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Abstract

Adenoviruses are a frequent cause of acute upper respiratory tract infections that can also cause disseminated disease in immunosuppressed patients. We identified a novel adenovirus, squirrel monkey adenovirus 1 (SqMAdV-1), as the cause of fatal infection in an immunocompromised squirrel monkey () at the Keeling Center for Comparative Medicine and Research (KCCMR). Sequencing of SqMAdV-1 revealed that it is most closely related (80.4 % pairwise nucleotide identity) to the titi monkey () adenovirus (TMAdV). Although identified in the titi monkey, TMAdV is highly lethal in these monkeys, and they are not thought to be the natural host. While SqMAdV-1 is similar to other primate adenoviruses in size and genomic characteristics, a nucleotide polymorphism at the expected stop codon of the DNA polymerase gene results in a 126 amino acid extension at the carboxy terminus, a feature not previously observed among other primate adenoviruses. PCR testing and partial sequencing of 95 archived faecal samples from other squirrel monkeys ( and ) housed at the KCCMR revealed the presence of three distinct, and apparently endemic species of adenoviruses. A grouping of ten squirrel monkey adenovirus variants has high similarity to SqMAdV-1. A single adenovirus variant (designated SqMAdV-3), detected in five monkeys, has similarity to tufted capuchin () adenoviruses. The largest group of adenovirus variants detected (designated SqMAdV-2.0–2.16) has very high similarity (93–99 %) to the TMAdV, suggesting that squirrel monkeys may be the natural host of the TMAdV.

Funding
This study was supported by the:
  • National Institute of Allergy and Infectious Diseases (Award R44AI103982)
    • Principle Award Recipient: John A. Vanchiere
  • NIH Office of the Director (Award R24OD018553)
    • Principle Award Recipient: John A. Vanchiere
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
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2020-07-02
2024-12-06
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References

  1. Virus Taxonomy Release. Available from: https://talk.ictvonline.org/taxonomy/ ; 2018b
  2. Chiu CY, Yagi S, Lu X, Yu G, Chen EC 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:e00084 [View Article][PubMed]
    [Google Scholar]
  3. Chen EC, Yagi S, Kelly KR, Mendoza SP, Tarara RP et al. Cross-species transmission of a novel adenovirus associated with a fulminant pneumonia outbreak in a new world monkey colony. PLoS Pathog 2011; 7:e1002155 [View Article][PubMed]
    [Google Scholar]
  4. Tan B, Wu L-J, Yang X-L, Li B, Zhang W et al. Isolation and characterization of adenoviruses infecting endangered golden snub-nosed monkeys (Rhinopithecus roxellana). Virol J 2016; 13:190 [View Article][PubMed]
    [Google Scholar]
  5. Wevers D, Metzger S, Babweteera F, Bieberbach M, Boesch C et al. Novel adenoviruses in wild primates: a high level of genetic diversity and evidence of zoonotic transmissions. J Virol 2011; 85:10774–10784 [View Article][PubMed]
    [Google Scholar]
  6. Heberling RL. The simian adenoviruses. Pathology of Simian Primates, Part II Basel: Karger; 1972 pp 572–591
    [Google Scholar]
  7. Shroyer EL, Kelley ST, Taylor PC, Vanderloo P, Lester TL. Three serologic types of adenovirus infections of owl monkeys. Am J Vet Res 1979; 40:532–536[PubMed]
    [Google Scholar]
  8. Heymann EW, Calouro AM, Fialho M, Vermeer J, de la Torre S. Plecturocebus cupreus. The IUCN Red List of Threatened Species 2018: e.T127530593A17972923. 2018 [May 6, 2020]; Available from: https://dx.doi.org/10.2305/IUCN.UK.2018-2.RLTS.T127530593A17972923.en .
  9. Gál J, Hornyák Ákos, Mándoki M, Bakonyi T, Balka G et al. Novel mastadenovirus infection and clinical disease in a pygmy marmoset (Callithrix [Cebuella] pygmaea). Vet Microbiol 2013; 167:695–699 [View Article][PubMed]
    [Google Scholar]
  10. Hall NH, Archer LL, Childress AL, Wellehan JFX. Identification of a novel adenovirus in a cotton-top tamarin (Saguinus oedipus). J Vet Diagn Invest 2012; 24:359–363 [View Article][PubMed]
    [Google Scholar]
  11. Podgorski II, Pantó L, Földes K, de Winter I, Jánoska M, Winter de I, Sos E et al. Adenoviruses of the most ancient primate lineages support the theory on virus-host co-evolution. Acta Vet Hung 2018; 66:474–487 [View Article][PubMed]
    [Google Scholar]
  12. Echavarría M. Adenoviruses in immunocompromised hosts. Clin Microbiol Rev 2008; 21:704–715 [View Article][PubMed]
    [Google Scholar]
  13. Hierholzer JC. Adenoviruses in the immunocompromised host. Clin Microbiol Rev 1992; 5:262–274 [View Article][PubMed]
    [Google Scholar]
  14. Gonzalez G, Yawata N, Aoki K, Kitaichi N. Challenges in management of epidemic keratoconjunctivitis with emerging recombinant human adenoviruses. J Clin Virol 2019; 112:1–9 [View Article][PubMed]
    [Google Scholar]
  15. Hiroi S, Kawahata T, Furubayashi K. First isolation of human adenovirus type 85 by molecular analysis of adenoviruses in cases of urethritis. J Med Microbiol 2020; 69:265–269 [View Article][PubMed]
    [Google Scholar]
  16. Holt CD. Overview of immunosuppressive therapy in solid organ transplantation. Anesthesiol Clin 2017; 35:365–380 [View Article][PubMed]
    [Google Scholar]
  17. Wang L, Wang F-S, Gershwin ME. Human autoimmune diseases: a comprehensive update. J Intern Med 2015; 278:369–395 [View Article][PubMed]
    [Google Scholar]
  18. Galluzzi L, Buqué A, Kepp O, Zitvogel L, Kroemer G. Immunological effects of conventional chemotherapy and targeted anticancer agents. Cancer Cell 2015; 28:690–714 [View Article][PubMed]
    [Google Scholar]
  19. Im A, Pavletic SZ. Immunotherapy in hematologic malignancies: past, present, and future. J Hematol Oncol 2017; 10:94 [View Article][PubMed]
    [Google Scholar]
  20. Schioppo T, Ingegnoli F. Current perspective on rituximab in rheumatic diseases. Drug Des Devel Ther 2017; 11:2891–2904 [View Article][PubMed]
    [Google Scholar]
  21. Lee YH, Bae S-C. Comparative efficacy and safety of tocilizumab, rituximab, abatacept and tofacitinib in patients with active rheumatoid arthritis that inadequately responds to tumor necrosis factor inhibitors: a Bayesian network meta-analysis of randomized controlled trials. Int J Rheum Dis 2016; 19:1103–1111 [View Article][PubMed]
    [Google Scholar]
  22. Barnett ANR, Hadjianastassiou VG, Mamode N. Rituximab in renal transplantation. Transpl Int 2013; 26:563–575 [View Article][PubMed]
    [Google Scholar]
  23. Mok CC. Current role of rituximab in systemic lupus erythematosus. Int J Rheum Dis 2015; 18:154–163 [View Article][PubMed]
    [Google Scholar]
  24. Salzer J, Svenningsson R, Alping P, Novakova L, Björck A et al. Rituximab in multiple sclerosis: a retrospective observational study on safety and efficacy. Neurology 2016; 87:2074–2081 [View Article][PubMed]
    [Google Scholar]
  25. Bohra C, Sokol L, Dalia S. Progressive Multifocal Leukoencephalopathy and Monoclonal Antibodies: A Review. Cancer control : journal of the Moffitt Cancer Center; 2017; 241073274817729901
  26. Carson KR, Focosi D, Major EO, Petrini M, Richey EA et al. Monoclonal antibody-associated progressive multifocal leucoencephalopathy in patients treated with rituximab, natalizumab, and efalizumab: a review from the research on adverse drug events and reports (radar) project. Lancet Oncol 2009; 10:816–824 [View Article][PubMed]
    [Google Scholar]
  27. Neil EC, DeAngelis LM. Progressive multifocal leukoencephalopathy and hematologic malignancies: a single cancer center retrospective review. Blood Adv 2017; 1:2041–2045 [View Article][PubMed]
    [Google Scholar]
  28. Iyer A, Mathur R, Deepak BV, Sinard J. Fatal adenoviral hepatitis after rituximab therapy. Arch Pathol Lab Med 2006; 130:1557–1560 [View Article][PubMed]
    [Google Scholar]
  29. Ronan BA, Agrwal N, Carey EJ, De Petris G, Kusne S et al. Fulminant hepatitis due to human adenovirus. Infection 2014; 42:105–111 [View Article][PubMed]
    [Google Scholar]
  30. Wachtman LM, Mansfield KG. Opportunistic infections in immunologically compromised nonhuman primates. Ilar J 2008; 49:191–208 [View Article][PubMed]
    [Google Scholar]
  31. Yu G, Yagi S, Carrion R, Chen EC, Liu M et al. Experimental cross-species infection of common marmosets by titi monkey adenovirus. PLoS One 2013; 8:e68558. Epub 2013/07/31 [View Article][PubMed]
    [Google Scholar]
  32. Abee CR. Squirrel monkey (Saimiri spp.) research and resources. ILAR J 2000; 41:2–9 [View Article][PubMed]
    [Google Scholar]
  33. Rogers DL, McClure GB, Ruiz JC, Abee CR, Vanchiere JA. Endemic viruses of squirrel monkeys (Saimiri spp.). Comp Med 2015; 65:232–240[PubMed]
    [Google Scholar]
  34. Hierholzer JC, Halonen PE, Dahlen PO, Bingham PG, McDonough MM. Detection of adenovirus in clinical specimens by polymerase chain reaction and liquid-phase hybridization quantitated by time-resolved fluorometry. J Clin Microbiol 1993; 31:1886–1891 [View Article][PubMed]
    [Google Scholar]
  35. Lu X, Erdman DD. Molecular typing of human adenoviruses by PCR and sequencing of a partial region of the hexon gene. Arch Virol 2006; 151:1587–1602 [View Article][PubMed]
    [Google Scholar]
  36. Crawford-Miksza L, Schnurr DP. Analysis of 15 adenovirus hexon proteins reveals the location and structure of seven hypervariable regions containing serotype-specific residues. J Virol 1996; 70:1836–1844 [View Article][PubMed]
    [Google Scholar]
  37. Pantó L, Podgorski II, Jánoska M, Márkó O, Harrach B. Taxonomy proposal for old World monkey adenoviruses: characterisation of several non-human, non-ape primate adenovirus lineages. Arch Virol 2015; 160:3165–3177 [View Article][PubMed]
    [Google Scholar]
  38. King NW, Hunt RD, Daniel MD, Melendez LV. Overt herpes-T infection in squirrel monkeys (Saimiri sciureus). Lab Anim Care 1967; 17:413–423[PubMed]
    [Google Scholar]
  39. Ebner K, Pinsker W, Lion T. Comparative sequence analysis of the hexon gene in the entire spectrum of human adenovirus serotypes: phylogenetic, taxonomic, and clinical implications. J Virol 2005; 79:12635–12642 [View Article][PubMed]
    [Google Scholar]
  40. J-JaFD P. Primates of the World. 2013 New Jersey: Princeton University Press; 2010 p 186 p.
    [Google Scholar]
  41. Wang X, Lim BK, Ting N, Hu J, Liang Y et al. Reconstructing the phylogeny of new world monkeys (platyrrhini): evidence from multiple non-coding loci. Curr Zool 2019; 65:579–588 [View Article][PubMed]
    [Google Scholar]
  42. Moorman EA, Mendoza SP, Shideler SE, Lasley BL. Excretion and measurement of estradiol and progesterone metabolites in the feces and urine of female squirrel monkeys (Saimiri sciureus). Am J Primatol 2002; 57:79–90 [View Article][PubMed]
    [Google Scholar]
  43. Schiml PA, Mendoza SP, Saltzman W, Lyons DM, Mason WA. Seasonality in squirrel monkeys (Saimiri sciureus): social facilitation by females. Physiol Behav 1996; 60:1105–1113 [View Article][PubMed]
    [Google Scholar]
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