Top

Published in:

01-11-2011 | Laboratory Investigation - Human/Animal Tissue

The CD133+ tumor stem-like cell-associated antigen may elicit highly intense immune responses against human malignant glioma

Authors: Wei Hua, Yu Yao, Yiwei Chu, Ping Zhong, Xiaofang Sheng, Baoguo Xiao, Jingsong Wu, Bojie Yang, Ying Mao, Liangfu Zhou

Published in: Journal of Neuro-Oncology | Issue 2/2011

Abstract

To explore the immunogenicity of glioma stem-like cell-associated antigens (SAAs) from sorted or unsorted glioma tumor stem-like cells (TSCs) as well as irradiated TSCs. Two primary human malignant glioma lines (SHG62, SHG66) and U87 cell line were primarily cultured in the serum-free medium (SFM) supplemented with EGF/bFGF. TSCs were identified by their self-renewal, multi-lineage differentiation and tumorigenic activity. To prepare SAAs in vitro, CD133+ TSCs were sorted either by magnetic cell sorting or with irradiation (6 Gy).The cytotoxicity induced by autogenous myeloid dendritic cell (DC)-mediated SAA-specific cytotoxic T lymphocytes (CTLs) was assessed by the Just Another Method test. SHG62, SHG66, and U87 cells contained TSCs. CD133+ SAAs-specific CTLs were significantly more cytotoxic than effector cells loaded with unsorted SAA (P < 0.05). Effector cells loaded with irradiated SAAs were more cyotoxic than those with regular SAAs (P < 0.01). SAAs from CD133+ TSCs and irradiated TSCs provide highly immunogenic antigens. TSCs might be a novel source of antigens for DC vaccination against malignant gliomas.

Gonzalez J, Gilbert MR (2005) Treatment of astrocytomas. Curr Opin Neurol 18:632–638PubMedCrossRef

Nano R, Ceroni M (2005) The immunobiology of malignant gliomas. Funct Neurol 20:39–42PubMed

McLendon RE, Wikstrand CJ, Matthews MR, Al-Baradei R, Bigner SH, Bigner DD (2000) Glioma-associated antigen expression in oligodendroglial neoplasms: Tenascin and epidermal growth factor receptor. J Histochem Cytochem 48:1103–1110PubMedCrossRef

Yamada Y, Kuroiwa T, Nakagawa T, Kajimoto Y, Dohi T, Azuma H, Tsuji M, Kami K, Miyatake S (2003) Transcriptional expression of survivin and its splice variants in brain tumors in humans. J Neurosurg 99:738–745PubMedCrossRef

Imaizumi T, Kuramoto T, Matsunaga K, Shichijo S, Yutani S, Shigemori M, Oizumi K, Itoh K (1999) Expression of the tumor-rejection antigen SART1 in brain tumors. Int J Cancer 83:760–764PubMedCrossRef

Okano F, Storkus WJ, Chambers WH, Pollack IF, Okada H (2002) Identification of a novel HLA-A*0201-restricted, cytotoxic T lymphocyte epitope in a human glioma-associated antigen, interleukin 13 receptor alpha2 chain. Clin Cancer Res 8:2851–2855PubMed

Chi DD, Merchant RE, Rand R, Conrad AJ, Garrison D, Turner R, Morton DL, Hoon DS (1997) Molecular detection of tumor-associated antigens shared by human cutaneous melanomas and gliomas. Am J Pathol 150:2143–2152PubMed

Schmitz M, Temme A, Senner V, Ebner R, Schwind S, Stevanovic S, Wehner R, Schackert G, Schackert HK, Fussel M, Bachmann M, Rieber EP, Weigle B (2007) Identification of SOX2 as a novel glioma-associated antigen and potential target for T cell-based immunotherapy. Br J Cancer 96:1293–1301PubMedCrossRef

Yu JS, Wheeler CJ, Zeltzer PM, Ying H, Finger DN, Lee PK, Yong WH, Incardona F, Thompson RC, Riedinger MS, Zhang W, Prins RM, Black KL (2001) Vaccination of malignant glioma patients with peptide-pulsed dendritic cells elicits systemic cytotoxicity and intracranial T-cell infiltration. Cancer Res 61:842–847PubMed

10.

Schulenburg A, Ulrich-Pur H, Thurnher D, Erovic B, Florian S, Sperr WR, Kalhs P, Marian B, Wrba F, Zielinski CC, Valent P (2006) Neoplastic stem cells: A novel therapeutic target in clinical oncology. Cancer 107:2512–2520PubMedCrossRef

11.

Pellegatta S, Poliani PL, Corno D, Menghi F, Ghielmetti F, Suarez-Merino B, Caldera V, Nava S, Ravanini M, Facchetti F, Bruzzone MG, Finocchiaro G (2006) Neurospheres enriched in cancer stem-like cells are highly effective in eliciting a dendritic cell-mediated immune response against malignant gliomas. Cancer Res 66:10247–10252PubMedCrossRef

12.

Xu Q, Liu G, Yuan X, Xu M, Wang H, Ji J, Konda B, Black KL, Yu JS (2009) Antigen-specific T-cell response from dendritic cell vaccination using cancer stem-like cell-associated antigens. Stem Cells 27:1734–1740PubMedCrossRef

13.

Wei H, Yao Yu, Liang-fu Z, Ying M, Bao-guo X, Yi-wei C, Feng X, Jian-hong Z (2009) Stem-like cells associated antigens augment the effect of dendritic cells-based vaccination against human malignant glioma cells in vitro. Chin J Neurosurg 25:847–852

14.

Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T, Henkelman RM, Cusimano MD, Dirks PB (2004) Identification of human brain tumour initiating cells. Nature 432:396–401PubMedCrossRef

15.

Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, Dewhirst MW, Bigner DD, Rich JN (2006) Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 444:756–760PubMedCrossRef

16.

Combs SE, Schulz-Ertner D, Roth W, Herold-Mende C, Debus J, Weber KJ (2007) In vitro responsiveness of glioma cell lines to multimodality treatment with radiotherapy, temozolomide, and epidermal growth factor receptor inhibition with cetuximab. Int J Radiat Oncol Biol Phys 68:873–882PubMedCrossRef

17.

Cho WC (2009) Updates in cancer research: insights from the AACR 100th annual meeting. Expert Rev Mol Diagn 9:411–416PubMedCrossRef

18.

Prestegarden L, Svendsen A, Wang J, Sleire L, Skaftnesmo KO, Bjerkvig R, Yan T, Askland L, Persson A, Sakariassen PØ, Enger PØ (2010) Glioma cell populations grouped by different cell type markers drive brain tumor growth. Cancer Res 70:4274–4279PubMedCrossRef

19.

Yao Y, Wang X, Jin K, Zhu J, Wang Y, Xiong S, Mao Y, Zhou L (2008) B7H4 is preferentially expressed in non-dividing brain tumor cells and in a subset of brain tumor stem-like cells. J Neurooncol 89:121–129PubMedCrossRef

20.

Newcomb EW, Demaria S, Lukyanov Y, Shao Y, Schnee T, Kawashima N, Lan L, Dewyngaert JK, Zagzag D, McBride WH, Formenti SC (2006) The combination of ionizing radiation and peripheral vaccination produces long-term survival of mice bearing established invasive GL261 gliomas. Clin Cancer Res 12:4730–4737PubMedCrossRef

21.

Dai J, Liu B, Caudill MM, Zheng H, Qiao Y, Podack ER, Li Z (2003) Cell surface expression of heat shock protein gp96 enhances cross-presentation of cellular antigens and the generation of tumor specific T cell memory. Cancer Immun 3:1–6PubMed

22.

Lumniczky K, Desaknai S, Mangel L, Szende B, Hamada H, Hidvegi EJ, Safrany G (2002) Local tumor irradiation augments the antitumor effect of cytokine-producing autologous cancer cell vaccines in a murine glioma model. Cancer Gene Ther 9:44–52PubMedCrossRef

23.

Wu A, Wiesner S, Xiao J, Ericson K, Chen W, Hall WA, Low WC, Ohlfest JR (2006) Expression of MHC I and NK ligands on human CD133(+) glioma cells: possible targets of immunotherapy. J Neurooncol 83:121–131PubMedCrossRef

24.

Di Tomaso T, Mazzoleni S, Wang E, Sovena G, Clavenna D, Franzin A, Mortini P, Ferrone S, Doglioni C, Marincola FM, Galli R, Parmiani G, Maccalli C (2010) Immunobiological characterization of cancer stem cells isolated from glioblastoma patients. Clin Cancer Res 16:800–813PubMedCrossRef

25.

Shafer JA, Bollard CM, Leen AM, Rooney CM, Brenner MK, Foster AE (2008) The “side-population” in human lymphoma cell lines have increased chemo-resistance, stem-like properties, as a target for immunotherapy. Biol Blood Marrow Transplant 14:65–66CrossRef

26.

Parajuli P, Mathupala S, Mittal S, Sloan AE (2007) Dendritic cell-based active specific immunotherapy for malignant glioma. Expert Opin Biol Ther 7:1–8CrossRef

Title: The CD133+ tumor stem-like cell-associated antigen may elicit highly intense immune responses against human malignant glioma
Authors: Wei Hua
Yu Yao
Yiwei Chu
Ping Zhong
Xiaofang Sheng
Baoguo Xiao
Jingsong Wu
Bojie Yang
Ying Mao
Liangfu Zhou
Publication date: 01-11-2011
Publisher: Springer US
Published in: Journal of Neuro-Oncology / Issue 2/2011
Print ISSN: 0167-594X
Electronic ISSN: 1573-7373
DOI: https://doi.org/10.1007/s11060-011-0572-y

Keynote webinar | Spotlight on medication adherence

Springer Medicine

The CD133+ tumor stem-like cell-associated antigen may elicit highly intense immune responses against human malignant glioma

Abstract

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 2/2011

Postoperative seizure in high grade glioma patients treated with BCNU wafers. A mono-institutional experience

Safety and feasibility of motexafin gadolinium administration with whole brain radiation therapy and stereotactic radiosurgery boost in the treatment of ≤6 brain metastases: a multi-institutional phase II trial

Herpes simplex encephalitis in patients with cancer

The natural history of extracranial metastasis from glioblastoma multiforme

Sarcoma arising as a distinct nodule within glioblastoma: a morphological and molecular perspective on gliosarcoma

Patterns of missing mini mental status exam (MMSE) in radiation therapy oncology group (RTOG) brain cancer trials