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Heat Acclimation, Epigenetics, and Cytoprotection Memory

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Abstract

Heat acclimation is a within‐life phenotypic adaptation to heat. Plasticity of the thermoregulatory system is crucial for the induction of heat acclimation. In the last two decades, it has become clear that heat causes adaptive shifts in gene expression which adjust the protein balance. These changes are part of the evolvement of the acclimated phenotype. The molecular‐cellular aspects of some acclimatory mechanisms that have only been explained by physiological‐effectorial mechanisms have been discovered. This review attempts to bridge the gap between the classic physiological heat acclimation profile and the molecular/cellular mechanisms underlying the evolvement of the acclimated phenotype. Heat acclimation leads to leftward and rightward shifts in temperature thresholds of heat dissipation organs and thermal injury, respectively, thereby expanding the acclimated dynamic thermoregulatory range. Interactions between ambient temperature and afferent drives from effector organs to the hypothalamic thermoregulatory center with modifications in warm/cold sensitive neuron ratio and excitability contribute to the threshold changes. The altered threshold for thermal injury is associated with progressive enhancement of inducible cytoprotective networks, including HSP70, HSF1, and HIF‐1α. These molecules are also important in acclimatory kinetics. Aspects of cross‐adaption, cross‐tolerance and interference with heat acclimation are explained using molecular‐cellular physiological interactions, with the heart, skeletal muscles, and water secretory glands as models. Lastly, the roles of epigenetic mechanisms in transcriptional regulation during induction of the acclimated phenotype, its decay, and reinduction are discussed. Posttranslational histone modifications in the promoters of hsp70 and hsp90 form part of our prototype model of heat‐acclimation‐mediated cytoprotective memory. © 2014 American Physiological Society. Compr Physiol 4:199‐230, 2014.

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Figure 1. Figure 1. Acclimation plasticity shown by changes in thermoregulatory temperature thresholds (T‐Tsh). (A) Heat acclimation expands the dynamic thermoregulatory range. T‐TshEV ‐temperature threshold for the onset of evaporative cooling. TshTI‐temperature threshold for failure of thermoregulation (Thermal Injury). (B) Heat acclimation mediates leftward shift in thresholds for evaporation and vasodilation, while the thermal injury threshold shifts to the right. Left panels: (top) T‐TshEV and water volume secreted for evaporative cooling in rats. Black lines ‐heat acclimated (AC), dashed lines ‐non acclimated (C). (Middle) Sweating threshold in humans acclimated to heat and exercise (heat/ex acc). (Bottom) Vasodilation threshold in humans acclimated to heat/ex acc. (Right panel) Thermal injury threshold in rats. Vertical arrows denote the T‐Tsh. (C) Dynamic thermoregulatory range (DTR) before and after heat acclimation in the splanchnic vascular bed [superior mesenteric artery (SMA) and portal vein (PV) blood flow (BF)]. The onset of the thermoregulatory‐induced vasomotor reflex is depicted by SMA vasoconstriction. Failure of this reflex is denoted by abrupt vasoconstriction of SMA and vasodilatation of the PV. DTR is clearly longer in the acclimated animal. Vertical arrows denote Tsh. Adapted from Horowitz/Horowitz et al, (75,78,83), Haddad et al. (57,58) Nadel et al. (149), Roberts et al. (175), with permission of FBS and the American Physiological Society.
Figure 2. Figure 2. (A) secretory activity of submaxillary salivary glands measured in heat‐stressed rats (40°C) and heat acclimating rats (34°C) in vivo and in isolated glands of similarly treated rats, stimulated with pilocarpine. “Excitability” line depicts the predicted chorda tympani firing rate required to produce the salivation observed in the intact animal. EO/AS—effector organ/autonomic signal ratio: EO/AS<1 denotes short‐term heat acclimation, and EO/AS>1 denotes long‐term heat acclimation. For further details, see text. [Redrawn, with permission, from Horowitz and Meiri (81)]. (B) changes in net contributions of autonomic and intrinsic factors to heat acclimation‐induced bradycardia during acclimation at 34°C for 1 month in the rat. The autonomic influence on heart rate (HR) was calculated as the parasympathetic minus the sympathetic influences. HR in intact animal was measured following administration of a combination of 0.1 mg/100g body weight atropine sulfate and 1 mg/100g body weight propranolol‐HCl. “Excitability correc.” line is the predicted excitability required to produce the HR measured in the intact body, despite atrial impaired/altered responsiveness to the autonomic transmitters [Redrawn from Horowitz and Meiri (90)]. Short‐term heat acclimation is characterized by accelerated excitability to overcome impaired organ responsiveness [for calculations of predicted excitability, see Refs. (81) and (90)]. C. Heat acclimation: a conceptual model. During phase 1 (STHA), accelerated autonomic discharges override impaired effector organ (EO) responsiveness. During phase 2 (LTHA), the share of peripheral adaptive features controlling homeostasis increases, thus diminishing the autonomic discharge. Central changes include decreased temperature threshold for activation of heat dissipation effectors with a concomitant increase in their sensitivity. Temperature threshold for accelerated heat production increases. Tcore ‐ core temperature. Redrawn from Horowitz 1998 (73) with permission of APS.
Figure 3. Figure 3. Thermoregulatory water secretion from the rat submaxillary gland changes during the course of heat acclimation. In the cell membrane, STHA augments the muscarinic receptors (MR3) density but increases the high affinity/low affinity receptor density ratio, reducing the IP3‐induced Ca2+ signal and secretion (displayed by Rb efflux). Upon LTHA receptor density continues to increase but the high‐affinity/low‐affinity ratio returns to control levels resulting in increased glandular output per Ca2+ signal which implies increased glandular efficiency. Adapted from Horowitz et al. Kaspler and horowitz and Kloog et al. (87,100,109) with permission of the APS.
Figure 4. Figure 4. Central‐Peripheral interactions during heat acclimation: a conceptual model. Chronic exposure to high ambient temperatures mobilizes the thermoregulatory system and impacts on core body temperature and the T‐Tsh of heat dissipation organs. At the onset of heat acclimation (STHA: a‐loop), increased autonomic excitability compensates for cellular impairments in peripheral effectors. However, the strain and the increased excitability lead to effector organ desensitization which, in turn, amplifies the afferent drives. Acclimatory homeostasis is displayed by the b‐loop. Thermoregulatory thresholds are determined by central peripheral cross‐talk. For detailed explanation see text. CSN/WSN – cold and warm sensitive neurons. Taken from Horowitz (78), with permission of FBS.
Figure 5. Figure 5. Left panel: Quantification of HSP72 levels in left ventricle of hearts from control (C) and heat‐acclimated rats (1, 2, and 30 days). Top: Semiquantitative RT‐PCR analysis of HSP72 mRNA shows stable levels in the left ventricle control (C) and heat‐acclimated rats (1, 2, and 30 days). *(0.001 > p < 0.005). Bottom: HSP protein levels in different groups of rats, normalized to a commercial HSP sample. Reprinted (with permission) from Maloyan et al. (134). Right panel: HSP70 kinetics during the course of acclimation. External environmental heat stimuli use the thermal receptor afferent pathway to the thermoregulatory loop to activate β‐adrenoreceptor sympathetic signaling and increase HSP cellular reserves and also contribute to the elevation of the heat injury temperature threshold. The process develops slowly. During STHA, the hsp transcript is elevated to produce larger HSP72 reserves when acclimatory homeostasis has been achieved. In the heat‐acclimated phenotype, constitutive elevation of HSP72 reserves and faster hsp transcriptional response (abrupt response) further delays the onset of injury (133). LTHA, long‐term heat acclimation; STHA, short‐term heat acclimation. Short thick arrows indicate RNA or protein levels; other arrows denote pathway direction. Reprinted [with permission from MSSE (89)].
Figure 6. Figure 6. The HSF1 inhibitor quercetin alters well‐established systemic adaptations that characterize the human heat‐acclimated phenotype, including lactulose excretion (marker of gut permeability) and Il‐6 and HSP70 levels (right panel). However, measurements of heart rate and the physiological strain index (left panel) suggest that acclimation persists, despite of the loss of thermotolerance as seen from increased gastrointestinal endothelial permeability (41) and attenuated heat shock response. Redrawn (with permission) from Kuennen et al. (113).
Figure 7. Figure 7. Evidence for epigenetic transcriptional regulation during induction of heat acclimation: a lesson from the heart. At the onset of heat acclimation (STHA), elevated basal body temperature and cell Ca2+ results in a significant elevation in the recruitment of MSK1 to the hsps promoters to phosphorylates histoe H3. Consequently, histone H4 is acetylated when acclimation homeostasis has achieved. HSF1 (heat shock factor 1) binds to the heat shock elements (HSE) on the promoters of the hsps genes and activates transcription/translation of the coded proteins. Adapted from Cohen et al. and Tetievsky and Horowitz (35,219) and unpublished data from Tetievsky and Horowitz.
Figure 8. Figure 8. Conceptual model of the kinetics of mitochondrial acclimation to heat. Initial rapid adaptation of mitochondrial membrane integrity is followed by long‐term progressive changes in respiratory chain complex activity, required for the contribution of the mitochondria to heat acclimation. This model is based on data from Assayag et al. (6,7). PTM, posttranslational modifications (phosphorylation). HACT‐heat acclimation mediated cross‐tolerance. Reprinted from Assayag et al. (with permission) (7).
Figure 9. Figure 9. (A) Individual and group mean changes in plasma volume during 10 days of heat acclimation combined with exercise training, measured before each exercise session. (B) Changes in plasma volume versus changes in albumin fraction (redrawn from (203). (C) Percent changes in heart rates expressed as a function of % changes in plasma volume. The first day heat exposure values were taken as control values. Reprinted [A, C, and redrawn B, with permission) from Senay et al. (203).
Figure 10. Figure 10. Effects of progressively increasing temperature and heart beat rates on pressure generation in isolated perfused hearts from normothermic and heat acclimated rats. Reprinted (with permission) from Cohen et al.(34).
Figure 11. Figure 11. Representative echographic images of the instantaneous dimensional changes by Mmode in control (C), heat acclimated (AC), exercise training under normothermic conditions (EX), and combined AC and EX (EXAC) groups. (A) interventricular septum thickness at diastole; (B) left ventricular end‐diastolic diameter; (C) left ventricular end systolic diameter; and (D) left ventricle posterior wall thickness at diastole. Reprinted from Kodesh et al. (with permission) (111).
Figure 12. Figure 12. Isometric force generation in the soleus muscle stimulated using gradually increasing frequencies. The EXAC muscles generated significantly greater force than all other groups. Insert: Power drop during progressively increased stimulation frequency after peak tetanic contractility was achieved, (% of peak power). The two acclimated groups (sedentary and exercising) demonstrated better power preservation. C‐ normothermic control, ACC‐heat acclimated under sedentary conditions, EX‐exercise training, EXAC. Reprinted from Kodesh and Horowitz (with permission) (110).
Figure 13. Figure 13. Expression level of (i) Ecitation‐contraction coupling and Ca2 regulatory genes in the heart and (ii) energy metabolism associated genes in the soleus. No other differences in functional categories expression levels were detected between the groups. The Venn diagrams show the number of stress specific genes (encircled) in each group. AC‐heat acclimated under sedentary conditions, EX‐exercise training—treadmill, EXAC‐combined heat acclimation, and exercise training. Adapted (with permission) from (94,95)
Figure 14. Figure 14. Conceptual model of the evolution of heat acclimatio memory with cross‐talk between the transcriptional activation of hsp70 and hsp90 genes. Chromatin panel (top) presents posttranslational H3 and H4 modifications and transcription factor binding, and the protein panel (bottom) presents the encoded proteins. Top and bottom panels represent the treatment protocol and cytoprotection, respectively. At the onset of heat acclimation (AC2d), histone H3 phosphorylation switches on HSF‐1 binding to the HSE with subsequent histone H4 acetylation at the HSE of both hsp70 and hsp90 genes. The acetylation persists throughout DeAC and ReAC, resulting in constitutive HSF‐1 binding to the hsp70 promoter throughout AC2d, AC (heat acclimation for 30d), DeAC, and ReAC. Concomitantly, HSF‐1 binding to hsp90 and the encoded protein are absent in DeAC. The constitutively elevated histone H4 acetylation at the hsp90 gene promoter, however, may facilitate the rapid resumption of HSF‐1 binding, hsp90 translation, and the formation of a cytoprotective milieu upon ReAC. This is displayed by constitutively higher HSP‐70 reserves throughout AC‐ReAC whereas HSP‐90 was only elevated in AC and ReAC hearts. Cytoprotection during these phases is demonstrated by reduced cardiac infarct size. Notably, while H3 phosphorylation is ambient temperature dependent, H4 is ambient temperature independent. H3, histone H3; H4, histone H4; P, phosphorylation; AC, acetylation; HSE‐heat shock element, Ta, ambient temperature effect. Reprinted (with permission) from Tetievsky and Horowitz (219).


Figure 1. Acclimation plasticity shown by changes in thermoregulatory temperature thresholds (T‐Tsh). (A) Heat acclimation expands the dynamic thermoregulatory range. T‐TshEV ‐temperature threshold for the onset of evaporative cooling. TshTI‐temperature threshold for failure of thermoregulation (Thermal Injury). (B) Heat acclimation mediates leftward shift in thresholds for evaporation and vasodilation, while the thermal injury threshold shifts to the right. Left panels: (top) T‐TshEV and water volume secreted for evaporative cooling in rats. Black lines ‐heat acclimated (AC), dashed lines ‐non acclimated (C). (Middle) Sweating threshold in humans acclimated to heat and exercise (heat/ex acc). (Bottom) Vasodilation threshold in humans acclimated to heat/ex acc. (Right panel) Thermal injury threshold in rats. Vertical arrows denote the T‐Tsh. (C) Dynamic thermoregulatory range (DTR) before and after heat acclimation in the splanchnic vascular bed [superior mesenteric artery (SMA) and portal vein (PV) blood flow (BF)]. The onset of the thermoregulatory‐induced vasomotor reflex is depicted by SMA vasoconstriction. Failure of this reflex is denoted by abrupt vasoconstriction of SMA and vasodilatation of the PV. DTR is clearly longer in the acclimated animal. Vertical arrows denote Tsh. Adapted from Horowitz/Horowitz et al, (75,78,83), Haddad et al. (57,58) Nadel et al. (149), Roberts et al. (175), with permission of FBS and the American Physiological Society.


Figure 2. (A) secretory activity of submaxillary salivary glands measured in heat‐stressed rats (40°C) and heat acclimating rats (34°C) in vivo and in isolated glands of similarly treated rats, stimulated with pilocarpine. “Excitability” line depicts the predicted chorda tympani firing rate required to produce the salivation observed in the intact animal. EO/AS—effector organ/autonomic signal ratio: EO/AS<1 denotes short‐term heat acclimation, and EO/AS>1 denotes long‐term heat acclimation. For further details, see text. [Redrawn, with permission, from Horowitz and Meiri (81)]. (B) changes in net contributions of autonomic and intrinsic factors to heat acclimation‐induced bradycardia during acclimation at 34°C for 1 month in the rat. The autonomic influence on heart rate (HR) was calculated as the parasympathetic minus the sympathetic influences. HR in intact animal was measured following administration of a combination of 0.1 mg/100g body weight atropine sulfate and 1 mg/100g body weight propranolol‐HCl. “Excitability correc.” line is the predicted excitability required to produce the HR measured in the intact body, despite atrial impaired/altered responsiveness to the autonomic transmitters [Redrawn from Horowitz and Meiri (90)]. Short‐term heat acclimation is characterized by accelerated excitability to overcome impaired organ responsiveness [for calculations of predicted excitability, see Refs. (81) and (90)]. C. Heat acclimation: a conceptual model. During phase 1 (STHA), accelerated autonomic discharges override impaired effector organ (EO) responsiveness. During phase 2 (LTHA), the share of peripheral adaptive features controlling homeostasis increases, thus diminishing the autonomic discharge. Central changes include decreased temperature threshold for activation of heat dissipation effectors with a concomitant increase in their sensitivity. Temperature threshold for accelerated heat production increases. Tcore ‐ core temperature. Redrawn from Horowitz 1998 (73) with permission of APS.


Figure 3. Thermoregulatory water secretion from the rat submaxillary gland changes during the course of heat acclimation. In the cell membrane, STHA augments the muscarinic receptors (MR3) density but increases the high affinity/low affinity receptor density ratio, reducing the IP3‐induced Ca2+ signal and secretion (displayed by Rb efflux). Upon LTHA receptor density continues to increase but the high‐affinity/low‐affinity ratio returns to control levels resulting in increased glandular output per Ca2+ signal which implies increased glandular efficiency. Adapted from Horowitz et al. Kaspler and horowitz and Kloog et al. (87,100,109) with permission of the APS.


Figure 4. Central‐Peripheral interactions during heat acclimation: a conceptual model. Chronic exposure to high ambient temperatures mobilizes the thermoregulatory system and impacts on core body temperature and the T‐Tsh of heat dissipation organs. At the onset of heat acclimation (STHA: a‐loop), increased autonomic excitability compensates for cellular impairments in peripheral effectors. However, the strain and the increased excitability lead to effector organ desensitization which, in turn, amplifies the afferent drives. Acclimatory homeostasis is displayed by the b‐loop. Thermoregulatory thresholds are determined by central peripheral cross‐talk. For detailed explanation see text. CSN/WSN – cold and warm sensitive neurons. Taken from Horowitz (78), with permission of FBS.


Figure 5. Left panel: Quantification of HSP72 levels in left ventricle of hearts from control (C) and heat‐acclimated rats (1, 2, and 30 days). Top: Semiquantitative RT‐PCR analysis of HSP72 mRNA shows stable levels in the left ventricle control (C) and heat‐acclimated rats (1, 2, and 30 days). *(0.001 > p < 0.005). Bottom: HSP protein levels in different groups of rats, normalized to a commercial HSP sample. Reprinted (with permission) from Maloyan et al. (134). Right panel: HSP70 kinetics during the course of acclimation. External environmental heat stimuli use the thermal receptor afferent pathway to the thermoregulatory loop to activate β‐adrenoreceptor sympathetic signaling and increase HSP cellular reserves and also contribute to the elevation of the heat injury temperature threshold. The process develops slowly. During STHA, the hsp transcript is elevated to produce larger HSP72 reserves when acclimatory homeostasis has been achieved. In the heat‐acclimated phenotype, constitutive elevation of HSP72 reserves and faster hsp transcriptional response (abrupt response) further delays the onset of injury (133). LTHA, long‐term heat acclimation; STHA, short‐term heat acclimation. Short thick arrows indicate RNA or protein levels; other arrows denote pathway direction. Reprinted [with permission from MSSE (89)].


Figure 6. The HSF1 inhibitor quercetin alters well‐established systemic adaptations that characterize the human heat‐acclimated phenotype, including lactulose excretion (marker of gut permeability) and Il‐6 and HSP70 levels (right panel). However, measurements of heart rate and the physiological strain index (left panel) suggest that acclimation persists, despite of the loss of thermotolerance as seen from increased gastrointestinal endothelial permeability (41) and attenuated heat shock response. Redrawn (with permission) from Kuennen et al. (113).


Figure 7. Evidence for epigenetic transcriptional regulation during induction of heat acclimation: a lesson from the heart. At the onset of heat acclimation (STHA), elevated basal body temperature and cell Ca2+ results in a significant elevation in the recruitment of MSK1 to the hsps promoters to phosphorylates histoe H3. Consequently, histone H4 is acetylated when acclimation homeostasis has achieved. HSF1 (heat shock factor 1) binds to the heat shock elements (HSE) on the promoters of the hsps genes and activates transcription/translation of the coded proteins. Adapted from Cohen et al. and Tetievsky and Horowitz (35,219) and unpublished data from Tetievsky and Horowitz.


Figure 8. Conceptual model of the kinetics of mitochondrial acclimation to heat. Initial rapid adaptation of mitochondrial membrane integrity is followed by long‐term progressive changes in respiratory chain complex activity, required for the contribution of the mitochondria to heat acclimation. This model is based on data from Assayag et al. (6,7). PTM, posttranslational modifications (phosphorylation). HACT‐heat acclimation mediated cross‐tolerance. Reprinted from Assayag et al. (with permission) (7).


Figure 9. (A) Individual and group mean changes in plasma volume during 10 days of heat acclimation combined with exercise training, measured before each exercise session. (B) Changes in plasma volume versus changes in albumin fraction (redrawn from (203). (C) Percent changes in heart rates expressed as a function of % changes in plasma volume. The first day heat exposure values were taken as control values. Reprinted [A, C, and redrawn B, with permission) from Senay et al. (203).


Figure 10. Effects of progressively increasing temperature and heart beat rates on pressure generation in isolated perfused hearts from normothermic and heat acclimated rats. Reprinted (with permission) from Cohen et al.(34).


Figure 11. Representative echographic images of the instantaneous dimensional changes by Mmode in control (C), heat acclimated (AC), exercise training under normothermic conditions (EX), and combined AC and EX (EXAC) groups. (A) interventricular septum thickness at diastole; (B) left ventricular end‐diastolic diameter; (C) left ventricular end systolic diameter; and (D) left ventricle posterior wall thickness at diastole. Reprinted from Kodesh et al. (with permission) (111).


Figure 12. Isometric force generation in the soleus muscle stimulated using gradually increasing frequencies. The EXAC muscles generated significantly greater force than all other groups. Insert: Power drop during progressively increased stimulation frequency after peak tetanic contractility was achieved, (% of peak power). The two acclimated groups (sedentary and exercising) demonstrated better power preservation. C‐ normothermic control, ACC‐heat acclimated under sedentary conditions, EX‐exercise training, EXAC. Reprinted from Kodesh and Horowitz (with permission) (110).


Figure 13. Expression level of (i) Ecitation‐contraction coupling and Ca2 regulatory genes in the heart and (ii) energy metabolism associated genes in the soleus. No other differences in functional categories expression levels were detected between the groups. The Venn diagrams show the number of stress specific genes (encircled) in each group. AC‐heat acclimated under sedentary conditions, EX‐exercise training—treadmill, EXAC‐combined heat acclimation, and exercise training. Adapted (with permission) from (94,95)


Figure 14. Conceptual model of the evolution of heat acclimatio memory with cross‐talk between the transcriptional activation of hsp70 and hsp90 genes. Chromatin panel (top) presents posttranslational H3 and H4 modifications and transcription factor binding, and the protein panel (bottom) presents the encoded proteins. Top and bottom panels represent the treatment protocol and cytoprotection, respectively. At the onset of heat acclimation (AC2d), histone H3 phosphorylation switches on HSF‐1 binding to the HSE with subsequent histone H4 acetylation at the HSE of both hsp70 and hsp90 genes. The acetylation persists throughout DeAC and ReAC, resulting in constitutive HSF‐1 binding to the hsp70 promoter throughout AC2d, AC (heat acclimation for 30d), DeAC, and ReAC. Concomitantly, HSF‐1 binding to hsp90 and the encoded protein are absent in DeAC. The constitutively elevated histone H4 acetylation at the hsp90 gene promoter, however, may facilitate the rapid resumption of HSF‐1 binding, hsp90 translation, and the formation of a cytoprotective milieu upon ReAC. This is displayed by constitutively higher HSP‐70 reserves throughout AC‐ReAC whereas HSP‐90 was only elevated in AC and ReAC hearts. Cytoprotection during these phases is demonstrated by reduced cardiac infarct size. Notably, while H3 phosphorylation is ambient temperature dependent, H4 is ambient temperature independent. H3, histone H3; H4, histone H4; P, phosphorylation; AC, acetylation; HSE‐heat shock element, Ta, ambient temperature effect. Reprinted (with permission) from Tetievsky and Horowitz (219).
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Michal Horowitz. Heat Acclimation, Epigenetics, and Cytoprotection Memory. Compr Physiol 2014, 4: 199-230. doi: 10.1002/cphy.c130025