An Acidic Microenvironment Increases NK Cell Killing of Cryptococcus neoformans and Cryptococcus gattii by Enhancing Perforin Degranulation

PLoS Pathogens

Volumn 9, Issue 7, 2013, Pages

  Islam, Anowara ^a   Li, Shu Shun ^a   Oykhman, Paul ^a   Timm McCann, Martina ^a   Huston, Shaunna M ^a   Stack, Danuta ^a   Xiang, Richard F ^a   Kelly, Margaret M ^a   Mody, Christopher H ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 3; PERFORIN; PROPIDIUM IODIDE;

ACIDITY; ANIMAL CELL; ANTINEOPLASTIC ACTIVITY; ARTICLE; COLONY FORMING UNIT; CONJUGATION; CONTROLLED STUDY; CRYPTOCOCCOSIS; CRYPTOCOCCUS GATTII; CRYPTOCOCCUS NEOFORMANS; FLOW CYTOMETRY; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOBLOTTING; MICROENVIRONMENT; NATURAL KILLER CELL; NONHUMAN;

EID: 84884790029     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003439     Document Type: Article

References (61)

1. Islam A, Mody CH, (2011) Management of fungal lung disease in the immunocompromised. Ther Adv Respir Dis 5: 305-324.
2. Bartlett KH, Cheng PY, Duncan C, Galanis E, Hoang L, et al. (2012) A decade of experience: Cryptococcus gattii in British Columbia. Mycopathologia 173: 311-319.
3. Chen S, Sorrell T, Nimmo G, Speed B, Currie B, et al. (2000) Epidemiology and host- and variety-dependent characteristics of infection due to Cryptococcus neoformans in Australia and New Zealand. Australasian Cryptococcal Study Group. Clin Infect Dis 31: 499-508.
4. Galanis E, Macdougall L, (2010) Epidemiology of Cryptococcus gattii, British Columbia, Canada, 1999-2007. Emerg Infect Dis 16: 251-257.
5. Dewar GJ, Kelly JK, (2008) Cryptococcus gattii: an emerging cause of pulmonary nodules. Can Respir J 15: 153-157.
6. Hidore MR, Murphy JW, (1986) Correlation of natural killer cell activity and clearance of Cryptococcus neoformans from mice after adoptive transfer of splenic nylon wool-nonadherent cells. Infect Immun 51: 547-555.
7. Salkowski CA, Balish E, (1991) Role of natural killer cells in resistance to systemic cryptococcosis. J Leukoc Biol 50: 151-159.
8. Lipscomb MF, Alvarellos T, Toews GB, Tompkins R, Evans Z, et al. (1987) Role of natural killer cells in resistance to Cryptococcus neoformans infections in mice. Am J Pathol 128: 354-361.
9. Bhat R, Watzl C, (2007) Serial killing of tumor cells by human natural killer cells-enhancement by therapeutic antibodies. PLoS One 2: e326.
10. Vieillard V, Strominger JL, Debré P, (2005) NK cytotoxicity against CD4+ T cells during HIV-1 infection: a gp41 peptide induces the expression of an NKp44 ligand. Proc Natl Acad Sci U S A 102: 10981-10986.
11. Jimenez BE, Murphy JW, (1984) In vitro effects of natural killer cells against Paracoccidioides brasiliensis yeast phase. Infect Immun 46: 552-558.
12. Longhi LN, da Silva RM, Fornazim MC, Spago MC, de Oliveira RT, et al. (2012) Phenotypic and Functional Characterization of NK Cells in Human Immune Response against the Dimorphic Fungus Paracoccidioides brasiliensis. J Immunol 189: 935-945.
13. Wright L, Bubb W, Davidson J, Santangelo R, Krockenberger M, et al. (2002) Metabolites released by Cryptococcus neoformans var. neoformans and var. gattii differentially affect human neutrophil function. Microbes Infect 4: 1427-1438.
14. Bubb WA, Wright LC, Cagney M, Santangelo RT, Sorrell TC, et al. (1999) Heteronuclear NMR studies of metabolites produced by Cryptococcus neoformans in culture media: identification of possible virulence factors. Magn Reson Med 42: 442-453.
15. Schornack PA, Gillies RJ, (2003) Contributions of cell metabolism and H+ diffusion to the acidic pH of tumors. Neoplasia 5: 135-145.
16. Thistlethwaite AJ, Leeper DB, Moylan DJ, Nerlinger RE, (1985) pH distribution in human tumors. Int J Radiat Oncol Biol Phys 11: 1647-1652.
17. Fischer B, Müller B, Fischer KG, Baur N, Kreutz W, (2000) Acidic pH inhibits non-MHC-restricted killer cell functions. Clin Immunol 96: 252-263.
18. Vivier E, Ugolini S, Blaise D, Chabannon C, Brossay L, (2012) Targeting natural killer cells and natural killer T cells in cancer. Nat Rev Immunol 12: 239-252.
19. Loeffler DA, Juneau PL, Heppner GH, (1991) Natural killer-cell activity under conditions reflective of tumor micro-environment. Int J Cancer 48: 895-899.
20. Redegeld F, Filippini A, Sitkovsky M, (1991) Comparative studies of the cytotoxic T lymphocyte-mediated cytotoxicity and of extracellular ATP-induced cell lysis. Different requirements in extracellular Mg2+ and pH. J Immunol 147: 3638-3645.
21. Wiseman JC, Ma LL, Marr KJ, Jones GJ, Mody CH, (2007) Perforin-dependent cryptococcal microbicidal activity in NK cells requires PI3K-dependent ERK1/2 signaling. J Immunol 178: 6456-6464.
22. Ma LL, Spurrell JC, Wang JF, Neely GG, Epelman S, et al. (2002) CD8 T cell-mediated killing of Cryptococcus neoformans requires granulysin and is dependent on CD4 T cells and IL-15. J Immunol 169: 5787-5795.
23. Ma LL, Wang CL, Neely GG, Epelman S, Krensky AM, et al. (2004) NK cells use perforin rather than granulysin for anticryptococcal activity. J Immunol 173: 3357-3365.
24. Schaffner A, Douglas H, Braude A, (1982) Selective protection against conidia by mononuclear and against mycelia by polymorphonuclear phagocytes in resistance to Aspergillus. Observations on these two lines of defense in vivo and in vitro with human and mouse phagocytes. J Clin Invest 69: 617-631.
25. Fuller SA, Takahashi M, Hurrell JG, (2001) Cloning of hybridoma cell lines by limiting dilution. Curr Protoc Mol Biol Chapter 11: Unit11.18.
26. Marr KJ, Jones GJ, Zheng C, Huston SM, Timm-McCann M, et al. (2009) Cryptococcus neoformans directly stimulates perforin production and rearms NK cells for enhanced anticryptococcal microbicidal activity. Infect Immun 77: 2436-2446.
27. Uellner R, Zvelebil MJ, Hopkins J, Jones J, MacDougall LK, et al. (1997) Perforin is activated by a proteolytic cleavage during biosynthesis which reveals a phospholipid-binding C2 domain. EMBO J 16: 7287-7296.
28. Masson D, Peters PJ, Geuze HJ, Borst J, Tschopp J, (1990) Interaction of chondroitin sulfate with perforin and granzymes of cytolytic T-cells is dependent on pH. Biochemistry 29: 11229-11235.
29. Chaushu S, Wilensky A, Gur C, Shapira L, Elboim M, et al. (2012) Direct recognition of Fusobacterium nucleatum by the NK cell natural cytotoxicity receptor NKp46 aggravates periodontal disease. PLoS Pathog 8: e1002601.
30. Raghavan M, Bonagura VR, Morrison SL, Bjorkman PJ, (1995) Analysis of the pH dependence of the neonatal Fc receptor/immunoglobulin G interaction using antibody and receptor variants. Biochemistry 34: 14649-14657.
31. López DH, Trevani AS, Salamone G, Andonegui G, Raiden S, et al. (1999) Acidic pH increases the avidity of FcgammaR for immune complexes. Immunology 98: 450-455.
32. Trevani AS, Andonegui G, Giordano M, López DH, Gamberale R, et al. (1999) Extracellular acidification induces human neutrophil activation. J Immunol 162: 4849-4857.
33. Fischer B, Müller B, Fisch P, Kreutz W, (2000) An acidic microenvironment inhibits antitumoral non-major histocompatibility complex-restricted cytotoxicity: implications for cancer immunotherapy. J Immunother 23: 196-207.
34. Hidore MR, Murphy JW, (1989) Murine natural killer cell interactions with a fungal target, Cryptococcus neoformans. Infect Immun 57: 1990-1997.
35. Murphy JW, Hidore MR, Nabavi N, (1991) Binding interactions of murine natural killer cells with the fungal target Cryptococcus neoformans. Infect Immun 59: 1476-1488.
36. Nabavi N, Murphy JW, (1985) In vitro binding of natural killer cells to Cryptococcus neoformans targets. Infect Immun 50: 50-57.
37. Jones GJ, Wiseman JC, Marr KJ, Wei S, Djeu JY, et al. (2009) In contrast to anti-tumor activity, YT cell and primary NK cell cytotoxicity for Cryptococcus neoformans bypasses LFA-1. Int Immunol 21: 423-432.
38. Martínez D, Vermeulen M, von Euw E, Sabatté J, Maggíni J, et al. (2007) Extracellular acidosis triggers the maturation of human dendritic cells and the production of IL-12. J Immunol 179: 1950-1959.
39. Fishelson Z, Horstmann RD, Müller-Eberhard HJ, (1987) Regulation of the alternative pathway of complement by pH. J Immunol 138: 3392-3395.
40. Levitz SM, Dupont MP, Smail EH, (1994) Direct activity of human T lymphocytes and natural killer cells against Cryptococcus neoformans. Infect Immun 62: 194-202.
41. Serrano CV, Fraticelli A, Paniccia R, Teti A, Noble B, et al. (1996) pH dependence of neutrophil-endothelial cell adhesion and adhesion molecule expression. Am J Physiol 271: C962-970.
42. Stock C, Gassner B, Hauck CR, Arnold H, Mally S, et al. (2005) Migration of human melanoma cells depends on extracellular pH and Na+/H+ exchange. J Physiol 567: 225-238.
43. Paradise RK, Lauffenburger DA, Van Vliet KJ, (2011) Acidic extracellular pH promotes activation of integrin α(v)β(3). PLoS One 6: e15746.
44. Ghanouni P, Schambye H, Seifert R, Lee TW, Rasmussen SG, et al. (2000) The effect of pH on beta(2) adrenoceptor function. Evidence for protonation-dependent activation. J Biol Chem 275: 3121-3127.
45. Martínez D, Vermeulen M, Trevani A, Ceballos A, Sabatté J, et al. (2006) Extracellular acidosis induces neutrophil activation by a mechanism dependent on activation of phosphatidylinositol 3-kinase/Akt and ERK pathways. J Immunol 176: 1163-1171.
46. Xu L, Fukumura D, Jain RK, (2002) Acidic extracellular pH induces vascular endothelial growth factor (VEGF) in human glioblastoma cells via ERK1/2 MAPK signaling pathway: mechanism of low pH-induced VEGF. J Biol Chem 277: 11368-11374.
47. Ludwig MG, Vanek M, Guerini D, Gasser JA, Jones CE, et al. (2003) Proton-sensing G-protein-coupled receptors. Nature 425: 93-98.
48. Murakami N, Yokomizo T, Okuno T, Shimizu T, (2004) G2A is a proton-sensing G-protein-coupled receptor antagonized by lysophosphatidylcholine. J Biol Chem 279: 42484-42491.
49. Wang JQ, Kon J, Mogi C, Tobo M, Damirin A, et al. (2004) TDAG8 is a proton-sensing and psychosine-sensitive G-protein-coupled receptor. J Biol Chem 279: 45626-45633.
50. Maghazachi AA, Knudsen E, Jin Y, Jenstad M, Chaudhry FA, (2004) D-galactosyl-beta1-1′-sphingosine and D-glucosyl-beta1-1′-sphingosine induce human natural killer cell apoptosis. Biochem Biophys Res Commun 320: 810-815.
51. Alspaugh JA, Cavallo LM, Perfect JR, Heitman J, (2000) RAS1 regulates filamentation, mating and growth at high temperature of Cryptococcus neoformans. Mol Microbiol 36: 352-365.
52. Yamaguchi M, Ohkusu M, Biswas SK, Kawamoto S, (2007) Cytological study of cell cycle of the pathogenic yeast Cryptococcus neoformans. Nihon Ishinkin Gakkai Zasshi 48: 147-152.
53. Pasternak CA, Warmsley AM, Thomas DB, (1971) Structural alterations in the surface membrane during the cell cycle. J Cell Biol 50: 562-564.
54. Valeriote F, van Putten L, (1975) Proliferation-dependent cytotoxicity of anticancer agents: a review. Cancer Res 35: 2619-2630.
55. Leneva NV, Svet-Moldavsky GJ, (1974) Susceptibility of tumor cells in different phases of the mitotic cycle to the effect of immune lymphocytes. J Natl Cancer Inst 52: 699-704.
56. Lerner RA, Oldstone MB, Cooper NR, (1971) Cell cycle-dependent immune lysis of Moloney virus-transformed lymphocytes: presence of viral antigen, accessibility to antibody, and complement activation. Proc Natl Acad Sci U S A 68: 2584-2588.
57. Lanier LL, Warner NL, (1981) Cell cycle related heterogeneity of Ia antigen expression on a murine B lymphoma cell line:analysis by flow cytometry. J Immunol 126: 626-631.
58. Nolte-'t Hoen EN, Almeida CR, Cohen NR, Nedvetzki S, Yarwood H, et al. (2007) Increased surveillance of cells in mitosis by human NK cells suggests a novel strategy for limiting tumor growth and viral replication. Blood 109: 670-673.
59. Mody CH, Tyler CL, Sitrin RG, Jackson C, Toews GB, (1991) Interferon-gamma activates rat alveolar macrophages for anticryptococcal activity. Am J Respir Cell Mol Biol 5: 19-26.
60. Schmid I, Krall WJ, Uittenbogaart CH, Braun J, Giorgi JV, (1992) Dead cell discrimination with 7-amino-actinomycin D in combination with dual color immunofluorescence in single laser flow cytometry. Cytometry 13: 204-208.
61. Mollenhauer HH, Morre DJ, Rowe LD, (1990) Alteration of intracellular traYc by monensin; mechanism, specificity and relationship to toxicity. Biochim Biophys Acta 1031: 225-246.