Clonal expansion and genomic characterization of the human T-cell lymphotropic virus type I during the integration process in adult T-cell leukemia/lymphoma
Keywords:
Virus integration, human T-lymphotropic virus 1, leukaemia-lymphoma, adult T-cell, polymerase chain reaction, genome, human, computational biology
Abstract
Introduction. Although the integration of human T-cell lymphotropic virus type I into the T-cells is not a random process, the mechanistic details are not understood.Objectives. The characteristics of the flanking host chromatin were evaluated at the integration sites in adult T-cell leukaemia/lymphoma (ATLL) patients infected with the virus.
Materials and methods. From seven leukemic Colombian patients positive for the human T-cell lymphotropic virus type I (HTLV-I), lymphocyte DNA samples were extracted and amplified by inverse polymerase chain reaction (IPCR). Clonal expansion and human genome nucleotide composition in an extension of 50 bp was determined. To establish the characteristics of the human genome flanking provirus, 61 IPCR sequences from Colombian and Japanese ATLL patients, were analyzed in silico to obtain insights about the genomic structure, functions and nature of associated chromatin.
Results. The clonal expansion of cell clones was predominantly oligoclonal. From 61 IPCR sequences, 155 alignments with homology higher than 95% (e-value <0.05) were screened. Seventy-five percent of those sequences corresponded to non coding elements that include repetitive and non-repetitive DNA. Fifty percent of the proviral integrations were associated with chromosomes of A and B groups. Viral DNA integration tended to favor exons of genes that replicated early, controlled the cell cycle, or were involved in signal transduction.
Conclusions. The results indicated that HTLV-I integration was preferentially directed towards genomic environments with high C:G content, and toward genes that replicate early, regulate cell cycle or involved with signal transduction.
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References
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6. Yoshida M. Multiple viral strategies of HTLV-1 for dysregulation of cell growth control. Annu Rev Immunol. 2001;19:475-96.
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8. Zoubak S, Richardson J, Rynditch AV, Hollsberg P, Hafler DA, Boeri E, et al. Regional specificity of HTLV-I proviral integration in the human genome. Gene. 1994;143:155-63.
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11. Saccone S, De Sario A, Wiegant J, Raap AK, Della-Valle G, Bernardi G. Correlations between isochores and chromosomal bands in the human genome. Proc Natl Acad Sci USA. 1993;90:11929-33.
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14. Kim MA, Johannsmann R, Grzeschik KH. Giemsa staining of the sites replicating DNA early in human lymphocyte chromosomes. Cytogenet Cell Genet. 1975;15:363-71.
15. Federico C, Saccone S, Bernardi G. The gene-richest bands of human chromosomes replicate at the onset of the S-phase. Cytogenet Cell Genet. 1998;80:83-8.
16. Albrecht B, Lairmore MD. Critical role of human T-lymphotropic virus type 1 accessory proteins in viral replication and pathogenesis. Microbiol Mol Biol Rev. 2002;66:396-406.
17. Yasunaga JI, Matsuoka M. Human T-cell leukemia virus type I induces adult T-cell leukemia: From clinical aspects to molecular mechanisms. Cancer Control. 2007;14:133-40.
18. Albrecht B, Collins ND, Burrinstom MT, Nisbet JW, Ratner L, Green PL, et al. Human T-lymphotropic virus type I open reading frame I p12(I) is required for efficient viral infectivity in primary lymphocytes. J Virol. 2000;74:9828-35.
19. Bindhu M, Nair A, Lairmore MD. Role of accessory proteins of HTLV-1 in viral replication, T cell activation, and cellular gene expression. Front Biosci. 2004;9: 2556-76.
20. Carrascal E, Cortés A, Akiba S, Tamayo O, Quiñónez F, Floréz L, et al. Epidemiología y patología de la leucemia/linfoma de células T del adulto en Cali y el suroccidente colombiano. Colombia Médica. 2004;35:12-7.
21. República de Colombia. Ministerio de Salud. Por la cual se establecen las normas científicas, técnicas y administrativas para la investigación en salud Resolución No 008430 de octubre 4 de 1993. Bogotá: Ministerio de Salud; 1993.
22. Sambrook J, Fritzch EF, Maniatis T. Molecular cloning. A laboratory manual. New York: Ed. Cold Spring Harbor Press; 1989.
23. Seiki M, Hattori S, Hirayama Y, Yoshida M. Human adult T-cell leukemia virus: complete nucleotide sequence of the provirus genome integrated in leukemia cell DNA. Proc Natl Acad Sci USA. 1983;80:3618-22.
24. Feinberg AP, Vogelstein B. Technique for radiolabeling of restriction endonuclease fragments. Anal Biochem. 1983;132:6-13.
25. Miyoshi I, Kubonishi I, Yoshimoto S, Akagi T, Ohtsuki Y, Shiraishi Y, et al. Type C virus particles in a cord T-cell line derived by co-cultivating normal human cord leukocytes and human leukaemic T cells. Nature.1981;294:770-1.
26. Takemoto S, Matsuoka M, Yamaguchi K, Takatsuki K. A novel diagnostic method of adult T-cell leukemia: Monoclonal integration of human T-cell lymphotropic virus type I provirus DNA detected by inverse polymerase chain reaction. Blood. 1994;84:3080-5.
27. Cavrois M, Gessain A, Wain-Hobson S, Wattel E. Proliferation of HTLV-I infected circulating cells in vivo in all asymptomatic carries and patients with TSP/HAM. Oncogen. 1996;12:2419-23.
28. Cabrera J, García-Vallejo F. Aumento del número de amplicones obtenidos por IPCR en el ADN de personas seropositivas para HTLV-I afectadas con PET/HAM. Colombia Médica. 2000;31:169-75.
29. Ozawa T, Itoyama T, Sadamori N, Yamada Y, Hata T, Tomonaga M, et al. Rapid isolation of viral integration site reveals frequent integration of HTLV-1 into expressed loci. J Hum Genet. 2004;49:154-29.
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32. International Human Genome Sequencing Consortium. Initial sequencing and analysis of the human genome. Nature. 2001;409:860-921.
33. Blank A. Adult T-cell leukemia/lymphoma in southwest Colombia. En: HTLV, truths and questions. Cali: Edit Zaninovic; 1996. p. 266-71.
34. Wattel E, Vartanian JP, Pannetier CH, Wain-Hobson S. Clonal expansión of human T-cell leukemia and symptomatic carries without malignancy. J. Virol. 1995;69:2863-8.
35. Wattel E, Cavrois, Gessain MA, Wain-Hobson S. Clonal expansion of infected cells –a way of life for HTLV-I. J Acquir Immune Defic Syndr Hum Retrovirol. 1996;13(Supl.1):92-9.
36. Doi K, Wu X, Taniguchi Y, Yasunaga J, Satou Y, Okayama A, et al. Preferential selection of human T-cell leukemia virus type I provirus integration sites in leukemic versus carrier status. Blood. 2005;106:1048-53.
37. Hanai S, Nitta T, Shoda M, Tanaka M, Iso N, Mizoguchi I, et al. Integration of human T-cell leukemia virus type 1 in genes of leukemia cells of patients with adult T-cell leukemia. Cancer Sci. 2004;95:306-10.
38. Spence JM, Mills W, Mann K, Huxley C, Farr CJ. Increased missegregation and chromosome loss with decreasing chromosome size in vertebrate cells. Chromosoma. 2006;115:60-74.
39. Leclercq I, Mortreux F, Cavrois M, Leroy A, Gessain A, Wain-Hobson S, et al. Host sequences flanking the human T-cell leukemia virus type 1 provirus in vivo. J Virol. 2000;74:2305-12.
40. Oliver JL, Carpena P, Román-Rolatán R, Mata-Balaguer T, Mejias-Romero A, Hackenberg M, et al. Isochore chromosome maps of the human genome. Gene. 2002;300:117-27.
41. Lengauer C, Kinzler KW, Vogelstein B. Genetic instabilities in human cancers. Nature. 1998; 396:643-9.
42. Pavlícek A, Jabbari K, Paces J, Paces V, Hejnar J, Bernardi G. Similar integration but different stability of Alus and LINEs in the human genome. Gene. 2001;276:39-45.
43. Tsuji T, Sugahara K, Tsuruda K, Uemura A, Harasawa H, Hasegawa H, et al. Clinical and oncologic implications in epigenetic down-regulation of CD26/dipeptidyl peptidase IV in adult T-cell leukemia cells. Int J Hematol. 2004;80:254-60.
44. Derce D, Crise B, Li Y, Princler G, Lum N, Stewart C, et al. Human T-cell leukemia virus type 1 integration target sites in the human genome: comparison with those of other retroviruses. J Virol. 2007;81:6731-41.
45. Agbottah E, Deng L, Dannenberg LO, Pumfery A, Kashanchi F. Effect of SWI/SNF chromatin remodeling complex on HIV-1 Tat activated transcription. Retrovirology. 2006;3:48-67.
46. Mitchell RS, Beitzel BF, Schroder AR, Shinn P, Chen H, Berry CC, et al. Retroviral DNA integration: ASLV, HIV, and MLV show distinct target site preferences. PLoS Biol. 2004;2:1127-37.
47. Wu X, Burgess S M. Integration target site selection for retroviruses and transposable elements. Cell Mol Life Sci. 2004;61:2588-96.
48. Versteeg R, van Schaik BD, van Batenburg MF, Roos M, Monajemi R, Caron H, et al. The human transcriptome map reveals extremes in gene density, intron length, GC content, and repeat pattern for domains of highly and weakly wxpressed genes. Genome Res. 2003;13:1998-2004.
2. Edlich RF, Arnette JA, Williams FM. Global epidemic of human T-cell lymphotropic virus type-I (HTLV-I). J Emerg Med. 2000;18:109-19.
3. Quintana M, Villalobos J, Domínguez M, Tamayo O, García-Vallejo F. Estudio de la seroprevalencia de la infección por los virus linfotrópicos humanos (HTLV) I y II en poblaciones del departamento de Córdoba, Colombia. Colombia Médica. 2004;35:22-30.
4. García-Vallejo F. Caracterización molecular y genómica del proceso de integración del provirus del virus linfotropico humano (HTLV) tipo I. Rev Acad Colomb Cienc. 2006;30:155-70.
5. Yoshida M, Seiki M, Yamaguchi K, Takatsuki K. Monoclonal integration of human T-cell leukemia provirus in all primary tumors of adult T-cell leukemia suggests causative role of human T-cell leukemia virus in the disease. Proc Natl Acad Sci USA.1984;81:2534-7.
6. Yoshida M. Multiple viral strategies of HTLV-1 for dysregulation of cell growth control. Annu Rev Immunol. 2001;19:475-96.
7. Leclerq I, Mortreux F, Gabet AS, Jonson CB, Wattel E. Basis of HTLV type I site selection. AIDS Res Hum Retroviruses. 2000;16:1653-9.
8. Zoubak S, Richardson J, Rynditch AV, Hollsberg P, Hafler DA, Boeri E, et al. Regional specificity of HTLV-I proviral integration in the human genome. Gene. 1994;143:155-63.
9. Glukhova LA, Zoubak SV, Rynditch AV, Miller GG, Titova IV, Vorovyeva N, et al. Localization of HTLV-1 and HIV-1 proviral sequences in chromosomes of persistently infected cells. Chromosome Res.1999;7:177-83.
10. Richarsond JH, Rose NJ, Mann S, Ferguson-Smith M, Lever AM. Chromosomal positioning of human T-lymphotropic type I proviruses by fluorescent in situ hybridisation. J Virol Methods. 2001;93 65-74.
11. Saccone S, De Sario A, Wiegant J, Raap AK, Della-Valle G, Bernardi G. Correlations between isochores and chromosomal bands in the human genome. Proc Natl Acad Sci USA. 1993;90:11929-33.
12. Woodfine K, Fiegler H, Beare DM, Collins JE, McCann OT, Young BD, et al. Replication timing of the human genome. Hum Mol Genet. 2004;13:191-202.
13. Saccone S, Cacciò S, Kusuda J, Andreozzi L, Bernardi G. Identification of the gene-richest bands in human chromosomes. Gene. 1996;174:85-94.
14. Kim MA, Johannsmann R, Grzeschik KH. Giemsa staining of the sites replicating DNA early in human lymphocyte chromosomes. Cytogenet Cell Genet. 1975;15:363-71.
15. Federico C, Saccone S, Bernardi G. The gene-richest bands of human chromosomes replicate at the onset of the S-phase. Cytogenet Cell Genet. 1998;80:83-8.
16. Albrecht B, Lairmore MD. Critical role of human T-lymphotropic virus type 1 accessory proteins in viral replication and pathogenesis. Microbiol Mol Biol Rev. 2002;66:396-406.
17. Yasunaga JI, Matsuoka M. Human T-cell leukemia virus type I induces adult T-cell leukemia: From clinical aspects to molecular mechanisms. Cancer Control. 2007;14:133-40.
18. Albrecht B, Collins ND, Burrinstom MT, Nisbet JW, Ratner L, Green PL, et al. Human T-lymphotropic virus type I open reading frame I p12(I) is required for efficient viral infectivity in primary lymphocytes. J Virol. 2000;74:9828-35.
19. Bindhu M, Nair A, Lairmore MD. Role of accessory proteins of HTLV-1 in viral replication, T cell activation, and cellular gene expression. Front Biosci. 2004;9: 2556-76.
20. Carrascal E, Cortés A, Akiba S, Tamayo O, Quiñónez F, Floréz L, et al. Epidemiología y patología de la leucemia/linfoma de células T del adulto en Cali y el suroccidente colombiano. Colombia Médica. 2004;35:12-7.
21. República de Colombia. Ministerio de Salud. Por la cual se establecen las normas científicas, técnicas y administrativas para la investigación en salud Resolución No 008430 de octubre 4 de 1993. Bogotá: Ministerio de Salud; 1993.
22. Sambrook J, Fritzch EF, Maniatis T. Molecular cloning. A laboratory manual. New York: Ed. Cold Spring Harbor Press; 1989.
23. Seiki M, Hattori S, Hirayama Y, Yoshida M. Human adult T-cell leukemia virus: complete nucleotide sequence of the provirus genome integrated in leukemia cell DNA. Proc Natl Acad Sci USA. 1983;80:3618-22.
24. Feinberg AP, Vogelstein B. Technique for radiolabeling of restriction endonuclease fragments. Anal Biochem. 1983;132:6-13.
25. Miyoshi I, Kubonishi I, Yoshimoto S, Akagi T, Ohtsuki Y, Shiraishi Y, et al. Type C virus particles in a cord T-cell line derived by co-cultivating normal human cord leukocytes and human leukaemic T cells. Nature.1981;294:770-1.
26. Takemoto S, Matsuoka M, Yamaguchi K, Takatsuki K. A novel diagnostic method of adult T-cell leukemia: Monoclonal integration of human T-cell lymphotropic virus type I provirus DNA detected by inverse polymerase chain reaction. Blood. 1994;84:3080-5.
27. Cavrois M, Gessain A, Wain-Hobson S, Wattel E. Proliferation of HTLV-I infected circulating cells in vivo in all asymptomatic carries and patients with TSP/HAM. Oncogen. 1996;12:2419-23.
28. Cabrera J, García-Vallejo F. Aumento del número de amplicones obtenidos por IPCR en el ADN de personas seropositivas para HTLV-I afectadas con PET/HAM. Colombia Médica. 2000;31:169-75.
29. Ozawa T, Itoyama T, Sadamori N, Yamada Y, Hata T, Tomonaga M, et al. Rapid isolation of viral integration site reveals frequent integration of HTLV-1 into expressed loci. J Hum Genet. 2004;49:154-29.
30. STATA CORP. Stata Statistical Software: Release 8.0. College Station TX: Stata Corporative; 2000.
31. Venter JC, Adams MD, Myers EW, Li PW, Mural RJ, Sutton GG, et al. The sequence of the human genome. Science. 2001;291:1304-51.
32. International Human Genome Sequencing Consortium. Initial sequencing and analysis of the human genome. Nature. 2001;409:860-921.
33. Blank A. Adult T-cell leukemia/lymphoma in southwest Colombia. En: HTLV, truths and questions. Cali: Edit Zaninovic; 1996. p. 266-71.
34. Wattel E, Vartanian JP, Pannetier CH, Wain-Hobson S. Clonal expansión of human T-cell leukemia and symptomatic carries without malignancy. J. Virol. 1995;69:2863-8.
35. Wattel E, Cavrois, Gessain MA, Wain-Hobson S. Clonal expansion of infected cells –a way of life for HTLV-I. J Acquir Immune Defic Syndr Hum Retrovirol. 1996;13(Supl.1):92-9.
36. Doi K, Wu X, Taniguchi Y, Yasunaga J, Satou Y, Okayama A, et al. Preferential selection of human T-cell leukemia virus type I provirus integration sites in leukemic versus carrier status. Blood. 2005;106:1048-53.
37. Hanai S, Nitta T, Shoda M, Tanaka M, Iso N, Mizoguchi I, et al. Integration of human T-cell leukemia virus type 1 in genes of leukemia cells of patients with adult T-cell leukemia. Cancer Sci. 2004;95:306-10.
38. Spence JM, Mills W, Mann K, Huxley C, Farr CJ. Increased missegregation and chromosome loss with decreasing chromosome size in vertebrate cells. Chromosoma. 2006;115:60-74.
39. Leclercq I, Mortreux F, Cavrois M, Leroy A, Gessain A, Wain-Hobson S, et al. Host sequences flanking the human T-cell leukemia virus type 1 provirus in vivo. J Virol. 2000;74:2305-12.
40. Oliver JL, Carpena P, Román-Rolatán R, Mata-Balaguer T, Mejias-Romero A, Hackenberg M, et al. Isochore chromosome maps of the human genome. Gene. 2002;300:117-27.
41. Lengauer C, Kinzler KW, Vogelstein B. Genetic instabilities in human cancers. Nature. 1998; 396:643-9.
42. Pavlícek A, Jabbari K, Paces J, Paces V, Hejnar J, Bernardi G. Similar integration but different stability of Alus and LINEs in the human genome. Gene. 2001;276:39-45.
43. Tsuji T, Sugahara K, Tsuruda K, Uemura A, Harasawa H, Hasegawa H, et al. Clinical and oncologic implications in epigenetic down-regulation of CD26/dipeptidyl peptidase IV in adult T-cell leukemia cells. Int J Hematol. 2004;80:254-60.
44. Derce D, Crise B, Li Y, Princler G, Lum N, Stewart C, et al. Human T-cell leukemia virus type 1 integration target sites in the human genome: comparison with those of other retroviruses. J Virol. 2007;81:6731-41.
45. Agbottah E, Deng L, Dannenberg LO, Pumfery A, Kashanchi F. Effect of SWI/SNF chromatin remodeling complex on HIV-1 Tat activated transcription. Retrovirology. 2006;3:48-67.
46. Mitchell RS, Beitzel BF, Schroder AR, Shinn P, Chen H, Berry CC, et al. Retroviral DNA integration: ASLV, HIV, and MLV show distinct target site preferences. PLoS Biol. 2004;2:1127-37.
47. Wu X, Burgess S M. Integration target site selection for retroviruses and transposable elements. Cell Mol Life Sci. 2004;61:2588-96.
48. Versteeg R, van Schaik BD, van Batenburg MF, Roos M, Monajemi R, Caron H, et al. The human transcriptome map reveals extremes in gene density, intron length, GC content, and repeat pattern for domains of highly and weakly wxpressed genes. Genome Res. 2003;13:1998-2004.
How to Cite
1.
Salcedo-Cifuentes M, Cabrera J, Cuesta-Astroz Y, Carrascal E, Eizuru Y, Domínguez MC, et al. Clonal expansion and genomic characterization of the human T-cell lymphotropic virus type I during the integration process in adult T-cell leukemia/lymphoma. biomedica [Internet]. 2009 Jun. 1 [cited 2024 May 11];29(2):218-31. Available from: https://revistabiomedica.org/index.php/biomedica/article/view/24
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