#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Histo-Blood Group Antigens Act as Attachment Factors of Rabbit Hemorrhagic Disease Virus Infection in a Virus Strain-Dependent Manner


Rabbit Hemorrhagic disease virus (RHDV), a calicivirus of the Lagovirus genus, and responsible for rabbit hemorrhagic disease (RHD), kills rabbits between 48 to 72 hours post infection with mortality rates as high as 50–90%. Caliciviruses, including noroviruses and RHDV, have been shown to bind histo-blood group antigens (HBGA) and human non-secretor individuals lacking ABH antigens in epithelia have been found to be resistant to norovirus infection. RHDV virus-like particles have previously been shown to bind the H type 2 and A antigens. In this study we present a comprehensive assessment of the strain-specific binding patterns of different RHDV isolates to HBGAs. We characterized the HBGA expression in the duodenum of wild and domestic rabbits by mass spectrometry and relative quantification of A, B and H type 2 expression. A detailed binding analysis of a range of RHDV strains, to synthetic sugars and human red blood cells, as well as to rabbit duodenum, a likely gastrointestinal site for viral entrance was performed. Enzymatic cleavage of HBGA epitopes confirmed binding specificity. Binding was observed to blood group B, A and H type 2 epitopes in a strain-dependent manner with slight differences in specificity for A, B or H epitopes allowing RHDV strains to preferentially recognize different subgroups of animals. Strains related to the earliest described RHDV outbreak were not able to bind A, whereas all other genotypes have acquired A binding. In an experimental infection study, rabbits lacking the correct HBGA ligands were resistant to lethal RHDV infection at low challenge doses. Similarly, survivors of outbreaks in wild populations showed increased frequency of weak binding phenotypes, indicating selection for host resistance depending on the strain circulating in the population. HBGAs thus act as attachment factors facilitating infection, while their polymorphism of expression could contribute to generate genetic resistance to RHDV at the population level.


Vyšlo v časopise: Histo-Blood Group Antigens Act as Attachment Factors of Rabbit Hemorrhagic Disease Virus Infection in a Virus Strain-Dependent Manner. PLoS Pathog 7(8): e32767. doi:10.1371/journal.ppat.1002188
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1002188

Souhrn

Rabbit Hemorrhagic disease virus (RHDV), a calicivirus of the Lagovirus genus, and responsible for rabbit hemorrhagic disease (RHD), kills rabbits between 48 to 72 hours post infection with mortality rates as high as 50–90%. Caliciviruses, including noroviruses and RHDV, have been shown to bind histo-blood group antigens (HBGA) and human non-secretor individuals lacking ABH antigens in epithelia have been found to be resistant to norovirus infection. RHDV virus-like particles have previously been shown to bind the H type 2 and A antigens. In this study we present a comprehensive assessment of the strain-specific binding patterns of different RHDV isolates to HBGAs. We characterized the HBGA expression in the duodenum of wild and domestic rabbits by mass spectrometry and relative quantification of A, B and H type 2 expression. A detailed binding analysis of a range of RHDV strains, to synthetic sugars and human red blood cells, as well as to rabbit duodenum, a likely gastrointestinal site for viral entrance was performed. Enzymatic cleavage of HBGA epitopes confirmed binding specificity. Binding was observed to blood group B, A and H type 2 epitopes in a strain-dependent manner with slight differences in specificity for A, B or H epitopes allowing RHDV strains to preferentially recognize different subgroups of animals. Strains related to the earliest described RHDV outbreak were not able to bind A, whereas all other genotypes have acquired A binding. In an experimental infection study, rabbits lacking the correct HBGA ligands were resistant to lethal RHDV infection at low challenge doses. Similarly, survivors of outbreaks in wild populations showed increased frequency of weak binding phenotypes, indicating selection for host resistance depending on the strain circulating in the population. HBGAs thus act as attachment factors facilitating infection, while their polymorphism of expression could contribute to generate genetic resistance to RHDV at the population level.


Zdroje

1. MorisseJPLe GallGBoilletotE 1991 Hepatitis of viral origin in Leporidae: introduction and aetiological hypotheses. Rev Sci Tech 10 269 310

2. XuZJChenWX 1989 Viral haemorrhagic disease in rabbits: a review. Vet Res Commun 13 205 212

3. MarcatoPSBenazziCVecchiGGaleottiMDella SaldaL 1991 Clinical and pathological features of viral haemorrhagic disease of rabbits and the European brown hare syndrome. Rev Sci Tech 10 371 392

4. Turcot-DuboisALLe Moullac-VaidyeBDespiauSRoubinetFBovinN 2007 Long-term evolution of the CAZY glycosyltransferase 6 (ABO) gene family from fishes to mammals: a birth-and-death evolution model. Glycobiology 17 516 528

5. CookeBDFennerF 2002 Rabbit haemorrhagic disease and the biological control of wild rabbits, Oryctolagus cuniculus, in Australia and New Zealand. Wildl Res 29 689 706

6. Delibes-MateosMFarfanMAOliveroJMarquezALVargasJM 2009 Long-term changes in game species over a long period of transformation in the Iberian Mediterranean landscape. Environ Manage 43 1256 1268

7. MarchandeauSChavalYLe GoffE 2000 Prolonged decline in the abundance of wild European rabbits and high immunity level over three years following the arrival of rabbit haemorrhagic disease. Wildl Biol 6 141 147

8. BravoLGBelliureJRebolloS 2009 European rabbits as ecosystem engineers: warrens increase lizard density and diversity. Biodivers Conserv 18 869 885

9. PeshevRChristovaL 2003 The efficacy of a bivalent vaccine against pasteurellosis and rabbit haemorrhagic disease virus. Vet Res Commun 27 433 444

10. RodakLSmidBValicekLVeselyTStepanekJ 1990 Enzyme-linked immunosorbent assay of antibodies to rabbit haemorrhagic disease virus and determination of its major structural proteins. J Gen Virol 71 Pt 5 1075 1080

11. CapucciLFusiPLavazzaAPacciariniMLRossiC 1996 Detection and preliminary characterization of a new rabbit calicivirus related to rabbit hemorrhagic disease virus but nonpathogenic. J Virol 70 8614 8623

12. Le Gall-ReculeGZwingelsteinFFagesMPBertagnoliSGelfiJ 2011 Characterisation of a non-pathogenic and non-protective infectious rabbit lagovirus related to RHDV. Virology 410 395 402

13. StriveTWrightJDRobinsonAJ 2009 Identification and partial characterisation of a new Lagovirus in Australian wild rabbits. Virology 384 97 105

14. JahnkeMHolmesECKerrPJWrightJDStriveT 2010 Evolution and phylogeography of the nonpathogenic calicivirus RCV-A1 in wild rabbits in Australia. J Virol 84 12397 12404

15. StriveTWrightJKovaliskiJBottiGCapucciL 2010 The non-pathogenic Australian lagovirus RCV-A1 causes a prolonged infection and elicits partial cross-protection to rabbit haemorrhagic disease virus. Virology 398 125 134

16. MarchandeauSLe Gall-ReculeGBertagnoliSAubineauJBottiG 2005 Serological evidence for a non-protective RHDV-like virus. Vet Res 36 53 62

17. Le Gall-ReculeGZwingelsteinFLaurentSde BoissesonCPortejoieY 2003 Phylogenetic analysis of rabbit haemorrhagic disease virus in France between 1993 and 2000, and the characterisation of RHDV antigenic variants. Arch Virol 148 65 81

18. CapucciLFallacaraFGrazioliSLavazzaAPacciariniML 1998 A further step in the evolution of rabbit hemorrhagic disease virus: the appearance of the first consistent antigenic variant. Virus Res 58 115 126

19. MullerAFreitasJSilvaELe Gall-ReculeGZwingelsteinF 2009 Evolution of rabbit haemorrhagic disease virus (RHDV) in the European rabbit (Oryctolagus cuniculus) from the Iberian Peninsula. Vet Microbiol 135 368 373

20. KerrPJKitchenAHolmesEC 2009 Origin and phylodynamics of rabbit hemorrhagic disease virus. J Virol 83 12129 12138

21. Ruvoen-ClouetNGaniereJPAndre-FontaineGBlanchardDLe PenduJ 2000 Binding of rabbit hemorrhagic disease virus to antigens of the ABH histo-blood group family. J Virol 74 11950 11954

22. AldaFGaiteroTSuarezMMerchanTRochaG 2010 Evolutionary history and molecular epidemiology of rabbit haemorrhagic disease virus in the Iberian Peninsula and Western Europe. BMC Evol Biol 10 347

23. Niedzwiedzka-RystwejPDeptulaW 2010 Non-specific immunity in rabbits infected with 10 strains of the rabbit haemorrhagic disease virus with different biological properties. Cent Eur J Biol 5 613 632

24. BerginILWiseAGBolinSRMullaneyTPKiupelM 2009 Novel calicivirus identified in rabbits, Michigan, USA. Emerg Infect Dis 15 1955 1962

25. MitroSKraussH 1993 Rabbit hemorrhagic disease: a review with special reference to its epizootiology. Eur J Epidemiol 9 70 78

26. SurridgeAKvan der LooWAbrantesJCarneiroMHewittGM 2008 Diversity and evolutionary history of the MHC DQA gene in leporids. Immunogenetics 60 515 525

27. EstevesPJLanningDFerrandNKnightKLZhaiSK 2004 Allelic variation at the VHa locus in natural populations of rabbit (Oryctolagus cuniculus, L.). J Immunol 172 1044 1053

28. QueneyGFerrandNWeissSMougelFMonnerotM 2001 Stationary distributions of microsatellite loci between divergent population groups of the European rabbit (Oryctolagus cuniculus). Mol Biol Evol 18 2169 2178

29. BrancoMFerrandNMonnerotM 2000 Phylogeography of the European rabbit (Oryctolagus cuniculus) in the Iberian Peninsula inferred from RFLP analysis of the cytochrome b gene. Heredity 85 Pt 4 307 317

30. van der LooWMougelFBoutonCSanchezMSMonnerotM 1999 The allotypic patchwork pattern of the rabbit IGKC1 allele b5wf: genic exchange or common ancestry? Immunogenetics 49 7 14

31. TianLLiaoJLiJWZhouWRZhangXL 2007 Isolation and identification of a non-haemagglutinating strain of rabbit hemorrhagic disease virus from China and sequence analysis for the VP60 Gene. Virus Genes 35 745 752

32. OriolRDalixAM 1977 Differences in the maturation of the immune response of A- and A+ rabbits. Good and poor responders respectively for the A antigen. Immunology 33 91 99

33. BreimerMEHanssonGCKarlssonKALefflerH 1981 Blood group type glycosphingolipids from the small intestine of different animals analysed by mass spectrometry and thin-layer chromatography. A note on species diversity. J Biochem 90 589 609

34. HanssonGC 1988 Structural aspects of blood group glycosphingolipids in the gastrointestinal tract. Adv Exp Med Biol 228 465 494

35. GuillonPRuvoen-ClouetNLe Moullac-VaidyeBMarchandeauSLe PenduJ 2009 Association between expression of the H histo-blood group antigen, alpha1,2fucosyltransferases polymorphism of wild rabbits, and sensitivity to rabbit hemorrhagic disease virus. Glycobiology 19 21 28

36. TurcotALBlancherALe Moullac-VaidyeBDespiauSRocherJ 2003 Cloning of a rat gene encoding the histo-blood group B enzyme: rats have more than one Abo gene. Glycobiology 13 919 928

37. IwamotoSKumadaMKamesakiTOkudaHKajiiE 2002 Rat encodes the paralogous gene equivalent of the human histo-blood group ABO gene. J Biol Chem 277 46463 46469

38. GorvelJPRigalASarlesJMarouxS 1985 Aminopeptidase N- and human blood group A-antigenicity along the digestive tract and associated glands in the rabbit. Cell Tissue Res 239 241 248

39. AsgariSHardyJRSinclairRGCookeBD 1998 Field evidence for mechanical transmission of rabbit haemorrhagic disease virus (RHDV) by flies (Diptera:Calliphoridae) among wild rabbits in Australia. Virus Res 54 123 132

40. TeunisPFMoeCLLiuPMillerSELindesmithL 2008 Norwalk virus: how infectious is it? J Med Virol 80 1468 1476

41. MutzeGCookeBAlexanderP 1998 The initial impact of rabbit hemorrhagic disease on European rabbit populations in South Australia. J Wildl Dis 34 221 227

42. FouchetDGuittonJSMarchandeauSPontierD 2008 Impact of myxomatosis in relation to local persistence in wild rabbit populations: the role of waning immunity and the reproductive period. J Theor Biol 250 593 605

43. FouchetDMarchandeauSLanglaisMPontierD 2006 Waning of maternal immunity and the impact of diseases: the example of myxomatosis in natural rabbit populations. J Theor Biol 242 81 89

44. FouchetDLe PenduJGuittonJSGuiserixMMarchandeauS 2009 Evolution of microparasites in spatially and genetically structured host populations: the example of RHDV infecting rabbits. J Theor Biol 257 212 227

45. Le PenduJRuvoen-ClouetNKindbergESvenssonL 2006 Mendelian resistance to human norovirus infections. Semin Immunol 18 375 386

46. MarionneauSRuvoenNLe Moullac-VaidyeBClementMCailleau-ThomasA 2002 Norwalk virus binds to histo-blood group antigens present on gastroduodenal epithelial cells of secretor individuals. Gastroenterology 122 1967 1977

47. DonaldsonEFLindesmithLCLobueADBaricRS 2008 Norovirus pathogenesis: mechanisms of persistence and immune evasion in human populations. Immunol Rev 225 190 211

48. TanMJiangX 2010 Norovirus gastroenteritis, carbohydrate receptors, and animal models. PLoS Pathog 6 e1000983

49. TanMJiangX 2005 Norovirus and its histo-blood group antigen receptors: an answer to a historical puzzle. Trends Microbiol 13 285 293

50. MarionneauSCailleau-ThomasARocherJLe Moullac-VaidyeBRuvoën-clouetN 2001 ABH and Lewis histo-blood group antigens, a model for the meaning of oligosaccharide diversity in the face of a changing world. Biochimie 83 565 573

51. GlassRIParasharUDEstesMK 2009 Norovirus gastroenteritis. New Engl J Med 361 1776 1785

52. HutsonAMAiraudFLe PenduJEstesMKAtmarRL 2005 Norwalk virus infection associates with secretor status genotyped from sera. J Med Virol 77 116 120

53. LindesmithLMoeCLMarionneauSRuvoën-clouetNJiangX 2003 Human susceptibility and resistance to Norwalk virus infection. Nat Med 9 548 553

54. Le GuyaderFSKrolJAmbert-BalayKRuvöen-ClouetNDesaubliauxB 2010 Comprehensive analysis of a norovirus-associated gastroenteritis outbreak from the environment to the consumer. J Clin Microbiol 48 915 920

55. BucardoFKindbergEPaniaguaMGrahnALarsonG 2009 Genetic susceptibility to symtomatic norovirus infection in Nicaragua. J Med Virol 81 728 735

56. TanMJinMXieHDuanZJiangX 2008 Outbreak studies of a GII-3 and a GII.4 norovirus revealed an association between HBGA phenotypes and viral infection. J Med Virol 80 1296 1301

57. KindbergEAkerlindBJohnsenCKnudsenJDHeltbergO 2007 Host genetic resistance to symptomatic norovirus (GGII.4) infections in Denmark. J Clin Microbiol 45 2720 2722

58. ThorvenMGrahnAHedlundK-OJohanssonHWahlfridC 2005 A homozygous nonsense mutation (428G>A) in the human FUT2 gene provides resistance to symptomatic norovirus (GGII) infections. J Virol 79 15351 15355

59. DonaldsonEFLindesmithLLoBueADBaricRS 2010 Viral shape-shifting: norovirus evasion of the human immune system. Nat Rev Microbiol 8 231 240

60. TanMJiangX 2007 Norovirus-host interaction: implications for disease control and prevention. Expert Rev Mol Med 9 1 22

61. SilvaLMCarvalhoASGuillonPSeixasSAzevedoM 2010 Infection-associated FUT2 (fucosyltransferase 2) genetic variation and impact on functionality assessed by in vivo studies. Glycoconj J 27 61 68

62. Ferrer-AdmetllaASikoraMLaayouniHEsteveARoubinetF 2009 A natural history of FUT2 polymorphism in humans. Mol Biol Evol 26 1993 2003

63. FryAEGriffithsMJAuburnSDiakiteMFortonJT 2008 Common variation in the ABO glycosyltransferase is associated with susceptibility to severe Plasmodium falciparum malaria. Hum Mol Genet 17 567 576

64. CalafellFRoubinetFRamirez-SorianoASaitouNBertanpetitJ 2008 Evolutionary dynamics of the human ABO gene. Hum Genet 124 123 135

65. KodaYTachidaHWangHLiuYSoejimaM 2001 Contrasting patterns of polymorphisms at the ABO-secretor gene (FUT2) and plasma α(1,3)fucosyltrasnferase gene (FUT6) in human populations. Genetics 158 747 756

66. AbrantesJPosadaDGuillonPEstevesPJLe PenduJ 2009 Widespread gene conversion of alpha-2-fucosyltransferase genes in mammals. J Mol Evol 69 22 31

67. NeiMRooneyAP 2005 Concerted and birth-and-death evolution of multigene families. Annu Rev Genet 39 121 152

68. Le PenduJLe CabellecMBaraJ 1997 Immunohistological analysis of antibodies against ABH and other glycoconjugates in normal human pyloric and duodenal mucosae. Transfus Clin Biol 1 41 46

69. Le PenduJHenryS 2002 Immunochemical, immunohistological and serological analysis of monoclonal antibodies with carbohydrates: Coordinator's report. Transfus Clin Biol 9 55 60

70. McIntoshMTBehanSCMohamedFMLuZMoranKE 2007 A pandemic strain of calicivirus threatens rabbit industries in the Americas. Virol J 4 96

71. Sutton-SmithMDellA 2006 Analysis of carbohydrates/glycoproteins by mass spectrometry. CelisJE Cell Biology: A Laboratory Handbook. San Diego Elsevier Academic Press 415 425 In:

72. ParrySLedgerVTissotBHaslamSMScottJ 2007 Integrated mass spectrometric strategy for characterizing the glycans from glycosphingolipids and glycoproteins: direct identification of sialyl Le(x) in mice. Glycobiology 17 646 654

73. NorthSJJang-LeeJHarrisonRCanisKIsmailMN 2010 Mass spectrometric analysis of mutant mice. Methods Enzymol 478 27 77

74. DellA 1990 Preparation and desorption mass spectrometry of permethyl and peracetyl derivatives of oligosaccarides. Methods Enzymol 193 647 660

75. CeroniAMaassKGeyerHGeyerRDellA 2008 GlycoWorkbench: a tool for the computer-assisted annotation of mass spectra of glycans. J Proteome Res 7 1650 1659

76. AbrantesJEstevesPJvan der LooW 2008 Evidence for recombination in the major capsid gene VP60 of the rabbit haemorrhagic disease virus (RHDV). Arch Virol 153 329 335

77. ForresterNLMossSRTurnerSLSchirrmeierHGouldEA 2008 Recombination in rabbit haemorrhagic disease virus: Possible impact on evolution and epidemiology. Virology 376 390 396

78. MartinDPLemeyPLottMMoultonVPosadaD 2010 RDP3: a flexible and fast computer program for analyzing recombination. Bioinformatics 26 2462 2463

79. SaitouNNeiM 1987 The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4 406 425

80. TamuraKDudleyJNeiMKumarS 2007 MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24 1596 1599

81. ZwicklDJ 2006 Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. Austin, Texas University of Texas at Austin 125

Štítky
Hygiena a epidemiológia Infekčné lekárstvo Laboratórium

Článok vyšiel v časopise

PLOS Pathogens


2011 Číslo 8
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Aktuální možnosti diagnostiky a léčby litiáz
nový kurz
Autori: MUDr. Tomáš Ürge, PhD.

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#