Table of Contents
Journal of Signal Transduction
Volume 2011 (2011), Article ID 317852, 10 pages
http://dx.doi.org/10.1155/2011/317852
Review Article

Tyrosine Kinase Signaling in Kidney Glomerular Podocytes

1Division of Biochemistry, School of Pharmaceutical Science, Kitasato University, 5-9-1 Shirokane, Minato-ku, Tokyo 108-8641, Japan
2Department of Pediatrics, Graduate School of Medicine, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-8655, Japan
3Department of Molecular Biology, Yokohama City University School of Medicine, Kanazawa-ku, Yokohama 236-0004, Japan
4Division of Functional Proteomics, Graduate School of Nanobioscience, Yokohama City University Tsurumi-ku, Yokohama, Kanagawa 230-0045, Japan

Received 21 January 2011; Revised 17 March 2011; Accepted 30 March 2011

Academic Editor: J. Adolfo García-Sáinz

Copyright © 2011 Seisuke Hattori et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. H. Pavenstadt, W. Kriz, and M. Kretzler, “Cell biology of the glomerular podocyte,” Physiological Reviews, vol. 83, no. 1, pp. 253–307, 2003. View at Google Scholar · View at Scopus
  2. K. Tryggvason, J. Patrakka, and J. Wartiovaara, “Hereditary proteinuria syndromes and mechanisms of proteinuria,” The New England Journal of Medicine, vol. 354, no. 13, pp. 1387–1401, 2006. View at Publisher · View at Google Scholar · View at Scopus
  3. J. Patrakka and K. Tryggvason, “New insights into the role of podocytes in proteinuria,” Nature Reviews Nephrology, vol. 5, no. 8, pp. 463–468, 2009. View at Publisher · View at Google Scholar · View at Scopus
  4. M. M. Löwik, P. J. Groenen, E. N. Levtchenko, L. A. Monnens, and L. P. van den Heuvel, “Molecular genetic analysis of podocyte genes in focal segmental glomerulosclerosis—a review,” European Journal of Pediatrics, vol. 168, no. 11, pp. 1291–1304, 2009. View at Publisher · View at Google Scholar · View at Scopus
  5. D. Kerjaschki, “Caught flat-footed: podocyte damage and the molecular bases of focal glomerulosclerosis,” Journal of Clinical Investigation, vol. 108, no. 11, pp. 1583–1587, 2001. View at Publisher · View at Google Scholar · View at Scopus
  6. M. Kestilä, U. Lenkkeri, M. Männikkö et al., “Positionally cloned gene for a novel glomerular protein—nephrin—is mutated in congenital nephrotic syndrome,” Molecular Cell, vol. 1, no. 4, pp. 575–582, 1998. View at Google Scholar · View at Scopus
  7. H. Putaala, R. Soininen, P. Kilpeläinen, J. Wartiovaara, and K. Tryggvason, “The murine nephrin gene is specifically expressed in kidney, brain and pancreas: inactivation of the gene leads to massive proteinuria and neonatal death,” Human Molecular Genetics, vol. 10, no. 1, pp. 1–8, 2001. View at Google Scholar · View at Scopus
  8. D. B. Donoviel, D. D. Freed, H. Vogel et al., “Proteinuria and perinatal lethality in mice lacking NEPH1, a novel protein with homology to NEPHRIN,” Molecular and Cellular Biology, vol. 21, no. 14, pp. 4829–4836, 2001. View at Publisher · View at Google Scholar · View at Scopus
  9. N. Boute, O. Gribouval, S. Roselli et al., “NPHS2, encoding the glomerular protein podocin, is mutated in autosomal recessive steroid-resistant nephrotic syndrome,” Nature Genetics, vol. 24, no. 4, pp. 349–354, 2000. View at Publisher · View at Google Scholar · View at Scopus
  10. J. M. Kaplan, S. H. Kim, K. N. North et al., “Mutations in ACTN4, encoding α-actinin-4, cause familial focal segmental glomerulosclerosis,” Nature Genetics, vol. 24, no. 3, pp. 251–256, 2000. View at Publisher · View at Google Scholar · View at Scopus
  11. N. Y. Shih, J. Li, V. Karpitsk II et al., “Congenital nephrotic syndrome in mice lacking CD2-associated protein,” Science, vol. 286, no. 5438, pp. 312–315, 1999. View at Publisher · View at Google Scholar · View at Scopus
  12. L. Ciani, A. Patel, N. D. Allen, and C. Ffrench-Constant, “Mice lacking the giant protocadherin mFAT1 exhibit renal slit junction abnormalities and a partially penetrant cyclopia and anophthalmia phenotype,” Molecular and Cellular Biology, vol. 23, no. 10, pp. 3575–3582, 2003. View at Publisher · View at Google Scholar · View at Scopus
  13. S. Roselli, L. Heidet, M. Sich et al., “Early glomerular filtration defect and severe renal disease in podocin-deficient mice,” Molecular and Cellular Biology, vol. 24, no. 2, pp. 550–560, 2004. View at Publisher · View at Google Scholar · View at Scopus
  14. K. Schwarz, M. Simons, J. Reiser et al., “Podocin, a raft-associated component of the glomerular slit diaphragm, interacts with CD2AP and nephrin,” Journal of Clinical Investigation, vol. 108, no. 11, pp. 1621–1629, 2001. View at Publisher · View at Google Scholar · View at Scopus
  15. G. M. Barletta, I. A. Kovari, R. K. Verma, D. Kerjaschki, and L. B. Holzman, “Nephrin and Neph1 co-localize at the podocyte foot process intercellular junction and form cis hetero-oligomers,” Journal of Biological Chemistry, vol. 278, no. 21, pp. 19266–19271, 2003. View at Publisher · View at Google Scholar · View at Scopus
  16. P. Gerke, T. B. Huber, L. Sellin, T. Benzing, and G. Walz, “Homodimerization and heterodimerization of the glomerular podocyte proteins nephrin and NEPH1,” Journal of the American Society of Nephrology, vol. 14, no. 4, pp. 918–926, 2003. View at Publisher · View at Google Scholar · View at Scopus
  17. L. Sellin, T. B. Huber, P. Gerke, I. Quack, H. Pavenstädt, and G. Walz, “NEPH1 defines a novel family of podocin interacting proteins,” The FASEB Journal, vol. 17, no. 1, pp. 115–117, 2003. View at Google Scholar · View at Scopus
  18. T. B. Huber, M. Schmidts, P. Gerke et al., “The carboxyl terminus of Neph family members binds to the PDZ domain protein zonula occludens-1,” Journal of Biological Chemistry, vol. 278, no. 15, pp. 13417–13421, 2003. View at Publisher · View at Google Scholar · View at Scopus
  19. N. Y. Shi, J. Li, R. Cotran, P. Mundel, J. H. Miner, and A. S. Shaw, “CD2AP localizes to the slit diaphragm and binds to nephrin via a novel C-terminal domain,” American Journal of Pathology, vol. 159, no. 6, pp. 2303–2308, 2001. View at Google Scholar · View at Scopus
  20. S. Hirabayashi, M. Tajima, I. Yao, W. Nishimura, H. Mori, and Y. Hata, “JAM4, a junctional cell adhesion molecule interacting with a tight junction protein, MAGI-1,” Molecular and Cellular Biology, vol. 23, no. 12, pp. 4267–4282, 2003. View at Publisher · View at Google Scholar · View at Scopus
  21. S. Lehtonen, J. J. Ryan, K. Kudlicka, N. Iino, H. Zhou, and M. G. Farquhar, “Cell junction-associated proteins IQGAP1, MAGI-2, CASK, spectrins, and α-actinin are components of the nephrin multiprotein complex,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 28, pp. 9814–9819, 2005. View at Publisher · View at Google Scholar · View at Scopus
  22. T. Benzing, “Signaling at the slit diaphragm,” Journal of the American Society of Nephrology, vol. 15, no. 6, pp. 1382–1391, 2004. View at Publisher · View at Google Scholar · View at Scopus
  23. X. L. Liu, P. Kilpeläinen, U. Hellman et al., “Characterization of the interactions of the nephrin intracellular domain,” FEBS Journal, vol. 272, no. 1, pp. 228–243, 2005. View at Publisher · View at Google Scholar · View at Scopus
  24. T. B. Huber, B. Hartleben, J. Kim et al., “Nephrin and CD2AP associate with phosphoinositide 3-OH kinase and stimulate AKT-dependent signaling,” Molecular and Cellular Biology, vol. 23, no. 14, pp. 4917–4928, 2003. View at Publisher · View at Google Scholar · View at Scopus
  25. M. Simons, K. Schwarz, W. Kriz et al., “Involvement of lipid rafts in nephrin phosphorylation and organization of the glomerular slit diaphragm,” American Journal of Pathology, vol. 159, no. 3, pp. 1069–1077, 2001. View at Google Scholar · View at Scopus
  26. R. Verma, B. Wharram, I. Kovari et al., “Fyn binds to and phosphorylates the kidney slit diaphragm component Nephrin,” Journal of Biological Chemistry, vol. 278, no. 23, pp. 20716–20723, 2003. View at Publisher · View at Google Scholar · View at Scopus
  27. J. Lahdenperä, P. Kilpeläinen, X. L. Liu et al., “Clustering-induced tyrosine phosphorylation of nephrin by Src family kinases,” Kidney International, vol. 64, no. 2, pp. 404–413, 2003. View at Publisher · View at Google Scholar · View at Scopus
  28. H. Li, S. Lemay, L. Aoudjit, H. Kawachi, and T. Takano, “Src-family kinase Fyn phosphorylates the cytoplasmic domain of nephrin and modulates its interaction with podocin,” Journal of the American Society of Nephrology, vol. 15, no. 12, pp. 3006–3015, 2004. View at Publisher · View at Google Scholar · View at Scopus
  29. C. C. K. Yu, T. S. B. Yen, C. A. Lowell, and A. L. DeFranco, “Lupus-like kidney disease in mice deficient in the Src family tyrosine kinases Lyn and Fyn,” Current Biology, vol. 11, no. 1, pp. 34–38, 2001. View at Publisher · View at Google Scholar · View at Scopus
  30. R. Verma, I. Kovari, A. Soofi, D. Nihalani, K. Patrie, and L. B. Holzman, “Nephrin ectodomain engagement results in Src kinase activation, nephrin phosphorylation, Nck recruitment, and actin polymerization,” Journal of Clinical Investigation, vol. 116, no. 5, pp. 1346–1359, 2006. View at Publisher · View at Google Scholar · View at Scopus
  31. N. Jones, I. M. Blasutig, V. Eremina et al., “Nck adaptor proteins link nephrin to the actin cytoskeleton of kidney podocytes,” Nature, vol. 440, no. 7085, pp. 818–823, 2006. View at Publisher · View at Google Scholar · View at Scopus
  32. S. Gruenheid, R. DeVinney, F. Bladt et al., “Enteropathogenic E. coli Tir binds Nck to initiate actin pedestal formation in host cells,” Nature Cell Biology, vol. 3, no. 9, pp. 856–859, 2001. View at Publisher · View at Google Scholar · View at Scopus
  33. Y. Harita, H. Kurihara, H. Kosako et al., “Phosphorylation of nephrin triggers Ca2+ signaling by recruitment and activation of phospholipase C-γ1,” Journal of Biological Chemistry, vol. 284, no. 13, pp. 8951–8962, 2009. View at Publisher · View at Google Scholar · View at Scopus
  34. W. Li, J. Fan, and D. T. Woodley, “Nck/Dock: an adapter between cell surface receptors and the actin cytoskeleton,” Oncogene, vol. 20, no. 44, pp. 6403–6417, 2001. View at Publisher · View at Google Scholar · View at Scopus
  35. K. Uchida, K. Suzuki, M. Iwamoto et al., “Decreased tyrosine phosphorylation of nephrin in rat and human nephrosis,” Kidney International, vol. 73, no. 8, pp. 926–932, 2008. View at Publisher · View at Google Scholar · View at Scopus
  36. T. Ohashi, K. Uchida, Y. Asamiya et al., “Phosphorylation status of nephrin in human membranous nephropathy,” Clinical and Experimental Nephrology, vol. 14, no. 1, pp. 51–55, 2010. View at Publisher · View at Google Scholar · View at Scopus
  37. H. Li, J. Zhu, L. Aoudjit et al., “Rat nephrin modulates cell morphology via the adaptor protein Nck,” Biochemical and Biophysical Research Communications, vol. 349, no. 1, pp. 310–316, 2006. View at Publisher · View at Google Scholar · View at Scopus
  38. S. Y. Zhang, M. Kamal, K. Dahan et al., “C-mip impairs podocyte proximal signaling and induces heavy proteinuria,” Science Signaling, vol. 3, no. 122, p. ra39, 2010. View at Publisher · View at Google Scholar · View at Scopus
  39. H. Li, S. Lemay, L. Aoudjit, H. Kawachi, and T. Takano, “Src-family kinase Fyn phosphorylates the cytoplasmic domain of nephrin and modulates its interaction with podocin,” Journal of the American Society of Nephrology, vol. 15, no. 12, pp. 3006–3015, 2004. View at Publisher · View at Google Scholar · View at Scopus
  40. P. Garg, R. Verma, D. Nihalani, D. B. Johnstone, and L. B. Holzman, “Neph1 cooperates with nephrin to transduce a signal that induces actin polymerization,” Molecular and Cellular Biology, vol. 27, no. 24, pp. 8698–8712, 2007. View at Publisher · View at Google Scholar · View at Scopus
  41. Y. Harita, H. Kurihara, H. Kosako et al., “Neph1, a component of the kidney slit diaphragm, is tyrosine-phosphorylated by the Src family tyrosine kinase and modulates intracellular signaling by binding to Grb2,” Journal of Biological Chemistry, vol. 283, no. 14, pp. 9177–9186, 2008. View at Publisher · View at Google Scholar · View at Scopus
  42. N. Jones, L. A. New, M. A. Fortino et al., “Nck proteins maintain the adult glomerular filtration barrier,” Journal of the American Society of Nephrology, vol. 20, no. 7, pp. 1533–1543, 2009. View at Publisher · View at Google Scholar · View at Scopus
  43. S. Suetsugu, H. Miki, and T. Takenawa, “Spatial and temporal regulation of actin polymerization for cytoskeleton formation through Arp2/3 complex and WASP/WAVE proteins,” Cell Motility and the Cytoskeleton, vol. 51, no. 3, pp. 113–122, 2002. View at Publisher · View at Google Scholar · View at Scopus
  44. H. N. Higgs, “Actin nucleation: nucleation-promoting factors are not all equal,” Current Biology, vol. 11, no. 24, pp. R1009–R1012, 2001. View at Publisher · View at Google Scholar · View at Scopus
  45. R. Rohatgi, P. Nollau, H. Y. Henry Ho, M. W. Kirschner, and B. J. Mayer, “Nck and phosphatidylinositol 4,5-bisphosphate synergistically activate actin polymerization through the N-WASP-Arp2/3 pathway,” Journal of Biological Chemistry, vol. 276, no. 28, pp. 26448–26452, 2001. View at Publisher · View at Google Scholar · View at Scopus
  46. M. B. Goldberg, “Actin-based motility of intracellular microbial pathogens,” Microbiology and Molecular Biology Reviews, vol. 65, no. 4, pp. 595–626, 2001. View at Publisher · View at Google Scholar · View at Scopus
  47. M. A. Lemmon and J. Schlessinger, “Cell signaling by receptor tyrosine kinases,” Cell, vol. 141, no. 7, pp. 1117–1134, 2010. View at Publisher · View at Google Scholar · View at Scopus
  48. G. M. Rivera, C. A. Briceño, F. Takeshima, S. B. Snapper, and B. J. Mayer, “Inducible clustering of membrane-targeted SH3 domains of the adaptor protein Nck triggers localized actin polymerization,” Current Biology, vol. 14, no. 1, pp. 11–22, 2004. View at Publisher · View at Google Scholar · View at Scopus
  49. S. Etienne-Manneville and A. Hall, “Rho GTPases in cell biology,” Nature, vol. 420, no. 6916, pp. 629–635, 2002. View at Publisher · View at Google Scholar · View at Scopus
  50. P. Garg, R. Verma, L. Cook et al., “Actin-depolymerizing factor cofilin-1 is necessary in maintaining mature podocyte architecture,” Journal of Biological Chemistry, vol. 285, no. 29, pp. 22676–22688, 2010. View at Google Scholar
  51. S. Ashworth, B. Teng, J. Kaufeld et al., “Cofilin-1 inactivation leads to proteinuria—studies in zebrafish, mice and humans,” PLoS One, vol. 5, no. 9, Article ID e12626, 2010. View at Google Scholar
  52. N. Scaplehorn, A. Holmsträm, V. Moreau, F. Frischknecht, I. Reckmann, and M. Way, “Grb2 and Nck act cooperatively to promote actin-based motility of vaccinia virus,” Current Biology, vol. 12, no. 9, pp. 740–745, 2002. View at Publisher · View at Google Scholar · View at Scopus
  53. J. Zhu, N. Sun, L. Aoudjit et al., “Nephrin mediates actin reorganization via phosphoinositide 3-kinase in podocytes,” Kidney International, vol. 73, no. 5, pp. 556–566, 2008. View at Publisher · View at Google Scholar · View at Scopus
  54. A. Sakakibara, Y. Ohba, K. Kurokawa, M. Matsuda, and S. Hattori, “Novel function of Chat in controlling cell adhesion via Cas-Crk-C3G-pathway-mediated Rap1 activation,” Journal of Cell Science, vol. 115, no. 24, pp. 4915–4924, 2002. View at Publisher · View at Google Scholar · View at Scopus
  55. B. Hinkes, R. C. Wiggins, R. Gbadegesin et al., “Positional cloning uncovers mutations in PLCE1 responsible for a nephrotic syndrome variant that may be reversible,” Nature Genetics, vol. 38, no. 12, pp. 1397–1405, 2006. View at Publisher · View at Google Scholar · View at Scopus
  56. X. S. Qin, H. Tsukaguchi, A. Shono, A. Yamamoto, H. Kurihara, and T. Doi, “Phosphorylation of nephrin triggers its internalization by raft-mediated endocytosis,” Journal of the American Society of Nephrology, vol. 20, no. 12, pp. 2534–2545, 2009. View at Publisher · View at Google Scholar · View at Scopus
  57. I. Quack, L. C. Rump, P. Gerke et al., “β-arrestin2 mediates nephrin endocytosis and impairs slit diaphragm integrity,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 38, pp. 14110–14115, 2006. View at Publisher · View at Google Scholar · View at Scopus
  58. H. Hanafusa, S. Tor II, T. Yasunaga, and E. Nishida, “Sprouty1 and sprouty2 provide a control mechanism for the Ras/MAPK signalling pathway,” Nature Cell Biology, vol. 4, no. 11, pp. 850–858, 2002. View at Publisher · View at Google Scholar · View at Scopus
  59. M. Honma, O. Higuchi, M. Shirakata et al., “Dok-3 sequesters Grb2 and inhibits the Ras-Erk pathway downstream of protein-tyrosine kinases,” Genes to Cells, vol. 11, no. 2, pp. 143–151, 2006. View at Publisher · View at Google Scholar · View at Scopus
  60. Y. P. Chong, T. D. Mulhern, and H. C. Cheng, “C-terminal Src kinase (CSK) and CSK-homologous kinase (CHK)—endogenous negative regulators of Src-family protein kinases,” Growth Factors, vol. 23, no. 3, pp. 233–244, 2005. View at Publisher · View at Google Scholar · View at Scopus
  61. Y. Zhang, Y. Yoshida, M. Nameta et al., “Glomerular proteins related to slit diaphragm and matrix adhesion in the foot processes are highly tyrosine phosphorylated in the normal rat kidney,” Nephrology Dialysis Transplantation, vol. 25, no. 6, pp. 1785–1795, 2010. View at Publisher · View at Google Scholar · View at Scopus
  62. J. Reiser, F. J. Pixle, and A. Hug, “Regulation of mouse podocyte process dynamics by protein tyrosine phosphatases rapid communication,” Kidney International, vol. 57, no. 5, pp. 2035–2042, 2000. View at Google Scholar
  63. B. L. Wharram, M. Goyal, P. J. Gillespie et al., “Altered podocyte structure in GLEPP1 (Ptpro)-deficient mice associated with hypertension and low glomerular filtration rate,” Journal of Clinical Investigation, vol. 106, no. 10, pp. 1281–1290, 2000. View at Google Scholar · View at Scopus
  64. S. Deane, R. C. Wiggins, M. Goyal et al., “Antibodies to protein tyrosine phosphatase receptor type O (PTPro) increase glomerular albumin permeability (Palb),” American Journal of Physiology—Renal Physiology, vol. 297, no. 1, pp. F138–F144, 2009. View at Publisher · View at Google Scholar · View at Scopus
  65. H. Kurihara, Y. Harita, and K. Ichimura, “SIRP-alpha-CD47 system functions as an intercellular signal in the renal glomerulus,” American Journal of Physiology and Renal Physiology, vol. 299, no. 3, pp. F517–F527, 2010. View at Google Scholar
  66. G. Mouneimne, L. Soon, V. DesMarais et al., “Phospholipase C and cofilin are required for carcinoma cell directionality in response to EGF stimulation,” Journal of Cell Biology, vol. 166, no. 5, pp. 697–708, 2004. View at Publisher · View at Google Scholar · View at Scopus
  67. H. Pavenstädt, “Roles of the podocyte in glomerular function,” American Journal of Physiology, vol. 278, no. 2, pp. F173–F179, 2000. View at Google Scholar · View at Scopus
  68. M. P. Winn, P. J. Conlon, K. L. Lynn et al., “Medicine: a mutation in the TRPC6 cation channel causes familial focal segmental glomerulosclerosis,” Science, vol. 308, no. 5729, pp. 1801–1804, 2005. View at Publisher · View at Google Scholar · View at Scopus
  69. J. Reiser, K. R. Polu, C. C. Möller et al., “TRPC6 is a glomerular slit diaphragm-associated channel required for normal renal function,” Nature Genetics, vol. 37, no. 7, pp. 739–744, 2005. View at Publisher · View at Google Scholar · View at Scopus
  70. J. Abramowitz and L. Birnbaumer, “Physiology and pathophysiology of canonical transient receptor potential channels,” The FASEB Journal, vol. 23, no. 2, pp. 297–328, 2009. View at Publisher · View at Google Scholar · View at Scopus
  71. B. Nilius, G. Owsianik, T. Voets, and J. A. Peters, “Transient receptor potential cation channels in disease,” Physiological Reviews, vol. 87, no. 1, pp. 165–217, 2007. View at Publisher · View at Google Scholar · View at Scopus
  72. K. Kiselyov and R. L. Patterson, “The integrative function of TRPC channels,” Frontiers in Bioscience, vol. 14, pp. 45–58, 2009. View at Google Scholar · View at Scopus
  73. C. C. Möller, C. Wei, M. M. Altintas et al., “Induction of TRPC6 channel in acquired forms of proteinuric kidney disease,” Journal of the American Society of Nephrology, vol. 18, no. 1, pp. 29–36, 2007. View at Publisher · View at Google Scholar · View at Scopus
  74. P. Krall, C. P. Canales, P. Kairath et al., “Podocyte-specific overexpression of wild type or mutant trpc6 in mice is sufficient to cause glomerular disease,” PLoS One, vol. 5, no. 9, Article ID e12859, 2010. View at Google Scholar
  75. J. Schlöndorff, D. Del Camino, R. Carrasquillo, V. Lacey, and M. R. Pollak, “TRPC6 mutations associated with focal segmental glomerulosclerosis cause constitutive activation of NFAT-dependent transcription,” American Journal of Physiology, vol. 296, no. 3, pp. C558–C569, 2009. View at Publisher · View at Google Scholar · View at Scopus
  76. C. Hisatsune, Y. Kuroda, K. Nakamura et al., “Regulation of TRPC6 channel activity by tyrosine phosphorylation,” Journal of Biological Chemistry, vol. 279, no. 18, pp. 18887–18894, 2004. View at Publisher · View at Google Scholar · View at Scopus