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[Cancer Research 55, 1407-1412, April 1, 1995]
© 1995 American Association for Cancer Research
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Thymidylate Synthase Gene and Protein Expression Correlate and Are Associated with Response to 5-Fluorouracil in Human Colorectal and Gastric Tumors1

Patrick G. Johnston2, Heinz-Josef Lenz, Cynthia G. Leichman, Kathleen D. Danenberg, Carmen J. Allegra, Peter V. Danenberg and Lawrence Leichman

NCI-Navy Medical Oncology Branch, National Cancer Institute, National Institute of Health, Bethesda, Maryland 20889-5105 [P. G. J., C. J. A.], and Norris Comprehensive Cancer Center, University of Southern California School of Medicine, Los Angeles, California 90033 [H-J. L., C. G. L., K. D. D., P. V. D., L. L.]

Thymidylate synthase (TS) is the target enzyme for 5-fluorouracil (5-FU). We have correlated TS protein and gene expression with the response in patients with colorectal (n = 9) and gastric cancer (n = 12) treated with infusional 5-FU plus leucovorin (LV) or infusional 5-FU/LV and cisplatin, respectively. TS protein expression was analyzed by Western blot using TS106 monoclonal antibody and densitometry scanning. TS gene expression was measured by PCR analysis using ß-actin as an internal standard and expressed as a TS:ß-actin mRNA ratio. A close linear relationship was noted between TS protein expression and TS gene expression (r2 = 0.60) for the 21 tumor samples analyzed. TS immunohistochemical staining on 15 of the 21 samples revealed that the TS staining intensity correlated closely with TS protein and mRNA expression. In two biopsy samples, TS protein levels and TS gene expression did not correlate; however, one of these exhibited a focal TS staining pattern.

Both the TS protein level and TS gene expression were significantly associated with response to 5-FU-based therapy. Patients with responsive disease had a mean TS protein level of 0.17 ± 0.03 arbitrary units (range, 0.05 to 0.38), whereas in patients whose tumors did not respond, the mean TS protein level was significantly higher 0.60 ± 0.09 (range, 0.06 to 1.01; P < 0.01). A similar pattern was noted with TS gene expression. In patients with responsive disease, the mean TS:ß-actin gene ratio was 1.36 ± 0.3 (range, 0.5–3.3 x 10-3). In contrast, biopsies from patients with unresponsive disease had a mean TS:ß-actin gene ratio of 15.4 ± 2.6 x 10-3 (range, 2.7–35.9; P < 0.01). TS protein and TS mRNA expression are highly correlated, and each predict for response to 5-FU/LV-based chemotherapy in patients with colorectal and gastric cancer.

1 Partially supported by Grants 5 U01 CA60108 and 5 R01 CA56119 from the National Cancer Institute.

2 To whom requests for reprints should be addressed, at NCI-Navy Medical Oncology Branch, National Cancer Institute, National Naval Medical Center, 8901 Wisconsin Ave., Bldg. 8, Room 5101, Bethesda, MD 20889-5105.

Received 12/22/94. Accepted 2/14/95.




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M. L. Rothenberg
Irinotecan (CPT-11): Recent Developments and Future Directions-Colorectal Cancer and Beyond
Oncologist, February 1, 2001; 6(1): 66 - 80.
[Abstract] [Full Text]

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 Nucleic Acids ResHome page
J. C. Schmitz, D. Yu, S. Agrawal, and E. Chu
Effect of 2'-O-methyl antisense ORNs on expression of thymidylate synthase in human colon cancer RKO cells
Nucleic Acids Res., January 15, 2001; 29(2): 415 - 422.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
T. Grundei, H. Vogelsang, K. Ott, J. Mueller, M. Scholz, K. Becker, U. Fink, J. R. Siewert, H. Höfler, and G. Keller
Loss of Heterozygosity and Microsatellite Instability as Predictive Markers for Neoadjuvant Treatment in Gastric Carcinoma
Clin. Cancer Res., December 1, 2000; 6(12): 4782 - 4788.
[Abstract] [Full Text]

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 Cancer Res.Home page
R. D. Ladner, F. J. Lynch, S. Groshen, Y. P. Xiong, A. Sherrod, S. J. Caradonna, J. Stoehlmacher, and H.-J. Lenz
dUTP Nucleotidohydrolase Isoform Expression in Normal and Neoplastic Tissues: Association with Survival and Response to 5-Fluorouracil in Colorectal Cancer
Cancer Res., July 1, 2000; 60(13): 3493 - 3503.
[Abstract] [Full Text]

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 Clin. Cancer Res.Home page
M. Kasahara, Y. Takahashi, T. Nagata, S. Asai, T. Eguchi, Y. Ishii, M. Fujii, and K. Ishikawa
Thymidylate Synthase Expression Correlates Closely with E2F1 Expression in Colon Cancer
Clin. Cancer Res., July 1, 2000; 6(7): 2707 - 2711.
[Abstract] [Full Text]

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 Clin. Cancer Res.Home page
S. J. Welsh, J. Titley, L. Brunton, M. Valenti, P. Monaghan, A. L. Jackman, and G. W. Aherne
Comparison of Thymidylate Synthase (TS) Protein Up-Regulation after Exposure to TS Inhibitors in Normal and Tumor Cell Lines and Tissues
Clin. Cancer Res., June 1, 2000; 6(6): 2538 - 2546.
[Abstract] [Full Text]

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 Cancer Res.Home page
D. Banerjee, R. Gorlick, A. Liefshitz, K. Danenberg, P. C. Danenberg, P. V. Danenberg, D. Klimstra, S. Jhanwar, C. Cordon-Cardo, Y. Fong, et al.
Levels of E2F-1 Expression Are Higher in Lung Metastasis of Colon Cancer As Compared with Hepatic Metastasis and Correlate with Levels of Thymidylate Synthase
Cancer Res., May 1, 2000; 60(9): 2365 - 2367.
[Abstract] [Full Text]

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 Clin. Cancer Res.Home page
D. Salonga, K. D. Danenberg, M. Johnson, R. Metzger, S. Groshen, D. D. Tsao-Wei, H.-J. Lenz, C. G. Leichman, L. Leichman, R. B. Diasio, et al.
Colorectal Tumors Responding to 5-Fluorouracil Have Low Gene Expression Levels of Dihydropyrimidine Dehydrogenase, Thymidylate Synthase, and Thymidine Phosphorylase
Clin. Cancer Res., April 1, 2000; 6(4): 1322 - 1327.
[Abstract] [Full Text]

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 Clin. Cancer Res.Home page
D. Edler, M. Hallström, P. G. Johnston, I. Magnusson, P. Ragnhammar, and H. Blomgren
Thymidylate Synthase Expression: An Independent Prognostic Factor for Local Recurrence, Distant Metastasis, Disease-free and Overall Survival in Rectal Cancer
Clin. Cancer Res., April 1, 2000; 6(4): 1378 - 1384.
[Abstract] [Full Text]

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 Clin. Cancer Res.Home page
D. Edler, U. Kressner, P. Ragnhammar, P. G. Johnston, I. Magnusson, B. Glimelius, L. Påhlman, G. Lindmark, and H. Blomgren
Immunohistochemically Detected Thymidylate Synthase in Colorectal Cancer: An Independent Prognostic Factor of Survival
Clin. Cancer Res., February 1, 2000; 6(2): 488 - 492.
[Abstract] [Full Text]

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 J. Histochem. Cytochem.Home page
A. S. Haqqani, R. T. Cowling, J. A. Maroun, and H. C. Birnboim
Characterization of a Polyclonal Antibody to Human Thymidylate Synthase Suitable for the Study of Colorectal Cancer Specimens
J. Histochem. Cytochem., December 1, 1999; 47(12): 1563 - 1574.
[Abstract] [Full Text]

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 Clin. Cancer Res.Home page
H. Shiga, E. I. Heath, A. A. Rasmussen, B. Trock, P. G. Johnston, A. A. Forastiere, M. Langmacher, A. Baylor, M. Lee, and K. J. Cullen
Prognostic Value of p53, Glutathione S-Transferase {{pi}}, and Thymidylate Synthase for Neoadjuvant Cisplatin-based Chemotherapy in Head and Neck Cancer
Clin. Cancer Res., December 1, 1999; 5(12): 4097 - 4104.
[Abstract] [Full Text] [PDF]

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 Mol. Pharmacol.Home page
M. E. Kitchens, A. M. Forsthoefel, K. W. Barbour, H. T. Spencer, and F. G. Berger
Mechanisms of Acquired Resistance to Thymidylate Synthase Inhibitors: The Role of Enzyme Stability
Mol. Pharmacol., November 1, 1999; 56(5): 1063 - 1070.
[Abstract] [Full Text]

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 Clin. Cancer Res.Home page
J. L. Grem, J. M. Sorensen, E. Cullen, C. H. Takimoto, S. M. Steinberg, A. P. Chen, J. M. Hamilton, S. G. Arbuck, N. McAtee, D. Lawrence, et al.
A Phase I Study of Raltitrexed, an Antifolate Thymidylate Synthase Inhibitor, in Adult Patients with Advanced Solid Tumors
Clin. Cancer Res., September 1, 1999; 5(9): 2381 - 2391.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
J. M. Collins, R. W. Klecker, and A. G. Katki
Suicide Prodrugs Activated by Thymidylate Synthase: Rationale for Treatment and Noninvasive Imaging of Tumors with Deoxyuridine Analogues
Clin. Cancer Res., August 1, 1999; 5(8): 1976 - 1981.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
S. Cascinu, C. Aschele, S. Barni, D. Debernardis, C. Baldo, G. Tunesi, V. Catalano, M. P. Staccioli, A. Brenna, P. Muretto, et al.
Thymidylate Synthase Protein Expression in Advanced Colon Cancer: Correlation with the Site of Metastasis and the Clinical Response to Leucovorin-modulated Bolus 5-Fluorouracil
Clin. Cancer Res., August 1, 1999; 5(8): 1996 - 1999.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
M. Kornmann, K. D. Danenberg, N. Arber, H. G. Beger, P. V. Danenberg, and M. Korc
Inhibition of Cyclin D1 Expression in Human Pancreatic Cancer Cells Is Associated with Increased Chemosensitivity and Decreased Expression of Multiple Chemoresistance Genes
Cancer Res., July 1, 1999; 59(14): 3505 - 3511.
[Abstract] [Full Text] [PDF]

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 JCOHome page
C. Aschele, D. Debernardis, S. Casazza, G. Antonelli, G. Tunesi, C. Baldo, R. Lionetto, F. Maley, and A. Sobrero
Immunohistochemical Quantitation of Thymidylate Synthase Expression in Colorectal Cancer Metastases Predicts for Clinical Outcome to Fluorouracil-Based Chemotherapy
J. Clin. Oncol., June 1, 1999; 17(6): 1760 - 1760.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
Y. Ishikawa, T. Kubota, Y. Otani, M. Watanabe, T. Teramoto, K. Kumai, M. Kitajima, T. Takechi, H. Okabe, and M. Fukushima
Dihydropyrimidine Dehydrogenase Activity and Messenger RNA Level May Be Related to the Antitumor Effect of 5-Fluorouracil on Human Tumor Xenografts in Nude Mice
Clin. Cancer Res., April 1, 1999; 5(4): 883 - 889.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
M. M. Davies, P. G. Johnston, S. Kaur, and T. G. Allen-Mersh
Colorectal Liver Metastasis Thymidylate Synthase Staining Correlates with Response to Hepatic Arterial Floxuridine
Clin. Cancer Res., February 1, 1999; 5(2): 325 - 328.
[Abstract] [Full Text] [PDF]

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 The OncologistHome page
M. R. Posner, P. G. Johnston, R. B. Tishler, J. Andersen, M. Fiorentino, P. M. Busse, L. A. Cavacini, A. D. Colevas, J. Clark, and C. M. Norris
The Prognostic Value of Thymidylate Synthase and p53 Expression in Patients Treated with Induction Chemotherapy for Squamous Cell Carcinoma of the Head and Neck
Oncologist, December 1, 1998; 3(6): 424 - 431.
[Abstract] [Full Text]

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 BloodHome page
R. Gorlick, E. Goker, T. Trippett, P. Steinherz, Y. Elisseyeff, M. Mazumdar, W. F. Flintoff, and J. R. Bertino
Defective Transport Is a Common Mechanism of Acquired Methotrexate Resistance in Acute Lymphocytic Leukemia and Is Associated With Decreased Reduced Folate Carrier Expression
Blood, February 1, 1997; 89(3): 1013 - 1018.
[Abstract] [Full Text] [PDF]

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 The OncologistHome page
J. Jolivet, A. Dayan, M. Beauchemin, D. Chahla, A. Mamo, and R. Bertrand
Biochemical and Molecular Studies of Human Methenyltetrahydrofolate Synthetase
Oncologist, August 1, 1996; 1(4): 248 - 253.
[Abstract] [Full Text] [PDF]

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 The OncologistHome page
E. Chu, J. L. Grem, P. G. Johnston, and C. J. Allegra
New Concepts for the Development and Use of Antifolates
Oncologist, August 1, 1996; 1(4): 255 - 259.
[Abstract] [Full Text] [PDF]


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