Copper regulates cyclic-AMP-dependent lipolysis

Nature Chemical Biology

Volumn 12, Issue 8, 2016, Pages 586-592

  Krishnamoorthy, Lakshmi ^a   Cotruvo, Joseph A ^a   Chan, Jefferson ^a,c   Kaluarachchi, Harini ^a   Muchenditsi, Abigael ^b   Pendyala, Venkata S ^b   Jia, Shang ^a   Aron, Allegra T ^a   Ackerman, Cheri M ^a   Wal, Mark N Vander ^a   Guan, Timothy ^a   Smaga, Lukas P ^a   Farhi, Samouil L ^a   New, Elizabeth J ^a,c,d   Lutsenko, Svetlana ^b   Chang, Christopher J ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

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

^c UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^d UNIVERSITY OF SYDNEY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

COPPER; CYCLIC AMP; PHOSPHODIESTERASE 3B; PHOSPHODIESTERASE III; UNCLASSIFIED DRUG; PDE3B PROTEIN, MOUSE; PHOSPHODIESTERASE III INHIBITOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; LIPOLYSIS; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; SECOND MESSENGER; WHITE ADIPOCYTE; 3T3-L1 CELL LINE; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; DOSE RESPONSE; DRUG EFFECTS; METABOLISM; STRUCTURE ACTIVITY RELATION;

3T3-L1 CELLS; ANIMALS; COPPER; CYCLIC AMP; CYCLIC NUCLEOTIDE PHOSPHODIESTERASES, TYPE 3; DOSE-RESPONSE RELATIONSHIP, DRUG; LIPOLYSIS; MICE; MOLECULAR STRUCTURE; PHOSPHODIESTERASE 3 INHIBITORS; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84976274777     PISSN: 15524450     EISSN: 15524469     Source Type: Journal    
DOI: 10.1038/nchembio.2098     Document Type: Article

References (60)

1. Lippard, S.J. & Berg, J.M. Principles of Bioinorganic Chemistry (University Science Books, Mill Valley, California, USA, 1994).
2. Barnham, K.J., Masters, C.L. & Bush, A.I. Neurodegenerative diseases and oxidative stress. Nat. Rev. Drug Discov. 3, 205-214 (2004).
3. Rae, T.D., Schmidt, P.J., Pufahl, R.A., Culotta, V.C. & OHalloran, T.V. Undetectable intracellular free copper: The requirement of a copper chaperone for superoxide dismutase. Science 284, 805-808 (1999).
4. Robinson, N.J. & Winge, D.R. Copper metallochaperones. Annu. Rev. Biochem. 79, 537-562 (2010).
5. Banci, L. et al. Affinity gradients drive copper to cellular destinations. Nature 465, 645-648 (2010).
6. Boal, A.K. & Rosenzweig, A.C. Structural biology of copper trafficking. Chem. Rev. 109, 4760-4779 (2009).
7. Brady, D.C. et al. Copper is required for oncogenic BRAF signalling and tumorigenesis. Nature 509, 492-496 (2014).
8. Turski, M.L. et al. A novel role for copper in Ras/mitogen-Activated protein kinase signaling. Mol. Cell. Biol. 32, 1284-1295 (2012).
9. Dodani, S.C. et al. Calcium-dependent copper redistributions in neuronal cells revealed by a fluorescent copper sensor and X-ray fluorescence microscopy. Proc. Natl. Acad. Sci. USA 108, 5980-5985 (2011).
10. Dodani, S.C. et al. Copper is an endogenous modulator of neural circuit spontaneous activity. Proc. Natl. Acad. Sci. USA 111, 16280-16285 (2014).
11. Cotruvo, J.A. Jr., Aron, A.T., Ramos-Torres, K.M. & Chang, C.J. Synthetic fluorescent probes for studying copper in biological systems. Chem. Soc. Rev. 44, 4400-4414 (2015).
12. Chang, C.J. Searching for harmony in transition-metal signaling. Nat. Chem. Biol. 11, 744-747 (2015).
13. Aron, A.T., Ramos-Torres, K.M., Cotruvo, J.A. Jr. & Chang, C.J. Recognition-And reactivity-based fluorescent probes for studying transition metal signaling in living systems. Acc. Chem. Res. 48, 2434-2442 (2015).
14. Kahn, S.E., Hull, R.L. & Utzschneider, K.M. Mechanisms linking obesity to insulin resistance and type 2 diabetes. Nature 444, 840-846 (2006).
15. Khandekar, M.J., Cohen, P. & Spiegelman, B.M. Molecular mechanisms of cancer development in obesity. Nat. Rev. Cancer 11, 886-895 (2011).
16. Van Gaal, L.F., Mertens, I.L. & De Block, C.E. Mechanisms linking obesity with cardiovascular disease. Nature 444, 875-880 (2006).
17. Burkhead, J.L. & Lutsenko, S. The role of copper as a modifier of lipid metabolism. in Lipid Metabolism (ed. Baez, R.V.) (InTech 2013).
18. Engle, T.E. Copper and lipid metabolism in beef cattle: A review. J. Anim. Sci. 89, 591-596 (2011).
19. al-Othman, A.A., Rosenstein, F. & Lei, K.Y. Copper deficiency alters plasma pool size, percent composition and concentration of lipoprotein components in rats. J. Nutr. 122, 1199-1204 (1992).
20. Carr, T.P. & Lei, K.Y. High-density lipoprotein cholesteryl ester and protein catabolism in hypercholesterolemic rats induced by copper deficiency. Metabolism 39, 518-524 (1990).
21. Huster, D. et al. High copper selectively alters lipid metabolism and cell cycle machinery in the mouse model of Wilson disease. J. Biol. Chem. 282, 8343-8355 (2007).
22. Huster, D. & Lutsenko, S. Wilson disease: not just a copper disorder. Analysis of a Wilson disease model demonstrates the link between copper and lipid metabolism. Mol. Biosyst. 3, 816-824 (2007).
23. Seessle, J. et al. Alterations of lipid metabolism in Wilson disease. Lipids Health Dis. 10, 83 (2011).
24. Huster, D. et al. Consequences of copper accumulation in the livers of the Atp7b-/-(Wilson disease gene) knockout mice. Am. J. Pathol. 168, 423-434 (2006).
25. Lutsenko, S. Atp7b-/-mice as a model for studies of Wilsons disease. Biochem. Soc. Trans. 36, 1233-1238 (2008).
26. Buiakova, O.I. et al. Null mutation of the murine ATP7B (Wilson disease) gene results in intracellular copper accumulation and late-onset hepatic nodular transformation. Hum. Mol. Genet. 8, 1665-1671 (1999).
27. Gerbasi, V., Lutsenko, S. & Lewis, E.J. A mutation in the ATP7B copper transporter causes reduced dopamine beta-hydroxylase and norepinephrine in mouse adrenal. Neurochem. Res. 28, 867-873 (2003).
28. Aigner, E. et al. A role for low hepatic copper concentrations in nonalcoholic fatty liver disease. Am. J. Gastroenterol. 105, 1978-1985 (2010).
29. Kawamura, M. et al. Hormone-sensitive lipase in differentiated 3T3-L1 cells and its activation by cyclic AMP-dependent protein kinase. Proc. Natl. Acad. Sci. USA 78, 732-736 (1981).
30. Kim, B.E. et al. Cardiac copper deficiency activates a systemic signaling mechanism that communicates with the copper acquisition and storage organs. Cell Metab. 11, 353-363 (2010).
31. Duncan, R.E., Ahmadian, M., Jaworski, K., Sarkadi-Nagy, E. & Sul, H.S. Regulation of lipolysis in adipocytes. Annu. Rev. Nutr. 27, 79-101 (2007).
32. Chijiwa, T. et al. Inhibition of forskolin-induced neurite outgrowth and protein phosphorylation by a newly synthesized selective inhibitor of cyclic AMP-dependent protein kinase, N-[2-(p-bromocinnamylamino)ethyl]-5-isoquinolinesulfonamide (H-89), of PC12D pheochromocytoma cells. J. Biol. Chem. 265, 5267-5272 (1990).
33. Greenberg, A.S. et al. Stimulation of lipolysis and hormone-sensitive lipase via the extracellular signal-regulated kinase pathway. J. Biol. Chem. 276, 45456-45461 (2001).
34. Xue, B., Greenberg, A.G., Kraemer, F.B. & Zemel, M.B. Mechanism of intracellular calcium ([Ca2+]i) inhibition of lipolysis in human adipocytes. FASEB J. 15, 2527-2529 (2001).
35. Zhou, L. et al. Berberine attenuates cAMP-induced lipolysis via reducing the inhibition of phosphodiesterase in 3T3-L1 adipocytes. Biochim. Biophys. Acta 1812, 527-535 (2011).
36. Zhou, D. et al. CD36 level and trafficking are determinants of lipolysis in adipocytes. FASEB J. 26, 4733-4742 (2012).
37. Snyder, P.B., Esselstyn, J.M., Loughney, K., Wolda, S.L. & Florio, V.A. The role of cyclic nucleotide phosphodiesterases in the regulation of adipocyte lipolysis. J. Lipid Res. 46, 494-503 (2005).
38. Ahmad, F. et al. Insulin-induced formation of macromolecular complexes involved in activation of cyclic nucleotide phosphodiesterase 3B (PDE3B) and its interaction with PKB. Biochem. J. 404, 257-268 (2007).
39. Varnerin, J.P. et al. Expression, refolding, and purification of recombinant human phosphodiesterase 3B: definition of the N-Terminus of the catalytic core. Protein Expr. Purif. 35, 225-236 (2004).
40. McMillin, D.R. The origin of the intense absorption in azurin. Bioinorg. Chem. 8, 179-184 (1978).
41. Pountney, D.L., Schauwecker, I., Zarn, J. & Vasák, M. Formation of mammalian Cu8-metallothionein in vitro: evidence for the existence of two Cu(I)4-Thiolate clusters. Biochemistry 33, 9699-9705 (1994).
42. Angeletti, B. et al. BACE1 cytoplasmic domain interacts with the copper chaperone for superoxide dismutase-1 and binds copper. J. Biol. Chem. 280, 17930-17937 (2005).
43. Omburo, G.A., Brickus, T., Ghazaleh, F.A. & Colman, R.W. Divalent metal cation requirement and possible classification of cGMP-inhibited phosphodiesterase as a metallohydrolase. Arch. Biochem. Biophys. 323, 1-5 (1995).
44. Scapin, G. et al. Crystal structure of human phosphodiesterase 3B: Atomic basis for substrate and inhibitor specificity. Biochemistry 43, 6091-6100 (2004).
45. Degerman, E., Belfrage, P. & Manganiello, V.C. Structure, localization, and regulation of cGMP-inhibited phosphodiesterase (PDE3). J. Biol. Chem. 272, 6823-6826 (1997).
46. Hung, S.H. et al. New insights from the structure-function analysis of the catalytic region of human platelet phosphodiesterase 3A: A role for the unique 44-Amino acid insert. J. Biol. Chem. 281, 29236-29244 (2006).
47. Tang, K.M., Jang, E.K. & Haslam, R.J. Expression and mutagenesis of the catalytic domain of cGMP-inhibited phosphodiesterase (PDE3) cloned from human platelets. Biochem. J. 323, 217-224 (1997).
48. Ovadia, H. et al. Increased adipocyte S-nitrosylation targets anti-lipolytic action of insulin: relevance to adipose tissue dysfunction in obesity. J. Biol. Chem. 286, 30433-30443 (2011).
49. Maurice, D.H. et al. Advances in targeting cyclic nucleotide phosphodiesterases. Nat. Rev. Drug Discov. 13, 290-314 (2014).
50. Chung, Y.W. et al. Targeted disruption of PDE3B, but not PDE3A, protects murine heart from ischemia/reperfusion injury. Proc. Natl. Acad. Sci. USA 112, E2253-E2262 (2015).
51. Gray, N.E. et al. Angiopoietin-like 4 (Angptl4) protein is a physiological mediator of intracellular lipolysis in murine adipocytes. J. Biol. Chem. 287, 8444-8456 (2012).
52. Stephens, J.M., Lee, J. & Pilch, P.F. Tumor necrosis factor-Alpha-induced insulin resistance in 3T3-L1 adipocytes is accompanied by a loss of insulin receptor substrate-1 and GLUT4 expression without a loss of insulin receptor-mediated signal transduction. J. Biol. Chem. 272, 971-976 (1997).
53. Hong-Hermesdorf, A. et al. Subcellular metal imaging identifies dynamic sites of Cu accumulation in Chlamydomonas. Nat. Chem. Biol. 10, 1034-1042 (2014).
54. Kenan, Y., Murata, T., Shakur, Y., Degerman, E. & Manganiello, V.C. Functions of the N-Terminal region of cyclic nucleotide phosphodiesterase 3 (PDE 3) isoforms. J. Biol. Chem. 275, 12331-12338 (2000).
55. Cotruvo, J.A. Jr. & Stubbe, J. NrdI, a flavodoxin involved in maintenance of the diferric-Tyrosyl radical cofactor in Escherichia coli class Ib ribonucleotide reductase. Proc. Natl. Acad. Sci. USA 105, 14383-14388 (2008).
56. Leonard, W.R., Romine, J.L. & Meyers, A.I. A rapid and efficient synthesis of chiral 2-hydro-2-oxazolines. J. Org. Chem. 56, 1961-1963 (1991).
57. Gibson, D.G. et al. Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat. Methods 6, 343-345 (2009).
58. Cobine, P.A. et al. Stoichiometry of complex formation between copper(I) and the N-Terminal domain of the Menkes protein. Biochemistry 39, 6857-6863 (2000).
59. Xiao, Z. et al. Unification of the copper(I) binding affinities of the metallo-chaperones Atx1, Atox1, and related proteins: detection probes and affinity standards. J. Biol. Chem. 286, 11047-11055 (2011).
60. Dworkin, M. & Keller, K.H. Solubility and diffusion coefficient of adenosine 3′:5′-monophosphate. J. Biol. Chem. 252, 864-865 (1977).