The Role of Glial Cell Line-Derived Neurotrophic Factor in the Functioning of the Nervous System (Review)
Glial cell line-derived neurotrophic factor (GDNF) is one of the most important factors participating in the neuronal survival as well as promoting the differentiation and maintenance of various cellular populations in the central and peripheral nervous systems. In contrast to other neurotrophic factors, GDNF does not directly bind to its receptor. For the implementation of GDNF biological functions, the presence of co-receptor, acting as a mediator in the interaction with the receptor, is necessary required. Receptor with tyrosine kinase activity (Ret) regarded as the main receptor to GDNF, able to subsequent launch an intracellular molecular cascade.
Particular attention to GDNF investigation caused by the fact that, among other neurotrophic factors GDNF has potent neuroprotective effect. Therefore, GDNF is considered as a possible factor for the correction of various nervous system disorders, including neurodegenerative diseases.
In this review basic information concerning the molecular structure of GDNF and its receptors as well as the mechanisms for implementation the main functions of GDNF from the beginning of active receptor complex formation to the subsequent launching of intracellular signaling cascades until appropriate cellular response achieving, is collected. Furthermore, the review contains the data, indicating the possible GDNF effect on synaptogenesis.
- Chao M.V. Neurotrophins and their receptors: a convergence point for many signalling pathways. Nat Rev Neurosci 2003; 4(4): 299–309, http://dx.doi.org/10.1038/nrn1078.
- Davies A.M. Regulation of neuronal survival and death by extracellular signals during development. EMBO J 2003; 22(11): 2537–2545, http://dx.doi.org/10.1093/emboj/cdg254.
- Gomazkov O.A. Neyrotroficheskie faktory mozga: spravochno-informatsionnoe izdanie. CD-versiya [Brain-derived neurotrophic factor: the reference edition. CD-version]. Moscow; 2004.
- Sakharnova T.A., Vedunova M.V., Mukhina I.V. Brain-derived neurotrophic factor (BDNF) and its role in the functioning of the central nervous system. Neurochemical Journal 2012; 6(4): 251–259, http://dx.doi.org/10.1134/s1819712412030129.
- Vedunova M.V., Mishchenko T.A., Mitroshina E.V., Mukhina I.V. TrkB-mediated neuroprotective and antihypoxic properties of brain-derived neurotrophic factor. Oxid Med Cell Longev 2015; 2015: 453901, http://dx.doi.org/10.1155/2015/453901.
- Costantini F., Shakya R. GDNF/Ret signaling and the development of the kidney. Bioessays 2006; 28(2): 117–127, http://dx.doi.org/10.1002/bies.20357.
- Naughton C.K., Jain S., Strickland A.M., Gupta A., Milbrandt J. Glial cell-line derived neurotrophic factor-mediated RET signaling regulates spermatogonial stem cell fate. Biol Reprod 2006; 74(2): 314–321, http://dx.doi.org/10.1095/biolreprod.105.047365.
- Mironov V.I., Romanov A.S., Simonov A.Y., Vedunova M.V., Kazantsev V.B. Oscillations in a neurite growth model with extracellular feedback. Neurosci Lett 2014; 570: 16–20, http://dx.doi.org/10.1016/j.neulet.2014.03.041.
- Mickiewicz A.L., Kordower J.H. GDNF family ligands: a potential future for Parkinson’s disease therapy. CNS Neurol Disord Drug Targets 2011; 10(6): 703–711, http://dx.doi.org/10.2174/187152711797247876.
- Duarte E.P., Curcio M., Canzoniero L.M., Duarte C.B. Neuroprotection by GDNF in the ischemic brain. Growth Factors 2012; 30(4): 242–257, http://dx.doi.org/10.3109/08977194.2012.691478.
- Allen S.J., Watson J.J., Shoemark D.K., Barua N.U., Patel N.K. GDNF, NGF and BDNF as therapeutic options for neurodegeneration. Pharmacol Ther 2013; 138(2): 155–175, http://dx.doi.org/10.1016/j.pharmthera.2013.01.004.
- Vedunova М.V., Sakharnova Т.А., Mitroshina E.V., Shishkina T.V., Astrakhanova T.A., Mukhina I.V. Antihypoxic and neuroprotective properties of BDNF and GDNF in vitro and in vivo under hypoxic conditions. Sovremennye tehnologii v medicine 2014; 6(4): 38–47.
- Lin L.F., Doherty D.H., Lile J.D., Bektesh S., Collins F. GDNF: a glial cell line-derived neurotrophic factor for midbrain dopaminergic neurons. Science 1993; 260(5111): 1130–1132, http://dx.doi.org/10.1126/science.8493557.
- He Z., Jiang J., Kokkinaki M., Golestaneh N., Hofmann M.C., Dym M. GDNF upregulates c-Fos transcription via the Ras/Erk1/2 pathway to promote mouse spermatogonial stem cell proliferation. Stem Cells 2008; 26(1): 266–278, http://dx.doi.org/10.1634/stemcells.2007-0436.
- Eigenbrot C., Gerber N. X-ray structure of glial cell-derived neurotrophic factor at 1.9 A resolution and implications for receptor binding. Nat Struct Biol 1997; 4(6): 435–438, http://dx.doi.org/10.1038/nsb0697-435.
- Chen Z.Y., He Z.Y., He C., Lu C.L., Wu X.F. Human glial cell-line-derived neurotrophic factor: a structure-function analysis. Biochem Biophys Res Commun 2000; 268(3): 692–696, http://dx.doi.org/10.1006/bbrc.2000.2196.
- Chen Z., He Z., He C., Lu C., Wu X. A structure-function analysis of human GDNF. Acta Biochimica et Biophysica Sinica 2000; 32(3): 243–247.
- Parkash V., Lindholm P., Peränen J., Kalkkinen N., Oksanen E., Saarma M., Leppänen V.M., Goldman A. The structure of the conserved neurotrophic factors MANF and CDNF explains why they are bifunctional. Protein Eng Des Sel 2009; 22(4): 233–241, http://dx.doi.org/10.1093/protein/gzn080.
- Lonka-Nevalaita L., Lume M., Leppänen S., Jokitalo E., Peränen J., Saarma M. Characterization of the intracellular localization, processing, and secretion of two glial cell line-derived neurotrophic factor splice isoforms. J Neurosci 2010; 30(34): 11403–11413, http://dx.doi.org/10.1523/JNEUROSCI.5888-09.2010.
- Airavaara M., Pletnikova O., Doyle M.E., Zhang Y.E., Troncoso J.C., Liu Q.R. Identification of novel GDNF isoforms and cis-antisense GDNFOS gene and their regulation in human middle temporal gyrus of Alzheimer disease. J Biol Chem 2011; 286(52): 45093–45102, http://dx.doi.org/10.1074/jbc.M111.310250.
- Schindelhauer D., Schuffenhauer S., Gasser T., Steinkasserer A., Meitinger T. The gene coding for glial cell line derived neurotrophic factor (GDNF) maps to chromosome 5p12-p13.1. Genomics 1995; 28(3): 605–607, http://dx.doi.org/10.1006/geno.1995.1202.
- Woodbury D., Schaar D.G., Ramakrishnan L., Black I.B. Novel structure of the human GDNF gene. Brain Res 1998; 803(1–2): 95–104, http://dx.doi.org/10.1016/S0006-8993(98)00627-1.
- Sariola H., Saarma M. Novel functions and signalling pathways for GDNF. J Cell Sci 2003; 116(Pt 19): 3855–3862, http://dx.doi.org/10.1242/jcs.00786.
- Kotzbauer P.T., Lampe P.A., Heuckeroth R.O., Golden J.P., Creedon D.J., Johnson E.M. Jr., Milbrandt J. Neurturin, a relative of glial-cell-line-derived neurotrophic factor. Nature 1996; 384(6608): 467–470, http://dx.doi.org/10.1038/384467a0.
- Horger B.A., Nishimura M.C., Armanini M.P., Wang L.S., Poulsen K.T., Rosenblad C., Kirik D., Moffat B., Simmons L., Johnson E. Jr., Milbrandt J., Rosenthal A., Bjorklund A., Vandlen R.A., Hynes M.A., Phillips H.S. Neurturin exerts potent actions on survival and function of midbrain dopaminergic neurons. J Neurosci 1998; 18(13): 4929–4937.
- Zihlmann K.B., Ducray A.D., Schaller B., Huber A.W., Krebs S.H., Andres R.H., Seiler R.W., Meyer M., Widmer H.R. The GDNF family members neurturin, artemin and persephin promote the morphological differentiation of cultured ventral mesencephalic dopaminergic neurons. Brain Res Bull 2005; 68(1–2): 42–53, http://dx.doi.org/10.1016/j.brainresbull.2004.10.012.
- Widenfalk J., Nosrat C., Tomac A., Westphal H., Hoffer B., Olson L. Neurturin and glial cell line-derived neurotrophic factor receptor-beta (GDNFR-beta), novel proteins related to GDNF and GDNFR-alpha with specific cellular patterns of expression suggesting roles in the developing and adult nervous system and in peripheral organs. J Neurosci 1997; 17(21): 8506–8519.
- Luukko K., Saarma M., Thesleff I. Neurturin mRNA expression suggests roles in trigeminal innervation of the first branchial arch and in tooth formation. Dev Dyn 1998; 213(2): 207–219, http://dx.doi.org/10.1002/(SICI)1097-0177(199810)213:2207::AID-AJA63.0.CO;2-K.
- Milbrandt J., de Sauvage F.J., Fahrner T.J., Baloh R.H., Leitner M.L., Tansey M.G., Lampe P.A., Heuckeroth R.O., Kotzbauer P.T., Simburger K.S., Golden J.P., Davies J.A., Vejsada R., Kato A.C., Hynes M., Sherman D., Nishimura M., Wang L.C., Vandlen R., Moffat B., Klein R.D., Poulsen K., Gray C., Garce A., Johnson E.M. Jr. Persephin, a novel neurotrophic factor related to GDNF and neurturin. Neuron 1998; 20(2): 245–253, http://dx.doi.org/10.1016/S0896-6273(00)80453-5.
- Golden J.P., DeMaro J.A., Osborne P.A., Milbrandt J., Johnson E.M. Jr. Expression of neurturin, GDNF, and GDNF family-receptor mRNA in the developing and mature mouse. Exp Neurol 1999; 158(2): 504–528, http://dx.doi.org/10.1006/exnr.1999.7127.
- Golden J.P., Milbrandt J., Johnson E.M. Jr. Neurturin and persephin promote the survival of embryonic basal forebrain cholinergic neurons in vitro. Exp Neurol 2003; 184(1): 447–455, http://dx.doi.org/10.1016/j.expneurol.2003.07.999.
- Baloh R.H., Tansey M.G., Lampe P.A., Fahrner T.J., Enomoto H., Simburger K.S., Leitner M.L., Araki T., Johnson E.M. Jr., Milbrandt J. Artemin, a novel member of the GDNF ligand family, supports peripheral and central neurons and signals through the GFRalpha3-RET receptor complex. Neuron 1998; 21(6): 1291–1302, http://dx.doi.org/10.1016/S0896-6273(00)80649-2.
- Nishino J., Mochida K., Ohfuji Y., Shimazaki T., Meno C., Ohishi S., Matsuda Y., Fujii H., Saijoh Y., Hamada H. GFR alpha3, a component of the artemin receptor, is required for migration and survival of the superior cervical ganglion. Neuron 1999; 23(4): 725–736,http://dx.doi.org/10.1016/S0896-6273(01)80031-3.
- Honma Y., Araki T., Gianino S., Bruce A., Heuckeroth R., Johnson E., Milbrandt J. Artemin is a vascular-derived neurotropic factor for developing sympathetic neurons. Neuron 2002; 35(2): 267–282, http://dx.doi.org/10.1016/S0896-6273(02)00774-2.
- Gardell L.R., Wang R., Ehrenfels C., Ossipov M.H., Rossomando A.J., Miller S., Buckley C., Cai A.K., Tse A., Foley S.F., Gong B., Walus L., Carmillo P., Worley D., Huang C., Engber T., Pepinsky B., Cate R.L., Vanderah T.W., Lai J., Sah D.W., Porreca F. Multiple actions of systemic artemin in experimental neuropathy. Nat Med 2003; 9(11): 1383–1389, http://dx.doi.org/10.1038/nm944.
- Bennett D.L., Boucher T.J., Michael G.J., Popat R.J., Malcangio M., Averill S.A., Poulsen K.T., Priestley J.V., Shelton D.L., McMahon S.B. Artemin has potent neurotrophic actions on injured C-fibres. J Peripher Nerv Syst 2006; 11(4): 330–345, http://dx.doi.org/10.1111/j.1529-8027.2006.00106.x.
- Thornton P., Hatcher J.P., Robinson I., Sargent B., Franzén B., Martino G., Kitching L., Glover C.P., Anderson D., Forsmo-Bruce H., Low C.P., Cusdin F., Dosanjh B., Williams W., Steffen A.C., Thompson S., Eklund M., Lloyd C., Chessell I., Hughes J. Artemin-GFRα3 interactions partially contribute to acute inflammatory hypersensitivity. Neurosci Lett 2013; 545: 23–28, http://dx.doi.org/10.1016/j.neulet.2013.04.007.
- Jing S., Wen D., Yu Y., Holst P.L., Luo Y., Fang M., Tamir R., Antonio L., Hu Z., Cupples R., Louis J.C., Hu S., Altrock B.W., Fox G.M. GDNF-induced activation of the ret protein tyrosine kinase is mediated by GDNFR-alpha, a novel receptor for GDNF. Cell 1996; 85(7): 1113–1124, http://dx.doi.org/10.1016/S0092-8674(00)81311-2.
- Treanor J.J., Goodman L., de Sauvage F., Stone D.M., Poulsen K.T., Beck C.D., Gray C., Armanini M.P., Pollock R.A., Hefti F., Phillips H.S., Goddard A., Moore M.W., Buj-Bello A., Davies A.M., Asai N., Takahashi M., Vandlen R., Henderson C.E., Rosenthal A. Characterization of a multicomponent receptor for GDNF. Nature 1996; 382(6586): 80–83, http://dx.doi.org/10.1038/382080a0.
- Aron L. Genetic analysis of dopaminergic neuron survival GDNF/Ret signaling and the Parkinson’s disease-associated gene DJ-1 [dissertation]. München: Ludwig-Maximilians-Universität München; 2009.
- Serra M.P., Quartu M., Mascia F., Manca A., Boi M., Pisu M.G., Lai M.L., Del Fiacco M. Ret, GFRalpha-1, GFRalpha-2 and GFRalpha-3 receptors in the human hippocampus and fascia dentate. Int J Dev Neurosci 2005; 23: 425–438, http://dx.doi.org/10.1016/j.ijdevneu.2005.05.003.
- Airaksinen M.S., Saarma M. The GDNF family: signalling, biological functions and therapeutic value. Nat Rev Neurosci 2002; 3(5): 383–394, http://dx.doi.org/10.1038/nrn812.
- Lucini C., Facello B., Maruccio L., Langellotto F., Sordino P., Castaldo L. Distribution of glial cell line-derived neurotrophic factor receptor alpha-1 in the brain of adult zebrafish. J Anat 2010; 217(2): 174–185, http://dx.doi.org/10.1111/j.1469-7580.2010.01254.x.
- Tomac A., Widenfalk J., Lin L.F., Kohno T., Ebendal T., Hoffer B.J., Olson L. Retrograde axonal transport of glial cell line-derived neurotrophic factor in the adult nigrostriatal system suggests a trophic role in the adult. Proc Natl Acad Sci USA 1995; 92(18): 8274–8278,http://dx.doi.org/10.1073/pnas.92.18.8274.
- Leitner M.L., Molliver D.C., Osborne P.A., Vejsada R., Golden J.P., Lampe P.A., Kato A.C., Milbrandt J., Johnson E.M. Jr. Analysis of the retrograde transport of glial cell line-derived neurotrophic factor (GDNF), neurturin, and persephin suggests that in vivo signaling for the GDNF family is GFRalpha coreceptor-specific. J Neurosci 1999; 19(21): 9322–9331.
- Rind H.B., Butowt R., von Bartheld C.S. Synaptic targeting of retrogradely transported trophic factors in motoneurons: comparison of glial cell line-derived neurotrophic factor, brain-derived neurotrophic factor, and cardiotrophin-1 with tetanus toxin. J Neurosci 2005; 25(3): 539–549,http://dx.doi.org/10.1523/jneurosci.4322-04.2005.
- Tsui C.C., Pierchala B.A. The differential axonal degradation of Ret accounts for cell-type-specific function of glial cell line-derived neurotrophic factor as a retrograde survival factor. J Neurosci 2010; 30: 5149–5158, http://dx.doi.org/10.1523/JNEUROSCI.5246-09.2010.
- Baloh R.H., Tansey M.G., Golden J.P., Creedon D.J., Heuckeroth R.O., Keck C.L., Zimonjic D.B., Popescu N.C., Johnson E.M. Jr., Milbrandt J. TrnR2, a novel receptor that mediates neurturin and GDNF signaling through Ret. Neuron 1997; 18(5): 793–802, http://dx.doi.org/10.1016/S0896-6273(00)80318-9.
- Buj-Bello A., Adu J., Piñón L.G., Horton A., Thompson J., Rosenthal A., Chinchetru M., Buchman V.L., Davies A.M. Neurturin responsiveness requires a GPI-linked receptor and the Ret receptor tyrosine kinase. Nature 1997; 387(6634): 721–724, http://dx.doi.org/10.1038/42729.
- Klein R.D., Sherman D., Ho W.H., Stone D., Bennett G.L., Moffat B., Vandlen R., Simmons L., Gu Q., Hongo J.A., Devaux B., Poulsen K., Armanini M., Nozaki C., Asai N., Goddard A., Phillips H., Henderson C.E., Takahashi M., Rosenthal A. A GPI-linked protein that interacts with Ret to form a candidate neurturin receptor. Nature 1997; 387: 717–721, http://dx.doi.org/10.1038/42722.
- Sanicola M., Hession C., Worley D., Carmillo P., Ehrenfels C., Walus L., Robinson S., Jaworski G., Wei H., Tizard R., Whitty A., Pepinsky R.B., Cate R.L. Glial cell line-derived neurotrophic factor-dependent RET activation can be mediated by two different cell-surface accessory proteins. Proc Natl Acad Sci USA 1997; 94(12): 6238–6243, http://dx.doi.org/10.1073/pnas.94.12.6238.
- Naveilhan P., Baudet C., Mikaels A., Shen L., Westphal H., Ernfors P. Expression and regulation of GFRalpha3, a glial cell line-derived neurotrophic factor family receptor. Proc Natl Acad Sci USA 1998; 95(3): 1295–1300, http://dx.doi.org/10.1073/pnas.95.3.1295.
- Widenfalk J., Tomac A., Lindqvist E., Hoffer B., Olson L. GFRalpha-3, a protein related to GFRalpha-1, is expressed in developing peripheral neurons and ensheathing cells. Eur J Neurosci 1998; 10(4): 1508–1517, http://dx.doi.org/10.1046/j.1460-9568.1998.00192.x.
- Enokido Y., de Sauvage F., Hongo J.A., Ninkina N., Rosenthal A., Buchman V.L., Davies A.M. GFRalpha-4 and the tyrosine kinase Ret form a functional receptor complex for persephin. Curr Biol 1998; 8(18): 1019–1022, http://dx.doi.org/10.1016/s0960-9822(07)00422-8.
- Lindahl M., Poteryaev D., Yu L., Arumae U., Timmusk T., Bongarzone I., Aiello A., Pierotti M.A., Airaksinen M.S., Saarma M. Human glial cell line-derived neurotrophic factor receptor alpha 4 is the receptor for persephin and is predominantly expressed in normal and malignant thyroid medullary cells. J Biol Chem 2001; 276(12): 9344–9351, http://dx.doi.org/10.1074/jbc.m008279200.
- Creedon D.J., Tansey M.G., Baloh R.H., Osborne P.A., Lampe P.A., Fahrner T.J., Heuckeroth R.O., Milbrandt J., Johnson E.M. Jr. Neurturin shares receptors and signal transduction pathways with glial cell line-derived neurotrophic factor in sympathetic neurons. Proc Natl Acad Sci USA 1997; 94(13): 7018–7023,http://dx.doi.org/10.1073/pnas.94.13.7018.
- Suvanto P., Wartiovaara K., Lindahl M., Arumae U., Moshnyakov M., Horelli-Kuitunen N., Airaksinen M.S., Palotie A., Sariola H., Saarma M. Cloning, mRNA distribution and chromosomal localisation of the gene for glial cell line-derived neurotrophic factor receptor beta, a homologue to GDNFR-alpha. Hum Mol Genet 1997; 6(8): 1267–1273, http://dx.doi.org/10.1093/hmg/6.8.1267.
- Airaksinen M.S., Titievsky A., Saarma M. GDNF family neurotrophic factor signaling: four masters, one servant? Mol Cell Neurosci 1999; 13(5): 313–325, http://dx.doi.org/10.1006/mcne.1999.0754.
- Dey B.K., Wong Y.W., Too H.P. Cloning of a novel murine isoform of the glial cell line-derived neurotrophic factor receptor. Neuroreport 1998; 9(1): 37–42, http://dx.doi.org/10.1097/00001756-199801050-00008.
- Shefelbine S.E., Khorana S., Schultz P.N., Huang E., Thobe N., Hu Z.J., Fox G.M., Jing S., Cote G.J., Gagel R.F. Mutational analysis of the GDNF/RET-GDNFR alpha signaling complex in a kindred with vesicoureteral reflux. Hum Genet 1998; 102(4): 474–478,http://dx.doi.org/10.1007/s004390050724.
- Yoong L.F., Peng Z.N., Wan G., Too H.P. Tissue expression of alternatively spliced GFRalpha1, NCAM and RET isoforms and the distinct functional consequence of ligand-induced activation of GFRalpha1 isoforms. Brain Res Mol Brain Res 2005; 139(1): 1–12,http://dx.doi.org/10.1016/j.molbrainres.2005.05.016.
- Baloh R.H., Enomoto H., Johnson E.M. Jr., Milbrandt J. The GDNF family ligands and receptors — implications for neural development. Curr Opin Neurobiol 2000; 10(1): 103–110, http://dx.doi.org/10.1016/s0959-4388(99)00048-3.
- Wang X. Structural studies of GDNF family ligands with their receptors — Insights into ligand recognition and activation of receptor tyrosine kinase RET. Biochim Biophys Acta 2013; 1834(10): 2205–2212, http://dx.doi.org/10.1016/j.bbapap.2012.10.008.
- Takahashi M., Ritz J., Cooper G.M. Activation of a novel human transforming gene, ret, by DNA rearrangement. Cell 1985; 42(2): 581–588, http://dx.doi.org/10.1016/0092-8674(85)90115-1.
- Iwamoto T., Taniguchi M., Asai N., Ohkusu K., Nakashima I., Takahashi M. cDNA cloning of mouse ret proto-oncogene and its sequence similarity to the cadherin superfamily. Oncogene 1993; 8(4): 1087–1091.
- Schneider R. The human protooncogene ret: a communicative cadherin? Trends Biochem Sci 1992; 17(11): 468–469, http://dx.doi.org/10.1016/0968-0004(92)90490-z.
- Traugott A.L., Moley J.F. The RET protooncogene. Cancer Treat Res 2010; 153: 303–319, http://dx.doi.org/10.1007/978-1-4419-0857-5_17.
- Anders J., Kjar S., Ibáсez C.F. Molecular modeling of the extracellular domain of the RET receptor tyrosine kinase reveals multiple cadherin-like domains and a calcium-binding site. J Biol Chem 2001; 276(38): 35808–35817, http://dx.doi.org/10.1074/jbc.m104968200.
- Nozaki C., Asai N., Murakami H., Iwashita T., Iwata Y., Horibe K., Klein R.D., Rosenthal A., Takahashi M. Calcium-dependent Ret activation by GDNF and neurturin. Oncogene 1998; 16(3): 293–299, http://dx.doi.org/10.1038/sj.onc.1201548.
- van Weering D.H., Bos J.L. Signal transduction by the receptor tyrosine kinase Ret. Recent Results Cancer Res 1998; 154: 271–281, http://dx.doi.org/10.1007/978-3-642-46870-4_18.
- van Weering D.H., Moen T.C., Braakman I., Baas P.D., Bos J.L. Expression of the receptor tyrosine kinase Ret on the plasma membrane is dependent on calcium. J Biol Chem 1998; 273(20): 12077–12081, http://dx.doi.org/10.1074/jbc.273.20.12077.
- Ibáñez C.F. Structure and physiology of the RET receptor tyrosine kinase. Cold Spring Harb Perspect Biol 2013; 5(2): a009134, http://dx.doi.org/10.1101/cshperspect.a009134.
- Runeberg-Roos P., Saarma M. Neurotrophic factor receptor RET: structure, cell biology, and inherited diseases. Ann Med 2007; 39(8): 572–580, http://dx.doi.org/10.1080/07853890701646256.
- Liu X., Vega Q.C., Decker R.A., Pandey A., Worby C.A., Dixon J.E. Oncogenic RET receptors display different autophosphorylation sites and substrate binding specificities. J Biol Chem 1996; 271(10): 5309–5312, http://dx.doi.org/10.1074/jbc.271.10.5309.
- Kawamoto Y., Takeda K., Okuno Y., Yamakawa Y., Ito Y., Taguchi R., Kato M., Suzuki H., Takahashi M., Nakashima I. Identification of RET autophosphorylation sites by mass spectrometry. J Biol Chem 2004; 279(14): 14213–14224, http://dx.doi.org/10.1074/jbc.m312600200.
- Lemmon M.A., Schlessinger J. Cell signaling by receptor tyrosine kinases. Cell 2010; 141(7): 1117–1134, http://dx.doi.org/10.1016/j.cell.2010.06.011.
- Dhillon A.S., Hagan S., Rath O., Kolch W. MAP kinase signalling pathways in cancer. Oncogene 2007; 26(22): 3279–3290, http://dx.doi.org/10.1038/sj.onc.1210421.
- Krishna M., Narang H. The complexity of mitogen-activated protein kinases (MAPKs) made simple. Cell Mol Life Sci 2008; 65(22): 3525–3544, http://dx.doi.org/10.1007/s00018-008-8170-7.
- Yang S.H., Sharrocks A.D., Whitmarsh A.J. MAP kinase signalling cascades and transcriptional regulation. Gene 2013; 513(1): 1–13, http://dx.doi.org/10.1016/j.gene.2012.10.033.
- Raman M., Chen W., Cobb M.H. Differential regulation and properties of MAPKs. Oncogene 2007; 26(22): 3100–3112, http://dx.doi.org/10.1038/sj.onc.1210392.
- Turjanski A.G., Vaqué J.P., Gutkind J.S. MAP kinases and the control of nuclear events. Oncogene 2007; 26(22): 3240–3253, http://dx.doi.org/10.1038/sj.onc.1210415.
- Reichardt L.F. Neurotrophin-regulated signalling pathways. Philos Trans R Soc Lond B Biol Sci 2006; 361(1473): 1545–1564, http://dx.doi.org/10.1098/rstb.2006.1894.
- Ron D., Janak P.H. GDNF and addiction. Rev Neurosci 2005; 16(4): 277–285, http://dx.doi.org/10.1515/revneuro.2005.16.4.277.
- Manning B.D., Cantley L.C. AKT/PKB signaling: navigating downstream. Cell 2007; 129(7): 1261–1274, http://dx.doi.org/10.1016/j.cell.2007.06.009.
- Kim D., Chung J. Akt: versatile mediator of cell survival and beyond. J Biochem Mol Biol 2002; 35(1): 106–115, http://dx.doi.org/10.5483/bmbrep.2002.35.1.106.
- Datta S.R., Brunet A., Greenberg M.E. Cellular survival: a play in three Akts. Genes Dev 1999; 13(22): 2905–2927, http://dx.doi.org/10.1101/gad.13.22.2905.
- Paratcha G., Ledda F., Ibáсez C.F. The neural cell adhesion molecule NCAM is an alternative signaling receptor for GDNF family ligands. Cell 2003; 113(7): 867–879, http://dx.doi.org/10.1016/S0092-8674(03)00435-5.
- Schmutzler B.S., Roy S., Pittman S.K., Meadows R.M., Hingtgen C.M. Ret-dependent and Ret-independent mechanisms of Gfl-induced sensitization. Mol Pain 2011; 7: 22, http://dx.doi.org/10.1186/1744-8069-7-22.
- Gegelashvili G., Bock E., Schousboe A., Linnemann D. Two types of amyloid precursor protein (APP) mRNA in rat glioma cell lines: upregulation via a cyclic AMP-dependent pathway. Brain Res Mol Brain Res 1996; 37(1–2): 151–156, http://dx.doi.org/10.1016/0169-328x(95)00302-9.
- Owczarek S., Kristiansen L.V., Hortsch M., Walmod P.S. Cell adhesion molecules of the NCAM family and their roles at synapses. The Sticky Synapse 2009; 265–299, http://dx.doi.org/10.1007/978-0-387-92708-4_13.
- Ibáñez C.F. Beyond the cell surface: new mechanisms of receptor function. Biochem Biophys Res Commun 2010; 396(1): 24–27, http://dx.doi.org/10.1016/j.bbrc.2010.01.136.
- Canty A.J., Dietze J., Harvey M., Enomoto H., Milbrandt J., Ibáñez C.F. Regionalized loss of parvalbumin interneurons in the cerebral cortex of mice with deficits in GFRalpha1 signaling. J Neurosci 2009; 29(34): 10695–10705, http://dx.doi.org/10.1523/JNEUROSCI.2658-09.2009.
- Sjöstrand D., Ibáсez C.F. Insights into GFRalpha1 regulation of neural cell adhesion molecule (NCAM) function from structure-function analysis of the NCAM/GFRalpha1 receptor complex. J Biol Chem 2008; 283(20): 13792–13898, http://dx.doi.org/10.1074/jbc.M800283200.
- Yuste R. From the neuron doctrine to neural networks. Nat Rev Neurosci 2015; 16(8): 487–497, http://dx.doi.org/10.1038/nrn3962.
- Schlingloff D., Káli S., Freund T.F., Hájos N., Gulyás A.I. Mechanisms of sharp wave initiation and ripple generation. J Neurosci 2014; 20(34): 11385–11398, http://dx.doi.org/10.1523/JNEUROSCI.0867-14.2014.
- Tong M.T., Peace S.T., Cleland T.A. Properties and mechanisms of olfactory learning and memory. Front Behav Neurosci 2014; 8: 238, http://dx.doi.org/10.3389/fnbeh.2014.00238.
- Bourque M.J., Trudeau L.E. GDNF enhances the synaptic efficacy of dopaminergic neurons in culture. Eur J Neurosci 2000; 12(9): 3172–3180, http://dx.doi.org/10.1046/j.1460-9568.2000.00219.x.
- Nguyen Q.T., Parsadanian A.Sh., Snider W.D., Lichtman J.W. Hyperinnervation of neuromuscular junctions caused by GDNF overexpressionin muscle. Science 1998; 279: 1725–1729, http://dx.doi.org/10.1126/science.279.5357.1725
- Yang F., Feng L., Zheng F., Johnson S.W., Du J., Shen L., Wu C.P., Lu B. GDNF acutely modulates excitability and A-type K(+) channels in midbrain dopaminergic neurons. Nat Neurosci 2001; 4(11): 1071–1078, http://dx.doi.org/10.1038/nn734.
- Wang C.Y., Yang F., He X.P., Je H.S., Zhou J.Z., Eckermann K., Kawamura D., Feng L., Shen L., Lu B. Regulation of neuromuscular synapse development by glial cell line-derived neurotrophic factor and neurturin. J Biol Chem 2002; 277(12): 10614–10625,http://dx.doi.org/10.1074/jbc.M106116200.
- Wang J., Chen G., Lu B., Wu C.P. GDNF acutely potentiates Ca2+ channels and excitatory synaptic transmission in midbrain dopaminergic neurons. Neurosignals 2003; 12(2): 78–88, http://dx.doi.org/10.1159/000071817.
- Weiss J.L., Burgoyne R.D. Sense and sensibility in the regulation of voltage-gated Ca2+ channels. Trends Neurosci 2002; 25(10): 489–491, http://dx.doi.org/10.1016/S0166-2236(02)02247-6.
- Ledda F., Paratcha G., Sandoval-Guzmán T., Ibáñez C.F. GDNF and GFRalpha1 promote formation of neuronal synapses by ligand-induced cell adhesion. Nat Neurosci 2007; 10(3): 293–300, http://dx.doi.org/10.1038/nn1855.
- Rutishauser U. Polysialic acid in the plasticity of the developing and adult vertebrate nervous system. Nat Rev Neurosci 2008; 9(1): 26–35, http://dx.doi.org/10.1038/nrn2285.
- Võikar V., Rossi J., Rauvala H., Airaksinen M.S. Impaired behavioural flexibility and memory in mice lacking GDNF family receptor alpha2. Eur J Neurosci 2004; 20(1): 308–312, http://dx.doi.org/10.1111/j.1460-9568.2004.03475.x.
- Paratcha G., Ledda F. GDNF and GFRalpha: a versatile molecular complex for developing neurons. Trends Neurosci 2008; 31(8): 384–391, http://dx.doi.org/10.1016/j.tins.2008.05.003.
- Choi D.W. Excitotoxic cell death. J Neurobiol 1992; 23(9): 1261–1276, http://dx.doi.org/10.1002/neu.480230915.
- Lipton S.A., Rosenberg P.A. Excitatory amino acids as a final common pathway for neurologic disorders. N Engl J Med 1994; 330(9): 613–622, http://dx.doi.org/10.1056/nejm199403033300907.
- Vedunova M., Sakharnova T., Mitroshina E., Perminova M., Pimashkin A., Zakharov Yu., Dityatev A., Mukhina I. Seizure-like activity in hyaluronidase-treated dissociated hippocampal cultures. Front Cell Neurosci 2013; 7: 149, http://dx.doi.org/10.3389/fncel.2013.00149.
- Brené S., Messer C., Okado H., Hartley M., Heinemann S.F., Nestler E.J. Regulation of GluR2 promoter activity by neurotrophic factors via a neuron-restrictive silencer element. Eur J Neurosci 2000; 12(5): 1525–1533, http://dx.doi.org/10.1046/j.1460-9568.2000.00040.x.