Prenatal betamethasone exposure alters renal function in immature sheep: Sex differences in effects

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 299, Issue 3, 2010, Pages

  Tang, Lijun ^a   Bi, Jianli ^a   Valego, Nancy ^a   Carey, Luke ^a   Figueroa, Jorge ^a   Chappell, Mark ^a   Rose, James C ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

Angiotensin (1 7); Glomerular filtration rate; Na excretion; Na load; Prenatal steroid exposure

Indexed keywords

ANGIOTENSIN[1-7]; BETAMETHASONE ACETATE PLUS BETAMETHASONE SODIUM PHOSPHATE; BETAMETHASONE; GLUCOCORTICOID; POTASSIUM; SODIUM;

ANIMAL EXPERIMENT; ARTICLE; BLOOD PRESSURE; CONTROLLED STUDY; EWE; FEMALE; GESTATION PERIOD; GLOMERULUS FILTRATION RATE; KIDNEY BLOOD FLOW; KIDNEY FUNCTION; MALE; NATRIURESIS; NONHUMAN; PRENATAL DRUG EXPOSURE; PRIORITY JOURNAL; PROGENY; RAM (SHEEP); RISK ASSESSMENT; SEX DIFFERENCE; SODIUM EXCRETION; SODIUM LOAD; ANIMAL; BLOOD; CONTROLLED CLINICAL TRIAL; DRUG EFFECTS; KIDNEY; METABOLISM; PHYSIOLOGY; PREGNANCY; PRENATAL EXPOSURE; SEXUAL DEVELOPMENT; SEXUAL MATURATION; SHEEP; URINE;

ANIMALS; BETAMETHASONE; BLOOD PRESSURE; FEMALE; GLUCOCORTICOIDS; KIDNEY; MALE; POTASSIUM; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; SEX CHARACTERISTICS; SEXUAL MATURATION; SHEEP; SODIUM;

EID: 77956705405     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00590.2009     Document Type: Article

References (61)

1. Armando I, Jezova M, Juorio AV, Terron JA, Falcon-Neri A, Semino-Mora C, Imboden H, Saavedra JM. Estrogen upregulates renal angiotensin II AT(2) receptors. Am J Physiol Renal Physiol 283: F934-F943, 2002. (Pubitemid 35192459)
2. Barker DJP, Fall CHD. Fetal and infant origins of cardiovascular disease. Arch Dis Child 68: 797-799, 1993. (Pubitemid 23199873)
3. Baum M. Role of the kidney in the prenatal and early postnatal programming of hypertension. Am J Physiol Renal Physiol 298: F235-F247, 2010.
4. Baylis C. Sexual dimorphism, the aging kidney, and involvement of nitric oxide deficiency. Semin Nephrol 29: 569-578, 2009.
5. Baylis C, Corman B. The aging kidney: insights from experimental studies. J Am Soc Nephrol 9: 699-709, 1998. (Pubitemid 28186060)
6. Baylis C. Sexual dimorphism of the aging kidney: role of nitric oxide deficiency. Physiology 23: 142-150, 2008.
7. Bloomfield FH, Oliver MH, Hawkins P, Holloway AC, Campbell M, Gluckman PD, Harding JE, Challis JR. Periconceptional undernutrition in sheep accelerates maturation of the fetal hypothalamic-pituitary-adrenal axis in late gestation. Endocrinology 145: 4278-4285, 2004. (Pubitemid 39120577)
8. Brandes RP, Fleming I, Busse R. Endothelial aging. Cardiovasc Res 66: 286-294, 2005.
9. Brandon AE, Boyce AC, Lumbers ER, Zimanyi MA, Bertram JF, Gibson KJ. Glomerular hypertrophy in offspring of subtotally nephrectomized ewes. Anat Rec (Hoboken) 291: 318-324, 2008.
10. Brenner BM, Chertow GM. Congenital oligonephropathy and the etiology of adult hypertension and progressive renal injury. Am J Kidney Dis 23: 171-175, 1994.
11. Chacko M, Fordtran JS, Emmett M. Effect of mineralocorticoid activity on transtubular potassium gradient, urinary [K]/[Na] ratio, and fractional excretion of potassium. Am J Kidney Dis 32: 47-51, 1998. (Pubitemid 28311870)
12. + exchanger by dexamethasone. Am J Physiol Regul Integr Comp Physiol 292: R1230-R1235, 2007.
13. Davidson WD, Sackner MA. Simplification of the anthrone method for the deternination of inulin in clearance studies. J Lab Clin Med 62: 351-356, 1963.
14. Dilauro M, Burns KD. Angiotensin-(1-7) and its effects in the kidney. Sci World J 9: 522-535, 2009.
15. Dodic M, Abouantoun T, O'Connor A, Wintour EM, Moritz KM. Programming effects of short prenatal exposure to dexamethasone in sheep. Hypertension 40: 729-734, 2002. (Pubitemid 35278611)
16. Dodic M, May CN, Wintour EM, Coghlan JP. An early prenatal exposure to excess glucocorticoid leads to hypertensive offspring in sheep. Clin Sci (Lond) 94: 149-155, 1998. (Pubitemid 28052645)
17. Doyle LW, Ford GW, Davis NM, Callanan C. Antenatal corticosteroid therapy and blood pressure at 14 years of age in preterm children. Clin Sci (Lond) 98: 137-142, 2000. (Pubitemid 30105520)
18. Ferrario CM, Chappell MC, Dean RH, Iyer SN. Novel angiotensin peptides regulate blood pressure, endothelial function, and natriuresis. J Am Soc Nephrol 9: 1716-1722, 1998.
19. Figueroa JP, Rose JC, Massmann GA, Zhang J, Acuna G. Alterations in fetal kidney development and elevations in arterial blood pressure in young adult sheep after clinical doses of antenatal glucocorticoids. Pediatr Res 58: 510-515, 2005. (Pubitemid 41254516)
20. Gilbert JS, Nijland MJ. Sex differences in the developmental origins of hypertension and cardiorenal disease. Am J Physiol Regul Integr Comp Physiol 295: R1941-R1952, 2008.
21. Grigore D, Ojeda NB, Alexander BT. Sex differences in the fetal programming of hypertension. Gender Med 5: S121-S132, 2008. (Pubitemid 351455237)
22. Gwathmey-Williams T, Shaltout HA, Diz DI, Figueroa JP, Rose JC, Chappell MC. Steroid-induced fetal programming alters angiotensin II receptor subtype expression in the sheep kidney. FASEB J 22: 735-735.15, 2008.
23. Hagenfeldt Y, Eriksson HA. The estrogen receptor in the rat kidney. Ontogeny, properties and effects of gonadectomy on its concentration. J Steroid Biochem 31: 49-56, 1988.
24. Hall JE, Guyton AC, Smith MJ Jr., Coleman TG. Blood pressure and renal function during chronic changes in sodium intake: role of angiotensin. Am J Physiol Renal Fluid Electrolyte Physiol 239: F271-F280, 1980.
25. Handa RK, Ferrario CM, Strandhoy JW. Renal actions of angiotensin-(1-7): in vivo and in vitro studies. Am J Physiol Renal Fluid Electrolyte Physiol 270: F141-F147, 1996. (Pubitemid 26055243)
26. Harrison-Bernard LM, Schulman IH, Raij L. Postovariectomy hypertension is linked to increased renal AT1 receptor and salt sensitivity. Hypertension 42: 1157-1163, 2003. (Pubitemid 37549071)
27. Heller J, Kramer HJ, Maly J, Cervenka L, Horacek V. Effect of intrarenal infusion of angiotensin-(1-7) in the dog. Kidney Blood Press Res 23: 89-94, 2000. (Pubitemid 30175627)
28. Jung K, Klotzek S, Schulze BD. Refinements of assays for low concentrations of inulin in serum. Nephron 54: 360-361, 1990. (Pubitemid 20097886)
29. Loria A, Reverte V, Salazar F, Saez F, Llinas MT, Salazar FJ. Sex and age differences of renal function in rats with reduced ANG II activity during the nephrogenic period. Am J Physiol Renal Physiol 293: F506-F510, 2007.
30. Mahon JM, Carr RD, Nicol AK, Henderson IW. Angiotensin(1-7) is an antagonist at the type 1 angiotensin II receptor. J Hypertens 12: 1377-1381, 1994.
31. Matz RL, Andriantsitohaina R. Age-related endothelial dysfunction : potential implications for pharmacotherapy. Drugs Aging 20: 527-550, 2003.
32. Miller JA, Anacta LA, Cattran DC. Impact of gender on the renal response to angiotensin II. Kidney Int 55: 278-285, 1999.
33. Moritz KM, Dodic M, Wintour EM. Kidney development and the fetal programming of adult disease. Bioessays 25: 212-220, 2003.
34. NIH Consensus Development Panel. NIH Consensus Development Conference 1995 Effects of corticosteroid for fetal maturation on perinatal outcomes. JAMA 273: 413-418, 1995.
35. Orlando R, Floreani M, Padrini R, Palatini P. Determination of inulin clearance by bolus intravenous injection in healthy subjects and ascitic patients: equivalence of systemic and renal clearances as glomerular filtration markers. Br J Clin Pharmacol 46: 605-609, 1998.
36. Ortiz LA, Quan A, Weinberg A, Baum M. Effect of prenatal dexamethasone on rat renal development. Kidney Int 59: 1663-1669, 2001.
37. Ortiz LA, Quan A, Zarzar F, Weinberg A, Baum M. Prenatal dexamethasone programs hypertension and renal injury in the rat. Hypertension 41: 328-334, 2003.
38. Osei SY, Ahima RS, Minkes RK, Weaver JP, Khosla MC, Kadowitz PJ. Differential responses to angiotensin-(1-7) in the feline mesenteric and hindquarters vascular beds. Eur J Pharmacol 234: 35-42, 1993.
39. Pinheiro SV, Ferreira AJ, Kitten GT, da Silveira KD, da Silva DA, Santos SH, Gava E, Castro CH, Magalhaes JA, da Mota RK, Botelho- Santos GA, Bader M, Alenina N, Santos RA, Simoes e Silva AC. Genetic deletion of the angiotensin-(1-7) receptor Mas leads to glomerular hyperfiltration and microalbuminuria. Kidney Int 75: 1184-1193, 2009.
40. Redgrave J, Rabinowe S, Hollenberg NK, Williams GH. Correction of abnormal renal blood flow response to angiotensin II by converting enzyme inhibition in essential hypertensives. J Clin Invest 75: 1285-1290, 1985.
41. Ren Y, Garvin JL, Carretero OA. Vasodilator action of angiotensin-(1-7) on isolated rabbit afferent arterioles. Hypertension 39: 799-802, 2002.
42. Salazar F, Reverte V, Saez F, Loria A, Llinas MT, Salazar FJ. Age- and sodium-sensitive hypertension and sex-dependent renal changes in rats with a reduced nephron number. Hypertension 51: 1184-1189, 2008.
43. Sampaio WO, Nascimento AA, Santos RA. Systemic and regional hemodynamic effects of angiotensin-(1-7) in rats. Am J Physiol Heart Circ Physiol 284: H1985-H1994, 2003.
44. Sampaio WO, Souza Dos Santos RA, Faria-Silva R, da Mata Machado LT, Schiffrin EL, Touyz RM. Angiotensin-(1-7) through receptor Mas mediates endothelial nitric oxide synthase activation via Akt-dependent pathways. Hypertension 49: 185-192, 2007.
45. Sandgaard NC, Andersen JL, Bie P. Hormonal regulation of renal sodium and water excretion during normotensive sodium loading in conscious dogs. Am J Physiol Regul Integr Comp Physiol 278: R11-R18, 2000.
46. Schnurr E, Lahme W, Kuppers H. Measurement of renal clearance of inulin and PAH in the steady state without urine collection. Clin Nephrol 13: 26-29, 1980. (Pubitemid 10139745)
47. Shaltout HA, Figueroa JP, Rose JC, Chappell MC, Averill DB and Diz DI. Deleterious cardiovascular effects of antenatal betamethasone exposure in young and adult sheep. FASEB J 22: 1129.16, 2008.
48. Shaltout HA, Figueroa JP, Rose JC, Diz DI, Chappell MC. Alterations in circulatory and renal angiotensin-converting enzyme and angiotensin-converting enzyme 2 in fetal programmed hypertension. Hypertension 53: 404-408, 2009.
49. Shaltout HA, Westwood BM, Averill DB, Ferrario CM, Figueroa JP, Diz DI, Rose JC, Chappell MC. Angiotensin metabolism in renal proximal tubules, urine, and serum of sheep: evidence for ACE2-dependent processing of angiotensin II. Am J Physiol Renal Physiol 292: F82-F91, 2007.
50. Silbiger S, Neugarten J. Gender and human chronic renal disease. Gender Med 5: S3-S10, 2008. (Pubitemid 351455227)
51. Singh RR, Denton KM, Bertram JF, Jefferies AJ, Head GA, Lombardo P, Schneider-Kolsky M, Moritz KM. Development of cardiovascular disease due to renal insufficiency in male sheep following fetal unilateral nephrectomy. J Hypertens 27: 386-396, 2009.
52. Sion-Vardi N, Kaneti J, Segal-Abramson T, Giat J, Levy J, Sharoni Y. Gonadotropin-releasing hormone specific binding sites in normal and malignant renal tissue. J Urol 148: 1568-1570, 1992.
53. Smith J, Nakahara S, Westwood B, Figueroa J, Chappell M, Rose JC. Prenatal betamethasone exposure alters renin angiotensin system enzyme expression in adult male sheep. Reprod Sci 15: 274A, 2008.
54. Souza Dos Santos RA, Passaglio KT, Pesquero JB, Bader M, Simoes e Silva AC. Interactions between angiotensin-(1-7), kinins, and angiotensin II in kidney and blood vessels. Hypertension 38: 660-664, 2001.
55. Tang L, Carey LC, Bi J, Valego N, Sun X, Deibel P, Perrott J, Figueroa JP, Chappell MC, Rose JC. Gender differences in the effects of antenatal betamethasone exposure on renal function in adult sheep. Am J Physiol Regul Integr Comp Physiol 296: R309-R317, 2009.
56. Vallon V, Richter K, Heyne N, Osswald H. Effect of intratubular application of angiotensin 1-7 on nephron function. Kidney Blood Press Res 20: 233-239, 1997. (Pubitemid 27487509)
57. Velazquez H, Bartiss A, Bernstein P, Ellison DH. Adrenal steroids stimulate thiazide-sensitive NaCl transport by rat renal distal tubules. Am J Physiol Renal Fluid Electrolyte Physiol 270: F211-F219, 1996. (Pubitemid 26055253)
58. Wintour EM, Moritz KM, Johnson K, Ricardo S, Samuel CS, Dodic M. Reduced nephron number in adult sheep, hypertensive as a result of prenatal glucocorticoid treatment. J Physiol 549: 929-935, 2003. (Pubitemid 36889780)
59. Wood RI, Foster DL. Sexual differentiation of reproductive neuroendocrine function in sheep. Rev Reprod 3: 130-140, 1998.
60. Woods LL, Weeks DA, Rasch R. Programming of adult blood pressure by maternal protein restriction: role of nephrogenesis. Kidney Int 65: 1339-1348, 2004. (Pubitemid 38406972)
61. Zhang J, Massman GA, Rose JC, Figueroa JP. Differential effects of a clinical dose of betamethasone on nephron endowment and glomerular filtration in adult sheep. Reprod Sci 17: 186-195, 2009.