Kif3a Controls Murine Nephron Number Via GLI3 Repressor, Cell Survival, and Gene Expression in a Lineage-Specific Manner

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Chi, Lijun ^a   Galtseva, Alevtina ^a   Chen, Lin ^a   Mo, Rong ^a   Hui, Chi chung ^a,b   Rosenblum, Norman D ^a,b,c  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

FIBROBLAST GROWTH FACTOR 8; PROTEIN KIF3A; PROTEIN RET; REGULATOR PROTEIN; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR GLI3; UNCLASSIFIED DRUG; WNT11 PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRANCHING MORPHOGENESIS; CELL LINEAGE; CELL SURVIVAL; CONTROLLED STUDY; EUKARYOTIC FLAGELLUM; FEMALE; GENE EXPRESSION; KIDNEY CELL; MESENCHYMAL STEM CELL; MOUSE; NEPHRON; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION;

ANIMALS; CELL LINEAGE; CELL SURVIVAL; CILIA; FIBROBLAST GROWTH FACTOR 8; GENE EXPRESSION REGULATION; KINESIN; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MESODERM; MICE; MODELS, BIOLOGICAL; MORPHOGENESIS; NEPHRONS; NERVE TISSUE PROTEINS; SIGNAL TRANSDUCTION; TAMOXIFEN;

MURINAE; MUS;

EID: 84878760611     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0065448     Document Type: Article

References (47)

1. Goetz SC, Anderson KV, (2010) The primary cilium: a signalling centre during vertebrate development. Nat Rev Genet 11: 331-344.
2. Scholey JM, Anderson KV, (2006) Intraflagellar transport and cilium-based signaling. Cell 125: 439-442.
3. Marszalek JR, Ruiz-Lozano P, Roberts E, Chien KR, Goldstein LS, (1999) Situs inversus and embryonic ciliary morphogenesis defects in mouse mutants lacking the KIF3A subunit of kinesin-II. Proc Natl Acad Sci U S A 96: 5043-5048.
4. Huangfu D, Liu A, Rakeman AS, Murcia NS, Niswander L, et al. (2003) Hedgehog signalling in the mouse requires intraflagellar transport proteins. Nature 426: 83-87.
5. Corbit KC, Aanstad P, Singla V, Norman AR, Stainier DY, et al. (2005) Vertebrate Smoothened functions at the primary cilium. Nature 437: 1018-1021.
6. Haycraft CJ, Banizs B, Aydin-Son Y, Zhang Q, Michaud EJ, et al. (2005) Gli2 and gli3 localize to cilia and require the intraflagellar transport protein polaris for processing and function. PLoS Genet 1: e53.
7. Rohatgi R, Milenkovic L, Scott MP, (2007) Patched1 regulates hedgehog signaling at the primary cilium. Science 317: 372-376.
8. Huangfu D, Anderson KV, (2005) Cilia and Hedgehog responsiveness in the mouse. Proc Natl Acad Sci U S A 102: 11325-11330.
9. Simons M, Gloy J, Ganner A, Bullerkotte A, Bashkurov M, et al. (2005) Inversin, the gene product mutated in nephronophthisis type II, functions as a molecular switch between Wnt signaling pathways. Nat Genet 37: 537-543.
10. Lancaster MA, Louie CM, Silhavy JL, Sintasath L, Decambre M, et al. (2009) Impaired Wnt-beta-catenin signaling disrupts adult renal homeostasis and leads to cystic kidney ciliopathy. Nat Med 15: 1046-1054.
11. Neugebauer JM, Amack JD, Peterson AG, Bisgrove BW, Yost HJ, (2009) FGF signalling during embryo development regulates cilia length in diverse epithelia. Nature 458: 651-654.
12. Evans MJ, Fanucchi MV, Van Winkle LS, Baker GL, Murphy AE, et al. (2002) Fibroblast growth factor-2 during postnatal development of the tracheal basement membrane zone. Am J Physiol Lung Cell Mol Physiol 283: L1263-1270.
13. Yoder BK, (2007) Role of primary cilia in the pathogenesis of polycystic kidney disease. J Am Soc Nephrol 18: 1381-1388.
14. Lin F, Hiesberger T, Cordes K, Sinclair AM, Goldstein LS, et al. (2003) Kidney-specific inactivation of the KIF3A subunit of kinesin-II inhibits renal ciliogenesis and produces polycystic kidney disease. Proc Natl Acad Sci U S A 100: 5286-5291.
15. Saxen L (1987) Organogenesis of the kidney. Cambridge: Cambridge University Press.
16. Hu MC, Mo R, Bhella S, Wilson CW, Chuang PT, et al. (2006) GLI3-dependent transcriptional repression of Gli1, Gli2 and kidney patterning genes disrupts renal morphogenesis. Development 133: 569-578.
17. Cain JE, Islam E, Haxho F, Chen L, Bridgewater D, et al. (2009) GLI3 Repressor Controls Nephron Number Via Regulation of Wnt11 and Ret in Ureteric Tip Cells. PLoS ONE 4: e7313.
18. Bridgewater D, Cox B, Cain J, Lau A, Althaide V, et al. (2008) Canonical WNT/beta-catenin signaling is required for ureteric branching. Dev Biol 317: 83-94.
19. Park JS, Valerius MT, McMahon AP, (2007) Wnt/{beta}-catenin signaling regulates nephron induction during mouse kidney development. Development 134: 2533-2539.
20. 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.
21. 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.
22. Grieshammer U, Cebrian C, Ilagan R, Meyers E, Herzlinger D, et al. (2005) FGF8 is required for cell survival at distinct stages of nephrogenesis and for regulation of gene expression in nascent nephrons. Development 132: 3847-3857.
23. 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.
24. Zhao H, Kegg H, Grady S, Truong HT, Robinson ML, et al. (2004) Role of fibroblast growth factor receptors 1 and 2 in the ureteric bud. Dev Biol 276: 403-415.
25. Kobayashi A, Kwan KM, Carroll TJ, McMahon AP, Mendelsohn CL, et al. (2005) Distinct and sequential tissue-specific activities of the LIM-class homeobox gene Lim1 for tubular morphogenesis during kidney development. Development 132: 2809-2823.
26. Lin F, Hiesberger T, Cordes K, Sinclair AM, Goldstein LS, et al. (2003) Kidney-specific inactivation of the KIF3A subunit of kinesin-II inhibits renal ciliogenesis and produces polycystic kidney disease. Proc Natl Acad Sci USA 100: 5286-5291.
27. 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.
28. 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.
29. Bose J, Grotewold L, Ruther U, (2002) Pallister-Hall syndrome phenotype in mice mutant for Gli3. Hum Mol Genet 11: 1129-1135.
30. Soriano P, (1999) Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat Genet 21: 70-71.
31. Di Giovanni V, Alday A, Chi L, Mishina Y, Rosenblum ND, (2011) Alk3 controls nephron number and androgen production via lineage-specific effects in intermediate mesoderm. Development 138: 2717-2727.
32. Rosenbaum JL, Witman GB, (2002) Intraflagellar transport. Nat Rev Mol Cell Biol 3: 813-825.
33. Gerdes JM, Davis EE, Katsanis N, (2009) The vertebrate primary cilium in development, homeostasis, and disease. Cell 137: 32-45.
34. Jonassen JA, San Agustin J, Follit JA, Pazour GJ, (2008) Deletion of IFT20 in the mouse kidney causes misorientation of the mitotic spindle and cystic kidney disease. J Cell Biol 183: 377-384.
35. Pazour GJ, Dickert BL, Vucica Y, Seeley ES, Rosenbaum JL, et al. (2000) Chlamydomonas IFT88 and its mouse homologue, polycystic kidney disease gene tg737, are required for assembly of cilia and flagella. J Cell Biol 151: 709-718.
36. 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.
37. Cain JE, Islam E, Haxho F, Blake J, Rosenblum ND, (2011) GLI3 Repressor controls functional development of the mouse ureter. Journal of Clinical Investigation 121: 1199-1206.
38. Ding Q, Motoyama J, Gasca S, Mo R, Sasaki H, et al. (1998) Diminished Sonic hedgehog signaling and lack of floor plate differentiation in Gli2 mutant mice. Development 125: 2533-2543.
39. Vainio S, Heikkila M, Kispert A, Chin N, McMahon AP, (1999) Female development in mammals is regulated by Wnt-4 signalling. Nature 397: 405-409.
40. Kispert A, Vainio S, Shen L, Rowitch DH, McMahon AP, (1996) Proteoglycans are required for maintenance of Wnt-11 expression in the ureter tips. Development 122: 3627-3637.
41. Sainio K, Suvanto P, Davies J, Wartiovaara J, Wartiovaara K, et al. (1997) Glial-cell-line-derived neurotrophic factor is required for bud initiation from ureteric epithelium. Development 124: 4077-4087.
42. Hatini V, Huh SO, Herzlinger D, Soares VC, Lai E, (1996) Essential role of stromal mesenchyme in kidney morphogenesis revealed by targeted disruption of Winged Helix transcription factor BF-2. Genes Dev 10: 1467-1478.
43. Chi L, Zhang S, Lin Y, Prunskaite-Hyyrylainen R, Vuolteenaho R, et al. (2004) Sprouty proteins regulate ureteric branching by coordinating reciprocal epithelial Wnt11, mesenchymal Gdnf and stromal Fgf7 signalling during kidney development. Development 131: 3345-3356.
44. Rosenquist TA, Martin GR, (1996) Fibroblast growth factor signalling in the hair growth cycle: expression of the fibroblast growth factor receptor and ligand genes in the murine hair follicle. Dev Dyn 205: 379-386.
45. Chi L, Rosenblum N, (2012) Investigating primary cilia in cultured metanephric mesenchymal cells. Methods Mol Biol 886: 157-163.
46. Chi L, Itaranta P, Zhang S, Vainio S, (2006) Sprouty2 is involved in male sex organogenesis by controlling fibroblast growth factor 9-induced mesonephric cell migration to the developing testis. Endocrinology 147: 3777-3788.
47. Hartwig S, Bridgewater D, Di Giovanni V, Cain J, Mishina Y, et al. (2008) BMP receptor ALK3 controls collecting system development. J Am Soc Nephrol 19: 117-124.