Sialic acid tissue distribution and influenza virus tropism

Influenza and other Respiratory Viruses

Volumn 2, Issue 5, 2008, Pages 147-154

  Kumlin, Urban ^a   Olofsson, Sigvard ^b   Dimock, Ken ^c   Arnberg, Niklas ^a  

^a UMEÅ UNIVERSITY   (Sweden)

^b UNIVERSITY OF GOTHENBURG   (Sweden)

^c UNIVERSITY OF OTTAWA   (Canada)

Author keywords

Eye; Influenza; Receptor; Sialic acid; Tropism

Indexed keywords

SIALIC ACID;

AVIAN INFLUENZA; CENTRAL NERVOUS SYSTEM DISEASE; EYE; HUMAN; INFLUENZA VIRUS; INFLUENZA VIRUS A; NONHUMAN; PRIORITY JOURNAL; RECEPTOR SENSITIVITY; REVIEW; TISSUE DISTRIBUTION; VIRUS CELL INTERACTION; VIRUS ENTRY; VIRUS PATHOGENESIS; VIRUS REPLICATION; VIRUS TRANSMISSION; VIRUS VIRULENCE; ZOONOSIS;

HUMANS; N-ACETYLNEURAMINIC ACID; ORTHOMYXOVIRIDAE; TISSUE DISTRIBUTION; VIRUS ATTACHMENT;

EID: 57649215883     PISSN: 17502640     EISSN: 17502659     Source Type: Journal    
DOI: 10.1111/j.1750-2659.2008.00051.x     Document Type: Review

References (83)

1. Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y. Evolution and ecology of influenza A viruses. Microbiol Rev 1992; 56: 152-179.
2. Kawaoka Y, Krauss S, Webster RG. Avian-to-human transmission of the PB1 gene of influenza A viruses in the 1957 and 1968 pandemics. J Virol 1989; 63: 4603-4608.
3. Scholtissek C, Rohde W, Von Hoyningen V, Rott R. On the origin of the human influenza virus subtypes H2N2 and H3N2. Virology 1978; 87: 13-20.
4. Taubenberger JK, Reid AH, Lourens RM et al. Characterization of the 1918 influenza virus polymerase genes. Nature 2005; 437: 889-893.
5. Olofsson S, Kumlin U, Dimock K, Arnberg N. Avian influenza and sialic acid receptors: More than meets the eye? Lancet Infect Dis 2005; 5: 184-188.
6. Arnberg N, Edlund K, Kidd AH, Wadell G. Adenovirus type 37 uses sialic acid as a cellular receptor. J Virol 2000; 74: 42-48.
7. Nokhbeh MR, Hazra S, Alexander DA et al. Enterovirus 70 binds to different glycoconjugates containing α2,3-linked sialic acid on different cell lines. J Virol 2005; 79: 7087-7094.
8. Rogers GN, Paulson JC. Receptor determinants of human and animal influenza virus isolates: Differences in receptor specificity of the H3 hemagglutinin based on species of origin. Virology 1983; 127: 361-373.
9. 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 1985; 97: 1189-1199.
10. Angata T, Varki A. Chemical diversity in the sialic acids and related alpha-keto acids: An evolutionary perspective. Chem Rev 2002; 102: 439-469.
11. Baum LG, Paulson JC. Sialyloligosaccharides of the respiratory epithelium in the selection of human influenza virus receptor specificity. Acta Histochem Suppl 1990; 40: 35-38.
12. Couceiro JN, Paulson JC, Baum LG. Influenza virus strains selectively recognize sialyloligosaccharides on human respiratory epithelium; the role of the host cell in selection of hemagglutinin receptor specificity. Virus Res 1993; 29: 155-165.
13. Gagneux P, Cheriyan M, Hurtado-Ziola N et al. Human-specific regulation of alpha2-6 linked sialic acids. J Biol Chem 2003; 278: 48245-48250.
14. Subbarao K, Webster RG, Kawaoka Y, Murphy BR. Are there alternative avian influenza viruses for generation of stable attenuated avian-human influenza A reassortant viruses? Virus Res 1995; 39: 105-118.
15. Chou HH, Hayakawa T, Diaz S et al. Inactivation of CMP-N-acetylneuraminic acid hydroxylase occurred prior to brain expansion during human evolution. Proc Natl Acad Sci 2002; 99: 11736-11741.
16. Van Blerkom LM. Role of viruses in human evolution. Am J Phys Anthropol 2003; 37: 14-46.
17. Ito T, Suzuki Y, Suzuki T et al. Recognition of N -glycolylneuraminic acid linked to galactose by the alpha2,3 linkage is associated with intestinal replication of influenza A virus in ducks. J Virol 2000; 74: 9300-9305.
18. Wright PF, Neumann G, Kawaoka Y. Orthomyxoviruses; in Knipe DM, Howley PM (ed): Fields Virology. Philadelphia: Lippincott Williams & Wilkins, 2007; 1691-1740.
19. Peiris JS, Yu WC, Leung CW et al. Re-emergence of fatal human influenza A subtype H5N1 disease. Lancet 2004; 363: 617-619.
20. Uiprasertkul M, Puthavathana P, Sangsiriwut K et al. Influenza A H5N1 replication sites in humans. Emerg Infect Dis 2005; 11: 1036-1041.
21. Fujimura Y, Takeda M, Ikai H et al. The role of M cells of human nasopharyngeal lymphoid tissue in influenza virus sampling. Virchows Arch 2004; 444: 36-42.
22. Shinya K, Ebina M, Yamada S et al. Avian flu: Influenza virus receptors in the human airway. Nature 2006; 440: 435-436.
23. Paulsen FP, Tschernig T, Debertin AS et al. Similarities and differences in lectin cytochemistry of laryngeal and tracheal epithelium and subepithelial seromucous glands in cases of sudden infant death and controls. Thorax 2001; 56: 223-227.
24. Ibricevic A, Pekosz A, Walter MJ et al. Influenza virus receptor specificity and cell tropism in mouse and human airway epithelial cells. J Virol 2006; 80: 7469-7480.
25. Matrosovich MN, Matrosovich TY, Gray T, Roberts NA, Klenk H-D. Human and avian influenza viruses target different cell types in cultures of human airway epithelium. Proc Natl Acad Sci 2004; 101: 4620-4624.
26. Thompson CI, Barclay WS, Zambon MC, Pickles RJ. Infection of human airway epithelium by human and avian strains of influenza a virus. J Virol 2006; 80: 8060-8068.
27. Kogure T, Suzuki T, Takahashi T et al. Human trachea primary epithelial cells express both sialyl(alpha2-3)Gal receptor for human parainfluenza virus type 1 and avian influenza viruses, and sialyl(alpha2-6)Gal receptor for human influenza viruses. Glycoconj J 2006; 23: 101-106.
28. Nicholls JM, Chan MC, Chan WY et al. Tropism of avian influenza A (H5N1) in the upper and lower respiratory tract. Nat Med 2007; 13: 147-149.
29. van Riel D, Munster VJ, de Wit E et al. Human and Avian Influenza Viruses Target Different Cells in the Lower Respiratory Tract of Humans and Other Mammals. Am J Pathol 2007; 171: 1215-1223.
30. De Jong JC, Wigand R, Wadell G et al. Adenovirus 37: Identification and characterization of a medically important new adenovirus type of subgroup D. J Med Virol 1981; 7: 105-118.
31. Gordon YJ, Aoki K, Kinchington PR. Adenovirus keratoconjunctivitis; in Pepose JS, Holland GN, Wilhelmus KR (ed): Ocular Infection and Immunity. St Louis, MO: Mosby, 1996; 877-894.
32. Heim A, Ebnet C, Harste G, Pring-Akerblom P. Rapid and quantitative detection of human adenovirus DNA by real-time PCR. J Med Virol 2003; 70: 228-239.
33. Azar MJ, Dhaliwal DK, Bower KS, Kowalski RP, Gordon YJ. Possible consequences of shaking hands with your patients with epidemic keratoconjunctivitis. Am J Ophthalmol 1996; 121: 711-712.
34. Aoki K, Tagawa Y. A twenty-one year surveillance of adenoviral conjunctivitis in Sapporo, Japan. Int Ophthalmol Clin 2002; 42: 49-54.
35. Hierholzer JC, Pallansch MA. Acute hemorrhagic conjunctivitis in the western hemisphere (1980-1987); in Uchida Y, Ishii K, Miyamura K, Yamazaki S (ed): Acute Hemorrhagic Conjunctivitis Etiology, Epidemiology, and Clinical Manifestations. New York: S. Karger AG, 1989; 49-56.
36. Ishii K. Acute hemorrhagic conjunctivitis in the eastern hemisphere; in Uchida Y, Ishii K, Miyamura K, Yamazaki Y (ed): Acute Hemorrhagic Conjunctivitis. Etiology, Epidemiology and Clinical Manifestations. New York: S. Karger AG, 1989; 11-33.
37. Howitt BF, K BL, Kissling RE. Presence of neutralizing antib odies of newcastle disease virus in human sera. Am J Public Health 1948; 38: 1263-1272.
38. Creuzot-Garcher C, Guerzider V, Assem M et.al. Alteration of sialyl Lewis epitope expression in pterygium. Invest Ophthalmol Vis Sci 1999; 40: 1631-1636.
39. Terraciano AJ, Wang N, Schuman JS et al. Sialyl Lewis X, Lewis X, and N -acetyllactosamine expression on normal and glaucomatous eyes. Curr Eye Res 1999; 18: 73-78.
40. Nilsson EC, Jamshidi F, Johansson SM, Oberste MS, Arnberg N. Sialic Acid is a cellular receptor for coxsackievirus a24 variant, an emerging virus with pandemic potential. J Virol 2008; 82: 3061-3068.
41. Scholtissek C, Burger H, Kistner O, Shortridge KF. The nucleoprotein as a possible major factor in determining host specificity of influenza H3N2 viruses. Virology 1985; 147: 287-294.
42. Chan PKS. Outbreak of avian influenza A (H5N1) virus infection in Hong Kong in 1997. Clin Infect Dis 2002; 34: 58-64.
43. Li KS, Guan Y, Wang J et al. Genesis of a highly pathogenic and potentially pandemic H5N1 influenza virus in eastern Asia. Nature 2004; 430: 209-213.
44. de Jong MD, Bach VC, Phan TQ et al. Fatal avian influenza A (H5N1) in a child presenting with diarrhea followed by coma. N Engl J Med 2005; 352: 686-691.
45. Wright PW, Strauss GH, Langford MP. Acute hemorrhagic conjunctivitis. Am Fam Physician 1992; 45: 173-178.
46. McChesney MB, Miller MC, Rota PA et al. Experimental measles I. Pathogenesis in the normal and the immunized host. Virology 1997; 233: 74-84.
47. Bitko V, Musiyenko A, Barik S. Viral infection of the lungs through the eye. J Virol 2007; 81: 783-790.
48. Langford MP, Stanton GJ, Barber JC, Baron S. Early-appearing antiviral activity in human tears during a case of picornavirus epidemic conjunctivitis. J Infect Dis 1979; 139: 653-658.
49. Jaax NK, Davis KJ, Geisbert TJ et al. Lethal experimental infection of rhesus monkeys with Ebola-Zaire (Mayinga) virus by the oral and conjunctival route of exposure. Arch Pathol Lab Med 1996; 120: 140-155.
50. Tannock GA, Paul JA, Barry RD. Immunization against influenza by the ocular route. Vaccine 1985; 3: 277-280.
51. Klopfleisch R, Werner O, Mundt E, Harder T, Teifke JP. Neurotropism of highly pathogenic avian influenza virus A/chicken/Indonesia/2003 (H5N1) in experimentally infected pigeons (Columbia livia f. domestica). Vet Pathol 2006; 43: 463-470.
52. CDC. CfDCaP update: Influenza activity -United States and worldwide, 2003-04 season, and composition of the 2004-05 influenza vaccine. MMWR Morb Mortal Wkly Rep. 2004; 53: 547-552.
53. Marshall M. Avian influenza H7N2, human -United Kingdom (Wales) (08) 2007. Available at: http://www.promedmail.org/pls/otn/f?p= 2400:1202:857450566246460::NO::F2400_P1202_CHECK_ DISPLAY,F2400_P1202_PUB_MAIL_ID:X,37732.
54. Nguyen-Van-Tam JS, Nair P, Acheson P, et al. Outbreak of low pathogenicity H7N3 avian influenza in UK, including associated case of human conjunctivitis. Euro Surveill 2006; 11: 2952. Available at http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=2952.
55. Webster RG, Geraci J, Petursson G, Skirnisson K. Conjunctivitis in human beings caused by influenza A virus of seals. N Engl J Med 1981; 304: 911.
56. Fouchier RA, Schneeberger PM, Rozendaal FW et al. Avian influenza A virus (H7N7) associated with human conjunctivitis and a fatal case of acute respiratory distress syndrome. Proc Natl Acad Sci 2004; 101: 1356-1361.
57. Munster VJ, de Wit E, van Riel D et.al. The molecular basis of the pathogenicity of the Dutch highly pathogenic human influenza A H7N7 viruses. J Infect Dis 2007; 196: 258-265.
58. Oner AF, Bay A, Arslan S et al. Avian influenza A (H5N1) infection in eastern Turkey in 2006. N Engl J Med 2006; 355: 2179-2185.
59. Writing committee of the second world health organization consultation on clinical aspects of human infection with avian influenza A (H5N1) virus. Update on avian influenza A (H5N1) virus infection in humans. N Engl J Med 2008; 358: 261-273.
60. Van Borm S, Thomas I, Hanquet G et al. Highly pathogenic H5N1 influenza virus in smuggled Thai eagles, Belgium. Emerg Infect Dis 2005; 11: 702-705.
61. Tweed SA, Skowronski DM, David TS et al. Human illness from avian influenza H7N3, British Columbia. Emerg Inf Dis 2004; 10: 2196-2199.
62. Kurtz J, Manvell RJ, Banks J. Avian influenza virus isolated from a woman with conjunctivitis. Lancet 1996; 348: 901-902.
63. Taylor HR, Turner AJ. A case report of fowl plague keratoconjunctivitis. Br J Ophthalmol 1977; 61: 86-88.
64. Human cases of influenza A(H5N1) infection in eastern Turkey, December 2005 to January 2006, Wkly Epidemiol Rec, 2006; 81: 410-416.
65. Belser JA, Lu X, Maines TR et al. Pathogenesis of avian influenza (H7) virus infection in mice and ferrets: enhanced virulence of Eurasian H7N7 viruses isolated from humans. J Virol 2007; 81: 11139-11147.
66. Belser JA, Blixt O, Chen LM et al. Contemporary North American influenza H7 viruses possess human receptor specificity: Implications for virus transmissibility. Proc Natl Acad Sci USA 2008; 105: 7558-7563.
67. Stevens J, Blixt O, Paulson JC, Wilson IA. Glycan microarray technologies: tools to survey host specificity of influenza viruses. Nat Rev Microbiol 2006; 4: 857-864.
68. Stevens J, Blixt O, Tumpey TM et al. Structure and receptor specificity of the hemagglutinin from an H5N1 influenza virus. Science 2006; 312: 404-410.
69. Enserink M. Bird flu infected 1000, Dutch researchers say. Science 2004; 306: 590.
70. Beigel JH, Farrar J, Han AM et.al. Avian influenza A (H5N1) infection in humans. N Engl J Med 2005; 353: 1374-1385.
71. Diebold Y, Calonge M, de Salamanca AE et al. Characterization of a spontaneously immortalized cell line (IOBA-NHC) from normal human conjunctiva. Invest Ophthalmol Vis Sci 2003; 44: 4263-4274.
72. Schiff LA, Nibert ML, Tyler KL. Orthoreoviruses and their replication;in Knipe DM, Howley PM (ed): Fields Virology. Philadelphia, PA: Lippincott Williams & Wilkins, 2007; 1853-1916.
73. Arisoy ES, Demmler GJ, Thakar S, Doerr C. Meningitis due to parainfluenza virus type 3: report of two cases and review. Clin Infect Dis 1993; 17: 995-997.
74. Zhang L, Bukreyev A, Thompson CI et al. Infection of ciliated cells by human parainfluenza virus type 3 in an in vitro model of human airway epithelium. J Virol 2005; 79: 1113-1124.
75. Yuan P, Thompson TB, Wurzburg BA et al. Structural studies of the parainfluenza virus 5 hemagglutinin-neuraminidase tetramer in complex with its receptor, sialyllactose. Structure 2005; 13: 803-815.
76. Russell RJ, Stevens DJ, Haire LF, Gamblin SJ, Skehel JJ. Avian and human receptor binding by hemagglutinins of influenza A viruses. Glycoconj J 2006; 23: 85-92.
77. Ando Y, Iwasaki T, Terao K, Nishimura H, Tamura S. Conjunctivitis following accidental exposure to influenza B virus/Shangdong/07/97. J Infect Dis 2001; 42: 223-224.
78. Kunkel F, Herrler G. Structural and functional analysis of the surface protein of human coronavirus OC43. Virology 1993; 195: 195-202.
79. Arbour N, Day R, Newcombe J, Talbot PJ. Neuroinvasion by human respiratory coronaviruses. J Virol 2000; 74: 8913-8921.
80. Imperiale M, Major EO. Polyomaviruses; in Knipe DM, Howley PM (ed): Fields Virology. Philadelphia, PA: Lippincott Williams & Wilkins, 2007; 2263-2298.
81. Liu CK, Wei G, Atwood WJ. Infection of glial cells by the human polyomavirus JC is mediated by an N-linked glycoprotein containing terminal alpha(2-6)-linked sialic acids. J Virol 1998; 72: 4643-4649.
82. Reploeg MD, Storch GA, Clifford DB. BK virus: a clinical review. Clin Infect Dis 2001; 33: 191-202.
83. Dugan AS, Eash S, Atwood WJ. An N-linked glycoprotein with alpha(2,3)-linked sialic acid is a receptor for BK virus. J Virol 2005; 79: 14442-14445.