Skip to main content
SpringerLink
Log in

Glycosylphosphatidylinositol-anchored proteins as regulators of cortical cytoskeleton

  • Review-Hypothesis
  • Published:
Biochemistry (Moscow) Aims and scope Submit manuscript

Abstract

Glycosylphosphatidylinositol-anchored proteins (GPI-AP) are important players in reception and signal transduction, cell adhesion, guidance, formation of immune synapses, and endocytosis. At that, a particular GPI-AP can have different activities depending on a ligand. It is known that GPI-AP oligomer creates a lipid raft in its base on plasma membrane, which serves as a signaling platform for binding and activation of src-family kinases. Yet, this does not explain different activities of GPI-APs. Meanwhile, it has been shown that short-lived actomyosin complexes are bound to GPI-APs through lipid rafts. Here, we hypothesize that cell cortical cytoskeleton is the main target of GPI-AP signaling. Our hypothesis is based on the fact that the GPI-AP-induced lipid raft bound to actin filaments and anionic lipids of this raft is known to interact with and activate various actin-nucleating factors, such as formins and N-WASP. It is also known that these and other actin-regulating proteins are activated by src-family kinases directly or through their effectors, such as cortactin and abl-kinases. Regulation of cytoskeleton by GPI-APs may have impact on morphogenesis, cell guidance, and endocytosis, as well as on signaling of other receptors. To evaluate our hypothesis, we have comprehensively considered physiological activities of two GPI-APs–urokinase receptor and T-cadherin.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

DRM:

detergent resistant membrane

EGFR:

epidermal growth factor receptor

Gai2:

ai2 subunit of het-erotrimeric G-protein

GEEC:

GPI-APs enriched early endo-somal compartments

GPCR:

G-protein coupled receptor

GPI:

glycosylphosphatidylinositol

GPI-AP:

glycosylphos-phatidylinositol-anchored proteins

LDL:

low density lipopro-teins

NgR:

Nogo66 receptor

PI(x)P:

phosphatidyl-inositol(x)phosphate

PLC:

phospholipase C

PM:

plasma membrane

PS:

phosphatidylserine

RTK:

receptor tyrosine kinase

SFK:

src-family kinases

uPAR:

urokinase receptor

References

  1. Kinoshita, T. (2014) Biosynthesis and deficiencies of glycosylphosphatidylinositol, Proc. Jpn. Acad. Ser. B, 90, 130–143.

    Article  CAS  Google Scholar 

  2. Stefanova, I., Horejsi, V., Ansotegui, I. J., Knapp, W., and Stockinger, H. (1991) GPI-anchored cell-surface molecules complexed to protein tyrosine kinases, Science, 254, 1016–1019.

    Article  CAS  PubMed  Google Scholar 

  3. Suzuki, K. G. N., Fujiwara, T. K., Sanematsu, F., Iino, R., Edidin, M., and Kusumi, A. (2007) GPI-anchored receptor clusters transiently recruit Lyn and G alpha for temporary cluster immobilization and Lyn activation: single-molecule tracking study 1, J. Cell Biol., 177, 717–730.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Suzuki, K. G. N., Fujiwara, T. K., Edidin, M., and Kusumi, A. (2007) Dynamic recruitment of phospholipase C gamma at transiently immobilized GPI-anchored receptor clusters induces IP3-Ca2+ signaling: single-molecule tracking study 2, J. Cell Biol., 177, 731–742.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Suzuki, K. G. N., Kasai, R. S., Hirosawa, K. M., Nemoto, Y. L., Ishibashi, M., Miwa, Y., Fujiwara, T. K., and Kusumi, A. (2012) Transient GPI-anchored protein homodimers are units for raft organization and function, Nat. Chem. Biol., 8, 774–783.

    Article  CAS  PubMed  Google Scholar 

  6. Loertscher, R., and Lavery, P. (2002) The role of glycosyl phosphatidyl inositol (GPI)-anchored cell surface proteins in T-cell activation, Transpl. Immunol., 9, 93–96.

    Article  CAS  PubMed  Google Scholar 

  7. Tkachuk, V. A., Bochkov, V. N., Philippova, M. P., Stambolsky, D. V., Kuzmenko, E. S., Sidorova, M. V., Molokoedov, A. S., Spirov, V. G., and Resink, T. J. (1998) Identification of an atypical lipoprotein-binding protein from human aortic smooth muscle as T-cadherin, FEBS Lett., 421, 208–212.

    Article  CAS  PubMed  Google Scholar 

  8. Bochkov, V. N., Tkachuk, V. A., Hahn, A. W., Bernhardt, J., Buhler, F. R., and Resink, T. J. (1993) Concerted effects of lipoproteins and angiotensin II on signal transduction processes in vascular smooth muscle cells, Arterioscler. Thromb., 13, 1261–1269.

    Article  CAS  PubMed  Google Scholar 

  9. Bochkov, V. N., Tkachuk, V. A., Kuzmenko, Y. S., Borisova, Y. L., Buhler, F. R., and Resink, T. J. (1994) Characteristics of low and high-density lipoprotein binding and lipoprotein-induced signaling in quiescent human vascular smooth muscle cells, Mol. Pharmacol., 45, 262–270.

    CAS  PubMed  Google Scholar 

  10. Denzel, M. S., Scimia, M.-C., Zumstein, P. M., Walsh, K., Ruiz-Lozano, P., and Ranscht, B. (2010) T-cadherin is critical for adiponectin-mediated cardioprotection in mice, J. Clin. Invest., 120, 4342–4352.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Fredette, B. J., and Ranscht, B. (1994) T-cadherin expression delineates specific regions of the developing motor axonhindlimb projection pathway, J. Neurosci., 14, 7331–7346.

    CAS  PubMed  Google Scholar 

  12. Rubina, K., Kalinina, N., Potekhina, A., Efimenko, A., Semina, E., Poliakov, A., Wilkinson, D. G., Parfyonova, Y., and Tkachuk, V. (2007) T-cadherin suppresses angiogenesis in vivo by inhibiting migration of endothelial cells, Angiogenesis, 10, 183–195.

    Article  CAS  PubMed  Google Scholar 

  13. Benting, J., Rietveld, A., Ansorge, I., and Simons, K. (1999) Acyl and alkyl chain length of GPI-anchors is critical for raft association in vitro, FEBS Lett., 462, 47–50.

    Article  CAS  PubMed  Google Scholar 

  14. Raghupathy, R., Anilkumar, A. A., Polley, A., Singh, P. P., Yadav, M., Johnson, C., Suryawanshi, S., Saikam, V., Sawant, S. D., Panda, A., Guo, Z., Vishwakarma, R. A., Rao, M., and Mayor, S. (2015) Transbilayer lipid interactions mediate nanoclustering of lipid-anchored proteins, Cell, 161, 581–594.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Pike, L. J. (2009) The challenge of lipid rafts, J. Lipid Res., 50, S323–328.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  16. Binder, W. H., Barragan, V., and Menger, F. M. (2003). Domains and rafts in lipid membranes, Angew. Chem. Int. Ed., 42, 5802–5827.

    Article  CAS  Google Scholar 

  17. Hancock, J. F. (2006) Lipid rafts: contentious only from simplistic standpoints, Nat. Rev. Mol. Cell Biol., 7, 456–462.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Viola, A., and Gupta, N. (2007) Tether and trap: regulation of membrane-raft dynamics by actin-binding proteins, Nat. Rev. Immunol., 7, 889–896.

    Article  CAS  PubMed  Google Scholar 

  19. Zhou, Y., and Hancock, J. F. (2015) Ras nanoclusters: versatile lipid-based signaling platforms, Biochim. Biophys. Acta, 1853, 841–849.

    Article  CAS  PubMed  Google Scholar 

  20. Simons, K., and Sampaio, J. L. (2011) Membrane organization and lipid rafts, Cold Spring Harb. Perspect. Biol., 3, a004697.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  21. Saha, S., Lee, I.-H., Polley, A., Groves, J. T., Rao, M., and Mayor, S. (2015) Diffusion of GPI-anchored proteins is influenced by the activity of dynamic cortical actin, Mol. Biol. Cell, 25, 4033–4045.

    Article  CAS  Google Scholar 

  22. Lee, I.-H., Saha, S., Polley, A., Huang, H., Mayor, S., Rao, M., and Groves, J. T. (2015) Live cell plasma membranes do not exhibit a miscibility phase transition over a wide range of temperatures, J. Phys. Chem. B, 119, 4450–4459.

    Article  CAS  PubMed  Google Scholar 

  23. Owen, D. M., Williamson, D. J., Magenau, A., and Gaus, K. (2012) Sub-resolution lipid domains exist in the plasma membrane and regulate protein diffusion and distribution, Nat. Commun., 3, 1256.

    Article  PubMed  CAS  Google Scholar 

  24. Harder, T., and Simons, K. (1999) Clusters of glycolipid and glycosylphosphatidylinositol-anchored proteins in lymphoid cells: accumulation of actin regulated by local tyrosine phosphorylation, Eur. J. Immunol., 29, 556–562.

    Article  CAS  PubMed  Google Scholar 

  25. Degryse, B., Resnati, M., Rabbani, S. A., Villa, A., Fazioli, F., and Blasi, F. (1999) Src-dependence and pertussis-toxin sensitivity of urokinase receptor-dependent chemotaxis and cytoskeleton reorganization in rat smooth muscle cells, Blood, 94, 649–662.

    CAS  PubMed  Google Scholar 

  26. Varma, R., and Mayor, S. (1998) GPI-anchored proteins are organized in submicron domains at the cell surface, Nature, 394, 798–801.

    Article  CAS  PubMed  Google Scholar 

  27. Sharma, P., Varma, R., Sarasij, R. C., Ira, Gousset, K., Krishnamoorthy, G., Rao, M., and Mayor, S. (2004) Nanoscale organization of multiple GPI-anchored proteins in living cell membranes, Cell, 116, 577–589.

    Article  CAS  PubMed  Google Scholar 

  28. Goswami, D., Gowrishankar, K., Bilgrami, S., Ghosh, S., Raghupathy, R., Chadda, R., Vishwakarma, R., Rao, M., and Mayor, S. (2008) Nanoclusters of GPI-anchored proteins are formed by cortical actin-driven activity, Cell, 135, 1085–1097.

    Article  CAS  PubMed  Google Scholar 

  29. Gowrishankar, K., Ghosh, S., Saha, S. C. R., Mayor, S., and Rao, M. (2012) Active remodeling of cortical actin regulates spatiotemporal organization of cell surface molecules, Cell, 149, 1353–1367.

    Article  CAS  PubMed  Google Scholar 

  30. Saha, S., Lee, I.-H., Polley, A., Groves, J. T., Rao, M., and Mayor, S. (2015) Diffusion of GPI-anchored proteins is influenced by the activity of dynamic cortical actin, Mol. Biol. Cell, 26, 4033–4045.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Rubina, K. A., and Tkachuk, V. A. (2015) Guidance receptors in the nervous and cardiovascular systems, Biochemistry (Moscow), 80, 1235–1253.

    Article  CAS  Google Scholar 

  32. Philippova, M., Joshi, M. B., Pfaff, D., Kyriakakis, E., Maslova, K., Erne, P., and Resink, T. J. (2012) T-cadherin attenuates insulin-dependent signaling, eNOS activation, and angiogenesis in vascular endothelial cells, Cardiovasc. Res., 93, 498–507.

    Article  CAS  PubMed  Google Scholar 

  33. Semina, E. V., Rubina, K. A., Sysoeva, V. Y., Rutkevich, P. N., Kashirina, N. M., and Tkachuk, V. A. (2013) Novel mechanism regulating endothelial permeability via T-cadherin-dependent VE-cadherin phosphorylation and clathrin-mediated endocytosis, Mol. Cell. Biochem., 387, 39–53.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  34. Tyrberg, B., Miles, P., Azizian, K. T., Denzel, M. S., Nieves, M. L., Monosov, E. Z., Levine, F., and Ranscht, B. (2011) T-cadherin (Cdh13) in aßsociation with pancreatic ß-cell granules contributes to second phase insulin secretion, Islets, 3, 327–337.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Blasi, F., and Tjwa, M. (2002) uPAR: a versatile signaling orchestrator, Nat. Rev. Mol. Cell Biol., 3, 932–943.

    Article  CAS  PubMed  Google Scholar 

  36. Smith, H. W., and Marshall, C. J. (2010) Regulation of cell signaling by uPAR, Nat. Rev. Mol. Cell Biol., 11, 23–36.

    Article  CAS  PubMed  Google Scholar 

  37. Stepanova, V. V., and Tkachuk, V. A. (2002) Urokinase as a multidomain protein and polyfunctional cell regulator, Biochemistry (Moscow), 67, 109–118.

    Article  CAS  Google Scholar 

  38. Kapustin, A., Stepanova, V., Aniol, N., Cines, D. B., Poliakov, A., Yarovoi, S., Lebedeva, T., Wait, R., Ryzhakov, G., Parfyonova, Y., Gursky, Y., Yanagisawa, H., Minashkin, M., Beabealashvilli, R., Vorotnikov, A., Bobik, A., and Tkachuk, V. (2012) Fibulin-5 binds urokinase-type plasminogen activator and mediates urokinase-stimulated ß1integrin-dependent cell migration, Biochem. J., 443, 491–503.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Blasi, F., and Sidenius, N. (2010) The urokinase receptor: focused cell surface proteolysis, cell adhesion and signaling, FEBS Lett., 584, 1923–1930.

    CAS  PubMed  Google Scholar 

  40. Resnati, M., Pallavicini, I., Wang, J. M., Oppenheim, J., Serhan, C. N., Romano, M., and Blasi, F. (2002) The fibrinolytic receptor for urokinase activates the G proteincoupled chemotactic receptor FPRL1/LXA4R, Proc. Natl. Acad. Sci. USA, 99, 1359–1364.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Liu, D., Aguirre Ghiso, J., Estrada, Y., and Ossowski, L. (2002) EGFR is a transducer of the urokinase receptor initiated signal that is required for in vivo growth of a human carcinoma, Cancer Cell, 1, 445–457.

    Article  CAS  PubMed  Google Scholar 

  42. Madsen, C. D., Ferraris, G. M. S., Andolfo, A., Cunningham, O., and Sidenius, N. (2007) uPAR-induced cell adhesion and migration: vitronectin provides the key, J. Cell Biol., 177, 927–939.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Zanoni, I., Ostuni, R., Marek, L. R., Barresi, S., Barbalat, R., Barton, G. M., Granucci, F., and Kagan, J. C. (2011) CD14 controls the LPS-induced endocytosis of Toll-like receptor 4, Cell, 147, 868–880.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Sabharanjak, S., and Mayor, S. (2004) Folate receptor endocytosis and trafficking, Adv. Drug Deliv. Rev., 56, 1099–1109.

    Article  CAS  PubMed  Google Scholar 

  45. Bhagatji, P., Leventis, R., Comeau, J., Refaei, M., and Silvius, J. R. (2009) Steric and not structure-specific factors dictate the endocytic mechanism of glycosylphosphatidylinositol-anchored proteins, J. Cell Biol., 186, 615628.

    Article  CAS  Google Scholar 

  46. Koprivica, V., Cho, K.-S., Park, J. B., Yiu, G., Atwal, J., Gore, B., Kim, J. A., Lin, E., Tessier-Lavigne, M., Chen, D. F., and He, Z. (2005) EGFR activation mediates inhibition of axon regeneration by myelin and chondroitin sulfate proteoglycans, Science, 310, 106–110.

    Article  CAS  PubMed  Google Scholar 

  47. Eggeling, C., Ringemann, C., Medda, R., Schwarzmann, G., Sandhoff, K., Polyakova, S., Belov, V. N., Hein, B., Von Middendorff, C., Schonle, A., and Hell, S. W. (2009) Direct observation of the nanoscale dynamics of membrane lipids in a living cell, Nature, 457, 1159–1162.

    Article  CAS  PubMed  Google Scholar 

  48. Kay, J. G., Koivusalo, M., Ma, X., Wohland, T., and Grinstein, S. (2012) Phosphatidylserine dynamics in cellular membranes, Mol. Biol. Cell, 23, 2198–2212.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Wei, Y., Lukashev, M., Simon, D. I., Bodary, S. C., Rosenberg, S., Doyle, M. V., and Chapman, H. A. (1996) Regulation of integrin function by the urokinase receptor, Science, 273, 1551–1555.

    Article  CAS  PubMed  Google Scholar 

  50. Busso, N., Masur, S. K., Lazega, D., Waxman, S., and Ossowski, L. (1994) Induction of cell migration by prourokinase binding to its receptor: possible mechanism for signal transduction in human epithelial cells, J. Cell Biol., 126, 259–270.

    Article  CAS  PubMed  Google Scholar 

  51. Ben-Harush, K., Maimon, T., Patla, I., Villa, E., and Medalia, O. (2010) Visualizing cellular processes at the molecular level by cryo-electron tomography, J. Cell Sci., 123, 7–12.

    Article  CAS  PubMed  Google Scholar 

  52. Lucic, V., Rigort, A., and Baumeister, W. (2013) Cryo-electron tomography: the challenge of doing structural biology in situ, J. Cell Biol., 202, 407–419.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Urban, E., Jacob, S., Nemethova, M., Resch, G. P., and Small, J. V. (2010) Electron tomography reveals unbranched networks of actin filaments in lamellipodia, Nat. Cell Biol., 12, 429–435.

    Article  CAS  PubMed  Google Scholar 

  54. Medalia, O., Weber, I., Frangakis, A. S., and Nicastro, D. (2002) Macromolecular architecture in eukaryotic cells visualized by cryoelectron tomography, Science, 298, 12091213.

    Article  CAS  Google Scholar 

  55. Medalia, O., Beck, M., Ecke, M., Weber, I., and Neujahr, R. (2007) Organization of actin networks in intact filopodia, Curr. Biol., 17, 79–84.

    Article  CAS  PubMed  Google Scholar 

  56. Maurer, U. E., Sodeik, B., and Grunewald, K. (2008) Native 3D intermediates of membrane fusion in herpes simplex virus 1 entry, Proc. Natl. Acad. Sci. USA, 105, 10559–10564.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Kudryashev, M., Lepper, S., Baumeister, W., Cyrklaff, M., and Frischknecht, F. (2010) Geometric constrains for detecting short actin filaments by cryogenic electron tomography, PMC Biophys., 3, 6.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  58. Suzuki, K., and Sheetz, M. P. (2001) Binding of crosslinked glycosylphosphatidylinositol-anchored proteins to discrete actin-associated sites and cholesterol-dependent domains, Biophys. J., 81, 2181–2189.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Sanchez, T., Chen, D. T. N., DeCamp, S. J., Heymann, M., and Dogic, Z. (2012) Spontaneous motion in hierarchically assembled active matter, Nature, 491, 431–434.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Reymann, A.-C., Boujemaa-Paterski, R., Martiel, J.-L., Guerin, C., Cao, W., Chin, H. F., La Cruz, De, E. M., Thery, M., and Blanchoin, L. (2012) Actin network architecture can determine myosin motor activity, Science, 336, 1310–1314.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Dent, E. W., Gupton, S. L., and Gertler, F. B. (2011) The growth cone cytoskeleton in axon outgrowth and guidance, Cold Spring Harb. Perspect. Biol., 3, a001800.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  62. Fagotto, F., Rohani, N., Touret, A.-S., and Li, R. (2014) A molecular base for cell sorting at embryonic boundaries: contact inhibition of cadherin adhesion by ephrin/Ephdependent contractility, Dev. Cell, 27, 1–16.

    Google Scholar 

  63. Reynolds, A. B., Kanner, S. B., Bouton, A. H., Schaller, M. D., Weed, S. A., Flynn, D. C., and Parsons, J. T. (2014) SRChing for the substrates of Src, Oncogene, 33, 45374547.

    Google Scholar 

  64. Greuber, E. K., Smith-Pearson, P., Wang, J., and Pendergast, A. M. (2013) Role of ABL family kinases in cancer: from leukemia to solid tumors, Nat. Rev. Cancer, 13, 559–571.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Girao, H., Geli, M.-I., and Idrissi, F.-Z. (2008) Actin in the endocytic pathway: from yeast to mammals, FEBS Lett., 582, 2112–2119.

    Article  CAS  PubMed  Google Scholar 

  66. Herve, J.-C. (2014) Reciprocal influences between cell cytoskeleton and membrane channels, receptors and transporters, Biochim. Biophys. Acta, 1838, 511–513.

    Article  CAS  PubMed  Google Scholar 

  67. Gorelik, R., Yang, C., Kameswaran, V., Dominguez, R., and Svitkina, T. (2011) Mechanisms of plasma membrane targeting of formin mDia2 through its amino terminal domains, Mol. Biol. Cell, 22, 189–201.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Blanchoin, L., Boujemaa-Paterski, R., Sykes, C., and Plastino, J. (2014) Actin dynamics, architecture, and mechanics in cell motility, Physiol. Rev., 94, 235–263.

    CAS  PubMed  Google Scholar 

  69. Takenawa, T., and Suetsugu, S. (2007) The WASP-WAVE protein network: connecting the membrane to the cytoskeleton, Nat. Rev. Mol. Cell Biol., 8, 37–48.

    Article  CAS  PubMed  Google Scholar 

  70. McConnell, R. E., and Tyska, M. J. (2010) Leveraging the membrane–cytoskeleton interface with myosin-1, Trends Cell Biol., 20, 418–426.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Clucas, J., and Valderrama, F. (2015) ERM proteins in cancer progression, J. Cell Sci., 128, 1253–1253.

    Article  CAS  PubMed  Google Scholar 

  72. Saarikangas, J., Zhao, H., and Lappalainen, P. (2010) Regulation of the actin cytoskeleton–plasma membrane interplay by phosphoinositides, Physiol. Rev., 90, 259–289.

    Article  CAS  PubMed  Google Scholar 

  73. Mayor, S., and Riezman, H. (2004) Sorting GPI-anchored proteins, Nat. Rev. Mol. Cell Biol., 5, 110–120.

    Article  CAS  PubMed  Google Scholar 

  74. Sprenger, R. R., Fontijn, R. D., Van Marle, J., Pannekoek, H., and Horrevoets, A. J. G. (2006) Spatial segregation of transport and signaling functions between human endothelial caveolae and lipid raft proteomes, Biochem. J., 400, 401–410.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Locker, J. K., and Schmid, S. L. (2013) Integrated electron microscopy: super-duper resolution, PLoS Biol., 11, e1001639

    Article  CAS  Google Scholar 

  76. Tsui-Pierchala, B. A., Encinas, M., Milbrandt, J., and Johnson, E. M. (2002) Lipid rafts in neuronal signaling and function, Trends Neurosci., 25, 412–417.

    Article  CAS  PubMed  Google Scholar 

  77. Patel, H. H., Murray, F., and Insel, P. A. (2008) Caveolae as organizers of pharmacologically relevant signal transduction molecules, Annu. Rev. Pharmacol. Toxicol., 48, 359–391.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Cheng, J. P. X., and Nichols, B. J. (2015) Caveolae: one function or many? Trends Cell. Biol., 26, 1–13.

    Google Scholar 

  79. Echarri, A., and Del Pozo, M. A. (2015) Caveolae–mechanosensitive membrane invaginations linked to actin filaments, J. Cell Sci., 128, 2747–2758.

    Article  CAS  PubMed  Google Scholar 

  80. Andrews, N. W., Almeida, P. E., and Corrotte, M. (2014) Damage control: cellular mechanisms of plasma membrane repair, Trends Cell Biol., 24, 1–9.

    Article  CAS  Google Scholar 

  81. Echarri, A., Muriel, O., Pavon, D. M., Azegrouz, H., Escolar, F., Terron, M. C., Sanchez-Cabo, F., Martinez, F., Montoya, M. C., Llorca, O., and Del Pozo, M. A. (2012) Caveolar domain organization and trafficking is regulated by Abl kinases and mDia1, J. Cell Sci., 125, 3097–3113.

    Article  CAS  PubMed  Google Scholar 

  82. Mayor, S., Rothberg, K. G., and Maxfield, F. R. (1994) Sequestration of GPI-anchored proteins in caveolae triggered by cross-linking, Science, 264, 1948–1951.

    Article  CAS  PubMed  Google Scholar 

  83. Stahl, A., and Mueller, B. M. (1995) The urokinase-type plasminogen activator receptor, a GPI-linked protein, is localized in caveolae, J. Cell Biol., 129, 335–344.

    CAS  PubMed  Google Scholar 

  84. Ying, Y. S., and Anderson, R. (1992) Each caveola contains multiple glycosylphosphatidylinositol-anchored membrane proteins, Cold Spring Harb. Symp. Quant. Biol., 57, 593–604.

    Article  CAS  PubMed  Google Scholar 

  85. Abrami, L., Fivaz, M., Kobayashi, T., Kinoshita, T., Parton, R. G., and Van der Goot, F. G. (2001) Cross-talk between caveolae and glycosylphosphatidylinositol-rich domains, J. Biol. Chem., 276, 30729–30736.

    Article  CAS  PubMed  Google Scholar 

  86. Doherty, G. J., and McMahon, H. T. (2009) Mechanisms of endocytosis, Annu. Rev. Biochem., 78, 857–902.

    Article  CAS  PubMed  Google Scholar 

  87. Gauthier, N. C., Masters, T. A., and Sheetz, M. P. (2012) Mechanical feedback between membrane tension and dynamics, Trends Cell Biol., 22, 527–535.

    Article  CAS  PubMed  Google Scholar 

  88. Kirkham, M., Fujita, A., Chadda, R., Nixon, S. J., Kurzchalia, T. V., Sharma, D. K., Pagano, R. E., Hancock, J. F., Mayor, S., and Parton, R. G. (2005) Ultrastructural identification of uncoated caveolin-independent early endocytic vehicles, J. Cell Biol., 168, 465476.

    Article  CAS  Google Scholar 

  89. Johannes, L., Parton, R. G., Bassereau, P., and Mayor, S. (2015) Building endocytic pits without clathrin, Nat. Rev. Mol. Cell Biol., 16, 1–11.

    Article  CAS  Google Scholar 

  90. Chadda, R., Howes, M. T., Plowman, S. J., Hancock, J. F., Parton, R. G., and Mayor, S. (2007) Cholesterol-sensitive Cdc42 activation regulates actin polymerization for endocytosis via the GEEC pathway, Traffic, 8, 702–717.

    Article  CAS  PubMed  Google Scholar 

  91. Kumari, S., and Mayor, S. (2008) ARF1 is directly involved in dynamin-independent endocytosis, Nat. Cell Biol., 10, 30–41.

    Article  CAS  PubMed  Google Scholar 

  92. Dustin, M. L., and Groves, J. T. (2012) Receptor signaling clusters in the immune synapse, Annu. Rev. Biophys., 41, 543–556.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Yu, Y., Smoligovets, A. A., and Groves, J. T. (2013) Modulation of T-cell signaling by the actin cytoskeleton, J. Cell Sci., 126, 1049–1058.

    Article  CAS  PubMed  Google Scholar 

  94. Liu, B., Chen, W., Evavold, B. D., and Zhu, C. (2014) Accumulation of dynamic catch bonds between TCR and agonist peptide-MHC triggers T-cell signaling, Cell, 157, 357–368.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Bakker, G. J., Eich, C., Torreno-Pina, J. A., Diez-Ahedo, R., Perez-Samper, G., Van Zanten, T. S., Figdor, C. G., Cambi, A., and Garcia-Parajo, M. F. (2012) Lateral mobility of individual integrin nanoclusters orchestrates the onset for leukocyte adhesion, Proc. Natl. Acad. Sci. USA, 109, 4869–4874.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Kaizuka, Y., Douglass, A. D., Varma, R., Dustin, M. L., and Vale, R. D. (2007) Mechanisms for segregating T-cell receptor and adhesion molecules during immunological synapse formation in Jurkat T-cells, Proc. Natl. Acad. Sci. USA, 104, 20296–20301.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Ilangumaran, S., He, H. T., and Hoessli, D. C. (2000) Microdomains in lymphocyte signaling: beyond GPIanchored proteins, Immunol. Today, 21, 2–7.

    Article  CAS  PubMed  Google Scholar 

  98. Blasi, F., and Sidenius, N. (2009) Efferocytosis: another function of uPAR, Blood, 114, 752–753.

    Article  CAS  PubMed  Google Scholar 

  99. Blasi, F. (1988) A surface receptor for urokinase plasminogen activator: a link between the cytoskeleton and the extracellular matrix, Protoplasma, 145, 95–98.

    Article  Google Scholar 

  100. Ossowski, L., and Aguirre-Ghiso, J. A. (2000) Urokinase receptor and integrin partnership: coordination of signaling for cell adhesion, migration and growth, Curr. Opin. Cell Biol., 12, 613–620.

    Article  CAS  Google Scholar 

  101. Shen, B., Delaney, M. K., and Du, X. (2012) Inside-out, outside-in, and inside-outside-in: G protein signaling in integrin-mediated cell adhesion, spreading, and retraction, Curr. Opin. Cell Biol., 24, 600–606.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Zhu, S., Gladson, C. L., White, K. E., Ding, Q., Stewart, J., Jin, T. H., Chapman, H. A., and Olman, M. A. (2009) Urokinase receptor mediates lung fibroblast attachment and migration toward provisional matrix proteins through interaction with multiple integrins, Am. J. Physiol. Lung Cell. Mol. Physiol., 297, L97–L108.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Sitrin, R. G., Pan, P. M., Harper, H. A., Todd, R. F., Harsh, D. M., and Blackwood, R. A. (2000) Clustering of urokinase receptors (uPAR; CD87) induces proinflammatory signaling in human polymorphonuclear neutrophils, J. Immunol., 165, 3341–3349.

    Article  CAS  PubMed  Google Scholar 

  104. Chen, Y. A., and Scheller, R. H. (2001) SNARE-mediated membrane fusion, Nat. Rev. Mol. Cell Biol., 2, 98–106.

    Article  CAS  PubMed  Google Scholar 

  105. Porat-Shliom, N., Milberg, O., Masedunskas, A., and Weigert, R. (2012) Multiple roles for the actin cytoskeleton during regulated exocytosis, Cell. Mol. Life Sci., 70, 2099–2121.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  106. Somlyo, A. P., and Somlyo, A. V. (2003) Ca2+ sensitivity of smooth muscle and nonmuscle myosin II: modulated by G proteins, kinases, and myosin phosphatase, Physiol. Rev., 83, 1325–1358.

    Article  CAS  PubMed  Google Scholar 

  107. Salaita, K., and Groves, J. T. (2010) Roles of the cytoskeleton in regulating EphA2 signals, Commun. Integr. Biol., 3, 454–457.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Ivanov, D. B., Philippova, M. P., and Tkachuk, V. A. (2001) Structure and functions of classical cadherins, Biochemistry (Moscow), 66, 1174–1186.

    Article  CAS  Google Scholar 

  109. Rubina, K. A., Kalinina, N. I., Parfenova, E. V., and Tkachuk, V. A. (2007) T-cadherin as a receptor involved in the regulation of angiogenesis and the remodeling of blood vessels, Biol. Membr. (Moscow), 24, 62–69.

    CAS  Google Scholar 

  110. Fredette, B. J., Miller, J., and Ranscht, B. (1996) Inhibition of motor axon growth by T-cadherin substrata, Development, 122, 3163–3171.

    CAS  PubMed  Google Scholar 

  111. Kuzmenko, Y. S., Stambolsky, D., Kern, F., Bochkov, V. N., Tkachuk, V. A., and Resink, T. J. (1998) Characteristics of smooth muscle cell lipoprotein binding proteins (p105/p130) as T-cadherin and regulation by positive and negative growth regulators, Biochem. Biophys. Res. Commun., 246, 489–494.

    Article  CAS  PubMed  Google Scholar 

  112. Bochkov, V. N., Voino-Yasenetskaya, T. A., and Tkachuk, V. A. (1991) Epinephrine potentiates activation of human platelets by low-density lipoproteins, Biochim. Biophys. Acta, 1097, 123–127.

    Article  CAS  PubMed  Google Scholar 

  113. Rubina, K., Talovskaya, E., Cherenkov, V., Ivanov, D., Stambolsky, D., Storozhevykh, T., Pinelis, V., Shevelev, A., Parfyonova, Y., Resink, T., Erne, P., and Tkachuk, V. (2005) LDL induces intracellular signaling and cell migration via atypical LDL-binding protein T-cadherin, Mol. Cell. Biochem., 273, 33–41.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Hug, C., Wang, J., Ahmad, N. S., and Bogan, J. S. (2004) T-cadherin is a receptor for hexameric and high-molecular-weight forms of Acrp30/adiponectin, Proc. Natl. Acad. Sci. USA, 101, 10308–10313.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Doyle, D. D., Goings, G. E., Upshaw-Earley, J., and Page, E. (1998) T-cadherin is a major glycophosphoinositol-anchored protein associated with noncaveolar detergent-insoluble domains of the cardiac sarcolemma, J. Biol. Chem., 273, 6937–6943.

    Article  CAS  PubMed  Google Scholar 

  116. Vu, V., Bui, P., Eguchi, M., Xu, A., and Sweeney, G. (2013) Globular adiponectin induces LKB1/AMPKdependent glucose uptake via actin cytoskeleton remodeling, J. Mol. Endocrinol., 51, 155–165.

    Article  CAS  PubMed  Google Scholar 

  117. Palanivel, R., Ganguly, R., Turdi, S., Xu, A., and Sweeney, G. (2014) Adiponectin stimulates Rho-mediated actin cytoskeleton remodeling and glucose uptake via APPL1 in primary cardiomyocytes, Metabolism, 63, 1363–1373.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Faculty of Medicine, Lomonosov Moscow State University, 119992, Moscow, Russia

    G. V. Sharonov, M. N. Balatskaya & V. A. Tkachuk

  2. Structural Biology Department, Shemyakin–Ovchinnikov Institute of Bioorganic Chemistry, 117997, Moscow, Russia

    G. V. Sharonov

Authors
  1. G. V. Sharonov
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. N. Balatskaya
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. V. A. Tkachuk
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to G. V. Sharonov.

Additional information

Published in Russian in Biokhimiya, 2016, Vol. 81, No. 6, pp. 844-859.

Biochemistry (Moscow). Papers in Press. Published on May 1, 2016 as Manuscript BM15-363.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sharonov, G.V., Balatskaya, M.N. & Tkachuk, V.A. Glycosylphosphatidylinositol-anchored proteins as regulators of cortical cytoskeleton. Biochemistry Moscow 81, 636–650 (2016). https://doi.org/10.1134/S0006297916060110

Download citation

  • Received:

  • Revised:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0006297916060110

Key words

Search

Navigation