Cytokine & Growth Factor Reviews
Volume 21, Issue 2 , Pages 169-175 , April 2010

Oncolytic viral purging of leukemic hematopoietic stem and progenitor cells with Myxoma virus

  • Masmudur M. Rahman

      Affiliations

    • Department of Molecular Genetics and Microbiology, University of Florida, Gainesville, FL 32610, USA
    • ,
  • Gerard J. Madlambayan

      Affiliations

    • Division of Hematology/Oncology, Department of Medicine, University of Florida, Gainesville, FL 32610, USA
    • ,
  • Christopher R. Cogle

      Affiliations

    • Division of Hematology/Oncology, Department of Medicine, University of Florida, Gainesville, FL 32610, USA
    • ,
  • Grant McFadden

      Affiliations

    • Department of Molecular Genetics and Microbiology, University of Florida, Gainesville, FL 32610, USA
    • Corresponding Author InformationCorresponding author at: Department of Molecular Genetics and Microbiology, College of Medicine, University of Florida, 1600 SW Archer Road, PO Box 100266, Gainesville, FL 32610, USA. Tel.: +1 352 273 6852; fax: +1 352 273 6849.

References 

  1. Kvalheim G. Purging of autografts: methods and clinical significance. Ann Med. 1996;28:167–173
  2. Gribben JG, Nadler LM. Bone marrow purging for autologous bone marrow transplantation. Leuk Lymphoma. 1993;11(Suppl. 2):141–148
  3. Rill DR, Santana VM, Roberts WM, et al. Direct demonstration that autologous bone marrow transplantation for solid tumors can return a multiplicity of tumorigenic cells. Blood. 1994;84:380–383
  4. Motta MR, Mangianti S, Rizzi S, et al. Pharmacological purging of minimal residual disease from peripheral blood stem cell collections of acute myeloblastic leukemia patients: preclinical studies. Exp Hematol. 1997;25:1261–1269
  5. Strauss G, Westhoff MA, Fischer-Posovszky P, et al. 4-hydroperoxy-cyclophosphamide mediates caspase-independent T-cell apoptosis involving oxidative stress-induced nuclear relocation of mitochondrial apoptogenic factors AIF and EndoG. Cell Death Differ. 2008;15:332–343
  6. Abonour R, Scott KM, Kunkel LA, et al. Autologous transplantation of mobilized peripheral blood CD34+ cells selected by immunomagnetic procedures in patients with multiple myeloma. Bone Marrow Transplant. 1998;22:957–963
  7. Spyridonidis A, Schmidt M, Bernhardt W, et al. Purging of mammary carcinoma cells during ex vivo culture of CD34+ hematopoietic progenitor cells with recombinant immunotoxins. Blood. 1998;91:1820–1827
  8. Gee A, Moss T, Mansour V, et al. Large-scale immunomagnetic separation system for the removal of tumor cells from bone marrow. Prog Clin Biol Res. 1992;377:181–187
  9. Thirukkumaran CM, Russell JA, Stewart DA, Morris DG. Viral purging of haematological autografts: should we sneeze on the graft?. Bone Marrow Transplant. 2007;40:1–12
  10. Stewart AK, Vescio R, Schiller G, et al. Purging of autologous peripheral-blood stem cells using CD34 selection does not improve overall or progression-free survival after high-dose chemotherapy for multiple myeloma: results of a multicenter randomized controlled trial. J Clin Oncol. 2001;19:3771–3779
  11. Kvalheim G, Wang MY, Pharo A, et al. Purging of tumor cells from leukapheresis products: experimental and clinical aspects. J Hematother. 1996;5:427–436
  12. Zhong RK, Donnenberg AD, Rubin J, Ball ED. Differential effect of 4-hydroperoxycyclophosphamide and antimyeloid monoclonal antibodies on T and natural killer cells during bone marrow purging. Blood. 1994;83:2345–2351
  13. Shimoni A, Korbling M. Tumor cell contamination in re-infused stem cell autografts: does it have clinical significance?. Crit Rev Oncol Hematol. 2002;41:241–250
  14. Cripe TP, Wang PY, Marcato P, Mahller YY, Lee PW. Targeting cancer-initiating cells with oncolytic viruses. Mol Ther. 2009;17:1677–1682
  15. Liu TC, Galanis E, Kirn D. Clinical trial results with oncolytic virotherapy: a century of promise, a decade of progress. Nat Clin Pract Oncol. 2007;4:101–117
  16. Roberts MS, Lorence RM, Groene WS, Bamat MK. Naturally oncolytic viruses. Curr Opin Mol Ther. 2006;8:314–321
  17. Khuri FR, Nemunaitis J, Ganly I, et al. A controlled trial of intratumoral ONYX-015, a selectively-replicating adenovirus, in combination with cisplatin and 5-fluorouracil in patients with recurrent head and neck cancer. Nat Med. 2000;6:879–885
  18. Garber K. China approves world's first oncolytic virus therapy for cancer treatment. J Natl Cancer Inst. 2006;98:298–300
  19. Liu TC, Kirn D. Systemic efficacy with oncolytic virus therapeutics: clinical proof-of-concept and future directions. Cancer Res. 2007;67:429–432
  20. Mastrangelo MJ, Maguire HC, Eisenlohr LC, et al. Intratumoral recombinant GM-CSF-encoding virus as gene therapy in patients with cutaneous melanoma. Cancer Gene Ther. 1999;6:409–422
  21. Freytag SO, Khil M, Stricker H, et al. Phase I study of replication-competent adenovirus-mediated double suicide gene therapy for the treatment of locally recurrent prostate cancer. Cancer Res. 2002;62:4968–4976
  22. Hu JC, Booth MJ, Tripuraneni G, et al. A novel HSV-1 virus, JS1/34.5-/47-, purges contaminating breast cancer cells from bone marrow. Clin Cancer Res. 2006;12:6853–6862
  23. Wu A, Mazumder A, Martuza RL, et al. Biological purging of breast cancer cells using an attenuated replication-competent herpes simplex virus in human hematopoietic stem cell transplantation. Cancer Res. 2001;61:3009–3015
  24. Lichty BD, Stojdl DF, Taylor RA, et al. Vesicular stomatitis virus: a potential therapeutic virus for the treatment of hematologic malignancy. Hum Gene Ther. 2004;15:821–831
  25. Thirukkumaran CM, Luider JM, Stewart DA, et al. Reovirus oncolysis as a novel purging strategy for autologous stem cell transplantation. Blood. 2003;102:377–387
  26. Thirukkumaran CM, Luider JM, Stewart DA, et al. Biological purging of breast cancer cell lines using a replication-competent oncolytic virus in human stem cell autografts. Bone Marrow Transplant. 2005;35:1055–1064
  27. Lillo R, Ramirez M, Alvarez A, et al. Efficient and nontoxic adenoviral purging method for autologous transplantation in breast cancer patients. Cancer Res. 2002;62:5013–5018
  28. Wagner LM, Guichard SM, Burger RA, et al. Efficacy and toxicity of a virus-directed enzyme prodrug therapy purging method: preclinical assessment and application to bone marrow samples from neuroblastoma patients. Cancer Res. 2002;62:5001–5007
  29. Wolff G, Korner IJ, Schumacher A, Arnold W, Dorken B, Mapara MY. Ex vivo breast cancer cell purging by adenovirus-mediated cytosine deaminase gene transfer and short-term incubation with 5-fluorocytosine completely prevents tumor growth after transplantation. Hum Gene Ther. 1998;9:2277–2284
  30. Kirn DH, Thorne SH. Targeted and armed oncolytic poxviruses: a novel multi-mechanistic therapeutic class for cancer. Nat Rev Cancer. 2009;9:64–71
  31. Shen Y, Nemunaitis J. Fighting cancer with vaccinia virus: teaching new tricks to an old dog. Mol Ther. 2005;11:180–195
  32. Thorne SH, Bartlett DL, Kirn DH. The use of oncolytic vaccinia viruses in the treatment of cancer: a new role for an old ally?. Curr Gene Ther. 2005;5:429–443
  33. Worschech A, Haddad D, Stroncek DF, Wang E, Marincola FM, Szalay AA. The immunologic aspects of poxvirus oncolytic therapy. Cancer Immunol Immunother. 2009;58:1355–1362
  34. Gilbert PA, McFadden G. Poxvirus cancer therapy. Recent Pat Antiinfect Drug Discov. 2006;1:309–321
  35. Guo ZS, Thorne SH, Bartlett DL. Oncolytic virotherapy: molecular targets in tumor-selective replication and carrier cell-mediated delivery of oncolytic viruses. Biochim Biophys Acta. 2008;1785:217–231
  36. McFadden G. Poxvirus tropism. Nat Rev Microbiol. 2005;3:201–213
  37. Mercer J, Helenius A. Vaccinia virus uses macropinocytosis and apoptotic mimicry to enter host cells. Science. 2008;320:531–535
  38. Moss B. Poxvirus entry and membrane fusion. Virology. 2006;344:48–54
  39. Putz MM, Midgley CM, Law M, Smith GL. Quantification of antibody responses against multiple antigens of the two infectious forms of Vaccinia virus provides a benchmark for smallpox vaccination. Nat Med. 2006;12:1310–1315
  40. Vora S, Damon I, Fulginiti V, et al. Severe eczema vaccinatum in a household contact of a smallpox vaccinee. Clin Infect Dis. 2008;46:1555–1561
  41. Stanford MM, McFadden G. Myxoma virus and oncolytic virotherapy: a new biologic weapon in the war against cancer. Expert Opin Biol Ther. 2007;7:1415–1425
  42. Fenner F. Adventures with poxviruses of vertebrates. FEMS Microbiol Rev. 2000;24:123–133
  43. Stanford MM, Werden SJ, McFadden G. Myxoma virus in the European rabbit: interactions between the virus and its susceptible host. Vet Res. 2007;38:299–318
  44. Barrett JW, Cao JX, Hota-Mitchell S, McFadden G. Immunomodulatory proteins of myxoma virus. Semin Immunol. 2001;13:73–84
  45. Kerr P, McFadden G. Immune responses to myxoma virus. Viral Immunol. 2002;15:229–246
  46. Zuniga MC. A pox on thee! Manipulation of the host immune system by myxoma virus and implications for viral-host co-adaptation. Virus Res. 2002;88:17–33
  47. Wang F, Ma Y, Barrett JW, et al. Disruption of Erk-dependent type I interferon induction breaks the myxoma virus species barrier. Nat Immunol. 2004;5:1266–1274
  48. Wang F, Gao X, Barrett JW, et al. RIG-I mediates the co-induction of tumor necrosis factor and type I interferon elicited by myxoma virus in primary human macrophages. PLoS Pathog. 2008;4:e1000099
  49. Bartee E, Mohamed MR, Lopez MC, Baker HV, McFadden G. The addition of tumor necrosis factor plus beta interferon induces a novel synergistic antiviral state against poxviruses in primary human fibroblasts. J Virol. 2009;83:498–511
  50. Sypula J, Wang F, Ma Y, Bell J, McFadden G. Myxoma virus tropism in human tumor cells. Gene Ther Mol Biol. 2004;8:103–114
  51. Bartee E, McFadden G. Human cancer cells have specifically lost the ability to induce the synergistic state caused by tumor necrosis factor plus interferon-beta. Cytokine. 2009;47:199–205
  52. Wang G, Barrett JW, Stanford M, et al. Infection of human cancer cells with myxoma virus requires Akt activation via interaction with a viral ankyrin-repeat host range factor. Proc Natl Acad Sci USA. 2006;103:4640–4645
  53. Stanford MM, Shaban M, Barrett JW, et al. Myxoma virus oncolysis of primary and metastatic B16F10 mouse tumors in vivo. Mol Ther. 2008;16:52–59
  54. Tokunaga E, Oki E, Egashira A, et al. Deregulation of the Akt pathway in human cancer. Curr Cancer Drug Targets. 2008;8:27–36
  55. Werden SJ, McFadden G. The role of cell signaling in poxvirus tropism: the case of the M-T5 host range protein of myxoma virus. Biochim Biophys Acta. 2008;1784:228–237
  56. Stanford MM, Barrett JW, Nazarian SH, Werden S, McFadden G. Oncolytic virotherapy synergism with signaling inhibitors: Rapamycin increases myxoma virus tropism for human tumor cells. J Virol. 2007;81:1251–1260
  57. Lun XQ, Zhou H, Alain T, et al. Targeting human medulloblastoma: oncolytic virotherapy with myxoma virus is enhanced by rapamycin. Cancer Res. 2007;67:8818–8827
  58. Katsafanas GC, Moss B. Vaccinia virus intermediate stage transcription is complemented by Ras-GTPase-activating protein SH3 domain-binding protein (G3BP) and cytoplasmic activation/proliferation-associated protein (p137) individually or as a heterodimer. J Biol Chem. 2004;279:52210–52217
  59. Yang H, Kim SK, Kim M, et al. Antiviral chemotherapy facilitates control of poxvirus infections through inhibition of cellular signal transduction. J Clin Invest. 2005;115:379–387
  60. Soares JA, Leite FG, Andrade LG, et al. Activation of the PI3K/Akt pathway early during vaccinia and cowpox virus infections is required for both host survival and viral replication. J Virol. 2009;83:6883–6899
  61. Lun X, Yang W, Alain T, et al. Myxoma virus is a novel oncolytic virus with significant antitumor activity against experimental human gliomas. Cancer Res. 2005;65:9982–9990
  62. Wu Y, Lun X, Zhou H, et al. Oncolytic efficacy of recombinant vesicular stomatitis virus and myxoma virus in experimental models of rhabdoid tumors. Clin Cancer Res. 2008;14:1218–1227
  63. Fenner F, Ratcliffe F. Myxomatosis. Cambridge: University Press; 1965;
  64. Barrett JW, Alston LR, Wang F, et al. Identification of host range mutants of myxoma virus with altered oncolytic potential in human glioma cells. J Neurovirol. 2007;13:549–560
  65. Kim M, Madlambayan GJ, Rahman MM, et al. Myxoma virus targets primary human leukemia stem and progenitor cells while sparing normal hematopoietic stem and progenitor cells. Leukemia. 2009;23:2313–2317
  66. Kiyoi H, Naoe T, Nakano Y, et al. Prognostic implication of FLT3 and N-RAS gene mutations in acute myeloid leukemia. Blood. 1999;93:3074–3080
  67. Thiede C, Steudel C, Mohr B, et al. Analysis of FLT3-activating mutations in 979 patients with acute myelogenous leukemia: association with FAB subtypes and identification of subgroups with poor prognosis. Blood. 2002;99:4326–4335
  68. Schnittger S, Schoch C, Dugas M, et al. Analysis of FLT3 length mutations in 1003 patients with acute myeloid leukemia: correlation to cytogenetics, FAB subtype, and prognosis in the AMLCG study and usefulness as a marker for the detection of minimal residual disease. Blood. 2002;100:59–66
  69. Martelli AM, Nyakern M, Tabellini G, et al. Phosphoinositide 3-kinase/Akt signaling pathway and its therapeutical implications for human acute myeloid leukemia. Leukemia. 2006;20:911–928
  70. Shpall EJ, Jones RB, Bast RC, et al. 4-Hydroperoxycyclophosphamide purging of breast cancer from the mononuclear cell fraction of bone marrow in patients receiving high-dose chemotherapy and autologous marrow support: a phase I trial. J Clin Oncol. 1991;9:85–93
  71. Cheson BD. Monoclonal antibody therapy for B-cell malignancies. Semin Oncol. 2006;33:S2–S14
  72. Mohr M, Dalmis F, Hilgenfeld E, et al. Simultaneous immunomagnetic CD34+ cell selection and B-cell depletion in peripheral blood progenitor cell samples of patients suffering from B-cell non-Hodgkin's lymphoma. Clin Cancer Res. 2001;7:51–57
  73. Goggins TF, Chao N. Depletion of host reactive T cells by photodynamic cell purging and prevention of graft versus host disease. Leuk Lymphoma. 2003;44:1871–1879
  74. Keir M, Fiddes R, Biggs JC, Kearney PP. Sensitivity of c-erbB positive cells to a ligand toxin and its utility in purging breast cancer cells from peripheral blood stem cell (PBSC) collections. Stem Cells. 2000;18:422–427
  75. Carella AM, Lerma E, Corsetti MT, et al. Autografting with philadelphia chromosome-negative mobilized hematopoietic progenitor cells in chronic myelogenous leukemia. Blood. 1999;93:1534–1539
  76. Bhatia S, Sather HN, Heerema NA, Trigg ME, Gaynon PS, Robison LL. Racial and ethnic differences in survival of children with acute lymphoblastic leukemia. Blood. 2002;100:1957–1964

PII: S1359-6101(10)00021-3

doi: 10.1016/j.cytogfr.2010.02.010

Cytokine & Growth Factor Reviews
Volume 21, Issue 2 , Pages 169-175 , April 2010

Article Tools