Myeloprotection by cytidine deaminase gene transfer in antileukemic therapy

Neoplasia (United States)

Volumn 15, Issue 3, 2013, Pages 239-248

  Lachmann, Nico ^a   Brennig, Sebastian ^a   Phaltane, Ruhi ^a   Flasshove, Michael ^b   Dilloo, Dagmar ^c   Moritz, Thomas ^a  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b Hosp Duren Gemeinnutzige GmbH   (Germany)

^c UNIVERSITY OF BONN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; 6 O BENZYLGUANINE; ANTHRACYCLINE; AZACITIDINE; BLEOMYCIN; CAMPTOTHECIN; CHLOROETHYLNITROSOUREA DERIVATIVE; CYCLOPHOSPHAMIDE; CYTARABINE; CYTIDINE DEAMINASE; DACARBAZINE; ETOPOSIDE; GEMCITABINE; HYDROXYUREA; MELPHALAN; METHOTREXATE; MULTIDRUG RESISTANCE PROTEIN 1; NITROBENZYLTHIOINOSINE; PARAQUAT; RALTITREXED; TAXOID; TEMOZOLOMIDE; THIOTEPA; TIOGUANINE; TRIMETREXATE; VINCA ALKALOID;

ACUTE GRANULOCYTIC LEUKEMIA; BONE MARROW CELL; BONE MARROW SUPPRESSION; BONE MARROW TOXICITY; BONE MARROW TRANSPLANTATION; CANCER RISK; DISEASE ASSOCIATION; DRUG MEGADOSE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; GENE THERAPY; GENE TRANSFER; GENETIC TRANSDUCTION; GLIOBLASTOMA; HEMATOPOIETIC STEM CELL; HUMAN; LEUKEMIA; LOW DRUG DOSE; MYELODYSPLASTIC SYNDROME; NONHUMAN; PHASE 1 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; REVIEW; TRANSGENE;

EID: 84874598284     PISSN: 15228002     EISSN: 14765586     Source Type: Journal    
DOI: 10.1593/neo.121954     Document Type: Article

References (88)

1. Dick JE, Magli MC, Huszar D, Phillips RA, and Bernstein A (1985). Introduction of a selectable gene into primitive stem cells capable of long-term reconstitution of the hemopoietic system of W/Wv mice. Cell 42, 71-79.
2. Keller G, Paige C, Gilboa E, and Wagner EF (1985). Expression of a foreign gene in myeloid and lymphoid cells derived from multipotent haematopoietic precursors. Nature 318, 149-154.
3. Williams DA, Lemischka IR, Nathan DG, and Mulligan RC (1984). Introduction of new genetic material into pluripotent haematopoietic stem cells of the mouse. Nature 310, 476-480.
4. Fischer A, Hacein-Bey-Abina S, and Cavazzana-Calvo M (2011). Gene therapy for primary immunodeficiencies. Hematol Oncol Clin North Am 25, 89-100.
5. Rivat C, Santilli G, Gaspar HB, and Thrasher AJ (2012). Gene therapy for primary immunodeficiencies. Hum Gene Ther 23, 668-675.
6. Flasshove M, Moritz T, Bardenheuer W, and Seeber S (2003). Hematoprotection by transfer of drug-resistance genes. Acta Haematol 110, 93-106.
7. Moritz T and Williams DA (2001). Marrow protection-transduction of hematopoietic cells with drug resistance genes. Cytotherapy 3, 67-84.
8. Trobridge GD and Kiem HP (2010). Large animal models of hematopoietic stem cell gene therapy. Gene Ther 17, 939-948.
9. Liu L and Gerson SL (2006). Targeted modulation of MGMT: clinical implications. Clin Cancer Res 12, 328-331.
10. Milsom MD and Williams DA (2007). Live and let die: in vivo selection of gene-modified hematopoietic stem cells via MGMT-mediated chemoprotection. DNA Repair (Amst) 6, 1210-1221.
11. Adair JE, Beard BC, Trobridge GD, Neff T, Rockhill JK, Silbergeld DL, Mrugala MM, and Kiem HP (2012). Extended survival of glioblastoma patients after chemoprotective HSC gene therapy. Sci Transl Med 4, 133-157.
12. Li Y and McClay EF (2002). Systemic chemotherapy for the treatment of metastatic melanoma. Semin Oncol 29, 413-426.
13. Geiger H, Schleimer D, Nattamai KJ, Dannenmann SR, Davies SM, and Weiss BD (2006). Mutagenic potential of temozolomide in bone marrow cells in vivo. Blood 107, 3010-3011.
14. Banerjee D, Mayer-Kuckuk P, Capiaux G, Budak-Alpdogan T, Gorlick R, and Bertino JR (2002). Novel aspects of resistance to drugs targeted to dihydrofolate reductase and thymidylate synthase. Biochim Biophys Acta 1587, 164-173.
15. Schiedlmeier B, Kuhlcke K, Eckert HG, Baum C, Zeller WJ, and Fruehauf S (2000). Quantitative assessment of retroviral transfer of the human multidrug resistance 1 gene to human mobilized peripheral blood progenitor cells engrafted in nonobese diabetic/severe combined immunodeficient mice. Blood 95, 1237-1248.
16. Sorrentino BP, Brandt SJ, Bodine D, Gottesman M, Pastan I, Cline A, and Nienhuis AW (1992). Selection of drug-resistant bone marrow cells in vivo after retroviral transfer of human MDR1. Science 257, 99-103.
17. Abonour R, Williams DA, Einhorn L, Hall KM, Chen J, Coffman J, Traycoff CM, Bank A, Kato I, Ward M, et al. (2000). Efficient retrovirus-mediated transfer of the multidrug resistance 1 gene into autologous human long-term repopulating hematopoietic stem cells. Nat Med 6, 652-658.
18. Cowan KH, Moscow JA, Huang H, Zujewski JA, O'Shaughnessy J, Sorrentino B, Hines K, Carter C, Schneider E, Cusack G, et al. (1999). Paclitaxel chemotherapy after autologous stem-cell transplantation and engraftment of hematopoietic cells transduced with a retrovirus containing the multidrug resistance complementary DNA (MDR1) in metastatic breast cancer patients. Clin Cancer Res 5, 1619-1628.
19. Iwasaki H, Huang P, Keating MJ, and Plunkett W (1997). Differential incorporation of ara-C, gemcitabine, and fludarabine into replicating and repairing DNA in proliferating human leukemia cells. Blood 90, 270-278.
20. Schroder JK, Kirch C, Flasshove M, Kalweit H, Seidelmann M, Hilger R, Seeber S, and Schutte J (1996). Constitutive overexpression of the cytidine deaminase gene confers resistance to cytosine arabinoside in vitro. Leukemia 10, 1919-1924.
21. Gran C, Boyum A, Johansen RF, Lovhaug D, and Seeberg EC (1998). Growth inhibition of granulocyte-macrophage colony-forming cells by human cytidine deaminase requires the catalytic function of the protein. Blood 91, 4127-4135.
22. Steuart CD and Burke PJ (1971). Cytidine deaminase and the development of resistance to arabinosyl cytosine. Nat New Biol 233, 109-110.
23. Momparler RL, Laliberte J, Eliopoulos N, Beausejour C, and Cournoyer D (1996). Transfection of murine fibroblast cells with human cytidine deaminase cDNA confers resistance to cytosine arabinoside. Anticancer Drugs 7, 266-274.
24. Neff T and Blau CA (1996). Forced expression of cytidine deaminase confers resistance to cytosine arabinoside and gemcitabine. Exp Hematol 24, 1340-1346.
25. Momparler RL, Eliopoulos N, Bovenzi V, Letourneau S, Greenbaum M, and Cournoyer D (1996). Resistance to cytosine arabinoside by retrovirally mediated gene transfer of human cytidine deaminase into murine fibroblast and hematopoietic cells. Cancer Gene Ther 3, 331-338.
26. Beausejour CM, Eliopoulos N, Momparler L, Le NL, and Momparler RL (2001). Selection of drug-resistant transduced cells with cytosine nucleoside analogs using the human cytidine deaminase gene. Cancer Gene Ther 8, 669-676.
27. Eliopoulos N, Bovenzi V, Le NL, Momparler LF, Greenbaum M, Letourneau S, Cournoyer D, and Momparler RL (1998). Retroviral transfer and long-term expression of human cytidine deaminase cDNA in hematopoietic cells following transplantation in mice. Gene Ther 5, 1545-1551.
28. Eliopoulos N, Cournoyer D, and Momparler RL (1998). Drug resistance to 5-aza-2′-deoxycytidine, 2′,2′-difluorodeoxycytidine, and cytosine arabinoside conferred by retroviral-mediated transfer of human cytidine deaminase cDNA into murine cells. Cancer Chemother Pharmacol 42, 373-378.
29. Flasshove M, Frings W, Schroder JK, Moritz T, Schutte J, and Seeber S (1999). Transfer of the cytidine deaminase cDNA into hematopoietic cells. Leuk Res 23, 1047-1053.
30. Eliopoulos N, Al-Khaldi A, Beausejour CM, Momparler RL, Momparler LF, and Galipeau J (2002). Human cytidine deaminase as an ex vivo drug selectable marker in gene-modified primary bone marrow stromal cells. Gene Ther 9, 452-462.
31. Bauer TR Jr, Miller AD, and Hickstein DD (1995). Improved transfer of the leukocyte integrin CD18 subunit into hematopoietic cell lines by using retroviral vectors having a gibbon ape leukemia virus envelope. Blood 86, 2379-2387.
32. Burns JC, Friedmann T, Driever W, Burrascano M, and Yee JK (1993). 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 90, 8033-8037.
33. Hanenberg H, Xiao XL, Dilloo D, Hashino K, Kato I, and Williams DA (1996). Colocalization of retrovirus and target cells on specific fibronectin fragments increases genetic transduction of mammalian cells. Nat Med 2, 876-882.
34. Moritz T, Dutt P, Xiao X, Carstanjen D, Vik T, Hanenberg H, and Williams DA (1996). Fibronectin improves transduction of reconstituting hematopoietic stem cells by retroviral vectors: evidence of direct viral binding to chymotryptic carboxy-terminal fragments. Blood 88, 855-862.
35. Zhang CC and Lodish HF (2005). Murine hematopoietic stem cells change their surface phenotype during ex vivo expansion. Blood 105, 4314-4320.
36. Bardenheuer W, Lehmberg K, Rattmann I, Brueckner A, Schneider A, Sorg UR, Seeber S, Moritz T, and Flasshove M (2005). Resistance to cytarabine and gemcitabine and in vitro selection of transduced cells after retroviral expression of cytidine deaminase in human hematopoietic progenitor cells. Leukemia 19, 2281-2288.
37. Rattmann I, Kleff V, Sorg UR, Bardenheuer W, Brueckner A, Hilger RA, Opalka B, Seeber S, Flasshove M, and Moritz T (2006). Gene transfer of cytidine deaminase protects myelopoiesis from cytidine analogs in an in vivo murine transplant model. Blood 108, 2965-2971.
38. Brennig S, Rattmann I, Lachmann N, Schambach A, Williams DA, and Moritz T (2012). In vivo enrichment of cytidine deaminase gene-modified hematopoietic cells by prolonged cytosine-arabinoside application. Cytotherapy 14, 451-460.
39. Lachmann N, Brennig S, Pfaff N, Schermeier H, Dahlmann J, Phaltane R, Gruh I, Modlich U, Schambach A, Baum C, et al. (in press). Efficient in vivo regulation of cytidine deaminase expression in the haematopoietic system using a doxycycline-inducible lentiviral vector system. Gene Ther.
40. Neben S, Hellman S, Montgomery M, Ferrara J, and Mauch P (1993). Hematopoietic stem cell deficit of transplanted bone marrow previously exposed to cytotoxic agents. Exp Hematol 21, 156-162.
41. Leach WB, Laster WR Jr, Mayo JG, Griswold DP Jr, and Schabel FM Jr (1969). Toxicity studies in mice treated with 1-β-D-arabinofuranosylcytosine (ara-C). Cancer Res 29, 529-535.
42. Beausejour CM, Le NL, Letourneau S, Cournoyer D, and Momparler RL (1998). Coexpression of cytidine deaminase and mutant dihydrofolate reductase by a bicistronic retroviral vector confers resistance to cytosine arabinoside and methotrexate. Hum Gene Ther 9, 2537-2544.
43. Sauerbrey A, McPherson JP, Zhao SC, Banerjee D, and Bertino JR (1999). Expression of a novel double-mutant dihydrofolate reductase-cytidine deaminase fusion gene confers resistance to both methotrexate and cytosine arabinoside. Hum Gene Ther 10, 2495-2504.
44. Budak-Alpdogan T, Alpdogan O, Banerjee D, Wang E, Moore MA, and Bertino JR (2004). Methotrexate and cytarabine inhibit progression of human lymphoma in NOD/SCID mice carrying a mutant dihydrofolate reductase and cytidine deaminase fusion gene. Mol Ther 10, 574-584.
45. Letourneau S, Palerme JS, Delisle JS, Beausejour CM, Momparler RL, and Cournoyer D (2000). Coexpression of rat glutathione S-transferase A3 and human cytidine deaminase by a bicistronic retroviral vector confers in vitro resistance to nitrogen mustards and cytosine arabinoside in murine fibroblasts. Cancer Gene Ther 7, 757-765.
46. Burnett AK (2012). New induction and postinduction strategies in acute myeloid leukemia. Curr Opin Hematol 19, 76-81.
47. Schroeder TC, Czibere A, Kroeger N, Platzbecker U, Bug G, Uharek L, Luft T, Wolschke C, Bruns I, Zohren F, et al. (2011). Phase II study of Azacitidine (Vidaza®, Aza) and donor lymphocyte infusion (DLI) as first salvage therapy in patients with acute myeloid leukemia (AML) or myelodysplastic syndromes (MDS) relapsing after allogeneic hematopoietic stem cell transplantation (allSCT): final results from the AZARELA-trial (NCT-00795548). Blood 118, 300.
48. Bolanos-Meade J, Smith BD, Gore SD, McDevitt MA, Luznik L, Fuchs EJ, and Jones RJ (2011). 5-Azacytidine as salvage treatment in relapsed myeloid tumors after allogeneic bone marrow transplantation. Biol Blood Marrow Transplant 17, 754-758.
49. Platzbecker U, Wermke M, Radke J, Oelschlaegel U, Seltmann F, Kiani A, Klut IM, Knoth H, Rollig C, Schetelig J, et al. (2012). Azacitidine for treatment of imminent relapse in MDS or AML patients after allogeneic HSCT: results of the RELAZA trial. Leukemia 26, 381-389.
50. Roboz GJ (2011). Novel approaches to the treatment of acute myeloid leukemia. Hematology Am Soc Hematol Educ Program 2011, 43-50.
51. Eppert K, Takenaka K, Lechman ER, Waldron L, Nilsson B, van Galen P, Metzeler KH, Poeppl A, Ling V, Beyene J, et al. (2011). Stem cell gene expression programs influence clinical outcome in human leukemia. Nat Med 17, 1086-1093.
52. Moshaver B, van Rhenen A, Kelder A, van der Pol M, Terwijn M, Bachas C, Westra AH, Ossenkoppele GJ, Zweegman S, and Schuurhuis GJ (2008). Identification of a small subpopulation of candidate leukemia-initiating cells in the side population of patients with acute myeloid leukemia. Stem Cells 26, 3059-3067.
53. Dick JE (2005). Acute myeloid leukemia stem cells. Ann N Y Acad Sci 1044, 1-5.
54. Lapidot T, Pflumio F, Doedens M, Murdoch B, Williams DE, and Dick JE (1992). Cytokine stimulation of multilineage hematopoiesis from immature human cells engrafted in SCID mice. Science 255, 1137-1141.
55. Guzman ML, Neering SJ, Upchurch D, Grimes B, Howard DS, Rizzieri DA, Luger SM, and Jordan CT (2001). Nuclear factor-κB is constitutively activated in primitive human acute myelogenous leukemia cells. Blood 98, 2301-2307.
56. Roboz GJ and Guzman M (2009). Acute myeloid leukemia stem cells: seek and destroy. Expert Rev Hematol 2, 663-672.
57. Saito Y, Kitamura H, Hijikata A, Tomizawa-Murasawa M, Tanaka S, Takagi S, Uchida N, Suzuki N, Sone A, Najima Y, et al. (2010). Identification of therapeutic targets for quiescent, chemotherapy-resistant human leukemia stem cells. Sci Transl Med 2, 17-19.
58. Essers MA, Offner S, Blanco-Bose WE, Waibler Z, Kalinke U, Duchosal MA, and Trumpp A (2009). IFNα activates dormant haematopoietic stem cells in vivo. Nature 458, 904-908.
59. Morrison SJ, Wright DE, and Weissman IL (1997). Cyclophosphamide/ granulocyte colony-stimulating factor induces hematopoietic stem cells to proliferate prior to mobilization. Proc Natl Acad Sci USA 94, 1908-1913.
60. Schambach A and Baum C (2008). Clinical application of lentiviral vectors- concepts and practice. Curr Gene Ther 8, 474-482.
61. Estey EH (2012). Acute myeloid leukemia: 2012 update on diagnosis, risk stratification, and management. Am J Hematol 87, 89-99.
62. Baum C, von Kalle C, Staal FJ, Li Z, Fehse B, Schmidt M, Weerkamp F, Karlsson S, Wagemaker G, and Williams DA (2004). Chance or necessity? Insertional mutagenesis in gene therapy and its consequences. Mol Ther 9, 5-13.
63. Maetzig T, Galla M, Baum C, and Schambach A (2011). Gammaretroviral vectors: biology, technology and application. Viruses 3, 677-713.
64. Barese CN, Krouse AE, Metzger ME, King CA, Traversari C, Marini FC, Donahue RE, and Dunbar CE (2012). Thymidine kinase suicide gene-mediated ganciclovir ablation of autologous gene-modified rhesus hematopoiesis. Mol Ther 20, 1932-1943.
65. Ramos CA, Asgari Z, Liu E, Yvon E, Heslop HE, Rooney CM, Brenner MK, and Dotti G (2010). An inducible caspase 9 suicide gene to improve the safety of mesenchymal stromal cell therapies. Stem Cells 28, 1107-1115.
66. Gyurkocza B, Rezvani A, and Storb RF (2010). Allogeneic hematopoietic cell transplantation: the state of the art. Expert Rev Hematol 3, 285-299.
67. Toy G, Austin WR, Liao HI, Cheng D, Singh A, Campbell DO, Ishikawa TO, Lehmann LW, Satyamurthy N, Phelps ME, et al. (2010). Requirement for deoxycytidine kinase in T and B lymphocyte development. Proc Natl Acad Sci USA 107, 5551-5556.
68. Gossen M and Bujard H (1992). Tight control of gene expression in mammalian cells by tetracycline-responsive promoters. Proc Natl Acad Sci USA 89, 5547-5551.
69. Ting DT, Kyba M, and Daley GQ (2005). Inducible transgene expression in mouse stem cells. Methods Mol Med 105, 23-46.
70. Brown BD, Venneri MA, Zingale A, Sergi Sergi L, and Naldini L (2006). Endogenous microRNA regulation suppresses transgene expression in hematopoietic lineages and enables stable gene transfer. Nat Med 12, 585-591.
71. Gentner B, Visigalli I, Hiramatsu H, Lechman E, Ungari S, Giustacchini A, Schira G, Amendola M, Quattrini A, Martino S, et al. (2010). Identification of hematopoietic stem cell-specific miRNAs enables gene therapy of globoid cell leukodystrophy. Sci Transl Med 2, 58-84.
72. Lachmann N, Jagielska J, Heckl D, Brennig S, Pfaff N, Maetzig T, Modlich U, Cantz T, Gentner B, Schambach A, et al. (2012). MicroRNA-150-regulated vectors allow lymphocyte-sparing transgene expression in hematopoietic gene therapy. Gene Ther 19, 915-924.
73. Papapetrou EP, Kovalovsky D, Beloeil L, Sant'angelo D, and Sadelain M (2009). Harnessing endogenous miR-181a to segregate transgenic antigen receptor expression in developing versus post-thymic T cells in murine hematopoietic chimeras. J Clin Invest 119, 157-168.
74. Moscow JA, Huang H, Carter C, Hines K, Zujewski J, Cusack G, Chow C, Venzon D, Sorrentino B, Chiang Y, et al. (1999). Engraftment of MDR1 and NeoR gene-transduced hematopoietic cells after breast cancer chemotherapy. Blood 94, 52-61.
75. Zhou J and Du Y (2012). Acquisition of resistance of pancreatic cancer cells to 2-methoxyestradiol is associated with the upregulation of manganese superoxide dismutase. Mol Cancer Res 10, 768-777.
76. Patel DH, Allay JA, Belt JA, and Sorrentino BP (2000). Retroviral transfer of the hENT2 nucleoside transporter cDNA confers broad-spectrum antifolate resistance in murine bone marrow cells. Blood 95, 2356-2363.
77. Balabanov S, Gontarewicz A, Keller G, Raddrizzani L, Braig M, Bosotti R, Moll J, Jost E, Barett C, Rohe I, et al. (2011). Abcg2 overexpression represents a novel mechanism for acquired resistance to the multi-kinase inhibitor Danusertib in BCR-ABL-positive cells in vitro. PLoS One 6, e19164.
78. Munster PN and Daud AI (2011). Preclinical and clinical activity of the topoisomerase I inhibitor, karenitecin, in melanoma. Expert Opin Investig Drugs 20, 1565-1574.
79. Tomicic MT and Kaina B (2013). Topoisomerase degradation, DSB repair, p53 and IAPs in cancer cell resistance to camptothecin-like topoisomerase I inhibitors. Biochim Biophys Acta 1835, 11-27.
80. Matsunaga T, Sakamaki S, Kuga T, Kuroda H, Kusakabe T, Akiyama T, Konuma Y, Hirayama Y, Kobune M, Kato J, et al. (2000). GST-π genetransduced hematopoietic progenitor cell transplantation overcomes the bone marrow toxicity of cyclophosphamide in mice. Hum Gene Ther 11, 1671-1681.
81. Capiaux GM, Budak-Alpdogan T, Alpdogan O, Bornmann W, Takebe N, Banerjee D, Maley F, and Bertino JR (2004). Protection of hematopoietic stem cells from pemetrexed toxicity by retroviral gene transfer with a mutant dihydrofolate reductase-mutant thymidylate synthase fusion gene. Cancer Gene Ther 11, 767-773.
82. Mayhew CN, Mampuru LJ, Chendil D, Ahmed MM, Phillips JD, Greenberg RN, Elford HL, and Gallicchio VS (2002). Suppression of retrovirus-induced immunodeficiency disease (murine AIDS) by trimidox and didox: novel ribonucleotide reductase inhibitors with less bone marrow toxicity than hydroxyurea. Antiviral Res 56, 167-181.
83. Sumpter LR, Inayat MS, Yost EE, Duvall W, Hagan E, Mayhew CN, Elford HL, and Gallicchio VS (2004). In vivo examination of hydroxyurea and the novel ribonucleotide reductase inhibitors trimidox and didox in combination with the reverse transcriptase inhibitor abacavir: suppression of retrovirusinduced immunodeficiency disease. Antiviral Res 62, 111-120.
84. Fung H and Demple B (2011). Distinct roles of Ape1 protein in the repair of DNA damage induced by ionizing radiation or bleomycin. J Biol Chem 286, 4968-4977.
85. Morris LP, Degtyareva N, Sheppard C, Heyburn L, Ivanov AA, Kow YW, and Doetsch PW (2012). Saccharomyces cerevisiae Apn1 mutation affecting stable protein expression mimics catalytic activity impairment: implications for assessing DNA repair capacity in humans. DNA Repair (Amst) 11, 753-765.
86. Kobune M, Xu Y, Baum C, Kelley MR, and Williams DA (2001). Retrovirusmediated expression of the base excision repair proteins, formamidopyrimidine DNA glycosylase or human oxoguanine DNA glycosylase, protects hematopoietic cells from N,N ′,N ″-triethylenethiophosphoramide (thioTEPA)-induced toxicity in vitro and in vivo. Cancer Res 61, 5116-5125.
87. Dhar SK, Tangpong J, Chaiswing L, Oberley TD, and St Clair DK (2011). Manganese superoxide dismutase is a p53-regulated gene that switches cancers between early and advanced stages. Cancer Res 71, 6684-6695.
88. Hacke K, Szakmary A, Cuddihy AR, Rozengurt N, Lemp NA, Aubrecht J, Lawson GW, Rao NP, Crooks GM, Schiestl RH, et al. (2012). Combined preconditioning and in vivo chemoselection with 6-thioguanine alone achieves highly efficient reconstitution of normal hematopoiesis with HPRT-deficient bone marrow. Exp Hematol 40, 3-13.