Magnetic Nano-Platform Enhanced iPSC-Derived Trabecular Meshwork Delivery and Tracking Efficiency

References

• Jonas JB, Aung T, Bourne RR, Bron AM, Ritch R, Panda-Jonas S. Glaucoma. Lancet. 2017;390(10108):2183–2193. doi:10.1016/s0140-6736(17)31469-1
   PubMed Web of Science ®Google Scholar
• Goel M, Picciani RG, Lee RK, Bhattacharya SK. Aqueous humor dynamics: a review. Open Ophthalmol J. 2010;4:52–59. doi:10.2174/1874364101004010052
   PubMedGoogle Scholar
• Fautsch MP, Johnson DH. Aqueous humor outflow: what do we know? Where will it lead us? Invest Ophthalmol Vis Sci. 2006;47(10):4181–4187. doi:10.1167/iovs.06-0830
   PubMed Web of Science ®Google Scholar
• Johnson M. What controls aqueous humour outflow resistance? Exp Eye Res. 2006;82(4):545–557. doi:10.1016/j.exer.2005.10.011
   PubMed Web of Science ®Google Scholar
• Jasien JV, Zohner YE, Asif SK, et al. Comparison of extraocular and intraocular pressure transducers for measurement of transient intraocular pressure fluctuations using continuous wireless telemetry. Sci Rep. 2020;10(1):20893. doi:10.1038/s41598-020-77880-8
   PubMed Web of Science ®Google Scholar
• Borghi V, Bastia E, Guzzetta M, et al. A novel nitric oxide releasing prostaglandin analog, NCX 125, reduces intraocular pressure in rabbit, dog, and primate models of glaucoma. J Ocul Pharmacol Ther. 2010;26(2):125–132. doi:10.1089/jop.2009.0120
   PubMed Web of Science ®Google Scholar
• Kaneko Y, Ohta M, Inoue T, et al. Effects of K-115 (Ripasudil), a novel ROCK inhibitor, on trabecular meshwork and Schlemm’s canal endothelial cells. Sci Rep. 2016;6:19640. doi:10.1038/srep19640
   PubMed Web of Science ®Google Scholar
• Chen W, Yang X, Fang J, Zhang Y, Yang X. Rho-associated protein kinase inhibitor treatment promotes proliferation and phagocytosis in trabecular meshwork cells. Front Pharmacol. 2020;11:302. doi:10.3389/fphar.2020.00302
   PubMed Web of Science ®Google Scholar
• Dikopf MS, Vajaranant TS, Edward DP. Topical treatment of glaucoma: established and emerging pharmacology. Expert Opin Pharmacother. 2017;18(9):885–898. doi:10.1080/14656566.2017.1328498
   PubMed Web of Science ®Google Scholar
• Manuguerra‐GagnÉ R, Boulos PR, Ammar A, et al. Transplantation of mesenchymal stem cells promotes tissue regeneration in a glaucoma model through laser-induced paracrine factor secretion and progenitor cell recruitment. Stem Cells. 2013;31(6):1136–1148.
   PubMed Web of Science ®Google Scholar
• Du Y, Roh DS, Mann MM, Funderburgh ML, Funderburgh JL, Schuman JS. Multipotent stem cells from trabecular meshwork become phagocytic TM cells. Invest Ophthalmol Vis Sci. 2012;53(3):1566–1575. doi:10.1167/iovs.11-9134
   PubMed Web of Science ®Google Scholar
• Yun H, Zhou Y, Wills A, Du Y. Stem cells in the trabecular meshwork for regulating intraocular pressure. J Ocul Pharmacol Ther. 2016;32(5):253–260. doi:10.1089/jop.2016.0005
   PubMed Web of Science ®Google Scholar
• Du Y, Yun H, Yang E, Schuman JS. Stem cells from trabecular meshwork home to TM tissue in vivo. Invest Ophthalmol Vis Sci. 2013;54(2):1450–1459. doi:10.1167/iovs.12-11056
   PubMed Web of Science ®Google Scholar
• Yun H, Wang Y, Zhou Y, et al. Human stem cells home to and repair laser-damaged trabecular meshwork in a mouse model. Commun Biol. 2018;1:216. doi:10.1038/s42003-018-0227-z
   PubMed Web of Science ®Google Scholar
• Zhu W, Gramlich OW, Laboissonniere L, et al. Transplantation of iPSC-derived TM cells rescues glaucoma phenotypes in vivo. Proc Natl Acad Sci U S A. 2016;113(25):E3492–E3500. doi:10.1073/pnas.1604153113
   PubMed Web of Science ®Google Scholar
• Zhu W, Godwin CR, Cheng L, Scheetz TE, Kuehn MH. Transplantation of iPSC-TM stimulates division of trabecular meshwork cells in human eyes. Sci Rep. 2020;10(1):2905. doi:10.1038/s41598-020-59941-0
   PubMed Web of Science ®Google Scholar
• Zhu W, Jain A, Gramlich OW, Tucker BA, Sheffield VC, Kuehn MH. Restoration of aqueous humor outflow following transplantation of ipsc-derived trabecular meshwork cells in a transgenic mouse model of glaucoma. Invest Ophthalmol Vis Sci. 2017;58(4):2054–2062. doi:10.1167/iovs.16-20672
   PubMed Web of Science ®Google Scholar
• Yu H, Miao Y, Chen W, et al. Expressional and functional involvement of gap junctions in aqueous humor outflow into the ocular trabecular meshwork of the anterior chamber. Mol Vis. 2019;25:255–265.
   PubMed Web of Science ®Google Scholar
• Sui S, Yu H, Wang X, et al. iPSC-derived trabecular meshwork cells stimulate endogenous TM cell division through gap junction in a mouse model of glaucoma. Invest Ophthalmol Vis Sci. 2021;62(10):28. doi:10.1167/iovs.62.10.28
   PubMed Web of Science ®Google Scholar
• Roubeix C, Godefroy D, Mias C, et al. Intraocular pressure reduction and neuroprotection conferred by bone marrow-derived mesenchymal stem cells in an animal model of glaucoma. Stem Cell Res Ther. 2015;6(1):177. doi:10.1186/s13287-015-0168-0
   PubMed Web of Science ®Google Scholar
• Swaminathan SS, Oh DJ, Kang MH, Rhee DJ. Aqueous outflow: segmental and distal flow. J Cataract Refract Surg. 2014;40(8):1263–1272. doi:10.1016/j.jcrs.2014.06.020
   PubMed Web of Science ®Google Scholar
• Snider EJ, Kubelick KP, Tweed K, et al. Improving stem cell delivery to the trabecular meshwork using magnetic nanoparticles. Sci Rep. 2018;8(1):12251. doi:10.1038/s41598-018-30834-7
   PubMed Web of Science ®Google Scholar
• Qian X, Kang H, Li R, et al. In vivo visualization of eye vasculature using super-resolution ultrasound microvessel imaging. IEEE Trans Biomed Eng. 2020;67:2870–2880. doi:10.1109/TBME.2020.2972514
   PubMed Web of Science ®Google Scholar
• Zhou L, Zhang X, Wang Q, et al. Molecular engineering of a TBET-based two-photon fluorescent probe for ratiometric imaging of living cells and tissues. J Am Chem Soc. 2014;136(28):9838–9841. doi:10.1021/ja504015t
   PubMed Web of Science ®Google Scholar
• Page MJ, Lourenço AL, David T, et al. Non-invasive imaging and cellular tracking of pulmonary emboli by near-infrared fluorescence and positron-emission tomography. Nat Commun. 2015;6:8448. doi:10.1038/ncomms9448
   PubMed Web of Science ®Google Scholar
• Schuman JS, Hee MR, Arya AV, et al. Optical coherence tomography: a new tool for glaucoma diagnosis. Curr Opin Ophthalmol. 1995;6(2):89–95. doi:10.1097/00055735-199504000-00014
   PubMedGoogle Scholar
• Konstantopoulos A, Hossain P, Anderson DF. Recent advances in ophthalmic anterior segment imaging: a new era for ophthalmic diagnosis? Br J Ophthalmol. 2007;91(4):551–557. doi:10.1136/bjo.2006.103408
   PubMed Web of Science ®Google Scholar
• Chen G, Zhang Y, Li C, Huang D, Wang Q, Wang Q. Recent advances in tracking the transplanted stem cells using near‐infrared fluorescent nanoprobes: turning from the first to the second near‐infrared window. Adv Healthcare Mater. 2018;7(20):1800497. doi:10.1002/adhm.201800497
   Web of Science ®Google Scholar
• Fu Y, Kraitchman DL. Stem cell labeling for noninvasive delivery and tracking in cardiovascular regenerative therapy. Expert Rev Cardiovasc Ther. 2010;8(8):1149–1160. doi:10.1586/erc.10.106
   PubMedGoogle Scholar
• Goodfellow F, Simchick GA, Mortensen LJ, Stice SL, Zhao Q. Tracking and quantification of magnetically labeled stem cells using magnetic resonance imaging. Adv Funct Mater. 2016;26(22):3899–3915. doi:10.1002/adfm.201504444
   PubMed Web of Science ®Google Scholar
• Xiong S, Kumar A, Tian S, Taher E, Yang E. Stem cell transplantation rescued a primary open-angle glaucoma mouse model. Elife. 2021;10:e63677. doi:10.7554/eLife.63677
   PubMed Web of Science ®Google Scholar
• Mandegar MA, Moralli D, Khoja S, et al. Functional human artificial chromosomes are generated and stably maintained in human embryonic stem cells. Hum Mol Genet. 2011;20(15):2905–2913. doi:10.1093/hmg/ddr144
   PubMed Web of Science ®Google Scholar
• Momeni A, Neelamegham S, Parashurama N. Current challenges for the targeted delivery and molecular imaging of stem cells in animal models. Bioengineered. 2016;8(4):316–324. doi:10.1080/21655979.2016.1233090
   PubMed Web of Science ®Google Scholar
• Naldini L, Blömer U, Gage FH, Trono D, Verma IM. Efficient transfer, integration, and sustained long-term expression of the transgene in adult rat brains injected with a lentiviral vector. Proc Natl Acad Sci U S A. 1996;93(21):11382–11388. doi:10.1073/pnas.93.21.11382
   PubMed Web of Science ®Google Scholar
• Wolfbeis OS. An overview of nanoparticles commonly used in fluorescent bioimaging. Chem Soc Rev. 2015;44(14):4743–4768. doi:10.1039/c4cs00392f
   PubMed Web of Science ®Google Scholar
• Mao W, Liu Y, Mody A, Montecchi-Palmer M, Wordinger RJ, Clark AF. Characterization of a spontaneously immortalized bovine trabecular meshwork cell line. Exp Eye Res. 2012;105:53–59. doi:10.1016/j.exer.2012.10.007
   PubMed Web of Science ®Google Scholar
• Clark AF, Wilson K, McCartney MD, Miggans ST, Kunkle M, Howe W. Glucocorticoid-induced formation of cross-linked actin networks in cultured human trabecular meshwork cells. Invest Ophthalmol Vis Sci. 1994;35(1):281–294.
   PubMed Web of Science ®Google Scholar
• Shepard AR, Jacobson N, Fingert JH, Stone EM, Sheffield VC, Clark AF. Delayed secondary glucocorticoid responsiveness of MYOC in human trabecular meshwork cells. Invest Ophthalmol Vis Sci. 2001;42(13):3173–3181.
   PubMed Web of Science ®Google Scholar
• Stamer WD, Clark AF. The many faces of the trabecular meshwork cell. Exp Eye Res. 2016;158:112–123. doi:10.1016/j.exer.2016.07.009
   PubMed Web of Science ®Google Scholar
• Mao W, Liu Y, Wordinger RJ, Clark AF. A magnetic bead-based method for mouse trabecular meshwork cell isolation. Invest Ophthalmol Vis Sci. 2013;54(5):3600–3606. doi:10.1167/iovs.13-12033
   PubMed Web of Science ®Google Scholar
• Niu C, Wang Z, Lu G, et al. Doxorubicin loaded superparamagnetic PLGA-iron oxide multifunctional microbubbles for dual-mode US/MR imaging and therapy of metastasis in lymph nodes. Biomaterials. 2013;34(9):2307–2317. doi:10.1016/j.biomaterials.2012.12.003
   PubMed Web of Science ®Google Scholar
• Yallapu MM, Chauhan N, Othman SF, et al. Implications of protein Corona on physico-chemical and biological properties of magnetic nanoparticles. Biomaterials. 2015;46:1–12. doi:10.1016/j.biomaterials.2014.12.045
   PubMed Web of Science ®Google Scholar
• Liu Y, Wang J. Effects of DMSA-coated Fe3O4 nanoparticles on the transcription of genes related to iron and osmosis homeostasis. Toxicol Sci. 2013;131(2):521–536. doi:10.1093/toxsci/kfs300
   PubMed Web of Science ®Google Scholar
• Rad AM, Janic B, Iskander A, Soltanian-Zadeh H, Arbab AS. Measurement of quantity of iron in magnetically labeled cells: comparison among different UV/VIS spectrometric methods. Biotechniques. 2007;43(5):627–636. doi:10.2144/000112599
   PubMed Web of Science ®Google Scholar
• Zhang L, Xue H, Gao C, et al. Imaging and cell targeting characteristics of magnetic nanoparticles modified by a functionalizable zwitterionic polymer with adhesive 3,4-dihydroxyphenyl-l-alanine linkages. Biomaterials. 2010;31(25):6582–6588. doi:10.1016/j.biomaterials.2010.05.018
   PubMed Web of Science ®Google Scholar
• Gao Y, Xie J, Chen H, et al. Nanotechnology-based intelligent drug design for cancer metastasis treatment. Biotechnol Adv. 2014;32(4):761–777. doi:10.1016/j.biotechadv.2013.10.013
   PubMed Web of Science ®Google Scholar
• Lee P-W, Hsu S-H, Wang -J-J, et al. The characteristics, biodistribution, magnetic resonance imaging and biodegradability of superparamagnetic core-shell nanoparticles. Biomaterials. 2010;31(6):1316–1324. doi:10.1016/j.biomaterials.2009.11.010
   PubMed Web of Science ®Google Scholar
• Wahajuddin AS. Superparamagnetic iron oxide nanoparticles: magnetic nanoplatforms as drug carriers. Int J Nanomedicine. 2012;7:3445–3471. doi:10.2147/IJN.S30320
   PubMed Web of Science ®Google Scholar
• Barrow M, Taylor A, Murray P, Rosseinsky MJ, Adams DJ. Design considerations for the synthesis of polymer coated iron oxide nanoparticles for stem cell labelling and tracking using MRI. Chem Soc Rev. 2015;44(19):6733–6748. doi:10.1039/c5cs00331h
   PubMed Web of Science ®Google Scholar
• Bulte JWM. Superparamagnetic iron oxides as MPI tracers: a primer and review of early applications. Adv Drug Deliv Rev. 2019;138:293–301. doi:10.1016/j.addr.2018.12.007
   PubMed Web of Science ®Google Scholar
• Cao J, Chen D, Huang S, Deng D, Tang L, Gu Y. Multifunctional near-infrared light-triggered biodegradable micelles for chemo- and photo-thermal combination therapy. Oncotarget. 2016;7(50):82170–82184. doi:10.18632/oncotarget.10320
   PubMedGoogle Scholar
• Cao J, Huang S, Chen Y, et al. Near-infrared light-triggered micelles for fast controlled drug release in deep tissue. Biomaterials. 2013;34(26):6272–6283. doi:10.1016/j.biomaterials.2013.05.008
   PubMed Web of Science ®Google Scholar
• Ding QJ, Zhu W, Cook AC, Anfinson KR, Tucker BA, Kuehn MH. Induction of trabecular meshwork cells from induced pluripotent stem cells. Invest Ophthalmol Vis Sci. 2014;55(11):7065–7072. doi:10.1167/iovs.14-14800
   PubMed Web of Science ®Google Scholar
• Sharma S, Parmar A, Kori S, Sandhir R. PLGA-based nanoparticles: a new paradigm in biomedical applications. Trends Analyt Chem. 2016;80:30–40. doi:10.1016/j.trac.2015.06.014
   Web of Science ®Google Scholar
• Han Z, Lv L, Ma Y, et al. Cypate-mediated thermosensitive nanoliposome for tumor imaging and photothermal triggered drug release. J Biophotonics. 2017;10(12):1607–1616. doi:10.1002/jbio.201600270
   PubMed Web of Science ®Google Scholar
• Halamoda Kenzaoui B, Chapuis Bernasconi C, Guney-Ayra S, Juillerat-Jeanneret L. Induction of oxidative stress, lysosome activation and autophagy by nanoparticles in human brain-derived endothelial cells. Biochem J. 2012;441(3):813–821. doi:10.1042/BJ20111252
   PubMed Web of Science ®Google Scholar
• Calero M, Gutiérrez L, Salas G, et al. Efficient and safe internalization of magnetic iron oxide nanoparticles: two fundamental requirements for biomedical applications. Nanomedicine. 2014;10(4):733–743. doi:10.1016/j.nano.2013.11.010
   PubMed Web of Science ®Google Scholar
• Bellusci M, La Barbera A, Padella F, et al. Biodistribution and acute toxicity of a nanofluid containing manganese iron oxide nanoparticles produced by a mechanochemical process. Int J Nanomedicine. 2014;9:1919–1929. doi:10.2147/IJN.S56394
   PubMed Web of Science ®Google Scholar
• Yu Z, Li Q, Wang J, et al. Reactive oxygen species-related nanoparticle toxicity in the biomedical field. Nanoscale Res Lett. 2020;15(1):115. doi:10.1186/s11671-020-03344-7
   PubMed Web of Science ®Google Scholar
• Liu C, Lin Z, Qiao C, et al. Hemocompatibility assay of a micro-catheter using hydrophilic coating biomaterials. Biomed Mater Eng. 2019;30(1):1–9. doi:10.3233/BME-181028
   PubMed Web of Science ®Google Scholar
• Tsatsakis A, Stratidakis A, Goryachaya A, et al. In vitro blood compatibility and in vitro cytotoxicity of amphiphilic poly-N-vinylpyrrolidone nanoparticles. Food Chem Toxicol. 2019;127:42–52. doi:10.1016/j.fct.2019.02.041
   PubMed Web of Science ®Google Scholar
• Amin K, Dannenfelser RM. In vitro hemolysis: guidance for the pharmaceutical scientist. J Pharm Sci. 2006;95(6):1173–1176. doi:10.1002/jps.20627
   PubMed Web of Science ®Google Scholar
• Huang AS, Mohindroo C, Weinreb RN. Aqueous humor outflow structure and function imaging at the bench and bedside: a review. J Clin Exp Ophthalmol. 2016;7(4):578. doi:10.4172/2155-9570.1000578
   PubMedGoogle Scholar
• Jun YW, Lee JH, Cheon J. Chemical design of nanoparticle probes for high-performance magnetic resonance imaging. Angew Chem Int Ed Engl. 2008;47(28):5122–5135. doi:10.1002/anie.200701674
   PubMed Web of Science ®Google Scholar
• Veiseh O, Gunn JW, Zhang M. Design and fabrication of magnetic nanoparticles for targeted drug delivery and imaging. Adv Drug Deliv Rev. 2010;62(3):284–304. doi:10.1016/j.addr.2009.11.002
   PubMed Web of Science ®Google Scholar
• Na HB, Song IC, Hyeon T. Inorganic nanoparticles for MRI contrast agents. Adv Mater. 2009;21(21):2133–2148. doi:10.1002/adma.200802366
   Web of Science ®Google Scholar
• Hossain ST, Mukherjee SK. CdO nanoparticle toxicity on growth, morphology, and cell division in Escherichia coli. Langmuir. 2012;28(48):16614–16622. doi:10.1021/la302872y
   PubMed Web of Science ®Google Scholar
• Salvati A, Åberg C, Dos Santos T, et al. Experimental and theoretical comparison of intracellular import of polymeric nanoparticles and small molecules: toward models of uptake kinetics. Nanomedicine. 2011;7(6):818–826. doi:10.1016/j.nano.2011.03.005
   PubMed Web of Science ®Google Scholar
• Bhargava-Shah A, Foygel K, Devulapally R, Paulmurugan R. Orlistat and antisense-miRNA-loaded PLGA-PEG nanoparticles for enhanced triple negative breast cancer therapy. Nanomedicine. 2016;11(3):235–247. doi:10.2217/nnm.15.193
   PubMed Web of Science ®Google Scholar
• Rojas JM, Sanz-Ortega L, Mulens-Arias V, Gutiérrez L, Pérez-Yagüe S, Barber DF. Superparamagnetic iron oxide nanoparticle uptake alters M2 macrophage phenotype, iron metabolism, migration and invasion. Nanomedicine. 2016;12(4):1127–1138. doi:10.1016/j.nano.2015.11.020
   PubMed Web of Science ®Google Scholar
• Petters C, Irrsack E, Koch M, Dringen R. Uptake and metabolism of iron oxide nanoparticles in brain cells. Neurochem Res. 2014;39(9):1648–1660. doi:10.1007/s11064-014-1380-5
   PubMed Web of Science ®Google Scholar
• Wang Y, Wang HH, Au D, Zou BS, Teng LS. Pitfalls in employing superparamagnetic iron oxide particles for stem cell labelling and in vivo MRI tracking. Br J Radiol. 2008;81(972):987–988. doi:10.1259/bjr/55991430
   PubMed Web of Science ®Google Scholar
• Schäfer R, Kehlbach R, Müller M, et al. Labeling of human mesenchymal stromal cells with superparamagnetic iron oxide leads to a decrease in migration capacity and colony formation ability. Cytotherapy. 2009;11(1):68–78. doi:10.1080/14653240802666043
   PubMed Web of Science ®Google Scholar
• Schäfer R, Bantleon R, Kehlbach R, et al. Functional investigations on human mesenchymal stem cells exposed to magnetic fields and labeled with clinically approved iron nanoparticles. BMC Cell Biol. 2010;11(1):22. doi:10.1186/1471-2121-11-22
   PubMedGoogle Scholar
• Farrell E, Wielopolski P, Pavljasevic P, et al. Effects of iron oxide incorporation for long term cell tracking on MSC differentiation in vitro and in vivo. Biochem Biophys Res Commun. 2008;369(4):1076–1081. doi:10.1016/j.bbrc.2008.02.159
   PubMed Web of Science ®Google Scholar
• Kubelick KP, Snider EJ, Ethier CR, Emelianov S. Photoacoustic properties of anterior ocular tissues. J Biomed Opt. 2019;24(5):1–11. doi:10.1117/1.JBO.24.5.056004
   PubMed Web of Science ®Google Scholar