Suppressive Effects of Turmeric Extract on Muscle Atrophy in Dexamethasone-Treated Mice and Myotubes
Abstract
:1. Introduction
2. Materials and Methods
2.1. Preparation of TE and TE Fraction
2.2. Animal Experiments
2.3. Cell Caltivation
2.4. Isolation of Total RNA and Real-Time RT PCR Analysis
2.5. DNA Microarray Analysis
2.6. Western Blotting Analysis
2.7. LDH Assay
2.8. Statistical Analysis
3. Results
3.1. Effects of TE on Body Weight and Muscle Weight in DEX-Treated Mice
3.2. DNA Microarray Analysis of DEX-Injected and TE-Supplemented Mice
3.3. Effects of TE on FBXO32 and MurF1 Expression in DEX-Treated C2C12 Cells
3.4. Effects of Five TE Fractions on FBXO32 and MurF1 Expression in DEX-Treated C2C12 Cells
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Data Availability Statement
Conflicts of Interest
References
- Miljkovic, N.; Lim, J.Y.; Miljkovic, I.; Frontera, W.R. Aging of skeletal muscle fibers. Ann. Rehabil. Med. 2015, 39, 155–162. [Google Scholar] [CrossRef] [PubMed]
- Chen, L.K.; Woo, J.; Assantachai, P.; Auyeung, T.W.; Chou, M.Y.; Iijima, K.; Jang, H.C.; Kang, L.; Kim, M.; Kim, S.; et al. Asian Working Group for Sarcopenia: 2019 Consensus Update on Sarcopenia Diagnosis and Treatment. J. Am. Med. Dir. Assoc. 2020, 21, 300–307.e302. [Google Scholar] [CrossRef]
- Cruz-Jentoft, A.J.; Bahat, G.; Bauer, J.; Boirie, Y.; Bruyère, O.; Cederholm, T.; Cooper, C.; Landi, F.; Rolland, Y.; Sayer, A.A.; et al. Sarcopenia: Revised European consensus on definition and diagnosis. Age Ageing 2019, 48, 16–31. [Google Scholar] [CrossRef]
- Dao, T.; Green, A.E.; Kim, Y.A.; Bae, S.J.; Ha, K.T.; Gariani, K.; Lee, M.R.; Menzies, K.J.; Ryu, D. Sarcopenia and Muscle Aging: A Brief Overview. Endocrinol. Metab. 2020, 35, 716–732. [Google Scholar] [CrossRef]
- Sandri, M. Protein breakdown in muscle wasting: Role of autophagy-lysosome and ubiquitin-proteasome. Int. J. Biochem. Cell Biol. 2013, 45, 2121–2129. [Google Scholar] [CrossRef]
- Mankhong, S.; Kim, S.; Moon, S.; Kwak, H.-B.; Park, D.-H.; Kang, J.-H. Experimental Models of Sarcopenia: Bridging Molecular Mechanism and Therapeutic Strategy. Cells 2020, 9, 1385. [Google Scholar] [CrossRef] [PubMed]
- Shimizu, N.; Yoshikawa, N.; Ito, N.; Maruyama, T.; Suzuki, Y.; Takeda, S.; Nakae, J.; Tagata, Y.; Nishitani, S.; Takehana, K.; et al. Crosstalk between glucocorticoid receptor and nutritional sensor mTOR in skeletal muscle. Cell Metab. 2011, 13, 170–182. [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]
- Bodine, S.C.; Latres, E.; Baumhueter, S.; Lai, V.K.; Nunez, L.; Clarke, B.A.; Poueymirou, W.T.; Panaro, F.J.; Na, E.; Dharmarajan, K.; et al. Identification of ubiquitin ligases required for skeletal muscle atrophy. Science 2001, 294, 1704–1708. [Google Scholar] [CrossRef] [PubMed]
- Vainshtein, A.; Sandri, M. Signaling Pathways That Control Muscle Mass. Int. J. Mol. Sci. 2020, 21, 4759. [Google Scholar] [CrossRef]
- Vafaeipour, Z.; Razavi, B.M.; Hosseinzadeh, H. Effects of turmeric (Curcuma longa) and its constituent (curcumin) on the metabolic syndrome: An updated review. J. Integr. Med. 2022, 20, 193–203. [Google Scholar] [CrossRef] [PubMed]
- Uchio, R.; Higashi, Y.; Kohama, Y.; Kawasaki, K.; Hirao, T.; Muroyama, K.; Murosaki, S. A hot water extract of turmeric (Curcuma longa) suppresses acute ethanol-induced liver injury in mice by inhibiting hepatic oxidative stress and inflammatory cytokine production. J. Nutr. Sci. 2017, 6, e3. [Google Scholar] [CrossRef]
- Kunnumakkara, A.B.; Bordoloi, D.; Padmavathi, G.; Monisha, J.; Roy, N.K.; Prasad, S.; Aggarwal, B.B. Curcumin, the golden nutraceutical: Multitargeting for multiple chronic diseases. Br. J. Pharmacol. 2017, 174, 1325–1348. [Google Scholar] [CrossRef] [PubMed]
- Ashida, H.; Tian, X.; Kitakaze, T.; Yamashita, Y. Bisacurone suppresses hepatic lipid accumulation through inhibiting lipogenesis and promoting lipolysis. J. Clin. Biochem. Nutr. 2020, 67, 43–52. [Google Scholar] [CrossRef] [PubMed]
- Sun, D.-I.; Nizamutdinova, I.T.; Kim, Y.M.; Cai, X.F.; Lee, J.J.; Kang, S.S.; Kim, Y.S.; Kang, K.M.; Chai, G.Y.; Chang, K.C.; et al. Bisacurone inhibits adhesion of inflammatory monocytes or cancer cells to endothelial cells through down-regulation of VCAM-1 expression. Int. Immunopharmacol. 2008, 8, 1272–1281. [Google Scholar] [CrossRef]
- Ono, T.; Takada, S.; Kinugawa, S.; Tsutsui, H. Curcumin ameliorates skeletal muscle atrophy in type 1 diabetic mice by inhibiting protein ubiquitination. Exp. Physiol. 2015, 100, 1052–1063. [Google Scholar] [CrossRef]
- Jia, H.; Hanate, M.; Aw, W.; Itoh, H.; Saito, K.; Kobayashi, S.; Hachimura, S.; Fukuda, S.; Tomita, M.; Hasebe, Y.; et al. Eggshell membrane powder ameliorates intestinal inflammation by facilitating the restitution of epithelial injury and alleviating microbial dysbiosis. Sci. Rep. 2017, 7, 43993. [Google Scholar] [CrossRef]
- Furukawa, K.; Kono, M.; Kataoka, T.; Hasebe, Y.; Jia, H.; Kato, H. Effects of Eggshell Membrane on Keratinocyte Differentiation and Skin Aging In Vitro and In Vivo. Nutrients 2021, 13, 2144. [Google Scholar] [CrossRef]
- Kuo, T.; Liu, P.H.; Chen, T.C.; Lee, R.A.; New, J.; Zhang, D.; Lei, C.; Chau, A.; Tang, Y.; Cheung, E.; et al. Transcriptional Regulation of FoxO3 Gene by Glucocorticoids in Murine Myotubes. Am. J. Physiol. Endocrinol. Metab. 2016, 310, E572–E585. [Google Scholar] [CrossRef]
- Zhao, J.; Brault, J.J.; Schild, A.; Cao, P.; Sandri, M.; Schiaffino, S.; Lecker, S.H.; Goldberg, A.L. FoxO3 coordinately activates protein degradation by the autophagic/lysosomal and proteasomal pathways in atrophying muscle cells. Cell Metab. 2007, 6, 472–483. [Google Scholar] [CrossRef] [Green Version]
- Latres, E.; Amini, A.R.; Amini, A.A.; Griffiths, J.; Martin, F.J.; Wei, Y.; Lin, H.C.; Yancopoulos, G.D.; Glass, D.J. Insulin-like growth factor-1 (IGF-1) inversely regulates atrophy-induced genes via the phosphatidylinositol 3-kinase/Akt/mammalian target of rapamycin (PI3K/Akt/mTOR) pathway. J. Biol. Chem. 2005, 280, 2737–2744. [Google Scholar] [CrossRef]
- Stitt, T.N.; Drujan, D.; Clarke, B.A.; Panaro, F.; Timofeyva, Y.; Kline, W.O.; Gonzalez, M.; Yancopoulos, G.D.; Glass, D.J. The IGF-1/PI3K/Akt pathway prevents expression of muscle atrophy-induced ubiquitin ligases by inhibiting FOXO transcription factors. Mol. Cell 2004, 14, 395–403. [Google Scholar] [CrossRef]
- Britto, F.A.; Cortade, F.; Belloum, Y.; Blaquière, M.; Gallot, Y.S.; Docquier, A.; Pagano, A.F.; Jublanc, E.; Bendridi, N.; Koechlin-Ramonatxo, C.; et al. Glucocorticoid-dependent REDD1 expression reduces muscle metabolism to enable adaptation under energetic stress. BMC Biol. 2018, 16, 65. [Google Scholar] [CrossRef]
- Schakman, O.; Kalista, S.; Barbe, C.; Loumaye, A.; Thissen, J.P. Glucocorticoid-induced skeletal muscle atrophy. Int. J. Biochem. Cell Biol. 2013, 45, 2163–2172. [Google Scholar] [CrossRef]
- Asada, M.; Rauch, A.; Shimizu, H.; Maruyama, H.; Miyaki, S.; Shibamori, M.; Kawasome, H.; Ishiyama, H.; Tuckermann, J.; Asahara, H. DNA binding-dependent glucocorticoid receptor activity promotes adipogenesis via Krüppel-like factor 15 gene expression. Lab. Investig. 2011, 91, 203–215. [Google Scholar] [CrossRef] [PubMed]
- Tanganelli, F.; Meinke, P.; Hofmeister, F.; Jarmusch, S.; Baber, L.; Mehaffey, S.; Hintze, S.; Ferrari, U.; Neuerburg, C.; Kammerlander, C.; et al. Type-2 muscle fiber atrophy is associated with sarcopenia in elderly men with hip fracture. Exp. Gerontol. 2021, 144, 111171. [Google Scholar] [CrossRef] [PubMed]
- Augusto, V.; Padovani, C.; Eduardo, G.; Campos, R. Skeletal muscle fiber types in C57BL6J mice. J. Morphol. Sci. 2004, 21, 89–94. [Google Scholar]
- Balahbib, A.; El Omari, N.; Hachlafi, N.E.; Lakhdar, F.; El Menyiy, N.; Salhi, N.; Mrabti, H.N.; Bakrim, S.; Zengin, G.; Bouyahya, A. Health beneficial and pharmacological properties of p-cymene. Food Chem. Toxicol. 2021, 153, 112259. [Google Scholar] [CrossRef] [PubMed]
- Salehi, B.; Mishra, A.P.; Shukla, I.; Sharifi-Rad, M.; Contreras, M.d.M.; Segura-Carretero, A.; Fathi, H.; Nasrabadi, N.N.; Kobarfard, F.; Sharifi-Rad, J. Thymol, thyme, and other plant sources: Health and potential uses. Phytother. Res. 2018, 32, 1688–1706. [Google Scholar] [CrossRef]
- Meng, S.J.; Yu, L.J. Oxidative stress, molecular inflammation and sarcopenia. Int. J. Mol. Sci. 2010, 11, 1509–1526. [Google Scholar] [CrossRef]
- Sindhu, S.; Chempakam, B.; Leela, N.K.; Suseela Bhai, R. Chemoprevention by essential oil of turmeric leaves (Curcuma longa L.) on the growth of Aspergillus flavus and aflatoxin production. Food Chem. Toxicol. 2011, 49, 1188–1192. [Google Scholar] [CrossRef] [PubMed]
- Kang, D.-H.; Lee, Y.-S.; Oh, S.M.; Yoon, D.; Choi, D.J.; Kwon, D.-Y.; Kang, O.-H.; Lee, D.Y. Inhibitory Effects of Thymol Isolated from Curcuma longa L. on Adipogenesis in HepG2 Cells. Processes 2020, 8, 1191. [Google Scholar] [CrossRef]
- Ponnala, L.; Wang, Y.; Sun, Q.; van Wijk, K.J. Correlation of mRNA and protein abundance in the developing maize leaf. Plant J. 2014, 78, 424–440. [Google Scholar] [CrossRef] [PubMed]
Gene Symbol | Gene Name | Log Ratio (Dex vs. Con) |
---|---|---|
LCN2 | Lipocalin 2 | 7.43 |
CDKN1A | Cyclin Dependent Kinase Inhibitor 1A | 2.134 |
FOS | Fos Proto-Oncogene, AP-1 Transcription Factor Subunit | 1.912 |
GADD45B | Growth Arrest And DNA Damage Inducible Beta | 1.682 |
Mt1 | Metallothionein-1 | 1.535 |
Mt2 | Metallothionein-2 | 1.291 |
TPX2 | TPX2 Microtubule Nucleation Factor | 1.242 |
IRS2 | Insulin Receptor Substrate 2 | 1.079 |
FASN | Fatty Acid Synthase | 1.076 |
PPP1R15A | Protein Phosphatase 1 Regulatory Subunit 15A | 1.049 |
EGR1 | Early Growth Response 1 | 0.982 |
UBC | Ubiquitin C | 0.974 |
FBXO32 | F-Box Protein 32 | 0.906 |
MTHFD2 | Methylenetetrahydrofolate Dehydrogenase (NADP+ Dependent) 2 | 0.902 |
GABRR2 | Gamma-Aminobutyric Acid Type A Receptor Subunit Rho2 | 0.837 |
EIF4EBP1 | Eukaryotic Translation Initiation Factor 4E Binding Protein 1 | 0.79 |
JUNB | JunB Proto-Oncogene, AP-1 Transcription Factor Subunit | 0.738 |
BCL2L11 | BCL2-Like 11 | 0.733 |
OPTN | Optineurin | 0.677 |
CDKN1B | Cyclin Dependent Kinase Inhibitor 1B | 0.668 |
MAP1LC3A | Microtubule Associated Protein 1 Light Chain 3 Alpha | 0.633 |
PAK1 | P21 (RAC1) Activated Kinase 1 | −0.664 |
PTEN | Phosphatase And Tensin Homolog | −0.676 |
CCNE2 | Cyclin E2 | −0.726 |
GRB14 | Growth Factor Receptor Bound Protein 14 | −0.772 |
VCAM1 | Vascular Cell Adhesion Molecule 1 | −0.784 |
FMOD | Fibromodulin | −0.799 |
IGF1 | Insulin-Like Growth Factor 1 | −0.799 |
CCND1 | Cyclin D1 | −0.816 |
FN1 | Fibronectin 1 | −1.075 |
NFKBIA | NFKB Inhibitor Alpha | −1.296 |
TCIM | Transcriptional And Immune Response Regulator | −1.31 |
DDIT4 | DNA Damage Inducible Transcript 4 | −4.14 |
Gene Symbol | Gene Name | Log Ratio (DEX + TE vs. DEX) |
---|---|---|
SLC25A25 | Solute Carrier Family 25 Member 25 | 1.16 |
ADIPOQ | Adiponectin, C1Q And Collagen Domain Containing | 1.041 |
SCD | Stearoyl-CoA Desaturase | 0.888 |
TGFBI | Transforming Growth Factor Beta Induced | 0.787 |
IGF1 | Insulin-Like Growth Factor 1 | 0.733 |
C4A/C4B | Complement C4B (Chido Blood Group) | 0.679 |
COL3A1 | Collagen Type III Alpha 1 Chain | 0.677 |
FBXO32 | F-Box Protein 32 | −0.846 |
SLC20A1 | Solute Carrier Family 20 Member 1 | −0.997 |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 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
Furukawa, K.; Kousaka, M.; Jia, H.; Kato, H. Suppressive Effects of Turmeric Extract on Muscle Atrophy in Dexamethasone-Treated Mice and Myotubes. Nutrients 2022, 14, 3979. https://doi.org/10.3390/nu14193979
Furukawa K, Kousaka M, Jia H, Kato H. Suppressive Effects of Turmeric Extract on Muscle Atrophy in Dexamethasone-Treated Mice and Myotubes. Nutrients. 2022; 14(19):3979. https://doi.org/10.3390/nu14193979
Chicago/Turabian StyleFurukawa, Kyohei, Marika Kousaka, Huijuan Jia, and Hisanori Kato. 2022. "Suppressive Effects of Turmeric Extract on Muscle Atrophy in Dexamethasone-Treated Mice and Myotubes" Nutrients 14, no. 19: 3979. https://doi.org/10.3390/nu14193979