Roles of the three Ras proteins in the regulation of dimorphic transition in the yeast Yarrowia lipolytica

FEMS Yeast Research

Volumn 14, Issue 3, 2014, Pages 451-463

  Li, Min ^a   Li, Yun Qing ^a   Zhao, Xiao Feng ^a   Gao, Xiang Dong ^a,b  

^a WUHAN UNIVERSITY   (China)

^b Hubei Provincial Cooperative Innovation Center of Industrial Fermentation   (China)

Author keywords

Dimorphism; Filamentous growth; Hypha; Hyphal development; Pseudohypha

Indexed keywords

FUNGAL PROTEIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; GUANOSINE TRIPHOSPHATE; PROTEIN YLRAS 1; PROTEIN YLRAS 2; PROTEIN YLRAS 3; RAS PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL FUNCTION; CELL STRUCTURE; ENDOPLASMIC RETICULUM; FUNGUS GROWTH; INTRON; MORPHOGENESIS; NONHUMAN; OPEN READING FRAME; PALMITOYLATION; PROMOTER REGION; REGULATORY MECHANISM; YARROWIA LIPOLYTICA; YEAST CELL; CYTOLOGY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; SIGNAL TRANSDUCTION; YARROWIA;

MAMMALIA; SACCHAROMYCES CEREVISIAE; SACCHAROMYCETALES; YARROWIA LIPOLYTICA;

FUNGAL PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, FUNGAL; RAS PROTEINS; SIGNAL TRANSDUCTION; YARROWIA;

EID: 84899930774     PISSN: 15671356     EISSN: 15671364     Source Type: Journal    
DOI: 10.1111/1567-1364.12129     Document Type: Article

References (47)

1. Berman J & Sudbery PE (2002) Candida albicans: a molecular revolution built on lessons from budding yeast. Nat Rev Genet 3: 918-930.
2. Bhattacharya S, Chen L, Broach JR & Powers S (1995) Ras membrane targeting is essential for glucose signaling but not for viability in yeast. P Natl Acad Sci USA 92: 2984-2988.
3. Cervantes-Chavez JA & Ruiz-Herrera J (2006) STE11 disruption reveals the central role of a MAPK pathway in dimorphism and mating in Yarrowia lipolytica. FEMS Yeast Res 6: 801-815.
4. Cervantes-Chavez JA, Kronberg F, Passeron S & Ruiz-Herrera J (2009) Regulatory role of the PKA pathway in dimorphism and mating in Yarrowia lipolytica. Fungal Genet Biol 46: 390-399.
5. Cheng C-M, Li H, Gasman S, Juang J, Schiff R & Chang EC (2011) Compartmentalized Ras proteins transform NIH 3T3 cells with different efficiencies. Mol Cell Biol 31: 983-997.
6. Dong X, Mitchell DA, Lobo S, Zhao L, Bartels DJ & Deschenes RJ (2003) Palmitoylation and plasma membrane localization of Ras2p by a nonclassical trafficking pathway in Saccharomyces cerevisiae. Mol Cell Biol 23: 6574-6584.
7. Dujon B, Sherman D, Fischer G et al. (2004) Genome evolution in yeasts. Nature 430: 35-44.
8. Fang HM & Wang Y (2006) RA domain-mediated interaction of Cdc35 with Ras1 is essential for increasing cellular cAMP level for Candida albicans hyphal development. Mol Microbiol 61: 484-496.
9. Feng Q, Summers E, Guo B & Fink G (1999) Ras signaling is required for serum-induced hyphal differentiation in Candida albicans. J Bacteriol 181: 6339-6346.
10. Fickers P, Le Dall MT, Gaillardin C, Thonart P & Nicaud JM (2003) New disruption cassettes for rapid gene disruption and marker rescue in the yeast Yarrowia lipolytica. J Microbiol Methods 55: 727-737.
11. Fujiyama A & Tamanoi F (1990) RAS2 protein of Saccharomyces cerevisiae undergoes removal of methionine at N terminus and removal of three amino acids at C terminus. J Biol Chem 265: 3362-3368.
12. Fukui Y, Kozasa T, Kaziro Y, Takeda T & Yamamoto M (1986) Role of a ras homolog in the life cycle of Schizosaccharomyces pombe. Cell 44: 329-336.
13. Gietz RD, Schiestl RH, Willems AR & Woods RA (1995) Studies on the transformation of intact yeast cells by the LiAc/SS-DNA/PEG procedure. Yeast 11: 355-360.
14. Hancock JF (2003) Ras proteins: different signals from different locations. Nat Rev Mol Cell Biol 4: 373-384.
15. Hancock JF, Magee AI, Childs JE & Marshall CJ (1989) All ras proteins are polyisoprenylated but only some are palmitoylated. Cell 57: 1167-1177.
16. ras to the plasma membrane. Cell 63: 133-139.
17. Ho J & Bretscher A (2001) Ras regulates the polarity of the yeast actin cytoskeleton through the stress response pathway. Mol Biol Cell 12: 1541-1555.
18. 2-type zinc finger protein that promotes dimorphic transition in the yeast Yarrowia lipolytica. J Bacteriol 181: 3051-3057.
19. Jimenez-Bremont JF, Rodriguez-Hernandez AA & Rodriguez-Kessler M (2012) Development and dimorphism of the yeast Yarrowia lipolytica. Dimorphic Fungi: Their Importance as Models for Differentiation and Fungal Pathogenesis, Vol. 1 (Ruiz-Herrera J, ed.), pp. 58-66. Bentham Science Publishers, Oak Park, IL.
20. Leberer E, Harcus D, Dignard D, Johnson L, Ushinsky S, Thomas DY & Schroppel K (2001) Ras links cellular morphogenesis to virulence by regulation of the MAP kinase and cAMP signaling pathways in the pathogenic fungus Candida albicans. Mol Microbiol 42: 673-687.
21. Lee N & Kronstad JW (2002) ras2 controls morphogenesis, pheromone response, and pathogenicity in the fungal pathogen Ustilago maydis. Eukaryot Cell 1: 954-966.
22. Lengeler KB, Davidson RC, D'souza C, Harashima T, Shen WC, Wang P, Pan X, Waugh M & Heitman J (2000) Signal transduction cascades regulating fungal development and virulence. Microbiol Mol Biol Rev 64: 746-785.
23. Malumbres M & Barbacid M (2003) RAS oncogenes: the first 30 years. Nat Rev Cancer 3: 459-465.
24. Marshall MS, Gibbs JB, Scolnick EM & Sigal IS (1987) Regulatory function of the Saccharomyces cerevisiae RAS C-terminus. Mol Cell Biol 7: 2309-2315.
25. Masuda T, Kariya K, Shinkai M, Okada T & Kataoka T (1995) Protein kinase Byr2 is a target of Ras1 in the fission yeast Schizosaccharomyces pombe. J Biol Chem 270: 1979-1982.
26. Moodie SA, Willumsen BM, Weber MJ & Wolfman A (1993) Complexes of Ras.GTP with Raf-1 and mitogen-activated protein kinase kinase. Science 260: 1658-1661.
27. Mor A & Philips MR (2006) Compartmentalized Ras/MAPK signaling. Annu Rev Immunol 24: 771-800.
28. Morin M, Monteoliva L, Insenser M, Gil C & Dominguez A (2007) Proteomic analysis reveals metabolic changes during yeast to hypha transition in Yarrowia lipolytica. J Mass Spectrom 42: 1453-1462.
29. Mösch HU, Roberts RL & Fink GR (1996) Ras2 signals via the Cdc42/Ste20/mitogen-activated protein kinase module to induce filamentous growth in Saccharomyces cerevisiae. P Natl Acad Sci USA 93: 5352-5356.
30. Muller P, Katzenberger JD, Loubradou G & Kahmann R (2003) Guanyl nucleotide exchange factor Sql2 and Ras2 regulate filamentous growth in Ustilago maydis. Eukaryot Cell 2: 609-617.
31. Nadin-Davis SA, Nasim A & Beach D (1986) Involvement of ras in sexual differentiation but not in growth control in fission yeast. EMBO J 5: 2963-2971.
32. Nichols CB, Ferreyra J, Ballou E & Alspaugh JA (2009) Subcellular localization directs signaling specificity of the Cryptococcus neoformans Ras1 protein. Eukaryot Cell 8: 181-189.
33. Onken B, Wiener H, Philips MR & Chang EC (2006) Compartmentalized signaling of Ras in fission yeast. P Natl Acad Sci USA 103: 9045-9050.
34. Palecek SP, Parikh AS & Kron SJ (2002) Sensing, signaling and integrating physical processes during Saccharomyces cerevisiae invasive and filamentous growth. Microbiology 148: 893-907.
35. Piispanen AE, Bonnefoi O, Carden S, Deveau A, Bassilana M & Hogan DA (2011) Roles of Ras1 membrane localization during Candida albicans hyphal growth and farnesol response. Eukaryot Cell 10: 1473-1484.
36. Richard M, Quijano RR, Bezzate S, Bordon-Pallier F & Gaillardin C (2001) Tagging morphogenetic genes by insertional mutagenesis in the yeast Yarrowia lipolytica. J Bacteriol 183: 3098-3107.
37. Robertson LS & Fink GR (1998) The three yeast A kinases have specific signaling functions in pseudohyphal growth. P Natl Acad Sci USA 95: 13783-13787.
38. Ruiz-Herrera J & Sentandreu R (2002) Different effectors of dimorphism in Yarrowia lipolytica. Arch Microbiol 178: 477-483.
39. Stanhill A, Schick N & Engelberg D (1999) The yeast ras/cyclic AMP pathway induces invasive growth by suppressing the cellular stress response. Mol Cell Biol 19: 7529-7538.
40. Takai Y, Sasaki T & Matozaki T (2001) Small GTP-binding proteins. Physiol Rev 81: 153-208.
41. Uno I, Mitsuzawa H, Matsumoto K, Tanaka K, Oshima T & Ishikawa T (1985) Reconstitution of the GTP-dependent adenylate cyclase from products of the yeast CYR1 and RAS2 genes in Escherichia coli. P Natl Acad Sci USA 82: 7855-7859.
42. Waugh MS, Nichols CB, DeCesare CM, Cox GM, Heitman J & Alspaugh JA (2002) Ras1 and Ras2 contribute shared and unique roles in physiology and virulence of Cryptococcus neoformans. Microbiology 148: 191-201.
43. Weeks G & Spiegelman GB (2003) Roles played by Ras subfamily proteins in the cell and developmental biology of microorganisms. Cell Signal 15: 901-909.
44. Wolfe KH & Shields DC (1997) Molecular evidence for an ancient duplication of the entire yeast genome. Nature 387: 708-713.
45. Zhang J, Zhang Y, Zhong Y, Qu Y & Wang T (2012) Ras GTPases modulate morphogenesis, sporulation and cellulase gene expression in the cellulolytic fungus Trichoderma reesei. PLoS ONE 7: e48786.
46. Zhao X-F, Li M, Li Y-Q, Chen X-D & Gao X-D (2013) The TEA/ATTS transcription factor YlTec1p represses the yeast-to-hypha transition in the dimorphic yeast Yarrowia lipolytica. FEMS Yeast Res 13: 50-61.
47. Zhu Y, Fang H-M, Wang Y-M, Zeng G-S, Zheng X-D & Wang Y (2009) Ras1 and Ras2 play antagonistic roles in regulating cellular cAMP level, stationary-phase entry and stress response in Candida albicans. Mol Microbiol 74: 862-875.