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Review

Integrated analysis of FHIT gene alterations in cancer

ORCID Icon, ORCID Icon & ORCID Icon
Pages 92-113 | Received 16 Aug 2023, Accepted 08 Jan 2024, Published online: 18 Jan 2024

References

  • Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144(5):646–674. doi: 10.1016/j.cell.2011.02.013
  • Glover TW, Wilson TE, Arlt MF. Fragile sites in cancer: more than meets the eye. Nat Rev Cancer. 2017;17(8):489–501. doi: 10.1038/nrc.2017.52
  • Pekarsky Y, Garrison PN, Palamarchuk A, et al. Fhit is a physiological target of the protein kinase Src. Proc Natl Acad Sci. 2004;101(11):3775–3779. doi: 10.1073/pnas.0400481101
  • Nishizaki M, Sasaki J-I, Fang B, et al. Synergistic tumor suppression by coexpression of FHIT and p53 coincides with FHIT-Mediated MDM2 inactivation and p53 stabilization in human non-small cell lung cancer cells. Cancer Res. 2004;64(16):5745–5752. doi: 10.1158/0008-5472.CAN-04-0195
  • Rimessi A, Marchi S, Fotino C, et al. Intramitochondrial calcium regulation by the FHIT gene product sensitizes to apoptosis. Proc Natl Acad Sci. 2009;106(31):12753–12758. doi: 10.1073/pnas.0906484106
  • Brenner CH. Hint, Fhit, and GalT: function, structure, evolution, and mechanism of three branches of the histidine triad superfamily of nucleotide hydrolases and transferases. Biochemistry. 2002;41(29):9003–9014. doi: 10.1021/bi025942q
  • Pace HC, Garrison PN, Robinson AK, et al. Genetic, biochemical, and crystallographic characterization of fhit–substrate complexes as the active signaling form of fhit. Proc Natl Acad Sci. 1998;95(10):5484–5489. doi: 10.1073/pnas.95.10.5484
  • Lima CD, Klein MG, Hendrickson WA. Structure-based analysis of catalysis and substrate definition in the HIT protein family. Science. 1997;278(5336):286–290. doi: 10.1126/science.278.5336.286
  • Barnes LD, Fhit, a Putative Tumor Suppressor in Humans, Is a Dinucleoside 5',5' ''-P 1,P 3 -Triphosphate Hydrolase. Biochemistry. 1996;35(36):11529–11535. doi: 10.1021/bi961415t
  • Draganescu A, Hodawadekar SC, Gee KR, et al. Fhit-nucleotide specificity probed with novel fluorescent and fluorogenic substrates. J Biol Chem. 2000;275(7):4555–4560. doi: 10.1074/jbc.275.7.4555
  • Brenner C, Pace HC, Garrison PN, et al. Purification and crystallization of complexes modeling the active state of the fragile histidine triad protein. Protein Eng Des Sel. 1997;10(12):1461–1463. doi: 10.1093/protein/10.12.1461
  • Guranowski A, Wojdyła AM, Pietrowska-Borek M, et al. Fhit proteins can also recognize substrates other than dinucleoside polyphosphates. FEBS Lett. 2008;582(20):3152–3158. doi: 10.1016/j.febslet.2008.07.060
  • Wojdyła-Mamoń AM, Guranowski A. Adenylylsulfate–ammonia adenylyltransferase activity is another inherent property of fhit proteins. Biosci Rep. 2015;35(4):e00235. doi: 10.1042/BSR20150135
  • Zamecnik PG, Stephenson ML, Janeway CM, et al. Enzymatic synthesis of diadenosine tetraphosphate and diadenosine triphosphate with a purified lysyl-sRNA synthetase. Biochem Biophys Res Commun. 1966;24(1):91–97. doi: 10.1016/0006-291X(66)90415-3
  • Goerlich O, Foeckler R, Holler E. Mechanism of synthesis of Adenosine(5’)tetraphospho(5’)adenosine (AppppA) by Aminoacyl-tRNA Synthetases. Eur J Biochem. 1982;126(1):135–142. doi: 10.1111/j.1432-1033.1982.tb06757.x
  • Brevet A, Chen J, Lévêque F, et al. In vivo synthesis of adenylylated bis(5’-nucleosidyl) tetraphosphates (Ap4N) by Escherichia coli aminoacyl-tRNA synthetases. Proc Natl Acad Sci. 1989;86(21):8275–8279. doi: 10.1073/pnas.86.21.8275
  • Merkulova T, Kovaleva G, Kisselev LP. P1 , P3 -bis(5’-adenosyl)triphosphate (ap 3 A) as a substrate and a product of mammalian tryptophanyl-tRNA synthetase. FEBS Lett. 1994;350(2–3):287–290. doi: 10.1016/0014-5793(94)00764-0
  • Flores NA, Stavrou BM, Sheridan DJ. The effects of diadenosine polyphosphates on the cardiovascular system. Cardiovasc Res. 1999;42(1):15–26. doi: 10.1016/S0008-6363(99)00004-8
  • Verspohl EJ, Johannwille B. Diadenosine polyphosphates in insulin-secreting cells: interaction with specific receptors and degradation. Diabetes. 1998;47(11):1727–1734. doi: 10.2337/diabetes.47.11.1727
  • Luthje J, Ogilvie A. Catabolism of Ap3A and Ap4A in human plasma. Purification and characterization of a glycoprotein complex with 5’-nucleotide phosphodiesterase activity. Eur J Biochem. 1985;149(1):119–127. doi: 10.1111/j.1432-1033.1985.tb08901.x
  • Rubino A, Burnstock G. Possible role of diadenosine polyphosphates as modulators of cardiac sensory-motor neurotransmission in guinea-pigs. J Physiol. 1996;495(2):515–523. doi: 10.1113/jphysiol.1996.sp021611
  • Vartanian A, Alexandrov I, Prudowski I, et al. Ap 4 A induces apoptosis in human cultured cells. FEBS Lett. 1999;456(1):175–180. doi: 10.1016/S0014-5793(99)00956-4
  • Fisher DI, McLennan AG. Correlation of intracellular diadenosine triphosphate (Ap3A) with apoptosis in fhit-positive HEK293 cells. Cancer Lett. 2008;259(2):186–191. doi: 10.1016/j.canlet.2007.10.007
  • Siprashvili Z, Sozzi G, Barnes LD, et al. Replacement of fhit in cancer cells suppresses tumorigenicity. Proc Natl Acad Sci. 1997;94(25):13771–13776. doi: 10.1073/pnas.94.25.13771
  • Roz L, Gramegna M, Ishii H, et al. Restoration of fragile histidine triad (FHIT) expression induces apoptosis and suppresses tumorigenicity in lung and cervical cancer cell lines. Proc Natl Acad Sci. 2002;99(6):3615–3620. doi: 10.1073/pnas.062030799
  • Trapasso F, Krakowiak A, Cesari R, et al. Designed FHIT alleles establish that fhit-induced apoptosis in cancer cells is limited by substrate binding. Proc Natl Acad Sci. 2003;100(4):1592–1597. doi: 10.1073/pnas.0437915100
  • Herzog D, Jansen J, Mißun M, et al. Chemical proteomics of the tumor suppressor fhit covalently bound to the cofactor Ap3 a elucidates its inhibitory action on translation. J Am Chem Soc. 2022;144(19):8613–8623. doi: 10.1021/jacs.2c00815
  • Lee PC, Bochner BR, Ames BN. AppppA, heat-shock stress, and cell oxidation. Proc Natl Acad Sci. 1983;80(24):7496–7500. doi: 10.1073/pnas.80.24.7496
  • Baker JC, Jacobson MK. Alteration of adenyl dinucleotide metabolism by environmental stress. Proc Natl Acad Sci. 1986;83(8):2350–2352. doi: 10.1073/pnas.83.8.2350
  • Krüger L, Albrecht CJ, Schammann HK, et al. Chemical proteomic profiling reveals protein interactors of the alarmones diadenosine triphosphate and tetraphosphate. Nat Commun. 2021;12(1):5808. doi: 10.1038/s41467-021-26075-4
  • Albrecht CJ, Stumpf FM, Krüger L, et al. Chemical proteomics reveals interactors of the alarmone diadenosine triphosphate in the cancer cell line H1299†. J Pept Sci. 2023;29(3). doi: 10.1002/psc.3458
  • McLennan AG. Dinucleoside polyphosphates—friend or foe? Pharmacol Ther. 2000;87(2–3):73–89. doi: 10.1016/S0163-7258(00)00041-3
  • Ohta M, Inoue, H., Cotticelli, M. G.,The FHIT gene, spanning the chromosome 3p14.2 fragile site and Renal Carcinoma–associated t(3;8) breakpoint, is abnormal in digestive tract cancers. Cell. 1996;84(4):587–597. doi: 10.1016/S0092-8674(00)81034-X
  • Sozzi G, Veronese ML, Negrini M, et al. The FHIT gene at 3p14.2 is abnormal in lung cancer. Cell. 1996;85(1):17–26. doi: 10.1016/S0092-8674(00)81078-8
  • Sozzi G, Alder, H., Tornielli, S,Aberrant FHIT transcripts in Merkel cell carcinoma. Cancer Res. 1996;56(11):2472–2474.
  • Negrini M, Monaco, C, Vorechovsky, I. The FHIT gene at 3p14.2 is abnormal in breast carcinomas. Cancer Res. 1996;56(14):3173–3179.
  • Virgilio L, Shuster M, Gollin SM, et al. FHIT gene alterations in head and neck squamous cell carcinomas. Proc Natl Acad Sci. 1996;93(18):9770–9775. doi: 10.1073/pnas.93.18.9770
  • Thiagalingam S, Lisitsyn, NA, Hamaguchi, M. Evaluation of the FHIT gene in colorectal cancers. Cancer Res. 1996;56(13):2936–2939.
  • Shridhar R, Shridhar V, Wang X. Frequent breakpoints in the 3p14.2 fragile site, FRA3B, in pancreatic tumors. Cancer Res. 1996;56(19):4347–4350.
  • Man S, Ellis IO, Sibbering M, et al. High levels of allele loss at the FHIT and ATM genes in non-comedo ductal carcinoma in situ and grade I tubular invasive breast cancers. Cancer Res. 1996;56(23):5484–5489.
  • Panagopoulos I, Pandis, N, Thelin, S. The FHIT and PTPRG genes are deleted in benign proliferative breast disease associated with familial breast cancer and cytogenetic rearrangements of chromosome band 3p14. Cancer Res. 1996;56(21):4871–4875.
  • Mao L, Fan YH, Lotan R, et al. Frequent abnormalities of FHIT, a candidate tumor suppressor gene, in head and neck cancer cell lines. Cancer Res. 1996;56(22):5128–5131.
  • Bignell GR, Greenman CD, Davies H, et al. Signatures of mutation and selection in the cancer genome. Nature. 2010;463(7283):893–898. doi: 10.1038/nature08768
  • Futreal PA, Coin L, Marshall M, et al. A census of human cancer genes. Nat Rev Cancer. 2004;4(3):177–183. doi: 10.1038/nrc1299
  • Fong LYY, Fidanza V, Zanesi N. Muir–Torre-like syndrome in Fhit-deficient mice. Proc Natl Acad Sci. 2000;97(9):4742–4747. doi: 10.1073/pnas.080063497
  • Zanesi N, Fidanza V, Fong LY, et al. The tumor spectrum in FHIT-deficient mice. Proc Natl Acad Sci. 2001;98(18):10250–10255. doi: 10.1073/pnas.191345898
  • Fujishita T, Doi Y, Sonoshita M, et al. Development of spontaneous tumours and intestinal lesions in fhit gene knockout mice. Br J Cancer. 2004;91(8):1571–1574. doi: 10.1038/sj.bjc.6602182
  • Park SH, Bennett-Baker, P., Ahmed, S., Locus-specific transcription silencing at the FHIT gene suppresses replication stress-induced copy number variant formation and associated replication delay. Nucleic Acids Res. 2021;49(13):7507–7524. doi: 10.1093/nar/gkab559
  • Weinstein JN, Collisson EA, Mills GB, et al. The cancer genome atlas pan-cancer analysis project. Nat Genet. 2013;45(10):1113–1120. doi: 10.1038/ng.2764
  • Cerami E, Gao J, Dogrusoz U, et al. The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data. Cancer Discov. 2012;2(5):401–404. doi: 10.1158/2159-8290.CD-12-0095
  • Tate JG, Bamford S, Jubb HC, et al. COSMIC: the catalogue of somatic mutations in cancer. Nucleic Acids Res. 2019;47(D1):D941–D947. doi: 10.1093/nar/gky1015
  • Klonowska K, Czubak K, Wojciechowska M, et al. Oncogenomic portals for the visualization and analysis of genome-wide cancer data. Oncotarget. 2016;7(1):176–192. doi: 10.18632/oncotarget.6128
  • Zack TI, Schumacher SE, Carter SL, et al. Pan-cancer patterns of somatic copy number alteration. Nat Genet. 2013;45(10):1134–1140. doi: 10.1038/ng.2760
  • Martínez-Jiménez F, Muiños F, Sentís I, et al. A compendium of mutational cancer driver genes. Nat Rev Cancer. 2020;20(10):555–572. doi: 10.1038/s41568-020-0290-x
  • Beroukhim R, Getz G, Nghiemphu L, et al. Assessing the significance of chromosomal aberrations in cancer: methodology and application to glioma. Proc Natl Acad Sci. 2007;104(50):20007–20012. doi: 10.1073/pnas.0710052104
  • Durkin SG, Glover TW. Chromosome fragile sites. Ann Rev Genet. 2007;41(1):169–192. doi: 10.1146/annurev.genet.41.042007.165900
  • Tsantoulis PK, Kotsinas A, Sfikakis PP, et al. Oncogene-induced replication stress preferentially targets common fragile sites in preneoplastic lesions. A genome-wide study. Oncogene. 2008;27(23):3256–3264. doi: 10.1038/sj.onc.1210989
  • Marsit CJ. Loss of heterozygosity of chromosome 3p21 is associated with mutant TP53 and Better Patient Survival in non–small-Cell lung cancer. Cancer Res. 2004;64(23):8702–8707. doi: 10.1158/0008-5472.CAN-04-2558
  • Sha D, Jin Z, Budczies J, et al. Tumor mutational burden as a predictive biomarker in solid tumors. Cancer Discov. 2020;10(12):1808–1825. doi: 10.1158/2159-8290.CD-20-0522
  • Vilar E, Gruber SB. Microsatellite instability in colorectal cancer—the stable evidence. Nat Rev Clin Oncol. 2010;7(3):153–162. doi: 10.1038/nrclinonc.2009.237
  • Taylor AM, Shih J, Ha G, et al. Genomic and functional approaches to understanding cancer aneuploidy. Cancer Cell. 2018;33(4):676–689.e3. doi: 10.1016/j.ccell.2018.03.007
  • He D, Zhang Y-W, Zhang N-N, et al. Aberrant gene promoter methylation of p16, FHIT, CRBP1, WWOX, and DLC-1 in Epstein–barr virus-associated gastric carcinomas. Med Oncol. 2015;32(4):92. doi: 10.1007/s12032-015-0525-y
  • Inokawa Y, Hayashi M, Begum S, et al. High-risk HPV infection-associated hypermethylated genes in oropharyngeal squamous cell carcinomas. BMC Cancer. 2022;22(1):1146. doi: 10.1186/s12885-022-10227-w
  • Ki K-D, Lee S-K, Tong S-Y, et al. Role of 5’-CpG island hypermethylation of the FHIT gene in cervical carcinoma. J Gynecol Oncol. 2008;19(2):117. doi: 10.3802/jgo.2008.19.2.117
  • Yang Y, Takeuchi S, Hofmann WK, et al. Aberrant methylation in promoter-associated CpG islands of multiple genes in acute lymphoblastic leukemia. Leuk Res. 2006;30(1):98–102. doi: 10.1016/j.leukres.2005.06.002
  • Kvasha S, Gordiyuk V, Kondratov A, et al. Hypermethylation of the 5’CpG island of the FHIT gene in clear cell renal carcinomas. Cancer Lett. 2008;265(2):250–257. doi: 10.1016/j.canlet.2008.02.036
  • Maruyama R, Toyooka S, Toyooka KO., Aberrant promoter methylation profile of bladder cancer and its relationship to clinicopathological features. Cancer Res. 2001;61(24):8659–8663.
  • Yang Q, Nakamura M, Nakamura Y. Two-hit inactivation of FHIT by loss of heterozygosity and hypermethylation in breast cancer. Clin Cancer Res Off J Am Assoc Cancer Res. 2002;8:2890–2893.
  • Kim JS, Kim JW, Han J, et al. Cohypermethylation of p16 and FHIT promoters as a prognostic factor of recurrence in surgically resected stage I non–small cell lung cancer. Cancer Res. 2006;66(8):4049–4054. doi: 10.1158/0008-5472.CAN-05-3813
  • Wali A, Srinivasan R, Shabnam MS, et al. Loss of fragile histidine triad gene expression in advanced lung cancer is consequent to allelic loss at 3p14 locus and promoter methylation. Mol Cancer Res. 2006;4(2):93–99. doi: 10.1158/1541-7786.MCR-05-0070
  • Li Y, Ge D, Lu C. The SMART app: an interactive web application for comprehensive DNA methylation analysis and visualization. Epigenet Chromatin. 2019;12(1):71. doi: 10.1186/s13072-019-0316-3
  • Vogelstein B, Papadopoulos N, Velculescu VE, et al. Cancer genome landscapes. Science. 2013;339(6127):1546–1558. doi: 10.1126/science.1235122
  • Bailey MH, Tokheim C, Porta-Pardo E, et al. Comprehensive characterization of cancer Driver genes and mutations. Cell. 2018;173(2):371–385.e18. doi: 10.1016/j.cell.2018.02.060
  • Miuma S, Saldivar JC, Karras JR, et al. Fhit deficiency-induced global genome instability promotes mutation and clonal expansion. PLoS One. 2013;8(11):e80730. doi: 10.1371/journal.pone.0080730
  • Paisie CA, Schrock, M. S., Karras, J. R., Exome‐wide single‐base substitutions in tissues and derived cell lines of the constitutive fhit knockout mouse. Cancer Sci. 2016;107(4):528–535. doi: 10.1111/cas.12887
  • Volinia S, Druck T, Paisie CA, et al. The ubiquitous ‘cancer mutational signature’ 5 occurs specifically in cancers with deleted FHIT alleles. Oncotarget. 2017;8(60):102199–102211. doi: 10.18632/oncotarget.22321
  • Saldivar JC, Miuma S, Bene J, et al. Initiation of genome instability and preneoplastic processes through loss of fhit expression. PLoS Genet. 2012;8(11):e1003077. doi: 10.1371/journal.pgen.1003077
  • Huiping C, Kristjansdottir S, Bergthorsson JT, et al. High frequency of LOH, MSI and abnormal expression of FHIT in gastric cancer. Eur J Cancer. 2002;38(5):728–735. doi: 10.1016/S0959-8049(01)00432-4
  • Andachi H, Yashima K, Koda M, et al. Reduced fhit expression is associated with mismatch repair deficiency in human advanced colorectal carcinoma. Br J Cancer. 2002;87(4):441–445. doi: 10.1038/sj.bjc.6600501
  • Sarli L, Bottarelli L, Azzoni C, et al. Abnormal fhit protein expression and high frequency of microsatellite instability in sporadic colorectal cancer. Eur J Cancer. 2004;40(10):1581–1588. doi: 10.1016/j.ejca.2004.02.021
  • Vernole P, Muzi A, Volpi A, et al. Common fragile sites in colon cancer cell lines: role of mismatch repair, RAD51 and poly(ADP-ribose) polymerase-1. Mutat Res Mol Mech Mutagen. 2011;712(1–2):40–48. doi: 10.1016/j.mrfmmm.2011.04.006
  • Jahid S, Sun J, Gelincik O, et al. Inhibition of colorectal cancer genomic copy number alterations and chromosomal fragile site tumor suppressor FHIT and WWOX deletions by DNA mismatch repair. Oncotarget. 2017;8(42):71574–71586. doi: 10.18632/oncotarget.17776
  • Bhandari V, Hoey C, Liu LY, et al. Molecular landmarks of tumor hypoxia across cancer types. Nat Genet. 2019;51(2):308–318. doi: 10.1038/s41588-018-0318-2
  • Da Silva J, Jouida A, Ancel J. FHIT low / pHER2 high signature in non-small cell lung cancer is predictive of anti-HER2 molecule efficacy. J Pathol. 2020;251(2):187–199. doi: 10.1002/path.5439
  • Bianchi F, Magnifico A, Olgiati C, et al. FHIT-proteasome degradation caused by mitogenic stimulation of the EGF receptor family in cancer cells. Proc Natl Acad Sci. 2006;103(50):18981–18986. doi: 10.1073/pnas.0605821103