Gene regulatory network of renal primordium development

Pediatric Nephrology

Volumn 29, Issue 4, 2014, Pages 637-644

  Marcotte, Michael ^a   Sharma, Richa ^a   Bouchard, Maxime ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

Gata3; Gene regulatory network; Kidney; Lxh1 Lim1; Mouse pronephros mesonephros; Pax2 Pax8

Indexed keywords

ACTIVIN; BETA CATENIN; BONE MORPHOGENETIC PROTEIN 4; FIBROBLAST GROWTH FACTOR; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; MATRIX METALLOPROTEINASE 14; PROTEIN RET; RETINOIC ACID; TRANSCRIPTION FACTOR EMX2; TRANSCRIPTION FACTOR GATA 3; TRANSCRIPTION FACTOR PAX2; TRANSCRIPTION FACTOR PAX8; UVOMORULIN; WNT11 PROTEIN;

BRANCHING MORPHOGENESIS; CELL MIGRATION; CELL PROLIFERATION; CELL SHAPE; CONFERENCE PAPER; ECTODERM; EMBRYO DEVELOPMENT; GENE ACTIVATION; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETIC CONSERVATION; HOX GENE; HYDRONEPHROSIS; KIDNEY AGENESIS; KIDNEY DEVELOPMENT; KIDNEY DUPLICATION; KIDNEY HYPOPLASIA; MESODERM; NONHUMAN; POSITIVE FEEDBACK; PRIMORDIUM; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANIMALS; EMBRYONIC DEVELOPMENT; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE REGULATORY NETWORKS; HUMANS; KIDNEY;

EID: 84896694893     PISSN: 0931041X     EISSN: 1432198X     Source Type: Journal    
DOI: 10.1007/s00467-013-2635-0     Document Type: Conference Paper

References (86)

1. Alon U (2007) Network motifs: theory and experimental approaches. Nat Rev Genet 8:450-461
2. Davidson EH (2010) Emerging properties of animal gene regulatory networks. Nature 468:911-920
3. Olson EN (2002) A genetic blueprint for growth and development of the heart. Harvey Lect 98:41-64
4. Davidson EH (2009) Network design principles from the sea urchin embryo. Curr Opin Genet Dev 19:535-540
5. Uetani N, Bouchard M (2009) Plumbing in the embryo: developmental defects of the urinary tracts. Clin Genet 75:307-317
6. Bouchard M, Souabni A, Busslinger M (2004) Tissue-specific expression of cre recombinase from the Pax8 locus. Genesis 38:105-109
7. Dressler GR (2006) The cellular basis of kidney development. Annu Rev Cell Dev Biol 22:509-529
8. Barak H, Rosenfelder L, Schultheiss TM, Reshef R (2005) Cell fate specification along the anterior-posterior axis of the intermediate mesoderm. Dev Dyn 232:901-914
9. 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
10. 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
11. 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
12. James RG, Kamei CN, Wang Q, Jiang R, Schultheiss TM (2006) Odd-skipped related 1 is required for development of the metanephric kidney and regulates formation and differentiation of kidney precursor cells. Development 133:2995-3004
13. Wilm B, James RG, Schultheiss TM, Hogan BL (2004) The forkhead genes, Foxc1 and Foxc2, regulate paraxial versus intermediate mesoderm cell fate. Dev Biol 271:176-189
14. Fleming BM, Yelin R, James RG, Schultheiss TM (2013) A role for Vg1/Nodal signaling in specification of the intermediate mesoderm. Development 140:1819-1829
15. Cartry J, Nichane M, Ribes V, Colas A, Riou JF, Pieler T, Dolle P, Bellefroid EJ, Umbhauer M (2006) Retinoic acid signalling is required for specification of pronephric cell fate. Dev Biol 299:35-51
16. Moriya N, Uchiyama H, Asashima M (1993) Induction of pronephric tubules by activin and retinoic acid in presumptive ectoderm of Xenopus laevis. Dev Growth Diff 35:123-128
17. Taira M, Jamrich M, Good PJ, Dawid IB (1992) The LIM domain-containing homeo box gene Xlim-1 is expressed specifically in the organizer region of Xenopus gastrula embryos. Genes Dev 6:356-366
18. 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
19. Wingert RA, Selleck R, Yu J, Song HD, Chen Z, Song A, Zhou Y, Thisse B, Thisse C, McMahon AP, Davidson AJ (2007) The cdx genes and retinoic acid control the positioning and segmentation of the zebrafish pronephros. PLoS Genet 3:1922-1938
20. Taira M, Otani H, Saint-Jeannet JP, Dawid IB (1994) Role of the LIM class homeodomain protein Xlim-1 in neural and muscle induction by the Spemann organizer in Xenopus. Nature 372:677-679
21. Preger-Ben Noon E, Barak H, Guttmann-Raviv N, Reshef R (2009) Interplay between activin and Hox genes determines the formation of the kidney morphogenetic field. Development 136:1995-2004
22. Attia L, Yelin R, Schultheiss TM (2012) Analysis of nephric duct specification in the avian embryo. Development 139:4143-4151
23. 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
24. Krauss S, Johansen T, Korzh V, Fjose A (1991) Expression of the zebrafish paired box gene pax[zf-b] during early neurogenesis. Development 113:1193-1206
25. Pfeffer PL, Gerster T, Lun K, Brand M, Busslinger M (1998) Characterization of three novel members of the zebrafish Pax2/5/8 family: dependency of Pax5 and Pax8 expression on the Pax2.1 (noi) function. Development 125:3063-3074
26. Puschel AW, Westerfield M, Dressler GR (1992) Comparative analysis of Pax-2 protein distributions during neurulation in mice and zebrafish. Mech Dev 38:197-208
27. Carroll TJ, Wallingford JB, Vize PD (1999) Dynamic patterns of gene expression in the developing pronephros of Xenopus laevis. Dev Genet 24:199-207
28. Sheng G, Stern CD (1999) Gata2 and Gata3: novel markers for early embryonic polarity and for non-neural ectoderm in the chick embryo. Mech Dev 87:213-216
29. Wingert RA, Davidson AJ (2011) Zebrafish nephrogenesis involves dynamic spatiotemporal expression changes in renal progenitors and essential signals from retinoic acid and irx3b. Dev Dyn 240:2011-2027
30. Bouchard M, Souabni A, Mandler M, Neubuser A, Busslinger M (2002) Nephric lineage specification by Pax2 and Pax8. Genes Dev 16:2958-2970
31. Barnes JD, Crosby JL, Jones CM, Wright CV, Hogan BL (1994) Embryonic expression of Lim-1, the mouse homolog of Xenopus Xlim-1, suggests a role in lateral mesoderm differentiation and neurogenesis. Dev Biol 161:168-178
32. Fujii T, Pichel JG, Taira M, Toyama R, Dawid IB, Westphal H (1994) Expression patterns of the murine LIM class homeobox gene lim1 in the developing brain and excretory system. Dev Dyn 199:73-83
33. 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 132:2809-2823
34. Tsang TE, Shawlot W, Kinder SJ, Kobayashi A, Kwan KM, Schughart K, Kania A, Jessell TM, Behringer RR, Tam PP (2000) Lim1 activity is required for intermediate mesoderm differentiation in the mouse embryo. Dev Biol 223:77-90
35. Pedersen A, Skjong C, Shawlot W (2005) Lim 1 is required for nephric duct extension and ureteric bud morphogenesis. Dev Biol 288:571-581
36. Shawlot W, Behringer RR (1995) Requirement for Lim1 in head-organizer function. Nature 374:425-430
37. Boualia SK, Gaitan Y, Tremblay M, Sharma R, Cardin J, Kania A, Bouchard M (2013) A core transcriptional network composed of Pax2/8, Gata3 and Lim1 regulates key players of pro/mesonephros morphogenesis. Dev Biol. doi: 10.1016/j.ydbio.2013.07.028
38. Grote D, Souabni A, Busslinger M, Bouchard M (2006) Pax2/8-regulated Gata3 expression is necessary for morphogenesis and guidance of the nephric duct in the developing kidney. Development 133:53-61
39. Boualia SK, Gaitan Y, Murawski I, Nadon R, Gupta IR, Bouchard M (2011) Vesicoureteral reflux and other urinary tract malformations in mice compound heterozygous for Pax2 and Emx2. PloS One 6:e21529
40. Bedell VM, Person AD, Larson JD, McLoon A, Balciunas D, Clark KJ, Neff KI, Nelson KE, Bill BR, Schimmenti LA, Beiraghi S, Ekker SC (2012) The lineage-specific gene ponzr1 is essential for zebrafish pronephric and pharyngeal arch development. Development 139:793-804
41. Linton JM, Martin GR, Reichardt LF (2007) The ECM protein nephronectin promotes kidney development via integrin alpha8beta1-mediated stimulation of Gdnf expression. Development 134:2501-2509
42. Grote D, Boualia SK, Souabni A, Merkel C, Chi X, Costantini F, Carroll T, Bouchard M (2008) Gata3 acts downstream of beta-catenin signaling to prevent ectopic metanephric kidney induction. PLoS Genet 4:e1000316
43. Vega QC, Worby CA, Lechner MS, Dixon JE, Dressler GR (1996) Glial cell line-derived neurotrophic factor activates the receptor tyrosine kinase RET and promotes kidney morphogenesis. Proc Nat Acad Sci USA 93:10657-10661
44. Chia I, Grote D, Marcotte M, Batourina E, Mendelsohn C, Bouchard M (2011) Nephric duct insertion is a crucial step in urinary tract maturation that is regulated by a Gata3-Raldh2-Ret molecular network in mice. Development 138:2089-2097
45. Marose TD, Merkel CE, McMahon AP, Carroll TJ (2008) Beta-catenin is necessary to keep cells of ureteric bud/Wolffian duct epithelium in a precursor state. Dev Biol 314:112-126
46. Batourina E, Choi C, Paragas N, Bello N, Hensle T, Costantini FD, Schuchardt A, Bacallao RL, Mendelsohn CL (2002) Distal ureter morphogenesis depends on epithelial cell remodeling mediated by vitamin A and Ret. Nat Genet 32:109-115
47. Rosselot C, Spraggon L, Chia I, Batourina E, Riccio P, Lu B, Niederreither K, Dolle P, Duester G, Chambon P, Costantini F, Gilbert T, Molotkov A, Mendelsohn C (2010) Non-cell-autonomous retinoid signaling is crucial for renal development. Development 137:283-292
48. Pachnis V, Mankoo B, Costantini F (1993) Expression of the c-ret proto-oncogene during mouse embryogenesis. Development 119:1005-1017
49. Bridgewater D, Cox B, Cain J, Lau A, Athaide V, Gill PS, Kuure S, Sainio K, Rosenblum ND (2008) Canonical WNT/beta-catenin signaling is required for ureteric branching. Dev Biol 317:83-94
50. Miyamoto N, Yoshida M, Kuratani S, Matsuo I, Aizawa S (1997) Defects of urogenital development in mice lacking Emx2. Development 124:1653-1664
51. 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
52. Menshykau D, Iber D (2013) Kidney branching morphogenesis under the control of a ligand-receptor-based Turing mechanism. Phys Biol 10:046003
53. Lu BC, Cebrian C, Chi X, Kuure S, Kuo R, Bates CM, Arber S, Hassell J, MacNeil L, Hoshi M, Jain S, Asai N, Takahashi M, Schmidt-Ott KM, Barasch J, D'Agati V, Costantini F (2009) Etv4 and Etv5 are required downstream of GDNF and Ret for kidney branching morphogenesis. Nat Genet 41:1295-1302
54. Basson MA, Akbulut S, Watson-Johnson J, Simon R, Carroll TJ, Shakya R, Gross I, Martin GR, Lufkin T, McMahon AP, Wilson PD, Costantini FD, Mason IJ, Licht JD (2005) Sprouty1 is a critical regulator of GDNF/RET-mediated kidney induction. Dev Cell 8:229-239
55. Tufro A, Teichman J, Woda C, Villegas G (2008) Semaphorin3a inhibits ureteric bud branching morphogenesis. Mech Dev 125:558-568
56. Ueland J, Yuan A, Marlier A, Gallagher AR, Karihaloo A (2009) A novel role for the chemokine receptor Cxcr4 in kidney morphogenesis: an in vitro study. Dev Dyn 238:1083-1091
57. Cacalano G, Farinas I, Wang LC, Hagler K, Forgie A, Moore M, Armanini M, Phillips H, Ryan AM, Reichardt LF, Hynes M, Davies A, Rosenthal A (1998) GFRalpha1 is an essential receptor component for GDNF in the developing nervous system and kidney. Neuron 21:53-62
58. Enomoto H, Araki T, Jackman A, Heuckeroth RO, Snider WD, Johnson EM Jr, Milbrandt J (1998) GFR alpha1-deficient mice have deficits in the enteric nervous system and kidneys. Neuron 21:317-324
59. 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 382:76-79
60. 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 382:73-76
61. Sainio K, Suvanto P, Davies J, Wartiovaara J, Wartiovaara K, Saarma M, Arumae U, Meng X, Lindahl M, Pachnis V, Sariola H (1997) Glial-cell-line-derived neurotrophic factor is required for bud initiation from ureteric epithelium. Development 124:4077-4087
62. 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 382:70-73
63. van Amerongen R, Nusse R (2009) Towards an integrated view of Wnt signaling in development. Development 136:3205-3214
64. Ye X, Wang Y, Rattner A, Nathans J (2011) Genetic mosaic analysis reveals a major role for frizzled 4 and frizzled 8 in controlling ureteric growth in the developing kidney. Development 138:1161-1172
65. 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
66. 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
67. Michos O, Goncalves A, Lopez-Rios J, Tiecke E, Naillat F, Beier K, Galli A, Vainio S, Zeller R (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
68. Michos O, Panman L, Vintersten K, Beier K, Zeller R, Zuniga A (2004) Gremlin-mediated BMP antagonism induces the epithelial-mesenchymal feedback signaling controlling metanephric kidney and limb organogenesis. Development 131:3401-3410
69. Goncalves A, Zeller R (2011) Genetic analysis reveals an unexpected role of BMP7 in initiation of ureteric bud outgrowth in mouse embryos. PloS One 6:e19370
70. Choi Y, Tee JB, Gallegos TF, Shah MM, Oishi H, Sakurai H, Kitamura S, Wu W, Bush KT, Nigam SK (2009) Neuropeptide Y functions as a facilitator of GDNF-induced budding of the Wolffian duct. Development 136:4213-4224
71. Wellik DM, Hawkes PJ, Capecchi MR (2002) Hox11 paralogous genes are essential for metanephric kidney induction. Genes Dev 16:1423-1432
72. Sajithlal G, Zou D, Silvius D, Xu PX (2005) Eya 1 acts as a critical regulator for specifying the metanephric mesenchyme. Dev Biol 284:323-336
73. Gong KQ, Yallowitz AR, Sun H, Dressler GR, Wellik DM (2007) A Hox-Eya-Pax complex regulates early kidney developmental gene expression. Mol Cell Biol 27:7661-7668
74. Xu PX, Zheng W, Huang L, Maire P, Laclef C, Silvius D (2003) Six1 is required for the early organogenesis of mammalian kidney. Development 130:3085-3094
75. Kobayashi H, Kawakami K, Asashima M, Nishinakamura R (2007) Six1 and Six4 are essential for Gdnf expression in the metanephric mesenchyme and ureteric bud formation, while Six1 deficiency alone causes mesonephric-tubule defects. Mech Dev 124:290-303
76. Esquela AF, Lee SJ (2003) Regulation of metanephric kidney development by growth/differentiation factor 11. Dev Biol 257:356-370
77. Kume T, Deng K, Hogan BL (2000) Murine forkhead/winged helix genes Foxc1 (Mf1) and Foxc2 (Mfh1) are required for the early organogenesis of the kidney and urinary tract. Development 127:1387-1395
78. 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
79. Michos O, Cebrian C, Hyink D, Grieshammer U, Williams L, D'Agati V, Licht JD, Martin GR, Costantini F (2010) Kidney development in the absence of Gdnf and Spry1 requires Fgf10. PLoS Genet 6:e1000809
80. Barak H, Huh SH, Chen S, Jeanpierre C, Martinovic J, Parisot M, Bole-Feysot C, Nitschke P, Salomon R, Antignac C, Ornitz DM, Kopan R (2012) FGF9 and FGF20 maintain the stemness of nephron progenitors in mice and man. Dev Cell 22:1191-1207
81. Qiao J, Uzzo R, Obara-Ishihara T, Degenstein L, Fuchs E, Herzlinger D (1999) FGF-7 modulates ureteric bud growth and nephron number in the developing kidney. Development 126:547-554
82. Hains D, Sims-Lucas S, Kish K, Saha M, McHugh K, Bates CM (2008) Role of fibroblast growth factor receptor 2 in kidney mesenchyme. Pediatr Res 64:592-598
83. Hains DS, Sims-Lucas S, Carpenter A, Saha M, Murawski I, Kish K, Gupta I, McHugh K, Bates CM (2010) High incidence of vesicoureteral reflux in mice with Fgfr2 deletion in kidney mesenchyma. J Urol 183:2077-2084
84. Zhao H, Kegg H, Grady S, Truong HT, Robinson ML, Baum M, Bates CM (2004) Role of fibroblast growth factor receptors 1 and 2 in the ureteric bud. Dev Biol 276:403-415
85. Gerber SD, Steinberg F, Beyeler M, Villiger PM, Trueb B (2009) The murine Fgfrl1 receptor is essential for the development of the metanephric kidney. Dev Biol 335:106-119
86. Gerber SD, Amann R, Wyder S, Trueb B (2012) Comparison of the gene expression profiles from normal and Fgfrl1 deficient mouse kidneys reveals downstream targets of Fgfrl1 signaling. PloS One 7:e33457