Conservation of the sterol regulatory element-binding protein pathway and its pathobiological importance in cryptococcus neoformans

Eukaryotic Cell

Volumn 8, Issue 11, 2009, Pages 1770-1779

  Chang, Yun C ^a   Ingavale, Susham S ^a   Bien, Clara ^b   Espenshade, Peter ^b   Kwon Chung, Kyung J ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FILOBASIDIELLA NEOFORMANS; FUNGI; MAMMALIA; MUS;

EID: 72449173927     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00207-09     Document Type: Article

References (44)

1. Berlett, B. S., and E. R. Stadtman. 1997. Protein oxidation in aging, disease, and oxidative stress. J. Biol. Chem. 272:20313-20316.
2. Burg, J. S., D. W. Powell, R. Chai, A. L. Hughes, A. J. Link, and P. J. Espenshade. 2008. Insig regulates HMG-CoA reductase by controlling enzyme phosphorylation in fission yeast. Cell Metab. 8:522-531.
3. Chang, Y. C., C. M. Bien, H. Lee, P. J. Espenshade, and K. J. Kwon-Chung. 2007. Sre1p, a regulator of oxygen sensing and sterol homeostasis, is required for virulence in Cryptococcus neoformans. Mol. Microbiol. 64:614-629.
4. Chang, Y. C., L. A. Penoyer, and K. J. Kwon-Chung. 2001. The second STE12 homologue of Cryptococcus neoformans is MATa-specific and plays an important role in virulence. Proc. Nad. Acad. Sci. USA 98:3258-3263.
5. Chun, C. D., O. W. Liu, and H. D. Madhani. 2007. A link between virulence and homeostatic responses to hypoxia during infection by the human fungal pathogen Cryptococcus neoformans. PLoS Pathog. 3:e22.
6. Cocheme, H. M., and M. P. Murphy. 2008. Complex I is the major site of mitochondrial superoxide production by paraquat. J. Biol. Chem. 283:1786-1798.
7. Espenshade, P. J., and A. L. Hughes. 2007. Regulation of sterol synthesis in eukaryotes. Annu. Rev. Genet. 41:401-427.
8. Espenshade, P. J., W. P. Li, and D. Yabe. 2002. Sterols block binding of COPII proteins to SCAP, thereby controlling SCAP sorting in ER. Proc. Natl. Acad. Sci. USA 99:11694-11699.
9. Flury, I., R. Garza, A. Shearer, J. Rosen, S. Cronin, and R. Y. Hampton. 2005. INSIG: a broadly conserved transmembrane chaperone for sterolsensing domain proteins. EMBO J. 24:3917-3926. (Pubitemid 41637998)
10. Frame, S., and P. Cohen. 2001. GSK3 takes centre stage more than 20 years after its discovery. Biochem. J. 359:1-16. (Pubitemid 32939202)
11. Freeman, M. L., S. A. Huntley, M. J. Meredith, G. A. Senisterra, and J. Lepock. 1997. Destabilization and denaturation of cellular protein by glutathione depletion. Cell Stress Chaperones 2:191-198.
12. Goldstein, J. L., R. A. DeBose-Boyd, and M. S. Brown. 2006. Protein sensors for membrane sterols. Cell 124:35-46.
13. Gordan, J. D., and M. C. Simon. 2007. Hypoxia-inducible factors: central regulators of the tumor phenotype. Curr. Opin. Genet. Dev. 17:71-77.
14. Harvey, B. H. 2000. Acid-dependent dismutation of nitrogen oxides may be a critical source of nitric oxide in human macrophages. Med. Hypotheses 54:829-831.
15. Horton, J. D., N. A. Shah, J. A. Warrington, N. N. Anderson, S. W. Park, M. S. Brown, and J. L. Goldstein. 2003. Combined analysis of oligonucleotide microarray data from transgenic and knockout mice identifies direct SREBP target genes. Proc. Natl. Acad. Sci. USA 100:12027-12032.
16. Hughes, A. L., B. L. Todd, and P. J. Espenshade. 2005. SREBP pathway responds to sterols and functions as an oxygen sensor in fission yeast. Cell 120:831-842.
17. Hughes, B. T., and P. J. Espenshade. 2008. Oxygen-regulated degradation of fission yeast SREBP by Ofd1, a prolyl hydroxylase family member. EMBO J. 27:1491-1501.
18. Ingavale, S., Y. C. Chang, H. Lee, C. M. McClelland, M. L. Leong, and K. J. Kwon-Chung. 2008. Importance of mitochondria in survival of Cryptococcus neoformans under low oxygen conditions and tolerance to cobalt chloride. PLoS Pathog. 4:e1000155.
19. Jamieson, D. J. 1998. Oxidative stress responses of the yeast Saccharomyces cerevisiae. Yeast 14:1511-1527.
20. Jolly, W. L. 1964. The inorganic chemistry of nitrogen, p.68-79. W.A. Benjamin, Inc., New York. NY.
21. Kim, K. H., M. J. Song, E. J. Yoo, S. S. Choe, S. D. Park, and J. B. Kim. 2004. Regulatory role of glycogen synthase kinase 3 for transcriptional activity of ADD1/SREBP1c. J. Biol. Chem. 279:51999-52006.
22. Kwon-Chung, K. J., and J. E. Bennett. 1992. Medical mycology. Lea & Febiger, Philadelphia, PA.
23. Lee, H., C. M. Bien, A. L. Hughes, P. J. Espenshade, K. J. Kwon-Chung, and Y. C. Chang. 2007. Cobalt chloride, a hypoxia-mimicking agent, targets sterol synthesis in the pathogenic fungus Cryptococcus neoformans. Mol. Microbiol. 65:1018-1033.
24. Lee, S. J., T. Sekimoto, E. Yamashita, E. Nagoshi, A. Nakagawa, N. Imamoto, M. Yoshimura, H. Sakai, K. T. Chong, T. Tsukihara, and Y. Yoneda. 2003. The structure of importin-beta bound to SREBP-2: nuclear import of a transcription factor. Science 302:1571-1575. (Pubitemid 37475702)
25. Loftus, B. J., E. Fung, P. Roncaglia, D. Rowley, P. Amedeo, D. Bruno, J. Vamathevan, M. Miranda, I. J. Anderson, J. A. Fraser, J. E. Allen, I. E. Bosdet, M. R. Brent, R. Chiu, T. L. Doering, M. J. Donlin, C. A. D'Souza, D. S. Fox, V. Grinberg, J. Fu, M. Fukushima, B. J. Haas, J. C. Huang, G. Janbon, S. J. Jones, H. L. Koo, M. I. Krzywinski, J. K. Kwon-Chung, K. B. Lengeler, R. Maiti, M. A. Marra, R. E. Marra, C. A. Mathewson, T. G. Mitchell, M. Pertea, F. R. Riggs, S. L. Salzberg, J. E. Schein, A. Shvartsbeyn, H. Shin, M. Shumway, C. A. Specht, B. B. Suh, A. Tenney, T. R. Utterback, B. L. Wickes, J. R. Wortman, N. H. Wye, J. W. Kronstad, J. K. Lodge, J. Heitman, R. W. Davis, C. M. Fraser, and R. W. Hyman. 2005. The genome of the basidiomycetous yeast and human pathogen Cryptococcus neoformans. Science 307:1321-1324.
26. McClelland, C. M., Y. C. Chang, and K. J. Kwon-Chung. 2005. High frequency transformation of Cryptococcus neoformans and Cryptococcus gattii by Agrobacterium tumefaciens. Fungal Genet. Biol. 42:904-913.
27. Monks, T. J., R. P. Hanzlik, G. M. Cohen, D. Ross, and D. G. Graham. 1992. Quinone chemistry and toxicity. Toxicol. Appl. Pharmacol. 112:2-16.
28. Mosammaparast, N., and L. F. Pemberton. 2004. Karyopherins: from nuclear-transport mediators to nuclear-function regulators. Trends Cell Biol. 14:547-556. (Pubitemid 39296617)
29. Nagasaki, K., N. Maass, T. Manabe, H. Hanzawa, T. Tsukada, K. Kikuchi, and K. Yamaguchi. 1999. Identification of a novel gene, DAM1, amplified at chromosome 1p13.3-21 region in human breast cancer cell lines. Cancer Lett. 140:219-226. (Pubitemid 29251334)
30. Nagoshi, E., N. Imamoto, R. Sato, and Y. Yoneda. 1999. Nuclear import of sterol regulatory element-binding protein-2, a basic helix-loop-helix-leucine zipper (bHLH-Zip)-containing transcription factor, occurs through the direct interaction of importin beta with HLH-Zip. Mol. Biol. Cell 10:2221-2233.
31. Ozer, A., and R. K. Bruick. 2007. Non-heme dioxygenases: cellular sensors and regulators jelly rolled into one? Nat. Chem. Biol. 3:144-153.
32. Peng, R., A. De Antoni, and D. Gallwitz. 2000. Evidence for overlapping and distinct functions in protein transport of coat protein Sec24p family members. J. Biol. Chem. 275:11521-11528.
33. Peng, Y., E. J. Schwarz, M. A. Lazar, A. Genin, N. B. Spinner, and R. Taub. 1997. Cloning, human chromosomal assignment, and adipose and hepatic expression of the CL-6/INSIG1 gene. Genomics 43:278-284. (Pubitemid 27353703)
34. Raghow, R., C. Yellaturu, X. Deng, E. A. Park, and M. B. Elam. 2008. SREBPs: the crossroads of physiological and pathological lipid homeostasis. Trends Endocrinol. Metab. 19:65-73.
35. Rawson, R. B. 2003. The SREBF pathway: insights from Insigs and insects. Nat. Rev. Mol. Cell Biol. 4:631-640.
36. Schofleld, C. J., and P. J. Ratcliffe. 2005. Signalling hypoxia by HIF hydroxylases. Biochem. Biophys. Res. Commun. 338:617-626.
37. Somesh, B. P., J. Reid, W. F. Liu, T. M. Sogaard, H. Erdjument-Bromage, P. Tempst, and J. Q. Svejstrup. 2005. Multiple mechanisms confining RNA polymerase II ubiquitylation to polymerases undergoing transcriptional arrest. Cell 121:913-923.
38. Sun, L. P., L. Li, J. L. Goldstein, and M. S. Brown. 2005. Insig required for sterol-mediated inhibition of Scap/SREBP binding to COPII proteins in vitro. J. Biol. Chem. 280:26483-26490.
39. Sundqvist, A., M. T. Bengoechea-Alonso, X. Ye, V. Lukiyanchuk, J. Jin, J. W. Harper, and J. Ericsson. 2005. Control of lipid metabolism by phosphorylation-dependent degradation of the SREBP family of transcription factors by SCF(Fbw7). Cell Metab. 1:379-391. (Pubitemid 43960622)
40. Sydorskyy, Y., D. J. Dilworth, E. C. Yi, D. R. Goodlett, R. W. Wozniak, and J. D. Aitchison. 2003. Intersection of the Kap123p-mediated nuclear import and ribosome export pathways. Mol. Cell. Biol. 23:2042-2054.
41. Todd, B. L., E. V. Stewart, J. S. Burg, A. L. Hughes, and P. J. Espenshade. 2006. Sterol regulatory element binding protein is a principal regulator of anaerobic gene expression in fission yeast. Mol. Cell. Biol. 26:2817-2831.
42. Toffaletti, D. L., T. H. Rude, S. A. Johnston, D. T. Durack, and J. R. Perfect. 1993. Gene transfer in Cryptococcus neoformans by use of biolistic delivery of DNA. J. Bacteriol. 175:1405-1411.
43. Willger, S. D., N. Grahl, and R. A. Cramer, Jr. 2009. Aspergillus fumigatus metabolism: clues to mechanisms of in vivo fungal growth and virulence. Med. Mycol. 47(Suppl. 1):S72-S79.
44. Yang, J., J. L. Goldstein, R. E. Hammer, Y. A. Moon, M. S. Brown, and J. D. Horton. 2001. Decreased lipid synthesis in livers of mice with disrupted site-1 protease gene. Proc. Natl. Acad. Sci. USA 98:13607-13612.