Characterization of pyrimidine nucleoside phosphorylase of Mycoplasma hyorhinis: Implications for the clinical efficacy of nucleoside analogues

Biochemical Journal

Volumn 445, Issue 1, 2012, Pages 113-123

  Vande Voorde, Johan ^a   Gago, Federico ^b   Vrancken, Kristof ^a   Liekens, Sandra ^a   Balzarini, Jan ^a  

^a REGA INSTITUTE FOR MEDICAL RESEARCH   (Belgium)

^b UNIVERSITY OF ALCALÁ   (Spain)

Author keywords

Antiviral anticancer activity; Mycoplasma hyorhinis; Nucleoside analogue; Pyrimidine nucleoside phosphorylase (PyNP); Thymidine phosphorylase (TP); Uridine phosphorylase (UP)

Indexed keywords

5 (2 BROMOVINYL) 2' DEOXYURIDINE; DEOXYURIDINE; IDOXURIDINE; NUCLEOSIDE ANALOG; PYRIMIDINE NUCLEOSIDE PHOSPHORYLASE; THYMIDINE; THYMIDINE PHOSPHORYLASE;

ANTIVIRAL ACTIVITY; ARTICLE; CANCER CHEMOTHERAPY; CATABOLISM; CELL CULTURE; CYTOSTASIS; ENZYME ACTIVITY; ENZYME SPECIFICITY; ESCHERICHIA COLI; GENE; GENOME; HUMAN; HUMAN CELL; IMMUNOCOMPROMISED PATIENT; MOLECULAR CLONING; MYCOPLASMA; MYCOPLASMA HYORHINIS; MYCOPLASMOSIS; NONHUMAN; PH MEASUREMENT; PRIORITY JOURNAL; SEQUENCE ANALYSIS; TEMPERATURE MEASUREMENT; THYMIDINE PHOSPHORYLASE GENE;

AMINO ACID SEQUENCE; ANTIVIRAL AGENTS; BREAST NEOPLASMS; BROMODEOXYURIDINE; COMPUTATIONAL BIOLOGY; FEMALE; HUMANS; IDOXURIDINE; KINETICS; MOLECULAR SEQUENCE DATA; MYCOPLASMA HYORHINIS; MYCOPLASMA INFECTIONS; PROTEIN CONFORMATION; PYRIMIDINE NUCLEOSIDES; SEQUENCE HOMOLOGY, AMINO ACID; SUBSTRATE SPECIFICITY; THYMIDINE PHOSPHORYLASE; TUMOR CELLS, CULTURED; URIDINE PHOSPHORYLASE; VIRUSES;

EID: 84862501733     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20112225     Document Type: Article

References (61)

1. Galmarini, C. M., Mackey, J. R. and Dumontet, C. (2002) Nucleoside analogues and nucleobases in cancer treatment. Lancet Oncol. 3, 415-424 (Pubitemid 36958272)
2. De Clercq, E. (2004) Antivirals and antiviral strategies. Nat. Rev. Microbiol. 2, 704-720
3. 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
4. Jetté, L., Bissoon-Haqqani, S., Le François, B., Maroun, J. A. and Birnboim, H. C. (2008) Resistance of colorectal cancer cells to 5-FUdR and 5-FU caused by mycoplasma infection. Anticancer Res. 28, 2175-2180
5. 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
6. Vande Voorde, J., Liekens, S., McGuigan, C., Murziani, P. G., Slusarczyk, M. and Balzarini, J. (2011) The cytostatic activity of NUC-3073, a phosphoramidate prodrug of 5-fluoro-2′-deoxyuridine, is independent of activation by thymidine kinase and insensitive to degradation by phosphorolytic enzymes. Biochem. Pharmacol. 82, 441-452
7. Razin, S., Yogev, D. and Naot, Y. (1998) Molecular biology and pathogenicity of mycoplasmas. Microbiol. Mol. Biol. Rev. 62, 1094-1156 (Pubitemid 28558294)
8. Meyer, R. D. and Clough, W. (1993) Extragenital Mycoplasma hominis infections in adults: emphasis on immunosuppression. Clin. Infect. Dis. 17, S243-S249 (Pubitemid 23227139)
9. Wolff, A. J. and O'Donnell, A. E. (2003) HIV-related pulmonary infections: a review of the recent literature. Curr. Opin. Pulm. Med. 9, 210-214 (Pubitemid 36432896)
10. 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 (Pubitemid 26398609)
11. 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-conserved DNA using sensitive PCR-ELISA. Gynecol. Oncol. 71, 254-257 (Pubitemid 28550809)
12. 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 (Pubitemid 32377482)
13. 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 (Pubitemid 38757842)
14. 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 (Pubitemid 40248052)
15. 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
16. 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
17. 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
18. McGuigan, C., Murziani, P., Slusarczyk, M., Gonczy, B., Vande Voorde, J., Liekens, S. and Balzarini, J. (2011) Phosphoramidate ProTides of the anticancer agent FUDR successfully deliver the preformed bioactive monophosphate in cells and confer advantage over the parent nucleoside. J. Med. Chem. 54, 7247-7258
19. Pugmire, M. J. and Ealick, S. E. (2002) Structural analyses reveal two distinct families of nucleoside phosphorylases. Biochem. J. 361, 1-25 (Pubitemid 34171404)
20. 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 (Pubitemid 30157885)
21. Balzarini, J., Gamboa, A. E., Esnouf, R., Liekens, S., Neyts, J., De Clercq, E., Camarasa, M. J. and Pérez-Pérez, M. J. (1998) 7-Deazaxanthine, a novel prototype inhibitor of thymidine phosphorylase. FEBS Lett. 438, 91-95 (Pubitemid 28517841)
22. Liu, W., Fang, L., Li, S., Li, Q., Zhou, Z., Feng, Z., Luo, R., Shao, G., Wang, L., Chen, H. and Xiao, S. (2010) Complete genome sequence of Mycoplasma hyorhinis strain HUB-1. J Bacteriol. 192, 5844-5845
23. Liekens, S., Hernández, A. I., Ribatti, D., De Clercq, E., Camarasa, M. J., Pérez-Pérez, M. J. and Balzarini, J. (2004) The nucleoside derivative 5′-O-trityl-inosine (KIN59) suppresses thymidine phosphorylase-triggered angiogenesis via a noncompetitive mechanism of action. J. Biol. Chem. 279, 29598-29605 (Pubitemid 38915842)
24. Kelley, L. A. and Sternberg, M. J. (2009) Protein structure prediction on the web: a case study using the Phyre server. Nat. Protoc. 4, 363-371
25. 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
26. Desgranges, C., Razaka, G., Rabaud, M., Bricaud, H., Balzarini, J. and De Clercq, E. (1983) Phosphorolysis of (E) -5-(2-bromovinyl)-2′-deoxyuridine (BVDU) and other 5-substituted-2′-deoxyuridines by purified human thymidine phosphorylase and intact blood platelets. Biochem. Pharmacol. 32, 3583-3590 (Pubitemid 14205368)
27. Liermann, B. and Herrmann, G. (1983) (E) -5-(2-Bromovinyl)-2′- deoxyuridine: a good substrate for mammalian pyrimidine nucleoside phosphorylases. Biomed. Biochim. Acta 42, K35-K38 (Pubitemid 14127373)
28. Balzarini, J., Sienaert, R., Liekens, S., Van Kuilenburg, A., Carangio, A., Esnouf, R., De Clercq, E. and McGuigan, C. (2002) Lack of susceptibility of bicyclic nucleoside analogs, highly potent inhibitors of varicella-zoster virus, to the catabolic action of thymidine phosphorylase and dihydropyrimidine dehydrogenase. Mol. Pharmacol. 61, 1140-1145 (Pubitemid 34441779)
29. Kornspan, J. D., Lysnyansky, I., Kahan, T., Herrmann, R., Rottem, S. and Nir-Paz, R. (2011) Genome analysis of a Mycoplasma hyorhinis strain derived from a primary human melanoma cell line. J. Bacteriol. 193, 4543-4544
30. Rodriguez, R., Chinea, G., Lopez, N., Pons, T. and Vriend, G. (1998) Homology modeling, model and software evaluation: three related resources. Bioinformatics 14, 523-528 (Pubitemid 28416766)
31. Norman, R. A., Barry, S. T., Bate, M., Breed, J., Colls, J. G., Ernill, R. J., Luke, R. W., Minshull, C. A., McAlister, M. S., McCall, E. J. et al. (2004) Crystal structure of human thymidine phosphorylase in complex with a small molecule inhibitor. Structure 12, 75-84 (Pubitemid 38120276)
32. 85 in the catalytic mechanism of thymidine phosphorylase as assessed by targeted molecular dynamics simulations and quantum mechanical calculations. Biochemistry 43, 405-414
33. el Kouni, M. H., el Kouni, M. M. and Naguib, F. N. (1993) Differences in activities and substrate specificity of human and murine pyrimidine nucleoside phosphorylases: implications for chemotherapy with 5-fluoropyrimidines. Cancer Res. 53, 3687-3693
34. Saunders, P. P., Wilson, B. A. and Saunders, G. F. (1969) Purification and comparative properties of a pyrimidine nucleoside phosphorylase from Bacillus stearothermophilus. J. Biol. Chem. 244, 3691-3697
35. Scocca, J. J. (1971) Purification and substrate specificity of pyrimidine nucleoside phosphorylase from Haemophilus influenzae. J. Biol. Chem. 246, 6606-6610
36. Lee, C. S., Jiménez, B. M. and O'Sullivan, W. J. (1988) Purification and characterization of uridine (thymidine) phosphorylase from Giardia lamblia . Mol. Biochem. Parasitol. 30, 271-277
37. Walter, M. R., Cook, W. J., Cole, L. B., Short, S. A., Koszalka, G. W., Krenitsky, T. A. and Ealick, S. E. (1990) Three-dimensional structure of thymidine phosphorylase from Escherichia coli at 2.8Å resolution. J. Biol. Chem. 265, 14016-14022
38. Pugmire, M. J., Cook, W. J., Jasanoff, A., Walter, M. R. and Ealick, S. E. (1998) Structural and theoretical studies suggest domain movement produces an active conformation of thymidine phosphorylase. J. Mol. Biol. 81, 285-299 (Pubitemid 28360595)
39. Temmink, O. H., Emura, T., de Bruin, M., Fukushima, M. and Peters, G. J. (2007) Therapeutic potential of the dual-targeted TAS-102 formulation in the treatment of gastrointestinal malignancies. Cancer Sci. 98, 779-789 (Pubitemid 46691813)
40. Overman, M. J., Kopetz, S., Varadhachary, G., Fukushima, M., Kuwata, K., Mita, A., Wolff, R. A., Hoff, P., Xiong, H. and Abbruzzese, J. L. (2008) Phase I clinical study of three times a day oral administration of TAS-102 in patients with solid tumors. Cancer Invest. 26, 794-799
41. Overman, M. J., Varadhachary, G., Kopetz, S., Thomas, M. B., Fukushima, M., Kuwata, K., Mita, A., Wolff, R. A., Hoff, P. M., Xiong, H. and Abbruzzese, J. L. (2008) Phase 1 study of TAS-102 administered once daily on a 5-day-per-week schedule in patients with solid tumors. Invest. New Drugs 26, 445-454
42. Niedzwicki, J. G., Chu, S. H., el Kouni, M. H., Rowe, E. C. and Cha, S. (1982) 5-Benzylacyclouridine and 5-benzyloxybenzylacyclouridine, potent inhibitors of uridine phosphorylase. Biochem. Pharmacol. 31, 1857-1861 (Pubitemid 12123092)
43. Park, K. S., el Kouni, M. H., Krenitsky, T. A., Chu, S. H. and Cha, S. (1986) Inhibition of uridine phosphorylase from Escherichia coli by benzylacyclouridines. Biochem. Pharmacol. 35, 3853-3855 (Pubitemid 17180438)
44. Finnis, C., Dodsworth, N., Pollitt, C. E., Carr, G. and Sleep, D. (1993) Thymidine phosphorylase activity of platelet-derived endothelial growth factor is responsible for endothelial cell mitogenicity. Eur. J. Biochem. 212, 201-210 (Pubitemid 23064618)
45. McGarrity, G. J., Gamon, L., Steiner, T., Tully, J. and Kotani, H. (1985) Uridine phosphorylase activity among the class Mollicutes. Curr. Microbiol. 12, 107-112 (Pubitemid 15229928)
46. Finch, L. R. and Mitchell, A. (1992) Sources of nucleotides. In Mycoplasmas, Molecular Biology and Pathogenesis (Maniloff, J., McElhany, R., Fynch, L. and Baseman, J., eds), pp. 211-230, ASM Press, Washington, D.C.
47. Levine, E. M. (1972) Mycoplasma contamination of animal cell cultures: a simple, rapid detection method. Exp. Cell Res. 74, 99-109
48. Schneider, E. L., Stanbridge, E. J. and Epstein, C. J. (1974) Incorporation of 3H-uridine and 3H-uracil into RNA: a simple technique for the detection of mycoplasma contamination of cultured cells. Exp. Cell Res. 84, 311-318
49. 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 (Pubitemid 23232595)
50. Bizarro, C. V. and Schuck, D. C. (2007) Purine and pyrimidine nucleotide metabolism in Mollicutes. Genet. Mol. Biol. 30, 190-201 (Pubitemid 47496705)
51. Mushegian, A. R. and Koonin, E. V. (1996) A minimal gene set for cellular life derived by comparison of complete bacterial genomes. Proc. Natl. Acad. Sci. U.S.A. 93, 10268-10273 (Pubitemid 26314611)
52. Glass, J. I., Assad-Garcia, N., Alperovich, N., Yooseph, S., Lewis, M. R., Maruf, M., Hutchison, III, C. A., Smith, H. O. and Venter, J. C. (2006) Essential genes of a minimal bacterium. Proc. Natl. Acad. Sci. U.S.A. 103, 425-430 (Pubitemid 43122417)
53. Kuhner, S., van Noort, V., Betts, M. J., Leo-Macias, A., Batisse, C., Rode, M., Yamada, T., Maier, T., Bader, S., Beltran-Alvarez, P. et al. (2009) Proteome organization in a genome-reduced bacterium. Science 326, 1235-1240
54. Desgranges, C., Razaka, G., De Clercq, E., Herdewijn, P., Balzarini, J., Drouillet, F. and Bricaud, H. (1986) Effect of (E) -5-(2-bromovinyl)uracil on the catabolism and antitumor activity of 5-fluorouracil in rats and leukemic mice. Cancer Res. 46, 1094-1101 (Pubitemid 16048236)
55. Ogura, K., Nishiyama, T., Takubo, H., Kato, A., Okuda, H., Arakawa, K., Fukushima, M., Nagayama, S., Kawaguchi, Y. and Watabe, T. (1998) Suicidal inactivation of human dihydropyrimidine dehydrogenase by (E) -5-(2-bromovinyl)uracil derived from the antiviral, sorivudine. Cancer Lett. 122, 107-113 (Pubitemid 28058624)
56. Nishiyama, T., Ogura, K., Okuda, H., Suda, K., Kato, A. and Watabe, T. (2000) Mechanism-based inactivation of human dihydropyrimidine dehydrogenase by (E) -5-(2-bromovinyl)uracil in the presence of NADPH. Mol. Pharmacol. 57, 899-905 (Pubitemid 30253372)
57. Keizer, H. J., De Bruijn, E. A., Tjaden, U. R. and De Clercq, E. (1994) Inhibition of fluorouracil catabolism in cancer patients by the antiviral agent (E) -5-(2-bromovinyl)-2′-deoxyuridine. J. Cancer Res. Clin. Oncol. 120, 545-549 (Pubitemid 24246572)
58. Okuda, H., Nishiyama, T., Ogura, K., Nagayama, S., Ikeda, K., Yamaguchi, S., Nakamura, Y., Kawaguchi, K., Watabe, T. and Ogura, Y. (1997) Lethal drug interactions of sorivudine, a new antiviral drug, with oral 5-fluorouracil prodrugs. Drug Metab. Dispos. 25, 270-273 (Pubitemid 27086129)
59. Okuda, H., Ogura, K., Kato, A., Takubo, H. and Watabe, T. (1998) A possible mechanism of eighteen patient deaths caused by interactions of sorivudine, a new antiviral drug, with oral 5-fluorouracil prodrugs. J. Pharmacol. Exp. Ther. 287, 791-799 (Pubitemid 29133684)
60. Labenz, J., Friedich, D. and Falke, D. (1982) Analysis of the TK enzyme complex induced by HSV types 1 and 2 by means of isoelectric focusing and polyacrylamide gel electrophoresis. Arch. Virol. 71, 235-249 (Pubitemid 12072658)
61. Balzarini, J., De Clercq, E., Mertes, M. P., Shugar, D. and Torrence, P. F. (1982) 5-Substituted 2′-deoxyuridines: correlation between inhibition of tumor cell growth and inhibition of thymidine kinase and thymidylate synthetase. Biochem. Pharmacol. 31, 3673-3682 (Pubitemid 13244137)