The Journal of Contemporary Dental Practice

Register      Login

SEARCH WITHIN CONTENT

FIND ARTICLE

Volume / Issue

Online First

Archive
Related articles

VOLUME 23 , ISSUE 2 ( February, 2022 ) > List of Articles

REVIEW ARTICLE

Nanopore Sequencing Technology in Oral Oncology: A Comprehensive Insight

Vanishri C Haragannavar, Afrah Yousef, Neethi Gujjar, Suman Kashyap

Keywords : Epigenetics, Genomics, Nanopore sequencing, Oral cancer, Third-generation sequencing

Citation Information : Haragannavar VC, Yousef A, Gujjar N, Kashyap S. Nanopore Sequencing Technology in Oral Oncology: A Comprehensive Insight. J Contemp Dent Pract 2022; 23 (2):268-275.

DOI: 10.5005/jp-journals-10024-3240

License: CC BY-NC 4.0

Published Online: 10-06-2022

Copyright Statement:  Copyright © 2022; The Author(s).


Abstract

Aim: To review the principles and application of Nanopore Sequencing Technology (NPST) in oral cancer. Background: Oral cancer is a disease caused by aberrations in the genes. Substantial research at the genomic level is still required for in-depth understanding of the molecular mechanism in oral cancer. The advent of the novel nanopore sequencing technique has the potential to detect the alterations at the genomic level. This review highlights nanopore sequencing, its advantages and disadvantages, and how research supports its application in the field of oral oncology. Materials and methods: Web-based search via PubMed database, internet sources using keywords “nanopore sequencing, third-generation sequencing, next generation sequencing, cancer, oral squamous cell carcinoma, genetic, epigenetic, oncogenic viruses” was performed in this review. Original research, reviews, and short discussions published from 2008 to 2020 were included. The findings are discussed with emphasis on common gene mutations, epigenetic alterations, and oncogenic viruses in oral cancer. A brief mention regarding translational nanopore sequencing research in oral cancer and future perspectives is also discussed. Results: The results obtained reveal that cost-effectiveness and rapid turnaround time make nanopore sequencing an enticing platform to resolve the ambiguity of genomes, epigenomes, and transcriptomes. Conclusion: The findings will encourage researchers to further adopt NPST in their studies and give an overview of the latest findings of oral squamous cell carcinoma (OSCC) management. To highlight the importance of NPST application in OSCC studies, this paper not only discusses the use of NPST in identifying the behavior of malignancy but also implies the need for further research using this technique. Clinical significance: The review suggests that nanopore sequencing can be utilized for diagnosis and achieving personalized treatment in each oral cancer patient.


HTML PDF Share
  1. Kim S, Lee JW, Park YS. The application of next-generation sequencing to define factors related to oral cancer and discover novel biomarkers. Life (Basel) 2020;10(10):228. DOI: 10.3390/life10100228.
  2. Sakamoto Y, Sereewattanawoot S, Suzuki A. A new era of long-read sequencing for cancer genomics. J Hum Genet 2020;65:3–10. DOI: 10.1038/s10038-019-0658-5.
  3. Rizzo G, Black M, Mymryk JS, et al. Defining the genomic landscape of head and neck cancers through next-generation sequencing. Oral Dis 2015;21(1):e11–e24. DOI: 10.1111/odi.12246.
  4. Xiao T, Zhou W. The third generation sequencing: the advanced approach to genetic diseases. Transl Pediatr 2020;9(2):163–173. DOI: 10.21037/tp.2020.03.06.
  5. Liu L, Li Y, Li S, et al. Comparison of next-generation sequencing systems. Biomed Res Int 2012;2012:251364. DOI: 10.1155/2012/251364.
  6. Sun X, Song L, Yang W, et al. Nanopore Sequencing and its clinical applications. Methods Mol Biol 2020;2204:13–32. DOI: 10.1007/978-1-0716-0904-0_2.
  7. Petersen LM, Martin IW, Moschetti WE, et al. Third-generation sequencing in the clinical laboratory: exploring the advantages and challenges of nanopore sequencing. J Clin Microbiol 2020;58(1):e01315–e01319. DOI: 10.1128/JCM.01315-19.
  8. Kamps R, Brandao RD, Van Den Bosch BJ, et al. Next-generation sequencing in oncology: genetic diagnosis, risk prediction and cancer classification. Int J Mol Sci 2017;18(2):308. DOI: 10.3390/ijms18020308.
  9. Kono N, Arakawa K. Nanopore sequencing: review of potential applications in functional genomics. Dev Growth Differ 2019;61(5):316–326. DOI: 10.1111/dgd.12608.
  10. Feng Y, Zhang Y, Ying C, et al. Nanopore-based fourth-generation DNA sequencing technology. Genomics Proteomics Bioinformatics 2015;13(1):4–16. DOI: 10.1016/j.gpb.2015.01.009.
  11. Wang Y, Yang Q, Wang Z. The evolution of nanopore sequencing. Front Genet 2014;5:449. DOI: 10.3389/fgene.2014.00449.
  12. Kchouk M, Gibrat JF, Elloumi M. Generations of sequencing technologies: from first to next generation. Biol Med (Aligarh) 2017;9(3):395. DOI: 10.4172/0974-8369.1000395.
  13. Haque F, Li J, Wu HC, et al. Solid-state and biological nanopore for real-time sensing of single chemical and sequencing of DNA. Nano Today 2013;8(1):56–74. DOI: 10.1016/j.nantod.2012.12.008.
  14. Heather JM, Chain B. The sequence of sequencers: the history of sequencing DNA. Genomics 2016;107(1):1–8. DOI: 10.1016/j.ygeno.2015.11.003
  15. Van Dijk EL, Jaszczyszyn Y, Naquin D, et al. The third revolution in sequencing technology. Trends Genet 2018;34(9):666–681. DOI: 10.1016/j.tig.2018.05.008.
  16. Li J, Wang H, Mao L, et al. Rapid genomic characterization of SARS-CoV-2 viruses from clinical specimens using nanopore sequencing. Sci Rep 2020;10(1):17492. DOI: 10.1038/s41598-020-74656-y.
  17. Bull RA, Adikari TN, Ferguson JM, et al. Analytical validity of nanopore sequencing for rapid SARS-CoV-2 genome analysis. Nat Commun 2020;11(1):6272. DOI: 10.1038/s41467-020-20075-6.
  18. Oxford Nanopore Technologies. Two new papers further demonstrate the role adaptive sampling could play in understanding genetic diseases. 2020. Available from: https://www.nanoporetech.com.
  19. Kovaka S, Fan Y, Ni B, et al. Targeted nanopore sequencing by real-time mapping of raw electrical signal with UNCALLED. Nat Biotechnol 2021;39(4):431. PMID: 33257863.
  20. Payne A, Holmes N, Clarke T, et al. Readfish enables targeted nanopore sequencing of gigabase-sized genomes. Nat Biotechnol 2021;39(4):442–450. PMID:33257864
  21. Dutta UR, Rao SN, Pidugu VK, et al. Breakpoint mapping of a novel de novo translocation t(X;20) (q11.1;p13) by positional cloning and long read sequencing. Genomics 2019;111(5):1108–1114. DOI: 10.1016/j.ygeno.2018.07.005.
  22. Salahshourifar I, Chong VKV, Kallarakkal TG, et al. Genomic DNA copy number alterations from precursor oral lesions to oral squamous cell carcinoma. Oral Oncol 2014;50(5):404–412. DOI: 10.1016/j.oraloncology.2014.02.005.
  23. Ali J, Sabiha B, Jan HU, et al. Genetic etiology of oral cancer. Oral Oncol 2017;70:23–28. DOI: 10.1016/j.oraloncology.2017.05.004.
  24. Noguti J, De Moura CFG, De Jesus GPP, et al. Metastasis from oral cancer: an overview. Cancer Genomics Proteomics 2012;9(5):329–335. PMID: 22990112.
  25. Muller S, Pan Y, Li R, et al. Changing trends in oral squamous cell carcinoma with particular reference to young patients: 1971–2006. The Emory University experience. Head Neck Pathol 2008;2(2):60–66. DOI: 10.1007/s12105-008-0054-5.
  26. Patel SC, Carpenter WR, Tyree S, et al. Increasing incidence of oral tongue squamous cell carcinoma in young white women, age 18 to 44 years. J Clin Oncol 2011;29(11):1488–1494. DOI: 10.1200/JCO.2010.31.7883.
  27. Faden DL, Arron ST, Heaton CM, et al. Targeted next-generation sequencing of TP53 in oral tongue carcinoma from nonsmokers. J Otolaryngol Head Neck Surg 2016;45(1):47. DOI: 10.1186/s40463-016-0160-4.
  28. Kumar M, Nanavati R, Modi TG, et al. Oral cancer: etiology and risk factors: a review. J Cancer Res Therapeut 2016;12(2):458–463. DOI: 10.4103/0973-1482.186696.
  29. Pickering CR, Zhang J, Yoo SK, et al. Integrative genomic characterization of oral squamous cell carcinoma identifies frequent somatic drivers. Cancer Discov 2013;3(7):770–781. DOI: 10.1158/2159-8290.CD-12-0537.
  30. Zhang L, Meng X, Zhu XW, et al. Long non-coding RNAs in oral squamous cell carcinoma: biologic function, mechanisms and clinical implications. Mol Cancer 2019;18(1):102. DOI: 10.1186/s12943-019-1021-3.
  31. Song X, Xia R, Li J, et al. Common and complex Notch1 mutations in Chinese oral squamous cell carcinoma. Clin Cancer Res 2014;20(3):701–710. DOI: 10.1158/1078-0432.CCR-13-1050.
  32. Izumchenko E, Sun K, Jones S, et al. Notch1 mutations are drivers of oral tumorigenesis. Cancer Prev Res 2014;8(4):277–286. DOI: 10.1158/1940-6207.CAPR-14-0257.
  33. Nakagaki T, Tamura M, Kobashi K, et al. Targeted next-generation sequencing of 50 cancer-related genes in Japanese patients with oral squamous cell carcinoma. Tumor Biol 2018;4(9):1010428318800180. DOI: 10.1177/1010428318800180.
  34. Nakagaki T, Tamura M, Kobashi K, et al. Profiling cancer-related gene mutations in oral squamous cell carcinoma from Japanese patients by targeted amplicon sequencing. Oncotarget 2017;8(35):59113–59122. DOI: 10.18632/oncotarget.19262.
  35. Jayaprakash C, Varghese VK, Jayaram P, et al. Relevance and actionable mutational spectrum in oral squamous cell carcinoma. J Oral Pathol Med 2020;49(5):427–434. DOI: 10.1111/jop.12985.
  36. Ma J, Fu Y, Tu YY, et al. Mutation allele frequency threshold does not affect prognostic analysis using next generation sequencing in oral squamous cell carcinoma. BMC Cancer 2018;18(1):758. DOI: 10.1186/s12885-018-4481-8.
  37. Er TK, Wang YY, Chen CC, et al. Molecular characterization of oral squamous cell carcinoma using targeted next-generation sequencing. Oral Dis 2015;21(7):872–878. DOI: 10.1111/odi.12357.
  38. Batta N, Pandey M. Mutational spectrum of tobacco associated oral squamous carcinoma and its therapeutic significance. World J Surg Oncol 2019;17(1):198. DOI: 10.1186/s12957-019-1741-2.
  39. Chen TW, Lee CC, Liu H, et al. APOBEC3A is an oral cancer prognostic biomarker in Taiwanese carriers of an APOBEC deletion polymorphism. Nat. Commun 2017;8(1):465. DOI: 10.1038/s41467-017-00493-9.
  40. Oikawa Y, Morita KI, Kayamori K, et al. Receptor tyrosine kinase amplification is predictive of distant metastasis in patients with oral squamous cell carcinoma. Cancer Sci 2017;108(2):256–266. DOI: 10.1111/cas.13126.
  41. van Ginkel JH, de Leng WWJ, de Bree R, et al. Targeted sequencing reveals TP53 as a potential diagnostic biomarker in the post-treatment surveillance of head and neck cancer. Oncotarget 2016;7(38)61575–61586. DOI: 10.18632/oncotarget.11196.
  42. Chen SJ, Liu H, Liao CT, et al. Ultra-deep targeted sequencing of advanced oral squamous cell carcinoma identifies a mutation-based prognostic gene signature. Oncotarget 2015;6(20):18066–18080. DOI: 10.18632/oncotarget.3768.
  43. Baylin SB, Jones PA. Epigenetic determinants of cancer. Cold Spring Harb Perspect Biol 2016;8(9):a019505. DOI: 10.1101/cshperspect.a019505.
  44. Michael C Schatz. Nanopore sequencing meets epigenetics. Nat Methods 2017;14(4):347–348. DOI: 10.1038/nmeth.4240.
  45. Mascolo M, Siano M, Ilardi G, et al. Epigenetic disregulation in oral cancer. Int J Mol Sci 2012;13(2):2331–2353. DOI: 10.3390/ijms13022331.
  46. Gomes CC, Gomez RS. MicroRNA and oral cancer: future perspectives. Oral Oncol 2008;44(10):910–914. DOI: 10.1016/j.oraloncology.2008.01.002.
  47. Eljabo N, Nikolic N, Carkic J, et al. Genetic and epigenetic alterations in the tumour, tumour margins, and normal buccal mucosa of patients with oral cancer. Int J Oral Maxillofac Surg 2018;47(8):976–982. DOI: 10.1016/j.ijom.2018.01.020.
  48. Wang H, Peng R, Wang J, et al. Circulating microRNAs as potential cancer biomarkers: the advantage and disadvantage. Clin Epigenetics 2018;10:59. DOI: 10.1186/s13148-018-0492-1.
  49. Yan Y, Wang X, Veno MT, et al. Circulating miRNAs as biomarkers for oral squamous cell carcinoma recurrence in operated patients. Oncotarget 2017;8(5):8206–8214. DOI: 10.18632/oncotarget.14143.
  50. Hillbertz NS, Hirsch JM, Jalouli J, et al. Viral and molecular aspects of oral cancer. Anticancer Res 2012;32(10):4201–4212. PMID: 23060540.
  51. Metgud R, Astekar M, Verma M, et al. Role of viruses in oral squamous cell carcinoma. Oncol Rev 2012;6(2):e21. DOI: 10.4081/oncol.2012.e21.
  52. Chaitanya NC, Allam NS, Gandhi Babu DB, et al. Systematic meta-analysis on association of human papilloma virus and oral cancer. J Cancer Res Ther 2016;12(2):969–974. DOI: 10.4103/0973-1482.179098.
  53. Kim SM. Human papilloma virus in oral cancer. J Korean Assoc Oral Maxillofac Surg 2016;42(6):327–336. DOI: 10.5125/jkaoms.2016.42.6.327.
  54. Loman NJ, Quick J, Simpson JT. A complete bacterial genome assembled de novo using only nanopore sequencing data. Nat Methods 2015;12(8):733–735. DOI: 10.1038/nmeth.3444.
  55. Magi A, Giusti B, Tattini L. Characterization of MinION nanopore data for resequencing analyses. Briefings Bioinform 2017;18(6):940–953. DOI: 10.1093/bib/bbw077.
  56. Brown BL, Watson M, Minot SS, et al. MinIONTM nanopore sequencing of environmental metagenomes: a synthetic approach. GigaScience 2017;6(3):1–10. DOI: 10.1093/gigascience/gix007.
  57. Greninger AL, Naccache SN, Federman S, et al. Rapid metagenomic identification of viral pathogens in clinical samples by real-time nanopore sequencing analysis. Genome Med 2015;7:99. DOI: 10.1186/s13073-015-0220-9.
  58. Depledge DP, Srinivas KP, Sadaoka T, et al. Direct RNA sequencing on nanopore arrays redefines the transcriptional complexity of a viral pathogen. Nature Commun 2019;10(1):754. DOI: 10.1038/s41467-019-08734-9.
  59. Yang M, Cousineau A, Liu X, et al. Direct metatranscriptome RNA-seq and multiplex RT-PCR amplicon sequencing on nanopore MinION–promising strategies for multiplex identification of viable pathogens in food. Front Microbiol 2020;11:514. DOI: 10.3389/fmicb.2020.00514.
  60. Kilianski A, Roth PA, Liem AT, et al. Use of unamplified RNA/cDNA–hybrid nanopore sequencing for rapid detection and characterization of rna viruses. Emerg Infect Dis 2016;22(8):1448–1451. DOI: 10.3201/eid2208.160270.
  61. Laszloa AH, Derringtona IM, Brinkerhoffa H, et al. Detection and mapping of 5-methylcytosine and 5-hydroxymethylcytosine with nanopore MspA. Proc Natl Acad Sci USA 2013;110(47):18904–18909. DOI: 10.1073/pnas.1310240110.
  62. Santos A, van Aerle R, Barrientos L, et al. Computational methods for 16S metabarcoding studies using Nanopore sequencing data. Comput Struct Biotechnol J 2010;18:296–305. DOI: 10.1016/j.csbj.2020.01.005.
  63. Calus ST, Ijaz UZ, Pinto AJ. NanoAmpli-Seq: a workflow for amplicon sequencing for mixed microbial communities on the nanopore sequencing platform. GigaScience 2018;7(12):1–16. DOI: 10.1093/gigascience/giy140.
  64. Ku C, Roukos DH. From next-generation sequencing to nanopore sequencing technology: paving the way to personalized genomic medicine. Expert Rev Med Devices 2013;10(1):1–6. DOI: 10.1586/erd.12.63.
  65. LeBlanc VG, Marra MA. Next-generation sequencing approaches in cancer: where have they brought us and where will they take us? Cancers (Basel) 2015;7(3):1925–1958. DOI: 10.3390/cancers7030869.
  66. Supic G, Kozomara R, Jovic N, et al. Prognostic significance of tumor related genes hypermethylation detected in cancer-free surgical margins of oral squamous cell carcinomas. Oral Oncol 2011;47(8): 702–708. DOI: 10.1016/j.oraloncology.2011.05.014.
  67. Kaur J, Demokan S, Tripathi SC, et al. Pro-moter hypermethylation in Indian primary oral squamous cell carcinoma. Int J Cancer 2010;127(10):2367–2373. DOI: 10.1002/ijc.25377.
  68. Suzuki A, Suzuki M, Sugano JM, et al. Sequencing and phasing cancer mutations in lung cancers using a long-read portable sequencer. DNA Res 2017;24(6):585–596. DOI: 10.1093/dnares/dsx027.
  69. Sharma N, Annigeri RG. Translational research in oral cancer: a challenging key step in moving from bench to bedside. J Can Res Ther 2018;14(2):245–248. DOI: 10.4103/0973-1482.183556.
  70. Gupta P, Sivasankari P. Specific role of targeted molecular therapy in treatment of oral squamous cell carcinoma. Oncobiol Targets 2017;4:511575. DOI: 10.18639/ONBT.2017.04.511575.
  71. Ketabat F, Pundir M, Mohabatpour F, et al. Controlled drug delivery systems for oral cancer treatment—current status and future perspectives. Pharmaceutics 2019;11(7):302. DOI: 10.3390/pharmaceutics11070302.
  72. Tsai LL, Yu CC, Lo JF, et al. Enhanced cisplatin resistance in oral-cancer stem-like cells is correlated with upregulation of excision-repair cross-complementation group 1. J Dent Sci 2012;7(2):111–117. DOI: 10.1016/j.jds.2012.03.006.
  73. Euskirchen P, Bielle F, Labreche K, et al. Same-day genomic and epigenomic diagnosis of brain tumors using real-time nanopore sequencing. Acta Neuropathol 2017;134(5):691–703. DOI: 10.1007/s00401-017-1743-5.
  74. Ma S, Yang J, Wang W, et al. Simultaneous detection and comprehensive analysis of HPV and microbiome status of a cervical liquid-based cytology sample using Nanopore MinION sequencing. Sci Rep 2019;9(1):19337. DOI: 10.1038/s41598-019-55843-y.
  75. Minervini CF, Cumbo C, Orsini P, et al. Nanopore sequencing in blood diseases: a wide range of opportunities. Front Genet 2020;11:76. DOI: 10.3389/fgene.2020.00076.
  76. Aminuddin A, Ng PY, Leong CO, et al. Mitochondrial DNA alterations may influence the cisplatin responsiveness of oral squamous cell carcinoma. Sci Rep 2020;10(1):7885. DOI: 10.1038/s41598-020-64664-3.
  77. Wongsurawat T, Nakagawa M, Atiq O, et al. An assessment of Oxford Nanopore sequencing for human gut metagenome profiling: a pilot study of head and neck cancer patients. J Microbiol Methods 2019;166:105739. DOI: 10.1016/j.mimet.2019.105739.
  78. Marcozzi A, Jager M, Elferink M, et al. Accurate detection of circulating tumor DNA using nanopore consensus sequencing. NPJ genomic medicine 2021;6(1):1–1. DOI: 10.1038/s41525-021-00272-y.
  79. Rang FJ, Kloosterman WP, de Ridder J. From squiggle to basepair: computational approaches for improving nanopore sequencing read accuracy. Genome Biol 2018;19(1):90. DOI: 10.1186/s13059-018-1462-9.
  80. James P, Stoddart D, Harrington ED, et al. LamPORE: rapid, accurate and highly scalable molecular screening for SARS-CoV-2 infection, based on nanoporesequencing. medRxiv 2020. DOI: 10.1101/2020.08.07.20161737.
  81. Peto L, Rodger G, Carter DP, et al. Diagnosis of SARS-CoV-2 infection with LamPORE, a high throughput platform combining loop-mediated isothermal amplification and nanopore sequencing. Journal of Clinical Microbiology 2021;59(6):e03271-20. DOI: 10.1101/2020.09.18.20195370.
  82. Oxford Nanopore Technologies. AT NCM announcements include single-read accuracy of 99.1% on new chemistry and sequencing a record 10Tb in a single PromethION run. 2020. Available from: https://www.nanoporetech.com.
  83. Stangl C, de Blank S, Renkens I, et al. Partner independent fusion gene detection by multiplexed CRISPR-Cas9 enrichment and long read nanopore sequencing. Nat Commun 2020;11(1):2861. DOI: 10.1038/s41467-020-16641-7.
  84. Makalowski W, Shabardina V. Bioinformatics of nanopore sequencing. J Hum Genet 2020;65(1):61–67. DOI: 10.1038/s10038-019-0659-4.
PDF Share
PDF Share

© Jaypee Brothers Medical Publishers (P) LTD.