Mechanism of raloxifene-induced upregulation of glutamate transporters in rat primary astrocytes

GLIA

Volumn 62, Issue 8, 2014, Pages 1270-1283

  Karki, Pratap ^a   Webb, Anton ^a   Zerguine, Abdelbassat ^a   Choi, Joseph ^a   Son, Deok Soo ^a   Lee, Eunsook ^a  

^a MEHARRY MEDICAL COLLEGE   (United States)

Author keywords

Estrogen receptors; GLAST; GLT 1; Manganese; NF B; Raloxifene

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; G PROTEIN COUPLED RECEPTOR 30; GLUTAMATE TRANSPORTER; GLUTAMIC ACID; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MANGANESE; MESSENGER RNA; PROTEIN P50; RALOXIFENE; SYNAPTOTAGMIN I; CYCLIC AMP DEPENDENT PROTEIN KINASE; EGFR PROTEIN, RAT; EXCITATORY AMINO ACID TRANSPORTER 1; EXCITATORY AMINO ACID TRANSPORTER 2; G PROTEIN COUPLED RECEPTOR; GPR30 PROTEIN, RAT; SELECTIVE ESTROGEN RECEPTOR MODULATOR; SLC1A2 PROTEIN, RAT; SLC1A3 PROTEIN, RAT;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; ASTROCYTE; CONTROLLED STUDY; DEGENERATIVE DISEASE; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; CELL CULTURE; DRUG EFFECTS; GENETIC TRANSCRIPTION; METABOLISM; SPRAGUE DAWLEY RAT;

ANIMALS; ASTROCYTES; CELLS, CULTURED; CYCLIC AMP-DEPENDENT PROTEIN KINASES; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; EXCITATORY AMINO ACID TRANSPORTER 1; EXCITATORY AMINO ACID TRANSPORTER 2; MAP KINASE SIGNALING SYSTEM; NF-KAPPA B; RALOXIFENE; RATS, SPRAGUE-DAWLEY; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTORS, G-PROTEIN-COUPLED; RNA, MESSENGER; SELECTIVE ESTROGEN RECEPTOR MODULATORS; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC; UP-REGULATION;

EID: 84902331100     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22679     Document Type: Article

References (66)

1. Abdelhamid R, Luo J, Vandevrede L, Kundu I, Michalsen B, Litosh VA, Schiefer IT, Gherezghiher T, Yao P, Qin Z, Thatcher GR. 2011. Benzothiophene selective estrogen receptor modulators provide neuroprotection by a novel GPR30-dependent mechanism. ACS Chem Neurosci 2:256-268.
2. Arevalo MA, Santos-Galindo M, Lagunas N, Azcoitia I, Garcia-Segura LM. 2011. Selective estrogen receptor modulators as brain therapeutic agents. J Mol Endocrinol 46:R1-9.
3. Aschner M, Gannon M, Kimelberg HK. 1992. Manganese uptake and efflux in cultured rat astrocytes. J Neurochem 58:730-735.
4. Baltan S, Murphy SP, Danilov CA, Bachleda A, Morrison RS. 2011. Histone deacetylase inhibitors preserve white matter structure and function during ischemia by conserving ATP and reducing excitotoxicity. J Neurosci 31:3990-3999.
5. Behar TN, Scott CA, Greene CL, Wen X, Smith SV, Maric D, Liu QY, Colton CA, Barker JL. 1999. Glutamate acting at NMDA receptors stimulates embryonic cortical neuronal migration. J Neurosci 19:4449-4461.
6. Behl C, Skutella T, Lezoualc'h F, Post A, Widmann M, Newton CJ, Holsboer F. 1997. Neuroprotection against oxidative stress by estrogens: structure-activity relationship. Mol Pharmacol 51:535-541.
7. Bowman AB, Kwakye GF, Hernandez EH, Aschner M. 2011. Role of manganese in neurodegenerative diseases. J Trace Elem Med Biol 25:191-203.
8. Brann DW, Dhandapani K, Wakade C, Mahesh VB, Khan MM. 2007. Neurotrophic and neuroprotective actions of estrogen: Basic mechanisms and clinical implications. Steroids 72:381-405.
9. Brinton RD. 2002. Selective estrogen receptor modulators (SERM) for the brain: Recent advances and remaining challenges for developing a NeuroSERM™. Drug Dev Res 56:380-392.
10. Canonico M, Plu-Bureau G, Lowe GD, Scarabin PY. 2008. Hormone replacement therapy and risk of venous thromboembolism in postmenopausal women: systematic review and meta-analysis. BMJ 336:1227-1231.
11. Cerciat M, Unkila M, Garcia-Segura LM, Arevalo MA. 2010. Selective estrogen receptor modulators decrease the production of interleukin-6 and interferon-gamma-inducible protein-10 by astrocytes exposed to inflammatory challenge in vitro. Glia 58:93-102.
12. Ciriza I, Carrero P, Azcoitia I, Lundeen SG, Garcia-Segura LM. 2004. Selective estrogen receptor modulators protect hippocampal neurons from kainic acid excitotoxicity: differences with the effect of estradiol. J Neurobiol 61:209-221.
13. Clemett D, Spencer CM. 2000. Raloxifene: A review of its use in postmenopausal osteoporosis. Drugs 60:379-411.
14. D'Amelio P, Isaia GC. 2013. The use of raloxifene in osteoporosis treatment. Expert Opin Pharmacother 14:949-956.
15. Dai X, Wu J, Sun X-p, Gao L, Cui Y-g, Liu J-y. 2012. Neuroprotective effects of raloxifene on Aβ25-35-induced damages in PC12 cells via mitogen-activated protein kinase signaling pathway. J Reprod Contracept 23:1-16.
16. Danbolt NC. 2001. Glutamate uptake. Prog Neurobiol 65:1-105.
17. Dhandapani KM, Brann DW. 2002. Protective effects of estrogen and selective estrogen receptor modulators in the brain. Biol Reprod 67:1379-1385.
18. DonCarlos LL, Azcoitia I, Garcia-Segura LM. 2009. Neuroprotective actions of selective estrogen receptor modulators. Psychoneuroendocrinology 34 Suppl 1:S113-122.
19. Du B, Ohmichi M, Takahashi K, et al. 2004. Both estrogen and raloxifene protect against beta-amyloid-induced neurotoxicity in estrogen receptor alpha-transfected PC12 cells by activation of telomerase activity via Akt cascade. J Endocrinol 183:605-615.
20. Erikson KM, Dorman DC, Lash LH, Aschner M. 2007. Manganese inhalation by rhesus monkeys is associated with brain regional changes in biomarkers of neurotoxicity. Toxicol Sci 97:459-466.
21. Fang M, Wu XC, Huang W. 2013. Raloxifene upregulated mesangial cell MMP-2 activity via ER-beta through transcriptional regulation. Cell Biochem Biophys 67:607-613.
22. Fattorini G, Melone M, Bragina L, Candiracci C, Cozzi A, Pellegrini Giampietro DE, Torres-Ramos M, Perez-Samartin A, Matute C, Conti F. 2008. GLT-1 expression and Glu uptake in rat cerebral cortex are increased by phencyclidine. Glia 56:1320-1327.
23. Honda K, Sawada H, Kihara T, Urushitani M, Nakamizo T, Akaike A, Shimohama S. 2000. Phosphatidylinositol 3-kinase mediates neuroprotection by estrogen in cultured cortical neurons. J Neurosci Res 60:321-327.
24. Jacobsen DE, Samson MM, Emmelot-Vonk MH, Verhaar HJ. 2010. Raloxifene improves verbal memory in late postmenopausal women: a randomized, double-blind, placebo-controlled trial. Menopause 17:309-314.
25. Jayakumar AR, Panickar KS, Murthy Ch R, Norenberg MD. 2006. Oxidative stress and mitogen-activated protein kinase phosphorylation mediate ammonia-induced cell swelling and glutamate uptake inhibition in cultured astrocytes. J Neurosci 26:4774-4784.
26. Ji YF, Zhou L, Xie YJ, Xu SM, Zhu J, Teng P, Shao CY, Wang Y, Luo JH, Shen Y. 2013. Upregulation of glutamate transporter GLT-1 by mTOR-Akt-NF-small ka, CyrillicB cascade in astrocytic oxygen-glucose deprivation. Glia 61:1959-1975.
27. Kajta M, Beyer C. 2003. Cellular strategies of estrogen-mediated neuroprotection during brain development. Endocrine 21:3-9.
28. Karki P, Webb A, Smith K, Johnson J, Jr., Lee K, Son DS, Aschner M, Lee E. 2014. Yin Yang 1 Is a Repressor of Glutamate Transporter EAAT2, and It Mediates Manganese-Induced Decrease of EAAT2 Expression in Astrocytes. Mol Cell Biol 34:1280-1289.
29. Karki P, Webb A, Smith K, Lee K, Son DS, Aschner M, Lee E. 2013. cAMP response element-binding protein (CREB) and nuclear factor kappaB mediate the tamoxifen-induced up-regulation of glutamate transporter 1 (GLT-1) in rat astrocytes. J Biol Chem 288:28975-28986.
30. Kawahara K, Hosoya R, Sato H, Tanaka M, Nakajima T, Iwabuchi S. 2002. Selective blockade of astrocytic glutamate transporter GLT-1 with dihydrokainate prevents neuronal death during ouabain treatment of astrocyte/neuron cocultures. Glia 40:337-349.
31. Kim K, Lee SG, Kegelman TP, et al. 2011. Role of excitatory amino acid transporter-2 (EAAT2) and glutamate in neurodegeneration: Opportunities for developing novel therapeutics. J Cell Physiol 226:2484-2493.
32. Lebesgue D, Chevaleyre V, Zukin RS, Etgen AM. 2009. Estradiol rescues neurons from global ischemia-induced cell death: multiple cellular pathways of neuroprotection. Steroids 74:555-561.
33. Lee E, Sidoryk-Wegrzynowicz M, Wang N, Webb A, Son DS, Lee K, Aschner M. 2012a. GPR30 regulates glutamate transporter GLT-1 expression in rat primary astrocytes. J Biol Chem 287:26817-26828.
34. Lee E, Sidoryk-Wegrzynowicz M, Yin Z, Webb A, Son DS, Aschner M. 2012b. Transforming growth factor-alpha mediates estrogen-induced upregulation of glutamate transporter GLT-1 in rat primary astrocytes. Glia 60:1024-1036.
35. Lee ES, Sidoryk M, Jiang H, Yin Z, Aschner M. 2009a. Estrogen and tamoxifen reverse manganese-induced glutamate transporter impairment in astrocytes. J Neurochem 110:530-544.
36. Lee ES, Yin Z, Milatovic D, Jiang H, Aschner M. 2009b. Estrogen and tamoxifen protect against Mn-induced toxicity in rat cortical primary cultures of neurons and astrocytes. Toxicol Sci 110:156-167.
37. Lee SA, Kim EY, Jeon WK, Woo CH, Choe J, Han S, Kim BC. 2011. The inhibitory effect of raloxifene on lipopolysaccharide-induced nitric oxide production in RAW264.7 cells is mediated through a ROS/p38 MAPK/CREB pathway to the up-regulation of heme oxygenase-1 independent of estrogen receptor. Biochimie 93:168-174.
38. Lee SG, Su ZZ, Emdad L, Gupta P, Sarkar D, Borjabad A, Volsky DJ, Fisher PB. 2008. Mechanism of ceftriaxone induction of excitatory amino acid transporter-2 expression and glutamate uptake in primary human astrocytes. J Biol Chem 283:13116-13123.
39. Lewis JS, Jordan VC. 2005. Selective estrogen receptor modulators (SERMs): Mechanisms of anticarcinogenesis and drug resistance. Mutat Res 591:247-263.
40. Lin CL, Kong Q, Cuny GD, Glicksman MA. 2012. Glutamate transporter EAAT2: A new target for the treatment of neurodegenerative diseases. Future Med Chem 4:1689-1700.
41. Littleton-Kearney MT, Ostrowski NL, Cox DA, Rossberg MI, Hurn PD. 2002. Selective estrogen receptor modulators: tissue actions and potential for CNS protection. CNS Drug Rev 8:309-330.
42. Moen MD, Keating GM. 2008. Raloxifene: a review of its use in the prevention of invasive breast cancer. Drugs 68:2059-2083.
43. Mutkus L, Aschner JL, Fitsanakis V, Aschner M. 2005. The in vitro uptake of glutamate in GLAST and GLT-1 transfected mutant CHO-K1 cells is inhibited by manganese. Biol Trace Elem Res 107:221-230.
44. Pawlak J, Brito V, Kuppers E, Beyer C. 2005. Regulation of glutamate transporter GLAST and GLT-1 expression in astrocytes by estrogen. Brain Res Mol Brain Res 138:1-7.
45. Persson I, Weiderpass E, Bergkvist L, Bergstrom R, Schairer C. 1999. Risks of breast and endometrial cancer after estrogen and estrogen-progestin replacement. Cancer Causes Control 10:253-260.
46. Rosas S, Vargas MA, Lopez-Bayghen E, Ortega A. 2007. Glutamate-dependent transcriptional regulation of GLAST/EAAT1: A role for YY1. J Neurochem 101:1134-1144.
47. Scarabin-Carre V, Canonico M, Brailly-Tabard S, et al. 2012. High level of plasma estradiol as a new predictor of ischemic arterial disease in older postmenopausal women: The three-city cohort study. J Am Heart Assoc 1:e001388.
48. Sheldon AL, Robinson MB. 2007. The role of glutamate transporters in neurodegenerative diseases and potential opportunities for intervention. Neurochem Int 51:333-355.
49. Singer CA, Figueroa-Masot XA, Batchelor RH, Dorsa DM. 1999. The mitogen-activated protein kinase pathway mediates estrogen neuroprotection after glutamate toxicity in primary cortical neurons. J Neurosci 19:2455-2463.
50. Singh M. 2001. Ovarian hormones elicit phosphorylation of Akt and extracellular-signal regulated kinase in explants of the cerebral cortex. Endocrine 14:407-415.
51. Singh M, Setalo G Jr., Guan X, Frail DE, Toran-Allerand CD. 2000. Estrogen-induced activation of the mitogen-activated protein kinase cascade in the cerebral cortex of estrogen receptor-alpha knock-out mice. J Neurosci 20:1694-1700.
52. Sitcheran R, Gupta P, Fisher PB, Baldwin AS. 2005. Positive and negative regulation of EAAT2 by NF-kappaB: A role for N-myc in TNFalpha-controlled repression. EMBO J 24:510-520.
53. Slatore CG, Chien JW, Au DH, Satia JA, White E. 2010. Lung cancer and hormone replacement therapy: association in the vitamins and lifestyle study. J Clin Oncol 28:1540-1546.
54. Srivastava DP, Waters EM, Mermelstein PG, Kramar EA, Shors TJ, Liu F. 2011. Rapid estrogen signaling in the brain: Implications for the fine-tuning of neuronal circuitry. J Neurosci 31:16056-16063.
55. Stice JP, Mbai FN, Chen L, Knowlton AA. 2012. Rapid activation of nuclear factor kappaB by 17beta-estradiol and selective estrogen receptor modulators: Pathways mediating cellular protection. Shock 38:128-136.
56. Su ZZ, Leszczyniecka M, Kang DC, Sarkar D, Chao W, Volsky DJ, Fisher PB. 2003. Insights into glutamate transport regulation in human astrocytes: cloning of the promoter for excitatory amino acid transporter 2 (EAAT2). Proc Natl Acad Sci USA 100:1955-1960.
57. Tai YH, Tsai RY, Wang YH, Cherng CH, Tao PL, Liu TM, Wong CS. 2008. Amitriptyline induces nuclear transcription factor-kappaB-dependent glutamate transporter upregulation in chronic morphine-infused rats. Neuroscience 153:823-831.
58. Thomas P, Pang Y, Filardo EJ, Dong J. 2005. Identity of an estrogen membrane receptor coupled to a G protein in human breast cancer cells. Endocrinology 146:624-632.
59. Ullensvang K, Lehre KP, Storm-Mathisen J, Danbolt NC. 1997. Differential developmental expression of the two rat brain glutamate transporter proteins GLAST and GLT. Eur J Neurosci 9:1646-1655.
60. Vogel VG, Costantino JP, Wickerham DL, et al. 2006. Effects of tamoxifen vs raloxifene on the risk of developing invasive breast cancer and other disease outcomes: The NSABP Study of Tamoxifen and Raloxifene (STAR) P-2 trial. JAMA 295:2727-2741
61. Yaffe K, Krueger K, Cummings SR, Blackwell T, Henderson VW, Sarkar S, Ensrud K, Grady D. 2005. Effect of raloxifene on prevention of dementia and cognitive impairment in older women: The Multiple Outcomes of Raloxifene Evaluation (MORE) randomized trial. Am J Psychiatry 162:683-690.
62. Yalcin A, Kanit L, Durmaz G, Sargin S, Terek CH, Tanyolac B. 2005. Altered level of apurinic/apyrimidinic endonuclease/redox factor-1 (APE/REF-1) mRNA in the hippocampus of ovariectomized rats treated by raloxifene against kainic acid. Clin Exp Pharmacol Physiol 32:611-614.
63. Zhang L, Rubinow DR, Xaing G, Li BS, Chang YH, Maric D, Barker JL, Ma W. 2001. Estrogen protects against beta-amyloid-induced neurotoxicity in rat hippocampal neurons by activation of Akt. Neuroreport 12:1919-1923.
64. Zhang Y, Milatovic D, Aschner M, Feustel PJ, Kimelberg HK. 2007. Neuroprotection by tamoxifen in focal cerebral ischemia is not mediated by an agonist action at estrogen receptors but is associated with antioxidant activity. Exp Neurol 204:819-827.
65. Zhao L, O'Neill K, Diaz Brinton R. 2005. Selective estrogen receptor modulators (SERMs) for the brain: Current status and remaining challenges for developing NeuroSERMs. Brain Res Brain Res Rev 49:472-493.
66. Zhao L, Wu TW, Brinton RD. 2004. Estrogen receptor subtypes alpha and beta contribute to neuroprotection and increased Bcl-2 expression in primary hippocampal neurons. Brain Res 1010:22-34.