Identification of the fungal ligand triggering cytotoxic PRR-mediated NK cell killing of Cryptococcus and Candida

Nature Communications

Volumn 9, Issue 1, 2018, Pages

  Li, Shu Shun ^a   Ogbomo, Henry ^a   Mansour, Michael K ^b   Xiang, Richard F ^a   Szabo, Lian ^c   Munro, Fay ^a   Mukherjee, Priyanka ^a   Mariuzza, Roy A ^d   Amrein, Matthias ^a   Vyas, Jatin M ^b   Robbins, Stephen M ^a,c   Mody, Christopher H ^a,c  

^a UNIVERSITY OF CALGARY   (Canada)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c UNIVERSITY OF CALGARY   (Canada)

^d University of Maryland   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA 1,3 GLUCAN; CASPOFUNGIN; CURDLAN; DASATINIB; DIMETHYL SULFOXIDE; IMMUNOGLOBULIN G; LAMINARAN; LAMINARIHEXAOSE; MANNAN; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY 1C01; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 3; PERFORIN; POLYSACCHARIDE; POLYSTYRENE; PROTEIN TYROSINE KINASE; PUSTULAN; SML 0425; UNCLASSIFIED DRUG; BETA GLUCAN; BETA-1,3-GLUCAN; LIGAND; NCR3 PROTEIN, HUMAN; PATHOGEN ASSOCIATED MOLECULAR PATTERN; RECOMBINANT PROTEIN;

ANTIBODY DETECTION; ANTIFUNGAL ACTIVITY; ARTICLE; ATOMIC FORCE MICROSCOPY; BINDING AFFINITY; CANDIDA ALBICANS; CELL GRANULE; CELL INTERACTION; CELL KILLING; CELL POLARITY; CELLULAR IMMUNITY; CONTROLLED STUDY; CONVERGENT EVOLUTION; CRYPTOCOCCUS NEOFORMANS; CYTOTOXICITY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; FUNGAL CELL WALL; FUNGUS IMMUNITY; HOST RESISTANCE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS INFECTED PATIENT; IMMUNOLOGICAL SYNAPSE; K-562 CELL LINE; LIVE CELL IMAGING; NATURAL KILLER CELL; NONHUMAN; NORMAL HUMAN; ORGANISMAL INTERACTION; PROTEIN CARBOHYDRATE INTERACTION; PROTEIN EXPRESSION; PROTEIN SECRETION; SIGNAL TRANSDUCTION; SINGLE CELL ANALYSIS; TOTAL INTERNAL REFLECTION FLUORESCENCE MICROSCOPY; YT CELL LINE; CELL LINE; HOST PATHOGEN INTERACTION; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOLOGY; SOLUBILITY;

CANDIDA; CANDIDA ALBICANS; FILOBASIDIELLA NEOFORMANS; FUNGI;

BETA-GLUCANS; CANDIDA ALBICANS; CELL LINE; CELL POLARITY; CRYPTOCOCCUS NEOFORMANS; CYTOPLASMIC GRANULES; CYTOTOXICITY, IMMUNOLOGIC; HIV INFECTIONS; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNOLOGICAL SYNAPSES; KILLER CELLS, NATURAL; LIGANDS; MICROSCOPY, ATOMIC FORCE; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 3; PATHOGEN-ASSOCIATED MOLECULAR PATTERN MOLECULES; PERFORIN; RECOMBINANT PROTEINS; SOLUBILITY;

EID: 85042366997     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/s41467-018-03014-4     Document Type: Article

References (64)

1. Vallabhaneni, S., Mody, R. K., Walker, T. & Chiller, T. The global burden of fungal diseases. Infect. Dis. Clin. North. Am. 30, 1-11 (2016).
2. Enoch, D. A., Yang, H., Aliyu, S. H. & Micallef, C. The changing epidemiology of invasive fungal infections. Methods Mol. Biol. 1508, 17-65 (2017).
3. Kullberg, B. J. & Arendrup, M. C. Invasive Candidiasis. N. Engl. J. Med. 373, 1445-1456 (2015).
4. Jarvis, J. N. et al. Determinants of mortality in a combined cohort of 501 patients with HIV-Associated Cryptococcal meningitis: implications for improving outcomes. Clin. Infect. Dis. 58, 736-745 (2014).
5. Hidore, M. R., Mislan, T. W. & Murphy, J. W. Responses of murine natural killer cells to binding of the fungal target Cryptococcus neoformans. Infect. Immun. 59, 1489-1499 (1991).
6. Hidore, M. R. & Murphy, J. W. Natural cellular resistance of beige mice against Cryptococcus neoformans. J. Immunol. 137, 3624-3631 (1986).
7. Hidore, M. R. & Murphy, J. W. 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 (1986).
8. Hidore, M. R. & Murphy, J. W. Murine natural killer cell interactions with a fungal target, Cryptococcus neoformans. Infect. Immun. 57, 1990-1997 (1989).
9. Hidore, M. R., Nabavi, N., Sonleitner, F. & Murphy, J. W. Murine natural killer cells are fungicidal to Cryptococcus neoformans. Infect. Immun. 59, 1747-1754 (1991).
10. Murphy, J. W., Hidore, M. R. & Wong, S. C. Direct interactions of human lymphocytes with the yeast-like organism, Cryptococcus neoformans. J. Clin. Invest. 91, 1553-1566 (1993).
11. Levitz, S. M., Dupont, M. P. & Smail, E. H. Direct activity of human T lymphocytes and natural killer cells against Cryptococcus neoformans. Infect. Immun. 62, 194-202 (1994).
12. Gonzalez-Amaro, R. et al. Natural killer cell-mediated cytotoxicity in cryptococcal meningitis. Rev. Invest. Clin. 43, 133-138 (1991).
13. Horn, C. A. & Washburn, R. G. Anticryptococcal activity of NK cell-enriched peripheral blood lymphocytes from human immunodeficiency virus-infected subjects: responses to interleukin-2, interferon-gamma, and interleukin-12. J. Infect. Dis. 172, 1023-1027 (1995).
14. Islam, A. et al. An acidic microenvironment increases NK cell killing of Cryptococcus neoformans and Cryptococcus gattii by enhancing perforin degranulation. PLoS Pathog. 9, e1003439 (2013).
15. Li, S. S. et al. The NK receptor NKp30 mediates direct fungal recognition and killing and is diminished in NK cells from HIV-infected patients. Cell Host Microbe 14, 387-397 (2013).
16. Brown, G. D. Dectin-1: A signalling non-TLR pattern-recognition receptor. Nat. Rev. Immunol. 6, 33-43 (2006).
17. Elomaa, O. et al. Cloning of a novel bacteria-binding receptor structurally related to scavenger receptors and expressed in a subset of macrophages. Cell 80, 603-609 (1995).
18. Bowdish, D. M. & Gordon, S. Conserved domains of the class A scavenger receptors: evolution and function. Immunol. Rev. 227, 19-31 (2009).
19. Ezekowitz, R. A., Sastry, K., Bailly, P. & Warner, A. Molecular characterization of the human macrophage mannose receptor: demonstration of multiple carbohydrate recognition-like domains and phagocytosis of yeasts in Cos-1 cells. J. Exp. Med. 172, 1785-1794 (1990).
20. Kawai, T. & Akira, S. The roles of TLRs, RLRs and NLRs in pathogen recognition. Int. Immunol. 21, 317-337 (2009).
21. Vitenshtein, A. et al. NK cell recognition of candida glabrata through binding of NKp46 and NCR1 to fungal ligands Epa1, Epa6, and Epa7. Cell Host Microbe 20, 527-534 (2016).
22. Brueggemann, S., Schmitt, A. L., Einsele, H., Loeffler, J. Characterization of human natural killer cell receptors recognizing Aspergillus fumigatus. In 6th Advances Against Aspergillosis Madrid, Spain (2014).
23. Mavoungou, E., Held, J., Mewono, L. & Kremsner, P. G. A Duffy binding-like domain is involved in the NKp30-mediated recognition of Plasmodium falciparum-parasitized erythrocytes by natural killer cells. J. Infect. Dis. 195, 1521-1531 (2007).
24. Janeway, C. A. Jr. Approaching the asymptote? Evolution and revolution in immunology. Cold Spring Harb. Symp. Quant. Biol. 54(Pt 1), 1-13 (1989).
25. McFadden, D., Zaragoza, O. & Casadevall, A. The capsular dynamics of Cryptococcus neoformans. Trends Microbiol. 14, 497-505 (2006).
26. de Souza Pereira, R. & Geibel, J. Direct observation of oxidative stress on the cell wall of Saccharomyces cerevisiae strains with atomic force microscopy. Mol. Cell. Biochem. 201, 17-24 (1999).
27. Nimrichter, L., Rodrigues, M. L., Rodrigues, E. G. & Travassos, L. R. The multitude of targets for the immune system and drug therapy in the fungal cell wall. Microbes Infect. 7, 789-798 (2005).
28. Sipiczki, M. Where does fission yeast sit on the tree of life? Genome Biol. 1, REVIEWS1011 (2000).
29. Klutts, J. S., Yoneda, A., Reilly, M. C., Bose, I. & Doering, T. L. Glycosyltransferases and their products: cryptococcal variations on fungal themes. FEMS Yeast Res. 6, 499-512 (2006).
30. Free, S. J. Fungal cell wall organization and biosynthesis. Adv. Genet. 81, 33-82 (2013).
31. Mody, C. H. et al. Proteins in the cell wall and membrane of Cryptococcus neoformans stimulate lymphocytes from both adults and fetal cord blood to proliferate. Infect. Immun. 64, 4811-4819 (1996).
32. Nisizawa, K., Yamaguchi, T., Handa, N., Maeda, M. & Yamazaki, H. Chemical nature of a uronic acid-containing polysaccharide in the peritrophic membrane of the silkworm. J. Biochem. 54, 419-426 (1963).
33. Tam, J. M., Mansour, M. K., Khan, N. S., Yoder, N. C. & Vyas, J. M. Use of fungal derived polysaccharide-conjugated particles to probe dectin-1 responses in innate immunity. Integr. Biol. 4, 220-227 (2012).
34. Deresinski, S. C. & Stevens, D. A. Caspofungin. Clin. Infect. Dis. 36, 1445-1457 (2003).
35. Maligie, M. A. & Selitrennikoff, C. P. Cryptococcus neoformans resistance to echinocandins: (1,3)beta-glucan synthase activity is sensitive to echinocandins. Antimicrob. Agents Chemother. 49, 2851-2856 (2005).
36. Kyei, S. K., et al. Mechanisms by which Interleukin-12 corrects defective NK cell anticryptococcal activity in HIV-infected patients. MBio 7, e00878-16 (2016).
37. Whited, A. M. & Park, P. S. Atomic force microscopy: A multifaceted tool to study membrane proteins and their interactions with ligands. Biochim. Biophys. Acta 1838, 56-68 (2014).
38. Zhang, X., Wojcikiewicz, E. & Moy, V. T. Force spectroscopy of the leukocyte function-Associated antigen-1/intercellular adhesion molecule-1 interaction. Biophys. J. 83, 2270-2279 (2002).
39. Zhang, X., Wojcikiewicz, E. P. & Moy, V. T. Dynamic adhesion of T lymphocytes to endothelial cells revealed by atomic force microscopy. Exp. Biol. Med. 231, 1306-1312 (2006).
40. Tsoni, S. V. & Brown, G. D. beta-Glucans and dectin-1. Ann. NY Acad. Sci. 1143, 45-60 (2008).
41. Marr, K. J. et al. Cryptococcus neoformans directly stimulates perforin production and rearms NK cells for enhanced anticryptococcal microbicidal activity. Infect. Immun. 77, 2436-2446 (2009).
42. Oykhman, P. et al. Requirement and redundancy of the Src family kinases Fyn and Lyn in perforin-dependent killing of Cryptococcus neoformans by NK cells. Infect. Immun. 81, 3912-3922 (2013).
43. Gratacap, M. P. et al. The new tyrosine-kinase inhibitor and anticancer drug dasatinib reversibly affects platelet activation in vitro and in vivo. Blood 114, 1884-1892 (2009).
44. Di Luzio, N. R. & Williams, D. L. Protective effect of glucan against systemic Staphylococcus aureus septicemia in normal and leukemic mice. Infect. Immun. 20, 804-810 (1978).
45. Reynolds, J. A. et al. Glucan-induced enhancement of host resistance to selected infectious diseases. Infect. Immun. 30, 51-57 (1980).
46. Song, M. & di Luzio, N. R. Yeast glucan and immunotherapy of infectious diseases. Front. Biol. 48, 533-547 (1979).
47. Williams, D. L. & Di Luzio, N. R. Glucan-induced modification of murine viral hepatitis. Science 208, 67-69 (1980).
48. Williams, D. L., Cook, J. A., Hoffmann, E. O. & Di Luzio, N. R. Protective effect of glucan in experimentally induced candidiasis. J. Reticuloendothel. Soc. 23, 479-490 (1978).
49. Cook, J. A., Holbrook, T. W. & Parker, B. W. Visceral leishmaniasis in mice: protective effect of glucan. J. Reticuloendothel. Soc. 27, 567-573 (1980).
50. Babineau, T. J. et al. Randomized phase I/II trial of a macrophage-specific immunomodulator (PGG-glucan) in high-risk surgical patients. Ann. Surg. 220, 601-609 (1994).
51. Babineau, T. J. et al. A phase II multicenter, double-blind, randomized, placebo-controlled study of three dosages of an immunomodulator (PGG-glucan) in high-risk surgical patients. Arch. Surg. 129, 1204-1210 (1994).
52. Dellinger, E. P. et al. Effect of PGG-glucan on the rate of serious postoperative infection or death observed after high-risk gastrointestinal operations. Betafectin Gastrointestinal Study Group. Arch. Surg. 134, 977-983 (1999).
53. Willment, J. A. et al. The human beta-glucan receptor is widely expressed and functionally equivalent to murine Dectin-1 on primary cells. Eur. J. Immunol. 35, 1539-1547 (2005).
54. Taylor, P. R. et al. The beta-glucan receptor, dectin-1, is predominantly expressed on the surface of cells of the monocyte/macrophage and neutrophil lineages. J. Immunol. 169, 3876-3882 (2002).
55. Di Renzo, L., Yefenof, E. & Klein, E. The function of human NK cells is enhanced by beta-glucan, a ligand of CR3 (CD11b/CD18). Eur. J. Immunol. 21, 1755-1758 (1991).
56. Jones, G. J. et al. In contrast to anti-Tumor activity, YT cell and primary NK cell cytotoxicity for Cryptococcus neoformans bypasses LFA-1. Int. Immunol. 21, 423-432 (2009).
57. Ostrosky-Zeichner, L. et al. Multicenter clinical evaluation of the (1->3) beta-D-glucan assay as an aid to diagnosis of fungal infections in humans. Clin. Infect. Dis. 41, 654-659 (2005).
58. Miyazaki, T. et al. Plasma (1->3)-beta-D-glucan and fungal antigenemia in patients with candidemia, aspergillosis, and cryptococcosis. J. Clin. Microbiol. 33, 3115-3118 (1995).
59. Denning, D. W. Echinocandin antifungal drugs. Lancet 362, 1142-1151 (2003).
60. Krensky, A. M. & Clayberger, C. Biology and clinical relevance of granulysin. Tissue Antigens 73, 193-198 (2009).
61. Li, Y., Wang, Q. & Mariuzza, R. A. Structure of the human activating natural cytotoxicity receptor NKp30 bound to its tumor cell ligand B7-H6. J. Exp. Med. 208, 703-714 (2011).
62. Team RDC. R: A Language and Environment for Statistical Computing (The R Foundation for Statistical Computing, Vienna, 2011).
63. RStudio. RStudio: Integrated Development Environment for R (Version 0.98, 1091) (RStudio, Inc, Boston, 2012).
64. Pau, G., Fuchs, F., Sklyar, O., Boutros, M. & Huber, W. EBImage-an R package for image processing with applications to cellular phenotypes. Bioinformatics 26, 979-981 (2010).