Advertisement

Protein–Protein Interaction in the -Omics Era: Understanding Mycobacterium tuberculosis Function

Chapter

Abstract

An important challenge for TB investigators in the postgenomic era is to integrate distinct functional strategies to study the molecular mechanism of Mycobacterium tuberculosis (Mtb) virulence. However, the biological function of the majority of Mtb genes is unknown. This has revealed the need for an approach to convert raw genome sequence data into functional information. In the past decade, the yeast two-hybrid system (Y2H) has contributed significantly towards studying TB virulence and persistence, but has several drawbacks. Recently, several mycobacterial protein–protein interaction (PPI) technologies have been reported that helped propose functions for unknown proteins through “guilt by association” and will be discussed in this chapter. We will examine the advantages, disadvantages and limitations of these systems and how these technologies can be used to dissect ­signaling, drug resistance, and virulence pathways. We will also discuss how ­mycobacterial PPI technologies can be exploited to force proteins to interact and for the discovery of small-molecule inhibitors against protein complexes. In sum, by characterizing Mtb PPIs on a genomic scale, it will be possible to assemble ­physiologically relevant protein pathways in mycobacteria, the outcome of which will be invaluable for determining virulence mechanisms and the function of previously uncharacterized proteins.

Keywords

Bait Protein Prey Protein Virulence Pathway Bubonic Plague Bacterial Adenylate Cyclase 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Abbreviations

BACTH

Bacterial adenylate cyclase two-hybrid

BM

BacterioMatch

hDHFR

Human dihydrofolate reductase

Mbov

Mycobacterium bovis

M-PFC

Mycobacterial protein fragment complementation

Msm

Mycobacterium smegmatis

Mtb

Mycobacterium tuberculosis

NO

Nitric oxide

PFC

Protein fragment complementation

PPI

Protein–protein interaction

RNAi

RNA interference

RNAP

RNA polymerase

TRX

Thioredoxin

Y2H

Yeast two-hybrid system

Y3H

Yeast three-hybrid system

References

  1. 1.
    Arno PS, Murray CJ, Bonuck KA, Alcabes P (1993) The economic impact of tuberculosis in hospitals in New York City: a preliminary analysis. J Law Med Ethics 21(3–4):317–323PubMedCrossRefGoogle Scholar
  2. 2.
    Murray CJ, Salomon JA (1998) Modeling the impact of global tuberculosis control strategies. Proc Natl Acad Sci USA 95(23):13881–13886PubMedCrossRefGoogle Scholar
  3. 3.
    Pelicic V, Jackson M, Reyrat JM, Jacobs WR Jr, Gicquel B, Guilhot C (1997) Efficient allelic exchange and transposon mutagenesis in Mycobacterium tuberculosis. Proc Natl Acad Sci USA 94(20):10955–10960PubMedCrossRefGoogle Scholar
  4. 4.
    Bardarov S, Kriakov J, Carriere C, Yu S, Vaamonde C, McAdam RA, Bloom BR, Hatfull GF, Jacobs WR Jr (1997) Conditionally replicating mycobacteriophages: a system for transposon delivery to Mycobacterium tuberculosis. Proc Natl Acad Sci USA 94(20):10961–10966PubMedCrossRefGoogle Scholar
  5. 5.
    Bardarov S, Bardarov S Jr, Pavelka MS Jr, Sambandamurthy V, Larsen M, Tufariello J, Chan J, Hatfull G, Jacobs WR Jr (2002) Specialized transduction: an efficient method for generating marked and unmarked targeted gene disruptions in Mycobacterium tuberculosis, M. bovis BCG and M. smegmatis. Microbiology 148(Pt 10):3007–3017PubMedGoogle Scholar
  6. 6.
    Cox JS, Chen B, McNeil M, Jacobs WR Jr (1999) Complex lipid determines tissue-specific replication of Mycobacterium tuberculosis in mice. Nature 402(6757):79–83PubMedCrossRefGoogle Scholar
  7. 7.
    Camacho LR, Ensergueix D, Perez E, Gicquel B, Guilhot C (1999) Identification of a virulence gene cluster of Mycobacterium tuberculosis by signature-tagged transposon mutagenesis. Mol Microbiol 34(2):257–267PubMedCrossRefGoogle Scholar
  8. 8.
    Dubnau E, Fontan P, Manganelli R, Soares-Appel S, Smith I (2002) Mycobacterium tuberculosis genes induced during infection of human macrophages. Infect Immun 70(6):2787–2795PubMedCrossRefGoogle Scholar
  9. 9.
    Dubnau E, Chan J, Mohan VP, Smith I (2005) Responses of Mycobacterium tuberculosis to growth in the mouse lung. Infect Immun 73(6):3754–3757PubMedCrossRefGoogle Scholar
  10. 10.
    Mollenkopf HJ, Grode L, Mattow J, Stein M, Mann P, Knapp B, Ulmer J, Kaufmann SH (2004) Application of mycobacterial proteomics to vaccine design: improved protection by Mycobacterium bovis BCG prime-Rv3407 DNA boost vaccination against tuberculosis. Infect Immun 72(11):6471–6479PubMedCrossRefGoogle Scholar
  11. 11.
    Mattow J, Schaible UE, Schmidt F, Hagens K, Siejak F, Brestrich G, Haeselbarth G, Muller EC, Jungblut PR, Kaufmann SH (2003) Comparative proteome analysis of culture supernatant proteins from virulent Mycobacterium tuberculosis H37Rv and attenuated M. bovis BCG Copenhagen. Electrophoresis 24(19–20):3405–3420PubMedCrossRefGoogle Scholar
  12. 12.
    Schnappinger D, Ehrt S, Voskuil MI, Liu Y, Mangan JA, Monahan IM, Dolganov G, Efron B, Butcher PD, Nathan C, Schoolnik GK (2003) Transcriptional adaptation of Mycobacterium tuberculosis within macrophages: insights into the phagosomal environment. J Exp Med 198(5):693–704PubMedCrossRefGoogle Scholar
  13. 13.
    Sherman DR, Voskuil M, Schnappinger D, Liao R, Harrell MI, Schoolnik GK (2001) Regulation of the Mycobacterium tuberculosis hypoxic response gene encoding alpha-crystallin. Proc Natl Acad Sci USA 98(13):7534–7539PubMedCrossRefGoogle Scholar
  14. 14.
    Voskuil MI, Schnappinger D, Visconti KC, Harrell MI, Dolganov GM, Sherman DR, Schoolnik GK (2003) Inhibition of respiration by nitric oxide induces a Mycobacterium tuberculosis dormancy program. J Exp Med 198(5):705–713PubMedCrossRefGoogle Scholar
  15. 15.
    Voskuil MI, Visconti KC, Schoolnik GK (2004) Mycobacterium tuberculosis gene expression during adaptation to stationary phase and low-oxygen dormancy. Tuberculosis (Edinb) 84(3–4):218–227CrossRefGoogle Scholar
  16. 16.
    Sassetti CM, Boyd DH, Rubin EJ (2003) Genes required for mycobacterial growth defined by high density mutagenesis. Mol Microbiol 48(1):77–84PubMedCrossRefGoogle Scholar
  17. 17.
    Ford CB, Lin PL, Chase MR, Shah RR, Iartchouk O, Galagan J, Mohaideen N, Ioerger TR, Sacchettini JC, Lipsitch M (2011) Use of whole genome sequencing to estimate the mutation rate of Mycobacterium tuberculosis during latent infection. Nat Genet 43(5):482–486PubMedCrossRefGoogle Scholar
  18. 18.
    Ioerger TR, Koo S, No EG, Chen X, Larsen MH, Jacobs WR Jr, Pillay M, Sturm AW, Sacchettini JC (2009) Genome analysis of multi-and extensively-drug-resistant tuberculosis from KwaZulu-Natal, South Africa. PLoS One 4(11):e7778PubMedCrossRefGoogle Scholar
  19. 19.
    Steyn AJ, Collins DM, Hondalus MK, Jacobs WR Jr, Kawakami RP, Bloom BR (2002) Mycobacterium tuberculosis WhiB3 interacts with RpoV to affect host survival but is dispensable for in vivo growth. Proc Natl Acad Sci USA 99(5):3147–3152PubMedCrossRefGoogle Scholar
  20. 20.
    Steyn AJ, Joseph J, Bloom BR (2003) Interaction of the sensor module of Mycobacterium tuberculosis H37Rv KdpD with members of the Lpr family. Mol Microbiol 47(4):1075–1089PubMedCrossRefGoogle Scholar
  21. 21.
    Pellegrini M, Marcotte EM, Thompson MJ, Eisenberg D, Yeates TO (1999) Assigning protein functions by comparative genome analysis: protein phylogenetic profiles. Proc Natl Acad Sci USA 96(8):4285–4288PubMedCrossRefGoogle Scholar
  22. 22.
    Marcotte EM, Pellegrini M, Thompson MJ, Yeates TO, Eisenberg D (1999) A combined algorithm for genome-wide prediction of protein function. Nature 402(6757):83–86PubMedCrossRefGoogle Scholar
  23. 23.
    Overbeek R, Fonstein M, D’Souza M, Pusch GD, Maltsev N (1999) The use of gene clusters to infer functional coupling. Proc Natl Acad Sci USA 96(6):2896–2901PubMedCrossRefGoogle Scholar
  24. 24.
    Dandekar T, Snel B, Huynen M, Bork P (1998) Conservation of gene order: a fingerprint of proteins that physically interact. Trends Biochem Sci 23(9):324–328PubMedCrossRefGoogle Scholar
  25. 25.
    De Las RJ, De Luis A (2004) Interactome data and databases: different types of protein interaction. Comp Funct Genomics 5(2):173–178CrossRefGoogle Scholar
  26. 26.
    Bartel PL, Roecklein JA, SenGupta D, Fields S (1996) A protein linkage map of Escherichia coli bacteriophage T7. Nat Genet 12(1):72–77PubMedCrossRefGoogle Scholar
  27. 27.
    Ito T, Chiba T, Ozawa R, Yoshida M, Hattori M, Sakaki Y (2001) A comprehensive two-hybrid analysis to explore the yeast protein interactome. Proc Natl Acad Sci USA 98(8):4569–4574PubMedCrossRefGoogle Scholar
  28. 28.
    Uetz P, Giot L, Cagney G, Mansfield TA, Judson RS, Knight JR, Lockshon D, Narayan V, Srinivasan M, Pochart P, Qureshi-Emili A, Li Y, Godwin B, Conover D, Kalbfleisch T, Vijayadamodar G, Yang M, Johnston M, Fields S, Rothberg JM (2000) A comprehensive analysis of protein-protein interactions in Saccharomyces cerevisiae. Nature 403(6770):623–627PubMedCrossRefGoogle Scholar
  29. 29.
    Schwikowski B, Uetz P, Fields S (2000) A network of protein-protein interactions in yeast. Nat Biotechnol 18(12):1257–1261PubMedCrossRefGoogle Scholar
  30. 30.
    Ito T, Tashiro K, Muta S, Ozawa R, Chiba T, Nishizawa M, Yamamoto K, Kuhara S, Sakaki Y (2000) Toward a protein-protein interaction map of the budding yeast: a comprehensive system to examine two-hybrid interactions in all possible combinations between the yeast proteins. Proc Natl Acad Sci USA 97(3):1143–1147PubMedCrossRefGoogle Scholar
  31. 31.
    Formstecher E, Aresta S, Collura V, Hamburger A, Meil A, Trehin A, Reverdy C, Betin V, Maire S, Brun C, Jacq B, Arpin M, Bellaiche Y, Bellusci S, Benaroch P, Bornens M, Chanet R, Chavrier P, Delattre O, Doye V, Fehon R, Faye G, Galli T, Girault JA, Goud B, de Gunzburg J, Johannes L, Junier MP, Mirouse V, Mukherjee A, Papadopoulo D, Perez F, Plessis A, Rosse C, Saule S, Stoppa-Lyonnet D, Vincent A, White M, Legrain P, Wojcik J, Camonis J, Daviet L (2005) Protein interaction mapping: a Drosophila case study. Genome Res 15(3):376–384PubMedCrossRefGoogle Scholar
  32. 32.
    Giot L, Bader JS, Brouwer C, Chaudhuri A, Kuang B, Li Y, Hao YL, Ooi CE, Godwin B, Vitols E, Vijayadamodar G, Pochart P, Machineni H, Welsh M, Kong Y, Zerhusen B, Malcolm R, Varrone Z, Collis A, Minto M, Burgess S, McDaniel L, Stimpson E, Spriggs F, Williams J, Neurath K, Ioime N, Agee M, Voss E, Furtak K, Renzulli R, Aanensen N, Carrolla S, Bickelhaupt E, Lazovatsky Y, DaSilva A, Zhong J, Stanyon CA, Finley RL Jr, White KP, Braverman M, Jarvie T, Gold S, Leach M, Knight J, Shimkets RA, McKenna MP, Chant J, Rothberg JM (2003) A protein interaction map of Drosophila melanogaster. Science 302(5651):1727–1736PubMedCrossRefGoogle Scholar
  33. 33.
    de Folter S, Immink RG, Kieffer M, Parenicova L, Henz SR, Weigel D, Busscher M, Kooiker M, Colombo L, Kater MM, Davies B, Angenent GC (2005) Comprehensive interaction map of the Arabidopsis MADS box transcription factors. Plant Cell 17(5):1424–1433PubMedCrossRefGoogle Scholar
  34. 34.
    Li S, Armstrong CM, Bertin N, Ge H, Milstein S, Boxem M, Vidalain PO, Han JD, Chesneau A, Hao T, Goldberg DS, Li N, Martinez M, Rual JF, Lamesch P, Xu L, Tewari M, Wong SL, Zhang LV, Berriz GF, Jacotot L, Vaglio P, Reboul J, Hirozane-Kishikawa T, Li Q, Gabel HW, Elewa A, Baumgartner B, Rose DJ, Yu H, Bosak S, Sequerra R, Fraser A, Mango SE, Saxton WM, Strome S, Van Den Heuvel S, Piano F, Vandenhaute J, Sardet C, Gerstein M, Doucette-Stamm L, Gunsalus KC, Harper JW, Cusick ME, Roth FP, Hill DE, Vidal M (2004) A map of the interactome network of the metazoan C. elegans. Science 303(5657):540–543PubMedCrossRefGoogle Scholar
  35. 35.
    Fields S, Song O (1989) A novel genetic system to detect protein protein interactions. Nature 340(6230):245–246PubMedCrossRefGoogle Scholar
  36. 36.
    Vidal M, Brachmann RK, Fattaey A, Harlow E, Boeke JD (1996) Reverse two-hybrid and one-hybrid systems to detect dissociation of protein-protein and DNA-protein interactions. Proc Natl Acad Sci 93(19):10315PubMedCrossRefGoogle Scholar
  37. 37.
    SenGupta DJ, Zhang B, Kraemer B, Pochart P, Fields S, Wickens M (1996) A three-hybrid system to detect RNA-protein interactions in vivo. Proc Natl Acad Sci 93(16):8496PubMedCrossRefGoogle Scholar
  38. 38.
    Dove SL, Joung JK, Hochschild A (1997) Activation of prokaryotic transcription through arbitrary protein-protein contacts. Nature 386(6625):627–630PubMedCrossRefGoogle Scholar
  39. 39.
    Dove SL, Hochschild A (2004) A bacterial two-hybrid system based on transcription activation. Methods Mol Biol 261:231–246PubMedGoogle Scholar
  40. 40.
    Tharad M, Samuchiwal SK, Bhalla K, Ghosh A, Kumar K, Kumar S, Ranganathan A (2011) A three-hybrid system to probe in vivo protein-protein interactions: application to the essential proteins of the RD1 complex of M. tuberculosis. PLoS One 6(11):e27503PubMedCrossRefGoogle Scholar
  41. 41.
    Wang Y, Cui T, Zhang C, Yang M, Huang Y, Li W, Zhang L, Gao C, He Y, Li Y (2010) A global protein-protein interaction network in the human pathogen Mycobacterium tuberculosis H37Rv. J Proteome Res 9(12):6665–6677PubMedCrossRefGoogle Scholar
  42. 42.
    Karimova G, Dautin N, Ladant D (2005) Interaction network among Escherichia coli membrane proteins involved in cell division as revealed by bacterial two-hybrid analysis. J Bacteriol 187(7):2233–2243PubMedCrossRefGoogle Scholar
  43. 43.
    Baulard AR, Gurcha SS, Engohang-Ndong J, Gouffi K, Locht C, Besra GS (2003) In vivo interaction between the polyprenol phosphate mannose synthase Ppm1 and the integral membrane protein Ppm2 from Mycobacterium smegmatis revealed by a bacterial two-hybrid system. J Biol Chem 278(4):2242PubMedCrossRefGoogle Scholar
  44. 44.
    Dziedzic R, Kiran M, Plocinski P, Ziolkiewicz M, Brzostek A, Moomey M, Vadrevu IS, Dziadek J, Madiraju M, Rajagopalan M (2010) Mycobacterium tuberculosis ClpX interacts with FtsZ and interferes with FtsZ assembly. PLoS One 5(7):e11058PubMedCrossRefGoogle Scholar
  45. 45.
    Galarneau A, Primeau M, Trudeau LE, Michnick SW (2002) Beta-lactamase protein fragment complementation assays as in vivo and in vitro sensors of protein protein interactions. Nat Biotechnol 20(6):619–622PubMedCrossRefGoogle Scholar
  46. 46.
    Nyfeler B, Michnick SW, Hauri HP (2005) Capturing protein interactions in the secretory pathway of living cells. Proc Natl Acad Sci USA 102(18):6350–6355PubMedCrossRefGoogle Scholar
  47. 47.
    Remy I, Michnick SW (2001) Visualization of biochemical networks in living cells. Proc Natl Acad Sci USA 98(14):7678–7683PubMedCrossRefGoogle Scholar
  48. 48.
    Subramaniam R, Desveaux D, Spickler C, Michnick SW, Brisson N (2001) Direct visualization of protein interactions in plant cells. Nat Biotechnol 19(8):769–772PubMedCrossRefGoogle Scholar
  49. 49.
    Gegg CV, Bowers KE, Matthews CR (1997) Probing minimal independent folding units in dihydrofolate reductase by molecular dissection. Protein Sci 6(9):1885–1892PubMedCrossRefGoogle Scholar
  50. 50.
    Remy I, Michnick SW (1999) Clonal selection and in vivo quantitation of protein interactions with protein-fragment complementation assays. Proc Natl Acad Sci USA 96(10):5394–5399PubMedCrossRefGoogle Scholar
  51. 51.
    Remy I, Galarneau A, Michnick SW (2002) Detection and visualization of protein interactions with protein fragment complementation assays. Methods Mol Biol 185:447–459PubMedGoogle Scholar
  52. 52.
    Singh A, Mai D, Kumar A, Steyn AJ (2006) Dissecting virulence pathways of Mycobacterium tuberculosis through protein-protein association. Proc Natl Acad Sci USA 103(30):11346–11351PubMedCrossRefGoogle Scholar
  53. 53.
    Pearce MJ, Mintseris J, Ferreyra J, Gygi SP, Darwin KH (2008) Ubiquitin-like protein involved in the proteasome pathway of Mycobacterium tuberculosis. Science 322(5904):1104PubMedCrossRefGoogle Scholar
  54. 54.
    Mai D, Jones J, Rodgers JW, Hartman JL, Kutsch O, Steyn AJC (2011) A screen to identify small molecule inhibitors of protein-protein interactions in Mycobacteria. Assay Drug Dev Technol 9(3):299–310PubMedCrossRefGoogle Scholar
  55. 55.
    Tafelmeyer P, Johnsson N, Johnsson K (2004) Transforming a ([beta]/[alpha]) 8-barrel enzyme into a split-protein sensor through directed evolution. Chem Biol 11(5):681–689PubMedGoogle Scholar
  56. 56.
    O’Hare H, Juillerat A, Dianiskova P, Johnsson K (2008) A split-protein sensor for studying protein-protein interaction in mycobacteria. J Microbiol Methods 73(2):79–84PubMedCrossRefGoogle Scholar
  57. 57.
    Rual JF, Venkatesan K, Hao T, Hirozane-Kishikawa T, Dricot A, Li N, Berriz GF, Gibbons FD, Dreze M, Ayivi-Guedehoussou N, Klitgord N, Simon C, Boxem M, Milstein S, Rosenberg J, Goldberg DS, Zhang LV, Wong SL, Franklin G, Li S, Albala JS, Lim J, Fraughton C, Llamosas E, Cevik S, Bex C, Lamesch P, Sikorski RS, Vandenhaute J, Zoghbi HY, Smolyar A, Bosak S, Sequerra R, Doucette-Stamm L, Cusick ME, Hill DE, Roth FP, Vidal M (2005) Towards a proteome-scale map of the human protein-protein interaction network. Nature 437(7062):1173–1178PubMedCrossRefGoogle Scholar
  58. 58.
    Collins DM, Kawakami RP, de Lisle GW, Pascopella L, Bloom BR, Jacobs WR Jr (1995) Mutation of the principal sigma factor causes loss of virulence in a strain of the Mycobacterium tuberculosis complex. Proc Natl Acad Sci USA 92(17):8036–8040PubMedCrossRefGoogle Scholar
  59. 59.
    Singh A, Guidry L, Narasimhulu KV, Mai D, Trombley J, Redding KE, Giles GI, Lancaster JR, Steyn AJC (2007) Mycobacterium tuberculosis WhiB3 responds to O2 and nitric oxide via its [4Fe-4S] cluster and is essential for nutrient starvation survival. Proc Natl Acad Sci 104(28):11562PubMedCrossRefGoogle Scholar
  60. 60.
    Singh A, Crossman DK, Mai D, Guidry L, Voskuil MI, Renfrow MB, Steyn AJC (2009) Mycobacterium tuberculosis WhiB3 maintains redox homeostasis by regulating virulence lipid anabolism to modulate macrophage response. PLoS Pathog 5(8):e1000545PubMedCrossRefGoogle Scholar
  61. 61.
    Farhana A, Guidry L, Srivastava A, Singh A, Hondalus MK, Steyn AJC (2010) Reductive stress in microbes: implications for understanding Mycobacterium tuberculosis disease and persistence. Adv Microb Physiol 57:43–117PubMedCrossRefGoogle Scholar
  62. 62.
    Saini V, Farhana A, Steyn AJ (2012) Mycobacterium tuberculosis WhiB3: a novel iron-sulfur cluster protein that regulates redox homeostasis and virulence. Antioxid Redox Signal 16(7):687–697PubMedCrossRefGoogle Scholar
  63. 63.
    Abdallah AM, van Pittius NCG, Champion PADG, Cox J, Luirink J, Vandenbroucke-Grauls CMJE, Appelmelk BJ, Bitter W (2007) Type VII secretion: mycobacteria show the way. Nat Rev Microbiol 5(11):883–891PubMedCrossRefGoogle Scholar
  64. 64.
    Teutschbein J, Schumann G, Möllmann U, Grabley S, Cole ST, Munder T (2009) A protein linkage map of the ESAT-6 secretion system 1 (ESX-1) of Mycobacterium tuberculosis. Microbiol Res 164(3):253–259PubMedCrossRefGoogle Scholar
  65. 65.
    Champion PADG, Stanley SA, Champion MM, Brown EJ, Cox JS (2006) C-terminal signal sequence promotes virulence factor secretion in Mycobacterium tuberculosis. Science 313(5793):1632PubMedCrossRefGoogle Scholar
  66. 66.
    DiGiuseppe Champion PA, Champion MM, Manzanillo P, Cox JS (2009) ESX-1 secreted virulence factors are recognized by multiple cytosolic AAA ATPases in pathogenic mycobacteria. Mol Microbiol 73(5):950–962PubMedCrossRefGoogle Scholar
  67. 67.
    Lightbody KL, Renshaw PS, Collins ML, Wright RL, Hunt DM, Gordon SV, Hewinson RG, Buxton RS, Williamson RA, Carr MD (2004) Characterisation of complex formation between members of the Mycobacterium tuberculosis complex CFP-10/ESAT-6 protein family: towards an understanding of the rules governing complex formation and thereby functional flexibility. FEMS Microbiol Lett 238(1):255–262PubMedGoogle Scholar
  68. 68.
    MacGurn JA, Raghavan S, Stanley SA, Cox JS (2005) A non-RD1 gene cluster is required for Snm secretion in Mycobacterium tuberculosis. Mol Microbiol 57(6):1653–1663PubMedCrossRefGoogle Scholar
  69. 69.
    Shrivastava R, Ghosh AK, Das AK (2009) Intra-and intermolecular domain interactions among novel two-component system proteins coded by Rv0600c, Rv0601c and Rv0602c of Mycobacterium tuberculosis. Microbiology 155(3):772PubMedCrossRefGoogle Scholar
  70. 70.
    Parida BK, Douglas T, Nino C, Dhandayuthapani S (2005) Interactions of anti-sigma factor antagonists of Mycobacterium tuberculosis in the yeast two-hybrid system. Tuberculosis 85(5):347–355PubMedCrossRefGoogle Scholar
  71. 71.
    Saïd-Salim B, Mostowy S, Kristof AS, Behr MA (2006) Mutations in Mycobacterium tuberculosis Rv0444c, the gene encoding anti-SigK, explain high level expression of MPB70 and MPB83 in Mycobacterium bovis. Mol Microbiol 62(5):1251–1263PubMedCrossRefGoogle Scholar
  72. 72.
    Handa P, Acharya N, Thanedar S, Purnapatre K, Varshney U (2000) Distinct properties of Mycobacterium tuberculosis single-stranded DNA binding protein and its functional characterization in Escherichia coli. Nucleic Acids Res 28(19):3823PubMedCrossRefGoogle Scholar
  73. 73.
    Kana BD, Abrahams GL, Sung N, Warner DF, Gordhan BG, Machowski EE, Tsenova L, Sacchettini JC, Stoker NG, Kaplan G (2010) Role of the DinB homologs Rv1537 and Rv3056 in Mycobacterium tuberculosis. J Bacteriol 192(8):2220PubMedCrossRefGoogle Scholar
  74. 74.
    Sinha KM, Stephanou NC, Gao F, Glickman MS, Shuman S (2007) Mycobacterial UvrD1 is a Ku-dependent DNA helicase that plays a role in multiple DNA repair events, including double-strand break repair. J Biol Chem 282(20):15114PubMedCrossRefGoogle Scholar
  75. 75.
    Warner DF, Ndwandwe DE, Abrahams GL, Kana BD, Machowski EE, Venclovas Ä, Mizrahi V (2010) Essential roles for imuA′- and imuB-encoded accessory factors in DnaE2-dependent mutagenesis in Mycobacterium tuberculosis. Proc Natl Acad Sci 107(29):13093–13098PubMedCrossRefGoogle Scholar
  76. 76.
    Garg S, Alam MS, Bajpai R, Kishan KVR, Agrawal P (2009) Redox biology of Mycobacterium tuberculosis H37Rv: protein-protein interaction between GlgB and WhiB1 involves exchange of thiol-disulfide. BMC Biochem 10(1):1PubMedCrossRefGoogle Scholar
  77. 77.
    Huet G, Castaing JP, Fournier D, Daffé M, Saves I (2006) Protein splicing of SufB is crucial for the functionality of the Mycobacterium tuberculosis SUF machinery. J Bacteriol 188(9):3412–3414PubMedCrossRefGoogle Scholar
  78. 78.
    Huet G, Daffa M, Saves I (2005) Identification of the Mycobacterium tuberculosis SUF machinery as the exclusive mycobacterial system of [Fe-S] cluster assembly: evidence for its implication in the pathogen’s survival. J Bacteriol 187(17):6137PubMedCrossRefGoogle Scholar
  79. 79.
    Veyron-Churlet R, Guerrini O, Mourey L, Daffa M, Zerbib D (2004) Protein-protein interactions within the Fatty Acid Synthase-II system of Mycobacterium tuberculosis are essential for mycobacterial viability. Mol Microbiol 54(5):1161–1172PubMedCrossRefGoogle Scholar
  80. 80.
    Veyron-Churlet R, Bigot S, Guerrini O, Verdoux S, Malaga W, Daffe M, Zerbib D (2005) The biosynthesis of mycolic acids in Mycobacterium tuberculosis relies on multiple specialized elongation complexes interconnected by specific protein-protein interactions. J Mol Biol 353(4):847–858PubMedCrossRefGoogle Scholar
  81. 81.
    Curry JM, Whalan R, Hunt DM, Gohil K, Strom M, Rickman L, Colston MJ, Smerdon SJ, Buxton RS (2005) An ABC transporter containing a forkhead-associated domain interacts with a serine-threonine protein kinase and is required for growth of Mycobacterium tuberculosis in mice. Infect Immun 73(8):4471–4477PubMedCrossRefGoogle Scholar
  82. 82.
    Hett EC, Chao MC, Steyn AJ, Fortune SM, Deng LL, Rubin EJ (2007) A partner for the resuscitation-promoting factors of Mycobacterium tuberculosis. Mol Microbiol 66(3):658–668PubMedCrossRefGoogle Scholar
  83. 83.
    Sasindran S, Saikolappan S, Scofield V, Dhandayuthapani S (2011) Biochemical and physiological characterization of the GTP-binding protein Obg of Mycobacterium tuberculosis. BMC Microbiol 11(1):43PubMedCrossRefGoogle Scholar
  84. 84.
    Ahidjo BA, Kuhnert D, McKenzie JL, Machowski EE, Gordhan BG, Arcus V, Abrahams GL, Mizrahi V (2011) VapC toxins from Mycobacterium tuberculosis are ribonucleases that differentially inhibit growth and are neutralized by cognate VapB antitoxins. PLoS One 6(6):e21738PubMedCrossRefGoogle Scholar
  85. 85.
    Rain JC, Selig L, De Reuse H, Battaglia V, Reverdy C, Simon S, Lenzen G, Petel F, Wojcik J, Schachter V, Chemama Y, Labigne A, Legrain P (2001) The protein-protein interaction map of Helicobacter pylori. Nature 409(6817):211–215PubMedCrossRefGoogle Scholar
  86. 86.
    LaCount DJ, Vignali M, Chettier R, Phansalkar A, Bell R, Hesselberth JR, Schoenfeld LW, Ota I, Sahasrabudhe S, Kurschner C (2005) A protein interaction network of the malaria parasite Plasmodium falciparum. Nature 438(7064):103–107PubMedCrossRefGoogle Scholar
  87. 87.
    Malek JA, Wierzbowski JM, Tao W, Bosak SA, Saranga DJ, Doucette-Stamm L, Smith DR, McEwan PJ, McKernan KJ (2004) Protein interaction mapping on a functional shotgun sequence of Rickettsia sibirica. Nucleic Acids Res 32(3):1059–1064PubMedCrossRefGoogle Scholar
  88. 88.
    Dyer MD, Neff C, Dufford M, Rivera CG, Shattuck D, Bassaganya-Riera J, Murali TM, Sobral BW (2010) The human-bacterial pathogen protein interaction networks of Bacillus anthracis, Francisella tularensis, and Yersinia pestis. PLoS One 5(8):e12089PubMedCrossRefGoogle Scholar
  89. 89.
    Parrish JR, Yu J, Liu G, Hines JA, Chan JE, Mangiola BA, Zhang H, Pacifico S, Fotouhi F, DiRita VJ (2007) A proteome-wide protein interaction map for Campylobacter jejuni. Genome Biol 8(7):R130PubMedCrossRefGoogle Scholar
  90. 90.
    Titz B, Rajagopala SV, Goll J, Häuser R, McKevitt MT, Palzkill T, Uetz P (2008) The binary protein interactome of Treponema pallidum: the syphilis spirochete. PLoS One 3(5):e2292PubMedCrossRefGoogle Scholar
  91. 91.
    Zhang L, Villa NY, Rahman MM, Smallwood S, Shattuck D, Neff C, Dufford M, Lanchbury JS, LaBaer J, McFadden G (2009) Analysis of vaccinia virus-host protein-protein interactions: validations of yeast two-hybrid screenings. J Proteome Res 8(9):4311–4318PubMedCrossRefGoogle Scholar
  92. 92.
    Gavin AC, Basche M, Krause R, Grandi P, Marzioch M, Bauer A, Schultz J, Rick JM, Michon AM, Cruciat CM (2002) Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature 415(6868):141–147PubMedCrossRefGoogle Scholar
  93. 93.
    Gerber D, Maerkl SJ, Quake SR (2008) An in vitro microfluidic approach to generating protein-interaction networks. Nat Methods 6(1):71–74PubMedCrossRefGoogle Scholar
  94. 94.
    Ho Y, Gruhler A, Heilbut A, Bader GD, Moore L, Adams SL, Millar A, Taylor P, Bennett K, Boutilier K (2002) Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectrometry. Nature 415(6868):180–183PubMedCrossRefGoogle Scholar
  95. 95.
    Xiang G, Yao X, Guowu B, Yan X, Zhiyong X (2010) Response of the mosquito protein interaction network to dengue infection. BMC Genomics 11:380CrossRefGoogle Scholar
  96. 96.
    Marchadier E, Carballidoa-Lapez R, Brinster S, Fabret C, Mervelet P, Bessiares P, Noirota-Gros MF, Fromion V, Noirot P (2011) An expanded protein-protein interaction network in Bacillus subtilis reveals a group of hubs: exploration by an integrative approach. Proteomics 11(15):2981–2991PubMedCrossRefGoogle Scholar
  97. 97.
    Cherkasov A, Hsing M, Zoraghi R, Foster LJ, See RH, Stoynov N, Jiang J, Kaur S, Lian T, Jackson L (2011) Mapping the protein interaction network in methicillin-resistant Staphylococcus aureus. J Proteome Res 10(3):1139–1150PubMedCrossRefGoogle Scholar
  98. 98.
    Callahan B, Nguyen K, Collins A, Valdes K, Caplow M, Crossman DK, Steyn AJC, Eisele L, Derbyshire KM (2010) Conservation of structure and protein-protein interactions mediated by the secreted mycobacterial proteins EsxA, EsxB, and EspA. J Bacteriol 192(1):326PubMedCrossRefGoogle Scholar
  99. 99.
    Matsumoto A, Comatas KE, Liu L, Stamler JS (2003) Screening for nitric oxide-dependent protein-protein interactions. Science 301(5633):657PubMedCrossRefGoogle Scholar
  100. 100.
    Vignols F, Brahalin C, Surdin-Kerjan Y, Thomas D, Meyer Y (2005) A yeast two-hybrid knockout strain to explore thioredoxin-interacting proteins in vivo. Proc Natl Acad Sci USA 102(46):16729PubMedCrossRefGoogle Scholar
  101. 101.
    Andries K, Verhasselt P, Guillemont J, Gohlmann HW, Neefs JM, Winkler H, Van Gestel J, Timmerman P, Zhu M, Lee E, Williams P, de Chaffoy D, Huitric E, Hoffner S, Cambau E, Truffot-Pernot C, Lounis N, Jarlier V (2005) A diarylquinoline drug active on the ATP synthase of Mycobacterium tuberculosis. Science 307(5707):223–227PubMedCrossRefGoogle Scholar
  102. 102.
    Manjunatha UH, Boshoff H, Dowd CS, Zhang L, Albert TJ, Norton JE, Daniels L, Dick T, Pang SS, Barry CE 3rd (2006) Identification of a nitroimidazo-oxazine-specific protein involved in PA-824 resistance in Mycobacterium tuberculosis. Proc Natl Acad Sci USA 103(2):431–436PubMedCrossRefGoogle Scholar
  103. 103.
    Stover CK, Warrener P, VanDevanter DR, Sherman DR, Arain TM, Langhorne MH, Anderson SW, Towell JA, Yuan Y, McMurray DN, Kreiswirth BN, Barry CE, Baker WR (2000) A small-molecule nitroimidazopyran drug candidate for the treatment of tuberculosis. Nature 405(6789):962–966PubMedCrossRefGoogle Scholar
  104. 104.
    Bogan AA, Thorn KS (1998) Anatomy of hot spots in protein interfaces. J Mol Biol 280(1):1–9PubMedCrossRefGoogle Scholar
  105. 105.
    Clackson T, Wells JA (1995) A hot spot of binding energy in a hormone-receptor interface. Science 267(5196):383PubMedCrossRefGoogle Scholar
  106. 106.
    Tsai CJ, Lin SL, Wolfson HJ, Nussinov R (1997) Studies of protein-protein interfaces: a statistical analysis of the hydrophobic effect. Protein Sci 6(1):53–64PubMedCrossRefGoogle Scholar
  107. 107.
    Xu D, Tsai CJ, Nussinov R (1997) Hydrogen bonds and salt bridges across protein-protein interfaces. Protein Eng 10(9):999–1012PubMedCrossRefGoogle Scholar
  108. 108.
    McCoy AJ, Chandana Epa V, Colman PM (1997) Electrostatic complementarity at protein/protein interfaces. J Mol Biol 268(2):570–584PubMedCrossRefGoogle Scholar
  109. 109.
    Jones S, Thornton JM (1996) Principles of protein-protein interactions. Proc Natl Acad Sci USA 93(1):13–20PubMedCrossRefGoogle Scholar
  110. 110.
    Gadek TR, Nicholas JB (2003) Small molecule antagonists of proteins. Biochem Pharmacol 65(1):1–8PubMedCrossRefGoogle Scholar
  111. 111.
    Laskowski RA, Luscombe NM, Swindells MB, Thornton JM (1996) Protein clefts in ­molecular recognition and function. Protein Sci 5(12):2438–2452PubMedGoogle Scholar
  112. 112.
    Loregian A, Palu G (2005) Disruption of protein-protein interactions: towards new targets for chemotherapy. J Cell Physiol 204(3):750–762PubMedCrossRefGoogle Scholar
  113. 113.
    Wells JA, McClendon CL (2007) Reaching for high-hanging fruit in drug discovery at protein-protein interfaces. Nature 450(7172):1001–1009PubMedCrossRefGoogle Scholar
  114. 114.
    Arkin MR, Wells JA (2004) Small-molecule inhibitors of protein-protein interactions: progressing towards the dream. Nat Rev Drug Discov 3(4):301–317PubMedCrossRefGoogle Scholar
  115. 115.
    Strosberg AD (2007) Protein-protein interactions as targets for novel therapeutics. Drug DiscovGoogle Scholar
  116. 116.
    Vassilev LT, Vu BT, Graves B, Carvajal D, Podlaski F, Filipovic Z, Kong N, Kammlott U, Lukacs C, Klein C, Fotouhi N, Liu EA (2004) In vivo activation of the p53 pathway by small-molecule antagonists of MDM2. Science 303(5659):844–848PubMedCrossRefGoogle Scholar
  117. 117.
    Kussie PH, Gorina S, Marechal V, Elenbaas B, Moreau J, Levine AJ, Pavletich NP (1996) Structure of the MDM2 oncoprotein bound to the p53 tumor suppressor transactivation domain. Science 274(5289):948–953PubMedCrossRefGoogle Scholar
  118. 118.
    Hung DT, Shakhnovich EA, Pierson E, Mekalanos JJ (2005) Small-molecule inhibitor of Vibrio cholerae virulence and intestinal colonization. Science 310(5748):670–674PubMedCrossRefGoogle Scholar
  119. 119.
    Shakhnovich EA, Hung DT, Pierson E, Lee K, Mekalanos JJ (2007) Virstatin inhibits dimerization of the transcriptional activator ToxT. Proc Natl Acad Sci USA 104(7):2372–2377PubMedCrossRefGoogle Scholar
  120. 120.
    McMillan K, Adler M, Auld DS, Baldwin JJ, Blasko E, Browne LJ, Chelsky D, Davey D, Dolle RE, Eagen KA, Erickson S, Feldman RI, Glaser CB, Mallari C, Morrissey MM, Ohlmeyer MH, Pan G, Parkinson JF, Phillips GB, Polokoff MA, Sigal NH, Vergona R, Whitlow M, Young TA, Devlin JJ (2000) Allosteric inhibitors of inducible nitric oxide synthase dimerization discovered via combinatorial chemistry. Proc Natl Acad Sci USA 97(4):1506–1511PubMedCrossRefGoogle Scholar
  121. 121.
    Sennequier N, Wolan D, Stuehr DJ (1999) Antifungal imidazoles block assembly of inducible NO synthase into an active dimer. J Biol Chem 274(2):930–938PubMedCrossRefGoogle Scholar
  122. 122.
    Gorczynski MJ, Grembecka J, Zhou Y, Kong Y, Roudaia L, Douvas MG, Newman M, Bielnicka I, Baber G, Corpora T, Shi J, Sridharan M, Lilien R, Donald BR, Speck NA, Brown ML, Bushweller JH (2007) Allosteric inhibition of the protein-protein interaction between the leukemia-associated proteins Runx1 and CBFbeta. Chem Biol 14(10):1186–1197PubMedCrossRefGoogle Scholar
  123. 123.
    Last-Barney K, Davidson W, Cardozo M, Frye LL, Grygon CA, Hopkins JL, Jeanfavre DD, Pav S, Qian C, Stevenson JM, Tong L, Zindell R, Kelly TA (2001) Binding site elucidation of hydantoin-based antagonists of LFA-1 using multidisciplinary technologies: evidence for the allosteric inhibition of a protein-protein interaction. J Am Chem Soc 123(24):5643–5650PubMedCrossRefGoogle Scholar
  124. 124.
    Horn JR, Shoichet BK (2004) Allosteric inhibition through core disruption. J Mol Biol 336(5):1283–1291PubMedCrossRefGoogle Scholar
  125. 125.
    He MM, Smith AS, Oslob JD, Flanagan WM, Braisted AC, Whitty A, Cancilla MT, Wang J, Lugovskoy AA, Yoburn JC, Fung AD, Farrington G, Eldredge JK, Day ES, Cruz LA, Cachero TG, Miller SK, Friedman JE, Choong IC, Cunningham BC (2005) Small-molecule inhibition of TNF-alpha. Science 310(5750):1022–1025. doi: 10.1126/science.1116304 PubMedCrossRefGoogle Scholar
  126. 126.
    Bochkareva E, Safro M, Girshovich A (1999) Interaction of 4,4′-dithiodipyridine with Cys(458) triggers disassembly of GroEL. J Biol Chem 274(30):20756–20758PubMedCrossRefGoogle Scholar
  127. 127.
    Tachedjian G, Orlova M, Sarafianos SG, Arnold E, Goff SP (2001) Nonnucleoside reverse transcriptase inhibitors are chemical enhancers of dimerization of the HIV type 1 reverse transcriptase. Proc Natl Acad Sci USA 98(13):7188–7193PubMedCrossRefGoogle Scholar
  128. 128.
    Crabtree GR, Schreiber SL (1996) Three-part inventions: intracellular signaling and induced proximity. Trends Biochem Sci 21(11):418–422PubMedCrossRefGoogle Scholar
  129. 129.
    Michnick SW (2000) Chemical biology beyond binary codes. Chem Biol 7(12):R217–221, pii: S1074-5521(00)00040-5PubMedCrossRefGoogle Scholar
  130. 130.
    Liu J, Farmer JD Jr, Lane WS, Friedman J, Weissman I, Schreiber SL (1991) Calcineurin is a common target of cyclophilin-cyclosporin A and FKBP-FK506 complexes. Cell 66(4):807–815, pii: 0092-8674(91)90124-HPubMedCrossRefGoogle Scholar
  131. 131.
    Brown EJ, Albers MW, Shin TB, Ichikawa K, Keith CT, Lane WS, Schreiber SL (1994) A mammalian protein targeted by G1-arresting rapamycin-receptor complex. Nature 369(6483):756–758. doi: 10.1038/369756a0 PubMedCrossRefGoogle Scholar
  132. 132.
    Williams DJ, Puhl HL, Ikeda SR, Brezina V (2009) Rapid modification of proteins using a rapamycin-inducible tobacco etch virus protease system. PLoS One 4(10):e7474PubMedCrossRefGoogle Scholar
  133. 133.
    Remy I, Michnick SW (2006) A highly sensitive protein-protein interaction assay based on Gaussia luciferase. Nat Methods 3(12):977–979PubMedCrossRefGoogle Scholar
  134. 134.
    Janse DM, Crosas B, Finley D, Church GM (2004) Localization to the proteasome is sufficient for degradation. J Biol Chem 279(20):21415–21420PubMedCrossRefGoogle Scholar
  135. 135.
    Joshi PB, Hirst M, Malcolm T, Parent J, Mitchell D, Lund K, Sadowski I (2007) Identification of protein interaction antagonists using the repressed transactivator two-hybrid system. Biotechniques 42(5):635–644PubMedCrossRefGoogle Scholar
  136. 136.
    Kley N (2004) Chemical dimerizers and three-hybrid systems: scanning the proteome for targets of organic small molecules. Chem Biol 11(5):599–608PubMedCrossRefGoogle Scholar
  137. 137.
    Veselovsky AV, Ivanov YD, Ivanov AS, Archakov AI, Lewi P, Janssen P (2002) Protein-protein interactions: mechanisms and modification by drugs. J Mol Recognit 15(6):405–422PubMedCrossRefGoogle Scholar
  138. 138.
    Valencia A, Pazos F (2002) Computational methods for the prediction of protein interactions. Curr Opin Struct Biol 12(3):368–373PubMedCrossRefGoogle Scholar
  139. 139.
    Marcotte EM, Pellegrini M, Ng HL, Rice DW, Yeates TO, Eisenberg D (1999) Detecting protein function and protein-protein interactions from genome sequences. Science 285(5428):751PubMedCrossRefGoogle Scholar
  140. 140.
    Bock JR, Gough DA (2001) Predicting protein-protein interactions from primary structure. Bioinformatics 17(5):455–460PubMedCrossRefGoogle Scholar
  141. 141.
    Eisenberg D, Marcotte EM, Xenarios I, Yeates TO (2000) Protein function in the post-genomic era. Nature 405(6788):823–826PubMedCrossRefGoogle Scholar
  142. 142.
    Enright AJ, Iliopoulos I, Kyrpides NC, Ouzounis CA (1999) Protein interaction maps for complete genomes based on gene fusion events. Nature 402(6757):86–90PubMedCrossRefGoogle Scholar
  143. 143.
    Fraser HB, Hirsh AE, Wall DP, Eisen MB (2004) Coevolution of gene expression among interacting proteins. Proc Natl Acad Sci USA 101(24):9033PubMedCrossRefGoogle Scholar
  144. 144.
    Blaschke C, Andrade MA, Ouzounis C, Valencia A (1999) Automatic extraction of biological information from scientific text: protein-protein interactions. Proc Int Conf Intell Syst Mol Biol 1999:60–67Google Scholar
  145. 145.
    Cusick ME, Yu H, Smolyar A, Venkatesan K, Carvunis AR, Simonis N, Rual JF, Borick H, Braun P, Dreze M (2008) Literature-curated protein interaction datasets. Nat Methods 6(1):39–46CrossRefGoogle Scholar
  146. 146.
    Russell RB, Alber F, Aloy P, Davis FP, Korkin D, Pichaud M, Topf M, Sali A (2004) A structural perspective on protein-protein interactions. Curr Opin Struct Biol 14(3):313–324PubMedCrossRefGoogle Scholar
  147. 147.
    Neuvirth H, Raz R, Schreiber G (2004) ProMate: a structure based prediction program to identify the location of protein-protein binding sites. J Mol Biol 338(1):181–199PubMedCrossRefGoogle Scholar
  148. 148.
    Stein A, Caol A, Aloy P (2011) 3did: identification and classification of domain-based interactions of known three-dimensional structure. Nucleic Acids Res 39(suppl 1):D718PubMedCrossRefGoogle Scholar
  149. 149.
    Aloy P, Russell RB (2003) InterPreTS: protein interaction prediction through tertiary structure. Bioinformatics 19(1):161PubMedCrossRefGoogle Scholar
  150. 150.
    Pazos F, Valencia A (2001) Similarity of phylogenetic trees as indicator of protein-protein interaction. Protein Eng 14(9):609PubMedCrossRefGoogle Scholar
  151. 151.
    Pagel P, Wong P, Frishman D (2004) A domain interaction map based on phylogenetic profiling. J Mol Biol 344(5):1331–1346PubMedCrossRefGoogle Scholar
  152. 152.
    Shoemaker BA, Panchenko AR (2007) Deciphering protein-protein interactions. Part II. Computational methods to predict protein and domain interaction partners. PLoS Comput Biol 3(4):e43PubMedCrossRefGoogle Scholar
  153. 153.
    Mavromatis K, Chu K, Ivanova N, Hooper SD, Markowitz VM, Kyrpides NC (2009) Gene context analysis in the Integrated Microbial Genomes (IMG) data management system. PLoS One 4(11):e7979PubMedCrossRefGoogle Scholar
  154. 154.
    Pazos F, Valencia A (2002) In silico two-hybrid system for the selection of physically interacting protein pairs. Proteins 47(2):219–227PubMedCrossRefGoogle Scholar
  155. 155.
    Pazos F, Valencia A (2008) Protein co-evolution, co-adaptation and interactions. EMBO J 27(20):2648–2655PubMedCrossRefGoogle Scholar
  156. 156.
    Friedberg I (2006) Automated protein function prediction: the genomic challenge. Brief Bioinform 7(3):225–242PubMedCrossRefGoogle Scholar
  157. 157.
    Snitkin E, Gustafson A, Mellor J, Wu J, DeLisi C (2006) Comparative assessment ofperformance and genome dependence among phylogenetic profiling methods. BMC Bioinformatics 7(1):420PubMedCrossRefGoogle Scholar
  158. 158.
    Orchard S, Salwinski L, Kerrien S, Montecchi-Palazzi L, Oesterheld M, Stümpflen V, Ceol A, Chatr-aryamontri A, Armstrong J, Woollard P (2007) The minimum information required for reporting a molecular interaction experiment (MIMIx). Nat Biotechnol 25(8):894–898PubMedCrossRefGoogle Scholar
  159. 159.
    Taylor CF, Paton NW, Lilley KS, Binz PA, Julian RK, Jones AR, Zhu W, Apweiler R, Aebersold R, Deutsch EW (2007) The minimum information about a proteomics experiment (MIAPE). Nat Biotechnol 25(8):887–893PubMedCrossRefGoogle Scholar
  160. 160.
    Gmuender H, Kuratli K, Di Padova K, Gray CP, Keck W, Evers S (2001) Gene expression changes triggered by exposure of Haemophilus influenzae to novobiocin or ciprofloxacin: combined transcription and translation analysis. Genome Res 11(1):28–42PubMedCrossRefGoogle Scholar
  161. 161.
    Yoon SH, Han MJ, Lee SY, Jeong KJ, Yoo JS (2003) Combined transcriptome and proteome analysis of Escherichia coli during high cell density culture. Biotechnol Bioeng 81(7):753–767PubMedCrossRefGoogle Scholar
  162. 162.
    Mostertz J, Scharf C, Hecker M, Homuth G (2004) Transcriptome and proteome analysis of Bacillus subtilis gene expression in response to superoxide and peroxide stress. Microbiology 150(2):497PubMedCrossRefGoogle Scholar
  163. 163.
    Gygi SP, Rochon Y, Franza BR, Aebersold R (1999) Correlation between protein and mRNA abundance in yeast. Mol Cell Biol 19(3):1720–1730PubMedGoogle Scholar
  164. 164.
    Bro C, Regenberg B, Lagniel G, Labarre J, Montero-Lomelí M, Nielsen J (2003) Transcriptional, proteomic, and metabolic responses to lithium in galactose-grown yeast cells. J Biol Chem 278(34):32141–32149PubMedCrossRefGoogle Scholar
  165. 165.
    Kramer JO, Sorgenfrei O, Klopprogge K, Heinzle E, Wittmann C (2004) In-depth profiling of lysine-producing Corynebacterium glutamicum by combined analysis of the transcriptome, metabolome, and fluxome. J Bacteriol 186(6):1769–1784CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2013

Authors and Affiliations

  • Adrie J. C. Steyn
    • 1
    • 2
    • 3
  • D. Mai
    • 1
  • V. Saini
    • 1
  • A. Farhana
    • 1
  1. 1.Department of MicrobiologyUniversity of Alabama at BirminghamBirminghamUSA
  2. 2.Center for AIDS ResearchUniversity of Alabama at BirminghamBirminghamUSA
  3. 3.KwaZulu-Natal Research Institute for Tuberculosis and HIV, CongellaDurbanSouth Africa

Personalised recommendations