Human natural killer cells acting as phagocytes against Candida albicans and mounting an inflammatory response that modulates neutrophil antifungal activity

Journal of Infectious Diseases

Volumn 209, Issue 4, 2014, Pages 616-626

  Voigt, Jessica ^a   Hünniger, Kerstin ^a   Bouzani, Maria ^e   Jacobsen, Ilse D ^b   Barz, Dagmar ^c   Hube, Bernhard ^a,b,d   Löffler, Jürgen ^e   Kurzai, Oliver ^a  

^a FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^b Department of Microbial Pathogenicity Mechanisms   (Germany)

^c JENA UNIVERSITY HOSPITAL   (Germany)

^d Center of Sepsis Control and Care   (Germany)

^e UNIVERSITY HOSPITAL WÜRZBURG   (Germany)

Author keywords

C. albicans; IFN ; neutrophils; NK cells; perforin; phagocytosis; TNF

Indexed keywords

C. ALBICANS; IFN-Γ; NEUTROPHILS; NK CELLS; PERFORIN; PHAGOCYTOSIS; TNF-Α;

CANDIDA ALBICANS; CELL COMMUNICATION; CELL DEGRANULATION; CELLS, CULTURED; CYTOKINES; HUMANS; KILLER CELLS, NATURAL; LYMPHOCYTE ACTIVATION; MICROSCOPY, FLUORESCENCE; NEUTROPHILS; PERFORIN; PHAGOCYTOSIS;

EID: 84893259804     PISSN: 00221899     EISSN: None     Source Type: Journal    
DOI: 10.1093/infdis/jit574     Document Type: Conference Paper

References (48)

1. Smyth MJ, Cretney E, Kelly JM, et al. Activation of NK cell cytotoxicity. Mol Immunol 2005; 42:501-10.
2. Zucchini N, Crozat K, Baranek T, Robbins SH, Altfeld M, Dalod M. Natural killer cells in immunodefense against infective agents. Expert Rev Anti Infect Ther 2008; 6:867-85.
3. van Dommelen SL, Sumaria N, Schreiber RD, Scalzo AA, Smyth MJ, Degli-Esposti MA. Perforin and granzymes have distinct roles in defensive immunity and immunopathology. Immunity 2006; 25:835-48.
4. Murphy JW, McDaniel DO. In vitro reactivity of natural killer (NK) cells against Cryptococcus neoformans. J Immunol 1982; 128:1577-83.
5. Hidore MR, Murphy JW. Natural cellular resistance of beige mice against Cryptococcus neoformans. J Immunol 1986; 137:3624-31.
6. Ma LL, Wang CL, Neely GG, Epelman S, Krensky AM, Mody CH. NK cells use perforin rather than granulysin for anticryptococcal activity. J Immunol 2004; 173:3357-65.
7. Jimenez BE, Murphy JW. In vitro effects of natural killer cells against Paracoccidioides brasiliensis yeast phase. Infect Immun 1984; 46:552-8.
8. Petkus AF, Baum LL. Natural killer cell inhibition of young spherules and endospores of Coccidioides immitis. J Immunol 1987; 139:3107-11.
9. Passweg JR, Koehl U, Uharek L, Meyer-Monard S, Tichelli A. Naturalkiller-cell-based treatment in haematopoietic stem-cell transplantation. Best Pract Res Clin Haematol 2006; 19:811-24.
10. Morrison BE, Park SJ, Mooney JM, Mehrad B. Chemokine-mediated recruitment of NK cells is a critical host defense mechanism in invasive aspergillosis. J Clin Invest 2003; 112:1862-70.
11. Park SJ, Hughes MA, Burdick M, Strieter RM, Mehrad B. Early NK cell-derived IFN-gamma is essential to host defense in neutropenic invasive aspergillosis. J Immunol 2009; 182:4306-12.
12. Schmidt S, Tramsen L, Hanisch M, et al. Human natural killer cells exhibit direct activity against Aspergillus fumigatus hyphae, but not against resting conidia. J Infect Dis 2011; 203:430-5.
13. Bouzani M, Ok M, McCormick A, et al. Human NK cells display important antifungal activity against Aspergillus fumigatus, which is directly mediated by IFN-gamma release. J Immunol 2011; 187: 1369-76.
14. Beno DW, Stover AG, Mathews HL. Growth inhibition of Candida albicans hyphae by CD8+ lymphocytes. J Immunol 1995; 154:5273-81.
15. Arancia G, Molinari A, Crateri P, et al. Noninhibitory binding of human interleukin-2-activated natural killer cells to the germ tube forms of Candida albicans. Infect Immun 1995; 63:280-8.
16. Arancia G, Stringaro A, Crateri P, et al. Interaction between human interleukin-2-activated natural killer cells and heat-killed germ tube forms of Candida albicans. Cell Immunol 1998; 186:28-38.
17. Mathews HL, Witek-Janusek L. Antifungal activity of interleukin-2- activated natural killer (NK1.1+) lymphocytes against Candida albicans. J Med Microbiol 1998; 47:1007-14.
18. Balish E, Warner T, Pierson CJ, Bock DM, Wagner RD. Oroesophageal candidiasis is lethal for transgenic mice with combined natural killer and T-cell defects. Med Mycol 2001; 39:261-8.
19. Djeu JY, Blanchard DK, Richards AL, Friedman H. Tumor necrosis factor induction by Candida albicans from human natural killer cells and monocytes. J Immunol 1988; 141:4047-52.
20. Scaringi L, Rosati E, Cornacchione P, et al. Local and systemic immune response to inactivated Candida albicans in mice. Nat Immun 1995; 14:234-49.
21. Djeu JY, Blanchard DK, Halkias D, Friedman H. Growth inhibition of Candida albicans by human polymorphonuclear neutrophils: activation by interferon-gamma and tumor necrosis factor. J Immunol 1986; 137:2980-4.
22. Marodi L, Schreiber S, Anderson DC, MacDermott RP, Korchak HM, Johnston RB Jr. Enhancement of macrophage candidacidal activity by interferon-gamma: increased phagocytosis, killing, and calcium signal mediated by a decreased number of mannose receptors. J Clin Invest 1993; 91:2596-601.
23. Ferrante A. Tumor necrosis factor alpha potentiates neutrophil antimicrobial activity: increased fungicidal activity against Torulopsis glabrata and Candida albicans and associated increases in oxygen radical production and lysosomal enzyme release. Infect Immun 1989; 57: 2115-22.
24. Algarra I, Ortega E, Serrano MJ, Alvarez de Cienfuegos G, Gaforio JJ. Suppression of splenic macrophage Candida albicans phagocytosis following in vivo depletion of natural killer cells in immunocompetent BALB/c mice and T-cell-deficient nude mice. FEMS Immunol Med Microbiol 2002; 33:159-63.
25. Gaforio JJ, Ortega E, Algarra I, Serrano MJ, Alvarez de Cienfuegos G. NK cells mediate increase of phagocytic activity but not of proinflammatory cytokine (interleukin-6 [IL-6], tumor necrosis factor alpha, and IL-12) production elicited in splenic macrophages by tilorone treatment of mice during acute systemic candidiasis. Clin Diagn Lab Immunol 2002; 9:1282-94.
26. Naora H, Gougeon ML. Enhanced survival and potent expansion of the natural killer cell population of HIV-infected individuals by exogenous interleukin-15. Immunol Lett 1999; 68:359-67.
27. Wozniok I, Hornbach A, Schmitt C, et al. Induction of ERK-kinase signalling triggers morphotype-specific killing of Candida albicans filaments by human neutrophils. Cell Microbiol 2008; 10:807-20.
28. Bryceson YT, March ME, Barber DF, Ljunggren HG, Long EO. Cytolytic granule polarization and degranulation controlled by different receptors in resting NK cells. J Exp Med 2005; 202:1001-12.
29. Kataoka T, Shinohara N, Takayama H, et al. Concanamycin A, a powerful tool for characterization and estimation of contribution of perforinand Fas-based lytic pathways in cell-mediated cytotoxicity. J Immunol 1996; 156:3678-86.
30. Costantini C, Micheletti A, Calzetti F, Perbellini O, Pizzolo G, Cassatella MA. Neutrophil activation and survival are modulated by interaction with NK cells. Int Immunol 2010; 22:827-38.
31. Gresnigt MS, Joosten LA, Verschueren I, et al. Neutrophil-mediated inhibition of proinflammatory cytokine responses. J Immunol 2012; 189:4806-15.
32. Miller JS, Soignier Y, Panoskaltsis-Mortari A, et al. Successful adoptive transfer and in vivo expansion of human haploidentical NK cells in patients with cancer. Blood 2005; 105:3051-7.
33. Huenecke S, Zimmermann SY, Kloess S, et al. IL-2-driven regulation of NK cell receptors with regard to the distribution of CD16+ and CD16-subpopulations and in vivo influence after haploidentical NK cell infusion. J Immunother 2010; 33:200-10.
34. Suck G, Koh MB. Emerging natural killer cell immunotherapies: largescale ex vivo production of highly potent anticancer effectors. Hematol Oncol Stem Cell Ther 2010; 3:135-42.
35. Sone S, Utsugi T, Nii A, Ogura T. Differential effects of recombinant interferons alpha, beta, and gamma on induction of human lymphokine (IL-2)-activated killer activity. J Natl Cancer Inst 1988; 80:425-31.
36. Kurzai O, Schmitt C, Brocker E, Frosch M, Kolb-Maurer A. Polymorphism of Candida albicans is a major factor in the interaction with human dendritic cells. Int J Med Microbiol 2005; 295:121-7.
37. Banerjee PP, Pandey R, Zheng R, Suhoski MM, Monaco-Shawver L, Orange JS. Cdc42-interacting protein-4 functionally links actin and microtubule networks at the cytolytic NK cell immunological synapse. J Exp Med 2007; 204:2305-20.
38. Orange JS, Harris KE, Andzelm MM, Valter MM, Geha RS, Strominger JL. The mature activating natural killer cell immunologic synapse is formed in distinct stages. Proc Natl Acad Sci USA 2003; 100: 14151-6.
39. Wulfing C, Purtic B, Klem J, Schatzle JD. Stepwise cytoskeletal polarization as a series of checkpoints in innate but not adaptive cytolytic killing. Proc Natl Acad Sci USA 2003; 100:7767-72.
40. Alter G, Malenfant JM, Altfeld M. CD107a as a functional marker for the identification of natural killer cell activity. J Immunol Methods 2004; 294:15-22.
41. Grzywacz B, Kataria N, Verneris MR. CD56dimCD16+ NK cells downregulate CD16 following target cell induced activation of matrix metalloproteinases. Leukemia 2007; 21:356-9; author reply 359.
42. Joag S, Zychlinsky A, Young JD. Mechanisms of lymphocyte-mediated lysis. J Cell Biochem 1989; 39:239-52.
43. Robertson MJ, Ritz J. Biology and clinical relevance of human natural killer cells. Blood 1990; 76:2421-38.
44. Marr KJ, Jones GJ, Zheng C, et al. Cryptococcus neoformans directly stimulates perforin production and rearms NK cells for enhanced anticryptococcal microbicidal activity. Infect Immun 2009; 77: 2436-46.
45. Fulurija A, Ashman RB, Papadimitriou JM. Neutrophil depletion increases susceptibility to systemic and vaginal candidiasis in mice, and reveals differences between brain and kidney in mechanisms of host resistance. Microbiology 1996; 142 (Pt 12):3487-96.
46. Anaissie EJ, Rex JH, Uzun O, Vartivarian S. Predictors of adverse outcome in cancer patients with candidemia. Am J Med 1998; 104:238-45.
47. Costantini C, Cassatella MA. The defensive alliance between neutrophils and NK cells as a novel arm of innate immunity. J Leukoc Biol 2011; 89:221-33.
48. Quintin J, Saeed S, Martens JH, et al. Candida albicans infection affords protection against reinfection via functional reprogramming of monocytes. Cell Host Microbe 2012; 12:223-32.