Modulation of Differentiation of Embryonic Stem Cells by Polypyrrole: The Impact on Neurogenesis
Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
19-16861S
Czech Science Foundation
17-05466S
Czech Science Foundation
IGA/CPS/2020/001
Internal grant agency of Tomas Bata University in Zlín
PubMed
33419082
PubMed Central
PMC7825406
DOI
10.3390/ijms22020501
PII: ijms22020501
Knihovny.cz E-zdroje
- Klíčová slova
- biocompatibility, conducting polymer, neurogenesis, polypyrrole, stem cells,
- MeSH
- buněčná diferenciace účinky léků genetika MeSH
- buněčné linie MeSH
- embryoidní tělíska cytologie účinky léků MeSH
- exprese genu účinky léků MeSH
- molekulární struktura MeSH
- myší embryonální kmenové buňky cytologie účinky léků metabolismus MeSH
- myši MeSH
- nervové kmenové buňky cytologie účinky léků metabolismus MeSH
- neurogeneze účinky léků genetika MeSH
- polymerázová řetězová reakce s reverzní transkripcí MeSH
- polymery chemie farmakologie MeSH
- pyrroly chemie farmakologie MeSH
- transkripční faktor PAX6 genetika MeSH
- transkripční faktory bHLH genetika MeSH
- transkripční faktory SOXB1 genetika MeSH
- zvířata MeSH
- Check Tag
- myši MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- Ascl1 protein, mouse MeSH Prohlížeč
- polymery MeSH
- polypyrrole MeSH Prohlížeč
- pyrroly MeSH
- transkripční faktor PAX6 MeSH
- transkripční faktory bHLH MeSH
- transkripční faktory SOXB1 MeSH
The active role of biomaterials in the regeneration of tissues and their ability to modulate the behavior of stem cells in terms of their differentiation is highly advantageous. Here, polypyrrole, as a representantive of electro-conducting materials, is found to modulate the behavior of embryonic stem cells. Concretely, the aqueous extracts of polypyrrole induce neurogenesis within embryonic bodies formed from embryonic stem cells. This finding ledto an effort to determine the physiological cascade which is responsible for this effect. The polypyrrole modulates signaling pathways of Akt and ERK kinase through their phosphorylation. These effects are related to the presence of low-molecular-weight compounds present in aqueous polypyrrole extracts, determined by mass spectroscopy. The results show that consequences related to the modulation of stem cell differentiation must also be taken into account when polypyrrole is considered as a biomaterial.
Centre of Polymer Systems Tomas Bata University in Zlín 760 01 Zlín Czech Republic
Department of Experimental Biology Faculty of Science Masaryk University 625 00 Brno Czech Republic
Department of Surface Engineering Jožef Stefan Institute Jamova cesta 39 SI 1000 Ljubljana Slovenia
Faculty of Technology Tomas Bata University in Zlín 760 01 Zlín Czech Republic
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Ateh D., Navsaria H., Vadgama P. Polypyrrole-based conducting polymers and interactions with biological tissues. J. R. Soc. Interface. 2006;3:741–752. doi: 10.1098/rsif.2006.0141. PubMed DOI PMC
Kim S.Y., Kim K.-M., Hoffman-Kim D., Song H.-K., Palmore G.T.R. Quantitative Control of Neuron Adhesion at a Neural Interface Using a Conducting Polymer Composite with Low Electrical Impedance. ACS Appl. Mater. Interfaces. 2011;3:16–21. doi: 10.1021/am1008369. PubMed DOI
Gomez N., Schmidt C.E. Nerve growth factor-immobilized polypyrrole: Bioactive electrically conducting polymer for en-hanced neurite extension. J. Biomed. Mater. Res. Part A. 2007;81:135–149. doi: 10.1002/jbm.a.31047. PubMed DOI PMC
Mittnacht U., Hartmann H., Hein S., Oliveira H., Dong M., Pêgo A.P., Kjems J., Howard K.A., Schlosshauer B. Chitosan/siRNA Nanoparticles Biofunctionalize Nerve Implants and Enable Neurite Outgrowth. Nano Lett. 2010;10:3933–3939. doi: 10.1021/nl1016909. PubMed DOI
Yamada M., Tanemura K., Okada S., Iwanami A., Nakamura M., Mizuno H., Ozawa M., Ohyama-Goto R., Kitamura N., Kawano M., et al. Electrical Stimulation Modulates Fate Determination of Differentiating Embryonic Stem Cells. Stem Cells. 2006;25:562–570. doi: 10.1634/stemcells.2006-0011. PubMed DOI
Fonner J.M., Forciniti L., Nguyen H., Byrne J.D., Kou Y.F., Syeda-Nawaz J., Schmidt C.E. Biocompatibility implications of polypyrrole synthesis techniques. Biomed. Mater. 2008;3:034124. doi: 10.1088/1748-6041/3/3/034124. PubMed DOI PMC
Vernitskaya T.V., Efimov O.N. Polypyrrole: A conducting polymer; its synthesis, properties and applications. Russ. Chem. Rev. 1997;66:443–457. doi: 10.1070/RC1997v066n05ABEH000261. DOI
Castano H., O’Rear E.A., McFetridge P.S., Sikavitsas V.I. Polypyrrole Thin Films Formed by Admicellar Polymeriza-tion Support the Osteogenic Differentiation of Mesenchymal Stem Cells. Macromol. Biosci. 2004;4:785–794. doi: 10.1002/mabi.200300123. PubMed DOI
Omastová M., Trchová M., Kovářová J., Stejskal J. Synthesis and structural study of polypyrroles prepared in the presence of surfactants. Synth. Met. 2003;138:447–455. doi: 10.1016/S0379-6779(02)00498-8. DOI
Stejskal J., Trchová M., Bober P., Morávková Z., Kopecký D., Vrňata M., Prokeš J., Varga M., Watzlová E. Polypyrrole salts and bases: Superior conductivity of nanotubes and their stability towards the loss of conductivity by depro-tonation. RSC Adv. 2016;6:88382–88391. doi: 10.1039/C6RA19461C. DOI
Lee J.-W., Serna F., Nickels A.J., Schmidt C.E. Carboxylic Acid-Functionalized Conductive Polypyrrole as a Bioactive Platform for Cell Adhesion. Biomacromolecules. 2006;7:1692–1695. doi: 10.1021/bm060220q. PubMed DOI PMC
Gilmore K.J., Kita M., Han Y., Gelmi A., Higgins M.J., Moulton S.E., Clark G.M., Kapsa R., Wallace G.G. Skeletal muscle cell proliferation and differentiation on polypyrrole substrates doped with extracellular matrix components. Biomaterials. 2009;30:5292–5304. doi: 10.1016/j.biomaterials.2009.06.059. PubMed DOI
Richardson R.T., Thompson B., Moulton S.E., Newbold C., Lum M.G., Cameron A., Wallace G.G., Kapsa R., Clark G., O’Leary S. The effect of polypyrrole with incorporated neurotrophin-3 on the promotion of neurite outgrowth from auditory neurons. Biomaterials. 2007;28:513–523. doi: 10.1016/j.biomaterials.2006.09.008. PubMed DOI
Milakin K.A., Capáková Z., Acharya U., Vajďák J., Morávková Z., Hodan J., Humpolíček P., Bober P. Bio-compatible and antibacterial gelatin-based polypyrrole cryogels. Polymer. 2020;197:122491. doi: 10.1016/j.polymer.2020.122491. DOI
Kang S.Y., Park E.J., Park W.K., Kim H.J., Jeong D., Jung M.E., Song K.S., Lee S.H., Seo H.J., Kim M.J., et al. Arylpiperazine-containing pyrrole 3-carboxamide derivatives targeting serotonin 5-HT2A, 5-HT2C, and the serotonin transporter as a potential antidepressant. Bioorganic Med. Chem. Lett. 2010;20:1705–1711. doi: 10.1016/j.bmcl.2010.01.093. PubMed DOI
Bavadi M., Niknam K., Shahraki O. Novel pyrrole derivatives bearing sulfonamide groups: Synthesis in vitro cytotoxicity evaluation, molecular docking and DFT study. J. Mol. Struct. 2017;1146:242–253. doi: 10.1016/j.molstruc.2017.06.003. DOI
Aiello A., D’Esposito M., Fattorusso E., Menna M., Müller W.E.G., Perović-Ottstadt S., Tsuruta H., Gulder T.A.M., Bringmann G. Daminin, a bioactive pyrrole alkaloid from the Mediterranean sponge Axinella damicornis. Tetrahedron. 2005;61:7266–7270. doi: 10.1016/j.tet.2005.05.025. DOI
Ahmad S., Alam O., Naim M.J., Shaquiquzzaman M., Alam M.M., Iqbal M. Pyrrole: An insight into recent pharmacological advances with structure activity relationship. Eur. J. Med. Chem. 2018;157:527–561. doi: 10.1016/j.ejmech.2018.08.002. PubMed DOI
Humpolíček P., Kašpárková V., Pacherník J., Stejskal J., Bober P., Capáková Z., Radaszkiewicz K.A., Junkar I., Lehocký M. The biocompatibility of polyaniline and polypyrrole: A comparative study of their cytotoxicity, em-bryotoxicity and impurity profile. Mater. Sci. Eng. C. 2018;91:303–310. doi: 10.1016/j.msec.2018.05.037. PubMed DOI
Nagy A., Rossant J., Abramow-Newerly W., Roder J.C. Derivation of completely cell culture-derived mice from early-passage embryonic stem cells. Proc. Natl. Acad. Sci. USA. 1993;90:8424–8428. doi: 10.1073/pnas.90.18.8424. PubMed DOI PMC
Humpolíček P., Radaszkiewicz K.A., Kašpárková V., Stejskal J., Trchová M., Kuceková Z., Vičarová H., Pacherník J., Lehocký M., Minařík A. Stem cell differentiation on conducting polyaniline. RSC Adv. 2015;5:68796–68805. doi: 10.1039/C5RA12218J. DOI
Bober P., Humpolíček P., Pacherník J., Stejskal J., Lindfors T. Conducting polyaniline based cell culture substrate for embryonic stem cells and embryoid bodies. RSC Adv. 2015;5:50328–50335. doi: 10.1039/C5RA07504A. DOI
Konopka R., Hýzdalová M., Kubala L., Pacherník J. New luminescence-based approach to measurement of luciferase gene expression reporter activity and adenosine triphosphate-based determination of cell viability. Folia Biol. 2010;56:66–71. PubMed
Willems E., Mateizel I., Kemp C., Cauffman G., Sermon K., Leyns L. Selection of reference genes in mouse embryos and in differentiating human and mouse ES cells. Int. J. Dev. Biol. 2006;50:627–635. doi: 10.1387/ijdb.052130ew. PubMed DOI
Abranches E., Silva M., Pradier L., Schulz H., Hummel O., Henrique D., Bekman E. Neural Differentiation of Embryonic Stem Cells In Vitro: A Road Map to Neurogenesis in the Embryo. PLoS ONE. 2009;4:e6286. doi: 10.1371/journal.pone.0006286. PubMed DOI PMC
Večeřa J., Kudová J., Kučera J., Kubala L., Pacherník J. Neural Differentiation Is Inhibited through HIF1α/β-Catenin Signaling in Embryoid Bodies. Stem Cells Int. 2017;2017:8715798. doi: 10.1155/2017/8715798. PubMed DOI PMC
Kučera J., Binó L., Štefková K., Jaroš J., Vašíček O., Večeřa J., Kubala L., Pacherník J. Apocynin and Diphe-nyleneiodonium Induce Oxidative Stress and Modulate PI3K/Akt and MAPK/Erk Activity in Mouse Embryonic Stem Cells. Oxidative Med. Cell. Longev. 2016;2016:7409196. doi: 10.1155/2016/7409196. PubMed DOI PMC
Binó L., Veselá I., Papežíková I., Procházková J., Vašíček O., Štefková K., Kučera J., Hanáčková M., Ku-bala L., Pacherník J. The depletion of p38alpha kinase upregulates NADPH oxidase 2/NOX2/gp91 expression and the pro-duction of superoxide in mouse embryonic stem cells. Arch. Biochem. Biophys. 2019;671:18–26. doi: 10.1016/j.abb.2019.06.001. PubMed DOI
Chen J., Zacharek A., Li Y., Li A., Wang L., Katakowski M., Roberts C., Lu M., Chopp M. N-cadherin me-diates nitric oxide-induced neurogenesis in young and retired breeder neurospheres. Neuroscience. 2006;140:377–388. doi: 10.1016/j.neuroscience.2006.02.064. PubMed DOI PMC
Fiszbein A., Schor I.E., Kornblihtt A.R. Fundamentals of NCAM Expression, Function, and Regulation of Alternative Splicing in Neuronal Differentiation. In: Pruszak J., editor. Neural Surface Antigens. Academic Press; Boston, MA, USA: 2015. pp. 131–140.
Fanarraga M.L., Avila J., Zabala J.C. Expression of unphosphorylated class III beta-tubulin isotype in neuroepithelial cells demonstrates neuroblast commitment and differentiation. Eur. J. Neurosci. 1999;11:516–527. doi: 10.1046/j.1460-9568.1999.00459.x. PubMed DOI
Gleeson J.G., Lin P.T., Flanagan L.A., Park P.J. Doublecortin Is a Microtubule-Associated Protein and Is Expressed Widely by Migrating Neurons. Neuron. 1999;23:257–271. doi: 10.1016/S0896-6273(00)80778-3. PubMed DOI
Fourniol F., Perderiset M., Houdusse A., Moores C. Chapter 3—Structural Studies of the Doublecortin Family of MAPs. In: Correia J.J., Wilson L., editors. Methods in Cell Biology. Volume 115. Academic Press; Boston, MA, USA: 2013. pp. 27–48. PubMed
She X., Rohl C.A., Castle J.C., Kulkarni A., Johnson J.M., Chen R. Definition, conservation and epigenetics of housekeeping and tissue-enriched genes. BMC Genom. 2009;10:269. doi: 10.1186/1471-2164-10-269. PubMed DOI PMC
Capáková Z., Radaszkiewicz K.A., Acharya U., Truong T.H., Pacherník J., Bober P., Kašpárková V., Stejskal J., Pfleger J., Lehocký M., et al. The biocompatibility of polyaniline and polypyrrole 211.Doping with organic phosphonates. Mater. Sci. Eng. C. 2020;113:110986. doi: 10.1016/j.msec.2020.110986. PubMed DOI
Smith A., Nichols J., Robertson M., Rathjen P.D. Differentiation inhibiting activity (DIA/LIF) and mouse development. Dev. Biol. 1992;151:339–351. doi: 10.1016/0012-1606(92)90174-F. PubMed DOI
Cerdan C., Hong S.H., Bhatia M. Formation and Hematopoietic Differentiation of Human Embryoid Bodies by Suspen-sion and Hanging Drop Cultures. Curr. Protoc. Stem Cell Biol. 2007;3:1D.2.1–1D.2.16. doi: 10.1002/9780470151808.sc01d02s3. PubMed DOI
Granato A.E.C., Ribeiro A.C., Marciano F.R., Rodrigues B.V.M., Lobo A.O., Porcionatto M. Polypyrrole in-creases branching and neurite extension by Neuro2A cells on PBAT ultrathin fibers. Nanomed. Nanotechnol. Biol. Med. 2018;14:1753–1763. doi: 10.1016/j.nano.2018.05.004. PubMed DOI
Stewart E., Kobayashi N.R., Higgins M.J., Quigley A.F., Jamali S.C., Moulton S.E., Kapsa R., Wallace G.G., Crook J.M. Electrical Stimulation Using Conductive Polymer Polypyrrole Promotes Differentiation of Human Neural Stem Cells: A Biocompatible Platform for Translational Neural Tissue Engineering. Tissue Eng. Part C Methods. 2015;21:385–393. doi: 10.1089/ten.tec.2014.0338. PubMed DOI
Wang X., Gu X., Yuan C., Chen S., Zhang P., Zhang T., Yao J., Chen F., Chen G. Evaluation of biocompat-ibility of polypyrrole in vitro and in vivo. J. Biomed. Mater. Res. Part A. 2004;68:411–422. doi: 10.1002/jbm.a.20065. PubMed DOI
Sun B., Wu T., Wang J., Li D., Wang J., Gao Q., Bhutto M.A., El-Hamshary H., Al-Deyab S.S., Mo X. Polypyrrole-coated poly(l-lactic acid-co-ε-caprolactone)/silk fibroin nanofibrous membranes promoting neural cell proliferation and differentiation with electrical stimulation. J. Mater. Chem. B. 2016;4:6670–6679. doi: 10.1039/C6TB01710J. PubMed DOI
Simpson T.I., Price D.J. Pax6: A pleiotropic player in development. BioEssays. 2002;24:1041–1051. doi: 10.1002/bies.10174. PubMed DOI
Pevny L.H., Sockanathan S., Placzek M., Lovell-Badge R. A role for SOX1 in neural determination. Development. 1998;125:1967–1978. PubMed
Lo L., Tiveron M.C., Anderson D.J. MASH1 activates expression of the paired homeodomain transcription factor Phox2a, and couples pan-neuronal and subtype-specific components of autonomic neuronal identity. Development. 1998;125:609–620. PubMed
Kumar N., Afeyan R., Sheppard S., Harms B., Lauffenburger D.A. Quantitative analysis of Akt phosphorylation and activity in response to EGF and insulin treatment. Biochem. Biophys. Res. Commun. 2007;354:14–20. doi: 10.1016/j.bbrc.2006.12.188. PubMed DOI PMC
Kučera J., Netušilová J., Sladeček S., Lánová M., Vašíček O., Štefková K., Navrátilová J., Kubala L., Pacherník J. Hypoxia Downregulates MAPK/ERK but Not STAT3 Signaling in ROS-Dependent and HIF-1-Independent Manners in Mouse Embryonic Stem Cells. Oxidative Med. Cell. Longev. 2017;2017:1–16. doi: 10.1155/2017/4386947. PubMed DOI PMC
Rai S.N., Dilnashin H., Birla H., Singh S.S., Zahra W., Rathore A.S., Singh B.K., Singh S.P. The Role of PI3K/Akt and ERK in Neurodegenerative Disorders. Neurotox. Res. 2019;35:775–795. doi: 10.1007/s12640-019-0003-y. PubMed DOI
Burke R.E. Inhibition of mitogen-activated protein kinase and stimulation of Akt kinase signaling pathways: Two approaches with therapeutic potential in the treatment of neurodegenerative disease. Pharmacol. Ther. 2007;114:261–277. doi: 10.1016/j.pharmthera.2007.02.002. PubMed DOI PMC
Cross D.A.E., Alessi D.R., Cohen P., Andjelkovich M., Hemmings B.A. Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nat. Cell Biol. 1995;378:785–789. doi: 10.1038/378785a0. PubMed DOI
McCubrey J.A., Steelman L.S., Bertrand F.E., Davis N.M., Sokolosky M., Abrams S.L., Montalto G., D’Assoro A.B., Libra M., Nicoletti F., et al. GSK-3 as potential target for therapeutic intervention in cancer. Oncotarget. 2014;5:2881–2911. doi: 10.18632/oncotarget.2037. PubMed DOI PMC
Eldar-Finkelman H., Martinez A. GSK-3 Inhibitors: Preclinical and Clinical Focus on CNS. Front. Mol. Neurosci. 2011;4:32. doi: 10.3389/fnmol.2011.00032. PubMed DOI PMC
Pap M., Cooper G.M. Role of Glycogen Synthase Kinase-3 in the Phosphatidylinositol 3-Kinase/Akt Cell Survival Pathway. J. Biol. Chem. 1998;273:19929–19932. doi: 10.1074/jbc.273.32.19929. PubMed DOI
Coghlan M.P., Culbert A.A., Cross D.A.E., Corcoran S.L., Yates J.W., Pearce N.J., Rausch O.L., Mur-phy G.J., Carter P.S., Roxbee Cox L., et al. Selective small molecule inhibitors of glycogen synthase kinase-3 modulate glycogen metab-olism and gene transcription. Chem. Biol. 2000;7:793–803. doi: 10.1016/S1074-5521(00)00025-9. PubMed DOI
Kramer T., Schmidt B., Monte F.L. Small-Molecule Inhibitors of GSK-3: Structural Insights and Their Application to Alzheimer’s Disease Models. Int. J. Alzheimer’s Dis. 2012;2012:1–32. doi: 10.1155/2012/381029. PubMed DOI PMC
Desai M.C., Ng S., Ni Z.J., Pfister K.B., Ramurthy S., Subramanian S., Wagman A.S. Pyrrole Based Inhibitors of Glycogen Synthase Kinase 3. No. 7,250,443. U.S. Patent. 2007 Jul 31;
Beurel E., Grieco S.F., Jope R.S. Glycogen synthase kinase-3 (GSK3): Regulation, actions, and diseases. Pharmacol. Ther. 2015;148:114–131. doi: 10.1016/j.pharmthera.2014.11.016. PubMed DOI PMC
Seira O., del Río J.A. Glycogen Synthase Kinase 3 Beta (GSK3β) at the Tip of Neuronal Development and Regeneration. Mol. Neurobiol. 2014;49:931–944. doi: 10.1007/s12035-013-8571-y. PubMed DOI
Manning B.D., Toker A. AKT/PKB Signaling: Navigating the Network. Cell. 2017;169:381–405. doi: 10.1016/j.cell.2017.04.001. PubMed DOI PMC
Kotasová H., Veselá I., Kučera J., Houdek Z., Procházková J., Králičková M., Pacherník J. Phosphoinositide 3-kinase inhibition enables retinoic acid-induced neurogenesis in monolayer culture of embryonic stem cells. J. Cell. Biochem. 2012;113:563–570. doi: 10.1002/jcb.23380. PubMed DOI
Wataya T., Ando S., Muguruma K., Ikeda H., Watanabe K., Eiraku M., Kawada M., Takahashi J., Hashimoto N., Sasai Y. Minimization of exogenous signals in ES cell culture induces rostral hypothalamic differentiation. Proc. Natl. Acad. Sci. USA. 2008;105:11796–11801. doi: 10.1073/pnas.0803078105. PubMed DOI PMC
Pacherník J., Esner M., Bryja V., Dvořak P., Hampl A. Neural differentiation of mouse embryonic stem cells grown in monolayer. Reprod. Nutr. Dev. 2003;42:317–326. doi: 10.1051/rnd:2002028. PubMed DOI
Stejskal J., Hajná M., Kašpárková V., Humpolíček P., Zhigunov A., Trchová M. Purification of a conducting polymer, polyaniline, for biomedical applications. Synth. Met. 2014;195:286–293. doi: 10.1016/j.synthmet.2014.06.020. DOI
Kašpárková V., Humpolíček P., Stejskal J., Kopecká J., Kuceková Z., Moučka R. Conductivity, impurity profile, and cytotoxicity of solvent-extracted polyaniline. Polym. Adv. Technol. 2016;27:156–161. doi: 10.1002/pat.3611. DOI
Appel G., Schmeißer D., Bauer J., Bauer M., Egelhaaf H.J., Oelkrug D. The formation of oligomers in the electrolyte upon polymerization of pyrrole. Synth. Met. 1999;99:69–77. doi: 10.1016/S0379-6779(98)00200-8. DOI
Fermin D., Scharifker B. Products in solution during electrodeposition of polypyrrole. J. Electroanal. Chem. 1993;357:273–287. doi: 10.1016/0022-0728(93)80385-U. DOI
Ozeki Y., Omae M., Kitagawa S., Ohtani H. Electrospray ionization-ion mobility spectrometry-high resolution tandem mass spectrometry with collision-induced charge stripping for the analysis of highly multiply charged intact polymers. Analyst. 2019;144:3428–3435. doi: 10.1039/C8AN02500B. PubMed DOI
Park S.J., Park N.H., Kim N.H., Lee S., Yoon B.H., Jung W.Y., Lee K.-T., Cheong J.H., Ryu J.H. The memory-enhancing effects of Euphoria longan fruit extract in mice. J. Ethnopharmacol. 2010;128:160–165. doi: 10.1016/j.jep.2010.01.001. PubMed DOI
Zheng G., Wei X., Xu L., Li Z., Liu G., Zhang X. A New Natural Lactone from Dimocarpus longan Lour. Seeds. Molecules. 2012;17:9421–9425. doi: 10.3390/molecules17089421. PubMed DOI PMC
Reddy C.R., Tukaram A.G., Mohammed S.Z., Dilipkumar U., Babu B.N., Chakravarty S., Bhattacharya D., Joshi P., Gree R. Synthesis and biological evaluation of longanlactone analogues as neurotrophic agents. Bioorganic Med. Chem. Lett. 2018;28:673–676. doi: 10.1016/j.bmcl.2018.01.020. PubMed DOI