Entry of viruses through the epithelial barrier: Pathogenic trickery

Nature Reviews Molecular Cell Biology

Volumn 4, Issue 1, 2003, Pages 57-68

  Bomsel, Morgane ^a   Alfsen, Annette ^a  

^a UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSID PROTEIN; CELL ADHESION MOLECULE; GENOMIC DNA; GLYCOSPHINGOLIPID; HEMAGGLUTININ; INTEGRIN; OLIGOSACCHARIDE; PROTEOGLYCAN; RNA; SIALIDASE; VIRUS PROTEIN; VIRUS RECEPTOR;

ADENOVIRUS; CELL JUNCTION; DNA VIRUS; ENDOCYTOSIS; ENDOSOME; EPITHELIUM CELL; HOST CELL; HUMAN; INFLUENZA VIRUS; NONHUMAN; PRIORITY JOURNAL; REVIEW; RNA VIRUS; VIRUS CELL INTERACTION; VIRUS INFECTION;

ANIMALS; BIOLOGICAL TRANSPORT; EPITHELIAL CELLS; HUMANS; RECEPTORS, VIRUS; SIGNAL TRANSDUCTION; VIRAL PHYSIOLOGY; VIRUSES;

ADENOVIRIDAE; DNA VIRUSES; INFLUENZA VIRUS; RNA VIRUSES;

EID: 0037226498     PISSN: 14710072     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrm1005     Document Type: Review

References (124)

1. Gabius, H., Andre, S., Kaltner, H. & Siebert, H. The sugar code: functional lectinomics. Biochim. Biophys. Acta 19, 2-3 (2002).
2. Compans, R. W. Virus entry and release in polarized epithelial cells Curr. Top. Microbiol. Immunol. 202, 209-219 (1995)
3. Bomsel, M. Transcytosis of infectious human immunodeficiency virus across a tight human epithelial cell line barrier. Nature Med. 3, 42-47 (1997). This reports the characterization of a novel pathway for HIV transmission at mucosal sites.
4. Meng, G. et al. Primary intestinal epithelial cells selectively transfer R5 HIV-1 to CCR5+ cells. Nature Med. 8, 150-156 (2002). An ex vivo system using human primary epithelial cells to show the selective filter function of an epithelial barrier during a viral infection.
5. Smith, G. A. & Enquist, L. W. Break ins and break outs: viral interactions with the cytoskeleton of mammalian cells. Annu. Rev. Cell Dev. Biol. 8, 135-161 (2002)
6. Gan, Y. J., Chodosh, J., Morgan, A. & Sixbey, J. W. Epithelial cell polarization is a determinant in the infectious outcome of immunoglobulin A-mediated entry by Epstein-Barr virus. J. Virol. 71, 519-526 (1997).
7. Eliopoulos, A. G. et al. Epstein-Barr virus-encoded LMP1 and CD40 mediate IL-6 production in epithelial cells via an NF-κB pathway involving TNF receptor-associated factors. Oncogene 14, 2899-2916 (1997).
8. Desgranges, C. et al. Detection of Epstein-Barr viral DNA internal repeats in the nasopharyngeal mucosa of Chinese with IgA/EBV-specific antibodies. Int. J. Cancer 29, 87-91 (1982).
9. Iwasaki, A. et al. Immunofluorescence analysis of poliovirus receptor expression in Payer's patches of humans, primates, and CD155 transgenic mice: implications for poliovirus infection. J. Infect. Dis. 186, 585-592 (2002).
10. Fotopoulos, G. et al. Transepithelial transport of HIV-1 by M cells is receptor-mediated. Proc. Natl Acad. Sci. USA 99, 9410-9414 (2002).
11. Wolf, J. L. et al. Intestinal M cells: a pathway for entry of reovirus into the host. Science 212, 471-472 (1981).
12. Wang, G. Human coronavirus 229E infects polarized airway epithelia from the apical surface. J. Virol. 74, 9234-9239 (2000).
13. Blau, D. M. & Compans, R. W. Entry and release of measles virus are polarized in epithelial cells. Virology 210, 91-99 (1995).
14. Ravkov, E. V., Nichol, S. T. & Compans, R. W. Polarized entry and release in epithelial cells of Black Creek Canal virus, a New World hantavirus. J. Virol. 71, 1147-1154 (1997).
15. Jarvis, M. A. et al. Human cytomegalovirus infection of caco-2 cells occurs at the basolateral membrane and is differentiation state dependent. J. Virol. 73, 4552-4560 (1999).
16. Spear, P. G. A first step toward understanding membrane fusion induced by herpes simplex virus. Mol. Cell 8, 2-4 (2001).
17. Yoon, M. & Spear, P. G. Disruption of adherens junctions liberates nectin-1 to serve as receptor for herpes simplex virus and pseudorabies virus entry. J. Virol. 76, 7203-7208 (2002).
18. Irurzun, A. & Carrasco, L. Entry of poliovirus into cells is blocked by valinomycin and concanamycin A. Biochemistry 40, 3589-3600 (2001)
19. Kronenberger, P. et al. Uptake of poliovirus into the endosomal system of HeLa cells. Arch. Virol. 143, 1417-1424 (1998).
20. Ciarlet, M. & Estes, M. K. Interactions between rotavirus and gastrointestinal cells. Curr. Opin. Microbiol. 4, 435-441 (2001).
21. Hughes, M. T., Matrosovich, M., Rodgers, M. E., McGregor, M. & Kawaoka, Y. Influenza A viruses lacking sialidase activity can undergo multiple cycles of replication in cell culture, eggs, or mice. J. Virol. 74, 5206-5212 (2000).
22. Blank, C. A., Anderson, D. A., Beard, M. & Lemon, S. M. Infection of polarized cultures of human intestinal epithelial cells with hepatitis A virus: vectorial release of progeny virions through apical cellular membranes. J. Virol. 74, 6476-6484 (2000).
23. Carfi, A. et al. Herpes simplex virus glycoprotein D bound to the human receptor HveA. Mol. Cell 8, 169-179 (2001).
24. Topp, K. S., Bisla, K., Saks, N. D & Lavail, J. H. Centripetal transport of herpes simplex virus in human retinal pigment epithelial cells in vitro Neuroscience 71, 1133-1144 (1996).
25. Bodaghi, B. et al. Entry of human cytomegalovirus into retinal pigment epithelial and endothelial cells by endocytosis. Invest. Ophthalmol. Vis. Sci. 40, 2598-2607 (1999).
26. Tugizov, S. Maidji, E. & Pereira, L. Role of apical and basolateral membranes in replication of human cytomegalovirus in polarized retinal pigment epithelial cells. J. Gen. Virol. 77, 61-74 (1996).
27. Topp, K. S., Rothman, A. L. & Lavail, J. H. Herpes virus infection of RPE and MDCK cells: polarity of infection. Exp. Eye Res. 64, 343-354 (1997).
28. Duan, D., Yue, Y., Yan, Z., McCray, P. B. Jr & Engelhardt, J. F. Polarity influences the efficiency of recombinant adenoassociated virus infection in differentiated airway epithelia. Hum. Gene Ther. 9, 2761-2776 (1998).
29. Strous, G. J. & Govers, R. The ubiquitin-proteasome system and endocytosis. J. Cell Sci. 112, 1417-1423 (1999).
30. Duan, D., Yue, Y., Yan, Z., Yang, J. & Engelhardt, J. F. Endosomal processing limits gene transfer to polarized airway epithelia by adeno-associated virus. J. Clin. Invest. 105, 1573-1587 (2000).
31. Bavari, S. et al. Lipid raft microdomains: a gateway for compartmentalized trafficking of Ebola and Marburg viruses. J. Exp. Med. 195, 593-602 (2002).
32. Manie, S. N., Debreyne, S., Vincent, S. & Gerlier, D. Measles virus structural components are enriched into lipid raft microdomains: a potential cellular location for virus assembly. J. Virol. 74, 305-311 (2000).
33. Simons, K. & Toomre, D. Lipid rafts and signal transduction. Nature Rev. Mol. Cell Biol. 1, 31-39 (2000).
34. Norkin, L C., Anderson, H. A., Wolfrom, S. A. & Oppenheim, A. Caveolar endocytosis of simian virus 40 is followed by Brefeldin A-sensitive transport to the endoplasmic reticulum, where the virus disassembles. J. Virol. 76, 5156-5166 (2002).
35. Stang, E., Kartenbeck, J. & Parton, R. G. Major histocompatibility complex class I molecules mediate association of SV40 with caveolae. Mol. Biol. Cell 8, 47-57 (1997).
36. Pho, M. T., Ashok, A. & Atwood, W. J. JC virus enters human glial cells by clathrin-dependent receptor-mediated endocytosis. J. Virol. 74, 2288-2292 (2000).
37. Parker, J. S., Murphy, W. J., Wang, D., O'Brien, S. J. & Parrish, C. R. Canine and feline parvoviruses can use human or feline transferrin receptors to bind, enter, and infect cells. J. Virol. 75, 3896-3902 (2001).
38. Joki-Korpela, P., Marjomaki, V., Krogerus, C., Heino, J. & Hyypia, T. Entry of human parechovirus 1. J. Virol. 75, 1958-1967 (2001).
39. DeTulleo, L. & Kirchhausen, T. The clathrin endocytic pathway in viral infection EMBO J. 17, 4585-4593 (1998).
40. Fry, E. E. et al. The structure and function of a foot-and-mouth disease virus-oligosaccharide receptor complex. EMBO J. 18, 543-554 (1999).
41. Schober, D., Kronenberger, P., Prchia, E., Blaas, D. & Fuchs, R. Major and minor receptor group human rhinoviruses penetrate from endosomes by different mechanisms. J. Virol. 72, 1354-1364 (1998). This work tracks the entry of comparatively different viruses of the same family into cells by cell-fractionation analysis.
42. 2+ in the replication and pathogenesis of rotavirus and other viral infections. Cell Calcium 28, 137-149 (2000) A clear review on the role of calcium in viral infection of the epithelial cell, and the viral soluble virulence factors.
43. Knodler, L. A., Celli, J. & Finlay, B. B. Pathogenic trickery: deception of host cell processes. Nature Rev. Mol. Cell Biol. 2, 578-588 (2001).
44. Weis, W. I. & Drickamer, K. Structural basis of lectin-carbohydrate recognition. Annu. Rev. Biochem. 65, 441-473 (1996). An important review on the characteristics of lectin-carbohydrate interactions that rely on the structure and oligomerization state of the lectin peptide, as well as on the nature and conformation of the carbohydrate.
45. Stuart, A. D., Eustace, H. E., McKee, T. A. & Brown, T. D. A novel cell entry pathway for a DAF-using human enterovirus is dependent on lipid rafts. J. Virol. 76, 9307-9322 (2002).
46. Dimitrov, D. S. Cell biology of virus entry. Cell 101, 697-702 (2000).
47. Shukla, D. & Spear, P. G. Herpesviruses and heparansulfate: an intimate relationship in aid of viral entry. J. Clin. Invest. 108, 503-510 (2001). Reference 47 uses herpesviruses to emphasize the role of heparan sulphate - a ubiquitous component of cell proteoglycans - in viral entry into host cells.
48. Skehel, J. J. & Wiley D. C. Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. Annu. Rev. Biochem. 69, 531-569 (2000).
49. Suzuki, S. et al. Broad distribution of the JC virus receptor contrasts with a marked cellular restriction of virus replication Virology 286, 100-112 (2001).
50. Markwell, M. A. & Paulson, J. C. Sendai virus utilizes specific sialyloligosaccharides as host cell receptor determinants. Proc. Natl Acad. Sci. USA 77, 5693-5697 (1980).
51. Delorme, C. et al. Glycosphingolipid binding specificities of rotavirus: identification of a sialic acid-binding epitope. J. Virol. 75, 2276-2287 (2001). Among the various ganglioside specificities for different rotavirus strains, a common carbohydrate minimal structural element is shown to be required for binding of these strains.
52. Barton, E. S., Connolly, J. L., Forrest, J. C., Chappell, J. D. & Dermody, T. S. Utilization of sialic acid as a coreceptor enhances reovirus attachment by multistep adhesion strengthening J. Biol. Chem. 276, 2200-2211 (2001). Using naked reovirus as an example, this paper shows the cooperativity of carbohydrate attachment and protein receptors for virus interaction with epithelial cells.
53. van der Bijl, P., Lopes-Cardozo, M. & van Meer, G. Sorting of newly synthesized glycosphingolipids to the two surface domains of epithelial cells. J. Cell Biol. 132, 813-821 (1996).
54. Hakomori, S. I. Inaugural article: the glycosynapse. Proc. Natl Acad. Sci, USA 99, 225-232 (2002). The cell-to-cell transfer of information through the synapse, which is characteristic of neural cells, has recently been extended to other cell types such as immunological synapses. The importance of carbohydrates in such cellular functions is underlined.
55. Raulin, J. Human immunodeficiency virus and host cell lipids. Interesting pathways in research for a new HIV therapy. Prog. Lipid Res. 41, 27-65 (2002).
56. Alfsen, A., Iniguez, R., Bouguyon, E. & Bomsel, M. Secretory IgA specific for a conserved epitope on gp41 envelope glycoprotein inhibits epithelial transcytosis of HIV-1. J. Immunol. 166, 6257-6265 (2001).
57. Alfsen, A. & Bomsel, M. HIV-1 gp41 envelope residues 650-685 exposed on native virus act as a lectin to bind epithelial cell galactosyl ceramide. J. Biol Chem. 277, 25649-25659 (2002).
58. Fantini, J. et al. Synthetic soluble analogs of galactosylceramide (GalCer) bind to the V3 domain of HIV-1 gp120 and inhibit HIV-1-induced fusion and entry. J. Biol. Chem. 272, 7245-7452 (1997).
59. Simons, K. A. & van Meer, G. Lipid sorting in epithelial cells. Biochemistry 27, 6197-6202 (1988).
60. Mahfoud, R. et al. Identification of a common sphingolipid-binding domain in Alzheimer, prion, and HIV-1 proteins. J. Biol. Chem. 277, 11292-11296 (2002).
61. Hallak, L. K., Spillmann, D., Collins, P. L. & Peeples, M. E. Glycosaminoglycan sulfation requirements for respiratory syncytial virus infection. J. Virol. 74, 10508-10513 (2000).
62. Turnbull, J., Powell, A. & Guimond, S. Heparan sulfate: decoding a dynamic multifunctional cell regulator. Trends Cell Biol. 11, 75-82 (2001). An informative review on the structure and function of heparan sulphate.
63. Immergruck, L. C., Domowicz, M. S., Schwartz, N. B. & Herold, B. C. Viral and cellular requirements for entry of herpes simplex virus type 1 into primary neuronal cells. J. Gen. Virol. 79, 549-559 (1998).
64. Wang, F. Z., Akula, S. M., Pramod, N. P., Zeng, L. & Chandran, B. Human herpesvirus 8 envelope glycoprotein K8.1 A interaction with the target cells involves heparan sulfate. J. Virol. 75, 7517-7527 (2001).
65. Feldman, S. A., Audet, S. & Beeler, J. A. The fusion glycoprotein of human respiratory syncytial virus facilitates virus attachment and infectivity via an interaction with cellular heparan sulfate. J. Virol. 74, 6442-6447 (2000).
66. Dechecchi, M. C. et al. Heparan sulfate glycosaminoglycans are receptors sufficient to mediate the initial binding of adenovirus types 2 and 5, J. Virol. 75, 8772-8780 (2001).
67. Goodfellew, I. G., Sioofy, A. B., Powell, R. M. & Evans, D. J., Echoviruses bind heparan sulfate at the cell surface. J. Virol. 75, 4918-4921 (2001).
68. Summerford, C. & Samulski, R. J. Membrane-associated heparan sulfate proteoglycan is a receptor for adeno-associated virus type 2 virions. J. Virol. 72, 1438-1445 (1998).
69. Barton, E. S. et al. Junction adhesion molecule is a receptor for reovirus, Cell 104, 441-451 (2001).
70. Giroglou, T., Florin, L., Schafer, F., Streeck, R. E. & Sapp, M. Human papillomavirus infection requires cell surface heparan sulfate. J. Virol. 75, 1565-1570 (2001).
71. 6 in infection by foot-and-mouth disease virus. J. Virol. 75, 4158-4164 (2001).
72. WuDunn, D. & Spear, P. G. Initial interaction of herpes simplex virus with cells is binding to heparan sulfate. J. Virol. 63, 52-58 (1989).
73. [3], mediates rotavirus cell entry. Proc. Natl Acad. Sci. USA 97, 14644-14849 (2000).
74. Ruoslahti, E. RGD and other recognition sequences for integrins. Annu. Rev. Cell Dev. Biol. 12, 697-715 (1996).
75. 1 (CD 49c/29) is a cellular receptor for Kaposi's sarcoma-associated herpesvirus (KSHV/HHV-8) entry into the target cells. Cell 108, 407-419 (2002).
76. 1) integrin promotes rotavirus entry into cells but is not necessary for rotavirus attachment J. Virol. 76, 1109-1123 (2002).
77. Coulson, B. S., Londrigan, S. L. & Lee, D. J. Rotavirus contains integrin ligand sequences and a disintegrin-like domain that are implicated in virus entry into cells. Proc. Natl Acad. Sci USA 94, 5389-5394 (1997)
78. Mendez, E., Lopez, S., Cuadras, M. A., Romero, R & Arias, C. F. Entry of rotaviruses is a multistep process. Virology 263, 450-459 (1999).
79. [v] integrins requires phosphoinositide-3-OH kinase. J. Virol. 72, 2055-2061 (1998).
80. Marjomaki, V. et al. Internalization of echovirus 1 in caveolae. J. Virol. 76, 1856-1865 (2002).
81. Reischl, A. et al. Viral evolution toward change in receptor usage: adaptation of a major group of human rhinovirus to grow in ICAM-1-negative cells. J. Virol. 75, 9312-9319 (2001). The ability of a group of viruses to adapt to different cell receptors seems, in part, to be responsible for the difficulties in protecting a specific type of cell from viral entry.
82. Cohen, C. J. et al. The coxsackievirus and adenovirus receptor is a transmembrane component of the tight junction. Proc. Natl Acad. Sci. USA 98, 15191-15196 (2001). This characterization of the cellular function of the coxsackievirus and adenovirus receptor (CAR) sheds light on the polarity of the entry of these viruses into epithelial cells.
83. Geraghty, R. J., Krummenacher, C., Cohen, G. H., Eisenberg, R. J. & Spear, P. G. Entry of α-herpesviruses mediated by poliovirus receptor-related protein 1 and pollovirus receptor Science 280, 1618-1620 (1998).
84. Rossen, J. W., Horzinek, M. C. & Rottier, P. J. Coronavirus infection of polarized epithelial cells. Trends Microbiol. 3, 488-490 (1995).
85. Lewicki, D. N. & Gallagher, T. M. Quaternary structure of coronavirus spikes in complex with carcinoembryonic antigen-related cell adhesion molecule cellular receptors. J. Biol. Chem. 277, 19727-19734 (2002).
86. Rodriguez-Boulan, E. & Sabatini, D. D. Assymetric budding of viruses in epthelial cells: a model system for study of epithelial polarity. Proc. Natl. Acad. Sci. USA 75, 5071-5075 (1978).
87. Yongning, H. et al. Interaction of the poliovirus receptor with poliovirus. Proc. Natl Acad. Sci. USA 97, 79-84 (2000).
88. Apodaca, G. Endocytic traffic in polarized epithelial cells: role of the actin and microtubule cytoskeleton. Traffic 2, 149-159 (2001).
89. Sabharanjak, S., Sharma, P., Parton, R. G. & Mayor, S. GPI-anchored proteins are delivered to recycling endosomes via a distinct cdc42-regulated, clathrin-independent pinocytic pathway. Dev. Cell 2, 411-423 (2002).
90. Kerneis, S., Bogdanova, A., Kraehenbuhl, J. P. & Pringault, E. Conversion by Peyer's patch lymphocytes of human enterocytes into M cells that transport bacteria. Science 277, 949-952 (1997).
91. Phirlips, D. M. The role of cell-to-cell transmission in HIV infection. AIDS 8, 719-731 (1994).
92. Imai, S., Nishikawa, J. & Takada, K. Cell-to-cell contact as an efficient mode of Epstein-Barr virus infection of diverse human epithelial cells. J. Virol. 72, 4371-4378 (1998).
93. Smith, P. D., Meng, G. Sellers, M. T., Rogers, T. S. & Shaw, G. M. Biological parameters of HIV-1 infection in primary intestinal lymphocytes. J. Leukoc. Biol. 68, 360-365 (2000)
94. Agace, W. W. et al. Constitutive expression of stromal derived factor-1 by mucosal epithelia. Curr. Biol. 10, 325-328 (2000).
95. Elliott, G. & O'Hare, P. Intercellular trafficking and protein delivery by a herpesvirus structural protein. Cell 88, 223-233 (1997).
96. Hayashi, K. Role of tight junctions of polarized epithelial MDCK cells in the replication of herpes simplex virus type 1. J. Med. Virol. 47, 323-329 (1995).
97. Ohare, P. T., Chin, M. S. & La Vail J. H. The spread of herpes simplex virus type 1 from trigeminal neurons to the murine cornea: an immunoelectron microscopy study. J. Virol. 74, 4776-4786 (2000)
98. Miyazaki, D. et al. Neutrophil chemotaxis induced corneal epithelial cells after herpes simplex virus type 1 infection. Curr. Eye Res. 17, 687-693 (1998).
99. Esclatine, A., Lemullois, M., Servin, A. L., Quero, A. M. & Geniteau-Legendre, M. Human cytomegalovirus infects Caco-2 intestinal epithelial cells basolaterally regardless of the differentiation state. J. Virol. 74, 513-517 (2000).
100. Chodosh, J., Gan, Y., Holder, V. P. & Sixbey, J. W. Patterned entry and egress by Epstein-Barr virus in polarized CR2-posttive epithelial cells. Virology 266, 387-396 (2000)
101. Molesworth, S. J., Lake, C. M., Borza, C. M., Turk, S. M. & Hutt-Fletcher, L. M. Epstein-Barr virus gH is essential for penetration of B cells but also plays a role in attachment of virus to epithelial cells. J. Virol. 74, 6324-6332 (2000).
102. Rodriguez, D., Rodriguez, J. R., Ojakian, G. K. & Esteban, M. Vaccinia virus preferentially enters polarized epithelial cells through the basolateral surface. J. Virol. 65, 494-498 (1991).
103. Hammache, D. et al. Specific interaction of HIV-1 and HIV-2 surface envelope glycoproteins with monolayers of galactosylceramide and ganglioside GM3. J. Biol. Chem. 273, 7967-7971 (1998).
104. Saito, T. et al. Respiratory syncytial virus induces selective production of the chemokine RANTES by upper airway epithelial cells. J. Infect. Dis. 175, 497-504 (1997).
105. Techaarpornkul, S., Collins, P. L. & Peeples, M. E. Respiratory syncytial virus with the fusion protein as its only viral glycoprotein is less dependent on cellular glycosaminoglycans for attachment than complete virus, Virology 294, 296-304 (2002).
106. Fujioka, H. et al. Immunocytochemical colocalization of specific immunoglobulin A with Sendai virus protein in infected polarized epithelium. J. Exp. Med. 188, 1223-1229 (1998).
107. Maisner, A., Klenk, H. & Herrler, G. Polarized budding of measles virus is not determined by viral surface glycoproteins. J. Virol. 72, 5276-5278 (1998).
108. Naim, H. Y., Ehler, E. & Billeter M. A. Measles virus matrix protein specifies apical virus release and glycoprotein sorting in epithelial cells. EMBO J. 19, 3576-3585 (2000).
109. 5 integrin as a candidate receptor for papillomaviruses. J. Virol. 71, 2449-2456 (1997)
110. Zhang, J., Pekosz, A. & Lamb, R. A. Influenza virus assembly and lipid raft microdomains: a role for the cytoplasmic tails of the spike glycoproteins. J. Virol. 74, 4634-6444 (2000).
111. Zimmer, G., Zimmer K. P., Trotz, I. & Herrler, G. Vesicular stomatitis virus glycoprotein does not determine the site of virus release in polarized epithelial cells. J. Virol. 76, 4103-4107 (2002).
112. Brunet, J. P. et al. Rotavirus infection induces cytoskeleton disorganization in human intestinal epithelial cells: implication of an increase in intracellular calcium concentration. J. Virol. 74, 10801-10806 (2000).
113. Casola, A. et al. Rotavirus infection of cultured intestinal epithelial cells induces secretion of CXC and CC chemokines. Gastroenterology 114, 947-955 (1998).
114. Barton, E. S., Chappell, J. D., Connolly, J. L., Forrest, J. C. & Dermody, T. S. Reovirus receptors and apoptosis. Virology 290, 173-180 (2001).
115. Chappell, J. D., Duong, J. L., Wright, B. W. & Dermody, T. S. Identification of carbohydrate-binding domains in the attachment proteins of type 1 and type 3 reoviruses. J. Virol. 74, 8472-8479 (2000).
116. Pickles, R. J., Fahrner, J. A., Petrella, J. M., Boucher, R. C. & Bergelson, J. M. Retargeting the coxsackievirus and adenovirus receptor to the apical surface of polarized epithelial cells reveals the glycocafyx as a barrier to adenovirus-mediated gene transfer. J. Virol. 74, 6050-6057 (2000).
117. Walters, R. W. et al. Basolateral localization of fiber receptors limits adenovirus infection from the apical surface of airway epithelia. J. Biol. Chem. 274, 10219-10226 (1999).
118. Kolatkar, P. R. et al. Structural studies of two rhinovirus serotypes complexed with fragments of their cellular receptor. EMBO J 18, 6249-6259 (1999)
119. Bayer, N., Schober, D., Huttinger, M., Blaas, D. & Fuchs, R. Inhibition of clathrin-dependent endocytosis has multiple effects on human rhinovirus serotype 2 cell entry. J. Biol. Chem. 276, 3952-3962 (2001).
120. Golovkina, T. V. et al. A novel membrane protein is a mouse mammary tumor virus receptor. J. Virol. 72, 3066-3071 (1998).
121. Rossen, J. W. et al. Coronaviruses in polarized epithelial cells. Adv. Exp. Med. Biol. 380, 135-138 (1995).
122. Lin, X., O'Reilly, K. L. & Storz, J. Infection of polarized epithelial cells with enteric and respiratory tract bovine coronaviruses and release of virus progeny. Am. J. Vet. Res. 58, 1120-1124 (1997).
123. Rossen, J. W. Strous, G. J., Horzinek, M. C. & Rottier, P. J. Mouse hepatitis virus strain A59 is released from opposite sides of different epithelial cell types. J. Gen. Virol. 78, 61-69 (1997).
124. Claret, M., Isa, P., Conner, M. E. & Liprandi, F. Antigenic and molecular analyses reveal that the equine rotavirus strain H-1 is closely related to porcine, but not equine, rotaviruses: interspecies transmission from pigs to horses? Virus Genes 22, 5-20 (2001).