Changes in plasma hydroxyproline and plasma cell-free DNA concentrations after higher- versus lower-intensity eccentric cycling.

Connective tissue Delayed onset muscle soreness Eccentric exercise Extracellular matrix Maximal voluntary isometric contraction Muscle damage

Journal

European journal of applied physiology
ISSN: 1439-6327
Titre abrégé: Eur J Appl Physiol
Pays: Germany
ID NLM: 100954790

Informations de publication

Date de publication:
Apr 2021
Historique:
received: 30 10 2020
accepted: 18 12 2020
pubmed: 14 1 2021
medline: 27 10 2021
entrez: 13 1 2021
Statut: ppublish

Résumé

We examined changes in plasma creatine kinase (CK) activity, hydroxyproline and cell-free DNA (cfDNA) concentrations in relation to changes in maximum voluntary isometric contraction (MVIC) torque and delayed-onset muscle soreness (DOMS) following a session of volume-matched higher- (HI) versus lower-intensity (LI) eccentric cycling exercise. Healthy young men performed either 5 × 1-min HI at 20% of peak power output (n = 11) or 5 × 4-min LI eccentric cycling at 5% of peak power output (n = 9). Changes in knee extensor MVIC torque, DOMS, plasma CK activity, and hydroxyproline and cfDNA concentrations before, immediately after, and 24-72 h post-exercise were compared between groups. Plasma CK activity increased post-exercise (141 ± 73.5%) and MVIC torque decreased from immediately (13.3 ± 7.8%) to 48 h (6.7 ± 13.5%) post-exercise (P < 0.05), without significant differences between groups. DOMS was greater after HI (peak: 4.5 ± 3.0 on a 10-point scale) than LI (1.2 ± 1.0). Hydroxyproline concentration increased 40-53% at 24-72 h after both LI and HI (P < 0.05). cfDNA concentration increased immediately after HI only (2.3 ± 0.9-fold, P < 0.001), with a significant difference between groups (P = 0.002). Lack of detectable methylated HOXD4 indicated that the cfDNA was not derived from skeletal muscle. No significant correlations were evident between the magnitude of change in the measures, but the cfDNA increase immediately post-exercise was correlated with the maximal change in heart rate during exercise (r = 0.513, P = 0.025). Changes in plasma hydroxyproline and cfDNA concentrations were not associated with muscle fiber damage, but the increased hydroxyproline in both groups suggests increased collagen turnover. cfDNA may be a useful metabolic-intensity exercise marker.

Identifiants

pubmed: 33439308
doi: 10.1007/s00421-020-04593-1
pii: 10.1007/s00421-020-04593-1
doi:

Substances chimiques

Cell-Free Nucleic Acids 0
Creatine Kinase EC 2.7.3.2
Hydroxyproline RMB44WO89X

Types de publication

Comparative Study Journal Article Randomized Controlled Trial

Langues

eng

Sous-ensembles de citation

IM

Pagination

1087-1097

Références

Andreatta MV, Curty VM, Coutinho JVS et al (2018) Cell-free DNA as an earlier predictor of exercise-induced performance decrement related to muscle damage. Int J Sports Physiol Perform 13:953–956. https://doi.org/10.1123/ijspp.2017-0421
doi: 10.1123/ijspp.2017-0421 pubmed: 29182414
Atamaniuk J, Vidotto C, Tschan H et al (2004) Increased concentrations of cell-free plasma DNA after exhaustive exercise. Clin Chem 50:1668–1670. https://doi.org/10.1373/clinchem.2004.034553
doi: 10.1373/clinchem.2004.034553 pubmed: 15331502
Atamaniuk J, Stuhlmeier KM, Vidotto C et al (2008) Effects of ultra-marathon on circulating DNA and mRNA expression of pro- and anti-apoptotic genes in mononuclear cells. Eur J Appl Physiol 104:711–717. https://doi.org/10.1007/s00421-008-0827-2
doi: 10.1007/s00421-008-0827-2 pubmed: 18651163
Atamaniuk J, Vidotto C, Kinzlbauer M et al (2010) Cell-free plasma DNA and purine nucleotide degradation markers following weightlifting exercise. Eur J Appl Physiol 110:695–701. https://doi.org/10.1007/s00421-010-1532-5
doi: 10.1007/s00421-010-1532-5 pubmed: 20577758
Beiter T, Fragasso A, Hudemann J et al (2011) Short-term treadmill running as a model for studying cell-free DNA kinetics in vivo. Clin Chem 57:633–636. https://doi.org/10.1373/clinchem.2010.158030
doi: 10.1373/clinchem.2010.158030 pubmed: 21296972
Beiter T, Fragasso A, Hudemann J et al (2014) Neutrophils release extracellular DNA traps in response to exercise. J Appl Physiol 117:325–333. https://doi.org/10.1152/japplphysiol.00173.2014
doi: 10.1152/japplphysiol.00173.2014 pubmed: 24833781
Beiter T, Fragasso A, Hartl D, Nieß AM (2015) Neutrophil extracellular traps: a walk on the wild side of exercise immunology. Sports Med 45:625–640. https://doi.org/10.1007/s40279-014-0296-1
doi: 10.1007/s40279-014-0296-1 pubmed: 25504501
Borg G (1998) Borg’s perceived exertion and pain scales. Human Kinetics, Champaign
Breitbach S, Tug S, Simon P (2012) Circulating cell-free DNA: an up-coming molecular marker in exercise physiology. Sports Med 42:565–586. https://doi.org/10.2165/11631380-000000000-00000
doi: 10.2165/11631380-000000000-00000 pubmed: 22694348
Breitbach S, Sterzing B, Magallanes C et al (2014) Direct measurement of cell-free DNA from serially collected capillary plasma during incremental exercise. J Appl Physiol 117:119–130. https://doi.org/10.1152/japplphysiol.00002.2014
doi: 10.1152/japplphysiol.00002.2014 pubmed: 24876361
Brown SJ, Child RB, Day SH, Donnelly AE (1997) Indices of skeletal muscle damage and connective tissue breakdown following eccentric muscle contractions. Eur J Appl Physiol Occup Physiol 75:369–374. https://doi.org/10.1007/s004210050174
doi: 10.1007/s004210050174 pubmed: 9134370
Brown S, Day S, Donnelly A (1999) Indirect evidence of human skeletal muscle damage and collagen breakdown after eccentric muscle actions. J Sports Sci 17:397–402. https://doi.org/10.1080/026404199365911
doi: 10.1080/026404199365911 pubmed: 10413267
Clarkson PM, Nosaka K, Braun B (1992) Muscle function after exercise-induced muscle damage and rapid adaptation. Med Sci Sports Exerc 24:512–520. https://doi.org/10.1249/00005768-199205000-00004
doi: 10.1249/00005768-199205000-00004 pubmed: 1569847
Crameri RM, Aagaard P, Qvortrup K et al (2007) Myofibre damage in human skeletal muscle: effects of electrical stimulation versus voluntary contraction. J Physiol 583:365–380. https://doi.org/10.1113/jphysiol.2007.128827
doi: 10.1113/jphysiol.2007.128827 pubmed: 17584833 pmcid: 2277245
Ehrlich M, Lacey M (2013) DNA methylation and differentiation: silencing, upregulation and modulation of gene expression. Epigenomics 5:553–568. https://doi.org/10.2217/epi.13.43
doi: 10.2217/epi.13.43 pubmed: 24059801
Fatouros IG, Jamurtas AZ, Nikolaidis MG et al (2010) Time of sampling is crucial for measurement of cell-free plasma DNA following acute aseptic inflammation induced by exercise. Clin Biochem 43:1368–1370. https://doi.org/10.1016/j.clinbiochem.2010.08.020
doi: 10.1016/j.clinbiochem.2010.08.020 pubmed: 20800058
Ferrandi PJ, Fico BG, Whitehurst M et al (2018) Acute high-intensity interval exercise induces comparable levels of circulating cell-free DNA and Interleukin-6 in obese and normal-weight individuals. Life Sci 202:161–166. https://doi.org/10.1016/j.lfs.2018.04.007
doi: 10.1016/j.lfs.2018.04.007 pubmed: 29653118
Frühbeis C, Helmig S, Tug S et al (2015) Physical exercise induces rapid release of small extracellular vesicles into the circulation. J Extracell Vesicles 4:28239. https://doi.org/10.3402/jev.v4.28239
doi: 10.3402/jev.v4.28239 pubmed: 26142461
Grounds MD, Sorokin L, White J (2005) Strength at the extracellular matrix-muscle interface. Scand J Med Sci Sports 15:381–391. https://doi.org/10.1111/j.1600-0838.2005.00467.x
doi: 10.1111/j.1600-0838.2005.00467.x pubmed: 16293150
Haller N, Tug S, Breitbach S et al (2017) Increases in circulating cell-free DNA during aerobic running depend on intensity and duration. Int J Sports Physiol Perform 12:455–462. https://doi.org/10.1123/ijspp.2015-0540
doi: 10.1123/ijspp.2015-0540 pubmed: 27617389
Haller N, Helmig S, Taenny P et al (2018) Circulating, cell-free DNA as a marker for exercise load in intermittent sports. PLoS ONE 13:e0191915. https://doi.org/10.1371/journal.pone.0191915
doi: 10.1371/journal.pone.0191915 pubmed: 29370268 pmcid: 5784997
Helmig S, Frühbeis C, Krämer-Albers E-M et al (2015) Release of bulk cell free DNA during physical exercise occurs independent of extracellular vesicles. Eur J Appl Physiol 115:2271–2280. https://doi.org/10.1007/s00421-015-3207-8
doi: 10.1007/s00421-015-3207-8 pubmed: 26126838
Julian V, Thivel D, Costes F et al (2018) Eccentric training improves body composition by inducing mechanical and metabolic adaptations: a promising approach for overweight and obese individuals. Front Physiol. https://doi.org/10.3389/fphys.2018.01013
doi: 10.3389/fphys.2018.01013 pubmed: 30131705 pmcid: 6090036
Kish K, Mezil Y, Ward WE et al (2015) Effects of plyometric exercise session on markers of bone turnover in boys and young men. Eur J Appl Physiol 115:2115–2124. https://doi.org/10.1007/s00421-015-3191-z
doi: 10.1007/s00421-015-3191-z pubmed: 26016944
Koskinen SOA, Ahtikoski AM, Komulainen J et al (2002) Short-term effects of forced eccentric contractions on collagen synthesis and degradation in rat skeletal muscle. Pflügers Arch 444:59–72. https://doi.org/10.1007/s00424-002-0792-2
doi: 10.1007/s00424-002-0792-2 pubmed: 11976917
Kotch FW, Guzei IA, Raines RT (2008) Stabilization of the collagen triple helix by o-methylation of hydroxyproline residues. J Am Chem Soc 130:2952–2953. https://doi.org/10.1021/ja800225k
doi: 10.1021/ja800225k pubmed: 18271593 pmcid: 2802593
LaStayo PC, Pierotti DJ, Pifer J et al (2000) Eccentric ergometry: increases in locomotor muscle size and strength at low training intensities. Am J Physiol Regul Integr Comp Physiol 278:R1282-1288. https://doi.org/10.1152/ajpregu.2000.278.5.R1282
doi: 10.1152/ajpregu.2000.278.5.R1282 pubmed: 10801298
Maïmoun L, Manetta J, Couret I et al (2006) The intensity level of physical exercise and the bone metabolism response. Int J Sports Med 27:105–111. https://doi.org/10.1055/s-2005-837621
doi: 10.1055/s-2005-837621 pubmed: 16475055
Mavropalias G, Koeda T, Barley OR et al (2020) Comparison between high- and low-intensity eccentric cycling of equal mechanical work for muscle damage and the repeated bout effect. Eur J Appl Physiol 120:1015–1025. https://doi.org/10.1007/s00421-020-04341-5
doi: 10.1007/s00421-020-04341-5 pubmed: 32170443
Murguia MJ, Vailas A, Mandelbaum B et al (1988) Elevated plasma hydroxyproline. A possible risk factor associated with connective tissue injuries during overuse. Am J Sports Med 16:660–664. https://doi.org/10.1177/036354658801600619
doi: 10.1177/036354658801600619 pubmed: 3239623
Paschalis V, Koutedakis Y, Jamurtas AZ et al (2005) Equal volumes of high and low intensity of eccentric exercise in relation to muscle damage and performance. J Strength Cond Res 19:184–188. https://doi.org/10.1519/R-14763.1
doi: 10.1519/R-14763.1 pubmed: 15705032
Paulsen G, Crameri R, Benestad HB et al (2010) Time course of leukocyte accumulation in human muscle after eccentric exercise. Med Sci Sports Exerc 42:75–85. https://doi.org/10.1249/MSS.0b013e3181ac7adb
doi: 10.1249/MSS.0b013e3181ac7adb pubmed: 20010127
Peñailillo L, Blazevich A, Numazawa H, Nosaka K (2013) Metabolic and muscle damage profiles of concentric versus repeated eccentric cycling. Med Sci Sports Exerc 45:1773–1781. https://doi.org/10.1249/MSS.0b013e31828f8a73
doi: 10.1249/MSS.0b013e31828f8a73 pubmed: 23475167
Peñailillo L, Mackay K, Abbiss CR (2018) Rating of perceived exertion during concentric and eccentric cycling: are we measuring effort or exertion? Int J Sports Physiol Perform 13:517–523. https://doi.org/10.1123/ijspp.2017-0171
doi: 10.1123/ijspp.2017-0171 pubmed: 29035598
Stawski R, Walczak K, Kosielski P et al (2017) Repeated bouts of exhaustive exercise increase circulating cell free nuclear and mitochondrial DNA without development of tolerance in healthy men. PLoS ONE 12:e0178216. https://doi.org/10.1371/journal.pone.0178216
doi: 10.1371/journal.pone.0178216 pubmed: 28542490 pmcid: 5443547
Tofas T, Jamurtas AZ, Fatouros I et al (2008) Plyometric exercise increases serum indices of muscle damage and collagen breakdown. J Strength Cond Res 22:490–496. https://doi.org/10.1519/JSC.0b013e31816605a0
doi: 10.1519/JSC.0b013e31816605a0 pubmed: 18550965
Tug S, Helmig S, Deichmann ER et al (2015) Exercise-induced increases in cell free DNA in human plasma originate predominantly from cells of the haematopoietic lineage. Exerc Immunol Rev 21:164–173
pubmed: 25826002
Tug S, Mehdorn M, Helmig S et al (2017a) Exploring the potential of cell-free-DNA measurements after an exhaustive cycle-ergometer test as a marker for performance-related parameters. Int J Sports Physiol Perform 12:597–604. https://doi.org/10.1123/ijspp.2016-0157
doi: 10.1123/ijspp.2016-0157 pubmed: 27617485
Tug S, Tross A-K, Hegen P et al (2017b) Acute effects of strength exercises and effects of regular strength training on cell free DNA concentrations in blood plasma. PLoS ONE 12:e0184668. https://doi.org/10.1371/journal.pone.0184668
doi: 10.1371/journal.pone.0184668 pubmed: 28910365 pmcid: 5599009
Velders M, Treff G, Machus K et al (2014) Exercise is a potent stimulus for enhancing circulating DNase activity. Clin Biochem 47:471–474. https://doi.org/10.1016/j.clinbiochem.2013.12.017
doi: 10.1016/j.clinbiochem.2013.12.017 pubmed: 24373926
Virtanen P, Viitasalo JT, Vuori J et al (1993) Effect of concentric exercise on serum muscle and collagen markers. J Appl Physiol 75:1272–1277. https://doi.org/10.1152/jappl.1993.75.3.1272
doi: 10.1152/jappl.1993.75.3.1272 pubmed: 8226540
Wobbrock JO, Findlater L, Gergle D, Higgins JJ (2011) The aligned rank transform for nonparametric factorial analyses using only ANOVA procedures. In: CHI 2011—29th Annual CHI Conference on Human Factors in Computing Systems, Conference Proceedings and Extended Abstracts. Vancouver, BC, Canada, pp 143–146
Woodward MI, Cunningham JL (1993) Skeletal accelerations measured during different exercises. Proc Inst Mech Eng H 207:79–85. https://doi.org/10.1243/PIME_PROC_1993_207_274_02
doi: 10.1243/PIME_PROC_1993_207_274_02 pubmed: 8280317

Auteurs

Georgios Mavropalias (G)

School of Medical and Health Sciences, Edith Cowan University, Joondalup, Australia. georgios.mavropalias@gmail.com.
Exercise Medicine Research Institute, Edith Cowan University, Joondalup, Australia. georgios.mavropalias@gmail.com.

Leslie Calapre (L)

School of Medical and Health Sciences, Edith Cowan University, Joondalup, Australia.

Michael Morici (M)

School of Medical and Health Sciences, Edith Cowan University, Joondalup, Australia.

Tomoko Koeda (T)

Faculty of Rehabilitation Sciences, Nagoya Gakuin University, Nagoya, Japan.

Wayne C K Poon (WCK)

School of Medical and Health Sciences, Edith Cowan University, Joondalup, Australia.

Oliver R Barley (OR)

School of Medical and Health Sciences, Edith Cowan University, Joondalup, Australia.

Elin Gray (E)

School of Medical and Health Sciences, Edith Cowan University, Joondalup, Australia.

Anthony J Blazevich (AJ)

School of Medical and Health Sciences, Edith Cowan University, Joondalup, Australia.

Kazunori Nosaka (K)

School of Medical and Health Sciences, Edith Cowan University, Joondalup, Australia.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH