Long interspersed nuclear element-1 hypomethylation in cancer: Biology and clinical applications

Clinical Epigenetics

Volumn 2, Issue 2, 2011, Pages 315-330

  Kitkumthorn, Nakarin ^a   Mutirangura, Apiwat ^b  

^a MAHIDOL UNIVERSITY   (Thailand)

^b NONE

Author keywords

Cancer; DNA methylation; Hypomethylation; LINE 1; Long interspersed nuclear element 1s; Partial methylation

Indexed keywords

GENOMIC DNA;

CANCER RESEARCH; CANCER RISK; CARCINOGENESIS; CPG ISLAND; DNA METHYLATION; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE LOCATION; GENE LOCUS; GENETIC ASSOCIATION; GENOMIC INSTABILITY; HUMAN; INTERSPERSED REPEAT; LONG INTERSPERSED NUCLEAR ELEMENT 1 GENE; MOLECULAR INTERACTION; NONHUMAN; ONCOGENE; PHENOTYPE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DETERMINATION; REVIEW; RISK ASSESSMENT; SENSITIVITY AND SPECIFICITY; SEQUENCE ANALYSIS;

EID: 84856268173     PISSN: 18687075     EISSN: 18687083     Source Type: Journal    
DOI: 10.1007/s13148-011-0032-8     Document Type: Review

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80. Miki Y, Nishisho I, Horii A, Miyoshi Y, Utsunomiya J, Kinzler KW, Vogelstein B, Nakamura Y (1992) Disruption of the APC gene by a retrotransposal insertion of L1 sequence in a colon cancer. Cancer Res 52(3):643-645
81. Moran JV (1999) Human L1 retrotransposition: insights and peculiarities learned from a cultured cell retrotransposition assay. Genetica 107(1-3):39-51 (Pubitemid 129574949)
82. Moran JV, DeBerardinis RJ, Kazazian HH Jr (1999) Exon shuffling by L1 retrotransposition. Science 283(5407):1530-1534
83. Neuhausen A, Florl AR, Grimm MO, Schulz WA (2006) DNA methylation alterations in urothelial carcinoma. Cancer Biol Ther 5(8):993-1001. doi:2885
84. Nosho K, Kure S, Irahara N, Shima K, Baba Y, Spiegelman D, Meyerhardt JA, Giovannucci EL, Fuchs CS, Ogino S (2009a) A prospective cohort study shows unique epigenetic, genetic, and prognostic features of synchronous colorectal cancers. Gastroenterology 137(5):1609-1620. doi:10.1053/j.gastro.2009.08.002, e1601-1603
85. Nosho K, Shima K, Irahara N, Kure S, Baba Y, Kirkner GJ, Chen L, Gokhale S, Hazra A, Spiegelman D, Giovannucci EL, Jaenisch R, Fuchs CS, Ogino S (2009b) DNMT3B expression might contribute to CpG island methylator phenotype in colorectal cancer. Clin Cancer Res 15(11):3663-3671. doi:10.1158/1078-0432.CCR- 08-2383
86. Ogino S, Kawasaki T, Nosho K, Ohnishi M, Suemoto Y, Kirkner GJ, Fuchs CS (2008a) LINE-1 hypomethylation is inversely associated with microsatellite instability and CpG island methylator phenotype in colorectal cancer. Int J Cancer 122(12):2767-2773. doi:10.1002/ijc.23470 (Pubitemid 351631379)
87. Ogino S, Nosho K, Kirkner GJ, Kawasaki T, Chan AT, Schernhammer ES, Giovannucci EL, Fuchs CS (2008b) A cohort study of tumoral LINE-1 hypomethylation and prognosis in colon cancer. J Natl Cancer Inst 100(23):1734-1738. doi:10.1093/jnci/djn359
88. Park SY, Yoo EJ, Cho NY, Kim N, Kang GH (2009) Comparison of CpG island hypermethylation and repetitive DNA hypomethylation in premalignant stages of gastric cancer, stratified for Helicobacter pylori infection. J Pathol 219(4):410-416. doi:10.1002/path.2596
89. Pattamadilok J, Huapai N, Rattanatanyong P, Vasurattana A, Triratanachat S, Tresukosol D, Mutirangura A (2008) LINE-1 hypomethylation level as a potential prognostic factor for epithelial ovarian cancer. Int J Gynecol Cancer 18(4):711-717. doi:10.1111/j.1525-1438.2007.01117.x (Pubitemid 352020191)
90. Penzkofer T, Dandekar T, Zemojtel T (2005) L1Base: from functional annotation to prediction of active LINE-1 elements. Nucleic Acids Res 33(Database issue):D498-500 (Pubitemid 40207923)
91. Perrin D, Ballestar E, Fraga MF, Frappart L, EstellerM, Guerin JF, Dante R (2007) Specific hypermethylation of LINE-1 elements during abnormal overgrowth and differentiation of human placenta. Oncogene 26(17):2518-2524. doi:10.1038/sj.onc.1210039 (Pubitemid 46597269)
92. Phokaew C, Kowudtitham S, Subbalekha K, Shuangshoti S, Mutirangura A (2008) LINE-1 methylation patterns of different loci in normal and cancerous cells. Nucleic Acids Res 36(17):5704-5712. doi:10.1093/nar/gkn571
93. Pobsook T, Subbalekha K, Sannikorn P, Mutirangura A (2011) Improved measurement of LINE-1 sequence methylation for cancer detection. Clin Chim Acta 412(3-4):314-321. doi:10.1016/j.cca.2010.10.030
94. Pornthanakasem W, Kongruttanachok N, Phuangphairoj C, Suyarnsestakorn C, Sanghangthum T, Oonsiri S, Ponyeam W, Thanasupawat T, Matangkasombut O, Mutirangura A (2008) LINE-1 methylation status of endogenous DNA double-strand breaks. Nucleic Acids Res 36(11):3667-3675. doi:10.1093/nar/gkn261 (Pubitemid 351934065)
95. Rangwala SH, Zhang L, Kazazian HH Jr (2009) Many LINE1 elements contribute to the transcriptome of human somatic cells. Genome Biol 10(9):R100. doi:10.1186/gb-2009-10-9-r100
96. Richardson B, Scheinbart L, Strahler J, Gross L, Hanash S, Johnson M (1990) Evidence for impaired T cell DNA methylation in systemic lupus erythematosus and rheumatoid arthritis. Arthritis Rheum 33(11):1665-1673
97. Rodriguez J, Vives L, Jorda M, Morales C, Munoz M, Vendrell E, Peinado MA (2008) Genome-wide tracking of unmethylated DNA Alu repeats in normal and cancer cells. Nucleic Acids Res 36(3):770-784. doi:10.1093/nar/gkm1105 (Pubitemid 351267234)
98. Roman-Gomez J, Jimenez-Velasco A, Agirre X, Cervantes F, Sanchez J, Garate L, Barrios M, Castillejo JA, Navarro G, Colomer D, Prosper F, Heiniger A, Torres A (2005) Promoter hypomethylation of the LINE-1 retrotransposable elements activates sense/antisense transcription and marks the progression of chronic myeloid leukemia. Oncogene 24(48):7213-7223. doi:10.1038/sj.onc.1208866 (Pubitemid 41679283)
99. Roman-Gomez J, Jimenez-Velasco A, Agirre X, Castillejo JA, Navarro G, San Jose-Eneriz E, Garate L, Cordeu L, Cervantes F, Prosper F, Heiniger A, Torres A (2008) Repetitive DNA hypomethylation in the advanced phase of chronic myeloid leukemia. Leuk Res 32 (3):487-490. doi:10.1016/j.leukres.2007.07.021 (Pubitemid 351308023)
100. Romermann D, Hasemeier B, Metzig K, Schlegelberger B, Langer F, Kreipe H, Lehmann U (2007) Methylation status of LINE-1 sequences in patients with MDS or secondary AML. Verh Dtsch Ges Pathol 91:338-342
101. Saito K, Kawakami K, Matsumoto I, Oda M, Watanabe G, Minamoto T (2010) Long interspersed nuclear element 1 hypomethylation is a marker of poor prognosis in stage IA non-small cell lung cancer. Clin Cancer Res 16(8):2418-2426. doi:10.1158/1078-0432.CCR-09-2819
102. Santourlidis S, Florl A, Ackermann R, Wirtz HC, Schulz WA (1999) High frequency of alterations in DNA methylation in adenocarcinoma of the prostate. Prostate 39(3):166-174. doi:10.1002/(SICI)1097-0045(19990515)39:3 (Pubitemid 29203403)
103. J Sassaman DM, Dombroski BA, Moran JV, Kimberland ML, Naas TP, DeBerardinis RJ, Gabriel A, Swergold GD, Kazazian HH Jr (1997) Many human L1 elements are capable of retrotransposition. Nat Genet 16(1):37-43. doi:10.1038/ng0597-37 (Pubitemid 27198154)
104. Schulz WA, Elo JP, Florl AR, Pennanen S, Santourlidis S, Engers R, Buchardt M, Seifert HH, Visakorpi T (2002) Genomewide DNA hypomethylation is associated with alterations on chromosome 8 in prostate carcinoma. Genes Chromosom Cancer 35(1):58-65. doi:10.1002/gcc.10092 (Pubitemid 34847869)
105. Schulz WA, Steinhoff C, Florl AR (2006) Methylation of endogenous human retroelements in health and disease. Curr Top Microbiol Immunol 310:211-250 (Pubitemid 47400292)
106. Shuangshoti S, Hourpai N, Pumsuk U, Mutirangura A (2007) Line-1 hypomethylation in multistage carcinogenesis of the uterine cervix. Asian Pac J Cancer Prev 8(2):307-309
107. Smith IM, Mydlarz WK, Mithani SK, Califano JA (2007) DNA global hypomethylation in squamous cell head and neck cancer associated with smoking, alcohol consumption and stage. Int J Cancer 121(8):1724-1728. doi:10.1002/ijc.22889 (Pubitemid 47417289)
108. Sonpavde G, Aparicio AM, Zhan F, North B, Delaune R, Garbo LE, Rousey SR, Weinstein RE, Xiao L, Boehm KA, Asmar L, Fleming MT, Galsky MD, Berry WR, Von Hoff DD (2009) Azacitidine favorably modulates PSA kinetics correlating with plasma DNA LINE-1 hypomethylation in men with chemonaive castration-resistant prostate cancer. Urol Oncol. doi:10.1016/j. urolonc.2009.09.015
109. Speek M (2001) Antisense promoter of human L1 retrotransposon drives transcription of adjacent cellular genes. Mol Cell Biol 21 (6):1973-1985. doi:10.1128/MCB.21.6.1973-1985.2001 (Pubitemid 32479621)
110. Migeon BR, Holland MM, Driscoll DJ, Robinson JC (1991) Programmed demethylation in CpG islands during human fetal development. Somat Cell Mol Genet 17(2):159-168
111. Miki Y, Nishisho I, Horii A, Miyoshi Y, Utsunomiya J, Kinzler KW, Vogelstein B, Nakamura Y (1992) Disruption of the APC gene by a retrotransposal insertion of L1 sequence in a colon cancer. Cancer Res 52(3):643-645
112. Moran JV (1999) Human L1 retrotransposition: insights and peculiarities learned from a cultured cell retrotransposition assay. Genetica 107(1-3):39-51 (Pubitemid 129574949)
113. Moran JV, DeBerardinis RJ, Kazazian HH Jr (1999) Exon shuffling by L1 retrotransposition. Science 283(5407):1530-1534
114. Neuhausen A, Florl AR, Grimm MO, Schulz WA (2006) DNA methylation alterations in urothelial carcinoma. Cancer Biol Ther 5(8):993-1001.
115. Nosho K, Kure S, Irahara N, Shima K, Baba Y, Spiegelman D, Meyerhardt JA, Giovannucci EL, Fuchs CS, Ogino S (2009a) A prospective cohort study shows unique epigenetic, genetic, and prognostic features of synchronous colorectal cancers. Gastroenterology 137(5):1609-1620. doi:10.1053/j.gastro.2009.08.002, e1601-1603
116. Nosho K, Shima K, Irahara N, Kure S, Baba Y, Kirkner GJ, Chen L, Gokhale S, Hazra A, Spiegelman D, Giovannucci EL, Jaenisch R, Fuchs CS, Ogino S (2009b) DNMT3B expression might contribute to CpG island methylator phenotype in colorectal cancer. Clin Cancer Res 15(11):3663-3671. doi:10.1158/1078-0432.CCR- 08-2383
117. Ogino S, Kawasaki T, Nosho K, Ohnishi M, Suemoto Y, Kirkner GJ, Fuchs CS (2008a) LINE-1 hypomethylation is inversely associated with microsatellite instability and CpG island methylator phenotype in colorectal cancer. Int J Cancer 122(12):2767-2773. doi:10.1002/ijc.23470 (Pubitemid 351631379)
118. Ogino S, Nosho K, Kirkner GJ, Kawasaki T, Chan AT, Schernhammer ES, Giovannucci EL, Fuchs CS (2008b) A cohort study of tumoral LINE-1 hypomethylation and prognosis in colon cancer. J Natl Cancer Inst 100(23):1734-1738. doi:10.1093/jnci/djn359
119. Park SY, Yoo EJ, Cho NY, Kim N, Kang GH (2009) Comparison of CpG island hypermethylation and repetitive DNA hypomethylation in premalignant stages of gastric cancer, stratified for Helicobacter pylori infection. J Pathol 219(4):410-416. doi:10.1002/path.2596
120. Pattamadilok J, Huapai N, Rattanatanyong P, Vasurattana A, Triratanachat S, Tresukosol D, Mutirangura A (2008) LINE-1 hypomethylation level as a potential prognostic factor for epithelial ovarian cancer. Int J Gynecol Cancer 18(4):711-717. doi:10.1111/j.1525-1438.2007.01117.x (Pubitemid 352020191)
121. Penzkofer T, Dandekar T, Zemojtel T (2005) L1Base: from functional annotation to prediction of active LINE-1 elements. Nucleic Acids Res 33(Database issue):D498-500 (Pubitemid 40207923)
122. Perrin D, Ballestar E, Fraga MF, Frappart L, EstellerM, Guerin JF, Dante R (2007) Specific hypermethylation of LINE-1 elements during abnormal overgrowth and differentiation of human placenta. Oncogene 26(17):2518-2524. doi:10.1038/sj.onc.1210039 (Pubitemid 46597269)
123. Phokaew C, Kowudtitham S, Subbalekha K, Shuangshoti S, Mutirangura A (2008) LINE-1 methylation patterns of different loci in normal and cancerous cells. Nucleic Acids Res 36(17):5704-5712. doi:10.1093/nar/gkn571
124. Pobsook T, Subbalekha K, Sannikorn P, Mutirangura A (2011) Improved measurement of LINE-1 sequence methylation for cancer detection. Clin Chim Acta 412(3-4):314-321. doi:10.1016/j.cca.2010.10.030
125. Pornthanakasem W, Kongruttanachok N, Phuangphairoj C, Suyarnsestakorn C, Sanghangthum T, Oonsiri S, Ponyeam W, Thanasupawat T, Matangkasombut O, Mutirangura A (2008) LINE-1 methylation status of endogenous DNA double-strand breaks. Nucleic Acids Res 36(11):3667-3675. doi:10.1093/nar/gkn261 (Pubitemid 351934065)
126. Rangwala SH, Zhang L, Kazazian HH Jr (2009) Many LINE1 elements contribute to the transcriptome of human somatic cells. Genome Biol 10(9):R100. doi:10.1186/gb-2009-10-9-r100
127. Richardson B, Scheinbart L, Strahler J, Gross L, Hanash S, Johnson M (1990) Evidence for impaired T cell DNA methylation in systemic lupus erythematosus and rheumatoid arthritis. Arthritis Rheum 33(11):1665-1673
128. Rodriguez J, Vives L, Jorda M, Morales C, Munoz M, Vendrell E, Peinado MA (2008) Genome-wide tracking of unmethylated DNA Alu repeats in normal and cancer cells. Nucleic Acids Res 36(3):770-784. doi:10.1093/nar/gkm1105 (Pubitemid 351267234)
129. Roman-Gomez J, Jimenez-Velasco A, Agirre X, Cervantes F, Sanchez J, Garate L, Barrios M, Castillejo JA, Navarro G, Colomer D, Prosper F, Heiniger A, Torres A (2005) Promoter hypomethylation of the LINE-1 retrotransposable elements activates sense/antisense transcription and marks the progression of chronic myeloid leukemia. Oncogene 24(48):7213-7223. doi:10.1038/sj.onc.1208866 (Pubitemid 41679283)
130. Roman-Gomez J, Jimenez-Velasco A, Agirre X, Castillejo JA, Navarro G, San Jose-Eneriz E, Garate L, Cordeu L, Cervantes F, Prosper F, Heiniger A, Torres A (2008) Repetitive DNA hypomethylation in the advanced phase of chronic myeloid leukemia. Leuk Res 32 (3):487-490. doi:10.1016/j.leukres.2007.07.021 (Pubitemid 351308023)
131. Romermann D, Hasemeier B, Metzig K, Schlegelberger B, Langer F, Kreipe H, Lehmann U (2007) Methylation status of LINE-1 sequences in patients with MDS or secondary AML. Verh Dtsch Ges Pathol 91:338-342
132. Saito K, Kawakami K, Matsumoto I, Oda M, Watanabe G, Minamoto T (2010) Long interspersed nuclear element 1 hypomethylation is a marker of poor prognosis in stage IA non-small cell lung cancer. Clin Cancer Res 16(8):2418-2426. doi:10.1158/1078-0432.CCR-09-2819
133. Santourlidis S, Florl A, Ackermann R, Wirtz HC, Schulz WA (1999) High frequency of alterations in DNA methylation in adenocarcinoma of the prostate. Prostate 39(3):166-174. doi:10.1002/(SICI)1097-0045(19990515)39:3 (Pubitemid 29203403)
134. J Sassaman DM, Dombroski BA, Moran JV, Kimberland ML, Naas TP, DeBerardinis RJ, Gabriel A, Swergold GD, Kazazian HH Jr (1997) Many human L1 elements are capable of retrotransposition. Nat Genet 16(1):37-43. doi:10.1038/ng0597-37 (Pubitemid 27198154)
135. Schulz WA, Elo JP, Florl AR, Pennanen S, Santourlidis S, Engers R, Buchardt M, Seifert HH, Visakorpi T (2002) Genomewide DNA hypomethylation is associated with alterations on chromosome 8 in prostate carcinoma. Genes Chromosom Cancer 35(1):58-65. doi:10.1002/gcc.10092 (Pubitemid 34847869)
136. Schulz WA, Steinhoff C, Florl AR (2006) Methylation of endogenous human retroelements in health and disease. Curr Top Microbiol Immunol 310:211-250 (Pubitemid 47400292)
137. Shuangshoti S, Hourpai N, Pumsuk U, Mutirangura A (2007) Line-1 hypomethylation in multistage carcinogenesis of the uterine cervix. Asian Pac J Cancer Prev 8(2):307-309
138. Smith IM, Mydlarz WK, Mithani SK, Califano JA (2007) DNA global hypomethylation in squamous cell head and neck cancer associated with smoking, alcohol consumption and stage. Int J Cancer 121(8):1724-1728. doi:10.1002/ijc.22889 (Pubitemid 47417289)
139. Sonpavde G, Aparicio AM, Zhan F, North B, Delaune R, Garbo LE, Rousey SR, Weinstein RE, Xiao L, Boehm KA, Asmar L, Fleming MT, Galsky MD, Berry WR, Von Hoff DD (2009) Azacitidine favorably modulates PSA kinetics correlating with plasma DNA LINE-1 hypomethylation in men with chemonaive castration-resistant prostate cancer. Urol Oncol. doi:10.1016/j. urolonc.2009.09.015
140. Speek M (2001) Antisense promoter of human L1 retrotransposon drives transcription of adjacent cellular genes. Mol Cell Biol 21(6):1973-1985. doi:10.1128/MCB.21.6.1973-1985.2001 (Pubitemid 32479621)