Antigen-specific cytotoxic T lymphocytes can target chemoresistant side-population tumor cells in Hodgkin lymphoma

References

• Evens AM, Hutchings M, Diehl V. Treatment of Hodgkin lymphoma: the past, present, and future. Nat Clin Pract Oncol 2008;5:543–556.
   PubMedGoogle Scholar
• Reis LAG, Melbert D, Krapcho M, et al SEER cancer statistics review, 1975–2005. Bethesda, MD: National Cancer Institute; 2008.
   Google Scholar
• Goodell MA, Brose K, Paradis G, Conner AS, Mulligan RC. Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. J Exp Med 1996;183:1797–1806.
   PubMed Web of Science ®Google Scholar
• Goodell MA, Rosenzweig M, Kim H, et al Dye efflux studies suggest that hematopoietic stem cells expressing low or undetectable levels of CD34 antigen exist in multiple species. Nat Med 1997;3:1337–1345.
   PubMed Web of Science ®Google Scholar
• Wulf GG, Wang RY, Kuehnle I, et al A leukemic stem cell with intrinsic drug efflux capacity in acute myeloid leukemia. Blood 2001;98:1166–1173.
   PubMed Web of Science ®Google Scholar
• Hirschmann-Jax C, Foster AE, Wulf GG, et al A distinct ‘side population’ of cells with high drug efflux capacity in human tumor cells. Proc Natl Acad Sci USA 2004;101:14228–14233.
   PubMed Web of Science ®Google Scholar
• Patrawala L, Calhoun T, Schneider-Broussard R, Zhou J, Claypool K, Tang DG. Side population is enriched in tumorigenic, stem-like cancer cells, whereas ABCG2+ and ABCG2- cancer cells are similarly tumorigenic. Cancer Res 2005;65:6207–6219.
   PubMed Web of Science ®Google Scholar
• Haraguchi N, Utsunomiya T, Inoue H, et al Characterization of a side population of cancer cells from human gastrointestinal system. Stem Cells 2006;24:506–513.
   PubMed Web of Science ®Google Scholar
• Szotek PP, Chang HL, Brennand K, et al Normal ovarian surface epithelial label-retaining cells exhibit stem/progenitor cell characteristics. Proc Natl Acad Sci USA 2008;105:12469–12473.
   PubMed Web of Science ®Google Scholar
• Ho MM, Ng AV, Lam S, Hung JY. Side population in human lung cancer cell lines and tumors is enriched with stem-like cancer cells. Cancer Res 2007;67:4827–4833.
   PubMed Web of Science ®Google Scholar
• Kayo H, Yamazaki H, Nishida H, Dang NH, Morimoto C. Stem cell properties and the side population cells as a target for interferon-alpha in adult T-cell leukemia/lymphoma. Biochem Biophys Res Commun 2007;364:808–814.
   PubMed Web of Science ®Google Scholar
• Matsui W, Wang Q, Barber JP, et al Clonogenic multiple myeloma progenitors, stem cell properties, and drug resistance. Cancer Res 2008;68:190–197.
   PubMed Web of Science ®Google Scholar
• Moshaver B, van Rhenen A, Kelder A, et al Identification of a small subpopulation of candidate leukemia-initiating cells in the side population of patients with acute myeloid leukemia. Stem Cells 2008;26:3059–3067.
   PubMed Web of Science ®Google Scholar
• Bunting KD. ABC transporters as phenotypic markers and functional regulators of stem cells. Stem Cells 2002;20:11–20.
   PubMed Web of Science ®Google Scholar
• Zhou S, Schuetz JD, Bunting KD, et al The ABC transporter Bcrp1/ABCG2 is expressed in a wide variety of stem cells and is a molecular determinant of the side-population phenotype. Nat Med 2001;7:1028–1034.
   PubMed Web of Science ®Google Scholar
• Doyle LA, Yang W, Abruzzo LV, et al A multidrug resistance transporter from human MCF-7 breast cancer cells. Proc Natl Acad Sci USA 1998;95:15665–15670.
   PubMed Web of Science ®Google Scholar
• Bunting KD. ABC transporters as phenotypic markers and functional regulators of stem cells. Stem Cells 2002;20:11–20.
   PubMed Web of Science ®Google Scholar
• Plasschaert SL, de Bont ES, Boezen M, et al Expression of multidrug resistance-associated proteins predicts prognosis in childhood and adult acute lymphoblastic leukemia. Clin Cancer Res 2005;11:8661–8668.
   PubMed Web of Science ®Google Scholar
• Engelmann K, Shen H, Finn OJ. MCF7 side population cells with characteristics of cancer stem/progenitor cells express the tumor antigen MUC1. Cancer Res 2008;1:2419–2126.
   Web of Science ®Google Scholar
• Woodward WA, Chen MS, Behbod F, Alfaro MP, Buchholz TA, Rosen JM. WNT/beta-catenin mediates radiation resistance of mouse mammary progenitor cells. Proc Natl Acad Sci USA 2007;104:618–623.
   PubMed Web of Science ®Google Scholar
• Brossart P, Heinrich KS, Stuhler G, et al Identification of HLA-A2-restricted T-cell epitopes derived from the MUC1 tumor antigen for broadly applicable vaccine therapies. Blood 1999;93:4309–4317.
   PubMed Web of Science ®Google Scholar
• Gong J, Apostolopoulos V, Chen D, et al Selection and characterization of MUC1-specific CD8+ T cells from MUC1 transgenic mice immunized with dendritic-carcinoma fusion cells. Immunology 2000;101:316–324.
   PubMed Web of Science ®Google Scholar
• Bollard CM, Aguilar L, Straathof KC, et al Cytotoxic T lymphocyte therapy for Epstein-Barr virus+ Hodgkin's disease. J Exp Med 2004;200:1623–1633.
   PubMed Web of Science ®Google Scholar
• Bollard CM, Gottschalk S, Leen AM, et al Complete responses of relapsed lymphoma following genetic modification of tumor-antigen presenting cells and T-lymphocyte transfer. Blood 2007;110:2838–2845.
   PubMed Web of Science ®Google Scholar
• Till BG, Jensen MC, Wang J, et al Adoptive immunotherapy for indolent non-Hodgkin lymphoma and mantle cell lymphoma using genetically modified autologous CD20-specific T cells. Blood 2008;112:2261–2271.
   PubMed Web of Science ®Google Scholar
• Bedner E, Smolewski P, Amstad P, Darzynkiewicz Z. Activation of caspases measured in situ by binding of fluorochrome-labeled inhibitors of caspases (FLICA): correlation with DNA fragmentation. Exp Cell Res 2000;259:308–313.
   PubMed Web of Science ®Google Scholar
• Gottschalk S, Edwards OL, Sili U, et al Generating CTLs against the subdominant Epstein-Barr virus LMP1 antigen for the adoptive immunotherapy of EBV-associated malignancies. Blood 2003;101:1905–1912.
   PubMed Web of Science ®Google Scholar
• Chan WC. The Reed-Sternberg cell in classical Hodgkin's disease. Hematol Oncol 2001;19:1–17.
   PubMed Web of Science ®Google Scholar
• Fromm JR, Kussick SJ, Wood BL. Identification and purification of classical Hodgkin cells from lymph nodes by flow cytometry and flow cytometric cell sorting. Am J Clin Pathol 2006;126:764–780.
   PubMed Web of Science ®Google Scholar
• Fromm JR, Thomas A, Wood BL. Flow cytometry can diagnose classical Hodgkin lymphoma in lymph nodes with high sensitivity and specificity. Am J Clin Pathol 2009;131:322–332.
   PubMed Web of Science ®Google Scholar
• Haraguchi N, Utsunomiya T, Inoue H, et al Characterization of a side population of cancer cells from human gastrointestinal system. Stem Cells 2006;24:506–513.
   PubMed Web of Science ®Google Scholar
• Oguri T, Achiwa H, Sato S, et al The determinants of sensitivity and acquired resistance to gemcitabine differ in non-small cell lung cancer: a role of ABCC5 in gemcitabine sensitivity. Mol Cancer Ther 2006;5:1800–1806.
   PubMed Web of Science ®Google Scholar
• Chambost H, Van BN, Brasseur F, et al Expression of gene MAGE-A4 in Reed-Sternberg cells. Blood 2000;95:3530–3533.
   PubMed Web of Science ®Google Scholar
• Colleoni GW, Capodieci P, Tickoo S, Cossman J, Filippa DA, Ladanyi M. Expression of SSX genes in the neoplastic cells of Hodgkin's lymphoma. Hum Pathol 2002;33:496–502.
   PubMed Web of Science ®Google Scholar
• Harris MA, Yang H, Low BE, et al Cancer stem cells are enriched in the side population cells in a mouse model of glioma. Cancer Res 2008;68:10051–10059.
   PubMed Web of Science ®Google Scholar
• Schatton T, Murphy GF, Frank NY, et al Identification of cells initiating human melanomas. Nature 2008;451:345–349.
   PubMed Web of Science ®Google Scholar
• Wang J, Guo LP, Chen LZ, Zeng YX, Lu SH. Identification of cancer stem cell-like side population cells in human nasopharyngeal carcinoma cell line. Cancer Res 2007;67:3716–3724.
   PubMed Web of Science ®Google Scholar
• Wu C, Wei Q, Utomo V, et al Side population cells isolated from mesenchymal neoplasms have tumor initiating potential. Cancer Res 2007;67:8216–8222.
   PubMed Web of Science ®Google Scholar
• Woodward WA, Chen MS, Behbod F, Alfaro MP, Buchholz TA, Rosen JM. WNT/beta-catenin mediates radiation resistance of mouse mammary progenitor cells. Proc Natl Acad Sci USA 2007;104:618–623.
   PubMed Web of Science ®Google Scholar
• Santoro A, Bredenfeld H, Devizzi L, et al Gemcitabine in the treatment of refractory Hodgkin's disease: results of a multicenter phase II study. J Clin Oncol 2000;18:2615–2619.
   PubMed Web of Science ®Google Scholar
• Zinzani PL, Bendandi M, Stefoni V, et al Value of gemcitabine treatment in heavily pretreated Hodgkin's disease patients. Haematologica 2000;85:926–929.
   PubMed Web of Science ®Google Scholar
• Zhou J, Wang CY, Liu T, et al Persistence of side population cells with high drug efflux capacity in pancreatic cancer. World J Gastroenterol 2008;14:925–930.
   PubMed Web of Science ®Google Scholar
• Duxbury MS, Ito H, Benoit E, Waseem T, Ashley SW, Whang EE. A novel role for carcinoembryonic antigen-related cell adhesion molecule 6 as a determinant of gemcitabine chemoresistance in pancreatic adenocarcinoma cells. Cancer Res 2004;64:3987–3993.
   PubMed Web of Science ®Google Scholar
• Bleau AM, Hambardzumyan D, Ozawa T, et al PTEN/PI3K/Akt pathway regulates the side population phenotype and ABCG2 activity in glioma tumor stem-like cells. Cell Stem Cell 2009;4:226–235.
   PubMed Web of Science ®Google Scholar
• Heslop HE, Stevenson FK, Molldrem JJ. Immunotherapy of hematologic malignancy. Hematology Am Soc Hematol Educ Program 2003:331–349.
   PubMedGoogle Scholar
• Kolb HJ. Graft-versus-leukemia effects of transplantation and donor lymphocytes. Blood 2008;112:4371–4383.
   PubMed Web of Science ®Google Scholar
• Doerr JR, Malone CS, Fike FM, et al Patterned CpG methylation of silenced B cell gene promoters in classical Hodgkin lymphoma-derived and primary effusion lymphoma cell lines. J Mol Biol 2005;350:631–640.
   PubMed Web of Science ®Google Scholar
• Melki JR, Clark SJ. DNA methylation changes in leukaemia. Semin Cancer Biol 2002;12:347–357.
   PubMed Web of Science ®Google Scholar
• Serrano A, Tanzarella S, Lionello I, et al Rexpression of HLA class I antigens and restoration of antigen-specific CTL response in melanoma cells following 5-aza-2′-deoxycytidine treatment. Int J Cancer 2001;94:243–251.
   PubMed Web of Science ®Google Scholar
• Maio M, Coral S, Fratta E, Altomonte M, Sigalotti L. Epigenetic targets for immune intervention in human malignancies. Oncogene 2003;22:6484–6488.
   PubMed Web of Science ®Google Scholar
• Sigalotti L, Fratta E, Coral S, et al Intratumor heterogeneity of cancer/testis antigens expression in human cutaneous melanoma is methylation-regulated and functionally reverted by 5-aza-2′-deoxycytidine. Cancer Res 2004;64:9167–9171.
   PubMed Web of Science ®Google Scholar
• Guo ZS, Hong JA, Irvine KR, et al De novo induction of a cancer/testis antigen by 5-aza-2′-deoxycytidine augments adoptive immunotherapy in a murine tumor model. Cancer Res 2006;66:1105–1113.
   PubMed Web of Science ®Google Scholar
• Fonsatti E, Sigalotti L, Coral S, Colizzi F, Altomonte M, Maio M. Methylation-regulated expression of HLA class I antigens in melanoma. Int J Cancer 2003;105:430–431.
   PubMed Web of Science ®Google Scholar
• Woloszynska-Read A, Mhawech-Fauceglia P, Yu J, Odunsi K, Karpf AR. Intertumor and intratumor NY-ESO-1 expression heterogeneity is associated with promoter-specific and global DNA methylation status in ovarian cancer. Clin Cancer Res 2008;14:3283–3290.
   PubMed Web of Science ®Google Scholar
• Hambach L, Ling KW, Pool J, et al Hypomethylating drugs convert HA-1-negative solid tumors into targets for stem cell-based immunotherapy. Blood 2009;113:2715–2722.
   PubMed Web of Science ®Google Scholar
• Gottschalk S, Ng CY, Perez M, et al An Epstein-Barr virus deletion mutant associated with fatal lymphoproliferative disease unresponsive to therapy with virus-specific CTLs. Blood 2001;97:835–843.
   PubMed Web of Science ®Google Scholar