Neisseria gonorrhoeae modulates immunity by polarizing human macrophages to a M2 profile

PLoS ONE

Volumn 10, Issue 6, 2015, Pages

  Ortiz, María Carolina ^a   Lefimil, Claudia ^a   Rodas, Paula I ^b   Vernal, Rolando ^a   Lopez, Mercedes ^c   Acuña Castillo, Claudio ^d   Imarai, Mónica ^d   Escobar, Alejandro ^a  

^a UNIVERSITY OF CHILE   (Chile)

^b UNIVERSIDAD ANDRÉS BELLO   (Chile)

^c UNIVERSITY OF CHILE   (Chile)

^d UNIVERSIDAD DE SANTIAGO DE CHILE   (Chile)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SURFACE MARKER; CYTOKINE; GENTAMICIN; PROGRAMMED DEATH 1 LIGAND 1; CD274 PROTEIN, HUMAN;

ARTICLE; CONTROLLED STUDY; GONORRHEA; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNE EVASION; IMMUNE RESPONSE; IMMUNOFLUORESCENCE; IMMUNOMODULATION; LYMPHOCYTE PROLIFERATION; MACROPHAGE; MACROPHAGE ACTIVATION; NEISSERIA GONORRHOEAE; NONHUMAN; PHAGOCYTOSIS; PHENOTYPE; POLARIZATION; SIGNAL TRANSDUCTION; T LYMPHOCYTE; UPREGULATION; CELL PROLIFERATION; IMMUNOLOGY; MICROBIOLOGY; MONOCYTE; PHYSIOLOGY;

NEISSERIA; NEISSERIA GONORRHOEAE;

ANTIGENS, CD274; CELL PROLIFERATION; GONORRHEA; HUMANS; MACROPHAGES; MONOCYTES; NEISSERIA GONORRHOEAE; PHENOTYPE; T-LYMPHOCYTES; UP-REGULATION;

EID: 84938704360     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0130713     Document Type: Article

References (54)

1. WHO. Global action plan to control the spread and impact of antimicrobial resistance in Neisseria gonorrhoeae. 2012.1
2. Handsfield HH, Lipman TO, Harnisch JP, Tronca E, Holmes KK. Asymptomatic gonorrhea in men. Diagnosis, natural course, prevalence and significance. N Engl J Med. 1974 Jan 17; 290(3):117-23.106 PMID: 4202519
3. Farley TA, Cohen DA, Wu SY, Besch CL. The value of screening for sexually transmitted diseases in an HIV clinic. J Acquir Immune Defic Syndr. 2003 Aug 15; 33(5):642-8.345 PMID: 12902810
4. Fleming DT, Wasserheit JN. From epidemiological synergy to public health policy and practice: the contribution of other sexually transmitted diseases to sexual transmission of HIV infection. Sex Transm Infect. 1999 Feb; 75(1):3-17.346 PMID: 10448335
5. Feinen B, Jerse AE, Gaffen SL, Russell MW. Critical role of Th17 responses in a murine model of Neisseria gonorrhoeae genital infection. Mucosal Immunol. 2010 May; 3(3):312-21.444 doi: 10.1038/mi.2009.139 PMID: 20107432
6. Fox KK, Thomas JC, Weiner DH, Davis RH, Sparling PF, Cohen MS. Longitudinal evaluation of serovar-specific immunity to Neisseria gonorrhoeae. Am J Epidemiol. 1999 Feb 15; 149(4):353-8.344 PMID: 10025478
7. Hedges SR, Mayo MS, Mestecky J, Hook EW 3rd, Russell MW. Limited local and systemic antibody responses to Neisseria gonorrhoeae during uncomplicated genital infections. Infect Immun. 1999 Aug; 67(8):3937-46.2 PMID: 10417159
8. Imarai M, Candia E, Rodriguez-Tirado C, Tognarelli J, Pardo M, Perez T, et al. Regulatory T cells are locally induced during intravaginal infection of mice with Neisseria gonorrhoeae. Infect Immun. 2008 Dec; 76(12):5456-65.123 doi: 10.1128/IAI.00552-08 PMID: 18824531
9. Liu Y, Islam EA, Jarvis GA, Gray-Owen SD, Russell MW. Neisseria gonorrhoeae selectively suppresses the development of Th1 and Th2 cells, and enhances Th17 cell responses, through TGF-beta-dependent mechanisms. Mucosal Immunol. 2012 May; 5(3):320-31.349 doi: 10.1038/mi.2012.12 PMID: 22354319
10. Liu Y, Liu W, Russell MW. Suppression of host adaptive immune responses by Neisseria gonorrhoeae: role of interleukin 10 and type 1 regulatory T cells. Mucosal Immunol. 2013 Jun 12.348
11. Plant LJ, Jonsson AB. Type IV pili of Neisseria gonorrhoeae influence the activation of human CD4+ T cells. Infect Immun. 2006 Jan; 74(1):442-8.229 PMID: 16369000
12. Boulton IC, Gray-Owen SD. Neisserial binding to CEACAM1 arrests the activation and proliferation of CD4+ T lymphocytes. Nat Immunol. 2002 Mar; 3(3):229-36.23 PMID: 11850628
13. Lee HS, Ostrowski MA, Gray-Owen SD. CEACAM1 dynamics during neisseria gonorrhoeae suppression of CD4+ T lymphocyte activation. J Immunol. 2008 May 15; 180(10):6827-35.359 PMID: 18453603
14. Zhu W, Ventevogel MS, Knilans KJ, Anderson JE, Oldach LM, McKinnon KP, et al. Neisseria gonorrhoeae Suppresses Dendritic Cell-Induced, Antigen-Dependent CD4 T Cell Proliferation. PLoS One. 2012; 7(7):e41260.558 doi: 10.1371/journal.pone.0041260 PMID: 22844448
15. Escobar A, Candia E, Reyes-Cerpa S, Villegas-Valdes B, Neira T, Lopez M, et al. Neisseria gonorrhoeae Induces a Tolerogenic Phenotype in Macrophages to Modulate Host Immunity. Mediators Inflamm. 2013; 2013:127017.361 doi: 10.1155/2013/127017 PMID: 24204097
16. Biswas SK, Mantovani A. Macrophage plasticity and interaction with lymphocyte subsets: cancer as a paradigm. Nat Immunol. 2010 Oct; 11(10):889-96.418 doi: 10.1038/ni.1937 PMID: 20856220
17. Sica A, Mantovani A. Macrophage plasticity and polarization: in vivo veritas. J Clin Invest. 2012 Mar 1; 122(3):787-95.535 doi: 10.1172/JCI59643 PMID: 22378047
18. Wynn TA, Chawla A, Pollard JW. Macrophage biology in development, homeostasis and disease. Nature. 2013 Apr 25; 496(7446):445-55.559 doi: 10.1038/nature12034 PMID: 23619691
19. Benoit M, Barbarat B, Bernard A, Olive D, Mege JL. Coxiella burnetii, the agent of Q fever, stimulates an atypical M2 activation program in human macrophages. Eur J Immunol. 2008 Apr; 38(4):1065-70.415 doi: 10.1002/eji.200738067 PMID: 18350541
20. Mege JL, Mehraj V, Capo C. Macrophage polarization and bacterial infections. Curr Opin Infect Dis. 2011 Jun; 24(3):230-4.504 doi: 10.1097/QCO.0b013e328344b73e PMID: 21311324
21. Tumitan AR, Monnazzi LG, Ghiraldi FR, Cilli EM, Machado de Medeiros BM. Pattern of macrophage activation in yersinia-resistant and yersinia-susceptible strains of mice. Microbiol Immunol. 2007; 51(10):1021-8.542 PMID: 17951992
22. Kiszewski AE, Becerril E, Aguilar LD, Kader IT, Myers W, Portaels F, et al. The local immune response in ulcerative lesions of Buruli disease. Clin Exp Immunol. 2006 Mar; 143(3):445-51.477 PMID: 16487243
23. Duncan JA, Gao X, Huang MT, O'Connor BP, Thomas CE, Willingham SB, et al. Neisseria gonorrhoeae activates the proteinase cathepsin B to mediate the signaling activities of the NLRP3 and ASC-containing inflammasome. J Immunol. 2009 May 15; 182(10):6460-9.68 doi: 10.4049/jimmunol.0802696 PMID: 19414800
24. Christodoulides M, Everson JS, Liu BL, Lambden PR, Watt PJ, Thomas EJ, et al. Interaction of primary human endometrial cells with Neisseria gonorrhoeae expressing green fluorescent protein. Mol Microbiol. 2000 Jan; 35(1):32-43.42 PMID: 10632875
25. Gomez-Duarte OG, Dehio M, Guzman CA, Chhatwal GS, Dehio C, Meyer TF. Binding of vitronectin to opa-expressing Neisseria gonorrhoeae mediates invasion of HeLa cells. Infect Immun. 1997 Sep; 65 (9):3857-66.292 PMID: 9284164
26. Vernal R, Velasquez E, Gamonal J, Garcia-Sanz JA, Silva A, Sanz M. Expression of proinflammatory cytokines in osteoarthritis of the temporomandibular joint. Arch Oral Biol. 2008 Oct; 53(10):910-5.588 doi: 10.1016/j.archoralbio.2008.04.004 PMID: 18508030
27. Fleetwood AJ, Dinh H, Cook AD, Hertzog PJ, Hamilton JA. GM-CSF- and M-CSF-dependent macrophage phenotypes display differential dependence on type I interferon signaling. J Leukoc Biol. 2009 Aug; 86(2):411-21.560 doi: 10.1189/jlb.1108702 PMID: 19406830
28. Benoit M, Desnues B, Mege JL. Macrophage polarization in bacterial infections. J Immunol. 2008 Sep 15; 181(6):3733-9.416 PMID: 18768823
29. Butte MJ, Keir ME, Phamduy TB, Sharpe AH, Freeman GJ. Programmed death-1 ligand 1 interacts specifically with the B7-1 costimulatory molecule to inhibit T cell responses. Immunity. 2007 Jul; 27 (1):111-22.397 PMID: 17629517
30. Chen L. Co-inhibitory molecules of the B7-CD28 family in the control of T-cell immunity. Nat Rev Immunol. 2004 May; 4(5):336-47.409 PMID: 15122199
31. Okazaki T, Honjo T. PD-1 and PD-1 ligands: from discovery to clinical application. Int Immunol. 2007 Jul; 19(7):813-24.618 PMID: 17606980
32. Dong H, Zhu G, Tamada K, Chen L. B7-H1, a third member of the B7 family, co-stimulates T-cell proliferation and interleukin-10 secretion. Nat Med. 1999 Dec; 5(12):1365-9.619 PMID: 10581077
33. Baecher-Allan C, Brown JA, Freeman GJ, Hafler DA. CD4+CD25+ regulatory cells from human peripheral blood express very high levels of CD25 ex vivo. Novartis Found Symp. 2003; 252:67-88; discussion -91, 106-14.624 PMID: 14609213
34. Krupnick AS, Gelman AE, Barchet W, Richardson S, Kreisel FH, Turka LA, et al. Murine vascular endothelium activates and induces the generation of allogeneic CD4+25+Foxp3+ regulatory T cells. J Immunol. 2005 Nov 15; 175(10):6265-70.625 PMID: 16272276
35. Francisco LM, Salinas VH, Brown KE, Vanguri VK, Freeman GJ, Kuchroo VK, et al. PD-L1 regulates the development, maintenance, and function of induced regulatory T cells. J Exp Med. 2009 Dec 21; 206(13):3015-29.405 doi: 10.1084/jem.20090847 PMID: 20008522
36. Mantovani A, Sica A, Sozzani S, Allavena P, Vecchi A, Locati M. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol. 2004 Dec; 25(12):677-86.496 PMID: 15530839
37. Zizzo G, Hilliard BA, Monestier M, Cohen PL. Efficient clearance of early apoptotic cells by human macrophages requires M2c polarization and MerTK induction. J Immunol. 2012 Oct 1; 189(7):3508-20.589 PMID: 22942426
38. Vogel DY, Vereyken EJ, Glim JE, Heijnen PD, Moeton M, van der Valk P, et al. Macrophages in inflammatory multiple sclerosis lesions have an intermediate activation status. J Neuroinflammation. 2013; 10:35.581 doi: 10.1186/1742-2094-10-35 PMID: 23452918
39. Sundquist M, Wick MJ. TNF-alpha-dependent and-independent maturation of dendritic cells and recruited CD11c(int)CD11b+ Cells during oral Salmonella infection. J Immunol. 2005 Sep 1; 175 (5):3287-98.627 PMID: 16116221
40. Mihret A, Mamo G, Tafesse M, Hailu A, Parida S. Dendritic Cells Activate and Mature after Infection with Mycobacterium tuberculosis. BMC Res Notes. 2011; 4:247.628 doi: 10.1186/1756-0500-4-247 PMID: 21777464
41. Acuto O, Michel F. CD28-mediated co-stimulation: a quantitative support for TCR signalling. Nat Rev Immunol. 2003 Dec; 3(12):939-51.583 PMID: 14647476
42. Abel B, Thieblemont N, Quesniaux VJ, Brown N, Mpagi J, Miyake K, et al. Toll-like receptor 4 expression is required to control chronic Mycobacterium tuberculosis infection in mice. J Immunol. 2002 Sep 15; 169(6):3155-62.563 PMID: 12218133
43. Ravetch JV, Kinet JP. Fc receptors. Annu Rev Immunol. 1991; 9:457-92.585 PMID: 1910686
44. Hristodorov D, Mladenov R, Huhn M, Barth S, Thepen T. Macrophage-targeted therapy: CD64-based immunotoxins for treatment of chronic inflammatory diseases. Toxins (Basel). 2012 Sep; 4(9):676-94.601
45. Packiam M, Veit SJ, Anderson DJ, Ingalls RR, Jerse AE. Mouse strain-dependent differences in susceptibility to Neisseria gonorrhoeae infection and induction of innate immune responses. Infect Immun. 2010 Jan; 78(1):433-40.615 doi: 10.1128/IAI.00711-09 PMID: 19901062
46. Saraiva M, O'Garra A. The regulation of IL-10 production by immune cells. Nat Rev Immunol. 2010 Mar; 10(3):170-81.605 doi: 10.1038/nri2711 PMID: 20154735
47. Guleria I, Khosroshahi A, Ansari MJ, Habicht A, Azuma M, Yagita H, et al. A critical role for the programmed death ligand 1 in fetomaternal tolerance. J Exp Med. 2005 Jul 18; 202(2):231-7.629 PMID: 16027236
48. Mozaffarian N, Wiedeman AE, Stevens AM. Active systemic lupus erythematosus is associated with failure of antigen-presenting cells to express programmed death ligand-1. Rheumatology (Oxford). 2008 Sep; 47(9):1335-41.630
49. Hirata S, Senju S, Matsuyoshi H, Fukuma D, Uemura Y, Nishimura Y. Prevention of experimental autoimmune encephalomyelitis by transfer of embryonic stem cell-derived dendritic cells expressing myelin oligodendrocyte glycoprotein peptide along with TRAIL or programmed death-1 ligand. J Immunol. 2005 Feb 15; 174(4):1888-97.631 PMID: 15699115
50. Ding H, Wu X, Wu J, Yagita H, He Y, Zhang J, et al. Delivering PD-1 inhibitory signal concomitant with blocking ICOS co-stimulation suppresses lupus-like syndrome in autoimmune BXSB mice. Clin Immunol. 2006 Feb-Mar; 118(2-3):258-67.632 PMID: 16386962
51. Bruhns P. Properties of mouse and human IgG receptors and their contribution to disease models. Blood. 2012 Jun 14; 119(24):5640-9.600 doi: 10.1182/blood-2012-01-380121 PMID: 22535666
52. Kiekens RC, Thepen T, Bihari IC, Knol EF, Van De Winkel JG, Bruijnzeel-Koomen CA. Expression of Fc receptors for IgG during acute and chronic cutaneous inflammation in atopic dermatitis. Br J Dermatol. 2000 Jun; 142(6):1106-13.602 PMID: 10848732
53. Jounai K, Ikado K, Sugimura T, Ano Y, Braun J, Fujiwara D. Spherical lactic acid bacteria activate plasmacytoid dendritic cells immunomodulatory function via TLR9-dependent crosstalk with myeloid dendritic cells. PLoS One. 2012; 7(4):e32588.610 doi: 10.1371/journal.pone.0032588 PMID: 22505996
54. Peng B, Lu C, Tang L, Yeh IT, He Z, Wu Y, et al. Enhanced upper genital tract pathologies by blocking Tim-3 and PD-L1 signaling pathways in mice intravaginally infected with Chlamydia muridarum. BMC Infect Dis. 2011; 11:347.611 doi: 10.1186/1471-2334-11-347 PMID: 22168579