Cellular morphogenesis under stress is influenced by the sphingolipid pathway gene ISC1 and DNA integrity checkpoint genes in saccharomyces cerevisiae

Genetics

Volumn 189, Issue 2, 2011, Pages 533-547

  Tripathi, Kaushlendra ^a   Matmati, Nabil ^a   Zheng, W Jim ^a   Hannun, Yusuf A ^a   Mohanty, Bidyut K ^a  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; CERAMIDE; CHECKPOINT KINASE 2; CSM3 PROTEIN; CYCLIN DEPENDENT KINASE 1; FUNGAL DNA; FUNGAL PROTEIN; HYDROXYUREA; ISC1 PROTEIN; MESYLIC ACID METHYL ESTER; MRC1 PROTEIN; PROTEIN RAD9; PROTEIN SWE1; REGULATOR PROTEIN; SPHINGOLIPID; TOF1 PROTEIN; UNCLASSIFIED DRUG;

ACTIN DEPOLYMERIZATION; ARTICLE; CELL CYCLE REGULATION; CELL STRESS; CONTROLLED STUDY; DEPOLYMERIZATION; DNA DAMAGE; FUNGAL CELL; FUNGAL CELL CULTURE; FUNGAL STRAIN; GENE DELETION; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE; YEAST;

ACTINS; BLOTTING, WESTERN; CDC28 PROTEIN KINASE, S CEREVISIAE; CELL CYCLE PROTEINS; CELL WALL; CHITIN; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; DNA-BINDING PROTEINS; HYDROXYUREA; METHYL METHANESULFONATE; MICROSCOPY, FLUORESCENCE; MUTAGENS; MUTATION; NUCLEIC ACID SYNTHESIS INHIBITORS; PROTEIN-TYROSINE KINASES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SPHINGOLIPIDS; TYPE C PHOSPHOLIPASES;

SACCHAROMYCES CEREVISIAE;

EID: 80053950193     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.111.132092     Document Type: Article

References (78)

1. Alcasabas, A. A., A. J. Osborn, J. Bachant, F. Hu, P. J. Werler et al., 2001 Mrc1 transduces signals of DNA replication stress to activate Rad53. Nat. Cell Biol. 3: 958-965.
2. Bando, M., Y. Katou, M. Komata, H. Tanaka, T. Itoh et al., 2009 Csm3, Tof1, and Mrc1 form a heterotrimeric mediator complex that associates with DNA replication forks. J. Biol. Chem. 284: 34355-34365.
3. Bharucha, N., J. Ma, C. J. Dobry, S. K. Lawson, Z. Yang et al., 2008 Analysis of the yeast kinome reveals a network of regulated protein localization during filamentous growth. Mol. Biol. Cell 19: 2708-2717.
4. Bidlingmaier, S., and M. Snyder, 2004 Regulation of polarized growth initiation and termination cycles by the polarisome and Cdc42 regulators. J. Cell Biol. 164: 207-218.
5. Branzei, D., and M. Foiani, 2007 Interplay of replication checkpoints and repair proteins at stalled replication forks. DNA Repair (Amst.) 6: 994-1003.
6. Cali, B. M., T. C. Doyle, D. Botstein, and G. R. Fink, 1998 Multiple functions for actin during filamentous growth of Saccharomyces cerevisiae. Mol. Biol. Cell 9: 1873-1889.
7. Calzada, A., B. Hodgson, M. Kanemaki, A. Bueno, and K. Labib, 2005 Molecular anatomy and regulation of a stable replisome at a paused eukaryotic DNA replication fork. Genes Dev. 19: 1905-1919.
8. Chang, M., M. Bellaoui, C. Boone, and G. W. Brown, 2002 A genome-wide screen for methyl methanesulfonate-sensitive mutants reveals genes required for S phase progression in the presence of DNA damage. Proc. Natl. Acad. Sci. USA 99: 16934-16939.
9. Cordon-Preciado, V., S. Ufano, and A. Bueno, 2006 Limiting amounts of budding yeast Rad53 S-phase checkpoint activity results in increased resistance to DNA alkylation damage. Nucleic Acids Res. 34: 5852-5862.
10. de Groot, P. W., C. Ruiz, C. R. Vazquez de Aldana, E. Duenas, V. J. Cid et al., 2001 A genomic approach for the identification and classification of genes involved in cell wall formation and its regulation in Saccharomyces cerevisiae. Comp. Funct. Genomics 2: 124-142.
11. Diani, L., C. Colombelli, B. T. Nachimuthu, R. Donnianni, P. Plevani et al., 2009 Saccharomyces CDK1 phosphorylates Rad53 kinase in metaphase, influencing cellular morphogenesis. J. Biol. Chem. 284: 32627-32634.
12. Enserink, J. M., M. B. Smolka, H. Zhou, and R. D. Kolodner, 2006 Checkpoint proteins control morphogenetic events during DNA replication stress in Saccharomyces cerevisiae. J. Cell Biol. 175: 729-741.
13. Enserink, J. M., H. Hombauer, M. E. Huang, and R. D. Kolodner, 2009 Cdc28/Cdk1 positively and negatively affects genome stability in S. cerevisiae. J. Cell Biol. 185: 423-437.
14. Feoktistova, A., P. Magnelli, C. Abeijon, P. Perez, R. L. Lester et al., 2001 Coordination between fission yeast glucan formation and growth requires a sphingolipase activity. Genetics 158: 1397-1411.
15. Fiedler, D., H. Braberg, M. Mehta, G. Chechik, G. Cagney et al., 2009 Functional organization of the S. cerevisiae phosphorylation network. Cell 136: 952-963.
16. Foss, E. J., 2001 Tof1p regulates DNA damage responses during S phase in Saccharomyces cerevisiae. Genetics 157: 567-577.
17. Futerman, A. H., and H. Riezman, 2005 The ins and outs of sphingolipid synthesis. Trends Cell Biol. 15: 312-318.
18. Gandhi, M., V. Achard, L. Blanchoin, and B. L. Goode, 2009 Coronin switches roles in actin disassembly depending on the nucleotide state of actin. Mol. Cell 34: 364-374.
19. Gimeno, C. J., P. O. Ljungdahl, C. A. Styles, and G. R. Fink, 1992 Unipolar cell divisions in the yeast S. cerevisiae lead to filamentous growth: regulation by starvation and RAS. Cell 68: 1077-1090.
20. Gueldener, U., J. Heinisch, G. J. Koehler, D. Voss, and J. H. Hegemann, 2002 A second set of loxP marker cassettes for Cre-mediated multiple gene knockouts in budding yeast. Nucleic Acids Res. 30: e23
21. Haarer, B., S. Viggiano, M. A. Hibbs, O. G. Troyanskaya, and D. C. Amberg, 2007 Modeling complex genetic interactions in a simple eukaryotic genome: actin displays a rich spectrum of complex haploinsufficiencies. Genes Dev. 21: 148-159.
22. Hanway, D., J. K. Chin, G. Xia, G. Oshiro, E. A. Winzeler et al., 2002 Previously uncharacterized genes in the UV-and MMSinduced DNA damage response in yeast. Proc. Natl. Acad. Sci. USA 99: 10605-10610.
23. Harvey, S. L., and D. R. Kellogg, 2003 Conservation of mechanisms controlling entry into mitosis: budding yeast wee1 delays entry into mitosis and is required for cell size control. Curr. Biol. 13: 264-275.
24. Imamura, H., K. Tanaka, T. Hihara, M. Umikawa, T. Kamei et al., 1997 Bni1p and Bnr1p: downstream targets of the Rho family small G-proteins which interact with profilin and regulate actin cytoskeleton in Saccharomyces cerevisiae. EMBO J. 16: 2745-2755.
25. Jiang, Y. W., and C. M. Kang, 2003 Induction of S. cerevisiae filamentous differentiation by slowed DNA synthesis involves Mec1, Rad53 and Swe1 checkpoint proteins. Mol. Biol. Cell 14: 5116-5124.
26. Katou, Y., Y. Kanoh, M. Bando, H. Noguchi, H. Tanaka et al., 2003 S-phase checkpoint proteins Tof1 and Mrc1 form a stable replication-pausing complex. Nature 424: 1078-1083.
27. Keaton, M. A., E. S. Bardes, A. R. Marquitz, C. D. Freel, T. R. Zyla et al., 2007 Differential susceptibility of yeast S and M phase CDK complexes to inhibitory tyrosine phosphorylation. Curr. Biol. 17: 1181-1189.
28. Kitagaki, H., L. A. Cowart, N. Matmati, D. Montefusco, J. Gandy et al., 2009 ISC1-dependent metabolic adaptation reveals an indispensable role for mitochondria in induction of nuclear genes during the diauxic shift in Saccharomyces cerevisiae. J. Biol. Chem. 284: 10818-10830.
29. Lee, K. S., S. Asano, J. E. Park, K. Sakchaisri, and R. L. Erikson, 2005 Monitoring the cell cycle by multi-kinase-dependent regulation of Swe1/Wee1 in budding yeast. Cell Cycle 4: 1346-1349.
30. Lengeler, K. B., R. C. Davidson, C. D'Souza, T. Harashima, W. C. Shen et al., 2000 Signal transduction cascades regulating fun-gal development and virulence. Microbiol. Mol. Biol. Rev. 64: 746-785.
31. Lew, D. J., 2003 The morphogenesis checkpoint: how yeast cells watch their figures. Curr. Opin. Cell Biol. 15: 648-653.
32. Lew, D. J., and S. I. Reed, 1995 Cell cycle control of morphogenesis in budding yeast. Curr. Opin. Genet. Dev. 5: 17-23.
33. Lin, M. C., B. J. Galletta, D. Sept, and J. A. Cooper, 2010 Overlapping and distinct functions for cofilin, coronin and Aip1 in actin dynamics in vivo. J. Cell Sci. 123: 1329-1342.
34. Liu, B., L. Larsson, A. Caballero, X. Hao, D. Oling et al., 2010 The polarisome is required for segregation and retrograde transport of protein aggregates. Cell 140: 257-267.
35. Liu, H., C. A. Styles, and G. R. Fink, 1993 Elements of the yeast pheromone response pathway required for filamentous growth of diploids. Science 262: 1741-1744.
36. Longtine, M. S., A. McKenzie III. D. J. Demarini, N. G. Shah, A. Wach et al., 1998 Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14: 953-961.
37. Lorenz, M. C., N. S. Cutler, and J. Heitman, 2000 Characterization of alcohol-induced filamentous growth in Saccharomyces cerevisiae. Mol. Biol. Cell 11: 183-199.
38. Matmati, N., and Y. A. Hannun, 2008 Thematic review series: sphingolipids. ISC1 (inositol phosphosphingolipid-phospholipase C), the yeast homologue of neutral sphingomyelinases. J. Lipid Res. 49: 922-928.
39. Matmati, N., H. Kitagaki, D. Montefusco, B. K. Mohanty, and Y. A. Hannun, 2009 Hydroxyurea sensitivity reveals a role for ISC1 in the regulation of G2/M. J. Biol. Chem. 284: 8241-8246.
40. Mayer, M. L., I. Pot, M. Chang, H. Xu, V. Aneliunas et al., 2004 Identification of protein complexes required for efficient sister chromatid cohesion. Mol. Biol. Cell 15: 1736-1745.
41. McMillan, J. N., R. A. Sia, and D. J. Lew, 1998 A morphogenesis checkpoint monitors the actin cytoskeleton in yeast. J. Cell Biol. 142: 1487-1499.
42. McMillan, J. N., R. A. Sia, E. S. Bardes, and D. J. Lew, 1999 Phosphorylation-independent inhibition of Cdc28p by the tyrosine kinase Swe1p in the morphogenesis checkpoint. Mol. Cell. Biol. 19: 5981-5990.
43. Milhas, D., C. J. Clarke, and Y. A. Hannun, 2010 Sphingomyelin metabolism at the plasma membrane: implications for bioactive sphingolipids. FEBS Lett. 584: 1887-1894.
44. Mohanty, B. K., N. K. Bairwa, and D. Bastia, 2006 The Tof1p-Csm3p protein complex counteracts the Rrm3p helicase to control replication termination of Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 103: 897-902.
45. Moseley, J. B., and B. L. Goode, 2006 The yeast actin cytoskeleton: from cellular function to biochemical mechanism. Microbiol. Mol. Biol. Rev. 70: 605-645.
46. Munn, A. L., B. J. Stevenson, M. I. Geli, and H. Riezman, 1995 end5, end6, and end7: Mutations that cause actin delocalization and block the internalization step of endocytosis in Saccharomyces cerevisiae. Mol. Biol. Cell 6: 1721-1742.
47. Palecek, S. P., A. S. Parikh, J. H. Huh, and S. J. Kron, 2002 Depression of Saccharomyces cerevisiae invasive growth on non-glucose carbon sources requires the Snf1 kinase. Mol. Microbiol. 45: 453-469.
48. Pan, X., and J. Heitman, 2002 Protein kinase A operates a molecular switch that governs yeast pseudohyphal differentiation. Mol. Cell. Biol. 22: 3981-3993.
49. Pan, X., T. Harashima, and J. Heitman, 2000 Signal transduction cascades regulating pseudohyphal differentiation of Saccharomyces cerevisiae. Curr. Opin. Microbiol. 3: 567-572.
50. Pan, X., P. Ye, D. S. Yuan, X. Wang, J. S. Bader et al., 2006 A DNA integrity network in the yeast Saccharomyces cerevisiae. Cell 124: 1069-1081.
51. Parsons, A. B., R. L. Brost, H. Ding, Z. Li, C. Zhang et al., 2004 Integration of chemical-genetic and genetic interaction data links bioactive compounds to cellular target pathways. Nat. Biotechnol. 22: 62-69.
52. Pruyne, D., and A. Bretscher, 2000a Polarization of cell growth in yeast. J. Cell Sci. 113(Pt. 4): 571-585.
53. Pruyne, D., and A. Bretscher, 2000b Polarization of cell growth in yeast. I. Establishment and maintenance of polarity states. J. Cell Sci. 113(Pt. 3): 365-375.
54. Pruyne, D., L. Gao, E. Bi, and A. Bretscher, 2004 Stable and dynamic axes of polarity use distinct formin isoforms in budding yeast. Mol. Biol. Cell 15: 4971-4989.
55. Putnam, C. D., E. J. Jaehnig, and R. D. Kolodner, 2009 Perspectives on the DNA damage and replication checkpoint responses in Saccharomyces cerevisiae. DNA Repair (Amst.) 8: 974-982.
56. Riezman, H., 2006 Organization and functions of sphingolipid biosynthesis in yeast. Biochem. Soc. Trans. 34: 367-369.
57. Roberts, R. L., and G. R. Fink, 1994 Elements of a single MAP kinase cascade in Saccharomyces cerevisiae mediate two developmental programs in the same cell type: mating and invasive growth. Genes Dev. 8: 2974-2985.
58. Rodal, A. A., O. Sokolova, D. B. Robins, K. M. Daugherty, S. Hippenmeyer et al., 2005 Conformational changes in the Arp2/3 complex leading to actin nucleation. Nat. Struct. Mol. Biol. 12: 26-31.
59. Roncero, C., 2002 The genetic complexity of chitin synthesis in fungi. Curr. Genet. 41: 367-378.
60. Sawai, H., Y. Okamoto, C. Luberto, C. Mao, A. Bielawska et al., 2000 Identification of ISC1 (YER019w) as inositol phosphosphingolipid phospholipase C in Saccharomyces cerevisiae. J. Biol. Chem. 275: 39793-39798.
61. Shi, Q. M., Y. M. Wang, X. D. Zheng, R. T. Lee, and Y. Wang, 2007 Critical role of DNA checkpoints in mediating genotoxic-stress-induced filamentous growth in Candida albicans. Mol. Biol. Cell 18: 815-826.
62. Sia, R. A., E. S. Bardes, and D. J. Lew, 1998 Control of Swe1p degradation by the morphogenesis checkpoint. EMBO J. 17: 6678-6688.
63. Slater, M. L., 1973 Effect of reversible inhibition of deoxyribonucleic acid synthesis on the yeast cell cycle. J. Bacteriol. 113: 263-270.
64. Smolka, M. B., S. H. Chen, P. S. Maddox, J. M. Enserink, C. P. Albuquerque et al., 2006 An FHA domain-mediated protein interaction network of Rad53 reveals its role in polarized cell growth. J. Cell Biol. 175: 743-753.
65. Szyjka, S. J., C. J. Viggiani, and O. M. Aparicio, 2005 Mrc1 is required for normal progression of replication forks throughout chromatin in S. cerevisiae. Mol. Cell 19: 691-697.
66. Tabuchi, M., A. Audhya, A. B. Parsons, C. Boone, and S. D. Emr, 2006 The phosphatidylinositol 4,5-biphosphate and TORC2 binding proteins Slm1 and Slm2 function in sphingolipid regulation. Mol. Cell. Biol. 26: 5861-5875.
67. Tanaka, H., Y. Katou, M. Yagura, K. Saitoh, T. Itoh et al., 2009 Ctf4 coordinates the progression of helicase and DNA polymerase alpha. Genes Cells 14: 807-820.
68. Tercero, J. A., and J. F. Diffley, 2001 Regulation of DNA replication fork progression through damaged DNA by the Mec1/Rad53 checkpoint. Nature 412: 553-557.
69. Tong, A. H., G. Lesage, G. D. Bader, H. Ding, H. Xu et al., 2004 Global mapping of the yeast genetic interaction network. Science 303: 808-813.
70. Tourriere, H., G. Versini, V. Cordon-Preciado, C. Alabert, and P. Pasero, 2005 Mrc1 and Tof1 promote replication fork progression and recovery independently of Rad53. Mol. Cell 19: 699-706.
71. Vaena de Avalos, S., Y. Okamoto, and Y. A. Hannun, 2004 Activation and localization of inositol phosphosphingolipid phospholipase C, Isc1p, to the mitochondria during growth of Saccharomyces cerevisiae. J. Biol. Chem. 279: 11537-11545.
72. Wang, Y., 2009 CDKs and the yeast-hyphal decision. Curr. Opin. Microbiol. 12: 644-649.
73. Ward, M. P., C. J. Gimeno, G. R. Fink, and S. Garrett, 1995 SOK2 may regulate cyclic AMP-dependent protein kinase-stimulated growth and pseudohyphal development by repressing transcription. Mol. Cell. Biol. 15: 6854-6863.
74. Weinert, T. A., and L. H. Hartwell, 1988 The RAD9 gene controls the cell cycle response to DNA damage in Saccharomyces cerevisiae. Science 241: 317-322.
75. Wertman, K. F., D. G. Drubin, and D. Botstein, 1992 Systematic mutational analysis of the yeast ACT1 gene. Genetics 132: 337-350.
76. Xu, H., C. Boone, and G. W. Brown, 2007 Genetic dissection of parallel sister-chromatid cohesion pathways. Genetics 176: 1417-1429.
77. Zanolari, B., S. Friant, K. Funato, C. Sutterlin, B. J. Stevenson et al., 2000 Sphingoid base synthesis requirement for endocytosis in Saccharomyces cerevisiae. EMBO J. 19: 2824-2833.
78. Zegerman, P., and J. F. Diffley, 2003 Lessons in how to hold a fork. Nat. Struct. Biol. 10: 778-779.