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Acetyl salicylic acid protected against heat stress damage in chicken myocardial cells and may associate with induced Hsp27 expression

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Cell Stress and Chaperones Aims and scope

Abstract

We investigated whether acetyl salicylic acid (ASA) protects chicken myocardial cells from heat stress-mediated damage in vivo and whether the induction of Hsp27 expression is connected with this function. Pathological changes, damage-related enzyme levels, and Hsp27 expression were studied in chickens following heat stress (40 ± 1 °C for 0, 1, 2, 3, 5, 7, 10, 15, or 24 h, respectively) with or without ASA administration (1 mg/kg BW, 2 h prior). Appearance of pathological lesions such as degenerations and karyopyknosis as well as the myocardial damage-related enzyme activation indicated that heat stress causes considerable injury to the myocardial cells in vivo. Myocardial cell injury was most serious in chickens exposed to heat stress without prior ASA administration; meanwhile, ASA pretreatment acted protective function against high temperature-induced injury. Hsp27 expression was induced under all experimental conditions but was one-fold higher in the ASA-pretreated animals (0.3138 ± 0.0340 ng/mL) than in untreated animals (0.1437 ± 0.0476 ng/mL) 1 h after heat stress exposure, and such an increase was sustained over the length of the experiment. Our findings indicate that pretreatment with ASA protects chicken myocardial cells from acute heat stress in vivo with almost no obvious side effects, and this protection may involve an enhancement of Hsp27 expression. However, the detailed mechanisms underlying this effect require further investigation.

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References

  • Abravaya K, Phillips B, Morimoto RI (1991) Attenuation of the heat shock response in HeLa cells is mediated by the release of bound heat shock transcription factor and is modulated by changes in growth and in heat shock temperatures. Genes Dev 5:2117–2127

    Article  CAS  PubMed  Google Scholar 

  • Acunzo J, Katsogiannou M, Rocchi P (2012) Small heat shock proteins HSP27 (HspB1), alphaB-crystallin (HspB5) and HSP22 (HspB8) as regulators of cell death. Int J Biochem Cell Biol 44:1622–1631. doi:10.1016/j.biocel.2012.04.002

    Article  CAS  PubMed  Google Scholar 

  • Acunzo J, Andrieu C, Baylot V, So A, Rocchi P (2014) Hsp27 as a therapeutic target in cancers. Curr Drug Targets 15:423–431

    Article  CAS  PubMed  Google Scholar 

  • Amani M, Jeddi S, Ahmadiasl N, Usefzade N, Zaman J (2013) Effect of HEMADO on level of CK-MB and LDH enzymes after ischemia/reperfusion injury in isolated rat heart. Bioimpacts : BI 3:101–104. doi:10.5681/bi.2013.003

    PubMed Central  PubMed  Google Scholar 

  • Amberger A, Hala M, Saurwein-Teissl M, Metzler B, Grubeck-Loebenstein B, Xu Q, Wick G (1999) Suppressive effects of anti-inflammatory agents on human endothelial cell activation and induction of heat shock proteins. Mol Med 5:117–128

    CAS  PubMed Central  PubMed  Google Scholar 

  • Arrigo AP, Landry J (1994) Expression and function of the low-molecular-weight heat shock proteins. In: Morimoto RI, Tissieres A, Georgopoulos C (eds) The biology of heat shock proteins and molecular chaperones, p 335–373

  • Arrigo AP, Suhan JP, Welch WJ (1988) Dynamic changes in the structure and intracellular locale of the mammalian low-molecular-weight heat shock protein. Mol Cell Biol 8:5059–5071

    CAS  PubMed Central  PubMed  Google Scholar 

  • Batulan Z et al (2003) High threshold for induction of the stress response in motor neurons is associated with failure to activate HSF1. J Neurosci Off J Soc Neurosci 23:5789–5798

    CAS  Google Scholar 

  • Benn SC et al (2002) Hsp27 upregulation and phosphorylation is required for injured sensory and motor neuron survival. Neuron 36:45–56

    Article  CAS  PubMed  Google Scholar 

  • Bukau B, Horwich AL (1998) The Hsp70 and Hsp60 chaperone machines. Cell 92:351–366

    Article  CAS  PubMed  Google Scholar 

  • Chen TH, Yang YC, Wang JC, Wang JJ (2013) Curcumin treatment protects against renal ischemia and reperfusion injury-induced cardiac dysfunction and myocardial injury. Transplant Proc 45:3546–3549. doi:10.1016/j.transproceed.2013.09.006

    Article  CAS  PubMed  Google Scholar 

  • Chon H, Lee S, Yoon SY, Lee EK, Chang SI, Choo J (2013) SERS-based competitive immunoassay of troponin I and CK-MB markers for early diagnosis of acute myocardial infarction. Chem Commun (Camb). doi:10.1039/c3cc47850e

    Google Scholar 

  • Cotto JJ, Kline M, Morimoto RI (1996) Activation of heat shock factor 1 DNA binding precedes stress-induced serine phosphorylation. Evidence for a multistep pathway of regulation. J Biol Chem 271:3355–3358

    Article  CAS  PubMed  Google Scholar 

  • de Graauw M, Tijdens I, Cramer R, Corless S, Timms JF, van de Water B (2005) Heat shock protein 27 is the major differentially phosphorylated protein involved in renal epithelial cellular stress response and controls focal adhesion organization and apoptosis. J Biol Chem 280:29885–29898. doi:10.1074/jbc.M412708200

    Article  PubMed  Google Scholar 

  • Ebert MP et al (2005) Protective role of heat shock protein 27 in gastric mucosal injury. J Pathol 207:177–184. doi:10.1002/path.1815

    Article  CAS  PubMed  Google Scholar 

  • Endo S et al (2007) Geranylgeranylacetone, an inducer of the 70-kDa heat shock protein (HSP70), elicits unfolded protein response and coordinates cellular fate independently of HSP70. Mol Pharmacol 72:1337–1348. doi:10.1124/mol.107.039164

    Article  CAS  PubMed  Google Scholar 

  • Fuquay JW (1981) Heat stress as it affects animal production. J Anim Sci 52:164–174

    CAS  PubMed  Google Scholar 

  • Gathiram P, Gaffin SL, Brock-Utne JG, Wells MT (1987) Time course of endotoxemia and cardiovascular changes in heat-stressed primates. Aviat Space Environ Med 58:1071–1074

    CAS  PubMed  Google Scholar 

  • Gathiram P, Wells MT, Raidoo D, Brock-Utne JG, Gaffin SL (1988) Portal and systemic plasma lipopolysaccharide concentrations in heat-stressed primates. Circ Shock 25:223–230

    CAS  PubMed  Google Scholar 

  • Geum D, Son GH, Kim K (2002) Phosphorylation-dependent cellular localization and thermoprotective role of heat shock protein 25 in hippocampal progenitor cells. J Biol Chem 277:19913–19921. doi:10.1074/jbc.M104396200

    Article  CAS  PubMed  Google Scholar 

  • Ghavami A, Hardy SP (2002) Heat shock protein and high-dose aspirin: effects on random skin flap survival in a rat model. Ann Plast Surg 48:60–67

    Article  PubMed  Google Scholar 

  • Hollander JM, Martin JL, Belke DD, Scott BT, Swanson E, Krishnamoorthy V, Dillmann WH (2004) Overexpression of wild-type heat shock protein 27 and a nonphosphorylatable heat shock protein 27 mutant protects against ischemia/reperfusion injury in a transgenic mouse model. Circulation 110:3544–3552. doi:10.1161/01.CIR.0000148825.99184.50

    Article  CAS  PubMed  Google Scholar 

  • Ito H, Hasegawa K, Inaguma Y, Kozawa O, Kato K (1996) Enhancement of stress-induced synthesis of hsp27 and alpha B crystallin by modulators of the arachidonic acid cascade. J Cell Physiol 166:332–339. doi:10.1002/(SICI)1097-4652(199602)166:2<332::AID-JCP11>3.0.CO;2-D

    Article  CAS  PubMed  Google Scholar 

  • Jurivich DA, Sistonen L, Kroes RA, Morimoto RI (1992) Effect of sodium salicylate on the human heat shock response. Science 255:1243–1245

    Article  CAS  PubMed  Google Scholar 

  • Jurivich DA, Pachetti C, Qiu L, Welk JF (1995) Salicylate triggers heat shock factor differently than heat. J Biol Chem 270:24489–24495

    Article  CAS  PubMed  Google Scholar 

  • Kamboh AA, Hang SQ, Bakhetgul M, Zhu WY (2013) Effects of genistein and hesperidin on biomarkers of heat stress in broilers under persistent summer stress. Poult Sci 92:2411–2418. doi:10.3382/ps.2012-02960

    Article  CAS  PubMed  Google Scholar 

  • Kargul J, Laurent GJ (2012) Small heat shock proteins: molecular protectors against the disease. Int J Biochem Cell Biol 44:1587. doi:10.1016/j.biocel.2012.06.022

    Article  CAS  PubMed  Google Scholar 

  • Kato K, Hasegawa K, Goto S, Inaguma Y (1994) Dissociation as a result of phosphorylation of an aggregated form of the small stress protein, hsp27. J Biol Chem 269:11274–11278

    CAS  PubMed  Google Scholar 

  • Kim SR, Bae MK, Kim JY, Wee HJ, Yoo MA, Bae SK (2009) Aspirin induces apoptosis through the blockade of IL-6-STAT3 signaling pathway in human glioblastoma A172 cells. Biochem Biophys Res Commun 387:342–347. doi:10.1016/j.bbrc.2009.07.022

    Article  CAS  PubMed  Google Scholar 

  • Lambert H, Charette SJ, Bernier AF, Guimond A, Landry J (1999) HSP27 multimerization mediated by phosphorylation-sensitive intermolecular interactions at the amino terminus. J Biol Chem 274:9378–9385

    Article  CAS  PubMed  Google Scholar 

  • Lamoureux F, Thomas C, Yin MJ, Fazli L, Zoubeidi A, Gleave ME (2013) Suppression of heat shock protein 27 using OGX-427 induces endoplasmic reticulum stress and potentiates heat shock protein 90 inhibitors to delay castrate-resistant prostate cancer. Eur Urol. doi:10.1016/j.eururo.2013.12.019

    PubMed  Google Scholar 

  • Lappas GD, Karl IE, Hotchkiss RS (1994) Effect of ethanol and sodium arsenite on HSP-72 formation and on survival in a murine endotoxin model. Shock 2:34–39, discussion 40

    Article  CAS  PubMed  Google Scholar 

  • Lindquist S (1986) The heat-shock response. Annu Rev Biochem 55:1151–1191. doi:10.1146/annurev.bi.55.070186.005443

    Article  CAS  PubMed  Google Scholar 

  • Liu L et al (2007) Over-expression of heat shock protein 27 attenuates doxorubicin-induced cardiac dysfunction in mice. Eur J Heart Fail 9:762–769. doi:10.1016/j.ejheart.2007.03.007

    Article  CAS  PubMed  Google Scholar 

  • Ma X et al (2013) Heat shock protein 27 attenuates neointima formation and accelerates reendothelialization after arterial injury and stent implantation: importance of vascular endothelial growth factor up-regulation. FASEB J. doi:10.1096/fj.13-230417

    Google Scholar 

  • Mansoor AH, Mujtaba MT, Silver B (2013) Antiplatelet therapy to prevent recurrent stroke: Three good options. CleveClin J Med 80:787–795. doi:10.3949/ccjm.80a.12149

    Google Scholar 

  • Marber MS, Mestril R, Chi SH, Sayen MR, Yellon DM, Dillmann WH (1995) Overexpression of the rat inducible 70-kD heat stress protein in a transgenic mouse increases the resistance of the heart to ischemic injury. J Clin Invest 95:1446–1456. doi:10.1172/JCI117815

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mathew A, Mathur SK, Morimoto RI (1998) Heat shock response and protein degradation: regulation of HSF2 by the ubiquitin-proteasome pathway. Mol Cell Biol 18:5091–5098

    CAS  PubMed Central  PubMed  Google Scholar 

  • Mearow KM, Dodge ME, Rahimtula M, Yegappan C (2002) Stress-mediated signaling in PC12 cells - the role of the small heat shock protein, Hsp27, and Akt in protecting cells from heat stress and nerve growth factor withdrawal. J Neurochem 83:452–462

    Article  CAS  PubMed  Google Scholar 

  • Mehlen P, Kretz-Remy C, Preville X, Arrigo AP (1996) Human hsp27, Drosophila hsp27 and human alphaB-crystallin expression-mediated increase in glutathione is essential for the protective activity of these proteins against TNFalpha-induced cell death. EMBO J 15:2695–2706

    CAS  PubMed Central  PubMed  Google Scholar 

  • Mitchell MA, Sandercock DA (1995) Creatine kinase isoenzyme profiles in the plasma of the domestic fowl (Gallus domesticus): effects of acute heat stress. Res Vet Sci 59:30–34

    Article  CAS  PubMed  Google Scholar 

  • Morrison S (1983) Ruminant heat stress: effect on production and means of alleviation. J Anim Sci 57:1594–1600

    CAS  PubMed  Google Scholar 

  • Park IS et al (2010) Aspirin induces apoptosis in YD-8 human oral squamous carcinoma cells through activation of caspases, down-regulation of Mcl-1, and inactivation of ERK-1/2 and AKT. Toxicol in Vitro 24:713–720. doi:10.1016/j.tiv.2010.01.010

    Article  CAS  PubMed  Google Scholar 

  • Patrono C, Garcia Rodriguez LA, Landolfi R, Baigent C (2005) Low-dose aspirin for the prevention of atherothrombosis. N Engl J Med 353:2373–2383. doi:10.1056/NEJMra052717

    Article  CAS  PubMed  Google Scholar 

  • Piestun Y, Druyan S, Brake J, Yahav S (2013) Thermal manipulations during broiler incubation alter performance of broilers to 70 days of age. Poult Sci 92:1155–1163. doi:10.3382/ps.2012-02609

    Article  CAS  PubMed  Google Scholar 

  • Rai UC, Ambwany P (1980) Cardiovascular changes during varied thermal stress. Indian J Physiol Pharmacol 24:119–125

    CAS  PubMed  Google Scholar 

  • Ribeiro SP, Villar J, Downey GP, Edelson JD, Slutsky AS (1994) Sodium arsenite induces heat shock protein-72 kilodalton expression in the lungs and protects rats against sepsis. Crit Care Med 22:922–929

    Article  CAS  PubMed  Google Scholar 

  • Rogalla T et al (1999) Regulation of Hsp27 oligomerization, chaperone function, and protective activity against oxidative stress/tumor necrosis factor alpha by phosphorylation. J Biol Chem 274:18947–18956

    Article  CAS  PubMed  Google Scholar 

  • Ryan AJ, Flanagan SW, Moseley PL, Gisolfi CV (1992) Acute heat stress protects rats against endotoxin shock. J Appl Physiol (1985) 73:1517–1522

    CAS  Google Scholar 

  • Rylander MN, Feng Y, Bass J, Diller KR (2005) Thermally induced injury and heat-shock protein expression in cells and tissues. Ann N Y Acad Sci 1066:222–242. doi:10.1196/annals.1363.009

    Article  CAS  PubMed  Google Scholar 

  • Sandoval-Montiel AA, Zentella-de-Pina M, Ventura-Gallegos JL, Frias-Gonzalez S, Lopez-Macay A, Zentella-Dehesa A (2013) HSP-72 accelerated expression in mononuclear cells induced in vivo by acetyl salicylic acid can be reproduced in vitro when combined with H2O2. PLoS One 8:e65449. doi:10.1371/journal.pone.0065449

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Saravanan G, Ponmurugan P, Sathiyavathi M, Vadivukkarasi S, Sengottuvelu S (2013) Cardioprotective activity of Amaranthus viridis Linn: effect on serum marker enzymes, cardiac troponin and antioxidant system in experimental myocardial infarcted rats. Int J Cardiol 165:494–498. doi:10.1016/j.ijcard.2011.09.005

    Article  CAS  PubMed  Google Scholar 

  • Singh A, Rathaur S (2010) Combination of DEC plus aspirin induced mitochondrial mediated apoptosis in filarial parasite Setaria cervi. Biochimie 92:894–900. doi:10.1016/j.biochi.2010.03.018

    Article  CAS  PubMed  Google Scholar 

  • Solomon DH, Glynn RJ, Levin R, Avorn J (2002) Nonsteroidal anti-inflammatory drug use and acute myocardial infarction. Arch Intern Med 162:1099–1104

    Article  CAS  PubMed  Google Scholar 

  • Stetler RA, Gao Y, Signore AP, Cao G, Chen J (2009) HSP27: mechanisms of cellular protection against neuronal injury. Curr Mol Med 9:863–872

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • St-Pierre* NR, Cobanov B, Schnitkey G† (2003) Economic losses from heat stress by US livestock industries. J Dairy Sci 86

  • Sutcliffe P et al (2013) Aspirin in primary prevention of cardiovascular disease and cancer: a systematic review of the balance of evidence from reviews of randomized trials. PLoS One 8, e81970. doi:10.1371/journal.pone.0081970

    Article  PubMed Central  PubMed  Google Scholar 

  • Taba K et al (2010) Heat-shock protein 27 is phosphorylated in gemcitabine-resistant pancreatic cancer cells. Anticancer Res 30:2539–2543

    CAS  PubMed  Google Scholar 

  • Tang S et al (2013) Localization and expression of Hsp27 and alphaB-crystallin in rat primary myocardial cells during heat stress in vitro. PLoS One 8, e69066. doi:10.1371/journal.pone.0069066

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Villar J, Ribeiro SP, Mullen JB, Kuliszewski M, Post M, Slutsky AS (1994) Induction of the heat shock response reduces mortality rate and organ damage in a sepsis-induced acute lung injury model. Crit Care Med 22:914–921

    Article  CAS  PubMed  Google Scholar 

  • Wang Z, Gao R, Huang Y, Tian B, Zhou Y (2009) Effects of mitogen-activated protein kinase signal pathway on heat shock protein 27 expression in human lens epithelial cells exposed to sodium salicylate in vitro. J Huazhong Univ Sci TechnologMed Sci 29:377–382. doi:10.1007/s11596-009-0323-x

    Article  CAS  Google Scholar 

  • Wischmeyer PE (2002) Glutamine and heat shock protein expression. Nutrition 18:225–228

    Article  CAS  PubMed  Google Scholar 

  • Wong HR (1999) Heat shock proteins. Facts, thoughts, and dreams. A. De Maio. Shock 11:1-12, 1999. Shock 12:323–325

    Article  CAS  PubMed  Google Scholar 

  • Wu NC, Chen TH, Yang YC, Liao FT, Wang JJ (2013) N-acetylcysteine improves cardiac contractility and ameliorates myocardial injury in a rat model of lung ischemia and reperfusion injury. Transplant Proc 45:3550–3554. doi:10.1016/j.transproceed.2013.09.005

    Article  CAS  PubMed  Google Scholar 

  • Zeren G et al (2013) Relation of heart-type fatty acid-binding protein with the degree and extent of atherosclerosis in patients with non-ST elevation acute coronary syndrome. Turk Kardiyoloji Dernegi arsivi : Turk Kardiyoloji Derneginin yayin organidir 41:610–616. doi:10.5543/tkda.2013.26974

    Article  Google Scholar 

  • Zhao W, Wisniewski M, Wang W, Liu J, Liu Y (2013) Heat-induced oxidative injury contributes to inhibition of Botrytis cinerea spore germination and growth. World J Microbiol Biotechnol. doi:10.1007/s11274-013-1513-z

    Google Scholar 

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Acknowledgments

This work was supported by grants from the National Natural Science Foundation of China (31372403), the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD), and the Sino-German Agricultural Cooperation Project of the Federal Ministry of Food, the Agriculture and Consumer Production, Berlin, Germany.

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Authors and Affiliations

  1. College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, 210095, China

    Di Wu, Jiao Xu, Erbao Song, Shu Tang, Xiaohui Zhang & Endong Bao

  2. Institute for Animal Hygiene, Animal Welfare and Farm Animal Behaviour, University of Veterinary Medicine Hannover, Foundation, Hannover, Germany

    N. Kemper & J. Hartung

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  1. Di Wu
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  2. Jiao Xu
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  3. Erbao Song
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  4. Shu Tang
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Wu, D., Xu, J., Song, E. et al. Acetyl salicylic acid protected against heat stress damage in chicken myocardial cells and may associate with induced Hsp27 expression. Cell Stress and Chaperones 20, 687–696 (2015). https://doi.org/10.1007/s12192-015-0596-x

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