Synthetic Lethality between Gene Defects Affecting a Single Non-essential Molecular Pathway with Reversible Steps

PLoS Computational Biology

Volumn 9, Issue 4, 2013, Pages

  Zinovyev, Andrei ^a,b,c   Kuperstein, Inna ^a,b,c   Barillot, Emmanuel ^a,b,c   Heyer, Wolf Dietrich ^d  

^a INSTITUT CURIE   (France)

^b INSERM U900   (France)

^c PSL RESEARCH UNIVERSITY   (France)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENES;

GENE FUNCTION; GENETIC INTERACTION; GENOME WIDE ANALYSIS; KINETIC TRAPPING; MECHANISTICS; MOLECULAR MECHANISM; MOLECULAR PATHWAYS; NON ESSENTIAL; SYSTEMATIC ANALYSIS; SYSTEMS BIOLOGY;

YEAST;

ARTICLE; CATALYSIS; COMPUTER SIMULATION; GENE FUNCTION; GENE IDENTIFICATION; GENE INTERACTION; GENE MUTATION; GENE OVEREXPRESSION; HOMOLOGOUS RECOMBINATION; LETHALITY; MATHEMATICAL MODEL; MUTATIONAL ANALYSIS; RECOMBINATION REPAIR; SIGNAL TRANSDUCTION; SYNTHETIC LETHALITY; TRANSPORT KINETICS;

EID: 84876908617     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1003016     Document Type: Article

References (68)

1. Dobzhansky T, (1946) Genetics of natural populations. XIII. Recombination and variability in populations of Drosophila pseudoobscura. Genetics 31: 269-290.
2. Collins SR, Miller KM, Maas NL, Roguev A, Fillingham J, et al. (2007) Functional dissection of protein complexes involved in yeast chromosome biology using a genetic interaction map. Nature 446: 806-810.
3. Bandyopadhyay S, Mehta M, Kuo D, Sung MK, Chuang R, et al. (2010) Rewiring of Genetic Networks in Response to DNA Damage. Science 330: 1385-1389.
4. Tong AHY, Evangelista M, Parsons AB, Xu H, Bader GD, et al. (2001) Systematic genetic analysis with ordered arrays of yeast deletion mutants. Science 294: 2363-2368.
5. Costanzo M, Baryshnikova A, Bellay J, Kim Y, Spear ED, et al. (2010) The genetic landscape of a cell. Science 327: 425-431.
6. Boone C, Bussey H, Andrews BJ, (2007) Exploring genetic interactions and networks with yeast. Nature Reviews Genetics 8: 437-449.
7. Kroll ES, Hyland KM, Hieter P, Li JJ, (1996) Establishing genetic interactions by a synthetic dosage lethality phenotype. Genetics 143: 95-102.
8. Silva JM, Marran K, Parker JS, Silva J, Golding M, et al. (2008) Profiling essential genes in human mammary cells by multiplex RNAi screening. Science 319: 617-620.
9. Iorns E, Lord CJ, Turner N, Ashworth A, (2007) Utilizing RNA interference to enhance cancer drug discovery. Nature Reviews Drug Discovery 6: 556-568.
10. Hartwell LH, Szankasi P, Roberts CJ, Murray AW, Friend SH, (1997) Integrating genetic approaches into the discovery of anticancer drugs. Science 278: 1064-1068.
11. Farmer H, McCabe N, Lord CJ, Tutt ANJ, Johnson DA, et al. (2005) Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature 434: 917-921.
12. Bryant HE, Schultz N, Thomas HD, Parker KM, Flower D, et al. (2005) Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase. Nature 434: 913-917.
13. Helleday T, (2011) The underlying mechanism for the PARP and BRCA synthetic lethality: Clearing up the misunderstandings. Molecular Oncology 5: 387-393.
14. Fong PC, Boss DS, Yap TA, Tutt A, Wu P, et al. (2009) Inhibition of poly(ADP-ribose) polymerase in tumors from BRCA mutation carriers. New England Journal of Medicine 361: 123-134.
15. Mizuarai S, Kotani H, (2010) Synthetic lethal interactions for the development of cancer therapeutics: biological and methodological advancements. Human Genetics 128: 567-575.
16. Baryshnikova A, Costanzo M, Kim Y, Ding H, Koh J, et al. (2010) Quantitative analysis of fitness and genetic interactions in yeast on a genome scale. Nature Methods 7: 1017-1024.
17. Kelley R, Ideker T, (2005) Systematic interpretation of genetic interactions using protein networks. Nature Biotechnology 23: 561-566.
18. Michaut M, Baryshnikova A, Costanzo M, Myers CL, Andrews BJ, et al. (2011) Protein complexes are central in the yeast genetic landscape. PLoS Comput Biol 7: e1001092.
19. Bellay J, Atluri G, Sing TL, Toufighi K, Costanzo M, et al. (2011) Putting genetic interactions in context through a global modular decomposition. Genome Research 21: 1375-1387.
20. Costanzo M, Baryshnikova A, Myers CL, Andrews B, Boone C, (2011) Charting the genetic interaction map of a cell. Current Opinion in Biotechnology 22: 66-74.
21. Sopko R, Huang D, Preston N, Chua G, Papp B, et al. (2006) Mapping pathways and phenotypes by systematic gene overexpression. Molecular Cell 21: 319-330.
22. Bandyopadhyay S, Kelley R, Krogan NJ, Ideker T, (2008) Functional maps of protein complexes from quantitative genetic interaction data. PLoS Comput Biol 4: e1000065.
23. Heyer WD, Ehmsen KT, Liu J, (2010) Regulation of homologous recombination in eukaryotes. Annual Reviews Genetics 44: 113-139.
24. Kanaar R, Wyman C, Rothstein R, (2008) Quality control of DNA break metabolism: in the 'end', it's a good thing. EMBO Journal 27: 581-588.
25. Symington LS, Heyer WD, (2006) Some disassembly required: role of DNA translocases in the disruption of recombination intermediates and dead-end complexes. Genes and Development 20: 2479-2486.
26. Alon U, (2003) Biological Networks: The tinkerer as an engineer. Science 301: 1866-1867.
27. Savageau M, (1971) Parameter sensitivity as a criterion for evaluating and comparing the performance of biochemical systems. Nature 229: 542-544.
28. Kitano H, (2004) Biological robustness. Nature Reviews Genetics 5: 826-837.
29. Li X, Heyer WD, (2008) Homologous recombination in DNA repair and DNA damage tolerance. Cell Research 18: 99-113.
30. Kanehisa M, Goto S, Sato Y, Furumichi M, Tanabe M, (2012) KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Research 40: D109-114.
31. Veaute X, Jeusset J, Soustelle C, Kowalczykowski SC, Le Cam E, et al. (2003) The Srs2 helicase prevents recombination by disrupting Rad51 nucleoprotein filaments. Nature 423: 309-312.
32. Krejci L, Van Komen S, Li Y, Villemain J, Reddy MS, et al. (2003) DNA helicase Srs2 disrupts the Rad51 presynaptic filament. Nature 423: 305-309.
33. Liu J, Renault L, Veaute X, Fabre F, Stahlberg H, et al. (2011) Rad51 paralogs Rad55-Rad57 balance the anti-recombinase function of Srs2 in Rad51 pre-synaptic filament formation. Nature 479: 245-248.
34. Hopfield JJ, (1974) Kintic proofreading: a new mechanism for reducing errors in biosynthetic processes requiting high specifcity. Proceedings National Academy of Sciences USA 71: 4135-4139.
35. Palladino F, Klein HL, (1992) Analysis of mitotic and meiotic defects in Saccharomyces cerevisiae SRS2 DNA helicase mutants. Genetics 132: 23-37.
36. Heyer WD, Li X, Rolfsmeier M, Zhang XP, (2006) Rad54: the Swiss Army knife of homologous recombination? Nucleic Acids Research 34: 4115-4125.
37. Fugger K, Mistrik M, Danielsen JR, Dinant C, Falck J, et al. (2009) Human Fbh1 helicase contributes to genome maintenance via pro- and anti-recombinase activities. Journal of Cell Biology 186: 655-663.
38. Sommers JA, Rawtani N, Gupta R, Bugreev DV, Mazin AV, et al. (2009) FANCJ uses its motor ATPase to destabilize protein-DNA complexes, unwind triplexes, and inhibit RAD51 strand exchange. Journal of Biological Chemistry 284: 7502-7514.
39. Schwendener S, Raynard S, Paliwal S, Cheng A, Kanagaraj R, et al. (2010) Physical Interaction of RECQ5 Helicase with RAD51 Facilitates Its Anti-recombinase Activity. Journal of Biological Chemistry 285: 15739-15745.
40. McManus KJ, Barrett IJ, Nouhi Y, Hieter P, (2009) Specific synthetic lethal killing of RAD54B-deficient human colorectal cancer cells by FEN1 silencing. Proceedings National Academy of Sciences USA 106: 3276-3281.
41. Klein HL, (2008) The consequences of Rad51 overexpression for normal and tumor cells. DNA Repair 7: 686-693.
42. Feng ZH, Scott SP, Bussen W, Sharma GG, Guo G, et al. (2010) Rad52 inactivation is synthetically lethal with BRCA2 deficiency. Proceedings National Academy of Sciences USA 108: 686-691.
43. Slupianek A, Schmutte C, Tombline G, Nieborowska-Skorska M, Hoser G, et al. (2001) BCR/ABL regulates mammalian RecA homologs, resulting in drug resistance. Molecular Cell 8: 795-806.
44. Maacke H, Opitz S, Jost K, Hamdorf W, Henning W, et al. (2000) Over-expression of wild-type Rad51 correlates with histological grading of invasive ductal breast cancer. International Journal of Cancer 88: 907-913.
45. Christodoulopoulos G, Malapetsa A, Schipper H, Golub E, Radding C, et al. (1999) Chlorambucil induction of HsRad51 in B-cell chronic lymphocytic leukemia. Clinical Cancer Research 5: 2178-2184.
46. Fabre F, Chan A, Heyer WD, Gangloff S, (2002) Alternate pathways involving Sgs1/Top3, Mus81/Mms4, and Srs2 prevent formation of toxic recombination intermediates from single-stranded gaps created by DNA replication. Proceedings National Academy of Sciences USA 99: 16887-16892.
47. Gangloff S, Soustelle C, Fabre F, (2000) Homologous recombination is responsible for cell death in the absence of the Sgs1 and Srs2 helicases. Nature Genetics 25: 192-194.
48. Maftahi M, Hope JC, Delgado-Cruzata L, Han CS, Freyer GA, (2002) The severe slow growth of Delta srs2 Delta rqh1 in Schizosaccharomyces pombe is suppressed by loss of recombination and checkpoint genes. Nucleic Acids Research 30: 4781-4792.
49. Schild D, (1995) Suppression of a new allele of the yeast RAD52 gene by overexpression of RAD51, mutations in srs2 and ccr4, or mating-type heterozygosity. Genetics 140: 115-127.
50. Trowbridge K, McKim K, Brill SJ, Sekelsky J, (2007) Synthetic lethality of Drosophila in the absence of the MUS81 endonuclease and the DmBlm helicase is associated with elevated apoptosis. Genetics 176: 1993-2001.
51. De Muyt A, Jessop L, Kolar E, Sourirajan A, Chen JH, et al. (2012) BLM Helicase Ortholog Sgs1 Is a Central Regulator of Meiotic Recombination Intermediate Metabolism. Molecular Cell 46: 43-53.
52. Zakharyevich K, Tang SM, Ma YM, Hunter N, (2012) Delineation of Joint Molecule Resolution Pathways in Meiosis Identifies a Crossover-Specific Resolvase. Cell 149: 334-347.
53. St Onge RP, Mani R, Oh J, Proctor M, Fung E, et al. (2007) Systematic pathway analysis using high-resolution fitness profiling of combinatorial gene deletions. Nature Genetics 39: 199-206.
54. Gorban A, Radulescu O, Zinovyev A, (2010) Asymptotology of chemical reactions networks. Chemical Engineering Sciences 65: 2310-2324.
55. Hartl FU, Bracher A, Hayer-Hartl M, (2011) Molecular chaperones in protein folding and proteostasis. Nature 475: 324-332.
56. Voisine C, Pedersen JS, Morimoto RI, (2010) Chaperone networks: tipping the balance in protein folding diseases. Neurobiological Diseases 40: 12-20.
57. Bartz RR, Piantadosi CA, (2010) Clinical review: oxygen as a signaling molecule. Critical Care 14: 234.
58. Hamanaka RB, Chandel NS, (2012) Mitochondrial reactive oxygen species regulate cellular signaling and dictate biological outcomes. Trends in Biochemical Sciences 35: 505-513.
59. Karihtala P, Soini Y, (2007) Reactive oxygen species and antioxidant mechanisms in human tissues and their relation to malignancies. APMIS 115: 81-103.
60. Gareau JR, Lima CD, (2010) The SUMO pathway: emerging mechanisms that shape specificity, conjugation and recognition. Nature Reviews Molecular Cell Biology 11: 861-871.
61. Geiss-Friedlander R, Melchior F, (2007) Concepts in sumoylation: a decade on. Nature Reviews Molecular Cell Biology 8: 947-956.
62. Wilkinson KA, Henley JM, (2010) Mechanisms, regulation and consequences of protein SUMOylation. Biochemical Journal 428: 133-145.
63. Moremen KW, Tiemeyer M, Nairn AV, (2012) Vertebrate protein glycosylation: diversity, synthesis and function. Nature Reviews Molecular Cell Biology 13: 448-462.
64. Schwarz F, Aebi M, (2011) Mechanisms and principles of N-linked protein glycosylation. Current Opinion Structural Biology 21: 576-582.
65. Kulathu Y, Komander D, (2012) Atypical ubiquitylation- the unexplored world of polyubiquitin beyond Lys48 and Lys63 linkages. Nature Reviews Molecular Cell Biology 13: 508-523.
66. Sigismund S, Polo S, Di Fiore PP, (2004) Signaling through monoubiquitination. Curr Top Microbiology Immunology 286: 149-185.
67. Vertegaal AC, (2011) Uncovering ubiquitin and ubiquitin-like signaling networks. Chemical Reviews 111: 7923-7940.
68. Chen X, Zhang B, Fischer JA, (2002) A specific protein substrate for a deubiquitinating enzyme: Liquid facets is the substrate of Fat facets. Genes and Development 16: 289-294.