Regulatory network features in Listeria monocytogenes-Changing the way we talk

Frontiers in Cellular and Infection Microbiology

Volumn 5, Issue FEB, 2014, Pages

  Guariglia Oropeza, Veronica ^a   Orsi, Renato H ^a   Yu, Haiyuan ^b,c   Boor, Kathryn J ^a   Wiedmann, Martin ^a   Guldimann, Claudia ^a  

^a Department of Obstetrics Gynecology   (United States)

^b Program on Infrastructure Policy   (United States)

^c School of Integrative Plant Sciences   (United States)

Author keywords

Listeria monocytogenes; Network motif; PrfA; Regulatory network; SigB

Indexed keywords

CTSR PROTEIN; ENDOPEPTIDASE CLP; GLUCOSAMINE 6 PHOSPHATE DEAMINASE; N ACETYLGLUCOSAMINE 6 PHOSPHATE DEACETYLASE; PEPTIDES AND PROTEINS; PRFA PROTEIN; SREA PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

AUTOREGULATION; BACTERIAL VIRULENCE; CELLULAR STRESS RESPONSE; DOWN REGULATION; GENE REGULATORY NETWORK; GENETIC TRANSCRIPTION; LISTERIA MONOCYTOGENES; MATHEMATICAL MODEL; NONHUMAN; SHORT SURVEY; UPREGULATION; GENE EXPRESSION REGULATION; GENETICS; NETWORK MOTIF; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PRFA; REGULATORY NETWORK; REVIEW; SIGB; SYSTEMS BIOLOGY; VIRULENCE;

LISTERIA MONOCYTOGENES; NETWORK MOTIF; PRFA; REGULATORY NETWORK; SIGB;

GENE EXPRESSION REGULATION, BACTERIAL; GENE REGULATORY NETWORKS; LISTERIA MONOCYTOGENES; STRESS, PHYSIOLOGICAL; SYSTEMS BIOLOGY; VIRULENCE;

EID: 84897920341     PISSN: None     EISSN: 22352988     Source Type: Journal    
DOI: 10.3389/fcimb.2014.00014     Document Type: Short Survey

References (82)

1. Ake, F. M., Joyet, P., Deutscher, J., and Milohanic, E. (2011). Mutational analysis of glucose transport regulation and glucose-mediated virulence gene repression in Listeria monocytogenes. Mol. Microbiol. 81, 274-293. doi: 10.1111/j.1365-2958.2011.07692.x.
2. Alon, U. (2007). Network motifs: theory and experimental approaches. Nat. Rev. Genet. 8, 450-461. doi: 10.1038/nrg2102.
3. Arous, S., Buchrieser, C., Folio, P., Glaser, P., Namane, A., Hebraud, M., et al. (2004). Global analysis of gene expression in an rpoN mutant of Listeria monocytogenes. Microbiology 150(Pt 5), 1581-1590. doi: 10.1099/mic.0.26860-0.
4. Autret, N., Raynaud, C., Dubail, I., Berche, P., and Charbit, A. (2003). Identification of the agr locus of Listeria monocytogenes: role in bacterial virulence. Infect. Immun. 71, 4463-4471. doi: 10.1128/IAI.71.8.4463-4471.2003.
5. Barabasi, A. L., and Oltvai, Z. N. (2004). Network biology: understanding the cell's functional organization. Nat. Rev. Genet. 5, 101-113. doi: 10.1038/nrg1272.
6. Becskei, A., and Serrano, L. (2000). Engineering stability in gene networks by autoregulation. Nature 405, 590-593. doi: 10.1038/35014651.
7. Bennett, H. J., Pearce, D. M., Glenn, S., Taylor, C. M., Kuhn, M., Sonenshein, A. L., et al. (2007). Characterization of relA and codY mutants of Listeria monocytogenes: identification of the CodY regulon and its role in virulence. Mol. Microbiol. 63, 1453-1467. doi: 10.1111/j.1365-2958.2007.05597.x.
8. Bertram, R., Rigali, S., Wood, N., Lulko, A. T., Kuipers, O. P., and Titgemeyer, F. (2011). Regulon of the N-acetylglucosamine utilization regulator NagR in Bacillus subtilis. J. Bacteriol. 193, 3525-3536. doi: 10.1128/JB.00264-11.
9. Bonneau, R., Facciotti, M. T., Reiss, D. J., Schmid, A. K., Pan, M., Kaur, A., et al. (2007). A predictive model for transcriptional control of physiology in a free living cell. Cell 131, 1354-1365. doi: 10.1016/j.cell.2007.10.053.
10. Chan, Y. C., Hu, Y., Chaturongakul, S., Files, K. D., Bowen, B. M., Boor, K. J., et al. (2008). Contributions of two-component regulatory systems, alternative sigma factors, and negative regulators to Listeria monocytogenes cold adaptation and cold growth. J. Food Prot. 71, 420-425.
11. Chaturongakul, S., and Boor, K. J. (2006). SigmaB activation under environmental and energy stress conditions in Listeria monocytogenes. Appl. Environ. Microbiol. 72, 5197-5203. doi: 10.1128/AEM.03058-05.
12. Chaturongakul, S., Raengpradub, S., Palmer, M. E., Bergholz, T. M., Orsi, R. H., Hu, Y., et al. (2011). Transcriptomic and phenotypic analyses identify coregulated, overlapping regulons among PrfA, CtsR, HrcA, and the alternative sigma factors sigmaB, sigmaC, sigmaH, and sigmaL in Listeria monocytogenes. Appl. Environ. Microbiol. 77, 187-200. doi: 10.1128/AEM.00952-10.
13. Chaturongakul, S., Raengpradub, S., Wiedmann, M., and Boor, K. J. (2008). Modulation of stress and virulence in Listeria monocytogenes. Trends Microbiol. 16, 388-396. doi: 10.1016/j.tim.2008.05.006.
14. Dalet, K., Cenatiempo, Y., Cossart, P., and Hechard, Y. (2001). A sigma(54)-dependent PTS permease of the mannose family is responsible for sensitivity of Listeria monocytogenes to mesentericin Y105. Microbiology 147, 3263-3269.
15. de Hoon, M. J., Eichenberger, P., and Vitkup, D. (2010). Hierarchical evolution of the bacterial sporulation network. Curr. Biol. 20, R735-R745. doi: 10.1016/j.cub.2010.06.031.
16. de Las Heras, A., Cain, R. J., Bielecka, M. K., and Vazquez-Boland, J. A. (2011). Regulation of Listeria virulence: PrfA master and commander. Curr. Opin. Microbiol. 14, 118-127. doi: 10.1016/j.mib.2011.01.005.
17. Dufour, Y. S., and Donohue, T. J. (2012). Signal correlations in ecological niches can shape the organization and evolution of bacterial gene regulatory networks. Adv. Microb. Physiol. 61, 1-36. doi: 10.1016/B978-0-12-394423-8.00001-9.
18. Dussurget, O., Cabanes, D., Dehoux, P., Lecuit, M., Buchrieser, C., Glaser, P., et al. (2002). Listeria monocytogenes bile salt hydrolase is a PrfA-regulated virulence factor involved in the intestinal and hepatic phases of listeriosis. Mol. Microbiol. 45, 1095-1106. doi: 10.1046/j.1365-2958.2002.03080.x.
19. Freitag, N. E., Port, G. C., and Miner, M. D. (2009). Listeria monocytogenes-from saprophyte to intracellular pathogen. Nat. Rev. Microbiol. 7, 623-628. doi: 10.1038/nrmicro2171.
20. Gaillot, O., Bregenholt, S., Jaubert, F., Di Santo, J. P., and Berche, P. (2001). Stress-induced ClpP serine protease of Listeria monocytogenes is essential for induction of listeriolysin O-dependent protective immunity. Infect. Immun. 69, 4938-4943. doi: 10.1128/IAI.69.8.4938-4943.2001.
21. Gaillot, O., Pellegrini, E., Bregenholt, S., Nair, S., and Berche, P. (2000). The ClpP serine protease is essential for the intracellular parasitism and virulence of Listeria monocytogenes. Mol. Microbiol. 35, 1286-1294. doi: 10.1046/j.1365-2958.2000.01773.x.
22. Garmyn, D., Augagneur, Y., Gal, L., Vivant, A. L., and Piveteau, P. (2012). Listeria monocytogenes differential transcriptome analysis reveals temperature-dependent Agr regulation and suggests overlaps with other regulons. PLoS ONE 7:e43154. doi: 10.1371/journal.pone.0043154.
23. Glaser, P., Frangeul, L., Buchrieser, C., Rusniok, C., Amend, A., Baquero, F., et al. (2001). Comparative genomics of Listeria species. Science 294, 849-852. doi: 10.1126/science.1063447.
24. Guelzim, N., Bottani, S., Bourgine, P., and Kepes, F. (2002). Topological and causal structure of the yeast transcriptional regulatory network. Nat. Genet. 31, 60-63. doi: 10.1038/ng873.
25. Hanawa, T., Kai, M., Kamiya, S., and Yamamoto, T. (2000). Cloning, sequencing, and transcriptional analysis of the dnaK heat shock operon of Listeria monocytogenes. Cell Stress Chaperones 5, 21-29. doi: 10.1379/1466-1268(2000)005%3C0021:CSATAO%3E2.0.CO;2.
26. Hu, Y., Oliver, H. F., Raengpradub, S., Palmer, M. E., Orsi, R. H., Wiedmann, M., et al. (2007b). Transcriptomic and phenotypic analyses suggest a network between the transcriptional regulators HrcA and sigmaB in Listeria monocytogenes. Appl. Environ. Microbiol. 73, 7981-7991. doi: 10.1128/AEM.01281-07.
27. Hu, Y., Raengpradub, S., Schwab, U., Loss, C., Orsi, R. H., Wiedmann, M., et al. (2007a). Phenotypic and transcriptomic analyses demonstrate interactions between the transcriptional regulators CtsR and Sigma B in Listeria monocytogenes. Appl. Environ. Microbiol. 73, 7967-7980. doi: 10.1128/AEM.01085-07.
28. Johansson, J., Mandin, P., Renzoni, A., Chiaruttini, C., Springer, M., and Cossart, P. (2002). An RNA thermosensor controls expression of virulence genes in Listeria monocytogenes. Cell 110, 551-561. doi: 10.1016/S0092-8674(02)00905-4.
29. Jones, B. V., Begley, M., Hill, C., Gahan, C. G., and Marchesi, J. R. (2008). Functional and comparative metagenomic analysis of bile salt hydrolase activity in the human gut microbiome. Proc. Natl. Acad. Sci. U.S.A. 105, 13580-13585. doi: 10.1073/pnas.0804437105.
30. Kamerlin, S. C., Vicatos, S., Dryga, A., and Warshel, A. (2011). Coarse-grained (multiscale) simulations in studies of biophysical and chemical systems. Annu. Rev. Phys. Chem. 62, 41-64. doi: 10.1146/annurev-physchem-032210-103335.
31. Kato, A., Latifi, T., and Groisman, E. A. (2003). Closing the loop: the PmrA/PmrB two-component system negatively controls expression of its posttranscriptional activator PmrD. Proc. Natl. Acad. Sci. U.S.A. 100, 4706-4711. doi: 10.1073/pnas.0836837100.
32. Kazmierczak, M. J., Mithoe, S. C., Boor, K. J., and Wiedmann, M. (2003). Listeria monocytogenes sigma B regulates stress response and virulence functions. J. Bacteriol. 185, 5722-5734. doi: 10.1128/JB.185.19.5722-5734.2003.
33. Kim, D., Kwon, Y. K., and Cho, K. H. (2008). The biphasic behavior of incoherent feed-forward loops in biomolecular regulatory networks. Bioessays 30, 1204-1211. doi: 10.1002/bies.20839.
34. Klinger, B., Sieber, A., Fritsche-Guenther, R., Witzel, F., Berry, L., Schumacher, D., et al. (2013). Network quantification of EGFR signaling unveils potential for targeted combination therapy. Mol. Syst. Biol. 9, 673. doi: 10.1038/msb.2013.29.
35. Kruger, E., Zuhlke, D., Witt, E., Ludwig, H., and Hecker, M. (2001). Clp-mediated proteolysis in Gram-positive bacteria is autoregulated by the stability of a repressor. EMBO J. 20, 852-863. doi: 10.1093/emboj/20.4.852.
36. Lee, T. I., Rinaldi, N. J., Robert, F., Odom, D. T., Bar-Joseph, Z., Gerber, G. K., et al. (2002). Transcriptional regulatory networks in Saccharomyces cerevisiae. Science 298, 799-804. doi: 10.1126/science.1075090.
37. Lingnau, A., Domann, E., Hudel, M., Bock, M., Nichterlein, T., Wehland, J., et al. (1995). Expression of the Listeria monocytogenes EGD inlA and inlB genes, whose products mediate bacterial entry into tissue culture cell lines, by PrfA-dependent and-independent mechanisms. Infect. Immun. 63, 3896-3903.
38. Lobel, L., Sigal, N., Borovok, I., Ruppin, E., and Herskovits, A. A. (2012). Integrative genomic analysis identifies isoleucine and CodY as regulators of Listeria monocytogenes virulence. PLoS Genet. 8:e1002887. doi: 10.1371/journal.pgen.1002887.
39. Loh, E., Dussurget, O., Gripenland, J., Vaitkevicius, K., Tiensuu, T., Mandin, P., et al. (2009). A trans-acting riboswitch controls expression of the virulence regulator PrfA in Listeria monocytogenes. Cell 139, 770-779. doi: 10.1016/j.cell.2009.08.046.
40. Mangan, S., and Alon, U. (2003). Structure and function of the feed-forward loop network motif. Proc. Natl. Acad. Sci. U.S.A. 100, 11980-11985. doi: 10.1073/pnas.2133841100.
41. Mangan, S., Zaslaver, A., and Alon, U. (2003). The coherent feedforward loop serves as a sign-sensitive delay element in transcription networks. J. Mol. Biol. 334, 197-204. doi: 10.1016/j.jmb.2003.09.049.
42. McAdams, H. H., and Arkin, A. (1997). Stochastic mechanisms in gene expression. Proc. Natl. Acad. Sci. U.S.A. 94, 814-819. doi: 10.1073/pnas.94.3.814.
43. McGann, P., Wiedmann, M., and Boor, K. J. (2007). The alternative sigma factor sigma B and the virulence gene regulator PrfA both regulate transcription of Listeria monocytogenes internalins. Appl. Environ. Microbiol. 73, 2919-2930. doi: 10.1128/AEM.02664-06.
44. Mellin, J. R., and Cossart, P. (2012). The non-coding RNA world of the bacterial pathogen Listeria monocytogenes. RNA Biol. 9, 372-378. doi: 10.4161/rna.19235.
45. Mengaud, J., Dramsi, S., Gouin, E., Vazquez-Boland, J. A., Milon, G., and Cossart, P. (1991). Pleiotropic control of Listeria monocytogenes virulence factors by a gene that is autoregulated. Mol. Microbiol. 5, 2273-2283. doi: 10.1111/j.1365-2958.1991.tb02158.x.
46. Middleton, A. M., Farcot, E., Owen, M. R., and Vernoux, T. (2012). Modeling regulatory networks to understand plant development: small is beautiful. Plant Cell 24, 3876-3891. doi: 10.1105/tpc.112.101840.
47. Mujahid, S., Orsi, R. H., Boor, K. J., and Wiedmann, M. (2013b). Protein level identification of the Listeria monocytogenes sigma H, sigma L, and sigma C regulons. BMC Microbiol. 13:156. doi: 10.1186/1471-2180-13-156.
48. Mujahid, S., Orsi, R. H., Vangay, P., Boor, K. J., and Wiedmann, M. (2013a). Refinement of the Listeria monocytogenes sigmaB regulon through quantitative proteomic analysis. Microbiology 159(Pt 6), 1109-1119. doi: 10.1099/mic.0.066001-0.
49. Nadon, C. A., Bowen, B. M., Wiedmann, M., and Boor, K. J. (2002). Sigma B contributes to PrfA-mediated virulence in Listeria monocytogenes. Infect. Immun. 70, 3948-3952. doi: 10.1128/IAI.70.7.3948-3952.2002.
50. Nair, S., Derre, I., Msadek, T., Gaillot, O., and Berche, P. (2000). CtsR controls class III heat shock gene expression in the human pathogen Listeria monocytogenes. Mol. Microbiol. 35, 800-811. doi: 10.1046/j.1365-2958.2000.01752.x.
51. O'Byrne, C. P., and Karatzas, K. A. (2008). The role of sigma B (sigma B) in the stress adaptations of Listeria monocytogenes: overlaps between stress adaptation and virulence. Adv. Appl. Microbiol. 65, 115-140. doi: 10.1016/S0065-2164(08)00605-9.
52. Oliver, H. F., Orsi, R. H., Ponnala, L., Keich, U., Wang, W., Sun, Q., et al. (2009). Deep RNA sequencing of L. monocytogenes reveals overlapping and extensive stationary phase and sigma B-dependent transcriptomes, including multiple highly transcribed noncoding RNAs. BMC Genomics 10:641. doi: 10.1186/1471-2164-10-641.
53. Oliver, H. F., Orsi, R. H., Wiedmann, M., and Boor, K. J. (2010). Listeria monocytogenes {sigma} B has a small core regulon and a conserved role in virulence but makes differential contributions to stress tolerance across a diverse collection of strains. Appl. Environ. Microbiol. 76, 4216-4232. doi: 10.1128/AEM.00031-10.
54. Ollinger, J., Bowen, B., Wiedmann, M., Boor, K. J., and Bergholz, T. M. (2009). Listeria monocytogenes sigmaB modulates PrfA-mediated virulence factor expression. Infect. Immun. 77, 2113-2124. doi: 10.1128/IAI.01205-08.
55. Popowska, M., Osinska, M., and Rzeczkowska, M. (2012). N-acetylglucosamine-6-phosphate deacetylase (NagA) of Listeria monocytogenes EGD, an essential enzyme for the metabolism and recycling of amino sugars. Arch. Microbiol. 194, 255-268. doi: 10.1007/s00203-011-0752-3.
56. Raengpradub, S., Wiedmann, M., and Boor, K. J. (2008). Comparative analysis of the sigma B-dependent stress responses in Listeria monocytogenes and Listeria innocua strains exposed to selected stress conditions. Appl. Environ. Microbiol. 74, 158-171. doi: 10.1128/AEM.00951-07.
57. Raimann, E., Schmid, B., Stephan, R., and Tasara, T. (2009). The alternative sigma factor sigma(L) of L. monocytogenes promotes growth under diverse environmental stresses. Foodborne Pathog. Dis. 6, 583-591. doi: 10.1089/fpd.2008.0248.
58. Rea, R. B., Gahan, C. G., and Hill, C. (2004). Disruption of putative regulatory loci in Listeria monocytogenes demonstrates a significant role for Fur and PerR in virulence. Infect. Immun. 72, 717-727. doi: 10.1128/IAI.72.2.717-727.2004.
59. Resch, M., Schiltz, E., Titgemeyer, F., and Muller, Y. A. (2010). Insight into the induction mechanism of the GntR/HutC bacterial transcription regulator YvoA. Nucleic Acids Res. 38, 2485-2497. doi: 10.1093/nar/gkp1191.
60. Ruiz, N., Peterson, C. N., and Silhavy, T. J. (2001). RpoS-dependent transcriptional control of sprE: regulatory feedback loop. J. Bacteriol. 183, 5974-5981. doi: 10.1128/JB.183.20.5974-5981.2001.
61. Schwab, U., Bowen, B., Nadon, C., Wiedmann, M., and Boor, K. J. (2005). The Listeria monocytogenes prfAP2 promoter is regulated by sigma B in a growth phase dependent manner. FEMS Microbiol. Lett. 245, 329-336. doi: 10.1016/j.femsle.2005.03.025.
62. Scortti, M., Monzo, H. J., Lacharme-Lora, L., Lewis, D. A., and Vazquez-Boland, J. A. (2007). The PrfA virulence regulon. Microbes Infect. 9, 1196-1207. doi: 10.1016/j.micinf.2007.05.007.
63. Seifart, G. C., Izar, B., Pazan, F., Mohamed, W., Mraheil, M. A., Mukherjee, K., et al. (2011). Universal stress proteins are important for oxidative and acid stress resistance and growth of Listeria monocytogenes EGD-e in vitro and in vivo. PLoS ONE 6:e24965. doi: 10.1371/journal.pone.0024965.
64. Shen-Orr, S. S., Milo, R., Mangan, S., and Alon, U. (2002). Network motifs in the transcriptional regulation network of Escherichia coli. Nat. Genet. 31, 64-68. doi: 10.1038/ng881.
65. Snoep, J. L., Bruggeman, F., Olivier, B. G., and Westerhoff, H. V. (2006). Towards building the silicon cell: a modular approach. Biosystems 83, 207-216. doi: 10.1016/j.biosystems.2005.07.006.
66. Sue, D., Boor, K. J., and Wiedmann, M. (2003). Sigma(B)-dependent expression patterns of compatible solute transporter genes opuCA and lmo1421 and the conjugated bile salt hydrolase gene bsh in Listeria monocytogenes. Microbiology 149(Pt 11), 3247-3256. doi: 10.1099/mic.0.26526-0.
67. Sue, D., Fink, D., Wiedmann, M., and Boor, K. J. (2004). SigmaB-dependent gene induction and expression in Listeria monocytogenes during osmotic and acid stress conditions simulating the intestinal environment. Microbiology 150(Pt 11), 3843-3855. doi: 10.1099/mic.0.27257-0.
68. Tessema, G. T., Moretro, T., Kohler, A., Axelsson, L., and Naterstad, K. (2009). Complex phenotypic and genotypic responses of Listeria monocytogenes strains exposed to the class IIa bacteriocin sakacin P. Appl. Environ. Microbiol. 75, 6973-6980. doi: 10.1128/AEM.00608-09.
69. Tessema, G. T., Moretro, T., Snipen, L., Heir, E., Holck, A., Naterstad, K., et al. (2012). Microarray-based transcriptome of Listeria monocytogenes adapted to sublethal concentrations of acetic acid, lactic acid, and hydrochloric acid. Can. J. Microbiol. 58, 1112-1123. doi: 10.1139/w2012-091.
70. Thattai, M., and van Oudenaarden, A. (2001). Intrinsic noise in gene regulatory networks. Proc. Natl. Acad. Sci. U.S.A. 98, 8614-8619. doi: 10.1073/pnas.151588598.
71. Thieffry, D., Huerta, A. M., Perez-Rueda, E., and Collado-Vides, J. (1998). From specific gene regulation to genomic networks: a global analysis of transcriptional regulation in Escherichia coli. Bioessays 20, 433-440. doi: 10.1002/(SICI)1521-1878(199805)20:5<433::AID-BIES10>3.0.CO;2-2.
72. Tyson, J. J., and Novak, B. (2010). Functional motifs in biochemical reaction networks. Annu. Rev. Phys. Chem. 61, 219-240. doi: 10.1146/annurev.physchem.012809.103457.
73. Utratna, M., Cosgrave, E., Baustian, C., Ceredig, R., and O'Byrne, C. (2012). Development and optimization of an EGFP-based reporter for measuring the general stress response in Listeria monocytogenes. Bioeng. Bugs 3, 93-103. doi: 10.4161/bbug.19476.
74. van Helden, J., Toussaint, A., and Thieffry, D. (2012). Bacterial molecular networks: bridging the gap between functional genomics and dynamical modelling. Methods Mol. Biol. 804, 1-11. doi: 10.1007/978-1-61779-361-5_1.
75. Wemekamp-Kamphuis, H. H., Wouters, J. A., de Leeuw, P. P., Hain, T., Chakraborty, T., and Abee, T. (2004). Identification of sigma factor sigma B-controlled genes and their impact on acid stress, high hydrostatic pressure, and freeze survival in Listeria monocytogenes EGD-e. Appl. Environ. Microbiol. 70, 3457-3466. doi: 10.1128/AEM.70.6.3457-3466.2004.
76. Wichadakul, D., McDermott, J., and Samudrala, R. (2009). Prediction and integration of regulatory and protein-protein interactions. Methods Mol. Biol. 541, 101-143. doi: 10.1007/978-1-59745-243-4_6.
77. Williams, T., Bauer, S., Beier, D., and Kuhn, M. (2005). Construction and characterization of Listeria monocytogenes mutants with in-frame deletions in the response regulator genes identified in the genome sequence. Infect. Immun. 73, 3152-3159. doi: 10.1128/IAI.73.5.3152-3159.2005.
78. Wuchty, S., Oltvai, Z. N., and Barabasi, A. L. (2003). Evolutionary conservation of motif constituents in the yeast protein interaction network. Nat. Genet. 35, 176-179. doi: 10.1038/ng1242.
79. Xia, Y., Yu, H., Jansen, R., Seringhaus, M., Baxter, S., Greenbaum, D., et al. (2004). Analyzing cellular biochemistry in terms of molecular networks. Annu. Rev. Biochem. 73, 1051-1087. doi: 10.1146/annurev.biochem.73.011303.073950.
80. Yu, H., and Gerstein, M. (2006). Genomic analysis of the hierarchical structure of regulatory networks. Proc. Natl. Acad. Sci. U.S.A. 103, 14724-14731. doi: 10.1073/pnas.0508637103.
81. Yu, H., Luscombe, N. M., Qian, J., and Gerstein, M. (2003). Genomic analysis of gene expression relationships in transcriptional regulatory networks. Trends Genet. 19, 422-427. doi: 10.1016/S0168-9525(03)00175-6.
82. Zhang, C., Nietfeldt, J., Zhang, M., and Benson, A. K. (2005). Functional consequences of genome evolution in Listeria monocytogenes: the lmo0423 and lmo0422 genes encode sigmaC and LstR, a lineage II-specific heat shock system. J. Bacteriol. 187, 7243-7253. doi: 10.1128/JB.187.21.7243-7253.2005.