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Article

Structural Analysis of the Myo1c and Neph1 Complex Provides Insight into the Intracellular Movement of Neph1

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Pages 1639-1654 | Received 08 Jan 2016, Accepted 21 Mar 2016, Published online: 17 Mar 2023

REFERENCES

  • Tryggvason K, Patrakka J, Wartiovaara J. 2006. Hereditary proteinuria syndromes and mechanisms of proteinuria. N Engl J Med 354:1387–1401. http://dx.doi.org/10.1056/NEJMra052131.
  • Tryggvason K, Pikkarainen T, Patrakka J. 2006. Nck links nephrin to actin in kidney podocytes. Cell 125:221–224. http://dx.doi.org/10.1016/j.cell.2006.04.002.
  • Welsh GI, Saleem MA. 2012. The podocyte cytoskeleton—key to a functioning glomerulus in health and disease. Nat Rev Nephrol 8:14–21.
  • Faul C, Asanuma K, Yanagida-Asanuma E, Kim K, Mundel P. 2007. Actin up: regulation of podocyte structure and function by components of the actin cytoskeleton. Trends Cell Biol 17:428–437. http://dx.doi.org/10.1016/j.tcb.2007.06.006.
  • Buccione R, Orth JD, McNiven MA. 2004. Foot and mouth: podosomes, invadopodia and circular dorsal ruffles. Nat Rev Mol Cell Biol 5:647–657. http://dx.doi.org/10.1038/nrm1436.
  • Kerjaschki D. 2001. Caught flat-footed: podocyte damage and the molecular bases of focal glomerulosclerosis. J Clin Invest 108:1583–1587. http://dx.doi.org/10.1172/JCI200114629.
  • Takeda T, McQuistan T, Orlando RA, Farquhar MG. 2001. Loss of glomerular foot processes is associated with uncoupling of podocalyxin from the actin cytoskeleton. J Clin Invest 108:289–301. http://dx.doi.org/10.1172/JCI12539.
  • D'Agati VD, Kaskel FJ, Falk RJ. 2011. Focal segmental glomerulosclerosis. N Engl J Med 365:2398–2411. http://dx.doi.org/10.1056/NEJMra1106556.
  • Verma R, Kovari I, Soofi A, Nihalani D, Patrie K, Holzman LB. 2006. Nephrin ectodomain engagement results in Src kinase activation, nephrin phosphorylation, Nck recruitment, and actin polymerization. J Clin Invest 116:1346–1359. http://dx.doi.org/10.1172/JCI27414.
  • Barletta GM, Kovari IA, Verma RK, Kerjaschki D, Holzman LB. 2003. Nephrin and Neph1 co-localize at the podocyte foot process intercellular junction and form cis hetero-oligomers. J Biol Chem 278:19266–19271. http://dx.doi.org/10.1074/jbc.M301279200.
  • Doublier S, Ruotsalainen V, Salvidio G, Lupia E, Biancone L, Conaldi PG, Reponen P, Tryggvason K, Camussi G. 2001. Nephrin redistribution on podocytes is a potential mechanism for proteinuria in patients with primary acquired nephrotic syndrome. Am J Pathol 158:1723–1731. http://dx.doi.org/10.1016/S0002-9440(10)64128-4.
  • Otaki Y, Miyauchi N, Higa M, Takada A, Kuroda T, Gejyo F, Shimizu F, Kawachi H. 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. http://dx.doi.org/10.1152/ajprenal.00075.2008.
  • Wernerson A, Duner F, Pettersson E, Widholm SM, Berg U, Ruotsalainen V, Tryggvason K, Hultenby K, Soderberg M. 2003. Altered ultrastructural distribution of nephrin in minimal change nephrotic syndrome. Nephrol Dial Transplant 18:70–76. http://dx.doi.org/10.1093/ndt/18.1.70.
  • Wagner MC, Rhodes G, Wang E, Pruthi V, Arif E, Saleem MA, Wean SE, Garg P, Verma R, Holzman LB, Gattone V, Molitoris BA, Nihalani D. 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. http://dx.doi.org/10.1074/jbc.M805507200.
  • Arif E, Wagner MC, Johnstone DB, Wong HN, George B, Pruthi PA, Lazzara MJ, Nihalani D. 2011. Motor protein Myo1c is a podocyte protein that facilitates the transport of slit diaphragm protein Neph1 to the podocyte membrane. Mol Cell Biol 31:2134–2150. http://dx.doi.org/10.1128/MCB.05051-11.
  • Nabet B, Tsai A, Tobias JW, Carstens RP. 2009. Identification of a putative network of actin-associated cytoskeletal proteins in glomerular podocytes defined by co-purified mRNAs. PLoS One 4:e6491. http://dx.doi.org/10.1371/journal.pone.0006491.
  • Pierchala BA, Munoz MR, Tsui CC. 2010. Proteomic analysis of the slit diaphragm complex: CLIC5 is a protein critical for podocyte morphology and function. Kidney Int 78:868–882. http://dx.doi.org/10.1038/ki.2010.212.
  • Krendel M, Osterweil EK, Mooseker MS. 2007. Myosin 1E interacts with synaptojanin-1 and dynamin and is involved in endocytosis. FEBS Lett 581:644–650. http://dx.doi.org/10.1016/j.febslet.2007.01.021.
  • Mele C, Iatropoulos P, Donadelli R, Calabria A, Maranta R, Cassis P, Buelli S, Tomasoni S, Piras R, Krendel M, Bettoni S, Morigi M, Delledonne M, Pecoraro C, Abbate I, Capobianchi MR, Hildebrandt F, Otto E, Schaefer F, Macciardi F, Ozaltin F, Emre S, Ibsirlioglu T, Benigni A, Remuzzi G, Noris M. 2011. MYO1E mutations and childhood familial focal segmental glomerulosclerosis. N Engl J Med 365:295–306. http://dx.doi.org/10.1056/NEJMoa1101273.
  • Pecci A, Panza E, Pujol-Moix N, Klersy C, Di Bari F, Bozzi V, Gresele P, Lethagen S, Fabris F, Dufour C, Granata A, Doubek M, Pecoraro C, Koivisto PA, Heller PG, Iolascon A, Alvisi P, Schwabe D, De Candia E, Rocca B, Russo U, Ramenghi U, Noris P, Seri M, Balduini CL, Savoia A. 2008. Position of nonmuscle myosin heavy chain IIA (NMMHC-IIA) mutations predicts the natural history of MYH9-related disease. Hum Mutat 29:409–417. http://dx.doi.org/10.1002/humu.20661.
  • Sekine T, Konno M, Sasaki S, Moritani S, Miura T, Wong WS, Nishio H, Nishiguchi T, Ohuchi MY, Tsuchiya S, Matsuyama T, Kanegane H, Ida K, Miura K, Harita Y, Hattori M, Horita S, Igarashi T, Saito H, Kunishima S. 2010. Patients with Epstein-Fechtner syndromes owing to MYH9 R702 mutations develop progressive proteinuric renal disease. Kidney Int 78:207–214. http://dx.doi.org/10.1038/ki.2010.21.
  • Wagner MC, Barylko B, Albanesi JP. 1992. Tissue distribution and subcellular localization of mammalian myosin I. J Cell Biol 119:163–170.
  • Barylko B, Jung G, Albanesi JP. 2005. Structure, function, and regulation of myosin 1C. Acta Biochim Pol 52:373–380.
  • Sellers JR. 2000. Myosins: a diverse superfamily. Biochim Biophys Acta 1496:3–22. http://dx.doi.org/10.1016/S0167-4889(00)00005-7.
  • Gillespie PG, Cyr JL. 2004. Myosin-1c, the hair cell's adaptation motor. Annu Rev Physiol 66:521–545. http://dx.doi.org/10.1146/annurev.physiol.66.032102.112842.
  • Tang N, Lin T, Ostap EM. 2002. Dynamics of Myo1c (myosin-Ibeta) lipid binding and dissociation. J Biol Chem 277:42763–42768. http://dx.doi.org/10.1074/jbc.M206388200.
  • Brandstaetter H, Kendrick-Jones J, Buss F. 2012. Myo1c regulates lipid raft recycling to control cell spreading, migration and Salmonella invasion. J Cell Sci 125:1991–2003. http://dx.doi.org/10.1242/jcs.097212.
  • Johnstone DB, Holzman LB. 2006. Clinical impact of research on the podocyte slit diaphragm. Nat Clin Pract Nephrol 2:271–282. http://dx.doi.org/10.1038/ncpneph0180.
  • Patrakka J, Tryggvason K. 2010. Molecular make-up of the glomerular filtration barrier. Biochem Biophys Res Commun 396:164–169. http://dx.doi.org/10.1016/j.bbrc.2010.04.069.
  • Saleem MA, Ni L, Witherden I, Tryggvason K, Ruotsalainen V, Mundel P, Mathieson PW. 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. http://dx.doi.org/10.1016/S0002-9440(10)64421-5.
  • Arif E, Kumari B, Wagner MC, Zhou W, Holzman LB, Nihalani D. 29 May 2013. Myo1c is an unconventional myosin required for zebrafish glomerular development. Kidney Int http://dx.doi.org/10.1038/ki.2013.201.
  • Münnich S, Taft MH, Manstein DJ. 2014. Crystal structure of human myosin 1c–the motor in GLUT4 exocytosis: implications for Ca2+ regulation and 14-3-3 binding. J Mol Biol 426:2070–2081. http://dx.doi.org/10.1016/j.jmb.2014.03.004.
  • Münnich S, Manstein DJ. 2013. Expression, purification, crystallization and preliminary X-ray crystallographic analysis of human myosin 1c in complex with calmodulin. Acta Crystallogr Sect F Struct Biol Cryst Commun 69:1020–1022. http://dx.doi.org/10.1107/S1744309113020988.
  • Lu Q, Li J, Ye F, Zhang M. 2015. Structure of myosin-1c tail bound to calmodulin provides insights into calcium-mediated conformational coupling. Nat Struct Mol Biol 22:81–88.
  • Yip MF, Ramm G, Larance M, Hoehn KL, Wagner MC, Guilhaus M, James DE. 2008. CaMKII-mediated phosphorylation of the myosin motor Myo1c is required for insulin-stimulated GLUT4 translocation in adipocytes. Cell Metab 8:384–398. http://dx.doi.org/10.1016/j.cmet.2008.09.011.
  • Chen XW, Leto D, Chiang SH, Wang Q, Saltiel AR. 2007. Activation of RalA is required for insulin-stimulated Glut4 trafficking to the plasma membrane via the exocyst and the motor protein Myo1c. Dev Cell 13:391–404. http://dx.doi.org/10.1016/j.devcel.2007.07.007.
  • Arif E, Rathore YS, Kumari B, Ashish F, Wong HN, Holzman LB, Nihalani D. 2014. Slit diaphragm protein Neph1 and its signaling: a novel therapeutic target for protection of podocytes against glomerular injury. J Biol Chem 289:9502–9518. http://dx.doi.org/10.1074/jbc.M113.505743.
  • Qin X-S, Tsukaguchi H, Shono A, Yamamoto A, Kurihara H, Doi T. 2009. Phosphorylation of nephrin triggers its internalization by raft-mediated endocytosis. J Am Soc Nephrol 20:2534–2545. http://dx.doi.org/10.1681/ASN.2009010011.
  • Mallik L, Arif E, Sharma P, Rathore YS, Wong HN, Holzman LB, Ashish, Nihalani D. 2012. Solution structure analysis of cytoplasmic domain of podocyte protein Neph1 using small/wide angle x-ray scattering (SWAXS). J Biol Chem 287:9441–9453. http://dx.doi.org/10.1074/jbc.M111.284927.
  • Lin T, Greenberg MJ, Moore JR, Ostap EM. 2011. A hearing loss-associated myo1c mutation (R156W) decreases the myosin duty ratio and force sensitivity. Biochemistry 50:1831–1838. http://dx.doi.org/10.1021/bi1016777.
  • Hokanson DE, Ostap EM. 2006. Myo1c binds tightly and specifically to phosphatidylinositol 4,5-bisphosphate and inositol 1,4,5-trisphosphate. Proc Natl Acad Sci U S A 103:3118–3123. http://dx.doi.org/10.1073/pnas.0505685103.
  • Konarev PV, Volkov VV, Sokolova AV, Koch MHJ, Svergun DI. 2003. PRIMUS: a Windows PC-based system for small-angle scattering data analysis. J Appl Crystallogr 36:1277–1282. http://dx.doi.org/10.1107/S0021889803012779.
  • Svergun DI. 1992. Determination of the regularization parameter in indirect-transform methods using perceptual criteria. J Appl Crystallogr 25:495–503. http://dx.doi.org/10.1107/S0021889892001663.
  • Biasini M, Bienert S, Waterhouse A, Arnold K, Studer G, Schmidt T, Kiefer F, Gallo Cassarino T, Bertoni M, Bordoli L, Schwede T. 2014. SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information. Nucleic Acids Res 42:W252–W258. http://dx.doi.org/10.1093/nar/gku340.
  • Kozin MB, Svergun DI. 2001. Automated matching of high- and low-resolution structural models. J Appl Crystallogr 34:33–41. http://dx.doi.org/10.1107/S0021889800014126.
  • Pierce BG, Wiehe K, Hwang H, Kim BH, Vreven T, Weng Z. 2014. ZDOCK server: interactive docking prediction of protein-protein complexes and symmetric multimers. Bioinformatics 30:1771–1773. http://dx.doi.org/10.1093/bioinformatics/btu097.
  • McKenna JM, Ostap EM. 2009. Kinetics of the interaction of myo1c with phosphoinositides. J Biol Chem 284:28650–28659. http://dx.doi.org/10.1074/jbc.M109.049791.
  • Adamek N, Coluccio LM, Geeves MA. 2008. Calcium sensitivity of the cross-bridge cycle of Myo1c, the adaptation motor in the inner ear. Proc Natl Acad Sci U S A 105:5710–5715. http://dx.doi.org/10.1073/pnas.0710520105.
  • Bose A, Guilherme A, Robida SI, Nicoloro SM, Zhou QL, Jiang ZY, Pomerleau DP, Czech MP. 2002. Glucose transporter recycling in response to insulin is facilitated by myosin Myo1c. Nature 420:821–824. http://dx.doi.org/10.1038/nature01246.
  • Nakamori Y, Emoto M, Fukuda N, Taguchi A, Okuya S, Tajiri M, Miyagishi M, Taira K, Wada Y, Tanizawa Y. 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. http://dx.doi.org/10.1083/jcb.200601065.
  • Hagan GN, Lin Y, Magnuson MA, Avruch J, Czech MP. 2008. A Rictor-Myo1c complex participates in dynamic cortical actin events in 3T3-L1 adipocytes. Mol Cell Biol 28:4215–4226. http://dx.doi.org/10.1128/MCB.00867-07.
  • Huber TB, Benzing T. 2005. The slit diaphragm: a signaling platform to regulate podocyte function. Curr Opin Nephrol Hypertens 14:211–216. http://dx.doi.org/10.1097/01.mnh.0000165885.85803.a8.
  • Huber TB, Schmidts M, Gerke P, Schermer B, Zahn A, Hartleben B, Sellin L, Walz G, Benzing T. 2003. The carboxyl terminus of Neph family members binds to the PDZ domain protein zonula occludens-1. J Biol Chem 278:13417–13421. http://dx.doi.org/10.1074/jbc.C200678200.
  • Pyrpassopoulos S, Feeser EA, Mazerik JN, Tyska MJ, Ostap EM. 2012. Membrane-bound myo1c powers asymmetric motility of actin filaments. Curr Biol 22:1688–1692. http://dx.doi.org/10.1016/j.cub.2012.06.069.
  • Fan Y, Eswarappa SM, Hitomi M, Fox PL. 2012. Myo1c facilitates G-actin transport to the leading edge of migrating endothelial cells. J Cell Biol 198:47–55. http://dx.doi.org/10.1083/jcb.201111088.
  • Garg P, Verma R, Nihalani D, Johnstone DB, Holzman LB. 2007. Neph1 cooperates with nephrin to transduce a signal that induces actin polymerization. Mol Cell Biol 27:8698–8712. http://dx.doi.org/10.1128/MCB.00948-07.
  • Boguslavsky S, Chiu T, Foley KP, Osorio-Fuentealba C, Antonescu CN, Bayer KU, Bilan PJ, Klip A. 2012. Myo1c binding to submembrane actin mediates insulin-induced tethering of GLUT4 vesicles. Mol Biol Cell 23:4065–4078. http://dx.doi.org/10.1091/mbc.E12-04-0263.
  • Sugie A, Umetsu D, Yasugi T, Fischbach KF, Tabata T. 2010. Recognition of pre- and postsynaptic neurons via nephrin/NEPH1 homologs is a basis for the formation of the Drosophila retinotopic map. Development 137:3303–3313. http://dx.doi.org/10.1242/dev.047332.
  • Neumann-Haefelin E, Kramer-Zucker A, Slanchev K, Hartleben B, Noutsou F, Martin K, Wanner N, Ritter A, Godel M, Pagel P, Fu X, Muller A, Baumeister R, Walz G, Huber TB. 2010. A model organism approach: defining the role of Neph proteins as regulators of neuron and kidney morphogenesis. Hum Mol Genet 19:2347–2359. http://dx.doi.org/10.1093/hmg/ddq108.
  • Greenberg MJ, Lin T, Goldman YE, Shuman H, Ostap EM. 2012. Myosin IC generates power over a range of loads via a new tension-sensing mechanism. Proc Natl Acad Sci U S A 109:E2433–E2440. http://dx.doi.org/10.1073/pnas.1207811109.

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