Patterning the embryonic kidney: BMP signaling mediates the differentiation of the pronephric tubules and duct in Xenopus laevis

Developmental Dynamics

Volumn 237, Issue 1, 2008, Pages 132-144

  Bracken, Christina M ^a   Mizeracka, Karolina ^a   McLaughlin, Kelly A ^a  

^a TUFTS UNIVERSITY   (United States)

Author keywords

BMP signaling; Development; Duct; Kidney; Morphogenesis; Nephron; Organogenesis; Patterning; Pronephros; Tubules; Xenopus laevis

Indexed keywords

BONE MORPHOGENETIC PROTEIN;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; EMBRYO PATTERN FORMATION; KIDNEY DEVELOPMENT; KIDNEY TUBULE; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TISSUE DIFFERENTIATION; XENOPUS LAEVIS;

ANIMALS; BODY PATTERNING; BONE MORPHOGENETIC PROTEINS; CELL DIFFERENTIATION; EMBRYO, NONMAMMALIAN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; IN SITU NICK-END LABELING; KIDNEY; KIDNEY TUBULES; MICROINJECTIONS; MORPHOGENESIS; NEPHRONS; RECEPTORS, GLUCOCORTICOID; RNA, MESSENGER; SIGNAL TRANSDUCTION; SMAD6 PROTEIN; XENOPUS LAEVIS; XENOPUS PROTEINS;

AMPHIBIA; GLOMUS; MAMMALIA; MUS; VERTEBRATA; XENOPUS LAEVIS;

EID: 38149057248     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.21387     Document Type: Article

References (88)

1. Beck CW, Christen B, Barker D, Slack JM. 2006. Temporal requirement for bone morphogenetic proteins in regeneration of the tail and limb of Xenopus tadpoles. Mech Dev 123:674-688.
2. Bovolenta P. 2005. Morphogen signaling at the vertebrate growth cone: a few cases or a general strategy? J Neurobiol 64:405-416.
3. Brandli AW. 1999. Towards a molecular anatomy of the Xenopus pronephric kidney. Int J Dev Biol 43:381-395.
4. Breckenridge RA, Mohun TJ, Amaya E. 2001. A role for BMP signalling in heart looping morphogenesis in Xenopus. Dev Biol 232:191-203.
5. Brennan HC, Nijjar S, Jones EA. 1998. The specification of the pronephric tubules and duct in Xenopus laevis. Mech Dev 57:127-137.
6. Brennan H, Nijar S, Jones EA. 1999. The specification and growth factor inducibility of the pronephric glomus in Xenopus laevis. Development 126:5847-5856.
7. Carroll TJ, Vize PD. 1996. Wilms' tumor suppressor gene is involved in the development of disparate kidney forms: evidence from expression in the Xenopus pronephros. Dev Dyn 206:131-138.
8. Carroll TJ, Vize PD. 1999. Synergism between Pax-8 and Lim-1 in embryonic kidney development. Dev Biol 214:46-59.
9. Carroll TJ, Wallingford JB, Vize PD. 1999. Dynamic patterns of gene expression in the developing pronephros of Xenopus laevis. Dev Genet 24:199-207.
10. Chan TC, Takahashi S, Asashima M. 2000. A role for Xlim-1 in pronephros development in Xenopus laevis. Dev Biol 228:256-269.
11. Dale L, Jones CM. 1999. BMP signalling in early Xenopus development. Bioessays 21:751-760.
12. Dosch R, Gawantka V, Delius H, Blumenstock C, Niehrs C. 1997. Bmp-4 acts as a morphogen in dorsoventral mesoderm patterning in Xenopus. Development 124:2325-2334.
13. Drawbridge J, Wolfe AE, Delgado YL, Steinberg MS. 1995. The epidermis is a source of directional information for the migrating pronephric duct in Ambystoma mexicanum embryos. Dev Biol 172:440-451.
14. Drummond IA, Majumdar A, Hentschel H, Elger M, Solnica-Krezel L, Schier AF, Neuhauss SC, Stemple DL, Zwartkruis F, Rangini Z, Driever W, Fishman MC. 1998. Early development of the zebrafish pronephros and analysis of mutations affecting pronephric function. Development 125:4655-4667.
15. 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.
16. Durbec P, Marcos-Gutierrez CV, Kilkenny C, Grigoriou M, Wartiowaara K, Suvanto P, Smith D, Ponder B, Costantini F, Saarma M, Sariola H, Pachnis V. 1996. GDNF signalling through the Ret receptor tyrosine kinase. Nature 381:789-793.
17. Eid SR, Brandli AW. 2001. Xenopus Na,K-ATPase: primary sequence of the beta2 subunit and in situ localization of alpha1, beta1, and gamma expression during pronephric kidney development. Differentiation 68:115-125.
18. Faure S, Lee MA, Keller T, ten Dijke P, Whitman M. 2000. Endogenous patterns of TGFbeta superfamily signaling during early Xenopus development. Development 127:2917-2931.
19. Faure S, de Santa Barbara P, Roberts DJ, Whitman M. 2002. Endogenous patterns of BMP signaling during early chick development. Dev Biol 244:44-65.
20. Gerth VE, Zhou X, Vize PD. 2005. Nephrin expression and three-dimensional morphogenesis of the Xenopus pronephric glomus. Dev Dyn 233:1131-1139.
21. Godin RE, Takaesu NT, Robertson EJ, Dudley AT. 1998. Regulation of BMP7 expression during kidney development. Development 125:3473-3482.
22. Graff JM. 1997. Embryonic patterning: to BMP or not to BMP, that is the question. Cell 89:171-174.
23. Harland RM. 1991. In situ hybridization: an improved whole-mount method for Xenopus embryos. Methods Cell Biol 36:685-695.
24. Harland R. 2000. Neural induction. Curr Opin Genet Dev 10:357-362.
25. Hawley SH, Wunnenberg-Stapleton K, Hashimoto C, Laurent MN, Watabe T, Blumberg BW, Cho KW. 1995. Disruption of BMP signals in embryonic Xenopus ectoderm leads to direct neural induction. Genes Dev 9:2923-2935.
26. Heller N, Brandli AW. 1999. Xenopus Pax-2/5/8 orthologues: novel insights into Pax gene evolution and identification of Pax-8 as the earliest marker for otic and pronephric cell lineages. Dev Genet 24:208-219.
27. Hemmati-Brivanlou A, Thomsen GH. 1995. Ventral mesodermal patterning in Xenopus embryos: expression patterns and activities of BMP-2 and BMP-4. Dev Genet 17:78-89.
28. Hensey C, Gautier J. 1998. Programmed cell death during Xenopus development: a spatio-temporal analysis. Dev Biol 203:36-48.
29. Hocking JC, McFarlane S. 2007. Expression of Bmp ligands and receptors in the developing Xenopus retina. Int J Dev Biol 51:161-165.
30. Hogan BL. 1996. Bone morphogenetic proteins in development. Curr Opin Genet Dev 6:432-438.
31. Hsu DR, Economides AN, Wang X, Eimon PM, Harland RM. 1998. The Xenopus dorsalizing factor Gremlin identifies a novel family of secreted proteins that antagonize BMP activities. Mol Cell 1:673-683.
32. Huber TB, Benzing T. 2005. The slit diaphragm: a signaling platform to regulate podocyte function. Curr Opin Nephrol Hypertens 14:211-216.
33. Ishisaki A, Yamato K, Hashimoto S, Nakao A, Tamaki K, Nonaka K, ten Dijke P, Sugino H, Nishihara T. 1999. Differential inhibition of Smad6 and Smad7 on bone morphogenetic protein- and activin-mediated growth arrest and apoptosis in B cells. J Biol Chem 274:13637-13642.
34. Jamali M, Karamboulas C, Rogerson PJ, Skerjanc IS. 2001. BMP signaling regulates Nkx2-5 activity during cardiomyogenesis. FEBS Lett 509:126-130.
35. James RG, Schultheiss TM. 2005. Bmp signaling promotes intermediate mesoderm gene expression in a dose-dependent, cell-autonomous and translation-dependent manner. Dev Biol 288:113-125.
36. Johnstone DB, Holzman LB. 2006. Clinical impact of research on the podocyte slit diaphragm. Nat Clin Pract Nephrol 2:271-282.
37. Kolm PJ, Sive HL. 1995. Efficient hormone-inducible protein function in Xenopus laevis. Dev Biol 171:267-272.
38. Kumano G, Ezal C, Smith WC. 2006. ADMP2 is essential for primitive blood and heart development in Xenopus. Dev Biol 299:411-423.
39. Kurata T, Nakabayashi J, Yamamoto TS, Mochii M, Ueno N. 2001. Visualization of endogenous BMP signaling during Xenopus development. Differentiation 67:33-40.
40. Lane MC, Davidson L, Sheets MD. 2004. BMP antagonism by Spemann's organizer regulates rostral-caudal fate of mesoderm. Dev Biol 275:356-374.
41. Lane MC, Sheets MD. 2000. Designation of the anterior/posterior axis in pregastrula Xenopus laevis. Dev Biol 225:37-58.
42. Lane MC, Sheets MD. 2002. Rethinking axial patterning in amphibians. Dev Dyn 225:434-447.
43. Lane MC, Sheets MD. 2006. Heading in a new direction: implications of the revised fate map for understanding Xenopus laevis development. Dev Biol 296:12-28.
44. Lang RA. 2004. Pathways regulating lens induction in the mouse. Int J Dev Biol 48:783-791.
45. Li X, Cao X. 2003. BMP signaling and HOX transcription factors in limb development. Front Biosci 8:s805-812.
46. Luo G, Hofmann C, Bronckers AL, Sohocki M, Bradley A, Karsenty G. 1995. BMP-7 is an inducer of nephrogenesis, and is also required for eye development and skeletal patterning. Genes Dev 9:2808-2820.
47. Martinez G, Mishina Y, Bertram JF. 2002. BMPs and BMP receptors in mouse metanephric development: in vivo and in vitro studies. Int J Dev Biol 46:525-533.
48. Mauch TJ, Yang G, Wright M, Smith D, Schoenwolf GC. 2000. Signals from trunk paraxial mesoderm induce pronephros formation in chick intermediate mesoderm. Dev Biol 220:62-75.
49. Mitchell T, Jones EA, Weeks DL, Sheets MD. 2007. Chordin affects pronephros development in Xenopus embryos by anteriorizing presomitic mesoderm. Dev Dyn 236:251-261.
50. Mohun TJ, Brennan S, Dathan N, Fairman S, Gurdon JB. 1984. Cell type-specific activation of actin genes in the early amphibian embryo. Nature 311:716-721.
51. Moreau M, Leclerc C. 2004. The choice between epidermal and neural fate: a matter of calcium. Int J Dev Biol 48:75-84.
52. Nakayama T, Gardner H, Berg LK, Christian JL. 1998. Smad6 functions as an intracellular antagonist of some TGF-b family members during Xenopus embryogenesis. Genes Cell 3:387-394.
53. Nieuwkoop PD, Faber J. 1994. Normal table of Xenopus laevis. Amsterdam: North-Holland Publishing Company.
54. Obara-Ishihara T, Kuhlman J, Niswander L, Herzlinger D. 1999. The surface ectoderm is essential for nephric duct formation in intermediate mesoderm. Development 126:1103-1108.
55. Oxburgh L, Robertson EJ. 2002. Dynamic regulation of Smad expression during mesenchyme to epithelium transition in the metanephric kidney. Mech Dev 112:207-211.
56. 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.
57. Peng HB. 1991. Solution and protocols. In: Methods cell biology. p 657-662.
58. Piccolo S, Sasai Y, Lu B, DeRobertis EM. 1996. Dorsoventral patterning in Xenopus: inhibition of ventral signals by direct binding of chordin to bmp-4. Cell 86:589-598.
59. Sasai Y, Lu B, Steinbeisser H, Geissert D, Gont LK, De Robertis EM. 1994. Xenopus chordin: a novel dorsalizing factor activated by organizer-specific homeobox genes. Cell 79:779-790.
60. Sato A, Asashima M, Yokota T, Nishinakamura R. 2000. Cloning and expression pattern of a Xenopus pronephros-specific gene, XSMP-30. Mech Dev 92:273-275.
61. Saxén L. 1987. Organogenesis of the kidney. Cambridge: Cambridge University Press.
62. Schier AF, Talbot WS. 2005. Molecular genetics of axis formation in zebrafish. Annu Rev Genet 39:561-613.
63. Schmerer M, Evans T. 2003. Primitive erythropoiesis is regulated by Smad-dependent signaling in postgastrulation mesoderm. Blood 102:3196-3205.
64. Semba K, Saito-Ueno R, Takayama G, Kondo M. 1996. cDNA cloning and its pronephros-specific expression of the Wilms' tumor suppressor gene, WT1, from Xenopus laevis. Gene 175:167-172.
65. Seufert DW, Brennan HC, DeGuire J, Jones EA, Vize PD. 1999. Developmental basis of pronephric defects in Xenopus body plan phenotypes. Dev Biol 215:233-242.
66. Shawlot W, Behringer RR. 1995. Requirement for Lim1 in head-organizer function. Nature 374:425-430.
67. Shi Y, Katsev S, Cai C, Evans S. 2000. BMP signaling is required for heart formation in vertebrates. Dev Biol 224:226-237.
68. Slack JM, Beck CW, Gargioli C, Christen B. 2004. Cellular and molecular mechanisms of regeneration in Xenopus. Philos Trans R Soc Lond B Biol Sci 359:745-751.
69. Smith JC. 1995. Mesoderm-inducing factors and mesodermal patterning. Curr Opin Cell Biol 7:856-861.
70. Sugimoto H, Yang C, LeBleu VS, Soubasakos MA, Giraldo M, Zeisberg M, Kalluri R. 2007. BMP-7 functions as a novel hormone to facilitate liver regeneration. Faseb J 21:256-264.
71. Suzuki A, Ueno N, Hemmati-Brivanlou A. 1997. Xenopus msx1 mediates epidermal induction and neural inhibition by BMP4. Development 124:3037-3044.
72. Taira M, Otani H, Jamrich M, Dawid IB. 1994. Expression of the LIM class homeobox gene Xlim-1 in pronephros and CNS cell lineages of Xenopus embryos is affected by retinoic acid and exogastrulation. Development 120:1525-1536.
73. Torres M, Gomez-Pardo E, Dressler GR, Gruss P. 1995. Pax-2 controls multiple steps of urogenital development. Development 121:4057-4065.
74. Urban AE, Zhou X, Ungos JM, Raible DW, Altmann CR, Vize PD. 2006. FGF is essential for both condensation and mesenchymal-epithelial transition stages of pronephric kidney tubule development. Dev Biol 297:103-117.
75. Urist MR. 1965. Bone: formation by auto-induction. Science 150:893-899.
76. Vize PD. 2003. The chloride conductance channel ClC-K is a specific marker for the Xenopus pronephric distal tubule and duct. Gene Expr Patterns 3:347-350.
77. Vize PD, Jones EA, Pfister R. 1995. Development of the Xenopus pronephric system. Dev Biol 171:531-540.
78. Vize PD, Seufert DW, Carroll TJ, Wallingford JB. 1997. Model systems for the study of kidney development: use of the pronephros in the analysis of organ induction and patterning. Dev Biol 188:189-204.
79. Vrljicak P, Myburgh D, Ryan AK, van Rooijen MA, Mummery CL, Gupta IR. 2004. Smad expression during kidney development. Am J Physiol Renal Physiol 286:F625-633.
80. Wallingford JB, Carroll TJ, Vize PD. 1998. Precocious expression of the Wilms' tumor gene xWT1 inhibits embryonic kidney development in Xenopus laevis. Dev Biol 202:103-112.
81. Wang S, Krinks M, Kleinwaks L, Moos M Jr. 1997. A novel Xenopus homologue of bone morphogenetic protein-7 (BMP-7). Genes Funct 1:259-271.
82. Wardle FC, Welch JV, Dale L. 1999. Bone morphogenetic protein 1 regulates dorsal-ventral patterning in early Xenopus embryos by degrading chordin, a BMP4 antagonist. Mech Dev 86:75-85.
83. Wawersik S, Evola C, Whitman M. 2005. Conditional BMP inhibition in Xenopus reveals stage-specific roles for BMPs in neural and neural crest induction. Dev Biol 277:425-442.
84. Wozney JM, Rosen V, Celeste AJ, Mitsock LM, Whitters MJ, Kriz RW, Hewick RM, Wang EA. 1988. Novel regulators of bone formation: molecular clones and activities. Science 242:1528-1534.
85. Zhao GQ. 2003. Consequences of knocking out BMP signaling in the mouse. Genesis 35:43-56.
86. Zhou X, Vize PD. 2004. Proximo-distal specialization of epithelial transport processes within the Xenopus pronephric kidney tubules. Dev Biol 271:322-338.
87. Zorn AM, Butler K, Gurdon JB. 1999. Anterior endomesoderm specification in Xenopus by Wnt/beta-catenin and TGF-beta signalling pathways. Dev Biol 209:282-297.
88. Zou H, Choe KM, Lu Y, Massague J, Niswander L. 1997. BMP signaling and vertebrate limb development. Cold Spring Harb Symp Quant Biol 62:269-272.