Overnight transduction with foamyviral vectors restores the long-term repopulating activity of Fancc / stem cells

Blood

Volumn 112, Issue 12, 2008, Pages 4458-4465

  Si, Yue ^a   Pulliam, Anna C ^a   Linka, Yvonne ^b   Ciccone, Samantha ^a   Leurs, Cordula ^b   Yuan, Jin ^a   Eckermann, Olaf ^b   Fruehauf, Stefan ^c   Mooney, Sean ^d   Hanenberg, Helmut ^a,b   Clapp, D Wade ^a,e  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b HEINRICH HEINE UNIVERSITY   (Germany)

^c UNIVERSITY OF HEIDELBERG   (Germany)

^d INDIANA UNIVERSITY   (United States)

^e INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; FANCONI ANEMIA GROUP C PROTEIN; FANCONI ANEMIA GROUP D2 PROTEIN; RETROVIRUS VECTOR; STEM CELL FACTOR; FANCC PROTEIN, MOUSE; STEM CELL FACTOR RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL ACTIVITY; CELL POPULATION; CONTROLLED STUDY; FANCONI ANEMIA; GENE EXPRESSION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; RECOMBINANT GENE; STEM CELL; STEM CELL GENE THERAPY; TRANSGENE; VIRAL GENE DELIVERY SYSTEM; VIRAL GENE THERAPY; WILD TYPE; ANIMAL; ANIMAL DISEASE; C57BL MOUSE; CELL CULTURE; CELL PROLIFERATION; CIRCADIAN RHYTHM; EVALUATION; GENE THERAPY; GENE VECTOR; GENETIC TRANSDUCTION; GENETICS; HEMATOPOIETIC STEM CELL; HEMATOPOIETIC STEM CELL TRANSPLANTATION; METABOLISM; METHODOLOGY; MOUSE MUTANT; PATHOLOGY; PHYSIOLOGY; SPUMA VIRUS; TIME;

ANIMALS; CELL PROLIFERATION; CELLS, CULTURED; CIRCADIAN RHYTHM; FANCONI ANEMIA; FANCONI ANEMIA COMPLEMENTATION GROUP C PROTEIN; GENE THERAPY; GENETIC VECTORS; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HEMATOPOIETIC STEM CELLS; HUMANS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PROTO-ONCOGENE PROTEINS C-KIT; SPUMAVIRUS; TIME FACTORS; TRANSDUCTION, GENETIC;

EID: 58149390274     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2007-07-102947     Document Type: Article

References (76)

1. Auerbach AD, Buchwald M, Joenje H. Fanconi anemia. In: Vogelstein B, Kinzler KW, eds. The Genetic Bases of Human Cancer. 2nd ed. New York, NY: McGraw-Hill; 2002:289-306.
2. Bagby GC, Alter BP. Fanconi anemia. Semin Hematol. 2006;43:147-156.
3. Kennedy RD, D'Andrea AD. DNA repair pathways in clinical practice: lessons from pediatric cancer susceptibility syndromes. J Clin Oncol. 2006;5:952-961.
4. Kutler DI, Singh B, Satagopan J, et al. A 20-year perspective on the International Fanconi Anemia Registry (IFAR). Blood. 2003;101:1249-1256.
5. Mathew CG. Fanconi anaemia genes and susceptibility to cancer. Oncogene. 2006;25:5875-5884.
6. Levitus M, Joenje H, de Winter JP. The Fanconi anemia pathway of genomic maintenance. Cell Oncol. 2006;28:3-29.
7. Mirchandani KD, D'Andrea AD. The Fanconi anemia/BRCA pathway: a coordinator of cross-link repair. Exp Cell Res. 2006;312:2647-2653.
8. Niedernhofer LJ, Lalai AS, Hoeijmakers JH. Fan-coni anemia (cross)linked to dna repair. Cell. 2005;123:1191-1198.
9. Taniguchi T, D'Andrea AD. The molecular pathogenesis of Fanconi anemia: recent progress. Blood. 2006;107:4223-4233.
10. Dorsman JC, Levitus M, Rockx D, et al. Identification of the Fanconi anemia complementation group I gene, FANCI. Cell Oncol. 2007;29:211-218.
11. Reid S, Schindler D, Hanenberg H, et al. Biallelic mutations in PALB2 cause Fanconi anemia subtype FA-N and predispose to childhood cancer. Nat Genet. 2007;39:162-164.
12. Sims AE, Spiteri E, Sims RJ 3rd, et al. FANCI is a second monoubiquitinated member of the Fanconi anemia pathway. Nat Struct Mol Biol. 2007; 14:564-567.
13. Smogorzewska A, Matsuoka S, Vinciguerra P, et al. Identification of the FANCI protein, a monoubiquitinated FANCD2 paralog required for DNA repair. Cell. 2007;129:289-301.
14. Xia B, Dorsman JC, Ameziane N, et al. Fanconi anemia is associated with a defect in the BRCA2 partner PALB2. Nat Genet. 2007;39:159-161.
15. Gregory JJ, Wagner JE, Verlander PC, et al. Somatic mosaicism in Fanconi anemia: evidence of genotypic reversion in lymphohematopoietic stem cells. Proc Natl Acad Sci U S A. 2001;98:2532-2537.
16. Gross M, Hanenberg H, Lobitz S, et al. Reverse mosaicism in Fanconi anemia: natural gene therapy via molecular self-correction. Cytogenet Genome Res. 2002;98:126-135.
17. Mankad A, Taniguchi T, Cox B, et al. Natural gene therapy in monozygotic twins with Fanconi anemia. Blood. 2006;107:3084-3090.
18. Soulier J, Leblanc T, Larghero J, et al. Detection of somatic mosaicism and classification of Fanconi anemia patients by analysis of the FA/BRCA pathway. Blood. 2005;105:1329-1336.
19. Waisfisz Q, Morgan NV, Savino M, et al. Spontaneous functional correction of homozygous fanconi anaemia alleles reveals novel mechanistic basis for reverse mosaicism. Nat Genet. 1999;22: 379-383.
20. Galimi F, Noll M, Kanazawa Y, et al. Genetherapy of Fanconi anemia: preclinical efficacy using lenti-viral vectors. Blood. 2002;100:2732-2736.
21. Gush KA, Fu KL, Grompe M, Walsh CE. Phenotypic correction of Fanconi anemia group C knockout mice. Blood. 2000;95:700-704.
22. Haneline LS, Li X, Ciccone SL, et al. Retroviral-mediated expression of recombinant Fancc enhances the repopulating ability of Fancc-/- hematopoietic stem cells and decreases the risk of clonal evolution. Blood. 2003;101:1299-1307.
23. Kelly PF, Radtke S, Kalle C, et al. Stem cell collection and gene transfer in fanconi anemia. Mol Ther. 2007;15:211-219.
24. Liu JM, Young NS, Walsh CE, et al. Retroviral mediated gene transfer of the Fanconi anemia complementation group C gene to hematopoietic progenitors of group C patients. Hum Gene Ther. 1997;8:1715-1730.
25. Roe T, Reynolds TC, Yu G, Brown PO. Integration of murine leukemia virus DNAdepends on mitosis. EMBO J. 1993;12:2099-2108.
26. Trobridge G, Russell DW. Cell cycle requirements for transduction by foamy virus vectors compared to those of oncovirus and lentivirus vectors. J Virol. 2004;78:2327-2335.
27. Hanenberg H, Hashino K, Konishi H, Hock RA, Kato I, Williams DA. Optimization of fibronectin-assisted retroviral gene transfer into human CD34+ hematopoietic cells. Hum Gene Ther. 1997;8:2193-2206.
28. Hanenberg H, Xiao XL, Dilloo D, Hashino K, Kato I, Williams DA. Colocalization of retrovirus and target cells on specific fibronectin fragments increases genetic transduction of mammalian cells. Nat Med. 1996;2:876-882.
29. Cavazzana-Calvo M, Lagresle C, Hacein-Bey-Abina S, Fischer A. Gene therapy for severe combined immunodeficiency. Annu Rev Med. 2005; 56:585-602.
30. Macchiarini F, Manz MG, Palucka AK, Shultz LD. Humanized mice: are we there yet? J Exp Med. 2005;202:1307-1311.
31. Trobridge G, Beard BC, Kiem HP. Hematopoietic stem cell transduction and amplification in large animal models. Hum Gene Ther. 2005;16:1355-1366.
32. Haneline LS, Gobbett TA, Ramani R, et al. Loss of FancC function results in decreased hematopoietic stem cell repopulating ability. Blood. 1999;94:1-8.
33. Li X, Le Beau MM, Ciccone S, et al. Ex vivo culture of Fancc-/- stem/progenitor cells predisposes cells to undergo apoptosis, and surviving stem/ progenitor cells display cytogenetic abnormalities and an increased risk of malignancy. Blood. 2005; 105:3465-3471.
34. Linial M. Foamy viruses. In: Knipe DM, Howley PM, eds. Fields Virology. Vol 2. 5th ed 5th. Philadelphia, PA: Lippincott Williams & Wilkins; 2007: 2245-2262.
35. Meiering CD, Linial ML. Historical perspective of foamy virus epidemiology and infection. Clin Microbiol Rev. 2001;14:165-176.
36. Rethwilm A. Foamy viruses. In: Mahy B, ter Meulen V, eds. Topley & Wilson's Microbiology & Microbiotic Infections. 10th ed. London, United Kingdom: Arnold; 2005:1304-1321.
37. Vassilopoulos G, Trobridge G, Josephson NC, Russell DW. Gene transfer into murine hematopoietic stem cells with helper-free foamy virus vectors. Blood. 2001;98:604-609.
38. Kiem HP, Allen J, Trobridge G, et al. Foamy virus-mediated gene transfer to canine repopulating cells. Blood. 2007;109:65-70.
39. Josephson NC, Vassilopoulos G, Trobridge GD, et al. Transduction of human NOD/SCID-repopu-lating cells with both lymphoid and myeloid potential by foamy virus vectors. Proc Natl Acad Sci USA. 2002;99:8295-8300.
40. Leurs C, Jansen M, Pollok KE, et al. Comparison of three retroviral vector systems for transduction of nonobese diabetic/severe combined immunodeficiency mice repopulating human CD34(+) cord blood cells. Hum Gene Ther. 2003;14:509-519.
41. Zucali JR, Ciccarone T, Kelley V, Park J, Johnson CM, Mergia A. Transduction of umbilical cord blood CD34+ NOD/SCID-repopulating cells by simian foamy virus type 1 (SFV-1) vector. Virology. 2002;302:229-235.
42. Heinkelein M, Dressler M, Jarmy G, et al. Improved primate foamy virus vectors and packaging constructs. J Virol. 2002;76:3774-3783.
43. Haneline LS, Broxmeyer HE, Cooper S, et al. Multiple inhibitory cytokines induce deregulated progenitor growth and apoptosis in hematopoietic cells from Fac-/- mice. Blood. 1998;91:4092-4098.
44. Koh PS, Hughes GC, Faulkner GR, Keeble WW, Bagby GC. The Fanconi anemia group C gene product modulates apoptotic responses to tumor necrosis factor-alpha and Fas ligand but does not suppress expression of receptors of the tumor necrosis factor receptor superfamily. Exp Hematol. 1999;27:1-8.
45. Laufs S, Gentner B, Nagy KZ, et al. Retroviral vector integration occurs in preferred genomic targets of human bone marrow-repopulating cells. Blood. 2003;101:2191-2198.
46. Cai S, Ernstberger A, Wang H, et al. In vivo selection of hematopoietic stem cells transduced at a low multiplicity-of-infection with a foamy viral MGMT(P140K) vector. Exp Hematol. 2008;36:283-292.
47. Wellcome Trust Sanger. Ensembl. http://www.ensembl.org. Accessed August 29, 2005.
48. University of California Santa Cruz. UCSC Genome Browser. http://genome.ucsc.edu. Accessed August 29, 2005.
49. Garcia-Higuera I, Taniguchi T, Ganesan S, et al. Interaction of the Fanconi anemia proteins and BRCA1 in a common pathway. Mol Cell. 2001;7: 249-262.
50. Taniguchi T, Garcia-Higuera I, Andreassen PR, Gregory RC, Grompe M, D'Andrea AD. S-phase-specific interaction of the Fanconi anemia protein, FANCD2, with BRCA1 and RAD51. Blood. 2002; 100:2414-2420.
51. Broxmeyer HE, Orschell CM, Clapp DW, et al. Rapid mobilization of murine and human hematopoietic stem and progenitor cells with AMD3100, aCXCR4 antagonist. J Exp Med. 2005;201:1307-1318.
52. Christopherson KW2nd, Hangoc G, Mantel CR, Broxmeyer HE. Modulation of hematopoietic stem cell homing and engraftment by CD26. Science. 2004;305:1000-1003.
53. Harrison DE. Competitive repopulation: anew assay for long-term stem cell functional capacity. Blood. 1980;55:77-81.
54. Uchida N, Aguila HL, Fleming WH, Jerabek L, Weissman IL. Rapid and sustained hematopoietic recovery in lethally irradiated mice transplanted with purified Thy-1.1lo Lin-Sca-1 + hematopoietic stem cells. Blood. 1994;83:3758-3779.
55. Yoder MC, Hiatt K, Dutt P, Mukherjee P, Bodine DM, Orlic D. Characterization of definitive lymphohematopoietic stem cells in the day 9 murine yolk sac. Immunity. 1997;7:335-344.
56. Zhang F, Thornhill SI, Howe SJ, et al. Lentiviral vectors containing an enhancer-less ubiquitously acting chromatin opening element (UCOE) provide highly reproducible and stable transgene expression in hematopoietic cells. Blood. 2007; 110:1448-1457.
57. Bauer TR, Jr., Allen JM, Hai M, et al. Successful treatment of canine leukocyte adhesion deficiency by foamy virus vectors. Nat Med. 2008;14: 93-97.
58. Nowrouzi A, Dittrich M, Klanke C, et al. Genomewide mapping of foamy virus vector integrations into a human cell line. J Gen Virol. 2006;87:1339-1347.
59. Schmidt M, Glimm H, Wissler M, et al. Efficient characterization of retro-, lenti-, and foamyvector-transduced cell populations by high-accuracy insertion site sequencing. Ann N YAcad Sci. 2003; 996:112-121.
60. Trobridge GD, Miller DG, Jacobs MA, et al. Foamy virus vector integration sites in normal human cells. Proc Natl Acad Sci U SA. 2006;103: 1498-1503.
61. Davies SM, Khan S, Wagner JE, et al. Unrelated donor bone marrow transplantation for Fanconi anemia. Bone Marrow Transplant. 1996;17:43-47.
62. Gluckman E, Broxmeyer HE, Auerbach AD, et al. Hematopoietic reconstitution in a patient with Fanconi's anemia by means of umbilical-cord blood from an HLA-identical sibling. N Engl J Med. 1989;321:1174-1178.
63. Guardiola P, Pasquini R, Dokal I, et al. Outcome of 69 allogeneic stem cell transplantations for Fanconi anemia using HLA-matched unrelated donors: a study on behalf of the European Group for Blood and Marrow Transplantation. Blood. 2000;95:422-429.
64. Wagner JE, Eapen M, MacMillan ML, et al. Unrelated donor bone marrow transplantation for the treatment of Fanconi anemia. Blood. 2007;109: 2256-2262.
65. Kutler DI, Auerbach AD, Satagopan J, et al. High incidence of head and neck squamous cell carcinoma in patients with Fanconi anemia. Arch Otolaryngol Head Neck Surg. 2003;129:106-112.
66. Rosenberg PS, Socie G, Alter BP, Gluckman E. Risk of head and neck squamous cell cancer and death in patients with Fanconi anemia who did and did not receive transplants. Blood. 2005;105:67-73.
67. Si Y, Ciccone S, Yang FC, et al. Continuous in vivo infusion of interferon-gamma (IFN-{gamma}) enhances engraftment of syngeneic wild-type cells in Fanca-/- and Fancg-/- mice. Blood. 2006; 108:4283-4287.
68. Williams DA, Croop J, Kelly P. Gene therapy in the treatment of Fanconi anemia, a progressive bone marrow failure syndrome. Curr Opin Mol Ther. 2005;7:461-466.
69. Switzer WM, Bhullar V, Shanmugam V, et al. Frequent simian foamy virus infection in persons occupationally exposed to nonhuman primates. J Virol. 2004;78:2780-2789.
70. Andreadis ST, Brott D, Fuller AO, Palsson BO. Moloney murine leukemia virus-derived retroviral vectors decay intracellularly with a half-life in the range of 4-6 hours. J Virol. 1997;71:7541-7548.
71. Lehmann-Che J, Renault N, Giron ML, et al. Centrosomal latency of incoming foamy viruses in resting cells. PLoS Pathog. (http://www.pubmedcentral. nih.gov/articlerender.fcgi?artid1871606) 2007;3:e74.
72. Si Y. Use of a Human Foamy Viral Construct Encoding Recombinant FANCC to Correct the Hematopoietic Stem Cell Defect and Prevent the Development of Myeloid Malignancies in Fancc-/-Mice. Microbiology and Immunology. Vol. PhD. Indianapolis, IN: Indiana University School of Medicine; 2005:113.
73. Jordan CT, Lemischka IR. Clonal and systemic analysis of long-term hematopoiesis in the mouse. Genes Dev. 1990;4:220-232.
74. Jordan CT, McKearn JP, Lemischka IR. Cellular and developmental properties of fetal hematopoietic stem cells. Cell. 1990;61:953-963.
75. Duda A, Luftenegger D, Pietschmann T, Lindemann D. Characterization of the prototype foamy virus envelope glycoprotein receptor-binding domain. J Virol. 2006;80:8158-8167.
76. Stanke N, Stange A, Luftenegger D, Zentgraf H, Lindemann D. Ubiquitination of the prototype foamy virus envelope glycoprotein leader peptide regulates subviral particle release. J Virol. 2005; 79:15074-15083.