Skip to main content
Erschienen in: European Journal of Pediatrics 2/2017

19.12.2016 | Original Article

(Pro)renin and (pro)renin receptor expression during kidney development in neonates

verfasst von: Tomomasa Terada, Maki Urushihara, Takahiko Saijo, Ryuji Nakagawa, Shoji Kagami

Erschienen in: European Journal of Pediatrics | Ausgabe 2/2017

Einloggen, um Zugang zu erhalten

Abstract

Although a recent study demonstrated that the (pro)renin receptor ((P)RR) was highly expressed in the developing kidney during the mouse embryonic development, the mechanism by which (P)RR supports renal development in humans is not fully understood. In this study, we examined the plasma levels of (pro)renin and soluble (P)RR (s(P)RR) in cord blood and neonates as well as (P)RR expression in human kidney tissues. Samples were collected from 57 preterm and 67 full-term human neonates. (Pro)renin and s(P)RR levels were measured using enzyme-linked immunosorbent assays. Additionally, we performed an immunohistochemical (IHC) analysis of kidney tissues from neonates and minor glomerular abnormalities in order to assess (P)RR expression in the kidney. Plasma (pro)renin and s(P)RR levels in cord blood were significantly higher in preterm neonates than in full-term neonates. Four weeks after birth, these differences were no longer evident for either plasma (pro)renin or s(P)RR levels between the two groups. Importantly, plasma (pro)renin and s(P)RR levels in cord blood were inversely correlated with gestational age. Furthermore, IHC indicated that renal expression levels of (P)RR in neonates were stronger than those in minor glomerular abnormalities.
Conclusion: (P)RR may play a pivotal role in prenatal renal development in humans.
What is Known:
Renal renin-angiotensin system (RAS) has several pathophysiologic functions not only in blood pressure regulation but also in pediatric renal disease.
Renal RAS activation plays a key role of renal development during gestation.
What is New :
Plasma (pro)renin and soluble (pro)renin receptor (s(P)RR) levels in cord blood were significantly higher in preterm neonates than in full-term neonates.
Immunohistochemical analysis of kidney tissue indicated that renal expression levels of (P)RR in neonates were stronger than in minor glomerular abnormalities.
Literatur
1.
Zurück zum Zitat Amsterdam A, Nissen RM, Sun Z, Swindell EC, Farrington S, Hopkins N (2004) Identification of 315 genes essential for early zebrafish development. Proc Natl Acad Sci U S A 101:12792–12797CrossRefPubMedPubMedCentral Amsterdam A, Nissen RM, Sun Z, Swindell EC, Farrington S, Hopkins N (2004) Identification of 315 genes essential for early zebrafish development. Proc Natl Acad Sci U S A 101:12792–12797CrossRefPubMedPubMedCentral
2.
Zurück zum Zitat el-Dahr SS, Gomez RA, Gray MS, Peach MJ, Carey RM, Chevalier RL (1990) In situ localization of renin and its mRNA in neonatal ureteral obstruction. Am J Phys 258:F854–F862 el-Dahr SS, Gomez RA, Gray MS, Peach MJ, Carey RM, Chevalier RL (1990) In situ localization of renin and its mRNA in neonatal ureteral obstruction. Am J Phys 258:F854–F862
3.
Zurück zum Zitat Gomez RA, Robillard JE (1984) Developmental aspects of the renal responses to hemorrhage during converting-enzyme inhibition in fetal lambs. Circ Res 54:301–312CrossRefPubMed Gomez RA, Robillard JE (1984) Developmental aspects of the renal responses to hemorrhage during converting-enzyme inhibition in fetal lambs. Circ Res 54:301–312CrossRefPubMed
4.
Zurück zum Zitat Gonzalez AA, Lara LS, Luffman C, Seth DM, Prieto MC (2011) Soluble form of the (pro)renin receptor is augmented in the collecting duct and urine of chronic angiotensin II-dependent hypertensive rats. Hypertension 57:859–864CrossRefPubMedPubMedCentral Gonzalez AA, Lara LS, Luffman C, Seth DM, Prieto MC (2011) Soluble form of the (pro)renin receptor is augmented in the collecting duct and urine of chronic angiotensin II-dependent hypertensive rats. Hypertension 57:859–864CrossRefPubMedPubMedCentral
5.
Zurück zum Zitat Gubler MC, Antignac C (2010) Renin-angiotensin system in kidney development: renal tubular dysgenesis. Kidney Int 77:400–406CrossRefPubMed Gubler MC, Antignac C (2010) Renin-angiotensin system in kidney development: renal tubular dysgenesis. Kidney Int 77:400–406CrossRefPubMed
6.
Zurück zum Zitat Hirose T, Hashimoto M, Totsune K, Metoki H, Hara A, Satoh M, Kikuya M, Ohkubo T, Asayama K, Kondo T, Kamide K, Katsuya T, Ogihara T, Izumi S, Rakugi H, Takahashi K, Imai Y (2011) Association of (pro)renin receptor gene polymorphisms with lacunar infarction and left ventricular hypertrophy in Japanese women: the Ohasama study. Hypertens Res 34:530–535CrossRefPubMed Hirose T, Hashimoto M, Totsune K, Metoki H, Hara A, Satoh M, Kikuya M, Ohkubo T, Asayama K, Kondo T, Kamide K, Katsuya T, Ogihara T, Izumi S, Rakugi H, Takahashi K, Imai Y (2011) Association of (pro)renin receptor gene polymorphisms with lacunar infarction and left ventricular hypertrophy in Japanese women: the Ohasama study. Hypertens Res 34:530–535CrossRefPubMed
7.
Zurück zum Zitat Ichihara A, Kinouchi K (2011) Current knowledge of (pro)renin receptor as an accessory protein of vacuolar H+-ATPase. J Renin-Angiotensin-Aldosterone Syst 12:638–640CrossRefPubMed Ichihara A, Kinouchi K (2011) Current knowledge of (pro)renin receptor as an accessory protein of vacuolar H+-ATPase. J Renin-Angiotensin-Aldosterone Syst 12:638–640CrossRefPubMed
8.
Zurück zum Zitat Kinouchi K, Ichihara A, Sano M, Sun-Wada GH, Wada Y, Kurauchi-Mito A, Bokuda K, Narita T, Oshima Y, Sakoda M, Tamai Y, Sato H, Fukuda K, Itoh H (2010) The (pro)renin receptor/ATP6AP2 is essential for vacuolar H+-ATPase assembly in murine cardiomyocytes. Circ Res 107:30–34CrossRefPubMed Kinouchi K, Ichihara A, Sano M, Sun-Wada GH, Wada Y, Kurauchi-Mito A, Bokuda K, Narita T, Oshima Y, Sakoda M, Tamai Y, Sato H, Fukuda K, Itoh H (2010) The (pro)renin receptor/ATP6AP2 is essential for vacuolar H+-ATPase assembly in murine cardiomyocytes. Circ Res 107:30–34CrossRefPubMed
9.
Zurück zum Zitat Madsen K, Tinning AR, Marcussen N, Jensen BL (2013) Postnatal development of the renal medulla; role of the renin-angiotensin system. Acta Physiol 208:41–49CrossRef Madsen K, Tinning AR, Marcussen N, Jensen BL (2013) Postnatal development of the renal medulla; role of the renin-angiotensin system. Acta Physiol 208:41–49CrossRef
10.
Zurück zum Zitat Mahieu-Caputo D, Dommergues M, Delezoide AL, Lacoste M, Cai Y, Narcy F, Jolly D, Gonzales M, Dumez Y, Gubler MC (2000) Twin-to-twin transfusion syndrome. Role of the fetal renin-angiotensin system. Am J Pathol 156:629–636CrossRefPubMedPubMedCentral Mahieu-Caputo D, Dommergues M, Delezoide AL, Lacoste M, Cai Y, Narcy F, Jolly D, Gonzales M, Dumez Y, Gubler MC (2000) Twin-to-twin transfusion syndrome. Role of the fetal renin-angiotensin system. Am J Pathol 156:629–636CrossRefPubMedPubMedCentral
11.
Zurück zum Zitat Martinovic J, Benachi A, Laurent N, Daikha-Dahmane F, Gubler MC (2001) Fetal toxic effects and angiotensin-II-receptor antagonists. Lancet 358:241–242CrossRefPubMed Martinovic J, Benachi A, Laurent N, Daikha-Dahmane F, Gubler MC (2001) Fetal toxic effects and angiotensin-II-receptor antagonists. Lancet 358:241–242CrossRefPubMed
12.
Zurück zum Zitat Maruyama N, Segawa T, Kinoshita N, Ichihara A (2013) Novel sandwich ELISA for detecting the human soluble (pro)renin receptor. Front Biosci (Elite Ed) 5:583–590CrossRef Maruyama N, Segawa T, Kinoshita N, Ichihara A (2013) Novel sandwich ELISA for detecting the human soluble (pro)renin receptor. Front Biosci (Elite Ed) 5:583–590CrossRef
13.
Zurück zum Zitat Mounier F, Hinglais N, Sich M, Gros F, Lacoste M, Deris Y, Alhenc-Gelas F, Gubler MC (1987) Ontogenesis of angiotensin-I converting enzyme in human kidney. Kidney Int 32:684–690CrossRefPubMed Mounier F, Hinglais N, Sich M, Gros F, Lacoste M, Deris Y, Alhenc-Gelas F, Gubler MC (1987) Ontogenesis of angiotensin-I converting enzyme in human kidney. Kidney Int 32:684–690CrossRefPubMed
14.
Zurück zum Zitat Navar LG (2013) Translational studies on augmentation of intratubular renin-angiotensin system in hypertension. Kidney Int Suppl (2011) 3:321–325CrossRef Navar LG (2013) Translational studies on augmentation of intratubular renin-angiotensin system in hypertension. Kidney Int Suppl (2011) 3:321–325CrossRef
15.
Zurück zum Zitat Nguyen G, Muller DN (2010) The biology of the (pro)renin receptor. J Am Soc Nephrol 21:18–23CrossRefPubMed Nguyen G, Muller DN (2010) The biology of the (pro)renin receptor. J Am Soc Nephrol 21:18–23CrossRefPubMed
16.
Zurück zum Zitat Ohashi N, Isobe S, Ishigaki S, Suzuki T, Iwakura T, Ono M, Fujikura T, Tsuji T, Otsuka A, Ishii Y, Furuse H, Kato A, Ozono S, Yasuda H (2016) Plasma soluble (pro)renin receptor reflects renal damage. PLoS One 11:e0156165CrossRefPubMedPubMedCentral Ohashi N, Isobe S, Ishigaki S, Suzuki T, Iwakura T, Ono M, Fujikura T, Tsuji T, Otsuka A, Ishii Y, Furuse H, Kato A, Ozono S, Yasuda H (2016) Plasma soluble (pro)renin receptor reflects renal damage. PLoS One 11:e0156165CrossRefPubMedPubMedCentral
17.
Zurück zum Zitat Oshima Y, Kinouchi K, Ichihara A, Sakoda M, Kurauchi-Mito A, Bokuda K, Narita T, Kurosawa H, Sun-Wada GH, Wada Y, Yamada T, Takemoto M, Saleem MA, Quaggin SE, Itoh H (2011) Prorenin receptor is essential for normal podocyte structure and function. J Am Soc Nephrol 22:2203–2212CrossRefPubMedPubMedCentral Oshima Y, Kinouchi K, Ichihara A, Sakoda M, Kurauchi-Mito A, Bokuda K, Narita T, Kurosawa H, Sun-Wada GH, Wada Y, Yamada T, Takemoto M, Saleem MA, Quaggin SE, Itoh H (2011) Prorenin receptor is essential for normal podocyte structure and function. J Am Soc Nephrol 22:2203–2212CrossRefPubMedPubMedCentral
19.
Zurück zum Zitat Pelayo JC, Eisner GM, Jose PA (1981) The ontogeny of the renin-angiotensin system. Clin Perinatol 8:347–359PubMed Pelayo JC, Eisner GM, Jose PA (1981) The ontogeny of the renin-angiotensin system. Clin Perinatol 8:347–359PubMed
20.
Zurück zum Zitat Pryde PG, Sedman AB, Nugent CE, Barr M Jr (1993) Angiotensin-converting enzyme inhibitor fetopathy. J Am Soc Nephrol 3:1575–1582PubMed Pryde PG, Sedman AB, Nugent CE, Barr M Jr (1993) Angiotensin-converting enzyme inhibitor fetopathy. J Am Soc Nephrol 3:1575–1582PubMed
21.
Zurück zum Zitat Ramser J, Abidi FE, Burckle CA, Lenski C, Toriello H, Wen G, Lubs HA, Engert S, Stevenson RE, Meindl A, Schwartz CE, Nguyen G (2005) A unique exonic splice enhancer mutation in a family with X-linked mental retardation and epilepsy points to a novel role of the renin receptor. Hum Mol Genet 14:1019–1027CrossRefPubMed Ramser J, Abidi FE, Burckle CA, Lenski C, Toriello H, Wen G, Lubs HA, Engert S, Stevenson RE, Meindl A, Schwartz CE, Nguyen G (2005) A unique exonic splice enhancer mutation in a family with X-linked mental retardation and epilepsy points to a novel role of the renin receptor. Hum Mol Genet 14:1019–1027CrossRefPubMed
22.
Zurück zum Zitat Riediger F, Quack I, Qadri F, Hartleben B, Park JK, Potthoff SA, Sohn D, Sihn G, Rousselle A, Fokuhl V, Maschke U, Purfurst B, Schneider W, Rump LC, Luft FC, Dechend R, Bader M, Huber TB, Nguyen G, Muller DN (2011) Prorenin receptor is essential for podocyte autophagy and survival. J Am Soc Nephrol 22:2193–2202CrossRefPubMedPubMedCentral Riediger F, Quack I, Qadri F, Hartleben B, Park JK, Potthoff SA, Sohn D, Sihn G, Rousselle A, Fokuhl V, Maschke U, Purfurst B, Schneider W, Rump LC, Luft FC, Dechend R, Bader M, Huber TB, Nguyen G, Muller DN (2011) Prorenin receptor is essential for podocyte autophagy and survival. J Am Soc Nephrol 22:2193–2202CrossRefPubMedPubMedCentral
23.
Zurück zum Zitat Schutz S, Le Moullec JM, Corvol P, Gasc JM (1996) Early expression of all the components of the renin-angiotensin-system in human development. Am J Pathol 149:2067–2079PubMedPubMedCentral Schutz S, Le Moullec JM, Corvol P, Gasc JM (1996) Early expression of all the components of the renin-angiotensin-system in human development. Am J Pathol 149:2067–2079PubMedPubMedCentral
24.
Zurück zum Zitat Sihn G, Rousselle A, Vilianovitch L, Burckle C, Bader M (2010) Physiology of the (pro)renin receptor: Wnt of change? Kidney Int 78:246–256CrossRefPubMed Sihn G, Rousselle A, Vilianovitch L, Burckle C, Bader M (2010) Physiology of the (pro)renin receptor: Wnt of change? Kidney Int 78:246–256CrossRefPubMed
25.
Zurück zum Zitat Song R, Preston G, Ichihara A, Yosypiv IV (2013) Deletion of the prorenin receptor from the ureteric bud causes renal hypodysplasia. PLoS One 8:e63835CrossRefPubMedPubMedCentral Song R, Preston G, Ichihara A, Yosypiv IV (2013) Deletion of the prorenin receptor from the ureteric bud causes renal hypodysplasia. PLoS One 8:e63835CrossRefPubMedPubMedCentral
26.
Zurück zum Zitat Song R, Preston G, Kidd L, Bushnell D, Sims-Lucas S, Bates CM, Yosypiv IV (2016) Prorenin receptor is critical for nephron progenitors. Dev Biol 409:382–391CrossRefPubMed Song R, Preston G, Kidd L, Bushnell D, Sims-Lucas S, Bates CM, Yosypiv IV (2016) Prorenin receptor is critical for nephron progenitors. Dev Biol 409:382–391CrossRefPubMed
27.
Zurück zum Zitat Song R, Preston G, Yosypiv IV (2013) Ontogeny of the (pro)renin receptor. Pediatr Res 74:5–10CrossRefPubMed Song R, Preston G, Yosypiv IV (2013) Ontogeny of the (pro)renin receptor. Pediatr Res 74:5–10CrossRefPubMed
28.
Zurück zum Zitat Suzue M, Urushihara M, Nakagawa R, Saijo T, Kagami S (2015) Urinary angiotensinogen level is increased in preterm neonates. Clin Exp Nephrol 19:293–297CrossRefPubMed Suzue M, Urushihara M, Nakagawa R, Saijo T, Kagami S (2015) Urinary angiotensinogen level is increased in preterm neonates. Clin Exp Nephrol 19:293–297CrossRefPubMed
29.
Zurück zum Zitat Tufro-McReddie A, Gomez RA (1993) Ontogeny of the renin-angiotensin system. Semin Nephrol 13:519–530PubMed Tufro-McReddie A, Gomez RA (1993) Ontogeny of the renin-angiotensin system. Semin Nephrol 13:519–530PubMed
30.
Zurück zum Zitat Urushihara M, Kagami S (2011) Urinary angiotensinogen as a biomarker of nephropathy in childhood. International journal of nephrology 2011:206835CrossRefPubMedPubMedCentral Urushihara M, Kagami S (2011) Urinary angiotensinogen as a biomarker of nephropathy in childhood. International journal of nephrology 2011:206835CrossRefPubMedPubMedCentral
31.
Zurück zum Zitat Watanabe N, Bokuda K, Fujiwara T, Suzuki T, Mito A, Morimoto S, Jwa SC, Egawa M, Arai Y, Suzuki F, Sago H, Ichihara A (2012) Soluble (pro)renin receptor and blood pressure during pregnancy: a prospective cohort study. Hypertension 60:1250–1256CrossRefPubMed Watanabe N, Bokuda K, Fujiwara T, Suzuki T, Mito A, Morimoto S, Jwa SC, Egawa M, Arai Y, Suzuki F, Sago H, Ichihara A (2012) Soluble (pro)renin receptor and blood pressure during pregnancy: a prospective cohort study. Hypertension 60:1250–1256CrossRefPubMed
32.
Zurück zum Zitat Watanabe N, Morimoto S, Fujiwara T, Suzuki T, Taniguchi K, Ando T, Kimura T, Sago H, Ichihara A (2013) Association between soluble (Pro)renin receptor concentration in cord blood and small for gestational age birth: a cross-sectional study. PLoS One 8:e60036CrossRefPubMedPubMedCentral Watanabe N, Morimoto S, Fujiwara T, Suzuki T, Taniguchi K, Ando T, Kimura T, Sago H, Ichihara A (2013) Association between soluble (Pro)renin receptor concentration in cord blood and small for gestational age birth: a cross-sectional study. PLoS One 8:e60036CrossRefPubMedPubMedCentral
Metadaten
Titel
(Pro)renin and (pro)renin receptor expression during kidney development in neonates
verfasst von
Tomomasa Terada
Maki Urushihara
Takahiko Saijo
Ryuji Nakagawa
Shoji Kagami
Publikationsdatum
19.12.2016
Verlag
Springer Berlin Heidelberg
Erschienen in
European Journal of Pediatrics / Ausgabe 2/2017
Print ISSN: 0340-6199
Elektronische ISSN: 1432-1076
DOI
https://doi.org/10.1007/s00431-016-2820-9

Weitere Artikel der Ausgabe 2/2017

European Journal of Pediatrics 2/2017 Zur Ausgabe

Update Pädiatrie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.