Betaglycan is required for the establishment of nephron endowment in the mouse

PLoS ONE

Volumn 6, Issue 4, 2011, Pages

  Walker, Kenneth A ^a,b   Sims Lucas, Sunder ^a,c   Caruana, Georgina ^a   Cullen McEwen, Luise ^a   Li, Jinhua ^a   Sarraj, Mai A ^b   Bertram, John F ^a   Stenvers, Kaye L ^a,b  

^a MONASH UNIVERSITY   (Australia)

^b HUDSON INSTITUTE OF MEDICAL RESEARCH   (Australia)

^c CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 3; PROTEOGLYCAN; TRANSFORMING GROWTH FACTOR BETA RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BMP4 GENE; BRANCHING MORPHOGENESIS; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; EMBRYO DEVELOPMENT; EYA1 GENE; GDNF GENE; GENE; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GROWTH REGULATION; HETEROZYGOTE; KIDNEY DEVELOPMENT; KIDNEY HYPOPLASIA; MOUSE; NEPHRON; NONHUMAN; NUCLEOTIDE SEQUENCE; PAX2 GENE; PHENOTYPE; REGULATOR GENE; RET GENE; TGFB1 GENE; TGFB2 GENE; URETER; WNT4 GENE; WT1 GENE; ANIMAL; GENETICS; MOUSE MUTANT; PHYSIOLOGY; POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

MURINAE;

ANIMALS; MICE; MICE, KNOCKOUT; NEPHRONS; POLYMERASE CHAIN REACTION; PROTEOGLYCANS; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; SIGNAL TRANSDUCTION;

EID: 79955144738     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0018723     Document Type: Article

References (51)

1. Saxen L, Sariola H, (1987) Early organogenesis of the kidney. Pediatr Nephrol 1: 385-392.
2. Costantini F, (2006) Renal branching morphogenesis: concepts, questions, and recent advances. Differentiation 74: 402-421.
3. Meyer TN, Schwesinger C, Bush KT, Stuart RO, Rose DW, et al. (2004) Spatiotemporal regulation of morphogenetic molecules during in vitro branching of the isolated ureteric bud: toward a model of branching through budding in the developing kidney. Dev Biol 275: 44-67.
4. Plisov SY, Yoshino K, Dove LF, Higinbotham KG, Rubin JS, et al. (2001) TGF beta 2, LIF and FGF2 cooperate to induce nephrogenesis. Development 128: 1045-1057.
5. Bush KT, Sakurai H, Steer DL, Leonard MO, Sampogna RV, et al. (2004) TGF-beta superfamily members modulate growth, branching, shaping, and patterning of the ureteric bud. Dev Biol 266: 285-298.
6. Sims-Lucas S, Caruana G, Dowling J, Kett MM, Bertram JF, (2008) Augmented and accelerated nephrogenesis in TGF-beta2 heterozygous mutant mice. Pediatr Res 63: 607-612.
7. Esquela AF, Lee SJ, (2003) Regulation of metanephric kidney development by growth/differentiation factor 11. Dev Biol 257: 356-370.
8. Sakurai H, Nigam SK, (1997) Transforming growth factor-beta selectively inhibits branching morphogenesis but not tubulogenesis. Am J Physiol 272: F139-146.
9. 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: 2795-2807.
10. Michos O, Goncalves A, Lopez-Rios J, Tiecke E, Naillat F, et al. (2007) Reduction of BMP4 activity by gremlin 1 enables ureteric bud outgrowth and GDNF/WNT11 feedback signalling during kidney branching morphogenesis. Development 134: 2397-2405.
11. Oxburgh L, Chu GC, Michael SK, Robertson EJ, (2004) TGFbeta superfamily signals are required for morphogenesis of the kidney mesenchyme progenitor population. Development 131: 4593-4605.
12. Sanford LP, Ormsby I, Gittenberger-de Groot AC, Sariola H, Friedman R, et al. (1997) TGFbeta2 knockout mice have multiple developmental defects that are non-overlapping with other TGFbeta knockout phenotypes. Development 124: 2659-2670.
13. Letterio JJ, Geiser AG, Kulkarni AB, Roche NS, Sporn MB, et al. (1994) Maternal rescue of transforming growth factor-beta 1 null mice. Science 264: 1936-1938.
14. Kaartinen V, Voncken JW, Shuler C, Warburton D, Bu D, et al. (1995) Abnormal lung development and cleft palate in mice lacking TGF-beta 3 indicates defects of epithelial-mesenchymal interaction. Nat Genet 11: 415-421.
15. Stenvers KL, Tursky ML, Harder KW, Kountouri N, Amatayakul-Chantler S, et al. (2003) Heart and liver defects and reduced transforming growth factor beta2 sensitivity in transforming growth factor beta type III receptor-deficient embryos. Mol Cell Biol 23: 4371-4385.
16. Compton LA, Potash DA, Brown CB, Barnett JV, (2007) Coronary vessel development is dependent on the type III transforming growth factor beta receptor. Circ Res 101: 784-791.
17. Lopez-Casillas F, Wrana JL, Massague J, (1993) Betaglycan presents ligand to the TGF beta signaling receptor. Cell 73: 1435-1444.
18. Esparza-Lopez J, Montiel JL, Vilchis-Landeros MM, Okadome T, Miyazono K, et al. (2001) Ligand binding and functional properties of betaglycan, a co-receptor of the transforming growth factor-beta superfamily. Specialized binding regions for transforming growth factor-beta and inhibin A. J Biol Chem 276: 14588-14596.
19. Lewis KA, Gray PC, Blount AL, MacConell LA, Wiater E, et al. (2000) Betaglycan binds inhibin and can mediate functional antagonism of activin signalling. Nature 404: 411-414.
20. Kirkbride KC, Townsend TA, Bruinsma MW, Barnett JV, Blobe GC, (2008) Bone morphogenetic proteins signal through the transforming growth factor-beta type III receptor. J Biol Chem 283: 7628-7637.
21. Schuchardt A, D'Agati V, Pachnis V, Costantini F, (1996) Renal agenesis and hypodysplasia in ret-k- mutant mice result from defects in ureteric bud development. Development 122: 1919-1929.
22. 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: 3175-3185.
23. Clarke JC, Patel SR, Raymond RM Jr, Andrew S, Robinson BG, et al. (2006) Regulation of c-Ret in the developing kidney is responsive to Pax2 gene dosage. Hum Mol Genet 15: 3420-3428.
24. Davies JA, Ladomery M, Hohenstein P, Michael L, Shafe A, et al. (2004) Development of an siRNA-based method for repressing specific genes in renal organ culture and its use to show that the Wt1 tumour suppressor is required for nephron differentiation. Hum Mol Genet 13: 235-246.
25. Kim HS, Kim MS, Hancock AL, Harper JC, Park JY, et al. (2007) Identification of novel Wilms' tumor suppressor gene target genes implicated in kidney development. J Biol Chem 282: 16278-16287.
26. Brodbeck S, Englert C, (2004) Genetic determination of nephrogenesis: the Pax/Eya/Six gene network. Pediatr Nephrol 19: 249-255.
27. Stark K, Vainio S, Vassileva G, McMahon AP, (1994) Epithelial transformation of metanephric mesenchyme in the developing kidney regulated by Wnt-4. Nature 372: 679-683.
28. Valerius MT, McMahon AP, (2008) Transcriptional profiling of Wnt4 mutant mouse kidneys identifies genes expressed during nephron formation. Gene Expr Patterns 8: 297-306.
29. Massague J, Seoane J, Wotton D, (2005) Smad transcription factors. Genes Dev 19: 2783-2810.
30. Schmierer B, Hill CS, (2007) TGFbeta-SMAD signal transduction: molecular specificity and functional flexibility. Nat Rev Mol Cell Biol 8: 970-982.
31. Wiater E, Harrison CA, Lewis KA, Gray PC, Vale WW, (2006) Identification of distinct inhibin and transforming growth factor beta-binding sites on betaglycan: functional separation of betaglycan co-receptor actions. J Biol Chem 281: 17011-17022.
32. Miyazaki Y, Oshima K, Fogo A, Ichikawa I, (2003) Evidence that bone morphogenetic protein 4 has multiple biological functions during kidney and urinary tract development. Kidney Int 63: 835-844.
33. Michos O, Panman L, Vintersten K, Beier K, Zeller R, et al. (2004) Gremlin-mediated BMP antagonism induces the epithelial-mesenchymal feedback signaling controlling metanephric kidney and limb organogenesis. Development 131: 3401-3410.
34. Brophy PD, Ostrom L, Lang KM, Dressler GR, (2001) Regulation of ureteric bud outgrowth by Pax2-dependent activation of the glial derived neurotrophic factor gene. Development 128: 4747-4756.
35. Xu PX, Zheng W, Huang L, Maire P, Laclef C, et al. (2003) Six1 is required for the early organogenesis of mammalian kidney. Development 130: 3085-3094.
36. Kim SJ, Angel P, Lafyatis R, Hattori K, Kim KY, et al. (1990) Autoinduction of transforming growth factor beta 1 is mediated by the AP-1 complex. Mol Cell Biol 10: 1492-1497.
37. Tang B, Bottinger EP, Jakowlew SB, Bagnall KM, Mariano J, et al. (1998) Transforming growth factor-beta1 is a new form of tumor suppressor with true haploid insufficiency. Nat Med 4: 802-807.
38. Pelton RW, Saxena B, Jones M, Moses HL, Gold LI, (1991) Immunohistochemical localization of TGF beta 1, TGF beta 2, and TGF beta 3 in the mouse embryo: expression patterns suggest multiple roles during embryonic development. J Cell Biol 115: 1091-1105.
39. Sims-Lucas S, (2007) Investigating the role of transforming growth factor-β2 in mouse metanephric development [Doctor of Philosophy]. Melbourne Monash University.
40. Zhao J, Tefft JD, Lee M, Smith S, Warburton D, (1998) Abrogation of betaglycan attenuates TGF-beta-mediated inhibition of embryonic murine lung branching morphogenesis in culture. Mech Dev 75: 67-79.
41. Sims-Lucas S, Young RJ, Martinez G, Taylor D, Grimmond SM, et al. (2010) Redirection of renal mesenchyme to stromal and chondrocytic fates in the presence of TGF-beta2. Differentiation 79: 272-284.
42. Tomoda T, Shirasawa T, Yahagi YI, Ishii K, Takagi H, et al. (1996) Transforming growth factor-beta is a survival factor for neonate cortical neurons: coincident expression of type I receptors in developing cerebral cortices. Dev Biol 179: 79-90.
43. Winyard P, Chitty LS, (2008) Dysplastic kidneys. Semin Fetal Neonatal Med 13: 142-151.
44. Sarraj MA, Chua HK, Umbers A, Loveland KL, Findlay JK, et al. (2007) Differential expression of TGFBR3 (betaglycan) in mouse ovary and testis during gonadogenesis. Growth Factors 25: 334-345.
45. Hacker A, Capel B, Goodfellow P, Lovell-Badge R, (1995) Expression of Sry, the mouse sex determining gene. Development 121: 1603-1614.
46. Cullen-McEwen LA, Drago J, Bertram JF, (2001) Nephron endowment in glial cell line-derived neurotrophic factor (GDNF) heterozygous mice. Kidney Int 60: 31-36.
47. Cebrian C, Borodo K, Charles N, Herzlinger DA, (2004) Morphometric index of the developing murine kidney. Dev Dyn 231: 601-608.
48. Walker KA, Caruana G, Bertram JF, McInnes KJ, (2009) Sexual dimorphism in mouse metanephroi exposed to 17beta-estradiol in vitro. Nephron Exp Nephrol 111: e42-50.
49. Bertram JF, (1995) Analyzing renal glomeruli with the new stereology. Int Rev Cytol 161: 111-172.
50. Bertram JF, Nurcombe V, (1992) Counting cells with the new stereology. Trends Cell Biol 2: 177-180.
51. Bilandzic M, Chu S, Farnworth PG, Harrison C, Nicholls P, et al. (2009) Loss of betaglycan contributes to the malignant properties of human granulosa tumor cells. Mol Endocrinol 23: 539-548.