The renin-angiotensin system from conception to old age: The good, the bad and the ugly

Clinical and Experimental Pharmacology and Physiology

Volumn 40, Issue 11, 2013, Pages 743-752

  Lumbers, Eugenie R ^a   Pringle, Kirsty G ^a   Wang, Yu ^a   Gibson, Karen J ^b  

^a UNIVERSITY OF NEWCASTLE   (Australia)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

Chronic kidney disease; Indigenous Australians; Nephrogenesis; Placentation; Renin angiotensin aldosterone system

Indexed keywords

ANGIOTENSIN; CYTOKINE;

ALLERGIC GLOMERULONEPHRITIS; ANGIOGENESIS; ARTICLE; AUSTRALIA; CELL PROLIFERATION; CONCEPTION; DISEASE PREDISPOSITION; DNA POLYMORPHISM; EPIDEMIC; EPIGENETIC REPRESSION; FAILURE TO THRIVE; GLOMERULUS FILTRATION RATE; HUMAN; INCIDENCE; INDIGENOUS PEOPLE; INFECTION; INTERSTITIAL NEPHRITIS; KIDNEY DEVELOPMENT; KIDNEY DISEASE; KIDNEY FAILURE; LOW BIRTH WEIGHT; NEPHRON; NON INSULIN DEPENDENT DIABETES MELLITUS; PATHOGENESIS; PLACENTA DISORDER; PREMATURE LABOR; PREMATURITY; PRENATAL PERIOD; PREVALENCE; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; REPRODUCTION; SENESCENCE;

CHRONIC KIDNEY DISEASE; INDIGENOUS AUSTRALIANS; NEPHROGENESIS; PLACENTATION; RENIN-ANGIOTENSIN-ALDOSTERONE SYSTEM;

AGING; ANIMALS; AUSTRALIA; DISEASE PROGRESSION; DNA METHYLATION; EPIGENESIS, GENETIC; FEMALE; FETAL DEVELOPMENT; HUMANS; HYPERTENSION; KIDNEY; MALE; OCEANIC ANCESTRY GROUP; PLACENTATION; PREGNANCY; RENAL INSUFFICIENCY, CHRONIC; RENIN-ANGIOTENSIN SYSTEM;

EID: 84886783411     PISSN: 03051870     EISSN: 14401681     Source Type: Journal    
DOI: 10.1111/1440-1681.12098     Document Type: Article

References (94)

1. Barker DJ. Sir Richard Doll Lecture. Developmental origins of chronic disease. Public Health 2012; 126: 185-9.
2. Sutherland MR, Gubhaju L, Moore L et al. Accelerated maturation and abnormal morphology in the preterm neonatal kidney. J. Am. Soc. Nephrol. 2011; 22: 1365-74.
3. Kandasamy Y, Smith R, Wright IM, Lumbers ER. Relationships between glomerular filtration rate and kidney Volume in low-birth-weight neonates. J. Nephrol. 2012. doi:10.5301z/jn.5000220 [Epub ahead of print].
4. Konje JC, Okaro CI, Bell SC, de Chazal R, Taylor DJ. A cross-sectional study of changes in fetal renal size with gestation in appropriate- and small-for-gestational-age fetuses. Ultrasound Obstet. Gynecol. 1997; 10: 22-6.
5. Hinchliffe SA, Lynch MR, Sargent PH, Howard CV, Van Velzen D. The effect of intrauterine growth retardation on the development of renal nephrons. Br. J. Obstet. Gynaecol. 1992; 99: 296-301.
6. HealthInfoNet. Review of the Kidney Health of Indigenous Peoples. 2006. Available from: http://www.healthinfonet.ecu.edu.au/chronic-conditions/kidney/reviews/our-review2006 (accessed 29 March 2013).
7. Schiffrin EL, Lipman ML, Mann JF. Chronic kidney disease: Effects on the cardiovascular system. Circulation 2007; 116: 85-97.
8. von Lueder TG, Krum H. RAAS inhibitors and cardiovascular protection in large scale trials. Cardiovasc. Drugs Ther. 2013; 27: 171-9.
9. Stevenson KM, Gibson KJ, Lumbers ER. Comparison of the transplacental transfer of enalapril, captopril and losartan in sheep. Br. J. Pharmacol. 1995; 114: 1495-501.
10. Lumbers ER. Activation of renin in human amniotic fluid by low pH. Enzymologia 1971; 40: 329-36.
11. Morris BJ, Lumbers ER. The activation of renin in human amniotic fluid by proteolytic enzymes. Biochim. Biophys. Acta 1972; 289: 385-91.
12. Nguyen G, Delarue F, Burckle C, Bouzhir L, Giller T, Sraer JD. Pivotal role of the renin/prorenin receptor in angiotensin II production and cellular responses to renin. J. Clin. Invest. 2002; 109: 1417-27.
13. Nguyen G. Renin, (pro)renin and receptor: An update. Clin. Sci. 2011; 120: 169-78.
14. de Gasparo M, Catt KJ, Inagami T, Wright JW, Unger T. International Union of pharmAcology. XXIII. The angiotensin II receptors. Pharmacol. Rev. 2000; 52: 415-72.
15. Santos RA, Ferreira AJ, Verano-Braga T, Bader M. Angiotensin-converting enzyme 2, angiotensin-(1-7) and Mas: New players of the renin angiotensin system. J. Endocrinol. 2013; 216: R1-17.
16. Passos-Silva DG, Verano-Braga T, Santos RA. Angiotensin-(1-7): Beyond the cardio-renal actions. Clin. Sci. 2013; 124: 443-56.
17. Khong TY, De Wolf F, Robertson WB, Brosens I. Inadequate maternal vascular response to placentation in pregnancies complicated by pre-eclampsia and by small-for-gestational age infants. Br. J. Obstet. Gynaecol. 1986; 93: 1049-59.
18. Arroyo JA, Winn VD. Vasculogenesis and angiogenesis in the IUGR placenta. Semin. Perinatol. 2008; 32: 172-7.
19. Kim YM, Bujold E, Chaiworapongsa T et al. Failure of physiologic transformation of the spiral arteries in patients with preterm labor and intact membranes. Am. J. Obstet. Gynecol. 2003; 189: 1063-9.
20. Barker DJ, Larsen G, Osmond C, Thornburg KL, Kajantie E, Eriksson JG. The placental origins of sudden cardiac death. Int. J. Epidemiol. 2012; 41: 1394-9.
21. Le Noble FA, Hekking JW, Van Straaten HW, Slaaf DW, Struyker Boudier HA. Angiotensin II stimulates angiogenesis in the chorio-allantoic membrane of the chick embryo. Eur. J. Pharmacol. 1991; 195: 305-6.
22. Sanchez-Lopez E, Lopez AF, Esteban V et al. Angiotensin II regulates vascular endothelial growth factor via hypoxia-inducible factor-1alpha induction and redox mechanisms in the kidney. Antioxid. Redox Signal. 2005; 7: 1275-84.
23. Herr D, Rodewald M, Fraser HM et al. Regulation of endothelial proliferation by the renin-angiotensin system in human umbilical vein endothelial cells. Reproduction 2008; 136: 125-30.
24. Pupilli C, Lasagni L, Romagnani P et al. Angiotensin II stimulates the synthesis and secretion of vascular permeability factor/vascular endothelial growth factor in human mesangial cells. J. Am. Soc. Nephrol. 1999; 10: 245-55.
25. Tamarat R, Silvestre JS, Durie M, Levy BI. Angiotensin II angiogenic effect in vivo involves vascular endothelial growth factor- and inflammation-related pathways. Lab. Invest. 2002; 82: 747-56.
26. Miyajima A, Kosaka T, Asano T, Seta K, Kawai T, Hayakawa M. Angiotensin II type I antagonist prevents pulmonary metastasis of murine renal cancer by inhibiting tumor angiogenesis. Cancer Res. 2002; 62: 4176-9.
27. Barleon B, Hauser S, Schollmann C et al. Differential expression of the two VEGF receptors flt and KDR in placenta and vascular endothelial cells. J. Cell. Biochem. 1994; 54: 56-66.
28. Tsoi SCM, Wen Y, Chung J-Y, Chen D, Magness RR, Zheng J. Co-expression of vascular endothelial growth factor and neuropilin-1 in ovine feto-placental artery endothelial cells. Mol. Cell. Endocrinol. 2002; 196: 95-106.
29. Bird IM, Sullivan JA, Di T et al. Pregnancy-dependent changes in cell signaling underlie changes in differential control of vasodilator production in uterine artery endothelial cells. Endocrinology 2000; 141: 1107-17.
30. Cowden Dahl KD, Fryer BH, Mack FA et al. Hypoxia-inducible factors 1alpha and 2alpha regulate trophoblast differentiation. Mol. Cell. Biol. 2005; 25: 10479-91.
31. Walther T, Jank A, Heringer-Walther S, Horn LC, Stepan H. Angiotensin II type 1 receptor has impact on murine placentation. Placenta 2008; 29: 905-9.
32. Soto-Pantoja DR, Menon J, Gallagher PE, Tallant EA. Angiotensin-(1-7) inhibits tumor angiogenesis in human lung cancer xenografts with a reduction in vascular endothelial growth factor. Mol. Cancer Ther. 2009; 8: 1676-83.
33. George AJ, Thomas WG, Hannan RD. The renin-angiotensin system and cancer: Old dog, new tricks. Nat. Rev. Cancer 2010; 10: 745-59.
34. Gallagher PE, Tallant EA. Inhibition of human lung cancer cell growth by angiotensin-(1-7). Carcinogenesis 2004; 25: 2045-52.
35. Krishnan B, Torti FM, Gallagher PE, Tallant EA. Angiotensin-(1-7) reduces proliferation and angiogenesis of human prostate cancer xenografts with a decrease in angiogenic factors and an increase in sFlt-1. Prostate 2013; 73: 60-70.
36. Pringle KG, Tadros MA, Callister RJ, Lumbers ER. The expression and localization of the human placental prorenin/renin-angiotensin system throughout pregnancy. Roles in trophoblast invasion and angiogenesis? Placenta 2011; 32: 956-62.
37. Lumbers ER, Reid GC. The actions of vasoactive compounds in the foetus and the effect of perfusion through the placenta on their biological activity. Aust. J. Exp. Biol. Med. Sci. 1978; 56: 11-24.
38. Wang Y, Pringle KG, Chen YX, Zakar T, Lumbers ER. Regulation of the renin-angiotensin system (RAS) in BeWo and HTR-8/SVneo trophoblast cell lines. Placenta 2012; 33: 634-9.
39. Wang Y, Pringle KG, Lumbers ER. The effects of cyclic AMP, sex steroids and global hypomethylation on the expression of genes controlling the activity of the renin-angiotensin system in placental cell lines. Placenta 2013; 34: 275-80.
40. Pinet F, Mizrahi J, Menard J, Corvol P. Role of cyclic AMP in renin secretion by human transfected juxtaglomerular cells. J. Hypertens. Suppl. 1986; 4: S421-3.
41. Poisner AM, Downing GJ, Poisner R. Prorenin secretion from villous placenta. Regulation by cyclic AMP and angiotensin. Placenta 1994; 15: 487-99.
42. Bogdarina I, Welham S, King PJ, Burns SP, Clark AJ. Epigenetic modification of the renin-angiotensin system in the fetal programming of hypertension. Circ. Res. 2007; 100: 520-6.
43. Morgan HD, Jin XL, Li A, Whitelaw E, O'Neill C. The culture of zygotes to the blastocyst stage changes the postnatal expression of an epigentically labile allele, agouti viable yellow, in mice. Biol. Reprod. 2008; 79: 618-23.
44. Pentz ES, Lopez ML, Cordaillat M, Gomez RA. Identity of the renin cell is mediated by cAMP and chromatin remodeling. An in vitro model for studying cell recruitment and plasticity. Am. J. Physiol. Heart Circ. Physiol. 2008; 294: H699-707.
45. Goyal R, Lister R, Leitzke A, Goyal D, Gheorghe CP, Longo LD. Antenatal maternal hypoxic stress: Adaptations of the placental renin-angiotensin system in the mouse. Placenta 2011; 32: 134-9.
46. Goyal R, Leitzke A, Goyal D, Gheorghe CP, Longo LD. Antenatal maternal hypoxic stress: Adaptations in fetal lung renin-angiotensin system. Reprod. Sci. 2011; 18: 180-9.
47. Jauniaux E, Watson AL, Hempstock J, Bao YP, Skepper JN, Burton GJ. Onset of maternal arterial blood flow and placental oxidative stress. A possible factor in human early pregnancy failure. Am. J. Pathol. 2000; 157: 2111-22.
48. Tufro-McReddie A, Romano LM, Harris JM, Ferder L, Gomez RA. Angiotensin II regulates nephrogenesis and renal vascular development. Am. J. Physiol. 1995; 269: F110-5.
49. Tufro-McReddie A, Norwood VF, Aylor KW, Botkin SJ, Carey RM, Gomez RA. Oxygen regulates vascular endothelial growth factor-mediated vasculogenesis and tubulogenesis. Dev. Biol. 1997; 183: 139-49.
50. Pentz ES, Moyano MA, Thornhill BA, Sequeira Lopez ML, Gomez RA. Ablation of renin-expressing juxtaglomerular cells results in a distinct kidney phenotype. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2004; 286: R474-83.
51. Sequeira Lopez ML, Pentz ES, Nomasa T, Smithies O, Gomez RA. Renin cells are precursors for multiple cell types that switch to the renin phenotype when homeostasis is threatened. Dev. Cell 2004; 6: 719-28.
52. Moravski CJ, Kelly DJ, Cooper ME et al. Retinal neovascularization is prevented by blockade of the renin-angiotensin system. Hypertension 2000; 36: 1099-104.
53. 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: 460-7.
54. Lumbers ER, Burrell JH, Menzies RI, Stevens AD. The effects of a converting enzyme inhibitor (captopril) and angiotensin II on fetal renal function. Br. J. Pharmacol. 1993; 110: 821-7.
55. Wang Z, Hoy WE. Albuminuria and incident coronary heart disease in Australian Aboriginal people. Kidney Int. 2005; 68: 1289-93.
56. Navar LG, Prieto MC, Satou R, Kobori H. Intrarenal angiotensin II and its contribution to the genesis of chronic hypertension. Curr. Opin. Pharmacol. 2011; 11: 180-6.
57. Prieto-Carrasquero MC, Harrison-Bernard LM, Kobori H et al. Enhancement of collecting duct renin in angiotensin II-dependent hypertensive rats. Hypertension 2004; 44: 223-9.
58. Coffman TM, Crowley SD. Kidney in hypertension: Guyton redux. Hypertension 2008; 51: 811-6.
59. 1A angiotensin receptors in the renal proximal tubule regulate blood pressure. Cell Metab. 2011; 13: 469-75.
60. Crowley SD, Zhang J, Herrera M, Griffiths R, Ruiz P, Coffman TM. Role of AT(1) receptor-mediated salt retention in angiotensin II-dependent hypertension. Am. J. Physiol. Renal Physiol. 2011; 301: F1124-30.
61. Siragy HM, Carey RM. Role of the intrarenal renin-angiotensin-aldosterone system in chronic kidney disease. Am. J. Nephrol. 2010; 31: 541-50.
62. Xue C, Siragy HM. Local renal aldosterone system and its regulation by salt, diabetes, and angiotensin II type 1 receptor. Hypertension 2005; 46: 584-90.
63. Lee SH, Yoo TH, Nam BY et al. Activation of local aldosterone system within podocytes is involved in apoptosis under diabetic conditions. Am. J. Physiol. Renal Physiol. 2009; 297: F1381-90.
64. Siragy HM, Xue C. Local renal aldosterone production induces inflammation and matrix formation in kidneys of diabetic rats. Exp. Physiol. 2008; 93: 817-24.
65. Ruster C, Wolf G. Renin-angiotensin-aldosterone system and progression of renal disease. J. Am. Soc. Nephrol. 2006; 17: 2985-91.
66. Toma I, Kang JJ, Sipos A et al. Succinate receptor GPR91 provides a direct link between high glucose levels and renin release in murine and rabbit kidney. J. Clin. Invest. 2008; 118: 2526-34.
67. Kobori H, Ohashi N, Katsurada A et al. Urinary angiotensinogen as a potential biomarker of severity of chronic kidney diseases. J. Am. Soc. Hypertens. 2008; 2: 349-54.
68. Kobori H, Alper AB Jr, Shenava R et al. Urinary angiotensinogen as a novel biomarker of the intrarenal renin-angiotensin system status in hypertensive patients. Hypertension 2009; 53: 344-50.
69. Sawaguchi M, Araki SI, Kobori H et al. Association between urinary angiotensinogen levels and renal and cardiovascular prognoses in patients with type 2 diabetes mellitus. J. Diabetes Investig. 2012; 3: 318-24.
70. Kobori H, Navar LG. Urinary angiotensinogen as a novel biomarker of intrarenal renin-angiotensin system in chronic kidney disease. Int. Rev. Thromb. 2011; 6: 108-16.
71. Urushihara M, Kondo S, Kagami S, Kobori H. Urinary angiotensinogen accurately reflects intrarenal renin-angiotensin system activity. Am. J. Nephrol. 2010; 31: 318-25.
72. Kamiyama M, Zsombok A, Kobori H. Urinary angiotensinogen as a novel early biomarker of intrarenal renin-angiotensin system activation in experimental type 1 diabetes. J. Pharmacol. Sci. 2012; 119: 314-23.
73. HealthInfoNet. Births and Pregnancy Outcome. 2006. Available from: http://www.healthinfonet.ecu.edu.au/health-facts/overviews/births-and-pregnancy-outcome (accessed 29 March 2013).
74. Langridge AT, Nassar N, Li J, Stanley FJ. Social and racial inequalities in preterm births in Western Australia, 1984-2006. Paediatr. Perinat. Epidemiol. 2010; 24: 352-62.
75. Hoy WE, Hughson MD, Singh GR, Douglas-Denton R, Bertram JF. Reduced nephron number and glomerulomegaly in Australian Aborigines. A group at high risk for renal disease and hypertension. Kidney Int. 2006; 70: 104-10.
76. Brandon AE, Boyce AC, Lumbers ER, Zimanyi MA, Bertram JF, Gibson KJ. Glomerular hypertrophy in offspring of subtotally nephrectomized ewes. Anat. Rec. 2008; 291: 318-24.
77. Hoy WE, Wang Z, VanBuynder P, Baker PR, McDonald SM, Mathews JD. The natural history of renal disease in Australian Aborigines. Part 2. Albuminuria predicts natural death and renal failure. Kidney Int. 2001; 60: 249-56.
78. Cunningham FG, Cox SM, Harstad TW, Mason RA, Pritchard JA. Chronic renal disease and pregnancy outcome. Am. J. Obstet. Gynecol. 1990; 163: 453-9.
79. Jones DC, Hayslett JP. Outcome of pregnancy in women with moderate or severe renal insufficiency. N. Engl. J. Med. 1996; 335: 226-32.
80. Jungers P, Chauveau D. Pregnancy in renal disease. Kidney Int. 1997; 52: 871-85.
81. HealthInfoNet. Review of Diabetes among Indigenous Peoples. 2007. Available from: http://www.healthinfonet.ecu.edu.au/chronic-conditions/diabetes/reviews/our-review, accessed 29 March 2013.
82. Prime Minister's Science, Engineering and Innovation Council (PMSEIC) Working Group on Aboriginal and Islander Health Focusing on Maternal, Fetal and Postnatal Health. The Health of the Adult Begins in the Womb. A Report of the PMSEIC Working Group April 2008. 2008. Available from: http://www.innovation.gov.au/Science/PMSEIC/Documents/AboriginalandTorresStraitIslandHealth.pdf, accessed 29 March 2013.
83. Lester S, Heatley S, Bardy P et al. The DD genotype of the angiotensin-converting enzyme gene occurs in very low frequency in Australian Aboriginals. Nephrol. Dial. Transplant. 1999; 14: 887-90.
84. Campbell CY, Fang BF, Guo X et al. Associations between genetic variants in the ACE, AGT, AGTR1 and AGTR2 genes and renal function in the multi-ethnic study of atherosclerosis. Am. J. Nephrol. 2010; 32: 156-62.
85. Huang HD, Lin FJ, Li XJ, Wang LR, Jiang GR. Genetic polymorphisms of the renin-angiotensin-aldosterone system in Chinese patients with end-stage renal disease secondary to IgA nephropathy. Chin. Med. J. 2010; 123: 3238-42.
86. Ahluwalia TS, Ahuja M, Rai TS et al. ACE variants interact with the RAS pathway to confer risk and protection against type 2 diabetic nephropathy. DNA Cell Biol. 2009; 28: 141-50.
87. Zhu X, Bouzekri N, Southam L et al. Linkage and association analysis of angiotensin I-converting enzyme (ACE)-gene polymorphisms with ACE concentration and blood pressure. Am. J. Hum. Genet. 2001; 68: 1139-48.
88. Moscovis SM, Gordon AE, Al Madani OM et al. IL6 G-174C associated with sudden infant death syndrome in a Caucasian Australian cohort. Hum. Immunol. 2006; 67: 819-25.
89. Satou R, Gonzalez-Villalobos RA, Miyata K et al. IL-6 augments angiotensinogen in primary cultured renal proximal tubular cells. Mol. Cell. Endocrinol. 2009; 311: 24-31.
90. Skinner SL, Lumbers ER, Symonds EM. Alteration by oral contraceptives of normal menstrual changes in plasma renin activity, concentration and substrate. Clin. Sci. 1969; 36: 67-76.
91. 1 receptor mediated augmentation of intrarenal angiotensinogen in angiotensin II-dependent hypertension. Hypertension 2004; 43: 1126-32.
92. Chamarthi B, Williams GH, Ricchiuti V et al. Inflammation and hypertension: The interplay of interleukin-6, dietary sodium, and the renin-angiotensin system in humans. Am. J. Hypertens. 2011; 24: 1143-8.
93. Santos RA, Ferreira AJ, Simoes ESAC. Recent advances in the angiotensin-converting enzyme 2-angiotensin (1-7)-Mas axis. Exp. Physiol. 2008; 93: 519-27.
94. Shankland SJ. The podocyte's response to injury: Role in proteinuria and glomerulosclerosis. Kidney Int. 2006; 69: 2131-47.