Exercise, heat shock proteins and insulin resistance
Open accessAbstract
Best known as chaperones, heat shock proteins (HSPs) also have roles in cell signalling and regulation of metabolism. Rodent studies demonstrate that heat treatment, transgenic overexpression and pharmacological induction of HSP72 prevent high-fat diet-induced glucose intolerance and skeletal muscle insulin resistance. Overexpression of skeletal muscle HSP72 in mice has been shown to increase endurance running capacity nearly twofold and increase mitochondrial content by 50%. A positive correlation between HSP72 mRNA expression and mitochondrial enzyme activity has been observed in human skeletal muscle, and HSP72 expression is markedly decreased in skeletal muscle of insulin resistant and type 2 diabetic patients. In addition, decreased levels of HSP72 correlate with insulin resistance and non-alcoholic fatty liver disease progression in livers from obese patients. These data suggest the targeted induction of HSPs could be a therapeutic approach for preventing metabolic disease by maintaining the body's natural stress response. Exercise elicits a number of metabolic adaptations and is a powerful tool in the prevention and treatment of insulin resistance. Exercise training is also a stimulus for increased HSP expression. Although the underlying mechanism(s) for exercise-induced HSP expression are currently unknown, the HSP response may be critical for the beneficial metabolic effects of exercise. Exercise-induced extracellular HSP release may also contribute to metabolic homeostasis by actively restoring HSP72 content in insulin resistant tissues containing low endogenous levels of HSPs. This article is part of the theme issue ‘Heat shock proteins as modulators and therapeutic targets of chronic disease: an integrated perspective’.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Hepatokines are a novel class of exercise-inducible soluble factors released by the liver during and after physical activity, including selenoprotein P, FGF21, HSP72, and hepassocin.
“Hepatokines represent a novel class of exercise-inducible soluble factors released by the liver during and after physical activity, including selenoprotein P (SeP) [93], FGF21 [118], heat shock protein 72 (HSP72) [119], and hepassocin (HPS) (Figure 3) [120].”
From Exerkines and Sarcopenia: Unveiling the Mechanism Behind Exercise-Induced Mitochondrial Homeostasis (2025) · cites this paper as [119]
Cites
1 retracted
Dysregulation of muscle lipid metabolism in rats selectively bred for low aerobic running capacity
Spargo, F. J., McGee, S. L., Dzamko, N. L., Watt, M. J., Kemp, B. E., Britton, S. L., Koch, L. G., Hargreaves, M., & Hawley, J. A. (2007) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00702.2006 · Cited by 21 · see citing works
RetractedInflammation and metabolic disorders
Hotamisligil, G. S. (2006) · Nature · doi:10.1038/nature05485 · Cited by 9,199 · see citing works
Wu, Z., Puigserver, P., Andersson, U., Zhang, C., Adelmant, G., Mootha, V., Troy, A., Cinti, S., Lowell, B., Scarpulla, R. C., et al. (1999) · Cell · doi:10.1016/s0092-8674(00)80611-x · Cited by 4,139 · see citing works
The unfolded protein response: controlling cell fate decisions under ER stress and beyond
Hetz, C. A. (2012) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3270 · Cited by 4,118 · see citing works
A Cold-Inducible Coactivator of Nuclear Receptors Linked to Adaptive Thermogenesis
Puigserver, P., Wu, Z., Park, C. W., Graves, R., Wright, M., & Spiegelman, B. M. (1998) · Cell · doi:10.1016/s0092-8674(00)81410-5 · Cited by 3,864 · see citing works
Endoplasmic Reticulum Stress Links Obesity, Insulin Action, and Type 2 Diabetes
Özcan, U., Cao, Q., Yilmaz, E., Lee, A.-H., Iwakoshi, N. N., Özdelen, E., Tuncman, G., Görgün, C., Glimcher, L. H., & Hotamisligil, G. S. (2004) · Science · doi:10.1126/science.1103160 · Cited by 3,844 · see citing works
Mutation of the mouse klotho gene leads to a syndrome resembling ageing
Kuro-o, M., Matsumura, Y., Aizawa, H., Kawaguchi, H., Suga, T., Utsugi, T., Ohyama, Y., Kurabayashi, M., Kaname, T., Kume, E., et al. (1997) · Nature · doi:10.1038/36285 · Cited by 3,837 · see citing works
A central role for JNK in obesity and insulin resistance
Hirosumi, J., Tuncman, G., Chang, L., Görgün, C. Z., Uysal, K. T., Maeda, K., Karin, M., & Hotamisligil, G. S. (2002) · Nature · doi:10.1038/nature01137 · Cited by 3,359 · see citing works
Özcan, U., Yilmaz, E., Özcan, L., Furuhashi, M., Vaillancourt, E., Smith, R. O., Görgün, C. Z., & Hotamisligil, G. S. (2006) · Science · doi:10.1126/science.1128294 · Cited by 2,413 · see citing works
Impaired Mitochondrial Activity in the Insulin-Resistant Offspring of Patients with Type 2 Diabetes
Petersen, K. F., Dufour, S., Befroy, D., Garcia, R., & Shulman, G. I. (2004) · New England Journal of Medicine · doi:10.1056/nejmoa031314 · Cited by 2,193 · see citing works
Patti, M. E., Butte, A. J., Crunkhorn, S., Cusi, K., Berria, R., Kashyap, S., Miyazaki, Y., Kohane, I., Costello, M., Saccone, R., et al. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1032913100 · Cited by 1,952 · see citing works
Morimoto, R. I. (1998) · Genes & Development · doi:10.1101/gad.12.24.3788 · Cited by 1,898 · see citing works
Yuan, M., Konstantopoulos, N., Lee, J., Hansen, L., Li, Z.-W., Karin, M., & Shoelson, S. E. (2001) · Science · doi:10.1126/science.1061620 · Cited by 1,884 · see citing works
Asea, A. A. A., Kraeft, S., Kurt‐Jones, E. A., Stevenson, M. A., Chen, L. B., Finberg, R. W., Koo, G. C., & Calderwood, S. K. (2000) · Nature Medicine · doi:10.1038/74697 · Cited by 1,621 · see citing works
Yu, C., Chen, Y., Cline, G. W., Zhang, D., Zong, H., Wang, Y., Bergeron, R., Kim, J. K., Cushman, S. W., Cooney, G. J., et al. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m200958200 · Cited by 1,561 · see citing works
Ross, R., Dagnone, D., Jones, P. J. H., Smith, H., Paddags, A., Hudson, R., & Janssen, I. (2000) · Annals of Internal Medicine · doi:10.7326/0003-4819-133-2-200007180-00008 · Cited by 1,435 · see citing works
CD91 Is a Common Receptor for Heat Shock Proteins gp96, hsp90, hsp70, and Calreticulin
Basu, S., Binder, R. J., Ramalingam, T. R., & Srivastava, P. K. (2001) · Immunity · doi:10.1016/s1074-7613(01)00111-x · Cited by 1,123 · see citing works
Sounding the Alarm: Protein Kinase Cascades Activated by Stress and Inflammation
Kyriakis, J. M., & Avruch, J. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.40.24313 · Cited by 1,083 · see citing works
Adaptations of skeletal muscle to exercise: rapid increase in the transcriptional coactivator PGC-1
Baar, K., Wende, A. R., Jones, T. E., Marison, M., Nolte, L. A., Chen, M., Kelly, D. P., & Holloszy, J. O. (2002) · The FASEB Journal · doi:10.1096/fj.02-0367com · Cited by 1,020 · see citing works
Marber, M. S., Latchman, D. S., Walker, J. M., & Yellon, D. M. (1993) · Circulation · doi:10.1161/01.cir.88.3.1264 · Cited by 1,000 · see citing works
Regulation of Hepatic Lipogenesis by the Transcription Factor XBP1
Lee, A., Scapa, E. F., Cohen, D. E., & Glimcher, L. H. (2008) · Science · doi:10.1126/science.1158042 · Cited by 978 · see citing works
Morino, K., Petersen, K. F., & Shulman, G. I. (2006) · Diabetes · doi:10.2337/db06-s002 · Cited by 853 · see citing works
Perry, R. J., Camporez, J.-P. G., Kursawe, R., Titchenell, P. M., Zhang, D., Perry, C. J., Jurczak, M. J., Abudukadier, A., Han, M. S., Zhang, X.-M., et al. (2015) · Cell · doi:10.1016/j.cell.2015.01.012 · Cited by 719 · see citing works
JNK Expression by Macrophages Promotes Obesity-Induced Insulin Resistance and Inflammation
Han, M. S., Jung, D. Y., Morel, C., Lakhani, S. A., Kim, J. K., Flavell, R. A., & Davis, R. J. (2012) · Science · doi:10.1126/science.1227568 · Cited by 635 · see citing works
Activation and Dysregulation of the Unfolded Protein Response in Nonalcoholic Fatty Liver Disease
Puri, P., Mirshahi, F., Cheung, O., Natarajan, R., Maher, J. W., Kellum, J. M., & Sanyal, A. J. (2007) · Gastroenterology · doi:10.1053/j.gastro.2007.10.039 · Cited by 596 · see citing works
Rutkowski, D. T., Wu, J., Back, S.-H., Callaghan, M. U., Ferris, S. P., Iqbal, J., Clark, R. L., Miao, H. Z., Hassler, J. R., Fornek, J. L., et al. (2008) · Developmental Cell · doi:10.1016/j.devcel.2008.10.015 · Cited by 580 · see citing works
Effect of the volume and intensity of exercise training on insulin sensitivity
Houmard, J. A., Tanner, C. J., Slentz, C. A., Duscha, B. D., McCartney, J. S., & Kraus, W. E. (2004) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00707.2003 · Cited by 568 · see citing works
HSP72 protects against obesity-induced insulin resistance
Chung, J., Nguyen, A.-K., Henstridge, D. C., Holmes, A. G., Chan, M. H. S., Mesa, J. L., Lancaster, G. I., Southgate, R. J., Bruce, C. R., Duffy, S. J., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0705799105 · Cited by 553 · see citing works
Exosome-dependent Trafficking of HSP70
Lancaster, G. I., & Febbraio, M. A. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m502017200 · Cited by 547 · see citing works
Wang, D., Wei, Y., & Pagliassotti, M. J. (2005) · Endocrinology · doi:10.1210/en.2005-0570 · Cited by 529 · see citing works
Hanawa, N., Shinohara, M., Saberi, B., Gaarde, W. A., Han, D., & Kaplowitz, N. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m708916200 · Cited by 527 · see citing works
Repeated high-force eccentric exercise: effects on muscle pain and damage
Newham, D. J., Jones, D. A., & CLARKSON, P. M. (1987) · Journal of Applied Physiology · doi:10.1152/jappl.1987.63.4.1381 · Cited by 494 · see citing works
Endoplasmic reticulum stress is reduced in tissues of obese subjects after weight loss
Gregor, M. F., Yang, L., Fabbrini, E., Mohammed, B. S., Eagon, J. C., Hotamisligil, G. S., & Klein, S. (2009) · Diabetes · doi:10.2337/db08-1220 · Cited by 488 · see citing works
Cytosolic proteostasis through importing of misfolded proteins into mitochondria
Ruan, L., Zhou, C., Jin, E., Kucharavy, A., Zhang, Y., Wen, Z., Florens, L. A., & Li, R. (2017) · Nature · doi:10.1038/nature21695 · Cited by 474 · see citing works
Kim, B.-J., Ryu, S.-W., & Song, B.-J. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m510644200 · Cited by 470 · see citing works
c-Jun N-terminal Kinase (JNK) Mediates Feedback Inhibition of the Insulin Signaling Cascade
Lee, Y. H., Giraud, J., Davis, R. J., & White, M. F. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m208359200 · Cited by 441 · see citing works
Goodpaster, B. H., Katsiaras, A., & Kelley, D. E. (2003) · Diabetes · doi:10.2337/diabetes.52.9.2191 · Cited by 390 · see citing works
Tuncman, G., Hirosumi, J., Solinas, G., Chang, L., Karin, M., & Hotamisligil, G. S. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0603509103 · Cited by 350 · see citing works
Ma, X., Xu, L., Alberobello, A. T., Gavrilova, O., Bagattin, A., Skarulis, M. C., Liu, J., Finkel, T., & Mueller, E. (2015) · Cell Metabolism · doi:10.1016/j.cmet.2015.08.005 · Cited by 337 · see citing works
Bruce, C. R., Carey, A. L., Hawley, J. A., & Febbraio, M. A. (2003) · Diabetes · doi:10.2337/diabetes.52.9.2338 · Cited by 318 · see citing works
Hsp72 functions as a natural inhibitory protein of c‐Jun N‐terminal kinase
Park, H.-S., Lee, J., Huh, S., Seo, J., & Choi, E. (2001) · The EMBO Journal · doi:10.1093/emboj/20.3.446 · Cited by 317 · see citing works
Brunt, V. E., Howard, M. J., Francisco, M. A., Ely, B. R., & Minson, C. T. (2016) · The Journal of Physiology · doi:10.1113/jp272453 · Cited by 317 · see citing works
Kline, M. P., & Morimoto, R. I. (1997) · Molecular and Cellular Biology · doi:10.1128/mcb.17.4.2107 · Cited by 312 · see citing works
Wu, J., Ruas, J. L., Estall, J. L., Rasbach, K. A., Choi, J. H., Ye, L., Boström, P., Tyra, H. M., Crawford, R. W., Campbell, K. P., et al. (2011) · Cell Metabolism · doi:10.1016/j.cmet.2011.01.003 · Cited by 312 · see citing works
Broquet, A. H., Thomas, G., Masliah, J., Trugnan, G., & Bachelet, M. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m302326200 · Cited by 303 · see citing works
Role of the unfolded protein response, GRP78 and GRP94 in organ homeostasis
Zhu, G., & Lee, A. S. (2014) · Journal of Cellular Physiology · doi:10.1002/jcp.24923 · Cited by 301 · see citing works
Splanchnic and Peripheral Disposal of Oral Glucose in Man
Katz, L. D., Glickman, M. G., Rapoport, S. I., Ferrannini, E., & DeFronzo, R. A. (1983) · Diabetes · doi:10.2337/diab.32.7.675 · Cited by 287 · see citing works
Silencing of Lipid Metabolism Genes through IRE1α-Mediated mRNA Decay Lowers Plasma Lipids in Mice
So, J., Hur, K. Y., Tarrio, M. L., Ruda, V. M., Frank-Kamenetsky, M. D., Fitzgerald, K. J., Koteliansky, V., Lichtman, A. H., Iwawaki, T., Glimcher, L. H., et al. (2012) · Cell Metabolism · doi:10.1016/j.cmet.2012.09.004 · Cited by 280 · see citing works
Mosser, D. D., Kotzbauer, P. T., Sarge, K. D., & Morimoto, R. I. (1990) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.87.10.3748 · Cited by 280 · see citing works
Genetics of aerobic and anaerobic performances.
Bouchard, C., Dionne, F. T., Simoneau, J. A., & Boulay, M. R. (1992) · PubMed · Cited by 272 · see citing works
PGC-1α mRNA expression is influenced by metabolic perturbation in exercising human skeletal muscle
Norrbom, J., Sundberg, C. J., Rundqvist, H., Kraus, W. E., Jansson, E., & Gustafsson, T. P. (2004) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00765.2003 · Cited by 263 · see citing works
cDNA Cloning and mRNA Analysis of PGC-1 in Epitrochlearis Muscle in Swimming-Exercised Rats
Goto, M., Terada, S., Kato, M., Katoh, M., Yokozeki, T., Tabata, I., & Shimokawa, T. (2000) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.2000.3134 · Cited by 258 · see citing works
Kurucz, I., Morva, Á., Vaag, A. A., Eriksson, K., Huang, X., Groop, L., & Koranyi, L. I. (2002) · Diabetes · doi:10.2337/diabetes.51.4.1102 · Cited by 254 · see citing works
Gupta, S., Deepti, A., Deegan, S., Lisbona, F., Hetz, C. A., & Afshin Samali, A. (2010) · PLoS Biology · doi:10.1371/journal.pbio.1000410 · Cited by 245 · see citing works
Prada, P. O., Zecchin, H. G., Gasparetti, A. L., Torsoni, M. A., Ueno, M., Hirata, A. E., do Amaral, M. E. C., Höehr, N. F., Boschero, A. C., & Saad, M. J. A. (2005) · Endocrinology · doi:10.1210/en.2004-0767 · Cited by 244 · see citing works
Hsp70 release from peripheral blood mononuclear cells
Hunter-Lavin, C., Davies, E. L., Bacelar, M. M. F. V. G., et al. (2004) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2004.09.075 · Cited by 240 · see citing works
Gupte, A. A., Bomhoff, G. L., Swerdlow, R. H., & Geiger, P. C. (2008) · Diabetes · doi:10.2337/db08-1070 · Cited by 227 · see citing works
Self-citationGrune, T., Catalgol, B., Licht, A., Ermak, G., Pickering, A. M., Ngo, J. K., & Davies, K. J. A. (2011) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2011.06.015 · Cited by 217 · see citing works
Takeuchi, T., Suzuki, M., Fujikake, N., Popiel, H. A., Kikuchi, H., Futaki, S., Wada, K., & Nagai, Y. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1412651112 · Cited by 209 · see citing works
Hot-Tub Therapy for Type 2 Diabetes Mellitus
Hooper, P. L. (1999) · New England Journal of Medicine · doi:10.1056/nejm199909163411216 · Cited by 208 · see citing works
Henstridge, D. C., Bruce, C. R., Drew, B. G., Tory, K., Kolonics, A., Estevez, E., Chung, J., Watson, N., Gardner, T., Lee-Young, R. S., et al. (2014) · Diabetes · doi:10.2337/db13-0967 · Cited by 201 · see citing works
Exercise training modulates heat shock protein response in diabetic rats
Atalay, M., Oksala, N., Laaksonen, D. E., Khanna, S., Nakao, C., Lappalainen, J., Roy, S., Hänninen, O., & Sen, C. K. (2004) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01183.2003 · Cited by 200 · see citing works
Vernia, S., Cavanagh, J., García-Haro, L., Sabio, G., Barrett, T., Jung, D. Y., Kim, J. K., Xu, J. L., Shulha, H. P., Garber, M. G., et al. (2014) · Cell Metabolism · doi:10.1016/j.cmet.2014.06.010 · Cited by 200 · see citing works
Gong, P., Li, L., Liu, Y., Pu, J., Zhang, S., Yu, J., Zhao, J., & Liu, P. (2011) · Endocrinology · doi:10.1210/en.2010-1369 · Cited by 199 · see citing works
Exercise-induced elevation of HSP70 is intensity dependent
Milne, K. J., & Noble, E. G. (2002) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00528.2001 · Cited by 196 · see citing works
Exercise induces hepatosplanchnic release of heat shock protein 72 in humans
Febbraio, M. A., Ott, P., Nielsen, H. B., Steensberg, A., Keller, C., Krustrup, P., Secher, N. H., & Pedersen, B. K. (2002) · The Journal of Physiology · doi:10.1113/jphysiol.2002.025148 · Cited by 187 · see citing works
Koh, T. J., & Escobedo, J. (2004) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00341.2003 · Cited by 177 · see citing works
Smolka, M. B., Zoppi, C. C., Alves, A. A., Silveira, L. R., Marangoni, S., Pereira-da-Silva, L., Novello, J. C., & de Macedo, D. V. (2000) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.2000.279.5.r1539 · Cited by 176 · see citing works
Krause, M. D. S., Heck, T. G., Bittencourt, A., Scomazzon, S. P., Newsholme, P., Curi, R., & de Bittencourt, P. I. H. (2015) · Mediators of Inflammation · doi:10.1155/2015/249205 · Cited by 175 · see citing works
Win, S., Than, T. A., Fernández-Checa, J. C., & Kaplowitz, N. (2014) · Cell Death and Disease · doi:10.1038/cddis.2013.522 · Cited by 174 · see citing works
Thyfault, J. P., Rector, R. S., Uptergrove, G. M., Borengasser, S. J., Morris, E. M., Wei, Y., Laye, M. J., Burant, C., Qi, N., Ridenhour, S. E., et al. (2009) · The Journal of Physiology · doi:10.1113/jphysiol.2009.169060 · Cited by 173 · see citing works
Activation of the heat shock transcription factor by hypoxia in mammalian cells.
Benjamin, I. J., Kröger, B., & Williams, R. S. (1990) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.87.16.6263 · Cited by 171 · see citing works
Labbadia, J. P., Cunliffe, H. E., Weiss, A., Katsyuba, E., Sathasivam, K., Seredenina, T. S., Woodman, B., Moussaoui, S. M., Frentzel, S., Luthi‐Carter, R., et al. (2011) · Journal of Clinical Investigation · doi:10.1172/jci57413 · Cited by 171 · see citing works
HSP70 induction during exercise and heat stress in rats: role of internal temperature
Skidmore, R., Gutierrez, J. A., Guerriero, V., & Kregel, K. C. (1995) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1995.268.1.r92 · Cited by 170 · see citing works
Inducible isoform of HSP70 is constitutively expressed in a muscle fiber type specific pattern
Locke, M., Noble, E. G., & Atkinson, B. G. (1991) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.1991.261.5.c774 · Cited by 169 · see citing works
Chaanine, A. H., Jeong, D., Liang, L., Chemaly, E. R., Fish, K. M., Gordon, R. E., & Hajjar, R. J. (2012) · Cell Death and Disease · doi:10.1038/cddis.2012.5 · Cited by 167 · see citing works
Mycobacterium tuberculosis-Induced Neutrophil Extracellular Traps Activate Human Macrophages
Braian, C., Hogea, V., & Stendahl, O. I. (2013) · Journal of Innate Immunity · doi:10.1159/000348676 · Cited by 164 · see citing works
Deldicque, L., Cani, P. D., Philp, A., Raymackers, J.-M., Meakin, P. J., Ashford, M. L. J., Delzenne, N. M., Francaux, M., & Baar, K. (2010) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00038.2010 · Cited by 163 · see citing works
Mild heat stress induces mitochondrial biogenesis in C2C12 myotubes
Liu, C.-T., & Brooks, G. A. (2011) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00989.2011 · Cited by 158 · see citing works
Rahman, S. M., Schroeder‐Gloeckler, J. M., Janssen, R. C., Jiang, H., Qadri, I., Maclean, K. N., & Friedman, J. E. (2007) · Hepatology · doi:10.1002/hep.21614 · Cited by 155 · see citing works
Drew, B. G., Ribas, V., Le, J. A., Henstridge, D. C., Phun, J., Zhou, Z., Soleymani, T., Daraei, P., Sitz, D., Vergnes, L., et al. (2014) · Diabetes · doi:10.2337/db13-0665 · Cited by 145 · see citing works
Noland, R. C., Thyfault, J. P., Henes, S. T., Whitfield, B. R., Woodlief, T., Evans, J. R., Lust, J. A., Britton, S. L., Koch, L. G., Dudek, R. W., et al. (2007) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00500.2006 · Cited by 141 · see citing works
Win, S., Than, T. A., Le, B. H. A., García‐Ruiz, C., Fernández-Checa, J. C., & Kaplowitz, N. (2015) · Journal of Hepatology · doi:10.1016/j.jhep.2015.01.032 · Cited by 140 · see citing works
Endoplasmic reticulum stress in obesity and obesity-related disorders: An expanded view
Pagliassotti, M. J., Kim, P., Estrada, A. L., Stewart, C. M., & Gentile, C. L. (2016) · Metabolism · doi:10.1016/j.metabol.2016.05.002 · Cited by 134 · see citing works
Role of extracellular HSP72 in acute stress-induced potentiation of innate immunity in active rats
Campisi, J., & Fleshner, M. (2003) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00681.2002 · Cited by 133 · see citing works
Clinical Implications of Thermal Therapy in Lifestyle-Related Diseases
Biro, S., Masuda, A., Kihara, T., & Tei, C. (2003) · Experimental Biology and Medicine · doi:10.1177/153537020322801023 · Cited by 132 · see citing works
Schroeder‐Gloeckler, J. M., Rahman, S. M., Janssen, R. C., Qiao, L., Shao, J., Roper, M. D., Fischer, S. J., Lowe, E., Orlicky, D. J., McManaman, J. L., et al. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m701329200 · Cited by 126 · see citing works
Thompson, H. S., Clarkson, P. M., & Scordilis, S. P. (2002) · Acta Physiologica Scandinavica · doi:10.1046/j.1365-201x.2002.00922.x · Cited by 120 · see citing works
Benjamin, I. J., Horie, S., Greenberg, M., et al. (1992) · Journal of Clinical Investigation · doi:10.1172/jci115768 · Cited by 118 · see citing works
Marques, C., Guo, W., Pereira, P., Taylor, A., Patterson, C., Evans, P. C., & Shang, F. (2006) · The FASEB Journal · doi:10.1096/fj.05-5080fje · Cited by 116 · see citing works
Henstridge, D. C., Whitham, M., & Febbraio, M. A. (2014) · Molecular Metabolism · doi:10.1016/j.molmet.2014.08.003 · Cited by 110 · see citing works
Constitutive Role for IRE1α-XBP1 Signaling Pathway in the Insulin-Mediated Hepatic Lipogenic Program
Ning, J., Hong, T., Ward, A. R., Pi, J., Liu, Z., Liu, H.-Y., & Cao, W. (2011) · Endocrinology · doi:10.1210/en.2010-1036 · Cited by 109 · see citing works
Human Skeletal Muscle HSP70 Response to Physical Training Depends on Exercise Intensity
Liu, Y., Lormes, Baur, et al. (2000) · International Journal of Sports Medicine · doi:10.1055/s-2000-3784 · Cited by 108 · see citing works
Divergence of intracellular and extracellular HSP72 in type 2 diabetes: does fat matter?
Rodrigues-Krause, J. D. C., Krause, M. D. S., O’Hagan, C., VITO, G. D., Boreham, C. A., Murphy, C., Newsholme, P., & Colleran, G. (2012) · Cell Stress and Chaperones · doi:10.1007/s12192-011-0319-x · Cited by 107 · see citing works
Goto, K., Okuyama, R., Sugiyama, H., Honda, M., Kobayashi, T., Uehara, K., Akema, T., Sugiura, T., Yamada, S., Ohira, Y., et al. (2003) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-003-1177-x · Cited by 107 · see citing works
Obesity depresses the anti‐inflammatory HSP 70 pathway, contributing to NAFLD progression
Naso, F. C. D., Porto, R. R., Fillmann, H. S., Maggioni, L., Padoin, A. V., Ramos, R. J., Mottin, C. C., Bittencourt, A., Marroni, N. P., & de Bittencourt, P. I. H. (2014) · Obesity · doi:10.1002/oby.20919 · Cited by 106 · see citing works
Exercise induces the release of heat shock protein 72 from the human brain in vivo
Lancaster, G. I., Møller, K., Nielsen, B., Secher, N. H., Febbraio, M. A., & Nybo, L. (2004) · Cell Stress and Chaperones · doi:10.1379/csc-18r.1 · Cited by 103 · see citing works
Muscle Fibre Stress in Response to Exercise
Hernando, R., & Manso, R. (1997) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1997.0460a.x · Cited by 102 · see citing works
Resistance training increases heat shock protein levels in skeletal muscle of young and old rats
Murlasits, Z., Cutlip, R. G., Geronilla, K. B., Rao, K. M. K., Wonderlin, W. F., & Alway, S. E. (2006) · Experimental Gerontology · doi:10.1016/j.exger.2006.01.005 · Cited by 99 · see citing works
Marineli, R. D. S., Moura, C. S., Moraes, É. A., Lenquiste, S. A., Lollo, P. C. B., Morato, P. N., Amaya‐Farfán, J., & Maróstica, M. R. (2014) · Nutrition · doi:10.1016/j.nut.2014.11.009 · Cited by 97 · see citing works
Liu, Y., Lormes, W., Wang, L., Reissnecker, S., & Steinacker, J. M. (2004) · European Journal of Applied Physiology · doi:10.1007/s00421-003-0976-2 · Cited by 97 · see citing works
Febbraio, M. A., Mesa, J. L. M., Chung, J. Z. Y., Steensberg, A., Keller, C., Nielsen, H. B., Krustrup, P., Ott, P., Secher, N. H., & Pedersen, B. K. (2004) · Cell Stress and Chaperones · doi:10.1379/csc-24r1.1 · Cited by 95 · see citing works
Fischer, C. P., Hiscock, N. J., Basu, S., Vessby, B. O., Kallner, A., Sjöberg, L., Febbraio, M. A., & Pedersen, B. K. (2005) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00421.2005 · Cited by 92 · see citing works
Similar dose response of heat shock protein synthesis and intracellular pH change in yeast
Weitzel, G., Pilatus, U., & Rensing, L. (1985) · Experimental Cell Research · doi:10.1016/s0014-4827(85)80054-9 · Cited by 90 · see citing works
Heat shock proteins and exercise adaptations. Our knowledge thus far and the road still ahead
Henstridge, D. C., Febbraio, M. A., & Hargreaves, M. (2015) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00811.2015 · Cited by 87 · see citing works
Acute heat treatment improves insulin-stimulated glucose uptake in aged skeletal muscle
Gupte, A. A., Bomhoff, G. L., Touchberry, C. D., & Geiger, P. C. (2010) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00849.2010 · Cited by 86 · see citing works
Self-citationMorino, S., Kondo, T., Sasaki, K., Adachi, H., Suico, M. A., Sekimoto, E., Matsuda, T., Shuto, T., Araki, E., & Kai, H. (2008) · PLoS ONE · doi:10.1371/journal.pone.0004068 · Cited by 82 · see citing works
Characterization of a Receptor for Heat Shock Protein 70 on Macrophages and Monocytes
Sondermann, H., Becker, T., Mayhew, M., Wieland, F., & Hartl, F. U. (2000) · Biological Chemistry · doi:10.1515/bc.2000.144 · Cited by 81 · see citing works
Tamura, Y., Kitaoka, Y., Matsunaga, Y., Hoshino, D., & Hatta, H. (2015) · The Journal of Physiology · doi:10.1113/jp270093 · Cited by 81 · see citing works
Adaptation to exercise-induced muscle damage
Clarkson, P. M., Byrnes, W. C., Gillisson, E., et al. (1987) · Clinical Science · doi:10.1042/cs0730383 · Cited by 80 · see citing works
Gupte, A. A., Bomhoff, G. L., Morris, J. K., Gorres, B. K., & Geiger, P. C. (2009) · Journal of Applied Physiology · doi:10.1152/japplphysiol.91210.2008 · Cited by 78 · see citing works
Self-citationHeat shock protein 72 : release and biological significance during exercise
Whitham, M. (2007) · Frontiers in bioscience · doi:10.2741/2765 · Cited by 77 · see citing works
Zeng, X., Wang, H., Bai, F., Zhou, X., Li, S., Ren, L., Sun, R., Xue, C. C., Jiang, H., Hu, L., et al. (2015) · British Journal of Pharmacology · doi:10.1111/bph.13209 · Cited by 70 · see citing works
Trained Men Display Increased Basal Heat Shock Protein Content of Skeletal Muscle
Morton, J. P., MacLaren, D. P. M., Cable, N. T., Campbell, I. T., Evans, L., Kayani, A. C., McArdle, A., & Drust, B. (2008) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e31816a7171 · Cited by 67 · see citing works
Tei, C., Imamura, T., Kinugawa, K., Inoue, T., Masuyama, T., Inoue, H., Noike, H., Muramatsu, T., Takeishi, Y., Saku, K., et al. (2016) · Circulation Journal · doi:10.1253/circj.cj-16-0051 · Cited by 61 · see citing works
Xu, L., Ma, X., Bagattin, A., et al. (2016) · Cell Death and Disease · doi:10.1038/cddis.2016.22 · Cited by 55 · see citing works
Lee, K., Lee, C., Kim, Y. W., Han, S. K., Shim, Y., & Yoo, C. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m410059200 · Cited by 54 · see citing works
Gjøvaag, T. F., & Dahl, H. A. (2006) · European Journal of Applied Physiology · doi:10.1007/s00421-006-0281-y · Cited by 51 · see citing works
Beever, R. (2010) · The Journal of Alternative and Complementary Medicine · doi:10.1089/acm.2009.0358 · Cited by 51 · see citing works
Modeling type 2 diabetes-like hyperglycemia in C. elegans on a microdevice
Zhu, G., Yin, F., Wang, L., Wei, W., Jiang, L., & Qin, J. (2015) · Integrative Biology · doi:10.1039/c5ib00243e · Cited by 49 · see citing works
Deficiency in the Heat Stress Response Could Underlie Susceptibility to Metabolic Disease
Rogers, R. S., Morris, E. M., Wheatley, J. L., Archer, A. E., McCoin, C. S., White, K. S., Wilson, D. R., Meers, G. M.-E., Koch, L. G., Britton, S. L., et al. (2016) · Diabetes · doi:10.2337/db16-0292 · Cited by 44 · see citing works
Self-citationYonezawa, K., Yamamoto, Y., Yamamoto, H., et al. (2001) · Journal of Hepatology · doi:10.1016/s0168-8278(01)00191-x · Cited by 40 · see citing works
Aerobic capacity mediates susceptibility for the transition from steatosis to steatohepatitis
Morris, E. M., McCoin, C. S., Allen, J., Gastecki, M. L., Koch, L. G., Britton, S. L., Fletcher, J. A., Fu, X., Ding, W., Burgess, S. C., et al. (2017) · The Journal of Physiology · doi:10.1113/jp274281 · Cited by 37 · see citing works
Daviau, A., Proulx, R., Robitaille, K., et al. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m607612200 · Cited by 36 · see citing works
Divergent Selection for Aerobic Capacity in Rats as a Model for Complex Disease
Koch, L. G. (2005) · Integrative and Comparative Biology · doi:10.1093/icb/45.3.405 · Cited by 36 · see citing works
Larkins, N. T., Murphy, R. M., & Lamb, G. D. (2011) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00266.2011 · Cited by 35 · see citing works
Exercise reduces cellular stress related to skeletal muscle insulin resistance
de Matos, M. A., Ottone, V. D. O., Duarte, T. C., Sampaio, P. F. D. M., Costa, K. B., Fonseca, C. A., Neves, M. P. C., Schneider, S. M., Moseley, P. L., Coimbra, C. C., et al. (2013) · Cell Stress and Chaperones · doi:10.1007/s12192-013-0453-8 · Cited by 34 · see citing works
Lollo, P. C. B., Moura, C. S., Morato, P. N., & Amaya‐Farfán, J. (2013) · Europe PMC (PubMed Central) · Cited by 33 · see citing works
Silverstein‐Metzler, M. G., Ordanes, D., Wylie, A. T., Files, D. C., Milligan, C., Presley, T. D., & Kavanagh, K. (2014) · The Journals of Gerontology Series A · doi:10.1093/gerona/glu119 · Cited by 32 · see citing works
Henstridge, D. C., Forbes, J. M., Penfold, S. A., Formosa, M. F., Dougherty, S. L., Gasser, A., de Courten, M., Cooper, M. E., Kingwell, B. A., & de Courten, B. V. (2010) · Metabolism · doi:10.1016/j.metabol.2010.01.027 · Cited by 29 · see citing works
Adachi, H., Kondo, T., Ogawa, R., Sasaki, K., Morino‐Koga, S., Sakakida, M., Kawashima, J., Motoshima, H., Furukawa, N., Tsuruzoe, K., et al. (2010) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00075.2010 · Cited by 29 · see citing works
Kavanagh, K., Davis, A., Jenkins, K. A., & Flynn, D. M. (2016) · Cell Stress and Chaperones · doi:10.1007/s12192-016-0699-z · Cited by 26 · see citing works
Aging Does Not Reduce Heat Shock Protein 70 in the Absence of Chronic Insulin Resistance
Kavanagh, K., Wylie, A. T., Chavanne, T. J., Jorgensen, M. J., Voruganti, V. S., Comuzzie, A. G., Kaplan, J. R., McCall, C. E., & Kritchevsky, S. B. (2012) · The Journals of Gerontology Series A · doi:10.1093/gerona/gls008 · Cited by 23 · see citing works
Rivas, E., Newmire, D. E., Crandall, C. G., Hooper, P. L., & Ben‐Ezra, V. (2016) · Journal of Thermal Biology · doi:10.1016/j.jtherbio.2016.04.010 · Cited by 21 · see citing works
Chen, H.-W., Chen, S., Tsai, J.-L., et al. (1999) · PubMed · Cited by 20 · see citing works
Exercise training and experimental diabetes modulate heat shock protein response in brain
Lappalainen, Z., Lappalainen, J., Oksala, N., et al. (2010) · Scandinavian Journal of Medicine and Science in Sports · doi:10.1111/j.1600-0838.2008.00872.x · Cited by 19 · see citing works
Liang, M., Wang, X., Yuan, Y., et al. (2009) · Acta Biochimica et Biophysica Sinica · doi:10.1093/abbs/gmn020 · Cited by 18 · see citing works
Bock, P. M., Krause, M. D. S., Schroeder, H. T., Hahn, G. F., Takahashi, H., Schöler, C. M., Nicoletti, G., Neto, L. D. Z., Rodrigues, M. I. L., Bruxel, M. A., et al. (2015) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-015-2597-6 · Cited by 18 · see citing works
Glucose regulates heat shock factor 1 transcription activity via mTOR pathway in HCC cell lines
Ma, W., Zhang, Y., Mu, H., et al. (2015) · Cell Biology International · doi:10.1002/cbin.10493 · Cited by 14 · see citing works
Rivas, E., Newmire, D. E., & Ben‐Ezra, V. (2016) · Physiology & Behavior · doi:10.1016/j.physbeh.2016.08.026 · Cited by 9 · see citing works
Martín-Cordero, L., García, J. J., Hinchado, M. D., Bote, E., & Ortega, E. (2012) · Journal of Physiology and Biochemistry · doi:10.1007/s13105-012-0196-5 · Cited by 7 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
The Sleep-Immune Crosstalk in Health and Disease
Besedovsky, L., Lange, T., & Haack, M. (2019) · Physiological Reviews · doi:10.1152/physrev.00010.2018 · Cited by 1,479 · see citing works
“For example, they increase in the brain during synaptic firing (305) and in the periphery during acute mental (52, 273) or physical stress (13).”
BackgroundExercise sustains the hallmarks of health
Qiu, Y., Fernández-García, B., Lehmann, H. I., Li, G., Kroemer, G., López-Otín, C., & Xiao, J. (2023) · Journal of Sport and Health Science · doi:10.1016/j.jshs.2022.10.003 · Cited by 270 · see citing works
Exerkines and Sarcopenia: Unveiling the Mechanism Behind Exercise-Induced Mitochondrial Homeostasis
Wang, J., Jia, D., Zhang, Z., & Wang, D. (2025) · Metabolites · doi:10.3390/metabo15010059 · Cited by 23 · see citing works
- Authors
- Archer, A. E., Von Schulze, A. T., & Geiger, P. C.
- Affiliations
- University of Kansas Medical Center (US)
- ORCID
- Geiger, Paige C.
- Venue
- Philosophical Transactions of the Royal Society B: Biological Sciences
- Publisher
- The Royal Society
- Published
- 2017-12-04
- Volume
- 373
- Issue
- 1738
- Pages
- 20160529
- ISSN
- 0962-8436 (ISSN-L)
- 1471-2970
- PMC
- PMC5717529
- OpenAlex
- W2772015960
- Cited by
- 122
- References
- 141
- Citations by year
- 2026: 6 · 2025: 11 · 2024: 15 · 2023: 20 · 2022: 24 · 2021: 16 · 2020: 16 · 2019: 6 · 2018: 7 · 2017: 1
- FWCI
- 0.77
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Philosophical Transactions of the Royal Society B Biological Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (HD-002528)
- Foundation for the National Institutes of Health (AG-031575)
- National Institute of General Medical Sciences (P20 GM103418)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Heat shock proteins research
- Health Sciences › Medicine › Rehabilitation › Exercise and Physiological Responses
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
- Keywords
- heat shock proteins, HSP72, insulin resistance, exercise training, skeletal muscle, type 2 diabetes, non-alcoholic fatty liver disease, mitochondrial function, impaired glucose tolerance, high-fat diet, metabolic adaptation, stress response
- MeSH terms
- Animals, Heat-Shock Proteins, Humans, Insulin Resistance, Physical Conditioning, Animal, Exercise, Mice, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review