Eukaryotic response to hypothermia in relation to integrated stress responses.

Naki A Adjirackor, Katie E Harvey, Simon C Harvey
Author Information
  1. Naki A Adjirackor: School of Human and Life Sciences, Canterbury Christ Church University, Canterbury, CT1 1QU, UK. n.adjirackor247@canterbury.ac.uk. ORCID
  2. Katie E Harvey: School of Human and Life Sciences, Canterbury Christ Church University, Canterbury, CT1 1QU, UK.
  3. Simon C Harvey: School of Human and Life Sciences, Canterbury Christ Church University, Canterbury, CT1 1QU, UK.

Abstract

Eukaryotic cells respond to hypothermic stress through a series of regulatory mechanisms that preserve energy resources and prolong cell survival. These mechanisms include alterations in gene expression, attenuated global protein synthesis and changes in the lipid composition of the phospholipid bilayer. Cellular responses to hyperthermia, hypoxia, nutrient deprivation and oxidative stress have been comprehensively investigated, but studies of the cellular response to cold stress are more limited. Responses to cold stress are however of great importance both in the wild, where exposure to low and fluctuating environmental temperatures is common, and in medical and biotechnology settings where cells and tissues are frequently exposed to hypothermic stress and cryopreservation. This means that it is vitally important to understand how cells are impacted by low temperatures and by the decreases and subsequent increases in temperature associated with cold stress. Here, we review the ways in which eukaryotic cells respond to hypothermic stress and how these compare to the well-described and highly integrated stress response systems that govern the cellular response to other types of stress.

Keywords

References

  1. Mol Cell. 2010 Oct 22;40(2):294-309 [PMID: 20965423]
  2. Mediators Inflamm. 2012;2012:762840 [PMID: 22481864]
  3. J Cell Biol. 1985 Oct;101(4):1198-211 [PMID: 3900086]
  4. PLoS One. 2016 Sep 14;11(9):e0162766 [PMID: 27627766]
  5. Gene. 1997 Dec 19;204(1-2):115-20 [PMID: 9434172]
  6. Mol Cell. 2012 Jul 27;47(2):242-52 [PMID: 22727621]
  7. J Biol Chem. 2004 Jun 11;279(24):25164-71 [PMID: 15066988]
  8. J Cell Biol. 1999 Dec 27;147(7):1431-42 [PMID: 10613902]
  9. J Cell Sci. 2008 Sep 15;121(Pt 18):3002-14 [PMID: 18713834]
  10. Oncogene. 2006 Oct 16;25(48):6373-83 [PMID: 17041623]
  11. J Adv Res. 2019 Nov 22;22:105-118 [PMID: 31969994]
  12. Mol Cell. 2009 Dec 25;36(6):932-41 [PMID: 20064460]
  13. Mol Biol Cell. 2012 Oct;23(19):3786-800 [PMID: 22875991]
  14. Prog Mol Biol Transl Sci. 2009;90:155-85 [PMID: 20374741]
  15. Apoptosis. 2004 Sep;9(5):635-48 [PMID: 15314292]
  16. Plant J. 2008 Nov;56(4):517-30 [PMID: 18643965]
  17. Am J Pathol. 2000 May;156(5):1685-92 [PMID: 10793079]
  18. Nat Genet. 2001 Jan;27(1):121-4 [PMID: 11138012]
  19. Biochem J. 2006 Jul 15;397(2):247-59 [PMID: 16792527]
  20. Cell Stress Chaperones. 2020 Nov;25(6):857-868 [PMID: 32307648]
  21. Physiology (Bethesda). 2006 Oct;21:362-9 [PMID: 16990457]
  22. Cell. 2013 May 23;153(5):1064-79 [PMID: 23706743]
  23. Front Neuroendocrinol. 2018 Apr;49:3-7 [PMID: 29470993]
  24. Mol Cell. 2016 Apr 7;62(1):63-78 [PMID: 27052732]
  25. Genes Dev. 2015 Nov 15;29(22):2331-6 [PMID: 26543160]
  26. Eur J Biochem. 2002 Nov;269(22):5360-8 [PMID: 12423334]
  27. Annu Rev Nutr. 2005;25:317-40 [PMID: 16011470]
  28. Dev Cell. 2006 Dec;11(6):859-71 [PMID: 17141160]
  29. Am J Physiol Cell Physiol. 2008 Oct;295(4):C849-68 [PMID: 18684987]
  30. Cell Mol Life Sci. 2018 Aug;75(16):2897-2916 [PMID: 29774376]
  31. FEBS Lett. 2008 Jan 9;582(1):90-6 [PMID: 18023282]
  32. J Virol. 2015 Mar;89(5):2575-89 [PMID: 25520508]
  33. Int J Cancer. 2007 Oct 1;121(7):1424-32 [PMID: 17551921]
  34. J Appl Physiol (1985). 2009 Feb;106(2):662-7 [PMID: 18845774]
  35. Mol Cell. 2004 Mar 26;13(6):771-81 [PMID: 15053871]
  36. Curr Mol Med. 2005 Nov;5(7):653-61 [PMID: 16305491]
  37. Plant Physiol. 1997 Nov;115(3):875-879 [PMID: 12223851]
  38. Proc Natl Acad Sci U S A. 2005 Feb 8;102(6):1865-70 [PMID: 15684048]
  39. J Natl Cancer Inst. 2000 Oct 4;92(19):1564-72 [PMID: 11018092]
  40. J Cell Biol. 2016 Nov 7;215(3):313-323 [PMID: 27821493]
  41. J Cell Biol. 2007 Oct 8;179(1):65-74 [PMID: 17908917]
  42. Proc Natl Acad Sci U S A. 2007 Dec 11;104(50):19671-8 [PMID: 18003906]
  43. Proc Natl Acad Sci U S A. 2002 Dec 10;99(25):15920-5 [PMID: 12446838]
  44. EMBO Rep. 2016 Oct;17(10):1374-1395 [PMID: 27629041]
  45. J Biol Chem. 2004 Mar 26;279(13):12220-31 [PMID: 14709557]
  46. Mol Cell Biol. 2004 Apr;24(8):3112-24 [PMID: 15060135]
  47. Reprod Fertil Dev. 2016;28(1-2):1-10 [PMID: 27062870]
  48. Science. 2016 Jan 1;351(6268):48-52 [PMID: 26678875]
  49. Cancer Res. 2014 Mar 1;74(5):1379-89 [PMID: 24408918]
  50. Cell Mol Life Sci. 2010 Jan;67(2):239-53 [PMID: 19823764]
  51. Cell Mol Life Sci. 2016 Oct;73(20):3839-59 [PMID: 27147467]
  52. Genes Dev. 2013 May 15;27(10):1115-31 [PMID: 23699409]
  53. J Biol Chem. 1998 Jun 5;273(23):14484-94 [PMID: 9603962]
  54. J Cell Biol. 2008 Nov 3;183(3):441-55 [PMID: 18981231]
  55. Curr Biol. 2013 Dec 16;23(24):2452-62 [PMID: 24291094]
  56. Eur J Biochem. 2002 Nov;269(22):5338-49 [PMID: 12423332]
  57. FEBS J. 2009 Jan;276(1):286-302 [PMID: 19054067]
  58. Eur J Biochem. 1998 Dec 1;258(2):820-30 [PMID: 9874252]
  59. J Mol Biol. 2020 Mar 27;432(7):2349-2368 [PMID: 32105731]
  60. Nat Rev Mol Cell Biol. 2013 Apr;14(4):197-210 [PMID: 23847781]
  61. EMBO J. 2001 Aug 15;20(16):4370-9 [PMID: 11500364]
  62. Apoptosis. 2012 Sep;17(9):989-97 [PMID: 22460505]
  63. Int J Cell Biol. 2010;2010:214074 [PMID: 20182529]
  64. Genes Dev. 2011 Sep 15;25(18):1895-908 [PMID: 21937710]
  65. Int J Mol Sci. 2016 Mar 02;17(3):327 [PMID: 26950115]
  66. J Bacteriol. 1998 Apr;180(8):2194-200 [PMID: 9555904]
  67. J Biol Chem. 2014 Feb 7;289(6):3352-64 [PMID: 24347168]
  68. Sci Rep. 2017 May 23;7(1):2295 [PMID: 28536481]
  69. Science. 2016 Jul 1;353(6294):aac4354 [PMID: 27365453]
  70. J Biochem. 2018 Nov 1;164(5):381-391 [PMID: 30020475]
  71. Autophagy. 2010 Oct;6(7):999-1005 [PMID: 20639698]
  72. J Clin Invest. 2002 May;109(9):1125-31 [PMID: 11994399]
  73. Mol Cell Biol. 2006 May;26(10):3955-65 [PMID: 16648488]
  74. Oxid Med Cell Longev. 2017;2017:6098107 [PMID: 29317983]
  75. Cell Rep. 2018 Aug 7;24(6):1415-1424 [PMID: 30089253]
  76. Free Radic Biol Med. 2013 Sep;64:20-30 [PMID: 23712003]
  77. Cryobiology. 2003 Jun;46(3):230-7 [PMID: 12818212]
  78. Biochim Biophys Acta. 2015 Jul;1849(7):861-70 [PMID: 25482014]
  79. Biochem Biophys Res Commun. 2012 Jul 13;423(4):763-9 [PMID: 22705549]
  80. Cell. 2011 Aug 5;146(3):408-20 [PMID: 21816276]
  81. J Invest Dermatol. 1993 Aug;101(2):196-9 [PMID: 8345221]
  82. F1000Res. 2016 Aug 25;5: [PMID: 27635236]
  83. Neurobiol Dis. 2011 Aug;43(2):388-96 [PMID: 21527344]
  84. Mol Cell Biol. 2004 Nov;24(21):9508-16 [PMID: 15485918]
  85. N Engl J Med. 2007 Apr 26;356(17):1751-8 [PMID: 17460229]
  86. Biochem Soc Trans. 2002 Nov;30(Pt 6):1076-9 [PMID: 12440976]
  87. J Biol Chem. 2001 Feb 9;276(6):4365-72 [PMID: 11085986]
  88. J Cell Biol. 2005 Jun 20;169(6):871-84 [PMID: 15967811]
  89. Free Radic Biol Med. 2018 Jun;121:157-168 [PMID: 29704622]
  90. Curr Opin Cell Biol. 2017 Apr;45:72-82 [PMID: 28411448]
  91. J Appl Physiol (1985). 2002 Apr;92(4):1725-42 [PMID: 11896043]
  92. Acta Paediatr. 2007 May;96(5):617-21 [PMID: 17462054]
  93. Cell. 2014 Apr 24;157(3):624-35 [PMID: 24766808]
  94. EMBO J. 2006 Mar 8;25(5):1114-25 [PMID: 16467844]
  95. Cold Spring Harb Perspect Biol. 2016 Oct 3;8(10): [PMID: 27698029]
  96. Cell Stress Chaperones. 2004 Mar;9(1):21-8 [PMID: 15270074]
  97. Science. 1991 Aug 23;253(5022):905-9 [PMID: 1715094]
  98. Biochim Biophys Acta. 2004 Nov 3;1666(1-2):142-57 [PMID: 15519313]
  99. Cell. 2005 Nov 18;123(4):569-80 [PMID: 16286006]
  100. Proc Natl Acad Sci U S A. 2005 Jul 26;102(30):10460-5 [PMID: 16030146]
  101. Trends Ecol Evol. 2000 Apr;15(4):156-160 [PMID: 10717685]
  102. Science. 2005 Feb 18;307(5712):1098-101 [PMID: 15718470]
  103. J Biol Chem. 2007 Feb 9;282(6):3450-7 [PMID: 17158099]
  104. EMBO J. 2005 Oct 5;24(19):3470-81 [PMID: 16148948]
  105. Biochem Biophys Res Commun. 2005 Jul 8;332(3):735-42 [PMID: 15907797]
  106. FEBS Lett. 2007 Jul 31;581(19):3608-15 [PMID: 17412325]
  107. Mol Cancer Ther. 2008 Jul;7(7):1851-63 [PMID: 18606717]
  108. Mol Cell. 2010 Oct 22;40(2):253-66 [PMID: 20965420]
  109. Wiley Interdiscip Rev RNA. 2014 May-Jun;5(3):301-15 [PMID: 24375939]
  110. J Neurochem. 2007 Jun;101(5):1367-79 [PMID: 17403028]
  111. Ann Surg. 1958 Feb;147(2):264-6 [PMID: 13498651]
  112. EMBO J. 2004 Apr 21;23(8):1761-9 [PMID: 15071500]
  113. Cell Cycle. 2015;14(16):2571-7 [PMID: 26039820]
  114. Oxid Med Cell Longev. 2017;2017:1809592 [PMID: 28194255]
  115. J Biol Chem. 2009 Mar 20;284(12):8023-32 [PMID: 19150980]
  116. Genes Dev. 1998 Oct 15;12(20):3182-94 [PMID: 9784493]

MeSH Term

Animals
Cell Membrane
Eukaryota
Humans
Hypothermia
Hypoxia
Oxidative Stress
Stress, Physiological

Word Cloud

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