Advertisement

Molecular Biology

, Volume 52, Issue 6, pp 937–946 | Cite as

The Effect of Beta-Amyloid Peptides and Main Stress Protein HSP70 on Human SH-SY5Y Neuroblastoma Proteome

  • A. P. Rezvykh
  • M. M. Yurinskaya
  • M. G. Vinokurov
  • G. S. Krasnov
  • V. A. Mitkevich
  • A. A. Makarov
  • M. B. Evgen’ev
  • O. G. ZatsepinaEmail author
PROTEOMICS
  • 35 Downloads

Abstract

The accumulation and aggregation of β-amyloids are major molecular events underlying the progression of Alzheimer’s disease. In neural cells, recombinant HSP70 reduces the toxic effect of Aβ and its isomeric forms. Here we describe the proteome of the neuroblastoma cell line after incubation with amyloid peptides Aβ42 and isomerized Asp7 (isoAβ42) without and with human recombinant heat shock protein 70 (HSP70). Incubation of SH-SY5Y cell culture with the synthetic Aβ-peptides leads to a decrease in the levels of several cytoskeleton proteins (e.g., ACTN1, VIME, TPM3) and several chaperonines involved in the folding of actin and tubulin (TCPQ, TCPG, TCPE, TCPB). These changes are accompanied by an increase in the expression of calmodulin and the proteins involved in folding in the endoplasmic reticulum and endoplasmic cell stress response. The presence of exogenous HSP70 has led to an increase in expression of several chaperones and a few other proteins including endogenous HSP70. A combined effect of recombinant HSP70 with Aβ peptides reduced cell apoptosis and significantly decreased the level of tubulin phosphorylation caused by the addition of Aβ peptides.

Keywords:

HSP70 β-amyloid Аβ (1–42) apoptosis neuroblastoma SH-SY5Y proteomics 

Notes

REFERENCES

  1. 1.
    Murphy M.P., LeVine H. III. 2010. Alzheimer’s disease and the amyloid-beta peptide. J. Alzheimers Dis. 19, 311–323.CrossRefGoogle Scholar
  2. 2.
    Hosoda R., Saido T.C., Otvos L., Arai T., Mann D.M., Lee V.M.Y., Trojanowski J.Q., Iwatsubo T. 1998. Quantification of modified amyloid β peptides in Alzheimer disease and Down syndrome brains. J. Neuropathol. Exp. Neurol. 57, 1089–1095.CrossRefGoogle Scholar
  3. 3.
    Shimizu T., Fukuda H., Murayama S., Izumiyama N., Shirasawa T. 2002. Isoaspartate formation at position 23 of amyloid beta peptide enhanced fibril formation and deposited onto senile plaques and vascular amyloids in Alzheimer’s disease. J. Neurosci. Res. 70, 451–461.CrossRefGoogle Scholar
  4. 4.
    Mitkevich V.A., Petrushanko I.Y., Yegorov Y.E., Simonenko O.V., Vishnyakova K.S., Kulikova A.A., Tsvetkov P.O., Makarov A.A., Kozin S.A. 2013. Isomerization of Asp7 leads to increased toxic effect of amyloid-b42 on human neuronal cells. Cell Death Dis. 4, 492.CrossRefGoogle Scholar
  5. 5.
    Kozin S.A., Mitkevich V.A., Makarov A.A. 2016. Amyloid-β containing isoaspartate 7 as potential biomarker and drug target in Alzheimer’s disease. Mendeleev Commun. 26, 269–275.CrossRefGoogle Scholar
  6. 6.
    Verdier Y., Zarándi M., Penke B. 2004. Amyloid  β‑peptide interactions with neuronal and glial cell plasma membrane: Binding sites and implications for Alzheimer’s disease. J. Pept. Sci. 10, 229–248.CrossRefGoogle Scholar
  7. 7.
    Kumar S., Wirths O., Theil S., Gerth J., Bayer T.A., Walter J. 2013. Early intraneuronal accumulation and increased aggregation of phosphorylated Abeta in a mouse model of Alzheimer’s disease. Acta Neuropathol. 125, 699–709.CrossRefGoogle Scholar
  8. 8.
    Medvedev A.E., Buneeva O.A., Kopylov A.T., Mitke-vich V.A., Kozin S.A., Zgoda V.G., Makarov A.A. 2016. Chemical modifications of amyloid-β(1-42) have a significant impact on the repertoire of brain amyloid-β(1-42) binding proteins. Biochimie. 128–129, 55–58.CrossRefGoogle Scholar
  9. 9.
    Henriques A.G., Müller T., Oliveira J.M.H., Cova M., Cristóvão B., Odete A.B. 2016. Altered protein phosphorylation as a resource for potential AD biomarkers. Sci. Rep. 6, 1–12.CrossRefGoogle Scholar
  10. 10.
    Zatsepina O.G., Kechko O.I., Mitkevich V.A., Kozin S.A., Yurinskaya M.M., Vinokurov M.G., Serebryakova M.V., Rezvykh A.P., Evgen’ev M.B., Makarov A.A. 2018. Amyloid-β with isomerized Asp7 cytotoxicity is coupled to protein phosphorylation. Sci. Rep. 8, 3518.CrossRefGoogle Scholar
  11. 11.
    Evgen’ev M.B., Krasnov G.S., Nesterova I.V., Garbuz D.G., Karpov V.L., Morozov A.V., Snezhkina A.V., Samokhin A.N., Sergeev A., Kulikov A.M., Bobkova N.V. 2017. Molecular mechanisms underlying neuroprotective effect of intranasal administration of human Hsp70 in mouse model of Alzheimer’s disease. J. Alzheimer’s Dis. 59, 1415–1426.CrossRefGoogle Scholar
  12. 12.
    Bobkova N.V., Evgen’ev M.B., Garbuz D.G., Kulikov A.M., Morozov A.V., Samokhin A.N., Velmeshev D., Medvinskaya N., Nesterova I., Pollock A., Nudler E. 2015. Exogenous Hsp70 delays senescence and improves cognitive function in aging mice. Proc. Natl. Acad. Sci. U. S. A. 112, 16006–16011.CrossRefGoogle Scholar
  13. 13.
    Yurinskaya M.M., Mitkevich V.A., Kozin S.A., Evgen’ev M.B., Makarov A.A., Vinokurov M.G. 2015. HSP70 protects human neuroblastoma cells from apoptosis and oxidative stress induced by amyloid peptide isoAsp7-Aβ(1-42). Cell Death Dis. 6, 336.CrossRefGoogle Scholar
  14. 14.
    Lu R.-C., Tan M.-S., Wang H., Xie A.-M., Yu J.T., Tan L. 2014. Heat shock protein 70 in Alzheimer’s disease. Biomed. Res. Int. 2014, 1–8.Google Scholar
  15. 15.
    Paul S., Mahanta S. 2014. Association of heat-shock proteins in various neurodegenerative disorders: Is it a master key to open the therapeutic door? Mol. Cell. Biochem. 386, 45–61.CrossRefGoogle Scholar
  16. 16.
    Luckow V.A., Lee S.C., Barry G.F., Olins P.O. 1993. Efficient generation of infectious recombinant baculoviruses by site-specific transposon-mediated insertion of foreign genes into a baculovirus genome propagated in Escherichia coli. J. Virol. 67, 4566–4579.Google Scholar
  17. 17.
    Peng Y., Hu Y., Feng N., Wang L., Wang X. 2011. L-3-n-butylphthalide alleviates hydrogen peroxide-induced apoptosis by PKC pathway in human neuroblastoma SK-N-SH cells. Naunyn-Schmiedeberg’s Arch. Pharmacol. 383, 91‒99.CrossRefGoogle Scholar
  18. 18.
    Bloom G.S. 2014. Amyloid-β and tau: The trigger and bullet in Alzheimer disease pathogenesis. JAMA Neurol. 71, 505–508.CrossRefGoogle Scholar
  19. 19.
    Huang H.C., Jiang Z.F. 2009. Accumulated amyloid β‑peptide and hyperphosphorylated tau protein: Relationship and links in Alzheimer’s disease. J. Alzheimer’s Dis. 16, 15–27.CrossRefGoogle Scholar
  20. 20.
    Huang W., Zhang X., Chen W. 2016. Role of oxidative stress in Alzheimer’s disease (review). Biomed. Repts. 4, 519–522.CrossRefGoogle Scholar
  21. 21.
    Stadtman E.R., Levine R.L. 2000. Protein oxidation. Ann. N.Y. Acad. Sci. 899, 191–208.CrossRefGoogle Scholar
  22. 22.
    Castegna A., Aksenov M., Aksenova M., Klein V.T., Pierce W.M., Booze R., Markesbery W.R., Butterfiels A.D. 2002. Proteomic identification of oxidatively modified proteins in Alzheimer’s disease brain: 1. Creatine kinase BB, glutamine synthase, and ubiquitin carboxy-terminal hydrolase. J. Neurochem. 82, 562–571.CrossRefGoogle Scholar
  23. 23.
    Castegna A., Aksenov M., Thongboonkerd V., Klein J.B., Pierce W.M., Booze R., Markesbery W.R., Butterfiels A.D. 2002. Proteomic identification of oxidatively modified proteins in Alzheimer’s disease brain: 2. Dihydropyrimidinase-related protein 2, α-enolase and heat shock cognate 71. J. Neurochem. 82, 1524–1532.CrossRefGoogle Scholar
  24. 24.
    Salminen A., Kauppinen A., Suuronen T., Kaarniranta K., Ojala J. 2009. ER stress in Alzheimer’s disease: A novel neuronal trigger for inflammation and Alzheimer’s pathology. J. Neuroinflam. 6, 1–13.CrossRefGoogle Scholar
  25. 25.
    Seyb K., Ansar S., Bean J., Michaelis M. 2006. β-Amyloid and endoplasmic reticulum stress reponses in primary neurons. J. Mol. Neurosci. 28, 111–123.CrossRefGoogle Scholar
  26. 26.
    Sato S., Fujita N., Tsuruo T. 2002. Regulation of kinase activity of 3-phosphoinositide-dependent protein kinase-1 by binding to 14-3-3. J. Biol. Chem. 277, 39360–39367.CrossRefGoogle Scholar
  27. 27.
    Liu F., Grundke-Iqbal I., Iqbal K., Gong C.X. 2005. Contributions of protein phosphatases PP1, PP2A, PP2B and PP5 to the regulation of tau phosphorylation. Eur. J. Neurosci. 22, 1942–1950.CrossRefGoogle Scholar
  28. 28.
    Swulius M.T., Waxham M.N. 2008. Ca2+/calmodulin-dependent protein kinases. Cell. Mol. Life Sci. 65, 2637–2657.CrossRefGoogle Scholar
  29. 29.
    Colbran R.J. 2004. Protein phosphatases and calcium/calmodulin-dependent protein kinase II-dependent synaptic plasticity. J. Neurosci. 24, 8404–8409.CrossRefGoogle Scholar
  30. 30.
    Hong L., Huang H.C., Jiang Z.F. 2014. Relationship between amyloid-beta and the ubiquitin–proteasome system in Alzheimer’s disease. Neurol. Res. 36, 276–282.CrossRefGoogle Scholar
  31. 31.
    Lopez Salon M., Pasquini L., Besio Moreno M., Pasquini J.M., Soto E. 2003. Relationship between β-amyloid degradation and the 26S proteasome in neural cells. Exp. Neurol. 180, 131–143.CrossRefGoogle Scholar
  32. 32.
    Ramser J., Ahearn M.E., Lenski C., Yariz K.O., Hellebrand H., Rhein., Clark R.D., Shmutzler R.K., Lichtner P., Hoffman E.P., Meindl A., Baumach-Reardon L. 2008. Rare missense and synonymous variants in UBE1 are associated with X-linked infantile spinal muscular atrophy. Am. J. Hum. Genet. 82, 188–193.CrossRefGoogle Scholar
  33. 33.
    Wishart T.M., Mutsaers C.A., Riessland M., Reimer M.M., Hunter G., Hannam M.L., Eaton S.L., Fuller H.R., Roche S.L., Somers E, Morse R., Young P.J., Lamont D.J., Hammerschmidt M., Joshi A., et al. 2014. Dysregulation of ubiquitin homeostasis and β-catenin signaling promote spinal muscular atrophy. J. Clin. Invest. 124, 1821–1834.CrossRefGoogle Scholar
  34. 34.
    Groen E.J.N., Gillingwater T.H. 2015. UBA1: At the crossroads of ubiquitin homeostasis and neurodegeneration. Trends Mol. Med. 21, 622–632.CrossRefGoogle Scholar
  35. 35.
    Vattemi G., Engel W.K., McFerrin J., Askanas V. 2004. Endoplasmic reticulum stress and unfolded protein response in inclusion body myositis muscle. Am. J. Pathol. 164, 1–7.CrossRefGoogle Scholar
  36. 36.
    Grace E., Rabiner C., Busciglio J. 2002. Characterization of neuronal dystrophy induced by fibrillar amyloid β: Implications for Alzheimer’s disease. Neuroscience. 114, 265–273.CrossRefGoogle Scholar
  37. 37.
    Henriques A.G., Vieira S.I., Da Cruz E Silva E.F., Da Cruz e Silva O.A.B. 2010. Aβ promotes Alzheimer’s disease-like cytoskeleton abnormalities with consequences to APP processing in neurons. J. Neurochem. 113, 761–771.CrossRefGoogle Scholar
  38. 38.
    Morris M., Maeda S., Vossel K., Mucke L. 2011. The many faces of tau. Neuron. 70, 410–426.CrossRefGoogle Scholar
  39. 39.
    Vijayan S., El-Akkad E., Grundke-Iqbal I., Iqbal K. 2001. A pool of β-tubulin is hyperphosphorylated at serine residues in Alzheimer disease brain. FEBS Lett. 509, 375–381.CrossRefGoogle Scholar
  40. 40.
    Bobkova N.V., Garbuz D.G., Nesterova I., Medvinskaya N., Samokhin A., Alexandrova I., Yashin V., Karpov V., Kukharsky M.S., Ninkina N.N., Smirnov A.A., Nudler E., Evgen’ev M. 2014. Therapeutic effect of exogenous Hsp70 in mouse models of Alzheimer’s disease. J. Alzheimer’s Dis. 38, 425–435.CrossRefGoogle Scholar
  41. 41.
    Evans C.G., Wisén S., Gestwicki J.E. 2006. Heat shock proteins 70 and 90 inhibit early stages of amyloid β-(1-42) aggregation in vitro. J. Biol. Chem. 281, 33182–33191.CrossRefGoogle Scholar
  42. 42.
    Magrane J. 2004. Heat shock protein 70 participates in the neuroprotective response to intracellularly expressed β‑amyloid in neurons. J. Neurosci. 24, 1700–1706.CrossRefGoogle Scholar
  43. 43.
    Lee Jeong J., Yoo C. 2013. Positive feedback regulation of heat shock protein 70 (Hsp70) is mediated through Toll-like receptor 4-PI3K/Akt-glycogen synthase kinase-3b pathway. Exp. Cell Res. 319, 88–95.CrossRefGoogle Scholar
  44. 44.
    Wang L., Schumann U., Liu Y., Prokopchuk O., Steinacker J.M. 2012. Heat shock protein 70 (Hsp70) inhibits oxidative phosphorylation and compensates ATP balance through enhanced glycolytic activity. J. Appl. Physiol. 113, 1669–1676.CrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Inc. 2018

Authors and Affiliations

  • A. P. Rezvykh
    • 1
  • M. M. Yurinskaya
    • 1
    • 2
  • M. G. Vinokurov
    • 2
  • G. S. Krasnov
    • 1
  • V. A. Mitkevich
    • 1
  • A. A. Makarov
    • 1
  • M. B. Evgen’ev
    • 1
  • O. G. Zatsepina
    • 1
    Email author
  1. 1.Engelhardt Institute of Molecular Biology, Russian Academy of SciencesMoscowRussia
  2. 2.Institute of Cell Biophysics, Russian Academy of SciencesPushchinoRussia

Personalised recommendations