Skip to main content
Log in

Distinctive features of immune proteasome expression during the development of the central nervous system in rats

  • Published:
Russian Journal of Bioorganic Chemistry Aims and scope Submit manuscript

Abstract

Formation of the central nervous system in ontogeny and its functioning in adult mammals are controlled by the universal ubiquitin-proteasome proteolytic system. The aim of the present work was to study the dynamics of immune proteasome expression as compared with the dynamics of chymotrypsin-like and caspase-like activities of the proteasome (ChLA and CLA) and expression of the transcription factor Zif268 in selected brain structures (cortex, hippocampus, and brainstem) in embryonic (days E19 and E21 of embryonic development) and early postnatal (postnatal days P1, P3, P4, P5, P7, and P15) development in rats. ChLA and CLA were determined in clarified homogenates of rat brain structures using commercial fluorogenic oligopeptide substrates Suc-LLVY-AMC and Z-LLG-AMC, respectively. Levels of constitutive (β1 and β5) and immune (LMP7 and LMP2) proteasome subunits, as well as those of proteasome activators PA700 and PA28 and the transcription factor Zif268, were evaluated by Western blotting. Increased expression of the immune subunit LMP7 in the cerebral cortex and hippocampus was observed during the period of active formation of the biochemical mediator structure of neurons (P7-P15). Increased ChLA and CLA were registered in the cortex during this period. The content of the immune subunit LMP2 was significantly elevated in all brain structures between P7 and P15. The content of the constitutive proteolytic subunit β1 in all structures was lower on P4 than on P1 and increased to the same level as on P1 by P15. However, the expression level of the constitutive proteolytic β5 subunit of the proteasome in the cortex, hippocampus, and brainstem increased starting from E21 and reached maximal values at P3, P5 and P1, respectively, with a sharp decline in all structures by P7. Expression of the immune subunit LMP2 and the constitutive subunit β1 in all structures increased sharply around P15 concomitantly to the increase in the content of the immune subunit LMP7. Moreover, a positive correlation of increased expression of the activator PA28 and the constitutive β5 subunit in the hippocampus during P3-P5 and in the brain stem during P1-P5 has been demonstrated. Elevation of proteasome CLA and expression levels of immune proteasome subunits LMP2 and LMP7 during days P7-P15 of postnatal development in the brain regions investigated were related to the expression of the transcription factor Zif268. Immune proteasomes probably play an important role in the regulation of key biochemical processes during early ontogenesis of the central nervous system and are necessary for the emergence and maintenance of synaptic plasticity in rat brain structures analyzed.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

AMC:

7-amido-4-methylcoumarin

Suc:

succinyl

Z:

benzyloxycarbonyl

P1-P15:

days of postnatal development

UPS:

the ubiquitin-proteasome system

CNS:

central nervous system

E19-E21:

days of embryonic development

References

  1. Ba, A. and Seri, B.V., Neurosci. Biobehav. Rev., 1995, vol. 19, pp. 413–425.

    Article  CAS  PubMed  Google Scholar 

  2. Tolkunov, B.F., Striatum i sensornaya spetsializatsiya neironnoi seti (Striatum and Sensor Specialization of the Neuronal Network), Leningrad: Nauka, 1978.

    Google Scholar 

  3. Goldman-Rakic, P.S. and Selemon, L.D., Trends Neurosci., 1990, vol. 13, pp. 241–244.

    Article  CAS  PubMed  Google Scholar 

  4. Ellis, R.J. and Van der Vies, S.M., Annu. Rev. Biochem., 1991, vol. 1, pp. 321–347.

    Article  Google Scholar 

  5. Ciechanover, A., Orian, A., and Schwartz, A.L., J. Cell. Biochem., 2000, vol. 77, pp. 40–51.

    Article  Google Scholar 

  6. Hershko, A., Cell Death Differ., 2005, vol. 12, pp. 1191–1197.

    Article  CAS  PubMed  Google Scholar 

  7. Rock, K.L. and Goldberg, A.L., Annu. Rev. Immunol., 1999, vol. 17, pp. 739–779.

    Article  CAS  PubMed  Google Scholar 

  8. Abramova, E.B., Sharova, N.P., and Karpov, V.L., Biol. Bull. (Moscow), 2002, vol. 36, pp. 761–776.

    CAS  Google Scholar 

  9. Grune, T., Reinheckel, T., and Davies, K.J.A., J. Biol. Chem., 1996, vol. 271, pp. 15504–15509.

    Article  CAS  PubMed  Google Scholar 

  10. Sharova, N.P., Russ. J. Dev. Biol., 2006, vol. 37, pp. 139–145.

    Article  CAS  Google Scholar 

  11. Groettrup, M., Standera, S., Stohwasser, R., and Kloetzel, P.M., Proc. Natl. Acad. Sci. USA, 1997, vol. 94, pp. 8970–8975.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  12. Dahlmann, B., Ruppert, T., Kuehn, L., Merforth, S., and Kloetzel, P.M., J. Mol. Biol., 2000, vol. 303, pp. 643–653.

    Article  CAS  PubMed  Google Scholar 

  13. Dahlmann, B., Ruppert, T., Kloetzel, P.M., and Kuehn, L., Biochimie, 2001, vol. 83, no. 3, pp. 295–299.

    Article  CAS  PubMed  Google Scholar 

  14. Astakhova, T.M. and Sharova, N.P., Biol. Bull. (Moscow), 2006, vol. 33, no. 3, pp. 216–233.

    Article  CAS  Google Scholar 

  15. Shimbara, N., Nakajima, H., Tanahashi, N., Ogawa, K., Niwa, S., Uenaka, A., Nakayama, E., and Tanaka, K., Genes to Cells, 1997, vol. 2, pp. 785–800.

    Article  CAS  PubMed  Google Scholar 

  16. Janeway, C. and Travers, P., Immunobiology: The Immune System in Health and Disease, New York: Current Biology Limited, Garland Pub. Inc., 1994.

    Google Scholar 

  17. Galaktionov, V.G., Immunologiya (Immunology), Moscow: Izdat. tsentr Akademiya, 2004.

    Google Scholar 

  18. Yarilin, A.A., Immunologiya (Immunology), Moscow: Izdat. Gruppa GEOTAR-Media, 2010.

    Google Scholar 

  19. Caudill, C.M., Jayarapu, K., Elenich, L., Monaco, J.J., Colbert, R.A., and Griffin, T.A., J. Immunol., 2006, vol. 176, pp. 4075–4082.

    Article  CAS  PubMed  Google Scholar 

  20. Sijts, E. and Kloetzel, P.M., Cell. Mol. Life Sci., 2011, vol. 68, pp. 1491–1502.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  21. Stohwasser, R., Giesebrecht, J., Kraft, R., Müller, E.C., Häusler, K.G., Kettenmann, H., Hanisch, U.K., and Kloetzel, P.M., Glia, 2000, vol. 29, pp. 355–365.

    Article  CAS  PubMed  Google Scholar 

  22. Needleman, L.A., Liu, X.B., El-Sabeawy, F., Jones, E.G., and McAllister, A.K., Proc. Natl. Acad. Sci. USA, 2010, vol. 107, pp. 16999–17004.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  23. Loconto, J., Papes, F., Chang, E., Stowers, L., Jones, E.P., Takada, T., Kumanovics, A., Fischer, L.K., and Dulac, C., Cell, 2003, vol. 112, pp. 607–618.

    Article  CAS  PubMed  Google Scholar 

  24. Barco, A., Patterson, S.L., Alarcon, J.M., Gromova, P., Mata-Roig, M., Morozov, A., and Kandel, E.R., Neuron, 2005, vol. 48, pp. 123–137.

    Article  CAS  PubMed  Google Scholar 

  25. Lyupina, Yu.V., Orlova, A.Sh., Gornostaev, N.G., Karpova, Ya.D., Mikhailov, V.S., and Sharova, N.P., Zh. Obshch. Biol., 2014, vol. 75, pp. 3–24.

    Google Scholar 

  26. Qureshi, N., Vogel, S.N., Van Way, C., 3rd, Papasian, C.J., Qureshi, A.A., and Morrison, D.C., Immun. Res., 2005, vol. 31, pp. 243–260.

    Article  CAS  Google Scholar 

  27. Shen, J., Reis, J., Morrison, D.C., Papasian, C., Raghavakaimal, S., Kolbert, C., Qureshi, A.A., Vogel, S.N., and Qureshi, N., Shock, 2006, vol. 25, pp. 472–484.

    Article  CAS  PubMed  Google Scholar 

  28. Bi, W., Zhu, L., Zeng, Z., Jing, X., Liang, Y., Guo, L., Shi, Q., Xu, A., and Tao, E., Neuroimmunomodulation, 2014 (Epub ahead of print).

    Google Scholar 

  29. Szabo, Z., Ying, Z., Radak, Z., and Gomez-Pinilla, F., Brain Res., 2010, vol. 1341, pp. 25–31.

    Article  CAS  PubMed  Google Scholar 

  30. Bozon, B., Davis, S., and Laroche, S., Neuron, 2003, vol. 40, pp. 695–701.

    Article  CAS  PubMed  Google Scholar 

  31. Knapska, E. and Kaczmarek, L., Progr. Neurobiol., 2004, vol. 74, pp. 183–211.

    Article  CAS  Google Scholar 

  32. Lee, J.L.C., Everitt, B.J., and Thomas, K.L., Science, 2004, vol. 304, pp. 839–843.

    Article  CAS  PubMed  Google Scholar 

  33. Clayton, D.F., Neurobiol. Learn. Mem., 2000, vol. 74, pp. 185–216.

    Article  CAS  PubMed  Google Scholar 

  34. James, A.B., Conway, A.-M., and Morris, B.J., J. Neurosci., 2006, vol. 26, pp. 1624–1634.

    Article  CAS  PubMed  Google Scholar 

  35. James, A.B., Conway, A.-M., and Morris, B.J., J. Neurochem., 2005, vol. 95, pp. 796–810.

    Article  CAS  PubMed  Google Scholar 

  36. Gavilan, M.P., Castano, A., Torres, M., Potravella, M., Caballero, C., Jimenez, S., Garcia-Martines, A., Parrado, J., Victorica, J., and Ruano, D., J. Neurochem., 2009, vol. 108, pp. 260–272.

    Article  CAS  PubMed  Google Scholar 

  37. Fabunmi, R.P., Wigley, W.C., Thomas, P.G., and DeMartino, G.N., J. Cell Sci., 2000, vol. 114, pp. 29–36.

    Google Scholar 

  38. Dick, T.P., Ruppert, T., Groettrup, M., Kloetzel, P.M., Kuehn, L., Koszinowski, U.H., Stevanovic, S., Schild, H., and Rammensee, H.G., Cell, 1996, vol. 86, pp. 253–262.

    Article  CAS  PubMed  Google Scholar 

  39. Groettrup, M., Soza, A., Eggers, M., Kuehn, L., Dick, T.P., Schild, H., Rammensee, H.G., Koszinowski, U.H., and Kloetzel, P.M., Nature, 1996, vol. 381, pp. 166–168.

    Article  CAS  PubMed  Google Scholar 

  40. Fabunmi, R.P., Wigley, W.C., Thomas, P.G., and DeMartino, G.N., J. Cell Sci., 2000, vol. 114, pp. 29–36.

    Google Scholar 

  41. Minami, Y., Kawasaki, H., Minami, M., Tanahashi, N., Tanaka, K., and Yahara, I., J. Biol. Chem., 2000, vol. 275, pp. 9055–9061.

    Article  CAS  PubMed  Google Scholar 

  42. Olenev, S.N., Razvivayushchiisya mozg: Kletochnye, molekulyarnye i geneticheskie aspekty neirofiziologii (Developing Brain: Cellular, Molecular, and Genetic Aspects of Neurophysiology), Leningrad: Nauka, 1978.

    Google Scholar 

  43. Hegde, A.N., Learn. Mem., 2010, vol. 17, pp. 314–327.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  44. Ehlers, M.D., Nat. Neurosci., 2003, vol. 6, pp. 231–242.

    Article  CAS  PubMed  Google Scholar 

  45. Karpova, Ya.D., Lyupina, Yu.V., Astakhova, T.M., Stepanova, A.A., Erokhov, P.A., Abramova, E.B., and Sharova, N.P., Russ. J. Bioorgan. Chem., 2013, vol. 39, pp. 356–365.

    Article  CAS  Google Scholar 

  46. Laemmli, U.K., Nature, 1970, vol. 227, pp. 680–685.

    Article  CAS  PubMed  Google Scholar 

  47. Smolen, A.J., Methods Neurosci., 1990, vol. 3, pp. 208–229.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yu. V. Lyupina.

Additional information

Original Russian Text © A.Sh. Orlova, Yu.V. Lyupina, S.B. Abaturova, N.P. Sharova, 2014, published in Bioorganicheskaya Khimiya, 2014, Vol. 40, No. 6, pp. 703–711.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Orlova, A.S., Lyupina, Y.V., Abaturova, S.B. et al. Distinctive features of immune proteasome expression during the development of the central nervous system in rats. Russ J Bioorg Chem 40, 649–657 (2014). https://doi.org/10.1134/S1068162014060119

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1068162014060119

Keywords

Navigation