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Abstract:

Nerve growth factor (NGF) is a target-derived neurotrophic growth factor that controls many aspects of sensory and sympathetic neuronal development. The identification of transcription factors and downstream target genes that mediate NGF-dependent neuronal differentiation and target field innervation is currently a major challenge. Here, we show that the Pea3 transcription factor family members Etv4 and Etv5 are expressed by developing TrkA-positive dorsal root ganglion (DRG) neurons during the period of target innervation. Real-time PCR assays indicated that Etv4 and Etv5 mRNAs are significantly induced by NGF in different neuronal cells, suggesting that they could be involved in the biological responses induced by this neurotrophin. Interestingly, distal axon application of NGF in compartmentalized cultures of rat DRG sensory neurons was sufficient to induce a significant increase in Etv4 and Etv5 mRNA expression. Pharmacological assays also revealed that activation of MEK/ERK (MAPK) pathway is required for Etv4 and Etv5 gene induction in response to NGF. Downregulation of Etv4 and Etv5 using small interference RNA knockdown experiments inhibited NGFinduced neurite outgrowth of rat sensory neurons, while overexpression of full-length Etv4 or Etv5 potentiated neuronal differentiation in response to this neurotrophin. Together, these data establish Etv4 and Etv5 as essential molecules of the transcriptional program linking neurotrophin signaling to sensory neuronal differentiation, and suggest that they can be involved in NGF-mediated target innervation. © 2013 the authors.

Registro:

Documento: Artículo
Título:Pea3 transcription factor family members Etv4 and Etv5 mediate retrograde signaling and axonal growth of DRG sensory neurons in response to NGF
Autor:Fontanet, P.; Irala, D.; Alsina, F.C.; Paratcha, G.; Ledda, F.
Filiación:Division of Molecular and Cellular Neuroscience, Institute of Cellular Biology and Neuroscience (IBCN), CONICET-UBA, School of Medicine, Buenos Aires 1428, Argentina
Laboratory of Molecular and Cellular Neuroscience, Department of Neuroscience, Karolinska Institute, 171 77 Stockholm, Sweden
Palabras clave:2 (2 amino 3 methoxyphenyl) chromone; collagenase 3; mitogen activated protein kinase; nerve growth factor; protein tyrosine kinase A; stromelysin; transcription factor; transcription factor ER81; transcription factor etv4; transcription factor ETV5; unclassified drug; animal cell; animal tissue; article; cell survival; controlled study; down regulation; embryo; gene expression; genetic transfection; immunofluorescence; nerve cell differentiation; nerve fiber growth; nonhuman; priority journal; rat; real time polymerase chain reaction; RNA interference; sensory nerve cell; signal transduction; spinal ganglion; Western blotting; Animals; Axons; Chick Embryo; DNA-Binding Proteins; Ganglia, Spinal; Nerve Growth Factor; PC12 Cells; Rats; Rats, Wistar; Sensory Receptor Cells; Trans-Activators; Transcription Factors
Año:2013
Volumen:33
Número:40
Página de inicio:15940
Página de fin:15951
DOI: http://dx.doi.org/10.1523/JNEUROSCI.0928-13.2013
Título revista:Journal of Neuroscience
Título revista abreviado:J. Neurosci.
ISSN:02706474
CODEN:JNRSD
CAS:collagenase 3, 175449-82-8; mitogen activated protein kinase, 142243-02-5; nerve growth factor, 9061-61-4; stromelysin, 79955-99-0; DNA-Binding Proteins; ETV4 protein, rat; Etv5 protein, rat; Nerve Growth Factor, 9061-61-4; Trans-Activators; Transcription Factors
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_02706474_v33_n40_p15940_Fontanet

Referencias:

  • Alessi, D.R., Cuenda, A., Cohen, P., Dudley, D.T., Saltiel, A.R., PD 098059 is a specific inhibitor of the activation of mitogen-activated protein kinase kinase in vitro and in vivo (1995) J Biol Chem, 270, pp. 27489-27494. , CrossRef Medline
  • Arber, S., Ladle, D.R., Lin, J.H., Frank, E., Jessell, T.M., ETS gene Er81 controls the formation of functional connections between group Ia sensory afferents and motor neurons (2000) Cell, 101, pp. 485-498. , CrossRef Medline
  • Ascano, M., Bodmer, D., Kuruvilla, R., Endocytic trafficking of neurotrophins in neural development (2012) Trends Cell Biol, 22, pp. 266-273. , CrossRef Medline
  • Barker, P.A., Hussain, N.K., McPherson, P.S., Retrograde signaling by the neurotrophins follows a well-worn trk (2002) Trends Neurosci, 25, pp. 379-381. , CrossRef Medline
  • Baudet, C., Mikaels, A., Westphal, H., Johansen, J., Johansen, T.E., Ernfors, P., Positive and negative interactions of GDNF, NTN and ART in developing sensory neuron subpopulations, and their collaboration with neurotrophins (2000) Development, 127, pp. 4335-4344. , Medline
  • Bibel, M., Barde, Y.A., Neurotrophins: Key regulators of cell fate and cell shape in the vertebrate nervous system (2000) Genes Dev, 14, pp. 2919-2937. , CrossRef Medline
  • Campenot, R.B., NGF and the local control of nerve terminal growth (1994) J Neurobiol, 25, pp. 599-611. , CrossRef Medline
  • Chen, L., Maures, T.J., Jin, H., Huo, J.S., Rabbani, S.A., Schwartz, J., Carter-Su, C., SH2B1beta (SH2-Bbeta) enhances expression of a subset of nerve growth factor-regulated genes important for neuronal differentiation including genes encoding urokinase plasminogen activator receptor and matrix metalloproteinase 3/10 (2008) Mol Endocrinol, 22, pp. 454-476. , Medline
  • Chen, W.P., Chang, Y.C., Hsieh, S.T., Trophic interactions between sensory nerves and their targets (1999) J Biomed Sci, 6, pp. 79-85. , CrossRef Medline
  • Chotteau-Lelievre, A., Desbiens, X., Pelczar, H., Defossez, P.A., de Launoit, Y., Differential expression patterns of the PEA3 group transcription factors through murine embryonic development (1997) Oncogene, 15, pp. 937-952. , CrossRef Medline
  • Cosker, K.E., Courchesne, S.L., Segal, R.A., Action in the axon: Generation and transport of signaling endosomes (2008) Curr Opin Neurobiol, 18, pp. 270-275. , CrossRef Medline
  • Crowley, C., Spencer, S.D., Nishimura, M.C., Chen, K.S., Pitts-Meek, S., Armanini, M.P., Ling, L.H., Levinson, A.D., Mice lacking nerve growth factor display perinatal loss of sensory and sympathetic neurons yet develop basal forebrain cholinergic neurons (1994) Cell, 76, pp. 1001-1011. , CrossRef Medline
  • de Launoit, Y., Baert, J.L., Chotteau-Lelievre, A., Monte, D., Coutte, L., Mauen, S., Firlej, V., Verreman, K., The Ets transcription factors of the PEA3 group: Transcriptional regulators in metastasis (2006) Biochim Biophys Acta, 1766, pp. 79-87. , Medline
  • Ginty, D.D., Segal, R.A., Retrograde neurotrophin signaling: Trk-ing along the axon (2002) Curr Opin Neurobiol, 12, pp. 268-274. , CrossRef Medline
  • Graef, I.A., Wang, F., Charron, F., Chen, L., Neilson, J., Tessier-Lavigne, M., Crabtree, G.R., Neurotrophins and netrins require calcineurin/NFAT signaling to stimulate outgrowth of embryonic axons (2003) Cell, 113, pp. 657-670. , CrossRef Medline
  • Hagedorn, L., Paratore, C., Brugnoli, G., Baert, J.L., Mercader, N., Suter, U., Sommer, L., The Ets domain transcription factor Erm distinguishes rat satellite glia from Schwann cells and is regulated in satellite cells by neuregulin signaling (2000) Dev Biol, 219, pp. 44-58. , CrossRef Medline
  • Harrington, A.W., Ginty, D.D., Long-distance retrograde neurotrophic factor signalling in neurons (2013) Nat Rev Neurosci, 14, pp. 177-187. , CrossRef Medline
  • Hippenmeyer, S., Vrieseling, E., Sigrist, M., Portmann, T., Laengle, C., Ladle, D.R., Arber, S., A developmental switch in the response of DRG neurons to ETS transcription factor signaling (2005) PLoS Biol, 3, pp. e159. , CrossRef Medline
  • Hollenhorst, P.C., McIntosh, L.P., Graves, B.J., Genomic and biochemical insights into the specificity of ETS transcription factors (2011) Annu Rev Biochem, 80, pp. 437-471. , CrossRef Medline
  • Holtzman, D.M., Li, Y., Parada, L.F., Kinsman, S., Chen, C.K., Valletta, J.S., Zhou, J., Mobley, W.C., p140trk mRNA marks NGF-responsive forebrain neurons: Evidence that trk gene expression is induced by NGF (1992) Neuron, 9, pp. 465-478. , CrossRef Medline
  • Huang, E.J., Reichardt, L.F., Neurotrophins: Roles in neuronal development and function (2001) Annu Rev Neurosci, 24, pp. 677-736. , CrossRef Medline
  • Huang, E.J., Reichardt, L.F., Trk receptors: Roles in neuronal signal transduction (2003) Annu Rev Biochem, 72, pp. 609-642. , CrossRef Medline
  • Lallemend, F., Ernfors, P., Molecular interactions underlying the specification of sensory neurons (2012) Trends Neurosci, 35, pp. 373-381. , CrossRef Medline
  • Ledda, F., Paratcha, G., Ibanez, C.F., Target-derived GFRalpha1 as an attractive guidance signal for developing sensory and sympathetic axons via activation of Cdk5 (2002) Neuron, 36, pp. 387-401. , CrossRef Medline
  • Ledda, F., Paratcha, G., Sandoval-Guzman, T., Ibanez, C.F., GDNF and GFRalpha1 promote formation of neuronal synapses by ligand-induced cell adhesion (2007) Nat Neurosci, 10, pp. 293-300. , CrossRef Medline
  • Ledda, F., Bieraugel, O., Fard, S.S., Vilar, M., Paratcha, G., Lrig1 is an endogenous inhibitor of Ret receptor tyrosine kinase activation, downstream signaling, and biological responses to GDNF (2008) J Neurosci, 28, pp. 39-49. , CrossRef Medline
  • Li, R., Pei, H., Watson, D.K., Regulation of Ets function by proteinprotein interactions (2000) Oncogene, 19, pp. 6514-6523. , CrossRef Medline
  • Lin, J.H., Saito, T., Anderson, D.J., Lance-Jones, C., Jessell, T.M., Arber, S., Functionally related motor neuron pool and muscle sensory afferent subtypes defined by coordinate ETS gene expression (1998) Cell, 95, pp. 393-407. , CrossRef Medline
  • Lonze, B.E., Ginty, D.D., Function and regulation of CREB family transcription factors in the nervous system (2002) Neuron, 35, pp. 605-623. , CrossRef Medline
  • Lu, B.C., Cebrian, C., Chi, X., Kuure, S., Kuo, R., Bates, C.M., Arber, S., Costantini, F., Etv4 and Etv5 are required downstream of GDNF and Ret for kidney branching morphogenesis (2009) Nat Genet, 41, pp. 1295-1302. , CrossRef Medline
  • Luo, W., Wickramasinghe, S.R., Savitt, J.M., Griffin, J.W., Dawson, T.M., Ginty, D.D., AhierarchicalNGFsignaling cascade controls Ret-dependent and Ret-independent events during development of nonpeptidergic DRG neurons (2007) Neuron, 54, pp. 739-754. , CrossRef Medline
  • Mao, J., McGlinn, E., Huang, P., Tabin, C.J., McMahon, A.P., Fgf-dependent Etv4/5 activity is required for posterior restriction of Sonic Hedgehog and promoting outgrowth of the vertebrate limb (2009) Dev Cell, 16, pp. 600-606. , CrossRef Medline
  • Markus, A., Patel, T.D., Snider, W.D., Neurotrophic factors and axonal growth (2002) Curr Opin Neurobiol, 12, pp. 523-531. , CrossRef Medline
  • Neumar, R.W., Xu, Y.A., Gada, H., Guttmann, R.P., Siman, R., Cross-talk between calpain and caspase proteolytic systems during neuronal apoptosis (2003) J Biol Chem, 278, pp. 14162-14167. , CrossRef Medline
  • Nordstrom, L.A., Lochner, J., Yeung, W., Ciment, G., The metalloproteinase stromelysin-1 (transin) mediates PC12 cell growth cone invasiveness through basal laminae (1995) Mol Cell Neurosci, 6, pp. 56-68. , CrossRef Medline
  • Oh, S., Shin, S., Janknecht, R., ETV1, 4 and 5: An oncogenic subfamily of ETS transcription factors (2012) Biochim Biophys Acta, 1826, pp. 1-12. , CrossRef Medline
  • Oikawa, T., Yamada, T., Molecular biology of the Ets family of transcription factors (2003) Gene, 303, pp. 11-34. , CrossRef Medline
  • Page-McCaw, A., Ewald, A.J., Werb, Z., Matrix metalloproteinases and the regulation of tissue remodelling (2007) Nat Rev Mol Cell Biol, 8, pp. 221-233. , CrossRef Medline
  • Paratcha, G., Ledda, F., Ibanez, C.F., The neural cell adhesion molecule NCAM is an alternative signaling receptor for GDNF family ligands (2003) Cell, 113, pp. 867-870. , CrossRef Medline
  • Paratore, C., Brugnoli, G., Lee, H.Y., Suter, U., Sommer, L., The role of the Ets domain transcription factor Erm in modulating differentiation of neural crest stem cells (2002) Dev Biol, 250, pp. 168-180. , CrossRef Medline
  • Patel, T.D., Jackman, A., Rice, F.L., Kucera, J., Snider, W.D., Development of sensory neurons in the absence of NGF/TrkA signaling in vivo (2000) Neuron, 25, pp. 345-357. , CrossRef Medline
  • Patel, T.D., Kramer, I., Kucera, J., Niederkofler, V., Jessell, T.M., Arber, S., Snider, W.D., Peripheral NT3 signaling is required for ETS protein expression and central patterning of proprioceptive sensory afferents (2003) Neuron, 38, pp. 403-416. , CrossRef Medline
  • Pazyra-Murphy, M.F., Hans, A., Courchesne, S.L., Karch, C., Cosker, K.E., Heerssen, H.M., Watson, F.L., Segal, R.A., A retrograde neuronal survival response: Target-derived neurotrophins regulate MEF2D and bcl-w (2009) J Neurosci, 29, pp. 6700-6709. , CrossRef Medline
  • Riccio, A., Pierchala, B.A., Ciarallo, C.L., Ginty, D.D., An NGF-TrkAmediated retrograde signal to transcription factor CREB in sympathetic neurons (1997) Science, 277, pp. 1097-1100. , CrossRef Medline
  • Shirazi Fard, S., Kele, J., Vilar, M., Paratcha, G., Ledda, F., Tiam1 as a signaling mediator of nerve growth factor-dependent neurite outgrowth (2010) PLoS One, 5, pp. e9647. , CrossRef Medline
  • Tardif, G., Reboul, P., Pelletier, J.P., Martel-Pelletier, J., Ten years in the life of an enzyme: The story of the human MMP-13 (collagenase-3) (2004) Mod Rheumatol, 14, pp. 197-204. , Medline
  • Trojanowska, M., Ets factors and regulation of the extracellular matrix (2000) Oncogene, 19, pp. 6464-6471. , CrossRef Medline
  • Verger, A., Duterque-Coquillaud, M., When Ets transcription factors meet their partners (2002) Bioessays, 24, pp. 362-370. , CrossRef Medline
  • Wakamatsu, Y., Maynard, T.M., Weston, J.A., Fate determination of neural crest cells by NOTCH-mediated lateral inhibition and asymmetrical cell division during gangliogenesis (2000) Development, 127, pp. 2811-2821. , Medline
  • Wasylyk, B., Hagman, J., Gutierrez-Hartmann, A., Ets transcription factors: Nuclear effectors of the Ras-MAP-kinase signaling pathway (1998) Trends Biochem Sci, 23, pp. 213-216. , CrossRef Medline
  • Watson, F.L., Heerssen, H.M., Bhattacharyya, A., Klesse, L., Lin, M.Z., Segal, R.A., Neurotrophins use the Erk5 pathway to mediate a retrograde survival response (2001) Nat Neurosci, 4, pp. 981-988. , CrossRef Medline
  • Wickramasinghe, S.R., Alvania, R.S., Ramanan, N., Wood, J.N., Mandai, K., Ginty, D.D., Serum response factor mediates NGF-dependent target innervation by embryonic DRG sensory neurons (2008) Neuron, 58, pp. 532-545. , CrossRef Medline
  • Yan, C., Boyd, D.D., Regulation of matrix metalloproteinase gene expression (2007) J Cell Physiol, 211, pp. 19-26. , CrossRef Medline
  • Ye, H., Kuruvilla, R., Zweifel, L.S., Ginty, D.D., Evidence in support of signaling endosome-based retrograde survival of sympathetic neurons (2003) Neuron, 39, pp. 57-68. , CrossRef Medline
  • Yordy, J.S., Muise-Helmericks, R.C., Signal transduction and the Ets family of transcription factors (2000) Oncogene, 19, pp. 6503-6513. , CrossRef Medline
  • Zhang, Z., Verheyden, J.M., Hassell, J.A., Sun, X., FGF-regulated Etv genes are essential for repressing Shh expression in mouse limb buds (2009) Dev Cell, 16, pp. 607-613. , CrossRef Medline
  • Zhong, J., Li, X., McNamee, C., Chen, A.P., Baccarini, M., Snider, W.D., Raf kinase signaling functions in sensory neuron differentiation and axon growth in vivo (2007) Nat Neurosci, 10, pp. 598-607. , CrossRef Medline
  • Znosko, W.A., Yu, S., Thomas, K., Molina, G.A., Li, C., Tsang, W., Dawid, I.B., Tsang, M., Overlapping functions of Pea3 ETS transcription factors in FGF signaling during zebrafish development (2010) Dev Biol, 342, pp. 11-25. , CrossRef Medline
  • Zweifel, L.S., Kuruvilla, R., Ginty, D.D., Functions and mechanisms of retrograde neurotrophin signalling (2005) Nat Rev Neurosci, 6, pp. 615-625. , CrossRef Medline

Citas:

---------- APA ----------
Fontanet, P., Irala, D., Alsina, F.C., Paratcha, G. & Ledda, F. (2013) . Pea3 transcription factor family members Etv4 and Etv5 mediate retrograde signaling and axonal growth of DRG sensory neurons in response to NGF. Journal of Neuroscience, 33(40), 15940-15951.
http://dx.doi.org/10.1523/JNEUROSCI.0928-13.2013
---------- CHICAGO ----------
Fontanet, P., Irala, D., Alsina, F.C., Paratcha, G., Ledda, F. "Pea3 transcription factor family members Etv4 and Etv5 mediate retrograde signaling and axonal growth of DRG sensory neurons in response to NGF" . Journal of Neuroscience 33, no. 40 (2013) : 15940-15951.
http://dx.doi.org/10.1523/JNEUROSCI.0928-13.2013
---------- MLA ----------
Fontanet, P., Irala, D., Alsina, F.C., Paratcha, G., Ledda, F. "Pea3 transcription factor family members Etv4 and Etv5 mediate retrograde signaling and axonal growth of DRG sensory neurons in response to NGF" . Journal of Neuroscience, vol. 33, no. 40, 2013, pp. 15940-15951.
http://dx.doi.org/10.1523/JNEUROSCI.0928-13.2013
---------- VANCOUVER ----------
Fontanet, P., Irala, D., Alsina, F.C., Paratcha, G., Ledda, F. Pea3 transcription factor family members Etv4 and Etv5 mediate retrograde signaling and axonal growth of DRG sensory neurons in response to NGF. J. Neurosci. 2013;33(40):15940-15951.
http://dx.doi.org/10.1523/JNEUROSCI.0928-13.2013