Uteroplacental insufficiency alters nephrogenesis and downregulates cyclooxygenase-2 expression in a model of IUGR with adult-onset hypertension

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 292, Issue 5, 2007, Pages

  Baserga, Mariana ^a   Hale, Merica A ^a   Zheng, Ming Wang ^a   Yu, Xing ^a   Callaway, Christopher W ^a   McKnight, Robert A ^a   Lane, Robert H ^a  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

11 hydroxysteroid dehydrogenase type 2; Glucocorticoid receptor; Mineralocorticoid receptor

Indexed keywords

11BETA HYDROXYSTEROID DEHYDROGENASE; 11BETA HYDROXYSTEROID DEHYDROGENASE TYPE 2; CORTICOSTERONE; CYCLOOXYGENASE 2; DEHYDROCORTICOSTERONE; GLUCOCORTICOID; GLUCOCORTICOID RECEPTOR; MESSENGER RNA; MINERALOCORTICOID RECEPTOR; UNCLASSIFIED DRUG;

ADOLESCENT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CONTROLLED STUDY; DIASTOLIC BLOOD PRESSURE; DISEASE PREDISPOSITION; DOWN REGULATION; ENZYME LOCALIZATION; FEMALE; FETUS; HYPERTENSION; IMMUNOHISTOCHEMISTRY; INTRAUTERINE GROWTH RETARDATION; KIDNEY DEVELOPMENT; KIDNEY FAILURE; MALE; NEPHRON; NONHUMAN; ONSET AGE; PLACENTA INSUFFICIENCY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEX DIFFERENCE; SYSTOLIC BLOOD PRESSURE; UPREGULATION; UTERINE TUBE LIGATION; WESTERN BLOTTING;

11-BETA-HYDROXYSTEROID DEHYDROGENASE TYPE 2; AGING; ANIMALS; CYCLOOXYGENASE 2; DOWN-REGULATION; FEMALE; FETAL GROWTH RETARDATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HYPERTENSION; KIDNEY; PLACENTAL CIRCULATION; PLACENTAL INSUFFICIENCY; PREGNANCY; RATS; RECEPTORS, GLUCOCORTICOID; RECEPTORS, MINERALOCORTICOID; RNA, MESSENGER; SEX CHARACTERISTICS;

EID: 34248184460     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00558.2006     Document Type: Article

References (62)

1. American Physiological Society. Guiding principles for research involving animals and human beings. Am J Physiol Regul Integr Comp Physiol 283: R281-R283, 2002.
2. Alexander BT. Placental insufficiency leads to development of hypertension in growth-restricted offspring. Hypertension 41: 457-462, 2003.
3. Alikhani-Koopaei R, Fouladkou F, Frey FJ, Frey BM. Epigenetic regulation of 11β-hydroxysteroid dehydrogenase type 2 expression. J Clin Invest 114: 1146-1157, 2004.
4. Barker DJ, Hales CN, Fall CH, Osmond C, Phipps K, Clark PM. Type 2 (non-insulin-dependent) diabetes mellitus, hypertension and hyperlipidaemia (syndrome X): relation to reduced fetal growth. Diabetologia 36: 62-67, 1993.
5. Baserga M, Bertolotto C, Maclennan NK, Hsu JL, Pham T, Laksana GS, Lane RH. Uteroplacental insufficiency decreases small intestine growth and alters apoptotic homeostasis in term intrauterine growth retarded rats. Early Hum Dev 79: 93-105, 2004.
6. Baserga M, Hale MA, Ke X, Wang ZM, Yu X, Callaway CW, McKnight RA, Lane RH. Uteroplacental insufficiency increases p53 phosphorylation without triggering the p53-MDM2 functional circuit response in the IUGR rat kidney. Am J Physiol Regul Integr Comp Physiol 291: R412-R418, 2006.
7. Baserga M, Hale MA, McKnight RA, Yu X, Callaway CW, Lane RH. Uteroplacental insufficiency alters hepatic expression, phosphorylation, and activity of the glucocorticoid receptor in fetal IUGR rats. Am J Physiol Regul Integr Comp Physiol 289: R1348-R1353, 2005.
8. Battista MC, Oligny LL, St-Louis J, Brochu M. Intrauterine growth restriction in rats is associated with hypertension and renal dysfunction in adulthood. Am J Physiol Endocrinol Metab 283: E124-E131, 2002.
9. Bauer R, Walter B, Bauer K, Klupsch R, Patt S, Zwiener U. Intrauterine growth restriction reduces nephron number and renal excretory function in newborn piglets. Acta Physiol Scand 176: 83-90, 2002.
10. Cock ML, Camm EJ, Louey S, Joyce BJ, Harding R. Postnatal outcomes in term and preterm lambs following fetal growth restriction. Clin Exp Pharmacol Physiol 28: 931-937, 2001.
11. Condon J, Gosden C, Gardener D, Nickson P, Hewison M, Howie AJ, Stewart PM. Expression of type 2 11β-hydroxysteroid dehydrogenase and corticosteroid hormone receptors in early human fetal life. J Clin Endocrinol Metab 83: 4490-4497, 1998.
12. Darnel AD, Archer TK, Yang K. Regulation of 11β- hydroxysteroid dehydrogenase type 2 by steroid hormones and epidermal growth factor in the Ishikawa human endometrial cell line. J Steroid Biochem Mol Biol 70: 203-210, 1999.
13. de Kloet ER, Reul JM, Sutanto W. Corticosteroids and the brain. J Steroid Biochem Mol Biol 37: 387-394, 1990.
14. Dinchuk JE, Car BD, Focht RJ, Johnston JJ, Jaffee BD, Covington MB, Contel NR, Eng VM, Collins RJ, Czerniak PM, Gorry SA, Trzaskos JM. Renal abnormalities and an altered inflammatory response in mice lacking cyclooxygenase II. Nature 378: 406-409, 1995.
15. Economides DL, Nicolaides KH. Blood glucose and oxygen tension levels in small-for-gestational-age fetuses. Am J Obstet Gynecol 160: 385-389, 1989.
16. Economides DL, Nicolaides KH, Linton EA, Perry LA, Chard T. Plasma cortisol and adrenocorticotropin in appropriate and small for gestational age fetuses. Fetal Ther 3: 158-164, 1988.
17. Edwards LJ, Coulter CL, Symonds ME, McMillen IC. Prenatal under-nutrition, glucocorticoids and the programming of adult hypertension. Clin Exp Pharmacol Physiol 28: 938-941, 2001.
18. Ferrari P, Krozowski Z. Role of the 11β-hydroxysteroid dehydrogenase type 2 in blood pressure regulation. Kidney Int 57: 1374-1381, 2000.
19. Freeman AI, Munn HL, Lyons V, Dammermann A, Seckl JR, Chapman KE. Glucocorticoid down-regulation of rat glucocorticoid receptor does not involve differential promoter regulation. J Endocrinol 183: 365-374, 2004.
20. Frey FJ, Odermatt A, Frey BM. Glucocorticoid-mediated mineralocorticoid receptor activation and hypertension. Curr Opin Nephrol Hypertens 13: 451-458, 2004.
21. Fu Q, McKnight RA, Yu X, Wang L, Callaway CW, Lane RH. Uteroplacental insufficiency induces site-specific changes in histone H3 covalent modifications and affects DNA-histone H3 positioning in day 0 IUGR rat liver. Physiol Genomics 20: 108-116, 2004.
22. Funder JW, Pearce PT, Smith R, Smith AI. Mineralocorticoid action: target tissue specificity is enzyme, not receptor, mediated. Science 242: 583-585, 1988.
23. Gagnon R. Placental insufficiency and its consequences. Eur J Obstet Gynecol Reprod Biol 110, Suppl 1: S99-S107, 2003.
24. Heiniger CD, Kostadinova RM, Rochat MK, Serra A, Ferrari P, Dick B, Frey BM, Frey FJ. Hypoxia causes down-regulation of 11β-hydroxysteroid dehydrogenase type 2 by induction of Egr-1. FASEB J 17: 917-919, 2003.
25. Henning SJ. Plasma concentrations of total and free corticosterone during development in the rat. Am J Physiol Endocrinol Metab 235: E451-E456, 1978.
26. Houang M, Morineau G, le Bouc Y, Fiet J, Gourmelen M. The cortisol-cortisone shuttle in children born with intrauterine growth retardation. Pediatr Res 46: 189-193, 1999.
27. Ke X, Lei Q, James SJ, Kelleher SL, Melnyk S, Jernigan S, Yu X, Wang L, Callaway CW, Gill G, Chan GM, Albertine KH, McKnight RA, Lane RH. Uteroplacental insufficiency affects epigenetic determinants of chromatin structure in brains of neonatal and juvenile IUGR rats. Physiol Genomics 25: 16-28, 2006.
28. Keller G, Zimmer G, Mall G, Ritz E, Amann K. Nephron number in patients with primary hypertension. N Engl J Med 348: 101-108, 2003.
29. Khan KN, Stanfield KM, Dannenberg A, Seshan SV, Baergen RN, Baron DA, Soslow RA. Cyclooxygenase-2 expression in the developing human kidney. Pediatr Dev Pathol 4: 461-466, 2001.
30. Komhoff M, Grone HJ, Klein T, Seyberth HW, Nusing RM. Localization of cyclooxygenase-1 and -2 in adult and fetal human kidney: implication for renal function. Am J Physiol Renal Physiol 272: F460-F468, 1997.
31. Komhoff M, Wang JL, Cheng HF, Langenbach R, McKanna JA, Harris RC, Breyer MD. Cyclooxygenase-2-selective inhibitors impair glomerulogenesis and renal cortical development. Kidney Int 57: 414-422, 2000.
32. Lane RH, Kelley DE, Ritov VH, Tsirka AE, Gruetzmacher EM. Altered expression and function of mitochondrial β-oxidation enzymes in juvenile intrauterine-growth-retarded rat skeletal muscle. Pediatr Res 50: 83-90, 2001.
33. Lane RH, Maclennan NK, Daood MJ, Hsu JL, Janke SM, Pham TD, Puri AR, Watchko JF. IUGR alters postnatal rat skeletal muscle peroxisome proliferator-activated receptor-gamma coactivator-1 gene expression in a fiber specific manner. Pediatr Res 53: 994-1000, 2003.
34. Langley SC, Jackson AA. Increased systolic blood pressure in adult rats induced by fetal exposure to maternal low protein diets. Clin Sci (Lond) 86: 217-222, 1994.
35. Lindsay RS, Lindsay RM, Edwards CR, Seckl JR. Inhibition of 11-β-hydroxysteroid dehydrogenase in pregnant rats and the programming of blood pressure in the offspring. Hypertension 27: 1200-1204, 1996.
36. MacLennan NK, James SJ, Melnyk S, Piroozi A, Jernigan S, Hsu JL, Janke SM, Pham TD, Lane RH. Uteroplacental insufficiency alters DNA methylation, one-carbon metabolism, and histone acetylation in IUGR rats. Physiol Genomics 18: 43-50, 2004.
37. Madsen K, Stubbe J, Yang T, Skott O, Bachmann S, Jensen BL. Low endogenous glucocorticoid allows induction of kidney cortical cyclooxygenase-2 during postnatal rat development. Am J Physiol Renal Physiol 286: F26-F37, 2004.
38. Menon RK, Shaufl A, Yu JH, Stephan DA, Friday RP. Identification and characterization of a novel transcript of the murine growth hormone receptor gene exhibiting development- and tissue-specific expression. Mol Cell Endocrinol 172: 135-146, 2001.
39. Morham SG, Langenbach R, Loftin CD, Tiano HF, Vouloumanos N, Jennette JC, Mahler JF, Kluckman KD, Ledford A, Lee CA, Smithies O. Prostaglandin synthase 2 gene disruption causes severe renal pathology in the mouse. Cell 83: 473-482, 1995.
40. Naray-Fejes-Toth A, Colombowala IK, Fejes-Toth G. The role of 11β-hydroxysteroid dehydrogenase in steroid hormone specificity. J Steroid Biochem Mol Biol 65: 311-316, 1998.
41. Norwood VF, Morham SG, Smithies O. Postnatal development and progression of renal dysplasia in cyclooxygenase-2 null mice. Kidney Int 58: 2291-2300, 2000.
42. Nyirenda MJ, Lindsay RS, Kenyon CJ, Burchell A, Seckl JR. Glucocorticoid exposure in late gestation permanently programs rat hepatic phosphoenolpyruvate carboxykinase and glucocorticoid receptor expression and causes glucose intolerance in adult offspring. J Clin Invest 101: 2174-2181, 1998.
43. Ogata ES, Bussey ME, Finley S. Altered gas exchange, limited glucose and branched chain amino acids, and hypoinsulinism retard fetal growth in the rat. Metabolism 35: 970-977, 1986.
44. Okret S, Dong Y, Bronnegard M, Gustafsson JA. Regulation of glucocorticoid receptor expression. Biochimie 73: 51-59, 1991.
45. Ostensen M. Nonsteroidal anti-inflammatory drugs during pregnancy. Scand J Rheumatol Suppl 107: 128-132, 1998.
46. Pachi A, Lubrano R, Maggi E, Giancotti A, Giampa G, Elli M, Mannarino O, Castello MA. Renal tubular damage in fetuses with intrauterine growth retardation. Fetal Diagn Ther 8: 109-113, 1993.
47. Pascual-Le Tallec L, Lombes M. The mineralocorticoid receptor: a journey exploring its diversity and specificity of action. Mol Endocrinol 19: 2211-2221, 2005.
48. Peruzzi L, Gianoglio B, Porcellini MG, Coppo R. Neonatal end-stage renal failure associated with maternal ingestion of cyclo-oxygenase-type-1 selective inhibitor nimesulide as tocolytic. Lancet 354: 1615, 1999.
49. Pham TD, MacLennan NK, Chiu CT, Laksana GS, Hsu JL, Lane RH. Uteroplacental insufficiency increases apoptosis and alters p53 gene methylation in the full-term IUGR rat kidney. Am J Physiol Regul Integr Comp Physiol 285: R962-R970, 2003.
50. Prevot A, Mosig D, Martini S, Guignard JP. Nimesulide, a cyclooxygenase-2 preferential inhibitor, impairs renal function in the newborn rabbit. Pediatr Res 55: 254-260, 2004.
51. Roghair RD, Segar JL, Sharma RV, Zimmerman MC, Jagadeesha DK, Segar EM, Scholz TD, Lamb FS. Newborn lamb coronary artery reactivity is programmed by early gestation dexamethasone before the onset of systemic hypertension. Am J Physiol Regul Integr Comp Physiol 289: R1169-R1176, 2005.
52. Schmitt R, Ellison DH, Farman N, Rossier BC, Reilly RF, Reeves WB, Oberbaumer I, Tapp R, Bachmann S. Developmental expression of sodium entry pathways in rat nephron. Am J Physiol Renal Physiol 276: F367-F381, 1999.
53. Schreuder MF, Nyengaard JR, Fodor M, van Wijk JA, Delemarrevan de Waal HA. Glomerular number and function are influenced by spontaneous and induced low birth weight in rats. J Am Soc Nephrol 16: 2913-2919, 2005.
54. Silver LE, Decamps PJ, Korst LM, Platt LD, Castro LC. Intrauterine growth restriction is accompanied by decreased renal volume in the human fetus. Am J Obstet Gynecol 188: 1320-1325, 2003.
55. Simmons RA, Templeton LJ, Gertz SJ. Intrauterine growth retardation leads to the development of type 2 diabetes in the rat. Diabetes 50: 2279-2286, 2001.
56. Steele BT, Paes B, Towell ME, Hunter DJ. Fetal renal failure associated with intrauterine growth retardation. Am J Obstet Gynecol 159: 1200-1202, 1988.
57. White PC, Mune T, Agarwal AK. 11β-Hydroxysteroid dehydrogenase and the syndrome of apparent mineralocorticoid excess. Endocr Rev 18: 135-156, 1997.
58. Whitesall SE, Hoff JB, Vollmer AP, D'Alecy LG. Comparison of simultaneous measurement of mouse systolic arterial blood pressure by radiotelemetry and tail-cuff methods. Am J Physiol Heart Circ Physiol 286: H2408-H2415, 2004.
59. 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.
60. Witlin AG, Sibai BM. Hypertension in pregnancy: current concepts of preeclampsia. Annu Rev Med 48: 115-127, 1997.
61. Woods LL, Weeks DA, Rasch R. Programming of adult blood pressure by maternal protein restriction: role of nephrogenesis. Kidney Int 65: 1339-1348, 2004.
62. Yao B, Harris RC, Zhang MZ. Interactions between 11β-hydroxysteroid dehydrogenase and COX-2 in kidney. Am J Physiol Regul Integr Comp Physiol 288: R1767-R1773, 2005.