Correspondence
Tumor Content of the Antiapoptosis Molecule Survivin and Recurrence of Bladder Cancer
N Engl J Med 1999; 341:452-453August 5, 1999
- Article
To the Editor:
Transitional-cell carcinoma of the bladder is the fourth most common cancer among American men, with approximately 50,000 new cases and 10,500 deaths from the disease every year. Fifty to 80 percent of affected patients have local recurrence of tumor, an event that frequently heralds muscle invasion and metastatic disease. Despite the search for markers that can be used to predict disease progression, no single molecule studied to date has been shown to identify patients at high risk for recurrences.1 Recently, a newly identified inhibitor of apoptosis,2 survivin, was found to be expressed in many cancers but not in normal tissues in adults,3 and its presence was correlated with more aggressive forms of neuroblastoma and poor survival among patients with colorectal cancer.4
We used immunohistochemical methods to study the expression of survivin, bcl-2, and p53 in the primary tumors of 36 patients with localized bladder cancer (25 men and 11 women; average age, 66 years; range, 51 to 78). Primary tumors were graded according to the classification system of the American Joint Committee on Cancer. Survivin was detected in 28 of the 36 tumors (78 percent). It was more common in higher-grade tumors (9 of 10 grade II tumors [90 percent] and 6 of 6 grade III tumors [100 percent]) than in lower-grade tumors (13 of 20 grade I tumors [65 percent]) and was absent in normal bladder epithelium (Figure 1Figure 1
Immunostaining for Survivin in Grade I Bladder-Cancer Specimens (×400).). No staining of normal or tumor tissue was seen with the use of nonimmune serum. The mean (±SD) time to first recurrence among patients with survivin-negative grade I tumors was 36±16 months, as compared with 12±6 months among the patients with survivin-positive grade I tumors (P<0.001). Immunostaining for antiapoptotic bcl-2 or p53 was not correlated with disease recurrence. All the tumors had a low apoptotic index (0.8 to 1 percent) on the basis of an assessment of internucleosomal DNA fragmentation.We propose that the presence of survivin in tumor tissue could be used to identify patients at high risk for recurrence of bladder cancer. When this test is integrated with tests for other molecular markers of disease progression, including alterations in p53 and retinoblastoma protein,5 it may help determine whether more stringent follow-up or aggressive treatments are needed.
5 ReferencesHubert S. Swana, M.D.
Douglas Grossman, M.D., Ph.D.
Julian N. Anthony, M.D.
Robert M. Weiss, M.D.
Dario C. Altieri, M.D.
Yale University School of Medicine, New Haven, CT 065361
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- Citing Articles (104)
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Christian Weiss, Felix von Römer, Gianni Capalbo, Oliver J. Ott, Michael Wittlinger, Steffen F. Krause, Rolf Sauer, Claus Rödel, Franz Rödel. (2009) Survivin Expression as a Predictive Marker for Local Control in Patients With High-Risk T1 Bladder Cancer Treated With Transurethral Resection and Radiochemotherapy. International Journal of Radiation Oncology*Biology*Physics 74:5, 1455-1460
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Jared M. Whitson, Emily J. Noonan, Deepa Pookot, Robert F. Place, Rajvir Dahiya. (2009) Double stranded-RNA-mediated activation of P21 gene induced apoptosis and cell cycle arrest in renal cell carcinoma. International Journal of Cancer 125:2, 446-452
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Uta B. Hofmann, Heike Voigt, Mads H. Andersen, Per thor Straten, Jürgen C. Becker, Andreas O. Eggert. (2009) Identification and characterization of survivin-derived H-2Kb-restricted CTL epitopes. European Journal of Immunology 39:5, 1419-1424
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In Gab Jeong, Sung Han Kim, Hwang Gyun Jeon, Baek Hee Kim, Kyung Chul Moon, Sang Eun Lee, Eunsik Lee. (2009) Prognostic value of apoptosis-related markers in urothelial cancer of the upper urinary tract. Human Pathology 40:5, 668-677
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Dong-Guk Park. (2009) The Changes of Expression of Survivin by Butyrate in HCT116 Colon Cancer Cells. Journal of the Korean Surgical Society 77:5, 297
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Wan-Sik Lee, Sung-Bum Cho, Jong-Sun Rew, Jae-Hyuk Lee, Chang-Soo Park, Young-Eun Joo. (2009) Expression of Survivin in Gastric Carcinoma and its Relation to Tumor Cell Proliferation and Apoptosis. The Korean Journal of Pathology 43:4, 329
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Dong Yun Kwak, Ji Yong Ha, Hyuk Soo Chang, Mi Sun Choi, Choal Hee Park, Chun Il Kim. (2009) Clinical Implications of the Expression of Survivin and p53 in Superficial Transitional Cell Carcinoma of the Bladder. Korean Journal of Urology 50:1, 12
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Tae Jung Jang, Kyung Seob Lee. (2009) The Expression of Cyclooxygenase-2 and Survivin in Urinary Bladder Transitional Cell Carcinoma. The Korean Journal of Pathology 43:3, 206
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C. Maxia, M. T. Perra, P. Demurtas, L. Minerba, D. Murtas, F. Piras, A. Corbu, D. C. Gotuzzo, R. G. Cabrera, D. Ribatti, P. Sirigu. (2008) Expression of survivin protein in pterygium and relationship with oxidative DNA damage. Journal of Cellular and Molecular Medicine 12:6a, 2372-2380
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W. Velando Rankin, C. J. Henry, S. E. Turnquist, J. R. Turk, M. E. Beissenherz, J. W. Tyler, E. B. Rucker, D. W. Knapp, C. O. Rodriguez, J. A. Green. (2008) Identification of survivin, an inhibitor of apoptosis, in canine urinary bladder transitional cell carcinoma*. Veterinary and Comparative Oncology 6:3, 141-150
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Wendi Velando Rankin, Carolyn J. Henry, Susan E. Turnquist, James R. Turk, Marilyn E. Beissenherz, Jeffrey W. Tyler, Jonathan A. Green. (2008) Comparison of distributions of survivin among tissues from urinary bladders of dogs with cystitis, transitional cell carcinoma, or histologically normal urinary bladders. American Journal of Veterinary Research 69:8, 1073-1078
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Xiao-Yong Pu, Zhi-Ping Wang, Yi-Rong Chen, Xing-Huan Wang, Yi-Long Wu, Huai-Peng Wang. (2008) The value of combined use of survivin, cytokeratin 20 and mucin 7 mRNA for bladder cancer detection in voided urine. Journal of Cancer Research and Clinical Oncology 134:6, 659-665
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Jinah Kim, Jennifer M McNiff. (2008) Nuclear expression of survivin portends a poor prognosis in Merkel cell carcinoma. Modern Pathology 21:6, 764-769
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Andrea Kiessling, Susanne Füssel, Rebekka Wehner, Michael Bachmann, Manfred P. Wirth, E. Peter Rieber, Marc Schmitz. (2008) Advances in Specific Immunotherapy for Prostate Cancer. European Urology 53:4, 694-708
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L. Pina-Cabral, L. Santos, B. Mesquita, T. Amaro, S. Magalhães, B. Criado. (2007) Detection of survivin mRNA in urine of patients with superficial urothelial cell carcinomas. Clinical and Translational Oncology 9:11, 731-736
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Jose A. Karam, Yair Lotan, Raheela Ashfaq, Arthur I. Sagalowsky, Shahrokh F. Shariat. (2007) Survivin Expression in Patients with Non-Muscle-Invasive Urothelial Cell Carcinoma of the Bladder. Urology 70:3, 482-486
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G-Y Chau, A F-Y Lee, S-H Tsay, Y-R Ke, H-L Kao, F-H Wong, A-P Tsou, Y-P Chau. (2007) Clinicopathological significance of survivin expression in patients with hepatocellular carcinoma. Histopathology 51:2, 204-218
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Achim Temme, Jose A. Rodriguez, Sandy Hendruschk, Serap Günes, Bernd Weigle, Knut Schäkel, Marc Schmitz, Michael Bachmann, Gabriele Schackert, E. Peter Rieber. (2007) Nuclear localization of Survivin renders HeLa tumor cells more sensitive to apoptosis by induction of p53 and Bax. Cancer Letters 250:2, 177-193
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F Piras, D Murtas, L Minerba, J Ugalde, C Floris, C Maxia, R Colombari, M T Perra, P Sirigu. (2007) Nuclear survivin is associated with disease recurrence and poor survival in patients with cutaneous malignant melanoma. Histopathology 50:7, 835-842
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Sergio Piña-Oviedo, Katarzyna Urbanska, Sujatha Radhakrishnan, Thersa Sweet, Krzysztof Reiss, Kamel Khalili, Luis Del Valle. (2007) Effects of JC Virus Infection on Anti-Apoptotic Protein Survivin in Progressive Multifocal Leukoencephalopathy. The American Journal of Pathology 170:4, 1291-1304
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Shahrokh F. Shariat, Raheela Ashfaq, Pierre I. Karakiewicz, Osamah Saeedi, Arthur I. Sagalowsky, Yair Lotan. (2007) Survivin expression is associated with bladder cancer presence, stage, progression, and mortality. Cancer 109:6, 1106-1113
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Vahid Haghpanah, Peiman Shooshtarizadeh, Ramin Heshmat, Bagher Larijani, Seyed Mohamad Tavangar. (2006) Immunohistochemical Analysis of Survivin Expression in Thyroid Follicular Adenoma and Carcinoma. Applied Immunohistochemistry & Molecular Morphology 14:4, 422-425
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Chatchai Tayapiwatana, Roongsiri Chotpadiwetkul, Watchara Kasinrerk. (2006) A novel approach using streptavidin magnetic bead-sorted in vivo biotinylated survivin for monoclonal antibody production. Journal of Immunological Methods 317:1-2, 1-11
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Mandy Wagner, Karin Schmelz, Christian Wuchter, Wolf-Dieter Ludwig, Bernd Dörken, Ingo Tamm. (2006) In vivo expression of survivin and its splice variant survivin-2B: Impact on clinical outcome in acute myeloid leukemia. International Journal of Cancer 119:6, 1291-1297
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K. Karabatsou, P. Pal, S. Dodd, B. Haylock, M. Aguirreburualde, N. Moxam, W. Pinson-Ellis, J. Broome, N.G. Rainov. (2006) Expression of survivin, platelet-derived growth factor A (PDGF-A) and PDGF receptor α in primary central nervous system lymphoma. Journal of Neuro-Oncology 79:2, 171-179
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Hao Deng, Renliang Wu, Ying Chen, Lijiang Liu. (2006) STAT1 and survivin expression in full lymph node examined gastric cancer by using tissue microarray technique. The Chinese-German Journal of Clinical Oncology 5:4, 249-252
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Wenji Wang, Huiying Luo, Aiqin Wang. (2006) Expression of survivin and correlation with PCNA in osteosarcoma. Journal of Surgical Oncology 93:7, 578-584
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William K. Decker, Jianxia Qiu, Farhang Farhangfar, Jenny H. Hester, Dario C. Altieri, Augustine Y. Lin. (2006) A retrogen plasmid-based vaccine generates high titer antibody responses against the autologous cancer antigen survivin and demonstrates anti-tumor efficacy. Cancer Letters 237:1, 45-55
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Iman J. Schultz, J. Alfred Witjes, Dorine W. Swinkels, Jacques B. de Kok. (2006) Bladder cancer diagnosis and recurrence prognosis: Comparison of markers with emphasis on survivin. Clinica Chimica Acta 368:1-2, 20-32
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Omar Moussa, Hassan Abol-Enein, Nabil K. Bissada, Thomas Keane, Mohamed A. Ghoneim, Dennis K. Watson. (2006) Evaluation of Survivin Reverse Transcriptase-Polymerase Chain Reaction for Noninvasive Detection of Bladder Cancer. The Journal of Urology 175:6, 2312-2316
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Mohammed Akhtar, Lisa Gallagher, Stephen Rohan. (2006) Survivin: Role in Diagnosis, Prognosis, and Treatment of Bladder Cancer. Advances in Anatomic Pathology 13:3, 122-126
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Hiroshi Kitamura, Toshihiko Torigoe, Ichiya Honma, Hiroko Asanuma, Emiri Nakazawa, Kumiko Shimozawa, Yoshihiko Hirohashi, Eiji Sato, Noriyuki Sato, Taiji Tsukamoto. (2006) Expression and antigenicity of survivin, an inhibitor of apoptosis family member, in bladder cancer: Implications for specific immunotherapy. Urology 67:5, 955-959
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Alvaro Lladser, Mario Párraga, Licarallén Quevedo, Maria Carmen Molina, Soledad Silva, Arturo Ferreira, Rosario Billetta, Andrew F. G. Quest. (2006) Naked DNA immunization as an approach to target the generic tumor antigen survivin induces humoral and cellular immune responses in mice. Immunobiology 211:1-2, 11-27
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Susanne Fuessel, Jana Herrmann, Shuangli Ning, Matthias Kotzsch, Kai Kraemer, Uta Schmidt, Oliver W. Hakenberg, Manfred P. Wirth, Axel Meye. (2006) Chemosensitization of bladder cancer cells by survivin-directed antisense oligodeoxynucleotides and siRNA. Cancer Letters 232:2, 243-254
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Linetta B. Koppert, Bas P.L. Wijnhoven, Herman van Dekken, Hugo W. Tilanus, Winand N.M. Dinjens. (2005) The molecular biology of esophageal adenocarcinoma. Journal of Surgical Oncology 92:3, 169-190
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Steffen Weikert, Frank Christoph, Mark Schrader, Hans Krause, Kurt Miller, Markus Müller. (2005) Quantitative analysis of survivin mRNA expression in urine and tumor tissue of bladder cancer patients and its potential relevance for disease detection and prognosis. International Journal of Cancer 116:1, 100-104
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Min Zhang, Neelanjan Mukherjee, R. Scott Bermudez, Douglas E. Latham, Meaghan A. Delaney, Anthony L. Zietman, William U. Shipley, Arnab Chakravarti. (2005) Adenovirus-mediated inhibition of survivin expression sensitizes human prostate cancer cells to paclitaxel in vitro and in vivo. The Prostate 64:3, 293-302
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Claudia S. Vetter, Katrin Müller-Blech, David Schrama, Eva-B. Bröcker, Jürgen C. Becker. (2005) Cytoplasmic and nuclear expression of survivin in melanocytic skin lesions. Archives of Dermatological Research 297:1, 26-30
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Enrico Conte, Fabio Stagno, Patrizia Guglielmo, Anna Scuto, Carla Consoli, Angelo Messina. (2005) Survivin expression in chronic myeloid leukemia. Cancer Letters 225:1, 105-110
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Lorenzo Lo Muzio, Antonio Farina, Corrado Rubini, Furio Pezzetti, Giordano Stabellini, Gregorio Laino, Andrea Santarelli, Giuseppe Pannone, Pantaleo Bufo, Alfredo de Lillo, Francesco Carinci. (2005) Survivin as prognostic factor in squamous cell carcinoma of the oral cavity. Cancer Letters 225:1, 27-33
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G Tonini, B Vincenzi, D Santini, S Scarpa, T Vasaturo, C Malacrino, R Coppola, P Magistrelli, D Borzomati, A Baldi, A Antinori, M Caricato, G Nuzzo, A Picciocchi. (2005) Nuclear and cytoplasmic expression of survivin in 67 surgically resected pancreatic cancer patients. British Journal of Cancer 92:12, 2225-2232
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Myung-Jin Kim, Koo-Young Lim, Jong-Won Kim, Il-Woo Nam, Jong-Ho Lee, Hoon Myoung. (2005) Stage and mRNA expression of survivin in lymph node as prognostic indicators in patients with oral squamous cell carcinoma. Cancer Letters 224:2, 253-261
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Mohammad H. Soltani, Rita Pichardo, Ziqui Song, Namrata Sangha, Fabian Camacho, Kapaettu Satyamoorthy, Omar P. Sangueza, Vijayasaradhi Setaluri. (2005) Microtubule-Associated Protein 2, a Marker of Neuronal Differentiation, Induces Mitotic Defects, Inhibits Growth of Melanoma Cells, and Predicts Metastatic Potential of Cutaneous Melanoma. The American Journal of Pathology 166:6, 1841-1850
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Shui Ping Tu, Jian Tao Cui, Peter Liston, Xiao Hua Jiang, Ruian Xu, Marie C.M. Lin, Yan Bo Zhu, Bing Zou, Samuel S.M. Ng, Shi Hu Jiang, Harry H.X. Xia, Wai Man Wong, Annie O.O. Chan, Man Fung Yuen, Shiu Kum Lam, Hsiang Fu Kung, Benjamin C.Y. Wong. (2005) Gene therapy for colon cancer by adeno-associated viral vector-mediated transfer of survivin Cys84Ala mutant. Gastroenterology 128:2, 361-375
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SHAHROKH F. SHARIAT, ROBERTO CASELLA, SEYED M. KHODDAMI, GINA HERNANDEZ, TULLIO SULSER, THOMAS C. GASSER, SETH P. LERNER. (2004) Urine Detection of Survivin is a Sensitive Marker for the Noninvasive Diagnosis of Bladder Cancer. The Journal of Urology 171:2, 626-630
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Moammir Hasan Aziz, Amaninderapal S. Ghotra, Yogeshwer Shukla, Nihal Ahmad. (2004) Ultraviolet-B Radiation Causes an Upregulation of Survivin in Human Keratinocytes and Mouse Skin¶. Photochemistry and Photobiology 80:3, 602
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Anil K Tyagi, Chapla Agarwal, Rana P Singh, Kenneth R Shroyer, L.Michael Glode, Rajesh Agarwal. (2003) Silibinin down-regulates survivin protein and mRNA expression and causes caspases activation and apoptosis in human bladder transitional-cell papilloma RT4 cells. Biochemical and Biophysical Research Communications 312:4, 1178-1184
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Kuniaki Nakanishi, Toshiaki Kawai, Fumiyuki Kumaki, Sadayuki Hiroi, Makio Mukai, Eiji Ikeda. (2003) Survivin Expression in Atypical Adenomatous Hyperplasia of the Lung. American Journal of Clinical Pathology 120:5, 712-719
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Monica Falleni, Caterina Pellegrini, Antonio Marchetti, Barbara Oprandi, Fiamma Buttitta, Fabio Barassi, Luigi Santambrogio, Guido Coggi, Silvano Bosari. (2003) Survivin gene expression in early-stage non-small cell lung cancer. The Journal of Pathology 200:5, 620-626
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Michael A. Simon, Vinata B. Lokeshwar, Mark S. Soloway. (2003) Current bladder cancer tests: unnecessary or beneficial?. Critical Reviews in Oncology/Hematology 47:2, 91-107
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Wen-zhe Song, yan Song, Jian-qiao Ye, Dong-tao Qiu. (2003) Survivin and tumor. Chinese Journal of Cancer Research 15:2, 152-156
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Yoshinori Kajiwara, Fumiyuki Yamasaki, Seiji Hama, Kaita Yahara, Hiroyuki Yoshioka, Kazuhiko Sugiyama, Kazunori Arita, Kaoru Kurisu. (2003) Expression of survivin in astrocytic tumors. Cancer 97:4, 1077-1083
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Noriyuki Takai, Tami Miyazaki, Masakazu Nishida, Kaei Nasu, Isao Miyakawa. (2002) Survivin expression correlates with clinical stage, histological grade, invasive behavior and survival rate in endometrial carcinoma. Cancer Letters 184:1, 105-116
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Najla Amira, Samia Mourah, François Rozet, Pierre Teillac, Jean Fiet, Philippe Aubin, Ariane Cortesse, François Desgrandchamps, Alain Le Duc, Olivier Cussenot, Hany Soliman. (2002) Non-invasive molecular detection of bladder cancer recurrence. International Journal of Cancer 101:3, 293-297
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Masatoshi Deguchi, Katsuya Shiraki, Hidekazu Inoue, Hiroshi Okano, Takeshi Ito, Takenari Yamanaka, Kazushi Sugimoto, Takahisa Sakai, Shigeru Ohmori, Kazumoto Murata, Akihiro Furusaka, Hisashi Hisatomi, Takeshi Nakano. (2002) Expression of survivin during liver regeneration. Biochemical and Biophysical Research Communications 297:1, 59-64
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Koichi Asanuma, Daisuke Kobayashi, Daisuke Furuya, Naoki Tsuji, Atsuhito Yagihashi, Naoki Watanabe. (2002) A Role for Survivin in Radioresistance of Pancreatic Cancer Cells. Cancer Science 93:9, 1057-1062
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Csaba Mahotka, Thomas Krieg, Andreas Krieg, Michael Wenzel, Christoph V. Suschek, Manfred Heydthausen, Helmut E. Gabbert, Claus D. Gerharz. (2002) Distinctin vivo expression patterns of survivin splice variants in renal cell carcinomas. International Journal of Cancer 100:1, 30-36
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