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The NGF System and its interplay with endocannabinoid signalling, from peripheral sensory terminals to the brain: new targets for the development of next generation drugs for neuropathic pain

Submitted (last update 26/05/2017)

Zhang MD, Su J, Adori C, Löw P, Borguis L, Kiehn O, Uhlen M, Mulder J, Harkany T, Hökfelt T. A role for the cacium binding protein NECAB2 in inflammatory pain. 2017, submitted.

In press (last update 26/05/2017)

Peng C, Li L, Zhang MD, Bengtsson Gonzales C, Parisien M, Belfer I, Usoskin D, Abdo H, Furlan A, Harkany T, Diatchenko L, Hökfelt T, Hjerling-Leffler J and Ernfors P. MicroRNA-183 cluster continuously scales mechanical pain sensitivity by regulating basal and neuropathic pain gene pathways. Science 2017, in press.

Published

Rivetti di Val Cervo P, Romanov RA, Spigolon G, Masini D, Martín-Montañez E, Toledo EM, La Manno G, Feyder M, Pifl C, Ng YH, Sánchez SP, Linnarsson S, Wernig M, Harkany T, Fisone G, Arenas E. Induction of functional dopamine neurons from human astrocytes in vitro and mouse astrocytes in a Parkinson’s disease model. Nat Biotechnol. 2017, 35:444-452.

Sánchez-Sánchez J, Arévalo JC. A Review on Ubiquitination of Neurotrophin Receptors: Facts and Perspectives, Int J Mol Sci. 2017 Mar 14;18(3). pii: E630. doi: 10.3390/ijms18030630. Review.

Busquets-Garcia A, Soria-Gómez E, Redon B, Mackenbach Y, Vallée M, Chaouloff F, Varilh M, Ferreira G, Piazza PV, Marsicano G. Pregnenolone blocks cannabinoid-induced acute psychotic-like states in mice. Mol Psychiatry. 2017. doi: 10.1038/mp.2017.4.

Piazza PV, Cota D, Marsicano G. The CB1 receptor as the cornerstone of exostasis. Neuron. 2017; 93:1252-1274.

Romanov RA, Zeisel A, Bakker J, Girach F, Hellysaz A, Tomer R, Alpár A, Mulder J, Clotman F, Keimpema E, Hsueh B, Crow AK, Martens H, Schwindling C, Calvigioni D, Bains JS, Máté Z, Szabó G, Yanagawa Y, Zhang MD, Rendeiro A, Farlik M, Uhlén M, Wulff P, Bock C, Broberger C, Deisseroth K, Hökfelt T, Linnarsson S, Horvath TL, Harkany T. Molecular interrogation of hypothalamic organization reveals distinct dopamine neuronal subtypes. Nat Neurosci. 2017; 20:176-188.

Marrone MC, Morabito A, Giustizieri M, Mattioli M, Marinelli S, Riganti L, Lombardi M, Chiurchiùc V, Leuti A, Murana E, Totaro A, Piomelli D, Oddi S, Maccarrone M, Ragozzino D, Verderio C and Marinelli S: TRPV1 channels are critical brain inflammation detectors and neuropathic pain biomarkers in mice. Nature Communication 2017 10.1038/NCOMMS15292

Francesca Paoletti, Cesira de Chiara, Geoff Kelly,  Sonia Covaceuszach, Francesca Malerba,  Robert Yan,  Doriano Lamba,  Antonino Cattaneo,  and  Annalisa Pastore, Conformational rigidity within plasticity promotes differential target recognition of Nerve Growth Factor, Front. Mol. Biosci. 3:83 doi: 10.3389/fmolb.2016.00083

Hebert-Chatelain E, Desprez T, Serrat R, Bellocchio L, Soria-Gomez E, Busquets-Garcia A, Pagano Zottola A, Delamarre A, Cannich A, Vincent P, M. Robin L, Terral G, García-Fernández M-D, Colavita M, Mazier W, Drago F, Puente N, Reguero L, Elezgarai I, Dupuy J-W, Cota D, Lopez-Rodriguez M-L, Barreda-Gómez G, Massa F, Grandes P, Bénard G*, Marsicano G*. A Cannabinoid Link Between Mitochondria and Memory. Nature 2016; 539:555-559.

Zhang MD, Barde S, Yang T, Lei B, Eriksson LI, Mathew JP, Andreska T, Akassoglou K, Harkany T, Hökfelt TG and Terrando N. Orthopedic surgery affects neuropeptide and BDNF expression at the spinal level and hippocampal levels. PNAS 2016; 113:E6686-E6695.

Sara B. Jager, Christian Bjerggaard Vaegter. Avoiding experimental bias by systematic antibody validation. NEURAL REGENERATION RESEARCH. 2016; Volume 11, Issue 7

Malerba F., Paoletti F., Cattaneo A. “NGF andproNGF reciprocal interference in immunoassays : open questions, criticalities and ways forward”, Front Mol Neurosci. 2016 Aug 3;9:63. doi: 10.3389/fnmol.2016.00063. eCollection 2016.PMID: 27536217

Anta, B., Martín-Rodríguez, C., Gomis-Pérez, C., Calvo, L., López-Benito, S., Calderón-García, A.A., Vicente-García, C., Villarroel, A. and Arévalo, J.C. Ubiquitin Specific Protease 36 (USP36) controls Neuronal precursor cell-Expressed Developmentally Down-regulated 4-2 (Nedd4-2) actions over the neurotrophin receptor TrkA and potassium voltage-gated channels 7.2/3 (Kv7.2/3). J. Biol. Chem. 2016 Jul 21. pii: jbc.M116.722637.

Marques S, Zeisel A, Codeluppi S, van Bruggen D, Mendanha Falcão A, Xiao L, Li H, Häring M, Hochgerner H, Romanov RA, Gyllborg D, Muñoz-Manchado AB, La Manno G, Lönnerberg P, Floriddia EM, Rezayee F, Ernfors P, Arenas E, Hjerling-Leffler J, Harkany T, Richardson WD, Linnarsson S, Castelo-Branco G. Oligodendrocyte heterogeneity in the mouse juvenile and adult central nervous system. Science. 2016, 352(6291):1326-9.

Colavita M, Terral G, Lemercier CE, Drago F, Marsicano G, Massa F. Layer-specific potentiation of network GABAergic inhibition in the CA1 area of the hippocampus. Sci Rep. 2016; 6:28454.

Blanchart A, Fernando R, Häring M, Assaife-Lopes N, Romanov RA, Andäng M, Harkany T, Ernfors P. Endogenous GABAA receptor activity suppresses glioma growth. Oncogene. 2016 Jul 4. doi: 10.1038/onc.2016.245.

Calvigioni D, Máté Z, Fuzik J, Girach F, Zhang MD, Varro A, Beiersdorf J, Schwindling C, Yanagawa Y, Dockray GJ, McBain CJ, Hökfelt T, Szabó G, Keimpema E, Harkany T. Functional Differentiation of Cholecystokinin-Containing Interneurons Destined for the Cerebral Cortex. Cereb Cortex. (2016) pii: bhw094. [Epub ahead of print]

Fuzik J, Zeisel A, Máté Z, Calvigioni D, Yanagawa Y, Szabó G, Linnarsson S, Harkany T. Integration of electrophysiological recordings with single-cell RNA-seq data identifies neuronal subtypes. Nat Biotechnol. (2016) 34(2):175-83.

Zhang MD, Barde S, Szodorai E, Josephson A, Mitsios N, Watanabe M, Attems J, Lubec G, Kovács GM, Uhlén M, Mulder J, Harkany T, Hökfelt T. Comparative anatomical distribution of neuronal calcium-binding protein (NECAB) 1 and -2 in rodent and human spinal cord. Brain Struct Funct. (2016) Feb 2. [Epub ahead of print]

Busquets Garcia A, Soria-Gomez E, Bellocchio L, Marsicano G. Cannabinoid receptor type-1: breaking the dogmas. F1000Res. 2016 May 24;5. pii: F1000 Faculty Rev-990.

Jimenez-Gonzalez, A., García-Concejo, A., López-Benito, S., Gonzalez-Nunez, V.,  Arévalo, J.C. and Rodriguez, R.E. Role of morphine, miR-212/132 and mu opioid receptor in the regulation of Bdnf in zebrafish embryos. BBA – General Subjects 2016. 1860(6): 1308-1316.

Urresti, J., Ruiz-Meana, M., Coccia, E., Arévalo, J.C., Castellano, J., Fernandez-Sanz, C., Galenkamp, K.M.O., Planells-Ferrer, L., Moubarak, R.S., Llecha-Cano, N., Reix, S., Garcia-Dorado, D., Barneda-Zahonero, B. and Comella, J.X. Lifeguard inhibits Fas ligand-mediated endoplasmic reticulum-calcium release mandatory for apoptosis in type II apoptotic cells. J. Biol. Chem. 2016; 291:1221-34.

López-Benito, S., Lillo, C., Hernández-Hernández, A., Chao, M.V. and Arévalo, J.C. 2016. ARMS/Kidins220 and Synembryn-B levels regulate NGF-mediated secretion. J. Cell Science Mar 10. pii: jcs.184168. [Epub ahead of print]

Francesca Malerba , Francesca Paoletti, Bruno Bruni Ercole, Serena Materazzi, Romina Nassini, Elisabetta Coppi, Riccardo Patacchini, Simona Capsoni, Doriano Lamba, Antonino Cattaneo, Functional Characterization of Human ProNGF and NGF Mutants: Identification of NGF P61SR100E as a “Painless” Lead Investigational Candidate for Therapeutic Applications, PLOS ONE Sept. 15, 2015

Busquets-Garcia A, Desprez T, Metna-Laurent M, Bellocchio LMarsicano GSoria-Gomez E. Dissecting the cannabinergic control of behavior: The where matters. Bioessays. 2015 Nov;37(11):1215-25.

Malenczyk K, Keimpema E, Piscitelli F, Calvigioni D, Björklund P, Mackie K, Di Marzo V, Hökfelt TG*, Dobrzyn A, Harkany T*. Fetal endocannabinoids orchestrate the organization of pancreatic islet microarchitecture. Proc Natl Acad Sci USA (2015) Oct 22. pii: 201519040.

Soria-Gómez E, Busquets-Garcia A, Hu F, Mehidi A, Cannich A, Roux L, Louit I, Alonso L, Wiesner T, Georges F, Verrier D, Vincent P, Ferreira G, Luo M, Marsicano G. Habenular CB1 Receptors Control the Expression of Aversive Memories. Neuron. 2015 Oct 21;88(2):306-13. doi: 10.1016/j.neuron.2015.08.035. Press release related to this paper: http://presse.inserm.fr/en/should-i-stay-or-should-i-go-on-the-importance-of-aversive-memories-and-the-endogenous-cannabinoid-system/20775/?add_doc=20775

Covaceuszach S, Konarev PV, Cassetta A, Paoletti F, Svergun DI, Lamba D, Cattaneo A., The conundrum of the high-affinity NGF binding site formation unveiled? Biophys J. 2015 Feb 3;108(3):687-97.  doi: 10.1016/j.bpj.2014.11.3485

Metna-Laurent M, Marsicano G. Rising stars: modulation of brain functions by astroglial type-1 cannabinoid receptors.  Glia. 2015 Mar;63(3):353-64. [WP1]

Arévalo, J.C. 2015. Nedd4-2 regulation of voltage-gated ion channels: an update on structure-function relationships and the pathophysiological consequences of dysfunction. Journal of Receptor, Ligand and Channel Research 8: 53-63.

Paniagua, A.E., Herranz-Martín, S., Jimeno, D., Jimeno, A., López-Benito, S., Arévalo, J.C., Velasco, A., Aijón, J. and Lillo C. 2015. CRB2 completes a fully expressed Crumbs complex in the Retinal Pigment Epithelium. Scientific Reports 5: 14504.

Calvo, L., Anta, B., López-Benito, S., Martín-Rodríguez, C., Lee, F.S., Pérez, P., Martín-Zanca, D. and Arévalo, J.C. Bex3 dimerization regulates NGF-dependent neuronal survival and differentiation by enhancing trkA gene transcription. J. Neurosci. 2015; 35: 7190-7202.

Lamas, V., Arévalo, J.C., Juiz, J.M., Merchán, M.A. 2015. Acoustic input and efferent activity regulate the expression of molecules involved in cochlear micromechanics. Front Syst Neurosci. 8:253.

Oliveira da Cruz JF, Robin LM, Drago F, Marsicano G, Metna-Laurent M., Astroglial type-1 cannabinoid receptor (CB1): A new player in the tripartite synapse.  Neuroscience. 2015 May 9. pii: S0306-4522(15)00434-0. [WP1]

Lutz B, Marsicano G, Maldonado R, Hillard CJ. The endocannabinoid system in guarding against fear, anxiety and stress. Nat Rev Neurosci. 2015; 16:705-718.

Bitencourt RM, Alpár A, Cinquina V, Ferreira SG, Pinheiro BS, Lemos C, Ledent C, Takahashi RN, Sialana FJ, Lubec G, Cunha RA, Harkany T, Köfalvi A. Lack of presynaptic interaction between glucocorticoid and CB1 cannabinoid receptors in GABA- and glutamatergic terminals in the frontal cortex of laboratory rodents. Neurochem Int. (2015) doi: 10.1016/j.neuint.2015.07.014.

Penz OK, Fuzik J, Kurek AB, Romanov R, Larson J, Park TJ, Harkany T, Keimpema E. Protracted brain development in a rodent model of extreme longevity. Sci Rep. (2015) 5:11592. doi: 10.1038/srep11592. OPEN

Richner M, Ulrichsen M, Elmegaard SL, Dieu R, Pallesen LT, Vaegter CB, Peripheral nerve injury modulates neurotrophin signaling in the peripheral and central nervous system, Mol Neurobiol. 2014 Dec;50(3):945-70. [WP1]

Lewin GR and Nykjaer A., Pro-neurotrophins, sortilin, and nociception,  Eur J Neurosci. 2014 Feb;39(3):363-74 [WP1]

Romanov RA, Alpár A, Zhang MD, Zeisel A, Calas A, Landry M, Fuszard M, Shirran SL, Schnell R, Dobolyi A, Oláh M, Spence L, Mulder J, Martens H, Palkovits M, Uhlen M, Sitte HH, Botting CH, Wagner L, Linnarsson S, Hökfelt T, Harkany T. A secretagogin locus of the mammalian hypothalamus controls stress hormone release, EMBO J. 2014 Nov 27. pii: e201488977. Press release related to this publication: http://www.meduniwien.ac.at/homepage/1/news-and-topstories/?tx_ttnews%5Btt_news%5D=5302&cHash=217cf5c503a66cf6434b2cf627c08280 and http://ki.se/en/news/secretagogin-triggers-stress-process-in-the-brain

Maccarrone M, Guzmán M, Mackie K, Doherty P, Harkany T. Programming of neural cells by (endo)cannabinoids: from physiological rules to emerging therapies. Nat Rev Neurosci. (2014) 15:786-801.

Zhang MD, Tortoriello G, Hsueh B, Tomer R, Ye L, Mitsios N, Borgius L, Grant G, Kiehn O, Watanabe M, Uhlén M, Mulder J, Deisseroth K, Harkany T* and Hökfelt TGM*. Neuronal calcium-binding proteins 1/2 localize to dorsal root ganglia and excitatory spinal neurons and are regulated by nerve injury. Proc Natl Acad Sci USA (2014) 111:1149-1158.

Keimpema E, Hökfelt T, Harkany T and Doherty P. The molecular interplay between endocannabinoid and neurotrophin signals in the nervous system and beyond, Eur J Neurosci (2014) 39:334-343.

Harkany T, Zeilhofer HU, Cattaneo A. Neurotrophin and endocannabinoid interactions in the neurobiology of pain (editorial), Eur J Neurosci (2014) 39:331-333.

Capsoni S. From genes to pain: nerve growth factor and hereditary sensory and autonomic neuropathy type,V. Eur J Neurosci. 2014 Feb;39(3):392-400.

The above references that had appeared in the European Journal of Neuroscience are part of a “Special Issue” whose concept and editorial work were performed by T. Harkany and A. Cattaneo, as part of the PAINCAGE consortium’s pledge to disseminate contemporary concepts on endocannabinoid and/or neurotrophin signaling in sensory neurons and ascending spinal networks.

*Yu, T., *Calvo, L., Anta, B., López-Benito, S., López-Bellido, R., Vicente-Garcia, C., Tessarollo, L., Rodríguez, R.E. and Arévalo, J.C. 2014. In vivo regulation of NGF-mediated functions by Nedd4-2 ubiquitination of TrkA. J. Neurosci. 34: 6098-6106. *Equal contribution