Synthetic chemically modified mRNA (ModRNA): Toward a new technology platform for cardiovascular biology and medicine

Cold Spring Harbor Perspectives in Medicine

Volumn 5, Issue 1, 2015, Pages

  Chien, Kenneth R ^a,b   Zangi, Lior ^c   Lui, Kathy O ^a  

^a Harvard University   (United States)

^b KAROLINSKA INSTITUTE   (Sweden)

^c BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; INTERFERON; RECOMBINANT RNA; SYNTHETIC CHEMICALLY MODIFIED MESSENGER RNA; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 8; UNCLASSIFIED DRUG; MESSENGER RNA; PROTEIN; VASCULOTROPIN A;

ADENO ASSOCIATED VIRUS; ARTICLE; CELL FATE; CLINICAL PROTOCOL; EMBRYONIC STEM CELL; HEART DISEASE; HEART MUSCLE CELL; HUMAN; IN VITRO GENE TRANSFER; IN VIVO GENE TRANSFER; INNATE IMMUNITY; MYOTUBE; NONHUMAN; PARACRINE SIGNALING; PROTEIN EXPRESSION; VIRAL GENE THERAPY; ANIMAL; CYTOLOGY; GENE THERAPY; GENE TRANSFER; HEART; HEART DISEASES; HEART MUSCLE; METABOLISM; MOUSE; PHYSIOLOGY; PIG; PROCEDURES; RAT; REGENERATION; SKELETAL MUSCLE; STEM CELL; SYNTHESIS;

ADENO-ASSOCIATED VIRUS; MAMMALIA; PRIMATES; RATTUS; SUS;

ANIMALS; GENE TRANSFER TECHNIQUES; GENETIC THERAPY; HEART; HEART DISEASES; HUMANS; MICE; MUSCLE, SKELETAL; MYOCARDIUM; MYOCYTES, CARDIAC; PARACRINE COMMUNICATION; PROTEINS; RATS; REGENERATION; RNA, MESSENGER; STEM CELLS; SWINE; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84923828111     PISSN: None     EISSN: 21571422     Source Type: Journal    
DOI: 10.1101/cshperspect.a014035     Document Type: Article

References (48)

1. Bolli R, Chugh AR, D’Amario D, Loughran JH, Stoddard MF, Ikram S, Beache GM, Wagner SG, Leri A, Hosoda T, et al. 2011. Cardiac stem cells in patients with ischaemic cardiomyopathy (SCIPIO): Initial results of a randomised phase 1 trial. Lancet 378: 1847-1857.
2. Braun S. 2004. Naked plasmid DNA for the treatment of muscular dystrophy. Curr Opin Mol Ther 6: 499-505.
3. Carmeliet P, Ng YS, Nuyens D, Theilmeier G, Brusselmans K, Cornelissen I, Ehler E, Kakkar VV, Stalmans I, Mattot V, et al. 1999. Impaired myocardial angiogenesis and ischemic cardiomyopathy in mice lacking the vascular endothelial growth factor isoforms VEGF164 and VEGF188. Nat Med 5: 495-502.
4. Chen J, Huang ZP, Seok HY, Ding J, Kataoka M, Zhang Z, Hu X, Wang G, Lin Z, Wang S, et al. 2013a. Mir-17-92 cluster is required for and sufficient to induce cardiomyocyte proliferation in postnatal and adult hearts. Circ Res 112: 1557-1566.
5. Chen SJ, Johnston J, Sandhu A, Bish LT, Hovhannisyan R, Jno-Charles O, Sweeney HL, Wilson JM. 2013b. Enhancing the utility of adeno-associated virus gene transfer through inducible tissue-specific expression. Hum Gene Ther Methods 24: 270-278.
6. Deng Y, Wang CC, Choy KW, Du Q, Chen J, Wang Q, Li L, Chung TK, Tang T. 2014. Therapeutic potentials of gene silencing by RNA interference: Principles, challenges, and new strategies. Gene 538: 217-227.
7. Eulalio A, Mano M, Dal Ferro M, Zentilin L, Sinagra G, Zacchigna S, Giacca M. 2012. Functional screening identifies miRNAs inducing cardiac regeneration. Nature 492: 376-381.
8. Gao J, Liu J, Gao Y, Wang C, Zhao Y, Chen B, Xiao Z, Miao Q, Dai J. 2011. A myocardial patch made of collagen membranes loaded with collagen-binding human vascular endothelial growth factor accelerates healing of the injured rabbit heart. Tissue Eng Part A 17: 2739-2747.
9. Hagiwara S, Iwasaka H, Shingu C, Matumoto S, Hasegawa A, Nogushi T. 2011. Heat shock protein 47 (HSP47) antisense oligonucleotides reduce cardiac remodeling and improve cardiac function in a rat model of myocardial infarction. Thorac Cardiovasc Surg 59: 386-392.
10. Hedman M, Hartikainen J, Syvänne M, Stjernvall J, Hedman A, Kivelä A, Vanninen E, Mussalo H, Kauppila E, Simula S, et al. 2003. Safety and feasibility of catheter-based local intracoronary vascular endothelial growth factor gene transfer in the prevention of postangioplasty and in-stent restenosis and in the treatment of chronic myocardial ischemia: Phase II results of the Kuopio Angiogenesis Trial (KAT). Circulation 107: 2677-2683.
11. Hendel RC, Henry TD, Rocha-Singh K, Isner JM, Kereiakes DJ, Giordano FJ, Simons M, Bonow RO. 2000. Effect of intracoronary recombinant human vascular endothelial growth factor on myocardial perfusion: Evidence for a dose-dependent effect. Circulation 101: 118-121.
12. Henry TD, Annex BH, McKendall GR, Azrin MA, Lopez JJ, Giordano FJ, Shah PK, Willerson JT, Benza RL, Berman DS, et al. 2003. The VIVA trial: Vascular endothelial growth factor in ischemia for vascular angiogenesis. Circulation 107: 1359-1365.
13. Hinkel R, Trenkwalder T, Kupatt C. 2011. Gene therapy for ischemic heart disease. Expert Opin Biol Ther 11: 723-737.
14. Hinkel R, Penzkofer D, Zuhlke S, Fischer A, Husada W, Xu QF, Baloch E, van Rooij E, Zeiher AM, Kupatt C, et al. 2013. Inhibition of microRNA-92a protects against ischemia/reperfusion injury in a large-animal model. Circulation 128: 1066-1075.
15. Kariko K, Ni H, Capodici J, Lamphier M, Weissman D. 2004. MRNA is an endogenous ligand for Toll-like receptor 3. J Biol Chem 279: 12542-12550.
16. Kariko K, Buckstein M, Ni H, Weissman D. 2005. Suppression of RNA recognition by Toll-like receptors: The impact of nucleoside modification and the evolutionary origin of RNA. Immunity 23, 165-175.
17. Kariko K, Muramatsu H, Ludwig J, Weissman D. 2011. Generating the optimal mRNA for therapy: HPLC purification eliminates immune activation and improves translation of nucleoside-modified, protein-encoding mRNA. Nucleic Acids Res 39: e142.
18. Kariko K, Muramatsu H, Keller JM, Weissman D. 2012. Increased erythropoiesis in mice injected with submicrogram quantities of pseudouridine-containing mRNA encoding erythropoietin. Mol Ther 20: 948-953.
19. Khatri N, Rathi M, Baradia D, Trehan S, Misra A. 2012. In vivo delivery aspects of miRNA, shRNA and siRNA. Crit Rev Ther Drug Carrier Syst 29: 487-527.
20. Kobara M, Noda K, Kitamura M, Okamoto A, Shiraishi T, Toba H, Matsubara H, Nakata T. 2010. Antibody against interleukin-6 receptor attenuates left ventricular remodelling after myocardial infarction in mice. Cardiovasc Res 87: 424-430.
21. Kormann MS, Hasenpusch G, Aneja MK, Nica G, Flemmer AW, Herber-Jonat S, Huppmann M, Mays LE, Illenyi M, Schams A, et al. 2011. Expression of therapeutic proteins after delivery of chemically modified mRNA in mice. Nat Biotechnol 29: 154-157.
22. Lin YD, Luo CY, Hu YN, Yeh ML, Hsueh YC, Chang MY, Tsai DC, Wang JN, Tang MJ, Wei EI, et al. 2012. Instructive nanofiber scaffolds with VEGF create a microenvironment for arteriogenesis and cardiac repair. Sci Transl Med 4: 146ra109.
23. Losordo DW, Vale PR, Symes JF, Dunnington CH, Esakof DD, Maysky M, Ashare AB, Lathi K, Isner JM. 1998. Gene therapy for myocardial angiogenesis: Initial clinical results with direct myocardial injection of phVEGF165 as sole therapy for myocardial ischemia. Circulation 98: 2800-2804.
24. Lui KO, Zangi L, Silva EA, Bu L, Sahara M, Li RA, Mooney DJ, Chien KR. 2013a. Driving vascular endothelial cell fate of human multipotent Isl1þ heart progenitors with VEGF modified mRNA. Cell Res 23: 1172-1186.
25. Lui KO, Stachel MW, Li RA, Bu L. 2013b. Human pluripotent stem cell-derived cardiovascular progenitors for heart regeneration. Drug Discov Today Dis Models 9: e189-e197.
26. Majmudar MD, Keliher EJ, Heidt T, Leuschner F, Truelove J, Sena BF, Gorbatov R, Iwamoto Y, Dutta P, Wojtkiewicz G, et al. 2013. Monocyte-directed RNAi targeting CCR2 improves infarct healing in atherosclerosis-prone mice. Circulation 127: 2038-2046.
27. Makkar RR, Smith RR, Cheng K, Malliaras K, Thomson LE, Berman D, Czer LS, Marbán L, Mendizabal A, Johnston PV, et al. 2012. Intracoronary cardiosphere-derived cells for heart regeneration after myocardial infarction (CADUCEUS): A prospective, randomised phase 1 trial. Lancet 379: 895-904.
28. Malliaras K, Makkar RR, Smith RR, Cheng K, Wu E, Bonow RO, Marbán L, Mendizabal A, Cingolani E, Johnston PV, et al. 2014. Intracoronary cardiosphere-derived cells after myocardial infarction: Evidence of therapeutic regeneration in the final 1-year results of the CADUCEUS trial (CArdiosphere-Derived aUtologous stem CElls to reverse ventricUlar dySfunction). J Am Coll Cardiol 63: 110-122.
29. Mandal PK, Rossi DJ. 2013. Reprogramming human fibro- blasts to pluripotency using modified mRNA. Nat Protoc 8: 568-582.
30. Martin-Puig S, Wang Z, Chien KR. 2008. Lives of a heart cell: Tracing the origins of cardiac progenitors. Cell Stem Cell 2: 320-331.
31. Ni H, Capodici J, Cannon G, Communi D, Boeynaems JM, Karikó K, Weissman D. 2002. Extracellular mRNA induces dendritic cell activation by stimulating tumor necrosis factor-a secretion and signaling through a nucleotide receptor. J Biol Chem 277: 12689-12696.
32. Papadakis ED, Nicklin SA, Baker AH, White SJ. 2004. Promoters and control elements: Designing expression cassettes for gene therapy. Curr Gene Ther 4: 89-113.
33. Purdham DM, Rajapurohitam V, Zeidan A, Huang C, Gross GJ, Karmazyn M. 2008. A neutralizing leptin receptor antibody mitigates hypertrophy and hemodynamic dysfunction in the postinfarcted rat heart. Am J Physiol Heart Circ Physiol 295: H441-H446.
34. Sanganalmath SK, Bolli R. 2013. Cell therapy for heart failure: A comprehensive overview of experimental and clinical studies, current challenges, and future directions. Circ Res 113: 810-834.
35. Sato K, Wu T, Laham RJ, Johnson RB, Douglas P, Li J, Sellke FW, Bunting S, Simons M, Post MJ. 2001. Efficacy of intracoronary or intravenous VEGF165 in a pig model of chronic myocardial ischemia. J Am Coll Cardiol 37: 616-623.
36. Stewart DJ, Hilton JD, Arnold JM, Gregoire J, Rivard A, Archer SL, Charbonneau F, Cohen E, Curtis M, Buller CE, et al. 2006. Angiogenic gene therapy in patients with nonrevascularizable ischemic heart disease: A phase 2 randomized, controlled trial of AdVEGF121 (AdVEGF121) versus maximum medical treatment. Gene Ther 13: 1503-1511.
37. Stewart DJ, Kutryk MJ, Fitchett D, Freeman M, Camack N, Su Y, Della Siega A, Bilodeau L, Burton JR, Proulx G, et al. 2009. VEGF gene therapy fails to improve perfusion of ischemic myocardium in patients with advanced coronary disease: Results of the NORTHERN trial. Mol Ther 17: 1109-1115.
38. Taniyama Y, Azuma J, Kunugiza Y, Iekushi K, Rakugi H, Morishita R. 2012. Therapeutic option of plasmid-DNA based gene transfer. Curr Top Med Chem 12: 1630-1637.
39. Vader P, van der Aa LJ, Storm G, Schiffelers RM, Engbersen JF. 2012. Polymeric carrier systems for siRNA delivery. Curr Top Med Chem 12: 108-119.
40. van Rooij E, Marshall WS, Olson EN. 2008. Toward microRNA-based therapeutics for heart disease: The sense in antisense. Circ Res 103: 919-928.
41. Warren L, Manos PD, Ahfeldt T, Loh YH, Li H, Lau F, Ebina W, Mandal PK, Smith ZD, Meissner A, et al. 2010. Highly efficient reprogramming to pluripotency and directed differentiation of human cells with synthetic modified mRNA. Cell Stem Cell 7: 618-630.
42. Weissman D, Ni H, Scales D, Dude A, Capodici J, McGibney K, Abdool A, Isaacs SN, Cannon G, Karikó K. 2000. HIV gag mRNA transfection of dendritic cells (DC) delivers encoded antigen to MHC class I and II molecules, causes DC maturation, and induces a potent human in vitro primary immune response. J Immunol 165: 4710-4717.
43. Wu J, Zeng F, Huang XP, Chung JC, Konecny F, Weisel RD, Li RK. 2011. Infarct stabilization and cardiac repair with a VEGF-conjugated, injectable hydrogel. Biomaterials 32: 579-586.
44. Wu H, Zhu Q, Cai M, Tong X, Liu D, Huang J, Yang G, Jiang Y. 2014. Effect of inhibiting malonyl-CoA decarboxylase on cardiac remodeling after myocardial infarction in rats. Cardiology 127: 236-244.
45. Yang R, Ogasawara AK, Zioncheck TF, Ren Z, He GW, DeGuzman GG, Pelletier N, Shen BQ, Bunting S, Jin H. 2002. Exaggerated hypotensive effect of vascular endothelial growth factor in spontaneously hypertensive rats. Hypertension 39: 815-820.
46. Zacchigna S, Zentilin L, Giacca M. 2014. Adeno-associated virus vectors as therapeutic and investigational tools in the cardiovascular system. Circ Res 114: 1827-1846.
47. Zangi L, Lui KO, von Gise A, Ma Q, Ebina W, Ptaszek LM, Später D, Xu H, Tabebordbar M, Gorbatov R, et al. 2013. Modified mRNA directs the fate of heart progenitor cells and induces vascular regeneration after myocardial infarction. Nat Biotechnol 31: 898-907.
48. Zhou B, Ma Q, Rajagopal S, Wu SM, Domian I, RiveraFeliciano J, Jiang D, von Gise A, Ikeda S, Chien KR, et al. 2008. Epicardial progenitors contribute to the cardiomyocyte lineage in the developing heart. Nature 454: 109-113.