Prostate cancer stem cells are targets of both innate and adaptive immunity and elicit tumor-specific immune responses

References

• Siegel R, Naishadham D, Jemal A. Cancer statistics, 2012. CA Cancer J Clin 2012; 62:10 - 29; http://dx.doi.org/10.3322/caac.20138; PMID: 22237781
   PubMed Web of Science ®Google Scholar
• Smith MR, Kaufman D, George D, Oh WK, Kazanis M, Manola J, et al. Selective aromatase inhibition for patients with androgen-independent prostate carcinoma. Cancer 2002; 95:1864 - 8; http://dx.doi.org/10.1002/cncr.10844; PMID: 12404279
   PubMed Web of Science ®Google Scholar
• Tannock IF, de Wit R, Berry WR, Horti J, Pluzanska A, Chi KN, et al, TAX 327 Investigators. Docetaxel plus prednisone or mitoxantrone plus prednisone for advanced prostate cancer. N Engl J Med 2004; 351:1502 - 12; http://dx.doi.org/10.1056/NEJMoa040720; PMID: 15470213
   PubMed Web of Science ®Google Scholar
• Petrylak DP, Tangen CM, Hussain MH, Lara PN Jr., Jones JA, Taplin ME, et al. Docetaxel and estramustine compared with mitoxantrone and prednisone for advanced refractory prostate cancer. N Engl J Med 2004; 351:1513 - 20; http://dx.doi.org/10.1056/NEJMoa041318; PMID: 15470214
   PubMed Web of Science ®Google Scholar
• Antonarakis ES, Eisenberger MA. Expanding treatment options for metastatic prostate cancer. N Engl J Med 2011; 364:2055 - 8; http://dx.doi.org/10.1056/NEJMe1102758; PMID: 21612475
   PubMed Web of Science ®Google Scholar
• Visvader JE, Lindeman GJ. Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat Rev Cancer 2008; 8:755 - 68; http://dx.doi.org/10.1038/nrc2499; PMID: 18784658
   PubMed Web of Science ®Google Scholar
• Kantoff PW, Higano CS, Shore ND, Berger ER, Small EJ, Penson DF, et al, IMPACT Study Investigators. Sipuleucel-T immunotherapy for castration-resistant prostate cancer. N Engl J Med 2010; 363:411 - 22; http://dx.doi.org/10.1056/NEJMoa1001294; PMID: 20818862
   PubMed Web of Science ®Google Scholar
• Di Tomaso T, Mazzoleni S, Wang E, Sovena G, Clavenna D, Franzin A, et al. Immunobiological characterization of cancer stem cells isolated from glioblastoma patients. Clin Cancer Res 2010; 16:800 - 13; http://dx.doi.org/10.1158/1078-0432.CCR-09-2730; PMID: 20103663
   PubMed Web of Science ®Google Scholar
• Brown CE, Starr R, Martinez C, Aguilar B, D’Apuzzo M, Todorov I, et al. Recognition and killing of brain tumor stem-like initiating cells by CD8+ cytolytic T cells. Cancer Res 2009; 69:8886 - 93; http://dx.doi.org/10.1158/0008-5472.CAN-09-2687; PMID: 19903840
   PubMed Web of Science ®Google Scholar
• Pietra G, Manzini C, Vitale M, Balsamo M, Ognio E, Boitano M, et al. Natural killer cells kill human melanoma cells with characteristics of cancer stem cells. Int Immunol 2009; 21:793 - 801; http://dx.doi.org/10.1093/intimm/dxp047; PMID: 19491215
   PubMed Web of Science ®Google Scholar
• Todaro M, D’Asaro M, Caccamo N, Iovino F, Francipane MG, Meraviglia S, et al. Efficient killing of human colon cancer stem cells by gammadelta T lymphocytes. J Immunol 2009; 182:7287 - 96; http://dx.doi.org/10.4049/jimmunol.0804288; PMID: 19454726
   PubMed Web of Science ®Google Scholar
• Pellegatta S, Poliani PL, Corno D, Menghi F, Ghielmetti F, Suarez-Merino B, et al. Neurospheres enriched in cancer stem-like cells are highly effective in eliciting a dendritic cell-mediated immune response against malignant gliomas. Cancer Res 2006; 66:10247 - 52; http://dx.doi.org/10.1158/0008-5472.CAN-06-2048; PMID: 17079441
   PubMed Web of Science ®Google Scholar
• Xu Q, Liu G, Yuan X, Xu M, Wang H, Ji J, et al. Antigen-specific T-cell response from dendritic cell vaccination using cancer stem-like cell-associated antigens. Stem Cells 2009; 27:1734 - 40; http://dx.doi.org/10.1002/stem.102; PMID: 19536809
   PubMed Web of Science ®Google Scholar
• Ning N, Pan Q, Zheng F, Teitz-Tennenbaum S, Egenti M, Yet J, et al. Cancer stem cell vaccination confers significant antitumor immunity. Cancer Res 2012; 72:1853 - 64; http://dx.doi.org/10.1158/0008-5472.CAN-11-1400; PMID: 22473314
   PubMed Web of Science ®Google Scholar
• Collins AT, Berry PA, Hyde C, Stower MJ, Maitland NJ. Prospective identification of tumorigenic prostate cancer stem cells. Cancer Res 2005; 65:10946 - 51; http://dx.doi.org/10.1158/0008-5472.CAN-05-2018; PMID: 16322242
   PubMed Web of Science ®Google Scholar
• Guzmán-Ramírez N, Völler M, Wetterwald A, Germann M, Cross NA, Rentsch CA, et al. In vitro propagation and characterization of neoplastic stem/progenitor-like cells from human prostate cancer tissue. Prostate 2009; 69:1683 - 93; http://dx.doi.org/10.1002/pros.21018; PMID: 19644960
   PubMed Web of Science ®Google Scholar
• Rajasekhar VK, Studer L, Gerald W, Socci ND, Scher HI. Tumour-initiating stem-like cells in human prostate cancer exhibit increased NF-κB signalling. Nat Commun 2011; 2:162; http://dx.doi.org/10.1038/ncomms1159; PMID: 21245843
   PubMed Web of Science ®Google Scholar
• Wang ZA, Shen MM. Revisiting the concept of cancer stem cells in prostate cancer. Oncogene 2011; 30:1261 - 71; http://dx.doi.org/10.1038/onc.2010.530; PMID: 21119602
   PubMed Web of Science ®Google Scholar
• Rietze RL, Reynolds BA. Neural stem cell isolation and characterization. Methods Enzymol 2006; 419:3 - 23; http://dx.doi.org/10.1016/S0076-6879(06)19001-1; PMID: 17141049
   PubMed Web of Science ®Google Scholar
• Galli R, Binda E, Orfanelli U, Cipelletti B, Gritti A, De Vitis S, et al. Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res 2004; 64:7011 - 21; http://dx.doi.org/10.1158/0008-5472.CAN-04-1364; PMID: 15466194
   PubMed Web of Science ®Google Scholar
• Greenberg NM, DeMayo F, Finegold MJ, Medina D, Tilley WD, Aspinall JO, et al. Prostate cancer in a transgenic mouse. Proc Natl Acad Sci U S A 1995; 92:3439 - 43; http://dx.doi.org/10.1073/pnas.92.8.3439; PMID: 7724580
   PubMed Web of Science ®Google Scholar
• Shappell SB, Thomas GV, Roberts RL, Herbert R, Ittmann MM, Rubin MA, et al. Prostate pathology of genetically engineered mice: definitions and classification. The consensus report from the Bar Harbor meeting of the Mouse Models of Human Cancer Consortium Prostate Pathology Committee. Cancer Res 2004; 64:2270 - 305; http://dx.doi.org/10.1158/0008-5472.CAN-03-0946; PMID: 15026373
   PubMed Web of Science ®Google Scholar
• Mazzoleni S, Jachetti E, Morosini S, Grioni M, Piras I, Pala M, et al. Gene signatures distinguish stage-specific prostate cancer stem cells from transgenic adenocarcinoma of the mouse prostate (TRAMP) lesions and predict the malignancy of human tumors.. Stem Cells Trans Med 2013;
   Google Scholar
• Foster BA, Gingrich JR, Kwon ED, Madias C, Greenberg NM. Characterization of prostatic epithelial cell lines derived from transgenic adenocarcinoma of the mouse prostate (TRAMP) model. Cancer Res 1997; 57:3325 - 30; PMID: 9269988
   PubMed Web of Science ®Google Scholar
• Chiaverotti T, Couto SS, Donjacour A, Mao JH, Nagase H, Cardiff RD, et al. Dissociation of epithelial and neuroendocrine carcinoma lineages in the transgenic adenocarcinoma of mouse prostate model of prostate cancer. Am J Pathol 2008; 172:236 - 46; http://dx.doi.org/10.2353/ajpath.2008.070602; PMID: 18156212
   PubMed Web of Science ®Google Scholar
• Huss WJ, Gray DR, Tavakoli K, Marmillion ME, Durham LE, Johnson MA, et al. Origin of androgen-insensitive poorly differentiated tumors in the transgenic adenocarcinoma of mouse prostate model. Neoplasia 2007; 9:938 - 50; http://dx.doi.org/10.1593/neo.07562; PMID: 18030362
   PubMed Web of Science ®Google Scholar
• Mulholland DJ, Xin L, Morim A, Lawson D, Witte O, Wu H. Lin-Sca-1+CD49fhigh stem/progenitors are tumor-initiating cells in the Pten-null prostate cancer model. Cancer Res 2009; 69:8555 - 62; http://dx.doi.org/10.1158/0008-5472.CAN-08-4673; PMID: 19887604
   PubMed Web of Science ®Google Scholar
• Clarke MF, Dick JE, Dirks PB, Eaves CJ, Jamieson CH, Jones DL, et al. Cancer stem cells--perspectives on current status and future directions: AACR Workshop on cancer stem cells. Cancer Res 2006; 66:9339 - 44; http://dx.doi.org/10.1158/0008-5472.CAN-06-3126; PMID: 16990346
   PubMedGoogle Scholar
• Diefenbach A, Jamieson AM, Liu SD, Shastri N, Raulet DH. Ligands for the murine NKG2D receptor: expression by tumor cells and activation of NK cells and macrophages. Nat Immunol 2000; 1:119 - 26; http://dx.doi.org/10.1038/77793; PMID: 11248803
   PubMed Web of Science ®Google Scholar
• Huss WJ, Gray DR, Greenberg NM, Mohler JL, Smith GJ. Breast cancer resistance protein-mediated efflux of androgen in putative benign and malignant prostate stem cells. Cancer Res 2005; 65:6640 - 50; http://dx.doi.org/10.1158/0008-5472.CAN-04-2548; PMID: 16061644
   PubMed Web of Science ®Google Scholar
• Yeh IT, Reddick RL, Kumar AP. Malignancy arising in seminal vesicles in the transgenic adenocarcinoma of mouse prostate (TRAMP) model. Prostate 2009; 69:755 - 60; http://dx.doi.org/10.1002/pros.20924; PMID: 19170049
   PubMed Web of Science ®Google Scholar
• Degl’Innocenti E, Grioni M, Boni A, Camporeale A, Bertilaccio MT, Freschi M, et al. Peripheral T cell tolerance occurs early during spontaneous prostate cancer development and can be rescued by dendritic cell immunization. Eur J Immunol 2005; 35:66 - 75; http://dx.doi.org/10.1002/eji.200425531; PMID: 15597325
   PubMed Web of Science ®Google Scholar
• Garcia-Hernandez MdeL, Gray A, Hubby B, Klinger OJ, Kast WM. Prostate stem cell antigen vaccination induces a long-term protective immune response against prostate cancer in the absence of autoimmunity. Cancer Res 2008; 68:861 - 9; http://dx.doi.org/10.1158/0008-5472.CAN-07-0445; PMID: 18245488
   PubMed Web of Science ®Google Scholar
• Hess Michelini R, Freschi M, Manzo T, Jachetti E, Degl’Innocenti E, Grioni M, et al. Concomitant tumor and minor histocompatibility antigen-specific immunity initiate rejection and maintain remission from established spontaneous solid tumors. Cancer Res 2010; 70:3505 - 14; http://dx.doi.org/10.1158/0008-5472.CAN-09-4253; PMID: 20388780
   PubMed Web of Science ®Google Scholar
• Capobianco A, Manfredi AA, Monno A, Rovere-Querini P, Rugarli C. Melanoma and lymphoma rejection associated with eosinophil infiltration upon intratumoral injection of dendritic and NK/LAK cells. J Immunother 2008; 31:458 - 65; http://dx.doi.org/10.1097/CJI.0b013e318174a512; PMID: 18463539
   PubMed Web of Science ®Google Scholar
• Vesely MD, Kershaw MH, Schreiber RD, Smyth MJ. Natural innate and adaptive immunity to cancer. Annu Rev Immunol 2011; 29:235 - 71; http://dx.doi.org/10.1146/annurev-immunol-031210-101324; PMID: 21219185
   PubMed Web of Science ®Google Scholar
• Ronchetti A, Rovere P, Iezzi G, Galati G, Heltai S, Protti MP, et al. Immunogenicity of apoptotic cells in vivo: role of antigen load, antigen-presenting cells, and cytokines. J Immunol 1999; 163:130 - 6; PMID: 10384108
   PubMed Web of Science ®Google Scholar
• Degl’Innocenti E, Grioni M, Capuano G, Jachetti E, Freschi M, Bertilaccio MT, et al. Peripheral T-cell tolerance associated with prostate cancer is independent from CD4+CD25+ regulatory T cells. Cancer Res 2008; 68:292 - 300; http://dx.doi.org/10.1158/0008-5472.CAN-07-2429; PMID: 18172322
   PubMed Web of Science ®Google Scholar
• Garcia-Hernandez MdeL, Gray A, Hubby B, Kast WM. In vivo effects of vaccination with six-transmembrane epithelial antigen of the prostate: a candidate antigen for treating prostate cancer. Cancer Res 2007; 67:1344 - 51; http://dx.doi.org/10.1158/0008-5472.CAN-06-2996; PMID: 17283172
   PubMed Web of Science ®Google Scholar
• Abou-Kheir WG, Hynes PG, Martin PL, Pierce R, Kelly K. Characterizing the contribution of stem/progenitor cells to tumorigenesis in the Pten-/-TP53-/- prostate cancer model. Stem Cells 2010; 28:2129 - 40; http://dx.doi.org/10.1002/stem.538; PMID: 20936707
   PubMed Web of Science ®Google Scholar
• Zhou Z, Flesken-Nikitin A, Nikitin AY. Prostate cancer associated with p53 and Rb deficiency arises from the stem/progenitor cell-enriched proximal region of prostatic ducts. Cancer Res 2007; 67:5683 - 90; http://dx.doi.org/10.1158/0008-5472.CAN-07-0768; PMID: 17553900
   PubMed Web of Science ®Google Scholar
• Wang X, Kruithof-de Julio M, Economides KD, Walker D, Yu H, Halili MV, et al. A luminal epithelial stem cell that is a cell of origin for prostate cancer. Nature 2009; 461:495 - 500; http://dx.doi.org/10.1038/nature08361; PMID: 19741607
   PubMed Web of Science ®Google Scholar
• Rigamonti N, Bellone M. Prostate cancer, tumor immunity and a renewed sense of optimism in immunotherapy. Cancer Immunol Immunother 2012; 61:453 - 68; http://dx.doi.org/10.1007/s00262-012-1216-6; PMID: 22331081
   PubMed Web of Science ®Google Scholar
• Reiter RE, Gu Z, Watabe T, Thomas G, Szigeti K, Davis E, et al. Prostate stem cell antigen: a cell surface marker overexpressed in prostate cancer. Proc Natl Acad Sci U S A 1998; 95:1735 - 40; http://dx.doi.org/10.1073/pnas.95.4.1735; PMID: 9465086
   PubMed Web of Science ®Google Scholar
• Hubert RS, Vivanco I, Chen E, Rastegar S, Leong K, Mitchell SC, et al. STEAP: a prostate-specific cell-surface antigen highly expressed in human prostate tumors. Proc Natl Acad Sci U S A 1999; 96:14523 - 8; http://dx.doi.org/10.1073/pnas.96.25.14523; PMID: 10588738
   PubMed Web of Science ®Google Scholar
• Yang D, Holt GE, Velders MP, Kwon ED, Kast WM. Murine six-transmembrane epithelial antigen of the prostate, prostate stem cell antigen, and prostate-specific membrane antigen: prostate-specific cell-surface antigens highly expressed in prostate cancer of transgenic adenocarcinoma mouse prostate mice. Cancer Res 2001; 61:5857 - 60; PMID: 11479226
   PubMed Web of Science ®Google Scholar
• Gray A, de la Luz Garcia-Hernandez M, van West M, Kanodia S, Hubby B, Kast WM. Prostate cancer immunotherapy yields superior long-term survival in TRAMP mice when administered at an early stage of carcinogenesis prior to the establishment of tumor-associated immunosuppression at later stages. Vaccine 2009; 27:Suppl 6 G52 - 9; http://dx.doi.org/10.1016/j.vaccine.2009.09.106; PMID: 20006141
   PubMed Web of Science ®Google Scholar
• Uccelli A, Moretta L, Pistoia V. Mesenchymal stem cells in health and disease. Nat Rev Immunol 2008; 8:726 - 36; http://dx.doi.org/10.1038/nri2395; PMID: 19172693
   PubMed Web of Science ®Google Scholar
• Schatton T, Schütte U, Frank NY, Zhan Q, Hoerning A, Robles SC, et al. Modulation of T-cell activation by malignant melanoma initiating cells. Cancer Res 2010; 70:697 - 708; http://dx.doi.org/10.1158/0008-5472.CAN-09-1592; PMID: 20068175
   PubMed Web of Science ®Google Scholar
• Alves PM, Faure O, Graff-Dubois S, Cornet S, Bolonakis I, Gross DA, et al. STEAP, a prostate tumor antigen, is a target of human CD8+ T cells. Cancer Immunol Immunother 2006; 55:1515 - 23; http://dx.doi.org/10.1007/s00262-006-0165-3; PMID: 16622681
   PubMed Web of Science ®Google Scholar
• Thomas-Kaskel AK, Zeiser R, Jochim R, Robbel C, Schultze-Seemann W, Waller CF, et al. Vaccination of advanced prostate cancer patients with PSCA and PSA peptide-loaded dendritic cells induces DTH responses that correlate with superior overall survival. Int J Cancer 2006; 119:2428 - 34; http://dx.doi.org/10.1002/ijc.22097; PMID: 16977630
   PubMed Web of Science ®Google Scholar
• Restifo NP, Dudley ME, Rosenberg SA. Adoptive immunotherapy for cancer: harnessing the T cell response. Nat Rev Immunol 2012; 12:269 - 81; http://dx.doi.org/10.1038/nri3191; PMID: 22437939
   PubMed Web of Science ®Google Scholar
• Mylin LM, Bonneau RH, Lippolis JD, Tevethia SS. Hierarchy among multiple H-2b-restricted cytotoxic T-lymphocyte epitopes within simian virus 40 T antigen. J Virol 1995; 69:6665 - 77; PMID: 7474076
   PubMed Web of Science ®Google Scholar
• Ljunggren HG, Kärre K. Host resistance directed selectively against H-2-deficient lymphoma variants. Analysis of the mechanism. J Exp Med 1985; 162:1745 - 59; http://dx.doi.org/10.1084/jem.162.6.1745; PMID: 3877776
   PubMed Web of Science ®Google Scholar
• Townsend A, Ohlén C, Bastin J, Ljunggren HG, Foster L, Kärre K. Association of class I major histocompatibility heavy and light chains induced by viral peptides. Nature 1989; 340:443 - 8; http://dx.doi.org/10.1038/340443a0; PMID: 2666863
   PubMed Web of Science ®Google Scholar
• Camporeale A, Boni A, Iezzi G, Degl’Innocenti E, Grioni M, Mondino A, et al. Critical impact of the kinetics of dendritic cells activation on the in vivo induction of tumor-specific T lymphocytes. Cancer Res 2003; 63:3688 - 94; PMID: 12839960
   PubMed Web of Science ®Google Scholar
• Granucci F, Zanoni I, Pavelka N, Van Dommelen SL, Andoniou CE, Belardelli F, et al. A contribution of mouse dendritic cell-derived IL-2 for NK cell activation. J Exp Med 2004; 200:287 - 95; http://dx.doi.org/10.1084/jem.20040370; PMID: 15289500
   PubMed Web of Science ®Google Scholar