Integration of cistromic and transcriptomic analyses identifies Nphs2, Mafb, and Magi2 as Wilms' tumor 1 target genes in podocyte differentiation and maintenance

Journal of the American Society of Nephrology

Volumn 26, Issue 9, 2015, Pages 2118-2128

  Dong, Lihua ^a   Pietsch, Stefan ^a   Tan, Zenglai ^a   Perner, Birgit ^a   Sierig, Ralph ^a   Kruspe, Dagmar ^a   Groth, Marco ^a   Witzgall, Ralph ^b   Gröne, Hermann Josef ^c   Platzer, Matthias ^a   Englert, Christoph ^a,d  

^a FRITZ LIPMANN INSTITUTE   (Germany)

^b UNIVERSITY OF REGENSBURG   (Germany)

^c GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^d FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CRE RECOMBINASE; GUANYLATE KINASE; MEMBRANE ASSOCIATED GUANYLATE KINASE INVERTED 2; PODOCIN; TRANSCRIPTION FACTOR MAFB; UNCLASSIFIED DRUG; WT1 PROTEIN; ACVRINP1 PROTEIN, MOUSE; MAFB PROTEIN, MOUSE; MAFB PROTEIN, ZEBRAFISH; MAGI2 PROTEIN, ZEBRAFISH; MEMBRANE PROTEIN; NERVE PROTEIN; REPRESSOR PROTEIN; SIGNAL PEPTIDE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; WT1 PROTEIN, MOUSE; WT1A PROTEIN, ZEBRAFISH; ZEBRAFISH PROTEIN;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANURIA; ARTICLE; CELL DIFFERENTIATION; CELL MATURATION; CHROMATIN IMMUNOPRECIPITATION; CISTRON; CONTROLLED STUDY; DNA BINDING; DNA MICROARRAY; EMBRYO; EMBRYO DEVELOPMENT; FOCAL ADHESION; GENE DELETION; GENE TARGETING; GENETIC CONSERVATION; GLOMERULUS; HIGH THROUGHPUT SEQUENCING; HOMEOSTASIS; KIDNEY HEMORRHAGE; LYSOSOME; MOUSE; NERVE FIBER; NEWBORN; NONHUMAN; PODOCYTE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; TRANSCRIPTION INITIATION SITE; TRANSCRIPTOMICS; ZEBRA FISH; ANIMAL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; KNOCKOUT MOUSE; PHYSIOLOGY; TUMOR SUPPRESSOR GENE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CELL DIFFERENTIATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENES, WILMS TUMOR; GUANYLATE KINASE; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MAFB TRANSCRIPTION FACTOR; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PODOCYTES; REPRESSOR PROTEINS; WT1 PROTEINS; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84940761009     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2014080819     Document Type: Article

References (59)

1. Pavenstdt H, Kriz W, Kretzler M: Cell biology of the glomerular podocyte. Physiol Rev 83: 253-307, 2003
2. Dressler GR: The cellular basis of kidney development. Annu Rev Cell Dev Biol 22: 509-529, 2006
3. Greka A,Mundel P:Cell biology and pathology of podocytes. Annu Rev Physiol 74: 299-323, 2012
4. Kestil M, Lenkkeri U,MnnikköM, Lamerdin J,McCready P, Putaala H, Ruotsalainen V,Morita T, NissinenM, Herva R, Kashtan CE, Peltonen L, Holmberg C, Olsen A, Tryggvason K: Positionally cloned gene for a novel glomerular protein-nephrin-is mutated in congenital nephrotic syndrome. Mol Cell 1: 575-582, 1998
5. Boute N, Gribouval O, Roselli S, Benessy F, Lee H, Fuchshuber A, Dahan K, Gubler MC, Niaudet P, Antignac C: NPHS2, encoding the glomerular protein podocin, is mutated in autosomal recessive steroidresistant nephrotic syndrome. Nat Genet 24: 349-354, 2000
6. Hinkes B, Wiggins RC,Gbadegesin R, VlangosCN, SeelowD,Nürnberg G, Garg P, Verma R, Chaib H, Hoskins BE, Ashraf S, Becker C, Hennies HC, Goyal M, Wharram BL, Schachter AD, Mudumana S, Drummond I, Kerjaschki D,Waldherr R, Dietrich A, Ozaltin F, Bakkaloglu A, Cleper R, Basel-Vanagaite L, Pohl M, Griebel M, Tsygin AN, Soylu A, Müller D, Sorli CS, Bunney TD, Katan M, Liu J, Attanasio M, O'toole JF, Hasselbacher K, Mucha B, Otto EA, Airik R, Kispert A, Kelley GG, Smrcka AV, Gudermann T, Holzman LB, Nürnberg P, Hildebrandt F: Positional cloning uncovers mutations in PLCE1 responsible for a nephrotic syndrome variant that may be reversible. Nat Genet 38: 1397-1405, 2006
7. Call KM, Glaser T, Ito CY, Buckler AJ, Pelletier J, Haber DA, Rose EA, Kral A, Yeger H, Lewis WH, Jones C, Housman DE: Isolation and characterization of a zinc finger polypeptide gene at the human chromosome 11 Wilms' tumor locus. Cell 60: 509-520, 1990
8. Gessler M, Poustka A, Cavenee W, Neve RL, Orkin SH, Bruns GA: Homozygous deletion inWilms tumours of a zinc-finger gene identified by chromosome jumping. Nature 343: 774-778, 1990
9. Haber DA, Buckler AJ, Glaser T, Call KM, Pelletier J, Sohn RL, Douglass EC, Housman DE: An internal deletion within an 11p13 zinc finger gene contributes to the development of Wilms' tumor. Cell 61: 1257-1269, 1990
10. Rose EA, Glaser T, Jones C, Smith CL, Lewis WH, Call KM, Minden M, Champagne E, Bonetta L, Yeger H, Housman DE: Complete physical map of the WAGR region of 11p13 localizes a candidate Wilms' tumor gene. Cell 60: 495-508, 1990
11. Huff V: Wilms tumor genetics. Am J Med Genet 79: 260-267, 1998
12. Narahara K, Kikkawa K, Kimira S, Kimoto H, Ogata M, Kasai R, Hamawaki M, Matsuoka K: Regional mapping of catalase and Wilms tumor-aniridia, genitourinary abnormalities, and mental retardation triad loci to the chromosome segment 11p1305-p1306. Hum Genet 66: 181-185, 1984
13. Pelletier J, BrueningW, Kashtan CE,Mauer SM,Manivel JC, Striegel JE, Houghton DC, Junien C, Habib R, Fouser L, Fine RN, Silverman BL, Harber DA, Housman D: Germline mutations in the Wilms' tumor suppressor gene are associated with abnormal urogenital development in Denys-Drash syndrome. Cell 67: 437-447, 1991
14. Barbaux S, Niaudet P, Gubler MC, Grünfeld JP, Jaubert F, Kuttenn F, Fékété CN, Souleyreau-Therville N, Thibaud E, Fellous M, McElreavey K: Donor splice-site mutations in WT1 are responsible for Frasier syndrome. Nat Genet 17: 467-470, 1997
15. Mundlos S, Pelletier J, Darveau A, Bachmann M, Winterpacht A, Zabel B: Nuclear localization of the protein encoded by the Wilms' tumor gene WT1 in embryonic and adult tissues. Development 119: 1329-1341, 1993
16. Kreidberg JA, Sariola H, Loring JM, Maeda M, Pelletier J, Housman D, Jaenisch R: WT-1 is required for early kidney development. Cell 74: 679-691, 1993
17. Ozdemir DD, Hohenstein P: WT1 in the kidney-a tale in mouse models. Pediatr Nephrol 29: 687-693, 2014
18. Bickmore WA, Oghene K, Little MH, Seawright A, van Heyningen V, Hastie ND: Modulation of DNA binding specificity by alternative splicing of theWilms tumor wt1 gene transcript. Science 257: 235-237, 1992
19. Caricasole A, Duarte A, Larsson SH, Hastie ND, Little M, Holmes G, Todorov I, Ward A: RNA binding by the Wilms tumor suppressor zinc finger proteins. Proc Natl Acad Sci U S A 93: 7562-7566, 1996
20. Gebeshuber CA, Kornauth C, Dong L, Sierig R, Seibler J, Reiss M, Tauber S, Bilban M, Wang S, Kain R, Böhmig GA, Moeller MJ, Gröne HJ, Englert C, Martinez J, Kerjaschki D: Focal segmental glomerulosclerosis is induced by microRNA-193a and its downregulation ofWT1. Nat Med 19: 481-487, 2013
21. Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, NusbaumC,Myers RM, BrownM, LiW, Liu XS:Model-based analysis of ChIP-Seq (MACS). Genome Biol 9: R137, 2008
22. Machanick P, Bailey TL: MEME-ChIP: Motif analysis of large DNA datasets. Bioinformatics 27: 1696-1697, 2011
23. Saito R, Smoot ME, Ono K, Ruscheinski J, Wang PL, Lotia S, Pico AR, Bader GD, Ideker T: A travel guide to Cytoscape plugins. NatMethods 9: 1069-1076, 2012
24. Huang W, Sherman BT, Lempicki RA: Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44-57, 2009
25. Gupta S, Stamatoyannopoulos JA, Bailey TL, Noble WS: Quantifying similarity between motifs. Genome Biol 8: R24, 2007
26. Boerries M, Grahammer F, Eiselein S, Buck M, Meyer C, Goedel M, Bechtel W, Zschiedrich S, Pfeifer D, Lalo D, Arrondel C, Gonalves S, Krüger M, Harvey SJ, Busch H, Dengjel J, Huber TB: Molecular fingerprinting of the podocyte reveals novel gene and protein regulatory networks. Kidney Int 83: 1052-1064, 2013
27. WagnerN,Wagner KD, Xing Y, Scholz H, Schedl A: Themajor podocyte protein nephrin is transcriptionally activated by the Wilms' tumor suppressor WT1. J Am Soc Nephrol 15: 3044-3051, 2004
28. GuoG,MorrisonDJ, Licht JD,Quaggin SE:WT1 activates a glomerularspecific enhancer identified from the human nephrin gene. J Am Soc Nephrol 15: 2851-2856, 2004
29. Schumacher VA, Schlötzer-Schrehardt U, Karumanchi SA, Shi X, Zaia J, Jeruschke S, Zhang D, Pavenstdt H, Drenckhan A, Amann K, Ng C, Hartwig S, Ng KH, Ho J, Kreidberg JA, TaglientiM, Royer-Pokora B, Ai X: WT1-dependent sulfatase expression maintains the normal glomerular filtration barrier. J Am Soc Nephrol 22: 1286-1296, 2011
30. Ratelade J, Arrondel C, Hamard G, Garbay S, Harvey S, Biebuyck N, Schulz H, Hastie N, Pontoglio M, Gubler MC, Antignac C, Heidet L: A murine model of Denys-Drash syndrome reveals novel transcriptional targets of WT1 in podocytes. Hum Mol Genet 19: 1-15, 2010
31. Davies JA, LittleMH,AronowB,ArmstrongJ, Brennan J, Lloyd-MacGilp S, ArmitC,Harding S, Piu X, Roochun Y, Haggarty B, Houghton D, Davidson D, Baldock R: Access and use of the GUDMAP database of genitourinary development. Methods Mol Biol 886: 185-201, 2012
32. Sadl V, Jin F, Yu J, Cui S, Holmyard D,Quaggin S, Barsh G, Cordes S: The mouse Kreisler (Krml1/MafB) segmentation gene is required for differentiation of glomerular visceral epithelial cells. Dev Biol 249: 16-29, 2002
33. Moriguchi T, HamadaM,Morito N, Terunuma T, Hasegawa K, Zhang C, Yokomizo T, Esaki R, Kuroda E, Yoh K, Kudo T, Nagata M, Greaves DR, Engel JD, Yamamoto M, Takahashi S: MafB is essential for renal development and F4/80 expression in macrophages. Mol Cell Biol 26: 5715-5727, 2006
34. Lehtonen S, Ryan JJ, Kudlicka K, Iino N, Zhou H, Farquhar MG: Cell junction-associated proteins IQGAP1, MAGI-2, CASK, spectrins, and alpha-actinin are components of the nephrin multiprotein complex. Proc Natl Acad Sci U S A 102: 9814-9819, 2005
35. Ihara K, Asanuma K, Fukuda T, Ohwada S, Yoshida M, Nishimori K: MAGI-2 is critical for the formation and maintenance of the glomerular filtration barrier in mouse kidney. Am J Pathol 184: 2699-2708, 2014
36. Kroeger PT Jr.,Wingert RA: Using zebrafish to study podocyte genesis during kidney development and regeneration. Genesis 52: 771-792, 2014
37. Kramer-Zucker AG, Wiessner S, Jensen AM, Drummond IA: Organization of the pronephric filtration apparatus in zebrafish requires Nephrin, Podocin and the FERMdomain proteinMosaic eyes. Dev Biol 285: 316-329, 2005
38. O'Brien LL, Grimaldi M, Kostun Z, Wingert RA, Selleck R, Davidson AJ: WT1a, Foxc1a, andtheNotchmediatorRbpj physically interact and regulate the formation of podocytes in zebrafish. Dev Biol 358: 318-330, 2011
39. Perner B, Englert C, Bollig F: The Wilms tumor genes wt1a and wt1b control different steps during formation of the zebrafish pronephros. Dev Biol 309: 87-96, 2007
40. Mondini A, Messa P, RastaldiMP: The sclerosing glomerulus inmice and man: Novel insights. Curr Opin Nephrol Hypertens 23: 239-244, 2014
41. Chau YY, Brownstein D, Mjoseng H, Lee WC, Buza-Vidas N, Nerlov C, Jacobsen SE, Perry P, Berry R, Thornburn A, Sexton D, Morton N, Hohenstein P, Freyer E, Samuel K, van't Hof R, Hastie N: Acutemultiple organ failure in adult mice deleted for the developmental regulator WT1. PLoS Genet 7: e1002404, 2011
42. Motamedi FJ, BadroDA, Clarkson M, LeccaMR, Bradford ST, Buske FA, Saar K, Hübner N, Brndli AW, Schedl A: WT1 controls antagonistic FGF and BMP-pSMAD pathways in early renal progenitors. Nat Commun 5: 4444, 2014
43. Hartwig S, Ho J, Pandey P, Macisaac K, TaglientiM, XiangM, Alterovitz G, Ramoni M, Fraenkel E, Kreidberg JA: Genomic characterization of Wilms' tumor suppressor 1 targets in nephron progenitor cells during kidney development. Development 137: 1189-1203, 2010
44. Moffett P, Bruening W, Nakagama H, Bardeesy N, Housman D, Housman DE, Pelletier J: Antagonism of WT1 activity by protein selfassociation. Proc Natl Acad Sci U S A 92: 11105-11109, 1995
45. HolmesG, Boterashvili S, EnglishM,Wainwright B, Licht J, LittleM: Two N-terminal self-association domains are required for the dominant negative transcriptional activity of WT1 Denys-Drash mutant proteins. Biochem Biophys Res Commun 233: 723-728, 1997
46. Essafi A, Webb A, Berry RL, Slight J, Burn SF, Spraggon L, Velecela V, Martinez-Estrada OM, Wiltshire JH, Roberts SG, Brownstein D, Davies JA, Hastie ND, Hohenstein P: A wt1-controlled chromatin switching mechanism underpins tissue-specific wnt4 activation and repression. Dev Cell 21: 559-574, 2011
47. Brinkkoetter PT, Ising C, Benzing T: The role of the podocyte in albumin filtration. Nat Rev Nephrol 9: 328-336, 2013
48. Schwarz K, Simons M, Reiser J, Saleem MA, Faul C, Kriz W, Shaw AS, Holzman LB, Mundel P: Podocin, a raft-associated component of the glomerular slit diaphragm, interacts with CD2AP and nephrin. J Clin Invest 108: 1621-1629, 2001
49. Sellin L, Huber TB, Gerke P, Quack I, Pavenstadt H, Walz G: NEPH1 defines a novel family of podocin interacting proteins. FASEB J 17: 115-117, 2003
50. Zankl A, Duncan EL, Leo PJ, Clark GR, Glazov EA, Addor MC, Herlin T, Kim CA, Leheup BP, McGill J, McTaggart S, Mittas S, Mitchell AL, Mortier GR, Robertson SP, Schroeder M, Terhal P, Brown MA: Multicentric carpotarsal osteolysis is caused by mutations clustering in the amino-terminal transcriptional activation domain of MAFB. Am J Hum Genet 90: 494-501, 2012
51. Ihara KI, Nishimura T, Fukuda T, Ookura T, Nishimori K: Generation of Venus reporter knock-in mice revealed MAGI-2 expression patterns in adult mice. Gene Expr Patterns 12: 95-101, 2012
52. Moeller MJ, Sanden SK, Soofi A, Wiggins RC, Holzman LB: Podocytespecific expression of cre recombinase in transgenic mice. Genesis 35: 39-42, 2003
53. Akis N, Madaio MP: Isolation, culture, and characterization of endothelial cells from mouse glomeruli. Kidney Int 65: 2223-2227, 2004
54. Heliot C, Cereghini S: Analysis of in vivo transcription factor recruitment by chromatin immunoprecipitation of mouse embryonic kidney. Methods Mol Biol 886: 275-291, 2012
55. Feng J, Liu T, Qin B, Zhang Y, Liu XS: Identifying ChIP-seq enrichment using MACS. Nat Protoc 7: 1728-1740, 2012
56. TakemotoM, Asker N, Gerhardt H, Lundkvist A, Johansson BR, Saito Y, Betsholtz C: A new method for large scale isolation of kidney glomeruli from mice. Am J Pathol 161: 799-805, 2002
57. Sanges R, Cordero F, Calogero RA: oneChannelGUI: A graphical interface to Bioconductor tools, designed for life scientists who are not familiar with R language. Bioinformatics 23: 3406-3408, 2007
58. Westerfield M: The Zebrafish Book. A Guide for the Laboratory Use of Zebrafish (Danio rerio), 3rd Edition Eugene, OR, University of Oregon Press,385 (Book) 1995.
59. Kimmel CB, BallardWW, Kimmel SR, Ullmann B, Schilling TF: Stages of embryonic development of the zebrafish. Dev Dyn 203: 253-310, 1995