Our laboratory specializes in mass spectrometry based proteomics and systems biology to study host immunity, the microbiome, and interactions in disease. A central focus of our research has been to study host and microbial factors at mucosal surfaces that underlie susceptibility to infectious disease and cancer.
Research Information
Research Interests
Our laboratory specializes in mass spectrometry based on proteomics and systems biology to study host immunity, the microbiome, and interactions in infectious diseases. A central focus of our research has been to study host and microbial factors at mucosal surfaces that underlie the acquisition and pathogenesis of HIV. The goal is to apply this knowledge to develop novel preventative, diagnostic, and therapeutic strategies. Our program works in close collaboration and partnership with many domestic and international institutions, and clinical cohorts from Africa, United States, Sweden, and Canada.
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Publications
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Tanko RF, Bunjun R, Dabee S, Jaumdally SZ, Onono M, Nair G, Palanee-Phillips T, Harryparsad R, Happel AU, Gamieldien H, Qumbelo Y, Sinkala M, Scoville CW, Heller K, Baeten JM, Bosinger SE, Burgener A, Heffron R, Jaspan HB, Passmore JAS. The Effect of Contraception on Genital Cytokines in Women Randomized to Copper Intrauterine Device, Depot Medroxyprogesterone Acetate, or Levonorgestrel Implant. J Infect Dis. 2022 Sep 13;226(5):907-919. doi: 10.1093/infdis/jiac084. PubMed PMID: 35263421; PubMed Central PMCID: PMC9470113.
Ferrari B, Da Silva AC, Liu KH, Saidakova EV, Korolevskaya LB, Shmagel KV, Shive C, Pacheco Sanchez G, Retuerto M, Sharma AA, Ghneim K, Noel-Romas L, Rodriguez B, Ghannoum MA, Hunt PP, Deeks SG, Burgener AD, Jones DP, Dobre MA, Marconi VC, Sekaly RP, Younes SA. Gut-derived bacterial toxins impair memory CD4+ T cell mitochondrial function in HIV-1 infection. J Clin Invest. 2022 May 2;132(9). doi: 10.1172/JCI149571. PubMed PMID: 35316209; PubMed Central PMCID: PMC9057623.
Borgognone A, Noguera-Julian M, Oriol B, Noël-Romas L, Ruiz-Riol M, Guillén Y, Parera M, Casadellà M, Duran C, Puertas MC, Català -Moll F, De Leon M, Knodel S, Birse K, Manzardo C, Miró JM, Clotet B, Martinez-Picado J, Moltó J, Mothe B, Burgener A, Brander C, Paredes R. Gut microbiome signatures linked to HIV-1 reservoir size and viremia control. Microbiome. 2022 Apr 11;10(1):59. doi: 10.1186/s40168-022-01247-6. PubMed PMID: 35410461; PubMed Central PMCID: PMC9004083.
Shvartsman E, Richmond MEI, Schellenberg JJ, Lamont A, Perciani C, Russell JNH, Poliquin V, Burgener A, Jaoko W, Sandstrom P, MacDonald KS. Comparative analysis of DNA extraction and PCR product purification methods for cervicovaginal microbiome analysis using cpn60 microbial profiling. PLoS One. 2022;17(1):e0262355. doi: 10.1371/journal.pone.0262355. eCollection 2022. PubMed PMID: 35025956; PubMed Central PMCID: PMC8758110.
Berard AR, Miller C, AraÃnga M, Broedlow CA, Noël-Romas L, Schifanella L, Hensley-McBain T, Roederer A, Driscoll CB, Coronado E, Manuzak J, McKinnon LR, Villinger F, Hope TJ, Burgener AD, Klatt NR. Simian Immunodeficiency Virus Susceptibility, Immunology, and Microbiome in the Female Genital Tract of Adolescent Versus Adult Pigtail Macaques. AIDS Res Hum Retroviruses. 2021 Jul;37(7):510-522. doi: 10.1089/AID.2020.0271. Epub 2021 Jun 22. PubMed PMID: 33446027; PubMed Central PMCID: PMC8260895.
Rizzo AE, Gordon JC, Berard AR, Burgener AD, Avril S. The Female Reproductive Tract Microbiome-Implications for Gynecologic Cancers and Personalized Medicine. J Pers Med. 2021 Jun 11;11(6). doi: 10.3390/jpm11060546. Review. PubMed PMID: 34208337; PubMed Central PMCID: PMC8231212.
Svanberg C, Ellegård R, Crisci E, Khalid M, Borendal Wodlin N, Svenvik M, Nyström S, Birse K, Burgener A, Shankar EM, Larsson M. Complement-Opsonized HIV Modulates Pathways Involved in Infection of Cervical Mucosal Tissues: A Transcriptomic and Proteomic Study. Front Immunol. 2021;12:625649. doi: 10.3389/fimmu.2021.625649. eCollection 2021. PubMed PMID: 34093520; PubMed Central PMCID: PMC8173031.
Farr Zuend C, Noël-Romas L, Hoger S, McCorriser S, Westmacott G, Marrazzo J, Hillier SL, Dezzutti C, Squires K, Bunge KE, Burgener A. Influence of dapivirine vaginal ring use on cervicovaginal immunity and functional microbiome in adolescent girls. AIDS. 2021 Mar 1;35(3):369-380. doi: 10.1097/QAD.0000000000002751. PubMed PMID: 33181534; PubMed Central PMCID: PMC7924934.
Noël-Romas L, Perner M, Molatlhegi R, Farr Zuend C, Mabhula A, Hoger S, Lamont A, Birse K, Berard A, McCorrister S, Westmacott G, Leslie A, Poliquin V, Heffron R, McKinnon LR, Burgener AD. Vaginal microbiome-hormonal contraceptive interactions associate with the mucosal proteome and HIV acquisition. PLoS Pathog. 2020 Dec;16(12):e1009097. doi: 10.1371/journal.ppat.1009097. eCollection 2020 Dec. PubMed PMID: 33362285; PubMed Central PMCID: PMC7790405.
Hughes SM, Levy CN, Calienes FL, Stekler JD, Pandey U, Vojtech L, Berard AR, Birse K, Noël-Romas L, Richardson B, Golden JB, Cartwright M, Collier AC, Stevens CE, Curlin ME, Holtz TH, Mugo N, Irungu E, Katabira E, Muwonge T, Lama JR, Baeten JM, Burgener A, Lingappa JR, McElrath MJ, Mackelprang R, McGowan I, Cranston RD, Cameron MJ, Hladik F. Treatment with Commonly Used Antiretroviral Drugs Induces a Type I/III Interferon Signature in the Gut in the Absence of HIV Infection. Cell Rep Med. 2020 Sep 22;1(6):100096. doi: 10.1016/j.xcrm.2020.100096. PubMed PMID: 33015651; PubMed Central PMCID: PMC7511692.
SahBandar IN, Chew GM, Corley MJ, Pang APS, Tsai N, Hanks N, Khadka VS, Klatt NR, Hensley-McBain T, Somsouk M, Vujkovic-Cvijin I, Chow DC, Shikuma CM, Ndhlovu LC. Changes in gastrointestinal microbial communities influence HIV-specific CD8+ T-cell responsiveness to immune checkpoint blockade. AIDS. 2020 Aug 1;34(10):1451-1460. doi: 10.1097/QAD.0000000000002557. PubMed PMID: 32675558; PubMed Central PMCID: PMC7371239.
Farr Zuend C, Tobin NH, Vera T, Kotyrba L, Noël-Romas L, Birse K, Mutch S, Li F, Lee D, McCorrister S, Westmacott G, Aldrovandi GM, Burgener AD. Pregnancy associates with alterations to the host and microbial proteome in vaginal mucosa. Am J Reprod Immunol. 2020 Jun;83(6):e13235. doi: 10.1111/aji.13235. Epub 2020 Apr 9. PubMed PMID: 32196803; PubMed Central PMCID: PMC7317380.
Birse KD, Kratzer K, Zuend CF, Mutch S, Noël-Romas L, Lamont A, Abou M, Jalil E, Veloso V, Grinsztejn B, Friedman RK, Broliden K, Bradley F, Poliquin V, Li F, Yanavich C, Burgener A, Aldrovandi G. The neovaginal microbiome of transgender women post-gender reassignment surgery. Microbiome. 2020 May 5;8(1):61. doi: 10.1186/s40168-020-00804-1. PubMed PMID: 32370783; PubMed Central PMCID: PMC7201977.
Molatlhegi RP, Liebenberg LJ, Leslie A, Noel-Romas L, Mabhula A, Mchunu N, Perner M, Birse K, Ngcapu S, Adamson JH, Govender K, Garrett NJ, Samsunder N, Burgener AD, Abdool Karim SS, Abdool Karim Q, Passmore JS, McKinnon LR. Plasma concentration of injectable contraceptive correlates with reduced cervicovaginal growth factor expression in South African women. Mucosal Immunol. 2020 May;13(3):449-459. doi: 10.1038/s41385-019-0249-y. Epub 2020 Jan 2. PubMed PMID: 31896762.
Manuzak JA, Zevin AS, Cheu R, Richardson B, Modesitt J, Hensley-McBain T, Miller C, Gustin AT, Coronado E, Gott T, Fang M, Cartwright M, Wangari S, Agricola B, May D, Smith E, Hampel HB, Gale M, Cameron CM, Cameron MJ, Smedley J, Klatt NR. Antibiotic-induced microbiome perturbations are associated with significant alterations to colonic mucosal immunity in rhesus macaques. Mucosal Immunol. 2020 May;13(3):471-480. doi: 10.1038/s41385-019-0238-1. Epub 2019 Dec 4. PubMed PMID: 31797911; PubMed Central PMCID: PMC7183431.
Günaydın G, Edfeldt G, Garber DA, Asghar M, Noȅl-Romas L, Burgener A, Wählby C, Wang L, Rohan LC, Guenthner P, Mitchell J, Matoba N, McNicholl JM, Palmer KE, Tjernlund A, Broliden K. Impact of Q-Griffithsin anti-HIV microbicide gel in non-human primates: In situ analyses of epithelial and immune cell markers in rectal mucosa. Sci Rep. 2019 Dec 2;9(1):18120. doi: 10.1038/s41598-019-54493-4. PubMed PMID: 31792342; PubMed Central PMCID: PMC6889265.
McQueen P, Busman-Sahay K, Rieder F, Noël-Romas L, McCorrister S, Westmacott G, Estes JD, Burgener A. Intestinal proteomic analysis of a novel non-human primate model of experimental colitis reveals signatures of mitochondrial and metabolic dysfunction. Mucosal Immunol. 2019 Nov;12(6):1327-1335. doi: 10.1038/s41385-019-0200-2. Epub 2019 Sep 3. PubMed PMID: 31481749; PubMed Central PMCID: PMC7673647.
Hensley-McBain T, Wu MC, Manuzak JA, Cheu RK, Gustin A, Driscoll CB, Zevin AS, Miller CJ, Coronado E, Smith E, Chang J, Gale M Jr, Somsouk M, Burgener AD, Hunt PW, Hope TJ, Collier AC, Klatt NR. Increased mucosal neutrophil survival is associated with altered microbiota in HIV infection. PLoS Pathog. 2019 Apr;15(4):e1007672. doi: 10.1371/journal.ppat.1007672. eCollection 2019 Apr. PubMed PMID: 30973942; PubMed Central PMCID: PMC6459500.
Månberg A, Bradley F, Qundos U, Guthrie BL, Birse K, Noël-Romas L, Lindskog C, Bosire R, Kiarie J, Farquhar C, Burgener AD, Nilsson P, Broliden K. A High-throughput Bead-based Affinity Assay Enables Analysis of Genital Protein Signatures in Women At Risk of HIV Infection. Mol Cell Proteomics. 2019 Mar;18(3):461-476. doi: 10.1074/mcp.RA118.000757. Epub 2018 Nov 30. PubMed PMID: 30504243; PubMed Central PMCID: PMC6398207.
McKinnon LR, Achilles SL, Bradshaw CS, Burgener A, Crucitti T, Fredricks DN, Jaspan HB, Kaul R, Kaushic C, Klatt N, Kwon DS, Marrazzo JM, Masson L, McClelland RS, Ravel J, van de Wijgert JHHM, Vodstrcil LA, Tachedjian G. The Evolving Facets of Bacterial Vaginosis: Implications for HIV Transmission. AIDS Res Hum Retroviruses. 2019 Mar;35(3):219-228. doi: 10.1089/AID.2018.0304. PubMed PMID: 30638028; PubMed Central PMCID: PMC6434601.
Lo M, Zhu J, Hansen SG, Carroll T, Farr Zuend C, Nöel-Romas L, Ma ZM, Fritts L, Huang ML, Sun S, Huang Y, Koelle DM, Picker LJ, Burgener A, Corey L, Miller CJ. Acute Infection and Subsequent Subclinical Reactivation of Herpes Simplex Virus 2 after Vaginal Inoculation of Rhesus Macaques. J Virol. 2019 Jan 15;93(2). doi: 10.1128/JVI.01574-18. Print 2019 Jan 15. PubMed PMID: 30333177; PubMed Central PMCID: PMC6321901.
Govia RNM, Birse KD, Sepehri S, Khafipour E, Menticoglou SM, Burgener AD, Poliquin V. Amniotic fluid proteomic signatures of cervical insufficiency and their association with length of latency. Am J Reprod Immunol. 2018 Nov;80(5):e13030. doi: 10.1111/aji.13030. Epub 2018 Aug 3. PubMed PMID: 30076666.
Hensley-McBain T, Berard AR, Manuzak JA, Miller CJ, Zevin AS, Polacino P, Gile J, Agricola B, Cameron M, Hu SL, Estes JD, Reeves RK, Smedley J, Keele BF, Burgener AD, Klatt NR. Intestinal damage precedes mucosal immune dysfunction in SIV infection. Mucosal Immunol. 2018 Sep;11(5):1429-1440. doi: 10.1038/s41385-018-0032-5. Epub 2018 Jun 15. PubMed PMID: 29907866; PubMed Central PMCID: PMC6162106.
Berard AR, Perner M, Mutch S, Farr Zuend C, McQueen P, Burgener AD. Understanding mucosal and microbial functionality of the female reproductive tract by metaproteomics: Implications for HIV transmission. Am J Reprod Immunol. 2018 Aug;80(2):e12977. doi: 10.1111/aji.12977. Epub 2018 May 22. Review. PubMed PMID: 29790240.
Bradley F, Birse K, Hasselrot K, Noël-Romas L, Introini A, Wefer H, Seifert M, Engstrand L, Tjernlund A, Broliden K, Burgener AD. The vaginal microbiome amplifies sex hormone-associated cyclic changes in cervicovaginal inflammation and epithelial barrier disruption. Am J Reprod Immunol. 2018 Jul;80(1):e12863. doi: 10.1111/aji.12863. Epub 2018 Apr 30. PubMed PMID: 29709092.
Lajoie J, Birse K, Mwangi L, Chen Y, Cheruiyot J, Akolo M, Mungai J, Boily-Larouche G, Romas L, Mutch S, Kimani M, Oyugi J, Ho EA, Burgener A, Kimani J, Fowke KR. Using safe, affordable and accessible non-steroidal anti-inflammatory drugs to reduce the number of HIV target cells in the blood and at the female genital tract. J Int AIDS Soc. 2018 Jul;21(7):e25150. doi: 10.1002/jia2.25150. PubMed PMID: 30047573; PubMed Central PMCID: PMC6060422.
Girard L, Birse K, Holm JB, Gajer P, Humphrys MS, Garber D, Guenthner P, Noël-Romas L, Abou M, McCorrister S, Westmacott G, Wang L, Rohan LC, Matoba N, McNicholl J, Palmer KE, Ravel J, Burgener AD. Impact of the griffithsin anti-HIV microbicide and placebo gels on the rectal mucosal proteome and microbiome in non-human primates. Sci Rep. 2018 May 23;8(1):8059. doi: 10.1038/s41598-018-26313-8. PubMed PMID: 29795295; PubMed Central PMCID: PMC5966460.
Hensley-McBain T, Klatt NR. The Dual Role of Neutrophils in HIV Infection. Curr HIV/AIDS Rep. 2018 Feb;15(1):1-10. doi: 10.1007/s11904-018-0370-7. Review. PubMed PMID: 29516266; PubMed Central PMCID: PMC6086572.
Fulcher JA, Romas L, Hoffman JC, Elliott J, Saunders T, Burgener AD, Anton PA, Yang OO. Highly Human Immunodeficiency Virus-Exposed Seronegative Men Have Lower Mucosal Innate Immune Reactivity. AIDS Res Hum Retroviruses. 2017 Aug;33(8):788-795. doi: 10.1089/AID.2017.0014. Epub 2017 Jun 19. PubMed PMID: 28503933; PubMed Central PMCID: PMC5564013.
Klatt NR, Cheu R, Birse K, Zevin AS, Perner M, Noël-Romas L, Grobler A, Westmacott G, Xie IY, Butler J, Mansoor L, McKinnon LR, Passmore JS, Abdool Karim Q, Abdool Karim SS, Burgener AD. Vaginal bacteria modify HIV tenofovir microbicide efficacy in African women. Science (New York, N.Y.). 2017; 356(6341):938-945. PubMed [journal] PMID: 28572388
Birse KD, Romas LM, Guthrie BL, Nilsson P, Bosire R, Kiarie J, Farquhar C, Broliden K, Burgener AD. Genital Injury Signatures and Microbiome Alterations Associated With Depot Medroxyprogesterone Acetate Usage and Intravaginal Drying Practices. The Journal of infectious diseases. 2017; 215(4):590-598. PubMed [journal] PMID: 28011908, PMCID: PMC5388302
Zevin AS, Xie IY, Birse K, Arnold K, Romas L, Westmacott G, Novak RM, McCorrister S, McKinnon LR, Cohen CR, Mackelprang R, Lingappa J, Lauffenburger DA, Klatt NR, Burgener AD. Microbiome Composition and Function Drives Wound-Healing Impairment in the Female Genital Tract. PLoS pathogens. 2016; 12(9):e1005889. PubMed [journal] PMID: 27656899, PMCID: PMC5033340
Romas L, Birse K, Mayer KH, Abou M, Westmacott G, Giguere R, Febo I, Cranston RD, Carballo-Diéguez A, McGowan I, Burgener A. Rectal 1% Tenofovir Gel Use Associates with Altered Epidermal Protein Expression. AIDS research and human retroviruses. 2016; 32(10-11):1005-1015. PubMed [journal] PMID: 27316778, PMCID: PMC5067863
Fulcher JA, Romas L, Hoffman JC, Elliott J, Saunders T, Burgener A, Anton PA, Yang OO. Highly HIV-Exposed Seronegative Men Have Lower Mucosal Innate Immune Reactivity. AIDS research and human retroviruses. 2017; PubMed [journal] PMID:
28503933
Reeves RK, Burgener A, Klatt NR. Targeting the gastrointestinal tract to develop novel therapies for HIV. Clinical pharmacology and therapeutics. 2015; 98(4):381-6. PubMed [journal] PMID: 26179624
Burgener A, McGowan I, Klatt NR. HIV and mucosal barrier interactions: consequences for transmission and pathogenesis. Current opinion in immunology. 2015; 36:22-30. PubMed [journal] PMID: 26151777
Arnold KB, Burgener A, Birse K, Romas L, Dunphy LJ, et al. Increased levels of inflammatory cytokines in the female reproductive tract are associated with altered expression of proteases, mucosal barrier proteins, and an influx of HIV-susceptible target cells. Mucosal immunology. 2015; PubMed [journal] PMID: 26104913
Birse KD, Cole AL, Hirbod T, McKinnon L, Ball TB, et al. Non-Cationic Proteins Are Associated with HIV Neutralizing Activity in Genital Secretions of Female Sex Workers. PloS one. 2015; 10(6):e0130404. PubMed [journal] PMID: 26090884, PMCID: PMC4475052
Birse K, Arnold KB, Novak RM, McCorrister S, Shaw S, et al. Molecular Signatures of Immune Activation and Epithelial Barrier Remodeling Are Enhanced during the Luteal Phase of the Menstrual Cycle: Implications for HIV Susceptibility. Journal of virology. 2015; 89(17):8793-805. PubMed [journal] PMID: 26085144, PMCID: PMC4524071
Hladik F, Burgener A, Ballweber L, Gottardo R, Vojtech L, et al. Correction: Musosal effects for tenofovir 1% gel. eLife. 2015; 4. PubMed [journal] PMID: 25803485, PMCID: PMC4371375