Signatures of oral microbiome in HIV-infected individuals with oral Kaposi's sarcoma and cell-associated KSHV DNA
Autoři:
Marion Gruffaz aff001; Tinghe Zhang aff002; Vickie Marshall aff003; Priscila Gonçalves aff004; Ramya Ramaswami aff004; Nazzarena Labo aff003; Denise Whitby aff003; Thomas S. Uldrick aff004; Robert Yarchoan aff004; Yufei Huang aff002; Shou-Jiang Gao aff001
Působiště autorů:
Department of Molecular Microbiology and Immunology, Keck School of Medicine, University of Southern California, Los Angeles, United States of America
aff001; Department of Electrical and Computer Engineering, University of Texas at San Antonio, San Antonio, Texas, United States of America
aff002; Viral Oncology Section, AIDS and Cancer Virus Program, Leidos Biomedical Research Inc., Frederick National Laboratory for Cancer Research, Frederick, Maryland, United States of America
aff003; HIV and AIDS Malignancy Branch, Center for Cancer Research, National Cancer Institute, Bethesda, Maryland, United States of America
aff004; Fred Hutchinson Cancer Research Center, Seattle, Washington, United States of America
aff005; Department of Epidemiology and Biostatistics, The University of Texas Health San Antonio, San Antonio, Texas, United States of America
aff006; UPMC Hillman Cancer Center, Department of Microbiology and Molecular Genetics, University of Pittsburgh, Pittsburgh, Pennsylvania, United States of America
aff007
Vyšlo v časopise:
Signatures of oral microbiome in HIV-infected individuals with oral Kaposi's sarcoma and cell-associated KSHV DNA. PLoS Pathog 16(1): e32767. doi:10.1371/journal.ppat.1008114
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.ppat.1008114
Souhrn
Infection by Kaposi’s sarcoma-associated herpesvirus (KSHV) is necessary for the development of Kaposi’s sarcoma (KS), which most often develops in HIV-infected individuals. KS frequently has oral manifestations and KSHV DNA can be detected in oral cells. Numerous types of cancer are associated with the alteration of microbiome including bacteria and virus. We hypothesize that oral bacterial microbiota affects or is affected by oral KS and the presence of oral cell-associated KSHV DNA. In this study, oral and blood specimens were collected from a cohort of HIV/KSHV-coinfected individuals all previously diagnosed with KS, and were classified as having oral KS with any oral cell-associated KSHV DNA status (O-KS, n = 9), no oral KS but with oral cell-associated KSHV DNA (O-KSHV, n = 10), or with neither oral KS nor oral cell-associated KSHV DNA (No KSHV, n = 10). We sequenced the hypervariable V1-V2 region of the 16S rRNA gene present in oral cell-associated DNA by next generation sequencing. The diversity, richness, relative abundance of operational taxonomic units (OTUs) and taxonomic composition of oral microbiota were analyzed and compared across the 3 studied groups. We found impoverishment of oral microbial diversity and enrichment of specific microbiota in O-KS individuals compared to O-KSHV or No KSHV individuals. These results suggest that HIV/KSHV coinfection and oral microbiota might impact one another and influence the development of oral KS.
Klíčová slova:
Bacteria – HIV – Kaposi sarcoma – Kaposi's sarcoma-associated herpesvirus – Microbial taxonomy – Microbiome – Species diversity – T cells
Zdroje
1. Greene W, Kuhne K, Ye F, Chen J, Zhou F, Lei X, et al. Molecular biology of KSHV in relation to AIDS-associated oncogenesis. Cancer Treat Res. 2007;133:69–127. Epub 2007/08/04. doi: 10.1007/978-0-387-46816-7_3 17672038; PubMed Central PMCID: PMC2798888.
2. Uldrick TS, Wang V, O'Mahony D, Aleman K, Wyvill KM, Marshall V, et al. An interleukin-6-related systemic inflammatory syndrome in patients co-infected with Kaposi sarcoma-associated herpesvirus and HIV but without Multicentric Castleman disease. Clin Infect Dis. 2010;51(3):350–8. Epub 2010/06/30. doi: 10.1086/654798 20583924; PubMed Central PMCID: PMC2946207.
3. Ye F, Lei X, Gao SJ. Mechanisms of Kaposi's sarcoma-associated herpesvirus latency and reactivation. Adv Virol. 2011;2011. Epub 2011/06/01. doi: 10.1155/2011/193860 21625290; PubMed Central PMCID: PMC3103228.
4. Newton R, Labo N, Wakeham K, Marshall V, Roshan R, Nalwoga A, et al. Determinants of gammaherpesvirus shedding in saliva among Ugandan children and their mothers. J Infect Dis. 2018;218(6):892–900. doi: 10.1093/infdis/jiy262 29762709; PubMed Central PMCID: PMC6093317.
5. Ganem D. KSHV and the pathogenesis of Kaposi sarcoma: listening to human biology and medicine. J Clin Invest. 2010;120(4):939–49. doi: 10.1172/JCI40567 20364091; PubMed Central PMCID: PMC2847423.
6. Pantanowitz L, Khammissa RA, Lemmer J, Feller L. Oral HIV-associated Kaposi sarcoma. J Oral Pathol Med. 2013;42(3):201–7. Epub 2012/06/08. doi: 10.1111/j.1600-0714.2012.01180.x 22672182.
7. Shiels MS, Islam JY, Rosenberg PS, Hall HI, Jacobson E, Engels EA. Projected cancer incidence rates and burden of incident cancer cases in HIV-infected adults in the United States through 2030. Ann Intern Med. 2018;168(12):866–73. doi: 10.7326/M17-2499 29801099.
8. Casper C, Redman M, Huang ML, Pauk J, Lampinen TM, Hawes SE, et al. HIV infection and human herpesvirus-8 oral shedding among men who have sex with men. J Acquir Immune Defic Syndr. 2004;35(3):233–8. doi: 10.1097/00126334-200403010-00003 15076237.
9. IeDEA AI-dCPWGf, EuroCoord Ci. Comparison of Kaposi sarcoma risk in human immunodeficiency virus-positive adults across 5 continents: a multiregional multicohort study. Clin Infect Dis. 2017;65(8):1316–26. doi: 10.1093/cid/cix480 28531260; PubMed Central PMCID: PMC5850623.
10. Leidner RS, Aboulafia DM. Recrudescent Kaposi's sarcoma after initiation of HAART: a manifestation of immune reconstitution syndrome. AIDS Patient Care STDS. 2005;19(10):635–44. Epub 2005/10/20. doi: 10.1089/apc.2005.19.635 16232048.
11. Hosseinipour MC, Kang M, Krown SE, Bukuru A, Umbleja T, Martin JN, et al. As-needed vs immediate etoposide chemotherapy in combination with antiretroviral therapy for mild-to-moderate AIDS-associated Kaposi sarcoma in resource-limited settings: A5264/AMC-067 randomized clinical trial. Clin Infect Dis. 2018;67(2):251–60. doi: 10.1093/cid/ciy044 29365083; PubMed Central PMCID: PMC6030807.
12. Labo N, Miley W, Benson CA, Campbell TB, Whitby D. Epidemiology of Kaposi's sarcoma-associated herpesvirus in HIV-1-infected US persons in the era of combination antiretroviral therapy. AIDS. 2015;29(10):1217–25. doi: 10.1097/QAD.0000000000000682 26035321.
13. Hugerth LW, Andersson AF. Analysing microbial community composition through amplicon sequencing: from sampling to hypothesis testing. Front Microbiol. 2017;8:1561. Epub 2017/09/21. doi: 10.3389/fmicb.2017.01561 28928718; PubMed Central PMCID: PMC5591341.
14. Moyes DL, Saxena D, John MD, Malamud D. The gut and oral microbiome in HIV disease: a workshop report. Oral Dis. 2016;22 Suppl 1:166–70. doi: 10.1111/odi.12415 27109284.
15. Schwabe RF, Jobin C. The microbiome and cancer. Nat Rev Cancer. 2013;13(11):800–12. Epub 2013/10/18. doi: 10.1038/nrc3610 24132111; PubMed Central PMCID: PMC3986062.
16. Bullman S, Pedamallu CS, Sicinska E, Clancy TE, Zhang X, Cai D, et al. Analysis of Fusobacterium persistence and antibiotic response in colorectal cancer. Science. 2017;358(6369):1443–8. Epub 2017/11/25. doi: 10.1126/science.aal5240 29170280; PubMed Central PMCID: PMC5823247.
17. Watari J, Chen N, Amenta PS, Fukui H, Oshima T, Tomita T, et al. Helicobacter pylori associated chronic gastritis, clinical syndromes, precancerous lesions, and pathogenesis of gastric cancer development. World J Gastroenterol. 2014;20(18):5461–73. Epub 2014/05/17. doi: 10.3748/wjg.v20.i18.5461 24833876; PubMed Central PMCID: PMC4017061.
18. Shannon BA, Garrett KL, Cohen RJ. Links between Propionibacterium acnes and prostate cancer. Future Oncol. 2006;2(2):225–32. Epub 2006/03/28. doi: 10.2217/14796694.2.2.225 16563091.
19. Fais T, Delmas J, Cougnoux A, Dalmasso G, Bonnet R. Targeting colorectal cancer-associated bacteria: A new area of research for personalized treatments. Gut Microbes. 2016;7(4):329–33. Epub 2016/03/24. doi: 10.1080/19490976.2016.1155020 27007710; PubMed Central PMCID: PMC4988430.
20. Gruffaz M, Vasan K, Tan B, Ramos da Silva S, Gao SJ. TLR4-mediated inflammation promotes KSHV-induced cellular transformation and tumorigenesis by activating the STAT3 pathway. Cancer Res. 2017;77(24):7094–108. Epub 2017/10/21. doi: 10.1158/0008-5472.CAN-17-2321 29051178; PubMed Central PMCID: PMC5732873.
21. Yu X, Shahir AM, Sha J, Feng Z, Eapen B, Nithianantham S, et al. Short-chain fatty acids from periodontal pathogens suppress histone deacetylases, EZH2, and SUV39H1 to promote Kaposi's sarcoma-associated herpesvirus replication. J Virol. 2014;88(8):4466–79. Epub 2014/02/07. doi: 10.1128/JVI.03326-13 24501407; PubMed Central PMCID: PMC3993761.
22. Gorres KL, Daigle D, Mohanram S, Miller G. Activation and repression of Epstein-Barr virus and Kaposi's sarcoma-associated herpesvirus lytic cycles by short- and medium-chain fatty acids. J Virol. 2014;88(14):8028–44. Epub 2014/05/09. doi: 10.1128/JVI.00722-14 24807711; PubMed Central PMCID: PMC4097796.
23. Mataftsi M, Skoura L, Sakellari D. HIV infection and periodontal diseases: an overview of the post-HAART era. Oral Dis. 2011;17(1):13–25. Epub 2010/10/30. doi: 10.1111/j.1601-0825.2010.01727.x 21029260.
24. Gandhi M, Koelle DM, Ameli N, Bacchetti P, Greenspan JS, Navazesh M, et al. Prevalence of human herpesvirus-8 salivary shedding in HIV increases with CD4 count. J Dent Res. 2004;83(8):639–43. doi: 10.1177/154405910408300811 15271974.
25. Guadalupe M, Pollock BH, Westbrook S, Redding S, Bullock D, Anstead G, et al. Risk factors influencing antibody responses to Kaposi's sarcoma-associated herpesvirus latent and lytic antigens in patients under antiretroviral therapy. J Acquir Immune Defic Syndr. 2011;56(1):83–90. doi: 10.1097/QAI.0b013e3181fdc928 21084997; PubMed Central PMCID: PMC3051282.
26. Bik EM, Long CD, Armitage GC, Loomer P, Emerson J, Mongodin EF, et al. Bacterial diversity in the oral cavity of 10 healthy individuals. ISME J. 2010;4(8):962–74. Epub 2010/03/26. doi: 10.1038/ismej.2010.30 20336157; PubMed Central PMCID: PMC2941673.
27. Verma D, Garg PK, Dubey AK. Insights into the human oral microbiome. Arch Microbiol. 2018;200(4):525–40. Epub 2018/03/25. doi: 10.1007/s00203-018-1505-3 29572583.
28. Gopalakrishnan V, Spencer CN, Nezi L, Reuben A, Andrews MC, Karpinets TV, et al. Gut microbiome modulates response to anti-PD-1 immunotherapy in melanoma patients. Science. 2018;359(6371):97–103. doi: 10.1126/science.aan4236 29097493; PubMed Central PMCID: PMC5827966.
29. Goodman B, Gardner H. The microbiome and cancer. J Pathol. 2018;244(5):667–76. Epub 2018/01/30. doi: 10.1002/path.5047 29377130.
30. Aviles-Jimenez F, Yu G, Torres-Poveda K, Madrid-Marina V, Torres J. On the Search to Elucidate the Role of Microbiota in the Genesis of Cancer: The Cases of Gastrointestinal and Cervical Cancer. Arch Med Res. 2017;48(8):754–65. Epub 2017/12/06. doi: 10.1016/j.arcmed.2017.11.008 29203054.
31. Routy B, Le Chatelier E, Derosa L, Duong CPM, Alou MT, Daillere R, et al. Gut microbiome influences efficacy of PD-1-based immunotherapy against epithelial tumors. Science. 2018;359(6371):91–7. doi: 10.1126/science.aan3706 29097494.
32. Thomson PJ. Perspectives on oral squamous cell carcinoma prevention-proliferation, position, progression and prediction. J Oral Pathol Med. 2018. Epub 2018/05/13. doi: 10.1111/jop.12733 29752860.
33. Shiga K, Tateda M, Saijo S, Hori T, Sato I, Tateno H, et al. Presence of Streptococcus infection in extra-oropharyngeal head and neck squamous cell carcinoma and its implication in carcinogenesis. Oncol Rep. 2001;8(2):245–8. Epub 2001/02/22. 11182034.
34. Mager DL, Haffajee AD, Devlin PM, Norris CM, Posner MR, Goodson JM. The salivary microbiota as a diagnostic indicator of oral cancer: a descriptive, non-randomized study of cancer-free and oral squamous cell carcinoma subjects. J Transl Med. 2005;3:27. Epub 2005/07/01. doi: 10.1186/1479-5876-3-27 15987522; PubMed Central PMCID: PMC1226180.
35. Guerrero-Preston R, Godoy-Vitorino F, Jedlicka A, Rodriguez-Hilario A, Gonzalez H, Bondy J, et al. 16S rRNA amplicon sequencing identifies microbiota associated with oral cancer, human papilloma virus infection and surgical treatment. Oncotarget. 2016;7(32):51320–34. Epub 2016/06/05. doi: 10.18632/oncotarget.9710 27259999; PubMed Central PMCID: PMC5239478.
36. Chen W, Liu F, Ling Z, Tong X, Xiang C. Human intestinal lumen and mucosa-associated microbiota in patients with colorectal cancer. PLoS One. 2012;7(6):e39743. Epub 2012/07/05. doi: 10.1371/journal.pone.0039743 22761885; PubMed Central PMCID: PMC3386193.
37. Kilian M, Chapple IL, Hannig M, Marsh PD, Meuric V, Pedersen AM, et al. The oral microbiome—an update for oral healthcare professionals. Br Dent J. 2016;221(10):657–66. Epub 2016/11/20. doi: 10.1038/sj.bdj.2016.865 27857087.
38. Passariello C, Gigola P, Testarelli L, Puttini M, Schippa S, Petti S. Evaluation of microbiota associated with Herpesviruses in active sites of generalized aggressive periodontitis. Ann Stomatol (Roma). 2017;8(2):59–70. Epub 2018/01/05. doi: 10.11138/ads/2017.8.2.071 29299190; PubMed Central PMCID: PMC5749375.
39. Lewy T, Hong BY, Weiser B, Burger H, Tremain A, Weinstock G, et al. Oral microbiome in HIV-infected women: Shifts in the abundance of pathogenic and beneficial bacteria are associated with aging, HIV load, CD4 count, and ART. AIDS Res Hum Retroviruses. 2018. Epub 2018/05/29. doi: 10.1089/AID.2017.0200 29808701.
40. Noguera-Julian M, Guillen Y, Peterson J, Reznik D, Harris EV, Joseph SJ, et al. Oral microbiome in HIV-associated periodontitis. Medicine (Baltimore). 2017;96(12):e5821. Epub 2017/03/23. doi: 10.1097/MD.0000000000005821 28328799; PubMed Central PMCID: PMC5371436.
41. Starr JR, Huang Y, Lee KH, Murphy CM, Moscicki AB, Shiboski CH, et al. Oral microbiota in youth with perinatally acquired HIV infection. Microbiome. 2018;6(1):100. Epub 2018/06/02. doi: 10.1186/s40168-018-0484-6 29855347; PubMed Central PMCID: PMC5984365.
42. Presti RM, Handley SA, Droit L, Ghannoum M, Jacobson M, Shiboski CH, et al. Alterations in the oral microbiome in HIV-infected participants after antiretroviral therapy administration are influenced by immune status. AIDS. 2018;32(10):1279–87. Epub 2018/06/01. doi: 10.1097/QAD.0000000000001811 29851662.
43. Gaboriau-Routhiau V, Rakotobe S, Lecuyer E, Mulder I, Lan A, Bridonneau C, et al. The key role of segmented filamentous bacteria in the coordinated maturation of gut helper T cell responses. Immunity. 2009;31(4):677–89. Epub 2009/10/17. doi: 10.1016/j.immuni.2009.08.020 19833089.
44. Arpaia N, Campbell C, Fan X, Dikiy S, van der Veeken J, deRoos P, et al. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature. 2013;504(7480):451–5. Epub 2013/11/15. doi: 10.1038/nature12726 24226773; PubMed Central PMCID: PMC3869884.
45. Qiu X, Zhang M, Yang X, Hong N, Yu C. Faecalibacterium prausnitzii upregulates regulatory T cells and anti-inflammatory cytokines in treating TNBS-induced colitis. J Crohns Colitis. 2013;7(11):e558–68. Epub 2013/05/07. doi: 10.1016/j.crohns.2013.04.002 23643066.
46. Atarashi K, Tanoue T, Oshima K, Suda W, Nagano Y, Nishikawa H, et al. Treg induction by a rationally selected mixture of Clostridia strains from the human microbiota. Nature. 2013;500(7461):232–6. Epub 2013/07/12. doi: 10.1038/nature12331 23842501.
47. Ganem D. KSHV-induced oncogenesis. In: Arvin A, Campadelli-Fiume G, Mocarski E, Moore PS, Roizman B, Whitley R, et al., editors. Human Herpesviruses: Biology, Therapy, and Immunoprophylaxis. Cambridge2007.
48. Niederman R, Buyle-Bodin Y, Lu BY, Robinson P, Naleway C. Short-chain carboxylic acid concentration in human gingival crevicular fluid. J Dent Res. 1997;76(1):575–9. Epub 1997/01/01. doi: 10.1177/00220345970760010801 9042080.
49. Orbe-Orihuela YC, Lagunas-Martinez A, Bahena-Roman M, Madrid-Marina V, Torres-Poveda K, Flores-Alfaro E, et al. High relative abundance of firmicutes and increased TNF-alpha levels correlate with obesity in children. Salud Publica Mex. 2018;60(1):5–11. Epub 2018/04/25. doi: 10.21149/8133 29689651.
50. Krown SE, Testa MA, Huang J. AIDS-related Kaposi's sarcoma: prospective validation of the AIDS Clinical Trials Group staging classification. AIDS Clinical Trials Group Oncology Committee. J Clin Oncol. 1997;15(9):3085–92. doi: 10.1200/JCO.1997.15.9.3085 9294471.
51. Polizzotto MN, Uldrick TS, Wyvill KM, Aleman K, Peer CJ, Bevans M, et al. Pomalidomide for symptomatic Kaposi's sarcoma in people with and without HIV infection: a phase I/II study. J Clin Oncol. 2016;34(34):4125–31. doi: 10.1200/JCO.2016.69.3812 27863194; PubMed Central PMCID: PMC5477825.
52. Yuan CC, Miley W, Waters D. A quantification of human cells using an ERV-3 real time PCR assay. J Virol Methods. 2001;91(2):109–17. doi: 10.1016/s0166-0934(00)00244-5 11164492.
53. Youssef N, Sheik CS, Krumholz LR, Najar FZ, Roe BA, Elshahed MS. Comparison of species richness estimates obtained using nearly complete fragments and simulated pyrosequencing-generated fragments in 16S rRNA gene-based environmental surveys. Appl Environ Microbiol. 2009;75(16):5227–36. Epub 2009/06/30. doi: 10.1128/AEM.00592-09 19561178; PubMed Central PMCID: PMC2725448.
54. Brown J, Pirrung M, McCue LA. FQC Dashboard: integrates FastQC results into a web-based, interactive, and extensible FASTQ quality control tool. Bioinformatics. 2017. Epub 2017/06/13. doi: 10.1093/bioinformatics/btx373 28605449; PubMed Central PMCID: PMC5870778.
55. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7(5):335–6. Epub 2010/04/13. doi: 10.1038/nmeth.f.303 20383131; PubMed Central PMCID: PMC3156573.
56. Hu J, Koh H, He L, Liu M, Blaser MJ, Li H. A two-stage microbial association mapping framework with advanced FDR control. Microbiome. 2018;6(1):131. doi: 10.1186/s40168-018-0517-1 30045760; PubMed Central PMCID: PMC6060480.
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