Assessment of the gorilla gut virome in association with natural simian immunodeficiency virus infection

Retrovirology

Volumn 15, Issue 1, 2018, Pages

  D'arc, Mirela ^a,b   Furtado, Carolina ^a   Siqueira, Juliana D ^a   Seuánez, Héctor N ^a,b   Ayouba, Ahidjo ^c   Peeters, Martine ^c   Soares, Marcelo A ^a,b  

^a INSTITUTO NACIONAL DE CÂNCER   (Brazil)

^b FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^c UNIV MONTPELLIER   (France)

Author keywords

Dysbiosis; Gorilla; Pathogenesis; SIVgor; Virome

Indexed keywords

ARTICLE; CONTROLLED STUDY; DYSBIOSIS; GORILLA; GUT VIROME; HERPESVIRIDAE; INTESTINE FLORA; MICROBIAL DIVERSITY; MICROBIOME; NEXT GENERATION SEQUENCING; NONHUMAN; PATHOGENESIS; POPULATION ABUNDANCE; REOVIRIDAE; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; VIRUS IDENTIFICATION; ANIMAL; BIODIVERSITY; BLOOD; CLASSIFICATION; CLUSTER ANALYSIS; COMPARATIVE STUDY; COMPLICATION; FECES; GENETICS; GORILLA GORILLA; PATHOGENICITY; VIROLOGY; VIRUS; VIRUS LOAD; WILD ANIMAL;

VIRUS ANTIBODY; VIRUS ANTIGEN;

ANIMALS; ANIMALS, WILD; ANTIBODIES, VIRAL; ANTIGENS, VIRAL; BIODIVERSITY; CLUSTER ANALYSIS; DYSBIOSIS; FECES; GASTROINTESTINAL MICROBIOME; GORILLA GORILLA; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; VIRAL LOAD; VIRUSES;

EID: 85041387387     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/s12977-018-0402-9     Document Type: Article

References (52)

1. Keele BF, Van Heuverswyn F, Li Y, Bailes E, Takehisa J, Santiago ML, et al. Chimpanzee reservoirs of pandemic and nonpandemic HIV-1. Science. 2006;313:523-6.
2. D'arc M, Ayouba A, Esteban A, Learn GH, Boué V, Liegeois F, et al. Origin of the HIV-1 group O epidemic in western lowland gorillas. Proc Natl Acad Sci. 2015;112:E1343-52.
3. Santiago ML, Range F, Keele BF, Li Y, Bailes E, Bibollet-Ruche F, et al. Simian immunodeficiency virus infection in free-ranging sooty mangabeys (Cercocebus atys atys) from the Taï Forest, Côte d'Ivoire: implications for the origin of epidemic human immunodeficiency virus type 2. J Virol. 2005;79:12515-27.
4. Sharp PM, Bailes E, Chaudhuri RR, Rodenburg CM, Santiago MO, Hahn BH. The origins of acquired immune deficiency syndrome viruses: where and when? Philos Trans R Soc Lond B Biol Sci. 2001;356:867-76.
5. Ayouba A, Akoua-Koffi C, Calvignac-Spencer S, Esteban A, Locatelli S, Li H, et al. Evidence for continuing cross-species transmission of SIVsmm to humans: characterization of a new HIV-2 lineage in rural Côte d'Ivoire. AIDS. 2013;27:2488-91.
6. Peeters M, D'Arc M, Delaporte E. The origin and diversity of human retroviruses. AIDS Rev. 2014;16:23-34.
7. Paiardini M, Pandrea I, Apetrei C, Silvestri G. Lessons learned from the natural hosts of HIV-related viruses. Annu Rev Med. 2009;60:485-95.
8. Silvestri G. Naturally SIV-infected sooty mangabeys: are we closer to understanding why they do not develop AIDS? J Med Primatol. 2005;34:243-52.
9. Silvestri G. Immunity in natural SIV infections. J Int Med. 2009;265:97-109.
10. Daniel MD, Letvin NL, King NW, Kannagi M, Sehgal PK, Hunt RD, et al. Isolation of T-cell tropic HTLV-III-like retrovirus from macaques. Science. 1985;228:1201-4.
11. Kanki PJ, McLane MF, King NW, Letvin NL, Hunt RD, Sehgal P, et al. Serologic identification and characterization of a macaque T-lymphotropic retrovirus closely related to HTLV-III. Science. 1985;228:1199-201.
12. Keele BF, Jones JH, Terio KA, Estes JD, Rudicell RS, Wilson ML, et al. Increased mortality and AIDS-like immunopathology in wild chimpanzees infected with SIVcpz. Nature. 2009;460:515-9.
13. Rudicell RS, Holland Jones J, Wroblewski EE, Learn GH, Li Y, Robertson JD, et al. Impact of simian immunodeficiency virus infection on chimpanzee population dynamics. PLoS Pathog. 2010;6:e1001116.
14. Etienne L, Nerrienet E, LeBreton M, Bibila GT, Foupouapouognigni Y, Rousset D, et al. Characterization of a new simian immunodeficiency virus strain in a naturally infected Pan troglodytes troglodytes chimpanzee with AIDS related symptoms. Retrovirology. 2011;8:4.
15. Sharp PM, Hahn BH. Origins of HIV and the AIDS pandemic. Cold Spring Harb Perspect Med. 2011;1:a006841.
16. Monaco CL, Gootenberg DB, Zhao G, Handley SA, Ghebremichael MS, Lim ES, et al. Altered virome and bacterial microbiome in human immunodeficiency virus-associated acquired immunodeficiency syndrome. Cell Host Microbe. 2016;19:311-22.
17. Moeller AH, Shilts M, Li Y, Rudicell RS, Lonsdorf EV, Pusey AE, et al. SIV-induced instability of the chimpanzee gut microbiome. Cell Host Microbe. 2013;14:340-5.
18. Moeller AH, Peeters M, Ayouba A, Ngole EM, Esteban A, Hahn BH, et al. Stability of the gorilla microbiome despite simian immunodeficiency virus infection. Mol Ecol. 2015;24:690-7.
19. Handley SA, Thackray LB, Zhao G, Presti R, Miller AD, Droit L, et al. Pathogenic simian immunodeficiency virus infection is associated with expansion of the enteric virome. Cell. 2012;151:253-66.
20. Etienne L, Locatelli S, Ayouba A, Esteban A, Butel C, Liegeois F, et al. Noninvasive follow-up of simian immunodeficiency virus infection in wild-living nonhabituated western lowland gorillas in Cameroon. J Virol. 2012;86:9760-72.
21. Neel C, Etienne L, Li Y, Takehisa J, Rudicell RS, Bass IN, et al. Molecular epidemiology of simian immunodeficiency virus infection in wild-living gorillas. J Virol. 2010;84:1464-76.
22. Van Heuverswyn F, Li Y, Neel C, Bailes E, Keele BF, Liu W, et al. Human immunodeficiency viruses: SIV infection in wild gorillas. Nature. 2006;444:164.
23. Etienne L, Eymard-Duvernay S, Aghokeng A, Butel C, Monleau M, Peeters M. Single real-time reverse transcription-PCR assay for detection and quantification of genetically diverse HIV-1, SIVcpz, and SIVgor strains. J Clin Microbiol. 2013;51:787-98.
24. Takehisa J, Kraus MH, Ayouba A, Bailes E, Van Heuverswyn F, Decker JM, et al. Origin and biology of simian immunodeficiency virus in wild-living western gorillas. J Virol. 2009;83:1635-48.
25. Joshi N, Sickle FJ.: A sliding-window, adaptive, quality-based trimming tool for FastQ files. https://github.com/najoshi/sickle (2011). Accessed 15 Jan 2015.
26. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215:403-10.
27. Brenchley JM, Price DA, Schacker TW, Asher TE, Silvestri G, Rao S, et al. Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat Med. 2006;12:1365-71.
28. Cotten M, Oude Munnink B, Canuti M, Deijs M, Watson SJ, Kellam P, et al. Full genome virus detection in fecal samples using sensitive nucleic acid preparation, deep sequencing, and a novel iterative sequence classification algorithm. PLoS ONE. 2014;2:e93269.
29. Cunningham AL, Grohman GS, Harkness J, Law C, Marriott D, Tindall B, et al. Gastrointestinal viral infections in homosexual men who were symptomatic and seropositive for human immunodeficiency virus. J Infect Dis. 1988;158:386-91.
30. Gilger MA, Matson DO, Conner ME, Rosenblatt HM, Finegold MJ, Estes MK. Extraintestinal rotavirus infections in children with immunodeficiency. J Pediatr. 1992;120:912-7.
31. Handley SA. The virome: a missing component of biological interaction networks in health and disease. Genome Med. 2016;8:32.
32. Li SK, Leung RKK, Guo HX, Wei JF, Wang JH, Kwong KT, et al. Detection and identification of plasma bacterial and viral elements in HIV/AIDS patients in comparison to healthy adults. Clin Microbiol Infect. 2012;18:1126-33.
33. Marchetti G, Tincati C, Silvestri G. Microbial translocation in the pathogenesis of HIV infection and AIDS. Clin Microbiol Rev. 2013;26:2-18.
34. Minot S, Bryson A, Chehoud C, Wu GD, Lewis JD, Bushman FD. Rapid evolution of the human gut virome. Proc Natl Acad Sci USA. 2013;110:12450-5.
35. Naeger DM, Martin JN, Sinclair E, Hunt PW, Bangsberg DR, Hecht F, et al. Cytomegalovirus-specific T cells persist at very high levels during long-term antiretroviral treatment of HIV disease. PLoS ONE. 2010;29(5):e8886.
36. Sandler NG, Douek DC. Microbial translocation in HIV infection: causes, consequences and treatment opportunities. Nat Rev Microbiol. 2012;10:655-66.
37. Springer KL, Weinberg A. Cytomegalovirus infection in the era of HAART: fewer reactivations and more immunity. J Antimicrob Chemother. 2004;54:582-6.
38. Williams B, Landay A, Presti RM. Microbiome alterations in HIV infection a review. Cell Microbiol. 2016;18:645-51.
39. Zou S, Caler L, Colombini-Hatch S, Glynn S, Srinivas P. Research on the human virome: where are we and what is next. Microbiome. 2016;24(4):32.
40. Chang Y, Cesarman E, Pessin MS, Lee F, Culpepper J, Knowles DM, et al. Identification of herpesvirus-like DNA sequences in AIDS-associated Kaposi's sarcoma. Science. 1994;266:1865-9.
41. Giordano MO, Martinez LC, Rinaldi D, Gúinard S, Naretto E, Casero R, et al. Detection of picobirnavirus in HIV-infected patients with diarrhea in Argentina. J Acquir Immune Defic Syndr Hum Retrovirol. 1998;18:380-3.
42. González GG, Pujol FH, Liprandi F, Deibis L, Ludert JE. Prevalence of enteric viruses in human immunodeficiency virus seropositive patients in Venezuela. J Med Virol. 1998;55:288-92.
43. Raini SK, Nyangao J, Kombich J, Sang C, Gikonyo J, Ongus JR, et al. Human rotavirus group a serotypes causing gastroenteritis in children less than 5 years and HIV-infected adults in Viwandani slum, Nairobi. Ethiop J Health Sci. 2015;25:39-46.
44. Stevens SJC, Blank BSN, Smits PHM, Meenhorst PL, Middeldorp JM. High Epstein-Barr virus (EBV) DNA loads in HIV-infected patients: correlation with antiretroviral therapy and quantitative EBV serology. AIDS. 2002;16:993-1001.
45. Minot S, Sinha R, Chen J, Li H, Keilbaugh SA, Wu GD, et al. The human gut virome: inter-individual variation and dynamic response to diet. Genome Res. 2011;21:1616-25.
46. Zhang T, Breitbart M, Lee WH, Run J-Q, Wei CL, Soh SWL, et al. RNA viral community in human feces: prevalence of plant pathogenic viruses. PLoS Biol. 2006;4:e3.
47. Moeller AH, Peeters M, Ndjango JB, Li Y, Hahn BH, Ochman H. Sympatric chimpanzees and gorillas harbor convergent gut microbial communities. Genome Res. 2013;23:1715-20.
48. Hazenberg MD, Otto SA, van Benthem BHB, Roos MTL, Coutinho RA, Lange JMA, et al. Persistent immune activation in HIV-1 infection is associated with progression to AIDS. AIDS. 2003;17:1881-8.
49. Brenchley JM, Silvestri G, Douek DC. Nonprogressive and progressive primate immunodeficiency lentivirus infections. Immunity. 2010;32:737-42.
50. Terio KA, Kinsel MJ, Raphael J, Mlengeya T, Lipende I, Kirchhoff CA, et al. Pathologic lesions in chimpanzees (Pan trogylodytes schweinfurthii) from Gombe National Park, Tanzania, 2004-2010. J Zoo Wildl Med. 2011;42:597-607.
51. Barbian HJ, Li Y, Ramirez M, Klase Z, Lipende I, Mjungu D, et al. Destabilization of the gut microbiome marks the end-stage of simian immunodeficiency virus infection in wild chimpanzees. Am J Primatol. 2015. https://doi.org/10.1002/ajp.22515.
52. Moeller AH, Peeters M, Ayouba A, Ngole EM, Esteban A, Hahn BH, et al. Stability of the gorilla microbiome despite simian immunodeficiency virus infection. Mol Ecol. 2015;24:690-7.