#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Human Adenovirus 52 Uses Sialic Acid-containing Glycoproteins and the Coxsackie and Adenovirus Receptor for Binding to Target Cells


HAdVs are common pathogens in humans, causing disease mainly in eyes, airways and gastrointestinal tract. Most HAdVs are equipped with twelve protruding fiber proteins that mediate attachment to host cell receptor molecules. Recently, a new human gastroenteritis-associated adenovirus (HAdV-52) was identified and classified as the first member of a novel species (HAdV-G). Unlike most other HAdVs, this virus contains two different fiber proteins, a long and a short one, a feature shared only with the two members of species HAdV-F (HAdV-40 and -41). To gain further insights into the mechanisms of HAdV-52 infection of human cells, we set out to identify the host cell receptors used by the long and short fibers. We find that the long fiber binds to a protein-based receptor known as the coxsackievirus and adenovirus receptor (CAR), and that the short fiber binds to glycoproteins that contain sialic acid-capped glycans. The crystal structure determination of a complex of the short fiber knob bound to sialic acid demonstrates that this interaction is unique among HAdVs, and bioinformatic analysis indicates that simian AdVs may also engage sialic acids in the manner seen in HAdV-52. The results presented here provide insights into the plasticity of adenovirus-host cell interactions.


Vyšlo v časopise: Human Adenovirus 52 Uses Sialic Acid-containing Glycoproteins and the Coxsackie and Adenovirus Receptor for Binding to Target Cells. PLoS Pathog 11(2): e32767. doi:10.1371/journal.ppat.1004657
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004657

Souhrn

HAdVs are common pathogens in humans, causing disease mainly in eyes, airways and gastrointestinal tract. Most HAdVs are equipped with twelve protruding fiber proteins that mediate attachment to host cell receptor molecules. Recently, a new human gastroenteritis-associated adenovirus (HAdV-52) was identified and classified as the first member of a novel species (HAdV-G). Unlike most other HAdVs, this virus contains two different fiber proteins, a long and a short one, a feature shared only with the two members of species HAdV-F (HAdV-40 and -41). To gain further insights into the mechanisms of HAdV-52 infection of human cells, we set out to identify the host cell receptors used by the long and short fibers. We find that the long fiber binds to a protein-based receptor known as the coxsackievirus and adenovirus receptor (CAR), and that the short fiber binds to glycoproteins that contain sialic acid-capped glycans. The crystal structure determination of a complex of the short fiber knob bound to sialic acid demonstrates that this interaction is unique among HAdVs, and bioinformatic analysis indicates that simian AdVs may also engage sialic acids in the manner seen in HAdV-52. The results presented here provide insights into the plasticity of adenovirus-host cell interactions.


Zdroje

1. Harrach B, Benkö M, Both GW, Brown M, Davison AJ, et al. (2011) Family Adenoviridae. In: King AMQ, Adams MJ, Carstens EB, LE J, editors. Virus Taxonomy Ninth Report of the International Committee on Taxonomy of Viruses. San Diego: Elsevier Academic Press. pp. 125–141.

2. Wold WSM, Horwitz MS (2007) Adenoviruses. In: Knipe DM, Howley PM, editors. Fields Virology. 5 ed. Philadelphia: Lippincott Williams & Wilkins. pp. 2395–2436.

3. Jones MS, Harrach B, Ganac RD, Gozum MM, Dela Cruz WP, et al. (2007) New adenovirus species found in a patient presenting with gastroenteritis. J Virol 81: 5978–5984. 17360747

4. Bergelson JM, Cunningham JA, Droguett G, Kurt-Jones EA, Krithivas A, et al. (1997) Isolation of a common receptor for Coxsackie B viruses and adenoviruses 2 and 5. Science 275: 1320–1323. 9036860

5. Tomko RP, Xu R, Philipson L (1997) HCAR and MCAR: the human and mouse cellular receptors for subgroup C adenoviruses and group B coxsackieviruses. Proc Natl Acad Sci U S A 94: 3352–3356. 9096397

6. Roelvink PW, Lizonova A, Lee JG, Li Y, Bergelson JM, et al. (1998) The coxsackievirus-adenovirus receptor protein can function as a cellular attachment protein for adenovirus serotypes from subgroups A, C, D, E, and F. J Virol 72: 7909–7915. 9733828

7. Gaggar A, Shayakhmetov DM, Lieber A (2003) CD46 is a cellular receptor for group B adenoviruses. Nat Med 9: 1408–1412. 14566335

8. Segerman A, Atkinson JP, Marttila M, Dennerquist V, Wadell G, et al. (2003) Adenovirus type 11 uses CD46 as a cellular receptor. J Virol 77: 9183–9191. 12915534

9. Marttila M, Persson D, Gustafsson D, Liszewski MK, Atkinson JP, et al. (2005) CD46 is a cellular receptor for all species B adenoviruses except types 3 and 7. J Virol 79: 14429–14436. 16254377

10. Wang H, Li ZY, Liu Y, Persson J, Beyer I, et al. (2011) Desmoglein 2 is a receptor for adenovirus serotypes 3, 7, 11 and 14. Nat Med 17: 96–104. doi: 10.1038/nm.2270 21151137

11. Arnberg N, Edlund K, Kidd AH, Wadell G (2000) Adenovirus type 37 uses sialic acid as a cellular receptor. J Virol 74: 42–48. 10590089

12. Arnberg N, Kidd AH, Edlund K, Olfat F, Wadell G (2000) Initial interactions of subgenus D adenoviruses with A549 cellular receptors: sialic acid versus alpha(v) integrins. J Virol 74: 7691–7693. 10906228

13. Nilsson E (2011) Cellular receptors for viruses with ocular tropism. Umeå: Umeå university. doi: 10.1080/17437199.2011.587961 25473706

14. Rademacher C, Bru T, McBride R, Robison E, Nycholat CM, et al. (2012) A Siglec-like sialic-acid-binding motif revealed in an adenovirus capsid protein. Glycobiology 22: 1086–1091. doi: 10.1093/glycob/cws073 22522600

15. Bewley MC, Springer K, Zhang YB, Freimuth P, Flanagan JM (1999) Structural analysis of the mechanism of adenovirus binding to its human cellular receptor, CAR. Science 286: 1579–1583. 10567268

16. Persson BD, Müller S, Reiter DM, Schmitt BBT, Marttila M, et al. (2009) An arginine switch in the species B adenovirus knob determines high-affinity engagement of the cellular receptor CD46. J Virol 83: 673–686. doi: 10.1128/JVI.01967-08 18987134

17. Wu E, Pache L, Von Seggern DJ, Mullen TM, Mikyas Y, et al. (2003) Flexibility of the adenovirus fiber is required for efficient receptor interaction. J Virol 77: 7225–7235. 12805421

18. Waddington SN, McVey JH, Bhella D, Parker AL, Barker K, et al. (2008) Adenovirus serotype 5 hexon mediates liver gene transfer. Cell 132: 397–409. doi: 10.1016/j.cell.2008.01.016 18267072

19. Lenman A, S. M, Nygren MI, Frängsmyr L, Stehle T, et al. (2011) Coagulation factor IX mediates serotype-specific binding of species A adenoviruses to host cells. J Virol 85: 13420–13431. doi: 10.1128/JVI.06088-11 21976659

20. Kidd AH, Chroboczek J, Cusack S, Ruigrok RW (1993) Adenovirus type 40 virions contain two distinct fibers. Virology 192: 73–84. 8517033

21. Yeh HY, Pieniazek N, Pieniazek D, Gelderblom H, Luftig RB (1994) Human adenovirus type 41 contains two fibers. Virus Res 33: 179–198. 7975882

22. Roy S, Sandhu A, Medina A, Clawson DS, M. WJ (2012) Adenoviruses in fecal samples from asymptomatic rhesus macaques, United States. Emerg Infect Dis 18: 1081–1088. doi: 10.3201/eid1807.111665 22709783

23. Wei CJ, Boyington JC, McTamney PM, Kong WP, Pearce MB, et al. (2010) Induction of broadly neutralizing H1N1 influenza antibodies by vaccination. Science 329: 1060–1064. doi: 10.1126/science.1192517 20647428

24. Barouch DH, Liu J, Li H, Maxfield LF, Abbink P, et al. (2012) Vaccine protection against acquisition of neutralization-resistant SIV challenges in rhesus monkeys. Nature 482: 89–93. doi: 10.1038/nature10766 22217938

25. Roberts DM, Nanda A, Havenga MJ, Abbink P, Lynch DM, et al. (2006) Hexon-chimaeric adenovirus serotype 5 vectors circumvent pre-existing anti-vector immunity. Nature 441: 239–243. 16625206

26. Heise C, Hermiston T, Johnson L, Brooks G, Sampson-Johannes A, et al. (2000) An adenovirus E1A mutant that demonstrates potent and selective systemic anti-tumoral efficacy. Nat Med 6. 11100133

27. Kozarsky KE, Jooss K, Donahee M, F. SJ, M. WJ (1996) Effective treatment of familial hypercholesterolaemia in the mouse model using adenovirus-mediated transfer of the VLDL receptor gene. Nat Gen 13: 54–62. 8673104

28. George SJ, Wan S, Hu J, MacDonald R, Johnson JL, et al. (2011) Sustained reduction of vein graft neointima formation by ex vivo TIMP-3 gene therapy. Circulation 124: S135–142. doi: 10.1161/CIRCULATIONAHA.110.012732 21911803

29. Stadtfeld M, Nagaya M, Utikal J, Weir G, Hochedlinger K (2008) Induced pluripotent stem cells generated without viral integration. Science 322: 945–949. doi: 10.1126/science.1162494 18818365

30. Zak DE, Andersen-Nissen E, Peterson ER, Sato A, Hamilton MK, et al. (2012) Merck Ad5/HIV induces broad innate immune activation that predicts CD8? T-cell responses but is attenuated by preexisting Ad5 immunity. Proc Natl Acad Sci U S A 109: 3503–3512.

31. Li Y, Pong RC, Bergelson JM, Hall MC, Sagalowsky AI, et al. (1999) Loss of adenoviral receptor expression in human bladder cancer cells: a potential impact on the efficacy of gene therapy. Cancer Res 59: 325–330. 9927041

32. Li H, Rhee EG, Masek-Hammerman K, Teigler JE, Abbink P, et al. (2012) Adenovirus serotype 26 utilizes CD46 as a primary cellular receptor and only transiently activates T lymphocytes following vaccination of rhesus monkeys. J Virol 86: 10862–10865. doi: 10.1128/JVI.00928-12 22811531

33. Thirion C, Lochmüller H, Ruzsics Z, Boelhauve M, König C, et al. (2006) Adenovirus vectors based on human adenovirus type 19a have high potential for human muscle-directed gene therapy. Hum Gene Ther 17: 193–205. 16454653

34. Arnberg N (2012) Adenovirus receptors: implications for targeting of viral vectors. Trends Pharmacol Sci 33: 442–448. doi: 10.1016/j.tips.2012.04.005 22621975

35. Jarecki-Khan K, Unicomb LE (1992 Oct;) Seroprevalence of enteric and nonenteric adenoviruses in Bangladesh. J Clin Microbiol 30: 2733–2734. 1400977

36. Saderi H, Roustai MH, Sabahi F (2000) Antibodies to enteric adenoviruses (Ad40 and Ad41) in sera from Iranian children. J Clin Virol 16: 145–147. 10720819

37. Shinozaki T, Araki K, Ushijima H, Fujii R (1987) Antibody response to enteric adenovirus types 40 and 41 in sera from people in various age groups. J Clin Microbiol 25: 1679–1682. 3654940

38. Bányai K, Martella V, Meleg E, Kisfali P, Péterfi Z, et al. (2009) Searching for HAdV-52, the putative gastroenteritis-associated human adenovirus serotype in Southern Hungary. New Microbiol 32: 185–188. 19579697

39. Song JD, Liu XL, Chen DL, Zou XH, Wang M, et al. (2012) Human adenovirus type 41 possesses different amount of short and long fibers in the virion. Virology 432: 336–342. doi: 10.1016/j.virol.2012.05.020 22727834

40. Roelvink PW, Mi Lee G, Einfeld DA, Kovesdi I, Wickham TJ (1999) Identification of a conserved receptor-binding site on the fiber proteins of CAR-recognizing adenoviridae. Science 286: 1568–1571. 10567265

41. Nilsson E, Storm RJ, Bauer J, Johansson SM, Lookene A, et al. (2011) The GD1a glycan is a cellular receptor for adenoviruses causing epidemic keratoconjunctivitis. Nat Med 17: 105–109. doi: 10.1038/nm.2267 21151139

42. Kirby I, Lord R, Davison E, Wickham TJ, Roelwink PW, et al. (2001) Adenovirus type 9 fiber knob binds to the coxsackie B virus-adenovirus receptor (CAR) with lower affinity than fiber knobs of other CAR-binding adenovirus serotypes. J Virol 75: 7210–7214. 11435605

43. Walters RW, Freimuth P, Moninger TO, Ganske I, Zabner J, et al. (2002) Adenovirus fiber disrupts CAR-mediated intercellular adhesion allowing virus escape. Cell 110: 789–799. 12297051

44. Lu ZZ, Wang H, Zhang Y, Cao H, Li Z, et al. (2013) Penton-dodecahedral particles trigger opening of intercellular junctions and facilitate viral spread during adenovirus serotype 3 infection of epithelial cells. PLoS Pathog Oct;9(10):e1003718. doi: 10.1371/journal.ppat.1003718 24204268

45. Walters RW, Grunst T, Bergelson JM, Finberg RW, Welsh MJ, et al. (1999) Basolateral localization of fiber receptors limits adenovirus infection from the apical surface of airway epithelia. J Biol Chem 274: 10219–10226. 10187807

46. Xia D, Henry LJ, Gerard RD, Diesenhofer J (1995) Crystal structure of the receptor-bining domain of adenovirus type 5 fiber protein at 1.7 Å resolution. Sructure 2: 7907–7915.

47. Persson BD, Reiter DM, Marttila M, Mei YF, Casasnovas JM, et al. (2007) Adenovirus type 11 binding alters the conformation of its receptor CD46. Nat Struct Mol Biol 14: 164–166. 17220899

48. Seiradake E, Cusack S (2005) Crystal structure of enteric adenovirus serotype 41 short fiber head. J Virol 79: 14088–14094. 16254343

49. Neu U, Bauer J, Stehle T (2011) Viruses and sialic acids: rules of engagement. Curr Opin Struct Biol 21: 610–618. doi: 10.1016/j.sbi.2011.08.009 21917445

50. Burmeister WP, Guilligay D, S. C, Wadell G, Arnberg N (2004) Crystal structure of species D adenovirus fiber knobs and their sialic acid binding sites. J Virol 78: 7727–7736. 15220447

51. Seiradake E, Henaff D, Wodrich H, O. B, Perreau M, et al. (2009) The cell adhesion molecule "CAR" and sialic acid on human erythrocytes influence adenovirus in vivo biodistribution. PLoS Pathog 5: e1000277. doi: 10.1371/journal.ppat.1000277 19119424

52. Seiradake E, Lortat-Jacob H, Billet O, Kremer EJ, Cusack S (2006) Structural and mutational analysis of human Ad37 and canine adenovirus 2 fiber heads in complex with the D1 domain of coxsackie and adenovirus receptor. J Biol Chem 281: 33704–33716. 16923808

53. Araki-Sasaki K, Ohasi KY, Sasabe T, Hayashi K, Watanabe H, et al. (1995) An SV-40-immortalized human corneal epithelial cell line and its characterization. Investig Ophtahlmol 36: 614–621.

54. Stanley P, Caillibot V, Siminovitch L (1975) Selection and characterization of eight phenotypically distinct lines of lectin-resistant Chinese hamster ovary cell. Cell 6: 121–128. 1182798

55. Deutscher SL, Nuwayhid N, Stanley P, Briles EI, Hirschberg CB (1984) Translocation across Golgi vesicle membranes: a CHO glycosylation mutant deficient in CMP-sialic acid transport. Cell 39: 295–299. 6498937

56. Liszewski MK, Atkinson JP (1996) Membrane cofactor protein (MCP; CD46). Isoforms differ in protection against the classical pathway of complement. J Immunol 156: 4415–4421. 8666815

57. Johansson SM, Nilsson EC, Elofsson M, Ahlskog N, Kihlberg J, et al. (2007) Multivalent sialic acid conjugates inhibit adenovirus type 37 from binding to and infecting human corneal epithelial cells. Antiviral Res 73: 92–100. 17014916

58. Wadell G, Allard A, Hierholzer JC (1999) Adenoviruses. In: Murray PR, Baron EJ, Pfaller MA, Tenover FC, Yolken RH, editors. Manual of Clinical Microbiology. 7th ed. Washington: ASM Press. pp. 970–982.

59. Mistry N, Inoue H, Jamshidi F, Storm RJ, Oberste MS, et al. (2011) Coxsackievirus A24 variant uses sialic acid-containing O-linked glycoconjugates as cellular receptors on human ocular cells. J Virol 85: 11283–11290. doi: 10.1128/JVI.05597-11 21880775

60. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9: 671–675. 22930834

61. Rofougaran R, Vodnala M, Hofer A (2006) Enzymatically active mammalian ribonucleotide reductase exists primarily as an alpha6beta2 octamer. J Biol Chem 281: 27705–27711. 16861739

62. Liu Y, Childs RA, Palma AS, Campanero-Rhodes MA, Stoll MS, et al. (2012) Neoglycolipid-based oligosaccharide microarray system: preparation of NGLs and their noncovalent immobilization on nitrocellulose-coated glass slides for microarray analyses. Methods Mol Biol 808: 117–136. doi: 10.1007/978-1-61779-373-8_8 22057521

63. Neu U, Khan ZM, Schuch B, Palma AS, Liu Y, et al. (2013) Structures of B-Lymphotropic Polyomavirus VP1 in complex with oligosaccharide ligands. PLoS Pathog 9: e1003714. doi: 10.1371/journal.ppat.1003714 24204265

64. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, et al. (2007) Phaser crystallographic software. J Appl Crystallogr 40: 658–674. 19461840

65. Adams PD, Grosse-Kunstleve RW, Hung LW, Ioerger TR, McCoy AJ, et al. (2002) PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr D Biol Crystallogr 58: 1948–1954. 12393927

66. Bricogne G. BE, Brandl M., Flensburg C., Keller P., Paciorek W., Roversi P, Sharff A., Smart O.S., Vonrhein C., Womack T.O. (2011) BUSTER version 2.10.0. Cambridge, United Kingdom: Global Phasing Ltd. doi: 10.1080/17437199.2011.587961 25473706

Štítky
Hygiena a epidemiológia Infekčné lekárstvo Laboratórium

Článok vyšiel v časopise

PLOS Pathogens


2015 Číslo 2
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#