High expression of CD109 antigen regulates the phenotype of cancer stem-like cells/cancer-initiating cells in the novel epithelioid sarcoma cell line ESX and is related to poor prognosis of soft tissue sarcoma

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Emori, Makoto ^a   Tsukahara, Tomohide ^a   Murase, Masaki ^a   Kano, Masanobu ^a   Murata, Kenji ^a   Takahashi, Akari ^a   Kubo, Terufumi ^a   Asanuma, Hiroko ^a   Yasuda, Kazuyo ^a   Kochin, Vitaly ^a   Kaya, Mitsunori ^a   Nagoya, Satoshi ^a   Nishio, Jun ^b   Iwasaki, Hiroshi ^b   Sonoda, Tomoko ^a   Hasegawa, Tadashi ^a   Torigoe, Toshihiko ^a   Wada, Takuro ^a   Yamashita, Toshihiko ^a   Sato, Noriyuki ^a  

^a SAPPORO MEDICAL UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b FUKUOKA UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALDEHYDE DEHYDROGENASE; CD109 ANTIGEN; LYMPHOCYTE ANTIGEN; MESSENGER RNA; SMAD PROTEIN; TRANSCRIPTION FACTOR SNAIL; TRANSCRIPTION FACTOR TWIST; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; CANCER CELL CULTURE; CANCER PROGNOSIS; CANCER STEM CELL; CARCINOGENICITY; CELL INVASION; CELL PROLIFERATION; CELL SUBPOPULATION; CLONOGENESIS; CONTROLLED STUDY; CORRELATION ANALYSIS; DISEASE FREE SURVIVAL; ENZYME ACTIVITY; EPITHELIAL MESENCHYMAL TRANSITION; EPITHELIOID SARCOMA; FEMALE; GENE EXPRESSION PROFILING; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INHIBITION KINETICS; MOUSE; NONHUMAN; OVERALL SURVIVAL; PHENOTYPE; PROBABILITY; PROTEIN EXPRESSION; SOFT TISSUE SARCOMA;

ADULT; ANTIGENS, CD; CELL LINE, TUMOR; DNA PRIMERS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GPI-LINKED PROTEINS; HUMANS; IMMUNOHISTOCHEMISTRY; ISOENZYMES; KAPLAN-MEIER ESTIMATE; NEOPLASM PROTEINS; NEOPLASTIC STEM CELLS; POLYMERASE CHAIN REACTION; PROGNOSIS; RETINAL DEHYDROGENASE; RNA, SMALL INTERFERING; SARCOMA;

EID: 84893502568     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0084187     Document Type: Article

References (48)

1. Weiss SW, Goldblum JR (2008) Enzinger and Weiss's soft tissue tumors. Mosby, Inc.
2. Jordan CT, Guzman ML, Noble M (2006) Cancer stem cells. N Engl J Med 355: 1253-1261. doi:10.1056/NEJMra061808. PubMed: 16990388. (Pubitemid 44427449)
3. Sládek NE (2003) Human aldehyde dehydrogenases: potential pathological, pharmacological, and toxicological impact. J Biochem Mol Toxicol 17: 7-23. doi:10.1002/jbt.10057. PubMed: 12616643.
4. Vasiliou V, Pappa A, Petersen DR (2000) Role of aldehyde dehydrogenases in endogenous and xenobiotic metabolism. Chem Biol Interact 129: 1-19. doi:10.1016/S0009-2797(00)00211-8. PubMed: 11154732. (Pubitemid 32061051)
5. van den Hoogen C, van der Horst G, Cheung H, Buijs JT, Lippitt JM et al. (2010) High aldehyde dehydrogenase activity identifies tumor-initiating and metastasis-initiating cells in human prostate cancer. Cancer Res 70: 5163-5173. doi:10.1158/0008-5472.CAN-09-3806. PubMed: 20516116.
6. Cheung AM, Wan TS, Leung JC, Chan LY, Huang H et al. (2007) Aldehyde dehydrogenase activity in leukemic blasts defines a subgroup of acute myeloid leukemia with adverse prognosis and superior NOD/SCID engrafting potential. Leukemia 21: 1423-1430. doi:10.1038/sj.leu.2404721. PubMed: 17476279. (Pubitemid 46965282)
7. Jiang F, Qiu Q, Khanna A, Todd NW, Deepak J et al. (2009) Aldehyde dehydrogenase 1 is a tumor stem cell-associated marker in lung cancer. Mol Cancer Res 7: 330-338. doi: 10.1158/1541-7786.MCR-08-0393. PubMed: 19276181.
8. Li T, Su Y, Mei Y, Leng Q, Leng B et al. (2010) ALDH1A1 is a marker for malignant prostate stem cells and predictor of prostate cancer patients' outcome. Lab Invest 90: 234-244. doi:10.1038/labinvest.2009.127. PubMed: 20010854.
9. Ishibe T, Nakayama T, Okamoto T, Aoyama T, Nishijo K et al. (2005) Disruption of fibroblast growth factor signal pathway inhibits the growth of synovial sarcomas: potential application of signal inhibitors to molecular target therapy. Clin Cancer Res 11: 2702-2712. doi: 10.1158/1078-0432.CCR-04- 2057. PubMed: 15814652. (Pubitemid 40569472)
10. Nishio J, Iwasaki H, Nabeshima K, Ishiguro M, Naumann S et al. (2005) Establishment of a new human epithelioid sarcoma cell line, FU-EPS-1: molecular cytogenetic characterization by use of spectral karyotyping and comparative genomic hybridization. Int J Oncol 27: 361-369. PubMed: 16010416.
11. Wada T, Uede T, Ishii S, Matsuyama K, Yamawaki S et al. (1988) Monoclonal antibodies that detect different antigenic determinants of the same human osteosarcoma-associated antigen. Cancer Res 48: 2273-2279. PubMed: 2450650.
12. Nabeta Y, Kawaguchi S, Sahara H, Ikeda H, Hirohashi Y et al. (2003) Recognition by cellular and humoral autologous immunity in a human osteosarcoma cell line. J Orthop Sci 8: 554-559. doi:10.1007/s00776-003-0663-5. PubMed: 12898310. (Pubitemid 37012069)
13. Tsukahara T, Kawaguchi S, Ida K, Kimura S, Tamura Y et al. (2006) HLA-restricted specific tumor cytolysis by autologous T-lymphocytes infiltrating metastatic bone malignant fibrous histiocytoma of lymph node. J Orthop Res 24: 94-101. doi:10.1002/jor.20019. PubMed: 16419974. (Pubitemid 43772613)
14. Kimura S, Kozakai Y, Kawaguchi S, Tsukahara T, Ida K et al. (2008) Clonal T-cell response against autologous pleomorphic malignant fibrous histiocytoma antigen presented by retrieved HLA-A*0206. J Orthop Res 26: 271-278. doi:10.1002/jor.20497. PubMed: 17853492. (Pubitemid 351220147)
15. Tsukahara T, Kawaguchi S, Torigoe T, Kimura S, Murase M et al. (2008) Prognostic impact and immunogenicity of a novel osteosarcoma antigen, papillomavirus binding factor, in patients with osteosarcoma. Cancer Sci 99: 368-375. doi:10.1111/j.1349-7006.2008.00695.x. PubMed: 18271936. (Pubitemid 351228494)
16. Murase M, Kano M, Tsukahara T, Takahashi A, Torigoe T et al. (2009) Side population cells have the characteristics of cancer stem-like cells/cancer-initiating cells in bone sarcomas. Br J Cancer 101: 1425-1432. doi:10.1038/sj.bjc.6605330. PubMed: 19826427.
17. Nichols J, Zevnik B, Anastassiadis K, Niwa H, Klewe-Nebenius D et al. (1998) Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell 95: 379-391. doi: 10.1016/S0092-8674(00) 81769-9. PubMed: 9814708. (Pubitemid 28507326)
18. Chambers I, Colby D, Robertson M, Nichols J, Lee S et al. (2003) Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell 113: 643-655. doi:10.1016/S0092-8674(03)00392-1. PubMed: 12787505. (Pubitemid 36694189)
19. Yasuda K, Torigoe T, Morita R, Kuroda T, Takahashi A et al. (2013) Ovarian cancer stem cells are enriched in side population and aldehyde dehydrogenase bright overlapping population. PLOS ONE (in press).
20. Sutherland DR, Yeo E, Ryan A, Mills GB, Bailey D et al. (1991) Identification of a cell-surface antigen associated with activated T lymphoblasts and activated platelets. Blood 77: 84-93. PubMed: 1984805.
21. Murray LJ, Bruno E, Uchida N, Hoffman R, Nayar R et al. (1999) CD109 is expressed on a subpopulation of CD34+ cells enriched in hematopoietic stem and progenitor cells. Exp Hematol 27: 1282-1294. doi:10.1016/S0301-472X(99)00071-5. PubMed: 10428505.
22. Finnson KW, Tam BY, Liu K, Marcoux A, Lepage P et al. (2006) Identification of CD109 as part of the TGF-beta receptor system in human keratinocytes. FASEB J 20: 1525-1527. doi:10.1096/fj.05-5229fje. PubMed: 16754747.
23. Hollmann TJ, Hornick JL (2011) INI1-deficient tumors: diagnostic features and molecular genetics. Am J Surg Pathol 35: e47-e63. doi: 10.1097/PAS. 0b013e31822b325b. PubMed: 21934399.
24. Reeves BR, Fisher C, Smith S, Courtenay VD, Robertson D (1987) Ultrastructural, immunocytochemical, and cytogenetic characterization of a human epithelioid sarcoma cell line (RM-HS1). J Natl Cancer Inst 78: 7-18. PubMed: 2432306. (Pubitemid 17009765)
25. Kelland LR, Bingle L (1988) Radiosensitivity and characterisation of a newly established cell line from an epithelioid sarcoma. Br J Cancer 58: 322-325. doi:10.1038/bjc.1988.211. PubMed: 3179184.
26. Stenman G, Kindblom LG, Willems J, Angervall L (1990) A cell culture, chromosomal and quantitative DNA analysis of a metastatic epithelioid sarcoma. Deletion 1p, a possible primary chromosomal abnormality in epithelioid sarcoma. Cancer 65: 2006-2013. doi: 10.1002/1097-0142(19900501)65:9. PubMed: 2196989. (Pubitemid 20147641)
27. Gerharz CD, Moll R, Ramp U, Mellin W, Gabbert HE (1990) Multidirectional differentiation in a newly established human epithelioid sarcoma cell line (GRU-1) with co-expression of vimentin, cytokeratins and neurofilament proteins. Int J Cancer 45: 143-152. doi:10.1002/ijc.2910450126. PubMed: 1688830. (Pubitemid 20032112)
28. Roché H, Julia AM, Jozan S, Muller C, Dastugue N et al. (1993) Characterization and chemosensitivity of a human epithelioid sarcoma cell line (SARCCR 2). Int J Cancer 54: 663-668. doi:10.1002/ijc.2910540423. PubMed: 8099901. (Pubitemid 23188200)
29. Sonobe H, Furihata M, Iwata J, Oka T, Ohtsuki Y et al. (1993) Morphological characterization of a new human epithelioid sarcoma cell line, ES020488, in vitro and in vivo. Virchows Arch B Cell Pathol Incl Mol Pathol 63: 219-225. doi:10.1007/BF02899265. PubMed: 7685133. (Pubitemid 23134400)
30. Cordoba JC, Parham DM, Meyer WH, Douglass EC (1994) A new cytogenetic finding in an epithelioid sarcoma, t(8;22)(q22;q11). Cancer Genet Cytogenet 72: 151-154. (Pubitemid 24161950)
31. Helson C, Melamed M, Braverman S, Traganos F, Preti R et al. (1995) Va-es-bj - an epithelioid sarcoma cell-line. Int J Oncol 7: 51-56. PubMed: 21552805.
32. Iwasaki H, Ohjimi Y, Ishiguro M, Isayama T, Kaneko Y et al. (1996) Epithelioid sarcoma with an 18q aberration. Cancer Genet Cytogenet 91: 46-52. doi:10.1016/S0165-4608(95)00315-0. PubMed: 8908166. (Pubitemid 26398363)
33. Kusakabe H, Sakatani S, Yonebayashi K, Kiyokane K (1997) Establishment and characterization of an epithelioid sarcoma cell line with an autocrine response to interleukin-6. Arch Dermatol Res 289: 224-233. doi:10.1007/ s004030050184. PubMed: 9143739. (Pubitemid 27170476)
34. Russo JE, Hilton J (1988) Characterization of cytosolic aldehyde dehydrogenase from cyclophosphamide resistant L1210 cells. Cancer Res 48: 2963-2968. PubMed: 3365687.
35. Visus C, Ito D, Amoscato A, Maciejewska-Franczak M, Abdelsalem A et al. (2007) Identification of human aldehyde dehydrogenase 1 family member A1 as a novel CD8+ T-cell-defined tumor antigen in squamous cell carcinoma of the head and neck. Cancer Res 67: 10538-10545. doi:10.1158/0008-5472.CAN-07-1346. PubMed: 17974998. (Pubitemid 350070830)
36. Awad O, Yustein JT, Shah P, Gul N, Katuri V et al. (2010) High ALDH activity identifies chemotherapy-resistant Ewing's sarcoma stem cells that retain sensitivity to EWS-FLI1 inhibition. PLOS ONE 5: e13943. doi:10.1371/journal.pone.0013943. PubMed: 21085683.
37. Nakatsugawa M, Takahashi A, Hirohashi Y, Torigoe T, Inoda S et al. (2011) SOX2 is overexpressed in stem-like cells of human lung adenocarcinoma and augments the tumorigenicity. Lab Invest 91: 1796-1804. doi:10.1038/labinvest. 2011.140. PubMed: 21931300.
38. Jaenisch R, Young R (2008) Stem cells, the molecular circuitry of pluripotency and nuclear reprogramming. Cell 132: 567-582. doi: 10.1016/j.cell.2008.01.015. PubMed: 18295576. (Pubitemid 351253686)
39. Schatton T, Frank MH (2008) Cancer stem cells and human malignant melanoma. Pigment. Cell - Melanoma Res 21: 39-55. (Pubitemid 351421465)
40. Velcheti V, Schalper K, Yao X, Cheng H, Kocoglu M et al. (2013) High SOX2 levels predict better outcome in non-small cell lung carcinomas. PLOS ONE 8: e61427. doi:10.1371/journal.pone.0061427. PubMed: 23620753.
41. Hwang SM, Kim MJ, Chang HE, Hong YJ, Kim TS, et al. (2013) Human platelet antigen genotyping and expression of CD109 (human platelet antigen 15) mRNA in various human cell types. Biomed Res Int 2013: 946403
42. Man XY, Finnson KW, Baron M, Philip A (2012) CD109, a TGF-beta co-receptor, attenuates extracellular matrix production in scleroderma skin fibroblasts. Arthritis Res Ther 14: R144. doi:10.1186/ar3877. PubMed: 22694813.
43. Hagiwara S, Murakumo Y, Sato T, Shigetomi T, Mitsudo K et al. (2008) Up-regulation of CD109 expression is associated with carcinogenesis of the squamous epithelium of the oral cavity. Cancer Sci 99: 1916-1923. PubMed: 19016750.
44. Hagiwara S, Murakumo Y, Mii S, Shigetomi T, Yamamoto N et al. (2010) Processing of CD109 by furin and its role in the regulation of TGF-beta signaling. Oncogene 29: 2181-2191. doi:10.1038/onc.2009.506. PubMed: 20101215.
45. Bizet AA, Liu K, Tran-Khanh N, Saksena A, Vorstenbosch J et al. (2011) The TGF-beta co-receptor, CD109, promotes internalization and degradation of TGF-beta receptors. Biochim Biophys Acta 1813: 742-753. doi:10.1016/j.bbamcr. 2011.01.028. PubMed: 21295082.
46. Hagikura M, Murakumo Y, Hasegawa M, Jijiwa M, Hagiwara S et al. (2010) Correlation of pathological grade and tumor stage of urothelial carcinomas with CD109 expression. Pathol Int 60: 735-743. doi: 10.1111/j.1440-1827.2010.02592.x. PubMed: 20946523.
47. Ikushima H, Miyazono K (2012) TGF-beta signal transduction spreading to a wider field: a broad variety of mechanisms for context-dependent effects of TGF-beta. Cell Tissue Res 347: 37-49. doi: 10.1007/s00441-011-1179-5. PubMed: 21618142.
48. Miura Y, Keira Y, Ogino J, Nakanishi K, Noguchi H et al. (2012) Detection of specific genetic abnormalities by fluorescence in situ hybridization in soft tissue tumors. Pathol Int 62: 16-27. doi:10.1111/j.1440-1827.2011.02739.x. PubMed: 22192800.