| ORIGINAL ARTICLES |
|
|
|
|
|
Modulation of mitochondrial activity by sugarcane (Saccharum officinarum L.) top extract and its bioactive polyphenols: a comprehensive transcriptomics analysis in C2C12 myotubes and HepG2 hepatocytes |
| Kengo Iwata1,2, Farhana Ferdousi1,3, Yoshinobu Arai2, Hiroko Isoda1,3,4 |
1. Alliance for Research on the Mediterranean and North Africa (ARENA), University of Tsukuba, Tsukuba, Ibaraki, 305-8572, Japan;
2. Nippo Co., Ltd., Daito, Osaka, 574-0062, Japan;
3. Institute of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Ibaraki, 305-8572, Japan;
4. AIST-University of Tsukuba Open Innovation Laboratory for Food and Medicinal Resource Engineering (FoodMed-OIL), Tsukuba, Ibaraki, 305-8572, Japan |
|
|
|
|
Abstract Age-related mitochondrial dysfunction leads to defects in cellular energy metabolism and oxidative stress defense systems, which can contribute to tissue damage and disease development. Among the key regulators responsible for mitochondrial quality control, peroxisome proliferator-activated receptor gamma coactivator 1-alpha (PGC-1α) is an important target for mitochondrial dysfunction. We have previously reported that bioactive polyphenols extracted from sugarcane top (ST) ethanol extract (STEE) could activate neuronal energy metabolism and increase astrocyte PGC-1α transcript levels. However, their potential impact on the mitochondria activity in muscle and liver cells has not yet been investigated. To address this gap, our current study examined the effects of STEE and its polyphenols on cultured myotubes and hepatocytes in vitro. Rhodamine 123 assay revealed that the treatment with STEE and its polyphenols resulted in an increase in mitochondrial membrane potential in C2C12 myotubes. Furthermore, a comprehensive examination of gene expression patterns through transcriptome-wide microarray analysis indicated that STEE altered gene expressions related to mitochondrial functions, fatty acid metabolism, inflammatory cytokines, mitogen-activated protein kinase (MAPK) signaling, and cAMP signaling in both C2C12 myotubes and HepG2 hepatocytes. Additionally, protein–protein interaction analysis identified the PGC-1α interactive-transcription factors-targeted regulatory network of the genes regulated by STEE, and the quantitative polymerase chain reaction results confirmed that STEE and its polyphenols upregulated the transcript levels of PGC-1α in both C2C12 and HepG2 cells. These findings collectively suggest the potential beneficial effects of STEE on muscle and liver tissues and offer novel insights into the potential nutraceutical applications of this material.
|
| Keywords
Sugarcane top
Polyphenol
Mitochondria
PGC-1α
Fatty acid metabolism
Inflammatory cytokine
|
| Fund:This work was partially funded by Nippo Co., Ltd., Japan Science and Technology Agency (JST COI-NEXT, grant no. JPMJPF2017). |
|
Corresponding Authors:
Hiroko Isoda,E-mail:isoda.hiroko.ga@u.tsukuba.ac.jp
E-mail: isoda.hiroko.ga@u.tsukuba.ac.jp
|
|
Issue Date: 19 February 2024
|
|
|
[1] Sun N, Youle RJ, Finkel T. The mitochondrial basis of aging. Mol Cell. 2016;61(5):654–66. https://doi.org/10.1016/j.molcel.2016.01.028.
[2] Sharma A, Smith HJ, Yao P, Mair WB. Causal roles of mitochondrial dynamics in longevity and healthy aging. EMBO Rep. 2019;20(12): e48395. https://doi.org/10.15252/embr.201948395.
[3] Lima T, Li TY, Mottis A, Auwerx J. Pleiotropic effects of mitochondria in aging. Nat Aging. 2022;2(3):199–213. https://doi.org/10.1038/s43587-022-00191-2.
[4] Kim Y, Triolo M, Hood DA. Impact of aging and exercise on mitochondrial quality control in skeletal muscle. Oxid Med Cell Longev. 2017;2017:3165396. https://doi.org/10.1155/2017/3165396.
[5] Ploumi C, Daskalaki I, Tavernarakis N. Mitochondrial biogenesis and clearance: a balancing act. FEBS J. 2017;284(2):183–95. https://doi.org/10.1111/febs.13820.
[6] Abu Shelbayeh O, Arroum T, Morris S, Busch KB. PGC-1α is a master regulator of mitochondrial lifecycle and ROS stress response. Antioxidants (Basel). 2023. https://doi.org/10.3390/antiox12051075.
[7] Wu Z, Puigserver P, Andersson U, Zhang C, Adelmant G, Mootha V, Troy A, Cinti S, Lowell B, Scarpulla RC, Spiegelman BM. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell. 1999;98(1):115–24. https://doi.org/10.1016/S0092-8674(00)80611-X.
[8] Settembre C, Di Malta C, Polito VA, Garcia Arencibia M, Vetrini F, Erdin S, Erdin SU, Huynh T, Medina D, Colella P, Sardiello M, Rubinsztein DC, Ballabio A. TFEB links autophagy to lysosomal biogenesis. Science. 2011;332(6036):1429–33. https://doi.org/10.1126/science.1204592.
[9] Chowanadisai W, Bauerly KA, Tchaparian E, Wong A, Cortopassi GA, Rucker RB. Pyrroloquinoline quinone stimulates mitochondrial biogenesis through cAMP response element-binding protein phosphorylation and increased PGC-1alpha expression. J Biol Chem. 2010;285(1):142–52. https://doi.org/10.1074/jbc.M109.030130.
[10] Herzig S, Shaw RJ. AMPK: guardian of metabolism and mitochondrial homeostasis. Nat Rev Mol Cell Biol. 2018;19(2):121–35. https://doi.org/10.1038/nrm.2017.95.
[11] Akimoto T, Pohnert SC, Li P, Zhang M, Gumbs C, Rosenberg PB, Williams RS, Yan Z. Exercise stimulates Pgc-1alpha transcription in skeletal muscle through activation of the p38 MAPK pathway. J Biol Chem. 2005;280(20):19587–93. https://doi.org/10.1074/jbc.M408862200.
[12] Kadomatsu T, Oike Y. Healthy aging based on suppression of chronic inflammation and enhanced mitochondrial homeostasis. Anti-aging Med. 2021;17(4):352–7.
[13] Iwata K, Wu Q, Ferdousi F, Sasaki K, Tominaga K, Uchida H, Arai Y, Szele FG, Isoda H. Sugarcane (Saccharum officinarum L.) top extract ameliorates cognitive decline in senescence model SAMP8 mice: modulation of neural development and energy metabolism. Front Cell Dev Biol. 2020;8: 573487. https://doi.org/10.3389/fcell.2020.573487.
[14] Iwata K, Ferdousi F, Arai Y, Isoda H. Interactions between major bioactive polyphenols of sugarcane top: effects on human neural stem cell differentiation and astrocytic maturation. Int J Mol Sci. 2022. https://doi.org/10.3390/ijms232315120.
[15] Mansouri A, Gattolliat CH, Asselah T. Mitochondrial dysfunction and signaling in chronic liver diseases. Gastroenterology. 2018;155(3):629–47. https://doi.org/10.1053/j.gastro.2018.06.083.
[16] Paradies G, Paradies V, Ruggiero FM, Petrosillo G. Oxidative stress, cardiolipin and mitochondrial dysfunction in nonalcoholic fatty liver disease. World J Gastroenterol. 2014;20(39):14205–18. https://doi.org/10.3748/wjg.v20.i39.14205.
[17] Abrigo J, Simon F, Cabrera D, Vilos C, Cabello-Verrugio C. Mitochondrial dysfunction in skeletal muscle pathologies. Curr Protein Pept Sci. 2019;20(6):536–46. https://doi.org/10.2174/1389203720666190402100902.
[18] Marzetti E, Calvani R, Cesari M, Buford TW, Lorenzi M, Behnke BJ, Leeuwenburgh C. Mitochondrial dysfunction and sarcopenia of aging: from signaling pathways to clinical trials. Int J Biochem Cell Biol. 2013;45(10):2288–301. https://doi.org/10.1016/j.biocel.2013.06.024.
[19] Ong KW, Hsu A, Tan BK. Chlorogenic acid stimulates glucose transport in skeletal muscle via AMPK activation: a contributor to the beneficial effects of coffee on diabetes. PLoS ONE. 2012;7(3): e32718. https://doi.org/10.1371/journal.pone.0032718.
[20] Takahashi S, Saito K, Li X, Jia H, Kato H. iTRAQ-based quantitative proteomics reveals the energy metabolism alterations induced by chlorogenic acid in HepG2 cells. Nutrients. 2022. https://doi.org/10.3390/nu14081676.
[21] Mthembu SXH, Muller CJF, Dludla PV, Madoroba E, Kappo AP, Mazibuko-Mbeje SE. Rooibos flavonoids, aspalathin, isoorientin, and orientin ameliorate antimycin A-induced mitochondrial dysfunction by improving mitochondrial bioenergetics in cultured skeletal muscle cells. Molecules. 2021. https://doi.org/10.3390/molecules26206289.
[22] Fan X, Lv H, Wang L, Deng X, Ci X. Isoorientin ameliorates APAP-induced hepatotoxicity via activation Nrf2 antioxidative pathway: the involvement of AMPK/Akt/GSK3β. Front Pharmacol. 2018;9:1334. https://doi.org/10.3389/fphar.2018.01334.
[23] Lim JH, Park HS, Choi JK, Lee IS, Choi HJ. Isoorientin induces Nrf2 pathway-driven antioxidant response through phosphatidylinositol 3-kinase signaling. Arch Pharmacal Res. 2007;30(12):1590–8. https://doi.org/10.1007/bf02977329.
[24] Skou JC, Esmann M. The Na, K-ATPase. J Bioenerg Biomembr. 1992;24(3):249–61. https://doi.org/10.1007/bf00768846.
[25] Imamura H, Nakano M, Noji H, Muneyuki E, Ohkuma S, Yoshida M, Yokoyama K. Evidence for rotation of V1-ATPase. Proc Natl Acad Sci U S A. 2003;100(5):2312–5. https://doi.org/10.1073/pnas.0436796100.
[26] Fernández-Moncada I, Barros LF. Non-preferential fuelling of the Na(+)/K(+)-ATPase pump. Biochem J. 2014;460(3):353–61. https://doi.org/10.1042/bj20140003.
[27] Croft D, O’Kelly G, Wu G, Haw R, Gillespie M, Matthews L, Caudy M, Garapati P, Gopinath G, Jassal B, Jupe S, Kalatskaya I, Mahajan S, May B, Ndegwa N, Schmidt E, Shamovsky V, Yung C, Birney E, Hermjakob H, D’Eustachio P, Stein L. Reactome: a database of reactions, pathways and biological processes. Nucleic Acids Res. 2011;39(Database issue6):D691–7. https://doi.org/10.1093/nar/gkq1018.
[28] Kanehisa M, Furumichi M, Tanabe M, Sato Y, Morishima K. KEGG: new perspectives on genomes, pathways, diseases and drugs. Nucleic Acids Res. 2017;45(D1):D353–61. https://doi.org/10.1093/nar/gkw1092.
[29] Han H, Shim H, Shin D, Shim JE, Ko Y, Shin J, Kim H, Cho A, Kim E, Lee T, Kim H, Kim K, Yang S, Bae D, Yun A, Kim S, Kim CY, Cho HJ, Kang B, Shin S, Lee I. TRRUST: a reference database of human transcriptional regulatory interactions. Sci Rep. 2015;5(1):11432. https://doi.org/10.1038/srep11432.
[30] Consortium EP. The ENCODE (ENCyclopedia Of DNA Elements) Project. Science. 2004;306(5696):636–40. https://doi.org/10.1126/science.1105136.
[31] Puigserver P, Rhee J, Donovan J, Walkey CJ, Yoon JC, Oriente F, Kitamura Y, Altomonte J, Dong H, Accili D, Spiegelman BM. Insulin-regulated hepatic gluconeogenesis through FOXO1-PGC-1alpha interaction. Nature. 2003;423(6939):550–5. https://doi.org/10.1038/nature01667.
[32] Scarpulla RC. Metabolic control of mitochondrial biogenesis through the PGC-1 family regulatory network. Biochim Biophys Acta. 2011;1813(7):1269–78. https://doi.org/10.1016/j.bbamcr.2010.09.019.
[33] Rui L. Energy metabolism in the liver. Compr Physiol. 2014;4(1):177–97. https://doi.org/10.1002/cphy.c130024.
[34] Ramsell KD, Zhao B-G, Baker D, Cobbett P. Serum modulates cyclic AMP-dependent morphological changes in cultured neurohypophysial astrocytes. Brain Res Bull. 1996;39(2):109–14. https://doi.org/10.1016/0361-9230(95)02057-8.
[35] Zorec R, Horvat A, Vardjan N, Verkhratsky A. Memory formation shaped by astroglia. Front Integr Neurosci. 2015;9:56. https://doi.org/10.3389/fnint.2015.00056.
[36] Zehnder T, Petrelli F, Romanos J, De Oliveira Figueiredo EC, Lewis TL Jr, Deglon N, Polleux F, Santello M, Bezzi P. Mitochondrial biogenesis in developing astrocytes regulates astrocyte maturation and synapse formation. Cell Rep. 2021;35(2): 108952. https://doi.org/10.1016/j.celrep.2021.108952.
[37] Valsecchi F, Ramos-Espiritu LS, Buck J, Levin LR, Manfredi G. cAMP and mitochondria. Physiology (Bethesda). 2013;28(3):199–209. https://doi.org/10.1152/physiol.00004.2013.
[38] Bos JL. Epac: a new cAMP target and new avenues in cAMP research. Nat Rev Mol Cell Biol. 2003;4(9):733–8. https://doi.org/10.1038/nrm1197.
[39] Wittköpper K, Dobrev D, Eschenhagen T, El-Armouche A. Phosphatase-1 inhibitor-1 in physiological and pathological β-adrenoceptor signalling. Cardiovasc Res. 2011;91(3):392–401. https://doi.org/10.1093/cvr/cvr058.
[40] Acin-Perez R, Salazar E, Kamenetsky M, Buck J, Levin LR, Manfredi G. Cyclic AMP produced inside mitochondria regulates oxidative phosphorylation. Cell Metab. 2009;9(3):265–76. https://doi.org/10.1016/j.cmet.2009.01.012.
[41] Schwoch G, Trinczek B, Bode C. Localization of catalytic and regulatory subunits of cyclic AMP-dependent protein kinases in mitochondria from various rat tissues. Biochem J. 1990;270(1):181–8. https://doi.org/10.1042/bj2700181.
[42] Acin-Perez R, Gatti DL, Bai Y, Manfredi G. Protein phosphorylation and prevention of cytochrome oxidase inhibition by ATP: coupled mechanisms of energy metabolism regulation. Cell Metab. 2011;13(6):712–9. https://doi.org/10.1016/j.cmet.2011.03.024.
[43] Wang Y, Hekimi S. Understanding ubiquinone. Trends Cell Biol. 2016;26(5):367–78. https://doi.org/10.1016/j.tcb.2015.12.007.
[44] Acin-Perez R, Salazar E, Brosel S, Yang H, Schon EA, Manfredi G. Modulation of mitochondrial protein phosphorylation by soluble adenylyl cyclase ameliorates cytochrome oxidase defects. EMBO Mol Med. 2009;1(8–9):392–406. https://doi.org/10.1002/emmm.200900046.
[45] Evans MJ, Scarpulla RC. NRF-1: a trans-activator of nuclear-encoded respiratory genes in animal cells. Genes Dev. 1990;4(6):1023–34. https://doi.org/10.1101/gad.4.6.1023.
[46] Taherzadeh-Fard E, Saft C, Akkad DA, Wieczorek S, Haghikia A, Chan A, Epplen JT, Arning L. PGC-1alpha downstream transcription factors NRF-1 and TFAM are genetic modifiers of Huntington disease. Mol Neurodegener. 2011;6(1):32. https://doi.org/10.1186/1750-1326-6-32.
[47] Herzig S, Long F, Jhala US, Hedrick S, Quinn R, Bauer A, Rudolph D, Schutz G, Yoon C, Puigserver P, Spiegelman B, Montminy M. CREB regulates hepatic gluconeogenesis through the coactivator PGC-1. Nature. 2001;413(6852):179–83. https://doi.org/10.1038/35093131.
[48] Murphy MP. How mitochondria produce reactive oxygen species. Biochem J. 2009;417(1):1–13. https://doi.org/10.1042/bj20081386.
[49] Ventura-Clapier R, Moulin M, Piquereau J, Lemaire C, Mericskay M, Veksler V, Garnier A. Mitochondria: a central target for sex differences in pathologies. Clin Sci (Lond). 2017;131(9):803–22. https://doi.org/10.1042/cs20160485.
[50] Zhang Z, Zhang X, Meng L, Gong M, Li J, Shi W, Qiu J, Yang Y, Zhao J, Suo Y, Liang X, Wang X, Tse G, Jiang N, Li G, Zhao Y, Liu T. Pioglitazone inhibits diabetes-induced atrial mitochondrial oxidative stress and improves mitochondrial biogenesis, dynamics, and function through the PPAR-γ/PGC-1α signaling pathway. Front Pharmacol. 2021;12: 658362. https://doi.org/10.3389/fphar.2021.658362.
[51] Archer SL. Mitochondrial dynamics–mitochondrial fission and fusion in human diseases. N Engl J Med. 2013;369(23):2236–51. https://doi.org/10.1056/NEJMra1215233.
[52] Xiong S, Patrushev N, Forouzandeh F, Hilenski L, Alexander RW. PGC-1α modulates telomere function and DNA damage in protecting against aging-related chronic diseases. Cell Rep. 2015;12(9):1391–9. https://doi.org/10.1016/j.celrep.2015.07.047.
[53] Sahin E, Colla S, Liesa M, Moslehi J, Müller FL, Guo M, Cooper M, Kotton D, Fabian AJ, Walkey C, Maser RS, Tonon G, Foerster F, Xiong R, Wang YA, Shukla SA, Jaskelioff M, Martin ES, Heffernan TP, Protopopov A, Ivanova E, Mahoney JE, Kost-Alimova M, Perry SR, Bronson R, Liao R, Mulligan R, Shirihai OS, Chin L, DePinho RA. Telomere dysfunction induces metabolic and mitochondrial compromise. Nature. 2011;470(7334):359–65. https://doi.org/10.1038/nature09787.
[54] Watkins PA. Very-long-chain acyl-CoA synthetases. J Biol Chem. 2008;283(4):1773–7. https://doi.org/10.1074/jbc.R700037200.
[55] Schroeder F, Petrescu AD, Huang H, Atshaves BP, McIntosh AL, Martin GG, Hostetler HA, Vespa A, Landrock D, Landrock KK, Payne HR, Kier AB. Role of fatty acid binding proteins and long chain fatty acids in modulating nuclear receptors and gene transcription. Lipids. 2008;43(1):1–17. https://doi.org/10.1007/s11745-007-3111-z.
[56] Hoffman DL, Brookes PS. Oxygen sensitivity of mitochondrial reactive oxygen species generation depends on metabolic conditions. J Biol Chem. 2009;284(24):16236–45. https://doi.org/10.1074/jbc.M809512200.
[57] Mantena SK, Vaughn DP, Andringa KK, Eccleston HB, King AL, Abrams GA, Doeller JE, Kraus DW, Darley-Usmar VM, Bailey SM. High fat diet induces dysregulation of hepatic oxygen gradients and mitochondrial function in vivo. Biochem J. 2009;417(1):183–93. https://doi.org/10.1042/bj20080868.
[58] Li LO, Mashek DG, An J, Doughman SD, Newgard CB, Coleman RA. Overexpression of rat long chain acyl-coa synthetase 1 alters fatty acid metabolism in rat primary hepatocytes. J Biol Chem. 2006;281(48):37246–55. https://doi.org/10.1074/jbc.M604427200.
[59] Makowski L, Hotamisligil GS. Fatty acid binding proteins–the evolutionary crossroads of inflammatory and metabolic responses. J Nutr. 2004;134(9):2464s-s2468. https://doi.org/10.1093/jn/134.9.2464S.
[60] Hardwick JP. Cytochrome P450 omega hydroxylase (CYP4) function in fatty acid metabolism and metabolic diseases. Biochem Pharmacol. 2008;75(12):2263–75. https://doi.org/10.1016/j.bcp.2008.03.004.
[61] Hardwick JP, Osei-Hyiaman D, Wiland H, Abdelmegeed MA, Song BJ. PPAR/RXR regulation of fatty acid metabolism and fatty acid omega-hydroxylase (CYP4) isozymes: implications for prevention of lipotoxicity in fatty liver disease. PPAR Res. 2009;2009: 952734. https://doi.org/10.1155/2009/952734.
[62] Evans JL, Goldfine ID, Maddux BA, Grodsky GM. Oxidative stress and stress-activated signaling pathways: a unifying hypothesis of type 2 diabetes. Endocr Rev. 2002;23(5):599–622. https://doi.org/10.1210/er.2001-0039.
[63] Eisele PS, Handschin C. Functional crosstalk of PGC-1 coactivators and inflammation in skeletal muscle pathophysiology. Semin Immunopathol. 2014;36(1):27–53. https://doi.org/10.1007/s00281-013-0406-4.
[64] Li X, Moody MR, Engel D, Walker S, Clubb FJ Jr, Sivasubramanian N, Mann DL, Reid MB. Cardiac-specific overexpression of tumor necrosis factor-alpha causes oxidative stress and contractile dysfunction in mouse diaphragm. Circulation. 2000;102(14):1690–6. https://doi.org/10.1161/01.cir.102.14.1690.
[65] Goodpaster BH, Park SW, Harris TB, Kritchevsky SB, Nevitt M, Schwartz AV, Simonsick EM, Tylavsky FA, Visser M, Newman AB, Study ftHA. The loss of skeletal muscle strength, mass, and quality in older adults: the health, aging and body composition study. J Gerontol Ser A. 2006;61(10):1059–64. https://doi.org/10.1093/gerona/61.10.1059.
[66] Tuttle CSL, Thang LAN, Maier AB. Markers of inflammation and their association with muscle strength and mass: a systematic review and meta-analysis. Ageing Res Rev. 2020;64: 101185. https://doi.org/10.1016/j.arr.2020.101185.
[67] Dalakas MC. Immunotherapy of myositis: issues, concerns and future prospects. Nat Rev Rheumatol. 2010;6(3):129–37. https://doi.org/10.1038/nrrheum.2010.2.
[68] Syriga M, Mavroidis M. Complement system activation in cardiac and skeletal muscle pathology: friend or foe? Adv Exp Med Biol. 2013;735:207–18. https://doi.org/10.1007/978-1-4614-4118-2_14.
[69] Legoedec J, Gasque P, Jeanne JF, Scotte M, Fontaine M. Complement classical pathway expression by human skeletal myoblasts in vitro. Mol Immunol. 1997;34(10):735–41. https://doi.org/10.1016/s0161-5890(97)00093-x.
[70] Liang Z, Zhang T, Liu H, Li Z, Peng L, Wang C, Wang T. Inflammaging: the ground for sarcopenia? Exp Gerontol. 2022;168: 111931. https://doi.org/10.1016/j.exger.2022.111931.
[71] Silveira LR, Pilegaard H, Kusuhara K, Curi R, Hellsten Y. The contraction induced increase in gene expression of peroxisome proliferator-activated receptor (PPAR)-gamma coactivator 1alpha (PGC-1alpha), mitochondrial uncoupling protein 3 (UCP3) and hexokinase II (HKII) in primary rat skeletal muscle cells is dependent on reactive oxygen species. Biochim Biophys Acta. 2006;1763(9):969–76. https://doi.org/10.1016/j.bbamcr.2006.06.010.
[72] Hirata Y, Takahashi M, Morishita T, Noguchi T, Matsuzawa A. Post-translational modifications of the TAK1-TAB complex. Int J Mol Sci. 2017. https://doi.org/10.3390/ijms18010205.
[73] Kim YH, Jung JI, Jeon YE, Kim SM, Oh TK, Lee J, Moon JM, Kim TY, Kim EJ. Gynostemma pentaphyllum extract and Gypenoside L enhance skeletal muscle differentiation and mitochondrial metabolism by activating the PGC-1α pathway in C2C12 myotubes. Nutr Res Pract. 2022;16(1):14–32. https://doi.org/10.4162/nrp.2022.16.1.14.
[74] Ni HY, Yu L, Zhao XL, Wang LT, Zhao CJ, Huang H, Zhu HL, Efferth T, Gu CB, Fu YJ. Seed oil of Rosa roxburghii Tratt against non-alcoholic fatty liver disease in vivo and in vitro through PPARα/PGC-1α-mediated mitochondrial oxidative metabolism. Phytomedicine. 2022;98: 153919. https://doi.org/10.1016/j.phymed.2021.153919.
[75] Ao X, Yan J, Liu S, Chen S, Zou L, Yang Y, He L, Li S, Liu A, Zhao K. Extraction, isolation and identification of four phenolic compounds from Pleioblastus amarus shoots and their antioxidant and anti-inflammatory properties in vitro. Food Chem. 2022;374: 131743. https://doi.org/10.1016/j.foodchem.2021.131743.
[76] Liu R, Sun Y, Wu H, Ni S, Wang J, Li T, Bi Y, Feng X, Zhang C, Sun Y. In-depth investigation of the effective substances of traditional Chinese medicine formula based on the novel concept of co-decoction reaction-using Zuojin decoction as a model sample. J Chromatogr B Analyt Technol Biomed Life Sci. 2021;1179: 122869. https://doi.org/10.1016/j.jchromb.2021.122869.
[77] Ornitz DM, Itoh N. The fibroblast growth factor signaling pathway. Wiley Interdiscip Rev Dev Biol. 2015;4(3):215–66. https://doi.org/10.1002/wdev.176.
[78] Prudovsky I. Cellular mechanisms of FGF-stimulated tissue repair. Cells. 2021. https://doi.org/10.3390/cells10071830.
[79] Wei EQ, Barnett AS, Pitt GS, Hennessey JA. Fibroblast growth factor homologous factors in the heart: a potential locus for cardiac arrhythmias. Trends Cardiovasc Med. 2011;21(7):199–203. https://doi.org/10.1016/j.tcm.2012.05.010.
[80] Ginis I, Luo Y, Miura T, Thies S, Brandenberger R, Gerecht-Nir S, Amit M, Hoke A, Carpenter MK, Itskovitz-Eldor J, Rao MS. Differences between human and mouse embryonic stem cells. Dev Biol. 2004;269(2):360–80. https://doi.org/10.1016/j.ydbio.2003.12.034.
[81] Mullen PJ, Zahno A, Lindinger P, Maseneni S, Felser A, Krähenbühl S, Brecht K. Susceptibility to simvastatin-induced toxicity is partly determined by mitochondrial respiration and phosphorylation state of Akt. Biochim Biophys Acta. 2011;1813(12):2079–87. https://doi.org/10.1016/j.bbamcr.2011.07.019.
[82] Breiter T, Laue C, Kressel G, Groll S, Engelhardt UH, Hahn A. Bioavailability and antioxidant potential of rooibos flavonoids in humans following the consumption of different rooibos formulations. Food Chem. 2011;128(2):338–47. https://doi.org/10.1016/j.foodchem.2011.03.029.
[83] Renouf M, Marmet C, Giuffrida F, Lepage M, Barron D, Beaumont M, Williamson G, Dionisi F. Dose-response plasma appearance of coffee chlorogenic and phenolic acids in adults. Mol Nutr Food Res. 2014;58(2):301–9. https://doi.org/10.1002/mnfr.201300349.
[84] Kumar P, Nagarajan A, Uchil PD. Analysis of cell viability by the MTT assay. Cold Spring Harb Protoc. 2018. https://doi.org/10.1101/pdb.prot095505.
[85] Fujihara T, Nakagawa-Izumi A, Ozawa T, Numata O. High-molecular-weight polyphenols from oolong tea and black tea: purification, some properties, and role in increasing mitochondrial membrane potential. Biosci Biotechnol Biochem. 2007;71(3):711–9. https://doi.org/10.1271/bbb.60562.
[86] Johnson LV, Walsh ML, Chen LB. Localization of mitochondria in living cells with rhodamine 123. Proc Natl Acad Sci U S A. 1980;77(2):990–4. https://doi.org/10.1073/pnas.77.2.990.
[87] Zhou Y, Zhou B, Pache L, Chang M, Khodabakhshi AH, Tanaseichuk O, Benner C, Chanda SK. Metascape provides a biologist-oriented resource for the analysis of systems-level datasets. Nat Commun. 2019;10(1):1523. https://doi.org/10.1038/s41467-019-09234-6.
[88] Xie Z, Bailey A, Kuleshov MV, Clarke DJB, Evangelista JE, Jenkins SL, Lachmann A, Wojciechowicz ML, Kropiwnicki E, Jagodnik KM, Jeon M, Ma’ayan A. Gene set knowledge discovery with enrichr. Curr Protoc. 2021;1(3): e90. https://doi.org/10.1002/cpz1.90.
[89] Chen EY, Tan CM, Kou Y, Duan Q, Wang Z, Meirelles GV, Clark NR, Ma’ayan A. Enrichr: interactive and collaborative HTML5 gene list enrichment analysis tool. BMC Bioinform. 2013;14:128. https://doi.org/10.1186/1471-2105-14-128.
[90] Kuleshov MV, Jones MR, Rouillard AD, Fernandez NF, Duan Q, Wang Z, Koplev S, Jenkins SL, Jagodnik KM, Lachmann A, McDermott MG, Monteiro CD, Gundersen GW, Ma’ayan A. Enrichr: a comprehensive gene set enrichment analysis web server 2016 update. Nucleic Acids Res. 2016;44(W1):W90–7. https://doi.org/10.1093/nar/gkw377.
[91] Breuer K, Foroushani AK, Laird MR, Chen C, Sribnaia A, Lo R, Winsor GL, Hancock RE, Brinkman FS, Lynn DJ. InnateDB: systems biology of innate immunity and beyond—recent updates and continuing curation. Nucleic Acids Res. 2013;41(Database issue):D1228-33. https://doi.org/10.1093/nar/gks1147.
[92] Xia J, Benner MJ, Hancock RE. NetworkAnalyst–integrative approaches for protein-protein interaction network analysis and visual exploration. Nucleic Acids Res. 2014;42(Web Server issue):W167-74. https://doi.org/10.1093/nar/gku443. |
|
Viewed |
|
|
|
Full text
|
|
|
|
|
Abstract
|
|
|
|
|
Cited |
|
|
|
|
| |
Shared |
|
|
|
|
| |
Discussed |
|
|
|
|
