Membrane organization and cell fusion during mating in fission yeast requires multipass membrane protein Prm1

Genetics

Volumn 196, Issue 4, 2014, Pages 1059-1076

  Curto, M Ángeles ^a   Sharifmoghadam, Mohammad Reza ^b,c   Calpena, Eduardo ^a   De León, Nagore ^a   Hoya, Marta ^a   Doncel, Cristina ^a   Leatherwood, Janet ^b   Valdivieso, M Henar ^a  

^a Instituto de Biología Funcional y Genómica and Departamento de Microbiología y Genética   (Spain)

^b STONY BROOK UNIVERSITY   (United States)

^c FERDOWSI UNIVERSITY OF MASHHAD   (Iran)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CLAUDIN; MEMBRANE PROTEIN; PHOSPHATIDYLSERINE; PRM1 PROTEIN; UNCLASSIFIED DRUG; DEPSIPEPTIDE; DNI1 PROTEIN, S POMBE; MICONAZOLE; MONOUNSATURATED FATTY ACID; PAPUAMIDE B; PRM1 PROTEIN, S POMBE; SCHIZOSACCHAROMYCES POMBE PROTEIN; THERMOZYMOCIDIN;

ARTICLE; CELL CONTACT; CELL FUSION; CELL INTERACTION; CELL MEMBRANE; CELL WALL; CELLULAR DISTRIBUTION; CONTROLLED STUDY; FUNGAL STRAIN; GENE; LIPOGENESIS; MATING; MEMBRANE STRUCTURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN MODIFICATION; SCHIZOSACCHAROMYCES POMBE; WILD TYPE; ZYGOTE; BIOLOGICAL MODEL; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; SCHIZOSACCHAROMYCES; ULTRASTRUCTURE;

CELL MEMBRANE; CELL WALL; DEPSIPEPTIDES; FATTY ACIDS, MONOUNSATURATED; GENE EXPRESSION REGULATION, FUNGAL; MEMBRANE PROTEINS; MICONAZOLE; MODELS, BIOLOGICAL; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS;

EID: 84901311439     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.113.159558     Document Type: Article

References (56)

1. Aguilar, P. S., A. Engel, and P. Walter, 2007 The plasma membrane proteins Prm1 and Fig1 ascertain fidelity of membrane fusion during yeast mating. Mol. Biol. Cell 18: 547-556.
2. Aguilar, P. S., M. G. Heiman, T. C. Walther, A. Engel, D. Schwudke et al., 2010 Structure of sterol aliphatic chains affects yeast cell shape and cell fusion during mating. Proc. Natl. Acad. Sci. USA 107: 4170-4175.
3. Alvarez, F. J., L. M. Douglas, A. Rosebrock, and J. B. Konopka, 2008 The Sur7 protein regulates plasma membrane organization and prevents intracellular cell wall growth in Candida albicans. Mol. Biol. Cell 19: 5214-5225.
4. Arcangioli, B., and G. Thon, 2004 Mating-type cassettes: structure, switchin and silencing, pp. 9-147 in The Molecular Biology of Schizosaccharomyces pombe, edited by R. Egel. Springer, Heidelberg, Germany.
5. Bagnat, M., and K. Simons, 2002 Cell surface polarization during yeast mating. Proc. Natl. Acad. Sci. USA 99: 14183-14188.
6. Bähler, J., J. Q. Wu, M. S. Longtine, N. G. Shah, A. McKenzie, 3rd, et al., 1998 Heterologous modules for efficient and versatile PCR-based gene targeting in Schizosaccharomyces pombe. Yeast 14: 943-951.
7. Calleja, G., Y. Bong, and B. Johnson, 1977 Fusion and erosion of cell walls during conjugation in the fission yeast Schizosaccharomyces pombe. J. Cell Sci. 25: 139-155.
8. +. Yeast 23: 375-388.
9. Chamoun-Emanuelli, A. M., E. I. Pecheur, R. L. Simeon, D. Huang, P. S. Cremer et al., 2013 Phenothiazines inhibit hepatitis C virus entry, likely by increasing the fluidity of cholesterol-rich membranes. Antimicrob. Agents Chemother. 57: 2571-2581.
10. Clemente-Ramos, J. A., R. Martin-Garcia, M. R. Sharifmoghadam, M. Konomi, M. Osumi et al., 2009 The tetraspan protein Dni1p is required for correct membrane organization and cell wall remodelling during mating in Schizosaccharomyces pombe. Mol. Microbiol. 73: 695-709.
11. Davey, J., 1998 Fusion of a fission yeast. Yeast 14: 1529-1566.
12. Douglas, L. M., H. X. Wang, S. Keppler-Ross, N. Dean, and J. B. Konopka, 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.
13. Doyle, A., R. Martin-Garcia, A. T. Coulton, S. Bagley, and D. P. Mulvihill, 2009 Fission yeast Myo51 is a meiotic spindle pole body component with discrete roles during cell fusion and spore formation. J. Cell Sci. 122: 4330-4340.
14. Drabikowski, W., E. Lagwinska, and M. G. Sarzala, 1973 Filipin as a fluorescent probe for the location of cholesterol in the membranes of fragmented sarcoplasmic reticulum. Biochim. Biophys. Acta 291: 61-70.
15. Engel, A., P. S. Aguilar, and P. Walter, 2010 The yeast cell fusion protein Prm1p requires covalent dimerization to promote membrane fusion. PLoS ONE 5: e10593.
16. Erdman, S., L. Lin, M. Malczynski, and M. Snyder, 1998 Pheromoneregulated genes required for yeast mating differentiation. J. Cell Biol. 140: 461-483.
17. Fleissner, A., S. Diamond, and N. L. Glass, 2009 The Saccharomyces cerevisiae PRM1 homolog in Neurospora crassa is involved in vegetative and sexual cell fusion events but also has postfertilization functions. Genetics 181: 497-510.
18. Gordon, L. M., R. D. Sauerheber, and J. A. Esgate, 1978 Spin label studies on rat liver and heart plasma membranes: effects of temperature, calcium, and lanthanum on membrane fluidity. J. Supramol. Struct. 9: 299-326.
19. Grote, E., 2010 Secretion is required for late events in the cellfusion pathway of mating yeast. J. Cell Sci. 123: 1902-1912.
20. Heiman, M. G., and P. Walter, 2000 Prm1p, a pheromone-regulated multispanning membrane protein, facilitates plasma membrane fusion during yeast mating. J. Cell Biol. 151: 719-730.
21. Heiman, M. G., A. Engel, and P. Walter, 2007 The Golgi-resident protease Kex2 acts in conjunction with Prm1 to facilitate cell fusion during yeast mating. J. Cell Biol. 176: 209-222.
22. Jin, H., C. Carlile, S. Nolan, and E. Grote, 2004 Prm1 prevents contact-dependent lysis of yeast mating pairs. Eukaryot. Cell 3: 1664-1673.
23. Jin, H., J. M. McCaffery, and E. Grote, 2008 Ergosterol promotes pheromone signaling and plasma membrane fusion in mating yeast. J. Cell Biol. 180: 813-826.
24. Kozlov, M. M., H. T. McMahon, and L. V. Chernomordik, 2010 Protein-driven membrane stresses in fusion and fission. Trends Biochem. Sci. 35: 699-706.
25. Kurahashi, H., Y. Imai, and M. Yamamoto, 2002 Tropomyosin is required for the cell fusion process during conjugation in fission yeast. Genes Cells 7: 375-384.
26. Marki, F., E. Hanni, A. Fredenhagen, and J. Van Oostrum, 1991 Mode of action of the lanthionine-containing peptide antibiotics duramycin, duramycin B and C, and cinnamycin as indirect inhibitors of phospholipase A2. Biochem. Pharmacol. 42: 2027-2035.
27. Marks, J., and J. S. Hyams, 1985 Localisation of F-actin through the cell division cycle of Schizosaccharomyces pombe. Eur. J. Cell Biol. 39: 27-32.
28. Marsh, D., 2008 Protein modulation of lipids, and vice-versa, in membranes. Biochim. Biophys. Acta 1778: 1545-1575.
29. Mata, J., and J. Bahler, 2006 Global roles of Ste11p, cell type, and pheromone in the control of gene expression during early sexual differentiation in fission yeast. Proc. Natl. Acad. Sci. USA 103: 15517-15522.
30. Mata, J., R. Lyne, G. Burns, and J. Bähler, 2002 The transcriptional program of meiosis and sporulation in fission yeast. Nat. Genet. 32: 143-147.
31. Merlini, L., O. Dudin, and S. G. Martin, 2013 Mate and fuse: how yeast cells do it. Open Biol. 3: 130008.
32. Moreno, S., A. Klar, and P. Nurse, 1991 Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol. 194: 795-823.
33. Muller, E. M., N. A. Mackin, S. E. Erdman, and K. W. Cunningham, 2003 Fig1p facilitates Ca2+ influx and cell fusion during mating of Saccharomyces cerevisiae. J. Biol. Chem. 278: 38461-38469.
34. Neiman, A. M., 1998 Prospore membrane formation defines a developmentally regulated branch of the secretory pathway in yeast. J. Cell. Biol. 140: 29-37.
35. Nielsen, O., 2004 Mating-type control and differentiation, pp. 281-296 in The Molecular Biology of Schizosaccharomyces pombe, edited by R. Egel. Springer, Heidelberg, Germany.
36. Norman, L. L., J. Brugues, K. Sengupta, P. Sens, and H. Aranda-Espinoza, 2010 Cell blebbing and membrane area homeostasis in spreading and retracting cells. Biophys. J. 99: 1726-1733.
37. Olmo, V. N., and E. Grote, 2010a Prm1 functions as a disulfidelinked complex in yeast mating. J. Biol. Chem. 285: 2274-2283.
38. Olmo, V. N., and E. Grote, 2010b Prm1 targeting to contact sites enhances fusion during mating in Saccharomyces cerevisiae. Eukaryot. Cell 9: 1538-1548.
39. Orr-Weaver, T. L., J. W. Szostak, and R. J. Rothstein, 1983 Genetic applications of yeast transformation with linear and gapped plasmids. Methods Enzymol. 101: 228-245.
40. Parsons, A. B., A. Lopez, I. E. Givoni, D. E. Williams, C. A. Gray et al., 2006 Exploring the mode-of-action of bioactive compounds by chemical-genetic profiling in yeast. Cell 126: 611-625.
41. Petersen, J., M. J. Heitz, and I. M. Hagan, 1998a Conjugation in S. pombe: identification of a microtubule-organising centre, a requirement for microtubules and a role for Mad2. Curr. Biol. 8: 963-966.
42. Petersen, J., O. Nielsen, R. Egel, and I. M. Hagan, 1998b F-actin distribution and function during sexual differentiation in Schizosaccharomyces pombe. J. Cell Sci. 111: 867-876.
43. Petersen, J., D. Weilguny, R. Egel, andO. Nielsen, 1995 Characterization of fus1 of Schizosaccharomyces pombe: a developmentally controlled function needed for conjugation. Mol. Cell. Biol. 15: 3697-3707.
44. Proszynski, T. J., R. Klemm, M. Bagnat, K. Gaus, and K. Simons, 2006 Plasma membrane polarization during mating in yeast cells. J. Cell Biol. 173: 861-866.
45. Sato, M., S. Dhut, and T. Toda, 2005 New drug-resistant cassettes for gene disruption and epitope tagging in Schizosaccharomyces pombe. Yeast 22: 583-591.
46. Sharifmoghadam, M. R., and M. H. Valdivieso, 2008 The Schizosaccharomyces pombe Map4 adhesin is a glycoprotein that can be extracted from the cell wall with alkali but not with beta-glucanases and requires the C-terminal DIPSY domain for function. Mol. Microbiol. 69: 1476-1490.
47. Sharifmoghadam, M. R., P. Bustos-Sanmamed, and M. H. Valdivieso, 2006 The fission yeast Map4 protein is a novel adhesin required for mating. FEBS Lett. 580: 4457-4462.
48. Sharifmoghadam, M. R., M. A. Curto, M. Hoya, N. De Leon, R. Martin-Garcia et al., 2012 The integrity of the cytokinesis machinery under stress conditions requires the glucan synthase Bgs1p and its regulator Cfh3p. PLoS ONE 7: e42726.
49. Sipiczki, M., 2000 Where does fission yeast sit on the tree of life? Genome Biol. 1(2). Reviews 1011.
50. cdc2 kinase. EMBO J. 16: 534.
51. Trueheart, J., J. D. Boeke, and G. R. Fink, 1987 Two genes required for cell fusion during yeast conjugation: evidence for a pheromone-induced surface protein. Mol. Cell. Biol. 7: 2316-2328.
52. Wachtler, V., S. Rajagopalan, and M. K. Balasubramanian, 2003 Sterol-rich plasma membrane domains in the fission yeast Schizosaccharomyces pombe. J. Cell Sci. 116: 867-874.
53. White, J. M., and M. D. Rose, 2001 Yeast mating: getting close to membrane merger. Curr. Biol. 11: R16-R20.
54. Yamamoto, M., 2004 Initiation of meiosis, pp. 297-310 in The Molecular Biology of Schizosaccharomyces pombe, edited by R. Egel. Springer, Heidelberg, Germany.
55. Yamamoto, M., Y. Imai, and Y. Watanabe, 1997 Mating and sporulation in Schizosaccharomyces pombe, pp. 1037-1106 in The Molecular and Cellular Biology of the Yeast Saccharomyces, edited by J. R. Pringle, J. R. Broach, and E. W. Jones. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
56. Yeung, T., G. E. Gilbert, J. Shi, J. Silvius, A. Kapus et al., 2008 Membrane phosphatidylserine regulates surface charge and protein localization. Science 319: 210-213.