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Journal of Neural Transmission

Erschienen in:

02.06.2017 | Translational Neurosciences - Original Article

Type B and A monoamine oxidase and their inhibitors regulate the gene expression of Bcl-2 and neurotrophic factors in human glioblastoma U118MG cells: different signal pathways for neuroprotection by selegiline and rasagiline

verfasst von: Keiko Inaba-Hasegawa, Masayo Shamoto-Nagai, Wakako Maruyama, Makoto Naoi

Erschienen in: Journal of Neural Transmission | Ausgabe 9/2017

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Abstract

Type B monoamine oxidase (MAO-B) in glial cells has been considered to be associated with neuronal death in Parkinson’s disease. MAO-B inhibitors, rasagiline and selegiline [(−)deprenyl], protect neurons in animal and cellular models of neurodegeneration. However, the role of MAO-B itself in the regulation of cell death processing remains elusive, whereas type A MAO (MAO-A) mediates the induction of anti-apoptotic Bcl-2 genes by rasagiline and selegiline. In this paper, the involvement of MAOs in the induction of neuroprotective genes by MAO inhibitors was investigated in human glioblastoma U118MG cells expressing mainly MAO-B. Selegiline significantly increased Mao-B, which was suppressed by Mao-A knockdown with short interfering (si)RNA, whereas rasagiline less markedly increased Mao-B, which was not affected by Mao-A knockdown. Mao-A mRNA was also markedly increased by rasagiline and selegiline, and Mao-B knockdown significantly enhanced the induction by selegiline, but not by rasagiline. Mao-B knockdown also significantly increased mRNA levels of Bcl-2, brain-derived neurotrophic factor (BDNF) and glial cell line-derived neurotrophic factor (GDNF). Selegiline synergistically enhanced the expression of these genes in Mao-B knockdown cells, but Mao-A knockdown suppressed the increase. Rasagiline increased BDNF and GDNF, which Mao-B and Mao-A knockdown inhibited. These results show that MAO-B might function as a repressor and MAO-A as a mediator in the constitutional expression of pro-survival genes, and that MAO-B and MAO-A might regulate different signal pathways for rasagiline and selegiline to induce neuroprotective genes. The novel role of glial MAOs in the regulation of gene expression is discussed.

Bar Am O, Amit T, Youdim MBH (2004) Contrasting neuroprotective and neurotoxic actions of respective metabolites of anti-Parkinson drugs rasagiline and selegiline. Neurosci Lett 355(3):169–172CrossRefPubMed

Bortolato M, Chen K, Shih JC (2008) Monoamine inactivation: from pathophysiology to therapeutics. Adv Drug Deliv Rev 60(13–14):1527–1533CrossRefPubMedPubMedCentral

Chen Z, Trapp B (2016) Microglia and neuroprotection. J Neurochem 136(Suppl 1):10–17CrossRefPubMed

Chen K, Ou XM, Chen G, Choi SH, Shih JC (2005) R1, a novel receptor of the human monoamine oxidase A. J Biol Chem 280(12):11552–11559CrossRefPubMedPubMedCentral

Damier P, Kastner A, Agid Y, Hirsch EC (1996) Does monoamine oxidase type B play a role in dopaminergic nerve cell death in Parkinson’s disease? Neurology 46(5):1262–1269CrossRefPubMed

De Girolamo LA, Hargreaves AJ, Billett EE (2001) Protection from MPTP-induced neurotoxicity in differentiating mouse N2a neuroblastoma cells. J Neurochem 78(3):650–660

De Zutter GS, Davis RJ (2001) Pro-apoptotic gene expression mediated by the p38 mitogen-activated protein kinase signal transduction pathway. Proc Natl Acad Sci USA 98(11):6168–6173CrossRefPubMedPubMedCentral

Ekblom J, Oreland L, Chen K, Shih JC (1998) Is there a “non-MAO” macromolecular target for l-deprenyl?: studies on MAOB mutant mice. Life Sci 63(2):181–186

Fitzgerald JC, Ugun-Klusek A, Allen G, De Cirolamo LA, Hargreaves I, Ufer C, Abramov AY, Billett EE (2014) Monoamine oxidase-A knockdown in human neuroblastoma cells reveals protection against mitochondrial toxins. FASEB J 28(1):218–229CrossRefPubMed

Holschneider DP, Scremin OU, Huynh L, Chen K, Shih JC (1999) Lack of protection from ischemic injury of monoamine oxidase B-deficient mice following middle cerebral artery occlusion. Neurosci Lett 259(3):161–164CrossRefPubMed

Inaba-Hasegawa K, Akao Y, Maruyama W, Naoi M (2012) Type A monoamine oxidase is associated with induction of neuroprotective Bcl-2 by rasagiline, an inhibitor of type B monoamine oxidase. J Neural Transm 119(4):405–414CrossRefPubMed

Inaba-Hasegawa K, Akao Y, Maruyama W, Naoi M (2013) Rasagiline and selegiline, inhibitors of type B monoamine oxidase, induce type A monoamine oxidase in human SH-SY5Y cells. J Neural Transm 120(3):435–444CrossRefPubMed

Jenner P, Olanow CW (1996) Oxidative stress and the pathogenesis of Parkinson’s disease. Neurology 47(Suppl 3):S161–S170CrossRefPubMed

Juric DM, Miklic S, Carman-Krzan M (2006) Monoaminergic neuronal activity up-regulates BDNF synthesis in cultured neonatal rat astrocytes. Brain Res 1108:54–62CrossRefPubMed

Juric DM, Loncar D, Carman-Lrzan M (2008) Noradrenergic stimulation of BDNF synthesis in astrocytes: mediation via α1- and β1/β2-adrenergic receptors. Neurochem Int 52(1–2):297–306CrossRefPubMed

Kajitani N, Hisaoka-Nakanishi K, Morioka N, Okada-Tsuchiuoka M, Kaneko M, Kasai M, Shibasaki C, Nakata Y, Takebayashi M (2012) Antidepressant acts on astrocytes leading to an increase in the expression of neurotrophic/growth factors: different regulation of FGF-2 by noradrenalin. PLoS One 7(12):e51197CrossRefPubMedPubMedCentral

Kraml M (1965) A rapid microfluorometric determination of monoamine oxidase. Biochem Pharmacol 14:1684–1686CrossRef

Magyar K (2011) Pharmacology of selegiline. Int Rev Neurobiol 100:65–84CrossRefPubMed

Mallajosyula JK, Kauer AD, Chinta SJ, Rajagopalan S, Rane A, Nicholis DG, Di Monte DA, Macarthour H, Andersen JA (2008) MAO-B elevation in mouse brain astrocytes results in Parkinson’s pathology. PLoS One 3:e1616CrossRefPubMedPubMedCentral

Malorni W, Giammarioli AM, Matarrese P, Pieryrangeli P, Agostinelli E, Cianccio A, Grassilli E, Mondovi B (1998) Protection against apoptosis by monoamine oxidase A inhibitors. FEBS Lett 426(1):155–159CrossRefPubMed

Marcocci L, de Marchi U, Salvi M, Milella ZG, Nocera S, Agostinelli E, Mondovi B, Toninello A (2002) Tyramine and monoamine oxidase inhibitors as modulators of the mitochondrial membrane permeability transition. J Membr Biol 188(1):12–31CrossRef

Maruyama W, Naoi M (2010) “70th birthday Professor Riederer” induction of glial cell-line-derived and brain-derived neurotrophic factors by rasagiline and (−)deprenyl: a way to a disease-modifying therapy? J Neural Transm 120(1):83–89CrossRef

Maruyama W, Nitta A, Shamoto-Nagai M, Hirata Y, Akao Y, Youdim M, Furukawa S, Nabeshima T, Naoi M (2004) N-Propargyl-1-(R)-aminoindan, rasagiline, increases glial cell line-derived neurotrophic factor (GDNF) in neuroblastoma SH-SY5Y cells through activation of NF-κB transcription factor. Neurochem Int 44(6):293–400CrossRef

Miklic S, Juric DM, Caman-Krzan M (2004) Differences in the regulation of BDNF and NGF synthesis in cultured neonatal rat astrocytes. Int J Dev Neurosci 22(3):119–130CrossRefPubMed

Mizuta I, Ohta M, Ohta K, Nishimura M, Mizuta E, Hayashi K, Kuno S (2000) Selegiline and desmethylselegiline stimulate NGF, BDNF and GDNF synthesis in cultured mouse astrocytes. Biochem Biophys Res Commun 279(3):751–755CrossRefPubMed

Mosley RL, Benner EJ, Kadiu I, Thomas M, Boska MD, Hasan K, Laurie C, Gendelman HE (2006) Neuroinflammation, oxidative stress and the pathogenesis of Parkinson’s disease. Clin Neurosci Res 6(5):261–281CrossRefPubMedPubMedCentral

Naoi M, Maruyama W, Inaba-Hasegawa K (2012) Type A and B monoamine oxidase in age-related neurodegenerative disorders. Their distinct roles in neuronal death and survival. Curr Top Med Chem 12(20):2177–2188CrossRefPubMed

Naoi M, Maruyama W, Inaba-Hasegawa K (2013a) Revelation in neuroprotective functions of rasagiline and selegiline: the induction of distinct genes by different mechanisms. Expert Rev Neurother 13(6):671–684CrossRefPubMed

Naoi M, Maruyama W, Yi H (2013b) Rasagiline prevents apoptosis induced by PK11195, a ligand of the outer membrane translocator protein (18 kDa), in SH-SH5Y cells through suppression of cytochrome c release from mitochondria. J Neural Transm 120(11):1539–1551CrossRefPubMed

Naoi M, Riederer P, Maruyama W (2016) Modulation of monoamine oxidase (MAO) expression in neuropsychiatric disorders: genetic and environmental factors involved in type A MAO expression. J Neural Transm 123(2):91–106CrossRefPubMed

Naoi M, Maruyama W, Shamoto-Nagai M (2017) Type A monoamine oxidase and serotonin are coordinately involved in depressive disorders: from neurotransmitter imbalance to impaired neurogenesis. J Neural Transm. doi:10.1007/s00702-017-1709-8

Ohta K, Kuno S, Inoue S, Ikeda E, Fujinami A, Ohta M (2010) The effect of dopamine agonists; the expression of GDNF, NGF, and BDNF in cultured mouse astrocytes. J Neurol Sci 291(1–2):12–26CrossRefPubMed

Ou X-M, Chen K, Shih JC (2004) Dual functions of transcription factors, transforming growth factor-beta-inducible early gene (TIEG)2 and Sp3, are mediated by CACCC element and Sp1 sites of human monoamine oxidase (MAO) B gene. J Biol Chem 279(20):21021–21028CrossRefPubMed

Ou X-M, Stockmeier CA, Meltzer HY et al (2010) A novel role for GADPDH-MAO B cascade in ethanol-induced cellular damage. Biol Psychiatry 67(9):855–863CrossRefPubMed

Rappold PM, Tieu K (2010) Astrocytes and therapeutics for Parkinson’s disease. Neurotherapeutics 7(4):413–423CrossRefPubMedPubMedCentral

Saura J, Andres N, Andrade C, Ojuel J, Eriksson K, Mahy N (1997) Biphasic and region-specific MAO-B response to aging in normal human brain. Neurobiol Aging 18(5):497–507CrossRefPubMed

Seymour CB, Mothersill C, Mooney R, Moriarty M, Tipton KF (2003) Monoamine oxidase inhibitors l-deprenyl and clorgyline protect nonmalignant human cells from ionising radiation and chemotherapy toxicity. Br J Cancer 89(10):20CrossRef

Shih JC, Chen K, Ridd MJ (1999) Monoamine oxidase: from genes to behavior. Ann Rev Neurosci 22:197–217CrossRefPubMedPubMedCentral

Shih JC, Wu JB, Chen K (2011) Transcriptional regulation and multiple functions of MAO genes. J Neural Transm 118(7):979–986CrossRefPubMedPubMedCentral

Siddiqui A, Mallajosyula JK, Rane A, Anderson JK (2010) Ability to delay neuropathological events associated with astrocytic MAO-B increase in a Parkinsonian mouse model: implications for early intervention on disease progression. Neurobiol Dis 40(2):444–448CrossRefPubMedPubMedCentral

Tsuchioka M, Takebayashi M, Hisaoka K, Maeda N, Nakata Y (2008) Serotonin (5-HT) induces glial cell line-derived neurotrophic factor (GDNF) mRNA expression via the transactivation of fibroblast growth factor 2 (FGR2) in rat C6 glioma cells. J Neurochem 106(1):244–257CrossRefPubMed

Weinreb O, Amit T, Bar-Am O, Youdim MB (2007) Induction of neurotrophic factors GDNF and BDNF associated with the mechanism of neurorescue action of rasagiline and ladostigil: new insights and implications for therapy. Ann N Y Acad Sci 1122:155–168CrossRefPubMed

Wu Y, Kazumura K, Maruyama W, Osawa T, Naoi M (2015) Rasagiline and selegiline suppress calcium efflux from mitochondria by PK11195-induced opening of mitochondrial permeability transition pore: a novel anti-apoptotic function for neuroprotection. J Neural Transm 122(10):1399–1407CrossRefPubMed

Wu Y, Shamoto-Nagai M, Maruyama W, Osawa T, Naoi M (2016) Rasagiline prevents cyclosporin A-sensitive superoxide flashes induced by PK11195, the initial signal of mitochondrial membrane permeabilization and apoptosis. J Neural Transm 123(5):491–494CrossRefPubMed

Yi H, Akao Y, Maruyama W, Chen K, Shih J, Naoi M (2006) Type A monoamine oxidase is the target of an endogenous dopaminergic neurotoxin, N-methyl(R)salsolinol, leading to apoptosis in SH-SY5Y cells. J Neurochem 96(2):541–549CrossRefPubMed

Youdim MBH, Bakhle YS (2006) Monoamine oxidase: isoforms and inhibitors in Parkinson’s disease and depressive illness. Br J Pharmacol 147(Suppl 1):S287–S296PubMedPubMedCentral

Youdim MBH, Edmondson D, Tipton KF (2006) The therapeutic potential of monoamine oxidase inhibitors. Nat Rev Neurosci 7(4):295–309CrossRefPubMed

Titel: Type B and A monoamine oxidase and their inhibitors regulate the gene expression of Bcl-2 and neurotrophic factors in human glioblastoma U118MG cells: different signal pathways for neuroprotection by selegiline and rasagiline
verfasst von: Keiko Inaba-Hasegawa
Masayo Shamoto-Nagai
Wakako Maruyama
Makoto Naoi
Publikationsdatum: 02.06.2017
Verlag: Springer Vienna
Erschienen in: Journal of Neural Transmission / Ausgabe 9/2017
Print ISSN: 0300-9564
Elektronische ISSN: 1435-1463
DOI: https://doi.org/10.1007/s00702-017-1740-9

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Type B and A monoamine oxidase and their inhibitors regulate the gene expression of Bcl-2 and neurotrophic factors in human glioblastoma U118MG cells: different signal pathways for neuroprotection by selegiline and rasagiline

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