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Erschienen in: Neurotoxicity Research 3/2017

01.10.2017 | ORIGINAL ARTICLE

Morphine Withdrawal Increases Brain-Derived Neurotrophic Factor Precursor

verfasst von: Alessia Bachis, Lee A. Campbell, Kierra Jenkins, Erin Wenzel, Italo Mocchetti

Erschienen in: Neurotoxicity Research | Ausgabe 3/2017

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Abstract

Morphine has been shown to increase the expression of brain-derived neurotrophic factor (BDNF) in the brain. However, little is known about the effect of morphine withdrawal on BDNF and its precursor protein, or proBDNF, which induces neuronal apoptosis. In this work, we examined whether BDNF and proBDNF levels change in rats chronically injected with escalating doses of morphine and those who undergo spontaneous withdrawal for 60 h. We observed, in the frontal cortex and striatum, that the ratio of BDNF to proBDNF changed depending upon the experimental paradigm. Morphine treatment and morphine withdrawal increased both BDNF and proBDNF levels. However, the increase in proBDNF immunoreactivity in withdrawal rats was more robust than that observed in morphine-treated rats. proBDNF is processed either intracellularly by furin or extracellularly by the tissue plasminogen activator (tPA)/plasminogen system or matrix metalloproteases (MMPs). To examine the mechanisms whereby chronic morphine treatment and morphine withdrawal differentially affects BDNF/proBDNF, the levels MMP-3 and MMP-7, furin, and tPA were analyzed. We found that morphine increases tPA levels, whereas withdrawal causes a decrease. To confirm the involvement of tPA in the morphine-mediated effect on BDNF/proBDNF, we exposed cortical neurons to morphine in the presence of the tPA inhibitor plasminogen activator inhibitor-1 (PAI-1). This inhibitor reversed the morphine-mediated decrease in proBDNF, supporting the hypothesis that morphine increases the availability of BDNF by promoting the extracellular processing of proBDNF by tPA. Because proBDNF could negatively influence synaptic repair, preventing withdrawal is crucial for reducing neurotoxic mechanisms associated with opioid abuse.
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Literatur
Zurück zum Zitat Akbarian S, Rios M, Liu RJ, Gold SJ, Fong HF, Zeiler S, Coppola V, Tessarollo L, Jones KR, Nestler EJ, Aghajanian GK, Jaenisch R (2002) Brain-derived neurotrophic factor is essential for opiate-induced plasticity of noradrenergic neurons. J Neurosci 22:4153-4162 doi:20026381 Akbarian S, Rios M, Liu RJ, Gold SJ, Fong HF, Zeiler S, Coppola V, Tessarollo L, Jones KR, Nestler EJ, Aghajanian GK, Jaenisch R (2002) Brain-derived neurotrophic factor is essential for opiate-induced plasticity of noradrenergic neurons. J Neurosci 22:4153-4162 doi:20026381
Zurück zum Zitat Altar CA, Cai N, Bliven T, Juhasz M, Conner JM, Acheson AL, Lindsay RM, Wiegand SJ (1997) Anterograde transport of brain-derived neurotrophic factor and its role in the brain. Nature 389:856–860CrossRefPubMed Altar CA, Cai N, Bliven T, Juhasz M, Conner JM, Acheson AL, Lindsay RM, Wiegand SJ (1997) Anterograde transport of brain-derived neurotrophic factor and its role in the brain. Nature 389:856–860CrossRefPubMed
Zurück zum Zitat Avdoshina V, Biggio F, Palchik G, Campbell LA, Mocchetti I (2010) Morphine induces the release of CCL5 from astrocytes: potential neuroprotective mechanism against the HIV protein gp120. Glia 58:1630–1639. doi:10.1002/glia.21035 PubMedPubMedCentral Avdoshina V, Biggio F, Palchik G, Campbell LA, Mocchetti I (2010) Morphine induces the release of CCL5 from astrocytes: potential neuroprotective mechanism against the HIV protein gp120. Glia 58:1630–1639. doi:10.​1002/​glia.​21035 PubMedPubMedCentral
Zurück zum Zitat Beattie MS, Harrington AW, Lee R, Kim JY, Boyce SL, Longo FM, Bresnahan JC, Hempstead BL, Yoon SO (2002) ProNGF induces p75-mediated death of oligodendrocytes following spinal cord injury. Neuron 36:375–386CrossRefPubMedPubMedCentral Beattie MS, Harrington AW, Lee R, Kim JY, Boyce SL, Longo FM, Bresnahan JC, Hempstead BL, Yoon SO (2002) ProNGF induces p75-mediated death of oligodendrocytes following spinal cord injury. Neuron 36:375–386CrossRefPubMedPubMedCentral
Zurück zum Zitat Bruno MA, Cuello AC (2006) Activity-dependent release of precursor nerve growth factor, conversion to mature nerve growth factor, and its degradation by a protease cascade. Proc Natl Acad Sci U S A 103:6735–6740CrossRefPubMedPubMedCentral Bruno MA, Cuello AC (2006) Activity-dependent release of precursor nerve growth factor, conversion to mature nerve growth factor, and its degradation by a protease cascade. Proc Natl Acad Sci U S A 103:6735–6740CrossRefPubMedPubMedCentral
Zurück zum Zitat Calabresi P, Napolitano M, Centonze D, Marfia GA, Gubellini P, Teule MA, Berretta N, Bernardi G, Frati L, Tolu M, Gulino A (2000) Tissue plasminogen activator controls multiple forms of synaptic plasticity and memory. Eur J Neurosci 12:1002–1012CrossRefPubMed Calabresi P, Napolitano M, Centonze D, Marfia GA, Gubellini P, Teule MA, Berretta N, Bernardi G, Frati L, Tolu M, Gulino A (2000) Tissue plasminogen activator controls multiple forms of synaptic plasticity and memory. Eur J Neurosci 12:1002–1012CrossRefPubMed
Zurück zum Zitat Cale JM, Lawrence DA (2007) Structure-function relationships of plasminogen activator inhibitor-1 and its potential as a therapeutic agent. Curr Drug Targets 8:971–981CrossRefPubMed Cale JM, Lawrence DA (2007) Structure-function relationships of plasminogen activator inhibitor-1 and its potential as a therapeutic agent. Curr Drug Targets 8:971–981CrossRefPubMed
Zurück zum Zitat Centonze D, Napolitano M, Saulle E, Gubellini P, Picconi B, Martorana A, Pisani A, Gulino A, Bernardi G, Calabresi P (2002) Tissue plasminogen activator is required for corticostriatal long-term potentiation. Eur J Neurosci 16:713–721CrossRefPubMed Centonze D, Napolitano M, Saulle E, Gubellini P, Picconi B, Martorana A, Pisani A, Gulino A, Bernardi G, Calabresi P (2002) Tissue plasminogen activator is required for corticostriatal long-term potentiation. Eur J Neurosci 16:713–721CrossRefPubMed
Zurück zum Zitat Chen ZY, Ieraci A, Teng H, Dall H, Meng CX, Herrera DG, Nykjaer A, Hempstead BL, Lee FS (2005) Sortilin controls intracellular sorting of brain-derived neurotrophic factor to the regulated secretory pathway. J Neurosci 25:6156–6166 doi:10.1523/JNEUROSCI.1017-05.2005 Chen ZY, Ieraci A, Teng H, Dall H, Meng CX, Herrera DG, Nykjaer A, Hempstead BL, Lee FS (2005) Sortilin controls intracellular sorting of brain-derived neurotrophic factor to the regulated secretory pathway. J Neurosci 25:6156–6166 doi:10.​1523/​JNEUROSCI.​1017-05.​2005
Zurück zum Zitat Ciammola A, Sassone J, Cannella M, Calza S, Poletti B, Frati L, Squitieri F, Silani V (2007) Low brain-derived neurotrophic factor (BDNF) levels in serum of Huntington's disease patients. Am J Med Genet B Neuropsychiatr Genet 144:574–577CrossRef Ciammola A, Sassone J, Cannella M, Calza S, Poletti B, Frati L, Squitieri F, Silani V (2007) Low brain-derived neurotrophic factor (BDNF) levels in serum of Huntington's disease patients. Am J Med Genet B Neuropsychiatr Genet 144:574–577CrossRef
Zurück zum Zitat Dieni S, Matsumoto T, Dekkers M, Rauskolb S, Ionescu MS, Deogracias R, Gundelfinger ED, Kojima M, Nestel S, Frotscher M, Barde YA (2012) BDNF and its pro-peptide are stored in presynaptic dense core vesicles in brain neurons. J Cell Biol 196:775–788. doi:10.1083/jcb.201201038 CrossRefPubMedPubMedCentral Dieni S, Matsumoto T, Dekkers M, Rauskolb S, Ionescu MS, Deogracias R, Gundelfinger ED, Kojima M, Nestel S, Frotscher M, Barde YA (2012) BDNF and its pro-peptide are stored in presynaptic dense core vesicles in brain neurons. J Cell Biol 196:775–788. doi:10.​1083/​jcb.​201201038 CrossRefPubMedPubMedCentral
Zurück zum Zitat Egan MF, Kojima M, Callicott JH, Goldberg TE, Kolachana BS, Bertolino A, Zaitsev E, Gold B, Goldman D, Dean M, Lu B, Weinberger DR (2003) The BDNF val66met polymorphism affects activity-dependent secretion of BDNF and human memory and hippocampal function. Cell 112:257–269CrossRefPubMed Egan MF, Kojima M, Callicott JH, Goldberg TE, Kolachana BS, Bertolino A, Zaitsev E, Gold B, Goldman D, Dean M, Lu B, Weinberger DR (2003) The BDNF val66met polymorphism affects activity-dependent secretion of BDNF and human memory and hippocampal function. Cell 112:257–269CrossRefPubMed
Zurück zum Zitat Flavin MP, Zhao G, Ho LT (2000) Microglial tissue plasminogen activator (tPA) triggers neuronal apoptosis in vitro. Glia 29:347–354CrossRefPubMed Flavin MP, Zhao G, Ho LT (2000) Microglial tissue plasminogen activator (tPA) triggers neuronal apoptosis in vitro. Glia 29:347–354CrossRefPubMed
Zurück zum Zitat Han BH, Holtzman DM (2000) BDNF protects the neonatal brain from hypoxic-ischemic injury in vivo via the ERK pathway. J Neurosci 20:5775–5781PubMed Han BH, Holtzman DM (2000) BDNF protects the neonatal brain from hypoxic-ischemic injury in vivo via the ERK pathway. J Neurosci 20:5775–5781PubMed
Zurück zum Zitat Harrington AW, Leiner B, Blechschmitt C, Arevalo JC, Lee R, Morl K, Meyer M, Hempstead BL, Yoon SO, Giehl KM (2004) Secreted proNGF is a pathophysiological death-inducing ligand after adult CNS injury. Proc Natl Acad Sci U S A 101:6226–6230CrossRefPubMedPubMedCentral Harrington AW, Leiner B, Blechschmitt C, Arevalo JC, Lee R, Morl K, Meyer M, Hempstead BL, Yoon SO, Giehl KM (2004) Secreted proNGF is a pathophysiological death-inducing ligand after adult CNS injury. Proc Natl Acad Sci U S A 101:6226–6230CrossRefPubMedPubMedCentral
Zurück zum Zitat Hatami H, Oryan S, Semnanian S, Kazemi B, Bandepour M, Ahmadiani A (2007) Alterations of BDNF and NT-3 genes expression in the nucleus paragigantocellularis during morphine dependency and withdrawal. Neuropeptides 41:321–328. doi:10.1016/j.npep.2007.04.007 CrossRefPubMed Hatami H, Oryan S, Semnanian S, Kazemi B, Bandepour M, Ahmadiani A (2007) Alterations of BDNF and NT-3 genes expression in the nucleus paragigantocellularis during morphine dependency and withdrawal. Neuropeptides 41:321–328. doi:10.​1016/​j.​npep.​2007.​04.​007 CrossRefPubMed
Zurück zum Zitat Heberlein A, Dursteler-MacFarland KM, Lenz B, Frieling H, Grosch M, Bonsch D, Kornhuber J, Wiesbeck GA, Bleich S, Hillemacher T (2011) Serum levels of BDNF are associated with craving in opiate-dependent patients. J Psychopharmacol 25:1480–1484. doi:10.1177/0269881111411332 CrossRefPubMed Heberlein A, Dursteler-MacFarland KM, Lenz B, Frieling H, Grosch M, Bonsch D, Kornhuber J, Wiesbeck GA, Bleich S, Hillemacher T (2011) Serum levels of BDNF are associated with craving in opiate-dependent patients. J Psychopharmacol 25:1480–1484. doi:10.​1177/​0269881111411332​ CrossRefPubMed
Zurück zum Zitat Howells DW, Porritt MJ, Wong JYF, Batchelor PE, Kalnins R, Hughes AJ, Donnan GA (2000) Reduced BDNF mRNA expression in the Parkinson's disease substantia nigra. Exp Neurol 166:127–135CrossRefPubMed Howells DW, Porritt MJ, Wong JYF, Batchelor PE, Kalnins R, Hughes AJ, Donnan GA (2000) Reduced BDNF mRNA expression in the Parkinson's disease substantia nigra. Exp Neurol 166:127–135CrossRefPubMed
Zurück zum Zitat Hutchinson MR, Shavit Y, Grace PM, Rice KC, Maier SF, Watkins LR (2011) Exploring the neuroimmunopharmacology of opioids: an integrative review of mechanisms of central immune signaling and their implications for opioid analgesia. Pharmacol Rev 63:772–810. doi:10.1124/pr.110.004135 CrossRefPubMedPubMedCentral Hutchinson MR, Shavit Y, Grace PM, Rice KC, Maier SF, Watkins LR (2011) Exploring the neuroimmunopharmacology of opioids: an integrative review of mechanisms of central immune signaling and their implications for opioid analgesia. Pharmacol Rev 63:772–810. doi:10.​1124/​pr.​110.​004135 CrossRefPubMedPubMedCentral
Zurück zum Zitat Hyman C, Hofer M, Barde YA, Juhasz M, Yancopoulos GD, Squinto SP, Lindsay RM (1991) BDNF is a neurotrophic factor for dopaminergic neurons of the substantia nigra. Nature 350:230–232CrossRefPubMed Hyman C, Hofer M, Barde YA, Juhasz M, Yancopoulos GD, Squinto SP, Lindsay RM (1991) BDNF is a neurotrophic factor for dopaminergic neurons of the substantia nigra. Nature 350:230–232CrossRefPubMed
Zurück zum Zitat Jacovina AT, Zhong F, Khazanova E, Lev E, Deora AB, Hajjar KA (2001) Neuritogenesis and the nerve growth factor-induced differentiation of PC-12 cells requires annexin II-mediated plasmin generation. J Biol Chem 276:49350–49358. doi:10.1074/jbc.M106289200 CrossRefPubMed Jacovina AT, Zhong F, Khazanova E, Lev E, Deora AB, Hajjar KA (2001) Neuritogenesis and the nerve growth factor-induced differentiation of PC-12 cells requires annexin II-mediated plasmin generation. J Biol Chem 276:49350–49358. doi:10.​1074/​jbc.​M106289200 CrossRefPubMed
Zurück zum Zitat Koo JW, Mazei-Robison MS, Chaudhury D, Juarez B, LaPlant Q, Ferguson D, Feng J, Sun H, Scobie KN, Damez-Werno D, Crumiller M, Ohnishi YN, Ohnishi YH, Mouzon E, Dietz DM, Lobo MK, Neve RL, Russo SJ, Han MH, Nestler EJ (2012) BDNF is a negative modulator of morphine action. Science 338:124–128. doi:10.1126/science.1222265 CrossRefPubMedPubMedCentral Koo JW, Mazei-Robison MS, Chaudhury D, Juarez B, LaPlant Q, Ferguson D, Feng J, Sun H, Scobie KN, Damez-Werno D, Crumiller M, Ohnishi YN, Ohnishi YH, Mouzon E, Dietz DM, Lobo MK, Neve RL, Russo SJ, Han MH, Nestler EJ (2012) BDNF is a negative modulator of morphine action. Science 338:124–128. doi:10.​1126/​science.​1222265 CrossRefPubMedPubMedCentral
Zurück zum Zitat Lebrun-Julien F, Bertrand MJ, De Backer O, Stellwagen D, Morales CR, Di Polo A, Barker PA (2010) ProNGF induces TNFalpha-dependent death of retinal ganglion cells through a p75NTR non-cell-autonomous signaling pathway. Proc Natl Acad Sci U S A 107:3817–3822. doi:10.1073/pnas.0909276107 CrossRefPubMedPubMedCentral Lebrun-Julien F, Bertrand MJ, De Backer O, Stellwagen D, Morales CR, Di Polo A, Barker PA (2010) ProNGF induces TNFalpha-dependent death of retinal ganglion cells through a p75NTR non-cell-autonomous signaling pathway. Proc Natl Acad Sci U S A 107:3817–3822. doi:10.​1073/​pnas.​0909276107 CrossRefPubMedPubMedCentral
Zurück zum Zitat Mamounas LA, Blue ME, Siuciak JA, Altar CA (1995) Brain-derived neurotrophic factor promotes the survival and sprouting of serotonergic axons in rat brain. J Neurosci 15:7929–7939PubMed Mamounas LA, Blue ME, Siuciak JA, Altar CA (1995) Brain-derived neurotrophic factor promotes the survival and sprouting of serotonergic axons in rat brain. J Neurosci 15:7929–7939PubMed
Zurück zum Zitat Mashayekhi FJ, Rasti M, Rahvar M, Mokarram P, Namavar MR, Owji AA (2012) Expression levels of the BDNF gene and histone modifications around its promoters in the ventral tegmental area and locus ceruleus of rats during forced abstinence from morphine. Neurochem Res 37:1517–1523. doi:10.1007/s11064-012-0746-9 CrossRefPubMed Mashayekhi FJ, Rasti M, Rahvar M, Mokarram P, Namavar MR, Owji AA (2012) Expression levels of the BDNF gene and histone modifications around its promoters in the ventral tegmental area and locus ceruleus of rats during forced abstinence from morphine. Neurochem Res 37:1517–1523. doi:10.​1007/​s11064-012-0746-9 CrossRefPubMed
Zurück zum Zitat Mowla SJ, Farhadi HF, Pareek S, Atwal JK, Morris SJ, Seidah NG, Murphy RA (2001) Biosynthesis and post-translational processing of the precursor to brain-derived neurotrophic factor. J Biol Chem 276:12660–12666. doi:10.1074/jbc.M008104200 CrossRefPubMed Mowla SJ, Farhadi HF, Pareek S, Atwal JK, Morris SJ, Seidah NG, Murphy RA (2001) Biosynthesis and post-translational processing of the precursor to brain-derived neurotrophic factor. J Biol Chem 276:12660–12666. doi:10.​1074/​jbc.​M008104200 CrossRefPubMed
Zurück zum Zitat Nagai T, Yamada K, Yoshimura M, Ishikawa K, Miyamoto Y, Hashimoto K, Noda Y, Nitta A, Nabeshima T (2004) The tissue plasminogen activator-plasmin system participates in the rewarding effect of morphine by regulating dopamine release. Proc Natl Acad Sci U S A 101:3650–3655. doi:10.1073/pnas.0306587101 CrossRefPubMedPubMedCentral Nagai T, Yamada K, Yoshimura M, Ishikawa K, Miyamoto Y, Hashimoto K, Noda Y, Nitta A, Nabeshima T (2004) The tissue plasminogen activator-plasmin system participates in the rewarding effect of morphine by regulating dopamine release. Proc Natl Acad Sci U S A 101:3650–3655. doi:10.​1073/​pnas.​0306587101 CrossRefPubMedPubMedCentral
Zurück zum Zitat Numan S, Lane-Ladd SB, Zhang L, Lundgren KH, Russell DS, Seroogy KB, Nestler EJ (1998) Differential regulation of neurotrophin and trk receptor mRNAs in catecholaminergic nuclei during chronic opiate treatment and withdrawal. J Neurosci 18:10700–10708PubMed Numan S, Lane-Ladd SB, Zhang L, Lundgren KH, Russell DS, Seroogy KB, Nestler EJ (1998) Differential regulation of neurotrophin and trk receptor mRNAs in catecholaminergic nuclei during chronic opiate treatment and withdrawal. J Neurosci 18:10700–10708PubMed
Zurück zum Zitat Nykjaer A, Lee R, Teng KK, Jansen P, Madsen P, Nielsen MS, Jacobsen C, Kliemannel M, Schwarz E, Willnow TE, Hempstead BL, Petersen CM (2004) Sortilin is essential for proNGF-induced neuronal cell death. Nature 427:843CrossRefPubMed Nykjaer A, Lee R, Teng KK, Jansen P, Madsen P, Nielsen MS, Jacobsen C, Kliemannel M, Schwarz E, Willnow TE, Hempstead BL, Petersen CM (2004) Sortilin is essential for proNGF-induced neuronal cell death. Nature 427:843CrossRefPubMed
Zurück zum Zitat Pang PT, Teng HK, Zaitsev E, Woo NT, Sakata K, Zhen S, Teng KK, Yung WH, Hempstead BL, Lu B (2004) Cleavage of proBDNF by tPA/plasmin is essential for long-term hippocampal plasticity. Science 306:487–491 doi:10.1126/science.1100135 Pang PT, Teng HK, Zaitsev E, Woo NT, Sakata K, Zhen S, Teng KK, Yung WH, Hempstead BL, Lu B (2004) Cleavage of proBDNF by tPA/plasmin is essential for long-term hippocampal plasticity. Science 306:487–491 doi:10.​1126/​science.​1100135
Zurück zum Zitat Pawlak R, Magarinos AM, Melchor J, McEwen B, Strickland S (2003) Tissue plasminogen activator in the amygdala is critical for stress-induced anxiety-like behavior. Nat Neurosci 6:168–174. doi:10.1038/nn998 CrossRefPubMed Pawlak R, Magarinos AM, Melchor J, McEwen B, Strickland S (2003) Tissue plasminogen activator in the amygdala is critical for stress-induced anxiety-like behavior. Nat Neurosci 6:168–174. doi:10.​1038/​nn998 CrossRefPubMed
Zurück zum Zitat Plow EF, Herren T, Redlitz A, Miles LA, Hoover-Plow JL (1995) The cell biology of the plasminogen system. FASEB J 9:939–945PubMed Plow EF, Herren T, Redlitz A, Miles LA, Hoover-Plow JL (1995) The cell biology of the plasminogen system. FASEB J 9:939–945PubMed
Zurück zum Zitat Robinson TE, Gorny G, Savage VR, Kolb B (2002) Widespread but regionally specific effects of experimenter- versus self-administered morphine on dendritic spines in the nucleus accumbens, hippocampus, and neocortex of adult rats. Synapse 46:271–279. doi:10.1002/syn.10146 CrossRefPubMed Robinson TE, Gorny G, Savage VR, Kolb B (2002) Widespread but regionally specific effects of experimenter- versus self-administered morphine on dendritic spines in the nucleus accumbens, hippocampus, and neocortex of adult rats. Synapse 46:271–279. doi:10.​1002/​syn.​10146 CrossRefPubMed
Zurück zum Zitat Schluger JH, Bart G, Green M, Ho A, Kreek MJ (2003) Corticotropin-releasing factor testing reveals a dose-dependent difference in methadone maintained vs control subjects. Neuropsychopharmacology 28:985–994. doi:10.1038/sj.npp.1300156 PubMed Schluger JH, Bart G, Green M, Ho A, Kreek MJ (2003) Corticotropin-releasing factor testing reveals a dose-dependent difference in methadone maintained vs control subjects. Neuropsychopharmacology 28:985–994. doi:10.​1038/​sj.​npp.​1300156 PubMed
Zurück zum Zitat Seeds NW, Basham ME, Haffke SP (1999) Neuronal migration is retarded in mice lacking the tissue plasminogen activator gene. Proc Natl Acad Sci U S A 96:14118–14123CrossRefPubMedPubMedCentral Seeds NW, Basham ME, Haffke SP (1999) Neuronal migration is retarded in mice lacking the tissue plasminogen activator gene. Proc Natl Acad Sci U S A 96:14118–14123CrossRefPubMedPubMedCentral
Zurück zum Zitat Spiga S, Serra GP, Puddu MC, Foddai M, Diana M (2003) Morphine withdrawal-induced abnormalities in the VTA: confocal laser scanning microscopy. Eur J Neurosci 17:605–612CrossRefPubMed Spiga S, Serra GP, Puddu MC, Foddai M, Diana M (2003) Morphine withdrawal-induced abnormalities in the VTA: confocal laser scanning microscopy. Eur J Neurosci 17:605–612CrossRefPubMed
Zurück zum Zitat Teng HK, Teng KK, Lee R, Wright S, Tevar S, Almeida RD, Kermani P, Torkin R, Chen ZY, Lee FS, Kraemer RT, Nykjaer A, Hempstead BL (2005) ProBDNF induces neuronal apoptosis via activation of a receptor complex of p75NTR and sortilin. J Neurosci 25:5455–5463. doi:10.1523/JNEUROSCI.5123-04.2005 CrossRefPubMed Teng HK, Teng KK, Lee R, Wright S, Tevar S, Almeida RD, Kermani P, Torkin R, Chen ZY, Lee FS, Kraemer RT, Nykjaer A, Hempstead BL (2005) ProBDNF induces neuronal apoptosis via activation of a receptor complex of p75NTR and sortilin. J Neurosci 25:5455–5463. doi:10.​1523/​JNEUROSCI.​5123-04.​2005 CrossRefPubMed
Zurück zum Zitat Toda T, Momose Y, Murata M, Tamiya G, Yamamoto M, Hattori N, Inoko H (2003) Toward identification of susceptibility genes for sporadic Parkinson's disease. J Neurol 250(Suppl 3):III40–III43PubMed Toda T, Momose Y, Murata M, Tamiya G, Yamamoto M, Hattori N, Inoko H (2003) Toward identification of susceptibility genes for sporadic Parkinson's disease. J Neurol 250(Suppl 3):III40–III43PubMed
Zurück zum Zitat Weed MR, Steward DJ (2005) Neuropsychopathology in the SIV/macaque model of AIDS. Front Biosci 10:710–727CrossRefPubMed Weed MR, Steward DJ (2005) Neuropsychopathology in the SIV/macaque model of AIDS. Front Biosci 10:710–727CrossRefPubMed
Zurück zum Zitat Woo NH, Teng HK, Siao CJ, Chiaruttini C, Pang PT, Milner TA, Hempstead BL, Lu B (2005) Activation of p75(NTR) by proBDNF facilitates hippocampal long-term depression. Nat Neurosci 8:1069–1077. doi:10.1038/Nn1510 CrossRefPubMed Woo NH, Teng HK, Siao CJ, Chiaruttini C, Pang PT, Milner TA, Hempstead BL, Lu B (2005) Activation of p75(NTR) by proBDNF facilitates hippocampal long-term depression. Nat Neurosci 8:1069–1077. doi:10.​1038/​Nn1510 CrossRefPubMed
Zurück zum Zitat Yamada K, Nagai T, Nabeshima T (2005) Drug dependence, synaptic plasticity, and tissue plasminogen activator. J Pharmacol Sci 97:157–161CrossRefPubMed Yamada K, Nagai T, Nabeshima T (2005) Drug dependence, synaptic plasticity, and tissue plasminogen activator. J Pharmacol Sci 97:157–161CrossRefPubMed
Zurück zum Zitat Yang M, Lim Y, Li X, Zhong JH, Zhou XF (2011) Precursor of brain-derived neurotrophic factor (proBDNF) forms a complex with huntingtin-associated protein-1 (HAP1) and sortilin that modulates proBDNF trafficking, degradation, and processing. J Biol Chem 286:16272–16284. doi:10.1074/jbc.M110.195347 CrossRefPubMedPubMedCentral Yang M, Lim Y, Li X, Zhong JH, Zhou XF (2011) Precursor of brain-derived neurotrophic factor (proBDNF) forms a complex with huntingtin-associated protein-1 (HAP1) and sortilin that modulates proBDNF trafficking, degradation, and processing. J Biol Chem 286:16272–16284. doi:10.​1074/​jbc.​M110.​195347 CrossRefPubMedPubMedCentral
Zurück zum Zitat Yoshida T, Ishikawa M, Niitsu T, Nakazato M, Watanabe H, Shiraishi T, Shiina A, Hashimoto T, Kanahara N, Hasegawa T, Enohara M, Kimura A, Iyo M, Hashimoto K (2012) Decreased serum levels of mature brain-derived neurotrophic factor (BDNF), but not its precursor proBDNF, in patients with major depressive disorder. PLoS One 7:e42676. doi:10.1371/journal.pone.0042676 CrossRefPubMedPubMedCentral Yoshida T, Ishikawa M, Niitsu T, Nakazato M, Watanabe H, Shiraishi T, Shiina A, Hashimoto T, Kanahara N, Hasegawa T, Enohara M, Kimura A, Iyo M, Hashimoto K (2012) Decreased serum levels of mature brain-derived neurotrophic factor (BDNF), but not its precursor proBDNF, in patients with major depressive disorder. PLoS One 7:e42676. doi:10.​1371/​journal.​pone.​0042676 CrossRefPubMedPubMedCentral
Zurück zum Zitat Zuccato C, Cattaneo E (2009) Brain-derived neurotrophic factor in neurodegenerative diseases. Nat Rev Neurol 5:311–322CrossRefPubMed Zuccato C, Cattaneo E (2009) Brain-derived neurotrophic factor in neurodegenerative diseases. Nat Rev Neurol 5:311–322CrossRefPubMed
Metadaten
Titel
Morphine Withdrawal Increases Brain-Derived Neurotrophic Factor Precursor
verfasst von
Alessia Bachis
Lee A. Campbell
Kierra Jenkins
Erin Wenzel
Italo Mocchetti
Publikationsdatum
01.10.2017
Verlag
Springer US
Erschienen in
Neurotoxicity Research / Ausgabe 3/2017
Print ISSN: 1029-8428
Elektronische ISSN: 1476-3524
DOI
https://doi.org/10.1007/s12640-017-9788-8

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