References
Adachi H, Katsuno M, Waza M, Minamiyama M, Tanaka F, Sobue G (2009) Heat shock proteins in neurodegenerative diseases: pathogenic roles and therapeutic implications. Int J Hyperthermia 25(8):647–654. doi:10.3109/02656730903315823
Asea A, Kraeft SK, Kurt-Jones EA, Stevenson MA, Chen LB, Finberg RW, Koo GC, Calderwood SK (2000) HSP70 stimulates cytokine production through a CD14-dependant pathway, demonstrating its dual role as a chaperone and cytokine. Nat Med 6(4):435–442. doi:10.1038/74697
Bathaie SZ, Jafarnejad A, Hosseinkhani S, Nakhjavani M (2010) The effect of hot-tub therapy on serum Hsp70 level and its benefit on diabetic rats: a preliminary report. Int J Hyperthermia 26(6):577–585. doi:10.3109/02656736.2010.485594
Beckmann RP, Lovett M, Welch WJ (1992) Examining the function and regulation of hsp 70 in cells subjected to metabolic stress. J Cell Biol 117(6):1137–1150
Bernstein RK (2000) Hot-tub therapy for type 2 diabetes mellitus. N Engl J Med 342(3):218. doi:10.1056/NEJM200001203420318, author reply 218–219
Bruce CR, Carey AL, Hawley JA, Febbraio MA (2003) Intramuscular heat shock protein 72 and heme oxygenase-1 mRNA are reduced in patients with type 2 diabetes: evidence that insulin resistance is associated with a disturbed antioxidant defense mechanism. Diabetes 52(9):2338–2345
Calderwood SK, Theriault JR, Gong J (2005) Message in a bottle: role of the 70-kDa heat shock protein family in anti-tumor immunity. Eur J Immunol 35(9):2518–2527. doi:10.1002/eji.200535002
Calderwood SK, Mambula SS, Gray PJ Jr, Theriault JR (2007) Extracellular heat shock proteins in cell signaling. FEBS Lett 581(19):3689–3694. doi:10.1016/j.febslet.2007.04.044
Chirico WJ, Waters MG, Blobel G (1988) 70K heat shock related proteins stimulate protein translocation into microsomes. Nature 332(6167):805–810. doi:10.1038/332805a0
Chung J, Nguyen AK, Henstridge DC, Holmes AG, Chan MH, Mesa JL, Lancaster GI, Southgate RJ, Bruce CR, Duffy SJ, Horvath I, Mestril R, Watt MJ, Hooper PL, Kingwell BA, Vigh L, Hevener A, Febbraio MA (2008) HSP72 protects against obesity-induced insulin resistance. Proc Natl Acad Sci U S A 105(5):1739–1744. doi:10.1073/pnas.0705799105
Feder ME, Hofmann GE (1999) Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol 61:243–282. doi:10.1146/annurev.physiol.61.1.243
Friedewald WT, Levy RI, Fredrickson DS (1972) Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem 18(6):499–502
Garrido C, Gurbuxani S, Ravagnan L, Kroemer G (2001) Heat shock proteins: endogenous modulators of apoptotic cell death. Biochem Biophys Res Commun 286(3):433–442. doi:10.1006/bbrc.2001.5427
Gruden G, Bruno G, Chaturvedi N, Burt D, Pinach S, Schalkwijk C, Stehouwer CD, Witte DR, Fuller JH, Cavallo-Perin P (2009) ANTI-HSP60 and ANTI-HSP70 antibody levels and micro/macrovascular complications in type 1 diabetes: the EURODIAB Study. J Intern Med 266(6):527–536. doi:10.1111/j.1365-2796.2009.02129.x
Gupte AA, Bomhoff GL, Morris JK, Gorres BK, Geiger PC (2009a) Lipoic acid increases heat shock protein expression and inhibits stress kinase activation to improve insulin signaling in skeletal muscle from high-fat-fed rats. J Appl Physiol 106(4):1425–1434. doi:10.1152/japplphysiol.91210.2008
Gupte AA, Bomhoff GL, Swerdlow RH, Geiger PC (2009b) Heat treatment improves glucose tolerance and prevents skeletal muscle insulin resistance in rats fed a high-fat diet. Diabetes 58(3):567–578. doi:10.2337/db08-1070
Hayashida K, Kume N, Murase T, Minami M, Nakagawa D, Inada T, Tanaka M, Ueda A, Kominami G, Kambara H, Kimura T, Kita T (2005) Serum soluble lectin-like oxidized low-density lipoprotein receptor-1 levels are elevated in acute coronary syndrome: a novel marker for early diagnosis. Circulation 112(6):812–818. doi:10.1161/CIRCULATIONAHA.104.468397
Hayot M, Michaud A, Koechlin C, Caron MA, Leblanc P, Prefaut C, Maltais F (2005) Skeletal muscle microbiopsy: a validation study of a minimally invasive technique. Eur Respir J 25(3):431–440. doi:10.1183/09031936.05.00053404
Henstridge DC, Forbes JM, Penfold SA, Formosa MF, Dougherty S, Gasser A, de Courten MP, Cooper ME, Kingwell BA, de Courten B (2010) The relationship between heat shock protein 72 expression in skeletal muscle and insulin sensitivity is dependent on adiposity. Metabolism 59(11):1556–1561. doi:10.1016/j.metabol.2010.01.027
Homem de Bittencourt PI Jr, Lagranha DJ, Maslinkiewicz A, Senna SM, Tavares AM, Baldissera LP, Janner DR, Peralta JS, Bock PM, Gutierrez LL, Scola G, Heck TG, Krause MS, Cruz LA, Abdalla DS, Lagranha CJ, Lima T, Curi R (2007) LipoCardium: endothelium-directed cyclopentenone prostaglandin-based liposome formulation that completely reverses atherosclerotic lesions. Atherosclerosis 193(2):245–258. doi:10.1016/j.atherosclerosis.2006.08.049
Hooper PL (1999) Hot-tub therapy for type 2 diabetes mellitus. N Engl J Med 341(12):924–925. doi:10.1056/NEJM199909163411216
Hooper PL (2009) Inflammation, heat shock proteins, and type 2 diabetes. Cell Stress Chaperones 14(2):113–115. doi:10.1007/s12192-008-0073-x
Hooper PL, Hooper JJ (2005) Loss of defense against stress: diabetes and heat shock proteins. Diabetes Technol Ther 7(1):204–208. doi:10.1089/dia.2005.7.204
Horn P, Kalz A, Lim CL, Pyne D, Saunders P, Mackinnon L, Peake J, Suzuki K (2007) Exercise-recruited NK cells display exercise-associated eHSP-70. Exerc Immunol Rev 13:100–111
Johnson JD, Fleshner M (2006) Releasing signals, secretory pathways, and immune function of endogenous extracellular heat shock protein 72. J Leukoc Biol 79(3):425–434. doi:10.1189/jlb.0905523
Kampinga HH, Henning RH, van Gelder IC, Brundel BJ (2007) Heat shock proteins and atrial fibrillation. Cell Stress Chaperones 12(2):97–100
Kampinga HH, Hageman J, Vos MJ, Kubota H, Tanguay RM, Bruford EA, Cheetham ME, Chen B, Hightower LE (2009) Guidelines for the nomenclature of the human heat shock proteins. Cell Stress Chaperones 14(1):105–111. doi:10.1007/s12192-008-0068-7
Kaneto H, Matsuoka TA, Nakatani Y, Kawamori D, Miyatsuka T, Matsuhisa M, Yamasaki Y (2005) Oxidative stress, ER stress, and the JNK pathway in type 2 diabetes. J Mol Med (Berl) 83(6):429–439. doi:10.1007/s00109-005-0640-x
Kavanagh K, Flynn DM, Jenkins KA, Zhang L, Wagner JD (2009) Restoring HSP70 deficiencies improves glucose tolerance in diabetic monkeys. Am J Physiol Endocrinol Metab 300(5):E894–901. doi:10.1152/ajpendo.00699.2010
Krause M, Rodrigues-Krause Jda C (2011) Extracellular heat shock proteins (eHSP70) in exercise: possible targets outside the immune system and their role for neurodegenerative disorders treatment. Med Hypotheses 76(2):286–290. doi:10.1016/j.mehy.2010.10.025
Krause MS, Oliveira LP Jr, Silveira EM, Vianna DR, Rossato JS, Almeida BS, Rodrigues MF, Fernandes AJ, Costa JA, Curi R, de Bittencourt PI Jr (2007) MRP1/GS-X pump ATPase expression: is this the explanation for the cytoprotection of the heart against oxidative stress-induced redox imbalance in comparison to skeletal muscle cells? Cell Biochem Funct 25(1):23–32. doi:10.1002/cbf.1343
Krause M, McClenaghan N, Flatt PR, Homem de Bittencourt PI, Murphy C, Newsholme P (2011) L-arginine is essential for pancreatic beta-cell functional integrity, metabolism and defence from inflammatory challenge. J Endocrinol. doi:10.1530/JOE-11-0236
Kume N, Mitsuoka H, Hayashida K, Tanaka M, Kominami G, Kita T (2010) Soluble lectin-like oxidized LDL receptor-1 (sLOX-1) as a sensitive and specific biomarker for acute coronary syndrome—comparison with other biomarkers. J Cardiol 56(2):159–165. doi:10.1016/j.jjcc.2010.05.002
Kurthy M, Mogyorosi T, Nagy K, Kukorelli T, Jednakovits A, Talosi L, Biro K (2002) Effect of BRX-220 against peripheral neuropathy and insulin resistance in diabetic rat models. Ann N Y Acad Sci 967:482–489
Kurucz I, Morva A, Vaag A, Eriksson KF, Huang X, Groop L, Koranyi L (2002) Decreased expression of heat shock protein 72 in skeletal muscle of patients with type 2 diabetes correlates with insulin resistance. Diabetes 51(4):1102–1109
Lindquist S, Craig EA (1988) The heat-shock proteins. Annu Rev Genet 22:631–677. doi:10.1146/annurev.ge.22.120188.003215
Literati-Nagy B, Kulcsar E, Literati-Nagy Z, Buday B, Peterfai E, Horvath T, Tory K, Kolonics A, Fleming A, Mandl J, Koranyi L (2009) Improvement of insulin sensitivity by a novel drug, BGP-15, in insulin-resistant patients: a proof of concept randomized double-blind clinical trial. Horm Metab Res 41(5):374–380. doi:10.1055/s-0028-1128142
Locke M, Noble EG (1995) Stress proteins: the exercise response. Can J Appl Physiol 20(2):155–167
Madden LA, Sandstrom ME, Lovell RJ, McNaughton L (2008) Inducible heat shock protein 70 and its role in preconditioning and exercise. Amino Acids 34(4):511–516. doi:10.1007/s00726-007-0004-7
Mayer MP, Bukau B (2005) Hsp70 chaperones: cellular functions and molecular mechanism. Cell Mol Life Sci 62(6):670–684. doi:10.1007/s00018-004-4464-6
Nakhjavani M, Morteza A, Khajeali L, Esteghamati A, Khalilzadeh O, Asgarani F, Outeiro TF (2010) Increased serum HSP70 levels are associated with the duration of diabetes. Cell Stress Chaperones 15(6):959–964. doi:10.1007/s12192-010-0204-z
Nakhjavani M, Morteza A, Meysamie A, Esteghamati A, Khalilzadeh O, Esfahanian F, Khajeali L, Feiz F (2011) Serum heat shock protein 70 and oxidized LDL in patients with type 2 diabetes: does sex matter? Cell Stress Chaperones 16(2):195–201. doi:10.1007/s12192-010-0232-8
Newsholme P, Homem De Bittencourt PI, O' Hagan C, De Vito G, Murphy C, Krause MS (2009) Exercise and possible molecular mechanisms of protection from vascular disease and diabetes: the central role of ROS and nitric oxide. Clin Sci (Lond) 118(5):341–349. doi:10.1042/CS20090433
Njemini R, Demanet C, Mets T (2004) Inflammatory status as an important determinant of heat shock protein 70 serum concentrations during aging. Biogerontology 5(1):31–38
Njemini R, Bautmans I, Onyema OO, Van Puyvelde K, Demanet C, Mets T (2011) Circulating heat shock protein 70 in health, aging and disease. BMC Immunol 12:24. doi:10.1186/1471-2172-12-24
Noble EG, Milne KJ, Melling CW (2008) Heat shock proteins and exercise: a primer. Appl Physiol Nutr Metab 33(5):1050–1065. doi:10.1139/H08-069
Oglesbee MJ, Herdman AV, Passmore GG, Hoffman WH (2005) Diabetic ketoacidosis increases extracellular levels of the major inducible 70-kDa heat shock protein. Clin Biochem 38(10):900–904. doi:10.1016/j.clinbiochem.2005.05.011
Ortega E, Giraldo E, Hinchado MD, Martinez M, Ibanez S, Cidoncha A, Collazos ME, Garcia JJ (2006) Role of Hsp72 and norepinephrine in the moderate exercise-induced stimulation of neutrophils' microbicide capacity. Eur J Appl Physiol 98(3):250–255. doi:10.1007/s00421-006-0269-7
Ortega E, Hinchado MD, Martin-Cordero L, Asea A (2009) The effect of stress-inducible extracellular Hsp72 on human neutrophil chemotaxis: a role during acute intense exercise. Stress 12(3):240–249. doi:10.1080/10253890802309853
Patti ME, Butte AJ, Crunkhorn S, Cusi K, Berria R, Kashyap S, Miyazaki Y, Kohane I, Costello M, Saccone R, Landaker EJ, Goldfine AB, Mun E, DeFronzo R, Finlayson J, Kahn CR, Mandarino LJ (2003) Coordinated reduction of genes of oxidative metabolism in humans with insulin resistance and diabetes: potential role of PGC1 and NRF1. Proc Natl Acad Sci U S A 100(14):8466–8471. doi:10.1073/pnas.1032913100
Richard V, Kaeffer N, Thuillez C (1996) Delayed protection of the ischemic heart—from pathophysiology to therapeutic applications. Fundam Clin Pharmacol 10(5):409–415
Silveira EM, Rodrigues MF, Krause MS, Vianna DR, Almeida BS, Rossato JS, Oliveira LP Jr, Curi R, de Bittencourt PI Jr (2007) Acute exercise stimulates macrophage function: possible role of NF-kappaB pathways. Cell Biochem Funct 25(1):63–73. doi:10.1002/cbf.1365
Tytell M (2005) Release of heat shock proteins (Hsps) and the effects of extracellular Hsps on neural cells and tissues. Int J Hyperthermia 21(5):445–455. doi:10.1080/02656730500041921
Vitai M, Buday B, Kulcsar E, Literati-Nagy B, Vecsei I, Bezzegh K, Peterfai E, Kurucz I, Koranyi L (2009) Occurrence of GRB10 (+11275 G > A) polymorphism in Hungarian population and its relationship to glucose metabolism. Orv Hetil 150(40):1845–1851. doi:10.1556/OH.2009.28729
Walsh RC, Koukoulas I, Garnham A, Moseley PL, Hargreaves M, Febbraio MA (2001) Exercise increases serum Hsp72 in humans. Cell Stress Chaperones 6(4):386–393
Watt MJ, Hevener A, Lancaster GI, Febbraio MA (2006) Ciliary neurotrophic factor prevents acute lipid-induced insulin resistance by attenuating ceramide accumulation and phosphorylation of c-Jun N-terminal kinase in peripheral tissues. Endocrinology 147(5):2077–2085. doi:10.1210/en.2005-1074
Wei W, Liu Q, Tan Y, Liu L, Li X, Cai L (2009) Oxidative stress, diabetes, and diabetic complications. Hemoglobin 33(5):370–377. doi:10.3109/03630260903212175
Westerheide SD, Morimoto RI (2005) Heat shock response modulators as therapeutic tools for diseases of protein conformation. J Biol Chem 280(39):33097–33100. doi:10.1074/jbc.R500010200
Whitham M, Fortes MB (2008) Heat shock protein 72: release and biological significance during exercise. Front Biosci 13:1328–1339
Wright E Jr, Scism-Bacon JL, Glass LC (2006) Oxidative stress in type 2 diabetes: the role of fasting and postprandial glycaemia. Int J Clin Pract 60(3):308–314. doi:10.1111/j.1368-5031.2006.00825.x
Yang XM, Baxter GF, Heads RJ, Yellon DM, Downey JM, Cohen MV (1996) Infarct limitation of the second window of protection in a conscious rabbit model. Cardiovasc Res 31(5):777–783. doi:10.1016/0008-6363(96)00026-0
Acknowledgements
We thank the Department of Science, Institute of Technology Tallaght, Dublin, Ireland, UCD School of Biomolecular and Biomedical Science, and UCD Institute for Sport and Health and the TSR: Strand III—Core Research Strengths Enhancement Scheme (Ireland) for supporting this work.
Declaration of interest
The authors declare that there is no conflict of interest that could be perceived as prejudicing the impartiality of the research reported.
Funding
This work was supported by the Institute of Technology Technological Sector Research (TSR): Strand III – Core Research Strengths Enhancement Scheme (Ireland).
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Rodrigues-Krause, J., Krause, M., O’Hagan, C. et al. Divergence of intracellular and extracellular HSP72 in type 2 diabetes: does fat matter?. Cell Stress and Chaperones 17, 293–302 (2012). https://doi.org/10.1007/s12192-011-0319-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12192-011-0319-x