Injectable graphene oxide/hydrogel-based angiogenic gene delivery system for vasculogenesis and cardiac repair

ACS Nano

Volumn 8, Issue 8, 2014, Pages 8050-8062

  Paul, Arghya ^a,b,c   Hasan, Anwarul ^a,c,i   Kindi, Hamood Al ^e   Gaharwar, Akhilesh K ^d   Rao, Vijayaraghava T S ^f   Nikkhah, Mehdi ^a,c,j   Shin, Su Ryon ^a,b,c   Krafft, Dorothee ^a,c   Dokmeci, Mehmet R ^a,c   Shum Tim, Dominique ^e   Khademhosseini, Ali ^a,b,c,g,h  

^a HARVARD MEDICAL SCHOOL   (United States)

^b HARVARD UNIVERSITY   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^d TEXAS A AND M UNIVERSITY   (United States)

^e ROYAL VICTORIA HOSPITAL   (Canada)

^f MCGILL UNIVERSITY   (Canada)

^g Kyung Hee University   (South Korea)

^h KING ABDULAZIZ UNIVERSITY   (Saudi Arabia)

ⁱ AMERICAN UNIVERSITY OF BEIRUT   (Lebanon)

^j Arizona State University   (United States)

more..

Author keywords

gene delivery; graphene oxide; injectable hydrogel; myocardial therapy; nanomedicine

Indexed keywords

BIOCOMPATIBILITY; CARDIOLOGY; DISEASE CONTROL; ECHOCARDIOGRAPHY; ENDOTHELIAL CELLS; GENE THERAPY; GENE TRANSFER; GRAPHENE OXIDE; HYDROGELS; MEDICAL NANOTECHNOLOGY; POLYMERASE CHAIN REACTION; RNA;

ACUTE MYOCARDIAL INFARCTION; GENE DELIVERY; INJECTABLE HYDROGELS; ISCHEMIC HEART DISEASE; MYOCARDIAL THERAPY; NANOCOMPOSITE HYDROGELS; NON-VIRAL GENE DELIVERY; VASCULAR ENDOTHELIAL GROWTH FACTOR;

GRAPHENE;

DRUG CARRIER; GRAPHITE; HYDROGEL; OXIDE; POLYETHYLENEIMINE; VASCULOTROPIN A;

ANGIOGENESIS; ANIMAL; CARDIAC MUSCLE; CELL PROLIFERATION; CHEMISTRY; CYTOLOGY; FLOW KINETICS; GENE THERAPY; GENETICS; HUMAN; HYDROGEL; INJECTION; MEDICINAL CHEMISTRY; METABOLISM; MYOCARDIAL INFARCTION; PATHOPHYSIOLOGY; RAT; UMBILICAL VEIN ENDOTHELIAL CELL;

ANIMALS; CELL PROLIFERATION; CHEMISTRY, PHARMACEUTICAL; DRUG CARRIERS; GENETIC THERAPY; GRAPHITE; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; HYDROGEL; INJECTIONS; MYOCARDIAL INFARCTION; MYOCARDIUM; NEOVASCULARIZATION, PHYSIOLOGIC; OXIDES; POLYETHYLENEIMINE; RATS; RHEOLOGY; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84906673698     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/nn5020787     Document Type: Article

References (59)

1. Slaughter, B. V.; Khurshid, S. S.; Fisher, O. Z.; Khademhosseini, A.; Peppas, N. A. Hydrogels in Regenerative Medicine Adv. Mater. 2009, 21, 3307-3329
2. Langer, R.; Vacanti, J. P. Tissue Engineering Science 1993, 260, 920-926
3. Khademhosseini, A.; Vacanti, J. P.; Langer, R. Progress in Tissue Engineering Sci. Am. 2009, 300, 64-71
4. Khademhosseini, A.; Langer, R.; Borenstein, J.; Vacanti, J. P. Microscale Technologies for Tissue Engineering and Biology Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 2480-2487
5. Schukur, L.; Zorlutuna, P.; Cha, J. M.; Bae, H.; Khademhosseini, A. Directed Differentiation of Size-Controlled Embryoid Bodies towards Endothelial and Cardiac Lineages in RGD-Modified Poly(ethylene glycol) Hydrogels Adv. Healthcare Mater. 2013, 2, 195-205
6. Khetan, S.; Guvendiren, M.; Legant, W. R.; Cohen, D. M.; Chen, C. S.; Burdick, J. A. Degradation-Mediated Cellular Traction Directs Stem Cell Fate in Covalently Crosslinked Three-Dimensional Hydrogels Nat. Mater. 2013, 12, 458-465
7. Ashley, G. W.; Henise, J.; Reid, R.; Santi, D. V. Hydrogel Drug Delivery System with Predictable and Tunable Drug Release and Degradation Rates Proc. Natl. Acad. Sci. U.S.A. 2013, 110, 2318-2323
8. Jang, J. H.; Schaffer, D. V.; Shea, L. D. Engineering Biomaterial Systems to Enhance Viral Vector Gene Delivery Mol. Ther. 2011, 19, 1407-1415
9. Kong, H. J.; Liu, J.; Riddle, K.; Matsumoto, T.; Leach, K.; Mooney, D. J. Non-viral Gene Delivery Regulated by Stiffness of Cell Adhesion Substrates Nat. Mater. 2005, 4, 460-464
10. Cam, C.; Segura, T. Matrix-based Gene Delivery for Tissue Repair Curr. Opin. Biotechnol. 2013, 24, 855-863
11. Holladay, C.; Keeney, M.; Greiser, U.; Murphy, M.; OBrien, T.; Pandit, A. A Matrix Reservoir for Improved Control of Non-viral Gene Delivery J. Controlled Release 2009, 136, 220-225
12. Schek, R. M.; Hollister, S. J.; Krebsbach, P. H. Delivery and Protection of Adenoviruses using Biocompatible Hydrogels for Localized Gene Therapy Mol. Ther. 2004, 9, 130-138
13. Paul, A.; Shao, W.; Abbasi, S.; Shum-Tim, D.; Prakash, S. PAMAM Dendrimer-Baculovirus Nanocomplex for Microencapsulated Adipose Stem Cell-Gene Therapy: In Vitro and in Vivo Functional Assessment Mol. Pharmaceutics 2012, 9, 2479-2488
14. Hu, W. W.; Wang, Z.; Hollister, S. J.; Krebsbach, P. H. Localized Viral Vector Delivery to Enhance in Situ Regenerative Gene Therapy Gene Ther. 2007, 14, 891-901
15. Paul, A.; Elias, C. B.; Shum-Tim, D.; Prakash, S. Bioactive Baculovirus Nanohybrids for Stent Based Rapid Vascular Re-endothelialization Sci. Rep. 2013, 3, 2366
16. Curtin, C. M.; Cunniffe, G. M.; Lyons, F. G.; Bessho, K.; Dickson, G. R.; Duffy, G. P.; OBrien, F. J. Innovative Collagen Nano-hydroxyapatite Scaffolds Offer a Highly Efficient Non-viral Gene Delivery Platform for Stem Cell-Mediated Bone Formation Adv. Mater. 2012, 24, 749-754
17. Yin, L.; Song, Z.; Kim, K. H.; Zheng, N.; Gabrielson, N. P.; Cheng, J. Non-viral Gene Delivery via Membrane-penetrating, Mannose-Targeting Supramolecular Self-Assembled Nanocomplexes Adv. Mater. 2013, 25, 3063-3070
18. Kim, H.; Namgung, R.; Singha, K.; Oh, I. K.; Kim, W. J. Graphene oxide-Polyethylenimine Nanoconstruct as a Gene Delivery Vector and Bioimaging Tool Bioconjugate Chem. 2011, 22, 2558-2567
19. Feng, L.; Zhang, S.; Liu, Z. Graphene Based Gene Transfection Nanoscale 2011, 3, 1252-1257
20. Yin, D.; Li, Y.; Lin, H.; Guo, B.; Du, Y.; Li, X.; Jia, H.; Zhao, X.; Tang, J.; Zhang, L. Functional Graphene Oxide as a Plasmid-based Stat3 siRNA Carrier Inhibits Mouse Malignant Melanoma Growth in Vivo Nanotechnology 2013, 24, 105102
21. Kim, H.; Kim, W. J. Photothermally Controlled Gene Delivery by Reduced Graphene Oxide-Polyethylenimine Nanocomposite Small 2014, 10, 117-126
22. Bitounis, D.; Ali-Boucetta, H.; Hong, B. H.; Min, D. H.; Kostarelos, K. Prospects and Challenges of Graphene in Biomedical Applications Adv. Mater. 2013, 25, 2258-2268
23. Feng, L.; Yang, X.; Shi, X.; Tan, X.; Peng, R.; Wang, J.; Liu, Z. Polyethylene Glycol and Polyethylenimine Dual-functionalized Nano-graphene Oxide for Photothermally Enhanced Gene Delivery Small 2013, 9, 1989-1997
24. Nichol, J. W.; Koshy, S. T.; Bae, H.; Hwang, C. M.; Yamanlar, S.; Khademhosseini, A. Cell-Laden Microengineered Gelatin Methacrylate Hydrogels Biomaterials 2010, 31, 5536-5544
25. Chen, Y. C.; Lin, R. Z.; Qi, H.; Yang, Y.; Bae, H.; Melero-Martin, J. M.; Khademhosseini, A. Functional Human Vascular Network Generated in Photocrosslinkable Gelatin Methacrylate Hydrogels Adv. Funct. Mater. 2012, 22, 2027-2039
26. Lin, R. Z.; Chen, Y. C.; Moreno-Luna, R.; Khademhosseini, A.; Melero-Martin, J. M. Transdermal Regulation of Vascular Network Bioengineering using a Photopolymerizable Methacrylated Gelatin Hydrogel Biomaterials 2013, 34, 6785-6796
27. Nikkhah, M.; Eshak, N.; Zorlutuna, P.; Annabi, N.; Castello, M.; Kim, K.; Dolatshahi-Pirouz, A.; Edalat, F.; Bae, H.; Yang, Y. et al. Directed Endothelial Cell Morphogenesis in Micropatterned Gelatin Methacrylate Hydrogels Biomaterials 2012, 33, 9009-9018
28. Shin, S. R.; Bae, H.; Cha, J. M.; Mun, J. Y.; Chen, Y. C.; Tekin, H.; Shin, H.; Farshchi, S.; Dokmeci, M. R.; Tang, S. et al. Carbon Nanotube Reinforced Hybrid Microgels as Scaffold Materials for Cell Encapsulation ACS Nano 2012, 6, 362-372
29. Shin, S. R.; Jung, S. M.; Zalabany, M.; Kim, K.; Zorlutuna, P.; Kim, S. B.; Nikkhah, M.; Khabiry, M.; Azize, M.; Kong, J. et al. Carbon-Nanotube Embedded Hydrogel Sheets for Engineering Cardiac Constructs and Bioactuators ACS Nano 2013, 7, 2369-2380
30. Ramon-Azcon, J.; Ahadian, S.; Estili, M.; Liang, X.; Ostrovidov, S.; Kaji, H.; Shiku, H.; Ramalingam, M.; Nakajima, K.; Sakka, Y. et al. Dielectrophoretically Aligned Carbon Nanotubes to Control Electrical and Mechanical Properties of Hydrogels to Fabricate Contractile Muscle Myofibers Adv. Mater. 2013, 25, 4028-4034
31. Shin, S. R.; Aghaei-Ghareh-Bolagh, B.; Dang, T. T.; Topkaya, S. N.; Gao, X.; Yang, S. Y.; Jung, S. M.; Oh, J. H.; Dokmeci, M. R.; Tang, X. S. et al. Cell-Laden Microengineered and Mechanically Tunable Hybrid Hydrogels of Gelatin and Graphene Oxide Adv. Mater. 2013, 25, 6385-6391
32. Cha, C.; Shin, S. R.; Gao, X.; Annabi, N.; Dokmeci, M. R.; Tang, X. S.; Khademhosseini, A. Controlling Mechanical Properties of Cell-Laden Hydrogels by Covalent Incorporation of Graphene Oxide Small 2014, 10, 514-523
33. Mihaila, S. M.; Gaharwar, A. K.; Reis, R. L.; Marques, A. P.; Gomes, M. E.; Khademhosseini, A. Photocrosslinkable Kappa-carrageenan Hydrogels for Tissue Engineering Applications Adv. Healthcare Mater. 2013, 2, 895-907
34. Seif-Naraghi, S. B.; Singelyn, J. M.; Salvatore, M. A.; Osborn, K. G.; Wang, J. J.; Sampat, U.; Kwan, O. L.; Strachan, G. M.; Wong, J.; Schup-Magoffin, P. J. Safety and Efficacy of an Injectable Extracellular Matrix Hydrogel for Treating Myocardial Infarction Sci. Transl. Med. 2013, 5, 173ra25
35. Liu, Z.; Wang, H.; Wang, Y.; Lin, Q.; Yao, A.; Cao, F.; Li, D.; Zhou, J.; Duan, C.; Du, Z. et al. The Influence of Chitosan Hydrogel on Stem Cell Engraftment, Survival and Homing in the Ischemic Myocardial Microenvironment Biomaterials 2012, 33, 3093-3106
36. Shuman, J. A.; Zurcher, J. R.; Sapp, A. A.; Burdick, J. A.; Gorman, R. C.; Gorman, J. H., 3rd; Goldsmith, E. C.; Spinale, F. G. Localized Targeting of Biomaterials Following Myocardial Infarction: A Foundation to Build on Trends Cardiovasc. Med. 2013, 23, 301-311
37. MacArthur, J. W., Jr.; Purcell, B. P.; Shudo, Y.; Cohen, J. E.; Fairman, A.; Trubelja, A.; Patel, J.; Hsiao, P.; Yang, E.; Lloyd, K. et al. Sustained Release of Engineered Stromal Cell-derived Factor 1-alpha from Injectable Hydrogels Effectively Recruits Endothelial Progenitor Cells and Preserves Ventricular Function After Myocardial Infarction Circulation 2013, 128, S79-S86
38. Johnson, T. D.; Christman, K. L. Injectable Hydrogel Therapies and Their Delivery Strategies for Treating Myocardial Infarction Expert Opin. Drug Delivery 2013, 10, 59-72
39. Tous, E.; Purcell, B.; Ifkovits, J. L.; Burdick, J. A. Injectable Acellular Hydrogels for Cardiac Repair J. Cardiovasc. Transl. Res. 2011, 4, 528-542
40. Ifkovits, J. L.; Tous, E.; Minakawa, M.; Morita, M.; Robb, J. D.; Koomalsingh, K. J.; Gorman, J. H., 3rd; Gorman, R. C.; Burdick, J. A. Injectable Hydrogel Properties Influence Infarct Expansion and Extent of Postinfarction Left Ventricular Remodeling in an Ovine Model Proc. Natl. Acad. Sci. U.S.A. 2010, 107, 11507-11512
41. Paul, A.; Shao, W.; Shum-Tim, D.; Prakash, S. The Attenuation of Restenosis Following Arterial Gene Transfer Using Carbon Nanotube Coated Stent Incorporating TAT/DNA(Ang1+Vegf) Nanoparticles Biomaterials 2012, 33, 7655-7664
42. Paul, A.; Binsalamah, Z. M.; Khan, A. A.; Abbasia, S.; Elias, C. B.; Shum-Tim, D.; Prakash, S. A Nanobiohybrid Complex of Recombinant Baculovirus and Tat/DNA Nanoparticles for Delivery of Ang-1 Transgene in Myocardial Infarction Therapy Biomaterials 2011, 32, 8304-8318
43. Gerczuk, P. Z.; Kloner, R. A. An Update on Cardioprotection: A Review of the Latest Adjunctive Therapies To Limit Myocardial Infarction Size in Clinical Trials J. Am. Coll. Cardiol. 2012, 59, 969-978
44. Windecker, S.; Bax, J. J.; Myat, A.; Stone, G. W.; Marber, M. S. Future Treatment Strategies in ST-segment Elevation Myocardial Infarction Lancet 2013, 382, 644-657
45. Nabel, E. G.; Braunwald, E. A Tale of Coronary Artery Disease and Myocardial Infarction N. Engl. J. Med. 2012, 366, 54-63
46. Takahashi, K.; Ito, Y.; Morikawa, M.; Kobune, M.; Huang, J.; Tsukamoto, M.; Sasaki, K.; Nakamura, K.; Dehari, H.; Ikeda, K. et al. Adenoviral-delivered Angiopoietin-1 Reduces the Infarction and Attenuates the Progression of Cardiac Dysfunction in the Rat Model of Acute Myocardial Infarction Mol. Ther. 2003, 8, 584-592
47. Tao, Z.; Chen, B.; Tan, X.; Zhao, Y.; Wang, L.; Zhu, T.; Cao, K.; Yang, Z.; Kan, Y. W.; Su, H. Coexpression of VEGF and Angiopoietin-1 Promotes Angiogenesis and Cardiomyocyte Proliferation Reduces Apoptosis in Porcine Myocardial Infarction (MI) Heart Proc. Natl. Acad. Sci. U.S.A. 2011, 108, 2064-2069
48. Moore, C. S.; Rao, V. T.; Durafourt, B. A.; Bedell, B. J.; Ludwin, S. K.; Bar-Or, A.; Antel, J. P. miR-155 as a Multiple Sclerosis-Relevant Regulator of Myeloid Cell Polarization Ann. Neurol. 2013, 74, 709-720
49. OConnell, R. M.; Rao, D. S.; Baltimore, D. microRNA Regulation of Inflammatory Responses Annu. Rev. Immunol. 2012, 30, 295-312
50. Dai, R.; Ahmed, S. A. MicroRNA, a New Paradigm for Understanding Immunoregulation, Inflammation, and Autoimmune Diseases Transl. Res. 2011, 157, 163-179
51. Nazari-Jahantigh, M.; Wei, Y.; Schober, A. The role of microRNAs in arterial remodelling Thromb. Haemost. 2012, 107, 611-618
52. Boon, R. A.; Iekushi, K.; Lechner, S.; Seeger, T.; Fischer, A.; Heydt, S.; Kaluza, D.; Treguer, K.; Carmona, G.; Bonauer, A. et al. MicroRNA-34a Regulates Cardiac Ageing and Function Nature 2013, 495, 107-110
53. 2)-induced Apoptosis Through Targeting the Mitochondria Apoptotic Pathway PLoS One 2012, 7, e44907
54. Chowdhury, S. M.; Kanakia, S.; Toussaint, J. D.; Frame, M. D.; Dewar, A. M.; Shroyer, K. R.; Moore, W.; Sitharaman, B. In vitro Hematological and in Vivo Vasoactivity Assessment of Dextran Functionalized Graphene Sci. Rep 2013, 3, 2584
55. Yang, K.; Gong, H.; Shi, X.; Wan, J.; Zhang, Y.; Liu, Z. In vivo Biodistribution and Toxicology of Functionalized Nano-Graphene Oxide in Mice After Oral and Intraperitoneal Administration Biomaterials 2013, 34, 2787-2795
56. Yang, K.; Wan, J.; Zhang, S.; Zhang, Y.; Lee, S. T.; Liu, Z. In Vivo Pharmacokinetics, Long-Term Biodistribution, and Toxicology of PEGylated Graphene in Mice ACS Nano 2011, 5, 516-522
57. Liu, Y.; Luo, Y.; Wu, J.; Wang, Y.; Yang, X.; Yang, R.; Wang, B.; Yang, J.; Zhang, N. Graphene Oxide Can Induce in Vitro and in Vivo Mutagenesis Sci. Rep. 2013, 3, 3469
58. Qu, G.; Liu, S.; Zhang, S.; Wang, L.; Wang, X.; Sun, B.; Yin, N.; Gao, X.; Xia, T.; Chen, J. J.; Jiang, G. B. Graphene Oxide Induces Toll-like Receptor 4 (TLR4)-Dependent Necrosis in Macrophages ACS Nano 2013, 7, 5732-5745
59. Paul, A.; Srivastava, S.; Chen, G.; Shum-Tim, D.; Prakash, S. Functional Assessment of Adipose Stem Cells for Xenotransplantation using Myocardial Infarction Immunocompetent Models: Comparison with Bone Marrow Stem Cells Cell Biochem. Biophys. 2013, 67, 263-273