Transgenerational programming of fetal nephron deficits and sex-specific adult hypertension in rats

Reproduction, Fertility and Development

Volumn 26, Issue 7, 2014, Pages 1032-1043

  Gallo, Linda A ^a,d   Tran, Melanie ^a   Cullen Mcewen, Luise A ^b   Denton, Kate M ^b   Jefferies, Andrew J ^a   Moritz, Karen M ^c   Wlodek, Mary E ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b MONASH UNIVERSITY   (Australia)

^c UNIVERSITY OF QUEENSLAND   (Australia)

^d TRANSLATIONAL RESEARCH INSTITUTE   (Australia)

Author keywords

fetal programming; intrauterine growth; pregnancy; sexual dimorphism

Indexed keywords

AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD PRESSURE; CONTROLLED STUDY; ELEVATED BLOOD PRESSURE; FEMALE; FETUS; FLUID INTAKE; FOOD INTAKE; GROWTH RATE; HYPERTENSION; KIDNEY DEVELOPMENT; KIDNEY FAILURE; KIDNEY FUNCTION; LOW BIRTH WEIGHT; MALE; MATERNAL STRESS; NEPHRON; NONHUMAN; ORGAN WEIGHT; PLACENTA INSUFFICIENCY; RAT; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; SODIUM EXCRETION; SYSTOLIC BLOOD PRESSURE; URINARY EXCRETION; UTERINE BLOOD VESSEL; ANIMAL; BODY WEIGHT; CONGENITAL MALFORMATION; EMBRYOLOGY; GROWTH, DEVELOPMENT AND AGING; INTRAUTERINE GROWTH RETARDATION; KIDNEY; NEWBORN; ORGAN SIZE; PATHOPHYSIOLOGY; PHYSIOLOGY; PLACENTA CIRCULATION; PREGNANCY; SEX DIFFERENCE; UTERUS; VASCULARIZATION; WISTAR KYOTO RAT;

ANIMALS; ANIMALS, NEWBORN; BODY WEIGHT; FEMALE; FETAL GROWTH RETARDATION; HYPERTENSION; KIDNEY; MALE; NEPHRONS; ORGAN SIZE; PLACENTAL CIRCULATION; PLACENTAL INSUFFICIENCY; PREGNANCY; RATS; RATS, INBRED WKY; RENIN-ANGIOTENSIN SYSTEM; SEX FACTORS; UTERUS;

EID: 84907360758     PISSN: 10313613     EISSN: 14485990     Source Type: Journal    
DOI: 10.1071/RD13133     Document Type: Article

References (49)

1. Anderson, C. M., Lopez, F., Zimmer, A., and Benoit, J. N. (2006). Placental insufficiency leads to developmental hypertension and mesenteric artery dysfunction in two generations of Sprague-Dawley rat offspring. Biol. Reprod. 74, 538-544. doi:10.1095/BIOLREPROD.105.045807
2. Armitage, J. A., Khan, I. Y., Taylor, P. D., Nathanielsz, P. W., and Poston, L. (2004). Developmental programming of the metabolic syndrome by maternal nutritional imbalance: how strong is the evidence from experimental models in mammals? J. Physiol. 561, 355-377. doi:10.1113/ JPHYSIOL.2004.072009
3. Barker, D. J. P. (1995). Fetal origins of coronary heart disease. BMJ 311, 171-174. doi:10.1136/BMJ.311.6998.171
4. Barker, D. J., Winter, P. D., Osmond, C., Margetts, B., and Simmonds, S. J. (1989). Weight in infancy and death from ischaemic heart disease. Lancet 334, 577-580. doi:10.1016/S0140-6736(89)90710-1
5. Ben-Shlomo, Y., McCarthy, A., Hughes, R., Tilling, K., Davies, D., and Smith, G. D. (2008). Immediate postnatal growth is associated with blood pressure in young adulthood: the Barry Caerphilly Growth Study. Hypertension 52, 638-644. doi:10.1161/HYPERTENSIONAHA.108. 114256
6. Bertram, J. F. (1995). Analysing renal glomeruli with the new stereology. Int. Rev. Cytol. 161, 111-172. doi:10.1016/S0074-7696(08)62497-3
7. Brawley, L., Itoh, S., Torrens, C., Barker, A., Bertram, C., Poston, L., and Hanson, M. (2003). Dietary protein restriction in pregnancy induces hypertension and vascular defects in rat male offspring. Pediatr. Res. 54, 83-90. doi:10.1203/01.PDR.0000065731.00639.02
8. Brenner, B. M., Garcia, D. L., and Anderson, S. (1988). Glomeruli and blood pressure. Less of one, more the other? Am. J. Hypertens. 1, 335-347. doi:10.1093/AJH/1.4.335
9. Cullen-McEwen, L. A., Armitage, J. A., Nyengaard, J. R., and Moritz, K. M. (2011). A design-based method for estimating glomerular number in the developing kidney. Am. J. Physiol. Renal Physiol. 300, F1448-F1453.
10. Cullen-McEwen, L. A., Armitage, J. A., Nyengaard, J. R., and Bertram, J. F. (2012). Estimating nephron number in the developing kidney using the physical dissector/fractionator combination. Methods Mol. Biol. 886, 109-119. doi:10.1007/978-1-61779-851-1-10
11. Denton, K., and Baylis, C. (2007). Physiological and molecular mechanisms governing sexual dimorphism of kidney, cardiac and vascular function. Am. J. Physiol. Regul. Integr. Comp. Physiol. 292, R697-R699.
12. Eriksson, J., Forsen, T., Tuomilehto, J., Osmond, C., and Barker, D. (2000). Fetal and childhood growth and hypertension in adult life. Hypertension 36, 790-794. doi:10.1161/01.HYP.36.5.790
13. Eriksson, J. G., Forsén, T., Tuomilehto, J., Osmond, C., and Barker, D. J. P. (2001). Early growth and coronary heart disease in later life: longitudinal study. BMJ 322, 949. doi:10.1136/BMJ.322.7292.949
14. Gallo, L. A., Denton, K. M., Moritz, K. M., Tare, M., Parkington, H. C., Davies, M., Tran, M., Jefferies, A. J., and Wlodek, M. E. (2012a). Longterm alteration in maternal blood pressure and renal function after pregnancy in normal and growth-restricted rats. Hypertension 60, 206-213. doi:10.1161/HYPERTENSIONAHA.112.195578
15. Gallo, L. A., Tran, M., Master, J. S., Mortiz, K. M., and Wlodek, M. E. (2012b). Maternal adaptations and inheritance in the transgenerational programming of adult disease. Cell Tissue Res. 349, 863-880. doi:10.1007/S00441-012-1411-Y
16. Gallo, L. A., Tran, M., Moritz, K. M., Jefferies, A. J., and Wlodek, M. E. (2012c). Pregnancy in aged rats that were born small: cardio-renal and metabolic adaptations and second-generation fetal growth. FASEB J. 26, 4337-4347. doi:10.1096/FJ.12-210401
17. Gallo, L. A., Tran, M., Moritz, K. M., Mazzuca, M. Q., Parry, L. J., Westcott, K. T., Jefferies, A. J., Cullen-McEwen, L. A., and Wlodek, M. E. (2012d). Cardio-renal and metabolic adaptations during pregnancy in female rats born small: implications for maternal health and secondgeneration fetal growth. J. Physiol. 590, 617-630.
18. Giussani, D. A., Fletcher, A. J., and Gardner, D. S. (2011). Sex differences in the ovine fetal cortisol response to stress. Pediatr. Res. 69, 118-122. doi:10.1203/PDR.0B013E3182042A20
19. Grigore, D., Ojeda, N. B., Robertson, E. B., Dawson, A. S., Huffman, C. A., Bourassa, E. A., Speth, R. C., Brosnihan, K. B., and Alexander, B. T. (2007). Placental insufficiency results in temporal alterations in the renin-angiotensin system in male hypertensive growth restricted offspring. Am. J. Physiol. Regul. Integr. Comp. Physiol. 293, R804-R811.
20. Grigore, D., Ojeda, N. B., and Alexander, B. T. (2008). Sex differences in the fetal programming of hypertension. Gend. Med. 5, S121-S132. doi:10.1016/J.GENM.2008.03.012
21. Gubhaju, L., Sutherland, M. R., Yoder, B. A., Zulli, A., Bertram, J. F., and Black, M. J. (2009). Is nephrogenesis affected by preterm birth? Studies in a non-human primate model. Am. J. Physiol. Renal Physiol. 297, F1668-F1677.
22. Hanson, M., and Gluckman, P. (2005). Endothelial dysfunction and cardiovascular disease: the role of predictive adaptive responses. Heart 91, 864-866. doi:10.1136/HRT.2004.047381
23. Harrison, M., and Langley-Evans, S. C. (2009). Intergenerational programming of impaired nephrogenesis and hypertension in rats following maternal protein restriction during pregnancy. Br. J. Nutr. 101, 1020-1030. doi:10.1017/S0007114508057607
24. Henriksen, T., and Clausen, T. (2002). The fetal origins hypothesis: placental insufficiency and inheritance versus maternal malnutrition in well-nourished populations. Acta Obstet. Gynecol. Scand. 81, 112-114. doi:10.1034/J.1600-0412.2002.810204.X
25. Hoy, W. E., Rees, M., Kile, E., Mathews, J. D., and Wang, Z. (1999). A new dimension to the Barker hypothesis: low birthweight and susceptibility to renal disease. Kidney Int. 56, 1072-1077. doi:10.1046/J.1523-1755. 1999.00633.X
26. Hoy, W. E., Hughson, M. D., Bertram, J. F., Denton, D. R., and Amann, K. (2005). Nephron number, hypertension, renal disease and renal failure. J. Am. Soc. Nephrol. 16, 2557-2564. doi:10.1681/ASN.2005020172
27. Lim, K., Armitage, J. A., Stefanidis, A., Oldfield, B. J., and Black, M. J. (2011). IUGR in the absence of postnatal ''catch-up'' growth leads to improved whole body insulin sensitivity in rat offspring. Pediatr. Res. 70, 339-344. doi:10.1203/PDR.0B013E31822A65A3
28. Mazzuca, M. Q., Tare, M., Parkington, H. C., Dragomir, N. M., Parry, L. J., and Wlodek, M. E. (2012). Utero-placental insufficiency programmes vascular dysfunction in non-pregnant rats: compensatory adaptations in pregnancy. J. Physiol. 590, 3375-3388. doi:10.1113/JPHYSIOL.2012. 230011
29. Mercuro, G., Deidda, M., Piras, A., Dessalvi, C. C., Maffei, S., and Rosano, G. M. (2010). Gender determinants of cardiovascular risk factors and diseases. J. Cardiovasc. Med. 11, 207-220. doi:10.2459/JCM. 0B013E32833178ED
30. Moritz, K. M., Mazzuca, M. Q., Siebel, A. L., Mibus, A., Arena, D., Tare, M., Owens, J. A., and Wlodek, M. E. (2009). Utero-placental insufficiency causes a nephron deficit, modest renal insufficiency but no hypertension with ageing in female rats. J. Physiol. 587, 2635-2646. doi:10.1113/ JPHYSIOL.2009.170407
31. O'Dowd, R., Kent, J. C., Moseley, J. M., and Wlodek, M. E. (2008). Effects of utero-placental insufficiency and reducing litter size on maternal mammary function and postnatal offspring growth. Am. J. Physiol. Regul. Integr. Comp. Physiol. 294, R539-R548.
32. Ojeda, N. B., Grigore, D., Robertson, E. B., and Alexander, B. T. (2007a). Oestrogen protects against increased blood pressure in postpubertal female growth-restricted offspring. Hypertension 50, 679-685. doi:10.1161/HYPERTENSIONAHA.107.091785
33. Ojeda,N. B.,Grigore,D.,Yanes, L.L., Iliescu,R., Robertson, E. B.,Zhang,H., and Alexander, B. T. (2007b). Testosterone contributes to marked elevations in mean arterial pressure in adult male intrauterine growthrestricted offspring. Am. J. Physiol. Regul. Integr. Comp. Physiol. 292, R758-R763.
34. Painter, R. C., Osmond, C., Gluckman, P., Hanson, M., Phillips, D. I., and Roseboom, T. J. (2008). Transgenerational effects of prenatal exposure to the Dutch famine on neonatal adiposity and health in later life. BJOG 115, 1243-1249. doi:10.1111/J.1471-0528.2008.01822.X
35. Ponzio, B. F., Carvalho, M. H., Fortes, Z. B., and do Carmo, F. M. (2012). Implications of maternal nutrient restriction in transgenerational programming of hypertension and endothelial dysfunction across F1-F3 offspring. Life Sci. 90, 571-577. doi:10.1016/J.LFS.2012.01.017
36. Roseboom, T. J., and Watson, E. D. (2012). The next generation of disease risk: are the effects of prenatal nutrition transmitted across generations? Evidence from animal and human studies. Placenta 33(Suppl 2), e40-e44. doi:10.1016/J.PLACENTA.2012.07.018
37. Schreuder, M. F., Van Wijk, J. A., Fodor, M., and Delemarre-van de Waal, H. A. (2007). Influence of intrauterine growth restriction on renal function in the adult rat. J. Physiol. Biochem. 63, 213-219. doi:10.1007/BF03165784
38. Simmons, R. A., Templeton, L. J., and Gertz, S. J. (2001). Intrauterine growth retardation leads to the development of Type 2 diabetes in the rat. Diabetes 50, 2279-2286. doi:10.2337/DIABETES.50.10.2279
39. Singh, R. R., Moritz, K. M., Wintour, E. M., Jefferies, A. J., Iqbal, J., Bertram, J. F., and Denton, K. M. (2011). Fetal uninephrectomy in male sheep alters the systemic and renal responses to angiotensin II infusion and AT1R blockade. Am. J. Physiol. Renal Physiol. 301, F319-F326.
40. Torrens, C., Brawley, L., Barker, A. C., Itoh, S., Poston, L., and Hanson, M. A. (2003). Maternal protein restriction in the rat impairs resistance artery but not conduit artery function in pregnant offspring. J. Physiol. 547, 77-84. doi:10.1113/JPHYSIOL.2002.026120
41. Torrens, C., Poston, L., and Hanson, M. A. (2008). Transmission of raised blood pressure and endothelial dysfunction to the F2 generation induced by maternal protein restriction in the F0, in the absence of dietary challenge in the F1 generation. Br. J. Nutr. 100, 760-766. doi:10.1017/ S0007114508921747
42. Vehaskari, V. M. (2010). Prenatal programming of kidney disease. Curr. Opin. Pediatr. 22, 176-182. doi:10.1097/MOP.0B013E328336EBC9
43. Vehaskari, V. M., Aviles, D. H., and Manning, J. (2001). Prenatal programming of adult hypertension in the rat. Kidney Int. 59, 238-245. doi:10.1046/J.1523-1755.2001.00484.X
44. Vehaskari, V.M., Stewart, T., Lafont,D., Soyez, C., Seth, D., and Manning, J. (2004). Kidney angiotensin and angiotensin receptor expression in prenatally programmed hypertension. Am. J. Physiol. Renal Physiol. 287, F262-F267.
45. Vikse, B. E., Irgens, L. M., Leivestad, T., Hallan, S., and Iversen, B. M. (2008). Low birthweight increases risk for end-stage renal disease. J. Am. Soc. Nephrol. 19, 151-157. doi:10.1681/ASN.2007020252
46. Wadley, G. D., Siebel, A. L., Cooney, G. J., McConell, G. K., Wlodek, M. E., and Owens, J. A. (2008). Utero-placental insufficiency and reducing litter size alters skeletal muscle mitochondrial biogenesis in a sexspecific manner in the adult rat. Am. J. Physiol. Endocrinol. Metab. 294, E861-E869.
47. Wlodek, M. E., Mibus, A., Tan, A., Siebel, A. L., Owens, J. A., and Moritz, K. M. (2007). Normal lactational environment restores nephron endowment and prevents hypertension after placental restriction in the rat. J. Am. Soc. Nephrol. 18, 1688-1696. doi:10.1681/ASN.2007010015
48. Wlodek, M. E., Westcott, K., Siebel, A. L., Owens, J. A., and Moritz, K. M. (2008). Growth restriction before or after birth reduces nephron number and increases blood pressure in male rats. Kidney Int. 74, 187-195. doi:10.1038/KI.2008.153
49. Zimanyi, M. A., Denton, K. M., Forbes, J. M., Thallas-Bonke, V., Thomas, M. C., Poon, F., and Black, M. J. (2006). A developmental nephron deficit in rats is associated with increased susceptibility to a secondary renal injury due to advanced glycation end-products. Diabetologia 49, 801-810. doi:10.1007/S00125-006-0175-X