Retrovirus entry by endocytosis and cathepsin proteases

Advances in Virology

Volumn 2012, Issue , 2012, Pages

  Kubo, Yoshinao ^a   Hayashi, Hideki ^a   Matsuyama, Toshifumi ^a   Sato, Hironori ^a,b   Yamamoto, Naoki ^a,c  

^a NAGASAKI UNIVERSITY   (Japan)

^b NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALIA; HUMAN IMMUNODEFICIENCY VIRUS; MURINE LEUKEMIA VIRUS;

EID: 84873802570     PISSN: 16878639     EISSN: 16878647     Source Type: Journal    
DOI: 10.1155/2012/640894     Document Type: Review

References (136)

1. Harris R. S., Hultquist J. F., Evans D. T., The restriction factors of human immunodeficiency virus. Journal of Biological Chemistry 2012 287 48 40875 40883
2. Checkley M. A., Luttge B. G., Freed E. O., HIV-1 envelope glycoprotein biosynthesis, trafficking, and incorporation. Journal of Molecular Biology 2011 410 4 582 608 10.1016/j.jmb.2011.04.042
3. Wilen C. B., Tilton J. C., Doms R. W., Molecular mechanisms of HIV entry. Advances in Experimental Medicine and Biology 2012 726 223 242 10.1007/978-1-4614-0980-9-10
4. Cai L., Gochin M., Liu K., Biochemistry and biophysics of HIV-1 gp41-membrane interactions and implications for HIV-1 envelope protein mediated viral-cell fusion and fusion inhibitor design. Current Topics in Medicinal Chemistry 2011 11 24 2959 2984 10.2174/156802611798808497
5. Melikyan G. B., Membrane fusion mediated by human immunodeficiency virus envelope glycoprotein. Current Topics in Membranes 2011 68 82 106 2-s2.0-79960435702 10.1016/B978-0-12-385891-7.00004-0
6. Sodroski J. G., HIV-1 entry inhibitors in the side pocket. Cell 1999 99 3 243 246 2-s2.0-0033615735 10.1016/S0092-8674(00)81655-4 (Pubitemid 29519903)
7. Melikyan G. B., Common principles and intermediates of viral protein-mediated fusion: the HIV-1 paradigm. Retrovirology 2008 5, article 111 2-s2.0-59849107898 10.1186/1742-4690-5-111
8. Plemper R. K., Cell entry of enveloped viruses. Current Opinion in Virology 2011 1 2 92 100 10.1016/j.coviro.2011.06.002
9. Hunt C. L., Lennemann N. J., Maury W., Filovirus entry: a novelty in the viral fusion world. Viruses 2012 4 2 258 275 10.3390/v4020258
10. Tailor C. S., Lavillette D., Marin M., Kabat D., Cell surface receptors for gammaretroviruses. Current Topics in Microbiology and Immunology 2003 281 29 106 2-s2.0-0042164510 (Pubitemid 36950683)
11. Barnard R. J. O., Young J. A. T., Alpharetrovirus envelope-receptor interactions. Current Topics in Microbiology and Immunology 2003 281 107 136 2-s2.0-0041663560 (Pubitemid 36950684)
12. Albritton L. M., Tseng L., Scadden D., Cunningham J. M., A putative murine ecotropic retrovirus receptor gene encodes a multiple membrane-spanning protein and confers susceptibility to virus infection. Cell 1989 57 4 659 666 2-s2.0-0024370460 (Pubitemid 19140646)
13. Miller D. G., Edwards R. H., Miller A. D., Cloning of the cellular receptor for amphotropic murine retroviruses reveals homology to that for gibbon ape leukemia virus. Proceedings of the National Academy of Sciences of the United States of America 1994 91 1 78 82 2-s2.0-0027976910 10.1073/pnas.91.1.78 (Pubitemid 24018646)
14. Van Zeijl M., Johann S. V., Closs E., Cunningham J., Eddy R., Shows T. B., O'Hara B., A human amphotropic retrovirus receptor is a second member of the gibbon ape leukemia virus receptor family. Proceedings of the National Academy of Sciences of the United States of America 1994 91 3 1168 1172 2-s2.0-0028158411 (Pubitemid 24048530)
15. Battini J. L., Rasko J. E. J., Miller A. D., A human cell-surface receptor for xenotropic and polytropic murine leukemia viruses: possible role in G protein-coupled signal transduction. Proceedings of the National Academy of Sciences of the United States of America 1999 96 4 1385 1390 2-s2.0-0033573904 10.1073/pnas.96.4.1385 (Pubitemid 29098460)
16. Tailor C. S., Nouri A., Lee C. G., Kozak C., Kabat D., Cloning and characterization of a cell surface receptor for xenotropic and polytropic marine leukemia viruses. Proceedings of the National Academy of Sciences of the United States of America 1999 96 3 927 932 2-s2.0-0033514357
17. Yang Y. L., Guo L., Xu S., Holland C. A., Kitamura T., Hunter K., Cunningham J. M., Receptors for polytropic and xenotropic mouse leukaemia viruses encoded by a single gene at Rmc1. Nature Genetics 1999 21 2 216 219 2-s2.0-0032964564 10.1038/6005 (Pubitemid 29070371)
18. Berger E. A., Murphy P. M., Farber J. M., Chemokine receptors as HIV-1 coreceptors: roles in viral entry, tropism, and disease. Annual Review of Immunology 1999 17 657 700 2-s2.0-0033012398 10.1146/annurev.immunol.17.1.657 (Pubitemid 29241137)
19. Xiao P., Usami O., Suzuki Y., Ling H., Shimizu N., Hoshino H., Zhuang M., Ashino Y., Gu H., Hattori T., Characterization of a CD4-independent clinical HIV-1 that can efficiently infect human hepatocytes through chemokine (C-X-C motif) receptor 4. AIDS 2008 22 14 1749 1757 2-s2.0-66349116273 10.1097/QAD.0b013e328308937c
20. + lymphocytes. Journal of Virology 2004 78 3 1243 1255 10.1128/JVI.78.3.1243-1255.2004 (Pubitemid 38095834)
21. Yoshii H., Kamiyama H., Goto K., Oishi K., Katunuma N., Tanaka Y., Hayashi H., Matsuyama T., Sato H., Yamamoto N., Kubo Y., CD4-independent human immunodeficiency virus infection involves participation of endocytosis and cathepsin B. PLoS ONE 2011 6 4 2-s2.0-79955563682 10.1371/journal.pone.0019352 e19352
22. Edinger A. L., Blanpain C., Kunstman K. J., Wolinsky S. M., Parmentier M., Doms R. W., Functional dissection of CCR5 coreceptor function through the use of CD4-independent simian immunodeficiency virus strains. Journal of Virology 1999 73 5 4062 4073 2-s2.0-0032899496 (Pubitemid 29189851)
23. Puffer B. A., Pöhlmann S., Edinger A. L., Carlin D., Sanchez M. D., Reitter J., Watry D. D., Fox H. S., Desrosiers R. C., Doms R. W., CD4 independence of simian immunodeficiency virus Envs is associated with macrophage tropism, neutralization sensitivity, and attenuated pathogenicity. Journal of Virology 2002 76 6 2595 2605 2-s2.0-0036187795 10.1128/JVI.76.6.2595-2605.2002 (Pubitemid 34184844)
24. Kubo Y., Yokoyama M., Yoshii H., Mitani C., Tominaga C., Tanaka Y., Sato H., Yamamoto N., Inhibitory role of CXCR4 glycan in CD4-independent X4-tropic human immunodeficiency virus type 1 infection and its abrogation in CD4-dependent infection. Journal of General Virology 2007 88 11 3139 3144 2-s2.0-36249032566 10.1099/vir.0.83202-0 (Pubitemid 350131256)
25. Sato H., Orenstein J., Dimitrov D., Martin M., Cell-to-cell spread of HIV-1 occurs within minutes and may not involve the participation of virus particles. Virology 1992 186 2 712 724 2-s2.0-0026587543 10.1016/0042-6822(92) 90038-Q
26. Dimitrov D. S., Willey R. L., Sato H., Chang L. J., Blumenthal R., Martin M. A., Quantitation of human immunodeficiency virus type 1 infection kinetics. Journal of Virology 1993 67 4 2182 2190 2-s2.0-0027468750 (Pubitemid 23088394)
27. Sigal A., Kim J. T., Balazs A. B., Dekel E., Mayo A., Milo R., Baltimore D., Cell-to-cell spread of HIV permits ongoing replication despite antiretroviral therapy. Nature 2011 477 7362 95 99 10.1038/nature10347
28. Ferri K. F., Jacotot E., Blanco J., Esté J. A., Zamzami N., Susin S. A., Xie Z., Brothers G., Reed J. C., Penninger J. M., Kroemer G., Apoptosis control in syncytia induced by the HIV type 1-envelope glycoprotein complex: role of mitochondria and caspases. Journal of Experimental Medicine 2000 192 8 1081 1092 2-s2.0-0034676090 10.1084/jem.192.8.1081
29. Scheller C., Jassoy C., Syncytium formation amplifies apoptotic signals: a new view on apoptosis in HIV infection in vitro. Virology 2001 282 1 48 55 2-s2.0-0035970310 10.1006/viro.2000.0811 (Pubitemid 32881774)
30. Maldarelli F., Sato H., Berthold E., Orenstein J., Martin M. A., Rapid induction of apoptosis by cell-to-cell transmission of human immunodeficiency virus type 1. Journal of Virology 1995 69 10 6457 6465 2-s2.0-0029100490
31. Green N., Shinnick T. M., Witte O., Sequence-specific antibodies show that maturation of Moloney leukemia virus envelope polyprotein involves removal of a COOH-terminal peptide. Proceedings of the National Academy of Sciences of the United States of America 1981 78 10 I 6023 6027 2-s2.0-0019844429 (Pubitemid 12247457)
32. Henderson L. E., Sowder R., Copeland T. D., Quantitative separation of murine leukemia virus proteins by reversed-phase high-pressure liquid chromatography reveals newly described gag and env cleavage products. Journal of Virology 1984 52 2 492 500 2-s2.0-0021690345 (Pubitemid 15202485)
33. Ragheb J. A., Anderson W. F., pH-independent murine leukemia virus ecotropic envelope-mediated cell fusion: implications for the role of the R peptide and p12E TM in viral entry. Journal of Virology 1994 68 5 3220 3231 2-s2.0-0028271720 (Pubitemid 24129772)
34. Rein A., Mirro J., Haynes J. G., Ernst S. M., Nagashima K., Function of the cytoplasmic domain of a retroviral transmembrane protein: p15E-p2E cleavage activates the membrane fusion capability of the murine leukemia virus Env protein. Journal of Virology 1994 68 3 1773 1781 2-s2.0-0028047579 (Pubitemid 24065746)
35. Kubo Y., Amanuma H., Mutational analysis of the R peptide cleavage site of Moloney murine leukaemia virus envelope protein. Journal of General Virology 2003 84 8 2253 2257 2-s2.0-0042167361 10.1099/vir.0.19126-0 (Pubitemid 36927257)
36. Kubo Y., Tominaga C., Yoshii H., Kamiyama H., Mitani C., Amanuma H., Yamamoto N., Characterization of R peptide of murine leukemia virus envelope glycoproteins in syncytium formation and entry. Archives of Virology 2007 152 12 2169 2182 2-s2.0-36749036754 10.1007/s00705-007-1054-6 (Pubitemid 350215783)
37. Kiernan R. E., Freed E. O., Cleavage of the murine leukemia virus transmembrane Env protein by human immunodeficiency virus type 1 protease: transdominant inhibition by matrix mutations. Journal of Virology 1998 72 12 9621 9627 2-s2.0-0031743807 (Pubitemid 28520825)
38. Aguilar H. C., Anderson W. F., Cannon P. M., Cytoplasmic tail of moloney murine leukemia virus envelope protein influences the conformation of the extracellular domain: implications for mechanism of action of the R peptide. Journal of Virology 2003 77 2 1281 1291 2-s2.0-0037225634 10.1128/JVI.77.2.1281- 1291.2003 (Pubitemid 36055551)
39. Löving R., Li K., Wallin M., Sjöberg M., Garoff H., R-peptide cleavage potentiates fusion-controlling isomerization of the intersubunit disulfide in moloney murine leukemia virus Env. Journal of Virology 2008 82 5 2594 2597 2-s2.0-39749162175 10.1128/JVI.02039-07 (Pubitemid 351293563)
40. Löving R., Wu S.-R., Sjöberg M., Lindqvist B., Garoff H., Maturation cleavage of the murine leukemia virus Env precursor separates the transmembrane subunits to prime it for receptor triggering. Proceedings of the National Academy of Sciences of the United States of America 2012 109 20 7735 7740 10.1073/pnas.1118125109
41. Murakami T., Ablan S., Freed E. O., Tanaka Y., Regulation of Human Immunodeficiency Virus Type 1 Env-Mediated Membrane Fusion by Viral Protease Activity. Journal of Virology 2004 78 2 1026 1031 2-s2.0-0347319099 10.1128/JVI.78.2.1026-1031.2004 (Pubitemid 38067625)
42. Bobkova M., Stitz J., Engelstädter M., Cichutek K., Buchholtz C. J., Identification of R-peptides in envelope proteins of C-type retroviruses. Journal of General Virology 2002 83 9 2241 2246 2-s2.0-0036711683 (Pubitemid 34993731)
43. Brody B. A., Rhee S. S., Hunter E., Postassembly cleavage of a retroviral glycoprotein cytoplasmic domain removes a necessary incorporation signal and activates fusion activity. Journal of Virology 1994 68 7 4620 4627 2-s2.0-0028241598 (Pubitemid 24183059)
44. Kim F. J., Manel N., Boublik Y., Battini J. L., Sitbon M., Human T-cell leukemia virus type 1 envelope-mediated syncytium formation can be activated in resistant mammalian cell lines by a carboxy-terminal truncation of the envelope cytoplasmic domain. Journal of Virology 2003 77 2 963 969 2-s2.0-0037225838 10.1128/JVI.77.2.963-969.2003 (Pubitemid 36055518)
45. Lerner D. L., Elder J. H., Expanded host cell tropism and cytopathic properties of feline immunodeficiency virus strain PPR subsequent to passage through interleukin- 2-independent T cells. Journal of Virology 2000 74 4 1854 1863 2-s2.0-0033934726 10.1128/JVI.74.4.1854-1863.2000 (Pubitemid 30434044)
46. Bowman E. J., Siebers A., Altendorf K., Bafilomycins; A class of inhibitors of membrane ATPases from microorganisms, animal cells, and plant cells. Proceedings of the National Academy of Sciences of the United States of America 1988 85 21 7972 7976 2-s2.0-0011913143
47. Yoshimori T., Yamamoto A., Moriyama Y., Futai M., Tashiro Y., Bafilomycin A1, a specific inhibitor of vacuolar-type H+-ATPase, inhibits acidification and protein degradation in lysosomes of cultured cells. Journal of Biological Chemistry 1991 266 26 17707 17712 2-s2.0-0025925091 (Pubitemid 21907995)
48. Forgac M., Vacuolar ATPases: rotary proton pumps in physiology and pathophysiology. Nature Reviews Molecular Cell Biology 2007 8 11 917 929 2-s2.0-35448946098 10.1038/nrm2272 (Pubitemid 47622561)
49. McClure M. O., Sommerfelt M. A., Marsh M., Weiss R. A., The pH independence of mammalian retrovirus infection. Journal of General Virology 1990 71 4 767 773 2-s2.0-0025348115 (Pubitemid 20132879)
50. Gilbert M. A., Charreau B., Vicart P., Paulin D., Nandi P. K., Mechanism of entry of a xenotropic MMuLV-derived recombinant retrovirus into porcine cells using the expression of the reporter nlslacZ gene. Archives of Virology 1992 124 1-2 57 67 2-s2.0-0026488006 10.1007/BF01314625
51. Katen L. J., Januszeski M. M., Anderson W. F., Hasenkrug K. J., Evans L. H., Infectious entry by amphotropic as well as ecotropic murine leukemia viruses occurs through an endocytic pathway. Journal of Virology 2001 75 11 5018 5026 2-s2.0-0035039738 10.1128/JVI.75.11.5018-5026.2001 (Pubitemid 32448522)
52. Kamiyama H., Kakoki K., Yoshii H., Iwao M., Igawa T., Sakai H., Hayashi H., Matsuyama T., Yamamoto N., Kubo Y., Infection of XC cells by MLVs and Ebola virus is endosome-dependent but acidification-independent. PLoS ONE 2011 6 10 e26180 10.1371/journal.pone.0026180
53. Côté M., Zheng Y.-M., Liu S.-L., Membrane fusion and cell entry of XMRV are pH-independent and modulated by the envelope glycoprotein's cytoplasmic tail. PLoS ONE 2012 7 3 e33734 10.1371/journal.pone.0033734
54. Gilbert J. M., Mason D., White J. M., Fusion of Rous sarcoma virus with host cells does not require exposure to low pH. Journal of Virology 1990 64 10 5106 5113 2-s2.0-0025093305 (Pubitemid 20329833)
55. Earp L. J., Delos S. E., Netter R. C., Bates P., White J. M., The avian retrovirus avian sarcoma/leukosis virus subtype A reaches the lipid mixing stage of fusion at neutral pH. Journal of Virology 2003 77 5 3058 3066 2-s2.0-0037370724 10.1128/JVI.77.5.3058-3066.2003 (Pubitemid 36228091)
56. Melikyan G. B., Barnard R. J. O., Markosyan R. M., Young J. A. T., Cohen F. S., Low pH is required for avian sarcoma and leukosis virus Env-induced hemifusion and fusion pore formation but not for pore growth. Journal of Virology 2004 78 7 3753 3762 2-s2.0-1842509971 10.1128/JVI.78.7.3753-3762.2004 (Pubitemid 38568313)
57. Barnard R. J. O., Narayan S., Dornadula G., Miller M. D., Young J. A. T., Low pH is required for avian sarcoma and leukosis virus Env-dependent viral penetration into the cytosol and not for viral uncoating. Journal of Virology 2004 78 19 10433 10441 2-s2.0-4544371670 10.1128/JVI.78.19.10433-10441.2004 (Pubitemid 39258368)
58. Diaz-Griffero F., Hoschander S. A., Brojatsch J., Endocytosis is a critical step in entry of subgroup B avian leukosis viruses. Journal of Virology 2002 76 24 12866 12876 2-s2.0-0036892612 10.1128/JVI.76.24.12866-12876.2002 (Pubitemid 35386970)
59. Hernandez L. D., Peters R. J., Delos S. E., Young J. A. T., Agard D. A., White J. M., Activation of a retroviral membrane fusion protein: soluble receptor- induced liposome binding of the ALSV envelope glycoprotein. Journal of Cell Biology 1997 139 6 1455 1464 2-s2.0-0031440116 10.1083/jcb.139.6.1455 (Pubitemid 28013666)
60. Damico R. L., Crane J., Bates P., Receptor-triggered membrane association of a model retroviral glycoprotein. Proceedings of the National Academy of Sciences of the United States of America 1998 95 5 2580 2585 2-s2.0-0032478191 10.1073/pnas.95.5.2580 (Pubitemid 28145985)
61. Markosyan R. M., Bates P., Cohen F. S., Melikyan G. B., A study of low pH-induced refolding of Env of avian sarcoma and leukosis virus into a six-helix bundle. Biophysical Journal 2004 87 5 3291 3298 2-s2.0-16344374327 10.1529/biophysj.104.047696 (Pubitemid 40468584)
62. Matsuyama S., Delos S. E., White J. M., Sequential roles of receptor binding and low pH in forming prehairpin and hairpin conformations of a retroviral envelope glycoprotein. Journal of Virology 2004 78 15 8201 8209 2-s2.0-3242713988 10.1128/JVI.78.15.8201-8209.2004 (Pubitemid 38944303)
63. Mothes W., Boerger A. L., Narayan S., Cunningham J. M., Young J. A. T., Retroviral entry mediated by receptor priming and low pH triggering of an envelope glycoprotein. Cell 2000 103 4 679 689 2-s2.0-0033697734
64. Delos S. E., Brecher M. B., Chen Z., Melder D. C., Federspiel M. J., White J. M., Cysteines flanking the internal fusion peptide are required for the avian sarcoma/leukosis virus glycoprotein to mediate the lipid mixing stage of fusion with high efficiency. Journal of Virology 2008 82 6 3131 3134 2-s2.0-40149083415 10.1128/JVI.02266-07 (Pubitemid 351329201)
65. Ross S. R., Schofield J. J., Farr C. J., Bucan M., Mouse transferrin receptor 1 is the cell entry receptor for mouse mammary tumor virus. Proceedings of the National Academy of Sciences of the United States of America 2002 99 19 12386 12390 2-s2.0-0037126027 10.1073/pnas.192360099
66. Picard-Maureau M., Jarmy G., Berg A., Rethwilm A., Lindemann D., Foamy virus envelope glycoprotein-mediated entry involves a pH-dependent fusion process. Journal of Virology 2003 77 8 4722 4730 2-s2.0-0037383146 10.1128/JVI.77.8.4722-4730.2003 (Pubitemid 36402822)
67. Brindley M. A., Maury W., Endocytosis and a low-pH step are required for productive entry of equine infectious anemia virus. Journal of Virology 2005 79 23 14482 14488 2-s2.0-27744589244 10.1128/JVI.79.23.14482-14488.2005 (Pubitemid 41636246)
68. Jin S., Zhang B., Weisz O. A., Montelaro R. C., Receptor-mediated entry by equine infectious anemia virus utilizes a pH-dependent endocytic pathway. Journal of Virology 2005 79 23 14489 14497 2-s2.0-27744512883 10.1128/JVI.79.23.14489-14497.2005 (Pubitemid 41636247)
69. Bertrand P., Côté M., Zheng Y. M., Albritton L. M., Liu S. L., Jaagsiekte sheep retrovirus utilizes a pH-dependent endocytosis pathway for entry. Journal of Virology 2008 82 5 2555 2559 2-s2.0-39749094415 10.1128/JVI.01853-07 (Pubitemid 351293555)
70. Côté M., Kucharski T. J., Liu S. L., Enzootic nasal tumor virus envelope requires a very acidic pH for fusion activation and infection. Journal of Virology 2008 82 18 9023 9034 2-s2.0-50949103262 10.1128/JVI.00648-08
71. Vidricaire G., Tremblay M. J., A clathrin, caveolae, and dynamin-independent endocytic pathway requiring free membrane cholesterol drives HIV-1 internalization and infection in polarized trophoblastic cells. Journal of Molecular Biology 2007 368 5 1267 1283 2-s2.0-34247330185 10.1016/j.jmb.2007.03.003 (Pubitemid 46629083)
72. Mercer J., Schelhaas M., Helenius A., Virus entry by endocytosis. Annual Review of Biochemistry 2010 79 803 833 2-s2.0-77952692673 10.1146/annurev- biochem-060208-104626
73. Mercer J., Helenius A., Virus entry by macropinocytosis. Nature Cell Biology 2009 11 5 510 520 2-s2.0-65449120034 10.1038/ncb0509-510
74. Beer C., Andersen D. S., Rojek A., Pedersen L., Caveola-dependent endocytic entry of amphotropic murine leukemia virus. Journal of Virology 2005 79 16 10776 10787 2-s2.0-23244461734 10.1128/JVI.79.16.10776-10787.2005 (Pubitemid 41098616)
75. Lee S., Zhao Y., Anderson W. F., Receptor-mediated Moloney murine leukemia virus entry can occur independently of the clathrin-coated-pit-mediated endocytic pathway. Journal of Virology 1999 73 7 5994 6005 2-s2.0-0033052051 (Pubitemid 29274886)
76. Diaz-Griffero F., Jackson A. P., Brojatsch J., Cellular uptake of avian leukosis virus subgroup B is mediated by clathrin. Virology 2005 337 1 45 54 2-s2.0-19444368439 10.1016/j.virol.2005.02.027 (Pubitemid 40725439)
77. Brindley M. A., Maury W., Equine infectious anemia virus entry occurs through clathrin-mediated endocytosis. Journal of Virology 2008 82 4 1628 1637 2-s2.0-38849103049 10.1128/JVI.01754-07 (Pubitemid 351206914)
78. Yoshii H., Kamiyama H., Minematsu K., Goto K., Mizota T., Oishi K., Katunuma N., Yamamoto N., Kubo Y., Cathepsin L is required for ecotropic murine leukemia virus infection in NIH3T3 cells. Virology 2009 394 2 227 234 2-s2.0-70449102689 10.1016/j.virol.2009.08.045
79. Kumar P., Nachagari D., Fields C., Franks J., Albritton L. M., Host cell cathepsins potentiate moloney murine leukemia virus infection. Journal of Virology 2007 81 19 10506 10514 2-s2.0-34648830868 10.1128/JVI.02853-06 (Pubitemid 47463323)
80. Chandran K., Sullivan N. J., Felbor U., Whelan S. P., Cunningham J. M., Virology: endosomal proteolysis of the ebola virus glycoprotein is necessary for infection. Science 2005 308 5728 1643 1645 2-s2.0-19144365133 10.1126/science.1110656 (Pubitemid 40807517)
81. Mach L., Mort J. S., Glossl J., Maturation of human procathepsin B. Proenzyme activation and proteolytic processing of the precursor to the mature proteinase, in vitro, are primarily unimolecular processes. Journal of Biological Chemistry 1994 269 17 13030 13035 2-s2.0-0028237920
82. Kubo Y., Ishimoto A., Amanuma H., N-linked glycosylation is required for XC cell-specific syncytium formation by the R peptide-containing envelope protein of ecotropic murine leukemia viruses. Journal of Virology 2003 77 13 7510 7516 2-s2.0-0037791023 10.1128/JVI.77.13.7510-7516.2003 (Pubitemid 36734521)
83. Jones J. S., Risser R., Cell fusion induced by the murine leukemia virus envelope glycoprotein. Journal of Virology 1993 67 1 67 74 2-s2.0-0027398485 (Pubitemid 23002965)
84. Kizhatil K., Albritton L. M., Requirements for different components of the host cell cytoskeleton distinguish ecotropic murine leukemia virus entry via endocytosis from entry via surface fusion. Journal of Virology 1997 71 10 7145 7156 2-s2.0-0030865197 (Pubitemid 27391648)
85. Wilson C. A., Marsh J. W., Eiden M. V., The requirements for viral entry differ from those for virally induced syncytium formation in NIH 3T3/DTras cells exposed to moloney murine leukemia virus. Journal of Virology 1992 66 12 7262 7269 2-s2.0-0026472079
86. Sha M., Lee X., Li X. P., Veldman G. M., Finnerty H., Racie L., LaVallie E., Tang X. Y., Edouard P., Howes S., Keith J. C., McCoy J. M., Syncytin is a captive retroviral envelope protein involved in human placental morphogenesis. Nature 2000 403 6771 785 789 2-s2.0-0342545919 10.1038/35001608 (Pubitemid 30111841)
87. Dumonceaux J., Nisole S., Chanel C., Quivet L., Amara A., Baleux F., Briand P., Hazan U., Spontaneous mutations in the env gene of the human immunodeficiency virus type 1 NDK isolate are associated with a CD4-independent entry phenotype. Journal of Virology 1998 72 1 512 519 2-s2.0-0031985314 (Pubitemid 28048866)
88. + T lymphocytes genetically deficient in LFA-1: LFA-1 is required for HIV-mediated cell fusion but not for viral transmission. Journal of Experimental Medicine 1991 173 2 511 514 2-s2.0-0026073086
89. Fredericksen B. L., Wei B. L., Yao J., Luo T., Garcia J. V., Inhibition of endosomal/lysosomal degradation increases the infectivity of human immunodeficiency virus. Journal of Virology 2002 76 22 11440 11446 2-s2.0-0036827862 10.1128/JVI.76.22.11440-11446.2002 (Pubitemid 35231300)
90. Schaeffer E., Soros V. B., Greene W. C., Compensatory link between fusion and endocytosis of human immunodeficiency virus type 1 in human CD4 T lymphocytes. Journal of Virology 2004 78 3 1375 1383 2-s2.0-0347003570 10.1128/JVI.78.3.1375-1383.2004 (Pubitemid 38095847)
91. Wei B. L., Denton P. W., O'Neill E., Luo T., Foster J. L., Garcia J. V., Inhibition of lysosome and proteasome function enhances human immunodeficiency virus type 1 infection. Journal of Virology 2005 79 9 5705 5712 2-s2.0-17444388017 10.1128/JVI.79.9.5705-5712.2005 (Pubitemid 40548239)
92. McClure M. O., Marsh M., Weiss R. A., Human immunodeficiency virus infection of CD4-bearing cells occurs by a pH-independent mechanism. EMBO Journal 1988 7 2 513 518 2-s2.0-0023954154
93. Stein B. S., Gowda S. D., Lifson J. D., Penhallow R. C., Bensch K. G., Engleman E. G., pH-independent HIV entry into CD4-positive T cells via virus envelope fusion to the plasma membrane. Cell 1987 49 5 659 668 2-s2.0-0023644926
94. Permanyer M., Ballana E., Esté J. A., Endocytosis of HIV: anything goes. Trends in Microbiology 2010 18 12 543 551 2-s2.0-78649316355 10.1016/j.tim.2010.09.003
95. Miyauchi K., Kim Y., Latinovic O., Morozov V., Melikyan G. B., HIV enters cells via endocytosis and dynamin-dependent fusion with endosomes. Cell 2009 137 3 433 444 2-s2.0-65249139458 10.1016/j.cell.2009.02.046
96. Bosch B., Grigorov B., Senserrich J., Clotet B., Darlix J. L., Muriaux D., Este J. A., A clathrin-dynamin-dependent endocytic pathway for the uptake of HIV-1 by direct T cell-T cell transmission. Antiviral Research 2008 80 2 185 193 2-s2.0-53449085710 10.1016/j.antiviral.2008.06.004
97. Carter G. C., Bernstone L., Baskaran D., James W., HIV-1 infects macrophages by exploiting an endocytic route dependent on dynamin, Rac1 and Pak1. Virology 2011 409 2 234 250 2-s2.0-78650267415 10.1016/j.virol.2010.10.018
98. Daecke J., Fackler O. T., Dittmar M. T., Kräusslich H. G., Involvement of clathrin-mediated endocytosis in human immunodeficiency virus type 1 entry. Journal of Virology 2005 79 3 1581 1594 2-s2.0-13744252968 10.1128/JVI.79.3.1581-1594.2005 (Pubitemid 40459105)
99. de la Vega M., Marin M., Kondo N., Miyauchi K., Kim Y., Epand R. F., Epand R. M., Melikyan G. B., Inhibition of HIV-1 endocytosis allows lipid mixing at the plasma membrane, but not complete fusion. Retrovirology 2011 8 99 10.1186/1742-4690-8-99
100. Miyauchi K., Marin M., Melikyan G. B., Visualization of retrovirus uptake and delivery into acidic endosomes. Biochemical Journal 2011 434 3 559 569 2-s2.0-79952161998 10.1042/BJ20101588
101. Pauza C. D., Price T. M., Human immunodeficiency virus infection of T cells and manocytes proceeds via receptor-mediated endocytosis. Journal of Cell Biology 1988 107 3 959 968 2-s2.0-0023765764
102. Maréchal V., Prevost M. C., Petit C., Perret E., Heard J. M., Schwartz O., Human immunodeficiency virus type 1 entry into macrophages mediated by macropinocytosis. Journal of Virology 2001 75 22 11166 11177 2-s2.0-0034755158 10.1128/JVI.75.22.11166-11177.2001 (Pubitemid 33031583)
103. Vidricaire G., Gauthier S., Tremblay M. J., HIV-1 infection of trophoblast is independent of gp120/CD4 interactions but relies on heparan sulfate proteoglycans. Journal of Infectious Diseases 2007 195 10 1461 1471 2-s2.0-34248202589 10.1086/515576 (Pubitemid 46717464)
104. Vidricaire G., Tardif M. R., Tremblay M. J., The low viral production in trophoblastic cells is due to a high endocytic internalization of the human immunodeficiency virus type 1 and can be overcome by the pro-inflammatory cytokines tumor necrosis factor- α and interleukin-1. Journal of Biological Chemistry 2003 278 18 15832 15841 2-s2.0-0038240663 10.1074/jbc.M210470200 (Pubitemid 36799698)
105. Gobeil L. A., Lodge R., Tremblay M. J., Differential HIV-1 endocytosis and susceptibility to virus infection in human macrophages correlate with cell activation status. Journal of Virology 2012 86 19 10399 10407
106. Chapman H. A., Endosomal proteolysis and MHC class II function. Current Opinion in Immunology 1998 10 1 93 102 2-s2.0-0032005330 10.1016/S0952-7915(98) 80038-1 (Pubitemid 28112086)
107. Espagne E., Douris V., Lalmanach G., Provost B., Cattolico L., Lesobre J., Kurata S., Iatrou K., Drezen J. M., Huguet E., A virus essential for insect host-parasite interactions encodes cystatins. Journal of Virology 2005 79 15 9765 9776 2-s2.0-22544453620 10.1128/JVI.79.15.9765-9776.2005 (Pubitemid 41022319)
108. Manoury B., Gregory W. F., Maizels R. M., Watts C., Bm-CPI-2, a cystatin homolog secreted by the filarial parasite Brugia malayi, inhibits class II MHC-restricted antigen processing. Current Biology 2001 11 6 447 451 2-s2.0-0035916803 10.1016/S0960-9822(01)00118-X (Pubitemid 32241523)
109. Yu B., Fonseca D. P. A. J., O'Rourke S. M., Berman P. W., Protease cleavage sites in HIV-1 gp120 recognized by antigen processing enzymes are conserved and located at receptor binding sites. Journal of Virology 2010 84 3 1513 1526 2-s2.0-73949101842 10.1128/JVI.01765-09
110. Clements G. J., Price-Jones M. J., Stephens P. E., Sutton C., Schulz T. F., Clapham P. R., McKeating J. A., McClure M. O., Thomson S., Marsh M., Kay J., Weiss R. A., Moore J. P., The V3 loops of the HIV-1 and HIV-2 surface glycoproteins contain proteolytic cleavage sites: a possible function in viral fusion? AIDS Research and Human Retroviruses 1991 7 1 3 16 2-s2.0-0025969914
111. Ei Messaoudi K., Thiry L., Van Tieghem N., Liesnard C., Englert Y., Moguilevsky N., Bollen A., HIV-1 infectivity and host range modification by cathepsin D present in human vaginal secretions. AIDS 1999 13 3 333 339 2-s2.0-0032968948 10.1097/00002030-199902250-00005 (Pubitemid 29095095)
112. El Messaoudi K., Thiry L. F., Liesnard C., Van Tieghem N., Bollen A., Moguilevsky N., A human milk factor susceptible to cathepsin D inhibitors enhances human immunodeficiency virus type 1 infectivity and allows virus entry into a mammary epithelial cell line. Journal of Virology 2000 74 2 1004 1007 2-s2.0-0033989108 10.1128/JVI.74.2.1004-1007.2000 (Pubitemid 30036238)
113. Moriuchi H., Moriuchi M., Fauci A. S., Cathepsin G, A neutrophil-derived serine protease, Increases susceptibility of macrophages to acute human immunodeficiency virus type 1 infection. Journal of Virology 2000 74 15 6849 6855 2-s2.0-0033925796 10.1128/JVI.74.15.6849-6855.2000 (Pubitemid 30470668)
114. Frecha C., Szécsi J., Cosset F. L., Verhoeyen E., Strategies for targeting lentiviral vectors. Current Gene Therapy 2008 8 6 449 460 2-s2.0-60649084807 10.2174/156652308786848003
115. Morizono K., Chen I. S. Y., Receptors and tropisms of envelope viruses. Current Opinion in Virology 2011 1 1 13 18 2-s2.0-79960466427 10.1016/j.coviro.2011.05.001
116. Lin A. H., Kasahara N., Wu W., Stripecke R., Empig C. L., Anderson W. F., Cannon P. M., Receptor-specific targeting mediated by the coexpression of a targeted murine leukemia virus envelope protein and a binding-defective influenza hemagglutinin protein. Human Gene Therapy 2001 12 4 323 332 2-s2.0-0035119465 10.1089/10430340150503957 (Pubitemid 32186645)
117. Wu B. W., Lu J., Gallaher T. K., Anderson W. F., Cannon P. M., Identification of regions in the Moloney murine leukemia virus SU protein that tolerate the insertion of an integrin-binding peptide. Virology 2000 269 1 7 17 2-s2.0-0034732096 10.1006/viro.2000.0201 (Pubitemid 30183164)
118. Benedict C. A., Tun R. Y. M., Rubinstein D. B., Guillaume T., Cannon P. M., Anderson W. F., Targeting retroviral vectors to CD34-Expressing cells: binding to CD34 does not catalyze virus-cell fusion. Human Gene Therapy 1999 10 4 545 557 2-s2.0-0033106289 10.1089/10430349950018625 (Pubitemid 29131321)
119. Martin F., Kupsch J., Takeuchi Y., Russell S., Cosset F. L., Collins M., Retroviral vector targeting to melanoma cells by single-chain antibody incorporation in envelope. Human Gene Therapy 1998 9 5 737 746 2-s2.0-0032549491 (Pubitemid 28200629)
120. Cosset F. L., Morling F. J., Takeuchi Y., Weiss R. A., Collins M. K. L., Russell S. J., Retroviral retargeting by envelopes expressing an N-terminal binding domain. Journal of Virology 1995 69 10 6314 6322 2-s2.0-0029094549
121. Gollan T. J., Green M. R., Selective targeting and inducible destruction of human cancer cells by retroviruses with envelope proteins bearing short peptide ligands. Journal of Virology 2002 76 7 3564 3569 2-s2.0-0036124254 10.1128/JVI.76.7.3564-3569.2002 (Pubitemid 34224558)
122. Yajima T., Kanda T., Yoshiike K., Kitamura Y., Retroviral vector targeting human cells via c-Kit-Stem cell factor interaction. Human Gene Therapy 1998 9 6 779 787 2-s2.0-0032502850 (Pubitemid 28197365)
123. Katane M., Takao E., Kubo Y., Fujita R., Amanuma H., Factors affecting the direct targeting of murine leukemia virus vectors containing peptide ligands in the envelope protein. EMBO Reports 2002 3 9 899 904 2-s2.0-0036748470 10.1093/embo-reports/kvf179 (Pubitemid 35154118)
124. Li F., Ryu B. Y., Krueger R. L., Heldt S. A., Albritton L. M., Targeted entry via somatostatin receptors using a novel modified retrovirus glycoprotein that delivers genes at levels comparable to those of wild-type viral glycoproteins. Journal of Virology 2012 86 1 373 381 10.1128/JVI.05411-11
125. Katane M., Fujita R., Takao E., Kubo Y., Aoki Y., Amanuma H., An essential role for the His-8 residue of the SDF-1 α -chimeric, tropism-redirected Env protein of the Moloney murine leukemia virus in regulating postbinding fusion events. Journal of Gene Medicine 2004 6 3 260 267 2-s2.0-7444257938 10.1002/jgm.487 (Pubitemid 40228043)
126. Simmons G., Reeves J. D., Rennekamp A. J., Amberg S. M., Piefer A. J., Bates P., Characterization of severe acute respiratory syndrome-associated coronavirus (SARS-CoV) spike glycoprotein-mediated viral entry. Proceedings of the National Academy of Sciences of the United States of America 2004 101 12 4240 4245 2-s2.0-1642488368 10.1073/pnas.0306446101 (Pubitemid 38405913)
127. Moore M. J., Dorfman T., Li W., Wong S. K., Li Y., Kuhn J. H., Coderre J., Vasilieva N., Han Z., Greenough T. C., Farzan M., Choe H., Retroviruses pseudotyped with the severe acute respiratory syndrome coronavirus spike protein efficiently infect cells expressing angiotensin-converting enzyme 2. Journal of Virology 2004 78 19 10628 10635 2-s2.0-4544289289 10.1128/JVI.78.19.10628- 10635.2004 (Pubitemid 39258389)
128. Yonezawa A., Cavrois M., Greene W. C., Studies of Ebola virus glycoprotein-mediated entry and fusion by using pseudotyped human immunodeficiency virus type 1 virions: involvement of cytoskeletal proteins and enhancement by tumor necrosis factor alpha. Journal of Virology 2005 79 2 918 926 2-s2.0-11144221586 10.1128/JVI.79.2.918-926.2005 (Pubitemid 40053875)
129. Bhattacharyya S., Warfield K. L., Ruthel G., Bavari S., Aman M. J., Hope T. J., Ebola virus uses clathrin-mediated endocytosis as an entry pathway. Virology 2010 401 1 18 28 2-s2.0-77950934528 10.1016/j.virol.2010.02.015
130. Nanbo A., Imai M., Watanabe S., Noda T., Takahashi K., Neumann G., Halfmann P., Kawaoka Y., Ebolavirus is internalized into host cells via macropinocytosis in a viral glycoprotein-dependent manner. PLoS Pathogens 2010 6 9 2-s2.0-78149355646 10.1371/journal.ppat.1001121 e01121
131. Saeed M. F., Kolokoltsov A. A., Albrecht T., Davey R. A., Cellular entry of ebola virus involves uptake by a macropinocytosis-like mechanism and subsequent trafficking through early and late endosomes. PLoS Pathogens 2010 6 9 2-s2.0-78149301316 10.1371/journal.ppat.1001110 e01110
132. Aleksandrowicz P., Marzi A., Biedenkopf N., Beimforde N., Becker S., Hoenen T., Feldmann H., Schnittler H.-J., Ebola virus enters host cells by macropinocytosis and clathrin-mediated endocytosis. Journal of Infectious Diseases 2011 204 supplement 3 S957 S967 10.1093/infdis/jir326
133. Mulherkar N., Raaben M., de la Torre J. C., Whelan S. P., Chandran K., The Ebola virus glycoprotein mediates entry via a non-classical dynamin-dependent macropinocytic pathway. Virology 2011 419 2 72 83 10.1016/j.virol.2011.08.009
134. Hunt C. L., Kolokoltsov A. A., Davey R. A., Maury W., The Tyro3 receptor kinase Axl enhances macropinocytosis of Zaire ebolavirus. Journal of Virology 2011 85 1 334 347 2-s2.0-78650045778 10.1128/JVI.01278-09
135. Schornberg K., Matsuyama S., Kabsch K., Delos S., Bouton A., White J., Role of endosomal cathepsins in entry mediated by the Ebola virus glycoprotein. Journal of Virology 2006 80 8 4174 4178 2-s2.0-33645788357 10.1128/JVI.80.8. 4174-4178.2006
136. Cosset F.L. Lavillette D. Cell entry of enveloped viruses Advances in Genetics 2011 73 C 121-183 2-s2.0-79551639004 10.1016/B978-0-12-380860-8.00004- 5.