Clathrin-Mediated Endocytosis and Adaptor Proteins

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Abstract

Macromolecules gain access to the cytoplasm of eukaryotic cells using one of several ways of which clathrin-dependent endocytosis is the most researched. Although the mechanism of clathrin-mediated endocytosis is well understood in general, novel adaptor proteins that play various roles in ensuring specific regulation of the mentioned process are being discovered all the time. This review provides a detailed account of the mechanism of clathrin-mediated internalization of activated G protein-coupled receptors, as well as a description of the major proteins involved in this process.

About the authors

N. V. Popova

Shemyakin-Ovchinnikov Institute of Bioorganic Chemistry of the Russian Academy of Sciences

Author for correspondence.
Email: n.popova@gmail.com
Russian Federation

I. E. Deyev

Shemyakin-Ovchinnikov Institute of Bioorganic Chemistry of the Russian Academy of Sciences

Email: n.popova@gmail.com
Russian Federation

A. G. Petrenko

Shemyakin-Ovchinnikov Institute of Bioorganic Chemistry of the Russian Academy of Sciences

Email: n.popova@gmail.com
Russian Federation

References

  1. Pierce K.L., Premont R.T., Lefkowitz R.J. // Nat. Rev. Mol. Cell. Biol. 2002, V.3, P.639-650
  2. Ovchinnikov Yu.A. // FEBS Lett. 1982, V.148, P.179-191
  3. Clapham D.E., Neer E.J. // Nature 1993, V.365, P.403-406
  4. Oldham W.M., Hamm H.E. // Nat. Rev. Mol. Cell. Biol. 2008, V.9, P.60-71
  5. Shenoy S.K., Lefkowitz R.J. // Biochem. J. 2003, V.375, P.503-515
  6. Goodman O.B., Jr. I.O., Krupnick J.G., Santini F., Gurevich V.V., Penn R.B., Gagnon A.W., Keen J.H., Benovic J.L. // Nature 1996, V.383, P.447-450
  7. Laporte S.A., Oakley R.H., Zhang J., Holt J.A., Ferguson S.S., Caron M.G., Barak L.S. // Proc. Natl. Acad. Sci. USA. 1999, V.96, P.3712-3717
  8. Doherty G.J., McMahon H.T. // Annu. Rev. Biochem. 2009, V.78, P.857-902
  9. Calebiro D., Nikolaev V.O., Persani L., Lohse M.J. // Trends Pharmacol. Sci. 2010, V.31, P.221-228
  10. Hanyaloglu A.C., von Zastrow M. // Annu. Rev. Pharmacol. Toxicol. 2008, V.48, P.537-568
  11. Stenmark H. // Nat. Rev. Mol. Cell. Biol. 2009, V.10, P.513-525
  12. Poteryaev D., Datta S., Ackema K., Zerial M., Spang A. // Cell. 2010, V.141, P.497-508
  13. Young A. // Semin. Cell. Dev. Biol. 2007, V.18, P.448-458
  14. Ehrlich M., Boll W., van Oijen A., Hariharan R., Chandran K., Nibert M.L., Kirchhausen T. // Cell. 2004, V.118, P.591-605
  15. Ohno H., Stewart J., Fournier M.C., Bosshart H., Rhee I., Miyatake S., Saito T., Gallusser A., Kirchhausen T., Bonifacino J.S. // Science. 1995, V.269, P.1872-1875
  16. Edeling M.A., Mishra S.K., Keyel P.A., Steinhauser A.L., Collins B.M., Roth R., Heuser J.E., Owen D.J., Traub L.M. // Dev. Cell. 2006, V.10, P.329-342
  17. Honing S., Ricotta D., Krauss M., Spate K., Spolaore B., Motley A., Robinson M., Robinson C., Haucke V., Owen D.J. // Molecular Cell 2005, V.18, P.519-531
  18. Lauritsen J.P., Menne C., Kastrup J., Dietrich J., Odum N., Geisler C. // Biochim. Biophys. Acta. 2000, V.1497, P.297-307
  19. Ricotta D., Conner S.D., Schmid S.L., von Figura K., Honing S. // J. Cell. Biol. 2002, V.156, P.791-795
  20. Meyerholz A., Hinrichsen L., Groos S., Esk P.C., Brandes G., Ungewickell E.J. // Traffic. 2005, V.6, P.1225-1234
  21. Blood P.D., Voth G.A. // Proc. Natl. Acad. Sci. USA. 2006, V.103, P.15068-15072
  22. Takei K., Slepnev V.I., Haucke V., De Camilli P. // Nat. Cell. Biol. 1999, V.1, P.33-39
  23. Farsad K., Ringstad N., Takei K., Floyd S.R., Rose K., De Camilli P. // J. Cell. Biol. 2001, V.155, P.193-200
  24. Castillo P.E., Schoch S., Schmitz F., Sudhof T.C., Malenka R.C. // Nature 2002, V.415, P.327-330
  25. McMahon H.T., Boucrot E. // Nat. Rev. Mol. Cell. Biol. 2011, V.21, P.517-533
  26. Yoshida Y., Kinuta M., Abe T., Liang S., Araki K., Cremona O., Di Paolo G., Moriyama Y., Yasuda T., De Camilli P. // EMBO J. 2004, V.23, P.3483-3491
  27. Ferguson S.M., De Camilli P. // Nat. Rev. Mol. Cell. Biol. 2012, V.13, P.75-88
  28. Barouch W., Prasad K., Greene L., Eisenberg E. // Biochemistry (Mosc.). 1997, V.36, P.4303-4308
  29. Ungewickell E., Ungewickell H., Holstein S.E., Lindner R., Prasad K., Barouch W., Martin B., Greene L.E., Eisenberg E. // Nature 1995, V.378, P.632-635
  30. Ghosh P., Kornfeld S. // J. Cell. Biol. 2003, V.160, P.699-708
  31. Verstreken P., Koh T.W., Schulze K.L., Zhai R.G., Hiesinger P.R., Zhou Y., Mehta S.Q., Cao Y., Roos J., Bellen H.J. // Neuron. 2003, V.40, P.733-748
  32. Bockaert J., Fagni L., Dumuis A., Marin P. // Pharmacol Ther. 2004, V.103, P.203-221
  33. Lefkowitz R.J., Shenoy S.K. // Science. 20005, V.308, P.512-517
  34. Pitcher J.A., Freedman N.J., Lefkowitz R.J. // Annu. Rev. Biochem. 1998, V.67, P.653-692
  35. Gurevich V.V., Benovic J.L. // J. Biol. Chem. 1993, V.268, P.11628-11638
  36. Gurevich V.V., Richardson R.M., Kim C.M., Hosey M.M., Benovic J.L. // J. Biol. Chem. 1993, V.268, P.16879-16882
  37. Gurevich V.V., Dion S.B., Onorato J.J., Ptasienski J., Kim C.M., Sterne-Marr R., Hosey M.M., Benovic J.L. // J. Biol. Chem. 1995, V.270, P.720-731
  38. Gurevich V.V., Gurevich E.V. // Pharmacol. Ther. 2006, V.110, P.465-502
  39. Pearse B.M. // J. Mol. Biol. 1975, V.97, P.93-98
  40. Fotin A., Cheng Y., Sliz P., Grigorieff N., Harrison S.C., Kirchhausen T., Walz T. // Nature 2004, V.432, P.573-579
  41. Keen J.H. // Annu. Rev. Biochem. 1990, V.59, P.415-438
  42. Mueller S.C., Branton D. // J. Cell. Biol. 1984, V.98, P.341-346
  43. Wiedenhoeft R.E., Schmidt G.W., Palevitz B.A. // Plant Physiol. 1988, V.86, P.412-416
  44. Jackson A.P., Parham P. // J. Biol. Chem. 1988, V.263, P.16688-16695
  45. Ungewickell E. // EMBO J. 1983, V.2, P.1401-1408
  46. Chen C.Y., Reese M.L., Hwang P.K., Ota N., Agard D., Brodsky F.M. // EMBO J. 2002, V.21, P.6072-6082
  47. Blank G.S., Brodsky F.M. // EMBO J. 1986, V.5, P.2087-2095
  48. Blank G.S., Brodsky F.M. // J. Cell. Biol. 1987, V.105, P.2011-2019
  49. ter Haar E., Harrison S.C., Kirchhausen T. // Proc. Natl. Acad. Sci. USA. 2000, V.97, P.1096-1100
  50. Ramjaun A.R., McPherson P.S. // J. Neurochem. 1998, V.70, P.2369-2376
  51. Crowther R.A., Finch J.T., Pearse B.M. // J. Mol. Biol. 1976, V.103, P.785-798
  52. Kartenbeck J. // Cell Biol. Int. Rep. 1978, V.2, P.457-464
  53. Wakeham D.E., Chen C.Y., Greene B., Hwang P.K., Brodsky F.M. // EMBO J. 2003, V.22, P.4980-4990
  54. Greene B., Liu S.H., Wilde A., Brodsky F.M. // Traffic. 2000, V.1, P.69-75
  55. Smith C.J., Grigorieff N., Pearse B.M. // EMBO J. 1998, V.17, P.4943-4953
  56. Royle S.J. // J. Cell. Sci. 2012, V.125, P.19-28
  57. Keen J.H., Willingham M.C., Pastan I.H. // Cell. 1979, V.16, P.303-312
  58. Schmid S.L. // Annu. Rev. Biochem. 1997, V.66, P.511-548
  59. Gallusser A., Kirchhausen T. // EMBO J. 1993, V.12, P.5237-5244
  60. Stepp J.D., Pellicena-Palle A., Hamilton S., Kirchhausen T., Lemmon S.K. // Mol. Biol. Cell. 1995, V.6, P.41-58
  61. Simpson F., Peden A.A., Christopoulou L., Robinson M.S. // J. Cell. Biol. 1997, V.137, P.835-845
  62. DellíAngelica E.C., Mullins C., Bonifacino J.S. // J. Biol. Chem. 1999, V.274, P.7578-7285
  63. Robinson M.S., Bonifacino J.S. // Curr. Opin. Cell. Biol. 2001, V.13, P.444-453
  64. Aridor M., Traub L.M. // Traffic. 2002, V.3, P.537-546
  65. Wilbur J.D., Hwang P.K., Brodsky F.M. // Traffic. 2005, V.6, P.346-350
  66. Peden A.A., Oorschot V., Hesser B.A., Austin C.D., Scheller R.H., Klumperman J. // J. Cell. Biol. 2004, V.164, P.1065-1076
  67. Bonifacino J.S., Traub L.M. // Annu. Rev. Biochem. 2003, V.72, P.395-447
  68. Hofmann M.W., Honing S., Rodionov D., Dobberstein B., von Figura K., Bakke O. // J. Biol. Chem. 1999, V.274, P.36153-36158
  69. Honing S., Sandoval I.V., von Figura K. // EMBO J. 1998, V.17, P.1304-1314
  70. Maldonado-Baez L., Wendland B. // Trends Cell Biol. 2006, V.16, P.505-513
  71. Owen D.J., Collins B.M., Evans P.R. // Annu. Rev. Cell.Dev. Biol. 2004, V.20, P.153-191
  72. Ahle S., Ungewickell E. // J. Cell. Biol. 1990, V.111, P.19-29
  73. Ungewickell E., Ungewickell H., Holstein S.E. // J. Biol. Chem. 1997, V.272, P.19594-19600
  74. Lee D.W., Wu X., Eisenberg E., Greene L.E. // J. Cell Sci. 2006, V.119, P.3502-3512
  75. Massol R.H., Boll W., Griffin A.M., Kirchhausen T. // Proc. Natl. Acad. Sci. USA. 2006, V.103, P.10265-10270
  76. Scheele U., Kalthoff C., Ungewickell E. // J. Biol. Chem. 2001, V.276, P.36131-36138
  77. Newmyer S.L., Christensen A., Sever S. // Dev. Cell. 2003, V.4, P.929-940
  78. Smith C.J., Dafforn T.R., Kent H., Sims C.A., Khubchandani-Aswani K., Zhang L., Saibil H.R., Pearse B.M. // J. Mol. Biol. 2004, V.336, P.461-471
  79. Fotin A., Cheng Y., Grigorieff N., Walz T., Harrison S.C., Kirchhausen T. // Nature 2004, V.432, P.649-653
  80. Greene L.E., Eisenberg E. // J. Biol. Chem. 1990, V.265, P.6682-6687
  81. Barouch W., Prasad K., Greene L.E., Eisenberg E. // J. Biol. Chem. 1994, V.269, P.28563-28569
  82. Ma Y., Greener T., Pacold M.E., Kaushal S., Greene L.E., Eisenberg E. // J. Biol. Chem. 2002, V.277, P.49267-49274
  83. Hartl F.U., Hayer-Hartl M. // Science. 2002, V.295, P.1852-1858
  84. Rapoport I., Boll W., Yu A., Bocking T., Kirchhausen T. // Mol. Biol. Cell. 2008, V.19, P.405-413
  85. Xing Y., Bocking T., Wolf M., Grigorieff N., Kirchhausen T., Harrison S.C. // EMBO J. 2010, V.29, P.655-665
  86. Robinson M.S. // Trends Cell Biol. 2004, V.14, P.167-174
  87. Aguilar R.C., Watson H.A., Wendland B. // J. Biol. Chem. 2003, V.278, P.10737-10743
  88. Wolfe B.L., Trejo J. // Traffic. 2007, V.8, P.462-470
  89. Polo S., Di Fiore P.P. // Cell. 2006, V.124, P.897-900
  90. Le Borgne R. // Curr. Opin. Cell. Biol. 2006, V.18, P.213-222
  91. Hutterer A., Knoblich J.A. // EMBO Rep. 2005, V.6, P.836-842
  92. Horvath C.A., Vanden Broeck D., Boulet G.A., Bogers J., De Wolf M.J. // Int. J. Biochem. Cell. Biol. 2007, V.39, P.1765-1770
  93. Morgan J.R., Zhao X., Womack M., Prasad K., Augustine G.J., Lafer E.M. // J. Neurosci. 1999, V.19, P.10201-10212
  94. Zhang B., Koh Y.H., Beckstead R.B., Budnik V., Ganetzky B., Bellen H.J. // Neuron. 1998, V.21, P.1465-1475
  95. Bushlin I., Petralia R.S., Wu F., Harel A., Mughal M.R., Mattson M.P., Yao P.J. // J. Neurosci. 2008, V.28, P.10257-10271
  96. Chen S., Liang M.C., Chia J.N., Ngsee J.K., Ting A.E. // J. Biol. Chem. 2001, V.276, P.13209-13216
  97. Blatch G.L., Lassle M. // Bioessays. 1999, V.21, P.932-939
  98. DíAndrea L.D., Regan L. // Trends Biochem. Sci. 2003, V.28, P.655-662
  99. Santoro B., Wainger B.J., Siegelbaum S.A. // J. Neurosci. 2004, V.24, P.10750-10762
  100. Amery L., Sano H., Mannaerts G.P., Snider J., van Looy J., Fransen M., van Veldhoven P.P. // Biochem. J. 2001, V.357, P.635-646
  101. Zolles G., Wenzel D., Bildl W., Schulte U., Hofmann A., Muller C.S., Thumfart J.O., Vlachos A., Deller T., Pfeifer A. // Neuron. 2009, V.62, P.814-825
  102. Popova N.V., Plotnikov A., Deev I.E., Petrenko A.G. // Dokl. Biochem. Biophys. 2007, V.414, P.149-151
  103. Popova N.V., Plotnikov A.N., Ziganshin R., Deyev I.E., Petrenko A.G. // Biochemistry (Mosc.). 2008, V.73, P.644-651
  104. Santoro B., Grant S.G., Bartsch D., Kandel E.R. // Proc. Natl. Acad. Sci. USA. 1997, V.94, P.14815-14820
  105. Ludwig A., Zong X., Jeglitsch M., Hofmann F., Biel M. // Nature 1998, V.393, P.87-591
  106. Santoro B., Liu D.T., Yao H., Bartsch D., Kandel E.R., Siegelbaum S.A., Tibbs G.R. // Cell. 1998, V.93, P.717-729
  107. DiFrancesco D. // Annu. Rev. Physiol. 1993, V.55, P.455-472
  108. Robinson R.B., Siegelbaum S.A. // Annu. Rev. Physiol. 2003, V.65, P.453-480
  109. Lewis A.S., Schwartz E., Chan C.S., Noam Y., Shin M., Wadman W.J., Surmeier D.J., Baram T.Z., Macdonald R.L., Chetkovich D.M. // J. Neurosci. 2009, V.29, P.6250-6265
  110. Santoro B., Piskorowski R.A., Pian P., Hu L., Liu H., Siegelbaum S.A. // Neuron. 2009, V.62, P.802-813
  111. Han Y., Noam Y., Lewis A.S., Gallagher J.J., Wadman W.J., Baram T.Z., Chetkovich D.M. // J. Biol. Chem. 2011, V.286, P.20823-20834
  112. Santoro B., Hu L., Liu H., Saponaro A., Pian P., Piskorowski R.A., Moroni A., Siegelbaum S.A. // J. Neurosci. 2011, V.31, P.4074-4086
  113. Popova N.V., Deyev I.E., Petrenko A.G. // J. Neurochem. 2011, V.118, P.988-998
  114. Piskorowski R., Santoro B., Siegelbaum S.A. // Neuron. 2011, V.70, P.495-509
  115. Lewis A.S., Vaidya S.P., Blaiss C.A., Liu Z., Stoub T.R., Brager D.H., Chen X., Bender R.A., Estep C.M., Popov A.B. // J. Neurosci. 2011, V.31, P.7424-7440

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