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Journal of Biomedicine and Biotechnology
Volume 2011, Article ID 810242, 19 pages
http://dx.doi.org/10.1155/2011/810242
Review Article

Studies of Complex Biological Systems with Applications to Molecular Medicine: The Need to Integrate Transcriptomic and Proteomic Approaches

1Dipartimento di Scienze Biologiche ed Ambientali, Università degli Studi del Sannio, Via Port'Arsa 11, 82100 Benevento, Italy
2Dipartimento delle Scienze Biologiche, Sezione Fisiologia, Università degli Studi di Napoli “Federico II”, Via Mezzocannone 8, 80134 Napoli, Italy
3Dipartimento di Scienze della Vita, Seconda Università di Napoli, Via Vivaldi 43, 81100 Caserta, Italy

Received 15 April 2010; Accepted 8 September 2010

Academic Editor: Mika Ala-Korpela

Copyright © 2011 Elena Silvestri et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. M. Schena, D. Shalon, R. W. Davis, and P. O. Brown, “Quantitative monitoring of gene expression patterns with a complementary DNA microarray,” Science, vol. 270, no. 5235, pp. 467–470, 1995. View at Google Scholar · View at Scopus
  2. D. Gerhold, T. Rushmore, and C. T. Caskey, “DNA chips: promising toys have become powerful tools,” Trends in Biochemical Sciences, vol. 24, no. 5, pp. 168–173, 1999. View at Publisher · View at Google Scholar · View at Scopus
  3. G. G. Lennon, “High-throughput gene expression analysis for drug discovery,” Drug Discovery Today, vol. 5, no. 2, pp. 59–66, 2000. View at Publisher · View at Google Scholar · View at Scopus
  4. J. E. Celis, M. Østergaard, N. A. Jensen, I. Gromova, H. H. Rasmussen, and P. Gromov, “Human and mouse proteomic databases: novel resources in the protein universe,” FEBS Letters, vol. 430, no. 1-2, pp. 64–72, 1998. View at Publisher · View at Google Scholar · View at Scopus
  5. R. D. Appel, C. Hoogland, A. Bairoch, and D. F. Hochstrasser, “Constructing a 2-D database for the World Wide Web,” Methods in Molecular Biology, vol. 112, pp. 411–416, 1999. View at Google Scholar · View at Scopus
  6. M. J. Dunn, “Studying heart disease using the proteomic approach,” Drug Discovery Today, vol. 5, no. 2, pp. 76–84, 2000. View at Publisher · View at Google Scholar · View at Scopus
  7. P. G. Righetti, A. Castagna, F. Antonucci et al., “Critical survey of quantitative proteomics in two-dimensional electrophoretic approaches,” Journal of Chromatography A, vol. 1051, no. 1-2, pp. 3–17, 2004. View at Publisher · View at Google Scholar · View at Scopus
  8. A. Vlahou and M. Fountoulakis, “Proteomic approaches in the search for disease biomarkers,” Journal of Chromatography B, vol. 814, no. 1, pp. 11–19, 2005. View at Publisher · View at Google Scholar · View at Scopus
  9. A. A. Vandervoort, “Aging of the human neuromuscular system,” Muscle and Nerve, vol. 25, no. 1, pp. 17–25, 2002. View at Publisher · View at Google Scholar · View at Scopus
  10. L. J. Melton III, S. Khosla, C. S. Crowson, M. K. O'Connor, W. M. O'Fallon, and B. L. Riggs, “Epidemiology of sarcopenia,” Journal of the American Geriatrics Society, vol. 48, no. 6, pp. 625–630, 2000. View at Google Scholar · View at Scopus
  11. L. J. S. Greenlund and K. S. Nair, “Sarcopenia—consequences, mechanisms, and potential therapies,” Mechanisms of Ageing and Development, vol. 124, no. 3, pp. 287–299, 2003. View at Publisher · View at Google Scholar · View at Scopus
  12. E. Carmeli, R. Coleman, and A. Z. Reznick, “The biochemistry of aging muscle,” Experimental Gerontology, vol. 37, no. 4, pp. 477–489, 2002. View at Publisher · View at Google Scholar · View at Scopus
  13. L. Larsson, “The age-related motor disability: underlying mechanisms in skeletal muscle at the motor unit, cellular and molecular level,” Acta Physiologica Scandinavica, vol. 163, no. 3, pp. S27–S29, 1998. View at Google Scholar · View at Scopus
  14. D. V. Rao, G. M. Boyle, P. G. Parsons, K. Watson, and G. L. Jones, “Influence of ageing, heat shock treatment and in vivo total antioxidant status on gene-expression profile and protein synthesis in human peripheral lymphocytes,” Mechanisms of Ageing and Development, vol. 124, no. 1, pp. 55–69, 2003. View at Publisher · View at Google Scholar · View at Scopus
  15. D. H. Ly, D. J. Lockhart, R. A. Lerner, and P. G. Schultz, “Mitotic misregulation and human aging,” Science, vol. 287, no. 5462, pp. 2486–2492, 2000. View at Publisher · View at Google Scholar · View at Scopus
  16. K. J. Kyng, A. May, S. Kølvraa, and V. A. Bohr, “Gene expression profiling in Werner syndrome closely resembles that of normal aging,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 21, pp. 12259–12264, 2003. View at Publisher · View at Google Scholar · View at Scopus
  17. T. Lu, Y. Pan, S.-Y. Kao et al., “Gene regulation and DNA damage in the ageing human brain,” Nature, vol. 429, no. 6994, pp. 883–891, 2004. View at Publisher · View at Google Scholar · View at Scopus
  18. L. Erraji-Benchekroun, M. D. Underwood, V. Arango et al., “Molecular aging in human prefrontal cortex is selective and continuous throughout adult life,” Biological Psychiatry, vol. 57, no. 5, pp. 549–558, 2005. View at Publisher · View at Google Scholar · View at Scopus
  19. S. Welle, A. I. Brooks, J. M. Delehanty et al., “Skeletal muscle gene expression profiles in 20-29 year old and 65-71 year old women,” Experimental Gerontology, vol. 39, no. 3, pp. 369–377, 2004. View at Publisher · View at Google Scholar · View at Scopus
  20. A. B. Csoka, S. B. English, C. P. Simkevich et al., “Genome-scale expression profiling of Hutchinson-Gilford progeria syndrome reveals widespread transcriptional misregulation leading to mesodermal/mesenchymal defects and accelarated atherosclerosis,” Aging Cell, vol. 3, no. 4, pp. 235–243, 2004. View at Publisher · View at Google Scholar · View at Scopus
  21. J. M. Zahn, R. Sonu, H. Vogel et al., “Transcriptional profiling of aging in human muscle reveals a common aging signature,” PLoS genetics, vol. 2, no. 7, article e115, 2006. View at Publisher · View at Google Scholar · View at Scopus
  22. G. E. J. Rodwell, R. Sonu, J. M. Zahn et al., “A transcriptional profile of aging in the human kidney,” PLoS Biology, vol. 2, no. 12, article e427, 2004. View at Publisher · View at Google Scholar · View at Scopus
  23. S. Welle, A. I. Brooks, J. M. Delehanty, N. Needler, and C. A. Thornton, “Gene expression profile of aging in human muscle,” Physiological Genomics, vol. 14, pp. 149–159, 2003. View at Google Scholar · View at Scopus
  24. J. Tower, “Sex-specific regulation of aging and apoptosis,” Mechanisms of Ageing and Development, vol. 127, no. 9, pp. 705–718, 2006. View at Publisher · View at Google Scholar · View at Scopus
  25. C.-K. Lee, R. G. Klopp, R. Weindruch, and T. A. Prolla, “Gene expression profile of aging and its retardation by caloric restriction,” Science, vol. 285, no. 5432, pp. 1390–1393, 1999. View at Publisher · View at Google Scholar · View at Scopus
  26. A. Lombardi, E. Silvestri, F. Cioffi et al., “Defining the transcriptomic and proteomic profiles of rat ageing skeletal muscle by the use of a cDNA array, 2D- and Blue native-PAGE approach,” Journal of Proteomics, vol. 72, no. 4, pp. 708–721, 2009. View at Publisher · View at Google Scholar · View at Scopus
  27. T. Kayo, D. B. Allison, R. Weindruch, and T. A. Prolla, “Influences of aging and caloric restriction on the transcriptional profile of skeletal muscle from rhesus monkeys,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 9, pp. 5093–5098, 2001. View at Publisher · View at Google Scholar · View at Scopus
  28. R. Sreekumar, J. Unnikrishnan, A. Fu et al., “Effects of caloric restriction on mitochondrial function and gene transcripts in rat muscle,” American Journal of Physiology - Endocrinology and Metabolism, vol. 283, no. 1, pp. E38–43, 2002. View at Google Scholar
  29. M. Altun, E. Edström, E. Spooner et al., “Iron load and redox stress in skeletal muscle of aged rats,” Muscle and Nerve, vol. 36, no. 2, pp. 223–233, 2007. View at Publisher · View at Google Scholar · View at Scopus
  30. J. Gannon, L. Staunton, K. O'Connell, P. Doran, and K. Ohlendieck, “Phosphoproteomic analysis of aged skeletal muscle,” International Journal of Molecular Medicine, vol. 22, no. 1, pp. 33–42, 2008. View at Google Scholar · View at Scopus
  31. J. Kanski, M. A. Alterman, and C. Schöneich, “Proteomic identification of age-dependent protein nitration in rat skeletal muscle,” Free Radical Biology and Medicine, vol. 35, no. 10, pp. 1229–1239, 2003. View at Publisher · View at Google Scholar · View at Scopus
  32. J. Kanski, S. J. Hong, and C. Schöneich, “Proteomic analysis of protein nitration in aging skeletal muscle and identification of nitrotyrosine-containing sequences in vivo by nanoelectrospray ionization tandem mass spectrometry,” The Journal of Biological Chemistry, vol. 280, no. 25, pp. 24261–24266, 2005. View at Publisher · View at Google Scholar · View at Scopus
  33. K. O'Connell, P. Doran, J. Gannon, and K. Ohlendieck, “Lectin-based proteomic profiling of aged skeletal muscle: decreased pyruvate kinase isozyme M1 exhibits drastically increased levels of N-glycosylation,” European Journal of Cell Biology, vol. 87, no. 10, pp. 793–805, 2008. View at Publisher · View at Google Scholar · View at Scopus
  34. C. Gelfi, A. Viganò, M. Ripamonti et al., “The human muscle proteome in aging,” Journal of Proteome Research, vol. 5, no. 6, pp. 1344–1353, 2006. View at Publisher · View at Google Scholar · View at Scopus
  35. D. Cai, M. Li, K. Lee, K. Lee, W. Wong, and K. Chan, “Age-related changes of aqueous protein profiles in rat fast and slow twitch skeletal muscles,” Electrophoresis, vol. 21, no. 2, pp. 465–472, 2000. View at Publisher · View at Google Scholar · View at Scopus
  36. I. Piec, A. Listrat, J. Alliot, C. Chambon, R. G. Taylor, and D. Bechet, “Differential proteome analysis of aging in rat skeletal muscle,” The FASEB Journal, vol. 19, no. 9, pp. 1143–1145, 2005. View at Publisher · View at Google Scholar · View at Scopus
  37. K. O'Connell, J. Gannon, P. Doran, and K. Ohlendieck, “Proteomic profiling reveals a severely perturbed protein expression pattern in aged skeletal muscle,” International Journal of Molecular Medicine, vol. 20, no. 2, pp. 145–153, 2007. View at Google Scholar · View at Scopus
  38. P. Doran, K. O'Connell, J. Gannon, M. Kavanagh, and K. Ohlendieck, “Opposite pathobiochemical fate of pyruvate kinase and adenylate kinase in aged rat skeletal muscle as revealed by proteomic DIGE analysis,” Proteomics, vol. 8, no. 2, pp. 364–377, 2008. View at Publisher · View at Google Scholar · View at Scopus
  39. J. Chang, H. Van Remmen, J. Cornell, A. Richardson, and W. F. Ward, “Comparative proteomics: characterization of a two-dimensional gel electrophoresis system to study the effect of aging on mitochondrial proteins,” Mechanisms of Ageing and Development, vol. 124, no. 1, pp. 33–41, 2003. View at Publisher · View at Google Scholar · View at Scopus
  40. D. Q. Cai, M. Li, K. K. Lee et al., “Parvalbumin expression is downregulated in rat fast-twitch skeletal muscles during aging,” Archives of Biochemistry and Biophysics, vol. 387, no. 2, pp. 202–208, 2001. View at Google Scholar
  41. N. A. Dencher, S. Goto, N. H. Reifschneider, M. Sugawa, and F. Krause, “Unraveling age-dependent variation of the mitochondrial proteome,” Annals of the New York Academy of Sciences, vol. 1067, no. 1, pp. 116–119, 2006. View at Publisher · View at Google Scholar · View at Scopus
  42. J. Feng, H. Xie, D. L. Meany, L. V. Thompson, E. A. Arriaga, and T. J. Griffin, “Quantitative proteomic profiling of muscle type-dependent and age-dependent protein carbonylation in rat skeletal muscle mitochondria,” Journals of Gerontology A, vol. 63, no. 11, pp. 1137–1152, 2008. View at Google Scholar · View at Scopus
  43. G. S. Cobon, N. Verrills, P. Papakostopoulos et al., “Proteomics of ageing,” Biogerontology, vol. 3, no. 1-2, pp. 133–136, 2002. View at Google Scholar
  44. X. Feng, Y. Jiang, P. Meltzer, and P. M. Yen, “Thyroid hormone regulation of hepatic genes in vivo detected by complementary DNA microarray,” Molecular Endocrinology, vol. 14, no. 7, pp. 947–955, 2000. View at Publisher · View at Google Scholar · View at Scopus
  45. A. Flores-Morales, H. Gullberg, L. Fernandez et al., “Patterns of liver gene expression governed by TRβ,” Molecular Endocrinology, vol. 16, no. 6, pp. 1257–1268, 2002. View at Publisher · View at Google Scholar · View at Scopus
  46. L. D. Miller, P. McPhie, H. Suzuki, Y. Kato, E. T. Liu, and S. Y. Cheng, “Multi-tissue gene-expression analysis in a mouse model of thyroid hormone resistance,” Genome Biology, vol. 5, no. 5, article R31, 2004. View at Google Scholar · View at Scopus
  47. T. Ventura-Holman, A. Mamoon, J. F. Maher et al., “Thyroid hormone responsive genes in the murine hepatocyte cell line AML 12,” Gene, vol. 396, no. 2, pp. 332–327, 2007. View at Google Scholar
  48. H. Dong, C. L. Yauk, A. Williams, A. Lee, G. R. Douglas, and M. G. Wade, “Hepatic gene expression changes in hypothyroid juvenile mice: characterization of a novel negative thyroid-responsive element,” Endocrinology, vol. 148, no. 8, pp. 3932–3940, 2007. View at Publisher · View at Google Scholar · View at Scopus
  49. J. M. Weitzel, C. Radtke, and H. J. Seitz, “Two thyroid hormone-mediated gene expression patterns in vivo identified by cDNA expression arrays in rat,” Nucleic Acids Research, vol. 29, no. 24, pp. 5148–5155, 2001. View at Google Scholar · View at Scopus
  50. L. D. Miller, K. S. Park, Q. M. Guo et al., “Silencing of Wnt signaling and activation of multiple metabolic pathways in response to thyroid hormone-stimulated cell proliferation,” Molecular and Cellular Biology, vol. 21, no. 19, pp. 6626–6639, 2001. View at Publisher · View at Google Scholar · View at Scopus
  51. N. Viguerie and D. Langin, “Effect of thyroid hormone on gene expression,” Current Opinion in Clinical Nutrition and Metabolic Care, vol. 6, no. 4, pp. 377–381, 2003. View at Publisher · View at Google Scholar · View at Scopus
  52. L. C. Moeller, A. M. Dumitrescu, R. L. Walker, P. S. Meltzer, and S. Refetoff, “Thyroid hormone responsive genes in cultured human fibroblasts,” Journal of Clinical Endocrinology and Metabolism, vol. 90, no. 2, pp. 936–943, 2005. View at Publisher · View at Google Scholar · View at Scopus
  53. K. Clément, N. Viguerie, M. Diehn et al., “In vivo regulation of human skeletal muscle gene expression by thyroid hormone,” Genome Research, vol. 12, no. 2, pp. 281–291, 2002. View at Publisher · View at Google Scholar · View at Scopus
  54. W. E. Visser, K. A. Heemstra, S. M. A. Swagemakers et al., “Physiological thyroid hormone levels regulate numerous skeletal muscle transcripts,” Journal of Clinical Endocrinology and Metabolism, vol. 94, no. 9, pp. 3487–3496, 2009. View at Publisher · View at Google Scholar · View at Scopus
  55. E. Silvestri, M. Moreno, L. Schiavo et al., “A proteomics approach to identify protein expression changes in rat liver following administration of 3,5,3-triiodo-L-thyronine,” Journal of Proteome Research, vol. 5, no. 9, pp. 2317–2327, 2006. View at Publisher · View at Google Scholar · View at Scopus
  56. E. Silvestri, L. Burrone, P. de Lange et al., “Thyroid-state influence on protein-expression profile of rat skeletal muscle,” Journal of Proteome Research, vol. 6, no. 8, pp. 3187–3196, 2007. View at Publisher · View at Google Scholar · View at Scopus
  57. M. Mann and O. N. Jensen, “Proteomic analysis of post-translational modifications,” Nature Biotechnology, vol. 21, no. 3, pp. 255–261, 2003. View at Publisher · View at Google Scholar · View at Scopus
  58. C. Schöneich, “Protein modification in aging: an update,” Experimental Gerontology, vol. 41, no. 9, pp. 807–812, 2006. View at Publisher · View at Google Scholar · View at Scopus
  59. J. V. Olsen, B. Blagoev, F. Gnad et al., “Global, in vivo, and site-specific phosphorylation dynamics in signaling networks,” Cell, vol. 127, no. 3, pp. 635–648, 2006. View at Publisher · View at Google Scholar · View at Scopus
  60. K. Ohtsubo and J. D. Marth, “Glycosylation in cellular mechanisms of health and disease,” Cell, vol. 126, no. 5, pp. 855–867, 2006. View at Publisher · View at Google Scholar · View at Scopus
  61. H. H. Freeze, “Genetic defects in the human glycome,” Nature Reviews Genetics, vol. 7, no. 8, pp. 660–674, 2006. View at Publisher · View at Google Scholar · View at Scopus
  62. N. A. Dencher, M. Frenzel, N. H. Reifschneider, M. Sugawa, and F. Krause, “Proteome alterations in rat mitochondria caused by aging,” Annals of the New York Academy of Sciences, vol. 1100, pp. 291–298, 2007. View at Publisher · View at Google Scholar · View at Scopus
  63. S. Rexroth, J. M. W. Meyer zu Tittingdorf, F. Krause, N. A. Dencher, and H. Seelert, “Thylakoid membrane at altered metabolic state: challenging the forgotten realms of the proteome,” Electrophoresis, vol. 24, no. 16, pp. 2814–2823, 2003. View at Publisher · View at Google Scholar · View at Scopus
  64. F. Krause, “Detection and analysis of protein-protein interactions in organellar and prokaryotic proteomes by native gel electrophoresis: (Membrane) protein complexes and supercomplexes,” Electrophoresis, vol. 27, no. 13, pp. 2759–2781, 2006. View at Publisher · View at Google Scholar · View at Scopus
  65. V. Pesce, A. Cormio, F. Fracasso et al., “Age-related mitochondrial genotypic and phenotypic alterations in human skeletal muscle,” Free Radical Biology and Medicine, vol. 30, no. 11, pp. 1223–1233, 2001. View at Publisher · View at Google Scholar · View at Scopus
  66. D. Dani and N. A. Dencher, “Native-DIGE: a new look at the mitochondrial membrane proteome,” Biotechnology Journal, vol. 3, no. 6, pp. 817–822, 2008. View at Publisher · View at Google Scholar · View at Scopus
  67. J. Chang, J. E. Cornell, H. Van Remmen, K. Hakala, W. F. Ward, and A. Richardson, “Effect of aging and caloric restriction on the mitochondrial proteome,” Journals of Gerontology A, vol. 62, no. 3, pp. 223–234, 2007. View at Google Scholar · View at Scopus
  68. K. O'Connell and K. Ohlendieck, “Proteomic DIGE analysis of the mitochondria-enriched fraction from aged rat skeletal muscle,” Proteomics, vol. 9, no. 24, pp. 5509–5524, 2009. View at Publisher · View at Google Scholar
  69. H. Schägger and K. Pfeiffer, “Supercomplexes in the respiratory chains of yeast and mammalian mitochondria,” The EMBO Journal, vol. 19, no. 8, pp. 1777–1783, 2000. View at Google Scholar · View at Scopus
  70. D. S. Cooper, “Subclinical hypothyroidism,” The New England Journal of Medicine, vol. 345, no. 4, pp. 260–265, 2001. View at Publisher · View at Google Scholar · View at Scopus
  71. N. Knudsen, P. Laurberg, L. B. Rasmussen et al., “Small differences in thyroid function may be important for body mass index and the occurrence of obesity in the population,” Journal of Clinical Endocrinology and Metabolism, vol. 90, no. 7, pp. 4019–4024, 2005. View at Publisher · View at Google Scholar · View at Scopus
  72. A. Oetting and P. M. Yen, “New insights into thyroid hormone action,” Best Practice and Research in Clinical Endocrinology and Metabolism, vol. 21, no. 2, pp. 193–208, 2007. View at Publisher · View at Google Scholar · View at Scopus
  73. D. Robyr, A. P. Wolffe, and W. Wahli, “Nuclear hormone receptor coregulators in action: diversity for shared tasks,” Molecular Endocrinology, vol. 14, no. 3, pp. 329–347, 2000. View at Publisher · View at Google Scholar · View at Scopus
  74. J. Zhang and M. A. Lazar, “The mechanism of action of thyroid hormones,” Annual Review of Physiology, vol. 62, pp. 439–466, 2000. View at Publisher · View at Google Scholar · View at Scopus
  75. F. Flamant, K. Gauthier, and J. Samarut, “Thyroid hormones signaling is getting more complex: STORMs are coming,” Molecular Endocrinology, vol. 21, no. 2, pp. 321–333, 2007. View at Publisher · View at Google Scholar · View at Scopus
  76. M. Busson, L. Daury, P. Seyer et al., “Avian MyoD and c-Jun coordinately induce transcriptional activity of the 3,5,3′-triiodothyronine nuclear receptor c-ErbAα1 in proliferating myoblasts,” Endocrinology, vol. 147, no. 7, pp. 3408–3418, 2006. View at Publisher · View at Google Scholar · View at Scopus
  77. C. Desbois, D. Aubert, C. Legrand, B. Pain, and J. Samarut, “A novel mechanism of action for v-ErbA: abrogation of the inactivation of transcription factor AP-1 by retinoic acid and thyroid hormone receptors,” Cell, vol. 67, no. 4, pp. 731–740, 1991. View at Google Scholar · View at Scopus
  78. L. Daury, M. Busson, F. Casas, I. Cassar-Malek, C. Wrutniak-Cabello, and G. Cabello, “The triiodothyronine nuclear receptor c-ErbAα1 inhibits avian MyoD transcriptional activity in myoblasts,” FEBS Letters, vol. 508, no. 2, pp. 236–240, 2001. View at Publisher · View at Google Scholar · View at Scopus
  79. M. A. Lazar, “Thyroid hormone receptors: multiple forms, multiple possibilities,” Endocrine Reviews, vol. 14, no. 2, pp. 184–193, 1993. View at Publisher · View at Google Scholar · View at Scopus
  80. G. A. Brent, “Mechanisms of disease: the molecular basis of thyroid hormone action,” The New England Journal of Medicine, vol. 331, no. 13, pp. 847–853, 1994. View at Publisher · View at Google Scholar · View at Scopus
  81. J. Sap, A. Munoz, and K. Damm, “The c-erb-A protein is a high-affinity receptor for thyroid hormone,” Nature, vol. 324, no. 6098, pp. 635–640, 1986. View at Google Scholar · View at Scopus
  82. E. D. Abel, E. G. Moura, R. S. Ahima et al., “Dominant inhibition of thyroid hormone action selectively in the pituitary of thyroid hormone-receptor-β null mice abolishes the regulation of thyrotropin by thyroid hormone,” Molecular Endocrinology, vol. 17, no. 9, pp. 1767–1776, 2003. View at Publisher · View at Google Scholar · View at Scopus
  83. J. Burnside, D. S. Sarling, F. E. Carr, and W. W. Chin, “Thyroid hormone regulation of the rat glycoprotein hormone α-subunit gene promoter activity,” The Journal of Biological Chemistry, vol. 264, no. 12, pp. 6886–6891, 1989. View at Google Scholar · View at Scopus
  84. D. L. Bodenner, M. A. Mroczynski, B. D. Weintraub, S. Radovick, and F. E. Wondisford, “A detailed functional and structural analysis of a major thyroid hormone inhibitory element in the human thyrotropin β-subunit gene,” The Journal of Biological Chemistry, vol. 266, no. 32, pp. 21666–21673, 1991. View at Google Scholar · View at Scopus
  85. D. Forrest and B. Vennström, “Functions of thyroid hormone receptors in mice,” Thyroid, vol. 10, no. 1, pp. 41–52, 2000. View at Google Scholar · View at Scopus
  86. A. Lanni, M. Moreno, A. Lombardi, P. De Lange, and F. Goglia, “Control of energy metabolism by iodothyronines,” Journal of Endocrinological Investigation, vol. 24, no. 11, pp. 897–913, 2001. View at Google Scholar · View at Scopus
  87. A. Lanni, M. Moreno, A. Lombardi, and F. Goglia, “Thyroid hormone and uncoupling proteins,” FEBS Letters, vol. 543, no. 1*#8211;3, pp. 5–10, 2003. View at Publisher · View at Google Scholar · View at Scopus
  88. E. Silvestri, L. Schiavo, A. Lombardi, and F. Goglia, “Thyroid hormones as molecular determinants of thermogenesis,” Acta Physiologica Scandinavica, vol. 184, no. 4, pp. 265–283, 2005. View at Publisher · View at Google Scholar · View at Scopus
  89. J. E. Silva, “Thermogenic mechanisms and their hormonal regulation,” Physiological Reviews, vol. 86, no. 2, pp. 435–464, 2006. View at Publisher · View at Google Scholar · View at Scopus
  90. F. Goglia, M. Moreno, and A. Lanni, “Action of thyroid hormones at the cellular level: the mitochondrial target,” FEBS Letters, vol. 452, no. 3, pp. 115–120, 1999. View at Publisher · View at Google Scholar · View at Scopus
  91. M. Gaspari, N.-G. Larsson, and C. M. Gustafsson, “The transcription machinery in mammalian mitochondria,” Biochimica et Biophysica Acta, vol. 1659, no. 2-3, pp. 148–152, 2004. View at Publisher · View at Google Scholar · View at Scopus
  92. R. C. Scarpulla, “Nuclear control of respiratory gene expression in mammalian cells,” Journal of Cellular Biochemistry, vol. 97, no. 4, pp. 673–683, 2006. View at Publisher · View at Google Scholar · View at Scopus
  93. C. Wrutniak-Cabello, F. Casas, and G. Cabello, “Thyroid hormone action in mitochondria,” Journal of Molecular Endocrinology, vol. 26, no. 1, pp. 67–77, 2001. View at Publisher · View at Google Scholar · View at Scopus
  94. A.-M. G. Psarra, S. Solakidi, and C. E. Sekeris, “The mitochondrion as a primary site of action of steroid and thyroid hormones: presence and action of steroid and thyroid hormone receptors in mitochondria of animal cells,” Molecular and Cellular Endocrinology, vol. 246, no. 1-2, pp. 21–33, 2006. View at Publisher · View at Google Scholar · View at Scopus
  95. C. Wrutniak, P. Rochard, F. Casas, A. Fraysse, J. Charrier, and G. Cabello, “Physiological importance of the T3 mitochondrial pathway,” Annals of the New York Academy of Sciences, vol. 839, pp. 93–100, 1998. View at Publisher · View at Google Scholar · View at Scopus
  96. C. H. Gouveia, J. J. Schultz, D. J. Jackson, G. R. Williams, and G. A. Brent, “Thyroid hormone gene targets in ROS 17/2.8 osteoblast like cells identified by differential display analysis,” Thyroid, vol. 12, no. 8, pp. 663–671, 2002. View at Google Scholar · View at Scopus
  97. T. Iglesias, J. Caubín, A. Zaballos, J. Bernal, and A. Munoz, “Identification of the mitochondrial NADH dehydrogenase subunit 3 (ND3) as a thyroid hormone regulated gene by whole genome PCR analysis,” Biochemical and Biophysical Research Communications, vol. 210, no. 3, pp. 995–1000, 1995. View at Publisher · View at Google Scholar · View at Scopus
  98. R. J. Wiesner, T. T. Kurowski, and R. Zak, “Regulation by thyroid hormone of nuclear and mitochondrial genes encoding subunits of cytochrome-c oxidase in rat liver and skeletal muscle,” Molecular Endocrinology, vol. 6, no. 9, pp. 1458–1467, 1992. View at Publisher · View at Google Scholar · View at Scopus
  99. Y. Hiroi, H.-H. Kim, H. Ying et al., “Rapid nongenomic actions of thyroid hormone,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 38, pp. 14104–14109, 2006. View at Publisher · View at Google Scholar · View at Scopus
  100. S.-Y. Cheng, J. L. Leonard, and P. J. Davis, “Molecular aspects of thyroid hormone actions,” Endocrine Reviews, vol. 31, no. 2, pp. 139–170, 2010. View at Publisher · View at Google Scholar
  101. A. J. Hulbert, “Thyroid hormones and their effects: a new perspective,” Biological Reviews of the Cambridge Philosophical Society, vol. 75, no. 4, pp. 519–631, 2000. View at Google Scholar · View at Scopus
  102. M. Moreno, P. de Lange, A. Lombardi, E. Silvestri, A. Lanni, and F. Goglia, “Metabolic effects of thyroid hormone derivatives,” Thyroid, vol. 18, no. 2, pp. 239–253, 2008. View at Publisher · View at Google Scholar · View at Scopus
  103. N. S. Kavok, O. A. Krasilnikova, and N. A. Babenko, “Thyroxine signal transduction in liver cells involves phospholipase C and phospholipase D activation. Genomic independent action of thyroid hormone,” BMC Cell Biology, vol. 2, article 5, 2001. View at Publisher · View at Google Scholar · View at Scopus
  104. X. Cao, F. Kambe, L. C. Moeller, S. Refetoff, and H. Seo, “Thyroid hormone induces rapid activation of Akt/protein kinase B-mammalian target of rapamycin-p70S6K cascade through phosphatidylinositol 3-kinase in human fibroblasts,” Molecular Endocrinology, vol. 19, no. 1, pp. 102–112, 2005. View at Publisher · View at Google Scholar · View at Scopus
  105. S. Seelig, C. Liaw, H. C. Towle, and J. H. Oppenheimer, “Thyroid hormone attenuates and augments hepatic gene expression at a pretranslational level,” Proceedings of the National Academy of Sciences of the United States of America, vol. 78, no. 8, pp. 4733–4737, 1981. View at Google Scholar · View at Scopus
  106. H. Dong, M. Wade, A. Williams, A. Lee, G. R. Douglas, and C. Yauk, “Molecular insight into the effects of hypothyroidism on the developing cerebellum,” Biochemical and Biophysical Research Communications, vol. 330, no. 4, pp. 1182–1193, 2005. View at Publisher · View at Google Scholar · View at Scopus
  107. H.-M. Zhang, Q. Su, and M. Luo, “Thyroid hormone regulates the expression of SNAP-25 during rat brain development,” Molecular and Cellular Biochemistry, vol. 307, no. 1-2, pp. 169–175, 2008. View at Publisher · View at Google Scholar · View at Scopus
  108. D. Diez, C. Grijota-Martinez, P. Agretti et al., “Thyroid hormone action in the adult brain: gene expression profiling of the effects of single and multiple doses of triiodo-L-thyronine in the rat striatum,” Endocrinology, vol. 149, no. 8, pp. 3989–4000, 2008. View at Publisher · View at Google Scholar · View at Scopus
  109. W. E. Visser, E. C. H. Friesema, J. Jansen, and T. J. Visser, “Thyroid hormone transport by monocarboxylate transporters,” Best Practice and Research in Clinical Endocrinology and Metabolism, vol. 21, no. 2, pp. 223–236, 2007. View at Publisher · View at Google Scholar · View at Scopus
  110. J. Li, V. Nguyen, B. A. French et al., “Mechanism of the alcohol cyclic pattern: role of the hypothalamic-pituitary-thyroid axis,” American Journal of Physiology, vol. 279, no. 1, pp. G118–G125, 2000. View at Google Scholar · View at Scopus
  111. T. Merkulova, A. Keller, P. Oliviero et al., “Thyroid hormones differentially modulate enolase isozymes during rat skeletal and cardiac muscle development,” American Journal of Physiology, vol. 278, no. 2, pp. E330–E339, 2000. View at Google Scholar · View at Scopus
  112. M. Nagao, B. Parimoo, and K. Tanaka, “Developmental, nutritional, and hormonal regulation of tissue-specific expression of the genes encoding various acyl-CoA dehydrogenases and α-subunit of electron transfer flavoprotein in rat,” The Journal of Biological Chemistry, vol. 268, no. 32, pp. 24114–24124, 1993. View at Google Scholar · View at Scopus
  113. D. A. Hood and A.-M. Joseph, “Mitochondrial assembly: protein import,” Proceedings of the Nutrition Society, vol. 63, no. 2, pp. 293–300, 2004. View at Publisher · View at Google Scholar · View at Scopus
  114. M. Sochor, P. McLean, J. Brown, and A. L. Greenbaum, “Regulation of pathways of ornithine metabolism. Effects of thyroid hormone and diabetes on the activity of enzymes at the “ornithine crossroads” in rat liver,” Enzyme, vol. 26, no. 1, pp. 15–23, 1981. View at Google Scholar · View at Scopus
  115. G. D. Dimitriadis, B. Leighton, M. Parry-Billings, D. West, and E. A. Newsholme, “Effect of hypothyroidism on the sensitivity of glycolysis and glycogen synthesis to insulin in the soleus muscle of the rat,” Biochemical Journal, vol. 257, no. 2, pp. 369–373, 1989. View at Google Scholar · View at Scopus
  116. S. Somara and K. N. Bitar, “Tropomyosin interacts with phosphorylated HSP27 in agonist-induced contraction of smooth muscle,” American Journal of Physiology, vol. 286, no. 6, pp. C1290–C1301, 2004. View at Publisher · View at Google Scholar · View at Scopus
  117. M. F. McCarty, “Induction of heat shock proteins may combat insulin resistance,” Medical Hypotheses, vol. 66, no. 3, pp. 527–534, 2006. View at Publisher · View at Google Scholar · View at Scopus