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Published in: Pediatric Nephrology 10/2016

01-10-2016 | Review

Role of hypoxia during nephrogenesis

Authors: Shelby L. Hemker, Sunder Sims-Lucas, Jacqueline Ho

Published in: Pediatric Nephrology | Issue 10/2016

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Abstract

Mammals develop in a physiologically hypoxic state, and the oxygen tension of different tissues in the embryo is precisely controlled. Deviation from normal oxygenation, such as what occurs in placental insufficiency, can disrupt fetal development. Several studies demonstrate that intrauterine hypoxia has a negative effect on kidney development. As nascent nephrons are forming from nephron progenitors in the nephrogenic zone, they are exposed to varying oxygen tension by virtue of the development of the renal vasculature. Thus, nephrogenesis may be linked to oxygen tension. However, the mechanism(s) by which this occurs remains unclear. This review focuses on what is known about molecular mechanisms active in physiological and pathological hypoxia and their effects on kidney development.
Literature
2.
go back to reference Ivanovic Z (2009) Hypoxia or in situ normoxia: The stem cell paradigm. J Cell Physiol 219:271–275CrossRefPubMed Ivanovic Z (2009) Hypoxia or in situ normoxia: The stem cell paradigm. J Cell Physiol 219:271–275CrossRefPubMed
3.
go back to reference Mohyeldin A, Garzon-Muvdi T, Quinones-Hinojosa A (2010) Oxygen in stem cell biology: a critical component of the stem cell niche. Cell Stem Cell 7:150–161CrossRefPubMed Mohyeldin A, Garzon-Muvdi T, Quinones-Hinojosa A (2010) Oxygen in stem cell biology: a critical component of the stem cell niche. Cell Stem Cell 7:150–161CrossRefPubMed
4.
go back to reference Dunwoodie SL (2009) The role of hypoxia in development of the Mammalian embryo. Dev Cell 17:755–773CrossRefPubMed Dunwoodie SL (2009) The role of hypoxia in development of the Mammalian embryo. Dev Cell 17:755–773CrossRefPubMed
5.
6.
go back to reference Rinaudo PF, Giritharan G, Talbi S, Dobson AT, Schultz RM (2006) Effects of oxygen tension on gene expression in preimplantation mouse embryos. Fertil Steril 86:1252–1265, 1265 e1251-1236 CrossRefPubMed Rinaudo PF, Giritharan G, Talbi S, Dobson AT, Schultz RM (2006) Effects of oxygen tension on gene expression in preimplantation mouse embryos. Fertil Steril 86:1252–1265, 1265 e1251-1236 CrossRefPubMed
7.
go back to reference Xie Y, Zhang J, Lin Y, Gaeta X, Meng X, Wisidagama DR, Cinkornpumin J, Koehler CM, Malone CS, Teitell MA, Lowry WE (2014) Defining the role of oxygen tension in human neural progenitor fate. Stem Cell Rep 3:743–757CrossRef Xie Y, Zhang J, Lin Y, Gaeta X, Meng X, Wisidagama DR, Cinkornpumin J, Koehler CM, Malone CS, Teitell MA, Lowry WE (2014) Defining the role of oxygen tension in human neural progenitor fate. Stem Cell Rep 3:743–757CrossRef
8.
go back to reference Wagenfuh L, Meyer AK, Braunschweig L, Marrone L, Storch A (2015) Brain oxygen tension controls the expansion of outer subventricular zone-like basal progenitors in the developing mouse brain. Development 142:2904–2915CrossRef Wagenfuh L, Meyer AK, Braunschweig L, Marrone L, Storch A (2015) Brain oxygen tension controls the expansion of outer subventricular zone-like basal progenitors in the developing mouse brain. Development 142:2904–2915CrossRef
9.
go back to reference Puente BN, Kimura W, Muralidhar SA, Moon J, Amatruda JF, Phelps KL, Grinsfelder D, Rothermel BA, Chen R, Garcia JA, Santos CX, Thet S, Mori E, Kinter MT, Rindler PM, Zacchigna S, Mukherjee S, Chen DJ, Mahmoud AI, Giacca M, Rabinovitch PS, Aroumougame A, Shah AM, Szweda LI, Sadek HA (2014) The oxygen-rich postnatal environment induces cardiomyocyte cell-cycle arrest through DNA damage response. Cell 157:565–579CrossRefPubMedPubMedCentral Puente BN, Kimura W, Muralidhar SA, Moon J, Amatruda JF, Phelps KL, Grinsfelder D, Rothermel BA, Chen R, Garcia JA, Santos CX, Thet S, Mori E, Kinter MT, Rindler PM, Zacchigna S, Mukherjee S, Chen DJ, Mahmoud AI, Giacca M, Rabinovitch PS, Aroumougame A, Shah AM, Szweda LI, Sadek HA (2014) The oxygen-rich postnatal environment induces cardiomyocyte cell-cycle arrest through DNA damage response. Cell 157:565–579CrossRefPubMedPubMedCentral
10.
go back to reference Guimaraes-Camboa N, Stowe J, Aneas I, Sakabe N, Cattaneo P, Henderson L, Kilberg MS, Johnson RS, Chen J, McCulloch AD, Nobrega MA, Evans SM, Zambon AC (2015) HIF1alpha Represses Cell Stress Pathways to Allow Proliferation of Hypoxic Fetal Cardiomyocytes. Dev Cell 33:507–521CrossRefPubMedPubMedCentral Guimaraes-Camboa N, Stowe J, Aneas I, Sakabe N, Cattaneo P, Henderson L, Kilberg MS, Johnson RS, Chen J, McCulloch AD, Nobrega MA, Evans SM, Zambon AC (2015) HIF1alpha Represses Cell Stress Pathways to Allow Proliferation of Hypoxic Fetal Cardiomyocytes. Dev Cell 33:507–521CrossRefPubMedPubMedCentral
11.
go back to reference Eleftheriades M, Creatsas G, Nicolaides K (2006) Fetal growth restriction and postnatal development. Ann NY Acad Sci 1092:319–330CrossRefPubMed Eleftheriades M, Creatsas G, Nicolaides K (2006) Fetal growth restriction and postnatal development. Ann NY Acad Sci 1092:319–330CrossRefPubMed
12.
go back to reference Henriksen T, Clausen T (2002) The fetal origins hypothesis: placental insufficiency and inheritance versus maternal malnutrition in well-nourished populations. Acta Obstet Gynecol Scand 81:112–114CrossRefPubMed Henriksen T, Clausen T (2002) The fetal origins hypothesis: placental insufficiency and inheritance versus maternal malnutrition in well-nourished populations. Acta Obstet Gynecol Scand 81:112–114CrossRefPubMed
13.
go back to reference Stallmach T, Hebisch G, Meier K, Dudenhausen JW, Vogel M (2001) Rescue by birth: defective placental maturation and late fetal mortality. Obstet Gynecol 97:505–509PubMed Stallmach T, Hebisch G, Meier K, Dudenhausen JW, Vogel M (2001) Rescue by birth: defective placental maturation and late fetal mortality. Obstet Gynecol 97:505–509PubMed
14.
go back to reference Kingdom J, Huppertz B, Seaward G, Kaufmann P (2000) Development of the placental villous tree and its consequences for fetal growth. Eur J Obstet Gynecol Reprod Biol 92:35–43CrossRefPubMed Kingdom J, Huppertz B, Seaward G, Kaufmann P (2000) Development of the placental villous tree and its consequences for fetal growth. Eur J Obstet Gynecol Reprod Biol 92:35–43CrossRefPubMed
15.
16.
go back to reference Cosmi E, Fanelli T, Visentin S, Trevisanuto D, Zanardo V (2011) Consequences in infants that were intrauterine growth restricted. J Pregnancy 2011:364381CrossRefPubMedPubMedCentral Cosmi E, Fanelli T, Visentin S, Trevisanuto D, Zanardo V (2011) Consequences in infants that were intrauterine growth restricted. J Pregnancy 2011:364381CrossRefPubMedPubMedCentral
17.
go back to reference Bertram JF, Douglas-Denton RN, Diouf B, Hughson MD, Hoy WE (2011) Human nephron number: implications for health and disease. Pediatr Nephrol 26:1529–1533CrossRefPubMed Bertram JF, Douglas-Denton RN, Diouf B, Hughson MD, Hoy WE (2011) Human nephron number: implications for health and disease. Pediatr Nephrol 26:1529–1533CrossRefPubMed
18.
go back to reference Cebrian C, Asai N, D'Agati V, Costantini F (2014) The number of fetal nephron progenitor cells limits ureteric branching and adult nephron endowment. Cell Rep 7:127–137CrossRefPubMedPubMedCentral Cebrian C, Asai N, D'Agati V, Costantini F (2014) The number of fetal nephron progenitor cells limits ureteric branching and adult nephron endowment. Cell Rep 7:127–137CrossRefPubMedPubMedCentral
19.
20.
go back to reference Luyckx VA, Brenner BM (2015) Birth weight, malnutrition and kidney-associated outcomes--a global concern. Nat Rev Nephrol 11:135–149CrossRefPubMed Luyckx VA, Brenner BM (2015) Birth weight, malnutrition and kidney-associated outcomes--a global concern. Nat Rev Nephrol 11:135–149CrossRefPubMed
22.
go back to reference Swanson AM, David AL (2015) Animal models of fetal growth restriction: Considerations for translational medicine. Placenta 36:623–630CrossRefPubMed Swanson AM, David AL (2015) Animal models of fetal growth restriction: Considerations for translational medicine. Placenta 36:623–630CrossRefPubMed
23.
go back to reference Constancia M, Hemberger M, Hughes J, Dean W, Ferguson-Smith A, Fundele R, Stewart F, Kelsey G, Fowden A, Sibley C, Reik W (2002) Placental-specific IGF-II is a major modulator of placental and fetal growth. Nature 417:945–948CrossRefPubMed Constancia M, Hemberger M, Hughes J, Dean W, Ferguson-Smith A, Fundele R, Stewart F, Kelsey G, Fowden A, Sibley C, Reik W (2002) Placental-specific IGF-II is a major modulator of placental and fetal growth. Nature 417:945–948CrossRefPubMed
24.
go back to reference Dilworth MR, Kusinski LC, Baker BC, Renshall LJ, Baker PN, Greenwood SL, Wareing M, Sibley CP (2012) Crossing mice deficient in eNOS with placental-specific Igf2 knockout mice: a new model of fetal growth restriction. Placenta 33:1052–1054CrossRefPubMedPubMedCentral Dilworth MR, Kusinski LC, Baker BC, Renshall LJ, Baker PN, Greenwood SL, Wareing M, Sibley CP (2012) Crossing mice deficient in eNOS with placental-specific Igf2 knockout mice: a new model of fetal growth restriction. Placenta 33:1052–1054CrossRefPubMedPubMedCentral
25.
go back to reference Sparrow DB, Boyle SC, Sams RS, Mazuruk B, Zhang L, Moeckel GW, Dunwoodie SL, de Caestecker MP (2009) Placental insufficiency associated with loss of Cited1 causes renal medullary dysplasia. J Am Soc Nephrol 20:777–786CrossRefPubMedPubMedCentral Sparrow DB, Boyle SC, Sams RS, Mazuruk B, Zhang L, Moeckel GW, Dunwoodie SL, de Caestecker MP (2009) Placental insufficiency associated with loss of Cited1 causes renal medullary dysplasia. J Am Soc Nephrol 20:777–786CrossRefPubMedPubMedCentral
26.
go back to reference Habli M, Jones H, Aronow B, Omar K, Crombleholme TM (2013) Recapitulation of characteristics of human placental vascular insufficiency in a novel mouse model. Placenta 34:1150–1158CrossRefPubMed Habli M, Jones H, Aronow B, Omar K, Crombleholme TM (2013) Recapitulation of characteristics of human placental vascular insufficiency in a novel mouse model. Placenta 34:1150–1158CrossRefPubMed
27.
go back to reference Larkin J, Chen B, Shi XH, Mishima T, Kokame K, Barak Y, Sadovsky Y (2014) NDRG1 deficiency attenuates fetal growth and the intrauterine response to hypoxic injury. Endocrinology 155:1099–1106CrossRefPubMed Larkin J, Chen B, Shi XH, Mishima T, Kokame K, Barak Y, Sadovsky Y (2014) NDRG1 deficiency attenuates fetal growth and the intrauterine response to hypoxic injury. Endocrinology 155:1099–1106CrossRefPubMed
28.
go back to reference Elvidge GP, Glenny L, Appelhoff RJ, Ratcliffe PJ, Ragoussis J, Gleadle JM (2006) Concordant regulation of gene expression by hypoxia and 2-oxoglutarate-dependent dioxygenase inhibition: the role of HIF-1alpha, HIF-2alpha, and other pathways. J Biol Chem 281:15215–15226CrossRefPubMed Elvidge GP, Glenny L, Appelhoff RJ, Ratcliffe PJ, Ragoussis J, Gleadle JM (2006) Concordant regulation of gene expression by hypoxia and 2-oxoglutarate-dependent dioxygenase inhibition: the role of HIF-1alpha, HIF-2alpha, and other pathways. J Biol Chem 281:15215–15226CrossRefPubMed
29.
go back to reference Greijer AE, van der Groep P, Kemming D, Shvarts A, Semenza GL, Meijer GA, van de Wiel MA, Belien JA, van Diest PJ, van der Wall E (2005) Up-regulation of gene expression by hypoxia is mediated predominantly by hypoxia-inducible factor 1 (HIF-1). J Pathol 206:291–304CrossRefPubMed Greijer AE, van der Groep P, Kemming D, Shvarts A, Semenza GL, Meijer GA, van de Wiel MA, Belien JA, van Diest PJ, van der Wall E (2005) Up-regulation of gene expression by hypoxia is mediated predominantly by hypoxia-inducible factor 1 (HIF-1). J Pathol 206:291–304CrossRefPubMed
30.
go back to reference Hu CJ, Wang LY, Chodosh LA, Keith B, Simon MC (2003) Differential roles of hypoxia-inducible factor 1 alpha (HIF-1 alpha) and HIF-2 alpha in hypoxic gene regulation. Mol Cell Biol 23:9361–9374CrossRefPubMed Hu CJ, Wang LY, Chodosh LA, Keith B, Simon MC (2003) Differential roles of hypoxia-inducible factor 1 alpha (HIF-1 alpha) and HIF-2 alpha in hypoxic gene regulation. Mol Cell Biol 23:9361–9374CrossRefPubMed
31.
go back to reference Manalo DJ, Rowan A, Lavoie T, Natarajan L, Kelly BD, Ye SQ, Garcia JG, Semenza GL (2005) Transcriptional regulation of vascular endothelial cell responses to hypoxia by HIF-1. Blood 105:659–669CrossRefPubMed Manalo DJ, Rowan A, Lavoie T, Natarajan L, Kelly BD, Ye SQ, Garcia JG, Semenza GL (2005) Transcriptional regulation of vascular endothelial cell responses to hypoxia by HIF-1. Blood 105:659–669CrossRefPubMed
32.
go back to reference Wenger RH, Stiehl DP, Camenisch G (2005) Integration of oxygen signaling at the consensus HRE. Sci STKE 2005:re12PubMed Wenger RH, Stiehl DP, Camenisch G (2005) Integration of oxygen signaling at the consensus HRE. Sci STKE 2005:re12PubMed
33.
go back to reference Semenza GL (1999) Regulation of mammalian O2 homeostasis by hypoxia-inducible factor 1. Annu Rev Cell Dev Biol 15:551–578CrossRefPubMed Semenza GL (1999) Regulation of mammalian O2 homeostasis by hypoxia-inducible factor 1. Annu Rev Cell Dev Biol 15:551–578CrossRefPubMed
34.
go back to reference Kato H, Tamamizu-Kato S, Shibasaki F (2004) Histone deacetylase 7 associates with hypoxia-inducible factor 1alpha and increases transcriptional activity. J Biol Chem 279:41966–41974CrossRefPubMed Kato H, Tamamizu-Kato S, Shibasaki F (2004) Histone deacetylase 7 associates with hypoxia-inducible factor 1alpha and increases transcriptional activity. J Biol Chem 279:41966–41974CrossRefPubMed
35.
go back to reference Vacanti NM, Metallo CM (2013) Exploring metabolic pathways that contribute to the stem cell phenotype. Biochim Biophys Acta 1830:2361–2369CrossRefPubMed Vacanti NM, Metallo CM (2013) Exploring metabolic pathways that contribute to the stem cell phenotype. Biochim Biophys Acta 1830:2361–2369CrossRefPubMed
36.
go back to reference Kulsheshtha R, Ferracin M, Wojcik SE, Garzon R, Alder H, Agosto-Perez FJ, Davuluri R, Liu CG, Croce CM, Negrini M, Calin GA, Ivan M (2007) A microRNA signature of hypoxia. Mol Cell Biol 27:1859–1867CrossRef Kulsheshtha R, Ferracin M, Wojcik SE, Garzon R, Alder H, Agosto-Perez FJ, Davuluri R, Liu CG, Croce CM, Negrini M, Calin GA, Ivan M (2007) A microRNA signature of hypoxia. Mol Cell Biol 27:1859–1867CrossRef
38.
go back to reference Pocock R (2011) Invited review: decoding the microRNA response to hypoxia. Pflugers Arch 461:307–315CrossRefPubMed Pocock R (2011) Invited review: decoding the microRNA response to hypoxia. Pflugers Arch 461:307–315CrossRefPubMed
40.
go back to reference Kaelin WG Jr, Ratcliffe PJ (2008) Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol Cell 30:393–402CrossRefPubMed Kaelin WG Jr, Ratcliffe PJ (2008) Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol Cell 30:393–402CrossRefPubMed
41.
go back to reference Gunaratnam L, Bonventre JV (2009) HIF in kidney disease and development. J Am Soc Nephrol 20:1877–1887CrossRefPubMed Gunaratnam L, Bonventre JV (2009) HIF in kidney disease and development. J Am Soc Nephrol 20:1877–1887CrossRefPubMed
42.
go back to reference Bernhardt WM, Schmitt R, Rosenberger C, Munchenhagen PM, Grone HJ, Frei U, Warnecke C, Bachmann S, Wiesener MS, Willam C, Eckardt KU (2006) Expression of hypoxia-inducible transcription factors in developing human and rat kidneys. Kidney Int 69:114–122CrossRef Bernhardt WM, Schmitt R, Rosenberger C, Munchenhagen PM, Grone HJ, Frei U, Warnecke C, Bachmann S, Wiesener MS, Willam C, Eckardt KU (2006) Expression of hypoxia-inducible transcription factors in developing human and rat kidneys. Kidney Int 69:114–122CrossRef
43.
go back to reference Freeburg PB, Robert B, St John PL, Abrahamson DR (2003) Podocyte expression of hypoxia-inducible factor (HIF)-1 and HIF-2 during glomerular development. J Am Soc Nephrol 14:927–938CrossRefPubMed Freeburg PB, Robert B, St John PL, Abrahamson DR (2003) Podocyte expression of hypoxia-inducible factor (HIF)-1 and HIF-2 during glomerular development. J Am Soc Nephrol 14:927–938CrossRefPubMed
44.
go back to reference Iyer NV, Kotch LE, Agani F, Leung SW, Laughner E, Wenger RH, Gassmann M, Gearhart JD, Lawler AM, Yu AY, Semenza GL (1998) Cellular and developmental control of O2 homeostasis by hypoxia-inducible factor 1a. Genes Dev 12:149–162CrossRefPubMedPubMedCentral Iyer NV, Kotch LE, Agani F, Leung SW, Laughner E, Wenger RH, Gassmann M, Gearhart JD, Lawler AM, Yu AY, Semenza GL (1998) Cellular and developmental control of O2 homeostasis by hypoxia-inducible factor 1a. Genes Dev 12:149–162CrossRefPubMedPubMedCentral
46.
go back to reference Freeburg PB, Abrahamson DR (2004) Divergent expression patterns for hypoxia-inducible factor-1beta and aryl hydrocarbon receptor nuclear transporter-2 in developing kidney. J Am Soc Nephrol 15:2569–2578CrossRefPubMed Freeburg PB, Abrahamson DR (2004) Divergent expression patterns for hypoxia-inducible factor-1beta and aryl hydrocarbon receptor nuclear transporter-2 in developing kidney. J Am Soc Nephrol 15:2569–2578CrossRefPubMed
47.
go back to reference Maltepe E, Schmidt JV, Baunoch D, Bradfield CA, Simon MC (1997) Abnormal angiogenesis and responses to glucose and oxygen deprivation in mice lacking the protein ARNT. Nature 386:403–407CrossRefPubMed Maltepe E, Schmidt JV, Baunoch D, Bradfield CA, Simon MC (1997) Abnormal angiogenesis and responses to glucose and oxygen deprivation in mice lacking the protein ARNT. Nature 386:403–407CrossRefPubMed
49.
go back to reference Tsuji K, Kitamura S, Makino H (2014) Hypoxia-inducible factor 1alpha regulates branching morphogenesis during kidney development. Biochem Biophys Res Commun 447:108–114CrossRef Tsuji K, Kitamura S, Makino H (2014) Hypoxia-inducible factor 1alpha regulates branching morphogenesis during kidney development. Biochem Biophys Res Commun 447:108–114CrossRef
50.
go back to reference Schley G, Scholz H, Kraus A, Hackenbeck T, Klanke B, Willam C, Wiesener MS, Heinze E, Burzlaff N, Eckardt KU, Buchholz B (2015) Hypoxia inhibits nephrogenesis through paracrine Vegfa despite the ability to enhance tubulogenesis. Kidney Int 88:1283–1292CrossRefPubMed Schley G, Scholz H, Kraus A, Hackenbeck T, Klanke B, Willam C, Wiesener MS, Heinze E, Burzlaff N, Eckardt KU, Buchholz B (2015) Hypoxia inhibits nephrogenesis through paracrine Vegfa despite the ability to enhance tubulogenesis. Kidney Int 88:1283–1292CrossRefPubMed
51.
go back to reference Wilkinson LJ, Neal CS, Singh RR, Sparrow DB, Kurniawan ND, Ju A, Grieve SM, Dunwoodie SL, Moritz KM, Little MH (2015) Renal developmental defects resulting from in utero hypoxia are associated with suppression of ureteric beta-catenin signaling. Kidney Int 87:975–983CrossRefPubMed Wilkinson LJ, Neal CS, Singh RR, Sparrow DB, Kurniawan ND, Ju A, Grieve SM, Dunwoodie SL, Moritz KM, Little MH (2015) Renal developmental defects resulting from in utero hypoxia are associated with suppression of ureteric beta-catenin signaling. Kidney Int 87:975–983CrossRefPubMed
52.
go back to reference Rymer C, Paredes J, Halt K, Schaefer C, Wiersch J, Zhang G, Potoka D, Vainio S, Gittes GK, Bates CM, Sims-Lucas S (2014) Renal blood flow and oxygenation drive nephron progenitor differentiation. Am J Physiol Renal Physiol 307:F337–345CrossRefPubMedPubMedCentral Rymer C, Paredes J, Halt K, Schaefer C, Wiersch J, Zhang G, Potoka D, Vainio S, Gittes GK, Bates CM, Sims-Lucas S (2014) Renal blood flow and oxygenation drive nephron progenitor differentiation. Am J Physiol Renal Physiol 307:F337–345CrossRefPubMedPubMedCentral
53.
go back to reference Xia S, Lv J, Gao Q, Li L, Chen N, Wei X, Xiao J, Chen J, Tao J, Sun M, Mao C, Zhang L, Xu Z (2015) Prenatal exposure to hypoxia induced Beclin 1 signaling-mediated renal autophagy and altered renal development in rat fetuses. Reprod Sci 22:156–164CrossRefPubMedPubMedCentral Xia S, Lv J, Gao Q, Li L, Chen N, Wei X, Xiao J, Chen J, Tao J, Sun M, Mao C, Zhang L, Xu Z (2015) Prenatal exposure to hypoxia induced Beclin 1 signaling-mediated renal autophagy and altered renal development in rat fetuses. Reprod Sci 22:156–164CrossRefPubMedPubMedCentral
55.
go back to reference Boyle SC, Kim M, Valerius MT, McMahon AP, Kopan R (2011) Notch pathway activation can replace the requirement for Wnt4 and Wnt9b in mesenchymal-to-epithelial transition of nephron stem cells. Development 138:4245–4254CrossRefPubMedPubMedCentral Boyle SC, Kim M, Valerius MT, McMahon AP, Kopan R (2011) Notch pathway activation can replace the requirement for Wnt4 and Wnt9b in mesenchymal-to-epithelial transition of nephron stem cells. Development 138:4245–4254CrossRefPubMedPubMedCentral
56.
go back to reference Karner CM, Das A, Ma Z, Self M, Chen C, Lum L, Oliver G, Carroll TJ (2011) Canonical Wnt9b signaling balances progenitor cell expansion and differentiation during kidney development. Development 138:1247–1257CrossRefPubMedPubMedCentral Karner CM, Das A, Ma Z, Self M, Chen C, Lum L, Oliver G, Carroll TJ (2011) Canonical Wnt9b signaling balances progenitor cell expansion and differentiation during kidney development. Development 138:1247–1257CrossRefPubMedPubMedCentral
57.
go back to reference Gustafsson MV, Zheng X, Pereira T, Gradin K, Jin S, Lundkvist J, Ruas JL, Poellinger L, Lendahl U, Bondesson M (2005) Hypoxia requires notch signaling to maintain the undifferentiated cell state. Dev Cell 9:617–628CrossRefPubMed Gustafsson MV, Zheng X, Pereira T, Gradin K, Jin S, Lundkvist J, Ruas JL, Poellinger L, Lendahl U, Bondesson M (2005) Hypoxia requires notch signaling to maintain the undifferentiated cell state. Dev Cell 9:617–628CrossRefPubMed
58.
go back to reference Fujimura S, Jiang Q, Kobayashi C, Nishinakamura R (2010) Notch2 activation in the embryonic kidney depletes nephron progenitors. J Am Soc Nephrol 21:803–810CrossRefPubMedPubMedCentral Fujimura S, Jiang Q, Kobayashi C, Nishinakamura R (2010) Notch2 activation in the embryonic kidney depletes nephron progenitors. J Am Soc Nephrol 21:803–810CrossRefPubMedPubMedCentral
59.
go back to reference Briscoe TA, Rehn AE, Dieni S, Duncan JR, Wlodek ME, Owens JA, Rees SM (2004) Cardiovascular and renal disease in the adolescent guinea pig after chronic placental insufficiency. Am J Obstet Gynecol 191:847–855CrossRefPubMed Briscoe TA, Rehn AE, Dieni S, Duncan JR, Wlodek ME, Owens JA, Rees SM (2004) Cardiovascular and renal disease in the adolescent guinea pig after chronic placental insufficiency. Am J Obstet Gynecol 191:847–855CrossRefPubMed
60.
go back to reference Moritz KM, Mazzuca MQ, Siebel AL, Mibus A, Arena D, Tare M, Owens JA, Wlodek ME (2009) Uteroplacental insufficiency causes a nephron deficit, modest renal insufficiency but no hypertension with ageing in female rats. J Physiol 587:2635–2646CrossRefPubMedPubMedCentral Moritz KM, Mazzuca MQ, Siebel AL, Mibus A, Arena D, Tare M, Owens JA, Wlodek ME (2009) Uteroplacental insufficiency causes a nephron deficit, modest renal insufficiency but no hypertension with ageing in female rats. J Physiol 587:2635–2646CrossRefPubMedPubMedCentral
61.
go back to reference Figueroa H, Lozano M, Suazo C, Eixarch E, Illanes SE, Carreno JE, Villanueva S, Hernandez-Andrade E, Gratacos E, Irarrazabal CE (2012) Intrauterine growth restriction modifies the normal gene expression in kidney from rabbit fetuses. Early Hum Dev 88:899–904CrossRefPubMed Figueroa H, Lozano M, Suazo C, Eixarch E, Illanes SE, Carreno JE, Villanueva S, Hernandez-Andrade E, Gratacos E, Irarrazabal CE (2012) Intrauterine growth restriction modifies the normal gene expression in kidney from rabbit fetuses. Early Hum Dev 88:899–904CrossRefPubMed
Metadata
Title
Role of hypoxia during nephrogenesis
Authors
Shelby L. Hemker
Sunder Sims-Lucas
Jacqueline Ho
Publication date
01-10-2016
Publisher
Springer Berlin Heidelberg
Published in
Pediatric Nephrology / Issue 10/2016
Print ISSN: 0931-041X
Electronic ISSN: 1432-198X
DOI
https://doi.org/10.1007/s00467-016-3333-5

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