Protein-energy malnutrition during early gestation in sheep blunts fetal renal vascular and nephron development and compromises adult renal function

Journal of Physiology

Volumn 590, Issue 2, 2012, Pages 377-393

  Lloyd, Louise J ^a   Foster, Thomas ^a   Rhodes, Phillip ^a   Rhind, Stewart M ^b   Gardner, David S ^a  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^b SCOTTISH CROP RESEARCH INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AGING; ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; ASYMPTOMATIC DISEASE; CONTROLLED STUDY; DISEASE EXACERBATION; DISEASE SEVERITY; FEMALE; FETUS; FETUS CELL; GESTATION PERIOD; GLOMERULUS; KIDNEY BLOOD FLOW; KIDNEY BLOOD VESSEL; KIDNEY DEVELOPMENT; KIDNEY DYSFUNCTION; KIDNEY HYPERTROPHY; MALE; MATERNAL NUTRITION; MICROALBUMINURIA; MICROVASCULATURE; NEPHRON; NONHUMAN; OBESITY; PREDICTION; PRIORITY JOURNAL; PROTEIN CALORIE MALNUTRITION; SHEEP;

ANIMALS; APOPTOSIS; BLOOD VESSELS; BODY COMPOSITION; FEMALE; FETAL DEVELOPMENT; FETUS; KIDNEY; MALE; MODELS, ANIMAL; NEOVASCULARIZATION, PHYSIOLOGIC; NEPHRONS; ORGANOGENESIS; PREGNANCY; PREGNANCY COMPLICATIONS; PRENATAL EXPOSURE DELAYED EFFECTS; PROTEIN-ENERGY MALNUTRITION; SHEEP;

EID: 84855886811     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2011.220186     Document Type: Article

References (80)

1. Amann K, Wanner C & Ritz E (2006). Cross-talk between the kidney and the cardiovascular system. J Am Soc Nephrol 17, 2112-2119.
2. Bains RK, Sibbons PD, Murray RD, Howard CV & Van Velzen D (1996). Stereological estimation of the absolute number of glomeruli in the kidneys of lambs. Res Vet Sci 60, 122-125.
3. Bakris GL & Ritz E (2009). The message for World Kidney Day 2009: hypertension and kidney disease: a marriage that should be prevented. Kidney Int 75, 449-452.
4. Barker DJ & Osmond C (1986). Infant mortality, childhood nutrition, and ischaemic heart disease in England and Wales. Lancet 1, 1077-1081.
5. Barker DJ & Osmond C (1988). Low birth weight and hypertension. BMJ 297, 134-135.
6. Barker DJ, Osmond C, Forsen TJ, Kajantie E & Eriksson JG (2005). Trajectories of growth among children who have coronary events as adults. N Engl J Med 353, 1802-1809.
7. Bermejo-Alvarez P, Rizos D, Rath D, Lonergan P & Gutierrez-Adan A (2010). Sex determines the expression level of one third of the actively expressed genes in bovine blastocysts. Proc Natl Acad Sci U S A 107, 3394-3399.
8. Brennan KA, Gopalakrishnan GS, Kurlak L, Rhind SM, Kyle CE, Brooks AN et al (2005). Impact of maternal undernutrition and fetal number on glucocorticoid, growth hormone and insulin-like growth factor receptor mRNA abundance in the ovine fetal kidney. Reproduction 129, 151-159.
9. Brenner BM, Garcia DL & Anderson S (1988). Glomeruli and blood pressure. Less of one, more the other? Am J Hypertens 1, 335-347.
10. Carone BR, Fauquier L, Habib N, Shea JM, Hart CE, Li R et al (2010). Paternally induced transgenerational environmental reprogramming of metabolic gene expression in mammals. Cell 143, 1084-1096.
11. Cignarelli M & Lamacchia O (2007). Obesity and kidney disease. Nutr Metab Cardiovasc Dis 17, 757-762.
12. Cordain L, Eaton SB, Sebastian A, Mann N, Lindeberg S, Watkins BA et al (2005). Origins and evolution of the Western diet: health implications for the 21st century. Am J Clin Nutr 81, 341-354.
13. Cox LA, Nijland MJ, Gilbert JS, Schlabritz-Loutsevitch NE, Hubbard GB, McDonald TJ et al (2006). Effect of 30 per cent maternal nutrient restriction from 0.16 to 0.5 gestation on fetal baboon kidney gene expression. J Physiol 572, 67-85.
14. Crispi F, Bijnens B, Figueras F, Bartrons J, Eixarch E, Le Noble F et al (2010). Fetal growth restriction results in remodelled and less efficient hearts in children. Circulation 121, 2427-2436.
15. Crook ED (2002). Diabetic renal disease in African Americans. Am J Med Sci 323, 78-84.
16. Daar AS, Singer PA, Persad DL, Pramming SK, Matthews DR, Beaglehole R et al (2007). Grand challenges in chronic non-communicable diseases. Nature 450, 494-496.
17. Desai M, Crowther NJ, Lucas A & Hales CN (1996). Organ-selective growth in the offspring of protein-restricted mothers. Br J Nutr 76, 591-603.
18. Drummond GB (2009). Reporting ethical matters inThe Journal of Physiology: standards and advice. J Physiol 587, 713-719.
19. Eaton SB & Eaton SB, 3rd (2000). Paleolithicvs.modern diets - selected pathophysiological implications. Eur J Nutr 39, 67-70.
20. Egan BM, Zhao Y & Axon RN (2010). US trends in prevalence, awareness, treatment, and control of hypertension, 1988-2008. JAMA 303, 2043-2050.
21. Ejerblad E, Fored CM, Lindblad P, Fryzek J, McLaughlin JK & Nyren O (2006). Obesity and risk for chronic renal failure. J Am Soc Nephrol 17, 1695-1702.
22. Eremina V, Jefferson JA, Kowalewska J, Hochster H, Haas M, Weisstuch J et al (2008). VEGF inhibition and renal thrombotic microangiopathy. N Engl J Med 358, 1129-1136.
23. Fejzo MS, Poursharif B, Korst LM, Munch S, MacGibbon KW, Romero R & Goodwin TM (2009). Symptoms and pregnancy outcomes associated with extreme weight loss among women with hyperemesis gravidarum. J Womens Health (Larchmt) 18, 1981-1987.
24. Fox CS, Gona P, Larson MG, Selhub J, Tofler G, Hwang S-J et al (2010). A multi-marker approach to predict incident CKD and microalbuminuria. J Am Soc Nephrol 21, 2143-2149.
25. Gilbert JS, Lang AL, Grant AR & Nijland MJ (2005). Maternal nutrient restriction in sheep: hypertension and decreased nephron number in offspring at 9 months of age. J Physiol 565, 137-147.
26. Gleadhill A, Marlin D, Harris PA & Michell AR (1999). Use of a three-blood-sample plasma clearance technique to measure GFR in horses. Vet J 158, 204-209.
27. Gluckman PD, Hanson MA, Cooper C & Thornburg KL (2008). Effect of in utero and early-life conditions on adult health and disease. N Engl J Med 359, 61-73.
28. Gray SP, Kenna K, Bertram JF, Hoy WE, Yan EB, Bocking AD et al (2008). Repeated ethanol exposure during late gestation decreases nephron endowment in fetal sheep. Am J Physiol Regul Integr Comp Physiol 295, R568-R574.
29. Griffin KA, Kramer H & Bidani AK (2008). Adverse renal consequences of obesity. Am J Physiol Renal Physiol 294, F685-F696.
30. Grigore D, Ojeda NB & Alexander BT (2008). Sex differences in the fetal programming of hypertension. Gend Med 5, S121-S132.
31. Haraldsson B, Nystrom J & Deen WM (2008). Properties of the glomerular barrier and mechanisms of proteinuria. Physiol Rev 88, 451-487.
32. Hoppe CC, Evans RG, Moritz KM, Cullen-McEwen LA, Fitzgerald SM, Dowling J & Bertram JF (2006). Combined prenatal and postnatal protein restriction influences adult kidney structure, function, and arterial pressure. Am J Physiol Regul Integr Comp Physiol 292, R462-R469.
33. Hoy WE, Hughson MD, Bertram JF, Douglas-Denton R & Amann K (2005). Nephron number, hypertension, renal disease, and renal failure. J Am Soc Nephrol 16, 2557-2564.
34. Huang C, Li Z, Wang M & Martorell R (2010). Early life exposure to the 1959-1961 Chinese famine has long-term health consequences. J Nutr 140, 1874-1878.
35. Hughson M, Farris AB III, Douglas-Denton R, Hoy WE & Bertram JF (2003). Glomerular number and size in autopsy kidneys: The relationship to birth weight. Kidney Int 63, 2113-2122.
36. Huxley R, Neil A & Collins R (2002). Unravelling the fetal origins hypothesis: is there really an inverse association between birthweight and subsequent blood pressure? Lancet 360, 659-665.
37. Keller G, Zimmer G, Mall G, Ritz E & Amann K (2003). Nephron number in patients with primary hypertension. N Engl J Med 348, 101-108.
38. Kelly T, Yang W, Chen CS, Reynolds K & He J (2008). Global burden of obesity in 2005 and projections to 2030. Int J Obes 32, 1431-1437.
39. Kunkel PA (1930). The number and size of the glomeruli in the kidney of several mammals. Bulletin of the Johns Hopkins Hospital 47, 285-291.
40. Langley-Evans SC, Gardner DS & Jackson AA (1996). Association of disproportionate growth of fetal rats in late gestation with raised systolic blood pressure in later life. J Reprod Fertil 106, 307-312.
41. Law CM & Shiell AW (1996). Is blood pressure inversely related to birth weight? The strength of evidence from a systematic review of the literature. J Hypertens 14, 935-941.
42. Levy L & Jackson AA (1993). Modest restriction of dietary protein during pregnancy in the rat: fetal and placental growth. J Dev Physiol 19, 113-118.
43. Lysaght MJ (2002). Maintenance dialysis population dynamics: Current trends and long-term implications. J Am Soc Nephrol 13, S37-S40.
44. McCance RA & Widdowson EM (1986). Glimpses of comparative growth and development. In Developmental Biology and Prenatal Growth, ed. Falkner F & Tanner JM, pp. 133-151. Plenum Press, London
45. Mackenzie HS & Brenner BM (1995). Fewer nephrons at birth: a missing link in the etiology of essential hypertension? AmJ Kidney Dis 26, 91-98.
46. McMillen IC & Robinson JS (2005). Developmental origins of the metabolic syndrome: prediction, plasticity, and programming. Physiol Rev 85, 571-633.
47. McMullen S, Gardner DS & Langley-Evans SC (2004). Prenatal programming of angiotensin II type 2 receptor expression in the rat. Br J Nutr 91, 133-140.
48. McNamara BJ, Diouf B, Douglas-Denton RN, Hughson MD, Hoy WE & Bertram JF (2010). A comparison of nephron number, glomerular volume and kidney weight in Senegalese Africans and African Americans. Nephrol Dial Transplant 25, 1514-1520.
49. Manalich R, Reyes L, Herrera M, Melendi C & Fundora I (2000). Relationship between weight at birth and the number and size of renal glomeruli in humans: a histomorphometric study. Kidney Int 58, 770-773.
50. Moritz KM, Singh RR, Probyn ME & Denton KM (2009). Developmental programming of a reduced nephron endowment: more than just a baby's birth weight. Am J Physiol Renal Physiol 296, F1-F9.
51. Moritz KM & Wintour EM (1999). Functional development of the meso- and metanephros. Pediatr Nephrol 13, 171-178.
52. Narayan KMV, Ali MK & Koplan JP (2010). Global noncommunicable diseases - where worlds meet. N Engl J Med 363, 1196-1198.
53. Nehiri T, Duong Van Huyen J-P, Viltard M, Fassot C, Heudes D, Freund N et al (2008). Exposure to maternal diabetes induces salt-sensitive hypertension and impairs renal function in adult rat offspring. Diabetes 57, 2167-2175.
54. Ng S-F, Lin RCY, Laybutt DR, Barres R, Owens JA & Morris MJ (2010). Chronic high-fat diet in fathers programs β-cell dysfunction in female rat offspring. Nature 467, 963-966.
55. Ojeda NB, Grigore D & Alexander BT (2008). Intrauterine growth restriction: fetal programming of hypertension and kidney disease. Adv Chronic Kidney Dis 15, 101-106.
56. Painter RC, Roseboom TJ, van Montfrans GA, Bossuyt PM, Krediet RT, Osmond C et al (2005). Microalbuminuria in adults after prenatal exposure to the Dutch famine. J Am Soc Nephrol 16, 189-194.
57. Prynne CJ, Paul AA, Price GM, Day KC, Hilder WS & Wadsworth ME (1999). Food and nutrient intake of a national sample of 4-year-old children in 1950: comparison with the 1990s. Public Health Nutr 2, 537-547.
58. Puddu M, Fanos V, Podda F & Zaffanello M (2009). The kidney from prenatal to adult life: perinatal programming and reduction of number of nephrons during development. Am J Nephrol 30, 162-170.
59. Ravelli GP, Stein ZA & Susser MW (1976). Obesity in young men after famine exposure in utero and early infancy. N Engl J Med 295, 349-353.
60. Reilly RF & Perazella MA (2002). Chronic kidney disease: a new approach to an old problem. Conn Med 66, 579-583.
61. Rhodes P, Craigon J, Gray C, Rhind SM, Loughna PT & Gardner DS (2009). Adult-onset obesity reveals prenatal programming of glucose-insulin sensitivity in male sheep nutrient restricted during late gestation. PLoS One 4, e7393.
62. Roseboom TJ, van der Meulen JH, Ravelli AC, van Montfrans GA, Osmond C, Barker DJ & Bleker OP (1999). Blood pressure in adults after prenatal exposure to famine. J Hypertens 17, 325-330.
63. Sharkey D, Fainberg HP, Wilson V, Harvey E, Gardner DS, Symonds ME & Budge H (2009). Impact of early onset obesity and hypertension on the unfolded protein response in renal tissues of juvenile sheep. Hypertension 53, 925-931.
64. Simonetti GD, Raio L, Surbek D, Nelle M, Frey FJ & Mohaupt MG (2008). Salt sensitivity of children with low birth weight. Hypertension 52, 625-630.
65. Sinclair KD, Allegrucci C, Singh R, Gardner DS, Sebastian S, Bispham J et al (2007). DNA methylation, insulin resistance, and blood pressure in offspring determined by maternal periconceptional B vitamin and methionine status. Proc Natl Acad Sci U S A 104, 19351-19356.
66. Teeninga N, Schreuder MF, Bökenkamp A, Delemarre-van de Waal HA & van Wijk JA (2008). Influence of low birth weight on minimal change nephrotic syndrome in children, including a meta-analysis. Nephrol Dial Transplant 23, 1615-1620.
67. Tran S, Chen YW, Chenier I, Chan JSD, Quaggin S, Hebert MJ et al (2008). Maternal diabetes modulates renal morphogenesis in offspring. J Am Soc Nephrol 19, 943-952.
68. Vehaskari VM, Aviles DH & Manning J (2001). Prenatal programming of adult hypertension in the rat. Kidney Int 59, 238-245.
69. Veron D, Reidy KJ, Bertuccio C, Teichman J, Villegas G, Jimenez J et al (2010). Overexpression of VEGF-A in podocytes of adult mice causes glomerular disease. Kidney Int 77, 989-999.
70. Wang YC, McPherson K, Marsh T, Gortmaker SL & Brown M (2011). Health and economic burden of the projected obesity trends in the USA and the UK. Lancet 378, 815-825.
71. Welham SJ, Wade A & Woolf AS (2002). Protein restriction in pregnancy is associated with increased apoptosis of mesenchymal cells at the start of rat metanephrogenesis. Kidney Int 61, 1231-1242.
72. Whincup PH, Kaye SJ, Owen CG, Huxley R, Cook DG, Anazawa S et al (2008). Birth weight and risk of type 2 diabetes: a systematic review. JAMA 300, 2886-2897.
73. WHO (2011). Nutrition Landscape Information System. World Health Organisation.
74. Williams PJ, Kurlak LO, Perkins AC, Budge H, Stephenson T, Keisler D et al (2007). Hypertension and impaired renal function accompany juvenile obesity: the effect of prenatal diet. Kidney Int 73, 279-289.
75. Winearls CG & Glassock RJ (2009). Dissecting and refining the staging of chronic kidney disease. Kidney Int 75, 1009-1014.
76. Wintour EM & Moritz KM (1997). Comparative aspects of fetal renal development. Equine Vet J Suppl 24, 51-58.
77. Wood IS, de Heredia FP, Wang B & Trayhurn P (2009). Cellular hypoxia and adipose tissue dysfunction in obesity. Proc Nutr Soc 68, 370-377.
78. Woods LL, Weeks DA & Rasch R (2004). Programming of adult blood pressure by maternal protein restriction: role of nephrogenesis. Kidney Int 65, 1339-1348.
79. Zeman FJ (1967). Effect of the young rat of maternal protein restriction. J Nutr 93, 167-173.
80. Zimanyi MA, Hoy WE, Douglas-Denton RN, Hughson MD, Holden LM & Bertram JF (2009). Nephron number and individual glomerular volumes in male Caucasian and African American subjects. Nephrol Dial Transplant 24, 2428-2433.