GABA transport and neuroinflammation are coupled in multiple sclerosis: Regulation of the GABA transporter-2 by ganaxolone

Neuroscience

Volumn 273, Issue , 2014, Pages 24-38

  Paul, A M ^a   Branton, W G ^a   Walsh, J G ^a   Polyak, M J ^a   Lu, J Q ^a   Baker, G B ^a   Power, C ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Experimental autoimmune encephalitis; Ganaxolone; Multiple sclerosis; Neuroinflammation; amino butyric acid; amino butyric acid transporter 2

Indexed keywords

4 AMINOBUTYRIC ACID; DIMETHYL SULFOXIDE; GABA TRANSPORTER 2; GAMMA INTERFERON; GANAXOLONE; HLA DR ANTIGEN; JANUS KINASE 1; MESSENGER RNA; STAT1 PROTEIN; X BOX BINDING PROTEIN 1; 4 AMINOBUTYRIC ACID CARRIER; ELTANOLONE; NEUROPROTECTIVE AGENT; SLC6A12 PROTEIN, MOUSE; SLC6A13 PROTEIN, HUMAN;

4 AMINOBUTYRIC ACID BRAIN LEVEL; AMINO ACID TRANSPORT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; AXONAL INJURY; BRAIN LEVEL; CELL ACTIVATION; CELL CULTURE; CELL LINEAGE; CELL STIMULATION; CONTROLLED STUDY; DEMYELINATION; DISEASE MODEL; DRUG EFFECT; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; FEMALE; FETUS; GABAERGIC TRANSMISSION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOCYTOCHEMISTRY; IN VIVO STUDY; MACROPHAGE; MICROGLIA; MOUSE; MULTIPLE SCLEROSIS; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; SPINAL CORD; TREATMENT OUTCOME; WESTERN BLOTTING; WHITE MATTER; ANALOGS AND DERIVATIVES; ANIMAL; C57BL MOUSE; DRUG EFFECTS; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FRONTAL LOBE; IMMUNOMODULATION; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; T LYMPHOCYTE;

ANIMALS; ASTROCYTES; CELLS, CULTURED; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FEMALE; FRONTAL LOBE; GABA PLASMA MEMBRANE TRANSPORT PROTEINS; GAMMA-AMINOBUTYRIC ACID; INTERFERON-GAMMA; MACROPHAGES; MICE, INBRED C57BL; MICROGLIA; MULTIPLE SCLEROSIS; NEUROIMMUNOMODULATION; NEUROPROTECTIVE AGENTS; PREGNANOLONE; RNA, MESSENGER; SPINAL CORD; T-LYMPHOCYTES; WHITE MATTER;

EID: 84901367691     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2014.04.037     Document Type: Article

References (56)

1. Acharjee S., Zhu Y., Maingat F., Pardo C., Ballanyi K., Hollenberg M.D., Power C. Proteinase-activated receptor-1 mediates dorsal root ganglion neuronal degeneration in HIV/AIDS. Brain 2011, 134:3209-3221.
2. Antony J.M., Ellestad K.K., Hammond R., Imaizumi K., Mallet F., Warren K.G., Power C. The human endogenous retrovirus envelope glycoprotein, syncytin-1, regulates neuroinflammation and its receptor expression in multiple sclerosis: a role for endoplasmic reticulum chaperones in astrocytes. J Immunol 2007, 179:1210-1224.
3. Barbaro Ade L., Tosi G., Frumento G., Bruschi E., D'Agostino A., Valle M.T., Manca F., Accolla R.S. Block of Stat-1 activation in macrophages phagocytosing bacteria causes reduced transcription of CIITA and consequent impaired antigen presentation. Eur J Immunol 2002, 32:1309-1318.
4. Belelli D., Lambert J.J. Neurosteroids: endogenous regulators of the GABA(A) receptor. Nat Rev Neurosci 2005, 6:565-575.
5. Bhat R., Axtell R., Mitra A., Miranda M., Lock C., Tsien R.W., Steinman L. Inhibitory role for GABA in autoimmune inflammation. Proc Natl Acad Sci U S A 2010, 107:2580-2585.
6. Carmans S., Hendriks J.J., Slaets H., Thewissen K., Stinissen P., Rigo J.M., Hellings N. Systemic treatment with the inhibitory neurotransmitter gamma-aminobutyric acid aggravates experimental autoimmune encephalomyelitis by affecting proinflammatory immune responses. J Neuroimmunol 2013, 255:45-53.
7. Carter R.B., Wood P.L., Wieland S., Hawkinson J.E., Belelli D., Lambert J.J., White H.S., Wolf H.H., Mirsadeghi S., Tahir S.H., Bolger M.B., Lan N.C., Gee K.W. Characterization of the anticonvulsant properties of ganaxolone (CCD 1042; 3alpha-hydroxy-3beta-methyl-5alpha-pregnan-20-one), a selective, high-affinity, steroid modulator of the gamma-aminobutyric acid(A) receptor. J Pharmacol Exp Ther 1997, 280:1284-1295.
8. Christiansen B., Meinild A.K., Jensen A.A., Brauner-Osborne H. Cloning and characterization of a functional human gamma-aminobutyric acid (GABA) transporter, human GAT-2. J Biol Chem 2007, 282:19331-19341.
9. Conti F., Zuccarello L.V., Barbaresi P., Minelli A., Brecha N.C., Melone M. Neuronal, glial, and epithelial localization of gamma-aminobutyric acid transporter 2, a high-affinity gamma-aminobutyric acid plasma membrane transporter, in the cerebral cortex and neighboring structures. J Comp Neurol 1999, 409:482-494.
10. Conti F., Minelli A., Melone M. GABA transporters in the mammalian cerebral cortex: localization, development and pathological implications. Brain Res Brain Res Rev 2004, 45:196-212.
11. Cordeiro J.M., Silva V.S., Oliveira C.R., Goncalves P.P. Aluminium-induced impairment of Ca2+ modulatory action on GABA transport in brain cortex nerve terminals. J Inorg Biochem 2003, 97:132-142.
12. Demakova E.V., Korobov V.P., Lemkina L.M. Determination of gamma-aminobutyric acid concentration and activity of glutamate decarboxylase in blood serum of patients with multiple sclerosis. Klin Lab Diagn 2003, 15-17.
13. Deslauriers A.M., Afkhami-Goli A., Paul A.M., Bhat R.K., Acharjee S., Ellestad K.K., Noorbakhsh F., Michalak M., Power C. Neuroinflammation and endoplasmic reticulum stress are coregulated by crocin to prevent demyelination and neurodegeneration. J Immunol 2011, 187:4788-4799.
14. Dionisio L., Jose De Rosa M., Bouzat C., Esandi Mdel C. An intrinsic GABAergic system in human lymphocytes. Neuropharmacology 2011, 60:513-519.
15. Eikelenboom P., Bate C., Van Gool W.A., Hoozemans J.J., Rozemuller J.M., Veerhuis R., Williams A. Neuroinflammation in Alzheimer's disease and prion disease. Glia 2002, 40:232-239.
16. Ellestad K.K., Tsutsui S., Noorbakhsh F., Warren K.G., Yong V.W., Pittman Q.J., Power C. Early life exposure to lipopolysaccharide suppresses experimental autoimmune encephalomyelitis by promoting tolerogenic dendritic cells and regulatory T cells. J Immunol 2009, 183:298-309.
17. Falkenstein E., Tillmann H.C., Christ M., Feuring M., Wehling M. Multiple actions of steroid hormones - a focus on rapid, nongenomic effects. Pharmacol Rev 2000, 52:513-556.
18. Ferkany J.W., Smith L.A., Seifert W.E., Caprioli R.M., Enna S.J. Measurement of gamma-aminobutyric acid (GABA) in blood. Life Sci 1978, 22:2121-2128.
19. Frohman E.M., Racke M.K., Raine C.S. Multiple sclerosis - the plaque and its pathogenesis. N Engl J Med 2006, 354:942-955.
20. Goncalves P.P., Meireles S.M., Vale M.G. Regulation of the gamma-aminobutyric acid transporter activity by protein phosphatases in synaptic plasma membranes. Neurosci Res 1999, 33:41-47.
21. Grant S.L., Shulman Y., Tibbo P., Hampson D.R., Baker G.B. Determination of d-serine and related neuroactive amino acids in human plasma by high-performance liquid chromatography with fluorimetric detection. J Chromatogr B Analyt Technol Biomed Life Sci 2006, 844:278-282.
22. Hosie A.M., Wilkins M.E., da Silva H.M., Smart T.G. Endogenous neurosteroids regulate GABAA receptors through two discrete transmembrane sites. Nature 2006, 444:486-489.
23. Houtchens M.K. Pregnancy and multiple sclerosis. Semin Neurol 2007, 27:434-441.
24. Jorgensen EM (2005), Gaba. WormBook, pp 1-13.
25. LeWitt P.A., Rezai A.R., Leehey M.A., Ojemann S.G., Flaherty A.W., Eskandar E.N., Kostyk S.K., Thomas K., Sarkar A., Siddiqui M.S., Tatter S.B., Schwalb J.M., Poston K.L., Henderson J.M., Kurlan R.M., Richard I.H., Van Meter L., Sapan C.V., During M.J., Kaplitt M.G., Feigin A. AAV2-GAD gene therapy for advanced Parkinson's disease: a double-blind, sham-surgery controlled, randomised trial. Lancet Neurol 2011, 10:309-319.
26. Linhoff M.W., Harton J.A., Cressman D.E., Martin B.K., Ting J.P. Two distinct domains within CIITA mediate self-association: involvement of the GTP-binding and leucine-rich repeat domains. Mol Cell Biol 2001, 21:3001-3011.
27. Liptakova S., Velisek L., Veliskova J., Moshe S.L. Effect of ganaxolone on flurothyl seizures in developing rats. Epilepsia 2000, 41:788-793.
28. Maingat F., Vivithanaporn P., Zhu Y., Taylor A., Baker G., Pearson K., Power C. Neurobehavioral performance in feline immunodeficiency virus infection: integrated analysis of viral burden, neuroinflammation, and neuronal injury in cortex. J Neurosci 2009, 29:8429-8437.
29. Mellon S.H., Gong W., Schonemann M.D. Endogenous and synthetic neurosteroids in treatment of Niemann-Pick Type C disease. Brain Res Rev 2008, 57:410-420.
30. Nickerson K., Sisk T.J., Inohara N., Yee C.S., Kennell J., Cho M.C., Yannie P.J., Nunez G., Chang C.H. Dendritic cell-specific MHC class II transactivator contains a caspase recruitment domain that confers potent transactivation activity. J Biol Chem 2001, 276:19089-19093.
31. Nigam R., El-Nour H., Amatya B., Nordlind K. GABA and GABA(A) receptor expression on immune cells in psoriasis: a pathophysiological role. Arch Dermatol Res 2010, 302:507-515.
32. Noorbakhsh F., Tsutsui S., Vergnolle N., Boven L.A., Shariat N., Vodjgani M., Warren K.G., Andrade-Gordon P., Hollenberg M.D., Power C. Proteinase-activated receptor 2 modulates neuroinflammation in experimental autoimmune encephalomyelitis and multiple sclerosis. J Exp Med 2006, 203:425-435.
33. Noorbakhsh F., Ellestad K.K., Maingat F., Warren K.G., Han M.H., Steinman L., Baker G.B., Power C. Impaired neurosteroid synthesis in multiple sclerosis. Brain 2011, 134:2703-2721.
34. Oestreich K.J., Weinmann A.S. Master regulators or lineage-specifying? Changing views on CD4+ T cell transcription factors. Nat Rev Immunol 2012, 12:799-804.
35. Power C., McArthur J.C., Nath A., Wehrly K., Mayne M., Nishio J., Langelier T., Johnson R.T., Chesebro B. Neuronal death induced by brain-derived human immunodeficiency virus type 1 envelope genes differs between demented and nondemented AIDS patients. J Virol 1998, 72:9045-9053.
36. Ram K., Lam G.N., Chien B. A high-performance liquid chromatography-tandem mass spectrometric method for the determination of pharmacokinetics of ganaxolone in rat, monkey, dog and human plasma. J Chromatogr B Biomed Sci Appl 2001, 751:49-59.
37. Reddy D.S. Neurosteroids: endogenous role in the human brain and therapeutic potentials. Prog Brain Res 2010, 186:113-137.
38. Reddy D.S., Rogawski M.A. Ganaxolone suppression of behavioral and electrographic seizures in the mouse amygdala kindling model. Epilepsy Res 2010, 89:254-260.
39. Reddy D.S., Woodward R. Ganaxolone: a prospective overview. Drugs Future 2004, 29:227-242.
40. Reyes-Garcia M.G., Hernandez-Hernandez F., Hernandez-Tellez B., Garcia-Tamayo F. GABA (A) receptor subunits RNA expression in mice peritoneal macrophages modulate their IL-6/IL-12 production. J Neuroimmunol 2007, 188:64-68.
41. Robel P., Baulieu E.E. Neurosteroids biosynthesis and function. Trends Endocrinol Metab 1994, 5:1-8.
42. Ruiz-Tachiquin M.E., Sanchez-Lemus E., Soria-Jasso L.E., Arias-Montano J.A., Ortega A. Gamma-aminobutyric acid transporter (BGT-1) expressed in human astrocytoma U373 MG cells: pharmacological and molecular characterization and phorbol ester-induced inhibition. J Neurosci Res 2002, 69:125-132.
43. Rupprecht R. The neuropsychopharmacological potential of neuroactive steroids. J Psychiatr Res 1997, 31:297-314.
44. Rupprecht R., Reul J.M., Trapp T., van Steensel B., Wetzel C., Damm K., Zieglgansberger W., Holsboer F. Progesterone receptor-mediated effects of neuroactive steroids. Neuron 1993, 11:523-530.
45. Schneider C.A., Rasband W.S., Eliceiri K.W. NIH Image to ImageJ: 25 years of image analysis. Nat Methods 2012, 9:671-675.
46. Shiratsuchi H., Kouatli Y., Yu G.X., Marsh H.M., Basson M.D. Propofol inhibits pressure-stimulated macrophage phagocytosis via the GABAA receptor and dysregulation of p130cas phosphorylation. Am J Physiol Cell Physiol 2009, 296:C1400-C1410.
47. Soltani N., Qiu H., Aleksic M., Glinka Y., Zhao F., Liu R., Li Y., Zhang N., Chakrabarti R., Ng T., Jin T., Zhang H., Lu W.Y., Feng Z.P., Prud'homme G.J., Wang Q. GABA exerts protective and regenerative effects on islet beta cells and reverses diabetes. Proc Natl Acad Sci U S A 2011, 108:11692-11697.
48. Soudijn W., van Wijngaarden I. The GABA transporter and its inhibitors. Curr Med Chem 2000, 7:1063-1079.
49. Stadelmann C. Multiple sclerosis as a neurodegenerative disease: pathology, mechanisms and therapeutic implications. Curr Opin Neurol 2011, 24:224-229.
50. Stuckey D.J., Anthony D.C., Lowe J.P., Miller J., Palm W.M., Styles P., Perry V.H., Blamire A.M., Sibson N.R. Detection of the inhibitory neurotransmitter GABA in macrophages by magnetic resonance spectroscopy. J Leukoc Biol 2005, 78:393-400.
51. Tansey M.G., Frank-Cannon T.C., McCoy M.K., Lee J.K., Martinez T.N., McAlpine F.E., Ruhn K.A., Tran T.A. Neuroinflammation in Parkinson's disease: is there sufficient evidence for mechanism-based interventional therapy?. Front Biosci 2008, 13:709-717.
52. Tian J., Yong J., Dang H., Kaufman D.L. Oral GABA treatment downregulates inflammatory responses in a mouse model of rheumatoid arthritis. Autoimmunity 2011, 44:465-470.
53. Tsutsui S., Schnermann J., Noorbakhsh F., Henry S., Yong V.W., Winston B.W., Warren K., Power C. A1 adenosine receptor upregulation and activation attenuates neuroinflammation and demyelination in a model of multiple sclerosis. J Neurosci 2004, 24:1521-1529.
54. Vivithanaporn P., Maingat F., Lin L.T., Na H., Richardson C.D., Agrawal B., Cohen E.A., Jhamandas J.H., Power C. Hepatitis C virus core protein induces neuroimmune activation and potentiates Human Immunodeficiency Virus-1 neurotoxicity. PLoS One 2010, 5:e12856.
55. Yeh W.I., McWilliams I.L., Harrington L.E. Autoreactive Tbet-positive CD4 T cells develop independent of classic Th1 cytokine signaling during experimental autoimmune encephalomyelitis. J Immunol 2011, 187:4998-5006.
56. Zhu Y., Vergote D., Pardo C., Noorbakhsh F., McArthur J.C., Hollenberg M.D., Overall C.M., Power C. CXCR3 activation by lentivirus infection suppresses neuronal autophagy: neuroprotective effects of antiretroviral therapy. FASEB J 2009, 23:2928-2941.