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Journal of Bioenergetics and Biomembranes

, Volume 36, Issue 1, pp 35–45 | Cite as

Extreme Secretion: Protein Translocation Across the Archaeal Plasma Membrane

  • Gabriela Ring
  • Jerry Eichler
Article

Abstract

In all three domains of life, extracytoplasmic proteins must overcome the hurdle presented by hydrophobic, lipid-based membranes. While numerous aspects of the protein translocation process have been well studied in bacteria and eukarya, little is known about how proteins cross the membranes of archaea. Analysis to date suggests that archaeal protein translocation is a mosaic of bacterial, eukaryal, and archaeal features, as indeed is much of archaeal biology. Archaea encode homologues of selected elements of the bacterial and eukaryal translocation machines, yet lack other important components of these two systems. Other aspects of the archaeal translocation process appear specific to this domain, possibly related to the extreme environmental conditions in which archaea thrive. In the following, current understanding of archaeal protein translocation is reviewed, as is recent progess in reconstitution of the archaeal translocation process in vitro.

Archaea inverted membrane vesicles protein secretion protein translation protein translocation signal peptidase translocon 

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References

  1. Akimaru, J., Matsuyama, S., Tokuda, H., and Mizushima, S. (1991). Proc. Natl. Acad. Sci. U.S.A. 88, 6545-6549.Google Scholar
  2. Albers, S. V., and Driessen, A. M. (2002). Arch. Microbiol. 177, 209-216.Google Scholar
  3. Arkowitz, R. A., and Wickner, W. (1994). EMBO J. 13, 954-963.Google Scholar
  4. Arndt, E. (1992). Biochim. Biophys. Acta 1130, 113-116.Google Scholar
  5. Auer, J., Spicker, G., and Bock, A. (1991). Biochimie 73, 683-688.Google Scholar
  6. Ban, N., Nissen, P., Hansen, J., Moore, P. B., and Steitz, T. A. (2000). Science 289, 905-920.Google Scholar
  7. Brady, S. L., Eichler, J., and Jarrell, K. F. (2003). Protein Sci. 12, 1833-1843.Google Scholar
  8. Bayley, S. T., and Griffiths, E. (1968). Biochemistry 7, 2249-2256.Google Scholar
  9. Becher, B., and Muller, V. (1994). J. Bacteriol. 176, 2543-2550.Google Scholar
  10. Berks, B. C. (1996). Mol. Microbiol. 22, 393-404.Google Scholar
  11. Berks, B. C., Sargent, F., De Leeuw, E., Hinsley, A. P., Stanley, N. R., Jack, R. L., Buchanan, G., and Palmer, T. (2000). Biochim. Biophys. Acta 1459, 325-330.Google Scholar
  12. Bhuiyan, S. H., Gowda, K., Hotokezaka, H., and Zwieb, C. (2000). Nucleic Acids Res. 28, 1365-1373.Google Scholar
  13. Blobel, G., and Dobberstein, B. (1975). J. Cell Biol. 67, 835-851.Google Scholar
  14. Bogomolni, R. A., Taylor, M. E., and Stoeckenius, W. (1984). Proc. Natl. Acad. Sci. U.S.A. 81, 5408-5411.Google Scholar
  15. Bogsch, E., Brink, S., and Robinson, C. (1997). EMBO J. 16, 3851-3859.Google Scholar
  16. Bogsch, E. G., Sargent, F., Stanley, N. R., Berks, B. C., Robinson, C., and Palmer, T. (1998). J. Biol. Chem. 273, 18003-18006.Google Scholar
  17. Bolhuis, A. (2002). Microbiology 148, 3335-3346.Google Scholar
  18. Bolhuis, A., Broekhuizen, C. P., Sorokin, A., van Roosmalen, M. L., Venema, G., Bron, S., Quax, W. J., and van Dijl, J. M. (1998). J. Biol. Chem. 273, 21217-21224.Google Scholar
  19. Brock, I. W., Mills, J. D., Robinson, D., and Robinson, C. (1995). J. Biol. Chem. 270, 1657-1662.Google Scholar
  20. Brundage, L., Fimmel, C. J., Mizushima, S., and Wickner, W. (1992). J. Biol. Chem. 267, 4166-4170.Google Scholar
  21. Brundage, L., Hendrick, J. P., Schiebel, E., Driessen, A. J., and Wickner, W. (1990). Cell 62, 649-657.Google Scholar
  22. Cammarano, P., Teichner, A., Chinali, G., Londei, P., de Rosa, M., Gambacorta, A., and Nicolaus, B. (1982). FEBS Lett. 148, 255-259.Google Scholar
  23. Cao, T. B., and Saier, M. H., Jr. (2003). Biochim. Biophys. Acta 1609, 115Google Scholar
  24. Chen, M., Samuelson, J. C., Jiang, F., Muller, M., Kuhn, A., and Dalbey, R. E. (2002). J. Biol. Chem. 277, 7670-7675.Google Scholar
  25. Chung, Y. J., Krueger, C., Metzgar, D., and Saier, M. H., Jr. (2001). J. Bacteriol. 183, 1012-Google Scholar
  26. Cline, K., Ettinger, W. F., and Theg, S. M. (1992). J. Biol. Chem. 267, 2688-2696.Google Scholar
  27. Condo, I., Ciammaruconi, A., Benelli, D., Ruggero, D., and Londei, P. (1999). Mol. Microbiol. 34, 377-384.Google Scholar
  28. Cristobal, S., de Gier, J. W., Nielsen, H., and von Heijne, G. (1999). EMBO J. 18, 2982-2990.Google Scholar
  29. Dalbey, R. E., Lively, M. O., Bron, S., and van Dijl, J. M. (1997). Protein Sci. 6, 1129-1138.Google Scholar
  30. Dale, H., Angevine, C. M., and Krebs, M. P. (2000). Proc. Natl. Acad. Sci. U.S.A. 97, 7847-7852.Google Scholar
  31. Dale, H., and Krebs, M. P. (1999). J. Biol. Chem. 274, 22693-22698.Google Scholar
  32. De Rosa, M., and Gambacorta, A. (1988). Prog. Lipid Res. 27, 153-175.Google Scholar
  33. de Vrije, T., de Swart, R. L., Dowhan, W., Tommassen, J., and de Kruijff, B. (1988). Nature 334, 173-175.Google Scholar
  34. Diener, J. L., and Wilson, C. (2000). Biochemistry 39, 12862-12874.Google Scholar
  35. Dilks, K., Rose, R. W., Hartmann, E., and Pohlschroder, M. (2003). J. Bacteriol. 185, 1478-1483.Google Scholar
  36. Douville, K., Leonard, M., Brundage, L., Nishiyama, K., Tokuda, H., Mizushima, S., and Wickner, W. (1994). J. Biol. Chem. 269, 18705-18707.Google Scholar
  37. Duffner, F., Bertoldo, C., Andersen, J. T., Wagner, K., and Antranikian, G. (2000). J. Bacteriol. 182, 6331-6338.Google Scholar
  38. Duong, F., and Wickner, W. (1997a). EMBO J. 16, 2756-2768.Google Scholar
  39. Duong, F., and Wickner, W. (1997b). EMBO J. 16, 4871-4879.Google Scholar
  40. Economou, A., Pogliano, J. A., Beckwith, J., Oliver, D. B., and Wickner, W. (1995). Cell 83, 1171-1181.Google Scholar
  41. Eichler, J. (2000). Eur. J. Biochem. 267, 3402-3412.Google Scholar
  42. Eichler, J. (2002). J. Mol. Evol. 54, 411-415.Google Scholar
  43. Eichler, J. (2003). Mol. Phylogenet. Evol. 27, 504-509.Google Scholar
  44. Eichler, J., and Moll, R. (2001). Trends Microbiol. 9, 130-136.Google Scholar
  45. Eichler, J., and Zwieb, C. (2002). Archaea 1, 27-34.Google Scholar
  46. Elferink, M. G., de Wit, J. G., Demel, R., Driessen, A. J., and Konings, W. N. (1992). J. Biol. Chem. 267, 1375-1381.Google Scholar
  47. Elferink, M. G., de Wit, J. G., Driessen, A. J., and Konings, W. N. (1993). Eur. J. Biochem. 214, 917-925.Google Scholar
  48. Elferink, M. G., de Wit, J. G., Driessen, A. J., and Konings, W. N. (1994). Biochim. Biophys. Acta 1193, 247-254.Google Scholar
  49. Elhardt, D., and Bock, A. (1982). Mol. Gen. Genet. 188, 128-134.Google Scholar
  50. Faguy, D. M., Jarrell, K. F., Kuzio, J., and Kalmokoff, M. L. (1994). Can. J. Microbiol. 40, 67-71.Google Scholar
  51. Gleissner, M., Elferink, M. G., Driessen, A. J., Konings, W. N., Anemuller, S., and Schafer, G. (1994). Eur. J. Biochem. 224, 983-990.Google Scholar
  52. Gorlich, D., and Rapoport, T. A. (1993). Cell 75, 615-630.Google Scholar
  53. Grill, S., Gualerzi, C. O., Londei, P., and Blasi, U. (2000). EMBO J. 19, 4101-4110.Google Scholar
  54. Gropp, R., Gropp, F., and Betlach, M. C. (1992). Proc. Natl. Acad. Sci. U.S.A. 89, 1204-1208.Google Scholar
  55. Gropp, R., and Oesterhelt, D. (1989). FEBS Lett. 259, 5-9.Google Scholar
  56. Hainzl, T., Huang, S., and Sauer-Eriksson, A. E. (2002). Nature 417, 767-771.Google Scholar
  57. Hanada, M., Nishiyama, K. I., Mizushima, S., and Tokuda, H. (1994). J. Biol. Chem. 269, 23625-23631.Google Scholar
  58. Harano, T., Nose, S., Uezu, R., Shimizu, N., and Fujiki, Y. (2001). Biochem. J. 1, 157-165.Google Scholar
  59. Hartmann, E., Sommer, T., Prehn, S., Gorlich, D., Jentsch, S., and Rapoport, T. A. (1994). Nature 367, 654-657.Google Scholar
  60. Hell, K., Neupert, W., and Stuart, R. A. (2001). EMBO J. 20, 1281-1288.Google Scholar
  61. Hendrick, J. P., and Wickner, W. (1991). J. Biol. Chem. 266, 24596-24600.Google Scholar
  62. Hojeberg, B., Lind, C., and Khorana, H. G. (1982). J. Biol. Chem. 257, 1690-1694.Google Scholar
  63. Horlacher, R., Xavier, K. B., Santos, H., DiRuggiero, J., Kossmann, M., and Boos, W. (1998). J. Bacteriol. 180, 680-689.Google Scholar
  64. Huang, K. S., Bayley, H., and Khorana, H. G. (1980). Proc. Natl. Acad. Sci. U.S.A. 77, 323-327.Google Scholar
  65. In't Veld, G., Elferink, M. G., Driessen, A. J., and Konings, W. N. (1992). Biochemistry 31, 12493-12499.Google Scholar
  66. Irihimovitch, V., and Eichler, J. (2003). J. Biol. Chem. 278, 12881-12887.Google Scholar
  67. Irihimovitch, V., Ring, G., Elkayam, T., Konrad, Z., and Eichler, J. (2003). Extremophiles 7, 71-77.Google Scholar
  68. Joly, J. C., and Wickner, W. (1993). EMBO J. 12, 255-263.Google Scholar
  69. Jorgensen, S., Vorgias, C. E., and Antranikian, G. (1997). J. Biol. Chem. 272, 16335-16342.Google Scholar
  70. Kalies, K. U., Rapoport, T. A., and Hartmann, E. (1998). J. Cell Biol. 141, 887-894.Google Scholar
  71. Kates, M. (1993). Experientia 49, 1027-1036.Google Scholar
  72. Kath, T., and Schäfer, G. (1995). Biochim. Biophys. Acta 1264, 155-158.Google Scholar
  73. Keenan, R. J., Freymann, D. M., Stroud, R. M., and Walter, P. (2001). Annu. Rev. Biochem. 70, 755-775.Google Scholar
  74. Kessel, M., Buhle, E. L., Jr., Cohen, S., and Aebi, U. (1988). J. Ultrastruct. Mol. Struct. Res. 100 Google Scholar
  75. Kinch, L. N., Saier, M. H., Jr., and Grishin, N. V. (2002). Trends Biochem. Sci. 27, 17Google Scholar
  76. Klink, F., Schumann, H., and Thomsen, A. (1983). FEBS Lett. 155, 173-177.Google Scholar
  77. Koga, Y., Nishihara, M., Morii, H., and Akagawa-Matsushita, M. (1993). Microbiol. Rev. 57, 164-182.Google Scholar
  78. Komatsu, H., and Chong, P. L. (1998). Biochemistry 37, 107-115.Google Scholar
  79. Koshland, D., and Botstein, D. (1982). Cell 30, 893-902.Google Scholar
  80. Krebs, M. P., and Isenbarger, T. A. (2000). Biochim. Biophys. Acta 1460, 15-26.Google Scholar
  81. Kusters, R., Breukink, E., Gallusser, A., Kuhn, A., and de Kruijff, B. (1994). J. Biol. Chem. 269, 1560-1563.Google Scholar
  82. Kusters, R., Dowhan, W., and de Kruijff, B. (1991). J. Biol. Chem. 266, 8659-8662.Google Scholar
  83. Lill, R., Dowhan, W., and Wickner, W. (1990). Cell 60, 271-280.Google Scholar
  84. Londei, P., Altamura, S., Cammarano, P., and Petrucci, L. (1986). Eur. J. Biochem. 157, 455-462.Google Scholar
  85. Luirink, J., Samuelsson, T., and de Gier, J. W. (2001). FEBS Lett. 50, 1-5.Google Scholar
  86. Macara, I. G. (2001). Microbiol. Mol. Biol. Rev. 65, 570-594.Google Scholar
  87. Macario, A. J., Lange, M., Ahring, B. K., and de Macario, E. C. (1999). Microbiol. Mol. Biol. Rev. 63, 923-967.Google Scholar
  88. Maeshima, H., Okuno, E., Aimi, T., Morinaga, T., and Itoh, T. (2001). FEBS Lett. 507, 336-340.Google Scholar
  89. Manting, E. H., and Driessen, A. J. (2000). Mol. Microbiol. 37, 226-238.Google Scholar
  90. Matlack, K. E., Mothes, W., and Rapoport, T. A. (1998). Cell 92, 381-390.Google Scholar
  91. Matsumoto, K. (2001). Mol. Microbiol. 39, 1427-1433.Google Scholar
  92. Matsuyama, S., Fujita, Y., and Mizushima, S. (1993). EMBO J. 12, 265-270.Google Scholar
  93. Matsuyama, S., Fujita, Y., Sagara, K., and Mizushima, S. (1992). Biochim. Biophys. Acta 1122, 77-84.Google Scholar
  94. Moll, R. G. (2004). J. Bioenerg. Biomembr. 36(1), 47-53.Google Scholar
  95. Moore, M., Harrison, M. S., Peterson, E. C., and Henry, R. (2000). J. Biol. Chem. 275, 1529-1532.Google Scholar
  96. Morag, E., Lapidot, A., Govorko, D., Lamed, R., Wilchek, M., Bayer, E. A., and Shoham, Y. (1995). Appl. Environ. Microbiol. 61, 1980-1986.Google Scholar
  97. Mori, H., and Ito, K. (2001). Trends Microbiol. 9, 494-500.Google Scholar
  98. Mothes, W., Prehn, S., and Rapoport, T. A. (1994). EMBO J. 13, 3973-3982.Google Scholar
  99. Murphy, C. K., and Beckwith, J. (1994). Proc. Natl. Acad. Sci. U.S.A. 91, 2557-2561.Google Scholar
  100. Ngosuwan, J., Wang, N. M., Fung, K. L., and Chirico, W. J. (2003). J. Biol. Chem. 278, 7034-7042.Google Scholar
  101. Nielsen, H., Brunak, S., and von Heijne, G. (1999). Protein Eng. 12, 3-9.Google Scholar
  102. Ninio, S., and Schuldiner, S. (2003). J. Biol. Chem. 278, 12000-12005.Google Scholar
  103. Nishiyama, K., Hanada, M., and Tokuda, H. (1994). EMBO J. 13, 3272-3277.Google Scholar
  104. Nishiyama, K., Mizushima, S., and Tokuda, H. (1993). EMBO J. 12, 3409-3415.Google Scholar
  105. Nissen, P., Hansen, J., Ban, N., Moore, P. B., and Steitz, T. A. (2000). Science 289, 920-930.Google Scholar
  106. Nouwen, N., van der Laan, M., and Driessen, A. J. (2001). FEBS Lett. 508, 103-106.Google Scholar
  107. Ortenberg, R., and Mevarech, M. (2000). J. Biol. Chem. 275, 22839-22846.Google Scholar
  108. Oubridge, C., Kuglstatter, A., Jovine, L., and Nagai, K. (2002). Mol. Cell 9, 1251-1261.Google Scholar
  109. Paetzel, M., Dalbey, R. E., and Strynadka, N. C. (1998). Nature 396, 186-190.Google Scholar
  110. Paetzel, M., Dalbey, R. E., and Strynadka, N. C. (2000). Pharmacol. Ther. 87, 27-49.Google Scholar
  111. Pogliano, J. A., and Beckwith, J. (1994). EMBO J. 13, 554-561.Google Scholar
  112. Pohlschroder, M., Prinz, W. A., Hartmann, E., and Beckwith, J. (1997). Cell 91, 563-566.Google Scholar
  113. Qi, H. Y., Hyndman, J. B., and Bernstein, H. D. (2002). J. Biol. Chem. 277, 51077-51083.Google Scholar
  114. Randall, L. L. (1983). Cell 33, 231-240.Google Scholar
  115. Rapoport, T. A., Jungnickel, B., and Kutay, U. (1996). Annu. Rev. Biochem. 65, 271-303.Google Scholar
  116. Rapoport, T. A., Matlack, K. E., Plath, K., Misselwitz, B., and Staeck, O. (1999). Biol. Chem. 380, 1143-1150.Google Scholar
  117. Rensing, S. A., and Maier, U. G. (1994). Mol. Phylogenet. Evol. 3, 187-191.Google Scholar
  118. Rial, D. V., Arakaki, A. K., and Ceccarelli, E. A. (2000). Eur. J. Biochem. 267, 6239-6248.Google Scholar
  119. Rietveld, A. G., Koorengevel, M. C., and de Kruijff, B. (1995). EMBO J. 14, 5506-5513.Google Scholar
  120. Ring, G., and Eichler, J. (2001). J. Membr. Biol. 183, 195-204.Google Scholar
  121. Robinson, C., and Bolhuis, A. (2001). Nat. Rev. Mol. Cell Biol. 2, 350-356.Google Scholar
  122. Rose, R. W., Bruser, T., Kissinger, J. C., and Pohlschroder, M. (2002). Mol. Microbiol. 45, 943-950.Google Scholar
  123. Ruggero, D., Creti, R., and Londei, P. (1993). FEMS Microbiol. Lett. 107, 89-94.Google Scholar
  124. Samuelson, J. C., Chen, M., Jiang, F., Moller, I., Wiedmann, M., Kuhn, A., Phillips, G. J., and Dalbey, R. E. (2000). Nature 406, 637-641.Google Scholar
  125. Sanz, J. L., Marín, I., Balboa, M. A., Ureña, D., and Amils, R. (1988). Biochemistry 27, 8194-8199.Google Scholar
  126. Saruyama, H., and Nierhaus, K. (1985). FEBS Lett. 183, 390-394.Google Scholar
  127. Schafer, G., Engelhard, M., and Muller, V. (1999). Microbiol. Mol. Biol. Rev. 63, 570-620.Google Scholar
  128. Scotti, P. A., Urbanus, M. L., Brunner, J., de Gier, J. W., von Heijne, G., van der Does, C., Driessen, A. J., Oudega, B., and Luirink, J. (2000). EMBO J. 19, 542-549.Google Scholar
  129. Seehra, J. S., and Khorana, H. G. (1984). J. Biol. Chem. 259, 4187-4193.Google Scholar
  130. Smith, J. D., and Robinson, A. S. (2002). Biotechnol. Bioeng. 79, 713-723.Google Scholar
  131. Sprott, G. D. (1992). J. Bioenerg. Biomembr. 24, 555-566.Google Scholar
  132. Sumper, M., Berg, E., Mengele, R., and Strobel, I. (1990). J. Bacteriol. 172, 7111-7118.Google Scholar
  133. Tjalsma, H., Bolhuis, A., van Roosmalen, M. L., Wiegert, T., Schumann, W., Broekhuizen, C. P., Quax, W. J., Venema, G., Bron, S., and van Dijl, J. M. (1998). Genes Dev. 12, 2318-2331.Google Scholar
  134. Tozik, I., Huang, Q., Zwieb, C., and Eichler, J. (2002). Nucleic Acids Res. 30, 4166-4175.Google Scholar
  135. Tseng, T. T., Gratwick, K. S., Kollman, J., Park, D., Nies, D. H., Goffeau, A., and Saier, M. H., Jr. (1999). J. Mol. Microbiol. Biotechnol. 1, 107Google Scholar
  136. Ulbrandt, N. D., Newitt, J. A., and Bernstein, H. D. (1997). Cell 88, 187-196.Google Scholar
  137. Ungermann, C., Neupert, W., and Cyr, D. M. (1994). Science 266, 1250-1253.Google Scholar
  138. van de Vossenberg, J. L., Driessen, A. J., Grant, W. D., and Konings, W. N. (1999). Extremophiles 3, 253-257.Google Scholar
  139. von Heijne, G. (1990a). Curr. Opin. Cell Biol. 2, 604-608.Google Scholar
  140. von Heijne, G. (1990b). J. Membr. Biol. 115, 195-201.Google Scholar
  141. Wild, J., Altman, E., Yura, T., and Gross, C. A. (1992). Genes Dev. 6, 1165-1172.Google Scholar
  142. YaDeau, J. T., Klein, C., and Blobel, G. (1991). Proc. Natl. Acad. Sci. U.S.A. 88, 517-521.Google Scholar
  143. Yahr, T. L., and Wickner, W. T. (2001). EMBO J. 20, 2472-2479.Google Scholar
  144. Yamauchi, K., Doi, K., Kinoshita, M., Kii, F., and Fukuda, H. (1992). Biochim. Biophys. Acta 1110, 171-177.Google Scholar
  145. Yamauchi, K., Doi, K., Yoshida, Y., and Kinoshita, M. (1993). Biochim. Biophys. Acta 1146, 178-182.Google Scholar
  146. Yen, M. R., Harley, K. T., Tseng, Y. H., and Saier, M. H., Jr. (2001). FEMS Microbiol. Lett. 204, 223Google Scholar
  147. Yen, M. R., Tseng, Y. H., Nguyen, E. H., Wu, L. F., and Saier, M. H., Jr. (2002). Arch. Microbiol. 177, 441Google Scholar
  148. Yonath, A. (2002). Annu. Rev. Biophys. Biomol. Struct. 31, 257-273.Google Scholar
  149. Young, J. C., Hoogenraad, N. J., and Hartl, F. U. (2003). Cell 112, 41-50.Google Scholar

Copyright information

© Plenum Publishing Corporation 2004

Authors and Affiliations

  • Gabriela Ring
    • 1
  • Jerry Eichler
    • 1
  1. 1.Department of Life SciencesBen Gurion UniversityBeershevaIsrael

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