Cross-Species Transmission of a Novel Adenovirus Associated with a Fulminant Pneumonia Outbreak in a New World Monkey Colony
Adenoviruses are DNA viruses that naturally infect many vertebrates, including humans and monkeys, and cause a wide range of clinical illnesses in humans. Infection from individual strains has conventionally been thought to be species-specific. Here we applied the Virochip, a pan-viral microarray, to identify a novel adenovirus (TMAdV, titi monkey adenovirus) as the cause of a deadly outbreak in a closed colony of New World monkeys (titi monkeys; Callicebus cupreus) at the California National Primate Research Center (CNPRC). Among 65 titi monkeys housed in a building, 23 (34%) developed upper respiratory symptoms that progressed to fulminant pneumonia and hepatitis, and 19 of 23 monkeys, or 83% of those infected, died or were humanely euthanized. Whole-genome sequencing of TMAdV revealed that this adenovirus is a new species and highly divergent, sharing <57% pairwise nucleotide identity with other adenoviruses. Cultivation of TMAdV was successful in a human A549 lung adenocarcinoma cell line, but not in primary or established monkey kidney cells. At the onset of the outbreak, the researcher in closest contact with the monkeys developed an acute respiratory illness, with symptoms persisting for 4 weeks, and had a convalescent serum sample seropositive for TMAdV. A clinically ill family member, despite having no contact with the CNPRC, also tested positive, and screening of a set of 81 random adult blood donors from the Western United States detected TMAdV-specific neutralizing antibodies in 2 individuals (2/81, or 2.5%). These findings raise the possibility of zoonotic infection by TMAdV and human-to-human transmission of the virus in the population. Given the unusually high case fatality rate from the outbreak (83%), it is unlikely that titi monkeys are the native host species for TMAdV, and the natural reservoir of the virus is still unknown. The discovery of TMAdV, a novel adenovirus with the capacity to infect both monkeys and humans, suggests that adenoviruses should be monitored closely as potential causes of cross-species outbreaks.
Vyšlo v časopise:
Cross-Species Transmission of a Novel Adenovirus Associated with a Fulminant Pneumonia Outbreak in a New World Monkey Colony. PLoS Pathog 7(7): e32767. doi:10.1371/journal.ppat.1002155
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1002155
Souhrn
Adenoviruses are DNA viruses that naturally infect many vertebrates, including humans and monkeys, and cause a wide range of clinical illnesses in humans. Infection from individual strains has conventionally been thought to be species-specific. Here we applied the Virochip, a pan-viral microarray, to identify a novel adenovirus (TMAdV, titi monkey adenovirus) as the cause of a deadly outbreak in a closed colony of New World monkeys (titi monkeys; Callicebus cupreus) at the California National Primate Research Center (CNPRC). Among 65 titi monkeys housed in a building, 23 (34%) developed upper respiratory symptoms that progressed to fulminant pneumonia and hepatitis, and 19 of 23 monkeys, or 83% of those infected, died or were humanely euthanized. Whole-genome sequencing of TMAdV revealed that this adenovirus is a new species and highly divergent, sharing <57% pairwise nucleotide identity with other adenoviruses. Cultivation of TMAdV was successful in a human A549 lung adenocarcinoma cell line, but not in primary or established monkey kidney cells. At the onset of the outbreak, the researcher in closest contact with the monkeys developed an acute respiratory illness, with symptoms persisting for 4 weeks, and had a convalescent serum sample seropositive for TMAdV. A clinically ill family member, despite having no contact with the CNPRC, also tested positive, and screening of a set of 81 random adult blood donors from the Western United States detected TMAdV-specific neutralizing antibodies in 2 individuals (2/81, or 2.5%). These findings raise the possibility of zoonotic infection by TMAdV and human-to-human transmission of the virus in the population. Given the unusually high case fatality rate from the outbreak (83%), it is unlikely that titi monkeys are the native host species for TMAdV, and the natural reservoir of the virus is still unknown. The discovery of TMAdV, a novel adenovirus with the capacity to infect both monkeys and humans, suggests that adenoviruses should be monitored closely as potential causes of cross-species outbreaks.
Zdroje
1. RobinsonCMSinghGHenquellCWalshMPPeigue-LafeuilleH 2011 Computational analysis and identification of an emergent human adenovirus pathogen implicated in a respiratory fatality. Virology 409 141 147
2. HarrachBBenkõMBothGBrownMDavisonA 2011 Family Adenoviridae. KingACarstensEAdamsMLefkowitzE Virus Taxonomy: 9th Report of the International Committee on Taxonomy of Viruses New York Elsevier
3. FoxJPHallCECooneyMK 1977 The Seattle Virus Watch. VII. Observations of adenovirus infections. Am J Epidemiol 105 362 386
4. LewisPFSchmidtMALuXErdmanDDCampbellM 2009 A community-based outbreak of severe respiratory illness caused by human adenovirus serotype 14. J Infect Dis 199 1427 1434
5. RuuskanenOMeurmanOAkusjarviG 1997 Adenoviruses. RichmanDDWhitleyRJHaydenFG Clinical Virology New York Churchill Livingstone xvi 1355
6. BanyaiKEsonaMDLiuAWangYTuX 2010 Molecular detection of novel adenoviruses in fecal specimens of captive monkeys with diarrhea in China. Vet Microbiol 142 416 419
7. RoySVandenbergheLHKryazhimskiySGrantRCalcedoR 2009 Isolation and characterization of adenoviruses persistently shed from the gastrointestinal tract of non-human primates. PLoS Pathog 5 e1000503
8. WeversDLeendertzFHScudaNBoeschCRobbinsMM 2010 A novel adenovirus of Western lowland gorillas (Gorilla gorilla gorilla). Virol J 7 303
9. TongSSinghJRuoneSHumphreyCYipCC 2010 Identification of adenoviruses in fecal specimens from wild chimpanzees (Pan trogylodytes schweinfurthii) in western Tanzania. Am J Trop Med Hyg 82 967 970
10. GhoshSSGopinathPRameshA 2006 Adenoviral vectors: a promising tool for gene therapy. Appl Biochem Biotechnol 133 9 29
11. RoweWPHartleyJW 1962 A general review of the adenoviruses. Ann N Y Acad Sci 101 466 474
12. GinsbergHSMoldawerLLSehgalPBRedingtonMKilianPL 1991 A mouse model for investigating the molecular pathogenesis of adenovirus pneumonia. Proc Natl Acad Sci U S A 88 1651 1655
13. BasnightMJrRogersNGGibbsCJJrGajdusekDC 1971 Characterization of four new adenovirus serotypes isolated from chimpanzee tissue explants. Am J Epidemiol 94 166 171
14. XiangZLiYCunAYangWEllenbergS 2006 Chimpanzee adenovirus antibodies in humans, sub-Saharan Africa. Emerg Infect Dis 12 1596 1599
15. ErschingJHernandezMICezarottoFSFerreiraJDMartinsAB 2010 Neutralizing antibodies to human and simian adenoviruses in humans and New-World monkeys. Virology 407 1 6
16. ChiuCYAlizadehAARouskinSMerkerJDYehE 2007 Diagnosis of a critical respiratory illness caused by human metapneumovirus by use of a pan-virus microarray. J Clin Microbiol 45 2340 2343
17. ChiuCYGreningerALKanadaKKwokTFischerKF 2008 Identification of cardioviruses related to Theiler's murine encephalomyelitis virus in human infections. Proc Natl Acad Sci U S A 105 14124 14129
18. ChiuCYRouskinSKoshyAUrismanAFischerK 2006 Microarray detection of human parainfluenzavirus 4 infection associated with respiratory failure in an immunocompetent adult. Clin Infect Dis 43 e71 76
19. ChiuCYUrismanAGreenhowTLRouskinSYagiS 2008 Utility of DNA microarrays for detection of viruses in acute respiratory tract infections in children. J Pediatr 153 76 83
20. UrismanAMolinaroRJFischerNPlummerSJCaseyG 2006 Identification of a novel Gammaretrovirus in prostate tumors of patients homozygous for R462Q RNASEL variant. PLoS Pathog 2 e25
21. WangDCoscoyLZylberbergMAvilaPCBousheyHA 2002 Microarray-based detection and genotyping of viral pathogens. Proc Natl Acad Sci U S A 99 15687 15692
22. WangDUrismanALiuYTSpringerMKsiazekTG 2003 Viral discovery and sequence recovery using DNA microarrays. PLoS Biol 1 E2
23. GreningerALChenECSittlerTScheinermanARoubinianN 2010 A metagenomic analysis of pandemic influenza A (2009 H1N1) infection in patients from North America. PLoS One 5 e13381
24. RotaPAObersteMSMonroeSSNixWACampagnoliR 2003 Characterization of a novel coronavirus associated with severe acute respiratory syndrome. Science 300 1394 1399
25. EchavarriaMFormanMTicehurstJDumlerJSCharacheP 1998 PCR method for detection of adenovirus in urine of healthy and human immunodeficiency virus-infected individuals. J Clin Microbiol 36 3323 3326
26. HierholzerJCHalonenPEDahlenPOBinghamPGMcDonoughMM 1993 Detection of adenovirus in clinical specimens by polymerase chain reaction and liquid-phase hybridization quantitated by time-resolved fluorometry. J Clin Microbiol 31 1886 1891
27. LeeWMGrindleKPappasTMarshallDJMoserMJ 2007 High-throughput, sensitive, and accurate multiplex PCR-microsphere flow cytometry system for large-scale comprehensive detection of respiratory viruses. J Clin Microbiol 45 2626 2634
28. XuWMcDonoughMCErdmanDD 2000 Species-specific identification of human adenoviruses by a multiplex PCR assay. J Clin Microbiol 38 4114 4120
29. MadischIHarsteGPommerHHeimA 2005 Phylogenetic analysis of the main neutralization and hemagglutination determinants of all human adenovirus prototypes as a basis for molecular classification and taxonomy. J Virol 79 15265 15276
30. EchavarriaM 2008 Adenoviruses in immunocompromised hosts. Clin Microbiol Rev 21 704 715
31. HarrachBBenkõMBothGBrownMDavisonA 2011 Family Adenoviridae. KingACarstensEAdamsMLefkowitzE Virus Taxonomy (9th Report of the International Committee on Taxonomy of Viruses) New York Elsevier
32. KajonAELuXErdmanDDLouieJSchnurrD 2010 Molecular epidemiology and brief history of emerging adenovirus 14-associated respiratory disease in the United States. J Infect Dis 202 93 103
33. WalshMPChintakuntlawarARobinsonCMMadischIHarrachB 2009 Evidence of molecular evolution driven by recombination events influencing tropism in a novel human adenovirus that causes epidemic keratoconjunctivitis. PLoS ONE 4 e5635
34. DeferCBelinMTCaillet-BoudinMLBoulangerP 1990 Human adenovirus-host cell interactions: comparative study with members of subgroups B and C. J Virol 64 3661 3673
35. WickhamTJMathiasPChereshDANemerowGR 1993 Integrins alpha v beta 3 and alpha v beta 5 promote adenovirus internalization but not virus attachment. Cell 73 309 319
36. LawLKDavidsonBL 2005 What does it take to bind CAR? Mol Ther 12 599 609
37. WuENemerowGR 2004 Virus yoga: the role of flexibility in virus host cell recognition. Trends Microbiol 12 162 169
38. PacheLVenkataramanSNemerowGRReddyVS 2008 Conservation of fiber structure and CD46 usage by subgroup B2 adenoviruses. Virology 375 573 579
39. PacheLVenkataramanSReddyVSNemerowGR 2008 Structural variations in species B adenovirus fibers impact CD46 association. J Virol 82 7923 7931
40. WuETraugerSAPacheLMullenTMvon SeggernDJ 2004 Membrane cofactor protein is a receptor for adenoviruses associated with epidemic keratoconjunctivitis. J Virol 78 3897 3905
41. CarriganDR 1997 Adenovirus infections in immunocompromised patients. Am J Med 102 71 74
42. MwendaJMNyachieoALangatDKSteeleDA 2005 Serological detection of adenoviruses in non-human primates maintained in a colony in Kenya. East Afr Med J 82 371 375
43. LesslerJReichNGBrookmeyerRPerlTMNelsonKE 2009 Incubation periods of acute respiratory viral infections: a systematic review. Lancet Infect Dis 9 291 300
44. KassSMWilliamsPMReamyBV 2007 Pleurisy. Am Fam Physician 75 1357 1364
45. CalcedoRVandenbergheLHRoySSomanathanSWangL 2009 Host immune responses to chronic adenovirus infections in human and nonhuman primates. J Virol 83 2623 2631
46. LuXErdmanDD 2006 Molecular typing of human adenoviruses by PCR and sequencing of a partial region of the hexon gene. Arch Virol 151 1587 1602
47. McCarthyTLebeckMGCapuanoAWSchnurrDPGrayGC 2009 Molecular typing of clinical adenovirus specimens by an algorithm which permits detection of adenovirus coinfections and intermediate adenovirus strains. J Clin Virol 46 80 84
48. WoodsLWSwiftPKBarrBCHorzinekMCNordhausenRW 1996 Systemic adenovirus infection associated with high mortality in mule deer (Odocoileus hemionus) in California. Vet Pathol 33 125 132
49. KovacsGMDavisonAJZakhartchoukANHarrachB 2004 Analysis of the first complete genome sequence of an Old World monkey adenovirus reveals a lineage distinct from the six human adenovirus species. J Gen Virol 85 2799 2807
50. EisenMBSpellmanPTBrownPOBotsteinD 1998 Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci U S A 95 14863 14868
51. UrismanAFischerKFChiuCYKistlerALBeckS 2005 E-Predict: a computational strategy for species identification based on observed DNA microarray hybridization patterns. Genome Biol 6 R78
52. SorberKChiuCWebsterDDimonMRubyJG 2008 The long march: a sample preparation technique that enhances contig length and coverage by high-throughput short-read sequencing. PLoS ONE 3 e3495
53. WelchTA 1984 A Technique for High-Performance Data-Compression. Computer 17 8 19
54. DrummondAAshtonBCheungMHeledJKearseM 2010 Geneious v5.3.4. Available: http://www.geneious.com
55. LiKB 2003 ClustalW-MPI: ClustalW analysis using distributed and parallel computing. Bioinformatics 19 1585 1586
56. SaitouNNeiM 1987 The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4 406 425
57. BrudnoMMaldeSPoliakovADoCBCouronneO 2003 Glocal alignment: finding rearrangements during alignment. Bioinformatics 19 Suppl 1 i54 62
58. FrazerKAPachterLPoliakovARubinEMDubchakI 2004 VISTA: computational tools for comparative genomics. Nucleic Acids Res 32 W273 279
59. RobertsonDLHahnBHSharpPM 1995 Recombination in AIDS viruses. J Mol Evol 40 249 259
Štítky
Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
PLOS Pathogens
2011 Číslo 7
- Očkování proti virové hemoragické horečce Ebola experimentální vakcínou rVSVDG-ZEBOV-GP
- Parazitičtí červi v terapii Crohnovy choroby a dalších zánětlivých autoimunitních onemocnění
- Koronavirus hýbe světem: Víte jak se chránit a jak postupovat v případě podezření?
Najčítanejšie v tomto čísle
- Requires Glycerol for Maximum Fitness During The Tick Phase of the Enzootic Cycle
- Comparative Genomics Yields Insights into Niche Adaptation of Plant Vascular Wilt Pathogens
- The Role of IL-15 Deficiency in the Pathogenesis of Virus-Induced Asthma Exacerbations
- “Persisters”: Survival at the Cellular Level