Biochemistry (Moscow)

, Volume 69, Issue 9, pp 971–984 | Cite as

Protein Folding, Misfolding, and Aggregation. Formation of Inclusion Bodies and Aggresomes

  • K. A. Markossian
  • B. I. Kurganov
Article

Abstract

In this review the mechanisms of protein folding, misfolding, and aggregation as well as the mechanisms of cell defense against toxic protein aggregates are considered. Misfolded and aggregated proteins in cells are exposed to chaperonemediated refolding and are degraded by proteasomes if refolding is impossible. Proteolysis-stable protein aggregates accumulate, forming inclusion bodies. In eucaryotic cells, protein aggregates form structures in the pericentrosomal area that have been termed “aggresomes”. Formation of aggresomes in cells is a general cellular response to the presence of misfolded proteins when the degrading capacity of the cells is exceeded. The role of aggresomes in disturbance of the proteasomal system operation and in cellular death, particularly in the so-called “protein conformational diseases”, is discussed.

folding misfolding aggregation inclusion bodies aggresomes chaperones proteasomes microtubules 

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REFERENCES

  1. 1.
    Fink, A.L.(1998)Folding Des., 3, R9-R23.Google Scholar
  2. 2.
    Hurtley, S.M., and Helenius, A.(1989)Annu.Rev.Cell. Biol., 5, 277-307.PubMedGoogle Scholar
  3. 3.
    Dobson, C.M.(1999)Trends Biochem.Sci., 24, 329-332.CrossRefPubMedGoogle Scholar
  4. 4.
    Wood, J.D., Beaujeux, T.P.,and Shaw, P.J.(2003) Neuropathol.Appl.Neurobiol., 29, 529-545.CrossRefPubMedGoogle Scholar
  5. 5.
    Carrell, R.W.,and Lomas, D.A.(1997)Lancet, 350, 134-138.CrossRefPubMedGoogle Scholar
  6. 6.
    Lovestone, S.,and McLoughlin, D.M.(2001)J.Neurol. Neurosurg.Psychiatry, 72, 152-161.CrossRefGoogle Scholar
  7. 7.
    Busch, A., Engemann, S., Lurz, R., Okazawa, H., Lehrach, H.,and Wanker, E.E.(2003)J.Biol.Chem., 278, 41452-41461.CrossRefPubMedGoogle Scholar
  8. 8.
    Chai, Y.H., Koppenhafer, S.L., Shoesmith, S.J., Perez, M.K.,and Paulson, H.L.(1999)Hum.Mol.Genet., 8, 673-682.CrossRefPubMedGoogle Scholar
  9. 9.
    Prusiner, S.B.,and Hsiao, K.K.(1994)Annals Neurol., 35, 385-395.Google Scholar
  10. 10.
    Mishra, R.S., Bose, S., Gu, Y., Li, R.,and Singh, N.J. (2003)Alzheimers Dis., 5, 15-23.Google Scholar
  11. 11.
    Johnston, J.A., Dalton, M.J., Gurney, M.E.,and Kopito, R.R.(2000)Proc.Natl.Acad.Sci.USA, {vn97}, 12571-12576.CrossRefPubMedGoogle Scholar
  12. 12.
    Julien, J.P.(2001)Cell, 104, 581-591.CrossRefPubMedGoogle Scholar
  13. 13.
    Perutz, M.F.(1997)Nature, 385, 773-775.CrossRefPubMedGoogle Scholar
  14. 14.
    Johnston, J.A., Ward, C.L.,and Kopito, R.R.(1998)J. Cell Biol., 143, 1883-1898.CrossRefPubMedGoogle Scholar
  15. 15.
    Merlini, G., Bellotti, V., Andreola, A., Palladini, G., Obici, L., Casarini, S.,and Perfetti, V.(2001)Clin.Chem.Lab. Med., 39, 1065-1075.CrossRefPubMedGoogle Scholar
  16. 16.
    Anfinsen, C.B.(1973)Science, 181, 223-230.Google Scholar
  17. 17.
    Jaenicke, R.(1991)Biochemistry, 30, 3147-3161.PubMedGoogle Scholar
  18. 18.
    Finkelstein, A.V.,and Ptitsin, O.B.(2002)Physics of Proteins[in Russian ], Knizhnyi Dom, Moscow.Google Scholar
  19. 19.
    Kim, P.,and Baldwin, R.L.(1990)Annu.Rev.Biochem., 59, 631-660.CrossRefPubMedGoogle Scholar
  20. 20.
    Dill, K.A.(1989)Biochemistry, 29, 133-155.Google Scholar
  21. 21.
    Dill, K.A.,and Chan, H.S.(1997)Biochemistry, 4, 10-19.Google Scholar
  22. 22.
    Dobson, C.M., Sali, A.,and Karplus, M.(1998)Angew. Chem.Int., 37, 868 893.Google Scholar
  23. 23.
    Jaenicke, R.(1998)Biol.Chem., 379, 237-243.PubMedGoogle Scholar
  24. 24.
    Dinner, A.R., Sali, A., Smith, L.J., Dobson, C.M.,and Karplus, M.(2000)Trends Biochem.Sci., 25, 331-339.CrossRefPubMedGoogle Scholar
  25. 25.
    Hartl, F.U.(1996)Nature, 381, 571-579.CrossRefPubMedGoogle Scholar
  26. 26.
    Plaxco, K.W.,and Dobson, C.M.(1996)Curr.Opin. Struct.Biol., 6, 630-636.CrossRefPubMedGoogle Scholar
  27. 27.
    Roder, H.,and Colon, W.(1997)Curr.Opin.Struct.Biol., 7, 15-28.CrossRefPubMedGoogle Scholar
  28. 28.
    Jackson, S.E.(1998)Fold.Des., 3, R81-R91.PubMedGoogle Scholar
  29. 29.
    Dobson, C.,and Karplus, M.(1999)Curr.Opin.Struct. Biol., 9, 92-101CrossRefPubMedGoogle Scholar
  30. 30.
    Myers, J.K.,and Oas T.G.(2002)Annu.Rev.Biochem, 71, {pp783-815}.CrossRefPubMedGoogle Scholar
  31. 31.
    Van den Berg B., Ellis R.J.,and Dobson, C.M.(1999) EMBO J, 18, {pp6927-6933}.CrossRefPubMedGoogle Scholar
  32. 32.
    Frydman, J.(2001)Annu.Rev.Biochem, 70, {pp603-647}.CrossRefPubMedGoogle Scholar
  33. 33.
    Mendoza, J.A., Rogers, E., Lorimer, G.H.,and Horowitz, P.M.(1991)Biol.Chem, 266, {pp13044-13049}.Google Scholar
  34. 34.
    Nolting, B.(1999)Protein Folding Kinetics, Springer Verlag,Berlin Heidelberg New York Tokyo.Google Scholar
  35. 35.
    Nolting, B.(2000)Proteins, {vn41}, {pp288-298}.Google Scholar
  36. 36.
    Kim, P.S.,and Baldwin, R.L.(1982)Annu.Rev.Biochem, 51, {pp459-489}.CrossRefPubMedGoogle Scholar
  37. 37.
    Kim, P.S.,and Baldwin, R.L.(1990)Annu.Rev.Biochem, 59, {pp694-699}.CrossRefGoogle Scholar
  38. 38.
    Karplus, M.,and Weaver, D.L.(1994)Protein Sci., 3, {pp650-668}.PubMedGoogle Scholar
  39. 39.
    Wetlaufer, D.B.(1973)Proc.Natl.Acad.Sci.USA, 70, {pp697-701}.PubMedGoogle Scholar
  40. 40.
    Dill, K.A.(1985)Biochemisty, {vn24}, {pp1501-1509}.Google Scholar
  41. 41.
    Dill, K.A.(1990)Biochemistry, {vn29}, {pp7133-7155}.PubMedGoogle Scholar
  42. 42.
    Dill, K.A.(1990)Science, 250, {pp297-298}.PubMedGoogle Scholar
  43. 43.
    Fersht, A.R.(1995)Proc.Natl.Acad.Sci.USA, {vn92}, {pp10869-0873}.PubMedGoogle Scholar
  44. 44.
    Fersht, A.R.(1997)Curr.Opin.Struct.Biol, 7, {pp3-9}.CrossRefPubMedGoogle Scholar
  45. 45.
    Kiefhaber, T., Bachmann, A., Wildegger, G.,and Wagner, C.(1997)Biochemistry, { vn36}, {pp5108-5112}.Google Scholar
  46. 46.
    Daggett, V.,and Fersht, A.R.(2003)Trends Biochem.Sci, {vn28}, {pp18-25}.Google Scholar
  47. 47.
    Daggett, V.,and Fersht, A.R.(2003)Mol.Cell Biol, {vn4}, {pp497-502}.Google Scholar
  48. 48.
    Silow, M., Tan, Y.J., Fersht, A.R.,and Oliveberg, M. (1999)Biochemistry, {vn38}, {pp13006-13012}.CrossRefPubMedGoogle Scholar
  49. 49.
    Horwich, A.(2002)J.Clin.Invest, 110, {pp1221-1232}.CrossRefPubMedGoogle Scholar
  50. 50.
    Hartl, F.U.,and Hayer Hartl, M.(2002)Science, 295, {pp1852-1858}.CrossRefPubMedGoogle Scholar
  51. 51.
    Radford, S.E.(2000)Trends Biochem.Sci, 25, 611-618.CrossRefPubMedGoogle Scholar
  52. 52.
    Ellis, R.J.(1987)Natur, 181, {pp378-379}.CrossRefGoogle Scholar
  53. 53.
    Rothman, J.E.(1989)Cell, 59, {pp591-601}.CrossRefPubMedGoogle Scholar
  54. 54.
    Gething, M.J.,and Sambrook, J.(1992)Nature, {vn355}, {pp33-45}.CrossRefPubMedGoogle Scholar
  55. 55.
    Ellis, R.J.,and Hartl, F.U.(1996)FASEB J, 10, {pp20-26}.PubMedGoogle Scholar
  56. 56.
    Teter, S.A., Houry, W.A., Ang, D., Tradler, T., Rockabrand, D., Fischer, G., Blum, P., Georgopoulos, C., and Hartl, F.U.(1999)Cell, 97, {pp755-765}.CrossRefPubMedGoogle Scholar
  57. 57.
    Thulasiraman, V., Yang, C.F.,and Frydman, J.(1999) EMBO J, 18, {pp85-95}.CrossRefPubMedGoogle Scholar
  58. 58.
    Agashe, V.R.,and Hartl, F.U.(2000)Semin.Cell Dev. Biol, 11, {pp15-25}.CrossRefPubMedGoogle Scholar
  59. 59.
    Bukau, B., Deuerling, E., Pfund, C.,and Craig, E.A. (2000)Cell, 101, {pp119-122}.CrossRefPubMedGoogle Scholar
  60. 60.
    Houry, W.A.(2001)Curr.Protein Pept.Sci, {vn2}, {pp227-244}.Google Scholar
  61. 61.
    Panasenko, O.O., Kim, M.V.,and Gusev, N.B.(2003) Uspekhi Biol.Khim, 43, {pp59-98}.Google Scholar
  62. 62.
    Alix, J.H.,and Nierhaus, K.H.(2003)RNA, {vn9}, {pp787-793}.Google Scholar
  63. 63.
    Kramer, G., Rauch, T., Rist, W., Vorderwulbecke, S., Patzelt, H., Schulze Specking, A., Ban, N., Deuerling, E., and Bukau, B.(2002)Nature, {vn419}, {pp171-174}.CrossRefPubMedGoogle Scholar
  64. 64.
    Ghosh, J., Basu, A., Pal, S., Chowdhuri, S., Bhattacharya, A., Pal, D., Chattoraj, D.K.,and DasGupta, C.(2003) Mol.Microbiol, 48, {pp1679-1692}.CrossRefPubMedGoogle Scholar
  65. 65.
    Kolb, V.A., Makeyev, E.V.,and Spirin, A.S.(2000)J.Biol. Chem, {vn275}, {pp16597-16601}.Google Scholar
  66. 66.
    Kolb, V.A.(2001)Mol.Biol.Moscow, 35, {pp682-690}.CrossRefGoogle Scholar
  67. 67.
    Basharov, M.A.(2000)Biochemistry (Moscow), {vn65}, {pp1380-1384}.Google Scholar
  68. 68.
    Jaenicke, R.(1987)Progr.Biophys.Mol.Biol, 49, {pp117-237}.CrossRefGoogle Scholar
  69. 69.
    Creighton, T.E.(1990)Biochem.J, {vn270}, {pp1-16}.Google Scholar
  70. 70.
    Dill, K.A., Bromberg, S., Yue, K., Fiebig, K.M., Yee, D. P., Thomas, P.D.,and Chan, H.S.(1995)Protein Sci, {vn4}, {pp561-602}.Google Scholar
  71. 71.
    Basharov, M.A.(2002)Biophysics (Moscow), {vn47}, {pp989-995}.Google Scholar
  72. 72.
    Cardinale, A., Filesi, I.,and Biocca, S.(2001)Eur.J. Biochem, {vn268}, 268 277.Google Scholar
  73. 73.
    Kopito, R.R.(2000)Trends Cell Biol, 10, {pp524-530}.CrossRefPubMedGoogle Scholar
  74. 74.
    Minton, A.P.(2000)Curr.Opin.Struct.Biol, 10, {pp34-39}.CrossRefPubMedGoogle Scholar
  75. 75.
    Ellis, R.J.(2001)Curr.Opin.Struct.Biol, 11, {pp114-119}.CrossRefPubMedGoogle Scholar
  76. 76.
    Plaxco, K.W., Simons, K.T.,and Baker, D.(1998)J.Mol. Biol, 277, {pp985-994}.CrossRefPubMedGoogle Scholar
  77. 77.
    Garcia Mata, R., Bebok,Z., Sorscher, E.J.,and Sztul, E. S.(1999)J.Cell Biol, 146, {pp1239-1254}.CrossRefPubMedGoogle Scholar
  78. 78.
    Jaenicke, R.(1995)Philos.Trans.R.Soc.Lond.B Biol.Sci, 348, {pp97-105}.PubMedGoogle Scholar
  79. 79.
    De Bernardez Clark, E., Schwarz, E.,and Rudolph, R. (1999)Meth.Enzymol., 309, {pp217-236}.PubMedGoogle Scholar
  80. 80.
    Wetzel, R.(1994)Trends Biotechnol, {vn12}, {pp193-198}.Google Scholar
  81. 81.
    Haase Pettingell, C.A.,and King, J.(1988)J.Biol.Chem., 263, {pp4977-4983}.PubMedGoogle Scholar
  82. 82.
    Turnell, W.G.,and Finch, J.T.(1992)J.Mol.Biol., 227, 1205-1223.PubMedGoogle Scholar
  83. 83.
    Kurganov, B.I.(1998)Biochemistry (Moscow), 63, {pp364-366}.PubMedGoogle Scholar
  84. 84.
    Kurganov, B.I.(2002)Uspekhi Biol.Khim, 42, {pp89-138}.Google Scholar
  85. 85.
    Wang, K.,and Kurganov, B.I.(2003)Biophys.Chem, 106, {pp97-109}.CrossRefPubMedGoogle Scholar
  86. 86.
    Kurganov, B.I., Rafikova, E.R.,and Dobrov, E.N.(2002) Biochemistry (Moscow), 67, {pp525-533}.PubMedGoogle Scholar
  87. 87.
    Buckig, A., Tikkanen, R., Herzog, V.,and Schmitz, A. (2002)Histochem.Cell Biol, 118, {pp353-360}.CrossRefPubMedGoogle Scholar
  88. 88.
    Chiti, F., Stefani, M., Taddei, N., Ramponi, G.,and Dobson,C.M.(2003)Nature, 424, {pp805-808}.CrossRefPubMedGoogle Scholar
  89. 89.
    Vidair, C.A., Huang, R.N.,and Doxsey, S.J.(1996)Int.J. Hyperthermia, {vn12}, {pp681-695}.Google Scholar
  90. 90.
    Buchner, J.(1996)FASEB J, 10, {pp10-19}.PubMedGoogle Scholar
  91. 91.
    Wiertz, E.J., Tortorella, D., Bogyo, M., Yu, J., Mothes, W., Jones, T.R., Rapoport, T.A.,and Ploegh, H.L.(1996) Nature, 384, {pp432-438}.CrossRefPubMedGoogle Scholar
  92. 92.
    Levitskaya, J., Sharipo, A., Leonchiks, A., Ciechanover, A., and Masucci, M.G.(1997)Proc.Natl.Acad.Sci.USA, 94, 12616-12621.CrossRefPubMedGoogle Scholar
  93. 93.
    Bonifacino, J.S., Suzuki, C.K., Lippincott Schwartz, J., Weissman, A.M.,and Klausner, R.D.(1989)J.Cell Biol, 109, {pp73-83}.CrossRefPubMedGoogle Scholar
  94. 94.
    McLaurin, J., Yang, D., Yip, C.M.,and Fraser, P.E. (2000)J.Struct.Biol, 130, {pp259-270}.CrossRefPubMedGoogle Scholar
  95. 95.
    Prusiner, S.B.(1998)Proc.Natl.Acad.Sci.USA, 95, {pp13363-13383}.CrossRefPubMedGoogle Scholar
  96. 96.
    Serio, T.R.,and Lindquist, S.L.(2000)Trends Cell Biol, 10, {pp98-105}.CrossRefPubMedGoogle Scholar
  97. 97.
    Liu, Y., Gotte, G., Libonati, M.,and Eisenberg, D.(2001) Biochemistry, 8, {pp211-214}.Google Scholar
  98. 98.
    Rousseau, F., Schymkowitz, J.W., Wilkinson, H.R.,and Itzhaki, L.S.(2001)Proc.Natl.Acad.Sci.USA, 98, {pp5596-5601}.CrossRefPubMedGoogle Scholar
  99. 99.
    Uversky, V.N., Li, J., Souillac, P., Millett, I.S., Doniach, S., Jakes, R., Goedert, M.,and Fink, A.L.(2002)J.Biol. Chem, 277, {pp11970-11978}CrossRefPubMedGoogle Scholar
  100. 100.
    Betts, S.,and King, J.(1999)Struct.Fold.Des, 7, {ppR131-R139}.CrossRefGoogle Scholar
  101. 101.
    Wetzel, R.(1996)Cell, 86, {pp699-702}.CrossRefPubMedGoogle Scholar
  102. 102.
    Jarrett, J.T.,and Lansbury, P.T., Jr.(1992)Biochemistry, 31, {pp12345-12352}.PubMedGoogle Scholar
  103. 103.
    Lansbury, P.T., Jr.(1997)Neuron, 19, {pp1151-1154}.CrossRefPubMedGoogle Scholar
  104. 104.
    Rajan, R.S., Illing, M.E., Bence, N.F.,and Kopito R.R. (2001)Proc.Natl.Acad.Sci.USA, {vn98}, {pp13060-13065}.CrossRefPubMedGoogle Scholar
  105. 105.
    Steffan, J.S., Kazantsev, A., Spasic Boskovic, O., Greenwald, M., Zhu, Y.Z., Gohler, H., Wanker, E.E., Bates, G.P., Housman, D.E.,and Thompson, L.M. (2000)Proc.Natl.Acad.Sci.USA, {vn97}, {pp6763-6768}.CrossRefPubMedGoogle Scholar
  106. 106.
    Ben Zvi, A.P.,and Goloubinoff, P.(2002).J.Biol.Chem, 277, {pp49422-49427}.CrossRefPubMedGoogle Scholar
  107. 107.
    Derkatch, I.L., Bradley, M.E., Hong, J.Y.,and Liebman, S.W.(2001)Cell, 106, {pp171-182}.CrossRefPubMedGoogle Scholar
  108. 108.
    Glover, J.R.,and Lindquist, S.(1998)Cell, 94, {pp73-82}.CrossRefPubMedGoogle Scholar
  109. 109.
    Goloubinoff, P., Mogk, A., Ben Zvi, A.P., Tomoyasu, T., and Bukau, B.(1999)Proc.Natl.Acad.Sci.USA, { vn96}, {pp13732-13737}.Google Scholar
  110. 110.
    Parsell, D.A., Kowal, A.S., Singer, M.A.,and Lindquist, S.(1994)Nature, {vn372}, {pp475-478}.CrossRefPubMedGoogle Scholar
  111. 111.
    Diamant, S., Ben Zvi, A.P., Bukau, B.,and Goloubinoff, P.(2000)J.Biol.Chem., {vn275}, {pp21107-21113}.Google Scholar
  112. 112.
    Ben Zvi, A.P.,and Goloubinoff, P.(2001)J.Struct.Biol, 135, {pp84-93}.CrossRefPubMedGoogle Scholar
  113. 113.
    Diamant, S., Rosenthal, D., Azem, A., Eliahu, N., Ben Zvi, A.P.,and Goloubinoff, P.(2003)Mol.Microbiol, 4vn9, {pp401-404}.Google Scholar
  114. 114.
    Sakahira, H., Breuer, P., Hayer Hartl, M.K.,and Hartl, F. U.(2002)Proc.Natl.Acad.Sci.USA, 99, {pp16412-16418}.CrossRefGoogle Scholar
  115. 115.
    Mogk,A., Tomoyasu,T., Goloubinoff,P., Rudiger,S., Roder,D., Langen,H.,and Bukau,B.(1999)EMBO J., 18, {pp6934-6949}.CrossRefPubMedGoogle Scholar
  116. 116.
    Schiene Fischer,C., Habazettl,J., Schmid, F.X.,and Fischer,G.(2002)Nat.Struct.Biol., {vn9}, {pp419-424}.Google Scholar
  117. 117.
    Carrio, M.M.,and Villaverde,A.(2003)FEBS Lett., 537, {pp215-221}.CrossRefPubMedGoogle Scholar
  118. 118.
    DebBurman, S.K., Raymond G.J., Caughey, B.,and Lindquist, S.(1997)Proc.Natl.Acad.Sci.USA, 94, {pp13938-13943}.CrossRefGoogle Scholar
  119. 119.
    Stockel, J.,and Hartl, F.U.(2001)J.Mol.Biol, 313, {pp861-872}.CrossRefPubMedGoogle Scholar
  120. 120.
    Garrido,C., Gurbuxani,S., Ravagnan,L.,and Kroemer, G.(2001)Biochem.Biophys.Res.Commun., 286, {pp433-442}.CrossRefPubMedGoogle Scholar
  121. 121.
    Soti,C.,and Csermely,P.(2000)Biogerontology, {vn1}, {pp225-233}.Google Scholar
  122. 122.
    Chan,W., Helms, L.R., Brooks,I., Lee,G., Ngola,S., McNulty,D., Maleef,B., Hensley,P.,and Wetzel,R. (1996)Folding Des, {vn1}, {pp77-89}.Google Scholar
  123. 123.
    Carrio, M.M.,and Villaverde,A.(2002)J.Biotechnol, {vn96}, {pp3-12}.Google Scholar
  124. 124.
    Kane, J.F.,and Hartley, D.L.(1988)Trends Biotechnol, {vn6}, {pp95-101}.Google Scholar
  125. 125.
    Speed, M.A., Wang, D.I.,and King,J.(1996)Nat. Biotechnol, {vn14}, {pp1283-1287}.Google Scholar
  126. 126.
    Carrio, M.M., Corchero, J.L.,and Villaverde,A.(1998) FEMS Microbiol.Lett., 169, {pp9-15}.CrossRefPubMedGoogle Scholar
  127. 127.
    Carrio, M.M.,and Villaverde,A.(2001)FEBS Lett., 489, {pp29-33}.CrossRefPubMedGoogle Scholar
  128. 128.
    Villaverde,A.,and Carrio, M.M.(2003)Biotechnol.Lett., 25, {pp1385-1395}.CrossRefPubMedGoogle Scholar
  129. 129.
    Hammond,C.,and Helenius,A.(1995)Curr.Opin.Cell. Biol., 7, {pp523-529}.CrossRefPubMedGoogle Scholar
  130. 130.
    Brodsky, J.L.,and McCracken, A.A.(1999)Semin.Cell Dev.Biol, 10, {pp507-513}.CrossRefPubMedGoogle Scholar
  131. 131.
    Imai,J., Yashiroda,H., Maruya,M., Yahara,I.,and Tanaka,K.(2003)Cell Cycle, {vn2}, {pp585-590}.Google Scholar
  132. 132.
    Ellgaard,L.,and Helenius,A.(2001)Curr.Opin.Cell Biol., 13, {pp431-437}.CrossRefPubMedGoogle Scholar
  133. 133.
    Werner, E.D., Brodsky, J.L.,and McCracken, A.A.(1996)Proc.Natl.Acad.Sci.USA, 93, {pp13797-13801}.CrossRefPubMedGoogle Scholar
  134. 134.
    Luzikov, V.N.(2002)Biochemistry(Moscow), 67, {pp171-183}.PubMedGoogle Scholar
  135. 135.
    Corsi, A.K.,and Schekman,R.(1996)J.Biol.Chem., 271, {pp30299-30302}.CrossRefPubMedGoogle Scholar
  136. 136.
    Plemper, R.K.,and Wolf, D.H.(1999)Mol.Biol.Rep., 26, {pp125-130}.CrossRefPubMedGoogle Scholar
  137. 137.
    Johnson, A.E.,and Haigh, N.G.(2000)Cell, 102, {pp709-712}.CrossRefPubMedGoogle Scholar
  138. 138.
    Yu,H.,and Kopito, R.R.(1999)J.Biol.Chem., {vn274}, {pp36852-36858}.Google Scholar
  139. 139.
    Kopito, R.R.(1997)Cell, 88, {pp427-430}.CrossRefPubMedGoogle Scholar
  140. 140.
    Gelman, M.S., Kannegaard, E.S.,and Kopito, R.R. (2002)J.Biol.Chem., 277, {pp11709-11714}.CrossRefPubMedGoogle Scholar
  141. 141.
    Ward, C.L., Omura,S.,and Kopito, R.R.(1995)Cell, 83, {pp121-127}.CrossRefPubMedGoogle Scholar
  142. 142.
    Fayadat,L., Niccoli Sire,P., Lanet,J.,and Franc, J.L. (1998)Endocrinology, 139, {pp4277-4285}.CrossRefPubMedGoogle Scholar
  143. 143.
    Petaja Repo, U.E., Hogue,M., Laperriere,A., Walker,P., and Bouvier,M.(2000)J.Biol.Chem., {vn275}, {pp13727-13736}.Google Scholar
  144. 144.
    Couve,A., Filippov, A.K., Connolly, C.N., Bettler,B., Brown, D.A.,and Moss, S.J.(1998)J.Biol.Chem., 273, {pp26361-26367}.CrossRefPubMedGoogle Scholar
  145. 145.
    Chen,C., Bonifacino, J.S., Yuan, L.C.,and Klausner, R. D.(1988)J.Cell Biol, 107, {pp2149-2161}.CrossRefPubMedGoogle Scholar
  146. 146.
    Schubert,U., Anton, L.C., Gibbs,J., Norbury, C.C., Yewdell, J.W.,and Bennink, J.R.(2000)Nature, 404, {pp770-774}.CrossRefPubMedGoogle Scholar
  147. 147.
    Rock, K.L., Gramm,C., Rothstein,L., Clark,K., Stein, R., Dick,L., Hwang,D.,and Goldberg, A.L.(1994)Cell, 78, {pp761-771}.CrossRefPubMedGoogle Scholar
  148. 148.
    Palmer,A., RivettGoogle Scholar

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© MAIK “Nauka/Interperiodica” 2004

Authors and Affiliations

  • K. A. Markossian
    • 1
  • B. I. Kurganov
    • 1
  1. 1.Russian Academy of SciencesBach Institute of BiochemistryMoscowRussia

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