Expression of Coxsackie-Adenovirus receptor (CAR) in the developing mouse olfactory system

Journal of Neurocytology

Volumn 34, Issue 3-5, 2005, Pages 295-305

  Venkatraman, Giri ^a,b   Behrens, Maik ^a,c   Pyrski, Martina ^a,c   Margolis, Frank L ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b Sg2 Health Care Intelligence   (United States)

^c GERMAN INSTITUTE OF HUMAN NUTRITION   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

COXSACKIE VIRUS AND ADENOVIRUS RECEPTOR; MESSENGER RNA;

ADENOVIRUS; ADULTHOOD; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEVELOPMENTAL STAGE; EMBRYO; EMBRYO DEVELOPMENT; FEMALE; IN SITU HYBRIDIZATION; MALE; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; OLFACTORY EPITHELIUM; OLFACTORY SYSTEM; PERINATAL DEVELOPMENT; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENSORY NERVE CELL; VIRUS INFECTION; WESTERN BLOTTING;

ADENOVIRIDAE INFECTIONS; AGE FACTORS; ANIMALS; BASE SEQUENCE; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IN SITU HYBRIDIZATION; MALE; MICE; MOLECULAR SEQUENCE DATA; OLFACTORY BULB; OLFACTORY MUCOSA; PREGNANCY; RECEPTORS, VIRUS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER;

ADENOVIRIDAE; RODENTIA;

EID: 33746083214     PISSN: 03004864     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11068-005-8359-8     Document Type: Article

References (79)

1. ASTIC, L., SAUCIER, D., COULON, P., LAFAY, F. & FLAMAND, A. (1993) The CVS strain of rabies virus as transneuronal tracer in the olfactory system of mice. Brain Research 619, 146-156.
2. BABIC, N., METTENLEITER, T. C., UGOLINI, G., FLAMAND, A. & COULON, P. (1994) Propagation of pseudorabies virus in the nervous system of the mouse after intranasal inoculation. Virology 204, 616-625.
3. BANGARI, D. S. & MITTAL, S. K. (2005) Porcine adenovirus serotype 3 internalization is independent of CAR and alphavbeta3 or alphavbeta5 integrin. Virology. 332, 157-166.
4. BANGARI, D. S., SHARMA, A. & MITTAL, S. K. (2005a) Bovine adenovirus type 3 internalization is independent of primary receptors of human adenovirus type 5 and porcine adenovirus type 3. Biochemical and Biophysical Research Communications 331, 1478-1484.
5. BANGARI, D. S., SHUKLA, S. & MITTAL, S. K. (2005b) Comparative transduction efficiencies of human and nonhuman adenoviral vectors in human, murine, bovine, and porcine cells in culture. Biochemical and Biophysical Research Communications 327, 960-966.
6. BARNETT, E. M., CASSELL, M. D. & PERLMAN, S. (1993) Two neurotropic viruses, herpes simplex virus type 1 and mouse hepatitis virus, spread along different neural pathways from the main olfactory bulb. Neuroscience 57, 1007-1025.
7. BEHRENS, M., VENKATRAMAN, G., GRONOSTAJSKI, R. M., REED, R. R. & MARGOLIS, F. L. (2000) NFI in the development of the olfactory epithelium and the regulation of olfactory marker protein gene expression. European Journal of Neuroscience 12, 1372-1384.
8. BERGELSON J. M., CUNNINGHAM, J. A., DROGUETT, G., KURT-JONES, E. A., KRITHIVAS, A., HONG, J. S., HORWITZ, M. S., CROWELL, R. L. & FINBERG, R.W. (1997) Isolation of a common receptor for Coxsackie B viruses and adenoviruses 2 and 5. Science 275, 1320-1323.
9. BERGELSON, J. M., KRITHIVAS, A., CELI,L., DROGUETT, G., HORWITZ, M. S., WICKHAM, T., CROWELL, R. L. & FINBERG, R. W. (1998) The murine CAR homolog is a receptor for coxsackie B viruses and adenoviruses. Journal of Virology 72, 415-419.
10. BEWLEY, M. C., SPRINGER, K., ZHANG, Y. B., FREIMUTH, P. & FLANAGAN, J. M. (1999) Structural analysis of the mechanism of adenovirus binding to its human cellular receptor, CAR. Science 286, 1579-1583.
11. BILZER, T., PLANZ, O., LIPKIN, W. I. & STITZ, L. (1995) Presence of CD4+ and CD8+ T cells and expression of MHC class I and MHC class II antigen in horses with Borna disease virus-induced encephalitis. Brain Pathology 5, 223-230.
12. CAO, W., HENRY, M. D., BORROW, P., YAMADA, H., ELDER, J. H., RAVKOV, E. V., NICHOL, S. T., COMPANS, R. W., CAMPBELL, K. P. & OLDSTONE, M. B. (1998) Identification of alpha-dystroglycan as a receptor for lymphocytic choriomeningitis virus and Lassa fever virus. Science 282, 2079-2081
13. CHARLES, P. C., WALTERS, E., MARGOLIS, F. L. & JOHNSTON, R. E. (1995) Mechanism of neuroinvasion of Venezuelan equine encephalitis virus in the mouse. Virology 208, 662-671.
14. CHEN, W. R. & SHEPHERD, G. M. (2005) The olfactory glomerulus: A cortical module with specific functions. Journal of Neurocytology 34, 353-360.
15. CUMMINGS, D. M., EMGE, D. K., SMALL, S. L. & MARGOLIS, F. L. (2000) Pattern of olfactory bulb innervation returns after recovery from reversible peripheral deafferentation. Journal of Comparative Neurology 421, 362-373.
16. DEFER, C., BELIN, M. T., CAILLET-BOUDIN, M. L, & BOULANGER, P. (1990) Human adenovirus-host cell interactions: Comparative study with members of subgroups B and C. Journal of Virology 64, 3661-3673.
17. DALZIEL, R. G., HOPKINS, J., WATT, N. J., DUTIA, B. M., CLARKE, H, A. & MCCONNELL, I. (1991) Identification of a putative cellular receptor for the lentivirus visna virus. Journal of General Virology 72, 1905-1911.
18. DOI, K., NIBU, K., ISHIDA, H., OKADO, H., & TERSAHIMA, T. (2005) Adenovirus-mediated gene transfer in olfactory epithelium and olfactory bulb: A long term study. Annals of Otology, Rhinology & Laryngology 114, 629-633.
19. ESIRI, M. M. & TOMLINSON, A. H. (1984) Herpes simplex encephalitis. Immunohistological demonstration of spread of virus via olfactory and trigeminal pathways after infection of facial skin in mice. Journal of Neurological Science 64, 213-217.
20. FARBMAN, A. I. (1990) Olfactory neurogenesis: Genetic or environmental controls? Trends in Neuroscience 13, 362-365.
21. FARBMAN, A. I. (1992) Cell Biology of Olfaction. Cambridge, MA: Cambridge University Press.
22. FARBMAN, A. I. (1994) Developmental biology of olfactory sensory neurons. Seminars in Cell Biology 5, 3-10.
23. GRAHAM, F. L. (1990) Adenovirus-based expression vectors and recombinant vaccines. Trends in Biotechnology 8, 85-857.
24. GRAHAM, F. L. & PREVEC, L. (1992) Adenoviruses as expression vectors and recombinant vaccines. Biotechnology 20, 363-390.
25. GREBER, U. F., WILLETTS, M., WEBSTER, P. & HELENIUS, A. (1993) Stepwise dismantling of adenovirus 2 during entry into cells. Cell 75, 477-486.
26. GREVE, J. M., DAVIS, G., MEYER, A. M., FORTE, C .P., YOST, S. C., MARLOR, C. W., KAMARCK, M. E. & MCCLELLAND, A. (1989) The major human rhinovirus receptor is ICAM-1. Cell 56, 839-847.
27. GRILLO, M. & MARGOLIS, F. L. (1990) Use of reverse transcriptase polymerase chain reaction to monitor expression of intronless genes. Biotechniques 9, 262-268.
28. HARDY, S., KITAMURA, M., HARRIS-STANSIL, T., DAI, Y. & PHIPPS, M. L. (1997) Construction of adenovirus vectors through Cre-lox recombination. Journal of Virology 71, 1842-189
29. HAUWEL, M., FURON, E. & GASQUE, P. (2005) Molecular and cellular insights into the coxsackie-adenovirus receptor: Role in cellular interactions in the stem cell niche. Brain Research Brain Research Reviews 48, 265-272.
30. HILDEBRAND, J. G., & SHEPHERD, G. M. (1997) Mechanisms of olfactory discrimination: Converging evidence for common principles across phyla. Annual Review of Neuroscience 20, 595-631.
31. HOLTMAAT, A. J., HERMENS, W. T., OESTREICHER, A. B., GISPEN, W. H., KAPLITT, M. G. & VERHAAGEN, J. (1996) Efficient adenoviral vector-directed expression of a foreign gene to neurons and sustentacular cells in the mouse olfactory neuroepithelium. Brain Research Molecular Brain Research 41, 148-156.
32. HOLTMAAT, A. J., HERMENS, W. T., SONNEMANS, M. A., GIGER, R. J., VAN LEEUWEN, F. W., KAPLITT, M. G., OESTREICHER, A. B., GISPEN, W. H. & VERHAAGEN, J. (1997) Adenoviral vector-mediated expression of B-50/GAP-43 induces alterations in the membrane organization of olfactory axon terminals in vivo. Journal of Neuroscience 17, 6575-6586.
33. HONDA, T., SAITOH, H., MASUKO, M., KATAGIRIABE, T., TOMINAGA, K., KOZAKAI, I., KOBAYASHI, K., KUMANISHI, T., WATANABE, Y. G., ODANI, S. & KUWANO, R. (2000) The coxsackievirus-adenovirus receptor protein as a cell adhesion molecule in the developing mouse brain. Brain Research Molecular Brain Research. 77, 19-28.
34. HOTTA, Y., HONDA, T., NAITO, M. & KUWANO, R. (2003) Developmental distribution of coxsackie virus and adenovirus receptor localized in the nervous system. Brain Research Developmental Brain Research 143, 1-13.
35. HUARD, J. M., YOUNGENTOB, S. L., GOLDSTEIN, B. J, LUSKIN, M. B. & SCHWOB, J. E. (1998) Adult olfactory epithelium contains multipotent progenitors that give rise to neurons and non-neural cells. The Journal of Comparative Neurology 400, 469-486.
36. HUANG, D., DESBOIS, A., CHEN, G., FANG, H. & HOU, S. T. (2004) Characterization of the expression of key adenoviral receptors CAR and integrin beta3/beta5 subunits on the membrane of human NT2 neurons. Journal of Molecular Neuroscience 24, 323-328.
37. IVIC, L., PYRSKI, M. M., MARGOLIS, J. W., RICHARDS, L. J., FIRESTEIN, S. & MARGOLIS, F. L. (2000) Adenoviral vector-mediated rescue of the OMP-null phenotype in vivo. Nature Neuroscience 3, 1113-1120.
38. IVIC, L., ZHANG, C., ZHANG, X., YOON, S. O. & FIRESTEIN, S. (2002) Intracellular trafficking of a tagged and functional mammalian olfactory receptor. Journal of Neurobiology 50, 56-68.
39. LAFAY, F., COULON, P., ASTIC, L, SAUCIER, D., RICHE, D., HOLLEY, A. & FLAMAND, A. (1991) Spread of the CVS strain of rabies virus and of the avirulent mutant AvO1 along the olfactory pathways of the mouse after intranasal inoculation. Virology 183, 320-330.
40. LEE, W. C. & FULLER, A. O. (1993) Herpes simplex virus type 1 and pseudorabies virus bind to a common saturable receptor on Vero cells that is not heparan sulfate. Journal of Virology 67, 5088-5097.
41. LI, E., BROWN, S. L., STUPACK, D. G., PUENTE, X. S., CHERESH, D. A. & NEMEROW, G. R. (2001) Integrin alpha(v)beta1 is an adenovirus coreceptor. Journal of Virology 75, 5405-5409.
42. MARGOLIS, F. L., VERHAAGEN, J., BIFFO, S., HUANG, F. L. & GRILLO, M. (1991) Regulation of gene expression in the olfactory neuroepithelium: A neurogenetic matrix. Progress in Brain Research 89, 97-122.
43. MARKWELL, M. A., PORTNER, A. & SCHWARTZ, A. L. (1985) An alternative route of infection for viruses: Entry by means of the asialoglycoprotein receptor of a Sendai virus mutant lacking its attachment protein. Proceedings of the National Academy of Science USA 82, 978-982.
44. MARTIN, K., BRIE, A., SAULNIER, P., PERRICAUDET, M., YEH, P. & VIGNE, E. (2003) Simultaneous CAR-and alpha V integrin-binding ablation fails to reduce Ad5 liver tropism. Molecular Therapeutics 8, 485-494.
45. MEIER, O., & GREBER, U. F. (2004) Adenovirus endocytosis. Journal of Genetic Medicine 1 S152-S163.
46. MENDELSOHN, C. L., WIMMER, E. & RACANIELLO, V. R. (1989) Cellular receptor for poliovirus: Molecular cloning, nucleotide sequence, and expression of a new member of the immunoglobulin superfamily. Cell 10, 855-865.
47. MERKLE, F. T., TRAMONTIN, A. D., GARCIA-VERDUGO, J. M. & ALVAREZ-BUYLLA, A. (2004) Radial glia give rise to adult neural stem cells in the sub-ventricular zone. Proceedings of the National Academy of Sciences USA 101, 17528-17532.
48. MOMBAERTS, P. (1999) Molecular biology of odorant receptors in vertebrates. Annual Review of Neuroscience 22, 487-509.
49. NEMEROW, G. G., CHERESH, D. A. & WICKHAM, T. J. (1994) Adenovirus entry into host cells: A role for alpha(v) integrins. Trends in Cell Biology 4, 52-55.
50. PATTERSON, S. & RUSSELL, W. C. (1983) Ultrastructural and immunofluorescence studies of early events in adenovirus-HeLa cell interactions. Journal of General Virology 64, 1091-1099.
51. PERSSON, R., SVENSSON, U. & EVERITT, E. (1983) Virus receptor interaction in the adenovirus system. II. Capping and cooperative binding of virions on HeLa cells. Journal of Virology 46, 956-963.
52. PHILIPSON, L. & PETTERSSON, R. F. (2004) The coxsackie-adenovirus receptor-a new receptor in the immunoglobulin family involved in cell adhesion. Current Topics in Microbiology and Immunology 273, 87-111.
53. RICHARDSON, C, BRENNAN, P., POWELL, M., PRINCE, S., CHEN, Y. H., SPILLER, O. B. & ROWE, M. (2005) Susceptibility of B lymphocytes to adenovirus type 5 infection is dependent upon both coxsackie-adenovirus receptor and alphavbeta5 integrin expression. Journal of General Virology 86, 1669-1679.
54. ROELVINK, P. W., LIZONOVA, A., LEE, J. G., LI, Y., BERGELSON, J. M., FINBERG, R. W., BROUGH, D. E., KOVESDI, I. & WICKHAM, T. J. (1998) The coxsackievirus-adenovirus receptor protein can function as a cellular attachment protein for adenovirus serotypes from subgroups A, C, D, E, and F. Journal of Virology 72, 7909-7915.
55. ROELVINK, P. W., ML LEE, G., EINFELD, D. A., KOVESDI, I. & WICKHAM, T. J. (1999) Identification of a conserved receptor-binding site on the fiber proteins of CAR-recognizing adenoviridae. Science 286, 1568-1571.
56. SCHILD, D., & RESTREPO, D. (1998) Transduction mechanisms in vertebrate olfactory receptor cells. Physiological Reviews 78, 429-466.
57. SCHMIDT, A., BOCKMANN, M., STOLL, A., RACEK, T. & PUTZER, B. M. (2005) Analysis of adenovirus gene transfer into adult neural stem cells. Virus Research [Epub ahead of print].
58. SCHWOB, J. E . (2002) Neural regeneration and the peripheral olfactory system. The Anatomical Record 269, 33-49.
59. SCHWOB, J. E., SAHA, S., YOUNGENTOB, S. L. & JUBELT, B. (2001) Intranasal inoculation with the olfactory bulb line variant of mouse hepatitis virus causes extensive destruction of the olfactory bulb and accelerated turnover of neurons in the olfactory epithelium of mice. Chemical Senses 26, 937-952.
60. SHAFREN, D. R., DORAHY, D. J., INGHAM, R. A., BURNS, G. F. & BARRY, R. D.(1997) Coxsackievirus A21 binds to decay-accelerating factor but requires intercellular adhesion molecule 1 for cell entry. Journal of Virology 71, 4736-4743.
61. SMELT, S. C., BORROW, P., KUNZ, S., CAO, W., TISHON, A., LEWICKI, H., CAMPBELL, K. P. & OLDSTONE, M. B. (2001) Differences in affinity of binding of lymphocytic choriomeningitis virus strains to the cellular receptor alpha-dystroglycan correlate with viral tropism and disease kinetics. Journal of Virology 75, 448-457.
62. SOUDAIS, C., LAPLACE-BUILHE, C,. KISSA, K. & KREMER, E. J. (2001) Preferential transduction of neurons by canine adenovirus vectors and their efficient retrograde transport in vivo. FASEB Journal 15, 2283-2285.
63. SPEAR, P. G., SHIEH, M. T., HEROLD, B. C., WUDUNN, D. & KOSHY, T. I. (1992) Heparan sulfate glycosaminoglycans as primary cell surface receptors for herpes simplex virus. Advances in Experimental Medicine and Biology 313, 341-353.
64. STAUNTON, D. E., MERLUZZI, V. J., ROTHLEIN, R., BARTON, R., MARLIN, S. D. & SPRINGER, T. A. (1989) A cell adhesion molecule, ICAM-1, is the major surface receptor for rhinoviruses. Cell 56, 849-853.
65. TOMKO, R. P., XU, R. & PHILIPSON, L. (1997) HCAR and MCAR: The human and mouse cellular receptors for subgroup C adenoviruses and group B coxsackie viruses. Proceedings of the National Academy of Sciences USA 94, 3352-3356.
66. TOMKO, R. P., JOHANSSON, C. B., TOTROV, M., ABAGYAN, R., FRISEN, J. & PHILIPSON L. (2000) Expression of the adenovirus receptor and its interaction with the fiber knob. Experimental Cell Research 255, 47-55.
67. TOMLINSON, A. H. & ESIRI, M. M. (1983) Herpes simplex encephalitis. Immunohistological demonstration of spread of virus via olfactory pathways in mice. Journal of Neurological Science 60, 473-484.
68. VERHAAGEN, J., OESTREICHER, A. B., GRILLO, M., KHEW-GOODALL, Y. S., GISPEN, W. H. & MARGOLIS, F. L. (1990) Neuroplasticity in the olfactory system: Differential effects of central and peripheral lesions of the primary olfactory pathway on the expression of B-50/GAP43 and the olfactory marker protein. Journal of Neuroscience Research 26, 31-44.
69. WANG, K. S., KUHN, R. J., STRAUSS, E. G., OU, S. & STRAUSS, J. H. (1992) High-affinity laminin receptor is a receptor for Sindbis virus in mammalian cells. Journal of Virology 66, 4992-5001.
70. WHITE, J. M, & LITTMAN, D. R. (1989) Viral receptors of the immunoglobulin superfamily. Cell 56, 725-728.
71. WICKHAM, T. J., GRANADOS, R. R., WOOD, H. A., HAMMER, D. A. & SHULER, M. L. (1990) General analysis of receptor-mediated viral attachment to cell surfaces. Biophysical Journal 58, 1501-1516.
72. WUDUNN, D. & SPEAR, P. G. (1989) Initial interaction of herpes simplex virus with cells is binding to heparan sulfate. Journal of Virology 63, 52-58.
73. YOON, S. O., LOIS, C., ALVIREZ, M., ALVAREZ-BUYLLA, A., FALCK-PEDERSEN, E. & CHAO, M. V. (1996) Adenovirus-mediated gene delivery into neuronal precursors of the adult mouse brain. Proceedings of the National Academy of Sciences USA 93, 11974-11979.
74. YOUNGENTOB, S. L., SCHWOB, J. E., SAHA, S., MANGLAPUS, G. & JUBELT, B. (2001) Functional consequences following infection of the olfactory system by intranasal infusion of the olfactory bulb line variant (OBLV) of mouse hepatitis strain JHM. Chemical Senses 26, 953-963.
75. YOUNGENTOB, S. L., PYRSKI, M. M. & MARGOLIS, F. L. (2004) Adenoviral vector-mediated rescue of the OMP-null behavioral phenotype: Enhancement of odorant threshold sensitivity. Behavioral Neuroscience 118, 636-642.
76. XU, R., MOHANTY, J. G. & CROWELL, R. L. (1995) Receptor proteins on newborn Balb/c mouse brain cells for coxsackievirus B3 are immunologically distinct from those on HeLa cells. Virus Research 35, 323-340.
77. XU, R. & CROWELL, R. L (1996) Expression and distribution of the receptors for coxsackievirus B3 during fetal development of the Balb/c mouse and of their brain cells in culture. Virus Research 46, 157-170.
78. ZHAO, H., OTAKI, J. M. & FIRESTEIN, S. (1996) Adenovirus-mediated gene transfer in olfactory neurons in vivo. Journal of Neurobiology 30, 521-530.
79. ZHAO, H., IVIC, L., OTAKI, J. M., HASHIMOTO, M., MIKOSHIBA, K. & FIRESTEIN, S. (1998) Functional expression of a mammalian odorant receptor. Science 279, 237-242.