Knockdown of TNF-α by DNAzyme gold nanoparticles as an anti-inflammatory therapy for myocardial infarction

Biomaterials

Volumn 83, Issue , 2016, Pages 12-22

  Somasuntharam, Inthirai ^a,b   Yehl, Kevin ^c   Carroll, Sheridan L ^a   Maxwell, Joshua T ^a   Martinez, Mario D ^a   Che, Pao Lin ^a   Brown, Milton E ^a,b   Salaita, Khalid ^c   Davis, Michael E ^a,b  

^a GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c EMORY UNIVERSITY   (United States)

Author keywords

Deoxyribozyme (DNAzyme); Gene regulation; Myocardial infarction; Nanoparticles; Tumor necrosis factor (TNF )

Indexed keywords

CARDIOLOGY; DNA; FIBER OPTIC SENSORS; GENE EXPRESSION; GENES; GLYCOPROTEINS; GOLD; LIPOSOMES; MACROPHAGES; METAL NANOPARTICLES; TUMORS;

ANTI-INFLAMMATORIES; ANTI-INFLAMMATORY EFFECTS; DNAZYME; FUNCTIONALIZED GOLD NANOPARTICLES; GOLD NANOPARTICLES; MYOCARDIAL INFARCTION; POTENTIAL IMPACTS; TUMOR NECROSIS FACTORS;

NANOPARTICLES;

DEOXYRIBOZYME; GOLD NANOPARTICLE; LIPOFECTAMINE; TUMOR NECROSIS FACTOR ALPHA; ANTIINFLAMMATORY AGENT; GOLD; METAL NANOPARTICLE; TUMOR NECROSIS FACTOR;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CONJUGATE; CONJUGATION; CONTROLLED STUDY; GENE CONTROL; HEART FUNCTION; HEART INFARCTION; IN VIVO STUDY; MACROPHAGE; NONHUMAN; PRIORITY JOURNAL; RAT; ANIMAL; CARDIAC MUSCLE CELL; CELL DEATH; CHEMISTRY; COMPLICATION; DRUG EFFECTS; ENDOCYTOSIS; FLUORESCENCE; GENE SILENCING; GENETICS; HEART; HEART FUNCTION TEST; INFLAMMATION; METABOLISM; MOUSE; MYOCARDIAL INFARCTION; PATHOLOGY; PATHOPHYSIOLOGY; RAW 264.7 CELL LINE; SPRAGUE DAWLEY RAT; TISSUE DISTRIBUTION;

ANIMALS; ANTI-INFLAMMATORY AGENTS; CELL DEATH; DNA, CATALYTIC; ENDOCYTOSIS; FLUORESCENCE; GENE KNOCKDOWN TECHNIQUES; GOLD; HEART; HEART FUNCTION TESTS; INFLAMMATION; MACROPHAGES; METAL NANOPARTICLES; MICE; MYOCARDIAL INFARCTION; MYOCYTES, CARDIAC; RATS, SPRAGUE-DAWLEY; RAW 264.7 CELLS; TISSUE DISTRIBUTION; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84958041048     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2015.12.022     Document Type: Article

References (58)

1. Go A.S., Mozaffarian D., Roger V.L., Benjamin E.J., Berry J.D., Blaha M.J., et al. Heart disease and stroke statistics-2014 update: a report from the american heart association. Circulation 2014, 129:e28-e292.
2. Kereiakes D.J. Adjunctive pharmacotherapy before percutaneous coronary intervention in non-ST-elevation acute coronary syndromes: the role of modulating inflammation. Circulation 2003, 108:III22-7.
3. Nahrendorf M., Swirski F.K., Aikawa E., Stangenberg L., Wurdinger T., Figueiredo J.L., et al. The healing myocardium sequentially mobilizes two monocyte subsets with divergent and complementary functions. J. Exp. Med. 2007, 204:3037-3047.
4. Swirski F.K., Nahrendorf M., Etzrodt M., Wildgruber M., Cortez-Retamozo V., Panizzi P., et al. Identification of splenic reservoir monocytes and their deployment to inflammatory sites. Science 2009, 325:612-616.
5. Frangogiannis N.G., Smith C.W., Entman M.L. The inflammatory response in myocardial infarction. Cardiovasc Res. 2002, 53:31-47.
6. Troidl C., Mollmann H., Nef H., Masseli F., Voss S., Szardien S., et al. Classically and alternatively activated macrophages contribute to tissue remodelling after myocardial infarction. J. Cell. Mol. Med. 2009, 13:3485-3496.
7. Bonvini R.F. Inflammatory response post-myocardial infarction and reperfusion: a new therapeutic target?. Eur. Heart J. Suppl. 2005, 7:I27-I36.
8. Frangogiannis N.G. Targeting the inflammatory response in healing myocardial infarcts. Curr. Med. Chem. 2006, 13:1877-1893.
9. Kempf T., Zarbock A., Vestweber D., Wollert K.C. Anti-inflammatory mechanisms and therapeutic opportunities in myocardial infarct healing. J. Mol. Med. Berl. 2012, 90:361-369.
10. Nian M., Lee P., Khaper N., Liu P. Inflammatory cytokines and postmyocardial infarction remodeling. Circ. Res. 2004, 94:1543-1553.
11. Bozkurt B., Kribbs S.B., Clubb F.J., Michael L.H., Didenko V.V., Hornsby P.J., et al. Pathophysiologically relevant concentrations of tumor necrosis factor-alpha promote progressive left ventricular dysfunction and remodeling in rats. Circulation 1998, 97:1382-1391.
12. Kleinbongard P., Schulz R., Heusch G. TNFalpha in myocardial ischemia/reperfusion, remodeling and heart failure. Heart Fail Rev. 2011, 16:49-69.
13. Pagani F.D., Baker L.S., Hsi C., Knox M., Fink M.P., Visner M.S. Left ventricular systolic and diastolic dysfunction after infusion of tumor necrosis factor-alpha in conscious dogs. J. Clin. Investig. 1992, 90:389-398.
14. Sack M. Tumor necrosis factor-alpha in cardiovascular biology and the potential role for anti-tumor necrosis factor-alpha therapy in heart disease. Pharmacol. Ther. 2002, 94:123-135.
15. Sivasubramanian N., Coker M.L., Kurrelmeyer K.M., MacLellan W.R., DeMayo F.J., Spinale F.G., et al. Left ventricular remodeling in transgenic mice with cardiac restricted overexpression of tumor necrosis factor. Circulation 2001, 104:826-831.
16. Levine B., Kalman J., Mayer L., Fillit H.M., Packer M. Elevated circulating levels of tumor necrosis factor in severe chronic heart failure. N. Engl. J. Med. 1990, 323:236-241.
17. Irwin M.W., Mak S., Mann D.L., Qu R., Penninger J.M., Yan a, et al. Tissue expression and immunolocalization of tumor necrosis factor-alpha in postinfarction dysfunctional myocardium. Circulation 1999, 99:1492-1498.
18. Jacobs M., Staufenberger S., Gergs U., Meuter K., Brandstatter K., Hafner M., et al. Tumor necrosis factor-alpha at acute myocardial infarction in rats and effects on cardiac fibroblasts. J. Mol. Cell Cardiol. 1999, 31:1949-1959.
19. Kurrelmeyer K.M., Michael L.H., Baumgarten G., Taffet G.E., Peschon J.J., Sivasubramanian N., et al. Endogenous tumor necrosis factor protects the adult cardiac myocyte against ischemic-induced apoptosis in a murine model of acute myocardial infarction. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:5456-5461.
20. Anker S.D., Coats A.J. How to recover from renaissance? The significance of the results of recover, renaissance, renewal and attach. Int. J. Cardiol. 2002, 86:123-130.
21. Gilleron J., Querbes W., Zeigerer A., Borodovsky A., Marsico G., Schubert U., et al. Image-based analysis of lipid nanoparticle-mediated siRNA delivery, intracellular trafficking and endosomal escape. Nat. Biotechnol. 2013, 31:638-646.
22. Czech B., Hannon G.J. Small RNA sorting: matchmaking for Argonautes. Nat. Rev. Genet. 2011, 12:19-31.
23. Lv H., Zhang S., Wang B., Cui S., Yan J. Toxicity of cationic lipids and cationic polymers in gene delivery. J. Control Release 2006, 114:100-109.
24. Rosi N.L., Giljohann D.A., Thaxton C.S., Lytton-Jean A.K., Han M.S., Mirkin C.A. Oligonucleotide-modified gold nanoparticles for intracellular gene regulation. Science 2006, 312:1027-1030.
25. Cutler J.I., Auyeung E., Mirkin C.A. Spherical nucleic acids. J. Am. Chem. Soc. 2012, 134:1376-1391.
26. Cutler J.I., Auyeung E., Mirkin C.A. Spherical nucleic acids. J. Am. Chem. Soc. 2012, 134:1376-1391.
27. Choi C.H.J., Hao L.L., Narayan S.P., Auyeung E., Mirkin C.A. Mechanism for the endocytosis of spherical nucleic acid nanoparticle conjugates. P Natl. Acad. Sci. U. S. A. 2013, 110:7625-7630.
28. Wu X.C.A., Choi C.H.J., Zhang C., Hao L.L., Mirkin C.A. Intracellular fate of spherical nucleic acid nanoparticle conjugates. J. Am. Chem. Soc. 2014, 136:7726-7733.
29. Zheng D., Giljohann D.A., Chen D.L., Massich M.D., Wang X.Q., Iordanov H., et al. Topical delivery of siRNA-based spherical nucleic acid nanoparticle conjugates for gene regulation. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:11975-11980.
30. Jensen S.A., Day E.S., Ko C.H., Hurley L.A., Luciano J.P., Kouri F.M., et al. Spherical nucleic acid nanoparticle conjugates as an RNAi-based therapy for glioblastoma. Sci. Transl. Med. 2013, 5:209. ra152.
31. Bhindi R., Khachigian L.M., Lowe H.C. DNAzymes targeting the transcription factor Egr-reduce myocardial infarct size following ischemia-reperfusion in rats. J. Thromb. Haemost. 2006, 4:1479-1483.
32. Iversen P.O., Nicolaysen G., Sioud M. DNA enzyme targeting TNF-alpha mRNA improves hemodynamic performance in rats with postinfarction heart failure. Am. J. Physiol. Heart Circ. Physiol. 2001, 281:H2211-H2217.
33. Luo X., Cai H., Ni J., Bhindi R., Lowe H.C., Chesterman C.N., et al. c-Jun DNAzymes inhibit myocardial inflammation, ROS generation, infarct size, and improve cardiac function after ischemia-reperfusion injury. Arterioscler. Thromb. Vasc. Biol. 2009, 29:1836-1842.
34. Xiang G., Schuster M.D., Seki T., Witkowski P., Eshghi S., Itescu S. Downregulated expression of plasminogen activator inhibitor-augments myocardial neovascularization and reduces cardiomyocyte apoptosis after acute myocardial infarction. J. Am. Coll. Cardiol. 2005, 46:536-541.
35. Zhang L., Gasper W.J., Stass S.A., Ioffe O.B., Davis M.A., Mixson A.J. Angiogenic inhibition mediated by a DNAzyme that targets vascular endothelial growth factor receptor 2. Cancer Res. 2002, 62:5463-5469.
36. Yang L., Xu Z., Liu L., Luo X., Lu J., Sun L., et al. Targeting EBV-LMP1 DNAzyme enhances radiosensitivity of nasopharyngeal carcinoma cells by inhibiting telomerase activity. Cancer Biol. Ther. 2014, 15:61-68.
37. Krug N., et al. Allergen-induced asthmatic responses modified by a GATA3-specific DNAzyme. N. Engl. J. Med. 2015, 372:1987-1995.
38. Homburg U., et al. Safety and tolerability of a novel inhaled GATA3 mRNA targeting DNAzyme in patients with TH2-driven asthma. J. Allergy Clin. Immunol. 2015, 136:797-800.
39. Yehl K., Joshi J.P., Greene B.L., Dyer R.B., Nahta R., Salaita K. Catalytic deoxyribozyme-modified nanoparticles for RNAi-independent gene regulation. ACS Nano 2012, 6:9150-9157.
40. Hill H.D., Mirkin C.A. The bio-barcode assay for the detection of protein and nucleic acid targets using DTT-induced ligand exchange. Nat. Protoc. 2006, 1:324-336.
41. Hurst S.J., Lytton-Jean A.K., Mirkin C.A. Maximizing DNA loading on a range of gold nanoparticle sizes. Anal. Chem. 2006, 78:8313-8318.
42. Wang G.W., Guo Y., Vondriska T.M., Zhang J., Zhang S., Tsai L.L., et al. Acrolein consumption exacerbates myocardial ischemic injury and blocks nitric oxide-induced PKCepsilon signaling and cardioprotection. J. Mol. Cell Cardiol. 2008, 44:1016-1022.
43. Yehl K., Joshi J.P., Greene B.L., Dyer R.B., Nahta R., Salaita K. Catalytic deoxyribozyme-modified nanoparticles for RNAi-independent gene regulation. ACS Nano 2012, 6:9150-9157.
44. Giljohann D.A., Seferos D.S., Patel P.C., Millstone J.E., Rosi N.L., Mirkin C.A. Oligonucleotide loading determines cellular uptake of DNA-modified gold nanoparticles. Nano Lett. 2007, 7:3818-3821.
45. Yehl K., Joshi J.R., Greene B.L., Dyer R.B., Nahta R., Salaita K. Catalytic Deoxyribozyme-Modified Nanoparticles for RNAi-Independent gene regulation. ACS Nano 2012, 6:9150-9157.
46. Champion J.A., Walker A., Mitragotri S. Role of particle size in phagocytosis of polymeric microspheres. Pharm. Res. 2008, 25:1815-1821.
47. Hastings C.L., Roche E.T., Ruiz-Hernandez E., Schenke-Layland K., Walsh C.J., Duffy G.P. Drug and cell delivery for cardiac regeneration. Adv. Drug Deliv. Rev. 2015, 84:85-106.
48. Kumar A., Thota V., Dee L., Olson J., Uretz E., Parrillo J.E. Tumor necrosis factor alpha and interleukin 1beta are responsible for in vitro myocardial cell depression induced by human septic shock serum. J. Exp. Med. 1996, 183:949-958.
49. Ono K., Matsumori A., Shioi T., Furukawa Y., Sasayama S. Cytokine gene expression after myocardial infarction in rat hearts: possible implication in left ventricular remodeling. Circulation 1998, 98:149-156.
50. Moe G.W., Marin-Garcia J., Konig A., Goldenthal M., Lu X., Feng Q. In vivo TNF-alpha inhibition ameliorates cardiac mitochondrial dysfunction, oxidative stress, and apoptosis in experimental heart failure. Am. J. Physiol. Heart Circ. Physiol. 2004, 287:H1813-H1820.
51. Habib F.M., Springall D.R., Davies G.J., Oakley C.M., Yacoub M.H., Polak J.M. Tumour necrosis factor and inducible nitric oxide synthase in dilated cardiomyopathy. Lancet 1996, 347:1151-1155.
52. Watson D.C., Sargianou M., Panos G. Interleukin-12 (IL-12)/IL-10 ratio as a marker of disease severity in Crimean-Congo hemorrhagic fever. Clin. Vaccin. Immunol. CVI 2012, 19:823-824.
53. Yokoyama T., Vaca L., Rossen R.D., Durante W., Hazarika P., Mann D.L. Cellular basis for the negative inotropic effects of tumor necrosis factor-alpha in the adult mammalian heart. J. Clin. Investig. 1993, 92:2303-2312.
54. Gulick T., Chung M.K., Pieper S.J., Lange L.G., Schreiner G.F. Interleukin 1 and tumor necrosis factor inhibit cardiac myocyte beta-adrenergic responsiveness. Proc. Natl. Acad. Sci. U. S. A. 1989, 86:6753-6757.
55. Mazurek S.R., Bovo E., Zima A.V. Regulation of sarcoplasmic reticulum Ca(2+) release by cytosolic glutathione in rabbit ventricular myocytes. Free Radic. Biol. Med. 2014, 68:159-167.
56. Zima A.V., Blatter L.A. Redox regulation of cardiac calcium channels and transporters. Cardiovasc. Res. 2006, 71:310-321.
57. Finkel M.S., Oddis C.V., Jacob T.D., Watkins S.C., Hattler B.G., Simmons R.L. Negative inotropic effects of cytokines on the heart mediated by nitric oxide. Science 1992, 257:387-389.
58. Song W., Lu X., Feng Q. Tumor necrosis factor-alpha induces apoptosis via inducible nitric oxide synthase in neonatal mouse cardiomyocytes. Cardiovasc Res. 2000, 45:595-602.