The involvement of genes and proteins in apoptosis - Carcinogenesis regulation
DOI:
https://doi.org/10.32635/2176-9745.RBC.1997v43n3.2852Keywords:
Apoptosis, Oncogenes, Tumor Suppressor Genes, CarcinogenesisAbstract
Apoptosis is an importante feature in many normal biological process, such as embryogenesis, development of the immune system, cell maturation and differentiation. In occurrence of diseases, apoptosis seems to be involved in immunodeficiency, drug resistance and carcinogenesis. It is well known that carcinogenesis involves cumulative genetic alterations in oncogenes and tumor suppressor genes. Therefore the prognosis of each human tumor seems to be dependent on several genes, and it is foreseeable that a deeper knowledge on the co-operation and antagonism the these genes could provide, in the future, clinically relevant informations. We review some of the most recent developments concerning the genes involved in apoptosis and human cancers (p53, bcl-2, c-myc, fas-APO-l, mdr-l) and their clinical implications.
Downloads
References
Kerr, J.F.R.; Wyllie, A.H.; Currie, A.R. - Apoptosis: a basic biological phenomenon with wide ranging implications in tissue kinetics. Br J Cancer, 26: 239-257, 1972. DOI: https://doi.org/10.1038/bjc.1972.33
Schultze-Osthoff, K.; Walczak, H.; Droge, W.; Krammer, P.H. - Cell nucleus and DNA fragmentation are not required for apoptosis. J Cell Biol, 127: 15-19, 1994. DOI: https://doi.org/10.1083/jcb.127.1.15
Chandler, D.; El-Naggar, A.K.; Brisbay, S.; Redline, R. W.; Mc Donnel, T.J. – Apoptosis and expression of the bcl-2 proto-oncogene in the fetal and adult human kidney: evidence for the contribution of bcl-2 expression to renal carcinogenesis. Hum Pathol, 25(8): 789-796, 1994. DOI: https://doi.org/10.1016/0046-8177(94)90248-8
Robbins, et al. - Pathologic basis of disease. Quinta edição: 17-21, 1994.
Robertson, L.E.; Huang, P.; Keating, M.J.; Plunkett, W. - Apoptosis in chronic lymphocytic leukemia. Cancer Bull, 46(2): 130-134, 1994.
Pantaleo, G.; Graziosi, C.; Fauci, A.S. – The immunopathogenesis of human immunodeficiency virus infection. N Engl J Med, 328(5): 327-334, 1993. DOI: https://doi.org/10.1056/NEJM199302043280508
Meyn, R.W.; Milas, L.; Stephens, C. - Programmed cell death in normal development and disease. Cancer Bull, 46; 120-124,1994.
Saclarides, T.J.;Jakate, S.M.;Coon,J.S. et al. - Variable expression of P-glycoprotein in normal, inflamed, and dysplastic areas in ulcerative colitis. Dis Colon Rectum, 35(8); 747-751, 1992. DOI: https://doi.org/10.1007/BF02050323
Su, I-J.; Cheng, A-L; Tsai, T-F; Lay, J-D - Retinoic acid-induced apoptosis and regression of a refractory Epstein-Barr-virus-containing T cell lymphoma expressing multidrug-resistance phenotypes. Br J Haemat, 85; 826-828, 1993. DOI: https://doi.org/10.1111/j.1365-2141.1993.tb03235.x
lO.Green, D.R.; Martin, S.J. - The killer and the executioner; how apoptosis Controls malignancy. Curr Opin Immunol, 7; 694-703, 1995. DOI: https://doi.org/10.1016/0952-7915(95)80079-4
De Vinci, A.; Geido, E.; Infusini, E.; Giaretti, W. - Neuroblastoma cell apoptosis induced by the synthetic retinoid n-(4-hydroxyphenyl) retinamide. Int J Cancer, 59: 474-476, 1994. DOI: https://doi.org/10.1002/ijc.2910590322
Schulte-Hermann, R.; Burseh, W.; Grasl-Kraupp, B.; Tõrõk, L.; Ellinger, A.; Müllauer, L. - Role of active cell death (apoptosis) in multi-stage carcinogenesis. Toxicol Lett, 82/83; 143-148, 1995. DOI: https://doi.org/10.1016/0378-4274(95)03550-8
Donehower, L.A. - Tumor suppressor gene p53 and apoptosis. Câncer Bull,46; 161-166, 1994.
H.Macleod, K.F,; Sherry, N.; Hennen, G. et al. - p53-dependent and independent expression of p21 during cell growth, differentiation, and DNA damage. Gen Dev, 9; 935-944, 1995. DOI: https://doi.org/10.1101/gad.9.8.935
Lowe, S. W. - Câncer therapy and p53. Curr Opin Oncol, 7; 547-553, 1995. DOI: https://doi.org/10.1097/00001622-199511000-00013
Jonathan, D. Oliner - The role of p53 in cancer development. Scientific Am Science & Med. Sept-Oct; 16-25, 1994.
Symonds, H.; Krau, L.; Remington, L. et al. - p53-dependent apoptosis suppresses tumor growth and progression in vivo. Cell, 78; 703-711, 1994. DOI: https://doi.org/10.1016/0092-8674(94)90534-7
Lowe, S.W.; Jacks, T.; Housman, D.E.; Ruley, H.E. - Abrogation of oncogene-associated apoptosis allows transformation of p53-deficient cells. Proc Natl Acad Sci USA, 91; 2069-2070, 1994. DOI: https://doi.org/10.1073/pnas.91.6.2026
Sidransky, D.; Hollstein, M. - Clinicai implications of the p53 gene. Annu Rev Med, 47; 285-301, 1996. DOI: https://doi.org/10.1146/annurev.med.47.1.285
Reeve, J.G.; Xiong, J.; Morgan, J.; Bleehen, N.M. - Expression of apoptosis-regulatory genes in lung tumour cell lines; relationship to p53 expression and relevance to acquired drug resistance. Br J Cancer, 73; 1193-1200, 1996. DOI: https://doi.org/10.1038/bjc.1996.230
Rasbridge, S.A.; Gillett, C.E.; Seymour, A.M. et al. - The effects of chemotherapy on morphology, cellular proliferation, apoptosis and oncoprotein expression in primary breast carcinoma. Br J Cancer, 70; 335-341, 1994. DOI: https://doi.org/10.1038/bjc.1994.303
Eyfjõrd, J.E.; Thorlacius, S.; Steinarsdottir, M.; Valgardsdottir, R.; Ôgmundsdottir, H.M.; Anamthawat-Jonsson, K. - p53 abnormalities and genomic instability in primary human breast carcinomas. Cancer Res, 55; 646-665, 1995. DOI: https://doi.org/10.3109/02841869509094045
Rubio, C.A.; Rodensjõ, M. - p53 overexpression in flat serrated adenomas and flat tubular adenomas of the colorectal mucosa. J Cancer Res Clin Oncol, 121; 571-576, 1995. DOI: https://doi.org/10.1007/BF01197772
Schlichtholz, B.; Tredaniel, J.; Lubin, R.; Zalchan, G.; Hirseh, A.; Soussi, T. - Analyses of p53 antibodies in sera of patients with lung carcinoma define immunodominant regions in the p53 protein. Br J Cancer, 69; 809-816, 1994. DOI: https://doi.org/10.1038/bjc.1994.159
Seshadri, R.; Leong, A.S.Y.; Mc Caul, K.; Firgaira, F.A.; Setlur, V.; Horsfall, D.J. - Relationship between p53 gene abnormalities and other tumor characteristies in breast cancer prognosis. Int J Cancer (Pred. Oncol.), 69; 135-141, 1996. DOI: https://doi.org/10.1002/(SICI)1097-0215(19960422)69:2<135::AID-IJC12>3.0.CO;2-8
Peyrat, J-P.; Bonneterre, J.; Lubin, R.; Vanlemmens, L.; Fournier, J. – Prognostic significance of circulating p53 antibodies in patients undergoing surgery for locore gional breast cancer. Lancet, 345; 621 -22, 1995. DOI: https://doi.org/10.1016/S0140-6736(95)90523-5
Ozbun, M.A., Butel, J.S. - Tumor suppressor p53 mutations and breast cancer: a critical analysis. Adv Cancer Res, 66: 71-141, 1995. DOI: https://doi.org/10.1016/S0065-230X(08)60252-3
Williams, N.S. - Colorectal cancer 1996; 2-7.
Houbiers, J.G.A.; Van-der Burg, S.H.; Van de Watering, L.M.G. et al. – Antibodies against p53 are associated with poor prognosis of colorectal cancer. Br J Câncer, 72: 637-641, 1995. DOI: https://doi.org/10.1038/bjc.1995.386
Uchino, S.; Tsuda, H.; Noguchi, M. et al - Frequent loss of heterozigosity at DCC locus in gastric cancers. Cancer Res, 52: 3099-3102, 1992.
Fujimoto, K.; Yamada, Y.; Okajima, E. et al. - Frequent association of p53 gene mutation in invasivebladder cancer. Cancer Res, 52: 1393-1398, 1992.
Glick, S.H.; Howell, L.P.; Deverewhite, R.W. - Relationship of p53 and bcl-2 to prognosis in muscle-invasive transitional cell carcinoma of the bladder. J Urol, 155: 1754-1757, 1996. DOI: https://doi.org/10.1016/S0022-5347(01)66192-5
Yoshimura, I.; Kudoh, J.; Saito, S.; Tazaki, H.; Shimizu, N. - p53 gene mutation in recurrent superficial bladder cancer. J Urol, 153: 1711-1715, 1995. DOI: https://doi.org/10.1016/S0022-5347(01)67510-4
Nakopoulou, L.; Constantinides, C.; Papandropoulos, J. et al. - Evaluation of overexpression of p53 tumor supressor protein in superficial and invasive transitional cell bladder cancer: comparison with DNA ploidy. Urology, 46(3): 334-40, 1995. DOI: https://doi.org/10.1016/S0090-4295(99)80216-7
Têtu, B.; Fradet, Y.; Allard, P.; Veilleux, C.; Roberge, N.; Bernard, P. – Prevalence and clinicail significance of Her-2/neu, p53 and Rb expression in primary superficial bladder cancer. J Urol, 155: 1784-1788, 1996. DOI: https://doi.org/10.1016/S0022-5347(01)66198-6
Kurvinen, K.; Syrjãnen, K.; Syrjânen, S. - p53 and bcl-2 proteins as prognostic mar kers in human papillomavirus -associated cervical lesions. J Clin Oncol, 14(7): 2120-2130. 1996. DOI: https://doi.org/10.1200/JCO.1996.14.7.2120
Pilotti, S.; D’amato, L.; Delia Torre, G. et al. - Papillomavirus, p53 alteration and primary carcinoma of the vulva. Diag Mol Pathol, 4(4): 239-248, 1995. DOI: https://doi.org/10.1097/00019606-199512000-00003
Rose, P.G. - Endometrial carcinoma. N Engl JMed, 335(9); 640-648, 1996. DOI: https://doi.org/10.1056/NEJM199608293350907
Neubauer, A.; Thiede, C.; Huhn, D.; Wittig, B. - p53 and induction of apoptosis as a target for anticancer therapy. Leukemia, 10(suppl. 3): S2-S4, 1996.
Shaw, P.; Bovey, R.; Tardy, S.; Sahli, R.; Sordat, B.; Costa, J. - Induction of apoptosis by wild-type p53 in a human colon tumor derived cell line. Proc Natl Acad Sci USA, 89: 4495-4499, 1992. DOI: https://doi.org/10.1073/pnas.89.10.4495
Siles, E.; Villalobos, M.; Valenzuela, M.T. et al. - Relationship between p53 status and radiosensitivity in human tumour cell lines. Br J Cancer, 73: 581-588, 1996. DOI: https://doi.org/10.1038/bjc.1996.101
Lu, Q-L; Abel, P.; Foster, C.S.; Lalani, E-N. - Bcl-2: Role in epithelial differentiation and oncogenesis. Hum Pathol, 27(2): 102-109, 1996. DOI: https://doi.org/10.1016/S0046-8177(96)90362-7
Hockenbery, D.; Nunez, G.; Milliman, C.; Schreiber, R.D., Korsmeyer, S.J. - Bcl-2 is an inner mitochondrial membrane protein that blocks programmed cell death. Nature, 348: 334-336, 1990. DOI: https://doi.org/10.1038/348334a0
Chen-Levy, Z.; Nourse, J.; Cleary, M.L. – The bcl-2 candidate proto-oncogene produet is a 24 kilodalton integral-membrane protein highly expressed in lymphoid cell lines and lymphomas carrying the t(14-18) translocation. Mol Cell Biol, 9; 701-710, 1989. DOI: https://doi.org/10.1128/mcb.9.2.701-710.1989
Alnemri, E.S.; Robertson, N.M., Fernandes, T.F.; Croce, C.M.; Litwack, G. - Overexpressed full-length human bcl-2 extends the survival of baculovirus-infected Sf9 insect cells. Proc Natl Acad Sei USA, 89: 7295-7299, 1992. DOI: https://doi.org/10.1073/pnas.89.16.7295
Chiarugi, V.; Ruggiero, M. - Role of three cancer “master genes” p53, bcl-2 and c-myc on the apoptotic process. Tumori, 82: 205-209, 1996.
Jacobson, M.D.; Burne, J.F.; King, M.P.; Miyashita, T.; Reed, J.C.; Raff, M.C. - Bcl-2 blocks apoptosis in cells lacking mitochondrial DNA. Nature, 361: 365-368, 1993. DOI: https://doi.org/10.1038/361365a0
Baffy, G.; Miyashita, T.; Williamson Jr.; Reed, J.C. - Apoptosis induced by with-drawal of interleukin-3(IL-3) from an IL-3 dependent hematopoietic cell line is associated with repartitioning of intracelular calcium and is blocked by enforced bcl-2 oncoprotein production. J Biol Chem, 268: 6511-6519, 1993. DOI: https://doi.org/10.1016/S0021-9258(18)53280-4
Hockenbery, D.M.; Oltvai, Z.N.; Yin X-M.; Milliman, C.L.; Korsmeyer, S.J. - Bcl-2 functions in an antioxidant pathway to prevent apoptosis. 5011,75:241-251,1993. DOI: https://doi.org/10.1016/0092-8674(93)80066-N
Jacobson, M.D.; Raff, M.C. – Programmed cell death and bcl-2 protection in very low oxygen. Nature, 374: 814-816, 1995. DOI: https://doi.org/10.1038/374814a0
Shimizu, S.; Eguchi, Y.; Kosaka, H.; Kamiike, W.; Matsuda, H.; Tsujimoto, Y. - Prevention of hypoxia-induced cell death by bcl-2 and bcl-xl. Nature, 374: 811-813, 1995. DOI: https://doi.org/10.1038/374811a0
Wachsman, J.T. - The beneficiai effects of dietary restriction: reduced oxidative damage and enhanced apoptosis. Mut Res, 350: 25-34, 1996. DOI: https://doi.org/10.1016/0027-5107(95)00087-9
Kernohan, N.M.; Cox, L.S. - Regulation of apoptosis by Bcl-2 and its related proteins: immunochemical challenges and therapeutic implications. J Pathol, 179: 1-3, 1996. DOI: https://doi.org/10.1002/(SICI)1096-9896(199605)179:1<1::AID-PATH509>3.0.CO;2-E
Boise, L.H.; González-Garcia, M.; Postema, C.E. et al. - Bcl-x, a bcl-2 -related gene that functions as a dominator regulator of apoptotic cell death. Cell, 74: 597-608, 1994. DOI: https://doi.org/10.1016/0092-8674(93)90508-N
Reed, J.C. - Regulation of apoptosis by bcl-2 family proteins and its role in cancer and chemoresistance. Curr Opin Oncol, 7:541-546, 1995. DOI: https://doi.org/10.1097/00001622-199511000-00012
Oitvai, Z.N.; Milliman, C.L.; Korsmeyer, S.J. - Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmedcell death. Cell, 74:609-619, 1993. DOI: https://doi.org/10.1016/0092-8674(93)90509-O
Furihata, M.; Sonobe, H.; Ohtsuki, Y. et al. - Detection of p53 and bcl-2 protein in carcinoma of the renal pélvis and ureter including dysplasia. J Pathol, 178: 133-139, 1996. DOI: https://doi.org/10.1002/(SICI)1096-9896(199602)178:2<133::AID-PATH455>3.0.CO;2-F
Tomita, Y.; Bilim, V.; Kawasaki, T. et al. - Frequent expression of bcl-2 in renal-cell carcinomas carrying wild-type p53. Int J Cancer, 66: 322-325, 1996. DOI: https://doi.org/10.1002/(SICI)1097-0215(19960503)66:3<322::AID-IJC9>3.0.CO;2-0
Saegusa, M.; Takano, Y.; Okayasu, I. - Bcl-2 expression and its association with cell kinetics in human gastric carcinomas and intestinal metaplasia. J Cancer Res Clin Oncol, 121:357-363, 1995. DOI: https://doi.org/10.1007/BF01225688
Saegusa, M.; Takano, Y.; Kamata, Y.; Okayasu, I. - Bcl-2 expression and allelic loss of the p53 gene in gastric carcinomas. J Cancer Res Clin Oncol, 122: 427-432, 1996. DOI: https://doi.org/10.1007/BF01212883
Nicolson, N.L.; Talpaz, M.; Nicolson, G.L. - Chromatin nucleoprotein complexes containing tightly bound c-abl, p53 and bcl-2-gene sequences: correlation with progression of chronic myelogenous leukemia. Gene, 169: 173-178, 1996. DOI: https://doi.org/10.1016/0378-1119(96)88650-1
Coustan-Smith, E.; Kitanaka, A.; Pui, C- H. et al. - Clinical relevance of bcl-2 overexpression in childhood acute lymphoblastic leukemia. Blood, 3(1): 1140-1146, 1996. DOI: https://doi.org/10.1182/blood.V87.3.1140.bloodjournal8731140
Aguilar-Santelises, M.; Rottenberg, M.E.; Lewin, N.; Mellstedt, H.; Jondal, M. - Bcl-2, Bax and p53 expression in B-CLL in relation to in vitro survival and clinical progression. Int J Cancer (Pred. Oncol.), 69: 114-119, 1996. DOI: https://doi.org/10.1002/(SICI)1097-0215(19960422)69:2<114::AID-IJC8>3.0.CO;2-3
Mainou-Fowler, T.; Craig, V.A.; Copplestone, J.A.; Hamon, M.D.; Prentice, A.G. - Interleukin-5 (IL-5) increases spontaneous apoptosis of B-cell chronic lymphocytic leukemia cells in vitro independently of bcl-2 expression, and is inhi bited by IL-4. Blood, 84(7); 2297-2304, 1994. DOI: https://doi.org/10.1182/blood.V84.7.2297.2297
Panayiotidis, P.; Ganeshaguru, K.; Jabbar, S.A.B.; Hoffbrand, A.V. - Interleukin-4 inhibits apoptotic cell death and loss of the bcl-2 protein in B-chronic lymphocytic leukaemia cells in vitro. Br J Haematol, 85: 439-445, 1993. DOI: https://doi.org/10.1111/j.1365-2141.1993.tb03330.x
Selvakumaran, M.; Lin, H-K; Sjin, R.T.T.; Reed, J.C.; Liebermann, D.A.; Hoffman, B. - The novel primary response gene MyD118 and the proto-oncogenes myb, myc, and bcl-2 modulate transforming growth factor 61 -induced apoptosis of myeloid leucemia cells. Mol Cell Biol, 14(4); 2352-2360, 1994. DOI: https://doi.org/10.1128/MCB.14.4.2352
Chaouchi, N.; Wallon, C.; Taieb, J. et al. - Interferon-a-mediated prevention of in vitro apoptosis of chronic lymphocytic leukemia B cells; Role of bcl-2 and c-myc. Clin Immunol Immunopathol, 73(2): 197-204, 1994. DOI: https://doi.org/10.1006/clin.1994.1188
Fernandez, A.; Honnavara, N.; Ananthaswamy, N. - Molecular basis for tumor necrosis factor-induced apoptosis. Cancer Bull, 46(5); 153-160, 1994.
Fisher, T.C.; Milner, A.E.; Gregory, C.D. et al. - Bcl-2 modulation of apoptosis induced by anticancer drugs; resistance to thymidylate stress is independent of classical resistance pathways. Cancer Res, 53: 3321-3326, 1993.
Reed, J.C. - Bcl-2 family proteins: regulators of chemoresistance in cancer: Toxicol Lett, 82/83: 155-158, 1995. DOI: https://doi.org/10.1016/0378-4274(95)03551-6
Chiou, S-K; Rao, L.; White, E. - Bcl-2 blocks p53-dependent apoptosis. Mol Cell Biol, 14(4): 2556-2563, 1994. DOI: https://doi.org/10.1128/MCB.14.4.2556
Kondo,S.; Yin,D.;Takeuchi, J.;Morimura, T.; Oda, Y.; Kikuchi, H. - Bcl-2 gene enables rescue from in vitro myelosuppression (bone narrow cell death) induced by chemotherapy. Br J Cancer, 70: 421-426, 1994. DOI: https://doi.org/10.1038/bjc.1994.321
Cleveland, J.L.; Askew, D.S.; Packham, G. - Myc-mediated apoptosis in myeloid pro genitor cells. Cancer Bull, 46(2): 167-172, 1994.
Blackwood, E.M.; Eisenman, R.N. - Max; a helix-loop-helix zipper protein that forms a sequence-specific DNA-binding complex withmyc. Science, 251: 1211-1217,1991. DOI: https://doi.org/10.1126/science.2006410
Jansen-Dürr, P.; Meichle, A.; Steiner, P. et al. - Differential modulation of cyclin gene expression by myc. Proc Natl Acad Sci USA, 90: 3685-3689, 1993. DOI: https://doi.org/10.1073/pnas.90.8.3685
Shirodkar, S.; Ewen, M.; Decaprio, J.A.; Morgan, J.; Livingston, D.M. - The transcription factor E2F interacts with the retinoblastoma produet and a pl07-cyclin A complex in a cell cycle-regulated manner. Cell, 68; 157-166, 1992. DOI: https://doi.org/10.1016/0092-8674(92)90214-W
Kretzner, L.; Blackwood, E.M.; Eisenman, R.N. - Myc and Max proteins possess distinct transcriptional activities. Nature, 359: 426-428, 1992. DOI: https://doi.org/10.1038/359426a0
Packham, G.; Cleveland, J.L. – Ornitbine Decarboxylase is a mediator of c-myc-induced apoptosis. Mol Cell Biol, 14(9): 5741-5747, 1994. DOI: https://doi.org/10.1128/MCB.14.9.5741
Bissonnette, R.P.; Echeverri, F.; Mahboubi, A.; Green, D.R. - Apoptotic cell death induced by c-myc is inhibited by bcl-2. Nature, 359: 552-554, 1992. DOI: https://doi.org/10.1038/359552a0
Janicke, R.U.; Lee, F.H.H.; Porter, A.G. - Nuclear c-myc plays an important role in the cytotoxicity of tumor necrosis fator alphain tumor cells. Mol Cell Biol, 14(9): 5661-5670, 1994. DOI: https://doi.org/10.1128/MCB.14.9.5661
Shrivastava, A.; Saleque, S.; Kalpara, G.V.; Artandi, S.; Goff, S.P.; Calame, K. - Inhibition of transcriptional regulator Yin-Yang-1 by association with c-myc. Science, 262; 1889-1892, 1993. DOI: https://doi.org/10.1126/science.8266081
Shi, Y.; Glynn, J.M.; Guilbert, L.J.; Cotter, T.G.; Bissonnette, R.P.; Green, D.R. – Role for c-myc in activation-induced apoptotic cell death in T cell hybridomas. Science, 257; 212-214, 1992. DOI: https://doi.org/10.1126/science.1378649
Philipp, A.; Schneider, A.; Vâsrik, I. et al. - Repression of cyclin Dl: a novel function of Myc. Mol Cell Biol, 16(6): 4032-4043, 1994. DOI: https://doi.org/10.1128/MCB.14.6.4032
Askew, D.S.; Ihle, J.N.; Cleveland, J.L. - Activation of apoptosis associated with enforced Myc expression in myeloid pro-genitor cells is dominant to tbe suppression of apoptosis by interleukin-3 or erythropoetin. Blood, 82(7): 2079-2087, 1993. DOI: https://doi.org/10.1182/blood.V82.7.2079.2079
Fanidi, A.; Harrington, E.A.; Evan, G.I. - Cooperative interaction between c-myc and bcl-2 proto-oncogenes. Nature, 359: 554- 556, 1992. DOI: https://doi.org/10.1038/359554a0
Ryan, J.J.; Danish, R.; Gottliebel, C.A.; Clarke, M.F. - p53 induces apoptosis in G1 in hematopoietic cells. Mol Cell Biol, 13: 711-719, 1993. DOI: https://doi.org/10.1128/MCB.13.1.711
Lõnn, U.; Lõnn, S.; Stenkvist, B. - Prognostic value of erb-B2 and myc amplification in breast câncer imprints. Cancer, 75(11): 2681-2687, 1995. DOI: https://doi.org/10.1002/1097-0142(19950601)75:11<2681::AID-CNCR2820751107>3.0.CO;2-R
Ito, I.; Yoshimoto, M.; Iwase, T. et al. - Association of genetic alterations on chromosome 17 and loss of hormone receptors in breast cancer. Br J Cancer, 71:438-441, 1995. DOI: https://doi.org/10.1038/bjc.1995.89
Kubota, Y.; Miyamoto, H.; Noguchi, S. et al. - Tbe loss of retinoblastoma gene in association with c-myc and transforming growth factor-B 1 gene expression in human bladder câncer. JUrol, 154: 371-374, 1995. DOI: https://doi.org/10.1016/S0022-5347(01)67050-2
Trauth, B.C.; Klas, C.; Peters, A.M.J.et al. - Monoclonal antibody-mediated tumor regression by induction of apoptosis. Science, 245: 301-304, 1989. DOI: https://doi.org/10.1126/science.2787530
Owen-Schaub, L. - Fas/APO-1: A cell sur-face protein mediating apoptosis. Cancer Bull, 46(2): 141-145, 1994.
Weller, M.; Frei, K.; Groscurth, P.; Krammer, P.H.; Yonekawa, Y.; Fontana, A. - Anti-Fas antibody-mediated apoptosis of cultured human glioma cell. J Clin Invest, 94: 954-964, 1994. DOI: https://doi.org/10.1172/JCI117462
HSU, B.; Marin, M.C.; Brisbay, S.; Mc Connell, K.; Mc Donnell, T.J. – Expression of bcl-2 gene confers multidrug resistance to chemotherapy-induced cell death. Cancer Bull, 46(2): 125-129, 1994.
