DOI QR코드

DOI QR Code

Distributions of the GSTM1 and GSTT1 Null Genotypes Worldwide are Characterized by Latitudinal Clines

  • Saitou, Marie (Unit of Human Biology and Genetics, Department of Biological Sciences, Graduate School of Science, University of Tokyo) ;
  • Ishida, Takafumi (Unit of Human Biology and Genetics, Department of Biological Sciences, Graduate School of Science, University of Tokyo)
  • 발행 : 2015.02.04

초록

Background: Deletion types of genetic variants of glutathione S-transferase (GST) M1 and T1, the GSTM1 null and GSTT1 null which are risk factors for certain cancers, have been ubiquitously found in human populations but their worldwide distribution pattern is unclear. Materials and Methods: To perform a meta-analysis, a systematic search for the literature on GSTM1 and GSTT1 null genotypes was done to identify 63 reports for 81 human populations. Relationships between the GSTM1 and GSTT1 null genotype frequencies and the absolute latitude of 81 populations were tested by Spearman's rank correlation coefficient. Results: A significant positive correlation was detected between the GSTM1 null genotype frequency and the absolute latitude (r=0.28, p-value <0.05), whereas the GSTT1 null genotype frequency and absolute latitude showed a significant negative correlation (r= -0.41 p-value <0.01). There was no correlation between the frequencies of GSTM1 and GSTT1 null genotype in each population (r= -0.029, p-value=0.80). Conclusions: Latitudinal clines of the distribution of the GSTM1 and GSTT1 null genotypes may be attributed to the result of gene-environmental adaptation. No functional compensation between GSTM1 and GSTT1 was suggested by the lack of correlation between the null frequencies for GSTM1 and GSTT1.

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참고문헌

  1. Abbas A, Delvinquiere K, Lechevrel M, et al (2004). Susceptibility to esophageal cancer in a French population: Different pattern of squamous cell carcinoma and adenocarcinoma. World J Gastroenterol, 10, 3389-93. https://doi.org/10.3748/wjg.v10.i23.3389
  2. Ada AO, Kunak SC, Hancer F, et al (2012). Association between GSTM1, GSTT1, and GSTP1 polymorphisms and lung cancer risk in a Turkish population. Mol Biol Rep, 39, 5985-93. https://doi.org/10.1007/s11033-011-1411-0
  3. Agusa T, Iwata H, Fujihara J, et al (2010). Genetic polymorphisms in glutathione S-transferase (GST) superfamily and arsenic metabolism in residents of the Red River Delta, Vietnam. Toxicol Applied Pharmacol, 242, 352-62. https://doi.org/10.1016/j.taap.2009.11.007
  4. Al-Dayel F, Al-Rasheed M, Ibrahim M, et al (2008). Polymorphisms of drug-metabolizing enzymes CYP1A1, GSTT and GSTP contribute to the development of diffuse large B-cell lymphoma risk in the Saudi Arabian population. Leukemia Lymphoma, 49, 122-9. https://doi.org/10.1080/10428190701704605
  5. Amtha R, Ching CS, Zain R, et al (2009). GSTM1, GSTT1 and CYP1A1 polymorphisms and risk of oral cancer: a casecontrol study in Jakarta, Indonesia. Asian Pac J Cancer Prev, 10, 21-6.
  6. Baclig MO, Alvarez MR, Lozada XMR, et al (2012). Association of glutathione S-transferase T1 and M1 genotypes with chronic liver diseases among Filipinos. Int J Mol Epidemiol Genet, 3, 153-9.
  7. Buchard A, Sanchez JJ, Dalhoff K, Morling N (2007). Multiplex PCR detection of GSTM1, GSTT1, and GSTP1 gene variants: Simultaneously detecting GSTM1 and GSTT1 gene copy number and the allelic status of the GSTP1 Ile105Val genetic variant. J Mol Diagn, 9, 612-7. https://doi.org/10.2353/jmoldx.2007.070030
  8. Chen B, Bai Y, Sun M, et al (2012). Glutathione S-transferases T1 null genotype is associated with susceptibility to aristolochic acid nephropathy. Int Urol Nephrol, 44, 301-7. https://doi.org/10.1007/s11255-011-0082-z
  9. Da Fonseca RR, Johnson WE, O'Brien SJ, Vasconcelos V, Antunes A (2010). Molecular evolution and the role of oxidative stress in the expansion and functional diversification of cytosolic glutathione transferases. Evol Biol, 10, 281-91.
  10. Dialyna I, Arvanitis D, Spandidos D (2001). Genetic polymorphisms and transcriptional pattern analysis of CYP1A1, AhR, GSTM1, GSTP1 and GSTT1 genes in breast cancer. Int J Mol Med, 8, 79-87.
  11. Dolzan V, Rudolf Z, Breskvar K (2006). Genetic susceptibility to environmental carcinogenesis in Slovenian melanoma patients. Acta Dermatovenerol Alp Panonica Adriat, 15, 69-78.
  12. Ebeshi BU, Bolaji OO, Masimirembwa CM (2011). Glutathione-S-transferase (M1 and T1) polymorphisms in Nigerian populations. J Med Genet, 3, 56-60.
  13. Ebrahimi M, Podolskaya SV, Grigorieva N (2004). Genetic polymorphisms of glutathione S-transferase susceptibility in Ukrainian population. Iranian J Biotechnol, 2, 230-5.
  14. Frova C (2006). Glutathione transferases in the genomics era: New insights and perspectives. Biomol Eng, 23, 149-69. https://doi.org/10.1016/j.bioeng.2006.05.020
  15. Fuciarelli M, Caccuri A, De Francesca M, et al (2009). Modulation of the GSTT1 activity by the GSTM1 phenotype in a sample of Italian farm-workers. Arch Toxicol, 83, 115-20. https://doi.org/10.1007/s00204-008-0334-6
  16. Fujihara J, Yasuda T, Iida R, et al (2009). Cytochrome P450 1A1, glutathione S-transferases M1 and T1 polymorphisms in Ovambos and Mongolians. Legal Med, 11, 408-10. https://doi.org/10.1016/j.legalmed.2009.01.073
  17. Garte S, Gaspari L, Alexandrie AK, et al (2001). Metabolic gene polymorphism frequencies in control populations. Cancer Epidemiol Biomarkers Prev, 10, 1239-48.
  18. Gaspar P, Hutz MH, Salzano FM, et al (2002). Polymorphisms of CYP1a1, CYP2e1, GSTM1, GSTT1, and TP53 genes in Amerindians. Am J Phy Anthropol, 119, s249-56. https://doi.org/10.1002/ajpa.10128
  19. Gudmundsdottir K, Tryggvadottir L, Eyfjord JE (2001). GSTM1, GSTT1, and GSTP1 genotypes in relation to breast cancer risk and frequency of mutations in the p53 gene. Cancer Epidemiol Biomarkers Prev, 10, 1169-73.
  20. Gundacker C, Wittmann KJ, Kukuckova M, et al (2009), Genetic background of lead and mercury metabolism in a group of medical students in Austria. Environ Res, 109, 786-96. https://doi.org/10.1016/j.envres.2009.05.003
  21. Hamdy SI, Hiratsuka M, Narahara K, et al (2003). Genotype and allele frequencies of TPMT, NAT2, GST, SULT1A1 and MDR-1 in the Egyptian population. Br J Clin Pharmacol, 55, 560-9. https://doi.org/10.1046/j.1365-2125.2003.01786.x
  22. Hayes JD, Pulford DJ (1995). The Glutathione s-transferase supergene family: Regulation of GST and the contribution of the lsoenzymes to cancer chemoprotection and drug resistance. Crit Rev Biochem Mol Biol, 30, 445-520. https://doi.org/10.3109/10409239509083491
  23. Hayes JD, Flanagan JU, Jowsey IR (2005). Glutathione transferases. Annu Rev Pharmacol Toxicol, 45, 51-88. https://doi.org/10.1146/annurev.pharmtox.45.120403.095857
  24. Holla, LI, Stejskalova A, Vasku A (2006). Polymorphisms of the GSTM1 and GSTT1 genes in patients with allergic diseases in the Czech population. Allergy, 61, 265-7. https://doi.org/10.1111/j.1398-9995.2006.01000.x
  25. Jablonski NG, Chaplin G (2000). The evolution of human skin coloration. J Hum Evol, 39, 57-106. https://doi.org/10.1006/jhev.2000.0403
  26. Jablonski NG, Chaplin G (2010). Colloquium paper: Human skin pigmentation as an adaptation to UV radiation. Proc Natl Acad Sci U S A, 107, 8962-8. https://doi.org/10.1073/pnas.0914628107
  27. Jiang Y, Li N, Dong P, et al (2011). Polymorphisms in GSTM1, GSTTI and GSTP1 and nasopharyngeal cancer in the east of China: A case-control study. Asian Pac J Cancer Prev, 12, 3097-100.
  28. Jing C, Huang ZJ, Duan YQ, et al (2012). Glulathione-Stransferases gene polymorphism in prediction of gastric cancer risk by smoking and Helicobacter pylori infection status. Asian Pac J Cancer Prev, 13, 3325-8. https://doi.org/10.7314/APJCP.2012.13.7.3325
  29. Karban A, Krivoy N, Elkin H, et al (2011). Non-Jewish Israeli IBD patients have significantly higher glutathione S-transferase GSTT1-null frequency. Dig Dis Sci, 56, 2081-7. https://doi.org/10.1007/s10620-010-1543-4
  30. Kargas C, Krupa R, Walter Z (2003). Combined genotype analysis of GSTM1 and GSTT1 polymorphisms in a Polish population. Hum Biol, 75, 301-7. https://doi.org/10.1353/hub.2003.0033
  31. Katoh T, Nagata N, Kuroda Y, et al (1996). Glutathione S-transferase M1 (GSTM1) and T1 (GSTT1) genetic polymorphism and susceptibility to gastric and colorectal adenocarcinoma. Carcinogenesis, 17, 1855-9. https://doi.org/10.1093/carcin/17.9.1855
  32. Khan MI, Micheal S, Akhtar F, et al (2010). The association of glutathione S-transferase GSTT1 and GSTM1 gene polymorphism with pseudoexfoliative glaucoma in a Pakistani population. Mol Vision, 16, 2146-52.
  33. Kietthubthew S (2006). Molecular epidemiology of oral cancer susceptibility genes in Southern Thailand. Doctoral dissertation submitted to the University of Tokyo.
  34. Kirk GD, Turner PC, Gong Y, et al (2005). Hepatocellular carcinoma and polymorphisms in carcinogen-metabolizing and DNA repair enzymes in a population with aflatoxin exposure and hepatitis B virus endemicity. Cancer Epidemiol Biomarkers Prev, 14, 373-9. https://doi.org/10.1158/1055-9965.EPI-04-0161
  35. Lakhdar R, Denden S, Knani J, et al (2010). Association of GSTM1 and GSTT1 polymorphisms with chronic obstructive pulmonary disease in a Tunisian population. Biochem Genet, 48, 647-57. https://doi.org/10.1007/s10528-010-9346-z
  36. Li CG, Zhao Z-M, Hu MG, Liu R (2012). Predictive role of glutathione-S-transferase gene polymorphisms in risk and prognosis of hepatocellular carcinoma. Asian Pac J Cancer Prev, 13, 3247-52. https://doi.org/10.7314/APJCP.2012.13.7.3247
  37. Little J, Sharp L, Masson LF, et al (2006). Colorectal cancer and genetic polymorphisms of CYP1A1, GSTM1 and GSTT1: A case-control study in the Grampian region of Scotland. Int J Cancer, 119, 2155-64. https://doi.org/10.1002/ijc.22093
  38. Liu L, Li C, Gao J, et al (2009). Genetic polymorphisms of glutathione S-transferase and risk of vitiligo in the Chinese population. J Invest Dermatol, 129, 2646-52. https://doi.org/10.1038/jid.2009.143
  39. Lu XF, Yang WL, Wan ZH, Li J, Bi ZG (2011). Glutathione S-transferase polymorphisms and bone tumor risk in China. Asian Pac J Cancer Prev, 12, 3357-60.
  40. Malakar M, Devi KR, Phukan RK, et al (2012). Genetic polymorphism of glutathione S-transferases M1 and T1, tobacco habits and risk of stomach cancer in Mizoram, India. Asian Pac J Cancer Prev, 13, 4725-32. https://doi.org/10.7314/APJCP.2012.13.9.4725
  41. Malik MA, Upadhyay R, Mittal RD, Zargar SA, Mittal B (2010). Association of xenobiotic metabolizing enzymes genetic polymorphisms with esophageal cancer in Kashmir Valley and influence of environmental factors. Nutr Cancer, 62, 734-42. https://doi.org/10.1080/01635581003605904
  42. Matakova T, Sivonova M, Halasova E, et al (2009). Gene polymorphisms of biotransforming enzymes (GSTs) and their association with lung cancer in the Slovakian population. Eur J Med Res, 14, 275-279. https://doi.org/10.1186/2047-783X-14-S4-275
  43. McIlwain CC, Townsend DM, Tew KD (2006). Glutathione S-transferase polymorphisms: Cancer incidence and therapy. Oncogene, 25, 1639-48. https://doi.org/10.1038/sj.onc.1209373
  44. Minelli C, Granell R, Newson R, et al (2010). Glutathione-Stransferase genes and asthma phenotypes: A Human Genome Epidemiology (HuGE) systematic review and meta-analysis including unpublished data. Int J Epidemiol, 39, 539-62. https://doi.org/10.1093/ije/dyp337
  45. Mitrunen K, Jourenkova N, Kataja V, et al (2001). Polymorphisms and susceptibility to breast cancer. Cancer Epidemiol Biomarkers Prev, 10, 229-36.
  46. Moasser E, Kazemi-Nezhad SR, Saadat M, Azarpira N (2012). Study of the association between glutathione S-transferase (GSTM1, GSTT1, GSTP1) polymorphisms with type II diabetes mellitus in southern of Iran. Mol Biol Rep, 39, 10187-92. https://doi.org/10.1007/s11033-012-1893-4
  47. Nair UJ, Nair J, Mathew B, and Bartsch H (1999). Glutathione S-transferase M1 and T1 null genotypes as risk factors for oral leukoplakia in ethnic Indian betel quid/tobacco chewers. Carcinogenesis, 20, 743-8. https://doi.org/10.1093/carcin/20.5.743
  48. Niwa Y, Hirose K, Nakanishi, T et al (2005). Association of the NAD(P)H: Quinone oxidoreductase C609T polymorphism and the risk of cervical cancer in Japanese subjects. Gynecol Oncol, 96, 423-9. https://doi.org/10.1016/j.ygyno.2004.10.015
  49. Pakakasama S, Mukda E, Sasanakul W, et al (2005). Polymorphisms of drug-metabolizing enzymes and risk of childhood acute lymphoblastic leukemia. Am J Hematol, 79, 202-5. https://doi.org/10.1002/ajh.20404
  50. Palli D, Saieva C, Gemma S, et al (2005). GSTT1 and GSTM1 gene polymorphisms and gastric cancer in a high-risk Italian population. Int J Cancer, 115, 284-9. https://doi.org/10.1002/ijc.20864
  51. Pan S, Yang X, Yang L, et al (2011). Human GSTs polymorphisms in the Hakka population of south China and their associations with family history of several chronic diseases. Biomedical Environ Sci, 24, 491-8.
  52. Parl FF (2005). Glutathione S-transferase genotypes and cancer risk. Cancer Lett, 221, 123-9. https://doi.org/10.1016/j.canlet.2004.06.016
  53. Pemble S, Schroeder KR, Spencer SR, et al (1994). Human glutathione S-transferase theta (GSTT1): cDNA cloning and the characterization of a genetic polymorphism. Biochem J, 300, 271-6. https://doi.org/10.1042/bj3000271
  54. Piacentini S, Polimanti R, Porreca F, et al (2011). GSTT1 and GSTM1 gene polymorphisms in European and African populations. Mol Biol Rep, 38, 1225-30. https://doi.org/10.1007/s11033-010-0221-0
  55. Piacentini S, Polimanti R, Squitti R, et al (2012). GSTM1 null genotype as risk factor for late-onset Alzheimer's disease in Italian patients. J Neurol Sci, 317, 137-40. https://doi.org/10.1016/j.jns.2012.01.026
  56. Ramalhinho AC, Fonseca-Moutinho JA, Breitenfeld L (2011). Glutathione S-transferase M1, T1, and P1 genotypes and breast cancer risk: A study in a Portuguese population. Mol Cell Biochem, 355, 265-71. https://doi.org/10.1007/s11010-011-0863-9
  57. Roodi N, Dupont WD, Moore JH, Parl FF (2004). Association of Homozygous wild-type Glutathione S-Transferase M1 genotype with increased breast cancer risk. Cancer Res, 64, 1233-6. https://doi.org/10.1158/0008-5472.CAN-03-2861
  58. Saadat M (2007). GSTM1 null genotype associated with agestandardized cancer mortality rate in 45 countries from five continents: An ecologic study. Int J Cancer Res, 3, 74-91. https://doi.org/10.3923/ijcr.2007.74.91
  59. Safarinejad MR, Shafiei N, Safarinejad SH (2011). Glutathione S-transferase gene polymorphisms (GSTM1, GSTT1, GSTP1) and prostate cancer: A case-control study in Tehran, Iran. Prostate Cancer Prostatic Dis, 14, 105-13. https://doi.org/10.1038/pcan.2010.54
  60. Saify K, Saadat I, Saadat M (2012). Genetic polymorphisms of glutathione S-transferase T1 (GSTT1) and M1 (GSTM1) in selected populations of Afghanistan. Mol Biol Rep, 39, 7855-9. https://doi.org/10.1007/s11033-012-1628-6
  61. Salem AH, Yaqoob A, Ali M, et al (2011). Genetic polymorphism of the glutathione S-transferase M1 and T1 genes in three distinct Arab populations. Disease Markers, 31, 311-6. https://doi.org/10.1155/2011/796520
  62. Saravana-Devi S, Vinayagamoorthy N, Agrawal M, et al (2008). Distribution of detoxifying genes polymorphism in Maharastrian population of central India. Chemosphere, 70, 1835-9. https://doi.org/10.1016/j.chemosphere.2007.08.008
  63. Seidegard J, Vorachek WR, Pero RW and Pearson WR (1988) Hereditary differences in the expression of the human glutathione transferase active on trans-stilbene oxide are due to a gene deletion. Proc Natl Acad Sci USA, 85, 7293-7. https://doi.org/10.1073/pnas.85.19.7293
  64. Setiawan VW, Zhang ZF, Yu GP, et al (2000). GSTT1 and GSTM1 null genotypes and the risk of gastric cancer: A case-control study in a Chinese population. Cancer Epidemiol Biomarkers Prev, 9, 73-80.
  65. Settheetham-Ishida W, Yuenyao P, Kularbkaew C, Settheetham D, Ishida T (2009). Glutathione S-transferase (GSTM1 and GSTT1) polymorphisms in cervical cancer in Northeastern Thailand. Asian Pac J Cancer Prev, 10, 365-8.
  66. Shaikh RS, Amir M, Masood AI, et al (2010). Frequency distribution of GSTM1 and GSTT1 null allele in Pakistani population and risk of disease incidence. Environ Toxicol Pharmacol, 30, 76-9. https://doi.org/10.1016/j.etap.2010.04.002
  67. Sheehan D, Meade G, Foley VM, Dowd CA (2001). Structure, function and evolution of glutathione transferases: Implications for classification of non-mammalian members of an ancient enzyme superfamily. Biochem J, 16, 1-16.
  68. Shi H, Tan S-jie, Zhong H, et al (2009). Winter temperature and UV are tightly linked to genetic changes in the p53 tumor suppressor pathway in Eastern Asia. Am J Hum Genet, 84, 534-41. https://doi.org/10.1016/j.ajhg.2009.03.009
  69. Singh S, Kumar V, Thakur S, et al (2009). Genetic polymorphism of glutathione S-transferase M1 and T1 in Delhi population of Northern India. Environ Toxicol Pharmacol, 28, 25-9. https://doi.org/10.1016/j.etap.2009.01.010
  70. Singh N, Sinha N, Kumar S, Pandey CM, Agrawal S (2011). Glutathione S-transferase gene polymorphism as a susceptibility factor for acute myocardial infarction and smoking in the North Indian population. Cardiology, 118, 16-21. https://doi.org/10.1159/000324066
  71. Skjelbred CF, Svendsen M, Haugan V, et al (2011). Influence of GSTM1, GSTT1, GSTP1, NAT1, NAT2, EPHX1, MTR and MTHFR polymorphism on chromosomal aberration frequencies in human lymphocytes. Carcinogenesis, 32, 399-405. https://doi.org/10.1093/carcin/bgq246
  72. Song DK, Xing DL, Zhang, LR, et al (2009). Association of NAT2, GSTM1, GSTT1, CYP2A6, and CYP2A13 gene polymorphisms with susceptibility and clinicopathologic characteristics of bladder cancer in Central China. Cancer Detection Prev, 32, 416-23. https://doi.org/10.1016/j.cdp.2009.02.003
  73. Sprenger R, Schlagenhaufer R, Kerb R, et al (2000). Characterization of the glutathione S-transferase GSTT1 deletion: Discrimination of all genotypes by polymerase chain reaction indicates a trimodular genotype-phenotype correlation. Pharmacogenetics, 10, 557-65. https://doi.org/10.1097/00008571-200008000-00009
  74. Sreeja L, Syamala V, Hariharan S, et al (2005). Possible risk modification by CYP1A1, GSTM1 and GSTT1 gene polymorphisms in lung cancer susceptibility in a South Indian population. J Hum Genet, 50, 618-27. https://doi.org/10.1007/s10038-005-0303-3
  75. Sundberg K, Johansson AS, Stenberg G, et al (1998). Differences in the catalytic efficiencies of allelic variants of glutathione transferase P1-1 towards carcinogenic diol epoxides of polycyclic aromatic hydrocarbons Carcinogenesis. Carcinogenesis, 19, 433-6. https://doi.org/10.1093/carcin/19.3.433
  76. Suvakov S, Damjanovic T, Stefanovic A, et al (2012). Glutathione S-transferase A1, M1, P1 and T1 null or lowactivity genotypes are associated with enhanced oxidative damage among haemodialysis patients. Nephrol Dial Transplant, 28, 1-10.
  77. Tamaki Y, Arai T, Sugimura H, et al (2011). Association between cancer risk and drug-metabolizing enzyme gene (CYP2A6, CYP2A13, CYP4B1, SULT1A1, GSTM1, and GSTT1) polymorphisms in cases of lung cancer in Japan. Drug Metab Pharmacokinet, 26, 516-22. https://doi.org/10.2133/dmpk.DMPK-11-RG-046
  78. Tiemersma EW, Omer RE, Bunschoten A (2001). Role of genetic polymorphism of Glutathione- S -Transferase T1 and microsomal epoxide hydrolase in aflatoxin-associated hepatocellular carcinoma. Cancer Epidemiol Biomarkers Prev, 10, 785-91.
  79. Timofeeva M, Kropp S, Sauter W, et al (2010). Genetic polymorphisms of MPO, GSTT1, GSTM1, GSTP1, EPHX1 and NQO1 as risk factors of early-onset lung cancer. Int J Cancer, 127, 1547-61. https://doi.org/10.1002/ijc.25175
  80. To-Figueras J,Gene M, Gomez-Catalan J, et al (1997). Polymorphisms and lung cancer risk among Northwestern Mediterraneans. Carcinogenesis, 18, 1529-33. https://doi.org/10.1093/carcin/18.8.1529
  81. Uhm YK, Yoon SH, Kang IJ, et al (2007). Association of glutathione S-transferase gene polymorphisms (GSTM1 and GSTT1) of vitiligo in Korean population. Life Sci, 81, 223-7. https://doi.org/10.1016/j.lfs.2007.05.006
  82. Xu S, Wang Y, Roe B, Pearson WR (1998). Characterization of the human class Mu glutathione S-transferase gene cluster and the GSTM1 deletion. J Biol Chem, 273, 3517-27. https://doi.org/10.1074/jbc.273.6.3517
  83. Yalin S, Hatungil R, Tamer L (2007). Glutathione S-transferase gene polymorphisms in Turkish patients with diabetes mellitus. Cell Biochem Funct, 25, 509-13. https://doi.org/10.1002/cbf.1339
  84. Yan H, Sun X, Den W, Fan X, Liu T (2006). GSTP1, GSTM1, and GSTT1 polymorphism in Tibetan mountaineers. Biol Sport, 23, 303-11.
  85. Zhang AP, Liu BH, Wang L, et al (2011). Glutathione S-transferase gene polymorphisms and risk of gastric cancer in a Chinese population. Asian Pac J Cancer Prev, 12, 3421-5.

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