Nongenomic actions of thyroid hormone (original) (raw)

• Cheng, S. Y., Leonard, J. L. & Davis, P. J. Molecular aspects of thyroid hormone actions. Endocr. Rev. 31, 139–170 (2010).
  CAS PubMed PubMed Central Google Scholar
• Davis, P. J., Davis, F. B., Mousa, S. A., Luidens, M. K. & Lin, H. Y. Membrane receptor for thyroid hormone: physiologic and pharmacologic implications. Annu. Rev. Pharmacol. Toxicol. 51, 99–115 (2011).
  CAS PubMed Google Scholar
• Sterling, K., Brenner, M. A. & Sakurada, T. Rapid effect of triiodothyronine on the mitochondrial pathway in rat liver in vivo. Science 210, 340–342 (1980).
  CAS PubMed Google Scholar
• Siegrist-Kaiser, C. A., Juge-Aubry, C., Tranter, M. P., Ekenbarger, D. M. & Leonard, J. L. Thyroxine-dependent modulation of actin polymerization in cultured astrocytes. A novel, extranuclear action of thyroid hormone. J. Biol. Chem. 265, 5296–5302 (1990).
  CAS PubMed Google Scholar
• Mylotte, K. M. et al. Milrinone and thyroid hormone stimulate myocardial membrane Ca2+-ATPase activity and share structural homologies. Proc. Natl Acad. Sci. USA 82, 7974–7978 (1985).
  CAS PubMed PubMed Central Google Scholar
• Davis, P. J., Davis, F. B. & Lawrence, W. D. Thyroid hormone regulation of membrane Ca2+-ATPase activity. Endocr. Res. 15, 651–682 (1989).
  CAS PubMed Google Scholar
• Lin, H. Y. et al. Nongenomic regulation by thyroid hormone of plasma membrane ion and small molecule pumps. Discov. Med. 14, 199–206 (2012).
  PubMed Google Scholar
• Davis, F. B., Cody, V., Davis, P. J., Borzynski, L. J. & Blas, S. D. Stimulation by thyroid hormone analogues of red blood cell Ca2+-ATPase activity in vitro. Correlations between hormone structure and biological activity in a human cell system. J. Biol. Chem. 258, 12373–12377 (1983).
  CAS PubMed Google Scholar
• Nieman, L. K. et al. Effect of end-stage renal disease on responsiveness to calmodulin and thyroid hormone of calcium-ATPase in human red blood cells. Kidney Int. Suppl. 16, S167–S170 (1983).
  CAS PubMed Google Scholar
• Lei, J., Bhargava, M. & Ingbar, D. H. Cell-specific signal transduction pathways regulating Na+-K+-ATPase. Focus on 'short-term effects of thyroid hormones on the Na+-K+-ATPase activity of chick embryo hepatocytes during development: focus on signal transduction'. Am. J. Physiol. Cell Physiol. 296, C1–C3 (2009).
  CAS PubMed Google Scholar
• Lei, J., Mariash, C. N. & Ingbar, D. H. 3,3′,5-triiodo-l-thyronine up-regulation of Na,K-ATPase activity and cell surface expression in alveolar epithelial cells is Src kinase- and phosphoinositide 3-kinase-dependent. J. Biol. Chem. 279, 47589–47600 (2004).
  CAS PubMed Google Scholar
• Kahaly, G. J. & Dillmann, W. H. Thyroid hormone action in the heart. Endocr. Rev. 26, 704–728 (2005).
  CAS PubMed Google Scholar
• Lin, H. Y. et al. Potentiation by thyroid hormone of human IFN-γ-induced HLA-DR expression. J. Immunol. 161, 843–849 (1998).
  CAS PubMed Google Scholar
• Grasselli, E. et al. Non-receptor-mediated actions are responsible for the lipid-lowering effects of iodothyronines in FaO rat hepatoma cells. J. Endocrinol. 210, 59–69 (2011).
  CAS PubMed Google Scholar
• Lin, H. Y., Davis, F. B., Gordinier, J. K., Martino, L. J. & Davis, P. J. Thyroid hormone induces activation of mitogen-activated protein kinase in cultured cells. Am. J. Physiol. 276, C1014–C1024 (1999).
  CAS PubMed Google Scholar
• Lin, H. Y., Shih, A., Davis, F. B. & Davis, P. J. Thyroid hormone promotes the phosphorylation of STAT3 and potentiates the action of epidermal growth factor in cultured cells. Biochem. J. 338, 427–432 (1999).
  CAS PubMed PubMed Central Google Scholar
• Shih, A., Lin, H. Y., Davis, F. B. & Davis, P. J. Thyroid hormone promotes serine phosphorylation of p53 by mitogen-activated protein kinase. Biochemistry 40, 2870–2878 (2001).
  CAS PubMed Google Scholar
• Davis, F. B. et al. Proangiogenic action of thyroid hormone is fibroblast growth factor-dependent and is initiated at the cell surface. Circ. Res. 94, 1500–1506 (2004).
  CAS PubMed Google Scholar
• Cao, H. J., Lin, H. Y., Luidens, M. K., Davis, F. B. & Davis, P. J. Cytoplasm-to-nucleus shuttling of thyroid hormone receptor-β1 (Trβ1) is directed from a plasma membrane integrin receptor by thyroid hormone. Endocr. Res. 34, 31–42 (2009).
  PubMed Google Scholar
• Lin, H. Y. et al. L-thyroxine versus 3,5,3′-triiodo-l-thyronine and cell proliferation: activation of mitogen-activated protein kinase and phosphatidylinositol 3-kinase. Am. J. Physiol. Cell Physiol. 296, C980–C991 (2009).
  CAS PubMed Google Scholar
• Tang, H. Y., Lin, H. Y., Zhang, S., Davis, F. B. & Davis, P. J. Thyroid hormone causes mitogen-activated protein kinase-dependent phosphorylation of the nuclear estrogen receptor. Endocrinology 145, 3265–3272 (2004).
  CAS PubMed Google Scholar
• Hammes, S. R. & Davis, P. J. Overlapping nongenomic and genomic actions of thyroid hormone and steroids. Best Pract. Res. Clin. Endocrinol. Metab. 29, 581–593 (2015).
  CAS PubMed PubMed Central Google Scholar
• Bharali, D. J., Yalcin, M., Davis, P. J. & Mousa, S. A. Tetraiodothyroacetic acid-conjugated PLGA nanoparticles: a nanomedicine approach to treat drug-resistant breast cancer. Nanomed. (Lond.) 8, 1943–1954 (2013).
  CAS Google Scholar
• Bergh, J. J. et al. Integrin αVβ3 contains a cell surface receptor site for thyroid hormone that is linked to activation of mitogen-activated protein kinase and induction of angiogenesis. Endocrinology 146, 2864–2871 (2005).
  CAS PubMed Google Scholar
• Davis, P. J. et al. Cancer cell gene expression modulated from plasma membrane integrin αvβ3 by thyroid hormone and nanoparticulate tetrac. Front. Endocrinol. (Lausanne) 5, 240 (2014).
  Google Scholar
• Davis, P. J. et al. Corrigendum: 'cancer cell gene expression modulated from plasma membrane integrin αvβ3 by thyroid hormone and nanoparticulate tetrac'. Front. Endocrinol. (Lausanne) 6, 98 (2015).
  Google Scholar
• Lin, H. Y. et al. Nuclear monomeric integrin αv in cancer cells is a coactivator regulated by thyroid hormone. FASEB J. 27, 3209–3216 (2013).
  CAS PubMed Google Scholar
• Goolden, A. W., Gartside, J. M., Jackson, D. J. & Osorio, C. Uptake of 131I triiodothyronine by red cells. A diagnostic test of thyroid function. Lancet 2, 218–220 (1962).
  CAS PubMed Google Scholar
• Walfish, P. G., Britton, A., Volpe, R. & Ezrin, C. Experience with an in vitro test of thyroid function — the red blood cell uptake of l-triiodothyronine labelled with radioactive iodine. Can. Med. Assoc. J. 84, 637–641 (1961).
  CAS PubMed PubMed Central Google Scholar
• Kalyanaraman, H. et al. Nongenomic thyroid hormone signaling occurs through a plasma membrane-localized receptor. Sci. Signal. 7, ra48 (2014).
  PubMed PubMed Central Google Scholar
• Chen, Y. et al. Thyroid hormone enhances nitric oxide-mediated bacterial clearance and promotes survival after meningococcal infection. PLoS ONE 7, e41445 (2012).
  CAS PubMed PubMed Central Google Scholar
• Vié, M. P. et al. Purification, molecular cloning, and functional expression of the human nicodinamide-adenine dinucleotide phosphate-regulated thyroid hormone-binding protein. Mol. Endocrinol. 11, 1728–1736 (1997).
  PubMed Google Scholar
• Osty, J., Rappaport, L., Samuel, J. L. & Lennon, A. M. Characterization of a cytosolic triiodothyronine binding protein in atrium and ventricle of rat heart with different sensitivity toward thyroid hormone levels. Endocrinology 122, 1027–1033 (1988).
  CAS PubMed Google Scholar
• Nishii, Y. et al. Changes in cytosolic 3,5,3′-tri-iodo-l-thyronine (T3) binding activity during administration of L-thyroxine to thyroidectomized rats: cytosolic T3-binding protein and its activator act as intracellular regulators for nuclear T3 binding. J. Endocrinol. 123, 99–104 (1989).
  CAS PubMed Google Scholar
• Ashizawa, K. & Cheng, S. Y. Regulation of thyroid hormone receptor-mediated transcription by a cytosol protein. Proc. Natl Acad. Sci. USA 89, 9277–9281 (1992).
  CAS PubMed PubMed Central Google Scholar
• Takeshige, K. et al. Cytosolic T3-binding protein modulates dynamic alteration of T3-mediated gene expression in cells. Endocr. J. 61, 561–570 (2014).
  CAS PubMed Google Scholar
• Fanjul, A. N. & Farias, R. N. Cold-sensitive cytosolic 3,5,3′-triiodo-l-thyronine-binding protein and pyruvate kinase from human erythrocytes share similar regulatory properties of hormone binding by glycolytic intermediates. J. Biol. Chem. 268, 175–179 (1993).
  CAS PubMed Google Scholar
• Hallen, A., Cooper, A. J., Jamie, J. F. & Karuso, P. Insights into enzyme catalysis and thyroid hormone regulation of cerebral ketimine reductase/mu-crystallin under physiological conditions. Neurochem. Res. 40, 1252–1266 (2015).
  CAS PubMed Google Scholar
• Plow, E. F., Haas, T. A., Zhang, L., Loftus, J. & Smith, J. W. Ligand binding to integrins. J. Biol. Chem. 275, 21785–21788 (2000).
  CAS PubMed Google Scholar
• Lin, H. Y. et al. Identification and functions of the plasma membrane receptor for thyroid hormone analogues. Discov. Med. 11, 337–347 (2011).
  PubMed Google Scholar
• Cody, V., Davis, P. J. & Davis, F. B. Molecular modeling of the thyroid hormone interactions with αvβ3 integrin. Steroids 72, 165–170 (2007).
  CAS PubMed Google Scholar
• Hoffman, S. J. et al. Rapid inhibition of thyroxine-induced bone resorption in the rat by an orally active vitronectin receptor antagonist. J. Pharmacol. Exp. Ther. 302, 205–211 (2002).
  CAS PubMed Google Scholar
• Lin, H. Y. et al. Pharmacodynamic modeling of anti-cancer activity of tetraiodothyroacetic acid in a perfused cell culture system. PLoS Comput. Biol. 7, e1001073 (2011).
  CAS PubMed PubMed Central Google Scholar
• Liu, X., Zheng, N., Shi, Y. N., Yuan, J. & Li, L. Thyroid hormone induced angiogenesis through the integrin αvβ3/protein kinase D/histone deacetylase 5 signaling pathway. J. Mol. Endocrinol. 52, 245–254 (2014).
  CAS PubMed Google Scholar
• D'Arezzo, S. et al. Rapid nongenomic effects of 3,5,3′-triiodo-l-thyronine on the intracellular pH of L-6 myoblasts are mediated by intracellular calcium mobilization and kinase pathways. Endocrinology 145, 5694–5703 (2004).
  CAS PubMed Google Scholar
• Lei, J., Mariash, C. N., Bhargava, M., Wattenberg, E. V. & Ingbar, D. H. T3 increases Na-K-ATPase activity via a MAPK/ERK1/2-dependent pathway in rat adult alveolar epithelial cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 294, L749–L754 (2008).
  CAS PubMed Google Scholar
• Yonkers, M. A. & Ribera, A. B. Sensory neuron sodium current requires nongenomic actions of thyroid hormone during development. J. Neurophysiol. 100, 2719–2725 (2008).
  PubMed PubMed Central Google Scholar
• Yonkers, M. A. & Ribera, A. B. Molecular components underlying nongenomic thyroid hormone signaling in embryonic zebrafish neurons. Neural Dev. 4, 20 (2009).
  PubMed PubMed Central Google Scholar
• Cao, J. H. et al. L-thyroxine attenuates pyramidal neuron excitability in rat acute prefrontal cortex slices. Immunol. Endocr. Metab. Agents Med. Chem. 11, 152–156 (2011).
  CAS Google Scholar
• Carvalho, F. A. et al. Atomic force microscopy-based molecular recognition of a fibrinogen receptor on human erythrocytes. ACS Nano 4, 4609–4620 (2010).
  CAS PubMed Google Scholar
• Odievre, M. H. et al. Modulation of erythroid adhesion receptor expression by hydroxyurea in children with sickle cell disease. Haematologica 93, 502–510 (2008).
  CAS PubMed Google Scholar
• Zanatta, A. P., Zanatta, L., Goncalves, R., Zamoner, A. & Silva, F. R. Integrin participates in the effect of thyroxine on plasma membrane in immature rat testis. Biochim. Biophys. Acta 1830, 2629–2637 (2013).
  CAS PubMed Google Scholar
• Scarlett, A. et al. Thyroid hormone stimulation of extracellular signal-regulated kinase and cell proliferation in human osteoblast-like cells is initiated at integrin αVβ3. J. Endocrinol. 196, 509–517 (2008).
  CAS PubMed Google Scholar
• Cayrol, F. et al. Integrin αvβ3 acting as membrane receptor for thyroid hormones mediates angiogenesis in malignant T cells. Blood 125, 841–851 (2015).
  CAS PubMed PubMed Central Google Scholar
• Barbakadze, T., Natsvlishvili, N. & Mikeladze, D. Thyroid hormones differentially regulate phosphorylation of ERK and Akt via integrin αvβ3 receptor in undifferentiated and differentiated PC-12 cells. Cell Biochem. Funct. 32, 282–286 (2014).
  CAS PubMed Google Scholar
• Schmohl, K. A. et al. Thyroid hormones and tetrac: new regulators of tumour stroma formation via integrin αvβ3. Endocr. Relat. Cancer 22, 941–952 (2015).
  CAS PubMed Google Scholar
• Zvibel, I., Atias, D., Phillips, A., Halpern, Z. & Oren, R. Thyroid hormones induce activation of rat hepatic stellate cells through increased expression of p75 neurotrophin receptor and direct activation of Rho. Lab. Invest. 90, 674–684 (2010).
  CAS PubMed Google Scholar
• Dekkers, B. G. et al. L-thyroxine promotes a proliferative airway smooth muscle phenotype in the presence of TGF-β1. Am. J. Physiol. Lung Cell. Mol. Physiol. 308, L301–L306 (2015).
  CAS PubMed Google Scholar
• Stenzel, D., Wilsch-Brauninger, M., Wong, F. K., Heuer, H. & Huttner, W. B. Integrin αvβ3 and thyroid hormones promote expansion of progenitors in embryonic neocortex. Development 141, 795–806 (2014).
  CAS PubMed Google Scholar
• Mousa, S. A., O'Connor, L., Davis, F. B. & Davis, P. J. Proangiogenesis action of the thyroid hormone analog 3,5-diiodothyropropionic acid (DITPA) is initiated at the cell surface and is integrin mediated. Endocrinology 147, 1602–1607 (2006).
  CAS PubMed Google Scholar
• Mousa, S. A. et al. The proangiogenic action of thyroid hormone analogue GC-1 is initiated at an integrin. J. Cardiovasc. Pharmacol. 46, 356–360 (2005).
  CAS PubMed Google Scholar
• Mousa, S. S., Davis, F. B., Davis, P. J. & Mousa, S. A. Human platelet aggregation and degranulation is induced in vitro by l-thyroxine, but not by 3,5,3′-triiodo-l-thyronine or diiodothyropropionic acid (DITPA). Clin. Appl. Thromb. Hemost. 16, 288–293 (2010).
  PubMed Google Scholar
• Horacek, J. et al. Prothrombotic changes due to an increase in thyroid hormone levels. Eur. J. Endocrinol. 172, 537–542 (2015).
  CAS PubMed Google Scholar
• Yalcin, M. et al. Tetraiodothyroacetic acid (tetrac) and nanoparticulate tetrac arrest growth of medullary carcinoma of the thyroid. J. Clin. Endocrinol. Metab. 95, 1972–1980 (2010).
  CAS PubMed Google Scholar
• Glinskii, A. B. et al. Modification of survival pathway gene expression in human breast cancer cells by tetraiodothyroacetic acid (tetrac). Cell Cycle 8, 3562–3570 (2009).
  CAS PubMed Google Scholar
• Mousa, S. A. et al. Tetraiodothyroacetic acid and its nanoformulation inhibit thyroid hormone stimulation of non-small cell lung cancer cells in vitro and its growth in xenografts. Lung Cancer 76, 39–45 (2012).
  PubMed Google Scholar
• Yalcin, M. et al. Response of human pancreatic cancer cell xenografts to tetraiodothyroacetic acid nanoparticles. Horm. Cancer 4, 176–185 (2013).
  CAS PubMed Google Scholar
• Yalcin, M. et al. Tetraidothyroacetic acid (tetrac) and tetrac nanoparticles inhibit growth of human renal cell carcinoma xenografts. Anticancer Res. 29, 3825–3831 (2009).
  CAS PubMed Google Scholar
• Yoshida, T., Gong, J., Xu, Z., Wei, Y. & Duh, E. J. Inhibition of pathological retinal angiogenesis by the integrin αvβ3 antagonist tetraiodothyroacetic acid (tetrac). Exp. Eye Res. 94, 41–48 (2012).
  CAS PubMed Google Scholar
• Freindorf, M. et al. Combined QM/MM study of thyroid and steroid hormone analogue interactions with αvβ3 integrin. J. Biomed. Biotechnol. 2012, 959057 (2012).
  PubMed PubMed Central Google Scholar
• Yalcin, M. et al. Tetraiodothyroacetic acid and tetraiodothyroacetic acid nanoparticle effectively inhibit the growth of human follicular thyroid cell carcinoma. Thyroid 20, 281–286 (2010).
  CAS PubMed Google Scholar
• Meng, R. et al. Crosstalk between integrin αvβ3 and estrogen receptor-α is involved in thyroid hormone-induced proliferation in human lung carcinoma cells. PLoS ONE 6, e27547 (2011).
  CAS PubMed PubMed Central Google Scholar
• Schweizer, U., Johannes, J., Bayer, D. & Braun, D. Structure and function of thyroid hormone plasma membrane transporters. Eur. Thyroid J. 3, 143–153 (2014).
  CAS PubMed PubMed Central Google Scholar
• Visser, W. E., Friesema, E. C. & Visser, T. J. Minireview: thyroid hormone transporters: the knowns and the unknowns. Mol. Endocrinol. 25, 1–14 (2011).
  CAS PubMed PubMed Central Google Scholar
• Fu, J., Refetoff, S. & Dumitrescu, A. M. Inherited defects of thyroid hormone-cell-membrane transport: review of recent findings. Curr. Opin. Endocrinol. Diabetes Obes. 20, 434–440 (2013).
  CAS PubMed PubMed Central Google Scholar
• Bianco, A. C., Salvatore, D., Gereben, B., Berry, M. J. & Larsen, P. R. Biochemistry, cellular and molecular biology, and physiological roles of the iodothyronine selenodeiodinases. Endocr. Rev. 23, 38–89 (2002).
  CAS PubMed Google Scholar
• Horn, S. & Heuer, H. Thyroid hormone action during brain development: more questions than answers. Mol. Cell. Endocrinol. 315, 19–26 (2010).
  CAS PubMed Google Scholar
• Schroeder, A. C. & Privalsky, M. L. Thyroid hormones, T3 and T4, in the brain. Front. Endocrinol. (Lausanne) 5, 40 (2014).
  Google Scholar
• Morte, B. & Bernal, J. Thyroid hormone action: astrocyte–neuron communication. Front. Endocrinol. (Lausanne) 5, 82 (2014).
  Google Scholar
• Leonard, J. L. Regulation of T3 production in the brain. Acta Med. Austriaca 19 (Suppl. 1), 5–8 (1992).
  PubMed Google Scholar
• Visser, T. J. Pathways of thyroid hormone metabolism. Acta Med. Austriaca 23, 10–16 (1996).
  CAS PubMed Google Scholar
• Kuiper, G. G., Kester, M. H., Peeters, R. P. & Visser, T. J. Biochemical mechanisms of thyroid hormone deiodination. Thyroid 15, 787–798 (2005).
  CAS PubMed Google Scholar
• Farwell, A. P., Lynch, R. M., Okulicz, W. C., Comi, A. M. & Leonard, J. L. The actin cytoskeleton mediates the hormonally regulated translocation of type II iodothyronine 5′-deiodinase in astrocytes. J. Biol. Chem. 265, 18546–18553 (1990).
  CAS PubMed Google Scholar
• Farwell, A. P. & Leonard, J. L. in Recent Research Developments in Neuroendocrinology — Thyroid Hormone and Brain Maturation (ed. Hendrich, C. E.) 113–130 (Research Signpost, 1997).
  Google Scholar
• Faivre-Sarrailh, C. & Rabie, A. Developmental study of factors controlling microtubule in vitro cold-stability in rat cerebrum. Brain Res. 470, 199–204 (1988).
  CAS PubMed Google Scholar
• Farwell, A. P., Dubord-Tomasetti, S. A., Pietrzykowski, A. Z. & Leonard, J. L. Dynamic nongenomic actions of thyroid hormone in the developing rat brain. Endocrinology 147, 2567–2574 (2006).
  CAS PubMed Google Scholar
• Venstrom, K. A. & Reichardt, L. F. Extracellular matrix 2: role of extracellular matrix molecules and their receptors in the nervous system. FASEB J. 7, 996–1003 (1993).
  CAS PubMed Google Scholar
• Liesi, P. Extracellular matrix and neuronal movement. Experientia 46, 900–907 (1990).
  CAS PubMed Google Scholar
• Liesi, P. & Silver, J. Is astrocyte laminin involved in axon guidance in the mammalian CNS? Dev. Biol. 130, 774–785 (1988).
  CAS PubMed Google Scholar
• Liesi, P. Laminin-immunoreactive glia distinguish regenerative adult CNS systems from non-regenerative ones. EMBO J. 4, 2505–2511 (1985).
  CAS PubMed PubMed Central Google Scholar
• Hager, G., Dodt, H. U., Zieglgänsberger, W. & Liesi, P. Novel forms of neuronal migration in the rat cerebellum. J. Neurosci. Res. 40, 207–219 (1995).
  CAS PubMed Google Scholar
• Farwell, A. P. & Dubord-Tomasetti, S. A. Thyroid hormone regulates the expression of laminin in the developing rat cerebellum. Endocrinology 140, 4221–4227 (1999).
  CAS PubMed Google Scholar
• Ruoslahti, E. Integrins. J. Clin. Invest. 87, 1–5 (1991).
  CAS PubMed PubMed Central Google Scholar
• Hynes, R. O. Integrin: versitility, modulation, and signaling in cell adhesion. Cell 69, 11–25 (1992).
  CAS PubMed Google Scholar
• Maartens, A. P. & Brown, N. H. Anchors and signals: the diverse roles of integrins in development. Curr. Top. Dev. Biol. 112, 233–272 (2015).
  CAS PubMed Google Scholar
• Farwell, A. P., Tranter, M. P. & Leonard, J. L. Thyroxine-dependent regulation of integrin–laminin interactions in astrocytes. Endocrinology 136, 3909–3915 (1995).
  CAS PubMed Google Scholar
• Farwell, A. P. & Dubord, S. A. Thyroid hormone regulates neurite outgrowth and neuronal migration onto laminin. Thyroid 6, S-27 (1996).
  Google Scholar
• Farwell, A. P. & Dubord-Tomasetti, S. A. Thyroid hormone regulates the extracellular organization of laminin on astrocytes. Endocrinology 140, 5014–5021 (1999).
  CAS PubMed Google Scholar
• Dodd, J. & Jessel, T. M. Axon guidance and the patterning of neuronal projections in vertebrates. Science 242, 692–699 (1988).
  CAS PubMed Google Scholar
• Tessier-Lavigne, M. & Goodman, C. S. The molecular biology of axon guidance. Science 274, 1123–1133 (1996).
  CAS PubMed Google Scholar
• McKerracher, L., Chamoux, M. & Arregui, C. O. Role of laminin and integrin interactions in growth cone guidance. Mol. Neurobiol. 12, 95–116 (1996).
  CAS PubMed Google Scholar
• Schmidt, C. E., Dai, J., Lauffenburger, D. A., Sheetz, M. P. & Horwitz, A. F. Integrin–cytoskeletal interactions in neuronal growth cones. J. Neurosci. 15, 3400–3407 (1995).
  CAS PubMed PubMed Central Google Scholar
• Farwell, A. P., Dubord-Tomasetti, S. A., Pietrzykowski, A. Z., Stachelek, S. J. & Leonard, J. L. Regulation of cerebellar neuronal migration and neurite outgrowth by thyroxine and 3,3′,5′-triiodothyronine. Brain Res. Dev. Brain Res. 154, 121–135 (2005).
  CAS PubMed Google Scholar
• Safran, M., Farwell, A., Rokos, H. & Leonard, J. Structural requirements of iodothyronines for the rapid inactivation and internalization of type II iodothyronine 5′-deiodinase in glial cells. J. Biol. Chem. 268, 14224–14229 (1993).
  CAS PubMed Google Scholar
• Chassande, O. et al. Identification of transcripts initiated from an internal promoter in the c-erbAα locus that encode inhibitors of retinoic acid receptor-α and triiodothyronine receptor activities. Mol. Endocrinol. 11, 1278–1290 (1997).
  CAS PubMed Google Scholar
• Ribeiro, R. C. et al. X-ray crystallographic and functional studies of thyroid hormone receptor. J. Steroid Biochem. Mol. Biol. 65, 133–141 (1998).
  CAS PubMed Google Scholar
• Wagner, R. L. et al. A structural role for hormone in the thyroid hormone receptor. Nature 378, 690–697 (1995).
  CAS PubMed Google Scholar
• Wagner, R. L. et al. Hormone selectivity in thyroid hormone receptors. Mol. Endocrinol. 15, 398–410 (2001).
  CAS PubMed Google Scholar
• Furuya, F. et al. Nuclear receptor corepressor is a novel regulator of phosphatidylinositol 3-kinase signaling. Mol. Cell. Biol. 27, 6116–6126 (2007).
  CAS PubMed PubMed Central Google Scholar
• Lu, C., Willingham, M. C., Furuya, F. & Cheng, S. Y. Activation of phosphatidylinositol 3-kinase signaling promotes aberrant pituitary growth in a mouse model of thyroid-stimulating hormone-secreting pituitary tumors. Endocrinology 149, 3339–3345 (2008).
  CAS PubMed PubMed Central Google Scholar
• Fozzatti, L., Lu, C., Kim, D. W. & Cheng, S. Y. Differential recruitment of nuclear coregulators directs the isoform-dependent action of mutant thyroid hormone receptors. Mol. Endocrinol. 25, 908–921 (2011).
  CAS PubMed PubMed Central Google Scholar
• Hanna, S. & El-Sibai, M. Signaling networks of Rho GTPases in cell motility. Cell. Signal. 25, 1955–1961 (2013).
  CAS PubMed Google Scholar
• Cao, X., Kambe, F., Moeller, L. C., Refetoff, S. & Seo, H. Thyroid hormone induces rapid activation of Akt/protein kinase B-mammalian target of rapamycin-p70S6K cascade through phosphatidylinositol 3-kinase in human fibroblasts. Mol. Endocrinol. 19, 102–112 (2005).
  CAS PubMed Google Scholar
• Verga Falzacappa, C. et al. Thyroid hormone receptor TRβ1 mediates Akt activation by T3 in pancreatic β cells. J. Mol. Endocrinol. 38, 221–233 (2007).
  PubMed Google Scholar
• Martin, N. P. et al. A rapid cytoplasmic mechanism for PI3 kinase regulation by the nuclear thyroid hormone receptor, TRβ, and genetic evidence for its role in the maturation of mouse hippocampal synapses in vivo. Endocrinology 155, 3713–3724 (2014).
  PubMed PubMed Central Google Scholar
• Hiroi, Y. et al. Rapid nongenomic actions of thyroid hormone. Proc. Natl Acad. Sci. USA 103, 14104–14109 (2006).
  CAS PubMed PubMed Central Google Scholar
• Magnus-Levy, A. Uber den respiratorischen Gaswechechsel unter dem Einfluss der Thyroidea sowie unter verschiedenen pathologischen Zustanden. Berlin Klinische Wochenschrift 32, 650–652 (1895).
  Google Scholar
• Yehuda-Shnaidman, E., Kalderon, B. & Bar-Tana, J. Thyroid hormone, thyromimetics, and metabolic efficiency. Endocr. Rev. 35, 35–58 (2014).
  CAS PubMed Google Scholar
• Cioffi, F., Senese, R., Lanni, A. & Goglia, F. Thyroid hormones and mitochondria: with a brief look at derivatives and analogues. Mol. Cell. Endocrinol. 379, 51–61 (2013).
  CAS PubMed Google Scholar
• Weitzel, J. M. & Iwen, K. A. Coordination of mitochondrial biogenesis by thyroid hormone. Mol. Cell. Endocrinol. 342, 1–7 (2011).
  CAS PubMed Google Scholar
• Sterling, K. & Milch, P. O. Thyroid hormone binding by a component of mitochondrial membrane. Proc. Natl Acad. Sci. USA 72, 3225–3229 (1975).
  CAS PubMed PubMed Central Google Scholar
• Goglia, F., Torresani, J., Bugli, P., Barletta, A. & Liverini, G. In vitro binding of triiodothyronine to rat liver mitochondria. Pflugers Arch. 390, 120–124 (1981).
  CAS PubMed Google Scholar
• Morel, G., Ricard-Blum, S. & Ardail, D. Kinetics of internalization and subcellular binding sites for T3 in mouse liver. Biol. Cell 86, 167–174 (1996).
  CAS PubMed Google Scholar
• Wrutniak, C. et al. A 43-kDa protein related to c-Erb A α1 is located in the mitochondrial matrix of rat liver. J. Biol. Chem. 270, 16347–16354 (1995).
  CAS PubMed Google Scholar
• Wrutniak-Cabello, C., Casas, F. & Cabello, G. Thyroid hormone action in mitochondria. J. Mol. Endocrinol. 26, 67–77 (2001).
  CAS PubMed Google Scholar
• Casas, F. et al. A variant form of the nuclear triiodothyronine receptor c-Erb A α1 plays a direct role in regulation of mitochondrial RNA synthesis. Mol. Cell. Biol. 19, 7913–7924 (1999).
  CAS PubMed PubMed Central Google Scholar
• Pessemesse, L. et al. p28, a truncated form of TRα1 regulates mitochondrial physiology. FEBS Lett. 588, 4037–4043 (2014).
  CAS PubMed Google Scholar
• Horst, C., Rokos, H. & Seitz, H. J. Rapid stimulation of hepatic oxygen consumption by 3,5-di-iodo-l-thyronine. Biochem. J. 261, 945–950 (1989).
  CAS PubMed PubMed Central Google Scholar
• Tata, J. R., Ernster, L. & Lindberg, O. Control of basal metabolic rate by thyroid hormones and cellular function. Nature 193, 1058–1060 (1962).
  CAS PubMed Google Scholar
• Moreno, M., Lanni, A., Lombardi, A. & Goglia, F. How the thyroid controls metabolism in the rat: different roles for triiodothyronine and diiodothyronines. J. Physiol. 505, 529–538 (1997).
  CAS PubMed PubMed Central Google Scholar
• Tata, J. R. Inhibition of the biological action of thyroid hormones by actinomycin D and puromycin. Nature 197, 1167–1168 (1963).
  CAS PubMed Google Scholar
• Lombardi, A. et al. 3,5-diiodo-l-thyronine activates brown adipose tissue thermogenesis in hypothyroid rats. PLoS ONE 10, e0116498 (2015).
  PubMed PubMed Central Google Scholar
• Padron, A. S. et al. Administration of 3,5-diiodothyronine (3,5-T2) causes central hypothyroidism and stimulates thyroid-sensitive tissues. J. Endocrinol. 221, 415–427 (2014).
  CAS PubMed PubMed Central Google Scholar
• Goglia, F., Lanni, A., Horst, C., Moreno, M. & Thoma, R. In vitro binding of 3,5-di-iodo-l-thyronine to rat liver mitochondria. J. Mol. Endocrinol. 13, 275–282 (1994).
  CAS PubMed Google Scholar
• Arnold, S., Goglia, F. & Kadenbach, B. 3,5-diiodothyronine binds to subunit Va of cytochrome-c oxidase and abolishes the allosteric inhibition of respiration by ATP. Eur. J. Biochem. 252, 325–330 (1998).
  CAS PubMed Google Scholar
• Navarrete-Ramirez, P., Luna, M., Valverde, R. C. & Orozco, A. 3,5-di-iodothyronine stimulates tilapia growth through an alternate isoform of thyroid hormone receptor β1. J. Mol. Endocrinol. 52, 1–9 (2014).
  CAS PubMed Google Scholar
• Lanni, A. et al. 3,5-diiodo-l-thyronine powerfully reduces adiposity in rats by increasing the burning of fats. FASEB J. 19, 1552–1554 (2005).
  CAS PubMed Google Scholar
• Moreno, M. et al. 3,5-diiodo-l-thyronine prevents high-fat-diet-induced insulin resistance in rat skeletal muscle through metabolic and structural adaptations. FASEB J. 25, 3312–3324 (2011).
  CAS PubMed Google Scholar
• de Lange, P. et al. Nonthyrotoxic prevention of diet-induced insulin resistance by 3,5-diiodo-l-thyronine in rats. Diabetes 60, 2730–2739 (2011).
  CAS PubMed PubMed Central Google Scholar
• Singh, B. K. et al. FoxO1 deacetylation regulates thyroid hormone-induced transcription of key hepatic gluconeogenic genes. J. Biol. Chem. 288, 30365–30372 (2013).
  CAS PubMed PubMed Central Google Scholar
• Shang, G. et al. 3,5-diiodo-l-thyronine ameliorates diabetic nephropathy in streptozotocin-induced diabetic rats. Biochim. Biophys. Acta 1832, 674–684 (2013).
  CAS PubMed Google Scholar
• Jonas, W. et al. 3,5-diiodo-l-thyronine (3,5-T2) exerts thyromimetic effects on hypothalamus–pituitary–thyroid axis, body composition, and energy metabolism in male diet-induced obese mice. Endocrinology 156, 389–399 (2015).
  PubMed Google Scholar
• Goldberg, I. J. et al. Thyroid hormone reduces cholesterol via a non-LDL receptor-mediated pathway. Endocrinology 153, 5143–5149 (2012).
  CAS PubMed PubMed Central Google Scholar
• Luidens, M. K., Mousa, S. A., Davis, F. B., Lin, H. Y. & Davis, P. J. Thyroid hormone and angiogenesis. Vascul. Pharmacol. 52, 142–145 (2010).
  CAS PubMed Google Scholar
• Bogaard, H. J. et al. Severe pulmonary hypertension: the role of metabolic and endocrine disorders. Pulm. Circ. 2, 148–154 (2012).
  PubMed PubMed Central Google Scholar
• Al Husseini, A. et al. Thyroid hormone is highly permissive in angioproliferative pulmonary hypertension in rats. Eur. Respir. J. 41, 104–114 (2013).
  CAS PubMed Google Scholar
• Lin, H. Y., Glinsky, G. V., Mousa, S. A. & Davis, P. J. Thyroid hormone and anti-apoptosis in tumor cells. Oncotarget 6, 14735–14743 (2015).
  PubMed PubMed Central Google Scholar
• Mousa, S. A. et al. Modulation of angiogenesis by thyroid hormone and hormone analogues: implications for cancer management. Angiogenesis 17, 463–469 (2014).
  CAS PubMed Google Scholar
• Cohen, K. et al. Thyroid hormone regulates adhesion, migration and matrix metalloproteinase 9 activity via αvβ3 integrin in myeloma cells. Oncotarget 5, 6312–6322 (2014).
  PubMed PubMed Central Google Scholar
• Cohen, K. et al. Relevance of the thyroid hormones–αvβ3 pathway in primary myeloma bone marrow cells and to bortezomib action. Leuk. Lymphoma 56, 1107–1114 (2015).
  CAS PubMed Google Scholar
• Davis, P. J., Hercbergs, A., Luidens, M. K. & Lin, H. Y. Recurrence of differentiated thyroid carcinoma during full TSH suppression: is the tumor now thyroid hormone dependent? Horm. Cancer 6, 7–12 (2015).
  CAS PubMed Google Scholar
• Lin, H. Y. et al. The pro-apoptotic action of stilbene-induced COX-2 in cancer cells: convergence with the anti-apoptotic effect of thyroid hormone. Cell Cycle 8, 1877–1882 (2009).
  CAS PubMed Google Scholar
• Rudinger, A., Mylotte, K. M., Davis, P. J., Davis, F. B. & Blas, S. D. Rabbit myocardial membrane Ca2+-adenosine triphosphatase activity: stimulation in vitro by thyroid hormone. Arch. Biochem. Biophys. 229, 379–385 (1984).
  CAS PubMed Google Scholar
• Zinman, T., Shneyvays, V., Tribulova, N., Manoach, M. & Shainberg, A. Acute, nongenomic effect of thyroid hormones in preventing calcium overload in newborn rat cardiocytes. J. Cell. Physiol. 207, 220–231 (2006).
  CAS PubMed Google Scholar
• Forini, F. et al. Triiodothyronine prevents cardiac ischemia/reperfusion mitochondrial impairment and cell loss by regulating miR30a/p53 axis. Endocrinology 155, 4581–4590 (2014).
  PubMed Google Scholar
• Bertrand, C. et al. Mice lacking the p43 mitochondrial T3 receptor become glucose intolerant and insulin resistant during aging. PLoS ONE 8, e75111 (2013).
  CAS PubMed PubMed Central Google Scholar
• Cohen, K. et al. Relevance of the thyroid hormones–αvβ3 pathway in primary myeloma bone marrow cells and to bortezomib action. Leuk. Lymphoma 56, 1107–1114 (2014).
  PubMed Google Scholar
• Gnoni, G. V. et al. 3,5,3′triiodo-l-thyronine induces SREBP-1 expression by non-genomic actions in human HEP G2 cells. J. Cell. Physiol. 227, 2388–2397 (2012).
  CAS PubMed Google Scholar