Role of sphingosine-1-phosphate (S1P) and S1P receptor 2 in the phagocytosis of Cryptococcus neoformans by alveolar macrophages

Microbiology

Volumn 157, Issue 5, 2011, Pages 1416-1427

  McQuiston, Travis ^a   Luberto, Chiara ^a   del Poeta, Maurizio ^a,b  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD16 ANTIGEN; FC RECEPTOR; FC RECEPTOR I; FC RECEPTOR II; MESSENGER RNA; SPHINGOSINE 1 PHOSPHATE; SPHINGOSINE 1 PHOSPHATE RECEPTOR; SPHINGOSINE 1 PHOSPHATE RECEPTOR 2; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; CRYPTOCOCCUS NEOFORMANS; EXTRACELLULAR SPACE; HOST PATHOGEN INTERACTION; LUNG ALVEOLUS MACROPHAGE; MOUSE; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; WILD TYPE;

ANIMALS; CELLS, CULTURED; CRYPTOCOCCOSIS; CRYPTOCOCCUS NEOFORMANS; FEMALE; FUNGAL PROTEINS; HUMANS; LYSOPHOSPHOLIPIDS; MACROPHAGES, ALVEOLAR; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PHAGOCYTOSIS; RECEPTORS, IGG; RECEPTORS, LYSOSPHINGOLIPID; SPHINGOSINE;

FILOBASIDIELLA NEOFORMANS; FUNGI;

EID: 79955781310     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.045989-0     Document Type: Article

References (74)

1. Abadi, J. & Pirofski, L. (1999). Antibodies reactive with the cryptococcal capsular polysaccharide glucuronoxylomannan are present in sera from children with and without human immunodeficiency virus infection. J Infect Dis 180, 915-919.
2. Abe, K., Yoshinaga, M., Ishimatsu, Y., Iwashita, T., Matsubara, Y., Maesaki, S., Tomono, K., Kadota, J. & Kohno, S. (1998). [Cytokines produced by cells in bronchoalveolar lavage fluid from a patient with primary pulmonary cryptococcosis]. Nihon Kokyuki Gakkai Zasshi 36, 299-305 (in Japanese).
3. Allende, M. L., Sasaki, T., Kawai, H., Olivera, A., Mi, Y., van Echten-Deckert, G., Hajdu, R., Rosenbach, M., Keohane, C. A. & other authors (2004). Mice deficient in sphingosine kinase 1 are rendered lymphopenic by FTY720. J Biol Chem 279, 52487-52492.
4. Ammit, A. J., Hastie, A. T., Edsall, L. C., Hoffman, R. K., Amrani, Y., Krymskaya, V. P., Kane, S. A., Peters, S. P., Penn, R. B. & other authors (2001). Sphingosine 1-phosphate modulates human airway smooth muscle cell functions that promote inflammation and airway remodeling in asthma. FASEB J 15, 1212-1214.
5. Argraves, K. M., Gazzolo, P. J., Groh, E. M., Wilkerson, B. A., Matsuura, B. S., Twal, W. O., Hammad, S. M. & Argraves, W. S. (2008). High density lipoprotein-associated sphingosine 1-phosphate promotes endothelial barrier function. J Biol Chem 283, 25074-25081.
6. Bianco, C., Griffin, F. M., Jr & Silverstein, S. C. (1975). Studies of the macrophage complement receptor. Alteration of receptor function upon macrophage activation. J Exp Med 141, 1278-1290.
7. Buchanan, K. L. & Murphy, J. W. (1997). Kinetics of cellular infiltration and cytokine production during the efferent phase of a delayed-type hypersensitivity reaction. Immunology 90, 189-197.
8. Chiba, K. (2005). FTY720, a new class of immunomodulator, inhibits lymphocyte egress from secondary lymphoid tissues and thymus by agonistic activity at sphingosine 1-phosphate receptors. Pharmacol Ther 108, 308-319.
9. Chré tien, F., Lortholary, O., Kansau, I., Neuville, S., Gray, F. & Dromer, F. (2002). Pathogenesis of cerebral Cryptococcus neoformans infection after fungemia. J Infect Dis 186, 522-530.
10. Cox, G. M., McDade, H. C., Chen, S. C., Tucker, S. C., Gottfredsson, M., Wright, L. C., Sorrell, T. C., Leidich, S. D., Casadevall, A. & other authors (2001). Extracellular phospholipase activity is a virulence factor for Cryptococcus neoformans. Mol Microbiol 39, 166-175.
11. Cox, G. M., Harrison, T. S., McDade, H. C., Taborda, C. P., Heinrich, G., Casadevall, A. & Perfect, J. R. (2003). Superoxide dismutase influences the virulence of Cryptococcus neoformans by affecting growth within macrophages. Infect Immun 71, 173-180.
12. Daë ron, M. (1997). Structural bases of FcγR functions. Int Rev Immunol 16, 1-27.
13. - individuals. Clin Exp Immunol 99, 425-432.
14. Dromer, F., Perronne, C., Barge, J., Vilde, J. L. & Yeni, P. (1989). Role of IgG and complement component C5 in the initial course of experimental cryptococcosis. Clin Exp Immunol 78, 412-417.
15. Duong, C. Q., Bared, S. M., Abu-Khader, A., Buechler, C., Schmitz, A. & Schmitz, G. (2004). Expression of the lysophospholipid receptor family and investigation of lysophospholipid-mediated responses in human macrophages. Biochim Biophys Acta 1682, 112-119.
16. Edsall, L. C. & Spiegel, S. (1999). Enzymatic measurement of sphingosine 1-phosphate. Anal Biochem 272, 80-86.
17. Escá rcega-Barbosa, D., Ortiz-Jimé nez, M. P., Juárez-García, J. & Miranda-Feria, A. J. (2002). [Hyper-IgM syndrome: mucocutaneous lesions and neutropenia]. Rev Alerg Mex 49, 57-59 (in Spanish).
18. Feldmesser, M. & Casadevall, A. (1997). Effect of serum IgG1 to Cryptococcus neoformans glucuronoxylomannan on murine pulmonary infection. J Immunol 158, 790-799.
19. Feldmesser, M., Kress, Y., Novikoff, P. & Casadevall, A. (2000). Cryptococcus neoformans is a facultative intracellular pathogen in murine pulmonary infection. Infect Immun 68, 4225-4237.
20. Garg, S. K., Volpe, E., Palmieri, G., Mattei, M., Galati, D., Martino, A., Piccioni, M. S., Valente, E., Bonanno, E. & other authors (2004). Sphingosine 1-phosphate induces antimicrobial activity both in vitro and in vivo. J Infect Dis 189, 2129-2138.
21. Garg, S. K., Santucci, M. B., Panitti, M., Pucillo, L., Bocchino, M., Okajima, F., Bisen, P. S., Saltini, C. & Fraziano, M. (2006). Does sphingosine 1-phosphate play a protective role in the course of pulmonary tuberculosis? Clin Immunol 121, 260-264.
22. Goldman, D. L., Lee, S. C., Mednick, A. J., 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.
23. Greco, E., Santucci, M. B., Sali, M., De Angelis, F. R., Papi, M., De Spirito, M., Delogu, G., Colizzi, V. & Fraziano, M. (2010). Natural lysophospholipids reduce Mycobacterium tuberculosis-induced cytotoxicity and induce anti-mycobacterial activity by a phagolysosome maturation-dependent mechanism in A549 type II alveolar epithelial cells. Immunology 129, 125-132.
24. Hammad, S. M., Crellin, H. G., Wu, B. X., Melton, J., Anelli, V. & Obeid, L. M. (2008). Dual and distinct roles for sphingosine kinase 1 and sphingosine 1 phosphate in the response to inflammatory stimuli in RAW macrophages. Prostaglandins Other Lipid Mediat 85, 107-114.
25. Hla, T., Lee, M. J., Ancellin, N., Paik, J. H. & Kluk, M. J. (2001). Lysophospholipids-receptor revelations. Science 294, 1875-1878.
26. Hornuss, C., Hammermann, R., Fuhrmann, M., Juergens, U. R. & Racké, K. (2001). Human and rat alveolar macrophages express multiple EDG receptors. Eur J Pharmacol 429, 303-308.
27. Hughes, J. E., Srinivasan, S., Lynch, K. R., Proia, R. L., Ferdek, P. & Hedrick, C. C. (2008). Sphingosine-1-phosphate induces an antiinflammatory phenotype in macrophages. Circ Res 102, 950-958.
28. Ikeda, H., Satoh, H., Yanase, M., Inoue, Y., Tomiya, T., Arai, M., Tejima, K., Nagashima, K., Maekawa, H. & other authors (2003). Antiproliferative property of sphingosine 1-phosphate in rat hepatocytes involves activation of Rho via Edg-5. Gastroenterology 124, 459-469.
29. Jiang, L. I., Collins, J., Davis, R., Lin, K. M., DeCamp, D., Roach, T., Hsueh, R., Rebres, R. A., Ross, E. M. & other authors (2007). Use of a cAMP BRET sensor to characterize a novel regulation of cAMP by the sphingosine 1-phosphate/G13 pathway. J Biol Chem 282, 10576-10584.
30. Jo, E. K., Kim, H. S., Lee, M. Y., Iseki, M., Lee, J. H., Song, C. H., Park, J. K., Hwang, T. J. & Kook, H. (2002). X-linked hyper-IgM syndrome associated with Cryptosporidium parvum and Cryptococcus neoformans infections: the first case with molecular diagnosis in Korea. J Korean Med Sci 17, 116-120.
31. Jolly, P. S., Rosenfeldt, H. M., Milstien, S. & Spiegel, S. (2002). The roles of sphingosine-1-phosphate in asthma. Mol Immunol 38, 1239-1245.
32. Jolly, P. S., Bektas, M., Olivera, A., Gonzalez-Espinosa, C., Proia, R. L., Rivera, J., Milstien, S. & Spiegel, S. (2004). Transactivation of sphingosine-1-phosphate receptors by FceRI triggering is required for normal mast cell degranulation and chemotaxis. J Exp Med 199, 959-970.
33. Kechichian, T. B., Shea, J. & Del Poeta, M. (2007). Depletion of alveolar macrophages decreases the dissemination of a glucosylceramide- deficient mutant of Cryptococcus neoformans in immunodeficient mice. Infect Immun 75, 4792-4798.
34. Kono, M., Mi, Y., Liu, Y., Sasaki, T., Allende, M. L., Wu, Y. P., Yamashita, T. & Proia, R. L. (2004). The sphingosine-1-phosphate receptors S1P1, S1P2, and S1P3 function coordinately during embryonic angiogenesis. J Biol Chem 279, 29367-29373.
35. Kozel, T. R. & Pfrommer, G. S. (1986). Activation of the complement system by Cryptococcus neoformans leads to binding of iC3b to the yeast. Infect Immun 52, 1-5.
36. Kusner, D. J. (2005). Mechanisms of mycobacterial persistence in tuberculosis. Clin Immunol 114, 239-247.
37. Levitz, S. M. (2002). Receptor-mediated recognition of Cryptococcus neoformans. Nippon Ishinkin Gakkai Zasshi 43, 133-136.
38. Levitz, S. M., Tabuni, A., Kozel, T. R., MacGill, R. S., Ingalls, R. R. & Golenbock, D. T. (1997). Binding of Cryptococcus neoformans to heterologously expressed human complement receptors. Infect Immun 65, 931-935.
39. Levitz, S. M., Nong, S. H., Seetoo, K. F., Harrison, T. S., Speizer, R. A. & Simons, E. R. (1999). Cryptococcus neoformans resides in an acidic phagolysosome of human macrophages. Infect Immun 67, 885-890.
40. Luberto, C., Martinez-Mariñ o, B., Taraskiewicz, D., Bolañ os, B., Chitano, P., Toffaletti, D. L., Cox, G. M., Perfect, J. R., Hannun, Y. A. & other authors (2003). Identification of App1 as a regulator of phagocytosis and virulence of Cryptococcus neoformans. J Clin Invest 112, 1080-1094.
41. 2+ signaling by Mycobacterium tuberculosis is associated with reduced phagosome-lysosome fusion and increased survival within human macrophages. J Exp Med 191, 287-302.
42. McQuiston, T., Luberto, C. & Del Poeta, M. (2010). Role of host sphingosine kinase 1 in the lung response against cryptococcosis. Infect Immun 78, 2342-2352.
43. Monari, C., Bistoni, F., Casadevall, A., Pericolini, E., Pietrella, D., Kozel, T. R. & Vecchiarelli, A. (2005). Glucuronoxylomannan, a microbial compound, regulates expression of costimulatory molecules and production of cytokines in macrophages. J Infect Dis 191, 127-137.
44. Mukherjee, S., Lee, S., Mukherjee, J., Scharff, M. D. & Casadevall, A. (1994). Monoclonal antibodies to Cryptococcus neoformans capsular polysaccharide modify the course of intravenous infection in mice. Infect Immun 62, 1079-1088.
45. Mukherjee, S., Lee, S. C. & Casadevall, A. (1995). Antibodies to Cryptococcus neoformans glucuronoxylomannan enhance antifungal activity of murine macrophages. Infect Immun 63, 573-579.
46. Mukherjee, S., Feldmesser, M. & Casadevall, A. (1996). J774 murine macrophage-like cell interactions with Cryptococcus neoformans in the presence and absence of opsonins. J Infect Dis 173, 1222-1231.
47. Netski, D. & Kozel, T. R. (2002). Fc-dependent and Fc-independent opsonization of Cryptococcus neoformans by anticapsular monoclonal antibodies: importance of epitope specificity. Infect Immun 70, 2812-2819.
48. Nimmerjahn, F., Bruhns, P., Horiuchi, K. & Ravetch, J. V. (2005). FccγRIV: a novel FcR with distinct IgG subclass specificity. Immunity 23, 41-51.
49. Okamoto, H., Takuwa, N., Yokomizo, T., Sugimoto, N., Sakurada, S., Shigematsu, H. & Takuwa, Y. (2000). Inhibitory regulation of Rac activation, membrane ruffling, and cell migration by the G proteincoupled sphingosine-1-phosphate receptor EDG5 but not EDG1 or EDG3. Mol Cell Biol 20, 9247-9261.
50. Osada, M., Yatomi, Y., Ohmori, T., Ikeda, H. & Ozaki, Y. (2002). Enhancement of sphingosine 1-phosphate-induced migration of vascular endothelial cells and smooth muscle cells by an EDG-5 antagonist. Biochem Biophys Res Commun 299, 483-487.
51. Park, B. J., Wannemuehler, K. A., Marston, B. J., Govender, N., Pappas, P. G. & Chiller, T. M. (2009). Estimation of the current global burden of cryptococcal meningitis among persons living with HIV/ AIDS. AIDS 23, 525-530.
52. Ravetch, J. V. & Bolland, S. (2001). IgG Fc receptors. Annu Rev Immunol 19, 275-290.
53. Rittershaus, P. C., Kechichian, T. B., Allegood, J. C., Merrill, A. H., Jr, Hennig, M., Luberto, C. & Del Poeta, M. (2006). Glucosylceramide synthase is an essential regulator of pathogenicity of Cryptococcus neoformans. J Clin Invest 116, 1651-1659.
54. Rivera, J., Proia, R. L. & Olivera, A. (2008). The alliance of sphingosine-1-phosphate and its receptors in immunity. Nat Rev Immunol 8, 753-763.
55. Sali, M., Delogu, G., Greco, E., Rocca, S., Colizzi, V., Fadda, G. & Fraziano, M. (2009). Exploiting immunotherapy in Mycobacterium tuberculosis-infected mice: sphingosine 1-phosphate treatment results in a protective or detrimental effect depending on the stage of infection. Int J Immunopathol Pharmacol 22, 175-181.
56. Sanchez, T., Skoura, A., Wu, M. T., Casserly, B., Harrington, E. O. & Hla, T. (2007). Induction of vascular permeability by the sphingosine-1-phosphate receptor-2 (S1P2R) and its downstream effectors ROCK and PTEN. Arterioscler Thromb Vasc Biol 27, 1312-1318.
57. Santucci, M. B., Greco, E., De Spirito, M., Arcovito, G., De Angelis, G., Cauda, R. & Fraziano, M. (2007). Sphingosine 1-phosphate promotes antigen processing and presentation to CD4+ T cells in Mycobacterium tuberculosis-infected monocytes. Biochem Biophys Res Commun 361, 687-693.
58. Schwab, S. R., Pereira, J. P., Matloubian, M., Xu, Y., Huang, Y. & Cyster, J. G. (2005). Lymphocyte sequestration through S1P lyase inhibition and disruption of S1P gradients. Science 309, 1735-1739.
59. Shapiro, S., Beenhouwer, D. O., Feldmesser, M., Taborda, C., Carroll, M. C., Casadevall, A. & Scharff, M. D. (2002). Immunoglobulin G monoclonal antibodies to Cryptococcus neoformans protect mice deficient in complement component C3. Infect Immun 70, 2598-2604.
60. Shea, J. M., Kechichian, T. B., Luberto, C. & Del Poeta, M. (2006). The cryptococcal enzyme inositol phosphosphingolipid-phospholipase C confers resistance to the antifungal effects of macrophages and promotes fungal dissemination to the central nervous system. Infect Immun 74, 5977-5988.
61. Singer, I. I., Tian, M., Wickham, L. A., Lin, J., Matheravidathu, S. S., Forrest, M. J., Mandala, S. & Quackenbush, E. J. (2005). Sphingosine- 1-phosphate agonists increase macrophage homing, lymphocyte contacts, and endothelial junctional complex formation in murine lymph nodes. J Immunol 175, 7151-7161.
62. Snider, A. J., Kawamori, T., Bradshaw, S. G., Orr, K. A., Gilkeson, G. S., Hannun, Y. A. & Obeid, L. M. (2009). A role for sphingosine kinase 1 in dextran sulfate sodium-induced colitis. FASEB J 23, 143-152.
63. Taborda, C. P. & Casadevall, A. (2002). CR3 (CD11b/CD18) and CR4 (CD11c/CD18) are involved in complement-independent antibodymediated phagocytosis of Cryptococcus neoformans. Immunity 16, 791-802.
64. Thompson, C. R., Iyer, S. S., Melrose, N., VanOosten, R., Johnson, K., Pitson, S. M., Obeid, L. M. & Kusner, D. J. (2005). Sphingosine kinase 1 (SK1) is recruited to nascent phagosomes in human macrophages: inhibition of SK1 translocation by Mycobacterium tuberculosis. J Immunol 174, 3551-3561.
65. Vecchiarelli, A., Pietrella, D., Dottorini, M., Monari, C., Retini, C., Todisco, T. & Bistoni, F. (1994). Encapsulation of Cryptococcus neoformans regulates fungicidal activity and the antigen presentation process in human alveolar macrophages. Clin Exp Immunol 98, 217-223.
66. Voelz, K., Lammas, D. A. & May, R. C. (2009). Cytokine signaling regulates the outcome of intracellular macrophage parasitism by Cryptococcus neoformans. Infect Immun 77, 3450-3457.
67. Vora, K. A., Nichols, E., Porter, G., Cui, Y., Keohane, C. A., Hajdu, R., Hale, J., Neway, W., Zaller, D. & Mandala, S. (2005). Sphingosine 1-phosphate receptor agonist FTY720-phosphate causes marginal zone B cell displacement. J Leukoc Biol 78, 471-480.
68. Weigert, A., Weis, N. & Brü ne, B. (2009). Regulation of macrophage function by sphingosine-1-phosphate. Immunobiology 214, 748-760.
69. Wright, L. C., Santangelo, R. M., Ganendren, R., Payne, J., Djordjevic, J. T. & Sorrell, T. C. (2007). Cryptococcal lipid metabolism: phospholipase B1 is implicated in transcellular metabolism of macrophage-derived lipids. Eukaryot Cell 6, 37-47.
70. Xing, D., Hage, F. G., Chen, Y. F., McCrory, M. A., Feng, W., Skibinski, G. A., Majid-Hassan, E., Oparil, S. & Szalai, A. J. (2008). Exaggerated neointima formation in human C-reactive protein transgenic mice is IgG Fc receptor type I (FccRI)-dependent. Am J Pathol 172, 22-30.
71. Yatomi, Y., Igarashi, Y., Yang, L., Hisano, N., Qi, R., Asazuma, N., Satoh, K., Ozaki, Y. & Kume, S. (1997). Sphingosine 1-phosphate, a bioactive sphingolipid abundantly stored in platelets, is a normal constituent of human plasma and serum. J Biochem 121, 969-973.
72. Yauch, L. E., Mansour, M. K. & Levitz, S. M. (2005). Receptormediated clearance of Cryptococcus neoformans capsular polysaccharide in vivo. Infect Immun 73, 8429-8432.
73. Yokoo, E., Yatomi, Y., Takafuta, T., Osada, M., Okamoto, Y. & Ozaki, Y. (2004). Sphingosine 1-phosphate inhibits migration of RBL-2H3 cells via S1P2: cross-talk between platelets and mast cells. J Biochem 135, 673-681.
74. Zaragoza, O., Chrisman, C. J., Castelli, M. V., Frases, S., Cuenca- Estrella, M., Rodríguez-Tudela, J. L. & Casadevall, A. (2008). Capsule enlargement in Cryptococcus neoformans confers resistance to oxidative stress suggesting a mechanism for intracellular survival. Cell Microbiol 10, 2043-2057.