Monkeypox virus emerges from the shadow of its more infamous cousin: family biology matters

References

• Moss B. Poxviridae. In: Knipe DM, Howley PM, editor. Fields virology, Vol. 2. 6th ed. Philadelphia: Lippincott Williams & Wilkins; 2013. p. 2129–2159.
   Google Scholar
• Senkevich TG, Yutin N, Wolf YI, et al. Ancient gene capture and recent gene loss shape the evolution of orthopoxvirus-host interaction genes. MBio 2021 Aug 31;12(4):e0149521.
   PubMed Web of Science ®Google Scholar
• Damon IK. Poxviruses. In: Knipe DM, Howley PM, editors. Fields virology. Vol. 2. 6th ed. Philadelphia: Lippincott Williams & Wilkins; 2013. p. 2160–2184.
   Google Scholar
• Cardeti G, Gruber CEM, Eleni C, et al. Fatal outbreak in tonkean macaques caused by possibly novel orthopoxvirus, Italy, January 2015 (1). Emerg Infect Dis. 2017 Dec;23(12):1941–1949.
   PubMed Web of Science ®Google Scholar
• Gao J, Gigante C, Khmaladze E, et al. Genome sequences of akhmeta virus, an early divergent old world orthopoxvirus. Viruses. 2018 May 12;10(5):252.
   PubMed Web of Science ®Google Scholar
• Gigante CM, Gao J, Tang S, et al. Genome of alaskapox virus, a novel orthopoxvirus isolated from Alaska. Viruses. 2019 Aug 1;11(8):708.
   PubMed Web of Science ®Google Scholar
• Chen N, Li G, Liszewski MK, et al. Virulence differences between monkeypox virus isolates from West Africa and the Congo basin. Virology. 2005 Sep 15;340(1):46–63.
   PubMed Web of Science ®Google Scholar
• Likos AM, Sammons SA, Olson VA, et al. A tale of two clades: monkeypox viruses. J Gen Virol. 2005 Oct;86(Pt 10):2661–2672.
   PubMed Web of Science ®Google Scholar
• Bunge EM, Hoet B, Chen L, et al. The changing epidemiology of human monkeypox-a potential threat? A systematic review. PLoS Negl Trop Dis. 2022 Feb;16(2):e0010141.
   PubMed Web of Science ®Google Scholar
• WHO. Outbreaks and Emergencies Bulletin; 2022. Available from: https://www.afro.who.int/health-topics/disease-outbreaks/outbreaks-and-other-emergencies-updates.
   Google Scholar
• Magnus PV, Andersen EK, Petersen KB, et al. A pox-like disease in Cynomolgus Monkeys. Acta Pathologica Microbiologica Scandinavica. 1959;46(2):156–176.
   Google Scholar
• Cho CT, Wenner HA. Monkeypox virus. Bacteriol Rev. 1973 Mar;37(1):1–18.
   PubMedGoogle Scholar
• Marennikova SS, Seluhina EM, Mal'ceva NN, et al. Isolation and properties of the causal agent of a new variola-like disease (monkeypox) in man. Bull World Health Organ. 1972;46(5):599–611.
   PubMed Web of Science ®Google Scholar
• Ladnyj ID, Ziegler P, Kima E. A human infection caused by monkeypox virus in Basankusu territory, Democratic Republic of the Congo. Bull World Health Organ. 1972;46(5):593–597.
   PubMed Web of Science ®Google Scholar
• Foster SO, Brink EW, Hutchins DL, et al. Human monkeypox. Bull World Health Organ. 1972;46(5):569–576.
   PubMed Web of Science ®Google Scholar
• Rimoin AW, Mulembakani PM, Johnston SC, et al. Major increase in human monkeypox incidence 30 years after smallpox vaccination campaigns cease in the Democratic Republic of Congo. P Natl Acad Sci USA. 2010 Sep 14;107(37):16262–16267.
   PubMed Web of Science ®Google Scholar
• Learned LA, Reynolds MG, Wassa DW, et al. Extended interhuman transmission of monkeypox in a hospital community in the Republic of the Congo, 2003. Am J Trop Med Hyg. 2005 Aug;73(2):428–434.
   PubMed Web of Science ®Google Scholar
• Formenty P, Muntasir MO, Damon I, et al. Human monkeypox outbreak caused by novel virus belonging to Congo Basin clade, Sudan, 2005. Emerg Infect Dis. 2010;16(10):1539–1545.
   PubMed Web of Science ®Google Scholar
• Yinka-Ogunleye A, Aruna O, Dalhat M, et al. Outbreak of human monkeypox in Nigeria in 2017-18: a clinical and epidemiological report. Lancet Infect Dis. 2019 Aug;19(8):872–879.
   PubMed Web of Science ®Google Scholar
• Reed KD, Melski JW, Graham MB, et al. The detection of monkeypox in humans in the western hemisphere. N Engl J Med. 2004 Jan 22;350(4):342–350.
   PubMed Web of Science ®Google Scholar
• Mauldin MR, McCollum AM, Nakazawa YJ, et al. Exportation of monkeypox virus from the African continent. J Infect Dis. 2022 Apr 19;225(8):1367–1376.
   PubMed Web of Science ®Google Scholar
• Hobson G, Adamson J, Adler H, et al. Family cluster of three cases of monkeypox imported from Nigeria to the United Kingdom, May 2021. Euro Surveill. 2021 Aug;26(32):2100745.
   PubMedGoogle Scholar
• Mathieu E, Dattani S, Ritchie H, et al. “Monkeypox”. Published online at OurWorldInData.org; 2022. Available from: https://ourworldindata.org/monkeypox.
   Google Scholar
• Perez Duque M, Ribeiro S, Martins JV, et al. Ongoing monkeypox virus outbreak, Portugal, 29 April to 23 May 2022. Eurosurveillance. 2022;27(22):2200424.
   Web of Science ®Google Scholar
• Vivancos R, Anderson C, Blomquist P, et al. Community transmission of monkeypox in the United Kingdom, April to May 2022. Eurosurveillance. 2022;27(22):2200422.
   Web of Science ®Google Scholar
• Wolff HL, Croon JJ. The survival of smallpox virus (variola minor) in natural circumstances. Bull World Health Organ. 1968;38(3):492–493.
   PubMed Web of Science ®Google Scholar
• Damon IK. Status of human monkeypox: clinical disease, epidemiology and research. Vaccine. 2011 Dec 30;29(Suppl 4):D54–D59.
   PubMed Web of Science ®Google Scholar
• Heskin J, Belfield A, Milne C, et al. Transmission of monkeypox virus through sexual contact – A novel route of infection. Journal of Infection. 2022.
   Web of Science ®Google Scholar
• McCollum AM, Damon IK. Human monkeypox. Clin Infect Dis. 2014 Jan;58(2):260–267.
   PubMed Web of Science ®Google Scholar
• Ogoina D, Iroezindu M, James HI, et al. Clinical course and outcome of human monkeypox in Nigeria. Clin Infect Dis. 2020 Nov 5;71(8):e210–e214.
   PubMed Web of Science ®Google Scholar
• Whitehouse ER, Bonwitt J, Hughes CM, et al. Clinical and epidemiological findings from enhanced monkeypox surveillance in tshuapa province, Democratic Republic of the Congo during 2011-2015. J Infect Dis. 2021 Jun 4;223(11):1870–1878.
   PubMed Web of Science ®Google Scholar
• Khodakevich L, Jezek Z, Kinzanzka K. Isolation of monkeypox virus from wild squirrel infected in nature. Lancet. 1986 Jan 11;1(8472):98–99.
   PubMed Web of Science ®Google Scholar
• Radonic A, Metzger S, Dabrowski PW, et al. Fatal monkeypox in wild-living sooty mangabey, Cote d'Ivoire, 2012. Emerg Infect Dis. 2014 Jun;20(6):1009–1011.
   PubMed Web of Science ®Google Scholar
• Hutin YJ, Williams RJ, Malfait P, et al. Outbreak of human monkeypox, Democratic Republic of Congo, 1996 to 1997. Emerg Infect Dis. 2001 May-Jun;7(3):434–438.
   PubMed Web of Science ®Google Scholar
• Reynolds MG, Carroll DS, Olson VA, et al. A silent enzootic of an orthopoxvirus in Ghana, West Africa: evidence for multi-species involvement in the absence of widespread human disease. Am J Trop Med Hyg. 2010 Apr;82(4):746–754.
   PubMed Web of Science ®Google Scholar
• Doty JB, Malekani JM, Kalemba LN, et al. Assessing monkeypox virus prevalence in small mammals at the human-animal interface in the Democratic Republic of the Congo. Viruses. 2017 Oct 3;9(10):283.
   PubMed Web of Science ®Google Scholar
• Arita I, Henderson DA. Monkeypox and whitepox viruses in West and Central Africa. Bull World Health Organ. 1976;53(4):347–353.
   PubMed Web of Science ®Google Scholar
• Guagliardo SAJ, Monroe B, Moundjoa C, et al. Asymptomatic orthopoxvirus circulation in humans in the wake of a monkeypox outbreak among chimpanzees in Cameroon. Am J Trop Med Hyg. 2020 Jan;102(1):206–212.
   PubMed Web of Science ®Google Scholar
• Patrono LV, Pleh K, Samuni L, et al. Monkeypox virus emergence in wild chimpanzees reveals distinct clinical outcomes and viral diversity. Nat Microbiol. 2020 Jul;5(7):955–965.
   PubMed Web of Science ®Google Scholar
• Reynolds MG, Doty JB, McCollum AM, et al. Monkeypox re-emergence in Africa: a call to expand the concept and practice of One health. Expert Rev Anti Infect Ther. 2019 Feb;17(2):129–139.
   PubMed Web of Science ®Google Scholar
• Tesh RB, Watts DM, Sbrana E, et al. Experimental infection of ground squirrels (Spermophilus tridecemlineatus) with monkeypox virus. Emerging Infectious Disease Journal. 2004;10(9):1563.
   PubMed Web of Science ®Google Scholar
• Werden SJ, Rahman MM, McFadden G. Poxvirus host range genes. Adv Virus Res. 2008;71:135–171.
   PubMed Web of Science ®Google Scholar
• Bratke KA, McLysaght A, Rothenburg S. A survey of host range genes in poxvirus genomes. Infect Genet Evol. 2013 Mar;14:406–425.
   PubMed Web of Science ®Google Scholar
• Oliveira GP, Rodrigues RAL, Lima MT, et al. Poxvirus host range genes and virus-host spectrum: A critical review. Viruses. 2017 Nov 7;9(11):331.
   PubMed Web of Science ®Google Scholar
• Elde NC, Child SJ, Geballe AP, et al. Protein kinase R reveals an evolutionary model for defeating viral mimicry. Nature. 2009 Jan 22;457(7228):485–489.
   PubMed Web of Science ®Google Scholar
• Rothenburg S, Seo EJ, Gibbs JS, et al. Rapid evolution of protein kinase PKR alters sensitivity to viral inhibitors. Nat Struct Mol Biol. 2009 Jan;16(1):63–70.
   PubMed Web of Science ®Google Scholar
• Park C, Peng C, Rahman MJ, et al. Orthopoxvirus K3 orthologs show virus- and host-specific inhibition of the antiviral protein kinase PKR. PLoS Pathog. 2021 Jan;17(1):e1009183.
   PubMed Web of Science ®Google Scholar
• Cao J, Varga J, Deschambault Y. Poxvirus encoded eIF2alpha homolog, K3 family proteins, is a key determinant of poxvirus host species specificity. Virology. 2020 Feb;541:101–112.
   PubMed Web of Science ®Google Scholar
• Sivan G, Ormanoglu P, Buehler EC, et al. Identification of restriction factors by human genome-wide RNA interference screening of viral host range mutants exemplified by discovery of SAMD9 and WDR6 as inhibitors of the vaccinia virus K1L-C7L- mutant. mBio. 2015 Aug 4;6(4):e01122.
   PubMed Web of Science ®Google Scholar
• Liu J, McFadden G. SAMD9 is an innate antiviral host factor with stress response properties that can be antagonized by poxviruses. J Virol. 2015 Feb;89(3):1925–1931.
   PubMed Web of Science ®Google Scholar
• Meng X, Zhang F, Yan B, et al. A paralogous pair of mammalian host restriction factors form a critical host barrier against poxvirus infection. PLoS Pathog. 2018 Feb;14(2):e1006884.
   PubMed Web of Science ®Google Scholar
• Lemos de Matos A, Liu J, McFadden G, et al. Evolution and divergence of the mammalian SAMD9/SAMD9L gene family. BMC Evol Biol. 2013;13:121.
   PubMed Web of Science ®Google Scholar
• Zhang F, Meng X, Townsend MB, et al. Identification of CP77 as the third orthopoxvirus SAMD9 and SAMD9L inhibitor with unique specificity for a rodent SAMD9L. J Virol. 2019 Jun 15;93(12):e00225–19.
   PubMed Web of Science ®Google Scholar
• Peng C, Moss B. Repair of a previously uncharacterized second host-range gene contributes to full replication of modified vaccinia virus Ankara (MVA) in human cells. Proc Natl Acad Sci U S A. 2020 Feb 18;117(7):3759–3767.
   PubMed Web of Science ®Google Scholar
• Liu R, Mendez-Rios JD, Peng C, et al. SPI-1 is a missing host-range factor required for replication of the attenuated modified vaccinia Ankara (MVA) vaccine vector in human cells. PLoS Pathog. 2019 May;15(5):e1007710.
   PubMed Web of Science ®Google Scholar
• Peng C, Wyatt LS, Glushakow-Smith SG, et al. Zinc-finger antiviral protein (ZAP) is a restriction factor for replication of modified vaccinia virus Ankara (MVA) in human cells. PLoS Pathog. 2020 Aug;16(8):e1008845.
   PubMed Web of Science ®Google Scholar
• Moss B. Poxvirus DNA replication. Cold Spring Harbor Perspect Biol. 2013;5(9):a010199.
   PubMed Web of Science ®Google Scholar
• Firth C, Kitchen A, Shapiro B, et al. Using time-structured data to estimate evolutionary rates of double-stranded DNA viruses. Mol Biol Evol. 2010;27(9):2038–2051.
   PubMed Web of Science ®Google Scholar
• Duggan AT, Perdomo MF, Piombino-Mascali D, et al. 17 th century variola virus reveals the recent history of smallpox. Curr Biol. 2016;26(24):3407–3412.
   PubMed Web of Science ®Google Scholar
• Duffy S, Shackelton LA, Holmes EC. Rates of evolutionary change in viruses: patterns and determinants. Nat Rev Genet. 2008 Apr;9(4):267–276.
   PubMed Web of Science ®Google Scholar
• Ghafari M, du Plessis L, Raghwani J, et al. Purifying selection determines the short-term time dependency of Evolutionary Rates in SARS-CoV-2 and pH1N1 influenza. Mol Biol Evol. 2022;39(2):msac009.
   PubMed Web of Science ®Google Scholar
• Hendrickson RC, Wang C, Hatcher EL, et al. Orthopoxvirus genome evolution: the role of gene loss. Viruses. 2010 Sep;2(9):1933–1967.
   PubMed Web of Science ®Google Scholar
• Mühlemann B, Vinner L, Margaryan A, et al. Diverse variola virus (smallpox) strains were widespread in Northern Europe in the viking age. Science. 2020;369(6502):eaaw8977.
   PubMed Web of Science ®Google Scholar
• Alcamí A. Was smallpox a widespread mild disease? Science. 2020 Jul 24;369(6502):376–377.
   PubMed Web of Science ®Google Scholar
• Kugelman JR, Johnston SC, Mulembakani PM, et al. Genomic variability of monkeypox virus among humans, Democratic Republic of the Congo. Emerg Infect Dis. 2014 Feb;20(2):232–239.
   PubMed Web of Science ®Google Scholar
• Diaz-Cánova D, Moens UL, Brinkmann A, et al. Genomic sequencing and analysis of a novel human cowpox virus With mosaic sequences from North America and Old World orthopoxvirus. Front Microbiol. 2022;13:868887.
   PubMed Web of Science ®Google Scholar
• Agueda-Pinto A, de Matos A L, Abrantes M, et al. Genetic characterization of a recombinant Myxoma virus in the Iberian hare (Lepus granatensis). Viruses. 2019 Jun 7;11(6):530.
   PubMed Web of Science ®Google Scholar
• Agueda-Pinto A, Kraberger S, Everts A, et al. Identification of a novel Myxoma virus C7-like host range factor that enabled a species leap from rabbits to hares. mBio. 2022 Apr 26;13(2):e0346121.
   PubMed Web of Science ®Google Scholar
• Slabaugh MB, Roseman NA, Mathews CK. Amplification of the ribonucleotide reductase small subunit gene: analysis of novel joints and the mechanism of gene duplication in vaccinia virus. Nucleic Acids Res. 1989 Sep 12;17(17):7073–7088.
   PubMed Web of Science ®Google Scholar
• Erlandson KJ, Cotter CA, Charity JC, et al. Duplication of the A17L locus of vaccinia virus provides an alternate route to rifampin resistance. J Virol. 2014 Oct;88(19):11576–11585.
   PubMed Web of Science ®Google Scholar
• Elde NC, Child SJ, Eickbush MT, et al. Poxviruses deploy genomic accordions to adapt rapidly against host antiviral defenses. Cell. 2012 Aug 17;150(4):831–841.
   PubMed Web of Science ®Google Scholar
• Brennan G, Kitzman JO, Rothenburg S, et al. Adaptive gene amplification as an intermediate step in the expansion of virus host range. PLoS Pathog. 2014 Mar;10(3):e1004002.
   PubMed Web of Science ®Google Scholar
• Hammarlund E, Lewis MW, Hansen SG, et al. Duration of antiviral immunity after smallpox vaccination. Nat Med. 2003 Sep;9(9):1131–1137.
   PubMed Web of Science ®Google Scholar
• Crotty S, Felgner P, Davies H, et al. Cutting edge: long-term B cell memory in humans after smallpox vaccination. J Immunol. 2003 Nov 15;171(10):4969–4973.
   PubMed Web of Science ®Google Scholar
• Fine PE, Jezek Z, Grab B, et al. The transmission potential of monkeypox virus in human populations. Int J Epidemiol. 1988 Sep;17(3):643–650.
   PubMed Web of Science ®Google Scholar
• Rao AK, Petersen BW, Whitehill F, et al. Use of JYNNEOS (smallpox and monkeypox vaccine, live, nonreplicating) for preexposure vaccination of persons at risk for occupational exposure to orthopoxviruses: recommendations of the advisory committee on immunization practices - United States, 2022. MMWR Morb Mortal Wkly Rep. 2022 Jun 3;71(22):734–742.
   PubMed Web of Science ®Google Scholar
• Adler H, Gould S, Hine P, et al. Clinical features and management of human monkeypox: a retrospective observational study in the UK. Lancet Infect Dis. 2022;S1473-3099(22)00228-6.
   Web of Science ®Google Scholar
• Andrei G, Fiten P, Krečmerová M, et al. Poxviruses bearing DNA polymerase mutations show complex patterns of cross-resistance. Biomedicines. 2022 Mar 1;10(3):580.
   PubMed Web of Science ®Google Scholar
• Duraffour S, Lorenzo MM, Zöller G, et al. ST-246 is a key antiviral to inhibit the viral F13L phospholipase, one of the essential proteins for orthopoxvirus wrapping. J Antimicrob Chemother. 2015;70(5):1367–1380.
   PubMed Web of Science ®Google Scholar
• Sarkar JK, Mitra AC, Mukherjee MK. The minimum protective level of antibodies in smallpox. Bull World Health Organ. 1975;52(3):307–311.
   PubMed Web of Science ®Google Scholar
• Hopkins RJ, Lane JM. Clinical efficacy of intramuscular vaccinia immune globulin: a literature review. Clin Infect Dis. 2004 Sep 15;39(6):819–826.
   PubMed Web of Science ®Google Scholar
• Fogg C, Lustig S, Whitbeck JC, et al. Protective immunity to vaccinia virus induced by vaccination with multiple recombinant outer membrane proteins of intracellular and extracellular virions. J Virol. 2004 Oct;78(19):10230–10237.
   PubMed Web of Science ®Google Scholar
• Lustig S, Fogg C, Whitbeck JC, et al. Combinations of polyclonal or monoclonal antibodies to proteins of the outer membranes of the two infectious forms of vaccinia virus protect mice against a lethal respiratory challenge. J Virol. 2005 Nov;79(21):13454–13462.
   PubMed Web of Science ®Google Scholar
• Xu C, Meng X, Yan B, et al. An epitope conserved in orthopoxvirus A13 envelope protein is the target of neutralizing and protective antibodies. Virology. 2011 Sep 15;418(1):67–73.
   PubMed Web of Science ®Google Scholar
• Moss B. Smallpox vaccines: targets of protective immunity. Immunol Rev. 2011 Jan;239(1):8–26.
   PubMed Web of Science ®Google Scholar
• Benhnia MR, McCausland MM, Su HP, et al. Redundancy and plasticity of neutralizing antibody responses are cornerstone attributes of the human immune response to the smallpox vaccine. J Virol. 2008 Apr;82(7):3751–3768.
   PubMed Web of Science ®Google Scholar
• Davies DH, Molina DM, Wrammert J, et al. Proteome-wide analysis of the serological response to vaccinia and smallpox. Proteomics. 2007 May;7(10):1678–1686.
   PubMed Web of Science ®Google Scholar
• Gilchuk I, Gilchuk P, Sapparapu G, et al. Cross-Neutralizing and protective human antibody specificities to poxvirus infections. Cell. 2016 Oct 20;167(3):684–694.
   PubMed Web of Science ®Google Scholar
• Zajonc DM. Antibody recognition of immunodominant vaccinia virus envelope proteins. Subcell Biochem. 2017;83:103–126.
   PubMedGoogle Scholar
• Kaever T, Meng X, Matho MH, et al. Potent neutralization of vaccinia virus by divergent murine antibodies targeting a common site of vulnerability in L1 protein. J Virol. 2014 Oct;88(19):11339–11355.
   PubMed Web of Science ®Google Scholar
• Su HP, Golden JW, Gittis AG, et al. Structural basis for the binding of the neutralizing antibody, 7D11, to the poxvirus L1 protein. Virology. 2007 Nov 25;368(2):331–341.
   PubMed Web of Science ®Google Scholar
• Meyer H, Osterrieder N, Czerny CP. Identification of binding sites for neutralizing monoclonal antibodies on the 14-kDa fusion protein of orthopox viruses. Virology. 1994 May 1;200(2):778–783.
   PubMed Web of Science ®Google Scholar
• Kaever T, Matho MH, Meng X, et al. Linear epitopes in vaccinia virus A27 Are targets of protective antibodies induced by vaccination against smallpox. J Virol. 2016 May;90(9):4334–4345.
   PubMed Web of Science ®Google Scholar
• Matho MH, Schlossman A, Gilchuk IM, et al. Structure-function characterization of three human antibodies targeting the vaccinia virus adhesion molecule D8. J Biol Chem. 2018 Jan 5;293(1):390–401.
   PubMed Web of Science ®Google Scholar
• Matho MH, de Val N, Miller GM, et al. Murine anti-vaccinia virus D8 antibodies target different epitopes and differ in their ability to block D8 binding to CS-E. PLoS Pathog. 2014 Dec;10(12):e1004495.
   PubMed Web of Science ®Google Scholar
• Chen Z, Earl P, Americo J, et al. Characterization of chimpanzee/human monoclonal antibodies to vaccinia virus A33 glycoprotein and its variola virus homolog in vitro and in a vaccinia virus mouse protection model. J Virol. 2007 Sep;81(17):8989–8995.
   PubMed Web of Science ®Google Scholar
• Matho MH, Schlossman A, Meng X, et al. Structural and functional Characterization of anti-A33 antibodies reveal a potent cross-species Orthopoxviruses neutralizer. PLoS Pathog. 2015 Sep;11(9):e1005148.
   PubMed Web of Science ®Google Scholar
• O’Toole Á, Rambaut A. Initial observations about putative APOBEC3 deaminase editing driving short-term evolution of MPXV since 2017. virological.org; 2022.
   Google Scholar
• Heraud JM, Edghill-Smith Y, Ayala V, et al. Subunit recombinant vaccine protects against monkeypox. J Immunol. 2006 Aug 15;177(4):2552–2564.
   PubMed Web of Science ®Google Scholar