Abstract
The receptors on human cells which mediate adsorption of adenoviruses have not been identified. We found that murine A9 cells and Chinese hamster ovary (CHO) cells failed to bind significant levels of radiolabeled adenovirus type 2 (Ad2) virions but that derivatives of these cells carrying human chromosome 21 exhibited high levels of virus binding that was specific for the viral fiber protein. G418-resistant A9 cell transformants expressing Ad2 receptors were detected at a frequency of about 10(-4) following cotransfection with high-molecular-weight DNAs from mouse cells containing human chromosome 21 and plasmid DNA containing a neomycin resistance gene. The Ad2 receptors on the transformed A9 cells were similar to those on human cells with respect to their concentration on the cell membrane, their affinity for the viral fiber protein, and their ability to direct virus into cells along a pathway leading to delivery of the viral DNA genome into the cell nucleus. Furthermore, identical human DNA fragments were present in three independent mouse cell transformants expressing Ad2 receptors, supporting the conclusion that these human DNA fragments correspond to a gene or locus on chromosome 21 that directs the expression of Ad2 receptors in these cells.
Full Text
The Full Text of this article is available as a PDF (282.2 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Bai M., Campisi L., Freimuth P. Vitronectin receptor antibodies inhibit infection of HeLa and A549 cells by adenovirus type 12 but not by adenovirus type 2. J Virol. 1994 Sep;68(9):5925–5932. doi: 10.1128/jvi.68.9.5925-5932.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bai M., Harfe B., Freimuth P. Mutations that alter an Arg-Gly-Asp (RGD) sequence in the adenovirus type 2 penton base protein abolish its cell-rounding activity and delay virus reproduction in flat cells. J Virol. 1993 Sep;67(9):5198–5205. doi: 10.1128/jvi.67.9.5198-5205.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Belin M. T., Boulanger P. Involvement of cellular adhesion sequences in the attachment of adenovirus to the HeLa cell surface. J Gen Virol. 1993 Aug;74(Pt 8):1485–1497. doi: 10.1099/0022-1317-74-8-1485. [DOI] [PubMed] [Google Scholar]
- Boulanger P. A., Puvion F. Large-scale preparation of soluble adenovirus hexon, penton and fiber antigens in highly purified form. Eur J Biochem. 1973 Nov 1;39(1):37–42. doi: 10.1111/j.1432-1033.1973.tb03100.x. [DOI] [PubMed] [Google Scholar]
- Cuthbert A. P., Trott D. A., Ekong R. M., Jezzard S., England N. L., Themis M., Todd C. M., Newbold R. F. Construction and characterization of a highly stable human: rodent monochromosomal hybrid panel for genetic complementation and genome mapping studies. Cytogenet Cell Genet. 1995;71(1):68–76. doi: 10.1159/000134066. [DOI] [PubMed] [Google Scholar]
- Defer C., Belin M. T., Caillet-Boudin M. L., Boulanger P. Human adenovirus-host cell interactions: comparative study with members of subgroups B and C. J Virol. 1990 Aug;64(8):3661–3673. doi: 10.1128/jvi.64.8.3661-3673.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Di Guilmi A. M., Barge A., Kitts P., Gout E., Chroboczek J. Human adenovirus serotype 3 (Ad3) and the Ad3 fiber protein bind to a 130-kDa membrane protein on HeLa cells. Virus Res. 1995 Sep;38(1):71–81. doi: 10.1016/0168-1702(95)00043-p. [DOI] [PubMed] [Google Scholar]
- Duncan S. J., Gordon F. C., Gregory D. W., McPhie J. L., Postlethwaite R., White R., Willcox H. N. Infection of mouse liver by human adenovirus type 5. J Gen Virol. 1978 Jul;40(1):45–61. doi: 10.1099/0022-1317-40-1-45. [DOI] [PubMed] [Google Scholar]
- Eggerding F. A., Pierce W. C. Molecular biology of adenovirus type 2 semipermissive infections. I. Viral growth and expression of viral replicative functions during restricted adenovirus infection. Virology. 1986 Jan 15;148(1):97–113. doi: 10.1016/0042-6822(86)90406-x. [DOI] [PubMed] [Google Scholar]
- Freimuth P. A human cell line selected for resistance to adenovirus infection has reduced levels of the virus receptor. J Virol. 1996 Jun;70(6):4081–4085. doi: 10.1128/jvi.70.6.4081-4085.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ginsberg H. S., Moldawer L. L., Sehgal P. B., Redington M., Kilian P. L., Chanock R. M., Prince G. A. A mouse model for investigating the molecular pathogenesis of adenovirus pneumonia. Proc Natl Acad Sci U S A. 1991 Mar 1;88(5):1651–1655. doi: 10.1073/pnas.88.5.1651. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Goding J. W. The chromic chloride method of coupling antigens to erythrocytes: definition of some important parameters. J Immunol Methods. 1976;10(1):61–66. doi: 10.1016/0022-1759(76)90007-7. [DOI] [PubMed] [Google Scholar]
- Goyette M. C., Cho K., Fasching C. L., Levy D. B., Kinzler K. W., Paraskeva C., Vogelstein B., Stanbridge E. J. Progression of colorectal cancer is associated with multiple tumor suppressor gene defects but inhibition of tumorigenicity is accomplished by correction of any single defect via chromosome transfer. Mol Cell Biol. 1992 Mar;12(3):1387–1395. doi: 10.1128/mcb.12.3.1387. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hennache B., Boulanger P. Biochemical study of KB-cell receptor for adenovirus. Biochem J. 1977 Aug 15;166(2):237–247. doi: 10.1042/bj1660237. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Henry L. J., Xia D., Wilke M. E., Deisenhofer J., Gerard R. D. Characterization of the knob domain of the adenovirus type 5 fiber protein expressed in Escherichia coli. J Virol. 1994 Aug;68(8):5239–5246. doi: 10.1128/jvi.68.8.5239-5246.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hirt B. Selective extraction of polyoma DNA from infected mouse cell cultures. J Mol Biol. 1967 Jun 14;26(2):365–369. doi: 10.1016/0022-2836(67)90307-5. [DOI] [PubMed] [Google Scholar]
- Hong S. S., Boulanger P. Protein ligands of the human adenovirus type 2 outer capsid identified by biopanning of a phage-displayed peptide library on separate domains of wild-type and mutant penton capsomers. EMBO J. 1995 Oct 2;14(19):4714–4727. doi: 10.1002/j.1460-2075.1995.tb00153.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jeffreys A. J., Flavell R. A. A physical map of the DNA regions flanking the rabbit beta-globin gene. Cell. 1977 Oct;12(2):429–439. doi: 10.1016/0092-8674(77)90119-2. [DOI] [PubMed] [Google Scholar]
- Jelinek W. R., Schmid C. W. Repetitive sequences in eukaryotic DNA and their expression. Annu Rev Biochem. 1982;51:813–844. doi: 10.1146/annurev.bi.51.070182.004121. [DOI] [PubMed] [Google Scholar]
- Jelinek W. R., Toomey T. P., Leinwand L., Duncan C. H., Biro P. A., Choudary P. V., Weissman S. M., Rubin C. M., Houck C. M., Deininger P. L. Ubiquitous, interspersed repeated sequences in mammalian genomes. Proc Natl Acad Sci U S A. 1980 Mar;77(3):1398–1402. doi: 10.1073/pnas.77.3.1398. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Koi M., Shimizu M., Morita H., Yamada H., Oshimura M. Construction of mouse A9 clones containing a single human chromosome tagged with neomycin-resistance gene via microcell fusion. Jpn J Cancer Res. 1989 May;80(5):413–418. doi: 10.1111/j.1349-7006.1989.tb02329.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Levine A. J., Ginsberg H. S. Mechanism by which fiber antigen inhibits multiplication of type 5 adenovirus. J Virol. 1967 Aug;1(4):747–757. doi: 10.1128/jvi.1.4.747-757.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Littman D. R., Thomas Y., Maddon P. J., Chess L., Axel R. The isolation and sequence of the gene encoding T8: a molecule defining functional classes of T lymphocytes. Cell. 1985 Feb;40(2):237–246. doi: 10.1016/0092-8674(85)90138-2. [DOI] [PubMed] [Google Scholar]
- Lonberg-Holm K., Crowell R. L., Philipson L. Unrelated animal viruses share receptors. Nature. 1976 Feb 26;259(5545):679–681. doi: 10.1038/259679a0. [DOI] [PubMed] [Google Scholar]
- Longiaru M., Horwitz M. S. Chinese hamster ovary cells replicate adenovirus deoxyribonucleic acid. Mol Cell Biol. 1981 Mar;1(3):208–215. doi: 10.1128/mcb.1.3.208. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Louis N., Fender P., Barge A., Kitts P., Chroboczek J. Cell-binding domain of adenovirus serotype 2 fiber. J Virol. 1994 Jun;68(6):4104–4106. doi: 10.1128/jvi.68.6.4104-4106.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mathias P., Wickham T., Moore M., Nemerow G. Multiple adenovirus serotypes use alpha v integrins for infection. J Virol. 1994 Oct;68(10):6811–6814. doi: 10.1128/jvi.68.10.6811-6814.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mendelsohn C. L., Wimmer E., Racaniello V. R. Cellular receptor for poliovirus: molecular cloning, nucleotide sequence, and expression of a new member of the immunoglobulin superfamily. Cell. 1989 Mar 10;56(5):855–865. doi: 10.1016/0092-8674(89)90690-9. [DOI] [PubMed] [Google Scholar]
- Mendelsohn C., Johnson B., Lionetti K. A., Nobis P., Wimmer E., Racaniello V. R. Transformation of a human poliovirus receptor gene into mouse cells. Proc Natl Acad Sci U S A. 1986 Oct;83(20):7845–7849. doi: 10.1073/pnas.83.20.7845. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Moore E. E., Jones C., Kao F. T., Oates D. C. Synteny between glycinamide ribonucleotide synthetase and superoxide dismutase (soluble). Am J Hum Genet. 1977 Jul;29(4):389–396. [PMC free article] [PubMed] [Google Scholar]
- Ning Y., Weber J. L., Killary A. M., Ledbetter D. H., Smith J. R., Pereira-Smith O. M. Genetic analysis of indefinite division in human cells: evidence for a cell senescence-related gene(s) on human chromosome 4. Proc Natl Acad Sci U S A. 1991 Jul 1;88(13):5635–5639. doi: 10.1073/pnas.88.13.5635. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Persson R., Wohlfart C., Svensson U., Everitt E. Virus-receptor interaction in the adenovirus system: characterization of the positive cooperative binding of virions on HeLa cells. J Virol. 1985 Apr;54(1):92–97. doi: 10.1128/jvi.54.1.92-97.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Philipson L., Lonberg-Holm K., Pettersson U. Virus-receptor interaction in an adenovirus system. J Virol. 1968 Oct;2(10):1064–1075. doi: 10.1128/jvi.2.10.1064-1075.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Seth P., Rosenfeld M., Higginbotham J., Crystal R. G. Mechanism of enhancement of DNA expression consequent to cointernalization of a replication-deficient adenovirus and unmodified plasmid DNA. J Virol. 1994 Feb;68(2):933–940. doi: 10.1128/jvi.68.2.933-940.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Stevenson S. C., Rollence M., White B., Weaver L., McClelland A. Human adenovirus serotypes 3 and 5 bind to two different cellular receptors via the fiber head domain. J Virol. 1995 May;69(5):2850–2857. doi: 10.1128/jvi.69.5.2850-2857.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Svensson U., Persson R., Everitt E. Virus-receptor interaction in the adenovirus system I. Identification of virion attachment proteins of the HeLa cell plasma membrane. J Virol. 1981 Apr;38(1):70–81. doi: 10.1128/jvi.38.1.70-81.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Uzé G., Lutfalla G., Gresser I. Genetic transfer of a functional human interferon alpha receptor into mouse cells: cloning and expression of its cDNA. Cell. 1990 Jan 26;60(2):225–234. doi: 10.1016/0092-8674(90)90738-z. [DOI] [PubMed] [Google Scholar]
- Wickham T. J., Mathias P., Cheresh D. A., Nemerow G. R. Integrins alpha v beta 3 and alpha v beta 5 promote adenovirus internalization but not virus attachment. Cell. 1993 Apr 23;73(2):309–319. doi: 10.1016/0092-8674(93)90231-e. [DOI] [PubMed] [Google Scholar]
- Wigler M., Pellicer A., Silverstein S., Axel R. Biochemical transfer of single-copy eucaryotic genes using total cellular DNA as donor. Cell. 1978 Jul;14(3):725–731. doi: 10.1016/0092-8674(78)90254-4. [DOI] [PubMed] [Google Scholar]
- Xia D., Henry L. J., Gerard R. D., Deisenhofer J. Crystal structure of the receptor-binding domain of adenovirus type 5 fiber protein at 1.7 A resolution. Structure. 1994 Dec 15;2(12):1259–1270. doi: 10.1016/s0969-2126(94)00126-x. [DOI] [PubMed] [Google Scholar]
- Yang Y., Li Q., Ertl H. C., Wilson J. M. Cellular and humoral immune responses to viral antigens create barriers to lung-directed gene therapy with recombinant adenoviruses. J Virol. 1995 Apr;69(4):2004–2015. doi: 10.1128/jvi.69.4.2004-2015.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yang Y., Nunes F. A., Berencsi K., Furth E. E., Gönczöl E., Wilson J. M. Cellular immunity to viral antigens limits E1-deleted adenoviruses for gene therapy. Proc Natl Acad Sci U S A. 1994 May 10;91(10):4407–4411. doi: 10.1073/pnas.91.10.4407. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Young J. A., Bates P., Varmus H. E. Isolation of a chicken gene that confers susceptibility to infection by subgroup A avian leukosis and sarcoma viruses. J Virol. 1993 Apr;67(4):1811–1816. doi: 10.1128/jvi.67.4.1811-1816.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Younghusband H. B., Tyndall C., Bellett A. J. Replication and interaction of virus DNA and cellular DNA in mouse cells infected by a human adenovirus. J Gen Virol. 1979 Nov;45(2):455–467. doi: 10.1099/0022-1317-45-2-455. [DOI] [PubMed] [Google Scholar]