Display options
Cite
Bekere I, Huang J, Schnapp M, et al. Yersinia remodels epigenetic histone modifications in human macrophages. PLoS Pathog. 2021;17(11):e1010074doi: 10.1371/journal.ppat.1010074.
Bekere, I., Huang, J., Schnapp, M., Rudolph, M., Berneking, L., Ruckdeschel, K., Grundhoff, A., Günther, T., Fischer, N., & Aepfelbacher, M. (2021). Yersinia remodels epigenetic histone modifications in human macrophages. PLoS pathogens, 17(11), e1010074. https://doi.org/10.1371/journal.ppat.1010074
Bekere, Indra, et al. "Yersinia remodels epigenetic histone modifications in human macrophages." PLoS pathogens vol. 17,11 (2021): e1010074. doi: https://doi.org/10.1371/journal.ppat.1010074
Bekere I, Huang J, Schnapp M, Rudolph M, Berneking L, Ruckdeschel K, Grundhoff A, Günther T, Fischer N, Aepfelbacher M. Yersinia remodels epigenetic histone modifications in human macrophages. PLoS Pathog. 2021 Nov 18;17(11):e1010074. doi: 10.1371/journal.ppat.1010074. eCollection 2021 Nov. PMID: 34793580; PMCID: PMC8639070.
Copy Download .nbib Format: NLM
Share it on

PLoS Pathog. 2021 Nov 18;17(11):e1010074. doi: 10.1371/journal.ppat.1010074. eCollection 2021 Nov.

Yersinia remodels epigenetic histone modifications in human macrophages.

PLoS pathogens

Indra Bekere, Jiabin Huang, Marie Schnapp, Maren Rudolph, Laura Berneking, Klaus Ruckdeschel, Adam Grundhoff, Thomas Günther, Nicole Fischer, Martin Aepfelbacher

Affiliations

  1. Institute of Medical Microbiology, Virology and Hygiene, University Medical Center Hamburg-Eppendorf (UKE), Hamburg, Germany.
  2. Heinrich-Pette-Institute (HPI), Leibniz Institute for Experimental Virology, Research Group Virus Genomics, Hamburg, Germany.

PMID: 34793580 PMCID: PMC8639070 DOI: 10.1371/journal.ppat.1010074

Abstract

Various pathogens systematically reprogram gene expression in macrophages, but the underlying mechanisms are largely unknown. We investigated whether the enteropathogen Yersinia enterocolitica alters chromatin states to reprogram gene expression in primary human macrophages. Genome-wide chromatin immunoprecipitation (ChIP) seq analyses showed that pathogen-associated molecular patterns (PAMPs) induced up- or down-regulation of histone modifications (HMod) at approximately 14500 loci in promoters and enhancers. Effectors of Y. enterocolitica reorganized about half of these dynamic HMod, with the effector YopP being responsible for about half of these modulatory activities. The reorganized HMod were associated with genes involved in immune response and metabolism. Remarkably, the altered HMod also associated with 61% of all 534 known Rho GTPase pathway genes, revealing a new level in Rho GTPase regulation and a new aspect of bacterial pathogenicity. Changes in HMod were associated to varying degrees with corresponding gene expression, e. g. depending on chromatin localization and cooperation of the HMod. In summary, infection with Y. enterocolitica remodels HMod in human macrophages to modulate key gene expression programs of the innate immune response.

Conflict of interest statement

The authors have declared that no competing interests exist.

References

  1. Bioinformatics. 2009 Aug 1;25(15):1952-8 - PubMed
  2. Nat Cell Biol. 2019 Jul;21(7):867-878 - PubMed
  3. J Pathol. 2008 Jan;214(2):161-78 - PubMed
  4. Science. 2006 May 26;312(5777):1211-4 - PubMed
  5. Cell Res. 2011 Apr;21(4):564-78 - PubMed
  6. J Immunol. 2001 Feb 1;166(3):1823-31 - PubMed
  7. Int J Med Microbiol. 2016 Sep;306(6):357-66 - PubMed
  8. PLoS One. 2013 Jun 10;8(6):e65598 - PubMed
  9. Mol Biol Cell. 2006 Jun;17(6):2811-23 - PubMed
  10. Bioinformatics. 2009 Jul 15;25(14):1754-60 - PubMed
  11. Cell Microbiol. 2004 Apr;6(4):377-90 - PubMed
  12. Annu Rev Microbiol. 2020 Sep 8;74:221-245 - PubMed
  13. Nat Rev Mol Cell Biol. 2008 Sep;9(9):690-701 - PubMed
  14. Mol Immunol. 2016 Mar;71:184-191 - PubMed
  15. Cell Host Microbe. 2013 Apr 17;13(4):395-405 - PubMed
  16. Curr Biol. 2021 May 24;31(10):2051-2064.e8 - PubMed
  17. Nat Commun. 2019 Jul 25;10(1):3320 - PubMed
  18. Bioinformatics. 2014 Apr 1;30(7):923-30 - PubMed
  19. Mol Cell Biol. 2009 Apr;29(7):1735-48 - PubMed
  20. FEBS J. 2020 Oct;287(19):4232-4245 - PubMed
  21. FASEB J. 2000 Aug;14(11):1471-84 - PubMed
  22. Nat Genet. 2008 Jul;40(7):897-903 - PubMed
  23. Cell Microbiol. 2004 Feb;6(2):129-41 - PubMed
  24. Cell Microbiol. 2003 Dec;5(12):957-71 - PubMed
  25. J Exp Med. 2004 Jan 5;199(1):81-90 - PubMed
  26. Clin Microbiol Rev. 2009 Apr;22(2):240-73, Table of Contents - PubMed
  27. Nat Microbiol. 2020 Jan;5(1):14-26 - PubMed
  28. Nat Rev Microbiol. 2010 Feb;8(2):117-28 - PubMed
  29. Nat Protoc. 2009;4(1):44-57 - PubMed
  30. Blood. 2001 Apr 15;97(8):2457-68 - PubMed
  31. Trends Immunol. 2013 May;34(5):216-23 - PubMed
  32. PLoS One. 2019 Feb 21;14(2):e0209592 - PubMed
  33. Nucleic Acids Res. 2019 Jan 8;47(D1):D786-D792 - PubMed
  34. PLoS Pathog. 2016 Jun 14;12(6):e1005660 - PubMed
  35. Cell. 2010 Mar 19;140(6):805-20 - PubMed
  36. Semin Immunopathol. 2020 Apr;42(2):201-213 - PubMed
  37. Arch Immunol Ther Exp (Warsz). 2006 May-Jun;54(3):149-63 - PubMed
  38. Nature. 2018 Sep;561(7721):122-126 - PubMed
  39. Infect Immun. 2010 Dec;78(12):5086-98 - PubMed
  40. Biol Chem. 2000 May-Jun;381(5-6):421-6 - PubMed
  41. Infect Immun. 2009 Jun;77(6):2251-61 - PubMed
  42. Genome Biol. 2014;15(12):550 - PubMed
  43. Nat Rev Mol Cell Biol. 2006 Jan;7(1):54-62 - PubMed
  44. Mol Microbiol. 1997 Mar;23(5):861-7 - PubMed
  45. Int J Med Microbiol. 2013 Dec;303(8):433-42 - PubMed
  46. Curr Top Microbiol Immunol. 2017;399:201-220 - PubMed
  47. PLoS One. 2012;7(7):e40730 - PubMed
  48. Nat Cell Biol. 2020 Jan;22(1):120-134 - PubMed
  49. Cell. 2016 Nov 17;167(5):1354-1368.e14 - PubMed
  50. J Biol Chem. 2003 Jun 13;278(24):21909-19 - PubMed
  51. Science. 2014 Sep 26;345(6204):1251086 - PubMed
  52. Infect Immun. 2012 Jul;80(7):2519-27 - PubMed
  53. Front Cell Infect Microbiol. 2018 Aug 21;8:287 - PubMed
  54. Nucleic Acids Res. 2015 Apr 20;43(7):e47 - PubMed
  55. Cell Res. 2020 Apr;30(4):315-327 - PubMed
  56. Nucleic Acids Res. 2016 Mar 18;44(5):e45 - PubMed
  57. Mol Cell Proteomics. 2017 Jan;16(1):73-85 - PubMed
  58. Nat Rev Genet. 2016 Aug;17(8):487-500 - PubMed
  59. J Immunol. 2014 Sep 15;193(6):2661-8 - PubMed
  60. Mol Biol Evol. 2007 Jan;24(1):203-16 - PubMed
  61. Infect Immun. 2004 Sep;72(9):5227-34 - PubMed
  62. Front Immunol. 2019 Jul 31;10:1813 - PubMed
  63. J Biol Chem. 2002 Jul 12;277(28):25133-42 - PubMed
  64. J Allergy Clin Immunol. 2019 Nov;144(5):1364-1376 - PubMed
  65. PLoS Pathog. 2009 Dec;5(12):e1000686 - PubMed
  66. Bioessays. 2007 Apr;29(4):356-70 - PubMed
  67. Cell. 2013 Jan 17;152(1-2):157-71 - PubMed
  68. PLoS One. 2016 Mar 22;11(3):e0151788 - PubMed
  69. Curr Top Microbiol Immunol. 2016;397:69-90 - PubMed
  70. Proc Natl Acad Sci U S A. 2018 Nov 13;115(46):E10888-E10897 - PubMed
  71. Nature. 2006 Nov 30;444(7119):567-73 - PubMed
  72. Proc Natl Acad Sci U S A. 2017 Jan 31;114(5):E791-E800 - PubMed
  73. PLoS Pathog. 2006 Sep;2(9):e86 - PubMed
  74. Crit Rev Biochem Mol Biol. 2015 Mar-Apr;50(2):85-133 - PubMed
  75. Biochim Biophys Acta. 2014 Aug;1839(8):711-8 - PubMed
  76. Cell Host Microbe. 2010 May 20;7(5):376-87 - PubMed
  77. Proc Natl Acad Sci U S A. 2007 Oct 9;104(41):16245-50 - PubMed
  78. mBio. 2018 Feb 20;9(1): - PubMed
  79. Mol Microbiol. 2002 Aug;45(3):805-15 - PubMed
  80. Infect Immun. 2004 Dec;72(12):6780-9 - PubMed
  81. J Immunol. 2005 Jun 15;174(12):7939-49 - PubMed
  82. J Cell Sci. 2004 Mar 15;117(Pt 8):1301-12 - PubMed
  83. Annu Rev Cell Dev Biol. 2005;21:247-69 - PubMed
  84. Nature. 2011 Feb 10;470(7333):279-83 - PubMed
  85. Infect Immun. 2003 Oct;71(10):5892-9 - PubMed
  86. Cell. 2007 May 18;129(4):823-37 - PubMed
  87. BMC Bioinformatics. 2012 Jun 18;13:134 - PubMed
  88. Mol Cell. 2017 Sep 21;67(6):1037-1048.e6 - PubMed
  89. Biol Cell. 2007 Feb;99(2):67-86 - PubMed
  90. J Bacteriol. 1983 Aug;155(2):761-7 - PubMed
  91. Small GTPases. 2016 Oct;7(4):207-221 - PubMed
  92. Genome Biol. 2008;9(9):R137 - PubMed
  93. Cold Spring Harb Perspect Med. 2012 Dec 01;2(12):a010272 - PubMed
  94. Nat Protoc. 2016 Aug;11(8):1444-54 - PubMed
  95. Immunity. 2013 Sep 19;39(3):454-69 - PubMed
  96. Nat Rev Genet. 2019 Apr;20(4):207-220 - PubMed
  97. Nat Immunol. 2016 Jan;17(1):26-33 - PubMed
  98. Science. 2005 Sep 9;309(5741):1739-41 - PubMed
  99. Mol Cell. 2010 May 28;38(4):576-89 - PubMed
  100. Nature. 2009 May 7;459(7243):108-12 - PubMed
  101. Nat Rev Mol Cell Biol. 2016 Aug;17(8):496-510 - PubMed
  102. Nucleic Acids Res. 2009 Jan;37(1):1-13 - PubMed
  103. Bioinformatics. 2013 Jan 1;29(1):15-21 - PubMed
  104. Nucleic Acids Res. 2019 Jan 8;47(D1):D853-D858 - PubMed
  105. Sci Rep. 2019 Jun 27;9(1):9354 - PubMed
  106. Genes Dev. 2014 Mar 15;28(6):533-47 - PubMed
  107. Microbiol Spectr. 2019 Mar;7(2): - PubMed
  108. Trends Cell Biol. 2005 Mar;15(3):163-71 - PubMed
  109. Bioessays. 2002 Apr;24(4):362-70 - PubMed
  110. Curr Protoc Microbiol. 2016 Feb 08;40:1E.10.1-1E.10.21 - PubMed
  111. Dev Cell. 2014 Sep 8;30(5):569-84 - PubMed
  112. Annu Rev Microbiol. 2005;59:69-89 - PubMed
  113. Proc Natl Acad Sci U S A. 2019 Apr 2;116(14):6938-6943 - PubMed
  114. Mol Cell Biol. 1992 Jul;12(7):3138-48 - PubMed
  115. Nat Rev Microbiol. 2011 Jun 16;9(7):487-98 - PubMed
  116. Nat Cell Biol. 2020 Apr;22(4):498-511 - PubMed
  117. J Cell Sci. 2007 Jan 1;120(Pt 1):86-100 - PubMed
  118. Bioinformatics. 2009 Aug 15;25(16):2078-9 - PubMed
  119. Int J Cancer. 1999 May 31;81(5):682-7 - PubMed
  120. Curr Opin Virol. 2015 Jun;12:38-46 - PubMed
  121. Infect Immun. 1997 Nov;65(11):4813-21 - PubMed
  122. J Leukoc Biol. 2014 Mar;95(3):389-98 - PubMed
  123. Nat Immunol. 2017 Oct;18(10):1104-1116 - PubMed
  124. Bioinformatics. 2010 Mar 15;26(6):841-2 - PubMed
  125. Immunity. 2014 Sep 18;41(3):440-450 - PubMed
  126. Nat Rev Immunol. 2016 Jul;16(7):407-20 - PubMed
  127. PLoS Pathog. 2012;8(10):e1002978 - PubMed
  128. BMC Biol. 2018 Mar 6;16(1):29 - PubMed
  129. Oncogenesis. 2020 Sep 30;9(9):86 - PubMed
  130. Brief Bioinform. 2013 Mar;14(2):178-92 - PubMed
  131. Exp Cell Res. 2007 Oct 15;313(17):3673-9 - PubMed
  132. Nat Struct Mol Biol. 2016 Apr;23(4):349-57 - PubMed
  133. Curr Biol. 2006 Jan 10;16(1):35-46 - PubMed
  134. Annu Rev Immunol. 2020 Apr 26;38:289-313 - PubMed
  135. Blood. 2009 Jan 8;113(2):317-27 - PubMed
  136. PLoS Pathog. 2018 Feb 1;14(2):e1006858 - PubMed
  137. Cell Host Microbe. 2016 Sep 14;20(3):296-306 - PubMed

Publication Types