Engraftment and lineage potential of adult hematopoietic stem and progenitor cells is compromised following short-term culture in the presence of an aryl hydrocarbon receptor antagonist

Human Gene Therapy Methods

Volumn 25, Issue 4, 2014, Pages 221-231

  Gu, Angel ^a   Torres Coronado, Monica ^a   Tran, Chy Anh ^a,b   Vu, Hieu ^a,c   Epps, Elizabeth W ^a   Chung, Janet ^d   Gonzalez, Nancy ^a   Blanchard, Suzette ^e   Digiusto, David L ^a,f  

^a Department of Virology City of Hope   (United States)

^b Centre for Blood Cell Therapies at Peter McCallum Center   (Australia)

^c Nodality Inc   (United States)

^d Department of Molecular Biology ^*  (United States)

^e Division of Information Sciences   (United States)

^f CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARYL HYDROCARBON RECEPTOR ANTAGONIST; RECEPTOR BLOCKING AGENT; UNCLASSIFIED DRUG; 2-METHYL-2H-PYRAZOLE-3-CARBOXYLIC ACID (2-METHYL-4-O-TOLYLAZOPHENYL)AMIDE; AROMATIC HYDROCARBON RECEPTOR; AZO COMPOUND; CD34 ANTIGEN; CD45 ANTIGEN; PYRAZOLE DERIVATIVE; THY 1 ANTIGEN;

ADULT; ADULT STEM CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL LINEAGE; CONTROLLED STUDY; ENGRAFTMENT; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; MOUSE; MOUSE MODEL; NONHUMAN; PRIORITY JOURNAL; PROGENY; QUALITATIVE ANALYSIS; QUANTITATIVE ANALYSIS; STEM CELL CULTURE; STEM CELL EXPANSION; STEM CELL GENE THERAPY; UMBILICAL CORD BLOOD; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL CULTURE; CYTOLOGY; DRUG EFFECTS; FETUS BLOOD; HEMATOPOIETIC STEM CELL TRANSPLANTATION; METABOLISM; NONOBESE DIABETIC MOUSE; PHENOTYPE; XENOGRAFT;

ANIMALS; ANTIGENS, CD34; ANTIGENS, CD45; ANTIGENS, THY-1; AZO COMPOUNDS; CELL LINEAGE; CELLS, CULTURED; FETAL BLOOD; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HEMATOPOIETIC STEM CELLS; HUMANS; MICE; MICE, INBRED NOD; MODELS, ANIMAL; PHENOTYPE; PYRAZOLES; RECEPTORS, ARYL HYDROCARBON; TRANSPLANTATION, HETEROLOGOUS;

EID: 84906686932     PISSN: 19466536     EISSN: 19466544     Source Type: Journal    
DOI: 10.1089/hgtb.2014.043     Document Type: Article

References (53)

1. Andre, M.C., Erbacher, A., Gille, C., et al. (2010). Long-term human CD34 + stem cell-engrafted nonobese diabetic/SCID/IL-2R gamma(null) mice show impaired CD8 + T cell maintenance and a functional arrest of immature NK cells. J. Immunol. 185, 2710-2720.
2. Baum, C.M., Weissman, I.L., Tsukamoto, A.S., et al. (1992). Isolation of a candidate human hematopoietic stem-cell population. Proc. Natl. Acad. Sci. USA 89, 2804-2808.
3. Bensinger, W., Appelbaum, F., Rowley, S., et al. (1995a). Factors that influence collection and engraftment of autologous peripheral-blood stem cells. J. Clin. Oncol. 13, 2547-2555.
4. Bensinger, W.I., Weaver, C.H., Appelbaum, F.R., et al. (1995b). Transplantation of allogeneic peripheral blood stem cells mobilized by recombinant human granulocyte colonystimulating factor. Blood 85, 1655-1658.
5. Boitano, A.E., Wang, J., Romeo, R., et al. (2010). Aryl hydrocarbon receptor antagonists promote the expansion of human hematopoietic stem cells. Science 329, 1345-1348.
6. Brehm, M.A., Racki, W.J., Leif, J., et al. (2012). Engraftment of human HSCs in nonirradiated newborn NOD-scid IL2rgamma null mice is enhanced by transgenic expression of membranebound human SCF. Blood 119, 2778-2788.
7. Carlin, S.M., Ma, D.D., and Moore, J.J. (2013). T-cell potential of human adult and cord blood hemopoietic stem cells expanded with the use of aryl hydrocarbon receptor antagonists. Cytotherapy 15, 224-230.
8. Chevaleyre, J., Duchez, P., Rodriguez, L., et al. (2013). Busulfan administration flexibility increases the applicability of scid repopulating cell assay in NSG mouse model. PLoS One 8, e74361.
9. Choi, B., Chun, E., Kim, M., et al. (2011a). Human B cell development and antibody production in humanized NOD/SCID/IL-2Rgamma(null) (NSG) mice conditioned by busulfan. J. Clin. Immunol. 31, 253-264.
10. Choi, B., Chun, E., Kim, M., et al. (2011b). Human T cell development in the liver of humanized NOD/SCID/IL-2Rgamma(null)(NSG) mice generated by intrahepatic injection of CD34( + ) human (h) cord blood (CB) cells. Clin. Immunol. 139, 321-335.
11. Craig, W., Kay, R., Cutler, R.L., and Lansdorp, P.M. (1993). Expression of Thy-1 on human hematopoietic progenitor cells. J. Exp. Med. 177, 1331-1342.
12. DiGiusto, D.L., Krishnan, A., Li, L., et al. (2010). RNA-based gene therapy for HIV with lentiviral vector-modified CD34( + ) cells in patients undergoing transplantation for AIDS-related lymphoma. Sci. Transl. Med. 2, 1-8.
13. DiGiusto, D.L., Stan, R., Krishnan, A., et al. (2013). Development of hematopoietic stem cell based gene therapy for HIV-1 infection: considerations for proof of concept studies and translation to standard medical practice. Viruses 5, 2898-2919.
14. Donahue, R.E., Byrne, E.R., Thomas, T.E., et al. (1996). Transplantation and gene transfer of the human glucocerebrosidase gene into immunoselected primate CD34 + Thy-1+ cells. Blood 88, 4166-4172.
15. Esser, C. (2012). Biology and function of the aryl hydrocarbon receptor: report of an international and interdisciplinary conference. Arch. Toxicol. 86, 1323-1329.
16. Gaardbo, J.C., Hartling, H.J., Gerstoft, J., and Nielsen, S.D. (2012). Incomplete immune recovery in HIV infection: mechanisms, relevance for clinical care, and possible solutions. Clin. Dev. Immunol. 2012, 670957.
17. Gammaitoni, L., Bruno, S., Sanavio, F., et al. (2003). Ex vivo expansion of human adult stem cells capable of primary and secondary hemopoietic reconstitution. Exp. Hematol. 31, 261-270.
18. Gille, C., Orlikowsky, T.W., Spring, B., et al. (2012). Monocytes derived from humanized neonatal NOD/SCID/IL2Rgamma( null) mice are phenotypically immature and exhibit functional impairments. Hum. Immunol. 73, 346-354.
19. Hakki, M., Goldman, D.C., Streblow, D.N., et al. (2014). HCMV infection of humanized mice after transplantation of G-CSF-mobilized peripheral blood stem cells from HCMVseropositive donors. Biol. Blood Marrow Transplant. 20, 132-135.
20. Herrera, C., Sanchez, J., Torres, A., et al. (2001). Early-acting cytokine-driven ex vivo expansion of mobilized peripheral blood CD34 + cells generates post-mitotic offspring with preserved engraftment ability in non-obese diabetic/severe combined immunodeficient mice. Br. J. Haematol. 114, 920-930.
21. Holmes, T., Yan, F., Ko, K.H., et al. (2012). Ex vivo expansion of cord blood progenitors impairs their short-term and longterm repopulating activity associated with transcriptional dysregulation of signalling networks. Cell Prolif. 45, 266-278.
22. Holyoake, T.L., Alcorn, M.J., Richmond, L., et al. (1997). CD34 positive PBPC expanded ex vivo may not provide durable engraftment following myeloablative chemoradiotherapy regimens. Bone Marrow Transplant. 19, 1095-1101.
23. Hu, Y., and Smyth, G.K. (2009). Elda: extreme limiting dilution analysis for comparing depleted and enriched populations in stem cell and other assays. J. Immunol. Methods 347, 70-78.
24. Kramer, B.A., Lemckert, F.A., Alexander, I.E., et al. (2006). Characterisation of a P140K mutant O6-methylguanine-DNA-methyltransferase (MGMT)-expressing transgenic mouse line with drug-selectable bone marrow. J. Gene Med. 8, 1071-1085.
25. Lansdorp, P.M., Dragowska, W., and Mayani, H. (1993). Ontogeny-related changes in proliferative potential of human hematopoietic cells. J. Exp. Med. 178, 787-791.
26. Lepus, C.M., Gibson, T.F., Gerber, S.A., et al. (2009). Comparison of human fetal liver, umbilical cord blood, and adult blood hematopoietic stem cell engraftment in NOD-scid/gammac-/-, Balb/c-Rag1-/-gammac-/-, and C.B-17-scid/bg immunodeficient mice. Hum. Immunol. 70, 790-802.
27. Li, K., Li, C.K., Chuen, C.K., et al. (2005a). Preclinical ex vivo expansion of G-CSF-mobilized peripheral blood stem cells: effects of serum-free media, cytokine combinations and chemotherapy. Eur. J. Haematol. 74, 128-135.
28. Li, M.J., Kim, J., Li, S., et al. (2005b). Long-term inhibition of HIV-1 infection in primary hematopoietic cells by lentiviral vector delivery of a triple combination of anti-HIV shRNA, anti-CCR5 ribozyme, and a nucleolar-localizing TAR decoy. Mol. Ther. 12, 900-909.
29. Mayani, H., and Lansdorp, P.M. (1994). Thy-1 expression is linked to functional properties of primitive hematopoietic progenitor cells from human umbilical cord blood. Blood 83, 2410-2417.
30. McDermott, S.P., Eppert, K., Lechman, E.R., et al. (2010). Comparison of human cord blood engraftment between immunocompromised mouse strains. Blood 116, 193-200.
31. McNiece, I.K., Almeida-Porada, G., Shpall, E.J., and Zanjani, E. (2002). Ex vivo expanded cord blood cells provide rapid engraftment in fetal sheep but lack long-term engrafting potential. Exp. Hematol. 30, 612-616.
32. Naldini, L. (2011). Ex vivo gene transfer and correction for cellbased therapies. Nat. Rev. Genet. 12, 301-315.
33. National Research Council (U.S.), Committee for the Update of the Guide for the Care and use of Laboratory Animals, Institute for Laboratory Animal Research (U.S.), and National Academies Press (U.S.). (2011). Guide for the Care and Use of Laboratory Animals (National Academies Press, Washington, DC).
34. Notta, F., Doulatov, S., Laurenti, E., et al. (2011). Isolation of single human hematopoietic stem cells capable of long-term multilineage engraftment. Science 333, 218-221.
35. Peault, B., Weissman, I.L., Buckle, A.M., et al. (1993). Thy-1-expressing CD34 + human cells express multiple hematopoietic potentialities in vitro and in SCID-hu mice. Nouv. Rev. Fr. Hematol. 35, 91-93.
36. Peters, S.O., Kittler, E.L., Ramshaw, H.S., and Quesenberry, P.J. (1996). 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 87, 30-37.
37. Reimann, C., Six, E., Dal-Cortivo, L., et al. (2012). Human Tlymphoid progenitors generated in a feeder-cell-free Deltalike-4 culture system promote T-cell reconstitution in NOD/SCID/gammac(-/-) mice. Stem Cells 30, 1771-1780.
38. Scholbach, J., Schulz, A., Westphal, F., et al. (2012). Comparison of hematopoietic stem cells derived from fresh and cryopreserved whole cord blood in the generation of humanized mice. PLoS One 7, e46772.
39. Shultz, L.D., Lyons, B.L., Burzenski, L.M., et al. (2005). Human lymphoid and myeloid cell development in NOD/LtSz-scid IL2R gamma null mice engrafted with mobilized human hemopoietic stem cells. J. Immunol. 174, 6477-6489.
40. Shultz, L.D., Ishikawa, F., and Greiner, D.L. (2007). Humanized mice in translational biomedical research. Nat. Rev. Immunol. 7, 118-130.
41. Singh, K.P., Casado, F.L., Opanashuk, L.A., and Gasiewicz, T.A. (2009a). The aryl hydrocarbon receptor has a normal function in the regulation of hematopoietic and other stem/progenitor cell populations. Biochem. Pharmacol. 77, 577-587.
42. Singh, K.P., Wyman, A., Casado, F.L., et al. (2009b). Treatment of mice with the Ah receptor agonist and human carcinogen dioxin results in altered numbers and function of hematopoietic stem cells. Carcinogenesis 30, 11-19.
43. Singh, M., Singh, P., Gaudray, G., et al. (2012). An improved protocol for efficient engraftment in NOD/LTSZ-SCIDIL-2Rgammanull mice allows HIV replication and development of anti-HIV immune responses. PLoS One 7, e38491.
44. Singh, K.P., Bennett, J.A., Casado, F.L., et al. (2014). Loss of aryl hydrocarbon receptor promotes gene changes associated with premature hematopoietic stem cell exhaustion and development of a myeloproliferative disorder in aging mice. Stem Cells Dev. 23, 95-106.
45. Snoeck, H.W. (2013). Aging of the hematopoietic system. Curr. Opin. Hematol. 20, 355-361.
46. Strowig, T., Gurer, C., Ploss, A., et al. (2009). Priming of protective T cell responses against virus-induced tumors in mice with human immune system components. J. Exp. Med. 206, 1423-1434.
47. Tanavde, V.M., Malehorn, M.T., Lumkul, R., et al. (2002). Human stem-progenitor cells from neonatal cord blood have greater hematopoietic expansion capacity than those from mobilized adult blood. Exp. Hematol. 30, 816-823.
48. Thurmond, T.S., Silverstone, A.E., Baggs, R.B., et al. (1999). A chimeric aryl hydrocarbon receptor knockout mouse model indicates that aryl hydrocarbon receptor activation in hematopoietic cells contributes to the hepatic lesions induced by 2,3,7, 8-tetrachlorodibenzo-p-dioxin. Toxicol. Appl. Pharmacol. 158, 33-40.
49. Tisdale, J.F., Hanazono, Y., Sellers, S.E., et al. (1998). Ex vivo expansion of genetically marked rhesus peripheral blood progenitor cells results in diminished long-term repopulating ability. Blood 92, 1131-1141.
50. Tran, C.A., Torres-Coronado, M., Gardner, A., et al. (2012). Optimized processing of growth factor mobilized peripheral blood CD34 + products by counterflow centrifugal elutriation. Stem Cells Transl. Med. 1, 422-429.
51. Van Zant, G., and Liang, Y. (2012). Concise review: hematopoietic stem cell aging, life span, and transplantation. Stem Cells Transl. Med. 1, 651-657.
52. Von Drygalski, A., Alespeiti, G., Ren, L., and Adamson, J.W. (2004). Murine bone marrow cells cultured ex vivo in the presence of multiple cytokine combinations lose radioprotective and long-term engraftment potential. Stem Cells Dev. 13, 101-111.
53. Watts, K.L., Adair, J., and Kiem, H.P. (2011). Hematopoietic stem cell expansion and gene therapy. Cytotherapy 13, 1164-1171.