The MARVEL domain protein Nce102 regulates actin organization and invasive growth of Candida albicans

mBio

Volumn 4, Issue 6, 2013, Pages

  Douglas, Lois M ^a   Wang, Hong X ^a   Konopka, James B ^a  

^a STONY BROOK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; AGAR; BNI1 PROTEIN; CARRIER PROTEIN; MARVEL DOMAIN CONTAINING PROTEIN; NCE102 PROTEIN; PHALLOIDIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANDIDA ALBICANS; CANDIDIASIS; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENVIRONMENTAL FACTOR; FUNGAL VIRULENCE; FUNGUS GROWTH; FUNGUS HYPHAE; FUNGUS TRANSMISSION; GENE DELETION; MORPHOGENESIS; MOUSE; NONHUMAN; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; ANIMAL; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; PATHOLOGY; VIRULENCE;

ACTINS; ANIMALS; CANDIDA ALBICANS; CANDIDIASIS; GENE DELETION; HYPHAE; MARVEL DOMAIN-CONTAINING PROTEINS; MICE; VIRULENCE;

EID: 84891598101     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00723-13     Document Type: Article

References (64)

1. Heitman J, Filler SG, Edwards JEJ, Mitchell AP. 2006. Molecular principles of fungal pathogenesis. ASM Press, Washington, DC.
2. Odds FC. 1988. Candida and candidosis. Bailliere Tindall, Philadelphia, PA.
3. Pfaller MA, Diekema DJ. 2010. Epidemiology of invasive mycoses in North America. Crit. Rev. Microbiol. 36:1-53.
4. Sudbery PE. 2011. Growth of Candida albicans hyphae. Nat. Rev. Micro biol. 9:737-748.
5. Odds FC, Brown AJ, Gow NA. 2003. Antifungal agents: mechanisms of action. Trends Microbiol. 11:272-279.
6. Malinsky J, Opekarová M, Tanner W. 2010. The lateral compartmentation of the yeast plasma membrane. Yeast 27:473-478.
7. Olivera-Couto A, Aguilar PS. 2012. Eisosomes and plasma membrane organization. Mol. Genet. Genomics 287:607-620.
8. Douglas LM, Wang HX, Li L, Konopka JB. 2011. Membrane compartment occupied by Can1 (MCC) and eisosome subdomains of the fungal plasma Membrane. Membranes (Basel) 1:394-411.
9. Malínská K, Malínský J, Opekarová M, Tanner W. 2003. Visualization of protein compartmentation within the plasma membrane of living yeast cells. Mol. Biol. Cell 14:4427-4436.
10. Malinska K, Malinsky J, Opekarova M, Tanner W. 2004. Distribution of Can1p into stable domains reflects lateral protein segregation within the plasma membrane of living S. cerevisiae cells. J. Cell Sci. 117:6031-6041.
11. Strádalová V, Stahlschmidt W, Grossmann G, Blazíková M, Rachel R, Tanner W, Malinsky J. 2009. Furrow-like invaginations of the yeast plasma membrane correspond to membrane compartment of Can1. J. Cell Sci. 122:2887-2894.
12. Young ME, Karpova TS, Brügger B, Moschenross DM, Wang GK, Schneiter R, Wieland FT, Cooper JA. 2002. The Sur7p family defines novel cortical domains in Saccharomyces cerevisiae, affects sphingolipid metabolism, and is involved in sporulation. Mol. Cell. Biol. 22:927-934.
13. Grossmann G, Malinsky J, Stahlschmidt W, Loibl M, Weig-Meckl I, Frommer WB, Opekarová M, Tanner W. 2008. Plasma membrane mi November/December 2013 Volume 4 Issue 6 e00723-13 crodomains regulate turnover of transport proteins in yeast. J. Cell Biol. 183:1075-1088.
14. Walther TC, Brickner JH, Aguilar PS, Bernales S, Pantoja C, Walter P. 2006. Eisosomes mark static sites of endocytosis. Nature 439:998-1003.
15. Olivera-Couto A, Graña M, Harispe L, Aguilar PS. 2011. The eisosome core is composed of BAR domain proteins. Mol. Biol. Cell 22:2360-2372.
16. Ziółkowska NE, Karotki L, Rehman M, Huiskonen JT, Walther TC. 2011. Eisosome-driven plasma membrane organization is mediated by BAR domains. Nat. Struct. Mol. Biol. 18:854-856.
17. Walther TC, Aguilar PS, Fröhlich F, Chu F, Moreira K, Burlingame AL, Walter P. 2007. Pkh-kinases control eisosome assembly and organization. EMBO J. 26:4946-4955.
18. Luo G, Gruhler A, Liu Y, Jensen ON, Dickson RC. 2008. The sphingolipid long-chain base-Pkh1/2-Ypk1/2 signaling pathway regulates eisosome assembly and turnover. J. Biol. Chem. 283:10433-10444.
19. Berchtold D, Walther TC. 2009. TORC2 plasma membrane localization is essential for cell viability and restricted to a distinct domain. Mol. Biol. Cell 20:1565-1575.
20. Spira F, Mueller NS, Beck G, von Olshausen P, Beig J, Wedlich-Söldner R. 2012. Patchwork organization of the yeast plasma membrane into numerous coexisting domains. Nat. Cell Biol. 14:640-648.
21. Alvarez FJ, Douglas LM, Rosebrock A, Konopka JB. 2008. The Sur7 protein regulates plasma membrane organization and prevents intracellular cell wall growth in Candida albicans. Mol. Biol. Cell 19:5214-5225.
22. Wang HX, Douglas LM, Aimanianda V, Latgé JP, Konopka JB. 2011. The Candida albicans Sur7 protein is needed for proper synthesis of the fibrillar component of the cell wall that confers strength. Eukaryot. Cell 10:72-80.
23. Douglas LM, Wang HX, Keppler-Ross S, Dean N, Konopka JB. 2012. Sur7 promotes plasma membrane organization and is needed for resistance to stressful conditions and to the invasive growth and virulence of Candida albicans. mBio 3(1):e00254-11. doi:10.1128/mBio.00254-11.
24. Vernay A, Schaub S, Guillas I, Bassilana M, Arkowitz RA. 2012. A steep phosphoinositide bis-phosphate gradient forms during fungal filamentous growth. J. Cell Biol. 198:711-730.
25. Martin SW, Konopka JB. 2004. Lipid raft polarization contributes to hyphal growth in Candida albicans. Eukaryot. Cell 3:675-684.
26. Loibl M, Grossmann G, Stradalova V, Klingl A, Rachel R, Tanner W, Malinsky J, Opekarová M. 2010. C terminus of Nce102 determines the structure and function of microdomains in the Saccharomyces cerevisiae plasma membrane. Eukaryot. Cell 9:1184-1192.
27. Fröhlich F, Moreira K, Aguilar PS, Hubner NC, Mann M, Walter P, Walther TC. 2009. A genome-wide screen for genes affecting eisosomes reveals Nce102 function in sphingolipid signaling. J. Cell Biol. 185: 1227-1242.
28. Seger S, Rischatsch R, Philippsen P. 2011. Formation and stability of eisosomes in the filamentous fungus Ashbya gossypii. J. Cell Sci. 124: 1629-1634.
29. Sánchez-Pulido L, Martín-Belmonte F, Valencia A, Alonso MA. 2002.MARVEL: a conserved domain involved in membrane apposition events. Trends Biochem. Sci. 27:599-601.
30. Iatropoulos P, Gardella R, Valsecchi P, Magri C, Ratti C, Podavini D, Rossi G, Gennarelli M, Sacchetti E, Barlati S. 2009. Association study and mutational screening of SYNGR1 as a candidate susceptibility gene for schizophrenia. Psychiatr. Genet. 19:237-243.
31. Leblanc MA, Penney LS, Gaston D, Shi Y, Aberg E, Nightingale M, Jiang H, Gillett RM, Fahiminiya S, Macgillivray C, Wood EP, Acott PD, Khan MN, Samuels ME, Majewski J, Orr A, McMaster CR, Bedard K. 2013. A novel rearrangement of occludin causes brain calcification and renal dysfunction. Genet. Hum. 132:1223-1234.
32. Pérez JC, Kumamoto CA, Johnson AD. 2013. Candida albicans com-mensalism and pathogenicity are intertwined traits directed by a tightlyknit transcriptional regulatory circuit. PLoS Biol. 11:e1001510. doi:10.1371/journal.pbio.1001510.
33. Warenda AJ, Kauffman S, Sherrill TP, Becker JM, Konopka JB. 2003. Candida albicans septin mutants are defective for invasive growth and virulence. Infect. Immun. 71:4045-4051.
34. Zucchi PC, Davis TR, Kumamoto CA. 2010. A candida albicans cell wall-linked protein promotes invasive filamentation into semi-solid medium. Mol. Microbiol. 76:733-748.
35. Kumamoto CA. 2005. A contact-activated kinase signals Candida albicans invasive growth and biofilm development. Proc. Natl. Acad. Sci. U. S. A. 102:5576-5581.
36. Navarro-Garcia F, Alonso-Monge R, Rico H, Pla J, Sentandreu R, Nombela C. 1998. A role for the MAP kinase gene MKC1 in cell wall construction and morphological transitions in Candida albicans. Microbiology 144:411-424.
37. Liu H, Köhler J, Fink GR. 1994. Suppression of hyphal formation in Candida albicans by mutation of a STE12 homolog. Science 266: 1723-1726.
38. Zhang X, Lester RL, Dickson RC. 2004. Pil1p and Lsp1p negatively regulate the 3-phosphoinositide-dependent protein kinase-like kinase Pkh1p and downstream signaling pathways Pkc1p and Ypk1p. J. Biol. Chem. 279:22030-22038.
39. Casamayor A, Torrance PD, Kobayashi T, Thorner J, Alessi DR. 1999. Functional counterparts of mammalian protein kinases PDK1 and SGK in budding yeast. Curr. Biol. 9:186-197.
40. Hope H, Schmauch C, Arkowitz RA, Bassilana M. 2010. The Candida albicans ELMO homologue functions together with Rac1 and Dck1, upstream of the MAP kinase Cek1, in invasive filamentous growth. Mol. Microbiol. 76:1572-1590.
41. Zou H, Fang HM, Zhu Y, Wang Y. 2010. Candida albicans Cyr1, Cap1and G-actin form a sensor/effector apparatus for activating cAMP synthesis in hyphal growth. Mol. Microbiol. 75:579-591.
42. Wolyniak MJ, Sundstrom P. 2007. Role of actin cytoskeletal dynamics in activation of the cyclic AMP pathway and HWP1 gene expression in Candida albicans. Eukaryot. Cell 6:1824-1840.
43. Martin R, Walther A, Wendland J. 2005. Ras1-induced hyphal development in Candida albicans requires the formin Bni1. Eukaryot. Cell 4:1712-1724.
44. Li CR, Wang YM, De Zheng X, Liang HY, Tang JC, Wang Y. 2005. The formin family protein CaBni1p has a role in cell polarity control during both yeast and hyphal growth in Candida albicans. J. Cell Sci. 118: 2637-2648.
45. Riedl J, Crevenna AH, Kessenbrock K, Yu JH, Neukirchen D, Bista M, Bradke F, Jenne D, Holak TA, Werb Z, Sixt M, Wedlich-Soldner R. 2008. Lifeact: a versatile marker to visualize F-actin. Nat. Methods 5:605-607.
46. Lionakis MS, Lim JK, Lee CC, Murphy PM. 2011. Organ-specific innate immune responses in a mouse model of invasive candidiasis. J. Innate Immun. 3:180-199.
47. Hazan I, Liu H. 2002. Hyphal tip-associated localization of Cdc42 is F-actin dependent in Candida albicans. Eukaryot. Cell 1:856-864.
48. Douglas LM, Martin SW, Konopka JB. 2009. BAR domain proteins Rvs161 and Rvs167 contribute to Candida albicans endocytosis, morphogenesis, and virulence. I nfect. Immun. 77:4150-4160.
49. Epp E, Nazarova E, Regan H, Douglas LM, Konopka JB, Vogel J, Whiteway M. 2013. Clathrin and Arp2/3-independent endocytosis in the fungal pathogen Candida albicans. mBio 4(5): e00476-13. doi:10.1128/ mBio.00476-13.
50. Foster HA, Cui M, Naveenathayalan A, Unden H, Schwanbeck R, Höfken T. 2013. The zinc cluster protein Sut1 contributes to filamentation in Saccharomyces cerevisiae. Eukaryot. Cell 12:244-253.
51. Kabeche R, Baldissard S, Hammond J, Howard L, Moseley JB. 2011. The filament-forming protein Pil1 assembles linear eisosomes in fission yeast. Mol. Biol. Cell 22:4059-4067.
52. Khalaj V, Azizi M, Enayati S, Khorasanizadeh D, Ardakani EM. 2012. NCE102 homologue in Aspergillus fumigatus is required for normal sporulation, not hyphal growth or pathogenesis. FEMS Microbiol. Lett. 329: 138-145.
53. Grossmann G, Opekarová M, Malinsky J, Weig-Meckl I, Tanner W. 2007. Membrane potential governs lateral segregation of plasma membrane proteins and lipids in yeast. EMBO J. 26:1-8.
54. Saitou M, Furuse M, Sasaki H, Schulzke JD, Fromm M, Takano H, Noda T, Tsukita S. 2000. Complex phenotype of mice lacking occludin, a component of tight junction strands. Mol. Biol. Cell 11:4131-4142.
55. Cummins PM. 2012. Occludin: one protein, many forms. Mol. Cell. Biol. 32:242-250.
56. Janz R, Südhof TC, Hammer RE, Unni V, Siegelbaum SA, Bolshakov VY. 1999. Essential roles in synaptic plasticity for synaptogyrin I and synaptophysin I. Neuron 24:687-700.
57. Zhou G, Liang FX, Romih R, Wang Z, Liao Y, Ghiso J, Luque-Garcia JL, Neubert TA, Kreibich G, Alonso MA, Schaeren-Wiemers N, Sun TT. 2012. MAL facilitates the incorporation of exocytic uroplakin-delivering vesicles into the apical membrane of urothelial umbrella cells. Mol. Biol. Cell 23:1354-1366.
58. Kuwabara H, Kokai Y, Kojima T, Takakuwa R, Mori M, Sawada N. 2001. Occludin regulates actin cytoskeleton in endothelial cells. Cell Struct. Funct. 26:109-116.
59. Sala-Valdes M, Ailane N, Greco C, Rubinstein E, Boucheix C. 2012. Targeting tetraspanins in cancer. Expert Opin. Ther. Targets. 16:985-997.
60. Suzuki H, Kondoh M, Takahashi A, Yagi K. 2012. Proof of concept for claudin-targeted drug development. Ann. N. Y. Acad. Sci. 1258:65-70.
61. Wilson RB, Davis D, Mitchell AP. 1999. Rapid hypothesis testing with Candida albicans through gene disruption with short homology regions. J. Bacteriol. 181:1868-1874.
62. Reuss O, Vik A, Kolter R, Morschhäuser J. 2004. The SAT1 flipper, an optimized tool for gene disruption in Candida albicans. Gene 341: 119-127.
63. Zhang C, Konopka JB. 2010. A photostable green fluorescent protein variant for analysis of protein localization in Candida albicans. Eukaryot. Cell 9:224-226.
64. Keppler-Ross S, Noffz C, Dean N. 2008. A new purple fluorescent color marker for genetic studies in Saccharomyces cerevisiae and Candida albicans. Genetics 179:705-710.