Latent Upregulation of Nlrp3, Nlrc4 and Aim2 Differentiates between Asymptomatic and Symptomatic Trichomonas vaginalis Infection

References

• Abraham M, Desjardins M, Fillon L, Garber G. 1996. Inducible immunity to Trichomonas vaginalis in culture. Infect Immun. 64(9):3571–75.
   PubMed Web of Science ®Google Scholar
• Arana-Argáez VE, Ceballos-Góngora E, Alvarez-Sánchez ME, Euan-Canto A, Lara-Riegos J, Torres-Romero JC. 2020. In vitro activation of macrophages by an MHC class II-restricted Trichomonas vaginalis TvZIP8-derived synthetic peptide. Immunol Invest. 1–15. doi:https://doi.org/10.1080/08820139.2020.1810703
   Google Scholar
• Bae JH, Jo SI, Kim SJ, Lee JM, Jeong JH, Kang JS, Cho N-J, Kim SS, Lee EY, Moon J-S. 2019. Circulating cell-free mtDNA contributes to AIM2 inflammasome-mediated chronic inflammation in patients with type 2 diabetes. Cells. 8(4):328.
   Web of Science ®Google Scholar
• Broz P, Dixit VM. 2016. Inflammasomes: mechanism of assembly, regulation and signalling. Nat Rev Immunol. 16:407–20.
   PubMed Web of Science ®Google Scholar
• Bruno VM, Shetty AC, Yano J, Fidel PL, Noverr MC, Peters BM. 2015. Transcriptomic analysis of vulvovaginal candidiasis identifies a role for the NLRP3 inflammasome. MBio. 6(2):e00182–15.
   PubMed Web of Science ®Google Scholar
• Cauci S, Culhane JF. 2007. Modulation of vaginal immune response among pregnant women with bacterial vaginosis by Trichomonas vaginalis, chlamydia trachomatis, neisseria gonorrhoeae, and yeast. Am J Obstet Gynecol. 196(2):133. e131-133. e137.
   PubMedGoogle Scholar
• Centers for Disease Control and Prevention. 2012. Trichomoniasis-CDC fact sheet. Atlanta (GA): Centers for Disease Control and Prevention. https://www.cdc.gov/std/trichomonas/trichomoniasis-factsheet.pdf.
   Google Scholar
• Charmoy M, Hurrell BP, Romano A, Lee SH, Ribeiro‐Gomes F, Riteau N, Mayer‐Barber K, Tacchini‐Cottier F, Sacks DL. 2016. The Nlrp3 inflammasome, IL‐1β, and neutrophil recruitment are required for susceptibility to a nonhealing strain of Leishmania major in C57BL/6 mice. Eur J Immunol. 46(4):897–911.
   PubMed Web of Science ®Google Scholar
• Chaves MM, Sinflorio DA, Thorstenberg ML, Martins MDA, Moreira-Souza ACA, Rangel TP, Silva CL, Bellio M, Canetti C, Coutinho-Silva R. 2019. Non-canonical NLRP3 inflammasome activation and IL-1β signaling are necessary to L. amazonensis control mediated by P2X7 receptor and leukotriene B4. PLoS Pathog. 15(6):e1007887.
   PubMed Web of Science ®Google Scholar
• Chu JQ, Shi G, Fan YM, Choi IW, Cha GH, Zhou Y, Lee YH, Quan JH. 2016. Production of IL-1β and inflammasome with up-regulated expressions of NOD-like receptor related genes in Toxoplasma gondii-infected THP-1 macrophages. Korean J Parasitol. 54(6):711–17.
   PubMed Web of Science ®Google Scholar
• Chudnovskiy A, Mortha A, Kana V, Kennard A, Ramirez JD, Rahman A, Remark R, Mogno I, Ng R, Gnjatic S. 2016. Host-protozoan interactions protect from mucosal infections through activation of the inflammasome. Cell. 167(2):444–456. e414.
   PubMed Web of Science ®Google Scholar
• De Carvalho RV, Andrade WA, Lima-Junior DS, Dilucca M, De Oliveira CV, Wang K, Nogueira PM, Rugani JN, Soares RP, Beverley SM. 2019. Leishmania lipophosphoglycan triggers caspase-11 and the non-canonical activation of the NLRP3 inflammasome. Cell Rep. 26(2):429–437. e425.
   PubMed Web of Science ®Google Scholar
• De Jesus JB, Ferreira MA, Cuervo P, Britto C, E Silva-filho FC, Meyer-Fernandes JR. 2006. Iron modulates ecto-phosphohydrolase activities in pathogenic trichomonads. Parasitol Int. 55:285–90.
   PubMed Web of Science ®Google Scholar
• Demirezen S, Safi Z, Beksac S. 2000. The interaction of trichomonas vaginalis with epithelial cells, polymorphonuclear leucocytes and erythrocytes on vaginal smears: light microscopic observation. Cytopathology. 11(5):326–32.
   PubMed Web of Science ®Google Scholar
• Diamond LS. 1957. The establishment of various trichomonads of animals and man in axenic cultures. J Parasitol. 43(4):488–90.
   PubMed Web of Science ®Google Scholar
• Eida AM, Eida OM, Salem AS. 2015. Kinetics of serum and local leukotriene B4 response in experimental intravaginal trichomoniasis by T. vaginalis isolates from symptomatic and asymptomatic women. Adv Infect Dis. 5(1):37–47.
   Google Scholar
• Garber G, Proctor E, Bowie W. 1986. Immunogenic proteins of Trichomonas vaginalis as demonstrated by the immunoblot technique. Infect Immun. 51(1):250–53.
   PubMed Web of Science ®Google Scholar
• Ginzinger DG. 2002. Gene quantification using real-time quantitative PCR: an emerging technology hits the mainstream. Exp Hematol. 30(6):503–12.
   PubMed Web of Science ®Google Scholar
• Gu NY, Kim JH, Han IH, Im SJ, Seo MY, Chung YH, Ryu JS. 2016. Trichomonas vaginalis induces IL‐1β production in a human prostate epithelial cell line by activating the NLRP3 inflammasome via reactive oxygen species and potassium ion efflux. The Prostate. 76(10):885–96.
   PubMed Web of Science ®Google Scholar
• Gupta G, Santana AK, Gomes CM, Turatti A, Milanezi CM, Bueno Filho R, Fuzo C, Almeida RP, Carregaro V, Roselino AM. 2019. Inflammasome gene expression is associated with immunopathology in human localized cutaneous leishmaniasis. Cell Immunol. 341:103920.
   PubMed Web of Science ®Google Scholar
• Gutierrez O, Pipaon C, Fernandez-Luna JL. 2004. Ipaf is upregulated by tumor necrosis factor‐α in human leukemia cells. FEBS Lett. 568(1–2):79–82.
   PubMed Web of Science ®Google Scholar
• Hafner-Bratkovič I. 2017. The NLRC4 inflammasome: the pieces of the puzzle are falling into place. Inflammasome. 3:10–23.
   Google Scholar
• Helmy M, El-Gayar E, Hussein E, Abdou A, Mahdy Z. 2008. Comparison between trichomonas vaginalis symptomatic and asymptomatic isolates effects in intravaginally infected rats. J Egypt Soc Parasitol. 38(3):843–52.
   PubMedGoogle Scholar
• Henao-Mejia J, Elinav E, Thaiss CA, Flavell RA. 2013. The intestinal microbiota in chronic liver disease. In Advances in immunology. Vol. 117. Elsevier. p. 73–97. doi:https://doi.org/10.1016/b978-0-12-410524-9.00003-7
   Google Scholar
• Hise AG, Tomalka J, Ganesan S, Patel K, Hall BA, Brown GD, Fitzgerald KA. 2009. An essential role for the NLRP3 inflammasome in host defense against the human fungal pathogen Candida albicans. Cell Host Microbe. 5(5):487–97.
   PubMed Web of Science ®Google Scholar
• Hong EE, Okitsu CY, Smith AD, Hsieh C-L. 2013. Regionally specific and genome-wide analyses conclusively demonstrate the absence of CpG methylation in human mitochondrial DNA. Mol Cell Biol. 33(14):2683–90.
   PubMed Web of Science ®Google Scholar
• Kaur S, Khurana S, Bagga R, Wanchu A, Malla N. 2008. Trichomoniasis among women in North India: a hospital based study. Indian J Sexually Transmitted Dis AIDS. 29(2):76–81.
   Google Scholar
• Kissinger P. 2015. Epidemiology and treatment of trichomoniasis. Curr Infect Dis Rep. 17(6):484.
   PubMed Web of Science ®Google Scholar
• Knodler LA, Crowley SM, Sham HP, Yang H, Wrande M, Ma C, Ernst RK, Steele-Mortimer O, Celli J, Vallance BA. 2014. Noncanonical inflammasome activation of caspase-4/caspase-11 mediates epithelial defenses against enteric bacterial pathogens. Cell Host Microbe. 16(2):249–56.
   PubMed Web of Science ®Google Scholar
• Kucknoor A, Mundodi V, Alderete JF. 2005. Trichomonas vaginalis adherence mediates differential gene expression in human vaginal epithelial cells. Cell Microbiol. 7(6):887–97.
   PubMed Web of Science ®Google Scholar
• Lamkanfi M, Malireddi RS, Kanneganti T-D. 2009. Fungal zymosan and mannan activate the cryopyrin inflammasome. J Biol Chem. 284(31):20574–81.
   PubMed Web of Science ®Google Scholar
• Lazenby GB, Soper DE, Nolte FS. 2013. Correlation of leukorrhea and Trichomonas vaginalis infection. J Clin Microbiol. 51(7):2323–27.
   PubMed Web of Science ®Google Scholar
• Lupfer C, Anand PK. 2016. Integrating inflammasome signaling in sexually transmitted infections. Trends Immunol. 37(10):703–14.
   PubMed Web of Science ®Google Scholar
• Mankan AK, Schmidt T, Chauhan D, Goldeck M, Höning K, Gaidt M, Kubarenko AV, Andreeva L, Hopfner KP, Hornung V. 2014. Cytosolic RNA: DNA hybrids activate the cGAS–STING axis. Embo J. 33(24):2937–46.
   PubMed Web of Science ®Google Scholar
• McLean NW, Rosenstein IJ. 2000. Characterisation and selection of a Lactobacillus species to re-colonise the vagina of women with recurrent bacterial vaginosis. J Med Microbiol. 49(6):543–52.
   PubMed Web of Science ®Google Scholar
• Mercer F, Diala FGI, Chen Y-P, Molgora BM, Ng SH, Johnson PJ. 2016. Leukocyte lysis and cytokine induction by the human sexually transmitted parasite Trichomonas vaginalis. PLoS Negl Trop Dis. 10(8):e0004913.
   PubMed Web of Science ®Google Scholar
• Mercer F, Johnson PJ. 2018. Trichomonas vaginalis: pathogenesis, symbiont interactions, and host cell immune responses. Trends Parasitol. 34(8):683–93.
   PubMed Web of Science ®Google Scholar
• Nakahira K, Haspel JA, Rathinam VA, Lee S-J, Dolinay T, Lam HC, Englert JA, Rabinovitch M, Cernadas M, Kim HP. 2011. Autophagy proteins regulate innate immune responses by inhibiting the release of mitochondrial DNA mediated by the NALP3 inflammasome. Nat Immunol. 12(3):222–30.
   PubMed Web of Science ®Google Scholar
• Narantsogt G, Min A, Nam YH, Lee YA, Kim KA, Agvaandaram G, Dorjsuren T, El-Benna J, Shin MH. 2015. Activation of MAPK is required for ROS generation and exocytosis in HMC-1 cells induced by Trichomonas vaginalis-derived secretory products. Korean J Parasitol. 53(5):597–603.
   PubMed Web of Science ®Google Scholar
• Netea MG, Nold-Petry CA, Nold MF, Joosten LA, Opitz B, Van Der Meer JH, Van De Veerdonk FL, Ferwerda G, Heinhuis B, Devesa I. 2009. Differential requirement for the activation of the inflammasome for processing and release of IL-1β in monocytes and macrophages. Blood. 113(10):2324–35.
   PubMed Web of Science ®Google Scholar
• Paintlia M, Kaur S, Gupta I, Ganguly N, Mahajan R, Malla N. 2002. Specific IgA response, T-cell subtype and cytokine profile in experimental intravaginal trichomoniasis. Parasitol Res. 88(4):338–43.
   PubMed Web of Science ®Google Scholar
• Pelegrin P, Surprenant A. 2007. Pannexin-1 couples to maitotoxin-and nigericin-induced interleukin-1β release through a dye uptake-independent pathway. J Biol Chem. 282:2386–94.
   PubMed Web of Science ®Google Scholar
• Peters BM, Palmer GE, Nash AK, Lilly EA, Fidel PL, Noverr MC. 2014a. Fungal morphogenetic pathways are required for the hallmark inflammatory response during Candida albicans vaginitis. Infect Immun. 82(2):532–43.
   PubMed Web of Science ®Google Scholar
• Peters BM, Yano J, Noverr MC, Fidel PL Jr. 2014b. Candida vaginitis: when opportunism knocks, the host responds. PLoS Pathog. 10(4):e1003965.
   PubMed Web of Science ®Google Scholar
• Pietrella D, Pandey N, Gabrielli E, Pericolini E, Perito S, Kasper L, Bistoni F, Cassone A, Hube B, Vecchiarelli A. 2013. Secreted aspartic proteases of C andida albicans activate the NLRP 3 inflammasome. Eur J Immunol. 43(3):679–92.
   PubMed Web of Science ®Google Scholar
• Quan J-H, Huang R, Wang Z, Huang S, Choi I-W, Zhou Y, Lee Y-H, Chu J-Q. 2018. P2X7 receptor mediates NLRP3-dependent IL-1β secretion and parasite proliferation in Toxoplasma gondii-infected human small intestinal epithelial cells. Parasit Vectors. 11:1.
   PubMed Web of Science ®Google Scholar
• Rajamäki K, Lappalainen J, Öörni K, Välimäki E, Matikainen S, Kovanen PT, Eklund KK. 2010. Cholesterol crystals activate the NLRP3 inflammasome in human macrophages: a novel link between cholesterol metabolism and inflammation. PloS One. 5(7):e11765.
   PubMed Web of Science ®Google Scholar
• Rein M, Muller M. 1990. Trichomonas vaginalis and trichomoniasis. In Holmes KK, Mårdh PA, Sparling PF, et al, editors. Sexually transmitted diseases, 2nd ed. New York (NY): McGraw-Hill Book Co; p. 481–92.
   Google Scholar
• Riestra AM, Valderrama JA, Patras KA, Booth SD, Quek XY, Tsai C-M, Nizet V. 2019. Trichomonas vaginalis induces NLRP3 inflammasome activation and pyroptotic cell death in human macrophages. J Innate Immun. 11(1):86–98.
   PubMed Web of Science ®Google Scholar
• Riley JS, Tait SW. 2020. Mitochondrial DNA in inflammation and immunity. EMBO Rep. 21:e49799.
   PubMed Web of Science ®Google Scholar
• Russell MW, Mestecky J. 2010. Tolerance and protection against infection in the genital tract. Immunol Invest. 39:500–25.
   PubMed Web of Science ®Google Scholar
• Sadasivam S, Gupta S, Radha V, Batta K, Kundu TK, Swarup G. 2005. Caspase-1 activator Ipaf is a p53-inducible gene involved in apoptosis. Oncogene. 24(4):627–36.
   PubMed Web of Science ®Google Scholar
• Schaale K, Peters KM, Murthy AM, Fritzsche AK, Phan M-D, Totsika M, Robertson A, Nichols K, Cooper M, Stacey K. 2016. Strain-and host species-specific inflammasome activation, IL-1β release, and cell death in macrophages infected with uropathogenic Escherichia coli. Mucosal Immunol. 9(1):124–36.
   PubMed Web of Science ®Google Scholar
• Skeldon A, Saleh M. 2011. The inflammasomes: molecular effectors of host resistance against bacterial, viral, parasitic, and fungal infections. Front Microbiol. 2:15.
   PubMed Web of Science ®Google Scholar
• Sutterwala FS, Flavell RA. 2009. NLRC4/IPAF: a CARD carrying member of the NLR family. Clin immunol. 130(1):2–6.
   PubMed Web of Science ®Google Scholar
• Sutton M, Sternberg M, Koumans EH, McQuillan G, Berman S, Markowitz L. 2007. The prevalence of Trichomonas vaginalis infection among reproductive-age women in the United States, 2001–2004. Clin infect dis. 45(10):1319–26.
   PubMed Web of Science ®Google Scholar
• Tomalka J, Ganesan S, Azodi E, Patel K, Majmudar P, Hall BA, Fitzgerald KA, Hise AG. 2011. A novel role for the NLRC4 inflammasome in mucosal defenses against the fungal pathogen Candida albicans. PLoS Pathog. 7(12):e1002379.
   PubMed Web of Science ®Google Scholar
• Valadkhani Z, Sharma S, Harjai K, Gupta I, Malla N. 2004. Evaluation of Trichomonas vaginalis isolates from symptomatic and asymptomatic patients in mouse model. Iran J Public Health. 33(2):60–66.
   Google Scholar
• Verma V, Dhanda RS, Møller NF, Yadav M. 2016. Inflammasomes and their role in innate immunity of sexually transmitted infections. Front Immunol. 7:540. doi:https://doi.org/10.3389/fimmu.2016.00540
   Google Scholar
• Vick EJ, Park HS, Huff KA, Brooks KM, Farone AL, Farone MB. 2014. Gardnerella vaginalis triggers NLRP3 inflammasome recruitment in THP-1 monocytes. J Reprod Immunol. 106:67–75.
   PubMed Web of Science ®Google Scholar
• Warton A, Honigberg B. 1983. Analysis of surface saccharides in Trichomonas vaginalis strains with various pathogenicity levels by fluorescein-conjugated plant lectins. Zeitschrift für Parasitenkunde. 69:149–59.
   PubMed Web of Science ®Google Scholar
• World Health Organization 2001. Factsheet. Global prevalence and incidence of selected curable sexually transmitted infections: overview and estimates. Geneva, Switzerland: World Health Organization. WHO/HIV_AIDS/2001.02. WHO/CDS/CSR/EDC/2001.10
   Google Scholar
• Zhou R, Yazdi AS, Menu P, Tschopp J. 2011. A role for mitochondria in NLRP3 inflammasome activation. Nature. 469:221–25.
   PubMed Web of Science ®Google Scholar