Direct In Vivo Reprogramming with Sendai Virus Vectors Improves Cardiac Function after Myocardial Infarction

Cell Stem Cell

Volumn 22, Issue 1, 2018, Pages 91-103.e5

  Miyamoto, Kazutaka ^a   Akiyama, Mizuha ^a   Tamura, Fumiya ^a   Isomi, Mari ^a   Yamakawa, Hiroyuki ^a   Sadahiro, Taketaro ^a   Muraoka, Naoto ^a   Kojima, Hidenori ^a   Haginiwa, Sho ^a   Kurotsu, Shota ^a   Tani, Hidenori ^a   Wang, Li ^b   Qian, Li ^b   Inoue, Makoto ^c   Ide, Yoshinori ^d   Kurokawa, Junko ^e   Yamamoto, Tsunehisa ^a   Seki, Tomohisa ^a   Aeba, Ryo ^a   Yamagishi, Hiroyuki ^a   Fukuda, Keiichi ^a   Ieda, Masaki ^a   more..

^a KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^c Section of Cell Engineering   (Japan)

^d Pharmacological Evaluation Institute of Japan   (Japan)

^e UNIVERSITY OF SHIZUOKA   (Japan)

Author keywords

cardiomyocyte; fibroblast; integration; myocardial infarction; regeneration; reprogramming; Sendai virus

Indexed keywords

RETROVIRUS VECTOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GATA 4; TRANSCRIPTION FACTOR MEF2C; TRANSCRIPTION FACTOR TBX5; UNCLASSIFIED DRUG; VIRUS VECTOR;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARDIAC MUSCLE CELL; CELL LINEAGE; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; HEART FUNCTION; HEART INFARCTION; HEART MUSCLE FIBROSIS; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; NUCLEAR REPROGRAMMING; PRIORITY JOURNAL; SENDAI VIRUS; TRANSGENE; ACTION POTENTIAL; ANIMAL; CELL PROLIFERATION; FIBROBLAST; FIBROSIS; GENE VECTOR; GENETICS; METABOLISM; NEWBORN; PATHOLOGY; PATHOPHYSIOLOGY; VIRION;

ACTION POTENTIALS; ANIMALS; ANIMALS, NEWBORN; CELL LINEAGE; CELL PROLIFERATION; CELLULAR REPROGRAMMING; FIBROBLASTS; FIBROSIS; GENETIC VECTORS; HUMANS; MICE; MYOCARDIAL INFARCTION; MYOCYTES, CARDIAC; SENDAI VIRUS; TRANSCRIPTION FACTORS; TRANSGENES; VIRION;

EID: 85038859869     PISSN: 19345909     EISSN: 18759777     Source Type: Journal    
DOI: 10.1016/j.stem.2017.11.010     Document Type: Article

References (36)

1. Acharya, A., Baek, S.T., Banfi, S., Eskiocak, B., Tallquist, M.D., Efficient inducible Cre-mediated recombination in Tcf21 cell lineages in the heart and kidney. Genesis 49 (2011), 870–877.
2. Ban, H., Nishishita, N., Fusaki, N., Tabata, T., Saeki, K., Shikamura, M., Takada, N., Inoue, M., Hasegawa, M., Kawamata, S., Nishikawa, S., Efficient generation of transgene-free human induced pluripotent stem cells (iPSCs) by temperature-sensitive Sendai virus vectors. Proc. Natl. Acad. Sci. USA 108 (2011), 14234–14239.
3. Chen, J.X., Krane, M., Deutsch, M.A., Wang, L., Rav-Acha, M., Gregoire, S., Engels, M.C., Rajarajan, K., Karra, R., Abel, E.D., et al. Inefficient reprogramming of fibroblasts into cardiomyocytes using Gata4, Mef2c, and Tbx5. Circ. Res. 111 (2012), 50–55.
4. Dirkx, E., Gladka, M.M., Philippen, L.E., Armand, A.S., Kinet, V., Leptidis, S., El Azzouzi, H., Salic, K., Bourajjaj, M., da Silva, G.J., et al. Nfat and miR-25 cooperate to reactivate the transcription factor Hand2 in heart failure. Nat. Cell Biol. 15 (2013), 1282–1293.
5. Ferrari, S., Griesenbach, U., Iida, A., Farley, R., Wright, A.M., Zhu, J., Munkonge, F.M., Smith, S.N., You, J., Ban, H., et al. Sendai virus-mediated CFTR gene transfer to the airway epithelium. Gene Ther. 14 (2007), 1371–1379.
6. Fusaki, N., Ban, H., Nishiyama, A., Saeki, K., Hasegawa, M., Efficient induction of transgene-free human pluripotent stem cells using a vector based on Sendai virus, an RNA virus that does not integrate into the host genome. Proc. Jpn. Acad., Ser. B, Phys. Biol. Sci. 85 (2009), 348–362.
7. Ieda, M., Fu, J.D., Delgado-Olguin, P., Vedantham, V., Hayashi, Y., Bruneau, B.G., Srivastava, D., Direct reprogramming of fibroblasts into functional cardiomyocytes by defined factors. Cell 142 (2010), 375–386.
8. Inagawa, K., Miyamoto, K., Yamakawa, H., Muraoka, N., Sadahiro, T., Umei, T., Wada, R., Katsumata, Y., Kaneda, R., Nakade, K., et al. Induction of cardiomyocyte-like cells in infarct hearts by gene transfer of Gata4, Mef2c, and Tbx5. Circ. Res. 111 (2012), 1147–1156.
9. Ivey, M.J., Tallquist, M.D., Defining the cardiac fibroblast. Circ. J. 80 (2016), 2269–2276.
10. Jayawardena, T.M., Egemnazarov, B., Finch, E.A., Zhang, L., Payne, J.A., Pandya, K., Zhang, Z., Rosenberg, P., Mirotsou, M., Dzau, V.J., MicroRNA-mediated in vitro and in vivo direct reprogramming of cardiac fibroblasts to cardiomyocytes. Circ. Res. 110 (2012), 1465–1473.
11. Jayawardena, T.M., Finch, E.A., Zhang, L., Zhang, H., Hodgkinson, C.P., Pratt, R.E., Rosenberg, P.B., Mirotsou, M., Dzau, V.J., MicroRNA induced cardiac reprogramming in vivo: Evidence for mature cardiac myocytes and improved cardiac function. Circ. Res. 116 (2015), 418–424.
12. Kanisicak, O., Khalil, H., Ivey, M.J., Karch, J., Maliken, B.D., Correll, R.N., Brody, M.J.J., J Lin, S.C., Aronow, B.J., Tallquist, M.D., Molkentin, J.D., Genetic lineage tracing defines myofibroblast origin and function in the injured heart. Nat. Commun., 7, 2016, 12260.
13. Li, H.O., Zhu, Y.F., Asakawa, M., Kuma, H., Hirata, T., Ueda, Y., Lee, Y.S., Fukumura, M., Iida, A., Kato, A., et al. A cytoplasmic RNA vector derived from nontransmissible Sendai virus with efficient gene transfer and expression. J. Virol. 74 (2000), 6564–6569.
14. Ma, H., Wang, L., Yin, C., Liu, J., Qian, L., In vivo cardiac reprogramming using an optimal single polycistronic construct. Cardiovasc. Res. 108 (2015), 217–219.
15. Matsumoto, T., Tanaka, M., Yoshiya, K., Yoshiga, R., Matsubara, Y., Horiuchi-Yoshida, K., Yonemitsu, Y., Maehara, Y., Improved quality of life in patients with no-option critical limb ischemia undergoing gene therapy with DVC1-0101. Sci. Rep., 6, 2016, 30035.
16. Mohamed, T.M., Stone, N.R., Berry, E.C., Radzinsky, E., Huang, Y., Pratt, K., Ang, Y.S., Yu, P., Wang, H., Tang, S., et al. Chemical enhancement of in vitro and in vivo direct cardiac reprogramming. Circulation 135 (2017), 978–995.
17. Muraoka, N., Ieda, M., Stoichiometry of transcription factors is critical for cardiac reprogramming. Circ. Res. 116 (2015), 216–218.
18. Muraoka, N., Yamakawa, H., Miyamoto, K., Sadahiro, T., Umei, T., Isomi, M., Nakashima, H., Akiyama, M., Wada, R., Inagawa, K., et al. MiR-133 promotes cardiac reprogramming by directly repressing Snai1 and silencing fibroblast signatures. EMBO J. 33 (2014), 1565–1581.
19. Nakanishi, M., Otsu, M., Development of Sendai virus vectors and their potential applications in gene therapy and regenerative medicine. Curr. Gene Ther. 12 (2012), 410–416.
20. Nam, Y.J., Song, K., Luo, X., Daniel, E., Lambeth, K., West, K., Hill, J.A., DiMaio, J.M., Baker, L.A., Bassel-Duby, R., Olson, E.N., Reprogramming of human fibroblasts toward a cardiac fate. Proc. Natl. Acad. Sci. USA 110 (2013), 5588–5593.
21. Nam, Y.J., Lubczyk, C., Bhakta, M., Zang, T., Fernandez-Perez, A., McAnally, J., Bassel-Duby, R., Olson, E.N., Munshi, N.V., Induction of diverse cardiac cell types by reprogramming fibroblasts with cardiac transcription factors. Development 141 (2014), 4267–4278.
22. Pinto, A.R., Ilinykh, A., Ivey, M.J., Kuwabara, J.T., D'Antoni, M.L., Debuque, R., Chandran, A., Wang, L., Arora, K., Rosenthal, N.A., Tallquist, M.D., Revisiting cardiac cellular composition. Circ. Res. 118 (2016), 400–409.
23. Qian, L., Huang, Y., Spencer, C.I., Foley, A., Vedantham, V., Liu, L., Conway, S.J., Fu, J.D., Srivastava, D., In vivo reprogramming of murine cardiac fibroblasts into induced cardiomyocytes. Nature 485 (2012), 593–598.
24. Qian, L., Berry, E.C., Fu, J.D., Ieda, M., Srivastava, D., Reprogramming of mouse fibroblasts into cardiomyocyte-like cells in vitro. Nat. Protoc. 8 (2013), 1204–1215.
25. Sadahiro, T., Yamanaka, S., Ieda, M., Direct cardiac reprogramming: Progress and challenges in basic biology and clinical applications. Circ. Res. 116 (2015), 1378–1391.
26. Seki, T., Yuasa, S., Oda, M., Egashira, T., Yae, K., Kusumoto, D., Nakata, H., Tohyama, S., Hashimoto, H., Kodaira, M., et al. Generation of induced pluripotent stem cells from human terminally differentiated circulating T cells. Cell Stem Cell 7 (2010), 11–14.
27. Song, K., Nam, Y.J., Luo, X., Qi, X., Tan, W., Huang, G.N., Acharya, A., Smith, C.L., Tallquist, M.D., Neilson, E.G., et al. Heart repair by reprogramming non-myocytes with cardiac transcription factors. Nature 485 (2012), 599–604.
28. Srivastava, D., DeWitt, N., In vivo cellular reprogramming: The next generation. Cell 166 (2016), 1386–1396.
29. Srivastava, D., Ieda, M., Critical factors for cardiac reprogramming. Circ. Res. 111 (2012), 5–8.
30. Takeda, A., Igarashi, H., Kawada, M., Tsukamoto, T., Yamamoto, H., Inoue, M., Iida, A., Shu, T., Hasegawa, M., Matano, T., Evaluation of the immunogenicity of replication-competent V-knocked-out and replication-defective F-deleted Sendai virus vector-based vaccines in macaques. Vaccine 26 (2008), 6839–6843.
31. Wada, R., Muraoka, N., Inagawa, K., Yamakawa, H., Miyamoto, K., Sadahiro, T., Umei, T., Kaneda, R., Suzuki, T., Kamiya, K., et al. Induction of human cardiomyocyte-like cells from fibroblasts by defined factors. Proc. Natl. Acad. Sci. USA 110 (2013), 12667–12672.
32. Wang, L., Liu, Z., Yin, C., Asfour, H., Chen, O., Li, Y., Bursac, N., Liu, J., Qian, L., Stoichiometry of Gata4, Mef2c, and Tbx5 influences the efficiency and quality of induced cardiac myocyte reprogramming. Circ. Res. 116 (2015), 237–244.
33. Yamakawa, H., Muraoka, N., Miyamoto, K., Sadahiro, T., Isomi, M., Haginiwa, S., Kojima, H., Umei, T., Akiyama, M., Kuishi, Y., et al. Fibroblast growth factors and vascular endothelial growth factor promote cardiac reprogramming under defined conditions. Stem Cell Reports 5 (2015), 1128–1142.
34. Yonemitsu, Y., Kitson, C., Ferrari, S., Farley, R., Griesenbach, U., Judd, D., Steel, R., Scheid, P., Zhu, J., Jeffery, P.K., et al. Efficient gene transfer to airway epithelium using recombinant Sendai virus. Nat. Biotechnol. 18 (2000), 970–973.
35. Zhao, Y., Londono, P., Cao, Y., Sharpe, E.J., Proenza, C., O'Rourke, R., Jones, K.L., Jeong, M.Y., Walker, L.A., Buttrick, P.M., et al. High-efficiency reprogramming of fibroblasts into cardiomyocytes requires suppression of pro-fibrotic signalling. Nat. Commun., 6, 2015, 8243.
36. Zhou, Y., Wang, L., Vaseghi, H.R., Liu, Z., Lu, R., Alimohamadi, S., Yin, C., Fu, J.D., Wang, G.G., Liu, J., Qian, L., Bmi1 is a key epigenetic barrier to direct cardiac reprogramming. Cell Stem Cell 18 (2016), 382–395.