Extracellular ATP is generated by ATP synthase complex in adipocyte lipid rafts.
Open accessAbstract
Mitochondrial biogenesis is known to accompany adipogenesis to complement ATP and acetyl-CoA required for lipogenesis. Here, we demonstrated that mitochondrial proteins such as ATP synthase alpha and beta, and cytochrome c were highly expressed during the 3T3-L1 differentiation into adipocytes. Fully-differentiated adipocytes showed a significant increase of mitochondria under electron microscopy. Analysis by immunofluorescence, cellular fractionation, and surface biotinylation demonstrated the elevated levels of ATP synthase complex found not only in the mitochondria but also on the cell surface (particularly lipid rafts) of adipocytes. High rate of ATP (more than 30 microM) synthesis from the added ADP and P(i) in the adipocyte media suggests the involvement of the surface ATP synthase complex for the extracellular ATP synthesis. In addition, this ATP synthesis was significantly inhibited in the presence of oligomycin, an ATP synthase inhibitor, and carbonyl cyanide m-chlorophenylhydrazone (CCCP), an ATP synthase uncoupler. Decrease of extracellular ATP synthesis in acidic but not in basic media further indicates that the surface ATP synthase may also be regulated by proton gradient through the plasma membrane.
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Mitochondrial density increases dramatically, and mitochondrial remodeling occurs during white adipocyte differentiation, suggesting that mitochondrial functions are required to support the multiple biological roles of mature white adipocytes.
“However, mitochondrial density increases dramatically, and mitochondrial remodeling occurs during white adipocyte differentiation (156 -158), suggesting that mitochondrial functions are required to support the multiple biological roles of mature white adipocytes.”
From The role of mitochondria in the pathogenesis of type 2 diabetes (2010) · cites this paper as [157]
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Giorgio, V., Bisetto, E., Franca, R., Harris, D. A., Passamonti, S., & Lippe, G. (2010) · Journal of Bioenergetics and Biomembranes · doi:10.1007/s10863-010-9270-2 · Cited by 30 · see citing works
Cardouat, G., Duparc, T., Fried, S. G., Perret, B., Najib, S., & Martinez, L. O. (2017) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2017.05.005 · Cited by 29 · see citing works
Kim, M.-K., Oh, S., Lee, J. H., Im, H., Ryu, Y. M., Oh, E., Lee, J., Lee, E., & Sul, D. (2004) · Experimental & Molecular Medicine · doi:10.1038/emm.2004.52 · Cited by 29 · see citing works
Temporal Phosphoproteome Dynamics Induced by an ATP Synthase Inhibitor Citreoviridin*
Hu, C.-W., Hsu, C., Wang, Y., Ishihama, Y., Ku, W., Huang, H., & Juan, H. (2015) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m115.051383 · Cited by 28 · see citing works
Morelli, A. M., & Scholkmann, F. (2024) · Biochimie · doi:10.1016/j.biochi.2024.01.018 · Cited by 27 · see citing works
Kim, B., Lee, J., Choo, H. J., Lee, C. S., Jung, S., Yi, J.-S., Ham, Y., Lee, J., Hong, J. H., Kang, M. J., et al. (2010) · PROTEOMICS · doi:10.1002/pmic.200900826 · Cited by 27 · see citing works
“by immunofluorescence, biotin-surface labeling, and plasma membrane fractionation from various mammalian cell lines [4–10].”
BackgroundSecretion of adenylate kinase 1 is required for extracellular ATP synthesis in C2C12 myotubes
Choo, H. J., Kim, B., Kwon, O.-B., Lee, C. S., Choi, J., & Ko, Y. (2008) · Experimental & Molecular Medicine · doi:10.3858/emm.2008.40.2.220 · Cited by 27 · see citing works
“ATP synthase is expressed on the surfaces of mammalian cells (Arakaki et al., 2003; Bae et al., 2004; Kim et al., 2004; Kim et al., 2006; Martinez et al., 2003), and treatment with ATP synthase inhibitors (oligomycin and efrapeptin) and anti-ATP synthase antibody decreases exATP generation in HUVECs (Arakaki et al.”
BackgroundMethodInfluentialProtein kinase A mediates microglial activation induced by plasminogen and gangliosides
Min, K., Yang, M.-S., Jou, I., & Joe, E.-H. (2004) · Experimental & Molecular Medicine · doi:10.1038/emm.2004.58 · Cited by 27 · see citing works
Nutrigenomic Analysis of Diet-Gene Interactions on Functional Supplements for Weight Management
Lau, F. C., Bagchi, M., Sen, C. K., Roy, S., & Bagchi, D. (2008) · Current Genomics · doi:10.2174/138920208784533638 · Cited by 26 · see citing works
“It has been shown that PGC1-alpha is induced during mitochondrial biogenesis accompanied by adipogenesis to complement the requirement of ATP and acetyl-CoA for lipogenesis [98].”
BackgroundKim, B., Lee, C. S., Yi, J.-S., Lee, J.-H., Lee, J.-W., Choo, H. J., Jung, S.-Y., Kim, M., Lee, S., Lee, M., et al. (2010) · Expert Review of Proteomics · doi:10.1586/epr.10.87 · Cited by 26 · see citing works
Identification of hydrophobic proteins as biomarker candidates for colorectal cancer
Álvarez-Chaver, P., Rodríguez-Piñeiro, A. M., Rodrı́guez-Berrocal, F. J., Martínez-Zorzano, V. S., & de la Cadena, M. P. (2006) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2006.10.001 · Cited by 26 · see citing works
Melatonin: Regulation of Prion Protein Phase Separation in Cancer Multidrug Resistance
Loh, D., & Reiter, R. J. (2022) · Molecules · doi:10.3390/molecules27030705 · Cited by 25 · see citing works
Transcriptional regulation of Zic3 by heterodimeric AP-1(c-Jun/c-Fos) during Xenopus development
Lee, S., Lee, H., Moon, J. S., Kim, J., Park, J., Lee, J., Park, M. J., & Kim, J. (2004) · Experimental & Molecular Medicine · doi:10.1038/emm.2004.59 · Cited by 25 · see citing works
Giltaire, S., Lambert, S., & Poumay, Y. (2010) · Journal of Cellular Physiology · doi:10.1002/jcp.22496 · Cited by 24 · see citing works
“Kim et al. (2004) have also demonstrated that plasmamembrane lipid rafts do contain ATP synthase complex.”
BackgroundBecerra, S. P. (2012) · International Journal of Oncology · doi:10.3892/ijo.2012.1431 · Cited by 24 · see citing works
“cells such as endothelial cells (4), adipocytes (5), keratinocytes (6), and hepatic cells (7).”
BackgroundGhosh, S., & Saxena, R. K. (2004) · Experimental & Molecular Medicine · doi:10.1038/emm.2004.51 · Cited by 24 · see citing works
Weil, C., Sabin, N., Bugeon, J., Pabœuf, G., & Lefèvre, F. (2009) · Comparative Biochemistry and Physiology Part D Genomics and Proteomics · doi:10.1016/j.cbd.2009.05.002 · Cited by 20 · see citing works
Howard, A. D., Verghese, P. B., Arrese, E. L., & Soulages, J. L. (2010) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-010-0650-z · Cited by 20 · see citing works
Sphingosine mediates FTY720-induced apoptosis in LLC-PK1 cells
Lee, W.-J., Yoo, H., Suh, P., Lim, J., Oh, S., & Lee, Y.-M. (2004) · Experimental & Molecular Medicine · doi:10.1038/emm.2004.54 · Cited by 20 · see citing works
Kita, T., & Arakaki, N. (2015) · Biomedical Research · doi:10.2220/biomedres.36.115 · Cited by 19 · see citing works
Knockdown of aquaporin-8 induces mitochondrial dysfunction in 3T3-L1 cells
Ikaga, R., Namekata, I., Kotiadis, V. N., Ogawa, H. K., Duchen, M. R., Tanaka, H., & Iida‐Tanaka, N. (2015) · Biochemistry and Biophysics Reports · doi:10.1016/j.bbrep.2015.09.009 · Cited by 19 · see citing works
“adipocyte differentiation [27,28] suggesting that mitochondrial”
Mitochondrial oxidative phosphorylation complexes exist in the sarcolemma of skeletal muscle
Lee, H., Kim, S.-H., Lee, J., Yang, Y.-H., Nam, J., Kim, B., & Ko, Y. (2016) · BMB Reports · doi:10.5483/bmbrep.2016.49.2.232 · Cited by 18 · see citing works
“in the plasma membrane by using various experimental approaches such as cellular fractionation, immunofluorescence, and cell surface biotinylation (10, 11, 22-26), indicating that”
Methodβ-amyloid Peptide Binds and Regulates Ectopic ATP Synthase α-Chain on Neural Surface
Xing, S., Chen, B., Shen, D., & Zhu, C. (2011) · International Journal of Neuroscience · doi:10.3109/00207454.2011.649867 · Cited by 18 · see citing works
“Media were collected at sequential time points and assayed for ATP content by CellTiterGlo luminescence assay (Promega) as described [5].”
MethodLoh, D., & Reiter, R. J. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23158122 · Cited by 17 · see citing works
Amplification of Diacylglycerol Activation of Protein Kinase C by Cholesterol
Armstrong, D. L., & Zidovetzki, R. (2008) · Biophysical Journal · doi:10.1529/biophysj.107.121426 · Cited by 17 · see citing works
Park, M., Oh, H., & York, D. A. (2008) · Peptides · doi:10.1016/j.peptides.2008.11.005 · Cited by 17 · see citing works
“While ATP synthase activity has been associated with the activity of this protein in mitochondrial membranes, it may act as an ATP hydrolase in hepatic plasma membranes [13,22] (Park, unpublished data).”
Contessi, S., Haraux, F., Mavelli, I., & Lippe, G. (2005) · Journal of Bioenergetics and Biomembranes · doi:10.1007/s10863-005-8643-4 · Cited by 16 · see citing works
Chang, Y., Wang, C., Yin, C.-F., Wu, C.-H., Huang, H., & Juan, H. (2022) · Molecular & Cellular Proteomics · doi:10.1016/j.mcpro.2022.100237 · Cited by 15 · see citing works
“ecto-ATP synthase retains the catalytic activity of ATP synthase to phosphorylate ADP and generate extracellular ATP (eATP) (23, 24).”
BackgroundMuñoz-Antolí, C., Cortés, A., Sotillo, J., Fried, B. N., Esteban, J. G., & Toledo, R. (2014) · Journal of Proteomics · doi:10.1016/j.jprot.2014.02.014 · Cited by 15 · see citing works
“[37] Kim BW, Choo HJ, Lee JW, Kim JH, Ko YG.”
BackgroundBiomechanical stimulation effects on the metabolism of adipocyte
Moldovan, L. M., Kislev, N., Lustig, M., Pomeraniec, L., & Benayahu, D. (2020) · Journal of Cellular Physiology · doi:10.1002/jcp.29714 · Cited by 15 · see citing works
Park, H.-W., Song, J., Kim, K.-S., Han, Y., Kim, C., Yi, S.-Y., & Yun, Y. (2004) · Experimental & Molecular Medicine · doi:10.1038/emm.2004.53 · Cited by 15 · see citing works
Lee, H., Kim, B., Lee, J.-W., Hong, J. H., Lee, J.-W., Kim, H.-L., Lee, J., & Ko, Y. (2017) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2017.08.016 · Cited by 14 · see citing works
“Indeed, the cell-surface expression of OXPHOS V subunits such as ATP synthase and has been extensively investigated in a variety of mammalian cells such as tumor cells, endothelial cells, hepatocytes, adipocytes, myotubes and lymphocytes [11, 28-31].”
BackgroundPDE 5 inhibitor improves insulin sensitivity by enhancing mitochondrial function in adipocytes
Yu, H. M., Chung, H. K., Kim, K. S., Lee, J. M., Hong, J. H., & Park, K. S. (2017) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2017.08.140 · Cited by 14 · see citing works
Novel molecular targets for prevention of obesity and osteoporosis
Rayalam, S., Yang, J., Della‐Fera, M. A., & Baile, C. A. (2011) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2010.11.009 · Cited by 13 · see citing works
“[50].”
Efficient extra‐mitochondrial aerobic ATP synthesis in neuronal membrane systems
Ravera, S., Bartolucci, M., Calzia, D., Morelli, A. M., & Panfoli, I. (2021) · Journal of Neuroscience Research · doi:10.1002/jnr.24865 · Cited by 13 · see citing works
“Adipocyte plasma membrane rafts express cytochrome c and ATP synthase (Kim et al., 2004).”
BackgroundEncinas-García, T., Mendoza-Cano, F., Muhlia‐Almazán, A., Porchas‐Cornejo, M. A., & Sánchez‐Paz, A. (2023) · Reviews in Fisheries Science & Aquaculture · doi:10.1080/23308249.2023.2254401 · Cited by 12 · see citing works
“…thought to be limited to the inner mitochondrial membrane, new evidence has found that this enzyme complex can also be found on the cell surface of a variety of normal (endothelial, hepatocytes, adipocytes) and tumor cells (Das et al. 1994; Kim et al. 2004; Martinez et al. 2003; Moser et al. 1999).”
BackgroundKim, J., Choi, B. H., Jang, K. L., & Min, D. S. (2004) · Experimental & Molecular Medicine · doi:10.1038/emm.2004.57 · Cited by 12 · see citing works
Lu, Z., Hu, H., & Killiny, N. (2016) · Physiological Entomology · doi:10.1111/phen.12161 · Cited by 11 · see citing works
“The presence of ATP synthase is demonstrated experimentally at both sites (Galetto et al., 2011) and the enzyme is shown to contribute to the production of extracellular ATP (Kim et al., 2004; Lin et al., 2009).”
BackgroundGao, J., Zhang, T., Kang, Z., Ting, W., Xu, L., & Yin, D. (2017) · Molecular Immunology · doi:10.1016/j.molimm.2017.08.004 · Cited by 11 · see citing works
Regulation of neuronal toxicity of β-amyloid oligomers by surface ATP synthase
Xing, S., Shen, D., Chen, C., WANG, J., Liu, T., & Yu, Z. (2013) · Molecular Medicine Reports · doi:10.3892/mmr.2013.1722 · Cited by 11 · see citing works
Safety assessment of a calcium-potassium salt of (−)-hydroxycitric acid
Stohs, S. J., Lau, F. C., Kim, D., Kim, S. U., Bagchi, M., & Bagchi, D. (2010) · Toxicology Mechanisms and Methods · doi:10.3109/15376516.2010.521207 · Cited by 10 · see citing works
“It has been shown that PGC1-α gene is induced during mitochondrial biogenesis accompanied by adipogenesis to complement the requirement of ATP and acetyl-CoA for lipogenesis (Kim et al. 2004).”
BackgroundMitochondrial and cell-surface F0F1ATPsynthase in innate and acquired cardioprotection
Lippe, G., Bisetto, E., Comelli, M., Contessi, S., Pancrazio, F. D., & Mavelli, I. (2009) · Journal of Bioenergetics and Biomembranes · doi:10.1007/s10863-009-9208-8 · Cited by 10 · see citing works
“…target of calmodulin It has emerged that an enrichment of F0F1 components occurs in caveole/lipid rafts on plasma membrane of different cell types (Kim et al. 2004; Kim et al. 2006; Wang et al. 2006; Yamamoto et al. 2007), sometimes together with some other mitochondrial proteins suggesting…”
BackgroundPark, M., Lyons, J., Oh, H., Yu, Y., Woltering, E. A., Greenway, F. L., & York, D. A. (2008) · International Journal of Obesity · doi:10.1038/ijo.2008.16 · Cited by 10 · see citing works
Lindqvist, A., Berger, K., & Erlanson‐Albertsson, C. (2008) · Nutritional Neuroscience · doi:10.1179/147683008x301397 · Cited by 10 · see citing works
Lipid-lowering activity and mechanism of peptides from jellyfish Nemopilema nomurai
Ma, Y., Yu, H., Xing, R., Liu, S., & Li, P. (2023) · Journal of Functional Foods · doi:10.1016/j.jff.2023.105421 · Cited by 9 · see citing works
- Authors
- Kim, B.-W., Choo, H.-J., Lee, J.-W., Kim, J.-H., & Ko, Y.-G.
- Affiliations
- Korea University (KR)
- ORCID
- Kim, Ji-Hyun
- Venue
- Experimental & Molecular Medicine
- Published
- 2004-10-01
- Volume
- 36
- Issue
- 5
- Pages
- 476-485
- ISSN
- 1226-3613 (ISSN-L)
- 2092-6413
- OpenAlex
- W2033234176
- Cited by
- 128
- References
- 31
- Citations by year
- 2026: 1 · 2024: 3 · 2023: 3 · 2022: 4 · 2021: 3 · 2020: 7 · 2018: 3 · 2017: 6 · 2016: 4 · 2015: 4 · 2014: 4 · 2013: 1 · 2012: 6
- FWCI
- 4.03
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Experimental & Molecular Medicine (publishedVersion, cc-by-nc)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › ATP Synthase and ATPases Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Physiology › Adenosine and Purinergic Signaling
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Keywords
- extracellular ATP, ATP synthase, adipocytes, lipid rafts, mitochondrial biogenesis, adipogenesis, 3T3-L1 cells, cytochrome c, oligomycin, CCCP, proton gradient, plasma membrane, mitochondrial protein translocation
- MeSH terms
- Adenosine Triphosphate, Animals, Cell Differentiation, Cell Membrane, Cells, Cultured, Humans, Mitochondria, Adipocytes, Membrane Microdomains, Mitochondrial Proton-Translocating ATPases, Mice
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