The role of the ALKBH5 RNA demethylase in invasive breast cancer.

Breast cancer Epitranscriptomics N6-methyladenosine Prognosis m6A

Journal

Discover oncology
ISSN: 2730-6011
Titre abrégé: Discov Oncol
Pays: United States
ID NLM: 101775142

Informations de publication

Date de publication:
11 Aug 2024
Historique:
received: 17 01 2024
accepted: 30 07 2024
medline: 11 8 2024
pubmed: 11 8 2024
entrez: 11 8 2024
Statut: epublish

Résumé

N6-methyladenosine (m Publicly available data were used to investigate ALKBH5 mRNA alterations, prognostic significance, and association with clinical parameters at the genomic and transcriptomic level. Differentially expressed genes (DEGs) and enriched pathways with low or high ALKBH5 expression were investigated. Immunohistochemistry (IHC) was used to assess ALKBH5 protein expression in a large well-characterised BC series (n = 1327) to determine the clinical significance and association of ALKBH5 expression. Reduced ALKBH5 mRNA expression was significantly associated with poor prognosis and unfavourable clinical parameters. ALKBH5 gene harboured few mutations and/or copy number alternations, but low ALKBH5 mRNA expression was seen. Patients with low ALKBH5 mRNA expression had a number of differentially expressed genes and enriched pathways, including the cytokine-cytokine receptor interaction pathway. Low ALKBH5 protein expression was significantly associated with unfavourable clinical parameters associated with tumour progression including larger tumour size and worse Nottingham Prognostic Index group. This study implicates ALKBH5 in BC and highlights the need for further functional studies to decipher the role of ALKBH5 and RNA m

Sections du résumé

BACKGROUND BACKGROUND
N6-methyladenosine (m
METHODS METHODS
Publicly available data were used to investigate ALKBH5 mRNA alterations, prognostic significance, and association with clinical parameters at the genomic and transcriptomic level. Differentially expressed genes (DEGs) and enriched pathways with low or high ALKBH5 expression were investigated. Immunohistochemistry (IHC) was used to assess ALKBH5 protein expression in a large well-characterised BC series (n = 1327) to determine the clinical significance and association of ALKBH5 expression.
RESULTS RESULTS
Reduced ALKBH5 mRNA expression was significantly associated with poor prognosis and unfavourable clinical parameters. ALKBH5 gene harboured few mutations and/or copy number alternations, but low ALKBH5 mRNA expression was seen. Patients with low ALKBH5 mRNA expression had a number of differentially expressed genes and enriched pathways, including the cytokine-cytokine receptor interaction pathway. Low ALKBH5 protein expression was significantly associated with unfavourable clinical parameters associated with tumour progression including larger tumour size and worse Nottingham Prognostic Index group.
CONCLUSION CONCLUSIONS
This study implicates ALKBH5 in BC and highlights the need for further functional studies to decipher the role of ALKBH5 and RNA m

Identifiants

pubmed: 39127986
doi: 10.1007/s12672-024-01205-8
pii: 10.1007/s12672-024-01205-8
doi:

Types de publication

Journal Article

Langues

eng

Pagination

343

Subventions

Organisme : BBSRC Doctoral Training Program
ID : (BB/I024291/1)
Organisme : British Council ResearcherLinks program
ID : RLWK10-458041157

Informations de copyright

© 2024. The Author(s).

Références

Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, Bray F. 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. https://doi.org/10.3322/caac.21660 .
doi: 10.3322/caac.21660 pubmed: 33538338
Polyak K. Heterogeneity in breast cancer. J Clin Invest. 2011;121(10):3786–8. https://doi.org/10.1172/JCI60534 .
doi: 10.1172/JCI60534 pubmed: 21965334 pmcid: 3195489
Yang Y, Hsu PJ, Chen Y-S, Yang Y-G. Dynamic transcriptomic m6A decoration: writers, erasers, readers and functions in RNA metabolism. Cell Res. 2018;28(6):616–24. https://doi.org/10.1038/s41422-018-0040-8 .
doi: 10.1038/s41422-018-0040-8 pubmed: 29789545 pmcid: 5993786
Cao G, Li H-B, Yin Z, Flavell RA. Recent advances in dynamic m(6)A RNA modification. Open Biol. 2016;6(4): 160003. https://doi.org/10.1098/rsob.160003 .
doi: 10.1098/rsob.160003 pubmed: 27249342 pmcid: 4852458
Jia G, Fu Y, Zhao X, Dai Q, Zheng G, Yang Y, Yi C, Lindahl T, Pan T, Yang Y-G, He C. N6-Methyladenosine in nuclear RNA is a major substrate of the obesity-associated FTO. Nat Chem Biol. 2011;7(12):885–7. https://doi.org/10.1038/nchembio.687 .
doi: 10.1038/nchembio.687 pubmed: 22002720 pmcid: 3218240
Zheng G, Dahl JA, Niu Y, Fedorcsak P, Huang CM, Li CJ, Vagbo CB, Shi Y, Wang WL, Song SH, Lu Z, Bosmans RP, Dai Q, Hao YJ, Yang X, Zhao WM, Tong WM, Wang XJ, Bogdan F, Furu K, Fu Y, Jia G, Zhao X, Liu J, Krokan HE, Klungland A, Yang YG, He C. ALKBH5 is a mammalian RNA demethylase that impacts RNA metabolism and mouse fertility. Mol Cell. 2013;49(1):18–29. https://doi.org/10.1016/j.molcel.2012.10.015 .
doi: 10.1016/j.molcel.2012.10.015 pubmed: 23177736
Wang X, Lu Z, Gomez A, Hon GC, Yue Y, Han D, Fu Y, Parisien M, Dai Q, Jia G, Ren B, Pan T, He C. N6-methyladenosine-dependent regulation of messenger RNA stability. Nature. 2014;505(7481):117–20. https://doi.org/10.1038/nature12730 .
doi: 10.1038/nature12730 pubmed: 24284625
Wang X, Zhao BS, Roundtree IA, Lu Z, Han D, Ma H, Weng X, Chen K, Shi H, He C. N(6)-methyladenosine modulates messenger RNA translation efficiency. Cell. 2015;161(6):1388–99. https://doi.org/10.1016/j.cell.2015.05.014 .
doi: 10.1016/j.cell.2015.05.014 pubmed: 26046440 pmcid: 4825696
Adhikari S, Xiao W, Zhao YL, Yang YG. m(6)A: signaling for mRNA splicing. RNA Biol. 2016;13(9):756–9. https://doi.org/10.1080/15476286.2016.1201628 .
doi: 10.1080/15476286.2016.1201628 pubmed: 27351695 pmcid: 5013988
Haussmann IU, Bodi Z, Sanchez-Moran E, Mongan NP, Archer N, Fray RG, Soller M. m(6)A potentiates Sxl alternative pre-mRNA splicing for robust Drosophila sex determination. Nature. 2016;540(7632):301–4. https://doi.org/10.1038/nature20577 .
doi: 10.1038/nature20577 pubmed: 27919081
Huang H, Weng H, Sun W, Qin X, Shi H, Wu H, Zhao BS, Mesquita A, Liu C, Yuan CL, Hu YC, Huttelmaier S, Skibbe JR, Su R, Deng X, Dong L, Sun M, Li C, Nachtergaele S, Wang Y, Hu C, Ferchen K, Greis KD, Jiang X, Wei M, Qu L, Guan JL, He C, Yang J, Chen J. Recognition of RNA N(6)-methyladenosine by IGF2BP proteins enhances mRNA stability and translation. Nat Cell Biol. 2018;20(3):285–95. https://doi.org/10.1038/s41556-018-0045-z .
doi: 10.1038/s41556-018-0045-z pubmed: 29476152 pmcid: 5826585
Li Y, Xiao J, Bai J, Tian Y, Qu Y, Chen X, Wang Q, Li X, Zhang Y, Xu J. Molecular characterization and clinical relevance of m(6)A regulators across 33 cancer types. Mol Cancer. 2019;18:137.
doi: 10.1186/s12943-019-1066-3 pubmed: 31521193 pmcid: 6744659
Li Z, Weng H, Su R, Weng X, Zuo Z, Li C, Huang H, Nachtergaele S, Dong L, Hu C, Qin X, Tang L, Wang Y, Hong GM, Wang X, Chen P, Gurbuxani S, Arnovitz S, Li Y, Li S, Strong J, Neilly MB, Larson RA, Jiang X, Zhang P, Jin J, He C, Chen J. FTO plays an oncogenic role in acute myeloid leukemia as a N(6)-methyladenosine RNA demethylase. Cancer Cell. 2017;31(1):127–41. https://doi.org/10.1016/j.ccell.2016.11.017 .
doi: 10.1016/j.ccell.2016.11.017 pubmed: 28017614
Zhang S, Zhao BS, Zhou A, Lin K, Zheng S, Lu Z, Chen Y, Sulman EP, Xie K, Bogler O, Majumder S, He C, Huang S. m(6)A demethylase ALKBH5 maintains tumorigenicity of glioblastoma stem-like cells by sustaining FOXM1 expression and cell proliferation program. Cancer Cell. 2017;31(4):591-606.e6. https://doi.org/10.1016/j.ccell.2017.02.013 .
doi: 10.1016/j.ccell.2017.02.013 pubmed: 28344040 pmcid: 5427719
Li J, Han Y, Zhang H, Qian Z, Jia W, Gao Y, Zheng H, Li B. The m6A demethylase FTO promotes the growth of lung cancer cells by regulating the m6A level of USP7 mRNA. Biochem Biophys Res Commun. 2019;512(3):479–85. https://doi.org/10.1016/j.bbrc.2019.03.093 .
doi: 10.1016/j.bbrc.2019.03.093 pubmed: 30905413
Zhu H, Gan X, Jiang X, Diao S, Wu H, Hu J. ALKBH5 inhibited autophagy of epithelial ovarian cancer through miR-7 and BCL-2. J Exp Clin Cancer Res. 2019;38(1):163. https://doi.org/10.1186/s13046-019-1159-2 .
doi: 10.1186/s13046-019-1159-2 pubmed: 30987661 pmcid: 6463658
Li J, Meng S, Xu M, Wang S, He L, Xu X, Wang X, Xie L. Downregulation of N(6)-methyladenosine binding YTHDF2 protein mediated by miR-493-3p suppresses prostate cancer by elevating N(6)-methyladenosine levels. Oncotarget. 2018;9(3):3752–64. https://doi.org/10.18632/oncotarget.23365 .
doi: 10.18632/oncotarget.23365 pubmed: 29423080
Tang B, Yang Y, Kang M, Wang Y, Bi Y, He S, Shimamoto F. m(6)A demethylase ALKBH5 inhibits pancreatic cancer tumorigenesis by decreasing WIF-1 RNA methylation and mediating Wnt signaling. Mol Cancer. 2020;19(1):3. https://doi.org/10.1186/s12943-019-1128-6 .
doi: 10.1186/s12943-019-1128-6 pubmed: 31906946 pmcid: 6943907
Chen M, Wei L, Law CT, Tsang FH, Shen J, Cheng CL, Tsang LH, Ho DW, Chiu DK, Lee JM, Wong CC, Ng IO, Wong CM. RNA N6-methyladenosine methyltransferase-like 3 promotes liver cancer progression through YTHDF2-dependent posttranscriptional silencing of SOCS2. Hepatology. 2018;67(6):2254–70. https://doi.org/10.1002/hep.29683 .
doi: 10.1002/hep.29683 pubmed: 29171881
Cheng M, Sheng L, Gao Q, Xiong Q, Zhang H, Wu M, Liang Y, Zhu F, Zhang Y, Zhang X, Yuan Q, Li Y. The m(6)A methyltransferase METTL3 promotes bladder cancer progression via AFF4/NF-κB/MYC signaling network. Oncogene. 2019;38(19):3667–80. https://doi.org/10.1038/s41388-019-0683-z .
doi: 10.1038/s41388-019-0683-z pubmed: 30659266
Cai X, Wang X, Cao C, Gao Y, Zhang S, Yang Z, Liu Y, Zhang X, Zhang W, Ye L. HBXIP-elevated methyltransferase METTL3 promotes the progression of breast cancer via inhibiting tumor suppressor let-7g. Cancer Lett. 2018;415:11–9. https://doi.org/10.1016/j.canlet.2017.11.018 .
doi: 10.1016/j.canlet.2017.11.018 pubmed: 29174803
Niu Y, Lin Z, Wan A, Chen H, Liang H, Sun L, Wang Y, Li X, Xiong XF, Wei B, Wu X, Wan G. RNA N6-methyladenosine demethylase FTO promotes breast tumor progression through inhibiting BNIP3. Mol Cancer. 2019;18(1):46. https://doi.org/10.1186/s12943-019-1004-4 .
doi: 10.1186/s12943-019-1004-4 pubmed: 30922314 pmcid: 6437932
Liu L, Liu X, Dong Z, Li J, Yu Y, Chen X, Ren F, Cui G, Sun R. N6-methyladenosine-related genomic targets are altered in breast cancer tissue and associated with poor survival. J Cancer. 2019;10(22):5447–59. https://doi.org/10.7150/jca.35053 .
doi: 10.7150/jca.35053 pubmed: 31632489 pmcid: 6775703
Shi Y, Zheng C, Jin Y, Bao B, Wang D, Hou K, Feng J, Tang S, Qu X, Liu Y, Che X, Teng Y. Reduced expression of METTL3 promotes metastasis of triple-negative breast cancer by m6A methylation-mediated COL3A1 up-regulation. Front Oncol. 2020;10:1126. https://doi.org/10.3389/fonc.2020.01126 .
doi: 10.3389/fonc.2020.01126 pubmed: 32766145 pmcid: 7381173
Sun T, Wu Z, Wang X, Wang Y, Hu X, Qin W, Lu S, Xu D, Wu Y, Chen Q, Ding X, Guo H, Li Y, Fu B, Yao W, Wei M, Wu H. LNC942 promoting METTL14-mediated m(6)A methylation in breast cancer cell proliferation and progression. Oncogene. 2020;39(31):5358–72. https://doi.org/10.1038/s41388-020-1338-9 .
doi: 10.1038/s41388-020-1338-9 pubmed: 32576970
Zheng F, Du F, Qian H, Zhao J, Wang X, Yue J, Hu N, Si Y, Xu B, Yuan P. Expression and clinical prognostic value of m6A RNA methylation modification in breast cancer. Biomark Res. 2021;9(1):28. https://doi.org/10.1186/s40364-021-00285-w .
doi: 10.1186/s40364-021-00285-w pubmed: 33926554 pmcid: 8082898
Wang S, Zou X, Chen Y, Cho WC, Zhou X. Effect of N6-methyladenosine regulators on progression and prognosis of triple-negative breast cancer. Front Genet. 2020;11: 580036. https://doi.org/10.3389/fgene.2020.580036 .
doi: 10.3389/fgene.2020.580036 pubmed: 33584787
Zhang C, Samanta D, Lu H, Bullen JW, Zhang H, Chen I, He X, Semenza GL. Hypoxia induces the breast cancer stem cell phenotype by HIF-dependent and ALKBH5-mediated m(6)A-demethylation of NANOG mRNA. Proc Natl Acad Sci USA. 2016;113(14):E2047–56. https://doi.org/10.1073/pnas.1602883113 .
doi: 10.1073/pnas.1602883113 pubmed: 27001847 pmcid: 4833258
Zhang C, Zhi WI, Lu H, Samanta D, Chen I, Gabrielson E, Semenza GL. Hypoxia-inducible factors regulate pluripotency factor expression by ZNF217- and ALKBH5-mediated modulation of RNA methylation in breast cancer cells. Oncotarget. 2016;7(40):64527–42. https://doi.org/10.18632/oncotarget.11743 .
doi: 10.18632/oncotarget.11743 pubmed: 27590511 pmcid: 5323097
Fry NJ, Law BA, Ilkayeva OR, Carraway KR, Holley CL, Mansfield KD. N(6)-methyladenosine contributes to cellular phenotype in a genetically-defined model of breast cancer progression. Oncotarget. 2018;9(58):31231–43. https://doi.org/10.18632/oncotarget.25782 .
doi: 10.18632/oncotarget.25782 pubmed: 30131850 pmcid: 6101291
Wu L, Wu D, Ning J, Liu W, Zhang D. Changes of N6-methyladenosine modulators promote breast cancer progression. BMC Cancer. 2019;19(1):326. https://doi.org/10.1186/s12885-019-5538-z .
doi: 10.1186/s12885-019-5538-z pubmed: 30953473 pmcid: 6451293
Panneerdoss S, Eedunuri VK, Yadav P, Timilsina S, Rajamanickam S, Viswanadhapalli S, Abdelfattah N, Onyeagucha BC, Cui X, Lai Z, Mohammad TA, Gupta YK, Huang TH, Huang Y, Chen Y, Rao MK. Cross-talk among writers, readers, and erasers of m(6)A regulates cancer growth and progression. Sci Adv. 2018;4(10):eaar8263. https://doi.org/10.1126/sciadv.aar8263 .
doi: 10.1126/sciadv.aar8263 pubmed: 30306128 pmcid: 6170038
Nilsson EM, Laursen KB, Whitchurch J, McWilliam A, Ødum N, Persson JL, Heery DM, Gudas LJ, Mongan NP. MiR137 is an androgen regulated repressor of an extended network of transcriptional coregulators. Oncotarget. 2015;6(34):35710–25. https://doi.org/10.18632/oncotarget.5958 .
doi: 10.18632/oncotarget.5958 pubmed: 26461474 pmcid: 4742136
Kariri YA, Joseph C, Kurozumi S, Toss MS, Alsaleem M, Raafat S, Mongan NP, Aleskandarany MA, Green AR, Rakha EA. Prognostic significance of KN motif and ankyrin repeat domains 1 (KANK1) in invasive breast cancer. Breast Cancer Res Treat. 2020;179(2):349–57. https://doi.org/10.1007/s10549-019-05466-8 .
doi: 10.1007/s10549-019-05466-8 pubmed: 31679074
El Ansari R, Craze ML, Miligy I, Diez-Rodriguez M, Nolan CC, Ellis IO, Rakha EA, Green AR. The amino acid transporter SLC7A5 confers a poor prognosis in the highly proliferative breast cancer subtypes and is a key therapeutic target in luminal B tumours. Breast Cancer Res. 2018;20(1):21. https://doi.org/10.1186/s13058-018-0946-6 .
doi: 10.1186/s13058-018-0946-6 pubmed: 29566741 pmcid: 5863851
Abd El-Rehim DM, Ball G, Pinder SE, Rakha E, Paish C, Robertson JF, Macmillan D, Blamey RW, Ellis IO. High-throughput protein expression analysis using tissue microarray technology of a large well-characterised series identifies biologically distinct classes of breast cancer confirming recent cDNA expression analyses. Int J Cancer. 2005;116(3):340–50. https://doi.org/10.1002/ijc.21004 .
doi: 10.1002/ijc.21004 pubmed: 15818618
McCartyJr KS, Miller LS, Cox EB, Konrath J, McCartySr KS. Estrogen receptor analyses. Correlation of biochemical and immunohistochemical methods using monoclonal antireceptor antibodies. Arch Pathol. 1985;109(8):716–21.
Cerami E, Gao J, Dogrusoz U, Gross BE, Sumer SO, Aksoy BA, Jacobsen A, Byrne CJ, Heuer ML, Larsson E, Antipin Y, Reva B, Goldberg AP, Sander C, Schultz N. The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data. Cancer Discov. 2012;2(5):401–4. https://doi.org/10.1158/2159-8290.cd-12-0095 .
doi: 10.1158/2159-8290.cd-12-0095 pubmed: 22588877
Gao J, Aksoy BA, Dogrusoz U, Dresdner G, Gross B, Sumer SO, Sun Y, Jacobsen A, Sinha R, Larsson E, Cerami E, Sander C, Schultz N. Integrative analysis of complex cancer genomics and clinical profiles using the cBioPortal. Sci Signal. 2013;6(269):l1. https://doi.org/10.1126/scisignal.2004088 .
doi: 10.1126/scisignal.2004088
Liu J, Lichtenberg T, Hoadley KA, Poisson LM, Lazar AJ, Cherniack AD, Kovatich AJ, Benz CC, Levine DA, Lee AV, Omberg L, Wolf DM, Shriver CD, Thorsson V, Hu H. An integrated TCGA pan-cancer clinical data resource to drive high-quality survival outcome analytics. Cell. 2018;173(2):400-416.e11. https://doi.org/10.1016/j.cell.2018.02.052 .
doi: 10.1016/j.cell.2018.02.052 pubmed: 29625055 pmcid: 6066282
Curtis C, Shah SP, Chin SF, Turashvili G, Rueda OM, Dunning MJ, Speed D, Lynch AG, Samarajiwa S, Yuan Y, Gräf S, Ha G, Haffari G, Bashashati A, Russell R, McKinney S, Langerød A, Green A, Provenzano E, Wishart G, Pinder S, Watson P, Markowetz F, Murphy L, Ellis I, Purushotham A, Børresen-Dale AL, Brenton JD, Tavaré S, Caldas C, Aparicio S. The genomic and transcriptomic architecture of 2,000 breast tumours reveals novel subgroups. Nature. 2012;486(7403):346–52. https://doi.org/10.1038/nature10983 .
doi: 10.1038/nature10983 pubmed: 22522925 pmcid: 3440846
Pereira B, Chin SF, Rueda OM, Vollan HK, Provenzano E, Bardwell HA, Pugh M, Jones L, Russell R, Sammut SJ, Tsui DW, Liu B, Dawson SJ, Abraham J, Northen H, Peden JF, Mukherjee A, Turashvili G, Green AR, McKinney S, Oloumi A, Shah S, Rosenfeld N, Murphy L, Bentley DR, Ellis IO, Purushotham A, Pinder SE, Borresen-Dale AL, Earl HM, Pharoah PD, Ross MT, Aparicio S, Caldas C. The somatic mutation profiles of 2,433 breast cancers refines their genomic and transcriptomic landscapes. Nat Commun. 2016;7:11479. https://doi.org/10.1038/ncomms11479 .
doi: 10.1038/ncomms11479 pubmed: 27161491 pmcid: 4866047
Györffy B, Lanczky A, Eklund AC, Denkert C, Budczies J, Li Q, Szallasi Z. An online survival analysis tool to rapidly assess the effect of 22,277 genes on breast cancer prognosis using microarray data of 1,809 patients. Breast Cancer Res Treat. 2010;123(3):725–31. https://doi.org/10.1007/s10549-009-0674-9 .
doi: 10.1007/s10549-009-0674-9 pubmed: 20020197
Jézéquel P, Gouraud W, Ben Azzouz F, Guérin-Charbonnel C, Juin PP, Lasla H, Campone M. bc-GenExMiner 4.5: new mining module computes breast cancer differential gene expression analyses. Database (Oxford). 2021. https://doi.org/10.1093/database/baab007 .
doi: 10.1093/database/baab007 pubmed: 33599248 pmcid: 8191702
Goldman MJ, Craft B, Hastie M, Repečka K, McDade F, Kamath A, Banerjee A, Luo Y, Rogers D, Brooks AN, Zhu J, Haussler D. Visualizing and interpreting cancer genomics data via the Xena platform. Nat Biotechnol. 2020;38:675–8.
doi: 10.1038/s41587-020-0546-8 pubmed: 32444850 pmcid: 7386072
Liao Y, Wang J, Jaehnig EJ, Shi Z, Zhang B. WebGestalt 2019: gene set analysis toolkit with revamped UIs and APIs. Nucleic Acids Res. 2019;47(W1):W199-w205. https://doi.org/10.1093/nar/gkz401 .
doi: 10.1093/nar/gkz401 pubmed: 31114916 pmcid: 6602449
Camp RL, Dolled-Filhart M, Rimm DL. X-tile: a new bio-informatics tool for biomarker assessment and outcome-based cut-point optimization. Clin Cancer Res. 2004;10(21):7252–9. https://doi.org/10.1158/1078-0432.Ccr-04-0713 .
doi: 10.1158/1078-0432.Ccr-04-0713 pubmed: 15534099
McShane LM, Altman DG, Sauerbrei W, Taube SE, Gion M, Clark GM. REporting recommendations for tumour MARKer prognostic studies (REMARK). Br J Cancer. 2005;93(4):387–91. https://doi.org/10.1038/sj.bjc.6602678 .
doi: 10.1038/sj.bjc.6602678 pubmed: 16106245 pmcid: 2361579
Wirapati P, Sotiriou C, Kunkel S, Farmer P, Pradervand S, Haibe-Kains B, Desmedt C, Ignatiadis M, Sengstag T, Schütz F, Goldstein DR, Piccart M, Delorenzi M. Meta-analysis of gene expression profiles in breast cancer: toward a unified understanding of breast cancer subtyping and prognosis signatures. Breast Cancer Res. 2008;10(4):R65. https://doi.org/10.1186/bcr2124 .
doi: 10.1186/bcr2124 pubmed: 18662380 pmcid: 2575538
Alsaleem MA, Ball G, Toss MS, Raafat S, Aleskandarany M, Joseph C, Ogden A, Bhattarai S, Rida PCG, Khani F, Davis M, Elemento O, Aneja R, Ellis IO, Green A, Mongan NP, Rakha E. A novel prognostic two-gene signature for triple negative breast cancer. Mod Pathol. 2020;33(11):2208–20. https://doi.org/10.1038/s41379-020-0563-7 .
doi: 10.1038/s41379-020-0563-7 pubmed: 32404959
Zhang B, Gu Y, Jiang G. Expression and prognostic characteristics of m(6) A RNA methylation regulators in breast cancer. Front Genet. 2020;11: 604597. https://doi.org/10.3389/fgene.2020.604597 .
doi: 10.3389/fgene.2020.604597 pubmed: 33362863 pmcid: 7758326
Thalhammer A, Bencokova Z, Poole R, Loenarz C, Adam J, O’Flaherty L, Schodel J, Mole D, Giaslakiotis K, Schofield CJ, Hammond EM, Ratcliffe PJ, Pollard PJ. Human AlkB homologue 5 is a nuclear 2-oxoglutarate dependent oxygenase and a direct target of hypoxia-inducible factor 1alpha (HIF-1alpha). PLoS ONE. 2011;6(1): e16210. https://doi.org/10.1371/journal.pone.0016210 .
doi: 10.1371/journal.pone.0016210 pubmed: 21264265 pmcid: 3021549
Yu H, Yang X, Tang J, Si S, Zhou Z, Lu J, Han J, Yuan B, Wu Q, Lu Q, Yang H. ALKBH5 inhibited cell proliferation and sensitized bladder cancer cells to cisplatin by m6A-CK2α-mediated glycolysis. Mol Ther Nucleic Acids. 2021;23:27–41. https://doi.org/10.1016/j.omtn.2020.10.031 .
doi: 10.1016/j.omtn.2020.10.031 pubmed: 33376625
Esquivel-Velázquez M, Ostoa-Saloma P, Palacios-Arreola MI, Nava-Castro KE, Castro JI, Morales-Montor J. The role of cytokines in breast cancer development and progression. J Interferon Cytokine Res. 2015;35(1):1–16. https://doi.org/10.1089/jir.2014.0026 .
doi: 10.1089/jir.2014.0026 pubmed: 25068787 pmcid: 4291218
Coussens LM, Werb Z. Inflammation and cancer. Nature. 2002;420(6917):860–7. https://doi.org/10.1038/nature01322 .
doi: 10.1038/nature01322 pubmed: 12490959 pmcid: 2803035
Li HB, Tong J, Zhu S, Batista PJ, Duffy EE, Zhao J, Bailis W, Cao G, Kroehling L, Chen Y, Wang G, Broughton JP, Chen YG, Kluger Y, Simon MD, Chang HY, Yin Z, Flavell RA. m(6)A mRNA methylation controls T cell homeostasis by targeting the IL-7/STAT5/SOCS pathways. Nature. 2017;548(7667):338–42. https://doi.org/10.1038/nature23450 .
doi: 10.1038/nature23450 pubmed: 28792938 pmcid: 5729908
Wang H, Hu X, Huang M, Liu J, Gu Y, Ma L, Zhou Q, Cao X. Mettl3-mediated mRNA m(6)A methylation promotes dendritic cell activation. Nat Commun. 2019;10(1):1898. https://doi.org/10.1038/s41467-019-09903-6 .
doi: 10.1038/s41467-019-09903-6 pubmed: 31015515 pmcid: 6478715
Yang S, Wei J, Cui YH, Park G, Shah P, Deng Y, Aplin AE, Lu Z, Hwang S, He C, He YY. m(6)A mRNA demethylase FTO regulates melanoma tumorigenicity and response to anti-PD-1 blockade. Nat Commun. 2019;10(1):2782. https://doi.org/10.1038/s41467-019-10669-0 .
doi: 10.1038/s41467-019-10669-0 pubmed: 31239444 pmcid: 6592937
Li N, Kang Y, Wang L, Huff S, Tang R, Hui H, Agrawal K, Gonzalez GM, Wang Y, Patel SP, Rana TM. ALKBH5 regulates anti-PD-1 therapy response by modulating lactate and suppressive immune cell accumulation in tumor microenvironment. Proc Natl Acad Sci USA. 2020;117(33):20159–70. https://doi.org/10.1073/pnas.1918986117 .
doi: 10.1073/pnas.1918986117 pubmed: 32747553 pmcid: 7443867
Han D, Liu J, Chen C, Dong L, Liu Y, Chang R, Huang X, Wang J, Dougherty U, Bissonnette MB, Shen B, Weichselbaum RR, Xu MM, He C. Anti-tumour immunity controlled through mRNA m(6)A methylation and YTHDF1 in dendritic cells. Nature. 2019;566(7743):270–4. https://doi.org/10.1038/s41586-019-0916-x .
doi: 10.1038/s41586-019-0916-x pubmed: 30728504 pmcid: 6522227
Yi L, Wu G, Guo L, Zou X, Huang P. Comprehensive analysis of the PD-L1 and immune infiltrates of m(6)A RNA methylation regulators in head and neck squamous cell carcinoma. Mol Ther Nucleic Acids. 2020;21:299–314. https://doi.org/10.1016/j.omtn.2020.06.001 .
doi: 10.1016/j.omtn.2020.06.001 pubmed: 32622331 pmcid: 7332506
Zhang B, Wu Q, Li B, Wang D, Wang L, Zhou YL. m(6)A regulator-mediated methylation modification patterns and tumor microenvironment infiltration characterization in gastric cancer. Mol Cancer. 2020;19(1):53. https://doi.org/10.1186/s12943-020-01170-0 .
doi: 10.1186/s12943-020-01170-0 pubmed: 32164750 pmcid: 7066851
Gialeli C, Theocharis AD, Karamanos NK. Roles of matrix metalloproteinases in cancer progression and their pharmacological targeting. FEBS J. 2011;278(1):16–27. https://doi.org/10.1111/j.1742-4658.2010.07919.x .
doi: 10.1111/j.1742-4658.2010.07919.x pubmed: 21087457
Liu H, Kato Y, Erzinger SA, Kiriakova GM, Qian Y, Palmieri D, Steeg PS, Price JE. The role of MMP-1 in breast cancer growth and metastasis to the brain in a xenograft model. BMC Cancer. 2012;12:583. https://doi.org/10.1186/1471-2407-12-583 .
doi: 10.1186/1471-2407-12-583 pubmed: 23217186 pmcid: 3526403
Nakopoulou L, Giannopoulou I, Gakiopoulou H, Liapis H, Tzonou A, Davaris PS. Matrix metalloproteinase-1 and -3 in breast cancer: correlation with progesterone receptors and other clinicopathologic features. Hum Pathol. 1999;30(4):436–42. https://doi.org/10.1016/s0046-8177(99)90120-x .
doi: 10.1016/s0046-8177(99)90120-x pubmed: 10208466
McGowan PM, Duffy MJ. Matrix metalloproteinase expression and outcome in patients with breast cancer: analysis of a published database. Ann Oncol. 2008;19(9):1566–72. https://doi.org/10.1093/annonc/mdn180 .
doi: 10.1093/annonc/mdn180 pubmed: 18503039
Kraus D, Reckenbeil J, Perner S, Winter J, Probstmeier R. Expression pattern of matrix metalloproteinase 20 (MMP20) in human tumors. Anticancer Res. 2016;36(6):2713–8.
pubmed: 27272780
Wang S, Jia J, Liu D, Wang M, Wang Z, Li X, Wang H, Rui Y, Liu Z, Guo W, Nie J, Dai H. Matrix metalloproteinase expressions play important role in prediction of ovarian cancer outcome. Sci Rep. 2019;9(1):11677. https://doi.org/10.1038/s41598-019-47871-5 .
doi: 10.1038/s41598-019-47871-5 pubmed: 31406154 pmcid: 6691000
Zhou L, Gao HF, Liu DS, Feng JY, Gao DD, Xia W. Gene expression profiling of brain metastatic cell from triple negative breast cancer: understanding the molecular events. Gene. 2018;640:21–7. https://doi.org/10.1016/j.gene.2017.10.019 .
doi: 10.1016/j.gene.2017.10.019 pubmed: 29024707
Sarkar C, Chakroborty D, Chowdhury UR, Dasgupta PS, Basu S. Dopamine increases the efficacy of anticancer drugs in breast and colon cancer preclinical models. Clin Cancer Res. 2008;14(8):2502–10. https://doi.org/10.1158/1078-0432.ccr-07-1778 .
doi: 10.1158/1078-0432.ccr-07-1778 pubmed: 18413843
Jiang SH, Hu LP, Wang X, Li J, Zhang ZG. Neurotransmitters: emerging targets in cancer. Oncogene. 2020;39(3):503–15. https://doi.org/10.1038/s41388-019-1006-0 .
doi: 10.1038/s41388-019-1006-0 pubmed: 31527667
Chakroborty D, Sarkar C, Mitra RB, Banerjee S, Dasgupta PS, Basu S. Depleted dopamine in gastric cancer tissues: dopamine treatment retards growth of gastric cancer by inhibiting angiogenesis. Clin Cancer Res. 2004;10(13):4349–56. https://doi.org/10.1158/1078-0432.ccr-04-0059 .
doi: 10.1158/1078-0432.ccr-04-0059 pubmed: 15240521
Hoeppner LH, Wang Y, Sharma A, Javeed N, Van Keulen VP, Wang E, Yang P, Roden AC, Peikert T, Molina JR, Mukhopadhyay D. Dopamine D2 receptor agonists inhibit lung cancer progression by reducing angiogenesis and tumor infiltrating myeloid derived suppressor cells. Mol Oncol. 2015;9(1):270–81. https://doi.org/10.1016/j.molonc.2014.08.008 .
doi: 10.1016/j.molonc.2014.08.008 pubmed: 25226814
Roney MSI, Park SK. Antipsychotic dopamine receptor antagonists, cancer, and cancer stem cells. Arch Pharm Res. 2018;41(4):384–408. https://doi.org/10.1007/s12272-018-1017-3 .
doi: 10.1007/s12272-018-1017-3 pubmed: 29556831
Wu XY, Zhang CX, Deng LC, Xiao J, Yuan X, Zhang B, Hou ZB, Sheng ZH, Sun L, Jiang QC, Zhao W. Overexpressed D2 dopamine receptor inhibits non-small cell lung cancer progression through inhibiting NF-κB signaling pathway. Cell Physiol Biochem. 2018;48(6):2258–72. https://doi.org/10.1159/000492644 .
doi: 10.1159/000492644 pubmed: 30114693
Jandaghi P, Najafabadi HS, Bauer AS, Papadakis AI, Fassan M, Hall A, Monast A, von Knebel Doeberitz M, Neoptolemos JP, Costello E, Greenhalf W, Scarpa A, Sipos B, Auld D, Lathrop M, Park M, Büchler MW, Strobel O, Hackert T, Giese NA, Zogopoulos G, Sangwan V, Huang S, Riazalhosseini Y, Hoheisel JD. Expression of DRD2 is increased in human pancreatic ductal adenocarcinoma and inhibitors slow tumor growth in mice. Gastroenterology. 2016;151(6):1218–31. https://doi.org/10.1053/j.gastro.2016.08.040 .
doi: 10.1053/j.gastro.2016.08.040 pubmed: 27578530
Roy S, Lu K, Nayak MK, Bhuniya A, Ghosh T, Kundu S, Ghosh S, Baral R, Dasgupta PS, Basu S. Activation of D2 dopamine receptors in CD133+ve cancer stem cells in non-small cell lung carcinoma inhibits proliferation, clonogenic ability, and invasiveness of these cells. J Biol Chem. 2017;292(2):435–45. https://doi.org/10.1074/jbc.M116.748970 .
doi: 10.1074/jbc.M116.748970 pubmed: 27920206
Hess ME, Hess S, Meyer KD, Verhagen LA, Koch L, Bronneke HS, Dietrich MO, Jordan SD, Saletore Y, Elemento O, Belgardt BF, Franz T, Horvath TL, Ruther U, Jaffrey SR, Kloppenburg P, Bruning JC. The fat mass and obesity associated gene (Fto) regulates activity of the dopaminergic midbrain circuitry. Nat Neurosci. 2013;16(8):1042–8. https://doi.org/10.1038/nn.3449 .
doi: 10.1038/nn.3449 pubmed: 23817550
Koppenol WH, Bounds PL, Dang CV. Otto Warburg’s contributions to current concepts of cancer metabolism. Nat Rev Cancer. 2011;11(5):325–37. https://doi.org/10.1038/nrc3038 .
doi: 10.1038/nrc3038 pubmed: 21508971
Prickett TD, Samuels Y. Molecular pathways: dysregulated glutamatergic signaling pathways in cancer. Clin Cancer Res. 2012;18(16):4240–6. https://doi.org/10.1158/1078-0432.CCR-11-1217 .
doi: 10.1158/1078-0432.CCR-11-1217 pubmed: 22648273 pmcid: 3421042
Luksch H, Uckermann O, Stepulak A, Hendruschk S, Marzahn J, Bastian S, Staufner C, Temme A, Ikonomidou C. Silencing of selected glutamate receptor subunits modulates cancer growth. Anticancer Res. 2011;31(10):3181–92.
pubmed: 21965725
Beretta F, Bassani S, Binda E, Verpelli C, Bello L, Galli R, Passafaro M. The GluR2 subunit inhibits proliferation by inactivating Src-MAPK signalling and induces apoptosis by means of caspase 3/6-dependent activation in glioma cells. Eur J Neurosci. 2009;30(1):25–34. https://doi.org/10.1111/j.1460-9568.2009.06804.x .
doi: 10.1111/j.1460-9568.2009.06804.x pubmed: 19558602
Xiao B, Chen D, Zhou Q, Hang J, Zhang W, Kuang Z, Sun Z, Li L. Glutamate metabotropic receptor 4 (GRM4) inhibits cell proliferation, migration and invasion in breast cancer and is regulated by miR-328-3p and miR-370-3p. BMC Cancer. 2019;19(1):891. https://doi.org/10.1186/s12885-019-6068-4 .
doi: 10.1186/s12885-019-6068-4 pubmed: 31492116 pmcid: 6729096
Yankova E, Blackaby W, Albertella M, Rak J, De Braekeleer E, Tsagkogeorga G, Pilka ES, Aspris D, Leggate D, Hendrick AG, Webster NA, Andrews B, Fosbeary R, Guest P, Irigoyen N, Eleftheriou M, Gozdecka M, Dias JML, Bannister AJ, Vick B, Jeremias I, Vassiliou GS, Rausch O, Tzelepis K, Kouzarides T. Small-molecule inhibition of METTL3 as a strategy against myeloid leukaemia. Nature. 2021;593(7860):597–601. https://doi.org/10.1038/s41586-021-03536-w .
doi: 10.1038/s41586-021-03536-w pubmed: 33902106 pmcid: 7613134
Achour C, Bhattarai DP, Groza P, Román CÁ, Aguilo F. METTL3 regulates breast cancer-associated alternative splicing switches. Oncogene. 2023. https://doi.org/10.1038/s41388-023-02602-z .
doi: 10.1038/s41388-023-02602-z pubmed: 36725888 pmcid: 10020087

Auteurs

Corinne L Woodcock (CL)

University of Nottingham Biodiscovery Institute, University of Nottingham, Nottingham, UK. corinne.woodcock1@nottingham.ac.uk.
Faculty of Medicine and Health Science, School of Veterinary Medicine and Science, University of Nottingham, Nottingham, UK. corinne.woodcock1@nottingham.ac.uk.

Mansour Alsaleem (M)

Nottingham Breast Cancer Research Centre, School of Medicine, Academic Unit for Translational Medical Sciences, University of Nottingham, Nottingham, UK.
Unit of Scientific Research, Applied College, Qassim University, Qassim, Saudi Arabia.

Michael S Toss (MS)

Nottingham Breast Cancer Research Centre, School of Medicine, Academic Unit for Translational Medical Sciences, University of Nottingham, Nottingham, UK.

Jennifer Lothion-Roy (J)

University of Nottingham Biodiscovery Institute, University of Nottingham, Nottingham, UK.
Faculty of Medicine and Health Science, School of Veterinary Medicine and Science, University of Nottingham, Nottingham, UK.

Anna E Harris (AE)

University of Nottingham Biodiscovery Institute, University of Nottingham, Nottingham, UK.
Faculty of Medicine and Health Science, School of Veterinary Medicine and Science, University of Nottingham, Nottingham, UK.

Jennie N Jeyapalan (JN)

University of Nottingham Biodiscovery Institute, University of Nottingham, Nottingham, UK.
Faculty of Medicine and Health Science, School of Veterinary Medicine and Science, University of Nottingham, Nottingham, UK.

Nataliya Blatt (N)

University of Nottingham Biodiscovery Institute, University of Nottingham, Nottingham, UK.
Faculty of Medicine and Health Science, School of Veterinary Medicine and Science, University of Nottingham, Nottingham, UK.
Institute for Fundamental Medicine and Science, Kazan Federal University, Kazan, Tatarstan, Russia.

Albert A Rizvanov (AA)

Institute for Fundamental Medicine and Science, Kazan Federal University, Kazan, Tatarstan, Russia.

Regina R Miftakhova (RR)

Institute for Fundamental Medicine and Science, Kazan Federal University, Kazan, Tatarstan, Russia.

Yousif A Kariri (YA)

Nottingham Breast Cancer Research Centre, School of Medicine, Academic Unit for Translational Medical Sciences, University of Nottingham, Nottingham, UK.
Department of Clinical Laboratory Science, Faculty of Applied Medical Science, Shaqra University 33, 11961, Shaqra, Saudi Arabia.

Srinivasan Madhusudan (S)

University of Nottingham Biodiscovery Institute, University of Nottingham, Nottingham, UK.

Andrew R Green (AR)

Nottingham Breast Cancer Research Centre, School of Medicine, Academic Unit for Translational Medical Sciences, University of Nottingham, Nottingham, UK.

Catrin S Rutland (CS)

Faculty of Medicine and Health Science, School of Veterinary Medicine and Science, University of Nottingham, Nottingham, UK.

Rupert G Fray (RG)

School of Biosciences, Plant Science Division, University of Nottingham, Nottingham, UK.

Emad A Rakha (EA)

University of Nottingham Biodiscovery Institute, University of Nottingham, Nottingham, UK.
Nottingham Breast Cancer Research Centre, School of Medicine, Academic Unit for Translational Medical Sciences, University of Nottingham, Nottingham, UK.
Department of Histopathology, Nottingham University Hospitals NHS Trust, Nottingham City Hospital, Nottingham, UK.
Pathology Department, Hamad General Hospital, Hamad Medical Corporation, Doha, Qatar.

Nigel P Mongan (NP)

University of Nottingham Biodiscovery Institute, University of Nottingham, Nottingham, UK. nigel.mongan@nottingham.ac.uk.
Faculty of Medicine and Health Science, School of Veterinary Medicine and Science, University of Nottingham, Nottingham, UK. nigel.mongan@nottingham.ac.uk.
Department of Pharmacology, Weill Cornell Medicine, New York, NY, USA. nigel.mongan@nottingham.ac.uk.

Classifications MeSH