Lentiviral hematopoietic stem cell gene therapy benefits metachromatic leukodystrophy

Science

Volumn 341, Issue 6148, 2013, Pages

  Biffi, Alessandra ^a,b   Montini, Eugenio ^a   Lorioli, Laura ^a,b,c   Cesani, Martina ^a   Fumagalli, Francesca ^b,c   Plati, Tiziana ^a   Baldoli, Cristina ^b   Martino, Sabata ^d   Calabria, Andrea ^a   Canale, Sabrina ^b   Benedicenti, Fabrizio ^a   Vallanti, Giuliana ^e   Biasco, Luca ^a   Leo, Simone ^f   Kabbara, Nabil ^g   Zanetti, Gianluigi ^f   Rizzo, William B ^h   Mehta, Nalini A L ⁱ   Cicalese, Maria Pia ^b   Casiraghi, Miriam ^b   Boelens, Jaap J ^j   Del Carro, Ubaldo ^b   Dow, David J ⁱ   Schmidt, Manfred ^k   Assanelli, Andrea ^b   Neduva, Victor ⁱ   Di Serio, Clelia ^c   Stupka, Elia ^b   Gardner, Jason ^l   Von Kalle, Christof ^k   Bordignon, Claudio ^c,e   Ciceri, Fabio ^b   Rovelli, Attilio ^m   Roncarolo, Maria Grazia ^a,b,c   Aiuti, Alessandro ^a,b,n   Sessa, Maria ^b   Naldini, Luigi ^a,c   more..

^a SAN RAFFAELE SCIENTIFIC INSTITUTE   (Italy)

^b SAN RAFFAELE HOSPITAL   (Italy)

^c VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

^d UNIVERSITY OF PERUGIA   (Italy)

^e MOLMED S P A   (Italy)

^f CENTER FOR ADVANCED STUDIES   (Italy)

^g RAFIC HARIRI UNIVERSITY HOSPITAL   (Lebanon)

^h UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

ⁱ GLAXOSMITHKLINE   (United Kingdom)

^j UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^k GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^l GLAXOSMITHKLINE   (United States)

^m SAN GERARDO HOSPITAL   (Italy)

ⁿ UNIVERSITY OF ROME TOR VERGATA   (Italy)

more..

Author keywords

[No Author keywords available]

Indexed keywords

BUSULFAN; CEREBROSIDE SULFATASE; LENTIVIRUS VECTOR;

CLONAL GROWTH; DISEASE; DISEASE VECTOR; GENE; GENETIC ENGINEERING; STEM; SYMPTOM;

ARTICLE; CASE REPORT; CELL CULTURE; CEREBROSPINAL FLUID ANALYSIS; CHILD; ENZYME DEFICIENCY; EX VIVO STUDY; FOLLOW UP; GENE ACTIVITY; GENE EXPRESSION; GENE THERAPY; GENETIC VARIABILITY; GENOTOXICITY; HEMATOPOIETIC STEM CELL; HUMAN; LIQUID; METACHROMATIC LEUKODYSTROPHY; PERIPHERAL BLOOD STEM CELL; PHASE 2 CLINICAL TRIAL; PHASE 3 CLINICAL TRIAL; PRIORITY JOURNAL; TREATMENT OUTCOME; BRAIN; CLINICAL TRIAL; DNA DAMAGE; GENE VECTOR; GENETIC ENGINEERING; GENETIC TRANSDUCTION; GENETICS; HEMATOPOIETIC STEM CELL TRANSPLANTATION; LENTIVIRINAE; METABOLISM; METHODOLOGY; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOLOGY; VIRUS DNA CELL DNA INTERACTION;

BRAIN; CEREBROSIDE-SULFATASE; DNA DAMAGE; FOLLOW-UP STUDIES; GENETIC ENGINEERING; GENETIC THERAPY; GENETIC VECTORS; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HEMATOPOIETIC STEM CELLS; HUMANS; LENTIVIRUS; LEUKODYSTROPHY, METACHROMATIC; MAGNETIC RESONANCE IMAGING; TRANSDUCTION, GENETIC; TREATMENT OUTCOME; VIRUS INTEGRATION;

EID: 84879873039     PISSN: 00368075     EISSN: 10959203     Source Type: Journal    
DOI: 10.1126/science.1233158     Document Type: Article

References (47)

1. J. Aicardi, Diseases of the Nervous System in Childhood (Mac Keith Press, London, ed. 2, 1998).
2. A. Biffi, G. Lucchini, A. Rovelli, M. Sessa, Metachromatic leukodystrophy: An overview of current and prospective treatments. Bone Marrow Transplant. 42, S2-S6 (2008). doi: 10.1038/bmt.2008.275; pmid: 18978739
3. A. Biffi, P. Aubourg, N. Cartier, Gene therapy for leukodystrophies. Hum. Mol. Genet. 20, R42-R53 (2011). doi: 10.1093/hmg/ddr142; pmid: 21459776
4. W. Krivit, J. H. Sung, E. G. Shapiro, L. A. Lockman, Microglia: The effector cell for reconstitution of the central nervous system following bone marrow transplantation for lysosomal and peroxisomal storage diseases. Cell Transplant. 4, 385-392 (1995). doi: 10.1016/0963-6897(95)00021-O; pmid: 7582569
5. A. M. Rovelli, C. G. Steward, Hematopoietic cell transplantation activity in Europe for inherited metabolic diseases: Open issues and future directions. Bone Marrow Transplant. 35, S23 (2005). doi: 10.1038/sj.bmt.1704839
6. J. J. Boelens, V. K. Prasad, J. Tolar, R. F. Wynn, C. Peters, Current international perspectives on hematopoietic stem cell transplantation for inherited metabolic disorders. Pediatr. Clin. North Am. 57, 123-145 (2010). doi: 10.1016/j.pcl.2009.11.004; pmid: 20307715
7. J. J. Boelens, Trends in haematopoietic cell transplantation for inborn errors of metabolism. J. Inherit. Metab. Dis. 29, 413-420 (2006). doi: 10.1007/s10545-005-0258-8; pmid: 16763911
8. A. Biffi et al., Correction of metachromatic leukodystrophy in the mouse model by transplantation of genetically modified hematopoietic stem cells. J. Clin. Invest. 113, 1118-1129 (2004). pmid: 15085191
9. A. Biffi et al., Gene therapy of metachromatic leukodystrophy reverses neurological damage and deficits in mice. J. Clin. Invest. 116, 3070-3082 (2006). doi: 10.1172/JCI28873; pmid: 17080200
10. I. Visigalli et al., Gene therapy augments the efficacy of hematopoietic cell transplantation and fully corrects mucopolysaccharidosis type I phenotype in the mouse model. Blood 116, 5130-5139 (2010). doi: 10.1182/blood-2010-04- 278234; pmid: 20847202
11. B. Gentner et al., Identification of hematopoietic stem cell-specific miRNAs enables gene therapy of globoid cell leukodystrophy. Sci. Transl. Med. 2, 58ra84 (2010). doi: 10.1126/scitranslmed.3001522; pmid: 21084719
12. A. Aiuti et al., Gene therapy for immunodeficiency due to adenosine deaminase deficiency. N. Engl. J. Med. 360, 447-458 (2009). doi: 10.1056/NEJMoa0805817; pmid: 19179314
13. M. Cavazzana-Calvo, A. Fischer, Gene therapy for severe combined immunodeficiency: Are we there yet? J. Clin. Invest. 117, 1456-1465 (2007). doi: 10.1172/JCI30953; pmid: 17549248
14. M. G. Ott et al., Correction of X-linked chronic granulomatous disease by gene therapy, augmented by insertional activation of MDS1-EVI1, PRDM16 or SETBP1. Nat. Med. 12, 401-409 (2006). doi: 10.1038/nm1393; pmid: 16582916
15. L. Naldini, Ex vivo gene transfer and correction for cell-based therapies. Nat. Rev. Genet. 12, 301-315 (2011). doi: 10.1038/nrg2985; pmid: 21445084
16. L. Naldini et al., In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science 272, 263-267 (1996). doi: 10.1126/science.272.5259.263; pmid: 8602510
17. N. Cartier et al., Hematopoietic stem cell gene therapy with a lentiviral vector in X-linked adrenoleukodystrophy. Science 326, 818-823 (2009). doi: 10.1126/science.1171242; pmid: 19892975
18. S. Hacein-Bey-Abina et al., Insertional oncogenesis in 4 patients after retrovirus-mediated gene therapy of SCID-X1. J. Clin. Invest. 118, 3132-3142 (2008). doi: 10.1172/JCI35700; pmid: 18688285
19. E. Montini et al., Hematopoietic stem cell gene transfer in a tumor-prone mouse model uncovers low genotoxicity of lentiviral vector integration. Nat. Biotechnol. 24, 687-696 (2006). doi: 10.1038/nbt1216; pmid: 16732270
20. E. Montini et al., The genotoxic potential of retroviral vectors is strongly modulated by vector design and integration site selection in a mouse model of HSC gene therapy. J. Clin. Invest. 119, 964-975 (2009). doi: 10.1172/JCI37630; pmid: 19307726
21. A. Capotondo et al., Safety of arylsulfatase A overexpression for gene therapy of metachromatic leukodystrophy. Hum. Gene Ther. 18, 821-836 (2007). doi: 10.1089/hum.2007.048; pmid: 17845130
22. + cells transduced with lentiviral vector for the treatment of Wiskott-Aldrich syndrome. Mol. Ther. 21, 175-184 (2013). doi: 10.1038/mt.2012.23; pmid: 22371846
23. R. L. Koul et al., Late infantile metachromatic leucodystrophy in two siblings. Indian Pediatr. 31, 694-698 (1994).pmid: 7896397
24. S. Yatziv, A. Russell, An unusual form of metachromatic leukodystrophy in three siblings. Clin. Genet. 19, 222-227 (1981). doi: 10.1111/j.1399-0004.1981. tb00702.x; pmid: 6115727
25. T. Satoh et al., Metachromatic leukodystrophy. Report of siblings with the juvenile type of metachromatic leukodystrophy. Acta Pathol. Jpn. 38, 1041-1051 (1988). pmid: 3188912
26. A. Biffi et al., Metachromatic leukodystrophy-mutation analysis provides further evidence of genotype-phenotype correlation. Clin. Genet. 74, 349-357 (2008). doi: 10.1111/j.1399-0004.2008.01058.x; pmid: 18786133
27. C. Kehrer, G. Blumenstock, C. Raabe, I. Krägeloh-Mann, Development and reliability of a classification system for gross motor function in children with metachromatic leucodystrophy. Dev. Med. Child Neurol. 53, 156-160 (2011). doi: 10.1111/j.1469-8749.2010.03821.x; pmid: 21087233
28. S. Groeschel et al., Metachromatic leukodystrophy: Natural course of cerebral MRI changes in relation to clinical course. J. Inherit. Metab. Dis. 34, 1095-1102 (2011). doi: 10.1007/s10545-011-9361-1; pmid: 21698385
29. A. Biffi et al., Lentiviral vector common integration sites in preclinical models and a clinical trial reflect a benign integration bias and not oncogenic selection. Blood 117, 5332-5339 (2011). doi: 10.1182/blood-2010- 09-306761; pmid: 21403130
30. U. Abel et al., Real-time definition of non-randomness in the distribution of genomic events. PLoS ONE 2, e570 (2007). doi: 10.1371/journal.pone.0000570; pmid: 17593969
31. G. P. Wang et al., Dynamics of gene-modified progenitor cells analyzed by tracking retroviral integration sites in a human SCID-X1 gene therapy trial. Blood 115, 4356-4366 (2010). doi: 10.1182/blood-2009-12-257352; pmid: 20228274
32. F. Ginhoux et al., Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science 330, 841-845 (2010). doi: 10.1126/science.1194637; pmid: 20966214
33. J. Priller et al., Targeting gene-modified hematopoietic cells to the central nervous system: Use of green fluorescent protein uncovers microglial engraftment. Nat. Med. 7, 1356-1361 (2001). doi: 10.1038/nm1201-1356; pmid: 11726978
34. A. Capotondo et al., Brain conditioning is instrumental for successful microglia reconstitution following hematopoietic stem cell transplantation. Proc. Natl. Acad. Sci. U.S.A. 109, 15018-15023 (2012). doi: 10.1073/pnas. 1205858109; pmid: 22923692
35. K. Araya et al., Localized donor cells in brain of a Hunter disease patient after cord blood stem cell transplantation. Mol. Genet. Metab. 98, 255-263 (2009). doi: 10.1016/j.ymgme.2009.05.006; pmid: 19556155
36. K. Allers et al., Evidence for the cure of HIV infection by CCR5Δ32/Δ32 stem cell transplantation. Blood 117, 2791-2799 (2011). doi: 10.1182/blood-2010-09-309591; pmid: 21148083
37. S. J. Howe et al., Insertional mutagenesis combined with acquired somatic mutations causes leukemogenesis following gene therapy of SCID-X1 patients. J. Clin. Invest. 118, 3143-3150 (2008). doi: 10.1172/JCI35798; pmid: 18688286
38. S. Hacein-Bey-Abina et al., A serious adverse event after successful gene therapy for X-linked severe combined immunodeficiency. N. Engl. J. Med. 348, 255-256 (2003). doi: 10.1056/NEJM200301163480314; pmid: 12529469
39. S. Hacein-Bey-Abina et al., LMO2-associated clonal T cell proliferation in two patients after gene therapy for SCID-X1. Science 302, 415-419 (2003). doi: 10.1126/science.1088547; pmid: 14564000
40. S. Stein et al., Genomic instability and myelodysplasia with monosomy 7 consequent to EVI1 activation after gene therapy for chronic granulomatous disease. Nat. Med. 16, 198-204 (2010). doi: 10.1038/nm.2088; pmid: 20098431
41. D. Zychlinski et al., Physiological promoters reduce the genotoxic risk of integrating gene vectors. Mol. Ther. 16, 718-725 (2008). doi: 10.1038/mt.2008.5; pmid: 18334985
42. D. J. Russell et al., The gross motor function measure: A means to evaluate the effects of physical therapy. Dev. Med. Child Neurol. 31, 341-352 (1989). doi: 10.1111/j.1469-8749.1989.tb04003.x; pmid: 2753238
43. R. G. Voigt et al., Concurrent and predictive validity of the cognitive adaptive test/clinical linguistic and auditory milestone scale (CAT/CLAMS) and the Mental Developmental Index of the Bayley Scales of Infant Development. Clin. Pediatr. (Phila.) 42, 427-432 (2003). doi: 10.1177/000992280304200507; pmid: 12862346
44. C. Mattioli et al., Sedation for children with metachromatic leukodystrophy undergoing MRI. Paediatr. Anaesth. 17, 64-69 (2007). doi: 10.1111/j.1460-9592.2006.02002.x; pmid: 17184435
45. S. Martino et al., Expression and purification of a human, soluble Arylsulfatase A for Metachromatic Leukodystrophy enzyme replacement therapy. J. Biotechnol. 117, 243-251 (2005). doi: 10.1016/j.jbiotec.2005.01.018; pmid: 15862354
46. G. V. Childs, In situ hybridization with nonradioactive probes. Methods Mol. Biol. 123, 131-141 (2000). pmid: 10547766
47. A. Aiuti et al., Science 341, 1233151 (2013). doi: 341,1233151