Renin-angiotensin system in ureteric bud branching morphogenesis: Implications for kidney disease

Pediatric Nephrology

Volumn 29, Issue 4, 2014, Pages 609-620

  Yosypiv, Ihor V ^a  

^a TULANE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

Author keywords

Cakut; Kidney development; Prorenin receptor; Renin angiotensin; Ureteric bud

Indexed keywords

ANGIOTENSIN; ANGIOTENSIN II; ANGIOTENSINOGEN; AQUAPORIN 2; PRORENIN RECEPTOR; PROTEIN TYROSINE KINASE; RENIN; VASOPRESSIN;

BRANCHING MORPHOGENESIS; CELL PROLIFERATION; CELL SURVIVAL; CONFERENCE PAPER; DNA MODIFICATION; ENDOTHELIUM CELL; ENZYME ACTIVATION; EPIGENETICS; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HYDRONEPHROSIS; IMMUNOREACTIVITY; KIDNEY CONCENTRATING CAPACITY; KIDNEY DEVELOPMENT; KIDNEY DISEASE; KIDNEY FUNCTION; KIDNEY HYPOPLASIA; KIDNEY MALFORMATION; KIDNEY MEDULLA; KIDNEY PROXIMAL TUBULE; MESANGIUM; MULTICYSTIC DYSPLASTIC KIDNEY; NONHUMAN; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; URETER; URETER BUD; URINARY TRACT MALFORMATION; URINARY TRACT OBSTRUCTION; URINE ACIDIFICATION;

ANIMALS; HUMANS; KIDNEY; KIDNEY DISEASES; MORPHOGENESIS; RENIN-ANGIOTENSIN SYSTEM; URETER; UROGENITAL ABNORMALITIES;

EID: 84896709636     PISSN: 0931041X     EISSN: 1432198X     Source Type: Journal    
DOI: 10.1007/s00467-013-2616-3     Document Type: Conference Paper

References (105)

1. Reidy KJ, Rosenblum ND (2009) Cell and molecular biology of kidney development. Semin Nephrol 29:321-337
2. Dressler GR (2008) Epigenetics, development, and the kidney. J Am Soc Nephrol 19:2060-2067
3. Costantini F, Kopan R (2010) Patterning a complex organ: Branching morphogenesis and nephron segmentation in kidney development. Dev Cell 18:698-712
4. North American Pediatric Renal Trials and Collaborative Studies (2010) NAPRTCS 2010 annual report. Available at: https://web.emmes.com/study/ped/ annlrept/2010-Report.pdf
5. Nagata M, Tanimoto K, Fukamizu A, Kon Y, Sugiyama F, Yagami K, Murakami K, Watanabe T (1996) Nephrogenesis and renovascular development in angiotensinogen-deficient mice. Lab Invest 75:745-753
6. Niimura F, Labosky PA, Kakuchi J, Okubo S, Yoshida H, Oikawa T, Ichiki T, Naftilan AJ, Fogo A, Inagami T (1995) Gene targeting in mice reveals a requirement for angiotensin in the development and maintenance of kidney morphology and growth factor regulation. J Clin Invest 96:2947-2954
7. Takahashi N, Lopez ML, Co Whig JE, Jr TMA, Hatada T, Riggs E, Lee G, Gomez RA, Kim HS, Smithies O (2005) Ren1c homozygous null mice are hypotensive and polyuric, but heterozygotes are indistinguishable from wild-type. J Am Soc Nephrol 16:125-132
8. Esther CR Jr, Howard TE, Marino EM, Goddard JM, Capecchi MR, Bernstein KE (1996) Mice lacking angiotensin-converting enzyme have low blood pressure, renal pathology, and reduced male fertility. Lab Invest 7:953-965
9. 1B receptors for angiotensin II. Proc Natl Acad Sci USA 95:15496-15501
10. Tsuchida S, Matsusaka T, Chen X, Okubo S, Niimura F, Nishimura H, Fogo A, Utsunomiya H, Inagami T, Ichikawa I (1998) Murine double nullizygotes of the angiotensin type 1A and 1B receptor genes duplicate severe abnormal phenotypes of angiotensinogen nullizygotes. J Clin Invest 101:755-760
11. Miyazaki Y, Tsuchida S, Fogo A, Ichikawa I (1999) The renal lesions that develop in neonatal mice during angiotensin inhibition mimic obstructive nephropathy. Kidney Int 55:1683-1695
12. Wolf G, Thaiss F, Schoeppe W, Stahl RA (1992) Angiotensin II-induced proliferation of cultured murine mesangial cells: inhibitory role of atrial natriuretic peptide. J Am Soc Nephrol 3:1270-1278
13. Goto M, Mukoyama M, Suga S, Matsumoto T, Nakagawa M, Ishibashi R, Kasahara M, Sugawara A, Tanaka I, Nakao K (1997) Growth-dependent induction of angiotensin II type 2 receptor in rat mesangial cells. Hypertension 30:358-362
14. Nguyen G, Delarue F, Burcklé C, Bouzhir L, Giller T, Sraer JD (2002) Pivotal role of the renin/prorenin receptor in angiotensin II production and cellular responses to renin. J Clin Invest 109:1417-1427
15. Cousin C, Bracquart D, Contrepas A, Corvol P, Muller L, Nguyen G (2009) Soluble form of the (pro)renin receptor generated by intracellular cleavage by furin is secreted in plasma. Hypertension 53:1077-1082
16. Santos RA, Simoes E, Silva AC, Maric C, Silva DM, Machado RP, de Buhr I, Heringer-Walther S, Pinheiro SV, Lopes MT, Bader M, Mendes EP, Lemos VS, Campagnole-Santos MJ, Schultheiss HP, Speth R, Walther T (2003) Angiotensin-(1-7) is an endogenous ligand for the G protein-coupled receptor Mas. Proc Natl Acad Sci USA 100:8258-8263
17. Darby IA, Sernia C (1995) In situ hybridization and immunohistochemistry of renal angiotensinogen in neonatal and adult rat kidneys. Cell Tissue Res 281:197-206
18. Niimura F, Okubo S, Fogo A, Ichikawa I (1997) Temporal and spatial expression pattern of the angiotensinogen gene in mice and rats. Am J Physiol 272:R142-R147
19. Prieto M, Dipp S, Meleg-Smith S, El-Dahr SS (2001) Ureteric bud derivatives express angiotensinogen and AT1 receptors. Physiol Genomics 6:29-37
20. Iosipiv IV, Schroeder M (2003) A role for angiotensin II AT1 receptors in ureteric bud cell branching. Am J Physiol 285:F199-F207
21. Schutz S, Le Moullec J-M, Corvol P, Gasc JM (1996) Early expression of all the components of the renin-angiotensin sytem in human development. Am J Pathol 149:2067-2079
22. Jones CA, Sigmund CD, McGowan RA, Kane-Haas CM, Gross KW (1990) Expression of murine renin genes during fetal development. Mol Endocrinol 4:375-383
23. Gomez RA, Lynch KR, Sturgill BC, Elwood JP, Chevalier RL, Carey RM, Peach MJ (1989) Distribution of renin mRNA and its protein in the developing kidney. Am J Physiol 257:F850-F858
24. Song R, Preston G, Yosypiv IV (2013) Ontogeny of the prorenin receptor. Pediatr Res 74:5-10
25. Song R, Preston G, Ichihara A, Yosypiv IV (2013) Deletion of the prorenin receptor from the ureteric bud causes renal hypodysplasia. PLoS ONE 8:e63835
26. Jung FF, Bouyounes B, Barrio R, Tang SS, Diamant D, Ingelfinger JR (1993) Angiotensin converting enzyme in renal ontogeny: Hypothesis for multiple roles. Pediatr Nephrol 7:834-840
27. 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 32:684-690
28. Kakuchi J, Ichiki T, Kiyama S, Hogan BL, Fogo A, Inagami T, Ichikawa I (1995) Developmental expression of renal angiotensin II receptor genes in the mouse. Kidney Int 47:140-147
29. Garcia-Villalba P, Denkers ND, Wittwer CT, Hoff C, Nelson RD, Mauch TJ (2003) Real-time PCR quantification of AT1 and AT2 angiotensin receptor mRNA expression in the developing rat kidney. Nephron Exp Nephrol 94:e154-e159
30. Song R, Spera M, Garrett C, El-Dahr SS, Yosypiv IV (2010) Angiotensin II AT2 receptor regulates ureteric bud morphogenesis. Am J Physiol 298:F807-F817
31. O'Rahilly R, Müller F (2010) Developmental stages in human embryos: Revised and new measurements. Cells Tissues Organs 192:73-84
32. Yosipiv IV, Dipp S, El-Dahr SS (1994) Ontogeny of somatic angiotensin-converting enzyme. Hypertension 23:369-374
33. Miyazaki Y, Tsuchida S, Nishimura H, Pope JC IV, Harris RC, McKanna JM, Inagami T, Hogan BL, Fogo A, Ichikawa I (1998) Angiotensin induces the urinary peristaltic machinery during the perinatal period. J Clin Invest 102:1489-1497
34. Friberg P, Sundelin B, Bohman SO, Bobik A, Nilsson H, Wickman A, Gustafsson H, Petersen J, Adams MA (1994) renin-angiotensin system in neonatal rats: Induction of a renal abnormality in response to ACE inhibition or angiotensin II antagonism. Kidney Int 45:485-492
35. Guron G, Adams MA, Sundelin B, Friberg P (1997) Neonatal angiotensin-converting enzyme inhibition in the rat induces persistent abnormalities in renal function and histology. Hypertension 29:91-97
36. Madsen K, Marcussen N, Pedersen M, Kjaersgaard G, Facemire C, Coffman TM, Jensen BL (2010) Angiotensin II promotes development of the renal microcirculation through AT1 receptors. J Am Soc Nephrol 21:448-459
37. Guron G, Marcussen N, Nilsson A, Sundelin B, Friberg P (1999) Postnatal time frame for renal vulnerability to enalapril in rats. J Am Soc Nephrol 10:1550-1560
38. 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 22:2203-2212
39. Riediger F, Quack I, Qadri F, Hartleben B, Park JK, Potthoff SA, Sohn D, Sihn G, Rousselle A, Fokuhl V, Maschke U, Purfürst 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 22:2193-2202
40. Stegbauer J, Gurley SB, Sparks MA, Woznowski M, Kohan DE, Yan M, Lehrich RW, Coffman TM (2011) AT1 receptors in the collecting duct directly modulate the concentration of urine. J Am Soc Nephrol 22:2237-2246
41. Song R, Preston G, Khalili A, El-Dahr SS, Yosypiv IV (2012) Angiotensin II regulates growth of the developing papillas ex vivo. Am J Physiol 302:F1112-F1120
42. Oshima K, Miyazaki Y, Brock JW, Adams MC, Ichikawa I, Pope JC (2001) Angiotensin type II receptor expression and ureteral budding. J Urol 166:1848-1852
43. Kriz W (1981) Structural organization of the renal medulla: comparative and functional aspects. Am J Physiol 241:R3-R16
44. Oliverio MI, Delnomdedieu M, Best CF, Li P, Morris M, Callahan MF, Johnson GA, Smithies O, Coffman TM (2000) Abnormal water metabolism in mice lacking the type 1A receptor for ANG II. Am J Physiol 278:F75-82
45. Brooks HL, Allred AJ, Beutler KT, Coffman TM, Knepper MA (2002) Targeted proteomic profiling of renal Na(+) transporter and channel abundances in angiotensin II type 1a receptor knockout mice. Hypertension 39:470-473
46. Li XC, Shao Y, Zhuo JL (2012) AT1a receptor signaling is required for basal and water deprivation-induced urine concentration in AT1a receptor-deficient mice. Am J Physiol Renal Physiol 303:F746-F756
47. Weiner ID, New AR, Milton AE, Tisher CC (1995) Regulation of luminal alkalinization and acidification in the cortical collecting duct by angiotensin II. Am J Physiol 269:F730-F738
48. Tojo A, Tisher CC, Madsen KM (1994) Angiotensin II regulates H(+)-ATPase activity in rat cortical collecting duct. Am J Physiol 267:F1045-F1051
49. Advani A, Kelly DJ, Cox AJ, White KE, Advani SL, Thai K, Connelly KA, Yuen D, Trogadis J, Herzenberg AM, Kuliszewski MA, Leong-Poi H, Gilbert RE (2009) The (Pro) renin receptor site-specific and functional linkage to the vacuolar H(+)-ATPase in the Kidney. Hypertension 54:261-269
50. 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 57:859-864
51. Cruciat CM, Ohkawara B, Acebron SP, Karaulanov E, Reinhard C, Ingelfinger D, Boutros M, Niehrs C (2010) Requirement of prorenin receptor and vacuolar H(+)-ATPase-mediated acidification for Wnt signaling. Science 327:459-463
52. Stover EH, Borthwick KJ, Bavalia C, Eady N, Fritz DM, Rungroj N, Giersch AB, Morton CC, Axon PR, Akil I, Al-Sabban EA, Baguley DM, Bianca S, Bakkaloglu A, Bircan Z, Chauveau D, Clermont MJ, Guala A, Hulton SA, Kroes H, Li Volti G, Mir S, Mocan H, Nayir A, Ozen S, Rodriguez Soriano J, Sanjad SA, Tasic V, Taylor CM, Topaloglu R, Smith AN, Karet FE (2002) Novel ATP6V1B1 and ATP6V0A4 mutations in autosomal recessive distal renal tubular acidosis with new evidence for hearing loss. J Med Genet 39:796-803
53. Lopez ML, Pentz ES, Robert B, Abrahamson DR, Gomez RA (2001) Embryonic origin and lineage of juxtaglomerular cells. Am J Physiol 281:F345-F356
54. Song R, Preston G, Yosypiv IV (2011) Angiotensin II stimulates in vitro branching morphogenesis of the isolated ureteric bud. Mech Dev 128:359-367
55. Yoshikawa A, Aizaki Y, Kusano K, Kishi F, Susumu T, Iida S, Ishiura S, Nishimura S, Shichiri M, Senbonmatsu T (2011) The (pro)renin receptor is cleaved by ADAM19 in the Golgi leading to its secretion into extracellular space. Hypertens Res 34:599-605
56. Schaefer C (2003) Angiotensin II-receptor-antagonists: Further evidence of fetotoxicity but not teratogenicity. Part A Clin Mol Teratol Birth Defects Res 67:591-594
57. Tabacova S, Little R, Tsong Y, Vega A, Kimmel CA (2003) Adverse pregnancy outcomes associated with maternal enalapril antihypertensive treatment. Pharmacoepidemiol Drug Saf 12:633-646
58. Gribouval O, Gonzales M, Neuhaus T (2005) Mutations in genes in the renin-angiotensin system are associated with autosomal recessive renal tubular dysgenesis. Nat Genet 37:964-968
59. Gribouval O, Morinière V, Pawtowski A, Arrondel C, Sallinen SL, Saloranta C, Clericuzio C, Viot G, Tantau J, Blesson S, Cloarec S, Machet MC, Chitayat D, Thauvin C, Laurent N, Sampson JR, Bernstein JA, Clemenson A, Prieur F, Daniel L, Levy-Mozziconacci A, Lachlan K, Alessandri JL, Cartault F, Rivière JP, Picard N, Baumann C, Delezoide AL, Belar Ortega M, Chassaing N, Labrune P, Yu S, Firth H, Wellesley D, Bitzan M, Alfares A, Braverman N, Krogh L, Tolmie J, Gaspar H, Doray B, Majore S, Bonneau D, Triau S, Loirat C, David A, Bartholdi D, Peleg A, Brackman D, Stone R, DeBerardinis R, Corvol P, Michaud A (2012) Spectrum of mutations in the renin-angiotensin system genes in autosomal recessive renal tubular dysgenesis. Hum Mutat 33:316-326
60. Uematsu M, Sakamoto O, Nishio T, Ohura T, Matsuda T, Inagaki T, Abe T, Okamura K, Kondo Y, Tsuchiya S (2006) A case surviving for over a year of renal tubular dysgenesis with compound heterozygous angiotensinogen gene mutations. Am J Med Genet Part A 140:2355-2360
61. Uematsu M, Sakamoto O, Ohura T, Shimizu N, Satomura K, Tsuchiya S (2009) A further case of renal tubular dysgenesis surviving the neonatal period. Eur J Pediatr 168:207-209
62. Lacoste M, Cai Y, Guicharnaud L, Mounier F, Dumez Y, Bouvier R, Dijoud F, Gonzales M, Chatten J, Delezoide AL, Daniel L, Joubert M, Laurent N, Aziza J, Sellami T, Amar HB, Jarnet C, Frances AM, Daïkha-Dahmane F, Coulomb A, Neuhaus TJ, Foliguet B, Chenal P, Marcorelles P, Gasc JM, Corvol P, Gubler MC (2006) Renal tubular dysgenesis, a not uncommon autosomal recessive disorder leading to oligohydramnios: Role of the renin-angiotensin system. J Am Soc Nephrol 17:2253-2263
63. Zingg-Schenk A, Bacchetta J, Corvol P, Michaud A, Stallmach T, Cochat P, Gribouval O, Gubler MC, Neuhaus TJ (2008) Inherited renal tubular dysgenesis: The first patients surviving the neonatal period. Eur J Pediatr 167:311-316
64. Nishimura H, Yerkes E, Hohenfellner K, Miyazaki Y, Ma J, Hunley TE, Yoshida H, Ichiki T, Threadgill D, Phillips JA III, Hogan BM, Fogo A, Brock JW III (1999) Role of the angiotensin type 2 receptor gene in congenital anomalies of the kidney and urinary tract, CAKUT, of mice and men. Mol Cell 3:1-10
65. Hahn H, Ku SE, Kim KS, Park YS, Yoon CH, Cheong HI (2005) Implication of genetic variations in congenital obstructive nephropathy. Pediatr Nephrol 20:1541-1544
66. Rigoli L, Chimenz R, di Bella C, Cavallaro E, Caruso R, Briuglia S, Fede C, Salpietro CD (2004) Angiotensin-converting enzyme and angiotensin type 2 receptor gene genotype distributions in Italian children with congenital uropathies. Pediatr Res 56:988-993
67. Stanković A, Zivković M, Kostić M, Atanacković J, Krstić Z, Alavantić D (2010) Expression profiling of the AT2R mRNA in affected tissue from children with CAKUT. Clin Biochem 43:71-75
68. Cordell HJ, Darlay R, Charoen P, Stewart A, Gullett AM, Lambert HJ, Malcolm S, Feather SA, Goodship TH, Woolf AS, Kenda RB, Goodship JA, UK VUR Study (2010) Whole-genome linkage and association scan in primary, nonsyndromic vesicoureteric reflux. J Am Soc Nephrol 21:113-123
69. Peruzzi L, Lombardo F, Amore A, Merlini E, Restagno G, Silvestro L, PapaliaT CR (2005) Low renin-angiotensin system activity gene polymorphism and dysplasia associated with posterior urethral valves. J Urol 174:713-717
70. Song R, Van Buren T, Yosypiv IV (2010) Histone deacetylases are critical regulators of the renin-angiotensin system during ureteric bud branching morphogenesis. Pediatr Res 67:573-578
71. Zhang SL, Moini B, Ingelfinger JR (2004) Angiotensin II increases Pax-2 expression in fetal kidney cells via the AT2 receptor. J Am Soc Nephrol 15:1452-1465
72. Yosypiv IV, Boh MK, Spera M, El-Dahr SS (2008) Down regulation of Spry-1, an inhibitor of GDNF/Ret, as a mechanism for angiotensin II-induced ureteric bud branching. Kidney Int 74:1287-1293
73. Basson MA, Akbulut S, Watson-Johnson J, Simon R, Carroll TJ, Shakya R, Gross I, Martin GR, Lufkin T, McMahon AP, Wilson PD, Costantini FD, Mason IJ, Licht JD (2005) Sprouty1 is a critical regulator of GDNF/RET-mediated kidney induction. Dev Cell 8:229-239
74. Basson MA, Watson-Johnson J, Shakya R, Akbulut S, Hyink D, Costantini FD, Wilson PD, Mason IJ, Licht JD (2006) Branching morphogenesis of the ureteric epithelium during kidney development is coordinated by the opposing functions of GDNF and Sprouty1. Dev Biol 299:466-477
75. Chatterjee R, Ramos E, Hoffman M, VanWinkle J, Martin DR, Davis TK, Hoshi M, Hmiel SP, Beck A, Hruska K, Coplen D, Liapis H, Mitra R, Druley T, Austin P (2012) Traditional and targeted exome sequencing reveals common, rare and novel functional deleterious variants in RET-signaling complex in a cohort of living US patients with urinary tract malformations. Hum Genet Nov 131(11):1725-38
76. Skinner MA, Safford SD, Reeves JG, Jackson ME, Freemerman AJ (2008) Renal aplasia in humans is associated with RET mutations. Am J Hum Genet 82:344-351
77. Porteous S, Torban E, Cho NP, Cunliffe H, Chua L, McNoe L, Ward T, Souza C, Gus P, Giugliani R, Sato T, Yun K, Favor J, Sicotte M, Goodyer P, Eccles M (2000) Primary renal hypoplasia in humans and mice with PAX2 mutations: Evidence of increased apoptosis in fetal kidneys of Pax2(1Neu) +/- mutant mice. Hum Mol Genet 9:1-11
78. Buechling T, Bartscherer K, Ohkawara B, Chaudhary V, Spirohn K, Niehrs C, Boutros M (2010) Wnt/frizzled signaling requires dPRR, the drosophila homolog of the prorenin receptor. Curr Biol 20:1263-1268
79. Karner CM, Chirumamilla R, Aoki S, Igarashi P, Wallingford JB, Carroll TJ (2009) Wnt9b signaling regulates planar cell polarity and kidney tubule morphogenesis. Nat Genet 41:793-799
80. Yu J, Carroll TJ, Rajagopal J, Kobayashi A, Ren Q, McMahon AP (2009) A Wnt7b-dependent pathway regulates the orientation of epithelial cell division and establishes the cortico-medullary axis of the mammalian kidney. Development 136:161-171
81. Carroll TJ, Park JS, Hayashi S, Majumdar A, McMahon AP (2005) Wnt9b plays a central role in the regulation of mesenchymal to epithelial transitions underlying organogenesis of the mammalian urogenital system. Dev Cell 9:283-292
82. Lin Y, Liu A, Zhang S, Ruusunen T, Kreidberg JA, Peltoketo H, Drummond I, Vainio S (2001) Induction of ureter branching as a response to Wnt-2b signaling during early kidney organogenesis. Dev Dyn 222:26-39
83. Lange C, Prenninger S, Knuckles P, Taylor V, Levin M, Calegari F (2011) The H(+) vacuolar ATPase maintains neural stem cells in the developing mouse cortex. Stem Cells Dev 20:843-850
84. Jeong HW, Jeon US, Koo BK, Kim WY, Im SK, Shin J, Cho Y, Kim J, Kong YY (2009) Inactivation of Notch signaling in the renal collecting duct causes nephrogenic diabetes insipidus in mice. J Clin Invest 119:3290-3300
85. Hermle T, Guida MC, Beck S, Helmstädter S, Simons M (2013) Drosophila ATP6AP2/VhaPRR functions both as a novel planar cell polarity core protein and a regulator of endosomal trafficking. EMBO J 32:245-259
86. Yan Y, Denef N, Schüpbach T (2009) The vacuolar proton pump, V-ATPase, is required for notch signaling and endosomal trafficking in Drosophila. Dev Cell 17:387-402
87. Schefe JH, Menk M, Reinemund J, Effertz K, Hobbs RM, Pandolfi PP, Ruiz P, Unger T, Funke-Kaiser H (2006) A novel signal transduction cascade involving direct physical interaction of the renin/prorenin receptor with the transcription factor promyelocytic zinc finger protein. Circ Res 99:1355-1366
88. Song R, Spera M, Garrett C, Yosypiv IV (2010) Angiotensin II-induced activation of c-Ret signaling is critical in ureteric bud branching morphogenesis. Mech Dev 127:21-27
89. Schmidt-Ott KM, Masckauchan TN, Chen X, Hirsh BJ, Sarkar A, Yang J, Paragas N, Wallace VA, Dufort D, Pavlidis P, Jagla B, Kitajewski J, Barasch J (2007) βeta-catenin/TCF/Lef controls a differentiation-associated transcriptional program in renal epithelial progenitors. Development 134:3177-90
90. Filipponi D, Hobbs RM, Ottolenghi S, Rossi P, Jannini EA, Pandolfi PP, Dolci S (2007) Repression of kit expression by Plzf in germ cells. Mol Cell Biol 27:6770-6781
91. Spinello I, Quaranta MT, Pasquini L, Pelosi E, Petrucci E, Pagliuca A, Castelli G, Mariani G, Diverio D, Foà R, Testa U, Labbaye C (2009) PLZF-mediated control on c-kit expression in CD34(+) cells and early erythropoiesis. Oncogene 28:2276-88
92. Jain S, Knoten A, Hoshi M, Wang H, Vohra B, Heuckeroth RO, Milbrandt J (2010) Organotypic specificity of key RET adaptor-docking sites in the pathogenesis of neurocristopathies and renal malformations in mice. J Clin Invest 120:778-790
93. Besset V, Scott RP, Ibáñez CF (2000) Signaling complexes and protein-protein interactions involved in the activation of the Ras and phosphatidylinositol 3-kinase pathways by the c-Ret receptor tyrosine kinase. J Biol Chem 275:39159-39166
94. Hoshi M, Batourina E, Mendelsohn C, Jain S (2012) Novel mechanisms of early upper and lower urinary tract patterning regulated by RetY1015 docking tyrosine in mice. Development 139:2405-2415
95. Tang MJ, Cai Y, Tsai SJ, Wang YK, Dressler GR (2002) Ureteric bud outgrowth in response to RET activation is mediated by phosphatidylinositol 3-kinase. Dev Biol 243:128-136
96. Kim D, Dressler GR (2007) PTEN modulates GDNF/RET mediated chemotaxis and branching morphogenesis in the developing kidney. Dev Biol 307:290-299
97. Fisher CE, Michael L, Barnett MW, Davies JA (2001) Erk MAP kinase regulates branching morphogenesis in the developing mouse kidney. Development 128:4329-4338
98. 1R-EGFR crosstalk regulates ureteric bud branching morphogenesis. J Am Soc Nephrol 17:1005-1014
99. Michael L, Davies JA (2004) Pattern and regulation of cell proliferation during murine ureteric bud development. J Anat 204:241-255
100. Dziarmaga A, Eccles M, Goodyer P (2006) Suppression of ureteric bud apoptosis rescues nephron endowment and adult renal function in Pax2 mutant mice. J Am Soc Nephrol 17:1568-1575
101. Kuure S, Chi X, Lu B, Costantini F (2010) The transcription factors Etv4 and Etv5 mediate formation of the ureteric bud tip domain during kidney development. Development 137:1975-1979
102. Patel SR, Kim D, Levitan I, Dressler GR (2007) The BRCT-domain containing protein PTIP links PAX2 to a histone H3, lysine 4 methyltransferase complex. Dev Cell 13:580-592
103. Chen S, Bellew C, Yao X, Stefkova J, Dipp S, Saifudeen Z, Bachvarov D, El-Dahr SS (2011) Histone deacetylase (HDAC) activity is critical for embryonic kidney gene expression, growth, and differentiation. J Biol Chem 286:32775-32789
104. Gomez RA, Pentz ES, Jin X, Cordaillat M, Sequeira Lopez ML (2009) CBP and p300 are essential for renin cell identity and morphological integrity of the kidney. Am J Physiol 296:H1255-H1262
105. Norwood VF, Craig MR, Harris JM, Gomez RA (1997) Differential expression of angiotensin II receptors during early renal morphogenesis. Am J Physiol 272:R662-R668