Characterization of a Cancer Stem Cell-Like Side Population Derived from Human Pancreatic Adenocarcinoma Cells

American Cancer Society: Cancer Facts and Figures 2008. Atlanta, Ga: American Cancer Society, 2008. Also available online. Last accessed October 1, 2008.

Reya T. , Morrison S.J. , Clarke M.F. , Weissman I.L. : Stem cells, cancer, and cancer stem cells. Nature, 414: 105–111, 2001.

Beachy P.A. , Karhadkar S.S. , Berman D.M. : Tissue repair and stem cell renewal in carcinogenesis. Nature, 432: 324–331, 2004.

Wulf G.G. , Wang R.Y. , Kuehnle I. , Weidner D. , Marini F. , Brenner M.K. , Andreeff M. , Goodell M.A. : A leukemic stem cell with intrinsic drug efflux capacity in acute myeloid leukemia. Blood, 98: 1166–1173, 2001.

Al-Hajj M. , Wicha M.S. , Benito-Hernandez A. , Morrison S.J. , Clarke M.F. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA, 100: 3983–3988, 2003.

Singh S.K. , Clarke I.D. , Terasaki M. , Bonn V.E. , Hawkins C. , Squire J. , Dirks P.B. : Identification of a cancer stem cell in human brain tumors. Cancer Res, 63: 5821–5828, 2003.

Kondo T. , Setoguchi T. , Taga T. : Persistence of a small subpopulation of cancer stem-like cells in the C6 glioma cell line. Proc Natl Acad Sci USA, 101: 781–786, 2004.

Yuan X. , Curtin J. , Xiong Y. , Liu G. , Waschsmann-Hogiu S. , Farkas D.L. , Black K.L. , Yu J.S. : Isolation of cancer stem cells from adult glioblastoma multiforme. Oncogene, 23: 9392–9400, 2004.

Singh S.K. , Hawkins C. , Clarke I.D. , Squire J.A. , Bayani J. , Hide T. , Henkelman R.M. , Cusimano M.D. , Dirks P.B. : Identification of human brain tumour initiating cells. Nature, 432: 281–282, 2004.

Chiba T. , Kita K. , Zheng Y.W. , Yokosuka O. , Saisho H. , Iwama A. , Nakauchi H. , Taniguchi H. : Side population purified from hepatocellular carcinoma cells harbors cancer stem cell-like properties. Hepatology, 44: 240–251, 2006.

Wang J. , Guo L.P. , Chen L.Z. , Zeng Y.X. , Lu S.H. : Identification of cancer stem cell-like side population cells in human nasopharyngeal carcinoma cell line. Cancer Res, 67: 3716–3721 2007.

Li C.W. , Heidt D.G. , Dalerba P. , Burant C.F. , Zhang L. , Adsay V. , Wicha M. , Clarke M.F. , Simeone D.M. : Identification of Pancreatic cancer stem cells. Cancer Res, 67: 1030–1037, 2007.

Hermann P.C. , Huber S.L. , Herrler T. , Aicher A. , Ellwart J.W. , Guba M. , Bruns C.J. , Heeschen C. : Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell, 1: 241–242, 2007.

Hadnagy A. , Gaboury L. , Beaulieu R. , Balicki D. : SP analysis may be used to identify cancer stem cell populations. Exp Cell Res, 312: 3701–3710, 2006.

Challen G.A. , Little M.H. : A side order of stem cells: the SP phenotype. Stem Cells, 24: 3–12, 2006.

Goodell M.A. , Rosenzweig M. , Kim H. , Marks D.F. , DeMaria M. , Paradis G. , Grupp S.A. , Sieff C.A. , Mulligan R.C. , Johnson R.P. : Dye efflux studies suggest that hematopoietic stem cells expressing low or undetectable levels of CD34 antigen exist in multiple species. Nat Med, 3: 1337–1345, 1997.

Scharenberg C.W. , Harkey M.A. , Torok-Storb B. : The ABCG2 transporter is an efficient Hoechst 33342 efflux pump and is preferentially expressed by immature human hematopoietic progenitors. Blood, 99: 507–512, 2002.

Kim M. , Turnquist H. , Jackson J. , Sgagias M. , Yan Y. , Gong M. , Dean M. , Sharp J.G. , Cowan K. : The multidrug resistance transporter ABCG2 (breast cancer resistance protein 1) effluxes Hoechst 33342 and is overexpressed in hematopoietic stem cells. Clin Cancer Res, 8: 22–28, 2002.

Bunting K.D. : ABC transporters as phenotypic markers and functional regulators of stem cells. Stem Cells, 20: 11–20, 2002.

Wang F.P. , Wang L. , Yang J.S. , Nomura M. , Miyamoto K. : Reversal of P-glycoprotein-dependent resistance to vinblastine by newly synthesized bisbenzylisoquinoline alkaloids in mouse leukemia P388 cells. Biol Pharm Bull, 28: 1979–1982, 2005.

Gréen H. , Söderkvist P. , Rosenberg P. , Horvath G. , Peterson C. : mdr-1 single nucleotide polymorphisms in ovarian cancer tissue: G2677T/A correlates with response to paclitaxel chemotherapy. Clin Cancer Res, 12: 854–859, 2006.

Hirschmann-Jax C. , Foster A.E. , Wulf G.G. , Wulf G.G. , Nuchtern J.G. , Jax T.W. , Gobel U. , Goodell M.A. , Brenner M.K. : A distinct “side population” of cells with high drug efflux capacity in human tumor cells. Proc Natl Acad Sci USA, 101: 14228–14233, 2004.

Sparreboom A. , Loos W.J. , Burger H. , Sissung T.M. , Verweij J. , Figg W.D. , Nooter K. , Gelderblom H. : Effect of ABCG2 genotype on the oral bioavailability of topotecan. Cancer Biol Ther, 4: 650–658, 2005.

Chen Z.S. , Robey R.W. , Belinsky M.G. , Shchaveleva I. , Ren X.Q. , Sugimoto Y. , Ross D.D. , Bates S.E. , Kruh G.D. : Transport of methotrexate, methotrexate polyglutamates, and 17beta-estradiol 17-(beta-D-glucuronide) by ABCG2: effects of acquired mutations at R482 on methotrexate transport. Cancer Res, 63: 4048–4054, 2003.

Burger H. , van Tol H. , Boersma A.W. , Brok M. , Wiemer E.A. , Stoter G. , Nooter K. : Imatinib mesylate (STI571) is a substrate for the breast cancer resistance protein (BCRP)/ABCG2 drug pump. Blood, 104: 2940–2942, 2004.

Haraguchi N. , Utsunomiya T. , Inoue H. , Tanaka F. , Mimori K. , Barnard G.F. , Mori M. : Charaterization of a side population of cancer cells from human gastrointestinal system. Stem Cells, 24: 506–513, 2006.

Sung J.M. , Cho H.J. , Yi H. , Lee C.H. , Kim H.S. , Kim D.K. , Abd El-Aty A.M. , Kim J.S. , Landowski C.P. , Hediger M.A. , Shin H.C. : Characterization of a stem cell population in lung cancer A549 cells. Biochem Biophys Res Commun, 371: 163–167, 2008.

Patrawala L. , Calhoun T. , Schneider-Broussard R. , Zhou J. , Claypool K. , Tang D.G. : Side population is enriched in tumorigenic, stem-like cancer cells, whereas ABCG2+ and ABCG2– cancer cells are similarly tumorigenic. Cancer Res, 65: 6207–6219, 2005.

Shi G.M. , Xu Y , Fan J. , Zhou J. , Yang X.R. , Qiu S.J. , Liao Y. , Wu W.Z. , Ji Y. , Ke A.W. , Ding Z.B. , He Y.Z. , Wu B. , Yang G.H. , Qin W.Z. , Zhang W. , Zu J. , Min Z.H. , Wu Z.Q. : Identification of side population cells in human hepatocellular carcinoma cell lines with stepwise metastatic potentials. J Cancer Res Clin Oncol, 134: 1155–1163, 2008.

Ricci-Vitiani L. , Lombardi D.G. , Pilozzi E. , Biffoni M. , Todaro M. , Peschle C. , De Maria R. : Identification and expansion of human colon-cancer-initiating cells. Nature, 445: 111–115, 2007.

Collins A.T. , Berry P.A. , Hyde C. , Stower M.J. , Maitland N.J. : Prospective identification of tumorigenic prostate cancer stem cells. Cancer Res, 65: 10946–10951, 2005.

Dou J. , Pan M. , Wen P. , Li Y. , Tang Q. , Chu L. , Zhao F. , Jiang C. , Hu W. , Hu K. , Gu N. : Isolation and identification of cancer stem-like cells from murine melanoma cell lines. Cell Mol Immunol, 4: 467–472, 2007.

Ponti D. , Costa A. , Zaffaroni N. , Pratesi G. , Petrangolini G. , Coradini D. , Pilotti S. , Pierotti M.A. , Daidone M.G. : Isolation and in vitro propagation of tumorigenic breast cancer cells with stem/progenitor cell properties. Cancer Res, 65: 5506–5511, 2005.

Inagaki A. , Soeda A. , Oka N. , Kitajima H. , Nakagawa J. , Motohashi T. , Kunisada T. , Iwama T. : Long-term maintenance of brain tumor stem cell properties under at non-adherent and adherent culture conditions. Biochem Biophys Res Commun, 361: 586–592, 2007.

Gou S. , Liu T. , Wang C. , Yin T. , Li K. , Yang M. , Zhou J. : Establishment of clonal colony-forming assay for propagation of pancreatic cancer cells with stem cell properties. Pancreas, 34: 429–435, 2007.

Yu F. , Yao H. , Zhu P. , Zhang X. , Pan Q. , Gong C. , Huang Y. , Hu X. , Su F. , Lieberman J. , Song E. : let-7 regulates self renewal and tumorigenicity of breast cancer cells. Cell, 131: 1109–1123, 2007.

Yin S. , Li J. , Hu C , Chen X. , Yao M. , Yan M. , Jiang G. , Ge C. , Xie H. , Wan D. : CD133 positive hepatocellular carcinoma cells possess high capacity for tumorigenicity. Int J Cancer, 120: 1444–1450, 2007.