Direct Cardiac Reprogramming with Engineered miRNA Scaffolds

Author(s): Priyadharshni Muniyandi, Toru Maekawa, Tatsuro Hanajiri, Vivekanandan Palaninathan*

Journal Name: Current Pharmaceutical Design

Volume 26 , Issue 34 , 2020


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Abstract:

Ischemic heart disease is a predominant cause of death worldwide. The loss or death of cardiomyocytes due to restricted blood flow often results in a cardiac injury. Myofibroblasts replace these injured cardiomyocytes to preserve structural integrity. However, the depleted cardiomyocytes lead to cardiac dysfunction such as pathological cardiac dilation, reduced cardiac contraction, and fibrosis. Repair and regeneration of myocardium are the best possible therapy for end-stage heart failure patients because the current cardiomyocytes restoration therapies are limited to heart transplantation only. The emergence of interests to directly reprogram a mammalian heart with minimal regenerative capacity holds a promising future in the field of cardiovascular regenerative medicine. Repair and regeneration become the two crucial factors in the field of cardiovascular regenerative medicine since heart muscles have no substitutes, like heart valves or blood vessels. Cardiac regeneration includes strategies to reprogram with diverse factors like small molecules, genetic and epigenetic regulators. However, there are some constraints like low efficacy, immunogenic problems, and unsafe delivery systems that pose a daunting challenge in human trial translations. Hence, there is a need for a holistic nanoscale approach in regulating cell fate effectively and efficiently with a safer delivery and a suitable microenvironment that mimics the extracellular matrix. In this review, we have discussed the current state-of-the-art techniques, challenges in direct reprogramming of fibroblasts to cardiac muscle, and prospects of biomaterials in miRNA delivery and cardiac regeneration predominantly during the past decade (2008-2019).

Keywords: Direct reprogramming, miRNA, scaffolds, miRNA delivery, cardiac tissue engineering, myofibroblasts.

[1]
Jaklenec A, Stamp A, Deweerd E, Sherwin A, Langer R. Progress in the tissue engineering and stem cell industry “are we there yet?”. Tissue Eng Part B Rev 2012; 18(3): 155-66.
[http://dx.doi.org/10.1089/ten.teb.2011.0553] [PMID: 22220809]
[2]
Mendelson A, Frenette PS. Hematopoietic stem cell niche maintenance during homeostasis and regeneration. Nat Med 2014; 20(8): 833-46.
[http://dx.doi.org/10.1038/nm.3647] [PMID: 25100529]
[3]
Vacanti JPOJ-B, Wertheim JA. In Introduction: regenerative medicine and solid organ transplantation from a historical perspectiveregenerative medicine applications in organ transplantation London: Elsevier 2014; 1-15.
[http://dx.doi.org/10.1016/B978-0-12-398523-1.00001-X]
[4]
Kami D, Gojo S. Tuning cell fate: from insights to vertebrate regeneration. Organogenesis 2014; 10(2): 231-40.
[http://dx.doi.org/10.4161/org.28816] [PMID: 24736602]
[5]
Joshi A Available from: . http://www.marketsandmarkets.com/Market-
[6]
Younger EM, Chapman MW. Morbidity at bone graft donor sites. J Orthop Trauma 1989; 3(3): 192-5.
[http://dx.doi.org/10.1097/00005131-198909000-00002] [PMID: 2809818]
[7]
Gleeson JP, Plunkett NA, O’Brien FJ. Addition of hydroxyapatite improves stiffness, interconnectivity and osteogenic potential of a highly porous collagen-based scaffold for bone tissue regeneration. Eur Cell Mater 2010; 20(218): 218-30.
[http://dx.doi.org/10.22203/eCM.v020a18] [PMID: 20922667]
[8]
O’Brien FJ. Biomaterials & scaffolds for tissue engineering. Mater Today 2011; 14(3): 88-95.
[http://dx.doi.org/10.1016/S1369-7021(11)70058-X]
[9]
Kattman SJ, Witty AD, Gagliardi M, et al. Stage-specific optimization of activin/nodal and BMP signaling promotes cardiac differentiation of mouse and human pluripotent stem cell lines. Cell Stem Cell 2011; 8(2): 228-40.
[http://dx.doi.org/10.1016/j.stem.2010.12.008] [PMID: 21295278]
[10]
Cao N, Liu Z, Chen Z, et al. Ascorbic acid enhances the cardiac differentiation of induced pluripotent stem cells through promoting the proliferation of cardiac progenitor cells. Cell Res 2012; 22(1): 219-36.
[http://dx.doi.org/10.1038/cr.2011.195] [PMID: 22143566]
[12]
Wang X, From AH, Zhang J. Myocardial regeneration: the role of progenitor cells derived from bone marrow and heart. Prog Mol Biol Transl Sci 2012; 111: 195-215.
[http://dx.doi.org/10.1016/B978-0-12-398459-3.00009-5] [PMID: 22917232]
[13]
Romaine SP, Tomaszewski M, Condorelli G, Samani NJ. MicroRNAs in cardiovascular disease: an introduction for clinicians. Heart 2015; 101(12): 921-8.
[http://dx.doi.org/10.1136/heartjnl-2013-305402] [PMID: 25814653]
[14]
Li Y, Kowdley KV. MicroRNAs in common human diseases. Genomics Proteomics Bioinformatics 2012; 10(5): 246-53.
[http://dx.doi.org/10.1016/j.gpb.2012.07.005] [PMID: 23200134]
[15]
Lee Y, Jeon K, Lee J-T, Kim S, Kim VN. MicroRNA maturation: stepwise processing and subcellular localization. EMBO J 2002; 21(17): 4663-70.
[http://dx.doi.org/10.1093/emboj/cdf476] [PMID: 12198168]
[16]
Garzon R, Marcucci G, Croce CM. Targeting microRNAs in cancer: rationale, strategies and challenges. Nat Rev Drug Discov 2010; 9(10): 775-89.
[http://dx.doi.org/10.1038/nrd3179] [PMID: 20885409]
[17]
Martino S, D’Angelo F, Armentano I, Kenny JM, Orlacchio A. Stem cell-biomaterial interactions for regenerative medicine. Biotechnol Adv 2012; 30(1): 338-51.
[http://dx.doi.org/10.1016/j.biotechadv.2011.06.015] [PMID: 21740963]
[18]
Levenberg S, Huang NF, Lavik E, Rogers AB, Itskovitz-Eldor J, Langer R. Differentiation of human embryonic stem cells on three dimensional polymer scaffolds. Proc Natl Acad Sci USA 2003; 100(22): 12741-6.
[http://dx.doi.org/10.1073/pnas.1735463100] [PMID: 14561891]
[19]
Sapir Y, Kryukov O, Cohen S. Integration of multiple cell-matrix interactions into alginate scaffolds for promoting cardiac tissue regeneration. Biomaterials 2011; 32(7): 1838-47.
[http://dx.doi.org/10.1016/j.biomaterials.2010.11.008] [PMID: 21112626]
[20]
Vunjak-Novakovic G, Lui KO, Tandon N, Chien KR. Bioengineering heart muscle: a paradigm for regenerative medicine. Annu Rev Biomed Eng 2011; 13: 245-67.
[http://dx.doi.org/10.1146/annurev-bioeng-071910-124701] [PMID: 21568715]
[21]
Segers VF, Lee RT. Biomaterials to enhance stem cell function in the heart. Circ Res 2011; 109(8): 910-22.
[http://dx.doi.org/10.1161/CIRCRESAHA.111.249052] [PMID: 21960724]
[22]
Masuda S, Shimizu T, Yamato M, Okano T. Cell sheet engineering for heart tissue repair. Adv Drug Deliv Rev 2008; 60(2): 277-85.
[http://dx.doi.org/10.1016/j.addr.2007.08.031] [PMID: 18006178]
[23]
Kofidis T, de Bruin JL, Hoyt G, et al. Injectable bioartificial myocardial tissue for large-scale intramural cell transfer and functional recovery of injured heart muscle. J Thorac Cardiovasc Surg 2004; 128(4): 571-8.
[http://dx.doi.org/10.1016/j.jtcvs.2004.05.021] [PMID: 15457158]
[24]
Li RK, Jia ZQ, Weisel RD, Mickle DA, Choi A, Yau TM. Survival and function of bioengineered cardiac grafts. Circulation 1999; 100(19)(Suppl.): II63-9.
[http://dx.doi.org/10.1161/01.CIR.100.suppl_2.II-63] [PMID: 10567280]
[25]
Doetschman TC, Eistetter H, Katz M, Schmidt W, Kemler R. The in vitro development of blastocyst-derived embryonic stem cell lines: formation of visceral yolk sac, blood islands and myocardium. J Embryol Exp Morphol 1985; 87: 27-45.
[PMID: 3897439]
[26]
Willems E, Spiering S, Davidovics H, et al. Small-molecule inhibitors of the Wnt pathway potently promote cardiomyocytes from human embryonic stem cell-derived mesoderm. Circ Res 2011; 109(4): 360-4.
[http://dx.doi.org/10.1161/CIRCRESAHA.111.249540] [PMID: 21737789]
[27]
Burridge PW, Thompson S, Millrod MA, et al. A universal system for highly efficient cardiac differentiation of human induced pluripotent stem cells that eliminates interline variability. PLoS One 2011; 6(4): e18293.
[http://dx.doi.org/10.1371/journal.pone.0018293] [PMID: 21494607]
[28]
Elliott DA, Braam SR, Koutsis K, et al. NKX2-5(eGFP/w) hESCs for isolation of human cardiac progenitors and cardiomyocytes. Nat Methods 2011; 8(12): 1037-40.
[http://dx.doi.org/10.1038/nmeth.1740] [PMID: 22020065]
[29]
Zhang Q, Jiang J, Han P, et al. Direct differentiation of atrial and ventricular myocytes from human embryonic stem cells by alternating retinoid signals. Cell Res 2011; 21(4): 579-87.
[http://dx.doi.org/10.1038/cr.2010.163] [PMID: 21102549]
[30]
Uosaki H, Fukushima H, Takeuchi A, et al. Efficient and scalable purification of cardiomyocytes from human embryonic and induced pluripotent stem cells by VCAM1 surface expression. PLoS One 2011; 6(8): e23657.
[http://dx.doi.org/10.1371/journal.pone.0023657] [PMID: 21876760]
[31]
Dubois NC, Craft AM, Sharma P, et al. SIRPA is a specific cell surface marker for isolating cardiomyocytes derived from human pluripotent stem cells. Nat Biotechnol 2011; 29(11): 1011-8.
[http://dx.doi.org/10.1038/nbt.2005] [PMID: 22020386]
[32]
Skelton RJ, Costa M, Anderson DJ, et al. SIRPA, VCAM1 and CD34 identify discrete lineages during early human cardiovascular development. Stem Cell Res (Amst) 2014; 13(1): 172-9.
[http://dx.doi.org/10.1016/j.scr.2014.04.016] [PMID: 24968096]
[33]
Tohyama S, Hattori F, Sano M, et al. Distinct metabolic flow enables large-scale purification of mouse and human pluripotent stem cell-derived cardiomyocytes. Cell Stem Cell 2013; 12(1): 127-37.
[http://dx.doi.org/10.1016/j.stem.2012.09.013] [PMID: 23168164]
[34]
Shiba Y, Fernandes S, Zhu WZ, et al. Human ES-cell-derived cardiomyocytes electrically couple and suppress arrhythmias in injured hearts. Nature 2012; 489(7415): 322-5.
[http://dx.doi.org/10.1038/nature11317] [PMID: 22864415]
[35]
Takahashi K, Tanabe K, Ohnuki M, et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007; 131(5): 861-72.
[http://dx.doi.org/10.1016/j.cell.2007.11.019] [PMID: 18035408]
[36]
Staerk J, Dawlaty MM, Gao Q, et al. Reprogramming of human peripheral blood cells to induced pluripotent stem cells. Cell Stem Cell 2010; 7(1): 20-4.
[http://dx.doi.org/10.1016/j.stem.2010.06.002] [PMID: 20621045]
[37]
Seki T, Yuasa S, Oda M, et al. Generation of induced pluripotent stem cells from human terminally differentiated circulating T cells. Cell Stem Cell 2010; 7(1): 11-4.
[http://dx.doi.org/10.1016/j.stem.2010.06.003] [PMID: 20621043]
[38]
Eghbali-Webb M. Molecular biology intelligence unit molecular biology of collagen matrix in the heart. Austin, TX: Landes 1994.
[39]
Kanekar S, Hirozanne T, Terracio L, Borg TK. Cardiac fibroblasts form and function. Cardiovasc Pathol 1998; 7(3): 127-33.
[http://dx.doi.org/10.1016/S1054-8807(97)00119-1] [PMID: 25851219]
[40]
Nag AC. Study of non-muscle cells of the adult mammalian heart: a fine structural analysis and distribution. Cytobios 1980; 28(109): 41-61.
[PMID: 7428441]
[41]
Zak R. Development and proliferative capacity of cardiac muscle cells Circulation 34/35 (Suppl. II). 1974.
[42]
Souders CA, Bowers SL, Baudino TA. Cardiac fibroblast: the renaissance cell. Circ Res 2009; 105(12): 1164-76.
[http://dx.doi.org/10.1161/CIRCRESAHA.109.209809] [PMID: 19959782]
[43]
Kohl P. Heterogeneous cell coupling in the heart: an electrophysiological role for fibroblasts. Circ Res 2003; 93(5): 381-3.
[http://dx.doi.org/10.1161/01.RES.0000091364.90121.0C]
[44]
Chilton L, Giles WR, Smith GL. Evidence of intercellular coupling between co-cultured adult rabbit ventricular myocytes and myofibroblasts. J Physiol 2007; 583(Pt 1): 225-36.
[http://dx.doi.org/10.1113/jphysiol.2007.135038] [PMID: 17569734]
[45]
Louault C, Benamer N, Faivre J-F, Potreau D, Bescond J. Implication of connexins 40 and 43 in functional coupling between mouse cardiac fibroblasts in primary culture. Biochim Biophys Acta 2008; 1778(10): 2097-104.
[http://dx.doi.org/10.1016/j.bbamem.2008.04.005] [PMID: 18482576]
[46]
Kakkar R, Lee RT. Intramyocardial fibroblast myocyte communication. Circ Res 2010; 106(1): 47-57.
[http://dx.doi.org/10.1161/CIRCRESAHA.109.207456] [PMID: 20056945]
[47]
Deschamps AM, Spinale FG. Disruptions and detours in the myocardial matrix highway and heart failure. Curr Heart Fail Rep 2005; 2(1): 10-7.
[http://dx.doi.org/10.1007/s11897-005-0002-6] [PMID: 16036046]
[48]
Kota J, Chivukula RR, O’Donnell KA, et al. Therapeutic microRNA delivery suppresses tumorigenesis in a murine liver cancer model. Cell 2009; 137(6): 1005-17.
[http://dx.doi.org/10.1016/j.cell.2009.04.021] [PMID: 19524505]
[49]
Zhou T, Benda C, Duzinger S, et al. Generation of induced pluripotent stem cells from urine. J Am Soc Nephrol 2011; 22(7): 1221-8.
[http://dx.doi.org/10.1681/ASN.2011010106] [PMID: 21636641]
[50]
Lee Y, Kim M, Han J, et al. MicroRNA genes are transcribed by RNA polymerase II. EMBO J 2004; 23(20): 4051-60.
[http://dx.doi.org/10.1038/sj.emboj.7600385] [PMID: 15372072]
[51]
Denli AM, Tops BB, Plasterk RH, Ketting RF, Hannon GJ. Processing of primary microRNAs by the Microprocessor complex. Nature 2004; 432(7014): 231-5.
[http://dx.doi.org/10.1038/nature03049] [PMID: 15531879]
[52]
Landthaler M, Yalcin A, Tuschl T. The human DiGeorge syndrome critical region gene 8 and Its D. melanogaster homolog are required for miRNA biogenesis. Curr Biol 2004; 14(23): 2162-7.
[http://dx.doi.org/10.1016/j.cub.2004.11.001] [PMID: 15589161]
[53]
Tsutsumi A, Kawamata T, Izumi N, Seitz H, Tomari Y. Recognition of the pre-miRNA structure by Drosophila Dicer-1. Nat Struct Mol Biol 2011; 18(10): 1153-8.
[http://dx.doi.org/10.1038/nsmb.2125] [PMID: 21926993]
[54]
Schwarz DS, Hutvágner G, Du T, Xu Z, Aronin N, Zamore PD. Asymmetry in the assembly of the RNAi enzyme complex. Cell 2003; 115(2): 199-208.
[http://dx.doi.org/10.1016/S0092-8674(03)00759-1] [PMID: 14567917]
[55]
Gregory RI, Chendrimada TP, Cooch N, Shiekhattar R. Human RISC couples microRNA biogenesis and posttranscriptional gene silencing. Cell 2005; 123(4): 631-40.
[http://dx.doi.org/10.1016/j.cell.2005.10.022] [PMID: 16271387]
[56]
Kozomara A, Griffiths-Jones S. miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res 2014; 42(Database issue): D68-73.
[http://dx.doi.org/10.1093/nar/gkt1181] [PMID: 24275495]
[57]
Friedman RC, Farh KK, Burge CB, Bartel DP. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 2009; 19(1): 92-105.
[http://dx.doi.org/10.1101/gr.082701.108] [PMID: 18955434]
[58]
Ha M, Kim VN. Regulation of microRNA biogenesis. Nat Rev Mol Cell Biol 2014; 15(8): 509-24.
[http://dx.doi.org/10.1038/nrm3838] [PMID: 25027649]
[59]
Malizia AP, Wang DZ. MicroRNAs in cardiomyocyte development. Wiley Interdiscip Rev Syst Biol Med 2011; 3(2): 183-90.
[http://dx.doi.org/10.1002/wsbm.111] [PMID: 21305703]
[60]
Ambros V. microRNAs: tiny regulators with great potential. Cell 2001; 107(7): 823-6.
[http://dx.doi.org/10.1016/S0092-8674(01)00616-X] [PMID: 11779458]
[61]
Jayawardena TM, Egemnazarov B, Finch EA, et al. MicroRNA mediated in vitro and in vivo direct reprogramming of cardiac fibroblasts to cardiomyocytes. Circ Res 2012; 110(11): 1465-73.
[http://dx.doi.org/10.1161/CIRCRESAHA.112.269035] [PMID: 22539765]
[62]
Rao PK, Kumar RM, Farkhondeh M, Baskerville S, Lodish HF. Myogenic factors that regulate expression of muscle-specific microRNAs. Proc Natl Acad Sci USA 2006; 103(23): 8721-6.
[http://dx.doi.org/10.1073/pnas.0602831103] [PMID: 16731620]
[63]
Joladarashi D, Thandavarayan RA, Babu SS, Krishnamurthy P. Small engine, big power: microRNAs as regulators of cardiac diseases and regeneration. Int J Mol Sci 2014; 15(9): 15891-911.
[http://dx.doi.org/10.3390/ijms150915891] [PMID: 25207600]
[64]
Azuma-Mukai A, Oguri H, Mituyama T, et al. Characterization of endogenous human Argonautes and their miRNA partners in RNA silencing. Proc Natl Acad Sci USA 2008; 105(23): 7964-9.
[http://dx.doi.org/10.1073/pnas.0800334105] [PMID: 18524951]
[65]
Kawamata T, Seitz H, Tomari Y. Structural determinants of miRNAs for RISC loading and slicer-independent unwinding. Nat Struct Mol Biol 2009; 16(9): 953-60.
[http://dx.doi.org/10.1038/nsmb.1630] [PMID: 19684602]
[66]
Chen JF, Murchison EP, Tang R, et al. Targeted deletion of Dicer in the heart leads to dilated cardiomyopathy and heart failure. Proc Natl Acad Sci USA 2008; 105(6): 2111-6.
[http://dx.doi.org/10.1073/pnas.0710228105] [PMID: 18256189]
[67]
Heidersbach A, Saxby C, Carver-Moore K, et al. microRNA-1 regulates sarcomere formation and suppresses smooth muscle gene expression in the mammalian heart. eLife 2013; 2: e01323.
[http://dx.doi.org/10.7554/eLife.01323] [PMID: 24252873]
[68]
Wei Y, Peng S, Wu M, et al. Multifaceted roles of miR-1s in repressing the fetal gene program in the heart. Cell Res 2014; 24(3): 278-92.
[http://dx.doi.org/10.1038/cr.2014.12] [PMID: 24481529]
[69]
Vidigal JA, Ventura A. Embryonic stem cell miRNAs and their roles in development and disease. Semin Cancer Biol 2012; 22(5-6): 428-36.
[http://dx.doi.org/10.1016/j.semcancer.2012.04.009] [PMID: 22561239]
[70]
Saxena A, Tabin CJ. miRNA-processing enzyme Dicer is necessary for cardiac outflow tract alignment and chamber septation. Proc Natl Acad Sci USA 2010; 107(1): 87-91.
[http://dx.doi.org/10.1073/pnas.0912870107] [PMID: 20018673]
[71]
da Costa Martins PA, Bourajjaj M, Gladka M, et al. Conditional dicer gene deletion in the postnatal myocardium provokes spontaneous cardiac remodeling. Circulation 2008; 118(15): 1567-76.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.108.769984] [PMID: 18809798]
[72]
Srivastava D. Making or breaking the heart: from lineage determination to morphogenesis. Cell 2006; 126(6): 1037-48.
[http://dx.doi.org/10.1016/j.cell.2006.09.003] [PMID: 16990131]
[73]
Dong DL, Chen C, Huo R, et al. Reciprocal repression between microRNA-133 and calcineurin regulates cardiac hypertrophy: a novel mechanism for progressive cardiac hypertrophy. Hypertension 2010; 55(4): 946-52.
[http://dx.doi.org/10.1161/HYPERTENSIONAHA.109.139519] [PMID: 20177001]
[74]
Wystub K, Besser J, Bachmann A, Boettger T, Braun T. miR-1/133a clusters cooperatively specify the cardiomyogenic lineage by adjustment of myocardin levels during embryonic heart development. PLoS Genet 2013; 9(9): e1003793.
[http://dx.doi.org/10.1371/journal.pgen.1003793] [PMID: 24068960]
[75]
Lompré AM, Nadal-Ginard B, Mahdavi V. Expression of the cardiac ventricular alpha- and beta-myosin heavy chain genes is developmentally and hormonally regulated. J Biol Chem 1984; 259(10): 6437-46.
[PMID: 6327679]
[76]
Cao X, Wang J, Wang Z, et al. MicroRNA profiling during rat ventricular maturation: A role for miR-29a in regulating cardiomyocyte cell cycle re-entry. FEBS Lett 2013; 587(10): 1548-55.
[http://dx.doi.org/10.1016/j.febslet.2013.01.075] [PMID: 23587482]
[77]
Callis TE, Pandya K, Seok HY, et al. MicroRNA-208a is a regulator of cardiac hypertrophy and conduction in mice. J Clin Invest 2009; 119(9): 2772-86.
[http://dx.doi.org/10.1172/JCI36154] [PMID: 19726871]
[78]
Dal-Pra S, Mirotsou M. Reprogramming approaches in cardiovascular regeneration. Curr Treat Options Cardiovasc Med 2014; 16(8): 327.
[http://dx.doi.org/10.1007/s11936-014-0327-0] [PMID: 24928147]
[79]
van Rooij E, Quiat D, Johnson BA, et al. A family of microRNAs encoded by myosin genes governs myosin expression and muscle performance. Dev Cell 2009; 17(5): 662-73.
[http://dx.doi.org/10.1016/j.devcel.2009.10.013] [PMID: 19922871]
[80]
Schraivogel D, Meister G. Import routes and nuclear functions of Argonaute and other small RNA-silencing proteins. Trends Biochem Sci 2014; 39(9): 420-31.
[http://dx.doi.org/10.1016/j.tibs.2014.07.004] [PMID: 25131816]
[81]
Morkin E. Control of cardiac myosin heavy chain gene expression. Microsc Res Tech 2000; 50(6): 522-31.
[http://dx.doi.org/10.1002/1097-0029(20000915)50:6<522::AIDJEMT9>3.0.CO;2-U] [PMID: 10998641]
[82]
Masserdotti G, Gascón S, Götz M. Direct neuronal reprogramming: learning from and for development. Development 2016; 143(14): 2494-510.
[http://dx.doi.org/10.1242/dev.092163] [PMID: 27436039]
[83]
Ifkovits JL, Addis RC, Epstein JA, Gearhart JD. Inhibition of TGFβ signaling increases direct conversion of fibroblasts to induced cardiomyocytes. PLoS One 2014; 9(2): e89678.
[http://dx.doi.org/10.1371/journal.pone.0089678] [PMID: 24586958]
[84]
Zhao Y, Londono P, Cao Y, et al. High-efficiency reprogramming of fibroblasts into cardiomyocytes requires suppression of pro-fibrotic signalling. Nat Commun 2015; 6: 8243.
[http://dx.doi.org/10.1038/ncomms9243] [PMID: 26354680]
[85]
Mohamed TM, Stone NR, Berry EC, et al. Chemical enhancement of in vitro and in vivo direct cardiac reprogramming. Circulation 2017; 135(10): 978-95.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.116.024692] [PMID: 27834668]
[86]
Zhou H, Dickson ME, Kim MS, Bassel-Duby R, Olson EN. Akt1/protein kinase B enhances transcriptional reprogramming of fibroblasts to functional cardiomyocytes. Proc Natl Acad Sci USA 2015; 112(38): 11864-9.
[http://dx.doi.org/10.1073/pnas.1516237112] [PMID: 26354121]
[87]
Zhou H, Morales MG, Hashimoto H, et al. ZNF281 enhances cardiac reprogramming by modulating cardiac and inflammatory gene expression. Genes Dev 2017; 31(17): 1770-83.
[http://dx.doi.org/10.1101/gad.305482.117] [PMID: 28982760]
[88]
Abad M, Hashimoto H, Zhou H, et al. Notch inhibition enhances cardiac reprogramming by increasing MEF2C transcriptional activity. Stem Cell Reports 2017; 8(3): 548-60.
[http://dx.doi.org/10.1016/j.stemcr.2017.01.025] [PMID: 28262548]
[89]
Yamakawa H, Muraoka N, Miyamoto K, et al. Fibroblast growth factors and vascular endothelial growth factor promote cardiac reprogramming under defined conditions. Stem Cell Reports 2015; 5(6): 1128-42.
[http://dx.doi.org/10.1016/j.stemcr.2015.10.019] [PMID: 26626177]
[90]
Ferreira MPA, Talman V, Torrieri G, et al. Dual-drug delivery using dextran-functionalized nanoparticles targeting cardiac fibroblasts for cellular reprogramming. Adv Funct Mater 2018; 28(15): 1705134.
[http://dx.doi.org/10.1002/adfm.201705134]
[91]
Morez C, Noseda M, Paiva MA, Belian E, Schneider MD, Stevens MM. Enhanced efficiency of genetic programming toward cardiomyocyte creation through topographical cues. Biomaterials 2015; 70: 94-104.
[http://dx.doi.org/10.1016/j.biomaterials.2015.07.063] [PMID: 26302234]
[92]
Sia J, Yu P, Srivastava D, Li S. Effect of biophysical cues on reprogramming to cardiomyocytes. Biomaterials 2016; 103: 1-11.
[http://dx.doi.org/10.1016/j.biomaterials.2016.06.034] [PMID: 27376554]
[93]
Engler AJ, Carag-Krieger C, Johnson CP, et al. Embryonic cardiomyocytes beat best on a matrix with heart-like elasticity: scar-like rigidity inhibits beating. J Cell Sci 2008; 121(Pt 22): 3794-802.
[http://dx.doi.org/10.1242/jcs.029678] [PMID: 18957515]
[94]
Chopra A, Lin V, McCollough A, et al. Reprogramming cardiomyocyte mechanosensing by crosstalk between integrins and hyaluronic acid receptors. J Biomech 2012; 45(5): 824-31.
[http://dx.doi.org/10.1016/j.jbiomech.2011.11.023] [PMID: 22196970]
[95]
Kong YP, Carrion B, Singh RK, Putnam AJ. Matrix identity and tractional forces influence indirect cardiac reprogramming. Sci Rep 2013; 3: 3474.
[http://dx.doi.org/10.1038/srep03474] [PMID: 24326998]
[96]
Li Y, Dal-Pra S, Mirotsou M, et al. Tissue-engineered 3-dimensional (3D) microenvironment enhances the direct reprogramming of fibroblasts into cardiomyocytes by microRNAs. Sci Rep 2016; 6: 38815.
[http://dx.doi.org/10.1038/srep38815] [PMID: 27941896]
[97]
Song SY, Yoo J, Go S, et al. Cardiac-mimetic cell-culture system for direct cardiac reprogramming. Theranostics 2019; 9(23): 6734-44.
[http://dx.doi.org/10.7150/thno.35574] [PMID: 31660065]
[98]
Ambros V. MicroRNAs and developmental timing. Curr Opin Genet Dev 2011; 21(4): 511-7.
[http://dx.doi.org/10.1016/j.gde.2011.04.003] [PMID: 21530229]
[99]
Eulalio A, Huntzinger E, Izaurralde E. Getting to the root of miRNA-mediated gene silencing. Cell 2008; 132(1): 9-14.
[http://dx.doi.org/10.1016/j.cell.2007.12.024] [PMID: 18191211]
[100]
Small EM, Olson EN. Pervasive roles of microRNAs in cardiovascular biology. Nature 2011; 469(7330): 336-42.
[http://dx.doi.org/10.1038/nature09783] [PMID: 21248840]
[101]
Rao PK, Toyama Y, Chiang HR, et al. Loss of cardiac microRNA-mediated regulation leads to dilated cardiomyopathy and heart failure. Circ Res 2009; 105(6): 585-94.
[http://dx.doi.org/10.1161/CIRCRESAHA.109.200451] [PMID: 19679836]
[102]
Liu N, Bezprozvannaya S, Williams AH, et al. microRNA-133a regulates cardiomyocyte proliferation and suppresses smooth muscle gene expression in the heart. Genes Dev 2008; 22(23): 3242-54.
[http://dx.doi.org/10.1101/gad.1738708] [PMID: 19015276]
[103]
Nam Y-J, Song K, Luo X, et al. Reprogramming of human fibroblasts toward a cardiac fate. Proc Natl Acad Sci USA 2013; 110(14): 5588-93.
[http://dx.doi.org/10.1073/pnas.1301019110] [PMID: 23487791]
[104]
Muraoka N, Yamakawa H, Miyamoto K, et al. MiR-133 promotes cardiac reprogramming by directly repressing Snai1 and silencing fibroblast signatures. EMBO J 2014; 33(14): 1565-81.
[http://dx.doi.org/10.15252/embj.201387605] [PMID: 24920580]
[105]
Singh VP, Mathison M, Patel V, et al. MiR-590 Promotes transdifferentiation of porcine and human fibroblasts toward a cardiomyocyte-like fate by directly repressing specificity protein 1. J Am Heart Assoc 2016; 5(11): e003922.
[http://dx.doi.org/10.1161/JAHA.116.003922] [PMID: 27930352]
[106]
Bird A. Perceptions of epigenetics. Nature 2007; 447(7143): 396-8.
[http://dx.doi.org/10.1038/nature05913] [PMID: 17522671]
[107]
Iurlaro M, Ficz G, Oxley D, et al. A screen for hydroxymethylcytosine and formylcytosine binding proteins suggests functions in transcription and chromatin regulation. Genome Biol 2013; 14(10): R119.
[http://dx.doi.org/10.1186/gb-2013-14-10-r119] [PMID: 24156278]
[108]
Wilson AG. Epigenetic regulation of gene expression in the inflammatory response and relevance to common diseases. J Periodontol 2008; 79(8)(Suppl.): 1514-9.
[http://dx.doi.org/10.1902/jop.2008.080172] [PMID: 18673005]
[109]
Bird A. DNA methylation patterns and epigenetic memory. Genes Dev 2002; 16(1): 6-21.
[http://dx.doi.org/10.1101/gad.947102] [PMID: 11782440]
[110]
Movassagh M, Choy MK, Goddard M, Bennett MR, Down TA, Foo RS. Differential DNA methylation correlates with differential expression of angiogenic factors in human heart failure. PLoS One 2010; 5(1): e8564.
[http://dx.doi.org/10.1371/journal.pone.0008564] [PMID: 20084101]
[111]
Dawber TR, Meadors GF, Moore FE Jr. Epidemiological approaches to heart disease: the Framingham Study. Am J Public Health Nations Health 1951; 41(3): 279-81.
[http://dx.doi.org/10.2105/AJPH.41.3.279] [PMID: 14819398]
[112]
Baccarelli A, Rienstra M, Benjamin EJ. Cardiovascular epigenetics: basic concepts and results from animal and human studies. Circ Cardiovasc Genet 2010; 3(6): 567-73.
[http://dx.doi.org/10.1161/CIRCGENETICS.110.958744] [PMID: 21156932]
[113]
Handy DE, Castro R, Loscalzo J. Epigenetic modifications: basic mechanisms and role in cardiovascular disease. Circulation 2011; 123(19): 2145-56.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.110.956839] [PMID: 21576679]
[114]
Kalani A, Kamat PK, Tyagi SC, Tyagi N. Synergy of homocysteine, microRNA, and epigenetics: a novel therapeutic approach for stroke. Mol Neurobiol 2013; 48(1): 157-68.
[http://dx.doi.org/10.1007/s12035-013-8421-y] [PMID: 23430482]
[115]
Backs J, Olson EN. Control of cardiac growth by histone acetylation/deacetylation. Circ Res 2006; 98(1): 15-24.
[http://dx.doi.org/10.1161/01.RES.0000197782.21444.8f] [PMID: 16397154]
[116]
Devaux Y, Vausort M, Goretti E, et al. Use of circulating microRNAs to diagnose acute myocardial infarction. Clin Chem 2012; 58(3): 559-67.
[http://dx.doi.org/10.1373/clinchem.2011.173823] [PMID: 22252325]
[117]
Olivieri F, Antonicelli R, Lorenzi M. Diagnostic potential of circulating miR-499-5p in elderly patients with acute non ST-elevation myocardial infarction. Int J Cardiol 2012; 167.
[PMID: 22330002]
[118]
Wang GK, Zhu JQ, Zhang JT, et al. Circulating microRNA: a novel potential biomarker for early diagnosis of acute myocardial infarction in humans. Eur Heart J 2010; 31(6): 659-66.
[http://dx.doi.org/10.1093/eurheartj/ehq013] [PMID: 20159880]
[119]
Meder B, Keller A, Vogel B, et al. MicroRNA signatures in total peripheral blood as novel biomarkers for acute myocardial infarction. Basic Res Cardiol 2011; 106(1): 13-23.
[http://dx.doi.org/10.1007/s00395-010-0123-2] [PMID: 20886220]
[120]
Chronis C, Fiziev P, Papp B, et al. Cooperative Binding of Transcription Factors Orchestrates Reprogramming. Cell 2017; 168(3): 442-59.e20.
[http://dx.doi.org/10.1016/j.cell.2016.12.016] [PMID: 28111071]
[121]
Zaret KS, Carroll JS. Pioneer transcription factors: establishing competence for gene expression. Genes Dev 2011; 25(21): 2227-41.
[http://dx.doi.org/10.1101/gad.176826.111] [PMID: 22056668]
[122]
Bossard P, Zaret KS. GATA transcription factors as potentiators of gut endoderm differentiation. Development 1998; 125(24): 4909-17.
[PMID: 9811575]
[123]
Takeuchi JK, Bruneau BG. Directed transdifferentiation of mouse mesoderm to heart tissue by defined factors. Nature 2009; 459(7247): 708-11.
[http://dx.doi.org/10.1038/nature08039] [PMID: 19396158]
[124]
Liu Z, Chen O, Zheng M, et al. Re-patterning of H3K27me3, H3K4me3 and DNA methylation during fibroblast conversion into induced cardiomyocytes. Stem Cell Res (Amst) 2016; 16(2): 507-18.
[http://dx.doi.org/10.1016/j.scr.2016.02.037] [PMID: 26957038]
[125]
Dal-Pra S, Hodgkinson CP, Mirotsou M, Kirste I, Dzau VJ. Demethylation of H3K27 is essential for the induction of direct cardiac reprogramming by miR combo. Circ Res 2017; 120(9): 1403-13.
[http://dx.doi.org/10.1161/CIRCRESAHA.116.308741] [PMID: 28209718]
[126]
Blasco MA, Serrano M, Fernandez-Capetillo O. Genomic instability in iPS: time for a break. EMBO J 2011; 30(6): 991-3.
[http://dx.doi.org/10.1038/emboj.2011.50] [PMID: 21407252]
[127]
Nashun B, Hill PW, Hajkova P. Reprogramming of cell fate: epigenetic memory and the erasure of memories past. EMBO J 2015; 34(10): 1296-308.
[http://dx.doi.org/10.15252/embj.201490649] [PMID: 25820261]
[128]
Zhou Y, Wang L, Vaseghi HR, et al. Bmi1 is a key epigenetic barrier to direct cardiac reprogramming. Cell Stem Cell 2016; 18(3): 382-95.
[http://dx.doi.org/10.1016/j.stem.2016.02.003] [PMID: 26942853]
[129]
Hirai H, Kikyo N. Inhibitors of suppressive histone modification promote direct reprogramming of fibroblasts to cardiomyocyte-like cells. Cardiovasc Res 2014; 102(1): 188-90.
[http://dx.doi.org/10.1093/cvr/cvu023] [PMID: 24477643]
[130]
Sauls K, Greco TM, Wang L, et al. Initiating events in direct cardiomyocyte reprogramming. Cell Rep 2018; 22(7): 1913-22.
[http://dx.doi.org/10.1016/j.celrep.2018.01.047] [PMID: 29444441]
[131]
Kashyap V, Rezende NC, Scotland KB, et al. Regulation of stem cell pluripotency and differentiation involves a mutual regulatory circuit of the NANOG, OCT4, and SOX2 pluripotency transcription factors with polycomb repressive complexes and stem cell microRNAs. Stem Cells Dev 2009; 18(7): 1093-108.
[http://dx.doi.org/10.1089/scd.2009.0113] [PMID: 19480567]
[132]
Gattazzo F, Urciuolo A, Bonaldo P. Extracellular matrix: a dynamic microenvironment for stem cell niche. Biochim Biophys Acta 2014; 1840(8): 2506-19.
[http://dx.doi.org/10.1016/j.bbagen.2014.01.010] [PMID: 24418517]
[133]
Kim SS, Garg H, Joshi A, Manjunath N. Strategies for targeted nonviral delivery of siRNAs in vivo. Trends Mol Med 2009; 15(11): 491-500.
[http://dx.doi.org/10.1016/j.molmed.2009.09.001] [PMID: 19846342]
[134]
Raemdonck K, Martens TF, Braeckmans K, Demeester J, De Smedt SC. Polysaccharide-based nucleic acid nanoformulations. Adv Drug Deliv Rev 2013; 65(9): 1123-47.
[http://dx.doi.org/10.1016/j.addr.2013.05.002] [PMID: 23680381]
[135]
Chen SS, Fitzgerald W, Zimmerberg J, Kleinman HK, Margolis L. Cell-cell and cell-extracellular matrix interactions regulate embryonic stem cell differentiation. Stem Cells 2007; 25(3): 553-61.
[http://dx.doi.org/10.1634/stemcells.2006-0419] [PMID: 17332514]
[136]
Wang HB, Dembo M, Wang YL. Substrate flexibility regulates growth and apoptosis of normal but not transformed cells. Am J Physiol Cell Physiol 2000; 279(5): C1345-50.
[http://dx.doi.org/10.1152/ajpcell.2000.279.5.C1345] [PMID: 11029281]
[137]
Xi J, Khalil M, Shishechian N, et al. Comparison of contractile behavior of native murine ventricular tissue and cardiomyocytes derived from embryonic or induced pluripotent stem cells. FASEB J 2010; 24(8): 2739-51.
[http://dx.doi.org/10.1096/fj.09-145177] [PMID: 20371616]
[138]
Khademhosseini A, Vacanti JP, Langer R. Progress in tissue engineering. Sci Am 2009; 300(5): 64-71.
[http://dx.doi.org/10.1038/scientificamerican0509-64] [PMID: 19438051]
[139]
Cutts J, Nikkhah M, Brafman DA. Biomaterial approaches for stem cell-based myocardial tissue engineering. Biomark Insights 2015; 10(Suppl. 1): 77-90.
[http://dx.doi.org/10.4137/BMI.S20313] [PMID: 26052226]
[140]
Lee S-W, Lee HJ, Hwang HS, Ko K, Han DW, Ko K. Optimization of Matrigel-based culture for expansion of neural stem cells. Anim Cells Syst 2015; 19(3): 175-80.
[http://dx.doi.org/10.1080/19768354.2015.1035750]
[141]
Ott HC, Matthiesen TS, Goh SK, et al. Perfusion-decellularized matrix: using nature’s platform to engineer a bioartificial heart. Nat Med 2008; 14(2): 213-21.
[http://dx.doi.org/10.1038/nm1684] [PMID: 18193059]
[142]
Olivieri IM, Bova S, Fazzi E, et al. SOLE VLBWI Questionnaire Study Group Patient-reported outcomes measure for children born preterm: validation of the SOLE VLBWI Questionnaire, a new quality of life self-assessment tool. Dev Med Child Neurol 2016; 58(9): 957-64.
[http://dx.doi.org/10.1111/dmcn.13122] [PMID: 27061508]
[143]
Badylak SF, Taylor D, Uygun K. Whole-organ tissue engineering: decellularization and recellularization of three-dimensional matrix scaffolds. Annu Rev Biomed Eng 2011; 13: 27-53.
[http://dx.doi.org/10.1146/annurev-bioeng-071910-124743] [PMID: 21417722]
[144]
Kelleher CM, Vacanti JP. Engineering extracellular matrix through nanotechnology. J R Soc Interface 2010; 7(Suppl. 6): S717-29.
[http://dx.doi.org/10.1098/rsif.2010.0345.focus] [PMID: 20861039]
[145]
Lockhart M, Wirrig E, Phelps A, Wessels A. Extracellular matrix and heart development. Birth Defects Res A Clin Mol Teratol 2011; 91(6): 535-50.
[http://dx.doi.org/10.1002/bdra.20810] [PMID: 21618406]
[146]
Prestwich GD. Simplifying the extracellular matrix for 3-D cell culture and tissue engineering: a pragmatic approach. J Cell Biochem 2007; 101(6): 1370-83.
[http://dx.doi.org/10.1002/jcb.21386] [PMID: 17492655]
[147]
Lutolf MP, Gilbert PM, Blau HM. Designing materials to direct stem-cell fate. Nature 2009; 462(7272): 433-41.
[http://dx.doi.org/10.1038/nature08602] [PMID: 19940913]
[148]
Kitsara M, Chatzichristidi M, Niakoula D, et al. Layer-by-layer UV micromachining methodology of epoxy resist embedded microchannels. Microelectron Eng 2006; 83(4-9): 1298-301.
[http://dx.doi.org/10.1016/j.mee.2006.01.157]]
[149]
Kitsara M, Nwankire C, Walsh LA, et al. Spin coating of hydrophilic polymeric films for enhanced centrifugal flow control by serial siphoning. Microfluid Nanofluidics 2014; 16: 691-9.
[150]
Kitsara JD M. Integration of functional materials and surface modification for polymeric microfluidic systems Micromech Microeng 2013; 23(3)
[151]
Lee CH, Lim YC, Farson DF, Powell HM, Lannutti JJ. Vascular wall engineering via femtosecond laser ablation: scaffolds with self-containing smooth muscle cell populations. Ann Biomed Eng 2011; 39(12): 3031-41.
[http://dx.doi.org/10.1007/s10439-011-0417-z] [PMID: 21971965]
[152]
Wu GH, Hsu SH. Review: Polymeric-based 3D printing for tissue engineering. J Med Biol Eng 2015; 35(3): 285-92.
[http://dx.doi.org/10.1007/s40846-015-0038-3] [PMID: 26167139]
[153]
Bonadio J, Smiley E, Patil P, Goldstein S. Localized, direct plasmid gene delivery in vivo: prolonged therapy results in reproducible tissue regeneration. Nat Med 1999; 5(7): 753-9.
[http://dx.doi.org/10.1038/10473] [PMID: 10395319]
[154]
Fang J, Zhu YY, Smiley E, et al. Stimulation of new bone formation by direct transfer of osteogenic plasmid genes. Proc Natl Acad Sci USA 1996; 93(12): 5753-8.
[http://dx.doi.org/10.1073/pnas.93.12.5753] [PMID: 8650165]
[155]
Lee K, Silva EA, Mooney DJ. Growth factor delivery-based tissue engineering: general approaches and a review of recent developments. J R Soc Interface 2011; 8(55): 153-70.
[http://dx.doi.org/10.1098/rsif.2010.0223] [PMID: 20719768]
[156]
Nguyen MK, Jeon O, Krebs MD, Schapira D, Alsberg E. Sustained localized presentation of RNA interfering molecules from in situ forming hydrogels to guide stem cell osteogenic differentiation. Biomaterials 2014; 35(24): 6278-86.
[http://dx.doi.org/10.1016/j.biomaterials.2014.04.048] [PMID: 24831973]
[157]
O’Brien FJ, Harley BA, Waller MA, Yannas IV, Gibson LJ, Prendergast PJ. The effect of pore size on permeability and cell attachment in collagen scaffolds for tissue engineering. Technol Health Care 2007; 15(1): 3-17.
[http://dx.doi.org/10.3233/THC-2007-15102] [PMID: 17264409]
[158]
Sriram M, Sainitya R, Kalyanaraman V, Dhivya S, Selvamurugan N. Biomaterials mediated microRNA delivery for bone tissue engineering. Int J Biol Macromol 2015; 74: 404-12.
[http://dx.doi.org/10.1016/j.ijbiomac.2014.12.034] [PMID: 25543062]
[159]
Pelled G, Ben-Arav A, Hock C, et al. Direct gene therapy for bone regeneration: gene delivery, animal models, and outcome measures. Tissue Eng Part B Rev 2010; 16(1): 13-20.
[http://dx.doi.org/10.1089/ten.teb.2009.0156] [PMID: 20143927]
[160]
Mariner PD, Johannesen E, Anseth KS. Manipulation of miRNA activity accelerates osteogenic differentiation of hMSCs in engineered 3D scaffolds. J Tissue Eng Regen Med 2012; 6(4): 314-24.
[http://dx.doi.org/10.1002/term.435] [PMID: 21706778]
[161]
Evans CH. Gene therapy for bone healing. Expert Rev Mol Med 2010; 12: e18.
[http://dx.doi.org/10.1017/S1462399410001493] [PMID: 20569532]
[162]
Agarwal S, Wendorff JH, Greiner A. Progress in the field of electrospinning for tissue engineering applications. Adv Mater 2009; 21(32-33): 3343-51.
[http://dx.doi.org/10.1002/adma.200803092] [PMID: 20882501]
[163]
Pham QP, Sharma U, Mikos AG. Electrospinning of polymeric nanofibers for tissue engineering applications: a review. Tissue Eng 2006; 12(5): 1197-211.
[http://dx.doi.org/10.1089/ten.2006.12.1197] [PMID: 16771634]
[164]
Frenot A. Chronakis, Ioannis S. Chronakis Polymer nanofibers assembled by electrospinning. Curr Opin Colloid Interface Sci 2003; 8(1): 64-75.
[165]
Schnell E, Klinkhammer K, Balzer S, et al. Guidance of glial cell migration and axonal growth on electrospun nanofibers of poly-epsilon-caprolactone and a collagen/poly-epsilon-caprolactone blend. Biomaterials 2007; 28(19): 3012-25.
[http://dx.doi.org/10.1016/j.biomaterials.2007.03.009] [PMID: 17408736]
[166]
Liang D, Hsiao BS, Chu B. Functional electrospun nanofibrous scaffolds for biomedical applications. Adv Drug Deliv Rev 2007; 59(14): 1392-412.
[http://dx.doi.org/10.1016/j.addr.2007.04.021] [PMID: 17884240]
[167]
Yin Z, Chen X, Chen JL, et al. The regulation of tendon stem cell differentiation by the alignment of nanofibers. Biomaterials 2010; 31(8): 2163-75.
[http://dx.doi.org/10.1016/j.biomaterials.2009.11.083] [PMID: 19995669]
[168]
Xin X, Hussain M, Mao JJ. Continuing differentiation of human mesenchymal stem cells and induced chondrogenic and osteogenic lineages in electrospun PLGA nanofiber scaffold. Biomaterials 2007; 28(2): 316-25.
[http://dx.doi.org/10.1016/j.biomaterials.2006.08.042] [PMID: 17010425]
[169]
Barnes CP, Pemble CW, Brand DD, Simpson DG, Bowlin GL. Cross-linking electrospun type II collagen tissue engineering scaffolds with carbodiimide in ethanol. Tissue Eng 2007; 13(7): 1593-605.
[http://dx.doi.org/10.1089/ten.2006.0292] [PMID: 17523878]
[170]
Shields KJ, Beckman MJ, Bowlin GL, Wayne JS. Mechanical properties and cellular proliferation of electrospun collagen type II. Tissue Eng 2004; 10(9-10): 1510-7.
[http://dx.doi.org/10.1089/ten.2004.10.1510] [PMID: 15588410]
[171]
Choi JS, Lee SJ, Christ GJ, Atala A, Yoo JJ. The influence of electrospun aligned poly(epsilon-caprolactone)/collagen nanofiber meshes on the formation of self-aligned skeletal muscle myotubes. Biomaterials 2008; 29(19): 2899-906.
[http://dx.doi.org/10.1016/j.biomaterials.2008.03.031] [PMID: 18400295]
[172]
Powell HM, Boyce ST. Engineered human skin fabricated using electrospun collagen-PCL blends: morphogenesis and mechanical properties. Tissue Eng Part A 2009; 15(8): 2177-87.
[http://dx.doi.org/10.1089/ten.tea.2008.0473] [PMID: 19231973]
[173]
Middleton JC, Tipton AJ. Synthetic biodegradable polymers as orthopedic devices. Biomaterials 2000; 21(23): 2335-46.
[http://dx.doi.org/10.1016/S0142-9612(00)00101-0] [PMID: 11055281]
[174]
Gilding DK, Reed AM. Biodegradable polymers for use in surgery-polyglycolic/poly(actic acid) homo- and copolymers: 1. Polymer (Guildf) 1979; 20(12): 1459-64.
[http://dx.doi.org/10.1016/0032-3861(79)90009-0]
[175]
Pietrzak WS, Sarver DR, Verstynen ML. Bioabsorbable polymer science for the practicing surgeon. J Craniofac Surg 1997; 8(2): 87-91.
[http://dx.doi.org/10.1097/00001665-199703000-00004] [PMID: 10332272]
[176]
Therin M, Christel P, Li S, Garreau H, Vert M. In vivo degradation of massive poly(alpha-hydroxy acids): validation of in vitro findings. Biomaterials 1992; 13(9): 594-600.
[http://dx.doi.org/10.1016/0142-9612(92)90027-L] [PMID: 1391406]
[177]
Browning A, Chu CC. The effect of annealing treatments on the tensile properties and hydrolytic degradative properties of polyglycolic acid sutures. J Biomed Mater Res 1986; 20(5): 613-32.
[http://dx.doi.org/10.1002/jbm.820200507] [PMID: 3011808]
[178]
Mauck RL, Baker BM, Nerurkar NL, et al. Engineering on the straight and narrow: the mechanics of nanofibrous assemblies for fiber-reinforced tissue regeneration. Tissue Eng Part B Rev 2009; 15(2): 171-93.
[http://dx.doi.org/10.1089/ten.teb.2008.0652] [PMID: 19207040]
[179]
Li WJ, Cooper JA Jr, Mauck RL, Tuan RS. Fabrication and characterization of six electrospun poly(alpha-hydroxy ester)-based fibrous scaffolds for tissue engineering applications. Acta Biomater 2006; 2(4): 377-85.
[http://dx.doi.org/10.1016/j.actbio.2006.02.005] [PMID: 16765878]
[180]
Inai R, Kotaki M, Ramakrishna S. Structure and properties of electrospun PLLA single nanofibres. Nanotechnology 2005; 16(2): 208-13.
[http://dx.doi.org/10.1088/0957-4484/16/2/005] [PMID: 21727424]
[181]
Chew SY, Hufnagel TC, Lim CT, Leong KW. Mechanical properties of single electrospun drug-encapsulated nanofibres. Nanotechnology 2006; 17(15): 3880-91.
[http://dx.doi.org/10.1088/0957-4484/17/15/045] [PMID: 19079553]
[182]
Moffat KL, Kwei AS, Spalazzi JP, Doty SB, Levine WN, Lu HH. Novel nanofiber-based scaffold for rotator cuff repair and augmentation. Tissue Eng Part A 2009; 15(1): 115-26.
[http://dx.doi.org/10.1089/ten.tea.2008.0014] [PMID: 18788982]
[183]
Nerurkar NL, Baker BM, Sen S, Wible EE, Elliott DM, Mauck RL. Nanofibrous biologic laminates replicate the form and function of the annulus fibrosus. Nat Mater 2009; 8(12): 986-92.
[http://dx.doi.org/10.1038/nmat2558] [PMID: 19855383]
[184]
Kim HN, Jiao A, Hwang NS, et al. Nanotopography-guided tissue engineering and regenerative medicine. Adv Drug Deliv Rev 2013; 65(4): 536-58.
[http://dx.doi.org/10.1016/j.addr.2012.07.014] [PMID: 22921841]
[185]
Li Y, Huang G, Zhang X, et al. Engineering cell alignment in vitro. Biotechnol Adv 2014; 32(2): 347-65.
[http://dx.doi.org/10.1016/j.biotechadv.2013.11.007] [PMID: 24269848]
[186]
Liu YW, Chang K-Y. Advanced transistor structures with optimum short channel controls for high density/high performance integrated circuits. United States patent US5877049A.
[187]
Discher DE, Janmey P, Wang YL. Tissue cells feel and respond to the stiffness of their substrate. Science 2005; 310(5751): 1139-43.
[http://dx.doi.org/10.1126/science.1116995] [PMID: 16293750]
[188]
Tan EP, Lim CT. Characterization of bulk properties of nanofibrous scaffolds from nanomechanical properties of single nanofibers. J Biomed Mater Res A 2006; 77(3): 526-33.
[http://dx.doi.org/10.1002/jbm.a.30646] [PMID: 16489588]
[189]
Ingber DE. Mechanosensation through integrins: cells act locally but think globally. Proc Natl Acad Sci USA 2003; 100(4): 1472-4.
[http://dx.doi.org/10.1073/pnas.0530201100] [PMID: 12578965]
[190]
Chen Q-Z, Bismarck A, Hansen U, et al. Characterisation of a soft elastomer poly(glycerol sebacate) designed to match the mechanical properties of myocardial tissue. Biomaterials 2008; 29(1): 47-57.
[http://dx.doi.org/10.1016/j.biomaterials.2007.09.010] [PMID: 17915309]
[191]
James EN, Delany AM, Nair LS. Post-transcriptional regulation in osteoblasts using localized delivery of miR-29a inhibitor from nanofibers to enhance extracellular matrix deposition. Acta Biomater 2014; 10(8): 3571-80.
[http://dx.doi.org/10.1016/j.actbio.2014.04.026] [PMID: 24816265]
[192]
Zhou F, Jia X, Yang Y, et al. Nanofiber-mediated microRNA-126 delivery to vascular endothelial cells for blood vessel regeneration. Acta Biomater 2016; 43: 303-13.
[http://dx.doi.org/10.1016/j.actbio.2016.07.048] [PMID: 27477849]
[193]
Qureshi AT, Doyle A, Chen C, et al. Photoactivated miR-148b-nanoparticle conjugates improve closure of critical size mouse calvarial defects. Acta Biomater 2015; 12: 166-73.
[http://dx.doi.org/10.1016/j.actbio.2014.10.010] [PMID: 25462528]
[194]
Diao HJ, Low WC, Lu QR, Chew SY. Topographical effects on fiber-mediated microRNA delivery to control oligodendroglial precursor cells development. Biomaterials 2015; 70: 105-14.
[http://dx.doi.org/10.1016/j.biomaterials.2015.08.029] [PMID: 26310106]
[195]
Boese AS, Majer A, Saba R, Booth SA. Small RNA drugs for prion disease: a new frontier. Expert Opin Drug Discov 2013; 8(10): 1265-84.
[http://dx.doi.org/10.1517/17460441.2013.818976] [PMID: 23848240]
[196]
Son S, Namgung R, Kim J, Singha K, Kim WJ. Bioreducible polymers for gene silencing and delivery. Acc Chem Res 2012; 45(7): 1100-12.
[http://dx.doi.org/10.1021/ar200248u] [PMID: 22129162]
[197]
Höbel S, Aigner A. Polyethylenimines for siRNA and miRNA delivery in vivo. Wiley Interdiscip Rev Nanomed Nanobiotechnol 2013; 5(5): 484-501.
[http://dx.doi.org/10.1002/wnan.1228] [PMID: 23720168]
[198]
Hwang DW, Son S, Jang J, et al. A brain-targeted rabies virus glycoprotein-disulfide linked PEI nanocarrier for delivery of neurogenic microRNA. Biomaterials 2011; 32(21): 4968-75.
[http://dx.doi.org/10.1016/j.biomaterials.2011.03.047] [PMID: 21489620]
[199]
Yeh P-H, Sun J-S, Wu H-C, Hwang L-H, Wang T-W. Stimuli-responsive HA-PEI nanoparticles encapsulating endostatin plasmid for stem cell gene therapy. RSC Advances 2013; 3(31): 12922-32.
[http://dx.doi.org/10.1039/c3ra40880a]
[200]
Zhao X, Li Z, Pan H, et al. Enhanced gene delivery by chitosan-disulfide-conjugated LMW-PEI for facilitating osteogenic differentiation. Acta Biomater 2013; 9(5): 6694-703.
[http://dx.doi.org/10.1016/j.actbio.2013.01.039] [PMID: 23395816]
[201]
Danhier F, Ansorena E, Silva JM, Coco R, Le Breton A, Préat V. PLGA-based nanoparticles: an overview of biomedical applications. J Control Release 2012; 161(2): 505-22.
[http://dx.doi.org/10.1016/j.jconrel.2012.01.043] [PMID: 22353619]
[202]
Reynolds AR, Moein Moghimi S, Hodivala-Dilke K. Nanoparticle-mediated gene delivery to tumour neovasculature. Trends Mol Med 2003; 9(1): 2-4.
[http://dx.doi.org/10.1016/S1471-4914(02)00004-7] [PMID: 12524203]
[203]
Ravi Kumar M, Hellermann G, Lockey RF, Mohapatra SS. Nanoparticle-mediated gene delivery: state of the art. Expert Opin Biol Ther 2004; 4(8): 1213-24.
[http://dx.doi.org/10.1517/14712598.4.8.1213] [PMID: 15268657]
[204]
Yuba E, Kojima C, Harada A. Tana, Watarai S, Kono K. pH-Sensitive fusogenic polymer-modified liposomes as a carrier of antigenic proteins for activation of cellular immunity. Biomaterials 2010; 31(5): 943-51.
[http://dx.doi.org/10.1016/j.biomaterials.2009.10.006] [PMID: 19850335]
[205]
Patil YB, Swaminathan SK, Sadhukha T, Ma L, Panyam J. The use of nanoparticle-mediated targeted gene silencing and drug delivery to overcome tumor drug resistance. Biomaterials 2010; 31(2): 358-65.
[http://dx.doi.org/10.1016/j.biomaterials.2009.09.048] [PMID: 19800114]
[206]
Blum JS, Saltzman WM. High loading efficiency and tunable release of plasmid DNA encapsulated in submicron particles fabricated from PLGA conjugated with poly-L-lysine. J Control Release 2008; 129(1): 66-72.
[http://dx.doi.org/10.1016/j.jconrel.2008.04.002] [PMID: 18511145]
[207]
Ramanlal Chaudhari K, Kumar A, Megraj Khandelwal VK, et al. Bone metastasis targeting: a novel approach to reach bone using Zoledronate anchored PLGA nanoparticle as carrier system loaded with Docetaxel. J Control Release 2012; 158(3): 470-8.
[http://dx.doi.org/10.1016/j.jconrel.2011.11.020] [PMID: 22146683]
[208]
Devulapally R, Sekar NM, Sekar TV, et al. Polymer nanoparticles mediated codelivery of antimiR-10b and antimiR-21 for achieving triple negative breast cancer therapy. ACS Nano 2015; 9(3): 2290-302.
[http://dx.doi.org/10.1021/nn507465d] [PMID: 25652012]
[209]
Wang S, Zhang J, Wang Y, Chen M. Hyaluronic acid-coated PEI-PLGA nanoparticles mediated co-delivery of doxorubicin and miR-542-3p for triple negative breast cancer therapy. Nanomedicine (Lond) 2016; 12(2): 411-20.
[http://dx.doi.org/10.1016/j.nano.2015.09.014] [PMID: 26711968]
[210]
Cheng CJ, Saltzman WM. Polymer nanoparticle-mediated delivery of microRNA inhibition and alternative splicing. Mol Pharm 2012; 9(5): 1481-8.
[http://dx.doi.org/10.1021/mp300081s] [PMID: 22482958]
[211]
Babar IA, Cheng CJ, Booth CJ, et al. Nanoparticle-based therapy in an in vivo microRNA-155 (miR-155)-dependent mouse model of lymphoma. Proc Natl Acad Sci USA 2012; 109(26): E1695-704.
[http://dx.doi.org/10.1073/pnas.1201516109] [PMID: 22685206]
[212]
Jonderian A, Maalouf R. Formulation and in vitro interaction of rhodamine-B loaded PLGA nanoparticles with cardiac myocytes. Front Pharmacol 2016; 7(458): 458.
[http://dx.doi.org/10.3389/fphar.2016.00458] [PMID: 27999542]
[213]
Zhang XQ, Chen M, Lam R, Xu X, Osawa E, Ho D. Polymer-functionalized nanodiamond platforms as vehicles for gene delivery. ACS Nano 2009; 3(9): 2609-16.
[http://dx.doi.org/10.1021/nn900865g] [PMID: 19719152]
[214]
Chen M, Zhang X-Q, Man HB, Lam R, Chow EK, Ho D. Nanodiamond vectors functionalized with polyethylenimine for siRNA delivery. J Phys Chem Lett 2010; 1(21): 3167-71.
[http://dx.doi.org/10.1021/jz1013278]
[215]
Alhaddad A, Adam MP, Botsoa J, et al. Nanodiamond as a vector for siRNA delivery to Ewing sarcoma cells. Small 2011; 7(21): 3087-95.
[http://dx.doi.org/10.1002/smll.201101193] [PMID: 21913326]
[216]
Cui C, Wang Y, Zhao W, et al. RGDS covalently surfaced nanodiamond as a tumor targeting carrier of VEGF-siRNA: synthesis, characterization and bioassay. J Mater Chem B Mater Biol Med 2015; 3(48): 9260-8.
[http://dx.doi.org/10.1039/C5TB01602A]
[217]
Deng Y, Zhou H, Zou D, et al. The role of miR-31-modified adipose tissue-derived stem cells in repairing rat critical-sized calvarial defects. Biomaterials 2013; 34(28): 6717-28.
[http://dx.doi.org/10.1016/j.biomaterials.2013.05.042] [PMID: 23768901]
[218]
Eskildsen T, Taipaleenmäki H, Stenvang J, et al. MicroRNA-138 regulates osteogenic differentiation of human stromal (mesenchymal) stem cells in vivo. Proc Natl Acad Sci USA 2011; 108(15): 6139-44.
[http://dx.doi.org/10.1073/pnas.1016758108] [PMID: 21444814]
[219]
Wang Z, Zhang D, Hu Z, et al. MicroRNA-26a-modified adipose-derived stem cells incorporated with a porous hydroxyapatite scaffold improve the repair of bone defects. Mol Med Rep 2015; 12(3): 3345-50.
[http://dx.doi.org/10.3892/mmr.2015.3795] [PMID: 25997460]
[220]
Lee SWL, Paoletti C, Campisi M, et al. MicroRNA delivery through nanoparticles. J Control Release 2019; 313: 80-95.
[http://dx.doi.org/10.1016/j.jconrel.2019.10.007] [PMID: 31622695]
[221]
Arora S, Swaminathan SK, Kirtane A, et al. Synthesis, characterization, and evaluation of poly (D,L-lactide-co-glycolide)-based nanoformulation of miRNA-150: potential implications for pancreatic cancer therapy. Int J Nanomedicine 2014; 9: 2933-42.
[PMID: 24971005]
[222]
Cao M, Deng X, Su S, et al. Protamine sulfate-nanodiamond hybrid nanoparticles as a vector for MiR-203 restoration in esophageal carcinoma cells. Nanoscale 2013; 5(24): 12120-5.
[http://dx.doi.org/10.1039/c3nr04056a] [PMID: 24154605]
[223]
Xia Y, Deng X, Cao M, et al. Nanodiamond-based layer-by-layer nanohybrids mediate targeted delivery of miR-34a for triple negative breast cancer therapy. RSC Advances 2018; 8(25): 13789-97.
[http://dx.doi.org/10.1039/C8RA00907D]
[224]
Marler JJ, Upton J, Langer R, Vacanti JP. Transplantation of cells in matrices for tissue regeneration. Adv Drug Deliv Rev 1998; 33(1-2): 165-82.
[http://dx.doi.org/10.1016/S0169-409X(98)00025-8] [PMID: 10837658]
[225]
Freed LE, Vunjak-Novakovic G, Biron RJ, et al. Biodegradable polymer scaffolds for tissue engineering. Biotechnology (N Y) 1994; 12(7): 689-93.
[PMID: 7764913]
[226]
Mikos AG, Sarakinos G, Lyman MD, Ingber DE, Vacanti JP, Langer R. Prevascularization of porous biodegradable polymers. Biotechnol Bioeng 1993; 42(6): 716-23.
[http://dx.doi.org/10.1002/bit.260420606] [PMID: 18613104]
[227]
Freed LE, Vunjak-Novakovic G. Microgravity tissue engineering. In Vitro Cell Dev Biol Anim 1997; 33(5): 381-5.
[http://dx.doi.org/10.1007/s11626-997-0009-2] [PMID: 9196897]
[228]
Bursac N, Papadaki M, Cohen RJ, et al. Cardiac muscle tissue engineering: toward an in vitro model for electrophysiological studies. Am J Physiol 1999; 277(2): H433-44.
[PMID: 10444466]
[229]
Shin M, Ishii O, Sueda T, Vacanti JP. Contractile cardiac grafts using a novel nanofibrous mesh. Biomaterials 2004; 25(17): 3717-23.
[http://dx.doi.org/10.1016/j.biomaterials.2003.10.055] [PMID: 15020147]


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VOLUME: 26
ISSUE: 34
Year: 2020
Published on: 27 March, 2020
Page: [4285 - 4303]
Pages: 19
DOI: 10.2174/1381612826666200327161112
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