Maternal undernutrition during the preimplantation period of rat development causes blastocyst abnormalities and programming of postnatal hypertension

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JOURNAL ARTICLES

Maternal undernutrition during the preimplantation period of rat development causes blastocyst abnormalities and programming of postnatal hypertension

WY Kwong, AE Wild, P Roberts, AC Willis and TP Fleming
Division of Cell Sciences, School of Biological Sciences, University of Southampton, Bassett Crescent East, Southampton SO16 7PX, UK.

Epidemiological studies have indicated that susceptibility of human adults to hypertension and cardiovascular disease may result from intrauterine growth restriction and low birth weight induced by maternal undernutrition. Although the 'foetal origins of adult disease' hypothesis has significant relevance to preventative healthcare, the origin and biological mechanisms of foetal programming are largely unknown. Here, we investigate the origin, embryonic phenotype and potential maternal mechanisms of programming within an established rat model. Maternal low protein diet (LPD) fed during only the preimplantation period of development (0-4.25 days after mating), before return to control diet for the remainder of gestation, induced programming of altered birthweight, postnatal growth rate, hypertension and organ/body-weight ratios in either male or female offspring at up to 12 weeks of age. Preimplantation embryos collected from dams after 0-4.25 days of maternal LPD displayed significantly reduced cell numbers, first within the inner cell mass (ICM; early blastocyst), and later within both ICM and trophectoderm lineages (mid/late blastocyst), apparently induced by a slower rate of cellular proliferation rather than by increased apoptosis. The LPD regimen significantly reduced insulin and essential amino acid levels, and increased glucose levels within maternal serum by day 4 of development. Our data indicate that long-term programming of postnatal growth and physiology can be induced irreversibly during the preimplantation period of development by maternal protein undernutrition. Further, we propose that the mildly hyperglycaemic and amino acid-depleted maternal environment generated by undernutrition may act as an early mechanism of programming and initiate conditions of 'metabolic stress', restricting early embryonic proliferation and the generation of appropriately sized stem-cell lineages.

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				C. E. Minge, B. D. Bennett, R. J. Norman, and R. L. Robker Peroxisome Proliferator-Activated Receptor-{gamma} Agonist Rosiglitazone Reverses the Adverse Effects of Diet-Induced Obesity on Oocyte Quality Endocrinology, May 1, 2008; 149(5): 2646 - 2656. [Abstract] [Full Text] [PDF]

				A. J. Watkins, A. Wilkins, C. Cunningham, V. H. Perry, M. J. Seet, C. Osmond, J. J. Eckert, C. Torrens, F. R. A. Cagampang, J. Cleal, et al. Low protein diet fed exclusively during mouse oocyte maturation leads to behavioural and cardiovascular abnormalities in offspring J. Physiol., April 15, 2008; 586(8): 2231 - 2244. [Abstract] [Full Text] [PDF]

				E. Kajantie, D. J P Barker, C. Osmond, T. Forsen, and J. G Eriksson Growth before 2 years of age and serum lipids 60 years later: The Helsinki Birth Cohort Study Int. J. Epidemiol., April 1, 2008; 37(2): 280 - 289. [Abstract] [Full Text] [PDF]

				A. J Watkins, E. Ursell, R. Panton, T. Papenbrock, L. Hollis, C. Cunningham, A. Wilkins, V. H. Perry, B. Sheth, W. Y. Kwong, et al. Adaptive Responses by Mouse Early Embryos to Maternal Diet Protect Fetal Growth but Predispose to Adult Onset Disease Biol Reprod, February 1, 2008; 78(2): 299 - 306. [Abstract] [Full Text] [PDF]

				B Mahsoudi, A Li, and C O'Neill Assessment of the Long-Term and Transgenerational Consequences of Perturbing Preimplantation Embryo Development in Mice Biol Reprod, November 1, 2007; 77(5): 889 - 896. [Abstract] [Full Text] [PDF]

				Wenjing Zhong, Yufen Xie, Yingchun Wang, J. Lewis, A. Trostinskaia, Fangfei Wang, E. E. Puscheck, and D. A. Rappolee Use of Hyperosmolar Stress to Measure Stress-Activated Protein Kinase Activation and Function in Human HTR Cells and Mouse Trophoblast Stem Cells Reproductive Sciences, September 1, 2007; 14(6): 534 - 547. [Abstract] [PDF]

				Y. Xie, W. Zhong, Y. Wang, A. Trostinskaia, F. Wang, E.E. Puscheck, and D.A. Rappolee Using hyperosmolar stress to measure biologic and stress-activated protein kinase responses in preimplantation embryos Mol. Hum. Reprod., July 1, 2007; 13(7): 473 - 481. [Abstract] [Full Text] [PDF]

				J. P. Porter, S. H. King, and A. D. Honeycutt Prenatal high-salt diet in the Sprague-Dawley rat programs blood pressure and heart rate hyperresponsiveness to stress in adult female offspring Am J Physiol Regulatory Integrative Comp Physiol, July 1, 2007; 293(1): R334 - R342. [Abstract] [Full Text] [PDF]

				J. G. Eriksson, T. J. Forsen, E. Kajantie, C. Osmond, and D. J.P. Barker Childhood Growth and Hypertension in Later Life Hypertension, June 1, 2007; 49(6): 1415 - 1421. [Abstract] [Full Text] [PDF]

				J. K. Cleal, K. R. Poore, J. P. Boullin, O. Khan, R. Chau, O. Hambidge, C. Torrens, J. P. Newman, L. Poston, D. E. Noakes, et al. Mismatched pre- and postnatal nutrition leads to cardiovascular dysfunction and altered renal function in adulthood PNAS, May 29, 2007; 104(22): 9529 - 9533. [Abstract] [Full Text] [PDF]

				A. J. Watkins, D. Platt, T. Papenbrock, A. Wilkins, J. J. Eckert, W. Y. Kwong, C. Osmond, M. Hanson, and T. P. Fleming From the Cover: Mouse embryo culture induces changes in postnatal phenotype including raised systolic blood pressure PNAS, March 27, 2007; 104(13): 5449 - 5454. [Abstract] [Full Text] [PDF]

				P D Gluckman and M A Hanson Adult disease: echoes of the past Eur. J. Endocrinol., November 1, 2006; 155(suppl_1): S47 - S50. [Abstract] [Full Text] [PDF]

				A. Chamson-Reig, S. M Thyssen, E. Arany, and D. J Hill Altered pancreatic morphology in the offspring of pregnant rats given reduced dietary protein is time and gender specific. J. Endocrinol., October 1, 2006; 191(1): 83 - 92. [Abstract] [Full Text] [PDF]

				C. Thone-Reineke, P. Kalk, M. Dorn, S. Klaus, K. Simon, T. Pfab, M. Godes, P. Persson, T. Unger, and B. Hocher High-protein nutrition during pregnancy and lactation programs blood pressure, food efficiency, and body weight of the offspring in a sex-dependent manner Am J Physiol Regulatory Integrative Comp Physiol, October 1, 2006; 291(4): R1025 - R1030. [Abstract] [Full Text] [PDF]

				A.-M. Samuelsson, C. Alexanderson, J. Molne, B. Haraldsson, P. Hansell, and A. Holmang Prenatal exposure to interleukin-6 results in hypertension and alterations in the renin-angiotensin system of the rat J. Physiol., September 15, 2006; 575(3): 855 - 867. [Abstract] [Full Text] [PDF]

				B. Dzyuba, K. J. W. Van Look, A. Cliffe, H. J. Koldewey, and W. V. Holt Effect of parental age and associated size on fecundity, growth and survival in the yellow seahorse Hippocampus kuda J. Exp. Biol., August 15, 2006; 209(16): 3055 - 3061. [Abstract] [Full Text] [PDF]

				W. Y. Kwong, D. J Miller, E. Ursell, A. E Wild, A. P Wilkins, C. Osmond, F. W Anthony, and T. P Fleming Imprinted gene expression in the rat embryo-fetal axis is altered in response to periconceptional maternal low protein diet. Reproduction, August 1, 2006; 132(2): 265 - 277. [Abstract] [Full Text] [PDF]

				M. Auroux The child of problems. Hum. Reprod., July 1, 2006; 21(7): 1943 - 1944. [Full Text] [PDF]

				F H Bloomfield, M H Oliver, and J E Harding The late effects of fetal growth patterns. Arch. Dis. Child. Fetal Neonatal Ed., July 1, 2006; 91(4): F299 - F304. [Abstract] [Full Text] [PDF]

				W. D. Rees, F. A. Wilson, and C. A. Maloney Sulfur Amino Acid Metabolism in Pregnancy: The Impact of Methionine in the Maternal Diet J. Nutr., June 1, 2006; 136(6): 1701S - 1705S. [Abstract] [Full Text] [PDF]

				H. S. Andersen, L. Gambling, G. Holtrop, and H. J. McArdle Maternal Iron Deficiency Identifies Critical Windows for Growth and Cardiovascular Development in the Rat Postimplantation Embryo J. Nutr., May 1, 2006; 136(5): 1171 - 1177. [Abstract] [Full Text] [PDF]

				G. A. Thouas, A. O. Trounson, and G. M. Jones Developmental Effects of Sublethal Mitochondrial Injury in Mouse Oocytes Biol Reprod, May 1, 2006; 74(5): 969 - 977. [Abstract] [Full Text] [PDF]

				C. Torrens, L. Brawley, F. W. Anthony, C. S. Dance, R. Dunn, A. A. Jackson, L. Poston, and M. A. Hanson Folate Supplementation During Pregnancy Improves Offspring Cardiovascular Dysfunction Induced by Protein Restriction Hypertension, May 1, 2006; 47(5): 982 - 987. [Abstract] [Full Text] [PDF]

				Y. Xie, E.E. Puscheck, and D.A. Rappolee Effects of SAPK/JNK inhibitors on preimplantation mouse embryo development are influenced greatly by the amount of stress induced by the media Mol. Hum. Reprod., April 1, 2006; 12(4): 217 - 224. [Abstract] [Full Text] [PDF]

				L. J. Van Winkle, J. K. Tesch, A. Shah, and A. L. Campione System B0,+ amino acid transport regulates the penetration stage of blastocyst implantation with possible long-term developmental consequences through adulthood Hum. Reprod. Update, March 1, 2006; 12(2): 145 - 157. [Abstract] [Full Text] [PDF]

				A. Watkins, A. Wilkins, C. Osmond, C. M. Warner, M. Comiskey, M. Hanson, and T. P. Fleming The influence of mouse Ped gene expression on postnatal development J. Physiol., February 15, 2006; 571(1): 211 - 220. [Abstract] [Full Text] [PDF]

				B. T. Alexander Fetal programming of hypertension Am J Physiol Regulatory Integrative Comp Physiol, January 1, 2006; 290(1): R1 - R10. [Abstract] [Full Text] [PDF]

				R. M Schultz From egg to embryo: a peripatetic journey Reproduction, December 1, 2005; 130(6): 825 - 828. [Abstract] [Full Text] [PDF]

				A. A. Jackson Integrating the Ideas of Life Course across Cellular, Individual, and Population Levels in Cancer Causation J. Nutr., December 1, 2005; 135(12): 2927S - 2933S. [Abstract] [Full Text] [PDF]