Methionine addiction of cancer cells targeted by methioninase
- Authors: Pokrovsky V.S1,2,3, Abo qoura L.1,2, Demidova E.A1, Han Q.4, Hoffman R.M4,5
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Affiliations:
- N. N. Blokhin National Medical Research Center of Oncology of Ministry of Health of Russian Federation
- Research Institute of Molecular and Cellular Medicine, People’s Friendship University of Russia (RUDN University)
- Sirius University of Science and Technology
- AntiCancer Inc
- University of California
- Issue: Vol 88, No 7 (2023)
- Pages: 1162-1172
- Section: Articles
- URL: https://journals.rcsi.science/0320-9725/article/view/141462
- DOI: https://doi.org/10.31857/S0320972523070072
- EDN: https://elibrary.ru/FXHDNJ
- ID: 141462
Cite item
Abstract
About the authors
V. S Pokrovsky
N. N. Blokhin National Medical Research Center of Oncology of Ministry of Health of Russian Federation;Research Institute of Molecular and Cellular Medicine, People’s Friendship University of Russia (RUDN University);Sirius University of Science and Technology
Email: v.pokrovsky@ronc.ru
115478 Moscow, Russia;117198 Moscow, Russia;354340 Sochi, Russia
L. Abo qoura
N. N. Blokhin National Medical Research Center of Oncology of Ministry of Health of Russian Federation;Research Institute of Molecular and Cellular Medicine, People’s Friendship University of Russia (RUDN University)
Email: louay.ko@gmail.com
115478 Moscow, Russia;117198 Moscow, Russia
E. A Demidova
N. N. Blokhin National Medical Research Center of Oncology of Ministry of Health of Russian Federation115478 Moscow, Russia
Q. Han
AntiCancer IncSan Diego, CA 92111, USA
R. M Hoffman
AntiCancer Inc;University of California
Email: all@anticancer.com
San Diego, CA 92111, USA;San Diego, La Jolla, CA 92037-7400, USA
References
- Sugimura, T., Birnbaum, S. M., Winitz, M., and Greenstein, J. P. (1959) Quantitative nutritional studies with water-soluble, chemically defined diets. VIII. The forced feeding of diets each lacking in one essential amino acid, Arch. Biochem. Biophys., 81, 448-455, doi: 10.1016/0003-9861(59)90225-5.
- Hoffman, R. M., and Erbe, R. W. (1976) High in vivo rates of methionine biosynthesis in transformed human and malignant rat cells auxotrophic for methionine, Proc. Natl. Acad. Sci. USA, 73, 1523-1527, doi: 10.1073/pnas.73.5.1523.
- Kaiser, P. (2020) Methionine dependence of cancer, Biomolecules, 10, 568, doi: 10.3390/biom10040568.
- Coalson, D. W., Mecham, J. O., Stern, P. H., and Hoffman, R. M. (1982) Reduced availability of endogenously synthesized methionine for S-adenosylmethionine formation in methionine-dependent cancer cells, Proc. Natl. Acad. Sci. USA, 79, 4248-4251, doi: 10.1073/pnas.79.14.4248.
- Stern, P. H., and Hoffman, R. M. (1984) Elevated overall rates of transmethylation in cell lines from diverse human tumors, In Vitro, 20, 663-670, doi: 10.1007/BF02619617.
- Stern, P. H., Mecham, J. O., Wallace, C. D., and Hoffman, R. M. (1983) Reduced free-methionine in methionine-dependent SV40-transformed human fibroblasts synthesizing apparently normal amounts of methionine, J. Cell. Physiol., 117, 9-14, doi: 10.1002/jcp.1041170103.
- Singhal, T., Narayanan, T. K., Jacobs, M. P., Bal, C., and Mantil, J. C. (2012) 11C-methionine PET for grading and prognostication in gliomas: a comparison study with 18F-FDG PET and contrast enhancement on MRI, J. Nucl. Med., 53, 1709-1715, doi: 10.2967/jnumed.111.102533.
- Tisdale, M. J. (1980) Effect of methionine deprivation on methylation and synthesis of macromolecules, Br. J. Cancer, 42, 121-128, doi: 10.1038/bjc.1980.210.
- Hoffman, R. M. (1984) Altered methionine metabolism, DNA methylation and oncogene expression in carcinogenesis, Biochim. Biophys. Acta BBA Rev. Cancer, 738, 49-87, doi: 10.1016/0304-419X(84)90019-2.
- Hoffman, R. M., Coalson, D. W., Jacobsen, S. J., and Erbe, R. W. (1981) Folate polyglutamate and monoglutamate accumulation in normal and SV40-transformed human fibroblasts, J. Cell. Physiol., 109, 497-505, doi: 10.1002/jcp.1041090316.
- Epner, D. E., Morrow, S., Wilcox, M., and Houghton, J. L. (2002) Nutrient intake and nutritional indexes in adults with metastatic cancer on a phase I clinical trial of dietary methionine restriction, Nutr. Cancer, 42, 158-166, doi: 10.1207/S15327914NC422_2.
- Hoshiya, Y., Guo, H., Kubota, T., Inada, T., Asanuma, F., Yamada, Y., Koh, J., Kitajima, M., Hoffman, R. M. (1995) Human tumors are methionine dependent in vivo, Anticancer Res., 15, 717-718.
- Tan, Y., Xu, M., Tan, X., Tan, X., Wang, X., Saikawa, Y., Nagahama, T., Sun, X., Lenz, M., and Hoffman, R. M. (1997) Overexpression and large-scale production of recombinant L-methionine-α-deamino-γ-mercaptomethane-lyase for novel anticancer therapy, Protein Expr. Purif., 9, 233-245, doi: 10.1006/prep.1996.0700.
- Stern, P. H., and Hoffman, R. M. (1986) Enhanced in vitro selective toxicity of chemotherapeutic agents for human cancer cells based on a metabolic defect, J. Natl. Cancer Inst., 76, 629-639, doi: 10.1093/jnci/76.4.629.
- Kubota, Y., Han, Q., Hamada, K., Aoki, Y., Masaki, N., Obara, K., Tsunoda, T., and Hoffman, R. M. (2022) Long-term stable disease in a rectal-cancer patient treated by methionine restriction with oral recombinant methioninase and a low-methionine diet, Anticancer Res., 42, 3857-3861, doi: 10.21873/anticanres.15877.
- Kubota, Y., Han, Q., Hozumi, C., Masaki, N., Yamamoto, J., Aoki, Y., Tsunoda, T., and Hoffman, R. M. (2022) Stage IV pancreatic cancer patient treated with FOLFIRINOX combined with oral methioninase: a highly-rare case with long-term stable disease, Anticancer Res., 42, 2567-2572, doi: 10.21873/anticanres.15734.
- Kubota, Y., Han, Q., Masaki, N., Hozumi, C., Hamada, K., Aoki, Y., Obara, K., Tsunoda, T., and Hoffman, R. M. (2022) Elimination of axillary-lymph-node metastases in a patient with invasive lobular breast cancer treated by first-line neo-adjuvant chemotherapy combined with methionine restriction, Anticancer Res., 42, 5819-5823, doi: 10.21873/anticanres.16089.
- Han, Q., and Hoffman, R. M. (2021) Chronic treatment of an advanced prostate-cancer patient with oral methioninase resulted in long-term stabilization of rapidly rising PSA levels, In Vivo, 35, 2171-2176, doi: 10.21873/invivo.12488.
- Han, Q., and Hoffman, R. M. (2021) Lowering and stabilizing PSA levels in advanced-prostate cancer patients with oral methioninase, Anticancer Res., 41, 1921-1926, doi: 10.21873/anticanres.14958.
- Han, Q., Tan, Y., and Hoffman, R. M. (2020) Oral dosing of recombinant methioninase is associated with a 70% drop in PSA in a patient with bone-metastatic prostate cancer and 50% reduction in circulating methionine in a high-stage ovarian cancer patient, Anticancer Res., 40, 2813-2819, doi: 10.21873/anticanres.14254.
- Cantoni, G. L. (1975) Biological methylation: selected aspects, Annu. Rev. Biochem., 44, 435-451, doi: 10.1146/annurev.bi.44.070175.002251.
- Hoffman, R. M. (2015) Development of recombinant methioninase to target the general cancer-specific metabolic defect of methionine dependence: a 40-year odyssey, Expert Opin. Biol. Ther., 15, 21-31, doi: 10.1517/14712598.2015.963050.
- Pokrovsky, V. S., Abo Qoura, L., Morozova, E., and Bunik, V. I. (2022) Predictive markers for efficiency of the amino-acid deprivation therapies in cancer, Front. Med., 9, 1035356, doi: 10.3389/fmed.2022.1035356.
- Mecham, J. O., Rowitch, D., Wallace, C. D., Stern, P. H., and Hoffman, R. M. (1983) The metabolic defect of methionine dependence occurs frequently in human tumor cell lines, Biochem. Biophys. Res. Commun., 117, 429-434, doi: 10.1016/0006-291X(83)91218-4.
- Tan, Y., Xu, M., and Hoffman, R. M. (2010) Broad selective efficacy of recombinant methioninase and polyethylene glycol-modified recombinant methioninase on cancer cells in vitro, Anticancer Res., 30, 1041-1046.
- Yamamoto, J., Han, Q., Inubushi, S., Sugisawa, N., Hamada, K., Nishino, H., Miyake, K., Kumamoto, T., Matsuyama, R., Bouvet, M., Endo, I., and Hoffman, R. M. (2020) Histone methylation status of H3K4me3 and H3K9me3 under methionine restriction is unstable in methionine-addicted cancer cells, but stable in normal cells, Biochem. Biophys. Res. Commun., 533, 1034-1038, doi: 10.1016/j.bbrc.2020.09.108.
- Yamamoto, J., Inubushi, S., Han, Q., Tashiro, Y., Sugisawa, N., Hamada, K., Aoki, Y., Miyake, K., Matsuyama, R., Bouvet, M., Clarke, S. G., Endo, I., and Hoffman, R. M. (2020) The linkage of methionine addiction, overmethylation of histone H3 lysines and malignancy demonstrated when cancer cells revert to methionine-independence, bioRxiv, doi: 10.1101/2020.12.04.412437.
- Wang, Z., Yip, L. Y., Lee, J. H. J., Wu, Z., Chew, H. Y., Chong, P. K. W., Teo, C. C., Ang, H. Y., Peh, K. L. E., Yuan, J., Ma, S., Choo, L. S. K., Basri, N., Jiang, X., Yu, Q., Hillmer, A. M., Lim, W. T., Lim, T. K. H., Takano, A., Tan, E. H., Tan, D. S. W., Ho, Y. S., Lim, B., and Tam, W. L. (2019) Methionine is a metabolic dependency of tumor-initiating cells, Nat. Med., 25, 825-837, doi: 10.1038/s41591-019-0423-5.
- Kubota, Y., Sato, T., Hozumi, C., Han, Q., Aoki, Y., Masaki, N., Obara, K., Tsunoda, T., and Hoffman, R. M. (2023) Superiority of [11C] methionine over [18F] deoxyglucose for PET imaging of multiple cancer types due to the methionine addiction of cancer, Int. J. Mol. Sci., 24, 1935, doi: 10.3390/ijms24031935.
- Bloomfield, M., and Duesberg, P. (2016) Inherent variability of cancer-specific aneuploidy generates metastases, Mol. Cytogenet., 9, 90, doi: 10.1186/s13039-016-0297-x.
- Hoffman, R. M., and Jacobsen, S. J. (1980) Reversible growth arrest in simian virus 40-transformed human fibroblasts, Proc. Natl. Acad. Sci. USA, 77, 7306-7310, doi: 10.1073/pnas.77.12.7306.
- Yamamoto, J., Han, Q., Simon, M., Thomas, D., and Hoffman, R. M. (2022) Methionine restriction: ready for prime time in the cancer clinic? Anticancer Res., 42, 641-644, doi: 10.21873/anticanres.15521.
- Tanaka, H., Esaki, N., and Soda, K. (1985) A versatile bacterial enzyme: l-methionine γ-lyase, Enzyme Microb. Technol., 7, 530-537, doi: 10.1016/0141-0229(85)90094-8.
- Tan, Y., Zavala, J., Han, Q., Xu, M., Sun, X., Tan, X., Tan, X., Magana, R., Geller, J., and Hoffman, R. M. (1997) Recombinant methioninase infusion reduces the biochemical endpoint of serum methionine with minimal toxicity in high-stage cancer patients, Anticancer Res., 17, 3857-3860.
- Hoffman, R. M. (2017) Is DNA methylation the new guardian of the genome? Mol. Cytogenet., 10, 11, doi: 10.1186/s13039-017-0314-8.
- Kreis, W., and Hession, C. (1973) Biological effects of enzymatic deprivation of L-methionine in cell culture and an experimental tumor, Cancer Res., 33, 1866-1869.
- Higuchi, T., Kawaguchi, K., Miyake, K., Han, Q., Tan, Y., Oshiro, H., Sugisawa, N., Zhang, Z., Razmjooei, S., Yamamoto, N., Hayashi, R., Kimura, H., Miwa, S., Igarashi, K., Chawla, S. P., Singh, A. S., Eilber, F. C., Singh, S. R., Tsuchiya, H., and Hoffman, R. M. (2018) Oral recombinant methioninase combined with caffeine and doxorubicin induced regression of a doxorubicin-resistant synovial sarcoma in a PDOX mouse model, Anticancer Res., 38, 5639-5644, doi: 10.21873/anticanres.12899.
- Higuchi, T., Oshiro, H., Miyake, K., Sugisawa, N., Han, Q., Tan, Y., Park, J., Zhang, Z., Razmjooei, S., Yamamoto, N., Hayashi, K., Kimura, H., Miwa, S., Igarashi, K., Bouvet, M., Chawla, S. P., Singh, S. R., Tsuchiya, H., and Hoffman, R. M. (2019) Oral recombinant methioninase, combined with oral caffeine and injected cisplatinum, overcome cisplatinum-resistance and regresses patient-derived orthotopic xenograft model of osteosarcoma, Anticancer Res., 39, 4653-4657, doi: 10.21873/anticanres.13646.
- Higuchi, T., Sugisawa, N., Yamamoto, J., Oshiro, H., Han, Q., Yamamoto, N., Hayashi, K., Kimura, H., Miwa, S., Igarashi, K., Tan, Y., Kuchipudi, S., Bouvet, M., Singh, S. R., Tsuchiya, H., and Hoffman, R. M. (2020) The combination of oral-recombinant methioninase and azacitidine arrests a chemotherapy-resistant osteosarcoma patient-derived orthotopic xenograft mouse model, Cancer Chemother. Pharmacol., 85, 285-291, doi: 10.1007/s00280-019-03986-0.
- Kawaguchi, K., Han, Q., Li, S., Tan, Y., Igarashi, K., Kiyuna, T., Miyake, T., Miyake, M., Chmielowski, B., Nelson, S. D., Russell, T. A., Dry, S. A., Li, Y., Singh, A. S., Eckardt, M. A. R., Unno, M., Eilber, F. C., and Hoffman, R. M.(2018) Targeting methionine with oral recombinant methioninase (o-rMETase) arrests a patient-derived orthotopic xenograft (PDOX) model of BRAF-V600E mutant melanoma: implications for chronic clinical cancer therapy and prevention, Cell Cycle, 17, 356-361, doi: 10.1080/15384101.2017.1405195.
- Kawaguchi, K., Han, Q., Li, S., Tan, Y., Igarashi, K., Murakami, T., Unno, M., and Hoffman, R. M. (2019) Efficacy of recombinant methioninase (rMETase) on recalcitrant cancer patient-derived orthotopic xenograft (PDOX) mouse models: a review, Cells, 8, 410, doi: 10.3390/cells8050410.
- Kawaguchi, K., Higuchi, T., Li, S., Han, Q., Tan, Y., Igarashi, K., Zhao, M., Miyake, K., Kiyuna, T., Miyake, M., Ohshiro, H., Sugisawa, N., Zhang, Z., Razmjooei, S., Wangsiricharoen, S., Chmielowski, B., Nelson, S. D., Russell, T. A., Dry, S. M., Li, Y., and Hoffman, R. M. (2018) Combination therapy of tumor-targeting Salmonella typhimurium A1-R and oral recombinant methioninase regresses a BRAF-V600E-negative melanoma, Biochem. Biophys. Res. Commun., 503, 3086-3092, doi: 10.1016/j.bbrc.2018.08.097.
- Kawaguchi, K., Miyake, K., Han, Q., Li, S., Tan, S., Igarashi, K., Kiyuna, K., Miyake, M., Higuchi, T., Oshiro, H., Zhang, Z., Razmjooei, S., Wangsiricharoen, S., Bouvet, M., Singh, S. R., Unno, M., and Hoffman, R. M. (2018) Oral recombinant methioninase (o-rMETase) is superior to injectable rMETase and overcomes acquired gemcitabine resistance in pancreatic cancer, Cancer Lett., 432, 251-259, doi: 10.1016/j.canlet.2018.06.016.
- Yoshioka, T., Wada, T., Uchida, N., Maki, H., Yoshida, H., Ide, N., Kasai, H., Hojo, K., Shono, K., Maekawa, R., Yagi, S., Hoffman, R. M., and Sugita, K. (1998) Anticancer efficacy in vivo and in vitro, synergy with 5-fluorouracil, and safety of recombinant methioninase, Cancer Res., 58, 2583-2587.
- Oshiro, H., Tome, Y., Kiyuna, T., Yoon, S. N., Lwin, T. M., Han, Q., Tan, Y., Miyake, K., Higuchi, T., Sugisawa, N., Katsuya, Y., Park, J. H., Zang, Z., Razmjooei, S., Bouvet, M., Clary, B., Singh, S. R., Kanaya, F., Nishida, F., and Hoffman, R. M. (2019) Oral recombinant methioninase overcomes colorectal-cancer liver metastasis resistance to the combination of 5-fluorouracil and oxaliplatinum in a patient-derived orthotopic xenograft mouse model, Anticancer Res., 39, 4667-4671, doi: 10.21873/anticanres.13648.
- Morozova, E. A., Kulikova, V. V., Yashin, D. V., Anufrieva, N. V., Anisimova, N. Y., Revtovich, S. V., Kotlov, M. I., Belyi, Y. F., Pokrovsky, V. S., and Demidkina, T. V. (2013) Kinetic Parameters and Cytotoxic Activity of Recombinant Methionine γ-Lyase from Clostridium tetani, Clostridium sporogenes, Porphyromonas gingivalis and Citrobacter freundii, Acta Naturae, 5, 92-98, doi: 10.32607/20758251-2013-5-3-92-98.
- Morozova, E. A., Anufrieva, N. V., Davydov, D. Zh., Komarova, M. V., Dyakov, I. N., Rodionov, A. N., Demidkina, T. V., and Pokrovsky, V. S. (2017) Plasma methionine depletion and pharmacokinetic properties in mice of methionine γ-lyase from Citrobacter freundii, Clostridium tetani and Clostridium sporogenes, Biomed. Pharmacother, 88, 978-984, doi: 10.1016/j.biopha.2017.01.127.
- Pokrovsky, V. S., Anisimova, N. Y., Davydov, D. Zh., Bazhenov, S. V., Bulushova, N. V., Zavilgelsky, G. B., Kotova, V. Y., and Manukhov, I. V. (2019) Methionine gamma lyase from Clostridium sporogenes increases the anticancer effect of doxorubicin in A549 cells and human cancer xenografts, Invest. New Drugs, 37, 201-209, doi: 10.1007/s10637-018-0619-4.
- Pokrovsky, V. S., Chepikova, O. E., Davydov, D. Zh., Zamyatnin, A. A., Lukashev, A. N., and Lukasheva, E. V. (2019) Amino acid degrading enzymes and their application in cancer therapy, Curr. Med. Chem., 26, 446-464, doi: 10.2174/0929867324666171006132729.
- Yang, Z., Wang, J., Yoshioka, T., Li, B., Lu, Q., Li, S., Sun, X., Tan, Y., Yagi, S., Frenkel, E. P., and Hoffman, R. M. (2004) Pharmacokinetics, methionine depletion, and antigenicity of recombinant methioninase in primates, Clin. Cancer Res., 10, 2131-2138, doi: 10.1158/1078-0432.CCR-03-0068.
- Tan, Y., Zavala, J., Xu, M., Zavala, J., and Hoffman, R. M. (1996) Serum methionine depletion without side effects by methioninase in metastatic breast cancer patients, Anticancer Res., 16, 3937-3942.