This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Wilson-Fritch, L.
Right arrow Articles by Corvera, S.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Wilson-Fritch, L.
Right arrow Articles by Corvera, S.

 Previous Article  |  Next Article 

Molecular and Cellular Biology, February 2003, p. 1085-1094, Vol. 23, No. 3
0270-7306/03/$08.00+0     DOI: 10.1128/MCB.23.3.1085-1094.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.

Mitochondrial Biogenesis and Remodeling during Adipogenesis and in Response to the Insulin Sensitizer Rosiglitazone

Leanne Wilson-Fritch,1,2 Alison Burkart,1 Gregory Bell,1 Karen Mendelson,1 John Leszyk,1 Sarah Nicoloro,1,3 Michael Czech,1,3 and Silvia Corvera1,2*

Program in Molecular Medicine,1 Interdisciplinary Graduate Program,2 Department of Biochemistry and Molecular Pharmacology, University of Massachusetts Medical School, Worcester, Massachusetts 016153

Received 19 February 2002/ Returned for modification 12 April 2002/ Accepted 16 October 2002

White adipose tissue is an important endocrine organ involved in the control of whole-body metabolism, insulin sensitivity, and food intake. To better understand these functions, 3T3-L1 cell differentiation was studied by using combined proteomic and genomic strategies. The proteomics approach developed here exploits velocity gradient centrifugation as an alternative to isoelectric focusing for protein separation in the first dimension. A 20- to 30-fold increase in the concentration of numerous mitochondrial proteins was observed during adipogenesis, as determined by mass spectrometry and database correlation analysis. Light and electron microscopy confirmed a large increase in the number of mitochondrion profiles with differentiation. Furthermore, mRNA profiles obtained by using Affymetrix GeneChips revealed statistically significant increases in the expression of many nucleus-encoded mitochondrial genes during adipogenesis. Qualitative changes in mitochondrial composition also occur during adipose differentiation, as exemplified by increases in expression of proteins involved in fatty acid metabolism and of mitochondrial chaperones. Furthermore, the insulin sensitizer rosiglitazone caused striking changes in mitochondrial shape and expression of selective mitochondrial proteins. Thus, although mitochondrial biogenesis has classically been associated with brown adipocyte differentiation and thermogenesis, our results reveal that mitochondrial biogenesis and remodeling are inherent to adipose differentiation per se and are influenced by the actions of insulin sensitizers.

* Corresponding author. Mailing address: Program in Molecular Medicine, University of Massachusetts Medical School, 373 Plantation St., Worcester, MA 01605. Phone: (508) 856-6898. Fax: (508) 856-1617. E-mail: silvia.corvera{at}umassmed.edu.

Molecular and Cellular Biology, February 2003, p. 1085-1094, Vol. 23, No. 3
0022-538X/03/$08.00+0     DOI: 10.1128/MCB.23.3.1085-1094.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Guilherme, A., Tesz, G. J., Guntur, K. V. P., Czech, M. P. (2009). Tumor Necrosis Factor-{alpha} Induces Caspase-mediated Cleavage of Peroxisome Proliferator-activated Receptor {gamma} in Adipocytes. J. Biol. Chem. 284: 17082-17091 [Abstract] [Full Text]  
  • Hausman, G. J., Dodson, M. V., Ajuwon, K., Azain, M., Barnes, K. M., Guan, L. L., Jiang, Z., Poulos, S. P., Sainz, R. D., Smith, S., Spurlock, M., Novakofski, J., Fernyhough, M. E., Bergen, W. G. (2009). BOARD-INVITED REVIEW: The biology and regulation of preadipocytes and adipocytes in meat animals. J ANIM SCI 87: 1218-1246 [Abstract] [Full Text]  
  • Li, B., Shin, J., Lee, K. (2009). Interferon-Stimulated Gene ISG12b1 Inhibits Adipogenic Differentiation and Mitochondrial Biogenesis in 3T3-L1 Cells. Endocrinology 150: 1217-1224 [Abstract] [Full Text]  
  • Shi, X., Burkart, A., Nicoloro, S. M., Czech, M. P., Straubhaar, J., Corvera, S. (2008). Paradoxical Effect of Mitochondrial Respiratory Chain Impairment on Insulin Signaling and Glucose Transport in Adipose Cells. J. Biol. Chem. 283: 30658-30667 [Abstract] [Full Text]  
  • Gealekman, O., Burkart, A., Chouinard, M., Nicoloro, S. M., Straubhaar, J., Corvera, S. (2008). Enhanced angiogenesis in obesity and in response to PPAR{gamma} activators through adipocyte VEGF and ANGPTL4 production. Am. J. Physiol. Endocrinol. Metab. 295: E1056-E1064 [Abstract] [Full Text]  
  • Quintanilla, R. A., Jin, Y. N., Fuenzalida, K., Bronfman, M., Johnson, G. V. W. (2008). Rosiglitazone Treatment Prevents Mitochondrial Dysfunction in Mutant Huntingtin-expressing Cells: POSSIBLE ROLE OF PEROXISOME PROLIFERATOR-ACTIVATED RECEPTOR-{gamma} (PPAR{gamma}) IN THE PATHOGENESIS OF HUNTINGTON DISEASE. J. Biol. Chem. 283: 25628-25637 [Abstract] [Full Text]  
  • Gondret, F., Guitton, N., Guillerm-Regost, C., Louveau, I. (2008). Regional differences in porcine adipocytes isolated from skeletal muscle and adipose tissues as identified by a proteomic approach. J ANIM SCI 86: 2115-2125 [Abstract] [Full Text]  
  • Tedesco, L., Valerio, A., Cervino, C., Cardile, A., Pagano, C., Vettor, R., Pasquali, R., Carruba, M. O., Marsicano, G., Lutz, B., Pagotto, U., Nisoli, E. (2008). Cannabinoid Type 1 Receptor Blockade Promotes Mitochondrial Biogenesis Through Endothelial Nitric Oxide Synthase Expression in White Adipocytes. Diabetes 57: 2028-2036 [Abstract] [Full Text]  
  • Petrovic, N., Shabalina, I. G., Timmons, J. A., Cannon, B., Nedergaard, J. (2008). Thermogenically competent nonadrenergic recruitment in brown preadipocytes by a PPAR{gamma} agonist. Am. J. Physiol. Endocrinol. Metab. 295: E287-E296 [Abstract] [Full Text]  
  • Schrauwen-Hinderling, V. B., Mensink, M., Hesselink, M. K. C., Sels, J.-P., Kooi, M. E., Schrauwen, P. (2008). The Insulin-Sensitizing Effect of Rosiglitazone in Type 2 Diabetes Mellitus Patients Does Not Require Improved in Vivo Muscle Mitochondrial Function. J. Clin. Endocrinol. Metab. 93: 2917-2921 [Abstract] [Full Text]  
  • Farmer, S. R. (2008). Molecular determinants of brown adipocyte formation and function. Genes Dev. 22: 1269-1275 [Abstract] [Full Text]  
  • Kim, M. J., Jardel, C., Barthelemy, C., Jan, V., Bastard, J. P., Fillaut-Chapin, S., Houry, S., Capeau, J., Lombes, A. (2008). Mitochondrial DNA Content, an Inaccurate Biomarker of Mitochondrial Alteration in Human Immunodeficiency Virus-Related Lipodystrophy. Antimicrob. Agents Chemother. 52: 1670-1676 [Abstract] [Full Text]  
  • Benton, C. R., Holloway, G. P., Campbell, S. E., Yoshida, Y., Tandon, N. N., Glatz, J. F. C., Luiken, J. J. J. F. P., Spriet, L. L., Bonen, A. (2008). Rosiglitazone increases fatty acid oxidation and fatty acid translocase (FAT/CD36) but not carnitine palmitoyltransferase I in rat muscle mitochondria. J. Physiol. 586: 1755-1766 [Abstract] [Full Text]  
  • Christianson, J. L., Nicoloro, S., Straubhaar, J., Czech, M. P. (2008). Stearoyl-CoA Desaturase 2 Is Required for Peroxisome Proliferator-activated Receptor {gamma} Expression and Adipogenesis in Cultured 3T3-L1 Cells. J. Biol. Chem. 283: 2906-2916 [Abstract] [Full Text]  
  • Brodbeck, J., Balestra, M. E., Saunders, A. M., Roses, A. D., Mahley, R. W., Huang, Y. (2008). Rosiglitazone increases dendritic spine density and rescues spine loss caused by apolipoprotein E4 in primary cortical neurons. Proc. Natl. Acad. Sci. USA 105: 1343-1346 [Abstract] [Full Text]  
  • Koh, E. H., Park, J.-Y., Park, H.-S., Jeon, M. J., Ryu, J. W., Kim, M., Kim, S. Y., Kim, M.-S., Kim, S.-W., Park, I. S., Youn, J. H., Lee, K.-U. (2007). Essential Role of Mitochondrial Function in Adiponectin Synthesis in Adipocytes. Diabetes 56: 2973-2981 [Abstract] [Full Text]  
  • Gustafson, B., Hammarstedt, A., Andersson, C. X., Smith, U. (2007). Inflamed Adipose Tissue: A Culprit Underlying the Metabolic Syndrome and Atherosclerosis. Arterioscler. Thromb. Vasc. Bio. 27: 2276-2283 [Abstract] [Full Text]  
  • Qiang, L., Wang, H., Farmer, S. R. (2007). Adiponectin Secretion Is Regulated by SIRT1 and the Endoplasmic Reticulum Oxidoreductase Ero1-L{alpha}. Mol. Cell. Biol. 27: 4698-4707 [Abstract] [Full Text]  
  • Rong, J. X., Qiu, Y., Hansen, M. K., Zhu, L., Zhang, V., Xie, M., Okamoto, Y., Mattie, M. D., Higashiyama, H., Asano, S., Strum, J. C., Ryan, T. E. (2007). Adipose Mitochondrial Biogenesis Is Suppressed in db/db and High-Fat Diet-Fed Mice and Improved by Rosiglitazone. Diabetes 56: 1751-1760 [Abstract] [Full Text]  
  • Wang, Z. V., Schraw, T. D., Kim, J.-Y., Khan, T., Rajala, M. W., Follenzi, A., Scherer, P. E. (2007). Secretion of the Adipocyte-Specific Secretory Protein Adiponectin Critically Depends on Thiol-Mediated Protein Retention. Mol. Cell. Biol. 27: 3716-3731 [Abstract] [Full Text]  
  • Chevillotte, E., Giralt, M., Miroux, B., Ricquier, D., Villarroya, F. (2007). Uncoupling Protein-2 Controls Adiponectin Gene Expression in Adipose Tissue Through the Modulation of Reactive Oxygen Species Production. Diabetes 56: 1042-1050 [Abstract] [Full Text]  
  • Rodrigue-Way, A., Demers, A., Ong, H., Tremblay, A. (2007). A Growth Hormone-Releasing Peptide Promotes Mitochondrial Biogenesis and a Fat Burning-Like Phenotype through Scavenger Receptor CD36 in White Adipocytes. Endocrinology 148: 1009-1018 [Abstract] [Full Text]  
  • Zvonic, S., Lefevre, M., Kilroy, G., Floyd, Z. E., DeLany, J. P., Kheterpal, I., Gravois, A., Dow, R., White, A., Wu, X., Gimble, J. M. (2007). Secretome of Primary Cultures of Human Adipose-derived Stem Cells: Modulation of Serpins by Adipogenesis. Mol. Cell. Proteomics 6: 18-28 [Abstract] [Full Text]  
  • Hondares, E., Mora, O., Yubero, P., de la Concepcion, M. R., Iglesias, R., Giralt, M., Villarroya, F. (2006). Thiazolidinediones and Rexinoids Induce Peroxisome Proliferator-Activated Receptor-Coactivator (PGC)-1{alpha} Gene Transcription: An Autoregulatory Loop Controls PGC-1{alpha} Expression in Adipocytes via Peroxisome Proliferator-Activated Receptor-{gamma} Coactivation. Endocrinology 147: 2829-2838 [Abstract] [Full Text]  
  • Nawrocki, A. R., Rajala, M. W., Tomas, E., Pajvani, U. B., Saha, A. K., Trumbauer, M. E., Pang, Z., Chen, A. S., Ruderman, N. B., Chen, H., Rossetti, L., Scherer, P. E. (2006). Mice Lacking Adiponectin Show Decreased Hepatic Insulin Sensitivity and Reduced Responsiveness to Peroxisome Proliferator-activated Receptor {gamma} Agonists. J. Biol. Chem. 281: 2654-2660 [Abstract] [Full Text]  
  • Bogacka, I., Ukropcova, B., McNeil, M., Gimble, J. M., Smith, S. R. (2005). Structural and Functional Consequences of Mitochondrial Biogenesis in Human Adipocytes in Vitro. J. Clin. Endocrinol. Metab. 90: 6650-6656 [Abstract] [Full Text]  
  • Christian, M., Kiskinis, E., Debevec, D., Leonardsson, G., White, R., Parker, M. G. (2005). RIP140-Targeted Repression of Gene Expression in Adipocytes. Mol. Cell. Biol. 25: 9383-9391 [Abstract] [Full Text]  
  • DeLany, J. P., Floyd, Z. E., Zvonic, S., Smith, A., Gravois, A., Reiners, E., Wu, X., Kilroy, G., Lefevre, M., Gimble, J. M. (2005). Proteomic Analysis of Primary Cultures of Human Adipose-derived Stem Cells: Modulation by Adipogenesis. Mol. Cell. Proteomics 4: 731-740 [Abstract] [Full Text]  
  • Scott, E. M, Carter, A. M, Findlay, J. B. (2005). The application of proteomics to diabetes. Diabetes and Vascular Disease Research 2: 54-60 [Abstract]  
  • Bogacka, I., Xie, H., Bray, G. A., Smith, S. R. (2005). Pioglitazone Induces Mitochondrial Biogenesis in Human Subcutaneous Adipose Tissue In Vivo. Diabetes 54: 1392-1399 [Abstract] [Full Text]  
  • Gleyzer, N., Vercauteren, K., Scarpulla, R. C. (2005). Control of Mitochondrial Transcription Specificity Factors (TFB1M and TFB2M) by Nuclear Respiratory Factors (NRF-1 and NRF-2) and PGC-1 Family Coactivators. Mol. Cell. Biol. 25: 1354-1366 [Abstract] [Full Text]  
  • Brasaemle, D. L., Dolios, G., Shapiro, L., Wang, R. (2004). Proteomic Analysis of Proteins Associated with Lipid Droplets of Basal and Lipolytically Stimulated 3T3-L1 Adipocytes. J. Biol. Chem. 279: 46835-46842 [Abstract] [Full Text]  
  • Carriere, A., Carmona, M.-C., Fernandez, Y., Rigoulet, M., Wenger, R. H., Penicaud, L., Casteilla, L. (2004). Mitochondrial Reactive Oxygen Species Control the Transcription Factor CHOP-10/GADD153 and Adipocyte Differentiation: A MECHANISM FOR HYPOXIA-DEPENDENT EFFECT. J. Biol. Chem. 279: 40462-40469 [Abstract] [Full Text]  
  • Yoneda, T., Benedetti, C., Urano, F., Clark, S. G., Harding, H. P., Ron, D. (2004). Compartment-specific perturbation of protein handling activates genes encoding mitochondrial chaperones. J. Cell Sci. 117: 4055-4066 [Abstract] [Full Text]  
  • Combs, T. P., Pajvani, U. B., Berg, A. H., Lin, Y., Jelicks, L. A., Laplante, M., Nawrocki, A. R., Rajala, M. W., Parlow, Albert. F., Cheeseboro, L., Ding, Y.-Y., Russell, R. G., Lindemann, D., Hartley, A., Baker, G. R. C., Obici, S., Deshaies, Y., Ludgate, M., Rossetti, L., Scherer, P. E. (2004). A Transgenic Mouse with a Deletion in the Collagenous Domain of Adiponectin Displays Elevated Circulating Adiponectin and Improved Insulin Sensitivity. Endocrinology 145: 367-383 [Abstract] [Full Text]  
  • Pandarpurkar, M., Wilson-Fritch, L., Corvera, S., Markholst, H., Hornum, L., Greiner, D. L., Mordes, J. P., Rossini, A. A., Bortell, R. (2003). Ian4 is required for mitochondrial integrity and T cell survival. Proc. Natl. Acad. Sci. USA 100: 10382-10387 [Abstract] [Full Text]  


Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»