Perinatal systemic gene delivery using adeno-associated viral vectors

Frontiers in Molecular Neuroscience

Volumn 7, Issue November, 2014, Pages

  Karda, Rajvinder ^a   Buckley, Suzanne M K ^a   Mattar, Citra N ^b   Ng, Joanne ^a   Massaro, Giulia ^c   Hughes, Michael P ^c   Kurian, Manju A ^d   Baruteau, Julien ^a   Gissen, Paul ^d   Chan, Jerry K Y ^b   Bacchelli, Chiara ^d   Waddington, Simon N ^a,e   Rahim, Ahad A ^c  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c UNIVERSITY OF LONDON   (United Kingdom)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

^e UNIVERSITY OF THE WITWATERSRAND   (South Africa)

Author keywords

Adeno associated virus; Gene therapy; Metabolic disease; Mouse models; Neurodegenerative disease; Non human primates; Perinatal; Systemic delivery

Indexed keywords

PARVOVIRUS VECTOR; SURVIVAL MOTOR NEURON PROTEIN;

BLOOD BRAIN BARRIER; CENTRAL NERVOUS SYSTEM; DEGENERATIVE DISEASE; DISEASE MODEL; DOWN SYNDROME; GENE; GENE DELIVERY SYSTEM; GENE EXPRESSION; GENE TARGETING; GENETIC TRANSDUCTION; HUMAN; IMMUNE RESPONSE; MONOGENIC DISORDER; NEXT GENERATION SEQUENCING; NIEMANN PICK DISEASE; NONHUMAN; PERINATAL PERIOD; PHASE 1 CLINICAL TRIAL (TOPIC); PRENATAL SCREENING; PRIMATE; REVIEW; SMN GENE; SPINAL MUSCULAR ATROPHY; SYSTEMIC THERAPY;

EID: 84926033975     PISSN: 16625099     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnmol.2014.00089     Document Type: Review

References (54)

1. Aiuti, A., Biasco, L., Scaramuzza, S., Ferrua, F., Cicalese, M. P., Baricordi, C.,et al. (2013). Lentiviral hematopoietic stem cell gene therapy in patients with Wiskott-Aldrich syndrome. Science 341:1233151. doi: 10.1126/science.1233151.
2. Bainbridge, J. W., Smith, A. J., Barker, S. S., Robbie, S., Henderson, R., Balaggan, K.,et al. (2008). Effect of gene therapy on visual function in Leber's congenital amaurosis. N. Engl. J. Med. 358, 2231-2239. doi: 10.1056/NEJMoa0802268.
3. Bevan, A. K., Duque, S., Foust, K. D., Morales, P. R., Braun, L., Schmelzer, L.,et al. (2011). Systemic gene delivery in large species for targeting spinal cord, brain, and peripheral tissues for pediatric disorders. Mol. Ther. 19, 1971-1980. doi: 10.1038/mt.2011.157.
4. Bianchi, D. W., Platt, L. D., Goldberg, J. D., Abuhamad, A. Z., Sehnert, A. J., Rava, R. P.,et al. (2012). Genome-wide fetal aneuploidy detection by maternal plasma DNA sequencing. Obstet. Gynecol. 119, 890-901. doi: 10.1097/AOG.0b013e31824fb482.
5. Biffi, A., Montini, E., Lorioli, L., Cesani, M., Fumagalli, F., Plati, T.,et al. (2013). Lentiviral hematopoietic stem cell gene therapy benefits metachromatic leukodystrophy. Science 341:1233158. doi: 10.1126/science.1233158.
6. Boutin, S., Monteilhet, V., Veron, P., Leborgne, C., Benveniste, O., Montus, M. F.,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, 704-712. doi: 10.1089/hum.2009.182.
7. Buckley, S. M., Rahim, A. A., Chan, J. K., David, A. L., Peebles, D. M., Coutelle, C.,et al. (2011). Recent advances in fetal gene therapy. Ther. Deliv. 2, 461-469. doi: 10.4155/tde.11.17.
8. Cartier, N., Hacein-Bey-Abina, S., Bartholomae, C. C., Veres, G., Schmidt, M., Kutschera, I.,et al. (2009). Hematopoietic stem cell gene therapy with a lentiviral vector in X-linked adrenoleukodystrophy. Science 326, 818-823. doi: 10.1126/science.1171242.
9. Cecchini, S., Virag, T., and Kotin, R. M. (2011). Reproducible high yields of recombinant adeno-associated virus produced using invertebrate cells in 0.02-to 200-liter cultures. Hum. Gene Ther. 22, 1021-1030. doi: 10.1089/hum.2010.250.
10. Coutelle, C., and Ashcroft, R. (2012). Risks, benefits and ethical, legal, and societal considerations for translation of prenatal gene therapy to human application. Methods Mol. Biol. 891, 371-387. doi: 10.1007/978-1-61779-873-3_17.
11. Coutelle, C., and Waddington, S. N. (2012). The concept of prenatal gene therapy. Methods Mol. Biol. 891, 1-7. doi: 10.1007/978-1-61779-873-3_1.
12. Cox, T. M. (2013). Competing for the treasure in exceptions. Am. J. Hematol. 88, 163-165. doi: 10.1002/ajh.23399.
13. Daley, R., Hill, M., and Chitty, L. S. (2014). Non-invasive prenatal diagnosis: progress and potential. Arch. Dis. Child Fetal Neonatal Ed. 99, 426-430. doi: 10.1136/archdischild-2013-304828.
14. David, A. L., and Peebles, D. (2008). Gene therapy for the fetus: is there a future? Best Pract. Res. Clin. Obstet. Gynaecol. 22, 203-218. doi: 10.1016/j.bpobgyn.2007.08.008.
15. Daya, S., and Berns, K. I. (2008). Gene therapy using adeno-associated virus vectors. Clin. Microbiol. Rev. 21, 583-593. doi: 10.1128/CMR.00008-08.
16. Devaney, S. A., Palomaki, G. E., Scott, J. A., and Bianchi, D. W. (2011). Noninvasive fetal sex determination using cell-free fetal DNA: a systematic review and meta-analysis. JAMA 306, 627-636. doi: 10.1001/jama.2011.1114.
17. Dong, B., Nakai, H., and Xiao, W. (2010). Characterization of genome integrity for oversized recombinant AAV vector. Mol. Ther. 18, 87-92. doi: 10.1038/mt.2009.258.
18. Duque, S., Joussemet, B., Riviere, C., Marais, T., Dubreil, L., Douar, A. M.,et al. (2009). Intravenous administration of self-complementary AAV9 enables transgene delivery to adult motor neurons. Mol. Ther. 17, 1187-1196. doi: 10.1038/mt.2009.71.
19. Eng, C. M., Schechter, C., Robinowitz, J., Fulop, G., Burgert, T., Levy, B.,et al. (1997). Prenatal genetic carrier testing using triple disease screening. JAMA 278, 1268-1272. doi: 10.1001/jama.1997.03550150072038.
20. Fan, H. C., Blumenfeld, Y. J., Chitkara, U., Hudgins, L., and Quake, S. R. (2008). Noninvasive diagnosis of fetal aneuploidy by shotgun sequencing DNA from maternal blood. Proc. Natl. Acad. Sci. U.S.A. 105, 16266-16271. doi: 10.1073/pnas.0808319105.
21. Foust, K. D., Nurre, E., Montgomery, C. L., Hernandez, A., Chan, C. M., and Kaspar, B. K. (2009). Intravascular AAV9 preferentially targets neonatal neurons and adult astrocytes. Nat. Biotechnol. 27, 59-65. doi: 10.1038/nbt.1515.
22. Foust, K. D., Wang, X., Mcgovern, V. L., Braun, L., Bevan, A. K., Haidet, A. M.,et al. (2010). Rescue of the spinal muscular atrophy phenotype in a mouse model by early postnatal delivery of SMN. Nat. Biotechnol. 28, 271-274. doi: 10.1038/nbt.1610.
23. Fu, H., Dirosario, J., Killedar, S., Zaraspe, K., and Mccarty, D. M. (2011). Correction of neurological disease of mucopolysaccharidosis IIIB in adult mice by rAAV9 trans-blood-brain barrier gene delivery. Mol. Ther. 19, 1025-1033. doi: 10.1038/mt.2011.34.
24. Futch, T., Spinosa, J., Bhatt, S., De Feo, E., Rava, R. P., and Sehnert, A. J. (2013). Initial clinical laboratory experience in noninvasive prenatal testing for fetal aneuploidy from maternal plasma DNA samples. Prenat. Diagn. 33, 569-574. doi: 10.1002/pd.4123.
25. Gaspar, H. B., Parsley, K. L., Howe, S., King, D., Gilmour, K. C., Sinclair, J.,et al. (2004). Gene therapy of X-linked severe combined immunodeficiency by use of a pseudotyped gammaretroviral vector. Lancet 364, 2181-2187. doi: 10.1016/S0140-6736(04)17590-9.
26. Gray, S. J., Matagne, V., Bachaboina, L., Yadav, S., Ojeda, S. R., and Samulski, R. J. (2011). Preclinical differences of intravascular AAV9 delivery to neurons and glia: a comparative study of adult mice and nonhuman primates. Mol. Ther. 19, 1058-1069. doi: 10.1038/mt.2011.72.
27. Gupta, N., Oppenheim, I. M., Kauvar, E. F., Tayebi, N., and Sidransky, E. (2011). Type 2 Gaucher disease: phenotypic variation and genotypic heterogeneity. Blood Cells Mol. Dis. 46, 75-84. doi: 10.1016/j.bcmd.2010.08.012.
28. Howe, S. J., Mansour, M. R., Schwarzwaelder, K., Bartholomae, C., Hubank, M., Kempski, H.,et al. (2008). Insertional mutagenesis combined with acquired somatic mutations causes leukemogenesis following gene therapy of SCID-X1 patients. J. Clin. Invest. 118, 3143-3150. doi: 10.1172/JCI35798.
29. Jeanty, C., Derderian, S. C., and Mackenzie, T. C. (2014). Maternal-fetal cellular trafficking: clinical implications and consequences. Curr. Opin. Pediatr. 26, 377-382. doi: 10.1097/MOP.0000000000000087.
30. Lam, K. W., Jiang, P., Liao, G. J., Chan, K. C., Leung, T. Y., Chiu, R. W.,et al. (2012). Noninvasive prenatal diagnosis of monogenic diseases by targeted massively parallel sequencing of maternal plasma: application to beta-thalassemia. Clin. Chem. 58, 1467-1475. doi: 10.1373/clinchem.2012.189589.
31. Lench, N., Barrett, A., Fielding, S., Mckay, F., Hill, M., Jenkins, L.,et al. (2013). The clinical implementation of non-invasive prenatal diagnosis for single-gene disorders: challenges and progress made. Prenat. Diagn. 33, 555-562. doi: 10.1002/pd.4124.
32. Lo, Y. M., Chan, K. C., Sun, H., Chen, E. Z., Jiang, P., Lun, F. M.,et al. (2010). Maternal plasma DNA sequencing reveals the genome-wide genetic and mutational profile of the fetus. Sci. Transl. Med. 2:61ra91. doi: 10.1126/scitranslmed.3001720.
33. Lo, Y. M., Corbetta, N., Chamberlain, P. F., Rai, V., Sargent, I. L., Redman, C. W.,et al. (1997). Presence of fetal DNA in maternal plasma and serum. Lancet 350, 485-487. doi: 10.1016/S0140-6736(97)02174-0.
34. Mattar, C. N., Waddington, S. N., Biswas, A., Davidoff, A. M., Choolani, M., Chan, J. K.,et al. (2012). The case for intrauterine gene therapy. Best Pract. Res. Clin. Obstet. Gynaecol. 26, 697-709. doi: 10.1016/j.bpobgyn.2012.06.006.
35. Mattar, C. N., Waddington, S. N., Biswas, A., Johana, N., Ng, X. W., Fisk, A. S.,et al. (2013). Systemic delivery of scAAV9 in fetal macaques facilitates neuronal transduction of the central and peripheral nervous systems. Gene Ther. 20, 69-83. doi: 10.1038/gt.2011.216.
36. Merianos, D. J., Tiblad, E., Santore, M. T., Todorow, C. A., Laje, P., Endo, M.,et al. (2009). Maternal alloantibodies induce a postnatal immune response that limits engraftment following in utero hematopoietic cell transplantation in mice. J. Clin. Invest. 119, 2590-2600. doi: 10.1172/JCI38979.
37. Nakai, H., Wu, X., Fuess, S., Storm, T. A., Munroe, D., Montini, E.,et al. (2005). Large-scale molecular characterization of adeno-associated virus vector integration in mouse liver. J. Virol. 79, 3606-3614. doi: 10.1128/JVI.79.6.3606-3614.2005.
38. Nathwani, A. C., Tuddenham, E. G., Rangarajan, S., Rosales, C., McIntosh, J., Linch, D. C.,et al. (2011). Adenovirus-associated virus vector-mediated gene transfer in hemophilia B. N. Engl. J. Med. 365, 2357-2365. doi: 10.1056/NEJMoa1108046.
39. Norton, M. E., Brar, H., Weiss, J., Karimi, A., Laurent, L. C., Caughey, A. B.,et al. (2012). Non-Invasive Chromosomal Evaluation (NICE) Study: results of a multicenter prospective cohort study for detection of fetal trisomy 21 and trisomy 18. Am. J. Obstet. Gynecol. 207, 137.e131-137.e138. doi: 10.1016/j.ajog.2012.05.021.
40. Ortolano, S., Vieitez, I., Navarro, C., and Spuch, C. (2014). Treatment of lysosomal storage diseases: recent patents and future strategies. Recent Pat. Endocr. Metab. Immune Drug Discov. 8, 9-25. doi: 10.2174/1872214808666140115111350.
41. Pastores, G. M., Sibille, A. R., and Grabowski, G. A. (1993). Enzyme therapy in Gaucher disease type 1: dosage efficacy and adverse effects in 33 patients treated for 6 to 24 months. Blood 82, 408-416.
42. Rahim, A. A., Wong, A. M., Buckley, S. M., Chan, J. K., David, A. L., Cooper, J. D.,et al. (2010). In utero gene transfer to the mouse nervous system. Biochem. Soc. Trans. 38, 1489-1493. doi: 10.1042/BST0381489.
43. Rahim, A. A., Wong, A. M., Hoefer, K., Buckley, S. M., Mattar, C. N., Cheng, S. H.,et al. (2011). Intravenous administration of AAV2/9 to the fetal and neonatal mouse leads to differential targeting of CNS cell types and extensive transduction of the nervous system. FASEB J. 25, 3505-3518. doi: 10.1096/fj.11-182311.
44. Roybal, J. L., Endo, M., Buckley, S. M., Herbert, B. R., Waddington, S. N., and Flake, A. W. (2012). Animal models for prenatal gene therapy: rodent models for prenatal gene therapy. Methods Mol. Biol. 891, 201-218. doi: 10.1007/978-1-61779-873-3_10.
45. Rubin, L. L., and Staddon, J. M. (1999). The cell biology of the blood-brain barrier. Annu. Rev. Neurosci. 22, 11-28. doi: 10.1146/annurev.neuro.22.1.11.
46. Samaranch, L., Salegio, E. A., San Sebastian, W., Kells, A. P., Foust, K. D., Bringas, J. R.,et al. (2012). Adeno-associated virus serotype 9 transduction in the central nervous system of nonhuman primates. Hum. Gene Ther. 23, 382-389. doi: 10.1089/hum.2011.200.
47. Spiegel, R., Raas-Rothschild, A., Reish, O., Regev, M., Meiner, V., Bargal, R.,et al. (2009). The clinical spectrum of fetal Niemann-Pick type C. Am. J. Med. Genet. A 149A, 446-450. doi: 10.1002/ajmg.a.32642.
48. Themis, M., Waddington, S. N., Schmidt, M., Von Kalle, C., Wang, Y., Al-Allaf, F.,et al. (2005). Oncogenesis following delivery of a nonprimate lentiviral gene therapy vector to fetal and neonatal mice. Mol. Ther. 12, 763-771. doi: 10.1016/j.ymthe.2005.07.358.
49. Towne, C., Raoul, C., Schneider, B. L., and Aebischer, P. (2008). Systemic AAV6 delivery mediating RNA interference against SOD1: neuromuscular transduction does not alter disease progression in fALS mice. Mol. Ther. 16, 1018-1025. doi: 10.1038/mt.2008.73.
50. Wynn, R. F., Wraith, J. E., Mercer, J., O'Meara, A., Tylee, K., Thornley, M.,et al. (2009). Improved metabolic correction in patients with lysosomal storage disease treated with hematopoietic stem cell transplant compared with enzyme replacement therapy. J. Pediatr. 154, 609-611. doi: 10.1016/j.jpeds.2008.11.005.
51. Yang, B., Li, S., Wang, H., Guo, Y., Gessler, D. J., Cao, C.,et al. (2014). Global CNS transduction of adult mice by intravenously delivered rAAVrh.8 and rAAVrh.10 and nonhuman primates by rAAVrh.10. Mol. Ther. 22, 1299-1309. doi: 10.1038/mt.2014.68.
52. Yla-Herttuala, S. (2012). Endgame: glybera finally recommended for approval as the first gene therapy drug in the European union. Mol. Ther. 20, 1831-1832. doi: 10.1038/mt.2012.194.
53. Zhang, H., Yang, B., Mu, X., Ahmed, S. S., Su, Q., He, R.,et al. (2011). Several rAAV vectors efficiently cross the blood-brain barrier and transduce neurons and astrocytes in the neonatal mouse central nervous system. Mol. Ther. 19, 1440-1448. doi: 10.1038/mt.2011.98.
54. Zincarelli, C., Soltys, S., Rengo, G., and Rabinowitz, J. E. (2008). Analysis of AAV serotypes 1-9 mediated gene expression and tropism in mice after systemic injection. Mol. Ther. 16, 1073-1080. doi: 10.1038/mt.2008.76.