VapC6, a ribonucleolytic toxin regulates thermophilicity in the crenarchaeote Sulfolobus solfataricus

RNA

Volumn 17, Issue 7, 2011, Pages 1381-1392

  Maezato, Yukari ^a   Daugherty, Amanda ^a   Dana, Karl ^a   Soo, Edith ^a   Cooper, Charlotte ^b   Tachdjian, Sabrina ^b   Kelly, Robert M ^b   Blum, Paul ^a  

^a UNIVERSITY OF NEBRASKA   (United States)

^b North Carolina State University   (United States)

Author keywords

Antitoxin; Archaea; Heat shock; RNA degradation; Transcription

Indexed keywords

BACTERIAL TOXIN; CHAPERONE; INITIATION FACTOR 2; UNCLASSIFIED DRUG; VAPC6 TOXIN;

ARTICLE; BACTERIAL GROWTH; BACTERIAL MUTATION; BACTERIAL STRAIN; BACTERIAL SURVIVAL; GENE DELETION; GENE DISRUPTION; GENE EXPRESSION; GENE LOCUS; GENE TARGETING; HEAT STRESS; HEAT TOLERANCE; MOLECULAR MECHANICS; OPERON; PHENOTYPE; PRIORITY JOURNAL; SULFOLOBUS SOLFATARICUS; TRANSCRIPTOMICS;

ADAPTATION, PHYSIOLOGICAL; CELL LINE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, ARCHAEAL; HYDROLYSIS; MODELS, BIOLOGICAL; RNA; SULFOLOBUS SOLFATARICUS; TEMPERATURE; TOXINS, BIOLOGICAL;

CRENARCHAEOTA; SULFOLOBUS SOLFATARICUS;

EID: 79959303354     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.2679911     Document Type: Article

References (62)

1. Allen MB. 1959. Studies with Cyanidium caldarium, an anomalously pigmented chlorophyte. Arch Mikrobiol 32: 270-277.
2. Anantharaman V, Aravind L. 2003. New connections in the prokaryotic toxin-antitoxin network: relationship with the eukaryotic nonsense-mediated RNA decay system. Genome Biol 4: R81. doi: 10.1186/gb-2003-4-12-r81.
3. Arcus VL, Backbro K, Roos A, Daniel EL, Baker EN. 2004. Distant structural homology leads to the functional characterization of an archaeal PIN domain as an exonuclease. J Biol Chem 279: 16471-16478.
4. Bates PA, Sternberg MJ. 1999. Model building by comparison at CASP3: using expert knowledge and computer automation. Proteins 37 Suppl 3: 47-54. (Pubitemid 29463514)
5. Bates PA, Kelley LA, MacCallum RM, Sternberg MJE. 2001. Enhancement of protein modelling by human intervention in applying the automatic programs 3D-JIGSAW and 3D-PSSM. Protein Struct Funct Genet (Suppl) 5: 39-46. (Pubitemid 34113166)
6. Berkner S, Grogan D, Albers SV, Lipps G. 2007. Small multicopy, nonintegrative shuttle vectors based on the plasmid pRN1 for Sulfolobus acidocaldarius and Sulfolobus solfataricus, model organisms of the (cren-)archaea. Nucleic Acids Res 35: e88. doi: 10.1093/nar/gkm449.
7. Bhagwat M, Meara D, Nossal NG. 1997. Identification of residues of T4 RNase H required for catalysis and DNA binding. J Biol Chem 272: 28531-28538. (Pubitemid 27517803)
8. Bini E, Dikshit V, Dirksen K, Drozda M, Blum P. 2002. Stability of mRNA in the hyperthermophilic archaeon Sulfolobus solfataricus. RNA 8: 1129-1136. (Pubitemid 35024569)
9. Blum P, Ory J, Bauernfeind J, Krska J. 1992a. Physiological consequences of DnaK and DnaJ overproduction in Escherichia coli. J Bacteriol 174: 7436-7444.
10. Blum P, Velligan M, Lin N, Matin A. 1992b. DnaK-mediated alterations in human growth hormone protein inclusion bodies. Biotechnology 10: 301-304.
11. Bodogai M, Ferenczi S, Bashtovyy D, Miclea P, Papp P, Dusha I. 2006. The ntrPR operon of Sinorhizobium meliloti is organized and functions as a toxin-antitoxin module. Mol Plant Microbe Interact 19: 811-822.
12. Bradford WD, Cahoon L, Freel SR, Hoopes LL, Eckdahl TT. 2005. An inexpensive gel electrophoresis-based polymerase chain reaction method for quantifying mRNA levels. Cell Biol Educ 4: 157-168. (Pubitemid 41126824)
13. Bunker RD, McKenzie JL, Baker EN, Arcus VL. 2008. Crystal structure of PAE0151 from Pyrobaculum aerophilum, a PIN-domain (VapC) protein from a toxin-antitoxin operon. Proteins 72: 510-518.
14. Cerchia L, Rossi M, Guagliardi A. 2000. An archaeal chaperonin-based reactor for renaturation of denatured proteins. Extremophiles 4: 1-7. (Pubitemid 30144314)
15. Chang AC, Cohen SN. 1978. Construction and characterization of amplifiable multicopy DNA cloning vehicles derived from the P15A cryptic miniplasmid. J Bacteriol 134: 1141-1156. (Pubitemid 8354538)
16. Christensen-Dalsgaard M, Gerdes K. 2006. Two higBA loci in the Vibrio cholerae superintegron encode mRNA cleaving enzymes and can stabilize plasmids. Mol Microbiol 62: 397-411. (Pubitemid 44477230)
17. Cooper CR, Daugherty AJ, Tachdjian S, Blum PH, Kelly RM. 2009. Role of vapBC toxin-antitoxin loci in the thermal stress response of Sulfolobus solfataricus. Biochem Soc Trans 37: 123-126.
18. Daines DA, Wu MH, Yuan SY. 2007. VapC-1 of nontypeable Haemophilus influenzae is a ribonuclease. J Bacteriol 189: 5041-5048. (Pubitemid 47076049)
19. Gerdes K. 2000. Toxin-antitoxin modules may regulate synthesis of macromolecules during nutritional stress. J Bacteriol 182: 561-572. (Pubitemid 30053984)
20. Gerdes K, Christensen SK, Lobner-Olesen A. 2005. Prokaryotic toxinantitoxin stress response loci. Nat Rev Microbiol 3: 371-382. (Pubitemid 40590380)
21. Haseltine C, Montalvo-Rodriguez R, Bini E, Carl A, Blum P. 1999. Coordinate transcriptional control in the hyperthermophilic archaeon Sulfolobus solfataricus. J Bacteriol 181: 3920-3927. (Pubitemid 29295908)
22. Hethke C, Bergerat A, Hausner W, Forterre P, Thomm M. 1999. Cell-free transcription at 95 degrees: thermostability of transcriptional components and DNA topology requirements of Pyrococcus transcription. Genetics 152: 1325-1333. (Pubitemid 29370316)
23. Hoang V, Bini E, Dixit V, Drozda M, Blum P. 2004. The role of cis-acting sequences governing catabolite repression control of lacS expression in the archaeon Sulfolobus solfataricus. Genetics 167: 1563-1572. (Pubitemid 39265896)
24. Hopper S, Wilbur JS, Vasquez BL, Larson J, Clary S, Mehr IJ, Seifert HS, So M. 2000. Isolation of Neisseria gonorrhoeae mutants that show enhanced trafficking across polarized T84 epithelial monolayers. Infect Immun 68: 896-905. (Pubitemid 30056550)
25. Jensen RB, Gerdes K. 1995. Programmed cell death in bacteria: proteic plasmid stabilization systems. Mol Microbiol 17: 205-210.
26. Jorgensen MG, Pandey DP, Jaskolska M, Gerdes K. 2009. HicA of Escherichia coli defines a novel family of translation-independent mRNA interferases in bacteria and archaea. J Bacteriol 191: 1191-1199.
27. Kim MS, Park JT, Kim YW, Lee HS, Nyawira R, Shin HS, Park CS, Yoo SH, Kim YR, Moon TW, et al. 2004. Properties of a novel thermostable glucoamylase from the hyperthermophilic archaeon Sulfolobus solfataricus in relation to starch processing. Appl Environ Microbiol 70: 3933-3940. (Pubitemid 38969731)
28. Lesur I, Campbell JL. 2004. The transcriptome of prematurely aging yeast cells is similar to that of telomerase-deficient cells. Mol Biol Cell 15: 1297-1312. (Pubitemid 38316236)
29. Liu W, Vierke G, Wenke AK, Thomm M, Ladenstein R. 2007. Crystal structure of the archaeal heat shock regulator from Pyrococcus furiosus: a molecular chimera representing eukaryal and bacterial features. J Mol Biol 369: 474-488. (Pubitemid 46678052)
30. Maaty WS, Wiedenheft B, Tarlykov P, Schaff N, Heinemann J, Robison-Cox J, Valenzuela J, Dougherty A, Blum P, Lawrence CM, et al. 2009. Something old, something new, something borrowed; how the thermoacidophilic archaeon Sulfolobus solfataricus responds to oxidative stress. PLoS ONE 4: e6964. doi: 10.1371/journal.pone.0006964.
31. Madl T, Van Melderen L, Mine N, Respondek M, Oberer M, Keller W, Khatai L, Zangger K. 2006. Structural basis for nucleic acid and toxin recognition of the bacterial antitoxin CcdA. J Mol Biol 364: 170-185. (Pubitemid 44647253)
32. Makarova KS, Wolf YI, Koonin EV. 2009. Comprehensive comparative-genomic analysis of Type 2 toxin-antitoxin systems and related mobile stress response systems in prokaryotes. Biol Direct 4: 19. doi: 10.1186/1745-6150-4-19.
33. Marone M, Mozzetti S, De Ritis D, Pierelli L, Scambia G. 2001. Semiquantitative RT-PCR analysis to assess the expression levels of multiple transcripts from the same sample. Biol Proced Online 3: 19-25. (Pubitemid 33807179)
34. Martusewitsch E, Sensen CW, Schleper C. 2000. High spontaneous mutation rate in the hyperthermophilic archaeon Sulfolobus solfataricus is mediated by transposable elements. J Bacteriol 182: 2574-2581. (Pubitemid 30212918)
35. Mattison K, Wilbur JS, So M, Brennan RG. 2006. Structure of FitAB from Neisseria gonorrhoeae bound to DNA reveals a tetramer of toxin-antitoxin heterodimers containing pin domains and ribbon-helix-helix motifs. J Biol Chem 281: 37942-37951. (Pubitemid 46042098)
36. Miallau L, Faller M, Chiang J, Arbing M, Guo F, Cascio D, Eisenberg D. 2009. Structure and proposed activity of a member of the VapBC family of toxin-antitoxin systems. VapBC-5 from Mycobacterium tuberculosis. J Biol Chem 284: 276-283.
37. Nakayama H, Yokoi H, Fujita J. 1992. Quantification of mRNA by non-radioactive RT-PCR and CCD imaging system. Nucleic Acids Res 20: 4939. doi: 10.1093/nar/20.18.4939.
38. Noonan KE, Beck C, Holzmayer TA, Chin JE, Wunder JS, Andrulis IL, Gazdar AF, Willman CL, Griffith B, Von Hoff DD, et al. 1990. Quantitative analysis of MDR1 (multidrug resistance) gene expression in human tumors by polymerase chain reaction. Proc Natl Acad Sci 87: 7160-7164.
39. Pandey DP, Gerdes K. 2005. Toxin-antitoxin loci are highly abundant in free-living but lost from host-associated prokaryotes. Nucleic Acids Res 33: 966-976. (Pubitemid 41430517)
40. Robson J, McKenzie JL, Cursons R, Cook GM, Arcus VL. 2009. The vapBC operon from Mycobacterium smegmatis is an autoregulated toxin-antitoxin module that controls growth via inhibition of translation. J Mol Biol 390: 353-367.
41. Rodriguez F, Arsene-Ploetze F, Rist W, Rudiger S, Schneider-Mergener J, Mayer MP, Bukau B. 2008. Molecular basis for regulation of the heat shock transcription factor s32 by the DnaK and DnaJ chaperones. Mol Cell 32: 347-358.
42. Rolfsmeier M, Blum P. 1995. Purification and characterization of a maltase from the extremely thermophilic crenarchaeote Sulfolobus solfataricus. J Bacteriol 177: 482-485.
43. Rolfsmeier M, Haseltine C, Bini E, Clark A, Blum P. 1998. Molecular characterization of the α-glucosidase gene (malA) from the hyperthermophilic archaeon Sulfolobus solfataricus. J Bacteriol 180: 1287-1295. (Pubitemid 28119489)
44. Schelert J. 2006. Mercury resistance in Sulfolobus solfataricus. In Microbiology. University of Nebraska-Lincoln, Lincoln, NE.
45. Schelert J, Dixit V, Hoang V, Simbahan J, Drozda M, Blum P. 2004. Occurrence and characterization of mercury resistance in the hyperthermophilic archaeon Sulfolobus solfataricus by use of gene disruption. J Bacteriol 186: 427-437. (Pubitemid 38076433)
46. Schelert J, Drozda M, Dixit V, Dillman A, Blum P. 2006. Regulation of mercury resistance in the crenarchaeote Sulfolobus solfataricus. J Bacteriol 188: 7141-7150. (Pubitemid 44547619)
47. Shapiro J, Brutlag D. 2004. FoldMiner and LOCK 2: protein structure comparison and motif discovery on the web. Nucleic Acids Res 32: W536-W541. (Pubitemid 38997391)
48. She Q, Singh RK, Confalonieri F, Zivanovic Y, Allard G, Awayez MJ, Chan-Weiher CC-Y, Clausen Ib G, Curtis BA, De Moors A, et al. 2001. The complete genome of the crenarchaeon Sulfolobus solfataricus P2. Proc Natl Acad Sci 98: 7835-7840. (Pubitemid 32642647)
49. Sowers KR, Blum PH, DasSharma S. 2006. Gene transfer in archaea. In Methods for general and molecular microbiology (ed. C Reddy). ASM Press, Washington, DC.
50. Tachdjian S, Kelly RM. 2006. Dynamic metabolic adjustments and genome plasticity are implicated in the heat shock response of the extremely thermoacidophilic archaeon Sulfolobus solfataricus. J Bacteriol 188: 4553-4559. (Pubitemid 43865774)
51. Thompson DK, Palmer JR, Daniels CJ. 1999. Expression and heatresponsive regulation of a TFIIB homologue from the archaeon Haloferax volcanii. Mol Microbiol 33: 1081-1092. (Pubitemid 29425259)
52. Trent JD, Osipiuk J, Pinkau T. 1990. Acquired thermotolerance and heat shock in the extremely thermophilic archaebacterium Sulfolobus sp. strain B12. J Bacteriol 172: 1478-1484. (Pubitemid 20085975)
53. Trent JD, Nimmesgern E, Wall JS, Hartl FU, Horwich AL. 1991. A molecular chaperone from a thermophilic archaebacterium is related to the eukaryotic protein t-complex polypeptide-1. Nature 354: 490-493. (Pubitemid 21896866)
54. Vierke G, Engelmann A, Hebbeln C, Thomm M. 2003. A novel archaeal transcriptional regulator of heat shock response. J Biol Chem 278: 18-26. (Pubitemid 36043539)
55. Vuister GW, Kim SJ, Orosz A, Marquardt J, Wu C, Bax A. 1994. Solution structure of the DNA-binding domain of Drosophila heat shock transcription factor. Nat Struct Biol 1: 605-614.
56. Wagner MA, Zahrl D, Rieser G, Koraimann G. 2009. Growth phaseand cell division-dependent activation and inactivation of the {σ}32 regulon in Escherichia coli. J Bacteriol 191: 1695-1702.
57. Westerheide SD, Anckar J, Stevens SM Jr, Sistonen L, Morimoto RI. 2009. Stress-inducible regulation of heat shock factor 1 by the deacetylase SIRT1. Science 323: 1063-1066.
58. Worthington P, Blum P, Perez-Pomares F, Elthon T. 2003a. Largescale cultivation of acidophilic hyperthermophiles for recovery of secreted proteins. Appl Environ Microbiol 69: 252-257. (Pubitemid 36077482)
59. Worthington P, Hoang V, Perez-Pomares F, Blum P. 2003b. Targeted disruption of the α-amylase gene in the hyperthermophilic archaeon Sulfolobus solfataricus. J Bacteriol 185: 482-488. (Pubitemid 36070474)
60. Wurtzel O, Sapra R, Chen F, Zhu Y, Simmons BA, Sorek R. 2010. A single-base resolution map of an archaeal transcriptome. Genome Res 20: 133-141.
61. Yamamoto N, Maeda Y, Ikeda A, Sakurai H. 2008. Regulation of thermotolerance by stress-induced transcription factors in Saccharomyces cerevisiae. Eukaryot Cell 7: 783-790. (Pubitemid 351968822)
62. Zuker M. 2003. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31: 3406-3415. (Pubitemid 37442169)