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Article

Brain-Derived Neurotrophic Factor Induces Matrix Metalloproteinase 9 Expression in Neurons via the Serum Response Factor/c-Fos Pathway

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Pages 2149-2162 | Received 03 Jan 2013, Accepted 13 Mar 2013, Published online: 20 Mar 2023

REFERENCES

  • Lu Y, Christian K, Lu B. 2008. BDNF: a key regulator for protein synthesis-dependent LTP and long-term memory? Neurobiol. Learn Mem. 89:312–323.
  • Cohen MS, Orth CB, Kim HJ, Jeon NL, Jaffrey SR. 2011. Neurotrophin-mediated dendrite-to-nucleus signaling revealed by microfluidic compartmentalization of dendrites. Proc. Natl. Acad. Sci. U. S. A. 108:11246–11251.
  • Ying SW, Futter M, Rosenblum K, Webber MJ, Hunt SP, Bliss TV, Bramham CR. 2002. Brain-derived neurotrophic factor induces long-term potentiation in intact adult hippocampus: requirement for ERK activation coupled to CREB and upregulation of Arc synthesis. J. Neurosci. 22:1532–1540.
  • Figurov A, Pozzo-Miller LD, Olafsson P, Wang T, Lu B. 1996. Regulation of synaptic responses to high-frequency stimulation and LTP by neurotrophins in the hippocampus. Nature 381:706–709.
  • Patterson SL, Abel T, Deuel TA, Martin KC, Rose JC, Kandel ER. 1996. Recombinant BDNF rescues deficits in basal synaptic transmission and hippocampal LTP in BDNF knockout mice. Neuron 16:1137–1145.
  • Messaoudi E, Ying SW, Kanhema T, Croll SD, Bramham CR. 2002. Brain-derived neurotrophic factor triggers transcription-dependent, late phase long-term potentiation in vivo. J. Neurosci. 22:7453–7461.
  • Kaplan DR, Miller FD. 2000. Neurotrophin signal transduction in the nervous system. Curr. Opin. Neurobiol. 10:381–391.
  • Sgambato V, Pages C, Rogard M, Besson MJ, Caboche J. 1998. Extracellular signal-regulated kinase (ERK) controls immediate early gene induction on corticostriatal stimulation. J. Neurosci. 18:8814–8825.
  • Valjent E, Caboche J, Vanhoutte P. 2001. Mitogen-activated protein kinase/extracellular signal-regulated kinase induced gene regulation in brain: a molecular substrate for learning and memory? Mol. Neurobiol 23:83–99.
  • Radwanska K, Caboche J, Kaczmarek L. 2005. Extracellular signal-regulated kinases (ERKs) modulate cocaine-induced gene expression in the mouse amygdala. Eur. J. Neurosci. 22:939–948.
  • Ramanan N, Shen Y, Sarsfield S, Lemberger T, Schutz G, Linden DJ, Ginty DD. 2005. SRF mediates activity-induced gene expression and synaptic plasticity but not neuronal viability. Nat. Neurosci. 8:759–767.
  • Knoll B, Kretz O, Fiedler C, Alberti S, Schutz G, Frotscher M, Nordheim A. 2006. Serum response factor controls neuronal circuit assembly in the hippocampus. Nat. Neurosci. 9:195–204.
  • Etkin A, Alarcon JM, Weisberg SP, Touzani K, Huang YY, Nordheim A, Kandel ER. 2006. A role in learning for SRF: deletion in the adult forebrain disrupts LTD and the formation of an immediate memory of a novel context. Neuron 50:127–143.
  • Carlezon WAJr, Duman RS, Nestler EJ. 2005. The many faces of CREB. Trends Neurosci. 28:436–445.
  • Meighan SE, Meighan PC, Choudhury P, Davis CJ, Olson ML, Zornes PA, Wright JW, Harding JW. 2006. Effects of extracellular matrix-degrading proteases matrix metalloproteinases 3 and 9 on spatial learning and synaptic plasticity. J. Neurochem. 96:1227–1241.
  • Nagy V, Bozdagi O, Matynia A, Balcerzyk M, Okulski P, Dzwonek J, Costa RM, Silva AJ, Kaczmarek L, Huntley GW. 2006. Matrix metalloproteinase-9 is required for hippocampal late-phase long-term potentiation and memory. J. Neurosci. 26:1923–1934.
  • Michaluk P, Kolodziej L, Mioduszewska B, Wilczynski GM, Dzwonek J, Jaworski J, Gorecki DC, Ottersen OP, Kaczmarek L. 2007. Beta-dystroglycan as a target for MMP-9, in response to enhanced neuronal activity. J. Biol. Chem. 282:16036–16041.
  • Okulski P, Jay TM, Jaworski J, Duniec K, Dzwonek J, Konopacki FA, Wilczynski GM, Sánchez-Capelo A, Mallet J, Kaczmarek L. 2007. TIMP-1 abolishes MMP-9-dependent long-lasting long-term potentiation in the prefrontal cortex. Biol. Psychiatry 62:359–362.
  • Michaluk P, Wawrzyniak M, Alot P, Szczot M, Wyrembek P, Mercik K, Medvedev N, Wilczek E, De Roo M, Zuschratter W, Muller D, Wilczynski GM, Mozrzymas JW, Stewart MG, Kaczmarek L, Wlodarczyk J. 2011. Influence of matrix metalloproteinase MMP-9 on dendritic spine morphology. J. Cell Sci. 124:3369–3380.
  • Wang XB, Bozdagi O, Nikitczuk JS, Zhai ZW, Zhou Q, Huntley GW. 2008. Extracellular proteolysis by matrix metalloproteinase-9 drives dendritic spine enlargement and long-term potentiation coordinately. Proc. Natl. Acad. Sci. U. S. A. 105:19520–19525.
  • Szklarczyk A, Lapinska J, Rylski M, McKay RD, Kaczmarek L. 2002. Matrix metalloproteinase-9 undergoes expression and activation during dendritic remodeling in adult hippocampus. J. Neurosci. 22:920–930.
  • Konopacki FA, Rylski M, Wilczek E, Amborska R, Detka D, Kaczmarek L, Wilczynski GM. 2007. Synaptic localization of seizure-induced matrix metalloproteinase-9 mRNA. Neuroscience 150:31–39.
  • Wilczynski GM, Konopacki FA, Wilczek E, Lasiecka Z, Gorlewicz A, Michaluk P, Wawrzyniak M, Malinowska M, Okulski P, Kolodziej LR, Konopka W, Duniec K, Mioduszewska B, Nikolaev E, Walczak A, Owczarek D, Gorecki DC, Zuschratter W, Ottersen OP, Kaczmarek L. 2008. Important role of matrix metalloproteinase 9 in epileptogenesis. J. Cell Biol. 180:1021–1035.
  • Rylski M, Amborska R, Zybura K, Michaluk P, Bielinska B, Konopacki FA, Wilczynski GM, Kaczmarek L. 2009. JunB is a repressor of MMP-9 transcription in depolarized rat brain neurons. Mol. Cell Neurosci. 40:98–110.
  • Yan C, Boyd DD. 2007. Regulation of matrix metalloproteinase gene expression. J. Cell. Physiol. 211:19–26.
  • Chakraborti S, Mandal M, Das S, Mandal A, Chakraborti T. 2003. Regulation of matrix metalloproteinases: an overview. Mol. Cell. Biochem. 253:269–285.
  • Impey S, Obrietan K, Wong ST, Poser S, Yano S, Wayman G, Deloulme JC, Chan G, Storm DR. 1998. Crosstalk between ERK and PKA is required for Ca2+ stimulation of CREB-dependent transcription and ERK nuclear translocation. Neuron 21:869–883.
  • Mansour SJ, Matten WT, Hermann AS, Candia JM, Rong S, Fukasawa K, Vande Woude GF, Ahn NG. 1994. Transformation of mammalian cells by constitutively active MAP kinase kinase. Science 265:966–970.
  • Poser S, Impey S, Trinh K, Xia Z, Storm DR. 2000. SRF-dependent gene expression is required for PI3-kinase-regulated cell proliferation. EMBO J. 19:4955–4966.
  • Chang SH, Poser S, Xia Z. 2004. A novel role for serum response factor in neuronal survival. J. Neurosci. 24:2277–2285.
  • Cen B, Selvaraj A, Burgess RC, Hitzler JK, Ma Z, Morris SW, Prywes R. 2003. Megakaryoblastic leukemia 1, a potent transcriptional coactivator for serum response factor (SRF), is required for serum induction of SRF target genes. Mol. Cell. Biol. 23:6597–6608.
  • Shaulian E, Zauberman A, Ginsberg D, Oren M. 1992. Identification of a minimal transforming domain of p53: negative dominance through abrogation of sequence-specific DNA binding. Mol. Cell. Biol. 12:5581–5592.
  • Kalita K, Kharebava G, Zheng JJ, Hetman M. 2006. Role of megakaryoblastic acute leukemia-1 in ERK1/2-dependent stimulation of serum response factor-driven transcription by BDNF or increased synaptic activity. J. Neurosci. 26:10020–10032.
  • Ahn S, Olive M, Aggarwal S, Krylov D, Ginty DD, Vinson C. 1998. A dominant-negative inhibitor of CREB reveals that it is a general mediator of stimulus-dependent transcription of c-fos. Mol. Cell. Biol. 18:967–977.
  • Klejman A, Kaczmarek L. 2006. Inducible cAMP early repressor (ICER) isoforms and neuronal apoptosis in cortical in vitro culture. Acta Neurobiol. Exp. (Wars.) 66:267–272.
  • Yin F, Hoggatt AM, Zhou J, Herring BP. 2006. 130-kDa smooth muscle myosin light chain kinase is transcribed from a CArG-dependent, internal promoter within the mouse mylk gene. Am. J. Physiol. Cell Physiol. 290:C1599–1609.
  • Bakiri L, Matsuo K, Wisniewska M, Wagner EF, Yaniv M. 2002. Promoter specificity and biological activity of tethered AP-1 dimers. Mol. Cell. Biol. 22:4952–4964.
  • Brummelkamp TR, Bernards R, Agami R. 2002. A system for stable expression of short interfering RNAs in mammalian cells. Science 296:550–553.
  • Habas A, Kharebava G, Szatmari E, Hetman M. 2006. NMDA neuroprotection against a phosphatidylinositol-3 kinase inhibitor, LY294002 by NR2B-mediated suppression of glycogen synthase kinase-3beta-induced apoptosis. J. Neurochem. 96:335–348.
  • Mullenbrock S, Shah J, Cooper GM. 2011. Global expression analysis identified a preferentially nerve growth factor-induced transcriptional program regulated by sustained mitogen-activated protein kinase/extracellular signal-regulated kinase (ERK) and AP-1 protein activation during PC12 cell differentiation. J. Biol. Chem. 286:45131–45145.
  • Rylski M, Amborska R, Zybura K, Mioduszewska B, Michaluk P, Jaworski J, Kaczmarek L. 2008. Yin Yang 1 is a critical repressor of matrix metalloproteinase-9 expression in brain neurons. J. Biol. Chem. 283:35140–35153.
  • Kaczmarek L. 1993. Molecular biology of vertebrate learning: is c-fos a new beginning? J. Neurosci. Res. 34:377–381.
  • Kaczmarek L, Chaudhuri A. 1997. Sensory regulation of immediate-early gene expression in mammalian visual cortex: implications for functional mapping and neural plasticity. Brain Res. Brain Res. Rev. 23:237–256.
  • Kaczmarek L, Lapinska-Dzwonek J, Szymczak S. 2002. Matrix metalloproteinases in the adult brain physiology: a link between c-Fos, AP-1 and remodeling of neuronal connections? EMBO J. 21:6643–6648.
  • Jaworski J, Spangler S, Seeburg DP, Hoogenraad CC, Sheng M. 2005. Control of dendritic arborization by the phosphoinositide-3′-kinase-Akt-mammalian target of rapamycin pathway. J. Neurosci. 25:11300–11312.
  • Xia Z, Dudek H, Miranti CK, Greenberg ME. 1996. Calcium influx via the NMDA receptor induces immediate early gene transcription by a MAP kinase/ERK-dependent mechanism. J. Neurosci. 16:5425–5436.
  • Park JK, Park SH, So K, Bae IH, Yoo YD, Um HD. 2010. ICAM-3 enhances the migratory and invasive potential of human non-small cell lung cancer cells by inducing MMP-2 and MMP-9 via Akt and CREB. Int. J. Oncol. 36:181–192.
  • Tsai LN, Ku TK, Salib NK, Crowe DL. 2008. Extracellular signals regulate rapid coactivator recruitment at AP-1 sites by altered phosphorylation of both CREB binding protein and c-jun. Mol. Cell. Biol. 28:4240–4250.
  • Gilles L, Bluteau D, Boukour S, Chang Y, Zhang Y, Robert T, Dessen P, Debili N, Bernard OA, Vainchenker W, Raslova H. 2009. MAL/SRF complex is involved in platelet formation and megakaryocyte migration by regulating MYL9 (MLC2) and MMP9. Blood 114:4221–4232.
  • Zafra F, Castren E, Thoenen H, Lindholm D. 1991. Interplay between glutamate and gamma-aminobutyric acid transmitter systems in the physiological regulation of brain-derived neurotrophic factor and nerve growth factor synthesis in hippocampal neurons. Proc. Natl. Acad. Sci. U. S. A. 88:10037–10041.
  • Jia JM, Chen Q, Zhou Y, Miao S, Zheng J, Zhang C, Xiong ZQ. 2008. Brain-derived neurotrophic factor-tropomyosin-related kinase B signaling contributes to activity-dependent changes in synaptic proteins. J. Biol. Chem. 283:21242–21250.
  • Verpelli C, Piccoli G, Zibetti C, Zanchi A, Gardoni F, Huang K, Brambilla D, Di Luca M, Battaglioli E, Sala C. 2010. Synaptic activity controls dendritic spine morphology by modulating eEF2-dependent BDNF synthesis. J. Neurosci. 30:5830–5842.
  • Hwang JJ, Park MH, Choi SY, Koh JY. 2005. Activation of the Trk signaling pathway by extracellular zinc. Role of metalloproteinases. J. Biol. Chem. 280:11995–12001.
  • Lee R, Kermani P, Teng KK, Hempstead BL. 2001. Regulation of cell survival by secreted proneurotrophins. Science 294:1945–1948.
  • Mizoguchi H, Nakade J, Tachibana M, Ibi D, Someya E, Koike H, Kamei H, Nabeshima T, Itohara S, Takuma K, Sawada M, Sato J, Yamada K. 2011. Matrix metalloproteinase-9 contributes to kindled seizure development in pentylenetetrazole-treated mice by converting Pro-BDNF to mature BDNF in the hippocampus. J. Neurosci. 31:12963–12971.
  • 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.
  • Yang J, Siao CJ, Nagappan G, Marinic T, Jing D, McGrath K, Chen ZY, Mark W, Tessarollo L, Lee FS, Lu B, Hempstead BL. 2009. Neuronal release of proBDNF. Nat. Neurosci. 12:113–115.
  • Dziembowska M, Milek J, Janusz A, Rejmak E, Romanowska E, Gorkiewicz T, Tiron A, Bramham CR, Kaczmarek L. 2012. Activity-dependent local translation of matrix metalloproteinase-9. J. Neurosci. 32:14538–14547.
  • Troussard AA, Costello P, Yoganathan TN, Kumagai S, Roskelley CD, Dedhar S. 2000. The integrin linked kinase (ILK) induces an invasive phenotype via AP-1 transcription factor-dependent upregulation of matrix metalloproteinase 9 (MMP-9). Oncogene 19:5444–5452.
  • Kobayashi T, Kishimoto J, Hattori S, Wachi H, Shinkai H, Burgeson RE. 2004. Matrix metalloproteinase 9 expression is coordinately modulated by the KRE-M9 and 12-O-tetradecanoyl-phorbol-13-acetate responsive elements. J. Investig. Dermatol. 122:278–285.
  • Crowe DL, Brown TN. 1999. Transcriptional inhibition of matrix metalloproteinase 9 (MMP-9) activity by a c-fos/estrogen receptor fusion protein is mediated by the proximal AP-1 site of the MMP-9 promoter and correlates with reduced tumor cell invasion. Neoplasia 1:368–372.
  • Moon SK, Kim HM, Kim CH. 2004. PTEN induces G1 cell cycle arrest and inhibits MMP-9 expression via the regulation of NF-κB and AP-1 in vascular smooth muscle cells. Arch. Biochem. Biophys. 421:267–276.
  • Morgan JI, Curran T. 1991. Stimulus-transcription coupling in the nervous system: involvement of the inducible proto-oncogenes fos and jun. Annu. Rev. Neurosci. 14:421–451.
  • Perez-Cadahia B, Drobic B, Davie JR. 2011. Activation and function of immediate-early genes in the nervous system. Biochem. Cell Biol. 89:61–73.
  • Yang JQ, Zhao W, Duan H, Robbins ME, Buettner GR, Oberley LW, Domann FE. 2001. v-Ha-RaS oncogene upregulates the 92-kDa type IV collagenase (MMP-9) gene by increasing cellular superoxide production and activating NF-κB. Free Radic. Biol. Med. 31:520–529.
  • Eberhardt W, Schulze M, Engels C, Klasmeier E, Pfeilschifter J. 2002. Glucocorticoid-mediated suppression of cytokine-induced matrix metalloproteinase-9 expression in rat mesangial cells: involvement of nuclear factor-kappaB and Ets transcription factors. Mol. Endocrinol. 16:1752–1766.
  • Dash PK, Orsi SA, Moore AN. 2005. Sequestration of serum response factor in the hippocampus impairs long-term spatial memory. J. Neurochem. 93:269–278.
  • Lindecke A, Korte M, Zagrebelsky M, Horejschi V, Elvers M, Widera D, Prüllage M, Pfeiffer J, Kaltschmidt B, Kaltschmidt C. 2006. Long-term depression activates transcription of immediate early transcription factor genes: involvement of serum response factor/Elk-1. Eur. J. Neurosci. 24:555–563.
  • Nikitin VP, Kozyrev SA. 2007. Transcription factor serum response factor is selectively involved in the mechanisms of long-term synapse-specific plasticity. Neurosci. Behav. Physiol. 37:83–88.
  • Johnson AW, Crombag HS, Smith DR, Ramanan N. 2011. Effects of serum response factor (SRF) deletion on conditioned reinforcement. Behav. Brain Res. 220:312–318.

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