Advertisement

Joining actions: crosstalk between intermediate filaments and actin orchestrates cellular physical dynamics and signaling

  • Jian Li
  • Yun Zou
  • Zhifang Li
  • Yaming JiuEmail author
Review
  • 7 Downloads

Abstract

Many key cellular functions are regulated by the interplay of three distinct cytoskeletal networks, made of actin filaments, microtubules, and intermediate filaments (IFs), which is a hitherto poorly investigated area of research. However, there are growing evidence in the last few years showing that the IFs cooperate with actin filaments to exhibit strongly coupled functions. This review recapitulates our current knowledge on how the crosstalk between IFs and actin filaments modulates the migration properties, mechano-responsiveness and signaling transduction of cells, from both biophysical and biochemical point of view.

intermediate filaments actin cytoskeletal interaction cell migration signaling pathway cell mechanosensing 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Notes

Acknowledgements

This work was supported by Collaborative Research Grant (KLMVI-OP-201904) of CAS Key Laboratory of Molecular Virology & Immunology, Institut Pasteur of Shanghai, Chinese Academy of Sciences, and the starting grant of Institut Pasteur of Shanghai (1185170000), Chinese Academy of Sciences.

References

  1. Buxboim, A., Swift, J., Irianto, J., Spinler, K.R., Dingal, P.C.D.P., Athirasala, A., Kao, Y.R.C., Cho, S., Harada, T., Shin, J.W., et al. (2014). Matrix elasticity regulates lamin-A,C phosphorylation and turnover with feedback to actomyosin. Curr Biol 24, 1909–1917.CrossRefGoogle Scholar
  2. Chang, L., and Goldman, R.D. (2004). Intermediate filaments mediate cytoskeletal crosstalk. Nat Rev Mol Cell Biol 5, 601–613.CrossRefGoogle Scholar
  3. Cheng, F., and Eriksson, J.E. Intermediate filaments and the regulation of cell motility during regeneration and wound healing. Cold Spring HarbRespect Biol 2017, 9.Google Scholar
  4. Cleary, R.A., Wang, R., Waqar, O., Singer, H.A., and Tang, D.D. (2014). Role of c-Abl tyrosine kinase in smooth muscle cell migration. Am J Physiol Cell Physiol 306, C753–C761.CrossRefGoogle Scholar
  5. De Pascalis, C., Pérez-González, C., Seetharaman, S., Boëda, B., Vianay, B., Burute, M., Leduc, C., Borghi, N., Trepat, X., and Etienne-Manneville, S. (2018). Intermediate filaments control collective migration by restricting traction forces and sustaining cell-cell contacts. J Cell Biol 217, 3031–3044.CrossRefGoogle Scholar
  6. Deng, M., Mohanan, S., Polyak, E., and Chacko, S. (2007). Caldesmon is necessary for maintaining the actin and intermediate filaments in cultured bladder smooth muscle cells. Cell Motil Cytoskel 64, 951–965.CrossRefGoogle Scholar
  7. Dupin, I., Camand, E., and Etienne-Manneville, S. (2009). Classical cadherins control nucleus and centrosome position and cell polarity. J Cell Biol 185, 779–786.CrossRefGoogle Scholar
  8. Dupin, I., Sakamoto, Y., and Etienne-Manneville, S. (2011). Cytoplasmic intermediate filaments mediate actin-driven positioning of the nucleus. J Cell Sci 124, 865–872.CrossRefGoogle Scholar
  9. Eckes, B., Dogic, D., Colucci-Guyon, E., Wang, N., Maniotis, A., Ingber, D., Merckling, A., Langa, F., Aumailley, M., Delouvee, A., Koteliansky, V., Babinet, C., and Krieg, T. (1998). Impaired mechanical stability, migration and contractile capacity in vimentin-deficient fibroblasts. J Cell Sci 111(Pt 13), 1897–1907.Google Scholar
  10. Esue, O., Carson, A.A., Tseng, Y., and Wirtz, D. (2006). A direct interaction between actin and vimentin filaments mediated by the tail domain of vimentin. J Biol Chem 281, 30393–30399.CrossRefGoogle Scholar
  11. Etienne-Manneville, S. (2018). Cytoplasmic intermediate filaments in cell biology. Ann Rev Cell Dev Biol 34, 1–28.CrossRefGoogle Scholar
  12. Folker, E.S., Ostlund, C., Luxton, G.W., Worman, H.J., and Gundersen, G. G. (2011). Lamin A variants that cause striated muscle disease are defective in anchoring transmembrane actin-associated nuclear lines for nuclear movement. Proc Natl Acad Sci USA 108, 131–136.CrossRefGoogle Scholar
  13. Fujiwara, S., Ohashi, K., Mashiko, T., Kondo, H., and Mizuno, K. (2016). Interplay between Solo and keratin filaments is crucial for mechanical force-induced stress fiber reinforcement. Mol Biol Cell 27, 954–966.CrossRefGoogle Scholar
  14. Gan, Z., Ding, L., Burckhardt, C.J., Lowery, J., Zaritsky, A., Sitterley, K., Mota, A., Costigliola, N., Starker, C.G., Voytas, D.F., et al. (2016). Vimentin intermediate filaments template microtubule networks to enhance persistence in cell polarity and directed migration. Cell Syst 3, 500–501.CrossRefGoogle Scholar
  15. Gerashchenko, M.V., Chernoivanenko, I.S., Moldaver, M.V., and Minin, A. A. (2009). Dynein is a motor for nuclear rotation while vimentin IFs is a “brake”. Cell Biol Int 33, 1057–1064.CrossRefGoogle Scholar
  16. Green, K.J., Talian, J.C., and Goldman, R.D. (1986). Relationship between intermediate filaments and microfilaments in cultured fibroblasts: evidence for common foci during cell spreading. Cell Motil Cytoskel 6, 406–418.CrossRefGoogle Scholar
  17. Green, K.J., Geiger, B., Jones, J.C., Talian, J.C., and Goldman, R.D. (1987). The relationship between intermediate filaments and microfilaments before and during the formation of desmosomes and adherens-type junctions in mouse epidermal keratinocytes. J Cell Biol 104, 1389–1402.CrossRefGoogle Scholar
  18. Gregor, M., Osmanagic-Myers, S., Burgstaller, G., Wolfram, M., Fischer, I., Walko, G., Resch, G.P., Jörgl, A., Herrmann, H., and Wiche, G. (2014). Mechanosensing through focal adhesion-anchored intermediate filaments. FASEB J 28, 715–729.CrossRefGoogle Scholar
  19. Gyoeva, F.K., and Gelfand, V.I. (1991). Coalignment of vimentin intermediate filaments with microtubules depends on kinesin. Nature 353, 445–448.CrossRefGoogle Scholar
  20. Havel, L.S., Kline, E.R., Salgueiro, A.M., and Marcus, A.I. (2015). Vimentin regulates lung cancer cell adhesion through a VAV2-Rac1 pathway to control focal adhesion kinase activity. Oncogene 34, 1979–1990.CrossRefGoogle Scholar
  21. Helfand, B.T., Chang, L., and Goldman, R.D. (2004). Intermediate filaments are dynamic and motile elements of cellular architecture. J Cell Sci 117, 133–141.CrossRefGoogle Scholar
  22. Helfand, B.T., Mendez, M.G., Murthy, S.N.P., Shumaker, D.K., Grin, B., Mahammad, S., Aebi, U., Wedig, T., Wu, Y.I., Hahn, K.M., et al. (2011). Vimentin organization modulates the formation of lamellipodia. Mol Biol Cell 22, 1274–1289.CrossRefGoogle Scholar
  23. Helfand, B.T., Mikami, A., Vallee, R.B., and Goldman, R.D. (2002). A requirement for cytoplasmic dynein and dynactin in intermediate filament network assembly and organization. J Cell Biol 157, 795–806.CrossRefGoogle Scholar
  24. Hesse, M., Magin, T.M., and Weber, K. (2001). Genes for intermediate filament proteins and the draft sequence of the human genome: novel keratin genes and a surprisingly high number of pseudogenes related to keratin genes 8 and 18. J Cell Sci 114, 2569–2575.Google Scholar
  25. Holaska, J.M., Kowalski, A.K., and Wilson, K.L. (2004). Emerin caps the pointed end of actin filaments: evidence for an actin cortical network at the nuclear inner membrane. PLoS Biol 2, e231.CrossRefGoogle Scholar
  26. Ivaska, J., Pallari, H.M., Nevo, J., and Eriksson, J.E. (2007). Novel functions of vimentin in cell adhesion, migration, and signaling. Exp Cell Res 313, 2050–2062.CrossRefGoogle Scholar
  27. Janmey, P.A., Euteneuer, U., Traub, P., and Schliwa, M. (1991). Viscoelastic properties of vimentin compared with other filamentous biopolymer networks. J Cell Biol 113, 155–160.CrossRefGoogle Scholar
  28. Jiu, Y., Lehtimäki, J., Tojkander, S., Cheng, F., Jäälinoja, H., Liu, X., Varjosalo, M., Eriksson, J.E., and Lappalainen, P. (2015). Bidirectional interplay between vimentin intermediate filaments and contractile actin stress fibers. Cell Rep 11, 1511–1518.CrossRefGoogle Scholar
  29. Jiu, Y., Peränen, J., Schaible, N., Cheng, F., Eriksson, J.E., Krishnan, R., and Lappalainen, P. (2017). Vimentin intermediate filaments control actin stress fiber assembly through GEF-H1 and RhoA. J Cell Sci 130, 892–902.CrossRefGoogle Scholar
  30. Lanier, M.H., Kim, T., and Cooper, J.A. (2015). CARMIL2 is a novel molecular connection between vimentin and actin essential for cell migration and invadopodia formation. Mol Biol Cell 26, 4577–4588.CrossRefGoogle Scholar
  31. Leduc, C., and Etienne-Manneville, S. (2015). Intermediate filaments in cell migration and invasion: the unusual suspects. Curr Opin Cell Biol 32, 102–112.CrossRefGoogle Scholar
  32. Li, J., Wang, R., Gannon, O.J., Rezey, A.C., Jiang, S., Gerlach, B.D., Liao, G., and Tang, D.D. (2016). Polo-like kinase 1 regulates vimentin phosphorylation at Ser-56 and contraction in smooth muscle. J Biol Chem 291, 23693–23703.CrossRefGoogle Scholar
  33. Li, Q.F., Spinelli, A.M., Wang, R., Anfinogenova, Y., Singer, H.A., and Tang, D.D. (2006). Critical role of vimentin phosphorylation at Ser-56 by p21-activated kinase in vimentin cytoskeleton signaling. J Biol Chem 281, 34716–34724.CrossRefGoogle Scholar
  34. Liao, G., and Gundersen, G.G. (1998). Kinesin is a candidate for crossbridging microtubules and intermediate filaments. Selective binding of kinesin to detyrosinated tubulin and vimentin. J Biol Chem 273, 9797–9803.CrossRefGoogle Scholar
  35. Liovic, M., Mogensen, M.M., and Prescott, A.R., Lane, E.B., (2003). Observation of keratin particles showing fast bidirectional movement colocalized with microtubules. J Cell Sci 116, 1417–1427.CrossRefGoogle Scholar
  36. Lobrinus, J.A., Janzer, R.C., Kuntzer, T., Matthieu, J.M., Pfend, G., Goy, J. J., and Bogousslavsky, J. (1998). Familial cardiomyopathy and distal myopathy with abnormal desmin accumulation and migration. Neuromusc Dis 8, 77–86.CrossRefGoogle Scholar
  37. Luxton, G.W.G., Gomes, E.R., Folker, E.S., Vintinner, E., and Gundersen, G.G. (2010). Linear arrays of nuclear envelope proteins harness retrograde actin flow for nuclear movement. Science 329, 956–959.CrossRefGoogle Scholar
  38. Mendez, M.G., Restle, D., and Janmey, P.A. (2014). Vimentin enhances cell elastic behavior and protects against compressive stress. Biophys J 107, 314–323.CrossRefGoogle Scholar
  39. Osmanagic-Myers, S., Dechat, T., and Foisner, R. (2015). Lamins at the crossroads of mechanosignaling. Genes Dev 29, 225–237.CrossRefGoogle Scholar
  40. Pallari, H.M., and Eriksson, J.E. (2006). Intermediate filaments as signaling platforms. Sci STKE 2006, pe53.CrossRefGoogle Scholar
  41. Pollard, T.D., and Borisy, G.G. (2003). Cellular motility driven by assembly and disassembly of actin filaments. Cell 112, 453–465.CrossRefGoogle Scholar
  42. Prahlad, V., Yoon, M., Moir, R.D., Vale, R.D., and Goldman, R.D. (1998). Rapid movements of vimentin on microtubule tracks: kinesin-dependent assembly of intermediate filament networks. J Cell Biol 143, 159–170.CrossRefGoogle Scholar
  43. Rao, M.V., Engle, L.J., Mohan, P.S., Yuan, A., Qiu, D., Cataldo, A., Hassinger, L., Jacobsen, S., Lee, V.M.Y., Andreadis, A., et al. (2002). Myosin Va binding to neurofilaments is essential for correct myosin Va distribution and transport and neurofilament density. J Cell Biol 159, 279–290.CrossRefGoogle Scholar
  44. Sharma, P., Bolten, Z.T., Wagner, D.R., and Hsieh, A.H. (2017). Deformability of human mesenchymal stem cells is dependent on vimentin intermediate filaments. Ann Biomed Eng 45, 1365–1374.CrossRefGoogle Scholar
  45. Sjuve, R., Arner, A., Li, Z., Mies, B., Paulin, D., Schmittner, M., and Small, J.V. (1998). Mechanical alterations in smooth muscle from mice lacking desmin. J Musc Res Cell Motil 19, 415–429.CrossRefGoogle Scholar
  46. Sullivan, T., Escalante-Alcalde, D., Bhatt, H., Anver, M., Bhat, N., Nagashima, K., Stewart, C.L., and Burke, B. (1999). Loss of A-type lamin expression compromises nuclear envelope integrity leading to muscular dystrophy. J Cell Biol 147, 913–920.CrossRefGoogle Scholar
  47. Swift, J., Ivanovska, I.L., Buxboim, A., Harada, T., Dingal, P.C.D.P., Pinter, J., Pajerowski, J.D., Spinler, K.R., Shin, J.W., Tewari, M., et al. (2013). Nuclear lamin-A scales with tissue stiffness and enhances matrix-directed differentiation. Science 341, 1240104.CrossRefGoogle Scholar
  48. Szeverenyi, I., Cassidy, A.J., Chung, C.W., Lee, B.T.K., Common, J.E.A., Ogg, S.C., Chen, H., Sim, S.Y., Goh, W.L.P., Ng, K.W., et al. (2008). The Human Intermediate Filament Database: comprehensive information on a gene family involved in many human diseases. Hum Mutat 29, 351–360.CrossRefGoogle Scholar
  49. Tang, D.D. (2008). Intermediate filaments in smooth muscle. Am J Physiol Cell Physiol 294, C869–C878.CrossRefGoogle Scholar
  50. Tang, D.D., and Anfinogenova, Y. (2008). Physiologic properties and regulation of the actin cytoskeleton in vascular smooth muscle. J Cardiovasc Pharmacol Ther 13, 130–140.CrossRefGoogle Scholar
  51. Tang, D.D. (2009). p130 Crk-associated substrate (CAS) in vascular smooth muscle. J Cardiovasc Pharmacol Ther 14, 89–98.CrossRefGoogle Scholar
  52. Tang, D.D. (2015). Critical role of actin-associated proteins in smooth muscle contraction, cell proliferation, airway hyperresponsiveness and airway remodeling. Respir Res 16, 134.CrossRefGoogle Scholar
  53. Tang, D.D., and Gerlach, B.D. (2017). The roles and regulation of the actin cytoskeleton, intermediate filaments and microtubules in smooth muscle cell migration. Respir Res 18, 54.CrossRefGoogle Scholar
  54. Wang, R., Li, Q., and Tang, D.D. (2006). Role of vimentin in smooth muscle force development. Am J Physiol Cell Physiol 291, C483–C489.CrossRefGoogle Scholar
  55. Wang, R., Li, Q.F., Anfinogenova, Y., and Tang, D.D. (2007). Dissociation of Crk-associated substrate from the vimentin network is regulated by p21-activated kinase on ACh activation of airway smooth muscle. Am J Physiol Lung Cell Mol Physiol 292, L240–L248.CrossRefGoogle Scholar
  56. Weber, K.L., and Bement, W.M. (2002). F-actin serves as a template for cytokeratin organization in cell free extracts. J Cell Sci 115, 1373–1382.Google Scholar
  57. Whipple, R.A., Balzer, E.M., Cho, E.H., Matrone, M.A., Yoon, J.R., and Martin, S.S. (2008). Vimentin filaments support extension of tubulin-based microtentacles in detached breast tumor cells. Cancer Res 68, 5678–5688.CrossRefGoogle Scholar
  58. Yoon, K.H., Yoon, M., Moir, R.D., Khuon, S., Flitney, F.W., and Goldman, R.D. (2001). Insights into the dynamic properties of keratin intermediate filaments in living epithelial cells. J Cell Biol 153, 503–516.CrossRefGoogle Scholar
  59. Yoon, M., Moir, R.D., Prahlad, V., and Goldman, R.D. (1998). Motile properties of vimentin intermediate filament networks in living cells. J Cell Biol 143, 147–157.CrossRefGoogle Scholar
  60. Zastrow, M.S., Vlcek, S., and Wilson, K.L. (2004). Proteins that bind A-type lamins: integrating isolated clues. J Cell Sci 117, 979–987.CrossRefGoogle Scholar

Copyright information

© Science China Press and Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.CAS Key Laboratory of Molecular Virology and Immunology, Institut Pasteur of ShanghaiChinese Academy of SciencesShanghaiChina
  2. 2.University of Chinese Academy of SciencesBeijingChina

Personalised recommendations