Exploring the Impact of Astaxanthin Supplementation in Conjunction with a 12-Week CrossFit Training Regimen on Selected Adipo-Myokines Levels in Obese Males
Abstract
:1. Introduction
2. Methods
3. Experimental Design
4. Training Protocols
5. Supplementation of Astaxanthin and Placebo
6. Nutrient Intake and Dietary Analysis
7. Blood Markers
- The plasma concentrations of TGF-β, decorin, myostatin, follistatin, and myostatin were measured with the R&D Systems (Boston Biochem, Boston, MA, USA) enzyme-linked immunosorbent assay (ELISA) kits.
- According to the R&D Systems guidelines, plasma activin A was quantified using ELISA (R&D Systems DAC00B) with intra- and inter-assay coefficients of variation less than 5%.
8. Statistical Analysis
- The threshold for establishing statistical significance was a p-value of less than 0.05.
- All the data were characterized using descriptive statistics, which are expressed as means ± standard deviation. The Shapiro/Wilk test was utilized to assess the normality of the data distribution.
- An ANOVA repeated measures test conducted in two ways was used to determine the group × time interaction.
- One-way ANOVA was used to evaluate the baseline data for each of the four groups, and Fisher LSD post hoc tests were used. Pairwise comparisons were used to ascertain mean differences in the cases where an ANOVA indicated a significant difference.
- Classified as trivial (<0.2), small (0.2–0.6), moderate (0.6–1.2), large (1.2–2.0), and very large (2.0–4.0). ESs were given as partial eta-squared.
9. Results
10. Discussion
11. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Tan, C.K.; Chong, H.C.; Tan, E.H.P.; Tan, N.S. Getting ‘Smad’ about obesity and diabetes. Nutr. Diabetes 2012, 2, e29. [Google Scholar] [CrossRef] [PubMed]
- Crewe, C.; An, Y.A.; Scherer, P.E. The ominous triad of adipose tissue dysfunction: Inflammation, fibrosis, and impaired angiogenesis. J. Clin. Investig. 2017, 127, 74–82. [Google Scholar] [CrossRef] [PubMed]
- Lee, Y.S.; Wollam, J.; Olefsky, J.M. An Integrated View of Immunometabolism. Cell 2018, 172, 22–40. [Google Scholar] [CrossRef] [PubMed]
- Patsouris, D.; Li, P.-P.; Thapar, D.; Chapman, J.; Olefsky, J.M.; Neels, J.G. Ablation of CD11c-positive cells normalizes insulin sensitivity in obese insulin resistant animals. Cell Metab. 2008, 8, 301–309. [Google Scholar] [CrossRef]
- Kahn, S.E.; Hull, R.L.; Utzschneider, K.M. Mechanisms linking obesity to insulin resistance and type 2 diabetes. Nature 2006, 444, 840–846. [Google Scholar] [CrossRef] [PubMed]
- Costamagna, D.; Costelli, P.; Sampaolesi, M.; Penna, F. Role of inflammation in muscle homeostasis and myogenesis. Mediat. Inflamm. 2015, 2015, 1–14. [Google Scholar] [CrossRef]
- Chen, W.; Wang, L.; You, W.; Shan, T. Myokines mediate the cross talk between skeletal muscle and other organs. J. Cell. Physiol. 2020, 236, 2393–2412. [Google Scholar] [CrossRef]
- Lee, M.-J. Transforming growth factor beta superfamily regulation of adipose tissue biology in obesity. Biochim. Biophys. Acta (BBA) Mol. Basis Dis. 2018, 1864, 1160–1171. [Google Scholar] [CrossRef]
- Allen, D.L.; Cleary, A.S.; Speaker, K.J.; Lindsay, S.F.; Uyenishi, J.; Reed, J.M.; Madden, M.C.; Mehan, R.S. Myostatin, activin receptor IIb, and follistatin-like-3 gene expression are altered in adipose tissue and skeletal muscle of obese mice. Am. J. Physiol. Metab. 2008, 294, E918–E927. [Google Scholar] [CrossRef]
- Hittel, D.S.; Berggren, J.R.; Shearer, J.; Boyle, K.; Houmard, J.A. Increased secretion and expression of myostatin in skeletal muscle from extremely obese women. Diabetes 2009, 58, 30–38. [Google Scholar] [CrossRef]
- Samad, F.; Yamamoto, K.; Pandey, M.; Loskutoff, D.J. Elevated expression of transforming growth factor-β in adipose tissue from obese mice. Mol. Med. 1997, 3, 37–48. [Google Scholar] [CrossRef] [PubMed]
- Hedger, M.P.; Winnall, W.R.; Phillips, D.J.; de Kretser, D.M. The regulation and functions of activin and follistatin in inflammation and immunity. Vitam. Horm. 2011, 85, 255–297. [Google Scholar] [PubMed]
- Silva, R.N.; Bueno, P.; Avó, L.; Nonaka, K.; Selistre-Araújo, H.; Leal, A. Effect of physical training on liver expression of activin A and follistatin in a nonalcoholic fatty liver disease model in rats. Braz. J. Med. Biol. Res. 2014, 47, 746–752. [Google Scholar] [CrossRef]
- Karagiannidis, C.; Hense, G.; Martin, C.; Epstein, M.; Ruckert, B.; Mantel, P.; Menz, G.; Uhlig, S.; Blaser, K.; Schmidtweber, C. Activin A is an acute allergen-responsive cytokine and provides a link to TGF-β–mediated airway remodeling in asthma. J. Allergy Clin. Immunol. 2006, 117, 111–118. [Google Scholar] [CrossRef] [PubMed]
- Lin, Y.; Nakachi, K.; Ito, Y.; Kikuchi, S.; Tamakoshi, A.; Yagyu, K.; Kazuo Tajima for the JACC Study Group. Variations in serum transforming growth factor-β1 levels with gender, age and lifestyle factors of healthy Japanese adults. Dis. Markers 2009, 27, 23–28. [Google Scholar] [CrossRef] [PubMed]
- Lyons, J.-A.; Haring, J.S.; Biga, P.R. Myostatin expression, lymphocyte population, and potential cytokine production correlate with predisposition to high-fat diet induced obesity in mice. PLoS ONE 2010, 5, e12928. [Google Scholar] [CrossRef]
- Han, H.; Zhou, X.; Mitch, W.E.; Goldberg, A.L. Myostatin/activin pathway antagonism: Molecular basis and therapeutic potential. Int. J. Biochem. Cell Biol. 2013, 45, 2333–2347. [Google Scholar] [CrossRef]
- Zamani, N.; Brown, C.W. Emerging roles for the transforming growth factor-β superfamily in regulating adiposity and energy expenditure. Endocr. Rev. 2011, 32, 387–403. [Google Scholar] [CrossRef]
- Srivastava, R.K.; Sim, E.; Sheng, N.C.; Ibáñez, C.F.; Lee, E.-S. Sustained anti-obesity effects of life-style change and anti-inflammatory interventions after conditional inactivation of the activin receptor ALK7. ASEB J. 2021, 35, e21759. [Google Scholar] [CrossRef]
- Fournier, B.; Murray, B.; Gutzwiller, S.; Marcaletti, S.; Marcellin, D.; Bergling, S.; Brachat, S.; Persohn, E.; Pierrel, E.; Bombard, F.; et al. Blockade of the activin receptor IIb activates functional brown adipogenesis and thermogenesis by inducing mitochondrial oxidative metabolism. Mol. Cell. Biol. 2012, 32, 2871–2879. [Google Scholar] [CrossRef] [PubMed]
- Dutra, D.B.; Bueno, P.G.; Silva, R.N.; Nakahara, N.H.; Selistre-Araújo, H.S.; O Nonaka, K.; Leal, A.M. Expression of myostatin, myostatin receptors and follistatin in diabetic rats submitted to exercise. Clin. Exp. Pharmacol. Physiol. 2012, 39, 417–422. [Google Scholar] [CrossRef] [PubMed]
- Bolton, K.; Segal, D.; McMillan, J.; Jowett, J.; Heilbronn, L.; Abberton, K.; Zimmet, P.; Chisholm, D.; Collier, G.; Walder, K. Decorin is a secreted protein associated with obesity and type 2 diabetes. Int. J. Obes. 2008, 32, 1113–1121. [Google Scholar] [CrossRef] [PubMed]
- Sylow, L.; Vind, B.F.; Kruse, R.; Møller, P.M.; Wojtaszewski, J.F.P.; A Richter, E.; Højlund, K. Circulating follistatin and activin A and their regulation by insulin in obesity and type 2 diabetes. J. Clin. Endocrinol. Metab. 2020, 105, 1343–1354. [Google Scholar] [CrossRef] [PubMed]
- Singh, R.; Pervin, S.; Lee, S.-J.; Kuo, A.; Grijalva, V.; David, J.; Vergnes, L.; Reddy, S.T. Metabolic profiling of follistatin overexpression: A novel therapeutic strategy for metabolic diseases. Diabetes Metab. Syndr. Obesity Targets Ther. 2018, 11, 65–84. [Google Scholar] [CrossRef]
- Amthor, H.; Nicholas, G.; McKinnell, I.; Kemp, C.F.; Sharma, M.; Kambadur, R.; Patel, K. Follistatin complexes Myostatin and antagonises Myostatin-mediated inhibition of myogenesis. Dev. Biol. 2004, 270, 19–30. [Google Scholar] [CrossRef]
- Heinemeier, K.M.; Bjerrum, S.S.; Schjerling, P.; Kjaer, M. Expression of extracellular matrix components and related growth factors in human tendon and muscle after acute exercise. Scand. J. Med. Sci. Sports 2013, 23, e150–e161. [Google Scholar] [CrossRef] [PubMed]
- Kishioka, Y.; Thomas, M.; Wakamatsu, J.; Hattori, A.; Sharma, M.; Kambadur, R.; Nishimura, T. Decorin enhances the proliferation and differentiation of myogenic cells through suppressing myostatin activity. J. Cell. Physiol. 2007, 215, 856–867. [Google Scholar] [CrossRef]
- Li, X.; McFarland, D.C.; Velleman, S.G. Extracellular matrix proteoglycan decorin-mediated myogenic satellite cell responsiveness to transforming growth factor-β1 during cell proliferation and differentiation: Decorin and transforming growth factor-β1 in satellite cells. Domest. Anim. Endocrinol. 2008, 35, 263–273. [Google Scholar] [CrossRef]
- Kanzleiter, T.; Rath, M.; Görgens, S.W.; Jensen, J.; Tangen, D.S.; Kolnes, A.J.; Kolnes, K.J.; Lee, S.; Eckel, J.; Schürmann, A.; et al. The myokine decorin is regulated by contraction and involved in muscle hypertrophy. Biochem. Biophys. Res. Commun. 2014, 450, 1089–1094. [Google Scholar] [CrossRef]
- Hansen, J.; Brandt, C.; Nielsen, A.R.; Hojman, P.; Whitham, M.; Febbraio, M.A.; Pedersen, B.K.; Plomgaard, P. Exercise induces a marked increase in plasma follistatin: Evidence that follistatin is a contraction-induced hepatokine. Endocrinology 2011, 152, 164–171. [Google Scholar] [CrossRef] [PubMed]
- Tsuchida, K. Myokines and signal crosstalk between skeletal muscle and adipose tissue. Austin. J. Endocrinol. Diabetes 2014, 1, 1013. [Google Scholar]
- Schlegel, P. CrossFit® training strategies from the perspective of concurrent training: A systematic review. J. Sports Sci. Med. 2020, 19, 670. [Google Scholar] [PubMed]
- Tibana, R.A.; De Almeida, L.M.; Frade de Sousa, N.M.; Nascimento Dda, C.; Neto, I.V.; De Almeida, J.A.; Prestes, J. Two consecutive days of crossfit training affects pro and anti-inflammatory cytokines and osteoprotegerin without impairments in muscle power. Front. Physiol. 2016, 7, 260. [Google Scholar] [CrossRef]
- Perciavalle, V.; Marchetta, N.S.; Giustiniani, S.; Borbone, C.; Perciavalle, V.; Petralia, M.C.; Coco, M. Attentive processes, blood lactate and CrossFit®. Physician Sportsmed. 2016, 44, 403–406. [Google Scholar] [CrossRef] [PubMed]
- Timón, R.; Olcina, G.; Camacho-Cardeñosa, M.; Camacho-Cardenosa, A.; Martinez-Guardado, I.; Marcos-Serrano, M. 48-hour recovery of biochemical parameters and physical performance after two modalities of CrossFit workouts. Biol. Sport 2019, 36, 283–289. [Google Scholar] [CrossRef]
- Mangine, G.T.; Van Dusseldorp, T.A.; Feito, Y.; Holmes, A.J.; Serafini, P.R.; Box, A.G.; Gonzalez, A.M. Testosterone and cortisol responses to five high-intensity functional training competition workouts in recreationally active adults. Sports 2018, 6, 62. [Google Scholar] [CrossRef] [PubMed]
- Aoi, W.; Naito, Y.; Takanami, Y.; Ishii, T.; Kawai, Y.; Akagiri, S.; Kato, Y.; Osawa, T.; Yoshikawa, T. Astaxanthin improves muscle lipid metabolism in exercise via inhibitory effect of oxidative CPT I modification. Biophys. Res. Commun. 2008, 366, 892–897. [Google Scholar] [CrossRef]
- Xia, W.; Tang, N.; Kord-Varkaneh, H.; Low, T.Y.; Tan, S.C.; Wu, X.; Zhu, Y. The effects of astaxanthin supplementation on obesity, blood pressure, CRP, glycemic biomarkers, and lipid profile: A meta-analysis of randomized controlled trials. Pharmacol. Res. 2020, 161, 105113. [Google Scholar] [CrossRef]
- Saeidi, A.; Saei, M.A.; Mohammadi, B.; Zarei HR, A.; Vafaei, M.; Mohammadi, A.S.; Zouhal, H. Supplementation with spinach-derived thylakoid augments the benefits of high intensity training on adipokines, insulin resistance and lipid profiles in males with obesity. Front. Endocrinol. 2023, 14, 1141796. [Google Scholar] [CrossRef]
- Supriya, R.; Shishvan, S.R.; Kefayati, M.; Abednatanzi, H.; Razi, O.; Bagheri, R.; Escobar, K.A.; Pashaei, Z.; Saeidi, A.; Shahrbanian, S.; et al. Astaxanthin Supplementation Augments the Benefits of CrossFit Workouts on Semaphorin 3C and Other Adipokines in Males with Obesity. Nutrients 2023, 15, 4803. [Google Scholar] [CrossRef]
- Dani, C. Activins in adipogenesis and obesity. Int. J. Obes. 2012, 37, 163–166. [Google Scholar] [CrossRef] [PubMed]
- Khan, T.; Muise, E.S.; Iyengar, P.; Wang, Z.V.; Chandalia, M.; Abate, N.; Zhang, B.B.; Bonaldo, P.; Chua, S.; Scherer, P.E. Metabolic dysregulation and adipose tissue fibrosis: Role of collagen VI. Mol. Cell. Biol. 2009, 29, 1575–1591. [Google Scholar] [CrossRef]
- Flanagan, J.N.; Linder, K.; Mejhert, N.; Dungner, E.; Wahlen, K.; Decaunes, P.; Rydén, M.; Björklund, P.; Arver, S.; Bhasin, S.; et al. Role of follistatin in promoting adipogenesis in women. J. Clin. Endocrinol. Metab. 2009, 94, 3003–3009. [Google Scholar] [CrossRef]
- Schönherr, E.; Sunderkötter, C.; Schaefer, L.; Thanos, S.; Grässel, S.; Oldberg, Å.; Iozzo, R.V.; Young, M.F.; Kresse, H. Decorin deficiency leads to impaired angiogenesis in injured mouse cornea. J. Vasc. Res. 2004, 41, 499–508. [Google Scholar] [CrossRef]
- Groeneveld, T.W.L.; Oroszlán, M.; Owens, R.T.; Faber-Krol, M.C.; Bakker, A.C.; Arlaud, G.J.; McQuillan, D.J.; Kishore, U.; Daha, M.R.; Roos, A. Interactions of the extracellular matrix proteoglycans decorin and biglycan with C1q and collectins. J. Immunol. 2005, 175, 4715–4723. [Google Scholar] [CrossRef] [PubMed]
- Daquinag, A.C.; Zhang, Y.; Amaya-Manzanares, F.; Simmons, P.J.; Kolonin, M.G. An isoform of decorin is a resistin receptor on the surface of adipose progenitor cells. Cell Stem Cell 2011, 9, 74–86. [Google Scholar] [CrossRef] [PubMed]
- Pessentheiner, A.R.; Ducasa, G.M.; Gordts, P.L. Proteoglycans in obesity-associated metabolic dysfunction and meta-inflammation. Front. Immunol. 2020, 11, 769. [Google Scholar] [CrossRef] [PubMed]
- Franchi, M.; Torricelli, P.; Giavaresi, G.; Fini, M. Role of moderate exercising on Achilles tendon collagen crimping patterns and proteoglycans. Connect. Tissue Res. 2013, 54, 267–274. [Google Scholar] [CrossRef] [PubMed]
- Xu, S.; Liu, S.; Xu, L.; Deng, S.; He, Y.; Li, S.; Ni, G. Response of decorin to different intensity treadmill running. Mol. Med. Rep. 2018, 17, 7911–7917. [Google Scholar] [CrossRef]
- Neill, T.; Schaefer, L.; Iozzo, R.V. Decorin: A guardian from the matrix. Am. J. Pathol. 2012, 181, 380–387. [Google Scholar] [CrossRef] [PubMed]
- Bahl, N.; Stone, G.; McLean, M.; Ho, K.K.Y.; Birzniece, V. Decorin, a growth hormone-regulated protein in humans. Eur. J. Endocrinol. 2018, 178, 145–152. [Google Scholar] [CrossRef] [PubMed]
- Sutton, J.; Lazarus, L.; Wadosky, K.M.; Rodríguez, J.E.; Hite, R.L.; Min, J.-N.; Walton, B.L.; Willis, M.S.; Thomas, G.A.; Kraemer, W.J.; et al. Growth hormone in exercise: Comparison of physiological and pharmacological stimuli. J. Appl. Physiol. 1976, 41, 523–527. [Google Scholar] [CrossRef]
- Zanchi, N.E.; Filho, M.A.D.S.; Lira, F.S.; Rosa, J.C.; Yamashita, A.S.; Carvalho, C.R.D.O.; Seelaender, M.; Lancha, A.H., Jr. Chronic resistance training decreases MuRF-1 and Atrogin-1 gene expression but does not modify Akt, GSK-3β and p70S6K levels in rats. Eur. J. Appl. Physiol. 2009, 106, 415–423. [Google Scholar] [CrossRef] [PubMed]
- Zhu, J.; Li, Y.; Shen, W.; Qiao, C.; Ambrosio, F.; Lavasani, M.; Huard, J. Relationships between transforming growth factor-β1, myostatin, and decorin: Implications for skeletal muscle fibrosis. J. Biol. Chem. 2007, 282, 25852–25863. [Google Scholar] [CrossRef]
- Li, Y.; Li, J.; Zhu, J.; Sun, B.; Branca, M.; Tang, Y.; Foster, W.; Xiao, X.; Huard, J. Decorin gene transfer promotes muscle cell differentiation and muscle regeneration. Mol. Ther. 2007, 15, 1616–1622. [Google Scholar] [CrossRef] [PubMed]
- Shen, M.; Chen, K.; Lu, J.; Cheng, P.; Xu, L.; Dai, W.; Guo, C. Protective effect of astaxanthin on liver fibrosis through modulation of TGF-1 expression and autophagy. Mediat. Inflamm. 2014, 2014, 954502. [Google Scholar] [CrossRef] [PubMed]
- Robinson, K.A.; Sun, M.; Barnum, C.E.; Weiss, S.N.; Huegel, J.; Shetye, S.S.; Lin, L.; Saez, D.; Adams, S.M.; Iozzo, R.V.; et al. Decorin and biglycan are necessary for maintaining collagen fibril structure, fiber realignment, and mechanical properties of mature tendons. Matrix Biol. 2017, 64, 81–93. [Google Scholar] [CrossRef]
- Wong, S.K.; Ima-Nirwana, S.; Chin, K. Effects of astaxanthin on the protection of muscle health. Exp. Ther. Med. 2020, 20, 2941–2952. [Google Scholar] [CrossRef]
- Relizani, K.; Mouisel, E.; Giannesini, B.; Hourdé, C.; Patel, K.; Gonzalez, S.M.; Jülich, K.; Vignaud, A.; Piétri-Rouxel, F.; Fortin, D.; et al. Blockade of ActRIIB signaling triggers muscle fatigability and metabolic myopathy. Mol. Ther. 2014, 22, 1423–1433. [Google Scholar] [CrossRef]
- Harrison, S.A.; Day, C.P. Benefits of lifestyle modification in NAFLD. Gut 2007, 56, 1760–1769. [Google Scholar] [CrossRef]
- Perakakis, N.; Mougios, V.; Fatouros, I.; Siopi, A.; Draganidis, D.; Peradze, N.; Ghaly, W.; Mantzoros, C.S. Physiology of activins/follistatins: Associations with metabolic and anthropometric variables and response to exercise. J. Clin. Endocrinol. Metab. 2018, 103, 3890–3899. [Google Scholar] [CrossRef]
- Kędzierski, W.; Kowalik, S.; Mojsym, W.; Janczarek, I.; Tkaczyk, E. Plasma Activin A and Decorin in Exercised Purebred Arabian Horses–Preliminary Study. J. Equine Veter. Sci. 2021, 102, 103638. [Google Scholar] [CrossRef] [PubMed]
- Shao, L.-E.; Frigon, J.N.L.; Yu, A.; Palyash, J.; Yu, J. Contrasting effects of inflammatroy cytokines and glucocorticoids on the production of activin a in human marrow stromal cells and their implications. Cytokine 1998, 10, 227–235. [Google Scholar] [CrossRef] [PubMed]
- Vamvini, M.T.; Aronis, K.N.; Chamberland, J.P.; Mantzoros, C.S. Energy deprivation alters in a leptin-and cortisol-independent manner circulating levels of activin A and follistatin but not myostatin in healthy males. J. Clin. Endocrinol. Metab. 2011, 96, 3416–3423. [Google Scholar] [CrossRef] [PubMed]
- Coletti, D.; Baccam, A.; Benoni, A.; Rocchi, M.; Moresi, V.; Seelaender, M.; Xue, Z. The mechanical stimulation of myotubes counteracts the effects of tumor-derived factors through the modulation of the activin/follistatin ratio. Front. Physiol. 2019, 10, 401. [Google Scholar]
- Jones, K.L.; Mansell, A.; Patella, S.; Scott, B.J.; Hedger, M.P.; de Kretser, D.M.; Phillips, D.J. Activin A is a critical component of the inflammatory response, and its binding protein, follistatin, reduces mortality in endotoxemia. Proc. Natl. Acad. Sci. USA 2007, 104, 16239–16244. [Google Scholar] [CrossRef]
- Choy, L.; Derynck, R. Transforming growth factor-β inhibits adipocyte differentiation by Smad3 interacting with CCAAT/enhancer-binding protein (C/EBP) and repressing C/EBP transactivation function. J. Biol. Chem. 2003, 278, 9609–9619. [Google Scholar] [CrossRef]
- Song, W.; Owusu-Ansah, E.; Hu, Y.; Cheng, D.; Ni, X.; Zirin, J.; Perrimon, N. Activin signaling mediates muscle-to-adipose communication in a mitochondria dysfunction-associated obesity model. Proc. Natl. Acad. Sci. USA 2017, 114, 8596–8601. [Google Scholar] [CrossRef]
- Latres, E.; Mastaitis, J.; Fury, W.; Miloscio, L.; Trejos, J.; Pangilinan, J.; Okamoto, H.; Cavino, K.; Na, E.; Papatheodorou, A.; et al. Activin A more prominently regulates muscle mass in primates than does GDF8. Nat. Commun. 2017, 8, 15153. [Google Scholar] [CrossRef]
- Davey, J.R.; Estevez, E.; Thomson, R.E.; Whitham, M.; Watt, K.I.; Hagg, A.; Qian, H.; Henstridge, D.C.; Ludlow, H.; Hedger, M.P.; et al. Intravascular Follistatin gene delivery improves glycemic control in a mouse model of type 2 diabetes. FASEB J. 2020, 34, 5697–5714. [Google Scholar] [CrossRef]
- Elliott, B.; Renshaw, D.; Getting, S.; Mackenzie, R. The central role of myostatin in skeletal muscle and whole body homeostasis. Acta Physiol. 2012, 205, 324–340. [Google Scholar] [CrossRef] [PubMed]
- Liu, X.H.; Bauman, W.A.; Cardozo, C.P. Myostatin inhibits glucose uptake via suppression of insulin-dependent and-independent signaling pathways in myoblasts. Physiol. Rep. 2018, 6, e13837. [Google Scholar] [CrossRef] [PubMed]
- Ge, X.; Sathiakumar, D.; Lua, B.J.G.; Kukreti, H.; Lee, M.; McFarlane, C. Myostatin signals through miR-34a to regulate Fndc5 expression and browning of white adipocytes. Int. J. Obes. 2016, 41, 137–148. [Google Scholar] [CrossRef]
- Elliott, B.T.; Herbert, P.; Sculthorpe, N.; Grace, F.M.; Stratton, D.; Hayes, L.D. Lifelong exercise, but not short-term high-intensity interval training, increases GDF 11, a marker of successful aging: A preliminary investigation. Physiol. Rep. 2017, 5, e13343. [Google Scholar] [CrossRef] [PubMed]
- Bagheri, R.; Rashidlamir, A.; Motevalli, M.S.; Elliott, B.T.; Mehrabani, J.; Wong, A. Effects of upper-body, lower-body, or combined resistance training on the ratio of follistatin and myostatin in middle-aged men. Eur. J. Appl. Physiol. 2019, 119, 1921–1931. [Google Scholar] [CrossRef]
- Micielska, K.; Gmiat, A.; Zychowska, M.; Kozlowska, M.; Walentukiewicz, A.; Lysak-Radomska, A.; Jaworska, J.; Rodziewicz, E.; Duda-Biernacka, B.; Ziemann, E. The beneficial effects of 15 units of high-intensity circuit training in women is modified by age, baseline insulin resistance and physical capacity. Diabetes Res. Clin. Pr. 2019, 152, 156–165. [Google Scholar] [CrossRef]
- Hittel, D.S.; Axelson, M.; Sarna, N.; Shearer, J.; Huffman, K.M.; Kraus, W.E. Myostatin decreases with aerobic exercise and associates with insulin resistance. Med. Sci. Sports Exerc. 2010, 42, 2023–2029. [Google Scholar] [CrossRef]
- Hulmi, J.J.; Tannerstedt, J.; Selänne, H.; Kainulainen, H.; Kovanen, V.; Mero, A.A. Resistance exercise with whey protein ingestion affects mTOR signaling pathway and myostatin in men. J. Appl. Physiol. 2009, 106, 1720–1729. [Google Scholar] [CrossRef]
- Louis, E.; Raue, U.; Yang, Y.; Jemiolo, B.; Trappe, S. Time course of proteolytic, cytokine, and myostatin gene expression after acute exercise in human skeletal muscle. J. Appl. Physiol. 2007, 103, 1744–1751. [Google Scholar] [CrossRef] [PubMed]
- Roth, S.M.; Martel, G.F.; Ferrell, R.E.; Metter, E.J.; Hurley, B.F.; Rogers, M.A. Myostatin gene expression is reduced in humans with heavy-resistance strength training: A brief communication. Exp. Biol. Med. 2003, 228, 706–709. [Google Scholar] [CrossRef]
- Bassi, D.; Bueno, P.D.G.; Nonaka, K.O.; Selistre-Araujo, H.S.; Leal, A.M.D.O. Exercise alters myostatin protein expression in sedentary and exercised streptozotocin-diabetic rats. Arq. Bras. Endocrinol. Metabol. 2015, 59, 148–153. [Google Scholar] [CrossRef] [PubMed]
- Kurose, S.; Onishi, K.; Takao, N.; Miyauchi, T.; Takahashi, K.; Kimura, Y. Association of serum adiponectin and myostatin levels with skeletal muscle in patients with obesity: A cross-sectional study. PLoS ONE 2021, 16, e0245678. [Google Scholar] [CrossRef] [PubMed]
- Zhou, Y.; Hellberg, M.; Hellmark, T.; Höglund, P.; Clyne, N. Muscle mass and plasma myostatin after exercise training: A substudy of Renal Exercise (RENEXC)—A randomized controlled trial. Nephrol. Dial. Transplant. 2021, 36, 95–103. [Google Scholar] [CrossRef]
- Bergen, H.R.; Farr, J.N.; Vanderboom, P.M.; Atkinson, E.J.; White, T.A.; Singh, R.J.; LeBrasseur, N.K. Myostatin as a mediator of sarcopenia versus homeostatic regulator of muscle mass: Insights using a new mass spectrometry-based assay. Skelet. Muscle 2015, 5, 1–16. [Google Scholar] [CrossRef] [PubMed]
- Covington, J.D.; Tam, C.S.; Bajpeyi, S.; Galgani, J.E.; Noland, R.C.; Smith, S.R.; Redman, L.M.; Ravussin, E. Myokine expression in muscle and myotubes in response to exercise stimulation. Med. Sci. Sports Exerc. 2016, 48, 384–390. [Google Scholar] [CrossRef] [PubMed]
- Kerschan-Schindl, K.; Thalmann, M.M.; Weiss, E.; Tsironi, M.; Föger-Samwald, U.; Meinhart, J.; Skenderi, K.; Pietschmann, P. Changes in serum levels of myokines and Wnt-antagonists after an ultramarathon race. PLoS ONE 2015, 10, e0132478. [Google Scholar] [CrossRef]
- Rad, M.M.; Bijeh, N.; Hosseini, S.R.A.; Saeb, A.R. The effect of two concurrent exercise modalities on serum concentrations of FGF21, irisin, follistatin, and myostatin in men with type 2 diabetes mellitus. Arch. Physiol. Biochem. 2020, 129, 424–433. [Google Scholar]
- García-Fontana, B.; Reyes-García, R.; Morales-Santana, S.; Ávila-Rubio, V.; Munoz-Garach, A.; Rozas-Moreno, P.; Muñoz-Torres, M. Relationship between myostatin and irisin in type 2 diabetes mellitus: A compensatory mechanism to an unfavourable metabolic state? Endocrine 2016, 52, 54–62. [Google Scholar] [CrossRef] [PubMed]
- Laurentino, G.C.; Ugrinowitsch, C.; Roschel, H.; Aoki, M.S.; Soares, A.G.; Neves, M.; Aihara, A.Y.; Fernandes, A.D.R.C.; Tricoli, V. Strength training with blood flow restriction diminishes myostatin gene expression. Med. Sci. Sports Exerc. 2012, 44, 406–412. [Google Scholar] [CrossRef]
- Schwarz, N.A.; McKinley-Barnard, S.K.; Spillane, M.B.; Andre, T.L.; Gann, J.J.; Willoughby, D.S. Effect of resistance exercise intensity on the expression of PGC-1α isoforms and the anabolic and catabolic signaling mediators, IGF-1 and myostatin, in human skeletal muscle. Appl. Physiol. Nutr. Metab. 2016, 41, 856–863. [Google Scholar] [CrossRef]
- Reza, M.M.; Subramaniyam, N.; Sim, C.M.; Ge, X.; Sathiakumar, D.; McFarlane, C.; Sharma, M.; Kambadur, R. Irisin is a pro-myogenic factor that induces skeletal muscle hypertrophy and rescues denervation-induced atrophy. Nat. Commun. 2017, 8, 1104. [Google Scholar] [CrossRef] [PubMed]
- Oldham, J.M.; Osepchook, C.C.; Jeanplong, F.; Falconer, S.J.; Matthews, K.G.; Conaglen, J.V.; Gerrard, D.F.; Smith, H.K.; Wilkins, R.J.; Bass, J.J.; et al. The decrease in mature myostatin protein in male skeletal muscle is developmentally regulated by growth hormone. J. Physiol. 2009, 587, 669–677. [Google Scholar] [CrossRef] [PubMed]
- Vingren, J.L.; Kraemer, W.J.; Ratamess, N.A.; Anderson, J.M.; Volek, J.S.; Maresh, C.M. Testosterone physiology in resistance exercise and training. Sports Med. 2010, 40, 1037–1053. [Google Scholar] [CrossRef]
- MacKenzie, M.G.; Hamilton, D.L.; Pepin, M.; Patton, A.; Baar, K. Inhibition of myostatin signaling through Notch activation following acute resistance exercise. PLoS ONE 2013, 8, e68743. [Google Scholar] [CrossRef]
- Lin, H.-M.; Lee, J.-H.; Yadav, H.; Kamaraju, A.K.; Liu, E.; Zhigang, D.; Vieira, A.; Kim, S.-J.; Collins, H.; Matschinsky, F.; et al. Transforming growth factor-β/Smad3 signaling regulates insulin gene transcription and pancreatic islet β-cell function. J. Biol. Chem. 2009, 284, 12246–12257. [Google Scholar] [CrossRef] [PubMed]
- Seong, H.-A.; Manoharan, R.; Ha, H. Smad proteins differentially regulate obesity-induced glucose and lipid abnormalities and inflammation via class-specific control of AMPK-related kinase MPK38/MELK activity. Cell Death Dis. 2018, 9, 1–13. [Google Scholar] [CrossRef] [PubMed]
- Yadav, H.; Quijano, C.; Kamaraju, A.K.; Gavrilova, O.; Malek, R.; Chen, W.; Zerfas, P.; Zhigang, D.; Wright, E.C.; Stuelten, C.; et al. Protection from obesity and diabetes by blockade of TGF-β/Smad3 signaling. Cell Metab. 2011, 14, 67–79. [Google Scholar] [CrossRef] [PubMed]
- Gutierrez, J.A.; Perr, H.A. Mechanical stretch modulates TGF-β1 and α1 (I) collagen expression in fetal human intestinal smooth muscle cells. Am. J. Physiol. Liver Physiol. 1999, 277, G1074–G1080. [Google Scholar] [CrossRef] [PubMed]
- Czarkowska-Paczek, B.; Zendzian-Piotrowska, M.; Bartlomiejczyk, I.; Przybylski, J.; Gorski, J. The effect of acute and prolonged endurance exercise on transforming growth factor-beta1 generation in rat skeletal and heart muscle. J. Physiol. Pharmacol. 2009, 60, 157–162. [Google Scholar] [PubMed]
- Heinemeier, K.M.; Olesen, J.L.; Haddad, F.; Langberg, H.; Kjaer, M.; Baldwin, K.M.; Schjerling, P. Expression of collagen and related growth factors in rat tendon and skeletal muscle in response to specific contraction types. J. Physiol. 2007, 582, 1303–1316. [Google Scholar] [CrossRef]
- Czarkowska-Pączek, B.; Piekarczyk-Persa, J.; Wyczałkowska-Tomasik, A.; Żendzian-Piotrowska, M.; Pączek, L. Increased TNF-α and TGF-β concentrations in rat liver after intense exercise. Pol. Ann. Med. 2018, 25. [Google Scholar] [CrossRef]
- Kim, J.; Lee, J. Role of transforming growth factor-β in muscle damage and regeneration: Focused on eccentric muscle contraction. J. Exerc. Rehabilitation 2017, 13, 621–626. [Google Scholar] [CrossRef] [PubMed]
- Zhao, W.; Zhao, T.; Chen, Y.; Ahokas, R.A.; Sun, Y. Oxidative stress mediates cardiac fibrosis by enhancing transforming growth factor-beta1 in hypertensive rats. Mol. Cell. Biochem. 2008, 317, 43–50. [Google Scholar] [CrossRef] [PubMed]
- Budasz-Rwiderska, M.; Jank, M.; Motyl, T. Transforming growth factor-beta1 upregulates myostatin expression in mouse C2C12 myoblasts. J. Physiol. Pharmacol. 2005, 56, 195–214. [Google Scholar] [PubMed]
- Böhm, A.; Hoffmann, C.; Irmler, M.; Schneeweiss, P.; Schnauder, G.; Sailer, C.; Schmid, V.; Hudemann, J.; Machann, J.; Schick, F.; et al. TGF-β contributes to impaired exercise response by suppression of mitochondrial key regulators in skeletal muscle. Diabetes 2016, 65, 2849–2861. [Google Scholar] [CrossRef]
- Radak, Z.; Chung, H.Y.; Goto, S. Systemic adaptation to oxidative challenge induced by regular exercise. Free Radic. Biol. Med. 2008, 44, 153–159. [Google Scholar] [CrossRef] [PubMed]
- Koli, K.; Myllärniemi, M.; Keski-Oja, J.; Kinnula, V.L. Transforming growth factor-β activation in the lung: Focus on fibrosis and reactive oxygen species. Antioxidants Redox Signal. 2008, 10, 333–342. [Google Scholar] [CrossRef] [PubMed]
- Akiho, M.; Nakashima, H.; Sakata, M.; Yamasa, Y.; Yamaguchi, A.; Sakuma, K. Expression profile of Notch-1 in mechanically overloaded plantaris muscle of mice. Life Sci. 2010, 86, 59–65. [Google Scholar] [CrossRef]
- Blazek, A.; Knapik, D.; Wu, L.C.; Young, N.A.; Jarjour, W.N.; Agarwal, S. Exercise Suppresses Systemic Inflammation via Inhibition of NF-kappa B Activation in Monocytes. In Arthritis and Rheumatism; Wiley-Blackwell: Hoboken, NJ, USA, 2013. [Google Scholar]
- Choi, H.D.; Kim, J.H.; Chang, M.J.; Kyu-Youn, Y.; Shin, W.G. Effects of astaxanthin on oxidative stress in overweight and obese adults. Phytotherapy Res. 2011, 25, 1813–1818. [Google Scholar] [CrossRef]
- Kim, S.H.; Kim, H. Inhibitory effect of astaxanthin on oxidative stress-induced mitochondrial dysfunction-a mini-review. Nutrients 2018, 10, 1137. [Google Scholar] [CrossRef]
- Kishimoto, Y.; Tani, M.; Uto-Kondo, H.; Iizuka, M.; Saita, E.; Sone, H.; Kondo, K. Astaxanthin suppresses scavenger receptor expression and matrix metalloproteinase activity in macrophages. Eur. J. Nutr. 2010, 49, 119–126. [Google Scholar] [CrossRef] [PubMed]
- Nawaz, A.; Nishida, Y.; Takikawa, A.; Fujisaka, S.; Kado, T.; Aminuddin, A.; Bilal, M.; Jeelani, I.; Aslam, M.R.; Nishimura, A.; et al. Astaxanthin, a Marine Carotenoid, Maintains the Tolerance and Integrity of Adipose Tissue and Contributes to Its Healthy Functions. Nutrients 2021, 13, 4374. [Google Scholar] [CrossRef]
- Liu, P.H.; Aoi, W.; Takami, M.; Terajima, H.; Tanimura, Y.; Naito, Y.; Itoh, Y.; Yoshikawa, T. The astaxanthin-induced improvement in lipid metabolism during exercise is mediated by a PGC-1α increase in skeletal muscle. J. Clin. Biochem. Nutr. 2014, 54, 86–89. [Google Scholar] [CrossRef] [PubMed]
- Phillips, D.J.; de Kretser, D.M. Follistatin: A multifunctional regulatory protein. Front. Neuroendocrinol. 1998, 19, 287–322. [Google Scholar] [CrossRef]
- Toloza, F.J.K.; Ricardo-Silgado, M.L.; Mantilla-Rivas, J.O.; Morales-Álvarez, M.C.; Pérez-Matos, M.C.; Pinzón-Cortés, J.A.; Mendivil, C.O. Folistatina, resistencia a la insulina y composición corporal en adultos colombianos. Rev. Colomb. De Endocrinol. Diabetes Metab. 2018, 5, 7–14. [Google Scholar] [CrossRef]
- Hansen, J.S.; Rutti, S.; Arous, C.; Clemmesen, J.O.; Secher, N.H.; Drescher, A.; Gonelle-Gispert, C.; Halban, P.A.; Pedersen, B.K.; Weigert, C.; et al. Circulating follistatin is liver-derived and regulated by the glucagon-to-insulin ratio. J. Clin. Endocrinol. Metab. 2016, 101, 550–560. [Google Scholar] [CrossRef]
- Diller, M.; Frommer, K.; Dankbar, B.; Tarner, I.; Hülser, M.-L.; Tsiklauri, L.; Hasseli, R.; Sauerbier, M.; Pap, T.; Rehart, S.; et al. The activin-follistatin anti-inflammatory cycle is deregulated in synovial fibroblasts. Arthritis Res. Ther. 2019, 21, 144. [Google Scholar] [CrossRef]
- Zhang, L.; Liu, K.; Han, B.; Xu, Z.; Gao, X. The emerging role of follistatin under stresses and its implications in diseases. Gene 2017, 639, 111–116. [Google Scholar] [CrossRef]
- Han, X.; Møller, L.L.V.; De Groote, E.; Bojsen-Møller, K.N.; Davey, J.; Henríquez-Olguin, C.; Li, Z.; Knudsen, J.R.; Jensen, T.E.; Madsbad, S.; et al. Mechanisms involved in follistatin-induced hypertrophy and increased insulin action in skeletal muscle. J. Cachex-Sarcopenia Muscle 2019, 10, 1241–1257. [Google Scholar] [CrossRef] [PubMed]
- Brouwers, M.C.; Jacobs, C.; Bast, A.; Stehouwer, C.D.; Schaper, N.C. Modulation of glucokinase regulatory protein: A double-edged sword? Trends Mol. Med. 2015, 21, 583–594. [Google Scholar] [CrossRef] [PubMed]
- Wu, C.; Borné, Y.; Gao, R.; Rodriguez, M.L.; Roell, W.C.; Wilson, J.M.; Regmi, A.; Luan, C.; Aly, D.M.; Peter, A.; et al. Elevated circulating follistatin associates with an increased risk of type 2 diabetes. Nat. Commun. 2021, 12, 6486. [Google Scholar] [CrossRef] [PubMed]
- Jones, K.L.; Brauman, J.N.; Groome, N.P.; de Kretser, D.M.; Phillips, D.J. Activin A release into the circulation is an early event in systemic inflammation and precedes the release of follistatin. Endocrinology 2000, 141, 1905–1908. [Google Scholar] [CrossRef] [PubMed]
- Tang, R.; Harasymowicz, N.S.; Wu, C.-L.; Collins, K.H.; Choi, Y.-R.; Oswald, S.J.; Guilak, F. Gene therapy for follistatin mitigates systemic metabolic inflammation and post-traumatic arthritis in high-fat diet–induced obesity. Sci. Adv. 2020, 6, eaaz7492. [Google Scholar] [CrossRef] [PubMed]
- Ni, Y.; Nagashimada, M.; Zhuge, F.; Zhan, L.; Nagata, N.; Tsutsui, A.; Nakanuma, Y.; Kaneko, S.; Ota, T. Astaxanthin prevents and reverses diet-induced insulin resistance and steatohepatitis in mice: A comparison with vitamin E. Sci. Rep. 2015, 5, 17192. [Google Scholar] [CrossRef]
CG | SG | TG | TSG | |||||
---|---|---|---|---|---|---|---|---|
Pre | Post | Pre | Post | Pre | Post | Pre | Post | |
Energy (kcal/d) | 2260 ± 47 | 2269 ± 56 | 2278 ± 101 | 2149 ± 100 | 2269 ± 117 | 2141 ± 117 | 2273 ± 157 | 2129 ± 126 |
CHO (g/d) | 281 ± 31.4 | 283 ± 33.3 | 279.4 ± 27.1 | 261 ± 27.5 | 289 ± 48.6 | 261 ± 39.2 | 288 ± 38.6 | 259 ± 29.1 |
Fat (g/d) | 82.2 ± 11.0 | 81 ± 9.8 | 86.5 ± 10.7 | 75 ± 11.2 | 83.4 ± 12.4 | 73.1 ± 11.2 | 80.8 ± 13.87 | 70.2 ± 11.3 |
Protein (g/d) | 104 ± 12.0 | 106 ± 11.3 | 101 ± 13.5 | 93 ± 12.6 | 103 ± 14.8 | 94 ± 11.7 | 102 ± 14.5 | 90 ± 13.5 |
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Moqaddam, M.A.; Nemati, M.; Dara, M.M.; Hoteit, M.; Sadek, Z.; Ramezani, A.; Rand, M.K.; Abbassi-Daloii, A.; Pashaei, Z.; Almaqhawi, A.; et al. Exploring the Impact of Astaxanthin Supplementation in Conjunction with a 12-Week CrossFit Training Regimen on Selected Adipo-Myokines Levels in Obese Males. Nutrients 2024, 16, 2857. https://doi.org/10.3390/nu16172857
Moqaddam MA, Nemati M, Dara MM, Hoteit M, Sadek Z, Ramezani A, Rand MK, Abbassi-Daloii A, Pashaei Z, Almaqhawi A, et al. Exploring the Impact of Astaxanthin Supplementation in Conjunction with a 12-Week CrossFit Training Regimen on Selected Adipo-Myokines Levels in Obese Males. Nutrients. 2024; 16(17):2857. https://doi.org/10.3390/nu16172857
Chicago/Turabian StyleMoqaddam, Mohammad Ahmadi, Morteza Nemati, Marjan Mansouri Dara, Maha Hoteit, Zahra Sadek, Akbar Ramezani, Mahboubeh Khak Rand, Asieh Abbassi-Daloii, Zhaleh Pashaei, Abdullah Almaqhawi, and et al. 2024. "Exploring the Impact of Astaxanthin Supplementation in Conjunction with a 12-Week CrossFit Training Regimen on Selected Adipo-Myokines Levels in Obese Males" Nutrients 16, no. 17: 2857. https://doi.org/10.3390/nu16172857