Expression of Stem Cell Markers, CD133 and CD44, in Pediatric Solid Tumors: A Study Using Tissue Microarray

REFERENCES

• Reya T, Morrison SJ, Clarke MF, Weissman IL. Stem cells, cancer, and cancer stem cells. Nature 414 (6859):105–11, 2001.
   PubMed Web of Science ®Google Scholar
• Marx J. Cancer research. Mutant stem cells may seed cancer. Science 301(5638):1308–10, 2003.
   Google Scholar
• Bonnet D, Dick JE. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med 3(7):730–7, 1997.
   PubMed Web of Science ®Google Scholar
• Diehn M, Clarke MF. Cancer stem cells and radiotherapy: new insights into tumor radioresistance. J Natl Cancer Inst 98(24):1755–7, 2006.
   PubMedGoogle Scholar
• Eyler CE, Rich JN. Survival of the fittest: cancer stem cells in therapeutic resistance and angiogenesis. J Clin Oncol 26(17):2839–45, 2008.
   PubMed Web of Science ®Google Scholar
• Li X, Lewis MT, Huang J, Gutierrez C, Osborne CK, Wu MF, Hilsenbeck SG, Pavlick A, Zhang X, Chamness GC, Wong H, Rosen J, Chang JC. Intrinsic resistance of tumorigenic breast cancer cells to chemotherapy. J Natl Cancer Inst 100(9):672–9, 2008.
   PubMedGoogle Scholar
• Phillips TM, McBride WH, Pajonk F. The response of CD24(–/low)/CD44 +breast cancer–initiating cells to radiation. J Natl Cancer Inst 98(24):1777–85, 2006.
   PubMedGoogle Scholar
• Collins AT, Berry PA, Hyde C, Stower MJ, Maitland NJ. Prospective identification of tumorigenic prostate cancer stem cells. Cancer Res 65(23):10946–51, 2005.
   PubMed Web of Science ®Google Scholar
• Fang D, Nguyen TK, Leishear K, Finko R, Kulp AN, Hotz SVan Belle PA, Xu X, Elder DE, Herlyn M. A tumorigenic subpopulation with stem cell properties in melanomas. Cancer Res 65(20):9328–37, 2005.
   PubMed Web of Science ®Google Scholar
• Li C, Heidt DG, Dalerba P, Burant CF, Zhang L, Adsay V, Wicha M, Clarke MF, Simeone DM. Identification of pancreatic cancer stem cells. Cancer Res 67(3):1030–7, 2007.
   PubMed Web of Science ®Google Scholar
• Matsui W, Huff CA, Wang Q, Malehorn MT, Barber J, Tanhehco Y, Smith BD, Civin CI, Jones RJ. Characterization of clonogenic multiple myeloma cells. Blood 103(6):2332–6, 2004.
   PubMed Web of Science ®Google Scholar
• Costa FFLe Blanc K, Brodin B. Concise review: cancer/testis antigens, stem cells, and cancer. Stem Cells. . 25(3):707–11, 2007.
   PubMed Web of Science ®Google Scholar
• Al–Hajj M, Wicha MS, Benito–Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A 100(7):3983–8, 2003.
   PubMed Web of Science ®Google Scholar
• Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, Squire J, Dirks PB. Identification of a cancer stem cell in human brain tumors. Cancer Res 63(18):5821–8, 2003.
   PubMed Web of Science ®Google Scholar
• Komuro H, Saihara R, Shinya M, Takita J, Kaneko S, Kaneko M, Hayashi Y. Identification of side population cells (stem–like cell population) in pediatric solid tumor cell lines. J Pediatr Surg 42(12):2040–5, 2007.
   Google Scholar
• Gatta G, Capocaccia R, Coleman MP, Ries LA, Berrino F. Childhood cancer survival in Europe and the United States. Cancer 95(8):1767–72, 2002.
   PubMed Web of Science ®Google Scholar
• Friedman GK, Gillespie GY. Cancer Stem Cells and Pediatric Solid Tumors. Cancers (Basel) 3(1):298–318, 2011.
   Google Scholar
• Immervoll H, Hoem D, Sakariassen PO, Steffensen OJ, Molven A. Expression of the “stem cell marker” CD133 in pancreas and pancreatic ductal adenocarcinomas. BMC Cancer 8:48, 2008.
   PubMed Web of Science ®Google Scholar
• Immervoll H, Hoem D, Steffensen OJ, Miletic H, Molven A. Visualization of CD44 and CD133 in normal pancreas and pancreatic ductal adenocarcinomas: non–overlapping membrane expression in cell populations positive for both markers. J Histochem Cytochem 59(4):441–55, 2011.
   Google Scholar
• Jiang F, Qiu Q, Khanna A, Todd NW, Deepak J, Xing L, Wang H, Liu Z, Su Y, Stass SA, Katz RL. Aldehyde dehydrogenase 1 is a tumor stem cell–associated marker in lung cancer. Mol Cancer Res 7(3):330–8, 2009.
   PubMed Web of Science ®Google Scholar
• Ginestier C, Hur MH, Charafe–Jauffret E, Monville F, Dutcher J, Brown M, Jacquemier J, Viens P, Kleer CG, Liu S, Schott A, Hayes D, Birnbaum D, Wicha MS, Dontu G. ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell 1(5):555–67, 2007.
   PubMed Web of Science ®Google Scholar
• Fabian A, Barok M, Vereb G, Szollosi J. Die hard: are cancer stem cells the Bruce Willises of tumor biology? Cytometry A 75(1):67–74, 2009.
   Google Scholar
• Bohl SR, Pircher A, Hilbe W. Cancer stem cells: characteristics and their potential role for new therapeutic strategies. Onkologie 34(5):269–74, 2011.
   Google Scholar
• Mizrak D, Brittan M, Alison MR. CD133: molecule of the moment. J Pathol 214(1):3–9, 2008.
   PubMed Web of Science ®Google Scholar
• Miraglia S, Godfrey W, Yin AH, Atkins K, Warnke R, Holden JT, Bray RA, Waller EK, Buck DW. A novel five–transmembrane hematopoietic stem cell antigen: isolation, characterization, and molecular cloning. Blood 90(12):5013–21, 1997.
   PubMed Web of Science ®Google Scholar
• Yin AH, Miraglia S, Zanjani ED, Almeida–Porada G, Ogawa M, Leary AG, Olweus J, Kearney J, Buck DW. AC133, a novel marker for human hematopoietic stem and progenitor cells. Blood 90(12):5002–12, 1997.
   PubMed Web of Science ®Google Scholar
• Pode–Shakked N, Metsuyanim S, Rom–Gross E, Mor Y, Fridman E, Goldstein I, Amariglio N, Rechavi G, Keshet G, Dekel B. Developmental tumourigenesis: NCAM as a putative marker for the malignant renal stem/progenitor cell population. J Cell Mol Med 13(8B):1792–808, 2009.
   Google Scholar
• Tong QS, Zheng LD, Tang ST, Ruan QL, Liu Y, Li SW, Jiang GS, Cai JB. Expression and clinical significance of stem cell marker CD133 in human neuroblastoma. World J Pediatr 4(1):58–62, 2008.
   Google Scholar
• Yin S, Li J, Hu C, Chen X, Yao M, Yan M, Jiang G, Ge C, Xie H, Wan D, Yang S, Zheng S, Gu J. CD133 positive hepatocellular carcinoma cells possess high capacity for tumorigenicity. Int J Cancer 120(7):1444–50, 2007.
   PubMed Web of Science ®Google Scholar
• Tirino V, Desiderio V, d'Aquino R, De Francesco F, Pirozzi G, Graziano A, Galderisi U, Cavaliere C, De Rosa A, Papaccio G, Giordano A. Detection and characterization of CD133+ cancer stem cells in human solid tumours. PLoS One 3(10):e3469, 2008.
   PubMed Web of Science ®Google Scholar
• Prince ME, Sivanandan R, Kaczorowski A, Wolf GT, Kaplan MJ, Dalerba P, Weissman IL, Clarke MF, Ailles LE. Identification of a subpopulation of cells with cancer stem cell properties in head and neck squamous cell carcinoma. Proc Natl Acad Sci U S A 104(3):973–8, 2007.
   PubMed Web of Science ®Google Scholar
• Choi D, Lee HW, Hur KY, Kim JJ, Park GS, Jang SH, Song YS, Jang KS, Paik SS. Cancer stem cell markers CD133 and CD24 correlate with invasiveness and differentiation in colorectal adenocarcinoma. World J Gastroenterol 15(18):2258–64, 2009.
   Google Scholar
• Wielenga VJ, Heider KH, Offerhaus GJ, Adolf GR, van den Berg FM, Ponta H, Herrlich P, Pals ST. Expression of CD44 variant proteins in human colorectal cancer is related to tumor progression. Cancer Res. 15; 53(20):4754–6, 1993.
   PubMed Web of Science ®Google Scholar
• Woodman AC, Sugiyama M, Yoshida K, Sugino T, Borgya A, Goodison S, Matsumura Y, Tarin D. Analysis of anomalous CD44 gene expression in human breast, bladder, and colon cancer and correlation of observed mRNA and protein isoforms. Am J Pathol 149(5):1519–30, 1996.
   PubMed Web of Science ®Google Scholar
• Kononen J, Bubendorf L, Kallioniemi A, Bärlund M, Schraml P, Leighton S, Torhorst J, Mihatsch MJ, Sauter G, Kallioniemi O. Tissue microarrays for high–throughput molecular profiling of tumor specimens. Nat Med 4(7):844–7, 1998.
   PubMed Web of Science ®Google Scholar
• Bubendorf L, Nocito A, Moch H, Sauter G. Tissue microarray (TMA) technology: miniaturized pathology archives for high–throughput in situ studies. J Pathol 195(1):72–9, 2001.
   Google Scholar
• Watson NF, Spendlove I, Madjd Z, McGilvray R, Green AR, Ellis IO, Scholefield JH, Durrant LG. Expression of the stress–related MHC class I chain–related protein MICA is an indicator of good prognosis in colorectal cancer patients. Int J Cancer 118(6):1445–52, 2006.
   PubMed Web of Science ®Google Scholar
• Camp RL, Charette LA, Rimm DL. Validation of tissue microarray technology in breast carcinoma. Lab Invest 80(12):1943–9, 2000.
   PubMed Web of Science ®Google Scholar
• Madjd Z, Mehrjerdi AZ, Sharifi AM, Molanaei S, Shahzadi SZ, Asadi–Lari M. CD44+ cancer cells express higher levels of the anti–apoptotic protein Bcl–2 in breast tumours. Cancer Immun 9:4, 2009.
   PubMedGoogle Scholar
• McCarty KS, Jr., Miller LS, Cox EB, Konrath J, McCarty KS, Sr. Estrogen receptor analyses. Correlation of biochemical and immunohistochemical methods using monoclonal antireceptor antibodies. Arch Pathol Lab Med 109(8):716–21, 1985.
   PubMed Web of Science ®Google Scholar
• Ehrlich PF, Ritchey ML, Hamilton TE, Haase GM, Ou S, Breslow N, Grundy P, Green D, Norkool P, Becker J, Shamberger RC. Quality assessment for Wilms' tumor: a report from the National Wilms' Tumor Study–5. J Pediatr Surg 40(1):208–12; discussion 212–3, 2005.
   Google Scholar
• Brodeur GM, Pritchard J, Berthold F, Carlsen NL, Castel V, Castelberry RP, De Bernardi B, Evans AE, Favrot M, Hedborg F, Revisions of the international criteria for neuroblastoma diagnosis, staging, and response to treatment. J Clin Oncol 11(8):1466–77, 1993.
   PubMed Web of Science ®Google Scholar
• Ries LAG, Melbert D, Krapcho M, Stinchcomb DG, Howlader N, Horner MJ, SEER Cancer Statistics Review, 1975–2005. Available from: http://seer.cancer.gov/csr/1975_2005, 2011.
   Google Scholar
• Hill RP. Identifying cancer stem cells in solid tumors: case not proven. Cancer Res 66(4):1891–5; discussion 1890, 2006.
   PubMed Web of Science ®Google Scholar
• Li MC, Deng YW, Wu J, Chen FH, Liu JF, Fang JS. [Isolation and characterization of brain tumor stem cells in human medulloblastoma]. Ai Zheng 25(2):241–6, 2006.
   Google Scholar
• Griguer CE, Oliva CR, Gobin E, Marcorelles P, Benos DJ, Lancaster JR Jr, Gillespie GY. CD133 is a marker of bioenergetic stress in human glioma. PLoS One 3(11):e3655, 2008.
   Google Scholar
• Soeda A, Park M, Lee D, Mintz A, Androutsellis–Theotokis A, McKay RD, Engh J, Iwama T, Kunisada T, Kassam AB, Pollack IF, Park DM. Hypoxia promotes expansion of the CD133–positive glioma stem cells through activation of HIF–1alpha. Oncogene 28(45):3949–59, 2009.
   PubMed Web of Science ®Google Scholar
• Kolenda J, Jensen SS, Aaberg–Jessen C, Christensen K, Andersen C, Brünner N, Kristensen BW. Effects of hypoxia on expression of a panel of stem cell and chemoresistance markers in glioblastoma–derived spheroids. J Neurooncol 103(1):43–58, 2011.
   Google Scholar
• Dekel B, Metsuyanim S, Schmidt–Ott KM, Fridman E, Jacob–Hirsch J, Simon A, Pinthus J, Mor Y, Barasch J, Amariglio N, Reisner Y, Kaminski N, Rechavi G. Multiple imprinted and stemness genes provide a link between normal and tumor progenitor cells of the developing human kidney. Cancer Res 66(12):6040–9, 2006.
   PubMed Web of Science ®Google Scholar
• Metsuyanim S, Harari–Steinberg O, Buzhor E, Omer D, Pode–Shakked N, Ben–Hur H, Halperin R, Schneider D, Dekel B. Expression of stem cell markers in the human fetal kidney. PLoS One 4(8):e6709, 2009.
   PubMed Web of Science ®Google Scholar
• Friedman GK, Gillespie GY, Pressey JG. Human rhabdomyosarcoma cell lines contain myogenically primitive CD133+ cells that are sensitive to killing by engineered herpes simplex virus, in 2009 ASPHO Abstracts. Pediatr Blood and Cancer. 734, 2009.
   Google Scholar
• Liu G, Yuan X, Zeng Z, Tunici P, Ng H, Abdulkadir IR, Lu L, Irvin D, Black KL, Yu JS. Analysis of gene expression and chemoresistance of CD133+ cancer stem cells in glioblastoma. Mol Cancer 5:67, 2006.
   PubMed Web of Science ®Google Scholar
• Al Dhaybi R, Sartelet H, Powell J, Kokta V. Expression of CD133+ cancer stem cells in childhood malignant melanoma and its correlation with metastasis. Mod Pathol 23(3):376–80, 2010.
   Google Scholar
• Balla MM, Vemuganti GK, Kannabiran C, Honavar SG, Murthy R. Phenotypic characterization of retinoblastoma for the presence of putative cancer stem–like cell markers by flow cytometry. Invest Ophthalmol Vis Sci 50(4):1506–14, 2009.
   PubMed Web of Science ®Google Scholar
• Ponti D, Costa A, Zaffaroni N, Pratesi G, Petrangolini G, Coradini D, Pilotti S, Pierotti MA, Daidone MG. Isolation and in vitro propagation of tumorigenic breast cancer cells with stem/progenitor cell properties. Cancer Res 65(13):5506–11, 2005.
   PubMed Web of Science ®Google Scholar