Sustained delivery of proangiogenic microRNA-132 by nanoparticle transfection improves endothelial cell transplantation

FASEB Journal

Volumn 28, Issue 2, 2014, Pages 908-922

  Devalliere, Julie ^a,b   Chang, William G ^b   Andrejecsk, Jillian W ^a   Abrahimi, Parwiz ^b   Cheng, Christopher J ^a,c   Jane Wit, Dan ^b   Saltzman, W Mark ^a   Pober, Jordan S ^b  

^a Yale University   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c YALE UNIVERSITY   (United States)

Author keywords

Controlled release; Nanotechnology; Neovascularization; Tissue engineering

Indexed keywords

MICRORNA 132; NANOPARTICLE; SMALL INTERFERING RNA; VITRONECTIN RECEPTOR; MICRORNA;

ANGIOGENESIS; ARTICLE; CELL MIGRATION; CELL PROLIFERATION; CELL TRANSPLANTATION; GENE TARGETING; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SYNTHESIS; TISSUE ENGINEERING; TISSUE PERFUSION; UMBILICAL VEIN ENDOTHELIAL CELL; ANIMAL; CONFOCAL MICROSCOPY; CONTROLLED RELEASE; FEMALE; FLOW CYTOMETRY; GENETICS; METHODOLOGY; MOUSE; NANOTECHNOLOGY; NEOVASCULARIZATION (PATHOLOGY); REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCID MOUSE; TRANSPLANTATION; WESTERN BLOTTING;

CONTROLLED RELEASE; NANOTECHNOLOGY; NEOVASCULARIZATION; TISSUE ENGINEERING;

ANIMALS; BLOTTING, WESTERN; FEMALE; FLOW CYTOMETRY; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MICE; MICE, SCID; MICRORNAS; MICROSCOPY, CONFOCAL; NANOPARTICLES; NANOTECHNOLOGY; NEOVASCULARIZATION, PHYSIOLOGIC; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TISSUE ENGINEERING; TRANSFECTION;

EID: 84897096350     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.13-238527     Document Type: Article

References (56)

1. Rosenzweig, A. (2006) Cardiac cell therapy-mixed results from mixed cells. N. Engl. J. Med. 355, 1274-1277
2. Gibot, L., Galbraith, T., Huot, J., and Auger, F. A. (2010) A preexisting microvascular network benefits in vivo revascularization of a microvascularized tissue-engineered skin substitute. Tissue Eng. A 16, 3199-3206
3. Shepherd, B. R., Enis, D. R., Wang, F., Suarez, Y., Pober, J. S., and Schechner, J. S. (2006) Vascularization and engraftment of a human skin substitute using circulating progenitor cell-derived endothelial cells. FASEB J. 20, 1739-1741
4. Johnson, P. C., Mikos, A. G., Fisher, J. P., and Jansen, J. A. (2007) Strategic directions in tissue engineering. Tissue Eng. 13, 2827-2837
5. Jain, R. K., Au, P., Tam, J., Duda, D. G., and Fukumura, D. (2005) Engineering vascularized tissue. Nat. Biotechnol. 23, 821-823.
6. Schechner, J. S. Nath, A. K., Zheng, L., Kluger, M. S., Hughes, C. C., Sierra-Honigmann, M. R., Lorber, M. I., Tellides, G., Kashgarian, M., Bothwell, A. L., and Pober, J. S. (2000) In vivo formation of complex microvessels lined by human endothelial cells in an immunodeficient mouse. Proc. Natl. Acad. Sci. U. S. A. 97, 9191-9196
7. Enis, D. R. Shepherd, B. R., Wang, Y., Qasim, A., Shanahan, C. M., Weissberg, P. L., Kashgarian, M., Pober, J. S., and Schechner, J. S. (2005) Induction, differentiation, and remodeling of blood vessels after transplantation of Bcl-2-transduced endothelial cells. Proc. Natl. Acad. Sci. U. S. A. 102, 425-430
8. Jay, S. M., Shepherd, B. R., Bertram, J. P., Pober, J. S., and Saltzman, W. M. (2008) Engineering of multifunctional gels integrating highly efficient growth factor delivery with endothelial cell transplantation. FASEB J. 22, 2949-2956
9. Jay, S. M., and Saltzman, W. M. (2009) Controlled delivery of VEGF via modulation of alginate microparticle ionic crosslinking. J. Control. Release 134, 26-34
10. Jay, S. M. Shepherd, B. R., Andrejecsk, J. W., Kyriakides, T. R., Pober, J. S., and Saltzman, W. M. (2010) Dual delivery of VEGF and MCP-1 to support endothelial cell transplantation for therapeutic vascularization. Biomaterials 31, 3054-3062
11. Suárez, Y., and Sessa, W. C. (2009) MicroRNAs as novel regulators of angiogenesis. Circ. Res. 104, 442-454
12. Anand, S. Majeti, B. K., Acevedo, L. M., Murphy, E. A., Mukthavaram, R., Scheppke, L., Huang, M., Shields, D. J., Lindquist, J. N., Lapinski, P. E., King, P. D., Weis, S. M., and Cheresh, D. A. (2010) MicroRNA-132-mediated loss of p120RasGAP activates the endothelium to facilitate pathological angiogenesis. Nat. Med. 16, 909-914
13. Woodrow, K. A. Cu, Y., Booth, C. J., Saucier-Sawyer, J. K., Wood, M. J., and Saltzman, W. M. (2009) Intravaginal gene silencing using biodegradable polymer nanoparticles densely loaded with small-interfering RNA. Nat. Mater. 8, 526-533
14. Cheng, C. J., and Saltzman, W. M. (2011) Enhanced siRNA delivery into cells by exploiting the synergy between targeting ligands and cell-penetrating peptides. Biomaterials 32, 6194-6203
15. Cartiera, M. S., Johnson, K. M., Rajendran, V., Caplan, M. J., and Saltzman, W. M. (2009) The uptake and intracellular fate of PLGA nanoparticles in epithelial cells. Biomaterials 30, 2790-2798
16. Liu, X. Q., Song, W. J., Sun, T. M., Zhang, P. Z. and Wang, J. (2011) Targeted delivery of antisense inhibitor of miRNA for antiangiogenesis therapy using cRGD-functionalized nanoparticles. Mol. Pharm. 8, 250-259
17. Livak, K. J., and Schmittgen, T. D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25, 402-408
18. Chang, W. G., Andrejecsk, J. W., Kluger, M. S., Saltzman, W. M., and Poner, J. S. (2013) Pericytes modulate endothelial sprouting. [E-pub ahead of print] Cardiovasc. Res. doi: 10.1093/cvr/ cvt215
19. Babar, I. A. Cheng, C. J., Booth, C. J., Liang, X., Weidhaas, J. B., Saltzman, W. M., and Slack, F. J. (2012) Nanoparticle-based therapy in an in vivo microRNA-155 (miR-155)-dependent mouse model of lymphoma. Proc. Natl. Acad. Sci. U. S. A. 109, E1695-E1704
20. Ilan, N., Mahooti, S., and Madri, J. A. (1998) Distinct signal transduction pathways are utilized during the tube formation and survival phases of in vitro angiogenesis. J. Cell Sci. 111, 3621-3631
21. Maier, C. L., Shepherd, B. R., Yi, T., and Pober, J. S. (2010) Explant outgrowth, propagation and characterization of human pericytes. Microcirculation 17, 367-380
22. Nimesh, S. (2012) Recent patents in siRNA delivery employing nanoparticles as delivery vectors. Recent Patents DNA Gene Seq. 6, 91-97
23. Vercauteren, D. Vandenbroucke, R. E., Jones, A. T., Rejman, J., Demeester, J., De Smedt, S. C., Sanders, N. N., and Braeckmans, K. (2010) The use of inhibitors to study endocytic pathways of gene carriers: optimization and pitfalls. Mol. Ther. J. Am. Soc. Gene Ther. 18, 561-569
24. El-Sayed, A., and Harashima, H. (2013) Endocytosis of gene delivery vectors: from clathrin-dependent to lipid raft-mediated endocytosis. Mol. Ther. 21, 1118-1130
25. Ivanov, A. I. (2008) Pharmacological inhibition of endocytic pathways: is it specific enough to be useful? Methods Mol. Biol. 440, 15-33
26. Conner, S. D., and Schmid, S. L. (2003) Regulated portals of entry into the cell. Nature 422, 37-44
27. Ruoslahti, E., and Pierschbacher, M. D. (1987) New perspectives in cell adhesion: RGD and integrins. Science 238, 491-497
28. Brooks, P. C., Clark, R. A., and Cheresh, D. A. (1994) Requirement of vascular integrin alpha v beta 3 for angiogenesis. Science 264, 569-571
29. Costouros, N. G., Diehn, F. E., and Libutti, S. K. (2002) Molecular imaging of tumor angiogenesis. J. Cell. Biochem. Suppl. 39, 72-78
30. Desgrosellier, J. S., and Cheresh, D. A. (2010) Integrins in cancer: biological implications and therapeutic opportunities. Nat. Rev. Cancer 10, 9-22
31. Danhier, F., Pourcelle, V., Marchand-Brynaert, J., Jérôme, C., Feron, O., and Préat, V. (2012) Targeting of tumor endothelium by RGDgrafted PLGA-nanoparticles. Methods Enzymol. 508, 157-175
32. Murphy, E. A. Majeti, B. K., Barnes, L. A., Makale, M., Weis, S. M., Lutu-Fuga, K., Wrasidlo, W., and Cheresh, D. A. (2008) Nanoparticle-mediated drug delivery to tumor vasculature suppresses metastasis. Proc. Natl. Acad. Sci. U. S. A. 105, 9343-9348
33. Pollinger, K. Hennig, R., Ohlmann, A., Fuchshofer, R., Wenzel, R., Breunig, M., Tessmar, J., Tamm, E. R., and Goepferich, A. (2013) Ligand-functionalized nanoparticles target endothelial cells in retinal capillaries after systemic application. Proc. Natl. Acad. Sci. U. S. A. 110, 6115-6120
34. Yigit, M., Ghosh, S., Zdravka Medarova, Z., and Moore, A. V. (2011) Abstract 2952: Image-guided miRNA therapy for metastatic breast cancer. Cancer Res. 72, 2952-2952
35. Zhou, J., Patel, T., Fu, M., Bertram, J. B., and Saltzman, W. M. (2012) (2012) Octa-functional PLGA nanoparticles for targeted and efficient siRNA delivery to tumors. Biomaterials 33, 583-591
36. Wiggins, J. F., Ruffino, L., Kelnar, K., Omotola, M., Patrawala, L., Brown, D., Bader, A. G. (2010) Development of a lung cancer therapeutic based on the tumor suppressor microRNA-34. Cancer Res. 70, 5923-5930
37. Johnson, S. M., Grosshans, H., Shingara, J., Byrom, M., Jarvis, R., Cheng, A., Labourier, E., Reinert, K. L., Brown, D., and Slack, F. J. (2005) RAS is regulated by the let-7 microRNA family. Cell 120, 635-647
38. Trang, P., Medina, P. P., Wiggins, J. F., Ruffino, L., Kelnar, K., Omotola, M., Homer, R., Brown, D., Bader, A. G., Weidhaas, J. B., and Slack, F. J. (2010) Regression of murine lung tumors by the let-7 microRNA. Oncogene 29, 1580-1587
39. Lanford, R. E., Hildebrandt-Eriksen, E. S., Petri, A., Persson, R., Lindow, M., Munk, M. E., Kauppinen, S., and ørum, H. (2010) Therapeutic silencing of microRNA-122 in primates with chronic hepatitis C virus infection. Science 327, 198-201
40. Jopling, C. L., Yi, M., Lancaster, A. M., Lemon, S. M., and Sarnow, P. (2005) Modulation of hepatitis C virus RNA abundance by a liver-specific MicroRNA. Science 309, 1577-1581
41. Breunig, M., Lungwitz, U., Liebl, R., and Goepferich, A. (2007) Breaking up the correlation between efficacy and toxicity for nonviral gene delivery. Proc. Natl. Acad. Sci. USA 104, 14454-14459
42. Lv, H., Zhang, S., Wang, B., Cui, S., and Yan, J. (2006) Toxicity of cationic lipids and cationic polymers in gene delivery. J. Control Release 114, 100-109
43. Khazanov, E., Simberg, D., and Barenholz, Y. (2006) Lipoplexes prepared from cationic liposomes and mammalian DNA induce CpG-independent, direct cytotoxic effects in cell cultures and in mice. J. Gene Med. 8, 998-1007
44. Szebeni, J., Muggia, F., Gabizon, A., and Barenholz, Y. (2011) Activation of complement by therapeutic liposomes and other lipid excipient-based therapeutic products: prediction and prevention. Adv. Drug Deliv. Rev. 63, 1020-1030
45. Conwell, C. C., Liu, F. and Huang, L. (2007) Several serum proteins significantly decrease inflammatory response to lipidbased non-viral vectors. Mol. Ther. 16, 370-377
46. Bergers, G., and Hanahan, D. (2008) Modes of resistance to anti-angiogenic therapy. Nat. Rev. Cancer 8, 592-603
47. Anand, S., and Cheresh, D. A. (2011) MicroRNA-mediated regulation of the angiogenic switch. Curr. Opin. Hematol. 18, 171-176
48. Katare, R. Riu, F., Mitchell, K., Gubernator, M., Campagnolo, P., Cui, Y., Fortunato, O., Avolio, E., Cesselli, D., Beltrami, A. P., Angelini, G., Emanueli, C., and Madeddu, P. (2011) Transplantation of human pericyte progenitor cells improves the repair of infarcted heart through activation of an angiogenic program involving micro-RNA-132. Circ. Res. 109, 894-906
49. Gomes, R. S. M., das Neves, R. P., Cochlin, L., Lima, A., Carvalho, R., Korpisalo, P., Dragneva, G., Turunen, M., Liimatainen, T., Clarke, K., Ylä-Herttuala, S., Carr, C., and Ferreira, L. (2013) Efficient pro-survival/angiogenic miRNA delivery by an MRI-detectable nanomaterial. ACS Nano 7, 3362-3372
50. Stratman, A. N., Schwindt, A. E., Malotte, K. M., and Davis, G. E. (2010) Endothelial-derived PDGF-BB and HB-EGF coordinately regulate pericyte recruitment during vasculogenic tube assembly and stabilization. Blood 116, 4720-4730
51. Bramfeldt, H., Sabra, G., Centis, V., and Vermette, P. (2010) Scaffold vascularization: a challenge for three-dimensional tissue engineering. Curr. Med. Chem. 17, 3944-3967
52. Assmus, B., Honold, J., Schächinger, V., Britten, M. B., Fischer- Rasokat, U., Lehmann, R., Teupe, C., Pistorius, K., Martin, H., Abolmaali, N. D., Tonn, T., Dimmeler, S., and Zeiher, A. M. (2006) Transcoronary transplantation of progenitor cells after myocardial infarction. N. Engl. J. Med. 355, 1222-1232
53. Lunde, K., Solheim, S., Aakhus, S., Arnesen, H., Abdelnoor, M., Egeland, T., Endresen, K., Ilebekk, A., Mangschau, A., Fjeld, J. G., Smith, H. J., Taraldsrud, E., Grøgaard, H. K., Bjørnerheim, R., Brekke, M., Müller, C., Hopp, E., Ragnarsson, A., Brinchmann, J. E., and Forfang, K. (2006) Intracoronary injection of mononuclear bone marrow cells in acute myocardial infarction. N. Engl. J. Med. 355, 1199-1209
54. Fischer-Rasokat, U., Assmus, B., Seeger, F. H., Honold, J., Leistner, D., Fichtlscherer, S., Schächinger, V., Tonn, T., Martin, H., Dimmeler, S., and Zeiher, AM. (2009) A pilot trial to assess potential effects of selective intracoronary bone marrowderived progenitor cell infusion in patients with nonischemic dilated cardiomyopathy: final 1-year results of the transplantation of progenitor cells and functional regeneration enhancement pilot trial in patients with nonischemic dilated cardiomyopathy. Circ. Heart Fail. 2, 417-423
55. Gui, L., Muto, A., Chan, S. A., Breuer, C. K., and Niklason, L. E. (2009) Development of decellularized human umbilical arteries as small-diameter vascular grafts. Tissue Eng. A 15, 2665-2676
56. Motlagh, D., Allen, J., Hoshi, R., Yang, J., Lui, K., and Ameer, G. (2007) Hemocompatibility evaluation of poly(diol citrate) in vitro for vascular tissue engineering. J. Biomed. Mater. Res. A 82, 907-916