All about that fat: Lipid modification of proteins in Cryptococcus neoformans

Journal of Microbiology

Volumn 54, Issue 3, 2016, Pages 212-222

  Santiago Tirado, Felipe H ^a   Doering, Tamara L ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cryptococcus; GPI anchored proteins; isoprenylation; lipid modification; myristoylation; palmitoylation; prenylation; protein lipidation

Indexed keywords

FUNGAL PROTEIN;

ACYLATION; CHEMISTRY; CRYPTOCOCCOSIS; CRYPTOCOCCUS NEOFORMANS; ENZYMOLOGY; HUMAN; LIPID METABOLISM; LIPOYLATION; METABOLISM; MICROBIOLOGY; MOLECULAR MODEL; PATHOGENICITY; PRENYLATION; PROCEDURES; PROTEIN PROCESSING; PROTEOMICS;

ACYLATION; CRYPTOCOCCOSIS; CRYPTOCOCCUS NEOFORMANS; FUNGAL PROTEINS; HUMANS; LIPID METABOLISM; LIPOYLATION; MODELS, MOLECULAR; PRENYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOMICS;

EID: 84959244665     PISSN: 12258873     EISSN: 19763794     Source Type: Journal    
DOI: 10.1007/s12275-016-5626-6     Document Type: Review

References (81)

1. Aitken, A., Cohen, P., Santikarn, S., Williams, D.H., Calder, A.G., Smith, A., and Klee, C.B. 1982. Identification of the NH2-terminal blocking group of calcineurin B as myristic acid. FEBS Lett.150, 314–318.
2. Blanc, M., Blaskovic, S., and van der Goot, F.G. 2013. Palmitoylation, pathogens and their host. Biochem. Soc. Trans.41, 84–88.
3. Brown, G.D., Denning, D.W., Gow, N.A., Levitz, S.M., Netea, M.G., and White, T.C. 2012. Hidden killers: human fungal infections. Sci. Transl. Med.4, 165rv113.
4. Caminero, A., Calvo, E., Valentin, E., Ruiz-Herrera, J., Lopez, J.A., and Sentandreu, R. 2014. Identification of Candida albicans wall mannoproteins covalently linked by disulphide and/or alkalisensitive bridges. Yeast31, 137–144.
5. Chayakulkeeree, M., Sorrell, T.C., Siafakas, A.R., Wilson, C.F., Pantarat, N., Gerik, K.J., Boadle, R., and Djordjevic, J.T. 2008. Role and mechanism of phosphatidylinositol-specific phospholipase C in survival and virulence of Cryptococcus neoformans. Mol. Microbiol.69, 809–826.
6. Costachel, C., Coddeville, B., Latge, J.P., and Fontaine, T. 2005. Glycosylphosphatidylinositol-anchored fungal polysaccharide in Aspergillus fumigatus. J. Biol. Chem.280, 39835–39842.
7. Das, U., Kumar, S., Dimmock, J.R., and Sharma, R.K. 2012. Inhibition of protein N-myristoylation: a therapeutic protocol in developing anticancer agents. Curr. Cancer Drug Target12, 667–692.
8. Davidson, R.C., Moore, T.D., Odom, A.R., and Heitman, J. 2000. Characterization of the MFalpha pheromone of the human fungal pathogen Cryptococcus neoformans. Mol. Microbiol.38, 1017–1026.
9. Djordjevic, J.T., Del Poeta, M., Sorrell, T.C., Turner, K.M., and Wright, L.C. 2005. Secretion of cryptococcal phospholipase B1 (PLB1) is regulated by a glycosylphosphatidylinositol (GPI) anchor. Biochem. J.389, 803–812.
10. Doering, T.L. 2009. How sweet it is! Cell wall biogenesis and polysaccharide capsule formation in Cryptococcus neoformans. Annu. Rev. Microbiol.63, 223–247.
11. Duronio, R.J., Reed, S.I., and Gordon, J.I. 1992. Mutations of human myristoyl-CoA:protein N-myristoyltransferase cause temperature- sensitive myristic acid auxotrophy in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA89, 4129–4133.
12. Eastman, R.T., Buckner, F.S., Yokoyama, K., Gelb, M.H., and Van Voorhis, W.C. 2006. Thematic review series: lipid posttranslational modifications. Fighting parasitic disease by blocking protein farnesylation. J. Lipid Res.47, 233–240.
13. Eichler, J. and Adams, M.W. 2005. Posttranslational protein modification in Archaea. Microbiol. Mol. Biol. Rev.69, 393–425.
14. Eigenheer, R.A., Jin Lee, Y., Blumwald, E., Phinney, B.S., and Gelli, A. 2007. Extracellular glycosylphosphatidylinositol-anchored mannoproteins and proteases of Cryptococcus neoformans. FEMS Yeast Res.7, 499–510.
15. Fang, W., Robinson, D.A., Raimi, O.G., Blair, D.E., Harrison, J.R., Lockhart, D.E., Torrie, L.S., Ruda, G.F., Wyatt, P.G., Gilbert, I.H., et al. 2015. N-myristoyltransferase is a cell wall target in Aspergillus fumigatus. ACS Chem. Biol.10, 1425–1434.
16. Ferguson, M.A., Low, M.G., and Cross, G.A. 1985. Glycosyl-sn-1,2- dimyristylphosphatidylinositol is covalently linked to Trypanosoma brucei variant surface glycoprotein. J. Biol. Chem.260, 14547–14555.
17. Folch, J. and Lees, M. 1951. Proteolipides, a new type of tissue lipoproteins; their isolation from brain. J. Biol. Chem.191, 807–817.
18. Fontaine, T., Magnin, T., Melhert, A., Lamont, D., Latge, J.P., and Ferguson, M.A. 2003. Structures of the glycosylphosphatidylinositol membrane anchors from Aspergillus fumigatus membrane proteins. Glycobiology13, 169–177.
19. Fortwendel, J.R., Juvvadi, P.R., Rogg, L.E., Asfaw, Y.G., Burns, K.A., Randell, S.H., and Steinbach, W.J. 2012. Plasma membrane localization is required for RasA-mediated polarized morphogenesis and virulence of Aspergillus fumigatus. Eukaryot. Cell11, 966–977.
20. Franzot, S.P. and Doering, T.L. 1999. Inositol acylation of glycosylphosphatidylinositols in the pathogenic fungus Cryptococcus neoformans and the model yeast Saccharomyces cerevisiae. Biochem. J.340(Pt 1), 25–32.
21. Frenal, K., Tay, C.L., Mueller, C., Bushell, E.S., Jia, Y., Graindorge, A., Billker, O., Rayner, J.C., and Soldati-Favre, D. 2013. Global analysis of apicomplexan protein S-acyl transferases reveals an enzyme essential for invasion. Traffic14, 895–911.
22. Frieman, M.B. and Cormack, B.P. 2004. Multiple sequence signals determine the distribution of glycosylphosphatidylinositol proteins between the plasma membrane and cell wall in Saccharomyces cerevisiae. Microbiology150, 3105–3114.
23. Georgopapadakou, N.H. 2002. Antifungals targeted to protein modification: focus on protein N-myristoyltransferase. Expert. Opin. Investig. Drugs11, 1117–1125.
24. Gilbert, N.M., Baker, L.G., Specht, C.A., and Lodge, J.K. 2012. A glycosylphosphatidylinositol anchor is required for membrane localization but dispensable for cell wall association of chitin deacetylase 2 in Cryptococcus neoformans. mBio3, e00007–12.
25. Gillingham, A.K. and Munro, S. 2007. The small G proteins of the Arf family and their regulators. Annu. Rev. Cell. Dev. Biol.23, 579–611.
26. Goldston, A.M., Sharma, A.I., Paul, K.S., and Engman, D.M. 2014. Acylation in trypanosomatids: an essential process and potential drug target. Trends Parasitol.30, 350–360.
27. Gutkowska, M. and Swiezewska, E. 2012. Structure, regulation and cellular functions of Rab geranylgeranyl transferase and its cellular partner Rab Escort Protein. Mol. Membr. Biol.29, 243–256.
28. Hast, M.A., Nichols, C.B., Armstrong, S.M., Kelly, S.M., Hellinga, H.W., Alspaugh, J.A., and Beese, L.S. 2011. Structures of Cryptococcus neoformans protein farnesyltransferase reveal strategies for developing inhibitors that target fungal pathogens. J. Biol. Chem.286, 35149–35162.
29. Hicks, S.W. and Galan, J.E. 2013. Exploitation of eukaryotic subcellular targeting mechanisms by bacterial effectors. Nat. Rev. Microbiol.11, 316–326.
30. Honscher, C. and Ungermann, C. 2014. A close-up view of membrane contact sites between the endoplasmic reticulum and the endolysosomal system: from yeast to man. Crit. Rev. Biochem. Mol. Biol.49, 262–268.
31. Howie, J., Reilly, L., Fraser, N.J., Vlachaki Walker, J.M., Wypijewski, K.J., Ashford, M.L., Calaghan, S.C., McClafferty, H., Tian, L., Shipston, M.J., et al. 2014. Substrate recognition by the cell surface palmitoyl transferase DHHC5. Proc. Natl. Acad. Sci. USA111, 17534–17539.
32. Ivanov, S.S. and Roy, C. 2013. Host lipidation: a mechanism for spatial regulation of Legionella effectors. Curr. Top. Microbiol. Immunol.376, 135–154.
33. Janbon, G., Ormerod, K.L., Paulet, D., Byrnes, E.J., 3rd, Yadav, V., Chatterjee, G., Mullapudi, N., Hon, C.C., Billmyre, R.B., Brunel, F., et al. 2014. Analysis of the genome and transcriptome of Cryptococcus neoformans var. grubii reveals complex RNA expression and microevolution leading to virulence attenuation. PLoS Genet.10, e1004261.
34. Jones, M.L., Collins, M.O., Goulding, D., Choudhary, J.S., and Rayner, J.C. 2012. Analysis of protein palmitoylation reveals a pervasive role in Plasmodium development and pathogenesis. Cell Host Microbe12, 246–258.
35. Kamiya, Y., Sakurai, A., Tamura, S., and Takahashi, N. 1978. Structure of rhodotorucine A, a novel lipopeptide, inducing mating tube formation in Rhodosporidium toruloides. Biochem. Biophys. Res. Commun.83, 1077–1083.
36. Kempf, M., Cottin, J., Licznar, P., Lefrancois, C., Robert, R., and Apaire-Marchais, V. 2009. Disruption of the GPI protein-encoding gene IFF4 of Candida albicans results in decreased adherence and virulence. Mycopathologia168, 73–77.
37. Lam, K.K., Davey, M., Sun, B., Roth, A.F., Davis, N.G., and Conibear, E. 2006. Palmitoylation by the DHHC protein Pfa4 regulates the ER exit of Chs3. J. Cell. Biol.174, 19–25.
38. Langner, C.A., Lodge, J.K., Travis, S.J., Caldwell, J.E., Lu, T., Li, Q., Bryant, M.L., Devadas, B., Gokel, G.W., Kobayashi, G.S., and et al. 1992. 4-oxatetradecanoic acid is fungicidal for Cryptococcus neoformans and inhibits replication of human immunodeficiency virus I. J. Biol. Chem.267, 17159–17169.
39. Lin, X., Hull, C.M., and Heitman, J. 2005. Sexual reproduction between partners of the same mating type in Cryptococcus neoformans. Nature434, 1017–1021.
40. Lin, X., Jackson, J.C., Feretzaki, M., Xue, C., and Heitman, J. 2010. Transcription factors Mat2 and Znf2 operate cellular circuits orchestrating opposite- and same-sex mating in Cryptococcus neoformans. PLoS Genet.6, e1000953.
41. Lobo, S., Greentree, W.K., Linder, M.E., and Deschenes, R.J. 2002. Identification of a Ras palmitoyltransferase in Saccharomyces cerevisiae. J. Biol. Chem.277, 41268–41273.
42. Lodge, J.K., Jackson-Machelski, E., Higgins, M., McWherter, C.A., Sikorski, J.A., Devadas, B., and Gordon, J.I. 1998. Genetic and biochemical studies establish that the fungicidal effect of a fully depeptidized inhibitor of Cryptococcus neoformans myristoyl- CoA:protein N-myristoyltransferase (Nmt) is Nmt-dependent. J. Biol. Chem.273, 12482–12491.
43. Lodge, J.K., Jackson-Machelski, E., Toffaletti, D.L., Perfect, J.R., and Gordon, J.I. 1994a. Targeted gene replacement demonstrates that myristoyl-CoA: protein N-myristoyltransferase is essential for viability of Cryptococcus neoformans. Proc. Natl. Acad. Sci. USA91, 12008–12012.
44. Lodge, J.K., Johnson, R.L., Weinberg, R.A., and Gordon, J.I. 1994b. Comparison of myristoyl-CoA:protein N-myristoyltransferases from three pathogenic fungi: Cryptococcus neoformans, Histoplasma capsulatum, and Candida albicans. J. Biol. Chem.269, 2996–3009.
45. Loftus, B.J., Fung, E., Roncaglia, P., Rowley, D., Amedeo, P., Bruno, D., Vamathevan, J., Miranda, M., Anderson, I.J., Fraser, J.A., et al. 2005. The genome of the basidiomycetous yeast and human pathogen Cryptococcus neoformans. Science307, 1321–1324.
46. McClelland, C.M., Fu, J., Woodlee, G.L., Seymour, T.S., and Wickes, B.L. 2002. Isolation and characterization of the Cryptococcus neoformans MATa pheromone gene. Genetics160, 935–947.
47. McLellan, C.A., Whitesell, L., King, O.D., Lancaster, A.K., Mazitschek, R., and Lindquist, S. 2012. Inhibiting GPI anchor biosynthesis in fungi stresses the endoplasmic reticulum and enhances immunogenicity. ACS Chem. Biol.7, 1520–1528.
48. Menon, A.K. 2008. Chapter 2: Lipid Modifications of Proteins, pp. xii, 631. In Vance, D.E. and Vance, J.E. (eds.), Biochemistry of lipids, lipoproteins and membranes. Elsevier, Amsterdam; Boston.
49. Michaelis, S. and Barrowman, J. 2012. Biogenesis of the Saccharomyces cerevisiae pheromone a-factor, from yeast mating to human disease. Microbiol. Mol. Biol. Rev.76, 626–651.
50. Miura, G.I. and Treisman, J.E. 2006. Lipid modification of secreted signaling proteins. Cell Cycle5, 1184–1188.
51. Moissoglu, K. and Schwartz, M.A. 2014. Spatial and temporal control of Rho GTPase functions. Cell Logist.4, e943618.
52. Muñiz, M. and Zurzolo, C. 2014. Sorting of GPI-anchored proteins from yeast to mammals—common pathways at different sites? J. Cell. Sci.127, 2793–2801.
53. Nakayama, H., Kurokawa, K., and Lee, B.L. 2012. Lipoproteins in bacteria: structures and biosynthetic pathways. FEBS J.279, 4247–4268.
54. Nguyen, U.T., Goody, R.S., and Alexandrov, K. 2010. Understanding and exploiting protein prenyltransferases. Chembiochem11, 1194–1201.
55. Nichols, C.B., Ferreyra, J., Ballou, E.R., and Alspaugh, J.A. 2009. Subcellular localization directs signaling specificity of the Cryptococcus neoformans Ras1 protein. Eukaryot. Cell8, 181–189.
56. Nichols, C.B., Ost, K.S., Grogan, D.P., Pianalto, K., Hasan, S., and Alspaugh, J.A. 2015. Impact of protein palmitoylation on the virulence potential of Cryptococcus neoformans. Eukaryot. Cell14, 626–635.
57. Ohno, Y., Kashio, A., Ogata, R., Ishitomi, A., Yamazaki, Y., and Kihara, A. 2012. Analysis of substrate specificity of human DHHC protein acyltransferases using a yeast expression system. Mol. Biol. Cell23, 4543–4551.
58. Ohno, Y., Kihara, A., Sano, T., and Igarashi, Y. 2006. Intracellular localization and tissue-specific distribution of human and yeast DHHC cysteine-rich domain-containing proteins. Biochim. Biophys. Acta.1761, 474–483.
59. Orlean, P. and Menon, A.K. 2007. Thematic review series: lipid posttranslational modifications. GPI anchoring of protein in yeast and mammalian cells, or: how we learned to stop worrying and love glycophospholipids. J. Lipid Res.48, 993–1011.
60. Panackal, A.A., Wuest, S.C., Lin, Y.C., Wu, T., Zhang, N., Kosa, P., Komori, M., Blake, A., Browne, S.K., Rosen, L.B., et al. 2015. Paradoxical immune responses in non-hiv cryptococcal meningitis. PLoS Pathog.11, e1004884.
61. Panethymitaki, C., Bowyer, P.W., Price, H.P., Leatherbarrow, R.J., Brown, K.A., and Smith, D.F. 2006. Characterization and selective inhibition of myristoyl-CoA:protein N-myristoyltransferase from Trypanosoma brucei and Leishmania major. Biochem. J.396, 277–285.
62. Park, B.J., Wannemuehler, K.A., Marston, B.J., Govender, N., Pappas, P.G., and Chiller, T.M. 2009. Estimation of the current global burden of cryptococcal meningitis among persons living with HIV/AIDS. AIDS23, 525–530.
63. Piispanen, A.E., Bonnefoi, O., Carden, S., Deveau, A., Bassilana, M., and Hogan, D.A. 2011. Roles of Ras1 membrane localization during Candida albicans hyphal growth and farnesol response. Eukaryot. Cell10, 1473–1484.
64. Richard, M., Ibata-Ombetta, S., Dromer, F., Bordon-Pallier, F., Jouault, T., and Gaillardin, C. 2002. Complete glycosylphosphatidylinositol anchors are required in Candida albicans for full morphogenesis, virulence and resistance to macrophages. Mol. Microbiol.44, 841–853.
65. Roth, A.F., Feng, Y., Chen, L., and Davis, N.G. 2002. The yeast DHHC cysteine-rich domain protein Akr1p is a palmitoyl transferase. J. Cell. Biol.159, 23–28.
66. Roth, A.F., Wan, J., Bailey, A.O., Sun, B., Kuchar, J.A., Green, W.N., Phinney, B.S., Yates, J.R.3rd, and Davis, N.G. 2006. Global analysis of protein palmitoylation in yeast. Cell125, 1003–1013.
67. Sanchez-Mir, L., Franco, A., Martin-Garcia, R., Madrid, M., Vicente- Soler, J., Soto, T., Gacto, M., Perez, P., and Cansado, J. 2014. Rho2 palmitoylation is required for plasma membrane localization and proper signaling to the fission yeast cell integrity mitogen-activated protein kinase pathway. Mol. Cell. Biol.34, 2745–2759.
68. Santiago-Tirado, F.H., Peng, T., Yang, M., Hang, H.C., and Doering, T.L. 2015. A single protein s-acyl transferase acts through diverse substrates to determine cryptococcal morphology, stress tolerance, and pathogenic outcome. PLoS Pathog.11, e1004908.
69. Schmidt, M.F., Bracha, M., and Schlesinger, M.J. 1979. Evidence for covalent attachment of fatty acids to Sindbis virus glycoproteins. Proc. Natl. Acad. Sci. USA76, 1687–1691.
70. Selvig, K., Ballou, E.R., Nichols, C.B., and Alspaugh, J.A. 2013. Restricted substrate specificity for the geranylgeranyltransferase-I enzyme in Cryptococcus neoformans: implications for virulence. Eukaryot. Cell12, 1462–1471.
71. Shen, H., Chen, S.M., Liu, W., Zhu, F., He, L.J., Zhang, J.D., Zhang, S.Q., Yan, L., Xu, Z., Xu, G.T., et al. 2015a. Abolishing cell wall glycosylphosphatidylinositol-anchored proteins in Candida albicans enhances recognition by host dectin-1. Infect. Immun.83, 2694–2704.
72. Shen, W.C., Davidson, R.C., Cox, G.M., and Heitman, J. 2002. Pheromones stimulate mating and differentiation via paracrine and autocrine signaling in Cryptococcus neoformans. Eukaryot. Cell1, 366–377.
73. Shen, M., Pan, P., Li, Y., Li, D., Yu, H., and Hou, T. 2015b. Farnesyltransferase and geranylgeranyltransferase I: structures, mechanism, inhibitors and molecular modeling. Drug Discov. Today20, 267–276.
74. Siafakas, A.R., Sorrell, T.C., Wright, L.C., Wilson, C., Larsen, M., Boadle, R., Williamson, P.R., and Djordjevic, J.T. 2007. Cell walllinked cryptococcal phospholipase B1 is a source of secreted enzyme and a determinant of cell wall integrity. J. Biol. Chem.282, 37508–37514.
75. Siafakas, A.R., Wright, L.C., Sorrell, T.C., and Djordjevic, J.T. 2006. Lipid rafts in Cryptococcus neoformans concentrate the virulence determinants phospholipase B1 and Cu/Zn superoxide dismutase. Eukaryot. Cell5, 488–498.
76. Srikanta, D., Santiago-Tirado, F.H., and Doering, T.L. 2014. Cryptococcus neoformans: historical curiosity to modern pathogen. Yeast31, 47–60.
77. Umemura, M., Okamoto, M., Nakayama, K., Sagane, K., Tsukahara, K., Hata, K., and Jigami, Y. 2003. GWT1 gene is required for inositol acylation of glycosylphosphatidylinositol anchors in yeast. J. Biol. Chem.278, 23639–23647.
78. Vallim, M.A., Fernandes, L., and Alspaugh, J.A. 2004. The RAM1 gene encoding a protein-farnesyltransferase beta-subunit homologue is essential in Cryptococcus neoformans. Microbiology150, 1925–1935.
79. Watanabe, N.A., Miyazaki, M., Horii, T., Sagane, K., Tsukahara, K., and Hata, K. 2012. E1210, a new broad-spectrum antifungal, suppresses Candida albicans hyphal growth through inhibition of glycosylphosphatidylinositol biosynthesis. Antimicrob. Agents Chemother.56, 960–971.
80. Young, E., Zheng, Z.Y., Wilkins, A.D., Jeong, H.T., Li, M., Lichtarge, O., and Chang, E.C. 2014. Regulation of Ras localization and cell transformation by evolutionarily conserved palmitoyltransferases. Mol. Cell. Biol.34, 374–385.
81. Zhang, M.M., Wu, P.Y., Kelly, F.D., Nurse, P., and Hang, H.C. 2013. Quantitative control of protein S-palmitoylation regulates meiotic entry in fission yeast. PLoS Biol.11, e1001597.