Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.
ADVANCED SEARCH
Log in
Top
Annals of Hematology
Published in: Annals of Hematology 5/2024

11-11-2023 | Hemophilia | Review Article

Non-viral and viral delivery systems for hemophilia A therapy: recent development and prospects

Authors: Ali Rajabi Zangi, Ala Amiri, Pouya Pazooki, Fatemeh Soltanmohammadi, Hamed Hamishehkar, Yousef Javadzadeh

Published in: Annals of Hematology | Issue 5/2024

Login to get access

Abstract

Recent advancements have focused on enhancing factor VIII half-life and refining its delivery methods, despite the well-established knowledge that factor VIII deficiency is the main clotting protein lacking in hemophilia. Consequently, both viral and non-viral delivery systems play a crucial role in enhancing the quality of life for hemophilia patients. The utilization of viral vectors and the manipulation of non-viral vectors through targeted delivery are significant advancements in the field of cellular and molecular therapies for hemophilia. These developments contribute to the progression of treatment strategies and hold great promise for improving the overall well-being of individuals with hemophilia. This review study comprehensively explores the application of viral and non-viral vectors in cellular (specifically T cell) and molecular therapy approaches, such as RNA, monoclonal antibody (mAb), and CRISPR therapeutics, with the aim of addressing the challenges in hemophilia treatment. By examining these innovative strategies, the study aims to shed light on potential solutions to enhance the efficacy and outcomes of hemophilia therapy.
Literature
1.
2.
Favier RM, Lavergne J-M, Costa J-M, Caron C, Mazurier C, Viémont Ml et al (2000) Unbalanced X-chromosome inactivation with a novel FVIII gene mutation resulting in severe hemophilia A in a female. Blood J Am Soc Hematol 96(13):4373–5
3.
Al-ghtani SK (2020) Future of gene therapy in hemophilia. J Univ Stud Incl Res 1(1):17–32
4.
Cohn EJ, Strong LE, Hughes W, Mulford D, Ashworth J, Melin ME et al (1946) Preparation and properties of serum and plasma proteins. IV. A System for the Separation into Fractions of the Protein and Lipoprotein Components of Biological Tissues and Fluids1a, b, c, d. J Am Chem Soc 68(3):459–75PubMedCrossRef
5.
Kasper C (2012) Judith Graham Pool and the discovery of cryoprecipitate. Haemophilia 18(6):833–835PubMedCrossRef
6.
Webster WP, Roberts HR, Thelin GM, Wagner RH, Brinkhous KM (1965) Clinical use of a new glycine-precipitated antihemophilic fraction. Am J Med Sci 250(6):643–651PubMedCrossRef
7.
Holstein K, Batorova A, Carvalho M, Fijnvandraat K, Holme P, Kavakli K et al (2016) Current view and outcome of ITI therapy-a change over time? Thromb Res 148:38–44PubMedCrossRef
8.
Chen C-Y, Tran DM, Cavedon A, Cai X, Rajendran R, Lyle MJ et al (2020) Treatment of hemophilia A using factor VIII messenger RNA lipid nanoparticles. Mol Ther-Nucleic Acids 20:534–544PubMedPubMedCentralCrossRef
9.
DeRosa F, Guild B, Karve S, Smith L, Love K, Dorkin J et al (2016) Therapeutic efficacy in a hemophilia B model using a biosynthetic mRNA liver depot system. Gene Ther 23(10):699–707PubMedPubMedCentralCrossRef
10.
Plug I, van der Bom JG, Peters M, Mauser-Bunschoten EP, de Goede-Bolder A, Heijnen L et al (2004) Thirty years of hemophilia treatment in the Netherlands, 1972–2001. Blood 104(12):3494–3500PubMedCrossRef
11.
Rosendaal F, Smit C, Briet E (1991) Hemophilia treatment in historical perspective: a review of medical and social developments. Ann Hematol 62(1):5–15PubMedCrossRef
12.
Mannucci PM, Tuddenham EG (2001) The hemophilias—from royal genes to gene therapy. N Engl J Med 344(23):1773–1779PubMedCrossRef
13.
Yatuv R, Robinson M, Dayan-Tarshish I, Baru M (2010) The use of PEGylated liposomes in the development of drug delivery applications for the treatment of hemophilia. Int J Nanomed 5:581
14.
15.
Adamson R (1994) Design and operation of a recombinant mammalian cell manufacturing process for rFVIII. Ann Haematol 68:S9–S14CrossRef
16.
Toole JJ, Knopf JL, Wozney JM, Sultzman LA, Buecker JL, Pittman DD et al (1984) Molecular cloning of a cDNA encoding human antihaemophilic factor. Nature 312(5992):342–347PubMedCrossRef
17.
Mannucci P (2003) AIDS, hepatitis and hemophilia in the 1980s: memoirs from an insider. J Thromb Haemost 1(10):2065–2069PubMedCrossRef
18.
Franchini M, Mannucci PM, editors (2014) The history of hemophilia. Seminars in thrombosis and hemostasis; Thieme Medical Publishers
19.
Ewenstein BM, Valentino L, Journeycake J, Tarantino M, Shapiro A, Blanchette V et al (2004) Consensus recommendations for use of central venous access devices in haemophilia. Haemophilia 10(5):629–48PubMedCrossRef
20.
Santagostino E, Mancuso M (2010) Venous access in haemophilic children: choice and management. Haemophilia 16:20–24PubMedCrossRef
21.
Franchini M, Lippi G, editors (2010) Recombinant factor VIII concentrates. Seminars in thrombosis and hemostasis; © Thieme Medical Publishers
22.
Franchini M (2010) Plasma-derived versus recombinant Factor VIII concentrates for the treatment of haemophilia A: recombinant is better. Blood Transfus 8(4):292PubMedPubMedCentral
23.
Santagostino E (2014) A new recombinant factor VIII: from genetics to clinical use. Drug Des Dev Ther 8:2507CrossRef
24.
Björkman S, Berntorp E (2001) Pharmacokinetics of coagulation factors. Clin Pharmacokinet 40(11):815–832PubMedCrossRef
25.
Bovenschen N, Mertens K, Hu L, Havekes LM, van Vlijmen BJ (2005) LDL receptor cooperates with LDL receptor–related protein in regulating plasma levels of coagulation factor VIII in vivo. Blood 106(3):906–912PubMedCrossRef
26.
Sarafanov AG, Ananyeva NM, Shima M, Saenko EL (2001) Cell surface heparan sulfate proteoglycans participate in factor VIII catabolism mediated by low density lipoprotein receptor-related protein. J Biol Chem 276(15):11970–11979PubMedCrossRef
27.
Mei B, Pan C, Jiang H, Tjandra H, Strauss J, Chen Y et al (2010) Rational design of a fully active, long-acting PEGylated factor VIII for hemophilia A treatment. Blood J Am Soc Hematol 116(2):270–279
28.
29.
Veronese FM, Mero A (2008) The impact of PEGylation on biological therapies. BioDrugs 22(5):315–329PubMedCrossRef
30.
Fishburn CS (2008) The pharmacology of PEGylation: balancing PD with PK to generate novel therapeutics. J Pharm Sci 97(10):4167–4183PubMedCrossRef
31.
Zangi AR, Amiri A, Borzouee F, Bagherifar R, Pazooki P, Hamishehkar H et al (2023) Immobilized nanoparticles-mediated enzyme therapy; promising way into clinical development. Discover Nano 18(1):55PubMedPubMedCentralCrossRef
32.
Thim L, Vandahl B, Karlsson J, Klausen N, Pedersen J, Krogh T et al (2010) Purification and characterization of a new recombinant factor VIII (N8). Haemophilia 16(2):349–359PubMedCrossRef
33.
Martinowitz U, Bjerre J, Brand B, Klamroth R, Misgav M, Morfini M et al (2011) Bioequivalence between two serum-free recombinant factor VIII preparations (N8 and ADVATE®)–an open-label, sequential dosing pharmacokinetic study in patients with severe haemophilia A. Haemophilia 17(6):854–859PubMedCrossRef
34.
Agersø H, Stennicke H, Pelzer H, Olsen E, Merricks E, Defriess N et al (2012) Pharmacokinetics and pharmacodynamics of turoctocog alfa and N8-GP in haemophilia A dogs. Haemophilia 18(6):941–947PubMedPubMedCentralCrossRef
35.
Tiede A, Brand B, Fischer R, Kavakli K, Lentz S, Matsushita T et al (2013) Enhancing the pharmacokinetic properties of recombinant factor VIII: first-in-human trial of glyco PEG ylated recombinant factor VIII in patients with hemophilia A. J Thromb Haemost 11(4):670–678PubMedCrossRef
36.
Cantore A, Naldini L (2021) WFH State-of-the-art paper 2020: In vivo lentiviral vector gene therapy for haemophilia. Haemophilia 27:122–125PubMedCrossRef
37.
Shen BW, Spiegel PC, Chang C-H, Huh J-W, Lee J-S, Kim J et al (2008) The tertiary structure and domain organization of coagulation factor VIII. Blood J Am Soc Hematol 111(3):1240–1247
38.
Ngo JCK, Huang M, Roth DA, Furie BC, Furie B (2008) Crystal structure of human factor VIII: implications for the formation of the factor IXa-factor VIIIa complex. Structure 16(4):597–606PubMedCrossRef
39.
Kempton C, Abshire T, Deveras R, Hoots W, Gill J, Kessler C et al (2012) Pharmacokinetics and safety of OBI-1, a recombinant B domain-deleted porcine factor VIII, in subjects with haemophilia A. Haemophilia 18(5):798–804PubMedCrossRef
40.
Parker E, Craddock H, Barrow R, Lollar P (2004) Comparative immunogenicity of recombinant B domain-deleted porcine factor VIII and Hyate: C in hemophilia A mice presensitized to human factor VIII. J Thromb Haemost 2(4):605–611PubMedCrossRef
41.
Turner NA, Moake JL (2015) Factor VIII is synthesized in human endothelial cells, packaged in Weibel-Palade bodies and secreted bound to ULVWF strings. PLoS One 10(10):e0140740PubMedPubMedCentralCrossRef
42.
Kannicht C, Ramström M, Kohla G, Tiemeyer M, Casademunt E, Walter O et al (2013) Characterisation of the post-translational modifications of a novel, human cell line-derived recombinant human factor VIII. Thromb Res 131(1):78–88PubMedCrossRef
43.
Everett LA, Cleuren AC, Khoriaty RN, Ginsburg D (2014) Murine coagulation factor VIII is synthesized in endothelial cells. Blood J Am Soc Hematol 123(24):3697–3705
44.
Jiang R, Monroe T, McRogers R, Larson P (2002) Manufacturing challenges in the commercial production of recombinant coagulation factor VIII. Haemophilia 8:1–5PubMedCrossRef
45.
Lenting PJ, Van Mourik JA, Mertens K (1998) The life cycle of coagulation factor VIII in view of its structure and function. Blood J Am Soc Hematol 92(11):3983–3996
46.
Pipe SW (2005) The promise and challenges of bioengineered recombinant clotting factors. J Thromb Haemost 3(8):1692–1701PubMedCrossRef
47.
Parker ET, Healey JF, Barrow RT, Craddock HN, Lollar P (2004) Reduction of the inhibitory antibody response to human factor VIII in hemophilia A mice by mutagenesis of the A2 domain B-cell epitope. Blood 104(3):704–710PubMedCrossRef
48.
Chao H, Mao L, Bruce AT, Walsh CE (2000) Sustained expression of human factor VIII in mice using a parvovirus-based vector. Blood J Am Soc Hematol 95(5):1594–1599
49.
50.
Collins PW, Chalmers E, Hart DP, Liesner R, Rangarajan S, Talks K et al (2013) Diagnosis and treatment of factor VIII and IX inhibitors in congenital haemophilia. Br J Haematol 160(2):153–170PubMedCrossRef
51.
DeFrates SR, McDonagh KT, Adams VR (2013) The reversal of inhibitors in congenital hemophilia. Pharmacother J Human Pharmacol Drug Ther 33(2):157–64CrossRef
52.
Makris M, Kasper C (2013) The World Federation of Hemophilia guideline on management of haemophilia. Haemophilia Off J World Fed Hemophilia 19(1):1CrossRef
53.
Prescott R, Nakai H, Saenko EL, Scharrer I, Nilsson IM, Humphries JE et al (1997) The inhibitor antibody response is more complex in hemophilia A patients than in most nonhemophiliacs with factor VIII autoantibodies. Blood J Am Soc Hematol 89(10):3663–3671
54.
Hay C (2000) Porcine factor VIII: past, present and future. Haematologica 85(10 Suppl):21–4 (discussion 4)PubMed
55.
56.
Lusher JM (1999) Gene therapy for hemophilia A and B: Patient selection and follow-up, requirements for a cure. Thromb Haemost 82(08):572–575PubMedCrossRef
57.
Thompson AR (2000) Gene therapy for the haemophilias. Haemophilia Off J World Fed Hemophilia 6:115–9CrossRef
58.
High KA, editor Gene transfer as an approach to treating hemophilia. Seminars in thrombosis and hemostasis; 2003: Copyright© 2003 by Thieme Medical Publishers, Inc., 333 Seventh Avenue, New ….
59.
Roth D, Tawa N, O'Brien J, Levine J, Furie B, Furie B, et al., editors. Non-viral gene transfer of blood coagulation factor VIII in patients with severe hemophilia A. Blood; 2000: AMER SOC HEMATOLOGY 2021 L ST NW, SUITE 900, WASHINGTON, DC 20036 USA
60.
Shenk Ti. Adenoviridae: the viruses and their replication, Fields Virology. Fields BN Knipe DM Howley PM. 1996;2111
61.
Graham FL, Smiley J, Russell W, Nairn R (1977) Characteristics of a human cell line transformed by DNA from human adenovirus type 5. J Gen Virol 36(1):59–72PubMedCrossRef
62.
Gallo-Penn AM, Shirley PS, Andrews JL, Tinlin S, Webster S, Cameron C et al (2001) Systemic delivery of an adenoviral vector encoding canine factor VIII results in short-term phenotypic correction, inhibitor development, and biphasic liver toxicity in hemophilia A dogs. Blood J Am Soc Hematol 97(1):107–113
63.
Brann T, Kayda D, Lyons RM, Shirley P, Roy S, Kaleko M et al (1999) Adenoviral vector-mediated expression of physiologic levels of human factor VIII in nonhuman primates. Hum Gene Ther 10(18):2999–3011PubMedCrossRef
64.
Connelly S, Gardner JM, McClelland A, Kaleko M (1996) High-level tissue-specific expression of functional human factor VIII in mice. Hum Gene Ther 7(2):183–195PubMedCrossRef
65.
Connelly S, Andrews JL, Gallo AM, Kayda DB, Qian J, Hoyer L et al (1998) Sustained phenotypic correction of murine hemophilia A by in vivo gene therapy. Blood J Am Soc Hematol 91(9):3273–3281
66.
Connelly S, Mount J, Mauser A, Gardner JM, Kaleko M, McClelland A, et al (1996) Complete short-term correction of canine hemophilia A by in vivo gene therapy
67.
Dai Y, Schwarz EM, Gu D, Zhang W-W, Sarvetnick N, Verma IM (1995) Cellular and humoral immune responses to adenoviral vectors containing factor IX gene: tolerization of factor IX and vector antigens allows for long-term expression. Proc Natl Acad Sci 92(5):1401–1405PubMedPubMedCentralCrossRef
68.
Yang Y, Nunes FA, Berencsi K, Furth EE, Gönczöl E, Wilson JM (1994) Cellular immunity to viral antigens limits E1-deleted adenoviruses for gene therapy. Proc Natl Acad Sci 91(10):4407–4411PubMedPubMedCentralCrossRef
69.
Yang Y, Li Q, Ertl H, Wilson JM (1995) Cellular and humoral immune responses to viral antigens create barriers to lung-directed gene therapy with recombinant adenoviruses. J Virol 69(4):2004–2015PubMedPubMedCentralCrossRef
70.
Parks RJ, Chen L, Anton M, Sankar U, Rudnicki MA, Graham FL (1996) A helper-dependent adenovirus vector system: removal of helper virus by Cre-mediated excision of the viral packaging signal. Proc Natl Acad Sci 93(24):13565–13570PubMedPubMedCentralCrossRef
71.
Balagué C, Zhou J, Dai Y, Alemany R, Josephs SF, Andreason G et al (2000) Sustained high-level expression of full-length human factor VIII and restoration of clotting activity in hemophilic mice using a minimal adenovirus vector. Blood J Am Soc Hematol 95(3):820–828
72.
Kumar-Singh R, Chamberlain JS (1996) Encapsidated adenovirus minichromosomes allow delivery and expression of a 14 kb dystrophin cDNA to muscle cells. Hum Mol Genet 5(7):913–921PubMedCrossRef
73.
Schiedner G, Morral N, Parks RJ, Wu Y, Koopmans SC, Langston C et al (1998) Genomic DNA transfer with a high-capacity adenovirus vector results in improved in vivo gene expression and decreased toxicity. Nat Genet 18(2):180–183PubMedCrossRef
74.
Maione D, Wiznerowicz M, Delmastro P, Cortese R, Ciliberto G, Monica NL et al (2000) Prolonged expression and effective readministration of erythropoietin delivered with a fully deleted adenoviral vector. Hum Gene Ther 11(6):859–868PubMedCrossRef
75.
Palmer D, Ng P (2003) Improved system for helper-dependent adenoviral vector production. Mol Ther 8(5):846–852PubMedCrossRef
76.
Brown BD, Shi CX, Powell S, Hurlbut D, Graham FL, Lillicrap D (2004) Helper-dependent adenoviral vectors mediate therapeutic factor VIII expression for several months with minimal accompanying toxicity in a canine model of severe hemophilia A. Blood 103(3):804–810PubMedCrossRef
77.
McCormack W Jr, Seiler M, Bertin T, Ubhayakar K, Palmer D, Ng P et al (2006) Helper-dependent adenoviral gene therapy mediates long-term correction of the clotting defect in the canine hemophilia A model. J Thromb Haemost 4(6):1218–1225PubMedPubMedCentralCrossRef
78.
Gringeri A, Mantovani LG, Scalone L, Mannucci PM, Group CS (2003) Cost of care and quality of life for patients with hemophilia complicated by inhibitors: the COCIS Study Group. Blood 102(7):2358–63PubMedCrossRef
79.
Hu C, Cela RG, Suzuki M, Lee B, Lipshutz GS (2011) Neonatal helper-dependent adenoviral vector gene therapy mediates correction of hemophilia A and tolerance to human factor VIII. Proc Natl Acad Sci 108(5):2082–2087PubMedPubMedCentralCrossRef
80.
Jiang H, Lillicrap D, Patarroyo-White S, Liu T, Qian X, Scallan CD et al (2006) Multiyear therapeutic benefit of AAV serotypes 2, 6, and 8 delivering factor VIII to hemophilia A mice and dogs. Blood 108(1):107–115PubMedCrossRef
81.
Rangarajan S, Walsh L, Lester W, Perry D, Madan B, Laffan M et al (2017) AAV5–factor VIII gene transfer in severe hemophilia A. N Engl J Med 377(26):2519–2530PubMedCrossRef
82.
McIntosh J, Lenting PJ, Rosales C, Lee D, Rabbanian S, Raj D et al (2013) Therapeutic levels of FVIII following a single peripheral vein administration of rAAV vector encoding a novel human factor VIII variant. Blood J Am Soc Hematol 121(17):3335–3344
83.
Ozelo MC, Mahlangu J, Pasi KJ, Giermasz A, Leavitt AD, Laffan M et al (2022) Valoctocogene roxaparvovec gene therapy for hemophilia A. N Engl J Med 386(11):1013–1025PubMedCrossRef
84.
Nathwani AC, Reiss UM, Tuddenham EG, Rosales C, Chowdary P, McIntosh J et al (2014) Long-term safety and efficacy of factor IX gene therapy in hemophilia B. N Engl J Med 371(21):1994–2004PubMedPubMedCentralCrossRef
85.
Pasi KJ, Rangarajan S, Mitchell N, Lester W, Symington E, Madan B et al (2020) Multiyear follow-up of AAV5-hFVIII-SQ gene therapy for hemophilia A. N Engl J Med 382(1):29–40PubMedCrossRef
86.
Weber A, Engelmaier A, Voelkel D, Pachlinger R, Scheiflinger F, Monahan PE et al (2018) Development of methods for the selective measurement of the single amino acid exchange variant coagulation factor IX Padua. Mol Ther-Methods Clin Dev 10:29–37PubMedPubMedCentralCrossRef
87.
Matsui H, Shibata M, Brown B, Labelle A, Hegadorn C, Andrews C et al (2007) 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 25(10):2660–2669PubMedCrossRef
88.
Gong J, Chung T-H, Zheng J, Zheng H, Chang L-J (2021) Transduction of modified factor VIII gene improves lentiviral gene therapy efficacy for hemophilia A. J Biol Chem. 297(6):101397
89.
Crawford B, Ozelo MC, Ogiwara K, Ahlin J, Albanez S, Hegadorn C et al (2015) Transgene-host cell interactions mediate significant influences on the production, stability, and function of recombinant canine FVIII. Mol Ther-Methods Clin Dev 2:15033PubMedPubMedCentralCrossRef
90.
Ward NJ, Buckley SM, Waddington SN, VandenDriessche T, Chuah MK, Nathwani AC et al (2011) Codon optimization of human factor VIII cDNAs leads to high-level expression. Blood J Am Soc Hematol 117(3):798–807
91.
Mingozzi F, High KA (2013) Immune responses to AAV vectors: overcoming barriers to successful gene therapy. Blood J Am Soc Hematol 122(1):23–36
92.
Rogers GL, Shirley JL, Zolotukhin I, Kumar SR, Sherman A, Perrin GQ et al (2017) Plasmacytoid and conventional dendritic cells cooperate in crosspriming AAV capsid-specific CD8+ T cells. Blood J Am Soc Hematol 129(24):3184–3195
93.
Ramezani A, Hawley RG (2009) Correction of murine hemophilia A following nonmyeloablative transplantation of hematopoietic stem cells engineered to encode an enhanced human factor VIII variant using a safety-augmented retroviral vector. Blood J Am Soc Hematol 114(3):526–534
94.
Song S, Lyle MJ, Noble-Vranish ML, Min-Tran DM, Harrang J, Xiao W, et al (2022) Ultrasound-mediated gene delivery of factor VIII plasmids for hemophilia A gene therapy in mice. Mol Ther-Nucleic Acids
95.
96.
Ding S, Wu X, Li G, Han M, Zhuang Y, Xu T (2005) Efficient transposition of the piggyBac (PB) transposon in mammalian cells and mice. Cell 122(3):473–483PubMedCrossRef
97.
Zhao S, Jiang E, Chen S, Gu Y, Shangguan AJ, Lv T et al (2016) PiggyBac transposon vectors: the tools of the human gene encoding. Transl lung Cancer Res 5(1):120PubMedPubMedCentral
98.
Matsui H, Fujimoto N, Sasakawa N, Ohinata Y, Shima M, Yamanaka S et al (2014) Delivery of full-length factor VIII using a piggyBac transposon vector to correct a mouse model of hemophilia A. PLoS One 9(8):e104957PubMedPubMedCentralCrossRef
99.
Noda M, Tatsumi K, Matsui H, Matsunari Y, Sato T, Fukuoka Y et al (2021) Development of alternative gene transfer techniques for ex vivo and in vivo gene therapy in a canine model. Regen Ther 18:347–354PubMedPubMedCentralCrossRef
100.
Amoabediny G, Khakbiz M, Jafarkhani S, Mohammadi J, Ilanlou S, Khajouei F et al (2023) The effect of nano-liposomal sodium nitrite on smooth muscle cell growth in a tissue-engineered small-diameter vascular graft. Artif Organs 47(7):1104–1121PubMedCrossRef
101.
Kiaie SH, Majidi Zolbanin N, Ahmadi A, Bagherifar R, Valizadeh H, Kashanchi F et al (2022) Recent advances in mRNA-LNP therapeutics: immunological and pharmacological aspects. J Nanobiotechnol 20(1):276CrossRef
102.
Kiaie SH, Mojarad-Jabali S, Khaleseh F, Allahyari S, Taheri E, Zakeri-Milani P et al (2020) Axial pharmaceutical properties of liposome in cancer therapy: recent advances and perspectives. Int J Pharm 581:119269PubMedCrossRef
103.
Debbage P (2009) Targeted drugs and nanomedicine: present and future. Curr Pharm Des 15(2):153–172PubMedCrossRef
104.
Caliceti P, Veronese FM (2003) Pharmacokinetic and biodistribution properties of poly (ethylene glycol)–protein conjugates. Adv Drug Deliv Rev 55(10):1261–1277PubMedCrossRef
105.
Photos PJ, Bacakova L, Discher B, Bates FS, Discher DE (2003) Polymer vesicles in vivo: correlations with PEG molecular weight. J Control Release 90(3):323–334PubMedCrossRef
106.
Spira J, Plyushch OP, Andreeva TA, Andreev Y (2006) Prolonged bleeding-free period following prophylactic infusion of recombinant factor VIII reconstituted with pegylated liposomes. Blood 108(12):3668–3673PubMedCrossRef
107.
Powell J, Martinowitz U, Windyga J, Di Minno G, Hellmann A, Pabinger I et al (2012) Efficacy and safety of prophylaxis with once-weekly BAY 79–4980 compared with thrice-weekly rFVIII-FS in haemophilia A patients. Thromb Haemost 108(11):913–922PubMedCrossRef
108.
Di Minno G, Cerbone A, Coppola A, Cimino E, Di Capua M, Pamparana F et al (2010) Longer-acting factor VIII to overcome limitations in haemophilia management: the PEGylated liposomes formulation issue. Haemophilia 16:2–6PubMedCrossRef
109.
Lin Q, Chen J, Zhang Z, Zheng G (2014) Lipid-based nanoparticles in the systemic delivery of siRNA. Nanomedicine 9(1):105–120PubMedCrossRef
110.
Hassett KJ, Benenato KE, Jacquinet E, Lee A, Woods A, Yuzhakov O et al (2019) Optimization of lipid nanoparticles for intramuscular administration of mRNA vaccines. Mol Ther-Nucleic Acids 15:1–11PubMedPubMedCentralCrossRef
111.
Cao J, An D, Galduroz M, Zhuo J, Liang S, Eybye M et al (2019) mRNA therapy improves metabolic and behavioral abnormalities in a murine model of citrin deficiency. Mol Ther 27(7):1242–1251PubMedPubMedCentralCrossRef
112.
Kwon H, Kim M, Seo Y, Moon YS, Lee HJ, Lee K et al (2018) Emergence of synthetic mRNA: In vitro synthesis of mRNA and its applications in regenerative medicine. Biomaterials 156:172–193PubMedCrossRef
113.
Karikó K, Muramatsu H, Welsh FA, Ludwig J, Kato H, Akira S et al (2008) Incorporation of pseudouridine into mRNA yields superior nonimmunogenic vector with increased translational capacity and biological stability. Mol Ther 16(11):1833–1840PubMedCrossRef
114.
Vaidyanathan S, Azizian KT, Haque AA, Henderson JM, Hendel A, Shore S et al (2018) Uridine depletion and chemical modification increase Cas9 mRNA activity and reduce immunogenicity without HPLC purification. Mol Ther-Nucleic Acids 12:530–542PubMedPubMedCentralCrossRef
115.
Saenko EL, Ananyeva NM, Moayeri M, Ramezani A, Hawley RG (2003) Development of improved factor VIII molecules and new gene transfer approaches for hemophilia A. Curr Gene Ther 3(1):27–41PubMedCrossRef
116.
Shetty KA, Kosloski MP, Mager DE, Balu-Iyer SV (2015) Soy phosphatidylinositol containing nanoparticle prolongs hemostatic activity of B-domain deleted factor VIII in hemophilia A mice. J Pharm Sci 104(2):388–395PubMedCrossRef
117.
Kiaie S, Karami C, Khodadadian A, Taher M, Soltanian S (2016) A facile method for detection of N-acetylcysteine and l-cysteine with silver nanoparticle in aqueous environments. J Bioequiv Availab 8:197–203
118.
Tavana B, Khatibi A, Jafarkhani S, Zahedi P, Hossein Zamani M, Hassan Jafari S et al (2023) Simulation and in vitro evaluations of microfluidically-fabricated clarithromycin-poly (ε-caprolactone) nanoparticles. J Ind Eng Chem 124:211–223CrossRef
119.
Mao H-Q, Roy K, Troung-Le VL, Janes KA, Lin KY, Wang Y et al (2001) Chitosan-DNA nanoparticles as gene carriers: synthesis, characterization and transfection efficiency. J Control Release 70(3):399–421PubMedCrossRef
120.
Bowman K, Sarkar R, Raut S, Leong KW (2008) Gene transfer to hemophilia A mice via oral delivery of FVIII–chitosan nanoparticles. J Control Release 132(3):252–259PubMedPubMedCentralCrossRef
121.
Ling D, Hyeon T (2013) Iron oxide nanoparticles: chemical design of biocompatible iron oxide nanoparticles for medical applications (Small 9–10/2013). Small 9(9–10):1449-CrossRef
122.
Ling D, Hyeon T (2013) Chemical design of biocompatible iron oxide nanoparticles for medical applications. Small 9(9–10):1450–1466PubMedCrossRef
123.
Wang J, Chen Y, Chen B, Ding J, Xia G, Gao C et al (2010) Pharmacokinetic parameters and tissue distribution of magnetic Fe3O4 nanoparticles in mice. Int J Nanomed 5:861
124.
Cristofolini L, Berzina T, Erokhina S, Konovalov O, Erokhin V (2007) Structural study of the DNA dipalmitoylphosphatidylcholine complex at the air− water interface. Biomacromol 8(7):2270–2275CrossRef
125.
Filion MC, Phillips NC (1997) Toxicity and immunomodulatory activity of liposomal vectors formulated with cationic lipids toward immune effector cells. Biochim Biophys Acta (BBA)-Biomembr 1329(2):345–56CrossRef
126.
Kao Y-T, Chen Y-T, Fan H-C, Tsai T-C, Cheng S-N, Lai P-S et al (2021) Novel coagulation factor viii gene therapy in a mouse model of hemophilia a by lipid-coated fe3o4 nanoparticles. Biomedicines 9(9):1116PubMedPubMedCentralCrossRef
127.
128.
Brown BD, Lillicrap D (2002) Dangerous liaisons: the role of “danger” signals in the immune response to gene therapy. Blood J Am Soc Hematol 100(4):1133–1140
129.
Boutin S, Monteilhet V, Veron P, Leborgne C, Benveniste O, Montus MF et al (2010) Prevalence of serum IgG and neutralizing factors against adeno-associated virus (AAV) types 1, 2, 5, 6, 8, and 9 in the healthy population: implications for gene therapy using AAV vectors. Hum Gene Ther 21(6):704–712PubMedCrossRef
130.
Ohmori T, Mizukami H, Ozawa K, Sakata Y, Nishimura S (2015) New approaches to gene and cell therapy for hemophilia. J Thromb Haemost 13:S133–S142PubMedCrossRef
131.
Roth DA, Tawa NE Jr, O’Brien JM, Treco DA, Selden RF (2001) Nonviral transfer of the gene encoding coagulation factor VIII in patients with severe hemophilia A. N Engl J Med 344(23):1735–1742PubMedCrossRef
132.
Hoeben R, Einerhand M, Briet E, Van Ormondt H, Valerio D, Van Der Eb A (1992) Toward gene therapy in haemophilia A: retrovirus-mediated transfer of a factor VIII gene into murine haematopoietic progenitor cells. Thromb Haemost 67(03):341–345PubMedCrossRef
133.
Moayeri M, Ramezani A, Morgan RA, Hawley TS, Hawley RG (2004) Sustained phenotypic correction of hemophilia a mice following oncoretroviral-mediated expression of a bioengineered human factor VIII gene in long-term hematopoietic repopulating cells. Mol Ther 10(5):892–902PubMedCrossRef
134.
Wang Q, Gong X, Gong Z, Ren X, Ren Z, Huang S et al (2013) The mesenchymal stem cells derived from transgenic mice carrying human coagulation factor VIII can correct phenotype in hemophilia A mice. J Genet Genomics 40(12):617–628PubMedCrossRef
135.
Park C-Y, Kim J, Kweon J, Son JS, Lee JS, Yoo J-E et al (2014) Targeted inversion and reversion of the blood coagulation factor 8 gene in human iPS cells using TALENs. Proc Natl Acad Sci 111(25):9253–9258PubMedPubMedCentralCrossRef
136.
Wang J, Kuang Y, Zhang L, Shen C, Wang L, Lu S et al (2013) Phenotypic correction and stable expression of factor VIII in hemophilia A mice by embryonic stem cell therapy. Genet Mol Res 12(2):1511–1521PubMedCrossRef
137.
Cucci A, Olgasi C, Merlin S, Borsotti C, Bergmann T, Bittorf P, et al (2020) Combined gene and cell therapy for the treatment of hemophilia A within an implantable therapeutic device
138.
Evans GL, Morgan RA (1998) Genetic induction of immune tolerance to human clotting factor VIII in a mouse model for hemophilia A. Proc Natl Acad Sci 95(10):5734–5739PubMedPubMedCentralCrossRef
139.
Ally BA, Hawley TS, McKall-Faienza KJ, Kündig T, Oehen SU, Pircher H et al (1995) Prevention of autoimmune disease by retroviral-mediated gene therapy. J Immunol 155(11):5404–5408PubMedCrossRef
140.
Forman D, Tian C, Iacomini J (2005) Induction of donor-specific tolerance in sublethally irradiated recipients by gene therapy. Mol Ther 12(2):353–359PubMedCrossRef
141.
Tian C, Bagley J, Forman D, Iacomini J (2004) Induction of central tolerance by mature T cells. J Immunol 173(12):7217–7222PubMedCrossRef
142.
Moayeri M, Hawley TS, Hawley RG (2005) Correction of murine hemophilia A by hematopoietic stem cell gene therapy. Mol Ther 12(6):1034–1042PubMedCrossRef
143.
144.
Bochenek MA, Veiseh O, Vegas AJ, McGarrigle JJ, Qi M, Marchese E et al (2018) Alginate encapsulation as long-term immune protection of allogeneic pancreatic islet cells transplanted into the omental bursa of macaques. Nat Biomed Eng 2(11):810–821PubMedPubMedCentralCrossRef
145.
Barney L, Heidebrecht Jr RW, Carmona G, Sewell J, Oberli M, Huang J, et al., editors. Optimization of shielded encapsulated cell therapy for hemophilia and beyond. Molecular Therapy; 2020: CELL PRESS 50 HAMPSHIRE ST, FLOOR 5, CAMBRIDGE, MA 02139 USA
146.
Shapiro AD, Konkle BA, Croteau SE, Miesbach WA, Hay CRM, Kazmi R et al (2020) First-in-human phase 1/2 clinical trial of SIG-001, an innovative shielded cell therapy platform, for hemophilia Α. Blood 136:8
147.
Parvathaneni K, Abdeladhim M, Pratt KP, Scott DW (2017) Hemophilia A inhibitor treatment: the promise of engineered T-cell therapy. Transl Res 187:44–52PubMedPubMedCentralCrossRef
148.
Sarkar D, Biswas M, Liao G, Seay HR, Perrin GQ, Markusic DM et al (2014) Ex vivo expanded autologous polyclonal regulatory T cells suppress inhibitor formation in hemophilia. Mol Ther-Methods Clin Dev 1:14030PubMedPubMedCentralCrossRef
149.
Smith BM, Lyle MJ, Chen AC, Miao CH (2020) Antigen-specific in vitro expansion of factor VIII-specific regulatory T cells induces tolerance in hemophilia A mice. J Thromb Haemost 18(2):328–340PubMedCrossRef
150.
Chai J-G, Coe D, Chen D, Simpson E, Dyson J, Scott D (2008) In vitro expansion improves in vivo regulation by CD4+ CD25+ regulatory T cells. J Immunol 180(2):858–869PubMedCrossRef
151.
Ojeda G, Pini E, Eguiluz C, Montes-Casado M, Broere F, van Eden W et al (2011) Complement regulatory protein Crry/p65 costimulation expands natural treg cells with enhanced suppressive properties in proteoglycan-induced arthritis. Arthritis Rheum 63(6):1562–1572PubMedCrossRef
152.
Kitazawa T, Igawa T, Sampei Z, Muto A, Kojima T, Soeda T et al (2012) A bispecific antibody to factors IXa and X restores factor VIII hemostatic activity in a hemophilia A model. Nat Med 18(10):1570–1574PubMedCrossRef
153.
Kanasty R, Dorkin JR, Vegas A, Anderson D (2013) Delivery materials for siRNA therapeutics. Nat Mater 12(11):967–977PubMedCrossRef
154.
Lee K, Jang B, Lee Y-R, Suh E-Y, Yoo J-S, Lee M-J et al (2018) The cutting-edge technologies of siRNA delivery and their application in clinical trials. Arch Pharm Res 41(9):867–74PubMedCrossRef
155.
156.
Pasi KJ, Lissitchkov T, Mamonov V, Mant T, Timofeeva M, Bagot C et al (2021) Targeting of antithrombin in hemophilia A or B with investigational siRNA therapeutic fitusiran—results of the phase 1 inhibitor cohort. J Thromb Haemost 19(6):1436–1446PubMedPubMedCentralCrossRef
157.
Cano V, Bartelt-Hofer J, Hu W, Andersson SR, Dasmahapatra P, Von Mackensen S (2021) Sustained improvement in health-related quality of life in patients with hemophilia A with or without inhibitors treated with fitusiran prophylaxis. Blood 138:3197CrossRef
158.
Park C-Y, Kim DH, Son JS, Sung JJ, Lee J, Bae S et al (2015) Functional correction of large factor VIII gene chromosomal inversions in hemophilia A patient-derived iPSCs using CRISPR-Cas9. Cell Stem Cell 17(2):213–220PubMedCrossRef
159.
Son JS, Park C-Y, Lee G, Park JY, Kim HJ, Kim G et al (2022) Therapeutic correction of hemophilia A using 2D endothelial cells and multicellular 3D organoids derived from CRISPR/Cas9-engineered patient iPSCs. Biomaterials 283:121429PubMedCrossRef
160.
Sung JJ, Park C-Y, Leem JW, Cho MS, Kim D-W (2019) Restoration of FVIII expression by targeted gene insertion in the FVIII locus in hemophilia A patient-derived iPSCs. Exp Mol Med 51(4):1–9PubMedCrossRef
161.
Kingdon HS, Lundblad RL (2002) An adventure in biotechnology: the development of haemophilia A therapeutics–from whole-blood transfusion to recombinant DNA to gene therapy. Biotechnol Appl Biochem 35(2):141–148PubMedCrossRef
162.
Peerlinck K, Hermans C (2006) Epidemiology of inhibitor formation with recombinant factor VIII replacement therapy. Haemophilia 12(6):579–590PubMedCrossRef
163.
Factor A, Factor C, Tarrytown N (2010) HELIXATE® FS. Director 267:685–2781 
164.
Pollmann H, Externest D, Ganser A, Eifrig B, Kreuz W, Lenk H et al (2007) Efficacy, safety and tolerability of recombinant factor VIII (REFACTO®) in patients with haemophilia A: interim data from a postmarketing surveillance study in Germany and Austria. Haemophilia 13(2):131–143PubMedCrossRef
165.
Lusher J, Lee C, Kessler C, Bedrosian C, Group RPS (2003) The safety and efficacy of B-domain deleted recombinant factor VIII concentrate in patients with severe haemophilia A. Haemophilia 9(1):38–49PubMedCrossRef
166.
Klamroth R, Simpson M, von Depka-Prondzinski M, Gill J, Morfini M, Powell JS et al (2016) Comparative pharmacokinetics of rVIII-SingleChain and octocog alfa (Advate®) in patients with severe haemophilia A. Haemophilia 22(5):730–738PubMedCrossRef
167.
Shapiro AD (2007) Anti-hemophilic factor (recombinant), plasma/albumin-free method (octocog-alpha; ADVATE®) in the management of hemophilia A. Vasc Health Risk Manag 3(5):555PubMedPubMedCentral
168.
Mahlangu J, Kuliczkowski K, Karim FA, Stasyshyn O, Kosinova MV, Lepatan LM et al (2016) Efficacy and safety of rVIII-SingleChain: results of a phase 1/3 multicenter clinical trial in severe hemophilia A. Blood J Am Soc Hematol 128(5):630–637
169.
Zollner SB, Raquet E, Müller-Cohrs J, Metzner HJ, Weimer T, Pragst I et al (2013) Preclinical efficacy and safety of rVIII-SingleChain (CSL627), a novel recombinant single-chain factor VIII. Thromb Res 132(2):280–287PubMedCrossRef
170.
Santagostino E, Lentz S, Misgav M, Brand B, Chowdary P, Savic A et al (2015) Safety and efficacy of turoctocog alfa (NovoEight®) during surgery in patients with haemophilia A: results from the multinational guardian™ clinical trials. Haemophilia 21(1):34–40PubMedCrossRef
171.
Jiménez-Yuste V, Lejniece S, Klamroth R, Suzuki T, Santagostino E, Karim F et al (2015) The pharmacokinetics of a B-domain truncated recombinant factor VIII, turoctocog alfa (NovoEight®), in patients with hemophilia A. J Thromb Haemost 13(3):370–379PubMedCrossRef
172.
Lissitchkov T, Klukowska A, Pasi J, Kessler CM, Klamroth R, Liesner RJ et al (2019) Efficacy and safety of simoctocog alfa (Nuwiq®) in patients with severe hemophilia A: a review of clinical trial data from the GENA program. Ther Adv Hematol 10:2040620719858471PubMedPubMedCentralCrossRef
173.
Keating GM (2016) BAY 81–8973 (Octocog Alfa; Kovaltry®): A Review in Haemophilia A. BioDrugs 30(5):453–459PubMedCrossRef
174.
D’Angiolella LS, Molinari AC, Cortesi PA, Coppola A, Mantovani LG (2017) Kovaltry® nel trattamento dell’emofilia A: aspetti clinici ed economici nei trial clinici registrativi
175.
George LA, Sullivan SK, Giermasz A, Rasko JE, Samelson-Jones BJ, Ducore J et al (2017) Hemophilia B gene therapy with a high-specific-activity factor IX variant. N Engl J Med 377(23):2215–2227PubMedPubMedCentralCrossRef
176.
Vandamme C, Adjali O, Mingozzi F (2017) Unraveling the complex story of immune responses to AAV vectors trial after trial. Hum Gene Ther 28(11):1061–1074PubMedPubMedCentralCrossRef
177.
178.
Siner JI, Iacobelli NP, Sabatino DE, Ivanciu L, Zhou S, Poncz M et al (2013) Minimal modification in the factor VIII B-domain sequence ameliorates the murine hemophilia A phenotype. Blood J Am Soc Hematol 121(21):4396–4403
179.
180.
181.
Doering CB, Denning G, Shields JE, Fine EJ, Parker ET, Srivastava A et al (2018) Preclinical development of a hematopoietic stem and progenitor cell bioengineered factor VIII lentiviral vector gene therapy for hemophilia A. Hum Gene Ther 29(10):1183–1201PubMedPubMedCentralCrossRef
182.
Berns K, Bohenzky R (1998) Adeno-associated virus expression system for gene transfer. Curr Opin Biotechnol 9:470–475CrossRef
183.
Dong J-Y, Fan P-D, Frizzell RA (1996) Quantitative analysis of the packaging capacity of recombinant adeno-associated virus. Hum Gene Ther 7(17):2101–2112PubMedCrossRef
Metadata
Title
Non-viral and viral delivery systems for hemophilia A therapy: recent development and prospects
Authors
Ali Rajabi Zangi
Ala Amiri
Pouya Pazooki
Fatemeh Soltanmohammadi
Hamed Hamishehkar
Yousef Javadzadeh
Publication date
11-11-2023
Publisher
Springer Berlin Heidelberg
Keyword
Hemophilia
Published in
Annals of Hematology / Issue 5/2024
Print ISSN: 0939-5555
Electronic ISSN: 1432-0584
DOI
https://doi.org/10.1007/s00277-023-05459-0

Other articles of this Issue 5/2024

Annals of Hematology 5/2024 Go to the issue

Correspondence

Concomitant large deletion and de novo duplication of factor VIII gene in an Indian patient with severe Hemophilia A

Original Article

Development of a whole spinal MRI-based tumor burden scoring method in participants with multiple myeloma: a pilot study of prognostic significance

Research

Impact of BK polyomavirus viremia on the outcomes of allogeneic hematopoietic stem cell transplantation

Original Article

Efficacy of prophylactic antibiotics for the prevention of neutropenic fever in patients with multiple myeloma receiving high-dose cyclophosphamide for stem cell mobilization

Editorial

Is eryptosis druggable?

Original Article

Spanish registry of hemoglobinopathies and rare anemias (REHem-AR): demographics, complications, and management of patients with β-thalassemia
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Reserve your place

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

Read more

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Pediatric Cardiology Video

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

Cardiopulmonary Comorbidity Video

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Valvular Heart Disease Video

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.

Watch now

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

16-04-2024 Type 2 Diabetes News

Incentivised to exercise

11-04-2024 Lifestyle Modifications News

New intervention for STEMI-related cardiogenic shock

10-04-2024 Myocardial Infarction News

» View more highlights on the ACC 2024 congress hub page

Image Credits