Eukaryotic response to hypothermia in relation to integrated stress responses

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Eukaryotic response to hypothermia in relation to integrated stress responses Naki A. Adjirackor 1

&

Katie E. Harvey 1 & Simon C. Harvey 1

Received: 1 April 2020 / Revised: 29 June 2020 / Accepted: 1 July 2020 # Cell Stress Society International 2020

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 Eukaryotic cells . Hypothermia . Cold stress response . Protein synthesis . mTOR

Abbreviations 4E-BP eIF4E binding protein AMPK AMP-activated protein kinase CIRP Cold-inducible RNA-binding protein CSP Cold shock protein EIF Eukaryotic initiation factor ER Endoplasmic reticulum GCN2 General Control Non-Derepressible 2 HIF Hypoxia-inducible factor HRE Hypoxia-responsive elements HRI Heme-regulated inhibitor HSE Heat shock element HSF Heat shock factor HSP Heat shock protein ILK Integrin-linked kinase mRNPs Ribonucleoprotein particles mTOR Mechanistic target of rapamycin PERK PKR-like endoplasmic reticulum kinase * Naki A. Adjirackor [email protected] 1

School of Human and Life Sciences, Canterbury Christ Church University, Canterbury CT1 1QU, UK

PIKK PIP2 PIP3 raptor RBM3 RBP rictor ROS S6K SCD SG SREBPs

PI3K-related protein kinase family Phosphatidylinositol (4,5)-biphosphate Phosphatidylinositol (3,4,5)-triphosphate Regulatory-associated protein of mTOR RNA-binding motif protein 3 RNA-binding protein Rapamycin-insensitive companion of mTOR Reactive oxygen species Ribosomal S6 kinase Stearoyl-CoA desaturase Stress granule Sterol regulatory element-binding proteins

Introduction The definition of ‘stress’ can be ambiguous. It is often used to describe the environmental perturbations that interrupt homeostasis in higher organisms, but in single cells it refers to changes in the internal or external environment that compromise cell survival. This means that organisms experience stress at various magnitudes depending on their biological fo