Engineering an arginine catabolizing bioconjugate: Biochemical and pharmacological characterization of PEGylated derivatives of arginine deiminase from Mycoplasma arthritidis

Bioconjugate Chemistry

Volumn 17, Issue 6, 2006, Pages 1447-1459

  Wang, Maoliang ^a   Basu, Amartya ^a   Palm, Thomas ^a   Hua, Jack ^a   Youngster, Stephen ^a   Hwang, Lisa ^a   Liu, Hsien Ching ^a   Li, Xiguang ^a   Peng, Ping ^a   Zhang, Yue ^a   Zhao, Hong ^a   Zhang, Zhihua ^a   Longley, Clifford ^a   Mehlig, Mary ^a   Borowski, Virna ^a   Sai, Prakash ^a   Viswanathan, Manickam ^a   Jang, Eun ^a   Petti, Gerald ^a   Liu, Sam ^a   Yang, Karen ^a   Filpula, David ^a   more..

^a Enzon Incorporated   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; DIMERS; ENZYME ACTIVITY; ENZYME INHIBITION; MAMMALS; NITRIC OXIDE; PHARMACOKINETICS; POLYETHYLENE GLYCOLS; STRUCTURAL OPTIMIZATION; TUMORS;

ANIMAL MODEL; ARGININE DEIMINASES; BIOCHEMICAL CHARACTERIZATION; BIOCONJUGATES; ENZYMATIC PROPERTIES; ENZYMES ACTIVITY; INTRAMUSCULAR; NORMAL FUNCTION; PEGYLATED; PHARMACOLOGICAL CHARACTERIZATION;

BIOMOLECULES;

ARGININE; ARGININE DEIMINASE; ARGININOSUCCINATE SYNTHASE; MACROGOL; RECOMBINANT ARGININE DEIMINASE; SUCCINIMIDE DERIVATIVE; SUCCINIMIDYL CARBONATE; UNCLASSIFIED DRUG;

AMINO ACID BLOOD LEVEL; ANIMAL CELL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL CULTURE; CANCER INHIBITION; CONTROLLED STUDY; CORRELATION ANALYSIS; DRUG CONJUGATION; DRUG POTENCY; DRUG STABILITY; DRUG STRUCTURE; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME ENGINEERING; ENZYME STABILITY; HUMAN; HUMAN CELL; IC 50; MOLECULAR WEIGHT; MOUSE; MYCOPLASMA ARTHRITIDIS; NONHUMAN; PH; PHARMACODYNAMICS; STRUCTURE ACTIVITY RELATION;

ANIMALIA; MYCOPLASMA ARTHRITIDIS; PSEUDOMONAS PUTIDA; RODENTIA;

EID: 33845200825     PISSN: 10431802     EISSN: None     Source Type: Journal    
DOI: 10.1021/bc060198y     Document Type: Article

References (59)

1. Abuchowski, A., Kazo, G. M., Verhoest, C. R., Van Es, T., Kafkewitz, D., Nucci, M. L., Viau, A. T., and Davis, F. F. (1984) Cancer therapy with chemically modified enzymes. 1. Antitumor properties of polyethylene glycol-modified asparaginase conjugates. Cancer Biochem. Biophys. 7, 175-186.
2. Wheatley, D. N. (2004) Controlling cancer by restricting arginine availability - arginine-catabolizing enzymes as anticancer agents. Anti-Cancer Drugs. 15, 825-833.
3. Takakura, T., Takimoto, A., Notsu, Y., Yoshida, H., Ito, T., Nagatome, H., Ohno, M., Kobayashi, Y., Yoshioka, T., Inagaki, K., Yagi, S., Hoffman, R. M., and Esaki, N. (2006) Physicochemical and pharmacokinetic characterization of highly potent recombinant L-methionine gamma-lyase conjugated with polyethylene glycol as an antitumor agent. Cancer Res. 66, 2807-2814.
4. Chan, B., Wara, D., Bastian, J., Hershfield, M. S., Bohnsack, J., Azen, C. G., Parkman, R., Weinberg, K., and Kohn, D. B. (2005) Long-term efficacy of enzyme replacement therapy for adenosine deaminase (ADA)-deficient severe combined immunodeficiency (SCID). Clin. Immunol. 117, 133-143.
5. Chester, K. A., Baker, M., and Mayer, A. (2005) Overcoming the immunologic response to foreign enzymes in cancer therapy. Expert Rev. Clin. Immunol. 1, 549-559.
6. Gamez, A., Sarkissian, C. N., Wang, L., Kim, W., Straub, M., Patch, M. G., Chen, L., Striepeke, S., Fitzpatrick, P., Lemontt, J. F., O'Neill, C., Scriver, C. R., and Stevens, R. C. (2005) Development of pegylated forms of recombinant Rhodosporidium toruloides phenylalanine ammonia-lyase for the treatment of classical phenylketonuria. Mol. Ther. 11, 986-989.
7. Graham, M. L. (2003) Pegaspargase: a review of clinical studies. Adv. Drug Delivery Rev. 55, 1293-1302.
8. Harris, J. M., and Chess, R. B. (2003) Effect of pegylation on pharmaceuticals. Nat. Rev. Drug Discovery 2, 214-221.
9. Hershfield, M. S., Chaffee, S., Koro-Johnson, L., Mary, A., Smith, A. A., and Short, S. A. (1991) Use of site-directed mutagenesis to enhance the epitope-shielding effect of covalent modification of proteins with polyethylene glycol. Proc. Natl. Acad. Sci. U.S.A. 88, 7185-7189.
10. Davis, F. F. (2003) PEG-adenosine deaminase and PEG-asparaginase. Adv. Exp. Med. Biol. 519, 51-58.
11. Muller, H. J., and Boos, J. (1998) Use of L-asparaginase in childhood ALL. Crit. Rev. Oncol. Hematol. 28, 97-113.
12. Jackson, M. J., Beaudet, A. L., and O'Brien, W. E. (1986) Mammalian urea cycle enzymes. Annu. Rev. Genet. 20, 431-464.
13. Rodriguez, P. C., Zea, A. H., Culotta, K. S., Zabaleta, J., Ochoa, J. B., and Ochoa, A. C. (2002) Regulation of T cell receptor CD3ζ chain expression by L-arginine. J. Biol. Chem. 277, 21123-21129.
14. Morris, S. M., Jr. (2006) Arginine: beyond protein. Am. J. Clin. Nutr. 83, 508S-512S.
15. Sugimura, K., Ohno, T., Kusuyama, T., and Azuma, I. (1992) High sensitivity of human melanoma cell lines to the growth inhibitory activity of mycoplasmal arginine deiminase in vitro. Melanoma Res. 2, 191-196.
16. Shen, L. J., Beloussow, K., and Shen, W. C. (2006) Modulation of arginine metabolic pathways as the potential anti-tumor mechanism of recombinant arginine deiminase. Cancer Lett. 231, 30-35.
17. Sarkar, S., Arunakumari, A., Wang, M., Filpula, D., and Shorr, R. G. L. (1996) Growth inhibition of melanoma cell lines by an arginine depleting enzyme and its reversal by argininosuccinate synthetase gene overexpression. Proc. Amer. Assoc. Cancer Res. 37, 418-419.
18. Wheatley, D. N., Kilfeather, R., Stitt, A., and Campbell, E. (2005) Integrity and stability of the citrulline-arginine pathway in normal and tumour cell lines. Cancer Lett. 227, 141-152.
19. Shen, L. J., Lin, W. C., Beloussow, K., and Shen, W. C. (2003) Resistance to the anti-proliferative activity of recombinant arginine deiminase in cell culture correlates with the endogenous enzyme, argininosuccinate synthetase. Cancer Lett. 191, 165-170.
20. Dillon, B. J., Prieto, V. G., Curley, S. A., Ensor, C. M., Holtsberg, F. W., Bomalaski, J. S., and Clark, M. A. (2004) Incidence and distribution of argininosuccinate synthetase deficiency in human cancers: a method for identifying cancers sensitive to arginine deprivation. Cancer 100, 826-833.
21. Misawa, S., Aoshima, M., Takaku, H., Matsumoto, M., and Hayashi, H. (1994) High-level expression of Mycoplasma arginine deiminase in Escherichia coli and its efficient renaturation as an anti-tumor enzyme. J. Biotechnol. 36, 145-155.
22. Lu, X., Galkin, A., Herzberg, O., and Dunaway-Mariano, D. (2004) Arginine deiminase uses an active-site cysteine in nucleophilic catalysis of L-arginine hydrolysis. J. Am. Chem. Soc. 126, 5374-5375.
23. Das, K., Butler, G. H., Kwiatkowski, V., Clark, A. D., Jr., Yadav, P., and Arnold, E. (2004) Crystal structures of arginine deiminase with covalent reaction intermediates: implications for catalytic mechanism. Structure 12, 657-667.
24. Galkin, A., Lu, X., Dunaway-Mariano, D., and Herzberg, O. (2005) Crystal structures representing the Michaelis complex and the thiouronium reaction intermediate of Pseudomonas aeruginosa arginine deiminase. J. Biol. Chem. 280, 34080-34087.
25. Lu, X., Li, L., Wu, R., Feng, X., Li, Z., Yang, H., Wang, C., Guo, H., Galkin, A., Herzberg, O., Mariano, P. S., Martin, B. M., and Dunaway-Mariano, D. (2006) Kinetic analysis of Pseudomonas aeruginosa arginine deiminase mutants and alternate substrates provides insight into structural determinants of function. Biochemistry 45, 1162-1172.
26. Baur, H., Luethi, E., Stalon, V., Mercenier, A., and Haas, D. (1989) Sequence analysis and expression of the arginine-deiminase and carbamate-kinase genes of Pseudomonas aeruginosa. Eur. J. Biochem. 179, 53-60.
27. Holtsberg, F. W., Ensor, C. M., Steiner, M. R., Bomalaski, J. S., and Clark, M. A. (2002) Poly(ethylene glycol) (PEG) conjugated arginine deiminase: effects of PEG formulations on its pharmacological properties. J. Controlled Release 80, 259-271.
28. Miyazaki, K., Takaku, H., Umeda, M., Fujita, T., Huang, W. D., Kimura, T., Yamashita, J., and Horio, T. (1990) Potent growth inhibition of human tumor cells in culture by arginine deiminase purified from a culture medium of a Mycoplasma-infected cell line. Cancer Res. 50, 4522-4527.
29. Takaku, H., Takase, M., Abe, S., Hayashi, H., and Miyazaki, K. (1992) In vivo anti-tumor activity of arginine deiminase purified from Mycoplasma arginini. Int. J. Cancer 51, 244-249.
30. Takaku, H., Misawa, S., Hayashi, H., and Miyazaki, K. (1993) Chemical modification by polyethylene glycol of the anti-tumor enzyme arginine deiminase from Mycoplasma arginini. Jpn. J. Cancer Res. 84, 1195-1200.
31. 20,000mw) inhibits human melanomas and hepatocellular carcinomas in vitro and in vivo. Cancer Res. 62, 5443-5450.
32. Beloussow, K., Wang, L., Wu, J., Ann, D., and Shen, W. C. (2002) Recombinant arginine deiminase as a potential anti-angiogenic agent. Cancer Lett. 183, 155-162.
33. Takaku, H., Matsumoto, M., Misawa, S., and Miyazaki, K. (1995) Anti-tumor activity of arginine deiminase from Mycoplasma arginini and its growth-inhibitory mechanism. Jpn. J. Cancer Res. 86, 840-846.
34. Cheng, P. N., Leung, Y. C., Lo, W. H., Tsui, S. M., and Lam, K. C. (2005) Remission of hepatocellular carcinoma with arginine depletion induced by systemic release of endogenous hepatic arginase due to transhepatic arterial embolisation, augmented by high-dose insulin: arginase as a potential drug candidate for hepatocellular carcinoma. Cancer Lett. 224, 67-80.
35. Kubo, M., Nishitsuji, H., Kurihara, K., Hayashi, T., Masuda, T., and Kannagi, M. (2006) Suppression of human immunodeficiency virus type 1 replication by arginine deiminase of Mycoplasma arginini. J. Gen. Virol. 87, 1589-1593.
36. Park, I.-S., Kang, S.-W., Shin, Y.-J., Chae, K.-Y., Park, M.-O., Kim, M.-Y., Wheatley, D. N., and Min, B.-H. (2003) Arginine deiminase: a potent inhibitor of angiogenesis and tumour growth. Br. J. Cancer 89, 907-914.
37. Thomas, J. B., Holtsberg, F. W., Ensor, C. W., Bomalaski, J. S., and Clark, M. A. (2002) Enzymic degradation of plasma arginine using arginine deiminase inhibits nitric oxide production and protects mice from the lethal effects of tumour necrosis factor α and endotoxin. Biochem. J. 363, 581-587.
38. Curley, S. A., Bomalaski, J. S., Ensor, C. M., Holtsberg, F. W., and Clark, M. A. (2003) Regression of hepatocellular cancer in a patient treated with arginine deiminase. Hepato-Gastroenterology 50, 1208-1211.
39. Izzo, F., Marra, P., Beneduce, G., Castello, G., Vallone, P., De Rosa, V., Cremona, F., Ensor, C. M., Holtsberg, F. W., Bomalaski, J. S., Clark, M. A., Ng, C., and Curley, S. A. (2004) Pegylated arginine deiminase treatment of patients with unresectable hepatocellular carcinoma: results from Phase I/II studies. J. Clin. Oncol. 22, 1815-1822.
40. Zalipsky, S. (1995) Functionalized poly(ethylene glycol) for preparation of biologically relevant conjugates. Bioconjugate Chem. 6, 150-165.
41. Basu, A., Yang, K., Wang, M., Liu, S., Chintala, R., Palm, T., Zhao, H., Peng, P., Wu, D., Zhang, Z., Hua, J., Hsieh, M.-C., Zhou, J., Petti, G., Li, X., Janjua, A., Mendez, M., Liu, J., Longley, C., Zhang, Z., Mehlig, M., Borowski, V., Viswanathan, M., and Filpula, D. (2006) Structure-function engineering of interferon-β-1b for improving stability, solubility, potency, immunogenicity, and pharmacokinetic properties by site-selective mono-PEGylation. Bioconjugate Chem. 17, 618-630.
42. Zhao, H., Yang, K., Martinez, A., Basu, A., Chintala, R., Liu, H.-C., Janjua, A., Wang, M., and Filpula, D. (2006) Linear and branched bicin linkers for releasable PEGylation of macromolecules: controlled release in vivo and in vitro from mono- and multi-PEGylated proteins. Bioconjugate Chem. 17, 341-351.
43. Yang, K., Basu, A., Wang, M., Chintala, R., Hsieh, M.-C., Liu, S., Hua, J., Zhang, Z., Zhou, J., Li, M., Phyu, H., Petti, G., Mendez, M., Janjua, H., Peng, P., Longley, C., Borowski, V., Mehlig, M., and Filpula, D. (2003) Tailoring structure-function and pharmacokinetic properties of single-chain Fv proteins by site-specific PEGylation. Protein Eng. 16, 761-770.
44. Greenwald, R. B. (2001) PEG drugs: an overview. J. Controlled Release 74, 159-171.
45. Greenwald, R. B., Yang, K., Zhao, H., Conover, C. D., Lee, S., and Filpula, D. (2003) Controlled release of proteins from their poly-(ethylene glycol) conjugates: drug delivery systems employing 1,6-elimination. Bioconjugate Chem. 14, 395-403.
46. Roberts, M. J., Bentley, M. D., and Harris, J. M. (2002) Chemistry for peptide and protein PEGylation. Adv. Drug Delivery Rev. 54, 459-476.
47. Wang, M., Lee, L. S., Nepomich, A., Yang, J.-D., Conover, C., Whitlow, M., and Filpula, D. (1998) Single-chain Fv with manifold N-glycans as bifunctional scaffolds for immunomolecules. Protein Eng. 11, 1277-1283.
48. Weickmann, J. L., and Fahrney, D. E. (1977) Arginine deiminase from Mycoplasma arthritidis: evidence for multiple forms. J. Biol. Chem. 252, 2615-2620.
49. Weickmann, J. L., Himmel, M. E., Squire, P. G., and Fahrney, D. E. (1978) Arginine deiminase from Mycoplasma arthritidis: properties of the enzyme from log phase cultures. J. Biol. Chem. 253, 6010-6015.
50. Smith, D. W., Ganaway, R. L., and Fahrney, D. E. (1978) Arginine deiminase from Mycoplasma arthritidis: structure-activity relationships among substrates and competitive inhibitors. J. Biol. Chem. 253, 6016-6020.
51. Miron, T., and Wilchek, M. (1993) A simplified method for the preparation of succinimidyl carbonate polyethylene glycol for coupling to proteins. Bioconjugate Chem. 4, 568-569.
52. Shibatani, T., Kakimoto, T., and Chibata, I. (1975) Crystallization and properties of L-arginine deiminase of Pseudomonas putida. J. Biol. Chem. 250, 4580-4583.
53. Oginsky, E. (1957) Isolation and determination of arginine and citrulline. Methods Enzymol. 3, 639-643.
54. Bagrel, A., Museur, G., and Siest, G. (1975) Colorimetric measurement of ornithine carbamoyl transferase activity in plasma, and results for a supposedly healthy population. Clin. Chem. 21, 1716-1720.
55. Smith, P. K., Krohn, R. I., Hermanson, G. T., Mallia, A. K., Gartner, F. H., Provenzano, M. D., Fujimoto, E. K., Goeke, N. M., Olson, B. J., and Klenk, D. C. (1985) Measurement of protein using bicinchoninic acid. Anal. Biochem. 150, 76-85.
56. Habeeb, A. F. (1966) Determination of free amino groups in proteins by trinitrobenzenesulfonic acid. Anal. Biochem. 14, 328-336.
57. Stocks, S. J., Jones, A. J., Ramey, C. W., and Brooks, D. E. (1986) A fluorometric assay of the degree of modification of protein primary amines with polyethylene glycol. Anal. Biochem. 154, 232-234.
58. Savoca, K. V., Abuchowski, A., van Es, T., Davis, F. F., and Palczuk, N. C. (1979) Preparation of a non-immunogenic arginase by the covalent attachment of polyethylene glycol. Biochim. Biophys. Acta 578, 47-53.
59. Chaffee, S., Mary, A., Stiehm, E. R., Girault, D., Fischer, A., and Hershfield, M. S. (1992) IgG antibody response to polyethylene glycol-modified adenosine deaminase in patients with adenosine deaminase deficiency. J. Clin. Invest. 89, 1643-1651.