Synergistic Effects of Korean Mistletoe and Apple Peel Extracts on Muscle Strength and Endurance
Abstract
:1. Introduction
2. Materials and Methods
2.1. Natural Products and Chemical Materials
2.2. Mistletoe and Apple Peel Extract Preparation
2.3. Total Polyphenol Measurement
2.4. Total Flavonoids Measurement
2.5. Animal Experiments
2.6. Measurement of Muscle Strength
2.7. Measurement of Muscle Endurance
2.8. Histological Analysis
2.9. Real-Time RT PCR
2.10. Western Blotting
2.11. Immunohistochemistry
2.12. Transmission Electron Microscopy (TEM)
2.13. Statistical Analysis
3. Results
3.1. Optimizing the Apple Peel Extraction Method to Maximize Flavonoids and Polyphenol Content
3.2. Synergistic Effect of Combined Mistletoe and Apple Peel Extracts on Muscle Strength and Muscular Endurance
3.3. Combined Mistletoe and Apple Peel Extracts Exerts a Synergistic Effect on Increasing the Size of Muscle Fibers
3.4. Combined Mistletoe and Apple Peel Extracts Exerts a Synergistic Effect on Enhancing Mitochondrial Biogenesis and Mitochondrial Fusion
3.5. Synergistic Effect of the Combine Mistletoe and Apple Peel Extracts on Increasing Different Types of Muscle Fibers
4. Discussion
5. Conclusions
6. Patents
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Gupta, D.S.R. A Comprehensive Study on the Relevance of Health, Fitness, and Wellness. J. Sports Sci. Nutr. 2022, 3, 145–148. [Google Scholar] [CrossRef]
- Ferguson, B. ACSM’s Guidelines for Exercise Testing and Prescription 9th Ed. 2014. J. Can. Chiropr. Assoc. 2014, 58, 328. [Google Scholar]
- Nuzzo, J.L. The Case for Retiring Flexibility as a Major Component of Physical Fitness. Sports Med. 2020, 50, 853–870. [Google Scholar] [CrossRef] [PubMed]
- Maestroni, L.; Read, P.; Bishop, C.; Papadopoulos, K.; Suchomel, T.J.; Comfort, P.; Turner, A. The Benefits of Strength Training on Musculoskeletal System Health: Practical Applications for Interdisciplinary Care. Sports Med. 2020, 50, 1431–1450. [Google Scholar] [CrossRef] [PubMed]
- Liu, X.; Gao, Y.; Lu, J.; Ma, Q.; Shi, Y.; Liu, J.; Xin, S.; Su, H. Effects of Different Resistance Exercise Forms on Body Composition and Muscle Strength in Overweight and/or Obese Individuals: A Systematic Review and Meta-Analysis. Front. Physiol. 2022, 12, 791999. [Google Scholar] [CrossRef]
- Kojima, Y.; Fukusaki, C.; Ishii, N. Effects of Hyperoxia on Dynamic Muscular Endurance Are Associated with Individual Whole-Body Endurance Capacity. PLoS ONE 2020, 15, e0231643. [Google Scholar] [CrossRef]
- Mettler, J.A.; Griffin, L. Muscular Endurance Training and Motor Unit Firing Patterns during Fatigue. Exp. Brain Res. 2016, 234, 267–276. [Google Scholar] [CrossRef]
- Volpi, E.; Nazemi, R.; Fujita, S. Muscle Tissue Changes with Aging. Curr. Opin. Clin. Nutr. Metab. Care 2004, 7, 405–410. [Google Scholar] [CrossRef]
- Woessner, M.N.; Tacey, A.; Levinger-Limor, A.; Parker, A.G.; Levinger, P.; Levinger, I. The Evolution of Technology and Physical Inactivity: The Good, the Bad, and the Way forward. Front. Public Health 2021, 9, 655491. [Google Scholar] [CrossRef]
- World Health Organization. Global Status Report on Physical Activity 2022: Country Profiles; World Health Organization: Geneva, Switzerland, 2022; ISBN 978-92-4-006411-9. [Google Scholar]
- Booth, F.W.; Roberts, C.K.; Laye, M.J. Lack of Exercise Is a Major Cause of Chronic Diseases. Compr. Physiol. 2012, 2, 1143–1211. [Google Scholar] [CrossRef]
- Bowden Davies, K.A.; Pickles, S.; Sprung, V.S.; Kemp, G.J.; Alam, U.; Moore, D.R.; Tahrani, A.A.; Cuthbertson, D.J. Reduced Physical Activity in Young and Older Adults: Metabolic and Musculoskeletal Implications. Ther. Adv. Endocrinol. Metab. 2019, 10, 2042018819888824. [Google Scholar] [CrossRef] [PubMed]
- Nishiguchi, S.; Yamada, M.; Kajiwara, Y.; Sonoda, T.; Yoshimura, K.; Kayama, H.; Tanigawa, T.; Yukutake, T.; Aoyama, T. Effect of Physical Activity at Midlife on Skeletal Muscle Mass in Old Age in Community-Dwelling Older Women: A Cross-Sectional Study. J. Clin. Gerontol. Geriatr. 2014, 5, 18–22. [Google Scholar] [CrossRef]
- Ekelund, U.; Ward, H.A.; Norat, T.; Luan, J.; May, A.M.; Weiderpass, E.; Sharp, S.J.; Overvad, K.; Østergaard, J.N.; Tjønneland, A.; et al. Physical Activity and All-Cause Mortality across Levels of Overall and Abdominal Adiposity in European Men and Women: The European Prospective Investigation into Cancer and Nutrition Study (EPIC). Am. J. Clin. Nutr. 2015, 101, 613–621. [Google Scholar] [CrossRef]
- Sellami, M.; Slimeni, O.; Pokrywka, A.; Kuvačić, G.; D Hayes, L.; Milic, M.; Padulo, J. Herbal Medicine for Sports: A Review. J. Int. Soc. Sports Nutr. 2018, 15, 14. [Google Scholar] [CrossRef] [PubMed]
- Yu, Z.; Wang, W.; Yang, K.; Gou, J.; Jiang, Y.; Yu, Z. Sports and Chinese Herbal Medicine. Pharmacol. Res. Mod. Chin. Med. 2023, 9, 100290. [Google Scholar] [CrossRef]
- Amir, M.; Vohra, M.; Raj, R.G.; Osoro, I.; Sharma, A. Adaptogenic Herbs: A Natural Way to Improve Athletic Performance. Health Sci. Rev. 2023, 7, 100092. [Google Scholar] [CrossRef]
- Bagherniya, M.; Mahdavi, A.; Shokri-Mashhadi, N.; Banach, M.; Von Haehling, S.; Johnston, T.P.; Sahebkar, A. The Beneficial Therapeutic Effects of Plant-Derived Natural Products for the Treatment of Sarcopenia. J. Cachexia Sarcopenia Muscle 2022, 13, 2772–2790. [Google Scholar] [CrossRef]
- Alamdari, N.; Aversa, Z.; Castillero, E.; Gurav, A.; Petkova, V.; Tizio, S.; Hasselgren, P.-O. Resveratrol Prevents Dexamethasone-Induced Expression of the Muscle Atrophy-Related Ubiquitin Ligases Atrogin-1 and MuRF1 in Cultured Myotubes through a SIRT1-Dependent Mechanism. Biochem. Biophys. Res. Commun. 2012, 417, 528–533. [Google Scholar] [CrossRef]
- Montesano, A.; Luzi, L.; Senesi, P.; Mazzocchi, N.; Terruzzi, I. Resveratrol Promotes Myogenesis and Hypertrophy in Murine Myoblasts. J. Transl. Med. 2013, 11, 310. [Google Scholar] [CrossRef] [PubMed]
- Momken, I.; Stevens, L.; Bergouignan, A.; Desplanches, D.; Rudwill, F.; Chery, I.; Zahariev, A.; Zahn, S.; Stein, T.P.; Sebedio, J.L.; et al. Resveratrol Prevents the Wasting Disorders of Mechanical Unloading by Acting as a Physical Exercise Mimetic in the Rat. FASEB J. 2011, 25, 3646–3660. [Google Scholar] [CrossRef]
- Kim, J.; Cho, E.H.; Kim, H.J.; Yoo, Y.C.; Kim, S.J.; Jung, H.-Y.; Lee, A.N.; Park, S.M.; Song, T.J.; Choung, H.J. Extracts Isolated from Mistletoe for Enhancing Power of Exercise Performance and Suppressing Fatigue. Korean Patent KR20090120348A, 24 November 2009. [Google Scholar]
- Goode, E.C.; Van Duser, S.E.; Rogers, R.R.; Williams, T.D.; Ballmann, C.G. Effects of Acute Mistletoe (Viscum album L.) Ingestion on Aerobic Exercise Performance. Nutraceuticals 2022, 2, 162–169. [Google Scholar] [CrossRef]
- Jung, H.-Y.; Lee, A.-N.; Song, T.-J.; An, H.-S.; Kim, Y.-H.; Kim, K.-D.; Kim, I.-B.; Kim, K.-S.; Han, B.-S.; Kim, C.-H.; et al. Korean Mistletoe (Viscum album coloratum) Extract Improves Endurance Capacity in Mice by Stimulating Mitochondrial Activity. J. Med. Food 2012, 15, 621–628. [Google Scholar] [CrossRef]
- Lee, S.-H.; Kim, I.-B.; Kim, J.-B.; Park, D.-H.; Min, K.-J. The Effects of Korean Mistletoe Extract on Endurance during Exercise in Mice. Anim. Cells Syst. 2014, 18, 34–40. [Google Scholar] [CrossRef]
- Szurpnicka, A.; Zjawiony, J.K.; Szterk, A. Therapeutic Potential of Mistletoe in CNS-Related Neurological Disorders and the Chemical Composition of Viscum Species. J. Ethnopharmacol. 2019, 231, 241–252. [Google Scholar] [CrossRef]
- Pietrzak, W.; Nowak, R. Impact of Harvest Conditions and Host Tree Species on Chemical Composition and Antioxidant Activity of Extracts from Viscum album L. Molecules 2021, 26, 3741. [Google Scholar] [CrossRef]
- Mudgal, G.; Kaur, J.; Chand, K.; Parashar, M.; Dhar, S.K.; Singh, G.B.; Gururani, M.A. Mitigating the Mistletoe Menace: Biotechnological and Smart Management Approaches. Biology 2022, 11, 1645. [Google Scholar] [CrossRef]
- Hutt, N.; Kopferschmitt-Kubler, M.; Cabalion, J.; Purohit, A.; Alt, M.; Pauli, G. Anaphylactic Reactions after Therapeutic Injection of Mistletoe (Viscum album L.). Allergol. Immunopathol. 2001, 29, 201–203. [Google Scholar] [CrossRef]
- Kim, H.J.; Kim, H.; Ahn, J.H.; Suk, H.J. Liver Injury Induced by Herbal Extracts Containing Mistletoe and Kudzu. J. Altern. Complement. Med. 2015, 21, 180–185. [Google Scholar] [CrossRef]
- Steele, M.L.; Axtner, J.; Happe, A.; Kröz, M.; Matthes, H.; Schad, F. Adverse Drug Reactions and Expected Effects to Therapy with Subcutaneous Mistletoe Extracts (Viscum album L.) in Cancer Patients. Evid.-Based Complement. Altern. Med. 2014, 2014, 724258. [Google Scholar] [CrossRef]
- Gutiérrez-Grijalva, E.P.; Zamudio-Sosa, V.E.; Contreras-Angulo, L.A.; Leyva-López, N.; Heredia, J.B. Bioaccessibility of Phenolic Compounds from Mistletoe Infusions and Effect of In Vitro Digestion on Its Antioxidant and Pancreatic Lipase Inhibitory Activity. Foods 2022, 11, 3319. [Google Scholar] [CrossRef]
- Kschonsek, J.; Wolfram, T.; Stöckl, A.; Böhm, V. Polyphenolic Compounds Analysis of Old and New Apple Cultivars and Contribution of Polyphenolic Profile to the In Vitro Antioxidant Capacity. Antioxidants 2018, 7, 20. [Google Scholar] [CrossRef]
- Boyer, J.; Liu, R.H. Apple Phytochemicals and Their Health Benefits. Nutr. J. 2004, 3, 5. [Google Scholar] [CrossRef]
- Bowtell, J.; Kelly, V. Fruit-Derived Polyphenol Supplementation for Athlete Recovery and Performance. Sports Med. 2019, 49, 3–23. [Google Scholar] [CrossRef]
- Kunkel, S.D.; Suneja, M.; Ebert, S.M.; Bongers, K.S.; Fox, D.K.; Malmberg, S.E.; Alipour, F.; Shields, R.K.; Adams, C.M. mRNA Expression Signatures of Human Skeletal Muscle Atrophy Identify a Natural Compound that Increases Muscle Mass. Cell Metab. 2011, 13, 627–638. [Google Scholar] [CrossRef]
- Mizunoya, W.; Miyahara, H.; Okamoto, S.; Akahoshi, M.; Suzuki, T.; Do, M.-K.Q.; Ohtsubo, H.; Komiya, Y.; Lan, M.; Waga, T.; et al. Improvement of Endurance Based on Muscle Fiber-Type Composition by Treatment with Dietary Apple Polyphenols in Rats. PLoS ONE 2015, 10, e0134303. [Google Scholar] [CrossRef]
- Tsao, R.; Yang, R.; Young, J.C.; Zhu, H. Polyphenolic Profiles in Eight Apple Cultivars Using High-Performance Liquid Chromatography (HPLC). J. Agric. Food Chem. 2003, 51, 6347–6353. [Google Scholar] [CrossRef]
- Gustavsson, J.; Cederberg, C.; Sonesson, U.; Van Otterdijk, R.; Meybeck, A. Global Food Losses and Food Waste; FAO: Rome, Italy, 2011. [Google Scholar]
- Hee, L.M.; Eun, L.J. Antioxidant and Antimicrobial Properties of Various Solvent Extracts from Robus idaeus. Korean J. Food Nutr. 2015, 28, 774–781. [Google Scholar]
- Shin, S.W.; Ghimeray, A.K.; Park, C.H. Investigation of Total Phenolic, Total Flavonoid, Antioxidant and Allyl Isothiocyanate Content in the Different Organs of Wasabi Japonica Grown in an Organic System. Afr. J. Tradit. Complement. Altern. Med. 2014, 11, 38–45. [Google Scholar] [CrossRef]
- Schneider, C.A.; Rasband, W.S.; Eliceiri, K.W. NIH Image to ImageJ: 25 Years of Image Analysis. Nat. Methods 2012, 9, 671–675. [Google Scholar] [CrossRef]
- Zhang, Q.-W.; Lin, L.-G.; Ye, W.-C. Techniques for Extraction and Isolation of Natural Products: A Comprehensive Review. Chin. Med. 2018, 13, 20. [Google Scholar] [CrossRef]
- Craig, D.M.; Ashcroft, S.P.; Belew, M.Y.; Stocks, B.; Currell, K.; Baar, K.; Philp, A. Utilizing Small Nutrient Compounds as Enhancers of Exercise-Induced Mitochondrial Biogenesis. Front. Physiol. 2015, 6, 296. [Google Scholar] [CrossRef] [PubMed]
- Yan, Z.; Okutsu, M.; Akhtar, Y.N.; Lira, V.A. Regulation of Exercise-Induced Fiber Type Transformation, Mitochondrial Biogenesis, and Angiogenesis in Skeletal Muscle. J. Appl. Physiol. 2011, 110, 264–274. [Google Scholar] [CrossRef] [PubMed]
- Ørtenblad, N.; Nielsen, J.; Boushel, R.; Söderlund, K.; Saltin, B.; Holmberg, H.-C. The Muscle Fiber Profiles, Mitochondrial Content, and Enzyme Activities of the Exceptionally Well-Trained Arm and Leg Muscles of Elite Cross-Country Skiers. Front. Physiol. 2018, 9, 1031. [Google Scholar] [CrossRef] [PubMed]
- Jeong, J.; Park, C.-H.; Kim, I.; Kim, Y.-H.; Yoon, J.-M.; Kim, K.-S.; Kim, J.-B. Korean Mistletoe (Viscum album coloratum) Extract Regulates Gene Expression Related to Muscle Atrophy and Muscle Hypertrophy. BMC Complement. Altern. Med. 2017, 17, 68. [Google Scholar] [CrossRef] [PubMed]
- Durazzo, A.; Lucarini, M.; Souto, E.B.; Cicala, C.; Caiazzo, E.; Izzo, A.A.; Novellino, E.; Santini, A. Polyphenols: A Concise Overview on the Chemistry, Occurrence, and Human Health. Phytother. Res. 2019, 33, 2221–2243. [Google Scholar] [CrossRef]
- Bordoni, B.; Varacallo, M. Anatomy, Bony Pelvis and Lower Limb, Gastrocnemius Muscle. In StatPearls; StatPearls Publishing: Treasure Island, FL, USA, 2024. [Google Scholar]
- Wilborn, C.D.; Willoughby, D.S. The Role of Dietary Protein Intake and Resistance Training on Myosin Heavy Chain Expression. J. Int. Soc. Sports Nutr. 2004, 1, 27. [Google Scholar] [CrossRef]
- Szurpnicka, A.; Kowalczuk, A.; Szterk, A. Biological Activity of Mistletoe: In Vitro and In Vivo Studies and Mechanisms of Action. Arch. Pharm. Res. 2020, 43, 593–629. [Google Scholar] [CrossRef]
- Makinde, E.; Ma, L.; Mellick, G.D.; Feng, Y. Mitochondrial Modulators: The Defender. Biomolecules 2023, 13, 226. [Google Scholar] [CrossRef]
- Larosa, V.; Remacle, C. Insights into the Respiratory Chain and Oxidative Stress. Biosci. Rep. 2018, 38, BSR20171492. [Google Scholar] [CrossRef]
- Green, A.; Hossain, T.; Eckmann, D.M. Mitochondrial Dynamics Involves Molecular and Mechanical Events in Motility, Fusion and Fission. Front. Cell Dev. Biol. 2022, 10, 1010232. [Google Scholar] [CrossRef]
- Yao, C.-H.; Wang, R.; Wang, Y.; Kung, C.-P.; Weber, J.D.; Patti, G.J. Mitochondrial Fusion Supports Increased Oxidative Phosphorylation during Cell Proliferation. Elife 2019, 8, e41351. [Google Scholar] [CrossRef] [PubMed]
- Jheng, H.-F.; Tsai, P.-J.; Guo, S.-M.; Kuo, L.-H.; Chang, C.-S.; Su, I.-J.; Chang, C.-R.; Tsai, Y.-S. Mitochondrial Fission Contributes to Mitochondrial Dysfunction and Insulin Resistance in Skeletal Muscle. Mol. Cell Biol. 2012, 32, 309–319. [Google Scholar] [CrossRef] [PubMed]
- Butkeviciute, A.; Petrikaite, V.; Jurgaityte, V.; Liaudanskas, M.; Janulis, V. Antioxidant, Anti-Inflammatory, and Cytotoxic Activity of Extracts from Some Commercial Apple Cultivars in Two Colorectal and Glioblastoma Human Cell Lines. Antioxidants 2021, 10, 1098. [Google Scholar] [CrossRef]
- Abu Shelbayeh, O.; Arroum, T.; Morris, S.; Busch, K.B. PGC-1α Is a Master Regulator of Mitochondrial Lifecycle and ROS Stress Response. Antioxidants 2023, 12, 1075. [Google Scholar] [CrossRef]
- Whitley, B.N.; Engelhart, E.A.; Hoppins, S. Mitochondrial Dynamics and Their Potential as a Therapeutic Target. Mitochondrion 2019, 49, 269–283. [Google Scholar] [CrossRef]
- Wilson, J.M.; Loenneke, J.P.; Jo, E.; Wilson, G.J.; Zourdos, M.C.; Kim, J.-S. The Effects of Endurance, Strength, and Power Training on Muscle Fiber Type Shifting. J. Strength. Cond. Res. 2012, 26, 1724–1729. [Google Scholar] [CrossRef]
- Zierath, J.R.; Hawley, J.A. Skeletal Muscle Fiber Type: Influence on Contractile and Metabolic Properties. PLoS Biol. 2004, 2, e348. [Google Scholar] [CrossRef] [PubMed]
- Westerblad, H.; Bruton, J.D.; Katz, A. Skeletal Muscle: Energy Metabolism, Fiber Types, Fatigue and Adaptability. Exp. Cell Res. 2010, 316, 3093–3099. [Google Scholar] [CrossRef]
- Liu, G.; Mac Gabhann, F.; Popel, A.S. Effects of Fiber Type and Size on the Heterogeneity of Oxygen Distribution in Exercising Skeletal Muscle. PLoS ONE 2012, 7, e44375. [Google Scholar] [CrossRef]
- Plotkin, D.L.; Roberts, M.D.; Haun, C.T.; Schoenfeld, B.J. Muscle Fiber Type Transitions with Exercise Training: Shifting Perspectives. Sports 2021, 9, 127. [Google Scholar] [CrossRef]
- Schiaffino, S.; Reggiani, C. Fiber Types in Mammalian Skeletal Muscles. Physiol. Rev. 2011, 91, 1447–1531. [Google Scholar] [CrossRef]
- Hennebry, A.; Oldham, J.; Shavlakadze, T.; Grounds, M.D.; Sheard, P.; Fiorotto, M.L.; Falconer, S.; Smith, H.K.; Berry, C.; Jeanplong, F.; et al. IGF1 Stimulates Greater Muscle Hypertrophy in the Absence of Myostatin in Male Mice. J. Endocrinol. 2017, 234, 187–200. [Google Scholar] [CrossRef]
- Yoshida, T.; Delafontaine, P. Mechanisms of IGF-1-Mediated Regulation of Skeletal Muscle Hypertrophy and Atrophy. Cells 2020, 9, 1970. [Google Scholar] [CrossRef]
- Halling, J.F.; Pilegaard, H. PGC-1α-Mediated Regulation of Mitochondrial Function and Physiological Implications. Appl. Physiol. Nutr. Metab. 2020, 45, 927–936. [Google Scholar] [CrossRef]
- Wang, H.; Guo, S.; Gao, H.; Ding, J.; Li, H.; Kong, X.; Zhang, S.; He, M.; Feng, Y.; Wu, W.; et al. Myostatin Regulates Energy Homeostasis through Autocrine- and Paracrine-Mediated Microenvironment Communication. J. Clin. Investig. 2024, 134, e178303. [Google Scholar] [CrossRef]
- Yang, L.; Miao, L.; Liang, F.; Huang, H.; Teng, X.; Li, S.; Nuriddinov, J.; Selzer, M.E.; Hu, Y. The mTORC1 Effectors S6K1 and 4E-BP Play Different Roles in CNS Axon Regeneration. Nat. Commun. 2014, 5, 5416. [Google Scholar] [CrossRef]
- Bodine, S.C.; Baehr, L.M. Skeletal Muscle Atrophy and the E3 Ubiquitin Ligases MuRF1 and MAFbx/Atrogin-1. Am. J. Physiol. Endocrinol. Metab. 2014, 307, E469–E484. [Google Scholar] [CrossRef]
- Sandri, M.; Sandri, C.; Gilbert, A.; Skurk, C.; Calabria, E.; Picard, A.; Walsh, K.; Schiaffino, S.; Lecker, S.H.; Goldberg, A.L. Foxo Transcription Factors Induce the Atrophy-Related Ubiquitin Ligase Atrogin-1 and Cause Skeletal Muscle Atrophy. Cell 2004, 117, 399–412. [Google Scholar] [CrossRef]
- Sartori, R.; Romanello, V.; Sandri, M. Mechanisms of Muscle Atrophy and Hypertrophy: Implications in Health and Disease. Nat. Commun. 2021, 12, 330. [Google Scholar] [CrossRef] [PubMed]
- Xu, J.; Li, R.; Workeneh, B.; Dong, Y.; Wang, X.; Hu, Z. Transcription Factor FoxO1, the Dominant Mediator of Muscle Wasting in Chronic Kidney Disease, Is Inhibited by microRNA-486. Kidney Int. 2012, 82, 401–411. [Google Scholar] [CrossRef] [PubMed]
- Cunningham, J.T.; Rodgers, J.T.; Arlow, D.H.; Vazquez, F.; Mootha, V.K.; Puigserver, P. mTOR Controls Mitochondrial Oxidative Function through a YY1–PGC-1α Transcriptional Complex. Nature 2007, 450, 736–740. [Google Scholar] [CrossRef]
- Mihaylov, S.R.; Castelli, L.M.; Lin, Y.-H.; Gül, A.; Soni, N.; Hastings, C.; Flynn, H.R.; Păun, O.; Dickman, M.J.; Snijders, A.P.; et al. The Master Energy Homeostasis Regulator PGC-1α Exhibits an mRNA Nuclear Export Function. Nat. Commun. 2023, 14, 5496. [Google Scholar] [CrossRef]
- Finck, B.N.; Kelly, D.P. PGC-1 Coactivators: Inducible Regulators of Energy Metabolism in Health and Disease. J. Clin. Investig. 2006, 116, 615–622. [Google Scholar] [CrossRef]
- Gureev, A.P.; Shaforostova, E.A.; Popov, V.N. Regulation of Mitochondrial Biogenesis as a Way for Active Longevity: Interaction between the Nrf2 and PGC-1α Signaling Pathways. Front. Genet. 2019, 10, 435. [Google Scholar] [CrossRef]
- Loumaye, A.; Lause, P.; Zhong, X.; Zimmers, T.A.; Bindels, L.B.; Thissen, J.-P. Activin A Causes Muscle Atrophy through MEF2C-Dependent Impaired Myogenesis. Cells 2022, 11, 1119. [Google Scholar] [CrossRef]
- Skrypnik, L.; Feduraev, P.; Golovin, A.; Maslennikov, P.; Belov, N.; Matveev, M.; Pungin, A. Biotechnological Potential of Different Organs of Mistletoe (Viscum album L.) Collected from Various Host Tree Species in an Urban Area. Plants 2022, 11, 2686. [Google Scholar] [CrossRef]
- Ommati, M.M.; Farshad, O.; Mousavi, K.; Khalili, M.; Jamshidzadeh, A.; Heidari, R. Chlorogenic Acid Supplementation Improves Skeletal Muscle Mitochondrial Function in a Rat Model of Resistance Training. Biologia 2020, 75, 1221–1230. [Google Scholar] [CrossRef]
- Nikawa, T.; Ulla, A.; Sakakibara, I. Polyphenols and Their Effects on Muscle Atrophy and Muscle Health. Molecules 2021, 26, 4887. [Google Scholar] [CrossRef]
- Ichwan, M.; Walker, T.L.; Nicola, Z.; Ludwig-Müller, J.; Böttcher, C.; Overall, R.W.; Adusumilli, V.S.; Bulut, M.; Sykes, A.M.; Hübner, N.; et al. Apple Peel and Flesh Contain Pro-Neurogenic Compounds. Stem Cell Rep. 2021, 16, 548–565. [Google Scholar] [CrossRef]
- Ghafouri-Fard, S.; Shoorei, H.; Khanbabapour Sasi, A.; Taheri, M.; Ayatollahi, S.A. The Impact of the Phytotherapeutic Agent Quercetin on Expression of Genes and Activity of Signaling Pathways. Biomed. Pharmacother. 2021, 141, 111847. [Google Scholar] [CrossRef]
- Peng, J.; Li, Q.; Li, K.; Zhu, L.; Lin, X.; Lin, X.; Shen, Q.; Li, G.; Xie, X. Quercetin Improves Glucose and Lipid Metabolism of Diabetic Rats: Involvement of Akt Signaling and SIRT1. J. Diabetes Res. 2017, 2017, e3417306. [Google Scholar] [CrossRef]
- Yao, R.-Q.; Qi, D.-S.; Yu, H.-L.; Liu, J.; Yang, L.-H.; Wu, X.-X. Quercetin Attenuates Cell Apoptosis in Focal Cerebral Ischemia Rat Brain Via Activation of BDNF–TrkB–PI3K/Akt Signaling Pathway. Neurochem. Res. 2012, 37, 2777–2786. [Google Scholar] [CrossRef]
- Khairallah, R.J.; O’Shea, K.M.; Ward, C.W.; Butteiger, D.N.; Mukherjea, R.; Krul, E.S. Chronic Dietary Supplementation with Soy Protein Improves Muscle Function in Rats. PLoS ONE 2017, 12, e0189246. [Google Scholar] [CrossRef]
- Otsuka, Y.; Egawa, K.; Kanzaki, N.; Izumo, T.; Rogi, T.; Shibata, H. Quercetin Glycosides Prevent Dexamethasone-Induced Muscle Atrophy in Mice. Biochem. Biophys. Rep. 2019, 18, 100618. [Google Scholar] [CrossRef]
- Wiebel, M.; Bensberg, K.; Wende, L.; Grandrath, R.; Plitzko, K.; Bohrmann-Linde, C.; Kirsch, S.F.; Schebb, N.H. Efficient and Simple Extraction Protocol for Triterpenic Acids from Apples. J. Chem. Educ. 2024, 101, 2087–2093. [Google Scholar] [CrossRef]
- Soursouri, A.; Hosseini, S.M.; Fattahi, F. Biochemical Analysis of European Mistletoe (Viscum album L.) Foliage and Fruit Settled on Persian Ironwood (Parrotia persica C. A. Mey.) and Hornbeam (Carpinus betulus L.). Biocatal. Agric. Biotechnol. 2019, 22, 101360. [Google Scholar] [CrossRef]
- Seo, D.Y.; Lee, S.R.; Heo, J.-W.; No, M.-H.; Rhee, B.D.; Ko, K.S.; Kwak, H.-B.; Han, J. Ursolic Acid in Health and Disease. Korean J. Physiol. Pharmacol. 2018, 22, 235–248. [Google Scholar] [CrossRef]
- Bashir, R. Chapter 49—Ursolic Acid and Maslinic Acid: Novel Candidates for Counteracting Muscle Loss and Enhancing Muscle Growth. In Nutrition and Enhanced Sports Performance; Bagchi, D., Nair, S., Sen, C.K., Eds.; Academic Press: San Diego, CA, USA, 2013; pp. 473–478. ISBN 978-0-12-396454-0. [Google Scholar]
- Song, M.-Y. The Study of the Changes of Obesity-Relating Biomarkers in High Fat Fed-Induced C57BL/6 Mice. J. Korean Med. Obes. Res. 2016, 16, 19–26. [Google Scholar] [CrossRef]
- Salahudeen, M.S.; Nishtala, P.S. An Overview of Pharmacodynamic Modelling, Ligand-Binding Approach and Its Application in Clinical Practice. Saudi Pharm. J. SPJ 2017, 25, 165. [Google Scholar] [CrossRef]
- Andrade, C. The Ceiling Effect, the Floor Effect, and the Importance of Active and Placebo Control Arms in Randomized Controlled Trials of an Investigational Drug. Indian. J. Psychol. Med. 2021, 43, 360–361. [Google Scholar] [CrossRef]
- Proost, J.H.; Eleveld, D.J.; Struys, M.M.R.F. Population Pharmacodynamic Modeling Using the Sigmoid Emax Model: Influence of Inter-Individual Variability on the Steepness of the Concentration–Effect Relationship. a Simulation Study. AAPS J. 2020, 23, 10. [Google Scholar] [CrossRef] [PubMed]
- Guan, Y.; Yan, Z. Molecular Mechanisms of Exercise and Healthspan. Cells 2022, 11, 872. [Google Scholar] [CrossRef] [PubMed]
- Ayyadurai, V.A.S.; Deonikar, P. In Silico Modeling and Quantification of Synergistic Effects of Multi-Combination Compounds: Case Study of the Attenuation of Joint Pain Using a Combination of Phytonutrients. Appl. Sci. 2022, 12, 10013. [Google Scholar] [CrossRef]
- Liu, H.; Fan, Z.; Lin, J.; Yang, Y.; Ran, T.; Chen, H. The Recent Progress of Deep-Learning-Based in Silico Prediction of Drug Combination. Drug Discov. Today 2023, 28, 103625. [Google Scholar] [CrossRef]
- Wilson, J.L.; Steinberg, E.; Racz, R.; Altman, R.B.; Shah, N.; Grimes, K. A Network Paradigm Predicts Drug Synergistic Effects Using Downstream Protein-Protein Interactions. CPT Pharmacomet. Syst. Pharmacol. 2022, 11, 1527–1538. [Google Scholar] [CrossRef]
Groups | Treatment |
---|---|
NC | Negative control: 200 µL 1 × phosphate buffered saline (PBS) |
PC | Positive control: 200 mg/kg creatine |
A | 200 mg/kg apple peel extract |
M | 200 mg/kg mistletoe extract |
AML | Low dose: 100 mg/kg apple peel extract + 100 mg/kg mistletoe extract |
AMH | High dose: 200 mg/kg apple peel extract + 200 mg/kg mistletoe extract |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Kang, Y.-G.; Kwon, J.; Kwon, S.; Kim, A.-R. Synergistic Effects of Korean Mistletoe and Apple Peel Extracts on Muscle Strength and Endurance. Nutrients 2024, 16, 3255. https://doi.org/10.3390/nu16193255
Kang Y-G, Kwon J, Kwon S, Kim A-R. Synergistic Effects of Korean Mistletoe and Apple Peel Extracts on Muscle Strength and Endurance. Nutrients. 2024; 16(19):3255. https://doi.org/10.3390/nu16193255
Chicago/Turabian StyleKang, Youn-Goo, Joonhyuk Kwon, Soonjun Kwon, and Ah-Ram Kim. 2024. "Synergistic Effects of Korean Mistletoe and Apple Peel Extracts on Muscle Strength and Endurance" Nutrients 16, no. 19: 3255. https://doi.org/10.3390/nu16193255