A Small Linear Peptide Encompassing the NGF N-Terminus Partly Mimics the Biological Activities of the Entire Neurotrophin in PC12 Cells(337 views) Travaglia A, Pietropaolo A, Di Martino R, Nicoletti VG, La Mendola D, Calissano P, Rizzarelli E
Center for Neural Science, New York University, 4 Washington Place, New York, NY, United States
Dipartimento di Scienze della Salute, Università di Catanzaro, Viale Europa, Catanzaro, Italy
Istituto di Bioimmagini e Fisiologia Molecolare (IBFM)-CNR, C.da Pietrapollastra-Pisciotto, Cefalù, Palermo, Italy
Istituto Nazionale Biostrutture e Biosistemi (INBB) - Sezione Biomolecole, Consorzio Interuniversitario, Viale Medaglie d'Oro 305, Roma, Italy
Department of Pharmacy, University of Pisa, Via Bonanno Pisano 6, Pisa, Italy
European Brain Research Institute (EBRI), Via del Fosso di Fiorano, 64-65, Rome, Italy
IBB-CNR, UOS Catania, via Paolo Gaifami 18, Catania, Italy
References: Huang, E.J., Reichardt, L.F., Neurotrophins: Roles in neuronal development and function (2001) Annu. Rev. Neurosci., 24, pp. 677-73
Chao, M.V., Neurotrophins and their receptors: A convergence point for many signalling pathways (2003) Nat. Rev. Neurosci, 4, pp. 299-309
Caporali, A., Emanueli, C., Cardiovascular actions of neurotrophins (2009) Physiol Rev., 89, pp. 279-308
Dechant, G., Barde, Y.A., The neurotrophin receptor p75(NTR): Novel functions and implications for diseases of the nervous system (2002) Nat. Neurosci., 5, pp. 1131-1136
Levi-Montalcini, R., Hamburger, V., Selective growth stimulating effects of mouse sarcoma on the sensory and sympathetic nervous system of the chick embryo (1951) J. Exp. Zool., 116, pp. 321-361
Cohen, S., Levi-Montalcini, R., Hamburger, V., A Nerve Growth-Stimulating Factor Isolated from Sarcom as 37 and 180 (1954) Proc. Natl. Acad. Sci. U. S. A., 40, pp. 1014-1018
Sobue, G., Yamamoto, M., Doyu, M., Li, M., Yasuda, T., Mitsuma, T., Expression of mRNAs for neurotrophins (NGF, BDNF, and NT-3) and their receptors (p75NGFR, trk, trkB, and trkC) in human peripheral neuropathies (1998) Neurochem. Res., 23, pp. 821-829
Allen, S.J., Dawbarn, D., Clinical relevance of the neurotrophins and their receptors (2006) Clin Sci., 110, pp. 175-191
Chao, M.V., Rajagopal, R., Lee, F.S., Neurotrophin signalling in health and disease (2006) Clin Sci., 110, pp. 167-173
Weissmiller, A.M., Wu, C., Current advances in using neurotrophic factors to treat neurodegenerative disorders (2012) Transl. Neurodegener., 1, p. 14
Wilson, R.M., Danishefsky, S.J., Applications of total synthesis to problems in neurodegeneration: Fascinating chemistry along the way (2006) Acc. Chem. Res., 39, pp. 539-549
Fahnestock, M., Michalski, B., Xu, B., Coughlin, M.D., The precursor pro-nerve growth factor is the predominant form of nerve growth factor in brain and is increased in Alzheimer's disease (2001) Mol. Cell. Neurosci., 18, pp. 210-220
Mufson, E.J., He, B., Nadeem, M., Perez, S.E., Counts, S.E., Leurgans, S., Fritz, J., Scheff, S.W., Hippocampal proNGF signaling pathways and beta-amyloid levels in mild cognitive impairment and Alzheimer disease (2012) J. Neuropathol. Exp. Neurol., 71, pp. 1018-1029
Dyck, P.J., Peroutka, S., Rask, C., Burton, E., Baker, M.K., Lehman, K.A., Gillen, D.A., O'Brien, P.C., Intradermal recombinant human nerve growth factor induces pressure allodynia and lowered heat-pain threshold in humans (1997) Neurology, 48, pp. 501-505
Bergmann, I., Reiter, R., Toyka, K.V., Koltzenburg, M., Nerve growth factor evokes hyperalgesia in mice lacking the low-affinity neurotrophin receptor p75 (1998) Neurosci. Lett., 255, pp. 87-90
Bai, Y., Xu, J., Brahimi, F., Zhuo, Y., Sarunic, M.V., Saragovi, H.U., An agonistic TrkB mAb causes sustained TrkB activation, delays RGC death, and protects the retinal structure in optic nerve axotomy and in glaucoma (2010) Invest. Ophthalmol. Visual Sci., 51, pp. 4722-4731
Guillemard, V., Ivanisevic, L., Garcia, A.G., Scholten, V., Lazo, O.M., Bronfman, F.C., Saragovi, H.U., An agonistic mAb directed to the TrkC receptor juxtamembrane region defines a trophic hot spot and interactions with p75 coreceptors (2010) Dev. Neurobiol., 70, pp. 150-164
Ugolini, G., Marinelli, S., Covaceuszach, S., Cattaneo, A., Pavone, F., The function neutralizing anti-TrkA antibody MNAC13 reduces inflammatory and neuropathic pain (2007) Proc. Natl. Acad. Sci. U. S. A., 104, pp. 2985-2990
Sahenk, Z., Galloway, G., Edwards, C., Malik, V., Kaspar, B.K., Eagle, A., Yetter, B., Lin, J.C., TrkB and TrkC agonist antibodies improve function, electrophysiologic and pathologic features in Trembler J mice (2010) Exp. Neurol., 224, pp. 495-506
Blesch, A., Uy, H.S., Diergardt, N., Tuszynski, M.H., Neurite outgrowth can be modulated in vitro using a tetracycline-repressible gene therapy vector expressing human nerve growth factor (2000) J. Neurosci. Res., 59, pp. 402-409
Taylor, L., Jones, L., Tuszynski, M.H., Blesch, A., Neurotrophin-3 gradients established by lentiviral gene delivery promote short-distance axonal bridging beyond cellular grafts in the injured spinal cord (2006) J. Neurosci., 26, pp. 9713-9721
Nagahara, A.H., Merrill, D.A., Coppola, G., Tsukada, S., Schroeder, B.E., Shaked, G.M., Wang, L., Tuszynski, M.H., Neuroprotective effects of brain-derived neurotrophic factor in rodent and primate models of Alzheimer's disease (2009) Nat. Med., 15, pp. 331-337
Chattopadhyay, M., Wolfe, D., Mata, M., Huang, S., Glorioso, J.C., Fink, D.J., Long-term neuroprotection achieved with latency-associated promoter-driven herpes simplex virus gene transfer to the peripheral nervous system (2005) Mol. Ther., 12, pp. 307-313
Travaglia, A., Satriano, C., Giuffrida, M.L., La Mendola, D., Rampazzo, E., Prodi, L., Rizzarelli, E., Electrostatically driven interaction of silica-supported lipid bilayer nanoplatforms and a nerve growth factor-mimicking peptide (2013) Soft Matter, 9, pp. 4648-4654
Capsoni, S., Covaceuszach, S., Marinelli, S., Ceci, M., Bernardo, A., Minghetti, L., Ugolini, G., Cattaneo, A., Taking pain out of NGF: A "painless" NGF mutant, linked to hereditary sensory autonomic neuropathy type V, with full neurotrophic activity (2011) PLoS One, 6, p. 17321
Longo, F.M., Massa, S.M., Small-molecule modulation of neurotrophin receptors: A strategy for the treatment of neurological disease (2013) Nat. Rev. Drug Discovery, 12, pp. 507-525
Liskamp, R.M., Rijkers, D.T., Kruijtzer, J.A., Kemmink, J., Peptides and proteins as a continuing exciting source of inspiration for peptidomimetics (2011) ChemBioChem, 12, pp. 1626-1653
Wiesmann, C., Ultsch, M.H., Bass, S.H., De Vos, A.M., Crystal structure of nerve growth factor in complex with the ligand-binding domain of the TrkA receptor (1999) Nature, 401, pp. 184-188
Wehrman, T., He, X., Raab, B., Dukipatti, A., Blau, H., Garcia, K.C., Structural and mechanistic insights into nerve growth factor interactions with the TrkA and p75 receptors (2007) Neuron, 53, pp. 25-38
Banfield, M.J., Naylor, R.L., Robertson, A.G., Allen, S.J., Dawbarn, D., Brady, R.L., Specificity in Trk receptor:neurotrophin interactions: The crystal structure of TrkB-d5 in complex with neurotrophin-4/5 (2001) Structure, 9, pp. 1191-1199
Ibanez, C.F., Emerging themes in structural biology of neurotrophic factors (1998) Trends Neurosci., 21, pp. 438-444
Arevalo, J.C., Conde, B., Hempstead, B.L., Chao, M.V., Martin-Zanca, D., Perez, P., TrkA immunoglobulin-like ligand binding domains inhibit spontaneous activation of the receptor (2000) Mol. Cell. Biol., 20, pp. 5908-5916
Shen, J., Maruyama, I.N., Nerve growth factor receptor TrkA exists as a preformed, yet inactive, dimer in living cells (2011) FEBS Lett., 585, pp. 295-299
Longo, F.M., Vu, T.K., Mobley, W.C., The in vitro biological effect of nerve growth factor is inhibited by synthetic peptides (1990) Cell Regul., 1, pp. 189-195
Lesauteur, L., Wei, L., Gibbs, B.F., Saragovi, H.U., Small peptide mimics of nerve growth factor bind TrkA receptors and affect biological responses (1995) J. Biol. Chem., 270, pp. 6564-6569
Maliartchouk, S., Debeir, T., Beglova, N., Cuello, A.C., Gehring, K., Saragovi, H.U., Genuine monovalent ligands of TrkA nerve growth factor receptors reveal a novel pharmacological mechanism of action (2000) J. Biol. Chem., 275, pp. 9946-9956
Xie, Y., Tisi, M.A., Yeo, T.T., Longo, F.M., Nerve growth factor (NGF) loop 4 dimeric mimetics activate ERK and AKT and promote NGF-like neurotrophic effects (2000) J. Biol. Chem., 275, pp. 29868-29874
Colangelo, A.M., Bianco, M.R., Vitagliano, L., Cavaliere, C., Cirillo, G., De Gioia, L., Diana, D., Martegani, E., A new nerve growth factor-mimetic peptide active on neuropathic pain in rats (2008) J. Neurosci., 28, pp. 2698-2709
Maliartchouk, S., Feng, Y., Ivanisevic, L., Debeir, T., Cuello, A.C., Burgess, K., Saragovi, H.U., A designed peptidomimetic agonistic ligand of TrkA nerve growth factor receptors (2000) Mol. Pharmacol., 57, pp. 385-391
Scarpi, D., Cirelli, D., Matrone, C., Castronovo, G., Rosini, P., Occhiato, E.G., Romano, F., Cozzolino, F., Low molecular weight, non-peptidic agonists of TrkA receptor with NGF-mimetic activity (2012) Cell Death Dis., 3, p. 389
Lin, B., Pirrung, M.C., Deng, L., Li, Z., Liu, Y., Webster, N.J., Neuroprotection by small molecule activators of the nerve growth factor receptor (2007) J. Pharmacol. Exp. Ther., 322, pp. 59-69
Jang, S.W., Okada, M., Sayeed, I., Xiao, G., Stein, D., Jin, P., Ye, K., Gambogic amide, a selective agonist for TrkA receptor that possesses robust neurotrophic activity, prevents neuronal cell death (2007) Proc. Natl. Acad. Sci. U. S. A., 104, pp. 16329-16334
Jang, S.W., Liu, X., Chan, C.B., Weinshenker, D., Hall, R.A., Xiao, G., Ye, K., Amitriptyline is a TrkA and TrkB receptor agonist that promotes TrkA/TrkB heterodimerization and has potent neurotrophic activity (2009) Chem. Biol., 16, pp. 644-656
Shih, A., Laramee, G.R., Schmelzer, C.H., Burton, L.E., Winslow, J.W., Mutagenesis identifies amino-terminal residues of nerve growth factor necessary for Trk receptor binding and biological activity (1994) J. Biol. Chem., 269, pp. 27679-27686
Kahle, P., Burton, L.E., Schmelzer, C.H., Hertel, C., The amino terminus of nerve growth factor is involved in the interaction with the receptor tyrosine kinase p140trkA (1992) J. Biol. Chem., 267, pp. 22707-22710
Woo, S.B., Timm, D.E., Neet, K.E., Alteration of NH2-terminal residues of nerve growth factor affects activity and Trk binding without affecting stability or conformation (1995) J. Biol. Chem., 270, pp. 6278-6285
Berrera, M., Cattaneo, A., Carloni, P., Molecular simulation of the binding of nerve growth factor peptide mimics to the receptor tyrosine kinase a (2006) Biophys. J., 91, pp. 2063-2071
Travaglia, A., Arena, G., Fattorusso, R., Isernia, C., La Mendola, D., Malgieri, G., Nicoletti, V.G., Rizzarelli, E., The inorganic perspective of nerve growth factor: Interactions of Cu2+ and Zn2+ with the N-terminus fragment of nerve growth factor encompassing the recognition domain of the TrkA receptor (2011) Chemistry, 17, pp. 3726-3738
Beglova, N., Maliartchouk, S., Ekiel, I., Zaccaro, M.C., Saragovi, H.U., Gehring, K., Design and solution structure of functional peptide mimetics of nerve growth factor (2000) J. Med. Chem., 43, pp. 3530-3540
Yao, R., Cooper, G.M., Requirement for phosphatidylinositol-3 kinase in the prevention of apoptosis by nerve growth factor (1995) Science, 267, pp. 2003-2006
Zhang, Y., Moheban, D.B., Conway, B.R., Bhattacharyya, A., Segal, R.A., Cell surface Trk receptors mediate NGF-induced survival while internalized receptors regulate NGF-induced differentiation (2000) J. Neurosci., 20, pp. 5671-5678
Cantley, L.C., The phosphoinositide 3-kinase pathway (2002) Science, 296, pp. 1655-1657
Crowder, R.J., Freeman, R.S., Phosphatidylinositol 3-kinase and Akt protein kinase are necessary and sufficient for the survival of nerve growth factor-dependent sympathetic neurons (1998) J. Neurosci., 18, pp. 2933-2943
Dudek, H., Datta, S.R., Franke, T.F., Birnbaum, M.J., Yao, R., Cooper, G.M., Segal, R.A., Greenberg, M.E., Regulation of neuronal survival by the serine-threonine protein kinase Akt (1997) Science, 275, pp. 661-665
Bartlett, S.E., Reynolds, A.J., Weible, M., Heydon, K., Hendry, I.A., In sympathetic but not sensory neurones, phosphoinositide-3 kinase is important for NGF-dependent survival and the retrograde transport of 125I-betaNGF (1997) Brain Res., 761, pp. 257-262
Kaidanovich-Beilin, O., Woodgett, J.R., GSK-3: Functional Insights from Cell Biology and Animal Models (2011) Front. Mol. Neurosci., 4, p. 40
Cross, D.A., Alessi, D.R., Cohen, P., Andjelkovich, M., Hemmings, B.A., Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B (1995) Nature, 378, pp. 785-789
Dajani, R., Fraser, E., Roe, S.M., Young, N., Good, V., Dale, T.C., Pearl, L.H., Crystal structure of glycogen synthase kinase 3 beta: Structural basis for phosphate-primed substrate specificity and autoinhibition (2001) Cell, 105, pp. 721-732
Wang, X., Proud, C.G., The mTOR pathway in the control of protein synthesis (2006) Physiology, 21, pp. 362-369
Pap, M., Cooper, G.M., Role of glycogen synthase kinase-3 in the phosphatidylinositol 3-Kinase/Akt cell survival pathway (1998) J. Biol. Chem., 273, pp. 19929-19932
Hetman, M., Cavanaugh, J.E., Kimelman, D., Xia, Z., Role of glycogen synthase kinase-3beta in neuronal apoptosis induced by trophic withdrawal (2000) J. Neurosci., 20, pp. 2567-2574
Cowley, S., Paterson, H., Kemp, P., Marshall, C.J., Activation of MAP kinase kinase is necessary and sufficient for PC12 differentiation and for transformation of NIH 3T3 cells (1994) Cell, 77, pp. 841-852
Qui, M.S., Green, S.H., PC12 cell neuronal differentiation is associated with prolonged p21ras activity and consequent prolonged ERK activity (1992) Neuron, 9, pp. 705-717
Finkbeiner, S., Tavazoie, S.F., Maloratsky, A., Jacobs, K.M., Harris, K.M., Greenberg, M.E., CREB: A major mediator of neuronal neurotrophin responses (1997) Neuron, 19, pp. 1031-1047
Teng, F.Y., Tang, B.L., Axonal regeneration in adult CNS neurons - Signaling molecules and pathways (2006) J. Neurochem., 96, pp. 1501-1508
Kim, J., Kwon, J.T., Kim, H.S., Han, J.H., CREB and neuronal selection for memory trace (2013) Front. Neural Circuits, 7, p. 44
Alberini, C.M., Transcription factors in long-term memory and synaptic plasticity (2009) Physiol. Rev., 89, pp. 121-145
Bisaz, R., Travaglia, A., Alberini, C.M., The neurobiological bases of memory formation: From physiological conditions to psychopathology (2014) Psychopathology, 47, pp. 347-356
Leone, V., D'Angelo, D., Ferraro, A., Pallante, P., Rubio, I., Santoro, M., Croce, C.M., Fusco, A., A TSH-CREB1-microRNA loop is required for thyroid cell growth (2011) Mol. Endocrinol., 25, pp. 1819-1830
Saragovi, H.U., Greene, M.I., Chrusciel, R.A., Kahn, M., Loops and secondary structure mimetics: Development and applications in basic science and rational drug design (1992) Biotechnology, 10, pp. 773-778
Saragovi, H.U., Zaccaro, M.C., Small molecule peptidomimetic ligands of neurotrophin receptors, identifying binding sites, activation sites and regulatory sites (2002) Curr. Pharm. Des., 8, pp. 2201-2216
Pollack, S.J., Harper, S.J., Small molecule Trk receptor agonists and other neurotrophic factor mimetics (2002) Curr. Drug Targets: CNS Neurol. Disord., 1, pp. 59-80
Massa, S.M., Xie, Y., Longo, F.M., Alzheimer's therapeutics: Neurotrophin domain small molecule mimetics (2003) J. Mol. Neurosci, 20, pp. 323-326
Zaccaro, M.C., Lee, H.B., Pattarawarapan, M., Xia, Z., Caron, A., L'Heureux, P.J., Bengio, Y., Saragovi, H.U., Selective small molecule peptidomimetic ligands of TrkC and TrkA receptors afford discrete or complete neurotrophic activities (2005) Chem. Biol., 12, pp. 1015-1028
Bradshaw, R.A., Murray-Rust, J., Ibanez, C.F., McDonald, N.Q., Lapatto, R., Blundell, T.L., Nerve growth factor: Structure/function relationships (1994) Protein Sci., 3, pp. 1901-1913
McDonald, N.Q., Chao, M.V., Structural determinants of neurotrophin action (1995) J. Biol. Chem., 270, pp. 19669-19672
Holland, D.R., Cousens, L.S., Meng, W., Matthews, B.W., Nerve growth factor in different crystal forms displays structural flexibility and reveals zinc binding sites (1994) J. Mol. Biol., 239, pp. 385-400
Ibanez, C.F., Ebendal, T., Barbany, G., Murray-Rust, J., Blundell, T.L., Persson, H., Disruption of the low affinity receptor-binding site in NGF allows neuronal survival and differentiation by binding to the trk gene product (1992) Cell, 69, pp. 329-341
Kruttgen, A., Heymach, J.V., Jr., Kahle, P.J., Shooter, E.M., The role of the nerve growth factor carboxyl terminus in receptor binding and conformational stability (1997) J. Biol. Chem., 272, pp. 29222-29228
Kullander, K., Kaplan, D., Ebendal, T., Two restricted sites on the surface of the nerve growth factor molecule independently determine specific TrkA receptor binding and activation (1997) J. Biol. Chem., 272, pp. 9300-9307
Drinkwater, C.C., Barker, P.A., Suter, U., Shooter, E.M., The carboxyl terminus of nerve growth factor is required for biological activity (1993) J. Biol. Chem., 268, pp. 23202-23207
Mobley, W.C., Schenker, A., Shooter, E.M., Characterization and isolation of proteolytically modified nerve growth factor (1976) Biochemistry, 15, pp. 5543-5552
Kortemme, T., Baker, D., A simple physical model for binding energy hot spots in protein-protein complexes (2002) Proc. Natl. Acad. Sci. U. S. A., 99, pp. 14116-14121
Kortemme, T., Kim, D.E., Baker, D., Computational alanine scanning of protein-protein interfaces (2004) Sci. STKE, 2004, p. 2
Zaccaro, M.C., Ivanisevic, L., Perez, P., Meakin, S.O., Saragovi, H.U., P75 Co-receptors regulate ligand-dependent and ligand-independent Trk receptor activation, in part by altering Trk docking subdomains (2001) J. Biol. Chem., 276, pp. 31023-31029
Coulier, F., Kumar, R., Ernst, M., Klein, R., Martin-Zanca, D., Barbacid, M., Human trk oncogenes activated by point mutation, in-frame deletion, and duplication of the tyrosine kinase domain (1990) Mol. Cell. Biol., 10, pp. 4202-4210
Jones, S., Thornton, J.M., Principles of protein-protein interactions (1996) Proc. Natl. Acad. Sci. U. S. A., 93, pp. 13-20
Bogan, A.A., Thorn, K.S., Anatomy of hot spots in protein interfaces (1998) J. Mol. Biol., 280, pp. 1-9
Heldin, C.H., Dimerization of cell surface receptors in signal transduction (1995) Cell, 80, pp. 213-223
Settanni, G., Cattaneo, A., Carloni, P., Molecular dynamics simulations of the NGF-TrkA domain 5 complex and comparison with biological data (2003) Biophys. J., 84, pp. 2282-2292
Stanzione, F., Esposito, L., Paladino, A., Pedone, C., Morelli, G., Vitagliano, L., Role of the conformational versatility of the neurotrophin N-terminal regions in their recognition by Trk receptors (2010) Biophys. J., 99, pp. 2273-2278
Marchetti, L., Callegari, A., Luin, S., Signore, G., Viegi, A., Beltram, F., Cattaneo, A., Ligand signature in the membrane dynamics of single TrkA receptor molecules (2013) J. Cell Sci., 126, pp. 4445-4456
Matusica, D., Coulson, E.J., Local versus long-range neurotrophin receptor signalling: Endosomes are not just carriers for axonal transport (2014) Semin. Cell Dev. Biol., 31, pp. 57-63
Xing, J., Kornhauser, J.M., Xia, Z., Thiele, E.A., Greenberg, M.E., Nerve growth factor activates extracellular signal-regulated kinase and p38 mitogen-activated protein kinase pathways to stimulate CREB serine 133 phosphorylation (1998) Mol. Cell. Biol., 18, pp. 1946-1955
Lonze, B.E., Riccio, A., Cohen, S., Ginty, D.D., Apoptosis, axonal growth defects, and degeneration of peripheral neurons in mice lacking CREB (2002) Neuron, 34, pp. 371-385
Forte, G., Travaglia, A., Magri, A., Satriano, C., La Mendola, D., Adsorption of NGF and BDNF derived peptides on gold surfaces (2014) Phys. Chem. Chem. Phys., 16, pp. 1536-1544
Hess, B., Kutzner, C., Van Der Spoel, D., Lindahl, E., GROMACS 4: Algorithms for highly efficient, load-balanced, and scalable molecular simulation (2008) J. Chem. Theory Comput., 4, pp. 435-447
Hornak, V., Abel, R., Okur, A., Strockbine, B., Roitberg, A., Simmerling, C., Comparison of multiple amber force fields and development of improved protein backbone parameters (2006) Proteins, 65, pp. 712-725
Jorgensen, W.L., Chandrasekhar, J., Madura, J.D., Impey, R.W., Klein, M.L., Comparison of Simple Potential Functions for Simulating Liquid Water (1983) J. Chem. Phys., 79, pp. 926-935
Essmann, U., Perera, L., Berkowitz, M.L., Darden, T., Lee, H., Pedersen, L.G., A Smooth Particle Mesh Ewald Method (1995) J. Chem. Phys., 103, pp. 8577-8593
Miyamoto, S., Kollman, P.A., Settle - An Analytical Version of the Shake and Rattle Algorithm for Rigid Water Models (1992) J. Comput. Chem., 13, pp. 952-962
Hess, B., P-LINCS: A parallel linear constraint solver for molecular simulation (2008) J. Chem. Theory Comput., 4, pp. 116-122
Bussi, G., Donadio, D., Parrinello, M., Canonical sampling through velocity rescaling (2007) J. Chem. Phys., 126
Rosta, E., Buchete, N.V., Hummer, G., Thermostat Artifacts in Replica Exchange Molecular Dynamics Simulations (2009) J. Chem. Theory Comput., 5, pp. 1393-1399
Daura, X., Gademann, K., Jaun, B., Seebach, D., Van Gunsteren, W.F., Mark, A.E., Peptide folding: When simulation meets experiment (1999) Angew. Chem., Int. Ed., 38, pp. 236-240
Han, B., Liu, Y., Ginzinger, S., Wishart, D., SHIFTX2: Significantly improved protein chemical shift prediction (2011) J. Biomol. NMR, 50, pp. 43-57
De Vries, S.J., Van Dijk, M., Bonvin, A.M.J.J., The HADDOCK web server for data-driven biomolecular docking (2010) Nat. Protoc., 5, pp. 883-897
Volonte, C., Ciotti, M.T., Battistini, L., Development of a method for measuring cell number: Application to CNS primary neuronal cultures (1994) Cytometry, 17, pp. 274-276
A Small Linear Peptide Encompassing the NGF N-Terminus Partly Mimics the Biological Activities of the Entire Neurotrophin in PC12 Cells