancreatic beta-cells. BMC Mol Biol 11:66
23. Rieck S, Kaestner KH (2010) Expansion of beta-cell mass in response to pregnancy. Trends Endocrinol Metab 21:151–158
24. Weinhaus AJ, Stout LE, Bhagroo NV, Brelje TC, Sorenson RL (2007) Regulation of glucokinase in pancreatic islets by prolactin: a mechanism for increasing glucose-stimulated insulin secretion during pregnancy. J Endocrinol 193:367–381
25. Parsons JA, Bartke A, Sorenson RL (1995) Number and size of islets of Langerhans in pregnant, human growth hormone-expressing transgenic, and pituitary dwarf mice: effect of lactogenic hormones. Endocrinology 136:2013–2021
26. Freemark M, Avril I, Fleenor D et al (2002) Targeted deletion of the PRL receptor: effects on islet development, insulin production, and glucose tolerance. Endocrinology 143:1378–1385
27. Huang C, Snider F, Cross JC (2009) Prolactin receptor is required for normal glucose homeostasis and modulation of beta-cell mass during pregnancy. Endocrinology 150:1618–1626
28. Zhang H, Zhang J, Pope CF et al (2010) 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
29. Gianani R, Campbell-Thompson M, Sarkar SA et al (2010) Dimorphic histopathology of long-standing childhood-onset diabetes. Diabetologia 53:690–698
30. Hasel C, Bhanot UK, Heydrich R, Strater J, Moller P (2005) Parenchymal regression in chronic pancreatitis spares islets reprogrammed for the expression of NFκB and IAPs. Lab Invest 85:1263–1275
31. Liggins C, Orlicky DJ, Bloomquist LA, Gianani R (2003) Developmentally regulated expression of survivin in human pancreatic islets. Pediatr Dev Pathol 6:392–397
32. Chen HZ, Tsai SY, Leone G (2009) Emerging roles of E2Fs in cancer: an exit from cell cycle control. Nat Rev Cancer 9:785–797
33. Chen J, Jackson PK, Kirschner MW, Dutta A (1995) Separate domains of p21 involved in the inhibition of Cdk kinase and PCNA. Nature 374:386–388
34. Goubin F, Ducommun B (1995) Identification of binding domains on the p21Cip1 cyclin-dependent kinase inhibitor. Oncogene 10:2281–2287
35. LaBaer J, Garrett MD, Stevenson LF et al (1997) New functional activities for the p21 family of CDK inhibitors. Genes Dev 11:847–862
36. Cheng M, Olivier P, Diehl JA et al (1999) The p21(Cip1) and p27(Kip1) CDK ‘inhibitors’ are essential activators of cyclin D-dependent kinases in murine fibroblasts. EMBO J 18:1571–1583
37. Li F, Ackermann EJ, Bennett CF et al (1999) Pleiotropic cell-division defects and apoptosis induced by interference with survivin function. Nat Cell Biol 1:461–466
38. Ezhevsky SA, Nagahara H, Vocero-Akbani AM, Gius DR, Wei MC, Dowdy SF (1997) Hypo-phosphorylation of the retinoblastoma protein (pRb) by cyclin D:Cdk4/6 complexes results in active pRb. Proc Natl Acad Sci U S A 94:10699–10704
39. Resnitzky D, Reed SI (1995) Different roles for cyclins D1 and E in regulation of the G1-to-S transition. Mol Cell Biol 15:3463–3469
40. Le TN, Elsea SH, Romero R, Chaiworapongsa T, Francis GL (2013) Prolactin receptor gene polymorphisms are associated with gestational diabetes. Genet Test Mol Biomarkers 17:567–571
41. Kalin TV, Ustiyan V, Kalinichenko VV (2011) Multiple faces of FoxM1 transcription factor: lessons from transgenic mouse models. Cell Cycle 10:396–405
42. Wang IC, Chen YJ, Hughes D et al (2005) Forkhead box M1 regulates the transcriptional network of genes essential for mitotic progression and genes encoding the SCF (Skp2-Cks1) ubiquitin ligase. Mol Cell Biol 25:10875–10894
43. Gannon M, Shiota C, Postic C, Wright CV, Magnuson M (2000) Analysis of the Cre-mediated recombination driven by rat insulin promoter in embryonic and adult mouse pancreas. Genesis 26:139–142
44. Brouwers B, de Faudeur G, Osipovich AB et al (2014) Impaired islet function in commonly used transgenic mouse lines due to human growth hormone minigene expression. Cell Metab 20:979–990