Role of <em>ABCB1</em> and glutathione S‑transferase gene variants in the association of porphyria cutanea tarda and human immunodeficiency virus infection

Pagnotta,Priscila Ayelén; Melito,Viviana Alicia; Lavandera,Jimena Verónica; Parera,Victoria Estela; Rossetti,María Victoria; Zuccoli,Johanna Romina; Buzaleh,Ana Maria

doi:10.3892/br.2020.1398

February-2021 Volume 14 Issue 2

Full Size Image

Journals

International Journal of Molecular Medicine

International Journal of Molecular Medicine is an international journal devoted to molecular mechanisms of human disease.

International Journal of Oncology

International Journal of Oncology is an international journal devoted to oncology research and cancer treatment.

Molecular Medicine Reports

Covers molecular medicine topics such as pharmacology, pathology, genetics, neuroscience, infectious diseases, molecular cardiology, and molecular surgery.

Oncology Reports

Oncology Reports is an international journal devoted to fundamental and applied research in Oncology.

Experimental and Therapeutic Medicine

Experimental and Therapeutic Medicine is an international journal devoted to laboratory and clinical medicine.

Oncology Letters

Oncology Letters is an international journal devoted to Experimental and Clinical Oncology.

Biomedical Reports

Explores a wide range of biological and medical fields, including pharmacology, genetics, microbiology, neuroscience, and molecular cardiology.

Molecular and Clinical Oncology

International journal addressing all aspects of oncology research, from tumorigenesis and oncogenes to chemotherapy and metastasis.

World Academy of Sciences Journal

Multidisciplinary open-access journal spanning biochemistry, genetics, neuroscience, environmental health, and synthetic biology.

International Journal of Functional Nutrition

Open-access journal combining biochemistry, pharmacology, immunology, and genetics to advance health through functional nutrition.

International Journal of Epigenetics

Publishes open-access research on using epigenetics to advance understanding and treatment of human disease.

Medicine International

An International Open Access Journal Devoted to General Medicine.

February-2021 Volume 14 Issue 2

Full Size Image

Article Open Access

Role of ABCB1 and glutathione S‑transferase gene variants in the association of porphyria cutanea tarda and human immunodeficiency virus infection

Authors:
- Priscila Ayelén Pagnotta
- Viviana Alicia Melito
- Jimena Verónica Lavandera
- Victoria Estela Parera
- María Victoria Rossetti
- Johanna Romina Zuccoli
- Ana Maria Buzaleh
View Affiliations / Copyright

Affiliations: Centro de Investigaciones sobre Porfirinas y Porfirias, Universidad de Buenos Aires, Argentina‑National Scientific and Technical Research Council, Hospital de Clínicas José de San Martín, Buenos Aires 1120, Argentina, Cátedra de Bromatología y Nutrición, Facultad de Bioquímica y Ciencias Biológicas, Universidad Nacional del Litoral, Santa Fe 3000, Argentina

Copyright: © Pagnotta et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
Article Number: 22
|
Published online on: December 4, 2020

https://doi.org/10.3892/br.2020.1398
Expand metrics +

Abstract

In Argentina, porphyria cutanea tarda (PCT) is strongly associated with infection with human immunodeficiency virus (HIV); however, whether the onset of this disease is associated with HIV infection and/or the antiretroviral therapy has not been determined. The ABCB1 gene variants c.1236C>T, c.2677G>T/A and c.3435C>T affect drug efflux. The GSTT1 null, GSTM1 null and GSTP1 (c.313A>G) gene variants alter Glutathione S‑transferase (GST) activity, modifying the levels of xenobiotics. The aim of the present study was to evaluate the role of genetic variants in initiation of PCT and to analyze the genetic basis of the PCT‑HIV association. Control individuals, and HIV, PCT and PCT‑HIV patients were recruited, PCR‑restriction fragment length polymorphism was used to genotype the ABCB1 and GSTP1 variants, and multiplex PCR was used to study the GSTM1 and GSTT1 variants. The high frequency of c.3435C>T (PCT and PCT‑HIV) and c.1236C>T (PCT) suggested that the onset of PCT were not specifically related to HIV infection or antiretroviral therapy for these variants. c.2677G>T/A frequencies in the PCT‑HIV patients were higher compared with the other groups, suggesting that a mechanism involving antiretroviral therapy served a role in this association. PCT‑HIV patients also had a high frequency of GSTT1 null and low frequency for GSTM1 null variants; thus, the genetic basis for PCT onset may involve a combination between the absence of GSTT1 and the presence of GSTM1. In conclusion, genes encoding for proteins involved in the flow and metabolism of xenobiotics may influence the PCT‑HIV association. The present study is the first to investigate the possible role of GST and ABCB1 gene variants in the triggering of PCT in HIV‑infected individuals, to the best of our knowledge, and may provide novel insights into the molecular basis of the association between PCT and HIV.

View Figures

View References

1	Batlle A: Porfirias humanas. Signos y tratamientos. En Porfirias y porfirinas. Aspectos clínicos, bioquímicos y biología molecular. Editorial Federación Bioquímica de la Provincia de Buenos Aires, La Plata, ISSN 0325-2957. Acta Bioquím Clín Latinoam Supl. 3:37–69. 1997.(In Spanish).
2	Rossetti MV, Buzaleh AM, Parera VE, Fukuda H, Lombardo ME, Lavandera J, Gerez EN, Melito VA, Zuccoli JR, Ruspini SV, et al: Metabolismo del Hemo: Las dos caras de los efectos de la acumulación de precursores y porfirinas. Acta Bioquim Clin Latinoamer Libro de Oro. 50:547–573. 2016.(In Spanish).
3	Méndez M, Rossetti MV, Gómez-Abecia S, Morán-Jiménez MJ, Parera V, Batlle A and Enríquez de Salamanca R: Molecular analysis of the UROD gene in 17 Argentinean patients with familial porphyria cutanea tarda: Characterization of four novel mutations. Mol Genet Metab. 105:629–633. 2012.PubMed/NCBI View Article : Google Scholar
4	Phillips JD: Heme biosynthesis and the porphyrias. Mol Genet Metab. 128:164–177. 2019.PubMed/NCBI View Article : Google Scholar
5	Weiss Y, Chen B, Yasuda M, Nazarenko I, Anderson KE and Desnick RJ: Porphyria cutanea tarda and hepatoerythropoietic porphyria: Identification of 19 novel uroporphyrinogen III decarboxylase mutations. Mol Genet Metab. 128:282–287. 2019.PubMed/NCBI View Article : Google Scholar
6	Jalil S, Grady JJ, Lee C and Anderson KE: Associations among behavior-related susceptibility factors in porphyria cutanea tarda. Clin Gastroenterol Hepatol. 8:297–302.e1. 2010.PubMed/NCBI View Article : Google Scholar
7	Singal AK, Venkata KVR, Jampana S, Islam FU and Anderson KE: Hepatitis C treatment in patients with porphyria Cutanea Tarda. Am J Med Sci. 353:523–528. 2017.PubMed/NCBI View Article : Google Scholar
8	To-Figueras J: Association between hepatitis C virus and porphyria Cutanea Tarda. Mol Genet Metab. 128:363–366. 2019.PubMed/NCBI View Article : Google Scholar
9	Ryan Caballes F, Sendi H and Bonkovsky HL: Hepatitis C, porphyria cutanea tarda, and liver iron: An update. Liver Int. 32:880–893. 2012.PubMed/NCBI View Article : Google Scholar
10	Usta Atmaca H and Akbas F: Porphyria cutanea tarda: A case report. J Med Case Rep. 13(17)2019.PubMed/NCBI View Article : Google Scholar
11	Franzon VA, Mikilita ES, Camelo FH and Camargo R: Porphyria cutanea tarda in a HIV-positive patient. An Bras Dermatol. 91:520–523. 2016.PubMed/NCBI View Article : Google Scholar
12	Melito VA, Parera VE, Rossetti MV and Batlle A: Manifestación de porfiria cutánea tardía en pacientes infectados con el virus de la inmunodeficiencia humana. Acta Bioquím Clín Latinoamer. 40:29–34. 2006.
13	Jalil SJ, Grady JJ, Lee C and Anderson KE: Associations among behavior-related susceptibility factors in porphyria cutanea tarda. Clin Gastroenterol Hepatol. 8(3):297–302. 2010.PubMed/NCBI View Article : Google Scholar
14	Aguilera P, Laguno M and To-Figueras J: Human immunodeficiency virus and risk of porphyria Cutanea Tarda: A possible association examined in a large hospital. Photodermatol Photoimmunol Photomed. 32:93–97. 2016.PubMed/NCBI View Article : Google Scholar
15	Hoffmeyer S, Burk O, von Richter O, Arnold HP, Brockmöller J, Johne A, Cascorbi I, Gerloff T, Roots I, Eichelbaum M and Brinkmann U: Functional polymorphisms of the human multidrug-resistance gene: Multiple sequence variations and correlation of one allele with P-glycoprotein expression and activity in vivo. Proc Natl Acad Sci USA. 97:3473–3478. 2000.PubMed/NCBI View Article : Google Scholar
16	Fung K and Gottesman M: A synonymous polymorphism in a common MDR1 (ABCB1) haplotype shapes protein function. Biochim Biophys Acta. 1794:860–871. 2009.PubMed/NCBI View Article : Google Scholar
17	Brambila-Tapia AJ: MDR1 (ABCB1) polymorphisms: Functional effects and clinical implications. Rev Invest Clin. 65:445–454. 2013.PubMed/NCBI
18	Yano K, Tomono T and Ogihara T: Advances in studies of P-Glycoprotein and its expression regulators. Biol Pharm Bull. 41:11–19. 2018.PubMed/NCBI View Article : Google Scholar
19	Arana MR and Altenberg GA: ATP-binding cassette exporters: Structure and mechanism with a focus on P-glycoprotein and MRP1. Curr Med Chem. 26:1062–1078. 2019.PubMed/NCBI View Article : Google Scholar
20	Wielandt AM, Vollrath V and Chianale J: Polymorphisms of the multiple drug resistance gene (MDR1) in Mapuche, Mestizo and Maori populations in Chile. Rev Med Chil. 132:1061–1068. 2004.PubMed/NCBI View Article : Google Scholar : (In Spanish).
21	Thuerauf N and Fromm MF: The role of the transporter P-glycoprotein for disposition and effects of centrally acting drugs and for the pathogenesis of CNS diseases. Eur Arch Psychiatry Clin Neurosci. 256:281–286. 2006.PubMed/NCBI View Article : Google Scholar
22	Fathy M, Kamal M, Mohy A and Nabil A: Impact of CYP3A5 and MDR-1 gene polymorphisms on the dose and level of tacrolimus among living-donor liver transplanted patients: Single center experience. Biomarkers. 21:335–341. 2016.PubMed/NCBI View Article : Google Scholar
23	Marzolini C, Paus E, Buclin T and Kim RB: Polymorphisms in human MDR1 (Pglycoprotein): Recent advances and clinical relevance. Clin Pharmacol Ther. 75:13–33. 2004.PubMed/NCBI View Article : Google Scholar
24	Sharom FJ: ABC multidrug transporters: Structure, function and role in chemoresistance. Pharmacogenomics. 9:105–127. 2008.PubMed/NCBI View Article : Google Scholar
25	Bellusci CP, Rocco C, Aulicino P, Mecikovsky D, Curras V, Hegoburu S, Bramuglia GF, Bologna R, Sen L and Mangano A: Influence of MDR1 C1236T polymorphism on lopinavir plasma concentration and virological response in HIV-1-infected children. Gene. 522:96–101. 2013.PubMed/NCBI View Article : Google Scholar
26	Yan Y, Liang H, Xie L, He Y, Li M, Li R, Li S and Qin X: Association of MDR1 G2677T polymorphism and leukemia risk: Evidence from a meta-analysis. Tumour Biol. 35:2191–2197. 2014.PubMed/NCBI View Article : Google Scholar
27	Strange RC, Spiteri MA, Ramachandran S and Fryer AA: Glutathione-S-transferase family of enzymes. Mutat Res. 482:21–26. 2001.PubMed/NCBI View Article : Google Scholar
28	Hayes JD, Flanagan JU and Jowsey IR: Glutathione transferases. Ann Rev Pharmacol Toxicol. 45:51–88. 2005.PubMed/NCBI View Article : Google Scholar
29	Schnekenburger M, Karius T and Diederich M: Regulation of epigenetic traits of the glutathione S-transferase P1 gene: From detoxification toward cancer prevention and diagnosis. Front Pharmacol. 16(170)2014.PubMed/NCBI View Article : Google Scholar
30	Weich N, Ferri C, Moiraghi B, Bengió R, Giere I, Pavlovsky C, Larripa IB and Fundia AF: GSTM1 and GSTP1, but not GSTT1 genetic polymorphisms are associated with chronic myeloid leukemia risk and treatment response. Cancer Epidemiol. 44:16–21. 2016.PubMed/NCBI View Article : Google Scholar
31	Brind AM, Hurlstone A, Edrisinghe D, Gilmore I, Fisher N, Pirmohamed M and Fryer AA: The role of polymorphisms of glutathione S-transferases GSTM1, M3, P1, T1 and A1 in susceptibility to alcoholic liver disease. Alcohol Alcohol. 39:478–483. 2004.PubMed/NCBI View Article : Google Scholar
32	Bowatte G, Lodge CJ, Perret JL, Matheson MC and Dharmage SC: Interactions of GST polymorphisms in air pollution exposure and respiratory diseases and allergies. Curr Allergy Asthma Rep. 16(85)2016.PubMed/NCBI View Article : Google Scholar
33	Singh HO, Lata S, Angadi M, Bapat S, Pawar J, Nema V, Ghate MV, Sahay S and Gangakhedkar RR: Impact of GSTM1, GSTT1 and GSTP1 gene polymorphism and risk of ARV-associated hepatotoxicity in HIV-infected individuals and its modulation. Pharmacogenomics J. 17:53–60. 2017.PubMed/NCBI View Article : Google Scholar
34	WMA Declaration of Helsinki-Ethical Principles for Medical Research Involving Human Subjects. World Medical Association: July 9, 2018 (urihttps://www.wma.net/policies-post/wma-declaration-of-helsinki-ethical-principles-for-medical-research-involving-human-subjectssimplehttps://www.wma.net/policies-post/wma-declaration-of-helsinki-ethical-principles-for-medical-research-involving-human-subjects).
35	Kim HJ, Hwang SY, Kim JH, Park HJ, Lee SG, Lee SW, Joo JC and Kim YK: Association between genetic polymorphism of multidrug resistance 1 gene and Sasang constitutions. Evid Based Complement Alternat Med. 6 (Suppl 1):S73–S80. 2009.PubMed/NCBI View Article : Google Scholar
36	Taheri M, Mahjoubi F and Omranipour R: Effect of MDR1 polymorphism on multidrug resistance expression in breast cancer patients. Gen Mol Res. 9:34–40. 2010.PubMed/NCBI View Article : Google Scholar
37	Zuccoli J, Melito V, Ruspini S, Lavandera J, Abelleyro M, Parera V, Rossetti MV, Batlle A and Buzaleh AM: Análisis de polimorfismos del exón 21 del gen MDR1 en la asociación Porfiria Cutánea Tardia-VIH. J Basic Appl Genetics. 25(278)2014.(In Spanish).
38	Solé X, Guinó E, Valls J, Iniesta R and Moreno V: SNPStats: A web tool for the analysis of association studies. Bioinformatics. 22:1928–1929. 2006.PubMed/NCBI View Article : Google Scholar
39	Moher D, Liberati A, Tetzlaff J and Altman DG: Preferred reporting items for systematic reviews and meta-analyses: The PRISMA Statement. PLoS Med. 6(e1000097)2009.PubMed/NCBI View Article : Google Scholar
40	Conde Almeida AC, Tadeu Villa R and Bedin V: Porfiria cutánea tarda no paciente infectado pelo vírus da imunodeficiência adquirida. Med Cutan Iber Lat Am. 38:91–93. 2010.
41	Quansah R, Cooper CJ, Said S, Bizet J, Paez D and Hernandez GT: Hepatitis C- and HIV-induced porphyria Cutanea Tarda. Am J Case Rep. 15:35–40. 2014.PubMed/NCBI View Article : Google Scholar
42	Farabaugh PJ and Björk G: How translational accuracy influences reading frame maintenance. EMBO J. 18:1427–1434. 1999.PubMed/NCBI View Article : Google Scholar
43	Kimchi-Sarfaty V, Oh J, Kim I, Sauna Z, Calcagno A, Ambudkar S and Gottesman MA: ‘Silent’ polymorphism in the MDR1 gene changes substrate specificity. Science. 315:525–528. 2007.PubMed/NCBI View Article : Google Scholar
44	Wen J and Brogna S: Nonsense-mediated mRNA decay. Biochem Soc Trans. 36:514–516. 2008.PubMed/NCBI View Article : Google Scholar
45	Kong LL, Zhuang XM, Yang HY, Yuan M, Xu L and Li H: Inhibition of P-glycoprotein gene expression and function enhances triptolide-induced hepatotoxicity in mice. Sci Rep. 5(11747)2015.PubMed/NCBI View Article : Google Scholar
46	Sakurai A, Onishi Y, Hirano H, Seigneuret M, Obanayama K, Kim G, Liew E, Sakaeda T, Yoshiura K, Niikawa N, et al: Quantitative Structure-activity relationship analysis and molecular dynamics simulation to functionally validate nonsynonymous polymorphisms of human ABC Transporter ABCB1 (P-Glycoprotein/MDR1). Biochemistry. 46:7678–7693. 2007.PubMed/NCBI View Article : Google Scholar
47	Ozdemir S, Uludag A, Silan F, Atik SY, Turgut B and Ozdemir O: Possible roles of the xenobiotic transporter P-glycoproteins encoded by the MDR1 3435 C>T gene polymorphism in differentiated thyroid cancers. Asian Pac J Cancer Prev. 14:3213–7321. 2013.PubMed/NCBI View Article : Google Scholar
48	Muralidharan N, Antony PT, Jain VK, Mariaselvam CM and Negi VS: Multidrug resistance 1 (MDR1) 3435C>T gene polymorphism influences the clinical phenotype and methotrexate-induced adverse events in South Indian Tamil rheumatoid arthritis. Eur J Clin Pharmacol. 71:959–965. 2015.PubMed/NCBI View Article : Google Scholar
49	Puoti M, Moioli MC, Travi G and Rossotti R: The burden of liver disease in human immunodeficiency virus-infected patients. Semin Liver Dis. 32:103–113. 2012.PubMed/NCBI View Article : Google Scholar
50	Debes JD, Bohjanen PR and Boonstra A: Mechanisms of accelerated liver fibrosis progression during HIV infection. J Clin Transl Hepatol. 4:328–335. 2016.PubMed/NCBI View Article : Google Scholar
51	Ganesan M, Poluektova LY, Kharbanda KK and Osna NA: Liver as a target of human immunodeficiency virus infection. World J Gastroenterol. 24:4728–4737. 2018.PubMed/NCBI View Article : Google Scholar
52	Ganesan M, New-Aaron M, Dagur RS, Makarov E, Wang W, Kharbanda KK, Kidambi S, Poluektova LY and Osna NA: Alcohol Metabolism potentiates HIV-induced hepatotoxicity: Contribution to End-stage liver disease. Biomolecules. 9(851)2019.PubMed/NCBI View Article : Google Scholar
53	Bhattacharjee P, Paul S, Banerjee M, Patra D, Banerjee P, Ghoshal N, Bandyopadhyay A and Giri AK: Functional compensation of glutathione S-transferase M1 (GSTM1) null by another GST superfamily member, GSTM2. Sci Rep. 3(2704)2013.PubMed/NCBI View Article : Google Scholar
54	Doukali H, Ben Salah G, Hamdaoui L, Hajjaji M, Tabebi M, Ammar-Keskes L, Masmoudi ME and Kamoun H: Oxidative stress and glutathione S-transferase genetic polymorphisms in medical staff professionally exposed to ionizing radiation. Int J Radiat Biol. 93:697–704. 2017.PubMed/NCBI View Article : Google Scholar
55	Datta SK, Kumar V, Pathak R, Tripathi AK, Ahmed RS, Kalra OP and Banerjee BD: Association of glutathione S-transferase M1 and T1 gene polymorphism with oxidative stress in diabetic and nondiabetic chronic kidney disease. Ren Fail. 32:1189–1195. 2010.PubMed/NCBI View Article : Google Scholar
56	Suvakov S, Damjanovic T, Stefanovic A, Pekmezovic T, Savic-Radojevic A, Pljesa-Ercegovac M, Matic M, Djukic T, Coric V, Jakovljevic J, et al: Glutathione S-transferase A1, M1, P1 and T1 null or low-activity genotypes are associated with enhanced oxidative damage among haemodialysis patients. Nephrol Dial Transplant. 28:202–212. 2013.PubMed/NCBI View Article : Google Scholar
57	Mhaidat N, Alshogran O, Khabour O, Alzoubi K, Matalka I, Haddadin W, Mahasneh I and Aldaher A: Multi-drug resistance 1 genetic polymorphism and prediction of chemotherapy response in Hodgkin's Lymphoma. J Exp Clin Cancer Res. 30(68)2011.PubMed/NCBI View Article : Google Scholar
58	Milojkovic M, Stojnev S, Jovanovic I, Ljubisavljevic S, Stefanovic V and Sunder-Plassman R: Frequency of the C1236T, G2677T/A and C3435T MDR1 gene polymorphisms in the Serbian population. Pharmacol Rep. 63:808–814. 2011.PubMed/NCBI View Article : Google Scholar
59	Komoto C, Nakamura T, Sakaeda T, Kroetz DL, Yamada T, Omatsu H, Koyama T, Okamura N, Miki I, Tamura T, et al: MDR1 haplotype frequencies in Japanese and Caucasian, and in Japanese patients with colorectal cancer and esophageal cancer. Drug Metab Pharmacokinet. 21:126–132. 2006.PubMed/NCBI View Article : Google Scholar
60	Weich N, Roisman A, Cerliani B, Aráoz HV, Chertkoff L, Richard SM, Slavutsky I, Larripa IB and Fundia AF: Gene polymorphism profiles of drug-metabolising enzymes GSTM1, GSTT1 and GSTP1 in an Argentinian population. Ann Hum Biol. 44:379–383. 2017.PubMed/NCBI View Article : Google Scholar
61	Rossini A, Rapozo D, Amorim L, Macedo J, Medina R, Neto J, Gallo C and Pinto L: Frequencies of GSTM1, GSTT1, and GSTP1polymorphisms in a Brazilian population. Genet Mol Res. 1:233–240. 2002.PubMed/NCBI
62	Pinheiro D, Santos R, Brito R, Cruz A, Ghedini P and Reis A: GSTM1/GSTT1 double-null genotype increases risk of treatment-resistant schizophrenia: A genetic association study in Brazilian patients. PLoS One. 12(e0183812)2017.PubMed/NCBI View Article : Google Scholar
63	Klusek J, Nasierowska-Guttmejer A, Kowalik A, Wawrzycka I, Lewitowicz P, Chrapek M and Głuszek S: GSTM1, GSTT1, and GSTP1 polymorphisms and colorectal cancer risk in Polish nonsmokers. Oncotarget. 9:21224–21230. 2018.PubMed/NCBI View Article : Google Scholar
64	Srivastava DSL, Jain VK, Verma P and Yadav JP: Polymorphism of glutathione S-transferase M1 and T1 genes and susceptibility to psoriasis disease: A study from North India. Indian J Dermatol Venereol Leprol. 84:39–44. 2018.PubMed/NCBI View Article : Google Scholar
65	Stamenkovic M, Lukic V, Suvakov S, Simic T, Sencanic I, Pljesa-Ercegovac M, Jaksic V, Babovic S, Matic M, Radosavljevic A, et al: GSTM1-null and GSTT1-active genotypes as risk determinants of primary open angle glaucoma among smokers. Int J Ophthalmol. 11:1514–1520. 2018.PubMed/NCBI View Article : Google Scholar
66	ThekkePurakkal AS, Nicolau B, Burk RD, Franco EL and Schlecht NF: Genetic variants in CYP and GST genes, smoking and risk for head and neck cancers: A gene-environment interaction hospital-based case-control study among Canadian Caucasians. Carcinogenesis: Apr 2, 2019 doi: 10.1093/carcin/bgz051 (Epub ahead of print).
67	Musavi Z, Moasser E, Zareei N, Azarpira N and Shamsaeefar A: Glutathione S-transferase gene polymorphisms and the development of new-onset diabetes after liver transplant. Exp Clin Transplant. 17:375–380. 2019.PubMed/NCBI View Article : Google Scholar
68	Zehra A, Zehra S, Ismail M and Azhar A: Glutathione S-transferase M1 and T1 gene deletions and susceptibility to acute lymphoblastic leukemia (ALL) in adults. Pak J Med Sci. 34:666–670. 2018.PubMed/NCBI View Article : Google Scholar
69	Saravani S, Miri-Moghaddam M, Bazi A and Miri-Moghaddam E: Association of glutathione-S-transferases M1 and T1 deletional variants with development of oral squamous cell carcinoma: A study in the South-East of Iran. Asian Pac J Cancer Prev. 20:1921–1926. 2019.PubMed/NCBI View Article : Google Scholar
70	Farmohammadi A, Arab-Yarmohammadi V and Ramzanpour R: Association analysis of rs1695 and rs1138272 variations in GSTP1 gene and breast cancer susceptibility. Asian Pac J Cancer Prev. 21:1167–1172. 2020.PubMed/NCBI View Article : Google Scholar
71	Oshodi Y, Ojewunmi O, Oshodi TA, Ijarogbe GT, Ogun OC, Aina OF and Lesi F: Oxidative stress markers and genetic polymorphisms of glutathione S-transferase T1, M1, and P1 in a subset of children with autism spectrum disorder in Lagos, Nigeria. Niger J Clin Pract. 20:1161–1167. 2017.PubMed/NCBI View Article : Google Scholar
72	Idris HM, Elderdery AY, Khalil HB and Mills J: Genetic Polymorphism of GSTP1, GSTM1 and GSTT1 genes and susceptibility to chronic myeloid leukaemia. Asian Pac J Cancer Prev. 21:499–503. 2020.PubMed/NCBI View Article : Google Scholar
73	Rebai A, Chbili C, Ben Amor S, Hassine A, Ben Ammou S and Saguem S: Effects of glutathione S-transferase M1 and T1 deletions on Parkinson's disease risk among a North African population. Rev Neurol (Paris): Apr 29, 2020 (Epub ahead of print).