Advertisement

Opportunities and Challenges in Activity-Based Protein Profiling of Mycobacteria

  • Hiren V. Patel
  • Michael Li
  • Jessica C. SeeligerEmail author
Chapter
Part of the Current Topics in Microbiology and Immunology book series (CT MICROBIOLOGY, volume 420)

Abstract

Mycobacteria, from saprophytic to pathogenic species, encounter diverse environments that demand metabolic versatility and rapid adaptation from these bacteria for their survival. The human pathogen Mycobacterium tuberculosis, for example, can enter a reversible state of dormancy in which it is metabolically active, but does not increase in number, and which is believed to enable its survival in the human host for years, with attendant risk for reactivation to active tuberculosis. Driven by the need to combat mycobacterial diseases like tuberculosis, efforts to understand such adaptations have benefitted in recent years from application of activity-based probes. These studies have been inspired by the potential of these chemical tools to uncover protein function for previously unannotated proteins, track shifts in protein activity as a function of environment, and provide a streamlined method for screening and developing inhibitors. Here we seek to contextualize progress thus far with achieving these goals and highlight the unique challenges and opportunities for activity-based probes to further our understanding of protein function and regulation, bacterial physiology, and antibiotic development.

Notes

Acknowledgements

We thank Dr. Benjamin Cravatt, Dr. Peter Tonge, and members of the Seeliger laboratory for helpful discussions on topics and concepts discussed in this review.

References

  1. Ansong C et al (2013) Identification of widespread adenosine nucleotide binding in Mycobacterium tuberculosis. Chem Biol 20:123–133CrossRefGoogle Scholar
  2. Arastu-Kapur S et al (2008) Identification of proteases that regulate erythrocyte rupture by the malaria parasite Plasmodium falciparum. Nat Chem Biol 4:203–213.  https://doi.org/10.1038/nchembio.70CrossRefGoogle Scholar
  3. Barglow KT, Cravatt BF (2007) Activity-based protein profiling for the functional annotation of enzymes. Nat Methods 4:822–827.  https://doi.org/10.1038/nmeth1092CrossRefPubMedGoogle Scholar
  4. Belardinelli JM, Larrouy-Maumus G, Jones V, Sorio de Carvalho LP, McNeil MR, Jackson M (2014) Biosynthesis and translocation of unsulfated acyltrehaloses in Mycobacterium tuberculosis. J Biol Chem 289:27952–27965.  https://doi.org/10.1074/jbc.M114.581199CrossRefPubMedPubMedCentralGoogle Scholar
  5. Cole ST et al (1998) Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393:537–544CrossRefGoogle Scholar
  6. Cowley S et al (2004) The Mycobacterium tuberculosis protein serine/threonine kinase PknG is linked to cellular glutamate/glutamine levels and is important for growth in vivo. Mol Microbiol 52:1691–1702.  https://doi.org/10.1111/j.1365-2958.2004.04085.xCrossRefPubMedGoogle Scholar
  7. Cravatt BF, Wright AT, Kozarich JW (2008) Activity-based protein profiling: from enzyme chemistry to proteomic chemistry. Annu Rev Biochem 77:383–414.  https://doi.org/10.1146/annurev.biochem.75.101304.124125CrossRefGoogle Scholar
  8. Duckworth BP, Wilson DJ, Nelson KM, Boshoff HI, Barry CE 3rd, Aldrich CC (2012) Development of a selective activity-based probe for adenylating enzymes: profiling MbtA Involved in siderophore biosynthesis from Mycobacterium tuberculosis. ACS Chem Biol 7:1653–1658.  https://doi.org/10.1021/cb300112xCrossRefPubMedPubMedCentralGoogle Scholar
  9. Ernst JD (2012) The immunological life cycle of tuberculosis. Nat Rev Immunol 12:581–591.  https://doi.org/10.1038/nri3259CrossRefPubMedGoogle Scholar
  10. Fernandez P, Saint-Joanis B, Barilone N, Jackson M, Gicquel B, Cole ST, Alzari PM (2006) The Ser/Thr protein kinase PknB is essential for sustaining mycobacterial growth. J Bacteriol 188:7778–7784.  https://doi.org/10.1128/JB.00963-06CrossRefPubMedPubMedCentralGoogle Scholar
  11. Galagan JE et al (2013) The Mycobacterium tuberculosis regulatory network and hypoxia. Nature 499:178–183.  https://doi.org/10.1038/nature12337CrossRefPubMedPubMedCentralGoogle Scholar
  12. Glickman MS, Cox JS, Jacobs WR (2000) A novel mycolic acid cyclopropane synthetase is required for cording persistence, and virulence of Mycobacterium tuberculosis. Mol Cell 5:717–727CrossRefGoogle Scholar
  13. Gold B, Nathan C (2017) Targeting phenotypically tolerant Mycobacterium tuberculosis. Microbiol Spectr 5  https://doi.org/10.1128/microbiolspec.tbtb2-0031-2016
  14. Greenbaum DC et al. (2002) A role for the protease falcipain 1 in host cell invasion by the human malaria parasite. Science 298:2002–2006  https://doi.org/10.1126/science.1077426CrossRefGoogle Scholar
  15. Hatzios SK et al. (2013) Osmosensory signaling in Mycobacterium tuberculosis mediated by a eukaryotic-like Ser/Thr protein kinase. Proc Natl Acad Sci USA 110:E5069–5077.  https://doi.org/10.1073/pnas.1321205110CrossRefGoogle Scholar
  16. Johnston JM, Jiang M, Guo Z, Baker EN (2010) Structural and functional analysis of Rv0554 from Mycobacterium tuberculosis: testing a putative role in menaquinone biosynthesis. Acta Crystallogr D Biol Crystallogr 66:909–917.  https://doi.org/10.1107/S0907444910025771CrossRefPubMedGoogle Scholar
  17. Kumar D, Palaniyandi K, Challu VK, Kumar P, Narayanan S (2013) PknE, a serine/threonine protein kinase from Mycobacterium tuberculosis has a role in adaptive responses. Arch Microbiol 195:75–80.  https://doi.org/10.1007/s00203-012-0848-4CrossRefPubMedGoogle Scholar
  18. Lehmann J et al (2017) An antibacterial beta-lactone kills Mycobacterium tuberculosis by infiltrating mycolic acid biosynthesis. Angew Chem Int Ed Engl.  https://doi.org/10.1002/anie.201709365CrossRefPubMedPubMedCentralGoogle Scholar
  19. Lentz CS et al (2016) Design of selective substrates and activity-based probes for hydrolase important for pathogenesis 1 (HIP1) from Mycobacterium tuberculosis. ACS Infect Dis  https://doi.org/10.1021/acsinfecdis.6b00092CrossRefGoogle Scholar
  20. Madacki J et al (2018) Impact of the epoxide hydrolase EphD on the metabolism of mycolic acids in mycobacteria. J Biol Chem 293:5172–5184.  https://doi.org/10.1074/jbc.RA117.000246CrossRefPubMedGoogle Scholar
  21. Meena LS, Chopra P, Vishwakarma RA, Singh Y (2013) Biochemical characterization of an S-adenosyl-l-methionine-dependent methyltransferase (Rv0469) of Mycobacterium tuberculosis. Biol Chem 394:871–877.  https://doi.org/10.1515/hsz-2013-0126CrossRefPubMedGoogle Scholar
  22. Ortega C et al (2016) Systematic survey of serine hydrolase activity in Mycobacterium tuberculosis defines changes associated with persistence cell. Chem Biol 23:290–298.  https://doi.org/10.1016/j.chembiol.2016.01.003CrossRefGoogle Scholar
  23. Ortega C et al (2014) Mycobacterium tuberculosis Ser/Thr protein kinase B mediates an oxygen-dependent replication switch. PLoS Biol 12:e1001746.  https://doi.org/10.1371/journal.pbio.1001746CrossRefPubMedPubMedCentralGoogle Scholar
  24. Portevin D, De Sousa-D’Auria C, Houssin C, Grimaldi C, Chami M, Daffe M, Guilhot C (2004) A polyketide synthase catalyzes the last condensation step of mycolic acid biosynthesis in mycobacteria and related organisms. Proc Natl Acad Sci U S A 101:314–319.  https://doi.org/10.1073/pnas.0305439101CrossRefPubMedGoogle Scholar
  25. Quadri LE (2014) Biosynthesis of mycobacterial lipids by polyketide synthases and beyond. Crit Rev Biochem Mol Biol 49:179–211.  https://doi.org/10.3109/10409238.2014.896859CrossRefPubMedGoogle Scholar
  26. Ravindran MS, Rao SP, Cheng X, Shukla A, Cazenave-Gassiot A, Yao SQ, Wenk MR (2014) Targeting lipid esterases in mycobacteria grown under different physiological conditions using activity-based profiling with Tetrahydrolipstatin (THL). Mol Cell Proteomics 13:435–448  https://doi.org/10.1074/mcp.m113.029942CrossRefGoogle Scholar
  27. Rittershaus ES, Baek SH, Sassetti CM (2013) The normalcy of dormancy: common themes in microbial quiescence. Cell Host Microbe 13:643–651.  https://doi.org/10.1016/j.chom.2013.05.012CrossRefPubMedPubMedCentralGoogle Scholar
  28. Rustad TR, Sherrid AM, Minch KJ, Sherman DR (2009) Hypoxia: a window into Mycobacterium tuberculosis latency. Cell Microbiol 11:1151–1159.  https://doi.org/10.1111/j.1462-5822.2009.01325.xCrossRefPubMedGoogle Scholar
  29. Seeliger JC et al (2012) Elucidation and chemical modulation of sulfolipid-1 biosynthesis in Mycobacterium tuberculosis. J Biol Chem 287:7990–8000.  https://doi.org/10.1074/jbc.M111.315473CrossRefPubMedGoogle Scholar
  30. Simon GM, Cravatt BF (2010) Activity-based proteomics of enzyme superfamilies: serine hydrolases as a case study. J Biol Chem 285:11051–11055.  https://doi.org/10.1074/jbc.R109.097600CrossRefPubMedPubMedCentralGoogle Scholar
  31. Tallman KR, Levine SR, Beatty KE (2016) Small-molecule probes Reveal Esterases with persistent activity in dormant and reactivating Mycobacterium tuberculosis ACS. Infect Dis 2:936–944.  https://doi.org/10.1021/acsinfecdis.6b00135CrossRefGoogle Scholar
  32. Touchette MH, Holsclaw CM, Previti ML, Solomon VC, Leary JA, Bertozzi CR, Seeliger JC (2015) The rv1184c locus encodes Chp2, an acyltransferase in Mycobacterium tuberculosis polyacyltrehalose lipid biosynthesis. J Bacteriol 197:201–210.  https://doi.org/10.1128/JB.02015-14CrossRefPubMedGoogle Scholar
  33. Viader A et al. (2016) A chemical proteomic atlas of brain serine hydrolases identifies cell type- specific pathways regulating neuroinflammation Elife 5  https://doi.org/10.7554/elife.12345
  34. Wei J-R et al (2011) Depletion of antibiotic targets has widely varying effects on growth. Proc Natl Acad Sci U S A 108:4176–4181.  https://doi.org/10.1073/pnas.1018301108CrossRefPubMedPubMedCentralGoogle Scholar
  35. Wolfe LM et al (2013) A chemical proteomics approach to profiling the ATP-binding proteome of Mycobacterium tuberculosis. Mol Cell Proteomics 12:1644–1660.  https://doi.org/10.1074/mcp.M112.025635CrossRefPubMedPubMedCentralGoogle Scholar
  36. Zimmer JS, Monroe ME, Qian WJ, Smith RD (2006) Advances in proteomics data analysis and display using an accurate mass and time tag approach. Mass Spectrom Rev 25:450–482.  https://doi.org/10.1002/mas.20071CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  • Hiren V. Patel
    • 1
  • Michael Li
    • 2
  • Jessica C. Seeliger
    • 2
    Email author
  1. 1.Department of Molecular Genetics and MicrobiologyStony Brook UniversityStony BrookUSA
  2. 2.Department of Pharmacological SciencesStony Brook UniversityStony BrookUSA

Personalised recommendations