Nanocarrier Mediated siRNA Delivery Targeting Stem Cell Differentiation

Author(s): Fiona Fernandes, Pooja Kotharkar, Adrija Chakravorty, Meenal Kowshik, Indrani Talukdar*

Journal Name: Current Stem Cell Research & Therapy

Volume 15 , Issue 2 , 2020

Become EABM
Become Reviewer

Abstract:

Stem cell-based regenerative medicine holds exceptional therapeutic potential and hence the development of efficient techniques to enhance control over the rate of differentiation has been the focus of active research. One of the strategies to achieve this involves delivering siRNA into stem cells and exploiting the RNA interference (RNAi) mechanism. Transport of siRNA across the cell membrane is a challenge due to its anionic property, especially in primary human cells and stem cells. Moreover, naked siRNA incites immune responses, may cause off-target effects, exhibits low stability and is easily degraded by endonucleases in the bloodstream. Although siRNA delivery using viral vectors and electroporation has been used in stem cells, these methods demonstrate low transfection efficiency, cytotoxicity, immunogenicity, events of integration and may involve laborious customization. With the advent of nanotechnology, nanocarriers which act as novel gene delivery vehicles designed to overcome the problems associated with safety and practicality are being developed. The various nanomaterials that are currently being explored and discussed in this review include liposomes, carbon nanotubes, quantum dots, protein and peptide nanocarriers, magnetic nanoparticles, polymeric nanoparticles, etc. These nanodelivery agents exhibit advantages such as low immunogenic response, biocompatibility, design flexibility allowing for surface modification and functionalization, and control over the surface topography for achieving the desired rate of siRNA delivery and improved gene knockdown efficiency. This review also includes discussion on siRNA co-delivery with imaging agents, plasmid DNA, drugs etc. to achieve combined diagnostic and enhanced therapeutic functionality, both for in vitro and in vivo applications.

Keywords: Stem cell, differentiation, nanoparticles, nanocarriers, transfection, siRNA, regenerative medicine.

[1]
Bianco P, Robey PG. Stem cells in tissue engineering. Nature 2001; 414(6859): 118-21.
[http://dx.doi.org/10.1038/35102181] [PMID: 11689957]
[2]
Biehl JK, Russell B. Introduction to stem cell therapy. J Cardiovasc Nurs 2009; 24(2): 98-103.
[http://dx.doi.org/10.1097/JCN.0b013e318197a6a5] [PMID: 19242274]
[3]
Moon SY, Park YB, Kim D-S, Oh SK, Kim D-W. Generation, culture, and differentiation of human embryonic stem cells for therapeutic applications. Mol Ther 2006; 13(1): 5-14.
[http://dx.doi.org/10.1016/j.ymthe.2005.09.008] [PMID: 16242999]
[4]
Strulovici Y, Leopold PL, O’Connor TP, Pergolizzi RG, Crystal RG. Human embryonic stem cells and gene therapy. Mol Ther 2007; 15(5): 850-66.
[http://dx.doi.org/10.1038/mt.sj.6300125] [PMID: 17356540]
[5]
Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006; 126(4): 663-76.
[http://dx.doi.org/10.1016/j.cell.2006.07.024] [PMID: 16904174]
[6]
Ergünay K. [RNA interference: mechanism and applications]. Mikrobiyol Bul 2004; 38(3): 285-94.
[PMID: 15490850]
[7]
Chaturvedi K, Ganguly K, Kulkarni AR, et al. Cyclodextrin-based siRNA delivery nanocarriers: a state-of-the-art review. Expert Opin Drug Deliv 2011; 8(11): 1455-68.
[http://dx.doi.org/10.1517/17425247.2011.610790] [PMID: 21867463]
[8]
Ying S-Y, Chang DC, Lin S-L. The microRNA (miRNA): overview of the RNA genes that modulate gene function. Mol Biotechnol 2008; 38(3): 257-68.
[http://dx.doi.org/10.1007/s12033-007-9013-8] [PMID: 17999201]
[9]
Dana H, Chalbatani GM, Mahmoodzadeh H, et al. Molecular mechanisms and biological functions of siRNA. Int J Biomed Sci 2017; 13(2): 48-57.
[PMID: 28824341]
[10]
Li Z, Rana TM. Molecular mechanisms of RNA-triggered gene silencing machineries. Acc Chem Res 2012; 45(7): 1122-31.
[http://dx.doi.org/10.1021/ar200253u] [PMID: 22304792]
[11]
Mohr SE, Perrimon N. RNAi screening: new approaches, understandings, and organisms. Wiley Interdiscip Rev RNA 2012; 3(2): 145-58.
[http://dx.doi.org/10.1002/wrna.110] [PMID: 21953743]
[12]
Brummelkamp TR, Bernards R, Agami R. A system for stable expression of short interfering RNAs in mammalian cells. Science 2002; 296(5567): 550-3.
[http://dx.doi.org/10.1126/science.1068999] [PMID: 11910072]
[13]
Kumar LD, Clarke AR. Gene manipulation through the use of small interfering RNA (siRNA): from in vitro to in vivo applications. Adv Drug Deliv Rev 2007; 59(2-3): 87-100.
[http://dx.doi.org/10.1016/j.addr.2007.03.009] [PMID: 17434644 ]
[14]
Gao Y, Liu X-L, Li X-R. Research progress on siRNA delivery with nonviral carriers. Int J Nanomedicine 2011; 6: 1017-25.
[http://dx.doi.org/10.2147/IJN.S17040] [PMID: 21720513]
[15]
Lee SJ, Son S, Yhee JY, et al. Structural modification of siRNA for efficient gene silencing. Biotechnol Adv 2013; 31(5): 491-503.
[http://dx.doi.org/10.1016/j.biotechadv.2012.09.002] [PMID: 22985697]
[16]
Tomar RS, Matta H, Chaudhary PM. Use of adeno-associated viral vector for delivery of small interfering RNA. Oncogene 2003; 22(36): 5712-5.
[http://dx.doi.org/10.1038/sj.onc.1206733] [PMID: 12944921]
[17]
Zaehres H, Lensch MW, Daheron L, Stewart SA, Itskovitz-Eldor J, Daley GQ. High-efficiency RNA interference in human embryonic stem cells. Stem Cells 2005; 23(3): 299-305.
[http://dx.doi.org/10.1634/stemcells.2004-0252] [PMID: 15749924]
[18]
Rubinson DA, Dillon CP, Kwiatkowski AV, et al. A lentivirus-based system to functionally silence genes in primary mammalian cells, stem cells and transgenic mice by RNA interference. Nat Genet 2003; 33(3): 401-6.
[http://dx.doi.org/10.1038/ng1117] [PMID: 12590264]
[19]
Chirmule N, Propert K, Magosin S, Qian Y, Qian R, Wilson J. Immune responses to adenovirus and adeno-associated virus in humans. Gene Ther 1999; 6(9): 1574-83.
[http://dx.doi.org/10.1038/sj.gt.3300994] [PMID: 10490767]
[20]
Kafri T, Morgan D, Krahl T, Sarvetnick N, Sherman L, Verma I. Cellular immune response to adenoviral vector infected cells does not require de novo viral gene expression: implications for gene therapy. Proc Natl Acad Sci USA 1998; 95(19): 11377-82.
[http://dx.doi.org/10.1073/pnas.95.19.11377] [PMID: 9736744]
[21]
Lehrman S. Virus treatment questioned after gene therapy death. Nature 1999; 401(6753): 517-8.
[http://dx.doi.org/10.1038/43977] [PMID: 10524611]
[22]
Shen C, Buck AK, Liu X, Winkler M, Reske SN. Gene silencing by adenovirus-delivered siRNA. FEBS Lett 2003; 539(1-3): 111-4.
[http://dx.doi.org/10.1016/S0014-5793(03)00209-6] [PMID: 12650936]
[23]
Hamm A, Krott N, Breibach I, Blindt R, Bosserhoff AK. Efficient transfection method for primary cells. Tissue Eng 2002; 8(2): 235-45.
[http://dx.doi.org/10.1089/107632702753725003] [PMID: 12031113]
[24]
Huang H, Wei Z, Huang Y, et al. An efficient and high-throughput electroporation microchip applicable for siRNA delivery. Lab Chip 2011; 11(1): 163-72.
[http://dx.doi.org/10.1039/C0LC00195C] [PMID: 20957267]
[25]
Wiese M, Castiglione K, Hensel M, Schleicher U, Bogdan C, Jantsch J. Small interfering RNA (siRNA) delivery into murine bone marrow-derived macrophages by electroporation. J Immunol Methods 2010; 353(1-2): 102-10.
[http://dx.doi.org/10.1016/j.jim.2009.12.002] [PMID: 20006615]
[26]
Prechtel AT, Turza NM, Theodoridis AA, Kummer M, Steinkasserer A. Small interfering RNA (siRNA) delivery into monocyte-derived dendritic cells by electroporation. J Immunol Methods 2006; 311(1-2): 139-52.
[http://dx.doi.org/10.1016/j.jim.2006.01.021] [PMID: 16556448]
[27]
Moore JC, Atze K, Yeung PL, et al. Efficient, high-throughput transfection of human embryonic stem cells. Stem Cell Res Ther 2010; 1(3): 23.
[http://dx.doi.org/10.1186/scrt23] [PMID: 20659329]
[28]
Gao K, Huang L. Nonviral methods for siRNA delivery. Mol Pharm 2009; 6(3): 651-8.
[http://dx.doi.org/10.1021/mp800134q] [PMID: 19115957]
[29]
Yin H, Kanasty RL, Eltoukhy AA, Vegas AJ, Dorkin JR, Anderson DG. Non-viral vectors for gene-based therapy. Nat Rev Genet 2014; 15(8): 541-55.
[http://dx.doi.org/10.1038/nrg3763] [PMID: 25022906]
[30]
Kesharwani P, Gajbhiye V, Jain NK. A review of nanocarriers for the delivery of small interfering RNA. Biomaterials 2012; 33(29): 7138-50.
[http://dx.doi.org/10.1016/j.biomaterials.2012.06.068] [PMID: 22796160]
[31]
Tatiparti K, Sau S, Kashaw SK, Iyer AK. siRNA delivery strategies: a comprehensive review of recent developments. Nanomaterials (Basel) 2017; 7(4): 77.
[http://dx.doi.org/10.3390/nano7040077] [PMID: 28379201]
[32]
Singh R, Lillard JW Jr. Nanoparticle-based targeted drug delivery. Exp Mol Pathol 2009; 86(3): 215-23.
[http://dx.doi.org/10.1016/j.yexmp.2008.12.004] [PMID: 19186176]
[33]
Solanki A, Kim J D, Lee K-B. Nanotechnology for regenerative medicine: nanomaterials for stem cell imaging. nanomaterials for stem cell imaging 2008.
[34]
Juliano R, Alam MR, Dixit V, Kang H. Mechanisms and strategies for effective delivery of antisense and siRNA oligonucleotides. Nucleic Acids Res 2008; 36(12): 4158-71.
[http://dx.doi.org/10.1093/nar/gkn342] [PMID: 18558618]
[35]
Kuhn DA, Vanhecke D, Michen B, et al. Different endocytotic uptake mechanisms for nanoparticles in epithelial cells and macrophages. Beilstein J Nanotechnol 2014; 5(1): 1625-36.
[http://dx.doi.org/10.3762/bjnano.5.174] [PMID: 25383275]
[36]
Sahay G, Alakhova DY, Kabanov AV. Endocytosis of nanomedicines. J Control Release 2010; 145(3): 182-95.
[http://dx.doi.org/10.1016/j.jconrel.2010.01.036] [PMID: 20226220]
[37]
Santos JL, Pandita D, Rodrigues J, Pêgo AP, Granja PL, Tomás H. Non-viral gene delivery to mesenchymal stem cells: methods, strategies and application in bone tissue engineering and regeneration. Curr Gene Ther 2011; 11(1): 46-57.
[http://dx.doi.org/10.2174/156652311794520102] [PMID: 21182464]
[38]
Lakshmipathy U, Pelacho B, Sudo K, et al. Efficient transfection of embryonic and adult stem cells. Stem Cells 2004; 22(4): 531-43.
[http://dx.doi.org/10.1634/stemcells.22-4-531] [PMID: 15277699]
[39]
Riley MK, Vermerris W. Recent advances in nanomaterials for gene delivery—a review. Nanomaterials (Basel) 2017; 7(5): 94.
[http://dx.doi.org/10.3390/nano7050094] [PMID: 28452950]
[40]
Dalby B, Cates S, Harris A, et al. Advanced transfection with Lipofectamine 2000 reagent: primary neurons, siRNA, and high-throughput applications. Methods 2004; 33(2): 95-103.
[http://dx.doi.org/10.1016/j.ymeth.2003.11.023] [PMID: 15121163]
[41]
Torchilin VP. Recent advances with liposomes as pharmaceutical carriers. Nat Rev Drug Discov 2005; 4(2): 145-60.
[http://dx.doi.org/10.1038/nrd1632] [PMID: 15688077]
[42]
Martino S, di Girolamo I, Tiribuzi R, D’Angelo F, Datti A, Orlacchio A. Efficient siRNA delivery by the cationic liposome DOTAP in human hematopoietic stem cells differentiating into dendritic cells. J Biomed Biotechnol 2009; 2009410260
[http://dx.doi.org/10.1155/2009/410260] [PMID: 19503805]
[43]
Cui Z-K, Fan J, Kim S, et al. Delivery of siRNA via cationic Sterosomes to enhance osteogenic differentiation of mesenchymal stem cells. J Control Release 2015; 217: 42-52.
[http://dx.doi.org/10.1016/j.jconrel.2015.08.031] [PMID: 26302903]
[44]
Cui Z-K, Sun JA, Baljon JJ, et al. Simultaneous delivery of hydrophobic small molecules and siRNA using Sterosomes to direct mesenchymal stem cell differentiation for bone repair. Acta Biomater 2017; 58: 214-24.
[http://dx.doi.org/10.1016/j.actbio.2017.05.057] [PMID: 28578107]
[45]
Ramasubramanian A, Shiigi S, Lee GK, Yang F. Non-viral delivery of inductive and suppressive genes to adipose-derived stem cells for osteogenic differentiation. Pharm Res 2011; 28(6): 1328-37.
[http://dx.doi.org/10.1007/s11095-011-0406-9] [PMID: 21424160]
[46]
Yang C, Gao S, Song P, Dagnæs-Hansen F, Jakobsen M, Kjems J. Theranostic Niosomes for Efficient siRNA/MicroRNA Delivery and Activatable Near-Infrared Fluorescent Tracking of Stem Cells. ACS Appl Mater Interfaces 2018; 10(23): 19494-503.
[http://dx.doi.org/10.1021/acsami.8b05513] [PMID: 29767944]
[47]
Hawkins MJ, Soon-Shiong P, Desai N. Protein nanoparticles as drug carriers in clinical medicine. Adv Drug Deliv Rev 2008; 60(8): 876-85.
[http://dx.doi.org/10.1016/j.addr.2007.08.044] [PMID: 18423779]
[48]
Zeineddine D, Papadimou E, Chebli K, et al. Oct-3/4 dose dependently regulates specification of embryonic stem cells toward a cardiac lineage and early heart development. Dev Cell 2006; 11(4): 535-46.
[http://dx.doi.org/10.1016/j.devcel.2006.07.013] [PMID: 17011492]
[49]
Crombez L, Aldrian-Herrada G, Konate K, et al. A new potent secondary amphipathic cell-penetrating peptide for siRNA delivery into mammalian cells. Mol Ther 2009; 17(1): 95-103.
[http://dx.doi.org/10.1038/mt.2008.215] [PMID: 18957965]
[50]
Eguchi A, Meade BR, Chang Y-C, et al. Efficient siRNA delivery into primary cells by a peptide transduction domain-dsRNA binding domain fusion protein. Nat Biotechnol 2009; 27(6): 567-71.
[http://dx.doi.org/10.1038/nbt.1541] [PMID: 19448630]
[51]
Patil Y, Panyam J. Polymeric nanoparticles for siRNA delivery and gene silencing. Int J Pharm 2009; 367(1-2): 195-203.
[http://dx.doi.org/10.1016/j.ijpharm.2008.09.039] [PMID: 18940242]
[52]
Lungwitz U, Breunig M, Blunk T, Göpferich A. Polyethylenimine-based non-viral gene delivery systems. Eur J Pharm Biopharm 2005; 60(2): 247-66.
[http://dx.doi.org/10.1016/j.ejpb.2004.11.011] [PMID: 15939236]
[53]
Tzeng SY, Hung BP, Grayson WL, Green JJ. Cystamine-terminated poly(beta-amino ester)s for siRNA delivery to human mesenchymal stem cells and enhancement of osteogenic differentiation. Biomaterials 2012; 33(32): 8142-51.
[http://dx.doi.org/10.1016/j.biomaterials.2012.07.036] [PMID: 22871421]
[54]
Núñez-Toldrà R, Dosta P, Montori S, Ramos V, Atari M, Borrós S. Improvement of osteogenesis in dental pulp pluripotent-like stem cells by oligopeptide-modified poly(β-amino ester)s. Acta Biomater 2017; 53: 152-64.
[http://dx.doi.org/10.1016/j.actbio.2017.01.077] [PMID: 28159719]
[55]
Benoit DS, Boutin ME. Controlling mesenchymal stem cell gene expression using polymer-mediated delivery of siRNA. Biomacromolecules 2012; 13(11): 3841-9.
[http://dx.doi.org/10.1021/bm301294n] [PMID: 23020123]
[56]
Malcolm DW, Freeberg MAT, Wang Y, Sims KR Jr, Awad HA, Benoit DSW. Diblock copolymer hydrophobicity facilitates efficient gene silencing and cytocompatible nanoparticle-mediated sirna delivery to musculoskeletal cell types. Biomacromolecules 2017; 18(11): 3753-65.
[http://dx.doi.org/10.1021/acs.biomac.7b01349] [PMID: 28960967]
[57]
Raisin S, Morille M, Bony C, Noël D, Devoisselle J-M, Belamie E. Tripartite polyionic complex (PIC) micelles as non-viral vectors for mesenchymal stem cell siRNA transfection. Biomater Sci 2017; 5(9): 1910-21.
[http://dx.doi.org/10.1039/C7BM00384F] [PMID: 28722044]
[58]
Liu X, Rocchi P, Peng L. Dendrimers as non-viral vectors for siRNA delivery. New J Chem 2012; 36(2): 256-63.
[http://dx.doi.org/10.1039/C1NJ20408D]
[59]
Ziraksaz Z, Nomani A, Soleimani M, et al. Evaluation of cationic dendrimer and lipid as transfection reagents of short RNAs for stem cell modification. Int J Pharm 2013; 448(1): 231-8.
[http://dx.doi.org/10.1016/j.ijpharm.2013.03.035] [PMID: 23535347]
[60]
Liu X, Zhou J, Yu T, et al. Adaptive amphiphilic dendrimer-based nanoassemblies as robust and versatile siRNA delivery systems. Angew Chem Int Ed Engl 2014; 53(44): 11822-7.
[http://dx.doi.org/10.1002/anie.201406764] [PMID: 25219970]
[61]
Liu H, Chang H, Lv J, et al. Screening of efficient siRNA carriers in a library of surface-engineered dendrimers. Sci Rep 2016; 6: 25069.
[http://dx.doi.org/10.1038/srep25069] [PMID: 27121799]
[62]
Chen C, Posocco P, Liu X, et al. Mastering Dendrimer Self-Assembly for Efficient siRNA Delivery: From Conceptual Design to In Vivo Efficient Gene Silencing. Small 2016; 12(27): 3667-76.
[http://dx.doi.org/10.1002/smll.201503866] [PMID: 27244195]
[63]
Loh XJ, Wu Y-L. Cationic star copolymers based on β-cyclodextrins for efficient gene delivery to mouse embryonic stem cell colonies. Chem Commun (Camb) 2015; 51(54): 10815-8.
[http://dx.doi.org/10.1039/C5CC03686K] [PMID: 26040469]
[64]
Shah S, Solanki A, Sasmal PK, Lee K-B. Single vehicular delivery of siRNA and small molecules to control stem cell differentiation. J Am Chem Soc 2013; 135(42): 15682-5.
[http://dx.doi.org/10.1021/ja4071738] [PMID: 24106916]
[65]
Nair BG, Hagiwara K, Ueda M, Yu HH, Tseng H-R, Ito Y. High density of aligned nanowire treated with polydopamine for efficient gene silencing by siRNA according to cell membrane perturbation. ACS Appl Mater Interfaces 2016; 8(29): 18693-700.
[http://dx.doi.org/10.1021/acsami.6b04913] [PMID: 27420034]
[66]
Link S, El-Sayed MA. Size and temperature dependence of the plasmon absorption of colloidal gold nanoparticles. J Phys Chem B 1999; 103(21): 4212-7.
[http://dx.doi.org/10.1021/jp984796o]
[67]
Link S, El-Sayed MA. Shape and size dependence of radiative, non-radiative and photothermal properties of gold nanocrystals. Int Rev Phys Chem 2000; 19(3): 409-53.
[http://dx.doi.org/10.1080/01442350050034180]
[68]
Daniel M-C, Astruc D. Gold nanoparticles: assembly, supramolecular chemistry, quantum-size-related properties, and applications toward biology, catalysis, and nanotechnology. Chem Rev 2004; 104(1): 293-346.
[http://dx.doi.org/10.1021/cr030698+] [PMID: 14719978]
[69]
Liu XY, Wang A, Zhang T, Mou C-Y. Catalysis by gold: New insights into the support effect. Nano Today 2013; 8(4): 403-16.
[http://dx.doi.org/10.1016/j.nantod.2013.07.005]
[70]
Khan MS, Vishakante GD, Siddaramaiah H. Gold nanoparticles: a paradigm shift in biomedical applications. Adv Colloid Interface Sci 2013; 199-200: 44-58.
[http://dx.doi.org/10.1016/j.cis.2013.06.003] [PMID: 23871224]
[71]
Shukla R, Bansal V, Chaudhary M, Basu A, Bhonde RR, Sastry M. Biocompatibility of gold nanoparticles and their endocytotic fate inside the cellular compartment: a microscopic overview. Langmuir 2005; 21(23): 10644-54.
[http://dx.doi.org/10.1021/la0513712] [PMID: 16262332]
[72]
Almeida JPM, Figueroa ER, Drezek RA. Gold nanoparticle mediated cancer immunotherapy. Nanomedicine (Lond) 2014; 10(3): 503-14.
[http://dx.doi.org/10.1016/j.nano.2013.09.011] [PMID: 24103304]
[73]
Baumgart J, Humbert L, Boulais É, Lachaine R, Lebrun J-J, Meunier M. Off-resonance plasmonic enhanced femtosecond laser optoporation and transfection of cancer cells. Biomaterials 2012; 33(7): 2345-50.
[http://dx.doi.org/10.1016/j.biomaterials.2011.11.062] [PMID: 22177619]
[74]
Peng L-H, Huang Y-F, Zhang C-Z, et al. Integration of antimicrobial peptides with gold nanoparticles as unique non-viral vectors for gene delivery to mesenchymal stem cells with antibacterial activity. Biomaterials 2016; 103: 137-49.
[http://dx.doi.org/10.1016/j.biomaterials.2016.06.057] [PMID: 27376562]
[75]
Zhao X, Huang Q, Jin Y. Gold nanorod delivery of LSD1 siRNA induces human mesenchymal stem cell differentiation. Mater Sci Eng C 2015; 54: 142-9.
[http://dx.doi.org/10.1016/j.msec.2015.05.013] [PMID: 26046277]
[76]
Zheng D, Giljohann DA, Chen DL, et al. Topical delivery of siRNA-based spherical nucleic acid nanoparticle conjugates for gene regulation. Proc Natl Acad Sci USA 2012; 109(30): 11975-80.
[http://dx.doi.org/10.1073/pnas.1118425109] [PMID: 22773805]
[77]
Chertok B, Moffat BA, David AE, et al. Iron oxide nanoparticles as a drug delivery vehicle for MRI monitored magnetic targeting of brain tumors. Biomaterials 2008; 29(4): 487-96.
[http://dx.doi.org/10.1016/j.biomaterials.2007.08.050] [PMID: 17964647]
[78]
Jang JT, Nah H, Lee JH, Moon SH, Kim MG, Cheon J. Critical enhancements of MRI contrast and hyperthermic effects by dopant-controlled magnetic nanoparticles. Angew Chem Int Ed Engl 2009; 48(7): 1234-8.
[http://dx.doi.org/10.1002/anie.200805149] [PMID: 19137514]
[79]
Sun C, Lee JS, Zhang M. Magnetic nanoparticles in MR imaging and drug delivery. Adv Drug Deliv Rev 2008; 60(11): 1252-65.
[http://dx.doi.org/10.1016/j.addr.2008.03.018] [PMID: 18558452]
[80]
Lee CH, Kim EY, Jeon K, et al. Simple, efficient, and reproducible gene transfection of mouse embryonic stem cells by magnetofection. Stem Cells Dev 2008; 17(1): 133-41.
[http://dx.doi.org/10.1089/scd.2007.0064] [PMID: 18271700]
[81]
Shah B, Yin PT, Ghoshal S, Lee KB. Multimodal magnetic core-shell nanoparticles for effective stem-cell differentiation and imaging. Angew Chem Int Ed Engl 2013; 52(24): 6190-5.
[http://dx.doi.org/10.1002/anie.201302245] [PMID: 23650180]
[82]
Zhang D, Wang J, Wang Z, et al. Polyethyleneimine-coated Fe3O4 nanoparticles for efficient siRNA delivery to human mesenchymal stem cells derived from different tissues. Sci Adv Mater 2015; 7(6): 1058-64.
[http://dx.doi.org/10.1166/sam.2015.2178]
[83]
Schade A, Delyagina E, Scharfenberg D, et al. Innovative strategy for microRNA delivery in human mesenchymal stem cells via magnetic nanoparticles. Int J Mol Sci 2013; 14(6): 10710-26.
[http://dx.doi.org/10.3390/ijms140610710] [PMID: 23702843]
[84]
Son S, Liang M-S, Lei P, Xue X, Furlani EP, Andreadis ST. Magnetofection mediated transient NANOG overexpression enhances proliferation and myogenic differentiation of human hair follicle derived mesenchymal stem cells. Bioconjug Chem 2015; 26(7): 1314-27.
[http://dx.doi.org/10.1021/bc5005203] [PMID: 25685943]
[85]
Adams CF, Pickard MR, Chari DM. Magnetic nanoparticle mediated transfection of neural stem cell suspension cultures is enhanced by applied oscillating magnetic fields. Nanomedicine (Lond) 2013; 9(6): 737-41.
[http://dx.doi.org/10.1016/j.nano.2013.05.014] [PMID: 23751375]
[86]
Pickard MR, Barraud P, Chari DM. The transfection of multipotent neural precursor/stem cell transplant populations with magnetic nanoparticles. Biomaterials 2011; 32(9): 2274-84.
[http://dx.doi.org/10.1016/j.biomaterials.2010.12.007] [PMID: 21193228]
[87]
Kairdolf BA, Smith AM, Stokes TH, Wang MD, Young AN, Nie S. Semiconductor quantum dots for bioimaging and biodiagnostic applications. Annu Rev Anal Chem (Palo Alto, Calif) 2013; 6: 143-62.
[http://dx.doi.org/10.1146/annurev-anchem-060908-155136] [PMID: 23527547]
[88]
Yukawa H, Baba Y. In vivo fluorescence imaging and the diagnosis of stem cells using quantum dots for regenerative medicine. Anal Chem 2017; 89(5): 2671-81.
[http://dx.doi.org/10.1021/acs.analchem.6b04763] [PMID: 28194939]
[89]
Subramaniam P, Lee SJ, Shah S, Patel S, Starovoytov V, Lee KB. Generation of a library of non-toxic quantum dots for cellular imaging and siRNA delivery. Adv Mater 2012; 24(29): 4014-9.
[http://dx.doi.org/10.1002/adma.201201019] [PMID: 22744954]
[90]
Wu Y, Zhou B, Xu F, et al. Functional quantum dot-siRNA nanoplexes to regulate chondrogenic differentiation of mesenchymal stem cells. Acta Biomater 2016; 46: 165-76.
[http://dx.doi.org/10.1016/j.actbio.2016.09.008] [PMID: 27615736]
[91]
Xu J, Li J, Lin S, et al. Nanocarrier‐Mediated Codelivery of Small Molecular Drugs and siRNA to Enhance Chondrogenic Differentiation and Suppress Hypertrophy of Human Mesenchymal Stem Cells. Adv Funct Mater 2016; 26(15): 2463-72.
[http://dx.doi.org/10.1002/adfm.201504070]
[92]
Li J, Lee WY, Wu T, et al. Multifunctional Quantum Dot Nanoparticles for Effective Differentiation and Long-Term Tracking of Human Mesenchymal Stem Cells In Vitro and In Vivo. Adv Healthc Mater 2016; 5(9): 1049-57.
[http://dx.doi.org/10.1002/adhm.201500879] [PMID: 26919348]
[93]
Cai Y, Tang R. Calcium phosphate nanoparticles in biomineralization and biomaterials. J Mater Chem 2008; 18(32): 3775-87.
[http://dx.doi.org/10.1039/b805407j]
[94]
Deshmukh K, Ramanan SR, Kowshik M. A novel method for genetic transformation of C albicans using modified-hydroxyapatite nanoparticles as plasmid DNA vehicle. Nanoscale Advances 2019.
[http://dx.doi.org/10.1039/C8NA00365C]
[95]
Deshmukh K, Ramanan SR, Kowshik M. Novel one step transformation method for Escherichia coli and Staphylococcus aureus using arginine-glucose functionalized hydroxyapatite nanoparticles. Mater Sci Eng C 2019; 96: 58-65.
[http://dx.doi.org/10.1016/j.msec.2018.10.088] [PMID: 30606568]
[96]
Choi B, Cui Z-K, Kim S, Fan J, Wu BM, Lee M. Glutamine-chitosan modified calcium phosphate nanoparticles for efficient siRNA delivery and osteogenic differentiation. J Mater Chem B Mater Biol Med 2015; 3(31): 6448-55.
[http://dx.doi.org/10.1039/C5TB00843C] [PMID: 26413302]
[97]
Baughman RH, Zakhidov AA, de Heer WA. Carbon nanotubes--the route toward applications. Science 2002; 297(5582): 787-92.
[http://dx.doi.org/10.1126/science.1060928] [PMID: 12161643]
[98]
Das K, Madhusoodan AP, Mili B, et al. Functionalized carbon nanotubes as suitable scaffold materials for proliferation and differentiation of canine mesenchymal stem cells. Int J Nanomedicine 2017; 12: 3235-52.
[http://dx.doi.org/10.2147/IJN.S122945] [PMID: 28458543]
[99]
Kirkpatrick DL, Weiss M, Naumov A, Bartholomeusz G, Weisman RB, Gliko O. Carbon nanotubes: solution for the therapeutic delivery of siRNA? Materials (Basel) 2012; 5(2): 278-301.
[http://dx.doi.org/10.3390/ma5020278] [PMID: 28817045]
[100]
Chao T-I, Xiang S, Chen C-S, et al. Carbon nanotubes promote neuron differentiation from human embryonic stem cells. Biochem Biophys Res Commun 2009; 384(4): 426-30.
[http://dx.doi.org/10.1016/j.bbrc.2009.04.157] [PMID: 19426708]
[101]
Pacelli S, Maloney R, Chakravarti AR, et al. Controlling adult stem cell behavior using nanodiamond-reinforced hydrogel: implication in bone regeneration therapy. Sci Rep 2017; 7(1): 6577.
[http://dx.doi.org/10.1038/s41598-017-06028-y] [PMID: 28747768]
[102]
Zhang Q, Mochalin VN, Neitzel I, et al. Fluorescent PLLA-nanodiamond composites for bone tissue engineering. Biomaterials 2011; 32(1): 87-94.
[http://dx.doi.org/10.1016/j.biomaterials.2010.08.090] [PMID: 20869765]
[103]
Moore L, Grobárová V, Shen H, et al. Comprehensive interrogation of the cellular response to fluorescent, detonation and functionalized nanodiamonds. Nanoscale 2014; 6(20): 11712-21.
[http://dx.doi.org/10.1039/C4NR02570A] [PMID: 25037888]
[104]
Zhang L, Zhou Q, Song W, Wu K, Zhang Y, Zhao Y. Dual-functionalized graphene oxide based siRNA delivery system for implant surface biomodification with enhanced osteogenesis. ACS Appl Mater Interfaces 2017; 9(40): 34722-35.
[http://dx.doi.org/10.1021/acsami.7b12079] [PMID: 28925678]
[105]
Yin F, Hu K, Chen Y, et al. SiRNA delivery with PEGylated graphene oxide nanosheets for combined photothermal and genetherapy for pancreatic cancer. Theranostics 2017; 7(5): 1133-48.
[http://dx.doi.org/10.7150/thno.17841] [PMID: 28435453]
[106]
Wang H, Zhong L, Liu Y, et al. A black phosphorus nanosheet-based siRNA delivery system for synergistic photothermal and gene therapy. Chem Commun (Camb) 2018; 54(25): 3142-5.
[http://dx.doi.org/10.1039/C8CC00931G] [PMID: 29527603]
[107]
Kou Z, Wang X, Yuan R, et al. A promising gene delivery system developed from PEGylated MoS2 nanosheets for gene therapy. Nanoscale Res Lett 2014; 9(1): 587.
[http://dx.doi.org/10.1186/1556-276X-9-587] [PMID: 25386104]
[108]
Ravichandran R, Liao S, Ng CCh, Chan CK, Raghunath M, Ramakrishna S. Effects of nanotopography on stem cell phenotypes. World J Stem Cells 2009; 1(1): 55-66.
[http://dx.doi.org/10.4252/wjsc.v1.i1.55] [PMID: 21607108]
[109]
Solanki A, Shah S, Yin PT, Lee K-B. Nanotopography-mediated reverse uptake for siRNA delivery into neural stem cells to enhance neuronal differentiation. Sci Rep 2013; 3: 1553.
[http://dx.doi.org/10.1038/srep01553] [PMID: 23531983]
[110]
Zoldan J, Lytton-Jean AK, Karagiannis ED, et al. Directing human embryonic stem cell differentiation by non-viral delivery of siRNA in 3D culture. Biomaterials 2011; 32(31): 7793-800.
[http://dx.doi.org/10.1016/j.biomaterials.2011.06.057] [PMID: 21835461]
[111]
Andersen MØ, Nygaard JV, Burns JS, et al. siRNA nanoparticle functionalization of nanostructured scaffolds enables controlled multilineage differentiation of stem cells. Mol Ther 2010; 18(11): 2018-27.
[http://dx.doi.org/10.1038/mt.2010.166] [PMID: 20808289]
[112]
Pinese C, Lin J, Milbreta U, et al. Sustained delivery of siRNA/mesoporous silica nanoparticle complexes from nanofiber scaffolds for long-term gene silencing. Acta Biomater 2018; 76: 164-77.
[http://dx.doi.org/10.1016/j.actbio.2018.05.054] [PMID: 29890267]
[113]
Squillaro T, Peluso G, Galderisi U. Clinical trials with mesenchymal stem cells: an update. Cell Transplant 2016; 25(5): 829-48.
[http://dx.doi.org/10.3727/096368915X689622] [PMID: 26423725]
[114]
Xiao Y, Shi K, Qu Y, Chu B, Qian Z. Engineering nanoparticles for targeted delivery of nucleic acid therapeutics in tumor. Mol Ther Methods Clin Dev 2018; 12: 1-18.
[http://dx.doi.org/10.1016/j.omtm.2018.09.002] [PMID: 30364598]
[115]
Madl CM, Heilshorn SC, Blau HM. Bioengineering strategies to accelerate stem cell therapeutics. Nature 2018; 557(7705): 335-42.
[http://dx.doi.org/10.1038/s41586-018-0089-z] [PMID: 29769665]


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 15
ISSUE: 2
Year: 2020
Page: [155 - 172]
Pages: 18
DOI: 10.2174/1574888X14666191202095041
Price: $65

Article Metrics

PDF: 13
HTML: 2