The spectrum of TP53 mutations in Rwandan patients with gastric cancer.
TP53
Africa
Gastric cancer
Genetic analysis
Mutation pattern
Mutation spectrum
Rwanda
Journal
Genes and environment : the official journal of the Japanese Environmental Mutagen Society
ISSN: 1880-7046
Titre abrégé: Genes Environ
Pays: England
ID NLM: 101285347
Informations de publication
Date de publication:
08 Mar 2024
08 Mar 2024
Historique:
received:
23
11
2023
accepted:
18
02
2024
medline:
9
3
2024
pubmed:
9
3
2024
entrez:
8
3
2024
Statut:
epublish
Résumé
Gastric cancer is the sixth most frequently diagnosed cancer and third in causing cancer-related death globally. The most frequently mutated gene in human cancers is TP53, which plays a pivotal role in cancer initiation and progression. In Africa, particularly in Rwanda, data on TP53 mutations are lacking. Therefore, this study intended to obtain TP53 mutation status in Rwandan patients with gastric cancer. Formalin-fixed paraffin-embedded tissue blocks of 95 Rwandan patients with histopathologically proven gastric carcinoma were obtained from the University Teaching Hospital of Kigali. After DNA extraction, all coding regions of the TP53 gene and the exon-intron boundary region of TP53 were sequenced using the Sanger sequencing. Mutated TP53 were observed in 24 (25.3%) of the 95 cases, and a total of 29 mutations were identified. These TP53 mutations were distributed between exon 4 and 8 and most of them were missense mutations (19/29; 65.5%). Immunohistochemical analysis for TP53 revealed that most of the TP53 missense mutations were associated with TP53 protein accumulation. Among the 29 mutations, one was novel (c.459_477delCGGCACCCGCGTCCGCGCC). This 19-bp deletion mutation in exon 5 caused the production of truncated TP53 protein (p.G154Wfs*10). Regarding the spectrum of TP53 mutations, G:C > A:T at CpG sites was the most prevalent (10/29; 34.5%) and G:C > T:A was the second most prevalent (7/29; 24.1%). Interestingly, when the mutation spectrum of TP53 was compared to three previous TP53 mutational studies on non-Rwandan patients with gastric cancer, G:C > T:A mutations were significantly more frequent in this study than in our previous study (p = 0.013), the TCGA database (p = 0.017), and a previous study on patients from Hong Kong (p = 0.006). Even after correcting for false discovery, statistical significance was observed. Our results suggested that TP53 G:C > T:A transversion mutation in Rwandan patients with gastric cancer is more frequent than in non-Rwandan patients with gastric cancer, indicating at an alternative etiological and carcinogenic progression of gastric cancer in Rwanda.
Sections du résumé
BACKGROUND
BACKGROUND
Gastric cancer is the sixth most frequently diagnosed cancer and third in causing cancer-related death globally. The most frequently mutated gene in human cancers is TP53, which plays a pivotal role in cancer initiation and progression. In Africa, particularly in Rwanda, data on TP53 mutations are lacking. Therefore, this study intended to obtain TP53 mutation status in Rwandan patients with gastric cancer.
RESULTS
RESULTS
Formalin-fixed paraffin-embedded tissue blocks of 95 Rwandan patients with histopathologically proven gastric carcinoma were obtained from the University Teaching Hospital of Kigali. After DNA extraction, all coding regions of the TP53 gene and the exon-intron boundary region of TP53 were sequenced using the Sanger sequencing. Mutated TP53 were observed in 24 (25.3%) of the 95 cases, and a total of 29 mutations were identified. These TP53 mutations were distributed between exon 4 and 8 and most of them were missense mutations (19/29; 65.5%). Immunohistochemical analysis for TP53 revealed that most of the TP53 missense mutations were associated with TP53 protein accumulation. Among the 29 mutations, one was novel (c.459_477delCGGCACCCGCGTCCGCGCC). This 19-bp deletion mutation in exon 5 caused the production of truncated TP53 protein (p.G154Wfs*10). Regarding the spectrum of TP53 mutations, G:C > A:T at CpG sites was the most prevalent (10/29; 34.5%) and G:C > T:A was the second most prevalent (7/29; 24.1%). Interestingly, when the mutation spectrum of TP53 was compared to three previous TP53 mutational studies on non-Rwandan patients with gastric cancer, G:C > T:A mutations were significantly more frequent in this study than in our previous study (p = 0.013), the TCGA database (p = 0.017), and a previous study on patients from Hong Kong (p = 0.006). Even after correcting for false discovery, statistical significance was observed.
CONCLUSIONS
CONCLUSIONS
Our results suggested that TP53 G:C > T:A transversion mutation in Rwandan patients with gastric cancer is more frequent than in non-Rwandan patients with gastric cancer, indicating at an alternative etiological and carcinogenic progression of gastric cancer in Rwanda.
Identifiants
pubmed: 38459566
doi: 10.1186/s41021-024-00302-y
pii: 10.1186/s41021-024-00302-y
doi:
Types de publication
Journal Article
Langues
eng
Pagination
8Subventions
Organisme : Japan Society for the Promotion of Science
ID : 20K07445
Organisme : Smoking Research Foundation
ID : 2019T009
Organisme : HUSM Grant-in-Aid
ID : No number
Informations de copyright
© 2024. The Author(s).
Références
Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, et al. Global Cancer statistics 2020: GLOBOCAN estimates of incidence and Mortality Worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2021;71(3):209–49.
pubmed: 33538338
doi: 10.3322/caac.21660
Farmer P, Frenk J, Knaul FM, Shulman LN, Alleyne G, Armstrong L, et al. Expansion of cancer care and control in countries of low and middle income: a call to action. Lancet. 2010;376(9747):1186–93.
pubmed: 20709386
doi: 10.1016/S0140-6736(10)61152-X
Asombang AW, Rahman R, Ibdah JA. Gastric cancer in Africa: current management and outcomes. World J Gastroenterol. 2014;20(14):3875–9.
pubmed: 24833842
pmcid: 3983443
doi: 10.3748/wjg.v20.i14.3875
Mei Y, Liang D, Wang T, Yu D. Gaining insights into relevance across cancers based on mutation features of TP53 gene. Biochem Biophys Rep. 2021;28(October):101165.
pubmed: 34786492
pmcid: 8579115
Imai S, Ooki T, Murata-Kamiya N, Komura D, Tahmina K, Wu W et al. Helicobacter pylori CagA elicits BRCAness to induce genome instability that may underlie bacterial gastric carcinogenesis. Cell Host Microbe. 2021;29(6).
Mansuri N, Birkman EM, Heuser VD, Lintunen M, Ålgars A, Sundström J et al. Association of tumor-infiltrating T lymphocytes with intestinal-type gastric cancer molecular subtypes and outcome. Virchows Arch. 2021;478(4).
Rahman MM, Sarker MAK, Hossain MM, Alam MS, Islam MM, Shirin L et al. Association of p53 gene mutation with Helicobacter pylori infection in gastric Cancer patients and its correlation with clinicopathological and environmental factors. World J Oncol. 2019;10(1).
Fedriga R, Calistri D, Nanni O, Cortesi L, Saragoni L, Amadori D. Relation between food habits and p53 mutational spectrum in gastric cancer patients. Int J Oncol. 2000;17(1):127–33.
pubmed: 10853029
Alexandrov LB, Nik-Zainal S, Wedge DC, Aparicio SAJR, Behjati S, Biankin AV, et al. Signatures of mutational processes in human cancer. Nature. 2013;500(7463):415–21.
pubmed: 23945592
pmcid: 3776390
doi: 10.1038/nature12477
Alexandrov LB, Stratton MR. Mutational signatures: the patterns of somatic mutations hidden in cancer genomes. Curr Opin Genet Dev. 2014;24(1):52–60.
pubmed: 24657537
pmcid: 3990474
doi: 10.1016/j.gde.2013.11.014
Degasperi A, Zou X, Amarante TD, Martinez-Martinez A, Koh GCC, Dias JML et al. Substitution mutational signatures in whole-genome–sequenced cancers in the UK population. Sci (80-). 2022;376(6591).
Hainaut P, Pfeifer GP. Somatic TP53 mutations in the era of genome sequencing. Cold Spring Harb Perspect Med. 2015;6(a026179):1–22.
Helleday T, Eshtad S, Nik-Zainal S. Mechanisms underlying mutational signatures in human cancers. Nat Rev Genet. 2014;15(9):585–98.
pubmed: 24981601
pmcid: 6044419
doi: 10.1038/nrg3729
GCO. Rwanda Fact Sheet. Vol. 237. 2021.
Kalisa E, Kuuire V, Adams M. A preliminary investigation comparing high-volume and low-volume air samplers for measurement of PAHs, NPAHs and airborne bacterial communities in atmospheric particulate matter. Environ Sci Atmos. 2022;2(5).
Nishimwe K, Bowers E, Ayabagabo J, de Habimana D, Mutiga R, Maier S. D. Assessment of aflatoxin and fumonisin contamination and associated risk factors in feed and feed ingredients in Rwanda. Toxins (Basel). 2019;11(5).
Pilati C, Shinde J, Alexandrov LB, Assié G, André T, Hélias-Rodzewicz Z et al. Mutational signature analysis identifies MUTYH deficiency in colorectal cancers and adrenocortical carcinomas. J Pathol. 2017;242(1).
Smetana J, Brož P. National Genome Initiatives in Europe and the United Kingdom in the era of whole-genome sequencing: a Comprehensive Review. Genes (Basel). 2022;13(3):1–12.
doi: 10.3390/genes13030556
Halldorsson BV, Eggertsson HP, Moore KHS, Hauswedell H, Eiriksson O, Ulfarsson MO, et al. The sequences of 150,119 genomes in the UK Biobank. Nature. 2022;607(7920):732–40.
pubmed: 35859178
pmcid: 9329122
doi: 10.1038/s41586-022-04965-x
Auton A, Abecasis GR, Altshuler DM, Durbin RM, Bentley DR, Chakravarti A, et al. A global reference for human genetic variation. Nature. 2015;526(7571):68–74.
pubmed: 26432245
doi: 10.1038/nature15393
Wall JD, Stawiski EW, Ratan A, Kim HL, Kim C, Gupta R, et al. The GenomeAsia 100K Project enables genetic discoveries across Asia. Nature. 2019;576(7785):106–11.
doi: 10.1038/s41586-019-1793-z
van Beek EJAH, Hernandez JM, Goldman DA, Davis JL, McLaughlin K, Ripley RT, et al. Rates of TP53 mutation are significantly elevated in African American patients with gastric Cancer. Ann Surg Oncol. 2018;25(7):2027–33.
pubmed: 29725898
pmcid: 6644702
doi: 10.1245/s10434-018-6502-x
Zhang C, Hansen MEB, Tishkoff SA. Advances in integrative African genomics. Trends Genet. 2022;38(2):152–68.
pubmed: 34740451
doi: 10.1016/j.tig.2021.09.013
Rotimi SO, Rotimi OA, Salhia B. A review of Cancer Genetics and Genomics studies in Africa. Front Oncol. 2021;10(February):1–24.
Uyisenga JP, Segers K, Lumaka AZ, Mugenzi P, Fasquelle C, Boujemila B, et al. Screening of germline mutations in young Rwandan patients with breast cancers. Mol Genet Genomic Med. 2020;8(11):1–10.
doi: 10.1002/mgg3.1500
Habyarimana T, Attaleb M, Mugenzi P, Mazarati JB, Bakri Y, El Mzibri M. CHEK2 germ line mutations are lacking among familial and sporadic breast cancer patients in Rwanda. Asian Pac J Cancer Prev. 2018;19(2):375–9.
pubmed: 29479983
pmcid: 5980922
Manirakiza F, Rutaganda E, Yamada H, Iwashita Y, Rugwizangoga B, Seminega B, et al. Clinicopathological characteristics and Mutational Landscape of APC, HOXB13, and KRAS among Rwandan patients with colorectal Cancer. Curr Issues Mol Biol. 2023;45(5):4359–74.
pubmed: 37232746
pmcid: 10217012
doi: 10.3390/cimb45050277
Mpunga T, Chantal Umulisa M, Tenet V, Rugwizangoga B, Milner DA, Munyanshongore C, et al. Human papillomavirus genotypes in cervical and other HPV-related anogenital cancer in Rwanda, according to HIV status. Int J Cancer. 2020;146(6):1514–22.
pubmed: 31173641
doi: 10.1002/ijc.32491
Mukanyangezi MF, Sengpiel V, Manzi O, Tobin G, Rulisa S, Bienvenu E, et al. Screening for human papillomavirus, cervical cytological abnormalities and associated risk factors in HIV-positive and HIV-negative women in Rwanda. HIV Med. 2018;19(2):152–66.
pubmed: 29210158
doi: 10.1111/hiv.12564
Laurén P. The two histological main types of gastric carcinoma: diffuse and so-called intestinal-type carcinoma. Acta Pathol Microbiol Scand. 1965;64(1):31–49.
pubmed: 14320675
doi: 10.1111/apm.1965.64.1.31
WHO Classification of Tumours Editorial Board; Digestive System Tumours. 5th ed. Lyon (France): International Agency for Research on Cancer.; 2019. 85–95 p.
Suzuki A, Katoh H, Komura D, Kakiuchi M, Tagashira A, Yamamoto S, et al. Defined lifestyle and germline factors predispose Asian populations to gastric cancer. Sci Adv. 2020;6(19):1–14.
doi: 10.1126/sciadv.aav9778
Natsume H, Szczepaniak K, Yamada H, Iwashita Y, Gędek M, Šuto J, et al. Non-CpG sites preference in G:C > A:T transition of TP53 in gastric cancer of Eastern Europe (Poland, Romania and Hungary) compared to east Asian countries (China and Japan). Genes Environ. 2023;45(1):1.
pubmed: 36600315
pmcid: 9811704
doi: 10.1186/s41021-022-00257-y
Okonechnikov K, Golosova O, Fursov M, Varlamov A, Vaskin Y, Efremov I, et al. Unipro UGENE: a unified bioinformatics toolkit. Bioinformatics. 2012;28(8):1166–7.
pubmed: 22368248
doi: 10.1093/bioinformatics/bts091
den Dunnen JT, Dalgleish R, Maglott DR, Hart RK, Greenblatt MS, Mcgowan-Jordan J, et al. HGVS recommendations for the description of sequence variants: 2016 update. Hum Mutat. 2016;37(6):564–9.
doi: 10.1002/humu.22981
Laboratories KD, Genetics M, Health O, Road P, Molecular C, Children N, et al. Standards and guidelines for the interpretation of sequence variants. Acta Ophthalmol. 2018;96(S261):134–4.
doi: 10.1111/aos.13972_502
National Library of Medicine.National Center for Biotechnology Information [Internet]. National Institute of Health (.gov). Available from: https://www.ncbi.nlm.nih.gov/clinvar/ .
Catalogue of Somatic Mutations. In Cancer [Internet]. Wellcome Sangaer Institute. [cited 2023 May 7]. Available from: https://cancer.sanger.ac.uk/cosmic/gene/analysis?ln=TP53 .
Lefter M, Vis JK, Vermaat M, den Dunnen JT, Taschner PEM, Laros JFJ. Mutalyzer 2: next generation HGVS nomenclature checker. Bioinformatics. 2021;37:18.
doi: 10.1093/bioinformatics/btab051
Steinhaus R, Proft S, Schuelke M, Schwarz JM, Seelow D, Cooper DN. MutationTaster2021. 2021;49(April):446–51.
Lek M, Karczewski KJ, Minikel EV, Samocha KE, Banks E, Fennell T, et al. Analysis of protein-coding genetic variation in 60,706 humans. Nature. 2016;536(7616):285–91.
pubmed: 27535533
pmcid: 5018207
doi: 10.1038/nature19057
Shinmura K, Goto M, Tao H, Matsuura S, Matsuda T, Sugimura H. Impaired suppressive activities of human MUTYH variant proteins against oxidative mutagenesis. World J Gastroenterol. 2012;18(47):6935–42.
pubmed: 23322991
pmcid: 3531677
doi: 10.3748/wjg.v18.i47.6935
Wang K, Yuen ST, Xu J, Lee SP, Yan HHN, Shi ST, et al. Whole-genome sequencing and comprehensive molecular profiling identify new driver mutations in gastric cancer. Nat Genet. 2014;46(6):573–82.
pubmed: 24816253
doi: 10.1038/ng.2983
Gao J, Aksoy BA, Dogrusoz U, Dresdner G, Gross B, Sumer SO et al. Integrative analysis of complex cancer genomics and clinical profiles using the cBioPortal. Sci Signal. 2013;6(269).
Degasperi A, Amarante TD, Czarnecki J, Shooter S, Zou X, Glodzik D, et al. A practical framework and online tool for mutational signature analyses show intertissue variation and driver dependencies. Nat Cancer. 2020;1(2):249–63.
pubmed: 32118208
pmcid: 7048622
doi: 10.1038/s43018-020-0027-5
Simes RJ. A improved Bonferroni procedure for multiple tests of significance. Biometrika. 1986;73(3):751–4.
doi: 10.1093/biomet/73.3.751
R Core Team. A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. Vienna, Austria; 2023.
Hervé M. Testing and plotting procedures for Biostatistics RVAideMemoire’. Cran. 2023.
Nelsen EM, Lochmann-Bailkey A, Grimes IC, Benson ME, Gopal DV, Pfau PR. Low yield and high cost of gastric and duodenal biopsies for investigation of symptoms of Abdominal Pain during Routine Esophagogastroduodenoscopy. Dig Dis Sci. 2017;62(2):418–23.
pubmed: 27995399
doi: 10.1007/s10620-016-4405-x
Kim KM, Ahn AR, Park HS, Jang KY, Moon WS, Kang MJ, et al. Clinical significance of p53 protein expression and TP53 variation status in colorectal cancer. BMC Cancer. 2022;22(1):1–17.
doi: 10.1186/s12885-022-10039-y
Sung YN, Kim D, Kim J. p53 immunostaining pattern is a useful surrogate marker for TP53 gene mutations. Diagn Pathol. 2022;17(1):1–9.
doi: 10.1186/s13000-022-01273-w
Stomach Adenocarcinoma (TCGA., PanCancer Atlas) [Internet]. Available from: http://www.cbioportal.org/datasets .
Beale RCL, Petersen-Mahrt SK, Watt IN, Harris RS, Rada C, Neuberger MS. Comparison of the Differential Context-dependence of DNA deamination by APOBEC enzymes: correlation with mutation Spectra in vivo. J Mol Biol. 2004;337(3).
Li-Chang HH, Kasaian K, Ng Y, Lum A, Kong E, Lim H et al. Retrospective review using targeted deep sequencing reveals mutational differences between gastroesophageal junction and gastric carcinomas. BMC Cancer. 2015;15(1).
Hwang HJ, Nam SK, Park H, Park Y, Koh J, Na HY, et al. Prediction of TP53 mutations by p53 immunohistochemistry and their prognostic significance in gastric cancer. J Pathol Transl Med. 2020;54(5):378–86.
pubmed: 32601264
pmcid: 7483024
doi: 10.4132/jptm.2020.06.01
Tahara T, Shibata T, Okamoto Y, Yamazaki J, Kawamura T, Horiguchi N, et al. Mutation spectrum of TP53 gene predicts clinicopathological features and survival of gastric cancer. Oncotarget. 2016;7(27):42252–60.
pubmed: 27323394
pmcid: 5173132
doi: 10.18632/oncotarget.9770
Saxena A, Shukla SK, Prasad KN, Ghoshal UC. Analysis of p53, K-ras gene mutation & Helicobacter pylori infection in patients with gastric cancer & peptic ulcer disease at a tertiary care hospital in north India. Indian J Med Res. 2012;136(4):664–70.
pubmed: 23168708
pmcid: 3516035
Palacio-Rúa KA, Isaza-Jiménez LF, Ahumada-Rodríguez E, Ceballos-García H, Muñetón-Peña CM. Genetic analysis in APC, KRAS, and TP53 in patients with stomach and colon cancer. Rev Gastroenterol Mex. 2014;79(2):79–89.
pubmed: 24861525
Rotimi SO, Rotimi OA, Salhia B. Authorship patterns in Cancer Genomics publications Across Africa. JCO Glob Oncol. 2021;(7):747–55.
Blanchet A, Bourgmayer A, Kurtz JE, Mellitzer G, Gaiddon C. Isoforms of the p53 family and gastric cancer: a ménage à Trois for an unfinished affair. Cancers (Basel). 2021;13(4):1–45.
doi: 10.3390/cancers13040916
Tolbert D, Fenoglio-Preiser C, Noffsinger A, De Voe G, MacDonald J, Benedetti J, et al. The relation of p53 gene mutations to gastric cancer subsite and phenotype. Cancer Causes Control. 1999;10(3):227–31.
pubmed: 10454068
doi: 10.1023/A:1008899111209
Petljak M, Alexandrov LB. Understanding mutagenesis through delineation of mutational signatures in human cancer. Carcinogenesis. 2016;37(6):531–40.
pubmed: 27207657
doi: 10.1093/carcin/bgw055
Nishimwe K, Wanjuki I, Karangwa C, Darnell R, Harvey J. An initial characterization of aflatoxin B1 contamination of maize sold in the principal retail markets of Kigali, Rwanda. Food Control. 2017;73(Part B):574–80.
doi: 10.1016/j.foodcont.2016.09.006
Meijer N, Kleter G, de Nijs M, Rau ML, Derkx R, van der Fels-Klerx HJ. The aflatoxin situation in Africa: systematic literature review. Compr Rev Food Sci Food Saf. 2021;20(3):2286–304.
pubmed: 33682354
doi: 10.1111/1541-4337.12731
Xue KS, Tang L, Shen CL, Pollock BH, Guerra F, Phillips TD, et al. Increase in aflatoxin exposure in two populations residing in East and West Texas, United States. Int J Hyg Environ Health. 2021;231:113662.
pubmed: 33197706
doi: 10.1016/j.ijheh.2020.113662
Chen T, Liu J, Li Y, Wei S. Burden of Disease Associated with Dietary exposure to aflatoxins in China in 2020. Nutrients. 2022;14(5).
Rubagumya F, Costas-Chavarri A, Manirakiza A, Murenzi G, Uwinkindi F, Ntizimira C et al. State of Cancer Control in Rwanda: past, Present, and Future opportunities. JCO Glob Oncol. 2020;(6).
National Institute of Statistics of Rwanda (NISR). [Rwanda]. Ministry of Health (MOH) [Rwanda] and ICF. 2021. Rwanda Demographic and Health Survey 2019-20 final report. Kigali, Rwanda, and Rockville. Maryland, USA: NISR and ICF; 2021.
Jha P. The hazards of smoking and the benefits of cessation: a critical summation of the epidemiological evidence in high-income countries. Elife. 2020;9.
Hoffman RM, Sanchez R. Lung Cancer Screening. Volume 101. Medical Clinics of North America; 2017.
Manczuk M, Sulkowska U, Łobaszewski J, Koczkodaj P, Przepiórka I, Cedzynska M et al. Time trends in tobacco-attributable cancer mortality in Poland - Direct estimation method. Nowotwory. 2017;67(4).
Gredner T, Mons U, Niedermaier T, Brenner H, Soerjomataram I. Impact of tobacco control policies implementation on future lung cancer incidence in Europe: an international, population-based modeling study. Lancet Reg Heal - Eur. 2021;4:100074.
doi: 10.1016/j.lanepe.2021.100074
Li N, Wu P, Wang Z, Shen Y, Zhang L, Xue F et al. Smoking-related cancer death among men and women in an ageing society (China 2020–2040): a population-based modelling study. Tob Control. 2023;32(2).
Katanoda K, Hirabayashi M, Saito E, Hori M, Abe SK, Matsuda T, et al. Burden of cancer attributable to tobacco smoke in Japan in 2015. GHM Open. 2021;1(2):202101013.
doi: 10.35772/ghmo.2021.01013
Hsu TM, Zhang YJ, Santella RM. Immunoperoxidase quantitation of 4-aminobiphenyl- and polycyclic aromatic hydrocarbon-DNA adducts in exfoliated oral and urothelial cells of smokers and nonsmokers. Cancer Epidemiol Biomarkers Prev. 1997;6(3).
Talaska G, Underwood P, Maier A, Lewtas J, Rothman N, Jaeger M. Polycyclic aromatic hydrocarbons (PAHs), nitro-PAHs and related environmental compounds: Biological markers of exposure and effects. In: Environmental Health Perspectives. 1996.
Kucab JE, Zou X, Morganella S, Joel M, Nanda AS, Nagy E, et al. A compendium of Mutational signatures of Environmental agents. Cell. 2019;177(4):821–836e16.
pubmed: 30982602
pmcid: 6506336
doi: 10.1016/j.cell.2019.03.001
Kasai H, Kawai K. Free radical-mediated acetaldehyde formation by model reactions of dietary components: effects of meat, wine, cooking oil and coffee. Genes Environ. 2021;43(1).
Ohno M. Spontaneous de novo germline mutations in humans and mice: rates, spectra, causes and consequences. Genes Genet Syst. 2019;94(1):13–22.
pubmed: 30381610
doi: 10.1266/ggs.18-00015
Shimizu T, Marusawa H, Matsumoto Y, Inuzuka T, Ikeda A, Fujii Y, et al. Accumulation of somatic mutations in TP53 in gastric epithelium with helicobacter pylori infection. Gastroenterology. 2014;147(2):407–417e3.
pubmed: 24786892
doi: 10.1053/j.gastro.2014.04.036
Oue N, Shigeishi H, Kuniyasu H, Yokozaki H, Kuraoka K, Ito R, et al. Promoter hypermethylation of MGMT is associated with protein loss in gastric carcinoma. Int J Cancer. 2001;93(6):805–9.
pubmed: 11519041
doi: 10.1002/ijc.1403
Vidal B, Parra M, Jardí M, Saito S, Appella E, Muñoz-Cánoves P. The alkylating carcinogen N-methyl-N′-nitro-N-nitrosoguanidine activates the plasminogen activator inhibitor-1 gene through sequential phosphorylation of p53 by ATM and ATR kinases. Thromb Haemost. 2005;93(3):584–91.
pubmed: 15735814
doi: 10.1160/TH04-10-0644
Kim WJ, Beardsley DI, Adamson AW, Brown KD. The monofunctional alkylating agent N-methyl-N′-nitro-N- nitrosoguanidine triggers apoptosis through p53-dependent and -independent pathways. Toxicol Appl Pharmacol. 2005;202(1):84–98.
pubmed: 15589979
doi: 10.1016/j.taap.2004.06.009
Fang J, Yang Y, Xie L, Yin W. Immunological role of TP53 somatic mutation classification in human cancers. J Oncol. 2023;2023:1–15.
doi: 10.1155/2023/1904309
Na K, Sung JY, Kim HS. TP53 mutation status of Tubo-ovarian and peritoneal high-grade Serous Carcinoma with a wild-type p53 immunostaining pattern. Anticancer Res. 2017;37(12):6697–703.
pubmed: 29187446
Garziera M, Cecchin E, Canzonieri V, Sorio R, Giorda G, Scalone S, et al. Identification of novel somatic TP53 mutations in patients with high-grade serous ovarian cancer (HGSOC) using next-generation sequencing (NGS). Int J Mol Sci. 2018;19(5):1510.
pubmed: 29783665
pmcid: 5983728
doi: 10.3390/ijms19051510
Tong DR, Zhou W, Katz C, Regunath K, Venkatesh D, Ihuegbu C, et al. P53 frameshift mutations couple loss-of-function with unique neomorphic activities. Mol Cancer Res. 2021;19(9):1522–33.
pubmed: 34045312
pmcid: 8419077
doi: 10.1158/1541-7786.MCR-20-0691
Tang YL, Gan RL, Dong BH, Jiang RC, Tang RJ. Detection and location of Helicobacter pylori in human gastric carcinomas. World J Gastroenterol. 2005;11(9):1387–91.
pubmed: 15761982
pmcid: 4250691
doi: 10.3748/wjg.v11.i9.1387
Wang JL, Fu YD, Gao YH, Li XP, Xiong Q, Li R et al. Unique characteristics of G719X and S768I compound double mutations of epidermal growth factor receptor (EGFR) gene in lung cancer of coal-producing areas of East Yunnan in Southwestern China. Genes Environ. 2022;44(1).
Manirakiza F, Yamada H, Iwashita Y, Ishino K, Ishikawa R, Kovacs Z et al. TP53 mutations in Romanian patients with colorectal cancer. Genes Environ. 2023;45(1).