Parallel regulation of thyroid hormone transporters OATP1c1 and MCT8 during and after endotoxemia at the blood-brain barrier of male rodents

Endocrinology (United States)

Volumn 156, Issue 4, 2015, Pages 1552-1564

  Wittmann, Gábor ^a   Szabon, Judit ^b   Mohácsik, Petra ^b,c   Nouriel, Shira S ^a   Gereben, Balázs ^b   Fekete, Csaba ^a,b   Lechan, Ronald M ^a,d  

^a Diabetes Unit   (United States)

^b INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^c SEMMELWEIS UNIVERSITY   (Hungary)

^d TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; MESSENGER RNA; MONOCARBOXYLATE TRANSPORTER 8; ORGANIC ANION TRANSPORTER F; CARRIER PROTEIN; MONOCARBOXYLATE TRANSPORTER; MONOCARBOXYLATE TRANSPORTER 8, RAT; OATP2 PROTEIN, MOUSE; ORGANIC CATION TRANSPORTER; SLC16A2 PROTEIN, MOUSE; SLCO1C1 PROTEIN, RAT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BLOOD BRAIN BARRIER; BRAIN BLOOD VESSEL; CONTROLLED STUDY; ENDOTOXEMIA; FOREBRAIN; HOMEOSTASIS; IMMUNOFLUORESCENCE; IN SITU HYBRIDIZATION; MALE; MOUSE; NERVE CELL; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; RAT; ANIMAL; C57BL MOUSE; GENETICS; METABOLISM; SPRAGUE DAWLEY RAT; WISTAR RAT;

ANIMALS; ASTROCYTES; BLOOD-BRAIN BARRIER; ENDOTOXEMIA; MALE; MEMBRANE TRANSPORT PROTEINS; MICE; MICE, INBRED C57BL; MONOCARBOXYLIC ACID TRANSPORTERS; NEURONS; ORGANIC CATION TRANSPORT PROTEINS; PROSENCEPHALON; RATS; RATS, SPRAGUE-DAWLEY; RATS, WISTAR;

EID: 84926444090     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2014-1830     Document Type: Article

References (47)

1. Boelen A, Kwakkel J, Fliers E. Beyond low plasma T3: Local thyroid hormone metabolism during inflammation and infection. Endocr Rev. 2011;32:670-693.
2. Fekete C, Lechan RM. Central regulation of hypothalamic-pituitary-thyroid axis under physiological and pathophysiological conditions. Endocr Rev. 2014;35:159-194.
3. Van den Berghe G. Non-thyroidal illness in the ICU: A Syndrome with different faces. Thyroid. 2014;24:1456-1465.
4. Gereben B, Zavacki AM, Ribich S, et al. Cellular and molecular basis of deiodinase-regulated thyroid hormone signaling. Endocr Rev. 2008;29:898-938.
5. Visser TJ. Thyroid hormone transporters and resistance. Endocr Dev. 2013;24:1-10.
6. Kwakkel J, Surovtseva OV, de Vries EM, Stap J, Fliers E, Boelen A. A novel role for the thyroid hormone-activating enzyme type 2 deiodinase in the inflammatory response of macrophages. Endocrinology. 2014;155:2725-2734.
7. de Vries EM, Kwakkel J, Eggels L, Kalsbeek A, Barrett P, Fliers E, Boelen A. NFκB signaling is essential for the lipopolysaccharide-induced increase of type 2 deiodinase in tanycytes. Endocrinology. 2014;155:2000-2008.
8. Barca-Mayo O, Liao XH, DiCosmo C, et al. Role of type 2 deiodinase in response to acute lung injury (ALI) in mice. Proc Natl Acad Sci U S A. 2011;108:E1321-1329.
9. Boelen A, Kwakkel J, Chassande O, Fliers E. Thyroid hormone receptor β mediates acute illness-induced alterations in central thyroid hormone metabolism. J Neuroendocrinol. 2009;21:465-472.
10. Boelen A, Kwakkel J, Thijssen-Timmer DC, Alkemade A, Fliers E, Wiersinga WM. Simultaneous changes in central and peripheral components of the hypothalamus-pituitary-thyroid axis in lipopolysaccharide-induced acute illness in mice. J Endocrinol. 2004;182:315-323.
11. Fekete C, Gereben B, Doleschall M, et al. Lipopolysaccharide induces type 2 iodothyronine deiodinase in the mediobasal hypothalamus: Implications for the nonthyroidal illness syndrome. Endocrinology. 2004;145:1649-1655.
12. Kwakkel J, Chassande O, van Beeren HC, Wiersinga WM, Boelen A. Lacking thyroid hormone receptor beta gene does not influence alterations in peripheral thyroid hormone metabolism during acute illness. J Endocrinol. 2008;197:151-158.
13. Kwakkel J, van Beeren HC, Ackermans MT, et al. Skeletal muscle deiodinase type 2 regulation during illness in mice. J Endocrinol. 2009;203:263-270.
14. Ma SF, Xie L, Pino-Yanes M, et al. Type 2 deiodinase and host responses of sepsis and acute lung injury. Am J Respir Cell Mol Biol. 2011;45:1203-1211.
15. Wittmann G, Harney JW, Singru PS, et al. Inflammation-inducible type 2 deiodinase expression in the leptomeninges, choroid plexus, and at brain blood vessels in male rodents. Endocrinology. 2014;155:2009-2019.
16. Chen Y, Sjolinder M, Wang X, et al. Thyroid hormone enhances nitric oxide-mediated bacterial clearance and promotes survival after meningococcal infection. PLoS One. 2012;7:e41445.
17. Cheng AW, Bolognesi M, Kraus VB. DIO2 modifies inflammatory responses in chondrocytes. Osteoarthritis Cartilage. 2012;20:440-445.
18. Perrotta C, Buldorini M, Assi E, et al. The thyroid hormone triiodothyronine controls macrophage maturation and functions: Protective role during inflammation. Am J Pathol. 2014;184:230-247.
19. Castro I, Quisenberry L, Calvo RM, Obregon MJ, Lado-Abeal J. Septic shock non-thyroidal illness syndrome causes hypothyroidism and conditions for reduced sensitivity to thyroid hormone. J Mol Endocrinol. 2013;50:255-266.
20. Rodriguez-Perez A, Palos-Paz F, Kaptein E, et al. Identification of molecular mechanisms related to nonthyroidal illness syndrome in skeletal muscle and adipose tissue from patients with septic shock. Clin Endocrinol (Oxf). 2008;68:821-827.
21. Mebis L, Debaveye Y, Ellger B, et al. Changes in the central component of the hypothalamus-pituitary-thyroid axis in a rabbit model of prolonged critical illness. Crit Care. 2009;13:R147.
22. Kinne A, Schulein R, Krause G. Primary and secondary thyroid hormone transporters. Thyroid Res. 2011;4 Suppl 1:S7.
23. Muller J, Heuer H. Expression pattern of thyroid hormone transporters in the postnatal mouse brain. Front Endocrinol (Lausanne). 2014;5:92.
24. Mayerl S, Müller J, Bauer R, et al. Transporters MCT8 and OATP1C1 maintain murine brain thyroid hormone homeostasis. J Clin Invest. 2014;124:1987-1999.
25. Heuer H, Maier MK, Iden S, et al. The monocarboxylate transporter 8 linked to human psychomotor retardation is highly expressed in thyroid hormone-sensitive neuron populations. Endocrinology. 2005;146:1701-1706.
26. Roberts LM, Woodford K, Zhou M, et al. Expression of the thyroid hormone transporters monocarboxylate transporter-8 (SLC16A2) and organic ion transporter-14 (SLCO1C1) at the blood-brain barrier. Endocrinology. 2008;149:6251-6261.
27. Schnell C, Shahmoradi A, Wichert SP, et al. The multispecific thyroid hormone transporter OATP1C1 mediates cell-specific sulforhodamine 101-labeling of hippocampal astrocytes. Brain Struct Funct. 2015;220:193-203.
28. Sugiyama D, Kusuhara H, Taniguchi H, et al. Functional characterization of rat brain-specific organic anion transporter (Oatp14) at the blood-brain barrier: High affinity transporter for thyroxine. J Biol Chem. 2003;278:43489-43495.
29. Tohyama K, Kusuhara H, Sugiyama Y. Involvement of multispecific organic anion transporter, Oatp14 (Slc21a14), in the transport of thyroxine across the blood-brain barrier. Endocrinology. 2004;145:4384-4391.
30. Wirth EK, Roth S, Blechschmidt C, et al. Neuronal 3′,3,5-triiodothyronine (T3) uptake and behavioral phenotype of mice deficient in Mct8, the neuronal T3 transporter mutated in Allan-Herndon-Dudley syndrome. J Neurosci. 2009;29:9439-9449.
31. Dumitrescu AM, Liao XH, Weiss RE, Millen K, Refetoff S. Tissue-specific thyroid hormone deprivation and excess in monocarboxylate transporter (mct) 8-deficient mice. Endocrinology. 2006;147:4036-4043.
32. Trajkovic M, Visser TJ, Mittag J, et al. Abnormal thyroid hormone metabolism in mice lacking the monocarboxylate transporter 8. J Clin Invest. 2007;117:627-635.
33. Ceballos A, Belinchon MM, Sanchez-Mendoza E, et al. Importance of monocarboxylate transporter 8 for the blood-brain barrier-dependent availability of 3,5,3′-triiodo-L-thyronine. Endocrinology. 2009;150:2491-2496.
34. Mayerl S, Visser TJ, Darras VM, Horn S, Heuer H. Impact of Oatp1c1 deficiency on thyroid hormone metabolism and action in the mouse brain. Endocrinology. 2012;153:1528-1537.
35. Bianco AC, Anderson G, Forrest D, et al. American thyroid association guide to investigating thyroid hormone economy and action in rodent and cell models. Thyroid. 2014;24:88-168.
36. Wittmann G, Hrabovszky E, Lechan RM. Distinct glutamatergic and GABAergic subsets of hypothalamic pro-opiomelanocortin neurons revealed by in situ hybridization in male rats and mice. J Comp Neurol. 2013;521:3287-3302.
37. Kallo I, Mohacsik P, Vida B, et al. Anovel pathway regulates thyroid hormone availability in rat and human hypothalamic neurosecretory neurons. PLoS One. 2012;7:e37860.
38. Grijota-Martínez C, Díez D, Morreale de Escobar G, Bernal J, Morte B. Lack of action of exogenously administered T3 on the fetal rat brain despite expression of the monocarboxylate transporter 8. Endocrinology. 2011;152:1713-1721.
39. Dratman MB, Crutchfield FL, Schoenhoff MB. Transport of iodothyronines from bloodstream to brain: Contributions by blood: brain and choroid plexus:cerebrospinal fluid barriers. Brain Res. 1991;554:229-236.
40. van der Deure WM, Appelhof BC, Peeters RP, et al. Polymorphisms in the brain-specific thyroid hormone transporter OATP1C1 are associated with fatigue and depression in hypothyroid patients. Clin Endocrinol (Oxf). 2008;69:804-811.
41. Zeöld A, Doleschall M, Haffner MC, et al. Characterization of the nuclear factor-kappa B responsiveness of the human dio2 gene. Endocrinology. 2006;147:4419-4429.
42. Elmquist JK, Breder CD, Sherin JE, et al. Intravenous lipopolysaccharide induces cyclooxygenase 2-like immunoreactivity in rat brain perivascular microglia and meningeal macrophages. J Comp Neurol. 1997;381:119-129.
43. Lacroix S, Feinstein D, Rivest S. The bacterial endotoxin lipopolysaccharide has the ability to target the brain in upregulating its membrane CD14 receptor within specific cellular populations. Brain Pathol. 1998;8:625-640.
44. Lacroix S, Rivest S. Effect of acute systemic inflammatory response and cytokines on the transcription of the genes encoding cyclooxygenase enzymes (COX-1 and COX-2) in the rat brain. J Neurochem. 1998;70:452-466.
45. Quan N, Whiteside M, Herkenham M. Time course and localization patterns of interleukin-1beta messenger RNA expression in brain and pituitary after peripheral administration of lipopolysaccharide. Neuroscience. 1998;83:281-293.
46. Nadeau S, Rivest S. Effects of circulating tumor necrosis factor on the neuronal activity and expression of the genes encoding the tumor necrosis factor receptors (p55 and p75) in the rat brain: A view from the blood-brain barrier. Neuroscience. 1999;93:1449-1464.
47. Nadeau S, Rivest S. Regulation of the gene encoding tumor necrosis factor alpha (TNF-alpha) in the rat brain and pituitary in response in different models of systemic immune challenge. J Neuropathol Exp Neurol. 1999;58:61-77.