Reproductive, endocrine and metabolic feto-maternal features and placental gene expression in a swine breed with obesity/leptin resistance

General and Comparative Endocrinology

Volumn 176, Issue 1, 2012, Pages 94-101

  Gonzalez Bulnes, A ^a   Torres Rovira, L ^a   Ovilo, C ^a   Astiz, S ^a   Gomez Izquierdo, E ^b   Gonzalez Anover P ^c   Pallares, P ^a   Perez Solana, M L ^a   Sanchez Sanchez, R ^a  

^a INIA   (Spain)

^b INSTITUTO TECNOLÓGICO AGRARIO DE CASTILLA Y LEÓN   (Spain)

^c NUTEGA   (Spain)

Author keywords

Leptin; Metabolism; Obesity; Pregnancy; Swine

Indexed keywords

CHOLESTEROL; GLUCOSE; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; HORMONE; LEPTIN; TRIACYLGLYCEROL;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL FOOD; ANIMAL GENETICS; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG RESISTANCE; DYSLIPIDEMIA; ENDOCRINE FUNCTION; FEMALE; FETOPLACENTAL UNIT; FETUS; GENE EXPRESSION; GENOTYPE; LEPTIN GENE; LIPID METABOLISM; LIPID STORAGE; METABOLIC PARAMETERS; METABOLOME; METABOLOMICS; MORPHOLOGICAL TRAIT; NONHUMAN; NUCLEOTIDE SEQUENCE; OBESITY; PRIORITY JOURNAL; PROGESTERONE BLOOD LEVEL; REPRODUCTION; SWINE; VEGFA GENE;

EID: 84857118544     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1016/j.ygcen.2011.12.038     Document Type: Article

References (66)

1. Bazer F.W. Establishment of pregnancy in sheep and pigs. Reprod. Fertil. Dev. 1989, 1:237-242.
2. Bazer F.W., Thatcher W.W., Martinat-Botte F., Terqui M. Conceptus development in large white and prolific Chinese Meishan pigs. J. Reprod. Fertil. 1988, 84:37-42.
3. Biensen N.J., Wilson M.E., Ford S.P. Differential mechanisms regulating Meishan (M) and Yorkshire (Y) fetal growth. J. Anim. Sci. 1996, 74:215.
4. Bolet G., Martinat-Botte F., Locatelli A., Gruand J., Terqui M., Berthelot F. Components of prolificacy in hyperprolific Large White sows compared with the Meishan and Large White breeds. Genet. Sel. Evol. 1986, 18:333-342.
5. Brewer C.J., Balen A.H. The adverse effects of obesity on conception and implantation. Reproduction 2010, 140:347-364.
6. Buhi W.C., Ducsay C.A., Bartol F.F., Bazer F.W., Roberts R.M. A function of the allantoic sac in the metabolism of uteroferrin and maternal iron by the fetal pig. Placenta 1983, 4:455-469.
7. Burgos C., Carrodeguas J.A., Moreno C., Altarriba J., Tarrafeta L., Barcelona J.A. Allelic incident in several pig breeds of a missense variant of pig melanocortin-4 receptor (MC4R) gene associated with carcass and productive traits; its relation to IGF2 genotype. Meat Sci. 2006, 73:144-150.
8. Cao Y. Angiogenesis modulates adipogenesis and obesity. J. Clin. Invest. 2007, 117:2362-2368.
9. Coleman R.A., Haynes E.B. Microsomal and lysosomal enzymes of triacylglycerol metabolism in rat placenta. Biochem. J. 1984, 217:391-397.
10. Evans J., Catalano R.D., Brown P., Sherwin R., Critchley H.O., Fazleabas A.T., Jabbour H.N. Prokineticin 1 mediates fetal-maternal dialogue regulating endometrial leukemia inhibitory factor. FASEB J. 2009, 23:2165-2175.
11. Farooqi I.S., O'Rahilly S. Mutations in ligands and receptors of the leptin-melanocortin pathway that lead to obesity. Nat. Clin. Pract. Endocrinol. Metab. 2008, 4:569-577.
12. Fedorcsák P., Storeng R. Effects of leptin and leukemia inhibitory factor on preimplantation development and STAT3 signaling of mouse embryos in vitro. Biol. Reprod. 2003, 69:1531-1538.
13. Fernandez-Figares I., Lachica M., Nieto R., Rivera-Ferre M.G., Aguilera J.F. Serum profile of metabolites and hormones in obese (Iberian) and lean (Landrace) growing gilts fed balanced or lysine deficient diets. Livestock Sci. 2007, 110:73-81.
14. Fietta P. Focus on leptin, a pleiotropic hormone. Minerva Medica 2005, 96:65-75.
15. Ford S.P. Control of blood flow to the gravid uterus of domestic livestock species. J. Anim. Sci. 1995, 73:1852-1860.
16. Ford S.P., Schwartz N.K., Rothschild M.F., Conley A.J., Warner C.M. Influence of SLA haplotype on preimplantation embryonic cell number in miniature pigs. J. Reprod. Fertil. 1988, 84:99-104.
17. Ford S.P., Youngs C.R. Early embryonic development in prolific Meishan pigs. J. Reprod. Fertil. Suppl. 1993, 48:271-278.
18. Fujimoto V.Y., Kane J.P., Ishida B.Y., Bloom M.S., Browne R.W. High density lipoprotein metabolism and the human embryo. Hum. Reprod. Update 2010, 16:20-38.
19. Gambino Y.P., Maymo J.L., Perez-Perez A., Dueñas J.L., Sanchez-Margalet V., Calvo J.C., Varone C.L. 17beta-estradiol enhances leptin expression in human placental cells through genomic and nongenomic actions. Biol. Reprod. 2010, 83:42-51.
20. Gargett C.E., Rogers P.A. Human endometrial angiogenesis. Reproduction 2001, 121:181-186.
21. Gonzalez-Añover P., Encinas T., Sanz E., Letelier C.A., Torres-Rovira L., Mercado E.D., Pallares P., Sanchez-Sanchez R., Gonzalez-Bulnes A. Preovulatory follicle dynamics and ovulatory efficiency in sows with thrifty genotype and leptin resistance due to leptin receptor gene polymorphisms (Iberian pig). Gen. Comp. Endocrinol. 2011, 170:200-206.
22. Gonzalez-Añover P., Encinas T., Torres-Rovira L., Pallares P., Muñoz-Frutos J., Gomez-Izquierdo E., Sanchez-Sanchez R., Gonzalez-Bulnes A. Ovulation rate, embryo mortality and intrauterine growth retardation in obese swine with gene polymorphisms for leptin and melanocortin receptors. Theriogenology 2011, 75:34-41.
23. Hagen D.R., Houtz S.K., Griel L.C., Kavanaugh J.F. Concentrations of progesterone in arterial and venous plasma of fetal pigs and their dams in late gestation. Biol. Reprod. 1983, 29:919-923.
24. Haley C.S., Lee G.J. Genetic basis of prolificacy in Meishan pigs. J. Reprod. Fertil. Suppl. 1993, 48:247-259.
25. Henson M.C., Castracane V.D. Leptin in pregnancy: an update. Biol. Reprod. 2006, 74:218-229.
26. Herrera E., Amusquivar E., Lopez-Soldado I., Ortega H. Maternal lipid metabolism and placental lipid transfer. Horm. Res. 2006, 65:58-63.
27. Herrera E. Implications of dietary fatty acids during pregnancy on placental, fetal and postnatal development - a review. Placenta 2002, 23:S9-19.
28. Hill M., Pařízek A., Cibula D., Kancheva R., Jirásek J.E., Jirkovská M., Velíková M., Kubátová J., Klímková M., Pašková A., Zižka Z., Kancheva L., Kazihnitková H., Zamrazilová L., Stárka L. Steroid metabolome in fetal and maternal body fluids in human late pregnancy. J. Steroid Biochem. Mol. Biol. 2010, 122:114-132.
29. Hill M., Pařízek A., Jirásek J.E., Jirkovská M., Velíková M., Dušková M., Klímková M., PaŠková A., Žižka Z., Germanová A., Koucký M., Kalousová M., Stárka L. Is maternal progesterone actually independent of the fetal steroids?. Physiol. Res. 2010, 59:211-224.
30. Hoch M., Eberle A.N., Wagner U., Bussmann C., Peters T., Peterli R. Expression and localization of melanocortin-1 receptor in human adipose tissues of severely obese patients. Obesity 2007, 15:40-49.
31. Islami D., Bischof P., Chardonnens D. Modulation of placental vascular endothelial growth factor by leptin and hCG. Mol. Human Reprod. 2003, 9:395-398.
32. Jindal R., Cosgrove J.R., Foxcroft G.R. Progesterone mediates nutritionally induced effects on embryonic survival in gilts. J. Anim. Sci. 1997, 75:1063-1070.
33. Kawamura K., Sato N., Fukuda J., Kodama H., Kumagai J., Tanikawa H., Nakamura A., Tanaka T. Leptin promotes the development of mouse preimplantation embryos in vitro. Endocrinology 2002, 143:1922-1931.
34. López-Bote C.J. Sustained utilization of the Iberian pig breed. Meat Sci. 1998, 49:17-27.
35. Lubis A.R., Widia F., Soegondo S., Setiawati A. The role of SOCS-3 protein in leptin resistance and obesity. Acta Med. Indon. 2008, 40:89-95.
36. McCance R.A., Dickerson J.W.T. The composition and origin of the foetal fluids of the pig. J. Embryol. Exp. Morph. 1957, 5:43-50.
37. Martin S.S., Qasim A., Reilly M.P. Leptin resistance. a possible interface of inflammation and metabolism in obesity-related cardiovascular disease. J. Am. Coll. Cardiol. 2008, 52:1201-1210.
38. Metwally M., Ledger W.L., Li T.C. Reproductive endocrinology and clinical aspects of obesity in women. Ann. N. Y. Acad. Sci. 2008, 1127:140-146.
39. Mizuta E., Kokubo Y., Yamanaka I., Miyamoto Y., Okayama A., Yoshimasa Y., Tomoike H., Morisaki H., Morisaki T. Leptin gene and leptin receptor gene polymorphisms are associated with sweet preference and obesity. Hypertension Res. 2008, 31:1069-1077.
40. Muñoz G., Ovilo C., Silió L., Tomás A., Noguera J.L., Rodríguez M.C. Single- and joint-population analyses of two experimental pig crosses to confirm quantitative trait loci on Sus scrofa chromosome 6 and leptin receptor effects on fatness and growth traits. J. Anim. Sci. 2009, 87:459-468.
41. Myers M.G., Cowley M.A., Münzberg H. Mechanisms of leptin action and leptin resistance. Ann. Rev. Physiol. 2008, 70:537-556.
42. Nelson S.M., Freeman D.J., Sattar N., Johnstone F.D., Lindsay R.S. IGF-1 and leptin associate with fetal HDL cholesterol at birth: examination in offspring of mothers with type 1 diabetes. Diabetes 2007, 56:2705-2709.
43. Nieto R., Miranda A., García M.A., Aguilera J.F. The effect of dietary protein content and feeding level on the rate of protein deposition and energy utilization in growing Iberian pigs from 15 to 50 kg body weight. British J. Nutr. 2002, 88:39-49.
44. Ovilo C., Beni{dotless}tez R., Nunez Y., Rodri{dotless}guez C., Silio L. Hypothalamic expression of porcine leptin receptor (LEPR), neuropeptide Y (NPY), and cocaine- and amphetamine-regulated transcript (CART) genes is influenced by LEPR genotype. Mamm. Genome. 2010, 21:583-591.
45. Ovilo C., Fernández A., Noguera J.L., Barragán C., Letón R., Rodríguez C., Mercadé A., Alves E., Folch J.M., Varona L., Toro M. Fine mapping of porcine chromosome 6 QTL and LEPR effects on body composition in multiple generations of an Iberian by Landrace intercross. Genet. Res. 2005, 85:57-67.
46. Ovilo C., Fernandez A., Rodriguez M.C., Nieto M., Silio L. Association of MC4R gene variants with growth, fatness, carcass composition and meat and fat quality traits in heavy pigs. Meat Sci. 2006, 73:42-47.
47. Palinski M. Maternal Fetal Cholesterol Transport in the Placenta: Good, Bad, and Target for Modulation. Circ. Res. 2009, 104:569-571.
48. Przała J., Gregoraszczuk E.L., Kotwica G., Stefańczyk-Krzymowska S., Ziecik A.J., Blitek A., Ptak A., Rak A., Wójtowicz A., Kamiński T., Siawrys G., Smolińska N., Franczak A., Kurowicka B., Oponowicz A., Wasowska B., Chłopek J., Kowalczyk A.E., Kaczmarek M.M., Wacławik A. Mechanisms ensuring optimal conditions of implantation and embryo development in the pig. Reprod. Biol. 2006, 6:59-87.
49. Reynolds L.P., Redmer D.A. Utero-placental vascular development and placental function. J. Anim. Sci. 1995, 73:1839-1851.
50. Sandrock M., Schulz A., Merkwitz C., Schöneberg T., Spanel-Borowski K., Ricken A. Reduction in corpora lutea number in obese melanocortin-4-receptor-deficient mice. Reprod. Biol. Endocrinol. 2009, 7:24. 10.1186/1477-7827-7-24.
51. Schmidt W. The amniotic fluid compartment: the fetal habitat. Adv. Anat. Embryol. Cell Biol. 1992, 127:1-100.
52. Shaw J.L., Denison F.C., Evans J., Durno K., Williams A.R., Entrican G., Critchley H.O., Jabbour H.N., Horne A.W. Evidence of prokineticin dysregulation in fallopian tube from women with ectopic pregnancy. Fertil. Steril. 2010, 94:1601-1608.
53. Shelley H.J., Bassett J.M., Milner R.D. Control of carbohydrate metabolism in the fetus and newborn. Br. Med. Bull. 1975, 31:37-43.
54. Suganami E., Takagi H., Ohashi H., Suzuma K., Suzuma I., Oh H., Watanabe D., Ojima T., Suganami T., Fujio Y., Nakao K., Ogawa Y., Yoshimura N. Leptin stimulates ischemia-induced retinal neovascularization: possible role of vascular endothelial growth factor expressed in retinal endothelial cells. Diabetes 2004, 53:2443-2448.
55. Szabo A.J., DeLellis R., Grimaldi R.D. Triglyceride synthesis by human placental incorporation of labeled palmitate into placental triglycerides. Am. J. Obs. Gynecol. 1973, 115:257-262.
56. Van der Waaij E.H., Hazeleger W., Soede N.M., Laurenssen B.F.A., Kemp B. Effect of excessive, hormonally induced intrauterine crowding in the gilt on fetal development on day 40 of pregnancy. J. Anim. Sci. 2010, 88:2611-2619.
57. Vecchione C., Maffei A., Colella S., Aretini A., Poulet R., Frati G., Gentile M.T., Fratta L., Trimarco V., Trimarco B., Lembo G. Leptin effect on endothelial nitric oxide is mediated through Akt-endothelial nitric oxide synthase phosphorylation pathway. Diabetes 2002, 51:168-173.
58. Vonnahme K.A., Wilson M.E., Ford S.P. Relationship between placental vascular endothelial growth factor expression and placental/endometrial vascularity in the pig. Biol. Reprod. 2001, 64:1821-1825.
59. Wadsack C., Tabano S., Maier A., Hiden U., Alvino G., Cozzi V., Hüttinger M., Schneider W.J., Lang U., Cetin I., Desoye G. Intrauterine growth restriction is associated with alterations in placental lipoprotein receptors and maternal lipoprotein composition. Am. J. Physiol. Endocrinol. Metab. 2007, 292:E476-484.
60. White V., González E., Capobianco E., Pustovrh C., Soñez C., Romanini M.C., Jawerbaum A. Modulatory effect of leptin on nitric oxide production and lipid metabolism in term placental tissues from control and streptozotocin-induced diabetic rats. Reprod. Fertil. Dev. 2004, 16:363-372.
61. Wise T., Roberts A.J., Christenson R.K. Relationships of light and heavy fetuses to uterine position, placental weight, gestational age, and fetal cholesterol concentrations. J. Anim. Sci. 1997, 75:2197-2207.
62. Wise T., Young L.D., Pond W.G. Reproductive, endocrine, and organ weight differences of swine selected for high or low serum cholesterol. J. Anim. Sci. 1993, 71:2732-2738.
63. Whittemore C.T., Kyriazakis I. Whittemore's Science and Practice of Pig Production 2006, Wiley-Blackwell. 3rd ed.
64. Woollett L.A. The origins and roles of cholesterol and fatty acids in the fetus. Curr. Opin. Lipidol. 2001, 12:305-312.
65. Young L.D. Comparison of Meishan, Fending, Minzhu and Duroc swine: Effects on reproductive traits of F1 gilts. J. Anim. Sci. 1993, 71:34.
66. Youngs C.R., Christenson L.K., Ford S.P. Investigations into the control of litter size in swine: III. A reciprocal embryo transfer study of early conceptus development. J. Anim. Sci. 1994, 72:725-731.