Maternal diabetes leads to unphysiological high lipid accumulation in rabbit preimplantation embryos

Endocrinology

Volumn 155, Issue 4, 2014, Pages 1498-1509

  Schindler, Maria ^a   Pendzialek, Mareike ^a   Santos, Alexander Navarrete ^a   Plos̈ch, Torsten ^b   Seyring, Stefanie ^a   Gur̈ke, Jacqueline ^a   Haucke, Elisa ^a   Knelangen, Julia Miriam ^a   Fischer, Bernd ^a   Santos, Anne Navarrete ^a  

^a MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^b UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPOPHILIN; FATTY ACID BINDING PROTEIN 4; FATTY ACID SYNTHASE; FATTY ACID TRANSPORTER 4; GLUCOSE; LIPID; PERILIPIN; TRIACYLGLYCEROL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLASTOCYST; CONTROLLED STUDY; EMBRYO; FEMALE; GLUCOSE BLOOD LEVEL; HYPERGLYCEMIA; IN VITRO STUDY; IN VIVO STUDY; INSULIN DEPENDENT DIABETES MELLITUS; LIPID STORAGE; MATERNAL BLOOD; MATERNAL DIABETES MELLITUS; NONHUMAN; PREIMPLANTATION EMBRYO; PRIORITY JOURNAL; PROTEIN EXPRESSION; RABBIT; TRIACYLGLYCEROL BLOOD LEVEL;

ALLOXAN; ANIMALS; BLASTOCYST; BLOOD GLUCOSE; DIABETES MELLITUS, TYPE 1; DISEASE MODELS, ANIMAL; FATTY ACID TRANSPORT PROTEINS; FATTY ACID-BINDING PROTEINS; FATTY ACIDS; FEMALE; LIPIDS; PREGNANCY; PREGNANCY COMPLICATIONS; PREGNANCY IN DIABETICS; PREGNANCY, ANIMAL; RABBITS; RNA, COMPLEMENTARY; TRIGLYCERIDES;

EID: 84897901771     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2013-1760     Document Type: Article

References (94)

1. Anna V, van der Ploeg HP, Cheung NW, Huxley RR, Bauman AE. Sociodemographic correlates of the increasing trend in prevalence of gestational diabetes mellitus in a large population of women between 1995 and 2005. Diabetes Care. 2008;31:2288-2293.
2. O'Brien T, Nguyen TT, Zimmerman BR. Hyperlipidemia and diabetes mellitus. Mayo Clin Proc. 1998;73:969-976. (Pubitemid 28467699)
3. Tsujii H, Yahia Khandoker MAM, Hamano K. Lipid in mammalian embryo development. J Mamm Ova Res. 2001;18:73-80.
4. Stubbs CD, Smith AD. The modification of mammalian membrane polyunsaturated fatty acid composition in relation to membrane fluidity and function. Biochim Biophys Acta. 1984;779:89-137. (Pubitemid 14199577)
5. Kikuchi K, Ekwall H, Tienthai P, et al. Morphological features of lipid droplet transition during porcine oocyte fertilisation and early embryonic development to blastocyst in vivo and in vitro. Zygote. 2002;10:355-366. (Pubitemid 135714205)
6. Abe H, Yamashita S, Itoh T, Satoh T, Hoshi H. Ultrastructure of bovine embryos developed from in vitro-matured and -fertilized oocytes: comparative morphological evaluation of embryos cultured either in serum-free medium or in serum-supplemented medium. Mol Reprod Dev. 1999;53:325-335. (Pubitemid 29247332)
7. Hoshi H. In vitro production of bovine embryos and their application for embryo transfer. Theriogenology. 2003;59:675-685. (Pubitemid 36093447)
8. Reis A, McCallum GJ, McEvoy TG. Accumulation and distribution of neutral lipid droplets is non-uniform in ovine blastocysts produced in vitro in either the presence or absence of serum. Reprod Fertil Dev. 2005;17:815-823. (Pubitemid 41790230)
9. Dobrinsky J, Nagashima H, Pursel V, Long C, Johnson L. Cryopreservation of swine embryos with reduced lipid content. Theriogenology. 1999;51:164.
10. Nagano M, Katagiri S, Takahashi Y. Relationship between bovine oocyte morphology and in vitro developmental potential. Zygote. 2006;14:53-61.
11. Jeong WJ, Cho SJ, Lee HS, et al. Effect of cytoplasmic lipid content on in vitro developmental efficiency of bovine IVP embryos. Theriogenology. 2009;72:584-589.
12. McEvoy TG, Coull GD, Broadbent PJ, Hutchinson JS, Speake BK. Fatty acid composition of lipids in immature cattle, pig and sheep oocytes with intact zona pellucida. J Reprod Fertil. 2000;118:163-170. (Pubitemid 30081641)
13. Ma W, Yang X, Liang X. Obesity does not aggravate vitrification injury in mouse embryos: a prospective study. Reprod Biol Endocrinol. 2012;10:68.
14. Heid HW, Moll R, Schwetlick I, Rackwitz HR, Keenan TW. Adipophilin is a specific marker of lipid accumulation in diverse cell types and diseases. Cell Tissue Res. 1998;294:309-321. (Pubitemid 28486407)
15. Miura S, Gan JW, Brzostowski J, et al. Functional conservation for lipid storage droplet association among Perilipin, ADRP, and TIP47 (PAT)-related proteins in mammals, Drosophila, and Dictyostelium. J Biol Chem. 2002;277:32253-32257. (Pubitemid 34969041)
16. Brasaemle DL. Thematic review series: adipocyte biology. The perilipin family of structural lipid droplet proteins: stabilization of lipid droplets and control of lipolysis. J Lipid Res. 2007;48:2547-2559. (Pubitemid 350272839)
17. Picone O, Laigre P, Fortun-Lamothe L, et al. Hyperlipidic hypercholesterolemic diet in prepubertal rabbits affects gene expression in the embryo, restricts fetal growth and increases offspring susceptibility to obesity. Theriogenology. 2011;75:287-299.
18. Königsdorf CA, Navarrete Santos A, Schmidt JS, Fischer S, Fischer B. Expression profile of fatty acid metabolism genes in preimplantation blastocysts of obese and non-obese mice. Obes Facts. 2012;5:575-586.
19. Mishima T, Miner JH, Morizane M, Stahl A, Sadovsky Y. The expression and function of fatty acid transport protein-2 and -4 in the murine placenta. PLoS ONE. 2011;6:e25865.
20. Scifres CM, Chen B, Nelson DM, Sadovsky Y. Fatty acid binding protein 4 regulates intracellular lipid accumulation in human trophoblasts. J Clin Endocrinol Metab. 2011;96:E1083-E1091.
21. Gertow K, Pietiläinen KH, Yki-Järvinen H, et al. Expression of fatty-acid-handling proteins in human adipose tissue in relation to obesity and insulin resistance. Diabetologia. 2004;47:1118-1125. (Pubitemid 38918172)
22. Storch J, Thumser AE. The fatty acid transport function of fatty acid-binding proteins. Biochim Biophys Acta. 2000;1486:28-44. (Pubitemid 30336790)
23. Storch J, McDermott L. Structural and functional analysis of fatty acid-binding proteins. J. Lipid Res. 2009;50(suppl):S126-S131.
24. Xu A, Wang Y, Xu JY, et al. Adipocyte fatty acid-binding protein is a plasma biomarker closely associated with obesity and metabolic syndrome. Clin Chem. 2006;52:405-413.
25. Karakas SE, Almario RU, Kim K. Serum fatty acid binding protein 4, free fatty acids, and metabolic risk markers. Metabolism. 2009;58:1002-1007.
26. Hillgartner FB, Salati LM, Goodridge AG. Physiological and molecular mechanisms involved in nutritional regulation of fatty acid synthesis. Physiol Rev. 1995;75:47-76.
27. Semenkovich CF. Regulation of fatty acid synthase (FAS). Prog Lipid Res. 1997;36:43-53. (Pubitemid 27387114)
28. Chirala SS, Chang H, Matzuk M, et al. Fatty acid synthesis is essential in embryonic development: fatty acid synthase null mutants and most of the heterozygotes die in utero. Proc Natl Acad Sci USA. 2003;100:6358-6363. (Pubitemid 36666586)
29. Horton JD, Goldstein JL, Brown MS. SREBPs: activators of the complete program of cholesterol and fatty acid synthesis in the liver. J Clin Invest. 2002;109:1125-1131. (Pubitemid 34496588)
30. Kim JB, Spotts GD, Halvorsen YD, et al. Dual DNA binding specificity of ADD1/SREBP1 controlled by a single amino acid in the basic helix-loop-helix domain. Mol Cell Biol. 1995;15:2582-2588.
31. Edwards PA, Tabor D, Kast HR, Venkateswaran A. Regulation of gene expression by SREBP and SCAP. Biochim Biophys Acta. 2000;1529:103-113.
32. Horton JD, Shimomura I, Brown MS, Hammer RE, Goldstein JL, Shimano H. Activation of cholesterol synthesis in preference to fatty acid synthesis in liver and adipose tissue of transgenic mice over-producing sterol regulatory element-binding protein-2. J Clin Invest. 1998;101:2331-2339. (Pubitemid 28270427)
33. Brown MS, Goldstein JL. The SREBP pathway: regulation of cholesterol metabolism by proteolysis of a membrane-bound transcription factor. Cell. 1997;89:331-340. (Pubitemid 27220877)
34. Shimano H, Horton JD, Hammer RE, Shimomura I, Brown MS, Goldstein JL. Overproduction of cholesterol and fatty acids causes massive liver enlargement in transgenic mice expressing truncated SREBP-1a. J Clin Invest. 1996;98:1575-1584. (Pubitemid 26327867)
35. Shimano H, Horton JD, Shimomura I, Hammer RE, Brown MS, Goldstein JL. Isoform 1c of sterol regulatory element binding protein is less active than isoform 1a in livers of transgenic mice and in cultured cells. J Clin Invest. 1997;99:846-854. (Pubitemid 27123620)
36. Engström E, Haglund A, Eriksson UJ. Effects of maternal diabetes or in vitro hyperglycemia on uptake of palmitic and arachidonic acid by rat embryos. Pediatr Res. 1991;30:150-153.
37. Pinter E, Reece EA, Leranth CZ, et al. Arachidonic acid prevents hyperglycemia-associated yolk sac damage and embryopathy. Am J Obstet Gynecol. 1986;155:691-702. (Pubitemid 17178308)
38. Pinter E, Reece EA, Ogburn PL Jr, et al. Fatty acid content of yolk sac and embryo in hyperglycemia-induced embryopathy and effect of arachidonic acid supplementation. Am J Obstet Gynecol. 1988;159:1484-1490. (Pubitemid 19021600)
39. Ramin N, Thieme R, Fischer S, et al. Maternal diabetes impairs gastrulation and insulin and IGF-I receptor expression in rabbit blastocysts. Endocrinology. 2010;151:4158-4167.
40. Santos AN, Körber S, Küllertz G, Fischer G, Fischer B. Oxygen stress increases prolyl cis/trans isomerase activity and expression of cyclophilin 18 in rabbit blastocysts. Biol Reprod. 2000;62:1-7. (Pubitemid 30013461)
41. Fischer B, Chavatte-Palmer P, Viebahn C, Navarrete Santos A, Duranthon V. Rabbit as a reproductive model for human health. Reproduction. 2012;144:1-10.
42. Maurer RR. Advances in rabbit embryo culture. In: Daniels JC, ed. Methods in Mammalian Reproduction. New York, NY: Academic Press; 1978:259-272.
43. Schaedlich K, Knelangen JM, Navarrete Santos A, Fischer B, Navarrete Santos A. A simple method to sort ESC-derived adipocytes. Cytometry A 2010;77,990-995.
44. Navarrete Santos A, Tonack S, Kirstein M, Kietz S, Fischer B. Two insulin-responsive glucose transporter isoforms and the insulin receptor are developmentally expressed in rabbit preimplantation embryos. Reproduction. 2004;128:503-516. (Pubitemid 40124281)
45. Tonack S, Fischer B, Navarrete Santos A. Expression of the insulin-responsive glucose transporter isoform 4 in blastocysts of C57/BL6 mice. Anat. Embryol. 2004;208:225-230. (Pubitemid 38925105)
46. Navarrete Santos A, Tonack S, Kirstein M, Pantaleon M, Kaye P, Fischer B. Insulin acts via mitogen-activated protein kinase phosphorylation in rabbit blastocysts. Reproduction. 2004;128:517-526. (Pubitemid 40124282)
47. Thieme R, Schindler M, Ramin N, et al. Insulin growth factor adjustment in preimplantation rabbit blastocysts and uterine tissues in response to maternal type 1 diabetes. Mol Cell Endocrinol. 2012;358:96-103.
48. Fischer S, Santos AN, Thieme R, Ramin N, Fischer B. Adiponectin stimulates glucose uptake in rabbit blastocysts. Biol Reprod. 2010;83:859-865.
49. Mills JL. Malformations in infants of diabetic mothers. Teratology. 1982;25:385-394.
50. Mills JL, Knopp RH, Simpson JL, et al. Lack of relation of increased malformation rates in infants of diabetic mothers to glycemic control during organogenesis. N Engl J Med. 1988;318:671-676. (Pubitemid 18083607)
51. Moley KH, Vaughn WK, DeCherney AH, Diamond MP. Effect of diabetes mellitus on mouse pre-implantation embryo development. J Reprod Fertil. 1991;93:325-332.
52. Silverman BL, Rizzo T, Green OC, et al. Long-term prospective evaluation of offspring of diabetic mothers. Diabetes 1991;40(suppl 2):121-125.
53. Silverman BL, Metzger BE, Cho NH, Loeb CA. Impaired glucose tolerance in adolescent offspring of diabetic mothers. Relationship to fetal hyperinsulinism. Diabetes Care 1995;18:611-617.
54. Moley KH. Diabetes and preimplantation events of embryogenesis. Semin Reprod Endocrinol. 1999;17:137-151.
55. Fraser RB, Waite SL, Wood KA, Martin KL. Impact of hyperglycemia on early embryo development and embryopathy: in vitro experiments using a mouse model. Hum Reprod. 2007;22:3059-3068. (Pubitemid 351696782)
56. Zusman I, Ornoy A, Yaffe P, Shafrir E. Effects of glucose and serum from streptozotocin-diabetic and nondiabetic rats on the in vitro development of preimplantation mouse embryos. Isr J Med Sci. 1985;21:359-365. (Pubitemid 15000507)
57. Diamond MP, Moley KH, Pellicer A, Vaughn WK, DeCherney AH. Effects of streptozotocin- and alloxan-induced diabetes mellitus on mouse follicular and early embryo development. J Reprod Fertil. 1989;86:1-10. (Pubitemid 19133459)
58. Pampfer S, de Hertogh R, Vanderheyden I, Michiels B, Vercheval M. Decreased inner cell mass proportion in blastocysts from diabetic rats. Diabetes. 1990;39:471-476. (Pubitemid 20111431)
59. De Hertogh R, Vanderheyden I, Pampfer S, Robin D, Dufrasne E, Delcourt J. Stimulatory and inhibitory effects of glucose and insulin on rat blastocyst development in vitro. Diabetes. 1991;40:641-647.
60. Moley KH, Chi MM, Manchester JK, McDougal DB, Lowry OH. Alterations of intraembryonic metabolites in preimplantation mouse embryos exposed to elevated concentrations of glucose: a metabolic explanation for the developmental retardation seen in preimplantation embryos from diabetic animals. Biol Reprod. 1996;54:1209-1216.
61. Moley KH. Hyperglycemia and apoptosis: mechanisms for congenital malformations and pregnancy loss in diabetic women. Trends Endocrinol Metab. 2001;12:78-82. (Pubitemid 33714193)
62. Cagnone GL, Dufort I, Vigneault C, Sirard MA. Differential gene expression profile in bovine blastocysts resulting from hyperglycemia exposure during early cleavage stages. Biol Reprod. 2012;86:50.
63. Scott-Drechsel DE, Rugonyi S, Marks DL, Thornburg KL, Hinds MT. Hyperglycemia slows embryonic growth and suppresses cell cycle via cyclin D1 and p21. Diabetes. 2013;62:234-242.
64. Abe H, Yamashita S, Satoh T, Hoshi H. Accumulation of cytoplasmic lipid droplets in bovine embryos and cryotolerance of embryos developed in different culture systems using serum-free or serum-containing media. Mol Reprod Dev. 2002;61:57-66. (Pubitemid 135715266)
65. Kissebah AH, Alfarsi S, Adams PW, Wynn V. The metabolic fate of plasma lipoproteins in normal subjects and in patients with insulin resistance and endogenous hypertriglyceridaemia. Diabetologia. 1976;12:501-509.
66. Kilby MD, Neary RH, Mackness MI, Durrington PN. Fetal and maternal lipoprotein metabolism in human pregnancy complicated by type I diabetes mellitus. J Clin Endocrinol Metab. 1998;83:1736-1741. (Pubitemid 28501050)
67. Merzouk H, Madani S, Korso N, Bouchenak M, Prost J, Belleville J. Maternal and fetal serum lipid and lipoprotein concentrations and compositions in type 1 diabetic pregnancy: relationship with maternal glycemic control. J Lab Clin Med. 2000;136:441-448.
68. Mooradian AD. Dyslipidemia in type 2 diabetes mellitus. Nat Clin Pract Endocrinol Metab. 2009;5:150-159.
69. Amri EZ, Bertrand B, Ailhaud G, Grimaldi P. Regulation of adipose cell differentiation. I. Fatty acids are inducers of the aP2 gene expression. J Lipid Res. 1991;32:1449-1456.
70. Elchalal U, Schaiff WT, Smith SD, et al. Insulin and fatty acids regulate the expression of the fat droplet-associated protein adipophilin in primary human trophoblasts. Am J Obstet Gynecol. 2005;193:1716-1723. (Pubitemid 41540472)
71. Pathmaperuma AN, Maña P, Cheung SN, et al. Fatty acids alter glycerolipid metabolism and induce lipid droplet formation, syncytialisation and cytokine production in human trophoblasts with minimal glucose effect or interaction. Placenta. 2010;31:230-239.
72. Flynn TJ, Hillman N. Lipid synthesis from [U14C]glucose in preimplantation mouse embryos in culture. Biol Reprod. 1978;19:922-926. (Pubitemid 9062158)
73. Sandberg MB, Fridriksson J, Madsen L, et al. Glucose-induced lipogenesis in pancreatic βcells is dependent on SREBP-1. Mol Cell Endocrinol. 2005;240:94-106. (Pubitemid 41135896)
74. Jun H, Song Z, Chen W, et al. In vivo and in vitro effects of SREBP-1 on diabetic renal tubular lipid accumulation and RNAi-mediated gene silencing study. Histochem Cell Biol. 2009;131:327-345.
75. Hao J, Zhu L, Zhao S, Liu S, Liu Q, Duan H. PTEN ameliorates high glucose-induced lipid deposits through regulating SREBP-1/FASN/ACC pathway in renal proximal tubular cells. Exp Cell Res. 2011;317:1629-1639.
76. Hao J, Liu S, Zhao S, et al. PI3K/Akt pathway mediates high glucose-induced lipogenesis and extracellular matrix accumulation in HKC cells through regulation of SREBP-1 and TGF-β1. Histochem Cell Biol. 2011;135:173-181.
77. Hasty AH, Shimano H, Yahagi N, et al. Sterol regulatory element-binding protein-1 is regulated by glucose at the transcriptional level. J Biol Chem. 2000;275:31069-31077.
78. Han C, Wang J, Li L, Zhang Z, Wang L, Pan Z. The role of insulin and glucose in goose primary hepatocyte triglyceride accumulation. J Exp Biol. 2009;212:1553-1558.
79. Uttarwar L, Gao B, Ingram AJ, Krepinsky JC. SREBP-1 activation by glucose mediates TGF-β upregulation in mesangial cells. Am J Physiol Renal Physiol. 2012;302:F329-F341.
80. Streicher R, Kotzka J, Müller-Wieland D, et al. SREBP-1 mediates activation of the low density lipoprotein receptor promoter by insulin and insulin-like growth factor-I. J Biol Chem. 1996;271:7128-7133. (Pubitemid 26104151)
81. Kaplan M, Kerry R, Aviram M, Hayek T. High glucose concentration increases macrophage cholesterol biosynthesis in diabetes through activation of the sterol regulatory element binding protein 1 (SREBP1): inhibitory effect of insulin. J Cardiovasc Pharmacol. 2008;52:324-332.
82. Xue JH, Yuan Z, Wu Y, et al. High glucose promotes intracellular lipid accumulation in vascular smooth muscle cells by impairing cholesterol influx and efflux balance. Cardiovasc Res. 2010;86:141-150.
83. Bavister BD. Culture of preimplantation embryos: facts and artifacts. Hum Reprod Update. 1995;1:91-148.
84. Young LE, Sinclair KD, Wilmut I. Large offspring syndrome in cattle and sheep. Rev Reprod. 1998;3:155-163. (Pubitemid 28508646)
85. McEvoy TG. Manipulation of domestic animal embryos and implications for development. Reprod Domest Anim. 2003;38:268-275. (Pubitemid 37053848)
86. Dumoulin JC, Land JA, Van Montfoort AP, et al. Effect of in vitro culture of human embryos on birthweight of newborns. Hum Reprod. 2010;25:605-612.
87. Knelangen JM, Kurz R, Schagdarsurengin U, Fischer B, Navarrete Santos A. Short-time glucose exposure of embryonic carcinoma cells impairs their function as terminally differentiated cardiomyocytes. Biochem Biophys Res Commun. 2012;420:230-235.
88. Wang Y, Jones Voy B, et al. The human fatty acid synthase gene and de novo lipogenesis are coordinately regulated in human adipose tissue. J Nutr. 2004;134:1032-1038. (Pubitemid 38619935)
89. Moustaïd N, Jones BH, Taylor JW. Insulin increases lipogenic enzyme activity in human adipocytes in primary culture. J Nutr. 1996;126:865-870. (Pubitemid 26100956)
90. Claycombe KJ, Jones BH, Standridge MK, et al. Insulin increases fatty acid synthase gene transcription in human adipocytes. Am J Physiol. 1998;274:R1253-R1259.
91. Smith PJ, Wise LS, Berkowitz R, Wan C, Rubin CS. Insulin-like growth factor-I is an essential regulator of the differentiation of 3T3-L1 adipocytes. J Biol Chem. 1988;263:9402-9408.
92. Blake WL, Clarke SD. Induction of adipose fatty acid binding protein (a-FABP) by insulin-like growth factor-1 (IGF-1) in 3T3-L1 preadipocytes. Biochem Biophys Res Commun. 1990;173:87-91.
93. Foretz M, Guichard C, Ferré P, Foufelle F. Sterol regulatory element binding protein-1c is a major mediator of insulin action on the hepatic expression of glucokinase and lipogenesis-related genes. Proc Natl Acad Sci USA. 1999;96:12737-12742. (Pubitemid 29513572)
94. Fleischmann M, Iynedjian PB. Regulation of sterol regulatory-element binding protein 1 gene expression in liver: role of insulin and protein kinase B/cAkt. Biochem J. 2000;349:13-17. (Pubitemid 30440159)