Synthesis, Assembly, and Intracellular Transport of Bunyaviridae Membrane Proteins

  • Ralf F. Pettersson
  • Lars Melin
Part of the The Viruses book series (VIRS)


One of the original criteria for classifying, in the early 1970s, a diverse collection of serologically related and unrelated arthropod-borne viruses into a new family, Bunyaviridae, was the site of maturation (budding) in a perinuclear region, later unambiguously shown to represent the Golgi complex (Murphy et al., 1973; Kuismanen et al., 1982). With only one documented exception (Anderson and Smith, 1987), all members of this large family studied so far have been found to mature in this intracellular organelle, raising the intriguing question of the molecular and cell biological mechanisms underlying this process.


Golgi Complex Cytoplasmic Tail Protein Disulfide Isomerase Tomato Spotted Wilt Virus Virus Glycoprotein 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Anderson, G. W., Jr., and Smith, J. F., 1987, Immunoelectron microscopy of Rift Valley fever viral morphogenesis in primary rat hepatocytes, Virology 161:91.PubMedGoogle Scholar
  2. Antic, D., Kang, C. Y., Spik, K., Schmaljohn, C., Vapalahti, O., and Vaheri, A., 1992a, Comparison of the deduced gene products of the L, M and S genome segments of hantaviruses, Virus Res. 24:35.PubMedGoogle Scholar
  3. Antic, D., Wright, K. E., and Kang, C. Y., 1992b, Maturation of Hantaan virus glycoproteins G1 and G2, Virology 189:324.PubMedGoogle Scholar
  4. Arikawa, J., Schmaljohn, A. L., Dalrymple, J. M., and Schmaljohn, C. S., 1989, Characterization of Hantaan virus envelope glycoprotein antigenic determinants defined by monoclonal antibodies, J. Gen. Virol. 70:615.PubMedGoogle Scholar
  5. Armstrong, J., and Patel, S., 1991, The Golgi sorting domain of coronavirus El protein, J. Cell Sci. 98:567.PubMedGoogle Scholar
  6. Bardwell, J. C. A., and Beckwith, J., 1993, The bonds that tie: Catalyzed disulfide bond formation, Cell 74:769.PubMedGoogle Scholar
  7. Bause, E., 1983, Structural requirements of N-glycosylation of proteins, Biochem. J. 209:331.PubMedGoogle Scholar
  8. Bergmann, C. C., Maass, D., Poruchynsky, M. S., Atkinson, P. H., and Bellamy, A. R., 1989, The topology of the non-structural rotavirus receptor glycoprotein NS28 in the rough endoplasmic reticulum, EMBO J. 8:1695.PubMedGoogle Scholar
  9. Bishop, D. H. L., and Shope, R. E., 1979, Bunyaviridae, Compr. Virol. 14:1.Google Scholar
  10. Booth, T. F., Gould, E. A., and Nuttall, P. A., 1991, Structure and morphogenesis of Dugbe virus (Bunyaviridae, Nairovirus) studied by immunogold electron microscopy of ultrathin cryosections, Virus Res. 21:199.PubMedGoogle Scholar
  11. Bouloy, M., 1991, Bunyaviridae: Genome organization and replication strategies, Adv. Virus Res. 40:235.PubMedGoogle Scholar
  12. Bupp, K., Prabakaran, I., Nathanson, N., and Gonzalez-Scarano, F., 1994, Expression of La Crosse virus glycocprotein G1 alone is insufficient for its proper Golgi targeting, Scientific Program and Abstracts book of the 13th Annual Meeting of the American Society for Virology.Google Scholar
  13. Burke, J., Pettitt, J. M., Schachter, H., Sarkar, M., and Gleeson, P. A., 1992, The transmembrane and flanking sequences of β-l,2-N-acetylglucosaminyltransferase I specify medial-Golgi localization, J. Biol. Chem. 267:24433.PubMedGoogle Scholar
  14. Cash, P., 1982, Inhibition of LaCrosse virus replication by monensin, a monovalent ionophore, J. Gen. Virol. 59:193.PubMedGoogle Scholar
  15. Cash, P., 1985, Polypeptide synthesis of Dugbe virus, a member of the Nairovirus genus of the Bunyaviridae, J. Gen. Virol. 66:141.PubMedGoogle Scholar
  16. Chen, S.-Y., and Compans, R. W., 1991, Oligomerization, transport, and Golgi-retention of Punta Toro virus glycoproteins, J. Virol. 65:5902.PubMedGoogle Scholar
  17. Chen, S.-Y., Matsuoka, Y., and Compans, R. W., 1991a, Assembly and polarized release of Punta Toro virus and effects of brefeldin A, J. Virol. 65:1427.PubMedGoogle Scholar
  18. Chen, S.-Y., Matsuoka, Y., and Compans, R. W., 1991b, Golgi complex localization of the Punta Toro virus G2 protein requires its association with G1 protein, Virology 183:351.PubMedGoogle Scholar
  19. Clerx, J. P. M., and Bishop, D. H. L., 1981, Qalyub virus, a member of the newly proposed Nairovirus genus (Bunyaviridae), Virology 108:361.PubMedGoogle Scholar
  20. Collett, M. S., Purchio, A. F., Keegan, K., Frazier, S., Hays, W., Anderson, D. K., Parker, M. D., Schmaljohn, C., Schmidt, J., and Dalrymple, J., 1985, Complete nucleotide sequence of the M RNA segment of Rift Valley fever virus, Virology 144:228.PubMedGoogle Scholar
  21. Dahllöf, B., Wallin, M., and Kvist, S., 1991, The endoplasmic reticulum retention signal of the E3/19K protein of adenovirus-2 is microtubule binding, J. Biol. Chem. 266:1804.PubMedGoogle Scholar
  22. Doms, R. W., Lamb, R. A., Rose, J. K., and Helenius, A., 1993, Folding and assembly of viral membrane proteins, Virology 193:545.PubMedGoogle Scholar
  23. Elliott, R. M., 1990, Molecular biology of the Bunyaviridae, J. Gen. Virol. 71:501.PubMedGoogle Scholar
  24. Elliott, R. M., Schmaljohn, C. S., and Collett, M. S., 1991, Bunyaviridae genome structure and gene expression, Curr. Top. Microbiol. Immunol. 169:91.PubMedGoogle Scholar
  25. Fazakerley, J. K., Gonzalez-Scarano, F., Strickler, J., Dietzschold, B., Karush, F., and Nathanson, N., 1988, Organization of the middle RNA segment of snowshoe hare bunyavirus, Virology 167:422.PubMedGoogle Scholar
  26. Foulke, R. S., Rosato, P. R., and Feench, G. R., 1981, Structural polypeptides of Hazara virus, J. Gen. Virol. 53:169.PubMedGoogle Scholar
  27. Francki, R. I. B., Fauquet, C. M., Knudson, D. L., and Brown, F., 1991, Classification and nomenclature of viruses. Bunyaviridae, Arch. Virol. Suppl. 2:273.Google Scholar
  28. Gahmberg, N., 1984, Characterization of two recombination-complementation groups of Uukuniemi virus temperature-sensitive mutants, J. Gen. Virol. 65:1079.PubMedGoogle Scholar
  29. Gahmberg, N., Pettersson, R. F., and Kääriäinen, L., 1986a, Efficient transport of Semliki Forest virus glycoproteins through a Golgi complex morphologically altered by Uukuniemi virus glycoproteins, EMBO J. 5:3111.PubMedGoogle Scholar
  30. Gahmberg, N., Kuismanen, E., Keränen, S., and Pettersson, R. F., 1986b, Uukuniemi virus glycoproteins accumulate in and cause morphological changes of the Golgi complex in the absence of virus maturation, J. Virol. 57:899.PubMedGoogle Scholar
  31. Garoff, H., and Simons, K., 1974, Location of the spike glycoproteins in the Semliki Forest virus membrane, Proc. Natl. Acad. Sci. USA 71:3988.PubMedGoogle Scholar
  32. Garoff, H., Frischauf, A.-M., Simons, K., Lehrach, H., and Delius, H., 1980, Nucleotide sequence of cDNA coding for Semliki Forest virus membrane glycoproteins, Nature 288:236.PubMedGoogle Scholar
  33. Gerbaud, S., Pardigon, N., Vialat, P., and Bouloy, M., 1992, Organization of Germiston bunyavirus M open reading frame and physicochemical properties of the envelope glycoproteins, J. Gen. Virol. 73:2245.PubMedGoogle Scholar
  34. Griffiths, G., and Rottier, P., 1992, Cell biology of viruses that assemble along the biosynthetic pathway, Semin. Cell Biol. 3:367.PubMedGoogle Scholar
  35. Hauri, H. P., and Schweizer, A., 1992, The endoplasmic reticulum-Golgi intermediate compartment, Curr. Opin. Cell Biol. 4:600.PubMedGoogle Scholar
  36. Hobman, T. C., 1993, Transport of viral glycoproteins into the Golgi complex, Trends Microbiol. 1:124.PubMedGoogle Scholar
  37. Hurtley, S. M., and Helenius, A., 1989, Protein oligomerization in the endoplasmic reticulum, Annu. Rev. Cell Biol. 5:277.PubMedGoogle Scholar
  38. Ihara, T., Smith, J., Dalrymple, J. M., and Bishop, D. H. L., 1985, Complete sequences of the glycoproteins and M RNA of Punta Toro phlebovirus compared to those of Rift Valley fever virus, Virology 144:246.PubMedGoogle Scholar
  39. Jackson, M. R., Nilsson, T., and Peterson, P. A., 1990, Identification of a consensus motif for retention of transmembrane proteins in the endoplasmic reticulum, EMBO J. 9:3153.PubMedGoogle Scholar
  40. Kakach, L. T., Wasmoen, T. L., and Collett, M. S., 1988, Rift Valley fever virus M segment: Use of recombinant vaccinia viruses to study Phlebovirus gene expression, J. Virol. 62:826.PubMedGoogle Scholar
  41. Kakach, L. T., Suzich, J. A., and Collett, M. S., 1989, Rift Valley fever virus M segment: Phlebovirus expression strategy and protein glycosylation, Virology 170:505.PubMedGoogle Scholar
  42. Kamrud, K. I., and Schmaljohn, C. S., 1994, Expression strategy of the M genome segment of Hantaan virus, Virus Res. 31:109.PubMedGoogle Scholar
  43. Kitajima, E. W., de Àvila, A. C., de O. Resende, R., Goldbach, R. W., and Peters, D., 1992, Comparative cytological and immunogold labelling studies on different isolates of tomato spotted wilt virus, J. Submicrosc. Cytol. Pathol. 24:1.Google Scholar
  44. Kormelink, R., de Haan, P., Meurs, C., Peters, D., and Goldbach, R., 1992, The nucleotide sequence of the M RNA segment of tomato spotted wilt virus, a bunyavirus with two ambisense RNA segments, J. Gen. Virol. 73:2795.PubMedGoogle Scholar
  45. Kormelink, R., Storms, M., van Lent, J., Peters, D., and Goldbach, R., 1994, Expression and subcellular location of the NSM protein of tomato spotted wilt virus (TSWV), a putative viral movement protein, Virology 200:56.PubMedGoogle Scholar
  46. Krijnse-Locker, J., Ericsson, M., Rottier, P. J. M., and Griffiths, G., 1994, Characterization of the budding compartment of mouse hepatitis virus: Evidence that transport from the RER to the Golgi complex requires only one vesicular transport step, J. Cell Biol. 124:55.PubMedGoogle Scholar
  47. Kuismanen, E., 1984, Posttranslational processing of Uukuniemi virus glycoproteins G1 and G2, J. Virol. 51:806.PubMedGoogle Scholar
  48. Kuismanen, E., Hedman, K., Saraste, J., and Pettersson, R. F., 1982, Uukuniemi virus maturation: Accumulation of virus particles and viral antigens in the Golgi complex, Mol. Cell. Biol. 2:1444.PubMedGoogle Scholar
  49. Kuismanen, E., Bång, B., Hurme, M., and Pettersson, R. F., 1984, Uukuniemi virus maturation: Immunofluorescence microscopy with monoclonal glycoprotein-specific antibodies, J. Virol. 51:137.PubMedGoogle Scholar
  50. Kuismanen, E., Saraste, J., and Pettersson, R. F., 1985, Effect of monensin on the assembly of Uukuniemi virus in the Golgi complex, J. Virol. 55:813.PubMedGoogle Scholar
  51. Lappin, D. F., Nakitare, G. W., Palfreyman, J. W., and Elliott, R. M., 1994, Localization of Bunyamwera bunyavirus G1 glycoprotein to the Golgi requires association with G2 but not with NSm, J. Gen. Virol. 75:1.Google Scholar
  52. Law, M. D., Speck, J., and Moyer, J. W., 1992, The M RNA of impatiens necrotic spot Tospovirus (Bunyaviridae) has an ambisense genomic organization, Virology 188:732.PubMedGoogle Scholar
  53. Liljeström, P., and Garoff, H., 1991, Internally located cleavable signal sequences direct the formation of Semliki Forest virus membrane proteins from a polyprotein precursor, J. Virol. 65:147.PubMedGoogle Scholar
  54. Liljeström, P., Lusa, S., Huylebroeck, D., and Garoff, H., 1991, In vitro mutagenesis of a full-length cDNA clone of Semliki Forest virus: The 6,000-molecular-weight membrane protein modulates virus release, J. Virol. 65:4107.PubMedGoogle Scholar
  55. Maass, D. R., and Atkinson, P. H., 1994, Retention by the endoplasmic reticulum of Rotavirus VP7 is controlled by three adjacent amino-terminal residues, J. Virol. 68:366.PubMedGoogle Scholar
  56. Machamer, C. E., Mentone, S. A., Rose, J. K., and Farquhar, M. G., 1990, the El glycoprotein of an avian coronavirus is targeted to the cis Golgi complex, Proc. Natl. Acad. Sci. USA 87:6944.PubMedGoogle Scholar
  57. Madoff, D. H., and Lenard, J., 1982, A membrane glycoprotein that accumulates intracellularly: Cellular processing of the large glycoprotein of La Crosse virus, Cell 28:821.PubMedGoogle Scholar
  58. Marriott, A. C., El-Ghorr, A. A., and Nuttall, P. A., 1992, Dugbe Nairovirus M RNA: Nucleotide sequence and coding strategy, Virology 190:606.PubMedGoogle Scholar
  59. Matsuoka, Y., Ihara, T., Bishop, D. H. L., and Compans, R. W., 1988, Intracellular accumulation of the Punta Toro virus glycoproteins expressed from cloned cDNA, Virology 167:251.PubMedGoogle Scholar
  60. Matsuoka, Y., Chen, S.-Y., and Compans, R. W., 1991, Bunyavirus protein transport and assembly, Curr. Top. Microbiol. Immunol. 169:161.PubMedGoogle Scholar
  61. Matsuoka, Y., Chen, S.-Y., and Compans, R. W., 1994, A signal for Golgi retention in the bunyavirus G1 glycoprotein, J. Biol. Chem. 269:22565.PubMedGoogle Scholar
  62. Melin, L., Persson, R., Rönnholm, R., Bergström, A., and Pettersson, R. F., 1995, The membrane glycoprotein G1 of Uukuniemi virus contains a signal for localization to the Golgi complex, Virus Res. 36:49–66.PubMedGoogle Scholar
  63. Munro, S., 1991, Sequences within and adjacent to the transmembrane segment of α-2,6-sialyltransferase specify Golgi retention, EMBO J. 10:3577.PubMedGoogle Scholar
  64. Murphy, R. A., Whitfield, S. G., Coleman, P. H., Calisher, C. H., Rabin, E. R., Jenson, A. B., Melnick, J. L., Edwards, M. R., and Whitney, E., 1968, California group arboviruses: Electron microscopic studies, Exp. Mol. Pathol. 9:44.PubMedGoogle Scholar
  65. Murphy, R. A., Harrison, A. K., and Whitfield, S. G., 1973, Bunyaviridae: Morphologic and morphogenetic similarities of Bunyamwera serologie supergroup viruses and several other arthropod borne viruses, Intervirology 1:297.PubMedGoogle Scholar
  66. Nakitare, G. W., and Elliott, R. M., 1993, Expression of the Bunyamwera virus M genome segment and intracellular localization of NSm, Virology 195:511.PubMedGoogle Scholar
  67. Nilsson, T., Lucocq, J. M., Mackay, D., and Warren, G., 1991, The membrane spanning domain of β-l,4-galactosyltransferase specifies trans Golgi localization, EMBO J. 10:3567.PubMedGoogle Scholar
  68. Nilsson, T., Hoe, M. H., Slusarewicz, P., Rabouille, C., Watson, R., Hunte, F., Watzele, G., Berger, E. G., and Warren, G., 1994, Kin recognition between medial Golgi enzymes in HeLa cells, EMBO J. 13:562.PubMedGoogle Scholar
  69. Ou, W.-J., Cameron, P. H., Thomas, D. Y., and Bergeron, J. M., 1993, Association of folding intermediates of glycoproteins with calnexin during protein maturation, Nature 364:771.PubMedGoogle Scholar
  70. Parrington, M. A., Lee, P.-W., and Kang, C. Y., 1991, Molecular characterization of the Prospect Hill virus M RNA segment: A comparison with the M RNA segments of other hantaviruses, J. Gen. Virol. 72:1845.PubMedGoogle Scholar
  71. Pelham, H. R. B., 1990, The retention signal for soluble proteins of the endoplasmic reticulum, Trends Biochem. Sci. 15:483.PubMedGoogle Scholar
  72. Pennington, T. H., Pringle, C. R., and McCrae, M. A., 1977, Bunyamwera virus-induced polypeptide synthesis, J. Virol. 24:397.PubMedGoogle Scholar
  73. Pensiero, M. N., and Hay, J., 1992, The Hantaan virus M-segment glycoproteins G1 and G2 can be expressed independently, J. Virol. 66:1907.PubMedGoogle Scholar
  74. Pensiero, M. N., Jennings, G. B., Schmaljohn, C. S., and Hay, J., 1988, Expression of the Hantaan virus M genome segment by using a vaccinia virus recombinant, J. Virol. 62:696.PubMedGoogle Scholar
  75. Persson, R., and Pettersson, R. F., 1991, Formation and intracellular transport of a heterodimeric viral spike protein complex, J. Cell Biol. 112:257.PubMedGoogle Scholar
  76. Pesonen, M., Kuismanen, E., and Pettersson, R. F., 1982a, Monosaccharide sequence of protein-bound glycans of Uukuniemi virus, J. Virol. 41:390.PubMedGoogle Scholar
  77. Pesonen, M., Rönnholm, R., Kuismanen, E., and Pettersson, R. F., 1982b, Characterization of the oligosaccharides of Inkoo virus envelope glycoproteins, J. Gen. Virol. 63:425.PubMedGoogle Scholar
  78. Pettersson, R. F., 1991, Protein localization and virus assembly at intracellular membranes, Curr. Top. Microbiol. Immunol. 170:67.PubMedGoogle Scholar
  79. Pettersson, R. F., and von Bonsdorff, C.-H., 1987, Bunyaviridae, Animal Virus Structure (M. V. Nermut and A. Steven, eds.), pp. 147-157, Elsevier, Amsterdam.Google Scholar
  80. Pettersson, R. F., Gahmberg, N., Kuismanen, E., Kääriäinen, L., Rönnholm, R., and Saraste, J., 1988, Bunyavirus membrane glycoproteins as models for Golgi-specific proteins, Modern Cell Biol. 6:65.Google Scholar
  81. Pettersson, R. F., Simons, J. F., Melin, L., Persson, R., and Rönnholm, R., 1993, Uukuniemi virus as a model for elucidating the molecular biology of bunyaviruses, in: Concepts in Virology from Ivanovsky to the Present (B. W. J. Mahy and D. K. Lvov, eds.), pp. 309-319, Harwood Academic.Google Scholar
  82. Pettersson, R. F., Andersson, A., and Melin, L., 1996, Mapping a retention signal for Golgilocalization of a viral spike protein complex, in: Protein Kinesis: The Dynamics of Protein Trafficking and Stability, Cold Spring Harbor Symp. Quant. Biol, Vol. 60, in press.Google Scholar
  83. Pfeffer, S. R., and Rothman, J. R., 1987, Biosynthetic protein transport and sorting by the endoplasmic reticulum and Golgi, Annu. Rev. Biochem. 56:829.PubMedGoogle Scholar
  84. Pryer, N. K., Wuestehube, L. J., and Schekman, R., 1992, Vesicle-mediated protein sorting, Annu. Rev. Biochem. 61:471.PubMedGoogle Scholar
  85. Rhee, S. S., and Hunter, E., 1991, Amino acid substitutions within the matrix protein of type D retroviruses affect assembly, transport and membrane association of a capsid, EMBO J. 10:535.PubMedGoogle Scholar
  86. Rönnholm, R., 1992, Localization to the Golgi complex of Uukuniemi virus glycoproteins G1 and G2 expressed from cloned cDNAs, J. Virol. 66:4525.PubMedGoogle Scholar
  87. Rönnholm, R., and Pettersson, R. F., 1987, Complete nucleotide sequence of the M RNA segment of Uukuniemi virus encoding the membrane glycoproteins G1 and G2, Virology 160:191.PubMedGoogle Scholar
  88. Ruusala, A., Persson, R., Schmaljohn, C. S., and Pettersson, R. F., 1992, Coexpression of the membrane glycoproteins G1 and G2 of Hantaan virus is required for targeting to the Golgi complex, Virology 186:53.PubMedGoogle Scholar
  89. Saraste, J., and Kuismanen, E., 1992, Pathways of protein sorting and membrane traffic between the rough endoplasmic reticulum and the Golgi complex, Semin. Cell Biol. 3:343.PubMedGoogle Scholar
  90. Schmaljohn, C. S., Hasty, S. E., Rasmussen, L., and Dalrymple, J. M., 1986, Hantaan virus replication: Effects of monensin, tunicamycin and endoglycosidase on the structural glycoproteins, J. Gen. Virol. 67:707.PubMedGoogle Scholar
  91. Schmaljohn, C. S., Schmaljohn, A. L., and Dalrymple, J. M., 1987, Hantaan virus M RNA: Coding strategy, nucleotide sequence, and gene order, Virology 157:31.PubMedGoogle Scholar
  92. Schmaljohn, C. S., Chu, Y.-K., Schmaljohn, A. L., and Dalrymple, J. M., 1990, Antigenic subunits of Hantaan virus expressed by baculovirus and vaccinia virus recombinants, J. Virol. 64: 3162.PubMedGoogle Scholar
  93. Slusarewicz, P., Nilsson, T., Hui, N., Watson, R., and Warren, G., 1994, Isolation of a matrix that binds medial Golgi enzymes, J. Cell Biol. 124:405.PubMedGoogle Scholar
  94. Smith, J. F., and Pifat, D., 1982, Morphogenesis of sandfly viruses (Bunyaviridae family), Virology 121:61.PubMedGoogle Scholar
  95. Sodeik, B., Doms, R. W., Ericsson, M., Hiller, G., Machamer, C. E., van Hof, W., van Meer, G., Moss, B., and Griffiths, G., 1993, Assembly of vaccinia virus: Role of the intermediate compartment between the endoplasmic reticulum and the Golgi stacks, J. Cell Biol. 121:521.PubMedGoogle Scholar
  96. Spiropoulou, C. F., Morzunov, S., Feldmann, H., Sanchez, A., Peters, C. J., and Nichol, S. T., 1994, Genome structure and variability of a virus causing hantavirus pulmonary syndrome, Virology 200:715.PubMedGoogle Scholar
  97. Stanley, K. K., and Howell, K. E., 1993, TGN38/41: A molecule on the move, Trends Cell Biol. 3:252.PubMedGoogle Scholar
  98. Stephens, E. B., and Compans, R. W., 1988, Assembly of animal viruses at cellular membranes, Annu. Rev. Microbiol. 42:489.PubMedGoogle Scholar
  99. Suomalainen, M., Liljeström, P., and Garoff, H., 1992, Spike protein-nucleocapsid interactions drive the budding of alphaviruses, J. Virol. 66:4737.PubMedGoogle Scholar
  100. Suzich, J. A., and Collett, M. S., 1988, Rift Valley fever virus M segment: Cell-free transcription and translation of virus complementary RNA, Virology 164:478.PubMedGoogle Scholar
  101. Suzich, J. A., Kakach, L. T., and Collett, M. S., 1990, Expression strategy of a phlebovirus: Biogenesis of proteins from the Rift Valley fever M segment, J. Virol. 64:1549.PubMedGoogle Scholar
  102. Takehara, K., Min, M.-K., Battles, J. K., Sugiyama, K., Emery, V. C., Dalrymple, J. M., and Bishop, D. H. L., 1989, Identification of mutations in the M RNA of a candidate vaccine strain of Rift Valley fever virus, Virology 169:452.PubMedGoogle Scholar
  103. Ulmanen, I., Seppälä, P., and Pettersson, R. F., 1981, In vitro translation of Uukuniemi virusspecific RNAs: Identification of a nonstructural protein and a precursor to the membrane glycoproteins, J. Virol. 37:72.PubMedGoogle Scholar
  104. von Bonsdorff, C.-H., and Pettersson, R., 1975, Surface structure of Uukuniemi virus, J. Virol. 16:1296.Google Scholar
  105. von Bonsdorff, C.-H., Saikku, P., and Oker-Blom, N., 1970, Electron microscope study on the development of Uukuniemi virus, Acta Virol. 14:109.Google Scholar
  106. von Heijne, G., 1990, Protein targeting signals, Curr. Opin. Cell Biol. 2:604.Google Scholar
  107. Vorndam, A. V., and Trent, D. W., 1979, Oligosaccharides of the California encephalitis viruses, Virology 95:1.PubMedGoogle Scholar
  108. Wahlberg, J. M., and Garoff, H., 1992, Membrane fusion process of Semliki Forest virus I: Low pH-induced rearrangement in spike protein quaternary structure precedes virus penetration into cells, J. Cell Biol. 116:339.PubMedGoogle Scholar
  109. Wasmoen, T. L., Kakach, L. T., and Collett, M. C., 1988, Rift Valley fever M segment: Cellular localization of M segment-encoded proteins, Virology 166:275.PubMedGoogle Scholar
  110. Watret, G. E., and Elliott, R. M., 1985, The proteins and RNAs specified by Clo Mor virus, a Scottish nairovirus, J. Gen. Virol. 66:2513.PubMedGoogle Scholar
  111. Weisz, O. A., Swift, A. M., and Machamer, C. E., 1993, Oligomerization of a membrane protein correlates with its retention in the Golgi complex, J. Cell Biol. 122:1185.PubMedGoogle Scholar
  112. Whitt, M. A., Chong, L., and Rose, J. K., 1989, Glycoprotein cytoplasmic domain sequences required for rescue of a vesicular stomatitis virus glycoprotein mutant, J. Virol. 63:3569.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1996

Authors and Affiliations

  • Ralf F. Pettersson
    • 1
  • Lars Melin
    • 1
  1. 1.Ludwig Institute for Cancer ResearchStockholm BranchStockholmSweden

Personalised recommendations