Two-component sensor histidine kinases of Mycobacterium tuberculosis: Beacons for niche navigation.

Miljan Stupar, Juanelle Furness, Christopher J De Voss, Lendl Tan, Nicholas P West
Author Information
  1. Miljan Stupar: School of Chemistry and Molecular Biosciences, Australian Infectious Disease Research Centre, University of Queensland, Brisbane, Queensland, Australia. ORCID
  2. Juanelle Furness: School of Chemistry and Molecular Biosciences, Australian Infectious Disease Research Centre, University of Queensland, Brisbane, Queensland, Australia. ORCID
  3. Christopher J De Voss: School of Chemistry and Molecular Biosciences, Australian Infectious Disease Research Centre, University of Queensland, Brisbane, Queensland, Australia. ORCID
  4. Lendl Tan: School of Chemistry and Molecular Biosciences, Australian Infectious Disease Research Centre, University of Queensland, Brisbane, Queensland, Australia. ORCID
  5. Nicholas P West: School of Chemistry and Molecular Biosciences, Australian Infectious Disease Research Centre, University of Queensland, Brisbane, Queensland, Australia. ORCID

Abstract

Intracellular bacterial pathogens such as Mycobacterium tuberculosis are remarkably adept at surviving within a host, employing a variety of mechanisms to counteract host defenses and establish a protected niche. Constant surveying of the environment is key for pathogenic mycobacteria to discern their immediate location and coordinate the expression of genes necessary for adaptation. Two-component systems efficiently perform this role, typically comprised of a transmembrane sensor kinase and a cytoplasmic response regulator. In this review, we describe the role of two-component systems in bacterial pathogenesis, focusing predominantly on the role of sensor kinases of M. tuberculosis. We highlight important features of sensor kinases in mycobacterial infection, discuss ways in which these signaling proteins sense and respond to environments, and how this is attuned to their intracellular lifestyle. Finally, we discuss recent studies which have identified and characterized inhibitors of two-component sensor kinases toward establishing a new strategy in anti-mycobacterial therapy.

Keywords

References

  1. Cell Microbiol. 2009 Aug;11(8):1151-9 [PMID: 19388905]
  2. BMC Microbiol. 2014 Jul 21;14:195 [PMID: 25048654]
  3. Antioxid Redox Signal. 2015 Mar 1;22(7):603-13 [PMID: 25333974]
  4. Mol Microbiol. 2006 Feb;59(4):1199-215 [PMID: 16430694]
  5. Microbiology (Reading). 2015 Mar;161(Pt 3):477-89 [PMID: 25536998]
  6. Infect Immun. 2019 Jan 24;87(2): [PMID: 30455198]
  7. Biochemistry. 2011 Feb 15;50(6):1023-8 [PMID: 21250657]
  8. Biochemistry. 2008 Nov 25;47(47):12523-31 [PMID: 18980385]
  9. Annu Rev Microbiol. 2012;66:325-47 [PMID: 22746333]
  10. J Biol Chem. 2008 Jun 27;283(26):18032-9 [PMID: 18400743]
  11. FEMS Microbiol Lett. 2004 Jul 15;236(2):341-7 [PMID: 15251217]
  12. Microbiology (Reading). 2013 Oct;159(Pt 10):2074-2086 [PMID: 23946493]
  13. Sci Signal. 2017 Jan 10;10(461): [PMID: 28074004]
  14. Mol Biol Cell. 2006 Jan;17(1):498-510 [PMID: 16251362]
  15. Oxid Med Cell Longev. 2018 Oct 11;2018:7695364 [PMID: 30405878]
  16. PLoS One. 2015 Aug 13;10(8):e0135208 [PMID: 26270051]
  17. J Bacteriol. 1993 Jun;175(11):3259-68 [PMID: 8501030]
  18. J Bacteriol. 2018 Mar 26;200(8): [PMID: 29378889]
  19. FEMS Microbiol Rev. 1995 Jul;16(4):309-21 [PMID: 7654406]
  20. Curr Opin Microbiol. 2010 Apr;13(2):116-23 [PMID: 20223701]
  21. FEBS J. 2019 Nov;286(21):4278-4293 [PMID: 31254441]
  22. Infect Immun. 2002 May;70(5):2256-63 [PMID: 11953357]
  23. FASEB J. 2021 Apr;35(4):e21475 [PMID: 33772870]
  24. Biochem Biophys Res Commun. 2014 Apr 18;446(4):1172-8 [PMID: 24667597]
  25. Tuberculosis (Edinb). 2004;84(3-4):247-55 [PMID: 15207494]
  26. Microbiology (Reading). 2000 Dec;146 Pt 12:3091-3098 [PMID: 11101667]
  27. Mol Microbiol. 2011 May;80(3):678-94 [PMID: 21401735]
  28. Trends Microbiol. 2019 Nov;27(11):942-953 [PMID: 31324436]
  29. J Bacteriol. 2007 Aug;189(15):5495-503 [PMID: 17526710]
  30. Front Microbiol. 2020 Sep 16;11:572433 [PMID: 33042081]
  31. Mucosal Immunol. 2021 Jan;14(1):229-241 [PMID: 32483198]
  32. Elife. 2021 May 18;10: [PMID: 34003742]
  33. Microbiology (Reading). 2004 Apr;150(Pt 4):865-875 [PMID: 15073296]
  34. J Bacteriol. 2013 Jan;195(1):66-75 [PMID: 23104803]
  35. Nat Med. 2014 Jan;20(1):75-9 [PMID: 24336248]
  36. Chem Rev. 2019 Jan 23;119(2):1193-1220 [PMID: 30474981]
  37. J Microbiol. 2012 Apr;50(2):270-7 [PMID: 22538656]
  38. Annu Rev Immunol. 2018 Apr 26;36:639-665 [PMID: 29400999]
  39. Biochem J. 2015 Jul 1;469(1):121-34 [PMID: 25929189]
  40. J Infect Dis. 2009 Oct 1;200(7):1126-35 [PMID: 19686042]
  41. J Med Chem. 2014 Aug 14;57(15):6572-82 [PMID: 24967731]
  42. Infect Immun. 2009 Aug;77(8):3258-63 [PMID: 19487478]
  43. J Bacteriol. 2014 Jan;196(2):391-406 [PMID: 24187094]
  44. Immunol Rev. 2015 Mar;264(1):288-307 [PMID: 25703567]
  45. J Bacteriol. 2012 Jan;194(2):354-61 [PMID: 22081401]
  46. Antimicrob Agents Chemother. 2015 Aug;59(8):4436-45 [PMID: 25987613]
  47. J Biol Chem. 2009 May 8;284(19):13057-67 [PMID: 19276084]
  48. J Biol Chem. 2015 Mar 27;290(13):8294-309 [PMID: 25659431]
  49. FEBS J. 2019 Feb;286(3):479-494 [PMID: 30570222]
  50. Mol Microbiol. 2001 Jul;41(1):179-87 [PMID: 11454210]
  51. J Clin Invest. 2016 Mar 1;126(3):1093-108 [PMID: 26901813]
  52. Microbiology (Reading). 2003 Jun;149(Pt 6):1423-1435 [PMID: 12777483]
  53. FEMS Microbiol Lett. 2006 May;258(2):250-6 [PMID: 16640581]
  54. Microbiology (Reading). 2004 Jan;150(Pt 1):241-246 [PMID: 14702417]
  55. Nat Rev Immunol. 2012 Apr 20;12(5):352-66 [PMID: 22517424]
  56. Biochemistry. 2012 Jan 10;51(1):159-66 [PMID: 22142262]
  57. J Biol Chem. 2016 Jul 29;291(31):16100-11 [PMID: 27235395]
  58. Mol Microbiol. 2017 May;104(3):400-411 [PMID: 28142206]
  59. J Mol Biol. 2019 Feb 15;431(4):777-793 [PMID: 30639188]
  60. Cell Microbiol. 2013 Jun;15(6):843-59 [PMID: 23253353]
  61. BMC Microbiol. 2014 Oct 25;14:265 [PMID: 25344463]
  62. FEBS Lett. 2006 Oct 2;580(22):5328-38 [PMID: 16979633]
  63. Microbiol Spectr. 2017 Jun;5(3): [PMID: 28597811]
  64. Infect Immun. 2015 Dec 28;84(3):735-46 [PMID: 26712204]
  65. J Struct Biol. 2012 Feb;177(2):498-505 [PMID: 22115998]
  66. J Biol Chem. 2004 May 28;279(22):23082-7 [PMID: 15033981]
  67. ACS Omega. 2017 Jul 31;2(7):3509-3517 [PMID: 28782049]
  68. PLoS Pathog. 2012;8(6):e1002769 [PMID: 22737072]
  69. FEBS Lett. 2005 Aug 1;579(19):4145-8 [PMID: 16026786]
  70. Infect Immun. 2003 Mar;71(3):1134-40 [PMID: 12595424]
  71. J Mol Biol. 2005 Nov 11;353(5):929-36 [PMID: 16213520]
  72. Microb Pathog. 1999 Apr;26(4):195-206 [PMID: 10089160]
  73. Biochem Biophys Res Commun. 2014 Feb 21;444(4):651-5 [PMID: 24491537]
  74. Mol Microbiol. 2016 May;100(3):510-26 [PMID: 26800324]
  75. PLoS Pathog. 2013;9(4):e1003282 [PMID: 23592993]
  76. FEBS Lett. 2007 May 1;581(9):1903-9 [PMID: 17434492]
  77. Proc Natl Acad Sci U S A. 2007 Jul 10;104(28):11568-73 [PMID: 17609369]
  78. Future Microbiol. 2012 Apr;7(4):513-8 [PMID: 22439727]
  79. Cell Host Microbe. 2014 Oct 8;16(4):538-48 [PMID: 25299337]
  80. Nat Chem Biol. 2017 Feb;13(2):218-225 [PMID: 27992879]
  81. Nature. 1998 Jun 11;393(6685):537-44 [PMID: 9634230]
  82. Proc Natl Acad Sci U S A. 2001 Jun 19;98(13):7534-9 [PMID: 11416222]
  83. Am J Respir Crit Care Med. 2015 May 15;191(10):1185-96 [PMID: 25730547]
  84. Biochemistry. 2007 Apr 10;46(14):4250-60 [PMID: 17371046]
  85. Structure. 2006 Feb;14(2):275-85 [PMID: 16472747]
  86. ACS Chem Biol. 2020 Jan 17;15(1):52-62 [PMID: 31556993]
  87. Mol Microbiol. 2022 May;117(5):973-985 [PMID: 35338720]
  88. Infect Immun. 2021 Mar 17;89(4): [PMID: 33526568]
  89. J Exp Med. 2003 Sep 1;198(5):693-704 [PMID: 12953091]
  90. Annu Rev Genet. 2007;41:121-45 [PMID: 18076326]
  91. mSystems. 2021 Feb 16;6(1): [PMID: 33594002]
  92. Infect Immun. 2009 Mar;77(3):1230-7 [PMID: 19103767]
  93. Nat Immunol. 2009 Sep;10(9):943-8 [PMID: 19692995]
  94. Biochemistry. 2007 Jun 12;46(23):6733-43 [PMID: 17511470]
  95. J Bacteriol. 2006 Mar;188(6):2134-43 [PMID: 16513743]
  96. Immunol Rev. 2014 Nov;262(1):179-92 [PMID: 25319335]
  97. J Biol Chem. 2019 Dec 27;294(52):19862-19876 [PMID: 31653701]
  98. Mol Microbiol. 2003 Feb;47(4):1075-89 [PMID: 12581360]
  99. Arch Biochem Biophys. 2016 Dec 15;612:1-8 [PMID: 27729224]
  100. J Exp Med. 2003 Sep 1;198(5):705-13 [PMID: 12953092]
  101. Cell Host Microbe. 2008 May 15;3(5):323-30 [PMID: 18474359]
  102. Infect Immun. 2013 Jan;81(1):317-28 [PMID: 23132496]
  103. J Bacteriol. 1992 Apr;174(7):2053-8 [PMID: 1551826]
  104. Mol Microbiol. 2003 May;48(3):833-43 [PMID: 12694625]
  105. Proc Natl Acad Sci U S A. 2001 Oct 23;98(22):12706-11 [PMID: 11675502]
  106. Annu Rev Microbiol. 2010;64:539-59 [PMID: 20825354]
  107. Protein Sci. 2007 Aug;16(8):1708-19 [PMID: 17600145]
  108. Mol Microbiol. 2014 Oct;94(1):56-69 [PMID: 24975990]
  109. Infect Immun. 2003 Dec;71(12):6962-70 [PMID: 14638785]
  110. Microbiology (Reading). 2007 Apr;153(Pt 4):1229-1242 [PMID: 17379732]
  111. Am J Med Sci. 2019 Mar;357(3):184-194 [PMID: 30797501]
  112. Commun Biol. 2019 Sep 20;2:349 [PMID: 31552302]
  113. Front Microbiol. 2017 Oct 12;8:2008 [PMID: 29085351]
  114. Genes Cells. 2000 Jul;5(7):555-69 [PMID: 10947842]
  115. ACS Chem Biol. 2015 Jan 16;10(1):213-24 [PMID: 25436989]
  116. Curr Opin Microbiol. 2021 Jun;61:107-114 [PMID: 33932730]
  117. Nat Rev Microbiol. 2018 Oct;16(10):585-593 [PMID: 30008469]
  118. Cell Host Microbe. 2018 Sep 12;24(3):439-446.e4 [PMID: 30146391]
  119. Cell Microbiol. 2003 Sep;5(9):637-48 [PMID: 12925133]
  120. Biochimie. 2010 Mar;92(3):263-72 [PMID: 19962420]
  121. Mol Microbiol. 2006 Apr;60(2):312-30 [PMID: 16573683]

MeSH Term

Adaptation, Physiological
Bacterial Proteins
Histidine
Histidine Kinase
Humans
Mycobacterium Infections
Mycobacterium tuberculosis

Chemicals

Bacterial Proteins
Histidine
Histidine Kinase

Word Cloud

Created with Highcharts 10.0.0sensorkinasesMycobacteriumtuberculosisroletwo-componentbacterialhostnicheTwo-componentsystemskinasediscusshistidineIntracellularpathogensremarkablyadeptsurvivingwithinemployingvarietymechanismscounteractdefensesestablishprotectedConstantsurveyingenvironmentkeypathogenicmycobacteriadiscernimmediatelocationcoordinateexpressiongenesnecessaryadaptationefficientlyperformtypicallycomprisedtransmembranecytoplasmicresponseregulatorreviewdescribepathogenesisfocusingpredominantlyMhighlightimportantfeaturesmycobacterialinfectionwayssignalingproteinssenserespondenvironmentsattunedintracellularlifestyleFinallyrecentstudiesidentifiedcharacterizedinhibitorstowardestablishingnewstrategyanti-mycobacterialtherapytuberculosis:BeaconsnavigationTBantibiotictargetstranscriptionalregulation

Similar Articles

Cited By