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

OncoImmunology

Volumn 2, Issue 5, 2013, Pages

  Jachetti, Elena ^a   Mazzoleni, Stefania ^a   Grioni, Matteo ^a   Ricupito, Alessia ^a   Brambillasca, Chiara ^a,b   Generoso, Luca ^a   Calcinotto, Arianna ^a,b   Freschi, Massimo ^a   Mondino, Anna ^a   Galli, Rossella ^a   Bellone, Matteo ^a  

^a SAN RAFFAELE HOSPITAL   (Italy)

^b VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

Author keywords

Cancer stem cells; Dendritic cell; Prostate cancer; Tumor immunity; Vaccination

Indexed keywords

DENDRITIC CELL VACCINE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; NATURAL KILLER CELL RECEPTOR;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN EXPRESSION; ARTICLE; CANCER INHIBITION; CANCER STEM CELL; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; DENDRITIC CELL; EMBRYO; FEMALE; IMMUNIZATION; IN VITRO STUDY; IN VIVO STUDY; INNATE IMMUNITY; LYMPHOCYTE FUNCTION; MALE; MOUSE; NATURAL KILLER CELL; NONHUMAN; PANCREATIC NEUROENDOCRINE TUMOR; PHENOTYPE; PROSTATE ADENOCARCINOMA; TUMOR IMMUNITY;

EID: 84880438429     PISSN: 21624011     EISSN: 2162402X     Source Type: Journal    
DOI: 10.4161/onci.24520     Document Type: Article

References (57)

1. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2012. CA Cancer J Clin 2012; 62:10-29; PMID:22237781;http://dx.doi.org/10.3322/caac.20138
2. 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; PMID:12404279; http://dx.doi.org/10.1002/cncr.10844
3. Tannock I F, 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; PMID:15470213; http://dx.doi. org/10.1056/NEJMoa040720
4. Petrylak D P, Tangen CM, Hussain MH, Lara PN Jr., Jones JA, Taplin ME, et al. Docetaxel and estramus-tine compared with mitoxantrone and prednisone for advanced refractory prostate cancer. N Engl J Med 2004; 351:1513-20; PMID:15470214; http://dx.doi. org/10.1056/NEJMoa041318
5. Antonarakis ES, Eisenberger MA. Expanding treatment options for metastatic prostate cancer. N Engl J Med 2011; 364:2055-8; PMID:21612475; http://dx.doi. org/10.1056/NEJMe1102758
6. Visvader JE, Lindeman GJ. Cancer stem cells in solid tumours: accumulating evidence and unre-solved questions. Nat Rev Cancer 2008; 8:755-68; PMID:18784658; http://dx.doi.org/10.1038/nrc2499
7. KantoffPW, Higano CS, Shore ND, Berger ER, Small EJ, Penson D F, et al.; IMPACT Study Investigators. Sipuleucel-T immunotherapy for castration-resistant prostate cancer. N Engl J Med 2010; 363:411-22; PMID:20818862;http://dx.doi.org/10.1056/NEJMoa1001294
8. Di Tomaso T, Mazzoleni S, Wang E, Sovena G, Clavenna D, Franzin A, et al. Immunobiological characterization of cancer stem cells isolated from glio-blastoma patients. Clin Cancer Res 2010; 16:800-13; PMID:20103663; http://dx.doi.org/10.1158/1078-0432.CCR-09-2730
9. 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; PMID:19903840; http://dx.doi.org/10.1158/0008-5472.CAN-09-2687
10. 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; PMID:19491215; http://dx.doi.org/10.1093/intimm/dxp047
11. Todaro M, D'Asaro M, Caccamo N, Iovino F, Francipane MG, Meraviglia S, et al. Efficient killing of human colon cancer stem cells by gammad-elta T lymphocytes. J Immunol 2009; 182:7287-96; PMID:19454726; http://dx.doi.org/10.4049/jimmu-nol.0804288
12. 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; PMID:17079441; http://dx.doi.org/10.1158/0008-5472.CAN-06-2048
13. 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; PMID:19536809; http://dx.doi.org/10.1002/stem.102
14. 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; PMID:22473314; http://dx.doi. org/10.1158/0008-5472.CAN-11-1400
15. Collins AT, Berry PA, Hyde C, Stower MJ, Maitland NJ. Prospective identification of tumorigenic prostate cancer stem cells. Cancer Res 2005; 65:10946-51; PMID:16322242; http://dx.doi.org/10.1158/0008-5472.CAN-05-2018
16. Guzmàn-Ramìrez 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; PMID:19644960; http://dx.doi.org/10.1002/pros.21018
17. Rajasekhar VK, Studer L, Gerald W, Socci ND, Scher HI. Tumour-initiating stem-like cells in human prostate cancer exhibit increased NF-?B signalling. Nat Commun 2011; 2:162; PMID:21245843; http://dx.doi.org/10.1038/ncomms1159
18. Wang ZA, Shen MM. Revisiting the concept of cancer stem cells in prostate cancer. Oncogene 2011; 30:1261-71; PMID:21119602; http://dx.doi.org/10.1038/onc.2010.530
19. Rietze RL, Reynolds BA. Neural stem cell isolation and characterization. Methods Enzymol 2006; 419:3-23; PMID:17141049; http://dx.doi.org/10.1016/S0076-6879(06)19001-1
20. 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; PMID:15466194; http://dx.doi.org/10.1158/0008-5472.CAN-04-1364
21. 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; PMID:7724580; http://dx.doi. org/10.1073/pnas.92.8.3439
22. Shappell SB, Thomas G V, Roberts RL, Herbert R, Ittmann MM, Rubin MA, et al. Prostate pathology of genetically engineered mice: definitions and clas-sification. 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; PMID:15026373; http://dx.doi.org/10.1158/0008-5472.CAN-03-0946
23. Mazzoleni S, Jachetti E, Morosini S, Grioni M, 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 Cell Trans Med 2013; In press.
24. Foster BA, Gingrich JR, Kwon ED, Madias C, Greenberg NM. Characterization of prostatic epithe-lial cell lines derived from transgenic adenocarcinoma of the mouse prostate (TRAMP) model. Cancer Res 1997; 57:3325-30; PMID:9269988
25. Chiaverotti T, Couto SS, Donjacour A, Mao JH, Nagase H, CardiffRD, et al. Dissociation of epithe-lial and neuroendocrine carcinoma lineages in the transgenic adenocarcinoma of mouse prostate model of prostate cancer. Am J Pathol 2008; 172:236-46; PMID:18156212; http://dx.doi.org/10.2353/ajpath.2008.070602
26. Huss WJ, Gray DR, Tavakoli K, Marmillion ME, Durham LE, Johnson MA, et al. Origin of andro-gen-insensitive poorly differentiated tumors in the transgenic adenocarcinoma of mouse prostate model. Neoplasia 2007; 9:938-50; PMID:18030362; http://dx.doi.org/10.1593/neo.07562
27. 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; PMID:19887604; http://dx.doi.org/10.1158/0008-5472.CAN-08-4673
28. Clarke M F, 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; PMID:16990346; http://dx.doi.org/10.1158/0008-5472.CAN-06-3126
29. Diefenbach A, Jamieson AM, Liu SD, Shastri N, Raulet DH. Ligands for the murine NKG2D recep-tor: expression by tumor cells and activation of NK cells and macrophages. Nat Immunol 2000; 1:119-26; PMID:11248803; http://dx.doi.org/10.1038/77793
30. 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; PMID:16061644; http://dx.doi.org/10.1158/0008-5472.CAN-04-2548
31. Yeh I T, Reddick RL, Kumar A P. Malignancy arising in seminal vesicles in the transgenic adenocarci-noma of mouse prostate (TRAMP) model. Prostate 2009; 69:755-60; PMID:19170049; http://dx.doi. org/10.1002/pros.20924
32. Degl'Innocenti E, Grioni M, Boni A, Camporeale A, Bertilaccio M T, 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; PMID:15597325; http://dx.doi.org/10.1002/eji.200425531
33. 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; PMID:18245488; http://dx.doi.org/10.1158/0008-5472.CAN-07-0445
34. 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; PMID:20388780; http://dx.doi. org/10.1158/0008-5472.CAN-09-4253
35. 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; PMID:18463539; http://dx.doi.org/10.1097/CJI.0b013e318174a512
36. Vesely MD, Kershaw MH, Schreiber RD, Smyth MJ. Natural innate and adaptive immunity to cancer. Annu Rev Immunol 2011; 29:235-71; PMID:21219185; http://dx.doi.org/10.1146/annurev-immunol-031210-101324
37. Ronchetti A, Rovere P, Iezzi G, Galati G, Heltai S, Protti M P, 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
38. 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; PMID:18172322; http://dx.doi. org/10.1158/0008-5472.CAN-07-2429
39. Garcia-Hernandez MdeL, Gray A, Hubby B, Kast WM. In vivo effects of vaccination with six-trans-membrane epithelial antigen of the prostate: a candidate antigen for treating prostate cancer. Cancer Res 2007; 67:1344-51; PMID:17283172; http://dx.doi. org/10.1158/0008-5472.CAN-06-2996
40. 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; PMID:20936707; http://dx.doi.org/10.1002/stem.538
41. 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; PMID:17553900; http://dx.doi.org/10.1158/0008-5472.CAN-07-0768
42. 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; PMID:19741607; http://dx.doi.org/10.1038/nature08361
43. Rigamonti N, Bellone M. Prostate cancer, tumor immunity and a renewed sense of optimism in immunotherapy. Cancer Immunol Immunother 2012; 61:453-68; PMID:22331081; http://dx.doi.org/10.1007/s00262-012-1216-6
44. 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; PMID:9465086; http://dx.doi.org/10.1073/pnas.95.4.1735
45. 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; PMID:10588738; http://dx.doi.org/10.1073/pnas.96.25.14523
46. Yang D, Holt GE, Velders M P, 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 trans-genic adenocarcinoma mouse prostate mice. Cancer Res 2001; 61:5857-60; PMID:11479226
47. 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; PMID:20006141; http://dx.doi.org/10.1016/j.vaccine.2009.09.106
48. Uccelli A, Moretta L, Pistoia V. Mesenchymal stem cells in health and disease. Nat Rev Immunol 2008; 8:726-36; PMID:19172693; http://dx.doi.org/10.1038/nri2395
49. 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; PMID:20068175; http://dx.doi. org/10.1158/0008-5472.CAN-09-1592
50. 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; PMID:16622681; http://dx.doi.org/10.1007/s00262-006-0165-3
51. Thomas-Kaskel AK, Zeiser R, Jochim R, Robbel C, Schultze-Seemann W, Waller C F, 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; PMID:16977630; http://dx.doi.org/10.1002/ijc.22097
52. Restifo N P, Dudley ME, Rosenberg SA. Adoptive immunotherapy for cancer: harnessing the T cell response. Nat Rev Immunol 2012; 12:269-81; PMID:22437939; http://dx.doi.org/10.1038/nri3191
53. 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
54. 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; PMID:3877776; http://dx.doi.org/10.1084/jem.162.6.1745
55. 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; PMID:2666863; http://dx.doi.org/10.1038/340443a0
56. 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
57. 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; PMID:15289500; http://dx.doi.org/10.1084/jem.20040370