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Clinical Cancer Research Vol. 6, 1322-1327, April 2000
© 2000 American Association for Cancer Research

Clinical Trials

Colorectal Tumors Responding to 5-Fluorouracil Have Low Gene Expression Levels of Dihydropyrimidine Dehydrogenase, Thymidylate Synthase, and Thymidine Phosphorylase1

Dennis Salonga, Kathleen D. Danenberg, Martin Johnson, Ralf Metzger, Susan Groshen, Denice D. Tsao-Wei, Heinz-Josef Lenz, C. Gail Leichman, Lawrence Leichman, Robert B. Diasio and Peter V. Danenberg2

University of Southern California/Norris Comprehensive Cancer Center, University of Southern California School of Medicine, Los Angeles, California 90033 [D. S., K. D. D., R. M., S. G., D. D. T-W., H-J. L., C. G. L., L. L., P. V. D.], and the Department of Pharmacology and Toxicology, University of Alabama, Birmingham, Alabama 35294 [M. J., R. B. D.]

We had previously shown that high gene expressions (mRNA levels) of thymidylate synthase (TS; Leichman et al., J. Clin. Oncol., 15: 3223–3229, 1997) and thymidine phosphorylase (TP; Metzger et al., Clin. Cancer Res., 4: 2371–2376, 1998) in pretreatment tumor biopsies could identify tumors that would be nonresponsive to 5-fluorouracil (5-FU)-based therapy. In this study, we investigated the association between intratumoral gene expression of the pyrimidine catabolism enzyme dihydropyrimidine dehydrogenase (DPD) and the response of colorectal tumors to the same 5-FU-based protocol. DPD expressions were measured by quantitative reverse transcription-PCR in 33 pretreatment biopsies of colorectal tumors from patients who went on to receive treatment with 5-FU and leucovorin (LV). The range of DPD gene expression in those tumors that were nonresponsive to 5-FU was much broader than that of the responding tumors. None of the tumors with basal-level DPD expressions above a DPD:ß-actin ratio of 2.5 x 10-3 (14 of 33) were responders to 5-FU/LV therapy, whereas those tumors with DPD gene expressions below DPD:ß-actin ratio of 2.5 x 10-3 had a response rate of 50%. There was no correlation among DPD, TS, and TP expression values in this set of colorectal tumors, which indicated that these gene expressions are independent variables. All of the tumors that responded to 5-FU therapy (11 of 33) had expression values of all three of the genes, TS, TP, and DPD, below their respective nonresponse cutoff values, whereas, in each of the nonresponding tumors, at least one of these gene expressions was high. The patients with low expression of all three of the genes had significantly longer survival than patients with a high value of any one of the gene expressions. The results of this study show that intratumoral gene expression level of DPD is associated with tumor response to 5-FU and that the use of more than one independent determinant of response permits the identification of a high percentage of responding patients.




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J. M. Mariadason, D. Arango, Q. Shi, A. J. Wilson, G. A. Corner, C. Nicholas, M. J. Aranes, M. Lesser, E. L. Schwartz, and L. H. Augenlicht
Gene Expression Profiling-Based Prediction of Response of Colon Carcinoma Cells to 5-Fluorouracil and Camptothecin
Cancer Res., December 15, 2003; 63(24): 8791 - 8812.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
S. P. Sanghani, S. K. Quinney, T. B. Fredenburg, Z. Sun, W. I. Davis, D. J. Murry, O. W. Cummings, D. E. Seitz, and W. F. Bosron
Carboxylesterases Expressed in Human Colon Tumor Tissue and Their Role in CPT-11 Hydrolysis
Clin. Cancer Res., October 15, 2003; 9(13): 4983 - 4991.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
A. B. P. van Kuilenburg, R. Meinsma, B. A. Zonnenberg, L. Zoetekouw, F. Baas, K. Matsuda, N. Tamaki, and A. H. van Gennip
Dihydropyrimidinase Deficiency and Severe 5-Fluorouracil Toxicity
Clin. Cancer Res., October 1, 2003; 9(12): 4363 - 4367.
[Abstract] [Full Text] [PDF]

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 JCOHome page
A. Alimonti, G. Ferretti, S. Di Cosimo, F. Cognetti, and A. Vecchione
Can Colorectal Cancer Patients With Thymidylate Synthase-Overexpressing Liver Metastases Have an Overall Survival Advantage With Hepatic Arterial Infusion Alone?
J. Clin. Oncol., September 15, 2003; 21(18): 3543 - 3544.
[Full Text] [PDF]

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 Clin. Cancer Res.Home page
M. Kornmann, W. Schwabe, S. Sander, M. Kron, J. Strater, S. Polat, E. Kettner, H. F. Weiser, W. Baumann, H. Schramm, et al.
Thymidylate Synthase and Dihydropyrimidine Dehydrogenase mRNA Expression Levels: Predictors for Survival in Colorectal Cancer Patients Receiving Adjuvant 5-Fluorouracil
Clin. Cancer Res., September 15, 2003; 9(11): 4116 - 4124.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
M. van Rijnsoever, H. Elsaleh, D. Joseph, K. McCaul, and B. Iacopetta
CpG Island Methylator Phenotype Is an Independent Predictor of Survival Benefit from 5-Fluorouracil in Stage III Colorectal Cancer
Clin. Cancer Res., August 1, 2003; 9(8): 2898 - 2903.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
H. Ezzeldin, M. R. Johnson, Y. Okamoto, and R. Diasio
Denaturing High Performance Liquid Chromatography Analysis of the DPYD Gene in Patients with Lethal 5-Fluorouracil Toxicity
Clin. Cancer Res., August 1, 2003; 9(8): 3021 - 3028.
[Abstract] [Full Text] [PDF]

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 Jpn J Clin OncolHome page
The Colorectal Cancer Chemotherapy Study Group of
Results of a Randomized Trial with or without 5-FU-based Preoperative Chemotherapy followed by Postoperative Chemotherapy in Resected Colon and Rectal Carcinoma
Jpn. J. Clin. Oncol., June 1, 2003; 33(6): 288 - 296.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
V. Cohen, V. Panet-Raymond, N. Sabbaghian, I. Morin, G. Batist, and R. Rozen
Methylenetetrahydrofolate Reductase Polymorphism in Advanced Colorectal Cancer: A Novel Genomic Predictor of Clinical Response to Fluoropyrimidine-based Chemotherapy
Clin. Cancer Res., May 1, 2003; 9(5): 1611 - 1615.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
J. R. Bertino and D. Banerjee
Is the Measurement of Thymidylate Synthase to Determine Suitability for Treatment with 5-Fluoropyrimidines Ready for Prime Time?
Clin. Cancer Res., April 1, 2003; 9(4): 1235 - 1239.
[Full Text] [PDF]

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 Clin. Cancer Res.Home page
A. Salesiotis, R. Soong, R. B. Diasio, A. Frost, and K. J. Cullen
Capecitabine Induces Rapid, Sustained Response in Two Patients with Extensive Oral Verrucous Carcinoma
Clin. Cancer Res., February 1, 2003; 9(2): 580 - 585.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
W. Ichikawa, H. Uetake, Y. Shirota, H. Yamada, N. Nishi, Z. Nihei, K. Sugihara, and R. Hirayama
Combination of Dihydropyrimidine Dehydrogenase and Thymidylate Synthase Gene Expressions in Primary Tumors as Predictive Parameters for the Efficacy of Fluoropyrimidine-based Chemotherapy for Metastatic Colorectal Cancer
Clin. Cancer Res., February 1, 2003; 9(2): 786 - 791.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
D. C. Farrugia, H. E. R. Ford, D. Cunningham, K. D. Danenberg, P. V. Danenberg, J. Brabender, A. D. McVicar, G. W. Aherne, A. Hardcastle, K. McCarthy, et al.
Thymidylate Synthase Expression in Advanced Colorectal Cancer Predicts for Response to Raltitrexed
Clin. Cancer Res., February 1, 2003; 9(2): 792 - 801.
[Abstract] [Full Text] [PDF]

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 Br Med BullHome page
N J Maughan and P Quirke
Pathology - a molecular prognostic approach: Advances in colorectal cancer
Br. Med. Bull., December 1, 2002; 64(1): 59 - 74.
[Abstract] [Full Text] [PDF]

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 Ann OncolHome page
C. Aschele, D. Debernardis, R. Bandelloni, S. Cascinu, V. Catalano, P. Giordani, S. Barni, D. Turci, G. Drudi, S. Lonardi, et al.
Thymidylate synthase protein expression in colorectal cancer metastases predicts for clinical outcome to leucovorin-modulated bolus or infusional 5-fluorouracil but not methotrexate-modulated bolus 5-fluorouracil
Ann. Onc., December 1, 2002; 13(12): 1882 - 1892.
[Abstract] [Full Text] [PDF]

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 Arch SurgHome page
A. J. Bilchik, D. T. Nora, S. Saha, R. Turner, D. Wiese, C. Kuo, X. Ye, D. L. Morton, and D. S. B. Hoon
The Use of Molecular Profiling of Early Colorectal Cancer to Predict Micrometastases
Arch Surg, December 1, 2002; 137(12): 1377 - 1383.
[Abstract] [Full Text] [PDF]

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 Molecular Cancer TherapeuticsHome page
C. Blanquicett, G. Y. Gillespie, L. B. Nabors, C. R. Miller, S. Bharara, D. J. Buchsbaum, Robert. B. Diasio, and M. R. Johnson
Induction of Thymidine Phosphorylase in Both Irradiated and Shielded, Contralateral Human U87MG Glioma Xenografts: Implications for a Dual Modality Treatment Using Capecitabine and Irradiation
Mol. Cancer Ther., October 1, 2002; 1(12): 1139 - 1145.
[Abstract] [Full Text] [PDF]

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 JCOHome page
M. Castro
Eniluracil's Need for a Targeted Approach: A Lesson in Drug Development
J. Clin. Oncol., September 1, 2002; 20(17): 3750 - 3750.
[Full Text] [PDF]

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 The OncologistHome page
B. A. Chabner
Cytotoxic Agents in the Era of Molecular Targets and Genomics
Oncologist, August 1, 2002; 7(90003): 34 - 41.
[Abstract] [Full Text] [PDF]

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 Ann. Surg. Oncol.Home page
Y. Shirota, W. Ichikawa, H. Uetake, H. Yamada, Z. Nihei, and K. Sugihara
Intratumoral Dihydropyrimidine Dehydrogenase Messenger RNA Level Reflects Tumor Progression in Human Colorectal Cancer
Ann. Surg. Oncol., July 1, 2002; 9(6): 599 - 603.
[Abstract] [Full Text] [PDF]

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M.-C. Etienne, M. Chazal, P. Laurent-Puig, N. Magne, C. Rosty, J.-L. Formento, M. Francoual, P. Formento, N. Renee, E. Chamorey, et al.
Prognostic Value of Tumoral Thymidylate Synthase and p53 in Metastatic Colorectal Cancer Patients Receiving Fluorouracil-Based Chemotherapy: Phenotypic and Genotypic Analyses
J. Clin. Oncol., June 15, 2002; 20(12): 2832 - 2843.
[Abstract] [Full Text] [PDF]

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M. M. Borner, D. Dietrich, R. Stupp, R. Morant, H. Honegger, M. Wernli, R. Herrmann, B. C. Pestalozzi, P. Saletti, S. Hanselmann, et al.
Phase II Study of Capecitabine and Oxaliplatin in First- and Second-Line Treatment of Advanced or Metastatic Colorectal Cancer
J. Clin. Oncol., April 1, 2002; 20(7): 1759 - 1766.
[Abstract] [Full Text] [PDF]

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 Ann OncolHome page
C.-H. Kohne, D. Cunningham, F. Di Costanzo, B. Glimelius, G. Blijham, E. Aranda, W. Scheithauer, P. Rougier, M. Palmer, J. Wils, et al.
Clinical determinants of survival in patients with 5-fluorouracil- based treatment for metastatic colorectal cancer: results of a multivariate analysis of 3825 patients
Ann. Onc., February 20, 2002; 13(2): 308 - 317.
[Abstract] [Full Text] [PDF]

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 JCOHome page
R. L. Schilsky, D. Bertucci, N. J. Vogelzang, H. L. Kindler, and M. J. Ratain
Dose-Escalating Study of Capecitabine Plus Gemcitabine Combination Therapy in Patients With Advanced Cancer
J. Clin. Oncol., January 15, 2002; 20(2): 582 - 587.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
H. Zembutsu, Y. Ohnishi, T. Tsunoda, Y. Furukawa, T. Katagiri, Y. Ueyama, N. Tamaoki, T. Nomura, O. Kitahara, R. Yanagawa, et al.
Genome-wide cDNA Microarray Screening to Correlate Gene Expression Profiles with Sensitivity of 85 Human Cancer Xenografts to Anticancer Drugs
Cancer Res., January 1, 2002; 62(2): 518 - 527.
[Abstract] [Full Text] [PDF]

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Y. Shirota, J. Stoehlmacher, J. Brabender, Y.-P. Xiong, H. Uetake, K. D. Danenberg, S. Groshen, D. D. Tsao-Wei, P. V. Danenberg, and H.-J. Lenz
ERCC1 and Thymidylate Synthase mRNA Levels Predict Survival for Colorectal Cancer Patients Receiving Combination Oxaliplatin and Fluorouracil Chemotherapy
J. Clin. Oncol., December 1, 2001; 19(23): 4298 - 4304.
[Abstract] [Full Text]

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 Molecular Cancer TherapeuticsHome page
J. Ciccolini, P. Cuq, A. Evrard, S. Giacometti, A. Pelegrin, C. Aubert, J.-P. Cano, and A. Iliadis
Combination of Thymidine Phosphorylase Gene Transfer and Deoxyinosine Treatment Greatly Enhances 5-Fluorouracil Antitumor Activity in Vitro and in Vivo
Mol. Cancer Ther., December 1, 2001; 1(2): 133 - 139.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
K. Kawakami, D. Salonga, J. M. Park, K. D. Danenberg, H. Uetake, J. Brabender, K. Omura, G. Watanabe, and P. V. Danenberg
Different Lengths of a Polymorphic Repeat Sequence in the Thymidylate Synthase Gene Affect Translational Efficiency but Not Its Gene Expression
Clin. Cancer Res., December 1, 2001; 7(12): 4096 - 4101.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
A. B. P. van Kuilenburg, E. W. Muller, J. Haasjes, R. Meinsma, L. Zoetekouw, H. R. Waterham, F. Baas, D. J. Richel, and A. H. van Gennip
Lethal Outcome of a Patient with a Complete Dihydropyrimidine Dehydrogenase (DPD) Deficiency after Administration of 5-Fluorouracil: Frequency of the Common IVS14+1G>A Mutation Causing DPD Deficiency
Clin. Cancer Res., May 1, 2001; 7(5): 1149 - 1153.
[Abstract] [Full Text]

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 NEJMHome page
T. Watanabe, T.-T. Wu, P. J. Catalano, T. Ueki, R. Satriano, D. G. Haller, A. B. Benson, and S. R. Hamilton
Molecular Predictors of Survival after Adjuvant Chemotherapy for Colon Cancer
N. Engl. J. Med., April 19, 2001; 344(16): 1196 - 1206.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
J. L. Grem, K. D. Danenberg, K. Behan, A. Parr, L. Young, P. V. Danenberg, D. Nguyen, J. Drake, A. Monks, and C. J. Allegra
Thymidine Kinase, Thymidylate Synthase, and Dihydropyrimidine Dehydrogenase Profiles of Cell Lines of the National Cancer Institute's Anticancer Drug Screen
Clin. Cancer Res., April 1, 2001; 7(4): 999 - 1009.
[Abstract] [Full Text]

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 Clin. Cancer Res.Home page
A. B. P. van Kuilenburg, J. Haasjes, D. J. Richel, L. Zoetekouw, H. Van Lenthe, R. A. De Abreu, J. G. Maring, P. Vreken, and A. H. van Gennip
Clinical Implications of Dihydropyrimidine Dehydrogenase (DPD) Deficiency in Patients with Severe 5-Fluorouracil-associated Toxicity: Identification of New Mutations in the DPD Gene
Clin. Cancer Res., December 1, 2000; 6(12): 4705 - 4712.
[Abstract] [Full Text]


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