Lmx1b and FoxC combinatorially regulate podocin expression in podocytes

Journal of the American Society of Nephrology

Volumn 25, Issue 12, 2014, Pages 2764-2777

  He, Bing ^a   Ebarasi, Lwaki ^a,b   Zhao, Zhe ^c   Guo, Jing ^a   Ojala, Juha R M ^a   Hultenby, Kjell ^a   De Val, Sarah ^c   Betsholtz, Christer ^a,b   Tryggvason, Karl ^a,d  

^a KAROLINSKA INSTITUTE   (Sweden)

^b UPPSALA UNIVERSITY   (Sweden)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

CIS ACTING ELEMENT; CYCLIN C; HOMEODOMAIN PROTEIN; MEIS2 PROTEIN; PODOCIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FOXC; TRANSCRIPTION FACTORS LMX1B; UNCLASSIFIED DRUG; FORKHEAD TRANSCRIPTION FACTOR; FOXC1 PROTEIN, MOUSE; FOXC1A PROTEIN, ZEBRAFISH; LIM HOMEOBOX TRANSCRIPTION FACTOR 1 BETA; LIM HOMEODOMAIN PROTEIN; LMX1B PROTEIN, ZEBRAFISH; MEMBRANE PROTEIN; SIGNAL PEPTIDE; ZEBRAFISH PROTEIN;

ANIMAL CELL; ARTICLE; BINDING SITE; CELL MATURATION; CONTROLLED STUDY; DNA BINDING; EMBRYO; ENHANCER REGION; GENE; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; GENETIC IDENTIFICATION; IN VIVO STUDY; NONHUMAN; PHENOTYPE; PODOCYTE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN INTERACTION; PROTEIN MOTIF; REGULATORY MECHANISM; TRANSCRIPTION REGULATION; TRANSGENICS; ZEBRA FISH; ANIMAL; C57BL MOUSE; CONFOCAL MICROSCOPY; CYTOLOGY; GENETIC TRANSCRIPTION; HEK293 CELL LINE; HUMAN; METABOLISM; MOUSE; MUTAGENESIS; TRANSGENIC ANIMAL;

AMINO ACID MOTIFS; ANIMALS; ANIMALS, GENETICALLY MODIFIED; BINDING SITES; ENHANCER ELEMENTS, GENETIC; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION; HEK293 CELLS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LIM-HOMEODOMAIN PROTEINS; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICROSCOPY, CONFOCAL; MUTAGENESIS; PHENOTYPE; PODOCYTES; PROMOTER REGIONS, GENETIC; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84912062949     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2012080823     Document Type: Article

References (48)

1. Pavensẗdt H, Kriz W, Kretzler M: Cell biology of the glomerular podocyte. Physiol Rev 83: 253-307, 2003
2. Somlo S, Mundel P: Getting a foothold in nephrotic syndrome. Nat Genet 24: 333-335, 2000
3. Tryggvason K, Wartiovaara J: How does the kidney filter plasma? Physiology (Bethesda) 20: 96-101, 2005
4. Tryggvason K, Patrakka J, Wartiovaara J: Hereditary proteinuria syndromes andmechanisms of proteinuria. NEngl J Med 354: 1387-1401, 2006
5. Quaggin SE: Transcriptional regulation of podocyte specification and differentiation. Microsc Res Tech 57: 208-211, 2002
6. Quaggin SE, Kreidberg JA: Development of the renal glomerulus: Good neighbors and good fences. Development 135: 609-620, 2008
7. 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 steroid-resistant nephrotic syndrome. Nat Genet 24: 349-354, 2000
8. Frishberg Y, Rinat C, Megged O, Shapira E, Feinstein S, Raas-Rothschild A: Mutations in NPHS2 encoding podocin are a prevalent cause of steroid-resistant nephrotic syndrome among Israeli-Arab children. J Am Soc Nephrol 13: 400-405, 2002
9. Karle SM, Uetz B, Ronner V, Glaeser L, Hildebrandt F, Fuchshuber A: Novel mutations in NPHS2 detected in both familial and sporadic steroid-resistant nephrotic syndrome. J Am Soc Nephrol 13: 388-393, 2002
10. 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
11. Sellin L, Huber TB, Gerke P, Quack I, Pavensẗdt H, Walz G: NEPH1 defines a novel family of podocin interacting proteins. FASEB J 17: 115-117, 2003
12. Moeller MJ, Sanden SK, Soofi A, Wiggins RC, Holzman LB: Two gene fragments that direct podocyte-specific expression in transgenic mice. J Am Soc Nephrol 13: 1561-1567, 2002
13. He B, Ebarasi L, Hultenby K, Tryggvason K, Betsholtz C: Podocin-green fluorescence protein allows visualization and functional analysis of podocytes. J Am Soc Nephrol 22: 1019-1023, 2011
14. Miner JH, Morello R, Andrews KL, Li C, Antignac C, Shaw AS, Lee B: Transcriptional induction of slit diaphragm genes by Lmx1b is required in podocyte differentiation. J Clin Invest 109: 1065-1072, 2002
15. Rohr C, Prestel J, Heidet L, Hosser H, Kriz W, Johnson RL, Antignac C, Witzgall R: The LIM-homeodomain transcription factor Lmx1b plays a crucial role in podocytes. J Clin Invest 109: 1073-1082, 2002
16. Johnson RL, Tabin CJ: Molecular models for vertebrate limb development. Cell 90: 979-990, 1997
17. Chen H, Lun Y, Ovchinnikov D, Kokubo H, Oberg KC, Pepicelli CV, Gan L, Lee B, Johnson RL: Limb and kidney defects in Lmx1b mutant mice suggest an involvement of LMX1B in human nail patella syndrome. Nat Genet 19: 51-55, 1998
18. Dreyer SD, Zhou G, Baldini A, Winterpacht A, Zabel B, Cole W, Johnson RL, Lee B: Mutations in LMX1B cause abnormal skeletal patterning and renal dysplasia in nail patella syndrome. Nat Genet 19: 47-50, 1998
19. Dreyer SD, Morello R, German MS, Zabel B, Winterpacht A, Lunstrum GP, Horton WA, Oberg KC, Lee B: LMX1B transactivation and expression in nail-patella syndrome. Hum Mol Genet 9: 1067-1074, 2000
20. Morello R, Zhou G, Dreyer SD, Harvey SJ, Ninomiya Y, Thorner PS, Miner JH, Cole W, Winterpacht A, Zabel B, Oberg KC, Lee B: Regulation of glomerular basement membrane collagen expression by LMX1B contributes to renal disease in nail patella syndrome. Nat Genet 27: 205-208, 2001
21. German MS, Wang J, Chadwick RB, Rutter WJ: Synergistic activation of the insulin gene by a LIM-homeo domain protein and a basic helixloop-helix protein: Building a functional insulinminienhancer complex. Genes Dev 6: 2165-2176, 1992
22. Suleiman H, Heudobler D, Raschta AS, Zhao Y, Zhao Q, Hertting I, Vitzthum H, Moeller MJ, Holzman LB, Rachel R, Johnson R, Westphal H, Rascle A, Witzgall R: The podocyte-specific inactivation of Lmx1b, Ldb1 and E2a yields new insight into a transcriptional network in podocytes. Dev Biol 304: 701-712, 2007
23. Dunston JA, Reimschisel T, Ding YQ, Sweeney E, Johnson RL, Chen ZF, McIntosh I: A neurological phenotype in nail patella syndrome (NPS) patients illuminated by studies ofmurine Lmx1b expression. Eur J Hum Genet 13: 330-335, 2005
24. Takemoto M, He L, Norlin J, Patrakka J, Xiao Z, Petrova T, Bondjers C, Asp J, Wallgard E, Sun Y, Samuelsson T, Mostad P, Lundin S, Miura N, Sado Y, Alitalo K, Quaggin SE, Tryggvason K, Betsholtz C: Large-scale identification of genes implicated in kidney glomerulus development and function. EMBO J 25: 1160-1174, 2006
25. Carlsson P, Mahlapuu M: Forkhead transcription factors: Key players in development and metabolism. Dev Biol 250: 1-23, 2002
26. Miura N, Iida K, Kakinuma H, Yang XL, Sugiyama T: Isolation of the mouse (MFH-1) and human (FKHL 14) mesenchyme fork head-1 genes reveals conservation of their gene and protein structures. Genomics 41: 489-492, 1997
27. Brunskill EW, Georgas K, Rumballe B, Little MH, Potter SS: Defining the molecular character of the developing and adult kidney podocyte. PLoS ONE 6: e24640, 2011
28. Yildirim-Toruner C, Subramanian K, El Manjra L, Chen E, Goldstein S, Vitale E: A novel frameshift mutation of FOXC2 gene in a family with hereditary lymphedema-distichiasis syndrome associated with renal disease and diabetes mellitus. Am J Med Genet A 131: 281-286, 2004
29. Topczewska JM, Topczewski J, Shostak A, Kume T, Solnica-Krezel L, Hogan BL: The winged helix transcription factor Foxc1a is essential for somitogenesis in zebrafish. Genes Dev 15: 2483-2493, 2001
30. O'Hara FP, Beck E, Barr LK, Wong LL, Kessler DS, Riddle RD: Zebrafish Lmx1b.1 and Lmx1b.2 are required for maintenance of the isthmic organizer. Development 132: 3163-3173, 2005
31. Kramer-Zucker AG, Wiessner S, Jensen AM, Drummond IA: Organization of the pronephric filtration apparatus in zebra fish requires Nephrin, Podocin and the FERM domain protein Mosaic eyes. Dev Biol 285: 316-329, 2005
32. Majumdar A, Drummond IA: The zebrafish floating head mutant demonstrates podocytes play an important role in directing glomerular differentiation. Dev Biol 222: 147-157, 2000
33. Mollet G, Ratelade J, Boyer O, Muda AO, Morisset L, Lavin TA, Kitzis D, Dallman MJ, Bugeon L, Hubner N, Gubler MC, Antignac C, Esquivel EL: Podocin inactivation in mature kidneys causes focal segmental glomerulosclerosis and nephrotic syndrome. J Am Soc Nephrol 20: 2181-2189, 2009
34. Roselli S, Heidet L, Sich M, Henger A, Kretzler M, Gubler MC, Antignac C: Early glomerular filtration defect and severe renal disease in podocin-deficient mice. Mol Cell Biol 24: 550-560, 2004
35. Reményi A, Schöler HR, Wilmanns M: Combinatorial control of gene expression. Nat Struct Mol Biol 11: 812-815, 2004
36. De Val S, Chi NC, Meadows SM, Minovitsky S, Anderson JP, Harris IS, Ehlers ML, Agarwal P, Visel A, Xu SM, Pennacchio LA, Dubchak I, Krieg PA, Stainier DY, Black BL: Combinatorial regulation of endothelial gene expression by ets and forkhead transcription factors. Cell 135: 1053-1064, 2008
37. Prunell A, Kornberg RD, Lutter L, Klug A, Levitt M, Crick FH: Periodicity of deoxyribonuclease I digestion of chromatin. Science 204: 855-858, 1979
38. White JT, Zhang B, Cerqueira DM, Tran U, Wessely O: Notch signaling, wt1 and foxc2 are key regulators of the podocyte gene regulatory network in Xenopus. Development 137: 1863-1873, 2010
39. O'Brien LL, Grimaldi M, Kostun Z, Wingert RA, Selleck R, Davidson AJ: Wt1a, Foxc1a, and the Notch mediator Rbpj physically interact and regulate the formation of podocytes in zebrafish. Dev Biol 358: 318-330, 2011
40. Jurata LW, Gill GN: Functional analysis of the nuclear LIM domain interactor NLI. Mol Cell Biol 17: 5688-5698, 1997
41. Marini M, Giacopelli F, Seri M, Ravazzolo R: Interaction of the LMX1B and PAX2 gene products suggests possible molecular basis of differential phenotypes in Nail-Patella syndrome. Eur J Hum Genet 13: 789-792, 2005
42. Hobert O, Westphal H: Functions of LIM-homeobox genes. Trends Genet 16: 75-83, 2000
43. Sage J: Cyclin C makes an entry into the cell cycle. Dev Cell 6: 607-608, 2004
44. Ren S, Rollins BJ: Cyclin C/cdk3 promotes Rb-dependent G0 exit. Cell 117: 239-251, 2004
45. Tassan JP, Jaquenoud M, Léopold P, Schultz SJ, Nigg EA: Identification of human cyclin-dependent kinase 8, a putative protein kinase partner for cyclin C. Proc Natl Acad Sci U S A 92: 8871-8875, 1995
46. Kawakami K, Takeda H, Kawakami N, Kobayashi M, Matsuda N, Mishina M: A transposon-mediated gene trap approach identifies developmentally regulated genes in zebra fish. Dev Cell 7: 133-144, 2004
47. De Val S, Anderson JP, Heidt AB, Khiem D, Xu SM, Black BL: Mef2c is activated directly by Ets transcription factors through an evolutionarily conserved endothelial cell-specific enhancer. Dev Biol 275: 424-434, 2004
48. Ebarasi L, He L, Hultenby K, Takemoto M, Betsholtz C, Tryggvason K, Majumdar A: A reverse genetic screen in the zebrafish identifies crb2b as a regulator of the glomerular filtration barrier. Dev Biol 334: 1-9, 2009