Skip to main content
SpringerLink
Log in

Induction of the Cholinergic Phenotype in Mouse Neuroblastoma Cells Using Nerve Growth Factor

  • EXPERIMENTAL ARTICLES
  • Published:
Neurochemical Journal Aims and scope Submit manuscript

Abstract—Nerve growth factor (NGF) is a factor which determines neuronal differentiation. NGF plays an important role in growth and differentiation of sensory and sympathetic neurons in the peripheral nervous system. In the mature brain, NGF is involved in the maintenance of the cholinergic neuronal phenotype. Here, we studied a possibility to induce the cholinergic phenotype in mouse neuroblastoma cells, which are often used to model various physiological and pathological processes occurring in the nervous system. Cells of NB41A3 and Neuro2a neuroblastoma lines are most frequently used to study the properties of cholinergic neurons. In the cells of these lines, the expression of TrkA and p75NGFR receptors, which is specific for the forebrain cholinergic nuclei, was revealed. Differentiation of the cells was induced by application of NGF or 8-Br-cAMP. NGF did not induce neuronal differentiation. Moreover, we did not find any changes in the content of choline acetyltransferase and vesicular acetylcholine transporter mRNA and protein, which were used as markers of the cholinergic phenotype. Thus, NB41A3 and Neuro2a cell lines cannot be advised as a model of cholinergic neurons in vitro because they do not differentiate and/or exhibit signs of the cholinergic phenotype in response to NGF stimulation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.

REFERENCES

  1. Meakin, S.O. and Shooter, E.M., Trends Neurosci., 1992, vol. 15, pp. 323–331.

    Article  CAS  PubMed  Google Scholar 

  2. Sofroniew, M.V., Howe, C.L., and Mobley, W.C., Annu. Rev. Neurosci., 2001, vol. 24, pp. 1217–1281.

    Article  CAS  PubMed  Google Scholar 

  3. Chao, M.V., Nat. Rev. Neurosci., 2003, vol. 4, pp. 299–309.

    Article  CAS  PubMed  Google Scholar 

  4. Niewiadomska, G., Mietelska-Porowska, A., and Mazurkiewicz, M., Behav. Brain Res., 2011, vol. 221, pp. 515–526.

    Article  CAS  PubMed  Google Scholar 

  5. Schliebs, R. and Arendt, T., Behav. Brain Res., 2011, vol. 221, pp. 555–563.

    Article  CAS  PubMed  Google Scholar 

  6. Tuszynski, M.H., Cell Transplant., 2000, vol. 9, pp. 629–636.

    Article  CAS  PubMed  Google Scholar 

  7. Dobryakova, Y.V., Spivak, Y.S., Zaichenko, M.I., Koryagina, A.A., Markevich, V.A., Stepanichev, M.Y., and Bolshakov, A.P., Front. Neurosci., 2021, vol. 15, p. 745050.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Dobryakova, Y.V., Zaichenko, M.I., Spivak, Y.S., Stepaniche, M.Y., Markevich, V.A., and Bolshakov, A.P., Neurochem. J., 2021, vol. 15, pp. 273–281.

    Article  CAS  Google Scholar 

  9. Stepanichev, M.Y., Neurochem. J., 2011, vol. 5, pp. 159–168.

    Article  CAS  Google Scholar 

  10. Tuszynski, M.H., Yang, J.H., Barb, D., U, H.S., Bakay, R.A., Pay, M.M., Masliah, E., Conner, J.M., Kobalka, P., Roy, S., and Nagahara, A.H, JAMA Neurol., 2015, vol. 72, pp. 1139–1147.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Tuszynski, M.H., Thal, L., Pay, M., Salmon, D.P., U, H.S., Bakay, R., Patel, P., Blesch, A., Vahlsing, H.L., Ho, G., Tong, G., Potkin, S.G., Fallon, J., Hansen, L., Mufson, E.J., Kordower, J.H., Gall, C., and Conner, J., Nat. Med., 2005, vol. 11, pp. 551–555.

    Article  CAS  Google Scholar 

  12. Ferro, M. and Doyle, A., Cell Biol. Toxicol., 2001, vol. 17, pp. 205–212.

    Article  CAS  PubMed  Google Scholar 

  13. Colom, L.V., Castaneda, M.T., Reyna, T., Hernandez, S., and Garrido-Sanabria, E., Synapse, 2005, vol. 58, pp. 151–164.

    Article  CAS  PubMed  Google Scholar 

  14. Colom, L.V., Castaneda, M.T., Aleman, D., and Touhami, A., Neurosci. Let., 2013, vol. 541, pp. 54–57.

    Article  CAS  Google Scholar 

  15. Huh, C.Y.L., Danik, M., Manseau, F., Trudeau, L.E., and Williams, S., J. Neurosci., 2008, vol. 28, pp. 1404–1409.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Teles-Grilo, RuivoL.M. and Mellor, J.R., Front. Synaptic Neurosci., 2013, vol. 5, p. 2.

    Google Scholar 

  17. Mangoura, D. and Vernadakis, A., Dev. Brain Res., 1988, vol. 40, pp. 25–35.

    Article  CAS  Google Scholar 

  18. Latina, V., Caioli, S., Zona, C., Ciotti, M.T., Amadoro, G., and Calissano, P., Front. Cell Neurosci., 2017, vol. 11, p. 68.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Antonov, S.A., Manuilova, E.S., Dolotov, O.V., Kobylyansky, A.G., Safina, D.R., and Grivennikov, I.A., Bull. Exp. Biol. Med., 2017, vol. 162, pp. 679–683.

    Article  CAS  PubMed  Google Scholar 

  20. Ortiz-Virumbrales, M., Moreno, C.L., Kruglikov, I., Marazuela, P., Sproul, A., Jacob, S., Zimmer, M., Paull, D., Zhang, B., Schadt, E.E., Ehrlich, M.E., Tanzi, R.E., Arancio, O., Noggle, S., and Gandy, S., Acta Neuropathol. Commun., 2017, vol. 5, p. 77.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Moreno, C.L., Guardia, L., Della, ShnyderV., Ortiz-Virumbrales, M., Kruglikov, I., Zhang, B., Schadt, E.E., Tanzi, R.E., Noggle, S., Buettner, C., and Gandy, S., Mol. Neurodegener., 2018, vol. 13, p. 33.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Campos, CogoS., Gradowski Farias Da Costa Do Nascimento, T., De Almeida Brehm Pinhatti, F., De Franca Junio, N., Santos Rodrigues, B., Cavalli, L.R., and Elifio-Esposito, S., Exp. Biol. Med., 2020, vol. 245, pp. 1637–1647.

    Google Scholar 

  23. Johnsen, J.I., Dyberg, C., and Wickstrom, M., Front. Mol. Neurosci., 2019, vol. 12, p. 9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Rosenberg, R.N., Vandeventer, L., De Francesco, L., and Friedkin, M.E., Proc. Natl. Acad. Sci. USA, 1971, vol. 68, pp. 1436–1440.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  25. Blusztajn, J.K., Venturini, A., Jackson, D.A., Lee, H.J., and Wainer, B.H., J. Neurosci., 1992, vol. 12, pp. 793–799.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Kumar, M. and Katyal, A., Data Br., 2018, vol. 21, pp. 2435–2440.

    Article  Google Scholar 

  27. Thompson, J., London, E., and Johnson, Jr., J., Neuroscience, 1982, vol. 7, pp. 1807–1815.

    Article  CAS  PubMed  Google Scholar 

  28. Thompson, G., Lewis, J., and Mawdsley, D., www.dst.defence.gov.au/publication/characterisation-cell-culture-system-investigating-nerve-agent-neurotoxicology-part-i

  29. Monsma, F.J., Brassard, D.L., and Sibley, D.R., Brain Res., 1989, vol. 492, pp. 314–324.

    Article  CAS  PubMed  Google Scholar 

  30. Dziedzicka-Wasylewska, M. and Solich, J., Mol. Brain Res., 2004, vol. 128, pp. 75–82.

    Article  CAS  PubMed  Google Scholar 

  31. Pemberton, K., Mersman, B., and Xu, F., J. Undergrad. Neurosci. Educ., 2018, vol. 16, pp. A186–A194.

    PubMed  PubMed Central  Google Scholar 

  32. Zeineldin, M., Patel, A.G., and Dyer, M.A., Neuron, 2022, vol. 110, pp. 2916–2928.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Chen, T., Hinton, D., Zidovetzki, R., and Hofman, F., Lab. Invest., 1998, vol. 78, pp. 165–174.

    CAS  PubMed  Google Scholar 

  34. Sanchez, S., Jimenez, C., Carrera, A.C., Diaz-Nido, J., Avila, J., and Wandosell, F., Neurochem. Int., 2004, vol. 44, pp. 231–242.

    Article  CAS  PubMed  Google Scholar 

  35. Aloe, L., Rocco, M.L., Balzamino, B.O., and Micera, A., J. Exp. Clin. Cancer Res., 2016, vol. 35, pp. 1–7.

    Article  Google Scholar 

  36. Martorana, F., Gaglio, D., Bianco, M.R., Aprea, F., Virtuoso, A., Bonanomi, M., Alberghina, L., Papa, M., and Colangelo, A.M., Cell Death Dis., 2018, vol. 9, p. 391.

    Article  PubMed  PubMed Central  Google Scholar 

  37. Reichardt, L.F., Philos. Trans. R. Soc. Lond. B. Biol. Sci., 2006, vol. 361, pp. 1545–1564.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Yeo, T.T., Chua-Couzens, J., Butcher, L.L., Bredesen, D.E., Cooper, J.D., Valletta, J.S., Mobley, W.C., and Longo, F.M., J. Neurosci., 1997, vol. 17, pp. 7594–7605.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Sobreviela, T., Clary, D.O., Reichardt, L.F., Brandabur, M.M., Kordower, J.H., and Mufson, E.J., J. Comp. Neurol., 1994, vol. 350, pp. 587–611.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Wu, D. and Hersh, L.B., J. Neurochem., 1994, vol. 62, pp. 1653–1663.

    Article  CAS  PubMed  Google Scholar 

  41. Blume, A., Gilbert, F., Wilson, S., Farber, J., Rosenberg, R., and Nirenberg, M., Proc. Natl. Acad. Sci. USA, 1970, vol. 67, pp. 786–792.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  42. Harris, A.J. and Dennis, M.J., Science, 1970, vol. 167, pp. 1253–1255.

    Article  CAS  PubMed  ADS  Google Scholar 

Download references

Funding

This study was supported by the Russian Basic Research Foundation, project no. 20-015-00226.

Author information

Authors and Affiliations

  1. Institute of Higher Nervous Activity and Neurophysiology, Russian Academy of Sciences, Moscow, Russia

    A. A. Koryagina, O. A. Nedogreeva, A. A. Buyanova, Yu. S. Spivak, A. P. Bolshakov, N. V. Gulyaeva & M. Yu. Stepanichev

Authors
  1. A. A. Koryagina
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. O. A. Nedogreeva
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. A. Buyanova
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yu. S. Spivak
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. A. P. Bolshakov
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. N. V. Gulyaeva
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. M. Yu. Stepanichev
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M. Yu. Stepanichev.

Ethics declarations

All experiments with animals were performed according to the Directive 2010/63/EU of the European Parliament and of the Council of 22 September 2010.

CONFLICT OF INTEREST

The authors of this work declare that they have no conflicts of interest.

Additional information

Publisher’s Note.

Pleiades Publishing remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Corresponding author: address: ul. Butlerova, 5a, Moscow, 117485 Russia; e-mail: m_stepanichev@ihna.ru.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Koryagina, A.A., Nedogreeva, O.A., Buyanova, A.A. et al. Induction of the Cholinergic Phenotype in Mouse Neuroblastoma Cells Using Nerve Growth Factor. Neurochem. J. 17, 740–750 (2023). https://doi.org/10.1134/S181971242304013X

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S181971242304013X

Key words:

Search

Navigation