Mathematical modeling of pathogenicity of Cryptococcus neoformans

Molecular Systems Biology

Volumn 4, Issue , 2008, Pages

  Garcia, Jacqueline ^a   Shea, John ^a   Alvarez Vasquez, Fernando ^a,b   Qureshi, Asfia ^a   Luberto, Chiara ^a   Voit, Eberhard O ^c   Del Poeta, Maurizio ^a,b  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^c GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Biochemical Systems Theory; Ceramide; Cryptococcus neoformans; S system; Sphingolipid

Indexed keywords

CERAMIDE DERIVATIVE; EBSELEN; FUNGAL ENZYME; INOSITOL PHOSPHORYLCERAMIDE SYNTHASE; INOSITOL PHOSPHOSPHINGOLIPID PHOSPHOLIPASE C; PHYTOCERAMIDE; SPHINGOLIPID; UNCLASSIFIED DRUG; CERAMIDE;

ARTICLE; CONTROLLED STUDY; CRYPTOCOCCUS NEOFORMANS; CYTOPLASM; DOWN REGULATION; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; FUNGUS GROWTH; GENE DELETION; LIPID METABOLISM; MATHEMATICAL MODEL; MITOCHONDRION; NONHUMAN; PATHOGENICITY; PH; PRIORITY JOURNAL; VALIDATION STUDY; BIOLOGICAL MODEL; BIOLOGY; GOLGI COMPLEX; METABOLISM; METHODOLOGY; SYSTEMS BIOLOGY; THEORETICAL MODEL; VIRULENCE;

FILOBASIDIELLA NEOFORMANS; FUNGI;

CERAMIDES; COMPUTATIONAL BIOLOGY; CRYPTOCOCCUS NEOFORMANS; CYTOPLASM; ENDOPLASMIC RETICULUM; GOLGI APPARATUS; HYDROGEN-ION CONCENTRATION; MITOCHONDRIA; MODELS, BIOLOGICAL; MODELS, THEORETICAL; SPHINGOLIPIDS; SYSTEMS BIOLOGY; VIRULENCE;

EID: 42149102534     PISSN: 17444292     EISSN: 17444292     Source Type: Journal    
DOI: 10.1038/msb.2008.17     Document Type: Article

References (70)

1. Achleitner G, Gaigg B, Krasser A, Kainersdorfer E, Kohlwein SD, Perktold A, Zellnig G, Daum G (1999) Association between the endoplasmic reticulum and mitochondria of yeast facilitates interorganelle transport of phospholipids through membrane contact. Eur J Biochem 264: 545-553
2. Ahn AC, Tewari M, Poon CS, Phillips RS (2006a) The clinical applications of a systems approach. PLoS Med 3: e209
3. Ahn AC, Tewari M, Poon CS, Phillips RS (2006b) The limits of reductionism in medicine: could systems biology offer an alternative? PLoS Med 3: e208
4. Akhter S, McDade HC, Gorlach JM, Heinrich G, Cox GM, Perfect JR (2003) Role of alternative oxidase gene in pathogenesis of Cryptococcus neoformans. Infect Immun 71: 5794-5802
5. Alvarez M, Casadevall A (2006) Phagosome extrusion and host-cell survival after Cryptococcus neoformans phagocytosis by macrophages. Curr Biol 16: 2161-2165
6. Alvarez-Vasquez F, Sims KJ, Cowart LA, Okamoto Y, Voit EO, Hannun YA (2005) Simulation and validation of modelled sphingolipid metabolism in Saccharomyces cerevisiae. Nature 433: 425-430
7. Alvarez-Vasquez F, Sims KJ, Hannun YA, Voit EO (2004) Integration of kinetic information on yeast sphingolipid metabolism in dynamical pathway models. J Theor Biol 226: 265-291
8. Berne S, Sepcic K, Anderluh G, Turk T, Macek P, Poklar Ulrih N (2005) Effect of pH on the pore forming activity and conformational stability of ostreolysin, a lipid raft-binding protein from the edible mushroom Pleurotus ostreatus. Biochemistry 44: 11137-11147
9. Birbes H, El Bawab S, Hannun YA, Obeid LM (2001) Selective hydrolysis of a mitochondrial pool of sphingomyelin induces apoptosis. FASEB J 15: 2669-2679
10. Birbes H, Luberto C, Hsu YT, El Bawab S, Hannun YA, Obeid LM (2005) A mitochondrial pool of sphingomyelin is involved in TNFalpha-induced Bax translocation to mitochondria. Biochem J 386: 445-451
11. Bligh EG, Dyer WJ (1959) A rapid method for total lipid extraction and purification. Can J Biochem Physiol 37: 911-917
12. Buede R, Rinker-Schaffer C, Pinto WJ, Lester RL, Dickson RC (1991) Cloning and characterization of LCB1, a Saccharomyces gene required for biosynthesis of the long-chain base component of sphingolipids. J Bacteriol 173: 4325-4332
13. Casadevall A, Perfect JR (1998) Cryptococcus neoformans, pp 381-405. Washington, DC: ASM Press
14. Chang A, Slayman CW (1991) Maturation of the yeast plasma membrane [H+]ATPase involves phosphorylation during intracellular transport. J Cell Biol 115: 289-295
15. Dickson RC, Lester RL (1999) Metabolism and selected functions of sphingolipids in the yeast Saccharomyces cerevisiae. Biochim Biophys Acta 1438: 305-321
16. Durand T, Delmas-Beauvieux MC, Canioni P, Gallis JL (1999) Role of intracellular buffering power on the mitochondria-cytosol pH gradient in the rat liver perfused at 4 degrees C. Cryobiology 38: 68-80
17. Fan W, Kraus PR, Boily MJ, Heitman J (2005) Cryptococcus neoformans gene expression during murine macrophage infection. Eukaryot Cell 4: 1420-1433
18. Feldmesser M, Tucker S, Casadevall A (2001) Intracellular parasitism of macrophages by Cryptococcus neoformans. Trends Microbiol 9: 273-278
19. Ferreira A (2000) Power Law Analysis and Simulation (PLAS), http://www.dqb.fc.ul.pt/docentes/aferreira/plas.html
20. Fronzes R, Chaignepain S, Bathany K, Giraud MF, Arselin G, Schmitter JM, Dautant A, Velours J, Brethes D (2003) Topological and functional study of subunit h of the F1Fo ATP synthase complex in yeast Saccharomyces cerevisiae. Biochemistry 42: 12038-12049
21. Funato K, Riezman H (2001) Vesicular and nonvesicular transport of ceramide from ER to the Golgi apparatus in yeast. J Cell Biol 155: 949-959
22. Futerman AH, Hannun YA (2004) The complex life of simple sphingolipids. EMBO Rep 5: 777-782
23. Gaigg B, Timischl B, Corbino L, Schneiter R (2005) Synthesis of sphingolipids with very long chain fatty acids but not ergosterol is required for routing of newly synthesized plasma membrane ATPase to the cell surface of yeast. J Biol Chem 280: 22515-22522
24. Gaigg B, Toulmay A, Schneiter R (2006) Very long-chain fatty acid-containing lipids rather than sphingolipids per se are required for raft association and stable surface transport of newly synthesized plasma membrane ATPase in yeast. J Biol Chem 281: 34135-34145
25. Hannun YA, Luberto C (2000) Ceramide in the eukaryotic stress response. Trends Cell Biol 10: 73-80
26. Hechtberger P, Zinser E, Saf R, Hummel K, Paltauf F, Daum G (1994) Characterization, quantification and subcellular localization of inositol-containing sphingolipids of the yeast, Saccharomyces cerevisiae. Eur J Biochem 225: 641-649
27. Heidler SA, Radding JA (2000) Inositol phosphoryl transferases from human pathogenic fungi. Biochim Biophys Acta 1500: 147-152
28. Heung LJ, Kaiser AE, Luberto C, Del Poeta M (2005) The role and mechanism of diacylglycerol-protein kinase C1 signaling in melanogenesis by Cryptococcus neoformans. J Biol Chem 280: 28547-28555
29. Heung LJ, Luberto C, Plowden A, Hannun YA, Del Poeta M (2004) The sphingolipid pathway regulates protein kinase C 1 (Pkc1) through the formation of diacylglycerol (DAG) in Cryptococcus neoformans. J Biol Chem 279: 21144-21153
30. Khan MA, Jabeen R, Mohammad O (2004) Prophylactic role of liposomized chloroquine against murine cryptococcosis less susceptible to fluconazole. Pharm Res 21: 2207-2212
31. Kitagaki H, Cowart LA, Matmati N, Vaena de Avalos S, Novgorodov SA, Zeidan YH, Bielawski J, Obeid LM, Hannun YA (2007) Isc1 regulates sphingolipid metabolism in yeast mitochondria. Biochim Biophys Acta 1768: 2849-2861
32. Kuroda M, Hashida-Okado T, Yasumoto R, Gomi K, Kato I, Takesako K (1999) An aureobasidin A resistance gene isolated from Aspergillus is a homolog of yeast AUR1, a gene responsible for inositol phosphorylceramide (IPC) synthase activity. Mol Gen Genet 261: 290-296
33. +-ATPase Pma1p in the yeast endoplasmic reticulum. J Biol Chem 277: 22395-22401
34. Levine TP, Wiggins CAR, Munro S (2000) Inositol phosphorylceramide synthase is located in the Golgi apparatus of Saccharomyces cerevisiae. Mol Biol Cell 11: 2267-2281
35. Liu K, Zhang X, Sumanasekera C, Lester RL, Dickson RC (2005) Signalling functions for sphingolipid long-chain bases in Saccharomyces cerevisiae. Biochem Soc Trans 33: 1170-1173
36. Luberto C, Hannun YA (1999) Sphingolipid metabolism in the regulation of bioactive molecules. Lipids 34: S5-11
37. Luberto C, Toffaletti DL, Wills EA, Tucker SC, Casadevall A, Perfect JR, Hannun YA, Del Poeta M (2001) Roles for inositol-phosphoryl ceramide synthase 1 (IPC1) in pathogenesis of C. neoformans. Genes Dev 15: 201-212
38. Ma H, Croudace JE, Lammas DA, May RC (2006) Expulsion of live pathogenic yeast by macrophages. Curr Biol 16: 2156-2160
39. Mao C, Obeid LM (2000) Yeast sphingosine-1-phosphate phosphatases: assay, expression, deletion, purification, and cellular localization by GFP tagging. Methods Enzymol 311: 223-232
40. Mao C, Xu R, Bielawska A, Obeid LM (2000) Cloning of an alkaline ceramidase from Saccharomyces cerevisiae. An enzyme with reverse (CoA-independent) ceramide synthase activity. J Biol Chem 275: 6876-6884
41. Mare L, Iatta R, Montagna MT, Luberto C, Del Poeta M (2005) APP1 transcription is regulated by IPC1-DAG pathway and is controlled by ATF2 transcription factor in Cryptococcus neoformans. J Biol Chem 280: 36055-36064
42. Matsuyama S, Reed JC (2000) Mitochondria-dependent apoptosis and cellular pH regulation. 7: 1155-1165
43. Mazzolla R, Barluzzi R, Brozzetti A, Boelaert JR, Luna T, Saleppico S, Bistoni F, Blasi E (1997) Enhanced resistance to Cryptococcus neoformans infection induced by chloroquine in a murine model of meningoencephalitis. Antimicrob Agents Chemother 41: 802-807
44. McQuiston TJ, Haller C, Del Poeta M (2006) Sphingolipids as targets for microbial infections. Mini Rev Med Chem 6: 671-680
45. NCCLS, Standards NCfCL (1997) Reference Method for Broth Dilution Susceptibility Testing of Yeasts. Approved Standard M27-A. Wayne, PA: National Committee for Clinical Laboratory Standards
46. Patton JL, Srinivasan B, Dickson RC, Lester RL (1992) Phenotypes of sphingolipid-dependent strains of Saccharomyces cerevisiae. J Bacteriol 174: 7180-7184
47. Perfect JR (2005) Cryptococcus neoformans: a sugar-coated killer with designer genes. FEMS Immunol Med Microbiol 45: 395-404
48. Perlin DS, Seto-Young D, Monk BC (1997) The plasma membrane H(+)-ATPase of fungi. A candidate drug target? Ann NY Acad Sci 834: 609-617
49. Perona R, Portillo F, Giraldez F, Serrano R (1990) Transformation and pH homeostasis of fibroblasts expressing yeast H(+)-ATPase containing site-directed mutations. Mol Cell Biol 10: 4110-4115
50. Perry DK, Bielawska A, Hannun YA (2000) Quantitative determination of ceramide using diglyceride kinase. Methods Enzymol 312: 22-31
51. Pettus BJ, Kroesen BJ, Szulc ZM, Bielawska A, Bielawski J, Hannun YA, Busman M (2004) Quantitative measurement of different ceramide species from crude cellular extracts by normal-phase high-performance liquid chromatography coupled to atmospheric pressure ionization mass spectrometry. Rapid Commun Mass Spectrom 18: 577-583
52. +-ATPase and identification of a regulatory domain at the carboxyl-terminus. FEBS Lett 247: 381-385
53. +-ATPase by directed mutagenesis and intragenic suppression. FEBS Lett 287: 71-74
54. Rittershaus PC, Kechichian TB, Allegood J, Merrill AHJ, Hennig M, Luberto C, Del Poeta M (2006) Glucosylceramide is an essential regulator of pathogenicity of Cryptococcus neoformans. J Clin Invest 116: 1651-1659
55. Saito K, Takakuwa N, Ohnishi M, Oda Y (2006) Presence of glucosylceramide in yeast and its relation to alkali tolerance of yeast. Appl Microbiol Biotechnol 69: 1-7
56. Savageau MA (1969a) Biochemical systems analysis. I. Some mathematical properties of the rate law for the component enzymatic reactions. J Theor Biol 25: 365-369
57. Savageau MA (1969b) Biochemical systems analysis. II. The steady-state solutions for an n-pool system using a power-law approximation. J Theor Biol 25: 370-379
58. Savageau MA (1976) Biochemical Systems Analysis. A Study of Function and Design in Molecular Biology. Reading, MA: Addison-Wesley
59. Serrano R (1988) Structure and function of proton translocating ATPase in plasma membranes of plants and fungi. Biochim Biophys Acta 947: 1-28
60. 2+-ATPases. Nature 319: 689-693
61. Shea J, Kechichian TB, Luberto C, Del Poeta M (2006) The cryptococcal enzyme inositol phosphosphingolipid-phospholipase C (Isc1) confers resistance to the antifungal effects of macrophages and promotes fungal dissemination to the central nervous system. Infect Immun 74: 5977-5988
62. Soteropoulos P, Vaz T, Santangelo R, Paderu P, Huang DY, Tamas MJ, Perlin DS (2000) Molecular characterization of the plasma membrane H(+)-ATPase, an antifungal target in Cryptococcus neoformans. Antimicrob Agents Chemother 44: 2349-2355
63. Torres NV, Voit EO (2002) Pathway Analysis and Optimization in Metabolic Engineering. Cambridge, UK: Cambridge University Press
64. Toulmay A, Schneiter R (2006) A two-step method for the introduction of single or multiple defined point mutations into the genome of Saccharomyces cerevisiae. Yeast 23: 825-831
65. Toulmay A, Schneiter R (2007) Lipid-dependent surface transport of the proton pumping ATPase: a model to study plasma membrane biogenesis in yeast. Biochimie 89: 249-254
66. Vaena de Avalos S, Okamoto Y, Hannun YA (2004) Activation and localization of inositol phosphosphingolipid phospholipase C, Isc1p, to the mitochondria during growth of Saccharomyces cerevisiae. J Biol Chem 279: 11537-11545
67. Vaena de Avalos S, Su X, Zhang M, Okamoto Y, Dowhan W, Hannun YA (2005) The phosphatidylglycerol/cardiolipin biosynthetic pathway is required for the activation of inositol phosphosphingolipid phospholipase C, Isc1p, during growth of Saccharomyces cerevisiae. J Biol Chem 280: 7170-7177
68. Voit EO (2000) Canonical modeling: review of concepts with emphasis on environmental health. Environ Health Perspect 108 (Suppl 5): 895-909
69. +-ATPase. J Biol Chem 271: 25438-25445
70. Wang Q, Chang A (2002) Sphingoid base synthesis is required for oligomerization and cell surface stability of the yeast plasma membrane ATPase, Pma1. Proc Natl Acad Sci USA 99: 12853-12858