Effect of therapeutic macromolecules in spheroids.
Abstract
Recent advances in biotechnology have allowed the production of new types of macromolecular therapeutic agents (antibodies, immunotoxins, cytokines, extracellular matrix molecule (ECM) proteins, vectors) that may eventually find broad clinical applications in the treatment of human tumors and other diseases. The model of the Multicellular Tumor Spheroids (MTS) represents a valuable tool to test the therapeutic potential of these new pharmacologic agents in a 3-D context. Specific questions pertaining to the behaviour in a 3-D setting of some of the macromolecules under evaluation for in vivo applications can also be addressed in the MTS model (e.g. 'binding site barrier', role of cell-cell and cell-ECM interactions). This paper reviews the most significant contributions regarding the delivery of macromolecules to MTS, the penetration and therapeutic effects of antibodies, radiolabelled antibodies, immunotoxins and other macromolecular compounds.
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Mohanam, S., Chintala, S. K., Go, Y., Bhattacharya, A., Venkaiah, B., Boyd, D. D., Gokaslan, Z. L., Sawaya, R. A., & Rao, J. S. (1997) · Oncogene · doi:10.1038/sj.onc.1200963 · Cited by 99 · see citing works
RetractedEstablishment in culture of pluripotential cells from mouse embryos
Evans, M. J., & Kaufman, M. H. (1981) · Nature · doi:10.1038/292154a0 · Cited by 8,623 · see citing works
Cell and environment interactions in tumor microregions: the multicell spheroid model.
Sutherland, R. M. (1988) · Science · doi:10.1126/science.2451290 · Cited by 1,803 · see citing works
Glycosphingolipids in Cellular Interaction, Differentiation, and Oncogenesis
Hakomori, S. (1981) · Annual Review of Biochemistry · doi:10.1146/annurev.bi.50.070181.003505 · Cited by 1,643 · see citing works
Colorectal carcinoma antigens detected by hybridoma antibodies
Koprowski, H., Steplewski, Z., Mitchell, K. F., Herlyn, M., Herlyn, D., & Fuhrer, P. (1979) · Somatic Cell and Molecular Genetics · doi:10.1007/bf01542654 · Cited by 1,360 · see citing works
The Gompertz Curve as a Growth Curve
Winsor, C. P. (1932) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.18.1.1 · Cited by 1,007 · see citing works
Laird, A. K. (1964) · British Journal of Cancer · doi:10.1038/bjc.1964.55 · Cited by 880 · see citing works
One molecule of diphtheria toxin fragment a introduced into a cell can kill the cell
Yamaizumi, M., Mekada, E., Uchida, T., & Okada, Y. (1978) · Cell · doi:10.1016/0092-8674(78)90099-5 · Cited by 745 · see citing works
Sethi, T., Rintoul, R. C., Moore, S. M., MacKinnon, A. C., Salter, D. M., Choo, C., Chilvers, E. R., Dransfield, I., Donnelly, S. C., Strieter, R. M., et al. (1999) · Nature Medicine · doi:10.1038/9511 · Cited by 739 · see citing works
Bremer, E. G., Schlessinger, J., & Hakomori, S. (1986) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)35954-9 · Cited by 706 · see citing works
Delivery of Novel Therapeutic Agents in Tumors: Physiological Barriers and Strategies
Jain, R. K. (1989) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/81.8.570 · Cited by 564 · see citing works
A simplified method for production and growth of multicellular tumor spheroids.
Yuhas, J. M., Li, A. P., Martinez, A. O., & Ladman, A. J. (1977) · PubMed · Cited by 506 · see citing works
Lasic, D. D., & Papahadjopoulos, D. (1995) · Science · doi:10.1126/science.7871422 · Cited by 434 · see citing works
Juweid, M. E., Neumann, R. D., Paik, C. H., Pérez-Bacete, M., Sato, J., van Osdol, W. W., & Weinstein, J. N. (1992) · PubMed · Cited by 406 · see citing works
SR-4233: A new bioreductive agent with high selective toxicity for hypoxic mammalian cells
Zeman, E. M., Brown, J. M., Lemmon, M. J., Hirst, V. K., & Lee, W. W. (1986) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/0360-3016(86)90267-1 · Cited by 402 · see citing works
Ribosome‐inactivating proteins up to date
Stirpe, F., & Barbieri, L. L. (1986) · FEBS Letters · doi:10.1016/0014-5793(86)80118-1 · Cited by 388 · see citing works
Dynamics of Tumour Growth: Comparison of Growth Rates and Extrapolation of Growth Curve to One Cell
Laird, A. K. (1965) · British Journal of Cancer · doi:10.1038/bjc.1965.32 · Cited by 308 · see citing works
Entry of lethal doses of abrin, ricin and modeccin into the cytosol of HeLa cells
Eiklid, K. L., Olsnes, S., & Pihl, A. (1980) · Experimental Cell Research · doi:10.1016/0014-4827(80)90270-0 · Cited by 303 · see citing works
Antibodies against metal chelates
Reardan, D. T., Meares, C. F., Goodwin, D. A., McTigue, M., David, G. S., Stone, M. R., Leung, J. P., Bartholomew, R. M., & Frincke, J. M. (1985) · Nature · doi:10.1038/316265a0 · Cited by 260 · see citing works
Apoptosis induced by inhibition of intercellular contact.
Bates, R. C., Buret, A. G., Helden, D. F. V., Horton, M. A., & Burns, G. F. (1994) · The Journal of Cell Biology · doi:10.1083/jcb.125.2.403 · Cited by 244 · see citing works
Bacha, P., Williams, D. P., Waters, C. A., Williams, J. M., Murphy, J. R., & Strom, T. B. (1988) · The Journal of Experimental Medicine · doi:10.1084/jem.167.2.612 · Cited by 220 · see citing works
Dosimetric aspects of radiolabeled antibodies for tumor therapy.
Humm, J. L. (1986) · PubMed · Cited by 213 · see citing works
A Multi-component Radiation Survival Curve Using anin VitroTumour Model
Sutherland, R. M., Inch, W. R., McCredie, J. A., & Kruuv, J. (1970) · International Journal of Radiation Biology and Related Studies in Physics Chemistry and Medicine · doi:10.1080/09553007014551401 · Cited by 201 · see citing works
Youle, R. J., & Neville, D. M. (1982) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)68077-4 · Cited by 196 · see citing works
Casellas, P., Bourrié, B., Gros, P., & Jansen, F. K. (1984) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)42707-4 · Cited by 194 · see citing works
Grimm, E. A. (1994) · Lung Cancer · doi:10.1016/0169-5002(94)92198-9 · Cited by 191 · see citing works
Mutations in Diphtheria Toxin Separate Binding from Entry and Amplify Immunotoxin Selectivity
Greenfield, L., Johnson, V. G., & Youle, R. J. (1987) · Science · doi:10.1126/science.3498987 · Cited by 175 · see citing works
Engebraaten, O., Bjerkvig, R., Pedersen, P., & Lærum, O. D. (1993) · International Journal of Cancer · doi:10.1002/ijc.2910530206 · Cited by 159 · see citing works
Thrush, G. R., Lr, L., Clinchy, B., & Vitetta, E. S. (1996) · Annual Review of Immunology · doi:10.1146/annurev.immunol.14.1.49 · Cited by 159 · see citing works
Fluence rate effects in photodynamic therapy of multicell tumor spheroids.
Foster, T. H., Hartley, D. F., Nichols, M. G., & Hilf, R. (1993) · PubMed · Cited by 157 · see citing works
DTPA-coupled antibodies labeled with yttrium-90.
Hnatowich, D. J., Virzi, F., & Doherty, P. W. (1985) · PubMed · Cited by 155 · see citing works
Vadhan‐Raj, S., Cordon‐Cardo, C., Carswell, E. A., Mintzer, D. M., Dantis, L., Duteau, C., Templeton, M. A., Oettgen, H. F., Old, L. J., & Houghton, A. N. (1988) · Journal of Clinical Oncology · doi:10.1200/jco.1988.6.10.1636 · Cited by 155 · see citing works
Sutherland, R. M., Buchegger, F., Schreyer, M., Vacca, A., & Mach, J. (1987) · PubMed · Cited by 151 · see citing works
Steinbach, P., Wedmgandt, H., Baumgartner, R., Kriegmair, M., Hofstädter, F., & Knüchel, R. (1995) · Photochemistry and Photobiology · doi:10.1111/j.1751-1097.1995.tb09152.x · Cited by 141 · see citing works
Efficient assembly of rat hepatocyte spheroids for tissue engineering applications
Wu, F. J., Friend, J. R., Hsiao, C. C., Zilliox, M. J., Ko, W., Cerra, F. B., & Hu, W. (1996) · Biotechnology and Bioengineering · doi:10.1002/(sici)1097-0290(19960520)50:4 · Cited by 139 · see citing works
Tenascin mediates human glioma cell migration and modulates cell migration on fibronectin
Deryugina, E. I., & Bourdon, M. A. (1996) · Journal of Cell Science · doi:10.1242/jcs.109.3.643 · Cited by 136 · see citing works
Growth of nodular carcinomas in rodents compared with multi-cell spheroids in tissue culture.
Inch, W. R., Ja, M., & Rm, S. (1970) · PubMed · Cited by 135 · see citing works
Tunggal, J. K., Cowan, D., Shaikh, H., & Tannock, I. F. (1999) · PubMed · Cited by 133 · see citing works
The Pharmacology of Monoclonal Antibodiesa
Weinstein, J. N., Eger, R. R., Covell, D. G., BLACK, C. D. V., Mulshine, J. L., Carrasquillo, J. A., Larson, S. M., & Keenan, A. M. (1987) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1987.tb45802.x · Cited by 127 · see citing works
Body-size indicators and risk of breast cancer according to menopause and estrogen-receptor status
Männistö, S., Pietinen, P., Pyy, M., Palmgren, J., Eskelinen, M. J., & Uusitupa, M. I. J. (1996) · International Journal of Cancer · doi:10.1002/(sici)1097-0215(19960927)68:1 · Cited by 126 · see citing works
Inhibition of Human Acute Lymphoblastic Leukemia Cells by Immunotoxins: Potentiation by Chloroquine
Ramakrishnan, S., & Houston, L. L. (1984) · Science · doi:10.1126/science.6318313 · Cited by 120 · see citing works
3-D Coculture of Hepatic Sinusoidal Cells with Primary Hepatocytes—Design of an Organotypical Model
Bader, A., Knop, E., Kern, A., Böker, K. H. W., Frühauf, N. R., Crome, O., Esselmann, H., Pape, C., Kempka, G., & Sewing, K. ‐. (1996) · Experimental Cell Research · doi:10.1006/excr.1996.0222 · Cited by 119 · see citing works
Photobleaching of protoporphyrin IX in cells incubated with 5-aminolevulinic acid
Moan, J. E., Streckytė, G., Bagdonas, S., Gadmar, Ø. B., & Berg, K. (1997) · International Journal of Cancer · doi:10.1002/(sici)1097-0215(19970106)70:1 · Cited by 118 · see citing works
An immunotoxin prepared with blocked ricin: a natural plant toxin adapted for therapeutic use.
Lambert, J., Goldmacher, V. S., Collinson, A. R., Nadler, L. M., & Blättler, W. A. (1991) · PubMed · Cited by 116 · see citing works
Comparative serum stability of radiochelates for antibody radiopharmaceuticals.
Cole, W. C., DeNardo, S. J., Meares, C. F., McCall, M. J., DeNardo, G. L., Epstein, A. L., O'Brien, H. A., & Moi, M. K. (1987) · PubMed · Cited by 108 · see citing works
Spheroid Culture in Cancer Research (1991)
(2017) · CRC Press eBooks · doi:10.1201/9780203710241 · Cited by 106 · see citing works
A chloride current associated with swelling of cultured chick heart cells.
Zhang, J., Rasmusson, R. L., Hall, S., & Lieberman, M. A. (1993) · The Journal of Physiology · doi:10.1113/jphysiol.1993.sp019974 · Cited by 97 · see citing works
Paulus, W., Huettner, C. S., & Tonn, J. C. (1994) · International Journal of Cancer · doi:10.1002/ijc.2910580616 · Cited by 97 · see citing works
Blockade of the galactose‐binding sites of ricin by its linkage to antibody
Thorpe, P. E., Ross, W. C. J., Brown, A. N. F., Myers, C. D., Cumber, A. J., Foxwell, B. M. J., & FORRESTER, J. T. (1984) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1984.tb08067.x · Cited by 94 · see citing works
Order, S. E., Klein, J. L., Ettinger, D. S., Alderson, P. O., Siegelman, S. S., & Leichner, P. K. (1980) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/0360-3016(80)90226-6 · Cited by 89 · see citing works
Cell culture as spheroids: an approach to multicellular resistance.
Desoize, B., Gimonet, D., & Jardiller, J. C. (1999) · PubMed · Cited by 88 · see citing works
A flow injection flow cytometry system for on-line monitoring of bioreactors
Zhao, R., Natarajan, A., & Srienc, F. (1999) · Biotechnology and Bioengineering · doi:10.1002/(sici)1097-0290(19990305)62:5 · Cited by 85 · see citing works
Phillips, R. M., Loadman, P. M., & Cronin, B. (1998) · British Journal of Cancer · doi:10.1038/bjc.1998.355 · Cited by 81 · see citing works
Colombatti, M., Greenfield, L., & Youle, R. J. (1986) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)35741-1 · Cited by 77 · see citing works
Characterization of Morphology and Cellular Metabolism during the Spheroid Formation by Fibroblasts
Takezawa, T., Mori, Y., Yonaha, T., & Yoshizato, K. (1993) · Experimental Cell Research · doi:10.1006/excr.1993.1265 · Cited by 77 · see citing works
Carboxylic ionophores enhance the cytotoxic potency of ligand- and antibody-delivered ricin A chain.
Raso, V., & Lawrence, J. (1984) · The Journal of Experimental Medicine · doi:10.1084/jem.160.4.1234 · Cited by 77 · see citing works
Interleukin 2-diphtheria toxin fusion protein can abolish cell-mediated immunity in vivo.
Kelley, V. E., Bacha, P., PANKEWYCZ, O. G., NICHOLS, J. C., Murphy, J. R., & Strom, T. B. (1988) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.85.11.3980 · Cited by 76 · see citing works
Skin Fibroblasts Are the Only Source of Nidogen During Early Basal Lamina Formation In Vitro
Fleischmajer, R., Schechter, A. N., Bruns, M., Perlish, J. S., MacDonald, E. D., Pan, T., Timpl, R., & Chu, M.-L. (1995) · Journal of Investigative Dermatology · doi:10.1111/1523-1747.ep12323604 · Cited by 74 · see citing works
Membrane-mediated cytotoxicity
(1986) · Journal of Cellular Biochemistry · doi:10.1002/jcb.240320603 · Cited by 73 · see citing works
Ionic basis of the chronotropic effect of acetylcholine on the rabbit sinoatrial node
Boyett, M. R., Kodama, I., Honjo, H., Arai, A., Suzuki, R., & Toyama, J. (1995) · Cardiovascular Research · doi:10.1016/s0008-6363(96)88625-1 · Cited by 68 · see citing works
Leptomeningeal Tissue: a Barrier Against Brain Tumor Cell Invasion
Pedersen, P., Rucklidge, G. J., Mørk, S. J., Terzis, A. J. A., Engebraaten, O., Lund‐Johansen, M., Backlund, E.-O., Lærum, O. D., & Bjerkvig, R. (1994) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/86.21.1593 · Cited by 63 · see citing works
Tibben, J. G., Boerman, O. C., Massuger, L. F. A. G., Schijf, C. P. T., Claessens, R. A. M. J., & Corstens, F. H. M. (1996) · International Journal of Cancer · doi:10.1002/(sici)1097-0215(19960516)66:4 · Cited by 60 · see citing works
Tumor Therapy by Immune Recruitment with Bispecific Antibodies
Renner, C., & Pfreundschuh, M. (1995) · Immunological Reviews · doi:10.1111/j.1600-065x.1995.tb00082.x · Cited by 58 · see citing works
Pullarkat, V., Deo, Y., Link, J., Spears, L., Marty, V., Curnow, R., Groshen, S., Gee, C., & Weber, J. S. (1999) · Cancer Immunology, Immunotherapy · doi:10.1007/s002620050543 · Cited by 55 · see citing works
Self-diffusion of water in multicellular spheroids measured by magnetic resonance microimaging.
Neeman, M., JARRETT, K. A., Sillerud, L. O., & Freyer, J. P. (1991) · PubMed · Cited by 53 · see citing works
Selective down-regulation of integrin receptors in spheroids of squamous cell carcinoma.
Waleh, N. S., Gallo, J., Grant, T. D., Murphy, B. J., Kramer, R. H., & Sutherland, R. M. (1994) · PubMed · Cited by 53 · see citing works
Lund‐Johansen, M., Forsberg, K., Bjerkvig, R., & Lærum, O. D. (1992) · Acta Neuropathologica · doi:10.1007/bf00311394 · Cited by 53 · see citing works
Freyer, J. P., Schor, P. L., JARRETT, K. A., Neeman, M., & Sillerud, L. O. (1991) · PubMed · Cited by 51 · see citing works
Klein, U., & Zimmermann, B. B. (1991) · Cell and Tissue Research · doi:10.1007/bf00318182 · Cited by 50 · see citing works
Chan, W., West, C., Moore, J., & Hart, I. (1991) · British Journal of Cancer · doi:10.1038/bjc.1991.408 · Cited by 49 · see citing works
Langmuir, V. K., Mendonca, H. L., & Woo, D. V. (1992) · PubMed · Cited by 47 · see citing works
Hauptmann, S., Denkert, C., Löhrke, H., Tietze, L., Ott, S. J., Klosterhalfen, B., & Mittermayer, C. (1995) · International Journal of Cancer · doi:10.1002/ijc.2910610613 · Cited by 46 · see citing works
Potentiation of cytotoxic activity of immunotoxins on cultured human cells.
Akiyama, S., Seth, P. K., Pirker, R., Fitzgerald, D., Gottesman, M. M., & Pastan, I. H. (1985) · PubMed · Cited by 45 · see citing works
Ronen, S. M., Rushkin, E., & Degani, H. (1992) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/0925-4439(92)90039-p · Cited by 43 · see citing works
Jääskeläinen, J. E., Kalliomäki, P., Paetau, A. E., & Timonen, T. T. (1989) · The Journal of Immunology · doi:10.4049/jimmunol.142.3.1036 · Cited by 39 · see citing works
Interaction of liposome-associated all- trans- retinoic acid with squamous carcinoma cells
Parthasarathy, R. V., Sacks, P. G., Harris, D., Brock, H., & Mehta, K. (1994) · Cancer Chemotherapy and Pharmacology · doi:10.1007/bf00685666 · Cited by 37 · see citing works
Barnea, A., Cho, G., Lü, G., & Mathis, J. M. (1995) · Journal of Neuroscience Research · doi:10.1002/jnr.490420506 · Cited by 36 · see citing works
Colombatti, M., Dell'Arciprete, L., Chignola, R., & Tridente, G. (1990) · PubMed · Cited by 36 · see citing works
Sensitivity of human glioma cells to cytotoxic heteroconjugates
Colombatti, M., Bisconti, M., Dell'Arciprete, L., Gerosa, M. A., & Tridente, G. (1988) · International Journal of Cancer · doi:10.1002/ijc.2910420322 · Cited by 36 · see citing works
McFadden, R., & Kwok, C. S. (1988) · PubMed · Cited by 35 · see citing works
Kinetics of Cytotoxicity Induced by Immunotoxins
Casellas, P., Bourrié, B., Gros, P., & Jansen, F. K. (1984) · Cited by 35 · see citing works
Proton NMR Microscopy of Multicellular Tumor Spheroid Morphology
Sillerud, L. O., Freyer, J. P., Neeman, M., & Mattingly, M. A. (1990) · Magnetic Resonance in Medicine · doi:10.1002/mrm.1910160304 · Cited by 34 · see citing works
Guillonneau, X., Tassin, J., Berrou, E., Bryckaert, M., Courtois, Y., & Mascarelli, F. (1996) · Journal of Cellular Physiology · doi:10.1002/(sici)1097-4652(199601)166:1 · Cited by 33 · see citing works
Essand, M., Grönvik, C., Hartman, T., & Carlsson, J. (1995) · International Journal of Cancer · doi:10.1002/ijc.2910630315 · Cited by 33 · see citing works
Heterogeneous response of individual multicellular tumour spheroids to immunotoxins and ricin toxin
Chignola, R., Foroni, R. I., Franceschi, A., Pasti, M., Candiani, C., Anselmi, C., Fracasso, G., Tridente, G., & Colombatti, M. (1995) · British Journal of Cancer · doi:10.1038/bjc.1995.381 · Cited by 32 · see citing works
Self-citationde Palazzo, I. G., Gerçel-Taylor, Ç., Kitson, J., & Weiner, L. M. (1990) · PubMed · Cited by 32 · see citing works
Bardiès, M., Thédrez, P., Gestin, J., Marcille, B., Guerreau, D., Faivre-Chauvet, A., Mahé, M. A., Maurel, C., & Chatal, J. (1992) · International Journal of Cancer · doi:10.1002/ijc.2910500627 · Cited by 31 · see citing works
Role of chloride currents in repolarizing rabbit atrial myocytes
Wang, Z., Fermini, B., Feng, J., & Nattel, S. (1995) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1995.268.5.h1992 · Cited by 31 · see citing works
Pervez, S., Kirkland, S. C., Epenetos, A. A., Mooi, W. J., Evans, D. J., & Krausz, T. N. (1989) · International Journal of Cancer · doi:10.1002/ijc.2910440532 · Cited by 30 · see citing works
Multicellular tumor spheroids in radiotherapy research (review).
Jh, S. (1990) · PubMed · Cited by 29 · see citing works
Automated selective dissociation of cells from different regions of multicellular spheroids
Freyer, J. P., & Schor, P. L. (1989) · In Vitro Cellular & Developmental Biology - Plant · doi:10.1007/bf02624405 · Cited by 28 · see citing works
Freyer, J. P., Fink, N. H., Schor, P. L., Coulter, J. R., Neeman, M., & Sillerud, L. O. (1990) · NMR in Biomedicine · doi:10.1002/nbm.1940030502 · Cited by 28 · see citing works
131I-anticarcinoembryonic antigen therapy of LS174T human colon adenocarcinoma spheroids.
Langmuir, V. K., McGann, J. K., Buchegger, F., & Sutherland, R. M. (1989) · PubMed · Cited by 28 · see citing works
A tumour spheroid model for antibody-targeted therapy of micrometastases
Walker, K. A., Murray, T. J., Hilditch, T., Wheldon, T. E., Gregor, A., & Hann, I. M. (1988) · British Journal of Cancer · doi:10.1038/bjc.1988.152 · Cited by 27 · see citing works
Targeting Radiation to Tumours
Wheldon, T. E. (1994) · International Journal of Radiation Biology · doi:10.1080/09553009414550151 · Cited by 26 · see citing works
Diffusion and Binding of Monoclonal Antibody TNT-1 in Multicellular Tumor Spheroids
Chen, F.-M., Hansen, E. B., Taylor, C. R., & Epstein, A. L. (1991) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/83.3.200 · Cited by 26 · see citing works
Tatsukawa, Y., Arita, M., Kiyosue, T., Mikuriya, Y., & Nasu, M. (1993) · Journal of Molecular and Cellular Cardiology · doi:10.1006/jmcc.1993.1083 · Cited by 25 · see citing works
Carlsson, J., Daniel-Szolgay, E., Frykholm, G. J., Glimelius, B. L. G., Hedin, A., & Larsson, B. S. (1989) · Cancer Immunology Immunotherapy · doi:10.1007/bf01744893 · Cited by 24 · see citing works
Effects of cellular pharmacology on drug distribution in tissues
Rippley, R. K., & Stokes, C. L. (1995) · Biophysical Journal · doi:10.1016/s0006-3495(95)79956-8 · Cited by 23 · see citing works
Mairs, R., Angerson, W. J., Gaze, M. N., Murray, T. J., Babich, J., Reid, R., & McSharry, C. P. (1991) · British Journal of Cancer · doi:10.1038/bjc.1991.93 · Cited by 23 · see citing works
Li, G., Feng, J., Shrier, A., & Nattel, S. (1995) · The Journal of Physiology · doi:10.1113/jphysiol.1995.sp020692 · Cited by 23 · see citing works
Ihara, S., Watanabe, M., Nagao, E., & Shioya, N. (1991) · Cell and Tissue Research · doi:10.1007/bf00678712 · Cited by 23 · see citing works
Shevchuk, I. N., Chekulayev, V. A., Moan, J. E., & Berg, K. (1996) · International Journal of Cancer · doi:10.1002/(sici)1097-0215(19960917)67:6 · Cited by 22 · see citing works
Langmuir, V. K., McGann, J. K., Buchegger, F., & Sutherland, R. M. (1991) · International Journal of Radiation Applications and Instrumentation Part B Nuclear Medicine and Biology · doi:10.1016/0883-2897(91)90014-c · Cited by 22 · see citing works
Resistance of ovarian teratocarcinoma cell spheroids to complement-mediated lysis
Bjørge, L., Junnikkala, S., Kristoffersen, E., Hakulinen, J., Matre, R., & Meri, S. (1997) · British Journal of Cancer · doi:10.1038/bjc.1997.213 · Cited by 22 · see citing works
Anti-GM2 monoclonal antibodies induce necrosis in GM2-rich cultures of a human glioma cell line.
Bjerkvig, R., Engebraaten, O., Lærum, O. D., Fredman, P., Svennerholm, L. T., Vrionis, F. D., Wikstrand, C. J., & Bigner, D. D. (1991) · PubMed · Cited by 21 · see citing works
Antitumor effects of a bispecific antibody targeting CA19-9 antigen and CD16.
de Palazzo, I. G., Holmes, M., Gerçel-Taylor, Ç., & Weiner, L. M. (1992) · PubMed · Cited by 21 · see citing works
Dynorphins Modulate DNA Synthesis in Fetal Brain Cell Aggregates
Gorodinsky, A., Barg, J., Belcheva, M. M., Levy, R., McHale, R. J., Vogel, Z., & Coscia, C. J. (1995) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1995.65041481.x · Cited by 21 · see citing works
MECHANISMS BEHIND THE RESISTANCE OF SPHEROIDS TO PHOTODYNAMIC TREATMENT: A FLOW CYTOMETRY STUDY
West, C., & Moore, J. V. (1992) · Photochemistry and Photobiology · doi:10.1111/j.1751-1097.1992.tb04257.x · Cited by 21 · see citing works
Iwasaki, K., Kikuchi, H., Miyatake, S.-I., Aoki, T., Yamasaki, T., & Oda, Y. (1990) · PubMed · Cited by 21 · see citing works
Optimization of radioimmunotherapy using human malignant melanoma multicell spheroids as a model.
Kwok, C. S., Crivici, A., MacGregor, W. D., & UNGER, M. W. (1989) · PubMed · Cited by 21 · see citing works
Casellas, P., Ravel, S. J., Bourrié, B., Derocq, J., Jansen, F. K., Laurent, G., & Gros, P. (1988) · Blood · doi:10.1182/blood.v72.4.1197.1197 · Cited by 21 · see citing works
The Combined Use of 131 I-Labeled Antibody and the Hypoxic Cytotoxin SR 4233 in Vitro and in Vivo
Langmuir, V. K., & Mendonca, H. L. (1992) · Radiation Research · doi:10.2307/3578244 · Cited by 20 · see citing works
Amantadine potentiates T lymphocyte killing by an anti-pan-T cell (CD5) ricin A-chain immunotoxin
Siena, S., Villa, S., Bregni, M., Bonadonna, G., & Am, G. (1987) · Blood · doi:10.1182/blood.v69.1.345.345 · Cited by 20 · see citing works
Laminin: a potential inhibitor of rat glioma cell invasion in vitro.
Reith, A., Bjerkvig, R., & Gj, R. (1994) · PubMed · Cited by 20 · see citing works
Candiani, C., Franceschi, A., Chignola, R., Pasti, M., Anselmi, C., Benoni, G., Tridente, G., & Colombatti, M. (1992) · PubMed · Cited by 18 · see citing works
Hjelstuen, M. H. B., Rasch-Halvorsen, K., Brekken, C., Bruland, Ø. S., & Davies, C. D. L. (1996) · Acta Oncologica · doi:10.3109/02841869609101641 · Cited by 17 · see citing works
Editorial: Your paper has been accepted
Murray, A. (1999) · Medical & Biological Engineering & Computing · doi:10.1007/bf02513257 · Cited by 14 · see citing works
Comparisons of the efficacy of 186Re- and 131I-labeled antibody in multicell spheroids
Langmuir, V. K., Mendonca, H. L., Vanderheyden, J., & Su, F. (1992) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/0360-3016(92)91031-h · Cited by 14 · see citing works
Chignola, R., Foroni, R. I., Candiani, C., Franceschi, A., Pasti, M., Stevanoni, G., Anselmi, C., Tridente, G., & Colombatti, M. (1994) · International Journal of Cancer · doi:10.1002/ijc.2910570223 · Cited by 14 · see citing works
Griffin, T. W., Childs, L. R., FitzGerald, D. J., & Levin, L. V. (1987) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/79.4.679 · Cited by 14 · see citing works
Olabiran, Y., Ledermann, J. A., Marston, N., Boxer, G., Hicks, R. J., Souhami, R. L., Spiro, S. G., & Stahel, R. A. (1994) · British Journal of Cancer · doi:10.1038/bjc.1994.47 · Cited by 13 · see citing works
Clay, J. R., Kristof, A. S., Shenasa, J., Brochu, R. M., & Shrier, A. (1994) · Progress in Biophysics and Molecular Biology · doi:10.1016/0079-6107(94)90011-6 · Cited by 12 · see citing works
Embleton, M. J., Charleston, A., & Affleck, K. (1991) · International Journal of Cancer · doi:10.1002/ijc.2910490416 · Cited by 10 · see citing works
A Novel Monoclonal Antibody, L1A3, Is Directed to the Functional Site of the α v Integrin Subunit
Deryugina, E. I., Strongin, A. Y., YU, C., & Bourdon, M. A. (1996) · Hybridoma · doi:10.1089/hyb.1996.15.279 · Cited by 10 · see citing works
Comparisons of sectioned micro‐TLD dose measurements with predicted dose from 131I‐labeled antibody
Langmuir, V. K., Wessels, B. W., Mendonca, H. L., Yorke, E. D., & Montilla, L. (1992) · Medical Physics · doi:10.1118/1.596753 · Cited by 10 · see citing works
Jääskeläinen, J. E., Lehtonen, E., Heikkilä, P., Kalliomäki, P. ‐., & Timonen, T. T. (1990) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/82.6.497 · Cited by 10 · see citing works
Tw, G., Pagnini, P., & Houston, L. L. (1987) · PubMed · Cited by 10 · see citing works
Penetration of anti-melanoma immunotoxin into multicellular tumor spheroids and cell kill effects
Kikuchi, T., Ohnuma, T., Holland, J. F., & S̄pitler, L. E. (1992) · Cancer Immunology Immunotherapy · doi:10.1007/bf01741142 · Cited by 8 · see citing works
Effects of131I-labeled TNT-1 radioimmunotherapy on HT-29 human colon adenocarcinoma spheroids
Chen, F., Liu, C.-Z., & Epstein, A. L. (1991) · Cancer Immunology Immunotherapy · doi:10.1007/bf01756136 · Cited by 7 · see citing works
Response of multicellular tumor spheroids to liposomes containing TNF-?
Weber, F., Kremer, C., Klinkhammer, M., Rasier, B., & Brock, M. (1994) · Journal of Neuro-Oncology · doi:10.1007/bf01328956 · Cited by 7 · see citing works
Rabkin, S. W. (1993) · General Pharmacology The Vascular System · doi:10.1016/0306-3623(93)90234-o · Cited by 7 · see citing works
Hjelstuen, M., Rasch-Halvorsen, K., Bruland, Ø. S., & Davies, C. D. L. (1998) · PubMed · Cited by 7 · see citing works
Cell death induced by a 131I-labeled monoclonal antibody in ovarian cancer multicell spheroids
Filippovich, I. V., Sorokina, N., Robillard, N., Faivre-Chauvet, A., Bardiès, M., & Chatal, J. (1996) · Nuclear Medicine and Biology · doi:10.1016/0969-8051(96)00059-5 · Cited by 6 · see citing works
A non-parametric method for the analysis of experimental tumour growth data
Chignola, R., Liberati, D., Chiesa, E., Anselmi, C., Foroni, R. I., Sartoris, S., Brendolan, A., Tridente, G., & Andrighetto, G. (1999) · Medical & Biological Engineering & Computing · doi:10.1007/bf02513343 · Cited by 5 · see citing works
Heiss, P., Bermatz, S., Wehnes, H., Heinzmann, U., & Senekowitsch–Schmidtke, R. (1997) · PubMed · Cited by 5 · see citing works
Dazord, L., Cavallier, A., Thomas, D., Guiraud, J.-M., Lannic, J. L., Robin, V., Collet, B., Desrues, B., Ramée, M. P., & Toujas, L. (1993) · PubMed · Cited by 4 · see citing works
Imbert‐Marcille, B., Berreur, M., Thédrez, P., Riet, A. V., Devys, A., Chatal, J., & Pradal, G. (1995) · PubMed · Cited by 4 · see citing works
Effects of epidermal growth factor receptor blocking in cultured glioma spheroids.
Capala, J., Acker, H., Lindström, A., & Carlsson, J. (1994) · PubMed · Cited by 2 · see citing works
Flagged first, then by citations
10 of the 149 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Kelm, J. M., Timmins, N. E., Brown, C. J., Fussenegger, M., & Nielsen, L. K. (2003) · Biotechnology and Bioengineering · doi:10.1002/bit.10655 · Cited by 934 · see citing works
The use of 3-d cultures for high-throughput screening: the multicellular spheroid model.
Kunz-Schughart, L. A., Freyer, J. P., Hofstaedter, F., & Ebner, R. (2004) · SLAS DISCOVERY · doi:10.1177/1087057104265040 · Cited by 797 · see citing works
Three-dimensional in vitro tumor models for cancer research and drug evaluation
Xu, X., Farach‐Carson, M. C., & Jia, X. (2014) · Biotechnology Advances · doi:10.1016/j.biotechadv.2014.07.009 · Cited by 462 · see citing works
Superior Penetration and Retention Behavior of 50 nm Gold Nanoparticles in Tumors
Huo, S., Ma, H., Huang, K., Liu, J., Wei, T., Jin, S., Zhang, J., He, S., & Liang, X. (2012) · Cancer Research · doi:10.1158/0008-5472.can-12-2071 · Cited by 337 · see citing works
Molecular description of a 3D in vitro model for the study of epithelial ovarian cancer (EOC)
Zietarska, M., Maugard, C. M., Filali‐Mouhim, A., Alam‐Fahmy, M., Tonin, P. N., Provencher, D. M., & Mes‐Masson, A. (2007) · Molecular Carcinogenesis · doi:10.1002/mc.20315 · Cited by 209 · see citing works
Salmonella typhimurium specifically chemotax and proliferate in heterogeneous tumor tissue in vitro
Kasinskas, R. W., & Forbes, N. S. (2006) · Biotechnology and Bioengineering · doi:10.1002/bit.20883 · Cited by 210 · see citing works
Graff, C. P., & Wittrup, K. D. (2003) · PubMed · Cited by 207 · see citing works
Xiang, D., Zheng, C., Zhou, S., Qiao, S., Tran, P. H. L., Pu, C., Li, Y., Kong, L., Kouzani, A. Z., Lin, J., et al. (2015) · Theranostics · doi:10.7150/thno.11711 · Cited by 205 · see citing works
Stimulus-responsive macromolecules and nanoparticles for cancer drug delivery
MacEwan, S. R., Callahan, D. J., & Chilkoti, A. (2010) · Nanomedicine · doi:10.2217/nnm.10.50 · Cited by 205 · see citing works
Ho, W. Y., Yeap, S. K., Ho, C. L., Rahim, R. A., & Alitheen, N. B. (2012) · PLoS ONE · doi:10.1371/journal.pone.0044640 · Cited by 173 · see citing works
Ware, M. J., Colbert, K. L., Keshishian, V., Ho, J., Corr, S. J., Curley, S. A., & Godin, B. (2016) · Tissue Engineering Part C Methods · doi:10.1089/ten.tec.2015.0280 · Cited by 171 · see citing works
Kim, T.-H., Mount, C., Gombotz, W. R., & Pun, S. H. (2010) · Biomaterials · doi:10.1016/j.biomaterials.2010.06.004 · Cited by 165 · see citing works
Spatio‐temporal modeling of nanoparticle delivery to multicellular tumor spheroids
Goodman, T. T., Chen, J., Matveev, K. I., & Pun, S. H. (2008) · Biotechnology and Bioengineering · doi:10.1002/bit.21910 · Cited by 158 · see citing works
Waite, C. L., & Roth, C. M. (2012) · Critical Reviews in Biomedical Engineering · doi:10.1615/critrevbiomedeng.v40.i1.20 · Cited by 156 · see citing works
Barbone, D., Yang, T., Morgan, J. R., Gaudino, G., & Broaddus, V. C. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m709698200 · Cited by 148 · see citing works
Digesting a Path Forward: The Utility of Collagenase Tumor Treatment for Improved Drug Delivery
Dolor, A., & Szoka, F. C. (2018) · Molecular Pharmaceutics · doi:10.1021/acs.molpharmaceut.8b00319 · Cited by 141 · see citing works
Quader, S., Liu, X., Chen, Y., Mi, P., Chida, T., Ishii, T., Miura, Y., Nishiyama, N., Cabral, H., & Kataoka, K. (2017) · Journal of Controlled Release · doi:10.1016/j.jconrel.2017.04.033 · Cited by 137 · see citing works
Sanga, S., Frieboes, H. B., Zheng, X., Gatenby, R. A., Bearer, E. L., & Vittorio Cristini, C. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2007.05.043 · Cited by 130 · see citing works
Davies, C. D. L., Berk, D. A., Pluen, A., & Jain, R. K. (2002) · British Journal of Cancer · doi:10.1038/sj.bjc.6600270 · Cited by 121 · see citing works
Issues related to targeted delivery of proteins and peptides
Lu, Y. J., Yang, J. J. J., & Sega, E. I. (2006) · The AAPS Journal · doi:10.1208/aapsj080355 · Cited by 99 · see citing works
Anti‐tumor effects of toxins targeted to the prostate specific membrane antigen
Fracasso, G., Bellisola, G., Cingarlini, S., Castelletti, D., Prayer‐Galetti, T., Pagano, F. C., Tridente, G., & Colombatti, M. (2002) · The Prostate · doi:10.1002/pros.10117 · Cited by 92 · see citing works
Self-citationCarver, K. A., Ming, X., & Juliano, R. L. (2014) · Molecular Therapy — Nucleic Acids · doi:10.1038/mtna.2014.5 · Cited by 75 · see citing works
A Novel In Vitro Model of Human Mesothelioma for Studying Tumor Biology and Apoptotic Resistance
Kim, K., Wilson, S. M., Abayasiriwardana, K. S., Collins, R., Fjellbirkeland, L., Xu, Z., Jablons, D. M., Nishimura, S. L., & Broaddus, V. C. (2005) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2004-0355oc · Cited by 73 · see citing works
Pharmacokinetic strategies to improve drug penetration and entrapment within solid tumors
Al-Abd, A. M., Aljehani, Z. K., Gazzaz, R. W., Fakhri, S. H., Jabbad, A. H., Alahdal, A. M., & Torchilin, V. P. (2015) · Journal of Controlled Release · doi:10.1016/j.jconrel.2015.08.055 · Cited by 66 · see citing works
Cavo, M., Cave, D. D., D’Amone, E., Gigli, G., Lonardo, E., & del Mercato, L. L. (2020) · Scientific Reports · doi:10.1038/s41598-020-66908-8 · Cited by 58 · see citing works
When the Optimal Is Not the Best: Parameter Estimation in Complex Biological Models
Fernández Slezak, D., Suárez, C., Cecchi, G. A., Marshall, G., & Stolovitzky, G. (2010) · PLoS ONE · doi:10.1371/journal.pone.0013283 · Cited by 57 · see citing works
“The multicellular spheroid model [15] is at present considered an excellent in vitro model to study complex aspects of tumor physiology, especially those related to therapeutic strategies that cannot be adequately treated by other simpler models [16,17].”
BackgroundAbuqayyas, L., & Balthasar, J. P. (2012) · Journal of Pharmacokinetics and Pharmacodynamics · doi:10.1007/s10928-012-9279-8 · Cited by 51 · see citing works
Development of radiotracers for oncology – the interface with pharmacology
Sharma, R., & Aboagye, E. O. (2010) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2010.01160.x · Cited by 50 · see citing works
Al-Abd, A. M., Hyeon, L. S., Kim, S. H., Cha, J., Park, T. G., Lee, S. J., & Kuh, H. (2009) · Journal of Controlled Release · doi:10.1016/j.jconrel.2009.03.009 · Cited by 48 · see citing works
Turetta, M., Ben, F. D., Brisotto, G., Biscontin, E., Bulfoni, M., Cesselli, D., Colombatti, A., Scoles, G., Gigli, G., & del Mercato, L. L. (2018) · Current Medicinal Chemistry · doi:10.2174/0929867325666180605122633 · Cited by 45 · see citing works
Monazzam, A., Josephsson, R., BLOMQVIST, C. P., Carlsson, J., Långström, B., & Bergström, M. (2007) · Breast Cancer Research · doi:10.1186/bcr1747 · Cited by 33 · see citing works
γH2AX and cleaved PARP-1 as apoptotic markers in irradiated breast cancer BT474 cellular spheroids
Qvarnström (2009) · International Journal of Oncology · doi:10.3892/ijo_00000311 · Cited by 30 · see citing works
WANG, Q., Li, S., Xie, Y., Yu, W., Xiong, Y., MA, X., & YUAN, Q. (2006) · Hepatology Research · doi:10.1016/j.hepres.2006.03.003 · Cited by 27 · see citing works
Prasad, S., Chandra, A., Cavo, M., Parasido, E., Fricke, S., Lee, Y., D’Amone, E., Gigli, G., Albanese, C., Rodriguez, O., et al. (2020) · Nanotechnology · doi:10.1088/1361-6528/abc208 · Cited by 23 · see citing works
Lang, S., Picu, A., Hofmann, T., Andratschke, M., Mack, B., Moosmann, A., Gires, O., Tiwari, S., & Zeidler, R. (2006) · International Journal of Immunopathology and Pharmacology · doi:10.1177/039463200601900217 · Cited by 24 · see citing works
Fogar, P., Navaglia, F., Basso, D., Zambon, C., Moserle, L., Indraccolo, S., Stranges, A., Greco, E., Fadi, E., Padoan, A., et al. (2009) · Cancer Gene Therapy · doi:10.1038/cgt.2009.48 · Cited by 23 · see citing works
Ex vivo cancer chemoprevention research possibilities
Hudson, E. A., Fox, L. H., Luckett, J., & Manson, M. M. (2005) · Environmental Toxicology and Pharmacology · doi:10.1016/j.etap.2005.07.011 · Cited by 22 · see citing works
Monazzam, A., Razifar, P., Ide, S. E., Jensen, M. R., Josephsson, R., BLOMQVIST, C. P., Långström, B., & Bergström, M. (2009) · Nuclear Medicine and Biology · doi:10.1016/j.nucmedbio.2008.12.009 · Cited by 22 · see citing works
What Do, Can and Should We Learn From Models To Evaluate Potential Anticancer Agents?
Burchill, S. A. (2006) · Future Oncology · doi:10.2217/14796694.2.2.201 · Cited by 20 · see citing works
Identification of three gene candidates for multicellular resistance in colon carcinoma
Timmins, N. E., Maguire, T. L., Grimmond, S. M., & Nielsen, L. K. (2004) · Cytotechnology · doi:10.1007/s10616-005-1476-5 · Cited by 18 · see citing works
Photochemically enhanced adenoviral transduction in a multicellular environment
Bonsted, A., Engesæter, B. Ø., Høgset, A., & Berg, K. (2006) · Photochemical & Photobiological Sciences · doi:10.1039/b515066c · Cited by 6 · see citing works
Tran, T. A. (2011) · International Journal of Oncology · doi:10.3892/ijo.2011.1045 · Cited by 5 · see citing works
Numerical simulation of avascular tumor growth
Slezak, D. F., Suárez, C. A., Soba, A., Risk, M. R., & Marshall, G. (2007) · Journal of Physics Conference Series · doi:10.1088/1742-6596/90/1/012049 · Cited by 5 · see citing works
Multicellular Tumour Spheroids in a Translational PET Imaging Strategy
Monazzam, A. (2007) · KTH Publication Database DiVA (KTH Royal Institute of Technology)
Photochemical delivery of bleomycin in malignant glioma cells
Blickenstaff, J. W. (2020) · Digital Scholarship - UNLV (University of Nevada Reno) · doi:10.34917/2508291
Waite, C. L. (2011) · Rutgers University Community Repository (Rutgers University) · doi:10.7282/t36m35xg
- Authors
- Fracasso, G.
- Affiliations
- University of Verona (IT)
- Corresponding author
- Fracasso, G
- ORCID
- Fracasso, G
- Venue
- Critical Reviews in Oncology/Hematology
- Publisher
- Elsevier BV
- Published
- 2000-11
- Volume
- 36
- Issue
- 2-3
- Pages
- 159-178
- ISSN
- 1040-8428 (ISSN-L)
- OpenAlex
- W2058131320
- Cited by
- 46
- References
- 149
- Citations by year
- 2020: 3 · 2018: 2 · 2017: 1 · 2016: 1 · 2015: 2 · 2014: 2 · 2012: 4
- FWCI
- 0.43
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Critical Reviews in Oncology/Hematology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Physical Sciences › Materials Science › Biomaterials › Nanoparticle-Based Drug Delivery
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Monoclonal and Polyclonal Antibodies Research
- Physical Sciences › Engineering › Biomedical Engineering › Ultrasound and Hyperthermia Applications
- Keywords
- tumor spheroids, antibody delivery, immunotoxins, radiolabeled antibodies, cytokines, extracellular matrix proteins, cell-cell interactions, cell-matrix interactions, drug penetration, cancer therapy
- MeSH terms
- Antineoplastic Agents, Humans, Neoplasms, Drug Delivery Systems, Spheroids, Cellular
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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