Mitochondrial biogenesis as a cellular signaling framework

Biochemical Pharmacology

Volumn 67, Issue 1, 2004, Pages 1-15

  Nisoli, Enzo ^a,b   Clementi, Emilio ^c,d,e   Moncada, Salvador ^f   Carruba, Michele O ^a,b  

^a UNIVERSITY OF MILAN   (Italy)

^b ISTITUTO AUXOLOGICO ITALIANO   (Italy)

^c SAN RAFFAELE HOSPITAL   (Italy)

^d SCIENTIFIC INSTITUTE   (Italy)

^e UNIVERSITY OF CALABRIA   (Italy)

^f UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Cellular signaling; Energy metabolism; Mitochondrial biogenesis

Indexed keywords

NITRIC OXIDE;

AEROBIC METABOLISM; BIOGENESIS; BIOSYNTHESIS; BROWN ADIPOSE TISSUE; CELL COMMUNICATION; CELL FUNCTION; CELL INTERACTION; CELL ORGANELLE; CELL PROLIFERATION; HUMAN; MACROMOLECULE; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; NONHUMAN; OXIDATION; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION;

EID: 0345118055     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bcp.2003.10.015     Document Type: Note

References (153)

1. Kennedy E.P., Lehninger A.L. Oxidation of fatty acids and tricarboxylic acid cycle intermediates by isolated rat liver mitochondria. J. Biol. Chem. 179:1949;957-963.
2. Tzagoloff A. Mitochondria. New York: Plenum; 1982.
3. Attardi G., Schatz G. Biogenesis of mitochondria. Annu. Rev. Cell Biol. 4:1988;289-333.
4. Neupert W. Protein import into mitochondria. Annu. Rev. Biochem. 66:1997;863-917.
5. Nisoli E., Clementi E., Paolucci C., Cozzi V., Tonello C., Sciorati C., Bracale R., Valerio A., Francolini M., Moncada S., Carruba M.O. Mitochondrial biogenesis in mammals: the role of endogenous nitric oxide. Science. 299:2003;896-899.
6. Lehninger AL. The mitochondrion. New York: W.A. Benjamin, Inc.; 1965.
7. Lewis M.R., Lewis W.H. Mitochondria (and other cytoplasmic structures) in tissue cultures. Am. J. Anat. 17:1914;339-401.
8. Krebs H.A., Kornberg H.L. Energy transformations in living matter. Ergeb. Physiol. 49:1957;212.
9. Claude A. Fractionation of mammalian liver cells by differential centrifugation. J. Exp. Med. 84:1946;51-61.
10. Sjöstrand F.S. The ultrastructure of cells as revealed by the electron microscope. Int. Rev. Cytol. 5:1956;455-533.
11. Palade G. The fine structure of mitochondria. Anat. Rec. 114:1952;427-451.
12. Frey T.G., Mannella C.A. The internal structure of mitochondria. Trends Biochem. Sci. 25:2000;319-324.
13. Mannella C.A., Marko M., Penczek P., Barnard D., Frank J. The internal compartmentation of rat-liver mitochondria: tomographic study using the high-voltage transmission electron microscope. Microsc. Res. Tech. 27:1994;278-283.
14. Mannella C.A., Marko M., Buttle K. Reconsidering mitochondrial structure: new views of an old organelle. Trends Biochem. Sci. 22:1997;37-38.
15. Penczek P., Marko M., Buttle K., Frank J. Double-tilt electron tomography. Ultramicroscopy. 60:1995;393-410.
16. Leaver CJ, Lonsdale DM. Mitochondrial biogenesis. London: Cambridge University Press; 1989.
17. Roodyn DB, Wilkie D. The biogenesis of mitochondria. London: Methuen; 1968.
18. Shepard T.H., Muffley L.A., Smith L.T. Ultrastructural study of mitochondria and their cristae in embryonic rats and primate (N. nemistrina). Anat. Rec. 252:1998;383-392.
19. López-Garcia P., Moreira D. Metabolic symbiosis at the origin of eukaryotes. Trends Biochem. Sci. 24:1999;88-93.
20. Andersson S.G.E., Kurland C.G. Origins of mitochondria and hydrogenosomes. Curr. Opin. Microbiol. 2:1999;535-541.
21. Gray M.G., Burger G., Lang B.F. Mitochondrial evolution. Science. 283:1999;1476-1481.
22. Gray M.G., Burger G., Lang B.F. The origin and early evolution of mitochondria. Genome Biol. 2:2001;1018.1-1018.5.
23. Rotte C., Henze K., Müller M., Martin W. Origins of hydrogenosomes and mitochondria. Trends Microbiol. 3:2000;481-486.
24. Margulis L. Origin of eukaryotic cells. New Haven, CT: Yale University Press; 1970.
25. Margulis L. Symbiosis in cell evolution. San Francisco: Freeman; 1981.
26. Altmann R. Die elementarorganismen und ihre beziehungen zu den zellen. Leipzig: Viet; 1890; Sapp J. Evolution by association. A history of symbiosis. New York: Oxford University Press; 1994.
27. Gray M.W. The endosymbiont hypothesis revisited. Int. Rev. Cytol. 141:1992;233-357.
28. Yang D., Oyaizu Y., Oyaizu H., Olsen G.J., Woese C.R. Mitochondrial origins. Proc. Natl. Acad. Sci. U.S.A. 82:1985;4443.
29. Gray MW, Spencer DF. Mitochondrial evolution. In: Roberts DM, Sharp P, Alderson G, Collins M, editors. Evolution of microbial life. Cambridge: Cambridge University Press; 1996. p. 107-26.
30. Sanger N., Strohmeier R., Kaufmann M., Kuhl H. Cell cycle-related expression and ligand binding of peripheral benzodiazepine receptor in human breast cancer cell lines. Eur. J. Cancer. 36:2000;2157-2163.
31. Brunk C.F. Mitochondrial proliferation during myogenesis. Exp. Cell Res. 136:1981;305-309.
32. Moyes C.D., Matthieu-Costello O.A., Tsuchiya N., Filburn C., Hansford R.G. Mitochondrial biogenesis during cellular differentiation. Am. J. Physiol. 272:1997;C1345-C1351.
33. Bereiter-Hahn J., Voth M. Dynamics of mitochondria in living cells: shape changes, dislocations, fusion, and fission of mitochondria. Microsc. Res. Tech. 27:1994;198-219.
34. Vorobjev I.A., Zorov D.B. Diazepam inhibits cell respiration and induces fragmentation of mitochondrial reticulum. FEBS Lett. 163:1983;311-314.
35. Muller-Hocker J., Pongratz D., Hubner G. Activation of mitochondrial ATPase as evidence of loosely coupled oxidative phosphorylation in various skeletal muscle disorders. A histochemical fine-structural study. J. Neurol. Sci. 74:1986;199-213.
36. Kawahara H., Houdou S., Inoue T. Scanning electron microscopic observations on muscle cells of experimental mitochondrial myopathy produced by 2,4-dinitrophenol. J. Submicrosc. Cytol. Pathol. 23:1991;397-403.
37. Goglia F., Moreno M., Lanni A. Action of thyroid hormones at the cellular level: the mitochondrial target. FEBS Lett. 452:1999;115-120.
38. Klaus S., Casteilla L., Bouillaud F., Ricquier D. The uncoupling protein UCP: a membraneous mitochondrial ion carrier exclusively expressed in brown adipose tissue. Int. J. Biochem. 23:1991;791-801.
39. Chen L.B. Mitochondrial membrane potential in living cells. Annu. Rev. Cell Biol. 4:1988;155-181.
40. Bereiter-Hahn J. Behavior of mitochondria in the living cell. Int. Rev. Cytol. 122:1990;1-63.
41. Nunnari J., Marshall W.F., Straight A., Murray A., Sedat J.W., Walter P. Mitochondrial transmission during mating in Saccharomyces cerevisiae is determined by mitochondrial fusion and fission and the intramitochondrial segregation of mitochondrial DNA. Mol. Biol. Cell. 8:1997;1233-1242.
42. Griparic L., van der Bliek A.M. The many shapes of mitochondrial membranes. Traffic. 2:2001;236-244.
43. Mozdy A.D., Shaw J.M. A fuzzy mitochondrial fusion apparatus comes into focus. Nat. Rev. Mol. Cell Biol. 4:2003;468-478.
44. Nakada K., Inoue K., Hayashi J. Interaction theory of mammalian mitochondria. Biochem. Biophys. Res. Commun. 288:2001;743-746.
45. Brown G.C. Control of respiration and ATP synthesis in mammalian mitochondria and cells. Biochem. J. 284:1992;1-13.
46. Balaban R.S. Regulation of oxidative phosphorylation in the mammalian cell. Am. J. Physiol. 258:1990;377-389.
47. Jeneson J.A., Westerhoff H.V., Kushmerick M.J. A metabolic control analysis of kinetic controls in ATP free energy metabolism in contracting skeletal muscle. Am. J. Physiol. Cell Physiol. 279:2000;C813-C832.
48. Chance B., Williams G.R. The respiratory chain and oxidative phosphorylation. Adv. Enzymol. 17:1956;65-134.
49. Arnold S., Kadenbach B. Cell respiration is controlled by ATP, an allosteric inhibitor of cytochrome c oxidase. Eur. J. Biochem. 249:1997;350-354.
50. Arnold S., Goglia F., Kadenbach B. 3,5-Diiodothyronine binds to subunit Va of cytochrome c oxidase and abolishes allosteric inhibition of respiration by ATP. Eur. J. Biochem. 252:1998;325-330.
51. Kadenbach B., Frank V., Rieger T., Napiwotzki J. Regulation of respiration and energy transduction in cytochrome c oxidase isozymes by allosteric effectors. Mol. Cell Biochem. 174:1997;131-135.
52. 2+ transport. J. Bioenerg. Biomembr. 26:1994;495-508.
53. Moyes C.D., Battersby B.J., Leary S.C. Regulation of muscle mitochondrial design. J. Exp. Biol. 201:1998;299-307.
54. Brookes P.S., Hulbert A.J., Brand M.D. The proton permeability of liposomes made from mitochondrial inner membrane phospholipids: no effect of fatty acid composition. Biochim. Biophys. Acta. 1330:1997;157-164.
55. Korshunov S.S., Skulachev V.P., Starkov A.A. High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria. FEBS Lett. 416:1997;15-18.
56. Porter R.K., Hulbert A.J., Brand M.D. Allometry of mitochondrial proton leak: influence of membrane surface area and fatty acid composition. Am. J. Physiol. Regul. Integr. Comp. Physiol. 271:1996;R1550-R1560.
57. Hulbert A.J., Else P.L. Membranes as possible pacemakers of metabolism. J. Theor. Biol. 199:1999;257-274.
58. Sluse F.E., Jarmuszkiewicz W. Uncoupling proteins outside the animal and plant kingdoms: functional and evolutionary aspects. FEBS Lett. 510:2002;117-120.
59. Garlid K.D., Jaburek M., Jezek P. Mechanism of uncoupling protein action. Biochem. Soc. Trans. 29:2001;803-806.
60. Klingenberg M., Winkler E., Echtay K. Uncoupling protein, H+ transport and regulation. Biochem. Soc. Trans. 29:2001;806-811.
61. Nedergaard J., Golozoubova V., Matthias A., Shabalina I., Ohba K., Ohlson K., Jacobsson A., Cannon B. Life without UCP1: mitochondrial, cellular and organismal characteristics of the UCP1-ablated mice. Biochem. Soc. Trans. 29:2001;756-763.
62. Echtay K.S., Winkler E., Klingenberg M. Coenzyme Q is an obligatory cofactor for uncoupling protein function. Nature. 408:2000;609-613.
63. Klingenberg M., Echtay K.S. Uncoupling proteins: the issues from a biochemist point of view. Biochim. Biophys. Acta. 1504:2001;128-143.
64. Winkler E., Klingenberg M. Effect of fatty acids on H+ transport activity of the reconstituted uncoupling protein. J. Biol. Chem. 269:1994;2508-2515.
65. Jezek P., Engstova H., Zackova M., Vercesi A.E., Costa A.D., Arruda P., Garlid K.D. Fatty acid cycling mechanism and mitochondrial uncoupling proteins. Biochim. Biophys. Acta. 1365:1998;319-327.
66. Rial E., Jiménez-Jimenéz J. Biochim. Biophys. Acta. EBEC 11(Suppl.):2000;112.
67. Rial E., Gonzalez-Barroso M.M. Physiological regulation of the transport activity in the uncoupling proteins UCP1 and UCP2. Biochim. Biophys. Acta. 1504:2001;70-81.
68. Matthias A., Jacobsson A., Cannon B., Nedergaard J. The bioenergetics of brown fat mitochondria from UCP1-ablated mice. Ucp1 is not involved in fatty acid-induced de-energization ("uncoupling"). J. Biol. Chem. 274:1999;28150-28160.
69. Nedergaard J., Golozoubova V., Matthias A., Asadi A., Jacobsson A., Cannon B. UCP1: the only protein able to mediate adaptive non-shivering thermogenesis and metabolic inefficiency. Biochim. Biophys. Acta. 1504:2001;82-106.
70. Stuart J.A., Cadenas S., Jacobsons M.B., Roussel D., Brand M.D. Mitochondrial proton leak and the uncoupling protein 1 homologues. Biochim. Biophys. Acta. 1504:2001;144-158.
71. Jaburek M., Varecha M., Gimeno R.E., Dembski M., Jezek P., Zhang M., Burn P., Tartaglia L.A., Garlid K.D. Transport function and regulation of mitochondrial uncoupling proteins 2 and 3. J. Biol. Chem. 274:1999;26003-26007.
72. Dulloo A.G., Samec S., Seydoux J. Uncoupling protein 3 and fatty acid metabolism. Biochem. Soc. Trans. 29:2001;785-791.
73. Nedergaard J., Cannon B. The "novel" "uncoupling" proteins UCP2 and UCP3: what do they really do? Pros and cons for suggested functions. Exp. Physiol. 88(Pt 1):2003;65-84.
74. Han D., Antunes F., Daneri F., Cadenas E. Mitochondrial superoxide anion production and release into intermembrane space. Methods Enzymol. 349:2002;271-280.
75. Leary SC, Moyes CD. The effects of bioenergetic stress and redox balance on the expression of genes critical to mitochondrial function. In: Storey KB, Storey J, editors. Cell and molecular responses to stress. Amsterdam: Elsevier; 2000. p. 209-29.
76. Bakeeva L.E., Chentsov Y.S., Skulachev V.P. Mitochondrial framework (reticulum mitochondriale) in rat diaphragm muscle. Biochim. Biophys. Acta. 501:1978;349-369.
77. Diaz G., Falchi A.M., Gremo F., Isola R., Diana A. Homogeneous longitudinal profiles and synchronous fluctuations of mitochondrial transmembrane potential. FEBS Lett. 475:2000;218-224.
78. Sidell B.D. Intracellular oxygen diffusion: the roles of myoglobin and lipid at cold body temperature. J. Exp. Biol. 201:1998;1119-1128.
79. Luzikov V.N. Quality control: from molecule to organelles. FEBS Lett. 448:1999;201-205.
80. Santel A., Fuller M.T. Control of mitochondrial morphology by a human mitofusin. J. Cell Sci. 114:2001;867-874.
81. Frank S., Gaume B., Bergmann-Leitner E.S., Leitner W.W., Robert E.G., Catez F., Smith C.L., Youle R.J. The role of dynamin-related protein 1, a mediator of mitochondrial fission, in apoptosis. Dev. Cell. 1:2001;515-525.
82. Hood D.A. Contractile activity-induced mitochondrial biogenesis in skeletal muscle. J. Appl. Physiol. 90:2001;1137-1157.
83. Adhihetty P.J., Irrcher I., Joseph A.M., Ljubicic V., Hood D.A. Plasticity of skeletal muscle mitochondria in response to contractile activity. Exp. Physiol. 88:2003;99-107.
84. Li B., Holloszy J.O., Semenkovich C.F. Respiratory uncoupling induces delta-aminolevulinate synthase expression through a nuclear respiratory factor-1-dependent mechanism in HeLa cells. J. Biol. Chem. 274:1999;17534-17540.
85. Bergeron R., Ren J.M., Cadman K.S., Moore I.K., Perret P., Pypaert M., Young L.H., Semenkovich C.F., Shulman G.I. Chronic activation of AMP kinase results in NRF-1 activation and mitochondrial biogenesis. Am. J. Physiol. Endocrinol. Metab. 281:2001;E1340-E1346.
86. Winder W.W., Holmes B.F., Rubink D.S., Jensen E.B., Chen M., Holloszy J.O. Activation of AMP-activated protein kinase increases mitochondrial enzymes in skeletal muscle. J. Appl. Physiol. 88:2000;2219-2226.
87. Hardie D.G., Hawley S.A. AMP-activated protein kinase: the energy charge hypothesis revisited. Bioessays. 23:2001;1112-1119.
88. Fulton D., Gratton J.P., Sessa W.C. Post-translational control of endothelial nitric oxide synthase: why isn't calcium/calmodulin enough? J. Pharmacol. Exp. Ther. 299:2001;818-824.
89. Davies K.J., Packer L., Brooks G.A. Biochemical adaptation of mitochondria, muscle, and whole-animal respiration to endurance training. Arch. Biochem. Biophys. 209:1981;539-554.
90. Wu H., Kanatous S.B., Thurmond F.A., Gallardo T., Isotani E., Bassel-Duby R., Williams R.S. Regulation of mitochondrial biogenesis in skeletal muscle by CaMK. Science. 296:2002;349-352.
91. Handschin C., Rhee J., Lin J., Tarr P.T., Spiegelman B.M. An autoregulatory loop controls peroxisome proliferator-activated receptor gamma coactivator 1alpha expression in muscle. Proc. Natl. Acad. Sci. U.S.A. 100:2003;7111-7116.
92. Lowell B.B., Spiegelman B.M. Towards a molecular understanding of adaptive thermogenesis. Nature. 404:2000;652-660.
93. Perkins G.A., Song J.Y., Tarsa L., Deerinck T.J., Ellisman M.H., Frey T.G. Electron tomography of mitochondria from brown adipocytes reveals crista junctions. J. Bioenerg. Biomembr. 30:1998;431-442.
94. Perkins G., Renken C., Martone M.E., Young S.J., Ellisman M., Frey T. Electron tomography of neuronal mitochondria: three-dimensional structure and organization of cristae and membrane contacts. J. Struct. Biol. 119:1997;260-272.
95. Seydoux J., Girardier L. Control of brown fat thermogenesis by the sympathetic nervous system. EXS. 32:1978;153-167.
96. Himms-Hagen J., Cui J., Danforth E. Jr., Taatjes D.J., Lang S.S., Waters B.L., Claus T.H. Effect of CL-316,243, a thermogenic beta 3-agonist, on energy balance and brown and white adipose tissues in rats. Am. J. Physiol. 266:1994;R1371-R1382.
97. Bronnikov G., Bengtsson T., Kramarova L., Golozoubova V., Cannon B., Nedergaard J. β1 to β3 switch in control of cyclic adenosine monophosphate during brown adipocyte development explains distinct β-adrenoceptor subtype mediation of proliferation and differentiation. Endocrinology. 140:1999;4185-4197.
98. Klaus S., Seivert A., Boeuf S. Effect of the beta(3)-adrenergic agonist CL316,243 on functional differentiation of white and brown adipocytes in primary cell culture. Biochim. Biophys. Acta. 1539:2001;85-92.
99. Zhao J., Cannon B., Nedergaard J. Thermogenesis is beta3- but not beta1-adrenergically mediated in rat brown fat cells, even after cold acclimation. Am. J. Physiol. 275:1998;R2002-R2011.
100. Nisoli E., Tonello C., Carruba M.O. Differential relevance of beta-adrenoceptor subtypes in modulating the rat brown adipocytes function. Arch. Int. Pharmacodyn. Ther. 329:1995;436-453.
101. Shih M.F., Taberner P.V. Selective activation of brown adipocyte hormone-sensitive lipase and cAMP production in the mouse by beta(3)-adrenoceptor agonists. Biochem. Pharmacol. 50:1995;601-608.
102. Nicholls D.G., Rial E. A history of the first uncoupling protein, UCP1. J. Bioenerg. Biomembr. 31:1999;399-406.
103. Matthias A., Jacobsson A., Cannon B., Nedergaard J. The bioenergetics of brown fat mitochondria from UCP1-ablated mice. UCP1 is not involved in fatty acid-induced de-energization. J. Biol. Chem. 274:1999;28150-28160.
104. Monemdjou S., Hofmann W.E., Kozak L.P., Harper M.E. Increased mitochondrial proton leak in skeletal muscle mitochondria of UCP1-deficient mice. Am. J. Physiol. Endocrinol. Metab. 279:2000;E941-E946.
105. Nedergaard J., Golozoubova V., Matthias A., Shabalina I., Ohba K., Ohlson K., Jacobsson A., Cannon B. Life without UCP1: mitochondrial, cellular and organismal characteristics of the UCP1-ablated mice. Biochem. Soc. Trans. 29:2001;756-763.
106. Rossmeisl M., Barbatelli G., Flachs P., Brauner P., Zingaretti M.C., Marelli M., Janovska P., Horakova M., Syrovy I., Cinti S., Kopecky J. Expression of the uncoupling protein 1 from the aP2 gene promoter stimulates mitochondrial biogenesis in unilocular adipocytes in vivo. Eur. J. Biochem. 269:2002;19-28.
107. Moncada S., Palmer R.M., Higgs E.A. Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol. Rev. 43:1991;109-142.
108. Alderton W.K., Cooper C.E., Knowles R.G. Nitric oxide synthases: structure, function and inhibition. Biochem. J. 357:2001;593-615.
109. Wolzt M., MacAllister R.J., Davis D., Feelisch M., Moncada S., Vallance P., Hobbs A.J. Biochemical characterization of S-nitrosohemoglobin. Mechanisms underlying synthesis, No release, and biological activity. J. Biol. Chem. 274:1999;28983-28990.
110. Cleeter M.W., Cooper J.M., Darley-Usmar V.M., Moncada S., Schapira A.H. Reversible inhibition of cytochrome c oxidase, the terminal enzyme of the mitochondrial respiratory chain, by nitric oxide. Implications for neurodegenerative diseases. FEBS Lett. 345:1994;50-54.
111. Brown G.C., Cooper C.E. Nanomolar concentrations of nitric oxide reversibly inhibit synaptosomal respiration by competing with oxygen at cytochrome oxidase. FEBS Lett. 356:1994;295-298.
112. Clementi E., Brown G.C., Feelisch M., Moncada S. Persistent inhibition of cell respiration by nitric oxide: crucial role of S-nitrosylation of mitochondrial complex I and protective action of glutathione. Proc. Natl. Acad. Sci. U.S.A. 95:1998;7631-7636.
113. Clementi E., Brown G.C., Foxwell N., Moncada S. On the mechanism by which vascular endothelial cells regulate their oxygen consumption. Proc. Natl. Acad. Sci. U.S.A. 96:1999;1559-1562.
114. Semenza G.L. Perspectives on oxygen sensing. Cell. 98:1999;281-284.
115. Ghafourifar P., Richter C. Nitric oxide synthase activity in mitochondria. FEBS Lett. 418:1997;291-296.
116. Giulivi C., Poderoso J.J., Boveris A. Production of nitric oxide by mitochondria. J. Biol. Chem. 273:1998;11038-11043.
117. Nisoli E., Tonello C., Briscini L., Carruba M.O. Inducible nitric oxide synthase in rat brown adipocytes: implications for blood flow to brown adipose tissue. Endocrinology. 138:1997;676-682.
118. Giordano A., Tonello C., Bulbarelli A., Cozzi V., Cinti S., Carruba M.O., Nisoli E. Evidence for a functional nitric oxide synthase system in brown adipocyte nucleus. FEBS Lett. 514:2002;135-140.
119. Puigserver P., Wu Z., Park C.W., Graves R., Wright M., Spiegelman B.M. A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell. 92:1998;829-839.
120. Nisoli E., Clementi E., Tonello C., Sciorati C., Briscini L., Carruba M.O. Effects of nitric oxide on proliferation and differentiation of rat brown adipocytes in primary cultures. Br. J. Pharmacol. 125:1998;888-894.
121. Saha S.K., Kuroshima A. Nitric oxide and thermogenic function of brown adipose tissue in rats. Jpn. J. Physiol. 50:2000;337-342.
122. Kikuchi-Utsumi K., Gao B., Ohinata H., Hashimoto M., Yamamoto N., Kuroshima A. Enhanced gene expression of endothelial nitric oxide synthase in brown adipose tissue during cold exposure. Am. J. Physiol. Regul. Integr. Comp. Physiol. 282:2002;R623-R626.
123. Uchida Y., Tsukahara F., Irie K., Nomoto T., Muraki T. Possible involvement of L-arginine-nitric oxide pathway in modulating regional blood flow to brown adipose tissue of rats. Naunyn Schmiedebergs Arch. Pharmacol. 349:1994;188-193.
124. Nagashima T., Ohinata H., Kuroshima A. Involvement of nitric oxide in noradrenaline-induced increase in blood flow through brown adipose tissue. Life Sci. 54:1994;17-25.
125. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxic assays. J. Immunol. Methods. 65:1983;55-63.
126. Reaven G.M. Banting lecture 1988. Role of insulin resistance in human disease. Diabetes. 37:1988;1595-1607.
127. National Institutes of Health: Third Report of the National Cholesterol Education Program Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel III). Bethesda, MD: National Institutes of Health; 2001 [NIH Publication 01-3670].
128. Ballantyne CM, Olsson AG, Cook TJ, Mercuri MF, Pedersen TR, Kjekshus J, for the 4S Group. Influence of low high-density lipoprotein cholesterol and elevated triglyceride on coronary heart disease events and response to simvastatin therapy in 4S. Circulation 2001;104:3046-51.
129. Ford E.S., Giles W.H., Dietz W.H. Prevalence of the metabolic syndrome among US adults. JAMA. 287:2002;356-359.
130. Patti M.E., Butte A.J., Crunkhorn S., Cusi K., Berria R., Kashyap S., Miyazaki Y., Kohane I., Costello M., Saccone R., Landaker E.J., Goldfine A.B., Mun E., DeFronzo R., Finlayson J., Kahn C.R., Mandarino L.J. Coordinated reduction of genes of oxidative metabolism in humans with insulin resistance and diabetes: potential role of PGC1 and NRF1. Proc. Natl. Acad. Sci. U.S.A. 100:2003;8466-8471.
131. Simoneau J.A., Veerkamp J.H., Turcotte L.P., Kelley D.E. Markers of capacity to utilize fatty acids in human skeletal muscle: relation to insulin resistance and obesity and effects of weight loss. FASEB J. 13:1999;2051-2060.
132. Kelley D.E., He J., Menshikova E.V., Ritov V.B. Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes. Diabetes. 51:2002;2944-2950.
133. Song J., Oh J.Y., Sung Y.A., Pak Y.K., Park K.S., Lee H.K. Peripheral blood mitochondrial DNA content is related to insulin sensitivity in offspring of type 2 diabetic patients. Diabetes Care. 24:2001;865-869.
134. Antonetti D.A., Reynet C., Kahn C.R. Increased expression of mitochondrial-encoded genes in skeletal muscle of humans with diabetes mellitus. J. Clin. Invest. 95:1995;1383-1388.
135. Yechoor V.K., Patti M.E., Saccone R., Kahn C.R. Coordinated patterns of gene expression for substrate and energy metabolism in skeletal muscle of diabetic mice. Proc. Natl. Acad. Sci. U.S.A. 99:2002;10587-10592.
136. Sreekumar R., Halvatsiotis P., Schimke J.C., Nair K.S. Gene expression profile in skeletal muscle of type 2 diabetes and the effect of insulin treatment. Diabetes. 51:2002;1913-1920.
137. Yang X., Pratley R.E., Tokraks S., Bogardus C., Permana P.A. Microarray profiling of skeletal muscle tissues from equally obese, non-diabetic insulin-sensitive and insulin-resistant Pima Indians. Diabetologia. 45:2002;1584-1593.
138. Vicent D., Piper M., Gammeltoft S., Maratos-Flier E., Kahn C.R. Alterations in skeletal muscle gene expression of ob/ob mice by mRNA differential display. Diabetes. 47:1998;1451-1458.
139. Mootha V.K., Lindgren C.M., Eriksson K.F., Subramanian A., Sihag S., Lehar J., Puigserver P., Carlsson E., Ridderstrale M., Laurila E., Houstis N., Daly M.J., Patterson N., Mesirov J.P., Golub T.R., Tamayo P., Spiegelman B., Lander E.S., Hirschhorn J.N., Altshuler D., Groop L.C. PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat. Genet. 34:2003;267-273.
140. Nathan C. Specificity of a third kind: reactive oxygen and nitrogen intermediates in cell signaling. J. Clin. Invest. 111:2003;769-778.
141. Palmer R.M., Ferrige A.G., Moncada S. Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature. 327:1987;524-526.
142. Ignarro L.J., Buga G.M., Wood K.S., Byrns R.E., Chaudhuri G. Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide. Proc. Natl. Acad. Sci. U.S.A. 84:1987;9265-9269.
143. Arnold W.P., Mittal C.K., Katsuki S., Murad F. Nitric oxide activates guanylate cyclase and increases guanosine 3′:5′-cyclic monophosphate levels in various tissue preparations. Proc. Natl. Acad. Sci. U.S.A. 74:1977;3203-3207.
144. Schreck R., Rieber P., Baeuerle P.A. Reactive oxygen intermediates as apparently widely used messengers in the activation of the NF-kappa B transcription factor and HIV-1. EMBO J. 10:1991;2247-2258.
145. Amstad P.A., Krupitza G., Cerutti P.A. Mechanism of c-fos induction by active oxygen. Cancer Res. 52:1992;3952-3960.
146. Golderer G., Werner E.R., Leitner S., Grobner P., Werner-Felmayer G. Nitric oxide synthase is induced in sporulation of Physarum polycephalum. Genes Dev. 15:2001;1299-1309.
147. Kuzin B., Roberts I., Peunova N., Enikolopov G. Nitric oxide regulates cell proliferation during Drosophila development. Cell. 87:1996;639-649.
148. Peunova N., Scheinker V., Cline H., Enikolopov G. Nitric oxide is an essential negative regulator of cell proliferation in Xenopus brain. J. Neurosci. 21:2001;8809-8818.
149. Klein J.A., Longo-Guess C.M., Rossmann M.P., Seburn K.L., Hurd R.E., Frankel W.N., Bronson R.T., Ackerman S.L. The harlequin mouse mutation downregulates apoptosis-inducing factor. Nature. 419:2002;367-374.
150. Gu Z., Kaul M., Yan B., Kridel S.J., Cui J., Strongin A., Smith J.W., Liddington R.C., Lipton S.A. S-Nitrosylation of matrix metalloproteinases: signaling pathway to neuronal cell death. Science. 297:2002;1186-1190.
151. Terman J.R., Mao T., Pasterkamp R.J., Yu H.H., Kolodkin A.L. MICALs, a family of conserved flavoprotein oxidoreductases, function in plexin-mediated axonal repulsion. Cell. 109:2002;887-900.
152. Moncada S., Erusalimsky J.D. Does nitric oxide modulate mitochondrial energy generation and apoptosis? Nat. Rev. Mol. Cell Biol. 3:2002;214-220.
153. Wu G., Meininger C.J. Regulation of nitric oxide synthesis by dietary factors. Annu. Rev. Nutr. 22:2002;61-86.