Preview

Current Pediatrics

Advanced search

Kidney Disease and Perinatal Programming of Arterial Hypertension: the Results of Experimental Researches

https://doi.org/10.15690/vsp.v16i6.1820

Abstract

Deterioration of development conditions in the perinatal period (starvation of the mother, excess sodium ions in her diet, exposure to glucocorticosteroids, placental insufficiency) programs significant  changes in the excretion of sodium ions in the newborn and leads to the development of hypertension. Studies on experimental animals show  that unfavourable conditions of intrauterine development can reduce the effective area of glomerular filtration and its rate. These circumstances  increase the expression of membrane carriers of sodium ions in the  apical membranes, the production of superoxide radicals and enhance  the reabsorption of sodium. The article discusses the potential mechanisms of perinatal programming of renal hypertension in humans.

About the Authors

Olga P. Kovtun
Ural State Medical University
Russian Federation

Disclosure of interest:

confirmed the absence of a reportable conflict of interests



Pavel B. Tsyvian
Ural State Medical University Ural Research Institute for Maternal and Infant Childhood Protection
Russian Federation

Disclosure of interest:

during 2013–2015 was a recipient of grant from Russian  Foundation of Basic Research (RFBR) #13-04-96080 «Research of cardiovascular function regulation in human embryo and  fetus conceived by in vitro fertilization technology»



References

1. Guyton AC. The surprising kidney-fluid mechanism for pressure control — its infinite gain. Hypertension. 1990;16(6):725–730. doi: 10.1161/01.hyp.16.6.725

2. Mesquita FF, Gontijo JA, Boer PA. Expression of renin-angiotensin system signalling compounds in maternal protein-restricted rats: effect on renal sodium excretion and blood pressure. Nephrol Dial Transplant. 2010;25(2):380–388. doi: 10.1093/ndt/gfp505.

3. Barker DJ. The origins of the developmental origins theory. J Intern Med. 2007;261(5):412–417. doi: 10.1111/j.1365-2796.2007.01809.x.

4. Gluckman PD, Hanson MA, Cooper C, Thornburg KL. Effect of in utero and early-life conditions on adult health and disease. N Engl J Med. 2008;359(1):61–73. doi: 10.1056/NEJMra0708473.

5. Ojeda NB, Grigore D, Alexander BT. Developmental programming of hypertension insight from animal models of nutritional manipulation. Hypertension. 2008;52(1):44–50. doi: 10.1161/Hypertensionaha.107.092890.

6. Vehaskari VM, Woods LL. Prenatal programming of hypertension: lessons from experimental models. J Am Soc Nephrol. 2005;16(9):2545–2556. doi: 10.1681/Asn.2005030300.

7. Hoppe CC, Evans RG, Moritz KM, et al. Combined prenatal and postnatal protein restriction influences adult kidney structure, function, and arterial pressure. Am J Physiol Regul Integr Comp Physiol. 2007;292(1):R462–R469. doi: 10.1152/ajpregu.00079.2006.

8. Seckl JR, Holmes MC. Mechanisms of disease: glucocorticoids, their placental metabolism and fetal ‘programming’ of adult pathophysiology. Nat Clin Pract Endocrinol Metab. 2007;3(6): 479–488. doi: 10.1038/ncpendmet0515.

9. Celsi G, Kistner A, Aizman R, et al. Prenatal dexamethasone causes oligonephronia, sodium retention, and higher blood pressure in the offspring. Pediatr Res. 1998;44(3):317– 322. doi: 10.1203/00006450-199809000-00009.

10. O’Regan D, Kenyon CJ, Seckl JR, Holmes MC. Prenatal dexamethasone ‘programmes’ hypotension, but stress-induced hypertension in adult offspring. J Endocrinol. 2008;196(2): 343–352. doi: 10.1677/JOE-07-0327.

11. Ortiz LA, Quan A, Zarzar F, et al. Prenatal dexamethasone programs hypertension and renal injury in the rat. Hypertension. 2003;41(2):328–334. doi: 10.1161/01.hyp.0000049763.51269.51

12. Henriksen T, Clausen T. The fetal origins hypothesis: placental insufficiency and inheritance versus maternal malnutrition in well-nourished populations. Acta Obstet Gynecol Scand. 2002; 81(2):112–114. doi: 10.1034/j.1600-0412.2002.810204.x.

13. Alexander BT. Placental insufficiency leads to develop ment of hypertension in growth- restricted offspring. Hypertension. 2003;41(3):457–462. doi: 10.1161/01.Hyp.0000053448.95913.3d.

14. Contreras RJ, Wong DL, Henderson R, et al. High dietary NaCl early in development enhances mean arterial pressure of adult rats. Physiol Behav. 2000;71(1–2):173–181. doi: 10.1016/S0031-9384(00)00331-0.

15. Koleganova N, Piecha G, Ritz E, et al. Both high and low maternal salt intake in pregnancy alter kidney development in the offspring. Am J Physiol Renal Physiol. 2011;301(2):F344–F354. doi: 10.1152/ajprenal.00626.2010.

16. Meneton P, Jeunemaitre X, De Wardener HE, Macgregor GA. Links between dietary salt intake, renal salt handling, blood pressure, and cardiovascular diseases. Physiol Rev. 2005;85(2):679–715. doi: 10.1152/physrev.00056.2003.

17. Eriksson JG, Forsen T, Tuomilehto J, et al. Early growth and coronary heart disease in later life: longitudinal study. BMJ. 2001;322(7292):949–953. doi: 10.1136/bmj.322.7292.949.

18. Eriksson JG. Early growth and coronary heart disease and type 2 diabetes: findings from the Helsinki Birth Cohort Study (HBCS). Am J Clin Nutr. 2011;94(6):1799s–1802s. doi: 10.3945/ajcn.110.000638.

19. Mackenzie HS, Brenner BM. Fewer nephrons at birth — a missing link in the etiology of essential-hypertension. Am J Kidney Dis. 1995;26(1):91–98. doi: 10.1016/0272-6386(95)90161-2.

20. Jansson N, Pettersson J, Haafiz A, et al. Down-regulation of placental transport of amino acids precedes the development of intrauterine growth restriction in rats fed a low protein diet. J Physiol. 2006;576(Pt 3):935–946. doi: 10.1113/jphysiol.2006.116509.

21. Hughson M, Farris AB, 3rd, Douglas-Denton R, et al. Glomerular number and size in autopsy kidneys: the relationship to birth weight. Kidney Int. 2003;63(6):2113–2122. doi: 10.1046/j.1523-1755.2003.00018.x.

22. Woods LL, Ingelfinger JR, Nyengaard JR, Rasch R. Maternal protein restriction suppresses the newborn renin-angiotensin system and programs adult hypertension in rats. Pediatr Res. 2001;49(4): 460–467. doi: 10.1203/00006450-200104000-00005.

23. Wlodek ME, Westcott K, Siebel AL, et al. Growth restriction before or after birth reduces nephron number and increases blood pressure in male rats. Kidney Int. 2008;74(2):187–195. doi: 10.1038/ki.2008.153.

24. Brennan KA, Kaufman S, Reynolds SW, et al. Differential effects of maternal nutrient restriction through pregnancy on kidney development and later blood pressure control in the resulting offspring. Am J Physiol Regul Integr Comp Physiol. 2008;295(1):R197–R205. doi: 10.1152/ajpregu.00741.2007.

25. Ruta LA, Dickinson H, Thomas MC, et al. High-salt diet reveals the hypertensive and renal effects of reduced nephron endowment. Am J Physiol Renal Physiol. 2010;298(6):F1384–F1392. doi: 10.1152/ajprenal.00049.2010.

26. Solomon S. Developmental-changes in nephron number, proximal tubular length and superficial nephron glomerular-filtration rate of rats. J Physiol. 1977;272(3):573–589. doi: 10.1113/jphysiol.1977.sp012061.

27. Tufro-McReddie A, Romano LM, Harris JM, et al. Angiotensin-II regulates nephrogenesis and renal vascular development. Am J Physiol. 1995;269(1):F110–F115.

28. Saez F, Castells MT, Zuasti A, et al. Sex differences in the renal changes elicited by angiotensin II blockade during the nephrogenic period. Hypertension. 2007;49(6):1429– 1435. doi: 10.1161/Hypertensionaha.107.087957.

29. Петренко В.М. Развитие человека. Вопросы развития в анатомии человека. — М.- Берлин: Директ-Медиа; 2015. — 165 с. [Petrenko VМ. Razvitie cheloveka. Voprosy razvitiya v anatomii cheloveka. Moscow-Berlin: Direct-Media; 2015. 165 p. (In Russ).]

30. Quigley R. Developmental changes in renal function. Curr Opin Pediatr. 2912;24(2):184–190.

31. Sutherland MR, Gubhaju L, Moore L, et al. Accelerated maturation and abnormal morphology in the preterm neonatal kidney. J Am Soc Nephrol. 2011;22(7):1365–1374. doi: 10.1681/Asn.2010121266.

32. Coresh J, Selvin E, Stevens LA, et al. Prevalence of chronic kidney disease in the United States. JAMA. 2007;298(17):2038–2047. doi: 10.1001/jama.298.17.2038.

33. Szabo AJ, Muller V, Chen GF, et al. Nephron number determines susceptibility to renal mass reduction-induced CKD in Lewis and Fisher 344 rats: implications for development of experimentally induced chronic allograft nephropathy. Nephrol Dial Transplant. 2008;23(8):2492–2495. doi: 10.1093/ndt/gfn112.

34. Ojeda NB. Low birth weight increases susceptibility to renal injury in a rat model of mild ischemia-reperfusion. Am J Physiol Renal Physiol. 2011;301(2):F420–426. doi: 10.1152/ajprenal.00045.2011.

35. Woods LL, Weeks DA, Rasch R. Programming of adult blood pressure by maternal protein restriction: role of nephrogenesis. Kidney Int. 2004;65(4):1339–1348. doi: 10.1111/j.1523-1755.2004.00511.x.

36. Lelievre-Pegorier M, Vilar J, Ferrier ML, et al. Mild vitamin A deficiency leads to inborn nephron deficit in the rat. Kidney Int. 1998;54(5):1455–1462. doi: 10.1046/j.1523-1755.1998.00151.x.

37. Drake KA, Sauerbry MJ, Blohowiak SE, et al. Iron deficiency and renal development in the newborn rat. Pediatr Res. 2009;66(6): 619–624. doi: 10.1203/PDR.0b013e3181be79c2.

38. Abdel-Hakeem AK, Henry TQ, Magee TR, et al. Mechanisms of impaired nephrogenesis with fetal growth restriction: altered renal transcription and growth factor expression. Am J Obstet Gynecol. 2008;199(3):252 e251–257. doi: 10.1016/j.ajog.2008.05.018.

39. Casanovas Mdel C, Lutter CK, Mangasaryan N, et al. Multisectoral interventions for healthy growth. Matern Child Nutr. 2013;9 Suppl 2:46–57. doi: 10.1111/mcn.12082.

40. Woods LL, Ingelfinger JR, Rasch R. Modest maternal protein restriction fails to program adult hypertension in female rats. Am J Physiol Regul Integr Comp Physiol. 2005;289(4):R1131–1136. doi: 10.1152/ajpregu.00037.2003.

41. Iosipiv IV, Schroeder M. A role for angiotensin II AT1 receptors in ureteric bud cell branching. Am J Physiol Renal Physiol. 2003;285(2):F199–207. doi: 10.1152/ajprenal.00401.2002.

42. McMullen S, Langley-Evans SC. Sex-specific effects of prenatal low-protein and carbenoxolone exposure on renal angiotensin receptor expression in rats. Hypertension. 2005;46(6):1374–1380. doi: 10.1161/01.HYP.0000188702.96256.46.

43. Dickinson H, Walker DW, Wintour EM, Moritz K. Maternal dexamethasone treatment at midgestation reduces nephron number and alters renal gene expression in the fetal spiny mouse. Am J Physiol Regul Integr Comp Physiol. 2007;292(1):R453–R461. doi: 10.1152/ajpregu.00481.2006.

44. Tay SH, Blache D, Gregg K, Revell DK. Consumption of a high-salt diet by ewes during pregnancy alters nephrogenesis in 5-month-old offspring. Animal. 2012;6(11):1803–1810. doi: 10.1017/S1751731112000584.

45. Balbi AP, Costa RS, Coimbra TM. Postnatal renal development of rats from mothers that received increased sodium intake. Pediatr Nephrol. 2004;19(11):1212–1218. doi: 10.1007/s00467-004-1586-x.

46. Pham TD, MacLennan NK, Chiu CT, et al. Uteroplacental insufficiency increases apoptosis and alters p53 gene methylation in the full-term IUGR rat kidney. Am J Physiol Regul Integr Comp Physiol. 2003;285(5):R962–R970. doi: 10.1152/ajpregu.00201.2003.

47. Bauer R, Walter B, Brust P, et al. Impact of asymmetric intrauterine growth restriction on organ function in newborn piglets. Eur J Obstet Gynecol Reprod Biol. 2003;110:S40–S49. doi: 10.1016/S0301-2115(03)00171-4.

48. Crowley SD, Coffman TM. Recent advances involving the reninangiotensin system. Exp Cell Res. 2012;318(9):1049–1056. doi: 10.1016/j.yexcr.2012.02.023.

49. Vehaskari VM, Stewart T, Lafont D, et al. Kidney angiotensin and angiotensin receptor expression in prenatally programmed hypertension. Am J Physiol Renal Physiol. 2004;287(2):F262–267. doi: 10.1152/ajprenal.00055.2004.

50. Goyal R, Goyal D, Leitzke A, et al. Brain renin-angiotensin system: fetal epigenetic programming by maternal protein restriction during pregnancy. Reprod Sci. 2010;17(3):227–238. doi: 10.1177/1933719109351935.

51. Vehaskari VM, Aviles DH, Manning J. Prenatal programming of adult hypertension in the rat. Kidney Int. 2001;59(1):238-245. doi: 10.1046/j.1523-1755.2001.00484.x.

52. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell. 2009;136(2):215–233. doi: 10.1016/j.cell.2009.01.002.

53. Marin EC, Balbi AP, Francescato HD, et al. Renal structure and function evaluation of rats from dams that received increased sodium intake during pregnancy and lactation submitted or not to 5/6 nephrectomy. Ren Fail. 2008;30(5):547–555. doi: 10.1080/08860220802060448.

54. Bertram C, Trowern AR, Copin N, et al. The maternal diet during pregnancy programs altered expression of the glucocorticoid receptor and type 2 11 beta-hydroxysteroid dehydrogenase: potential molecular mechanisms underlying the programming of hypertension in utero. Endocrinology. 2001;142(7):2841–2853. doi: 10.1210/en.142.7.2841.

55. Feraille E, Doucet A. Sodium-potassium-adenosinetriphosphatase-dependent sodium transport in the kidney: hormonal control. Physiol Rev. 2001;81(1):345–418.

56. Dagan A, Kwon HM, Dwarakanath V, Baum M. Effect of renal denervation on prenatal programming of hypertension and renal tubular transporter abundance. Am J Physiol Renal Physiol. 2008;295(1):F29–F34. doi: 10.1152/ajprenal.00123.2008.

57. Cuffe JSM, Burgess DJ, O’Sullivan L, et al. Maternal corticosterone exposure in the mouse programs sex-specific renal adaptations in the renin–angiotensin–aldosterone system in 6-month offspring. Physiol Rep. 2016;4(8):e12754. doi: 10.14814/phy2.12754.

58. Muller FL, Lustgarten MS, Jang Y, et al. Trends in oxidative aging theories. Free Radic Biol Med. 2007;43(4):477–503. doi: 10.1016/j.freeradbiomed.2007.03.034.

59. Boubred F, Saint-Faust M, Buffat C, et al. Developmental origins of chronic renal disease: an integrative hypothesis. Int J Nephrol. 2013;2013:346067. doi: 10.1155/2013/346067.

60. Feng D, Yang C, Geurts AM, et al. Increased expression of NAD(P)H oxidase subunit p67(phox) in the renal medulla contributes to excess oxidative stress and salt-sensitive hypertension. Cell Metab. 2012;15(2):201–208. doi: 10.1016/j.cmet.2012.01.003.

61. Evans RG, Majid DS, Eppel GA. Mechanisms mediating pressure natriuresis: what we know and what we need to find out. Clin Exp Pharmacol Physiol. 2005;32(5–6):400–409. doi: 10.1111/j.1440-1681.2005.04202.x.

62. Deng A, Miracle CM, Suarez JM, et al. Oxygen consumption in the kidney: effects of nitric oxide synthase isoforms and angiotensin II. Kidney Int. 2005;68(2):723–730. doi: 10.1111/j.1523-1755.2005.00450.x.

63. Kawarazaki H, Ando K, Shibata S, et al. Mineralocorticoid receptor-Rac1 activation and oxidative stress play major roles in salt-induced hypertension and kidney injury in prepubertal rats. J Hypertens. 2012;30(10):1977–1985. doi: 10.1097/HJH.0b013e3283576904.

64. Vieira LD, Lara LS, Silva PA, et al. Placental malnutrition changes the regulatory network of renal Na-ATPase in adult rat progeny: reprogramming by maternal alpha-tocopherol during lactation. Arch Biochem Biophys. 2011;505(1):91–97. doi: 10.1016/j.abb.2010.09.025.

65. Ojeda NB, Hennington BS, Williamson DT, et al. Oxidative stress contributes to sex differences in blood pressure in adult growth-restricted offspring. Hypertension. 2012;60(1):114–122. doi: 10.1161/Hypertensionaha.112.192955.

66. Reverte V, Tapia A, Baile G, et al. Role of angiotensin II in arterial pressure and renal hemodynamics in rats with altered renal development: age- and sex-dependent differences. Am J Physiol Renal Physiol. 2013;304(1):F33–F40. doi: 10.1152/ajprenal.00424.2012.

67. Bhatia K, Elmarakby AA, El-Remessey A, Sullivan JC. Oxidative stress contributes to sex differences in angiotensin II-mediated hypertension in spontaneously hypertensive rats. Am J Physiol Regul Integr Comp Physiol. 2012;302(2):R274–R282. doi: 10.1152/ajpregu.00546.2011.

68. Rexhaj E, Bloch J, Jayet PY, et al. Fetal programming of pulmonary vascular dysfunction in mice: role of epigenetic mechanisms. Am J Physiol Heart Circ Physiol. 2011;301(1):H247– H252. doi: 10.1152/ajpheart.01309.2010.

69. Vieira LD, Cabral EV, Santos FTJ, et al. Alpha-tocopherol prevents intrauterine undernutrition-induced oligonephronia in rats. Pediatr Nephrol. 2011;26(11):2019–2029. doi: 10.1007/s00467-011-1908-8.

70. Li J, Khodus GR, Kruusmagi M, et al. Ouabain protects against adverse developmental programming of the kidney. Nat Commun. 2010;1(4):1–7. doi: 10.1038/ncomms1043.

71. Khodus GR, Kruusmagi M, Li J, et al. Calcium signaling triggered by ouabain protects the embryonic kidney from adverse developmental programming. Pediatr Nephrol. 2011;26(9): 1479–1482. doi: 10.1007/s00467-011-1816-y.

72. Roghair RD, Wemmie JA, Volk KA, et al. Maternal antioxidant blocks programmed cardiovascular and behavioural stress responses in adult mice. Clin Sci (Lond). 2011;121(10):427–436. doi: 10.1042/CS20110153.

73. An WS, Kim HJ, Cho KH, Vaziri ND. Omega-3 fatty acid supplementation attenuates oxidative stress, inflammation, and tubulointerstitial fibrosis in the remnant kidney. Am J Physiol Renal Physiol. 2009;297(4):F895–903. doi: 10.1152/ajprenal.00217.2009.

74. Baum M. Developmental changes in proximal tubule NaCl transport. Pediatr Nephrol. 2008;23(2):185–194. doi: 10.1007/s00467-007-0569-0.

75. Manning J, Vehaskari VM. Postnatal modulation of prenatally programmed hypertension by dietary Na and ACE inhibition. Am J Physiol Regul Integr Comp Physiol. 2005;288(1):R80– 84. doi: 10.1152/ajpregu.00309.2004.


Review

For citations:


Kovtun O.P., Tsyvian P.B. Kidney Disease and Perinatal Programming of Arterial Hypertension: the Results of Experimental Researches. Current Pediatrics. 2017;16(6):481-486. (In Russ.) https://doi.org/10.15690/vsp.v16i6.1820

Views: 938


ISSN 1682-5527 (Print)
ISSN 1682-5535 (Online)