Thyroid Hormones as Modulators of Immune Activities at the Cellular Level
Abstract
BACKGROUND: Increasing evidence suggests that thyroid hormones, L-thyroxine (T(4)) and 3,3',5-triiodo-L-thyronine (T(3)), are modulators of the immune response. In monocytes, macrophages, leukocytes, natural killer cells, and lymphocytes, a wide range of immune functions such as chemotaxis, phagocytosis, generation of reactive oxygen species (ROS), and cytokine synthesis and release are altered under hypo- and hyperthyroid conditions. SUMMARY: Hyperthyroidism decreases the proinflammatory activities of monocytes and macrophages, whereas enhancement of phagocytosis and increased levels of ROS may occur during hypothyroidism. The expression of proinflammatory molecules such as macrophage inflammatory protein-1α and interleukin-1β increases in hypothyroidism. However, in Kupffer cells, proinflammatory activities such as the respiratory burst, nitric oxide synthase activity, and tumor necrosis factor-α expression may result from increased T(3) levels. Thyroid hormones also affect natural killer cell activity and cell-mediated immune responses. Still, for many immune cells no clear correlation has been found so far between abnormally high or low T(3) or T(4) levels and the effects observed on the immune responses. CONCLUSIONS: In this review we outline the contributions of thyroid hormones to different aspects of innate and adaptive immune responses. The relationship between thyroid hormones and immune cells is complex and T(3) and T(4) may modulate immune responses through both genomic and nongenomic mechanisms. Future studies of the molecular signaling mechanisms involved in this cross-talk between thyroid hormones and the immune system may support development of new strategies to improve clinical immune responses.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Thyroid hormones can bind to integrin αvβ3 to switch on a cascade of signaling events through MAPK, phospholipase C, proteinkinase Cα, ERK1/2, and/or hypoxia-inducible factor-1, leading to enhanced cytokine and growth factor action and angiogenesis.
“Thyroid hormones can bind to the integrin αvβ3 to switch on a cascade of signaling events through MAPK, phospholipase C, proteinkinase Cα, ERK1/2, and/or hypoxia-inducible factor-1, leading to enhanced cytokine and growth factor action and angiogenesis [128].”
From Interaction of the endocrine system with inflammation: a function of energy and volume regulation (2014) · cites this paper as [128]
Thyroid hormones induce oxygen radical production in neutrophils, IFN-γ-stimulated major histocompatibility complex class II expression, IL-6, IL-8, and IL-12 secretion from different cell types, lymphocyte proliferation, IFN-γ-stimulated natural killer cell activity, and superoxide anion production in human alveolar neutrophils and macrophages.
“Thyroid hormones induce oxygen radical production in neutrophils [128], IFN-γ-stimulated major histocompatibility complex class II expression [128], IL-6, IL-8, and IL-12 secretion from different cell types [128], lymphocyte proliferation [128], IFN-γ-stimulated natural killer cell activity [128], and superoxide anion production in human alveolar neutrophils and macrophages [129].”
From Interaction of the endocrine system with inflammation: a function of energy and volume regulation (2014) · cites this paper as [128]
Cites
Stress and disorders of the stress system
Chrousos, G. P. (2009) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2009.106 · Cited by 3,215 · see citing works
Antigen presentation and T cell stimulation by dendritic cells.
Guermonprez, P., Valladeau, J., Zitvogel, L., Théry, C., & Amigorena, S. (2002) · Annual Review of Immunology · doi:10.1146/annurev.immunol.20.100301.064828 · Cited by 2,106 · see citing works
Immune-neuro-endocrine interactions: facts and hypotheses.
BESEDOVSKY, H. O., & REY, A. D. (1996) · Endocrine Reviews · doi:10.1210/edrv-17-1-64 · Cited by 1,564 · see citing works
Nuclear Hormone Receptors and Gene Expression
Aranda, A., & Pascual, A. (2001) · Physiological Reviews · doi:10.1152/physrev.2001.81.3.1269 · Cited by 1,562 · see citing works
Molecular Aspects of Thyroid Hormone Actions
Cheng, S.-Y., Leonard, J. L., & Davis, P. J. (2010) · Endocrine Reviews · doi:10.1210/er.2009-0007 · Cited by 1,384 · see citing works
Self-citationIL-6, RANKL, TNF-alpha/IL-1: interrelations in bone resorption pathophysiology
Tat, S. K., Marc, P., Théoleyre, S., Heymann, D., & Fortun, Y. (2004) · Cytokine & Growth Factor Reviews · doi:10.1016/j.cytogfr.2003.10.005 · Cited by 959 · see citing works
The endocrine function of adipose tissue: an update
Ronti, T., Lupattelli, G., & Mannarino, E. (2006) · Clinical Endocrinology · doi:10.1111/j.1365-2265.2006.02474.x · Cited by 906 · see citing works
The syntax of immune-neuroendocrine communication
Blalock, J. E. (1994) · Immunology Today · doi:10.1016/0167-5699(94)90205-4 · Cited by 717 · see citing works
Effects of stress on the immune system
Khansari, D. N., Murgo, A. J., & Faith, R. E. (1990) · Immunology Today · doi:10.1016/0167-5699(90)90069-l · Cited by 664 · see citing works
The mononuclear phagocyte system
Hume, D. A. (2005) · Current Opinion in Immunology · doi:10.1016/j.coi.2005.11.008 · Cited by 655 · see citing works
Adhesion mechanisms regulating the migration of monocytes
Imhof, B. A., & Aurrand‐Lions, M. (2004) · Nature reviews. Immunology · doi:10.1038/nri1375 · Cited by 584 · see citing works
Bergh, J. J., Lin, H., Lansing, L., Mohamed, S. N., Davis, F. B., Mousa, S. A., & Davis, P. J. (2005) · Endocrinology · doi:10.1210/en.2005-0102 · Cited by 563 · see citing works
Self-citationMatarese, G., Moschos, S., & Mantzoros, C. S. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.174.6.3137 · Cited by 559 · see citing works
Redox signaling in macrophages.
Forman, H., & Torres, M. (2001) · Molecular Aspects of Medicine · doi:10.1016/s0098-2997(01)00010-3 · Cited by 539 · see citing works
Role of Kupffer cells in the pathogenesis of liver disease
Kolios, G. (2006) · World Journal of Gastroenterology · doi:10.3748/wjg.v12.i46.7413 · Cited by 505 · see citing works
Exercise and the immune system: a model of the stress response?
Hoffman-Goetz, L., & Pedersen, B. K. (1994) · Immunology Today · doi:10.1016/0167-5699(94)90177-5 · Cited by 481 · see citing works
The nervous system and innate immunity: the neuropeptide connection
Brogden, K. A., Guthmiller, J. M., Salzet, M., & ZASLOFF, M. A. (2005) · Nature Immunology · doi:10.1038/ni1209 · Cited by 445 · see citing works
Haddad, J. J., Saadé, N. E., & Safieh‐Garabedian, B. (2002) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(02)00357-0 · Cited by 416 · see citing works
Mechanisms of thyroid hormone receptor-specific nuclear and extra nuclear actions
Bassett, J. H. D., Harvey, C. B., & Williams, G. R. (2003) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2003.10.033 · Cited by 392 · see citing works
Weber, J. T., Slemmer, J. E., Shacka, J. J., & Sweeney, M. I. (2008) · Current Medicinal Chemistry · doi:10.2174/092986708783497337 · Cited by 386 · see citing works
Thyroid hormone-induced oxidative stress
Venditti, P., & Meo, S. D. (2006) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-005-5457-9 · Cited by 379 · see citing works
Dorshkind, K. A., & Horseman, N. D. (2000) · Endocrine Reviews · doi:10.1210/edrv.21.3.0397 · Cited by 370 · see citing works
Dorshkind, K. (2000) · Endocrine Reviews · doi:10.1210/er.21.3.292 · Cited by 370 · see citing works
Wrona, D. (2006) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2005.10.017 · Cited by 322 · see citing works
Nongenomic Actions of Thyroid Hormone
DAVIS, P. J., & Davis, F. B. (1996) · Thyroid · doi:10.1089/thy.1996.6.497 · Cited by 260 · see citing works
Self-citationLin, H., Sun, M., Tang, H.-Y., Lin, C., Luidens, M. K., Mousa, S. A., Incerpi, S., Drusano, G. L., Davis, F. B., & Davis, P. J. (2009) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00305.2008 · Cited by 255 · see citing works
Self-citationThyroid hormone induces activation of mitogen-activated protein kinase in cultured cells
Lin, H., Davis, F. B., Gordinier, J., Martino, L. J., & Davis, P. J. (1999) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.1999.276.5.c1014 · Cited by 238 · see citing works
Self-citationNongenomic Actions of Thyroid Hormone on the Heart
Davis, P. J., & Davis, F. B. (2002) · Thyroid · doi:10.1089/105072502760143827 · Cited by 223 · see citing works
Self-citationDavis, P. J., Shih, A., Lin, H., Martino, L. J., & Davis, F. B. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m002560200 · Cited by 220 · see citing works
Self-citationImmune-neuro-endocrine interactions: facts and hypotheses
Besedovsky, H. O. (1996) · Endocrine Reviews · doi:10.1210/er.17.1.64 · Cited by 194 · see citing works
NK and NKT cell functions in immunosenescence
Mocchegiani, E., & Malavolta, M. (2004) · Aging Cell · doi:10.1111/j.1474-9728.2004.00107.x · Cited by 192 · see citing works
Thyroid hormone transporters in health and disease
Jansen, J., Friesema, E. C. H., Milici, C., & Visser, T. J. (2005) · Thyroid · doi:10.1089/thy.2005.15.757 · Cited by 181 · see citing works
Stress — mechanisms of immunosuppression
Dohms, J. E., & Metz, A. L. (1991) · Veterinary Immunology and Immunopathology · doi:10.1016/0165-2427(91)90011-z · Cited by 181 · see citing works
Membrane receptors mediating thyroid hormone action
Davis, P. J., Davis, F. B., & Cody, V. (2005) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2005.09.007 · Cited by 178 · see citing works
Self-citationMastorakos, G. P., & Pavlatou, M. G. (2005) · Hormone and Metabolic Research · doi:10.1055/s-2005-870426 · Cited by 151 · see citing works
Immune-neuroendocrine interactions
Savino, W., & Dardenne, M. (1995) · Immunology Today · doi:10.1016/0167-5699(95)80144-8 · Cited by 147 · see citing works
Krüger, K., & Mooren, F. C. (2026) · PubMed · doi:10.22029/eir.2007.1629 · Cited by 137 · see citing works
Klecha, A. J., Genaro, A. M., Gorelik, G. J., Arcos, M. L. B., Silberman, D. M., Schuman, M. L., García, S. I., Pirola, C. J., & Cremaschi, G. (2006) · Journal of Endocrinology · doi:10.1677/joe.1.06137 · Cited by 136 · see citing works
Moeller, L. C., Cao, X., Dumitrescu, A. M., Seo, H., & Refetoff, S. (2006) · Nuclear Receptor Signaling · doi:10.1621/nrs.04020 · Cited by 133 · see citing works
Retinoic acids inhibit activation-induced apoptosis in T cell hybridomas and thymocytes
Iwata, M., Mukai, M., Nakai, Y., et al. (1992) · The Journal of Immunology · doi:10.4049/jimmunol.149.10.3302 · Cited by 126 · see citing works
D’Arezzo, S., Incerpi, S., Davis, F. B., Acconcia, F., Marino, M., Farı́as, R. N., & Davis, P. J. (2004) · Endocrinology · doi:10.1210/en.2004-0890 · Cited by 126 · see citing works
Self-citationThe Immune System as a Regulator of Thyroid Hormone Activity
Klein, J. R. (2006) · Experimental Biology and Medicine · doi:10.1177/153537020623100301 · Cited by 121 · see citing works
Immunodepression in thyroid-deprived animals.
Fabris, Ν. (1973) · PubMed · Cited by 119 · see citing works
Immune-Endocrine Interactions in Autoimmune Thyroid Diseases
Klecha, A. J., Arcos, M. L. B., Frick, L. R., Genaro, A. M., & Cremaschi, G. (2008) · NeuroImmunoModulation · doi:10.1159/000135626 · Cited by 118 · see citing works
The role of atrial natriuretic peptide in the immune system
Vollmar, A. M. (2005) · Peptides · doi:10.1016/j.peptides.2004.08.034 · Cited by 116 · see citing works
Ghrelin and immunity: A young player in an old field
Dixit, V. D., & Taub, D. D. (2005) · Experimental Gerontology · doi:10.1016/j.exger.2005.09.003 · Cited by 115 · see citing works
Thyroid Hormone Receptor-Dependent Transcriptional Regulation of Fibrinogen and Coagulation Proteins
Shih, C., Chen, S. L., Yen, C.-C., Huang, Y., Chen, C.-D., Lee, Y., & Lin, K. (2004) · Endocrinology · doi:10.1210/en.2003-1372 · Cited by 114 · see citing works
Chen, Y., Kobayashi, S., Chen, J., Redetzke, R. A., Said, S., Liang, Q., & Gerdes, A. M. (2007) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2007.09.009 · Cited by 109 · see citing works
Biology and clinical impact of human natural killer cells
Farag, S. S., VanDeusen, J. B., Fehniger, T. A., & Caligiuri, M. A. (2003) · International Journal of Hematology · doi:10.1007/bf02983234 · Cited by 109 · see citing works
Molecular modeling of the thyroid hormone interactions with αvβ3 integrin
Cody, V., Davis, P. J., & Davis, F. B. (2006) · Steroids · doi:10.1016/j.steroids.2006.11.008 · Cited by 106 · see citing works
Self-citationCerri, C., CHIMENTI, D., Conti, I., et al. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.177.3.1975 · Cited by 103 · see citing works
Pituitary-Thyroid Axis and Immune System: A Reciprocal Neuroendocrine-lmmune Interaction
Fabris, N., Mocchegiani, E., & Provinciali, M. (2008) · Hormone Research · doi:10.1159/000184234 · Cited by 95 · see citing works
Hodkinson, C., Simpson, E. E. A., Beattie, J. H., O’Connor, J. M., Campbell, D. J., Strain, J., & Wallace, J. M. W. (2009) · Journal of Endocrinology · doi:10.1677/joe-08-0488 · Cited by 95 · see citing works
Thyroid function and aging: gender-related differences
da Costa, V. C., Moreira, D., & Rosenthal, D. (2001) · Journal of Endocrinology · doi:10.1677/joe.0.1710193 · Cited by 93 · see citing works
Tri-iodothyronine stimulates rat osteoclastic bone resorption by an indirect effect
Allain, T., Chambers, T. J., Flanagan, A. M., & McGregor, A. M. (1992) · Journal of Endocrinology · doi:10.1677/joe.0.1330327 · Cited by 90 · see citing works
Control of dendritic cell maturation and function by triiodothyronine
Mascanfroni, I. D., Montesinos, M. M., Susperreguy, S., Cervi, L., Ilarregui, J. M., Ramseyer, V. D., Masini-Repiso, A. M., Targovnik, H. M., Rabinovich, G. A., & Pellizas, C. G. (2007) · The FASEB Journal · doi:10.1096/fj.07-8652com · Cited by 88 · see citing works
Klecha, A. J., Genaro, A. M., LYSIONEK, A. E., Caro, R. A., Coluccia, A., & Cremaschi, G. (2000) · International Journal of Immunopharmacology · doi:10.1016/s0192-0561(00)00012-6 · Cited by 87 · see citing works
Effects of Thyroid Hormones on Apoptotic Cell Death of Human Lymphocytes1
Mihara, S., Suzuki, N., Wakisaka, S., Suzuki, S. O., Sekita, N., Yamamoto, S., Saito, N., Hoshino, T., & Sakane, T. (1999) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.84.4.5598 · Cited by 87 · see citing works
Calzà, L., Fernández, M., & Giardino, L. (2009) · Journal of Molecular Endocrinology · doi:10.1677/jme-09-0067 · Cited by 87 · see citing works
Lania, A., Persani, L., & Beck-Peccoz, P. (2008) · Pituitary · doi:10.1007/s11102-008-0122-6 · Cited by 85 · see citing works
Davis, P. J., Davis, F. B., Lin, H., et al. (2009) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00480.2009 · Cited by 83 · see citing works
Self-citationThyroid-stimulating hormone pituitary adenomas
Clarke, M. J., Erickson, D. Z., Castro, M. R., & Atkinson, J. L. D. (2008) · Journal of neurosurgery · doi:10.3171/jns/2008/109/7/0017 · Cited by 82 · see citing works
Incerpi, S., Luly, P., Vito, P. D., & Farı́as, R. N. (1999) · Endocrinology · doi:10.1210/endo.140.2.6535 · Cited by 81 · see citing works
Self-citationCatecholamines: Physiological Immunomodulators During Health and Illness
Oberbeck, R. (2006) · Current Medicinal Chemistry · doi:10.2174/092986706777584997 · Cited by 80 · see citing works
Díez, D., Grijota-Martínez, C., Agretti, P., Marco, G. D., Tonacchera, M., Pinchera, A., de Escobar, G. M., Bernal, J., & Morte, B. (2008) · Endocrinology · doi:10.1210/en.2008-0350 · Cited by 79 · see citing works
Circulating Cells with Osteogenic Potential
Khosla, S., & Eghbali-Fatourechi, G. Z. (2006) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1346.022 · Cited by 78 · see citing works
Siddiqi, A., Burrin, J., Wood, D. F., & Monson, J. (1998) · Journal of Endocrinology · doi:10.1677/joe.0.1570453 · Cited by 77 · see citing works
Ortega, E., Forner, M. A., & Barriga, C. (1997) · The Journal of Physiology · doi:10.1113/jphysiol.1997.sp021897 · Cited by 73 · see citing works
Natural Killer Cell Immune Responses
Yokoyama, W. M. (2005) · Immunologic Research · doi:10.1385/ir:32:1-3:317 · Cited by 71 · see citing works
Dual Mechanisms of Apoptosis Induction by Cytotoxic Lymphocytes
Trapani, J. A. (1998) · International review of cytology · doi:10.1016/s0074-7696(08)62169-5 · Cited by 69 · see citing works
Volpe, R. J. (2001) · Current Pharmaceutical Design · doi:10.2174/1381612013397898 · Cited by 66 · see citing works
Tapia, G., Fernández, V., Varela, P., Cornejo, P., Guerrero, J., & Videla, L. A. (2003) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(03)00209-0 · Cited by 63 · see citing works
Rahaman, S. O., Ghosh, S., Mohanakumar, K. P., et al. (2001) · Neuroscience Research · doi:10.1016/s0168-0102(01)00237-1 · Cited by 63 · see citing works
Lin, H., Thacorf, H. R., Davis, F. B., & Davis, P. J. (1996) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.1996.271.4.c1256 · Cited by 63 · see citing works
Self-citationZamoner, A., Barreto, K. P., Filho, D. W., et al. (2007) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2007.01.005 · Cited by 62 · see citing works
Foster, M. P., Jensen, E. R., Montecino‐Rodriguez, E., Leathers, H., Horseman, N. D., & Dorshkind, K. A. (2000) · Clinical Immunology · doi:10.1006/clim.2000.4889 · Cited by 62 · see citing works
Immunological and hematological changes in patients with hyperthyroidism or hypothyroidism
Jafarzadeh, A., Poorgholami, M., Izadi, N., et al. (2010) · Clinical and investigative medicine · doi:10.25011/cim.v33i5.14352 · Cited by 61 · see citing works
Sarkar, M., Varshney, R. K., Chopra, M., Sekhri, T., Adhikari, J. S., & Dwarakanath, B. S. R. (2005) · Cytometry Part B Clinical Cytometry · doi:10.1002/cyto.b.20082 · Cited by 60 · see citing works
Mezősi, E., Szabó, J., Nagy, E. V., Borbely, A., Varga, E., Paragh, G., & Varga, Z. (2005) · Journal of Endocrinology · doi:10.1677/joe.1.05968 · Cited by 59 · see citing works
Kavok, N. S., Krasilnikova, O. A., & Babenko, N. A. (2001) · BMC Cell Biology · doi:10.1186/1471-2121-2-5 · Cited by 57 · see citing works
Frick, L. R., Rapanelli, M., Bussmann, U. A., Klecha, A. J., Arcos, M. L. B., Genaro, A. M., & Cremaschi, G. A. (2009) · Biological Psychiatry · doi:10.1016/j.biopsych.2008.12.013 · Cited by 55 · see citing works
The thyrotropin-releasing hormone (TRH)–immune system homeostatic hypothesis
Kamath, J., Yarbrough, G. G., Prange, A. J., & Winokur, A. (2008) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2008.09.004 · Cited by 51 · see citing works
Recovery of spleen cell natural killer activity by thyroid hormone treatment in old mice.
Provinciali, M., Muzzioli, M., Stefano, G. D., et al. (1991) · PubMed · Cited by 51 · see citing works
Mascanfroni, I. D., Montesinos, M. M., Alamino, V. A., et al. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.071241 · Cited by 50 · see citing works
Regulation of Tissue Iodothyronine Deiodinase Activity in a Model of Prolonged Critical Illness
Debaveye, Y., Ellger, B., Mebis, L., Darras, V. M., & Van den Berghe, G. (2008) · Thyroid · doi:10.1089/thy.2007.0287 · Cited by 50 · see citing works
Arcos, M. L. B., Sterle, H., Paulazo, M. A., Valli, E., Klecha, A. J., Issé, B. A., Pellizas, C. G., Farı́as, R. N., & Cremaschi, G. (2011) · Journal of Cellular Physiology · doi:10.1002/jcp.22681 · Cited by 50 · see citing works
Suppression of Cell-Mediated Immunity in Hypothyroidism
Schoenfeld, P., Myers, J. W., MYERS, L., et al. (1995) · Southern Medical Journal · doi:10.1097/00007611-199503000-00019 · Cited by 49 · see citing works
Stimulating effect of triiodothyronine on cell-mediated immunity
Bal�zs, C., Levey, A. S., Szab�, M., et al. (1980) · European Journal of Clinical Pharmacology · doi:10.1007/bf00561672 · Cited by 49 · see citing works
Arcos, M. L. B., Gorelik, G. J., Klecha, A. J., Genaro, A. M., & Cremaschi, G. (2006) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00316.2005 · Cited by 45 · see citing works
Pállinger, É., & Csaba, G. (2007) · Immunology · doi:10.1111/j.1365-2567.2007.02731.x · Cited by 43 · see citing works
Effects of Thyroid Hormones on Apoptotic Cell Death of Human Lymphocytes
Mihara, S. (1999) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.84.4.1378 · Cited by 43 · see citing works
Fernández, V., & Videla, L. A. (1995) · Free Radical Biology and Medicine · doi:10.1016/0891-5849(95)00016-q · Cited by 42 · see citing works
Magsino, C. H., Hamouda, W., Ghanim, H., Browne, R. W., Aljada, A., & Dandona, P. (2000) · Metabolism · doi:10.1053/meta.2000.6263 · Cited by 42 · see citing works
Hoffman, S. J., Vasko-Moser, J. A., Miller, W. H., Lark, M. W., Gowen, M., & Stroup, G. B. (2002) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.302.1.205 · Cited by 42 · see citing works
Thyrotropic hormone (TSH) regulation of triiodothyronine (T3) concentration in immune cells
Csaba, G., & Pállinger, É. (2009) · Inflammation Research · doi:10.1007/s00011-008-8076-8 · Cited by 41 · see citing works
Chatterjee, S., & Chandel, A. S. (1983) · European Journal of Endocrinology · doi:10.1530/acta.0.1030095 · Cited by 40 · see citing works
Kim, C. H., Kim, H. K., Shong, Y. K., et al. (1999) · Journal of Endocrinology · doi:10.1677/joe.0.1600097 · Cited by 40 · see citing works
Exercise-induced stimulation of murine macrophage phagocytosis may be mediated by thyroxine
Forner, M. A., Barriga, C., & Ortega, E. (1996) · Journal of Applied Physiology · doi:10.1152/jappl.1996.80.3.899 · Cited by 39 · see citing works
The Effects of Hyperthyroidism on Experimental Autoimmune Thyroiditis in the Rat*
HASSMAN, R., Weetman, A. P., Gunn, C., et al. (1985) · Endocrinology · doi:10.1210/endo-116-4-1253 · Cited by 38 · see citing works
The Effect of the Thyroidal State on the Immunological State of the Chicken
Yam, D., Heller, D. E., & Snapir, N. (1981) · Developmental & Comparative Immunology · doi:10.1016/s0145-305x(81)80060-2 · Cited by 38 · see citing works
Negative Regulation of Superoxide Dismutase-1 Promoter by Thyroid Hormone
Santos, G. M., Afonso, V., Barra, G. B., Togashi, M., Webb, P., Neves, F. D. A. R., Lomri, N., & Lomri, A. (2006) · Molecular Pharmacology · doi:10.1124/mol.106.025627 · Cited by 38 · see citing works
Effect of hypo‐ and hyperthyroidism on the function and metabolism of macrophages in rats
Rosa, L. F. B. P. C., Safi, D. A., & Curi, R. (1995) · Cell Biochemistry and Function · doi:10.1002/cbf.290130211 · Cited by 37 · see citing works
Thyroxine Administration Prevents Streptococcal Cell Wall-Induced Inflammatory Responses
Rittenhouse, P. A., & Redei, E. E. (1997) · Endocrinology · doi:10.1210/endo.138.4.5045 · Cited by 37 · see citing works
Wall, J. R., TWOHIG, P., & Chartier, B. (1981) · Journal of Endocrinology · doi:10.1677/joe.0.0910061 · Cited by 37 · see citing works
Modulation of lymphoid cell sensitivity to interferon by thyroid hormones
Provinciali, M., & Fabris, Ν. (1990) · Journal of Endocrinological Investigation · doi:10.1007/bf03349536 · Cited by 37 · see citing works
Effect of hypo- and hyperthyroidism on the balance between helper and suppressor T cells in rats
Pacini, F., Nakamura, H., & DeGroot, L. J. (1983) · European Journal of Endocrinology · doi:10.1530/acta.0.1030528 · Cited by 36 · see citing works
Forner, M. A., Collazos, M. E., Barriga, C., la Fuente, M. D., Rodríguez, A. B., & Ortega, E. (1994) · Mechanisms of Ageing and Development · doi:10.1016/0047-6374(94)90008-6 · Cited by 35 · see citing works
Videla, L. A., Correa, L. A., Rivera, M., & Sir, T. (1993) · Free Radical Biology and Medicine · doi:10.1016/0891-5849(93)90149-o · Cited by 35 · see citing works
Natural Killer Activity and Thyroid Hormone Levels in Young and Elderly Persons
Kmieć, Z., Myśliwska, J. M., Rachoń, D., Kotlarz, G., Sworczak, K., & Myśliwski, A. (2001) · Gerontology · doi:10.1159/000052813 · Cited by 34 · see citing works
Immunomodulation of peripheral lymphocytes by hormones of the hypothalamus-pituitary-thyroid axis
Kruger, T. E. (1996) · Advances in Neuroimmunology · doi:10.1016/s0960-5428(97)00033-2 · Cited by 32 · see citing works
Fernández, V., Tapia, G., Varela, P., et al. (2005) · Free Radical Research · doi:10.1080/10715760400029637 · Cited by 31 · see citing works
Marino, F., Guasti, L., Cosentino, M., Piazza, D. D., Simoni, C., Piantanida, E., Cimpanelli, M., Klersy, C., Bartalena, L., Venco, A., et al. (2005) · Life Sciences · doi:10.1016/j.lfs.2005.06.016 · Cited by 31 · see citing works
Thyroid hormone calorigenesis and mitochondrial redox signaling: upregulation of gene expression
Luis, A. (2006) · Frontiers in bioscience · doi:10.2741/2140 · Cited by 29 · see citing works
Tumor necrosis factor inhibitors for the treatment of asthma
Kim, J., & Remick, D. G. (2007) · Current Allergy and Asthma Reports · doi:10.1007/s11882-007-0013-3 · Cited by 29 · see citing works
Nandakumar, D. N., Koner, B. C., Vinayagamoorthi, R., et al. (2007) · Immunobiology · doi:10.1016/j.imbio.2007.10.005 · Cited by 29 · see citing works
Enhancement of mouse natural killer cell activity by thyroxine
Sharma, S., Tsai, V., & Proffitt, M. R. (1982) · Cellular Immunology · doi:10.1016/0008-8749(82)90437-3 · Cited by 29 · see citing works
Fas/FasL mediated apoptosis of thyrocytes in Graves' disease
Sera, N., Kawakami, A., Nakashima, T., et al. (2001) · Clinical & Experimental Immunology · doi:10.1046/j.1365-2249.2001.01476.x · Cited by 28 · see citing works
A Neuroendocrine-Immune Theory of Aging
Fabris, N. (1990) · International Journal of Neuroscience · doi:10.3109/00207459008999749 · Cited by 28 · see citing works
Short-term effects of thyroid hormones during development: Focus on signal transduction
Scapin, S., Leoni, S., Spagnuolo, S., Gnocchi, D., Vito, P. D., Luly, P., Pedersen, J. Z., & Incerpi, S. (2009) · Steroids · doi:10.1016/j.steroids.2009.10.013 · Cited by 28 · see citing works
Self-citationFeed-back interactions between immunological cells and the hypothalamus-pituitary-adrenal axis.
Besedovsky, H. O., & del Rey, A. (1991) · PubMed · Cited by 28 · see citing works
Haddad, E. E., & Mashaly, M. M. (1991) · Developmental & Comparative Immunology · doi:10.1016/0145-305x(91)90048-4 · Cited by 27 · see citing works
A Novel Pathway That Regulates Inflammatory Disease in the Respiratory Tract
Niu, N., Goff, M. K. L., Li, F., Rahman, M., Homer, R., & Cohn, L. E. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.178.6.3846 · Cited by 26 · see citing works
Wei, L., Lu, J., Li, F., Long, D., Shan, J., Li, S., & Li, Y. (2010) · Life Sciences · doi:10.1016/j.lfs.2010.05.012 · Cited by 26 · see citing works
Thyroid hormone potentiates the antiviral action of interferon-gamma in cultured human cells.
Lin, H., Thacore, H. R., Davis, P. J., et al. (1994) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.79.1.8027254 · Cited by 26 · see citing works
Self-citationRecovery of age‐dependent immunological deterioration in old mice by thyroxine treatment
El-Shaikh, K. A., Gabry, M. S. I., & Othman, G. A. (2006) · Journal of Animal Physiology and Animal Nutrition · doi:10.1111/j.1439-0396.2005.00602.x · Cited by 26 · see citing works
Szabó, J., Fóris, G., Mezősi, E., Nagy, E., Paragh, G., Sztojka, I., & Leovey, A. (2009) · Experimental and Clinical Endocrinology & Diabetes · doi:10.1055/s-0029-1211440 · Cited by 25 · see citing works
Alteration of lymphocyte reactivities by thyroid hormones
Ong, M., Malkin, D. G., & Malkin, A. (1986) · International Journal of Immunopharmacology · doi:10.1016/0192-0561(86)90012-3 · Cited by 25 · see citing works
Schaefer, J. S., & Klein, J. R. (2010) · The FASEB Journal · doi:10.1096/fj.10-168203 · Cited by 25 · see citing works
Endocytosing the death sentence
Griffiths, G. M. (2003) · The Journal of Cell Biology · doi:10.1083/jcb.200212143 · Cited by 25 · see citing works
Ortego, E., Forner, M. A., García, J. J., Rodríguez, A. B., & Barriga, C. (1999) · Molecular and Cellular Biochemistry · doi:10.1023/a:1007020804138 · Cited by 23 · see citing works
Effect of thyroxine on antioxidant defense system in the liver of rats of different age
Saičić, Z. S., Mijalkovic, D., Nikolić, A. L., et al. (2006) · Physiological Research · doi:10.33549/physiolres.930789 · Cited by 22 · see citing works
The effect of tri-iodothyronine on the phytohaemagglutinin response of T lymphocytes.
Keast, D. H., & Taylor, K. (1982) · PubMed · Cited by 22 · see citing works
Vinayagamoorthi, R., Koner, B. C., Kavitha, S. K., et al. (2005) · Cellular Immunology · doi:10.1016/j.cellimm.2006.01.002 · Cited by 21 · see citing works
Tri-iodothyronine differentially induces Kupffer cell ED1/ED2 subpopulations
Gomes, L. F., Lorente, S., Simon, K., Areco, K. C. N., Araújo-Peres, C., & Videla, L. A. (2004) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2004.02.018 · Cited by 19 · see citing works
Csaba, G., Kovacs, P. L., & Pállinger, É. (2005) · Life Sciences · doi:10.1016/j.lfs.2004.07.031 · Cited by 19 · see citing works
Blount, B. C., & Duncan, M. W. (1997) · Analytical Biochemistry · doi:10.1006/abio.1996.9900 · Cited by 19 · see citing works
Ohashi, H., & Itoh, M. (1994) · PubMed · Cited by 19 · see citing works
How antithyroid drugs work in Graves' disease
Weetman, A. P. (1992) · Clinical Endocrinology · doi:10.1111/j.1365-2265.1992.tb02330.x · Cited by 18 · see citing works
Williamson, R. A., Davison, T. F., & Payne, L. N. (1990) · Developmental & Comparative Immunology · doi:10.1016/0145-305x(90)90021-6 · Cited by 18 · see citing works
Pietrzak, M., & Puzianowska‐Kuźnicka, M. (2008) · Journal of Molecular Endocrinology · doi:10.1677/jme-08-0010 · Cited by 18 · see citing works
Nishizawa, Y., Fushiki, S., Amakata, Y., et al. (1998) · PubMed · Cited by 18 · see citing works
Repressed activity of peritoneal macrophages in methimazole-induced hypothyroid mice
Liu, W., Tsui, K. W., & WONG, C. C. (1993) · Virchows Archiv B Cell Pathology Including Molecular Pathology · doi:10.1007/bf02899252 · Cited by 17 · see citing works
Chandratilleke, D., Hala, K., & Marsh, J. A. (1996) · International Journal of Immunopharmacology · doi:10.1016/0192-0561(96)00010-0 · Cited by 16 · see citing works
Caleb, B. L., Hardenbrook, M. A., Cherington, V., & Castellot, J. J. (1996) · Journal of Cellular Physiology · doi:10.1002/(sici)1097-4652(199605)167:2 · Cited by 16 · see citing works
Dw, C., Jd, S., & Ja, D. (1978) · PubMed · Cited by 16 · see citing works
Ribeiro-Carvalho, M. M., Smaniotto, S., Neves-dos-Santos, S., et al. (2007) · Scandinavian Journal of Immunology · doi:10.1111/j.1365-3083.2007.01910.x · Cited by 15 · see citing works
Ingram, K. G., Crouch, D. A., Douez, D. L., et al. (1995) · International Journal of Immunopharmacology · doi:10.1016/0192-0561(94)00079-4 · Cited by 14 · see citing works
Thyroid hormone potentiates the antiviral action of interferon-gamma in cultured human cells
Lin, H. (1994) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.79.1.62 · Cited by 14 · see citing works
Polymorphonuclear Leucocyte Function in Hypothyroidism
Farid, N. R., Au, B., Woodford, G. A., et al. (2008) · Hormone Research · doi:10.1159/000178735 · Cited by 13 · see citing works
Antibody responses in hyperthyroid rats
Bittencourt, C. S., Azzolini, A. E. C. S., Ferreira, D. A., et al. (2007) · International Immunopharmacology · doi:10.1016/j.intimp.2007.02.016 · Cited by 13 · see citing works
Osamu, K. A. I., Nagase, H., Suzuki, M., et al. (1993) · Veterinary Immunology and Immunopathology · doi:10.1016/0165-2427(93)90102-a · Cited by 13 · see citing works
Valencia, C. A., Cornejo, P., Romanque, P., et al. (2004) · Toxicology Letters · doi:10.1016/j.toxlet.2003.12.003 · Cited by 13 · see citing works
Duarte, C. G., Azzolini, A. E. C. S., & de Assis-Pandochi, A. I. (2003) · International Immunopharmacology · doi:10.1016/s1567-5769(03)00139-5 · Cited by 12 · see citing works
Problems in the Management of Hypothyroidism
Ladenson, P. W. (2003) · Humana Press eBooks · doi:10.1007/978-1-59259-352-1_8 · Cited by 11 · see citing works
The effects of triodothyronine and thymulin on avian NK cytolytic activity
Marsh, J. A., Merlino, P. G., & Staeheli, P. (2001) · International Immunopharmacology · doi:10.1016/s1567-5769(01)00106-0 · Cited by 10 · see citing works
Kanazawa, H., Kurihara, N., Hirata, K., et al. (1992) · PubMed · Cited by 9 · see citing works
Neutrophil chemotaxis, random migration, and adherence in patients with hyperthyroidism
Wolach, B., Lebanon, B., Jedeikin, A., et al. (1989) · European Journal of Endocrinology · doi:10.1530/acta.0.1210817 · Cited by 9 · see citing works
Functional characterization of peripheral blood neutrophils in patients with primary hypothyroidism.
Hrycek, A. (1993) · PubMed · Cited by 9 · see citing works
Chandel, A. S., & Chatterjee, S. (1989) · PubMed · Cited by 8 · see citing works
[Effects of thyroxine on IgM production and beta-adrenergic receptor on lymphocyte in mice].
Huang, L.-Y. M., Zy, L., Sy, X., et al. (1990) · PubMed · Cited by 7 · see citing works
Functional characterization of peripheral blood neutrophils in patients with hyperthyroidism.
Hrycek, A. (1995) · PubMed · Cited by 6 · see citing works
Nongenomic Actions of Thyroid Hormone and Intracellular Calcium Metabolism
Incerpi, S., Davis, P. J., Vito, P. D., Farı́as, R. N., Lin, H., & Davis, F. B. (2008) · Clinical Reviews in Bone and Mineral Metabolism · doi:10.1007/s12018-008-9019-1 · Cited by 4 · see citing works
Self-citation[Cytochemical properties of peripheral blood neutrophils in patients with hyperthyroidism].
Hrycek, A., & Kalina, Z. (1992) · PubMed · Cited by 2 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Thyroid hormones and cardiovascular disease
Jabbar, A., Pingitore, A., Pearce, S. H. S., Zaman, A., Iervasi, G., & Razvi, S. (2017) · Nature Reviews Cardiology · doi:10.1038/nrcardio.2016.174 · Cited by 729 · see citing works
The Consortium on Thyroid and Pregnancy—Study Group on Preterm Birth, Korevaar, T. I. M., Derakhshan, A., Taylor, P. N., Meima, M., Chen, L., Bliddal, S., Carty, D. M., Meems, M., Vaidya, B., et al. (2019) · JAMA · doi:10.1001/jama.2019.10931 · Cited by 378 · see citing works
Cytokine dysregulation in autism spectrum disorders (ASD): Possible role of the environment
Goines, P. E., & Ashwood, P. (2013) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2012.07.006 · Cited by 314 · see citing works
Paradigms of dynamic control of thyroid hormone signaling
Bianco, A. C., Dumitrescu, A., Gereben, B., Ribeiro, M. O., Fonseca, T. L., Fernandes, G. W., & Bocco, B. M. L. C. (2019) · Endocrine Reviews · doi:10.1210/er.2018-00275 · Cited by 293 · see citing works
McLachlan, S. M., & Rapoport, B. (2013) · Thyroid · doi:10.1089/thy.2012.0374 · Cited by 239 · see citing works
Marques, A. H., O'Connor, T. G., Roth, C., Susser, E., & Bjørke-Monsen, A.-L. (2013) · Frontiers in Neuroscience · doi:10.3389/fnins.2013.00120 · Cited by 226 · see citing works
Interaction of the endocrine system with inflammation: a function of energy and volume regulation
Straub, R. H. (2014) · Arthritis Research & Therapy · doi:10.1186/ar4484 · Cited by 121 · see citing works
“Cα, ERK1/2, and/or hypoxia-inducible factor-1, leading to enhanced cytokine and growth factor action and angiogenesis [128].”
BackgroundInfluentialBliddal, S., Feldt-Rasmussen, U., Rasmussen, Å. K., Kolte, A. M., Hilsted, L. M., Christiansen, O. B., Nielsen, C. H., & Nielsen, H. S. (2019) · Thyroid® · doi:10.1089/thy.2019.0077 · Cited by 63 · see citing works
Role of thyroid dysimmunity and thyroid hormones in endometriosis
Peyneau, M., Kavian, N., Chouzenoux, S., Nicco, C., Jeljeli, M., Toullec, L., Reboul-Marty, J., Chenevier-Gobeaux, C., Reis, F. M., Santulli, P., et al. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1820469116 · Cited by 50 · see citing works
Stavreus Evers, A. (2012) · Frontiers in Endocrinology · doi:10.3389/fendo.2012.00050 · Cited by 36 · see citing works
- Authors
- De Vito, P., Incerpi, S., Pedersen, J. Z., Luly, P., Davis, F. B., & Davis, P. J.
- Affiliations
- Department of Biology, University of Rome Tor Vergata, Rome, Italy.
- Roma Tre University (IT)
- University of Rome Tor Vergata (IT)
- Signal Transduction Laboratory, Ordway Research Institute, Inc., Albany, New York.
- Corresponding author
- Incerpi, Sandra
- Venue
- Thyroid
- Publisher
- SAGE Publications
- Published
- 2011-08
- Volume
- 21
- Issue
- 8
- Pages
- 879-890
- ISSN
- 1050-7256 (ISSN-L)
- 1557-9077
- OpenAlex
- W2051241287
- Cited by
- 347
- References
- 163
- Citations by year
- 2026: 16 · 2025: 24 · 2024: 22 · 2023: 34 · 2022: 44 · 2021: 31 · 2020: 30 · 2019: 29 · 2018: 15 · 2017: 26 · 2016: 18 · 2015: 18 · 2014: 15 · 2013: 15 · 2012: 10
- FWCI
- 10.44
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Thyroid (publishedVersion)
- PubMed (publishedVersion)
- Cineca Institutional Research Information System (Tor Vergata University) (submittedVersion)
- Iris (Roma Tre University) (submittedVersion)
- Funders
- U.S. Food and Drug Administration
- Topics
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Thyroid Disorders and Treatments
- Life Sciences › Immunology and Microbiology › Immunology › Immunotoxicology and immune responses
- Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
- Keywords
- thyroid hormones, thyroxine, triiodothyronine, immunomodulation, hyperthyroidism, hypothyroidism, monocytes, macrophages, Kupffer cells, natural killer cells, phagocytosis, reactive oxygen species, cytokine production, macrophage inflammatory protein-1alpha, IL-1β, TNF-α, nitric oxide synthase, respiratory burst, innate immunity, adaptive immunity
- MeSH terms
- Animals, Humans, Hyperthyroidism, Immune System, Macrophages, Models, Biological, Thyroid Hormones, Thyroxine, Triiodothyronine, Reactive Oxygen Species, Interleukin-1beta, Chemokine CCL3
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review