Top

Published in:

Open Access 01-10-2007 | Review

Genetic approaches to human renal agenesis/hypoplasia and dysplasia

Authors: Simone Sanna-Cherchi, Gianluca Caridi, Patricia L. Weng, Francesco Scolari, Francesco Perfumo, Ali G. Gharavi, Gian Marco Ghiggeri

Published in: Pediatric Nephrology | Issue 10/2007

Abstract

Congenital abnormalities of the kidney and urinary tract are frequently observed in children and represent a significant cause of morbidity and mortality. These conditions are phenotypically variable, often affecting several segments of the urinary tract simultaneously, making clinical classification and diagnosis difficult. Renal agenesis/hypoplasia and dysplasia account for a significant portion of these anomalies, and a genetic contribution to its cause is being increasingly recognized. Nevertheless, overlap between diseases and challenges in clinical diagnosis complicate studies attempting to discover new genes underlying this anomaly. Most of the insights in kidney development derive from studies in mouse models or from rare, syndromic forms of human developmental disorders of the kidney and urinary tract. The genes implicated have been shown to regulate the reciprocal induction between the ureteric bud and the metanephric mesenchyme. Strategies to find genes causing renal agenesis/hypoplasia and dysplasia vary depending on the characteristics of the study population available. The approaches range from candidate gene association or resequencing studies to traditional linkage studies, using outbred pedigrees or genetic isolates, to search for structural variation in the genome. Each of these strategies has advantages and pitfalls and some have led to significant discoveries in human disease. However, renal agenesis/hypoplasia and dysplasia still represents a challenge, both for the clinicians who attempt a precise diagnosis and for the geneticist who tries to unravel the genetic basis, and a better classification requires molecular definition to be retrospectively improved. The goal appears to be feasible with the large multicentric collaborative groups that share the same objectives and resources.

Woolf AS (2000) A molecular and genetic view of human renal and urinary tract malformations. Kidney Int 58:500–512CrossRefPubMed

Schulman J, Edmonds LD, McClearn AB, Jensvold N, Shaw GM (1993) Surveillance for and comparison of birth defect prevalences in two geographic areas-United States, 1983–88. MMWR CDC Surveill Summ 42:1–7PubMed

Pope JC 4th, Brock JW 3rd, Adams MC, Stephens FD, Ichikawa I (1999) How they begin and how they end: classic and new theories for the development and deterioration of congenital anomalies of the kidney and urinary tract, CAKUT. J Am Soc Nephrol 10:2018–2028PubMed

Eccles MR, Schimmenti LA (1999) Renal-coloboma syndrome: a multi-system developmental disorder caused by PAX2 mutations. Clin Genet 56:1–9CrossRefPubMed

Weber S, Moriniere V, Knuppel T, Charbit M, Dusek J, Ghiggeri GM, Jankauskiene A, Mir S, Montini G, Peco-Antic A, Wuhl E, Zurowska AM, Mehls O, Antignac C, Schaefer F, Salomon R (2006) Prevalence of mutations in renal developmental genes in children with renal hypodysplasia: results of the ESCAPE Study. J Am Soc Nephrol 17:2864–2870CrossRefPubMed

Carter CO, Evans K, Pescia G (1979) A family study of renal agenesis. J Med Genet 16:176–188CrossRefPubMedPubMedCentral

Vainio S, Lin Y (2002) Coordinating early kidney development: lessons from gene targeting. Nat Rev Genet 3:533–543CrossRefPubMed

Woolf AS (2004) Embryology. In: Pediatric nephrology, 5th edn. Lippincott Williams & Wilkins, Philadelphia, pp 3–24

Majumdar A, Vainio S, Kispert A, McMahon J, McMahon AP (2003) Wnt11 and Ret/Gdnf pathways cooperate in regulating ureteric branching during metanephric kidney development. Development 130:3175–3185CrossRefPubMed

10.

Costantini F, Shakya R (2006) GDNF/Ret signaling and the development of the kidney. Bioessays 28:117–127CrossRefPubMed

11.

Limwongse C, Clarren SK, Cassidy SB (2004) Syndromes and malformations of the urinary tract. In Barratt TM, Avner ED, Harmon WE (eds) Pediatric Nephrology. Philadelphia, USA, pp 93–121

12.

Abdelhak S, Kalatzis V, Heilig R, Compain S, Samson D, Vincent C, Weil D, Cruaud C, Sahly I, Leibovici M, Bitner-Glindzicz M, Francis M, Lacombe D, Vigneron J, Charachon R, Boven K, Bedbeder P, Van Regemorter N, Weissenbach J, Petit C (1997) A human homologue of the Drosophila eyes absent gene underlies branchio-oto-renal (BOR) syndrome and identifies a novel gene family. Nat Genet 15:157–164CrossRefPubMed

13.

Ruf RG, Xu PX, Silvius D, Otto EA, Beekmann F, Muerb UT, Kumar S, Neuhaus TJ, Kemper MJ, Raymond RM Jr, Brophy PD, Berkman J, Gattas M, Hyland V, Ruf EM, Schwartz C, Chang EH, Smith RJ, Stratakis CA, Weil D, Petit C, Hildebrandt F (2004) SIX1 mutations cause branchio-oto-renal syndrome by disruption of EYA1-SIX1-DNA complexes. Proc Natl Acad Sci U S A 101:8090–8095CrossRefPubMedPubMedCentral

14.

Kohlhase J, Wischermann A, Reichenbach H, Froster U, Engel W (1998) Mutations in the SALL1 putative transcription factor gene cause Townes-Brocks syndrome. Nat Genet 18:81–83CrossRefPubMed

15.

Bingham C, Bulman MP, Ellard S, Allen LI, Lipkin GW, Hoff WG, Woolf AS, Rizzoni G, Novelli G, Nicholls AJ, Hattersley AT (2001) Mutations in the hepatocyte nuclear factor-1beta gene are associated with familial hypoplastic glomerulocystic kidney disease. Am J Hum Genet 68:219–224CrossRefPubMed

16.

McPherson E, Carey J, Kramer A, Hall JG, Pauli RM, Schimke RN, Tasin MH (1987) Dominantly inherited renal adysplasia. Am J Med Genet 26:863–872CrossRefPubMed

17.

Roodhooft AM, Birnholz JC, Holmes LB (1984) Familial nature of congenital absence and severe dysgenesis of both kidneys. N Engl J Med 310:1341–1345CrossRefPubMed

18.

Kerecuk L, Sajoo A, McGregor L, Berg J, Haq MR, Sebire NJ, Bingham C, Edghill EL, Ellard S, Taylor J, Rigden S, Flinter FA, Woolf AS (2007) Autosomal dominant inheritance of non-syndromic renal hypoplasia and dysplasia: dramatic variation in clinical severity in a single kindred. Nephrol Dial Transplant 22:259–263CrossRefPubMed

19.

Pasch A, Hoefele J, Grimminger H, Hacker HW, Hildebrandt F (2004) Multiple urinary tract malformations with likely recessive inheritance in a large Somalian kindred. Nephrol Dial Transplant 19:3172–3175CrossRefPubMed

20.

Stenson PD, Ball EV, Mort M, Phillips AD, Shiel JA, Thomas NS, Abeysinghe S, Krawczak M, Cooper DN (2003) Human Gene Mutation Database (HGMD): 2003 update. Hum Mutat 21:577–581CrossRefPubMed

21.

Cardon LR, Bell JI (2001) Association study designs for complex diseases. Nat Rev Genet 2:91–99CrossRefPubMed

22.

Tabor HK, Risch NJ, Myers RM (2002) Opinion: candidate-gene approaches for studying complex genetic traits: practical considerations. Nat Rev Genet 3:391–397CrossRefPubMed

23.

Hu P, Deng FM, Liang FX, Hu CM, Auerbach AB, Shapiro E, Wu XR, Kachar B, Sun TT (2000) Ablation of uroplakin III gene results in small urothelial plaques, urothelial leakage, and vesicoureteral reflux. J Cell Biol 151:961–972CrossRefPubMedPubMedCentral

24.

Giltay JC, van de Meerakker J, van Amstel HK, de Jong TP (2004) No pathogenic mutations in the uroplakin III gene of 25 patients with primary vesicoureteral reflux. J Urol 171:931–932CrossRefPubMed

25.

Jenkins D, Bitner-Glindzicz M, Malcolm S, Hu CC, Allison J, Winyard PJ, Gullett AM, Thomas DF, Belk RA, Feather SA, Sun TT, Woolf AS (2005) De novo Uroplakin IIIa heterozygous mutations cause human renal adysplasia leading to severe kidney failure. J Am Soc Nephrol 16:2141–2149CrossRefPubMed

26.

Jiang S, Gitlin J, Deng FM, Liang FX, Lee A, Atala A, Bauer SB, Ehrlich GD, Feather SA, Goldberg JD, Goodship JA, Goodship TH, Hermanns M, Hu FZ, Jones KE, Malcolm S, Mendelsohn C, Preston RA, Retik AB, Schneck FX, Wright V, Ye XY, Woolf AS, Wu XR, Ostrer H, Shapiro E, Yu J, Sun TT (2004) Lack of major involvement of human uroplakin genes in vesicoureteral reflux: implications for disease heterogeneity. Kidney Int 66:10–19CrossRefPubMed

27.

Kelly H, Ennis S, Yoneda A, Bermingham C, Shields DC, Molony C, Green AJ, Puri P, Barton DE (2005) Uroplakin III is not a major candidate gene for primary vesicoureteral reflux. Eur J Hum Genet 13:500–502CrossRefPubMed

28.

Schonfelder EM, Knuppel T, Tasic V, Miljkovic P, Konrad M, Wuhl E, Antignac C, Bakkaloglu A, Schaefer F, Weber S (2006) Mutations in Uroplakin IIIA are a rare cause of renal hypodysplasia in humans. Am J Kidney Dis 47:1004–1012CrossRefPubMed

29.

Woolf AS (2006) Renal hypoplasia and dysplasia: starting to put the puzzle together. J Am Soc Nephrol 17:2647–2649CrossRefPubMed

30.

Gribouval O, Gonzales M, Neuhaus T, Aziza J, Bieth E, Laurent N, Bouton JM, Feuillet F, Makni S, Ben Amar H, Laube G, Delezoide AL, Bouvier R, Dijoud F, Ollagnon-Roman E, Roume J, Joubert M, Antignac C, Gubler MC (2005) Mutations in genes in the renin-angiotensin system are associated with autosomal recessive renal tubular dysgenesis. Nat Genet 37:964–968CrossRefPubMed

31.

Emison ES, McCallion AS, Kashuk CS, Bush RT, Grice E, Lin S, Portnoy ME, Cutler DJ, Green ED, Chakravarti A (2005) A common sex-dependent mutation in a RET enhancer underlies Hirschsprung disease risk. Nature 434:857–863CrossRefPubMed

32.

Hirschhorn JN, Daly MJ (2005) Genome-wide association studies for common diseases and complex traits. Nat Rev Genet 6:95–108CrossRefPubMed

33.

Jimenez-Sanchez G, Childs B, Valle D (2001) Human disease genes. Nature 409:853–855CrossRefPubMed

34.

Sanna-Cherchi S, Reese A, Hensle T, Caridi G, Izzi C, Kim YY, Konka A, Murer L, Scolari F, Ravazzolo R, Ghiggeri GM, Gharavi AG (2005) Familial vesicoureteral reflux: testing replication of linkage in seven new multigenerational kindreds. J Am Soc Nephrol 16:1781–1787CrossRefPubMed

35.

Sanna-Cherchi S, Caridi G, Weng PL, Dagnino M, Seri M, Konka A, Somenzi D, Carrea A, Izzi C, Casu D, Allegri L, Schmidt-Ott KM, Barasch J, Scolari F, Ravazzolo R, Ghiggeri GM, Gharavi AG (2007) Localization of a gene for nonsyndromic renal hypodysplasia to chromosome 1p32–33. Am J Hum Genet 80:539–549CrossRefPubMedPubMedCentral

36.

Kittles RA, Perola M, Peltonen L, Bergen AW, Aragon RA, Virkkunen M, Linnoila M, Goldman D, Long JC (1998) Dual origins of Finns revealed by Y chromosome haplotype variation. Am J Hum Genet 62:1171–1179CrossRefPubMedPubMedCentral

37.

Sajantila A, Salem AH, Savolainen P, Bauer K, Gierig C, Paabo S (1996) Paternal and maternal DNA lineages reveal a bottleneck in the founding of the Finnish population. Proc Natl Acad Sci USA 93:12035–12039CrossRefPubMedPubMedCentral

38.

Peltonen L, Palotie A, Lange K (2000) Use of population isolates for mapping complex traits. Nat Rev Genet 1:182–190CrossRefPubMed

39.

Gianfrancesco F, Esposito T, Ombra MN, Forabosco P, Maninchedda G, Fattorini M, Casula S, Vaccargiu S, Casu G, Cardia F, Deiana I, Melis P, Falchi M, Pirastu M (2003) Identification of a novel gene and a common variant associated with uric acid nephrolithiasis in a Sardinian genetic isolate. Am J Hum Genet 72:1479–1491CrossRefPubMedPubMedCentral

40.

Houwen RH, Baharloo S, Blankenship K, Raeymaekers P, Juyn J, Sandkuijl LA, Freimer NB (1994) Genome screening by searching for shared segments: mapping a gene for benign recurrent intrahepatic cholestasis. Nat Genet 8:380–386CrossRefPubMed

41.

Nikali K, Suomalainen A, Terwilliger J, Koskinen T, Weissenbach J, Peltonen L (1995) Random search for shared chromosomal regions in four affected individuals: the assignment of a new hereditary ataxia locus. Am J Hum Genet 56:1088–1095PubMedPubMedCentral

42.

Izzi C, Sanna-Cherchi S, Prati E, Belleri R, Remedio A, Tardanico R, Foramitti M, Guerini S, Viola BF, Movilli E, Beerman I, Lifton R, Leone L, Gharavi A, Scolari F (2006) Familial aggregation of primary glomerulonephritis in an Italian population isolate: Valtrompia study. Kidney Int 69:1033–1040CrossRefPubMedPubMedCentral

43.

Kruglyak L, Nickerson DA (2001) Variation is the spice of life. Nat Genet 27:234–236CrossRefPubMed

44.

The International HapMap Consortium (2003) The International HapMap Project. Nature 426:789–796CrossRef

45.

Syvanen AC (2001) Accessing genetic variation: genotyping single nucleotide polymorphisms. Nat Rev Genet 2:930–942CrossRefPubMed

46.

Seal JL, Gornick MC, Gogtay N, Shaw P, Greenstein DK, Coffey M, Gochman PA, Stromberg T, Chen Z, Merriman B, Nelson SF, Brooks J, Arepalli S, Wavrant-De Vrieze F, Hardy J, Rapoport JL, Addington AM (2006) Segmental uniparental isodisomy on 5q32-qter in a patient with childhood-onset schizophrenia. J Med Genet 43:887–892CrossRefPubMedPubMedCentral

47.

Daiger SP (2005) Genetics. Was the Human Genome Project worth the effort? Science 308:362–364CrossRefPubMedPubMedCentral

48.

Klein RJ, Zeiss C, Chew EY, Tsai JY, Sackler RS, Haynes C, Henning AK, SanGiovanni JP, Mane SM, Mayne ST, Bracken MB, Ferris FL, Ott J, Barnstable C, Hoh J (2005) Complement factor H polymorphism in age-related macular degeneration. Science 308:385–389CrossRefPubMedPubMedCentral

49.

Grant SF, Thorleifsson G, Reynisdottir I, Benediktsson R, Manolescu A, Sainz J, Helgason A, Stefansson H, Emilsson V, Helgadottir A, Styrkarsdottir U, Magnusson KP, Walters GB, Palsdottir E, Jonsdottir T, Gudmundsdottir T, Gylfason A, Saemundsdottir J, Wilensky RL, Reilly MP, Rader DJ, Bagger Y, Christiansen C, Gudnason V, Sigurdsson G, Thorsteinsdottir U, Gulcher JR, Kong A, Stefansson K (2006) Variant of transcription factor 7-like 2 (TCF7L2) gene confers risk of type 2 diabetes. Nat Genet 38:320–323CrossRefPubMed

50.

Groves CJ, Zeggini E, Minton J, Frayling TM, Weedon MN, Rayner NW, Hitman GA, Walker M, Wiltshire S, Hattersley AT, McCarthy MI (2006) Association analysis of 6,736 U.K. subjects provides replication and confirms TCF7L2 as a type 2 diabetes susceptibility gene with a substantial effect on individual risk. Diabetes 55:2640–2644CrossRefPubMed

51.

Ogata T, Muroya K, Sasagawa I, Kosho T, Wakui K, Sakazume S, Ito K, Matsuo N, Ohashi H, Nagai T (2000) Genetic evidence for a novel gene(s) involved in urogenital development on 10q26. Kidney Int 58:2281–2290CrossRefPubMed

52.

Vats AN, Ishwad C, Vats KR, Moritz M, Ellis D, Mueller C, Surti U, Parizhskaya MZ, Meza MP, Burke L, Schneck FX, Saxena M, Ferrell R (2003) Steroid-resistant nephrotic syndrome and congenital anomalies of kidneys: evidence of locus on chromosome 13q. Kidney Int 64:17–24CrossRefPubMed

53.

Vats KR, Ishwad C, Singla I, Vats A, Ferrell R, Ellis D, Moritz M, Surti U, Jayakar P, Frederick DR, Vats AN (2006) A locus for renal malformations including vesico-ureteric reflux on chromosome 13q33–34. J Am Soc Nephrol 17:1158–1167CrossRefPubMed

54.

Feuk L, Carson AR, Scherer SW (2006) Structural variation in the human genome. Nat Rev Genet 7:85–97CrossRefPubMed

55.

Koolen DA, Vissers LE, Pfundt R, de Leeuw N, Knight SJ, Regan R, Kooy RF, Reyniers E, Romano C, Fichera M, Schinzel A, Baumer A, Anderlid BM, Schoumans J, Knoers NV, van Kessel AG, Sistermans EA, Veltman JA, Brunner HG, de Vries BB (2006) A new chromosome 17q21.31 microdeletion syndrome associated with a common inversion polymorphism. Nat Genet 38:999–1001CrossRefPubMed

56.

Sharp AJ, Hansen S, Selzer RR, Cheng Z, Regan R, Hurst JA, Stewart H, Price SM, Blair E, Hennekam RC, Fitzpatrick CA, Segraves R, Richmond TA, Guiver C, Albertson DG, Pinkel D, Eis PS, Schwartz S, Knight SJ, Eichler EE (2006) Discovery of previously unidentified genomic disorders from the duplication architecture of the human genome. Nat Genet 38:1038–1042CrossRefPubMed

57.

Shaw-Smith C, Pittman AM, Willatt L, Martin H, Rickman L, Gribble S, Curley R, Cumming S, Dunn C, Kalaitzopoulos D, Porter K, Prigmore E, Krepischi-Santos AC, Varela MC, Koiffmann CP, Lees AJ, Rosenberg C, Firth HV, de Silva R, Carter NP (2006) Microdeletion encompassing MAPT at chromosome 17q21.3 is associated with developmental delay and learning disability. Nat Genet 38:1032–1037CrossRefPubMed

58.

Vissers LE, van Ravenswaaij CM, Admiraal R, Hurst JA, de Vries BB, Janssen IM, van der Vliet WA, Huys EH, de Jong PJ, Hamel BC, Schoenmakers EF, Brunner HG, Veltman JA, van Kessel AG (2004) Mutations in a new member of the chromodomain gene family cause CHARGE syndrome. Nat Genet 36:955–957CrossRefPubMed

59.

Hatini V, Huh SO, Herzlinger D, Soares VC, Lai E (1996) Essential role of stromal mesenchyme in kidney morphogenesis revealed by targeted disruption of Winged Helix transcription factor BF-2. Genes Dev 10:1467–1478CrossRefPubMed

60.

Johnson KR, Cook SA, Erway LC, Matthews AN, Sanford LP, Paradies NE, Friedman RA (1999) Inner ear and kidney anomalies caused by IAP insertion in an intron of the Eya1 gene in a mouse model of BOR syndrome. Hum Mol Genet 8:645–653CrossRefPubMed

61.

Xu PX, Adams J, Peters H, Brown MC, Heaney S, Maas R (1999) Eya1-deficient mice lack ears and kidneys and show abnormal apoptosis of organ primordia. Nat Genet 23:113–117CrossRefPubMed

62.

Miyamoto N, Yoshida M, Kuratani S, Matsuo I, Aizawa S (1997) Defects of urogenital development in mice lacking Emx2. Development 124:1653–1664PubMed

63.

Davis AP, Witte DP, Hsieh-Li HM, Potter SS, Capecchi MR (1995) Absence of radius and ulna in mice lacking hoxa-11 and hoxd-11. Nature 375:791–795CrossRefPubMed

64.

Shawlot W, Behringer RR (1995) Requirement for Lim1 in head-organizer function. Nature 374:425–430CrossRefPubMed

65.

Torres M, Gomez-Pardo E, Dressler GR, Gruss P (1995) Pax-2 controls multiple steps of urogenital development. Development 121:4057–4065PubMed

66.

Kreidberg JA, Sariola H, Loring JM, Maeda M, Pelletier J, Housman D, Jaenisch R (1993) WT-1 is required for early kidney development. Cell 74:679–691CrossRefPubMed

67.

Nishimura H, Yerkes E, Hohenfellner K, Miyazaki Y, Ma J, Hunley TE, Yoshida H, Ichiki T, Threadgill D, Phillips JA 3rd, Hogan BM, Fogo A, Brock JW 3rd, Inagami T, Ichikawa I (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 3:1–10CrossRefPubMed

68.

Miyazaki Y, Oshima K, Fogo A, Hogan BL, Ichikawa I (2000) Bone morphogenetic protein 4 regulates the budding site and elongation of the mouse ureter. J Clin Invest 105:863–873CrossRefPubMedPubMedCentral

69.

Dudley AT, Lyons KM, Robertson EJ (1995) A requirement for bone morphogenetic protein-7 during development of the mammalian kidney and eye. Genes Dev 9:2795–2807CrossRefPubMed

70.

Stark K, Vainio S, Vassileva G, McMahon AP (1994) Epithelial transformation of metanephric mesenchyme in the developing kidney regulated by Wnt-4. Nature 372:679–683CrossRefPubMed

71.

Schuchardt A, D’Agati V, Larsson-Blomberg L, Costantini F, Pachnis V (1994) Defects in the kidney and enteric nervous system of mice lacking the tyrosine kinase receptor Ret. Nature 367:380–383CrossRefPubMed

72.

Sanchez MP, Silos-Santiago I, Frisen J, He B, Lira SA, Barbacid M (1996) Renal agenesis and the absence of enteric neurons in mice lacking GDNF. Nature 382:70–73CrossRefPubMed

73.

Moore MW, Klein RD, Farinas I, Sauer H, Armanini M, Phillips H, Reichardt LF, Ryan AM, Carver-Moore K, Rosenthal A (1996) Renal and neuronal abnormalities in mice lacking GDNF. Nature 382:76–79CrossRefPubMed

74.

Pichel JG, Shen L, Sheng HZ, Granholm AC, Drago J, Grinberg A, Lee EJ, Huang SP, Saarma M, Hoffer BJ, Sariola H, Westphal H (1996) Defects in enteric innervation and kidney development in mice lacking GDNF. Nature 382:73–76CrossRefPubMed

75.

Xu PX, Zheng W, Huang L, Maire P, Laclef C, Silvius D (2003) Six1 is required for the early organogenesis of mammalian kidney. Development 130:3085–3094CrossRefPubMed

76.

Self M, Lagutin OV, Bowling B, Hendrix J, Cai Y, Dressler GR, Oliver G (2006) Six2 is required for suppression of nephrogenesis and progenitor renewal in the developing kidney. EMBO J 25:5214–5228CrossRefPubMedPubMedCentral

77.

Nishinakamura R, Matsumoto Y, Nakao K, Nakamura K, Sato A, Copeland NG, Gilbert DJ, Jenkins NA, Scully S, Lacey DL, Katsuki M, Asashima M, Yokota T (2001) Murine homolog of SALL1 is essential for ureteric bud invasion in kidney development. Development 128:3105–3115PubMed

78.

Poladia DP, Kish K, Kutay B, Hains D, Kegg H, Zhao H, Bates CM (2006) Role of fibroblast growth factor receptors 1 and 2 in the metanephric mesenchyme. Dev Biol 291:325–339CrossRefPubMed

79.

Liu J, Zhang L, Wang D, Shen H, Jiang M, Mei P, Hayden PS, Sedor JR, Hu H (2003) Congenital diaphragmatic hernia, kidney agenesis and cardiac defects associated with Slit3-deficiency in mice. Mech Dev 120:1059–1070CrossRefPubMed

80.

Schnabel CA, Godin RE, Cleary ML (2003) Pbx1 regulates nephrogenesis and ureteric branching in the developing kidney. Dev Biol 254:262–276CrossRefPubMed

81.

Perantoni AO, Timofeeva O, Naillat F, Richman C, Pajni-Underwood S, Wilson C, Vainio S, Dove LF, Lewandoski M (2005) Inactivation of FGF8 in early mesoderm reveals an essential role in kidney development. Development 132:3859–3871CrossRefPubMed

82.

Mendelsohn C, Lohnes D, Decimo D, Lufkin T, LeMeur M, Chambon P, Mark M (1994) Function of the retinoic acid receptors (RARs) during development (II). Multiple abnormalities at various stages of organogenesis in RAR double mutants. Development 120:2749–2771PubMed

83.

Kobayashi A, Kwan KM, Carroll TJ, McMahon AP, Mendelsohn CL, Behringer RR (2005) Distinct and sequential tissue-specific activities of the LIM-class homeobox gene Lim1 for tubular morphogenesis during kidney development. Development 132:2809–2823CrossRefPubMed

Title: Genetic approaches to human renal agenesis/hypoplasia and dysplasia
Authors: Simone Sanna-Cherchi
Gianluca Caridi
Patricia L. Weng
Francesco Scolari
Francesco Perfumo
Ali G. Gharavi
Gian Marco Ghiggeri
Publication date: 01-10-2007
Publisher: Springer Berlin Heidelberg
Published in: Pediatric Nephrology / Issue 10/2007
Print ISSN: 0931-041X
Electronic ISSN: 1432-198X
DOI: https://doi.org/10.1007/s00467-007-0479-1

At a glance: The STEP trials

Springer Medicine

Genetic approaches to human renal agenesis/hypoplasia and dysplasia

Abstract

At a glance: The STEP trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 10/2007

End-stage renal failure in adolescence with Sjögren’s syndrome autoantibodies SSA and SSB

Improving outcomes from acute kidney injury: report of an initiative

Pathophysiology of hypercalciuria in children

Remission of steroid- and CyA-resistant nephrotic syndrome using multiple drug immunosuppression

Chronic kidney disease in children: state of the art

Bone mineral density and bone histomorphometry in children on long-term dialysis