Reconstitution of the myeloid and lymphoid compartments after the transplantation of autologous and genetically modified CD34+ bone marrow cells, following gamma irradiation in cynomolgus macaques

Retrovirology

Volumn 5, Issue , 2008, Pages

  Derdouch, Sonia ^a,b   Gay, Wilfried ^a,b   Nègre, Didier ^c,d,e   Prost, Stéphane ^a,b   Le Dantec, Mikael ^a,b   Delache, Benoît ^a,b   Auregan, Gwenaelle ^a,b   Andrieu, Thibault ^a,b   Leplat, Jean Jacques ^f,g   Cosset, François Loïc ^c,d,e   Le Grand, Roger ^a,b  

^a INSTITUT DE RADIOPROTECTION ET DE SÛRETÉ NUCLÉAIRE   (France)

^b UNIVERSITÉ PARIS SACLAY   (France)

^c UNIVERSITÉ DE LYON   (France)

^d INSERM   (France)

^e UNIVERSITÉ DE LYON   (France)

^f DIF   (France)

^g CEMAGREF   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CD34 ANTIGEN; ENHANCED GREEN FLUORESCENT PROTEIN; LENTIVIRUS VECTOR; PHOSPHOGLYCERATE KINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; AUTOLOGOUS BONE MARROW TRANSPLANTATION; BONE MARROW CELL; CELL COMPARTMENTALIZATION; CELL CULTURE; CELL DIFFERENTIATION; CELL PROLIFERATION; COLONY FORMING CELL; CONTROLLED STUDY; ERYTHROCYTE; EX VIVO GENE TRANSFER; GAMMA IRRADIATION; GRANULOCYTE; HEMATOPOIETIC CELL; MACACA; MALE; MONONUCLEAR CELL; NONHUMAN; SIMIAN IMMUNODEFICIENCY VIRUS; T LYMPHOCYTE; THROMBOCYTE; VIRAL GENE DELIVERY SYSTEM; ANIMAL; AUTOTRANSPLANTATION; BONE MARROW TRANSPLANTATION; CYTOLOGY; GAMMA RADIATION; GENETICS; HEMATOPOIETIC STEM CELL; LYMPHOCYTE; METABOLISM; RADIATION EXPOSURE;

LENTIVIRUS; MACACA; SIMIAE; VESICULAR STOMATITIS VIRUS;

ANIMALS; ANTIGENS, CD34; BONE MARROW CELLS; BONE MARROW TRANSPLANTATION; CELL DIFFERENTIATION; GAMMA RAYS; HEMATOPOIETIC STEM CELLS; LYMPHOCYTES; MACACA; MACACA FASCICULARIS; MYELOID CELLS; TRANSPLANTATION, AUTOLOGOUS;

EID: 47949086568     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/1742-4690-5-50     Document Type: Article

References (74)

1. Miller DG Adam MA Miller AD Gene transfer by retrovirus vectors occurs only in cells that are actively replicating at the time of infection Mol Cell Biol 1990, 10:4239-4242. 360961 2370865
2. Jones RJ Wagner JE Celano P Zicha MS Sharkis SJ Separation of pluripotent haematopoietic stem cells from spleen colony-forming cells Nature 1990, 347:188-189. 10.1038/347188a0 2395470
3. Gothot A Loo van der JC Clapp DW Srour EF Cell cycle-related changes in repopulating capacity of human mobilized peripheral blood CD34(+) cells in non-obese diabetic/severe combined immune-deficient mice Blood 1998, 92:2641-2649. 9763545
4. Hao QL Thiemann FT Petersen D Smogorzewska EM Crooks GM Extended long-term culture reveals a highly quiescent and primitive human hematopoietic progenitor population Blood 1996, 88:3306-3313. 8896394
5. Ploemacher RE Sluijs van der JP Voerman JS Brons NH An in vitro limiting-dilution assay of long-term repopulating hematopoietic stem cells in the mouse Blood 1989, 74:2755-2763. 2819245
6. Ploemacher RE Sluijs van der JP van Beurden CA Baert MR Chan PL Use of limiting-dilution type long-term marrow cultures in frequency analysis of marrow-repopulating and spleen colony-forming hematopoietic stem cells in the mouse Blood 1991, 78:2527-2533. 1824250
7. Traycoff CM Kosak ST Grigsby S Srour EF Evaluation of ex vivo expansion potential of cord blood and bone marrow hematopoietic progenitor cells using cell tracking and limiting dilution analysis Blood 1995, 85:2059-2068. 7536490
8. Bodine DM Crosier PS Clark SC Effects of hematopoietic growth factors on the survival of primitive stem cells in liquid suspension culture Blood 1991, 78:914-920. 1714328
9. Larochelle A Vormoor J Hanenberg H Wang JC Bhatia M Lapidot T Moritz T Murdoch B Xiao XL Kato I et al. Identification of primitive human hematopoietic cells capable of repopulating NOD/SCID mouse bone marrow: implications for gene therapy Nat Med 1996, 2:1329-1337. 10.1038/ nm1296-1329 8946831
10. Peters SO Kittler EL Ramshaw HS Quesenberry PJ Ex vivo expansion of murine marrow cells with interleukin-3 (IL-3), IL-6, IL-11, and stem cell factor leads to impaired engraftment in irradiated hosts Blood 1996, 87:30-37. 8547656
11. Tisdale JF Hanazono Y Sellers SE Agricola BA Metzger ME Donahue RE Dunbar CE Ex vivo expansion of genetically marked rhesus peripheral blood progenitor cells results in diminished long-term repopulating ability Blood 1998, 92:1131-1141. 9694700
12. Lewis PF Emerman M Passage through mitosis is required for oncoretroviruses but not for the human immunodeficiency virus J Virol 1994, 68:510-516. 236313 8254763
13. Naldini L Lentiviruses as gene transfer agents for delivery to non-dividing cells Curr Opin Biotechnol 1998, 9:457-463. 10.1016/ S0958-1669(98)80029-3 9821272
14. Fouchier RA Malim MH Nuclear import of human immunodeficiency virus type-1 preintegration complexes Adv Virus Res 1999, 52:275-299. 10384238
15. Naldini L Blomer U Gallay P Ory D Mulligan R Gage FH Verma IM Trono D In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector Science 1996, 272:263-267. 10.1126/ science.272.5259.263 8602510
16. Richardson JH Kaye JF Child LA Lever AM Helper virus-free transfer of human immunodeficiency virus type 1 vectors J Gen Virol 1995, 76(Pt 3):691-696. 10.1099/0022-1317-76-3-691 7897357
17. Arya SK Zamani M Kundra P Human immunodeficiency virus type 2 lentivirus vectors for gene transfer: Expression and potential for helper virus-free packaging Hum Gene Ther 1998, 9:1371-1380. 10.1089/ hum.1998.9.9-1371 9650621
18. Poeschla EM Wong-Staal F Looney DJ Efficient transduction of nondividing human cells by feline immunodeficiency virus lentiviral vectors Nat Med 1998, 4:354-357. 10.1038/nm0398-354 9500613
19. Mitrophanous K Yoon S Rohll J Patil D Wilkes F Kim V Kingsman S Kingsman A Mazarakis N Stable gene transfer to the nervous system using a non-primate lentiviral vector Gene Ther 1999, 6:1808-1818. 10.1038/ sj.gt.3301023 10602376
20. Hu J Dunbar CE Update on hematopoietic stem cell gene transfer using non-human primate models Curr Opin Mol Ther 2002, 4:482-490. 12435050
21. Donahue RE Dunbar CE Update on the use of nonhuman primate models for preclinical testing of gene therapy approaches targeting hematopoietic cells Hum Gene Ther 2001, 12:607-617. 10.1089/104303401300057289 11426461
22. Villinger F Brar SS Mayne A Chikkala N Ansari AA Comparative sequence analysis of cytokine genes from human and nonhuman primates J Immunol 1995, 155:3946-3954. 7561102
23. Farese AM MacVittie TJ Roskos L Stead RB Hematopoietic recovery following autologous bone marrow transplantation in a nonhuman primate: effect of variation in treatment schedule with PEG-rHuMGDF Stem Cells 2003, 21:79-89. 10.1634/stemcells.21-1-79 12529554
24. Dunbar CE Takatoku M Donahue RE The impact of ex vivo cytokine stimulation on engraftment of primitive hematopoietic cells in a non-human primate model Ann N Y Acad Sci 2001, 938:236-244. discussion 244-235. 11458513
25. Wagemaker G Neelis KJ Hartong SCC Wognum AW Thomas GR Fielder PJ Eaton DL The efficacy of recombinant TPO in murine And nonhuman primate models for myelosuppression and stem cell transplantation Stem Cells 1998, 16 (Suppl 2):127-141. 11012185
26. Shi PA Hematti P von Kalle C Dunbar CE Genetic marking as an approach to studying in vivo hematopoiesis: Progress in the non-human primate model Oncogene 2002, 21:3274-3283. 10.1038/sj.onc.1205320 12032769
27. Burkhard MJ Dean GA Transmission and immunopathogenesis of FIV in cats as a model for HIV Curr HIV Res 2003, 1:15-29. 10.2174/1570162033352101 15043209
28. Willett BJ Flynn JN Hosie MJ FIV infection of the domestic cat: An animal model for AIDS Immunol Today 1997, 18:182-189. 10.1016/ S0167-5699(97)84665-8 9136455
29. Talbott RL Sparger EE Lovelace KM Fitch WM Pedersen NC Luciw PA Elder JH Nucleotide sequence and genomic organization of feline immunodeficiency virus Proc Natl Acad Sci USA 1989, 86:5743-5747. 297706 2762293 10.1073/ pnas.86.15.5743
30. Olmsted RA Barnes AK Yamamoto JK Hirsch VM Purcell RH Johnson PR Molecular cloning of feline immunodeficiency virus Proc Natl Acad Sci USA 1989, 86:2448-2452. 286930 2928341 10.1073/pnas.86.7.2448
31. Schnell T Foley P Wirth M Munch J Uberla K Development of a self-inactivating, minimal lentivirus vector based on simian immunodeficiency virus Hum Gene Ther 2000, 11:439-447. 10.1089/ 10430340050015905 10697118
32. Wagner R Graf M Bieler K Wolf H Grunwald T Foley P Uberla K Rev-independent expression of synthetic gag-pol genes of human immunodeficiency virus type 1 and simian immunodeficiency virus: implications for the safety of lentiviral vectors Hum Gene Ther 2000, 11:2403-2413. 10.1089/104303400750038507 11096444
33. Negre D Mangeot PE Duisit G Blanchard S Vidalain PO Leissner P Winter AJ Rabourdin-Combe C Mehtali M Moullier P et al. Characterization of novel safe lentiviral vectors derived from simian immunodeficiency virus (SIVmac251) that efficiently transduce mature human dendritic cells Gene Ther 2000, 7:1613-1623. 10.1038/sj.gt.3301292 11083469
34. Mangeot PE Negre D Dubois B Winter AJ Leissner P Mehtali M Kaiserlian D Cosset FL Darlix JL Development of minimal lentivirus vectors derived from simian immunodeficiency virus (SIVmac251) and their use for gene transfer into human dendritic cells J Virol 2000, 74:8307-8315. 116340 10954529 10.1128/JVI.74.18.8307-8315.2000
35. Kiem HP Andrews RG Morris J Peterson L Heyward S Allen JM Rasko JE Potter J Miller AD Improved gene transfer into baboon marrow repopulating cells using recombinant human fibronectin fragment CH-296 in combination with interleukin-6, stem cell factor, FLT-3 ligand, and megakaryocyte growth and development factor Blood 1998, 92:1878-1886. 9731044
36. Wu T Kim HJ Sellers SE Meade KE Agricola BA Metzger ME Kato I Donahue RE Dunbar CE Tisdale JF Prolonged high-level detection of retrovirally marked hematopoietic cells in nonhuman primates after transduction of CD34+ progenitors using clinically feasible methods Mol Ther 2000, 1:285-293. 10.1006/mthe.2000.0034 10933944
37. Kim HJ Tisdale JF Wu T Takatoku M Sellers SE Zickler P Metzger ME Agricola BA Malley JD Kato I et al. Many multipotential gene-marked progenitor or stem cell clones contribute to hematopoiesis in nonhuman primates Blood 2000, 96:1-8. 10891424
38. Rosenzweig M MacVittie TJ Harper D Hempel D Glickman RL Johnson RP Farese AM et al. Whiting-Theobald N Linton GF Yamasaki G Efficient and durable gene marking of hematopoietic progenitor cells in nonhuman primates after nonablative conditioning Blood 1999, 94:2271-2286. 10498599
39. Kelly PF Donahue RE Vandergriff JA Takatoku M Bonifacino AC Agricola BA Metzger ME Dunbar CE Nienhuis AW Vanin EF Prolonged multilineage clonal hematopoiesis in a rhesus recipient of CD34 positive cells marked with a RD114 pseudotyped oncoretroviral vector Blood Cells Mol Dis 2003, 30:132-143. 10.1016/S1079-9796(03)00005-6 12667996
40. Hu J Kelly P Bonifacino A Agricola B Donahue R Vanin E Dunbar CE Direct comparison of RD114-pseudotyped versus amphotropic-pseudotyped retroviral vectors for transduction of rhesus macaque long-term repopulating cells Mol Ther 2003, 8:611-617. 10.1016/ S1525-0016(03)00239-9 14529834
41. Mangeot PE Duperrier K Negre D Boson B Rigal D Cosset FL Darlix JL High levels of transduction of human dendritic cells with optimized SIV vectors Mol Ther 2002, 5:283-290. 10.1006/mthe.2002.0541 11863418
42. Chen C Okayama H High-efficiency transformation of mammalian cells by plasmid DNA Mol Cell Biol 1987, 7:2745-2752. 367891 3670292
43. Munk C Brandt SM Lucero G Landau NR A dominant block to HIV-1 replication at reverse transcription in simian cells Proc Natl Acad Sci USA 2002, 99:13843-13848. 129785 12368468 10.1073/pnas.212400099
44. Besnier C Takeuchi Y Towers G Restriction of lentivirus in monkeys Proc Natl Acad Sci USA 2002, 99:11920-11925. 129369 12154231 10.1073/ pnas.172384599
45. Kootstra NA Munk C Tonnu N Landau NR Verma IM Abrogation of postentry restriction of HIV-1-based lentiviral vector transduction in simian cells Proc Natl Acad Sci USA 2003, 100:1298-1303. 298767 12547912 10.1073/pnas.0337541100
46. Berthoux L Sebastian S Sokolskaja E Luban J Cyclophilin A is required for TRIM5{alpha}-mediated resistance to HIV-1 in Old World monkey cells Proc Natl Acad Sci USA 2005, 102:14849-14853. 1239943 16203999 10.1073/ pnas.0505659102
47. Sandrin V Boson B Salmon P Gay W Negre D Le Grand R Trono D Cosset FL Lentiviral vectors pseudotyped with a modified RD114 envelope glycoprotein show increased stability in sera and augmented transduction of primary lymphocytes and CD34+ cells derived from human and nonhuman primates Blood 2002, 100:823-832. 10.1182/blood-2001-11-0042 12130492
48. Sutton RE Wu HT Rigg R Bohnlein E Brown PO Human immunodeficiency virus type 1 vectors efficiently transduce human hematopoietic stem cells J Virol 1998, 72:5781-5788. 110379 9621037
49. Evans JT Kelly PF O'Neill E Garcia JV Human cord blood CD34+CD38- cell transduction via lentivirus-based gene transfer vectors Hum Gene Ther 1999, 10:1479-1489. 10.1089/10430349950017815 10395373
50. Piconi S Trabattoni D Fusi ML Milazzo F Dix LP Rizzardini G Colombo F Bray D Clerici M Effect of two different combinations of antiretrovirals (AZT+ddI and AZT+3TC) on cytokine production and apoptosis in asymptomatic HIV infection Antiviral Res 2000, 46:171-179. 10.1016/ S0166-3542(00)00076-0 10867155
51. Case SS Price MA Jordan CT Yu XJ Wang L Bauer G Haas DL Xu D Stripecke R et al. Naldini L Stable transduction of quiescent CD34(+)CD38(-) human hematopoietic cells by HIV-1-based lentiviral vectors Proc Natl Acad Sci USA 1999, 96:2988-2993. 15882 10077624 10.1073/pnas.96.6.2988
52. Poznansky MC La Vecchio J Silva-Arietta S Porter-Brooks J Brody K Olszak IT Adams GB Ramstedt U Marasco WA Scadden DT Inhibition of human immunodeficiency virus replication and growth advantage of CD4+ T cells and monocytes derived from CD34+ cells transduced with an intracellular antibody directed against human immunodeficiency virus type 1 Tat Hum Gene Ther 1999, 10:2505-2514. 10.1089/10430349950016843 10543615
53. Rosenzweig M Marks DF Hempel D Lisziewicz J Johnson RP Transduction of CD34+ hematopoietic progenitor cells with an antitat gene protects T-cell and macrophage progeny from AIDS virus infection J Virol 1997, 71:2740-2746. 191396 9060627
54. Davis BR Saitta FP Bauer G Bunnell BA Morgan RA Schwartz DH Targeted transduction of CD34+ cells by transdominant negative Rev-expressing retrovirus yields partial anti-HIV protection of progeny macrophages Hum Gene Ther 1998, 9:1197-1207. 10.1089/hum.1998.9.8-1197 9625259
55. Chatterjee S Li W Wong CA Fisher-Adams G Lu D Guha M Macer JA Forman SJ Wong KK Jr Transduction of primitive human marrow and cord blood-derived hematopoietic progenitor cells with adeno-associated virus vectors Blood 1999, 93:1882-1894. 10068661
56. Shayakhmetov DM Carlson CA Stecher H Li Q Stamatoyannopoulos G Lieber A A high-capacity, capsid-modified hybrid adenovirus/adeno-associated virus vector for stable transduction of human hematopoietic cells J Virol 2002, 76:1135-1143. 135810 11773389
57. Amsellem S Ravet E Fichelson S Pflumio F Dubart-Kupperschmitt A Maximal lentivirus-mediated gene transfer and sustained transgene expression in human hematopoietic primitive cells and their progeny Mol Ther 2002, 6:673-677. 10.1016/S1525-0016(02)90718-5 12436963
58. Zielske SP Gerson SL Cytokines, including stem cell factor alone, enhance lentiviral transduction in nondividing human LTCIC and NOD/SCID repopulating cells Mol Ther 2003, 7:325-333. 10.1016/ S1525-0016(03)00005-4 12668128
59. Yam PY Yee JK Ito JI Sniecinski I Doroshow JH Forman SJ Zaia JA Comparison of amphotropic and pseudotyped VSV-G retroviral transduction in human CD34+ peripheral blood progenitor cells from adult donors with HIV-1 infection or cancer Exp Hematol 1998, 26:962-968. 9728931
60. Liu ML Winther BL Kay MA Pseudotransduction of hepatocytes by using concentrated pseudotyped vesicular stomatitis virus G glycoprotein (VSV-G)-Moloney murine leukemia virus-derived retrovirus vectors: comparison of VSV-G and amphotropic vectors for hepatic gene transfer J Virol 1996, 70:2497-2502. 190094 8642678
61. Gallardo HF Tan C Ory D Sadelain M Recombinant retroviruses pseudotyped with the vesicular stomatitis virus G glycoprotein mediate both stable gene transfer and pseudotransduction in human peripheral blood lymphocytes Blood 1997, 90:952-957. 9242523
62. Burns JC Friedmann T Driever W Burrascano M Yee JK Vesicular stomatitis virus G glycoprotein pseudotyped retroviral vectors: Concentration to very high titer and efficient gene transfer into mammalian and nonmammalian cells Proc Natl Acad Sci USA 1993, 90:8033-8037. 47282 8396259 10.1073/pnas.90.17.8033
63. Mikkola H Woods NB Sjogren M Helgadottir H Hamaguchi I Jacobsen SE Trono D Karlsson S Lentivirus gene transfer in murine hematopoietic progenitor cells is compromised by a delay in proviral integration and results in transduction mosaicism and heterogeneous gene expression in progeny cells J Virol 2000, 74:11911-11918. 112474 11090191 10.1128/ JVI.74.24.11911-11918.2000
64. Bolus NE Basic review of radiation biology and terminology J Nucl Med Technol 2001, 29:67-73. test 76-67. 11376098
65. MacVittie TJ Farese AM Herodin F Grab LB Baum CM McKearn JP Combination therapy for radiation-induced bone marrow aplasia in nonhuman primates using synthokine SC-55494 and recombinant human granulocyte colony-stimulating factor Blood 1996, 87:4129-4135. 8639770
66. Dainiak N Hematologic consequences of exposure to ionizing radiation Exp Hematol 2002, 30:513-528. 10.1016/S0301-472X(02)00802-0 12063018
67. Nieboer P de Vries EG Vellenga E Graaf van der WT Mulder NH Sluiter WJ de Wolf JT Factors influencing haematological recovery following high-dose chemotherapy and peripheral stem-cell transplantation for haematological malignancies; 1-year analysis Eur J Cancer 2004, 40:1199-1207. 10.1016/j.ejca.2004.01.029 15110884
68. Jillella AP Ustun C What is the optimum number of CD34+ peripheral blood stem cells for an autologous transplant? Stem Cells Dev 2004, 13:598-606. 10.1089/scd.2004.13.598 15684827
69. Hanawa H Hematti P Keyvanfar K Metzger ME Krouse A Donahue RE Kepes S Gray J Dunbar CE Persons DA Nienhuis AW Efficient gene transfer into rhesus repopulating hematopoietic stem cells using a simian immunodeficiency virus-based lentiviral vector system Blood 2004, 103:4062-4069. 10.1182/blood-2004-01-0045 14976042
70. Persons DA Allay JA Riberdy JM Wersto RP Donahue RE Sorrentino BP Nienhuis AW Use of the green fluorescent protein as a marker to identify and track genetically modified hematopoietic cells Nat Med 1998, 4:1201-1205. 10.1038/2704 9771757
71. Morris JC Conerly M Thomasson B Storek J Riddell SR Kiem HP Induction of cytotoxic T-lymphocyte responses to enhanced green and yellow fluorescent proteins after myeloablative conditioning Blood 2004, 103:492-499. 10.1182/blood-2003-07-2324 14512305
72. Rosenzweig M Connole M Glickman R Yue SP Noren B DeMaria M Johnson RP Induction of cytotoxic T lymphocyte and antibody responses to enhanced green fluorescent protein following transplantation of transduced CD34(+) hematopoietic cells Blood 2001, 97:1951-1959. 10.1182/ blood.V97.7.1951 11264158
73. Hacein-Bey-Abina S von Kalle C Schmidt M Le Deist F Wulffraat N McIntyre E Radford I Villeval JL Fraser CC Cavazzana-Calvo M Fischer A A serious adverse event after successful gene therapy for X-linked severe combined immunodeficiency N Engl J Med 2003, 348:255-256. 10.1056/ NEJM200301163480314 12529469
74. Hacein-Bey-Abina S Von Kalle C Schmidt M McCormack MP Wulffraat N Leboulch P Lim A Osborne CS Pawliuk R Morillon E et al. LMO2-associated clonal T cell proliferation in two patients after gene therapy for SCID-X1 Science 2003, 302:415-419. 10.1126/science.1088547 14564000