Anti-Obesity Effect of a Tea Mixture Nano-Formulation on Rats Occurs via the Upregulation of AMP-Activated Protein Kinase/Sirtuin-1/Glucose Transporter Type 4 and Peroxisome Proliferator-Activated Receptor Gamma Pathways
Abstract
:1. Introduction
2. Materials and Methods
2.1. General
2.2. Plant Material and Extraction
2.3. UPLC–HRMS-MS Analysis
2.4. Determination of Total Phenolics
2.5. Determination of Total Flavonoids
2.6. Pancreatic Lipase Inhibition
2.7. Alpha-Amylase Inhibition
2.8. Synthesis of Tea Extract Nanoparticles
2.9. Nanoparticle Characterization
2.10. The Experimental In Vivo Study
2.10.1. Animals
2.10.2. High-Fat Diet Induction
2.10.3. Experimental Design
2.10.4. Sample Collection and Biochemical Analysis
2.10.5. Adipose Tissue Collection and Analysis
2.10.6. Gene Expression and qRT-PCR
3. Results
3.1. Identification of Metabolites in the Tea Samples Following UPLC–HRMS-MS Analysis
3.2. Multivariate Analysis of Metabolic Differentiation of Green, White, and Oolong Tea Samples
3.3. Total Phenolics and Total Flavonoids
3.4. Pancreatic Lipase Inhibition
3.5. α-Amylase Inhibition
3.6. Shape Characterization
3.6.1. High-Resolution Transmission Electron Microscope (HRTEM) Observation
3.6.2. Atomic Force Microscope (AFM)
3.6.3. Size Characterization
Dynamic Light Scattering (DLS)
3.7. Effect of Conventional and Nano-Tea Mixture Extracts on Wister Rats’ Weight and Adipose Tissue Deposition
3.8. Effect of Herbal Treatment on Lipid Profile, Blood Glucose Levels, and Kidney and Liver Functions
3.9. Herbal Treatment with Conventional and Nano-Formulated Tea Managed to Control Adipocytokines and Anti-Inflammatory Values
3.10. Herbal Treatments with Conventional and Nano-Formulated Tea Managed to Control the Expression Levels of TNF-α, GLUT-4, Sirt-1, PPARγ, P-AMPK, and ADD1/SREP-1c
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Bhutani, K.K.; Birari, R.; Kapat, K. Potential anti-obesity and lipid lowering natural products: A review. Nat. Prod. Commun. 2007, 2, 331–348. [Google Scholar] [CrossRef]
- Blüher, M. Obesity: Global epidemiology and pathogenesis. Nat. Rev. Endocrinol. 2019, 15, 288–298. [Google Scholar] [CrossRef]
- Tran, B.X.; Dang, K.A.; Le, H.T.; Ha, G.H.; Nguyen, L.H.; Nguyen, T.H.; Tran, T.H.; Latkin, C.A.; Ho, C.S.; Ho, R.C. Global evolution of obesity research in children and youths: Setting priorities for interventions and policies. Obes. Facts 2019, 12, 137–149. [Google Scholar] [CrossRef]
- Srivastava, N.; Lakhan, R.; Mittal, B. Pathophysiology and genetics of obesity. Indian J. Exp. Biol. 2007, 45, 929–936. [Google Scholar]
- McKinney, L.; Skolnik, N.; Chrusch, A. Diagnosis and Management of Obesity; American Academy of Family Physicians: Leawood, KS, USA, 2013; pp. 7–8. [Google Scholar]
- Pi-Sunyer, F.X. The obesity epidemic: Pathophysiology and consequences of obesity. Obes. Res. 2002, 10, 97S–104S. [Google Scholar] [CrossRef]
- Cavaliere, H.; Floriano, I.; Medeiros-Neto, G. Gastrointestinal side effects of orlistat may be prevented by concomitant prescription of natural fibers (psyllium mucilloid). Int. J. Obes. 2001, 25, 1095–1099. [Google Scholar] [CrossRef] [Green Version]
- Sweeting, A.N.; Tabet, E.; Caterson, I.D.; Markovic, T.P. Management of obesity and cardiometabolic risk–role of phentermine/extended release topiramate. Diabetes Metab. Syndr. Obes. Targets Ther. 2014, 7, 35–44. [Google Scholar]
- Mohamed, G.A.; Ibrahim, S.R.M.; Elkhayat, E.S.; El Dine, R.S. Natural anti-obesity agents. Bull. Fac. Pharm. Cairo Univ. 2014, 52, 269–284. [Google Scholar] [CrossRef] [Green Version]
- Kim, S.; Lee, M.-S.; Jung, S.; Son, H.-Y.; Park, S.; Kang, B.; Kim, S.-Y.; Kim, I.-H.; Kim, C.-T.; Kim, Y. Ginger extract ameliorates obesity and inflammation via regulating microRNA-21/132 expression and AMPK activation in white adipose tissue. Nutrients 2018, 10, 1567. [Google Scholar] [CrossRef] [Green Version]
- Metwally, F.M.; Rashad, H.M.; Ahmed, H.H.; Mahmoud, A.A.; Raouf, E.R.A.; Abdalla, A.M. Molecular mechanisms of the anti-obesity potential effect of Moringa oleifera in the experimental model. Asian Pac. J. Trop. Biomed. 2017, 7, 214–221. [Google Scholar] [CrossRef]
- Zang, L.; Shimada, Y. Preventive Effects of Green Tea Extract against Obesity Development in Zebrafish. Molecules 2021, 26, 2627. [Google Scholar] [CrossRef]
- Sanlier, N.; Atik, İ.; Atik, A. A minireview of effects of white tea consumption on diseases. Trends Food Sci. Technol. 2018, 82, 82–88. [Google Scholar] [CrossRef]
- Han, L.K.; Takaku, T.; Li, J.; Kimura, Y.; Okuda, H. Anti-obesity action of oolong tea. Int. J. Obes. Relat. Metab. Disord. J. Int. Assoc. Study Obes. 1999, 23, 98–105. [Google Scholar] [CrossRef] [Green Version]
- Rains, T.M.; Agarwal, S.; Maki, K.C. Antiobesity effects of green tea catechins: A mechanistic review. J. Nutr. Biochem. 2011, 22, 1–7. [Google Scholar] [CrossRef]
- Tian, C.; Ye, X.; Zhang, R.; Long, J.; Ren, W.; Ding, S.; Liao, D.; Jin, X.; Wu, H.; Xu, S. Green tea polyphenols reduced fat deposits in high fat-fed rats via erk1/2-PPARγ-adiponectin pathway. PLoS ONE 2013, 8, e53796. [Google Scholar] [CrossRef]
- Söhle, J.; Knott, A.; Holtzmann, U.; Siegner, R.; Grönniger, E.; Schepky, A.; Gallinat, S.; Wenck, H.; Stäb, F.; Winnefeld, M. White Tea extract induces lipolytic activity and inhibits adipogenesis in human subcutaneous (pre)-adipocytes. Nutr. Metab. 2009, 6, 20. [Google Scholar] [CrossRef] [Green Version]
- Hassan, S.M.; Ibrahim, A.; Hassan, S.K.; Majeed, A.; Siddiqi, S.A.; Naeem, N. Importance of Nanotechnology: A Review. Lahore Garrison Univ. J. Life Sci. 2018, 2, 1–6. [Google Scholar] [CrossRef]
- Zhang, S.; Sun, S.; Wei, X.; Zhang, M.; Chen, Y.; Mao, X.; Chen, G.; Liu, C. Short-term moderate caloric restriction in a high-fat diet alleviates obesity via AMPK/SIRT1 signaling in white adipocytes and liver. Food Nutr. Res. 2022, 66. [Google Scholar] [CrossRef] [PubMed]
- Xu, F.; Chen, R.; Ma, C.; Tang, L.; Wan, W.; You, F.; Chen, L.; Li, J.; Chen, Z.; Liang, F. Electroacupuncture Improves Insulin Sensitivity in High-Fat Diet-Induced Insulin Resistant Rats by Activating SIRT1 and GLUT4 in Quadriceps Femoris. Acta Endocrinol. 2020, 16, 280. [Google Scholar] [CrossRef]
- Salem, M.A.; Aborehab, N.M.; Al-Karmalawy, A.A.; Fernie, A.R.; Alseekh, S.; Ezzat, S.M. Potential Valorization of Edible Nuts By-Products: Exploring the Immune-Modulatory and Antioxidants Effects of Selected Nut Shells Extracts in Relation to Their Metabolic Profiles. Antioxidants 2022, 11, 462. [Google Scholar] [CrossRef]
- Pang, Z.; Chong, J.; Zhou, G.; de Lima Morais, D.A.; Chang, L.; Barrette, M.; Gauthier, C.; Jacques, P.-É.; Li, S.; Xia, J. MetaboAnalyst 5.0: Narrowing the gap between raw spectra and functional insights. Nucleic Acids Res. 2021, 49, W388–W396. [Google Scholar] [CrossRef]
- Singleton, V.L.; Orthofer, R.; Lamuela-Raventós, R.M. [14] Analysis of total phenols and other oxidation substrates and antioxidants by means of folin-ciocalteu reagent. In Methods in Enzymology; Elsevier: Amsterdam, The Netherlands, 1999; Volume 299, pp. 152–178. [Google Scholar]
- Park, Y.-S.; Jung, S.-T.; Kang, S.-G.; Heo, B.G.; Arancibia-Avila, P.; Toledo, F.; Drzewiecki, J.; Namiesnik, J.; Gorinstein, S. Antioxidants and proteins in ethylene-treated kiwifruits. Food Chem. 2008, 107, 640–648. [Google Scholar] [CrossRef]
- Slanc, P.; Doljak, B.; Kreft, S.; Lunder, M.; Janeš, D.; Štrukelj, B. Screening of selected food and medicinal plant extracts for pancreatic lipase inhibition. Phytother. Res. Int. J. Devoted Pharmacol. Toxicol. Eval. Nat. Prod. Deriv. 2009, 23, 874–877. [Google Scholar] [CrossRef] [PubMed]
- Ali, H.; Houghton, P.; Soumyanath, A. α-Amylase inhibitory activity of some Malaysian plants used to treat diabetes; with particular reference to Phyllanthus amarus. J. Ethnopharmacol. 2006, 107, 449–455. [Google Scholar] [CrossRef]
- Youssef, F.; Mohamed, G.; Ismail, S.; Elzorba, H.; Galal, A.; Elbanna, H. Synthesis, characterization and in vitro antimicrobial activity of florfenicol-chitosan nanocomposite. Egypt. J. Chem. 2021, 64, 941–948. [Google Scholar] [CrossRef]
- Elabd, H.; Mahboub, H.H.; Salem, S.M.; Abdelwahab, A.M.; Alwutayd, K.M.; Shaalan, M.; Ismail, S.H.; Abdelfattah, A.M.; Khalid, A.; Mansour, A.T. Nano-Curcumin/Chitosan Modulates Growth, Biochemical, Immune, and Antioxidative Profiles, and the Expression of Related Genes in Nile tilapia, Oreochromis niloticus. Fishes 2023, 8, 333. [Google Scholar] [CrossRef]
- Mahboub, H.H.; Eltanahy, A.; Omran, A.; Mansour, A.T.; Safhi, F.A.; Alwutayd, K.M.; Khamis, T.; Husseiny, W.A.; Ismail, S.H.; Yousefi, M. Chitosan nanogel aqueous treatment improved blood biochemicals, antioxidant capacity, immune response, immune-related gene expression and infection resistance of Nile tilapia. Comp. Biochem. Physiol. Part B Biochem. Mol. Biol. 2023, 269, 110876. [Google Scholar] [CrossRef]
- Srinivasan, K.; Patole, P.; Kaul, C.; Ramarao, P. Reversal of glucose intolerance by pioglitazone in high fat diet-fed rats. Methods Find Exp Clin Pharmacol 2004, 26, 327–333. [Google Scholar] [CrossRef]
- Willems, J.L.; Khamis, M.M.; Mohammed Saeid, W.; Purves, R.W.; Katselis, G.; Low, N.H.; El-Aneed, A. Analysis of a series of chlorogenic acid isomers using differential ion mobility and tandem mass spectrometry. Anal. Chim. Acta 2016, 933, 164–174. [Google Scholar] [CrossRef]
- Salem, M.A.; Michel, H.E.; Ezzat, M.I.; Okba, M.M.; El-Desoky, A.M.; Mohamed, S.O.; Ezzat, S.M. Optimization of an Extraction Solvent for Angiotensin-Converting Enzyme Inhibitors from Hibiscus sabdariffa L. Based on Its UPLC-MS/MS Metabolic Profiling. Molecules 2020, 25, 307. [Google Scholar] [CrossRef]
- Ruan, J.; Yan, J.; Zheng, D.; Sun, F.; Wang, J.; Han, L.; Zhang, Y.; Wang, T. Comprehensive Chemical Profiling in the Ethanol Extract of Pluchea indica Aerial Parts by Liquid Chromatography/Mass Spectrometry Analysis of Its Silica Gel Column Chromatography Fractions. Molecules 2019, 24, 2784. [Google Scholar] [CrossRef] [Green Version]
- Li, P.; Dai, W.; Lu, M.; Xie, D.; Tan, J.; Yang, C.; Zhu, Y.; Lv, H.; Peng, Q.; Zhang, Y.; et al. Metabolomic analysis reveals the composition differences in 13 Chinese tea cultivars of different manufacturing suitabilities. J. Sci. Food Agric. 2018, 98, 1153–1161. [Google Scholar] [CrossRef]
- Lee, J.E.; Lee, B.J.; Chung, J.O.; Kim, H.N.; Kim, E.H.; Jung, S.; Lee, H.; Lee, S.J.; Hong, Y.S. Metabolomic unveiling of a diverse range of green tea (Camellia sinensis) metabolites dependent on geography. Food Chem. 2015, 174, 452–459. [Google Scholar] [CrossRef] [PubMed]
- Tao, W.; Zhou, Z.; Zhao, B.; Wei, T. Simultaneous determination of eight catechins and four theaflavins in green, black and oolong tea using new HPLC–MS–MS method. J. Pharm. Biomed. Anal. 2016, 131, 140–145. [Google Scholar] [CrossRef] [PubMed]
- Jang, W.S.; Choung, S.Y. Antiobesity effects of the ethanol extract of Laminaria japonica Areshoung in high-fat-diet-induced obese rat. Evid.-Based Complement. Altern. Med. 2013, 2013, 492807. [Google Scholar] [CrossRef] [Green Version]
- Chen, N.; Bezzina, R.; Hinch, E.; Lewandowski, P.A.; Cameron-Smith, D.; Mathai, M.L.; Jois, M.; Sinclair, A.J.; Begg, D.P.; Wark, J.D. Green tea, black tea, and epigallocatechin modify body composition, improve glucose tolerance, and differentially alter metabolic gene expression in rats fed a high-fat diet. Nutr. Res. 2009, 29, 784–793. [Google Scholar] [CrossRef]
- Yang, C.S.; Zhang, J.; Zhang, L.; Huang, J.; Wang, Y. Mechanisms of body weight reduction and metabolic syndrome alleviation by tea. Mol. Nutr. Food Res. 2016, 60, 160–174. [Google Scholar] [CrossRef] [Green Version]
- Teixeira, L.G.; Lages, P.C.; Jascolka, T.L.; Aguilar, E.C.; Soares, F.L.P.; Pereira, S.S.; Beltrão, N.R.M.; Matoso, R.d.O.; Nascimento, A.M.d.; Castilho, R.O.d. White tea (Camellia sinensis) extract reduces oxidative stress and triacylglycerols in obese mice. Food Sci. Technol. 2012, 32, 733–741. [Google Scholar] [CrossRef] [Green Version]
- Fardet, A.; Llorach, R.; Martin, J.-F.; Besson, C.; Lyan, B.; Pujos-Guillot, E.; Scalbert, A. A liquid chromatography− quadrupole time-of-flight (LC−QTOF)-based metabolomic approach reveals new metabolic effects of catechin in rats fed high-fat diets. J. Proteome Res. 2008, 7, 2388–2398. [Google Scholar] [CrossRef]
- Maki, K.C.; Reeves, M.S.; Farmer, M.; Yasunaga, K.; Matsuo, N.; Katsuragi, Y.; Komikado, M.; Tokimitsu, I.; Wilder, D.; Jones, F. Green tea catechin consumption enhances exercise-induced abdominal fat loss in overweight and obese adults. J. Nutr. 2009, 139, 264–270. [Google Scholar] [CrossRef] [Green Version]
- Kim, H.M.; Kim, J. The effects of green tea on obesity and type 2 diabetes. Diabetes Metab. J. 2013, 37, 173–175. [Google Scholar] [CrossRef] [Green Version]
- Liu, C.; Guo, Y.; Sun, L.; Lai, X.; Li, Q.; Zhang, W.; Xiang, L.; Sun, S.; Cao, F. Six types of tea reduce high-fat-diet-induced fat accumulation in mice by increasing lipid metabolism and suppressing inflammation. Food Funct. 2019, 10, 2061–2074. [Google Scholar] [CrossRef]
- Stern, J.H.; Rutkowski, J.M.; Scherer, P.E. Adiponectin, leptin, and fatty acids in the maintenance of metabolic homeostasis through adipose tissue crosstalk. Cell Metab. 2016, 23, 770–784. [Google Scholar] [CrossRef] [Green Version]
- Essex, K.; Mosawy, S. The anti-obesity potential of green tea: The effect on leptin and adiponectin. Clin. Immunol. Endocr. Metab. Drugs (Discontin.) 2017, 4, 14–18. [Google Scholar] [CrossRef] [Green Version]
- Auvichayapat, P.; Prapochanung, M.; Tunkamnerdthai, O.; Sripanidkulchai, B.-o.; Auvichayapat, N.; Thinkhamrop, B.; Kunhasura, S.; Wongpratoom, S.; Sinawat, S.; Hongprapas, P. Effectiveness of green tea on weight reduction in obese Thais: A randomized, controlled trial. Physiol. Behav. 2008, 93, 486–491. [Google Scholar] [CrossRef] [PubMed]
- de Freitas, L.M., Junior; de Almeida, E.B., Jr. Medicinal plants for the treatment of obesity: Ethnopharmacological approach and chemical and biological studies. Am. J. Transl. Res. 2017, 9, 2050. [Google Scholar]
- Herrera, B.M.; Lindgren, C.M. The genetics of obesity. Curr. Diabetes Rep. 2010, 10, 498–505. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Manna, P.; Achari, A.E.; Jain, S.K. Vitamin D supplementation inhibits oxidative stress and upregulate SIRT1/AMPK/GLUT4 cascade in high glucose-treated 3T3L1 adipocytes and in adipose tissue of high fat diet-fed diabetic mice. Arch. Biochem. Biophys. 2017, 615, 22–34. [Google Scholar] [CrossRef]
- Gong, P.; Xiao, X.; Wang, S.; Shi, F.; Liu, N.; Chen, X.; Yang, W.; Wang, L.; Chen, F. Hypoglycemic effect of astragaloside IV via modulating gut microbiota and regulating AMPK/SIRT1 and PI3K/AKT pathway. J. Ethnopharmacol. 2021, 281, 114558. [Google Scholar] [CrossRef]
- Yi, R.; Wang, R.; Sun, P.; Zhao, X. Antioxidant-mediated preventative effect of Dragon-pearl tea crude polyphenol extract on reserpine-induced gastric ulcers. Exp. Ther. Med. 2015, 10, 338–344. [Google Scholar] [CrossRef] [Green Version]
- Ahmadian, M.; Suh, J.M.; Hah, N.; Liddle, C.; Atkins, A.R.; Downes, M.; Evans, R.M. PPARγ signaling and metabolism: The good, the bad and the future. Nat. Med. 2013, 19, 557–566. [Google Scholar] [CrossRef] [Green Version]
- Barnea, M.; Shamay, A.; Stark, A.H.; Madar, Z. A high-fat diet has a tissue-specific effect on adiponectin and related enzyme expression. Obesity 2006, 14, 2145–2153. [Google Scholar] [CrossRef]
- Iwaki, M.; Matsuda, M.; Maeda, N.; Funahashi, T.; Matsuzawa, Y.; Makishima, M.; Shimomura, I. Induction of adiponectin, a fat-derived antidiabetic and antiatherogenic factor, by nuclear receptors. Diabetes 2003, 52, 1655–1663. [Google Scholar] [CrossRef] [Green Version]
- Tontonoz, P.; Spiegelman, B.M. Fat and beyond: The diverse biology of PPARγ. Annu. Rev. Biochem. 2008, 77, 289–312. [Google Scholar] [CrossRef] [PubMed]
- Wishart, D.S.; Guo, A.; Oler, E.; Wang, F.; Anjum, A.; Peters, H.; Dizon, R.; Sayeeda, Z.; Tian, S.; Lee, B.L.; et al. HMDB 5.0: The Human Metabolome Database for 2022. Nucleic Acids Res. 2022, 50, 622–631. [Google Scholar]
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Salem, M.A.; Aborehab, N.M.; Abdelhafez, M.M.; Ismail, S.H.; Maurice, N.W.; Azzam, M.A.; Alseekh, S.; Fernie, A.R.; Salama, M.M.; Ezzat, S.M. Anti-Obesity Effect of a Tea Mixture Nano-Formulation on Rats Occurs via the Upregulation of AMP-Activated Protein Kinase/Sirtuin-1/Glucose Transporter Type 4 and Peroxisome Proliferator-Activated Receptor Gamma Pathways. Metabolites 2023, 13, 871. https://doi.org/10.3390/metabo13070871
Salem MA, Aborehab NM, Abdelhafez MM, Ismail SH, Maurice NW, Azzam MA, Alseekh S, Fernie AR, Salama MM, Ezzat SM. Anti-Obesity Effect of a Tea Mixture Nano-Formulation on Rats Occurs via the Upregulation of AMP-Activated Protein Kinase/Sirtuin-1/Glucose Transporter Type 4 and Peroxisome Proliferator-Activated Receptor Gamma Pathways. Metabolites. 2023; 13(7):871. https://doi.org/10.3390/metabo13070871
Chicago/Turabian StyleSalem, Mohamed A., Nora M. Aborehab, Mai M. Abdelhafez, Sameh H. Ismail, Nadine W. Maurice, May A. Azzam, Saleh Alseekh, Alisdair R. Fernie, Maha M. Salama, and Shahira M. Ezzat. 2023. "Anti-Obesity Effect of a Tea Mixture Nano-Formulation on Rats Occurs via the Upregulation of AMP-Activated Protein Kinase/Sirtuin-1/Glucose Transporter Type 4 and Peroxisome Proliferator-Activated Receptor Gamma Pathways" Metabolites 13, no. 7: 871. https://doi.org/10.3390/metabo13070871