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J. Biol. Chem., Vol. 278, Issue 11, 9073-9085, March 14, 2003
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From the Departments of Acrp30/adiponectin is an
adipocyte-specific secretory protein that has recently been implicated
as a mediator of systemic insulin sensitivity with liver and muscle as
target organs. Acrp30 is found as two forms in serum, as a lower
molecular weight trimer-dimer and a high molecular weight
complex. Little is know about the regulation and significance of these
Acrp30 complexes in serum and about the events that lead to the
generation of the bioactive ligand. Here, we show that there is a
profound sexual dimorphism of Acrp30 levels and complex distribution in
serum. Female mice display significantly higher levels of the high
molecular weight complex in serum than males. In both females and
males, levels of the high molecular weight complex are significantly
reduced in response to a systemic increase of insulin. The ratio of the two complexes is restored upon normalization of glucose levels. Structurally, we show that oligomer formation of Acrp30 critically depends on disulfide bond formation mediated by Cys-39. Mutation of
Cys-39 results in trimers that are subject to proteolytic cleavage in
the collagenous domain. Surprisingly, Acrp30(C39S) or wild-type Acrp30 treated with dithiothreitol are significantly more bioactive than the higher order oligomeric forms of the protein with respect to
reduction of serum glucose levels. Furthermore, treatment of primary
hepatocytes with trimeric and higher order forms of Acrp30 confirms
that the increased bioactivity seen in vivo is reflected in
an augmented potency to reduce glucose output in the presence of
gluconeogenic stimuli. Combined, these results shed new light on the
regulation of this complex protein and suggest a new model for in
vivo activation of the protein, implicating a serum reductase activity.
Structure-Function Studies of the Adipocyte-secreted Hormone
Acrp30/Adiponectin
IMPLICATIONS FOR METABOLIC REGULATION AND BIOACTIVITY*
,,,,
, and**
Cell Biology and
§ Medicine and Pathology and Diabetes Research and
Training Center, Albert Einstein College of Medicine, Bronx,
New York 10461 and ¶ Department of Biophysical Chemistry,
Biozentrum, University of Basel, Klingelbergstrasse 70, CH-4056 Basel,
Switzerland
*
This work was supported in part by National Institutes of
Health Medical Scientist Training Grant T32-GM07288 (to U. B. P. and
M. W. R.), National Institutes of Health National Research Service
Award DK61228 (to T. P. C.), an American Diabetes Medical Scientist
Training grant (to A. H. B.), and National Institutes of Health Grant
1R01-DK55758 (to P. E. S.).The costs of publication of this
article were defrayed in part by the
payment of page charges. The article
must therefore be hereby marked
"advertisement" in accordance with 18 U.S.C. Section
1734 solely to indicate this fact.
Copyright © 2003 by The American Society for Biochemistry and Molecular Biology, Inc.
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 M. Neumeier, J. Weigert, A. Schaffler, G. Wehrwein, U. Muller-Ladner, J. Scholmerich, C. Wrede, and C. Buechler Different effects of adiponectin isoforms in human monocytic cells J. Leukoc. Biol., April 1, 2006; 79(4): 803 - 808. [Abstract] [Full Text] [PDF]
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N. Pannacciulli, J. C. Bunt, E. Ortega, T. Funahashi, A. D. Salbe, C. Bogardus, and J. Krakoff Lower Total Fasting Plasma Adiponectin Concentrations Are Associated with Higher Metabolic Rates J. Clin. Endocrinol. Metab., April 1, 2006; 91(4): 1600 - 1603. [Abstract] [Full Text] [PDF]
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L. Xie, D. Boyle, D. Sanford, P. E. Scherer, J. E. Pessin, and S. Mora Intracellular Trafficking and Secretion of Adiponectin Is Dependent on GGA-coated Vesicles J. Biol. Chem., March 17, 2006; 281(11): 7253 - 7259. [Abstract] [Full Text] [PDF]
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 G. W. Stone, S. Barzee, V. Snarsky, K. Kee, C. A. Spina, X.-F. Yu, and R. S. Kornbluth Multimeric Soluble CD40 Ligand and GITR Ligand as Adjuvants for Human Immunodeficiency Virus DNA Vaccines J. Virol., February 15, 2006; 80(4): 1762 - 1772. [Abstract] [Full Text] [PDF]
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 A. M. Kanaya, C. Wassel Fyr, E. Vittinghoff, T. B. Harris, S. W. Park, B. H. Goodpaster, F. Tylavsky, and S. R. Cummings Adipocytokines and incident diabetes mellitus in older adults: the independent effect of plasminogen activator inhibitor 1. Arch Intern Med, February 13, 2006; 166(3): 350 - 356. [Abstract] [Full Text] [PDF]
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A. R. Nawrocki, M. W. Rajala, E. Tomas, U. B. Pajvani, A. K. Saha, M. E. Trumbauer, Z. Pang, A. S. Chen, N. B. Ruderman, H. Chen, et al. Mice Lacking Adiponectin Show Decreased Hepatic Insulin Sensitivity and Reduced Responsiveness to Peroxisome Proliferator-activated Receptor {gamma} Agonists J. Biol. Chem., February 3, 2006; 281(5): 2654 - 2660. [Abstract] [Full Text] [PDF]
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C. G. Schalkwijk, N. Chaturvedi, M. T. Schram, J. H. Fuller, C. D. A. Stehouwer, and the EURODIAB Prospective Complications Study Group Adiponectin Is Inversely Associated with Renal Function in Type 1 Diabetic Patients J. Clin. Endocrinol. Metab., January 1, 2006; 91(1): 129 - 135. [Abstract] [Full Text] [PDF]
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J. Spranger, S. Verma, I. Gohring, T. Bobbert, J. Seifert, A. L. Sindler, A. Pfeiffer, S. M. Hileman, M. Tschop, and W. A. Banks Adiponectin Does Not Cross the Blood-Brain Barrier but Modifies Cytokine Expression of Brain Endothelial Cells Diabetes, January 1, 2006; 55(1): 141 - 147. [Abstract] [Full Text] [PDF]
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C. Lara-Castro, N. Luo, P. Wallace, R. L. Klein, and W. T. Garvey Adiponectin Multimeric Complexes and the Metabolic Syndrome Trait Cluster Diabetes, January 1, 2006; 55(1): 249 - 259. [Abstract] [Full Text] [PDF]
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 F. Abbasi, S.-A. Chang, J. W. Chu, T. P. Ciaraldi, C. Lamendola, T. McLaughlin, G. M. Reaven, and P. D. Reaven Improvements in insulin resistance with weight loss, in contrast to rosiglitazone, are not associated with changes in plasma adiponectin or adiponectin multimeric complexes Am J Physiol Regulatory Integrative Comp Physiol, January 1, 2006; 290(1): R139 - R144. [Abstract] [Full Text] [PDF]
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N. Rasouli, A. Yao-Borengasser, L. M. Miles, S. C. Elbein, and P. A. Kern Increased plasma adiponectin in response to pioglitazone does not result from increased gene expression Am J Physiol Endocrinol Metab, January 1, 2006; 290(1): E42 - E46. [Abstract] [Full Text] [PDF]
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 X Fang, R Palanivel, X Zhou, Y Liu, A Xu, Y Wang, and G Sweeney Hyperglycemia- and hyperinsulinemia-induced alteration of adiponectin receptor expression and adiponectin effects in L6 myoblasts J. Mol. Endocrinol., December 1, 2005; 35(3): 465 - 476. [Abstract] [Full Text] [PDF]
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J. J. Wilkes, M. T. A. Nguyen, G. K. Bandyopadhyay, E. Nelson, and J. M. Olefsky Topiramate treatment causes skeletal muscle insulin sensitization and increased Acrp30 secretion in high-fat-fed male Wistar rats Am J Physiol Endocrinol Metab, December 1, 2005; 289(6): E1015 - E1022. [Abstract] [Full Text] [PDF]
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 E. K. Wei, E. Giovannucci, C. S. Fuchs, W. C. Willett, and C. S. Mantzoros Low Plasma Adiponectin Levels and Risk of Colorectal Cancer in Men: A Prospective Study J Natl Cancer Inst, November 16, 2005; 97(22): 1688 - 1694. [Abstract] [Full Text] [PDF]
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 S. Stanley, K. Wynne, B. McGowan, and S. Bloom Hormonal Regulation of Food Intake Physiol Rev, October 1, 2005; 85(4): 1131 - 1158. [Abstract] [Full Text] [PDF]
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C. Graveleau, V. G. Zaha, A. Mohajer, R. R. Banerjee, N. Dudley-Rucker, C. M. Steppan, M. W. Rajala, P. E. Scherer, R. S. Ahima, M. A. Lazar, et al. Mouse and Human Resistins Impair Glucose Transport in Primary Mouse Cardiomyocytes, and Oligomerization Is Required for This Biological Action J. Biol. Chem., September 9, 2005; 280(36): 31679 - 31685. [Abstract] [Full Text] [PDF]
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P. W Peake, A. D Kriketos, L. V Campbell, Y. Shen, and J. A Charlesworth The metabolism of isoforms of human adiponectin: studies in human subjects and in experimental animals Eur. J. Endocrinol., September 1, 2005; 153(3): 409 - 417. [Abstract] [Full Text] [PDF]
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N. C. Bush, B. E. Darnell, R. A. Oster, M. I. Goran, and B. A. Gower Adiponectin Is Lower Among African Americans and Is Independently Related to Insulin Sensitivity in Children and Adolescents Diabetes, September 1, 2005; 54(9): 2772 - 2778. [Abstract] [Full Text] [PDF]
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 J. R. Berggren, M. W. Hulver, and J. A. Houmard Fat as an endocrine organ: influence of exercise J Appl Physiol, August 1, 2005; 99(2): 757 - 764. [Abstract] [Full Text] [PDF]
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J. E. Caminos, R. Nogueiras, R. Gallego, S. Bravo, S. Tovar, T. Garcia-Caballero, F. F. Casanueva, and C. Dieguez Expression and Regulation of Adiponectin and Receptor in Human and Rat Placenta J. Clin. Endocrinol. Metab., July 1, 2005; 90(7): 4276 - 4286. [Abstract] [Full Text] [PDF]
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E. Bugianesi, U. Pagotto, R. Manini, E. Vanni, A. Gastaldelli, R. de Iasio, E. Gentilcore, S. Natale, M. Cassader, M. Rizzetto, et al. Plasma Adiponectin in Nonalcoholic Fatty Liver Is Related to Hepatic Insulin Resistance and Hepatic Fat Content, Not to Liver Disease Severity J. Clin. Endocrinol. Metab., June 1, 2005; 90(6): 3498 - 3504. [Abstract] [Full Text] [PDF]
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Y.-H. Yu and H. N. Ginsberg Adipocyte Signaling and Lipid Homeostasis: Sequelae of Insulin-Resistant Adipose Tissue Circ. Res., May 27, 2005; 96(10): 1042 - 1052. [Abstract] [Full Text] [PDF]
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A. H. Berg and P. E. Scherer Adipose Tissue, Inflammation, and Cardiovascular Disease Circ. Res., May 13, 2005; 96(9): 939 - 949. [Abstract] [Full Text] [PDF]
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A. Xu, K. W. Chan, R. L. C. Hoo, Y. Wang, K. C. B. Tan, J. Zhang, B. Chen, M. C. Lam, C. Tse, G. J. S. Cooper, et al. Testosterone Selectively Reduces the High Molecular Weight Form of Adiponectin by Inhibiting Its Secretion from Adipocytes J. Biol. Chem., May 6, 2005; 280(18): 18073 - 18080. [Abstract] [Full Text] [PDF]
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Y. Wang, K. S. L. Lam, J. Y. Xu, G. Lu, L. Y. Xu, G. J. S. Cooper, and A. Xu Adiponectin Inhibits Cell Proliferation by Interacting with Several Growth Factors in an Oligomerization-dependent Manner J. Biol. Chem., May 6, 2005; 280(18): 18341 - 18347. [Abstract] [Full Text] [PDF]
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T. Kadowaki and T. Yamauchi Adiponectin and Adiponectin Receptors Endocr. Rev., May 1, 2005; 26(3): 439 - 451. [Abstract] [Full Text] [PDF]
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H. Satoh, M.T. A. Nguyen, M. Trujillo, T. Imamura, I. Usui, P. E. Scherer, and J. M. Olefsky Adenovirus-Mediated Adiponectin Expression Augments Skeletal Muscle Insulin Sensitivity in Male Wistar Rats Diabetes, May 1, 2005; 54(5): 1304 - 1313. [Abstract] [Full Text] [PDF]
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 A M Diehl, Z P Li, H Z Lin, and S Q Yang Cytokines and the pathogenesis of non-alcoholic steatohepatitis Gut, February 1, 2005; 54(2): 303 - 306. [Full Text] [PDF]
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