Human short-term repopulating cells have enhanced telomerase reverse transcriptase expression

Blood

Volumn 108, Issue 3, 2006, Pages 1084-1091

  Järås, Marcus ^b   Edqvist, Anna ^b   Rebetz, Johan ^b   Salford, Leif G ^b   Widegren, Bengt ^b   Fan, Xiaolong ^a  

^a LUND UNIVERSITY   (Sweden)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; CD34 ANTIGEN; GREEN FLUORESCENT PROTEIN; KI 67 ANTIGEN; TELOMERASE REVERSE TRANSCRIPTASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PURIFICATION; ARTICLE; BONE MARROW; CELL CYCLE G0 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE S PHASE; CELL SELECTION; COLONY FORMATION; CONTROLLED STUDY; DIABETES MELLITUS; DISEASE SEVERITY; GENETIC CODE; GENETIC REGULATION; GENETIC TRANSDUCTION; IMMUNE DEFICIENCY; MOUSE; MULTIPOTENT STEM CELL; NONHUMAN; OBESITY; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; UMBILICAL CORD BLOOD;

EID: 33746640430     PISSN: 00064971     EISSN: 00064971     Source Type: Journal    
DOI: 10.1182/blood-2005-09-008904     Document Type: Article

References (59)

1. Weissman IL. Stem cells: units of development, units of regeneration, and units in evolution. Cell. 2000;100:157-168.
2. Moyzis RK, Buckingham JM, Cram LS, et al. A highly conserved repetitive DNA sequence, (TTAGGG)n, present at the telomeres of human chromosomes. Proc Natl Acad Sci U S A. 1988;85:6622-6626.
3. Artandi SE, Chang S, Lee SL, et al. Telomere dysfunction promotes non-reciprocal translocations and epithelial cancers in mice. Nature. 2000;406:641-645.
4. Zakian VA. Telomeres: beginning to understand the end. Science. 1995;270:1601-1607.
5. Sharma GG, Gupta A, Wang H, et al. hTERT associates with human telomeres and enhances genomic stability and DNA repair. Oncogene. 2003;22:131-146.
6. Li S, Crothers J, Haqq CM, Blackburn EH. Cellular and gene expression responses involved in the rapid growth inhibition of human cancer cells by RNA interference-mediated depletion of telomerase RNA. J Biol Chem. 2005;280:23709-23717.
7. Belair CD, Yeager TR, Lopez PM, Reznikoff CA. Telomerase activity: a biomarker of cell proliferation, not malignant transformation. Proc Natl Acad Sci U S A. 1997;94:13677-13682.
8. Meyerson M, Counter CM, Eaton EN, et al. hEST2, the putative human telomerase catalytic subunit gene, is up-regulated in tumor cells and during immortalization. Cell. 1997;90:785-795.
9. Weinrich SL, Pruzan R, Ma L, et al. Reconstitution of human telomerase with the template RNA component hTR and the catalytic protein subunit hTRT. Nat Genet. 1997;17:498-502.
10. Sharpless NE, DePinho RA. Telomeres, stem cells, senescence, and cancer. J Clin Invest. 2004;113:160-168.
11. Morrison SJ, Prowse KR, Ho P, Weissman IL. Telomerase activity in hematopoietic cells is associated with self-renewal potential. Immunity. 1996;5:207-216.
12. Allsopp RC, Cheshier S, Weissman IL. Telomere shortening accompanies increased cell cycle activity during serial transplantation of hematopoietic stem cells. J Exp Med. 2001;193:917-924.
13. Allsopp RC, Morin GB, DePinho R, Harley CB, Weissman IL. Telomerase is required to slow telomere shortening and extend replicative lifespan of HSCs during serial transplantation. Blood. 2003;102:517-520.
14. Lee HW, Blasco MA, Gottlieb GJ, Horner JW 2nd, Greider CW, DePinho RA. Essential role of mouse telomerase in highly proliferative organs. Nature. 1998;392:569-574.
15. Ly H, Schertzer M, Jastaniah W, et al. Identification and functional characterization of 2 variant alleles of the telomerase RNA template gene (TERC) in a patient with dyskeratosis congenita. Blood. 2005;106:1246-1252.
16. Marrone A, Stevens D, Vulliamy T, Dokal I, Mason PJ. Heterozygous telomerase RNA mutations found in dyskeratosis congenita and aplastic anemia reduce telomerase activity via haploinsufficiency. Blood. 2004;104:3936-3942.
17. Vulliamy T, Marrone A, Szydlo R, Walne A, Mason PJ, Dokal I. Disease anticipation is associated with progressive telomere shortening in families with dyskeratosis congenita due to mutations in TERC. Nat Genet. 2004;36:447-449.
18. Vulliamy T, Marrone A, Dokal I, Mason PJ. Association between aplastic anaemia and mutations in telomerase RNA. Lancet. 2002;359:2168-2170.
19. Vulliamy T, Marrone A, Goldman F, et al. The RNA component of telomerase is mutated in autosomal dominant dyskeratosis congenita. Nature. 2001;413:432-435.
20. Fogarty PF, Yamaguchi H, Wiestner A, et al. Late presentation of dyskeratosis congenita as apparently acquired aplastic anaemia due to mutations in telomerase RNA. Lancet. 2003;362:1628-1630.
21. Yamaguchi H, Baerlocher GM, Lansdorp PM, et al. Mutations of the human telomerase RNA gene (TERC) in aplastic anemia and myelodysplastic syndrome. Blood. 2003;102:916-918.
22. Yamaguchi H, Calado RT, Ly H, et al. Mutations in TERT, the gene for telomerase reverse transcriptase, in aplastic anemia. N Engl J Med. 2005;352:1413-1424.
23. Engelhardt M, Kumar R, Albanell J, Pettengell R, Han W, Moore MA. Telomerase regulation, cell cycle, and telomere stability in primitive hematopoietic cells. Blood. 1997;90:182-193.
24. Engelhardt M, Mackenzie K, Drullinsky P, Silver RT, Moore MA. Telomerase activity and telomere length in acute and chronic leukemia, pre- and post-ex vivo culture. Cancer Res. 2000;60:610-617.
25. Yui J, Chiu CP, Lansdorp PM. Telomerase activity in candidate stem cells from fetal liver and adult bone marrow. Blood. 1998;91:3255-3262.
26. Bhatia M, Wang JCY, Kapp U, Bonnet D, Dick JE. Purification of primitive human hematopoietic cells capable of repopulating immune-deficient mice. Proc Natl Acad Sci U S A. 1997;94:5320-5325.
27. Hogan CJ, Shpall EJ, Keller G. Differential long-term and multilineage engraftment potential from subfractions of human CD34+ cord blood cells transplanted into NOD/SCID mice. Proc Natl Acad Sci U S A. 2002;99:413-418.
28. Guenechea G, Gan OI, Dorrell C, Dick JE. Distinct classes of human stem cells that differ in proliferative and self-renewal potential. Nat Immunol. 2001;2:75-82.
29. Glimm H, Eisterer W, Lee K, et al. Previously undetected human hematopoietic cell populations with short-term repopulating activity selectively engraft NOD/SCID-beta2 microglobulin-null mice. J Clin Invest. 2001;107:199-206.
30. Mazurier F, Doedens M, Gan OI, Dick JE. Rapid myeloerythroid repopulation after intrafemoral transplantation of NOD-SCID mice reveals a new class of human stem cells. Nat Med. 2003;9:959-963.
31. Shultz LD, Banuelos SJ, Leif J, et al. Regulation of human short-term repopulating cell (STRC) engraftment in NOD/SCID mice by host CD122+ cells. Exp Hematol. 2003;31:551-558.
32. Mazurier F, Gan OI, McKenzie JL, Doedens M, Dick JE. Lentivector-mediated clonal tracking reveals intrinsic heterogeneity in the human hematopoietic stem cell compartment and culture-induced stem cell impairment. Blood. 2004;103:545-552.
33. Nilsson M, Ljungberg J, Richter J, et al. Development of an adenoviral vector system with adenovirus serotype 35 tropism; efficient transient gene transfer into primary malignant hematopoietic cells. J Gene Med. 2004;6:631-641.
34. Shayakhmetov DM, Papayannopoulou T, Stamatoyannopoulos G, Lieber A. Efficient gene transfer into human CD34(+) cells by a retargeted adenovirus vector. J Virol. 2000;74:2567-2583.
35. Gaggar A, Shayakhmetov DM, Lieber A. CD46 is a cellular receptor for group B adenoviruses. Nat Med. 2003;9:1408-1412.
36. Nilsson M, Karlsson S, Fan X. Functionally distinct subpopulations of cord blood CD34+ cells are transduced by adenoviral vectors with serotype 5 or 35 tropism. Mol Ther. 2004;9:377-388.
37. Li X, Zhao X, Fang Y, et al. Generation of destabilized green fluorescent protein as a transcription reporter. J Biol Chem. 1998;273:34970-34975.
38. Edqvist A, Rebetz J, Järås M, Salford L, Widegren B, Fan X. Detection of cell cycle- and differentiation stage-dependent human telomerase reverse transcriptase expression in single living cancer cells. Mol Ther. Prepublished on March 31, 2006, as DOI 1016/j.ymthe.2005.12.018.
39. Thompson JM, Gralow JR, Levy R, Miller RA. The optimal application of forward and ninety-degree light scatter in flow cytometry for the gating of mononuclear cells. Cytometry. 1985;6:401-406.
40. Jordan CT, Yamasaki G, Minamoto D. High-resolution cell cycle analysis of defined phenotypic subsets within primitive human hematopoietic cell populations. Exp Hematol. 1996;24:1347-1355.
41. Fan X, Brun A, Segren S, Jacobsen SE, Karlsson S. Efficient adenoviral vector transduction of human hematopoietic SCID-repopulating and long-term culture-initiating cells. Hum Gene Ther. 2000;11:1313-1327.
42. Woods NB, Fahlman C, Mikkola H, et al. Lentiviral gene transfer into primary and secondary NOD/SCID repopulating cells. Blood. 2000;96:3725-3733.
43. Borge OJ, Ramsfjell V, Cui L, Jacobsen SE. Ability of early acting cytokines to directly promote survival and suppress apoptosis of human primitive CD34+CD38- bone marrow cells with multilineage potential at the single-cell level: key role of thrombopoietin. Blood. 1997;90:2282-2292.
44. Ramsfjell V, Borge OJ, Cui L, Jacobsen SE. Thrombopoietin directly and potently stimulates multilineage growth and progenitor cell expansion from primitive (CD34+ CD38-) human bone marrow progenitor cells: distinct and key interactions with the ligands for c-kit and flt3, and inhibitory effects of TGF-beta and TNF-alpha. J Immunol. 1997;158:5169-5177.
45. Holt SE, Aisner DL, Shay JW, Wright WE. Lack of cell cycle regulation of telomerase activity in human cells. Proc Natl Acad Sci U S A. 1997;94:10687-10692.
46. Holt SE, Wright WE, Shay JW. Regulation of telomerase activity in immortal cell lines. Mol Cell Biol. 1996;16:2932-2939.
47. Masutomi K, Yu EY, Khurts S, et al. Telomerase maintains telomere structure in normal human cells. Cell. 2003;114:241-253.
48. Zhu X, Kumar R, Mandal M, et al. Cell cycle-dependent modulation of telomerase activity in tumor cells. Proc Natl Acad Sci U S A. 1996;93:6091-6095.
49. Kollet O, Peled A, Byk T, et al. beta2 microglobulin-deficient (B2m(null)) NOD/SCID mice are excellent recipients for studying human stem cell function. Blood. 2000;95:3102-3105.
50. Glimm H, Oh IH, Eaves CJ. Human hematopoietic stem cells stimulated to proliferate in vitro lose engraftment potential during their S/G(2)/M transit and do not reenter G(0). Blood. 2000;96:4185-4193.
51. Chiu CP, Dragowska W, Kim NW, et al. Differential expression of telomerase activity in hematopoietic progenitors from adult human bone marrow. Stem Cells. 1996;14:239-248.
52. Gammaitoni L, Weisel KC, Gunetti M, et al. Elevated telomerase activity and minimal telomere loss in cord blood long-term cultures with extensive stem cell replication. Blood. 2004;103:4440-4448.
53. Dorrell C, Gan OI, Pereira DS, Hawley RG, Dick JE. Expansion of human cord blood CD34(+) CD38(-) cells in ex vivo culture during retroviral transduction without a corresponding increase in SCID repopulating cell (SRC) frequency: dissociation of SRC phenotype and function. Blood. 2000;95:102-110.
54. Allsopp RC, Weissman IL. Replicative senescence of hematopoietic stem cells during serial transplantation: does telomere shortening play a role? Oncogene. 2002;21:3270-3273.
55. Hiyama K, Hirai Y, Kyoizumi S, et al. Activation of telomerase in human lymphocytes and hematopoietic progenitor cells. J Immunol. 1995;155:3711-3715.
56. Roelofs H, de Pauw ES, Zwinderman AH, et al. Homeostasis of telomere length rather than telomere shortening after allogeneic peripheral blood stem cell transplantation. Blood. 2003;101:358-362.
57. Thornley I, Sutherland R, Wynn R, et al. Early hematopoietic reconstitution after clinical stem cell transplantation: evidence for stochastic stem cell behavior and limited acceleration in telomere loss. Blood. 2002;99:2387-2396.
58. Kohn DB, Sadelain M, Glorioso JC. Occurrence of leukaemia following gene therapy of X-linked SCID. Nat Rev Cancer. 2003;3:477-488.
59. Kustikova O, Fehse B, Modlich U, et al. Clonal dominance of hematopoietic stem cells triggered by retroviral gene marking. Science. 2005;308:1171-1174.