Nucleoside-catabolizing enzymes in mycoplasma-infected tumor cell cultures compromise the cytostatic activity of the anticancer drug gemcitabine

Journal of Biological Chemistry

Volumn 289, Issue 19, 2014, Pages 13054-13065

  Voorde, Johan Vande ^a   Sabuncuoǧlu, Suna ^a   Noppen, Sam ^b   Hofer, Anders ^b   Ranjbarian, Farahnaz ^c   Fieuws, Steffen ^a   Balzarini, Jan ^a   Liekens, Sandra ^a  

^a REGA INSTITUTE FOR MEDICAL RESEARCH   (Belgium)

^b UMEÅ UNIVERSITY   (Sweden)

^c KU LEUVEN   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

AMINES; AROMATIC COMPOUNDS; BIOMOLECULES; CELLS; CHEMOTHERAPY; ENZYME ACTIVITY; METABOLISM; RESTORATION; TUMORS;

ANTI-PROLIFERATIVE ACTIVITIES; CYTIDINE DEAMINASE; CYTOSTATIC ACTIVITIES; INTRACELLULAR METABOLISM; MYCOPLASMA PNEUMONIAE; MYCOPLASMA SPECIES; PYRIMIDINE NUCLEOSIDES; TUMOR MICROENVIRONMENT;

CELL CULTURE;

CYTIDINE DEAMINASE; DEOXYURIDINE; FLOXURIDINE; GEMCITABINE; PYRIMIDINE NUCLEOSIDE PHOSPHORYLASE; TETRAHYDROURIDINE; THYMIDINE; URIDINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOSTASIS; DRUG INACTIVATION; DRUG MECHANISM; DRUG METABOLISM; DRUG POTENTIATION; ENZYME ACTIVITY; ENZYME DEGRADATION; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR TRANSPORT; MOUSE; MYCOPLASMA HYORHINIS; MYCOPLASMA PNEUMONIA; MYCOPLASMOSIS; NONHUMAN; PRIORITY JOURNAL; TUMOR CELL CULTURE; TUMOR MICROENVIRONMENT;

ANTICANCER DRUG; CANCER THERAPY; CYTIDINE DEAMINASE; GEMCITABINE; MYCOPLASMA; MYCOPLASMA HYORHINIS; NUCLEOSIDE NUCLEOTIDE ANALOGS; NUCLEOSIDE NUCLEOTIDE METABOLISM; PHOSPHORYLASE; PYRIMIDINE NUCLEOSIDE PHOSPHORYLASE;

ANIMALS; ANTIMETABOLITES, ANTINEOPLASTIC; BACTERIAL PROTEINS; BREAST NEOPLASMS; CELL LINE, TUMOR; DEOXYCYTIDINE; FEMALE; HUMANS; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; MYCOPLASMA HYORHINIS; MYCOPLASMA INFECTIONS; PYRIMIDINE PHOSPHORYLASES; TETRAHYDROURIDINE; THYMIDINE; TUMOR MICROENVIRONMENT;

EID: 84900439025     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.558924     Document Type: Article

References (56)

1. Parker, W. B. (2009) Enzymology of purine and pyrimidine antimetabolites used in the treatment of cancer. Chem. Rev. 109, 2880-2893
2. Galmarini, C. M., Mackey, J. R., and Dumontet, C. (2002) Nucleoside analogues and nucleobases in cancer treatment. Lancet. Oncol. 3, 415-424
3. Huang, P., Chubb, S., Hertel, L. W., Grindey, G. B., and Plunkett W. (1991) Action of 2', 2'-difluorodeoxycytidine on DNA synthesis. Cancer Res. 51, 6110-6117
4. Ross, D. D., and Cuddy, D. P. (1994) Molecular effects of 2', 2'-difluorodeoxycytidine (Gemcitabine) on DNA replication in intact HL-60 cells. Biochem. Pharmacol. 48, 1619-1630
5. Heinemann, V., Hertel, L. W., Grindey, G. B., and Plunkett, W. (1988) Comparison of the cellular pharmacokinetics and toxicity of 2', 2'-difluorodeoxycytidine and 1-α-D-Arabinofuranosylcytosine. Cancer Res. 48, 4024-4031
6. Bergman, A. M., and Peters, G. J. (2006) Gemcitabine, mechanism of action and resistance. In Deoxynucleoside analogues in cancer therapy (Peters, G. J., ed) pp. 225-251, Humana Press Inc., Totowa, NJ
7. Heinemann, V., Xu, Y. Z., Chubb, S., Sen, A., Hertel, L. W., Grindey, G. B., and Plunkett, W. (1990) Inhibition of ribonucleotide reduction in CCRFCEM cells by 2', 2'-difluorodeoxycytidine. Mol. Pharmacol. 38, 567-572
8. Heinemann, V., Schulz, L., Issels, R. D., and Plunkett, W. (1995) Gemcitabine: a modulator of intracellular nucleotide and deoxynucleotide metabolism. Semin. Oncol. 22, 11-18
9. Xu, Y. Z., and Plunkett, W. (1992) Modulation of deoxycytidylate deaminase in intact human leukemia cells: action of 2', 2'- difluorodeoxycytidine. Biochem. Pharmacol. 44, 1819-1827
10. Iida, N., Dzutsev, A., Stewart, C. A., Smith, L., Bouladoux, N., Weingarten, R. A., Molina, D. A., Salcedo, R., Back, T., Cramer, S., Dai, R. M., Kiu, H., Cardone, M., Naik, S., Patri, A. K., Wang, E., Marincola, F. M., Frank, K. M., Belkaid, Y., Trinchieri, G., and Goldszmid, R. S. (2013) Commensal bacteria control cancer response to therapy by modulating the tumor microenvironment. Science 342, 967-970
11. Viaud, S., Saccheri, F., Mignot, G., Yamazaki, T., Daillère, R., Hannani, D., Enot, D. P., Pfirschke, C., Engblom, C., Pittet, M. J., Schlitzer, A., Ginhoux, F., Apetoh, L., Chachaty, E., Woerther, P. L., Eberl, G., Bérard, M., Ecobichon, C., Clermont, D., Bizet, C., Gaboriau-Routhiau, V., Cerf-Bensussan, N., Opolon, P., Yessaad, N., Vivier, E., Ryffel, B., Elson, C. O., Doré, J., Kroemer, G., Lepage, P., Boneca, I. G., Ghiringhelli, F., and Zitvogel, L. (2013) The intestinal microbiota modulates the anticancer immune effects of cyclophosphamide. Science 342, 971-976
12. Mager, D. L. (2006) Bacteria and cancer: cause, coincidence or cure? A review. J. Transl. Med. 4, 14
13. Cummins, J., and Tangney, M. (2013) Bacteria and tumours: causative agents or opportunistic inhabitants? Infect. Agent. Cancer 8, 11
14. Chan, P. J., Seraj, I. M., Kalugdan, T. H., and King, A. (1996) Prevalence of mycoplasma conserved DNA in malignant ovarian cancer detected using sensitive PCR-ELISA. Gynecol. Oncol. 63, 258-260
15. Kidder, M., Chan, P. J., Seraj, I. M., Patton, W. C., and King, A. (1998) Assessment of archived paraffin-embedded cervical condyloma tissues for mycoplasma-conservedDNAusing sensitive PCR-ELISA. Gynecol. Oncol. 71, 254-257
16. Huang, S., Li, J. Y., Wu, J., Meng, L., and Shou, C. C. (2001) Mycoplasma infections and different human carcinomas. World J. Gastroenterol. 7, 266-269
17. Pehlivan, M., Itirli, G., Onay, H., Bulut, H., Koyuncuoglu, M., and Pehlivan, S. (2004) Does Mycoplasma sp. play role in small cell lung cancer? Lung Cancer 45, 129-130
18. Pehlivan, M., Pehlivan, S., Onay, H., Koyuncuoglu, M., and Kirkali, Z. (2005) Can mycoplasma-mediated oncogenesis be responsible for formation of conventional renal cell carcinoma? Urology 65, 411-414
19. Yang, H., Qu, L., Ma, H., Chen, L., Liu, W., Liu, C., Meng, L., Wu, J., and Shou, C. (2010) Mycoplasma hyorhinis infection in gastric carcinoma and its effects on the malignant phenotypes of gastric cancer cells. BMC Gastroenterol. 10, 132
20. Apostolou, P., Tsantsaridou, A., Papasotiriou, I., Toloudi, M., Chatziioannou, M., and Giamouzis, G. (2011) Bacterial and fungal microflora in surgically removed lung cancer samples. J. Cardiothorac. Surg. 6, 137
21. Urbanek, C., Goodison, S., Chang, M., Porvasnik, S., Sakamoto, N., Li, C. Z., Boehlein, S. K., and Rosser, C. J. (2011) Detection of antibodies directed at M. hyorhinis p37 in the serum of men with newly diagnosed prostate cancer. BMC Cancer 11, 233
22. Barykova, Y. A., Logunov, D. Y., Shmarov, M. M., Vinarov, A. Z., Fiev, D. N., Vinarova, N. A., Rakovskaya, I. V., Baker, P. S., Shyshynova, I., Stephenson, A. J., Klein, E. A., Naroditsky, B. S., Gintsburg, A. L., and Gudkov, A. V. (2011) Association of Mycoplasma hominis infection with prostate cancer. Oncotarget 2, 289-297
23. Erturhan, S. M., Bayrak, O., Pehlivan, S., Ozgul, H., Seckiner, I., Sever, T., and Karakök, M. (2013) Can mycoplasma contribute to formation of prostate cancer? Int. Urol. Nephrol. 45, 33-38
24. Huang, G., Redelman-Sidi, G., Rosen, N., Glickman, M. S., and Jiang, X. (2012) Inhibition of mycobacterial infection by the tumor suppressor PTEN. J. Biol. Chem. 287, 23196-23202
25. Waites, K. B., and Talkington, D. F. (2004) Mycoplasma pneumoniae and its role as a human pathogen. Clin. Microbiol. Rev. 17, 697-728, table of contents
26. Razin, S., Yogev, D., and Naot, Y. (1998) Molecular biology and pathogenicity of mycoplasmas. Microbiol. Mol. Biol. Rev. 62, 1094-1156
27. Krause, D. C., and Taylor-Robinson, D. (1992) Mycoplasmas which infect humans. In: Mycoplasmas, molecular biology and pathogenesis (Maniloff, J., McElhaney, R. N., Finch, L. R., and Baseman, J. B., eds) pp. 417-744, American Society for Microbiology, Washington, D. C.
28. Finch, L. R., and Mitchell, A. (1992) Sources of nucleotides. In: Mycoplasmas, molecular biology and pathogenesis (Maniloff, J., McElhaney, R. N., Finch, L. R., and Baseman, J. B., eds) pp. 211-230, American Society for Microbiology, Washington, D. C.
29. Pollack, J. D., Williams, M. V., and McElhaney, R. N. (1997) The comparative metabolism of the mollicutes (mycoplasmas): the utility for taxonomic classification and the relationship of putative gene annotation and phylogeny to enzymatic function in the smallest free-living cells. Crit. Rev. Microbiol. 23, 269-354
30. Neale, G. A., Mitchell, A., and Finch, L. R. (1984) Uptake and utilization of deoxynucleoside 5'-monophosphates by Mycoplasma mycoides subsp. mycoides. J. Bacteriol. 158, 943-947
31. Tham, T. N., Ferris, S., Kovacic, R., Montagnier, L., and Blanchard, A. (1993) Identification of Mycoplasma pirum genes involved in the salvage pathways for nucleosides. J. Bacteriol. 175, 5281-5285
32. Bronckaers, A., Balzarini, J., and Liekens, S. (2008) The cytostatic activity of pyrimidine nucleosides is strongly modulated by Mycoplasma hyorhinis infection: implications for cancer therapy. Biochem. Pharmacol. 76, 188-197
33. Vande Voorde, J., Gago, F., Vrancken, K., Liekens, S., and Balzarini, J. (2012) Characterization of pyrimidine nucleoside phosphorylase of Mycoplasma hyorhinis: implications for the clinical efficacy of nucleoside analogues. Biochem. J. 445, 113-123
34. Liekens, S., Bronckaers, A., and Balzarini, J. (2009) Improvement of purine and pyrimidine antimetabolite-based anticancer treatment by selective suppression of mycoplasma-encoded catabolic enzymes. Lancet Oncol. 10, 628-635
35. Fukushima, M., Suzuki, N., Emura, T., Yano, S., Kazuno, H., Tada, Y., Yamada, Y., and Asao, T. (2000) Structure and activity of specific inhibitors of thymidine phosphorylase to potentiate the function of antitumor 2'-deoxyribonucleosides. Biochem. Pharmacol. 59, 1227-1236
36. Nakano, N. (1966) Establishment of cell lines in vitro from a mammary ascites tumor of mouse and biological properties of the established lines in a serum containing medium. Tohoku J. Exp. Med. 88, 69-84
37. Ayusawa, D., Koyama, H., Iwata, K., and Seno, T. (1980) Single-step selection of mouse FM3A cell mutants defective in thymidylate synthetase. Somatic Cell Genet. 6, 261-270
38. Wang, L., Schmidl, S., and Stülke, J. (2014) Mycoplasma pneumoniae thymidine phosphorylase. Nucleosides Nucleotides Nucleic Acids, in press
39. Balzarini, J., and De Clercq, E. (1984) Strategies for the measurement of the inhibitory effects of thymidine analogs on the activity of thymidylate synthase in intact murine leukemia L1210 cells. Biochim. Biophys. Acta 785, 36-45
40. Neff, T., and Blau, C. A. (1996) Forced expression of cytidine deaminase confers resistance to cytosine arabinoside and gemcitabine. Exp. Hematol. 24, 1340-1346
41. Yoshida, T., Endo, Y., Obata, T., Kosugi, Y., Sakamoto, K., and Sasaki, T. (2010) Influence of cytidine deaminase on antitumor activity of 2'-deoxycytidine analogs in vitro and in vivo. Drug Metab. Dispos. 38, 1814-1819
42. Bardenheuer, W., Lehmberg, K., Rattmann, I., Brueckner, A., Schneider, A., Sorg, U. R., Seeber, S., Moritz, T., and Flasshove, M. (2005) Resistance to cytarabine and gemcitabine and in vitro selection of transduced cells after retroviral expression of cytidine deaminase in human hematopoietic progenitor cells. Leukemia 19, 2281-2288
43. Amit, M., and Gil, Z. (2013) Macrophages increase the resistance of pancreatic adenocarcinoma cells to gemcitabine by up-regulating cytidine deaminase. Oncoimmunology 2, e27231
44. Weizman, N., Krelin, Y., Shabtay-Orbach, A., Amit, M., Binenbaum, Y., Wong, R. J., and Gil, Z. (2013) Macrophages mediate gemcitabine resistance of pancreatic adenocarcinoma by up-regulating cytidine deaminase. Oncogene 10.1038/onc.2013.357
45. McElwain, M. C., Chandler, D. K. F., Barile, M. F., Young, T. F., Tryon, V. V., Davis, J. W., Jr., Petzel, J. P., Chang, C. J., Williams, M. V., and Pollack, J. D. (1988) Purine and pyrimidine metabolism in Mollicutes species. Int. J. Syst. Bacteriol. 38, 417-423
46. Goodison, S., Urquidi, V., Kumar, D., Reyes, L., and Rosser, C. J. (2013) Complete genome sequence of Mycoplasma hyorhinis strain SK76. Genome Announc. 1, 1-2
47. Patterson, A. V., Zhang, H., Moghaddam, A., Bicknell, R., Talbot, D. C., Stratford, I. J., and Harris, A. L. (1995) Increased sensitivity to the prodrug 5'-deoxy-5-fluorouridine and modulation of 5-fluoro-2'-deoxyuridine sensitivity in MCF-7 cells transfected with thymidine phosphorylase. Br. J. Cancer 72, 669-675
48. Mini, E., Nobili, S., Caciagli, B., Landini, I., and Mazzei, T. (2006) Cellular pharmacology of gemcitabine. Ann. Oncol. 17, v7-v12
49. Jakway, J. P., and Shevach, E. M. (1984) Mycoplasma contamination: a hazard of screening hybridoma supernatants for inhibition of [3H]thymidine incorporation. J. Immunol. Methods 67, 337-345
50. Sinigaglia, F., and Talmadge, K. W. (1985) Inhibition of [3H]thymidine incorporation by Mycoplasma arginini-infected cells due to enzymatic cleavage of the nucleoside. Eur. J. Immunol. 15, 692-696
51. Merkenschlager, M., Kardamakis, D., Rawle, F. C., Spurr, N., and Beverley, P. C. (1988) Rate of incorporation of radiolabelled nucleosides does not necessarily reflect the metabolic state of cells in culture: effects of latent mycoplasma contamination. Immunology 63, 125-131
52. Hirschberg, L., Bölske, G., and Holme, T. (1989) Elimination of mycoplasmas from mouse myeloma cells by intraperitoneal passage in mice and by antibiotic treatment. Hybridoma 8, 249-257
53. Essig, A., Heinemann, M., Schweitzer, R., Simnacher, U., and Marre, R. (2000) Decontamination of a mycoplasma-infected Chlamydia pneumoniae strain by pulmonary passage in SCID mice. Int. J. Med. Microbiol. 290, 289-292
54. Vande Voorde, J., Liekens, S., and Balzarini, J. (2013) Mycoplasma hyorhinisencoded purine nucleoside phosphorylase: kinetic properties and its effect on the cytostatic potential of purine-based anticancer drugs. Mol. Pharmacol. 84, 865-875
55. Kreis, W., Budman, D. R., Chan, K., Allen, S. L., Schulman, P., Lichtman, S., Weiselberg, L., Schuster, M., Freeman, J., and Akerman, S. (1991) Therapy of refractory/relapsed acute leukemia with cytosine arabinoside plus tetrahydrouridine (an inhibitor of cytidine deaminase): a pilot study. Leukemia 5, 991-998
56. Yoshino, T., Mizunuma, N., Yamazaki, K., Nishina, T., Komatsu, Y., Baba, H., Tsuji, A., Yamaguchi, K., Muro, K., Sugimoto, N., Tsuji, Y., Moriwaki, T., Esaki, T., Hamada, C., Tanase, T., and Ohtsu, A. (2012) TAS-102 monotherapy for pretreated metastatic colorectal cancer: a double-blind, randomised, placebo-controlled phase 2 trial. Lancet Oncol. 13, 993-1001