DOI QR코드

DOI QR Code

How to Establish Acute Myeloid Leukemia Xenograft Models Using Immunodeficient Mice

  • Shan, Wu-Lin (Department of Laboratory Medicine, Anhui Provincial Hospital) ;
  • Ma, Xiao-Ling (Department of Laboratory Medicine, Anhui Provincial Hospital)
  • Published : 2013.12.31

Abstract

The discovery of the immunodeficient mice has provided a tool for establishing animal models as hosts for in vivo analysis of AML. Various model systems have been established in the last few decades, and it is essential that murine AML models are developed to exploit more specific, targeted therapeutics. In this review, we concentrate on the models of AML and discuss the development of immunodeficiency models for understanding of leukemogenesis, describe those now available and their values and document the methods used for establishing and identifying AML mice models, as well as factors influencing engraftment of human AML in immunodeficient mice. Thus, the function of this article is to provide clinicians and experimentalists with a chronological, comprehensive appraisal of all AML model systems.

References

  1. Agliano A, Martin-Padura I, Mancuso P, et al (2008). Human acute leukemia cells injected in NOD/LtSz-scid/IL-2R$\gamma$ null mice generate a faster and more efficient disease compared to other NOD/scid-related strains. Int J Cancer, 123, 2222-7. https://doi.org/10.1002/ijc.23772
  2. Ahmed F, Ings SJ, Pizzey AR, et al (2004). Impaired bone marrow homing of cytokine-activated CD34+ cells in the NOD/SCID model. Blood, 103, 2079-87. https://doi.org/10.1182/blood-2003-06-1770
  3. Ailles LE, Gerhard B, Hogge DE (1997). Detection and characterization of primitive malignant and normal progenitors in patients with acute myelogenous leukemia using long-term coculture with supportive feeder layers and cytokines. Blood, 90, 2555-64.
  4. Ailles LE, Gerhard B, Kawagoe H, et al (1999). Growth characteristics of acute myelogenous leukemia progenitors that initiate malignant hematopoiesis in nonobese diabetic/severe combined immunodeficient mice. Blood, 94, 1761-72.
  5. Appelbaum FR, Rowe JM, Radich J, et al (2001). Acute myeloid leukemia. Hematol Am Soc Hematol Educ Program, 2001, 62-86. https://doi.org/10.1182/asheducation-2001.1.62
  6. Avigdor A, Goichberg P, Shivtiel S, et al (2004). CD44 and hyaluronic acid cooperate with SDF-1 in the trafficking of human CD34+ stem/progenitor cells to bone marrow. Blood, 103, 2981-9. https://doi.org/10.1182/blood-2003-10-3611
  7. Bennett J, Catovsky D, Daniel M, et al (1989). Proposals for the classification of chronic (mature) B and T lymphoid leukaemias. French-American-British (FAB) Cooperative Group. Am J Clin Pathol, 42, 567-84. https://doi.org/10.1136/jcp.42.6.567
  8. Bennett JM, Catovsky D, Daniel MT, et al (1985). Proposed revised criteria for the classification of acute myeloid leukemia A report of the French-American-British Cooperative Group. Ann Intern Med, 103, 620-5. https://doi.org/10.7326/0003-4819-103-4-620
  9. Blair A, Hogge D, Sutherland H (1998). Most acute myeloid leukemia progenitor cells with long-term proliferative ability in vitro and in vivo have the phenotype CD34+/CD71−/HLA-DR−. Blood, 92, 4325-35.
  10. Bonnet D. Humanized model to study leukemic stem cells. Leukemia, 2009. p. 247-62.
  11. Bonnet D, Bhatia M, Wang J, et al (1999). Cytokine treatment or accessory cells are required to initiate engraftment of purified primitive human hematopoietic cells transplanted at limiting doses into NOD/SCID mice. Bone Marrow Transplant, 23, 203. https://doi.org/10.1038/sj.bmt.1701564
  12. Bonnet D, Dick JE (1997). Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med, 3, 730-7. https://doi.org/10.1038/nm0797-730
  13. Bosma GC, Custer RP, Bosma MJ (1983). A severe combined immunodeficiency mutation in the mouse. Nature, 301, 527-30. https://doi.org/10.1038/301527a0
  14. Bosma GC, Fried M, Custer RP, et al (1988). Evidence of functional lymphocytes in some (leaky) scid mice. J Exp Med, 167, 1016-33. https://doi.org/10.1084/jem.167.3.1016
  15. Brehm MA, Cuthbert A, Yang C, et al (2010). Parameters for establishing humanized mouse models to study human immunity: Analysis of human hematopoietic stem cell engraftment in three immunodeficient strains of mice bearing the< i> IL2r $\gamma$< sup> null mutation. Clin Immunol, 135, 84-98. https://doi.org/10.1016/j.clim.2009.12.008
  16. Caretto P, Forni M, d'Orazi G, et al (1989). Xenotransplantation in immunosuppressed nude mice of human solid tumors and acute leukemias directly from patients orin vitro cell lines. Ric Clin Lab, 19, 231-43.
  17. Carroll A, Hardy R, Bosma M (1989). Occurrence of mature B (IgM+, B220+) and T (CD3+) lymphocytes in scid mice. J Immunol, 143, 1087-93.
  18. Casasnovas R, Campos L, Mugneret F, et al (1998). Immunophenotypic patterns and cytogenetic anomalies in acute non-lymphoblastic leukemia subtypes: a prospective study of 432 patients. Leukemia, 12, 34-43. https://doi.org/10.1038/sj.leu.2400893
  19. Cashman JD, Lapidot T, Wang JC, et al (1997). Kinetic evidence of the regeneration of multilineage hematopoiesis from primitive cells in normal human bone marrow transplanted into immunodeficient mice. Blood, 89, 4307-16.
  20. Cesano A, Hoxie J, Lange B, et al (1992). The severe combined immunodeficient (SCID) mouse as a model for human myeloid leukemias. Oncogene, 7, 827.
  21. Cesano A, Visonneau S, Cioe L, et al (1994). Reversal of acute myelogenous leukemia in humanized SCID mice using a novel adoptive transfer approach. Eur J Clin Invest, 94, 1076. https://doi.org/10.1172/JCI117422
  22. Chelstrom LM, Gunther R, Simon J, et al (1994). Childhood acute myeloid leukemia in mice with severe combined immunodeficiency. Blood, 84, 20-6.
  23. Chen Y, Jacamo R, Shi Y-x, et al (2012). Human extramedullary bone marrow in mice: a novel in vivo model of genetically controlled hematopoietic microenvironment. Blood, 119, 4971-80. https://doi.org/10.1182/blood-2011-11-389957
  24. Cheson BD, Cassileth PA, Head DR, et al (1990). Report of the National Cancer Institute-sponsored workshop on definitions of diagnosis and response in acute myeloid leukemia. J Clin Oncol, 8, 813-9. https://doi.org/10.1200/JCO.1990.8.5.813
  25. Christianson SW, Greiner DL, Hesselton RA, et al (1997). Enhanced human CD4+ T cell engraftment in beta2-microglobulin-deficient NOD-scid mice. J Immunol, 158, 3578-86.
  26. De Lord C, Clutterbuck R, Titley J, et al (1991). Growth of primary human acute leukemia in severe combined immunodeficient mice. Exp Hematol, 19, 991.
  27. Dick JE (1996a). Human stem cell assays in immune-deficient mice. Curr Opin Hematol, 3, 405-9. https://doi.org/10.1097/00062752-199603060-00002
  28. Dick JE (1996). Normal and leukemic human stem cells assayed in SCID mice. Semin Immunol, 8, 197-206. https://doi.org/10.1006/smim.1996.0025
  29. Dick JE, Kamel-Reid S, Murdoch B, et al (1991a). Gene transfer into normal human hematopoietic cells using in vitro and in vivo assays. Blood, 78, 624-34.
  30. Dick JE, Lapidot T, Pflumio F (1991b). Transplantation of normal and leukemic human bone marrow into immunedeficient mice: development of animal models for human hematopoiesis. Immunol Rev, 124, 25-43. https://doi.org/10.1111/j.1600-065X.1991.tb00614.x
  31. Estey E, Dohner H (2006). Acute myeloid leukaemia. J Lancet, 368, 1894-907. https://doi.org/10.1016/S0140-6736(06)69780-8
  32. Fell A, Preston P (1993). Proliferation of Theileria annulata and Theileria parva macroschizont-infected bovine cells in scid mice. Int J Parasitol, 23, 77-87. https://doi.org/10.1016/0020-7519(93)90100-D
  33. Feuring-Buske M, Gerhard B, Cashman J, et al (2003). Improved engraftment of human acute myeloid leukemia progenitor cells in beta 2-microglobulin-deficient NOD/SCID mice and in NOD/SCID mice transgenic for human growth factors. Leukemia, 17, 760-3. https://doi.org/10.1038/sj.leu.2402882
  34. Fingert HJ, Chen Z, Mizrahi N, et al (1987). Rapid growth of human cancer cells in a mouse model with fibrin clot subrenal capsule assay. Cancer Res, 47, 3824-9.
  35. Flanagan S (1966). 'Nude', a new hairless gene with pleiotropic effects in the mouse. Genet Res, 8, 295-309. https://doi.org/10.1017/S0016672300010168
  36. Fortier JM, Graubert TA. Murine models of human acute myeloid leukemia. Cancer Treat Res, 2010. p. 183-96.
  37. Fritsche-Polanz R, Fritz M, Huber A, et al (2010). High frequency of concomitant mastocytosis in patients with acute myeloid leukemia exhibiting the transforming< i> KIT mutation D816V. Mol Oncol, 4, 335-46. https://doi.org/10.1016/j.molonc.2010.04.008
  38. Giavazzi R, Berardino CD, Garofalo A, et al (1995). Establishment of human acute myelogenous leukemia lines secreting interleukin-$1\beta$ in SCID mice. Int J Cancer, 61, 280-5. https://doi.org/10.1002/ijc.2910610223
  39. Goan S-R, Fichtner I, Just U, et al (1995). The severe combined immunodeficient-human peripheral blood stem cell (SCIDhuPBSC) mouse: a xenotransplant model for huPBSCinitiated hematopoiesis. Blood, 86, 89-100.
  40. Greiner DL, Shultz LD, Yates J, et al (1995). Improved engraftment of human spleen cells in NOD/LtSz-scid/scid mice as compared with CB-17-scid/scid mice. Am J Pathol, 146, 888-902.
  41. Henschler R, Göttig S, Junghahn I, et al (2005). Transplantation of human acute myeloid leukemia (AML) cells in immunodeficient mice reveals altered cell surface phenotypes and expression of human endothelial markers. Leuk Res, 29, 1191-9. https://doi.org/10.1016/j.leukres.2005.03.019
  42. Ishikawa F, Yoshida S, Saito Y, et al (2007). Chemotherapyresistant human AML stem cells home to and engraft within the bone-marrow endosteal region. Nat Biotechnol, 25, 1315-21. https://doi.org/10.1038/nbt1350
  43. Janssen J, Steenvoorden A, Losekoot M, et al (1987). Novel transforming sequences in human acute myelocytic leukemia cell lines. Oncogene, 1, 175-9.
  44. Kamel-Reid S, Dick JE (1988). Engraftment of immune-deficient mice with human hematopoietic stem cells. Science, 242, 1706-9. https://doi.org/10.1126/science.2904703
  45. Katano I, Ito R, Eto T, et al (2011). Immunodeficient NOD-scid IL-2R$\gamma$ null Mice Do Not Display T and B Cell Leakiness. Exp Anim, 60, 181-6. https://doi.org/10.1538/expanim.60.181
  46. Kato C, Fujii E, Chen YJ, et al (2009). Spontaneous thymic lymphomas in the non-obese diabetic/Shi-scid, IL-2R$\gamma$null mouse. Lab Anim, 43, 402-4. https://doi.org/10.1258/la.2009.009012
  47. Kawano N, Ishikawa F, Shimoda K, et al (2005). Efficient engraftment of primary adult T-cell leukemia cells in newborn NOD/SCID/$\beta2$-microglobulinnull mice. Leukemia, 19, 1384-90. https://doi.org/10.1038/sj.leu.2403829
  48. Kawata A, Yoshida M, Okazaki M, et al (1994). Establishment of new SCID and nude mouse models of human B leukemia/lymphoma and effective therapy of the tumors with immunotoxin and monoclonal antibody: marked difference between the SCID and nude mouse models in the antitumor efficacy of monoclonal antibody. Cancer Res, 54, 2688-94.
  49. Kim JB, O Hare MJ, Stein R (2004). Models of breast cancer: is merging human and animal models the future? Breast Cancer Res, 6, 22-30. https://doi.org/10.1186/bcr841
  50. Kiser M, McCubrey J, Steelman L, et al (2001). Oncogenedependent engraftment of human myeloid leukemia cells in immunosuppressed mice. Leukemia, 15, 814-8. https://doi.org/10.1038/sj.leu.2402084
  51. Kondo M, Horibe K, Takahashi Y, et al (1999). Prognostic value of internal tandem duplication of the FLT3 gene in childhood acute myelogenous leukemia. Med Pediatr Oncol, 33, 525-9. https://doi.org/10.1002/(SICI)1096-911X(199912)33:6<525::AID-MPO1>3.0.CO;2-8
  52. Koyanagi Y, Tanaka Y, Tanaka R, et al (1997). High levels of viremia in hu-PBL-NOD-scid mice with HIV-1 infection. Leukemia, 11, 109-12.
  53. Kudo T, Saijyo S, Saeki H, et al (1993). Production of a human monoclonal antibody to a synthetic peptide by active in vivo immunization using a SCID mouse grafted with human lymphocytes. Tohoku J Exp Med, 171, 327. https://doi.org/10.1620/tjem.171.327
  54. Lapidot T, Fajerman Y, Kollet O (1997). Immune-deficient SCID and NOD/SCID mice models as functional assays for studying normal and malignant human hematopoiesis. J Mol Med, 75, 664-73. https://doi.org/10.1007/s001090050150
  55. Lapidot T, Pflumio F, Doedens M, et al (1992). Cytokine stimulation of multilineage hematopoiesis from immature human cells engrafted in SCID mice. Science, 255, 1137-41. https://doi.org/10.1126/science.1372131
  56. Lapidot T, Sirard C, Vormoor J, et al (1994). A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature, 367, 645-8. https://doi.org/10.1038/367645a0
  57. Li P, Ji M, Park J, et al (2012). Th17 related cytokines in acute myeloid leukemia. Front Biosci, 17, 2284. https://doi.org/10.2741/4052
  58. Liu J, Li Y, Tang L, et al (2007). Treatment of lycorine on SCID mice model with human APL cells. Biomed Pharmacother, 61, 229-34. https://doi.org/10.1016/j.biopha.2007.01.003
  59. Lowenberg B, Downing JR, Burnett A (1999). Acute myeloid leukemia. N Engl J Med, 341, 1051-62. https://doi.org/10.1056/NEJM199909303411407
  60. Lumkul R, Gorin N, Malehorn M, et al (2002). Human AML cells in NOD/SCID mice: engraftment potential and gene expression. Leukemia, 16, 1818-26. https://doi.org/10.1038/sj.leu.2402632
  61. Machado EA, Gerard DA, Lozzio CB, et al (1984). Proliferation and differentiation of human myeloid leukemic cells in immunodeficient mice: electron microscopy and cytochemistry. Blood, 63, 1015-22.
  62. Martin-Padura I, Agliano A, Marighetti P, et al (2010). Sexrelated efficiency in NSG mouse engraftment. Blood, 116, 2616-7. https://doi.org/10.1182/blood-2010-07-295584
  63. Marx J (2003). Mutant stem cells may seed cancer. Science, 301, 1308-10. https://doi.org/10.1126/science.301.5638.1308
  64. Monaco G, Konopleva M, Munsell M, et al (2004). Engraftment of acute myeloid leukemia in NOD/SCID mice is independent of CXCR4 and predicts poor patient survival. Stem Cells, 22, 188-201. https://doi.org/10.1634/stemcells.22-2-188
  65. Mosier DE, Gulizia RJ, Torbett BE, et al (1991). Break for SCIDS. Nature, 353, 509.
  66. Mule JJ, Jicha DL, Rosenberg SA (1992). The use of congenitally immunodeficient mice to study human tumor metastases and immunotherapy. J Immunother, 12, 196-8. https://doi.org/10.1097/00002371-199210000-00011
  67. Na X, He Q, Jiang D (2000). Effect of a novel aminosteroid on animal model of murine myelomonocytic leukemia]. Hunan Yi Ke Da Xue Xue Bao, 25, 12.
  68. Namikawa R, Ueda R, Kyoizumi S (1993). Growth of human myeloid leukemias in the human marrow environment of SCID-hu mice. Blood, 82, 2526-36.
  69. Nara N, Miyamoto T (1982). Direct and serial transplantation of human acute myeloid leukaemia into nude mice. Br J Cancer, 45, 778. https://doi.org/10.1038/bjc.1982.120
  70. Nguyen HQ, Hoffman-Liebermann B, Liebermann DA (1993). The zinc finger transcription factor Egr-1 is essential for and restricts differentiation along the macrophage lineage. Cell, 72, 197-209. https://doi.org/10.1016/0092-8674(93)90660-I
  71. Nicolini F, Cashman J, Hogge D, et al (2003). NOD/SCID mice engineered to express human IL-3, GM-CSF and Steel factor constitutively mobilize engrafted human progenitors and compromise human stem cell regeneration. Leukemia, 18, 341-7.
  72. Nilsson K, Giovanella BC, Stehlin JS, et al (1977). Tumorigenicity of human hematopoietic cell lines in athymic nude mice. Int J Cancer, 19, 337-44. https://doi.org/10.1002/ijc.2910190309
  73. Ninomiya M, Abe A, Katsumi A, et al (2006). Homing, proliferation and survival sites of human leukemia cells in vivo in immunodeficient mice. Leukemia, 21, 136-42.
  74. Nitsche A, Junghahn I, Thulke S, et al (2003). Interleukin-3 promotes proliferation and differentiation of human hematopoietic stem cells but reduces their repopulation potential in NOD/SCID mice. Stem Cells, 21, 236-44. https://doi.org/10.1634/stemcells.21-2-236
  75. Ozpolat B, Lopez-Berestein G, Adamson P, et al (2003). Pharmacokinetics of intravenously administered liposomal all-trans-retinoic acid (ATRA) and orally administered ATRA in healthy volunteers. J Pharm Pharm Sci, 6, 292-301.
  76. Paine-Murrieta GD, Taylor CW, Curtis RA, et al (1997). Human tumor models in the severe combined immune deficient (scid) mouse. Cancer Chemother Pharmacol, 40, 209-14. https://doi.org/10.1007/s002800050648
  77. Palu G, Selby P, Powles R, et al (1979). Spontaneous regression of human acute myeloid leukaemia xenografts and phenotypic evidence for maturation. Br J Cancer, 40, 731. https://doi.org/10.1038/bjc.1979.253
  78. Pearce DJ, Taussig D, Zibara K, et al (2006). AML engraftment in the NOD/SCID assay reflects the outcome of AML: implications for our understanding of the heterogeneity of AML. Blood, 107, 1166-73.
  79. Perez LE, Alpdogan O, Shieh J-H, et al (2004). Increased plasma levels of stromal-derived factor-1 (SDF-1/CXCL12) enhance human thrombopoiesis and mobilize human colony-forming cells (CFC) in NOD/SCID mice. Exp Hematol, 32, 300-7. https://doi.org/10.1016/j.exphem.2003.12.005
  80. Pirruccello SJ, Jackson JD, Sharp JG (1994). The leukemic myeloid cell line OMA-AML-1: an in vitro model of hematopoietic cell differentiation. Leuk Lymphoma, 13, 169-78. https://doi.org/10.3109/10428199409051668
  81. Pollock PL, Germolec DR, Comment CE, et al (1994). Development of human lymphocyte-engrafted SCID mice as a model for immunotoxicity assessment. Toxicol Sci, 22, 130-8. https://doi.org/10.1093/toxsci/22.1.130
  82. Potter G, Shen RN, Chiao J (1984). Nude mice as models for human leukemia studies. Am J Pathol, 114, 360.
  83. Ratajczak MZ, Kant JA, Luger SM, et al (1992). In vivo treatment of human leukemia in a scid mouse model with c-myb antisense oligodeoxynucleotides. Proc Natl Acad Sci, 89, 11823-7. https://doi.org/10.1073/pnas.89.24.11823
  84. Ries L, Melbert D, Krapcho M, et al (2008). SEER cancer statistics review, 1975-2005. Natl Cancer Inst, 1975-2005.
  85. Rombouts W, Blokland I, Lowenberg B, et al (2000a). Biological characteristics and prognosis of adult acute myeloid leukemia with internal tandem duplications in the Flt3 gene. Leukemia, 14, 675-83. https://doi.org/10.1038/sj.leu.2401731
  86. Rombouts W, Martens A, Ploemacher R (2000b). Identification of variables determining the engraftment potential of human acute myeloid leukemia in the immunodeficient NOD/SCID human chimera model. Leukemia, 14, 889-97. https://doi.org/10.1038/sj.leu.2401777
  87. Sanchez P, Perry R, Sarry J, et al (2009). A robust xenotransplantation model for acute myeloid leukemia. Leukemia, 23, 2109-17. https://doi.org/10.1038/leu.2009.143
  88. Sandhu J, Boynton E, Gorczynski R, et al (1996a). The use of SCID mice in biotechnology and as a model for human disease. Crit Rev Biotechnol, 16, 95-118. https://doi.org/10.3109/07388559609146601
  89. Sandhu JS, Clark B, Boynton E, et al (1996b). Human hematopoiesis in SCID mice implanted with human adult cancellous bone. Blood, 88, 1973-82.
  90. Shpitz B, Chambers CA, Brij Singhal A, et al (1994). High level functional engraftment of severe combined immunodeficient mice with human peripheral blood lymphocytes following pretreatment with radiation and anti-asialo G< sub> M1. J Immunol Methods, 169, 1-15. https://doi.org/10.1016/0022-1759(94)90119-8
  91. Shultz LD (1991). Immunological mutants of the mouse. Am J Anat, 191, 303-11. https://doi.org/10.1002/aja.1001910310
  92. Shultz LD, Ishikawa F, Greiner DL (2007). Humanized mice in translational biomedical research. Nat Rev Immunol, 7, 118-30. https://doi.org/10.1038/nri2017
  93. Shultz LD, Lyons BL, Burzenski LM, et al (2005). Human lymphoid and myeloid cell development in NOD/LtSzscid IL2R$\gamma$null mice engrafted with mobilized human hemopoietic stem cells. J Immunol, 174, 6477-89. https://doi.org/10.4049/jimmunol.174.10.6477
  94. Shultz LD, Schweitzer PA, Christianson SW, et al (1995). Multiple defects in innate and adaptive immunologic function in NOD/LtSz-scid mice. J Immunol, 154, 180-91.
  95. Spiegel A, Kollet O, Peled A, et al (2004). Unique SDF-1-induced activation of human precursor-B ALL cells as a result of altered CXCR4 expression and signaling. Blood, 103, 2900-7. https://doi.org/10.1182/blood-2003-06-1891
  96. Tan K-B, Ling L-U, Bunte RM, et al (2012). < i> In vivo efficacy of a novel liposomal formulation of safingol in the treatment of acute myeloid leukemia. J Control Release, 160, 290-8. https://doi.org/10.1016/j.jconrel.2011.11.002
  97. Tavor S, Petit I, Porozov S, et al (2004). CXCR4 regulates migration and development of human acute myelogenous leukemia stem cells in transplanted NOD/SCID mice. Cancer Res, 64, 2817-24. https://doi.org/10.1158/0008-5472.CAN-03-3693
  98. Terpstra W, Leenen P, Van Den Bos C, et al (1997). Facilitated engraftment of human hematopoietic cells in severe combined immunodeficient mice following a single injection of Cl2MDP liposomes. Leukemia, 11, 1049-54. https://doi.org/10.1038/sj.leu.2400694
  99. Terpstra W, Prins A, Visser T, et al (1995). Conditions for engraftment of human acute myeloid leukemia (AML) in SCID mice. Leukemia, 9, 1573-7.
  100. Thacker J, Hogge D (1994). Cytokine-dependent engraftment of human myeloid leukemic cell lines in immunosuppressed nude mice. Leukemia, 8, 871-7.
  101. Trail PA, King DH, Dubowchik GM (2003). Monoclonal antibody drug immunoconjugates for targeted treatment of cancer. Cancer Immunol Immunother, 52, 328-37.
  102. Wang N, Huang L, Wang D, et al (2012). Successful engraftment of human acute lymphoblastic leukemia cells in NOD/SCID mice via intrasplenic inoculation. Cancer Biol Ther, 13, 1158-64. https://doi.org/10.4161/cbt.21345
  103. Watanabe S, Shimosato Y, Kuroki M, et al (1980). Transplantability of human lymphoid cell line, lymphoma, and leukemia in splenectomized and/or irradiated nude mice. Cancer Res, 40, 2588-95.
  104. Woiterski J, Ebinger M, Witte KE, et al (2013). Engraftment of low numbers of pediatric acute lymphoid and myeloid leukemias into NOD/SCID/IL2Rc$\gamma$null mice reflects individual leukemogenecity and highly correlates with clinical outcome. Int J Cancer, 133, 1547-56. https://doi.org/10.1002/ijc.28170
  105. YAMADA M, Midori M, SUGIMURA T (1983). Myeloperoxidases of human myeloid leukemia cells HL-60 grown in culture and in nude mice. J Biochem, 93, 1661-8. https://doi.org/10.1093/oxfordjournals.jbchem.a134306
  106. Yan Y, Salomon O, McGuirk J, et al (1996). Growth pattern and clinical correlation of subcutaneously inoculated human primary acute leukemias in severe combined immunodeficiency mice. Blood, 88, 3137-46.
  107. Yan Y, Wieman EA, Guan X, et al (2009). Autonomous growth potential of leukemia blast cells is associated with poor prognosis in human acute leukemias. J Hematol Oncol, 2, 51. https://doi.org/10.1186/1756-8722-2-51
  108. Zhang S, Zhang Y, Zhuang Y, et al (2012a). Matrine induces apoptosis in human acute myeloid leukemia cells via the mitochondrial pathway and Akt inactivation. PloS One, 7, e46853. https://doi.org/10.1371/journal.pone.0046853
  109. Zhang Y, Patel S, Abdelouahab H, et al (2012b). CXCR4 inhibitors selectively eliminate CXCR4-expressing human acute myeloid leukemia cells in NOG mouse model. Cell Death Dis, 3, e396. https://doi.org/10.1038/cddis.2012.137

Cited by

  1. Elevated Serum Ferritin Levels in Patients with Hematologic Malignancies vol.15, pp.15, 2014, https://doi.org/10.7314/APJCP.2014.15.15.6099