Publications

2019

­Barnard, K.N., Wasik, B.R., LaClair, J.R.a, Buchholz, D.W., Wendy S. Weichert, W.S., Alford-Lawrence, B.K., Aguilar, H.C., Parrish, C.R. (2019). Expression of 9-O– and 7,9-O-acetyl modified sialic acid in cells and their effects on influenza viruses. mBio in press.

Bensing, B.A., Li, L., Yakovenko, O., Wong, M., Barnard, K.N., Iverson, T.M., Lebrilla, C.B., Parrish, C.R., Thomas W.E., Xiong, Y., Sullam, P.M. Recognition of specific sialoglycan structures by oral streptococci impacts the severity of endocardial infection. PloS Pathogens, 15(6):e1007896.

Wasik, B.R., Voorhees, I.E.H., Barnard, K.N., Alford-Lawrence, B.K., Weichert, W.S., Hood, G., Nogales, A., Martínez-Sobrido, L., Holmes, E.C., Parrish, C.R. (2019). Influenza viruses in mice: deep sequencing analysis of serial passage and effects of sialic acid structural variation. Journal of Virology Sep 11. pii: JVI.01039-19.

Lee H, Callaway HM, Cifuente JO, Bator CM, Parrish CR, Hafenstein SL.(2019) Transferrin receptor binds virus capsid with dynamic motion. Proceedings of the National Academy of Sciences U S A. 116:20462-20471. doi: 10.1073/pnas.1904918116.

Voorhees, I.E.H., Lee, H., Allison, A.B., Lopez-Astacio, R., Goodman, L.B., Oyesola, O.O., Omobowale, O., Fagbohun, O., Dubovi, E.J., Hafenstein, S.L., Holmes, E.C., Parrish, C.R. (2019) Limited intra-host diversity and background evolution accompany 40 years of canine parvovirus host adaptation and spread. Journal of Virology pii: JVI.01162-19. doi: 10.1128/JVI.01162-19.

Wasik, B.R., de Wit, E., Munster, V., Lloyd-Smith, J., Martinez-Sobrido, L., Parrish, C.R. (2019) Onward transmission of viruses: how do viruses emerge to cause epidemics after spillover? Philos Trans R Soc Lond B Biol Sci. 374(1782):20190017.

Goetschius, D.J., Parrish, C.R., Hafenstein, S. (2019) Asymmetry in icosahedral viruses. Current Opinions in Virology 36:67-73. doi: 10.1016/j.coviro.2019.05.006.

Pepin, K.M., Hopken, M.W., Shriner, S.A., Spackman, E., Abdo, Z., Parrish, C., Riley, S., Lloyd-Smith, J.O., Piaggio, A.J. (2019) Improving risk assessment of the emergence of novel influenza A viruses by incorporating environmental surveillance. Philos Trans R Soc Lond B Biol Sci. 374(1782):20180346.

Parrish, C.R., Voorhees, I.E.H. (2019) H3N8 and H3N2 Canine Influenza Viruses: Understanding These New Viruses in Dogs. Vet Clin North Am Small Anim Pract. 49(4):643-649.

Callaway, H.M., Subramanian, S., Urbina, C., Barnard, K., Dick, R., Bator, C.M., Hafenstein, S.L., Gifford, R.J., Parrish, C.R. (2019). Examination and reconstruction of three ancient endogenous parvovirus capsid proteins in rodent genomes. J. Virol. 93(6). pii: e01542-18.

2018

Dunbar, C.A., Callaway, H.M., Parrish, C.R., Jarrold, M.F. Probing Fragment Antibody Binding to Canine Parvovirus Capsids with Charge Detection Mass Spectrometry. J. Amer. Chem. Soc., 140(46):15701-15711.

Chauché, C., Nogales, A., Zhu, H., Goldfarb, D., Shanizza, A.I.A., Gu, Q., Parrish, C.R., Martínez-Sobrido, L., Marshall, J.F., Murcia, P.R. (2018). Mammalian adaptation of an avian influenza A virus involves stepwise changes in NS1. J. Virol. 92: e01875-17

Mäntylä, E., Chacko, J.V., Aho, V., Parrish, C.R., Shahin, V., Kann, K., Digman, M.A., Gratton, E., Vihinen-Ranta, M. (2018). Viral highway to nucleus exposed by image correlation analyses. Scientific Reports 8: 1152

Voorhees, I.E.H., Dalziel, B.D., Glaser, A., Dubovi, E.J., Murcia, P.R., Newbury, S., Toohey-Kurth, K., Su, S., Kriti, D., Van Bakel, H., Goodman, L.B., Leutenegger, C., Holmes, E.C., Parrish, C.R. (2018). Multiple incursions and recurrent epidemic fade-out of H3N2 canine influenza A virus in the United States. J. Virol., 92. pii: e00323-18.

Callaway, H.M., Welsch, K., Weichert, W., Allison, A.B., Hafenstein, S.L., Huang, K., Iketani, S., Parrish, C.R. (2018). Complex and dynamic interactions between parvovirus capsids, transferrin receptors and antibodies control cell infection and host range. J. Virol., 92 no. 13 e00460-18

Joo, E.J., Wasik, B.R., Parrish, C., Paz, H., Muehlenhoff, M., Abdel-Azim, H., Groffenre, J., Heisterkamp, N. B (2018). Pre-B acute lymphoblastic leukemia expresses cell surface nucleolin as a 9-O-acetylated sialoglycoprotein. Scientific Reports, 8(1):17174.

2017

Voorhees, I.E.H., Glaser, A.L., Toohey-Kurth, K., Newbury, S., Dalziel, B.D., Dubovi, E.J., Poulsen, K., Leutenegger, C., Willgert, K.J.E., Laura Brisbane-Cohen, Richardson-Lopez, J., Holmes, E.C., Parrish, C.R. (2017). Spread of canine influenza A (H3N2) virus, United States. Emerging Infectious Diseases 23:1950

Nogales, A., Chauché, C., DeDiego, M.L., Topham, D.J., Parrish, C.R., Murcia, P.R., Martínez-Sobrido, L. (2017). The K186E amino acid substitution in the canine influenza virus H3N8 NS1 protein restores its ability to inhibit host gene expression. J. Virol., 91: e00877-17

Nogales, A., Huang, K., Chauche, C., DeDiego, M.L., Murcia, P.R., Parrish, C.R., Martinez-Sobrido, L. (2017) Canine influenza viruses with modified NS1 proteins for the development of live-attenuated vaccines. Virology, 500:1-10.

Plowright, R.K., Parrish, C.R., McCallum, H., Hudson, P.J., Ko, A.I., Graham, A.J., Lloyd-Smith, J.O. (2017). Pathways to zoonotic spillover. Nature Rev. Micro. 15, 502.

Wasik, B.R., Barnard, K.N., Ossiboff, R.J., Khedri, Z., Feng, F.H., Yu, H., Chen, X., Perez, D.R., Varki, A., Parrish, C.R. (2017). Distribution of O-Aacetylated sialic acids among target host tissues for influenza virus. mSphere 2 (5), e00379-16

2016

Callaway, H.M., Feng, K.H., Lee, D.W., Allison, A.B., Pinard, M., McKenna, R., Agbandje-McKenna, M., Hafenstein, S., Parrish, C.R. (2016). Parvovirus capsid structures required for infection: mutations controlling receptor recognition and protease cleavages. J. Virol., 91:871.

Lee, D.W., Allison A.B., Bacon, K.B., Parrish, C.R., Daniel, S. (2016). Single-particle tracking shows a point mutation in the carnivore parvovirus capsid switches binding between host-specific transferrin receptors. J. Virol., 90:4849-4853.

Khedri, Z., Xiao, A., Yu, H., Landig, C.S., Li, W., Diaz, S., Wasik, B.R., Parrish, C.R., Wang, L.P., Varki, A. and Chen, X., 2016. A Chemical Biology Solution to Problems with Studying Biologically Important but Unstable 9-O-Acetyl Sialic Acids. ACS Chemical Biology.

Organtini, L.J., Lee, H., Iketani, S., Huang, K., Ashley, R.E., Makhov, A.M., Conway, J.F., Parrish, C.R. and Hafenstein, S. (2016). The near-atomic resolution structure of a highly neutralizing Fab bound to canine parvovirus. J. Virol., JVI-01112.

Wasik, B.R., Barnard, K.N. and Parrish, C.R. (2016). Effects of Sialic Acid Modifications on Virus Binding and Infection. Trends in Microbiology 24:991-1001.

Feng, K.H., Sun, M., Iketani, S., Holmes, E.C. and Parrish, C.R. (2016). Comparing the functions of equine and canine influenza H3N8 virus PA-X proteins: Suppression of reporter gene expression and modulation of global host gene expression. Virology, 496, pp.138-146.

2015

Kailasan, S., Agbandje-McKenna, M. and Parrish, C.R., (2015). Parvovirus Family Conundrum: What Makes a Killer?. Annual Rev. Virol., 2, pp.425-450.

Allison, A. B., Organtini, L. J., Zhang, S., Hafenstein, S. L., Holmes, E. C., & Parrish, C. R. (2015). Single mutations in the VP2 300 loop region of the three-fold spike of the carnivore parvovirus capsid can determine host range. J. Virol., JVI-02636.

Feng KH, Gonzalez G, Deng L, Yu H, Tse VL, Huang L, Huang K, Wasik BR, Zhou B, Wentworth DE, Holmes EC, Chen X, Varki A, Murcia PR, Parrish CR. (2015) Equine and Canine Influenza H3N8 Viruses Show Minimal Biological Differences Despite Phylogenetic Divergence. J. Virol. 89(13):6860-73.

Parrish CR, Murcia PR, Holmes EC. (2015) Influenza virus reservoirs and intermediate hosts: dogs, horses, and new possibilities for influenza virus exposure of humans. J. Virol. 89:2990-4.

Organtini LJ, Allison AB, Lukk T, Parrish CR, Hafenstein S.(2015) Global displacement of canine parvovirus by a host-adapted variant: structural comparison between pandemic viruses with distinct host ranges. J. Virol. 89(3):1909-12.

Allison AB, Ballard JR, Tesh RB, Brown JD, Ruder MG, Keel MK, Munk BA, Mickley RM, Gibbs SE, Travassos da Rosa AP, Ellis JC, Ip HS, Shearn-Bochsler VI, Rogers MB, Ghedin E, Holmes EC, Parrish CR, Dwyer C. (2015) Cyclic avian mass mortality in the northeastern United States is associated with a novel orthomyxovirus. J Virol. 89(2):1389-403.

2014

Allison, A.B., Kohler, D.J., Ortega, A., Hoover, E.A., Grove, D.M., Holmes, E.C., Parrish, C.R. PLoS Pathog. (2014) Host-specific parvovirus evolution in nature is recapitulated by in vitro adaptation to different carnivore species. 10(11):e1004475.

Dalziel BD, Huang K, Geoghegan JL, Arinaminpathy N, Dubovi EJ, Grenfell BT, Ellner SP, Holmes EC, Parrish CR.(2014) Contact heterogeneity, rather than transmission efficiency, limits the emergence and spread of canine influenza virus. PLoS Pathog. Oct 23;10(10):e1004455.

Gonzalez, G., Marshall, J. F., Morrell, J., Robb, D., McCauley, J. W., Perez, D. R., … & Murcia, P. R. (2014). Infection and pathogenesis of canine, equine and human influenza viruses in canine tracheas. J. Virol., JVI-00887.

Lyi, S. M., Tan, M. J. A., & Parrish, C. R. (2014). Parvovirus particles and movement in the cellular cytoplasm and effects of the cytoskeleton. Virology, 456, 342-352.

2013

Gurda, B.S., DiMattia, M.A., Miller, E.B., Bennett, A., McKenna, R., Wendy S. Weichert, Nelson, C.D., Chen, W-J., Muzyczka, N., Olson, N.H., Sinkovits, R.S., Chiorini, J.A, Zolotutkhin, S., Kozyreva, O.G., Samulski, R.J., Baker; T.B., Parrish, C.R., Agbandje-McKenna, M. (2013). Capsid antibodies to different adeno-associated virus serotypes bind common regions. J. Virol. 87:9111-24.

Berns, K.I., Parrish, C.R. (2013). Chapter 57, Parvoviridae. Fields Virology. (In Press).

Löfling, J., Lyi, S.M., Parrish, C.R., Varki, A. (2013) Canine and feline parvoviruses preferentially recognize the non-human cell surface sialic acid N-glycolylneuraminic acid. Virology 440:89-96.

Allison, A.B., Kohler, D.J., Fox, K.A., Brown, J.D., Gerhold, R.W., Shearn-Bochsler, V.I., Dubovi, E.J., Parrish, C.R., Holmes, E.C. (2013) Frequent cross-species transmission of parvoviruses among diverse carnivore hosts. Journal of Virology 87:2342-2347.

Truyen, U., & Parrish, C. R. (2013). Feline Panleukopenia virus: Its interesting evolution and current problems in immunoprophylaxis against a serious pathogen. Vet. Micro.

2012

Markovich, J.E., Stucker, K.M., Carr, A.H., Harbison, C.E., Scarlett, J.M., Parrish, C.R. (2012). Effects of canine parvovirus strain variations on diagnostic test results and clinical management of enteritis in dogs. J. Amer. Vet. Med. Assoc. 241:66-72.

Allison, A.B., Harbison, C.E., Pagan, I., Stucker, K.M., Kaelber, J.T., Brown, J.T., Ruder, M.G., Keel, M.K., Dubovi, E.J., Holmes, E.C., Parrish, C.R. (2012). Role of multiple hosts in the cross-species transmission and emergence of a pandemic parvovirus. Journal of Virology, 86:865-872.

Stucker, K.M., Pagan, I., Cifuente, J.O., Kaelber, J.T., Lillie, T.D., Hafenstein, S., Holmes, E.C., Parrish, C.R. (2012). The role of evolutionary intermediates in the host adaptation of canine parvovirus. J. Virol., 86:1514-1521.

Harbison, C.E., Weichert, W.S., Gurda, B.L., Chiorini, J.A., Agbandje-McKenna, M., Parrish, C.R. (2012). Examining the cross-reactivity and neutralization mechanisms of a panel of mAbs against adeno-associated virus serotypes 1 and 5. J. Gen. Virol. 93:347-355.

Cureton, D.K., Harbison, C.E., Cocucci1, E., Parrish.C.R, and Kirchhausen, T. (2012) Limited receptor crosslinking promotes rapid diffusion of canine parvovirus into clathrin endocytic structures. J. Virol. 86:5330-5340.

Kaelber, J.T., Demogines, A., Harbison, C.E., Allison, A.B., Goodman, L.B., Sawyer, S.L., Parrish, C.R. (2012) Evolutionary reconstructions of the transferrin receptor of Caniforms supports canine parvovirus being a re-emerged and not a novel pathogen in dogs. PLoS Pathogens, 8(5):e1002666

Morse, S.S., Mazet J.A., Woolhouse, M, Parrish, C.R., Carroll, D., Karesh, W.B., Zambrana-Torrelio, C, Lipkin, W.I., Daszak, P. (2012). Prediction and prevention of the next pandemic zoonosis. Lancet. 380:1956-65.

2011

Kim, J.W., Lyi, S.M., Parrish, C.R., Parker, J.S. (2011). A proapoptotic peptide derived from reovirus outer capsid protein {micro}1 has membrane-destabilitzing activity. Journal of Virology 85:1507 � 1516.

Braganza, A., Wallace, K., Pell, L., Parrish, C.R., Siegel, D.L., Mason, N.J. (2011) Generation and validation of canine single chain variable fragment phage display libraries. Veterinary Immunolgy and Immunopathology 139:27 � 40.

Malilk Peiris J.S., Parrish, C.R. (2011) Emerging Viruses. Current Opinion Virology 1:617-619

Borer, E.T., Antonovics, J., Kinkel, L.L., Hudson, P.J., Daszak, P., Ferrari, M.J., Garrett, K.A., Parrish, C.R., Read, A.F., and Rizzo, D.M. (2011). Bridging taxonomic and disciplinary divides in infectious disease. Ecohealth 8: 261 – 267.

Flanagan, M.L., Parrish, C.R., Cobey, S., Glass, G.E., Bush, R.M., and Leighton, T.J. (2011). Anticipating the species jump: surveillance for emerging viral threats. Zoonoses Public Health. Sep 14. doi: 10.1111/j.1863-2378.2011.01439.x.

2010

Hayward, J.J., Dubovi., E.J., Scarlett, J.M., Janeczko, S., Holmes, E.C., Parrish, C.R. (2010). Microevolution of canine influenza virus in shelters and its molecular epidemiology in the United States. Journal of Virology 84:12636-12645.

Goodman L, Lyi S, Johnson N, Cifuente J., Hafenstein S, and CR Parrish. The binding site on the transferrin receptor for the parvovirus capsid, and the effects of altered affinity on cell uptake and infection. Journal of Virology 84:4969-4978.

Murcia P, Baillie G, Daly J, Elton D, Jervis C, Mumford J, Newton R, Parrish C, Hoelzer K, Holmes E, Grenfell B and J Wood. The intra- and inter-host evolutionary dynamics of equine influenza virus. Journal of Virology 84:6943-6954.

Hoelzer K, Murcia P, Baillie J, Wood J, Metzger S, Osterrieder N, Dubovi E, Holmes E, and CR Parrish. Intra-host dynamics of canine influenza virus in naïve and partially immune dogs. Journal of Virology 41(6):39.

Hoelzer K, and CR Parrish. The emergence of parvoviruses of carnivores. Veterinary Research in press.

CR Parrish. Microscopic analysis of viral cell binding, entry and infection in live cells. Royal Society of Chemisty ebooks collection No. 21, Structural Virology, Chap. 2.

CR Parrish. Structures and functions of parvovirus capsids and the process of cell infection. Current Topics in Microbiology and Immunology 343:149-176.

2009

Harbison C, Lyi S., Weichert, and CR Parrish. Early steps in cell infection by parvoviruses: endosomal trafficking and effects of host specific differences in cell receptor binding. Journal of Virology 83:10504�10514.

Hafenstein S, Bowman V, Sun T, Nelson C, Palermo L, Chipman P, Battisti T, Parrish C, and MG Rossmann. Structural comparison of different antibodies interacting with parvovirus capsids. Journal of Virology 83:5556-5566.

2008

Hafenstein, S., Bowman, V.D., Sun, T., Nelson, D.S., Palermo, L.M., Chipman, P.R., Battistia, A.J. Parrish, C.R., Rossmann, M.G.(2008) Structural comparison of different antibodies interacting with parvovirus capsids. Journal of Virology 83:5556-5566.

Nelson, C.D.S., Minkinen, E., Bergkvist, M., Hoelzer, K., Fisher, M., Bothner, B.P., Parrish, C.R. (2008). Detecting small changes and additional peptides in the canine parvovirus capsid structure. Journal of Virology 82:10397-10407.

Hoelzer, K., Shackelton, L.A., Holmes, E.C., Parrish, C.R.. (2008) Within-host genetic diversity of endemic and emerging parvoviruses of dogs and cats. Journal of Virology 82:11096-11105.

Hoelzer, K., Shackelton, L.A., Parrish, C.R. Holmes, E.C. (2008). Phylogenetic analysis reveals the emergence, evolution and dispersal of carnivore parvoviruses. Journal of General Virology 89:2280-2289

Parrish, C.R., Holmes, E.C., Morens, D., Park, E-C., Burke, D., Calisher, C., Saif, L., Daszak, P. (2008). Cross-species transmission and the emergence of new epidemic diseases. Microbiology and Molecular Biology Reviews. 2008 72:457-470.

Hoelzer, K., Parrish C.R. (2008) Evolution and variation of the parvoviruses. Chapt. 17. In: Origin and Evolution of Viruses, 2nd Edn. (Eds. Domingo, E. Holland, J., Parrish, C.R.). Elsevier.

Harbison, C.E., Chiorini, J.A., Parrish, C.R. (2008) The odyssey of the parvovirus capsid – journeying from the cell surface to the nucleus. Trends in Microbiology.16:208-214

Hoelzer, K., Shackelton, L.A., Parrish, C.R. Presence and role of cytosine methylation in DNA viruses. Nucl. Acids Res. 36: 2825-2837.

Rosas, C., Van de Walle, G.R, Metzger, S.M, Hoelzer, K., Dubovi, E.J., Sung, K., Parrish, C.R., Osterrieder, N.(2008) Evaluation of a vectored equine herpesvirus type 1 (EHV-1) vaccine expressing H3 Haemaggluninin in the protection of dogs against canine influenza. Vaccine 26:2335-43.

2007

Hafenstein, S., Palermo, L.M., Kostyuchenko, V.A., Xiao, C., Morais, M.C., Nelson, C.D.S., Bowman, V.D., Battisti, A.J., Chipman, P.R., Parrish, C.R., Rossmann, M.G. (2007). Asymmetric binding of transferrin receptor to parvovirus capsids. Proceedings of the National Academy of Sciences (USA) 104:6589-6589.

Kaufmann, B., Lopez-Bueno, A., Mateu, M. G., Chipman, P.R., Nelson, C.D., Parrish, C.R., Almendral, J.M. and Rossmann, M.G. (2007). Minute virus of mice, a parvovirus, in complex with the Fab fragment of a neutralizing monoclonal antibody. Journal of Virology 81:9851-9858.

Nelson, C. D., Palermo, L. S., Hafenstein, S. L. and Parrish, C. R. 2007. Different mechanisms of antibody-mediated neutralization of parvoviruses revealed using the Fab fragments of monoclonal antibodies. Virology: 361:283-293.

Shackelton, L.A., Hoelzer, K., Parrish, C.R., and Holmes, E.C. (2007). Comparative analysis reveals frequent recombination in the parvoviruses. Journal of General Virology 88:3294-3301.

Rossmann, M.G., Arisaka, F., Battisti, A.J., Bowman, V.D., Chipman, P.R., Fokine, A., Hafenstein, S., Kanamaru, S., Kostyuchenko, V.A., Mesyanzhinov, V.V., Shneider, M.M., Morais, M.C., Leiman, P.G., Palermo, L.M., Parrish, C.R., Xiao, C. (2007). From structure of the complex to understanding of the biology. Acta Crystallographica Section D Biological Crystallography D63:9-16.

2006

Palermo, L.M., Parrish, C.R. Purified feline and canine transferrin receptors show complex interactions with the capsids of canine and feline parvoviruses. Journal of Virology, 80:8482-8492.

Shackelton, L.A., Parrish, C.R., and Holmes, E.C. (2006). Evolutionary basis of codon usage and nucleotide composition bias in vertebrate DNA viruses. Journal of Molecular Evolution. 62:551-563.

2005

Shackelton, L.A., Parrish, C.R., Truyen, U., Holmes, E.C. (2005) High rate of viral evolution associated with the emergence of carnivore parvovirus. Proceedings of the National Academy of Science. (USA) 102: 379-384.

Parrish, C. R., and Kawaoka, Y. (2005). The origins of new pandemic viruses: the acquisition of new host ranges by canine parvovirus and influenza A viruses. Annu Rev Microbiol 59, 553-86

2004

Vihinen-Ranta, M., Suikkanen, S., Parrish, C.R. (2004). Pathways of cell infection by parvoviruses and adeno-associated viruses. Journal of Virology 78:6709-6714.

Hueffer, K., Palermo, L.M., Parrish, C.R. (2004). Parvovirus infection of cells using variants of the feline transferrin receptor altering clathrin-mediated endocytosis, membrane domain localization and capsid binding domains. Journal of Virology 78:5601-5611.