journal article·2017-10-01Open access

Topical tissue nano-transfection mediates non-viral stroma reprogramming and rescue

Daniel Gallego-Perez, Durba Pal, Subhadip Ghatak, Veysi Malkoc, Natalia Higuita-Castro, Surya Gnyawali, Lingqian Chang, Wei-Ching Liao, Junfeng Shi, Mithun Sinha, Kanhaiya Singh, Erin Steen, Alec Sunyecz, Richard Stewart, Jordan Moore, Thomas Ziebro, Robert G. Northcutt, Michael Homsy, Paul Bertani, Wu Lu, Sashwati Roy, Savita Khanna, Cameron Rink, Vishnu Baba Sundaresan, Jose J. Otero, L. James Lee, Chandan K. Sen

Nature Nanotechnology· Volume 12· Issue 10

Abstract

Although cellular therapies represent a promising strategy for a number of conditions, current approaches face major translational hurdles, including limited cell sources and the need for cumbersome pre-processing steps (for example, isolation, induced pluripotency). In vivo cell reprogramming has the potential to enable more-effective cell-based therapies by using readily available cell sources (for example, fibroblasts) and circumventing the need for ex vivo pre-processing. Existing reprogramming methodologies, however, are fraught with caveats, including a heavy reliance on viral transfection. Moreover, capsid size constraints and/or the stochastic nature of status quo approaches (viral and non-viral) pose additional limitations, thus highlighting the need for safer and more deterministic in vivo reprogramming methods. Here, we report a novel yet simple-to-implement non-viral approach to topically reprogram tissues through a nanochannelled device validated with well-established and newly developed reprogramming models of induced neurons and endothelium, respectively. We demonstrate the simplicity and utility of this approach by rescuing necrotizing tissues and whole limbs using two murine models of injury-induced ischaemia.
Source: europepmc · Quality: candidate unverified · Source record ↗

Research context

OpenAlex topics: Pluripotent Stem Cells Research · Neuroscience and Neural Engineering · RNA Interference and Gene Delivery

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

References (31)

Show source-provided references
1. Rosova, I., Dao, M., Capoccia, B., Link, D. & Nolta, J. A. Hypoxic preconditioning results in increased motility and improved therapeutic potential of human mesenchymal stem cells. Stem Cells 26, 2173–2182 (2008).10.1634/stemcells.2007-1104 ↗
2. Kinoshita, M. et al. Long-term clinical outcome after intramuscular transplantation of granulocyte colony stimulating factor-mobilized CD34 positive cells in patients with critical limb ischemia. Atherosclerosis 224, 440–445 (2012).10.1016/j.atherosclerosis.2012.07.031 ↗
3. Losordo, D. W. & Dimmeler, S. Therapeutic angiogenesis and vasculogenesis for ischemic disease. Part II: cell-based therapies. Circulation 109, 2692–2697 (2004).10.1161/01.CIR.0000128596.49339.05 ↗
4. Lee, A. S., Tang, C., Rao, M. S., Weissman, I. L . & Wu, J. C. Tumorigenicity as a clinical hurdle for pluripotent stem cell therapies. Nat. Med. 19, 998–1004 (2013).10.1038/nm.3267 ↗
5. Cunningham, J. J., Ulbright, T. M., Pera, M. F. & Looijenga, L. H. Lessons from human teratomas to guide development of safe stem cell therapies. Nat. Biotechnol. 30, 849–857 (2012).10.1038/nbt.2329 ↗
6. Leduc, P. R. et al. Towards an in vivo biologically inspired nanofactory. Nat. Nanotech. 2, 3–7 (2007).10.1038/nnano.2006.180 ↗
7. Heinrich, C. & Spagnoli, F. M. & Berninger, B. In vivo reprogramming for tissue repair. Nat. Cell Biol. 17, 204–211 (2015).10.1038/ncb3108 ↗
8. Karagiannis, P. & Yamanaka, S. The fate of cell reprogramming. Nat. Methods 11, 1006–1008 (2014).10.1038/nmeth.3109 ↗
9. Grande, A. et al. Environmental impact on direct neuronal reprogramming in vivo in the adult brain. Nat. Commun. 4, 2373 (2013).10.1038/ncomms3373 ↗
10. Morita, R. et al. ETS transcription factor ETV2 directly converts human fibroblasts into functional endothelial cells. Proc. Natl Acad. Sci. USA 112, 160–165 (2015).10.1073/pnas.1413234112 ↗
11. Gallego-Perez, D. et al. Deterministic transfection drives efficient nonviral reprogramming and uncovers reprogramming barriers. Nanomedicine 12, 399–409 (2016).10.1016/j.nano.2015.11.015 ↗
12. Marx, V. Cell biology: delivering tough cargo into cells. Nat. Methods 13, 37–40 (2016).10.1038/nmeth.3693 ↗
13. Boukany, P. E. et al. Nanochannel electroporation delivers precise amounts of biomolecules into living cells. Nat. Nanotech. 6, 747–754 (2011).10.1038/nnano.2011.164 ↗
14. Sen, C. K. & Ghatak, S. miRNA control of tissue repair and regeneration. Am. J. Pathol. 185, 2629–2640 (2015).10.1016/j.ajpath.2015.04.001 ↗
15. Vierbuchen, T. et al. Direct conversion of fibroblasts to functional neurons by defined factors. Nature 463, 1035–1041 (2010).10.1038/nature08797 ↗
16. Valadi, H. et al. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat. Cell Biol. 9, 654–659 (2007).10.1038/ncb1596 ↗
17. Davis, D. M. & Sowinski, S. Membrane nanotubes: dynamic long-distance connections between animal cells. Nat. Rev. Mol. Cell Biol. 9, 431–436 (2008).10.1038/nrm2399 ↗
18. Khanna, S. et al. Loss of miR-29b following acute ischemic stroke contributes to neural cell death and infarct size. J. Cereb. Blood Flow Metab. 33, 1197–1206 (2013).10.1038/jcbfm.2013.68 ↗
19. Venugopal, V. & Sundaresan, V. B. Polypyrrole-based amperometric cation sensor with tunable sensitivity. J. Intel. Mat. Syst. Str. 27, 1702–1709 (2016).10.1177/1045389X15604233 ↗
20. Venugopal, V., Venkatesh, V., Northcutt, R. G., Maddox, J. & Sundaresan, V. B. Nanoscale polypyrrole sensors for near-field electrochemical measurements. Sensors Actuat. B Chem. 242, 1193–1200 (2017).10.1016/j.snb.2016.09.121 ↗
21. Hunt, D. P. et al. A highly enriched niche of precursor cells with neuronal and glial potential within the hair follicle dermal papilla of adult skin. Stem Cells 26, 163–172 (2008).10.1634/stemcells.2007-0281 ↗
22. Higgins, C. A . et al. Reprogramming of human hair follicle dermal papilla cells into induced pluripotent stem cells. J. Invest. Dermatol. 132, 1725–1727 (2012).10.1038/jid.2012.12 ↗
23. Helisch, A. et al. Impact of mouse strain differences in innate hindlimb collateral vasculature. Arterioscler. Thromb. Vasc. Biol. 26, 520–526 (2006).10.1161/01.ATV.0000202677.55012.a0 ↗
24. Chalothorn, D., Clayton, J. A., Zhang, H., Pomp, D. & Faber, J. E. Collateral density, remodeling, and VEGF-A expression differ widely between mouse strains. Physiol. Genomics 30, 179–191 (2007).10.1152/physiolgenomics.00047.2007 ↗
25. Anokye-Danso, F. et al. Highly efficient miRNA-mediated reprogramming of mouse and human somatic cells to pluripotency. Cell Stem Cell 8, 376–388 (2011).10.1016/j.stem.2011.03.001 ↗
26. Limbourg, A. et al. Evaluation of postnatal arteriogenesis and angiogenesis in a mouse model of hind-limb ischemia. Nat. Protoc. 4, 1737–1746 (2009).10.1038/nprot.2009.185 ↗
27. Fiedler, G. B. et al. Localized semi-LASER dynamic 31P magnetic resonance spectroscopy of the soleus during and following exercise at 7 T. MAGMA 28, 493–501 (2015).10.1007/s10334-015-0484-5 ↗
28. Gnyawali, S. C. et al. High-frequency high-resolution echocardiography: first evidence on non-invasive repeated measure of myocardial strain, contractility, and mitral regurgitation in the ischemia-reperfused murine heart. J. Vis. Exp. 2010, e1781 (2010).
29. Roy, S . et al. Transcriptome-wide analysis of blood vessels laser captured from human skin and chronic wound-edge tissue. Proc. Natl Acad. Sci. USA 104, 14472–14477 (2007).10.1073/pnas.0706793104 ↗
30. Rink, C. et al. Oxygen-sensitive outcomes and gene expression in acute ischemic stroke. J. Cereb. Blood Flow Metab. 30, 1275–1287 (2010).10.1038/jcbfm.2010.7 ↗
31. Roy, S., Khanna, S., Rink, C., Biswas, S. & Sen, C. K. Characterization of the acute temporal changes in excisional murine cutaneous wound inflammation by screening of the wound-edge transcriptome. Physiol. Genomics 34, 162–184 (2008).10.1152/physiolgenomics.00045.2008 ↗