Hyperlipidic hypercholesterolemic diet in prepubertal rabbits affects gene expression in the embryo, restricts fetal growth and increases offspring susceptibility to obesity

Theriogenology

Volumn 75, Issue 2, 2011, Pages 287-299

  Picone, O ^a,b   Laigre, P ^c   Fortun Lamothe, L ^d,e,f   Archilla, C ^a   Peynot, N ^a   Ponter, A A ^g   Berthelot, V ^h   Cordier, A G ^a,b   Duranthon, V ^a   Chavatte Palmer, P ^a,i  

^a INRA Institut National de la Recherche Agronomique   (France)

^b UNIVERSITÉ PARIS SACLAY   (France)

^c Domaine de Bressonvilliers ^*  (France)

^d CEMAGREF   (France)

^e UNIVERSITÉ DE TOULOUSE   (France)

^f UNIVERSITÉ DE TOULOUSE   (France)

^g ECOLE NATIONALE VÉTÉRINAIRE D ALFORT   (France)

^h INRA Institut National de la Recherche Agronomique   (France)

ⁱ PremUP   (France)

Author keywords

Embryo; Lipids; Programming; Rabbit

Indexed keywords

ORYCTOLAGUS CUNICULUS;

EID: 78650253563     PISSN: 0093691X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.theriogenology.2010.08.015     Document Type: Article

References (50)

1. Barker D.J.P., Eriksson J.G., Forsen T., Osmond C. Fetal origins of adult disease: strength of effects and biological basis. International Journal of Epidemiology 2002, 31:1235-1239.
2. Gluckman P.D., Hanson M.A. Living with the past: evolution, development, and patterns of disease. Science 2004, 305:1733-1736.
3. Armitage J.A., Taylor P.D., Poston L. Experimental models of developmental programming: consequences of exposure to an energy rich diet during development. J Physiol (Lond) 2005, 565:3-8.
4. Napoli C., Glass C.K., Witztum J.L., Deutsch R., D'Armiento F.P., Palinski W. Influence of maternal hypercholesterolaemia during pregnancy on progression of early atherosclerotic lesions in childhood: Fate of Early Lesions in Children (FELIC) study. Lancet 1999, 354:1234-1241.
5. Herrera E., Amusquivar E., Lopez-Soldado I., Ortega H. Maternal lipid metabolism and placental lipid transfer. Horm Res 2006, 65:58-63.
6. Haggarty P. Placental Regulation of Fatty Acid Delivery and its Effect on Fetal Growth-A Review. Placenta 2002, 23:S28-S38.
7. Hendrickse W., Stammers J.P., Hull D. The transfer of free fatty acids across the human placenta. Br J Obstet Gynaecol 1985, 92.
8. Herrera E. Implications of dietary fatty acids during pregnancy on placental, fetal and postnatal development - a review. Placenta 2002, 23:S9-S19.
9. Ghosh P., Bitsanis D., Ghebremeskel K., Crawford M.A., Poston L. Abnormal aortic fatty acid composition and small artery function in offspring of rats fed a high fat diet in pregnancy. J Physiol 2001, 533:815-822.
10. Khan I.Y., Taylor P.D., Dekou V., Seed P.T., Lakasing L., Graham D., Dominiczak A.F., Hanson M.A., Poston L. Gender-Linked Hypertension in Offspring of Lard-Fed Pregnant Rats. Hypertension 2003, 41:168-175.
11. Howie G.J., Sloboda D.M., Kamal T., Vickers M.H. Maternal nutritional history predicts obesity in adult offspring independent of postnatal diet. The Journal of Physiology 2009, 587:905-915.
12. Fan J., Watanabe T. Transgenic rabbits as therapeutic protein bioreactors and human disease models. Pharmacol Ther 2003, 99:261-282.
13. Palinski W., D'Armiento F.P., Witztum J.L., de Nigris F., Casanada F., Condorelli M., Silvestre M., Napoli C. Maternal Hypercholesterolemia and Treatment During Pregnancy Influence the Long-Term Progression of Atherosclerosis in Offspring of Rabbits. Circ Res 2001, 89:991-996.
14. Yamashita T., Freigang S., Eberle C., Pattison J., Gupta S., Napoli C., Palinski W. Maternal immunization programs postnatal immune responses and reduces atherosclerosis in offspring. Circ Res 2006, 99:E51-E64.
15. Napoli C., Witztum J.L., Calara F., de Nigris F., Palinski W. Maternal Hypercholesterolemia Enhances Atherogenesis in Normocholesterolemic Rabbits, Which Is Inhibited by Antioxidant or Lipid-Lowering Intervention During Pregnancy: An Experimental Model of Atherogenic Mechanisms in Human Fetuses. Circ Res 2000, 87:946-952.
16. Montoudis A., Simoneau L., Brissette L., Forest J.-C., Savard R., Lafond J. Impact of a cholesterol enriched diet on maternal and fetal plasma lipids and fetal deposition in pregnant rabbits. Life Sci 1999, 64:2439-2450.
17. Kevorkova O., Ethier-Chiasson M., Lafond J. Differential expression of glucose transporters in rabbit placenta: Effect of hypercholesterolemia in dams. Biol Reprod 2007, 76:487-495.
18. Brachet A. Recherches sur le déterminisme héréditaire de l'oeuf des Mammifères. Développement 'in vitro' de jeunes vésicules blastodermiques de Lapin. Arch Biol (Liège) 1913, 28:447-503.
19. Montoudis A., Boileau S., Simoneau L., Lafond J. Impact of an enriched-cholesterol diet on enzymatic cholesterol metabolism during rabbit gestation. Life Sci 2003, 73:1463-1477.
20. Zilversmit D.G., Remington M., Hughes L.B. Fetal growth and placental permeability in rabbits fed cholesterol. J Nutr 1972, 102:1681-1687.
21. Evans, Madden, Denton Diversity of responses of renal cortical and medullary blood flow to vasoconstrictors in conscious rabbits. Acta Physiol Scand 2000, 169:297-308.
22. Leandri R.D., Archilla C., Bui L.C., Peynot N., Liu Z., Cabau C., Chastellier A., Renard J.P., Duranthon V. Revealing the dynamics of gene expression during embryonic genome activation and first differentiation in the rabbit embryo with a dedicated array screening. Physiol Genomics 2009, 36:98-113.
23. Didier G., Brezellec P., Remy E., Henaut A. GeneANOVA - gene expression analysis of variance. Bioinformatics 2002, 18:490-491.
24. Bui L.C., Evsikov A.V., Khan D.R., Archilla C., Peynot N., Henaut A., Le Bourhis D., Vignon X., Renard J.P., Duranthon V. Retrotransposon expression as a defining event of genome reprogramming in fertilized and cloned bovine embryos. Reproduction 2009, 138:289-299.
25. Chavatte-Palmer P., Laigre P., Simonoff E., Chesne P., Challah-Jacques M., Renard J.P. In utero characterisation of fetal growth by ultrasound scanning in the rabbit. Theriogenology 2008, 69:859-869.
26. Zhang C., Zheng H., Yu Q., Yang P., Li Y., Cheng F., Fan J., Liu E. A Practical Method for Quantifying Atherosclerotic Lesions in Rabbits. J Comp Pathol 2010, 142:122-128.
27. Jeon S.M., Park Y.B., Kwon O.S., Huh T.L., Lee W.H., Do K.M., Park T., Choi M.S. Vitamin E supplementation alters HDL-cholesterol concentration and paraoxonase activity in rabbits fed high-cholesterol diet: comparison with probucol. J Biochem Mol Toxicol 2005, 19:336-346.
28. Littell R.C., Henry P.R., Ammerman C.B. Statistical analysis of repeated measures data using SAS procedures. J Anim Sci 1998, 76:1216-1231.
29. Larigauderie G., Furman C., Jaye M., Lasselin C., Copin C., Fruchart J.C., Castro G., Rouis M. Adipophilin enhances lipid accumulation and prevents lipid efflux from THP-1 macrophages: potential role in atherogenesis. Arterioscler Thromb Vasc Biol 2004, 24:504-510.
30. Gao J., Serrero G. Adipose differentiation related protein (ADRP) expressed in transfected COS-7 cells selectively stimulates long chain fatty aciduptake. J Biol Chem 1999, 274:16825-16830.
31. Miura S., Gan J.-W., Brzostowski J., Parisi M.J., Schultz C.J., Londos C., Oliver B., Kimmel A.R. 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.
32. Kikuchi K., Ekwall H., Tienthai P., Kawai Y., Noguchi J., Kaneko H., Rodriguez-Martinez H. 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.
33. 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.
34. Cermelli S., Guo Y., Gross S.P., Welte M.A. The Lipid-Droplet Proteome Reveals that Droplets Are a Protein-Storage Depot. Curr Biol 2006, 16:1783-1795.
35. Sjoblom C., Roberts C.T., Wikland M., Robertson S.A. Granulocyte-Macrophage Colony-Stimulating Factor Alleviates Adverse Consequences of Embryo Culture on Fetal Growth Trajectory and Placental Morphogenesis. Endocrinology 2005, 146:2142-2153.
36. Kwong W., Wild A., Roberts P., Willis A., Fleming T. Maternal undernutrition during the preimplantation period of rat development causes blastocyst abnormalities and programming of postnatal hypertension. Development 2000, 127:4195-4202.
37. Fleming T.P., Kwong W.Y., Porter R., Ursell E., Fesenko I., Wilkins A., Miller D.J., Watkins A.J., Eckert J.J. The embryo and its future. Biol Reprod 2004, 71:1046-1054.
38. Maloney C.A., Rees W.D. Gene-nutrient interactions during foetal development. Reproduction 2005, 130:401-410.
39. Watkins A.J., Ursell E., Panton R., Papenbrock T., Hollis L., Cunningham C., Wilkins A., Perry V.H., Sheth B., Kwong W.Y., Eckert J.J., Wild A.E., Hanson M.A., Osmond C., Fleming T.P. Adaptive Responses by Mouse Early Embryos to Maternal Diet Protect Fetal Growth but Predispose to Adult Onset Disease. Biol Reprod 2008, 78:299-306.
40. Hales C.N., Desai M., Ozanne S.E., Crowther N.J. Fishing in the stream of diabetes: from measuring insulin to the control of fetal organogenesis. Biochem Soc Trans 1996, 24:341-350.
41. Hales N.C., Ozanne S.E. The dangerous road of catch-up growth. J Physiol 2003, 547:5-10.
42. Jennings B.J., Ozanne S.E., Dorling M.W., Hales C.N. Early growth determines longevity in male rats and may be related to telomere shortening in the kidney. Febs Lett 1999, 448:4-8.
43. Leon D.A., Koupilova I., Lithell H.O., Berglund L., Mohsen R., Vagero D., Lithell U.B., McKeigue P.M. Failure to realise growth potential in utero and adult obesity in relation to blood pressure in 50 year old Swedish men. Br Med J 1996, 312:401-406.
44. Eriksson J., Forsen T., Tuomilehto J., Winter P.D., Osmond C., Barker D. Catch-up growth in childhood and death from coronary heart disease: longitudinal study. Br Med J 1999, 318:427-431.
45. Forsen T., Eriksson J., Tuomilehto J., Reunanen A., Osmond C., Barker D. The fetal and childhood growth of persons who develop type 2 diabetes. Ann Intern Med 2000, 133:176-182.
46. Ong K.K., Ahmed M.L., Emmett P.M., Preece M.A., Dunger D.B. Association between postnatal catch-up growth and obesity in childhood: prospective cohort study. Br Med J 2000, 320:967-971.
47. Gluckman P.D., Hanson M.A. Developmental plasticity and human disease: research directions. J Intern Med 2007, 261:461-471.
48. O'Regan D., Kenyon C.J., Seckl J.R., Holmes M.C. Prenatal dexamethasone 'programmes' hypotension, but stress-induced hypertension in adult offspring. J Endocrinol 2008, 196:343-352.
49. Napoli C., D'Armiento F.P., Mancini F.P., Postiglione A., Witztum J.L., Palumbo G., Palinski W. Fatty streak formation occurs in human fetal aortas and is greatly enhanced by maternal hypercholesterolemia-Intimal accumulation of low density lipoprotein and its oxidation precede monocyte recruitment into early atherosclerotic lesions. J Clin Invest 1997, 100:2680-2690.
50. Lussana F., Painter R.C., Ocke M.C., Buller H.R., Bossuyt P.M., Roseboom T.J. Prenatal exposure to the Dutch famine is associated with a preference for fatty foods and a more atherogenic lipid profile. Am J Clin Nutr 2008, 88:1648-1652.