Hypoglycemia, hyperglucagonemia, and fetoplacental defects in glucagon receptor knockout mice: A role for glucagon action in pregnancy maintenance

American Journal of Physiology - Endocrinology and Metabolism

Volumn 302, Issue 5, 2012, Pages

  Ouhilal, Sophia ^a,e   Vuguin, Patricia ^a   Cui, Lingguang ^a   Du, Xiu Quan ^a   Gelling, Richard W ^a,c   Reznik, Sandra E ^b   Russell, Robert ^b,f   Parlow, Albert F ^d   Karpovsky, Clara ^g   Santoro, Nanette ^a,h   Charron, Maureen J ^a  

^a Department of Obstetrics and Gynecology ^*  (United States)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^c ABBOTT LABORATORIES   (United States)

^d HARBOR UCLA MEDICAL CENTER   (United States)

^e Montreal Fertility Centre   (Canada)

^f GEORGETOWN UNIVERSITY   (United States)

^g DARTMOUTH MEDICAL SCHOOL   (United States)

^h UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

Fetal growth; Placenta

Indexed keywords

ADRENERGIC RECEPTOR; CHEMOKINE RECEPTOR; G PROTEIN COUPLED RECEPTOR; GLUCAGON RECEPTOR; HYPOXIA INDUCIBLE FACTOR 1ALPHA; INSULIN RECEPTOR; LEPTIN RECEPTOR; SOMATOMEDIN B; SOMATOMEDIN BINDING PROTEIN 1; SOMATOMEDIN C; SOMATOMEDIN C RECEPTOR; VASCULOTROPIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL HYPERPLASIA; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; FEMALE; FETUS WEIGHT; GENE EXPRESSION; GLUCOSE TRANSPORT; HYPERGLUCAGONEMIA; HYPOGLYCEMIA; HYPOTHALAMUS HYPOPHYSIS SYSTEM; INTRAUTERINE GROWTH RETARDATION; MINERALIZATION; MOUSE; NECROSIS; NONHUMAN; OOCYTE; OXIDATIVE STRESS; PLACENTA CIRCULATION; PLACENTA DISORDER; PREGNANCY; PRENATAL GROWTH; PRIORITY JOURNAL; REPRODUCTION; SIGNAL TRANSDUCTION; TROPHOBLAST;

ANIMALS; FEMALE; FETAL DEATH; FETAL DISEASES; FETAL GROWTH RETARDATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLUCAGON; HETEROZYGOTE; HYPOGLYCEMIA; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; OVARY; PITUITARY GLAND, ANTERIOR; PLACENTA; PLACENTA DISEASES; PLACENTATION; PREGNANCY; PREGNANCY PROTEINS; RECEPTORS, GLUCAGON; SIGNAL TRANSDUCTION; SUPEROVULATION;

EID: 84857280811     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00420.2011     Document Type: Article

References (81)

1. Adam PA, King KC, Schwartz R, Teramo K. Human placental barrier to 125-I-glucagon early in gestation. J Clin Endocrinol Metab 34: 772-782, 1972.
2. Akamine R, Yamamoto T, Watanabe M, Yamazaki N, Kataoka M, Ishikawa M, Ooie T, Baba Y, Shinohara Y. Usefulness of the 5' region of the cDNA encoding acidic ribosomal phosphoprotein P0 conserved among rats, mice, and humans as a standard probe for gene expression analysis in different tissues and animal species. J Biochem Biophys Methods 70: 481-486, 2007.
3. Alfaidy N, Li W, MacIntosh T, Yang K, Challis J. Late gestation increase in 11beta-hydroxysteroid dehydrogenase 1 expression in human fetal membranes: a novel intrauterine source of cortisol. J Clin Endocrinol Metab 88: 5033-5038, 2003.
4. Baisden B, Sonne S, Joshi RM, Ganapathy V, Shekhawat PS. Antenatal dexamethasone treatment leads to changes in gene expression in a murine late placenta. Placenta 28: 1082-1090, 2007.
5. Baloǧlu E, Ke A, Abu-Taha IH, Bärtsch P, Mairbäurl H. In vitro hypoxia impairs β2-adrenergic receptor signaling in primary rat alveolar epithelial cells. Am J Physiol Lung Cell Mol Physiol 296: L500-L509, 2009.
6. Bamberger AM, Bamberger CM, Aupers S, Milde-Langosch K, Löning T, Makrigiannakis A. Expression pattern of the activating protein-1 family of transcription factors in the human placenta. Mol Hum Reprod 10: 223-228, 2004.
7. Barash V, Gimmon Z, Shafrir E. Placental glycogen accumulation and maternal-fetal metabolic responses in hyperglycaemic non-diabetic rats. Diabetes Res 3: 97-101, 1986.
8. Barash V, Gutman A, Shafrir E. Mechanism of placental glycogen deposition in diabetes in the rat. Diabetologia 24: 63-68, 1983.
9. Barash V, Shafrir E. Mobilization of placental glycogen in diabetic rats. Placenta 11: 515-521, 1990.
10. Barth WH Jr, Genest DR, Riley LE, Frigoletto FD Jr, Benacerraf BR, Greene MF. Uterine arcuate artery Doppler and decidual microvascular pathology in pregnancies complicated by type I diabetes mellitus. Ultrasound Obstet Gynecol 8: 98-103, 1996.
11. Baumann MU, Deborde S, Illsley NP. Placental glucose transfer and fetal growth. Endocrine 19: 13-22, 2002.
12. Belkacemi L, Chen CH, Ross MG, Desai M. Increased placental apoptosis in maternal food restricted gestations: role of the Fas pathway. Placenta 30: 739-751, 2009.
13. Billiard J, Grewal SS, Lukaesko L, Stork PJ, Rotwein P. Hormonal control of insulin-like growth factor I gene transcription in human osteoblasts: dual actions of cAMP-dependent protein kinase on CCAAT/ enhancer-binding protein delta. J Biol Chem 276: 31238-31246, 2001.
14. Bowman CJ, Streck RD, Chapin RE. Maternal-placental insulin-like growth factor (IGF) signaling and its importance to normal embryo-fetal development. Birth Defects Res B Dev Reprod Toxicol 89: 339-349, 2010.
15. Brubaker PL, Drucker DJ. Structure-function of the glucagon receptor family of G protein-coupled receptors: the glucagon, GIP, GLP-1, and GLP-2 receptors. Receptors Channels 8: 179-188, 2002.
16. Brüning JC, Gautam D, Burks DJ, Gillette J, Schubert M, Orban PC, Klein R, Krone W, Müller-Wieland D, Kahn CR. Role of brain insulin receptor in control of body weight and reproduction. Science 289: 2122-2125, 2000.
17. Buggy J, Hull J, Yoo-Warren H. Isolation and structural analysis of the 5' flanking region of the gene encoding the human glucagon receptor. Biochem Biophys Res Commun 208: 339-344, 1995.
18. Clark DE, Charnock-Jones DS. Placental angiogenesis: the role of the VEGF family of proteins. Angiogenesis 2: 309-318, 1998.
19. Coan PM, Conroy N, Burton GJ, Ferguson-Smith AC. Origin and characteristics of glycogen cells in the developing murine placenta. Dev Dyn 235: 3280-3294, 2006.
20. Constancia M, Hemberger M, Hughes J, Dean W, Ferguson-Smith A, Fundele R, Stewart F, Kelsey G, Fowden A, Sibley C, Reik W. Placental-specific IGF-II is a major modulator of placental and fetal growth. Nature 417: 945-948, 2002.
21. Desforges M, Lacey HA, Glazier JD, Greenwood SL, Mynett KJ, Speake PF, Sibley CP. SNAT4 isoform of system A amino acid transporter is expressed in human placenta. Am J Physiol Cell Physiol 290: C305-C312, 2006.
22. Esquiliano DR, Guo W, Liang L, Dikkes P, Lopez MF. Placental glycogen stores are increased in mice with H19 null mutations but not in those with insulin or IGF type 1 receptor mutations. Placenta 30: 693-699, 2009.
23. Feng Z. p53 regulation of the IGF-1/AKT/mTOR pathways and the endosomal compartment. Cold Spring Harb Perspect Biol 2: a001057, 2010.
24. Fujii R, Morikawa H, Ueda Y, Mochizuki M. [Studies on the fetal and neonatal secretion of glucagon and the development of glucagon receptors]. Nippon Naibunpi Gakkai Zasshi 65: 1239-1252, 1989.
25. Gabbe SG, Demers LM, Greep RO, Villee CA. Placental glycogen metabolism in diabetes mellitus. Diabetes 21: 1185-1191, 1972.
26. Gelling RW, Du XQ, Dichmann DS, Romer J, Huang H, Cui L, Obici S, Tang B, Holst JJ, Fledelius C, Johansen PB, Rossetti L, Jelicks LA, Serup P, Nishimura E, Charron MJ. Lower blood glucose, hyperglucagonemia, and pancreatic alpha cell hyperplasia in glucagon receptor knockout mice. Proc Natl Acad Sci USA 100: 1438-1443, 2003.
27. Gheorghe CP, Goyal R, Holweger JD, Longo LD. Placental gene expression responses to maternal protein restriction in the mouse. Placenta 30: 411-417, 2009.
28. Gheorghe CP, Goyal R, Mittal A, Longo LD. Gene expression in the placenta: maternal stress and epigenetic responses. Int J Dev Biol 54: 507-523, 2010.
29. Gheorghe CP, Mohan S, Oberg KC, Longo LD. Gene expression patterns in the hypoxic murine placenta: a role in epigenesis? Reprod Sci 14: 223-233, 2007.
30. Gill RD, Hart IC. Hepatic receptors for insulin and glucagon in relation to plasma hormones and metabolites in pregnant and unmated ewes. J Endocrinol 93: 231-238, 1982.
31. Goltzsch W, Bittner R, Böhme HJ, Hofmann E. Effect of prenatal insulin and glucagon injection on the glycogen content of rat placenta and fetal liver. Biomed Biochim Acta 46: 619-622, 1987.
32. Hadcock JR, Malbon CC. Down-regulation of beta-adrenergic receptors: agonist-induced reduction in receptor mRNA levels. Proc Natl Acad Sci USA 85: 5021-5025, 1988.
33. Hartil K, Vuguin PM, Kruse M, Schmuel E, Fiallo A, Vargas C, Warner MJ, Durand JL, Jelicks LA, Charron MJ. Maternal substrate utilization programs the development of the metabolic syndrome in male mice exposed to high fat in utero. Pediatr Res 66: 368-373, 2009.
34. Hauguel-de Mouzon S, Shafrir E. Carbohydrate and fat metabolism and related hormonal regulation in normal and diabetic placenta. Placenta 22: 619-627, 2001.
35. Jansson T, Wennergren M, Illsley NP. Glucose transporter protein expression in human placenta throughout gestation and in intrauterine growth retardation. J Clin Endocrinol Metab 77: 1554-1562, 1993.
36. Jansson T, Ylven K, Wennergren M, Powell TL. Glucose transport and system A activity in syncytiotrophoblast microvillous and basal plasma membranes in intrauterine growth restriction. Placenta 23: 392-399, 2002.
37. Jewell UR, Kvietikova I, Scheid A, Bauer C, Wenger RH, Gassmann M. Induction of HIF-1alpha in response to hypoxia is instantaneous. FASEB J 15: 1312-1314, 2001.
38. Johansson S, Dencker L, Dantzer V. Immunohistochemical localization of retinoid binding proteins at the materno-fetal interface of the porcine epitheliochorial placenta. Biol Reprod 64: 60-68, 2001.
39. Jones HN, Powell TL, Jansson T. Regulation of placental nutrient transport-a review. Placenta 28: 763-774, 2007.
40. Kingdom J, Huppertz B, Seaward G, Kaufmann P. Development of the placental villous tree and its consequences for fetal growth. Eur J Obstet Gynecol Reprod Biol 92: 35-43, 2000.
41. Kitamura T, Kahn CR, Accili D. Insulin receptor knockout mice. Annu Rev Physiol 65: 313-332, 2003.
42. König S, Vest M, Stahl M. Interrelation of maternal and foetal glucose and free fatty acids. The role of insulin and glucagon. Eur J Pediatr 128: 187-195, 1978.
43. Ktorza A, Bihoreau MT, Nurjhan N, Picon L, Girard J. Insulin and glucagon during the perinatal period: secretion and metabolic effects on the liver. Biol Neonate 48: 204-220, 1985.
44. Lee MJ, Wang Z, Yee H, Ma Y, Swenson N, Yang L, Kadner SS, Baergen RN, Logan SK, Garabedian MJ, Guller S. Expression and regulation of glucocorticoid receptor in human placental villous fibroblasts. Endocrinology 146: 4619-4626, 2005.
45. Leonce J, Brockton N, Robinson S, Venkatesan S, Bannister P, Raman V, Murphy K, Parker K, Pavitt D, Teoh TG, Regan L, Burchell A, Steer P, Johnston DG. Glucose production in the human placenta. Placenta 27, Suppl A: S103-S108, 2006.
46. Limesand SW, Hay WW Jr. Adaptation of ovine fetal pancreatic insulin secretion to chronic hypoglycaemia and euglycaemic correction. J Physiol 547: 95-105, 2003.
47. Maltepe E, Bakardjiev AI, Fisher SJ. The placenta: transcriptional, epigenetic, and physiological integration during development. J Clin Invest 120: 1016-1025, 2010.
48. Metzger BE, Rodeck C, Freinkel N, Price J, Young M. Transplacental arteriovenous gradients for glucose, insulin, glucagon and placental lactogen during normoglycaemia in human pregnancy at term. Placenta 6: 347-354, 1985.
49. Mistry HD, Kurlak LO, Williams PJ, Ramsay MM, Symonds ME, Pipkin FB. Differential expression and distribution of placental glutathione peroxidases 1, 3 and 4 in normal and preeclamptic pregnancy. Placenta 31: 401-408, 2010.
50. Muthig V, Gilsbach R, Haubold M, Philipp M, Ivacevic T, Gessler M, Hein L. Upregulation of soluble vascular endothelial growth factor receptor 1 contributes to angiogenesis defects in the placenta of alpha 2Badrenoceptor deficient mice. Circ Res 101: 682-691, 2007.
51. Nandi A, Wang X, Accili D, Wolgemuth DJ. The effect of insulin signaling on female reproductive function independent of adiposity and hyperglycemia. Endocrinology 151: 1863-1871, 2010.
52. Nuche-Berenguer B, Portal-Núñez S, Moreno P, González N, Acitores A, López-Herradón A, Esbrit P, Valverde I, Villanueva-Peñacarrillo ML. Presence of a functional receptor for GLP-1 in osteoblastic cells, independent of the cAMP-linked GLP-1 receptor. J Cell Physiol 225: 585-592, 2010.
53. Nyström T, Gonon AT, Sjöholm A, Pernow J. Glucagon-like peptide-1 relaxes rat conduit arteries via an endothelium-independent mechanism. Regul Pept 125: 173-177, 2005.
54. Ohtsuka K, Hata M. Molecular chaperone function of mammalian Hsp70 and Hsp40-a review. Int J Hyperthermia 16: 231-245, 2000.
55. Parlow AF, Shome B. A highly immunoreactive peptide fragment of human luteinizing hormone alpha subunit, discerned with a new, "sequence- specific" radioimmunoassay. J Clin Endocrinol Metab 41: 195-198, 1975.
56. Parlow AF, Shome B. Specific, homologous radioimmunoassay (RIA) of highly purified subunits of human pituitary follicle stimulating hormone (hFSH). J Clin Endocrinol Metab 39: 195-198, 1974.
57. Perlman R, Halabi C, Bick T, Hochberg Z. The human placenta as a target tissue for glucagon. Biochem Biophys Res Commun 151: 1019-1024, 1988.
58. Philipp M, Brede ME, Hadamek K, Gessler M, Lohse MJ, Hein L. Placental alpha(2)-adrenoceptors control vascular development at the interface between mother and embryo. Nat Genet 31: 311-315, 2002.
59. Poggi SH, Bostrom KI, Demer LL, Skinner HC, Koos BJ. Placental calcification: a metastatic process? Placenta 22: 591-596, 2001.
60. Radaelli T, Varastehpour A, Catalano P, Hauguel-de Mouzon S. Gestational diabetes induces placental genes for chronic stress and inflammatory pathways. Diabetes 52: 2951-2958, 2003.
61. Ranalletta M, Jiang H, Li J, Tsao TS, Stenbit AE, Yokoyama M, Katz EB, Charron MJ. Altered hepatic and muscle substrate utilization provoked by GLUT4 ablation. Diabetes 54: 935-943, 2005.
62. Resch BE, Ducza E, Gaspar R, Falkay G. Role of adrenergic receptor subtypes in the control of human placental blood vessels. Mol Reprod Dev 66: 166-171, 2003.
63. Roland-Zejly L, Moisan V, St-Pierre I, Bilodeau JF. Altered placental glutathione peroxidase mRNA expression in preeclampsia according to the presence or absence of labor. Placenta 32: 161-167, 2011.
64. Roos S, Lagerlöf O, Wennergren M, Powell TL, Jansson T. Regulation of amino acid transporters by glucose and growth factors in cultured primary human trophoblast cells is mediated by mTOR signaling. Am J Physiol Cell Physiol 297: C723-C731, 2009.
65. Roth M, Zhong J, Tamm M, Szilard J. Mesothelioma cells escape heat stress by upregulating Hsp40/Hsp70 expression via mitogen-activated protein kinases. J Biomed Biotechnol 2009: 451084, 2009.
66. Rouget C, Barthez O, Goirand F, Leroy MJ, Breuiller-Fouché M, Rakotoniaina Z, Guérard P, Morcillo EJ, Advenier C, Sagot P, Cabrol D, Dumas M, Bardou M. Stimulation of the ADRB3 adrenergic receptor induces relaxation of human placental arteries: influence of preeclampsia. Biol Reprod 74: 209-216, 2006.
67. Seckl JR, Meaney MJ. Glucocorticoid "programming" and PTSD risk. Ann NY Acad Sci 1071: 351-378, 2006.
68. Shafrir E, Barash V. Placental glycogen metabolism in diabetic pregnancy. Isr J Med Sci 27: 449-461, 1991.
69. Sitras V, Paulssen RH, Grønaas H, Vårtun A, Acharya G. Gene expression profile in labouring and non-labouring human placenta near term. Mol Hum Reprod 14: 61-65, 2008.
70. Snavely MD, Ziegler MG, Insel PA. Subtype-selective down-regulation of rat renal cortical alpha- and beta-adrenergic receptors by catecholamines. Endocrinology 117: 2182-2189, 1985.
71. Sood R, Zehnder JL, Druzin ML, Brown PO. Gene expression patterns in human placenta. Proc Natl Acad Sci USA 103: 5478-5483, 2006.
72. Spencer TE, Bazer FW. Uterine and placental factors regulating conceptus growth in domestic animals. J Anim Sci 82, E-Suppl: E4-E13, 2004.
73. Susztak K, Bottinger E, Novetsky A, Liang D, Zhu Y, Ciccone E, Wu D, Dunn S, McCue P, Sharma K. Molecular profiling of diabetic mouse kidney reveals novel genes linked to glomerular disease. Diabetes 53: 784-794, 2004.
74. Tachibana K, Hirota S, Iizasa H, Yoshida H, Kawabata K, Kataoka Y, Kitamura Y, Matsushima K, Yoshida N, Nishikawa S, Kishimoto T, Nagasawa T. The chemokine receptor CXCR4 is essential for vascularization of the gastrointestinal tract. Nature 393: 591-594, 1998.
75. Toft JH, Lian IA, Tarca AL, Erez O, Espinoza J, Eide IP, Bjørge L, Draghici S, Romero R, Austgulen R. Whole-genome microarray and targeted analysis of angiogenesis-regulating gene expression (ENG, FLT1, VEGF, PlGF) in placentas from pre-eclamptic and small-for-gestationalage pregnancies. J Matern Fetal Neonatal Med 21: 267-273, 2008.
76. Toth B, Fischl A, Scholz C, Kuhn C, Friese K, Karamouti M, Makrigiannakis A, Jeschke U. Insulin and leptin receptors as possible new candidates for endocrine control in normal and disturbed human pregnancy. Mol Hum Reprod 15: 231-239, 2009.
77. Tsao TS, Burcelin R, Katz EB, Huang L, Charron MJ. Enhanced insulin action due to targeted GLUT4 overexpression exclusively in muscle. Diabetes 45: 28-36, 1996.
78. Uchida T, Rossignol F, Matthay MA, Mounier R, Couette S, Clottes E, Clerici C. Prolonged hypoxia differentially regulates hypoxia-inducible factor (HIF)-1alpha and HIF-2alpha expression in lung epithelial cells: implication of natural antisense HIF-1alpha. J Biol Chem 279: 14871-14878, 2004.
79. Vuguin PM, Kedees MH, Cui L, Guz Y, Gelling RW, Nejathaim M, Charron MJ, Teitelman G. Ablation of the glucagon receptor gene increases fetal lethality and produces alterations in islet development and maturation. Endocrinology 147: 3995-4006, 2006.
80. Wenger RH, Rolfs A, Spielmann P, Zimmermann DR, Gassmann M. Mouse hypoxia-inducible factor-1alpha is encoded by two different mRNA isoforms: expression from a tissue-specific and a housekeepingtype promoter. Blood 91: 3471-3480, 1998.
81. Yang J, MacDougall ML, McDowell MT, Xi L, Wei R, Zavadoski WJ, Molloy MP, Baker JD, Kuhn M, Cabrera O, Treadway JL. Polyomic profiling reveals significant hepatic metabolic alterations in glucagonreceptor (GCGR) knockout mice: implications on anti-glucagon therapies for diabetes. BMC Genomics 12: 281, 2011.