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Published in: International Journal of Hematology 4/2021

01-04-2021 | Hemophilia | Original Article

Utilization of a novel Sendai virus vector in ex vivo gene therapy for hemophilia A

Authors: Yuni Yamaki, Takashi Fukushima, Naomi Yoshida, Ken Nishimura, Aya Fukuda, Koji Hisatake, Masayuki Aso, Tomoki Sakasai, Junko Kijima-Tanaka, Yoshihiro Miwa, Mahito Nakanishi, Ryo Sumazaki, Hidetoshi Takada

Published in: International Journal of Hematology | Issue 4/2021

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Abstract

Sendai virus (SeV) vectors are being recognized as a superior tool for gene transfer. Here, we report the transfection efficacy of a novel, high-performance, replication-defective, and persistent Sendai virus (SeVdp) vector in cultured cells and in mice using a near-infrared fluorescent protein (iRFP)-mediated in vivo imaging system. The novel SeVdp vector established persistent infection, and strong expression of inserted genes was sustained indefinitely in vitro. Analysis of iRFP-expressing cells transplanted subcutaneously into NOG, nude, and ICR mice suggests that innate immunity was involved in the exclusion of the transplanted cells. We also evaluated the feasibility of this novel SeVdp vector for hemophilia A gene therapy. This system enabled insertion of full-length FVIII genes, and transduced cells secreted FVIII into the culture medium. Transient FVIII activity was detected in the plasma of mice after intraperitoneal transplantation of these FVIII-secreting cells. Further improvement in methods to evade immunity, such as simultaneous expression of immunomodulatory genes, would make this novel vector a very useful tool in regenerative medicine.
Literature
1.
go back to reference Nakanishi M, Otsu M. Development of Sendai virus vectors and their potential applications in gene therapy and regenerative medicine. Curr Gene Ther. 2012;12:410–6.CrossRef Nakanishi M, Otsu M. Development of Sendai virus vectors and their potential applications in gene therapy and regenerative medicine. Curr Gene Ther. 2012;12:410–6.CrossRef
2.
go back to reference Hurwitz JL. Development of recombinant Sendai virus vaccines for prevention of human parainfluenza and respiratory syncytial virus infections. Pediatr Infect Dis J. 2008;27:S126–8.CrossRef Hurwitz JL. Development of recombinant Sendai virus vaccines for prevention of human parainfluenza and respiratory syncytial virus infections. Pediatr Infect Dis J. 2008;27:S126–8.CrossRef
3.
go back to reference Masaki I, Yonemitsu Y, Yamashita A, Sata S, Tanii M, Komori K, et al. Angiogenic gene therapy for experimental critical limb ischemia: acceleration of limb loss by overexpression of vascular endothelial growth factor 165 but not of fibroblast growth factor-2. Circ Res. 2002;90:966–73.CrossRef Masaki I, Yonemitsu Y, Yamashita A, Sata S, Tanii M, Komori K, et al. Angiogenic gene therapy for experimental critical limb ischemia: acceleration of limb loss by overexpression of vascular endothelial growth factor 165 but not of fibroblast growth factor-2. Circ Res. 2002;90:966–73.CrossRef
4.
go back to reference Hasegawa Y, Kinoh H, Iwadate Y, Onimaru M, Ueda Y, Harada Y, et al. Urokinase-targeted fusion by oncolytic Sendai virus eradicates orthotopic glioblastomas by pronounced synergy with interferon-beta gene. Mol Ther. 2010;18:1778–86.CrossRef Hasegawa Y, Kinoh H, Iwadate Y, Onimaru M, Ueda Y, Harada Y, et al. Urokinase-targeted fusion by oncolytic Sendai virus eradicates orthotopic glioblastomas by pronounced synergy with interferon-beta gene. Mol Ther. 2010;18:1778–86.CrossRef
5.
go back to reference Nishimura K, Sano M, Ohtaka M, Furuta B, Umemura Y, Nakajima Y, et al. Development of defective and persistent Sendai virus vector: a unique gene delivery/expression system ideal for cell reprogramming. J Biol Chem. 2011;286:4760–71.CrossRef Nishimura K, Sano M, Ohtaka M, Furuta B, Umemura Y, Nakajima Y, et al. Development of defective and persistent Sendai virus vector: a unique gene delivery/expression system ideal for cell reprogramming. J Biol Chem. 2011;286:4760–71.CrossRef
6.
go back to reference Yoshida T, Nagai Y, Maeno K, Iinuma M, Hamaguchi M, Matsumoto T, et al. Studies on the role of M protein in virus assembly using a ts mutant of HVJ (Sendai virus). Virology. 1979;92:139–54.CrossRef Yoshida T, Nagai Y, Maeno K, Iinuma M, Hamaguchi M, Matsumoto T, et al. Studies on the role of M protein in virus assembly using a ts mutant of HVJ (Sendai virus). Virology. 1979;92:139–54.CrossRef
7.
go back to reference Eguchi A, Kondoh T, Kosaka H, Suzuki T, Momota H, Masago A, et al. Identification and characterization of cell lines with a defect in a post-adsorption stage of Sendai virus-mediated membrane fusion. J Biol Chem. 2000;275:17549–55.CrossRef Eguchi A, Kondoh T, Kosaka H, Suzuki T, Momota H, Masago A, et al. Identification and characterization of cell lines with a defect in a post-adsorption stage of Sendai virus-mediated membrane fusion. J Biol Chem. 2000;275:17549–55.CrossRef
8.
go back to reference Manco-Johnson MJ, Abshire TC, Shapiro AD, Riske B, Hacker MR, Kilcoyne R, et al. Prophylaxis versus episodic treatment to prevent joint disease in boys with severe hemophilia. N Engl J Med. 2007;357:535–44.CrossRef Manco-Johnson MJ, Abshire TC, Shapiro AD, Riske B, Hacker MR, Kilcoyne R, et al. Prophylaxis versus episodic treatment to prevent joint disease in boys with severe hemophilia. N Engl J Med. 2007;357:535–44.CrossRef
9.
go back to reference Oldenburg J, Mahlangu JN, Kim B, Schmitt C, Callaghan MU, Young G, et al. Emicizumab prophylaxis in hemophilia A with inhibitors. N Engl J Med. 2017;377:809–18.CrossRef Oldenburg J, Mahlangu JN, Kim B, Schmitt C, Callaghan MU, Young G, et al. Emicizumab prophylaxis in hemophilia A with inhibitors. N Engl J Med. 2017;377:809–18.CrossRef
10.
go back to reference Matsui H, Shibata M, Brown B, Labelle A, Hegadorn C, Andrews C, et al. Ex vivo gene therapy for hemophilia A that enhances safe delivery and sustained in vivo factor VIII expression from lentivirally engineered endothelial progenitors. Stem Cells. 2007;25:2660–9.CrossRef Matsui H, Shibata M, Brown B, Labelle A, Hegadorn C, Andrews C, et al. Ex vivo gene therapy for hemophilia A that enhances safe delivery and sustained in vivo factor VIII expression from lentivirally engineered endothelial progenitors. Stem Cells. 2007;25:2660–9.CrossRef
11.
go back to reference Ohmori T, Mizukami H, Ozawa K, Sakata Y, Nishimura S. New approaches to gene and cell therapy for hemophilia. J Thromb Haemost. 2015;13(Suppl 1):S133–42.CrossRef Ohmori T, Mizukami H, Ozawa K, Sakata Y, Nishimura S. New approaches to gene and cell therapy for hemophilia. J Thromb Haemost. 2015;13(Suppl 1):S133–42.CrossRef
12.
go back to reference Rangarajan S, Walsh L, Lester W, Perry D, Madan B, Laffan M, et al. AAV5-factor VIII gene transfer in severe hemophilia A. N Engl J Med. 2017;377:2519–30.CrossRef Rangarajan S, Walsh L, Lester W, Perry D, Madan B, Laffan M, et al. AAV5-factor VIII gene transfer in severe hemophilia A. N Engl J Med. 2017;377:2519–30.CrossRef
13.
go back to reference Louis Jeune V, Joergensen JA, Hajjar RJ, Weber T. Pre-existing anti-adeno-associated virus antibodies as a challenge in AAV gene therapy. Hum Gene Ther Methods. 2013;24:59–67.CrossRef Louis Jeune V, Joergensen JA, Hajjar RJ, Weber T. Pre-existing anti-adeno-associated virus antibodies as a challenge in AAV gene therapy. Hum Gene Ther Methods. 2013;24:59–67.CrossRef
14.
go back to reference Wu Z, Yang H, Colosi P. Effect of genome size on AAV vector packaging. Mol Ther. 2010;18:80–6.CrossRef Wu Z, Yang H, Colosi P. Effect of genome size on AAV vector packaging. Mol Ther. 2010;18:80–6.CrossRef
15.
go back to reference Brown HC, Wright JF, Zhou S, Lytle AM, Shields JE, Spencer HT, et al. Bioengineered coagulation factor VIII enables long-term correction of murine hemophilia A following liver-directed adeno-associated viral vector delivery. Mol Ther Methods Clin Dev. 2014;1:14036.CrossRef Brown HC, Wright JF, Zhou S, Lytle AM, Shields JE, Spencer HT, et al. Bioengineered coagulation factor VIII enables long-term correction of murine hemophilia A following liver-directed adeno-associated viral vector delivery. Mol Ther Methods Clin Dev. 2014;1:14036.CrossRef
16.
go back to reference Hirsch ML, Wolf SJ, Samulski RJ. Delivering transgenic DNA exceeding the carrying capacity of AAV vectors. Methods Mol Biol. 2016;1382:21–39.CrossRef Hirsch ML, Wolf SJ, Samulski RJ. Delivering transgenic DNA exceeding the carrying capacity of AAV vectors. Methods Mol Biol. 2016;1382:21–39.CrossRef
17.
go back to reference Kaufman RJ, Pipe SW, Tagliavacca L, Swaroop M, Moussalli M. Biosynthesis, assembly and secretion of coagulation factor VIII. Blood Coagul Fibrinolysis. 1997;8(Suppl 2):S3-14.PubMed Kaufman RJ, Pipe SW, Tagliavacca L, Swaroop M, Moussalli M. Biosynthesis, assembly and secretion of coagulation factor VIII. Blood Coagul Fibrinolysis. 1997;8(Suppl 2):S3-14.PubMed
18.
go back to reference Fomin ME, Togarrati PP, Muench MO. Progress and challenges in the development of a cell-based therapy for hemophilia A. J Thromb Haemost. 2014;12:1954–65.CrossRef Fomin ME, Togarrati PP, Muench MO. Progress and challenges in the development of a cell-based therapy for hemophilia A. J Thromb Haemost. 2014;12:1954–65.CrossRef
19.
go back to reference Matsui H, Fujimoto N, Sasakawa N, Ohinata Y, Shima M, Yamanaka S, et al. Delivery of full-length factor VIII using a piggyBac transposon vector to correct a mouse model of hemophilia A. PLoS ONE. 2014;9:e104957.CrossRef Matsui H, Fujimoto N, Sasakawa N, Ohinata Y, Shima M, Yamanaka S, et al. Delivery of full-length factor VIII using a piggyBac transposon vector to correct a mouse model of hemophilia A. PLoS ONE. 2014;9:e104957.CrossRef
20.
go back to reference Shi Q. Platelet-targeted gene therapy for hemophilia. Mol Ther Methods Clin Dev. 2018;9:100–8.CrossRef Shi Q. Platelet-targeted gene therapy for hemophilia. Mol Ther Methods Clin Dev. 2018;9:100–8.CrossRef
21.
go back to reference Ito M, Bujo H, Takahashi K, Arai T, Tanaka I, Saito Y. Implantation of primary cultured adipocytes that secrete insulin modifies blood glucose levels in diabetic mice. Diabetologia. 2005;48:1614–20.CrossRef Ito M, Bujo H, Takahashi K, Arai T, Tanaka I, Saito Y. Implantation of primary cultured adipocytes that secrete insulin modifies blood glucose levels in diabetic mice. Diabetologia. 2005;48:1614–20.CrossRef
22.
go back to reference Aoyagi Y, Kuroda M, Asada S, Bujo H, Tanaka S, Konno S, et al. Fibrin glue increases the cell survival and the transduced gene product secretion of the ceiling culture-derived adipocytes transplanted in mice. Exp Mol Med. 2011;43:161–7.CrossRef Aoyagi Y, Kuroda M, Asada S, Bujo H, Tanaka S, Konno S, et al. Fibrin glue increases the cell survival and the transduced gene product secretion of the ceiling culture-derived adipocytes transplanted in mice. Exp Mol Med. 2011;43:161–7.CrossRef
23.
go back to reference Spalding KL, Arner E, Westermark PO, Bernard S, Buchholz BA, Bergmann O, et al. Dynamics of fat cell turnover in humans. Nature. 2008;453:783–7.CrossRef Spalding KL, Arner E, Westermark PO, Bernard S, Buchholz BA, Bergmann O, et al. Dynamics of fat cell turnover in humans. Nature. 2008;453:783–7.CrossRef
24.
go back to reference Shimizu T, Ishikawa T, Sugihara E, Kuninaka S, Miyamoto T, Mabuchi Y, et al. c-MYC overexpression with loss of Ink4a/Arf transforms bone marrow stromal cells into osteosarcoma accompanied by loss of adipogenesis. Oncogene. 2010;29:5687–99.CrossRef Shimizu T, Ishikawa T, Sugihara E, Kuninaka S, Miyamoto T, Mabuchi Y, et al. c-MYC overexpression with loss of Ink4a/Arf transforms bone marrow stromal cells into osteosarcoma accompanied by loss of adipogenesis. Oncogene. 2010;29:5687–99.CrossRef
25.
go back to reference Miao HZ, Sirachainan N, Palmer L, Kucab P, Cunningham MA, Kaufman RJ, et al. Bioengineering of coagulation factor VIII for improved secretion. Blood. 2004;103:3412–9.CrossRef Miao HZ, Sirachainan N, Palmer L, Kucab P, Cunningham MA, Kaufman RJ, et al. Bioengineering of coagulation factor VIII for improved secretion. Blood. 2004;103:3412–9.CrossRef
26.
go back to reference Filonov GS, Piatkevich KD, Ting LM, Zhang J, Kim K, Verkhusha VV. Bright and stable near-infrared fluorescent protein for in vivo imaging. Nat Biotechnol. 2011;29:757–61.CrossRef Filonov GS, Piatkevich KD, Ting LM, Zhang J, Kim K, Verkhusha VV. Bright and stable near-infrared fluorescent protein for in vivo imaging. Nat Biotechnol. 2011;29:757–61.CrossRef
27.
go back to reference Tran MT, Tanaka J, Hamada M, Sugiyama Y, Sakaguchi S, Nakamura M, et al. In vivo image analysis using iRFP transgenic mice. Exp Anim. 2014;63:311–9.CrossRef Tran MT, Tanaka J, Hamada M, Sugiyama Y, Sakaguchi S, Nakamura M, et al. In vivo image analysis using iRFP transgenic mice. Exp Anim. 2014;63:311–9.CrossRef
28.
go back to reference Jobsis FF. Noninvasive, infrared monitoring of cerebral and myocardial oxygen sufficiency and circulatory parameters. Science. 1977;198:1264–7.CrossRef Jobsis FF. Noninvasive, infrared monitoring of cerebral and myocardial oxygen sufficiency and circulatory parameters. Science. 1977;198:1264–7.CrossRef
29.
go back to reference Lai CW, Chen HL, Yen CC, Wang JL, Yang SH, Chen CM. Using dual fluorescence reporting genes to establish an in vivo imaging model of orthotopic lung adenocarcinoma in mice. Mol Imaging Biol. 2016;18:849–59.CrossRef Lai CW, Chen HL, Yen CC, Wang JL, Yang SH, Chen CM. Using dual fluorescence reporting genes to establish an in vivo imaging model of orthotopic lung adenocarcinoma in mice. Mol Imaging Biol. 2016;18:849–59.CrossRef
30.
go back to reference Neumeyer J, Lin RZ, Wang K, Hong X, Hua T, Croteau SE, et al. Bioengineering hemophilia A-specific microvascular grafts for delivery of full-length factor VIII into the bloodstream. Blood Adv. 2019;3:4166–76.CrossRef Neumeyer J, Lin RZ, Wang K, Hong X, Hua T, Croteau SE, et al. Bioengineering hemophilia A-specific microvascular grafts for delivery of full-length factor VIII into the bloodstream. Blood Adv. 2019;3:4166–76.CrossRef
Metadata
Title
Utilization of a novel Sendai virus vector in ex vivo gene therapy for hemophilia A
Authors
Yuni Yamaki
Takashi Fukushima
Naomi Yoshida
Ken Nishimura
Aya Fukuda
Koji Hisatake
Masayuki Aso
Tomoki Sakasai
Junko Kijima-Tanaka
Yoshihiro Miwa
Mahito Nakanishi
Ryo Sumazaki
Hidetoshi Takada
Publication date
01-04-2021
Publisher
Springer Singapore
Published in
International Journal of Hematology / Issue 4/2021
Print ISSN: 0925-5710
Electronic ISSN: 1865-3774
DOI
https://doi.org/10.1007/s12185-020-03059-6

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