Biomedical Science Letters (대한의생명과학회지)

The Korean Society for Biomedical Laboratory Sciences (대한의생명과학회)
권호 표지
DOI QR코드

DOI QR Code

Humanized (SCID) Mice as a Model to Study human Leukemia

  • Lee, Yoon (Cancer Research Institute, Department of Hematology, Catholic Blood and Marrow Transplantation Center, College of Medicine, The Catholic University of Korea) ;
  • Kim, Donghyun Curt (Northeastern University School of Pharmacy) ;
  • Kim, Hee-Je (Cancer Research Institute, Department of Hematology, Catholic Blood and Marrow Transplantation Center, College of Medicine, The Catholic University of Korea)
  • Received : 2015.06.22
  • Accepted : 2015.06.29
  • Published : 2015.06.30
Download PDF
⟨ Previous Next ⟩

Abstract

A humanized mice (hu-mice) model is extremely valuable to verify human cell activity in vivo condition and is regarded as an important tool in examining multimodal therapies and drug screening in tumor biology. Moreover, hu-mice models that simply received human $CD34^+$ blood cells and tissue transplants are also overwhelmingly useful in immunology and stem cell biology. Because generated hu-mice harboring a human immune system have displayed phenotype of human $CD45^+$ hematopoietic cells and when played partly with functional immune network, it could be used to evaluate human cell properties in vivo. Although the hu-mice model does not completely recapitulate human condition, it is a key methodological factor in studying human hematological malignancies with impaired immune cells. Also, an advanced humanized leukemic mice (hu-leukemic-mice) model has been developed by improving immunodeficient mice. In this review, we briefly described the history of development on immunodeficient SCID strain mice for hu-and hu-leukemic-mice model for immunologic and tumor microenviromental study while inferring the potential benefits of hu-leukemic-mice in cancer biology.

Keywords

References

  1. Ailles LE, Gerhard B, Kawagoe H, Hogge DE. Growth characteristics of acute myelogenous leukemia progenitors that initiate malignant hematopoiesis in nonobese diabetic/severe combined immunodeficient mice. Blood. 1999. 94: 1761-1772.
  2. Ayala F, Dewar R, Kieran M, Kalluri R. Contribution of bone microenvironment to Leukemogenesis and leukemia progression. Leukemia. 2009. 23: 2233-2241. https://doi.org/10.1038/leu.2009.175
  3. Bonnet D, Dick JE. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med. 1997. 3: 730-737. https://doi.org/10.1038/nm0797-730
  4. Bosma GC, Custer RP, Bosma MJ. A severe combined immunodeficiency mutation in the mouse. Nature. 1983. 301: 527-530. https://doi.org/10.1038/301527a0
  5. Boyerinas B, Zafrir M, Yesilkanal AE, Price TT, Hyjek EM, Sipkins DA. Adhesion to osteopontin in the bone marrow niche regulates lymphoblastic leukemia cell dormancy. Blood. 2013. 121: 4821-4831. https://doi.org/10.1182/blood-2012-12-475483
  6. Cao X, Shores EW, Hu-Li J, Anver MR, Kelsall BL, Russell SM, Drago J, Noguchi M, Grinberg A, Bloom ET, Paul WE, Katz SI, Love PE, Leonard WJ. Defective lymphoid development in mice lacking expression of the common cytokine receptor gamma chain. Immunity. 1995. 2: 223-238. https://doi.org/10.1016/1074-7613(95)90047-0
  7. Christianson SW, Greiner DL, Schweitzer IB, Gott B, Beamer GL, Schweitzer PA, Hesselton RM, Shultz LD. Role of natural killer cells on engraftment of human lymphoid cells and on metastasis of human t-lymphoblastoid leukemia cells in c57bl/6j-scid mice and in c57bl/6j-scid bg mice. Cell Immunol. 1996. 171: 186-199.
  8. Cogle CR, Bosse RC, Brewer T, Migdady Y, Shirzad R, Kampen KR, Saki N. Acute myeloid leukemia in the vascular niche. Cancer Lett. 2015. (in press)
  9. De Lord C, Clutterbuck R, Titley J, Ormerod M, Gordon-Smith T, Millar J, Powles R. Growth of primary human acute leukemia in severe combined immunodeficient mice. Exp Hematol. 1991. 19: 991-993.
  10. DiSanto JP, Muller W, Guy-Grand D, Fischer A, Rajewsky K. Lymphoid development in mice with a targeted deletion of the interleukin 2 receptor gamma chain. Proc Natl Acad Sci U S A. 1995. 92: 377-381. https://doi.org/10.1073/pnas.92.2.377
  11. Ferrara F, Schiffer CA. Acute myeloid leukaemia in adults. Lancet. 2013. 381: 484-495. https://doi.org/10.1016/S0140-6736(12)61727-9
  12. Flach J, Bakker ST, Mohrin M, Conroy PC, Pietras EM, Reynaud D, Alvarez S, Diolaiti ME, Ugarte F, Forsberg EC, Le Beau MM, Stohr BA, Mendez J, Morrison CG, Passegue E. Replication stress is a potent driver of functional decline in ageing haematopoietic stem cells. Nature. 2014. 512: 198-202. https://doi.org/10.1038/nature13619
  13. Goldman JP, Blundell MP, Lopes L, Kinnon C, Di Santo JP, Thrasher AJ. Enhanced human cell engraftment in mice deficient in rag2 and the common cytokine receptor gamma chain. Br J Haematol. 1998. 103: 335-342. https://doi.org/10.1046/j.1365-2141.1998.00980.x
  14. Humeau L, Namikawa R, Bardin F, Mannoni P, Roncarolo MG, Chabannon C. Ex vivo manipulations alter the reconstitution potential of mobilized human $CD34^+$ peripheral blood progenitors. Leukemia. 1999. 13: 438-452. https://doi.org/10.1038/sj.leu.2401329
  15. Huntington ND, Legrand N, Alves NL, Jaron B, Weijer K, Plet A, Corcuff E, Mortier E, Jacques Y, Spits H, Di Santo JP. Il-15 trans-presentation promotes human NK cell development and differentiation in vivo. J Exp Med. 2009. 206: 25-34. https://doi.org/10.1084/jem.20082013
  16. Ishikawa F, Yasukawa M, Lyons B, Yoshida S, Miyamoto T, Yoshimoto G, Watanabe T, Akashi K, Shultz LD, Harada M. Development of functional human blood and immune systems in nod/scid/il2 receptor {gamma} chain(null) mice. Blood. 2005. 106: 1565-1573 https://doi.org/10.1182/blood-2005-02-0516
  17. Ishikawa F, Yoshida S, Saito Y, Hijikata A, Kitamura H, Tanaka S, Nakamura R, Tanaka T, Tomiyama H, Saito N, Fukata M, Miyamoto T, Lyons B, Ohshima K, Uchida N, Taniguchi S, Ohara O, Akashi K, Harada M, Shultz LD. Chemotherapyresistant human aml stem cells home to and engraft within the bone-marrow endosteal region. Nat Biotechnol. 2007. 25: 1315-1321. https://doi.org/10.1038/nbt1350
  18. Ito M, Hiramatsu H, Kobayashi K, Suzue K, Kawahata M, Hioki K, Ueyama Y, Koyanagi Y, Sugamura K, Tsuji K, Heike T, Nakahata T. Nod/scid/gamma(c)(null) mouse: An excellent recipient mouse model for engraftment of human cells. Blood. 2002. 100: 3175-3182. https://doi.org/10.1182/blood-2001-12-0207
  19. Jin L, Hope KJ, Zhai Q, Smadja-Joffe F, Dick JE. Targeting of cd44 eradicates human acute myeloid leukemic stem cells. Nat Med. 2006. 12: 1167-1174. https://doi.org/10.1038/nm1483
  20. Jin L, Lee EM, Ramshaw HS, Busfield SJ, Peoppl AG, Wilkinson L, Guthridge MA, Thomas D, Barry EF, Boyd A, Gearing DP, Vairo G, Lopez AF, Dick JE, Lock RB. Monoclonal antibodymediated targeting of cd123, il-3 receptor alpha chain, eliminates human acute myeloid leukemic stem cells. Cell Stem Cell. 2009. 5: 31-42. https://doi.org/10.1016/j.stem.2009.04.018
  21. Kfoury Y, Scadden DT. Mesenchymal cell contributions to the stem cell niche. Cell Stem Cell. 2015. 16: 239-253. https://doi.org/10.1016/j.stem.2015.02.019
  22. Kim JA, Shim JS, Lee GY, Yim HW, Kim TM, Kim M, Leem SH, Lee JW, Min CK, Oh IH. Microenvironmental remodeling as a parameter and prognostic factor of heterogeneous leukemogenesis in acute myelogenous leukemia. Cancer Res. 2015. 75: 2222-2231. https://doi.org/10.1158/0008-5472.CAN-14-3379
  23. Kollet O, Peled A, Byk T, Ben-Hur H, Greiner D, Shultz L, Lapidot T. Beta2 microglobulin-deficient (b2m(null)) nod/scid mice are excellent recipients for studying human stem cell function. Blood. 2000. 95: 3102-3105.
  24. Konopleva M, Konoplev S, Hu W, Zaritskey AY, Afanasiev BV, Andreeff M. Stromal cells prevent apoptosis of aml cells by up-regulation of anti-apoptotic proteins. Leukemia. 2002. 16: 1713-1724. https://doi.org/10.1038/sj.leu.2402608
  25. Lapidot T, Pflumio F, Doedens M, Murdoch B, Williams DE, Dick JE. Cytokine stimulation of multilineage hematopoiesis from immature human cells engrafted in scid mice. Science. 1992. 255: 1137-1141. https://doi.org/10.1126/science.1372131
  26. Lapidot T, Sirard C, Vormoor J, Murdoch B, Hoang T, Caceres-Cortes J, Minden M, Paterson B, Caligiuri MA, Dick JE. A cell initiating human acute myeloid leukaemia after transplantation into scid mice. Nature. 1994. 367: 645-648. https://doi.org/10.1038/367645a0
  27. Lee JY, Park S, Min WS, Kim HJ. Restoration of natural killer cell cytotoxicity by vegfr-3 inhibition in myelogenous leukemia. Cancer Lett. 2014. 354: 281-289. https://doi.org/10.1016/j.canlet.2014.08.027
  28. Lee JY, Park S, Han AR, Lim J, Min WS, Kim HJ. High aldhdimexpressing $CD34^+CD38^-$ cells in leukapheresed peripheral blood is a reliable guide for a successful leukemic xenograft model of acute myeloid leukemia. Oncol Rep. 2014. 32: 1638-1646. https://doi.org/10.3892/or.2014.3359
  29. Lee JY, Kim HJ. (Lymph)angiogenic influences on hematopoietic cells in acute myeloid leukemia. Exp Mol Med. 2014. 46: e122. https://doi.org/10.1038/emm.2014.72
  30. Lion E, Willemen Y, Berneman ZN, Van Tendeloo VF, Smits EL. Natural killer cell immune escape in acute myeloid leukemia. Leukemia. 2012. 26: 2019-2026. https://doi.org/10.1038/leu.2012.87
  31. Lubin I, Faktorowich Y, Lapidot T, Gan Y, Eshhar Z, Gazit E, Levite M, Reisner Y. Engraftment and development of human t and b cells in mice after bone marrow transplantation. Science. 1991. 252: 427-431. https://doi.org/10.1126/science.1826797
  32. Lumkul R, Gorin NC, Malehorn MT, Hoehn GT, Zheng R, Baldwin B, Small D, Gore S, Smith D, Meltzer PS, Civin CI. Human aml cells in nod/scid mice: Engraftment potential and gene expression. Leukemia. 2002. 16: 1818-1826. https://doi.org/10.1038/sj.leu.2402632
  33. McCune JM, Namikawa R, Kaneshima H, Shultz LD, Lieberman M, Weissman IL. The scid-hu mouse: Murine model for the analysis of human hematolymphoid differentiation and function. Science. 1988. 241: 1632-1639. https://doi.org/10.1126/science.2971269
  34. Mercier FE, Ragu C, Scadden DT. The bone marrow at the crossroads of blood and immunity. Nat Rev Immunol. 2012. 12: 49-60. https://doi.org/10.1038/nri3132
  35. Mombaerts P, Iacomini J, Johnson RS, Herrup K, Tonegawa S, Papaioannou VE. Rag-1-deficient mice have no mature b and t lymphocytes. Cell. 1992. 68: 869-877. https://doi.org/10.1016/0092-8674(92)90030-G
  36. Mosier DE, Gulizia RJ, Baird SM, Wilson DB. Transfer of a functional human immune system to mice with severe combined immunodeficiency. Nature. 1988.335:256-259. https://doi.org/10.1038/335256a0
  37. Namikawa R, Kaneshima H, Lieberman M, Weissman IL, McCune JM. Infection of the scid-hu mouse by HIV-1. Science. 1988. 242: 1684-1686. https://doi.org/10.1126/science.3201256
  38. Ohbo K, Suda T, Hashiyama M, Mantani A, Ikebe M, Miyakawa K, Moriyama M, Nakamura M, Katsuki M, Takahashi K, Yamamura K, Sugamura K. Modulation of hematopoiesis in mice with a truncated mutant of the interleukin-2 receptor gamma chain. Blood. 1996. 87: 956-967.
  39. Palu G, Selby P, Powles R, Alexander P. Spontaneous regression of human acute myeloid leukaemia xenografts and phenotypic evidence for maturation. Br J Cancer. 1979. 40: 731-735. https://doi.org/10.1038/bjc.1979.253
  40. Pantelouris EM. Absence of thymus in a mouse mutant. Nature. 1968. 217: 370-371. https://doi.org/10.1038/217370a0
  41. Pearce DJ, Taussig D, Zibara K, Smith LL, Ridler CM, Preudhomme C, Young BD, Rohatiner AZ, Lister TA, Bonnet D. Aml engraftment in the nod/scid assay reflects the outcome of aml: Implications for our understanding of the heterogeneity of aml. Blood. 2006. 107: 1166-1173.
  42. Potter GK, Shen RN, Chiao JW. Nude mice as models for human leukemia studies. Am J Pathol. 1984. 114: 360-366.
  43. Sawyers CL, Gishizky ML, Quan S, Golde DW, Witte ON. Propagation of human blastic myeloid leukemias in the scid mouse. Blood. 1992. 79: 2089-2098.
  44. Shpitz B, Chambers CA, Singhal AB, Hozumi N, Fernandes BJ, Roifman CM, Weiner LM, Roder JC, Gallinger S. High level functional engraftment of severe combined immunodeficient mice with human peripheral blood lymphocytes following pretreatment with radiation and anti-asialo gm1. J Immunol Methods. 1994. 169: 1-15. https://doi.org/10.1016/0022-1759(94)90119-8
  45. Shultz LD, Ishikawa F, Greiner DL. Humanized mice in translational biomedical research. Nat Rev Immunol. 2007. 7: 118-130. https://doi.org/10.1038/nri2017
  46. Shultz LD, Schweitzer PA, Christianson SW, Gott B, Schweitzer IB, Tennent B, McKenna S, Mobraaten L, Rajan TV, Greiner DL, Leiter EH. Multiple defects in innate and adaptive immunologic function in nod/ltsz-scid mice. J Immunol. 1995. 154: 180-191.
  47. Shultz LD, Lyons BL, Burzenski LM, Gott B, Chen X, Chaleff S, Kotb M, Gillies SD, King M, Mangada J, Greiner DL, Handgretinger R. Human lymphoid and myeloid cell development in nod/ltsz-scid il2r gamma null mice engrafted with mobilized human hemopoietic stem cells. J Immunol. 2005. 174: 6477-6489. https://doi.org/10.4049/jimmunol.174.10.6477
  48. Theocharides AP, Jin L, Cheng PY, Prasolava TK, Malko AV, Ho JM, Poeppl AG, van Rooijen N, Minden MD, Danska JS, Dick JE, Wang JC. Disruption of sirpalpha signaling in macrophages eliminates human acute myeloid leukemia stem cells in xenografts. J Exp Med. 2012. 209: 1883-1899. https://doi.org/10.1084/jem.20120502
  49. Zheng J, Umikawa M, Cui C, Li J, Chen X, Zhang C, Huynh H, Kang X, Silvany R, Wan X, Ye J, Canto AP, Chen SH, Wang HY, Ward ES, Zhang CC. Inhibitory receptors bind angptls and support blood stem cells and leukaemia development. Nature. 2012. 485: 656-660. https://doi.org/10.1038/nature11095