Motor protein Myo1c is a podocyte protein that facilitates the transport of slit diaphragm protein Neph1 to the podocyte membrane

Molecular and Cellular Biology

Volumn 31, Issue 10, 2011, Pages 2134-2150

  Arif, E ^a   Wagner, M C ^b   Johnstone, D B ^a   Wong, H N ^a   George, B ^a   Pruthi, P A ^d   Lazzara, M J ^c   Nihalani, D ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b INDIANA UNIVERSITY   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d THE ENERGY AND RESOURCES INSTITUTE   (India)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; BOVINE SERUM ALBUMIN; MEMBRANE PROTEIN; MOLECULAR MOTOR; MYOSIN I; NEPHRIN; PROTEIN MYOSIN TYPE I C; PROTEIN NEPH1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL JUNCTION; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; CELL MIGRATION; CONTROLLED STUDY; DIAPHRAGM; ELECTRIC RESISTANCE; GENE SILENCING; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PODOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; RAT; TIGHT JUNCTION; WILD TYPE; WOUND; WOUND HEALING;

ACTINS; CELL LINE; CELL MEMBRANE; CELL MOVEMENT; ELECTRIC IMPEDANCE; GENE KNOCKDOWN TECHNIQUES; HUMANS; KIDNEY GLOMERULUS; MEMBRANE PROTEINS; MICROSCOPY, ELECTRON; MICROSCOPY, FLUORESCENCE; MYOSIN TYPE I; PODOCYTES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TIGHT JUNCTIONS;

BOVINAE;

EID: 79956081242     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.05051-11     Document Type: Article

References (50)

1. Bahler, M., and A. Rhoads. 2002. Calmodulin signaling via the IQ motif. FEBS Lett. 513:107-113.
2. Barletta, G. M., I. A. Kovari, R. K. Verma, D. Kerjaschki, and L. B. Holzman. 2003. Nephrin and Neph1 co-localize at the podocyte foot process intercellular junction and form cis hetero-oligomers. J. Biol. Chem. 278: 19266-19271.
3. Barylko, B., G. Jung, and J. P. Albanesi. 2005. Structure, function, and regulation of myosin 1C. Acta Biochim. Pol. 52:373-380.
4. Benzing, T. 2004. Signaling at the slit diaphragm. J. Am. Soc. Nephrol. 15:1382-1391.
5. Bose, A., et al. 2002. Glucose transporter recycling in response to insulin is facilitated by myosin Myo1c. Nature 420:821-824.
6. Coluccio, L. M. 1997. Myosin I. Am. J. Physiol. 273:C347-C359.
7. Donoviel, D. B., et al. 2001. Proteinuria and perinatal lethality in mice lacking NEPH1, a novel protein with homology to NEPHRIN. Mol. Cell. Biol. 21:4829-4836.
8. Doublier, S., et al. 2001. Nephrin redistribution on podocytes is a potential mechanism for proteinuria in patients with primary acquired nephrotic syndrome. Am. J. Pathol. 158:1723-1731.
9. Fath, K. R., and D. R. Burgess. 1993. Golgi-derived vesicles from developing epithelial cells bind actin filaments and possess myosin-I as a cytoplasmically oriented peripheral membrane protein. J. Cell Biol. 120:117-127.
10. Garg, P., R. Verma, D. Nihalani, D. B. Johnstone, and L. B. Holzman. 2007. Neph1 cooperates with Nephrin to transduce a signal that induces actin polymerization. Mol. Cell. Biol. 27:8698-8712.
11. Gerke, P., T. B. Huber, L. Sellin, T. Benzing, and G. Walz. 2003. Homodimerization and heterodimerization of the glomerular podocyte proteins nephrin and NEPH1. J. Am. Soc. Nephrol. 14:918-926.
12. Gillespie, P. G., et al. 2001. Myosin-I nomenclature. J. Cell Biol. 155:703-704.
13. Gillespie, P. G., and J. L. Cyr. 2004. Myosin-1c, the hair cell's adaptation motor. Annu. Rev. Physiol. 66:521-545.
14. Gillespie, P. G., M. C. Wagner, and A. J. Hudspeth. 1993. Identification of a 120 kd hair-bundle myosin located near stereociliary tips. Neuron 11:581-594.
15. Hartleben, B., et al. 2008. Neph-Nephrin proteins bind the Par3-Par6-atypical protein kinase C (aPKC) complex to regulate podocyte cell polarity. J. Biol. Chem. 283:23033-23038.
16. Heintzelman, M. B., T. Hasson, and M. S. Mooseker. 1994. Multiple unconventional myosin domains of the intestinal brush border cytoskeleton. J. Cell Sci. 107(Pt. 12):3535-3543.
17. Holt, J. R., et al. 2002. A chemical-genetic strategy implicates myosin-1c in adaptation by hair cells. Cell 108:371-381.
18. Holzman, L. B., et al. 1999. Nephrin localizes to the slit pore of the glomerular epithelial cell. Kidney Int. 56:1481-1491.
19. Huber, T. B., et al. 2003. The carboxyl terminus of Neph family members binds to the PDZ domain protein zonula occludens-1. J. Biol. Chem. 278: 13417-13421.
20. Johnstone, D. B., and L. B. Holzman. 2006. Clinical impact of research on the podocyte slit diaphragm. Nat. Clin. Pract. Nephrol. 2:271-282.
21. Jung, G., K. Remmert, X. Wu, J. M. Volosky, and J. A. Hammer III. 2001. The Dictyostelium CARMIL protein links capping protein and the Arp2/3 complex to type I myosins through their SH3 domains. J. Cell Biol. 153: 1479-1497.
22. Kwon, O., C. L. Phillips, and B. A. Molitoris. 2002. Ischemia induces alterations in actin filaments in renal vascular smooth muscle cells. Am. J. Physiol. Renal Physiol. 282:F1012-F1019.
23. Lambert, J., J. M. Naeyaert, T. Callens, A. De Paepe, and L. Messiaen. 1998. Human myosin V gene produces different transcripts in a cell type-specific manner. Biochem. Biophys. Res. Commun. 252:329-333.
24. Liu, G., et al. 2003. Neph1 and nephrin interaction in the slit diaphragm is an important determinant of glomerular permeability. J. Clin. Invest. 112: 209-221.
25. Lowenborg, E. K., G. Jaremko, and U. B. Berg. 2000. Glomerular function and morphology in puromycin aminonucleoside nephropathy in rats. Nephrol. Dial. Transplant. 15:1547-1555.
26. Manceva, S., et al. 2007. Calcium regulation of calmodulin binding to and dissociation from the myo1c regulatory domain. Biochemistry 46:11718-11726.
27. Marshall, C. B., J. W. Pippin, R. D. Krofft, and S. J. Shankland. 2006. Puromycin aminonucleoside induces oxidant-dependent DNA damage in podocytes in vitro and in vivo. Kidney Int. 70:1962-1973.
28. McConnell, R. E., and M. J. Tyska. 2010. Leveraging the membrane-cytoskeleton interface with myosin-1. Trends Cell Biol. 20:418-426.
29. Moreno, J. A., et al. 2008. A slit in podocyte death. Curr. Med. Chem. 15:1645-1654.
30. Nakamori, Y., et al. 2006. Myosin motor Myo1c and its receptor NEMO/IKK-gamma promote TNF-alpha-induced serine307 phosphorylation of IRS-1. J. Cell Biol. 173:665-671.
31. Neumann-Haefelin, E., et al. 2010. A model organism approach: defining the role of Neph proteins as regulators of neuron and kidney morphogenesis. Hum. Mol. Genet. 19:2347-2359.
32. Nihalani, D., H. Wong, R. Verma, and L. B. Holzman. 2007. Src family kinases directly regulate JIP1 module dynamics and activation. Mol. Cell. Biol. 27:2431-2441.
33. Novak, K. D., and M. A. Titus. 1998. The myosin I SH3 domain and TEDS rule phosphorylation site are required for in vivo function. Mol. Biol. Cell 9:75-88.
34. Otaki, Y., et al. 2008. Dissociation of NEPH1 from nephrin is involved in development of a rat model of focal segmental glomerulosclerosis. Am. J. Physiol. Renal Physiol. 295:F1376-F1387.
35. Patari-Sampo, A., P. Ihalmo, and H. Holthofer. 2006. Molecular basis of the glomerular filtration: nephrin and the emerging protein complex at the podocyte slit diaphragm. Ann. Med. 38:483-492.
36. Patrakka, J., and K. Tryggvason. 2010. Molecular make-up of the glomerular filtration barrier. Biochem. Biophys. Res. Commun. 396:164-169.
37. Patrakka, J., and K. Tryggvason. 2007. Nephrin-a unique structural and signaling protein of the kidney filter. Trends Mol. Med. 13:396-403.
38. Pierchala, B. A., M. R. Munoz, and C. C. Tsui. 2010. Proteomic analysis of the slit diaphragm complex: CLIC5 is a protein critical for podocyte morphology and function. Kidney Int. 78:868-882.
39. Saleem, M. A., et al. 2002. Co-localization of nephrin, podocin, and the actin cytoskeleton: evidence for a role in podocyte foot process formation. Am. J. Pathol. 161:1459-1466.
40. Sellin, L., et al. 2003. NEPH1 defines a novel family of podocin interacting proteins. FASEB J. 17:115-117.
41. Shankland, S. J. 2006. The podocyte's response to injury: role in proteinuria and glomerulosclerosis. Kidney Int. 69:2131-2147.
42. Swiatecka-Urban, A., et al. 2004. Myosin VI regulates endocytosis of the cystic fibrosis transmembrane conductance regulator. J. Biol. Chem. 279: 38025-38031.
43. Tang, N., T. Lin, and E. M. Ostap. 2002. Dynamics of myo1c (myosin-ibeta) lipid binding and dissociation. J. Biol. Chem. 277:42763-42768.
44. Tryggvason, K., T. Pikkarainen, and J. Patrakka. 2006. Nck links nephrin to actin in kidney podocytes. Cell 125:221-224.
45. Verma, R., et al. 2006. Nephrin ectodomain engagement results in Src kinase activation, nephrin phosphorylation, Nck recruitment, and actin polymerization. J. Clin. Invest. 116:1346-1359.
46. Wagner, M. C., B. Barylko, and J. P. Albanesi. 1992. Tissue distribution and subcellular localization of mammalian myosin I. J. Cell Biol. 119:163-170.
47. Wagner, M. C., et al. 2008. Ischemic injury to kidney induces glomerular podocyte effacement and dissociation of slit diaphragm proteins Neph1 and ZO-1. J. Biol. Chem. 283:35579-35589.
48. Wang, L., et al. 2005. Activation of Galpha q-coupled signaling pathways in glomerular podocytes promotes renal injury. J. Am. Soc. Nephrol. 16:3611-3622.
49. Wernerson, A., et al. 2003. Altered ultrastructural distribution of nephrin in minimal change nephrotic syndrome. Nephrol. Dial. Transplant. 18:70-76.
50. Yip, M. F., et al. 2008. CaMKII-mediated phosphorylation of the myosin motor Myo1c is required for insulin-stimulated GLUT4 translocation in adipocytes. Cell Metab. 8:384-398.