GST-Theta1 Enzyme Expression Levels in Brain Tumor and Their Relationship with the Clinical Data of the Patients
Yıl 2021,
Cilt: 5 Sayı: 2, 82 - 98, 01.12.2021
Onur Dirican
,
Pınar Kaygın
Sezen Yılmaz Sarıaltın
,
Can Yılmaz
,
Volkan Ateş
,
Gülçin Güler Şimşek
,
Serpil Oğuztüzün
,
Tülay Çoban
Yusuf İzci
Öz
The most important drug metabolizing enzyme of the detoxification mechanism is known as Glutathione S-Transferase. GST enzymes may be associated with brain tumor epidemiology, clinical and demographic factors. The correlation between parameters such as changes in Glutathione S-transferase Theta1 proteins, tumor localizations, age, gender, alcohol use, smoking, chemotherapeutic/radiotherapeutic treatment status in normal and brain tumor tissues, diagnosed in neurosurgery department, were examined by immunohistochemistry. GST-Theta1 expressions were analyzed using immunostaining in samples from 149 patients diagnosed with brain tumors between 2016 and 2018. The mean age of the patient group was 49.44 years. 83 (58.45%) patients were male. After immunohistochemical staining, GST-T1 expression was found approximately 9,46 times higher in tumor tissues than in normal tissues (p<0.0001). Tumor tissues from patients who received chemotheraphy showed higher expression of GST-T1 than those who did not (p<0,05). In addition, GST-T1 expression level was observed at a significantly higher level in patients younger than 60 years of age compared to patients over 60 years (p<0.026; p<0.05). There was no statistically significant relationship between patients smoking behaviors, alcohol consumption, tumor localization and GST-T1 expressions. It is aimed to determine the GST-T1 protein expressions and to contribute to the examination of epidemiological and prognostic factors of brain tumors by comparing them with demographic and clinical data.
Destekleyen Kurum
Kırıkkale University Scientific Research and Projects Department
Teşekkür
Studies was carried out in the Kırıkkale University, Department of Biology, Tissue Research Laboratory. I thanks to all author. Also we thanks to University of Health Sciences, Gulhane Training and Research Hospital, Department of Pathology and Department of Neurosurgery and Ankara University, Faculty of Pharmacy, Department of Pharmaceutical Toxicology.
Kaynakça
- Adwas, A.A., Elsayed, A.S.I., Azab, A.E.(2019). Oxidative stress and antioxidant mechanisms in human body. J Appl Biotechnol Bioeng. 2019;6(1):43-47. https://doi.org/10.15406/jabb.2019.06.00173
- Askari, H., Rajani, S. F., Poorebrahim, M., Haghi-Aminjan, H., Raeis-Abdollahi, E., & Abdollahi, M. (2018). A glance at the therapeutic potential of irisin against diseases involving inflammation, oxidative stress, and apoptosis: An introductory review. Pharmacological research, 129, 44–55. https://doi.org/10.1016/j.phrs.2018.01.012
- Backos, D. S., Franklin, C. C., & Reigan, P. (2012). The role of glutathione in brain tumor drug resistance. Biochemical pharmacology, 83(8), 1005-1012. https://doi.org/10.1016/j.bcp.2011.11.016
- Barnholtz-Sloan, J. S., Ostrom, Q. T., & Cote, D. (2018). Epidemiology of Brain Tumors. Neurologic clinics, 36(3), 395–419. https://doi.org/10.1016/j.ncl.2018.04.001.
- Calatozzolo, C., Gelati, M., Ciusani, E. (2005). Expression of Drug Resistance Proteins Pgp, MRP1, MRP3, MRP5 AND GST-π in Human Glioma. J Neurooncol 74, 113–121. https://doi.org/10.1007/s11060-004-6152-7
- Castello, L. M., Salmi, L., Zanotti, I., Gardino, C. A., Baldrighi, M., Settanni, F., & Avanzi, G. C. (2018). The increase in copeptin levels in mild head trauma does not predict the severity and the outcome of brain damage. Biomarkers in medicine, 12(6), 555–563. https://doi.org/10.2217/bmm-2018-0041.
- Cookson, M. S., Reuter, V. E., Linkov, I., & Fair, W. R. (1997). Glutathione S-transferase PI (GST-pi) class expression by immunohistochemistry in benign and malignant prostate tissue. The Journal of urology, 157(2), 673-676. https://doi.org/10.1016/S0022-5347(01)65248-0
- Courtens, A. M., Stevens, F. C., Crebolder, H. F., & Philipsen, H. (1996). Longitudinal study on quality of life and social support in cancer patients. Cancer nursing, 19(3), 162–169. https://doi.org/10.1097/00002820-199606000-00002.
- Darlix, A., Zouaoui, S., Rigau, V., Bessaoud, F., Figarella-Branger, D., Mathieu-Daudé, H., Trétarre, B., Bauchet, F., Duffau, H., Taillandier, L., & Bauchet, L. (2017). Epidemiology for primary brain tumors: a nationwide population-based study. Journal of neuro-oncology, 131(3), 525–546. https://doi.org/10.1007/s11060-016-2318-3.
- Ferlay, J., Colombet, M., Soerjomataram, I., Mathers, C., Parkin, D. M., Piñeros, M., Znaor, A., & Bray, F. (2019). Estimating the global cancer incidence and mortality in 2018: GLOBOCAN sources and methods. International journal of cancer, 144(8), 1941–1953. https://doi.org/10.1002/ijc.31937.
- Gulubova, M., & Vlaykova, T. (2010). Expression of the xenobiotic- and reactive oxygen species-detoxifying enzymes, GST-pi, Cu/Zn-SOD, and Mn-SOD in the endocrine cells of colorectal cancer. International journal of colorectal disease, 25(12), 1397–1405. https://doi.org/10.1007/s00384-010-1041-3
- Harrison, D. J., Kharbanda, R., Bishop, D., McLelland, L. I., & Hayes, J. D. (1989). Glutathione S-transferase isoenzymes in human renal carcinoma demonstrated by immunohistochemistry. Carcinogenesis, 10(7), 1257-1260. https://doi.org/10.1093/carcin/10.7.1257
- Hayat, B., Yavuz, M. S., Şahin, M. E., Dirican, O., Yılmaz, S., Yılmaz, C., Yıldırım, I., Çoban, T., Güler Şimşek, G. & Oğuztüzün, S. (2021). Kronik Obstrüktif Akciğer Hastalığında Glutatyon-S-Transferaz Mu1 ve Teta1 Polimorfizmlerinin Rolü. Journal of Faculty of Pharmacy of Ankara University, 45 (1), 41-56. https://doi.org/10.33483/jfpau.839530
- Hoshiya, T., Hasegawa, R., Hakoi, K., Cui, L., Ogiso, T., Cabral, R., & Ito, N. (1993). Enhancement by non-mutagenic pesticides of GST-P positive hepatic foci development initiated with diethylnitrosamine in the rat. Cancer letters, 72(1-2), 59-64. https://doi.org/10.1016/0304-3835(93)90011-W
- Huang, J., Tan, PH., Thiyagarajan, J.(2003). Prognostic Significance of Glutathione S-Transferase-Pi in Invasive Breast Cancer. Mod Pathol 16, 558–565. https://doi.org/10.1097/01.MP.0000071842.83169.5A
- Ji, C., Magnuson, J. T., Zhang, W., & Zhao, M. (2021). New insight into the enantioselective cytotoxicity of cypermethrin: imbalance between cell cycle and apoptosis. Journal of Hazardous Materials, 403, 123893. https://doi.org/10.1016/j.jhazmat.2020.123893.
- Jörg, S., Grohme, D. A., Erzler, M., Binsfeld, M., Haghikia, A., Müller, D. N., Linker, R. A., & Kleinewietfeld, M. (2016). Environmental factors in autoimmune diseases and their role in multiple sclerosis. Cellular and molecular life sciences : CMLS, 73(24), 4611–4622. https://doi.org/10.1007/s00018-016-2311-1.
- Kakehashi, A., Inoue, M., Wei, M., Fukushima, S., & Wanibuchi, H. (2009). Cytokeratin 8/18 overexpression and complex formation as an indicator of GST-P positive foci transformation into hepatocellular carcinomas. Toxicology and applied pharmacology, 238(1), 71-79. https://doi.org/10.1016/j.taap.2009.04.018
- Kumar, P. V., Ahamed, A. J., & Karthikeyan, M. (2019). Synthesis and characterization of NiO nanoparticles by chemical as well as green routes and their comparisons with respect to cytotoxic effect and toxicity studies in microbial and MCF-7 cancer cell models. SN Applied Sciences, 1(9), 1-15. https://doi.org/10.1007/s42452-019-1113-0
- Kural, C., Kaya Kocdogan, A., Şimşek, G. G., Oğuztüzün, S., Kaygın, P., Yılmaz, I., Bayram, T., & Izci, Y. (2019). Glutathione S-Transferases and Cytochrome P450 Enzyme Expression in Patients with Intracranial Tumors: Preliminary Report of 55 Patients. Medical principles and practice : international journal of the Kuwait University, Health Science Centre, 28(1), 56–62. https://doi.org/10.1159/000494496.
- Lark, A. L., Livasy, C. A., Calvo, B., Caskey, L., Moore, D. T., Yang, X., & Cance, W. G. (2003). Overexpression of focal adhesion kinase in primary colorectal carcinomas and colorectal liver metastases: immunohistochemistry and real-time PCR analyses. Clinical Cancer Research, 9(1), 215-222.
- Mathieu, A., Remmelink, M., D'Haene, N., Penant, S., Gaussin, J.-F., Van Ginckel, R., Darro, F., Kiss, R. and Salmon, I. (2004), Development of a chemoresistant orthotopic human nonsmall cell lung carcinoma model in nude mice. Cancer, 101: 1908-1918. https://doi.org/10.1002/cncr.20571
- Mendes, M., Sousa, J. J., Pais, A., & Vitorino, C. (2018). Targeted Theranostic Nanoparticles for Brain Tumor Treatment. Pharmaceutics, 10(4), 181. https://doi.org/10.3390/pharmaceutics10040181.
- Murray, G. I., & Burke, M. D. (1995). Immunohistochemistry of drug-metabolizing enzymes. Biochemical pharmacology, 50(7), 895-903. https://doi.org/10.1016/0006-2952(95)00136-N
- Nabetani, M., & Shintaku, H. (2018). New Strategy of Clinical Studies for Premature Babies with Ischemic Brain Damage. In Cell Therapy for Perinatal Brain Injury (pp. 17-24). Springer, Singapore.
- Nishimura, T., Newkirk, K., Sessions, R. B., Andrews, P. A., Trock, B. J., Rasmussen, A. A., Montgomery E. A., Bischoff E. K., Cullen, K. J. (1996). Immunohistochemical staining for glutathione S-transferase predicts response to platinum-based chemotherapy in head and neck cancer. Clinical cancer research, 2(11), 1859-1865.
- Nishimura, T., Newkirk, K., Sessions, R. B., Andrews, P. A., Trock, B. J., Rusmussen, A. A., Montgomery E. A., Bischoff E. K., Hanigan M. H., Cullen, K. J. (1998). Association between expression of glutathione-associated enzymes and response to platinum-based chemotherapy in head and neck cancer. Chemico-biological interactions, 111, 187-198.https://doi.org/10.1016/S0009-2797(97)00161-0
- Okidi, R., Ogwang, D. M., Okello, T. R., Ezati, D., Kyegombe, W., Nyeko, D., & Scolding, N. J. (2020). Factors affecting mortality after traumatic brain injury in a resource-poor setting. BJS open, 4(2), 320–325. https://doi.org/10.1002/bjs5.50243.
- Ostrom, Q. T., Adel Fahmideh, M., Cote, D. J., Muskens, I. S., Schraw, J. M., Scheurer, M. E., & Bondy, M. L. (2019). Risk factors for childhood and adult primary brain tumors. Neuro-oncology, 21(11), 1357–1375. https://doi.org/10.1093/neuonc/noz123.
- Ostrom, Q. T., Gittleman, H., Liao, P., Vecchione-Koval, T., Wolinsky, Y., Kruchko, C., & Barnholtz-Sloan, J. S. (2017). CBTRUS Statistical Report: Primary brain and other central nervous system tumors diagnosed in the United States in 2010-2014. Neuro-oncology, 19(suppl_5), v1–v88. https://doi.org/10.1093/neuonc/nox158.
- Park, J. H., de Lomana, A., Marzese, D. M., Juarez, T., Feroze, A., Hothi, P., Cobbs, C., Patel, A. P., Kesari, S., Huang, S., & Baliga, N. S. (2021). A Systems Approach to Brain Tumor Treatment. Cancers, 13(13), 3152. https://doi.org/10.3390/cancers13133152.
- Rahilly, M., Carder, P. J., al Nafussi, A., & Harrison, D. J. (1991). Distribution of glutathione S-transferase isoenzymes in human ovary. Journal of reproduction and fertility, 93(2), 303–311. https://doi.org/10.1530/jrf.0.0930303.
- Raza H.(2011). Dual localization of glutathione S-transferase in the cytosol and mitochondria: implications in oxidative stress, toxicity and disease. The FEBS Journal 2011; 278:4243–51. https://doi.org/10.1111/j.1742-4658.2011.08358.x
- Rustoen, T., Moum, T., Wiklund, I., & Hanestad, B. R. (1999). Quality of life in newly diagnosed cancer patients. Journal of advanced nursing, 29(2), 490–498. https://doi.org/10.1046/j.1365-2648.1999.00912.x
- Sarasso, E., Agosta, F., Piramide, N., & Filippi, M. (2021). Progression of grey and white matter brain damage in Parkinson's disease: a critical review of structural MRI literature. Journal of neurology, 268(9), 3144–3179. https://doi.org/10.1007/s00415-020-09863-8.
- Shang, W., Liu, WH., Zhao, XH.(2008). Expressions of glutathione S-transferase alpha, mu, and pi in brains of medically intractable epileptic patients. BMC Neurosci 9, 67. https://doi.org/10.1186/1471-2202-9-67
- Singh, R. R., & Reindl, K. M. (2021). Glutathione S-Transferases in Cancer. Antioxidants, 10(5), 701. MDPI AG. Retrieved from http://dx.doi.org/10.3390/antiox10050701.
- Sohn, S. W., Jung, J. W., Lee, S. Y., Kang, H. R., Park, H. W., Min, K. U., & Cho, S. H. (2013). Expression pattern of GSTP1 and GSTA1 in the pathogenesis of asthma. Experimental lung research, 39(4-5), 173-181. https://doi.org/10.3109/01902148.2013.789572
- Townsend, D. M., Findlay, V. L., & Tew, K. D. (2005). Glutathione S-transferases as regulators of kinase pathways and anticancer drug targets. Methods in enzymology, 401, 287–307. https://doi.org/10.1016/S0076-6879(05)01019-0
- Wahid, M., Mahjabeen, I., Baig, R. M., & Kayani, M. A. (2013). Expression of CYP1A1 and GSTP1 in human brain tumor tissues in Pakistan. Asian Pacific Journal of Cancer Prevention, 14(12), 7187-7191. https://doi.org/10.7314/APJCP.2013.14.12.7187
- Wang, B., Wang, W., Zhu, Z., Zhang, X., Tang, F., Wang, D., Liue, X., Yanc, L. X., Zhuang, H. (2017). Mitochondrial serine hydroxymethyltransferase 2 is a potential diagnostic and prognostic biomarker for human glioma. Clinical Neurology and Neurosurgery, 154, 28-33. https://doi.org/10.1016/j.clineuro.2017.01.005
- Wang, L., Chen, S., Ding, Y., Zhu, Q., Zhang, N., & Yu, S. (2018). Biofabrication of morphology improved cadmium sulfide nanoparticles using Shewanella oneidensis bacterial cells and ionic liquid: For toxicity against brain cancer cell lines. Journal of photochemistry and photobiology. B, Biology, 178, 424–427. https://doi.org/10.1016/j.jphotobiol.2017.11.007.
- Watson, R. R., & Killgore, W. D. (Eds.). (2016). Nutrition and lifestyle in neurological autoimmune diseases: multiple sclerosis. Academic Press.
- Wu, M., Chen, W., Chen, Y., Zhang, H., Liu, C., Deng, Z., Sheng, Z., Chen, J., Liu, X., Yan, F., & Zheng, H. (2018). Focused Ultrasound-Augmented Delivery of Biodegradable Multifunctional Nanoplatforms for Imaging-Guided Brain Tumor Treatment. Advanced science (Weinheim, Baden-Wurttemberg, Germany), 5(4), 1700474. https://doi.org/10.1002/advs.201700474.
- Yin, Z. L., Dahlstrom, J. E., Le Couteur, D. G., & Board, P. G. (2001). Immunohistochemistry of omega class glutathione S-transferase in human tissues. Journal of Histochemistry & Cytochemistry, 49(8), 983-987. https://doi.org/10.1177/002215540104900806
Yıl 2021,
Cilt: 5 Sayı: 2, 82 - 98, 01.12.2021
Onur Dirican
,
Pınar Kaygın
Sezen Yılmaz Sarıaltın
,
Can Yılmaz
,
Volkan Ateş
,
Gülçin Güler Şimşek
,
Serpil Oğuztüzün
,
Tülay Çoban
Yusuf İzci
Kaynakça
- Adwas, A.A., Elsayed, A.S.I., Azab, A.E.(2019). Oxidative stress and antioxidant mechanisms in human body. J Appl Biotechnol Bioeng. 2019;6(1):43-47. https://doi.org/10.15406/jabb.2019.06.00173
- Askari, H., Rajani, S. F., Poorebrahim, M., Haghi-Aminjan, H., Raeis-Abdollahi, E., & Abdollahi, M. (2018). A glance at the therapeutic potential of irisin against diseases involving inflammation, oxidative stress, and apoptosis: An introductory review. Pharmacological research, 129, 44–55. https://doi.org/10.1016/j.phrs.2018.01.012
- Backos, D. S., Franklin, C. C., & Reigan, P. (2012). The role of glutathione in brain tumor drug resistance. Biochemical pharmacology, 83(8), 1005-1012. https://doi.org/10.1016/j.bcp.2011.11.016
- Barnholtz-Sloan, J. S., Ostrom, Q. T., & Cote, D. (2018). Epidemiology of Brain Tumors. Neurologic clinics, 36(3), 395–419. https://doi.org/10.1016/j.ncl.2018.04.001.
- Calatozzolo, C., Gelati, M., Ciusani, E. (2005). Expression of Drug Resistance Proteins Pgp, MRP1, MRP3, MRP5 AND GST-π in Human Glioma. J Neurooncol 74, 113–121. https://doi.org/10.1007/s11060-004-6152-7
- Castello, L. M., Salmi, L., Zanotti, I., Gardino, C. A., Baldrighi, M., Settanni, F., & Avanzi, G. C. (2018). The increase in copeptin levels in mild head trauma does not predict the severity and the outcome of brain damage. Biomarkers in medicine, 12(6), 555–563. https://doi.org/10.2217/bmm-2018-0041.
- Cookson, M. S., Reuter, V. E., Linkov, I., & Fair, W. R. (1997). Glutathione S-transferase PI (GST-pi) class expression by immunohistochemistry in benign and malignant prostate tissue. The Journal of urology, 157(2), 673-676. https://doi.org/10.1016/S0022-5347(01)65248-0
- Courtens, A. M., Stevens, F. C., Crebolder, H. F., & Philipsen, H. (1996). Longitudinal study on quality of life and social support in cancer patients. Cancer nursing, 19(3), 162–169. https://doi.org/10.1097/00002820-199606000-00002.
- Darlix, A., Zouaoui, S., Rigau, V., Bessaoud, F., Figarella-Branger, D., Mathieu-Daudé, H., Trétarre, B., Bauchet, F., Duffau, H., Taillandier, L., & Bauchet, L. (2017). Epidemiology for primary brain tumors: a nationwide population-based study. Journal of neuro-oncology, 131(3), 525–546. https://doi.org/10.1007/s11060-016-2318-3.
- Ferlay, J., Colombet, M., Soerjomataram, I., Mathers, C., Parkin, D. M., Piñeros, M., Znaor, A., & Bray, F. (2019). Estimating the global cancer incidence and mortality in 2018: GLOBOCAN sources and methods. International journal of cancer, 144(8), 1941–1953. https://doi.org/10.1002/ijc.31937.
- Gulubova, M., & Vlaykova, T. (2010). Expression of the xenobiotic- and reactive oxygen species-detoxifying enzymes, GST-pi, Cu/Zn-SOD, and Mn-SOD in the endocrine cells of colorectal cancer. International journal of colorectal disease, 25(12), 1397–1405. https://doi.org/10.1007/s00384-010-1041-3
- Harrison, D. J., Kharbanda, R., Bishop, D., McLelland, L. I., & Hayes, J. D. (1989). Glutathione S-transferase isoenzymes in human renal carcinoma demonstrated by immunohistochemistry. Carcinogenesis, 10(7), 1257-1260. https://doi.org/10.1093/carcin/10.7.1257
- Hayat, B., Yavuz, M. S., Şahin, M. E., Dirican, O., Yılmaz, S., Yılmaz, C., Yıldırım, I., Çoban, T., Güler Şimşek, G. & Oğuztüzün, S. (2021). Kronik Obstrüktif Akciğer Hastalığında Glutatyon-S-Transferaz Mu1 ve Teta1 Polimorfizmlerinin Rolü. Journal of Faculty of Pharmacy of Ankara University, 45 (1), 41-56. https://doi.org/10.33483/jfpau.839530
- Hoshiya, T., Hasegawa, R., Hakoi, K., Cui, L., Ogiso, T., Cabral, R., & Ito, N. (1993). Enhancement by non-mutagenic pesticides of GST-P positive hepatic foci development initiated with diethylnitrosamine in the rat. Cancer letters, 72(1-2), 59-64. https://doi.org/10.1016/0304-3835(93)90011-W
- Huang, J., Tan, PH., Thiyagarajan, J.(2003). Prognostic Significance of Glutathione S-Transferase-Pi in Invasive Breast Cancer. Mod Pathol 16, 558–565. https://doi.org/10.1097/01.MP.0000071842.83169.5A
- Ji, C., Magnuson, J. T., Zhang, W., & Zhao, M. (2021). New insight into the enantioselective cytotoxicity of cypermethrin: imbalance between cell cycle and apoptosis. Journal of Hazardous Materials, 403, 123893. https://doi.org/10.1016/j.jhazmat.2020.123893.
- Jörg, S., Grohme, D. A., Erzler, M., Binsfeld, M., Haghikia, A., Müller, D. N., Linker, R. A., & Kleinewietfeld, M. (2016). Environmental factors in autoimmune diseases and their role in multiple sclerosis. Cellular and molecular life sciences : CMLS, 73(24), 4611–4622. https://doi.org/10.1007/s00018-016-2311-1.
- Kakehashi, A., Inoue, M., Wei, M., Fukushima, S., & Wanibuchi, H. (2009). Cytokeratin 8/18 overexpression and complex formation as an indicator of GST-P positive foci transformation into hepatocellular carcinomas. Toxicology and applied pharmacology, 238(1), 71-79. https://doi.org/10.1016/j.taap.2009.04.018
- Kumar, P. V., Ahamed, A. J., & Karthikeyan, M. (2019). Synthesis and characterization of NiO nanoparticles by chemical as well as green routes and their comparisons with respect to cytotoxic effect and toxicity studies in microbial and MCF-7 cancer cell models. SN Applied Sciences, 1(9), 1-15. https://doi.org/10.1007/s42452-019-1113-0
- Kural, C., Kaya Kocdogan, A., Şimşek, G. G., Oğuztüzün, S., Kaygın, P., Yılmaz, I., Bayram, T., & Izci, Y. (2019). Glutathione S-Transferases and Cytochrome P450 Enzyme Expression in Patients with Intracranial Tumors: Preliminary Report of 55 Patients. Medical principles and practice : international journal of the Kuwait University, Health Science Centre, 28(1), 56–62. https://doi.org/10.1159/000494496.
- Lark, A. L., Livasy, C. A., Calvo, B., Caskey, L., Moore, D. T., Yang, X., & Cance, W. G. (2003). Overexpression of focal adhesion kinase in primary colorectal carcinomas and colorectal liver metastases: immunohistochemistry and real-time PCR analyses. Clinical Cancer Research, 9(1), 215-222.
- Mathieu, A., Remmelink, M., D'Haene, N., Penant, S., Gaussin, J.-F., Van Ginckel, R., Darro, F., Kiss, R. and Salmon, I. (2004), Development of a chemoresistant orthotopic human nonsmall cell lung carcinoma model in nude mice. Cancer, 101: 1908-1918. https://doi.org/10.1002/cncr.20571
- Mendes, M., Sousa, J. J., Pais, A., & Vitorino, C. (2018). Targeted Theranostic Nanoparticles for Brain Tumor Treatment. Pharmaceutics, 10(4), 181. https://doi.org/10.3390/pharmaceutics10040181.
- Murray, G. I., & Burke, M. D. (1995). Immunohistochemistry of drug-metabolizing enzymes. Biochemical pharmacology, 50(7), 895-903. https://doi.org/10.1016/0006-2952(95)00136-N
- Nabetani, M., & Shintaku, H. (2018). New Strategy of Clinical Studies for Premature Babies with Ischemic Brain Damage. In Cell Therapy for Perinatal Brain Injury (pp. 17-24). Springer, Singapore.
- Nishimura, T., Newkirk, K., Sessions, R. B., Andrews, P. A., Trock, B. J., Rasmussen, A. A., Montgomery E. A., Bischoff E. K., Cullen, K. J. (1996). Immunohistochemical staining for glutathione S-transferase predicts response to platinum-based chemotherapy in head and neck cancer. Clinical cancer research, 2(11), 1859-1865.
- Nishimura, T., Newkirk, K., Sessions, R. B., Andrews, P. A., Trock, B. J., Rusmussen, A. A., Montgomery E. A., Bischoff E. K., Hanigan M. H., Cullen, K. J. (1998). Association between expression of glutathione-associated enzymes and response to platinum-based chemotherapy in head and neck cancer. Chemico-biological interactions, 111, 187-198.https://doi.org/10.1016/S0009-2797(97)00161-0
- Okidi, R., Ogwang, D. M., Okello, T. R., Ezati, D., Kyegombe, W., Nyeko, D., & Scolding, N. J. (2020). Factors affecting mortality after traumatic brain injury in a resource-poor setting. BJS open, 4(2), 320–325. https://doi.org/10.1002/bjs5.50243.
- Ostrom, Q. T., Adel Fahmideh, M., Cote, D. J., Muskens, I. S., Schraw, J. M., Scheurer, M. E., & Bondy, M. L. (2019). Risk factors for childhood and adult primary brain tumors. Neuro-oncology, 21(11), 1357–1375. https://doi.org/10.1093/neuonc/noz123.
- Ostrom, Q. T., Gittleman, H., Liao, P., Vecchione-Koval, T., Wolinsky, Y., Kruchko, C., & Barnholtz-Sloan, J. S. (2017). CBTRUS Statistical Report: Primary brain and other central nervous system tumors diagnosed in the United States in 2010-2014. Neuro-oncology, 19(suppl_5), v1–v88. https://doi.org/10.1093/neuonc/nox158.
- Park, J. H., de Lomana, A., Marzese, D. M., Juarez, T., Feroze, A., Hothi, P., Cobbs, C., Patel, A. P., Kesari, S., Huang, S., & Baliga, N. S. (2021). A Systems Approach to Brain Tumor Treatment. Cancers, 13(13), 3152. https://doi.org/10.3390/cancers13133152.
- Rahilly, M., Carder, P. J., al Nafussi, A., & Harrison, D. J. (1991). Distribution of glutathione S-transferase isoenzymes in human ovary. Journal of reproduction and fertility, 93(2), 303–311. https://doi.org/10.1530/jrf.0.0930303.
- Raza H.(2011). Dual localization of glutathione S-transferase in the cytosol and mitochondria: implications in oxidative stress, toxicity and disease. The FEBS Journal 2011; 278:4243–51. https://doi.org/10.1111/j.1742-4658.2011.08358.x
- Rustoen, T., Moum, T., Wiklund, I., & Hanestad, B. R. (1999). Quality of life in newly diagnosed cancer patients. Journal of advanced nursing, 29(2), 490–498. https://doi.org/10.1046/j.1365-2648.1999.00912.x
- Sarasso, E., Agosta, F., Piramide, N., & Filippi, M. (2021). Progression of grey and white matter brain damage in Parkinson's disease: a critical review of structural MRI literature. Journal of neurology, 268(9), 3144–3179. https://doi.org/10.1007/s00415-020-09863-8.
- Shang, W., Liu, WH., Zhao, XH.(2008). Expressions of glutathione S-transferase alpha, mu, and pi in brains of medically intractable epileptic patients. BMC Neurosci 9, 67. https://doi.org/10.1186/1471-2202-9-67
- Singh, R. R., & Reindl, K. M. (2021). Glutathione S-Transferases in Cancer. Antioxidants, 10(5), 701. MDPI AG. Retrieved from http://dx.doi.org/10.3390/antiox10050701.
- Sohn, S. W., Jung, J. W., Lee, S. Y., Kang, H. R., Park, H. W., Min, K. U., & Cho, S. H. (2013). Expression pattern of GSTP1 and GSTA1 in the pathogenesis of asthma. Experimental lung research, 39(4-5), 173-181. https://doi.org/10.3109/01902148.2013.789572
- Townsend, D. M., Findlay, V. L., & Tew, K. D. (2005). Glutathione S-transferases as regulators of kinase pathways and anticancer drug targets. Methods in enzymology, 401, 287–307. https://doi.org/10.1016/S0076-6879(05)01019-0
- Wahid, M., Mahjabeen, I., Baig, R. M., & Kayani, M. A. (2013). Expression of CYP1A1 and GSTP1 in human brain tumor tissues in Pakistan. Asian Pacific Journal of Cancer Prevention, 14(12), 7187-7191. https://doi.org/10.7314/APJCP.2013.14.12.7187
- Wang, B., Wang, W., Zhu, Z., Zhang, X., Tang, F., Wang, D., Liue, X., Yanc, L. X., Zhuang, H. (2017). Mitochondrial serine hydroxymethyltransferase 2 is a potential diagnostic and prognostic biomarker for human glioma. Clinical Neurology and Neurosurgery, 154, 28-33. https://doi.org/10.1016/j.clineuro.2017.01.005
- Wang, L., Chen, S., Ding, Y., Zhu, Q., Zhang, N., & Yu, S. (2018). Biofabrication of morphology improved cadmium sulfide nanoparticles using Shewanella oneidensis bacterial cells and ionic liquid: For toxicity against brain cancer cell lines. Journal of photochemistry and photobiology. B, Biology, 178, 424–427. https://doi.org/10.1016/j.jphotobiol.2017.11.007.
- Watson, R. R., & Killgore, W. D. (Eds.). (2016). Nutrition and lifestyle in neurological autoimmune diseases: multiple sclerosis. Academic Press.
- Wu, M., Chen, W., Chen, Y., Zhang, H., Liu, C., Deng, Z., Sheng, Z., Chen, J., Liu, X., Yan, F., & Zheng, H. (2018). Focused Ultrasound-Augmented Delivery of Biodegradable Multifunctional Nanoplatforms for Imaging-Guided Brain Tumor Treatment. Advanced science (Weinheim, Baden-Wurttemberg, Germany), 5(4), 1700474. https://doi.org/10.1002/advs.201700474.
- Yin, Z. L., Dahlstrom, J. E., Le Couteur, D. G., & Board, P. G. (2001). Immunohistochemistry of omega class glutathione S-transferase in human tissues. Journal of Histochemistry & Cytochemistry, 49(8), 983-987. https://doi.org/10.1177/002215540104900806