Development of a monoclonal antibody specific to the endonuclease domain of the human LINE-1 ORF2 protein

Mobile DNA

Volumn 5, Issue 1, 2014, Pages

  Sokolowski, Mark ^a   DeFreece, Cecily B ^b   Servant, Geraldine ^c   Kines, Kristine J ^a   DeHaro, Dawn L ^a   Belancio, Victoria P ^a  

^a TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b XAVIER UNIVERSITY OF LOUISIANA   (United States)

^c TULANE UNIVERSITY   (United States)

Author keywords

Endonuclease; In vitro assay; L1; L1 antibody; LINE 1; ORF2, Retrotransposition

Indexed keywords

ENDONUCLEASE; EPITOPE; MONOCLONAL ANTIBODY; OPEN READING FRAME 2 PROTEIN; PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CODON; CONTROLLED STUDY; ENDONUCLEASE DOMAIN; HUMAN; HUMAN CELL; IN VITRO STUDY; LONG INTERSPERSED REPEAT; LONG INTERSPERSED REPEAT 1; OPEN READING FRAME; PLASMID; PRIORITY JOURNAL; PROTEIN DOMAIN; TRANSIENT EXPRESSION;

EID: 84989211399     PISSN: None     EISSN: 17598753     Source Type: Journal    
DOI: 10.1186/s13100-014-0029-x     Document Type: Article

References (60)

1. Moran JV, Holmes SE, Naas TP, DeBerardinis RJ, Boeke JD, Kazazian HH Jr: High frequency retrotransposition in cultured mammalian cells. Cell 1996, 87(5):917-927.
2. Dewannieux M, Esnault C, Heidmann T: LINE-mediated retrotransposition of marked Alu sequences. Nat Genet 2003, 35(1):41-48.
3. Ostertag EM, Goodier JL, Zhang Y, Kazazian HH Jr: SVA Elements are nonautonomous retrotransposons that cause disease in humans. Am J Hum Genet 2003, 73(6):1444-1451.
4. Esnault C, Maestre J, Heidmann T: Human LINE retrotransposons generate processed pseudogenes. Nat Genet 2000, 24(4):363-367.
5. Kulpa DA, Moran JV: Ribonucleoprotein particle formation is necessary but not sufficient for LINE-1 retrotransposition. Hum Mol Genet 2005, 14(21):3237-3248.
6. Wei W, Gilbert N, Ooi SL, Lawler JF, Ostertag EM, Kazazian HH, Boeke JD, Moran JV: Human L1 retrotransposition: cispreference versus trans complementation. Mol Cell Biol 2001, 21(4):1429-1439.
7. Kolosha VO, Martin SL: In vitro properties of the first ORF protein from mouse LINE-1 support its role in ribonucleoprotein particle formation during retrotransposition. Proc Natl Acad Sci U S A 1997, 94(19):10155-10160.
8. Wallace N, Wagstaff BJ, Deininger PL, Roy-Engel AM: LINE-1 ORF1 protein enhances Alu SINE retrotransposition. Gene 2008, 419(1-2):1-6.
9. Luan DD, Korman MH, Jakubczak JL, Eickbush TH: Reverse transcription of R2Bm RNA is primed by a nick at the chromosomal target site: A mechanism for non-LTR retrotransposition. Cell 1993, 72(4):595-605.
10. Cost GJFQJABJD: Human L1 element target-primed reverse transcription in vitro. EMBO J 2002, 21(21):5899-5910.
11. Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC, Baldwin J, Devon K, Dewar K, Doyle M, FitzHugh W, Funke R, Gage D, Harris K, Heaford A, Howland J, Kann L, Lehoczky J, LeVine R, McEwan P, McKernan K, Meldrim J, Mesirov JP, Miranda C, Morris W, Naylor J, Raymond C, Rosetti M, Santos R, Sheridan A, Sougnez C, et al: Initial sequencing and analysis of the human genome. Nature 2001, 409(6822):860-921.
12. Konkel MK, Wang J, Liang P, Batzer MA: Identification and characterization of novel polymorphic LINE-1 insertions through comparison of two human genome sequence assemblies. Gene 2007, 390(1-2):28-38.
13. Beck CR, Collier P, Macfarlane C, Malig M, Kidd JM, Eichler EE, Badge RM, Moran JV: LINE-1 retrotransposition activity in human genomes. Cell 2010, 141(7):1159-1170.
14. Huang CRL, Schneider AM, Lu Y, Niranjan T, Shen P, Robinson MA, Steranka JP, Valle D, Civin CI, Wang T, Wheelan SJ, Ji H, Boeke JD, Burns KH: Mobile Interspersed repeats are major structural variants in the human genome. Cell 2010, 141(7):1171-1182.
15. Ewing AD, Kazazian HH: Whole-genome resequencing allows detection of many rare LINE-1 insertion alleles in humans. Genome Res 2011, 21(6):985-990.
16. Brouha B, Schustak J, Badge RM, Lutz-Prigge S, Farley AH, Moran JV, Kazazian HH: Hot L1s account for the bulk of retrotransposition in the human population. Proc Natl Acad Sci U S A 2003, 100(9):5280-5285.
17. Basame S, Wai-lun Li P, Howard G, Branciforte D, Keller D, Martin SL: Spatial assembly and RNA binding stoichiometry of a LINE-1 protein essential for retrotransposition. J Mol Biol 2006, 357(2):351-357.
18. Khazina E, Truffault V, Böttner R, Schmidt S, Coles M, Weichenrieder O: Trimeric structure and flexibility of the L1ORF1 protein in human L1 retrotransposition. Nat Struct Mol Biol 2011, 18(9):1006-1014.
19. Callahan KE, Hickman AB, Jones CE, Ghirlando R, Furano AV: Polymerization and nucleic acid-binding properties of human L1 ORF1 protein. Nucleic Acids Res 2012, 40(2):813-827.
20. Taylor MS, LaCava J, Mita P, Molloy KR, Huang CRL, Li D, Adney EM, Jiang H, Burns KH, Chait BT, Rout MP, Boeke JD, Dai L: Affinity proteomics reveals human host factors implicated in discrete stages of LINE-1 retrotransposition. Cell 2013, 155(5):1034-1048.
21. Feng Q, Moran JV, Kazazian HH Jr, Boeke JD: Human L1 retrotransposon encodes a conserved endonuclease required for retrotransposition. Cell 1996, 87(5):905-916.
22. Xiong Y, Eickbush TH: Origin and evolution of retroelements based upon their reverse transcriptase sequences. EMBO J 1990, 9(10):3353.
23. Fanning TG, Singer MF: LINE-1: A mammalian transposable element. Biochim Biophys Acta 1987, 910(3):203-212.
24. Piskareva O, Ernst C, Higgins N, Schmatchenko V: The carboxy-Terminal segment of the human LINE-1 ORF2 protein is involved in RNA binding. FEBS Open Bio 2013, 3:433-437.
25. Alisch RS, Garcia-Perez JL, Muotri AR, Gage FH, Moran JV: Unconventional translation of mammalian LINE-1 retrotransposons. Gene Dev 2006, 20(2):210-224.
26. Li PW-L, Li J, Timmerman SL, Krushel LA, Martin SL: The dicistronic RNA from the mouse LINE-1 retrotransposon contains an internal ribosome entry site upstream of each ORF: implications for retrotransposition. Nucleic Acids Res 2006, 34(3):853-864.
27. Ergön S, Buschmann C, Heukeshoven J, Dammann K, Schnieders F, Lauke H, Chalajour F, Kilic N, Strätling WH, Schumann GG: Cell type-specific expression of LINE-1 open reading frames 1 and 2 in fetal and adult human tissues. J Biol Chem 2004, 279(26):27753-27763.
28. Kines KJ, Sokolowski M, De Haro DL, Christian CM, Belancio VP: Potential for genomic instability associated with retrotranspositionally-incompetent L1 loci. Nucleic Acids Res 2014, 42(16):10488-10502.
29. Goodier JL, Ostertag EM, Engleka KA, Seleme MC, Kazazian HH: A potential role for the nucleolus in L1 retrotransposition. Hum Mol Genet 2004, 13(10):1041-1048.
30. Doucet AJ, Hulme AE, Sahinovic E, Kulpa DA, Moldovan JB, Kopera HC, Athanikar JN, Hasnaoui M, Bucheton A, Moran JV, Gilbert N: Characterization of LINE-1 ribonucleoprotein particles. PLoS Genet 2010, 6(10):e1001150.
31. Repanas K, Zingler N, Layer LE, Schumann GG, Perrakis A, Weichenrieder O: Determinants for DNA target structure selectivity of the human LINE-1 retrotransposon endonuclease. Nucleic Acids Res 2007, 35(14):4914-4926.
32. Nesterova IV, Bennett CA, Erdem SS, Hammer RP, Deininger PL, Soper SA: Near-IR single fluorophore quenching system based on phthalocyanine (Pc) aggregation and its application for monitoring inhibitor/activator action on a therapeutic target: L1-EN. Analyst 2011, 136(6):1103-1105.
33. Weichenrieder O, Repanas K, Perrakis A: Crystal structure of the targeting endonuclease of the human LINE-1 retrotransposon. Structure 2004, 12(6):975-986.
34. Morrish TA, Gilbert N, Myers JS, Vincent BJ, Stamato TD, Taccioli GE, Batzer MA, Moran JV: DNA repair mediated by endonuclease-independent LINE-1 retrotransposition. Nat Genet 2002, 31(2):159-165.
35. Han JS, Boeke JD: A highly active synthetic mammalian retrotransposon. Nature 2004, 429(6989):314-318.
36. Wagstaff BJ, Barnerboi M, Roy-Engel AM: Evolutionary conservation of the functional modularity of primate and murine LINE-1 elements. PLoS One 2011, 6(5):e19672.
37. Gasior SL, Wakeman TP, Xu B, Deininger PL: The human LINE-1 retrotransposon creates DNA double-strand breaks. J Mol Biol 2006, 357(5):1383-1393.
38. Robberecht C, Voet T, Esteki MZ, Nowakowska BA, Vermeesch JR: Nonallelic homologous recombination between retrotransposable elements is a driver of de novo unbalanced translocations. Genome Res 2013, 23(3):411-418.
39. Dombroski BA, Mathias SL, Nanthakumar E, Scott AF, Kazazian HH: Isolation of an active human transposable element. Science 1991, 254:1805-1808.
40. Han K, Lee J, Meyer TJ, Remedios P, Goodwin L, Batzer MA: L1 recombination-Associated deletions generate human genomic variation. Proc Natl Acad Sci U S A 2008, 105(49):19366-19371.
41. Miki Y, Nishisho I, Horii A, Miyoshi Y, Utsunomiya J, Kinzler KW, Vogelstein B, Nakamura Y: Disruption of the APC gene by a retrotransposal insertion of L1 sequence in a colon cancer. Cancer Res 1992, 52(3):643-645.
42. Pickeral OK, Makałowski W, Boguski MS, Boeke JD: Frequent human genomic DNA transduction driven by LINE-1 retrotransposition. Genome Res 2000, 10(4):411-415.
43. Zhang A, Dong B, Doucet AJ, Moldovan JB, Moran JV, Silverman RH: RNase L restricts the mobility of engineered retrotransposons in cultured human cells. Nucleic Acids Res 2014, 42(6):3803-3820.
44. Yang N, Kazazian HH: L1 retrotransposition is suppressed by endogenously encoded small interfering RNAs in human cultured cells. Nat Struct Mol Biol 2006, 13(9):763-771.
45. Goodier JL, Cheung LE, Kazazian HH: Mapping the LINE1 ORF1 protein interactome reveals associated inhibitors of human retrotransposition. Nucleic Acids Res 2013, 41(15):7401-7419.
46. Horn AV, Klawitter S, Held U, Berger A, Jaguva Vasudevan AA, Bock A, Hofmann H, Hanschmann K-MO, Trösemeier J-H, Flory E, Jabulowsky RA, Han JS, Löwer J, Löwer R, Mönk C, Schumann GG: Human LINE-1 restriction by APOBEC3C is deaminase independent and mediated by an ORF1p interaction that affects LINE reverse transcriptase activity. Nucleic Acids Res 2014, 42(1):396-416.
47. Belancio VP, Hedges DJ, Deininger P: LINE-1 RNA splicing and influences on mammalian gene expression. Nucleic Acids Res 2006, 34(5):1512-1521.
48. Bogerd HP, Wiegand HL, Hulme AE, Garcia-Perez JL, O'Shea KS, Moran JV, Cullen BR: Cellular inhibitors of long interspersed element 1 and Alu retrotransposition. Proc Natl Acad Sci U S A 2006, 103(23):8780-8785.
49. de Haro D, Kines KJ, Sokolowski M, Dauchy RT, Streva VA, Hill SM, Hanifin JP, Brainard GC, Blask DE, Belancio VP: Regulation of L1 expression and retrotransposition by melatonin and its receptor: implications for cancer risk associated with light exposure at night. Nucleic Acids Res 2014, 42(12):7694-7707.
50. Perepelitsa-Belancio V, Deininger P: RNA truncation by premature polyadenylation attenuates human mobile element activity. Nat Genet 2003, 35(4):363-366.
51. Sokolowski M, de Haro D, Christian CM, Kines KJ, Belancio VP: Characterization of L1 ORF1p self-interaction and cellular localization using a mammalian two-hybrid system. PLoS One 2013, 8(12):e82021.
52. Khan H, Smit A, Boissinot S: Molecular evolution and tempo of amplification of human LINE-1 retrotransposons since the origin of primates. Genome Res 2006, 16(1):78-87.
53. Dai L, Huang Q, Boeke J: Effect of reverse transcriptase inhibitors on LINE-1 and Ty1 reverse transcriptase activities and on LINE-1 retrotransposition. BMC Biochem 2011, 12(1):18.
54. Kroutter EN, Belancio VP, Wagstaff BJ, Roy-Engel AM: The RNA polymerase dictates ORF1 requirement and timing of LINE and SINE retrotransposition. PLoS Genet 2009, 5(4):e1000458.
55. Strahl C, Blackburn EH: Effects of reverse transcriptase inhibitors on telomere length and telomerase activity in two immortalized human cell lines. Mol Cell Biol 1996, 16(1):53-65.
56. D'Andrea G, Brisdelli F, Bozzi A: AZT: An old drug with new perspectives. Curr Clin Pharmacol 2008, 3(1):20-37.
57. Imai K, Takaoka A: Comparing antibody and small-molecule therapies for cancer. Nat Rev Cancer 2006, 6(9):714-727.
58. Hidalgo M, Eckhardt SG: Development of matrix metalloproteinase inhibitors in cancer therapy. J Natl Cancer Inst 2001, 93(3):178-193.
59. Madhusudan S, Smart F, Shrimpton P, Parsons JL, Gardiner L, Houlbrook S, Talbot DC, Hammonds T, Freemont PA, Sternberg MJ, Dianov GL, Hickson ID: Isolation of a small molecule inhibitor of DNA base excision repair. Nucleic Acids Res 2005, 33(15):4711-4724.
60. Naas TP, DeBerardinis RJ, Moran JV, Ostertag EM, Kingsmore SF, Seldin MF, Hayashizaki Y, Martin SL, Kazazian HH: An actively retrotransposing, novel subfamily of mouse L1 elements. EMBO J 1998, 17(2):590-597.