Endotoxin-induced inflammation down-regulates l-type amino acid transporter 1 (LAT1) expression at the blood-brain barrier of male rats and mice

Fluids and Barriers of the CNS

Volumn 12, Issue 1, 2015, Pages

  Wittmann, Gábor ^a   Mohácsik, Petra ^b,c   Balkhi, Mumtaz Yaseen ^a   Gereben, Balázs ^b   Lechan, Ronald M ^a,d  

^a TUFTS MEDICAL CENTER   (United States)

^b INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^c SEMMELWEIS UNIVERSITY   (Hungary)

^d TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Amino acid transport; Blood brain barrier; Inflammation; LAT1; LPS; Thyroid hormone

Indexed keywords

ENDOTOXIN; EXCITATORY AMINO ACID TRANSPORTER 1; EXCITATORY AMINO ACID TRANSPORTER 2; LIPOPOLYSACCHARIDE; MONOCARBOXYLATE TRANSPORTER 8; ORGANIC ANION TRANSPORTER F; AMINO ACID TRANSPORTER; MESSENGER RNA;

ADULT; AMINO ACID BRAIN LEVEL; AMINO ACID TRANSPORT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BRAIN BLOOD VESSEL; CELLULAR DISTRIBUTION; CHOROID PLEXUS; CONTROLLED STUDY; DOWN REGULATION; ENDOTOXEMIA; FOREBRAIN; GENE EXPRESSION REGULATION; GENE LOCATION; HORMONE TRANSPORT; IMMUNOFLUORESCENCE; IN SITU HYBRIDIZATION; MALE; MOUSE; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; TISSUE DISTRIBUTION; UPREGULATION; ANIMAL; C57BL MOUSE; CHEMICALLY INDUCED; DRUG EFFECTS; ENCEPHALITIS; METABOLISM; NERVE CELL; SPRAGUE DAWLEY RAT;

AMINO ACID TRANSPORT SYSTEM Y+; ANIMALS; BLOOD-BRAIN BARRIER; ENCEPHALITIS; LIPOPOLYSACCHARIDES; MALE; MICE; MICE, INBRED C57BL; NEURONS; PROSENCEPHALON; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER;

EID: 84940781234     PISSN: 20458118     EISSN: 20458118     Source Type: Journal    
DOI: 10.1186/s12987-015-0016-8     Document Type: Article

References (50)

1. 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(1-2):229-36 (pii:0006-8993(91)90194-Z).
2. Heuer H, Visser TJ. Minireview: pathophysiological importance of thyroid hormone transporters. Endocrinology. 2009;150(3):1078-83. doi: 10.1210/en.2008-1518 .
3. Wirth EK, Schweizer U, Kohrle J. Transport of thyroid hormone in brain. Front Endocrinol (Lausanne). 2014;5:98. doi: 10.3389/fendo.2014.00098 .
4. Ceballos A, Belinchon MM, Sanchez-Mendoza E, Grijota-Martinez C, Dumitrescu AM, Refetoff S, et al. Importance of monocarboxylate transporter 8 for the blood-brain barrier-dependent availability of 3,5,3'-triiodo-l-thyronine. Endocrinology. 2009;150(5):2491-6. doi: 10.1210/en.2008-1616 .
5. 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(9):4036-43. doi: 10.1210/en.2006-0390 .
6. Mayerl S, Muller J, Bauer R, Richert S, Kassmann CM, Darras VM, et al. Transporters MCT8 and OATP1C1 maintain murine brain thyroid hormone homeostasis. J Clin Invest. 2014;124(5):1987-99. doi: 10.1172/JCI70324 .
7. 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(3):1528-37. doi: 10.1210/en.2011-1633 .
8. Roberts LM, Woodford K, Zhou M, Black DS, Haggerty JE, Tate EH, 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(12):6251-61. doi: 10.1210/en.2008-0378 .
9. Trajkovic M, Visser TJ, Mittag J, Horn S, Lukas J, Darras VM, et al. Abnormal thyroid hormone metabolism in mice lacking the monocarboxylate transporter 8. J Clin Invest. 2007;117(3):627-35. doi: 10.1172/JCI28253 .
10. Wittmann G, Szabon J, Mohacsik P, Nouriel SS, Gereben B, Fekete C, et al. Parallel regulation of thyroid hormone transporters OATP1c1 and MCT8 during and after endotoxemia at the blood-brain barrier of male rodents. Endocrinology. 2015;156(4):1552-64. doi: 10.1210/en.2014-1830 .
11. Kinne A, Schulein R, Krause G. Primary and secondary thyroid hormone transporters. Thyroid Res. 2011;4(Suppl 1):S7. doi: 10.1186/1756-6614-4-S1-S7 .
12. Muller J, Heuer H. Expression pattern of thyroid hormone transporters in the postnatal mouse brain. Front Endocrinol (Lausanne). 2014;5:92. doi: 10.3389/fendo.2014.00092 .
13. Friesema EC, Docter R, Moerings EP, Verrey F, Krenning EP, Hennemann G, et al. Thyroid hormone transport by the heterodimeric human system l amino acid transporter. Endocrinology. 2001;142(10):4339-48. doi: 10.1210/endo.142.10.8418 .
14. Duelli R, Enerson BE, Gerhart DZ, Drewes LR. Expression of large amino acid transporter LAT1 in rat brain endothelium. J Cereb Blood Flow Metab. 2000;20(11):1557-62. doi: 10.1097/00004647-200011000-00005 .
15. Kageyama T, Imura T, Matsuo A, Minato N, Shimohama S. Distribution of the 4F2 light chain, LAT1, in the mouse brain. NeuroReport. 2000;11(17):3663-6.
16. Kageyama T, Nakamura M, Matsuo A, Yamasaki Y, Takakura Y, Hashida M, et al. The 4F2hc/LAT1 complex transports l-DOPA across the blood-brain barrier. Brain Res. 2000;879(1-2):115-21 (pii:S0006-8993(00)02758-X).
17. Matsuo H, Tsukada S, Nakata T, Chairoungdua A, Kim DK, Cha SH, et al. Expression of a system l neutral amino acid transporter at the blood-brain barrier. NeuroReport. 2000;11(16):3507-11.
18. Roberts LM, Black DS, Raman C, Woodford K, Zhou M, Haggerty JE, et al. Subcellular localization of transporters along the rat blood-brain barrier and blood-cerebral-spinal fluid barrier by in vivo biotinylation. Neuroscience. 2008;155(2):423-38. doi: 10.1016/j.neuroscience.2008.06.015 .
19. Nunez B, Martinez de Mena R, Obregon MJ, Font-Llitjos M, Nunes V, Palacin M, et al. Cerebral cortex hyperthyroidism of newborn mct8-deficient mice transiently suppressed by lat2 inactivation. PLoS One. 2014;9(5):e96915. doi: 10.1371/journal.pone.0096915 .
20. Wirth EK, Roth S, Blechschmidt C, Holter SM, Becker L, Racz I, 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(30):9439-49. doi: 10.1523/JNEUROSCI.6055-08.2009 .
21. Fekete C, Gereben B, Doleschall M, Harney JW, Dora JM, Bianco AC, et al. Lipopolysaccharide induces type 2 iodothyronine deiodinase in the mediobasal hypothalamus: implications for the nonthyroidal illness syndrome. Endocrinology. 2004;145(4):1649-55. doi: 10.1210/en.2003-1439 .
22. Wittmann G, Harney JW, Singru PS, Nouriel SS, Reed Larsen P, Lechan RM. Inflammation-inducible type 2 deiodinase expression in the leptomeninges, choroid plexus, and at brain blood vessels in male rodents. Endocrinology. 2014;155(5):2009-19. doi: 10.1210/en.2013-2154 .
23. 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(14):3287-302. doi: 10.1002/cne.23350 .
24. Lee DA, Bedont JL, Pak T, Wang H, Song J, Miranda-Angulo A, et al. Tanycytes of the hypothalamic median eminence form a diet-responsive neurogenic niche. Nat Neurosci. 2012;15(5):700-2. doi: 10.1038/nn.3079 .
25. Kokoeva MV, Yin H, Flier JS. Evidence for constitutive neural cell proliferation in the adult murine hypothalamus. J Comp Neurol. 2007;505(2):209-20. doi: 10.1002/cne.21492 .
26. Sidibe A, Mullier A, Chen P, Baroncini M, Boutin JA, Delagrange P, et al. Expression of the orphan GPR50 protein in rodent and human dorsomedial hypothalamus, tanycytes and median eminence. J Pineal Res. 2010;48(3):263-9. doi: 10.1111/j.1600-079X.2010.00750.x .
27. Mercier F, Hatton GI. Immunocytochemical basis for a meningeo-glial network. J Comp Neurol. 2000;420(4):445-65. doi: 10.1002/(SICI)1096-9861(20000515)420:4<445:AID-CNE4>3.0.CO;2-3 .
28. Ruderisch N, Virgintino D, Makrides V, Verrey F. Differential axial localization along the mouse brain vascular tree of luminal sodium-dependent glutamine transporters Snat1 and Snat3. J Cereb Blood Flow Metab. 2011;31(7):1637-47. doi: 10.1038/jcbfm.2011.21 .
29. Boado RJ, Li JY, Nagaya M, Zhang C, Pardridge WM. Selective expression of the large neutral amino acid transporter at the blood-brain barrier. Proc Natl Acad Sci USA. 1999;96(21):12079-84.
30. Enerson BE, Drewes LR. The rat blood-brain barrier transcriptome. J Cereb Blood Flow Metab. 2006;26(7):959-73. doi: 10.1038/sj.jcbfm.9600249 .
31. Braun D, Wirth EK, Wohlgemuth F, Reix N, Klein MO, Gruters A, et al. Aminoaciduria, but normal thyroid hormone levels and signalling, in mice lacking the amino acid and thyroid hormone transporter Slc7a8. Biochem J. 2011;439(2):249-55. doi: 10.1042/BJ20110759 .
32. Kido Y, Tamai I, Uchino H, Suzuki F, Sai Y, Tsuji A. Molecular and functional identification of large neutral amino acid transporters LAT1 and LAT2 and their pharmacological relevance at the blood-brain barrier. J Pharm Pharmacol. 2001;53(4):497-503.
33. Killian DM, Chikhale PJ. Predominant functional activity of the large, neutral amino acid transporter (LAT1) isoform at the cerebrovasculature. Neurosci Lett. 2001;306(1-2):1-4 S0304-3940(01)01810-9.
34. Akanuma S, Uchida Y, Ohtsuki S, Tachikawa M, Terasaki T, Hosoya K. Attenuation of prostaglandin E2 elimination across the mouse blood-brain barrier in lipopolysaccharide-induced inflammation and additive inhibitory effect of cefmetazole. Fluids Barriers CNS. 2011;8:24. doi: 10.1186/2045-8118-8-24 .
35. Mori S, Takanaga H, Ohtsuki S, Deguchi T, Kang YS, Hosoya K, et al. Rat organic anion transporter 3 (rOAT3) is responsible for brain-to-blood efflux of homovanillic acid at the abluminal membrane of brain capillary endothelial cells. J Cereb Blood Flow Metab. 2003;23(4):432-40.
36. Ose A, Kusuhara H, Endo C, Tohyama K, Miyajima M, Kitamura S, et al. Functional characterization of mouse organic anion transporting peptide 1a4 in the uptake and efflux of drugs across the blood-brain barrier. Drug Metab Dispos. 2010;38(1):168-76. doi: 10.1124/dmd.109.029454 .
37. Hayashi K, Jutabha P, Endou H, Sagara H, Anzai N. LAT1 is a critical transporter of essential amino acids for immune reactions in activated human T cells. J Immunol. 2013;191(8):4080-5. doi: 10.4049/jimmunol.1300923 .
38. Laflamme N, Rivest S. Effects of systemic immunogenic insults and circulating proinflammatory cytokines on the transcription of the inhibitory factor kappaB alpha within specific cellular populations of the rat brain. J Neurochem. 1999;73(1):309-21.
39. Quan N, Whiteside M, Kim L, Herkenham M. Induction of inhibitory factor kappaBalpha mRNA in the central nervous system after peripheral lipopolysaccharide administration: an in situ hybridization histochemistry study in the rat. Proc Natl Acad Sci USA. 1997;94(20):10985-90.
40. Elovson J. Biogenesis of plasma membrane glycoproteins. Tracer kinetic study of two rat liver plasma membrane glycoproteins in vivo. J Biol Chem. 1980;255(12):5816-25.
41. Kipp H, Pichetshote N, Arias IM. Transporters on demand: intrahepatic pools of canalicular ATP binding cassette transporters in rat liver. J Biol Chem. 2001;276(10):7218-24. doi: 10.1074/jbc.M007794200 .
42. Kogai T, Endo T, Saito T, Miyazaki A, Kawaguchi A, Onaya T. Regulation by thyroid-stimulating hormone of sodium/iodide symporter gene expression and protein levels in FRTL-5 cells. Endocrinology. 1997;138(6):2227-32. doi: 10.1210/endo.138.6.5189 .
43. Paire A, Bernier-Valentin F, Selmi-Ruby S, Rousset B. Characterization of the rat thyroid iodide transporter using anti-peptide antibodies. Relationship between its expression and activity. J Biol Chem. 1997;272(29):18245-9.
44. Scott LJ, Hubbard AL. Dynamics of four rat liver plasma membrane proteins and polymeric IgA receptor. Rates of synthesis and selective loss into the bile. J Biol Chem. 1992;267(9):6099-106.
45. Tanabe T, Pricer WE Jr, Ashwell G. Subcellular membrane topology and turnover of a rat hepatic binding protein specific for asialoglycoproteins. J Biol Chem. 1979;254(4):1038-43.
46. Tauber R, Kronenberger C, Reutter W. Decreased intramolecular turnover of l-fucose in membrane glycoproteins of rat liver during liver regeneration. Biol Chem Hoppe Seyler. 1989;370(11):1221-8.
47. Volk BA, Kreisel W, Kottgen E, Gerok W, Reutter W. Heterogeneous turnover of terminal and core sugars within the carbohydrate chain of dipeptidylaminopeptidase IV isolated from rat liver plasma membrane. FEBS Lett. 1983;163(1):150-2 (0014-5793(83)81183-1).
48. Boado RJ, Li JY, Pardridge WM. Site-directed mutagenesis of rabbit LAT1 at amino acids 219 and 234. J Neurochem. 2003;84(6):1322-31 (pii:1622).
49. Daniel PM, Moorhouse SR, Pratt OE. Amino acid precursors of monoamine neurotransmitters and some factors influencing their supply to the brain. Psychol Med. 1976;6(2):277-86.
50. Pardridge WM. Kinetics of competitive inhibition of neutral amino acid transport across the blood-brain barrier. J Neurochem. 1977;28(1):103-8.