Multicellular spheroids as an in vitro model in experimental oncology: applications in translational medicine

Bibliography

• VAN DYKE T, JACKS T: Cancer modeling in the modern era: progress and challenges. Cell (2002) 108:135-144.
   PubMed Web of Science ®Google Scholar
• GOLDIN A, JOHNSON RK, VENDITTI JM: Usefulness and limitations of murine tumor models for the identification of new antitumor agents. Antibiot. Chemother. (1980) 28:1-7.
   PubMedGoogle Scholar
• HANN B, BALMAIN A: Building ‘validated’ mouse models of human cancer. Curr. Opin. Cell Biol. (2001)13(6):778-784.
   Web of Science ®Google Scholar
• KAREN LS, MINA JB: Modeling tissue-specific signaling and organ function in three dimensions. J. Cell. Sci. (2003) 116:2377-2388.
   PubMed Web of Science ®Google Scholar
• AUERBACH R, GROBSTEIN C: Inductive interaction of embryonic tissues after dissociation and reaggregation. Exp. Cell Res. (1958) 15:384-397
   PubMed Web of Science ®Google Scholar
• DWARAKANATH BS, JAIN VK: Modification of the radiation induced damage by 2-deoxy-d-glucose in organ cultures of human cerebral gliomas. Int. J. Radiat. Oncol. Biol. Phys. (1987) 13:741-746.
   PubMed Web of Science ®Google Scholar
• DWARKANATH BS, JAIN VK: Effects of γ-rays and glucose analogs on energy metabolism of a cell line derived from human cerebral glioma. Indian J. Biochem. Biophy. (1991) 28:203-209.
   PubMed Web of Science ®Google Scholar
• LASNITZKI I: Animal cell culture, a practical approach. Freshney RI (Ed.). Oxford, IRL Press at Oxford University Press. (1992):213-261.
   Google Scholar
• SUTHERLAND RM, MCCREDIE JA, INCH WR: Growth of multicellular spheroids in tissue culture as a model of nodular carcinomas. J. Nat. Canc. Inst. (1971) 46:113-120.
   PubMed Web of Science ®Google Scholar
• KUNZ-SCHUGHART LA, KREUTZ M, KNUECHEL R: Multicellular spheroids: a three-dimensional in vitro culture system to study tumour biology. Int. J. Exp. Pathol. (1998) 79:1-23.
   PubMed Web of Science ®Google Scholar
• SANTINI MT, RAINALDI G, INDOVINA PL: Multicellular spheroids in radiation biology. Int. J. Rad. Biol. (1999) 75:787-799.
   PubMed Web of Science ®Google Scholar
• SANITINI MT, RAINALDI G, INDOVINA PL: Apoptosis, cell adhesion and extracellular matrix in three-dimentional growth of multicelluler tumor spheroids. Critical Rev. Oncol. Hematol. (2000) 36:75-87.
   PubMed Web of Science ®Google Scholar
• LAYER PG, ROBITZKI A, ROTHERMEL A, WILLBOLD E: Of layers and spheres: the reaggregate approach in tissue engineering. Trends Neurosci. (2002) 25:131-134.
   PubMed Web of Science ®Google Scholar
• ABU-ABSI SF, FRIEND JR, HANSEN LK, HU WS: Structural polarity and functional bile canaliculi in rat hepatocyte spheroids. Exp. Cell Res. (2002) 274:56-67.
   Google Scholar
• MUELLER-KLIESER W: Multicellular spheroids: a review on cellular aggregates in cancer research. J. Cancer Res. Clin. Oncol. (1987) 113:101-122.
   PubMed Web of Science ®Google Scholar
• SUTHERLAND RM, CARLSSON J, DURAND RE, YUHAS J: Spheroids in cancer research. Cancer Res. (1981) 41:2980-2994.
   Web of Science ®Google Scholar
• BJERKVIG R, LUND-JOHANSEN M, EDVARDSEN K: Tumor cell invasion and angiogenesis in the CNS. Curr. Opin. Oncol. (1997) 9:223-229.
   PubMed Web of Science ®Google Scholar
• LUND-JOHANSEN M, FORSBERG K, BJERKVIG R, LAERUM OD: Effects of growth factors on a human glioma cell line during invasion into rat brain aggregates in culture. Acta. Neuropathol. (1992) 84:190-197.
   Google Scholar
• YUHAS JM, LI AP, MARTINEZ AO, LADMAN AJ: A simplified method for production and growth of multicellular tumor spheroids. Cancer Res. (1977) 37:3639-3643.
   PubMed Web of Science ®Google Scholar
• KORFF T, AUGUSTIN HG: Integration of endothelial cells in multicellular spheroids prevents apoptosis and induces differentiation. J. Cell Biol. (1998) 143:1341-1352.
   Google Scholar
• MUELLER-KLIESER W: Three-dimensional cell cultures: from molecular mechanisms to clinical applications. Am. J. Physiol. (1997) 273:1109-1123.
   PubMed Web of Science ®Google Scholar
• SANTINI MT, RAINALDI G: Three-dimensional spheroid model in tumor biology. Pathobiology. (1999) 67:148-157.
   PubMed Web of Science ®Google Scholar
• RAK J, MITSUHASH Y, ERDOS V, HUANG SN, FILMNS J, KERBEL RS: Massive programmed cell death in intestinal epithelial cell induced by three-dimensional growth conditions: suppression by mutant c-H-Ras oncogene expression. J. Cell Biol. (1995) 131:1587-1598.
   PubMed Web of Science ®Google Scholar
• KHAITAN D, CHANDNA S, ARYA MB, DWARAKANATH BS: Establishment and characterization of multicellular spheroids from a human glioma cell line; Implications for tumor therapy. J. Trans. Med. (2006) 4:12.
   PubMed Web of Science ®Google Scholar
• GORCZYCA W, BIGMAN K, MITTELMAN A et al.: Induction of DNA trand breaks associated with apoptosis during treatment of leukemia. Leukemia. (1993) 7:659-670.
   PubMed Web of Science ®Google Scholar
• FISHER DE: Apoptosis in cancer therapy: crossing the threshold. Cell (1994) 78:539-542.
   PubMed Web of Science ®Google Scholar
• SUTHERLAND M: Cell and environment interactions in tumor microregions: the multicell spheroid model. Science (1988) 240:177-184.
   PubMed Web of Science ®Google Scholar
• BRIZEL DM, SCULLY SP, HARRELSON JM et al.: Tumor oxygenation predicts for the likelihood of distant metastases in human soft tissue sarcoma. Cancer Res. (1996) 56:941-943.
   PubMed Web of Science ®Google Scholar
• SEMENZA GL, ROTH PH, FANG HM, WANG GL: Transcriptional regulation of genes encoding glycolytic enzymes by hypoxia-inducible factor 1. J. Biol. Chem. (1994) 269:23757-23763.
   PubMed Web of Science ®Google Scholar
• SEMENZA GL, DANG CV: Oncogenic alterations of metabolism. Trends Biochem. Sci. (1999) 24:68-72.
   PubMed Web of Science ®Google Scholar
• CARMELIET P, DOR Y, HERBERT JM et al.: Role of HIF-1α in hypoxia-mediated apoptosis, cell proliferation and tumour angiogenesis. Nature. (1998) 394:485-490.
   PubMed Web of Science ®Google Scholar
• WALEH NS, BRODY MD, KNAPP MA et al.: Mapping of the vascular endothelial growth factor-producing hypoxic cells in multicellular tumor spheroids using a hypoxia-specific marker. Cancer Res. (1995) 55:6222-6226.
   PubMed Web of Science ®Google Scholar
• GROSS MW, KARBACH U, GROEBE K, FRANKO AJ, MUELLER-KLIESER W: Calibration of misonidazole labeling by simultaneous measurement of oxygen tension and labeling density in multicellular spheroids. Int. J. Cancer. (1995) 61:567-573.
   PubMed Web of Science ®Google Scholar
• OLIVE PL, VIKSE CM, DURAND RE: Hypoxic fractions measured in murine tumors and normal tissues using the comet assay. Int. J. Radiat. Oncol. Biol. Phys. (1994) 29:487-491.
   PubMed Web of Science ®Google Scholar
• FAIRBAIRN DW, OLIVE PL, O'NEILL KL: The comet assay: a comprehensive review. Mutat. Res. (1995) 339:37-59.
   PubMed Web of Science ®Google Scholar
• WARTENBERG M, DÖNMEZ F, LING FC, ACKER H, HESCHELER J, SAUER H: Tumor-induced angiogenesis studied in confrontation cultures of multicellular tumor spheroids and embryoid bodies grown from pluripotent embryonic stem cells. FASEB J. (2001) 15:995-1005.
   PubMed Web of Science ®Google Scholar
• SHWEIKI D, ITIN A, SOFFER D, KESHET E: Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis. Nature (1992) 359:843-845.
   PubMed Web of Science ®Google Scholar
• TORRES FILHO IP, HARTLEY-ASP B, BORGSTROM P: Quantitative angiogenesis in a syngeneic tumor spheroid model. Microvas. Res. (1995) 49:212-226.
   PubMed Web of Science ®Google Scholar
• JELENA K, JENS K, FRAUKE A et al.: Dissociation of angiogenesis and tumorigenesis in follistatin- and activin-expressing tumors. Cancer Res. (2006) 66:5686-5695.
   PubMed Web of Science ®Google Scholar
• HAUPTMANN S, ZWADLO-KLARWASSER G, JANSEN M, KLOSTERHALFEN B, KIRKPATRICK CJ: Macrophages and multicellular tumor spheroids in co-culture: a three-dimensional model to study tumor-host interactions. Evidence for macrophage-mediated tumor cell proliferation and migration. Am. J. Pathol. (1993) 143:1406-1415.
   PubMed Web of Science ®Google Scholar
• FURBERT-HARRIS PM, LANIYAN I, HARRIS D et al.: Activated eosinophils infiltrate MCF-7 breast multicellular tumor spheroids. Anticancer Res. (2003) 23:71-78.
   PubMed Web of Science ®Google Scholar
• WEZEMAN FH, GUZZINO KM, WAXLER B: Multicellular tumor spheroid interactions with bone cells and bone. Anatomic. Rec. (2005) 213:111-120.
   Google Scholar
• WILSON KM, LORD EM: Effects of radiation on host-tumor interactions using the multicellular tumor spheroid model. Cancer Immunol. Immunother. (1986) 23:20-24.
   PubMed Web of Science ®Google Scholar
• BERENS ME, RUTKA JT, ROSENBLUM ML: Brain tumour epidemiology, growth, and invasion. Neurosurg. Clin. N. Am. (1990) 1:1-18.
   PubMedGoogle Scholar
• Brain Tumours. Kaye AH, Laws ER (Eds). Churchill Livingstone (1997) 990.
   Google Scholar
• SHAPIRO WR, SHAPIRO JR: Biology and treatment of malignant glioma. Oncology. (1998) 12:233-240.
   PubMed Web of Science ®Google Scholar
• LUND-JOHANSEN M, FORSBERG K, BJERKVIG R, LAERUM OD: Effects of growth factors on a human glioma cell line during invasion into rat brain aggregates in culture. Acta. Neuropathol. Berl. (1992) 84:190-197.
   Google Scholar
• BRACKE ME, VYNCKE BM, BRUYNEEL EA et al.: Insulin-like growth factor I activates the invasion suppressor function of E-cadherin in MCF-7 human mammary carcinoma cells in vitro. Br. J. Cancer (1993) 68:282-289.
   PubMed Web of Science ®Google Scholar
• SCHUSTER UR, BUTTNER F, HOFSTADTER, KNUCHEL R: A heterologous in vitro coculture system to study interaction between human bladder cancer cells and fibroblasts. J. Urol. (1994) 151:1707-1711.
   PubMed Web of Science ®Google Scholar
• SPITZ DR, SIM JE, RIDNOUR LA, GALOFORO SS, LEE YJ: Glucose deprivation-induced oxidative stress in human tumor cells. A fundamental defect in metabolism? Ann. N. Y. Acad. Sci. (2000) 899:349-362.
   Google Scholar
• LEE YJ, GALOFORO SS, BERNS CM: Glucose deprivation-induced cytotoxicity and alterations in mitogen-activated protein kinase activation are mediated by oxidative stress in multidrug-resistant human breast carcinoma cells. J. Biol. Chem. (1998) 273:5294-5299.
   PubMed Web of Science ®Google Scholar
• KUNDU N, ZHANG S, FULTON AM: Sublethal oxidative stress inhibits tumor cell adhesion and enhances experimental metastasis of murine mammary carcinoma. Clin. Exp. Metastasis. (1995) 13:16-22.
   PubMed Web of Science ®Google Scholar
• FULTON AM, CHONG YC: The role of macrophage-derived TNFα in the induction of sublethal tumor cell DNA damage. Carcinogenesis (1992) 13:77-81.
   PubMed Web of Science ®Google Scholar
• GOTTESMAN MM, PASTAN I: Biochemistry of multidrug resistance mediated by the multidrug transporter. Annu. Rev. Biochem. (1993) 62:385-427.
   PubMed Web of Science ®Google Scholar
• SIMON SM, SCHINDLER M: Cell biological mechanisms of multidrug resistance in tumors. Proc. Nat. Acad. Sci. (1994) 91:3497-3504.
   PubMed Web of Science ®Google Scholar
• VOLM M: Multidrug resistance and its reversal. Anticancer Res. (1998) 18(4C):2905-2917.
   PubMed Web of Science ®Google Scholar
• ODA Y, SCHNEIDER-STOCK R, RYS J, GRUCHALA A, NIEZABITOWSKI A, ROESSNER A: Reverse transcriptase- polymerase chain reaction amplification of MDR1 gene expression in adult soft tissue sarcomas. Diagn. Mol. Pathol. (1996) 5:98-106.
   PubMed Web of Science ®Google Scholar
• DHAR DK, NAGASUE N, YOSHIMURA H: Overexpression of P-glycoprotein in untreated AFP-producing gastric carcinoma. J. Surg. Oncol. (1995) 60:50-54.
   PubMed Web of Science ®Google Scholar
• PILARSKI LM, BELCH AR: Intrinsic expression of the multidrug transporter, P-glycoprotein 170, in multiple myeloma: implications for treatment. Leuk Lymphoma. (1995) 17:367-374.
   PubMed Web of Science ®Google Scholar
• MARIA W, FREY C, DIEDERSHAGEN H, RITGEN J, HESCHELER J, SAUER H: Development of an intrinsic P-glycoprotein-mediated doxorubicin resistance in quiescent cell layers of large, multicellular prostate tumor spheroids. Int. J. Cancer. (1998) 75:855-863.
   PubMed Web of Science ®Google Scholar
• MARIA W, HESCHELER J, HELMUT A, DIEDERSHAGEN H, SAUER H: Doxorubicin distribution in multicellular prostate cancer spheroids evaluated by confocal laser scanning microscopy and the optical probe technique. Cytometry. (1998) 31:137-145.
   PubMedGoogle Scholar
• MARIA W, FISCHER K, HESCHELER J, SAUER H: Redox regulation of P-glycoprotein-mediated multidrug resistance in multicellular prostate tumor spheroids. Int. J. Cancer. (2000) 85:267-274.
   PubMed Web of Science ®Google Scholar
• LEE YJ, GALOFORO SS, BERNS CM: Glucose deprivation-induced cytotoxicity and alterations in mitogen activated protein kinase activation are mediated by oxidative stress in multidrug-resistant human breast carcinoma cells. J. Biol. Chem. (1998) 273:294-299.
   Google Scholar
• VARSHNEY R, ADHIKARI JS, DWARAKANATH BS: Contribution of oxidative stress to radiosensitization by a combination of 2-DG and 6-AN in human cancer cell line. Ind. J Exp. Biol. (2003) 41:1384-1391.
   PubMedGoogle Scholar
• KHAITAN D, CHANDNA S, ARYA MB, DWARAKANATH BS: Differential mechanisms of radiosensitization by 2-deoxy-d-glucose in the monolayers and multicellular spheroids of a human glioma cell line. Cancer Biol. Ther. (2006) 5:e1-e10.
   Google Scholar
• LI CK: The glucose distribution in 9L rat brain multicell tumor spheroids and its effect on cell necrosis. Cancer. (1982) 50:2066-2073.
   PubMed Web of Science ®Google Scholar
• SANTINI MT, RAINALDI G, ROMANO R et al.: MG-63 human osteosarcoma cells grown in monolayer and as three-dimensional tumor spheroids present a different metabolic profile: a 1H NMR study. FEBS Lett. (2004) 557:148-154.
   PubMed Web of Science ®Google Scholar
• AZITA M, PASHA R, MARTIN S et al.: Multicellular tumour spheroid as a model for evaluation of [18F]FDG as biomarker for breast cancer treatment monitoring. Cancer Cell Int. (2006) 6:6.
   PubMedGoogle Scholar
• WALENTA S, DOETSCH J, MUELLER-KLIESER W, KUNZ-SCHUGHART LA: Metabolic imaging in multicellular spheroids of oncogene-transfected fibroblasts. J. Histochem. Cytochem. (2000) 48:509-522.
   PubMed Web of Science ®Google Scholar
• CASCIARI JJ, SOTIRCHOS SV, SUTHERLAND RM: Variations in tumor cell growth rates and metabolism with oxygen concentration, glucose concentration, and extracellular pH. J. Cell Physiol. (2005) 151:386-394.
   Google Scholar
• CHAPMAN JD, DUGLE DL, REUVERS AP, MEEKER BE, BORSA J: Studies on the radiosensitizing effect of oxygen in Chinese hamster cells. Int. J. Radiat. Biol. Relat. Stud. Phys. Chem. Med. (1974) 26:383-389.
   PubMed Web of Science ®Google Scholar
• ROFSTAD EK, WAHL A, BRUSTAD T: Radiation response of multicellular spheroids initiated from five human melanoma xenograft lines. Relationship to the radioresponsiveness in vivo. Br. J Radiol. (1986) 59:1023-1029.
   PubMed Web of Science ®Google Scholar
• WEST CM, SANDHU RR, STRATFORD IJ: The radiation response of V79 and human tumour multicellular spheroids – cell survival and growth delay studies. Br J Cancer. (1984) 50:143.
   PubMed Web of Science ®Google Scholar
• OLIVE PL, DURAND RE: Drug and radiation resistance in spheroids: cell contact and kinetics. Cancer Metastasis Rev. (1994) 13:121-138.
   PubMed Web of Science ®Google Scholar
• CORDES N, VAN BEUNINGEN D: Cell adhesion to the extracellular matrix protein fibronectin modulates radiation- dependent G2 phase arrest involving integrin-linked kinase (ILK) and glycogen synthase kinase-3P (GSK-3P) in vitro. Br. J. Cancer. (2003) 88:1470-1479.
   PubMed Web of Science ®Google Scholar
• CORDES N, MEINEKE V: Integrin signaling and the cellular response to ionizing radiation. J. Mol. Histol. (2004) 35:327-337
   PubMed Web of Science ®Google Scholar
• BEINKE C, VAN BEUNINGEN D, CORDES N: Ionizing radiation modulates expression and tyrosine phosphorylation of the focal adhesion-associated proteins focal adhesion kinase (FAK) and its substrates p130cas and paxillin in A549 human lung carcinoma cells in vitro. Int. J. Radiat. Biol. (2003) 79:721-731.
   PubMed Web of Science ®Google Scholar
• SCHWACHOFER JH, CROOIJMANS RP, VAN GASTEREN JJ et al.: Radiosensitivity of different human tumor cells lines grown as multicellular spheroids determined from growth curves and survival data. Int. J. Radiat. Oncol. Biol. Phys. (1989) 17:1015-1020.
   PubMed Web of Science ®Google Scholar
• SCHWACHOFER JH: Multicellular tumor spheroids in radiotherapy research (review). Anticancer Res. (1990) 10:963-969.
   PubMed Web of Science ®Google Scholar
• DWARKANATH BS, JAIN VK: Energy linked modification of the radiation response in human cerebral glioma cell line. Int. J. Rad. Oncl. Bio. Phys. (1989) 17:1033-1040.
   PubMed Web of Science ®Google Scholar
• DWARAKANATH BS, ZOLZAR FJ, CHANDNA S: Heterogeneity in 2-DG induced modifications in energetics and radiation responses of human tumor cell lines. Int. J. Rad. Onc. Bio. Phys. (2001) 50:1051-1061.
   PubMed Web of Science ®Google Scholar
• SINGH D, BANERJI AK, DWARAKANATH BS et al.: Optimizing cancer radiotherapy with 2-deosxy- d-glucose: dose escalation studies in patients with glioblastoma multiforme. Strahlentherapie (2005) 181:507-514.
   Google Scholar
• KUNZ-SCHUGHART LA, FREYER JP, HOFSTAEDTER F, EBNER R: The use of three-dimentional cultures for high throughput screening: the multicellular spheroid model. J. Biomol. Screen. (2004) 9:273-285.
   PubMed Web of Science ®Google Scholar
• TOFILON PJ, BUCKLEY N, DEEN DF: Effect of cell–cell interactions on drug sensitivity and growth of drug-sensitive and -resistant tumor cells in spheroids. Science (1984) 226:862-864.
   PubMed Web of Science ®Google Scholar
• ERLICHMAN C, VIDGEN D: Cytotoxicity of adriamycin in MGH-U1 cells grown as monolayer cultures, spheroids and xenografts in immune-deprived mice. Cancer Res. (1984) 44:5369-5375.
   PubMed Web of Science ®Google Scholar
• FREEMAN AE, HOFFMAN RM: In vivo-like growth of human tumors in vitro. Proc. Natl. Acad. Sci. USA (1986) 83:2694-2698.
   PubMed Web of Science ®Google Scholar
• MILLER BE, MILLER FR, HEPPNER GH: Interactions between tumor subpopulations affecting their sensitivity to the antineoplastic agents cyclophosphamide and methotrexate. Cancer Res. (1981) 41:4378-4381.
   PubMed Web of Science ®Google Scholar
• BRAD ST, JANUSZ WR, SEAN K, CAPUCINE S, CHARLES HG, ROBERT SK: Reversal by hyaluronidase of adhesion-dependent multicellular drug resistance in mammary carcinoma cells. J. Nat. Cancer Inst. (1996) 88:285-1296.
   Web of Science ®Google Scholar
• SHANE KG, GIULIO F, CIRO I, ROBERT SK: Antiadhesive antibodies targeting E-cadherin sensitize multicellular tumor spheroids to chemotherapy in vitro. Mol. Cancer Ther. (2004) 3:149-159.
   PubMed Web of Science ®Google Scholar
• BARTHOLOMÄ P, IMPIDJATI A, REININGER-MACK, ZHIHONG Z, THIELECKE H, ROBITZKI A: More aggressive breast cancer spheroid model coupled to an electronic capillary sensor system for a high-content screening of cytotoxic agents in cancer therapy: three-dimensional in vitro tumor spheroids as a screening model. J. Biomol. Screen. (2005) 10:705-714.
   Google Scholar
• MADSEN SJ, SUN CH, TROMBERG BJ, HIRSCHBERG H: Repetitive 5-aminolevulinic acid-mediated photodynamic therapy on human glioma spheroids. J. Neuro-Oncol. (2003) 62:243-250.
   PubMed Web of Science ®Google Scholar
• HIRSCHBERG H, SUN CH, TROMBERG BJ, YEH AT, MADSEN SJ: Enhanced effects of concurrent 5-aminolevulinic acid-mediated photodynamic therapy by hyperthermia on human glioma spheroids. J. Neuro-Oncol. (2004) 70:289-299.
   PubMed Web of Science ®Google Scholar
• LAMFERS ML, HEMMINKI A: Multicellular tumor spheroids in gene therapy and oncolytic virus therapy. Curr. Opin. Mol. Ther. (2004) 6:403-411.
   PubMed Web of Science ®Google Scholar
• BOYD M, MAIRS RJ, CUNNINGHAM SH et al.: A gene therapy/targeted radiotherapy strategy for radiation cell kill. J. Gene Med. (2001) 3(2):165-172.
   Google Scholar
• BOYD M, MAIRS RJ, KEITH WN et al.: An efficient targeted radiotherapy/gene therapy strategy utilising human telomerase promoters and radioastatine and harnessing radiation-mediated bystander effects. J. Gene Med. (2004) 6:937-947.
   PubMed Web of Science ®Google Scholar
• GAZE MN, MAIRS RJ, BOYACK SM, WHELDON TE, BARRETT A: 131I-meta-iodobenzylguanidine therapy in neuroblastoma spheroids of different sizes. Br. J. Cancer (1992) 66(6):1048-1052.
   PubMed Web of Science ®Google Scholar
• LINDSTROM A, CARLSSON J: Penetration and binding of epidermal growth factor-dextran conjugates in spheroids of human glioma origin. Cancer Biother. (1993) 8(2):145-158.
   PubMedGoogle Scholar
• BISHAYEE A, HILL HZ, STEIN D, RAO DV, HOWELL RW: Free radical- initiated and gap junction-mediated bystander effect due to nonuniform distribution of incorporated radioactivity in a three-dimensional tissue culture model. Radiat. Res. (2001) 155:335-344.
   PubMed Web of Science ®Google Scholar