A sensitive high-throughput assay for evaluating host-pathogen interactions in Cryptococcus neoformans infection

PLoS ONE

Volumn 6, Issue 7, 2011, Pages

  Srikanta, Deepa ^a   Yang, Meng ^a   Williams, Matthew ^a   Doering, Tamara L ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LUCIFER YELLOW; DIAGNOSTIC AGENT; ISOQUINOLINE DERIVATIVE;

ANALYTIC METHOD; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY LABELING; ARTICLE; CELL INTERACTION; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; CRYPTOCOCCOSIS; CRYPTOCOCCUS NEOFORMANS; FUNGAL VIRULENCE; HIGH THROUGHPUT SCREENING; HOST CELL; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; IMAGE ANALYSIS; IN VITRO STUDY; MICROSCOPY; MOUSE; NONHUMAN; PATHOGENESIS; PHAGOCYTE; SENSITIVITY ANALYSIS; VALIDATION PROCESS; ANIMAL; AUTOMATION; C57BL MOUSE; CELL ADHESION; CELL CULTURE; FEMALE; IMMUNOLOGY; MACROPHAGE; MICROBIOLOGY; MONOCYTE; PATHOGENICITY; PATHOLOGY; PHAGOCYTOSIS; PHYSIOLOGY; VIRULENCE;

FILOBASIDIELLA NEOFORMANS; FUNGI; MAMMALIA;

ANIMALS; AUTOMATION; CELL ADHESION; CELLS, CULTURED; CRYPTOCOCCOSIS; CRYPTOCOCCUS NEOFORMANS; FEMALE; HIGH-THROUGHPUT SCREENING ASSAYS; HOST-PATHOGEN INTERACTIONS; HUMANS; ISOQUINOLINES; MACROPHAGES; MICE; MICE, INBRED C57BL; MONOCYTES; PHAGOCYTES; PHAGOCYTOSIS; VIRULENCE;

EID: 79960863043     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0022773     Document Type: Article

References (63)

1. Chayakulkeeree M, Perfect JR, (2006) Cryptococcosis. Infect Dis Clin North Am 20: 507-544, v-vi.
2. Park BJ, Wannemuehler KA, Marston BJ, Govender N, Pappas PG, et al. (2009) Estimation of the current global burden of cryptococcal meningitis among persons living with HIV/AIDS. AIDS 23: 525-530.
3. Doering TL, (2009) How sweet it is! Cell wall biogenesis and polysaccharide capsule formation in Cryptococcus neoformans. Annu Rev Microbiol 63: 223-247.
4. Eisenman HC, Casadevall A, McClelland EE, (2007) New insights on the pathogenesis of invasive Cryptococcus neoformans infection. Curr Infect Dis Rep 9: 457-464.
5. Bulmer GS, Sans MD, (1967) Cryptococcus neoformans. II. Phagocytosis by human leukocytes. J Bacteriol 94: 1480-1483.
6. Diamond RD, Bennett JE, (1973) Growth of Cryptococcus neoformans within human macrophages in vitro. Infect Immun 7: 231-236.
7. Levitz SM, Nong SH, Seetoo KF, Harrison TS, Speizer RA, et al. (1999) Cryptococcus neoformans resides in an acidic phagolysosome of human macrophages. Infect Immun 67: 885-890.
8. Tucker SC, Casadevall A, (2002) Replication of Cryptococcus neoformans in macrophages is accompanied by phagosomal permeabilization and accumulation of vesicles containing polysaccharide in the cytoplasm. Proc Natl Acad Sci U S A 99: 3165-3170.
9. Garcia-Hermoso D, Janbon G, Dromer F, (1999) Epidemiological evidence for dormant Cryptococcus neoformans infection. J Clin Microbiol 37: 3204-3209.
10. Ma H, Croudace JE, Lammas DA, May RC, (2006) Expulsion of live pathogenic yeast by macrophages. Curr Biol 16: 2156-2160.
11. Alvarez M, Casadevall A, (2006) Phagosome extrusion and host-cell survival after Cryptococcus neoformans phagocytosis by macrophages. Curr Biol 16: 2161-2165.
12. Ma H, Croudace JE, Lammas DA, May RC, (2007) Direct cell-to-cell spread of a pathogenic yeast. BMC Immunol 8: 15.
13. Alvarez M, Casadevall A, (2007) Cell-to-cell spread and massive vacuole formation after Cryptococcus neoformans infection of murine macrophages. BMC Immunol 8: 16.
14. Goldman DL, Lee SC, Mednick AJ, Montella L, Casadevall A, (2000) Persistent Cryptococcus neoformans pulmonary infection in the rat is associated with intracellular parasitism, decreased inducible nitric oxide synthase expression, and altered antibody responsiveness to cryptococcal polysaccharide. Infect Immun 68: 832-838.
15. Del Poeta M, (2004) Role of phagocytosis in the virulence of Cryptococcus neoformans. Eukaryot Cell 3: 1067-1075.
16. Voelz K, Lammas DA, May RC, (2009) Cytokine signaling regulates the outcome of intracellular macrophage parasitism by Cryptococcus neoformans. Infect Immun 77: 3450-3457.
17. Alvarez M, Burn T, Luo Y, Pirofski LA, Casadevall A, (2009) The outcome of Cryptococcus neoformans intracellular pathogenesis in human monocytes. BMC Microbiol 9: 51.
18. Oliveira DL, Freire-de-Lima CG, Nosanchuk JD, Casadevall A, Rodrigues ML, et al. (2010) Extracellular vesicles from Cryptococcus neoformans modulate macrophage functions. Infect Immun 78: 1601-1609.
19. Cummings CA, Relman DA, (2000) Using DNA microarrays to study host-microbe interactions. Emerg Infect Dis 6: 513-525.
20. Mylonakis E, Ausubel FM, Perfect JR, Heitman J, Calderwood SB, (2002) Killing of Caenorhabditis elegans by Cryptococcus neoformans as a model of yeast pathogenesis. Proc Natl Acad Sci U S A 99: 15675-15680.
21. Kurz CL, Ewbank JJ, (2000) Caenorhabditis elegans for the study of host-pathogen interactions. Trends Microbiol 8: 142-144.
22. Fan W, Kraus PR, Boily MJ, Heitman J, (2005) Cryptococcus neoformans gene expression during murine macrophage infection. Eukaryot Cell 4: 1420-1433.
23. Walenkamp AM, Scharringa J, Schramel FM, Coenjaerts FE, Hoepelman IM, (2000) Quantitative analysis of phagocytosis of Cryptococcus neoformans by adherent phagocytic cells by fluorescence multi-well plate reader. J Microbiol Methods 40: 39-45.
24. Chaka W, Scharringa J, Verheul AF, Verhoef J, Van Strijp AG, et al. (1995) Quantitative analysis of phagocytosis and killing of Cryptococcus neoformans by human peripheral blood mononuclear cells by flow cytometry. Clin Diagn Lab Immunol 2: 753-759.
25. Voelz K, Johnston SA, Rutherford JC, May RC, (2010) Automated analysis of cryptococcal macrophage parasitism using GFP-tagged cryptococci. PLoS One 5: e15968.
26. Falkow S, Small P, Isberg R, Hayes SF, Corwin D, (1987) A molecular strategy for the study of bacterial invasion. Rev Infect Dis 9 (Suppl 5): S450-455.
27. Zhang H, Gomez-Garcia MR, Brown MR, Kornberg A, (2005) Inorganic polyphosphate in Dictyostelium discoideum: influence on development, sporulation, and predation. Proc Natl Acad Sci U S A 102: 2731-2735.
28. Elsinghorst EA, (1994) Measurement of invasion by gentamicin resistance. Methods Enzymol 236: 405-420.
29. Darfeuille-Michaud A, Boudeau J, Bulois P, Neut C, Glasser AL, et al. (2004) High prevalence of adherent-invasive Escherichia coli associated with ileal mucosa in Crohn's disease. Gastroenterology 127: 412-421.
30. Boleti H, Ojcius DM, Dautry-Varsat A, (2000) Fluorescent labelling of intracellular bacteria in living host cells. J Microbiol Methods 40: 265-274.
31. Sveum RJ, Chused TM, Frank MM, Brown EJ, (1986) A quantitative fluorescent method for measurement of bacterial adherence and phagocytosis. J Immunol Methods 90: 257-264.
32. Dromer F, Ronin O, Dupont B, (1992) Isolation of Cryptococcus neoformans var. gattii from an Asian patient in France: evidence for dormant infection in healthy subjects. J Med Vet Mycol 30: 395-397.
33. Singh N, Dromer F, Perfect JR, Lortholary O, (2008) Cryptococcosis in solid organ transplant recipients: current state of the science. Clin Infect Dis 47: 1321-1327.
34. Bartlett KH, Kidd SE, Kronstad JW, (2008) The emergence of Cryptococcus gattii in British Columbia and the Pacific Northwest. Curr Infect Dis Rep 10: 58-65.
35. Byrnes EJ 3rd, Li W, Lewit Y, Ma H, Voelz K, et al. (2010) Emergence and pathogenicity of highly virulent Cryptococcus gattii genotypes in the northwest United States. PLoS Pathog 6: e1000850.
36. Ma H, Hagen F, Stekel DJ, Johnston SA, Sionov E, et al. (2009) The fatal fungal outbreak on Vancouver Island is characterized by enhanced intracellular parasitism driven by mitochondrial regulation. Proc Natl Acad Sci U S A 106: 12980-12985.
37. Feldmesser M, Rivera J, Kress Y, Kozel TR, Casadevall A, (2000) Antibody interactions with the capsule of Cryptococcus neoformans. Infect Immun 68: 3642-3650.
38. Kozel TR, (1996) Activation of the complement system by pathogenic fungi. Clin Microbiol Rev 9: 34-46.
39. Kwon-Chung KJ, Kozel TR, Edman JC, Polacheck I, Ellis D, et al. (1992) Recent advances in biology and immunology of Cryptococcus neoformans. J Med Vet Mycol 30 (Suppl 1): 133-142.
40. Carruthers VB, Giddings OK, Sibley LD, (1999) Secretion of micronemal proteins is associated with toxoplasma invasion of host cells. Cell Microbiol 1: 225-235.
41. MacGill TC, MacGill RS, Casadevall A, Kozel TR, (2000) Biological correlates of capsular (quellung) reactions of Cryptococcus neoformans. J Immunol 164: 4835-4842.
42. Tsuchiya S, Yamabe M, Yamaguchi Y, Kobayashi Y, Konno T, et al. (1980) Establishment and characterization of a human acute monocytic leukemia cell line (THP-1). Int J Cancer 26: 171-176.
43. Auwerx J, (1991) The human leukemia cell line, THP-1: a multifacetted model for the study of monocyte-macrophage differentiation. Experientia 47: 22-31.
44. Cossart P, Bierne H, (2001) The use of host cell machinery in the pathogenesis of Listeria monocytogenes. Curr Opin Immunol 13: 96-103.
45. Rogers PD, Thornton J, Barker KS, McDaniel DO, Sacks GS, et al. (2003) Pneumolysin-dependent and-independent gene expression identified by cDNA microarray analysis of THP-1 human mononuclear cells stimulated by Streptococcus pneumoniae. Infect Immun 71: 2087-2094.
46. Kohler S, Foulongne V, Ouahrani-Bettache S, Bourg G, Teyssier J, et al. (2002) The analysis of the intramacrophagic virulome of Brucella suis deciphers the environment encountered by the pathogen inside the macrophage host cell. Proc Natl Acad Sci U S A 99: 15711-15716.
47. Hickman-Davis JM, Fang FC, Nathan C, Shepherd VL, Voelker DR, et al. (2001) Lung surfactant and reactive oxygen-nitrogen species: antimicrobial activity and host-pathogen interactions. Am J Physiol Lung Cell Mol Physiol 281: L517-523.
48. Ralph P, Nakoinz I, (1977) Antibody-dependent killing of erythrocyte and tumor targets by macrophage-related cell lines: enhancement by PPD and LPS. J Immunol 119: 950-954.
49. Nilsson K, Sundstrom C, (1974) Establishment and characteristics of two unique cell lines from patients with lymphosarcoma. Int J Cancer 13: 808-823.
50. Kozel TR, Wilson MA, Murphy JW, (1991) Early events in initiation of alternative complement pathway activation by the capsule of Cryptococcus neoformans. Infect Immun 59: 3101-3110.
51. Diamond RD, May JE, Kane MA, Frank MM, Bennett JE, (1974) The role of the classical and alternate complement pathways in host defenses against Cryptococcus neoformans infection. J Immunol 112: 2260-2270.
52. Griffin FM Jr, (1981) Roles of macrophage Fc and C3b receptors in phagocytosis of immunologically coated Cryptococcus neoformans. Proc Natl Acad Sci U S A 78: 3853-3857.
53. Janbon G, Doering TL, (2011) Biosynthesis and genetics of the Cryptococcal capsule. In: Heitman J, Kozel TR, Kwon-Chung KJ, Perfect JR, Casadevall A, editors. Cryptococcus: From human pathogen to model yeast Washington D.C. ASM Press pp. 27-42.
54. Bose I, Reese AJ, Ory JJ, Janbon G, Doering TL, (2003) A yeast under cover: the capsule of Cryptococcus neoformans. Eukaryot Cell 2: 655-663.
55. Kozel TR, Gotschlich EC, (1982) The capsule of cryptococcus neoformans passively inhibits phagocytosis of the yeast by macrophages. J Immunol 129: 1675-1680.
56. Kozel TR, Pfrommer GS, Guerlain AS, Highison BA, Highison GJ, (1988) Role of the capsule in phagocytosis of Cryptococcus neoformans. Rev Infect Dis 10 (Suppl 2): S436-439.
57. Zhang JH, Chung TD, Oldenburg KR, (1999) A Simple Statistical Parameter for Use in Evaluation and Validation of High Throughput Screening Assays. J Biomol Screen 4: 67-73.
58. Zhang XD, (2007) A new method with flexible and balanced control of false negatives and false positives for hit selection in RNA interference high-throughput screening assays. J Biomol Screen 12: 645-655.
59. Zhang XD, Ferrer M, Espeseth AS, Marine SD, Stec EM, et al. (2007) The use of strictly standardized mean difference for hit selection in primary RNA interference high-throughput screening experiments. J Biomol Screen 12: 497-509.
60. Birmingham A, Selfors LM, Forster T, Wrobel D, Kennedy CJ, et al. (2009) Statistical methods for analysis of high-throughput RNA interference screens. Nat Methods 6: 569-575.
61. Kozel TR, Follette JL, (1981) Opsonization of encapsulated Cryptococcus neoformans by specific anticapsular antibody. Infect Immun 31: 978-984.
62. Pierini LM, Doering TL, (2001) Spatial and temporal sequence of capsule construction in Cryptococcus neoformans. Mol Microbiol 41: 105-115.
63. Daigneault M, Preston JA, Marriott HM, Whyte MK, Dockrell DH, (2010) The identification of markers of macrophage differentiation in PMA-stimulated THP-1 cells and monocyte-derived macrophages. PLoS One 5: e8668.