CLIC5A, a component of the ezrin-podocalyxin complex in glomeruli, is a determinant of podocyte integrity

American Journal of Physiology - Renal Physiology

Volumn 298, Issue 6, 2010, Pages

  Wegner, Binytha ^a   Al Momany, Abass ^a   Kulak, Stephen C ^a   Kozlowski, Kathy ^a   Obeidat, Marya ^a   Jahroudi, Nadia ^a   Paes, John ^b   Berryman, Mark ^b   Ballermann, Barbara J ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b OHIO UNIVERSITY   (United States)

Author keywords

Actin; Chloride intracellular channel 5; Endothelial; Jitterbug; Microvilli

Indexed keywords

ACTIN; CHLORIDE INTRACELLULAR CHANNEL 5A PROTEIN; CYTOSKELETON PROTEIN; DOXORUBICIN; EZRIN; ION CHANNEL; MESSENGER RNA; PODOCALYXIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL MEMBRANE; CELL VACUOLE; COMPARATIVE STUDY; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENDOTHELIUM CELL; GLOMERULUS; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOGOLD ELECTRON MICROSCOPY; IMMUNOPRECIPITATION; KIDNEY INJURY; MALE; MICROALBUMINURIA; MICROVILLUS; MOUSE; NONHUMAN; NORTHERN BLOTTING; NUCLEOTIDE SEQUENCE; PODOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSMISSION ELECTRON MICROSCOPY; WESTERN BLOTTING; WILD TYPE;

EID: 77952691580     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00030.2010     Document Type: Article

References (66)

1. Advani A, Kelly DJ, Advani SL, Cox AJ, Thai K, Zhang Y, White KE, Gow RM, Marshall SM, Steer BM, Marsden PA, Rakoczy PE, Gilbert RE. Role of VEGF in maintaining renal structure and function under normotensive and hypertensive conditions. Proc Natl Acad Sci USA 104: 14448-14453, 2007. (Pubitemid 350003281)
2. Ashley RH. Challenging accepted ion channel biology: p64 and the CLIC family of putative intracellular anion channel proteins (Review). Mol Membr Biol 20: 1-11, 2003.
3. Ballermann BJ. Glomerular endothelial cell differentiation. Kidney Int 67: 1668-1671, 2005.
4. Ballermann BJ. Regulation of bovine glomerular endothelial cell growth in vitro. Am J Physiol Cell Physiol 256: C182-C189, 1989.
5. Berry KL, Bülow HE, Hall DH, Hobert O. A C. elegans CLIC-like protein required for intracellular tube formation and maintenance. Science 302: 2134-2137, 2003. (Pubitemid 38017948)
6. Berry KL, Hobert O. Mapping functional domains of chloride intracellular channel (CLIC) proteins in vivo. J Mol Biol 359: 1316-1333, 2006. (Pubitemid 43903501)
7. Berryman M, Bretscher A. Identification of a novel member of the chloride intracellular channel gene family (CLIC5) that associates with the actin cytoskeleton of placental microvilli. Mol Biol Cell 11: 1509-1521, 2000. (Pubitemid 30307892)
8. Berryman M, Bruno J, Price J, Edwards JC. CLIC-5A functions as a chloride channel in vitro and associates with the cortical actin cytoskeleton in vitro and in vivo. J Biol Chem 279: 34794-34801, 2004. (Pubitemid 39318112)
9. Berryman M, Franck Z, Bretscher A. Ezrin is concentrated in the apical microvilli of a wide variety of epithelial cells whereas moesin is found primarily in endothelial cells. J Cell Sci 105: 1025-1043, 1993. (Pubitemid 23258665)
10. Berryman MA, Goldenring JR. CLIC4 is enriched at cell-cell junctions and colocalizes with AKAP350 at the centrosome and midbody of cultured mammalian cells. Cell Motil Cytoskeleton 56: 159-172, 2003.
11. Bohman S, Matsumoto T, Suh K, Dimberg A, Jakobsson L, Yuspa S, Claesson-Welsh L. Proteomic analysis of vascular endothelial growth factor-induced endothelial cell differentiation reveals a role for chloride intracellular channel 4 (CLIC4) in tubular morphogenesis. J Biol Chem 280: 42397-42404, 2005. (Pubitemid 43023212)
12. Bretscher A, Chambers D, Nguyen R, Reczek D. ERM-Merlin and EBP50 protein families in plasma membrane organization and function. Annu Rev Cell Dev Biol 16: 113-143, 2000. (Pubitemid 32037502)
13. Chabardès-Garonne D, Mejéan A, Aude JC, Cheval L, Di Stefano A, Gaillard MC, Imbert-Teboul M, Wittner M, Balian C, Anthouard V, Robert C, Ségurens B, Wincker P, Weissenbach J, Doucet A, Elalouf JM. A panoramic view of gene expression in the human kidney. Proc Natl Acad Sci USA 100: 13710-13715, 2003.
14. Chen J, Cohn JA, Mandel LJ. Dephosphorylation of ezrin as an early event in renal microvillar breakdown and anoxic injury. Proc Natl Acad Sci USA 92: 7495-7499, 1995.
15. Chuang JZ, Milner TA, Zhu M, Sung CH. A 29 kDa intracellular chloride channel p64H1 is associated with large dense-core vesicles in rat hippocampal neurons. J Neurosci 19: 2919-2928, 1999.
16. Cromer BA, Morton CJ, Board PG, Parker MW. From glutathione transferase to pore in a CLIC. Eur Biophys J 31: 356-364, 2002.
17. Deen WM, Lazzara MJ, Myers BD. Structural determinants of glomerular permeability. Am J Physiol Renal Physiol 281: F579-F596, 2001.
18. Dulhunty A, Gage P, Curtis S, Chelvanayagam G, Board P. The glutathione transferase structural family includes a nuclear chloride channel and a ryanodine receptor calcium release channel modulator. J Biol Chem 276: 3319-3323, 2001.
19. Elter A, Hartel A, Sieben C, Hertel B, Fischer-Schliebs E, Luttge U, Moroni A, Thiel G. A plant homolog of animal chloride intracellular channels (CLICs) generates an ion conductance in heterologous systems. J Biol Chem 282: 8786-8792, 2007.
20. Eremina V, Baelde HJ, Quaggin SE. Role of the VEGF-a signaling pathway in the glomerulus: evidence for crosstalk between components of the glomerular filtration barrier. Nephron Physiol 106: p32-p37, 2007.
21. Eremina V, Sood M, Haigh J, Nagy A, Lajoie G, Ferrara N, Gerber HP, Kikkawa Y, Miner JH, Quaggin SE. Glomerular-specific alterations of VEGF-A expression lead to distinct congenital and acquired renal diseases. J Clin Invest 111: 707-716, 2003.
22. Fernandez-Salas E, Sagar M, Cheng C, Yuspa SH, Weinberg WC. p53 and tumor necrosis factor alpha regulate the expression of a mitochondrial chloride channel protein. J Biol Chem 274: 36488-36497, 1999.
23. Gagnon LH, Longo-Guess CM, Berryman M, Shin JB, Saylor KW, Yu H, Gillespie PG, Johnson KR. The chloride intracellular channel protein CLIC5 is expressed at high levels in hair cell stereocilia and is essential for normal inner ear function. J Neurosci 26: 10188-10198, 2006. (Pubitemid 44527412)
24. Griffon N, Jeanneteau F, Prieur F, Diaz J, Sokoloff P. CLIC6, a member of the intracellular chloride channel family, interacts with dopamine D(2)-like receptors. Brain Res Mol Brain Res 117: 47-57, 2003. (Pubitemid 37123109)
25. Harrop SJ, DeMaere MZ, Fairlie WD, Reztsova T, Valenzuela SM, Mazzanti M, Tonini R, Qiu MR, Jankova L, Warton K, Bauskin AR, Wu WM, Pankhurst S, Campbell TJ, Breit SN, Curmi PM. Crystal structure of a soluble form of the intracellular chloride ion channel CLIC1 (NCC27) at 1.4-A resolution. J Biol Chem 276: 44993-45000, 2001.
26. Hayashi K, Yonemura S, Matsui T, Tsukita S. Immunofluorescence detection of ezrin/radixin/moesin (ERM) proteins with their carboxyl-terminal threonine phosphorylated in cultured cells and tissues. J Cell Sci 112: 1149-1158, 1999.
27. He L, Sun Y, Patrakka J, Mostad P, Norlin J, Xiao Z, Andrae J, Tryggvason K, Samuelsson T, Betsholtz C, Takemoto M. Glomerulus-specific mRNA transcripts and proteins identified through kidney expressed sequence tag database analysis. Kidney Int 71: 889-900, 2007. (Pubitemid 46663792)
28. Herrera GA. Plasticity of mesangial cells: a basis for understanding pathological alterations. Ultrastruct Pathol 30: 471-479, 2006.
29. Hugo C, Nangaku M, Shankland SJ, Pichler R, Gordon K, Amieva MR, Couser WG, Furthmayr H, Johnson RJ. The plasma membrane-actin linking protein, ezrin, is a glomerular epithelial cell marker in glomerulogenesis, in the adult kidney and in glomerular injury. Kidney Int 54: 1934-1944, 1998.
30. Jentsch TJ, Stein V, Weinreich F, Zdebik AA. Molecular structure and physiological function of chloride channels. Physiol Rev 82: 503-568, 2002.
31. Kestilä M, Lenkkeri U, Männikkö M, Lamerdin J, McCready P, Putaala H, Ruotsalainen V, Morita T, Nissinen M, 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.
32. Khan SY, Ahmed ZM, Shabbir MI, Kitajiri S, Kalsoom S, Tasneem S, Shayiq S, Ramesh A, Srisailpathy S, Khan SN, Smith RJ, Riazuddin S, Friedman TB. Mutations of the RDX gene cause nonsyndromic hearing loss at the DFNB24 locus. Hum Mutat 28: 417-423, 2007.
33. Kikkawa Y, Virtanen I, Miner JH. Mesangial cells organize the glomerular capillaries by adhering to the G domain of laminin alpha5 in the glomerular basement membrane. J Cell Biol 161: 187-196, 2003.
34. Kitajiri S, Fukumoto K, Hata M, Sasaki H, Katsuno T, Nakagawa T, Ito J, Tsukita S. Radixin deficiency causes deafness associated with progressive degeneration of cochlear stereocilia. J Cell Biol 166: 559-570, 2004.
35. Landry D, Sullivan S, Nicolaides M, Redhead C, Edelman A, Field M, al-Awqati Q, Edwards J. Molecular cloning and characterization of p64, a chloride channel protein from kidney microsomes. J Biol Chem 268: 14948-14955, 1993.
36. Landry DW, Akabas MH, Redhead C, Edelman A, Cragoe EJ Jr, Al-Awqati Q. Purification and reconstitution of chloride channels from kidney and trachea. Science 244: 1469-1472, 1989.
37. Leveen P, Pekny M, Gebre-Medhin S, Swolin B, Larsson E, Betsholtz C. Mice deficient for PDGF B show renal, cardiovascular, and hematological abnormalities. Genes Dev 8: 1875-1887, 1994.
38. Littler DR, Assaad NN, Harrop SJ, Brown LJ, Pankhurst GJ, Luciani P, Aguilar MI, Mazzanti M, Berryman MA, Breit SN, Curmi PM. Crystal structure of the soluble form of the redox-regulated chloride ion channel protein CLIC4. FEBS J 272: 4996-5007, 2005.
39. Littler DR, Harrop SJ, Brown LJ, Pankhurst GJ, Mynott AV, Luciani P, Mandyam RA, Mazzanti M, Tanda S, Berryman MA, Breit SN, Curmi PM. Comparison of vertebrate and invertebrate CLIC proteins: the crystal structures of Caenorhabditis elegans EXC-4 and Drosophila melanogaster DmCLIC. Proteins 71: 364-378, 2008.
40. Littler DR, Harrop SJ, Fairlie WD, Brown LJ, Pankhurst GJ, Pankhurst S, DeMaere MZ, Campbell TJ, Bauskin AR, Tonini R, Mazzanti M, Breit SN, Curmi PM. The intracellular chloride ion channel protein CLIC1 undergoes a redox-controlled structural transition. J Biol Chem 279: 9298-9305, 2004.
41. Mi W, Liang YH, Li L, Su XD. The crystal structure of human chloride intracellular channel protein 2: a disulfide bond with functional implications. Proteins 71: 509-513, 2008.
42. Nagai T, Yokomori H, Yoshimura K, Fujimaki K, Nomura M, Hibi T, Oda M. Actin filaments around endothelial fenestrae in rat hepatic sinusoidal endothelial cells. Med Electron Microsc 37: 252-255, 2004.
43. Nishizawa T, Nagao T, Iwatsubo T, Forte JG, Urushidani T. Molecular cloning and characterization of a novel chloride intracellular channel-related protein, parchorin, expressed in water-secreting cells. J Biol Chem 275: 11164-11173, 2000.
44. Nyström J, Fierlbeck W, Granqvist A, Kulak SC, Ballermann BJ. A human glomerular SAGE transcriptome database. BMC Nephrol 10: 13, 2009.
45. Orlando RA, Takeda T, Zak B, Schmieder S, Benoit VM, McQuistan T, Furthmayr H, Farquhar MG. The glomerular epithelial cell anti-adhesin podocalyxin associates with the actin cytoskeleton through interactions with ezrin. J Am Soc Nephrol 12: 1589-1598, 2001.
46. Pataky F, Pironkova R, Hudspeth AJ. Radixin is a constituent of stereocilia in hair cells. Proc Natl Acad Sci USA 101: 2601-2606, 2004.
47. Patari-Sampo A, Ihalmo P, Holthofer H. Molecular basis of the glomerular filtration: nephrin and the emerging protein complex at the podocyte slit diaphragm. Ann Med 38: 483-492, 2006.
48. Ponsioen B, van Zeijl L, Langeslag M, Berryman M, Littler D, Jalink K, Moolenaar WH. Spatiotemporal regulation of chloride intracellular channel protein CLIC4 by RhoA. Mol Biol Cell 20: 4664-4672, 2009.
49. Pozzi A, Jarad G, Moeckel GW, Coffa S, Zhang X, Gewin L, Eremina V, Hudson BG, Borza DB, Harris RC, Holzman LB, Phillips CL, Fassler R, Quaggin SE, Miner JH, Zent R. Beta1 integrin expression by podocytes is required to maintain glomerular structural integrity. Dev Biol 316: 288-301, 2008.
50. Redhead CR, Edelman AE, Brown D, Landry DW, al-Awqati Q. A ubiquitous 64-kDa protein is a component of a chloride channel of plasma and intracellular membranes. Proc Natl Acad Sci USA 89: 3716-3720, 1992.
51. Schmieder S, Nagai M, Orlando RA, Takeda T, Farquhar MG. Podocalyxin activates RhoA and induces actin reorganization through NHERF1 and Ezrin in MDCK cells. J Am Soc Nephrol 15: 2289-2298, 2004.
52. Sengoelge G, Luo W, Fine D, Perschl AM, Fierlbeck W, Haririan A, Sorensson J, Rehman TU, Hauser P, Trevick JS, Kulak SC, Wegner B, Ballermann BJ. A SAGE-based comparison between glomerular and aortic endothelial cells. Am J Physiol Renal Physiol 288: F1290-F1300, 2005.
53. Shanks RA, Larocca MC, Berryman M, Edwards JC, Urushidani T, Navarre J, Goldenring JR. AKAP350 at the Golgi apparatus. II. Association of AKAP350 with a novel chloride intracellular channel (CLIC) family member. J Biol Chem 277: 40973-40980, 2002.
54. Shearer AE, Hildebrand MS, Bromhead CJ, Kahrizi K, Webster JA, Azadeh B, Kimberling WJ, Anousheh A, Nazeri A, Stephan D, Najmabadi H, Smith RJ, Bahlo M. A novel splice site mutation in the RDX gene causes DFNB24 hearing loss in an Iranian family. Am J Med Genet A 149A: 555-558, 2009.
55. Singh H, Ashley RH. Redox regulation of CLIC1 by cysteine residues associated with the putative channel pore. Biophys J 90: 1628-1638, 2006.
56. Soriano P. Abnormal kidney development and hematological disorders in PDGF beta-receptor mutant mice. Genes Dev 8: 1888-1896, 1994.
57. Sugimoto H, Hamano Y, Charytan D, Cosgrove D, Kieran M, Sudhakar A, Kalluri R. Neutralization of circulating vascular endothelial growth factor (VEGF) by anti-VEGF antibodies and soluble VEGF receptor 1 (sFlt-1) induces proteinuria. J Biol Chem 278: 12605-12608, 2003.
58. Suh KS, Mutoh M, Nagashima K, Fernandez-Salas E, Edwards LE, Hayes DD, Crutchley JM, Marin KG, Dumont RA, Levy JM, Cheng C, Garfield S, Yuspa SH. The organellular chloride channel protein CLIC4/mtCLIC translocates to the nucleus in response to cellular stress and accelerates apoptosis. J Biol Chem 279: 4632-4641, 2004.
59. Takeda T, McQuistan T, Orlando RA, Farquhar MG. Loss of glomerular foot processes is associated with uncoupling of podocalyxin from the actin cytoskeleton. J Clin Invest 108: 289-301, 2001.
60. Takemoto M, 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.
61. Tulk BM, Kapadia S, Edwards JC. CLIC1 inserts from the aqueous phase into phospholipid membranes, where it functions as an anion channel. Am J Physiol Cell Physiol 282: C1103-C1112, 2002.
62. Tung JJ, Hobert O, Berryman M, Kitajewski J. Chloride intracellular channel 4 is involved in endothelial proliferation and morphogenesis in vitro. Angiogenesis 12: 209-220, 2009.
63. Ulmasov B, Bruno J, Gordon N, Hartnett ME, Edwards JC. Chloride intracellular channel protein-4 functions in angiogenesis by supporting acidification of vacuoles along the intracellular tubulogenic pathway. Am J Pathol 174: 1084-1096, 2009.
64. Valenzuela SM, Martin DK, Por SB, Robbins JM, Warton K, Bootcov MR, Schofield PR, Campbell TJ, Breit SN. Molecular cloning and expression of a chloride ion channel of cell nuclei. J Biol Chem 272: 12575-12582, 1997.
65. Warton K, Tonini R, Fairlie WD, Matthews JM, Valenzuela SM, Qiu MR, Wu WM, Pankhurst S, Bauskin AR, Harrop SJ, Campbell TJ, Curmi PM, Breit SN, Mazzanti M. Recombinant CLIC1 (NCC27) assembles in lipid bilayers via a pH-dependent two-state process to form chloride ion channels with identical characteristics to those observed in Chinese hamster ovary cells expressing CLIC1. J Biol Chem 277: 26003-26011, 2002.
66. Weerapana E, Simon GM, Cravatt BF. Disparate proteome reactivity profiles of carbon electrophiles. Nat Chem Biol 4: 405-407, 2008.