REVIEW
Adenovirus receptors on antigen-presenting cells of the skin
Elina Gerber-Tichet Dienst,
Eric J. Kremer,
Elina Gerber-Tichet Dienst
Institut de Génétique Moléculaire de Montpellier, Université de Montpellier, CNRS, Montpellier, France
Search for more papers by this authorCorresponding Author
Eric J. Kremer
Institut de Génétique Moléculaire de Montpellier, Université de Montpellier, CNRS, Montpellier, France
Correspondence
Eric J. Kremer, Institut de Génétique Moléculaire de Montpellier, Université de Montpellier, CNRS, 34090 Montpellier, France.
Email: [email protected]
Search for more papers by this authorElina Gerber-Tichet Dienst,
Eric J. Kremer,
Elina Gerber-Tichet Dienst
Institut de Génétique Moléculaire de Montpellier, Université de Montpellier, CNRS, Montpellier, France
Search for more papers by this authorCorresponding Author
Eric J. Kremer
Institut de Génétique Moléculaire de Montpellier, Université de Montpellier, CNRS, Montpellier, France
Correspondence
Eric J. Kremer, Institut de Génétique Moléculaire de Montpellier, Université de Montpellier, CNRS, 34090 Montpellier, France.
Email: [email protected]
Search for more papers by this authorAbstract
Skin, the largest human organ, is part of the first line of physical and immunological defense against many pathogens. Understanding how skin antigen-presenting cells (APCs) respond to viruses or virus-based vaccines is crucial to develop antiviral pharmaceutics, and efficient and safe vaccines. Here, we discuss the way resident and recruited skin APCs engage adenoviruses and the impact on innate immune responses.
CONFLICT OF INTEREST
The funders played no role in study design and analysis, the decision to publish, or preparation of the manuscript. We declare that we have no competing interests.
Open Research
DATA AVAILABILITY STATEMENT
All data are freely available and/or are included in the review.
REFERENCES
- Adams, W.C., Bond, E., Havenga, M.J.E., Holterman, L., Goudsmit, J., Hedestam, G.B.K., Koup, R.A., & Loré, K. (2009) Adenovirus serotype 5 infects human dendritic cells via a coxsackievirus-adenovirus receptor-independent receptor pathway mediated by lactoferrin and DC-SIGN. The Journal of General Virology, 90(Pt 7), 1600–1610.
- Arnberg, N., Kidd, A.H., Edlund, K., Nilsson, J., Pring-Åkerblom, P., & Wadell, G. (2002a) Adenovirus type 37 binds to cell surface sialic acid through a charge-dependent interaction. Virology, 302(1), 33–43.
- Arnberg, N., Pring-Åkerblom, P., & Wadell, G. (2002b). Adenovirus Type 37 Uses Sialic Acid as a Cellular 82 Receptor on Chang C Cells. Journal of Virology, 76(17), 8834–8841.
- Arnberg, N., Kidd, A.H., Edlund, K., Olfat, F., & Wadell, G. (2000) Initial interactions of subgenus D adenoviruses with A549 cellular receptors: sialic acid versus α v integrins. Journal of Virology, 74(16), 7691–7693.
- Baker, A.H., Nicklin, S.A., & Shayakhmetov, D.M. (2013) FX and host defense evasion tactics by adenovirus. Molecular Therapy, 21(6), 1109–1111.
- Baker, A.T., Mundy, R.M., Davies, J.A., Rizkallah, P.J., & Parker, A.L. (2019) Human adenovirus type 26 uses sialic acid-bearing glycans as a primary cell entry receptor. Science Advances, 5(9), eaax3567.
- Banchereau, J., & Steinman, R.M. (1998) Dendritic cells and the control of immunity. Nature, 392(6673), 245–252.
- Bar-On, L., Birnberg, T., Kim, K., & Jung, S. (2011) Dendritic cell-restricted CD80/86 deficiency results in peripheral regulatory T-cell reduction but is not associated with lymphocyte hyperactivation. European Journal of Immunology, 41(2), 291–298.
- 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 (New York), 275(5304), 1320–1323.
- Berlutti, F., Pantanella, F., Natalizi, T., Frioni, A., Paesano, R., Polimeni, A., & Valenti, P. (2011) Antiviral properties of lactoferrin – a natural immunity molecule. Molecules (Basel, Switzerland), 16(8), 6992–7012.
- 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 (New York), 286(5444), 1579–1583.
- Brice, D.C., & Diamond, G. (2020) Antiviral activities of human host defense peptides. Current Medicinal Chemistry, 27(9), 1420–1443.
- Burmeister, W.P., Guilligay, D., Cusack, S., Wadell, G., & Arnberg, N. (2004) Crystal structure of species D adenovirus fiber knobs and their sialic acid binding sites. Journal of Virology, 78(14), 7727–7736.
- Calabro, S., Tortoli, M., Baudner, B.C., Pacitto, A., Cortese, M., O'Hagan, D.T., De Gregorio, E., Seubert, A., & Wack, A. (2011) Vaccine adjuvants alum and MF59 induce rapid recruitment of neutrophils and monocytes that participate in antigen transport to draining lymph nodes. Vaccine, 29(9), 1812–1823.
- Cardone, J., Le Friec, G., & Kemper, C. (2011) CD46 in innate and adaptive immunity: an update. Clinical and Experimental Immunology, 164(3), 301–311.
- Caux, C., Vanbervliet, B., Massacrier, C., Azuma, M., Okumura, K., Lanier, L.L., & Banchereau, J. (1994) B70/B7-2 is identical to CD86 and is the major functional ligand for CD28 expressed on human dendritic cells. The Journal of Experimental Medicine, 180(5), 1841–1847.
- Cavallaro, U., & Dejana, E. (2011) Adhesion molecule signalling: not always a sticky business. Nature Reviews Molecular Cell Biology, 12(3), 189–197.
- Chéneau, C., Eichholz, K., Tran, T.H., Tran, T.T.P., Paris, O., Henriquet, C., Bajramovic, J.J., Pugniere, M., & Kremer, E.J. (2021) Lactoferrin retargets human adenoviruses to TLR4 to induce an abortive NLRP3-associated pyroptotic response in human phagocytes. Frontiers in Immunology, 12, 685218.
- Chéneau, C., & Kremer, E.J. (2020) Adenovirus-extracellular protein interactions and their impact on innate immune responses by human mononuclear phagocytes. Viruses, 12(12), 1351.
- Chitaev, N.A., & Troyanovsky, S.M. (1997) Direct Ca2+-dependent heterophilic interaction between desmosomal cadherins, desmoglein and desmocollin, contributes to cell-cell adhesion. The Journal of Cell Biology, 138(1), 193–201.
- Chroboczek, J., Ruigrok, R.W.H., & Cusack, S. (1995) Adenovirus fiber. Current Topics in Microbiology and Immunology, 199, 163–200.
- Collins, L.E., & Troeberg, L. (2019) Heparan sulfate as a regulator of inflammation and immunity. Journal of Leukocyte Biology, 105(1), 81–92.
- Coyne, C.B., & Bergelson, J.M. (2005) CAR: a virus receptor within the tight junction. Advanced Drug Delivery Reviews, 57(6), 869–882.
- Crespo, H.J., Guadalupe Cabral, M., Teixeira, A. V., Lau, J.T.Y., Trindade, H., & Videira, P.A. (2009) Effect of sialic acid loss on dendritic cell maturation. Immunology, 128(1), e621–e631.
- David Persson, B., John, L., Rafie, K., Strebl, M., Frängsmyr, L., Ballmann, M.Z., Mindler, K., Havenga, M., Lemckert, A., Stehle, T., Carlson, L.A., & Arnberg, N. (2021) Human species D adenovirus hexon capsid protein mediates cell entry through a direct interaction with CD46. Proceedings of the National Academy of Sciences of the United States of America, 118(3), e2020732118.
- De Witte, L., Nabatov, A., Pion, M., Fluitsma, D., De Jong, M.A.W.P., De Gruijl, T., Piguet, V., Van Kooyk, Y., & Geijtenbeek, T.B.H. (2007) Langerin is a natural barrier to HIV-1 transmission by Langerhans cells. Nature Medicine, 13(3), 367–371.
- Dechecchi, M.C., Melotti, P., Bonizzato, A., Santacatterina, M., Chilosi, M., & Cabrini, G. (2001) Heparan sulfate glycosaminoglycans are receptors sufficient to mediate the initial binding of adenovirus types 2 and 5. Journal of Virology, 75(18), 8772–8780.
- del Rio, D., Beucher, B., Lavigne, M., Wehbi, A., Gonzalez Dopeso-Reyes, I., Saggio, I., & Kremer, E.J. (2019) CAV-2 vector development and gene transfer in the central and peripheral nervous systems. Frontiers in Molecular Neuroscience, 12, 71.
- Delorme, C., Brüssow, H., Sidoti, J., Roche, N., Karlsson, K.-A., Neeser, J.-R., & Teneberg, S. (2001) Glycosphingolipid binding specificities of rotavirus: identification of a sialic acid-binding epitope. Journal of Virology, 75(5), 2276–2287.
- Doronin, K., Flatt, J.W., Di Paolo, N.C., Khare, R., Kalyuzhniy, O., Acchione, M., Sumida, J.P., Ohto, U., Shimizu, T., Akashi-Takamura, S., Miyake, K., MacDonald, J.W., Bammler, T.K., Beyer, R.P., Farin, F.M., Stewart, P.L., & Shayakhmetov, D.M. (2012) Coagulation factor X activates innate immunity to human species C adenovirus. Science (New York), 338(6108), 795–798.
- Doyle, A.D., Nazari, S.S., & Yamada, K.M. (2022) Cell-extracellular matrix dynamics. Physical Biology, 19(2), 10.
- Duffy, M.R., Alonso-Padilla, J., John, L., Chandra, N., Khan, S., Ballmann, M.Z., Lipiec, A., Heemskerk, E., Custers, J., Arnberg, N., Havenga, M., Baker, A.H., & Lemckert, A. (2018) Generation and characterization of a novel candidate gene therapy and vaccination vector based on human species D adenovirus type 56. The Journal of General Virology, 99(1), 135–147.
- Eichholz, K., Bru, T., Tran, T.T.P., Fernandes, P., Welles, H., Mennechet, F.J.D., Manel, N., Alves, P., Perreau, M., & Kremer, E.J. (2016) Immune-complexed adenovirus induce AIM2-mediated pyroptosis in human dendritic cells. PLoS Pathogens, 12(9), e1005871.
- Eichholz, K., Mennechet, F.J.D., & Kremer, E.J. (2015) Human coagulation factor X-adenovirus type 5 complexes poorly stimulate an innate immune response in human mononuclear phagocytes. Journal of Virology, 89(5), 2884–2891.
- Eichholz, K., Tran, T.H., Chéneau, C., Tran, T.T.P., Paris, O., Pugniere, M., & Kremer, E.J. (2022) Adenovirus-α-defensin complexes induce NLRP3-associated maturation of human phagocytes via Toll-like receptor 4 engagement. Journal of Virology, 96(6), e0185021.
- Elomaa, O., Kangas, M., Sahlberg, C., Tuukkanen, J., Sormunen, R., Liakka, A., Thesleff, I., Kraal, G., & Tryggvason, K. (1995) Cloning of a novel bacteria-binding receptor structurally related to scavenger receptors and expressed in a subset of macrophages. Cell, 80(4), 603–609.
- Essakalli, M., Atouf, O., Bennani, N., Benseffaj, N., Ouadghiri, S., & Brick, C. (2009) Toll-like récepteurs. Pathologie Biologie, 57(5), 430–438.
- Feng, Y., Yi, C., Liu, X., Qu, L., Su, W., Shu, T., Zheng, X., Ye, X., Luo, J., Hao, M., Sun, X., Li, L., Liu, X., Yang, C., Guan, S., Chen, L., & Feng, L. (2020) Human desmoglein-2 and human CD46 mediate human adenovirus type 55 infection, but human desmoglein-2 plays the major roles. Journal of Virology, 94(17), e00747-20.
- Feng, Z.H., Wang, Q.C., Nie, Q.H., Jia, Z.S., & Zhou, Y.X. (2004) DC-SIGN: binding receptor for HCV? World Journal of Gastroenterology, 10(7), 925–929.
- Fierro, N.A., Rivera-Toledo, E., Ávila-Horta, F., Anaya-Covarrubias, J.Y., & Mendlovic, F. (2022) Scavenger receptors in the pathogenesis of viral infections. Viral Immunology, 35(3), 175–191. Available from: https://Home-Liebertpub-Com.Insb.Bib.Cnrs.Fr/Vim
- Flatt, J.W., Kim, R., Smith, J.G., Nemerow, G.R., & Stewart, P.L. (2013) An intrinsically disordered region of the adenovirus capsid is implicated in neutralization by human alpha defensin 5. PloS ONE, 8(4), e61571.
- Fleischli, C., Sirena, D., Lesage, G., Havenga, M.J.E., Cattaneo, R., Greber, U.F., & Hemmi, S. (2007) Species B adenovirus serotypes 3, 7, 11 and 35 share similar binding sites on the membrane cofactor protein CD46 receptor. Journal of General Virology, 88(11), 2925–2934.
- Freeman, G.J., Freedman, A.S., Segil, J.M., Lee, G., Whitman, J.F., & Nadler, L.M. (1989) B7, a new member of the Ig superfamily with unique expression on activated and neoplastic B cells. The Journal of Immunology, 143(8), 2714–2722.
- Gaggar, A., Shayakhmetov, D.M., & Lieber, A. (2003) CD46 is a cellular receptor for group B adenoviruses. Nature Medicine, 9(11), 1408–1412.
- Gao, H., Gonçalves, C., Gallego, T., François-Heude, M., Malard, V., Mateo, V., Lemoine, F., Cendret, V., Djedaini-Pilard, F., Moreau, V., Pichon, C., & Midoux, P. (2020) Comparative binding and uptake of liposomes decorated with mannose oligosaccharides by cells expressing the mannose receptor or DC-SIGN. Carbohydrate Research, 487, 107877.
- Geijtenbeek, T.B.H., Kwon, D.S., Torensma, R., Van Vliet, S.J., Van Duijnhoven, G.C.F., Middel, J., Cornelissen, I.L.M.H.A., Nottet, H.S.L.M., KewalRamani, V.N., Littman, D.R., Figdor, C.G., & Van Kooyk, Y. (2000) DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells. Cell, 100(5), 587–597.
- Geijtenbeek, T.B.H., & Van Kooyk, Y. (2003) DC-SIGN: a novel HIV receptor on DCs that mediates HIV-1 transmission. Current Topics in Microbiology and Immunology, 276, 31–54.
- Ginsberg, M.H. (2014) Integrin activation. BMB Reports, 47(12), 655–659.
- Günther, P.S., Mikeler, E., Hamprecht, K., Schneider-Schaulies, J., Jahn, G., & Dennehy, K.M. (2011) CD209/DC-SIGN mediates efficient infection of monocyte-derived dendritic cells by clinical adenovirus 2C isolates in the presence of bovine lactoferrin. The Journal of General Virology, 92(Pt 8), 1754–1759.
- Hamilos, D.L. (1989) Antigen presenting cells. Immunologic Research, 8(2), 98–117.
- Harrach, B., & Benkő, M. (2021) Adenoviruses (Adenoviridae). Encyclopedia of Virology, 3–16.
10.1016/B978-0-12-814515-9.00057-6 Google Scholar
- Hemsath, J.R., Liaci, A.M., Rubin, J.D., Parrett, B.J., Lu, S.-C., Nguyen, T.V., Turner, M.A., Chen, C.Y., Cupelli, K., Reddy, V.S., Stehle, T., Liszewski, M.K., Atkinson, J.P., & Barry, M.A. (2022) Ex vivo and in vivo CD46 receptor utilization by species D human adenovirus serotype 26 (HAdV26). Journal of Virology, 96(3), e0082621.
- Hong, S.S., Karayan, L., Tournier, J., Curiel, D.T., & Boulanger, P.A. (1997) Adenovirus type 5 fiber knob binds to MHC class I alpha2 domain at the surface of human epithelial and B lymphoblastoid cells. The EMBO Journal, 16(9), 2294–2306.
- Howitt, J., Anderson, C.W., & Freimuth, P. (2003) Adenovirus interaction with its cellular receptor CAR. Current Topics in Microbiology and Immunology, 272, 331–364.
- Huang, S., Kamata, T., Takada, Y., Ruggeri, Z.M., & Nemerow, G.R. (1996) Adenovirus interaction with distinct integrins mediates separate events in cell entry and gene delivery to hematopoietic cells. Journal of Virology, 70(7), 4502–4508.
- Hung-Yueh, Y., Pieniazek, N., Pieniazek, D., Gelderblom, H., & Luftig, R.B. (1994) Human adenovirus type 41 contains two fibers. Virus Research, 33(2), 179–198.
- Iacobelli-Martinez, M., & Nemerow, G.R. (2007) Preferential activation of Toll-like receptor nine by CD46-utilizing adenoviruses. Journal of Virology, 81(3), 1305–1312.
- Isa, P., Arias, C.F., & López, S. (2006) Role of sialic acids in rotavirus infection. Glycoconjugate Journal, 23(1–2), 27–37.
- Jenssen, H., & Hancock, R.E.W. (2010) Therapeutic potential of HDPs as immunomodulatory agents. Methods in Molecular Biology (Clifton, N.J.), 618, 329–347.
- Johansson, C., Jonsson, M., Marttila, M., Persson, D., Fan, X.-L., Skog, J., Frängsmyr, L., Wadell, G., & Arnberg, N. (2007) Adenoviruses use lactoferrin as a bridge for CAR-independent binding to and infection of epithelial cells. Journal of Virology, 81(2), 954–963.
- Kalyuzhniy, O., Di Paolo, N.C., Silvestry, M., Hofherr, S.E., Barry, M.A., Stewart, P.L., & Shayakhmetov, D.M. (2008) Adenovirus serotype 5 hexon is critical for virus infection of hepatocytes in vivo. Proceedings of the National Academy of Sciences of the United States of America, 105(14), 5483–5488.
- Kissick, H.T., Dunn, L.K., Ghosh, S., Nechama, M., Kobzik, L., & Arredouani, M.S. (2014) The scavenger receptor MARCO modulates TLR-induced responses in dendritic cells. PLoS ONEe, 9(8), e104148. Available from: http://doi.org/10.1371/JOURNAL.PONE.0104148
- Kodaira, Y., Nair, S.K., Wrenshall, L.E., Gilboa, E., & Platt, J.L. (2000) Phenotypic and functional maturation of dendritic cells mediated by heparan sulfate. Journal of Immunology (Baltimore, Md. : 1950), 165(3), 1599–1604.
- Kremer, E.J., & Nemerow, G.R. (2015) Adenovirus tales: from the cell surface to the nuclear pore complex. PLoS Pathogens, 11(6), e1004821.
- Lanier, L.L., O'Fallon, S., Somoza, C., Phillips, J.H., Linsley, P.S., Okumura, K., Ito, D., & Azuma, M. (1995) CD80 (B7) and CD86 (B70) provide similar costimulatory signals for T cell proliferation, cytokine production, and generation of CTL. The Journal of Immunology, 154(1), 97–105.
- Lasswitz, L., Chandra, N., Arnberg, N., & Gerold, G. (2018) Glycomics and proteomics approaches to investigate early adenovirus–host cell interactions. Journal of Molecular Biology, 430(13), 1863–1882.
- Lee, S.K. (2007) Pattern-recognition receptor signaling initiated from extracellular, membrane, and cytoplasmic space. Molecules and Cells, 23(1), 1–10.
- Lemckert, A.A.C., Grimbergen, J., Smits, S., Hartkoorn, E., Holterman, L., Berkhout, B., Barouch, D.H., Vogels, R., Quax, P., Goudsmit, J., & Havenga, M.J.E. (2006) Generation of a novel replication-incompetent adenoviral vector derived from human adenovirus type 49: manufacture on PER.C6 cells, tropism and immunogenicity. The Journal of General Virology, 87(Pt 10), 2891–2899.
- Lenman, A., Liaci, A.M., Liu, Y., Årdahl, C., Rajan, A., Nilsson, E., Bradford, W., Kaeshammer, L., Jones, M.S., Frängsmyr, L., Feizi, T., Stehle, T., & Arnberg, N. (2015) Human adenovirus 52 uses sialic acid-containing glycoproteins and the coxsackie and adenovirus receptor for binding to target cells. PLoS Pathogens, 11(2), e1004657.
- Lenman, A., Manuel Liaci, A., Liu, Y., Frängsmyr, L., Frank, M., Blaum, B.S., Chai, W., Podgorski, I.I., Harrach, B., Benko, M., Feizi, T., Stehle, T., & Arnberg, N. (2018) Polysialic acid is a cellular receptor for human adenovirus 52. Proceedings of the National Academy of Sciences of the United States of America, 115(18), E4264–E42736.
- 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(11), 5405–5409.
- Li, Y., Hickey, L., Perrins, R., Werlen, E., Patel, A.A., Hirschberg, S., Jones, M.W., Salinas, S., Kremer, E.J., & Pickering, A.E. (2016) Retrograde optogenetic characterization of the pontospinal module of the locus coeruleus with a canine adenoviral vector. Brain Research, 1641, 274–290.
- Lion, T. (2014) Adenovirus infections in immunocompetent and immunocompromised patients. Clinical Microbiology Reviews, 27(3), 441–462.
- Lisewski, U., Shi, Y., Wrackmeyer, U., Fischer, R., Chen, C., Schirdewan, A., Jüttner, R., Rathjen, F., Poller, W., Radke, M.H., & Gotthardt, M. (2008) The tight junction protein CAR regulates cardiac conduction and cell-cell communication. The Journal of Experimental Medicine, 205(10), 2369–2379.
- Liszewski, M.K., Farries, T.C., Lublin, D.M., Rooney, I.A., & Atkinson, J.P. (1996) Control of the complement system. Advances in Immunology, 61, 201–283.
- Louis, N., Fender, P., Barge, A., Kitts, P., Chroboczek, J. (1994) Cell-binding domain of adenovirus serotype 2 fiber. Journal of Virology, 68(6), 4104–4106.
- Loustalot, F., Kremer, E.J., & Salinas, S. (2016) Membrane dynamics and signaling of the coxsackievirus and adenovirus receptor. International Review of Cell and Molecular Biology, 322, 331–362.
- Lozach, P.Y., Kühbacher, A., Meier, R., Mancini, R., Bitto, D., Bouloy, M., & Helenius, A. (2011) DC-SIGN as a receptor for phleboviruses. Cell Host & Microbe, 10(1), 75–88.
- Lyle, C., & McCormick, F. (2010) Integrin αvβ5 is a primary receptor for adenovirus in CAR-negative cells. Virology Journal, 7, 148.
- Macleod, D.T., Nakatsuji, T., Wang, Z., Di Nardo, A., & Gallo, R.L. (2015) Vaccinia virus binds to the scavenger receptor MARCO on the surface of keratinocytes. The Journal of Investigative Dermatology, 135(1), 142–150.
- MacLeod, D.T., Nakatsuji, T., Yamasaki, K., Kobzik, L., & Gallo, R.L. (2013) HSV-1 exploits the innate immune scavenger receptor MARCO to enhance epithelial adsorption and infection. Nature Communications, 4, 1963.
- Maler, M.D., Nielsen, P.J., Stichling, N., Cohen, I., Ruzsics, Z., Wood, C., Engelhard, P., Suomalainen, M., Gyory, I., Huber, M., Müller-Quernheim, J., Schamel, W.W.A., Gordon, S., Jakob, T., Martin, S.F., Jahnen-Dechent, W., Greber, U.F., Freudenberg, M.A., & Fejer, G. (2017) Key role of the scavenger receptor MARCO in mediating adenovirus infection and subsequent innate responses of macrophages. mBio, 8(4), e00670-17.
- Marchetti, M., Trybala, E., Superti, F., Johansson, M., & Bergström, T. (2004) Inhibition of herpes simplex virus infection by lactoferrin is dependent on interference with the virus binding to glycosaminoglycans. Virology, 318(1), 405–413.
- Marttila, M., Persson, D., Gustafsson, D., Liszewski, M.K., Atkinson, J.P., Wadell, G., & Arnberg, N. (2005) CD46 is a cellular receptor for all species B adenoviruses except types 3 and 7. Journal of Virology, 79(22), 14429–14436.
- Mathias, P., Galleno, M., & Nemerow, G.R. (1998) Interactions of soluble recombinant integrin αvβ5 with human adenoviruses. Journal of Virology, 72(11), 8669–8675.
- Matsushita, N., Komine, H., Grolleau-Julius, A., Pilon-Thomas, S., & Mulé, J.J. (2010) Targeting MARCO can lead to enhanced dendritic cell motility and anti-melanoma activity. Cancer Immunology, Immunotherapy : CII, 59(6), 875–884.
- Maurer, K., Krey, T., Moennig, V., Thiel, H.-J., & Rümenapf, T. (2004) CD46 is a cellular receptor for bovine viral diarrhea virus. Journal of Virology, 78(4), 1792–1799.
- Mennechet, F.J.D., Paris, O., Ouoba, A.R., Salazar Arenas, S., Sirima, S.B., Takoudjou Dzomo, G.R., Diarra, A., Traore, I.T., Kania, D., Eichholz, K., Weaver, E.A., Tuaillon, E., & Kremer, E.J. (2019) A review of 65 years of human adenovirus seroprevalence. Expert Review of Vaccines, 18(6), 597–613.
- Moretta, A., Scieuzo, C., Maria Petrone, A., Salvia, R., Dario Manniello, M., Franco, A., Lucchetti, D., Vassallo, A., Vogel, H., Sgambato, A., Falabella, P., Rabanal, F., Bhattacharjya, S., & Balleste, C. (2021) Antimicrobial peptides: a new hope in biomedical and pharmaceutical fields. Frontiers in Cellular and Infection Microbiology, 11, 668632.
- Louis, N., Fender, P., Barge, A., Kitts, P., & Chroboczek, J. (1994) Cell-binding domain of adenovirus serotype 2 fiber. Journal of Virology, 68(6), 4104–4106.
- Nakamura, T., Sato, K., & Hamada, H. (2003) Reduction of natural adenovirus tropism to the liver by both ablation of fiber-coxsackievirus and adenovirus receptor interaction and use of replaceable short fiber. Journal of Virology, 77(4), 2512–2521.
- Nemerow, G.R., & Stewart, P.L. (1999) Role of alpha(v) integrins in adenovirus cell entry and gene delivery. Microbiology and Molecular Biology Reviews, 63(3), 725–734.
- Nestić, D., Uil, T.G., Ma, J., Roy, S., Vellinga, J., Baker, A.H., Custers, J., & Majhen, D. (2018) αvβ3 Integrin is required for efficient infection of epithelial cells with human adenovirus type 26. Journal of Virology, 93(1), e01474-18.
- Ng, W.C., Londrigan, S.L., Nasr, N., Cunningham, A.L., Turville, S., Brooks, A.G., & Reading, P.C. (2015) The C-type lectin langerin functions as a receptor for attachment and infectious entry of influenza A virus. Journal of Virology, 90(1), 206–221.
- Nguyen, E.K., Nemerow, G.R., & Smith, J.G. (2010) Direct evidence from single-cell analysis that human {alpha}-defensins block adenovirus uncoating to neutralize infection. Journal of Virology, 84(8), 4041–4049.
- Nicol, C.G., Graham, D., Miller, W.H., White, S.J., Smith, T.A., Nicklin, S.A., Stevenson, S.C., & Baker, A.H. (2004) Effect of adenovirus serotype 5 fiber and penton modifications on in vivo tropism in rats. Molecular Therapy, 10(2), 344–354.
- Perreau, M., & Kremer, E.J. (2005) Frequency, proliferation, and activation of human memory T cells induced by a nonhuman adenovirus. Journal of Virology, 79(23), 14595–14605.
- Philipson, L., Lonberg-Holm, K., & Pettersson, U. (1968) Virus-receptor interaction in an adenovirus system. Journal of Virology, 2(10), 1064–1075.
- Rahimi, N. (2020) C-type Lectin CD209L/L-SIGN and CD209/DC-SIGN: cell adhesion molecules turned to pathogen recognition receptors. Biology, 10(1), 1–15.
- Rajan, A., Palm, E., Trulsson, F., Mundigl, S., Becker, M., Persson, B.D., Frängsmyr, L., & Lenman, A. (2021) Heparan sulfate is a cellular receptor for enteric human adenoviruses. Viruses, 13(2), 298.
- Rajan, A., Persson, B.D., Frängsmyr, L., Olofsson, A., Sandblad, L., Heino, J., Takada, Y., Mould, A.P., Schnapp, L.M., Gall, J., & Arnberg, N. (2018) Enteric species F human adenoviruses use laminin-binding integrins as co-receptors for infection of Ht-29 cells. Scientific Reports, 8(1), 1–14.
- Roelvink, P.W., Lizonova, A., Lee, J.G.M., 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(10), 7909–7915.
- Rowe, W.P., Huebner, R.J., Gilmore, L.K., Parrott, R.H., & Ward, T.G. (1953) Isolation of a cytopathogenic agent from human adenoids undergoing spontaneous degeneration in tissue culture. Proceedings of the Society for Experimental Biology and Medicine, 84(3), 570–573.
- Saikh, K.U. (2021) MyD88 and beyond: a perspective on MyD88-targeted therapeutic approach for modulation of host immunity. Immunologic Research, 69(2), 117–128.
- Salone, B., Martina, Y., Piersanti, S., Cundari, E., Cherubini, G., Franqueville, L., Failla, C.M., Boulanger, P., & Saggio, I. (2003) Integrin α3β1 is an alternative cellular receptor for adenovirus serotype 5. Journal of Virology, 77(24), 13448.
- Santoro, F., Kennedy, P.E., Locatelli, G., Malnati, M.S., Berger, E.A., & Lusso, P. (1999) CD46 is a cellular receptor for human herpesvirus 6. Cell, 99(7), 817–827.
- Schoehn, G., El Bakkouri, M., Fabry, C.M.S., Billet, O., Estrozi, L.F., Le, L., Curiel, D.T., Kajava, A.V., Ruigrok, R.W.H., & Kremer, E.J. (2008) Three-dimensional structure of canine adenovirus serotype 2 capsid. Journal of Virology, 82(7), 3192–3203.
- Schwegmann-Weßels, C., & Herrler, G. (2006) Sialic acids as receptor determinants for coronaviruses. Glycoconjugate Journal, 23(1–2), 51–58.
- Segerman, A., Atkinson, J.P., Marttila, M., Dennerquist, V., Wadell, G., & Arnberg, N. (2003) Adenovirus type 11 uses CD46 as a cellular receptor. Journal of Virology, 77(17), 9183–9191.
- Seiradake, E., Henaff, D., Wodrich, H., Billet, O., Perreau, M., Hippert, C., Mennechet, F., Schoehn, G., Lortat-Jacob, H., Dreja, H., Ibanes, S., Kalatzis, V., Wang, J.P., Finberg, R.W., Cusack, S., & Kremer, E.J. (2009) The cell adhesion molecule “CAR” and sialic acid on human erythrocytes influence adenovirus in vivo biodistribution. PLoS Pathogens, 5(1), e1000277.
- Short, J.J., Pereboev, A.V., Kawakami, Y., Vasu, C., Holterman, M.J., & Curiel, D.T. (2004) Adenovirus serotype 3 utilizes CD80 (B7.1) and CD86 (B7.2) as cellular attachment receptors. Virology, 322(2), 349–359.
- Short, J.J., Vasu, C., Holterman, M.J., Curiel, D.T., & Pereboev, A. (2006) Members of adenovirus species B utilize CD80 and CD86 as cellular attachment receptors. Virus Research, 122(1–2), 144–153.
- Simmons, G., Reeves, J.D., Grogan, C.C., Vandenberghe, L.H., Baribaud, F., Whitbeck, J.C., Burke, E., Buchmeier, M.J., Soilleux, E.J., Riley, J.L., Doms, R.W., Bates, P., & Pöhlmann, S. (2003) DC-SIGN and DC-SIGNR bind ebola glycoproteins and enhance infection of macrophages and endothelial cells. Virology, 305(1), 115–123.
- Sirena, D., Lilienfeld, B., Eisenhut, M., Kälin, S., Boucke, K., Beerli, R.R., Vogt, L., Ruedl, C., Bachmann, M.F., Greber, U.F., & Hemmi, S. (2004) The human membrane cofactor CD46 is a receptor for species B adenovirus serotype 3. Journal of Virology, 78(9), 4454–4462.
- Smith, J.G., & Nemerow, G.R. (2008) Mechanism of adenovirus neutralization by human alpha-defensins. Cell Host & Microbe, 3(1), 11–19.
- Smith, T.A., Idamakanti, N., Rollence, M.L., Marshall-Neff, J., Kim, J., Mulgrew, K., Nemerow, G.R., Kaleko, M., & Stevenson, S.C. (2003) Adenovirus serotype 5 fiber shaft influences in vivo gene transfer in mice. Human Gene Therapy, 14(8), 777–787.
- Soudais, C., Boutin, S., Hong, S.S., Chillon, M., Danos, O., Bergelson, J.M., Boulanger, P., & Kremer, E.J. (2000) Canine adenovirus type 2 attachment and internalization: coxsackievirus-adenovirus receptor, alternative receptors, and an RGD-independent pathway. Journal of Virology, 74(22), 10639–10649.
- Soudais, C., Skander, N., & Kremer, E.J. (2004) Long-term in vivo transduction of neurons throughout the rat CNS using novel helper-dependent CAV-2 vectors. FASEB Journal, 18(2), 1–20.
- Sprangers, M.C., Lakhai, W., Koudstaal, W., Verhoeven, M., Koel, B.F., Vogels, R., Goudsmit, J., Havenga, M.J.E., & Kostense, S. (2003) Quantifying adenovirus-neutralizing antibodies by luciferase transgene detection: addressing preexisting immunity to vaccine and gene therapy vectors. Journal of Clinical Microbiology, 41(11), 5046–5052.
- Springer, G.F., Schwick, H.G., & Fletcher, M.A. (1969) The relationship of the influenza virus inhibitory activity of glycoproteins to their molecular size and sialic acid content. Proceedings of the National Academy of Sciences of the United States of America, 64(2), 634–641.
- Stichling, N., Suomalainen, M., Flatt, J.W., Schmid, M., Pacesa, M., Hemmi, S., Jungraithmayr, W., Maler, M.D., Freudenberg, M.A., Plückthun, A., May, T., Köster, M., Fejer, G., & Greber, U.F. (2018) Lung macrophage scavenger receptor SR-A6 (MARCO) is an adenovirus type-specific virus entry receptor. PLoS Pathogens, 14(3), e1006914.
- Storm, R.J., Persson, B.D., Skalman, L.N., Frängsmyr, L., Lindström, M., Rankin, G., Lundmark, R., Domellöf, F.P., & Arnberg, N. (2017) Human adenovirus type 37 uses α V β 1 and α 3 β 1 integrins for infection of human corneal cells. Journal of Virology, 91(5), e02019-16.
- Summerford, C., Bartlett, J.S., & Samulski, R.J. (1999) αVβ5 integrin: a co-receptor for adeno-associated virus type 2 infection. Nature Medicine 5(1), 78–82.
- Swart, P.J., Kuipers, M.E., Smit, C., Pauwels, R., De Béthune, M.P., De Clercq, E., Meijer, D.K.F., & Huisman, J.G. (1996) Antiviral effects of milk proteins: acylation results in polyanionic compounds with potent activity against human immunodeficiency virus types 1 and 2 in vitro. AIDS Research and Human Retroviruses, 12(9), 769–775.
- Takeuchi, O., & Akira, S. (2010) Pattern recognition receptors and inflammation. Cell, 140(6), 805–820.
- Tassaneetrithep, B., Burgess, T.H., Granelli-Piperno, A., Trumpfheller, C., Finke, J., Sun, W., Eller, M.A., Pattanapanyasat, K., Sarasombath, S., Birx, D.L., Steinman, R.M., Schlesinger, S., & Marovich, M.A. (2003) DC-SIGN (CD209) mediates dengue virus infection of human dendritic cells. The Journal of Experimental Medicine, 197(7), 823–829.
- Thu, T., Tran, P., Eichholz, K., Amelio, P., Moyer, C., Nemerow, G.R., Perreau, M., Mennechet, F.J.D., & Kremer, E.J. (2018) Humoral immune response to adenovirus induce tolerogenic bystander dendritic cells that promote generation of regulatory T cells. PLoS Pathogens, 14(8), e1007127.
- Tran, T.T.P., Eichholz, K., Amelio, P., Moyer, C., Nemerow, G.R., Perreau, M., Mennechet, F.J.D., & Kremer, E.J. (2018) Humoral immune response to adenovirus induce tolerogenic bystander dendritic cells that promote generation of regulatory T cells. PLoS Pathogens, 14(8), 1–31.
- Tran, T.T.P., Tran, T.H., & Kremer, E.J. (2021) IgG-complexed adenoviruses induce human plasmacytoid dendritic cell activation and apoptosis. Viruses, 13(9), 1699.
- Trinh, H.V., Lesage, G., Chennamparampil, V., Vollenweider, B., Burckhardt, C.J., Schauer, S., Havenga, M., Greber, U.F., & Hemmi, S. (2012) Avidity binding of human adenovirus serotypes 3 and 7 to the membrane cofactor CD46 triggers infection. Journal of Virology, 86(3), 1623–1637.
- Tsoukas, R.L., Volkwein, W., Gao, J., Schiwon, M., Bahlmann, N., Dittmar, T., Hagedorn, C., Ehrke-Schulz, E., Zhang, W., Baiker, A., & Ehrhardt, A. (2022) A human in vitro model to study adenoviral receptors and virus cell interactions. Cells, 11(5), 841.
- Tuve, S., Wang, H., Jacobs, J.D., Yumul, R.C., Smith, D.F., & Lieber, A. (2008) Role of cellular heparan sulfate proteoglycans in infection of human adenovirus serotype 3 and 35. PLoS Pathogens, 4(10), e1000189.
- Tuve, S., Wang, H., Ware, C., Liu, Y., Gaggar, A., Bernt, K., Shayakhmetov, D., Li, Z., Strauss, R., Stone, D., & Lieber, A. (2006) A new group B adenovirus receptor is expressed at high levels on human stem and tumor cells. Journal of Virology, 80(24), 12109–12120.
- van der Aar, A.M.G., Sylva-Steenland, R.M.R., Bos, J.D., Kapsenberg, M.L., de Jong, E.C., & Teunissen, M.B.M. (2007) Cutting edge: loss of TLR2, TLR4, and TLR5 on langerhans cells abolishes bacterial recognition. The Journal of Immunology, 178(4), 1986–1990.
- Van der Strate, B.W.A., Beljaars, L., Molema, G., Harmsen, M.C., & Meijer, D.K.F. (2001) Antiviral activities of lactoferrin. Antiviral Research, 52(3), 225–239.
- Waddington, S.N., McVey, J.H., Bhella, D., Parker, A.L., Barker, K., Atoda, H., Pink, R., Buckley, S.M.K., Greig, J.A., Denby, L., Custers, J., Morita, T., Francischetti, I.M.B., Monteiro, R.Q., Barouch, D.H., van Rooijen, N., Napoli, C., Havenga, M.J.E., Nicklin, S.A., & Baker, A.H. (2008) Adenovirus serotype 5 hexon mediates liver gene transfer. Cell, 132(3), 397–409.
- Walters, R.W., Freimuth, P., Moninger, T.O., Ganske, I., Zabner, J., & Welsh, M.J. (2002) Adenovirus fiber disrupts CAR-mediated intercellular adhesion allowing virus escape. Cell, 110(6), 789–799.
- Wang, H., Li, Z.Y., Liu, Y., Persson, J., Beyer, I., Möller, T., Koyuncu, D., Drescher, M.R., Strauss, R., Zhang, X.B., Wahl, J.K., Urban, N., Drescher, C., Hemminki, A., Fender, P., & Lieber, A. (2011) Desmoglein 2 is a receptor for adenovirus serotypes 3, 7, 11 and 14. Nature Medicine, 17(1), 96–104.
- Wang, H., Liaw, Y.-C., Stone, D., Kalyuzhniy, O., Amiraslanov, I., Tuve, S., Verlinde, C.L.M.J., Shayakhmetov, D., Stehle, T., Roffler, S., & Lieber, A. (2007) Identification of CD46 binding sites within the adenovirus serotype 35 fiber knob. Journal of Virology, 81(23), 12785–12792.
- Wang, H., Yumul, R., Cao, H., Ran, L., Fan, X., Richter, M., Epstein, F., Gralow, J., Zubieta, C., Fender, P., & Lieber, A. (2013) Structural and functional studies on the interaction of adenovirus fiber knobs and desmoglein 2. Journal of Virology, 87, 11346–11362.
- Weaver, E.A., & Barry, M.A. (2013) Low seroprevalent species D adenovirus vectors as influenza vaccines. PLoS One, 8(8), e73313.
- Wickham, T.J., Mathias, P., Cheresh, D.A., & Nemerow, G.R. (1993) Integrins alpha v beta 3 and alpha v beta 5 promote adenovirus internalization but not virus attachment. Cell, 73(2), 309–319.
- Wu, E., Trauger, S.A., Pache, L., Mullen, T.-M., Von Seggern, D.J., Siuzdak, G., & Nemerow, G.R. (2004) Membrane cofactor protein is a receptor for adenoviruses associated with epidemic keratoconjunctivitis. Journal of Virology, 78(8), 3897–3905.
- Zaiss, A.K., Foley, E.M., Lawrence, R., Schneider, L.S., Hoveida, H., Secrest, P., Catapang, A.B., Yamaguchi, Y., Alemany, R., Shayakhmetov, D.M., Esko, J.D., & Herschman, H.R. (2015) Hepatocyte heparan sulfate is required for adeno-associated virus 2 but dispensable for adenovirus 5 liver transduction in vivo. Journal of Virology, 90(1), 412–420.
- Zhang, J., Ma, K., Wang, X., Jiang, Y., Zhao, S., Ou, J., Lan, W., Guan, W., Wu, X., Zheng, H., Yang, B., Wan, C., Zhao, W., Wu, J., & Zhang, Q. (2021) Desmoglein 2 (DSG2) is a receptor of human adenovirus type 55 causing adult severe community-acquired pneumonia. Virologica Sinica, 36(6), 1400–1410.
- Zheng, Y., Manzotti, C.N., Liu, M., Burke, F., Mead, K.I., & Sansom, D.M. (2004) CD86 and CD80 differentially modulate the suppressive function of human regulatory T cells. Journal of Immunology (Baltimore, Md. : 1950), 172(5), 2778–2784.
- Zhu, F.C., Guan, X.H., Li, Y.H., Huang, J.Y., Jiang, T., Hou, L.H., Li, J.X., Yang, B.F., Wang, L., Wang, W.J., Wu, S.P., Wang, Z., Wu, X.H., Xu, J.J., Zhang, Z., Jia, S.Y., Wang, B.S, Hu, Y., Liu, J.J., & Chen, W. (2020) Immunogenicity and safety of a recombinant adenovirus type-5-vectored COVID-19 vaccine in healthy adults aged 18 years or older: a randomised, double-blind, placebo-controlled, phase 2 trial. The Lancet (London, England), 396(10249), 479–488.
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