Abstract
Sialic acid-containing compounds play a key role in the initial steps of the paramyxovirus life cycle. As enveloped viruses, their entry into the host cell consists of two main events: binding to the host cell and membrane fusion. Virus adsorption occurs at the surface of the host cell with the recognition of specific receptor molecules located at the cell membrane by specific viral attachment proteins. The viral attachment protein present in some paramyxoviruses (Respirovirus, Rubulavirus and Avulavirus) is the HN glycoprotein, which binds to cellular sialic acid-containing molecules and exhibits sialidase and fusion promotion activities. Gangliosides of the gangliotetraose series bearing the sialic acid N-acetylneuraminic (Neu5Ac) on the terminal galactose attached in α2-3 linkage, such as GD1a, GT1b, and GQ1b, and neolacto-series gangliosides are the major receptors for Sendai virus. Much less is known about the receptors for other paramyxoviruses than for Sendai virus. Human parainfluenza viruses 1 and 3 preferentially recognize oligosaccharides containing N-acetyllactosaminoglycan branches with terminal Neu5Acα2-3Gal. In the case of Newcastle disease virus, has been reported the absence of a specific pattern of the gangliosides that interact with the virus. Additionally, several works have described the use of sialylated glycoproteins as paramyxovirus receptors. Accordingly, the design of specific sialic acid analogs to inhibit the sialidase and/or receptor binding activity of viral attachment proteins is an important antiviral strategy. In spite of all these data, the exact nature of paramyxovirus receptors, apart from their sialylated nature, and the mechanism(s) of viral attachment to the cell surface are poorly understood.
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Abbreviations
- DANA:
-
Neu5Ac2en 2,3-dehydro-2-deoxy-N-acetyl neuraminic acid
- FANA:
-
deoxy-2,3-dehydro-N-trifluoroacetylneuraminic acid
- 4-GU-DANA:
-
2,3-didehydro-2,4-dideoxy-4-guanidino-N-acetylneuraminic acid
- SV5:
-
simian virus 5
- hPIV1, 2 or 3:
-
human parainfluenza virus 1, 2 or 3
- NDV:
-
Newcastle Disease Virus
- Neu5Ac:
-
N-acetylneuraminic acid
- Neu5Gc:
-
N-glycolylneuraminic acid
- α-Neu5thioAc2Sme:
-
α-2-S-methyl-5-N-thioacetylneuraminic acid
- RSV:
-
Respiratory Syncitial Virus
References
Svennerholm, L.: Chromatographic separation of human brain gangliosides. J. Neurochem. 10, 613–623 (1963)
Ghazal, P., Gonzalez Armas J.C., Garcia-Ramirez, J.J., Kurz, S., Angulo, A.: Viruses: hostages to the cell. Virology 275, 233–237 (2000)
Holland, J., Domingo, E.: Origin and evolution of viruses. Virus Genes 16, 13–21 (1998)
Baranowski, E., Ruiz-Jarabo, C.M., Pariente, N., Verdaguer, N., Domingo, E.: Evolution of cell recognition by viruses: A source of biological novelty with medical implications. In: K. Maramorosch, F.A. Murphy, J. Shatkin (Eds.) Adv. Virus Res., Elsevier Academic Press London, vol. 62, pp. 19–111 (2003)
Domingo, E.: Host-microbe interactions: Viruses. Complexities of virus-cell interactions. Curr. Op. Microbiol. 6, 383–385 (2003)
Haywood, A.M.: Virus receptors: Binding, adhesion strengthening, and changes in viral structure. J. Virol. 68, 1–5 (1994)
Lamb, R.A., Kolakofsky, D.: Paramyxoviridae: The viruses and their replication. In: D.M. Knippe, P.M. Howley, 4th edition, Fields virology, Lippincot-Williams & Wilkins, New York, 2001, pp. 1305–1340
Lamb, RA.: Paramyxovirus fusion: A hypothesis for changes. Virology 197, 1–11 (1993)
Hadac, E.M., Peng, K.W., Nakamura, T., Russell, S.J.: Reengineering paramyxovirus tropism. Virology 329, 217–225 (2004)
San Roman, K.J., Villar, E., Muñoz Barroso, M.I.: Acidic pH enhancement of the fusion of Newcastle disease virus with cultured cells. Virology 260, 329–341 (1999)
Nakamura, K., Homma, M., Compans, R.W.: Effect of tunicamycin on the replication of Sendai virus. Virology 119, 474–487 (1982)
Morrison, T.G.: Structure, function and intracellular processing of paramyxovirus membrane proteins. Virus Res. 10, 113–136 (1988)
Morrison, T.G., Portner, A.: Structure, function and intracellular processing of the glycoproteins in Paramyxoviridae. In: D.W. Kingsbury (Ed.) The paramyxoviruses, Plenum Press. New York, 1991, pp. 347–382
Yoshida, T., Takao, S., Kiyotani, K., Sakaguchi, T.: Endoproteolytic activation of Newcastle disease virus fusion proteins requires an intracellular acidic environment. Virology 170, 571–574 (1989)
Ng, D.T., Hiebert, S.W., Lamb, R.A.: Different roles of the individual N-linked oligosaccharide chains in folding, assembly and transport of simian virus 5 hemagglutinin-neuraminidase. Moll. Cell Biol. 10, 1989–2001 (1990)
Hu, A., Cattaneo, R., Schwartz, S., Norrby, E.: Role of N-linked oligosaccharide chains in the processing and antigenicity of measles virus hemagglutinin protein. J. Gen. Virol. 75, 1043–1052 (1994)
Markwell, M.A., Fox, C.F.: Protein-protein interactions within paramyxoviruses identified by native disulfide bonding or reversible chemical cross-linking. J. Virol. 33, 152–166 (1980)
McGuinnes, L., Sergel, T., Morrison, T.: Mutations in the transmembrane domain of the HN protein of Newcastle disease virus affect the structure and activity of the protein. Virology 196, 101–110 (1993)
Garcia-Sastre, A., Cabezas, J.A., Villar, E.: Proteins of Newcastle disease virus envelope: Interaction between the outer hemagglutinin-neuraminidase glycoprotein and the inner non-glycosylated matrix protein. Biochim. Biophys. Acta. 999, 171–175 (1989)
Schmitt, A.P., Lamb, R.A.: Escaping from the Cell: Assembly and budding of negative- strand RNA viruses. Curr. Top. Microbiol. Immunol. 283, 145–196 (2004)
Klenk, H.D., Choppin, P.W.: Glycosphingolipids of plasma membranes of cultured cells and an enveloped virus (SV5) grown in this cells. Proc. Natl. Acad. Sci. USA 66, 57–64 (1970)
Klenk, H.D., Compans, R.W., Choppin, P.W., An electron microscopic study of the presence or absence of neuraminic acid in enveloped viruses. Virology 42, 1158–1162 (1970)
Porotto, M., Murrell, M., Greenhard, O., Doctor, L., Moscona, A.: Influence of the human Parainfluenza virus 3 attachment protein's neuraminidase activity on its capacity to activate the fusion protein. J. Virol. 79, 2383–2392 (2005)
Muñoz-Barroso, I., Cobaleda, C., Zhadan, G., Shnyrov, V., Villar, E.: Dynamic properties of Newcastle Disease Virus envelope and their relations with viral hemagglutinin-neuraminidase membrane glycoprotein. Biochim. Biophys. Acta. 1327, 17–31 (1997)
Morrison, T., McQuain, C., McGinnes, L.: Complementation between avirulent Newcastle disease virus and a fusion protein gene expressed from a retrovirus vector: Requirements for membrane fusion. J. Virol. 65, 813–822 (1991)
Sergel, T., McGuinnnes, L.W., Peeples, M.E., Morrison, T.G.: The attachment function of Newcastle disease virus hemagglutinin-neuraminidase protein can be separated from fusion promotion by mutation. Virology 193, 717–726 (1993)
Sergel, T., McGuinnes, L.W., Morrison, T.G.: The fusion promotion activity of the NDV HN protein does not correlate with neuraminidase activity. Virology 196, 831–834 (1993)
Moscona, A., Peluso, R.W.: Fusion properties of cells persistently infected with human parainfluenza virus type 3: Participation of hemagglutinin-neuraminidase in membrane fusion. J. Virol. 65, 2773–2777 (1991)
Wild. T.F., Malvoisin, E., Buckland, R.: Measles virus: Both the hemagglutinin-neuraminidase and fusion glycoproteins are required for fusion. J. Gen. Virol. 72, 439–442 (1991)
Hu. X.L., Ray, R.: Compans RW Functional interactions between the fusion protein and hemagglutinin-neuraminidase of human parainfluenza viruses. J. Virol. 66, 1528–1534 (1992)
Heminway, B.R., Yu, Y., Galinski, M.S.: Paramyxovirus mediated cell fusion requires co-expression of both the fusion and hemagglutinin-neuraminidase glycoproteins. Virus Re. 31, 1–16 (1994)
Ferreira, L., Muñoz-Barroso, I., Marcos, F., Shnyrov, V.L., Villar, E.: Sialidase, receptor-binding and fusion-promotion activities of Newcastle disease virus hemagglutinin-neuraminidase glycoprotein: A mutational and kinetic study, J Gen Virol 85, 1981–1988 (2004)
Miura, N., Uchida, T., Okada, Y.: HVJ (Sendai virus)-induced envelope fusion and cell fusion are blocked by monoclonal anti-HN protein antibody that does not inhibit hemagglutinin activity of HVJ, Exp Cell Res 141, 409–420 (1982)
Tsurudome, M., Yamada, A., Hishiyama, M., Ito, Y.: Monoclonal antibodies against the glycoproteins of mumps virus: Fusion inhibition by anti-HN monoclonal antibody. J. Gen. Virol. 67, 2259–2265 (1986)
Iorio, R.M., Glickman, R.L., Sheehan, J.P.: Inhibition of fusion by neutralizing monoclonal antibodies to the haemagglutinin-neuraminidase glycoprotein of Newcastle disease virus. J. Gen. Virol. 73, 1167–1176 (1992)
Schuy, W., Garten, W., Linder, D., Klenk, H.D.: The carboxyterminus of the hemagglutinin-neuraminidase of Newcastle disease virus is exposed at the surface of the viral envelope. Virus Res. 1, 415–426 (1984)
Colman, P.M., Hoyne, P.A., Lawrence, M.C.: Sequence and structure alignment of paramyxovirus hemagglutinin-neuraminidase and influenza virus neuraminidase. J. Virol. 67, 2972–2980 (1993)
Gaskell, A., Crennell, S.J., Taylor, G.: The three domains of a bacterial sialidase: a beta-propeller, an immunoglobulin module and a galactose-binding jelly-roll. Structure 3, 1197–1205 (1995)
Langedijk, J.P.M., Daus, F.J., van, Oirschot J.T.: Sequence and structure alignment of Paramyxoviridae attachment proteins and discovery of enzymatic activity for a morbillivirus hemagglutinin. J. Virol. 71, 6155–6167 (1997)
Crennell, S.J., Garman, E.F., Laver, W.G., Vimr, E.R., Taylor, G.L.: Crystal structure of a bacterial sialidase (from Salmonella typhimurium LT2) shows the same fold as an influenza virus neuraminidase. Proc. Natl. Acad. Sci. USA 90, 9852–9856 (1993)
Crennell, S.J., Garman, E.F., Laver, W.G., Vimr, E.R., Taylor, G.L.: Crystal structure of Vibrio cholerae neuraminidase reveals dual lectin-like domains in addition to the catalytic domain. Structure 2, 535–544 (1994)
Crennell, S.J., Takimoto, T., Portner, A., Taylor, G.: Crystal structure of the multifunctional paramyxovirus hemagglutinin-neuraminidase. Nature Structr. Biol. 7, 1068–1074 (2000)
Sagrera, A., Cobaleda, C., González de Buitrago, J.M., García-Sastre, A., Villar, E.: Membrane glycoproteins of Newcastle disease virus: nucleotide sequence of the hemagglutinin-neuraminidase cloned gene and structure/function relationships of predicted aminoacid sequence. Glycoconj. J. 18, 283–289 (2001)
Sagrera, A., Cobaleda, C., Muñoz-Barroso, I., Shnyrov, V., Villar, E.: Modulation of the neuraminidase activity of the HN protein from Newcastle disease virus by substrate binding and conformational change: Kinetic and thermal denaturation studies. Biochem. Mol. Biol. Int. 37, 717–727 (1995)
Scheid, A., Caliguiri, L.A., Compans, R.W., Choppin, P.W.: Isolation of paramyxovirus glyproteins. Association of both hemagglutinating and neuraminidase activities with the larger SV5 glycoprotein. Virology 50, 640–652 (1972)
Portner, A.: The HN glycoprotein of Sendai virus: Analysis of site(s) involved in hemagglutinating and neuraminidase activities. Virology 115, 375–384 (1981)
Iorio, R.M., Bratt, M.A.: Monoclonal antibodies as functional probes of the HN glycoprotein of Newcastle disease virus: Antigenic separation of the hemagglutinin and neuraminidase sites. J. Immunol. 133, 2215–2219 (1983)
Ray, R., Compans, P.W.: Monoclonal antibodies reveal extensive antigenic differences between the hemagglutinin-neuraminidase glycoproteins of human and bovine parainfluenza 3 viruses. Virology 148, 232–236 (1986)
Gorman, W.L., Gill, D.S., Scroggs, R.A., Portner, A.: The hemagglutinin-neuraminidase glycoproteins of human parainfluenza virus type 1 and Sendai virus have high structure-function similarity with limited antigenic cross-reactivity. Virology 175, 211–221 (1990)
Garcia-Sastre, A., Cobaleda, C., Cabezas, J.A., Villar, E.: On the inhibition mechanism of the sialidase activity of Newcastle disease virus. Biol. Chem. Hoppe-Seyler 372, 923–927 (1991)
Mirza, A.M., Deng, R., Iorio, R.M.: Site-directed mutagenesis of a conserved hexapeptide in the paramyxovirus hemagglutinin-neuraminidase glycoprotein: Effects on antigenic structure and function. J. Virol. 68, 5093–5099 (1994)
Stone-Hulslander, J., Morrison, T.G.: Mutational analysis of heptad-repeats in the membrane proximal region of Newcastle disease virus HN protein. J. Virol. 73, 3630–3637 (1999)
Iorio, R.M., Field, G.M., Sauvron, J.M., Mirza, A.M., Deng, R., Mahon, P.J., Langedijk, J.P.: Structural and functional relationship between the receptor recognition and neuraminidase activities of the Newcastle disease virus hemagglutinin-neuraminidase protein: Receptor recognition is dependent on neuraminidase activity. J. Virol. 75, 1918–1927 (2001)
Zaitsev, V., von Itzstein, M., Groves, D., Kiefel, M., Takimoto, T., Portner, A., Taylor, G.: Second sialic acid binding site in Newcastle disease virus hemagglutinin-neuraminidase: implications for fusion. J. Virol. 78, 3733–3741 (2004)
Li, J., Quinlan, E., Mirza, A., Iorio, R.M.: Mutated form of the Newcastle disease virus hemagglutinin-neuraminidase interacts with the homologous fusion protein despite deficiencies in both receptor recognition and fusion promotion. J. Virol. 78, 5299–5310 (2004)
Ferreira, L., Villar, E., Muñoz-Barroso, I.: Gangliosides and N-glycoproteins function as Newcastle disease virus receptors. Int. J. Biochem. Cell Biol. 36, 2344–2356 (2004)
Porotto, M., Murrell, M., Greengard, O., Lawrence, M.C., McKimm-Breschkin, J.L., Moscona, A.: Inhibition of parainfluenza virus type 3 and Newcastle disease virus hemagglutinin-neuraminidase receptor binding: effect of receptor avidity and steric hindrance at the inhibitor binding sites. J. Virol. 78, 13911–13919 (2004)
Bousse, T., Takimoto, T., Gorman, W.L., Takahashi, T., Portner, A.: Regions on the hemagglutinin-neuraminidase proteins of human parainfluenza virus type-1 and Sendai virus important for membrane fusion. Virology 204, 506–514 (1994)
Deng, R., Wang, Z., Glickman, R.L., Iorio, R.M.: Glycosylation within an antigenic site on the HN glycoprotein of Newcastle disease virus interferes with its role in the promotion of membrane fusion. Virology 209, 457–469 (1994)
Tanabayashi, K., Compans, R.W.: Functional interaction of paramyxovirus glycoproteins: identification of a domain in Sendai virus HN which promotes cell fusion. J. Virol. 70, 6112–6118 (1996)
Buchholz, C.J., Schneider, U., Devaux, P., Gerlier, D., Cattaneo, R.: Cell entry by measles virus: long hybrid receptors uncouple binding from membrane fusion. J. Virol. 70, 3716–3723 (1996)
Porotto, M., Murrell, M., Greengard, O., Moscona, A.: Triggering of human parainfluenza virus 3 fusion protein (F) by the hemagglutinin-neuraminidase (HN) protein: An HN mutation diminishes the rate of F activation and fusion. J. Virol. 77, 3647–3654
Tsurudome, M., Kawano, M., Yuasa, T., Tabata, N., Nishio, M., Komada. H., Ito, Y.: Identification of regions on the hemagglutinin-neuraminidase protein of human parainfluenza virus type 2 important for promoting cell fusion. Virology 213, 190–203 (1995)
Corey, E.A., Mirza, A.M., Levandowsky, E., Iorio, R.M.: Fusion deficiency induced by mutations at the dimer interface in the Newcastle disease virus hemagglutinin-neuraminidase is due to a temperature-dependent defect in receptor binding. J. Virol. 77, 6913–6922 (2003)
Stern, L.B.L., Greenberg, M., Gershoni, J.M., Rozenblatt, S.: The hemagglutinin envelope protein of canine distemper virus (CDV) confers cell tropism as illustrated by CDV and measles virus complementation analysis. J. Virol. 69, 1661–1668 (1995)
Griffin, D.E.: Measles virus. In Fields Virology, 4th edition, edited by Knippe DM, Howley PM (Lippincot-Williams & Wilkins, New York, 2001), pp. 1401–1441
Blain, F., Liston, P., Briedis, D.J.: The carboxy-terminal 18 amino acids of measles virus hemagglutinin are essential for its biological function. Biochem. Biophys. Res. Commun. 214, 1232–1238 (1995)
Levine, S., Klaiber-Franco, R., Paradiso, P.R.: Demonstration that glycoprotein G is the attachment protein of respiratory syncytial virus. J. Gen. Virol. 68, 2521–2524 (1987)
Karron, R.A., Bounagurio, D.A., Georgiu, A.F., Whitehead, S.S., Adamus, J.E., Clements-Mann, M.L., Harris, D.O., Randolph, V.B., Udem, S.A., Murphy, B.R., Sidhu, M.S.: Respiratory syncytial virus (RSV) SH and G proteins are not essential for viral replication in vitro: Clinical evaluation and molecular characterization of a cold-passaged, attenuated RSV subgroup B mutant. Proc. Natl. Acad. Sci. USA 94, 13961–13966 (1997)
Collins, P.L., Chanok, R.M., Murphy, B.R.: Respiratory syncytial virus. In Fields Virology, 4th edition, edited by Knippe DM, Howley PM (Lippincot-Williams & Wilkins, New York, 2001), pp. 1443–1485
Wertz, G.W., Krieger, M., Ball, L.A.: Structure an cell surface maturation of the attachment glycoprotein of human respiratory syncytial virus in a cell line deficient on O glycosylation. J. Virol. 63, 4767–4776 (1989)
Garcia-Beato, R., Martinez, I., Franci, C., Real, F.X.: Garcia-Barreno B, Melero JA, Host cell effect upon glycosylation and antigenicity of human respiratory syncytial virus G glycoprotein. Virology 221, 301–309 (1996)
Garcia-Beato, R., Melero, J.A.: The C-terminal third of human respiratory syncytial virus attachment (G) protein is partially resistant to protease digestion and is glycosylated in a cell-type-specific manner. J. Gen. Virol. 81, 919–927 (2000)
Collins, P.L.: O glycosylation of glycoprotein G of human respiratory syncytial virus is specified within the divergent ectodomain. J. Virol. 64, 4007–4012 (1990)
Lanjedijk, J.P., de Groot, B.L., Berendsen, H.J.: van Oirschot, Structural homology of the central conserved region of the attachment protein G of respiratory syncytial virus with the fourth subdomain of 55-kDa tumour necrosis factor receptor. Virology 243, 293–302 (1998)
Hallak, L.K., Collins, P.L., Knudson, W., Peeples, M.E.: Iduronic acid-containing glycosaminoglycans on target cells are required for efficient respiratory syncytial virus infection. Virology 271, 264–275 (2000)
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)
Markwell, MAK.: New frontiers opened by the exploration of host cell receptors. In: D.W. Kingsbury (Ed.) The paramyxoviruses, (Plenum Press, New York, 1991), pp. 407–425 (1991)
Herrler, G., Hausmann, J.: Klenk, H-D, Sialic acid as receptor determinant of Ortho- and Paramyxoviruses. In: A. Rosenberg (Ed.) Biology of the Sialic Acid, (Plenum Press, New York, 1995), pp. 315–336.
Suzuki, T., Harada, M., Suzuki, Y., Matsumoto, M.: Incorporation of sialoglycoprotein containing lacto-series oligosaccharides into chicken asialoerythrocyte membranes and restoration of receptor activity toward hemagglutinating virus of Japan (Sendai virus). J. Biochem. (Tokyo) 95, 1193–1200 (1984)
Wybenga, L.E., Epand, R.F., Nir, S., Chu, J.W., Sharom, F.J., Flanagan, T.D., Epand, R.M.: Glycophorin as a receptor for Sendai virus. Biochemistry 35, 9513–9518 (1996)
Markwell, M.A., Svennerholm, L., Paulson, J.C.: Specific gangliosides function as host cell receptors for Sendai virus. Proc. Natl. Acad. Sci. USA 78, 5406–5410 (1981)
Markwell, M.A., Moss, J., Hom, B.E., Fishman, P.H., Svennerholm, L.: Expression of gangliosides as receptors at the cell surface controls infection of NCTC 2071 cells by Sendai virus. Virology 155, 356–364 (1986)
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)
Umeda, M., Nojima, S., Inoue, K.: Activity of human erythrocyte gangliosides as a receptor to HVJ. Virology 133, 172–182 (1984)
Suzuki, Y., Suzuki, T., Matsunaga, M., Matsumoto, M.: Gangliosides as paramyxovirus receptor. Structural requirement of sialo-oligosaccharides in receptors for hemagglutinating virus of Japan (Sendai virus) and Newcastle disease virus. J. Biochem. (Tokyo) 97, 1189–1199 (1985)
Suzuki, T., Portner, A., Scroggs, R.A., Uchikawa, M., Koyama, N., Matsuo, K., Suzuki, Y., Takimoto, T.: Receptor specificities of human respiroviruses. J. Virol. 75, 4604–4613 (2001)
Hansson, G.C., Karlsson, K.A., Larson, G., Stromberg, N., Thurin, J., Orvell, C., Norrby, E.: A novel approach to the study of glycolipid receptors for viruses. Binding of Sendai virus to thin-layer chromatograms. FEBS Lett. 170, 15–18 (1984)
Muthing, J., Unland, F.: A comparative assessment of TLC overlay technique and microwell adsorption assay in the examination of influenza A and Sendai virus specificities towards oligosaccharides and sialic acid linkages of gangliosides. Glycoconj. J. 11, 486–492 (1994)
Schnaar, R.L.: Glycosphingolipids in cell surface recognition. Glycobiology 1, 477–485 (1991)
Oku, N., Nojima, S., Inoue, K.: Studies on the interaction of Sendai virus with liposomal membranes. Sendai virus-induced agglutination of liposomes containing glycophorin. Biochim. Biophys. Acta. 646, 36–42 (1981)
Oku, N., Inoue, K., Nojima, S., Sekiya, T., Nozawa, Y.: Electron microscopic study on the interaction of Sendai virus with liposomes containing glycophorin, Biochim Biophys Acta 691, 91–96 (1982)
Suzuki, Y., Suzuki, T., Matsumoto, M.: Isolation and characterization of receptor sialoglycoprotein for hemagglutinating virus of Japan (Sendai virus) from bovine erythrocyte membrane, J Biochem (Tokyo) 93, 1621–1633 (1983)
Leyrer, S., Bitzer, M., Lauer, U., Kramer, J., Neubert, W.J., Sedlmeier, R.: Sendai virus-like particles devoid of haemagglutinin-neuraminidase protein infect cells via the human asialoglycoprotein receptor. J. Gen. Virol. 79, 683–687 (1998)
Mahrkwell, M.A., Portner, A., Schwartz, A.L.: An alternative route of infection for viruses: Entry by means of the asialoglycoprotein receptor of a Sendai virus mutant lacking its attachment protein. Proc. Natl. Acad. Sci. USA 82, 978–982 (1985)
Cobaleda, C., Muñoz-Barroso, I., Sagrera, A., Villar, E.: Fusogenic activity of reconstituted Newcastle disease virus envelopes: a role for the hemagglutinin-neuraminidase protein in the fusion process. Int. J. Biochem. Cell Biol. 34, 403–413 (2002)
Dutch. RE., Joshi, S.B., Lamb, R.A.: Membrane fusion promoted by increasing surface densities of the paramyxovirus F and HN proteins: comparison of fusion reactions mediated by simian virus 5 F, human parainfluenza virus type 3 F, and influenza virus HA. J. Virol. 72, 7745–7753 (1998)
Barretto, N., Hallak, L.K., Peeples, M.E.: Neuraminidase treatment of respiratory syncytial virus-infected cells or virions, but not target cells, enhances cell-cell fusion and infection. Virology 313, 33–43 (2003)
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)
Ohki, S., Arnold, K., Srinivasakumar, N., Flanagan, T.D.: Effect of anionic polymers on fusion of Sendai virus with human erythrocyte ghosts. Antiviral. Res. 18, 163–177 (1992)
Zschornig, O., Arnold, K., Ohki, S.: Effect of glycosaminoglycans and PEG on fusion of Sendai virus with phosphatidylserine vesicles. Biochim. Biophys. Acta. 1148, 1–6 (1993)
Bose, S., Banerjee, A.K.: Role of heparan sulfate in human parainfluenza virus type 3 infection. Virology 298, 73–83 (2002)
Sergel, T.A., McGinnes, L.W., Morrison, T.G.: A single amino acid change in the Newcastle disease virus fusion protein alters the requirement for HN protein in fusion. J. Virol. 74, 5101–5107 (2000)
Li, J., Melanson, V.R., Mirza, A.M., Iorio, R.M.: Decreased dependence on receptor recognition for the fusion promotion activity of L289A-mutated Newcastle disease virus fusion protein correlates with a monoclonal antibody-detected conformational change. J. Virol. 79, 1180–1190 (2005)
Eckhardt, M., Gotza, B., Gerardy-Schahn, R.: Mutants of the CMP-sialic acid transporter causing the Lec2 phenotype. J. Biol. Chem. 273, 20189–20195 (1998)
Guerrero, C.A., Zarate, S., Corkidi, G., Lopez, S., Arias, C.F.: Biochemical characterization of rotavirus receptors in MA104 cells, J. Virol. 74, 9362–9371 (2000)
Arnberg, N., Kidd, A.H., Edlund, K., Olfat, F., Wadell, G.: Initial interactions of subgenus D adenoviruses with A549 cellular receptors: sialic acid versus alpha(v) integrins. J. Virol. 74, 7691–7693 (2000)
Suzuki, Y., Ito, T., Suzuki, T., Holland, RE Jr., Chambers, T.M., Kiso, M., Ishida, H., Kawaoka, Y.: Sialic acid species as a determinant of the host range of influenza A viruses. J. Virol. 74, 11825–11831 (2000)
Kaludov, N., Brown, K.E., Walters, R.W., Zabner, J., Chiorini, J.A.: Adeno-associated virus serotype 4 (AAV4) and AAV5 both require sialic acid binding for hemagglutination and efficient transduction but differ in sialic acid linkage specificity. J. Virol. 75, 6884–6893 (2001)
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)
Alexander, D.A., Dimock, K.: Sialic acid functions in enterovirus 70 binding and infection. J. Virol. 76, 11265–11272 (2002)
Puri, A., Hug, P., Munoz-Barroso, I., Blumenthal, R.: Human erythrocyte glycolipids promote HIV-1 envelope glycoprotein-mediated fusion of CD4+ cells. Biochem. Biophys. Res. Commun. 242, 219–225 (1998)
Hug, P., Lin, H.M., Korte, T., Xiao, X., Dimitrov, D.S., Wang, J.M., Puri, A., Blumenthal, R.: Glycosphingolipids promote entry of a broad range of human immunodeficiency virus type 1 isolates into cell lines expressing CD4, CXCR4, and/or CCR5. J. Virol. 74, 6377–6385 (2000)
Krusat, T., Streckert, H.J.: Heparin–dependent attachment of respiratory syncytial virus (RSV) to host cells. Arch. Virol. 142, 1247–1254 (1997)
Dorig, R.E., Marcil, A., Chopra, A., Richardson, C.D.: The human CD46 molecule is a receptor for measles virus (Edmonston strain). Cell 75, 295–305 (1993)
Naniche, D., Varior-Krishnan, G., Cervoni, F., Wild, T.F., Rossi, B., Rabourdin-Combe, C., Gerlier, D.: Human membrane cofactor protein (CD46) acts as a cellular receptor for measles virus. J. Virol. 67, 6025–6032 (1993)
Tatsuo, H., OkamaK, Tanaka, K., Yanagi, Y.: SLAM (CDw 150) is a cellular receptor for measles virus. Nature 406, 893–897 (2000)
Yanagi, Y., Ono, N., Tatsuo, H., Hashimoto, K., Minagawa, H.: Measles virus receptor SLAM (CD150). Virology 299, 155–161 (2002)
Tatsuo, H., Ono, N., Yanagi, Y.: Morbilliviruses use signaling lymphocyte activation molecules (CD150) as cellular receptors. J. Virol. 75, 5842–5850 (2001)
Eaton, B.T.: Introduction to Current focus on Hendra and Nipah viruses, Microbes. Infect. 3, 277–278 (2001)
Bossart, K.N., Wang, L.F., Eaton, B.T., Broder, C.C.: Functional expression and membrane fusion tropism of the envelope glycoproteins of Hendra virus. Virology 290, 121–135 (2001)
Morrison, T.G.: Structure and function of a paramyxovirus fusion protein. Biochim. Biophys. Acta. 1614, 73–84 (2003)
Ferreira, L., Villar, E., Muñoz-Barroso, I.: Conformational changes of Newcastle disease virus envelope glycoproteins triggered by gangliosides. Eur. J. Biochem. 271, 581–588 (2004)
Meindl, P., Bodo, G., Palese, P., Schulman, J., Tuppy, H.: Inhibition of neuraminidase activity by derivatives of 2-deoxy-2,3-dehydro-N-acetylneuraminic acid. Virology 58, 457–463 (1974)
Palese, P., Schulman, J.L., Bodo, G., Meindl, P.: Inhibition of influenza and parainfluenza virus replication in tissue culture by 2-deoxy-2,3-dehydro-N-trifluoroacetylneuraminic acid (FANA). Virology 59, 490–498 (1974)
Palese, P., Compans, R.W.: Inhibition of influenza virus replication in tissue culture by 2-deoxy-2,3-dehydro-N-trifluoroacetylneuraminic acid (FANA): mechanism of action. J. Gen. Virol. 33, 159–163 (1976)
Hayden, F.G., Osterhaus, A.D., Treanor, J.J., Fleming, D.M., Aoki, F.Y., Nicholson, K.G., Bohnen, A.M., Hirst, H.M., Keene, O., Wightman, K.: Efficacy and safety of the neuraminidase inhibitor zanamivir in the treatment of influenza virus infections. GG167 Influenza Study Group. N. Engl. J. Med. 337, 874–880 (1997)
Monto, A.S.: Fleming DM, Henry D, de Groot R, Makela M, Klein T, Elliott M, Keene ON, Man CY, Efficacy and safety of the neuraminidase inhibitor zanamivirin the treatment of influenza A and B virus infections. J. Infect. Dis. 180, 254–261 (1999)
Levin, P.S., Jordan, M., Brossmer, R., Greengard, O., Moscona, A.: The use of a quantitative fusion assay to evaluate HN-receptor interaction for human parainfluenza virus type 3. Virology 265, 57–65 (1999)
Greengard, O., Poltoratskaia, N., Leikina, E., Zimmerberg, J., Moscona, A.: The anti-influenza virus agent 4-GU-DANA (zanamivir) inhibits cell fusion mediated by human parainfluenza virus and influenza virus HA. J. Virol. 74, 11108–11114 (2000)
Murrell, M., Porotto, M., Weber, T., Greengard, O., Moscona, A.: Mutations in human parainfluenza virus type 3 hemagglutinin-neuraminidase causing increased receptor binding activity and resistance to the transition state sialic acid analog 4-GU-DANA (Zanamivir). J. Virol. 77, 309–317 (2003)
Bose, S., Banerjee, A.K.: Role of heparan sulfate in human parainfluenza virus type 3 infection. Virology 298, 73–83 (2002)
Alymova, I.V., Taylor, G., Takimoto, T., Lin, T.H., Chand, P., Babu, Y.S., Li, C., Xiong, X., Portner, A.: Efficacy of novel hemagglutinin-neuraminidase inhibitors BCX 2798 and BCX 2855 against human parainfluenza viruses in vitro and in vivo. Antimicrob. Agents Chemother. 48, 1495–1502 (2004)
Suzuki, T., Ikeda, K., Koyama, N., Hosokawa, C., Kogure, T., Takahashi, T., Jwa Hidari, K.I., Miyamoto, D., Tanaka, K., Suzuki, Y.: Inhibition of human parainfluenza virus type 1 sialidase by analogs of 2-deoxy-2,3-didehydro-N-acetylneuraminic acid. Glycoconj. J. 18, 331–337 (2001)
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The authors would like to dedicate this review to Prof. José A. Cabezas, recently retired who, as well being our mentor and colleague, introduced us into the fascinating field of sialic acid-containing glycoconjugates and viral sialidases at a time when just a very small number of scientists were paying attention to this important field of research. Also, he has been for us a continuous source of inspiration and friendship to us.
The ganglioside nomenclature of Svennerholm [1] is used.
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Villar, E., Barroso, I.M. Role of sialic acid-containing molecules in paramyxovirus entry into the host cell: A minireview. Glycoconj J 23, 5–17 (2006). https://doi.org/10.1007/s10719-006-5433-0
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DOI: https://doi.org/10.1007/s10719-006-5433-0