Abstract
Interest in reactive oxygen species and adipocyte differentiation/adipose tissue function is steadily increasing. This is due in part to a search for alternative avenues for combating obesity, which results from the excess accumulation of adipose tissue. Obesity is a major risk factor for complex disorders such as cancer, type 2 diabetes, and cardiovascular diseases. The ability of mesenchymal stromal/stem cells (MSCs) to differentiate into adipocytes is often used as a model for studying adipogenesis in vitro. A key focus is the effect of both intra- and extracellular reactive oxygen species (ROS) on adipogenesis. The consensus from the majority of studies is that ROS, irrespective of the source, promote adipogenesis.
The effect of ROS on adipogenesis is suppressed by antioxidants or ROS scavengers. Reactive oxygen species are generated during the process of adipocyte differentiation as well as by other cell metabolic processes. Despite many studies in this field, it is still not possible to state with certainty whether ROS measured during adipocyte differentiation are a cause or consequence of this process. In addition, it is still unclear what the exact sources are of the ROS that initiate and/or drive adipogenic differentiation in MSCs in vivo. This review provides an overview of our understanding of the role of ROS in adipocyte differentiation as well as how certain ROS scavengers and antioxidants might affect this process.
This is a preview of subscription content, log in via an institution.
Abbreviations
- ASCs:
-
Adipose-derived stem/stromal cells
- ATP:
-
Adenosine triphosphate
- BAT:
-
Brown adipose tissue
- BMAL1:
-
Brain and muscle ARNT-like protein 1
- BM-MSCs:
-
Bone marrow-derived MSCs
- BMP:
-
Bone morphogenic protein
- C/EBP:
-
CCAAT enhancer-binding protein
- C/EBPα:
-
CCAAT enhancer-binding protein alpha
- C/EBPβ:
-
CCAAT enhancer-binding protein beta
- C/EBPδ:
-
CCAAT enhancer-binding protein delta
- CAT:
-
Catalase
- CCL2:
-
C-C motif chemokine 2 precursor
- CoQ:
-
Oxidized ubiquinone
- CoQH2:
-
Reduced ubiquinol
- CREB:
-
Cyclic AMP response element-binding protein
- Cyt:
-
Cytochrome
- DPI:
-
Diphenyleneiodonium
- e−:
-
electron
- eNOS:
-
Endothelial nitric oxide
- EPAS1:
-
Endothelial PAS domain protein 1
- ETC:
-
Electron transport chain
- FABP4:
-
Fatty acid-binding protein 4
- FAT:
-
Fatty acid translocase (CD36)
- FOXA2:
-
Forkhead box A2
- FOXO1:
-
Forkhead box O1
- Ga:
-
One billion years
- GATA2:
-
GATA binding protein 2
- GATA3:
-
GATA binding protein 3
- GPx:
-
Glutathione peroxidase
- GSTA4:
-
Glutathione S-transferase A4
- H+:
-
Proton
- H2O:
-
Water
- H2O2:
-
Hydrogen peroxide
- IDII:
-
Standard adipogenic induction cocktail
- IL10:
-
Interleukin 10
- IL6:
-
Interleukin 6
- IL8:
-
Interleukin 8
- iNOS:
-
Inducible nitric oxide synthase
- KLF:
-
Kruppel-like factor
- LPL:
-
Lipoprotein lipase
- M1:
-
Classically activated macrophage phenotype
- MEFs:
-
Immortalized murine embryonic fibroblasts
- mESCs:
-
Murine embryonic stem cells
- MKP-1:
-
MAP kinase phosphatase-1
- mMSCs:
-
Murine mesenchymal stem/stromal cells
- MSCs:
-
Mesenchymal stem/stromal cells
- NAC:
-
N-acetyl-L-cysteine
- NEFA:
-
Nonesterified fatty acid
- NO:
-
Nitric oxide
- NOS:
-
Nitric oxide synthase
- NOX:
-
NADPH oxidase
- O2:
-
Oxygen
- O2−:
-
Superoxide
- PPARγ:
-
Proliferator-activated receptor-gamma
- Pref-1:
-
Preadipocyte factor-1
- Prx3:
-
Peroxiredoxin 3
- ROS:
-
Reactive oxygen species
- SIRT1:
-
Histone deacetylase sirtuin 1
- SOD:
-
Superoxide dismutase
- SOD2:
-
Superoxide dismutase 2
- SREBP1c:
-
Sterol regulatory element-binding transcription factor 1
- STAT5a:
-
Signal transducer and activator of transcription-5a
- TAZ:
-
Transcriptional coactivator with PDZ-binding motif
- TG:
-
Triacylglycerol
- TNFα:
-
Tumor necrosis factor alpha
- WAT:
-
White adipose tissue
- ZFP423:
-
Zinc finger protein 423
References
Alfadda, A. A., & Sallam, R. M. (2012a). Reactive oxygen species in health and disease. Journal of Biomedicine and Biotechnology, 2012, 14. https://doi.org/10.1155/2012/936486.
Alfadda, A. A., & Sallam, R. M. (2012b). Reactive oxygen species in health and disease. Journal of Biomedicine & Biotechnology, 2012, 936486. https://doi.org/10.1155/2012/936486.
Ali, A. T., Hochfeld, W. E., Myburgh, R., & Pepper, M. S. (2013). Adipocyte and adipogenesis. European Journal of Cell Biology, 92(6–7), 229–236. https://doi.org/10.1016/j.ejcb.2013.06.001.
Ambele, M. A., & Pepper, M. S. (2017). Identification of transcription factors potentially involved in human adipogenesis in vitro. Molecular Genetics & Genomic Medicine:n/a-n/a., 5, 210. https://doi.org/10.1002/mgg3.269.
Ambele, M. A., Dessels, C., Durandt, C., & Pepper, M. S. (2016). Genome-wide analysis of gene expression during adipogenesis in human adipose-derived stromal cells reveals novel patterns of gene expression during adipocyte differentiation. Stem Cell Research, 16(3), 725–734. https://doi.org/10.1016/j.scr.2016.04.011.
Atashi, F., Modarressi, A., & Pepper, M. S. (2015). The role of reactive oxygen species in mesenchymal stem cell Adipogenic and osteogenic differentiation: A review. Stem Cells and Development, 24(10), 1150–1163. https://doi.org/10.1089/scd.2014.0484.
Babior, B. M., Kipnes, R. S., & Curnutte, J. T. (1973). Biological defense mechanisms. The production by leukocytes of superoxide, a potential bactericidal agent. The Journal of Clinical Investigation, 52(3), 741–744. https://doi.org/10.1172/jci107236.
Bassi, G., Pacelli, L., Carusone, R., Zanoncello, J., & Krampera, M. (2012). Adipose-derived stromal cells (ASCs). Transfusion and Apheresis Science : Official Journal of the World Apheresis Association : Official Journal of the European Society for Haemapheresis, 47(2), 193–198. https://doi.org/10.1016/j.transci.2012.06.004.
Bedard, K., & Krause, K. H. (2007). The NOX family of ROS-generating NADPH oxidases: Physiology and pathophysiology. Physiological Reviews, 87(1), 245–313. https://doi.org/10.1152/physrev.00044.2005.
Bekker, A., Holland, H. D., Wang, P. L., Rumble, D., 3rd, Stein, H. J., Hannah, J. L., Coetzee, L. L., & Beukes, N. J. (2004). Dating the rise of atmospheric oxygen. Nature, 427(6970), 117–120. https://doi.org/10.1038/nature02260.
Bremer, A. A., & Jialal, I. (2013). Adipose tissue dysfunction in nascent metabolic syndrome. Journal of Obesity, 2013, 393192. https://doi.org/10.1155/2013/393192.
Carriere, A., Fernandez, Y., Rigoulet, M., Penicaud, L., & Casteilla, L. (2003). Inhibition of preadipocyte proliferation by mitochondrial reactive oxygen species. FEBS Letters, 550(1–3), 163–167.
Castro, J. P., Grune, T., & Speckmann, B. (2016). The two faces of reactive oxygen species (ROS) in adipocyte function and dysfunction. Biological Chemistry, 397(8), 709–724. https://doi.org/10.1515/hsz-2015-0305.
Chen, Y., & Junger, W. G. (2012). Measurement of oxidative burst in neutrophils. Methods in Molecular Biology (Clifton, NJ), 844, 115–124. https://doi.org/10.1007/978-1-61779-527-5_8.
Chen, J.-X., & Stinnett, A. (2008). Ang-1 gene therapy inhibits hypoxia-inducible factor-1α (HIF-1α)-Prolyl-4-Hydroxylase-2, stabilizes HIF-1α expression, and normalizes immature vasculature in db/db mice. Diabetes, 57(12), 3335–3343. https://doi.org/10.2337/db08-0503.
Commoner, B., Townsend, J., & Pake, G. E. (1954). Free radicals in biological materials. Nature, 174(4432), 689–691.
Cotillard, A., Poitou, C., Torcivia, A., Bouillot, J. L., Dietrich, A., Kloting, N., Gregoire, C., Lolmede, K., Bluher, M., & Clement, K. (2014). Adipocyte size threshold matters: Link with risk of type 2 diabetes and improved insulin resistance after gastric bypass. The Journal of Clinical Endocrinology and Metabolism, 99(8), E1466–E1470. https://doi.org/10.1210/jc.2014-1074.
Curtis, J. M., Grimsrud, P. A., Wright, W. S., Xu, X., Foncea, R. E., Graham, D. W., Brestoff, J. R., Wiczer, B. M., Ilkayeva, O., Cianflone, K., Muoio, D. E., Arriaga, E. A., & Bernlohr, D. A. (2010). Downregulation of adipose glutathione S-transferase A4 leads to increased protein carbonylation, oxidative stress, and mitochondrial dysfunction. Diabetes, 59(5), 1132–1142. https://doi.org/10.2337/db09-1105.
D’Autreaux, B., & Toledano, M. B. (2007). ROS as signalling molecules: Mechanisms that generate specificity in ROS homeostasis. Nature Reviews Molecular Cell Biology, 8(10), 813–824. https://doi.org/10.1038/nrm2256.
Den Hartigh, L. J., Omer, M., Goodspeed, L., Wang, S., Wietecha, T., O’Brien, K. D., & Han, C. Y. (2016). Adipocyte-specific deficiency of NADPH oxidase 4 delays the onset of insulin resistance and attenuates adipose tissue inflammation in obesity. Arteriosclerosis, Thrombosis, and Vascular Biology, 37(3), 466–475.
Drehmer, D. L., de Aguiar, A. M., Brandt, A. P., Petiz, L., Cadena, S. M., Rebelatto, C. K., Brofman, P. R., Filipak Neto, F., Dallagiovanna, B., & Abud, A. P. (2016). Metabolic switches during the first steps of adipogenic stem cells differentiation. Stem Cell Research, 17(2), 413–421. https://doi.org/10.1016/j.scr.2016.09.001.
Droge, W. (2002). Free radicals in the physiological control of cell function. Physiological Reviews, 82(1), 47–95. https://doi.org/10.1152/physrev.00018.2001.
Drong, A. W., Lindgren, C. M., & McCarthy, M. I. (2012). The genetic and epigenetic basis of type 2 diabetes and obesity. Clinical Pharmacology and Therapeutics, 92(6), 707–715. https://doi.org/10.1038/clpt.2012.149.
Drose, S., & Brandt, U. (2008). The mechanism of mitochondrial superoxide production by the cytochrome bc1 complex. The Journal of Biological Chemistry, 283(31), 21649–21654. https://doi.org/10.1074/jbc.M803236200.
Durandt, C., van Vollenstee, F. A., Dessels, C., Kallmeyer, K., de Villiers, D., Murdoch, C., Potgieter, M., & Pepper, M. S. (2016). Novel flow cytometric approach for the detection of adipocyte sub-populations during adipogenesis. Journal of Lipid Research, 57(4), 729–742. https://doi.org/10.1194/jlr.D065664.
Eseberri, I., Miranda, J., Lasa, A., Churruca, I., & Portillo, M. P. (2015). Doses of quercetin in the range of serum concentrations exert delipidating effects in 3T3-L1 preadipocytes by acting on different stages of adipogenesis, but not in mature adipocytes. Oxidative Medicine and Cellular Longevity, 2015, 480943. https://doi.org/10.1155/2015/480943.
Finkel, T. (2011). Signal transduction by reactive oxygen species. The Journal of Cell Biology, 194(1), 7–15. https://doi.org/10.1083/jcb.201102095.
Furukawa, S., Fujita, T., Shimabukuro, M., Iwaki, M., Yamada, Y., Nakajima, Y., Nakayama, O., Makishima, M., Matsuda, M., & Shimomura, I. (2004). Increased oxidative stress in obesity and its impact on metabolic syndrome. The Journal of Clinical Investigation, 114(12), 1752–1761. https://doi.org/10.1172/jci21625.
Furuyashiki, T., Nagayasu, H., Aoki, Y., Bessho, H., Hashimoto, T., Kanazawa, K., & Ashida, H. (2004). Tea catechin suppresses adipocyte differentiation accompanied by down-regulation of PPARgamma2 and C/EBPalpha in 3T3-L1 cells. Bioscience, Biotechnology, and Biochemistry, 68(11), 2353–2359. https://doi.org/10.1271/bbb.68.2353.
Galinier, A., Carriere, A., Fernandez, Y., Carpene, C., Andre, M., Caspar-Bauguil, S., Thouvenot, J. P., Periquet, B., Penicaud, L., & Casteilla, L. (2006). Adipose tissue proadipogenic redox changes in obesity. The Journal of Biological Chemistry, 281(18), 12682–12687. https://doi.org/10.1074/jbc.M506949200.
Gregoire, F. M., Smas, C. M., & Sul, H. S. (1998). Understanding adipocyte differentiation. Physiological Reviews, 78(3), 783–809.
Guilherme, A., Virbasius, J. V., Puri, V., & Czech, M. P. (2008). Adipocyte dysfunctions linking obesity to insulin resistance and type 2 diabetes. Nature Reviews Molecular Cell Biology, 9(5), 367–377. https://doi.org/10.1038/nrm2391.
Han, C. Y. (2016). Roles of reactive oxygen species on insulin resistance in adipose tissue. Diabetes & Metabolism Journal, 40(4), 272–279. https://doi.org/10.4093/dmj.2016.40.4.272.
Harman, D. (1956). Aging: A theory based on free radical and radiation chemistry. Journal of Gerontology, 11(3), 298–300.
Higuchi, M., Dusting, G. J., Peshavariya, H., Jiang, F., Hsiao, S. T., Chan, E. C., & Liu, G. S. (2013). Differentiation of human adipose-derived stem cells into fat involves reactive oxygen species and Forkhead box O1 mediated upregulation of antioxidant enzymes. Stem Cells and Development, 22(6), 878–888. https://doi.org/10.1089/scd.2012.0306.
Hinkle, P. C., Butow, R. A., Racker, E., & Chance, B. (1967). Partial resolution of the enzymes catalyzing oxidative phosphorylation. XV. Reverse electron transfer in the flavin-cytochrome beta region of the respiratory chain of beef heart submitochondrial particles. The Journal of Biological Chemistry, 242(22), 5169–5173.
Holzerova, E., & Prokisch, H. (2015). Mitochondria: Much ado about nothing? How dangerous is reactive oxygen species production? The International Journal of Biochemistry & Cell Biology, 63, 16–20. https://doi.org/10.1016/j.biocel.2015.01.021.
Hou, Y., Xue, P., Bai, Y., Liu, D., Woods, C. G., Yarborough, K., Fu, J., Zhang, Q., Sun, G., Collins, S., Chan, J. Y., Yamamoto, M., Andersen, M. E., & Pi, J. (2012). Nuclear factor erythroid-derived factor 2-related factor 2 regulates transcription of CCAAT/enhancer-binding protein beta during adipogenesis. Free Radical Biology & Medicine, 52(2), 462–472. https://doi.org/10.1016/j.freeradbiomed.2011.10.453.
Imhoff, B. R., & Hansen, J. M. (2011). Differential redox potential profiles during adipogenesis and osteogenesis. Cellular & Molecular Biology Letters, 16(1), 149–161. https://doi.org/10.2478/s11658-010-0042-0.
Iyer, G. Y. N., Islam, M. F., & Quastel, J. H. (1961). Biochemical aspects of phagocytosis. Nature, 192(4802), 535–541.
Jiang, F., Zhang, Y., & Dusting, G. J. (2011). NADPH oxidase-mediated redox signaling: Roles in cellular stress response, stress tolerance, and tissue repair. Pharmacological Reviews, 63(1), 218–242. https://doi.org/10.1124/pr.110.002980.
Jiang, Y., Jo, A. Y., & Graff, J. M. (2012). SnapShot: Adipocyte life cycle. Cell, 150(1), 234–234.e232. https://doi.org/10.1016/j.cell.2012.06.022.
Kanda, Y., Hinata, T., Kang, S. W., & Watanabe, Y. (2011). Reactive oxygen species mediate adipocyte differentiation in mesenchymal stem cells. Life Sciences, 89(7–8), 250–258. https://doi.org/10.1016/j.lfs.2011.06.007.
Kawagishi, H., & Finkel, T. (2014). Unraveling the truth about antioxidants: ROS and disease: Finding the right balance. Nature Medicine, 20(7), 711–713. https://doi.org/10.1038/nm.3625.
Krieger-Brauer, H. I., Medda, P. K., & Kather, H. (1997). Insulin-induced activation of NADPH-dependent H2O2 generation in human adipocyte plasma membranes is mediated by Galphai2. The Journal of Biological Chemistry, 272(15), 10135–10143.
Lalucque, H., & Silar, P. (2003). NADPH oxidase: An enzyme for multicellularity? Trends in Microbiology, 11(1), 9–12.
Le Lay, S., Simard, G., Martinez, M. C., & Andriantsitohaina, R. (2014). Oxidative stress and metabolic pathologies: From an adipocentric point of view. Oxidative Medicine and Cellular Longevity, 2014, 18. https://doi.org/10.1155/2014/908539.
Lee, H., Lee, Y. J., Choi, H., Ko, E. H., & J-w, K. (2009). Reactive oxygen species facilitate adipocyte differentiation by accelerating mitotic clonal expansion. The Journal of Biological Chemistry, 284(16), 10601–10609. https://doi.org/10.1074/jbc.M808742200.
Lefterova, M. I., & Lazar, M. A. (2009). New developments in adipogenesis. Trends in Endocrinology and Metabolism: TEM, 20(3), 107–114. https://doi.org/10.1016/j.tem.2008.11.005.
Li, N., Ragheb, K., Lawler, G., Sturgis, J., Rajwa, B., Melendez, J. A., & Robinson, J. P. (2003). Mitochondrial complex I inhibitor rotenone induces apoptosis through enhancing mitochondrial reactive oxygen species production. The Journal of Biological Chemistry, 278(10), 8516–8525. https://doi.org/10.1074/jbc.M210432200.
Li, Y., Mouche, S., Sajic, T., Veyrat-Durebex, C., Supale, R., Pierroz, D., Ferrari, S., Negro, F., Hasler, U., Feraille, E., Moll, S., Meda, P., Deffert, C., Montet, X., Krause, K. H., & Szanto, I. (2012). Deficiency in the NADPH oxidase 4 predisposes towards diet-induced obesity. International Journal of Obesity, 36(12), 1503–1513. https://doi.org/10.1038/ijo.2011.279.
Lindahl, P. E., & Oberg, K. E. (1960). Mechanism of the physiological action of rotenone. Nature, 187, 784.
Liu, G.-S., Chan, E. C., Higuchi, M., Dusting, G. J., & Jiang, F. (2012a). Redox mechanisms in regulation of adipocyte differentiation: Beyond a general stress response. Cell, 1(4), 976–993. https://doi.org/10.3390/cells1040976.
Liu, H., Yang, X., Zhang, Y., Dighe, A., Li, X., & Cui, Q. (2012b). Fullerol antagonizes dexamethasone-induced oxidative stress and adipogenesis while enhancing osteogenesis in a cloned bone marrow mesenchymal stem cell. Journal of Orthopaedic Research: Official Publication of the Orthopaedic Research Society, 30(7), 1051–1057. https://doi.org/10.1002/jor.22054.
Loschen, G., Azzi, A., Richter, C., & Flohe, L. (1974). Superoxide radicals as precursors of mitochondrial hydrogen peroxide. FEBS Letters, 42(1), 68–72.
MacFie, T. S., Poulsom, R., Parker, A., Warnes, G., Boitsova, T., Nijhuis, A., Suraweera, N., Poehlmann, A., Szary, J., Feakins, R., Jeffery, R., Harper, R. W., Jubb, A. M., Lindsay, J. O., & Silver, A. (2014). DUOX2 and DUOXA2 form the predominant enzyme system capable of producing the reactive oxygen species H2O2 in active ulcerative colitis and are modulated by 5-aminosalicylic acid. Inflammatory Bowel Diseases, 20(3), 514–524. https://doi.org/10.1097/01.MIB.0000442012.45038.0e.
Mahadev, K., Motoshima, H., Wu, X., Ruddy, J. M., Arnold, R. S., Cheng, G., Lambeth, J. D., & Goldstein, B. J. (2004). The NAD(P)H oxidase homolog Nox4 modulates insulin-stimulated generation of H2O2 and plays an integral role in insulin signal transduction. Molecular and Cellular Biology, 24(5), 1844–1854.
McCord, J. M., & Fridovich, I. (1969). Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein). The Journal of Biological Chemistry, 244(22), 6049–6055.
Meier, B., Cross, A. R., Hancock, J. T., Kaup, F. J., & Jones, O. T. (1991). Identification of a superoxide-generating NADPH oxidase system in human fibroblasts. The Biochemical Journal, 275(Pt 1), 241–245.
Mitchell, J. B., Xavier, S., DeLuca, A. M., Sowers, A. L., Cook, J. A., Krishna, M. C., Hahn, S. M., & Russo, A. (2003). A low molecular weight antioxidant decreases weight and lowers tumor incidence. Free Radical Biology & Medicine, 34(1), 93–102.
Moseti, D., Regassa, A., & Kim, W. K. (2016). Molecular regulation of Adipogenesis and potential anti-Adipogenic bioactive molecules. International Journal of Molecular Sciences, 17(1), 124. https://doi.org/10.3390/ijms17010124.
Mouche, S., Mkaddem, S. B., Wang, W., Katic, M., Tseng, Y. H., Carnesecchi, S., Steger, K., Foti, M., Meier, C. A., Muzzin, P., Kahn, C. R., Ogier-Denis, E., & Szanto, I. (2007). Reduced expression of the NADPH oxidase NOX4 is a hallmark of adipocyte differentiation. Biochimica et Biophysica Acta, 1773(7), 1015–1027. https://doi.org/10.1016/j.bbamcr.2007.03.003.
Munekata, K., & Sakamoto, K. (2009). Forkhead transcription factor Foxo1 is essential for adipocyte differentiation. In Vitro Cellular & Developmental Biology Animal, 45(10), 642–651. https://doi.org/10.1007/s11626-009-9230-5.
Murphy, S., Martin, S., & Parton, R. G. (2009). Lipid droplet-organelle interactions; sharing the fats. Biochimica et Biophysica Acta, 1791(6), 441–447. https://doi.org/10.1016/j.bbalip.2008.07.004.
Nakae, J., Kitamura, T., Kitamura, Y., Biggs, W. H., 3rd, Arden, K. C., & Accili, D. (2003). The forkhead transcription factor Foxo1 regulates adipocyte differentiation. Developmental Cell, 4(1), 119–129.
Nam, W. S., Park, K. M., & Park, J. W. (2012). RNA interference targeting cytosolic NADP(+)-dependent isocitrate dehydrogenase exerts anti-obesity effect in vitro and in vivo. Biochimica et Biophysica Acta, 1822(8), 1181–1188. https://doi.org/10.1016/j.bbadis.2012.04.003.
Nguyen, A., Guo, J., Banyard, D. A., Fadavi, D., Toranto, J. D., Wirth, G. A., Paydar, K. Z., Evans, G. R., & Widgerow, A. D. (2016). Stromal vascular fraction: A regenerative reality? Part 1: Current concepts and review of the literature. Journal of Plastic, Reconstructive & Aesthetic Surgery: JPRAS, 69(2), 170–179. https://doi.org/10.1016/j.bjps.2015.10.015.
Otto, T. C., & Lane, M. D. (2005). Adipose development: From stem cell to adipocyte. Critical Reviews in Biochemistry and Molecular Biology, 40(4), 229–242. https://doi.org/10.1080/10409230591008189.
Panday, A., Sahoo, M. K., Osorio, D., & Batra, S. (2015). NADPH oxidases: An overview from structure to innate immunity-associated pathologies. Cellular & Molecular Immunology, 12(1), 5–23. https://doi.org/10.1038/cmi.2014.89.
Pieralisi, A., Martini, C., Soto, D., Vila, M. C., Calvo, J. C., & Guerra, L. N. (2016). N-acetylcysteine inhibits lipid accumulation in mouse embryonic adipocytes. Redox Biology, 9, 39–44. https://doi.org/10.1016/j.redox.2016.05.006.
Quinlan, C. L., Orr, A. L., Perevoshchikova, I. V., Treberg, J. R., Ackrell, B. A., & Brand, M. D. (2012). Mitochondrial complex II can generate reactive oxygen species at high rates in both the forward and reverse reactions. The Journal of Biological Chemistry, 287(32), 27255–27264. https://doi.org/10.1074/jbc.M112.374629.
Riordan, N. H., Ichim, T. E., Min, W. P., Wang, H., Solano, F., Lara, F., Alfaro, M., Rodriguez, J. P., Harman, R. J., Patel, A. N., Murphy, M. P., Lee, R. R., & Minev, B. (2009). Non-expanded adipose stromal vascular fraction cell therapy for multiple sclerosis. Journal of Translational Medicine, 7, 29. https://doi.org/10.1186/1479-5876-7-29.
Rosen, E. D., & MacDougald, O. A. (2006). Adipocyte differentiation from the inside out. Nature Reviews Molecular Cell Biology, 7(12), 885–896. https://doi.org/10.1038/nrm2066.
Rossi, F., & Zatti, M. (1964). Biochemical aspects of phagocytosis in polymorphonuclear leucocytes. NADH and NADPH oxidation by the granules of resting and phagocytizing cells. Experientia, 20(1), 21–23.
Roy, J., Galano, J.-M., Durand, T., Le Guennec, J.-Y., & Lee, J. C.-Y. (2017). Physiological role of reactive oxygen species as promoters of natural defenses. The FASEB Journal, 31, 3729. https://doi.org/10.1096/fj.201700170R.
Ryu, J. M., Lee, H. J., Jung, Y. H., Lee, K. H., Kim, D. I., Kim, J. Y., Ko, S. H., Choi, G. E., Chai, I. I., Song, E. J., JY, O., Lee, S. J., & Han, H. J. (2015). Regulation of stem cell fate by ROS-mediated alteration of metabolism. International Journal of Stem Cells, 8(1), 24–35. 10.15283/ijsc.2015.8.1.24.
Sabharwal, S. S., & Schumacker, P. T. (2014). Mitochondrial ROS in cancer: Initiators, amplifiers or an Achilles’ heel? Nature Reviews Cancer, 14(11), 709–721. https://doi.org/10.1038/nrc3803.
Saitoh, Y., Xiao, L., Mizuno, H., Kato, S., Aoshima, H., Taira, H., Kokubo, K., & Miwa, N. (2010). Novel polyhydroxylated fullerene suppresses intracellular oxidative stress together with repression of intracellular lipid accumulation during the differentiation of OP9 preadipocytes into adipocytes. Free Radical Research, 44(9), 1072–1081. https://doi.org/10.3109/10715762.2010.499905.
Samuelsson, L., Stromberg, K., Vikman, K., Bjursell, G., & Enerback, S. (1991). The CCAAT/enhancer binding protein and its role in adipocyte differentiation: Evidence for direct involvement in terminal adipocyte development. The EMBO Journal, 10(12), 3787–3793.
Samuni, Y., Cook, J. A., Choudhuri, R., Degraff, W., Sowers, A. L., Krishna, M. C., & Mitchell, J. B. (2010). Inhibition of adipogenesis by Tempol in 3T3-L1 cells. Free Radical Biology & Medicine, 49(4), 667–673. https://doi.org/10.1016/j.freeradbiomed.2010.05.028.
Satish, L., Krill-Burger, J. M., Gallo, P. H., Etages, S. D., Liu, F., Philips, B. J., Ravuri, S., Marra, K. G., LaFramboise, W. A., Kathju, S., & Rubin, J. P. (2015). Expression analysis of human adipose-derived stem cells during in vitro differentiation to an adipocyte lineage. BMC Medical Genomics, 8, 41. https://doi.org/10.1186/s12920-015-0119-8.
Sbarra, A. J., & Karnovsky, M. L. (1959). The biochemical basis of phagocytosis. I. Metabolic changes during the ingestion of particles by polymorphonuclear leukocytes. The Journal of Biological Chemistry, 234(6), 1355–1362.
Schroder, K., Wandzioch, K., Helmcke, I., & Brandes, R. P. (2009). Nox4 acts as a switch between differentiation and proliferation in preadipocytes. Arteriosclerosis, Thrombosis, and Vascular Biology, 29(2), 239–245. https://doi.org/10.1161/atvbaha.108.174219.
Slauch, J. M. (2011). How does the oxidative burst of macrophages kill bacteria? Still an open question. Molecular Microbiology, 80(3), 580–583. https://doi.org/10.1111/j.1365-2958.2011.07612.x.
Stephens, J. M. (2012). The fat controller: Adipocyte development. PLoS Biology, 10(11), e1001436. https://doi.org/10.1371/journal.pbio.1001436.
Tahara, E. B., Navarete, F. D., & Kowaltowski, A. J. (2009). Tissue-, substrate-, and site-specific characteristics of mitochondrial reactive oxygen species generation. Free Radical Biology & Medicine, 46(9), 1283–1297. https://doi.org/10.1016/j.freeradbiomed.2009.02.008.
Thomas, D., & Apovian, C. (2017). Macrophage functions in lean and obese adipose tissue. Metabolism: Clinical and Experimental, 72, 120–143. https://doi.org/10.1016/j.metabol.2017.04.005.
Tormos, K. V., Anso, E., Hamanaka, R. B., Eisenbart, J., Joseph, J., Kalyanaraman, B., & Chandel, N. S. (2011). Mitochondrial complex III ROS regulate adipocyte differentiation. Cell Metabolism, 14(4), 537–544. https://doi.org/10.1016/j.cmet.2011.08.007.
Turrens, J. F. (2003). Mitochondrial formation of reactive oxygen species. The Journal of Physiology, 552(Pt 2), 335–344. https://doi.org/10.1113/jphysiol.2003.049478.
Vigilanza, P., Aquilano, K., Baldelli, S., Rotilio, G., & Ciriolo, M. R. (2011). Modulation of intracellular glutathione affects adipogenesis in 3T3-L1 cells. Journal of Cellular Physiology, 226(8), 2016–2024. https://doi.org/10.1002/jcp.22542.
Virtue, S., & Vidal-Puig, A. (2010). Adipose tissue expandability, lipotoxicity and the metabolic syndrome--an allostatic perspective. Biochimica et Biophysica Acta, 1801(3), 338–349. https://doi.org/10.1016/j.bbalip.2009.12.006.
Wang, Y., Hudak, C., & Sul, H. S. (2010a). Role of preadipocyte factor 1 in adipocyte differentiation. Clinical Lipidology, 5(1), 109–115. https://doi.org/10.2217/clp.09.80.
Wang, Y., Zhao, L., Smas, C., & Sul, H. S. (2010b). Pref-1 interacts with fibronectin to inhibit adipocyte differentiation. Molecular and Cellular Biology, 30(14), 3480–3492. https://doi.org/10.1128/mcb.00057-10.
Wang, W., Zhang, Y., Lu, W., & Liu, K. (2015). Mitochondrial reactive oxygen species regulate adipocyte differentiation of mesenchymal stem cells in hematopoietic stress induced by arabinosylcytosine. PLoS One, 10(3), e0120629. https://doi.org/10.1371/journal.pone.0120629.
Weisberg, S. P., McCann, D., Desai, M., Rosenbaum, M., Leibel, R. L., & Ferrante, A. W., Jr. (2003). Obesity is associated with macrophage accumulation in adipose tissue. The Journal of Clinical Investigation, 112(12), 1796–1808. https://doi.org/10.1172/jci19246.
Yan, H., Aziz, E., Shillabeer, G., Wong, A., Shanghavi, D., Kermouni, A., Abdel-Hafez, M., & Lau, D. C. (2002). Nitric oxide promotes differentiation of rat white preadipocytes in culture. Journal of Lipid Research, 43(12), 2123–2129.
Yang, J. Y., Della-Fera, M. A., Rayalam, S., Ambati, S., Hartzell, D. L., Park, H. J., & Baile, C. A. (2008). Enhanced inhibition of adipogenesis and induction of apoptosis in 3T3-L1 adipocytes with combinations of resveratrol and quercetin. Life Sciences, 82(19–20), 1032–1039. https://doi.org/10.1016/j.lfs.2008.03.003.
Yoshihara, A., Hara, T., Kawashima, A., Akama, T., Tanigawa, K., Wu, H., Sue, M., Ishido, Y., Hiroi, N., Ishii, N., Yoshino, G., & Suzuki, K. (2012). Regulation of dual oxidase expression and H2O2 production by thyroglobulin. Thyroid : Official Journal of the American Thyroid Association, 22(10), 1054–1062. https://doi.org/10.1089/thy.2012.0003.
Younce, C., & Kolattukudy, P. (2012). MCP-1 induced protein promotes adipogenesis via oxidative stress, endoplasmic reticulum stress and autophagy. Cellular Physiology and Biochemistry : International Journal of Experimental Cellular Physiology, Biochemistry, and Pharmacology, 30(2), 307–320. https://doi.org/10.1159/000339066.
Zhang, M., Ikeda, K., JW, X., Yamori, Y., Gao, X. M., & Zhang, B. L. (2009). Genistein suppresses adipogenesis of 3T3-L1 cells via multiple signal pathways. Phytotherapy Research: PTR, 23(5), 713–718. https://doi.org/10.1002/ptr.2724.
Zhao, W.-E., Fan, J., Gao, R., & Ngoc, N. B. (2017). Suppressive effects of carotenoids on proliferation and differentiation of 3T3-L1 Preadipocytes. Journal of Food and Nutrition Research, 5(2), 129–136. 10.12691/jfnr-5-2-9.
Acknowledgements
This research was funded by the South African Medical Research Council in terms of the SAMRC's Flagship Award Project SAMRC-RFA-UFSP-01-2013/STEM CELLS, the SAMRC Extramural Unit for Stem Cell Research and Therapy and the Institute for Cellular and Molecular Medicine of the University of Pretoria.
Conflicts of Interest Statement
The authors have no conflicts of interest to declare.
Author Contributions
Danielle de Villiers drafted the first version of the manuscript with input from Marnie Potgieter and Michael Pepper. Melvin Ambele, Chrisna Durandt, and Ladislaus Adam provided intellectual input and contributed to the writing of the manuscript. All authors vetted and approved the final version of the manuscript. Michael Pepper conceived the project.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2017 Springer International Publishing AG
About this paper
Cite this paper
de Villiers, D., Potgieter, M., Ambele, M.A., Adam, L., Durandt, C., Pepper, M.S. (2017). The Role of Reactive Oxygen Species in Adipogenic Differentiation. In: Van Pham, P. (eds) Stem Cells: Biology and Engineering. Advances in Experimental Medicine and Biology(), vol 1083. Springer, Cham. https://doi.org/10.1007/5584_2017_119
Download citation
DOI: https://doi.org/10.1007/5584_2017_119
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-77481-7
Online ISBN: 978-3-319-77482-4
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)