Genetic analysis reveals an unexpected role of BMP7 in initiation of ureteric bud outgrowth in mouse embryos

PLoS ONE

Volumn 6, Issue 4, 2011, Pages

  Gonçalves, Alexandre ^a   Zeller, Rolf ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

GENE PRODUCT; OSTEOGENIC PROTEIN 1; PROTEIN GREM1; UNCLASSIFIED DRUG; WNT11 PROTEIN; BMP4 PROTEIN, MOUSE; BMP7 PROTEIN, MOUSE; BONE MORPHOGENETIC PROTEIN 4; GREM1 PROTEIN, MOUSE; SIGNAL PEPTIDE;

ALLELE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRANCHING MORPHOGENESIS; CONTROLLED STUDY; EMBRYO; EPITHELIUM CELL; ETV4 GENE; GENE; GENE EXPRESSION; GENE INACTIVATION; GENETIC ANALYSIS; KIDNEY AGENESIS; KIDNEY DEVELOPMENT; KIDNEY DYSPLASIA; MESENCHYME; MOUSE; NEPHRON; NONHUMAN; PHENOTYPE; SIGNAL TRANSDUCTION; SIX2 GENE; STEM CELL; URETER; URETERIC BUD OUTGROWTH; ANIMAL; ANIMAL EMBRYO; CYTOLOGY; EMBRYONIC STRUCTURES; FEMALE; GENETICS; KIDNEY; MALE; METABOLISM; PREGNANCY; PRENATAL DEVELOPMENT;

ANIMALS; APOPTOSIS; BONE MORPHOGENETIC PROTEIN 4; BONE MORPHOGENETIC PROTEIN 7; EMBRYO, MAMMALIAN; FEMALE; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; KIDNEY; MALE; MICE; PREGNANCY; WOLFFIAN DUCTS;

EID: 79955736860     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0019370     Document Type: Article

References (34)

1. Affolter M, Zeller R, Caussinus E, (2009) Tissue remodelling through branching morphogenesis. Nat Rev Mol Cell Biol 10: 831-842.
2. Michos O, (2009) Kidney development: from ureteric bud formation to branching morphogenesis. Curr Opin Genet Dev 19: 484-490.
3. Chi X, Michos O, Shakya R, Riccio P, Enomoto H, et al. (2009) Ret-dependent cell rearrangements in the Wolffian duct epithelium initiate ureteric bud morphogenesis. Dev Cell 17: 199-209.
4. Shakya R, Jho EH, Kotka P, Wu Z, Kholodilov N, et al. (2005) The role of GDNF in patterning the excretory system. Dev Biol 283: 70-84.
5. 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.
6. Grieshammer U, Le M, Plump AS, Wang F, Tessier-Lavigne M, et al. (2004) SLIT2-mediated ROBO2 signaling restricts kidney induction to a single site. Dev Cell 6: 709-717.
7. Basson MA, Akbulut S, Watson-Johnson J, Simon R, Carroll TJ, et al. (2005) Sprouty1 is a critical regulator of GDNF/RET-mediated kidney induction. Dev Cell 8: 229-239.
8. Michos O, Cebrian C, Hyink D, Grieshammer U, Williams L, et al. (2010) Kidney development in the absence of Gdnf and Spry1 requires Fgf10. PLoS Genet 6: e1000809.
9. 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.
10. Lu BC, Cebrian C, Chi X, Kuure S, Kuo R, et al. (2009) Etv4 and Etv5 are required downstream of GDNF and Ret for kidney branching morphogenesis. Nat Genet 41: 1295-1302.
11. Sims-Lucas S, Cusack B, Baust J, Eswarakumar VP, Masatoshi H, et al. (2010) Fgfr1 and the IIIc isoform of Fgfr2 play critical roles in the metanephric mesenchyme mediating early inductive events in kidney development. Dev Dyn.
12. 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.
13. 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.
14. Kobayashi A, Valerius MT, Mugford JW, Carroll TJ, Self M, et al. (2008) Six2 defines and regulates a multipotent self-renewing nephron progenitor population throughout mammalian kidney development. Cell Stem Cell 3: 169-181.
15. Self M, Lagutin OV, Bowling B, Hendrix J, Cai Y, et al. (2006) Six2 is required for suppression of nephrogenesis and progenitor renewal in the developing kidney. EMBO J 25: 5214-5228.
16. Dudley AT, Robertson EJ, (1997) Overlapping expression domains of bone morphogenetic protein family members potentially account for limited tissue defects in BMP7 deficient embryos. Dev Dyn 208: 349-362.
17. 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.
18. 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.
19. Luo G, Hofmann C, Bronckers AL, Sohocki M, Bradley A, et al. (1995) BMP-7 is an inducer of nephrogenesis, and is also required for eye development and skeletal patterning. Genes Dev 9: 2808-2820.
20. Oxburgh L, Dudley AT, Godin RE, Koonce CH, Islam A, et al. (2005) BMP4 substitutes for loss of BMP7 during kidney development. Dev Biol 286: 637-646.
21. 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: 863-873.
22. Brenner-Anantharam A, Cebrian C, Guillaume R, Hurtado R, Sun TT, et al. (2007) Tailbud-derived mesenchyme promotes urinary tract segmentation via BMP4 signaling. Development 134: 1967-1975.
23. Raatikainen-Ahokas A, Hytonen M, Tenhunen A, Sainio K, Sariola H, (2000) BMP-4 affects the differentiation of metanephric mesenchyme and reveals an early anterior-posterior axis of the embryonic kidney. Dev Dyn 217: 146-158.
24. Benazet JD, Bischofberger M, Tiecke E, Goncalves A, Martin JF, et al. (2009) A self-regulatory system of interlinked signaling feedback loops controls mouse limb patterning. Science 323: 1050-1053.
25. Piscione TD, Phan T, Rosenblum ND, (2001) BMP7 controls collecting tubule cell proliferation and apoptosis via Smad1-dependent and-independent pathways. American journal of physiology Renal physiology 280: F19-33.
26. Blank U, Brown A, Adams DC, Karolak MJ, Oxburgh L, (2009) BMP7 promotes proliferation of nephron progenitor cells via a JNK-dependent mechanism. Development 136: 3557-3566.
27. Zhang Q, Shi Y, Wada J, Malakauskas SM, Liu M, et al. (2010) In vivo delivery of Gremlin siRNA plasmid reveals therapeutic potential against diabetic nephropathy by recovering bone morphogenetic protein-7. PLoS One 5: e11709.
28. Katagiri T, Boorla S, Frendo JL, Hogan BL, Karsenty G, (1998) Skeletal abnormalities in doubly heterozygous Bmp4 and Bmp7 mice. Dev Genet 22: 340-348.
29. Little SC, Mullins MC, (2009) Bone morphogenetic protein heterodimers assemble heteromeric type I receptor complexes to pattern the dorsoventral axis. Nat Cell Biol 11: 637-643.
30. Nishimatsu S, Thomsen GH, (1998) Ventral mesoderm induction and patterning by bone morphogenetic protein heterodimers in Xenopus embryos. Mech Dev 74: 75-88.
31. Suzuki A, Kaneko E, Maeda J, Ueno N, (1997) Mesoderm induction by BMP-4 and-7 heterodimers. Biochem Biophys Res Commun 232: 153-156.
32. Hayashi S, McMahon AP, (2002) Efficient recombination in diverse tissues by a tamoxifen-inducible form of Cre: a tool for temporally regulated gene activation/inactivation in the mouse. Dev Biol 244: 305-318.
33. Kulessa H, Hogan BL, (2002) Generation of a loxP flanked bmp4loxP-lacZ allele marked by conditional lacZ expression. Genesis 32: 66-68.
34. Shi SR, Chaiwun B, Young L, Cote RJ, Taylor CR, (1993) Antigen retrieval technique utilizing citrate buffer or urea solution for immunohistochemical demonstration of androgen receptor in formalin-fixed paraffin sections. J Histochem Cytochem 41: 1599-1604.