Dual role for microbial short-chain fatty acids in modifying SIV disease trajectory following anti-α4β7 antibody administration

References

• Gordon SN, Cervasi B, Odorizzi P, et al. Disruption of intestinal CD4+ T cell homeostasis is a key marker of systemic CD4+ T cell activation in HIV-infected individuals. J Immunol. 2010;185(9):1–16. doi: 10.4049/jimmunol.1001801.
   Web of Science ®Google Scholar
• Brenchley JM, Price DA, Schacker TW, et al. Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat Med. 2006;12(12):1365–1371. doi: 10.1038/nm1511.
   PubMed Web of Science ®Google Scholar
• Kløverpris HN, Kazer SW, Mjösberg J, et al. Innate lymphoid cells are depleted irreversibly during acute HIV-1 infection in the absence of viral suppression. Immunity. 2016;44(2):391–405. doi: 10.1016/j.immuni.2016.01.006.
   PubMed Web of Science ®Google Scholar
• Porichis F, Kaufmann DE. Role of PD-1 in HIV pathogenesis and as target for therapy. Curr HIV/AIDS Rep. 2012;9(1):81–90. doi: 10.1007/s11904-011-0106-4.
   PubMed Web of Science ®Google Scholar
• Horn C, Augustin M, Ercanoglu MS, et al. HIV DNA reservoir and elevated PD-1 expression of CD4 T-cell subsets particularly persist in the terminal ileum of HIV-positive patients despite cART. HIV Med. 2021;22(5):397–408. doi: 10.1111/hiv.13031.
   PubMed Web of Science ®Google Scholar
• Fromentin R, DaFonseca S, Costiniuk CT, et al. PD-1 blockade potentiates HIV latency reversal ex vivo in CD4(+) T cells from ART-suppressed individuals. Nat Commun. 2019;10(1):814. doi: 10.1038/s41467-019-08798-7.
   PubMedGoogle Scholar
• Thurman M, Johnson S, Acharya A, et al. Biomarkers of activation and inflammation to track disparity in chronological and physiological age of people living with HIV on combination antiretroviral therapy. Front Immunol. 2020;11:583934. doi: 10.3389/fimmu.2020.583934.
   PubMed Web of Science ®Google Scholar
• Vujkovic-Cvijin I, Sortino O, Verheij E, et al. HIV-associated gut dysbiosis is independent of sexual practice and correlates with noncommunicable diseases. Nat Commun. 2020;11(1):2448. doi: 10.1038/s41467-020-16222-8.
   PubMed Web of Science ®Google Scholar
• Serrano-Villar S, Talavera-Rodríguez A, Gosalbes MJ, et al. Fecal microbiota transplantation in HIV: a pilot placebo-controlled study. Nat Commun. 2021;12(1):1139. doi: 10.1038/s41467-021-21472-1.
   PubMed Web of Science ®Google Scholar
• Dillon SM, Kibbie J, Lee EJ, et al. Low abundance of colonic butyrate-producing bacteria in HIV infection is associated with microbial translocation and immune activation. AIDS. 2017;31(4):511–521. doi: 10.1097/QAD.0000000000001366.
   PubMed Web of Science ®Google Scholar
• Kaur US, Shet A, Rajnala N, et al. High abundance of genus prevotella in the gut of perinatally HIV-infected children is associated with IP-10 levels despite therapy. Sci Rep. 2018;8(1):17679. doi: 10.1038/s41598-018-35877-4.
   PubMedGoogle Scholar
• Johnson SD, Byrareddy SN. HIV‐associated dysbiosis and immune recovery during antiretroviral therapy. Clin Transl Discov. 2022;2(2):e58. doi: 10.1002/ctd2.58.
   PubMedGoogle Scholar
• Vujkovic-Cvijin I, Somsouk M. HIV and the gut microbiota: composition, consequences, and avenues for amelioration. Curr HIV/AIDS Rep. 2019;16(3):204–213. doi: 10.1007/s11904-019-00441-w.
   PubMed Web of Science ®Google Scholar
• Dillon SM, Lee EJ, Kotter CV, et al. An altered intestinal mucosal microbiome in HIV-1 infection is associated with mucosal and systemic immune activation and endotoxemia. Mucosal Immunol. 2014;7(4):983–994. doi: 10.1038/mi.2013.116.
   PubMed Web of Science ®Google Scholar
• Lozupone CA, Li M, Campbell TB, et al. Alterations in the gut microbiota associated with HIV-1 infection. Cell Host Microbe. 2013;14(3):329–339. doi: 10.1016/j.chom.2013.08.006.
   PubMed Web of Science ®Google Scholar
• Gori A, Rizzardini G, Van’t Land B, et al. Specific prebiotics modulate gut microbiota and immune activation in HAART-naive HIV-infected adults: results of the "COPA" pilot randomized trial. Mucosal Immunol. 2011;4(5):554–563. doi: 10.1038/mi.2011.15.
   PubMed Web of Science ®Google Scholar
• Murphey-Corb M, Martin LN, Rangan SR, et al. Isolation of an HTLV-III-related retrovirus from macaques with simian AIDS and its possible origin in asymptomatic mangabeys. Nature. 1986;321(6068):435–437. doi: 10.1038/321435a0.
   PubMed Web of Science ®Google Scholar
• Mattapallil JJ, Douek DC, Hill B, et al. Massive infection and loss of memory CD4+ T cells in multiple tissues during acute SIV infection. Nature. 2005;434(7037):1093–1097. doi: 10.1038/nature03501.
   PubMed Web of Science ®Google Scholar
• Chahroudi A, Bosinger SE, Vanderford TH, et al. Natural SIV hosts: showing AIDS the door. Science. 2012;335(6073):1188–1193. doi: 10.1126/science.1217550.
   PubMed Web of Science ®Google Scholar
• Byrareddy SN, Sidell N, Arthos J, et al. Species-Specific differences in the expression and regulation of α4β7 integrin in various nonhuman primates. J Immunol. 2015;194(12):5968–5979. doi: 10.4049/jimmunol.1402866.
   PubMed Web of Science ®Google Scholar
• Barrenas F, Raehtz K, Xu C, et al. Macrophage-associated wound healing contributes to african green monkey SIV pathogenesis control. Nat Commun. 2019;10(1):5101. doi: 10.1038/s41467-019-12987-9.
   PubMedGoogle Scholar
• Sidell N, Kane MA. Actions of retinoic acid in the pathophysiology of HIV infection. Nutrients. 2022;14(8):1611. doi: 10.3390/nu14081611.
   PubMed Web of Science ®Google Scholar
• Iwata M, Hirakiyama A, Eshima Y, et al. Retinoic acid imprints gut-homing specificity on T cells. Immunity. 2004;21(4):527–538. doi: 10.1016/j.immuni.2004.08.011.
   PubMed Web of Science ®Google Scholar
• Luzentales-Simpson M, Pang YCF, Zhang A, et al. Vedolizumab: potential mechanisms of action for reducing pathological inflammation in inflammatory bowel diseases. Front Cell Dev Biol. 2021;9(120):612830. doi: 10.3389/fcell.2021.612830.
   PubMedGoogle Scholar
• Johnson SD, Knight LA, Kumar N, et al. Early treatment with anti-α4β7 antibody facilitates increased gut macrophage maturity in SIV-infected rhesus macaques. Front Immunol. 2022;13:1001727. doi: 10.3389/fimmu.2022.1001727.
   PubMed Web of Science ®Google Scholar
• Takahashi N, Sugimoto C, Allers C, et al. Shifting dynamics of intestinal macrophages during simian immunodeficiency virus infection in adult rhesus macaques. J Immunol. 2019;202(9):2682–2689. doi: 10.4049/jimmunol.1801457.
   PubMed Web of Science ®Google Scholar
• Kane MA, Folias AE, Napoli JL, et al. HPLC/UV quantitation of retinal, retinol, and retinyl esters in serum and tissues. Anal Biochem. 2008;378(1):71–79. doi: 10.1016/j.ab.2008.03.038.
   PubMed Web of Science ®Google Scholar
• Kane MA, Folias AE, Wang C, et al. Quantitative profiling of endogenous retinoic acid in vivo and in vitro by tandem mass spectrometry. Anal Chem. 2008;80(5):1702–1708. doi: 10.1021/ac702030f.
   PubMed Web of Science ®Google Scholar
• Kane MA, Napoli JL. Quantification of endogenous retinoids. Methods Molecul Biol (Clifton, NJ). 2010;652:1–54.
   Google Scholar
• Villablanca EJ, Wang S, de Calisto J, et al. MyD88 and retinoic acid signaling pathways interact to modulate gastrointestinal activities of dendritic cells. Gastroenterology. 2011;141(1):176–185. doi: 10.1053/j.gastro.2011.04.010.
   PubMed Web of Science ®Google Scholar
• Jones JW, Pierzchalski K, Yu J, et al. Use of fast HPLC multiple reaction monitoring cubed for endogenous retinoic acid quantification in complex matrices. Anal Chem. 2015;87(6):3222–3230. doi: 10.1021/ac504597q.
   PubMed Web of Science ®Google Scholar
• Merenstein D, Fraser CM, Roberts RF, et al. Bifidobacterium animalis subsp. lactis BB-12 protects against Antibiotic-Induced functional and compositional changes in human fecal microbiome. Nutrients. 2021;13(8):2814. doi: 10.3390/nu13082814.
   PubMed Web of Science ®Google Scholar
• Acharya A, Olwenyi OA, Thurman M, et al. Chronic ­morphine administration differentially modulates viral reservoirs in a simian immunodeficiency virus SIVmac251-infected rhesus macaque model. J Virol. 2021;95(5):e01657–20. doi: 10.1128/JVI.01657-20.
   PubMed Web of Science ®Google Scholar
• Byrareddy SN, Kallam B, Arthos J, et al. Targeting α4β7 integrin reduces mucosal transmission of simian immunodeficiency virus and protects gut-associated lymphoid tissue from infection. Nat Med. 2014;20(12):1397–1400. doi: 10.1038/nm.3715.
   PubMed Web of Science ®Google Scholar
• Johnson SD, Fox HS, Buch S, et al. Chronic opioid administration is associated with prevotella-dominated dysbiosis in SIVmac251 infected, cART-treated macaques. J Neuroimmune Pharmacol. 2021;17(1-2):3–14. doi: 10.1007/s11481-021-09993-4.
   PubMed Web of Science ®Google Scholar
• R-Core-Team. 2018.
   Google Scholar
• Wei T, Simko V. R package ‘corrplot’: Visualization of a correlation matrix. 2021. (Version 0.92). Available from: https://github.com/taiyun/corrplot
   Google Scholar
• Wells CR, Cao Y, Durham DP, et al. Mechanistic basis of post-treatment control of SIV after anti-α4β7 antibody therapy. PLoS Comput Biol. 2021;17(6):e1009031. doi: 10.1371/journal.pcbi.1009031.
   PubMed Web of Science ®Google Scholar
• Ortiz AM, Simpson J, Langner CA, et al. Butyrate administration is not sufficient to improve immune reconstitution in antiretroviral-treated SIV-infected macaques. Sci Rep. 2022;12(1):7491. doi: 10.1038/s41598-022-11122-x.
   PubMed Web of Science ®Google Scholar
• Byrareddy SN, Arthos J, Cicala C, et al. Sustained virologic control in SIV + macaques after antiretroviral and α4β7 antibody therapy. Science. 2016;354(6309):197–202. doi: 10.1126/science.aag1276.
   PubMed Web of Science ®Google Scholar
• Bimczok D, Kao JY, Zhang M, et al. Human gastric epithelial cells contribute to gastric immune regulation by providing retinoic acid to dendritic cells. Mucosal Immunol. 2015;8(3):533–544. doi: 10.1038/mi.2014.86.
   PubMed Web of Science ®Google Scholar
• Salvi PS, Cowles RA. Butyrate and the intestinal epithelium: modulation of proliferation and inflammation in homeostasis and disease. Cells. 2021;10(7):1775. doi: 10.3390/cells10071775.
   PubMed Web of Science ®Google Scholar
• Wang J, Chen W-D, Wang Y-D, et al. The relationship between gut microbiota and inflammatory diseases: the role of macrophages. Front Microbiol. 2020;11:1065. doi: 10.3389/fmicb.2020.01065.
   PubMed Web of Science ®Google Scholar
• Isobe J, Maeda S, Obata Y, et al. Commensal-bacteria-derived butyrate promotes the T-cell-independent IgA response in the Colon. Int Immunol. 2020;32(4):243–258. doi: 10.1093/intimm/dxz078.
   PubMed Web of Science ®Google Scholar
• Gurav A, Sivaprakasam S, Bhutia YD, et al. Slc5a8, a Na+-coupled high-affinity transporter for short-chain fatty acids, is a conditional tumour suppressor in Colon that protects against colitis and Colon cancer under low-fibre dietary conditions. Biochem J. 2015;469(2):267–278. doi: 10.1042/BJ20150242.
   PubMed Web of Science ®Google Scholar
• Iliev ID, Spadoni I, Mileti E, et al. Human intestinal epithelial cells promote the differentiation of tolerogenic dendritic cells. Gut. 2009;58(11):1481–1489. doi: 10.1136/gut.2008.175166.
   PubMed Web of Science ®Google Scholar
• Ananthakrishnan AN, Luo C, Yajnik V, et al. Gut microbiome function predicts response to anti-integrin biologic therapy in inflammatory bowel diseases. Cell Host Microbe. 2017;21(5):603–610.e3. doi: 10.1016/j.chom.2017.04.010.
   PubMed Web of Science ®Google Scholar
• Clark RL, Connors BM, Stevenson DM, et al. Design of synthetic human gut microbiome assembly and butyrate production. Nat Commun. 2021;12(1):3254. doi: 10.1038/s41467-021-22938-y.
   PubMed Web of Science ®Google Scholar
• Das B, Dobrowolski C, Shahir A-M, et al. Short chain fatty acids potently induce latent HIV-1 in T-cells by activating P-TEFb and multiple histone modifications. Virology. 2015;474:65–81. doi: 10.1016/j.virol.2014.10.033.
   PubMed Web of Science ®Google Scholar
• Antunes KH, Stein RT, Franceschina C, et al. Short-chain fatty acid acetate triggers antiviral response mediated by RIG-I in cells from infants with respiratory syncytial virus bronchiolitis. eBioMedicine. 2022;77:103891. doi: 10.1016/j.ebiom.2022.103891.
   PubMed Web of Science ®Google Scholar
• Antunes KH, Fachi JL, de Paula R, et al. Microbiota-derived acetate protects against respiratory syncytial virus infection through a GPR43-type 1 interferon response. Nat Commun. 2019;10(1):3273. doi: 10.1038/s41467-019-11152-6.
   PubMed Web of Science ®Google Scholar
• Rasmussen TA, Lewin SR. Shocking HIV out of hiding: where are we with clinical trials of latency reversing agents? Curr Opin HIV AIDS. 2016;11(4):394–401. doi: 10.1097/COH.0000000000000279.
   PubMed Web of Science ®Google Scholar
• Yu J, Huang W, Liu T, et al. Effect of radiation on the essential nutrient homeostasis and signaling of retinoids in a non-human primate model with minimal bone marrow sparing. Health Phys. 2021;121(4):406–418. doi: 10.1097/HP.0000000000001477.
   PubMed Web of Science ®Google Scholar
• Olwenyi OA, Acharya A, Routhu NK, et al. Retinoic acid improves the recovery of replication-Competent virus from latent SIV infected cells. Cells. 2020;9(9):2076. doi: 10.3390/cells9092076.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Planas D, Raymond Marchand L, et al. Improving HIV outgrowth by optimizing cell-Culture conditions and supplementing with all-trans retinoic acid. Front Microbiol. 2020;11:902. doi: 10.3389/fmicb.2020.00902.
   PubMed Web of Science ®Google Scholar
• Li P, Kaiser P, Lampiris HW, et al. Stimulating the RIG-I pathway to kill cells in the latent HIV reservoir following viral reactivation. Nat Med. 2016;22(7):807–811. doi: 10.1038/nm.4124.
   PubMed Web of Science ®Google Scholar
• Shan L, Deng K, Shroff NS, et al. Stimulation of HIV-1-specific cytolytic T lymphocytes facilitates elimination of latent viral reservoir after virus reactivation. Immunity. 2012;36(3):491–501. doi: 10.1016/j.immuni.2012.01.014.
   PubMed Web of Science ®Google Scholar
• Bhattacharya N, Yuan R, Prestwood TR, et al. Normalizing microbiota-Induced retinoic acid deficiency stimulates protective CD8(+) T cell-mediated immunity in colorectal cancer. Immunity. 2016;45(3):641–655. doi: 10.1016/j.immuni.2016.08.008.
   PubMed Web of Science ®Google Scholar
• Kim MH, Taparowsky EJ, Kim CH, et al. Retinoic acid differentially regulates the migration of innate lymphoid cell subsets to the gut. Immunity. 2015;43(1):107–119. doi: 10.1016/j.immuni.2015.06.009.
   PubMed Web of Science ®Google Scholar
• Mortha A, Chudnovskiy A, Hashimoto D, et al. Microbiota-dependent crosstalk between macrophages and ILC3 promotes intestinal homeostasis. Science. 2014;343(6178):1249288. doi: 10.1126/science.1249288.
   PubMed Web of Science ®Google Scholar
• Castro-Dopico T, Fleming A, Dennison TW, et al. GM-CSF calibrates macrophage defense and wound healing programs during intestinal infection and inflammation. Cell Rep. 2020;32(1):107857. doi: 10.1016/j.celrep.2020.107857.
   PubMed Web of Science ®Google Scholar
• Stevison F, et al. Role of retinoic acid-Metabolizing cytochrome P450s, CYP26, in inflammation and cancer. Advances in Pharmacology (San Diego, Calif). 2015;74:373–412.
   PubMedGoogle Scholar