Endopeptidase cleavage generates a functionally distinct isoform of C1q/tumor necrosis factor-related protein-12 (CTRP12) with an altered oligomeric state and signaling specificity

Journal of Biological Chemistry

Volumn 287, Issue 43, 2012, Pages 35804-35814

  Wei, Zhikui ^a   Lei, Xia ^a   Seldin, Marcus M ^a   Wong, G William ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3T3-L1 ADIPOCYTES; ADIPOCYTES; ADIPOKINES; ADIPOSE TISSUE; BIOCHEMICAL PROPERTIES; CONSERVED RESIDUES; CONTEXT DEPENDENT; FULL-LENGTH PROTEINS; GLUCOSE METABOLISM; GLYCOSYLATED; HEPATOCYTES; INSULIN-STIMULATED GLUCOSE; ISOFORMS; NATURALLY OCCURRING; OLIGOMERIC STATE; OLIGOMERIC STRUCTURE; P38 MAPK; POST-TRANSLATIONAL MODIFICATIONS;

DIMERS; GLUCOSE; INSULIN; METABOLISM; PROTEINS; TISSUE;

SIGNALING;

ALANINE; ASPARAGINE; COMPLEMENT COMPONENT C1Q; CYSTEINE; FURIN; INSULIN; ISOPROTEIN; LYSINE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN KINASE B; PROTEINASE;

ADIPOCYTE; AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; CELL LINE; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVATION; GLUCOSE TRANSPORT; HORMONE RELEASE; LIVER CELL; MOUSE; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN GLYCOSYLATION; PROTEIN PROCESSING; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION;

3T3-L1 CELLS; ADIPOCYTES; ADIPOKINES; AMINO ACID SUBSTITUTION; ANIMALS; CHICKENS; FURIN; GLUCOSE; HEPATOCYTES; HUMANS; INSULIN; MAP KINASE SIGNALING SYSTEM; MICE; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; MUTATION, MISSENSE; PROTEIN ISOFORMS; PROTEIN MULTIMERIZATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOLYSIS; XENOPUS; ZEBRAFISH;

EID: 84867837394     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.365965     Document Type: Article

References (28)

1. Deng, Y., and Scherer, P. E. (2010) Adipokines as novel biomarkers and regulators of the metabolic syndrome. Ann. N.Y. Acad. Sci. 1212, E1-19
2. Scherer, P. E. (2006) Adipose tissue: from lipid storage compartment to endocrine organ. Diabetes 55, 1537-1545
3. Wong, G. W., Wang, J., Hug, C., Tsao, T. S., and Lodish, H. F. (2004) A family of Acrp30/adiponectin structural and functional paralogs. Proc. Natl. Acad. Sci. U.S.A. 101, 10302-10307 (Pubitemid 38924920)
4. Wong, G. W., Krawczyk, S. A., Kitidis-Mitrokostas, C., Ge, G., Spooner, E., Hug, C., Gimeno, R., and Lodish, H. F. (2009) Identification and characterization of CTRP9, a novel secreted glycoprotein, from adipose tissue that reduces serum glucose in mice and forms heterotrimers with adiponectin. FASEB J. 23, 241-258
5. Wong, G. W., Krawczyk, S. A., Kitidis-Mitrokostas, C., Revett, T., Gimeno, R., and Lodish, H. F. (2008) Molecular, biochemical and functional characterizations of C1q/TNF family members: adipose-tissue-selective expression patterns, regulation by PPAR-γ agonist, cysteine-mediated oligomerizations, combinatorial associations, and metabolic functions. Biochem. J. 416, 161-177
6. Wei, Z., Peterson, J. M., and Wong, G. W. (2011) Metabolic regulation by C1q/TNF-related protein-13 (CTRP13): activation of AMP-activated protein kinase and suppression of fatty acid-induced JNK signaling. J. Biol. Chem. 286, 15652-15665
7. Seldin, M. M., Peterson, J. M., Byerly, M. S., Wei, Z., and Wong, G. W. (2012) Myonectin (CTRP15), a novel myokine that links skeletal muscle to systemic lipid homeostasis. J. Biol. Chem. 287, 11968-11980
8. Kishore, U., Gaboriaud, C., Waters, P., Shrive, A. K., Greenhough, T. J., Reid, K. B., Sim, R. B., and Arlaud, G. J. (2004) C1q and tumor necrosis factor superfamily: modularity and versatility. Trends Immunol. 25, 551-561 (Pubitemid 39208354)
9. Peterson, J. M., Wei, Z., and Wong, G. W. (2010) C1q/TNF-related protein-3 (CTRP3), a novel adipokine that regulates hepatic glucose output. J. Biol. Chem. 285, 39691-39701
10. Wei, Z., Peterson, J. M., Lei, X., Cebotaru, L., Wolfgang, M. J., Baldeviano, G. C., and Wong, G. W. (2012) C1q/TNF-related protein-12 (CTRP12), a novel adipokine that improves insulin sensitivity and glycemic control in mouse models of obesity and diabetes. J. Biol. Chem. 287, 10301-10315
11. Peterson, J. M., Aja, S., Wei, Z., and Wong, G. W. (2012) CTRP1 protein enhances fatty acid oxidation via AMP-activated protein kinase (AMPK) activation and acetyl-CoA carboxylase (ACC) inhibition. J. Biol. Chem. 287, 1576-1587
12. Kopp, A., Bala, M., Buechler, C., Falk, W., Gross, P., Neumeier, M., Schölmerich, J., and Schäffler, A. (2010) C1q/TNF-related protein-3 represents a novel and endogenous lipopolysaccharide antagonist of the adipose tissue. Endocrinology 151, 5267-5278
13. Kopp, A., Bala, M., Weigert, J., Büchler, C., Neumeier, M., Aslanidis, C., Schölmerich, J., and Schäffler, A. (2010) Effects of the new adiponectin paralogous protein CTRP-3 and of LPS on cytokine release from monocytes of patients with type 2 diabetes mellitus. Cytokine 49, 51-57
14. Maeda, T., Abe, M., Kurisu, K., Jikko, A., and Furukawa, S. (2001) Molecular cloning and characterization of a novel gene, CORS26, encoding a putative secretory protein and its possible involvement in skeletal development. J. Biol. Chem. 276, 3628-3634
15. Maeda, T., Jikko, A., Abe, M., Yokohama-Tamaki, T., Akiyama, H., Furukawa, S., Takigawa, M., and Wakisaka, S. (2006) Cartducin, a paralog of Acrp30/adiponectin, is induced during chondrogenic differentiation and promotes proliferation of chondrogenic precursors and chondrocytes. J. Cell. Physiol. 206, 537-544 (Pubitemid 43062825)
16. Lasser, G., Guchhait, P., Ellsworth, J. L., Sheppard, P., Lewis, K., Bishop, P., Cruz, M. A., Lopez, J. A., and Fruebis, J. (2006) C1qTNF-related protein-1 (CTRP-1): a vascular wall protein that inhibits collagen-induced platelet aggregation by blocking VWF binding to collagen. Blood 107, 423-430 (Pubitemid 43076360)
17. Zheng, Q., Yuan, Y., Yi, W., Lau, W. B., Wang, Y., Wang, X., Sun, Y., Lopez, B. L., Christopher, T. A., Peterson, J. M., Wong, G. W., Yu, S., Yi, D., and Ma, X. L. (2011) C1q/TNF-related proteins, a family of novel adipokines, induce vascular relaxation through the adiponectin receptor-1/AMPK/eNOS/nitric oxide signaling pathway. Arterioscler. Thromb. Vasc. Biol. 31, 2616-2623
18. Hayward, C., Shu, X., Cideciyan, A. V., Lennon, A., Barran, P., Zareparsi, S., Sawyer, L., Hendry, G., Dhillon, B., Milam, A. H., Luthert, P. J., Swaroop, A., Hastie, N. D., Jacobson, S. G., and Wright, A. F. (2003) Mutation in a short-chain collagen gene, CTRP5, results in extracellular deposit formation in late-onset retinal degeneration: a genetic model for agerelated macular degeneration. Hum. Mol. Genet. 12, 2657-2667 (Pubitemid 37304688)
19. Ayyagari, R., Mandal, M. N., Karoukis, A. J., Chen, L., McLaren, N. C., Lichter, M., Wong, D. T., Hitchcock, P. F., Caruso, R. C., Moroi, S. E., Maumenee, I. H., and Sieving, P. A. (2005) Late-onset macular degeneration and long anterior lens zonules result from a CTRP5 gene mutation. Invest. Ophthalmol. Vis. Sci. 46, 3363-3371 (Pubitemid 44264327)
20. Chavali, V. R., Khan, N. W., Cukras, C. A., Bartsch, D. U., Jablonski, M. M., and Ayyagari, R. (2011) A CTRP5 gene S163R mutation knock-in mouse model for late-onset retinal degeneration. Hum. Mol. Genet. 20, 2000-2014
21. Yan, A., and Lennarz, W. J. (2005) Unraveling the mechanism of protein N-glycosylation. J. Biol. Chem. 280, 3121-3124 (Pubitemid 40223771)
22. Basak, S., Chrétien, M., Mbikay, M., and Basak, A. (2004) In vitro elucidation of substrate specificity and bioassay of proprotein convertase 4 using intramolecularly quenched fluorogenic peptides. Biochem. J. 380, 505-514 (Pubitemid 38788123)
23. Seidah, N. G. (2011) The proprotein convertases, 20 years later. Methods Mol. Biol. 768, 23-57
24. Enomoto, T., Ohashi, K., Shibata, R., Higuchi, A., Maruyama, S., Izumiya, Y., Walsh, K., Murohara, T., and Ouchi, N. (2011) Adipolin/C1qdc2/CTRP12 protein functions as an adipokine that improves glucose metabolism. J. Biol. Chem. 286, 34552-34558
25. Jaeken, J., and Matthijs, G. (2007) Congenital disorders of glycosylation: a rapidly expanding disease family. Annu. Rev. Genomics Hum. Genet. 8, 261-278
26. Tsao, T. S., Murrey, H. E., Hug, C., Lee, D. H., and Lodish, H. F. (2002) Oligomerization state-dependent activation of NF-κB signaling pathway by adipocyte complement-related protein of 30 kDa (Acrp30). J. Biol. Chem. 277, 29359-29362 (Pubitemid 41079218)
27. Tsao, T. S., Tomas, E., Murrey, H. E., Hug, C., Lee, D. H., Ruderman, N. B., Heuser, J. E., and Lodish, H. F. (2003) Role of disulfide bonds in Acrp30/ adiponectin structure and signaling specificity: different oligomers activate different signal transduction pathways. J. Biol. Chem. 278, 50810-50817 (Pubitemid 37548930)
28. Briggs, D. B., Giron, R. M., Malinowski, P. R., Nuñez, M., and Tsao, T. S. (2011) Role of redox environment on the oligomerization of higher molecular weight adiponectin. BMC Biochem. 12, 24