Effects of heat stress on muscle mass and the expression levels of heat shock proteins and lysosomal cathepsin L in soleus muscle of young and aged mice

Molecular and Cellular Biochemistry

Volumn 369, Issue 1-2, 2012, Pages 45-53

  Ohno, Yoshitaka ^a   Yamada, Sumio ^b   Goto, Ayumi ^a   Ikuta, Akihiro ^a   Sugiura, Takao ^c   Ohira, Yoshinobu ^d   Yoshioka, Toshitada ^e   Goto, Katsumasa ^a  

^a TOYOHASHI SOZO UNIVERSITY   (Japan)

^b NAGOYA UNIVERSITY   (Japan)

^c YAMAGUCHI UNIVERSITY   (Japan)

^d OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^e HIROSAKI GAKUIN UNIVERSITY   (Japan)

Author keywords

Aging; Heat shock proteins; Heat stress; Lysosomal enzyme; Skeletal muscle

Indexed keywords

CALPAIN 1; CALPAIN 2; CATHEPSIN L; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 25; HEAT SHOCK PROTEIN 72; S6 KINASE;

AGING; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; HEAT STRESS; LYSOSOME MEMBRANE; MALE; MOUSE; MUSCLE CELL; MUSCLE HYPERTROPHY; MUSCLE MASS; NONHUMAN; PROTEIN CONTENT; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SKELETAL MUSCLE; SOLEUS MUSCLE; UPREGULATION;

AGING; ANIMALS; CATHEPSIN L; GENE EXPRESSION; HOT TEMPERATURE; HSP27 HEAT-SHOCK PROTEINS; HSP72 HEAT-SHOCK PROTEINS; LYSOSOMES; MALE; MICE; MICE, INBRED C57BL; MUSCLE, SKELETAL;

MUS;

EID: 84865659118     PISSN: 03008177     EISSN: 15734919     Source Type: Journal    
DOI: 10.1007/s11010-012-1367-y     Document Type: Article

References (53)

1. G Goldspink 1999 Changes in muscle mass and phenotype and the expression of autocrine and systemic growth factors by muscle in response to stretch and overload J Anat 194 323 334 10.1046/j.1469-7580.1999.19430323.x 10386770 10.1046/j.1469-7580.1999.19430323.x 1:CAS:528:DyaK1MXktFemt7w%3D (Pubitemid 29241484)
2. DA Riley EI Ilyina-Kakueva S Ellis JL Bain GR Slocum FR Sedlak 1990 Skeletal muscle fiber, nerve, and blood vessel breakdown in space-flown rats FASEB J 4 84 91 2153085 1:STN:280:DyaK3c7gvVGisw%3D%3D
3. VJ Caiozzo MJ Baker RE Herrick M Tao KM Baldwin 1994 Effect of spaceflight on skeletal muscle: mechanical properties and myosin isoform content of a slow muscle J Appl Physiol 76 1764 1773 8045858 10.1063/1.357693 1:STN:280:DyaK2czitFaqtA%3D%3D (Pubitemid 24125700)
4. DL Allen W Yasui T Tanaka Y Ohira S Nagaoka C Sekiguchi WE Hinds RR Roy VR Edgerton 1996 Myonuclear number and myosin heavy chain expression in rat soleus single muscle fibers after spaceflight J Appl Physiol 81 145 151 8828656 1:CAS:528:DyaK28XkvFemt7Y%3D (Pubitemid 26255501)
5. ER Barton-Davis DI Shoturma A Musaro N Rosenthal HL Sweeney 1998 Viral mediated expression of insulin-like growth factor I blocks the aging-related loss of skeletal muscle function Proc Natl Acad Sci USA 95 15603 15607 9861016 10.1073/pnas.95.26.15603 1:CAS:528:DyaK1MXhvFejtA%3D%3D (Pubitemid 29018746)
6. RN Baumgartner KM Koehler D Gallagher L Romero SB Heymsfield RR Ross PJ Garry RD Lindeman 1998 Epidemiology of sarcopenia among the elderly in New Mexico Am J Epidemiol 147 755 763 9554417 10.1093/oxfordjournals.aje.a009520 1:STN:280:DyaK1c3htlSkuw%3D%3D (Pubitemid 28183275)
7. WR Frontera VA Hughes RA Fielding MA Fiatarone WJ Evans R Roubenoff 2000 Aging of skeletal muscle: a 12-yr longitudinal study J Appl Physiol 88 1321 1326 10749826 1:STN:280:DC%2BD3c3hsV2gug%3D%3D (Pubitemid 30217433)
8. L Combaret D Dardevet D Béchet D Taillandier L Mosoni D Attaix 2009 Skeletal muscle proteolysis in aging Curr Opin Clin Nutr Metab Care 12 37 41 10.1097/MCO.0b013e32831b9c31 19057185 10.1097/MCO.0b013e32831b9c31
9. K Lenk G Schuler V Adams 2010 Skeletal muscle wasting in cachexia and sarcopenia: molecular pathophysiology and impact of exercise training J Cachexia Sarcopenia Muscle 1 9 21 10.1007/s13539-010-0007-1 21475693 10.1007/s13539-010-0007-1
10. SM Phillips KD Tipton A Aarsland SE Wolf RR Wolfe 1997 Mixed muscle protein synthesis and breakdown after resistance exercise in humans Am J Physiol 273 E99 E107 9252485 1:CAS:528:DyaK2sXlt1SrsLk%3D
11. SM Phillips KD Tipton AA Ferrando RR Wolfe 1999 Resistance training reduces the acute exercise-induced increase in muscle protein turnover Am J Physiol 276 E118 E124 9886957 1:CAS:528:DyaK1MXntlemsg%3D%3D
12. D Cuthbertson K Smith J Babraj G Leese T Waddell P Atherton H Wackerhage PM Taylor MJ Rennie 2005 Anabolic signaling deficits underlie amino acid resistance of wasting, aging muscle FASEB J 19 422 424 10.1096/fj.04-2640fje 15596483 1:CAS:528:DC%2BD2MXit1Klu7k%3D (Pubitemid 40316537)
13. R Koopman LJ van Loon 2009 Aging, exercise, and muscle protein metabolism J Appl Physiol 106 2040 2048 10.1152/japplphysiol.91551.2008 19131471 10.1152/japplphysiol.91551.2008 1:CAS:528:DC%2BD1MXnvVWlsr0%3D
14. L Breen SM Phillips 2011 Skeletal muscle protein metabolism in the elderly: Interventions to counteract the 'anabolic resistance' of ageing Nutr Metab (Lond) 8 68 10.1186/1743-7075-8-68 10.1186/1743-7075-8-68 1:CAS:528:DC%2BC38XhsFWktQ%3D%3D
15. K Uehara K Goto T Kobayashi A Kojima T Akema T Sugiura S Yamada Y Ohira T Yoshioka H Aoki 2004 Heat-stress enhances proliferative potential in rat soleus muscle Jpn J Physiol 54 263 271 10.2170/jjphysiol.54.263 15541204 10.2170/jjphysiol.54.263 1:STN:280:DC%2BD2crntVWhtw%3D%3D (Pubitemid 39539299)
16. T Kobayashi K Goto A Kojima T Akema K Uehara H Aoki T Sugiura Y Ohira T Yoshioka 2005 Possible role of calcineurin in heating-related increase of rat muscle mass Biochem Biophys Res Commun 331 1301 1309 10.1016/j.bbrc.2005.04.096 15883017 10.1016/j.bbrc.2005.04.096 1:CAS:528:DC%2BD2MXjvFelsrY%3D (Pubitemid 40692498)
17. K Goto H Oda S Morioka T Naito T Akema H Kato H Fujiya Y Nakajima T Sugiura Y Ohira T Yoshioka 2007 Skeletal muscle hypertrophy induced by low-intensity exercise with heat-stress in healthy human subjects Jpn J Aerospace Environ Med 44 13 18
18. K Goto H Oda H Kondo M Igaki A Suzuki S Tsuchiya T Murase T Hase H Fujiya I Matsumoto H Naito T Sugiura Y Ohira T Yoshioka 2011 Responses of muscle mass, strength and gene transcripts to long-term heat stress in healthy human subjects Eur J Appl Physiol 111 17 27 10.1007/s00421-010-1617-1 20803152 10.1007/s00421-010-1617-1
19. H Naito SK Powers HA Demirel T Sugiura SL Dodd J Aoki 2000 Heat stress attenuates skeletal muscle atrophy in hindlimb-unweighted rats J Appl Physiol 88 359 363 10642402 1:STN:280:DC%2BD3c7gvFeisA%3D%3D (Pubitemid 30053868)
20. K Goto M Honda T Kobayashi K Uehara A Kojima T Akema T Sugiura S Yamada Y Ohira T Yoshioka 2004 Heat stress facilitates the recovery of atrophied soleus muscle in rat Jpn J Physiol 54 285 293 10.2170/jjphysiol.54.285 15541206 10.2170/jjphysiol.54.285 1:STN:280:DC%2BD2crntVWhtQ%3D%3D (Pubitemid 39539301)
21. WJ Welch 1992 Mammalian stress response: cell physiology, structure/function of stress proteins, and implications for medicine and disease Physiol Rev 72 1063 1081 1438579 1:CAS:528:DyaK3sXls1OltQ%3D%3D
22. EA Craig BD Gambill RJ Nelson 1993 Heat shock proteins: molecular chaperones of protein biogenesis Microbiol Rev 57 402 414 8336673 1:CAS:528:DyaK3sXlslOitbo%3D (Pubitemid 23170099)
23. D Hayes V Napoli A Mazurkie WF Stafford P Graceffa 2009 Phosphorylation dependence of hsp27 multimeric size and molecular chaperone function J Biol Chem 284 18801 18807 10.1074/jbc.M109.011353 19411251 10.1074/jbc.M109.011353 1:CAS:528:DC%2BD1MXotVKnsLc%3D
24. DS Latchman 2001 Heat shock proteins and cardiac protection Cardiovasc Res 51 637 646 10.1016/S0008-6363(01)00354-6 11530097 10.1016/S0008-6363(01) 00354-6 1:CAS:528:DC%2BD3MXmt1Kks7o%3D (Pubitemid 32800706)
25. L Chung YC Ng 2006 Age-related alterations in expression of apoptosis regulatory proteins and heat shock proteins in rat skeletal muscle Biochim Biophys Acta 1762 103 109 10.1016/j.bbadis.2005.08.003 16139996 10.1016/j.bbadis.2005.08.003 1:CAS:528:DC%2BD2MXht1OntbjN (Pubitemid 43021092)
26. J Nylandsted M Gyrd-Hansen A Danielewicz N Fehrenbacher U Lademann M Høyer-Hansen E Weber G Multhoff M Rohde M Jäättelä 2004 Heat shock protein 70 promotes cell survival by inhibiting lysosomal membrane permeabilization J Exp Med 200 425 435 10.1084/jem.20040531 15314073 10.1084/jem.20040531 1:CAS:528:DC%2BD2cXmvFehtrw%3D (Pubitemid 39121900)
27. C Bivik I Rosdahl K Ollinger 2007 Hsp70 protects against UVB induced apoptosis by preventing release of cathepsins and cytochrome c in human melanocytes Carcinogenesis 28 537 544 10.1093/carcin/bgl152 16950797 10.1093/carcin/bgl152 1:CAS:528:DC%2BD2sXjslOgu7Y%3D (Pubitemid 46523349)
28. AJ Barrett H Kirschke 1981 Cathepsin B, cathepsin H, and cathepsin L Methods Enzymol 80 535 561 7043200 10.1016/S0076-6879(81)80043-2 1:CAS:528:DyaL38XitFejsLw%3D
29. D Bechet A Tassa D Taillandier L Combaret D Attaix 2005 Lysosomal proteolysis in skeletal muscle Int J Biochem Cell Biol 37 2098 2114 10.1016/j.nmd.2008.04.010 16125113 10.1016/j.biocel.2005.02.029 1:CAS:528:DC%2BD2MXpsVWmsb4%3D (Pubitemid 41206824)
30. C Deval S Mordier C Obled D Bechet L Combaret D Attaix M Ferrara 2001 Identification of cathepsin L as a differentially expressed message associated with skeletal muscle wasting Biochem J 360 143 150 11696001 10.1042/0264-6021: 3600143 1:CAS:528:DC%2BD3MXovVCltLk%3D (Pubitemid 33081958)
31. SH Lecker RT Jagoe A Gilbert M Gomes V Baracos J Bailey SR Price WE Mitch AL Goldberg 2004 Multiple types of skeletal muscle atrophy involve a common program of changes in gene expression FASEB J 18 39 51 10.1096/fj.03-0610com 14718385 10.1096/fj.03-0610com 1:CAS:528:DC%2BD2cXmt1KgsA%3D%3D (Pubitemid 38076464)
32. JM Sacheck JP Hyatt A Raffaello RT Jagoe RR Roy VR Edgerton SH Lecker AL Goldberg 2007 Rapid disuse and denervation atrophy involve transcriptional changes similar to those of muscle wasting during systemic diseases FASEB J 21 140 155 10.1096/fj.06-6604com1 17116744 10.1096/fj.06-6604com 1:CAS:528:DC%2BD2sXmvFCjug%3D%3D (Pubitemid 46052553)
33. E Volpi M Sheffield-Moore BB Rasmussen RR Wolfe 2001 Basal muscle amino acid kinetics and protein synthesis in healthy young and older men JAMA 286 1206 1212 11559266 10.1001/jama.286.10.1206 1:CAS:528:DC%2BD3MXnt1Sns78%3D (Pubitemid 33015550)
34. SC Bodine TN Stitt M Gonzalez WO Kline GL Stover R Bauerlein E Zlotchenko A Scrimgeour JC Lawrence DJ Glass GD Yancopoulos 2001 Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo Nat Cell Biol 3 1014 1019 10.1038/ncb1101-1014 11715023 10.1038/ncb1101-1014 1:CAS:528:DC%2BD3MXosVCjsrk%3D (Pubitemid 34428747)
35. T Sugiura N Abe M Nagano K Goto K Sakuma H Naito T Yoshioka SK Powers 2005 Changes in PKB/Akt and calcineurin signaling during recovery in atrophied soleus muscle induced by unloading Am J Physiol Regul Integr Comp Physiol 288 R1273 R1278 10.1152/ajpregu.00688.2004 15821284 10.1152/ajpregu.00688.2004 1:CAS:528:DC%2BD2MXktlSgsLw%3D (Pubitemid 40593711)
36. SR Kimball JP O'Malley JC Anthony SJ Crozier LS Jefferson 2004 Assessment of biomarkers of protein anabolism in skeletal muscle during the life span of the rat: sarcopenia despite elevated protein synthesis Am J Physiol Endocrinol Metab 287 E772 E780 10.1152/ajpendo.00535.2003 15187001 10.1152/ajpendo.00535. 2003 1:CAS:528:DC%2BD2cXptVyiurg%3D (Pubitemid 39237908)
37. RS Kinnard DB Mylabathula S Uddemarri KM Rice GL Wright ER Blough 2005 Regulation of p70S6K, GSK-3β, and calcineurin in rat striated muscle during aging Biogerontology 6 173 184 10.1007/s10522-005-7953-6 16041621 10.1007/s10522-005-7953-6 1:CAS:528:DC%2BD2MXmsVyjsrY%3D (Pubitemid 41131167)
38. D Taillandier E Aurousseau L Combaret CY Guezennec D Attaix 2003 Regulation of proteolysis during reloading of the unweighted soleus muscle Int J Biochem Cell Biol 35 665 675 10.1016/S1357-2725(03)00004-9 12672458 10.1016/S1357-2725(03)00004-9 1:CAS:528:DC%2BD3sXisFShtLY%3D (Pubitemid 36369514)
39. S Servais D Letexier R Favier C Duchamp D Desplanches 2007 Prevention of unloading-induced atrophy by vitamin E supplementation: links between oxidative stress and soleus muscle proteolysis? Free Radic Biol Med 42 627 635 10.1016/j.freeradbiomed.2006.12.001 17291986 10.1016/j.freeradbiomed.2006.12.001 1:CAS:528:DC%2BD2sXhs1Smurc%3D (Pubitemid 46210130)
40. A Kojima K Goto S Morioka T Naito T Akema H Fujiya T Sugiura Y Ohira M Beppu H Aoki T Yoshioka 2007 Heat stress facilitates the regeneration of injured skeletal muscle in rats J Orthop Sci 12 74 82 10.1007/s00776-006-1083-0 17260121 10.1007/s00776-006-1083-0 (Pubitemid 46169943)
41. F Kawano A Ishihara JL Stevens XD Wang S Ohshima M Horisaka Y Maeda I Nonaka Y Ohira 2004 Tension- and afferent input-associated responses of neuromuscular system of rats to hindlimb unloading and/or tenotomy Am J Physiol Regul Integr Comp Physiol 287 R76 R86 10.1152/ajpregu.00694.2003 15031139 10.1152/ajpregu.00694.2003 1:CAS:528:DC%2BD2cXmtVeks7k%3D (Pubitemid 38856313)
42. DB Thomason RE Herrick KM Baldwin 1987 Activity influences on soleus muscle myosin during rodent hindlimb suspension J Appl Physiol 63 138 144 3624121 1:STN:280:DyaL2szgslOrtQ%3D%3D (Pubitemid 17107137)
43. K Yasuhara Y Ohno A Kojima K Uehara M Beppu T Sugiura M Fujimoto A Nakai Y Ohira T Yoshioka K Goto 2011 Absence of heat shock transcription factor 1 retards the regrowth of atrophied soleus muscle in mice J Appl Physiol 111 1142 1149 10.1152/japplphysiol.00471.2011 21817109 10.1152/japplphysiol.00471.2011 1:CAS:528:DC%2BC3MXhtl2ru7vE
44. L Guth FJ Samaha 1970 Procedure for the histochemical demonstration of actomyosin ATPase Exp Neurol 28 365 367 10.1016/0014-4886(70)90244-X 4248172 10.1016/0014-4886(70)90244-X 1:CAS:528:DyaE3cXltFOjtbk%3D
45. T Snijders LB Verdijk LJ van Loon 2009 The impact of sarcopenia and exercise training on skeletal muscle satellite cells Ageing Res Rev 8 328 338 10.1016/j.arr.2009.05.003 19464390 10.1016/j.arr.2009.05.003
46. T Ogata Y Oishi RR Roy H Ohmori 2003 Endogenous expression and developmental changes of HSP72 in rat skeletal muscles J Appl Physiol 95 1279 1286 10.1152/japplphysiol.00353.2003 12909603 1:CAS:528:DC%2BD3sXnsFCjt78%3D (Pubitemid 37034026)
47. KA Huey JS Thresher CM Brophy RR Roy 2004 Inactivity-induced modulation of Hsp20 and Hsp25 content in rat hindlimb muscles Muscle Nerve 30 95 101 10.1002/mus.20063 15221884 10.1002/mus.20063 1:CAS:528:DC%2BD2cXmtl2gtbk%3D (Pubitemid 38880330)
48. HM Argadine CB Mantilla WZ Zhan GC Sieck 2011 Intracellular signaling pathways regulating net protein balance following diaphragm muscle denervation Am J Physiol Cell Physiol 300 C318 C327 10.1152/ajpcell.00172.2010 21084642 10.1152/ajpcell.00172.2010 1:CAS:528:DC%2BC3MXisFyjtbg%3D
49. Y Ohno S Yamada T Sugiura Y Ohira T Yoshioka K Goto 2010 A possible role of NF-κB and HSP72 in skeletal muscle hypertrophy induced by heat stress in rats Gen Physiol Biophys 29 234 242 10.4149/gpb-2010-03-234 20817947 10.4149/gpb-2010-03-234 1:CAS:528:DC%2BC3cXhsVGhur3N
50. JT Selsby SL Dodd 2005 Heat treatment reduces oxidative stress and protects muscle mass during immobilization Am J Physiol Regul Integr Comp Physiol 289 R134 R139 10.1152/ajpregu.00497.2004 15761186 10.1152/ajpregu.00497. 2004 1:CAS:528:DC%2BD2MXmvVCjs7k%3D (Pubitemid 40874968)
51. K Goto R Okuyama H Sugiyama M Honda T Kobayashi K Uehara T Akema T Sugiura S Yamada Y Ohira T Yoshioka 2003 Effects of heat stress and mechanical stretch on protein expression in cultured skeletal muscle cells Pflugers Arch 447 247 253 10.1007/s00424-003-1177-x 14534791 10.1007/s00424-003-1177-x 1:CAS:528:DC%2BD3sXovVOhtLo%3D (Pubitemid 38177740)
52. KA Huey 2006 Regulation of HSP25 expression and phosphorylation in functionally overloaded rat plantaris and soleus muscles J Appl Physiol 100 451 456 10.1152/japplphysiol.01022.2005 16223977 10.1152/japplphysiol.01022.2005 1:CAS:528:DC%2BD28Xhs1KhurY%3D (Pubitemid 43671594)
53. Y Ohno S Yamada T Sugiura Y Ohira T Yoshioka K Goto 2011 Possible role of NF-κB signals in heat stress-associated increase in protein content of cultured C2C12 cells Cells Tissues Organs 194 363 370 10.1159/000323324 21422748 10.1159/000323324 1:CAS:528:DC%2BC3MXhtlWrtb7I