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Journal of Biomedicine and Biotechnology
Volume 2006, Article ID 83672, 12 pages
http://dx.doi.org/10.1155/JBB/2006/83672
Review Article

L1 Retrotransposons in Human Cancers

Department of Urology, Heinrich Heine University, Mooreustrasse 5, Düsseldorf 40225, Germany

Received 31 August 2005; Accepted 16 October 2005

Copyright © 2006 Wolfgang A. Schulz. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Citations to this Article [69 citations]

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  • U. Moens, M. Van Ghelue, and M. Johannessen, “Oncogenic potentials of the human polyomavirus regulatory proteins,” Cellular and Molecular Life Sciences, vol. 64, no. 13, pp. 1656–1678, 2007. View at Publisher · View at Google Scholar
  • C. Daniel Eller, Moira Regelson, Barry Merriman, Stan Nelson, Steve Horvath, and York Marahrens, “Repetitive sequence environment distinguishes housekeeping genes,” Gene, vol. 390, no. 1-2, pp. 153–165, 2007. View at Publisher · View at Google Scholar
  • Lara S. Collier, and David A. Largaespada, “Transposable elements and the dynamic somatic genome,” Genome Biology, vol. 8, 2007. View at Publisher · View at Google Scholar
  • S. S. Ryazansky, and V. A. Gvozdev, “Small RNAs and cancerogenesis,” Biochemistry-Moscow, vol. 73, no. 5, pp. 514–527, 2008. View at Publisher · View at Google Scholar
  • Alan Garen, and Xu Song, “Regulatory roles of tumor-suppressor proteins and noncoding RNA in cancer and normal cell functions,” International Journal Of Cancer, vol. 122, no. 8, pp. 1687–1689, 2008. View at Publisher · View at Google Scholar
  • J.D. Brown, D. Golden, and R.J. O'Neill, “Methylation perturbations in retroelements within the genome of a Mus interspecific hybrid correlate with double minute chromosome formation,” Genomics, vol. 91, no. 3, pp. 267–273, 2008. View at Publisher · View at Google Scholar
  • John L. Goodier, and Haig H. Kazazian, “Retrotransposons Revisited: The Restraint and Rehabilitation of Parasites,” Cell, vol. 135, no. 1, pp. 23–35, 2008. View at Publisher · View at Google Scholar
  • Chureerat Phokaew, Supakit Kowudtitham, Keskanya Subbalekha, Shanop Shuangshoti, and Apiwat Mutirangura, “LINE-1 methylation patterns of different loci in normal and cancerous cells,” Nucleic Acids Research, vol. 36, no. 17, pp. 5704–5712, 2008. View at Publisher · View at Google Scholar
  • Jennifer A. Rusiecki, Andrea Baccarelli, Valentina Bollati, Letizia Tarantini, Lee E. Moore, and Eva C. Bonefeld-Jorgensen, “Global DNA hypomethylation is associated with high serum-persistent organic pollutants in Greenlandic inuit,” Environmental Health Perspectives, vol. 116, no. 11, pp. 1547–1552, 2008. View at Publisher · View at Google Scholar
  • Rochat, “Importance of influx and efflux systems and xenobiotic metabolizing enzymes in intratumoral disposition of anticancer agents,” Current Cancer Drug Targets, vol. 9, no. 5, pp. 652–674, 2009. View at Publisher · View at Google Scholar
  • Diego E. Montoya-Durango, Yongqing Liu, Ivo Teneng, Ted Kalbfleisch, Mary E. Lacy, Marlene C. Steffen, and Kenneth S. Ramos, “Epigenetic control of mammalian LINE-1 retrotransposon by retinoblastoma proteins,” Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis, vol. 665, no. 1-2, pp. 20–28, 2009. View at Publisher · View at Google Scholar
  • Andrea Baccarelli, and Valentina Bollati, “Epigenetics and environmental chemicals,” Current Opinion in Pediatrics, vol. 21, no. 2, pp. 243–251, 2009. View at Publisher · View at Google Scholar
  • Alexandros Daskalos, Georgios Nikolaidis, George Xinarianos, Paraskevi Savvari, Adrian Cassidy, Roubini Zakopoulou, Athanasios Kotsinas, Vassilis Gorgoulis, John K. Field, and Triantafillos Liloglou, “Hypomethylation of retrotransposable elements correlates with genomic instability in non-small cell lung cancer,” International Journal Of Cancer, vol. 124, no. 1, pp. 81–87, 2009. View at Publisher · View at Google Scholar
  • Maria Berdasco, and Manel Esteller, “The Human Epigenome,” Molecular Pathology, pp. 151–163, 2009. View at Publisher · View at Google Scholar
  • Adam S. Wilkins, “The enemy within: An epigenetic role of retrotransposons in cancer initiation,” BioEssays, vol. 32, no. 10, pp. 856–865, 2010. View at Publisher · View at Google Scholar
  • Lisa Mirabello, Sharon A. Savage, Larissa Korde, Shahinaz M. Gadalla, and Mark H. Greene, “LINE-1 methylation is inherited in familial testicular cancer kindreds,” BMC Medical Genetics, vol. 11, no. 1, 2010. View at Publisher · View at Google Scholar
  • Yoshifumi Baba, Curtis Huttenhower, Katsuhiko Nosho, Noriko Tanaka, Kaori Shima, Aditi Hazra, Eva S. Schernhammer, David J. Hunter, Edward L. Giovannucci, Charles S. Fuchs, and Shuji Ogino, “Epigenomic diversity of colorectal cancer indicated by LINE-1 methylation in a database of 869 tumors,” Molecular Cancer, vol. 9, 2010. View at Publisher · View at Google Scholar
  • Jason P Ross, Keith N Rand, and Peter L Molloy, “Hypomethylation of repeated DNA sequences in cancer,” Epigenomics, vol. 2, no. 2, pp. 245–269, 2010. View at Publisher · View at Google Scholar
  • Andrea Baccarelli, Letizia Tarantini, Robert O Wright, Valentina Bollati, Augusto A. Litonjua, Antonella Zanobetti, David Sparrow, Pantel Vokonas, and Joel Schwartz, “Repetitive element dna methylation and circulating endothelial and inflammation markers in the VA normative aging study,” Epigenetics, vol. 5, no. 3, pp. 222–228, 2010. View at Publisher · View at Google Scholar
  • Atanu K. Khatua, Harry E. Taylor, James E. K. Hildreth, and Waldemar Popik, “Inhibition of LINE-1 and Alu retrotransposition by exosomes encapsidating APOBEC3G and APOBEC3F,” Virology, vol. 400, no. 1, pp. 68–75, 2010. View at Publisher · View at Google Scholar
  • Michiel B. Vandegehuchte, Filip Lemière, Lynn Vanhaecke, Wim Vanden Berghe, and Colin R. Janssen, “Direct and transgenerational impact on Daphnia magna of chemicals with a known effect on DNA methylation,” Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, vol. 151, no. 3, pp. 278–285, 2010. View at Publisher · View at Google Scholar
  • Atanu K. Khatua, Harry E. Taylor, James E.K. Hildreth, and Waldemar Popik, “Inhibition of LINE-1 and Alu retrotransposition by exosomes encapsidating APOBEC3G and APOBEC3F,” Virology, vol. 400, no. 1, pp. 68–75, 2010. View at Publisher · View at Google Scholar
  • Brunella Del Re, Pamela Marcantonio, Miriam Capri, and Gianfranco Giorgi, “Evaluation of LINE-1 mobility in neuroblastoma cells by in vitro retrotransposition reporter assay: FACS analysis can detect only the tip of the iceberg of the inserted L1 elements,” Experimental Cell Research, vol. 316, no. 20, pp. 3358–3367, 2010. View at Publisher · View at Google Scholar
  • S. Capomaccio, A. Verini-Supplizi, G. Galla, N. Vitulo, G. Barcaccia, M. Felicetti, M. Silvestrelli, and K. Cappelli, “Transcription of LINE-derived sequences in exercise-induced stress in horses,” Animal Genetics, vol. 41, pp. 23–27, 2010. View at Publisher · View at Google Scholar
  • Andrea Baccarelli, Robert Wright, Valentina Bollati, Augusto Litonjua, Antonella Zanobetti, Letizia Tarantini, David Sparrow, Pantel Vokonas, and Joel Schwartz, “Ischemic Heart Disease and Stroke in Relation to Blood DNA Methylation,” Epidemiology, vol. 21, no. 6, pp. 819–828, 2010. View at Publisher · View at Google Scholar
  • María Berdasco, and Manel Esteller, “Aberrant Epigenetic Landscape in Cancer: How Cellular Identity Goes Awry,” Developmental Cell, vol. 19, no. 5, pp. 698–711, 2010. View at Publisher · View at Google Scholar
  • Chris R. Harris, Robin Normart, Qifeng Yang, Elizabeth Stevenson, Bruce G. Haffty, Shridar Ganesan, Carlos Cordon-Cardo, Arnold J. Levine, and Laura H. Tang, “Association of nuclear localization of a long interspersed nuclear element-1 protein in breast tumors with poor prognostic outcomes,” Genes and Cancer, vol. 1, no. 2, pp. 115–124, 2010. View at Publisher · View at Google Scholar
  • Hongyan Zhu, Keyong Li, Jiren Liang, Jie Zhang, and Qing Wu, “Changes in the levels of DNA methylation in testis and liver of SD rats neonatally exposed to 5-aza-2 '-deoxycytidine and cadmium,” Journal Of Applied Toxicology, vol. 31, no. 5, pp. 484–495, 2011. View at Publisher · View at Google Scholar
  • Ilaria Sciamanna, Patrizia Vitullo, Angela Curatolo, and Corrado Spadafora, “A reverse transcriptase-dependent mechanism is essential for murine preimplantation development,” Genes, vol. 2, no. 2, pp. 360–373, 2011. View at Publisher · View at Google Scholar
  • N. Barron, O. Piskareva, P. Doolan, W. Lackington, D. Lemass, and C. Hendrick, “The Human L1 Element: A Potential Biomarker in Cancer Prognosis, Current Status and Future Directions,” Current Molecular Medicine, vol. 11, no. 4, pp. 286–303, 2011. View at Publisher · View at Google Scholar
  • Paola Sinibaldi-Vallebona, Claudia Matteucci, and Corrado Spadafora, “Retrotransposon-encoded reverse transcriptase in the genesis, progression and cellular plasticity of human cancer,” Cancers, vol. 3, no. 1, pp. 1141–1157, 2011. View at Publisher · View at Google Scholar
  • Gianfranco Giorgi, Pamela Marcantonio, and Brunella Del Re, “LINE-1 retrotransposition in human neuroblastoma cells is affected by oxidative stress,” Cell and Tissue Research, vol. 346, no. 3, pp. 383–391, 2011. View at Publisher · View at Google Scholar
  • Gui-deng Li, and Jin-xu Fang, “From bench to bedside: Targeting epigenetics for cancer therapy,” Clinical Oncology and Cancer Research, vol. 8, no. 4, pp. 191–201, 2011. View at Publisher · View at Google Scholar
  • Wolfgang Goering, Teodora Ribarska, and Wolfgang A. Schulz, “Selective changes of retroelement expression in human prostate cancer,” Carcinogenesis, vol. 32, no. 10, pp. 1484–1492, 2011. View at Publisher · View at Google Scholar
  • Ferya Banaz-Yasar, Nilgün Gedik, Selda Karahan, David Diaz-Carballo, Birthe M. Bongartz, and Süleyman Ergün, “LINE-1 Retrotransposition Events Regulate Gene Expression After X-Ray Irradiation,” DNA and Cell Biology, vol. 31, no. 9, pp. 1458–1467, 2012. View at Publisher · View at Google Scholar
  • Alessandro Fontana, and Borys Wróbel, “A model of evolution of development based on germline penetration of new "no-junk" DNA,” Genes, vol. 3, no. 3, pp. 492–504, 2012. View at Publisher · View at Google Scholar
  • H. H. Burris, S. L. Rifas-Shiman, A. Baccarelli, L. Tarantini, C. E. Boeke, K. Kleinman, A. A. Litonjua, J. W. Rich-Edwards, and M. W. Gillman, “Associations of long interspersed nuclear element-1 DNA methylation with preterm birth in a prospective cohort study,” Journal Of Developmental Origins Of Health And Disease, vol. 3, no. 3, pp. 173–181, 2012. View at Publisher · View at Google Scholar
  • Chatchai Nopavichai, Anapat Sanpawat, Peerapan Kantabandit, Apiwat Mutirangura, and Shanop Shuangshoti, “Changes in LINE-1 methylation level in cancers during metastasis,” Asian Biomedicine, vol. 6, no. 2, pp. 307–312, 2012. View at Publisher · View at Google Scholar
  • Jennifer A Rusiecki, Ligong Chen, Vasantha Srikantan, Lei Zhang, Liying Yan, Matthew L Polin, and Andrea Baccarelli, “DNA methylation in repetitive elements and post-traumatic stress disorder: a case–control study of US military service members,” Epigenomics, vol. 4, no. 1, pp. 29–40, 2012. View at Publisher · View at Google Scholar
  • Gary C. Hon, R. David Hawkins, Otavia L. Caballero, Christine Lo, Ryan Lister, Mattia Pelizzola, Armand Valsesia, Zhen Ye, Samantha Kuan, Lee E. Edsall, Anamaria Aranha Camargo, Brian J. Stevenson, Joseph R. Ecker, Vineet Bafna, Robert L. Strausberg, Andrew J. Simpson, and Bing Ren, “Global DNA hypomethylation coupled to repressive chromatin domain formation and gene silencing in breast cancer,” Genome Research, vol. 22, no. 2, pp. 246–258, 2012. View at Publisher · View at Google Scholar
  • Szilvia Solyom, and Haig H. Kazazian Jr, “Mobile elements in the human genome: Implications for disease,” Genome Medicine, vol. 4, no. 2, 2012. View at Publisher · View at Google Scholar
  • Aika Matsunoki, Kazuyuki Kawakami, Masanori Kotake, Mami Kaneko, Hirotaka Kitamura, Akishi Ooi, Go Watanabe, and Toshinari Minamoto, “LINE-1 methylation shows little intra-patient heterogeneity in primary and synchronous metastatic colorectal cancer,” Bmc Cancer, vol. 12, 2012. View at Publisher · View at Google Scholar
  • Brunella Del Re, Pamela Marcantonio, Entelë Gavoçi, Ferdinando Bersani, and Gianfranco Giorgi, “Assessing LINE-1 retrotransposition activity in neuroblastoma cells exposed to extremely low-frequency pulsed magnetic fields,” Mutation Research/Genetic Toxicology and Environmental Mutagenesis, vol. 749, no. 1-2, pp. 76–81, 2012. View at Publisher · View at Google Scholar
  • Deepak K. Singh, and Pramod C. Rath, “Long interspersed nuclear elements (LINEs) show tissue-specific, mosaic genome and methylation-unrestricted, widespread expression of noncoding RNAs in somatic tissues of the rat,” Rna Biology, vol. 9, no. 11, pp. 1380–1396, 2012. View at Publisher · View at Google Scholar
  • Linda N. Geng, Zizhen Yao, Lauren Snider, Abraham P. Fong, Jennifer N. Cech, Janet M. Young, Silvere M. van der Maarel, Walter L. Ruzzo, Robert C. Gentleman, Rabi Tawil, and Stephen J. Tapscott, “DUX4 Activates Germ line Genes, Retroelements, and Immune Mediators: Implications for Facioscapulohumeral Dystrophy,” Developmental Cell, vol. 22, no. 1, pp. 38–51, 2012. View at Publisher · View at Google Scholar
  • Chuan-Fang Wu, Guang-Hong Tan, Cheng-Chuan Ma, and Ling Li, “The Non-Coding RNA Llme23 Drives the Malignant Property of Human Melanoma Cells,” Journal of Genetics and Genomics, vol. 40, no. 4, pp. 179–188, 2013. View at Publisher · View at Google Scholar
  • Nozomi Mugitani, Yoshio Shimizu, Kenji Satake, Yusuke Suzuki, Satoshi Horikoshi, and Yasuhiko Tomino, “Acceleration of crescent formation by L1 retrotransposon in mouse BSA-induced nephritis,” Journal of Nephrology, vol. 26, no. 2, pp. 375–384, 2013. View at Publisher · View at Google Scholar
  • Ulrike Kreimer, Wolfgang A. Schulz, Annemarie Koch, Günter Niegisch, and Wolfgang Goering, “HERV-K and LINE-1 DNA methylation and reexpression in urothelial carcinoma,” Frontiers in Oncology, vol. 3, 2013. View at Publisher · View at Google Scholar
  • Fulvio Ricceri, Morena Trevisan, Valentina Fiano, Chiara Grasso, Francesca Fasanelli, Chiara Scoccianti, Laura De Marco, Anna Gillio Tos, Paolo Vineis, and Carlotta Sacerdote, “Seasonality Modifies Methylation Profiles in Healthy People,” Plos One, vol. 9, no. 9, 2014. View at Publisher · View at Google Scholar
  • Zhi-ming He, Jinping Li, Yi Lisa Hwa, Brian Brost, Qun Fang, and Shi-Wen Jiang, “Transition of LINE-1 DNA Methylation Status and Altered Expression in First and Third Trimester Placentas,” Plos One, vol. 9, no. 5, 2014. View at Publisher · View at Google Scholar
  • Wei Jie Seow, Molly L. Kile, Andrea A. Baccarelli, Wen-Chi Pan, Hyang-Min Byun, Golam Mostofa, Quazi Quamruzzaman, Mahmuder Rahman, Xihong Lin, and David C. Christiani, “Epigenome-wide DNA methylation changes with development of arsenic-induced skin lesions in Bangladesh: A case-control follow-up study,” Environmental and Molecular Mutagenesis, 2014. View at Publisher · View at Google Scholar
  • Yoshifumi Baba, Asuka Murata, Masayuki Watanabe, and Hideo Baba, “Clinical implications of the LINE-1 methylation levels in patients with gastrointestinal cancer,” Surgery Today, vol. 44, no. 10, pp. 1807–1816, 2014. View at Publisher · View at Google Scholar
  • Kazuto Harada, Yoshifumi Baba, Takatsugu Ishimoto, Akira Chikamoto, Keisuke Kosumi, Hiromitsu Hayashi, Hidetoshi Nitta, Daisuke Hashimoto, Toru Beppu, and Hideo Baba, “LINE-1 Methylation Level and Patient Prognosis in a Database of 208 Hepatocellular Carcinomas,” Annals of Surgical Oncology, 2014. View at Publisher · View at Google Scholar
  • Andrei P. Kozlovpp. 1–231, 2014. View at Publisher · View at Google Scholar
  • Raheleh Rahbari, Laleh Habibi, Jose L. Garcia-Puche, Richard M. Badge, and Jose Garcia-Perezpp. 51–99, 2015. View at Publisher · View at Google Scholar
  • Muhammad Ahmer Jamil, Ioanna Dimitriou, Amit Sharma, Heike Singer, Rolf Fimmers, Holger Fröhlich, Johannes Oldenburg, Antanas Gulbinas, Wolfgang A Schulz, Osman El-Maarri, Nicole Nüsgen, Wolfgang Goering, Albertas Dauksa, and Arijit Biswas, “Inter-locus as well as intra-locus heterogeneity in LINE-1 promoter methylation in common human cancers suggests selective demethylation pressure at specific CpGs,” Clinical Epigenetics, vol. 7, no. 1, 2015. View at Publisher · View at Google Scholar
  • Mohammadmersad Ghorbani, Michael Themis, and Annette Payne, “Genome wide classification and characterisation of CpG sites in cancer and normal cells,” Computers in Biology and Medicine, 2015. View at Publisher · View at Google Scholar
  • Wolfgang A. Schulz, Evangelia A. Koutsogiannouli, Günter Niegisch, and Michèle J Hoffmann, “Epigenetics of Urothelial Carcinoma,” Methods in Molecular Biology, vol. 1238, pp. 183–215, 2015. View at Publisher · View at Google Scholar
  • Jie-Ting Tang, Zhen-Hua Wang, and Jing-Yuan Fang, “Assessing the potential value of long interspersed element-1 hypomethylation in colorectal cancer: evidence from retrospective studies,” Oncotargets And Therapy, vol. 8, pp. 3265–3276, 2015. View at Publisher · View at Google Scholar
  • A. P. Kozlov, “Expression of evolutionarily novel genes in tumors,” Infectious Agents and Cancer, vol. 11, no. 1, 2016. View at Publisher · View at Google Scholar
  • Chiara De Luca, Fiorella Guadagni, Paola Sinibaldi-Vallebona, Steno Sentinelli, Michele Gallucci, Andreas Hoffmann, Gerald G. Schumann, Corrado Spadafora, and Ilaria Sciamanna, “Enhanced expression of LINE-1-encoded ORF2 protein in early stages of colon and prostate transformation,” Oncotarget, vol. 7, no. 4, pp. 4048–4061, 2016. View at Publisher · View at Google Scholar
  • Wenwen Li, Karen Goossens, Mario Van Poucke, Katrien Forier, Kevin Braeckmans, Ann Van Soom, and Luc J. Peelman, “High oxygen tension increases global methylation in bovine 4-cell embryos and blastocysts but does not affect general retrotransposon expression,” Reproduction Fertility And Development, vol. 28, no. 7, pp. 948–959, 2016. View at Publisher · View at Google Scholar
  • Xiao-Qing Zeng, Wang Jian, and Shi-Yao Chen, “Methylation modification in gastric cancer and approaches to targeted epigenetic therapy (Review),” International Journal of Oncology, vol. 50, no. 6, pp. 1921–1933, 2017. View at Publisher · View at Google Scholar
  • Natasha Vafadar-Isfahani, Christina Parr, Lara E. McMillan, Juliane Sanner, Zhao Yeo, Stephen Saddington, Oliver Peacock, Hazel A. Cruickshanks, Richard R. Meehan, Jonathan N. Lund, and Cristina Tufarelli, “Decoupling of DNA methylation and activity of intergenic LINE-1 promoters in colorectal cancer,” Epigenetics, pp. 00–00, 2017. View at Publisher · View at Google Scholar
  • Gianfranco Giorgi, Chiara Pirazzini, Maria Giulia Bacalini, Cristina Giuliani, Paolo Garagnani, Miriam Capri, Ferdinando Bersani, and Brunella Del Re, “Assessing the combined effect of extremely low-frequency magnetic field exposure and oxidative stress on LINE-1 promoter methylation in human neural cells,” Radiation and Environmental Biophysics, vol. 56, no. 2, pp. 193–200, 2017. View at Publisher · View at Google Scholar
  • Suzanne M. Benjes, and Christine M. Morris, “LINE-1 Elements,” Encyclopedia of Cancer, pp. 2041–2042, 2017. View at Publisher · View at Google Scholar
  • Beatriz de Camargo, Bruna M. de Sá Pereira, Rafaela Montalvão-de-Azevedo, Paulo Antônio Faria, Neimar de Paula Silva, Pedro Nicolau-Neto, Mariana Maschietto, and Sheila Coelho Soares Lima, “Association between long interspersed nuclear element-1 methylation levels and relapse in Wilms tumors,” Clinical Epigenetics, vol. 9, no. 1, 2017. View at Publisher · View at Google Scholar
  • Suk Min Jang, Annamaria Kauzlaric, Jean-Pierre Quivy, Julien Pontis, Benjamin Rauwel, Andrea Coluccio, Sandra Offner, Julien Duc, Priscilla Turelli, Geneviève Almouzni, and Didier Trono, “KAP1 facilitates reinstatement of heterochromatin after DNA replication,” Nucleic Acids Research, 2018. View at Publisher · View at Google Scholar
  • Gregory Brittingham, Susan K. Logan, Paolo Mita, Ilaria Sciamanna, Corrado Spadafora, Erica M. Briggs, and Susan Ha, “Long interspersed nuclear element-1 expression and retrotransposition in prostate cancer cells,” Mobile DNA, vol. 9, no. 1, 2018. View at Publisher · View at Google Scholar