Mitochondrial F0F1-ATP synthase is a molecular target of 3-iodothyronamine, an endogenous metabolite of thyroid hormone

British Journal of Pharmacology

Volumn 166, Issue 8, 2012, Pages 2331-2347

  Cumero, S ^a   Fogolari, F ^a   Domenis, R ^a   Zucchi, R ^c   Mavelli, I ^a,b   Contessi, S ^a  

^a UNIVERSITY OF UDINE   (Italy)

^b NATIONAL INSTITUTE OF BIOSTRUCTURES AND BIOSYSTEMS   (Italy)

^c UNIVERSITY OF PISA   (Italy)

Author keywords

3 iodothyronamine (T1AM); aurovertin B; F 1 ATPase; F0F1 ATP synthase; IF1; molecular docking analysis; multiple inhibition kinetics; resveratrol

Indexed keywords

3 IODOTHYRONAMINE; ADENOSINE DIPHOSPHATE; AUROVERTIN; IF1 PROTEIN; INHIBITOR PROTEIN; MITOCHONDRIAL ENZYME; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; THYROID HORMONE DERIVATIVE; UNCLASSIFIED DRUG;

ANALYSIS; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; BINDING SITE; BIOENERGY; CONCENTRATION RESPONSE; CONTROLLED STUDY; COW; DRUG TARGETING; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME KINETICS; HEART MUSCLE CELL; IN VITRO STUDY; METABOLITE; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; MOLECULAR DOCKING; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN SECRETION; RESPIROMETRIC ANALYSIS;

ANIMALS; BINDING SITES; BLOTTING, WESTERN; CATTLE; KINETICS; MITOCHONDRIA, HEART; MODELS, MOLECULAR; MOLECULAR STRUCTURE; OXYGEN CONSUMPTION; PROTON-TRANSLOCATING ATPASES; SIGNAL TRANSDUCTION; STILBENES; THYRONINES;

EID: 84864470600     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/j.1476-5381.2012.01958.x     Document Type: Article

References (86)

1. 1-ATPase from bovine heart mitochondria. Nature 370: 621-628.
2. th Edition. Br J Pharmacol 164 (Suppl. 1): S1-S324.
3. Bason JV, Runswick MJ, Fearnley IM, Walker JE, (2011). Binding of the inhibitor protein IF(1) to bovine F(1)-ATPase. J Mol Biol 406: 443-453.
4. Bertina RM, Schrier PI, Slater EC, (1973). The binding of aurovertin to mitochondria, and its effect on mitochondrial respiration. Biochim Biophys Acta 305: 503-518.
5. Boyer PD, (1997). The ATP synthase-a splendid molecular machine. Annu Rev Biochem 66: 717-749. (Pubitemid 27274672)
6. Braulke LJ, Klingenspor M, DeBarber A, Tobias SC, Grandy DK, Scanlan TS, et al,. (2008). 3-Iodothyronamine: a novel hormone controlling the balance between glucose and lipid utilisation. J Comp Physiol B 178: 167-177. (Pubitemid 351164900)
7. 1-ATPase by cationic dyes and amphipathic peptides. Biochim Biophys Acta 975: 377-383. (Pubitemid 19196353)
8. 1. Nat Struct Biol 10: 44-750.
9. 1. Cell Metab 8: 13-25. (Pubitemid 351859227)
10. 1, the endogenous regulator of the F(1)F(o)-ATP synthase, defines mitochondrial volume fraction in HeLa cells by regulating autophagy. Biochim Biophys Acta 1787: 393-401.
11. Capaldi RA, Aggeler R, (2002). Mechanism of the F(1)F(0)-type ATP synthase, a biological rotary motor. Trends Biochem Sci 27: 154-160. (Pubitemid 34219326)
12. 1 ATPase: metabolic and immunological functions (review). Curr Opin Lipidol 17: 279-284. (Pubitemid 43786062)
13. Chiellini G, Frascarelli S, Ghelardoni S, Carnicelli V, Tobias SC, DeBarber A, et al,. (2007). Cardiac effects of 3-iodothyronamine: a new aminergic system modulating cardiac function. FASEB J 21: 1597-1608. (Pubitemid 46684861)
14. Cole ST, Alzari PM, (2005). Microbiology. TB-a new target, a new drug. Science 307: 223-227.
15. 1 ATP synthase by diazoxide in cardiac myoblasts: a dual effect of the drug. Am J Physiol Heart Circ Physiol 292: H820-H829.
16. Comelli M, Domenis R, Bisetto E, Contin M, Marchini M, Ortolani F, et al,. (2011). Cardiac differentiation promotes mitochondria development and ameliorates oxidative capacity in H9c2 cardiomyoblasts. Mitochondrion 11: 315-326.
17. 1ATP synthase. Biochem Pharmacol 67: 1843-1851. (Pubitemid 38591373)
18. 1ATP synthase and calmodulin. J Bioenerg Biomembr 39: 291-300. (Pubitemid 350029429)
19. Cross RL, Kohlbrenner WE, (1978). The mode of inhibition of oxidative phosphorylation by efrapeptin (A23871). Evidence for an alternating site mechanism for ATP synthesis. J Biol Chem 253: 4865-4873. (Pubitemid 8382150)
20. Das AM, Harris DA, (1990). Regulation of the mitochondrial ATP synthase in intact rat cardiomyocytes. Biochem J 266: 355-361. (Pubitemid 20090132)
21. 1 in goat heart. Biochim Biophys Acta 1659: 52-62. (Pubitemid 39423607)
22. Dickson VK, Silvester JA, Fearnley IM, Leslie AG, Walker JE, (2006). On the structure of the stator of the mitochondrial ATP synthase. EMBO J 25: 2911-2918. (Pubitemid 43980397)
23. Ferguson SJ, Harris DA, Radda OK, (1977). The adenosine triphosphataseinhibitor content of bovine heart submitochondrial particles. Influence of the inhibitor on adenosine triphosphate-dependent reactions. Biochem J 162: 351-357. (Pubitemid 8024020)
24. Frascarelli S, Ghelardoni S, Chiellini G, Galli E, Ronca F, Scanlan TS, et al,. (2011). Cardioprotective effect of 3-iodothyronamine in perfused rat heart subjected to ischemia and reperfusion. Cardiovasc Drugs Ther 25: 307-313.
25. Galli E, Marchini M, Saba A, Berti S, Tonacchera M, Vitti P, et al,. (2012). Detection of 3-Iodothyronamine in human patients: a preliminary study. J Clin Endocrinol Metab 97: E69-E74.
26. 0-ATP synthase. Biochemistry 45: 12695-12703. (Pubitemid 44630855)
27. Gatza E, Wahl DR, Opipari AW, Sundberg TB, Reddy P, Liu C, et al,. (2011). Manipulating the bioenergetics of alloreactive T cells causes their selective apoptosis and arrests graft-versus-host disease. Sci Transl Med 3: 67ra8.
28. Ghelardoni S, Suffredini S, Frascarelli S, Brogioni S, Chiellini G, Ronca-Testoni S, et al,. (2009). Modulation of cardiac ionic homeostasis by 3-iodothyronamine. J Cell Mol Med 13: 3082-3090.
29. 1-ATPase at 2.4A°resolution. Nat Struct Biol 7: 1055-1061.
30. Giorgio V, Bisetto E, Franca R, Harris DA, Passamonti S, Lippe G, (2010). The ectopic F(O)F(1) ATP synthase of rat liver is modulated in acute cholestasis by the inhibitor protein IF1. J Bioenerg Biomembr 42: 117-123.
31. 1-ATPase from bovine heart mitochondria. Biochem J 386: 591-598. (Pubitemid 40445885)
32. 1-ATPase by resveratrol and related polyphenols. Proc Natl Acad Sci USA 104: 13632-13637. (Pubitemid 350003372)
33. 1-ATPase from bovine mitochondria. Proc Natl Acad Sci USA 104: 15671-15676. (Pubitemid 350035358)
34. Gnaiger E, (2009). Capacity of oxidative phosphorylation in human skeletal muscle. New perspectives of mitochondrial physiology. Int J Biochem Cell Biol 41: 1837-1845.
35. Gomez-Fernandez JC, Harris DA, (1978). A thermodynamic analysis of the interaction between the mitochondrial coupling adenosine triphosphatase and its naturally occurring inhibitor protein. Biochem J 176: 967-975. (Pubitemid 9090481)
36. Grandy DK, (2007). Trace amine-associated receptor 1-Family archetype or iconoclast? J Pharmacol Ther 116: 355-390. (Pubitemid 350123635)
37. 1-ATPase. Biochim Biophys Acta 1458: 343-355. (Pubitemid 30320716)
38. 0-ATP hydrolase inhibitor BMS-199264 in myocardial ischemia (Review). Cardiovasc Ther 26: 287-295.
39. 0-ATPase: effect of selective pharmacological inhibition of mitochondrial ATPase hydrolase activity. Am J Physiol Heart Circ Physiol 291: H484.
40. Hall AM, Unwin RJ, Parker N, Duchen MR, (2009). Multiphoton Imaging Reveals Differences in Mitochondrial Function between Nephron Segments. J Am Soc Nephrol 20: 1293-1302.
41. Harris DA, Das AM, (1991). Control of mitochondrial ATP synthesis in the heart. Biochem J 280: 561-573.
42. Hassinen IE, Vourinen KH, Ylitalo K, Ala-Raämi A, (1998). Role of cellular energetics in ischemia-reperfusion and ischemic preconditioning of myocardium. Mol Cell Biochem 184: 393-400. (Pubitemid 28398621)
43. Hong S, Pedersen L, (2008). ATP synthase and the actions of inhibitors utilized to study its roles in human health, disease, and other scientific areas. Microbiol Mol Biol Rev 72: 590-641.
44. Horstman LL, Racker E, (1970). Partial resolution of the enzyme catalyzing oxidative phosphorylation. XXII. Interaction between mitochondrial adenosine triphosphatase inhibitor and mitochondrial adenosine triphosphatase. J Biol Chem 245: 1336-1344.
45. Ianculescu AG, Scanlan TS, (2010). 3-Iothyronamine (T1AM): a new chapter of thyroid hormone endocrinology? Mol Bio Syst 6: 1338-1344.
46. Ianculescu AG, Giacomini KM, Scanlan TS, (2009). Identification and characterization of 3-iodothyronamine intracellular transport. Endocrinology 150: 1991-1999.
47. Johnson JA, Ogbi M, (2011). Targeting the F1Fo ATP synthase: modulation of the body's powerhouse and its implications for human disease. Curr Med Chem 18: 4684-4714.
48. 1-ATPase by aurovertin. Biopolymers 91: 830-840.
49. 1-ATPase inhibited by ADP and beryllium fluoride. EMBO J 23: 2734-2744. (Pubitemid 39013546)
50. Klieverik LP, Foppen E, Ackermans MT, Serlie MJ, Sauerwein HP, Scanlan TS, et al,. (2009). Central effects of thyronamines on glucose metabolism in rats. J Endocrinol 201: 377-386.
51. Laemmli UK, (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
52. Lee C, Ernster L, (1968). Studies of the energy-transfer system of submitochondrial particles. 2. Effects of oligomycin and aurovertin. Eur J Biochem 3: 391-400.
53. Lenaz G, (1965). Effect of aurovertin on energy-linked processes related to oxidative phosphorylation. Biochem Biophys Res Commun 21: 170-175.
54. 1-ATPase. Mol Membr Biol 20: 27-33. (Pubitemid 36460643)
55. Lippe G, Sorgato MC, Harris DA, (1988). The binding and release of the inhibitor protein are governed independently by ATP and membrane potential in ox-heart submitochondrial vesicles. Biochim Biophys Acta 933: 12-21. (Pubitemid 18086626)
56. 1ATP synthase in innate and acquired cardioprotection (Review). J Bioenerg Biomembr 41: 151-157.
57. Lowry OH, Rosenbrough NJ, Far AL, Randall RJ, (1951). Protein measurement with Folin phenol reagents. J Biol Chem 193: 265-275.
58. Martinez-Irujo JJ, Villahermosa ML, Mercapide J, Cabodevilla JF, Santiago E, (1998). Analysis of the combined effect of two linear inhibitors on a single enzyme. Biochem J 329: 689-698. (Pubitemid 28055195)
59. Menz RI, Walker JE, Leslie AG, (2001). Structure of bovine mitochondrial F(1)-ATPase with nucleotide bound to all three catalytic sites: implications for the mechanism of rotary catalysis. Cell 106: 331-341. (Pubitemid 32772617)
60. Morris GM, Huey R, Lindstrom W, Sanner MF, Belew RK, Goodsell DS, et al,. (2009). AutoDock4 and AutoDockTools4: automated docking with selective receptor flexibility. J Comput Chem 30: 2785-2791.
61. Pedersen PL, (2007). Transport ATPases into the year 2008: a brief overview related to types, structures, functions and roles in health and disease. J Bioenerg Biomembr 39: 349-355.
62. 1 ATP synthase activity is differently modulated by coronary reactive hyperemia before and after ischemic preconditioning in the goat. Am J Physiol Heart Circ Physiol 287: H2192-H2200. (Pubitemid 39430759)
63. Piehl S, Hoefig C, Scanlan TS, Köhrle J, (2011). Thyronamines-past, present, and future. Endocr Rev 32: 64-80.
64. Piper HM, Abdallah Y, Schäfer C, (2004). The first minutes of reperfusion: a window of opportunity for cardioprotection. Cardiovasc Res 61: 365-371. (Pubitemid 38210144)
65. Pirola L, Frojdo S, (2008). Resveratrol: one molecule, many targets. IUBMB Life 60: 323-332.
66. Rees MR, Leslie AGW, Walker JE, (2009). The structure of the membrane extrinsic region of bovine ATP synthase. Proc Natl Acad Sci USA 106: 21597-21601.
67. Regard JB, Kataoka H, Cano DA, Camerer E, Yin L, Zheng YW, et al,. (2007). Probing cell type-specific functions of Gi in vivo identifies GPCR regulators of insulin secretion. J Clin Invest 117: 4034-4043. (Pubitemid 350224112)
68. Roberton AM, Holloway CT, Knight IG, Beechey RB, (1968). A comparison of the effects of NN'-dicyclohexylcarbodi-imide, oligomycin A and aurovertin on enrgy-linked reactions in mitochondria and submitochondrial particles. Biochem J 108: 445-456.
69. Rouslin W, (1983). Protonic inhibition of the mitochondrial oligomycin-sensitive adenosine 50-triphosphatase in ischemic and autolyzing cardiac muscle. Possible mechanism for the mitigation of ATP hydrolysis under nonenergizing conditions. J Biol Chem 258: 9657-9661. (Pubitemid 13049097)
70. 1 content, and proton conductivity of ESMP from control and ischemic slow and fast heart-rate hearts. J Bioenerg Biomembr 27: 459-466.
71. Saba A, Chiellini G, Frascarelli S, Marchini M, Ghelardoni S, Raffaelli A, et al,. (2010). Tissue distribution and cardiac metabolism of 3-iodothyronamine. Endocrinology 151: 5063-5073.
72. Scanlan TS, Suchland KL, Hart ME, Chiellini G, Huang Y, Kruzich PJ, et al,. (2004). 3 iodothyronamine is an endogenous and rapid-acting derivative of thyroid hormone. Nat Med 10: 638-642. (Pubitemid 38796856)
73. Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, Provenzano MD, et al,. (1985). Measurement of protein using bicinchoninic acid. Anal Biochem 150: 76-85. (Pubitemid 16258399)
74. Snead AN, Santos MS, Seal RP, Miyakawa M, Edwards MH, Scanlan TS, (2007). Thyronamines inhibit plasma membrane and vescicular monoamine transport. ACS Chem Biol 2: 390-398. (Pubitemid 350001561)
75. Stock D, Gibbons C, Arechaga I, Leslie AG, Walker JE, (2000). The rotary mechanism of ATP synthase. Curr Opin Struct Biol 10: 672-679. (Pubitemid 32061482)
76. 1. Biochim Biophys Acta 1556: 133-141. (Pubitemid 35379671)
77. Trott O, Olson AJ, (2010). AutoDock Vina: improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. J Comput Chem 31: 455-461.
78. Vadineanu A, Berden JA, Slater EC, (1976). Proteins required for the binding of mitochondrial ATPase to the mitochondrial inner membrane. Biochim Biophys Acta 449: 468-479.
79. 1-ATPase complexed with the antibiotic inhibitor aurovertin B. Proc Natl Acad Sci USA 93: 6913-6917. (Pubitemid 26243474)
80. Venditti P, Napolitano G, Di Stefano L, Chiellini G, Zucchi R, Scanlan TS, et al,. (2011). Effects of the thyroid hormone derivatives 3-iodothyronamine and thyronamine on rat liver oxidative capacity. Mol Cell Endocrinol 341: 55-62.
81. Watt IN, Montgomery MG, Runswick MJ, Leslie AG, Walker JE, (2010). Bioenergetic cost of making an adenosine triphosphate molecule in animal mitochondria. Proc Natl Acad Sci USA 107: 16823-16827.
82. Yonetani T, Theorell H, (1964). Studies on liver alcohol hydrogenase complexes. III. Multiple inhibition kinetics in the presence of two competitive inhibitors. Arch Biochem Biophys 106: 243-251.
83. 1 complex. Biochem Biophys Res Commun 261: 499-503. (Pubitemid 29392505)
84. 1-ATPase/ATP synthase by polyphenolic phytochemicals. Br J Pharmacol 130: 1115-1123. (Pubitemid 30453547)
85. Zucchi R, Chiellini G, Scanlan TS, Grandy DK, (2006). Trace amine-associated receptors and their ligands. Br J Pharmacol 149: 967-978. (Pubitemid 44950800)
86. Zucchi R, Ghelardoni S, Chiellini G, (2010). Cardiac effects of thyronamines. Heart Fail Rev 15: 171-176.