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Chemotaxis: Movement, direction, control

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Abstract

This review focuses on basic principles of motility in different cell types, formation of the specific cell structures that enable directed migration, and how external signals are transduced into cells and coupled to the motile machinery. Feedback mechanisms and their potential role in maintenance of internal chemotactic gradients and persistence of directed migration are highlighted.

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Abbreviations

Arp:

actin-related protein

DOCK:

dedicator of cytokinesis, a group of guanine nucleotide exchange factors for Rhofamily proteins

EGF:

epidermal growth factor

Epac:

guanine nucleotide exchange protein directly activated by cAMP

Erk:

extracellularly regulated MAP-kinase

FAK:

focal adhesion kinase

FH1/FH2:

formin homology (domain) 1/2

GBD/CRIB:

GTPase-binding domain/Cdc42 and Rac interactive binding (domain)

GbpC:

cGMP-binding protein C in Dictyostelium cells

GPCR:

trimeric G-protein-coupled receptor

Grb2:

growth factor receptor-bound protein 2

IL-1β:

interleukin-1β

LEGI:

local excitation and global inhibition model

LIM-kinase:

protein kinase containing the LIM-domain encoded by the lin-11, isl-1, and mec-3 genes of Caenorhabditis

LPA:

lysophosphatidic acid

MLCK:

myosin II light chain kinase

NAD(P)H:

reduced nicotinamide adenine dinucleotide (phosphate)

NPF:

nucleation-promoting factor

PAK:

p21-activated kinase

PDGF:

platelet-derived growth factor

PDK:

phosphoinositide-dependent kinase

PH:

plekstrin homology (domain)

PI3K:

phosphatidylinositol-3-kinase which phosphorylates phosphatidylinositols at 3′-position of the inositol ring

PIP2:

PI(3,4)P2, and PI(4,5)P2, phosphatidylinositol bisphosphate with two phosphate groups attached to the indicated positions of inositol ring

PIP3 and PI(3,4,5)P2:

phosphatidylinositol 3,4,5-trisphosphate

PIX:

PAK-interacting exchange factor

PKB/Akt:

protein kinase B, aka Akt

PLA2:

phospholipase A2

PTEN:

phosphatase and tensin homolog deleted on chromosome ten that dephosphorylates phosphatidylinositols at 3′-position of the inositol ring

ROCK:

Rho-associated, coiled-coil containing protein kinase

ROS:

reactive oxygen species

RPTK:

receptor protein tyrosine kinase

Scar:

suppressor of cAMP receptor in Dictyostelium cells

sGC:

soluble guanylyl cyclase

SH2:

Srchomology 2 (domain)

SHIP1:

Src homology 2 domain containing inositol-5-phosphatase 1 that dephosphorylates phosphatidylinositols at the 5′-position of the inositol ring

Src:

Rous sarcoma tyrosine kinase

TorC2:

target of rapamycin complex 2

WASP:

Wiscott-Aldrich syndrome protein

WAVE:

WASP and verprolin homologous protein in mammalian cells

WH1/WH2:

WASP homology (domain)

References

  1. Geeves, M. A., and Holmes, K. C. (2005) Adv. Protein Chem., 71, 161–193.

    PubMed  CAS  Google Scholar 

  2. Swaney, K. F., Huang, C. H., and Devreotes, P. N. (2010) Annu. Rev. Biophys., 39, 265–289.

    PubMed  CAS  Google Scholar 

  3. Li, L., Norrelykke, S. F., and Cox, E. C. (2008) PLoS ONE, 3, e2093.

    PubMed  Google Scholar 

  4. Xiong, Y., Huang, C. H., Iglesias, P. A., and Devreotes, P. N. (2010) Proc. Natl. Acad. Sci. USA, 107, 17079–17086.

    PubMed  CAS  Google Scholar 

  5. Baker, M. D., Wolanin, P. M., and Stock, J. B. (2006) Bioessays, 28, 9–22.

    PubMed  CAS  Google Scholar 

  6. Lammermann, T., and Sixt, M. (2009) Curr. Opin. Cell Biol., 21, 636–644.

    PubMed  Google Scholar 

  7. Niggli, V. (2003) Int. J. Biochem. Cell Biol., 35, 1619–1638.

    PubMed  CAS  Google Scholar 

  8. Charest, P. G., and Firtel, R. A. (2006) Curr. Opin. Genet. Dev., 16, 339–347.

    PubMed  CAS  Google Scholar 

  9. Von Philipsborn, A., and Bastmeyer, M. (2007) Int. Rev. Cytol., 263, 1–62.

    Google Scholar 

  10. Sheetz, M. P. (1994) Semin. Cell Biol., 5, 149–155.

    PubMed  CAS  Google Scholar 

  11. Small, J. V., Anderson, K., and Rottner, K. (1996) Biosci. Rep., 16, 351–368.

    PubMed  CAS  Google Scholar 

  12. Haugh, J. M. (2006) Biophys. J., 90, 2297–2308.

    PubMed  CAS  Google Scholar 

  13. Haugh, J. M., Codazzi, F., Teruel, M., and Meyer, T. (2000) J. Cell Biol., 151, 1269–1280.

    PubMed  CAS  Google Scholar 

  14. Ronnstrand, L., and Heldin, C. H. (2001) Int. J. Cancer, 91, 757–762.

    PubMed  CAS  Google Scholar 

  15. Schneider, I. C., and Haugh, J. M. (2005) J. Cell Biol., 171, 883–892.

    PubMed  CAS  Google Scholar 

  16. Schneider, I. C., and Haugh, J. M. (2006) Cell Cycle, 5, 1130–1134.

    PubMed  CAS  Google Scholar 

  17. Condeelis, J., Singer, R. H., and Segall, J. E. (2005) Annu. Rev. Cell Dev. Biol., 21, 695–718.

    PubMed  CAS  Google Scholar 

  18. Kedrin, D., van Rheenen, J., Hernandez, L., Condeelis, J., and Segall, J. E. (2007) J. Mammary Gland. Biol. Neoplasia, 12, 143–152.

    PubMed  Google Scholar 

  19. Jekely, G., Sung, H. H., Luque, C. M., and Rorth, P. (2005) Dev. Cell, 9, 197–207.

    PubMed  CAS  Google Scholar 

  20. Janssens, K., Sung, H. H., and Rorth, P. (2010) Proc. Natl. Acad. Sci. USA, 107, 7323–7328.

    PubMed  CAS  Google Scholar 

  21. Keller, R. (2005) Curr. Opin. Cell Biol., 17, 533–541.

    PubMed  CAS  Google Scholar 

  22. Ozaki, Y., Nishimura, M., Sekiya, K., Suehiro, F., Kanawa, M., Nikawa, H., Hamada, T., and Kato, Y. (2007) Stem Cells Dev., 16, 119–129.

    PubMed  CAS  Google Scholar 

  23. Ponte, A. L., Marais, E., Gallay, N., Langonne, A., Delorme, B., Herault, O., Charbord, P., and Domenech, J. (2007) Stem Cells, 25, 1737–1745.

    PubMed  CAS  Google Scholar 

  24. Birchmeier, C. (2004) in Cell Motility (Ridley, M. P. A., and Clark, P., eds.) John Wiley and Sons, Ltd., Chichester, UK, pp. 317–330.

    Google Scholar 

  25. Annesley, S. J., and Fisher, P. R. (2009) Mol. Cell Biochem., 329, 73–91.

    PubMed  CAS  Google Scholar 

  26. Van Haastert, P. J., and Devreotes, P. N. (2004) Nat. Rev. Mol. Cell Biol., 5, 626–634.

    PubMed  Google Scholar 

  27. Tomchik, K. J., and Devreotes, P. N. (1981) Science, 212, 443–446.

    PubMed  CAS  Google Scholar 

  28. Geiger, J., Wessels, D., and Soll, D. R. (2003) Cell Motil. Cytoskeleton, 56, 27–44.

    PubMed  Google Scholar 

  29. Soll, D. R., Wessels, D., Heid, P. J., and Zhang, H. (2002) J. Muscle Res. Cell Motil., 23, 659–672.

    PubMed  CAS  Google Scholar 

  30. Eichinger, L., Pachebat, J. A., Glockner, G., Rajandream, M. A., Sucgang, R., et al. (2005) Nature, 435, 43–57.

    PubMed  CAS  Google Scholar 

  31. Chisholm, R. L., Gaudet, P., Just, E. M., Pilcher, K. E., Fey, P., Merchant, S. N., and Kibbe, W. A. (2006) Nucleic Acids Res., 34, D423–427.

    PubMed  CAS  Google Scholar 

  32. Zigmond, S. H. (1977) J. Cell Biol., 75, 606–616.

    PubMed  CAS  Google Scholar 

  33. Foxman, E. F., Kunkel, E. J., and Butcher, E. C. (1999) J. Cell Biol., 147, 577–588.

    PubMed  CAS  Google Scholar 

  34. Heit, B., Tavener, S., Raharjo, E., and Kubes, P. (2002) J. Cell Biol., 159, 91–102.

    PubMed  CAS  Google Scholar 

  35. Ali, H., Richardson, R. M., Haribabu, B., and Snyderman, R. (1999) J. Biol. Chem., 274, 6027–6030.

    PubMed  CAS  Google Scholar 

  36. Kharitonova, M. A., and Vasiliev, J. M. (2008) Semin. Cell Dev. Biol., 19, 480–484.

    PubMed  Google Scholar 

  37. Mogilner, A., and Keren, K. (2009) Curr. Biol., 19, R762–771.

    PubMed  CAS  Google Scholar 

  38. Small, J. V., Geiger, B., Kaverina, I., and Bershadsky, A. (2002) Nat. Rev. Mol. Cell Biol., 3, 957–964.

    PubMed  CAS  Google Scholar 

  39. Vasiliev, J. M. (2004) Int. J. Dev. Biol., 48, 425–439.

    PubMed  CAS  Google Scholar 

  40. Friedl, P., and Wolf, K. (2010) J. Cell Biol., 188, 11–19.

    PubMed  CAS  Google Scholar 

  41. Even-Ram, S., and Yamada, K. M. (2005) Curr. Opin. Cell Biol., 17, 524–532.

    PubMed  CAS  Google Scholar 

  42. Pierce, G. F., Mustoe, T. A., Altrock, B. W., Deuel, T. F., and Thomason, A. (1991) J. Cell Biochem., 45, 319–326.

    PubMed  CAS  Google Scholar 

  43. Seppa, H., Grotendorst, G., Seppa, S., Schiffmann, E., and Martin, G. R. (1982) J. Cell Biol., 92, 584–588.

    PubMed  CAS  Google Scholar 

  44. De Donatis, A., Comito, G., Buricchi, F., Vinci, M. C., Parenti, A., Caselli, A., Camici, G., Manao, G., Ramponi, G., and Cirri, P. (2008) J. Biol. Chem., 283, 19948–19956.

    PubMed  Google Scholar 

  45. Insall, R. H. (2010) Nat. Rev. Mol. Cell Biol., 11, 453–458.

    PubMed  CAS  Google Scholar 

  46. Shestakova, E. A., Singer, R. H., and Condeelis, J. (2001) Proc. Natl. Acad. Sci. USA, 98, 7045–7050.

    PubMed  CAS  Google Scholar 

  47. Kawada, K., Upadhyay, G., Ferandon, S., Janarthanan, S., Hall, M., Vilardaga, J. P., and Yajnik, V. (2009) Mol. Cell Biol., 29, 4508–4518.

    PubMed  CAS  Google Scholar 

  48. Bershadsky, A., Kozlov, M., and Geiger, B. (2006) Curr. Opin. Cell Biol., 18, 472–481.

    PubMed  CAS  Google Scholar 

  49. Lauffenburger, D. A., and Horwitz, A. F. (1996) Cell, 84, 359–369.

    PubMed  CAS  Google Scholar 

  50. Mitchison, T. J., and Cramer, L. P. (1996) Cell, 84, 371–379.

    PubMed  CAS  Google Scholar 

  51. Chhabra, E. S., and Higgs, H. N. (2007) Nat. Cell Biol., 9, 1110–1121.

    PubMed  CAS  Google Scholar 

  52. Pollard, T. D., and Borisy, G. G. (2003) Cell, 112, 453–465.

    PubMed  CAS  Google Scholar 

  53. Faix, J., Breitsprecher, D., Stradal, T. E., and Rottner, K. (2009) Int. J. Biochem. Cell Biol., 41, 1656–1664.

    PubMed  CAS  Google Scholar 

  54. Gardel, M. L., Schneider, I. C., Aratyn-Schaus, Y., and Waterman, C. M. (2010) Annu. Rev. Cell Dev. Biol., 26, 315–333.

    PubMed  CAS  Google Scholar 

  55. Pellegrin, S., and Mellor, H. (2007) J. Cell Sci., 120, 3491–3499.

    PubMed  CAS  Google Scholar 

  56. Vicente-Manzanares, M., Ma, X., Adelstein, R. S., and Horwitz, A. R. (2009) Nat. Rev. Mol. Cell Biol., 10, 778–790.

    PubMed  CAS  Google Scholar 

  57. Parsons, J. T., Horwitz, A. R., and Schwartz, M. A. (2010) Nat. Rev. Mol. Cell Biol., 11, 633–643.

    PubMed  CAS  Google Scholar 

  58. DiMilla, P. A., Stone, J. A., Quinn, J. A., Albelda, S. M., and Lauffenburger, D. A. (1993) J. Cell Biol., 122, 729–737.

    PubMed  CAS  Google Scholar 

  59. Rafelski, S. M., and Theriot, J. A. (2004) Annu. Rev. Biochem., 73, 209–239.

    PubMed  CAS  Google Scholar 

  60. Fackler, O. T., and Grosse, R. (2008) J. Cell Biol., 181, 879–884.

    PubMed  CAS  Google Scholar 

  61. Bretscher, M. S. (2008) Nat. Rev. Mol. Cell Biol., 9, 916.

    PubMed  CAS  Google Scholar 

  62. Bugyi, B., and Carlier, M. F. (2010) Annu. Rev. Biophys., 39, 449–470.

    PubMed  CAS  Google Scholar 

  63. Le Clainche, C., and Carlier, M. F. (2008) Physiol. Rev., 88, 489–513.

    PubMed  Google Scholar 

  64. Wegner, A. (1976) J. Mol. Biol., 108, 139–150.

    PubMed  CAS  Google Scholar 

  65. Huang, T. Y., DerMardirossian, C., and Bokoch, G. M. (2006) Curr. Opin. Cell Biol., 18, 26–31.

    PubMed  CAS  Google Scholar 

  66. DesMarais, V., Macaluso, F., Condeelis, J., and Bailly, M. (2004) J. Cell Sci., 117, 3499–3510.

    PubMed  CAS  Google Scholar 

  67. Mogilner, A. (2006) Curr. Opin. Cell Biol., 18, 32–39.

    PubMed  CAS  Google Scholar 

  68. Dos Remedios, C. G., Chhabra, D., Kekic, M., Dedova, I. V., Tsubakihara, M., Berry, D. A., and Nosworthy, N. J. (2003) Physiol. Rev., 83, 433–473.

    PubMed  Google Scholar 

  69. Small, J. V., Stradal, T., Vignal, E., and Rottner, K. (2002) Trends Cell Biol., 12, 112–120.

    PubMed  CAS  Google Scholar 

  70. Winder, S. J., and Ayscough, K. R. (2005) J. Cell Sci., 118, 651–654.

    PubMed  CAS  Google Scholar 

  71. Alexandrova, A. Y., Arnold, K., Schaub, S., Vasiliev, J. M., Meister, J. J., Bershadsky, A. D., and Verkhovsky, A. B. (2008) PLoS ONE, 3, e3234.

    PubMed  Google Scholar 

  72. Ponti, A., Machacek, M., Gupton, S. L., Waterman-Storer, C. M., and Danuser, G. (2004) Science, 305, 1782–1786.

    PubMed  CAS  Google Scholar 

  73. Ridley, A. J., Schwartz, M. A., Burridge, K., Firtel, R. A., Ginsberg, M. H., Borisy, G., Parsons, J. T., and Horwitz, A. R. (2003) Science, 302, 1704–1709.

    PubMed  CAS  Google Scholar 

  74. Ridley, A. J. (2006) Trends Cell Biol., 16, 522–529.

    PubMed  CAS  Google Scholar 

  75. Disanza, A., Steffen, A., Hertzog, M., Frittoli, E., Rottner, K., and Scita, G. (2005) Cell Mol. Life Sci., 62, 955–970.

    PubMed  CAS  Google Scholar 

  76. Otomo, T., Tomchick, D. R., Otomo, C., Panchal, S. C., Machius, M., and Rosen, M. K. (2005) Nature, 433, 488–494.

    PubMed  CAS  Google Scholar 

  77. Pollard, T. D. (2007) Annu. Rev. Biophys. Biomol. Struct., 36, 451–477.

    PubMed  CAS  Google Scholar 

  78. Kerkhoff, E. (2006) Trends Cell Biol., 16, 477–483.

    PubMed  CAS  Google Scholar 

  79. Stenmark, H., Aasland, R., and Driscoll, P. C. (2002) FEBS Lett., 513, 77–84.

    PubMed  CAS  Google Scholar 

  80. Insall, R. H., and Machesky, L. M. (2009) Dev. Cell, 17, 310–322.

    PubMed  CAS  Google Scholar 

  81. Welch, M. D., and Mullins, R. D. (2002) Annu. Rev. Cell Dev. Biol., 18, 247–288.

    PubMed  CAS  Google Scholar 

  82. Pantaloni, D., Boujemaa, R., Didry, D., Gounon, P., and Carlier, M. F. (2000) Nat. Cell Biol., 2, 385–391.

    PubMed  CAS  Google Scholar 

  83. Pollitt, A. Y., and Insall, R. H. (2009) J. Cell Sci., 122, 2575–2578.

    PubMed  CAS  Google Scholar 

  84. Stradal, T. E., and Scita, G. (2006) Curr. Opin. Cell Biol., 18, 4–10.

    PubMed  CAS  Google Scholar 

  85. Takenawa, T., and Suetsugu, S. (2007) Nat. Rev. Mol. Cell Biol., 8, 37–48.

    PubMed  CAS  Google Scholar 

  86. Kaverina, I., Krylyshkina, O., and Small, J. V. (2002) Int. J. Biochem. Cell Biol., 34, 746–761.

    PubMed  CAS  Google Scholar 

  87. Broussard, J. A., Webb, D. J., and Kaverina, I. (2008) Curr. Opin. Cell Biol., 20, 85–90.

    PubMed  CAS  Google Scholar 

  88. Geiger, B., Spatz, J. P., and Bershadsky, A. D. (2009) Nat. Rev. Mol. Cell Biol., 10, 21–33.

    PubMed  CAS  Google Scholar 

  89. Choi, C. K., Vicente-Manzanares, M., Zareno, J., Whitmore, L. A., Mogilner, A., and Horwitz, A. R. (2008) Nat. Cell Biol., 10, 1039–1050.

    PubMed  CAS  Google Scholar 

  90. Vicente-Manzanares, M., Koach, M. A., Whitmore, L., Lamers, M. L., and Horwitz, A. F. (2008) J. Cell Biol., 183, 543–554.

    PubMed  CAS  Google Scholar 

  91. Friedland, J. C., Lee, M. H., and Boettiger, D. (2009) Science, 323, 642–644.

    PubMed  CAS  Google Scholar 

  92. Vogel, V., and Sheetz, M. (2006) Nat. Rev. Mol. Cell Biol., 7, 265–275.

    PubMed  CAS  Google Scholar 

  93. Rottner, K., Hall, A., and Small, J. V. (1999) Curr. Biol., 9, 640–648.

    PubMed  CAS  Google Scholar 

  94. Riento, K., and Ridley, A. J. (2003) Nat. Rev. Mol. Cell Biol., 4, 446–456.

    PubMed  CAS  Google Scholar 

  95. Yoneda, A., Multhaupt, H. A., and Couchman, J. R. (2005) J. Cell Biol., 170, 443–453.

    PubMed  CAS  Google Scholar 

  96. Khapchaev, A. Yu., Shirinsky, V. P., and Vorotnikiv, A. V. (2003) Uspekhi Biol. Khim., 43, 365–420.

    CAS  Google Scholar 

  97. Chew, T. L., Wolf, W. A., Gallagher, P. J., Matsumura, F., and Chisholm, R. L. (2002) J. Cell Biol., 156, 543–553.

    PubMed  CAS  Google Scholar 

  98. Totsukawa, G., Wu, Y., Sasaki, Y., Hartshorne, D. J., Yamakita, Y., Yamashiro, S., and Matsumura, F. (2004) J. Cell Biol., 164, 427–439.

    PubMed  CAS  Google Scholar 

  99. Post, P. L., DeBiasio, R. L., and Taylor, D. L. (1995) Mol. Biol. Cell, 6, 1755–1768.

    PubMed  CAS  Google Scholar 

  100. Eddy, R. J., Pierini, L. M., Matsumura, F., and Maxfield, F. R. (2000) J. Cell Sci., 113(Pt. 7), 1287–1298.

    PubMed  CAS  Google Scholar 

  101. Lammermann, T., Bader, B. L., Monkley, S. J., Worbs, T., Wedlich-Soldner, R., Hirsch, K., Keller, M., Forster, R., Critchley, D. R., Fassler, R., and Sixt, M. (2008) Nature, 453, 51–55.

    PubMed  Google Scholar 

  102. Renkawitz, J., Schumann, K., Weber, M., Lammermann, T., Pflicke, H., Piel, M., Polleux, J., Spatz, J. P., and Sixt, M. (2009) Nat. Cell Biol., 11, 1438–1443.

    PubMed  CAS  Google Scholar 

  103. Yoshida, K., and Soldati, T. (2006) J. Cell Sci., 119, 3833–3844.

    PubMed  CAS  Google Scholar 

  104. Huxley, A. F. (2000) Philos. Trans. R. Soc. Lond. B: Biol. Sci., 355, 433–440.

    CAS  Google Scholar 

  105. Huxley, H. E. (2004) Eur. J. Biochem., 271, 1403–1415.

    PubMed  CAS  Google Scholar 

  106. Danuser, G. (2009) J. Cell Sci., 122, 1959–1962.

    PubMed  CAS  Google Scholar 

  107. Vallotton, P., and Small, J. V. (2009) J. Cell Sci., 122, 1955–1958.

    PubMed  CAS  Google Scholar 

  108. Cai, Y., Biais, N., Giannone, G., Tanase, M., Jiang, G., Hofman, J. M., Wiggins, C. H., Silberzan, P., Buguin, A., Ladoux, B., and Sheetz, M. P. (2006) Biophys. J., 91, 3907–3920.

    PubMed  CAS  Google Scholar 

  109. Even-Ram, S., Doyle, A. D., Conti, M. A., Matsumoto, K., Adelstein, R. S., and Yamada, K. M. (2007) Nat. Cell Biol., 9, 299–309.

    PubMed  CAS  Google Scholar 

  110. Kolega, J. (2003) Mol. Biol. Cell, 114, 4745–4757.

    Google Scholar 

  111. Vicente-Manzanares, M., Zareno, J., Whitmore, L., Choi, C. K., and Horwitz, A. F. (2007) J. Cell Biol., 176, 573–580.

    PubMed  CAS  Google Scholar 

  112. Sellers, J. R., and Knight, P. J. (2007) J. Muscle Res. Cell Motil., 28, 363–370.

    PubMed  CAS  Google Scholar 

  113. Bosgraaf, L., and van Haastert, P. J. (2006) Eur. J. Cell Biol., 85, 969–979.

    PubMed  CAS  Google Scholar 

  114. Craig, R., and Woodhead, J. L. (2006) Curr. Opin. Struct. Biol., 16, 204–212.

    PubMed  CAS  Google Scholar 

  115. Verkhovsky, A. B., and Borisy, G. G. (1993) J. Cell Biol., 123, 637–652.

    PubMed  CAS  Google Scholar 

  116. Verkhovsky, A. B., Svitkina, T. M., and Borisy, G. G. (1995) J. Cell Biol., 131, 989–1002.

    PubMed  CAS  Google Scholar 

  117. Hotulainen, P., and Lappalainen, P. (2006) J. Cell Biol., 173, 383–394.

    PubMed  CAS  Google Scholar 

  118. Lo, C. M., Buxton, D. B., Chua, G. C., Dembo, M., Adelstein, R. S., and Wang, Y. L. (2004) Mol. Biol. Cell, 15, 982–989.

    PubMed  CAS  Google Scholar 

  119. Dugina, V., Zwaenepoel, I., Gabbiani, G., Clement, S., and Chaponnier, C. (2009) J. Cell Sci., 122, 2980–2988.

    PubMed  CAS  Google Scholar 

  120. Huveneers, S., and Danen, E. H. (2009) J. Cell Sci., 122, 1059–1069.

    PubMed  CAS  Google Scholar 

  121. Franco, S. J., and Huttenlocher, A. (2005) J. Cell Sci., 118, 3829–3838.

    PubMed  CAS  Google Scholar 

  122. Jay, P. Y., Pham, P. A., Wong, S. A., and Elson, E. L. (1995) J. Cell Sci., 108 (Pt. 1), 387–393.

    PubMed  CAS  Google Scholar 

  123. Andrew, N., and Insall, R. H. (2007) Nat. Cell Biol., 9, 193–200.

    PubMed  CAS  Google Scholar 

  124. Bosgraaf, L., and van Haastert, P. J. (2009) PLoS ONE, 4, e5253.

    PubMed  Google Scholar 

  125. Van Haastert, P. J. (2011) Sci. Signal, 4, pe6.

    PubMed  Google Scholar 

  126. Kay, R. R., Langridge, P., Traynor, D., and Hoeller, O. (2008) Nat. Rev. Mol. Cell Biol., 9, 455–463.

    PubMed  CAS  Google Scholar 

  127. Iglesias, P. A., and Devreotes, P. N. (2008) Curr. Opin. Cell Biol., 20, 35–40.

    PubMed  CAS  Google Scholar 

  128. Meinhardt, H., and Gierer, A. (2000) Bioessays, 22, 753–760.

    PubMed  CAS  Google Scholar 

  129. Bosgraaf, L., and van Haastert, P. J. (2009) PLoS ONE, 4, e6842.

    PubMed  Google Scholar 

  130. Funamoto, S., Meili, R., Lee, S., Parry, L., and Firtel, R. A. (2002) Cell, 109, 611–623.

    PubMed  CAS  Google Scholar 

  131. Merlot, S., and Firtel, R. A. (2003) J. Cell Sci., 116, 3471–3478.

    PubMed  CAS  Google Scholar 

  132. Takeda, K., Sasaki, A. T., Ha, H., Seung, H. A., and Firtel, R. A. (2007) J. Biol. Chem., 282, 11874–11884.

    PubMed  CAS  Google Scholar 

  133. Ward, S. G. (2004) Trends Immunol., 25, 67–74.

    PubMed  CAS  Google Scholar 

  134. Cai, H., Das, S., Kamimura, Y., Long, Y., Parent, C. A., and Devreotes, P. N. (2010) J. Cell Biol., 190, 233–245.

    PubMed  CAS  Google Scholar 

  135. Chen, L., Iijima, M., Tang, M., Landree, M. A., Huang, Y. E., Xiong, Y., Iglesias, P. A., and Devreotes, P. N. (2007) Dev. Cell, 12, 603–614.

    PubMed  CAS  Google Scholar 

  136. Otsuji, M., Terashima, Y., Ishihara, S., Kuroda, S., and Matsushima, K. (2010) Sci. Signal, 3, ra89.

    PubMed  CAS  Google Scholar 

  137. Van Haastert, P. J. (2010) PLoS Comput. Biol., 6, e1000874.

    Google Scholar 

  138. Charest, P. G., and Firtel, R. A. (2007) Biochem. J., 401, 377–390.

    PubMed  CAS  Google Scholar 

  139. Kolsch, V., Charest, P. G., and Firtel, R. A. (2008) J. Cell Sci., 121, 551–559.

    PubMed  CAS  Google Scholar 

  140. Heasman, S. J., and Ridley, A. J. (2008) Nat. Rev. Mol. Cell Biol., 9, 690–701.

    PubMed  CAS  Google Scholar 

  141. Alam, N., Goel, H. L., Zarif, M. J., Butterfield, J. E., Perkins, H. M., Sansoucy, B. G., Sawyer, T. K., and Languino, L. R. (2007) J. Cell Physiol., 213, 649–653.

    PubMed  CAS  Google Scholar 

  142. Wells, A., Ware, M. F., Allen, F. D., and Lauffenburger, D. A. (1999) Cell Motil. Cytoskeleton, 44, 227–233.

    PubMed  CAS  Google Scholar 

  143. Haugh, J. M. (2002) Mol. Interv., 2, 292–307.

    PubMed  CAS  Google Scholar 

  144. Welf, E. S., and Haugh, J. M. (2011) Wiley Interdiscip. Rev. Syst. Biol. Med., 3, 231–240.

    PubMed  CAS  Google Scholar 

  145. Anand-Apte, B., and Zetter, B. (1997) Stem Cells, 15, 259–267.

    PubMed  CAS  Google Scholar 

  146. Xu, J., Wang, F., van Keymeulen, A., Herzmark, P., Straight, A., Kelly, K., Takuwa, Y., Sugimoto, N., Mitchison, T., and Bourne, H. R. (2003) Cell, 114, 201–214.

    PubMed  CAS  Google Scholar 

  147. Jin, T., Zhang, N., Long, Y., Parent, C. A., and Devreotes, P. N. (2000) Science, 287, 1034–1036.

    PubMed  CAS  Google Scholar 

  148. Xiao, Z., Zhang, N., Murphy, D. B., and Devreotes, P. N. (1997) J. Cell Biol., 139, 365–374.

    PubMed  CAS  Google Scholar 

  149. Servant, G., Weiner, O. D., Neptune, E. R., Sedat, J. W., and Bourne, H. R. (1999) Mol. Biol. Cell, 10, 1163–1178.

    PubMed  CAS  Google Scholar 

  150. Ueda, M., Sako, Y., Tanaka, T., Devreotes, P., and Yanagida, T. (2001) Science, 294, 864–867.

    PubMed  CAS  Google Scholar 

  151. Janetopoulos, C., Jin, T., and Devreotes, P. (2001) Science, 291, 2408–2411.

    PubMed  CAS  Google Scholar 

  152. Xu, X., Meier-Schellersheim, M., Jiao, X., Nelson, L. E., and Jin, T. (2005) Mol. Biol. Cell, 16, 676–688.

    PubMed  CAS  Google Scholar 

  153. Hawkins, P. T., Anderson, K. E., Davidson, K., and Stephens, L. R. (2006) Biochem. Soc. Trans., 34, 647–662.

    PubMed  CAS  Google Scholar 

  154. Kundra, V., Escobedo, J. A., Kazlauskas, A., Kim, H. K., Rhee, S. G., Williams, L. T., and Zetter, B. R. (1994) Nature, 367, 474–476.

    PubMed  CAS  Google Scholar 

  155. Bailly, M., Wyckoff, J., Bouzahzah, B., Hammerman, R., Sylvestre, V., Cammer, M., Pestell, R., and Segall, J. E. (2000) Mol. Biol. Cell, 11, 3873–3883.

    PubMed  CAS  Google Scholar 

  156. Wennerberg, K., Rossman, K. L., and Der, C. J. (2005) J. Cell Sci., 118, 843–846.

    PubMed  CAS  Google Scholar 

  157. Sasaki, A. T., Chun, C., Takeda, K., and Firtel, R. A. (2004) J. Cell Biol., 167, 505–518.

    PubMed  CAS  Google Scholar 

  158. Kundra, V., Anand-Apte, B., Feig, L. A., and Zetter, B. R. (1995) J. Cell Biol., 130, 725–731.

    PubMed  CAS  Google Scholar 

  159. Janetopoulos, C., Ma, L., Devreotes, P. N., and Iglesias, P. A. (2004) Proc. Natl. Acad. Sci. USA, 101, 8951–8956.

    PubMed  CAS  Google Scholar 

  160. Meili, R., Ellsworth, C., Lee, S., Reddy, T. B., Ma, H., and Firtel, R. A. (1999) Embo J., 18, 2092–2105.

    PubMed  CAS  Google Scholar 

  161. Hirsch, E., Katanaev, V. L., Garlanda, C., Azzolino, O., Pirola, L., Silengo, L., Sozzani, S., Mantovani, A., Altruda, F., and Wymann, M. P. (2000) Science, 287, 1049–1053.

    PubMed  CAS  Google Scholar 

  162. Rickert, P., Weiner, O. D., Wang, F., Bourne, H. R., and Servant, G. (2000) Trends Cell Biol., 10, 466–473.

    PubMed  CAS  Google Scholar 

  163. Weiner, O. D., Neilsen, P. O., Prestwich, G. D., Kirschner, M. W., Cantley, L. C., and Bourne, H. R. (2002) Nat. Cell Biol., 4, 509–513.

    PubMed  CAS  Google Scholar 

  164. Parent, C. A., Blacklock, B. J., Froehlich, W. M., Murphy, D. B., and Devreotes, P. N. (1998) Cell, 95, 81–91.

    PubMed  CAS  Google Scholar 

  165. Servant, G., Weiner, O. D., Herzmark, P., Balla, T., Sedat, J. W., and Bourne, H. R. (2000) Science, 287, 1037–1040.

    PubMed  CAS  Google Scholar 

  166. Iijima, M., and Devreotes, P. (2002) Cell, 109, 599–610.

    PubMed  CAS  Google Scholar 

  167. Iijima, M., Huang, Y. E., Luo, H. R., Vazquez, F., and Devreotes, P. N. (2004) J. Biol. Chem., 279, 16606–16613.

    PubMed  CAS  Google Scholar 

  168. Liliental, J., Moon, S. Y., Lesche, R., Mamillapalli, R., Li, D., Zheng, Y., Sun, H., and Wu, H. (2000) Curr. Biol., 10, 401–404.

    PubMed  CAS  Google Scholar 

  169. Nishio, M., Watanabe, K., Sasaki, J., Taya, C., Takasuga, S., et al. (2007) Nat. Cell Biol., 9, 36–44.

    PubMed  CAS  Google Scholar 

  170. Cantley, L. C., and Neel, B. G. (1999) Proc. Natl. Acad. Sci. USA, 96, 4240–4245.

    PubMed  CAS  Google Scholar 

  171. Sasaki, A. T., Janetopoulos, C., Lee, S., Charest, P. G., Takeda, K., Sundheimer, L. W., Meili, R., Devreotes, P. N., and Firtel, R. A. (2007) J. Cell Biol., 178, 185–191.

    PubMed  CAS  Google Scholar 

  172. Van Haastert, P. J., Keizer-Gunnink, I., and Kortholt, A. (2007) J. Cell Biol., 177, 809–816.

    PubMed  Google Scholar 

  173. Hoeller, O., and Kay, R. R. (2007) Curr. Biol., 17, 813–817.

    PubMed  CAS  Google Scholar 

  174. Cathcart, M. K. (2009) J. Lipid Res., 50 (Suppl.), S231–236.

    Google Scholar 

  175. Mishra, R. S., Carnevale, K. A., and Cathcart, M. K. (2008) J. Exp. Med., 205, 347–359.

    PubMed  CAS  Google Scholar 

  176. Moolenaar, W. H. (1999) Exp. Cell Res., 253, 230–238.

    PubMed  CAS  Google Scholar 

  177. Kim, J. H., and Adelstein, R. S. (2011) J. Cell Physiol., epub ahead of print, DOI 10.1002/jcp. 22631.

  178. Simons, K., and Gerl, M. J. (2010) Nat. Rev. Mol. Cell Biol., 11, 688–699.

    PubMed  CAS  Google Scholar 

  179. Shmelzer, Z., Haddad, N., Admon, E., Pessach, I., Leto, T. L., Eitan-Hazan, Z., Hershfinkel, M., and Levy, R. (2003) J. Cell Biol., 162, 683–692.

    PubMed  CAS  Google Scholar 

  180. Veltman, D. M., Keizer-Gunnik, I., and van Haastert, P. J. (2008) J. Cell Biol., 180, 747–753.

    PubMed  CAS  Google Scholar 

  181. Lemmon, M. A. (2008) Nat. Rev. Mol. Cell Biol., 9, 99–111.

    PubMed  CAS  Google Scholar 

  182. Li, Z., Hannigan, M., Mo, Z., Liu, B., Lu, W., Wu, Y., Smrcka, A. V., Wu, G., Li, L., Liu, M., Huang, C. K., and Wu, D. (2003) Cell, 114, 215–227.

    PubMed  CAS  Google Scholar 

  183. Welch, H. C., Coadwell, W. J., Stephens, L. R., and Hawkins, P. T. (2003) FEBS Lett., 546, 93–97.

    PubMed  CAS  Google Scholar 

  184. Monypenny, J., Zicha, D., Higashida, C., Oceguera-Yanez, F., Narumiya, S., and Watanabe, N. (2009) Mol. Cell Biol., 29, 2730–2747.

    PubMed  CAS  Google Scholar 

  185. Pankov, R., Endo, Y., Even-Ram, S., Araki, M., Clark, K., Cukierman, E., Matsumoto, K., and Yamada, K. M. (2005) J. Cell Biol., 170, 793–802.

    PubMed  CAS  Google Scholar 

  186. Kraynov, V. S., Chamberlain, C., Bokoch, G. M., Schwartz, M. A., Slabaugh, S., and Hahn, K. M. (2000) Science, 290, 333–337.

    PubMed  CAS  Google Scholar 

  187. Vidali, L., Chen, F., Cicchetti, G., Ohta, Y., and Kwiatkowski, D. J. (2006) Mol. Biol. Cell, 17, 2377–2390.

    PubMed  CAS  Google Scholar 

  188. Chen, L., Janetopoulos, C., Huang, Y. E., Iijima, M., Borleis, J., and Devreotes, P. N. (2003) Mol. Biol. Cell, 14, 5028–5037.

    PubMed  CAS  Google Scholar 

  189. Higuchi, M., Masuyama, N., Fukui, Y., Suzuki, A., and Gotoh, Y. (2001) Curr. Biol., 11, 1958–1962.

    PubMed  CAS  Google Scholar 

  190. Postma, M., Roelofs, J., Goedhart, J., Loovers, H. M., Visser, A. J., and van Haastert, P. J. (2004) J. Cell Sci., 117, 2925–2935.

    PubMed  CAS  Google Scholar 

  191. Manning, B. D., and Cantley, L. C. (2007) Cell, 129, 1261–1274.

    PubMed  CAS  Google Scholar 

  192. Bozulic, L., and Hemmings, B. A. (2009) Curr. Opin. Cell Biol., 21, 256–261.

    PubMed  CAS  Google Scholar 

  193. Sarbassov, D. D., Guertin, D. A., Ali, S. M., and Sabatini, D. M. (2005) Science, 307, 1098–1101.

    PubMed  CAS  Google Scholar 

  194. Zdychova, J., and Komers, R. (2005) Physiol. Res., 54, 1–16.

    PubMed  CAS  Google Scholar 

  195. Zhang, B., Ma, Y., Guo, H., Sun, B., Niu, R., Ying, G., and Zhang, N. (2009) Eur. J. Immunol., 39, 894–901.

    PubMed  CAS  Google Scholar 

  196. Morales-Ruiz, M., Fulton, D., Sowa, G., Languino, L. R., Fujio, Y., Walsh, K., and Sessa, W. C. (2000) Circ. Res., 86, 892–896.

    PubMed  CAS  Google Scholar 

  197. Enomoto, A., Murakami, H., Asai, N., Morone, N., Watanabe, T., Kawai, K., Murakumo, Y., Usukura, J., Kaibuchi, K., and Takahashi, M. (2005) Dev. Cell, 9, 389–402.

    PubMed  CAS  Google Scholar 

  198. Lee, S., Comer, F. I., Sasaki, A., McLeod, I. X., Duong, Y., Okumura, K., Yates, J. R., 3rd, Parent, C. A., and Firtel, R. A. (2005) Mol. Biol. Cell, 16, 4572–4583.

    PubMed  CAS  Google Scholar 

  199. Kamimura, Y., Xiong, Y., Iglesias, P. A., Hoeller, O., Bolourani, P., and Devreotes, P. N. (2008) Curr. Biol., 18, 1034–1043.

    PubMed  CAS  Google Scholar 

  200. Bosgraaf, L., and van Haastert, P. J. (2002) J. Muscle Res. Cell Motil., 23, 781–791.

    PubMed  CAS  Google Scholar 

  201. Kjoller, L., and Hall, A. (1999) Exp. Cell Res., 253, 166–179.

    PubMed  CAS  Google Scholar 

  202. Loewith, R., Jacinto, E., Wullschleger, S., Lorberg, A., Crespo, J. L., Bonenfant, D., Oppliger, W., Jenoe, P., and Hall, M. N. (2002) Mol. Cell, 10, 457–468.

    PubMed  CAS  Google Scholar 

  203. Sarbassov, D. D., Ali, S. M., Kim, D. H., Guertin, D. A., Latek, R. R., Erdjument-Bromage, H., Tempst, P., and Sabatini, D. M. (2004) Curr. Biol., 14, 1296–1302.

    PubMed  CAS  Google Scholar 

  204. Jacinto, E., Loewith, R., Schmidt, A., Lin, S., Ruegg, M. A., Hall, A., and Hall, M. N. (2004) Nat. Cell Biol., 6, 1122–1128.

    PubMed  CAS  Google Scholar 

  205. Grandoch, M., Roscioni, S. S., and Schmidt, M. (2010) Br. J. Pharmacol., 159, 265–284.

    PubMed  CAS  Google Scholar 

  206. Jeon, T. J., Lee, D. J., Merlot, S., Weeks, G., and Firtel, R. A. (2007) J. Cell Biol., 176, 1021–1033.

    PubMed  CAS  Google Scholar 

  207. Yokoyama, U., Minamisawa, S., Quan, H., Akaike, T., Jin, M., Otsu, K., Ulucan, C., Wang, X., Baljinnyam, E., Takaoka, M., Sata, M., and Ishikawa, Y. (2008) Am. J. Physiol. Heart Circ. Physiol., 295, H1547–1555.

    PubMed  CAS  Google Scholar 

  208. Bolourani, P., Spiegelman, G. B., and Weeks, G. (2008) J. Biol. Chem., 283, 10232–10240.

    PubMed  CAS  Google Scholar 

  209. Bosgraaf, L., Russcher, H., Smith, J. L., Wessels, D., Soll, D. R., and van Haastert, P. J. (2002) Embo J., 21, 4560–4570.

    PubMed  CAS  Google Scholar 

  210. Veltman, D. M., and van Haastert, P. J. (2006) Mol. Biol. Cell, 17, 3921–3929.

    PubMed  CAS  Google Scholar 

  211. De la Roche, M. A., and Cote, G. P. (2001) Biochim. Biophys. Acta, 1525, 245–261.

    PubMed  Google Scholar 

  212. Fincham, V. J., James, M., Frame, M. C., and Winder, S. J. (2000) Embo J., 19, 2911–2923.

    PubMed  CAS  Google Scholar 

  213. Yang, C., and Kazanietz, M. G. (2007) Biochem. J., 403, 1–12.

    PubMed  CAS  Google Scholar 

  214. Vicente-Manzanares, M., Newell-Litwa, K., Bachir, A. I., Whitmore, L. A., and Horwitz, A. R. (2011) J. Cell Biol., 193, 381–396.

    PubMed  CAS  Google Scholar 

  215. Srinivasan, S., Wang, F., Glavas, S., Ott, A., Hofmann, F., Aktories, K., Kalman, D., and Bourne, H. R. (2003) J. Cell Biol., 160, 375–385.

    PubMed  CAS  Google Scholar 

  216. Wang, F., Herzmark, P., Weiner, O. D., Srinivasan, S., Servant, G., and Bourne, H. R. (2002) Nat. Cell Biol., 4, 513–518.

    PubMed  CAS  Google Scholar 

  217. Weiger, M. C., Wang, C. C., Krajcovic, M., Melvin, A. T., Rhoden, J. J., and Haugh, J. M. (2009) J. Cell Sci., 122, 313–323.

    PubMed  CAS  Google Scholar 

  218. Arrieumerlou, C., and Meyer, T. (2005) Dev. Cell, 8, 215–227.

    PubMed  CAS  Google Scholar 

  219. Weiger, M. C., Ahmed, S., Welf, E. S., and Haugh, J. M. (2010) Biophys. J., 98, 67–75.

    PubMed  CAS  Google Scholar 

  220. Sorkin, A., and von Zastrow, M. (2009) Nat. Rev. Mol. Cell Biol., 10, 609–622.

    PubMed  CAS  Google Scholar 

  221. Park, H. S., Lee, S. H., Park, D., Lee, J. S., Ryu, S. H., Lee, W. J., Rhee, S. G., and Bae, Y. S. (2004) Mol. Cell Biol., 24, 4384–4394.

    PubMed  CAS  Google Scholar 

  222. Jones, M. C., Caswell, P. T., and Norman, J. C. (2006) Curr. Opin. Cell Biol., 18, 549–557.

    PubMed  CAS  Google Scholar 

  223. Rappoport, J. Z., and Simon, S. M. (2003) J. Cell Sci., 116, 847–855.

    PubMed  CAS  Google Scholar 

  224. Rhee, S. G. (2006) Science, 312, 1882–1883.

    PubMed  Google Scholar 

  225. Ushio-Fukai, M. (2006) Sci. STKE, 2006, re8.

    PubMed  Google Scholar 

  226. Bedard, K., and Krause, K. H. (2007) Physiol. Rev., 87, 245–313.

    PubMed  CAS  Google Scholar 

  227. Droge, W. (2002) Physiol. Rev., 82, 47–95.

    PubMed  CAS  Google Scholar 

  228. Winterbourn, C. C., and Hampton, M. B. (2008) Free Radic. Biol. Med., 45, 549–561.

    PubMed  CAS  Google Scholar 

  229. Sundaresan, M., Yu, Z. X., Ferrans, V. J., Sulciner, D. J., Gutkind, J. S., Irani, K., Goldschmidt-Clermont, P. J., and Finkel, T. (1996) Biochem. J., 318 (Pt. 2), 379–382.

    PubMed  CAS  Google Scholar 

  230. Brown, D. I., and Griendling, K. K. (2009) Free Radic. Biol. Med., 47, 1239–1253.

    PubMed  CAS  Google Scholar 

  231. Lee, S. R., Kwon, K. S., Kim, S. R., and Rhee, S. G. (1998) J. Biol. Chem., 273, 15366–15372.

    PubMed  CAS  Google Scholar 

  232. Kwon, J., Lee, S. R., Yang, K. S., Ahn, Y., Kim, Y. J., Stadtman, E. R., and Rhee, S. G. (2004) Proc. Natl. Acad. Sci. USA, 101, 16419–16424.

    PubMed  CAS  Google Scholar 

  233. Lee, S. R., Yang, K. S., Kwon, J., Lee, C., Jeong, W., and Rhee, S. G. (2002) J. Biol. Chem., 277, 20336–20342.

    PubMed  CAS  Google Scholar 

  234. Kim, J. S., Huang, T. Y., and Bokoch, G. M. (2009) Mol. Biol. Cell, 20, 2650–2660.

    PubMed  CAS  Google Scholar 

  235. Sroka, J., and Madeja, Z. (2009) Postepy Biochem., 55, 145–152.

    PubMed  CAS  Google Scholar 

  236. Niethammer, P., Grabher, C., Look, A. T., and Mitchison, T. J. (2009) Nature, 459, 996–999.

    PubMed  CAS  Google Scholar 

  237. Li, Q., Harraz, M. M., Zhou, W., Zhang, L. N., Ding, W., Zhang, Y., Eggleston, T., Yeaman, C., Banfi, B., and Engelhardt, J. F. (2006) Mol. Cell Biol., 26, 140–154.

    PubMed  CAS  Google Scholar 

  238. Mishina, N. M., Tyurin-Kuzmin, P. A., Markvicheva, K. N., Vorotnikov, A. V., Tkachuk, V. A., Laketa, V., Schultz, C., Lukyanov, S., and Belousov, V. V. (2011) Antioxid. Redox Signal., 14, 1–7.

    PubMed  CAS  Google Scholar 

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Published in Russian in Uspekhi Biologicheskoi Khimii, 2011, Vol. 51, pp. 335–400.

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Vorotnikov, A.V. Chemotaxis: Movement, direction, control. Biochemistry Moscow 76, 1528–1555 (2011). https://doi.org/10.1134/S0006297911130104

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