Skip to main content

Advertisement

Log in

Enhancement of Neural Stem Cell Survival, Proliferation, Migration, and Differentiation in a Novel Self-Assembly Peptide Nanofibber Scaffold

  • Published:
Molecular Neurobiology Aims and scope Submit manuscript

A Correction to this article was published on 06 June 2023

This article has been updated

Abstract

Considerable efforts have been made to combine biologically active molecules into the self-assembling peptide in order to improve cells growth, survival, and differentiation. In this study, a novel three-dimensional scaffold (RADA4GGSIKVAV; R-GSIK) was designed by adding glycine and serine between RADA4 and IKVAV to promote the strength of the peptide. The cell adhesion, viability, proliferation, migration, and differentiation of rat embryonic neural stem cells (NSCs) in R-GSIK were investigated and compared to laminin-coated, two-dimensional, and Puramatrix cultures. The scanning electron microscopy studies of the R-GSIK showed an open porous structure and a suitable surface area available for cell interaction. R-GSIK promoted the cell adhesion, viability, proliferation, and migration compared to the other cultures. In addition, the R-GSIK enhanced NSCs differentiation into neuronal cells. The NSCs injected in R-GSIK had a lower glial differentiation rate than in the Puramatrix. The results suggest that R-GSIK holds great promise for cell therapies and neuronal tissue repair.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

Change history

References

  1. Kothapalli CR, Kamm RD (2013) 3D matrix microenvironment for targeted differentiation of embryonic stem cells into neural and glial lineages. Biomaterials 34(25):5995–6007. doi:10.1016/j.biomaterials.2013.04.042

    Article  CAS  PubMed  Google Scholar 

  2. Egawa EY, Kato K, Hiraoka M, Nakaji-Hirabayashi T, Iwata H (2011) Enhanced proliferation of neural stem cells in a collagen hydrogel incorporating engineered epidermal growth factor. Biomaterials 32(21):4737–4743. doi:10.1016/j.biomaterials.2011.03.033

    Article  CAS  PubMed  Google Scholar 

  3. Xie H, Li J, Li L, Dong Y, Chen G-Q, Chen KC (2013) Enhanced proliferation and differentiation of neural stem cells grown on PHA films coated with recombinant fusion proteins. Acta Biomater 9(8):7845–7854. doi:10.1016/j.actbio.2013.04.038

    Article  CAS  PubMed  Google Scholar 

  4. Leipzig ND, Wylie RG, Kim H, Shoichet MS (2011) Differentiation of neural stem cells in three-dimensional growth factor-immobilized chitosan hydrogel scaffolds. Biomaterials 32(1):57–64. doi:10.1016/j.biomaterials.2010.09.031

    Article  CAS  PubMed  Google Scholar 

  5. Narmoneva DA, Oni O, Sieminski AL, Zhang S, Gertler JP, Kamm RD, Lee RT (2005) Self-assembling short oligopeptides and the promotion of angiogenesis. Biomaterials 26(23):4837–4846. doi:10.1016/j.biomaterials.2005.01.005

    Article  CAS  PubMed  Google Scholar 

  6. Raghavan S, Gilmont RR, Bitar KN (2013) Neuroglial differentiation of adult enteric neuronal progenitor cells as a function of extracellular matrix composition. Biomaterials 34(28):6649–6658. doi:10.1016/j.biomaterials.2013.05.023

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Colognato H, Yurchenco PD (2000) Form and function: the laminin family of heterotrimers. Dev Dyn 218(2):213–234. doi:10.1002/(sici)1097-0177(200006)218:2<213::aid-dvdy1>3.0.co;2-r

    Article  CAS  PubMed  Google Scholar 

  8. Jung SY, Kim JM, Min SK, Kim OB, Jang DH, Kang HK, Min BM (2012) The potential of laminin-2-biomimetic short peptide to promote cell adhesion, spreading and migration by inducing membrane recruitment and phosphorylation of PKCdelta. Biomaterials 33(15):3967–3979. doi:10.1016/j.biomaterials.2012.02.002

    Article  CAS  PubMed  Google Scholar 

  9. Cheng T-Y, Chen M-H, Chang W-H, Huang M-Y, Wang T-W (2013) Neural stem cells encapsulated in a functionalized self-assembling peptide hydrogel for brain tissue engineering. Biomaterials 34(8):2005–2016. doi:10.1016/j.biomaterials.2012.11.043

    Article  CAS  PubMed  Google Scholar 

  10. Cunha C, Panseri S, Villa O, Silva D, Gelain F (2011) 3D culture of adult mouse neural stem cells within functionalized self-assembling peptide scaffolds. Int J Nanomedicine 6:943–955. doi:10.2147/IJN.S17292

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Ringler P, Schulz GE (2003) Self-assembly of proteins into designed networks. Science 302(5642):106–109. doi:10.1126/science.1088074

    Article  CAS  PubMed  Google Scholar 

  12. Patterson J, Martino MM, Hubbell JA (2010) Biomimetic materials in tissue engineering. Mater Today 13(1):14–22. doi:10.1016/S1369-7021(10)70013-4

    Article  CAS  Google Scholar 

  13. Gelain F, Bottai D, Vescovi A, Zhang S (2006) Designer self-assembling peptide nanofiber scaffolds for adult mouse neural stem cell 3-dimensional cultures. PLoS One 1(1):e119. doi:10.1371/journal.pone.0000119

    Article  PubMed  PubMed Central  Google Scholar 

  14. Bokhari MA, Akay G, Zhang S, Birch MA (2005) The enhancement of osteoblast growth and differentiation in vitro on a peptide hydrogel—polyHIPE polymer hybrid material. Biomaterials 26(25):5198–5208. doi:10.1016/j.biomaterials.2005.01.040

    Article  CAS  PubMed  Google Scholar 

  15. Zhang ZX, Zheng QX, Wu YC, Hao DJ (2010) Compatibility of neural stem cells with functionalized self-assembling peptide scaffold in vitro. Biotechnol Bioprocess Eng 15(4):545–551. doi:10.1007/s12257-009-3076-2

    Article  CAS  Google Scholar 

  16. Azari H, Sharififar S, Rahman M, Ansari S, Reynolds BA (2011) Establishing embryonic mouse neural stem cell culture using the neurosphere assay. J Vis Exp: JoVE 47. doi:10.3791/2457

  17. Xu CY, Inai R, Kotaki M, Ramakrishna S (2004) Aligned biodegradable nanofibrous structure: a potential scaffold for blood vessel engineering. Biomaterials 25(5):877–886. doi:10.1016/S0142-9612(03)00593-3

    Article  CAS  PubMed  Google Scholar 

  18. Ananthanarayanan B, Little L, Schaffer DV, Healy KE, Tirrell M (2010) Neural stem cell adhesion and proliferation on phospholipid bilayers functionalized with RGD peptides. Biomaterials 31(33):8706–8715. doi:10.1016/j.biomaterials.2010.07.104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Aligholi H, Rezayat SM, Azari H, Mehr SE, Akbari M, Mousavi SMM, Attari F, Alipour F et al (2016) Preparing neural stem/progenitor cells in PuraMatrix hydrogel for transplantation after brain injury in rats: a comparative methodological study. Brain Res 1642:197–208. doi:10.1016/j.brainres.2016.03.043

    Article  CAS  PubMed  Google Scholar 

  20. Zou Z, Liu T, Li J, Li P, Ding Q, Peng G, Zheng Q, Zeng X et al (2014) Biocompatibility of functionalized designer self-assembling nanofiber scaffolds containing FRM motif for neural stem cells. J Biomed Mater Res A 102(5):1286–1293. doi:10.1002/jbm.a.34804

    Article  PubMed  Google Scholar 

  21. Moore SW, Sheetz MP (2011) Biophysics of substrate interaction: influence on neural motility, differentiation, and repair. Dev Neurobiol 71(11):1090–1101. doi:10.1002/dneu.20947

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Aoshiba K, Rennard SI, Spurzem JR (1997) Cell-matrix and cell-cell interactions modulate apoptosis of bronchial epithelial cells. Am J Physiol Lung Cell Mol Physiol 272(1):L28–L37

    CAS  Google Scholar 

  23. Ma Z, Kotaki M, Inai R, Ramakrishna S (2005) Potential of nanofiber matrix as tissue-engineering scaffolds. Tissue Eng 11(1–2):101–109. doi:10.1089/ten.2005.11.101

    Article  PubMed  Google Scholar 

  24. Horii A, Wang X, Gelain F, Zhang S (2007) Biological designer self-assembling peptide nanofiber scaffolds significantly enhance osteoblast proliferation, differentiation and 3-D migration. PLoS One 2(2):e190. doi:10.1371/journal.pone.0000190

    Article  PubMed  PubMed Central  Google Scholar 

  25. Moradi F, Bahktiari M, Joghataei MT, Nobakht M, Soleimani M, Hasanzadeh G, Fallah A, Zarbakhsh S et al (2012) BD PuraMatrix peptide hydrogel as a culture system for human fetal Schwann cells in spinal cord regeneration. J Neurosci Res 90(12):2335–2348. doi:10.1002/jnr.23120

    Article  CAS  PubMed  Google Scholar 

  26. Sun Y, Li W, Wu X, Zhang N, Zhang Y, Ouyang S, Song X, Fang X et al (2016) Functional self-assembling peptide nanofiber hydrogels designed for nerve degeneration. ACS Appl Mater Interfaces 8(3):2348–2359. doi:10.1021/acsami.5b11473

    Article  CAS  PubMed  Google Scholar 

  27. Harunaga JS, Yamada KM (2011) Cell-matrix adhesions in 3D. Matrix Biol 30(7):363–368. doi:10.1016/j.matbio.2011.06.001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Li Y-C, Liao Y-T, Chang H-H, Young T-H (2013) Covalent bonding of GYIGSR to EVAL membrane surface to improve migration and adhesion of cultured neural stem/precursor cells. Colloids Surf B Biointerfaces 102:53–62. doi:10.1016/j.colsurfb.2012.08.054

    Article  CAS  PubMed  Google Scholar 

  29. Flanagan LA, Rebaza LM, Derzic S, Schwartz PH, Monuki ES (2006) Regulation of human neural precursor cells by laminin and integrins. J Neurosci Res 83(5):845–856. doi:10.1002/jnr.20778

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Sahab Negah S, Aligholi H, Khaksar Z, Kazemi H, Modarres Mousavi SM, Safahani M, Barati Dowom P, Gorji A (2016) Survival, proliferation, and migration of human meningioma stem-like cells in a nanopeptide scaffold. Iran J Basic Med Sci 19(12):1271–1278

  31. Taraballi F, Natalello A, Campione M, Villa O, Doglia SM, Paleari A, Gelain F (2010) Glycine-spacers influence functional motifs exposure and self-assembling propensity of functionalized substrates tailored for neural stem cell cultures. Front Neuroeng 3:1. doi:10.3389/neuro.16.001.2010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Song Y, Li Y, Zheng Q, Wu K, Guo X, Wu Y, Yin M, Wu Q et al (2011) Neural progenitor cells survival and neuronal differentiation in peptide-based hydrogels. J Biomater Sci Polym Ed 22(4–6):475–487. doi:10.1163/092050610X487756

    Article  CAS  PubMed  Google Scholar 

  33. Silva GA (2006) Neuroscience nanotechnology: progress, opportunities and challenges. Nat Rev Neurosci 7(1):65–74. doi:10.1038/nrn1827

    Article  CAS  PubMed  Google Scholar 

  34. Semino CE, Merok JR, Crane GG, Panagiotakos G, Zhang S (2003) Functional differentiation of hepatocyte-like spheroid structures from putative liver progenitor cells in three-dimensional peptide scaffolds. Differentiation 71(4–5):262–270. doi:10.1046/j.1432-0436.2003.7104503.x

    Article  CAS  PubMed  Google Scholar 

  35. Li Q, Cheung WH, Chow KL, Ellis-Behnke RG, Chau Y (2012) Factorial analysis of adaptable properties of self-assembling peptide matrix on cellular proliferation and neuronal differentiation of pluripotent embryonic carcinoma. Nanomedicine 8(5):748–756. doi:10.1016/j.nano.2011.09.001

    Article  CAS  PubMed  Google Scholar 

  36. Silva GA, Czeisler C, Niece KL, Beniash E, Harrington DA, Kessler JA, Stupp SI (2004) Selective differentiation of neural progenitor cells by high-epitope density nanofibers. Science 303(5662):1352–1355. doi:10.1126/science.1093783

    Article  CAS  PubMed  Google Scholar 

  37. Rabchevsky AG, Smith GM (2001) Therapeutic interventions following mammalian spinal cord injury. Arch Neurol 58(5):721–726. doi:10.1001/archneur.58.5.721

    Article  CAS  PubMed  Google Scholar 

  38. Tavakol S, Saber R, Hoveizi E, Tavakol B, Aligholi H, Ai J, Rezayat SM (2016) Self-assembling peptide nanofiber containing long motif of laminin induces neural differentiation, tubulin polymerization, and neurogenesis: in vitro, ex vivo, and in vivo studies. Mol Neurobiol 53(8):5288–5299. doi:10.1007/s12035-015-9448-z

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by the Shefa Neuroscience Center, Tehran, Iran, grant related to Dr-Thesis 31528 and Iran National Science Foundation, Tehran, Iran (INSF).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ali Gorji.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Additional information

Sajad Sahab Negah and Zabihollah Khaksar contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sahab Negah, S., Khaksar, Z., Aligholi, H. et al. Enhancement of Neural Stem Cell Survival, Proliferation, Migration, and Differentiation in a Novel Self-Assembly Peptide Nanofibber Scaffold. Mol Neurobiol 54, 8050–8062 (2017). https://doi.org/10.1007/s12035-016-0295-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12035-016-0295-3

Keywords

Navigation