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2000
Volume 25, Issue 7
  • ISSN: 1568-0096
  • E-ISSN: 1873-5576

Abstract

In eukaryotic cells, primases are the key polymerase during DNA replication and DNA damage repair, which included primase subunit 1 (PRIM1) and primase subunit 2 (PRIM2). Recent studies reported that the aberrant expression and activity of PRIM enzymes are closely associated with the carcinogenesis and development of various cancers. PRIM1 is overexpressed in hepatocellular carcinoma, breast cancer, and other cancers, while PRIM2 is highly expressed in lung cancer, gastrointestinal cancer, and other cancers. Further studies revealed that the knockdown of PRIM1 promoted the apoptosis of liver cancer cells, while Dihydroartemisinin (DHA) can inhibit PRIM2 expression, suppress lung cancer cell proliferation, and result in ferroptosis. The present review summarized the recent advancements in the research of the aberrant expression of PRIM1 and PRIM2 and their activity in DNA replication, DNA damage repair, and carcinogenesis. Furthermore, the strategies targeting PRIM1 or/and PRIM2 become potential therapeutic approaches in cancer treatment.

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References

  1. CaoW. ChenH.D. YuY.W. LiN. ChenW.Q. Changing profiles of cancer burden worldwide and in China: a secondary analysis of the global cancer statistics 2020.Chin. Med. J. (Engl.)2021134778379110.1097/CM9.000000000000147433734139
    [Google Scholar]
  2. SungH. FerlayJ. SiegelR.L. LaversanneM. SoerjomataramI. JemalA. BrayF. Global Cancer Statistics 2020: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries.CA Cancer J. Clin.202171320924910.3322/caac.2166033538338
    [Google Scholar]
  3. VernieriC. NichettiF. RaimondiA. PuscedduS. PlataniaM. BerrinoF. de BraudF. Diet and supplements in cancer prevention and treatment: Clinical evidences and future perspectives.Crit. Rev. Oncol. Hematol.2018123577310.1016/j.critrevonc.2018.01.00229482780
    [Google Scholar]
  4. JinG. LvJ. YangM. WangM. ZhuM. WangT. YanC. YuC. DingY. LiG. RenC. NiJ. ZhangR. GuoY. BianZ. ZhengY. ZhangN. JiangY. ChenJ. WangY. XuD. ZhengH. YangL. ChenY. WaltersR. MillwoodI.Y. DaiJ. MaH. ChenK. ChenZ. HuZ. WeiQ. ShenH. LiL. Genetic risk, incident gastric cancer, and healthy lifestyle: a meta-analysis of genome-wide association studies and prospective cohort study.Lancet Oncol.202021101378138610.1016/S1470‑2045(20)30460‑533002439
    [Google Scholar]
  5. YuC. TangH. GuoY. BianZ. YangL. ChenY. TangA. ZhouX. YangX. ChenJ. ChenZ. LvJ. LiL. Hot tea consumption and its interactions with alcohol and tobacco use on the risk for esophageal cancer.Ann. Intern. Med.2018168748949710.7326/M17‑200029404576
    [Google Scholar]
  6. HanahanD. WeinbergR.A. Hallmarks of cancer: the next generation.Cell2011144564667410.1016/j.cell.2011.02.01321376230
    [Google Scholar]
  7. AjaniJ.A. D’AmicoT.A. BentremD.J. ChaoJ. CookeD. CorveraC. DasP. EnzingerP.C. EnzlerT. FantaP. FarjahF. GerdesH. GibsonM.K. HochwaldS. HofstetterW.L. IlsonD.H. KeswaniR.N. KimS. KleinbergL.R. KlempnerS.J. LacyJ. LyQ.P. MatkowskyjK.A. McNamaraM. MulcahyM.F. OutlawD. ParkH. PerryK.A. PimientoJ. PoultsidesG.A. ReznikS. RosesR.E. StrongV.E. SuS. WangH.L. WiesnerG. WillettC.G. YakoubD. YoonH. McMillianN. PluchinoL.A. Gastric cancer, version 2.2022, NCCN clinical practice guidelines in oncology.J. Natl. Compr. Canc. Netw.202220216719210.6004/jnccn.2022.000835130500
    [Google Scholar]
  8. AssarafY.G. BrozovicA. GonçalvesA.C. JurkovicovaD. LinēA. MachuqueiroM. SaponaraS. Sarmento-RibeiroA.B. XavierC.P.R. VasconcelosM.H. The multi-factorial nature of clinical multidrug resistance in cancer.Drug Resist. Updat.20194610064510.1016/j.drup.2019.10064531585396
    [Google Scholar]
  9. López-PlazaB. Loria-KohenV. González-RodríguezL.G. Fernández-CruzE. [Diet and lifestyle in cancer prevention].Nutr. Hosp.202239Spec No3747710.20960/nh.043.36040006
    [Google Scholar]
  10. BailisJ.M. ForsburgS.L. MCM proteins: DNA damage, mutagenesis and repair.Curr. Opin. Genet. Dev.2004141172110.1016/j.gde.2003.11.00215108800
    [Google Scholar]
  11. ShiratoriA. OkumuraK. NogamiM. TaguchiH. OnozakiT. InoueT. AndoT. ShibataT. IzumiM. MiyazawaH. HanaokaF. MurakamiY. EkiT. Assignment of the 49-kDa (PRIM1) and 58-kDa (PRIM2A and PRIM2B) subunit genes of the human DNA primase to chromosome bands 1q44 and 6p11.1-p12.Genomics199528235035310.1006/geno.1995.11558530050
    [Google Scholar]
  12. LeipeD.D. AravindL. KooninE.V. Did DNA replication evolve twice independently?Nucleic Acids Res.199927173389340110.1093/nar/27.17.338910446225
    [Google Scholar]
  13. OkazakiT. Days weaving the lagging strand synthesis of DNA — A personal recollection of the discovery of Okazaki fragments and studies on discontinuous replication mechanism —.Proc. Jpn. Acad., Ser. B, Phys. Biol. Sci.201793532233810.2183/pjab.93.02028496054
    [Google Scholar]
  14. BalakrishnanL. BambaraR.A. Okazaki fragment metabolism.Cold Spring Harb. Perspect. Biol.201352a010173a01017310.1101/cshperspect.a01017323378587
    [Google Scholar]
  15. YotovW.V. HamelH. RivardG.E. ChampagneM.A. RussoP.A. LeclercJ.M. BernsteinM.L. LevyE. Amplifications of DNA primase 1 (PRIM1) in human osteosarcoma.Genes Chromosomes Cancer1999261626910.1002/(SICI)1098‑2264(199909)26:1<62::AID‑GCC9>3.0.CO;2‑F10441007
    [Google Scholar]
  16. LeeW.H. ChenL.C. LeeC.J. HuangC.C. HoY.S. YangP.S. HoC.T. ChangH.L. LinI.H. ChangH.W. LiuY.R. WuC.H. TuS.H. DNA primase polypeptide 1 (PRIM1) involves in estrogen‐induced breast cancer formation through activation of the G2/M cell cycle checkpoint.Int. J. Cancer2019144361563010.1002/ijc.3178830097999
    [Google Scholar]
  17. JiangJ. ZhangY. XuR. RenL. ChenJ. LuH. PRIM1 promotes the proliferation of hepatocellular carcinoma cells in vitro and in vivo.J. Cancer202011226601661110.7150/jca.4787033046981
    [Google Scholar]
  18. GaoY. ZhangE. FeiX. KongL. LiuP. TanX. Identification of Novel metabolism-associated subtypes for pancreatic cancer to establish an eighteen-gene risk prediction model.Front. Cell Dev. Biol.2021969116110.3389/fcell.2021.69116134447748
    [Google Scholar]
  19. KimS.Y. KimK. ChoS.H. ChunS.M. TakE. HongY.S. KimJ.E. KimT.W. Longitudinal change of genetic variations in cetuximab-treated metastatic colorectal cancer.Cancer Genet.2021258-259273610.1016/j.cancergen.2021.06.00734315006
    [Google Scholar]
  20. WangT. TangT. JiangY. HeT. QiL. ChangH. QiaoY. SunM. ShanC. ZhuX. LiuJ. WangJ. PRIM2 promotes cell cycle and tumor progression in p53-mutant lung cancer.Cancers (Basel)20221414337010.3390/cancers1414337035884433
    [Google Scholar]
  21. JuhariW.K.W. Ahmad Amin NoordinK.B. ZakariaA.D. RahmanW.F.W.A. MokhterW.M.M.W.M. HassanM.R.A. SidekA.S.M. ZilfalilB.A. Whole-genome profiles of malay colorectal cancer patients with intact MMR proteins.Genes (Basel)2021129144810.3390/genes1209144834573430
    [Google Scholar]
  22. YuanB. LiaoF. ShiZ.Z. RenY. DengX.L. YangT.T. LiD.Y. LiR.F. PuD.D. WangY.J. TanY. YangZ. ZhangY.H. Dihydroartemisinin inhibits the proliferation, colony formation and induces ferroptosis of lung cancer cells by inhibiting PRIM2/SLC7A11 axis.OncoTargets Ther.202013108291084010.2147/OTT.S24849233149601
    [Google Scholar]
  23. BoosD. FerreiraP. Origin firing regulations to control genome replication timing.Genes (Basel)201910319910.3390/genes1003019930845782
    [Google Scholar]
  24. LemanA. NoguchiE. The replication fork: Understanding the eukaryotic replication machinery and the challenges to genome duplication.Genes (Basel)20134113210.3390/genes401000123599899
    [Google Scholar]
  25. CordobaJ.J. MullinsE.A. SalayL.E. EichmanB.F. ChazinW.J. Flexibility and distributive synthesis regulate RNA Priming and Handoff in human DNA polymerase α-primase.J. Mol. Biol.20234352416833010.1016/j.jmb.2023.16833037884206
    [Google Scholar]
  26. BaranovskiyA.G. ZhangY. SuwaY. GuJ. BabayevaN.D. PavlovY.I. TahirovT.H. Insight into the Human DNA primase interaction with template-primer.J. Biol. Chem.201629194793480210.1074/jbc.M115.70406426710848
    [Google Scholar]
  27. EkundayoB. BleichertF. Origins of DNA replication.PLoS Genet.2019159e100832010.1371/journal.pgen.100832031513569
    [Google Scholar]
  28. LisovaA.E. BaranovskiyA.G. MorstadtL.M. BabayevaN.D. TahirovT.H. Human DNA polymerase α has a strong mutagenic potential at the initial steps of DNA synthesis.Nucleic Acids Res.20225021122661227310.1093/nar/gkac110136454017
    [Google Scholar]
  29. AminA. WuR. CheungM.H. ScottJ.F. WangZ. ZhouZ. LiuC. ZhuG. WongC.K.C. YuZ. LiangC. An essential and cell-cycle-dependent orc dimerization cycle regulates eukaryotic chromosomal dna replication.Cell Rep.2020301033233338.e610.1016/j.celrep.2020.02.04632160540
    [Google Scholar]
  30. McCullochS.D. KunkelT.A. The fidelity of DNA synthesis by eukaryotic replicative and translesion synthesis polymerases.Cell Res.200818114816110.1038/cr.2008.418166979
    [Google Scholar]
  31. TomkinsonA.E. HowesT.R. WiestN.E. DNA ligases as therapeutic targets.Transl. Cancer Res.201323121910.1126/science.aam734424224145
    [Google Scholar]
  32. ShumanS. DNA ligases: Progress and prospects.J. Biol. Chem.200928426173651736910.1074/jbc.R90001720019329793
    [Google Scholar]
  33. JohanssonE. DixonN. Replicative DNA Polymerases.Cold Spring Harb. Perspect. Biol.201356a012799a01279910.1101/cshperspect.a01279923732474
    [Google Scholar]
  34. AreziB. KuchtaR.D. Eukaryotic DNA primase.Trends Biochem. Sci.2000251157257610.1016/S0968‑0004(00)01680‑711084371
    [Google Scholar]
  35. BainbridgeL.J. ZabradyK. DohertyA.J. Primase-polymerases: How to make a primer from scratch.Biosci. Rep.2023437BSR2022198610.1042/BSR2022198637358261
    [Google Scholar]
  36. ZhangY. BaranovskiyA.G. TahirovT.H. PavlovY.I. The C-terminal domain of the DNA polymerase catalytic subunit regulates the primase and polymerase activities of the human DNA polymerase α-primase complex.J. Biol. Chem.201428932220212203410.1074/jbc.M114.57033324962573
    [Google Scholar]
  37. KlingeS. Núñez-RamírezR. LlorcaO. PellegriniL. 3D architecture of DNA Pol α reveals the functional core of multi-subunit replicative polymerases.EMBO J.200928131978198710.1038/emboj.2009.15019494830
    [Google Scholar]
  38. FioaniM. LucchiniG. PlevaniP. The DNA polymerase α-primase complex couples DNA replication, cell-cycle progression and DNA-damage response.Trends Biochem. Sci.1997221142442710.1016/S0968‑0004(97)01109‑29397683
    [Google Scholar]
  39. TirmanS. CybullaE. QuinetA. MeroniA. VindigniA. PRIMPOL ready, set, reprime!Crit. Rev. Biochem. Mol. Biol.2021561173010.1080/10409238.2020.184108933179522
    [Google Scholar]
  40. CloutierS. HamelH. ChampagneM. YotovW.V. Mapping of the human DNA primase 1 (PRIM1) to chromosome 12q13.Genomics199743339840110.1006/geno.1997.48339268648
    [Google Scholar]
  41. VaithiyalingamS. WarrenE.M. EichmanB.F. ChazinW.J. Insights into eukaryotic DNA priming from the structure and functional interactions of the 4Fe-4S cluster domain of human DNA primase.Proc. Natl. Acad. Sci. USA201010731136841368910.1073/pnas.100200910720643958
    [Google Scholar]
  42. AreziB. KirkB.W. CopelandW.C. KuchtaR.D. Interactions of DNA with human DNA primase monitored with photoactivatable cross-linking agents: Implications for the role of the p58 subunit.Biochemistry19993839128991290710.1021/bi990899110504261
    [Google Scholar]
  43. LericheM. BonnetC. JanaJ. ChhetriG. MennourS. MartineauS. PennaneachV. BussoD. VeauteX. BertrandP. LambertS. SomyajitK. UguenP. VagnerS. 53BP1 interacts with the RNA primer from Okazaki fragments to support their processing during unperturbed DNA replication.Cell Rep.2023421111341210.1016/j.celrep.2023.11341237963016
    [Google Scholar]
  44. ZerbeL.K. KuchtaR.D. The p58 subunit of human DNA primase is important for primer initiation, elongation, and counting.Biochemistry200241154891490010.1021/bi016030b11939784
    [Google Scholar]
  45. O’BrienE. HoltM.E. SalayL.E. ChazinW.J. BartonJ.K. Substrate binding regulates redox signaling in human DNA primase.J. Am. Chem. Soc.201814049171531716210.1021/jacs.8b0991430433774
    [Google Scholar]
  46. ParryD.A. Tamayo-OrregoL. CarrollP. MarshJ.A. GreeneP. MurinaO. UggentiC. LeitchA. KáposztaR. MerőG. NagyA. OrlikB. Kovács-PászthyB. QuigleyA.J. RiszterM. RankinJ. ReijnsM.A.M. SzakszonK. JacksonA.P. PRIM1 deficiency causes a distinctive primordial dwarfism syndrome.Genes Dev.20203421-221520153310.1101/gad.340190.12033060134
    [Google Scholar]
  47. GuoZ. GuoL. YAP/TEAD-induced PRIM1 contributes to the progression and poor prognosis of gastric carcinoma.Transl. Oncol.20233810179110.1016/j.tranon.2023.10179137741096
    [Google Scholar]
  48. TakeuchiS. KasamatsuA. YamatojiM. NakashimaD. Endo-SakamotoY. KoideN. TakaharaT. ShimizuT. IyodaM. OgawaraK. ShiibaM. TanzawaH. UzawaK. TEAD4-YAP interaction regulates tumoral growth by controlling cell-cycle arrest at the G1 phase.Biochem. Biophys. Res. Commun.2017486238539010.1016/j.bbrc.2017.03.05028315328
    [Google Scholar]
  49. ZabradyK. LiA.W.H. DohertyA.J. Mechanism of primer synthesis by Primase-Polymerases.Curr. Opin. Struct. Biol.20238210265210.1016/j.sbi.2023.10265237459807
    [Google Scholar]
  50. BianchiJ. RuddS.G. JozwiakowskiS.K. BaileyL.J. SouraV. TaylorE. StevanovicI. GreenA.J. StrackerT.H. LindsayH.D. DohertyA.J. PrimPol bypasses UV photoproducts during eukaryotic chromosomal DNA replication.Mol. Cell201352456657310.1016/j.molcel.2013.10.03524267451
    [Google Scholar]
  51. MourónS. Rodriguez-AcebesS. Martínez-JiménezM.I. García-GómezS. ChocrónS. BlancoL. MéndezJ. Repriming of DNA synthesis at stalled replication forks by human PrimPol.Nat. Struct. Mol. Biol.201320121383138910.1038/nsmb.271924240614
    [Google Scholar]
  52. YanY. XuZ. HuangJ. GuoG. GaoM. KimW. ZengX. KloeberJ.A. ZhuQ. ZhaoF. LuoK. LouZ. The deubiquitinase USP36 Regulates DNA replication stress and confers therapeutic resistance through PrimPol stabilization.Nucleic Acids Res.20204822127111272610.1093/nar/gkaa109033237263
    [Google Scholar]
  53. da CostaA.A.B.A. ChowdhuryD. ShapiroG.I. D’AndreaA.D. KonstantinopoulosP.A. Targeting replication stress in cancer therapy.Nat. Rev. Drug Discov.2023221385810.1038/s41573‑022‑00558‑536202931
    [Google Scholar]
  54. BeroukhimR. MermelC.H. PorterD. WeiG. RaychaudhuriS. DonovanJ. BarretinaJ. BoehmJ.S. DobsonJ. UrashimaM. Mc HenryK.T. PinchbackR.M. LigonA.H. ChoY.J. HaeryL. GreulichH. ReichM. WincklerW. LawrenceM.S. WeirB.A. TanakaK.E. ChiangD.Y. BassA.J. LooA. HoffmanC. PrensnerJ. LiefeldT. GaoQ. YeciesD. SignorettiS. MaherE. KayeF.J. SasakiH. TepperJ.E. FletcherJ.A. TaberneroJ. BaselgaJ. TsaoM.S. DemichelisF. RubinM.A. JanneP.A. DalyM.J. NuceraC. LevineR.L. EbertB.L. GabrielS. RustgiA.K. AntonescuC.R. LadanyiM. LetaiA. GarrawayL.A. LodaM. BeerD.G. TrueL.D. OkamotoA. PomeroyS.L. SingerS. GolubT.R. LanderE.S. GetzG. SellersW.R. MeyersonM. The landscape of somatic copy-number alteration across human cancers.Nature2010463728389990510.1038/nature0882220164920
    [Google Scholar]
  55. GaillardH. García-MuseT. AguileraA. Replication stress and cancer.Nat. Rev. Cancer201515527628910.1038/nrc391625907220
    [Google Scholar]
  56. DengL. ThakurA. PengJ. SongL. LiZ. Multi-omics analysis of DNA replication-associated primase polymerase (PRIMPOL) in pan-cancer: a potential target for prognosis and immune response.Eur. J. Med. Res.202328120710.1186/s40001‑023‑01181‑937391787
    [Google Scholar]
  57. Díaz-TalaveraA. Montero-CondeC. Leandro-GarcíaL. RobledoM. PrimPol: A breakthrough among DNA replication enzymes and a potential new target for cancer therapy.Biomolecules202212224810.3390/biom1202024835204749
    [Google Scholar]
  58. DaiT. LiJ. LuX. YeL. YuH. ZhangL. DengM. ZhuS. LiuW. WangG. YangY. Prognostic role and potential mechanisms of the ferroptosis-related metabolic gene signature in hepatocellular carcinoma.Pharm. Genomics Pers. Med.20211492794510.2147/PGPM.S31952434377010
    [Google Scholar]
  59. EdgarR. DomrachevM. LashA.E. Gene expression omnibus: NCBI gene expression and hybridization array data repository.Nucleic Acids Res.200230120721010.1093/nar/30.1.20711752295
    [Google Scholar]
  60. LianQ. WangS. ZhangG. WangD. LuoG. TangJ. ChenL. GuJ. HCCDB: A database of hepatocellular carcinoma expression atlas.Gen. Proteomics Bioinforma.201816426927510.1016/j.gpb.2018.07.00330266410
    [Google Scholar]
  61. ZhuM. WuM. BianS. SongQ. XiaoM. HuangH. YouL. ZhangJ. ZhangJ. ChengC. NiW. ZhengW. DNA primase subunit 1 deteriorated progression of hepatocellular carcinoma by activating AKT/mTOR signaling and UBE2C-mediated P53 ubiquitination.Cell Biosci.20211114210.1186/s13578‑021‑00555‑y33622397
    [Google Scholar]
  62. ZhangY. LiL. LiuR. ZengC. DNA primase subunit 1 expression in hepatocellular carcinoma and its clinical implication.BioMed Res. Int.2020202011210.1155/2020/968931232908930
    [Google Scholar]
  63. LoP.K. LeeJ.S. LiangX. SukumarS. The dual role of FOXF2 in regulation of DNA replication and the epithelial-mesenchymal transition in breast cancer progression.Cell. Signal.201628101502151910.1016/j.cellsig.2016.06.02127377963
    [Google Scholar]
  64. AlbogamiS. AlnefaieA. Role of amygdalin in blocking DNA replication in breast cancer in vitro.Curr. Pharm. Biotechnol.202122121612162710.2174/138920102266621020312380333535947
    [Google Scholar]
  65. PaulsenR. CimprichK. The ATR pathway: Fine-tuning the fork.DNA Repair (Amst.)20076795396610.1016/j.dnarep.2007.02.01517531546
    [Google Scholar]
  66. JobA. SchmittL.M. von WenserskiL. Lankat-ButtgereitB. GressT.M. BuchholzM. GallmeierE. Inactivation of PRIM1 function sensitizes cancer cells to ATR and CHK1 inhibitors.Neoplasia201820111135114310.1016/j.neo.2018.08.00930257222
    [Google Scholar]
  67. LiuD. ZhangX.X. XiB.X. WanD.Y. LiL. ZhouJ. WangW. MaD. WangH. GaoQ.L. Sine oculis homeobox homolog 1 promotes DNA replication and cell proliferation in cervical cancer.Int. J. Oncol.20144531232124010.3892/ijo.2014.251024970368
    [Google Scholar]
  68. JonesM.L. AriaV. BarisY. YeelesJ.T.P. How Pol α-primase is targeted to replisomes to prime eukaryotic DNA replication.Mol. Cell2023831629112924.e1610.1016/j.molcel.2023.06.03537506699
    [Google Scholar]
  69. DaiX. ZhangX. ChenW. ChenY. ZhangQ. MoS. LuJ. Dihydroartemisinin: A potential natural anticancer drug.Int. J. Biol. Sci.202117260362210.7150/ijbs.5036433613116
    [Google Scholar]
  70. ZengZ. ChenD. ChenL. HeB. LiY. A comprehensive overview of Artemisinin and its derivatives as anticancer agents.Eur. J. Med. Chem.202324711500010.1016/j.ejmech.2022.11500036538859
    [Google Scholar]
  71. SuX.Z. MillerL.H. The discovery of artemisinin and the Nobel Prize in Physiology or Medicine.Sci. China Life Sci.201558111175117910.1007/s11427‑015‑4948‑726481135
    [Google Scholar]
  72. StockwellB.R. Friedmann AngeliJ.P. BayirH. BushA.I. ConradM. DixonS.J. FuldaS. GascónS. HatziosS.K. KaganV.E. NoelK. JiangX. LinkermannA. MurphyM.E. OverholtzerM. OyagiA. PagnussatG.C. ParkJ. RanQ. RosenfeldC.S. SalnikowK. TangD. TortiF.M. TortiS.V. ToyokuniS. WoerpelK.A. ZhangD.D. Ferroptosis: A regulated cell death nexus linking metabolism, redox biology, and disease.Cell2017171227328510.1016/j.cell.2017.09.02128985560
    [Google Scholar]
  73. KlemmS.L. ShiponyZ. GreenleafW.J. Chromatin accessibility and the regulatory epigenome.Nat. Rev. Genet.201920420722010.1038/s41576‑018‑0089‑830675018
    [Google Scholar]
  74. LiY. XuF. ChenF. ChenY. GeD. ZhangS. LuC. Transcriptomics based multi-dimensional characterization and drug screen in esophageal squamous cell carcinoma.EBioMedicine20217010351010.1016/j.ebiom.2021.10351034365093
    [Google Scholar]
  75. ChenQ. GuoH. ZongY. ZhaoX. Curcumin restrains hepatocellular carcinoma progression depending on the regulation of the circ_0078710/miR-378b/PRIM2 axis.J. Recept. Signal Transduct. Res.202242331332410.1080/10799893.2021.193655434139933
    [Google Scholar]
  76. ArbynM. WeiderpassE. BruniL. de SanjoséS. SaraiyaM. FerlayJ. BrayF. Estimates of incidence and mortality of cervical cancer in 2018: a worldwide analysis.Lancet Glob. Health202082e191e20310.1016/S2214‑109X(19)30482‑631812369
    [Google Scholar]
  77. MaH. LiuZ. LiH. GuoX. GuoS. QuP. WangY. YangJ. Bioinformatics analysis reveals MCM3 as an important prognostic marker in cervical cancer.Comput. Math. Methods Med.2021202111010.1155/2021/849426034671420
    [Google Scholar]
  78. YangM.Y. LinP.M. YangC.H. HuM.L. ChenI.Y. LinS.F. HsuC.M. Loss of ZNF215 imprinting is associated with poor five-year survival in patients with cytogenetically abnormal-acute myeloid leukemia.Blood Cells Mol. Dis.20219010257710.1016/j.bcmd.2021.10257734091126
    [Google Scholar]
  79. MossR.M. SorajjaN. MillsL.J. MoertelC.L. HoangT.T. SpectorL.G. LargaespadaD.A. WilliamsL.A. Sex differences in methylation profiles are apparent in medulloblastoma, particularly among SHH tumors.Front. Oncol.202313111312110.3389/fonc.2023.111312137035203
    [Google Scholar]
  80. SunR. ShaoX. AkterF. ZahidK.R. YaoS. MaL. XuG. PRIM2: A Marker of MYC-driven Hyper-proliferation, Disease Progression, Tumor Aggressiveness and Poor Survival in Glioma Patients.Cancer Genomics Proteomics202421218620210.21873/cgp.2044038423596
    [Google Scholar]
  81. EdwardsL. GuptaR. FilippF.V. Hypermutation of DPYD Deregulates Pyrimidine Metabolism and Promotes Malignant Progression.Mol. Cancer Res.201614219620610.1158/1541‑7786.MCR‑15‑040326609109
    [Google Scholar]
  82. KuC.R. LimH. LeeY.J. KimS.H. KimD. KimS.H. LeeM.K. BangD. LeeE.J. Novel somatic variants involved in biochemical activity of pure growth hormone-secreting pituitary adenoma without GNAS variant.Sci. Rep.20211111653010.1038/s41598‑021‑95829‑334400688
    [Google Scholar]
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  • Article Type:
    Review Article
Keyword(s): cancer; cell cycle; DNA primase; DNA replication; PRIM1; PRIM2
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