Pax8 and Pax2 are specifically required at different steps of Xenopus pronephros development

Developmental Biology

Volumn 397, Issue 2, 2015, Pages 175-190

  Buisson, Isabelle ^a,b   Le Bouffant, Ronan ^a,b   Futel, Mélinée ^a,b   Riou, Jean François ^a,b   Umbhauer, Muriel ^a,b  

^a SORBONNE UNIVERSITÉ   (France)

^b CNRS   (France)

Author keywords

Hnf1b; Pax2 8; Proliferation; Pronephros; Wnt; Xenopus

Indexed keywords

BETA CATENIN; DISHEVELLED 1; HNF1B PROTEIN; LHX1 PROTEIN; OSR2 PROTEIN; SFRP3 PROTEIN; TRANSCRIPTION FACTOR PAX2; TRANSCRIPTION FACTOR PAX8; UNCLASSIFIED DRUG; WNT PROTEIN; BROXURIDINE; PAIRED BOX TRANSCRIPTION FACTOR; PAX8 PROTEIN, XENOPUS; PRIMER DNA; XENOPUS PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD; CARDIOVASCULAR SYSTEM; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; CORRELATION ANALYSIS; DEVELOPMENTAL STAGE; EMBRYO; EMBRYONIC STRUCTURES; ENDOTHELIUM; GENE EXPRESSION; GLOMUS DEVELOPMENT; KIDNEY DEVELOPMENT; LOSS OF FUNCTION MUTATION; NONHUMAN; PRONEPHRIC TUBULE; PRONEPHROS; PRONEPHROS DEVELOPMENT; PROTEIN FUNCTION; WNT SIGNALING PATHWAY; XENOPUS; ANIMAL; EMBRYOLOGY; GENE EXPRESSION REGULATION; GENETICS; IN SITU HYBRIDIZATION; METABOLISM; PHYSIOLOGY; POLYMERASE CHAIN REACTION; REAL TIME POLYMERASE CHAIN REACTION;

GLOMUS; VERTEBRATA;

ANIMALS; BROMODEOXYURIDINE; DNA PRIMERS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IN SITU HYBRIDIZATION; PAIRED BOX TRANSCRIPTION FACTORS; PAX2 TRANSCRIPTION FACTOR; POLYMERASE CHAIN REACTION; PRONEPHROS; REAL-TIME POLYMERASE CHAIN REACTION; WNT SIGNALING PATHWAY; XENOPUS; XENOPUS PROTEINS;

EID: 84919608208     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2014.10.022     Document Type: Article

References (87)

1. Anderson C.B., Neufeld K.L., White R.L. Subcellular distribution of Wnt pathway proteins in normal and neoplastic colon. Proc. Natl. Acad. Sci. USA 2002, 99:8683-8688.
2. Batista M.F., Lewis K.E. Pax2/8 act redundantly to specify glycinergic and GABAergic fates of multiple spinal interneurons. Dev. Biol. 2008, 323:88-97.
3. Bello V., Sirour C., Moreau N., Denker E., Darribere T. A function for dystroglycan in pronephros development in Xenopus laevis. Dev. Biol. 2008, 317:106-120.
4. Bohn S., Thomas H., Turan G., Ellard S., Bingham C., Hattersley A.T., Ryffel G.U. Distinct molecular and morphogenetic properties of mutations in the human HNF1beta gene that lead to defective kidney development. J. Am. Soc. Nephrol. 2003, 14:2033-2041.
5. Bouchard M., Pfeffer P., Busslinger M. Functional equivalence of the transcription factors Pax2 and Pax5 in mouse development. Development 2000, 127:3703-3713.
6. Bouchard M., Souabni A., Mandler M., Neubuser A., Busslinger M. Nephric lineage specification by Pax2 and Pax8. Genes Dev. 2002, 16:2958-2970.
7. Brand M., Heisenberg C.P., Jiang Y.J., Beuchle D., Lun K., FurutaniSeiki M., Granato M., Haffter P., Hammerschmidt M., Kane D.A., Kelsh R.N., Mullins M.C., Odenthal J., vanEeden F.J.M., NussleinVolhard C. Mutations in zebrafish genes affecting the formation of the boundary between midbrain and hindbrain. Development 1996, 123:179-190.
8. Brandli A.W. Towards a molecular anatomy of the Xenopus pronephric kidney. Int. J. Dev. Biol. 1999, 43:381-395.
9. Brennan H.C., Nijjar S., Jones E.A. The specification of the pronephric tubules and duct in Xenopus laevis. Mech. Dev. 1998, 75:127-137.
10. Brennan H.C., Nijjar S., Jones E.A. The specification and growth factor inducibility of the pronephric glomus in Xenopus laevis. Development 1999, 126:5847-5856.
11. Brophy P.D., Lang K.M., Dressler G.R. The secreted frizzled related protein 2 (SFRP2) gene is a target of the Pax2 transcription factor. J. Biol. Chem. 2003, 278:52401-52405.
12. Brown L.A., Rodaway A.R., Schilling T.F., Jowett T., Ingham P.W., Patient R.K., Sharrocks A.D. Insights into early vasculogenesis revealed by expression of the ETS-domain transcription factor Fli-1 in wild-type and mutant zebrafish embryos. Mech. Dev. 2000, 90:237-252.
13. Burton Q., Cole L.K., Mulheisen M., Chang W., Wu D.K. The role of Pax2 in mouse inner ear development. Dev. Biol. 2004, 272:161-175.
14. Cai Y., Brophy P.D., Levitan I., Stifani S., Dressler G.R. Groucho suppresses Pax2 transactivation by inhibition of JNK-mediated phosphorylation. EMBO J. 2003, 22:5522-5529.
15. Carroll T.J., Vize P.D. Wilms[U+05F3] tumor suppressor gene is involved in the development of disparate kidney forms: evidence from expression in the Xenopus pronephros. Dev. Dyn. 1996, 206:131-138.
16. Carroll T.J., Vize P.D. Wilms[U+05F3] tumor suppressor gene is involved in the development of disparate kidney forms: evidence from expression in the Xenopus pronephros. Dev. Dyn. 1996, 206:131-138.
17. Carroll T.J., Vize P.D. Synergism between Pax-8 and lim-1 in embryonic kidney development. Dev. Biol. 1999, 214:46-59.
18. Carroll T.J., Wallingford J.B., Vize P.D. Dynamic patterns of gene expression in the developing pronephros of Xenopus laevis. Dev. Genet. 1999, 24:199-207.
19. Ciau-Uitz A., Liu F., Patient R. Genetic control of hematopoietic development in Xenopus and zebrafish. Int. J. Dev. Biol. 2010, 54:1139-1149.
20. Cleaver O., Tonissen K.F., Saha M.S., Krieg P.A. Neovascularization of the Xenopus embryo. Dev. Dyn. 1997, 210:66-77.
21. Colas A., Cartry J., Buisson I., Umbhauer M., Smith J.C., Riou J.F. Mix.1/2-dependent control of FGF availability during gastrulation is essential for pronephros development in Xenopus. Dev. Biol. 2008, 320:351-365.
22. de Croze N., Maczkowiak F., Monsoro-Burq A.H. Reiterative AP2a activity controls sequential steps in the neural crest gene regulatory network. P. Natl. Acad. Sci. USA 2011, 108:155-160.
23. del Viso F., Bhattacharya D., Kong Y., Gilchrist M.J., Khokha M.K. Exon capture and bulk segregant analysis: rapid discovery of causative mutations using high-throughput sequencing. BMC Genomics 2012, 13.
24. Dressler G.R., Deutsch U., Chowdhury K., Nornes H.O., Gruss P. Pax2, a new murine paired-box-containing gene and its expression in the developing excretory system. Development 1990, 109:787-795.
25. Dressler G.R., Douglass E.C. Pax-2 is a DNA-binding protein expressed in embryonic kidney and Wilms tumor. Proc. Natl. Acad. Sci. USA 1992, 89:1179-1183.
26. Dressler G.R., Wilkinson J.E., Rothenpieler U.W., Patterson L.T., Williams-Simons L., Westphal H. Deregulation of Pax-2 expression in transgenic mice generates severe kidney abnormalities. Nature 1993, 362:65-67.
27. Drummond I.A., Majumdar A., Hentschel H., Elger M., Solnica-Krezel L., Schier A.F., Neuhauss S.C., Stemple D.L., Zwartkruis F., Rangini Z., Driever W., Fishman M.C. Early development of the zebrafish pronephros and analysis of mutations affecting pronephric function. Development 1998, 125:4655-4667.
28. Eberhard D., Jimenez G., Heavey B., Busslinger M. Transcriptional repression by Pax5 (BSAP) through interaction with corepressors of the Groucho family. EMBO J. 2000, 19:2292-2303.
29. Eccles M.R., Wallis L.J., Fidler A.E., Spurr N.K., Goodfellow P.J., Reeve A.E. Expression of the PAX2 gene in human fetal kidney and Wilms[U+05F3] tumor. Cell Growth differ. 1992, 3:279-289.
30. El-Hodiri H., Bhatia-Dey N., Kenyon K., Ault K., Dirksen M., Jamrich M. Fox (forkhead) genes are involved in the dorso-ventral patterning of the Xenopus mesoderm. Int. J. Dev. Biol. 2001, 45:265-271.
31. Freter S., Muta Y., O'Neill P., Vassilev V.S., Kuraku S., Ladher R.K. Pax2 modulates proliferation during specification of the otic and epibranchial placodes. Dev. Dyn. 2012, 241:1716-1728.
32. Gering M., Rodaway A.R., Gottgens B., Patient R.K., Green A.R. The SCL gene specifies haemangioblast development from early mesoderm. EMBO J. 1998, 17:4029-4045.
33. Gerth V.E., Zhou X., Vize P.D. Nephrin expression and three-dimensional morphogenesis of the Xenopus pronephric glomus. Dev. Dyn. 2005, 233:1131-1139.
34. Haldin C.E., Masse K.L., Bhamra S., Simrick S., Kyuno J.I., Jones E.A. The lmx1b gene is pivotal in glomus development in Xenopus laevis. Dev. Biol. 2008, 322:74-85.
35. Hammachi F., Morrison G.M., Sharov A.A., Livigni A., Narayan S., Papapetrou E.P., O'Malley J., Kaji K., Ko M.S.H., Ptashne M., Brickman J.M. Transcriptional activation by Oct4 is sufficient for the maintenance and induction of pluripotency. Cell Rep. 2012, 1:99-109.
36. Hardcastle Z., Papalopulu N. Distinct effects of XBF-1 in regulating the cell cycle inhibitor p27(XIC1) and imparting a neural fate. Development 2000, 127:1303-1314.
37. Harland R.M. In situ hybridization: an improved whole-mount method for Xenopus embryos. Methods Cell Biol. 1991, 36:685-695.
38. Harris W.A., Hartenstein V. Neuronal determination without cell division in Xenopus embryos. Neuron 1991, 6:499-515.
39. Heliot C., Desgrange A., Buisson I., Prunskaite-Hyyrylainen R., Shan J., Vainio S., Umbhauer M., Cereghini S. HNF1B controls proximal-intermediate nephron segment identity in vertebrates by regulating Notch signalling components and Irx1/2. Development 2013, 140:873-885.
40. Heller N., Brandli A.W. Xenopus Pax-2 displays multiple splice forms during embryogenesis and pronephric kidney development. Mech. Dev. 1997, 69:83-104.
41. Heller N., Brandli A.W. 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. 1999, 24:208-219.
42. Inui M., Fukui A., Ito Y., Asashima M. Xapelin and Xmsr are required for cardiovascular development in Xenopus laevis. Dev. Biol. 2006, 298:188-200.
43. Kimmel C.B., Warga R.M., Schilling T.F. Origin and organization of the zebrafish fate map. Development 1990, 108:581-594.
44. Kolm P.J., Sive H.L. Efficient hormone-inducible protein function in Xenopus laevis. Dev. Biol. 1995, 171:267-272.
45. Le Bouffant R., Wang J.H., Futel M., Buisson I., Umbhauer M., Riou J.F. Retinoic acid-dependent control of MAP kinase phosphatase-3 is necessary for early kidney development in Xenopus. Biol. Cell 2012, 104:516-532.
46. Li C.G., Nyman J.E., Braithwaite A.W., Eccles M.R. PAX8 promotes tumor cell growth by transcriptionally regulating E2F1 and stabilizing RB protein. Oncogene 2011, 30:4824-4834.
47. Li H., Liu H., Corrales C.E., Mutai H., Heller S. Correlation of Pax-2 expression with cell proliferation in the developing chicken inner ear. J. Neurobiol. 2004, 60:61-70.
48. Lyons J.P., Miller R.K., Zhou X., Weidinger G., Deroo T., Denayer T., Park J.I., Ji H., Hong J.Y., Li A., Moon R.T., Jones E.A., Vleminckx K., Vize P.D., McCrea P.D. Requirement of Wnt/beta-catenin signaling in pronephric kidney development. Mech. Dev. 2009, 126:142-159.
49. Majumdar A., Lun K., Brand M., Drummond I.A. Zebrafish no isthmus reveals a role for pax2.1 in tubule differentiation and patterning events in the pronephric primordia. Development 2000, 127:2089-2098.
50. Mansouri A., Chowdhury K., Gruss P. Follicular cells of the thyroid gland require Pax8 gene function. Nat. Genet. 1998, 19:87-90.
51. McCoy K.E., Zhou X.L., Vize P.D. Non-canonical wnt signals antagonize and canonical wnt signals promote cell proliferation in early kidney development. Dev. Dyn. 2011, 240:1558-1566.
52. Mead P.E., Deconinck A.E., Huber T.L., Orkin S.H., Zon L.I. Primitive erythropoiesis in the Xenopus embryo: the synergistic role of LMO-2, SCL and GATA-binding proteins. Development 2001, 128:2301-2308.
53. Molenaar M., Brian E., Roose J., Clevers H., Destree O. Differential expression of the Groucho-related genes 4 and 5 during early development of Xenopus laevis. Mech. Dev. 2000, 91:311-315.
54. Mudumana S.P., Hentschel D., Liu Y., Vasilyev A., Drummond I.A. odd skipped related1 reveals a novel role for endoderm in regulating kidney versus vascular cell fate. Development 2008, 135:3355-3367.
55. Naylor R.W., Jones E.A. Notch activates Wnt-4 signalling to control medio-lateral patterning of the pronephros. Development 2009, 136:3585-3595.
56. Naylor R.W., Przepiorski A., Ren Q., Yu J., Davidson A.J. HNF1 beta is essential for nephron segmentation during nephrogenesis. J. Am. Soc. Nephrol. 2013, 24:77-87.
57. Nieuwkoop P.D., Faber J. Normal table of Xenopus lævis (Daudin) 1967, North-Holland Publishing Company, Amsterdam. 2nd ed.
58. Nornes H.O., Dressler G.R., Knapik E.W., Deutsch U., Gruss P. Spatially and temporally restricted expression of Pax2 during murine neurogenesis. Development 1990, 109:797-809.
59. Ordonez N.G. Value of PAX2 immunostaining in tumor diagnosis: a review and update. Adv. Anat. Pathol. 2012, 19:401-409.
60. Ordonez N.G. Value of PAX 8 immunostaining in tumor diagnosis: a review and update. Adv. Anat. Pathol. 2012, 19:140-151.
61. Plachov D., Chowdhury K., Walther C., Simon D., Guenet J.L., Gruss P. Pax8, a murine paired box gene expressed in the developing excretory system and thyroid-gland. Development 1990, 110:643.
62. Raciti D., Reggiani L., Geffers L., Jiang Q., Bacchion F., Subrizi A.E., Clements D., Tindal C., Davidson D.R., Kaissling B., Brandli A.W. Organization of the pronephric kidney revealed by large-scale gene expression mapping. Genome Biol. 2008, 9:R84.
63. Ryan G., Steele-Perkins V., Morris J.F., Rauscher F.J., Dressler G.R. Repression of Pax-2 by WT1 during normal kidney development. Development 1995, 121:867-875.
64. Sato A., Asashima M., Yokota T., Nishinakamura R. Cloning and expression pattern of a Xenopus pronephros-specific gene, XSMP-30. Mech. dev. 2000, 92:273-275.
65. Saxen L. Organogenesis of the Kidney 1987, Cambridge University Press, Cambridge, UK.
66. Schedl A., Hastie N.D. Cross-talk in kidney development. Curr. Opin. Genet. Dev. 2000, 10:543-549.
67. Short S., Kozmik Z., Holland L.Z. The function and developmental expression of alternatively spliced isoforms of amphioxus and Xenopus laevis Pax2/5/8 genes: revealing Divergence at the invertebrate to vertebrate transition. J. Exp. Zool. Part B 2012, 318B:555-571.
68. Tada M., O'Reilly M.A., Smith J.C. Analysis of competence and of Brachyury autoinduction by use of hormone-inducible Xbra. Development 1997, 124:2225-2234.
69. Taelman V., Van Campenhout C., Solter M., Pieler T., Bellefroid E.J. The Notch-effector HRT1 gene plays a role in glomerular development and patterning of the Xenopus pronephros anlagen. Development 2006, 133:2961-2971.
70. Tamimi Y., Ekuere U., Laughton N., Grundy P. WNT5A is regulated by PAX2 and may be involved in blastemal predominant Wilms tumorigenesis. Neoplasia 2008, 10:1470-1480.
71. Tena J.J., Neto A., de la Calle-Mustienes E., Bras-Pereira C., Casares F., Gomez-Skarmeta J.L. Odd-skipped genes encode repressors that control kidney development. Dev. Biol. 2007, 301:518-531.
72. Tetelin S., Jones E.A. Xenopus Wnt11b is identified as a potential pronephric inducer. Dev. Dyn. 2010, 239:148-159.
73. Tong G.X., Yu W.M., Beaubier N.T., Weeden E.M., Hamele-Bena D., Mansukhani M.M., O'Toole K.M. Expression of PAX8 in normal and neoplastic renal tissues: an immunohistochemical study. Mod. Pathol. 2009, 22:1218-1227.
74. Torban E., Dziarmaga A., Iglesias D., Chu L.L., Vassilieva T., Little M., Eccles M., Discenza M., Pelletier J., Goodyer P. PAX2 activates WNT4 expression during mammalian kidney development. J. Biol. Chem. 2006, 281:12705-12712.
75. Torres M., GomezPardo E., Dressler G.R., Gruss P. Pax-2 controls multiple steps of urogenital development. Development 1995, 121:4057-4065.
76. Umbhauer M., Penzo-Mendez A., Clavilier L., Boucaut J.C., Riou J.F. Signaling specificities of fibroblast growth factor receptors in early Xenopus embryo. J. Cell Sci. 2000, 113:2865-2875.
77. Van Campenhout C., Nichane M., Antoniou A., Pendeville H., Bronchain O.J., Marine J.C., Mazabraud A., Voz M.L., Bellefroid E.J. Evi1 is specifically expressed in the distal tubule and duct of the Xenopus pronephros and plays a role in its formation. Dev. Biol. 2006, 294:203-219.
78. Vize P.D., Jones E.A., Pfister R. Development of the Xenopus pronephric system. Dev. Biol. 1995, 171:531-540.
79. Vize P.D., Seufert D.W., Carroll T.J., Wallingford J.B. Model systems for the study of kidney development: use of the pronephros in the analysis of organ induction and patterning. Dev. Biol. 1997, 188:189-204.
80. Vize P.D., Woolf A.S., Bard J.B.L. The Kidney: From Normal Development to Congenital Disease 2003, Academic Press, London, UK.
81. Wagner K.D., Wagner N., Guo J.K., Elger M., Dallman M.J., Bugeon L., Schedl A. An inducible mouse model for PAX2-dependent glomerular disease: insights into a complex pathogenesis. Curr. Biol. 2006, 16:793-800.
82. Wallingford J.B., Carroll T.J., Vize P.D. Precocious expression of the Wilms[U+05F3] tumor gene xWT1 inhibits embryonic kidney development in Xenopus laevis. Dev. Biol. 1998, 202:103-112.
83. Walmsley M., Ciau-Uitz A., Patient R. Adult and embryonic blood and endothelium derive from distinct precursor populations which are differentially programmed by BMP in Xenopus. Development 2002, 129:5683-5695.
84. Yang Y., Jeanpierre C., Dressler G.R., Lacoste M., Niaudet P., Gubler M.C. WT1 and PAX-2 podocyte expression in Denys-Drash syndrome and isolated diffuse mesangial sclerosis. Am. J. Pathol. 1999, 154:181-192.
85. Zhang B., Tran U., Wessely O. Expression of Wnt signaling components during Xenopus pronephros development. Plos One 2011, 6:e26533.
86. Zhang H.S., Yan B., Li X.B., Fan L., Zhang Y.F., Wu G.H., Li M., Fang J. PAX2 protein induces expression of cyclin D1 through activating AP-1 protein and promotes proliferation of colon cancer cells. J. Biol. Chem. 2012, 287:44164-44172.
87. Zhou X., Vize P.D. Proximo-distal specialization of epithelial transport processes within the Xenopus pronephric kidney tubules. Dev. Biol. 2004, 271:322-338.