Immunotherapy of cancer stem cells in solid tumors: Initial findings and future prospective

Expert Opinion on Biological Therapy

Volumn 14, Issue 9, 2014, Pages 1259-1270

  Gammaitoni, Loretta ^a   Leuci, Valeria ^a   Mesiano, Giulia ^a   Giraudo, Lidia ^a,b   Todorovic, Maja ^a   Carnevale Schianca, Fabrizio ^a   Aglietta, Massimo ^a,b   Sangiolo, Dario ^a,b  

^a CANDIOLO CANCER INSTITUTE   (Italy)

^b UNIVERSITY OF TURIN   (Italy)

Author keywords

Cancer immunotherapy; Cancer stem cells; Cell therapy; Solid tumors

Indexed keywords

ADOPTIVE IMMUNOTHERAPY; ANIMAL; CANCER STEM CELL; CYTOKINE INDUCED KILLER CELL; DENDRITIC CELL; HUMAN; IMMUNOLOGY; IMMUNOTHERAPY; MAJOR HISTOCOMPATIBILITY COMPLEX; NATURAL KILLER CELL; NEOPLASMS; PATHOLOGY; PROCEDURES; T LYMPHOCYTE; TRANSPLANTATION; TRENDS;

ANIMALS; CYTOKINE-INDUCED KILLER CELLS; DENDRITIC CELLS; HUMANS; IMMUNOTHERAPY; IMMUNOTHERAPY, ADOPTIVE; KILLER CELLS, NATURAL; MAJOR HISTOCOMPATIBILITY COMPLEX; NEOPLASMS; NEOPLASTIC STEM CELLS; T-LYMPHOCYTES;

EID: 84905814437     PISSN: 14712598     EISSN: 17447682     Source Type: Journal    
DOI: 10.1517/14712598.2014.918099     Document Type: Review

References (120)

1. Visvader JE, Lindeman GJ. Cancer stem cells in solid tumours: Accumulating evidence and unresolved questions. Nat Rev Cancer 2008;8:755-68
2. Virchow R. Cellular-Pathologie. Arch Pathol Anat Physiol Klin Med. 1855;8:3-39
3. Cohnheim J. Congenitales, quergestreiftes Muskelsarkon Der Nireren. Virchows Arch 1875;65:64
4. Durante F. Nesso fisio-pathologico tra la struttura dei nei materni e la genesi di alcuni tumori maligni. Arch Memori Ed Osservazioni Di Chirugia Practica 1874;11:217-26
5. Bruce WR, Van Der Gaag H. A quantitative assay for the number of murine lymphoma cells capable of proliferation in vivo. Nature 1963;199:79-80
6. Lapidot T, Sirard C, Vormoor J, et al. A cell initiating human acute myeloid leukaemia after transplantation into scid mice. Nature 1994;367(6464):645-8
7. Bonnet D, Dick JE. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med 1997;3(7):730-7
8. Al-Hajj M, Wicha MS, Benito-Hernandez A, et al. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 2003;100(7):3983-8
9. Ponti D, Costa A, Zaffaroni N, et al. Isolation and in vitro propagation of tumorigenic breast cancer cells with stem/progenitor cell properties. Cancer Res 2005;65(13):5506-11
10. Kim CF, Jackson EL, Woolfenden AE, et al. Identification of bronchioalveolar stem cells in normal lung and lung cancer. Cell 2005;121(6):823-35
11. Eramo A, Lotti F, Sette G, et al. Identification and expansion of the tumorigenic lung cancer stem cell population. Cell Death Differ 2008;15(3):504-14
12. O'Brien CA, Pollett A, Gallinger S, Dick JE. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 2007;445(7123):106-10
13. Ricci-Vitiani L, Lombardi DG, Pilozzi E, et al. Identification and expansion of human colon-cancer-initiating cells. Nature 2007;445(7123):111-15
14. Collins AT, Berry PA, Hyde C, et al. Prospective identification of tumorigenic prostate cancer stem cells. Cancer Res 2005;65(23):10946-51
15. Szotek PP, Pieretti-Vanmarcke R, Masiakos PT, et al. Ovarian cancer side population defines cells with stem cell-like characteristics and mullerian inhibiting substance responsiveness. Proc Natl Acad Sci USA 2006;103(30):11154-9
16. Zhang S, Balch C, Chan MW, et al. Identification and characterization of ovarian cancer-initiating cells from primary human tumors. Cancer Res 2008;68(11):4311-20
17. Curley MD, Therrien VA, Cummings CL, et al. Cd133 expression defines a tumor initiating cell population in primary human ovarian cancer. Stem Cells 2009;27(12):2875-83
18. Piccirillo SG, Reynolds BA, Zanetti N, et al. Bone morphogenetic proteins inhibit the tumorigenic potential of human brain tumour-initiating cells. Nature 2006;444(7120):761-5
19. Singh SK, Hawkins C, Clarke ID, et al. Identification of human brain tumour initiating cells. Nature 2004;432(7015):396-401
20. Fang D, Nguyen TK, Leishear K, et al. A tumorigenic subpopulation with stem cell properties in melanomas. Cancer Res 2005;65(20):9328-37
21. La Porta C. Cancer stem cells: Lessons from melanoma. Stem Cell Rev 2009;5(1):61-5
22. Quintana E, Shackleton M, Sabel MS, et al. Efficient tumour formation by single human melanoma cells. Nature 2008;456(7222):593-8
23. Malanchi I, Peinado H, Kassen D, et al. Cutaneous cancer stem cell maintenance is dependent on beta-catenin signalling. Nature 2008;452(7187):650-3
24. Prince ME, Sivanandan R, Kaczorowski A, et al. Identification of a subpopulation of cells with cancer stem cell properties in head and neck squamous cell carcinoma. Proc Natl Acad Sci USA 2007;104(3):973-8
25. Li C, Heidt DG, Dalerba P, et al. Identification of pancreatic cancer stem cells. Cancer Res 2007;67(3):1030-7
26. Wilson A, Laurenti E, Oser G, et al. Hematopoietic stem cells reversibly switch from dormancy to self-renewal during homeostasis and repair. Cell 2008;135(6):1118-29
27. Fuchs E. The tortoise and the hair: Slowcycling cells in the stem cell race. Cell 2009;137(5):811-19
28. Clarke MF, Dick JE, Dirks PB, et al. Cancer stem cells-perspectives on current status and future directions: Aacr workshop on cancer stem cells. Cancer Res 2006;66(19):9339-44
29. Li L, Borodyansky L, Yang Y. Genomic instability en route to and from cancer stem cells. Cell Cycle 2009;8(7):1000-2
30. Rapp UR, Ceteci F, Schreck R. Oncogene-induced plasticity and cancer stem cells. Cell Cycle 2008;7(1):45-51
31. Reya T, Morrison SJ, Clarke MF, Weissman IL. Stem cells, cancer, and cancer stem cells. Nature 2001;414(6859):105-11
32. Alison MR, Lim SM, Nicholson LJ. Cancer stem cells: Problems for therapy?. J Pathol 2011;223(2):147-61
33. Calabrese C, Poppleton H, Kocak M, et al. A perivascular niche for brain tumor stem cells. Cancer Cell 2007;11(1):69-82
34. Li L, Neaves WB. Normal stem cells and cancer stem cells: The niche matters. Cancer Res 2006;66(9):4553-7
35. Takaishi S, Okumura T, Tu S, et al. Identification of gastric cancer stem cells using the cell surface marker Cd44. Stem Cells 2009;27(5):1006-20
36. Tirino V, Desiderio V, d'Aquino R, et al. Detection and characterization of Cd133+ cancer stem cells in human solid tumours. PLoS One 2008;3(10):e3469
37. Pearce DJ, Bonnet D. The combined use of hoechst efflux ability and aldehyde dehydrogenase activity to identify murine and human hematopoietic stem cells. Exp Hematol 2007;35(9):1437-46
38. Rybak AP, He L, Kapoor A, et al. Characterization of sphere-propagating cells with stem-like properties from Du145 prostate cancer cells. Biochim Biophys Acta 2011;1813(5):683-94
39. Dean M, Fojo T, Bates S. Tumour stem cells and drug resistance. Nat Rev Cancer 2005;5(4):275-84
40. Suvà ML, Riggi N, Stehle JC, et al. Identification of cancer stem cells in Ewing's sarcoma. Cancer Res 2009;69(5):1776-81
41. Rosen JM, Jordan CT. The increasing complexity of the cancer stem cell paradigm. Science 2009;324(5935):1670-3
42. Tirino V, Desiderio V, Paino F, et al. Cancer stem cells in solid tumors: An overview and new approaches for their isolation and characterization. FASEB J 2013;27(1):13-24
43. Awad O, Yustein JT, Shah P, et al. High Aldh activity identifies chemotherapyresistant ewing's sarcoma stem cells that retain sensitivity to Ews-Fli1 inhibition. PLoS One 2010;5(11):e13943
44. Hu Y, Yu X, Liu S. Cancer stem cells: A shifting subpopulation of cells with stemness?. Med Hypotheses 2013;80(5):649-55
45. La Porta CA. Thoughts about cancer stem cells in solid tumors. World J Stem Cells 2012;4(3):17-20
46. Graham SM, Jørgensen HG, Allan E, et al. Primitive, quiescent, Philadelphiapositive stem cells from patients with chronic myeloid leukemia are insensitive to Sti571 in vitro. Blood 2002;99(1):319-25
47. Januchowski R, Wojtowicz K, Zabel M. The role of aldehyde dehydrogenase (Aldh) in cancer drug resistance. Biomed Pharmacother 2013;67(7):669-80
48. Mohrin M, Bourke E, Alexander D, et al. Hematopoietic stem cell quiescence promotes error-prone DNA repair and mutagenesis. Cell Stem Cell 2010;7(2):174-85
49. Viale A, De Franco F, Orleth A, et al. Cell-cycle restriction limits DNA damage and maintains self-renewal of leukaemia stem cells. Nature 2009;457(7225):51-6
50. 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(39):14228-33
51. 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(9):1028-34
52. Allen JE, Hart LS, Dicker DT, et al. Visualization and enrichment of live putative cancer stem cell populations following P53 inactivation or Bax deletion using non-Toxic fluorescent dyes. Cancer Biol Ther 2009;8(22):2194-205
53. Braut-Boucher F, Pichon J, Rat P, et al. A non-isotopic, highly sensitive, fluorimetric, cell-cell adhesion microplate assay using calcein am-labeled lymphocytes. J Immunol Methods 1995;178(1):41-51
54. Telford WG, Bradford J, Godfrey W, et al. Side population analysis using a violet-excited cell-permeable Dna binding dye. Stem Cells 2007;25(4):1029-36
55. Richichi C, Brescia P, Alberizzi V, et al. Marker-independent method for isolating slow-dividing cancer stem cells in human glioblastoma. Neoplasia 2013;15(7):840-7
56. Salcido CD, Larochelle A, Taylor BJ, et al. Molecular characterisation of side population cells with cancer stem cell-like characteristics in small-cell lung cancer. Br J Cancer 2010;102(11):1636-44
57. Sullivan JP, Spinola M, Dodge M, et al. Aldehyde dehydrogenase activity selects for lung adenocarcinoma stem cells dependent on notch signaling. Cancer Res 2010;70(23):9937-48
58. Vermeulen L, De Sousa e Melo F, Richel DJ, Medema JP. The developing cancer stem-cell model: Clinical challenges and opportunities. Lancet Oncol 2012;13(2):e83-9
59. Kumar SM, Liu S, Lu H, et al. Acquired cancer stem cell phenotypes through Oct4-mediated dedifferentiation. Oncogene 2012;31(47):4898-911
60. Levings PP, McGarry SV, Currie TP, et al. Expression of an exogenous human Oct-4 promoter identifies tumorinitiating cells in osteosarcoma. Cancer Res 2009;69(14):5648-55
61. Chiou SH, Wang ML, Chou YT, et al. Coexpression of Oct4 and nanog enhances malignancy in lung adenocarcinoma by inducing cancer stem cell-like properties and epithelialmesenchymal transdifferentiation. Cancer Res 2010;70(24):10433-44
62. Gerrard L, Zhao D, Clark AJ, Cui W. Stably transfected human embryonic stem cell clones express Oct4-specific green fluorescent protein and maintain self-renewal and pluripotency. Stem Cells 2005;23(1):124-33
63. Gammaitoni L, Giraudo L, Leuci V, et al. Effective activity of cytokineinduced killer cells against autologous metastatic melanoma including cells with stemness features. Clin Cancer Res 2013;19(16):4347-58
64. Sangiolo D, Mesiano G, Gammaitoni L, et al. Cytokine-Induced killer cells eradicate bone and soft-Tissue sarcomas. Cancer Res 2014;74(1):119-29
65. Francipane MG, Chandler J, Lagasse E. Cancer stem cells: A moving target. Curr Pathobiol Rep 2013;1(2):111-18
66. Ashley N. Regulation of intestinal cancer stem cells. Cancer Lett 2013;338(1):120-6
67. Greenberg NM, DeMayo F, Finegold MJ, et al. Prostate cancer in a transgenic mouse. Proc Natl Acad Sci USA 1995;92(8):3439-43
68. Jachetti E, Mazzoleni S, Grioni M, et al. Prostate cancer stem cells are targets of both innate and adaptive immunity and elicit tumor-specific immune responses. Oncoimmunology 2013;2(5):e24520
69. Garcia-Hernandez MeL, Gray A, Hubby B, et al. Prostate stem cell antigen vaccination induces a long-Term protective immune response against prostate cancer in the absence of autoimmunity. Cancer Res 2008;68(3):861-9
70. Gu Z, Thomas G, Yamashiro J, et al. Prostate stem cell antigen (Psca) expression increases with high gleason score, advanced stage and bone metastasis in prostate cancer. Oncogene 2000;19(10):1288-96
71. Bahrenberg G, Brauers A, Joost HG, Jakse G. Reduced expression of Psca, a member of the Ly-6 family of cell surface antigens, in bladder, esophagus, and stomach tumors. Biochem Biophys Res Commun 2000;275(3):783-8
72. Pellegatta S, Poliani PL, Corno D, et al. Neurospheres enriched in cancer stemlike cells are highly effective in eliciting a dendritic cell-mediated immune response against malignant gliomas. Cancer Res 2006;66(21):10247-52
73. Brown CE, Starr R, Martinez C, et al. Recognition and killing of brain tumor stem-like initiating cells by Cd8+cytolytic T cells. Cancer Res 2009;69(23):8886-93
74. Xu Q, Liu G, Yuan X, et al. Antigen-specific T-cell response from dendritic cell vaccination using cancer stem-like cell-Associated antigens. Stem Cells 2009;27(8):1734-40
75. Vik-Mo EO, Nyakas M, Mikkelsen BV, et al. Therapeutic vaccination against autologous cancer stem cells with Mrnatransfected dendritic cells in patients with glioblastoma. Cancer Immunol Immunother 2013;62(9):1499-509
76. Ning N, Pan Q, Zheng F, et al. Cancer stem cell vaccination confers significant antitumor immunity. Cancer Res 2012;72(7):1853-64
77. Di Tomaso T, Mazzoleni S, Wang E, et al. Immunobiological characterization of cancer stem cells isolated from glioblastoma patients. Clin Cancer Res 2010;16(3):800-13
78. Volonté A, Di Tomaso T, Spinelli M, et al. Cancer-initiating cells from colorectal cancer patients escape from T cell-mediated immunosurveillance in vitro through membrane-bound Il-4. J Immunol 2014;192(1):523-32
79. Francipane MG, Alea MP, Lombardo Y, et al. Crucial role of interleukin-4 in the survival of colon cancer stem cells. Cancer Res 2008;68(11):4022-5
80. Deonarain MP, Kousparou CA, Epenetos AA. Antibodies targeting cancer stem cells: A new paradigm in immunotherapy?. MAbs 2009;1(1):12-25
81. Smith LM, Nesterova A, Ryan MC, et al. Cd133/prominin-1 is a potential therapeutic target for antibody-drug conjugates in hepatocellular and gastric cancers. Br J Cancer 2008;99(1):100-9
82. Goel S, Bauer RJ, Desai K, et al. Pharmacokinetic and safety study of subcutaneously administered weekly Ing-1, a human engineered monoclonal antibody targeting human epcam, in patients with advanced solid tumors. Ann Oncol 2007;18(10):1704-7
83. Naundorf S, Preithner S, Mayer P, et al. In vitro and in vivo activity of Mt201, a fully human monoclonal antibody for pancarcinoma treatment. Int J Cancer 2002;100(1):101-10
84. Oberneder R, Weckermann D, Ebner B, et al. A phase I study with adecatumumab, a human antibody directed against epithelial cell adhesion molecule, in hormone refractory prostate cancer patients. Eur J Cancer 2006;42(15):2530-8
85. Folkins C, Man S, Xu P, et al. Anticancer therapies combining antiangiogenic and tumor cell cytotoxic effects reduce the tumor stem-like cell fraction in glioma xenograft tumors. Cancer Res 2007;67(8):3560-4
86. Ottaiano A, di Palma A, Napolitano M, et al. Inhibitory effects of anti-Cxcr4 antibodies on human colon cancer cells. Cancer Immunol Immunother 2005;54(8):781-91
87. Sneddon JB, Werb Z. Location, location, location: The cancer stem cell niche. Cell Stem Cell 2007;1(6):607-11
88. Emlet DR, Gupta P, Holgado-Madruga M, et al. Targeting a glioblastoma cancer stem-cell population defined by Egf receptor variant Iii. Cancer Res 2014;74(4):1238-49
89. Farag SS, Caligiuri MA. Human natural killer cell development and biology. Blood Rev 2006;20(3):123-37
90. Caligiuri MA. Human natural killer cells. Blood 2008;112(3):461-9
91. Moretta L, Moretta A. Unravelling natural killer cell function: Triggering and inhibitory human Nk receptors. EMBO J 2004;23(2):255-9
92. Lanier LL. Up on the tightrope: Natural killer cell activation and inhibition. Nat Immunol 2008;9(5):495-502
93. Tallerico R, Todaro M, Di Franco S, et al. Human Nk cells selective targeting of colon cancer-initiating cells: A role for natural cytotoxicity receptors and Mhc class I molecules. J Immunol 2013;190(5):2381-90
94. Sandel MH, Speetjens FM, Menon AG, et al. Natural killer cells infiltrating colorectal cancer and Mhc class I expression. Mol Immunol 2005;42(4):541-6
95. Jewett A, Tseng HC, Arasteh A, et al. Natural killer cells preferentially target cancer stem cells; role of monocytes in protection against Nk cell mediated lysis of cancer stem cells. Curr Drug Deliv 2012;9(1):5-16
96. Castriconi R, Daga A, Dondero A, et al. Nk cells recognize and kill human glioblastoma cells with stem cell-like properties. J Immunol 2009;182(6):3530-9
97. Pietra G, Manzini C, Vitale M, et al. Natural killer cells kill human melanoma cells with characteristics of cancer stem cells. Int Immunol 2009;21(7):793-801
98. Todaro M, D'Asaro M, Caccamo N, et al. Efficient killing of human colon cancer stem cells by gammadelta T lymphocytes. J Immunol 2009;182(11):7287-96
99. Todaro M, Orlando V, Cicero G, et al. Chemotherapy sensitizes colon cancer initiating cells to Vg9vd2 T cellmediated cytotoxicity. PLoS One 2013;8(6):e65145
100. Constant P, Davodeau F, Peyrat MA, et al. Stimulation of human gamma delta T cells by nonpeptidic mycobacterial ligands. Science 1994;264(5156):267- 70
101. Vermijlen D, Ellis P, Langford C, et al. Distinct cytokine-driven responses of activated blood gammadelta T cells: Insights into unconventional T cell pleiotropy. J Immunol 2007;178(7):4304-14
102. Wesch D, Glatzel A, Kabelitz D. Differentiation of resting human peripheral blood gamma delta T cells toward Th1-or Th2-phenotype. Cell Immunol 2001;212(2):110-17
103. Caccamo N, La Mendola C, Orlando V, et al. Differentiation, phenotype, and function of interleukin-17-producing human Vgamma9vdelta2 T cells. Blood 2011;118(1):129-38
104. Fiore F, Castella B, Nuschak B, et al. Enhanced ability of dendritic cells to stimulate innate and adaptive immunity on short-Term incubation with zoledronic acid. Blood 2007;110(3):921-7
105. Hamilton E, Clay TM, Blackwell KL. New perspectives on zoledronic acid in breast cancer: Potential augmentation of anticancer immune response. Cancer Invest 2011;29(8):533-41
106. Nussbaumer O, Gruenbacher G, Gander H, Thurnher M. Dc-like cell-dependent activation of human natural killer cells by the bisphosphonate zoledronic acid is regulated by gammaelta T lymphocytes. Blood 2011;118(10):2743-51
107. Coscia M, Quaglino E, Iezzi M, et al. Zoledronic acid repolarizes tumourassociated macrophages and inhibits mammary carcinogenesis by targeting the mevalonate pathway. J Cell Mol Med 2010;14(12):2803-15
108. Mesiano G, Todorovic M, Gammaitoni L, et al. Cytokine-induced killer (Cik) cells as feasible and effective adoptive immunotherapy for the treatment of solid tumors. Expert Opin Biol Ther 2012;12(6):673-84
109. Schmidt-Wolf IG, Lefterova P, Mehta BA, et al. Phenotypic characterization and identification of effector cells involved in tumor cell recognition of cytokine-induced killer cells. Exp Hematol 1993;21(13):1673-9
110. Lu PH, Negrin RS. A novel population of expanded human Cd3+Cd56+ cells derived from T cells with potent in vivo antitumor activity in mice with severe combined immunodeficiency. J Immunol 1994;153(4):1687-96
111. Baker J, Verneris MR, Ito M, et al. Expansion of cytolytic Cd8(+) natural killer T cells with limited capacity for graft-versus-host disease induction due to interferon gamma production. Blood 2001;97(10):2923-31
112. Verneris MR, Karami M, Baker J, et al. Role of Nkg2d signaling in the cytotoxicity of activated and expanded Cd8+ T cells. Blood 2004;103(8):3065-72
113. Topalian SL, Hodi FS, Brahmer JR, et al. Safety, activity, and immune correlates of anti-Pd-1 antibody in cancer. N Engl J Med 2012;366(26):2443-54
114. Wolchok JD, Neyns B, Linette G, et al. Ipilimumab monotherapy in patients with pretreated advanced melanoma: A randomised, double-blind, multicentre, phase 2, dose-ranging study. Lancet Oncol 2010;11(2):155-64
115. Rizzo P, Osipo C, Foreman K, et al. Rational targeting of notch signaling in cancer. Oncogene 2008;27(38):5124-31
116. De Sousa EM, Vermeulen L, Richel D, Medema JP. Targeting Wnt signaling in colon cancer stem cells. Clin Cancer Res 2011;17(4):647-53
117. Korkaya H, Kim GI, Davis A, et al. Activation of an Il6 inflammatory loop mediates trastuzumab resistance in Her2+breast cancer by expanding the cancer stem cell population. Mol Cell 2012;47(4):570-84
118. Morgan RA, Yang JC, Kitano M, et al. Case report of a serious adverse event following the administration of T cells transduced with a chimeric antigen receptor recognizing Erbb2. Mol Ther 2010;18(4):843-51
119. Leuci V, Mesiano G, Gammaitoni L, et al. Genetically redirected T lymphocytes for adoptive immunotherapy of solid tumors. Curr Gene Ther 2014;14(1):52-62
120. Linette GP, Stadtmauer EA, Maus MV, et al. Cardiovascular toxicity and titin cross-reactivity of affinity-enhanced T cells in myeloma and melanoma. Blood 2013;122(6):863-71