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Immune cell arrival kinetics to peritoneum and role during murine-experimental trichomoniasis

Published online by Cambridge University Press:  09 August 2021

F. J. Rangel-Mata ,
E. E. Ávila-Muro Open the ORCID record for E. E. Ávila-Muro [Opens in a new window] ,
J. E. Reyes-Martínez Open the ORCID record for J. E. Reyes-Martínez [Opens in a new window] ,
L. M. Olmos-Ortiz Open the ORCID record for L. M. Olmos-Ortiz [Opens in a new window] ,
M. E. Brunck ,
L. A. Arriaga-Pizano  and
P. Cuéllar-Mata Open the ORCID record for P. Cuéllar-Mata [Opens in a new window]
F. J. Rangel-Mata
Affiliation:
Departamento de Biología, Universidad de Guanajuato, Guanajuato, Mexico
E. E. Ávila-Muro
Affiliation:
Departamento de Biología, Universidad de Guanajuato, Guanajuato, Mexico
J. E. Reyes-Martínez
Affiliation:
Departamento de Biología, Universidad de Guanajuato, Guanajuato, Mexico
L. M. Olmos-Ortiz
Affiliation:
Departamento de Biología, Universidad de Guanajuato, Guanajuato, Mexico
M. E. Brunck
Affiliation:
Escuela de Ingeniería y Ciencias, Tecnológico de Monterrey, Monterrey, Mexico
L. A. Arriaga-Pizano
Affiliation:
Unidad de Investigación Médica en Inmunoquímica, IMMS, Ciudad de México, Mexico
P. Cuéllar-Mata*
Affiliation:
Departamento de Biología, Universidad de Guanajuato, Guanajuato, Mexico
*
Author for correspondence: P. Cuéllar-Mata, E-mail: [email protected]
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Abstract

Trichomonas vaginalis causes trichomoniasis, an inflammatory process related to an increased rate of HIV transmission. In order to study T. vaginalis infection response in a microorganism-free environment, an infection model was established providing a host–parasite interaction system useful to study the interplay between immune cells and the parasite. Infected mice peritoneal cells were immunophenotyped at different times after infection using flow cytometry. Neutrophils and macrophages showed the most relevant increase from third to 12th day post-infection. A high number of B lymphocytes were present on 15th day post-infection, and an increase in memory T cells was observed on sixth day post-infection. The levels of NO increased at day 10 post-infection; no significant influence was observed on T. vaginalis clearance. Increased viability of T. vaginalis was observed when the NETs inhibitors, metformin and Cl− amidine, were administrated, highlighting the importance of this mechanism to control parasite infection (43 and 86%, respectively). This report presents a comprehensive cell count of the immune cells participating against trichomoniasis in an in vivo interaction system. These data highlight the relevance of innate mechanisms such as specific population changes of innate immune cells and their impact on the T. vaginalis viability.

Keywords

Host–parasite interactionNETstrichomoniasis
Type
Research Article
Information
Parasitology , Volume 148 , Issue 13 , November 2021 , pp. 1624 - 1635
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Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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References

Abraham, MC, Desjardins, M, Filion, LG and Garber, GE (1996) Inducible immunity to Trichomonas vaginalis in a mouse model of vaginal infection. Infection and Immunity 64, 3571–3575.CrossRefGoogle Scholar
Alderete, JF and Garza, GE (1985) Specific nature of Trichomonas vaginalis parasitism of host cell surfaces. Infection and Immunity 50, 701–708.CrossRefGoogle ScholarPubMed
Arias-Negrete, S, Jiménez-Romero, LA, Solís-Martínez, MO, Ramírez-Emiliano, J, Avila, EE and Cuéllar-Mata, P (2004) Indirect determination of nitric oxide production by reduction of nitrate with a freeze-thawing-resistant nitrate reductase from Escherichia coli MC1061. Analytical Biochemistry 328, 14–21.CrossRefGoogle ScholarPubMed
Barajas-Mendiola, MA, Castellano, LE, Barrios-Rodiles, M, Deveze-Alvarez, MA, Avila, EE and Cuellar-Mata, P (2019) Reduced Trichomonas vaginalis viability in mice pretreated with parasite DNA. Parasitology 146, 1636–1645.CrossRefGoogle ScholarPubMed
Bogdan, C (2015) Nitric oxide synthase in innate and adaptive immunity: an update. Trends in Immunology 36, 161–178.CrossRefGoogle ScholarPubMed
Brinkmann, V, Reichard, U, Goosmann, C, Fauler, B, Uhlemann, Y, Weiss, DS, Weinrauch, Y and Zychlinsky, A (2004) Neutrophil extracellular traps kill bacteria. Science (New York, N.Y.) 303, 1532–1535.CrossRefGoogle ScholarPubMed
Candeias, LP, Patel, KB, Stratford, MR and Wardman, P (1993) Free hydroxyl radicals are formed on reaction between the neutrophil-derived species superoxide anion and hypochlorous acid. FEBS Letters 333, 151–153.CrossRefGoogle ScholarPubMed
Carestia, A, Frechtel, G, Cerrone, G, Linari, MA, Gonzalez, CD, Casais, P and Schattner, M (2016) NETosis before and after hyperglycemic control in type 2 diabetes mellitus patients. PLoS ONE 11, e0168647.CrossRefGoogle ScholarPubMed
Cheng, WH, Huang, KY, Huang, PJ, Hsu, JH, Fang, YK, Chiu, CH and Tang, P (2015) Nitric oxide maintains cell survival of Trichomonas vaginalis upon iron depletion. Parasites & Vectors 8, 393.CrossRefGoogle ScholarPubMed
Critchlow, CW, Wolner-Hanssen, P, Eschenbach, DA, Kiviat, NB, Koutsky, LA, Stevens, CE and Holmes, KK (1995) Determinants of cervical ectopia and of cervicitis: age, oral contraception, specific cervical infection, smoking, and douching. American Journal Obstetrics & Gynecology 173, 534–543.CrossRefGoogle ScholarPubMed
Cusumano, ZT, Watson, ME and Caparon, MG (2014) Streptococcus pyogenes arginine and citrulline catabolism promotes infection and modulates innate immunity. Infection and Immunity 82, 233–242.CrossRefGoogle ScholarPubMed
Edwards, JN and Morris, HB (1985) Langerhans’ cells and lymphocyte subsets in the female genital tract. British Journal of Obstetrics and Gynaecology 92, 974–982.CrossRefGoogle ScholarPubMed
Fichorova, RN (2009) Impact of T. vaginalis infection on innate immune responses and reproductive outcome. Journal of Reproductive Immunology 83, 185–189.CrossRefGoogle Scholar
Fraga, J, Rojas, L, Sariego, I, Fernández-Calienes, A and Nuñez, FA (2012) Species typing of Cuban Trichomonas vaginalis virus by RT-PCR, and association of TVV-2 with high parasite adhesion levels and high pathogenicity in patients. Archives of Virology 157, 1789–1795.CrossRefGoogle ScholarPubMed
Fuchs, TA, Abed, U, Goosmann, C, Hurwitz, R, Schulze, I, Wahn, V, Weinrauch, Y, Brinkmann, V and Zychlinsky, A (2007) Novel cell death program leads to neutrophil extracellular traps. Journal of Cell Biology 176, 231–241.CrossRefGoogle ScholarPubMed
Gasper, DJ, Tejera, MM and Suresh, M (2014) CD4 T-cell memory generation and maintenance. Critical Reviews in Immunology 34, 121–146.CrossRefGoogle ScholarPubMed
Gomez-Barrio, A, Nogal-Ruiz, J.J., Montero-Pereira, D, Rodriguez-Gallego, E, Romero-Fernández, E and Escario, J.A. (2002) Biological variability in clinical isolates of Trichomonas vaginalis. Memorias do Instituto Osvaldo Cruz 97, 893–896.CrossRefGoogle ScholarPubMed
Goodman, RP, Freret, TS, Kula, T, Geller, AM, Talkington, MW, Tang-Fernandez, V, Suciu, O, Demidenko, AA, Ghabrial, SA, Beach, DH, Singh, BN, Fichorova, RN and Nibert, ML (2011) Clinical isolates of Trichomonas vaginalis concurrently infected by strains of up to four Trichomonas virus species (Family Totiviridae). Journal of Virology 85, 4258–4270.CrossRefGoogle Scholar
Green, SJ, Mellouk, S, Hoffman, SL, Meltzer, MS and Nacy, CA (1990) Cellular mechanisms of nonspecific immunity to intracellular infection: cytokine-induced synthesis of toxic nitrogen oxides from L-arginine by macrophages and hepatocytes. Immunology Letters 25, 15–19.CrossRefGoogle ScholarPubMed
Han, IH, Goo, SY, Park, SJ, Hwang, SJ, Kim, YS, Yang, MS, Ahn, MH and Ryu, JS (2009) Proinflammatory cytokine and nitric oxide production by human macrophages stimulated with Trichomonas vaginalis. Korean Journal of Parasitology 47, 205–212.CrossRefGoogle ScholarPubMed
Hänninen, A, Maksimow, M, Alam, C, Morgan, DJ and Jalkanen, S (2011) Ly6C supports preferential homing of central memory CD8+ T cells into lymph nodes. European Journal of Immunology 41, 634–644.CrossRefGoogle ScholarPubMed
Henderson, SC, Kamdar, MM and Bamezai, A (2002) Ly-6A.2 expression regulates antigen-specific CD4+ T cell proliferation and cytokine production. Journal of Immunology 168, 118–126.CrossRefGoogle ScholarPubMed
Huynh, AV and Ávila-Muro, EE (2015) Efecto del anticuerpo contra el receptor TLR4 en la formación de trampas extracelulares de neutrófilos inducidas por el parasito T. vaginalis. Jovenes en la Ciencia 1, 245–249.Google Scholar
James, SL and Glaven, J (1989) Macrophage cytotoxicity against schistosomula of Schistosoma mansoni involves arginine-dependent production of reactive nitrogen intermediates. Journal of Immunology 143, 4208–4212.Google ScholarPubMed
James, SL and Hibbs, JB (1990) The role of nitrogen oxides as effector molecules of parasite killing. Parasitology Today 6, 303–305.CrossRefGoogle ScholarPubMed
Kharsany, AB, Hoosen, AA, Moodley, J, Bagaratee, J and Gouws, E (1993) The association between sexually transmitted pathogens and cervical intra-epithelial neoplasia in a developing community. Genitourinary Medicine 69, 357–360.Google Scholar
Kissinger, P (2015) Trichomonas vaginalis: a review of epidemiologic, clinical and treatment issues. BMC Infectious Diseases 15, 307.CrossRefGoogle ScholarPubMed
Kissinger, P, Amedee, A, Clark, RA, Dumestre, J, Theall, KP, Myers, L, Hagensee, ME, Farley, TA and Martin, DH (2009) Trichomonas vaginalis treatment reduces vaginal HIV-1 shedding. Sexually Transmitted Diseases 36, 11–16.CrossRefGoogle ScholarPubMed
Knight, JS, Zhao, W, Luo, W, Subramanian, V, O'Dell, AA, Yalavarthi, S, Hodgin, JB, Eitzman, DT, Thompson, PR and Kaplan, MJ (2013) Peptidylarginine deiminase inhibition is immunomodulatory and vasculoprotective in murine lupus. The Journal of Clinical Investigation 123, 2981–2993.CrossRefGoogle ScholarPubMed
Kusunoki, Y, Nakazawa, D, Shida, H, Hattanda, F, Miyoshi, A, Masuda, S, Nishio, S, Tomaru, U, Atsumi, T and Ishizu, A (2016) Peptidylarginine deiminase inhibitor suppresses neutrophil extracellular trap formation and MPO-ANCA production. Frontiers in Immunology 7, 227.CrossRefGoogle ScholarPubMed
Lazenby, GB, Soper, DE and Nolte, FS (2013) Correlation of leukorrhea and Trichomonas vaginalis infection. Journal of Clinical Microbiology 51, 2323–2327.CrossRefGoogle ScholarPubMed
Leshner, M, Wang, S, Lewis, C, Zheng, H, Chen, XA, Santy, L and Wang, Y (2012) PAD4 mediated histone hypercitrullination induces heterochromatin decondensation and chromatin unfolding to form neutrophil extracellular trap-like structures. Frontiers in Immunology 3, 307.CrossRefGoogle ScholarPubMed
Levine, WC, Pope, V, Bhoomkar, A, Tambe, P, Lewis, JS, Zaidi, AA, Farshy, CE, Mitchell, S and Talkington, DF (1998) Increase in endocervical CD4 lymphocytes among women with nonulcerative sexually transmitted diseases. The Journal of Infectious Diseases 177, 167–174.CrossRefGoogle ScholarPubMed
Lin, Y, Roberts, TJ, Sriram, V, Cho, S and Brutkiewicz, RR (2003) Myeloid marker expression on antiviral CD8+ T cells following an acute virus infection. European Journal of Immunology 33, 2736–2743.CrossRefGoogle ScholarPubMed
Luo, Y, Arita, K, Bhatia, M, Knuckley, B, Lee, YH, Stallcup, MR, Sato, M and Thompson, PR (2006) Inhibitors and inactivators of protein arginine deiminase 4: functional and structural characterization. Biochemistry 45, 11727–11736.CrossRefGoogle ScholarPubMed
MacLennan, IC, Gulbranson-Judge, A, Toellner, KM, Casamayor-Palleja, M, Chan, E, Sze, DM, Luther, SA and Orbea, HA (1997) The changing preference of T and B cells for partners as T-dependent antibody responses develop. Immunology Reviews 156, 53–66.CrossRefGoogle Scholar
Malla, N, Valadkhani, Z, Harjai, K, Sharma, S and Gupta, I (2004) Reactive nitrogen intermediates in experimental trichomoniasis induced with isolates from symptomatic and asymptomatic women. Parasitology Research 94, 101–105.Google ScholarPubMed
Marcel, AM, Rojas, L, Rodríguez, SS, López, Y and Ramos, IS (2001) [Application of an alternative method to counting in Neubauer chamber to determine Trichomonas vaginalis concentrations]. Revista Cubana de Medicina Tropical 53, 180–188.Google Scholar
Marshall, HD, Chandele, A, Jung, YW, Meng, H, Poholek, AC, Parish, IA, Rutishauser, R, Cui, W, Kleinstein, SH, Craft, J and Kaech, SM (2011) Differential expression of Ly6C and T-bet distinguish effector and memory Th1 CD4(+) cell properties during viral infection. Immunity 35, 633–646.CrossRefGoogle ScholarPubMed
Mason, PR and Gwanzura, L (1990) Reduced lymphocyte responses to mitogens in natural and experimental trichomoniasis. Infection and Immunity 58, 3553–3557.CrossRefGoogle ScholarPubMed
Matsuda, JL, Zhang, Q, Ndonye, R, Richardson, SK, Howell, AR and Gapin, L (2006) T-bet concomitantly controls migration, survival, and effector functions during the development of Valpha14i NKT cells. Blood 107, 2797–2805.CrossRefGoogle ScholarPubMed
McClelland, RS, Sangare, L, Hassan, WM, Lavreys, L, Mandaliya, K, Kiarie, J, Ndinya-Achola, J, Jaoko, W and Baeten, JM (2007) Infection with Trichomonas vaginalis increases the risk of HIV-1 acquisition. The Journal of Infectious Diseases 195, 698–702.CrossRefGoogle ScholarPubMed
Menezes, CB and Tasca, T (2016) Trichomoniasis immunity and the involvement of the purinergic signaling. Biomedical Journal 39, 234–243.CrossRefGoogle ScholarPubMed
Mercer, F, Ng, SH, Brown, TM, Boatman, G and Johnson, PJ (2018) Neutrophils kill the parasite Trichomonas vaginalis using trogocytosis. PLoS Biology 16, e2003885.CrossRefGoogle ScholarPubMed
Metzler, KD, Goosmann, C, Lubojemska, A, Zychlinsky, A and Papayannopoulos, V (2014) A myeloperoxidase-containing complex regulates neutrophil elastase release and actin dynamics during NETosis. Cell Reports 8, 883–896.CrossRefGoogle ScholarPubMed
Misharin, AV, Morales-Nebreda, L, Mutlu, GM, Budinger, GR and Perlman, H (2013) Flow cytometric analysis of macrophages and dendritic cell subsets in the mouse lung. American Journal of Respiratory Cell Molecular Biology 49, 503–510.CrossRefGoogle ScholarPubMed
Misharin, AV, Cuda, CM, Saber, R, Turner, JD, Gierut, AK, Haines, GK, Berdnikovs, S, Filer, A, Clark, AR, Buckley, CD, Mutlu, GM, Budinger, GR and Perlman, H (2014) Nonclassical Ly6C(-) monocytes drive the development of inflammatory arthritis in mice. Cell Reports 9, 591–604.CrossRefGoogle ScholarPubMed
Morias, Y, Abels, C, Laoui, D, Van Overmeire, E, Guilliams, M, Schouppe, E, Tacke, F, deVries, CJ, De Baetselier, P and Beschin, A (2015) Ly6C-monocytes regulate parasite-induced liver inflammation by inducing the differentiation of pathogenic Ly6C+ monocytes into macrophages. PLoS Pathogens 11, e1004873.CrossRefGoogle ScholarPubMed
Nahrendorf, M, Swirski, FK, Aikawa, E, Stangenberg, L, Wurdinger, T, Figueiredo, JL, Libby, P, Weissleder, R and Pittet, MJ (2007) The healing myocardium sequentially mobilizes two monocyte subsets with divergent and complementary functions. Journal of Experimental Medicine 204, 3037–3047.CrossRefGoogle ScholarPubMed
Nam, YH, Min, A, Kim, SH, Lee, YA, Kim, KA, Song, KJ and Shin, MH (2012) Leukotriene B(4) receptors BLT1 and BLT2 are involved in interleukin-8 production in human neutrophils induced by Trichomonas vaginalis-derived secretory products. Inflammation Research 61, 97–102.CrossRefGoogle ScholarPubMed
Nemati, M, Malla, N, Yadav, M, Khorramdelazad, H and Jafarzadeh, A (2018) Humoral and T cell-mediated immune response against trichomoniasis. Parasite Immunology 40, 1–11. doi: 10.1111/pim.12510CrossRefGoogle Scholar
Nogal Ruiz, JJ, Escario, JA, Martinez Diaz, RA and Gomez Barrio, A (1997) Evaluation of a murine model of experimental trichomoniasis. Parasite 4, 127–132.CrossRefGoogle ScholarPubMed
Olmos-Ortiz, LM, Barajas-Mendiola, MA, Barrios-Rodiles, M, Castellano, LE, Arias-Negrete, S, Avila, EE and Cuéllar-Mata, P (2017) Trichomonas vaginalis exosome-like vesicles modify the cytokine profile and reduce inflammation in parasite-infected mice. Parasite Immunology 39, 1–10. doi: 10.1111/pim.12426CrossRefGoogle ScholarPubMed
Papayannopoulos, V, Metzler, KD, Hakkim, A and Zychlinsky, A (2010) Neutrophil elastase and myeloperoxidase regulate the formation of neutrophil extracellular traps. Journal of Cell Biology 191, 677–691.CrossRefGoogle ScholarPubMed
Park, GC, Ryu, JS and Min, DY (1997) The role of nitric oxide as an effector of macrophage-mediated cytotoxicity against Trichomonas vaginalis. The Korean Journal of Parasitology 35, 189–195.CrossRefGoogle ScholarPubMed
Petrin, D, Delgaty, K, Bhatt, R and Garber, G (1998) Clinical and microbiological aspects of Trichomonas vaginalis. Clinical Microbiology Reviews 11, 300–317.CrossRefGoogle ScholarPubMed
Reighard, SD, Sweet, RL, Vicetti Miguel, C, Vicetti Miguel, RD, Chivukula, M, Krishnamurti, U and Cherpes, TL (2011) Endometrial leukocyte subpopulations associated with Chlamydia trachomatis, Neisseria gonorrhoeae, and Trichomonas vaginalis genital tract infection. American Journal of Obstetrics & Gynecology 205, 324.e321–327.CrossRefGoogle ScholarPubMed
Rein, MF, Sullivan, JA and Mandell, GL (1980) Trichomonacidal activity of human polymorphonuclear neutrophils: killing by disruption and fragmentation. The Journal of Infection Diseases 142, 575–585.CrossRefGoogle ScholarPubMed
Röhm, M, Grimm, MJ, D'Auria, AC, Almyroudis, NG, Segal, BH and Urban, CF (2014) NADPH oxidase promotes neutrophil extracellular trap formation in pulmonary aspergillosis. Infection and Immunity 82, 1766–1777.CrossRefGoogle ScholarPubMed
Ryu, JS and Lloyd, D (1995) Cell cytotoxicity of sodium nitrite, sodium nitroprusside and Roussin's black salt against Trichomonas vaginalis. FEMS Microbiology Letters 130, 183–187.CrossRefGoogle ScholarPubMed
Ryu, JS, Kang, JH, Jung, SY, Shin, MH, Kim, JM, Park, H and Min, DY (2004) Production of interleukin-8 by human neutrophils stimulated with Trichomonas vaginalis. Infection and Immunity 72, 1326–1332.CrossRefGoogle ScholarPubMed
Shaio, MF, Lin, PR, Lee, CS, Hou, SC, Tang, P and Yang, KD (1992) A novel neutrophil-activating factor released by Trichomonas vaginalis. Infection and Immunity 60, 4475–4482.CrossRefGoogle ScholarPubMed
Shaio, MF, Lin, PR, Liu, JY and Tang, KD (1994) Monocyte-derived interleukin-8 involved in the recruitment of neutrophils induced by Trichomonas vaginalis infection. The Journal of Infection Diseases 170, 1638–1640.CrossRefGoogle ScholarPubMed
Shaio, MF, Lin, PR, Liu, JY and Yang, KD (1995) Generation of interleukin-8 from human monocytes in response to Trichomonas vaginalis stimulation. Infection and Immunity 63, 3864–3870.CrossRefGoogle ScholarPubMed
Smith, JD and Garber, GE (2015) Trichomonas vaginalis infection induces vaginal CD4+ T-cell infiltration in a mouse model: a vaccine strategy to reduce vaginal infection and HIV transmission. The Journal of Infection Diseases 212, 285–293.CrossRefGoogle Scholar
Song, HO, Shin, MH, Ahn, MH, Min, DY, Kim, YS and Ryu, JS (2008) Trichomonas vaginalis: reactive oxygen species mediates caspase-3 dependent apoptosis of human neutrophils. Experimental Parasitology 118, 59–65.CrossRefGoogle ScholarPubMed
Song, HO, Lim, YS, Moon, SJ, Ahn, MH and Ryu, JS (2010) Delayed human neutrophil apoptosis by Trichomonas vaginalis lysate. The Korean Journal of Parasitology 48, 1–7.CrossRefGoogle ScholarPubMed
Stadelmann, B, Hanevik, K, Andersson, MK, Bruserud, O and Svärd, SG (2013) The role of arginine and arginine-metabolizing enzymes during Giardia – host cell interactions in vitro. BMC Microbiology 13, 256.CrossRefGoogle ScholarPubMed
Swygard, H, Seña, AC, Hobbs, MM and Cohen, MS (2004) Trichomoniasis: clinical manifestations, diagnosis and management. Sexually Transmitted Infections 80, 91–95.CrossRefGoogle ScholarPubMed
Terrazas, C, Varikuti, S, Oghumu, S, Steinkamp, HM, Ardic, N, Kimble, J, Nakhasi, H and Satoskar, AR (2017) Ly6C. Scientific Report 7, 14693.CrossRefGoogle Scholar
Twu, O, de Miguel, N, Lustig, G, Stevens, GC, Vashisht, AA, Wohlschlegel, JA and Johnson, PJ (2013) Trichomonas vaginalis exosomes deliver cargo to host cells and mediate host∶parasite interactions. PLoS Pathogens 9, e1003482.CrossRefGoogle ScholarPubMed
Urban, CF, Reichard, U, Brinkmann, V and Zychlinsky, A (2006) Neutrophil extracellular traps capture and kill Candida albicans yeast and hyphal forms. Cell Microbiology 8, 668–676.CrossRefGoogle ScholarPubMed
Urban, CF, Ermert, D, Schmid, M, Abu-Abed, U, Goosmann, C, Nacken, W, Brinkmann, V, Jungblut, PR and Zychlinsky, A (2009) Neutrophil extracellular traps contain calprotectin, a cytosolic protein complex involved in host defense against Candida albicans. PLoS Pathogens 5, e1000639.CrossRefGoogle ScholarPubMed
Walunas, TL, Bruce, DS, Dustin, L, Loh, DY and Bluestone, JA (1995) Ly-6C is a marker of memory CD8+ T cells. The Journal of Immunology 155, 1873–1883.Google ScholarPubMed
Wang, Y, Li, M, Stadler, S, Correll, S, Li, P, Wang, D, Hayama, R, Leonelli, L, Han, H, Grigoryev, SA, Allis, CD and Coonrod, SA (2009) Histone hypercitrullination mediates chromatin decondensation and neutrophil extracellular trap formation. Journal of Cell Biology 184, 205–213.CrossRefGoogle ScholarPubMed
Wang, H, Li, T, Chen, S, Gu, Y and Ye, S (2015) Neutrophil extracellular trap mitochondrial DNA and its autoantibody in systemic lupus erythematosus and a proof-of-concept trial of metformin. Arthritis & Rheumatology 67, 3190–3200.CrossRefGoogle Scholar
Yano, A, Aosai, F, Yui, K, Kojima, S and Kawana, T (1983) Antigen-specific proliferation responses of peripheral blood lymphocytes to Trichomonas vaginalis antigen in patients with Trichomonas vaginitis. Journal of Clinical Microbiology 17, 175–180.CrossRefGoogle ScholarPubMed
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