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Current Vascular Pharmacology

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ISSN (Print): 1570-1611
ISSN (Online): 1875-6212

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Review Article

Metabolic Adaptations to Pregnancy in Healthy and Gestational Diabetic Pregnancies: The Pancreas - Placenta Axis

Author(s): Sandra K. Szlapinski and David J. Hill*

Volume 19, Issue 2, 2021

Published on: 20 March, 2020

Page: [141 - 153] Pages: 13

DOI: 10.2174/1570161118666200320111209

Price: $65

Abstract

Normal pregnancy is associated with increased insulin resistance as a metabolic adaptation to the nutritional demands of the placenta and fetus, and this is amplified in obese mothers. Insulin resistance is normally compensated for by an adaptive increase in pancreatic β-cell mass together with enhanced glucose-stimulated insulin release. Placentally-derived hormones and growth factors are central to the altered pancreatic morphology and function. A failure of β-cells to undergo adaptive change after the first trimester has been linked with gestational diabetes. In the pregnant mouse, an increase in β-cell replication contributes to a 2-3-fold increase in mass peaking in late gestation, depending on the proliferation of existing β-cells, the differentiation of resident progenitor β-cells, or islet cell transdifferentiation. Using mouse models and human studies placenta- and islet of Langerhans-derived molecules have been identified that are likely to contribute to the metabolic adaptations to pregnancy and whose physiology is altered in the obese, glucose-intolerant mother. Maternal obesity during pregnancy can create a pro-inflammatory environment that can disrupt the response of the β-cells to the endocrine signals of pregnancy and limit the adaptive changes in β-cell mass and function, resulting in an increased risk of gestational diabetes.

Keywords: β-cell, pancreas, placenta, placental lactogen, proliferation, apelin, kisspeptin, gestational diabetes.

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[1]
Finegood DT, Scaglia L, Bonner-Weir S. Dynamics of beta-cell mass in the growing rat pancreas. Estimation with a simple mathematical model. Diabetes 1995; 44(3): 249-56.
[http://dx.doi.org/10.2337/diab.44.3.249] [PMID: 7883109]
[2]
Perl S, Kushner JA, Buchholz BA, et al. Significant human beta-cell turnover is limited to the first three decades of life as determined by in vivo thymidine analog incorporation and radiocarbon dating. J Clin Endocrinol Metab 2010; 95(10): E234-9.
[http://dx.doi.org/10.1210/jc.2010-0932] [PMID: 20660050]
[3]
Meier JJ, Butler AE, Saisho Y, et al. Beta-cell replication is the primary mechanism subserving the postnatal expansion of beta-cell mass in humans. Diabetes 2008; 57(6): 1584-94.
[http://dx.doi.org/10.2337/db07-1369] [PMID: 18334605]
[4]
Bouwens L, Pipeleers DG. Extra-insular beta cells associated with ductules are frequent in adult human pancreas. Diabetologia 1998; 41(6): 629-33.
[http://dx.doi.org/10.1007/s001250050960] [PMID: 9662042]
[5]
Bonner-Weir S. beta-cell turnover: its assessment and implications. Diabetes 2001; 50(Suppl. 1): S20-4.
[http://dx.doi.org/10.2337/diabetes.50.2007.S20] [PMID: 11272192]
[6]
Newbern D, Freemark M. Placental hormones and the control of maternal metabolism and fetal growth. Curr Opin Endocrinol Diabetes Obes 2011; 18(6): 409-16.
[http://dx.doi.org/10.1097/MED.0b013e32834c800d] [PMID: 21986512]
[7]
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(20): 15399-406.
[http://dx.doi.org/10.1074/jbc.275.20.15399] [PMID: 10809775]
[8]
Baeyens L, Hindi S, Sorenson RL. German MS. β-Cell adaptation in pregnancy. Diabetes Obes Metab 2016; 18(Suppl. 1): 63-70.
[http://dx.doi.org/10.1111/dom.12716] [PMID: 27615133]
[9]
Parsons JA, Brelje TC, Sorenson RL. Adaptation of islets of Langerhans to pregnancy: increased islet cell proliferation and insulin secretion correlates with the onset of placental lactogen secretion. Endocrinology 1992; 130(3): 1459-66.
[http://dx.doi.org/10.1210/endo.130.3.1537300] [PMID: 1537300]
[10]
Lain KY, Catalano PM. Metabolic changes in pregnancy. Clin Obstet Gynecol 2007; 50(4): 938-48.
[http://dx.doi.org/10.1097/GRF.0b013e31815a5494] [PMID: 17982337]
[11]
Van Assche FA, Aerts L, Gepts W. Morphological changes in the endocrine pancreas in pregnant rats with experimental diabetes. J Endocrinol 1979; 80(2): 175-9.
[http://dx.doi.org/10.1677/joe.0.0800175] [PMID: 374672]
[12]
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(6): 301-7.
[http://dx.doi.org/10.1055/s-2007-979040] [PMID: 9230352]
[13]
Beamish CA, Zhang L, Szlapinski SK, Strutt BJ, Hill DJ. An increase in immature β-cells lacking Glut2 precedes the expansion of β-cell mass in the pregnant mouse. PLoS One 2017; 12(7)e0182256
[http://dx.doi.org/10.1371/journal.pone.0182256] [PMID: 28753672]
[14]
Rieck S, Kaestner KH. Expansion of β-cell mass in response to pregnancy. Trends Endocrinol Metab 2010; 21(3): 151-8.
[http://dx.doi.org/10.1016/j.tem.2009.11.001] [PMID: 20015659]
[15]
Szlapinski SK, King RT, Retta G, Yeo E, Strutt BJ, Hill DJ. A mouse model of gestational glucose intolerance through exposure to a low protein diet during fetal and neonatal development. J Physiol 2019; 597(16): 4237-50.
[http://dx.doi.org/10.1113/JP277884] [PMID: 31206692]
[16]
Malassiné A, Frendo J-L, Evain-Brion D. A comparison of placental development and endocrine functions between the human and mouse model. Hum Reprod Update 2003; 9(6): 531-9.
[http://dx.doi.org/10.1093/humupd/dmg043] [PMID: 14714590]
[17]
Mauvais-Jarvis F. Role of sex steroids in β cell function, growth, and surviva. Trends Endocrinol Metab 2016; 27(12): 844-55.
[http://dx.doi.org/10.1016/j.tem.2016.08.008] [PMID: 27640750]
[18]
Bone AJ, Taylor KW. Metabolic adaptation to pregnancy shown by increased biosynthesis of insulin in islets of Langerhans isolated from pregnant rats. Nature 1976; 262: 501-2.
[http://dx.doi.org/10.1038/262501a0] [PMID: 785279]
[19]
Green IC, Howell SL, Montague W, Taylor KW. Regulation of insulin release from isolated islets of Langerhans of the rat in pregnancy. The role of adenosine 3′:5′-cyclic monophosphate. Biochem J 1973; 134(2): 481-7.
[http://dx.doi.org/10.1042/bj1340481] [PMID: 16742808]
[20]
Scaglia L, Smith FE, Bonner-Weir S. Apoptosis contributes to the involution of beta cell mass in the post partum rat pancreas. Endocrinology 1995; 136(12): 5461-8.
[http://dx.doi.org/10.1210/endo.136.12.7588296] [PMID: 7588296]
[21]
Van Assche FA, Aerts L, De Prins F. A morphological study of the endocrine pancreas in human pregnancy. Br J Obstet Gynaecol 1978; 85(11): 818-20.
[http://dx.doi.org/10.1111/j.1471-0528.1978.tb15835.x] [PMID: 363135]
[22]
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(10): 2167-76.
[http://dx.doi.org/10.1007/s00125-010-1809-6] [PMID: 20523966]
[23]
Dolenšek J, Rupnik MS, Stožer A. Structural similarities and differences between the human and the mouse pancreas. Islets 2015; 7(1)e1024405
[http://dx.doi.org/10.1080/19382014.2015.1024405] [PMID: 26030186]
[24]
Wang P, Fiaschi-Taesch NM, Vasavada RC, Scott DK, García-Ocaña A, Stewart AF. Diabetes mellitus--advances and challenges in human β-cell proliferation. Nat Rev Endocrinol 2015; 11(4): 201-12.
[http://dx.doi.org/10.1038/nrendo.2015.9] [PMID: 25687999]
[25]
Huang C, Snider F, Cross JC. Prolactin receptor is required for normal glucose homeostasis and modulation of beta-cell mass during pregnancy. Endocrinology 2009; 150(4): 1618-26.
[http://dx.doi.org/10.1210/en.2008-1003] [PMID: 19036882]
[26]
Kim H, Toyofuku Y, Lynn FC, et al. Serotonin regulates pancreatic beta cell mass during pregnancy. Nat Med 2010; 16(7): 804-8.
[http://dx.doi.org/10.1038/nm.2173] [PMID: 20581837]
[27]
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(2): 879-87.
[http://dx.doi.org/10.1210/endo.132.2.8425500] [PMID: 8425500]
[28]
Chen H, Kleinberger JW, Takane KK, et al. Augmented stat5 signaling bypasses multiple Impediments to lactogen-mediated proliferation in human β-cells. Diabetes 2015; 64(11): 3784-97.
[http://dx.doi.org/10.2337/db15-0083] [PMID: 26159175]
[29]
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.
[http://dx.doi.org/10.1186/1471-2164-15-620] [PMID: 25051960]
[30]
Abouna S, Old RW, Pelengaris S, et al. Non-β-cell progenitors of β-cells in pregnant mice. Organogenesis 2010; 6(2): 125-33.
[http://dx.doi.org/10.4161/org.6.2.10374] [PMID: 20885859]
[31]
Xiao X, Chen Z, Shiota C, et al. No evidence for β cell neogenesis in murine adult pancreas. J Clin Invest 2013; 123(5): 2207-17.
[http://dx.doi.org/10.1172/JCI66323] [PMID: 23619362]
[32]
Toselli C, Hyslop CM, Hughes M, Natale DR, Santamaria P, Huang CTL. Contribution of a non-β-cell source to β-cell mass during pregnancy. PLoS One 2014; 9(6)e100398
[http://dx.doi.org/10.1371/journal.pone.0100398] [PMID: 24940737]
[33]
Zhao X. Increase of beta cell mass by beta cell replication, but not neogenesis, in the maternal pancreas in mice. Endocr J 2014; 61(6): 623-8.
[http://dx.doi.org/10.1507/endocrj.EJ14-0040] [PMID: 24748457]
[34]
Hakonen E, Ustinov J, Palgi J, Miettinen PJ, Otonkoski T. EGFR signaling promotes β-cell proliferation and survivin expression during pregnancy. PLoS One 2014; 9(4)e93651
[http://dx.doi.org/10.1371/journal.pone.0093651] [PMID: 24695557]
[35]
Seaberg RM, Smukler SR, Kieffer TJ, et al. Clonal identification of multipotent precursors from adult mouse pancreas that generate neural and pancreatic lineages. Nat Biotechnol 2004; 22(9): 1115-24.
[http://dx.doi.org/10.1038/nbt1004] [PMID: 15322557]
[36]
Smukler SR, Arntfield ME, Razavi R, et al. The adult mouse and human pancreas contain rare multipotent stem cells that express insulin. Cell Stem Cell 2011; 8(3): 281-93.
[http://dx.doi.org/10.1016/j.stem.2011.01.015] [PMID: 21362568]
[37]
Beamish CA, Strutt BJ, Arany EJ, Hill DJ. Insulin-positive, Glut2-low cells present within mouse pancreas exhibit lineage plasticity and are enriched within extra-islet endocrine cell clusters. Islets 2016; 8(3): 65-82.
[http://dx.doi.org/10.1080/19382014.2016.1162367] [PMID: 27010375]
[38]
Artner I, Hang Y, Mazur M, et al. MafA and MafB regulate genes critical to beta-cells in a unique temporal manner. Diabetes 2010; 59(10): 2530-9.
[http://dx.doi.org/10.2337/db10-0190] [PMID: 20627934]
[39]
Thorel F, Népote V, Avril I, et al. Conversion of adult pancreatic alpha-cells to beta-cells after extreme beta-cell loss. Nature 2010; 464(7292): 1149-54.
[http://dx.doi.org/10.1038/nature08894] [PMID: 20364121]
[40]
Ye L, Robertson MA, Hesselson D, Stainier DYR, Anderson RM. Glucagon is essential for alpha cell transdifferentiation and beta cell neogenesis. Development 2015; 142(8): 1407-17.
[http://dx.doi.org/10.1242/dev.117911] [PMID: 25852199]
[41]
White MG, Marshall HL, Rigby R, et al. Expression of mesenchymal and α-cell phenotypic markers in islet β-cells in recently diagnosed diabetes. Diabetes Care 2013; 36(11): 3818-20.
[http://dx.doi.org/10.2337/dc13-0705] [PMID: 24062329]
[42]
Quesada-Candela C, Tudurí E, Marroquí L, Alonso-Magdalena P, Quesada I, Nadal Á. Morphological and functional adaptations of pancreatic alpha-cells during late pregnancy in the mouse. Metabolism 2020; 102153963
[http://dx.doi.org/10.1016/j.metabol.2019.153963] [PMID: 31593706]
[43]
Banerjee RR, Cyphert HA, Walker EM, et al. Gestational diabetes mellitus from inactivation of prolactin receptor and MafB in islet β-cells. Diabetes 2016; 65(8): 2331-41.
[http://dx.doi.org/10.2337/db15-1527] [PMID: 27217483]
[44]
Radhakrishnan A, Raju R, Tuladhar N, et al. A pathway map of prolactin signaling. J Cell Commun Signal 2012; 6(3): 169-73.
[http://dx.doi.org/10.1007/s12079-012-0168-0] [PMID: 22684822]
[45]
Brelje TC, Stout LE, Bhagroo NV, Sorenson RL. Distinctive roles for prolactin and growth hormone in the activation of signal transducer and activator of transcription 5 in pancreatic islets of langerhans. Endocrinology 2004; 145(9): 4162-75.
[http://dx.doi.org/10.1210/en.2004-0201] [PMID: 15142985]
[46]
Amaral MEC, Cunha DA, Anhê GF, et al. 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 2004; 183(3): 469-76.
[http://dx.doi.org/10.1677/joe.1.05547] [PMID: 15590973]
[47]
Amaral MEC, Ueno M, Carvalheira JB, et al. Prolactin-signal transduction in neonatal rat pancreatic islets and interaction with the insulin-signaling pathway. Horm Metab Res 2003; 35(5): 282-9.
[http://dx.doi.org/10.1055/s-2003-41303] [PMID: 12915997]
[48]
Bishop JD, Nien WL, Dauphinee SM, Too CKL. Prolactin activates mammalian target-of-rapamycin through phosphatidylinositol 3-kinase and stimulates phosphorylation of p70S6K and 4E-binding protein-1 in lymphoma cells. J Endocrinol 2006; 190(2): 307-12.
[http://dx.doi.org/10.1677/joe.1.06368] [PMID: 16899564]
[49]
Ohara-Imaizumi M, Kim H, Yoshida M, et al. Serotonin regulates glucose-stimulated insulin secretion from pancreatic β cells during pregnancy. Proc Natl Acad Sci USA 2013; 110(48): 19420-5.
[http://dx.doi.org/10.1073/pnas.1310953110] [PMID: 24218571]
[50]
Hughes E, Huang C. Participation of Akt, menin, and p21 in pregnancy-induced β-cell proliferation. Endocrinology 2011; 152(3): 847-55.
[http://dx.doi.org/10.1210/en.2010-1250] [PMID: 21239436]
[51]
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(5851): 806-9.
[http://dx.doi.org/10.1126/science.1146812] [PMID: 17975067]
[52]
Balcazar N, Sathyamurthy A, Elghazi L, et al. mTORC1 activation regulates β-cell mass and proliferation by modulation of cyclin D2 synthesis and stability. J Biol Chem 2009; 284(12): 7832-42.
[http://dx.doi.org/10.1074/jbc.M807458200] [PMID: 19144649]
[53]
Zahr E, Molano RD, Pileggi A, et al. Rapamycin impairs in vivo proliferation of islet beta-cells. Transplantation 2007; 84(12): 1576-83.
[http://dx.doi.org/10.1097/01.tp.0000296035.48728.28] [PMID: 18165767]
[54]
Gupta RK, Gao N, Gorski RK, et al. Expansion of adult beta-cell mass in response to increased metabolic demand is dependent on HNF-4alpha. Genes Dev 2007; 21(7): 756-69.
[http://dx.doi.org/10.1101/gad.1535507] [PMID: 17403778]
[55]
Zhang H, Zhang J, Pope CF, et al. Gestational diabetes mellitus resulting from impaired beta-cell compensation in the absence of FoxM1, a novel downstream effector of placental lactogen. Diabetes 2010; 59(1): 143-52.
[http://dx.doi.org/10.2337/db09-0050] [PMID: 19833884]
[56]
Shih DQ, Stoffel M. Molecular etiologies of MODY and other early-onset forms of diabetes. Curr Diab Rep 2002; 2(2): 125-34.
[http://dx.doi.org/10.1007/s11892-002-0071-9] [PMID: 12643132]
[57]
Miura A, Yamagata K, Kakei M, et al. Hepatocyte nuclear factor-4alpha is essential for glucose-stimulated insulin secretion by pancreatic beta-cells. J Biol Chem 2006; 281(8): 5246-57.
[http://dx.doi.org/10.1074/jbc.M507496200] [PMID: 16377800]
[58]
Zhang H, Ackermann AM, Gusarova GA, et al. The FoxM1 transcription factor is required to maintain pancreatic β-cell mass. Mol Endocrinol 2006; 20(8): 1853-66.
[http://dx.doi.org/10.1210/me.2006-0056] [PMID: 16556734]
[59]
Pechhold S, Stouffer M, Walker G, et al. Transcriptional analysis of intracytoplasmically stained, FACS-purified cells by high-throughput, quantitative nuclease protection. Nat Biotechnol 2009; 27(11): 1038-42.
[http://dx.doi.org/10.1038/nbt.1579] [PMID: 19838197]
[60]
Hill DJ, Strutt B, Szlapinski S. Differential gene expression in beta cell progenitors compared with mature beta cells. Dia Med 2018; 35(Suppl. 1): A50.
[61]
Friedrichsen BN, Carlsson C, Møldrup A, et al. Expression, biosynthesis and release of preadipocyte factor-1/delta-like protein/fetal antigen-1 in pancreatic β-cells: possible physiological implications. J Endocrinol 2003; 176(2): 257-66.
[http://dx.doi.org/10.1677/joe.0.1760257] [PMID: 12553874]
[62]
Wang Y, Lee K, Moon YS, et al. Overexpression of Pref-1 in pancreatic islet β-cells in mice causes hyperinsulinemia with increased islet mass and insulin secretion. Biochem Biophys Res Commun 2015; 461(4): 630-5.
[http://dx.doi.org/10.1016/j.bbrc.2015.04.078] [PMID: 25918019]
[63]
Hou J, Wang L, Long H, et al. Hypoxia preconditioning promotes cardiac stem cell survival and cardiogenic differentiation in vitro involving activation of the HIF-1α/apelin/APJ axis. Stem Cell Res Ther 2017; 8(1): 215.
[http://dx.doi.org/10.1186/s13287-017-0673-4] [PMID: 28962638]
[64]
Pi J, Cheng Y, Sun H. The effect of apelin-13 on pancreatic islet beta cell mass and myocardial fatty acid and glucose metabolism of experimental type 2 diabetic rats. Peptides 2017; 114: 1-7.
[http://dx.doi.org/10.1016/j.peptides.2019.03.006] [PMID: 30954534]
[65]
Feng J, Zhao H, Du M, Wu X. The effect of apelin-13 on pancreatic islet beta cell mass and myocardial fatty acid and glucose metabolism of experimental type 2 diabetic rats. Peptides 2019; 114: 1-7.
[http://dx.doi.org/10.1016/j.peptides.2019.03.006] [PMID: 30954534]
[66]
Han S, Englander EW, Gomez GA, et al. Pancreatic islet APJ deletion reduces islet density and glucose tolerance in mice. Endocrinology 2015; 156(7): 2451-60.
[http://dx.doi.org/10.1210/en.2014-1631] [PMID: 25965959]
[67]
Azimi H, Szlapinski S, Hill DJ. Mice fed a low protein diet in utero Show decreased apelin receptor presence in Ins+Glut2Lo cells during pregnancy associated with lower ß-cell mass In: 79th American Diabetes Association, San Francisco, CA, USA In: 2019; p. 2154-P.
[68]
Ben-Othman N, Vieira A, Courtney M, et al. Long-term gaba administration induces alpha cell-mediated beta-like cell neogenesis. Cell 2017; 168(1-2): 73-85.
[http://dx.doi.org/10.1016/j.cell.2016.11.002] [PMID: 27916274]
[69]
Soltani N, Qiu H, Aleksic M, et al. GABA exerts protective and regenerative effects on islet beta cells and reverses diabetes. Proc Natl Acad Sci USA 2011; 108(28): 11692-7.
[http://dx.doi.org/10.1073/pnas.1102715108] [PMID: 21709230]
[70]
Caicedo A. Paracrine and autocrine interactions in the human islet: more than meets the eye. Semin Cell Dev Biol 2013; 24(1): 11-21.
[http://dx.doi.org/10.1016/j.semcdb.2012.09.007] [PMID: 23022232]
[71]
Sorenson RL, Garry DG, Brelje TC. Structural and functional considerations of GABA in islets of Langerhans. Beta-cells and nerves. Diabetes 1991; 40(11): 1365-74.
[http://dx.doi.org/10.2337/diab.40.11.1365] [PMID: 1936599]
[72]
Braun M, Wendt A, Buschard K, et al. GABAB receptor activation inhibits exocytosis in rat pancreatic beta-cells by G-protein-dependent activation of calcineurin. J Physiol 2004; 559(Pt 2): 397-409.
[http://dx.doi.org/10.1113/jphysiol.2004.066563] [PMID: 15235087]
[73]
Brice NL, Varadi A, Ashcroft SJ, Molnar E. Metabotropic glutamate and GABA(B) receptors contribute to the modulation of glucose-stimulated insulin secretion in pancreatic beta cells. Diabetologia 2002; 45(2): 242-52.
[http://dx.doi.org/10.1007/s00125-001-0750-0] [PMID: 11935156]
[74]
Gammelsaeter R, Frøyland M, Aragón C, et al. Glycine, GABA and their transporters in pancreatic islets of Langerhans: evidence for a paracrine transmitter interplay. J Cell Sci 2004; 117(Pt 17): 3749-58.
[http://dx.doi.org/10.1242/jcs.01209] [PMID: 15252115]
[75]
Wang Z, Purwana I, Zhao F, et al. β-cell proliferation is associated with increased A-type γ-aminobutyric acid receptor expression in pancreatectomized mice. Pancreas 2013; 42(3): 545-8.
[http://dx.doi.org/10.1097/MPA.0b013e318267c598] [PMID: 23486367]
[76]
Korol SV, Jin Z, Jin Y, et al. Functional characterization of native, high-affinity GABAA receptors in human pancreatic β cells. EBioMedicine 2018; 30: 273-82.
[http://dx.doi.org/10.1016/j.ebiom.2018.03.014] [PMID: 29606630]
[77]
Tian J, Dang H, Chen Z, et al. γ-Aminobutyric acid regulates both the survival and replication of human β-cells. Diabetes 2013; 62(11): 3760-5.
[http://dx.doi.org/10.2337/db13-0931] [PMID: 23995958]
[78]
Kilimnik G, Kim A, Steiner DF, Friedman TC, Hara M. Intraislet production of GLP-1 by activation of prohormone convertase 1/3 in pancreatic α-cells in mouse models of ß-cell regeneration. Islets 2010; 2(3): 149-55.
[http://dx.doi.org/10.4161/isl.2.3.11396] [PMID: 20657753]
[79]
Thyssen S, Arany E, Hill DJ. Ontogeny of regeneration of beta-cells in the neonatal rat after treatment with streptozotocin. Endocrinology 2006; 147(5): 2346-56.
[http://dx.doi.org/10.1210/en.2005-0396] [PMID: 16484329]
[80]
Moffett RC, Vasu S, Thorens B, Drucker DJ, Flatt PR. Incretin receptor null mice reveal key role of GLP-1 but not GIP in pancreatic beta cell adaptation to pregnancy. PLoS One 2014; 9(6)e96863
[http://dx.doi.org/10.1371/journal.pone.0096863] [PMID: 24927416]
[81]
Wang C, Mao R, Van de Casteele M, Pipeleers D, Ling Z. Glucagon-like peptide-1 stimulates GABA formation by pancreatic beta-cells at the level of glutamate decarboxylase. Am J Physiol Endocrinol Metab 2007; 292(4): E1201-6.
[http://dx.doi.org/10.1152/ajpendo.00459.2006] [PMID: 17190904]
[82]
Liang XD, Guo YY, Sun M, et al. Streptozotocin-induced expression of Ngn3 and Pax4 in neonatal rat pancreatic α-cells. World J Gastroenterol 2011; 17(23): 2812-20.
[http://dx.doi.org/10.3748/wjg.v17.i23.2812] [PMID: 21734788]
[83]
Hauge-Evans AC, Richardson CC, Milne HM, Christie MR, Persaud SJ, Jones PM. A role for kisspeptin in islet function. Diabetologia 2006; 49(9): 2131-5.
[http://dx.doi.org/10.1007/s00125-006-0343-z] [PMID: 16826407]
[84]
Bowe JE, King AJ, Kinsey-Jones JS, et al. Kisspeptin stimulation of insulin secretion: mechanisms of action in mouse islets and rats. Diabetologia 2009; 52(5): 855-62.
[http://dx.doi.org/10.1007/s00125-009-1283-1] [PMID: 19221709]
[85]
Bowe JE, Foot VL, Amiel SA, et al. GPR54 peptide agonists stimulate insulin secretion from murine, porcine and human islets. Islets 2012; 4(1): 20-3.
[http://dx.doi.org/10.4161/isl.18261] [PMID: 22192948]
[86]
Van Mieghem T, Doherty A, Baczyk D, et al. Apelin in normal pregnancy and pregnancies complicated by placental insufficiency. Reprod Sci 2016; 23(8): 1037-43.
[http://dx.doi.org/10.1177/1933719116630422] [PMID: 26880769]
[87]
Van Mieghem T, van Bree R, Van Herck E, Pijnenborg R, Deprest J, Verhaeghe J. Maternal apelin physiology during rat pregnancy: the role of the placenta. Placenta 2010; 31(8): 725-30.
[http://dx.doi.org/10.1016/j.placenta.2010.06.001] [PMID: 20580085]
[88]
Mayeur S, Wattez JS, Lukaszewski MA, et al. Apelin controls fetal and neonatal glucose homeostasis and is altered by maternal undernutrition. Diabetes 2016; 65(3): 554-60.
[http://dx.doi.org/10.2337/db15-0228] [PMID: 26631739]
[89]
Yamaleyeva LM, Chappell MC, Brosnihan KB, et al. Downregulation of apelin in the human placental chorionicvilli from preeclamptic pregnancies. Am J Physiol Endocrinol Metab 2015 309; 2015: E852-60.
[90]
Ho L, van Dijk M, Chye STJ, et al. ELABELA deficiency promotes preeclampsia and cardiovascular malformations in mice. Science 2017; 357(6352): 707-13.
[http://dx.doi.org/10.1126/science.aam6607] [PMID: 28663440]
[91]
Eberlé D, Marousez L, Hanssens S, et al. Elabela and Apelin actions in healthy and pathological pregnancies. Cytokine Growth Factor Rev 2019; 46: 45-53.
[http://dx.doi.org/10.1016/j.cytogfr.2019.03.003] [PMID: 30910349]
[92]
Vaughan OR, Powell TL, Jansson T. Apelin is a novel regulator of human trophoblast amino acid transport. Am J Physiol Endocrinol Metab 2019; 316(5): E810-6.
[http://dx.doi.org/10.1152/ajpendo.00012.2019] [PMID: 30835509]
[93]
Kotani M, Detheux M, Vandenbogaerde A, et al. The metastasis suppressor gene KiSS-1 encodes kisspeptins, the natural ligands of the orphan G protein-coupled receptor GPR54. J Biol Chem 2001; 276(37): 34631-6.
[http://dx.doi.org/10.1074/jbc.M104847200] [PMID: 11457843]
[94]
Hiden U, Bilban M, Knöfler M, Desoye G. Kisspeptins and the placenta: regulation of trophoblast invasion. Rev Endocr Metab Disord 2007; 8(1): 31-9.
[http://dx.doi.org/10.1007/s11154-007-9030-8] [PMID: 17351756]
[95]
Smets E, Deurloo KL, Go AT, van Vugt JM, Blankenstein MA, Oudejans CB. Oudejans, Decreased plasma levels of metastin in early pregnancy are associated with small for gestational age neonates. Prenat Diagn 2008; 28: 299-303.
[96]
Cetković A, Miljic D, Ljubić A, et al. Plasma kisspeptin levels in pregnancies with diabetes and hypertensive disease as a potential marker of placental dysfunction and adverse perinatal outcome. Endocr Res 2012; 37(2): 78-88.
[http://dx.doi.org/10.3109/07435800.2011.639319] [PMID: 22489921]
[97]
Horikoshi Y, Matsumoto H, Takatsu Y, et al. Dramatic elevation of plasma metastin concentrations in human pregnancy: metastin as a novel placenta-derived hormone in humans. J Clin Endocrinol Metab 2003; 88(2): 914-9.
[http://dx.doi.org/10.1210/jc.2002-021235] [PMID: 12574233]
[98]
Bowe JE, Hill TG, Hunt KF, et al. A role for placental kisspeptin in β cell adaptation to pregnancy. JCI Insight 2019; 4124540
[http://dx.doi.org/10.1172/jci.insight.124540] [PMID: 31619585]
[99]
Pantham P, Aye IL, Powell TL. Inflammation in maternal obesity and gestational diabetes mellitus. Placenta 2015; 36: 709-15.
[http://dx.doi.org/10.1016/j.placenta.2015.04.006] [PMID: 25972077]
[100]
Kupferminc MJ, Peaceman AM, Wigton TR, Rehnberg KA, Socol ML. Tumor necrosis factor-alpha is elevated in plasma and amniotic fluid of patients with severe preeclampsia. Am J Obstet Gynecol 1994; 170(6): 1752-7.
[http://dx.doi.org/10.1016/S0002-9378(94)70351-5] [PMID: 8203436]
[101]
Wedekind L, Belkacemi L. Altered cytokine network in gestational diabetes mellitus affects maternal insulin and placental-fetal development. J Diabetes Compl 2016; 30: 1393-400.
[PMID: 27230834]
[102]
Colli ML, Hill JLE, Marroquí L, et al. PDL1 is expressed in the islets of people with type 1 diabetes and is up-regulated by interferons-α and-γ via IRF1 induction. EBioMedicine 2018; 36: 367-75.
[http://dx.doi.org/10.1016/j.ebiom.2018.09.040] [PMID: 30269996]
[103]
Enninga EAL, Harrington SM, Creedon DJ, et al. Immune checkpoint molecules soluble program death ligand 1 and galectin-9 are increased in pregnancy. Am J Reprod Immunol 2018; 79(2)e12795
[http://dx.doi.org/10.1111/aji.12795] [PMID: 29205636]
[104]
Barbour LA, McCurdy CE, Hernandez TL, Kirwan JP, Catalano PM, Friedman JE. Cellular mechanisms for insulin resistance in normal pregnancy and gestational diabetes. Diabetes Care 2007; 30(Suppl. 2): S112-9.
[http://dx.doi.org/10.2337/dc07-s202] [PMID: 17596458]
[105]
Ferrara A. Increasing prevalence of gestational diabetes mellitus: a public health perspective. Diabetes Care 2007; 30(Suppl. 2): S141-6.
[http://dx.doi.org/10.2337/dc07-s206] [PMID: 17596462]
[106]
Nguyen CL, Pham NM, Binns CW, Duong DV, Lee AH. Prevalence of gestational diabetes mellitus in Eastern and Southeastern Asia: A systematic review and meta-analysis. J Diabetes Res 2018; 20186536974
[http://dx.doi.org/10.1155/2018/6536974] [PMID: 29675432]
[107]
Petra IL, Martín-Montalvo A, Cobo Vuilleumier N, Gauthier BR. Molecular modelling of islet β-cell adaptation to inflammation in pregnancy and gestational diabetes mellitus. Int J Mol Sci 2019; 20(24): 6171.
[http://dx.doi.org/10.3390/ijms20246171] [PMID: 31817798]
[108]
Heida KY, Franx A, van Rijn BB, et al. Earlier age of onset of chronic hypertension and type 2 diabetes mellitus after a hypertensive disorder of pregnancy or gestational diabetes mellitus. Hypertens 2015; 66: 1116-22.
[PMID: 26459420]
[109]
Melchior H, Kurch-Bek D, Mund M. The Prevalence of gestational diabetes. Dtsch Arztebl Int 2017; 114(24): 412-8.
[http://dx.doi.org/10.3238/arztebl.2017.0412] [PMID: 28669379]
[110]
Garcia-Vargas L, Addison SS, Nistala R, Kurukulasuriya D, Sowers JR. Gestational diabetes and the offspring: implications in the development of the cardiorenal metabolic syndrome in offspring. Cardiorenal Med 2012; 2(2): 134-42.
[http://dx.doi.org/10.1159/000337734] [PMID: 22851962]
[111]
Kim SY, Sharma AJ, Callaghan WM. Gestational diabetes and childhood obesity: what is the link? Curr Opin Obstet Gynecol 2012; 24(6): 376-81.
[http://dx.doi.org/10.1097/GCO.0b013e328359f0f4] [PMID: 23000698]
[112]
Mitanchez D, Yzydorczyk C, Simeoni U. What neonatal complications should the pediatrician be aware of in case of maternal gestational diabetes? World J Diabetes 2015; 6(5): 734-43.
[http://dx.doi.org/10.4239/wjd.v6.i5.734] [PMID: 26069722]
[113]
Buchanan TA, Xiang AH, Page KA. Gestational diabetes mellitus: risks and management during and after pregnancy. Nat Rev Endocrinol 2012; 8(11): 639-49.
[http://dx.doi.org/10.1038/nrendo.2012.96] [PMID: 22751341]
[114]
Al-Badri MR, Zantout MS, Azar ST. The role of adipokines in gestational diabetes mellitus. Ther Adv Endocrinol Metab 2015; 6(3): 103-8.
[http://dx.doi.org/10.1177/2042018815577039] [PMID: 26137214]
[115]
Plowden TC, Zarek SM, Rafique S, et al. Preconception leptin levels and pregnancy outcomes: A prospective cohort study. Obes Sci Pract 2020; Apr. 6(2): 181-88.
[PMID: 32313676]
[116]
Chen L, Chen R, Wang H, Liang F. Mechanisms linking inflammation to insulin resistance. Int J Endocrinol 2015; 2015508409
[http://dx.doi.org/10.1155/2015/508409] [PMID: 26136779]
[117]
Catalano PM. Trying to understand gestational diabetes. Diabet Med 2014; 31(3): 273-81.
[http://dx.doi.org/10.1111/dme.12381] [PMID: 24341419]
[118]
Yang Y, Liu L, Liu B, et al. Functional defects of regulatory T cell through interleukin 10 mediated mechanism in the induction of gestational diabetes mellitus. DNA Cell Biol 2018; 37(3): 278-85.
[http://dx.doi.org/10.1089/dna.2017.4005] [PMID: 29298097]
[119]
Vitoratos N, Valsamakis G, Mastorakos G, et al. Pre- and early post-partum adiponectin and interleukin-1beta levels in women with and without gestational diabetes. Hormones (Athens) 2008; 7(3): 230-6.
[http://dx.doi.org/10.14310/horm.2002.1202] [PMID: 18694861]
[120]
Nordmann TM, Dror E, Schulze F, et al. The role of inflammation in β-cell dedifferentiation. Sci Rep 2017; 7(1): 6285.
[http://dx.doi.org/10.1038/s41598-017-06731-w] [PMID: 28740254]
[121]
Tessier DR, Ferraro ZM, Gruslin A. Role of leptin in pregnancy: consequences of maternal obesity. Placenta 2013; 34(3): 205-11.
[http://dx.doi.org/10.1016/j.placenta.2012.11.035] [PMID: 23332215]
[122]
Wang L, Liu Y, Yan Lu S, et al. Deletion of Pten in pancreatic ß-cells protects against deficient ß-cell mass and function in mouse models of type 2 diabetes. Diabetes 2010; 59(12): 3117-26.
[http://dx.doi.org/10.2337/db09-1805] [PMID: 20852026]
[123]
Ye R, Wang M, Wang QA, Scherer PE. Adiponectin-mediated antilipotoxic effects in regenerating pancreatic islets. Endocrinology 2015; 156(6): 2019-28.
[http://dx.doi.org/10.1210/en.2015-1066] [PMID: 25815422]
[124]
Qiao L, Wattez J-S, Lee S, et al. Adiponectin deficiency impairs maternal metabolic adaptation to pregnancy in mice. Diabetes 2017; 66(5): 1126-35.
[http://dx.doi.org/10.2337/db16-1096] [PMID: 28073830]
[125]
Retnakaran R. Adiponectin and β-cell adaptation in pregnancy. Diabetes 2017; 66(5): 1121-2.
[http://dx.doi.org/10.2337/dbi17-0001] [PMID: 28507212]
[126]
Retnakaran R, Hanley AJG, Raif N, et al. Adiponectin and beta cell dysfunction in gestational diabetes: pathophysiological implications. Diabetologia 2005; 48(5): 993-1001.
[http://dx.doi.org/10.1007/s00125-005-1710-x] [PMID: 15778860]
[127]
Tang C, Han P, Oprescu AI, et al. Evidence for a role of superoxide generation in glucose-induced beta-cell dysfunction in vivo. Diabetes 2007; 56(11): 2722-31.
[http://dx.doi.org/10.2337/db07-0279] [PMID: 17682092]
[128]
Herrera Martínez A, Palomares Ortega R, Bahamondes Opazo R, Moreno-Moreno P, Molina Puerta MJ, Gálvez-Moreno MA. Hyperlipidemia during gestational diabetes and its relation with maternal and offspring complications. Nutr Hosp 2018; 35(3): 698-706.
[http://dx.doi.org/10.20960/nh.1539] [PMID: 29974782]
[129]
Sharma RB, Alonso LC. Lipotoxicity in the pancreatic beta cell: not just survival and function, but proliferation as well? Curr Diab Rep 2014; 14(6): 492.
[http://dx.doi.org/10.1007/s11892-014-0492-2] [PMID: 24740729]

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