Encyclopedia of Signaling Molecules

2018 Edition
| Editors: Sangdun Choi

Vimentin

  • Clarissa M. Koch
  • Karen M. Ridge
Reference work entry
DOI: https://doi.org/10.1007/978-3-319-67199-4_101951

Synonyms

 VIM

Historical Background

Intermediate filaments (IF) are a family of proteins that are an important cytoskeletal component. Vimentin is a Type III intermediate filament that is primarily found in mesenchymal cells. Initially, it was assumed that the IFs served purely as a structural entity to give cells their shape and maintain their integrity. Over the past two decades, numerous roles and functions of the vimentin protein have been uncovered such as cellular migration, adhesion, and signaling. Historically, vimentin has been used as a tumor marker (Kidd et al. 2014). Moreover, recent research has uncovered that the IF protein is involved in numerous aspects of cancer development such as metastasis and the epithelial-mesenchymal transition (EMT) (Mendez et al. 2010). Additionally, it has become clear in recent years that vimentin may also play a role in several other pathologies such as colitis (Mor-Vaknin et al. 2013), Crohn’s disease (Henderson et al. 2012), and...

This is a preview of subscription content, log in to check access.

References

  1. Byun Y, Chen F, Chang R, Trivedi M, Green KJ, Cryns VL. Caspase cleavage of vimentin disrupts intermediate filaments and promotes apoptosis. Cell Death Differ. 2001;8:443–50.  https://doi.org/10.1038/sj.cdd.4400840.CrossRefPubMedGoogle Scholar
  2. Chang L, Goldman RD. Intermediate filaments mediate cytoskeletal crosstalk. Nat Rev Mol Cell Biol. 2004;5:601–13.  https://doi.org/10.1038/nrm1438.CrossRefPubMedGoogle Scholar
  3. Cheng F, Shen Y, Mohanasundaram P, Lindstrom M, Ivaska J, Ny T, et al. Vimentin coordinates fibroblast proliferation and keratinocyte differentiation in wound healing via TGF-beta-slug signaling. Proc Natl Acad Sci USA. 2016;113:E4320–7.  https://doi.org/10.1073/pnas.1519197113.CrossRefPubMedPubMedCentralGoogle Scholar
  4. Chernoivanenko IS, Matveeva EA, Gelfand VI, Goldman RD, Minin AA. Mitochondrial membrane potential is regulated by vimentin intermediate filaments. FASEB J. 2015;29:820–7.  https://doi.org/10.1096/fj.14-259903.CrossRefPubMedGoogle Scholar
  5. Chernyatina AA, Nicolet S, Aebi U, Herrmann H, Strelkov SV. Atomic structure of the vimentin central alpha-helical domain and its implications for intermediate filament assembly. Proc Natl Acad Sci USA. 2012;109:13620–5.  https://doi.org/10.1073/pnas.1206836109.CrossRefPubMedPubMedCentralGoogle Scholar
  6. dos Santos G, Rogel MR, Baker MA, Troken JR, Urich D, Morales-Nebreda L, et al. Vimentin regulates activation of the NLRP3 inflammasome. Nat Commun. 2015;6:6574.  https://doi.org/10.1038/ncomms7574.CrossRefPubMedPubMedCentralGoogle Scholar
  7. Eckes B, Colucci-Guyon E, Smola H, Nodder S, Babinet C, Krieg T, et al. Impaired wound healing in embryonic and adult mice lacking vimentin. J Cell Sci. 2000;113(Pt 13):2455–62.PubMedGoogle Scholar
  8. Eriksson JE, He T, Trejo-Skalli AV, Harmala-Brasken AS, Hellman J, Chou YH, et al. Specific in vivo phosphorylation sites determine the assembly dynamics of vimentin intermediate filaments. J Cell Sci. 2004;117:919–32.  https://doi.org/10.1242/jcs.00906.CrossRefPubMedGoogle Scholar
  9. Goldman RD. The role of three cytoplasmic fibers in BHK-21 cell motility. I. Microtubules and the effects of colchicine. J Cell Biol. 1971;51:752–62.PubMedPubMedCentralCrossRefGoogle Scholar
  10. Goto H, Kosako H, Tanabe K, Yanagida M, Sakurai M, Amano M, et al. Phosphorylation of vimentin by Rho-associated kinase at a unique amino-terminal site that is specifically phosphorylated during cytokinesis. J Biol Chem. 1998;273:11728–36.CrossRefPubMedGoogle Scholar
  11. Goto H, Yasui Y, Kawajiri A, Nigg EA, Terada Y, Tatsuka M, et al. Aurora-B regulates the cleavage furrow-specific vimentin phosphorylation in the cytokinetic process. J Biol Chem. 2003;278:8526–30.  https://doi.org/10.1074/jbc.M210892200.CrossRefPubMedGoogle Scholar
  12. Gyoeva FK, Gelfand VI. Coalignment of vimentin intermediate filaments with microtubules depends on kinesin. Nature. 1991;353:445–8.  https://doi.org/10.1038/353445a0.CrossRefPubMedGoogle Scholar
  13. Henderson P, Wilson DC, Satsangi J, Stevens C. A role for vimentin in Crohn disease. Autophagy. 2012;8:1695–6.  https://doi.org/10.4161/auto.21690.CrossRefPubMedPubMedCentralGoogle Scholar
  14. Herrmann H, Haner M, Brettel M, Muller SA, Goldie KN, Fedtke B, et al. Structure and assembly properties of the intermediate filament protein vimentin: the role of its head, rod and tail domains. J Mol Biol. 1996;264:933–53.  https://doi.org/10.1006/jmbi.1996.0688.CrossRefPubMedGoogle Scholar
  15. Hookway C, Ding L, Davidson MW, Rappoport JZ, Danuser G, Gelfand VI. Microtubule-dependent transport and dynamics of vimentin intermediate filaments. Mol Biol Cell. 2015;26:1675–86.  https://doi.org/10.1091/mbc.E14-09-1398.CrossRefPubMedPubMedCentralGoogle Scholar
  16. Ivaska J, Vuoriluoto K, Huovinen T, Izawa I, Inagaki M, Parker PJ. PKCepsilon-mediated phosphorylation of vimentin controls integrin recycling and motility. EMBO J. 2005;24:3834–45.  https://doi.org/10.1038/sj.emboj.7600847.CrossRefPubMedPubMedCentralGoogle Scholar
  17. Ivaska J, Pallari HM, Nevo J, Eriksson JE. Novel functions of vimentin in cell adhesion, migration, and signaling. Exp Cell Res. 2007;313:2050–62.  https://doi.org/10.1016/j.yexcr.2007.03.040.CrossRefPubMedGoogle Scholar
  18. Kidd ME, Shumaker DK, Ridge KM. The role of vimentin intermediate filaments in the progression of lung cancer. Am J Respir Cell Mol Biol. 2014;50:1–6.  https://doi.org/10.1165/rcmb.2013-0314TR.CrossRefPubMedPubMedCentralGoogle Scholar
  19. Li QF, Spinelli AM, Wang R, Anfinogenova Y, Singer HA, Tang DD. Critical role of vimentin phosphorylation at Ser-56 by p21-activated kinase in vimentin cytoskeleton signaling. J Biol Chem. 2006;281:34716–24.  https://doi.org/10.1074/jbc.M607715200.CrossRefPubMedPubMedCentralGoogle Scholar
  20. Mendez MG, Kojima S, Goldman RD. Vimentin induces changes in cell shape, motility, and adhesion during the epithelial to mesenchymal transition. FASEB J. 2010;24:1838–51.  https://doi.org/10.1096/fj.09-151639.CrossRefPubMedPubMedCentralGoogle Scholar
  21. Mendez MG, Restle D, Janmey PA. Vimentin enhances cell elastic behavior and protects against compressive stress. Biophys J. 2014;107:314–23.  https://doi.org/10.1016/j.bpj.2014.04.050.CrossRefPubMedPubMedCentralGoogle Scholar
  22. Mor-Vaknin N, Legendre M, Yu Y, Serezani CH, Garg SK, Jatzek A, et al. Murine colitis is mediated by vimentin. Sci Rep. 2013;3:1045.  https://doi.org/10.1038/srep01045.CrossRefPubMedPubMedCentralGoogle Scholar
  23. Muller M, Bhattacharya SS, Moore T, Prescott Q, Wedig T, Herrmann H, et al. Dominant cataract formation in association with a vimentin assembly disrupting mutation. Hum Mol Genet. 2009;18:1052–7.  https://doi.org/10.1093/hmg/ddn440.CrossRefPubMedGoogle Scholar
  24. Nekrasova OE, Mendez MG, Chernoivanenko IS, Tyurin-Kuzmin PA, Kuczmarski ER, Gelfand VI, et al. Vimentin intermediate filaments modulate the motility of mitochondria. Mol Biol Cell. 2011;22:2282–9.  https://doi.org/10.1091/mbc.E10-09-0766.CrossRefPubMedPubMedCentralGoogle Scholar
  25. Nieminen M, Henttinen T, Merinen M, Marttila-Ichihara F, Eriksson JE, Jalkanen S. Vimentin function in lymphocyte adhesion and transcellular migration. Nat Cell Biol. 2006;8:156–62.  https://doi.org/10.1038/ncb1355.CrossRefPubMedGoogle Scholar
  26. Perez-Sala D, Oeste CL, Martinez AE, Carrasco MJ, Garzon B, Canada FJ. Vimentin filament organization and stress sensing depend on its single cysteine residue and zinc binding. Nat Commun. 2015;6:7287.  https://doi.org/10.1038/ncomms8287.CrossRefPubMedPubMedCentralGoogle Scholar
  27. Perreau J, Lilienbaum A, Vasseur M, Paulin D. Nucleotide sequence of the human vimentin gene and regulation of its transcription in tissues and cultured cells. Gene. 1988;62:7–16.CrossRefPubMedGoogle Scholar
  28. Robert A, Rossow MJ, Hookway C, Adam SA, Gelfand VI. Vimentin filament precursors exchange subunits in an ATP-dependent manner. Proc Natl Acad Sci USA. 2015;112:E3505–14.  https://doi.org/10.1073/pnas.1505303112.CrossRefPubMedPubMedCentralGoogle Scholar
  29. Rogel MR, Soni PN, Troken JR, Sitikov A, Trejo HE, Ridge KM. Vimentin is sufficient and required for wound repair and remodeling in alveolar epithelial cells. FASEB J. 2011;25:3873–83.  https://doi.org/10.1096/fj.10-170795.CrossRefPubMedPubMedCentralGoogle Scholar
  30. Schietke R, Brohl D, Wedig T, Mucke N, Herrmann H, Magin TM. Mutations in vimentin disrupt the cytoskeleton in fibroblasts and delay execution of apoptosis. Eur J Cell Biol. 2006;85:1–10.  https://doi.org/10.1016/j.ejcb.2005.09.019.CrossRefPubMedGoogle Scholar
  31. Sin WC, Chen XQ, Leung T, Lim L. RhoA-binding kinase alpha translocation is facilitated by the collapse of the vimentin intermediate filament network. Mol Cell Biol. 1998;18:6325–39.PubMedPubMedCentralCrossRefGoogle Scholar
  32. Stevens C, Henderson P, Nimmo ER, Soares DC, Dogan B, Simpson KW, et al. The intermediate filament protein, vimentin, is a regulator of NOD2 activity. Gut. 2013;62:695–707.  https://doi.org/10.1136/gutjnl-2011-301775.CrossRefPubMedGoogle Scholar
  33. Virtakoivu R, Mai A, Mattila E, De Franceschi N, Imanishi SY, Corthals G, et al. Vimentin-ERK signaling uncouples slug gene regulatory function. Cancer Res. 2015;75:2349–62.  https://doi.org/10.1158/0008-5472.CAN-14-2842.CrossRefPubMedGoogle Scholar
  34. Wang RC, Wei Y, An Z, Zou Z, Xiao G, Bhagat G, et al. Akt-mediated regulation of autophagy and tumorigenesis through Beclin 1 phosphorylation. Science. 2012;338:956–9.  https://doi.org/10.1126/science.1225967.CrossRefPubMedPubMedCentralGoogle Scholar
  35. Yamaguchi T, Goto H, Yokoyama T, Sillje H, Hanisch A, Uldschmid A, et al. Phosphorylation by Cdk1 induces Plk1-mediated vimentin phosphorylation during mitosis. J Cell Biol. 2005;171:431–6.  https://doi.org/10.1083/jcb.200504091.CrossRefPubMedPubMedCentralGoogle Scholar
  36. Zhu QS, Rosenblatt K, Huang KL, Lahat G, Brobey R, Bolshakov S, et al. Vimentin is a novel AKT1 target mediating motility and invasion. Oncogene. 2011;30:457–70.  https://doi.org/10.1038/onc.2010.421.CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG 2018

Authors and Affiliations

  1. 1.Division of Pulmonary and Critical CareNorthwestern UniversityChicagoUSA