Advertisement

Neurochemical Research

, Volume 44, Issue 12, pp 2695–2707 | Cite as

The Story of Nanoparticles in Differentiation of Stem Cells into Neural Cells

  • Vajihe Asgari
  • Amir Landarani-Isfahani
  • Hossein Salehi
  • Noushin Amirpour
  • Batool Hashemibeni
  • Saghar Rezaei
  • Hamid BahramianEmail author
Review
  • 72 Downloads

Abstract

Stem cells have been long looked at as possible therapeutic vehicles in regenerative medicine largely due to their multi-lineage differentiation potential and paracrine actions. Therefore, development of new procedures for the differentiation of stem cells into different cell types holds great potential for opening new opportunities in regenerative medicine. In addition to various methods for inducing stem cell differentiation, the utilization of nanomaterials for differentiation of stem cells has recently received considerable attention and has become a potential tool for such purpose. Multiple lines of evidence revealed that nanomaterial-based scaffolds, inorganic nanoparticles (NPs), and biodegradable polymers have led to significant progress in regulation of stem cell differentiation. Several studies indicated that different NPs including selenium, gold, graphene quantum dots (QDs) and silica could be employed for the regulation of differentiation of stem cells such as human mesenchymal stem cells (hMSCs). In addition, magnetic core–shell NPs could be applied for the regulation of neural stem cell (NSC) differentiation. Taken together, these findings suggested that NPs are potential candidates which could be utilized for the differentiation of stem cells into various cell types such as neural cells. Herein, we summarized the application of NPs for differentiation of stem cells into various cells in particular neural cells.

Keywords

Nanomaterial Nanoparticles Stem cells Differentiation Neural cells 

Notes

References

  1. 1.
    Rabieian R, Boshtam M, Zareei M, Kouhpayeh S, Masoudifar A, Mirzaei H (2018) Plasminogen activator inhibitor Type-1 as a regulator of fibrosis. J Cell BioChem 119:17–27PubMedGoogle Scholar
  2. 2.
    Moradian Tehrani R, Verdi J, Noureddini M, Salehi R, Salarinia R, Mosalaei M, Simonian M, Alani B, Ghiasi MR, Jaafari MR, Mirzaei HR, Mirzaei H (2018) Mesenchymal stem cells: a new platform for targeting suicide genes in cancer. J Cell Physiol 233:3831–3845PubMedGoogle Scholar
  3. 3.
    Goradel NH, Hour FG, Negahdari B, Malekshahi ZV, Hashemzehi M, Masoudifar A, Mirzaei H (2018) Stem cell therapy: a new therapeutic option for cardiovascular diseases. J Cell BioChem 119:95–104PubMedGoogle Scholar
  4. 4.
    Mohammadi M, Jaafari MR, Mirzaei HR, Mirzaei H (2016) Mesenchymal stem cell: a new horizon in cancer gene therapy. Cancer Gene Ther 23:285–286PubMedGoogle Scholar
  5. 5.
    Meng X, Ichim TE, Zhong J, Rogers A, Yin Z, Jackson J, Wang H, Ge W, Bogin V, Chan KW (2007) Endometrial regenerative cells: a novel stem cell population. J Transl Med 5:57PubMedPubMedCentralGoogle Scholar
  6. 6.
    Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, Jones JM (1998) Embryonic stem cell lines derived from human blastocysts. Science 282:1145–1147Google Scholar
  7. 7.
    Gholamin S, Mirzaei H (2018) GD2-targeted immunotherapy and potential value of circulating microRNAs in neuroblastoma. J Cell Physiol 233:866–879PubMedGoogle Scholar
  8. 8.
    Mirzaei H, Sahebkar A, Avan A, Jaafari MR, Salehi R, Salehi H, Baharvand H, Rezaei A, Hadjati J, Pawelek JM, Mirzaei HR (2016) Application of mesenchymal stem cells in melanoma: a potential therapeutic strategy for delivery of targeted agents. Curr Med Chem 23:455–463PubMedGoogle Scholar
  9. 9.
    Takahashi K, Yamanaka S (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126:663–676PubMedPubMedCentralGoogle Scholar
  10. 10.
    Yu J, Vodyanik MA, Smuga-Otto K, Antosiewicz-Bourget J, Frane JL, Tian S, Nie J, Jonsdottir GA, Ruotti V, Stewart R, Slukvin II, Thomson JA (2007) Induced pluripotent stem cell lines derived from human somatic cells. Science 318:1917–1920PubMedPubMedCentralGoogle Scholar
  11. 11.
    Okita K, Ichisaka T, Yamanaka S (2007) Generation of germline-competent induced pluripotent stem cells. Nature 448:313–317PubMedGoogle Scholar
  12. 12.
    McMurray RJ, Dalby MJ, Tsimbouri PM (2015) Using biomaterials to study stem cell mechanotransduction, growth and differentiation. J Tissue Eng Regen Med 9:528–539PubMedGoogle Scholar
  13. 13.
    Witkowska-Zimny M, Walenko K, Walkiewicz AE, Pojda Z, Przybylski J, Lewandowska-Szumiel M (2012) Effect of substrate stiffness on differentiation of umbilical cord stem cells. Acta Biochim Pol 59:261–264PubMedGoogle Scholar
  14. 14.
    Lee MH, Goralczyk AG, Kriszt R, Ang XM, Badowski C, Li Y, Summers SA, Toh SA, Yassin MS, Shabbir A, Sheppard A, Raghunath M (2016) ECM microenvironment unlocks brown adipogenic potential of adult human bone marrow-derived MSCs. Sci Rep 6:21173PubMedPubMedCentralGoogle Scholar
  15. 15.
    Fathullahzadeh S, Mirzaei H, Honardoost MA, Sahebkar A, Salehi M (2016) Circulating microRNA-192 as a diagnostic biomarker in human chronic lymphocytic leukemia. Cancer Gene Ther 23:327–332PubMedGoogle Scholar
  16. 16.
    Cha C, Liechty WB, Khademhosseini A, Peppas NA (2012) Designing biomaterials to direct stem cell fate. ACS Nano 6:9353–9358PubMedPubMedCentralGoogle Scholar
  17. 17.
    Pullisaar H, Verket A, Szoke K, Tiainen H, Haugen HJ, Brinchmann JE, Reseland JE, Ostrup E (2015) Alginate hydrogel enriched with enamel matrix derivative to target osteogenic cell differentiation in TiO2 scaffolds. J Tissue Eng.  https://doi.org/10.1177/2041731415575870 CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Lee WC, Lim CH, Shi H, Tang LA, Wang Y, Lim CT, Loh KP (2011) Origin of enhanced stem cell growth and differentiation on graphene and graphene oxide. ACS Nano 5:7334–7341PubMedGoogle Scholar
  19. 19.
    Przyborski SA (2005) Differentiation of human embryonic stem cells after transplantation in immune-deficient mice. Stem cells (Dayton, Ohio) 23:1242–1250Google Scholar
  20. 20.
    Wang Y, Yang D, Song L, Li T, Yang J, Zhang X, Le W (2012) Mifepristone-inducible caspase-1 expression in mouse embryonic stem cells eliminates tumor formation but spares differentiated cells in vitro and in vivo. Stem cells (Dayton, Ohio) 30:169–179Google Scholar
  21. 21.
    Daniel M-C, Astruc D (2004) Gold nanoparticles: assembly, supramolecular chemistry, quantum-size-related properties, and applications toward biology, catalysis, and nanotechnology. Chem Rev 104:293–346PubMedGoogle Scholar
  22. 22.
    Iravani S, Korbekandi H, Mirmohammadi SV, Zolfaghari B (2014) Synthesis of silver nanoparticles: chemical, physical and biological methods. Res Pharm Sci 9:385PubMedPubMedCentralGoogle Scholar
  23. 23.
    Hashemi Goradel N, Ghiyami-Hour F, Jahangiri S, Negahdari B, Sahebkar A, Masoudifar A, Mirzaei H (2018) Nanoparticles as new tools for inhibition of cancer angiogenesis. J Cell Physiol 233:2902–2910PubMedGoogle Scholar
  24. 24.
    Singh S, Zafar A, Khan S, Naseem I (2017) Towards therapeutic advances in melanoma management: an overview. Life Sci 174:50–58PubMedGoogle Scholar
  25. 25.
    Mucalo M (2015) Hydroxyapatite (HAp) for biomedical applications. Elsevier, AmsterdamGoogle Scholar
  26. 26.
    Jain A, Ranjan S, Dasgupta N, Ramalingam C (2018) Nanomaterials in food and agriculture: an overview on their safety concerns and regulatory issues. Crit Rev Food Sci Nutr 58:297–317PubMedGoogle Scholar
  27. 27.
    Wolfram J, Zhu M, Yang Y, Shen J, Gentile E, Paolino D, Fresta M, Nie G, Chen C, Shen H (2015) Safety of nanoparticles in medicine. Curr Drug Targets 16:1671–1681PubMedPubMedCentralGoogle Scholar
  28. 28.
    Oberdörster G (2010) Safety assessment for nanotechnology and nanomedicine: concepts of nanotoxicology. J Intern Med 267:89–105PubMedGoogle Scholar
  29. 29.
    Clift MJ, Raemy DO, Endes C, Ali Z, Lehmann AD, Brandenberger C, Petri-Fink A, Wick P, Parak WJ, Gehr P (2013) Can the Ames test provide an insight into nano-object mutagenicity? Investigating the interaction between nano-objects and bacteria. Nanotoxicology 7:1373–1385PubMedGoogle Scholar
  30. 30.
    Dayem AA, Choi HY, Yang GM, Kim K, Saha SK, Kim JH, Cho SG (2016) The potential of nanoparticles in stem cell differentiation and further therapeutic applications. Biotechnol J 11:1550–1560PubMedGoogle Scholar
  31. 31.
    Hadinoto K, Sundaresan A, Cheow WS (2013) Lipid-polymer hybrid nanoparticles as a new generation therapeutic delivery platform: a review. Eur J Pharm Biopharm 85:427–443PubMedGoogle Scholar
  32. 32.
    Parveen S, Misra R, Sahoo SK (2012) Nanoparticles: a boon to drug delivery, therapeutics, diagnostics and imaging. Nanomed Nanotechnol Biol Med 8:147–166Google Scholar
  33. 33.
    Michalet X, Pinaud FF, Bentolila LA, Tsay JM, Doose S, Li JJ, Sundaresan G, Wu AM, Gambhir SS, Weiss S (2005) Quantum dots for live cells, in vivo imaging, and diagnostics. Science (New York, NY) 307:538–544Google Scholar
  34. 34.
    Ghasemi Y, Peymani P, Afifi S (2009) Quantum dot: magic nanoparticle for imaging, detection and targeting. Acta Nio-med 80:156–165Google Scholar
  35. 35.
    Fernandez-Fernandez A, Manchanda R, McGoron AJ (2011) Theranostic applications of nanomaterials in cancer: drug delivery, image-guided therapy, and multifunctional platforms. Appl Biochem Biotechnol 165:1628–1651PubMedPubMedCentralGoogle Scholar
  36. 36.
    Dubertret B, Skourides P, Norris DJ, Noireaux V, Brivanlou AH, Libchaber A (2002) In vivo imaging of quantum dots encapsulated in phospholipid micelles. Science (New York, NY) 298:1759–1762Google Scholar
  37. 37.
    Bailey RE, Nie S (2003) Alloyed semiconductor quantum dots: tuning the optical properties without changing the particle size. J Am Chem Soc 125:7100–7106PubMedGoogle Scholar
  38. 38.
    Chen Z, Ma L, Liu Y, Chen C (2012) Applications of functionalized fullerenes in tumor theranostics. Theranostics 2:238–250PubMedPubMedCentralGoogle Scholar
  39. 39.
    Ma H, Liang X-J (2010) Fullerenes as unique nanopharmaceuticals for disease treatment. Sci China Chem 53:2233–2240Google Scholar
  40. 40.
    Bosi S, Da Ros T, Spalluto G, Prato M (2003) Fullerene derivatives: an attractive tool for biological applications. Eur J Med Chem 38:913–923PubMedGoogle Scholar
  41. 41.
    Hebard AF (1992) Superconductivity in doped fullerenes. Phys Today 45:26–32Google Scholar
  42. 42.
    Kim T, Hyeon T (2013) Applications of inorganic nanoparticles as therapeutic agents. Nanotechnology 25:012001PubMedGoogle Scholar
  43. 43.
    Mishra D, Hubenak JR, Mathur AB (2013) Nanoparticle systems as tools to improve drug delivery and therapeutic efficacy. J Biomed Mater Res, Part A 101:3646–3660Google Scholar
  44. 44.
    De Jong WH, Borm PJ (2008) Drug delivery and nanoparticles:applications and hazards. Int J Nanomed 3:133–149Google Scholar
  45. 45.
    Santo VE, Rodrigues MT, Gomes ME (2013) Contributions and future perspectives on the use of magnetic nanoparticles as diagnostic and therapeutic tools in the field of regenerative medicine. Expert Rev Mol Diagn 13:553–566PubMedGoogle Scholar
  46. 46.
    Morris AS, Adamcakova-Dodd A, Lehman SE, Wongrakpanich A, Thorne PS, Larsen SC, Salem AK (2016) Amine modification of nonporous silica nanoparticles reduces inflammatory response following intratracheal instillation in murine lungs. Toxicol Lett 241:207–215PubMedGoogle Scholar
  47. 47.
    Peñaloza JP, Márquez-Miranda V, Cabaña-Brunod M, Reyes-Ramírez R, Llancalahuen FM, Vilos C, Maldonado-Biermann F, Velásquez LA, Fuentes JA, González-Nilo FD (2017) Intracellular trafficking and cellular uptake mechanism of PHBV nanoparticles for targeted delivery in epithelial cell lines. J Nanobiotechnol 15:1Google Scholar
  48. 48.
    Rauch J, Kolch W, Laurent S, Mahmoudi M (2013) Big signals from small particles: regulation of cell signaling pathways by nanoparticles. Chem Rev 113:3391–3406PubMedGoogle Scholar
  49. 49.
    Venkatachalam K, Wong C-O, Zhu MX (2015) The role of TRPMLs in endolysosomal trafficking and function. Cell Calcium 58:48–56PubMedGoogle Scholar
  50. 50.
    Wong C-O, Gregory S, Hu H, Chao Y, Sepúlveda VE, He Y, Li-Kroeger D, Goldman WE, Bellen HJ, Venkatachalam K (2017) Lysosomal degradation is required for sustained phagocytosis of bacteria by macrophages. Cell Host Microbe 21(719–730):e716Google Scholar
  51. 51.
    Anding AL, Baehrecke EH (2017) Cleaning house: selective autophagy of organelles. Dev Cell 41:10–22PubMedPubMedCentralGoogle Scholar
  52. 52.
    Johnston HJ, Semmler-Behnke M, Brown DM, Kreyling W, Tran L, Stone V (2010) Evaluating the uptake and intracellular fate of polystyrene nanoparticles by primary and hepatocyte cell lines in vitro. Toxicol Appl Pharmacol 242:66–78PubMedGoogle Scholar
  53. 53.
    Moridikia A, Mirzaei H (2018) MicroRNAs: Potential candidates for diagnosis and treatment of colorectal cancer. J Cell Physiol 233:901–913PubMedGoogle Scholar
  54. 54.
    Salarinia R, Sahebkar A, Peyvandi M, Mirzaei HR, Jaafari MR, Riahi MM, Ebrahimnejad H, Nahand JS, Hadjati J, Asrami MO, Fadaei S, Salehi R, Mirzaei H (2016) Epi-Drugs and Epi-miRs: moving beyond current cancer therapies. Curr Cancer Drug Targets 16:773–788PubMedGoogle Scholar
  55. 55.
    Mirzaei H, Momeni F, Saadatpour L, Sahebkar A, Goodarzi M, Masoudifar A, Kouhpayeh S, Salehi H, Mirzaei HR, Jaafari MR (2018) MicroRNA: relevance to stroke diagnosis, prognosis, and therapy. J Cell Physiol 233:856–865PubMedGoogle Scholar
  56. 56.
    Gholamin S, Pasdar A, Khorrami MS, Mirzaei H, Mirzaei HR, Salehi R, Ferns GA, Ghayour-Mobarhan M, Avan A (2016) The potential for circulating microRNAs in the diagnosis of myocardial infarction: a novel approach to disease diagnosis and treatment. Curr Pharm Des 22:397–403PubMedGoogle Scholar
  57. 57.
    Mohammadi M, Goodarzi M, Jaafari MR, Mirzaei HR, Mirzaei H (2016) Circulating microRNA: a new candidate for diagnostic biomarker in neuroblastoma. Cancer Gene Ther 23:371–372PubMedGoogle Scholar
  58. 58.
    Khani P, Nasri F, Khani Chamani F, Saeidi F, Sadri Nahand J, Tabibkhooei A, Mirzaei H (2019) Genetic and epigenetic contribution to astrocytic gliomas pathogenesis. J Neurochem 148:188–203PubMedGoogle Scholar
  59. 59.
    Szuts EZ, Harosi FI (1991) Solubility of retinoids in water. Arch Biochem Biophys 287:297–304PubMedGoogle Scholar
  60. 60.
    Agrawal S, Zhao Q (1998) Antisense therapeutics. Curr Opin Chem Biol 2:519–528PubMedGoogle Scholar
  61. 61.
    Ha SW, Weitzmann MN, Beck GR Jr (2014) Bioactive silica nanoparticles promote osteoblast differentiation through stimulation of autophagy and direct association with LC3 and p62. ACS Nano 8:5898–5910PubMedPubMedCentralGoogle Scholar
  62. 62.
    Chen YS, Hsiue GH (2013) Directing neural differentiation of mesenchymal stem cells by carboxylated multiwalled carbon nanotubes. Biomaterials 34:4936–4944PubMedGoogle Scholar
  63. 63.
    Yi C, Liu D, Fong CC, Zhang J, Yang M (2010) Gold nanoparticles promote osteogenic differentiation of mesenchymal stem cells through p38 MAPK pathway. ACS Nano 4:6439–6448PubMedGoogle Scholar
  64. 64.
    Yang D, Li T, Xu M, Gao F, Yang J, Yang Z, Le W (2014) Graphene oxide promotes the differentiation of mouse embryonic stem cells to dopamine neurons. Nanomedicine (London, England) 9:2445–2455Google Scholar
  65. 65.
    Zhang R, Lee P, Lui VC, Chen Y, Liu X, Lok CN, To M, Yeung KW, Wong KK (2015) Silver nanoparticles promote osteogenesis of mesenchymal stem cells and improve bone fracture healing in osteogenesis mechanism mouse model. Nanomed Nanotechnol Biol Med 11:1949–1959Google Scholar
  66. 66.
    Ilie I, Ilie R, Mocan T, Bartos D, Mocan L (2012) Influence of nanomaterials on stem cell differentiation: designing an appropriate nanobiointerface. Int J Nanomed 7:2211–2225Google Scholar
  67. 67.
    Zhao F, Zhao Y, Liu Y, Chang X, Chen C, Zhao Y (2011) Cellular uptake, intracellular trafficking, and cytotoxicity of nanomaterials. Small 7:1322–1337PubMedGoogle Scholar
  68. 68.
    Ko WK, Heo DN, Moon HJ, Lee SJ, Bae MS, Lee JB, Sun IC, Jeon HB, Park HK, Kwon IK (2015) The effect of gold nanoparticle size on osteogenic differentiation of adipose-derived stem cells. J Colloid Interface Sci 438:68–76PubMedGoogle Scholar
  69. 69.
    Li J, Li JJ, Zhang J, Wang X, Kawazoe N, Chen G (2016) Gold nanoparticle size and shape influence on osteogenesis of mesenchymal stem cells. Nanoscale 8:7992–8007PubMedGoogle Scholar
  70. 70.
    Lv L, Liu Y, Zhang P, Zhang X, Liu J, Chen T, Su P, Li H, Zhou Y (2015) The nanoscale geometry of TiO2 nanotubes influences the osteogenic differentiation of human adipose-derived stem cells by modulating H3K4 trimethylation. Biomaterials 39:193–205PubMedGoogle Scholar
  71. 71.
    Rivera-Gil P, Jimenez de Aberasturi D, Wulf V, Pelaz B, del Pino P, Zhao Y, de la Fuente JM, Ruiz de Larramendi I, Rojo T, Liang XJ, Parak WJ (2013) The challenge to relate the physicochemical properties of colloidal nanoparticles to their cytotoxicity. Acc Chem Res 46:743–749PubMedGoogle Scholar
  72. 72.
    Chithrani BD, Ghazani AA, Chan WC (2006) Determining the size and shape dependence of gold nanoparticle uptake into mammalian cells. Nano Lett 6:662–668PubMedGoogle Scholar
  73. 73.
    Seong JM, Kim BC, Park JH, Kwon IK, Mantalaris A, Hwang YS (2010) Stem cells in bone tissue engineering. Biomed Mater (Bristol, England) 5:062001Google Scholar
  74. 74.
    Li JJ, Kawazoe N, Chen G (2015) Gold nanoparticles with different charge and moiety induce differential cell response on mesenchymal stem cell osteogenesis. Biomaterials 54:226–236PubMedGoogle Scholar
  75. 75.
    Choi SY, Song MS, Ryu PD, Lam AT, Joo SW, Lee SY (2015) Gold nanoparticles promote osteogenic differentiation in human adipose-derived mesenchymal stem cells through the Wnt/beta-catenin signaling pathway. Int J Nanomed 10:4383–4392Google Scholar
  76. 76.
    Ferreira L (2009) Nanoparticles as tools to study and control stem cells. J Cell Biochem 108:746–752PubMedGoogle Scholar
  77. 77.
    Zavan B, Vindigni V, Vezzu K, Zorzato G, Luni C, Abatangelo G, Elvassore N, Cortivo R (2009) Hyaluronan based porous nano-particles enriched with growth factors for the treatment of ulcers: a placebo-controlled study. J Mater Sci: Mater Med 20:235–247Google Scholar
  78. 78.
    Lundqvist M, Stigler J, Elia G, Lynch I, Cedervall T, Dawson KA (2008) Nanoparticle size and surface properties determine the protein corona with possible implications for biological impacts. Proc Natl Acad Sci USA 105:14265–14270PubMedGoogle Scholar
  79. 79.
    Mintzer MA, Simanek EE (2009) Nonviral vectors for gene delivery. Chem Rev 109:259–302PubMedGoogle Scholar
  80. 80.
    Pulavendran S, Rose C, Mandal AB (2011) Hepatocyte growth factor incorporated chitosan nanoparticles augment the differentiation of stem cell into hepatocytes for the recovery of liver cirrhosis in mice. J Nanobiotechnol 9:15Google Scholar
  81. 81.
    Cui ZK, Fan J, Kim S, Bezouglaia O, Fartash A, Wu BM, Aghaloo T, Lee M (2015) Delivery of siRNA via cationic Sterosomes to enhance osteogenic differentiation of mesenchymal stem cells. J Controll Release 217:42–52Google Scholar
  82. 82.
    Maia J, Santos T, Aday S, Agasse F, Cortes L, Malva JO, Bernardino L, Ferreira L (2011) Controlling the neuronal differentiation of stem cells by the intracellular delivery of retinoic acid-loaded nanoparticles. ACS Nano 5:97–106PubMedGoogle Scholar
  83. 83.
    Mirzaei H, Ferns GA, Avan A, Mobarhan MG (2017) Cytokines and MicroRNA in coronary artery disease. Adv Clin Chem 82:47–70PubMedGoogle Scholar
  84. 84.
    Keshavarzi M, Sorayayi S, Jafar Rezaei M, Mohammadi M, Ghaderi A, Rostamzadeh A, Masoudifar A, Mirzaei H (2017) MicroRNAs-based imaging techniques in cancer diagnosis and therapy. J Cell Biochem 118:4121–4128PubMedGoogle Scholar
  85. 85.
    Simonian M, Mosallayi M, Mirzaei H (2018) Circulating miR-21 as novel biomarker in gastric cancer: diagnostic and prognostic biomarker. J Cancer Res Ther 14:475PubMedGoogle Scholar
  86. 86.
    Tavakolizadeh J, Roshanaei K, Salmaninejad A, Yari R, Nahand JS, Sarkarizi HK, Mousavi SM, Salarinia R, Rahmati M, Mousavi SF, Mokhtari R, Mirzaei H (2018) MicroRNAs and exosomes in depression: potential diagnostic biomarkers. J Cell Biochem 119:3783–3797PubMedGoogle Scholar
  87. 87.
    Mirzaei H, Yazdi F, Salehi R, Mirzaei HR (2016) SiRNA and epigenetic aberrations in ovarian cancer. J Cancer Res Ther 12:498–508PubMedGoogle Scholar
  88. 88.
    Mirzaei H, Fathullahzadeh S, Khanmohammadi R, Darijani M, Momeni F, Masoudifar A, Goodarzi M, Mardanshah O, Stenvang J, Jaafari MR, Mirzaei HR (2018) State of the art in microRNA as diagnostic and therapeutic biomarkers in chronic lymphocytic leukemia. J Cell Physiol 233:888–900PubMedGoogle Scholar
  89. 89.
    Mirzaei H, Masoudifar A, Sahebkar A, Zare N, Sadri Nahand J, Rashidi B, Mehrabian E, Mohammadi M, Mirzaei HR, Jaafari MR (2018) MicroRNA: a novel target of curcumin in cancer therapy. J Cell Physiol 233:3004–3015PubMedGoogle Scholar
  90. 90.
    Saeedi Borujeni MJ, Esfandiary E, Taheripak G, Codoner-Franch P, Alonso-Iglesias E, Mirzaei H (2018) Molecular aspects of diabetes mellitus: resistin, microRNA, and exosome. J Cell Biochem 119:1257–1272PubMedGoogle Scholar
  91. 91.
    Jafari SH, Saadatpour Z, Salmaninejad A, Momeni F, Mokhtari M, Nahand JS, Rahmati M, Mirzaei H (2018) Breast cancer diagnosis: Imaging techniques and biochemical markers. J Cell Physiol 233:5200–5213PubMedGoogle Scholar
  92. 92.
    Rashidi B, Hoseini Z, Sahebkar A, Mirzaei H (2017) Anti-atherosclerotic effects of vitamins D and E in suppression of atherogenesis. J Cell Physiol 232:2968–2976PubMedGoogle Scholar
  93. 93.
    Mirzaei H (2017) Stroke in women: risk factors and clinical biomarkers. J Cell Biochem 118:4191–4202PubMedGoogle Scholar
  94. 94.
    Banikazemi Z, Haji HA, Mohammadi M, Taheripak G, Iranifar E, Poursadeghiyan M, Moridikia A, Rashidi B, Taghizadeh M, Mirzaei H (2018) Diet and cancer prevention: dietary compounds, dietary MicroRNAs, and dietary exosomes. J Cell Biochem 119:185–196PubMedGoogle Scholar
  95. 95.
    Hoseini Z, Sepahvand F, Rashidi B, Sahebkar A, Masoudifar A, Mirzaei H (2018) NLRP3 inflammasome: its regulation and involvement in atherosclerosis. J Cell Physiol 233:2116–2132PubMedGoogle Scholar
  96. 96.
    Masoudi MS, Mehrabian E, Mirzaei H (2018) MiR-21: a key player in glioblastoma pathogenesis. J Cell Biochem 119:1285–1290PubMedGoogle Scholar
  97. 97.
    Golabchi K, Soleimani-Jelodar R, Aghadoost N, Momeni F, Moridikia A, Nahand JS, Masoudifar A, Razmjoo H, Mirzaei H (2018) MicroRNAs in retinoblastoma: potential diagnostic and therapeutic biomarkers. J Cell Physiol 233:3016–3023PubMedGoogle Scholar
  98. 98.
    Mashreghi M, Azarpara H, Bazaz MR, Jafari A, Masoudifar A, Mirzaei H (2018) Angiogenesis biomarkers and their targeting ligands as potential targets for tumor angiogenesis. J Cell Physiol 233:2949–2965PubMedGoogle Scholar
  99. 99.
    Nahand JS, Taghizadeh-Boroujeni S, Karimzadeh M, Borran S, Pourhanifeh MH, Moghoofei M, Bokharaei-Salim F, Karampoor S, Jafari A, Asemi Z, Tbibzadeh A, Namdar A, Mirzaei H (2019) microRNAs: New prognostic, diagnostic, and therapeutic biomarkers in cervical cancer. J Cell Physiol 234:17064–17099PubMedGoogle Scholar
  100. 100.
    Aghdam AM, Amiri A, Salarinia R, Masoudifar A, Ghasemi F, Mirzaei H (2019) MicroRNAs as diagnostic, prognostic, and therapeutic biomarkers in prostate cancer. Crit Rev Eukaryot Gene Expr 29:127–139PubMedGoogle Scholar
  101. 101.
    Shabaninejad Z, Yousefi F, Movahedpour A, Ghasemi Y, Dokanehiifard S, Rezaei S, Aryan R, Savardashtaki A, Mirzaei H (2019) Electrochemical-based biosensors for microRNA detection: nanotechnology comes into view. Anal Biochem 581:113349PubMedGoogle Scholar
  102. 102.
    Jamali L, Tofigh R, Tutunchi S, Panahi G, Borhani F, Akhavan S, Nourmohammadi P, Ghaderian SM, Rasouli M, Mirzaei H (2018) Circulating microRNAs as diagnostic and therapeutic biomarkers in gastric and esophageal cancers. J Cell Physiol 233:8538–8550PubMedGoogle Scholar
  103. 103.
    Ferreira R, Fonseca MC, Santos T, Sargento-Freitas J, Tjeng R, Paiva F, Castelo-Branco M, Ferreira LS, Bernardino L (2016) Retinoic acid-loaded polymeric nanoparticles enhance vascular regulation of neural stem cell survival and differentiation after ischaemia. Nanoscale 8:8126–8137PubMedGoogle Scholar
  104. 104.
    Chen X, Gu S, Chen BF, Shen WL, Yin Z, Xu GW, Hu JJ, Zhu T, Li G, Wan C, Ouyang HW, Lee TL, Chan WY (2015) Nanoparticle delivery of stable miR-199a-5p agomir improves the osteogenesis of human mesenchymal stem cells via the HIF1a pathway. Biomaterials 53:239–250PubMedGoogle Scholar
  105. 105.
    Khanna P, Ong C, Bay BH, Baeg GH (2015) Nanotoxicity: an Interplay of Oxidative Stress, Inflammation and Cell Death. Nanomaterials (Basel, Switzerland) 5:1163–1180Google Scholar
  106. 106.
    Qureshi AT, Monroe WT, Dasa V, Gimble JM, Hayes DJ (2013) miR-148b-nanoparticle conjugates for light mediated osteogenesis of human adipose stromal/stem cells. Biomaterials 34:7799–7810PubMedGoogle Scholar
  107. 107.
    Ren M, Han Z, Li J, Feng G, Ouyang S (2015) Ascorbic acid delivered by mesoporous silica nanoparticles induces the differentiation of human embryonic stem cells into cardiomyocytes. Mater Sci Eng C 56:348–355Google Scholar
  108. 108.
    Liu D, He X, Wang K, He C, Shi H, Jian L (2010) Biocompatible silica nanoparticles-insulin conjugates for mesenchymal stem cell adipogenic differentiation. Bioconjug Chem 21:1673–1684PubMedGoogle Scholar
  109. 109.
    Namgung S, Baik KY, Park J, Hong S (2011) Controlling the growth and differentiation of human mesenchymal stem cells by the arrangement of individual carbon nanotubes. ACS Nano 5:7383–7390PubMedGoogle Scholar
  110. 110.
    Crowder SW, Liang Y, Rath R, Park AM, Maltais S, Pintauro PN, Hofmeister W, Lim CC, Wang X, Sung HJ (2013) Poly(epsilon-caprolactone)-carbon nanotube composite scaffolds for enhanced cardiac differentiation of human mesenchymal stem cells. Nanomedicine (London, England) 8:1763–1776Google Scholar
  111. 111.
    Saraiva C, Ferreira L, Bernardino L (2016) Traceable microRNA-124 loaded nanoparticles as a new promising therapeutic tool for Parkinson’s disease. Neurogenesis 3:e1256855PubMedPubMedCentralGoogle Scholar
  112. 112.
    Gu HR, Park SC, Choi SJ, Lee JC, Kim YC, Han CJ, Kim J, Yang KY, Kim YJ, Noh GY, No SH, Jeong JH (2015) Combined treatment with silibinin and either sorafenib or gefitinib enhances their growth-inhibiting effects in hepatocellular carcinoma cells. Clin Mol Hepatol 21:49–59PubMedPubMedCentralGoogle Scholar
  113. 113.
    Li X, Tzeng SY, Liu X, Tammia M, Cheng YH, Rolfe A, Sun D, Zhang N, Green JJ, Wen X, Mao HQ (2016) Nanoparticle-mediated transcriptional modification enhances neuronal differentiation of human neural stem cells following transplantation in rat brain. Biomaterials 84:157–166PubMedPubMedCentralGoogle Scholar
  114. 114.
    Park SJ, Kim S, Kim SY, Jeon NL, Song JM (2017) Highly Efficient and Rapid Neural Differentiation of Mouse Embryonic Stem Cells Based on Retinoic Acid Encapsulated Porous Nanoparticle. ACS Appl Mater Interface 9:34634–34640Google Scholar
  115. 115.
    Simonovic J, Toljic B, Nikolic N, Peric M, Vujin J, Panajotovic R, Gajic R, Bekyarova E, Cataldi A, Parpura V, Milasin J (2018) Differentiation of stem cells from apical papilla into neural lineage using graphene dispersion and single walled carbon nanotubes. J Biomed Mater Res A 106:2653–2661PubMedGoogle Scholar
  116. 116.
    Levy I, Sher I, Corem-Salkmon E, Ziv-Polat O, Meir A, Treves AJ, Nagler A, Kalter-Leibovici O, Margel S, Rotenstreich Y (2015) Bioactive magnetic near Infra-Red fluorescent core-shell iron oxide/human serum albumin nanoparticles for controlled release of growth factors for augmentation of human mesenchymal stem cell growth and differentiation. J Nanobiotechnol 13:34Google Scholar
  117. 117.
    Stephanopoulos N, Freeman R, North HA, Sur S, Jeong SJ, Tantakitti F, Kessler JA, Stupp SI (2015) Bioactive DNA-peptide nanotubes enhance the differentiation of neural stem cells into neurons. Nano Lett 15:603–609PubMedGoogle Scholar
  118. 118.
    Seo HI, Cho AN, Jang J, Kim DW, Cho SW, Chung BG (2015) Thermo-responsive polymeric nanoparticles for enhancing neuronal differentiation of human induced pluripotent stem cells. Nanomed Nanotechnol Biol Med 11:1861–1869Google Scholar
  119. 119.
    Ku B, Kim JE, Chung BH, Chung BG (2013) Retinoic acid-polyethyleneimine complex nanoparticles for embryonic stem cell-derived neuronal differentiation. Langmuir 29:9857–9862PubMedGoogle Scholar
  120. 120.
    Zhang R, Li Y, Hu B, Lu Z, Zhang J, Zhang X (2016) Traceable nanoparticle delivery of small interfering RNA and retinoic acid with temporally release ability to control neural stem cell differentiation for Alzheimer’s Disease Therapy. Adv Mater (Deerfield Beach, Fla) 28:6345–6352Google Scholar
  121. 121.
    Akhavan O, Ghaderi E (2013) Flash photo stimulation of human neural stem cells on graphene/TiO2 heterojunction for differentiation into neurons. Nanoscale 5:10316–10326PubMedGoogle Scholar
  122. 122.
    Park SY, Park J, Sim SH, Sung MG, Kim KS, Hong BH, Hong S (2011) Enhanced differentiation of human neural stem cells into neurons on graphene. Adv Mater (Deerfield Beach, Fla) 23:H263–H267Google Scholar
  123. 123.
    Guo W, Wang S, Yu X, Qiu J, Li J, Tang W, Li Z, Mou X, Liu H, Wang Z (2016) Construction of a 3D rGO-collagen hybrid scaffold for enhancement of the neural differentiation of mesenchymal stem cells. Nanoscale 8:1897–1904PubMedGoogle Scholar
  124. 124.
    Glaser T, Bueno VB, Cornejo DR, Petri DF, Ulrich H (2015) Neuronal adhesion, proliferation and differentiation of embryonic stem cells on hybrid scaffolds made of xanthan and magnetite nanoparticles. Biomed Mater (Bristol, England) 10:045002Google Scholar
  125. 125.
    Bostancioglu RB, Gurbuz M, Akyurekli AG, Dogan A, Koparal AS, Koparal AT (2017) Adhesion profile and differentiation capacity of human adipose tissue derived mesenchymal stem cells grown on metal ion (Zn, Ag and Cu) doped hydroxyapatite nano-coated surfaces. Colloids Surf B 155:415–428Google Scholar
  126. 126.
    Qin H, Zhu C, An Z, Jiang Y, Zhao Y, Wang J, Liu X, Hui B, Zhang X, Wang Y (2014) Silver nanoparticles promote osteogenic differentiation of human urine-derived stem cells at noncytotoxic concentrations. Int J Nanomed 9:2469–2478Google Scholar
  127. 127.
    Wang Q, Chen B, Cao M, Sun J, Wu H, Zhao P, Xing J, Yang Y, Zhang X, Ji M, Gu N (2016) Response of MAPK pathway to iron oxide nanoparticles in vitro treatment promotes osteogenic differentiation of hBMSCs. Biomaterials 86:11–20PubMedGoogle Scholar
  128. 128.
    Wu G, Feng C, Hui G, Wang Z, Tan J, Luo L, Xue P, Wang Q, Chen X (2016) Improving the osteogenesis of rat mesenchymal stem cells by chitosan-based-microRNA nanoparticles. Carbohyd Polym 138:49–58Google Scholar
  129. 129.
    Logan N, Sherif A, Cross AJ, Collins SN, Traynor A, Bozec L, Parkin IP, Brett P (2015) TiO2-coated CoCrMo: improving the osteogenic differentiation and adhesion of mesenchymal stem cells in vitro. J Biomed Mater Res, Part A 103:1208–1217Google Scholar
  130. 130.
    Nayak TR, Andersen H, Makam VS, Khaw C, Bae S, Xu X, Ee PL, Ahn JH, Hong BH, Pastorin G, Ozyilmaz B (2011) Graphene for controlled and accelerated osteogenic differentiation of human mesenchymal stem cells. ACS Nano 5:4670–4678PubMedGoogle Scholar
  131. 131.
    Luo Y, Shen H, Fang Y, Cao Y, Huang J, Zhang M, Dai J, Shi X, Zhang Z (2015) Enhanced proliferation and osteogenic differentiation of mesenchymal stem cells on graphene oxide-incorporated electrospun poly(lactic-co-glycolic acid) nanofibrous mats. ACS Appl Mater Interfaces 7:6331–6339PubMedGoogle Scholar
  132. 132.
    Akhavan O, Ghaderi E, Shahsavar M (2013) Graphene nanogrids for selective and fast osteogenic differentiation of human mesenchymal stem cells. Carbon 59:200–211Google Scholar
  133. 133.
    Nayak TR, Jian L, Phua LC, Ho HK, Ren Y, Pastorin G (2010) Thin films of functionalized multiwalled carbon nanotubes as suitable scaffold materials for stem cells proliferation and bone formation. ACS Nano 4:7717–7725PubMedGoogle Scholar
  134. 134.
    Ravichandran R, Venugopal JR, Sundarrajan S, Mukherjee S, Ramakrishna S (2012) Precipitation of nanohydroxyapatite on PLLA/PBLG/Collagen nanofibrous structures for the differentiation of adipose derived stem cells to osteogenic lineage. Biomaterials 33:846–855PubMedGoogle Scholar
  135. 135.
    Qiu J, Li D, Mou X, Li J, Guo W, Wang S, Yu X, Ma B, Zhang S, Tang W, Sang Y, Gil PR, Liu H (2016) Effects of Graphene Quantum dots on the self-renewal and differentiation of mesenchymal stem cells. Adv Healthcare Mater 5:702–710Google Scholar
  136. 136.
    Sridhar S, Venugopal JR, Sridhar R, Ramakrishna S (2015) Cardiogenic differentiation of mesenchymal stem cells with gold nanoparticle loaded functionalized nanofibers. Colloids Surf B 134:346–354Google Scholar
  137. 137.
    Ravichandran R, Sridhar R, Venugopal JR, Sundarrajan S, Mukherjee S, Ramakrishna S (2014) Gold nanoparticle loaded hybrid nanofibers for cardiogenic differentiation of stem cells for infarcted myocardium regeneration. Macromol Biosci 14:515–525PubMedGoogle Scholar
  138. 138.
    Xue D, Zheng Q, Zong C, Li Q, Li H, Qian S, Zhang B, Yu L, Pan Z (2010) Osteochondral repair using porous poly(lactide-co-glycolide)/nano-hydroxyapatite hybrid scaffolds with undifferentiated mesenchymal stem cells in a rat model. J Biomed Mater Res Part A 94:259–270Google Scholar
  139. 139.
    Wise JK, Yarin AL, Megaridis CM, Cho M (2009) Chondrogenic differentiation of human mesenchymal stem cells on oriented nanofibrous scaffolds: engineering the superficial zone of articular cartilage. Tissue Eng Part A 15:913–921PubMedGoogle Scholar
  140. 140.
    Spadaccio C, Rainer A, Trombetta M, Vadalá G, Chello M, Covino E, Denaro V, Toyoda Y, Genovese JA (2009) Poly-L-lactic acid/hydroxyapatite electrospun nanocomposites induce chondrogenic differentiation of human MSC. Ann Biomed Eng 37:1376–1389PubMedGoogle Scholar
  141. 141.
    Lee JH, Shim W, Choolakadavil Khalid N, Kang WS, Lee M, Kim HS, Choi J, Lee G, Kim JH (2015) Random networks of single-walled carbon nanotubes promote mesenchymal stem cell’s proliferation and differentiation. ACS Appl Mater Interfaces 7:1560–1567PubMedGoogle Scholar
  142. 142.
    Chen W, Tsai PH, Hung Y, Chiou SH, Mou CY (2013) Nonviral cell labeling and differentiation agent for induced pluripotent stem cells based on mesoporous silica nanoparticles. ACS Nano 7:8423–8440PubMedGoogle Scholar
  143. 143.
    Holmes B, Fang X, Zarate A, Keidar M, Zhang LG (2016) Enhanced human bone marrow mesenchymal stem cell chondrogenic differentiation in electrospun constructs with carbon nanomaterials. Carbon 97:1–13Google Scholar
  144. 144.
    Norizadeh-Abbariki T, Mashinchian O, Shokrgozar MA, Haghighipour N, Sen T, Mahmoudi M (2014) Superparamagnetic nanoparticles direct differentiation of embryonic stem cells into skeletal muscle cells. J Biomater Tissue Eng 4:579–585Google Scholar
  145. 145.
    Saraiva C, Praca C, Ferreira R, Santos T, Ferreira L, Bernardino L (2016) Nanoparticle-mediated brain drug delivery: overcoming blood-brain barrier to treat neurodegenerative diseases. J Control Release 235:34–47PubMedGoogle Scholar
  146. 146.
    Cao P, Mooney R, Tirughana R, Abidi W, Aramburo S, Flores L, Gilchrist M, Nwokafor U, Haber T, Tiet P, Annala AJ, Han E, Dellinger T, Aboody KS, Berlin JM (2017) Intraperitoneal administration of neural stem cell-nanoparticle conjugates targets chemotherapy to ovarian tumors. Bioconjug Chem 28:1767–1776PubMedPubMedCentralGoogle Scholar
  147. 147.
    Guimard NK, Gomez N, Schmidt CE (2007) Conducting polymers in biomedical engineering. Prog Polym Sci 32:876–921Google Scholar
  148. 148.
    Park SY, Park J, Sim SH, Sung MG, Kim KS, Hong BH, Hong S (2011) Enhanced differentiation of human neural stem cells into neurons on graphene. Adv Mater 23:H263–H267PubMedGoogle Scholar
  149. 149.
    Defteralı Ç, Verdejo R, Majeed S, Boschetti-de-Fierro A, Méndez-Gómez HR, Díaz-Guerra E, Fierro D, Buhr K, Abetz C, Martínez-Murillo R (2016) In vitro evaluation of biocompatibility of uncoated thermally reduced graphene and carbon nanotube-loaded PVDF membranes with adult neural stem cell-derived neurons and glia. Front Bioeng Biotechnol 4:94PubMedPubMedCentralGoogle Scholar
  150. 150.
    Santos T, Ferreira R, Maia J, Agasse F, Xapelli S, Ls Cortes, Bragança J, Malva JO, Ferreira L, Bernardino L (2012) Polymeric nanoparticles to control the differentiation of neural stem cells in the subventricular zone of the brain. ACS Nano 6:10463–10474PubMedGoogle Scholar
  151. 151.
    Baranes K, Shevach M, Shefi O, Dvir T (2015) Gold nanoparticle-decorated scaffolds promote neuronal differentiation and maturation. Nano Lett 16:2916–2920PubMedGoogle Scholar
  152. 152.
    He W, Bellamkonda RV (2005) Nanoscale neuro-integrative coatings for neural implants. Biomaterials 26:2983–2990PubMedGoogle Scholar
  153. 153.
    Chao T-I, Xiang S, Chen C-S, Chin W-C, Nelson A, Wang C, Lu J (2009) Carbon nanotubes promote neuron differentiation from human embryonic stem cells. Biochem Biophys Res Commun 384:426–430PubMedGoogle Scholar
  154. 154.
    Chao TI, Xiang S, Lipstate JF, Wang C, Lu J (2010) Poly (methacrylic acid)-grafted carbon nanotube scaffolds enhance differentiation of hESCs into neuronal cells. Adv Mater 22:3542–3547PubMedGoogle Scholar
  155. 155.
    Sridharan I, Kim T, Wang R (2009) Adapting collagen/CNT matrix in directing hESC differentiation. Biochem Biophys Res Commun 381:508–512PubMedPubMedCentralGoogle Scholar
  156. 156.
    Chen W, Tsai P-H, Hung Y, Chiou S-H, Mou C-Y (2013) Nonviral cell labeling and differentiation agent for induced pluripotent stem cells based on mesoporous silica nanoparticles. ACS Nano 7:8423–8440PubMedGoogle Scholar
  157. 157.
    Chen G-Y, Pang D-P, Hwang S-M, Tuan H-Y, Hu Y-C (2012) A graphene-based platform for induced pluripotent stem cells culture and differentiation. Biomaterials 33:418–427PubMedGoogle Scholar
  158. 158.
    Chung C-Y, Yang J-T, Kuo Y-C (2013) Polybutylcyanoacrylate nanoparticle-mediated neurotrophin-3 gene delivery for differentiating iPS cells into neurons. Biomaterials 34:5562–5570PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Vajihe Asgari
    • 1
  • Amir Landarani-Isfahani
    • 2
  • Hossein Salehi
    • 1
  • Noushin Amirpour
    • 1
  • Batool Hashemibeni
    • 1
  • Saghar Rezaei
    • 1
  • Hamid Bahramian
    • 1
    Email author
  1. 1.Department of Anatomical Sciences, Faculty of MedicineIsfahan University of Medical SciencesIsfahanIran
  2. 2.Department of ChemistryUniversity of IsfahanIsfahanIran

Personalised recommendations