Immortalization of Epstein-Barr virus-negative human B lymphocytes with minimal chromosomal instability

Pathology International

Volumn 56, Issue 11, 2006, Pages 659-667

  Yamashita, Yoriko ^a   Tsurumi, Tatsuya ^b   Mori, Naoyoshi ^a   Kiyono, Tohru ^c  

^a NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b AICHI CANCER CENTER HOSPITAL   (Japan)

^c NATIONAL CANCER CENTER RESEARCH INSTITUTE   (Japan)

Author keywords

CD40 CD40L interaction; Epstein Barr virus; HPV16 E6E7; Human B cells; Immortalization; Telomerase

Indexed keywords

CD40 ANTIGEN; CD40 LIGAND; PROTEIN E6; PROTEIN E7; PROTEIN P16; RETINOBLASTOMA PROTEIN; RETROVIRUS VECTOR; TELOMERASE;

ARTICLE; B LYMPHOCYTE; CELL IMMORTALIZATION; CELL LINE; CELL PROLIFERATION; CHROMOSOMAL INSTABILITY; CHROMOSOME ANALYSIS; CONTROLLED STUDY; ENZYME ACTIVITY; EPITHELIUM CELL; EPSTEIN BARR VIRUS; GENE; GENE FUNCTION; GENETIC TRANSDUCTION; HUMAN; HUMAN CELL; HUMAN PAPILLOMAVIRUS TYPE 16; KARYOTYPE; NONHUMAN; NORMAL HUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TELOMERE; VIRUS GENOME; VIRUS INFECTION;

ANTIGENS, CD40; B-LYMPHOCYTES; CD40 LIGAND; CELL LINE, TRANSFORMED; CELL TRANSFORMATION, VIRAL; CHROMOSOMAL INSTABILITY; FLOW CYTOMETRY; GENE EXPRESSION REGULATION, VIRAL; HERPESVIRUS 4, HUMAN; HUMANS; IMMUNOPHENOTYPING; IN SITU HYBRIDIZATION; KARYOTYPING; ONCOGENE PROTEINS, VIRAL; PAPILLOMAVIRUS E7 PROTEINS; REPRESSOR PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TELOMERASE; TRANSDUCTION, GENETIC;

EID: 33750033153     PISSN: 13205463     EISSN: 14401827     Source Type: Journal    
DOI: 10.1111/j.1440-1827.2006.02026.x     Document Type: Article

References (44)

1. Hayflick L. The limited in vitro lifespan of human diploid cell strains. Exp Cell Res 1965; 37: 614-21.
2. Ishikawa F. Cellular senescence, an unpopular yet trustworthy tumor suppressor mechanism. Cancer Sci 2003; 94: 944-7.
3. Itahana K, Campisi J, Dimri GP. Mechanisms of cellular senescence in human and mouse cells. Biogerontology 2004; 5: 1-10.
4. Sherr CJ. Principles of tumor suppression. Cell 2004; 116: 235-46.
5. Miller G. Immortalization of human lymphocytes by Epstein-Barr virus. Yale J Biol Med 1982; 55: 305-10.
6. Steinberg ML, Defendi V. Transformation and immortalization of human keratinocytes by SV40. J Invest Dermatol 1983; 81: 131-6.
7. Smogorzewska A, de Lange T. Different telomere damage signaling pathways in human and mouse cells. EMBO J 2002; 21: 4338-48.
8. Bodnar AG, Ouellette M, Frolkis M et al. Extension of life-span by introduction of telomerase into normal human cells. Science 1998; 279: 349-52.
9. Terai M, Uyama T, Sugiki T, Li XK, Umezawa A, Kiyono T. Immortalization of human fetal cells: The life span of umbilical cord blood-derived cells can be prolonged without manipulating p16INK4a/RB braking pathway. Mol Biol Cell 2005; 16: 1491-9.
10. Kiyono T, Foster SA, Koop JI, McDougall JK, Galloway DA, Klingelhutz AJ. Both Rb/p16INK4a inactivation and telomerase activity are required to immortalize human epithelial cells. Nature 1998; 396: 84-8.
11. Veldman T, Liu X, Yuan H, Schlegel R. Human papillomavirus E6 and Myc proteins associate in vivo and bind to and cooperatively activate the telomerase reverse transcriptase promoter. Proc Natl Acad Sci USA 2003; 100: 8211-16.
12. Gewin L, Myers H, Kiyono T, Galloway DA. Identification of a novel telomerase repressor that interacts with the human papillomavirus type-16, E6/E6-AP complex. Genes Dev 2004; 18: 2269-82.
13. Okamoto T, Aoyama T, Nakayama T et al. Clonal heterogeneity in differentiation potential of immortalized human mesenchymal stem cells. Biochem Biophys Res Commun 2002; 295: 354-61.
14. Kyo S, Nakamura M, Kiyono T et al. Successful immortalization of endometrial glandular cells with normal structural and functional characteristics. Am J Pathol 2003; 163: 2259-69.
15. Ahuja D, Saenz-Robles MT, Pipas JM. SV40 large T antigen targets multiple cellular pathways to elicit cellular transformation. Oncogene 2005; 24: 7729-45.
16. Sugimoto M, Tahara H, Ide T, Furuichi Y. Steps involved in immortalization and tumorigenesis in human B-lymphoblastoid cell lines transformed by Epstein-Barr virus. Cancer Res 2004; 64: 3361-4.
17. Cohen JI, Wang F, Kieff E. Epstein-Barr virus nuclear protein 2 mutations define essential domains for transformation and transactivation. J Virol 1991; 65: 2545-54.
18. Hammerschmidt W, Sugden B. Genetic analysis of immortalizing functions of Epstein-Barr virus in human B lymphocytes. Nature 1989; 340: 393-7.
19. Kaye KM, Izumi KM, Kieff E. Epstein-Barr virus latent membrane protein 1 is essential for B-lymphocyte growth transformation. Proc Natl Acad Sci USA 1993; 90: 9150-54.
20. Tomkinson B, Robertson E, Kieff E. Epstein-Barr virus nuclear proteins EBNA-3A and EBNA-3C are essential for B-lymphocyte growth transformation. J Virol 1993; 67: 2014-25.
21. Humme S, Reisbach G, Feederle R et al. The EBV nuclear antigen 1 (EBNA1) enhances B cell immortalization several thousandfold. Proc Natl Acad Sci USA 2003; 100: 10 989-94.
22. Masutomi K, Yu EY, Khurts S et al. Telomerase maintains telomere structure in normal human cells. Cell 2003; 114: 241-53.
23. Liu K, Schoonmaker MM, Levine BL, June CH, Hodes RJ, Weng NP. Constitutive and regulated expression of telomerase reverse transcriptase (hTERT) in human lymphocytes. Proc Natl Acad Sci USA 1999; 96: 5147-52.
24. Weng NP, Granger L, Hodes RJ. Telomere lengthening and telomerase activation during human B cell differentiation. Proc Natl Acad Sci USA 1997; 94: 10 827-32.
25. Hu BT, Lee SC, Marin E, Ryan DH, Insel RA. Telomerase is up-regulated in human germinal center B cells in vivo and can be re-expressed in memory B cells activated in vitro. J Immunol 1997; 159: 1068-71.
26. Schultze JL, Cardoso AA, Freeman GJ et al. Follicular lymphomas can be induced to present alloantigen efficiently: A conceptual model to improve their tumor immunogenicity. Proc Natl Acad Sci USA 1995; 92: 8200-4.
27. Kondo E, Topp MS, Kiem HP et al. Efficient generation of antigen-specific cytotoxic T cells using retrovirally transduced CD40-activated B cells. J Immunol 2002; 169: 2164-71.
28. Smotkin D, Prokoph H, Wettstein FO. Oncogenic and nononcogenic human genital papillomaviruses generate the E7 mRNA by different mechanisms. J Virol 1989; 63: 1441-7.
29. Naviaux RK, Costanzi E, Haas M, Verma IM. The pCL vector system: Rapid production of helper-free, high-titer, recombinant retroviruses. J Virol 1996; 70: 5701-5.
30. Miller AD, Garcia JV, von Suhr N, Lynch CM, Wilson C, Eiden MV. Construction and properties of retrovirus packaging cells based on gibbon ape leukemia virus. J Virol 1991; 65: 2220-24.
31. Gudjonsson T, Villadsen R, Nielsen HL, Ronnov-Jessen L, Bissell MJ, Petersen OW. Isolation, immortalization, and characterization of a human breast epithelial cell line with stem cell properties. Genes Dev 2002; 16: 693-706.
32. Foster SA, Wong DJ, Barrett MT, Galloway DA. Inactivation of p16 in human mammary epithelial cells by CpG island methylation. Mol Cell Biol 1998; 18: 1793-801.
33. Alcorta DA, Xiong Y, Phelps D, Hannon G, Beach D, Barrett JC. Involvement of the cyclin-dependent kinase inhibitor p16 (INK4a) in replicative senescence of normal human fibroblasts. Proc Natl Acad Sci USA 1996; 93: 13 742-7.
34. Erickson S, Sangfelt O, Heyman M, Castro J, Einhorn S, Grander D. Involvement of the Ink4 proteins p16 and p15 in T-lymphocyte senescence. Oncogene 1998; 17: 595-602.
35. Herbert BS, Wright WE, Shay JW. p16 (INK4a) inactivation is not required to immortalize human mammary epithelial cells. Oncogene 2002; 21: 7897-900.
36. Rheinwald JG, Hahn WC, Ramsey MR et al. A two-stage, p16 (INK4A)- and p53-dependent keratinocyte senescence mechanism that limits replicative potential independent of telomere status. Mol Cell Biol 2002; 22: 5157-72.
37. Igarashi H, Sakaguchi N. Telomerase activity is induced in human peripheral B lymphocytes by the stimulation to antigen receptor. Blood 1997; 89: 1299-307.
38. Jung D, Neron S, Lemieux R, Roy A, Richard M. Telomere-independent reduction of human B lymphocyte: Proliferation during long-term culture. Immunol Invest 2001; 30: 157-68.
39. Klingelhutz AJ, Foster SA, McDougall JK. Telomerase activation by the E6 gene product of human papillomavirus type 16. Nature 1996; 380: 79-82.
40. Scheffner M, Werness BA, Huibregtse JM, Levine AJ, Howley PM. The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53. Cell 1990; 63: 1129-36.
41. Imadome K, Shirakata M, Shimizu N, Nonoyama S, Yamanashi Y. CD40 ligand is a critical effector of Epstein-Barr virus in host cell survival and transformation. Proc Natl Acad Sci USA 2003; 100: 7836-40.
42. Yatabe Y, Oka K, Asai J, Mori N. Poor correlation between clonal immunoglobulin gene rearrangement and immunoglobulin gene transcription in Hodgkin's disease. Am J Pathol 1996; 149: 1351-61.
43. Akimov SS, Ramezani A, Hawley TS, Hawley RG. Bypass of senescence, immortalization, and transformation of human hematopoietic progenitor cells. Stem Cells 2005; 9: 1423-33.
44. Ohtani N, Brennan P, Gaubatz S et al. Epstein-Barr virus LMP1 blocks p16INK4a-RB pathway by promoting nuclear export of E2F4/5. J Cell Biol 2003; 162: 173-83.