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Men, Primates, and Germs: An Ongoing Affair

  • Jean Paul GonzalezEmail author
  • Frank Prugnolle
  • Eric Leroy
Part of the Current Topics in Microbiology and Immunology book series (CT MICROBIOLOGY, volume 365)

Abstract

Humans and nonhuman primates are phylogenetically (i.e., genetically) related and share pathogens that can jump from one species to another. The specific strategies of three groups of pathogens for crossing the species barrier among primates will be discussed. In Africa, gorillas and chimpanzees have succumbed for years to simultaneous epizootics (i.e.. “multi-emergence”) of Ebola virus in places where they are in contact with Chiropters, which could be animal reservoirs of these viruses. Human epidemics often follow these major outbreaks. Simian immunodeficiency viruses (SIVs) have an ancient history of coevolution and many interspecific exchanges with their natural hosts. Chimpanzee and gorilla SIVs have crossed the species barrier at different times and places, leading to the emergence of HIV-1 and HIV-2. Other retroviruses, such as the Simian T-Lymphotropic Viruses and Foamiviruses, have also a unique ancient or recent history of crossing the species barrier. The identification of gorilla Plasmodium parasites that are genetically close to P. falciparum suggests that gorillas were the source of the deadly human P. falciparum. Nonhuman plasmodium species that can infect humans represent an underestimated risk.

Keywords

Primates Nonhuman primates Cross-species transmission 

References

  1. Barrette RW, Metwally SA, Rowland JM, Xu L, Zaki SR, Nichol ST et al (2009) Discovery of swine as a host for the Reston ebola virus. Science 325:204–206CrossRefPubMedGoogle Scholar
  2. Bermejo M, Rodriguez-Teijeiro JD, Illera G, Barroso A, Vila C, Walsh PD (2006) Ebola outbreak killed 5000 gorillas. Science 314:1564CrossRefPubMedGoogle Scholar
  3. Bibollet-Ruche F, Bailes E, Gao F, Pourrut X, Barlow KL, Clewley JP et al (2004) New simian immunodeficiency virus infecting De Brazza’s monkeys (Cercopithecus neglectus): evidence for a Cercopithecus monkey virus clade. J Virol 78:7748–7762CrossRefPubMedGoogle Scholar
  4. Brack M (1987) Agents transmissible from simians to man. Springer-Verlag, Berlin, p 454pCrossRefGoogle Scholar
  5. Bronson RT et al (1972) Am J Pathol 69(2):289–308Google Scholar
  6. Coatney GR, Collins WE, Warren M, Contacos PG (1971) The primate malarias. U. S. Government Printing Office, Washington, p 366Google Scholar
  7. Damond F, Worobey M, Campa P, Farfara I, Colin G, Matheron S et al (2004) Identification of a highly divergent HIV type 2 and proposal for a change in HIV type 2 classification. AIDS Res Hum Retrovir 20:666–672CrossRefPubMedGoogle Scholar
  8. Daszak P, Cunningham AA, Hyatt AD (2000) Emerging infectious diseases of wildlife—threats to biodiversity and human health. Science 287(443):449Google Scholar
  9. Davies TJ, Pedersen AB (2008) Phylogeny and geography predict pathogen community similarity in wild primates and humans. Proc R Soc B Biol Sci 275:1695–1701CrossRefGoogle Scholar
  10. Duval L, Fourment M, Nerrienet E, Rousset D, Sadeuh SA et al (2010) African apes as reservoirs of Plasmodium falciparum and the origin and diversification of the Laverania subgenus. Proc Natl Acad Sci U S A 107(23):10561–10566CrossRefPubMedGoogle Scholar
  11. Escalante AA, Ayala FJ (1994) Phylogeny of the malarial genus Plasmodium, derived from rRNA gene sequences. Proc Natl Acad Sci U S A 91(24):11373–11377CrossRefPubMedGoogle Scholar
  12. Formenty P, Boesch C, Wyers M, Steiner C, Donati F, Dind F et al (1999) Ebola virus outbreak among wild chimpanzees living in a rain forest of cote d’ivoire. J Infect Dis 179(Suppl 1):S120–S126CrossRefPubMedGoogle Scholar
  13. Gao F, Bailes E, Robertson DL, Chen Y, Rodenburg CM, Michael SF et al (1999) Origin of HIV-1 in the chimpanzee Pan troglodytes troglodytes. Nature 397:436–441CrossRefPubMedGoogle Scholar
  14. Georges AJ, Leroy EM, Renaut AA, Tevi benissan C, Nabias RJ, Trinh Ngoc M et al (1999) Ebola hemorrhagic fever outbreaks in Gabon, 1994–1997: epidemiologic and health control issues. J Infect Dis 179(Suppl 1):S65–S75CrossRefPubMedGoogle Scholar
  15. Gessain A (2011) Human retrovirus HTLV-1: descriptive and molecular epidemiology, origin, evolution, diagnosis and associated diseases. Bull Soc Pathol Exot 104(3):167–180CrossRefPubMedGoogle Scholar
  16. Gifford RJ, Katzourakis A, Tristem M, Pybus OG, Winters M, Shafer RW (2008) A transitional endogenous lentivirus from the genome of a basal primate and implications for lentivirus evolution. Proc Natl Acad Sci 105:20362–20367CrossRefPubMedGoogle Scholar
  17. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704CrossRefPubMedGoogle Scholar
  18. Hahn BH, Shaw GM, De Cock KM, Sharp PM (2000) AIDS as a zoonosis: scientific and public health implications. Science 287:607–614CrossRefPubMedGoogle Scholar
  19. Heneine W, Schweizer M, Sandstrom P, Folks T (2003) Human infection with foamy viruses. Curr Top Microbiol Immunol 277:181–196CrossRefPubMedGoogle Scholar
  20. Hirsch VM, Olmsted RA, Murphey-Corb M, Purcell RH, Johnson PR (1989) An African primate lentivirus (SIVsm) closely related to HIV-2. Nature 339:389–392CrossRefPubMedGoogle Scholar
  21. Holmes EC (2003) Molecular clocks and the puzzle of RNA virus origins. J Virol 77:3893–3897CrossRefPubMedGoogle Scholar
  22. Jahrling PB, Geisbert TW, Dalgard DW, Johnson ED, Ksiazek TG, Hall WC et al (1990) Preliminary report: isolation of Ebola virus from monkeys imported to USA. Lancet 335:502–505CrossRefPubMedGoogle Scholar
  23. Kaiser M, Lowa A, Ulrich M, Ellerbrok H, Goffe AS et al (2010) Wild chimpanzees infected with 5 Plasmodium species. Emerg Infect Dis 16(12):1956–1959CrossRefPubMedGoogle Scholar
  24. Katzourakis A, Tristem M, Pybus OG, Gifford RJ (2007) Discovery and analysis of the first endogenous lentivirus. Proc Natl Acad Sci 104:6261–6265CrossRefPubMedGoogle Scholar
  25. Klempner MS, Shapiro DS (2004) Crossing the species barrier—one small step to man, one giant leap to mankind. N Engl J Med 350:1171–1172CrossRefPubMedGoogle Scholar
  26. Krief S, Escalante AA, Pacheco MA, Mugisha L, Andre C et al (2010) On the diversity of malaria parasites in African apes and the origin of Plasmodium falciparum from Bonobos. PLoS Pathog 6(2):e1000765CrossRefPubMedGoogle Scholar
  27. Leroy EM, Rouquet P, Formenty P, Souquière A, Kilbourne A, Froment J-M et al (2004a) Multiple Ebola virus transmission events and rapid decline of central African wildlife. Science 303:387–390CrossRefPubMedGoogle Scholar
  28. Leroy EM, Telfer P, Kumulungui B, Yaba P, rouquet P, Roques P et al (2004b) A serological survey of Ebola virus infection in central African nonhuman primates. J Infect Dis 190:1895–1899CrossRefPubMedGoogle Scholar
  29. Leroy EM, Kumulungui B, Pourrut X, Rouquet P, Hassanin A, Yaba P et al (2005) Fruit bats as reservoirs of Ebola virus. Nature 438:575–576CrossRefPubMedGoogle Scholar
  30. Leroy EM, Epelboin A, Mondonge V, Pourrt X, Gonzalez J-P, Muyembe Tamfum J-J et al (2009) Human ebola outbreak resulting from direct exposure to fruit bats in Luebo, Democratic Republic of Congo. Vector Borne Zoonotic Dis 6:723–728CrossRefGoogle Scholar
  31. Leroy EM, Gonzalez J-P, Baize S (2011) Ebola and Marburg haemorrhagic fever viruses: major scientific advances, but a relatively minor public health threat for Africa. Clin Microbiol Infect 17:964–976CrossRefPubMedGoogle Scholar
  32. Liu W, Li Y, Learn GH, Rudicell RS, Robertson JD et al (2010) Origin of the human malaria parasite Plasmodium falciparum in gorillas. Nature 467(7314):420–425CrossRefPubMedGoogle Scholar
  33. Locatelli S, Peeters M (2012) Simian retroviruses and emerging diseases AIDS 2012, 26. doi:  10.1097/QAD.0b013e328350fb68
  34. Mahieux R, Gessain A (2011) HTLV-3/STLV-3 and HTLV-4 viruses: discovery, epidemiology, serology and molecular aspects. Viruses 3(7):1074–90Google Scholar
  35. Martinsen ES, Perkins SL, Schall JJ (2008) A three-genome phylogeny of malaria parasites (Plasmodium and closely related genera): evolution of life-history traits and host switches. Mol Phylogenet Evol 47(1):261–273CrossRefPubMedGoogle Scholar
  36. Mu J, Joy DA, Duan J, Huang Y, Carlton J et al (2005) Host switch leads to emergence of Plasmodium vivax malaria in humans. Mol Biol Evol 22(8):1686–1693CrossRefPubMedGoogle Scholar
  37. Ollomo B, Durand P, Prugnolle F, Douzery E, Arnathau C et al (2009) A new malaria agent in African hominids. PLoS Pathog 5(5):e1000446CrossRefPubMedGoogle Scholar
  38. Plantier JC, Leoz M, Dickerson JE, De Oliveira F, Cordonnier F, Lemee V, Damond F, Robertson DL, Simon F (2009) A new human immunodeficiency virus derived from gorillas. Nature Med 15:871–872CrossRefPubMedGoogle Scholar
  39. Prugnolle F, Durand P, Neel C, Ollomo B, Ayala FJ et al (2010) African great apes are natural hosts of multiple related malaria species, including Plasmodium falciparum. Proc Natl Acad Sci U S A 107(4):1458–1463CrossRefPubMedGoogle Scholar
  40. Prugnolle F, Durand P, Ollomo B, Ayala FJ, Renauda F (2011a) Reply to Sharp et al.: host species sampling bias and Plasmodium falciparum origin paradigm shifts. Proc Natl Acad Sci U S A 108(43):E873CrossRefPubMedGoogle Scholar
  41. Prugnolle F, Durand P, Ollomo B, Duval L, Ariey F et al (2011b) A fresh look at the origin of Plasmodium falciparum, the most malignant malaria agent. PLoS Pathog 7(2):e1001283CrossRefPubMedGoogle Scholar
  42. Prugnolle F, Ollomo B, Durand P, Yalcindag E, Arnathau C et al (2011c) African monkeys are infected by Plasmodium falciparum nonhuman primate-specific strains. Proc Natl Acad Sci U S A 108(29):11948–11953CrossRefPubMedGoogle Scholar
  43. Renquist M, Whitney RA (1987) Zoonoses acquired from pet primates. Vet Clinics of North Am Small Anim Pract 17(1):219–240Google Scholar
  44. Rich SM, Leendertz FH, Xu G, LeBreton M, Djoko CF et al (2009) The origin of malignant malaria. Proc Natl Acad Sci U S A 106(35):14902–14907CrossRefPubMedGoogle Scholar
  45. Riedel S (2006) Crossing the species barrier: the threat of an avian influenza pandemic. Proc Baylor Univ Med Cent 19(1):16–20Google Scholar
  46. Ruch TC (1959) Diseases of laboratory primates. W.B. Saunders Company, Philadelphia, pp 1–159Google Scholar
  47. Sharp PM and Hahn BH (2011) AIDS: prehistory of HIV-1. In: Frederic D. Bushman, GJ Nabel, Swanstrom R (eds) Cold Spring Harb Perspect Med 2011, vol 1, pp a006841Google Scholar
  48. Souquiere S, Bibollet-Ruche F, Robertson DL, Makuwa M, Apetrei C, Onanga R et al (2001) Wild Mandrillus sphinx are carriers of two types of lentivirus. J Virol 75:7086–7096CrossRefPubMedGoogle Scholar
  49. Switzer WM, Parekh B, Shanmugam V, Bhullar V, Phillips S, Ely JJ et al (2005) The epidemiology of simian immunodeficiency virus infection in a large number of wild- and captive-born chimpanzees: evidence for a recent introduction following chimpanzee divergence. AIDS Res Hum Retrovir 21:335–342CrossRefPubMedGoogle Scholar
  50. Tazi L, Ayala FJ (2010) Unresolved direction of host transfer of Plasmodium vivax v. P. simium and P. malariae v. P. brasilianum. Infect Genet Evol 11:209–221Google Scholar
  51. Towner JS, Sealy TK, Khristova ML, Albarino CG, Conlan S, Reeder SA et al (2008) Newly discovered Ebola virus associated with hemorrhagic fever outbreak in Uganda. PLoS Pathog 4:e1000212CrossRefPubMedGoogle Scholar
  52. Wachtman LM, Keith GM (2008) Opportunistic infections in immunologically compromised nonhuman primates. ILAR J 49(2):191–208CrossRefPubMedGoogle Scholar
  53. Wallis J, Lee DR (1999) Primate conservation: the prevention of disease transmission. Int J Primatol 20(6):803–826CrossRefGoogle Scholar
  54. Walsh PD, Abernethy KA, Bermejo M, Beyers R, De Wachter P, Ella Akou M et al (2003) Catastrophic ape decline in western equatorial Africa. Nature 422:611–614CrossRefPubMedGoogle Scholar
  55. Walsh PD, Biek R, Real LA (2005) Wave-like spread of Ebola Zaire. PLoS Biol 3:e371CrossRefPubMedGoogle Scholar
  56. Waters AP, Higgins DG, McCutchan TF (1991) Plasmodium falciparum appears to have arisen as a result of lateral transfer between avian and human hosts. Proc Natl Acad Sci U S A 88(8):3140–3144CrossRefPubMedGoogle Scholar
  57. Waters AP, Higgins DG, McCutchan TF (1993) Evolutionary relatedness of some primate models of Plasmodium. Mol Biol Evol 10(4):914–923PubMedGoogle Scholar
  58. White NJ (2008) Plasmodium knowlesi: the fifth human malaria parasite. Clin Infect Dis 46(2):172–173CrossRefPubMedGoogle Scholar
  59. Wittmann TJ, Biek R, Hassanin A, Rouquet P, Reed P, Yaba P et al (2007) Isolates of zaire ebola virus from wild apes reveal genetic lineage and recombinants. Proc Natl Acad Sci U S A 104:17123–17127CrossRefPubMedGoogle Scholar
  60. Wolfe ND, Dunavan CP, Diamond J (2007) The origin of major human infectious diseases. Nature 447:279–283CrossRefPubMedGoogle Scholar
  61. Worobey M, Telfer P, Souquiere S, Hunter M, Coleman CA, Metzger MJ et al (2010) Island biogeography reveals the deep history of SIV. Science 329:1487CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • Jean Paul Gonzalez
    • 1
    • 2
    • 3
    • 4
    Email author
  • Frank Prugnolle
    • 1
    • 2
  • Eric Leroy
    • 1
    • 2
    • 4
  1. 1.International Center for Medical Research of FrancevilleFrancevilleGabon
  2. 2.Institute for Research Development (IRD)Marseille/MontpellierFrance
  3. 3.French Ministry of Foreign OfficeFrench EmbassyLibrevilleGabon
  4. 4.Global Virus Forecasting Inc. (METABIOTA)WashingtonUSA

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