L-3,3’,5-triiodothyronine and pregnenolone sulfate inhibit Torpedo nicotinic acetylcholine receptors
Autoři:
Steven X. Moffett aff001; Eric A. Klein aff001; Grace Brannigan aff001; Joseph V. Martin aff001
Působiště autorů:
Center for Computational and Integrative Biology, Rutgers University—Camden, Camden, New Jersey, United States of America
aff001; Department of Biology, Rutgers University—Camden, Camden, New Jersey, United States of America
aff002; Department of Physics, Rutgers University—Camden, Camden, New Jersey, United States of America
aff003
Vyšlo v časopise:
PLoS ONE 14(10)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0223272
Souhrn
The nicotinic acetylcholine receptor (nAChR) is an excitatory pentameric ligand-gated ion channel (pLGIC), homologous to the inhibitory γ-aminobutyric acid (GABA) type A receptor targeted by pharmaceuticals and endogenous sedatives. Activation of the GABAA receptor by the neurosteroid allopregnanolone can be inhibited competitively by thyroid hormone (L-3,3’,5-triiodothyronine, or T3), but modulation of nAChR by T3 or neurosteroids has not been investigated. Here we show that allopregnanolone inhibits the nAChR from Torpedo californica at micromolar concentrations, as do T3 and the anionic neurosteroid pregnenolone sulfate (PS). We test for the role of protein and ligand charge in mediated receptor inhibition by varying pH in a narrow range around physiological pH. We find that both T3 and PS become less potent with increasing pH, with remarkably similar trends in IC50 when T3 is neutral at pH < 7.3. After deprotonation of T3 (but no additional deprotonation of PS) at pH 7.3, T3 loses potency more slowly with increasing pH than PS. We interpret this result as indicating the negative charge is not required for inhibition but does increase activity. Finally, we show that both T3 and PS affect nAChR channel desensitization, which may implicate a binding site homologous to one that was recently indicated for accelerated desensitization of the GABAA receptor by PS.
Klíčová slova:
Sulfates – Acetylcholine – Thyroid hormones – Xenopus oocytes – Receptor physiology – Sucrose – Nicotinic acetylcholine receptors – Ligand-gated ion channels
Zdroje
1. Clarke PB, Schwartz RD, Paul SM, Pert CB, Pert A. Nicotinic binding in rat brain: autoradiographic comparison of [3H]acetylcholine, [3H]nicotine, and [125I]-alpha-bungarotoxin. The Journal of neuroscience: the official journal of the Society for Neuroscience. 1985;5(5):1307–15. Epub 1985/05/01. 3998824.
2. Hucho F. The nicotinic acetylcholine receptor and its ion channel. European journal of biochemistry. 1986;158(2):211–26. Epub 1986/07/15. doi: 10.1111/j.1432-1033.1986.tb09740.x 2426106.
3. Steinlein OK, Bertrand D. Nicotinic receptor channelopathies and epilepsy. Pflugers Archiv: European journal of physiology. 2010;460(2):495–503. Epub 2009/12/18. doi: 10.1007/s00424-009-0766-8 20016990.
4. Fambrough DM, Drachman DB, Satyamurti S. Neuromuscular junction in myasthenia gravis: decreased acetylcholine receptors. Science (New York, NY). 1973;182(4109):293–5. Epub 1973/10/19. doi: 10.1126/science.182.4109.293 4742736.
5. Drachman DB, Angus CW, Adams RN, Michelson JD, Hoffman GJ. Myasthenic antibodies cross-link acetylcholine receptors to accelerate degradation. The New England journal of medicine. 1978;298(20):1116–22. Epub 1978/05/18. doi: 10.1056/NEJM197805182982004 643030.
6. Sine SM, Engel AG. Recent advances in Cys-loop receptor structure and function. Nature. 2006;440(7083):448–55. Epub 2006/03/24. doi: 10.1038/nature04708 16554804.
7. Lester HA, Dibas MI, Dahan DS, Leite JF, Dougherty DA. Cys-loop receptors: new twists and turns. Trends in neurosciences. 2004;27(6):329–36. Epub 2004/05/29. doi: 10.1016/j.tins.2004.04.002 15165737.
8. Thompson AJ, Lester HA, Lummis SC. The structural basis of function in Cys-loop receptors. Quarterly reviews of biophysics. 2010;43(4):449–99. Epub 2010/09/21. doi: 10.1017/S0033583510000168 20849671.
9. Miller PS, Smart TG. Binding, activation and modulation of Cys-loop receptors. Trends in pharmacological sciences. 2010;31(4):161–74. Epub 2010/01/26. doi: 10.1016/j.tips.2009.12.005 20096941.
10. Lynagh T, Laube B. Opposing effects of the anesthetic propofol at pentameric ligand-gated ion channels mediated by a common site. The Journal of neuroscience: the official journal of the Society for Neuroscience. 2014;34(6):2155–9. Epub 2014/02/07. doi: 10.1523/jneurosci.4307-13.2014 24501356.
11. Miyazawa A, Fujiyoshi Y, Unwin N. Structure and gating mechanism of the acetylcholine receptor pore. Nature. 2003;423(6943):949–55. Epub 2003/06/27. doi: 10.1038/nature01748 12827192.
12. Corringer PJ, Poitevin F, Prevost MS, Sauguet L, Delarue M, Changeux JP. Structure and pharmacology of pentameric receptor channels: from bacteria to brain. Structure (London, England: 1993). 2012;20(6):941–56. Epub 2012/06/12. doi: 10.1016/j.str.2012.05.003 22681900.
13. Atluri N, Joksimovic SM, Oklopcic A, Milanovic D, Klawitter J, Eggan P, et al. A neurosteroid analogue with T-type calcium channel blocking properties is an effective hypnotic, but is not harmful to neonatal rat brain. British journal of anaesthesia. 2018;120(4):768–78. Epub 2018/03/27. doi: 10.1016/j.bja.2017.12.039 29576117; PubMed Central PMCID: PMC6200096.
14. Zhang M, Liu J, Zhou MM, Wu H, Hou Y, Li YF, et al. Anxiolytic effects of hippocampal neurosteroids in normal and neuropathic rats with spared nerve injury. Journal of neurochemistry. 2017;141(1):137–50. Epub 2017/01/28. doi: 10.1111/jnc.13965 28129443.
15. Gulinello M, Smith SS. Anxiogenic effects of neurosteroid exposure: sex differences and altered GABAA receptor pharmacology in adult rats. The Journal of pharmacology and experimental therapeutics. 2003;305(2):541–8. Epub 2003/02/28. doi: 10.1124/jpet.102.045120 12606703.
16. Frye CA. The neurosteroid 3 alpha, 5 apha-THP has antiseizure and possible neuroprotective effects in an animal model of epilepsy. Brain research. 1995;696(1–2):113–20. Epub 1995/10/23. doi: 10.1016/0006-8993(95)00793-p 8574658.
17. Joksimovic SL, Covey DF, Jevtovic-Todorovic V, Todorovic SM. Neurosteroids in Pain Management: A New Perspective on an Old Player. Frontiers in pharmacology. 2018;9:1127. Epub 2018/10/20. doi: 10.3389/fphar.2018.01127 30333753; PubMed Central PMCID: PMC6176051.
18. Belelli D, Pistis M, Peters JA, Lambert JJ. The interaction of general anaesthetics and neurosteroids with GABA(A) and glycine receptors. Neurochemistry international. 1999;34(5):447–52. Epub 1999/07/09. doi: 10.1016/s0197-0186(99)00037-6 10397373.
19. Li GD, Chiara DC, Cohen JB, Olsen RW. Neurosteroids allosterically modulate binding of the anesthetic etomidate to gamma-aminobutyric acid type A receptors. The Journal of biological chemistry. 2009;284(18):11771–5. Epub 2009/03/14. doi: 10.1074/jbc.C900016200 19282280; PubMed Central PMCID: PMC2673245.
20. Covey DF, Evers AS, Mennerick S, Zorumski CF, Purdy RH. Recent developments in structure-activity relationships for steroid modulators of GABA(A) receptors. Brain research Brain research reviews. 2001;37(1–3):91–7. Epub 2001/12/18. 11744077.
21. Covey DF, Han M, Kumar AS, de La Cruz MA, Meadows ES, Hu Y, et al. Neurosteroid analogues. 8. Structure-activity studies of N-acylated 17a-aza-D-homosteroid analogues of the anesthetic steroids (3alpha, 5alpha)- and (3alpha,5beta)-3-hydroxypregnan-20-one. Journal of medicinal chemistry. 2000;43(17):3201–4. Epub 2000/09/01. doi: 10.1021/jm0002477 10966737.
22. Covey DF, Nathan D, Kalkbrenner M, Nilsson KR, Hu Y, Zorumski CF, et al. Enantioselectivity of pregnanolone-induced gamma-aminobutyric acid(A) receptor modulation and anesthesia. The Journal of pharmacology and experimental therapeutics. 2000;293(3):1009–16. Epub 2000/06/28. 10869405.
23. Paradiso K, Sabey K, Evers AS, Zorumski CF, Covey DF, Steinbach JH. Steroid inhibition of rat neuronal nicotinic alpha4beta2 receptors expressed in HEK 293 cells. Molecular pharmacology. 2000;58(2):341–51. Epub 2000/07/25. doi: 10.1124/mol.58.2.341 10908302.
24. Uki M, Nabekura J, Akaike N. Suppression of the nicotinic acetylcholine response in rat superior cervical ganglionic neurons by steroids. Journal of neurochemistry. 1999;72(2):808–14. Epub 1999/02/04. doi: 10.1046/j.1471-4159.1999.0720808.x 9930757.
25. Wang M. Neurosteroids and GABA-A Receptor Function. Frontiers in endocrinology. 2011;2:44. Epub 2011/01/01. doi: 10.3389/fendo.2011.00044 22654809; PubMed Central PMCID: PMC3356040.
26. Belelli D, Casula A, Ling A, Lambert JJ. The influence of subunit composition on the interaction of neurosteroids with GABA(A) receptors. Neuropharmacology. 2002;43(4):651–61. Epub 2002/10/09. doi: 10.1016/s0028-3908(02)00172-7 12367610.
27. Hosie AM, Clarke L, da Silva H, Smart TG. Conserved site for neurosteroid modulation of doi: 10.1016/j.neuropharm.2008.07.050 18762201 A receptors. Neuropharmacology. 2009;56(1):149–54. Epub 2008/09/03.
28. Seljeset S, Bright DP, Thomas P, Smart TG. Probing GABAA receptors with inhibitory neurosteroids. Neuropharmacology. 2018;136(Pt A):23–36. Epub 2018/02/16. doi: 10.1016/j.neuropharm.2018.02.008 29447845; PubMed Central PMCID: PMC6018617.
29. Westergard T, Salari R, Martin JV, Brannigan G. Interactions of L-3,5,3'-Triiodothyronine [corrected], Allopregnanolone, and Ivermectin with the GABAA Receptor: Evidence for Overlapping Intersubunit Binding Modes. PloS one. 2015;10(9):e0139072. Epub 2015/10/01. doi: 10.1371/journal.pone.0139072 26421724; PubMed Central PMCID: PMC4589331.
30. Majewska MD. Neurosteroids: endogenous bimodal modulators of the GABAA receptor. Mechanism of action and physiological significance. Progress in neurobiology. 1992;38(4):379–95. Epub 1992/01/01. 1349441.
31. Majewska MD, Harrison NL, Schwartz RD, Barker JL, Paul SM. Steroid hormone metabolites are barbiturate-like modulators of the GABA receptor. Science (New York, NY). 1986;232(4753):1004–7. Epub 1986/05/23. doi: 10.1126/science.2422758 2422758.
32. Callachan H, Cottrell GA, Hather NY, Lambert JJ, Nooney JM, Peters JA. Modulation of the GABAA receptor by progesterone metabolites. Proceedings of the Royal Society of London Series B, Biological sciences. 1987;231(1264):359–69. Epub 1987/08/21. doi: 10.1098/rspb.1987.0049 2888123.
33. Martin JV, Padron JM, Newman MA, Chapell R, Leidenheimer NJ, Burke LA. Inhibition of the activity of the native gamma-aminobutyric acid A receptor by metabolites of thyroid hormones: correlations with molecular modeling studies. Brain research. 2004;1004(1–2):98–107. Epub 2004/03/23. doi: 10.1016/j.brainres.2003.12.043 15033424.
34. Martin JV, Williams DB, Fitzgerald RM, Im HK, Vonvoigtlander PF. Thyroid hormonal modulation of the binding and activity of the GABAA receptor complex of brain. Neuroscience. 1996;73(3):705–13. Epub 1996/08/01. doi: 10.1016/0306-4522(96)00052-8 8809792.
35. Chapell R, Martin J, Machu TK, Leidenheimer NJ. Direct channel-gating and modulatory effects of triiodothyronine on recombinant GABA(A) receptors. European journal of pharmacology. 1998;349(1):115–21. Epub 1998/07/21. doi: 10.1016/s0014-2999(98)00182-4 9669504.
36. Puia G, Losi G. Thyroid hormones modulate GABA(A) receptor-mediated currents in hippocampal neurons. Neuropharmacology. 2011;60(7–8):1254–61. Epub 2011/01/11. doi: 10.1016/j.neuropharm.2010.12.013 21215272.
37. Majewska MD, Mienville JM, Vicini S. Neurosteroid pregnenolone sulfate antagonizes electrophysiological responses to GABA in neurons. Neuroscience letters. 1988;90(3):279–84. Epub 1988/08/01. doi: 10.1016/0304-3940(88)90202-9 3138576.
38. Laverty D, Thomas P, Field M, Andersen OJ, Gold MG, Biggin PC, et al. Crystal structures of a GABAA-receptor chimera reveal new endogenous neurosteroid-binding sites. Nature structural & molecular biology. 2017;24(11):977–85. Epub 2017/10/03. doi: 10.1038/nsmb.3477 28967882.
39. Gielen M, Thomas P, Smart TG. The desensitization gate of inhibitory Cys-loop receptors. Nature communications. 2015;6:6829. Epub 2015/04/22. doi: 10.1038/ncomms7829 25891813; PubMed Central PMCID: PMC4410641.
40. Corrie J, Ogrel AA, McCardy EA, Blanton MP, Baenziger JE. Lipid-protein interactions at the nicotinic acetylcholine receptor A functional coupling between nicotinic receptors and phosphatidic acid-containing lipid bilayers. Journal of Biological Chemistry. 2002;277(1):201–8. doi: 10.1074/jbc.M108341200 11682482
41. daCosta CJ, Ogrel AA, McCardy EA, Blanton MP, Baenziger JE. Lipid-protein interactions at the nicotinic acetylcholine receptor. A functional coupling between nicotinic receptors and phosphatidic acid-containing lipid bilayers. The Journal of biological chemistry. 2002;277(1):201–8. Epub 2001/10/30. doi: 10.1074/jbc.M108341200 11682482.
42. Sharp L, Salari R, Brannigan G. Boundary lipids of the nicotinic acetylcholine receptor: spontaneous partitioning via coarse-grained molecular dynamics simulation. Biochimica et Biophysica Acta (BBA)-Biomembranes. 2019.
43. Rankin SE, Addona GH, Kloczewiak MA, Bugge B, Miller KW. The cholesterol dependence of activation and fast desensitization of the nicotinic acetylcholine receptor. Biophysical journal. 1997;73(5):2446–55. Epub 1997/11/25. doi: 10.1016/S0006-3495(97)78273-0 9370438; PubMed Central PMCID: PMC1181146.
44. Criado M, Eibl H, Barrantes FJ. Effects of lipids on acetylcholine receptor. Essential need of cholesterol for maintenance of agonist-induced state transitions in lipid vesicles. Biochemistry. 1982;21(15):3622–9. Epub 1982/07/20. doi: 10.1021/bi00258a015 7115688.
45. Campagna JA, Miller KW, Forman SA. Mechanisms of actions of inhaled anesthetics. The New England journal of medicine. 2003;348(21):2110–24. Epub 2003/05/23. doi: 10.1056/NEJMra021261 12761368.
46. Ke L, Lukas RJ. Effects of steroid exposure on ligand binding and functional activities of diverse nicotinic acetylcholine receptor subtypes. Journal of neurochemistry. 1996;67(3):1100–12. Epub 1996/09/01. doi: 10.1046/j.1471-4159.1996.67031100.x 8752117.
47. Barrantes FJ, Antollini SS, Bouzat CB, Garbus I, Massol RH. Nongenomic effects of steroids on the nicotinic acetylcholine receptor. Kidney international. 2000;57(4):1382–9. Epub 2000/04/12. doi: 10.1046/j.1523-1755.2000.00979.x 10760071.
48. Blanton MP, Xie Y, Dangott LJ, Cohen JB. The steroid promegestone is a noncompetitive antagonist of the Torpedo nicotinic acetylcholine receptor that interacts with the lipid-protein interface. Molecular pharmacology. 1999;55(2):269–78. Epub 1999/02/03. doi: 10.1124/mol.55.2.269 9927618.
49. Hamouda AK, Stewart DS, Husain SS, Cohen JB. Multiple transmembrane binding sites for p-trifluoromethyldiazirinyl-etomidate, a photoreactive Torpedo nicotinic acetylcholine receptor allosteric inhibitor. The Journal of biological chemistry. 2011;286(23):20466–77. Epub 2011/04/19. doi: 10.1074/jbc.M111.219071 21498509; PubMed Central PMCID: PMC3121496.
50. McGrath M, Yu Z, Jayakar SS, Ma C, Tolia M, Zhou X, et al. Etomidate and Etomidate Analog Binding and Positive Modulation of gamma-Aminobutyric Acid Type A Receptors: Evidence for a State-dependent Cutoff Effect. Anesthesiology. 2018;129(5):959–69. Epub 2018/07/28. doi: 10.1097/ALN.0000000000002356 30052529; PubMed Central PMCID: PMC6278829.
51. Sooksawate T, Simmonds MA. Effects of membrane cholesterol on the sensitivity of the GABA(A) receptor to GABA in acutely dissociated rat hippocampal neurones. Neuropharmacology. 2001;40(2):178–84. Epub 2000/12/15. doi: 10.1016/s0028-3908(00)00159-3 11114396.
52. Baenziger JE, Domville JA, Therien JPD. The Role of Cholesterol in the Activation of Nicotinic Acetylcholine Receptors. Current topics in membranes. 2017;80:95–137. Epub 2017/09/03. doi: 10.1016/bs.ctm.2017.05.002 28863823.
53. Kudo K, Tachikawa E, Kashimoto T. Inhibition by pregnenolone sulfate of nicotinic acetylcholine response in adrenal chromaffin cells. European journal of pharmacology. 2002;456(1–3):19–27. doi: 10.1016/s0014-2999(02)02623-7 12450565
54. Palma A, Li L, Chen XJ, Pappone P, McNamee M. Effects of pH on acetylcholine receptor function. The Journal of membrane biology. 1991;120(1):67–73. Epub 1991/02/01. doi: 10.1007/bf01868592 2020020.
55. li L, McNamee M. Modulation of Nicotinic Acetylcholine Receptor Channel by pH: A Difference in pH Sensitivity of Torpedo and Mouse Receptors Expressed in Xenopus Oocytes. Cellular and Molecular Biology. 1991;12(2):83–93.
56. Ochoa EL, Dalziel AW, McNamee MG. Reconstitution of acetylcholine receptor function in lipid vesicles of defined composition. Biochimica et biophysica acta. 1983;727(1):151–62. Epub 1983/01/05. doi: 10.1016/0005-2736(83)90379-6 6824649.
57. Mienville JM, Vicini S. Pregnenolone sulfate antagonizes GABAA receptor-mediated currents via a reduction of channel opening frequency. Brain research. 1989;489(1):190–4. Epub 1989/06/05. doi: 10.1016/0006-8993(89)90024-3 2472854.
58. Dratman MB, Futaesaku Y, Crutchfield FL, Berman N, Payne B, Sar M, et al. Iodine-125-labeled triiodothyronine in rat brain: evidence for localization in discrete neural systems. Science (New York, NY). 1982;215(4530):309–12. Epub 1982/01/15. doi: 10.1126/science.7053582 7053582.
59. Dratman MB, Crutchfield FL, Axelrod J, Colburn RW, Thoa N. Localization of triiodothyronine in nerve ending fractions of rat brain. Proceedings of the National Academy of Sciences of the United States of America. 1976;73(3):941–4. Epub 1976/03/01. doi: 10.1073/pnas.73.3.941 1062808; PubMed Central PMCID: PMC336036.
60. Dratman MB, Crutchfield FL. Synaptosomal [125I]triiodothyronine after intravenous [125I]thyroxine. The American journal of physiology. 1978;235(6):E638–47. Epub 1978/12/01. doi: 10.1152/ajpendo.1978.235.6.E638 736123.
61. Mason GA, Walker CH, Prange AJ Jr. L-triiodothyronine: is this peripheral hormone a central neurotransmitter? Neuropsychopharmacology: official publication of the American College of Neuropsychopharmacology. 1993;8(3):253–8. Epub 1993/05/01. doi: 10.1038/npp.1993.28 8099484.
62. Sarkar PK, Ray AK. Specific binding of L-triiodothyronine modulates Na(+)-K(+)-ATPase activity in adult rat cerebrocortical synaptosomes. Neuroreport. 1998;9(6):1149–52. Epub 1998/05/28. doi: 10.1097/00001756-199804200-00035 9601684.
63. Sarkar PK, Ray AK. Synaptosomal T3 content in cerebral cortex of adult rat in different thyroidal states. Neuropsychopharmacology: official publication of the American College of Neuropsychopharmacology. 1994;11(3):151–5. Epub 1994/11/01. doi: 10.1038/sj.npp.1380101 7865096.
64. Gunnarsson T, Sjöberg S, Eriksson M, Nordin C. Depressive symptoms in hypothyroid disorder with some observations on biochemical correlates. Neuropsychobiology. 2001;43(2):70–4. doi: 10.1159/000054869 11174048
65. Madhu K. Sleep in young untreated hypothyroid subjects. J Sleep Res. 1996;5(3):198–9. 8956211
66. Whybrow Bauer. Behavioral and psychiatric aspects of hypothyroidism. Braverman LE UR, editor. Philadelphia: Lippincott Williams and Wilkins; 2005.
67. Demet MM, Ozmen B, Deveci A, Boyvada S, Adiguzel H, Aydemir O. Depression and anxiety in hyperthyroidism. Archives of medical research. 2002;33(6):552–6. Epub 2002/12/31. 12505101.
68. Whybrow Bauer. Behavioral and psychiatric aspects of thyrotoxicosis. Braverman LE UR, editor. Philadelphia: Lippincott Williams and Wilkins; 2005.
69. Martin JV, Giannopoulos PF, Moffett SX, James TD. Effects of acute microinjections of thyroid hormone to the preoptic region of euthyroid adult male rats on sleep and motor activity. Brain research. 2013;1516:45–54. Epub 2013/01/26. doi: 10.1016/j.brainres.2013.01.032 23348377.
70. Moffett SX, Giannopoulos PF, James TD, Martin JV. Effects of acute microinjections of thyroid hormone to the preoptic region of hypothyroid adult male rats on sleep, motor activity and body temperature. Brain research. 2013;1516:55–65. Epub 2013/04/23. doi: 10.1016/j.brainres.2013.04.017 23603414.
71. Steiger A, Trachsel L, Guldner J, Hemmeter U, Rothe B, Rupprecht R, et al. Neurosteroid pregnenolone induces sleep-EEG changes in man compatible with inverse agonistic GABAA-receptor modulation. Brain research. 1993;615(2):267–74. doi: 10.1016/0006-8993(93)90037-n 8395958
72. Darnaudery M, Pallares M, Bouyer J, Le Moal M, Mayo W. Infusion of neurosteroids into the rat nucleus basalis affects paradoxical sleep in accordance with their memory modulating properties. Neuroscience. 1999;92(2):583–8. doi: 10.1016/s0306-4522(99)00019-6 10408607
73. Lancel M, Faulhaber J, Holsboer F, Rupprecht R. Progesterone induces changes in sleep comparable to those of agonistic GABAA receptor modulators. American Journal of Physiology-Endocrinology and Metabolism. 1996;271(4):E763–E72.
74. Damianisch K, Rupprecht R, Lancel M. The influence of subchronic administration of the neurosteroid allopregnanolone on sleep in the rat. Neuropsychopharmacology: official publication of the American College of Neuropsychopharmacology. 2001;25(4):576–84.
75. Shen H, Gong QH, Aoki C, Yuan M, Ruderman Y, Dattilo M, et al. Reversal of neurosteroid effects at α4β2δ GABA A receptors triggers anxiety at puberty. Nature neuroscience. 2007;10(4):469. doi: 10.1038/nn1868 17351635
76. Longone P, Rupprecht R, Manieri GA, Bernardi G, Romeo E, Pasini A. The complex roles of neurosteroids in depression and anxiety disorders. Neurochemistry international. 2008;52(4–5):596–601. doi: 10.1016/j.neuint.2007.10.001 17996986
77. Sarkar PK, Durga ND, Morris JJ, Martin JV. In vitro thyroid hormone rapidly modulates protein phosphorylation in cerebrocortical synaptosomes from adult rat brain. Neuroscience. 2006;137(1):125–32. Epub 2005/11/18. doi: 10.1016/j.neuroscience.2005.10.002 16289831.
78. Sarkar PK, Morris JJ, Martin JV. Non-genomic effect of L-triiodothyronine on calmodulin-dependent synaptosomal protein phosphorylation in adult rat cerebral cortex. Indian journal of experimental biology. 2011;49(3):169–76. Epub 2011/04/02. 21452595.
79. James TD, Moffett SX, Scanlan TS, Martin JV. Effects of acute microinjections of the thyroid hormone derivative 3-iodothyronamine to the preoptic region of adult male rats on sleep, thermoregulation and motor activity. Hormones and behavior. 2013;64(1):81–8. doi: 10.1016/j.yhbeh.2013.05.004 PMC4091812. 23702093
80. Dratman MB, Gordon JT. Thyroid hormones as neurotransmitters. Thyroid: official journal of the American Thyroid Association. 1996;6(6):639–47. Epub 1996/12/01. doi: 10.1089/thy.1996.6.639 9001201.
Článok vyšiel v časopise
PLOS One
2019 Číslo 10
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
- Nejasný stín na plicích – kazuistika
- Masturbační chování žen v ČR − dotazníková studie
- Těžké menstruační krvácení může značit poruchu krevní srážlivosti. Jaký management vyšetření a léčby je v takovém případě vhodný?
- Fixní kombinace paracetamol/kodein nabízí synergické analgetické účinky
Najčítanejšie v tomto čísle
- Correction: Low dose naltrexone: Effects on medication in rheumatoid and seropositive arthritis. A nationwide register-based controlled quasi-experimental before-after study
- Combining CDK4/6 inhibitors ribociclib and palbociclib with cytotoxic agents does not enhance cytotoxicity
- Experimentally validated simulation of coronary stents considering different dogboning ratios and asymmetric stent positioning
- Risk factors associated with IgA vasculitis with nephritis (Henoch–Schönlein purpura nephritis) progressing to unfavorable outcomes: A meta-analysis