Acute respiratory viral infections in monkeys

封面

如何引用文章

全文:

详细

Acute respiratory viral infections (ARVI) are one of the most significant infections affecting the breeding of monkeys, especially among imported and captive primates. Respiratory diseases are also an important cause of morbidity and mortality in wild populations, and most of these infections can affect humans. Many anthropoid species, including apes, are susceptible to ARVI. Outbreaks of spontaneous respiratory infections have been described in many zoos and primatological centers around the world. Moreover, the study of spontaneous and experimental infection in laboratory primates provides an invaluable source of information on the biology and pathogenesis of ARVI and remains an indispensable tool for testing vaccines and drugs. The aim of this literature review was to summarize and analyze published data on the circulation of ARVI causative agents (parainfluenza viruses, adenoviruses, respiratory syncytial virus, influenza viruses, rhinoviruses, coronaviruses, metapneumoviruses, bocaviruses) among wild and captive primates, as well as the results of experimental modeling these infections in monkeys.

关键词

作者简介

Dmitry Dogadov

Kurchatov Complex of Medical Primatology of NRC «Kurchatov Institute»

编辑信件的主要联系方式.
Email: dima_loko86@mail.ru
ORCID iD: 0000-0003-1596-0509

Ph.D. (Biol.), Head of the Laboratory of Infection Virology of Kurchatov Complex of Medical Primatology

俄罗斯联邦, 354376, Sochi

Karen Kyuregyan

Central Research Institute of Epidemiology of the Federal Service for Surveillance on Consumer Rights Protection and Human Wellbeing; I.I. Mechnikov Research Institute of Vaccines and Sera; Russian Medical Academy of Continuous Professional Education of the Ministry of Health of Russia

Email: karen-kyuregyan@yandex.ru
ORCID iD: 0000-0002-3599-117X

D.Sci. (Biol.), Professor of the RAS, Head of the Laboratory of Molecular Epidemiology of Viral Hepatitis Central Research Institute of Epidemiology of the Federal Service for Surveillance on Consumer Rights Protection and Human Wellbeing, Leading Researcher at the Laboratory of Viral Hepatitis, I.I. Mechnikov Research Institute of Vaccines and Sera

俄罗斯联邦, 111123, Moscow; 105064, Moscow; 125993, Moscow

Albert Minosyan

Kurchatov Complex of Medical Primatology of NRC «Kurchatov Institute»

Email: malbert97@bk.ru
ORCID iD: 0009-0007-6459-1451

research laboratory assistant at the Laboratory of Infection Virology

俄罗斯联邦, 354376, Sochi

Aleksandra Goncharenko

Kurchatov Complex of Medical Primatology of NRC «Kurchatov Institute»

Email: morgan_123@rambler.ru
ORCID iD: 0000-0002-6979-9784

researcher at the Laboratory of Infection Virology, Kurchatov Complex of Medical Primatology

俄罗斯联邦, 354376, Sochi

Elena Shmat

Sochi Institute (branch) of the Federal State Autonomous Educational Institution of Higher Education Peoples’ Friendship University of Russia named after Patrice Lumumba

Email: shmatlena@mail.ru
ORCID iD: 0009-0007-0610-7131

Ph.D. (Tech.), Associate Professor, Head of the Department of Veterinary Medicine and Veterinary-Sanitary Expertise

俄罗斯联邦, 354348, Sochi

Mikhail Mikhailov

Central Research Institute of Epidemiology of the Federal Service for Surveillance on Consumer Rights Protection and Human Wellbeing; I.I. Mechnikov Research Institute of Vaccines and Sera

Email: michmich2@yandex.ru
ORCID iD: 0000-0002-6636-6801

D.Sci. (Biol.), Professor, Academician of RAS, Chief Researcher at the Laboratory of Molecular Epidemiology of Viral Hepatitis Central Research Institute of Epidemiology of the Federal Service for Surveillance on Consumer Rights Protection and Human Wellbeing, Head of the Laboratory of Viral Hepatitis, I.I. Mechnikov Research Institute of Vaccines and Sera

俄罗斯联邦, 111123, Moscow; 105064, Moscow

参考

  1. Peltola V., Ruuskanen O. Editorial commentary: Respiratory viral infections in developing countries: common, severe, and unrecognized. Clin. Infect. Dis. 2008; 46(1): 58–60. https://doi.org/10.1086/524020
  2. Lemaitre J., Naninck T., Delache B., Creppy J., Huber P., Holzapfel M., et al. Non-human primate models of human respiratory infections. Mol. Immunol. 2021; 135: 147–64. https://doi.org/10.1016/j.molimm.2021.04.010
  3. Ponezheva Zh.B., Nikolaeva S.V., Turapova A.N., Gorelov A.V. Topical problems of respiratory infections. Epidemiologiya i infektsionnye bolezni. Aktual’nye voprosy. 2023; 13(2): 51–5. https://doi.org/10.18565/epidem.2023.13.2.51-5 https://elibrary.ru/iermkv (in Russian)
  4. Lowenstine L.J., Osborn K.J. Respiratory system diseases of nonhuman primates. In: Nonhuman Primates in Biomedical Research. Elsevier; 2012: 413–81. https://doi.org/10.1016/B978-0-12-381366-4.00009-2
  5. Sasaki M., Ishii A., Orba Y., Thomas Y., Hang’ombe B.M., Moonga L., et al. Human parainfluenza virus type 3 in wild nonhuman primates, Zambia. Emerg. Infect. Dis. 2013; 19(9): 1500–3. https://doi.org/10.3201/eid1909.121404
  6. Henrickson K.J. Parainfluenza viruses. Clin. Microbiol. Rev. 2003; 16(2): 242–64. https://doi.org/10.1128/CMR.16.2.242-264.2003
  7. Skiadopoulos M.H., Surman S.R., Riggs J.M., Elkins W.R., Claire M.S., Nishio M., et al. Sendai virus, a murine parainfluenza virus type 1, replicates to a level similar to human PIV1 in the upper and lower respiratory tract of African green monkeys and chimpanzees. Virology. 2002; 297(1): 153–60. https://doi.org/10.1006/viro.2002.1416
  8. Kalter S.S., Heberling R.L., Cooke A.W., Barry J.D., Tian P.Y., Northam W.J. Viral infections of nonhuman primates. Lab. Anim. Sci. 1997; 47(5): 461–7.
  9. Korzaya L.I., Dogadov D.I., Goncharenko A.M., Karlsen A.A., Kyuregyan K.K., Mikhailov M.I. Prevalence of laboratory markers of human respiratory viruses in monkeys of Adler primate center. Voprosy virusologii. 2022; 66(6): 425–33. https://doi.org/10.36233/0507-4088-77 https://elibrary.ru/cbntjh (in Russian)
  10. Dogadov D.I., Kyuregyan K.K., Alexandra G.M., Minosyan A.A., Kochkonyan A.A., Karlsen A.A., et al. Markers of antroponotic viral infections in vervet monkeys arrived from their natural habitat (Tanzania). Voprosy virusologii. 2023; 68(5): 394–403. https://doi.org/10.36233/0507-4088-188 https://elibrary.ru/awajxs (in Russian)
  11. Jones-Engel L., Engel G.A., Schillaci M.A., Babo R., Froehlich J. Detection of antibodies to selected human pathogens among wild and pet macaques (Macaca tonkeana) in Sulawesi, Indonesia. Am. J. Primatol. 2001; 54(3): 171–8. https://doi.org/10.1002/ajp.1021
  12. Bailly J.E., McAuliffe J.M., Durbin A.P., Elkins W.R., Collins P.L., Murphy B.R. A recombinant human parainfluenza virus type 3 (PIV3) in which the nucleocapsid N protein has been replaced by that of bovine PIV3 is attenuated in primates. J. Virol. 2000; 74(7): 3188–95. https://doi.org/10.1128/jvi.74.7.3188-3195.2000
  13. Zhan X., Slobod K.S., Jones B.G., Sealy R.E., Takimoto T., Boyd K., et al. Sendai virus recombinant vaccine expressing a secreted, unconstrained respiratory syncytial virus fusion protein protects against RSV in cotton rats. Int. Immunol. 2015; 27(5): 229–36. https://doi.org/10.1093/intimm/dxu107
  14. Hawthorne J.D., Lorenz D., Albrecht P. Infection of marmosets with parainfluenza virus types 1 and 3. Infect. Immun. 1982; 37(3): 1037–41. https://doi.org/10.1128/iai.37.3.1037-1041.1982
  15. Rijsbergen L. C., Schmitz K.S., Begeman L., Drew-Bear J., Gommers L., Lamers M.M., et al. Modeling infection and tropism of human parainfluenza virus type 3 in ferrets. mBio. 2021; 13(1): e0383121. https://doi.org/10.1128/mbio.03831-21.
  16. Mutanda L.N., Mufson M.A. Antibodies to viruses of human origin in monkeys from Uganda. Proc. Soc. Exp. Biol. Med. 1974; 145(3): 1069–73. https://doi.org/10.3181/00379727-145-37955
  17. Schillaci M.A., Jones-Engel L., Engel G.A., Kyes R.C. Exposure to human respiratory viruses among urban performing monkeys in Indonesia. Am. J. Trop. Med. Hyg. 2006; 75(4): 716–9.
  18. Dogadov D.I., Korzaya L.I., Kyuregyan K.K., Karlsen A.A., Mikhailov M.I. Markers of viral hepatitis E (Hepeviridae, Orthohepevirus, Orthohepevirus A) in the imported Old World monkeys. Voprosy virusologii. 2021; 66(3): 182–8. https://doi.org/10.36233/0507-4088-34 https://elibrary.ru/xvmkmz (in Russian)
  19. Durbin A. African green monkeys provide a useful nonhuman primate model for the study of human parainfluenza virus types-1, -2, and -3 infection. Vaccine. 2000; 18(22): 2462–9. https://doi.org/10.1016/S0264-410X(99)00575-7
  20. Korzaya L.I., Keburiya V.V., Goncharenko A.M., Dogadov D.I., Lapin B.A. Markers of laboratory primates’ viral infections. In: Materials of the 2nd International Scientific Conference «Fundamental and Applied Aspects of Medical Primatology» [Materialy vtoroi mezhdunarodnoi nauchnoi konferentsii «Fundamental’nye i prikladnye aspekty meditsinskoi primatologii»]. Sochi; 2011: 79–88. https://elibrary.ru/xwiobb (in Russian)
  21. Churchill A.E. The isolation of parainfluenza 3 virus from fatal cases of pneumonia in erythrocebus patas monkeys. Br. J. Exp. Pathol. 1963; 44(5): 529–37.
  22. Hawthorne J.D., Albrecht P. Sensitive plaque neutralization assay for parainfluenza virus types 1, 2, and 3 and respiratory syncytial virus. J. Clin. Microbiol. 1981; 13(4): 730–7. https://doi.org/10.1128/jcm.13.4.730-737.1981
  23. Komada H., Tsurudome M., Ueda M., Nishio M, Bando H., Ito Y. Isolation and characterization of monoclonal antibodies to human parainfluenza virus type 4 and their use in revealing antigenic relation between subtypes 4A and 4B. Virology. 1989; 171(1): 28–37. https://doi.org/10.1016/0042-6822(89)90507-2
  24. King A.M.Q., Adams M.J., Carstens E.B., Lefkowitz E.J. Virus taxonomy: classification and nomenclature of viruses. In: Ninth Report of the International Committee on Taxonomy of Viruses. Amsterdam: Elsevier; 2012.
  25. Lukashok S.A., Horwitz M.S. New perspectives in adenoviruses. Curr. Clin. Top. Infect. Dis. 1998; 18: 286–305.
  26. Benkő M., Aoki K., Arnberg N., Davison A.J., Echavarría M., Hess M., et al. ICTV virus taxonomy profile: adenoviridae 2022. J. Gen. Virol. 2022; 103(3): 001721. https://doi.org/10.1099/jgv.0.001721
  27. Roy S., Vandenberghe L.H., Kryazhimskiy S., Grant R., Calcedo R., Yuan X., et al. Isolation and characterization of adenoviruses persistently shed from the gastrointestinal tract of non-human primates. PLoS Pathogens. 2009; 5(7): e1000503. https://doi.org/10.1371/journal.ppat.1000503
  28. Maluquer de Motes C., Hundesa A., Almeida F.C., Bofill-Mas S., Girones R. Isolation of a novel monkey adenovirus reveals a new phylogenetic clade in the evolutionary history of simian adenoviruses. Virol. J. 2011; 8: 125. https://doi.org/10.1186/1743-422X-8-125
  29. Xiang Z., Li Y., Cun A., Yang W., Ellenberg S., Switzer W.M., et al. Chimpanzee adenovirus antibodies in humans, sub-Saharan Africa. Emerg. Infect. Dis. 2006; 12(10): 1596–9. https://doi.org/10.3201/eid1210.060078
  30. Ersching J., Hernandez M.I.M., Cezarotto F.S., Ferreira J.D.S., Martins A.B., William M., et al. Neutralizing antibodies to human and simian adenoviruses in humans and New-World monkeys. Virology. 2010; 407(1): 1–6. https://doi.org/10.1016/j.virol.2010.07.043
  31. Chiu C.Y., Yagi S., Lu X., Yu G., Chen E.C., Liu M., et al. A novel adenovirus species associated with an acute respiratory outbreak in a baboon colony and evidence of coincident human infection. mBio. 2013; 4(2): e00084-13. https://doi.org/10.1128/mBio.00084-13
  32. Chen E.C., Yagi S., Kelly K.R., Mendoza S.P., Maninger N., Rosenthal A., et al. Cross-species transmission of a novel adenovirus associated with a fulminant pneumonia outbreak in a New World monkey colony. PLoS Pathogens. 2011; 7(8): e1002155. https://doi.org/10.1371/journal.ppat.1002155
  33. Yu G., Yagi S., Carrion R., Chen E.C., Liu M., Brasky K.M., et al. Experimental cross-species infection of common marmosets by titi monkey adenovirus. PLoS One. 2013; 8(7): e68558. https://doi.org/10.1371/journal.pone.0068558
  34. Babkin I.V., Tyumentsev A.I., Tikunov A.Yu., Kurilshikov A.M., Ryabchikova E.I., Zhirakovskaya E.V., et al. Evolutionary time-scale of primate bocaviruses. Infect. Gen. Evol. 2013; 14: 265–74. https://doi.org/10.1016/j.meegid.2012.12.023
  35. Sharp C.P., LeBreton M., Kantola K., Nana A., Le Doux Diffo J., Djoko C.F., et al. Widespread infection with homologues of human parvoviruses B19, PARV4, and human bocavirus of chimpanzees and gorillas in the wild. J. Virol. 2010; 84(19): 10289–96. https://doi.org/10.1128/JVI.01304-10
  36. Kumakamba C., Lukusa I.N., Kingebeni P.M., N’Kawa F., Losoma J.A., Mulembakani P.M., et al. DNA indicative of human bocaviruses detected in non-human primates in the Democratic Republic of the Congo. J. Gen. Virol. 2018; 99(5): 676–81. https://doi.org/10.1099/jgv.0.001048
  37. Morris, J. A., R. E. Blount, and R. E. Savage. 1956. Recovery of Cytopathogenic Agent from Chimpanzees with Goryza. Experimental Biology and Medicine 92: 544–549. https://doi.org/10.3181/00379727-92-22538.
  38. Clarke C.J., Watt N.J., Meredith A., McIntyre N., Burns S.M. Respiratory syncytial virus-associated bronchopneumonia in a young chimpanzee. J. Comp. Pathol. 1994; 110(2): 207–12. https://doi.org/10.1016/s0021-9975(08)80191-0
  39. Belshe R.B., Richardson L.S., London W.T., Sly D.L., Lorfeld J.H., Camargo E., et al. Experimental respiratory syncytial virus infection of four species of primates. J. Med. Virol. 1977; 1(3): 157–62. https://doi.org/10.1002/jmv.1890010302
  40. Weltzin R., Traina-Dorge V., Soike K., Zhang J.Y., Mack P., Soman G., et al. Intranasal monoclonal IgA antibody to respiratory syncytial virus protects rhesus monkeys against upper and lower respiratory tract infection. J. Infect. Dis. 1996; 174(2): 256–61. https://doi.org/10.1093/infdis/174.2.256
  41. Simoes E.A., Hayward A.R., Ponnuraj E.M., Straumanis J.P., Stenmark K.R., Wilson H.L., et al. Respiratory syncytial virus infects the Bonnet monkey, Macaca radiata. Pediatr. Dev. Pathol. 1999; 2(4): 316–26. https://doi.org/10.1007/s100249900129
  42. McArthur-Vaughan K., Gershwin L.J. A rhesus monkey model of respiratory syncytial virus infection. J. Med. Primatol. 2002; 31(2): 61–73. https://doi.org/10.1034/j.1600-0684.2002.01006.x
  43. Ponnuraj E.M., Hayward A.R., Raj A., Wilson H., Simoes E.A.F. Increased replication of respiratory syncytial virus (RSV) in pulmonary infiltrates is associated with enhanced histopathological disease in bonnet monkeys (Macaca radiata) pre-immunized with a formalin-inactivated RSV vaccine. J. Gen. Virol. 2001; 82(Pt. 11): 2663–74. https://doi.org/10.1099/0022-1317-82-11-2663
  44. Kakuk T.J., Soike K., Brideau R.J., Zaya R.M., Cole S.L., Zhang J.Y., et al. A human respiratory syncytial virus (RSV) primate model of enhanced pulmonary pathology induced with a formalin-inactivated RSV vaccine but not a recombinant FG subunit vaccine. J. Infect. Dis. 1993; 167(3): 553–61. https://doi.org/10.1093/infdis/167.3.553
  45. Papin J.F., Wolf R.F., Kosanke S.D., Jenkins J.D., Moore S.N., Anderson M.P., et al. Infant baboons infected with respiratory syncytial virus develop clinical and pathological changes that parallel those of human infants. Am. J. Physiol. Lung. Cell Mol. Physiol. 2013; 304(8): L530–9. https://doi.org/10.1152/ajplung.00173.2012
  46. Richardson L.S., Belshe R.B., Sly D.L., London W.T., Prevar D.A., Camargo E., et al. Experimental respiratory syncytial virus pneumonia in cebus monkeys. J. Med. Virol. 1978; 2(1): 45–59. https://doi.org/10.1002/jmv.1890020108
  47. Koff W.C., Caplan F.R., Case S., Halstead S.B. Cell-mediated immune response to respiratory syncytial virus infection in owl monkeys. Clin. Exp. Immunol. 1983; 53(2): 272–80.
  48. Taylor G. Animal models of respiratory syncytial virus infection. Vaccine. 2017; 35(3): 469–80. https://doi.org/10.1016/j.vaccine.2016.11.054
  49. Crowe J.E., Collins P.L., London W.T., Chanock R.M., Murphy B.R. A comparison in chimpanzees of the immunogenicity and efficacy of live attenuated respiratory syncytial virus (RSV) temperature-sensitive mutant vaccines and vaccinia virus recombinants that express the surface glycoproteins of RSV. Vaccine. 1993; 11(14): 1395–404. https://doi.org/10.1016/0264-410X(93)90168-W
  50. Crowe Jr J.E, Bui P., Davis A., Chanock R., Murphy B. A further attenuated derivative of a cold-passaged temperature-sensitive mutant of human respiratory syncytial virus retains immunogenicity and protective efficacy against wild-type challenge in seronegative chimpanzees. Vaccine. 1994; 12(9): 783–90. https://doi.org/10.1016/0264-410X(94)90286-0
  51. Jin H., Cheng X., Traina-Dorge V.L., Park H.J., Zhou H., Soike K., et al. Evaluation of recombinant respiratory syncytial virus gene deletion mutants in African green monkeys for their potential as live attenuated vaccine candidates. Vaccine. 2003; 21(25-26): 3647–52. https://doi.org/10.1016/S0264-410X(03)00426-2
  52. Le Nouën C., Brock L.G., Luongo C., McCarty T., Yang L., Mehedi M., et al. Attenuation of human respiratory syncytial virus by genome-scale codon-pair deoptimization. Proc. Natl. Acad. Sci. USA. 2014; 111(36): 13169–74. https://doi.org/10.1073/pnas.1411290111
  53. Jones B.G., Sealy R.E., Rudraraju R., Traina-Dorge V.L., Finneyfrock B., Cook A., et al. Sendai virus-based RSV vaccine protects African green monkeys from RSV infection. Vaccine. 2012; 30(5): 959–68. https://doi.org/10.1016/j.vaccine.2011.11.046
  54. Tang R.S., MacPhail M., Schickli J.H., Kaur J., Robinson C.L., Lawlor H.A., et al. Parainfluenza virus type 3 expressing the native or soluble fusion (F) Protein of Respiratory Syncytial Virus (RSV) confers protection from RSV infection in African green monkeys. J. Virol. 2004; 78(20): 11198–207. https://doi.org/10.1128/JVI.78.20.11198-11207.2004
  55. Eyles J.E., Johnson J.E., Megati S., Roopchand V., Cockle P.J., Weeratna R., et al. Nonreplicating vaccines can protect African green monkeys from the Memphis 37 strain of respiratory syncytial virus. J. Infect. Dis. 2013; 208(2): 319–29. https://doi.org/10.1093/infdis/jit169
  56. Bates J.T., Pickens J.A., Schuster J.E., Johnson M., Tollefson S.J., Williams J.V., et al. Immunogenicity and efficacy of alphavirus-derived replicon vaccines for respiratory syncytial virus and human metapneumovirus in nonhuman primates. Vaccine. 2017; 34(7): 950–6. https://doi.org/10.1016/j.vaccine.2015.12.045
  57. De Swart R.L., Kuiken T., Timmerman H.H., van Amerongen G., Van Den Hoogen B.G., Vos H.W., et al. Immunization of macaques with formalin-inactivated respiratory syncytial virus (RSV) induces interleukin-13-associated hypersensitivity to subsequent RSV infection. J. Virol. 2002; 76(22): 11561–9. https://doi.org/10.1128/jvi.76.22.11561-11569.2002
  58. Richardson L.S., Belshe R.B., London W.T., Sly D.L., Prevar D.A., Camargo E., et al. Evaluation of five temperature-sensitive mutants of respiratory syncytial virus in primates: I. Viral shedding, immunologic response, and associated illness. J. Med. Virol. 1978; 3(2): 91–100. https://doi.org/10.1002/jmv.1890030202
  59. Philippot Q., Rammaert B., Dauriat G., Daubin C., Schlemmer F., Costantini A., et al. 2024. Human metapneumovirus infection is associated with a substantial morbidity and mortality burden in adult inpatients. Heliyon. 2024; 10(13): e33231. https://doi.org/10.1016/j.heliyon.2024.e33231
  60. De Graaf M., Osterhaus A.D.M.E., Fouchier R.A.M., Holmes E.C. Evolutionary dynamics of human and avian metapneumoviruses. J. Gen. Virol. 2008; 89(12): 2933–42. https://doi.org/10.1099/vir.0.2008/006957-0
  61. Buitendijk H., Fagrouch Z., Niphuis H., Bogers W., Warren K., Verschoor E. Retrospective serology study of respiratory virus infections in captive great Apes. Viruses. 2014; 6(3): 1442–53. https://doi.org/10.3390/v6031442
  62. Köndgen S., Kühl H., N’Goran P.K., Walsh P.D., Schenk S., Ernst N., et al. Pandemic Human viruses cause decline of endangered great Apes. Curr. Biol. 2008; 18(4): 260–4. https://doi.org/10.1016/j.cub.2008.01.012
  63. Kaur T., Singh J., Tong S., Humphrey C., Clevenger D., Tan W., et al. Descriptive epidemiology of fatal respiratory outbreaks and detection of a human-related metapneumovirus in wild chimpanzees (Pan troglodytes) at Mahale Mountains National Park, Western Tanzania. Am. J. Primatol. 2008; 70(8): 755–65. https://doi.org/10.1002/ajp.20565
  64. Palacios G., Lowenstine L.J., Cranfield M.R., Gilardi K.V.K., Spelman L., Lukasik-Braum M. Human metapneumovirus infection in wild mountain gorillas, Rwanda. Emerg. Infect. Dis. 2011; 17(4): 711–3. https://doi.org/10.3201/eid1704.100883
  65. Slater O.M., Terio K.A., Zhang Y., Erdman D.D., Schneider E., Kuypers J.M., et al. Human metapneumovirus infection in chimpanzees, United States. Emerg. Infect. Dis. 2014; 20(12): 2115–8. https://doi.org/10.3201/eid2012.140408
  66. Skiadopoulos M.H., Biacchesi S., Buchholz U.J., Riggs J.M., Surman S.R., Amaro-Carambot E., et al. The two major human metapneumovirus genetic lineages are highly related antigenically, and the fusion (f) protein is a major contributor to this antigenic relatedness. J. Virol. 2004; 78(13): 6927–37. https://doi.org/10.1128/JVI.78.13.6927-6937.2004
  67. Kuiken T., Van Den Hoogen B.G., Van Riel D.A.J., Laman J.D., Van Amerongen G., Sprong L., et al. Experimental human metapneumovirus infection of cynomolgus macaques (Macaca fascicularis) results in virus replication in ciliated epithelial cells and pneumocytes with associated lesions throughout the respiratory tract. Am. J. Pathol. 2004; 164(6): 1893–900. https://doi.org/10.1016/S0002-9440(10)63750-9
  68. MacPhail M., Schickli J.H., Tang R.S., Kaur J., Robinson C., Fouchier R.A.M. Identification of small-animal and primate models for evaluation of vaccine candidates for human metapneumovirus (hMPV) and implications for hMPV vaccine design. J. Gen. Virol. 2004; 85(6): 1655–63. https://doi.org/10.1099/vir.0.79805-0
  69. Schildgen O., Simon A., Williams J. Animal models for human Metapneumovirus (HMPV) infections. Vet. Res. 2007; 38(1): 117–26. https://doi.org/10.1051/vetres:2006051
  70. Thompson I.M., Goodman P.J., Tangen C.M., Lucia M.S., Miller G.J., Ford L.G., et al. The influence of finasteride on the development of prostate cancer. N. Engl. J. Med. 2003; 349(3): 215–24. https://doi.org/10.1056/NEJMoa030660
  71. O’Brien T.C., Tauraso N.M. Antibodies to type A influenza viruses in sera from nonhuman primates. Arch. Gesamte. Virusforsch. 1973; 40(3): 359–65. https://doi.org/10.1007/BF01242556
  72. Karlsson E.A., Engel G.A., Feeroz M.M., San S., Rompis A., Lee B.P., et al. Influenza virus infection in nonhuman primates. Emerg. Infect. Dis. 2012; 18(10): 1672–5. https://doi.org/10.3201/eid1810.120214
  73. Bodewes R., Rimmelzwaan G.F., Osterhaus A.D. Animal models for the preclinical evaluation of candidate influenza vaccines. Expert. Rev. Vaccines. 2010; 9(1): 59–72. https://doi.org/10.1586/erv.09.148
  74. Baskin C.R., Bielefeldt-Ohmann H., Tumpey T.M., Sabourin P.J., Long J.P., García-Sastre A., et al. Early and sustained innate immune response defines pathology and death in nonhuman primates infected by highly pathogenic influenza virus. Proc. Natl. Acad. Sci. USA. 2009; 106(9): 3455–60. https://doi.org/10.1073/pnas.0813234106
  75. Baskin C.R., García-Sastre A., Tumpey T.M., Bielefeldt-Ohmann H., Carter V.S., Nistal-Villán E., et al. Integration of clinical data, pathology, and cDNA microarrays in influenza virus-infected pigtailed macaques (Macaca nemestrina). J. Virol. 2004; 78(19): 10420–32. https://doi.org/10.1128/JVI.78.19.10420-10432.2004
  76. Carroll T.D., Matzinger S.R., Barro M., Fritts L., McChesney M.B., Miller C.J., et al. Alphavirus replicon-based adjuvants enhance the immunogenicity and effectiveness of Fluzone® in rhesus macaques. Vaccine. 2010; 29(5): 931–40. https://doi.org/10.1016/j.vaccine.2010.11.024
  77. Chen Y., Deng W., Jia C., Dai X., Zhu H., Kong Q., et al. Pathological lesions and viral localization of influenza A (H5N1) virus in experimentally infected Chinese rhesus macaques: implications for pathogenesis and viral transmission. Arch. Virol. 2009; 154(2): 227–33. https://doi.org/10.1007/s00705-008-0277-5
  78. Shinya K., Gao Y., Cilloniz C., Suzuki Y., Fujie M., Deng G., et al. Integrated clinical, pathologic, virologic, and transcriptomic analysis of H5N1 influenza virus-induced viral pneumonia in the rhesus macaque. J. Virol. 2012; 86(11): 6055–66. https://doi.org/10.1128/JVI.00365-12
  79. Itoh Y., Ozaki H., Tsuchiya H., Okamoto K., Torii R., Sakoda Y., et al. A vaccine prepared from a non-pathogenic H5N1 avian influenza virus strain confers protective immunity against highly pathogenic avian influenza virus infection in cynomolgus macaques. Vaccine. 2008; 26(4): 562–72. https://doi.org/10.1016/j.vaccine.2007.11.031
  80. Jegaskanda S., Weinfurter J.T., Friedrich T.C., Kent S.J. Antibody-dependent cellular cytotoxicity is associated with control of pandemic H1N1 influenza virus infection of macaques. J. Virol. 2013; 87(10): 5512–22. https://doi.org/10.1128/JVI.03030-12
  81. Matzinger S.R., Carroll T.D., Fritts L., McChesney M.B., Miller C.J. Exogenous IFN-alpha administration reduces influenza a virus replication in the lower respiratory tract of rhesus macaques. PLoS One. 2011; 6(12): e29255. https://doi.org/10.1371/journal.pone.0029255
  82. Rimmelzwaan G.F., Baars M., Van Amerongen G., Van Beek R., Osterhaus A.D.M.E. A single dose of an ISCOM influenza vaccine induces long-lasting protective immunity against homologous challenge infection but fails to protect cynomolgus macaques against distant drift variants of influenza A (H3N2) viruses. Vaccine. 2001; 20(1-2): 158–63. https://doi.org/10.1016/S0264-410X(01)00262-6
  83. Rimmelzwaan G.F., Kuiken T., Van Amerongen G., Bestebroer T.M., Fouchier R.A.M., Osterhaus A.D.M.E. Pathogenesis of influenza A (H5N1) virus infection in a primate model. J. Virology. 2001; 75(14): 6687–91. https://doi.org/10.1128/JVI.75.14.6687-6691.2001
  84. Cillóniz C., Shinya K., Peng X., Korth M.J., Proll S.C., Aicher L.D., et al. Lethal influenza virus infection in macaques is associated with early dysregulation of inflammatory related genes. PLoS Pathog. 2009; 5(10): e1000604. https://doi.org/10.1371/journal.ppat.1000604
  85. Murphy B.R., Hinshaw V.S., Sly D.L., London W.T., Hosier N.T., Wood F.T., et al. Virulence of avian influenza a viruses for squirrel monkeys. Infect. Immun. 1982; 37(3): 1119–26. https://doi.org/10.1128/iai.37.3.1119-1126.1982
  86. Mooij P., Koopman G., Mortier D., van Heteren M., Oostermeijer H., Fagrouch Z., et al. Pandemic swine-origin H1N1 influenza virus replicates to higher levels and induces more fever and acute inflammatory cytokines in cynomolgus versus rhesus monkeys and can replicate in common marmosets. PloS One. 2015; 10(5): e0126132. https://doi.org/10.1371/journal.pone.0126132
  87. Jacobs S.E., Lamson D.M., George K.St., Walsh T.J. Human rhinoviruses. Clin. Microbiol. Rev. 2013; 26(1): 135–62. https://doi.org/10.1128/CMR.00077-12
  88. Negrey J.D., Reddy R.B., Scully E.J., Phillips-Garcia S., Owens L.A., Kevin E., et al. Simultaneous outbreaks of respiratory disease in wild chimpanzees caused by distinct viruses of human origin. Emerg. Microb. Infect. 2019; 8(1): 139–49. https://doi.org/10.1080/22221751.2018.1563456
  89. Pinto C.A., Haff R.F. Experimental infection of gibbons with rhinovirus. Nature. 1969; 224(526): 1310–1.
  90. Martin G.V., Heath R.B. Rhinovirus infection of vervet monkeys. Br. J. Exp. Pathol. 1969; 50(5): 516–9.
  91. V’kovski P., Kratzel A., Steiner S., Stalder H., Thiel V. Coronavirus biology and replication: implications for SARS-CoV-2. Nat. Rev. Microbiol. 2021; 19(3): 155–70. https://doi.org/10.1038/s41579-020-00468-6
  92. Goncharuk E.I., Shevtsova Z.V., Rumel’ N.B., Krylova R.I. Spontaneous coronavirus infection in monkeys. Zhurnal mikrobiologii, epidemiologii i immunobiologii. 1994; (Suppl. 1): 109–14. (in Russian)
  93. Goncharuk E.I., Shevtsova Z.V., Krylova R.I., Rumel’ N.B., Stetsenko V.I. The experimental coronavirus infection of monkeys. Mikrobiologicheskii zhurnal (Kiev). 1994; 56(3): 65–71. (in Russian)
  94. Greenough T.C., Carville A., Coderre J., Somasundaran M., Sullivan J.L., Luzuriaga K., et al. Pneumonitis and multi-organ system disease in common marmosets (Callithrix jacchus) infected with the severe acute respiratory syndrome-associated coronavirus. Am. J. Pathol. 2005; 167(2): 455–63. https://doi.org/10.1016/S0002-9440(10)62989-6
  95. McAuliffe J., Vogel L., Roberts A., Fahle G., Fischer S., Shieh W.J., et al. Replication of SARS coronavirus administered into the respiratory tract of African Green, rhesus and cynomolgus monkeys. Virology. 2004; 330(1): 8–15. https://doi.org/10.1016/j.virol.2004.09.030
  96. Qin C., Wang J., Wei Q., She M., Marasco W.A., Jiang H., et al. An animal model of SARS produced by infection of Macaca mulatta with SARS coronavirus. J. Pathol. 2005; 206(3): 251–9. https://doi.org/10.1002/path.1769
  97. Rowe T., Gao G., Hogan R.J., Crystal R.G., Voss T.G., Grant R.L., et al. Macaque model for severe acute respiratory syndrome. J. Virol. 2004; 78(20): 11401–4. https://doi.org/10.1128/JVI.78.20.11401-11404.2004
  98. Kobinger G.P., Figueredo J.M., Rowe T., Zhi Y., Gao G., Sanmiguel J.C., et al. Adenovirus-based vaccine prevents pneumonia in ferrets challenged with the SARS coronavirus and stimulates robust immune responses in macaques. Vaccine. 2007; 25(28): 5220–31. https://doi.org/10.1016/j.vaccine.2007.04.065
  99. Kuiken T., Am Fouchier R., Schutten M., Rimmelzwaan G.F., Van Amerongen G., Van Riel D., et al. Newly discovered coronavirus as the primary cause of severe acute respiratory syndrome. Lancet. 2023; 362(9380): 263–70. https://doi.org/10.1016/S0140-6736(03)13967-0
  100. Aid M., Busman-Sahay K., Vidal S.J., Maliga Z., Bondoc S., Starke C., et al. Vascular disease and thrombosis in SARS-CoV-2-infected rhesus macaques. Cell. 2020; 183(5): 1354–66.e13. https://doi.org/10.1016/j.cell.2020.10.005
  101. Blair R.V., Vaccari M., Doyle-Meyers L.A., Roy C.J., Russell-Lodrigue K., Fahlberg M., et al. Acute respiratory distress in aged, SARS-CoV-2–infected African green monkeys but not rhesus macaques. Am. J. Pathol. 2021; 191(2): 274–82. https://doi.org/10.1016/j.ajpath.2020.10.016
  102. Chandrashekar A., Liu J., Martinot A.J., McMahan K., Mercado N.B., Peter L., et al. SARS-CoV-2 infection protects against rechallenge in rhesus macaques. Science. 2020; 369(6505): 812–7. https://doi.org/10.1126/science.abc4776
  103. Deng W., Bao L., Liu J., Xiao C., Liu J., Xue J., et al. Primary exposure to SARS-CoV-2 protects against reinfection in rhesus macaques. Science. 2020; 369(6505): 818–23. https://doi.org/10.1126/science.abc5343
  104. Deng W., Bao L., Gao H., Xiang Z., Qu Y., Song Z., et al. Ocular conjunctival inoculation of SARS-CoV-2 can cause mild COVID-19 in rhesus macaques. Nat. Commun. 2020; 11(1): 4400. https://doi.org/10.1038/s41467-020-18149-6
  105. Fahlberg M.D., Blair R.V., Doyle-Meyers L.A., Midkiff C.C., Zenere G., Russell-Lodrigue K.E., et al. Cellular events of acute, resolving or progressive COVID-19 in SARS-CoV-2 infected non-human primates. Nat. Commun. 2020; 11(1): 6078. https://doi.org/10.1038/s41467-020-19967-4
  106. Koo B.S., Oh H., Kim G., Hwang E.H., Jung H., Lee Y., et al. Transient lymphopenia and interstitial pneumonia with endotheliitis in SARS-CoV-2-infected macaques. J. Infect. Dis. 2020; 222(10): 1596–600. https://doi.org/10.1093/infdis/jiaa486
  107. Lu S., Zhao Y., Yu W., Yang Y., Gao J., Wang J., et al. Comparison of nonhuman primates identified the suitable model for COVID-19. Signal. Transduct. Target. Ther. 2020; 5(1): 157. https://doi.org/10.1038/s41392-020-00269-6
  108. Munster V.J., Feldmann F., Williamson B.N., Van Doremalen N., Pérez-Pérez L., Schulz J., et al. Respiratory disease in rhesus macaques inoculated with SARS-CoV-2. Nature. 2020; 585(7824): 268–72. https://doi.org/10.1038/s41586-020-2324-7
  109. Rosa B.A., Ahmed M., Singh D.K., Choreño-Parra J.A., Cole J., Jiménez-Álvarez L.A., et al. IFN signaling and neutrophil degranulation transcriptional signatures are induced during SARS-CoV-2 infection. Commun. Biol. 2021; 4(1): 290. https://doi.org/10.1038/s42003-021-01829-4
  110. Salguero F.J., White A.D., Slack G.S., Fotheringham S.A., Bewley K.R., Gooch K.E., et al. Comparison of rhesus and cynomolgus macaques as an infection model for COVID-19. Nat. Commun. 2021; 12(1): 1260. https://doi.org/10.1038/s41467-021-21389-9
  111. Shan C., Yao Y.F., Yang XL., Zhou YW., Gao G., Peng Y., et al. Infection with novel coronavirus (SARS-CoV-2) causes pneumonia in Rhesus macaques. Cell Res. 2020; 30(8): 670–7. https://doi.org/10.1038/s41422-020-0364-z
  112. Singh D.K., Singh B., Ganatra S.R., Gazi M., Cole J., Thippeshappa R., et al. Responses to acute infection with SARS-CoV-2 in the lungs of rhesus macaques, baboons and marmosets. Nat. Microbiol. 2020; 6(1): 73–86. https://doi.org/10.1038/s41564-020-00841-4
  113. Song T.Z., Zheng H.Y., Han J.B., Jin L., Yang X., Liu F.L., et al. Delayed severe cytokine storm and immune cell infiltration in SARS-CoV-2-infected aged Chinese rhesus macaques. Zool. Res. 2020; 41(5): 503–16. https://doi.org/10.24272/j.issn.2095-8137.2020.202
  114. Yu P., Qi F., Xu Y., Li F., Liu P., Liu J., et al. Age-related rhesus macaque models of COVID-19. Animal Model Exp. Med. 2020; 3(1): 93–7. https://doi.org/10.1002/ame2.12108
  115. Zheng H., Li H., Guo L., Liang Y., Li J., Wang X., et al. Virulence and pathogenesis of SARS-CoV-2 infection in rhesus macaques: A nonhuman primate model of COVID-19 progression. PLoS Pathog. 2020; 16(11): e1008949. https://doi.org/10.1371/journal.ppat.1008949
  116. Johnston S.C., Ricks K.M., Jay A., Raymond J.L., Rossi F., Zeng X., et al. Development of a coronavirus disease 2019 nonhuman primate model using airborne exposure. PLoS One. 2021; 16(2): e0246366. https://doi.org/10.1371/journal.pone.0246366
  117. Ishigaki H., Nakayama M., Kitagawa Y., Nguyen C.T., Hayashi K., Shiohara M., et al. Neutralizing antibody-dependent and -independent immune responses against SARS-CoV-2 in cynomolgus macaques. Virology. 2021; 554: 97–105. https://doi.org/10.1016/j.virol.2020.12.013
  118. Rockx B., Kuiken T., Herfst S., Bestebroer T., Lamers M.M., Munnink B.B.O., et al. Comparative pathogenesis of COVID-19, MERS, and SARS in a nonhuman primate model. Science. 2020; 368(6494): 1012–5. https://doi.org/10.1126/science.abb7314
  119. Cross R.W., Agans K.N., Prasad A.N., Borisevich V., Woolsey C., Deer D.J., et al. Intranasal exposure of African green monkeys to SARS-CoV-2 results in acute phase pneumonia with shedding and lung injury still present in the early convalescence phase. Virol. J. 2020; 17(1): 125. https://doi.org/10.1186/s12985-020-01396-w
  120. Hartman A.L., Nambulli S., McMillen C.M., White A.G., Tilston-Lunel N.L., Albe J.R., et al. SARS-CoV-2 infection of African green monkeys results in mild respiratory disease discernible by PET/CT imaging and shedding of infectious virus from both respiratory and gastrointestinal tracts. PLoS Pathog. 2020; 16(9): e1008903. https://doi.org/10.1371/journal.ppat.1008903
  121. Speranza E., Williamson B.N., Feldmann F., Sturdevant G.L., Pérez-Pérez L., Meade-White K., et al. Single-cell RNA sequencing reveals SARS-CoV-2 infection dynamics in lungs of African green monkeys. Sci. Transl. Med. 2021; 13(578): eabe8146. https://doi.org/10.1126/scitranslmed.abe8146
  122. Woolsey C., Borisevich V., Prasad A.N., Agans K.N., Deer D.J., Dobias N.S., et al. Establishment of an African green monkey model for COVID-19 and protection against re-infection. Nat. Immunol. 2021; 22(1): 86–98. https://doi.org/10.1038/s41590-020-00835-8
  123. Erasmus J.H., Khandhar A.P., O’Connor M.A., Walls A.C., Hemann E.A., Murapa P., et al. An Alphavirus -derived replicon RNA vaccine induces SARS-CoV-2 neutralizing antibody and T cell responses in mice and nonhuman primates. Sci. Transl. Med. 2020; 12: eabc9396. https://doi.org/10.1126/scitranslmed.abc9396
  124. Tian J.H., Patel N., Haupt R., Zhou H., Weston S., Hammond H., et al. SARS-CoV-2 spike glycoprotein vaccine candidate NVX-CoV2373 immunogenicity in baboons and protection in mice. Nat. Commun. 2021; 12(1): 372. https://doi.org/10.1038/s41467-020-20653-8
  125. Walls A.C., Fiala B., Schäfer A., Wrenn S., Pham M.N., Murphy M., et al. Elicitation of potent neutralizing antibody responses by designed protein nanoparticle vaccines for SARS-CoV-2. Cell. 2020; 183(5): 1367–82.e17. https://doi.org/10.1016/j.cell.2020.10.043
  126. Liu Z.J., Qian X.K., Hong M.H., Zhang J.L., Li D.Y., Wang T.H., et al. Global view on virus infection in non-human primates and implications for public health and wildlife conservation. Zool. Res. 2021; 42(5): 626–32. https://doi.org/10.24272/j.issn.2095-8137.2021.080
  127. Cano-Terriza D., Beato-Benítez A., Fernández-Bastit L., Segalés J., Vergara-Alert J., Martínez-Nevado E., et al. SARS-CoV-2 in captive nonhuman primates, Spain, 2020–2023. Emerg. Infect. Dis. 2024; 30(6): 1253–7. https://doi.org/10.3201/eid3006.231247
  128. Dusseldorp F., Bruins-van-Sonsbeek L.G.R., Buskermolen M., Niphuis H., Dirven M., Whelan J., et al. SARS-CoV-2 in lions, gorillas and zookeepers in the Rotterdam Zoo, the Netherlands, a One Health investigation, November 2021. Euro Surveill. 2023; 28(28): 2200741. https://doi.org/10.2807/1560-7917.ES.2023.28.28.2200741
  129. Nagy A., Stará M., Vodička R., Černíková L., Jiřincová H., Křivda V., et al. Reverse-zoonotic transmission of SARS-CoV-2 lineage alpha (B.1.1.7) to great apes and exotic felids in a zoo in the Czech Republic. Arch. Virol. 2022; 167(8): 1681–5. https://doi.org/10.1007/s00705-022-05469-9
  130. Yaglom H.D., Roth A., Alvarez C., Corbus E., Ghai R.R., Ferguson S., et al. Detection of SARS-CoV-2 in a squirrel monkey (Saimiri sciureus): a one health investigation and response. J. Zoo Wildl. Med. 2024; 55(2): 471–8. https://doi.org/10.1638/2023-0052
  131. Carvajal M., Saenz C., Fuentes N., Guevara R., Muñoz E., Prado-Vivar B., et al. SARS-CoV-2 infection in brown-headed spider monkeys (Ateles fusciceps) at a wildlife rescue center on the coast of Ecuador-South America. Microbiol. Spectr. 2024; 12(4): e0274123. https://doi.org/10.1128/spectrum.02741-23

补充文件

附件文件
动作
1. JATS XML

版权所有 © Dogadov D.I., Kyuregyan K.K., Minosyan A.A., Goncharenko A.M., Shmat E.V., Mikhailov M.I., 2025

Creative Commons License
此作品已接受知识共享署名 4.0国际许可协议的许可

Согласие на обработку персональных данных с помощью сервиса «Яндекс.Метрика»

1. Я (далее – «Пользователь» или «Субъект персональных данных»), осуществляя использование сайта https://journals.rcsi.science/ (далее – «Сайт»), подтверждая свою полную дееспособность даю согласие на обработку персональных данных с использованием средств автоматизации Оператору - федеральному государственному бюджетному учреждению «Российский центр научной информации» (РЦНИ), далее – «Оператор», расположенному по адресу: 119991, г. Москва, Ленинский просп., д.32А, со следующими условиями.

2. Категории обрабатываемых данных: файлы «cookies» (куки-файлы). Файлы «cookie» – это небольшой текстовый файл, который веб-сервер может хранить в браузере Пользователя. Данные файлы веб-сервер загружает на устройство Пользователя при посещении им Сайта. При каждом следующем посещении Пользователем Сайта «cookie» файлы отправляются на Сайт Оператора. Данные файлы позволяют Сайту распознавать устройство Пользователя. Содержимое такого файла может как относиться, так и не относиться к персональным данным, в зависимости от того, содержит ли такой файл персональные данные или содержит обезличенные технические данные.

3. Цель обработки персональных данных: анализ пользовательской активности с помощью сервиса «Яндекс.Метрика».

4. Категории субъектов персональных данных: все Пользователи Сайта, которые дали согласие на обработку файлов «cookie».

5. Способы обработки: сбор, запись, систематизация, накопление, хранение, уточнение (обновление, изменение), извлечение, использование, передача (доступ, предоставление), блокирование, удаление, уничтожение персональных данных.

6. Срок обработки и хранения: до получения от Субъекта персональных данных требования о прекращении обработки/отзыва согласия.

7. Способ отзыва: заявление об отзыве в письменном виде путём его направления на адрес электронной почты Оператора: info@rcsi.science или путем письменного обращения по юридическому адресу: 119991, г. Москва, Ленинский просп., д.32А

8. Субъект персональных данных вправе запретить своему оборудованию прием этих данных или ограничить прием этих данных. При отказе от получения таких данных или при ограничении приема данных некоторые функции Сайта могут работать некорректно. Субъект персональных данных обязуется сам настроить свое оборудование таким способом, чтобы оно обеспечивало адекватный его желаниям режим работы и уровень защиты данных файлов «cookie», Оператор не предоставляет технологических и правовых консультаций на темы подобного характера.

9. Порядок уничтожения персональных данных при достижении цели их обработки или при наступлении иных законных оснований определяется Оператором в соответствии с законодательством Российской Федерации.

10. Я согласен/согласна квалифицировать в качестве своей простой электронной подписи под настоящим Согласием и под Политикой обработки персональных данных выполнение мною следующего действия на сайте: https://journals.rcsi.science/ нажатие мною на интерфейсе с текстом: «Сайт использует сервис «Яндекс.Метрика» (который использует файлы «cookie») на элемент с текстом «Принять и продолжить».