Cell Entry of C3 Exoenzyme from Clostridium botulinum

  • Astrid Rohrbeck
  • Ingo JustEmail author
Part of the Current Topics in Microbiology and Immunology book series (CT MICROBIOLOGY, volume 406)


Clostridium botulinum C3 is the prototype of C3-like ADP-ribosyltransferases that selectively ADP-ribosylate the small GTP-binding proteins RhoA/B/C and inhibit their downstream signaling pathways. It is used as pharmacological tool to study cellular Rho functions. In addition, C3bot harbors a transferase-independent activity on neurons to promote axonal and dendritic growth and branching. Many bacterial protein toxins interact specifically with proteins and/or other membrane components at the surface of target cells. Binding enables access to the appropriate cellular compartment so that the knowledge of the receptor allows essential insight into the mechanism of these toxins. Unlike other bacterial protein toxins (such as the clostridial C1 and C2 toxins from C. botulinum), C3 exoenzyme is devoid of a binding and translocation domain, with which toxins usually initiate receptor-mediated endocytosis followed by access to the intact cell. To date, no specific mechanism for internalization of C3 exoenzyme has been identified. Recently, vimentin was identified as membranous C3-binding partner involved in binding and uptake of C3. Although vimentin is not detected in neurons, vimentin is re-expressed after damage in regenerating neurons. Reappearance of vimentin allows C3 to get access to lesioned neurons/axons to exhibit axonotrophic and dentritotrophic effects.


  1. Adolf A, Leondaritis G, Rohrbeck A, Eickholt BJ, Just I, Ahnert-Hilger G and Höltje M (2016) The intermediate filament protein vimentin is essential for axonotrophic effects of Clostridium botulinum C3 exoenzymeGoogle Scholar
  2. Aepfelbacher M, Essler M, Huber E, Sugai M, Weber PC (1997) Bacterial toxins block endothelial wound repair: evidence that Rho GTPases control cytoskeletal rearrangements in migrating endothelial cells. Arterioscler Thromb Vasc Biol 17:1623–1629. doi: 10.1161/01.ATV.17.9.1623 PubMedCrossRefGoogle Scholar
  3. Aggeler J, Seely K (1990) Cytoskeletal dynamics in rabbit synovial fibroblasts: I. Effects of acrylamide on intermediate filaments and microfilaments. Cell Motil Cytoskeleton 16:110–120PubMedCrossRefGoogle Scholar
  4. Ahnert-Hilger G, Höltje M, Grosse G, Pickert G, Mucke C, Nixdorf-Bergweiler B, Boquet P, Hofmann F, Just I (2004) Differential effects of Rho GTPases on axonal and dendritic development in hippocampal neurones. J Neurochem 90:9–18. doi: 10.1111/j.1471-4159.2004.02475.x PubMedCrossRefGoogle Scholar
  5. Aktories K, Braun U, Rösener S, Just I, Hall A (1989) The rho gene product expressed in E. coli is a substrate of botulinum ADP-ribosyltransferase C3. Biochem Biophys Res Commun 158:209–213PubMedCrossRefGoogle Scholar
  6. Aktories K, Just I (2005) Clostridial Rho-inhibiting protein toxins. Curr Top Microbiol Immunol 291:113–145PubMedGoogle Scholar
  7. Aktories K, Rösener S, Blaschke U, Chhatwal GS (1988) Botulinum ADP-ribosyltransferase C3 Purification of the enzyme and characterization of the ADP-ribosylation reaction in platelet membranes. Eur J Biochem 172:445–450PubMedCrossRefGoogle Scholar
  8. Albertinazzi C, Gilardelli D, Paris S, Longhi R, De Curtis I (1998) Overexpression of a neural-specific Rho family GTPase, cRac1B, selectively induces enhanced neuritogenesis and neurite branching in primary neurons. J Cell Biol 142:815–825. doi: 10.1083/jcb.142.3.815 PubMedPubMedCentralCrossRefGoogle Scholar
  9. Aullo P, Giry M, Olsnes S, Popoff MR, Kocks C, Boquet P (1993) A chimeric toxin to study the role of the 21 kDa GTP binding protein rho in the control of actin microfilament assembly. EMBO J 12:921–931PubMedPubMedCentralGoogle Scholar
  10. Babrak L, Danelishvili L, Rose SJ, Kornberg T, Bermudez LE (2015) The environment of “Mycobacterium avium subsp. hominissuis” microaggregates induces synthesis of small proteins associated with efficient infection of respiratory epithelial cells. Infect Immun 83:625–636. doi: 10.1128/IAI.02699-14 PubMedPubMedCentralCrossRefGoogle Scholar
  11. Bahl JMC, Jensen SS, Larsen MR, Heegaard NHH (2008) Characterization of the human cerebrospinal fluid phosphoproteome by titanium dioxide affinity chromatography and mass spectrometry. Anal Chem 80:6308–6316. doi: 10.1021/ac800835y PubMedCrossRefGoogle Scholar
  12. Barth H, Olenik C, Sehr P, Schmidt G, Aktories K, Meyer DK (1999) Neosynthesis and activation of Rho by Escherichia coli cytotoxic necrotizing factor (CNF1) reverse cytopathic effects of ADP-ribosylated Rho. J Biol Chem 274:27407–27414. doi: 10.1074/jbc.274.39.27407 PubMedCrossRefGoogle Scholar
  13. Barth H, Hofmann F, Olenik C, Just IAK (1998) The N-terminal part of the enzyme component (C2I) of the binary Clostridium botulinum C2 toxin interacts with the binding component C2II and functions as a carrier system for a Rho ADP-ribosylating C3-like fusion toxine. Infect Immun 66:1364–1369PubMedPubMedCentralGoogle Scholar
  14. Benlimame N, Le PU, Nabi IR (1998) Localization of autocrine motility factor receptor to caveolae and clathrin-independent internalization of its ligand to smooth endoplasmic reticulum. Mol Biol Cell 9:1773–1786PubMedPubMedCentralCrossRefGoogle Scholar
  15. Berg A, Zelano J, Pekna M, Wilhelmsson U, Pekny M, Cullheim S (2013) Axonal regeneration after sciatic nerve lesion is delayed but complete in GFAP- and vimentin-deficient mice. PLoS ONE. doi: 10.1371/journal.pone.0079395 Google Scholar
  16. Bhattacharya B, Noad RJ, Roy P (2007) Interaction between Bluetongue virus outer capsid protein VP2 and vimentin is necessary for virus egress. Virol J 4:7. doi: 10.1186/1743-422X-4-7 PubMedPubMedCentralCrossRefGoogle Scholar
  17. Bhattacharya R, Gonzalez AM, Debiase PJ, Trejo HE, Goldman RD, Flitney FW, Jones JCR (2009) Recruitment of vimentin to the cell surface by beta3 integrin and plectin mediates adhesion strength. J Cell Sci 122:1390–1400. doi: 10.1242/jcs.043042 PubMedPubMedCentralCrossRefGoogle Scholar
  18. Bonfiglio JJ, Inda C, Senin S, Maccarrone G, Refojo D, Giacomini D, Turck CW, Holsboer F, Arzt E, Silberstein S (2013) B-Raf and CRHR1 internalization mediate biphasic ERK1/2 activation by CRH in hippocampal HT22 Cells. Mol Endocrinol 27:491–510. doi: 10.1210/me.2012-1359 PubMedPubMedCentralCrossRefGoogle Scholar
  19. Boquet P, Munro P, Fiorentini C, Just I (1998) Toxins from anaerobic bacteria: specificity and molecular mechanisms of action. Curr Opin Microbiol 1:66–74. doi: 10.1016/S1369-5274(98)80144-6 PubMedCrossRefGoogle Scholar
  20. Bryant AE, Bayer CR, Huntington JD, Stevens DL (2006) Group A streptococcal myonecrosis: increased vimentin expression after skeletal-muscle injury mediates the binding of Streptococcus pyogenes. J Infect Dis 193:1685–1692. doi: 10.1086/504261 PubMedCrossRefGoogle Scholar
  21. Bucci C, Thomsen P, Nicoziani P, McCarthy J, van Deurs B (2000) Rab7: a key to lysosome biogenesis. Mol Biol Cell 11:467–480. doi: 10.1091/mbc.11.2.467 PubMedPubMedCentralCrossRefGoogle Scholar
  22. Burghoff S, Willberg W, Schrader J (2015) Identification of extracellularly phosphorylated membrane proteins. Proteomics 15(19):3310–3314. doi: 10.1002/pmic.201400595.
  23. Cebon J, Nicola N, Ward M, Gardner I, Dempsey P, Layton J, Duhrsen U, Burgess AW, Nice E, Morstyn G (1990) Granulocyte-macrophage colony stimulating factor from human lymphocytes. The effect of glycosylation on receptor binding and biological activity. J Biol Chem 265:4483–4491PubMedGoogle Scholar
  24. Chardin P, Boquet P, Madaule P, Popoff MR, Rubin EJ, Gill DM (1989) The mammalian G protein rhoC is ADP-ribosylated by Clostridium botulinum exoenzyme C3 and affects actin microfilaments in Vero cells. EMBO J 8:1087–1092PubMedPubMedCentralGoogle Scholar
  25. Chi F, Jong TD, Wang L, Ouyang Y, Wu C, Li W, Huang S-H (2010) Vimentin-mediated signalling is required for IbeA+ E. coli K1 invasion of human brain microvascular endothelial cells. Biochem J 427:79–90. doi: 10.1042/BJ20091097 PubMedCrossRefGoogle Scholar
  26. Chou YHGR (2000) Intermediate filaments on the move. J Cell Biol 150:F101–F106PubMedCrossRefGoogle Scholar
  27. Cogli L, Progida C, Bramato R, Bucci C (2013) Vimentin phosphorylation and assembly are regulated by the small GTPase Rab7a. Biochim Biophys Acta Mol Cell Res 1833:1283–1293. doi: 10.1016/j.bbamcr.2013.02.024 CrossRefGoogle Scholar
  28. Comer FI, Hart GW (2000) O-glycosylation of nuclear and cytosolic proteins. Dynamic interplay between O-GlcNAc and O-phosphate. J Biol Chem 275:29179–29182PubMedCrossRefGoogle Scholar
  29. Console S, Marty C, García-Echeverría C, Schwendener R, Ballmer-Hofer K (2003) Antennapedia and HIV transactivator of transcription (TAT) “protein transduction domains” promote endocytosis of high molecular weight cargo upon binding to cell surface glycosaminoglycans. J Biol Chem 278:35109–35114. doi: 10.1074/jbc.M301726200 PubMedCrossRefGoogle Scholar
  30. Damm EM, Pelkmans L, Kartenbeck J, Mezzacasa A, Kurzchalia T, Helenius A (2005) Clathrin- and caveolin-1-independent endocytosis: entry of simian virus 40 into cells devoid of caveolae. J Cell Biol 168:477–488. doi: 10.1083/jcb.200407113 PubMedPubMedCentralCrossRefGoogle Scholar
  31. Darling RJ, Kuchibhotla U, Glaesner W, Micanovic R, Witcher DR, Beals JM (2002) Glycosylation of erythropoietin affects receptor binding kinetics: role of electrostatic interactions. Biochemistry 41:14524–14531. doi: 10.1021/bi0265022 PubMedCrossRefGoogle Scholar
  32. Das S, Ravi V, Desai A (2011) Japanese encephalitis virus interacts with vimentin to facilitate its entry into porcine kidney cell line. Virus Res 160:404–408. doi: 10.1016/j.virusres.2011.06.001 PubMedCrossRefGoogle Scholar
  33. Dennis JW, Lau KS, Demetriou M, Nabi IR (2009) Adaptive regulation at the cell surface by N-glycosylation. Traffic 10:1569–1578PubMedCrossRefGoogle Scholar
  34. Dergham P, Ellezam B, Essagian C, Avedissian H, Lubell WD, McKerracher L (2002) Rho signaling pathway targeted to promote spinal cord repair. J Neurosci 22:6570–6577. doi:20026637Google Scholar
  35. Du N, Cong H, Tian H, Zhang H, Zhang W, Song L, Tien P (2014) Cell surface vimentin is an attachment receptor for enterovirus 71. J Virol 88:5816–5833. doi: 10.1128/JVI.03826-13 PubMedPubMedCentralCrossRefGoogle Scholar
  36. Dubey M, Hoda S, Chan WKH, Pimenta A, Ortiz DD, Shea TB (2004) Reexpression of vimentin in differentiated neuroblastoma cells enhances elongation of axonal neurites. J Neurosci Res 78:245–249. doi: 10.1002/jnr.20146 PubMedCrossRefGoogle Scholar
  37. Eckert BS (1985) Alteration of intermediate filament distribution in PtK1 cells by acrylamide. Eur J Cell Biol 37:169–174PubMedGoogle Scholar
  38. Ellezam B, Dubreuil C, Winton M, Loy L, Dergham P, Sellés-Navarro I, McKerracher L (2002) Inactivation of intracellular Rho to stimulate axon growth and regeneration. Prog Brain Res 371–380Google Scholar
  39. Eriksson JE, He T, Trejo-Skalli AV, Härmälä-Braskén A-S, Hellman J, Chou Y-H, Goldman RD (2004) Specific in vivo phosphorylation sites determine the assembly dynamics of vimentin intermediate filaments. J Cell Sci 117:919–932. doi: 10.1242/jcs.00906 PubMedCrossRefGoogle Scholar
  40. Fahrer J, Kuban J, Heine K, Rupps G, Kaiser E, Felder E, Benz R, Barth H (2010) Selective and specific internalization of clostridial C3 ADP-ribosyltransferases into macrophages and monocytes. Cell Microbiol 12:233–247PubMedCrossRefGoogle Scholar
  41. Faigle W, Colucci-Guyon E, Louvard D, Amigorena S, Galli T (2000) Vimentin filaments in fibroblasts are a reservoir for SNAP23, a component of the membrane fusion machinery. Mol Biol Cell 11:3485–3494PubMedPubMedCentralCrossRefGoogle Scholar
  42. Fawell S, Seery J, Daikh Y, Moore C, Chen LL, Pepinsky B, Barsoum J (1994) Tat-mediated delivery of heterologous proteins into cells. Proc Natl Acad Sci USA 91:664–668. doi: 10.1073/pnas.91.2.664 PubMedPubMedCentralCrossRefGoogle Scholar
  43. Fehlings MG, Theodore N, Harrop J, Maurais G, Kuntz C, Shaffrey CI, Kwon BK, Chapman J, Yee A, Tighe A, McKerracher L (2011) A phase I/IIa clinical trial of a recombinant Rho protein antagonist in acute spinal cord injury. J Neurotrauma 28:787–796. doi: 10.1089/neu.2011.1765 PubMedCrossRefGoogle Scholar
  44. Fensome A, Whatmore J, Morgan C, Jones D, Cockcroft S (1998) ADP-ribosylation factor and Rho proteins mediate fMLP-dependent activation of phospholipase D in human neutrophils. J Biol Chem 273:13157–13164PubMedCrossRefGoogle Scholar
  45. Frankel AD, Pabo CO (1988) Cellular uptake of the tat protein from human immunodeficiency virus. Cell 55:1189–1193. doi: 10.1016/0092-8674(88)90263-2 PubMedCrossRefGoogle Scholar
  46. Gallo G (2006) RhoA-kinase coordinates F-actin organization and myosin II activity during semaphorin-3A-induced axon retraction. J Cell Sci 119:3413–3423. doi: 10.1242/jcs.03084 PubMedPubMedCentralCrossRefGoogle Scholar
  47. Ganley IG, Carroll K, Bittova L, Pfeffer S (2004) Rab9 GTPase regulates late endosome size and requires effector interaction for its stability. Mol Biol Cell 15:5420–5430. doi: 10.1091/mbc.E04-08-0747 PubMedPubMedCentralCrossRefGoogle Scholar
  48. Gao YS, Sztul E (2001) A novel interaction of the Golgi complex with the vimentin intermediate filament cytoskeleton. J Cell Biol 152:877–893. doi: 10.1083/jcb.152.5.877 PubMedPubMedCentralCrossRefGoogle Scholar
  49. Genth H, Gerhard R, Maeda A, Amano M, Kaibuchi K, Aktories K, Just I (2003) Entrapment of Rho ADP-ribosylated by iC3 exoenzyme in the Rho-guanine nucleotide dissociation inhibitor-1 complex. J Biol Chem 278:28523–28527. doi: 10.1074/jbc.M301915200 PubMedCrossRefGoogle Scholar
  50. Glaser-Gabay L, Raiter A, Battler A, Hardy B (2011) Endothelial cell surface vimentin binding peptide induces angiogenesis under hypoxic/ischemic conditions. Microvasc Res 82:221–226PubMedCrossRefGoogle Scholar
  51. Graham ME, Kilby DM, Firth SM, Robinson PJ, Baxter RC (2007) The in vivo phosphorylation and glycosylation of human insulin-like growth factor-binding protein-5. Mol Cell Proteomics 6:1392–1405. doi: 10.1074/mcp.M700027-MCP200 PubMedCrossRefGoogle Scholar
  52. Gu J, Isaji T, Xu Q, Kariya Y, Gu W, Fukuda T, Du Y (2012) Potential roles of N-glycosylation in cell adhesion. Glycoconj J 29:599–607. doi: 10.1007/s10719-012-9386-1 PubMedCrossRefGoogle Scholar
  53. Guha A, Sriram V, Krishnan KS, Mayor S (2003) Shibire mutations reveal distinct dynamin-independent and -dependent endocytic pathways in primary cultures of Drosophila hemocytes. J Cell Sci 116:3373–3386PubMedCrossRefGoogle Scholar
  54. Hasegawa S, Hirashima N, Nakanishi M (2001) Microtubule involvement in the intracellular dynamics for gene transfection mediated by cationic liposomes. Gene Ther 8:1669–1673. doi: 10.1038/ PubMedCrossRefGoogle Scholar
  55. Helal MA, Khalifa S, Ahmed S (2013) Differential binding of latrunculins to G-actin: a molecular dynamics study. J Chem Inf Model 53:2369–2375. doi: 10.1021/ci400317j PubMedCrossRefGoogle Scholar
  56. Ho TTG, Merajver SD, Lapière CM, Nusgens BV, Deroanne CF (2008) RhoA-GDP regulates rhob protein stability potential involvement of RhoGDIα. J Biol Chem 283:21588–21598. doi: 10.1074/jbc.M710033200 PubMedCrossRefGoogle Scholar
  57. Höltje M, Djalali S, Hofmann F, Münster-Wandowski A, Hendrix S, Boato F, Dreger SC, Grosse G, Henneberger C, Grantyn R, Just I, Ahnert-Hilger G (2009) A 29-amino acid fragment of Clostridium botulinum C3 protein enhances neuronal outgrowth, connectivity, and reinnervation. FASEB J 23:1115–1126. doi: 10.1096/fj.08-116855 PubMedCrossRefGoogle Scholar
  58. Hookway C, Ding L, Davidson MW, Rappoport JZ, Danuser G, Gelfand V (2015) Microtubule-dependent transport and dynamics of vimentin intermediate filaments. Mol Biol Cell 26:1675–1686. doi: 10.1091/mbc.E14-09-1398 PubMedPubMedCentralCrossRefGoogle Scholar
  59. Hornbeck PV, Chabra I, Kornhauser JM, Skrzypek E, Zhang B (2004) PhosphoSite: a bioinformatics resource dedicated to physiological protein phosphorylation. Proteomics 4:1551–1561. doi: 10.1002/pmic.200300772 PubMedCrossRefGoogle Scholar
  60. Huelsenbeck J, Dreger SC, Gerhard R, Fritz G, Just I, Genth H (2007) Upregulation of the immediate early gene product RhoB by exoenzyme C3 from Clostridium limosum and toxin B from Clostridium difficile. Biochemistry 46:4923–4931. doi: 10.1021/bi602465z PubMedCrossRefGoogle Scholar
  61. Huelsenbeck SC, Rohrbeck A, Handreck A, Hellmich G, Kiaei E, Roettinger I, Grothe C, Just I, Haastert-Talini K (2012) C3 peptide promotes axonal regeneration and functional motor recovery after peripheral nerve injury. Neurotherapeutics 9:185–198. doi: 10.1007/s13311-011-0072-y PubMedCrossRefGoogle Scholar
  62. Hyder CL, Pallari H-M, Kochin V, Eriksson JE (2008) Providing cellular signposts—post-translational modifications of intermediate filaments. FEBS Lett 582:2140–2148. doi: 10.1016/j.febslet.2008.04.064 PubMedCrossRefGoogle Scholar
  63. Icenogle LM, Hengel SM, Coye LH, Streifel A, Collins CM, Goodlett DR, Moseley SL (2012) Molecular and biological characterization of streptococcal SpyA-mediated ADP-ribosylation of intermediate filament protein vimentin. J Biol Chem 287:21481–21491. doi: 10.1074/jbc.M112.370791 PubMedPubMedCentralCrossRefGoogle Scholar
  64. Inoue S, Sugai M, Murooka Y, Paik S-Y, Y-M H, Ohgai H, Suginaka H (1991) Molecular cloning and sequencing of the epidermal cell differentiation inhibitor gene from Staphylococcus aureus. Biochem Biophys Res Commun 174:459–464Google Scholar
  65. Ise H, Goto M, Komura K, Akaike T (2012) Engulfment and clearance of apoptotic cells based on a GlcNAc-binding lectin-like property of surface vimentin. Glycobiology 22:788–805. doi: 10.1093/glycob/cws052 PubMedCrossRefGoogle Scholar
  66. Jin Z, Strittmatter SM (1997) Rac1 mediates collapsin-1-induced growth cone collapse. J Neurosci 17:6256–6263PubMedGoogle Scholar
  67. Jobling MG, Holmes RK (2000) Identification of motifs in cholera toxin A1 polypeptide that are required for its interaction with human ADP-ribosylation factor 6 in a bacterial two-hybrid system. Proc Natl Acad Sci USA 97:14662–14667. doi: 10.1073/pnas.011442598 PubMedPubMedCentralCrossRefGoogle Scholar
  68. Just I, Boquet P (2000) Large clostridial cytotoxins as tools in cell biology. Curr Top Microbiol Immunol 250:97–107PubMedGoogle Scholar
  69. Just I, Rohrbeck A, Huelsenbeck SC, Hoeltje M (2011) Therapeutic effects of Clostridium botulinum C3 exoenzyme. Naunyn Schmiedebergs Arch Pharmacol 383:247–252. doi: 10.1007/s00210-010-0589-3 PubMedCrossRefGoogle Scholar
  70. Just I, Schallehns G, Menardll L, Didsburyll JR, Vandekerckhovell J, Van Dammeii J, Aktories K (1992) Purification and Characterization of an ADP-ribosyltransferase produced by Clostridium limosum. J Biol Chem 267:10274–10280PubMedGoogle Scholar
  71. Just I, Selzer J, Jung M, Van Damme J, Vandekerckhove J, Aktories K (1995) Rho-ADP-ribosylating exoenzyme from Bacillus cereus. Purification, characterization, and identification of the NAD-binding site. Biochemistry 34:334–340PubMedCrossRefGoogle Scholar
  72. Kim J-K, Fahad A-M, Shanmukhappa K, Kapil S (2006) Defining the cellular target(s) of porcine reproductive and respiratory syndrome virus blocking monoclonal antibody 7G10. J Virol 80:689–696. doi: 10.1128/JVI.80.2.689-696.2006 PubMedPubMedCentralCrossRefGoogle Scholar
  73. Kim S, Coulombe PA (2007) Intermediate filament scaffolds fulfill mechanical, organizational, and signaling functions in the cytoplasm. Genes Dev 21:1581–1597PubMedCrossRefGoogle Scholar
  74. Koch G, Norgauer J, Aktories K (1993) ADP-ribosylation of the GTP-binding protein Rho by Clostridium limosum exoenzyme affects basal, but not N-formyl-peptide-stimulated, actin polymerization in human myeloid leukaemic (HL60) cells.No Title. Biochem J 299:775–779CrossRefGoogle Scholar
  75. Koudelka KJ, Destito G, Plummer EM, Trauger SA, Siuzdak G, Manchester M (2009) Endothelial targeting of cowpea mosaic virus (CPMV) via surface vimentin. PLoS Pathog. doi: 10.1371/journal.ppat.1000417 PubMedPubMedCentralGoogle Scholar
  76. Kozma R, Sarner S, Ahmed S, Lim L (1997) Rho family GTPases and neuronal growth cone remodelling: relationship between increased complexity induced by Cdc42Hs, Rac1, and acetylcholine and collapse induced by RhoA and lysophosphatidic acid. Mol Cell Biol 17:1201–1211PubMedPubMedCentralCrossRefGoogle Scholar
  77. Krska D, Ravulapalli R, Fieldhouse RJ, Lugo MR Merrill AR (2014) C3larvin toxin, an ADP-ribosyltransferase from Paenibacillus larvae. J Biol Chem 290(3):1639–1653. doi: 10.1074/jbc.M114.589846
  78. Lang P, Guizani L, Vitté-Mony I, Stancou R, Dorseuil O, Gacon G, Bertoglio J (1992) ADP-ribosylation of the ras-related, GTP-binding protein RhoA inhibits lymphocyte-mediated cytotoxicity. J Biol Chem 267:11677–11680PubMedGoogle Scholar
  79. Laudanna C, Campbell JJ, Butcher EC (1996) Role of Rho in chemoattractant-activated leukocyte adhesion through integrins. Science (80) 271:981–983Google Scholar
  80. Lehmann M, Fournier a, Selles-Navarro I, Dergham P, Sebok a, Leclerc N, Tigyi G, McKerracher L (1999) Inactivation of Rho signaling pathway promotes CNS axon regeneration. J Neurosci 19:7537–7547Google Scholar
  81. Lillich M, Chen X, Weil T, Barth H, Fahrer J (2012) Streptavidin-conjugated C3 protein mediates the delivery of mono-biotinylated RNAse A into macrophages. Bioconjug Chem 23:1426–1436. doi: 10.1021/bc300041z PubMedCrossRefGoogle Scholar
  82. Loske P, Boato F, Hendrix S, Piepgras J, Just I, Ahnert-Hilger G, Höltje M (2012) Minimal essential length of Clostridium botulinum C3 peptides to enhance neuronal regenerative growth and connectivity in a non-enzymatic mode. J Neurochem 120:1084–1096. doi: 10.1111/j.1471-4159.2012.07657.x PubMedGoogle Scholar
  83. Mackay DJG, Esch F, Furthmayr H, Hall A (1997) Rho- and Rac-dependent assembly of focal adhesion complexes and actin filaments in permeabilized fibroblasts: an essential role for ezrin/radixin/moesin proteins. J Cell Biol 138:927–938. doi: 10.1083/jcb.138.4.927 PubMedPubMedCentralCrossRefGoogle Scholar
  84. Madden JC, Ruiz N, Caparon M, Louis S (2001) A functional equivalent of type III secretion in gram-positive bacteria. Cell 104:143–152PubMedCrossRefGoogle Scholar
  85. Mann DA, Frankel AD (1991) Endocytosis and targeting of exogenous HIV-1 Tat protein. EMBO J 10:1733–1739PubMedPubMedCentralGoogle Scholar
  86. Manning G, Whyte DB, Martinez R, Hunter T, Sudarsanam S (2002) The protein kinase complement of the human genome. Science 298:1912–1934. doi: 10.1126/science.1075762 PubMedCrossRefGoogle Scholar
  87. Martin A, Hofmann H-D, Kirsch M (2003) Glial reactivity in ciliary neurotrophic factor-deficient mice after optic nerve lesion. J Neurosci 23:5416–5424PubMedGoogle Scholar
  88. Marvaud JC, Stiles BG, Chenal A, Gillet D, Gibert M, Smith LA, Popoff MR (2002) Clostridium perfringens iota toxin: mapping of the Ia domain involved in docking with Ib and cellular internalization. J Biol Chem 277:43659–43666. doi: 10.1074/jbc.M207828200 PubMedCrossRefGoogle Scholar
  89. Massol RH, Larsen JE, Fujinaga Y, Lencer WI, Kirchhausen T (2004) Cholera toxin toxicity does not require functional Arf6- and dynamin-dependent endocytic pathways. Mol Biol Cell 15:3631–3641. doi: 10.1091/mbc.E04-04-0283 PubMedPubMedCentralCrossRefGoogle Scholar
  90. Mayor S, Pagano RE (2007) Pathways of clathrin-independent endocytosis. Nat Rev Mol Cell Biol 8:603–612. doi: 10.1038/nrm2216 PubMedCrossRefGoogle Scholar
  91. McKerracher L, Anderson KD (2013) Analysis of recruitment and outcomes in the phase I/IIa Cethrin clinical trial for acute spinal cord injury. J Neurotrauma 30:1795–1804. doi: 10.1089/neu.2013.2909 PubMedCrossRefGoogle Scholar
  92. Menzies BE, Kourteva I (1998) Internalization of Staphylococcus aureus by endothelial cells induces apoptosis. Infect Immun 66:5994–5998PubMedPubMedCentralGoogle Scholar
  93. Miller MS, Hertel L (2009) Onset of human cytomegalovirus replication in fibroblasts requires the presence of an intact vimentin cytoskeleton. J Virol 83:7015–7028. doi: 10.1128/JVI.00398-09 PubMedPubMedCentralCrossRefGoogle Scholar
  94. Mitra A, Satelli A, Xia X, Cutrera J, Mishra L, Li S (2015) Cell-surface Vimentin: a mislocalized protein for isolating csVimentin(+) CD133(−) novel stem-like hepatocellular carcinoma cells expressing EMT markers. Int J Cancer 137:491–496. doi: 10.1002/ijc.29382 PubMedCrossRefGoogle Scholar
  95. Miura Y, Kikuchi A, Musha T, Kuroda S, Yaku H, Sasaki T (1993) Regulation of morphology by rho p21 and its inhibitory GDP/GTP exchange protein (rho GDI) in Swiss 3T3 cells. J Biol Chem 268:510–515PubMedGoogle Scholar
  96. Moremen KW, Tiemeyer M, Nairn AV (2012) Vertebrate protein glycosylation: diversity, synthesis and function. Nat Rev Mol Cell Biol 13:448–462PubMedPubMedCentralCrossRefGoogle Scholar
  97. Mor-Vaknin N, Punturieri A, Sitwala K, Markovitz DM (2003) Vimentin is secreted by activated macrophages. Nat Cell Biol 5:59–63. doi: 10.1038/ncb898 PubMedCrossRefGoogle Scholar
  98. Murli S, Watson RO, Galán JE (2001) Role of tyrosine kinases and the tyrosine phosphatase SptP in the interaction of Salmonella with host cells. Cell Microbiol 3:795–810. doi: 10.1046/j.1462-5822.2001.00158.x PubMedCrossRefGoogle Scholar
  99. Nabi IR, Le PU (2003) Caveolae/raft-dependent endocytosis. J Cell Biol 161:673–677PubMedPubMedCentralCrossRefGoogle Scholar
  100. Nedellec P, Vicart P, Laurent-Winter C, Martinat C, Prevost MC, Brahic M (1998) Interaction of Theiler’s virus with intermediate filaments of infected cells. J Virol 72:9553–9560PubMedPubMedCentralGoogle Scholar
  101. Nichols BJ (2003) GM1-containing lipid rafts are depleted within clathrin-coated pits. Curr Biol 13:686–690. doi: 10.1016/S0960-9822(03)00209-4 PubMedCrossRefGoogle Scholar
  102. Nishida Y, Shibata K, Yamasaki M, Sato Y, Abe M (2009) A possible role of vimentin on the cell surface for the activation of latent transforming growth factor-beta. FEBS Lett 583:308–312. doi: 10.1016/j.febslet.2008.12.051 PubMedCrossRefGoogle Scholar
  103. Nishiki T, Narumiya S, Morii N, Yamamoto M, Fujiwara M, Kamata Y, Sakaguchi G, Kozaki S (1990) ADP-ribosylation of the rho rac proteins induces growth inhibition, neurite outgrowth and acetylcholine esterase in cultured PC-12 cells. Biochem Biophys Res Commun 167:265–272. doi: 10.1016/0006-291X(90)91760-P PubMedCrossRefGoogle Scholar
  104. Olson MF, Paterson HF, Marshall CJ (1998) Signals from Ras and Rho GTPases interact to regulate expression of p21Waf1/Cip1. Nature 394:295–299. doi: 10.1038/28425 PubMedCrossRefGoogle Scholar
  105. Orlandi PA, Fishman PH (1998) Filipin-dependent inhibition of cholera toxin: evidence for toxin internalization and activation through caveolae-like domains. J Cell Biol 141:905–915. doi: 10.1083/jcb.141.4.905 PubMedPubMedCentralCrossRefGoogle Scholar
  106. Park J, Kim J-S, Jung K-C, Lee H-J, Kim J-I, Kim J, Lee J-Y, Park J-B, Choi SY (2003) Exoenzyme Tat-C3 inhibits association of zymosan particles, phagocytosis, adhesion, and complement binding in macrophage cells. Mol Cells 16:216–223PubMedGoogle Scholar
  107. Parton RG (1994) Ultrastructural localization of gangliosides; GM1 is concentrated in caveolae. J Histochem Cytochem 42:155–166. doi: 10.1177/42.2.8288861 PubMedCrossRefGoogle Scholar
  108. Parton RG, Richards AA (2003) Lipid rafts and caveolae as portals for endocytosis: new insights and common mechanisms. Traffic 4:724–738. doi:128 [pii]Google Scholar
  109. Paterson HE, Self AJ, Garrett MD, Just I, Aktories K, Hall A (1990) Microinjection of recombinant p21rho induces rapid changes in cell morphology. J Cell Biol 11:1001–1007CrossRefGoogle Scholar
  110. Pautsch A, Vogelsgesang M, Tränkle J, Herrmann C, Aktories K (2005) Crystal structure of the C3bot-RalA complex reveals a novel type of action of a bacterial exoenzyme. EMBO J 24:3670–3680. doi: 10.1038/sj.emboj.7600813 PubMedPubMedCentralCrossRefGoogle Scholar
  111. Perlson E, Hanz S, Ben-Yaakov K, Segal-Ruder Y, Seger R, Fainzilber M (2005) Vimentin-dependent spatial translocation of an activated MAP kinase in injured nerve. Neuron 45:715–726. doi: 10.1016/j.neuron.2005.01.023 PubMedCrossRefGoogle Scholar
  112. Podor TJ, Singh D, Chindemi P, Foulon DM, McKelvie R, Weitz JI, Austin R, Boudreau G, Davies R (2002) Vimentin exposed on activated platelets and platelet microparticles localizes vitronectin and plasminogen activator inhibitor complexes on their surface. J Biol Chem 277:7529–7539. doi: 10.1074/jbc.M109675200 PubMedCrossRefGoogle Scholar
  113. Rho JH, Roehrl MH, Wang J (2009) Glycoproteomic analysis of human lung adenocarcinomas using glycoarrays and tandem mass spectrometry: differential expression and glycosylation patterns of vimentin and fetuin A isoforms. Protein J 28:148–160PubMedCrossRefGoogle Scholar
  114. Richard JP, Melikov K, Vives E, Ramos C, Verbeure B, Gait MJ, Chernomordik LV, Lebleu B (2003) Cell-penetrating peptides: a reevaluation of the mechanism of cllular uptake. J Biol Chem 278:585–590. doi: 10.1074/jbc.M209548200 PubMedCrossRefGoogle Scholar
  115. Ridley AJ, Hall A (1992) The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 70:389–399. doi: 10.1016/0962-8924(92)90173-K PubMedCrossRefGoogle Scholar
  116. Risco C, Rodríguez JR, López-Iglesias C, Carrascosa JL, Esteban M, Rodríguez D (2002) Endoplasmic reticulum-Golgi intermediate compartment membranes and vimentin filaments participate in vaccinia virus assembly. J Virol 76:1839–1855. doi: 10.1128/JVI.76.4.1839-1855.2002 PubMedPubMedCentralCrossRefGoogle Scholar
  117. Robert A, Hookway C, Gelfand V (2016) Intermediate filament dynamics: what we can see now and why it matters. BioEssays. doi: 10.1002/bies.201500142 PubMedCentralGoogle Scholar
  118. Robert A, Rossow MJ, Hookway C, Adam SA, Gelfand V (2015) Vimentin filament precursors exchange subunits in an ATP-dependent manner. Proc Natl Acad Sci USA 112:E3505–E3514. doi: 10.1073/pnas.1505303112 PubMedPubMedCentralCrossRefGoogle Scholar
  119. Rohrbeck A, Kolbe T, Hagemann S, Genth H, Just I (2012) Distinct biological activities of C3 and ADP-ribosyltransferase-deficient C3-E174Q. FEBS J 279:2657–2671. doi: 10.1111/j.1742-4658.2012.08645.x PubMedCrossRefGoogle Scholar
  120. Rohrbeck A, Schröder A, Hagemann S, Pich A, Höltje M, Ahnert-Hilger G, Just I (2014) Vimentin mediates uptake of C3 exoenzyme. PLoS ONE 9:e101071. doi: 10.1371/journal.pone.0101071 PubMedPubMedCentralCrossRefGoogle Scholar
  121. Rohrbeck A, von Elsner L, Hagemann S, Just I (2015) Uptake of Clostridium botulinum C3 exoenzyme into intact HT22 and J774A.1 cells. Toxins (Basel) 7:380–395CrossRefGoogle Scholar
  122. Rotsch J, Rohrbeck A, May M, Kolbe T, Hagemann S, Schelle I, Just I, Genth H, Huelsenbeck SC (2012) Inhibition of macrophage migration by C. botulinum exoenzyme C3. Naunyn Schmiedebergs Arch Pharmacol 385:883–890. doi: 10.1007/s00210-012-0764-9 PubMedCrossRefGoogle Scholar
  123. Rubin EJ, Gill DM, Boquet P, Popoff MR (1988) Functional modification of a 21-kilodalton G protein when ADP-ribosylated by exoenzyme C3 of Clostridium botulinum. Mol Cell Biol 8:418–426. doi: 10.1128/MCB.8.1.418.Updated PubMedPubMedCentralCrossRefGoogle Scholar
  124. Rusnati M, Tulipano G, Spillmann D, Tanghetti E, Oreste P, Zoppetti G, Giacca M, Presta M (1999) Multiple interactions of HIV-I Tat protein with size-defined heparin oligosaccharides. J Biol Chem 274:28198–28205. doi: 10.1074/jbc.274.40.28198 PubMedCrossRefGoogle Scholar
  125. Russo BC, Stamm LM, Raaben M, Kim CM, Kahoud E, Robinson LR, Bose S, Queiroz AL, Herrera BB, Baxt LA, Mor-Vaknin N, Fu Y, Molina G, Markovitz DM, SPW& MBG (2016) Intermediate filaments enable pathogen docking to trigger type 3 effector translocation. Nat Microbiol. doi: 10.1038/nmicrobiol.2016.25
  126. Sager PR (1989) Cytoskeletal effects of acrylamide and 2,5-hexanedione: selective aggregation of vimentin filaments. Toxicol Appl Pharmacol 97:141–155. doi: 10.1016/0041-008X(89)90063-X PubMedCrossRefGoogle Scholar
  127. Sahai E, Olson MF (2006) Purification of TAT-C3 exoenzyme. Methods Enzymol 406:128–140. doi: 10.1016/S0076-6879(06)06002-2 PubMedCrossRefGoogle Scholar
  128. Sánchez-San Martín C, López T, Arias CF, López S (2004) Characterization of rotavirus cell entry. J Virol 78:2310–2318. doi: 10.1128/JVI.78.5.2310-2318.2004 PubMedPubMedCentralCrossRefGoogle Scholar
  129. Sandvig K, Olsnes S, Petersen OW, Van Deurs B (1987) Acidification of the cytosol inhibits endocytosis from coated pits. J Cell Biol 105:679–689. doi: 10.1083/jcb.105.2.679 PubMedCrossRefGoogle Scholar
  130. Satelli A, Brownlee Z, Mitra A, Meng QH, Li S (2015) Circulating tumor cell enumeration with a combination of epithelial cell adhesion molecule- and cell-surface vimentin-based methods for monitoring breast cancer therapeutic response. Clin Chem 61:259–266. doi: 10.1373/clinchem PubMedCrossRefGoogle Scholar
  131. Schnitzer JE, Oh P, McIntosh DP (1996) Role of GTP hydrolysis in fission of caveolae directly from plasma membranes. Science 274:239–242. doi: 10.1126/science.274.5285.239 PubMedCrossRefGoogle Scholar
  132. Sebök Á, Nusser N, Debreceni B, Guo Z, Santos MF, Szeberenyi J, Tigyi G (1999) Different roles for RhoA during neurite initiation, elongation, and regeneration in PC12 cells. J Neurochem 73:949–960. doi: 10.1046/j.1471-4159.1999.0730949.x
  133. Sehr P, Joseph G, Genth H, Just I, Pick E, Aktories K (1998) Glucosylation and ADP ribosylation of Rho proteins: effects on nucleotide binding, GTPase activity, and effector coupling. Biochemistry 37:5296–5304. doi: 10.1021/bi972592c PubMedCrossRefGoogle Scholar
  134. Sekine A, Fujiwara M, Narumiya S (1989) Asparagine residue in the rho gene product is the modification site for botulinum ADP-ribosyltransferase. J Biol Chem 264:8602–8605PubMedGoogle Scholar
  135. Shime H, Ohnishi T, Nagao K, Oka K, Takao T, Horiguchi Y (2002) Association of Pasteurella multocida toxin with vimentin. Infect Immun 70:6460–6463. doi: 10.1128/IAI.70.11.6460-6463.2002 PubMedPubMedCentralCrossRefGoogle Scholar
  136. Slauson SR, Peters DM, Schwinn MK, Kaufman PL, Gabelt BT, Brandt C (2015) Viral vector effects on exoenzyme C3 transferase-mediated actin disruption and on outflow facility. Invest Ophthalmol Vis Sci 56:2431–2438. doi: 10.1167/iovs.14-15909 PubMedPubMedCentralCrossRefGoogle Scholar
  137. Stam JC, Michiels F, Van Der Kammen RA, Moolenaar WH, Collard JG (1998) Invasion of T-lymphoma cells: cooperation between Rho family GTPases and lysophospholipid receptor signaling. EMBO J 17:4066–4074. doi: 10.1093/emboj/17.14.4066 PubMedPubMedCentralCrossRefGoogle Scholar
  138. Steinmetz NF, Maurer J, Sheng H, Bensussan A, Maricic I et al (2011) Two domains of vimentin are expressed on the surface of lymph node, bone and brain metastatic prostate cancer lines along with the putative stem cell marker proteins CD44 and CD133. Cancers (Basel) 3:2870–2885PubMedCentralCrossRefGoogle Scholar
  139. Styers ML, Kowalczyk AP, Faundez V (2005) Intemediate filaments and vesicular membrane traffic: the odd couple’s first dance? Traffic 6:359–365PubMedCrossRefGoogle Scholar
  140. Styers ML, Salazar G, Love R, Peden AA, Kowalczyk AP, Faundez V (2004) The endo-lysosomal sorting machinery interacts with the intermediate filament cytoskeleton. Mol Biol Cell 15:5369–5382. doi: 10.1091/mbc.E04-03-0272 PubMedPubMedCentralCrossRefGoogle Scholar
  141. Suzuki T, Futaki S, Niwa M, Tanaka S, Ueda K, Sugiura Y (2002) Possible existence of common internalization mechanisms among arginine-rich peptides. J Biol Chem 277:2437–2443. doi: 10.1074/jbc.M110017200 PubMedCrossRefGoogle Scholar
  142. Tagliabracci VS, Wiley SE, Guo X, Kinch LN, Durrant E, Wen J, Xiao J, Cui J, Nguyen KB, Engel JL, Coon JJ, Grishin N, Pinna LA, Pagliarini DJ (2015) A single kinase generates the majority of the secreted phosphoproteome. Cell 161:1619–1632PubMedPubMedCentralCrossRefGoogle Scholar
  143. Takano T, Sawai C, Takeuchi Y (2004) Radial and tangential neuronal migration disorder in ibotenate-induced cortical lesions in hamsters: immunohistochemical study of reelin, vimentin, and calretinin. J Child Neurol 19:107–115PubMedCrossRefGoogle Scholar
  144. Tan EYM, Law JWS, Wang CH, Lee AYW (2007) Development of a cell transducible RhoA inhibitor TAT-C3 transferase and its encapsulation in biocompatible microspheres to promote survival and enhance regeneration of severed neurons. Pharm Res 24:2297–2308. doi: 10.1007/s11095-007-9454-6 PubMedCrossRefGoogle Scholar
  145. Teixeira AAR, de Cássia Veronica, de Vasconcelos Sardinha, Colli W, Alves MJM, Giordano R (2015) Trypanosoma cruzi binds to cytokeratin through conserved peptide motifs found in the laminin-G-like domain of the gp85/Trans-sialidase proteins. PloS PNTD 9:1–22. doi: 10.1371/journal.pntd.0004099 Google Scholar
  146. Thomas EK, Connelly RJ, Pennathur S, Dubrovsky L, Haffar OK, Bukrinsky MI (1996) Anti-idiotypic antibody to the V3 domain of gp120 binds to vimentin: a possible role of intermediate filaments in the early steps of HIV-1 infection cycle. Viral Immunol 9:73–87. doi: 10.1089/vim.1996.9.73 PubMedCrossRefGoogle Scholar
  147. Tokman MG, Porter RA, Williams CL (1997) Regulation of cadherin-mediated adhesion by the small GTP-binding protein Rho in small cell lung carcinoma cells. Cancer Res 57:1785–1793PubMedGoogle Scholar
  148. Torgersen ML, Skretting G, van Deurs B, Sandvig K (2001) Internalization of cholera toxin by different endocytic mechanisms. J Cell Sci 114:3737–3747PubMedGoogle Scholar
  149. van Deurs B, Holm PK, Sandvig K, Hansen SH (1993) Are caveolae involved in clathrin-independent endocytosis? Trends Cell Biol 3:249–251. doi: 10.1016/0962-8924(93)90045-3 PubMedCrossRefGoogle Scholar
  150. Van Hamme E, Dewerchin HL, Cornelissen E, Verhasselt B, Nauwynck HJ (2008) Clathrin- and caveolae-independent entry of feline infectious peritonitis virus in monocytes depends on dynamin. J Gen Virol 89:2147–2158. doi: 10.1099/vir.0.2008/001602-0 PubMedCrossRefGoogle Scholar
  151. Vogelsgesang M, Pautsch A, Aktories K (2007) C3 exoenzymes, novel insights into structure and action of Rho-ADP-ribosylating toxins. Naunyn Schmiedebergs Arch Pharmacol 374:347–360. doi: 10.1007/s00210-006-0113-y PubMedCrossRefGoogle Scholar
  152. Wahl S, Barth H, Ciossek T, Aktories K, Mueller BK (2000) Ephrin-A5 induces collapse of growth cones by activating Rho and Rho kinase. J Cell Biol 149:263–270. doi: 10.1083/jcb.149.2.263 PubMedPubMedCentralCrossRefGoogle Scholar
  153. Walter M, Chen FW, Tamari F, Wang R, Ioannou YA (2009) Endosomal lipid accumulation in NPC1 leads to inhibition of PKC, hypophosphorylation of vimentin and Rab9 entrapment. Biol Cell 101:141–152. doi: 10.1042/BC20070171 PubMedCrossRefGoogle Scholar
  154. Wang LH, Rothberg KG, Anderson RGW (1993) Mis-assembly of clathrin lattices on endosomes reveals a regulatory switch for coated pit formation. J Cell Biol 123:1107–1117. doi: 10.1083/jcb.123.5.1107 PubMedCrossRefGoogle Scholar
  155. Wang Z, Pandey A, Hart GW (2007) Dynamic interplay between O-linked N-acetylglucosaminylation and glycogen synthase kinase-3-dependent phosphorylation. Mol Cell Proteomics 6:1365–1379. doi: 10.1074/mcp.M600453-MCP200 PubMedCrossRefGoogle Scholar
  156. Wiegers W, Just I, Müller H, Hellwig A, Traub P, Aktories K (1991) Alteration of the cytoskeleton of mammalian cells cultured in vitro by Clostridium botulinum C2 toxin and C3 ADP-ribosyltransferase. Eur J Cell Biol 54:237–245PubMedGoogle Scholar
  157. Wilde C, Barth H, Sehr P, Han L, Schmidt M, Just I, Aktories K (2002) Interaction of the Rho-ADP-ribosylating C3 exoenzyme with RalA. J Biol Chem 277:14771–14776. doi: 10.1074/jbc.M201072200 PubMedCrossRefGoogle Scholar
  158. Wilde C, Chhatwal GS, Schmalzing G, Aktories K, Just I (2001) A novel C3-like ADP-ribosyltransferase from Staphylococcus aureus modifying RhoE and Rnd3. J Biol Chem 276:9537–9542. doi: 10.1074/jbc.M011035200 PubMedCrossRefGoogle Scholar
  159. Winton MJ, Dubreuil CI, Lasko D, Leclerc N, McKerracher L (2002) Characterization of new cell permeable C3-like proteins that inactivate Rho and stimulate neurite outgrowth on inhibitory substrates. J Biol Chem 277:32820–32829. doi: 10.1074/jbc.M201195200 PubMedCrossRefGoogle Scholar
  160. Yalak G, Vogel V (2012) Extracellular phosphorylation and phosphorylated proteins: not just curiosities but physiologically important. Sci Signal 5:re7. doi: 10.1126/scisignal.2003273
  161. Yoon M, Moir RD, Prahlad V, Goldman RD (1998) Motile properties of vimentin intermediate filament networks in living cells. J Cell Biol 143:147–157. doi: 10.1083/jcb.143.1.147 PubMedPubMedCentralCrossRefGoogle Scholar
  162. Yu YT, Chien SC, Chen IY, Lai CT, Tsay YG, Chang SC, Chang M (2016) Surface vimentin is critical for the cell entry of SARS-CoV. J Biomed Sci. doi: 10.1186/s12929-016-0234-7 Google Scholar
  163. Zhou W, Ross MM, Tessitore A, Ornstein D, VanMeter A, Liotta LA, Petricoin EF (2009) An initial characterization of the serum phosphoproteome. J Proteome Res 8:5523–5531. doi: 10.1021/pr900603n PubMedPubMedCentralCrossRefGoogle Scholar
  164. Zou Y, He L, Huang SH (2006) Identification of a surface protein on human brain microvascular endothelial cells as vimentin interacting with Escherichia coli invasion protein IbeA. Biochem Biophys Res Commun 351:625–630. doi: 10.1016/j.bbrc.2006.10.091 PubMedCrossRefGoogle Scholar

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© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Department of Pharmacology and ToxicologyHannover Medical SchoolHannoverGermany

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