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Published in: European Journal of Applied Physiology 4/2009

01-11-2009 | Original Article

Resistance exercise-induced changes of inflammatory gene expression within human skeletal muscle

Authors: Thomas W. Buford, Matthew B. Cooke, Darryn S. Willoughby

Published in: European Journal of Applied Physiology | Issue 4/2009

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Abstract

Aberrant local inflammatory signaling within skeletal muscle is now considered a contributing factor to the development of sarcopenia. Recent evidence indicates that chronic resistance training contributes to the control of locally derived inflammation via adaptations to repeated, acute increases in pro-inflammatory mRNA within muscle. However, only a limited number of gene transcripts related to the inflammatory process have been examined in the literature. The present study utilized an acute bout to examine the effects of resistance exercise on several inflammatory-related genes in 24 physically active, post-menopausal women not currently undergoing hormone replacement therapy. Following a standard warm-up, participants completed a lower-body resistance exercise bout consisting of 3 sets of 10 repetitions on machine squat, leg press, and leg extension exercises (80% intensity). Muscle biopsies were obtained from the vastus lateralis of the dominant leg at baseline and 3 h following exercise. Significant (p < 0.05) up-regulation in mRNA content was observed for TNFα, IL1β, IL6, IL8, SOCS2, COX2, SAA1, SAA2, IKKB, cfos, and junB. Muscle mRNA content was not significantly altered at the 0.05 level for IL2, IL5, IL10, or IL12 (p35). Venous blood samples were also obtained at baseline as well as at 3, 24, and 48 h post-exercise. Serum was analyzed for circulating TNFα, IL1β, IL6, IL8, COX2, and SAA with no significant changes observed. These results indicate that resistance exercise is capable of up-regulating transcription of numerous inflammatory mediators within skeletal muscle, and these appear to be worthy of future examination in chronic studies.
Literature
go back to reference Akerstrom T, Steensberg A, Keller P, Keller C, Penkowa M, Pedersen BK (2005) Exercise induces interleukin-8 expression in human skeletal muscle. J Physiol 563:507–516CrossRefPubMed Akerstrom T, Steensberg A, Keller P, Keller C, Penkowa M, Pedersen BK (2005) Exercise induces interleukin-8 expression in human skeletal muscle. J Physiol 563:507–516CrossRefPubMed
go back to reference Badolato R, Johnston JA, Wang JM et al (1995) Serum amyloid A induces calcium mobilization and chemotaxis of human monocytes by activating a pertussis toxin-sensitive signaling pathway. J Immunol 155:4004–4010PubMed Badolato R, Johnston JA, Wang JM et al (1995) Serum amyloid A induces calcium mobilization and chemotaxis of human monocytes by activating a pertussis toxin-sensitive signaling pathway. J Immunol 155:4004–4010PubMed
go back to reference Bassey EJ, Fiatarone MA, O’Neill EF, Kelly M, Evans WJ, Lipsitz LA (1992) Leg extensor power and functional performance in very old men and women. Clin Sci (Lond) 82:321–327 Bassey EJ, Fiatarone MA, O’Neill EF, Kelly M, Evans WJ, Lipsitz LA (1992) Leg extensor power and functional performance in very old men and women. Clin Sci (Lond) 82:321–327
go back to reference Bickel CS, Slade J, Mahoney E, Haddad F, Dudley GA, Adams GR (2005) Time course of molecular responses of human skeletal muscle to acute bouts of resistance exercise. J Appl Physiol 98:482–488PubMed Bickel CS, Slade J, Mahoney E, Haddad F, Dudley GA, Adams GR (2005) Time course of molecular responses of human skeletal muscle to acute bouts of resistance exercise. J Appl Physiol 98:482–488PubMed
go back to reference Bondesen BA, Mills ST, Kegley KM, Pavlath GK (2004) The COX-2 pathway is essential during early stages of skeletal muscle regeneration. Am J Physiol Cell Physiol 287:C475–C483CrossRefPubMed Bondesen BA, Mills ST, Kegley KM, Pavlath GK (2004) The COX-2 pathway is essential during early stages of skeletal muscle regeneration. Am J Physiol Cell Physiol 287:C475–C483CrossRefPubMed
go back to reference Bondesen BA, Mills ST, Pavlath GK (2006) The COX-2 pathway regulates growth of atrophied muscle via multiple mechanisms. Am J Physiol Cell Physiol 290:C1651–C1659CrossRefPubMed Bondesen BA, Mills ST, Pavlath GK (2006) The COX-2 pathway regulates growth of atrophied muscle via multiple mechanisms. Am J Physiol Cell Physiol 290:C1651–C1659CrossRefPubMed
go back to reference Bruunsgaard H, Bjerregaard E, Schroll M, Pedersen BK (2004) Muscle strength after resistance training is inversely correlated with baseline levels of soluble tumor necrosis factor receptors in the oldest old. J Am Geriatr Soc 52:237–241CrossRefPubMed Bruunsgaard H, Bjerregaard E, Schroll M, Pedersen BK (2004) Muscle strength after resistance training is inversely correlated with baseline levels of soluble tumor necrosis factor receptors in the oldest old. J Am Geriatr Soc 52:237–241CrossRefPubMed
go back to reference Cheng M, Nguyen MH, Fantuzzi G, Koh TJ (2008) Endogenous interferon-{gamma} is required for efficient skeletal muscle regeneration. Am J Physiol Cell Physiol 294:C1183–C1191CrossRefPubMed Cheng M, Nguyen MH, Fantuzzi G, Koh TJ (2008) Endogenous interferon-{gamma} is required for efficient skeletal muscle regeneration. Am J Physiol Cell Physiol 294:C1183–C1191CrossRefPubMed
go back to reference Dirks AJ, Leeuwenburgh C (2006) Tumor necrosis factor alpha signaling in skeletal muscle: effects of age and caloric restriction. J Nutr Biochem 17:501–508CrossRefPubMed Dirks AJ, Leeuwenburgh C (2006) Tumor necrosis factor alpha signaling in skeletal muscle: effects of age and caloric restriction. J Nutr Biochem 17:501–508CrossRefPubMed
go back to reference Douchi T, Yamamoto S, Nakamura S et al (1998) The effect of menopause on regional and total body lean mass. Maturitas 29:247–252CrossRefPubMed Douchi T, Yamamoto S, Nakamura S et al (1998) The effect of menopause on regional and total body lean mass. Maturitas 29:247–252CrossRefPubMed
go back to reference Durham WJ, Li YP, Gerken E et al (2004) Fatiguing exercise reduces DNA binding activity of NF-kappaB in skeletal muscle nuclei. J Appl Physiol 97:1740–1745CrossRefPubMed Durham WJ, Li YP, Gerken E et al (2004) Fatiguing exercise reduces DNA binding activity of NF-kappaB in skeletal muscle nuclei. J Appl Physiol 97:1740–1745CrossRefPubMed
go back to reference Frontera WR, Hughes VA, Lutz KJ, Evans WJ (1991) A cross-sectional study of muscle strength and mass in 45- to 78-yr-old men and women. J Appl Physiol 71:644–650PubMed Frontera WR, Hughes VA, Lutz KJ, Evans WJ (1991) A cross-sectional study of muscle strength and mass in 45- to 78-yr-old men and women. J Appl Physiol 71:644–650PubMed
go back to reference Frost RA, Lang CH (2005) Skeletal muscle cytokines: regulation by pathogen-associated molecules and catabolic hormones. Curr Opin Clin Nutr Metab Care 8:255–263CrossRefPubMed Frost RA, Lang CH (2005) Skeletal muscle cytokines: regulation by pathogen-associated molecules and catabolic hormones. Curr Opin Clin Nutr Metab Care 8:255–263CrossRefPubMed
go back to reference Girasole G, Giuliani N, Modena AB, Passeri G, Pedrazzoni M (1999) Oestrogens prevent the increase of human serum soluble interleukin-6 receptor induced by ovariectomy in vivo and decrease its release in human osteoblastic cells in vitro. Clin Endocrinol (Oxf) 51:801–807CrossRef Girasole G, Giuliani N, Modena AB, Passeri G, Pedrazzoni M (1999) Oestrogens prevent the increase of human serum soluble interleukin-6 receptor induced by ovariectomy in vivo and decrease its release in human osteoblastic cells in vitro. Clin Endocrinol (Oxf) 51:801–807CrossRef
go back to reference Gower BA, Nyman L (2000) Associations among oral estrogen use, free testosterone concentration, and lean body mass among postmenopausal women. J Clin Endocrinol Metab 85:4476–4480CrossRefPubMed Gower BA, Nyman L (2000) Associations among oral estrogen use, free testosterone concentration, and lean body mass among postmenopausal women. J Clin Endocrinol Metab 85:4476–4480CrossRefPubMed
go back to reference Greeves JP, Cable NT, Reilly T, Kingsland C (1999) Changes in muscle strength in women following the menopause: a longitudinal assessment of the efficacy of hormone replacement therapy. Clin Sci (Lond) 97:79–84CrossRef Greeves JP, Cable NT, Reilly T, Kingsland C (1999) Changes in muscle strength in women following the menopause: a longitudinal assessment of the efficacy of hormone replacement therapy. Clin Sci (Lond) 97:79–84CrossRef
go back to reference Greiwe JS, Cheng B, Rubin DC, Yarasheski KE, Semenkovich CF (2001) Resistance exercise decreases skeletal muscle tumor necrosis factor alpha in frail elderly humans. FASEB J 15:475–482CrossRefPubMed Greiwe JS, Cheng B, Rubin DC, Yarasheski KE, Semenkovich CF (2001) Resistance exercise decreases skeletal muscle tumor necrosis factor alpha in frail elderly humans. FASEB J 15:475–482CrossRefPubMed
go back to reference Haddad F, Adams GR (2006) Aging-sensitive cellular and molecular mechanisms associated with skeletal muscle hypertrophy. J Appl Physiol 100:1188–1203CrossRefPubMed Haddad F, Adams GR (2006) Aging-sensitive cellular and molecular mechanisms associated with skeletal muscle hypertrophy. J Appl Physiol 100:1188–1203CrossRefPubMed
go back to reference Haddad F, Zaldivar F, Cooper DM, Adams GR (2005) IL-6-induced skeletal muscle atrophy. J Appl Physiol 98:911–917CrossRefPubMed Haddad F, Zaldivar F, Cooper DM, Adams GR (2005) IL-6-induced skeletal muscle atrophy. J Appl Physiol 98:911–917CrossRefPubMed
go back to reference Hamada K, Vannier E, Sacheck JM, Witsell AL, Roubenoff R (2005) Senescence of human skeletal muscle impairs the local inflammatory cytokine response to acute eccentric exercise. FASEB J 19:264–266PubMed Hamada K, Vannier E, Sacheck JM, Witsell AL, Roubenoff R (2005) Senescence of human skeletal muscle impairs the local inflammatory cytokine response to acute eccentric exercise. FASEB J 19:264–266PubMed
go back to reference Hayot M, Michaud A, Koechlin C et al (2005) Skeletal muscle microbiopsy: a validation study of a minimally invasive technique. Eur Respir J 25:431–440CrossRefPubMed Hayot M, Michaud A, Koechlin C et al (2005) Skeletal muscle microbiopsy: a validation study of a minimally invasive technique. Eur Respir J 25:431–440CrossRefPubMed
go back to reference Hershkoviz R, Preciado-Patt L, Lider O et al (1997) Extracellular matrix-anchored serum amyloid A preferentially induces mast cell adhesion. Am J Physiol 273:C179–C187PubMed Hershkoviz R, Preciado-Patt L, Lider O et al (1997) Extracellular matrix-anchored serum amyloid A preferentially induces mast cell adhesion. Am J Physiol 273:C179–C187PubMed
go back to reference Janssen I, Shepard DS, Katzmarzyk PT, Roubenoff R (2004) The healthcare costs of sarcopenia in the United States. J Am Geriatr Soc 52:80–85CrossRefPubMed Janssen I, Shepard DS, Katzmarzyk PT, Roubenoff R (2004) The healthcare costs of sarcopenia in the United States. J Am Geriatr Soc 52:80–85CrossRefPubMed
go back to reference Ji LL, Gomez-Cabrera MC, Steinhafel N, Vina J (2004) Acute exercise activates nuclear factor (NF)-kappaB signaling pathway in rat skeletal muscle. FASEB J 18:1499–1506CrossRefPubMed Ji LL, Gomez-Cabrera MC, Steinhafel N, Vina J (2004) Acute exercise activates nuclear factor (NF)-kappaB signaling pathway in rat skeletal muscle. FASEB J 18:1499–1506CrossRefPubMed
go back to reference Kandarian SC, Jackman RW (2006) Intracellular signaling during skeletal muscle atrophy. Muscle Nerve 33:155–165CrossRefPubMed Kandarian SC, Jackman RW (2006) Intracellular signaling during skeletal muscle atrophy. Muscle Nerve 33:155–165CrossRefPubMed
go back to reference Kovacevic A, Hammer A, Stadelmeyer E et al (2008) Expression of serum amyloid A transcripts in human bone tissues, differentiated osteoblast-like stem cells and human osteosarcoma cell lines. J Cell Biochem 103:994–1004CrossRefPubMed Kovacevic A, Hammer A, Stadelmeyer E et al (2008) Expression of serum amyloid A transcripts in human bone tissues, differentiated osteoblast-like stem cells and human osteosarcoma cell lines. J Cell Biochem 103:994–1004CrossRefPubMed
go back to reference Kramer PR, Kramer SF, Guan G (2004) 17 beta-estradiol regulates cytokine release through modulation of CD16 expression in monocytes and monocyte-derived macrophages. Arthritis Rheum 50:1967–1975CrossRefPubMed Kramer PR, Kramer SF, Guan G (2004) 17 beta-estradiol regulates cytokine release through modulation of CD16 expression in monocytes and monocyte-derived macrophages. Arthritis Rheum 50:1967–1975CrossRefPubMed
go back to reference Lambert CP, Wright NR, Finck BN, Villareal DT (2008) Exercise but not diet-induced weight loss decreases skeletal muscle inflammatory gene expression in frail obese elderly persons. J Appl Physiol 105:473–478CrossRefPubMed Lambert CP, Wright NR, Finck BN, Villareal DT (2008) Exercise but not diet-induced weight loss decreases skeletal muscle inflammatory gene expression in frail obese elderly persons. J Appl Physiol 105:473–478CrossRefPubMed
go back to reference Lexell J, Taylor CC, Sjostrom M (1988) What is the cause of the ageing atrophy? total number, size and proportion of different fiber types studied in whole vastus lateralis muscle from 15- to 83-year-old men. J Neurol Sci 84:275–294CrossRefPubMed Lexell J, Taylor CC, Sjostrom M (1988) What is the cause of the ageing atrophy? total number, size and proportion of different fiber types studied in whole vastus lateralis muscle from 15- to 83-year-old men. J Neurol Sci 84:275–294CrossRefPubMed
go back to reference Louis E, Raue U, Yang Y, Jemiolo B, Trappe S (2007) Time course of proteolytic, cytokine, and myostatin gene expression after acute exercise in human skeletal muscle. J Appl Physiol 103:1744–1751CrossRefPubMed Louis E, Raue U, Yang Y, Jemiolo B, Trappe S (2007) Time course of proteolytic, cytokine, and myostatin gene expression after acute exercise in human skeletal muscle. J Appl Physiol 103:1744–1751CrossRefPubMed
go back to reference Mahoney DJ, Carey K, Fu MH et al (2004) Real-time RT-PCR analysis of housekeeping genes in human skeletal muscle following acute exercise. Physiol Genomics 18:226–231CrossRefPubMed Mahoney DJ, Carey K, Fu MH et al (2004) Real-time RT-PCR analysis of housekeeping genes in human skeletal muscle following acute exercise. Physiol Genomics 18:226–231CrossRefPubMed
go back to reference Manton KG, Gu X (2001) Changes in the prevalence of chronic disability in the United States black and nonblack population above age 65 from 1982 to 1999. Proc Natl Acad Sci USA 98:6354–6359CrossRefPubMed Manton KG, Gu X (2001) Changes in the prevalence of chronic disability in the United States black and nonblack population above age 65 from 1982 to 1999. Proc Natl Acad Sci USA 98:6354–6359CrossRefPubMed
go back to reference Melton LJ 3rd, Khosla S, Crowson CS, O’Connor MK, O’Fallon WM, Riggs BL (2000) Epidemiology of sarcopenia. J Am Geriatr Soc 48:625–630PubMed Melton LJ 3rd, Khosla S, Crowson CS, O’Connor MK, O’Fallon WM, Riggs BL (2000) Epidemiology of sarcopenia. J Am Geriatr Soc 48:625–630PubMed
go back to reference Moore MJ (2005) From birth to death: the complex lives of eukaryotic mRNAs. Science 309:1514–1518CrossRefPubMed Moore MJ (2005) From birth to death: the complex lives of eukaryotic mRNAs. Science 309:1514–1518CrossRefPubMed
go back to reference Mourkioti F, Rosenthal N (2005) IGF-1, inflammation and stem cells: interactions during muscle regeneration. Trends Immunol 26:535–542CrossRefPubMed Mourkioti F, Rosenthal N (2005) IGF-1, inflammation and stem cells: interactions during muscle regeneration. Trends Immunol 26:535–542CrossRefPubMed
go back to reference Pelosi L, Giacinti C, Nardis C et al (2007) Local expression of IGF-1 accelerates muscle regeneration by rapidly modulating inflammatory cytokines and chemokines. FASEB J 21:1393–1402CrossRefPubMed Pelosi L, Giacinti C, Nardis C et al (2007) Local expression of IGF-1 accelerates muscle regeneration by rapidly modulating inflammatory cytokines and chemokines. FASEB J 21:1393–1402CrossRefPubMed
go back to reference Phillips SK, Rook KM, Siddle NC, Bruce SA, Woledge RC (1993) Muscle weakness in women occurs at an earlier age than in men, but strength is preserved by hormone replacement therapy. Clin Sci (Lond) 84:95–98 Phillips SK, Rook KM, Siddle NC, Bruce SA, Woledge RC (1993) Muscle weakness in women occurs at an earlier age than in men, but strength is preserved by hormone replacement therapy. Clin Sci (Lond) 84:95–98
go back to reference Pilegaard H, Ordway GA, Saltin B, Neufer PD (2000) Transcriptional regulation of gene expression in human skeletal muscle during recovery from exercise. Am J Physiol Endocrinol Metab 279:E806–E814PubMed Pilegaard H, Ordway GA, Saltin B, Neufer PD (2000) Transcriptional regulation of gene expression in human skeletal muscle during recovery from exercise. Am J Physiol Endocrinol Metab 279:E806–E814PubMed
go back to reference Plomgaard P, Penkowa M, Pedersen BK (2005) Fiber type specific expression of TNF-alpha, IL-6 and IL-18 in human skeletal muscles. Exerc Immunol Rev 11:53–63PubMed Plomgaard P, Penkowa M, Pedersen BK (2005) Fiber type specific expression of TNF-alpha, IL-6 and IL-18 in human skeletal muscles. Exerc Immunol Rev 11:53–63PubMed
go back to reference Puntschart A, Wey E, Jostarndt K et al (1998) Expression of fos and jun genes in human skeletal muscle after exercise. Am J Physiol 274:C129–C137PubMed Puntschart A, Wey E, Jostarndt K et al (1998) Expression of fos and jun genes in human skeletal muscle after exercise. Am J Physiol 274:C129–C137PubMed
go back to reference Rannevik G, Jeppsson S, Johnell O, Bjerre B, Laurell-Borulf Y, Svanberg L (2008) A longitudinal study of the perimenopausal transition: altered profiles of steroid and pituitary hormones, SHBG and bone mineral density. Maturitas 61:67–77CrossRefPubMed Rannevik G, Jeppsson S, Johnell O, Bjerre B, Laurell-Borulf Y, Svanberg L (2008) A longitudinal study of the perimenopausal transition: altered profiles of steroid and pituitary hormones, SHBG and bone mineral density. Maturitas 61:67–77CrossRefPubMed
go back to reference Rippy L, Marsden J (2006) Is HRT justified for symptom management in women at higher risk of developing breast cancer? Climacteric 9:404–415CrossRefPubMed Rippy L, Marsden J (2006) Is HRT justified for symptom management in women at higher risk of developing breast cancer? Climacteric 9:404–415CrossRefPubMed
go back to reference Steensberg A, van Hall G, Osada T, Sacchetti M, Saltin B, Klarlund Pedersen B (2000) Production of interleukin-6 in contracting human skeletal muscles can account for the exercise-induced increase in plasma interleukin-6. J Physiol 529(Pt 1):237–242CrossRefPubMed Steensberg A, van Hall G, Osada T, Sacchetti M, Saltin B, Klarlund Pedersen B (2000) Production of interleukin-6 in contracting human skeletal muscles can account for the exercise-induced increase in plasma interleukin-6. J Physiol 529(Pt 1):237–242CrossRefPubMed
go back to reference Taaffe DR, Luz Villa M, Delay R, Marcus R (1995) Maximal muscle strength of elderly women is not influenced by oestrogen status. Age Ageing 24:329–333CrossRefPubMed Taaffe DR, Luz Villa M, Delay R, Marcus R (1995) Maximal muscle strength of elderly women is not influenced by oestrogen status. Age Ageing 24:329–333CrossRefPubMed
go back to reference Visser M, Pahor M, Taaffe DR et al (2002) Relationship of interleukin-6 and tumor necrosis factor-alpha with muscle mass and muscle strength in elderly men and women: the Health ABC Study. J Gerontol A Biol Sci Med Sci 57:M326–M332PubMed Visser M, Pahor M, Taaffe DR et al (2002) Relationship of interleukin-6 and tumor necrosis factor-alpha with muscle mass and muscle strength in elderly men and women: the Health ABC Study. J Gerontol A Biol Sci Med Sci 57:M326–M332PubMed
go back to reference Willoughby DS (2004) Effects of heavy resistance training on myostatin mRNA and protein expression. Med Sci Sports Exerc 36:574–582CrossRefPubMed Willoughby DS (2004) Effects of heavy resistance training on myostatin mRNA and protein expression. Med Sci Sports Exerc 36:574–582CrossRefPubMed
go back to reference Willoughby DS, Stout JR, Wilborn CD (2007) Effects of resistance training and protein plus amino acid supplementation on muscle anabolism, mass, and strength. Amino Acids 32:467–477CrossRefPubMed Willoughby DS, Stout JR, Wilborn CD (2007) Effects of resistance training and protein plus amino acid supplementation on muscle anabolism, mass, and strength. Amino Acids 32:467–477CrossRefPubMed
go back to reference World Health Organization (1981) Research on the menopause. World Health Organ Tech Rep Ser 670:1–120 World Health Organization (1981) Research on the menopause. World Health Organ Tech Rep Ser 670:1–120
go back to reference Yang Y, Creer A, Jemiolo B, Trappe S (2005) Time course of myogenic and metabolic gene expression in response to acute exercise in human skeletal muscle. J Appl Physiol 98:1745–1752CrossRefPubMed Yang Y, Creer A, Jemiolo B, Trappe S (2005) Time course of myogenic and metabolic gene expression in response to acute exercise in human skeletal muscle. J Appl Physiol 98:1745–1752CrossRefPubMed
Metadata
Title
Resistance exercise-induced changes of inflammatory gene expression within human skeletal muscle
Authors
Thomas W. Buford
Matthew B. Cooke
Darryn S. Willoughby
Publication date
01-11-2009
Publisher
Springer-Verlag
Published in
European Journal of Applied Physiology / Issue 4/2009
Print ISSN: 1439-6319
Electronic ISSN: 1439-6327
DOI
https://doi.org/10.1007/s00421-009-1145-z

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