Anti-adipogenesis activities of Zingiber cassumunar Roxb. rhizome extracts on L929 cells evaluated by image-based analysis
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Published:
Aug 21, 2018
Keywords:
Adipogenesis Zingiber cassumunar Image-based analysis L929
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Abstract
Some species in family Zingiberaceae have been reported as having anti-adipogenesis activity, but to date Zingiber cassumunar has not been investigated. Therefore, this paper investigates of Z. cassumunar extracts on mouse pre-adipocytes, L929 cell line; the first time this cell has been used as a non-inductive in vitro model. Dry rhizome was extracted by dichloromethane, absolute ethanol, and hot water obtaining the crude extracts: ZCD, ZCE and ZCW respectively. A non-cytotoxic activity was shown on the 24 h exposed cells to all extracts, evaluated by using the MTT (methyl-thiazolyldiphenyl-tetrazolium bromide) assay. An anti-proliferation assay was carried out to each of the extracts for 72 h, to determine the non-toxic inhibition-concentration (IC20). The quantity of lipid droplets in the cells, exposed to the IC20 or IC20/2 of each extract, was assessed by using photomicrographs and image-based assay under the ImageJ computer software. Cellular lipid accumulation was significantly decreased in the exposed cells to each of the extract in a concentration-dependent manner, in comparison to the unexposed cells, by which ZCE was the most effective followed by ZCW and ZCD respectively. Expression of adipogenesisrelated genes of the exposed cells to each extraction was evaluated through real-time PCR. All of the extracts down-regulated the activity of PPARγ (the key regulator of adipogenesis) while ZCE up-regulated Pref-1 (the pre-adipocyte regulatory gene inhibiting lipid accumulation). Four groups of genes were down-regulated by at least one or more of the extracts. These findings verified the anti-adipogenesis potential of Z. cassumunar in mammalian adipocyte.
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Sririwichitchai, R., Saiai, A., Inthanon, K., Chomdej, S., Wongkham, W., & Roongruangwongse, W. (2018). Anti-adipogenesis activities of Zingiber cassumunar Roxb. rhizome extracts on L929 cells evaluated by image-based analysis. Veterinary Integrative Sciences, 16(2), 35–51. Retrieved from https://he02.tci-thaijo.org/index.php/vis/article/view/141487
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References
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Quantitative high-content/high-throughput microscopy analysis of lipid droplets in subject specific adipogenesis models. Cytometry A. 91, 1068-1077.
Broeke, J., Pérez, J.M.M., Pascau, J., 2015. Image processing with ImageJ. Packt Publishing Ltd.
Buyukhatipoglu, H. 2008. A possibly overlooked side effect of Orlistat: gastroesophageal reflux disease. J. Natl. Med. Assoc. 100, 1207.
Chen, T.G., Chen, J.Z., Wang, X.X. 2006. Effects of rapamycin on number activity and eNOS of endothelial progenitor cells from peripheral blood. Cell Prolif. 39, 117-125.
Coe, N.R., Bernlohr, D.A. 1998. Physiological properties and functions of intracellular fatty acid-binding proteins. Biochim. Biophys. Acta. 1391, 287-306.
Copps, K.D., White, M.F. 2012. Regulation of insulin sensitivity by serine/ threonine phosphorylation of insulin receptor substrate proteins IRS1 and IRS2. Diabetologia. 55, 2565-2582.
Díez, J.J., Iglesias, P. 2003. The role of the novel adipocyte-derived hormone
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Ejaz, A., Wu, D., Kwan, P., Meydani, M. 2009. Curcumin inhibits adipogenesis in 3T3-L1 adipocytes and angiogenesis and obesity in C57/BL mice. J. Nutr. 139, 919-925.
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Gstraunthaler, G. 2003. Alternatives to the use of fetal bovine serum: serum-free cell culture. ALTEX. 20, 275-281.
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Hwang, D.I., Won, K.J., Kim, D.Y., Kim, B., Lee, H.M. 2017. Cinnamyl Alcohol, the bioactive component of chestnut flower absolute, inhibits adipocyte differentiation in 3T3-L1 cells by downregulating adipogenic transcription factors. Am. J. Chin. Med. 45, 833-846.
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Kinkel, A.D., Fernyhough, M.E., Helterline, D.L., Vierck, J.L., Oberg, K.S., Vance, T.J., Hausman, G.J., Hill, R.A., Dodson, M.V., 2004. Oil red-O stains non-adipogenic cells: a precautionary note. Cytotechnology. 46, 49-56.
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Koparde, A., Magdum, Cs. 2017. Phytochemical studies and pharmacognostical evaluation of Zingiber cassumunar Roxb. Asian J. Pharm. Clin. Res.10, 129-135.
Kwon, J.H., Hwang, S.Y., Han, J.S. 2017. Bamboo (Phyllostachys bambusoides) leaf extracts inhibit adipogenesis by regulating adipogenic transcription factors and enzymes in 3T3-L1 adipocytes. Food Sci. Biotechnol. 26, 11037–11044.
Lauvai, J., Schumacher, M., Finco, F. D. B. A., Graeve, L. 2017. Bacaba phenolic extract attenuates adipogenesis by down-regulating PPARγ and C/EBPα in 3T3-L1 cells. NFS Journal. 9, 8-14.
Lefterova, M.I., Lazar, M.A. 2009. New developments in adipogenesis. Trends Endocrinol. Metab. 20,107-114.
Li, X., Ycaza, J., Blumberg, B. 2011. The environmental obesogen tributyltin chloride acts via peroxisome proliferator activated receptor gamma to induce adipogenesis in murine 3T3-L1 preadipocytes. J. Steroid Biochem. Mol. Biol. 127, 9-15.
Livak, K.J., Schmittgen, T.D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 25, 402-408.
Lodhi, I.J., Yin, L., Jensen-Urstad, A.P., Funai, K., Coleman, T., Baird, J.H., El Ramahi, M.K., Razani, B., Song, H., Fu-Hsu, F., Turk, J., Semen kovich, C.F. 2012. Inhibiting adipose tissue lipogenesis reprograms thermogenesis and PPARγ activation to decrease diet-induced obesity.
Cell Metab. 16, 189-201.
Mukherjee, M., 2003. Human digestive and metabolic lipases—a brief review. J. Mol. Catal. B: Enzym. 22, 369-376.
Mahmoud, R.H., Elnour, W.A. 2013. Comparative evaluation of the efficacy of ginger and Orlistat on obesity management, pancreatic lipase and liver peroxisomal catalase enzyme in male albino rats. Eur. Rev. Med. Pharmacol. Sci. 17, 75-83.
Morak, M., Schmidinger, H., Riesenhuber, G., Rechberger, G.N., Kollroser, M., Haemmerle, G., Zechner, R., Kronenberg, F., Hermetter, A. 2012. Adipose triglyceride lipase (ATGL) and hormone-sensitive lipase (HSL) deficiencies affect expression of lipolytic activities in mouse
adipose tissues. Mol. Cell Proteomics. 11, 1777-1789.
Najafian, J., Abdar-Esfahani, M., Arab-Momeni, M., Akhavan-Tabib, A., 2014. Safety of herbal medicine in treatment of weight loss. ARYA atheroscler. 10, 55-58.
Ntambi, J.M., Young-Cheul, K., 2000. Adipocyte differentiation and gene expression. J. Nutr. 130, 3122S-3126S.
Romao, J.M., Jin, W., Dodson, M.V., Hausman, G.J., Moore, S.S., Guan, L.L., 2011. MicroRNA regulation in mammalian adipogenesis. Exp. Biol. Med. 236, 997-1004.
Sakuma, M., 1998. Probit analysis of preference data. Appl. Entomol. Zool. 33, 339-347.
Seo, E.Y., 2015. Effects of (6)-gingerol, ginger component on adipocyte development
and differentiation in 3T3-L1. J. Nutr. Health. 48, 327-334.
Serra, D., Mera, P., Malandrino, M.I., Mir, J.F., Herrero, L., 2013. Mitochondrial fatty acid oxidation in obesity. Antioxid. Redox Signal. 19, 269-284.
Serrano, M.C., Pagani, R., Vallet-Regı, M., Pena, J., Ramila, A., Izquierdo, I., Portolés, M.T., 2004. In vitro biocompatibility assessment of poly (ε-caprolactone) films using L929 mouse fibroblasts. Biomaterials. 25, 5603-5611.
Shan, T., Liu, W., Kuang, S., 2013. Fatty acid binding protein 4 expression marks a population of adipocyte progenitors in white and brown adipose tissues. FASEB. J. 27, 277-287.
Sharma, G.J., Chirangini, P., Kishor, R., 2011. Gingers of Manipur: diversity and potentials as bioresources. Genet. Resour. Crop Evol. 58, 753- 767.
Sharma, G.J., Chirangini, P., Mishra, K.P., 2007. Evaluation of antioxidant and cytotoxic properties of tropical ginger, Zingiber montanum (J.Konig) A Dietr. Gard. Bull Sing. 59, 189-202.
Shin, J.H., Gadde, K.M., 2013. Clinical utility of phentermine/topiramate (Qsymia™) combination for the treatment of obesity. DiabetesMetab. Syndr. Obes. 6, 131-139.
Singh, C., Manglembi, N., Swapana, N., Chanu, S., 2015. Ethnobotany, phytochemistry and pharmacology of Zingiber cassumunar Roxb. (Zingiberaceae). J. Pharmacogn. Phytochem. 4.
Stoecker, K., Sass, S., Theis, F.J., Hauner, H., Pfaffl, M.W., 2017. Inhibition of fat cell differentiation in 3T3-L1 pre-adipocytes by all-trans retinoic acid: Integrative analysis of transcriptomic and phenotypic data. Biomol. Detect. Quantif. 11, 31-44.
Suk, S., Seo, S.G., Yu, J.G., Yang, H., Jeong, E., Jang, Y.J., Yaghmoor, S.S., Ahmed, Y., Yousef, J.M., Abualnaja, K.O., Al‐Malki, A.L., 2016. A bioactive constituent of ginger, 6‐shogaol, prevents adipogenesis and stimulates lipolysis in 3T3‐L1 adipocytes. J. Food Biochem. 40, 84-90.
Todoric, J., Strobl, B., Jais, A., Boucheron, N., Bayer, M., Amann, S., Lindroos, J., Teperino, R., Prager, G., Bilban, M., Ellmeier, W., 2011. Cross-talk between interferon-γ and hedgehog signaling regulates adipogenesis. Diabetes. 60, 1668-1676.
Tzeng, T.F., Chang, C.J., Liu, I.M., 2014. 6‐Gingerol inhibits rosiglitazone‐ induced adipogenesis in 3T3‐L1 adipocytes. Phytother Res. 28(2), 187-192.
Tzeng, T.F., Liu, I.M., 2013. 6-Gingerol prevents adipogenesis and the accumulation of cytoplasmic lipid droplets in 3T3-L1 cells. Phytomedicine. 20, 481-487.
Wang, G.L., Shi, X., Salisbury, E., Sun, Y., Albrecht, J.H., Smith, R.G., Tim chenko, N.A., 2006. Cyclin D3 maintains growth-inhibitory activity of C/EBPα by stabilizing C/EBPα-cdk2 and C/EBPα-Brm complex es. Mol. Cell. Biol. 26, 2570-2582.
Zimmermann, R., Strauss, J.G., Haemmerle, G., Schoiswohl, G., Birner-Gruenberger, R.,
Riederer, M., Lass, A., Neuberger, G., Eisenhaber, F., Hermetter, A., Zechner, R., 2004. Fat mobilization in adipose tissue is promoted by adipose triglyceride lipase. Science. 306, 1383-1386.
Anasamy, T., Abdul, A.B., Sukari, M.A., Abdelwahab, S.I., Mohan, S., Ka malidehghan, B., Azid, M.Z., Muhammad Nadzri, N., Andas, A.R., Kuan Beng, N., Hadi, A.H., Sulaiman Rahman, H. 2013. A phenylbu enoid dimer, cis-3-(3′, 4′-dimethoxyphenyl)-4-[(E)-3′′′, 4′′′-dimethox ystyryl] cyclohex-1-ene, exhibits apoptogenic properties in T-acute lymphoblastic leukemia cells via induction of p53-independent mitochondrial signalling pathway. J. Evid. Based Complementary Altern. Med. 2013.
Bombrun, M., Gao, H., Ranefall, P., Mejhert, N., Arner, P., Wählby, C. 2017.
Quantitative high-content/high-throughput microscopy analysis of lipid droplets in subject specific adipogenesis models. Cytometry A. 91, 1068-1077.
Broeke, J., Pérez, J.M.M., Pascau, J., 2015. Image processing with ImageJ. Packt Publishing Ltd.
Buyukhatipoglu, H. 2008. A possibly overlooked side effect of Orlistat: gastroesophageal reflux disease. J. Natl. Med. Assoc. 100, 1207.
Chen, T.G., Chen, J.Z., Wang, X.X. 2006. Effects of rapamycin on number activity and eNOS of endothelial progenitor cells from peripheral blood. Cell Prolif. 39, 117-125.
Coe, N.R., Bernlohr, D.A. 1998. Physiological properties and functions of intracellular fatty acid-binding proteins. Biochim. Biophys. Acta. 1391, 287-306.
Copps, K.D., White, M.F. 2012. Regulation of insulin sensitivity by serine/ threonine phosphorylation of insulin receptor substrate proteins IRS1 and IRS2. Diabetologia. 55, 2565-2582.
Díez, J.J., Iglesias, P. 2003. The role of the novel adipocyte-derived hormone
adiponectin in human disease. Eur. J. Endocrinol.148, 293-300.
Eljezi, T., Pinta, P., Richard, D., Pinguet, J., Chezal, J.M., Chagnon, M.C., Sautou, V., Grimandi, G., Moreau, E. 2017. In vitro cytotoxic effects of DEHP-alternative plasticizers and their primary metabolites on a L929 cell line. Chemosphere. 173, 452-459.
Ejaz, A., Wu, D., Kwan, P., Meydani, M. 2009. Curcumin inhibits adipogenesis in 3T3-L1 adipocytes and angiogenesis and obesity in C57/BL mice. J. Nutr. 139, 919-925.
Farnsworth, R.N., Bunyapraphatsara, N., 1992. Garcinia mangostana Linn. Thai Medicinal Plants. Prachachon Co., Ltd.: Bangkok, pp.160-162.
Gstraunthaler, G. 2003. Alternatives to the use of fetal bovine serum: serum-free cell culture. ALTEX. 20, 275-281.
Harada, A., Okazaki, E., Okada, S., Tachibana, T., Ohkawa ,Y. 2014. Production of a monoclonal antibody for C/EBPβ:the subnuclear localization of C/EBPβ in mouse L929 cells. Monoclon. Antib. Immunodiagn. Immunother. 33, 34-37.
Hasani-Ranjbar, S., Jouyandeh, Z., Abdollahi, M. 2013. A systematic review of anti-obesity medicinal plants – an update. J. Diabetes Metab. Disord. 12, 28.
Hwang, D.I., Won, K.J., Kim, D.Y., Kim, B., Lee, H.M. 2017. Cinnamyl Alcohol, the bioactive component of chestnut flower absolute, inhibits adipocyte differentiation in 3T3-L1 cells by downregulating adipogenic transcription factors. Am. J. Chin. Med. 45, 833-846.
Iswantini, D., Silitonga, R.F., Martatilofa, E., Darusman, L.K., 2011. Zingiber cassumunar, Guazuma ulmifolia, and Murraya paniculata extracts as antiobesity: in vitro inhibitory effect on pancreatic lipase activity. HAYATI J. Biosci. 18, 6-10.
Jeney, F., Bazsó-Dombi. E., Oravecz, K., Szabó, J., Nagy, I.Z. 2000. Cytochemical studies on the fibroblast-preadipocyte relationships in cultured fibroblastcell lines. Acta. Histochem. 102, 381-389.
Kalantari, K., Moniri, M., Boroumand Moghaddam, A., Abdul Rahim, R., Bin Ariff, A., Izadiyan, Z., Mohamad, R. 2017. A review of the biomedical applications of zerumbone and the techniques for its extraction from ginger rhizomes. Molecules. 22, pii: E1645.
Kim, J.B., Sarraf, P., Wright, M., Yao, K.M., Mueller, E., Solanes, G., Lowell, B.B., Spiegelman, B.M. 1998. Nutritional and insulin regulation of fatty acid synthetase and leptin gene expression through ADD1/SRE BP1. J Clin Invest. 101, 1-9.
Kim, K.A., Kim, J.H., Wang, Y., Sul, H.S. 2007. Pref-1 (preadipocyte factor 1) activates the MEK/extracellular signal-regulated kinase pathway to inhibit adipocyte differentiation. Mol. Cell Biol. 27, 2294-308.
Kinkel, A.D., Fernyhough, M.E., Helterline, D.L., Vierck, J.L., Oberg, K.S., Vance, T.J., Hausman, G.J., Hill, R.A., Dodson, M.V., 2004. Oil red-O stains non-adipogenic cells: a precautionary note. Cytotechnology. 46, 49-56.
Kirchner, S., Kieu, T., Chow, C., Casey, S., Blumberg, B. 2010. Prenatal exposure to the environmental obesogen tributyltin predisposes multipotentstem cells to become adipocytes. Mol. Endocrinol. 24, 526-539.
Koparde, A., Magdum, Cs. 2017. Phytochemical studies and pharmacognostical evaluation of Zingiber cassumunar Roxb. Asian J. Pharm. Clin. Res.10, 129-135.
Kwon, J.H., Hwang, S.Y., Han, J.S. 2017. Bamboo (Phyllostachys bambusoides) leaf extracts inhibit adipogenesis by regulating adipogenic transcription factors and enzymes in 3T3-L1 adipocytes. Food Sci. Biotechnol. 26, 11037–11044.
Lauvai, J., Schumacher, M., Finco, F. D. B. A., Graeve, L. 2017. Bacaba phenolic extract attenuates adipogenesis by down-regulating PPARγ and C/EBPα in 3T3-L1 cells. NFS Journal. 9, 8-14.
Lefterova, M.I., Lazar, M.A. 2009. New developments in adipogenesis. Trends Endocrinol. Metab. 20,107-114.
Li, X., Ycaza, J., Blumberg, B. 2011. The environmental obesogen tributyltin chloride acts via peroxisome proliferator activated receptor gamma to induce adipogenesis in murine 3T3-L1 preadipocytes. J. Steroid Biochem. Mol. Biol. 127, 9-15.
Livak, K.J., Schmittgen, T.D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 25, 402-408.
Lodhi, I.J., Yin, L., Jensen-Urstad, A.P., Funai, K., Coleman, T., Baird, J.H., El Ramahi, M.K., Razani, B., Song, H., Fu-Hsu, F., Turk, J., Semen kovich, C.F. 2012. Inhibiting adipose tissue lipogenesis reprograms thermogenesis and PPARγ activation to decrease diet-induced obesity.
Cell Metab. 16, 189-201.
Mukherjee, M., 2003. Human digestive and metabolic lipases—a brief review. J. Mol. Catal. B: Enzym. 22, 369-376.
Mahmoud, R.H., Elnour, W.A. 2013. Comparative evaluation of the efficacy of ginger and Orlistat on obesity management, pancreatic lipase and liver peroxisomal catalase enzyme in male albino rats. Eur. Rev. Med. Pharmacol. Sci. 17, 75-83.
Morak, M., Schmidinger, H., Riesenhuber, G., Rechberger, G.N., Kollroser, M., Haemmerle, G., Zechner, R., Kronenberg, F., Hermetter, A. 2012. Adipose triglyceride lipase (ATGL) and hormone-sensitive lipase (HSL) deficiencies affect expression of lipolytic activities in mouse
adipose tissues. Mol. Cell Proteomics. 11, 1777-1789.
Najafian, J., Abdar-Esfahani, M., Arab-Momeni, M., Akhavan-Tabib, A., 2014. Safety of herbal medicine in treatment of weight loss. ARYA atheroscler. 10, 55-58.
Ntambi, J.M., Young-Cheul, K., 2000. Adipocyte differentiation and gene expression. J. Nutr. 130, 3122S-3126S.
Romao, J.M., Jin, W., Dodson, M.V., Hausman, G.J., Moore, S.S., Guan, L.L., 2011. MicroRNA regulation in mammalian adipogenesis. Exp. Biol. Med. 236, 997-1004.
Sakuma, M., 1998. Probit analysis of preference data. Appl. Entomol. Zool. 33, 339-347.
Seo, E.Y., 2015. Effects of (6)-gingerol, ginger component on adipocyte development
and differentiation in 3T3-L1. J. Nutr. Health. 48, 327-334.
Serra, D., Mera, P., Malandrino, M.I., Mir, J.F., Herrero, L., 2013. Mitochondrial fatty acid oxidation in obesity. Antioxid. Redox Signal. 19, 269-284.
Serrano, M.C., Pagani, R., Vallet-Regı, M., Pena, J., Ramila, A., Izquierdo, I., Portolés, M.T., 2004. In vitro biocompatibility assessment of poly (ε-caprolactone) films using L929 mouse fibroblasts. Biomaterials. 25, 5603-5611.
Shan, T., Liu, W., Kuang, S., 2013. Fatty acid binding protein 4 expression marks a population of adipocyte progenitors in white and brown adipose tissues. FASEB. J. 27, 277-287.
Sharma, G.J., Chirangini, P., Kishor, R., 2011. Gingers of Manipur: diversity and potentials as bioresources. Genet. Resour. Crop Evol. 58, 753- 767.
Sharma, G.J., Chirangini, P., Mishra, K.P., 2007. Evaluation of antioxidant and cytotoxic properties of tropical ginger, Zingiber montanum (J.Konig) A Dietr. Gard. Bull Sing. 59, 189-202.
Shin, J.H., Gadde, K.M., 2013. Clinical utility of phentermine/topiramate (Qsymia™) combination for the treatment of obesity. DiabetesMetab. Syndr. Obes. 6, 131-139.
Singh, C., Manglembi, N., Swapana, N., Chanu, S., 2015. Ethnobotany, phytochemistry and pharmacology of Zingiber cassumunar Roxb. (Zingiberaceae). J. Pharmacogn. Phytochem. 4.
Stoecker, K., Sass, S., Theis, F.J., Hauner, H., Pfaffl, M.W., 2017. Inhibition of fat cell differentiation in 3T3-L1 pre-adipocytes by all-trans retinoic acid: Integrative analysis of transcriptomic and phenotypic data. Biomol. Detect. Quantif. 11, 31-44.
Suk, S., Seo, S.G., Yu, J.G., Yang, H., Jeong, E., Jang, Y.J., Yaghmoor, S.S., Ahmed, Y., Yousef, J.M., Abualnaja, K.O., Al‐Malki, A.L., 2016. A bioactive constituent of ginger, 6‐shogaol, prevents adipogenesis and stimulates lipolysis in 3T3‐L1 adipocytes. J. Food Biochem. 40, 84-90.
Todoric, J., Strobl, B., Jais, A., Boucheron, N., Bayer, M., Amann, S., Lindroos, J., Teperino, R., Prager, G., Bilban, M., Ellmeier, W., 2011. Cross-talk between interferon-γ and hedgehog signaling regulates adipogenesis. Diabetes. 60, 1668-1676.
Tzeng, T.F., Chang, C.J., Liu, I.M., 2014. 6‐Gingerol inhibits rosiglitazone‐ induced adipogenesis in 3T3‐L1 adipocytes. Phytother Res. 28(2), 187-192.
Tzeng, T.F., Liu, I.M., 2013. 6-Gingerol prevents adipogenesis and the accumulation of cytoplasmic lipid droplets in 3T3-L1 cells. Phytomedicine. 20, 481-487.
Wang, G.L., Shi, X., Salisbury, E., Sun, Y., Albrecht, J.H., Smith, R.G., Tim chenko, N.A., 2006. Cyclin D3 maintains growth-inhibitory activity of C/EBPα by stabilizing C/EBPα-cdk2 and C/EBPα-Brm complex es. Mol. Cell. Biol. 26, 2570-2582.
Zimmermann, R., Strauss, J.G., Haemmerle, G., Schoiswohl, G., Birner-Gruenberger, R.,
Riederer, M., Lass, A., Neuberger, G., Eisenhaber, F., Hermetter, A., Zechner, R., 2004. Fat mobilization in adipose tissue is promoted by adipose triglyceride lipase. Science. 306, 1383-1386.