Cell Type-Specific Dependency on the PI3K/Akt Signaling Pathway for the Endogenous Epo and VEGF Induction by Baicalein in Neurons versus Astrocytes

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Sun, Yu Yo ^a   Lin, Shang Hsuan ^b   Lin, Hung Cheng ^c   Hung, Chia Chi ^c   Wang, Chen Yu ^b   Lin, Yen Chu ^b   Hung, Kuo Sheng ^c   Lien, Cheng Chang ^b   Kuan, Chia Yi ^a   Lee, Yi Hsuan ^b  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NATIONAL YANG MING UNIVERSITY   (Taiwan)

^c TAIPEI MEDICAL UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; BAICALEIN; ERYTHROPOIETIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; VASCULOTROPIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL TYPE; CONCENTRATION RESPONSE; CONTROLLED STUDY; EXCITOTOXICITY; FEMALE; GENETIC TRANSCRIPTION; NERVE CELL; NERVE CELL EXCITABILITY; NEUROPROTECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION;

ANIMALS; ASTROCYTES; CELLS, CULTURED; ENZYME INHIBITORS; ERYTHROPOIETIN; FEMALE; FLAVANONES; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MALE; NEURONS; NEUROPROTECTIVE AGENTS; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; TRANSCRIPTIONAL ACTIVATION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84880442452     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0069019     Document Type: Article

References (50)

1. Lee HH, Yang LL, Wang CC, Hu SY, Chang SF, et al. (2003) Differential effects of natural polyphenols on neuronal survival in primary cultured central neurons against glutamate- and glucose deprivation-induced neuronal death. Brain Res 986: 103-113. doi:10.1016/S0006-8993(03)03197-4. PubMed: 12965234.
2. Liu C, Wu J, Xu K, Cai F, Gu J, et al. (2010) Neuroprotection by baicalein in ischemic brain injury involves PTEN/AKT pathway. J Neurochem 112: 1500-1512. doi:10.1111/j.1471-4159.2009.06561.x. PubMed: 20050973.
3. van Leyen K, Kim HY, Lee SR, Jin G, Arai K, et al. (2006) Baicalein and 12/15-lipoxygenase in the ischemic brain. Stroke 37: 3014-3018. doi:10.1161/01.STR.0000249004.25444.a5. PubMed: 17053180.
4. Lapchak PA, Maher P, Schubert D, Zivin JA, (2007) Baicalein, an antioxidant 12/15-lipoxygenase inhibitor improves clinical rating scores following multiple infarct embolic strokes. Neuroscience 150: 585-591. doi:10.1016/j.neuroscience.2007.09.033. PubMed: 17942241.
5. Pallast S, Arai K, Wang X, Lo EH, van Leyen K, (2009) 12/15-Lipoxygenase targets neuronal mitochondria under oxidative stress. J Neurochem 111: 882-889. doi:10.1111/j.1471-4159.2009.06379.x. PubMed: 19737346.
6. Zaleska MM, Wilson DF, (1989) Lipid hydroperoxides inhibit reacylation of phospholipids in neuronal membranes. J Neurochem 52: 255-260. doi:10.1111/j.1471-4159.1989.tb10925.x. PubMed: 2491758.
7. Phillis JW, Horrocks LA, Farooqui AA, (2006) Cyclooxygenases, lipoxygenases, and epoxygenases in CNS: their role and involvement in neurological disorders. Brain Res Rev 52: 201-243. doi:10.1016/j.brainresrev.2006.02.002. PubMed: 16647138.
8. Jin G, Arai K, Murata Y, Wang S, Stins MF, et al. (2008) Protecting against cerebrovascular injury: contributions of 12/15-lipoxygenase to edema formation after transient focal ischemia. Stroke 39: 2538-2543. doi:10.1161/STROKEAHA.108.514927. PubMed: 18635843.
9. Cho H, Lee HY, Ahn DR, Kim SY, Kim S, et al. (2008) Baicalein induces functional hypoxia-inducible factor-1alpha and angiogenesis. Mol Pharmacol 74: 70-81. doi:10.1124/mol.107.040162. PubMed: 18426858.
10. Wang W, Wang F, Yang YJ, Hu ZL, Long LH, et al. (2011) The flavonoid baicalein promotes NMDA receptor-dependent long-term potentiation and enhances memory. Br J Pharmacol 162: 1364-1379. doi:10.1111/j.1476-5381.2010.01143.x. PubMed: 21133890.
11. Chan CB, Liu X, Pradoldej S, Hao C, An J, et al. (2011) Phosphoinositide 3-kinase enhancer regulates neuronal dendritogenesis and survival in neocortex. J Neurosci 31: 8083-8092. doi:10.1523/JNEUROSCI.1129-11.2011. PubMed: 21632930.
12. Vanhaesebroeck B, Guillermet-Guibert J, Graupera M, Bilanges B, (2010) The emerging mechanisms of isoform-specific PI3K signalling. Nat Rev Mol Cell Biol 11: 329-341. doi:10.1038/nrm2882. PubMed: 20379207.
13. Jiang BH, Jiang G, Zheng JZ, Lu Z, Hunter T, et al. (2001) Phosphatidylinositol 3-kinase signaling controls levels of hypoxia-inducible factor 1. Cell Growth Differ 12: 363-369. PubMed: 11457733.
14. Spinella F, Rosanò L, Del Duca M, Di Castro V, Nicotra MR, et al. (2010) Endothelin-1 inhibits prolyl hydroxylase domain 2 to activate hypoxia-inducible factor-1alpha in melanoma cells. PLOS ONE 5: e11241. doi:10.1371/journal.pone.0011241. PubMed: 20574527.
15. Sharp FR, Bernaudin M, (2004) HIF1 and oxygen sensing in the brain. Nat Rev Neurosci 5: 437-448. doi:10.1038/nrn1408. PubMed: 15152194.
16. Berra E, Benizri E, Ginouvès A, Volmat V, Roux D, et al. (2003) HIF prolyl-hydroxylase 2 is the key oxygen sensor setting low steady-state levels of HIF-1alpha in normoxia. EMBO J 22: 4082-4090. doi:10.1093/emboj/cdg392. PubMed: 12912907.
17. Kunze R, Zhou W, Veltkamp R, Wielockx B, Breier G, et al. (2012) Neuron-specific prolyl-4-hydroxylase domain 2 knockout reduces brain injury after transient cerebral ischemia. Stroke 43: 2748-2756. doi:10.1161/STROKEAHA.112.669598. PubMed: 22933585.
18. Ogle ME, Gu X, Espinera AR, Wei L, (2012) Inhibition of prolyl hydroxylases by dimethyloxaloylglycine after stroke reduces ischemic brain injury and requires hypoxia inducible factor-1alpha. Neurobiol Dis 45: 733-742. doi:10.1016/j.nbd.2011.10.020. PubMed: 22061780.
19. Dirnagl U, Becker K, Meisel A, (2009) Preconditioning and tolerance against cerebral ischaemia: from experimental strategies to clinical use. Lancet Neurol 8: 398-412. doi:10.1016/S1474-4422(09)70054-7. PubMed: 19296922.
20. Siddiq A, Ayoub IA, Chavez JC, Aminova L, Shah S, et al. (2005) Hypoxia-inducible factor prolyl 4-hydroxylase inhibition: a target for neuroprotection in the central nervous system. J Biol Chem 280: 41732-41743. doi:10.1074/jbc.M504963200. PubMed: 16227210.
21. Wang Y, Zhang ZG, Rhodes K, Renzi M, Zhang RL, et al. (2007) Post-ischemic treatment with erythropoietin or carbamylated erythropoietin reduces infarction and improves neurological outcome in a rat model of focal cerebral ischemia. Br J Pharmacol 151: 1377-1384. PubMed: 17603558.
22. Gunnarson E, Song Y, Kowalewski JM, Brismar H, Brines M, et al. (2009) Erythropoietin modulation of astrocyte water permeability as a component of neuroprotection. Proc Natl Acad Sci U S A 106: 1602-1607. doi:10.1073/pnas.0812708106. PubMed: 19164545.
23. Iwai M, Stetler RA, Xing J, Hu X, Gao Y, et al. (2010) Enhanced oligodendrogenesis and recovery of neurological function by erythropoietin after neonatal hypoxic/ischemic brain injury. Stroke 41: 1032-1037. doi:10.1161/STROKEAHA.109.570325. PubMed: 20360553.
24. Ehrenreich H, Weissenborn K, Prange H, Schneider D, Weimar C, et al. (2009) Recombinant human erythropoietin in the treatment of acute ischemic stroke. Stroke 40: e647-e656. doi:10.1161/STROKEAHA.109.564872. PubMed: 19834012.
25. Kilic E, Kilic U, Wang Y, Bassetti CL, Marti HH, et al. (2006) The phosphatidylinositol-3 kinase/Akt pathway mediates VEGF's neuroprotective activity and induces blood brain barrier permeability after focal cerebral ischemia. FASEB J 20: 1185-1187. doi:10.1096/fj.05-4829fje. PubMed: 16641198.
26. Mowat FM, Gonzalez F, Luhmann UF, Lange CA, Duran Y, et al. (2012) Endogenous erythropoietin protects neuroretinal function in ischemic retinopathy. Am J Pathol 180: 1726-1739. doi:10.1016/j.ajpath.2011.12.033. PubMed: 22342523.
27. Sun YY, Wang CY, Hsu MF, Juan SH, Chang CY, et al. (2010) Glucocorticoid protection of oligodendrocytes against excitotoxin involving hypoxia-inducible factor-1alpha in a cell-type-specific manner. J Neurosci 30: 9621-9630. PubMed: 20631191.
28. Rosenstein JM, Krum JM, Ruhrberg C, (2010) VEGF in the nervous system. Organogenesis 6. pp.: 107-114.
29. Sun FY, Guo X, (2005) Molecular and cellular mechanisms of neuroprotection by vascular endothelial growth factor. J Neurosci Res 79: 180-184. doi:10.1002/jnr.20321. PubMed: 15573409.
30. Argaw AT, Asp L, Zhang J, Navrazhina K, Pham T, et al. (2012) Astrocyte-derived VEGF-A drives blood-brain barrier disruption in CNS inflammatory disease. J Clin Invest 122: 2454-2468. doi:10.1172/JCI60842. PubMed: 22653056.
31. Liao JF, Hung WY, Chen CF, (2003) Anxiolytic-like effects of baicalein and baicalin in the Vogel conflict test in mice. Eur J Pharmacol 464: 141-146. doi:10.1016/S0014-2999(03)01422-5. PubMed: 12620506.
32. Sofroniew MV, (2009) Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci 32: 638-647. doi:10.1016/j.tins.2009.08.002. PubMed: 19782411.
33. Wu X, Kihara T, Akaike A, Niidome T, Sugimoto H, (2010) PI3K/Akt/mTOR signaling regulates glutamate transporter 1 in astrocytes. Biochem Biophys Res Commun 393: 514-518. doi:10.1016/j.bbrc.2010.02.038. PubMed: 20152809.
34. Lin MS, Hung KS, Chiu WT, Sun YY, Tsai SH, et al. (2011) Curcumin enhances neuronal survival in N-methyl-d-aspartic acid toxicity by inducing RANTES expression in astrocytes via PI-3K and MAPK signaling pathways. Prog Neuropsychopharmacol Biol Psychiatry 35: 931-938. doi:10.1016/j.pnpbp.2010.12.022. PubMed: 21199667.
35. Hwang KY, Oh YT, Yoon H, Lee J, Kim H, et al. (2008) Baicalein suppresses hypoxia-induced HIF-1alpha protein accumulation and activation through inhibition of reactive oxygen species and PI 3-kinase/Akt pathway in BV2 murine microglial cells. Neurosci Lett 444: 264-269. doi:10.1016/j.neulet.2008.08.057. PubMed: 18771709.
36. Pidgeon GP, Kandouz M, Meram A, Honn KV, (2002) Mechanisms controlling cell cycle arrest and induction of apoptosis after 12-lipoxygenase inhibition in prostate cancer cells. Cancer Res 62: 2721-2727. PubMed: 11980674.
37. Lee YH, Fang KM, Yang CM, Hwang HM, Chiu CT, et al. (2000) Kainic acid-induced neurotrophic activities in developing cortical neurons. J Neurochem 74: 2401-2411. PubMed: 10820201.
38. Lin MS, Sun YY, Chiu WT, Hung CC, Chang CY, et al. (2011) Curcumin Attenuates the Expression and Secretion of RANTES after Spinal Cord Injury In Vivo and Lipopolysaccharide-Induced Astrocyte Reactivation In Vitro. J Neurotrauma 28: 1259-1269. doi:10.1089/neu.2011.1768. PubMed: 21529317.
39. Lin CH, Chen CC, Chou CM, Wang CY, Hung CC, et al. (2009) Knockdown of the aryl hydrocarbon receptor attenuates excitotoxicity and enhances NMDA-induced BDNF expression in cortical neurons. J Neurochem 111: 777-789. doi:10.1111/j.1471-4159.2009.06364.x. PubMed: 19712055.
40. Weng JY, Lin YC, Lien CC, (2010) Cell type-specific expression of acid-sensing ion channels in hippocampal interneurons. J Neurosci 30: 6548-6558. doi:10.1523/JNEUROSCI.0582-10.2010. PubMed: 20463218.
41. Sutton G, Chandler LJ, (2002) Activity-dependent NMDA receptor-mediated activation of protein kinase B/Akt in cortical neuronal cultures. J Neurochem 82: 1097-1105. PubMed: 12358757.
42. Davies SP, Reddy H, Caivano M, Cohen P, (2000) Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem J 351: 95-105. doi:10.1042/0264-6021:3510095. PubMed: 10998351.
43. Chao CC, Ma YL, Lee EH, (2011) Brain-derived neurotrophic factor enhances Bcl-xL expression through protein kinase casein kinase 2-activated and nuclear factor kappa B-mediated pathway in rat hippocampus. Brain Pathol 21: 150-162. doi:10.1111/j.1750-3639.2010.00431.x. PubMed: 20731656.
44. Chavez JC, Baranova O, Lin J, Pichiule P, (2006) The transcriptional activator hypoxia inducible factor 2 (HIF-2/EPAS-1) regulates the oxygen-dependent expression of erythropoietin in cortical astrocytes. J Neurosci 26: 9471-9481. doi:10.1523/JNEUROSCI.2838-06.2006. PubMed: 16971531.
45. Mowat FM, Luhmann UF, Smith AJ, Lange C, Duran Y, et al. (2010) HIF-1alpha and HIF-2alpha are differentially activated in distinct cell populations in retinal ischaemia. PLOS ONE 5: e11103. doi:10.1371/journal.pone.0011103. PubMed: 20559438.
46. Kong D, Yamazaki K, Yamori T, (2010) Discovery of phosphatidylinositol 3-kinase inhibitory compounds from the Screening Committee of Anticancer Drugs (SCADS) library. Biol Pharm Bull 33: 1600-1604. doi:10.1248/bpb.33.1600. PubMed: 20823581.
47. Williams RJ, Spencer JP, (2012) Flavonoids, cognition, and dementia: actions, mechanisms, and potential therapeutic utility for Alzheimer disease. Free Radic Biol Med 52: 35-45. doi:10.1016/j.freeradbiomed.2011.09.010. PubMed: 21982844.
48. Viita H, Markkanen J, Eriksson E, Nurminen M, Kinnunen K, et al. (2008) 15-lipoxygenase-1 prevents vascular endothelial growth factor A- and placental growth factor-induced angiogenic effects in rabbit skeletal muscles via reduction in growth factor mRNA levels, NO bioactivity, and downregulation of VEGF receptor 2 expression. Circ Res 102: 177-184. doi:10.1161/CIRCRESAHA.107.155556. PubMed: 17991885.
49. Tang Y, Wang MT, Chen Y, Yang D, Che M, et al. (2009) Downregulation of vascular endothelial growth factor and induction of tumor dormancy by 15-lipoxygenase-2 in prostate cancer. Int J Cancer 124: 1545-1551. doi:10.1002/ijc.24118. PubMed: 19089921.
50. Tsai TH, Liu SC, Tsai PL, Ho LK, Shum AY, et al. (2002) The effects of the cyclosporin A, a P-glycoprotein inhibitor, on the pharmacokinetics of baicalein in the rat: a microdialysis study. Br J Pharmacol 137: 1314-1320. doi:10.1038/sj.bjp.0704959. PubMed: 12466241.