Scaffolding proteins DLG1 and CASK cooperate to maintain the nephron progenitor population during kidney development

Journal of the American Society of Nephrology

Volumn 24, Issue 7, 2013, Pages 1127-1138

  Ahn, Sun Young ^a   Kim, Yeawon ^a   Tae Kim, Sung ^a   Swat, Wojciech ^a   Miner, Jeffrey H ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CALMODULIN DEPENDENT SERINE PROTEIN KINASE; DISCS LARGE HOMOLOG 1 PROTEIN; FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 8; PROTEIN SIX2; RAS PROTEIN; SCAFFOLD PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL POLARITY; CELL POPULATION; CELL PROLIFERATION; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DISEASE SEVERITY; GENOTYPE; HYPOPLASIA; IN SITU HYBRIDIZATION; KIDNEY CELL; KIDNEY DEVELOPMENT; KIDNEY DYSPLASIA; KIDNEY FAILURE; KIDNEY INTERSTITIUM; MOUSE; NEPHRON; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; STEM CELL; SYNAPTIC TRANSMISSION;

EID: 84879948330     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2012111074     Document Type: Article

References (61)

1. Saxen L, Sariola H: Early organogenesis of the kidney. Pediatr Nephrol 1: 385-392, 1987
2. Dressler GR: The cellular basis of kidney development. Annu Rev Cell Dev Biol 22: 509-529, 2006
3. Vainio S, Lin Y: Coordinating early kidney development: Lessons from gene targeting. Nat Rev Genet 3: 533-543, 2002
4. Self M, Lagutin OV, Bowling B, Hendrix J, Cai Y, Dressler GR, Oliver G: Six2 is required for suppression of nephrogenesis and progenitor renewal in the developing kidney. EMBO J 25: 5214-5228, 2006
5. Blank U, Brown A, Adams DC, KarolakMJ, Oxburgh L: BMP7 promotes proliferation of nephron progenitor cells via a JNK-dependent mechanism. Development 136: 3557-3566, 2009
6. Dudley AT, Lyons KM, Robertson EJ: A requirement for bone morphogenetic protein-7 during development of the mammalian kidney and eye. Genes Dev 9: 2795-2807, 1995
7. Bates CM: Role of fibroblast growth factor receptor signaling in kidney development. Pediatr Nephrol 22: 343-349, 2007
8. Brown AC, Adams D, de Caestecker M, Yang X, Friesel R, Oxburgh L: FGF/EGF signaling regulates the renewal of early nephron progenitors during embryonic development. Development 138: 5099-5112, 2011
9. PoladiaDP, Kish K, Kutay B, HainsD, KeggH, Zhao H, Bates CM: Role of fibroblast growth factor receptors 1 and 2 in the metanephric mesenchyme. Dev Biol 291: 325-339, 2006
10. Boyle SC, Kim M, Valerius MT, McMahon AP, Kopan R: Notch pathway activation can replace the requirement for Wnt4 and Wnt9b in mesenchymal-to-epithelial transition of nephron stem cells. Development 138: 4245-4254, 2011
11. Woods DF, Hough C, Peel D, Callaini G, Bryant PJ: Dlg protein is required for junction structure, cell polarity, and proliferation control in Drosophila epithelia. J Cell Biol 134: 1469-1482, 1996
12. Kim E, ShengM: PDZ domain proteins of synapses. Nat Rev Neurosci 5: 771-781, 2004
13. CaruanaG, Bernstein A: Craniofacial dysmorphogenesis including cleft palate in mice with an insertional mutation in the discs large gene. Mol Cell Biol 21: 1475-1483, 2001
14. Mahoney ZX, Sammut B, Xavier RJ, Cunningham J, Go G, Brim KL, Stappenbeck TS, Miner JH, Swat W: Discs-large homolog 1 regulates smooth muscle orientation in the mouse ureter. Proc Natl Acad Sci U S A 103: 19872-19877, 2006
15. Iizuka-Kogo A, Ishidao T, Akiyama T, Senda T: Abnormal development of urogenital organs in Dlgh1-deficient mice. Development 134: 1799-1807, 2007
16. Naim E, Bernstein A, Bertram JF, Caruana G: Mutagenesis of the epithelial polarity gene, discs large 1, perturbs nephrogenesis in the developing mouse kidney. Kidney Int 68: 955-965, 2005
17. Fanning AS, Anderson JM: Proteinmodules as organizers of membrane structure. Curr Opin Cell Biol 11: 432-439, 1999
18. Caruana G: Genetic studies define MAGUK proteins as regulators of epithelial cell polarity. Int J Dev Biol 46: 511-518, 2002
19. Lee S, Fan S, Makarova O, Straight S, Margolis B: A novel and conserved protein-protein interaction domain of mammalian Lin-2/CASK binds and recruits SAP97 to the lateral surface of epithelia.Mol Cell Biol 22: 1778-1791, 2002
20. HowardMA, EliasGM, Elias LA, Swat W, Nicoll RA: The role of SAP97 in synaptic glutamate receptor dynamics. Proc Natl Acad Sci U S A 107: 3805-3810, 2010
21. Li J, Chen F, Epstein JA: Neural crest expression of Cre recombinase directed by the proximal Pax3 promoter in transgenic mice.Genesis 26: 162-164, 2000
22. Chang CP, McDill BW, Neilson JR, Joist HE, Epstein JA, Crabtree GR, Chen F: Calcineurin is required in urinary tract mesenchyme for the development of the pyeloureteral peristaltic machinery. J Clin Invest 113: 1051-1058, 2004
23. Grieshammer U, Cebrián C, Ilagan R, Meyers E, Herzlinger D, Martin GR: FGF8 is required for cell survival at distinct stages of nephrogenesis and for regulation of gene expression in nascent nephrons. Development 132: 3847-3857, 2005
24. Costantini F, Kopan R: Patterning a complex organ: Branching morphogenesis and nephron segmentation in kidney development. Dev Cell 18: 698-712, 2010
25. Boyle S, Shioda T, Perantoni AO, de Caestecker M: Cited1 and Cited2 are differentially expressed in the developing kidney but are not required for nephrogenesis. Dev Dyn 236: 2321-2330, 2007
26. Fujii T, Pichel JG, Taira M, Toyama R, Dawid IB,Westphal H: Expression patterns of the murine LIM class homeobox gene lim1 in the developing brain and excretory system. Dev Dyn 199: 73-83, 1994
27. Karavanov AA, Karavanova I, Perantoni A, Dawid IB: Expression pattern of the rat Lim-1 homeobox gene suggests a dual role during kidney development. Int J Dev Biol 42: 61-66, 1998
28. Lan Y, Kingsley PD, Cho ES, Jiang R: Osr2, a new mouse gene related to Drosophila odd-skipped, exhibits dynamic expression patterns during craniofacial, limb, andkidney development. MechDev107:175-179, 2001
29. Dorey K,Amaya E: FGF signalling: Diverse roles during early vertebrate embryogenesis. Development 137: 3731-3742, 2010
30. Di Giovanni V, Alday A, Chi L, Mishina Y, Rosenblum ND: Alk3 controls nephron number and androgen production via lineage-specific effects in intermediate mesoderm. Development 138: 2717-2727, 2011
31. Hoshi M, Batourina E, Mendelsohn C, Jain S: Novel mechanisms of early upper and lower urinary tract patterning regulated by RetY1015 docking tyrosine in mice. Development 139: 2405-2415, 2012
32. Oxburgh L, Brown AC, Fetting J, Hill B: BMP signaling in the nephron progenitor niche. Pediatr Nephrol 26: 1491-1497, 2011
33. Costantini F, Shakya R: GDNF/Ret signaling and the development of the kidney. Bioessays 28: 117-127, 2006
34. Michos O, Cebrian C, Hyink D, Grieshammer U, Williams L, D'Agati V, Licht JD, Martin GR, Costantini F: Kidney development in the absence of Gdnf and Spry1 requires Fgf10. PLoS Genet 6: e1000809, 2010
35. Dudley AT, Godin RE, Robertson EJ: Interaction between FGF andBMP signaling pathways regulates development of metanephric mesenchyme. Genes Dev 13: 1601-1613, 1999
36. Liu C, Goswami M, Talley J, Chesser-Martinez PL, Lou CH, Sater AK: TAK1 promotes BMP4/Smad1 signaling via inhibition of erk MAPK: A new link in the FGF/BMP regulatory network. Differentiation 83: 210-219, 2012
37. Park JS, Ma W, O'Brien LL, Chung E, Guo JJ, Cheng JG, Valerius MT, McMahon JA, Wong WH, McMahon AP: Six2 and Wnt regulate selfrenewal and commitment of nephron progenitors through shared gene regulatory networks. Dev Cell 23: 637-651, 2012
38. Roberts S, Delury C, Marsh E: The PDZ protein discs-large (DLG): the 'Jekyll and Hyde' of the epithelial polarity proteins. FEBS J 279: 3549-3558, 2012
39. Frese KK, Latorre IJ, Chung SH, Caruana G, Bernstein A, Jones SN, Donehower LA, Justice MJ, Garner CC, Javier RT: Oncogenic function for the Dlg1 mammalian homolog of the Drosophila discs-large tumor suppressor. EMBO J 25: 1406-1417, 2006
40. Najm J, Horn D, Wimplinger I, Golden JA, Chizhikov VV, Sudi J, Christian SL, Ullmann R, Kuechler A, Haas CA, Flubacher A, Charnas LR, Uyanik G, Frank U, Klopocki E, Dobyns WB, Kutsche K: Mutations of CASK cause an X-linked brain malformation phenotype with microcephaly and hypoplasia of the brainstem and cerebellum. Nat Genet 40: 1065-1067, 2008
41. Barasch J, Qiao J, McWilliams G, Chen D, Oliver JA, Herzlinger D: Ureteric bud cells secrete multiple factors, including bFGF, which rescue renal progenitors from apoptosis. Am J Physiol 273: F757-F767, 1997
42. PerantoniAO,Dove LF, Karavanova I: Basic fibroblast growth factor can mediate the early inductive events in renal development. Proc Natl Acad Sci U S A 92: 4696-4700, 1995
43. 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: FGF9 and FGF20 maintain the stemness of nephron progenitors in mice and man. Dev Cell 22: 1191-1207, 2012
44. Maher P: p38 mitogen-Activated protein kinase activation is required for fibroblast growth factor-2-stimulated cell proliferation but not differentiation. J Biol Chem274: 17491-17498, 1999
45. Cohen AR, Woods DF, Marfatia SM, Walther Z, Chishti AH, Anderson JM: Human CASK/LIN-2 binds syndecan-2 and protein 4.1 and localizes to the basolateral membrane of epithelial cells. J Cell Biol 142: 129-138, 1998
46. Gaudet S, Langlois MJ, Lue RA, Rivard N, Viel A: The MEK2-binding tumor suppressor hDlg is recruited by E-cadherin to the midbody ring. BMC Cell Biol 12: 55, 2011
47. Hsueh YP, Yang FC, Kharazia V, Naisbitt S, Cohen AR, Weinberg RJ, Sheng M: Direct interaction of CASK/LIN-2 and syndecan heparan sulfate proteoglycan and their overlapping distribution in neuronal synapses. J Cell Biol 142: 139-151, 1998
48. Maïga O, Philippe M, Kotelevets L, Chastre E, Benadda S, Pidard D, Vranckx R, Walch L: Identification of mitogen-Activated protein/extracellular signal-responsive kinase kinase 2 as a novel partner of the scaffolding protein human homolog of disc-large. FEBS J 278: 2655-2665, 2011
49. Masola V, Gambaro G, Tibaldi E, Brunati AM, Gastaldello A, D'Angelo A, Onisto M, Lupo A: Heparanase and syndecan-1 interplay orchestrates fibroblast growth factor-2-induced epithelial-mesenchymal transition in renal tubular cells. J Biol Chem287: 1478-1488, 2012
50. Carey DJ: Syndecans: multifunctional cell-surface co-receptors. Biochem J 327: 1-16, 1997
51. Cotter L, Ozcelik M, Jacob C, Pereira JA, Locher V, Baumann R, Relvas JB, Suter U, Tricaud N: Dlg1-PTEN interaction regulates myelin thickness to prevent damaging peripheral nerve overmyelination. Science 328: 1415-1418, 2010
52. Etienne-Manneville S, Manneville JB, Nicholls S, Ferenczi MA, Hall A: Cdc42 and Par6-PKCzeta regulate the spatially localized association of Dlg1 and APC to control cell polarization. J CellBiol 170: 895-901, 2005
53. Moog U, Kutsche K, Kortum F, Chilian B, Bierhals T, Apeshiotis N, Balg S, Chassaing N, Coubes C, Das S, Engels H, Van Esch H, Grasshoff U, Heise M, Isidor B, Jarvis J, Koehler U, Martin T, Oehl-Jaschkowitz B, Ortibus E, Pilz DT, Prabhakar P, Rappold G, Rau I, Rettenberger G, Schluter G, Scott RH, Shoukier M, Wohlleber E, Zirn B, Dobyns WB, Uyanik G: Phenotypic spectrum associated with CASK loss-of-function mutations. J Med Genet 48: 741-751, 2011
54. Stephenson LM, Sammut B, Graham DB, Chan-Wang J, Brim KL, Huett AS, Miletic AV, Kloeppel T, Landry A, Xavier R, Swat W: DLGH1 is a negative regulator of T-lymphocyte proliferation. Mol Cell Biol 27: 7574-7581, 2007
55. Atasoy D, Schoch S, Ho A, Nadasy KA, Liu X, Zhang W, Mukherjee K, Nosyreva ED, Fernandez-Chacon R, Missler M, Kavalali ET, Sudhof TC: Deletion of CASK in mice is lethal and impairs synaptic function. Proc Natl Acad Sci U S A 104: 2525-2530, 2007
56. Jarad G, Miner JH: The Pax3-Cre transgene exhibits a rostrocaudal gradient of expression in the skeletal muscle lineage. Genesis 47: 1-6, 2009
57. Zhao H, Kegg H, Grady S, Truong HT, Robinson ML, Baum M, Bates CM: Role of fibroblast growth factor receptors 1 and 2 in the ureteric bud. Dev Biol 276: 403-415, 2004
58. Kobayashi A, Valerius MT, Mugford JW, Carroll TJ, Self M, Oliver G, McMahon AP: Six2 defines and regulates a multipotent self-renewing nephron progenitor population throughout mammalian kidney development. Cell Stem Cell 3: 169-181, 2008
59. Hayashi S, Lewis P, Pevny L, McMahon AP: Efficient genemodulation in mouse epiblast using a Sox2Cre transgenic mouse strain. Mech Dev 119[Suppl 1]: S97-S101, 2002
60. Jarad G, Cunningham J, Shaw AS, Miner JH: Proteinuria precedes podocyte abnormalities inLamb2-/-mice, implicating the glomerular basement membrane as an albumin barrier. J Clin Invest 116: 2272-2279, 2006
61. Rogers SA, Ryan G, HammermanMR: Insulin-like growth factors I and II are produced in the metanephros and are required for growth and development in vitro. J Cell Biol 113: 1447-1453, 1991