γ-glutamylcysteine synthetase and L-buthionine-(S,R)-sulfoximine: A new selection strategy for gene-transduced neural and hematopoietic stem/progenitor cells

Human Gene Therapy

Volumn 16, Issue 6, 2005, Pages 711-724

  Lorico, Aurelio ^a,b,d   Bratbak, Daniel ^a   Meyer, Johann ^c   Kunke, David ^a   Krauss, Stefan ^a   Plott, Walter E ^b   Solodushko, Victor ^b   Baum, Christopher ^c   Fodstad, Oystein ^a,b   Rappa, Germana ^a,b  

^a OSLO UNIVERSITY HOSPITAL   (Norway)

^b UNIVERSITY OF SOUTH ALABAMA   (United States)

^c HANNOVER MEDICAL SCHOOL   (Germany)

^d Mitchell Cancer Institute   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BUTHIONINE SULFOXIMINE; ENHANCED GREEN FLUORESCENT PROTEIN; GLUTAMATE CYSTEINE LIGASE; GLUTATHIONE; MARKER; RETROVIRUS VECTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BONE MARROW; CELL CULTURE; CELL STRAIN 3T3; CLONOGENESIS; CONTROLLED STUDY; CYTOTOXICITY; EX VIVO STUDY; FIBROBLAST; FLOW CYTOMETRY; GENE OVEREXPRESSION; GENE THERAPY; GENETIC TRANSDUCTION; HEMATOPOIETIC STEM CELL; IN VITRO STUDY; LATERAL BRAIN VENTRICLE; MALE; MOUSE; NEURAL STEM CELL; NEWBORN; NONHUMAN; TRANSGENE;

3T3 CELLS; ANIMALS; BUTHIONINE SULFOXIMINE; CELLS, CULTURED; DRUG RESISTANCE, MULTIPLE; GLUTAMATE-CYSTEINE LIGASE; GLUTATHIONE; GREEN FLUORESCENT PROTEINS; HEMATOPOIETIC STEM CELLS; MALE; MICE; MICE, INBRED C57BL; NEURONS; SELECTION (GENETICS); STEM CELLS; TRANSDUCTION, GENETIC;

EID: 20844449559     PISSN: 10430342     EISSN: None     Source Type: Journal    
DOI: 10.1089/hum.2005.16.711     Document Type: Article

References (47)

1. ABOODY, K.S., BROWN, A., RAINOV, N.G., BOWER, K.A., LIU, S., YANG, W., SMALL, J.E., HERRLINGER, U., OUREDNIK, V., BLACK, P.M., BREAKEFIELD, X.O., and SNYDER, E.Y. (2000). Neural stem cells display extensive tropism for pathology in adult brain: Evidence from intracranial gliomas. Proc. Natl. Acad. Sci. U.S.A. 97, 12846-12851.
2. ALLAY, J.A., PERSONS, D.A., GALIPEAU, J., RIBERDY, J.M., ASHMUN, R.A., BLAKLEY, R.L., and SORRENTINO, B.P. (1998). In vivo selection of retrovirally transduced hematopoietic stem cells. Nat. Med. 4, 1136-1143.
3. ANDERSON, C.P., TSAI, J.M., MEEK, W.E., LIU, R.M., TANG, Y., FORMAN, H.J., and REYNOLDS, C.P. (1999). Depletion of glutathione by buthionine sulfoxine is cytotoxic for human neurobtastoma cell lines via apoptosis. Exp. Cell Res. 246, 183-192.
4. BAILEY, H.H. (1998). L-S,R-buthionine sulfoximine: Historical development and clinical issues. Chem. Biol. Interact. 111-112, 239-254.
5. BAILEY, H.H., MULCAHY, R.T., TUTSCH, K.D., ARZOOMANIAN, R.Z., ALBERTI, D., TOMBES, M.B., WILDING, G., POMPLUN, M., and SPRIGGS, D.R. (1994). Phase I clinical trial of intravenous L-buthionine sulfoximine and melphalan: An attempt at modulation of glutathione. J. Clin. Oncol. 12, 194-205.
6. BAILEY, H.H., RIPPLE, G., TUTSCH, K.D., ARZOOMANIAN, R.Z., ALBERTI, D., FEIERABEND, C., MAHVI, D., SCHINK, J., POMPLUN, M., MULCAHY, R.T., and WILDING, G. (1997). Phase I study of continuous-infusion L-S,R-buthionine sulfoximine with intravenous melphalan. J. Natl. Cancer Inst. 89, 1789-1796.
7. BAUM, C., HEGEWISCH-BECKER, S., ECKERT, H.G., STOCKING, C., and OSTERTAG, W. (1995). Novel retroviral vectors for efficient expression of the multidrug resistance (mdr-1) gene in early hematopoietic cells. J. Virol. 69, 7541-7547.
8. BAUM, C., ITOH, K., MEYER, J., LAKER, C., ITO, Y., and OSTERTAG, W. (1997). The potent enhancer activity of the polycythemic strain of spleen focus-forming virus in hematopoietic cells is governed by a binding site for Sp1 in the upstream control region and by a unique enhancer core motif, creating an exclusive target for PEBP/CBF. J. Virol. 71, 6323-6331.
9. BENEDETTI S., PIROLA, B., POLLO, B., MAGRASSI, L., BRUZZONE, M.G., RIGAMONTI, D., GALLI, R., SELLERI, S., DI MECO, F., DE ERAJA, C., VESCOVI, A., CATTANEO, E., and FINOCCHIARO, G. (2000). Gene therapy of experimental brain tumors using neural progenitor cells. Nat. Med. 6, 447-450.
10. CAMPBELL, E.B., HAYWARD, M.L., and GRIFFITH, O.W. (1391). Analytical and preparative separation of the diastereomers of L-buthionine (SR)-sulfoximine, a potent inhibitor of glutathione biosynthesis. Anal. Biochem. 194, 268-277.
11. , CAVAZZANA-CALVO, M., HACEIN-BEY, S., DE SAINT BASILE, G., GROSS, F., YVON, E., NUSBAUM, P., SELZ, F., HUE, C., CERTAIN, S., CASANOVA, J.L., BOUSSO, P., DEIST, F.L, and FISCHER, A. (2000), Gene therapy of human severe combined immunodeficiency (SCID)-X1 disease. Science 288, 669-672.
12. COLE, S.P., DOWNES, H.F., MIRSKI, S.E., and CLEMENTS, D.J. (1990). Alterations in glutathione and glutathione-related enzymes in a multidrug-resistant small cell lung cancer cell line. Mol. Pharmacol. 37, 192-197.
13. 6-methylguanine-DNA methyltransferase-transduced marrow progenitors repopulate nonmyeloablated mice after drug selection. Blood 95, 3078-3084.
14. FEHSE, B., KUSTIKOVA, O.S., BUBENHEIM, M., and BAUM, C. (2004). Pois(s)on: It's a question of dose. Gene Ther. 11, 879-881.
15. FEKETE, I., GRIFFITH, O.W., SCHLAGETER, K.E., BIGNER, D.D., FRIEDMAN, H.S., and GROOTHUIS, D.R. (1990). Rate of buthionine sulfoximine entry into brain and xenotransplanted human gliomas. Cancer Res. 50, 1251-1256.
16. FRIEDMANN, T. (1996). Human gene therapy: An immature genie, but certainly out of the bottle. Nat. Med. 2, 144-147.
17. HACEIN-BEY-ABINA, S., VON KALLE, C., SCHMIDT, M., MCCORMACK, M.P., WULFFRAAT, N., LEBOULCH, P., LIM, A., OSBORNE, C.S., PAWLIUK, R., MORILLON, E., SORENSEN, R., FORSTER, A., FRASER, P., COHEN, J.I., DE SAINT BASILE, G., ALEXANDER, I., WINTERGERST, U., FREBOURG, T., AURIAS, A., STOPPA-LYONNET, D., ROMANA, S., RADFORD-WEISS, I., GROSS, F., VALENSI, F., DELABESSE, E., MACINTYRE, E., SIGAUX, F., SOULIER, J., LEIVA, L.E., WISSLER, M., PRINZ, C., RABBITTS, T.H., LE DEIST, F., FISCHER, A., and CAVAZZANA-CALVO, M. (2003). LMO2-associated clonal T cell proliferation in two patients after gene therapy for SCID-X1. Science 302, 415-419.
18. HAMILTON, T.C., WINKER, M.A., LOUIE, K.G., BATIST, G., BEHRENS, B.C., TSURUO, T., GROTZINGER, K.R., MCKOY, W.M., YOUNG, R.C., and OZOLS, R.F. (1985). Augmentation of Adriamycin, melphalan, and cisplatin cytotoxicity in drug-resistant and -sensitive human ovarian carcinoma cell lines by buthionine sulfoximine mediated glutathione depletion. Biochem. Pharmacol. 34, 2583-2586.
19. HILDINGER, M., FEHSE, B., HEGEWISCH-BECKER, S., JOHN, J., RAFFERTY, J.R., OSTERTAG, W., and BAUM. C. (1998). Dominant selection of hematopoietic progenitor cells with retroviral MDRI co-expression vectors. Hum. Gene Ther. 9, 33-42.
20. KINSELLA, T.M., and NOLAN. G.P. (1996). Episomal vectors rapidly and stably produce high-titer recombinant retrovirus. Hum. Gene Ther. 7, 1405-1413.
21. KUSTIKOVA, O.S., WAHLERS, A., KUHLCKE, K., STAHLE, B., ZANDER, A.R., BAUM, C., and FEHSE, B. (2003). Dose finding with retroviral vectors: Correlation of retroviral vector copy numbers in single cells with gene transfer efficiency in a cell population. Blood 102, 3934-3937.
22. LE BELLE, J.E., and SVENDSEN, C.N. (2002). Stem cells for neurodegenerative disorders: Where can we go from here? Biodrugs 16, 389-401.
23. LI, Z., DULLMANN, J., SCHIEDLMEIER, B., SCHMIDT, M., VON KALLE, C., MEYER, J., FORSTER, M., STOCKING, C., WAHLERS, A., FRANK, O, OSTERTAG, W., KUHLCKE, K., ECKERT, H.G., FEHSE, B., and BAUM, C. (2002). Murine leukemia induced by retroviral gene marking. Science 296, 497.
24. LI, Z., SCHWIEGER, M., LANGE, C., KRAUNUS, J., SUN, H., VAN DEN AKKER, E., MODLICH, U., SERINSOZ, E., WILL, E., VON LAER, D., STOCKING, C., FEHSE, B., SCHIEDLMEIER, B., and BAUM, C. (2003). Predictable and efficient retroviral gene transfer into murine bone marrow repopulating cells using a defined vector dose. Exp. Hematol. 31, 1206-1214.
25. LORICO, A., BERTOLA, A., BAUM, C., FODSTAD, O., and RAPPA, G. (2002). Role of the multidrug resistance protein 1 in protection from heavy metal oxyanions: Investigations in vitro and in MRP1-deficient mice. Biochem. Biophys. Res. Commun. 291, 617-622.
26. MACHON, O., VAN DEN BOUT, C.J., BACKMAN, M., ROSOK, O., CAUBIT, X., FROMM, S.H., GERONIMO, B., and KRAUSS, S. (2002). Forebrain-specific promoter/enhancer D6 derived from the mouse Dach1 gene controls expression in neural stem cells. Neuroscience 112, 951-966.
27. MEISTER, A., and ANDERSON, M.E. (1983). Glutathione. Annu. Rev. Biochem. 52, 711-760.
28. MIGNON, A., GUIDOTTI, J.E., MITCHELL, C., FABRE, M., WERNET, A., DE LA COSTE, A., SOUBRANE, O., GILGENKRANTZ, H., and KAHN, A. (1998). Selective repopulation of normal mouse liver by Fas/CD95-resistant hepatocytes. Nat. Med. 4, 1185-1188.
29. NEFF, T., HORN, P.A., VALLI, V.E., GOWN, A.M., WARDWELL, S., WOOD, B.L., VON KALLE, C., SCHMIDT, M., PETERSON, L.J., MORRIS, J.C., RICHARD, R.E., CLACKSON, T., KIEM, H.P., and BLAU, C.A. (2002). Pharmacologically regulated in vivo selection in a large animal. Blood 100, 2026-2031.
30. O'BRIEN, M., KRUH, G.D., and TEW, K.D. (2000). The influence of coordinate overexpression of glutathione phase II detoxification gene products on drug resistance. J. Pharmacol. Exp. Ther. 294, 480-487.
31. O'DWYER, P.J., HAMILTON. T.C., LACRETA, P.P., GALLO, J.M., KILPATRICK, D., HALBHERR, T., BRENNAN, J., BOOKMAN, M.A., HOFFMAN, J., YOUNG, R.C., COMIS, R.L., and OZOLS, R.F, (1996). Phase I trial of buthionine sulfoximine in combination with melphalan in patients with cancer. J. Clin. Oncol. 14, 249-256.
32. PARK, K.I., OUREDNIK, J., OUREDNIK, V., TAYLOR, R.M., ABOODY, K.S., AUGUSTE, K.I., LACHYANKAR, M.B., REDMOND, D.E., and SNYDER, E.Y. (2002). Global gene and cell replacement strategies via stem cells. Gene Ther. 9, 613-624.
33. PLUCHINO, S., QUATTRINI, A., BRAMBILLA, E., GRITTI, A., SALANI, G., DINA, G., GALLI, R., DEL CARRO, U., AMADIO, S., BERGAMI, A., FURLAN, R., COMI, G., VESCOVI, A.L., and MARTINO, G. (2003). Injection of adult neurospheres induces recovery in a chronic model of multiple sclerosis. Nature 422, 688-694.
34. RAPPA, G., LORICO, A., HILDINGER, M., FODSTAD, O., and BAUM, C. (2001). Novel bicistronic retroviral vector expressing γ-glutamylcysteine synthetase and the multidrug resistance protein 1 (MRP1) protects cells from MRP1-effluxed drugs and alkylating agents. Hum. Gene Ther. 12, 1785-1796.
35. RAPPA, G., GAMCSIK, M.P., MITINA, R.L., BAUM, C., FODSTAD, O., and LORICO, A. (2003). Retroviral transfer of MRP1 and γ-glutamyl cysteine synthetase modulates cell sensitivity to L-buthionine-S,A-sulphoximine (BSO): New rationale for the use of BSO in cancer therapy. Eur. J. Cancer 39, 120-128.
36. RAPPA, G., KUNKE, D., HOLTER, J., DIEP, D.B., MEYER, J., BAUM, C., FODSTAD, O., KRAUSS, S., and LORICO, A. (2004). Efficient expansion and gene transduction of mouse neural stem/ progenitor cells on recombinant fibronectin. Neuroscience 124, 823-830.
37. REVESZ, L., EDGREN, M.R., and WAINSON, A.A. (1994). Selective toxicity of buthionine sulfoximine (BSO) to melanoma cells in vitro and in vivo. Int. J. Radiat. Oncol. Biol. Phys. 29, 403-406.
38. RIESS, P., ZHANG, C., SAATMAN, K.E., LAURER. H.L., LONGHI, L.G., RAGHUPATHI, R., LENZLINGER, P.M., LIFSHITZ, J., BOOCKVAR, J., NEUGEBAUER, E., SNYDER, E.Y., and MCINTOSH, T.K. (2002). Transplanted neural stem cells survive, differentiate, and improve neurological motor function after experimental traumatic brain injury. Neurosurgery 51, 1043-1052; discussion, 1052-1044.
39. RUSSO, A., TOCHNER, Z., PHILLIPS, T., CARMICHAEL, J., DEGRAFF, W., FRIEDMAN, N., FISHER, J., and MITCHELL, J.B. (1986). In vivo modulation of glutathione by buthionine sulfoximine: Effect on marrow response to melphalan. Int. J. Radiat. Oncol. Biol. Phys. 12, 1187-1189.
40. SADAT, M.A., PECH, N., SAULNIER, S., LEROY, B.A., HOSSLE, J.P., GREZ. M., and DINAUER, M.C. (2003). Long-term high-level reconstitution of NADPH oxidase activity in murine X-linked chronic granulomatous disease using a bicistronic vector expressing gp91phox and a Delta LNGFR cell surface marker. Hum. Gene Ther. 14, 651-666.
41. SCHAMBACH, A., WODRICH, H., HILDINGER, M., BOHNE, J., KRAUSSLICH, H.G., and BAUM, C. (2000). Context dependence of different modules for posttranscriptional enhancement of gene expression from retroviral vectors. Mol. Ther. 2, 435-445.
42. SORRENTINO, B.P., BRANDT, S.J., BODINE, D., GOTTESMAN, M., PASTAN, I., CLINE, A., and NIENHUIS, A.W. (1992). Selection of drug-resistant bone marrow cells in vivo after retroviral transfer of human MDR1. Science 257, 99-103.
43. TIETZE, F. (1969). Enzymic method for quantitative determination of nanogram amounts of total and oxidized glutathione: Applications to mammalian blood and other tissues. Anal. Biochem. 27, 502-522.
44. VANHOEFER, U., CAO, S., MINDERMAN. H., TOTH, K., SKENDERIS, B.S., II, SLOVAK, M.L., and RUSTUM, Y.M. (1996). D,L-Buthionine-(S,R)-sulfoximine potentiates in vivo the therapeutic efficacy of doxorubicin against multidrug resistance protein-expressing tumors. Clin. Cancer Res. 2, 1961-1968.
45. WAHLERS, A., SCHWIEGER, M., LI, Z., MEIER-TACKMANN, D., LINDEMANN, C., ECKERT, H.G., VON LAER, D., and BAUM, C. (2001). Influence of multiplicity of infection and protein stability on retroviral vector-mediated gene expression in hematopoietic cells. Gene Ther. 8, 477-486.
46. WAHLERS. A., ZIPFEL, P.F., SCHWIEGER, M., OSTERTAG, W., and BAUM, C. (2002). In vivo analysis of retroviral enhancer mutations in hematopoietic cells: SP1/EGR1 and ETS/GATA motifs contribute to long terminal repeat specificity. J. Virol. 76, 303-312.
47. YAO, K., GODWIN, A.K., OZOLS, R.F., HAMILTON, T.C., and O'DWYER, P.J. (1993). Variable baseline γ-glutamylcysteine synthetase messenger RNA expression in peripheral mononuclear cells of cancer patients, and its induction by buthionine sulfoximine treatment. Cancer Res. 53, 3662-3666.