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Häger SC, Dias C, Sønder SL, et al. Short-term transcriptomic response to plasma membrane injury. Sci Rep. 2021;11(1):19141doi: 10.1038/s41598-021-98420-y.
Häger, S. C., Dias, C., Sønder, S. L., Olsen, A. V., da Piedade, I., Heitmann, A. S. B., Papaleo, E., & Nylandsted, J. (2021). Short-term transcriptomic response to plasma membrane injury. Scientific reports, 11(1), 19141. https://doi.org/10.1038/s41598-021-98420-y
Häger, Swantje Christin, et al. "Short-term transcriptomic response to plasma membrane injury." Scientific reports vol. 11,1 (2021): 19141. doi: https://doi.org/10.1038/s41598-021-98420-y
Häger SC, Dias C, Sønder SL, Olsen AV, da Piedade I, Heitmann ASB, Papaleo E, Nylandsted J. Short-term transcriptomic response to plasma membrane injury. Sci Rep. 2021 Sep 27;11(1):19141. doi: 10.1038/s41598-021-98420-y. PMID: 34580330; PMCID: PMC8476590.
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Sci Rep. 2021 Sep 27;11(1):19141. doi: 10.1038/s41598-021-98420-y.

Short-term transcriptomic response to plasma membrane injury.

Scientific reports

Swantje Christin Häger, Catarina Dias, Stine Lauritzen Sønder, André Vidas Olsen, Isabelle da Piedade, Anne Sofie Busk Heitmann, Elena Papaleo, Jesper Nylandsted

Affiliations

  1. Membrane Integrity, Danish Cancer Society Research Center, Strandboulevarden 49, 2100, Copenhagen, Denmark.
  2. Computational Biology Laboratory, Center for Autophagy, Recycling and Disease, Danish Cancer Society Research Center, Strandboulevarden 49, 2100, Copenhagen, Denmark.
  3. Translational Disease Systems Biology, Faculty of Health and Medical Sciences, Novo Nordisk Foundation Center for Protein Research University of Copenhagen, Blegdamsvej 3B, 2200, Copenhagen N, Denmark.
  4. Membrane Integrity, Danish Cancer Society Research Center, Strandboulevarden 49, 2100, Copenhagen, Denmark. [email protected].
  5. Department of Cellular and Molecular Medicine, Faculty of Health Sciences, University of Copenhagen, Blegdamsvej 3C, 2200, Copenhagen N, Denmark. [email protected].

PMID: 34580330 PMCID: PMC8476590 DOI: 10.1038/s41598-021-98420-y

Abstract

Plasma membrane repair mechanisms are activated within seconds post-injury to promote rapid membrane resealing in eukaryotic cells and prevent cell death. However, less is known about the regeneration phase that follows and how cells respond to injury in the short-term. Here, we provide a genome-wide study into the mRNA expression profile of MCF-7 breast cancer cells exposed to injury by digitonin, a mild non-ionic detergent that permeabilizes the plasma membrane. We focused on the early transcriptional signature and found a time-dependent increase in the number of differentially expressed (> twofold, P < 0.05) genes (34, 114 and 236 genes at 20-, 40- and 60-min post-injury, respectively). Pathway analysis highlighted a robust and gradual three-part transcriptional response: (1) prompt activation of immediate-early response genes, (2) activation of specific MAPK cascades and (3) induction of inflammatory and immune pathways. Therefore, plasma membrane injury triggers a rapid and strong stress and immunogenic response. Our meta-analysis suggests that this is a conserved transcriptome response to plasma membrane injury across different cell and injury types. Taken together, our study shows that injury has profound effects on the transcriptome of wounded cells in the regeneration phase (subsequent to membrane resealing), which is likely to influence cellular status and has been previously overlooked.

© 2021. The Author(s).

References

  1. Nat Commun. 2017 Nov 20;8(1):1623 - PubMed
  2. Physiol Rev. 2015 Oct;95(4):1205-40 - PubMed
  3. Int Rev Cytol. 2006;255:133-76 - PubMed
  4. Cancers (Basel). 2019 Jul 23;11(7): - PubMed
  5. Mol Biol Cell. 1999 Apr;10(4):1247-57 - PubMed
  6. Curr Signal Transduct Ther. 2011;6(3):428-440 - PubMed
  7. J Neurotrauma. 2003 Oct;20(10):1039-49 - PubMed
  8. BMC Genomics. 2016 Oct 6;17(1):781 - PubMed
  9. Mol Cell Biol. 1998 Jul;18(7):3699-707 - PubMed
  10. Adv Biol Regul. 2016 Sep;62:37-49 - PubMed
  11. Cell Discov. 2021 Jan 19;7(1):4 - PubMed
  12. Br J Cancer. 2008 Jan 29;98(2):426-33 - PubMed
  13. Ann Dermatol. 2018 Feb;30(1):54-63 - PubMed
  14. J Cell Physiol. 2018 Apr;233(4):3615-3628 - PubMed
  15. J Neurosci. 2010 Nov 24;30(47):15790-800 - PubMed
  16. J Immunol. 2000 May 1;164(9):4465-70 - PubMed
  17. PLoS One. 2017 Jul 14;12(7):e0179762 - PubMed
  18. Cell Commun Signal. 2016 Jul 28;14(1):14 - PubMed
  19. Biochim Biophys Acta. 2005 Aug 15;1745(1):29-37 - PubMed
  20. J Clin Invest. 2012 Jun;122(6):2092-103 - PubMed
  21. Nat Rev Genet. 2008 Mar;9(3):165-78 - PubMed
  22. Int J Cancer. 2000 Mar 20;89(2):177-86 - PubMed
  23. Heart Vessels. 1997;12(3):128-35 - PubMed
  24. Cells. 2020 Aug 19;9(9): - PubMed
  25. Curr Pharm Des. 2012;18(30):4725-46 - PubMed
  26. J Med Chem. 2014 Aug 28;57(16):6930-48 - PubMed
  27. PLoS One. 2012;7(11):e50071 - PubMed
  28. Biochem Pharmacol. 2011 Mar 15;81(6):703-12 - PubMed
  29. Genes Cancer. 2011 Sep;2(9):900-9 - PubMed
  30. Proc Natl Acad Sci U S A. 2019 May 7;116(19):9453-9462 - PubMed
  31. Nat Commun. 2014 May 08;5:3795 - PubMed
  32. Proc Am Thorac Soc. 2005;2(4):386-90; discussion 394-5 - PubMed
  33. Biochim Biophys Acta. 2015 Sep;1853(9):2045-54 - PubMed
  34. Trends Cell Biol. 2014 Dec;24(12):734-42 - PubMed
  35. Bioelectrochemistry. 2007 May;70(2):363-8 - PubMed
  36. PLoS One. 2012;7(2):e31574 - PubMed
  37. Mol Syst Biol. 2017 May 3;13(5):928 - PubMed
  38. J Immunol. 2008 Mar 1;180(5):3520-34 - PubMed
  39. Mol Biol Cell. 2003 Jan;14(1):93-106 - PubMed
  40. Elife. 2016 Dec 06;5: - PubMed
  41. Crit Care Med. 2000 Apr;28(4 Suppl):N67-77 - PubMed
  42. Bioinformatics. 2014 Feb 15;30(4):523-30 - PubMed
  43. Sci Rep. 2018 Mar 16;8(1):4733 - PubMed
  44. Proc Natl Acad Sci U S A. 2004 Feb 24;101(8):2434-9 - PubMed
  45. Mol Cell Biol. 1998 May;18(5):2659-67 - PubMed
  46. BMC Bioinformatics. 2014 Mar 29;15:91 - PubMed
  47. J Cell Sci. 2004 Dec 1;117(Pt 25):5965-73 - PubMed
  48. Biochem Biophys Res Commun. 1998 Dec 30;253(3):743-9 - PubMed
  49. Biochem Pharmacol. 2007 Feb 15;73(4):481-90 - PubMed
  50. Cell Mol Life Sci. 2019 Apr;76(7):1319-1339 - PubMed
  51. Nat Rev Immunol. 2013 Sep;13(9):679-92 - PubMed
  52. Cells. 2020 Apr 21;9(4): - PubMed
  53. Biol Chem. 2016 Oct 1;397(10):961-9 - PubMed
  54. Neuron. 2012 Aug 23;75(4):633-47 - PubMed
  55. Nucleic Acids Res. 2020 Jan 8;48(D1):D498-D503 - PubMed
  56. J Biol Chem. 2004 Oct 22;279(43):44996-5003 - PubMed
  57. Nucleic Acids Res. 2021 Jan 8;49(D1):D545-D551 - PubMed
  58. Biophys J. 1993 Jun;64(6):1789-800 - PubMed
  59. Genomics Proteomics Bioinformatics. 2014 Oct;12(5):210-20 - PubMed
  60. Sci Rep. 2019 Apr 30;9(1):6726 - PubMed
  61. Cell Signal. 2010 Jun;22(6):894-9 - PubMed
  62. Bioinformatics. 2010 Jan 1;26(1):139-40 - PubMed
  63. Int J Mol Sci. 2019 Aug 03;20(15): - PubMed
  64. Exp Mol Med. 2008 Jun 30;40(3):332-8 - PubMed
  65. Nat Cell Biol. 2002 May;4(5):E131-6 - PubMed
  66. Cancers (Basel). 2014 Apr 16;6(2):897-925 - PubMed
  67. Semin Cell Dev Biol. 2015 Sep;45:18-23 - PubMed
  68. PLoS One. 2014 Oct 20;9(10):e109378 - PubMed
  69. Am J Physiol Lung Cell Mol Physiol. 2007 Dec;293(6):L1377-84 - PubMed
  70. Commun Integr Biol. 2019 Oct 13;12(1):162-165 - PubMed
  71. J Dent Res. 2010 Mar;89(3):219-29 - PubMed
  72. Protein Sci. 2019 Nov;28(11):1947-1951 - PubMed
  73. Genes Dev. 2006 Jan 1;20(1):101-12 - PubMed
  74. Biochim Biophys Acta. 2015 Jun;1851(6):882-97 - PubMed
  75. Environ Health Perspect. 1990 Mar;84:107-11 - PubMed
  76. Oncol Lett. 2013 Jan;5(1):107-112 - PubMed
  77. Biophys Rev. 2020 Feb;12(1):135-142 - PubMed
  78. Front Immunol. 2018 Jan 29;9:80 - PubMed
  79. Cell Rep. 2017 Sep 12;20(11):2719-2734 - PubMed
  80. Arch Phys Med Rehabil. 2007 May;88(5):617-25 - PubMed
  81. Am J Respir Cell Mol Biol. 1999 Apr;20(4):751-8 - PubMed
  82. Genome Biol. 2008;9(11):R166 - PubMed
  83. Cold Spring Harb Perspect Biol. 2009 Dec;1(6):a001651 - PubMed
  84. Nucleic Acids Res. 2000 Jan 1;28(1):27-30 - PubMed
  85. Oncogene. 2001 Apr 30;20(19):2378-89 - PubMed
  86. Curr Biol. 1999 Jun 3;9(11):579-87 - PubMed
  87. Cell. 2000 Oct 13;103(2):239-52 - PubMed
  88. Annu Rev Genomics Hum Genet. 2015;16:281-308 - PubMed
  89. Mol Biosyst. 2016 Feb;12(2):477-9 - PubMed
  90. Mol Med Today. 1999 Oct;5(10):439-47 - PubMed
  91. JAKSTAT. 2013 Jan 1;2(1):e23820 - PubMed
  92. Adv Exp Med Biol. 2016;941:21-29 - PubMed
  93. Front Immunol. 2018 Apr 09;9:613 - PubMed

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