Functional genomics via metabolic footprinting: Monitoring metabolite secretion by Escherichia coli tryptophan metabolism mutants using FT-IR and direct injection electrospray mass spectrometry

Comparative and Functional Genomics

Volumn 4, Issue 4, 2003, Pages 376-391

  Kaderbhai, Naheed N ^a   Broadhurst, David I ^a   Ellis, David I ^a   Goodacre, Royston ^a,b   Kell, Douglas B ^a,b  

^a ABERYSTWYTH UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Escherichia coli; FTIR spectroscopy; Genetic algorithm; Mass spectrometry; Metabolic footprinting; Metabolome; Metabolomics; Tryptophan

Indexed keywords

BACTERIAL RNA; MESSENGER RNA;

BACTERIAL METABOLISM; BACTERIAL STRAIN; BACTERIUM IDENTIFICATION; BACTERIUM MUTANT; CONTROLLED STUDY; CULTURE MEDIUM; GENE LIBRARY; GENETIC ALGORITHM; GENOMICS; HYPOTHESIS; INFRARED SPECTROSCOPY; KNOCKOUT GENE; MASS SPECTROMETRY; METABOLITE; METHODOLOGY; NONHUMAN; PRIORITY JOURNAL; PUBLICATION; REPRODUCIBILITY; REVIEW; RNA ANALYSIS; TRYPTOPHAN METABOLISM; WILD TYPE;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 0043282812     PISSN: 15316912     EISSN: None     Source Type: Journal    
DOI: 10.1002/cfg.302     Document Type: Review

References (122)

1. Abel CBL, Lindon JC, Noble D, et al. 1999. Characterization of metabolites in intact Streptomyces citricolor culture supernatants using high-resolution nuclear magnetic resonance and directly coupled high-pressure liquid chromatography - nuclear magnetic resonance spectroscopy. Anal Biochem 270: 220-230.
2. Akashi H, Gojobori T. 2002. Metabolic efficiency and amino acid composition in the proteomes of Escherichia coli and Bacillus subtilis. Proc Natl Acad Sci USA 99: 3695-3700.
3. Allen JK, Davey HM, Broadhurst D, et al. 2003. Metabolic footprinting: a high-throughput, high-information approach to cellular characterisation and functional genomics. Nature Biotechnol 21: 692-696.
4. Auer G, Alaiya A, Bergman AC, Bergman T. 1998. From genome to proteome: multiple gene expression analysis in human tumors. Cytology: Abstracts; XIIIth International Congress of Cytology, Tokyo, Japan, May 10-14, 1998; 460.
5. Beavis RB, Colby SM, Goodacre R, et al. 2000. Artificial intelligence and expert systems in mass spectrometry. In Encyclopedia of Analytical Chemistry, Meyers RA (ed.). Wiley: Chichester; 11558-11597.
6. Benton D. 1996. Bioinformatics - principles and potential of a new multidisciplinary tool. Trends Biotechnol 14: 261-272.
7. Blattner FR, Plunket G, Perna N, et al. 1998. Comparative genome sequencing of E. coli O157:H7 vs. E. coli K-12. In Proceedings of the 1998 Miami Bio/Technology Winter Symposium, Ahmad F, Baumbach L, Bernstein P, et al. (eds). IRL Press: Oxford; 3-4.
8. Blattner FR, Plunkett G, Bloch A, et al. 1997. The complete genome sequence of Escherichia coli K-12. Science 277: 1453-1474.
9. Brent R. 1999. Functional genomics: learning to think about gene expression data. Curr Biol 9: R338-341.
10. Brent R. 2000. Genomic biology. Cell 100: 169-183.
11. Broadhurst D, Goodacre R, Jones A, Rowland JJ, Kell DB. 1997. Genetic algorithms as a method for variable selection in multiple linear regression and partial least squares regression, with applications to pyrolysis mass spectrometry. Anal Chim Acta 348: 71-86.
12. Buchholz A, Takors R, Wandrey C. 2001. Quantification of intracellular metabolites in Escherichia coli K12 using liquid chromatographic-electrospray ionization tandem mass spectrometric techniques. Anal Biochem 295: 129-137.
13. Burge CB. 2001. Chipping away at the transcriptome. Nature Genet 27: 232-233.
14. Caceres A, Cardenas S, Gallego M, Rodriguez A, Valcarcel M. 2000. Automated flow system on-line to LC with post-column derivatization for determination of sugars in carbohydrate-rich foods. Chromatographia 52: 314-318.
15. Causton DR. 1987. A Biologist's Advanced Mathematics. Allen and Unwin: London.
16. Champion KM, Nishihara JC, Joly JC, Arnott D. 2001. Similarity of the Escherichia coli proteome upon completion of different biopharmaceutical fermentation processes. Proteomics 1: 1133-1148.
17. Choe LH, Chen W, Lee KH. 1998. Proteome analysis of factor for inversion stimulation (Fis) overproduction in Escherichia coli. In Two-dimensional Electrophoresis: From Genome to Proteome. Wiley-VCH: Siena, Italy; 798-805.
18. Clare A, King RD. 2002. Machine learning of functional class from phenotype data. Bioinformatics 18: 160-166.
19. Cole RB (ed.). 1997. Electrospray Ionization Mass Spectrometry: Fundamentals, Instrumentation and Applications. Wiley: New York.
20. Cook WJ, Cunningham WH, Pulleyblank WR, Schrijver A. 1998. Combinatorial Optimization. Wiley: New York.
21. Cornish-Bowden A, Cardenas ML. 2000. From genome to cellular phenotype - a role for metabolic flux analysis? Nature Biotechnol 18: 267-269.
22. Covert MW, Schilling CH, Famili I, et al. 2001. Metabolic modeling of microbial strains in silico. Trends Biochem Sci 26: 179-186.
23. De Koning W, van Dam K. 1992. A method for the determination of changes of glycolytic metabolites in yeast on a subsecond time scale using extraction at neutral pH. Anal Biochem 204: 118-123.
24. Devaux F, Marc P, Jacq C. 2001. Transcriptomes, transcription activators and microarrays. FEBS Lett 498: 140-144.
25. Dunn M. 1998. Proteome analysis: chemists are analysing the total protein content of organisms to gain insights into complex cellular processes and accelerate the drug discovery process. Chem Br 34: 54-58.
26. Featherstone DE, Broadie K. 2002. Wrestling with pleiotropy: genomic and topological analysis of the yeast gene expression network. Bioessays 24: 267-274.
27. Fiehn O. 2001. Combining genomics, metabolome analysis, and biochemical modelling to understand metabolic networks. Comp Funct Genom 2: 155-168.
28. Fiehn O. 2002. Metabolomics: the link between genotypes and phenotypes. Plant Mol Biol 48: 155-171.
29. Fiehn O, Kloska S, Altmann T. 2001. Integrated studies on plant biology using multiparallel techniques. Curr Opin Biotechnol 12: 82-86.
30. Fiehn O, Kopka J, Dormann P, et al. 2000. Metabolite profiling for plant functional genomics. Nature Biotechnol 18: 1157-1161.
31. Futcher B, Latter GI, Monardo P, McLaughlin CS, Garrels JI. 1999. A sampling of the yeast proteome. Mol Cell Biol 19: 7357-7368.
32. Futcher B, Latter J, Monardo P, McLaughlin C. 1997. The S. cerevisiae proteome. In Yeast Cell Biology. Cold Spring Harbor Laboratory Press: New York; 78.
33. Gaskell SJ. 1997. Electrospray: principles and practice. J Mass Spectrom 32: 677-688.
34. Goodacre R, Heald JK, Kell DB. 1999. Characterization of intact microorganisms using electrospray ionization mass spectrometry. FEMS Microbiol Lett 176: 17-24.
35. Goodacre R, Kell DB. 1993. Rapid and quantitative analysis of bioprocesses using pyrolysis mass spectrometry and neural networks: application to indole production. Anal Chim Acta 279: 17.
36. Goodacre R, Kell DB. 2003. Evolutionary computation for the interpretation of metabolome data. In Metabolic Profiling: Its, Role in Biomarker Discovery and Gene Function Analysis, Harrigan GG, Goodacre R (eds). Kluwer Academic: Dordrecht; 239-256.
37. Goodacre R, Rooney PJ, Kell DB. 1998a. Rapid analysis of microbial systems using vibrational spectroscopy and supervised learning methods: application to the discrimination between methicillin-resistant and methicillin-susceptible Staphylococcus aureus. Proceedings of SPIE: Infrared Spectroscopy: New Tool in Medicine, San Jose, CA; 220-229.
38. Goodacre R, Shann B, Gilbert RJ, et al. 2000. Detection of the dipicolinic acid biomarker in Bacillus spores using Curie-point pyrolysis mass spectrometry and Fourier transform infrared spectroscopy. Anal Chem 72: 119-127.
39. Goodacre R, Timmins ÉM, Burton R, et al. 1998b. Rapid identification of urinary tract infection bacteria using hyperspectral whole-organism fingerprinting and artificial neural networks. Microbiology UK 144: 1157-1170.
40. Goodacre R, Vaidyanathan S, Bianchi G, Kell DB. 2002. Metabolic profiling using direct infusion electrospray ionization mass spectrometry for the characterization of olive oils. Analyst 127: 1457-1462.
41. Goodacre R, York EV, Heald JK, Scott IM. 2003. Chemometric discrimination of unfractionated plant extracts profiled by flow-injection electrospray mass spectrometry. Phytochemistry 62: 859-863.
42. Goryanin I, Hodgman TC, Selkov E. 1999. Mathematical simulation and analysis of cellular metabolism and regulation. Bioinformatics 15: 749-758.
43. Hall R, Beale M, Fiehn O, Hardy N, Sumner L, Bino R. 2002. Plant metabolomics: the missing link in functional genomics strategies. Plant Cell 14: 1437-1440.
44. Han MJ, Yoon SS, Lee SY. 2001. Proteome analysis of metabolically engineered Escherichia coli producing poly(3-hydroxybutyrate). J Bacteriol 183: 301-308.
45. Hartbrich A, Schmitz G, Weuster-Botz D, De Graaf AA, Wandrey C. 1996. Development and application of a membrane cyclone reactor for in vivo NMR spectroscopy with high microbial cell densities. Biotechnol Bioeng 51: 624-635.
46. Hastie T, Tibshirani R, Friedman J. 2001. The Elements of Statistical Learning: Data Mining, Inference and Prediction. Springer-Verlag: Berlin.
47. Heatwole VM, Somerville RL. 1992. Synergism between the trp repressor and tyr repressor in repression of the arol promoter of Escherichia coli. J Bacteriol 174: 331-335.
48. Hieter P, Boguski M. 1997. Functional genomics: it's all how you read it. Science 278: 601-602.
49. Ilic N, Oestin A, Cohen JD. 1999. Differential inhibition of indole-3-acetic acid and tryptophan biosynthesis by indole analogues. I. Tryptophan-dependent IAA biosynthesis. Plant Growth Reg 27: 57-62.
50. Isaacs H, Chao D, Yanofsky C, Saier MH. 1994. Mechanism of catabolite repression of tryptophanase synthesis in Escherichia coli. Microbiology - Reading 140: 2125-2134.
51. Johnson HE, Gilbert RJ, Winson MK, et al. 2000. Explanatory analysis of the metabolome using genetic programming of simple, interpretable rules. Genetic Progr Evolvable Machines 1: 243-258.
52. Jolliffe IT. 1986. Principal Component Analysis. Springer-Verlag: Berlin.
53. Joubert-Caron R, Caron M. 1999. Proteome and proteomics: new concepts for new fields of application in biomedicine. Med Sci 15: 701-705.
54. Jurgen B, Hanschke R, Sarvas M, Hecker M, Schweder T. 2001. Proteome and transcriptome based analysis of Bacillus subtilis cells overproducing an insoluble heterologous protein. Appl Microbiol Biotechnol 55: 326-332.
55. Kabir MM, Shimizu K. 2001. Proteome analysis of a temperature-inducible recombinant Escherichia coli for poly-β-hydroxybutyrate production. J Biosci Bioeng 92: 277-284.
56. Kamath AV, Yanofsky C. 1992. Characterization of the tryptophanase operon of Proteus vulgaris. Cloning, nucleotide sequence, amino acid homology, and in vitro synthesis of the leader peptide and regulatory analysis. J Biol Chem 267: 19 978-19 985.
57. Kanehisa M, Goto S. 2000. KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res 28: 27-30.
58. Karp PD, Riley M, Paley SM, Pelligrini-Toole A. 1996. EcoCyc: an encyclopedia of Escherichia coli genes and metabolism. Nucleic Acids Res 24: 32-39.
59. Karp PD, Riley M, Saier M, et al. 2002a. The EcoCyc database. Nucleic Acids Res 30: 56-58.
60. Karp PD, Riley M, Saier M, et al. 2000b. The EcoCyc and MetaCyc databases. Nucleic Acids Res 28: 56-59.
61. Kell DB, King RD. 2000. On the optimization of classes for the assignment of unidentified reading frames in functional genomics programmes: the need for machine learning. Trends Biotechnol 18: 93-98.
62. Kell DB, Mendes P. 2000. Snapshots of systems: metabolic control analysis and biotechnology in the post-genomic era. In Technological and Medical Implications of Metabolic Control Analysis, Cornish-Bowden A, Cárdenas ML (eds). Kluwer Academic: Dordrecht; 3-25 (and see http://qbab.aber.ac.uk/dbk/mca99.htm).
63. Khodursky AB, Peter BJ, Cozzarelli NR, et al. 2000a. DNA microarray analysis of gene expression in response to physiological and genetic changes that affect tryptophan metabolism in Escherichia coli. Colloquium on Auditory Neuroscience: Development, Transduction and Integration, Irvine, CA; 12 170-12 175.
64. Khodursky AB, Peter BJ, Cozzarelli NR, et al. 2000b. DNA microarray analysis of gene expression in response to physiological and genetic changes that affect tryptophan metabolism in Escherichia coli. Proc Natl Acad Sci USA 97: 12 170-12 175.
65. King RD, Karwath A, Clare A, Dehaspe L. 2000. Accurate prediction of protein functional class from sequence in the Mycobacterium tuberculosis and Escherichia coli genomes using data mining. Yeast 17: 283-293.
66. Kose F, Weckwerth W, Linke T, Fiehn O. 2001. Visualizing plant metabolomic correlation networks using clique-metabolite matrices. Bioinformatics 17: 1198-1208.
67. Kramer R. 1994. Systems and mechanisms of amino acid uptake and excretion in prokaryotes. Arch Microbiol 162: 1-13.
68. Krishnamurthy T, Davis MT, Stahl DC, Lee TD. 1999. Liquid chromatography microspray mass spectrometry for bacterial investigations. Rapid Commun Mass Spectrom 13: 39-49.
69. Liang P, Labedan B, Riley M. 2002. Physiological genomics of Escherichia coli protein families. Physiol Genom 9: 15-26.
70. Liu XQ, Ng C, Ferenci T. 2000. Global adaptations resulting from high population densities in Escherichia coli cultures. J Bacteriol 182: 4158-4164.
71. Loo RRO, Cavalcoli JD, VanBogelen RA, et al. 2001. Virtual 2D gel electrophoresis: visualization and analysis of the E. coli proteome by mass spectrometry. Anal Chem 73: 4063-4070.
72. Magera MJ, Matern D, Rinaldo P. 2000. A method for the quantitative determination of methylmalonic acid in plasma by LC-MS/MS stable isotope dilution analysis. In Inborn Errors of Metabolism. Kluwer Academic Press: Cambridge; 96.
73. Manly BFJ. 1994. Multivariate Statistical Methods: A Primer. Chapman and Hall: London.
74. Martens H, Næs T. 1989. Multivariate Calibration. Wiley: New York.
75. McGovern AC, Broadhurst D, Taylor J, et al. 2002. Monitoring of complex industrial bioprocesses for metabolite concentrations using modern spectroscopies and machine learning: application to gibberellic acid production. Biotechnol Bioeng 78: 527-538.
76. McGovern AC, Ernill R, Kara BV, Kell DB, Goodacre R. 1999. Rapid analysis of the expression of heterologous proteins in Escherichia coli using pyrolysis mass spectrometry and Fourier transform infrared spectroscopy with chemometrics: application to α2-interferon production. J Biotechnol 72: 157-167.
77. Mendes P. 2002. Emerging bioinformatics for the metabolome. Brief Bioinform 3: 134-145.
78. Meyer S, Noisommit Rizzi N, Reuss M, Neubauer P. 1999. Optimized analysis of intracellular adenosine and guanosine phosphates in Escherichia coli. Anal Biochem 271: 43-52.
79. Michal G (ed.) 1999. Biochemical Pathways: An Atlas of Biochemistry and Molecular Biology. Wiley: New York.
80. Mohammed N, Onodera R, Khan RI. 1999. Tryptophan biosynthesis and production of other related compounds from indolepyruvic acid by mixed ruminal bacteria, protozoa, and their mixture in vitro. J Gen Appl Microbiol Tokyo 45: 143-148.
81. Morris M, Cooper D. 2000. Rapid analysis of amino acid isomers by LC-MS/MS. In Inborn Errors of Metabolism. Kluwer Academic Press: Cambridge; 273.
82. Naumann D, Keller S, Helm D, Schultz C, Schrader B. 1995. FT-IR spectroscopy and FT-Raman spectroscopy are powerful analytical tools for the non-invasive characterization of intact microbial cells. J Mol Struct 347: 399-405.
83. Nicholson JK, Lindon JC, Holmes E. 1999. 'Metabonomics': understanding the metabolic responses of living systems to pathophysiological stimuli via multivariate statistical analysis of biological NMR spectroscopic data. Xenobiotica 29: 1181-1189.
84. Oliver SG. 1996. From DNA sequence to biological function. Nature 379: 597-600.
85. Oliver SG. 1997. Yeast as a navigational aid in genome analysis. Microbiol UK 143: 1483-1487.
86. Oliver SG. 2000. Proteomics: guilt-by-association goes global. Nature 403: 601-603.
87. Oliver SG, Winson MK, Kell DB, Baganz F. 1998. Systematic functional analysis of the yeast genome. Trends Biotechnol 16: 373-378.
88. Oshima T, Aiba H, Masuda Y, et al. 2002. Transcriptome analysis of all two-component regulatory system mutants of Escherichia coli K-12. Mol Microbiol 46: 281-291.
89. Ouzounis CA, Karp PD. 2000. Global properties of the metabolic map of Escherichia coli. Genome Res 10: 568-576.
90. Prinsen E, Van Dongen W, Esmans EL, Van Onckelen HA. 1997. HPLC linked electrospray tandem mass spectrometry: a rapid and reliable method to analyse indole-3-acetic acid metabolism in bacteria. J Mass Spectrom 32: 12-22.
91. Raamsdonk LM, Teusink B, Broadhurst D, et al. 2001. A functional genomics strategy that uses metabolome data to reveal the phenotype of silent mutations. Nat Biotechnol 19: 45-50.
92. Radovic BS, Goodacre R, Anklam E. 2001. Contribution of pyrolysis mass spectrometry (Py-MS) to authenticity testing of honey. J Anal Appl Pyrol 60: 79-87.
93. Rashed MS, Bucknall MP, Little D, et al. 1997. Screening blood spots for inborn errors of metabolism by electrospray tandem mass spectrometry with a microplate batch process and a computer algorithm for automated flagging of abnormal profiles. Clin Chem 43: 1129-1141.
94. Riley M, Serres MH. 2000. Interim report on genomics of Escherichia coli. Ann Rev Microbiol 54: 341-411.
95. Roessner U, Luedemann A, Brust D, et al. 2001. Metabolic profiling allows comprehensive phenotyping of genetically or environmentally modified plant systems. Plant Cell 13: 11-29.
96. Schilling CH, Palsson BO. 2000. Assessment of the metabolic capabilities of Haemophilus influenzae Rd through a genome-scale pathway analysis. J Theor Biol 203: 249-283.
97. Shaw AD, Kaderbhai N, Jones A, et al. 1999a. Non-invasive, online monitoring of the biotransformation by yeast of glucose to ethanol using dispersive Raman spectroscopy and chemometrics. Appl Spectrosc 53: 1419-1428.
98. Shaw AD, Winson MK, Woodward AM, et al. 1999b. Rapid analysis of high-dimensional bioprocesses using multivariate spectroscopies and advanced chemometrics. Adv Biochem Eng 66: 83-113.
99. Skolnick J, Fetrow JS, Kolinski A. 2000. Structural genomics and its importance for gene function analysis. Nature Biotechnol 18: 283-287.
100. Smith TF. 1998. Functional genomics - bioinformatics is ready for the challenge. Trends Genet 14: 291-293.
101. Tao H, Bausch C, Richmond C, Blattner FR, Conway T. 1999. Functional genomics: expression analysis of Escherichia coli growing on minimal and rich media. J Bacteriol 181: 6425-6440.
102. Taylor J, Goodacre R, Wade WG, Rowland JJ, Kell DB. 1998. The deconvolution of pyrolysis mass spectra using genetic programming: application to the identification of some Eubacterium species. FEMS Microbiol Lett 160: 237-246.
103. Taylor J, King RD, Altmann T, Fiehn O. 2002. Application of metabolomics to plant genotype discrimination using statistics and machine learning. Bioinformatics 18(suppl 2): S241-248.
104. ter Kuile BH, Westerhoff HV. 2001. Transcriptome meets metabolome: hierarchical and metabolic regulation of the glycolytic pathway. FEBS Lett 500: 169-171.
105. Thomas GH. 1999. Completing the E. coli proteome: a database of gene products characterized since the completion of the genome sequence. Bioinformatics 15: 860-861.
106. n. Am Biotechnol Lab 18: 58-79.
107. Timmins ÉM, Howell SA, Alsberg BK, Noble WC, Goodacre R. 1998. Rapid differentiation of closely related Candida species and strains by pyrolysis mass spectrometry and Fourier transform infrared spectroscopy. J Clin Microbiol 36: 367-374.
108. Tjaden B, Saxena RM, Stolyar SI, et al. 2002. Transcriptome analysis of Escherichia coli using high-density oligonucleotide probe arrays. Nucleic Acids Res 30: 3732-3738.
109. Tomita M, Hashimoto K, Takahashi K, et al. 1999. E-CELL: software environment for whole-cell simulation. Bioinformatics 15: 72-84.
110. Tweeddale H, Notley-McRobb L, Ferenci T. 1998. Effect of slow growth on metabolism of Escherichia coli, as revealed by global metabolite pool ('metabolome') analysis. J Bacteriol 180: 5109-5116.
111. Tweeddale H, Notley-McRobb L, Ferenci T. 1999. Assessing the effect of reactive oxygen species on Escherichia coli using a metabolome approach. Redox Rep 4: 237-241.
112. Vaidyanathan S, Kell DB, Goodacre R. 2002. Rapid bacterial identification using flow-injection electrospray ionization mass spectrometry of whole cell extracts. J Am Soc Mass Spectrom 13: 118-128.
113. Vaidyanathan S, Rowland JJ, Kell DB, Goodacre R. 2001. Rapid discrimination of aerobic endospore-forming bacteria via electrospray ionization mass spectrometry of whole cell suspensions. Anal Chem 73: 4134-4144.
114. van Eijk HMH, Rooyakkers DR, Soeters PB, Deutz NEP. 1999. Determination of amino acid isotope enrichment using liquid chromatography-mass spectrometry. Anal Biochem 271: 8-17.
115. Warne MA, Lenz EM, Osborn D, Weeks JM, Nicholson JK. 2000. An NMR-based metabonomic investigation of the toxic effects of 3-trifluoromethyl-aniline on the earthworm Eisenia veneta. Biomarkers 5: 56-72.
116. Winson MK, Goodacre R, Timmins EM, et al. 1997. Diffuse reflectance absorbance spectroscopy taking in chemometrics (DRASTIC). A hyperspectral FT-IR-based approach to rapid screening for metabolite overproduction. Anal Chim Acta 348: 273-282.
117. Winson MK, Todd M, Rudd BAM, et al. 1998. A DRASTIC (Diffuse Reflectance Absorbance Spectroscopy Taking in Chemometrics) approach for the rapid analysis of microbial fermentation products: quantification of Aristeromycin and Neplanocin A in Streptomyces citricolor broths. In New Frontiers in Screening for Microbial Biocatalysts, Kieslich K, van der Beek CP, de Bont JAM, van den Tweel WJJ (eds). Elsevier: Amsterdam; 185-191.
118. Wixon J, Kell DB. 2000. The Kyoto Encyclopedia of Genes and Genomes - KEGG: http://www.genome.ad.jp/kegg. Yeast 17: 48-55.
119. Yanofsky C. 2000. Transcription attenuation: once viewed as a novel regulatory strategy. J Bacteriol 182: 1-8.
120. Yanofsky C, Horn V. 1994. Role of regulatory features of the trp operon of Escherichia coli in mediating a response to a nutritional shift. J Bacteriol 176: 6245-6254.
121. Yanofsky C, Konan KV, Sarsero JP. 1996. Some novel transcription attenuation mechanisms used by bacteria. Posttranscriptional Control of Gene Expression: The Regulatory Role of RNA. Elsevier: Hakone, Japan; 1017-1024.
122. Yanofsky C, Muh Ching Y, Horn V. 1993. Partial revertants of tryptophan synthetase α-chain active site mutant Asp60-Asn. J Biol Chem 268: 8213.