The SWI/SNF KlSnf2 subunit controls the glucose signaling pathway to coordinate glycolysis and glucose transport in Kluyveromyces lactis

Eukaryotic Cell

Volumn 11, Issue 11, 2012, Pages 1382-1390

  Cotton, Pascale ^a,b,c   Soulard, Alexandre ^a,b,c   Wésolowski Louvel, Micheline ^a,b,c   Lemaire, Marc ^a,b,c  

^a UNIVERSITÉ DE LYON   (France)

^b UNIVERSITÉ LYON 1   (France)

^c CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; DNA BINDING PROTEIN; FUNGAL PROTEIN; FUNGAL RNA; GLUCOSE; RAG4 PROTEIN, KLUYVEROMYCES; REPRESSOR PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN; SNF2 PROTEIN, S CEREVISIAE; TRANSCRIPTION FACTOR;

ARTICLE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN IMMUNOPRECIPITATION; ENZYMOLOGY; FUNGAL GENE; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETIC COMPLEMENTATION; GENETICS; GLYCOLYSIS; KLUYVEROMYCES; METABOLISM; MOLECULAR CLONING; MUTATION; PROMOTER REGION; PROTEIN DEGRADATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA PROCESSING; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; TRANSPORT AT THE CELLULAR LEVEL;

ADENOSINE TRIPHOSPHATASES; BIOLOGICAL TRANSPORT; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN IMMUNOPRECIPITATION; CLONING, MOLECULAR; DNA-BINDING PROTEINS; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; GENE REGULATORY NETWORKS; GENES, FUNGAL; GENETIC COMPLEMENTATION TEST; GLUCOSE; GLYCOLYSIS; KLUYVEROMYCES; MUTATION; PROMOTER REGIONS, GENETIC; PROTEOLYSIS; REPRESSOR PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, FUNGAL; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TRANSCRIPTIONAL ACTIVATION;

KLUYVEROMYCES LACTIS; SACCHAROMYCES CEREVISIAE;

EID: 84868095233     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00210-12     Document Type: Article

References (57)

1. Betina S, Goffrini P, Ferrero I, Wésolowski-Louvel M. 2001. RAG4 gene encodes a glucose sensor in Kluyveromyces lactis. Genetics 158:541-548.
2. Billard P, et al. 1996. Glucose uptake in Kluyveromyces lactis: role of the HGT1 gene in glucose transport. J. Bacteriol. 178:5860-5866.
3. Blaisonneau J, Fukuhara H, Wésolowski-Louvel M. 1997. The Kluyveromyces lactis equivalent of casein kinase I is required for the transcription of the gene encoding the low-affinity glucose permease. Mol. Gen. Genet. 253:469-477.
4. Bonhomme J, et al. 2011. Contribution of the glycolytic flux and hypoxia adaptation to efficient biofilm formation by Candida albicans. Mol. Microbiol. 80:995-1013.
5. Byrne KP, Wolfe KH. 2005. The Yeast Gene Order Browser: combining curated homology and syntenic context reveals gene fate in polyploid species. Genome Res. 15:1456-1461.
6. Cairns BR. 2009. The logic of chromatin architecture and remodelling at promoters. Nature 461:193-198.
7. Chen XJ. 1996. Low-and high-copy-number shuttle vectors for replication in the budding yeast Kluyveromyces lactis. Gene 172:131-136.
8. Chen XJ, Wésolowski-Louvel M, Fukuhara H. 1992. Glucose transport in the yeast Kluyveromyces lactis. II. Transcriptional regulation of the glucose transporter gene RAG1. Mol. Gen. Genet. 233:97-105.
9. Clapier CR, Cairns BR. 2009. The biology of chromatin remodeling complexes. Annu. Rev. Biochem. 78:273-304.
10. Cosma MP, Tanaka T, Nasmyth K. 1999. Ordered recruitment of transcription and chromatin remodeling factors to a cell cycle-and developmentally regulated promoter. Cell 97:299-311.
11. de la Serna IL, et al. 2005. MyoD targets chromatin remodeling complexes to the myogenin locus prior to forming a stable DNA-bound complex. Mol. Cell. Biol. 25:3997-4009.
12. Diamond DL, et al. 2010. Temporal proteome and lipidome profiles reveal hepatitis C virus-associated reprogramming of hepatocellular metabolism and bioenergetics. PLoS Pathog. 6:e1000719. doi:10.1371/ journal.ppat.1000719.
13. Doerks T, Copley RR, Schultz J, Ponting CP, Bork P. 2002. Systematic identification of novel protein domain families associated with nuclear functions. Genome Res. 12:47-56.
14. Dujon B, et al. 2004. Genome evolution in yeasts. Nature 430:35-44.
15. Dürr H, Körner C, Müller M, Hickmann V, Hopfner KP. 2005. X-ray structures of the Sulfolobus solfataricus SWI2/SNF2 ATPase core and its complex with DNA. Cell 121:363-373.
16. Edmondson DG, Smith MM, Roth SY. 1996. Repression domain of the yeast global repressor Tup1 interacts directly with histones H3 and H4. Genes Dev. 10:1247-1259.
17. Flaus A, Martin DM, Barton GJ, Owen-Hughes T. 2006. Identification of multiple distinct Snf2 subfamilies with conserved structural motifs. Nucleic Acids Res. 34:2887-2905.
18. Fleming AB, Pennings S. 2001. Antagonistic remodelling by Swi-Snf and Tup1-Ssn6 of an extensive chromatin region forms the background for FLO1 gene regulation. EMBO J. 20:5219-5231.
19. Friis RM, et al. 2009. A glycolytic burst drives glucose induction of global histone acetylation by picNuA4 and SAGA. Nucleic Acids Res. 37:3969-3980.
20. Hnatova M, Wesolowski-Louvel M, Dieppois G, Deffaud J, Lemaire M. 2008. Characterization of KlGRR1 and SMS1 genes, two new elements of the glucose signaling pathway of Kluyveromyces lactis. Eukaryot. Cell 7:1299-1308.
21. Holstege FC, et al. 1998. Dissecting the regulatory circuitry of a eukaryotic genome. Cell 95:717-728.
22. Johnston M, Kim JH. 2005. Glucose as a hormone: receptor-mediated glucose sensing in the yeast Saccharomyces cerevisiae. Biochem. Soc. Trans. 33:247-252.
23. Kushnirov VV. 2000. Rapid and reliable protein extraction from yeast. Yeast 16:857-860.
24. Lemaire M, Guyon A, Betina S, Wésolowski-Louvel M. 2002. Regulation of glycolysis by casein kinase I (Rag8p) in Kluyveromyces lactis involves a DNA-binding protein, Sck1p, a homologue of Sgc1p of Saccharomyces cerevisiae. Curr. Genet. 40:355-364.
25. Lemaire M, Wésolowski-Louvel M. 2004. Enolase and glycolytic flux play a role in the regulation of the glucose permease gene RAG1 of Kluyveromyces lactis. Genetics 168:723-731.
26. Longtine MS, et al. 1998. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14:953-961.
27. Macheda ML, Rogers S, Best JD. 2005. Molecular and cellular regulation of glucose transporter (GLUT) proteins in cancer. J. Cell. Physiol. 202: 654-662.
28. Mathupala SP, Rempel A, Pedersen PL. 2001. Glucose catabolism in cancer cells: identification and characterization of a marked activation response of the type II hexokinase gene to hypoxic conditions. J. Biol. Chem. 276:43407-43412.
29. McArdle J, Moorman NJ, Munger J. 2012. HCMV targets the metabolic stress response through activation of AMPK whose activity is important for viral replication. PLoS Pathog. 8:e1002502. doi:10.1371/ journal.ppat.1002502.
30. Moriya H, Johnston M. 2004. Glucose sensing and signaling in Saccharomyces cerevisiae through the Rgt2 glucose sensor and casein kinase I. Proc. Natl. Acad. Sci. U. S. A. 101:1572-1577.
31. Naidu SR, Love IM, Imbalzano AN, Grossman SR, Androphy EJ. 2009. The SWI/SNF chromatin remodeling subunit BRG1 is a critical regulator of p53 necessary for proliferation of malignant cells. Oncogene 28:2492-2501.
32. Neigeborn L, Carlson M. 1984. Genes affecting the regulation of SUC2 gene expression by glucose repression in Saccharomyces cerevisiae. Genetics 108:845-858.
33. Neil H, Hnatova M, Wesolowski-Louvel M, Rycovska A, Lemaire M. 2007. Sck1 activator coordinates glucose transport and glycolysis and is controlled by Rag8 casein kinase I in Kluyveromyces lactis. Mol. Microbiol. 63:1537-1548.
34. Ozcan S, Johnston M. 1996. Two different repressors collaborate to restrict expression of the yeast glucose transporter genes HXT2 and HXT4 to low levels of glucose. Mol. Cell. Biol. 16:5536-5545.
35. Ozcan S, Johnston M. 1999. Function and regulation of yeast hexose transporters. Microbiol. Mol. Biol. Rev. 63:554-569.
36. Peterson CL, Workman JL. 2000. Promoter targeting and chromatin remodeling by the SWI/SNF complex. Curr. Opin. Genet. Dev. 10:187-192.
37. Prior C, Mamessier P, Fukuhara H, Chen XJ, Wésolowski-Louvel M. 1993. The hexokinase gene is required for transcriptional regulation of the glucose transporter gene RAG1 in Kluyveromyces lactis. Mol. Cell. Biol. 13:3882-3889.
38. Prochasson P, Neely KE, Hassan AH, Li B, Workman JL. 2003. Targeting activity is required for SWI/SNF function in vivo and is accomplished through two partially redundant activator-interaction domains. Mol. Cell 12:983-990.
39. Rolland S, Hnatova M, Lemaire M, Leal-Sanchez J, Wesolowski-Louvel M. 2006. Connection between the Rag4 glucose sensor and the KlRgt1 repressor in Kluyveromyces lactis. Genetics 174:617-626.
40. Sabina J, Brown V. 2009. Glucose sensing network in Candida albicans: a sweet spot for fungal morphogenesis. Eukaryot. Cell 8:1314-1320.
41. Santangelo GM. 2006. Glucose signaling in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 70:253-282.
42. Smith CL, Peterson CL. 2005. A conserved Swi2/Snf2 ATPase motif couples ATP hydrolysis to chromatin remodeling. Mol. Cell. Biol. 25: 5880-5892.
43. Sudarsanam P, Iyer VR, Brown PO, Winston F. 2000. Whole-genome expression analysis of snf/swi mutants of Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. U. S. A. 97:3364-3369.
44. Thomä NH, et al. 2005. Structure of the SWI2/SNF2 chromatinremodeling domain of eukaryotic Rad54. Nat. Struct. Mol. Biol. 12:350-356.
45. Thorens B. 2008. Glucose sensing and the pathogenesis of obesity and type 2 diabetes. Int. J. Obes. (Lond.) 32(Suppl 6):S62-S71.
46. Tomas-Cobos L, Sanz P. 2002. Active Snf1 protein kinase inhibits expression of the Saccharomyces cerevisiae HXT1 glucose transporter gene. Biochem. J. 368:657-663.
47. van Oevelen CJC, van Teeffelen HAAM, van Werven FJ, Timmers HTM. 2006. Snf1p-dependent Spt-Ada-Gcn5-acetyltransferase (SAGA) recruitment and chromatin remodeling activities on the HXT2 and HXT4 promoters. J. Biol. Chem. 281:4523-4531.
48. Wellen KE, et al. 2009. ATP-citrate lyase links cellular metabolism to histone acetylation. Science 324:1076-1080.
49. Wésolowski M, Algeri A, Goffrini P, Fukuhara H. 1982. Killer DNA plasmids of the yeast Kluyveromyces lactis. Curr. Genet. 5:191-197.
50. Wésolowski-Louvel M. 2011. An efficient method to optimize Kluyveromyces lactis gene targeting. FEMS Yeast Res. 11:509-513.
51. Wésolowski-Louvel M, Goffrini P, Ferrero I, Fukuhara H. 1992. Glucose transport in the yeast Kluyveromyces lactis. I. Properties of an inducible low-affinity glucose transporter gene. Mol. Gen. Genet. 233:89-96.
52. Wésolowski-Louvel M, Prior C, Bornecque D, Fukuhara H. 1992. rag-mutations involved in glucose metabolism in yeast: isolation and genetic characterization. Yeast 8:711-719.
53. Wilson BG, Roberts CW. 2011. SWI/SNF nucleosome remodellers and cancer. Nat. Rev. Cancer 11:481-492.
54. Winston F, Allis CD. 1999. The bromodomain: a chromatin-targeting module? Nat. Struct. Biol. 6:601-604.
55. Wolfe KH, Shields DC. 1997. Molecular evidence for an ancient duplication of the entire yeast genome. Nature 387:708-713.
56. Yudkovsky N, Logie C, Hahn S, Peterson CL. 1999. Recruitment of the SWI/SNF chromatin remodeling complex by transcriptional activators. Genes Dev. 13:2369-2374.
57. Zawadzki KA, Morozov AV, Broach JR. 2009. Chromatin-dependent transcription factor accessibility rather than nucleosome remodeling predominates during global transcriptional restructuring in Saccharomyces cerevisiae. Mol. Biol. Cell 20:3503-3513.