Collapse of Telomere homeostasis in hematopoietic cells caused by heterozygous mutations in Telomerase genes

PLoS Genetics

Volumn 8, Issue 5, 2012, Pages

  Aubert, Geraldine ^a   Baerlocher, Gabriela M ^a,b,e   Vulto, Irma ^a   Poon, Steven S ^a   Lansdorp, Peter M ^a,c,d  

^a BRITISH COLUMBIA CANCER AGENCY   (Canada)

^b UNIVERSITY OF BERN   (Switzerland)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^d UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^e UNIVERSITY OF BERN   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

TELOMERASE; TELOMERASE REVERSE TRANSCRIPTASE; RNA; TELOMERASE RNA; TERT PROTEIN, HUMAN;

ADULT; AGE; AGE DISTRIBUTION; AGED; AGING; ARTICLE; CELL SUBPOPULATION; CHILD; CONTROLLED STUDY; DOWN REGULATION; FEMALE; FLUORESCENCE IN SITU HYBRIDIZATION; GENE FUNCTION; GENE IDENTIFICATION; GENE LOCATION; GENETIC SUSCEPTIBILITY; GRANULOCYTE; HEMATOPOIETIC CELL; HETEROZYGOTE; HUMAN; INFANT; MALE; MUTATIONAL ANALYSIS; MUTATOR GENE; SCHOOL CHILD; SEX DIFFERENCE; TELOMERASE REVERSE TRANSCRIPTASE GENE; TELOMERASE RNA TEMPLATE GENE; TELOMERE HOMEOSTASIS; ADOLESCENT; CELL AGING; CELL DEATH; CYTOLOGY; GENETICS; HEMATOPOIETIC STEM CELL; LYMPHOCYTE; MIDDLE AGED; MUTATION; PRESCHOOL CHILD; SEXUAL DEVELOPMENT; TELOMERE;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; AGING; CELL AGING; CELL DEATH; CHILD; CHILD, PRESCHOOL; GRANULOCYTES; HEMATOPOIETIC STEM CELLS; HETEROZYGOTE; HUMANS; INFANT; LYMPHOCYTES; MIDDLE AGED; MUTATION; RNA; SEX CHARACTERISTICS; TELOMERASE; TELOMERE; TELOMERE HOMEOSTASIS; YOUNG ADULT;

EID: 84863641682     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002696     Document Type: Article

References (64)

1. d'Adda di Fagagna F, Reaper PM, Clay-Farrace L, Fiegler H, Carr P, et al. (2003) A DNA damage checkpoint response in telomere-initiated senescence. Nature 426: 194-198.
2. Smogorzewska A, de Lange T, (2002) Different telomere damage signaling pathways in human and mouse cells. Embo J 21: 4338-4348.
3. Britt-Compton B, Rowson J, Locke M, Mackenzie I, Kipling D, et al. (2006) Structural stability and chromosome-specific telomere length is governed by cis-acting determinants in humans. Hum Mol Genet 15: 725-733.
4. Greider CW, Blackburn EH, (1985) Identification of a specific telomere terminal transferase activity in Tetrahymena extracts. Cell 43: 405-413.
5. Muntoni A, Neumann AA, Hills M, Reddel RR, (2009) Telomere elongation involves intra-molecular DNA replication in cells utilizing alternative lengthening of telomeres. Hum Mol Genet 18: 1017-1027.
6. Lansdorp PM, (2005) Major cutbacks at chromosome ends. Trends Biochem Sci 30: 388-395.
7. Hemann MT, Strong MA, Hao LY, Greider CW, (2001) The shortest telomere, not average telomere length, is critical for cell viability and chromosome stability. Cell 107: 67-77.
8. Aubert G, Lansdorp PM, (2008) Telomeres and aging. Physiol Rev 88: 557-579.
9. Aubert G, Hills M, Lansdorp PM, (2011) Telomere length measurement-Caveats and a critical assessment of the available technologies and tools. Mutat Res 730: 59-67.
10. Lansdorp PM, Verwoerd NP, van de Rijke FM, Dragowska V, Little MT, et al. (1996) Heterogeneity in telomere length of human chromosomes. Hum Mol Genet 5: 685-691.
11. Martens UM, Zijlmans JM, Poon SS, Dragowska W, Yui J, et al. (1998) Short telomeres on human chromosome 17p. Nat Genet 18: 76-80.
12. Chang E, Harley CB, (1995) Telomere length and replicative aging in human vascular tissues. Proc Natl Acad Sci U S A 92: 11190-11194.
13. Hastie ND, Dempster M, Dunlop MG, Thompson AM, Green DK, et al. (1990) Telomere reduction in human colorectal carcinoma and with ageing. Nature 346: 866-868.
14. Rufer N, Brummendorf TH, Kolvraa S, Bischoff C, Christensen K, et al. (1999) Telomere fluorescence measurements in granulocytes and T lymphocyte subsets point to a high turnover of hematopoietic stem cells and memory T cells in early childhood. J Exp Med 190: 157-167.
15. Slagboom PE, Droog S, Boomsma DI, (1994) Genetic determination of telomere size in humans: a twin study of three age groups. Am J Hum Genet 55: 876-882.
16. Harley CB, Futcher AB, Greider CW, (1990) Telomeres shorten during ageing of human fibroblasts. Nature 345: 458-460.
17. Baerlocher GM, Mak J, Roth A, Rice KS, Lansdorp PM, (2003) Telomere shortening in leukocyte subpopulations from baboons. J Leukoc Biol 73: 289-296.
18. Hills M, Lucke K, Chavez EA, Eaves CJ, Lansdorp PM, (2009) Probing the mitotic history and developmental stage of hematopoietic cells using single telomere length analysis (STELA). Blood 113: 5765-5775.
19. Vaziri H, Dragowska W, Allsopp RC, Thomas TE, Harley CB, et al. (1994) Evidence for a mitotic clock in human hematopoietic stem cells: loss of telomeric DNA with age. Proc Natl Acad Sci U S A 91: 9857-9860.
20. Broccoli D, Young JW, de Lange T, (1995) Telomerase activity in normal and malignant hematopoietic cells. Proc Natl Acad Sci U S A 92: 9082-9086.
21. Chiu CP, Dragowska W, Kim NW, Vaziri H, Yui J, et al. (1996) Differential expression of telomerase activity in hematopoietic progenitors from adult human bone marrow. Stem Cells 14: 239-248.
22. Weng NP, Palmer LD, Levine BL, Lane HC, June CH, et al. (1997) Tales of tails: regulation of telomere length and telomerase activity during lymphocyte development, differentiation, activation, and aging. Immunol Rev 160: 43-54.
23. Shepherd BE, Guttorp P, Lansdorp PM, Abkowitz JL, (2004) Estimating human hematopoietic stem cell kinetics using granulocyte telomere lengths. Exp Hematol 32: 1040-1050.
24. Calado RT, Young NS, (2009) Telomere diseases. N Engl J Med 361: 2353-2365.
25. Alter BP, Baerlocher GM, Savage SA, Chanock SJ, Weksler BB, et al. (2007) Very short telomere length by flow fluorescence in situ hybridization identifies patients with dyskeratosis congenita. Blood 110: 1439-1447.
26. Kirwan M, Dokal I, (2008) Dyskeratosis congenita: a genetic disorder of many faces. Clin Genet 73: 103-112.
27. Armanios MY, Chen JJ, Cogan JD, Alder JK, Ingersoll RG, et al. (2007) Telomerase mutations in families with idiopathic pulmonary fibrosis. N Engl J Med 356: 1317-1326.
28. Baerlocher GM, Rice K, Vulto I, Lansdorp PM, (2007) Longitudinal data on telomere length in leukocytes from newborn baboons support a marked drop in stem cell turnover around 1 year of age. Aging Cell 6: 121-123.
29. Ju Z, Jiang H, Jaworski M, Rathinam C, Gompf A, et al. (2007) Telomere dysfunction induces environmental alterations limiting hematopoietic stem cell function and engraftment. Nat Med 13: 742-747.
30. Park JI, Venteicher AS, Hong JY, Choi J, Jun S, et al. (2009) Telomerase modulates Wnt signalling by association with target gene chromatin. Nature 460: 66-72.
31. Xu L, Blackburn EH, (2007) Human cancer cells harbor T-stumps, a distinct class of extremely short telomeres. Mol Cell 28: 315-327.
32. Takai H, Smogorzewska A, de Lange T, (2003) DNA damage foci at dysfunctional telomeres. Curr Biol 13: 1549-1556.
33. Lansdorp PM, (2000) Repair of telomeric DNA prior to replicative senescence. Mech Ageing Dev 118: 23-34.
34. Rhee DB, Ghosh A, Lu J, Bohr VA, Liu Y, (2011) Factors that influence telomeric oxidative base damage and repair by DNA glycosylase OGG1. DNA Repair (Amst) 10: 34-44.
35. Sahin E, Colla S, Liesa M, Moslehi J, Muller FL, et al. (2011) Telomere dysfunction induces metabolic and mitochondrial compromise. Nature 470: 359-365.
36. Baker DJ, Wijshake T, Tchkonia T, LeBrasseur NK, Childs BG, et al. (2011) Clearance of p16Ink4a-positive senescent cells delays ageing-associated disorders. Nature 479: 232-236.
37. Vulliamy TJ, Dokal I, (2008) Dyskeratosis congenita: the diverse clinical presentation of mutations in the telomerase complex. Biochimie 90: 122-130.
38. Frenck RW Jr, Blackburn EH, Shannon KM, (1998) The rate of telomere sequence loss in human leukocytes varies with age. Proc Natl Acad Sci U S A 95: 5607-5610.
39. Lansdorp PM, Dragowska W, Mayani H, (1993) Ontogeny-related changes in proliferative potential of human hematopoietic cells. J Exp Med 178: 787-791.
40. Bowie MB, Kent DG, Dykstra B, McKnight KD, McCaffrey L, et al. (2007) Identification of a new intrinsically timed developmental checkpoint that reprograms key hematopoietic stem cell properties. Proc Natl Acad Sci U S A 104: 5878-5882.
41. Kim I, Saunders TL, Morrison SJ, (2007) Sox17 dependence distinguishes the transcriptional regulation of fetal from adult hematopoietic stem cells. Cell 130: 470-483.
42. Lansdorp PM, (2009) Telomeres and disease. EMBO J 28: 2532-2540.
43. Mocchegiani E, Malavolta M, (2004) NK and NKT cell functions in immunosenescence. Aging Cell 3: 177-184.
44. Buchkovich KJ, Greider CW, (1996) Telomerase regulation during entry into the cell cycle in normal human T cells. Mol Biol Cell 7: 1443-1454.
45. Geiger H, Rudolph KL, (2009) Aging in the lympho-hematopoietic stem cell compartment. Trends Immunol 30: 360-365.
46. Knudson M, Kulkarni S, Ballas ZK, Bessler M, Goldman F, (2005) Association of immune abnormalities with telomere shortening in autosomal-dominant dyskeratosis congenita. Blood 105: 682-688.
47. Benetos A, Okuda K, Lajemi M, Kimura M, Thomas F, et al. (2001) Telomere length as an indicator of biological aging: The gender effect and relation with pulse pressure and pulse wave velocity. Hypertension 37: 381-385.
48. Calado RT, Yewdell WT, Wilkerson KL, Regal JA, Kajigaya S, et al. (2009) Sex hormones, acting on the TERT gene, increase telomerase activity in human primary hematopoietic cells. Blood 114: 2236-2243.
49. Salpea KD, Humphries SE, (2010) Telomere length in atherosclerosis and diabetes. Atherosclerosis 209: 35-38.
50. Epel ES, Blackburn EH, Lin J, Dhabhar FS, Adler NE, et al. (2004) Accelerated telomere shortening in response to life stress. Proc Natl Acad Sci U S A 101: 17312-17315.
51. Cawthon RM, Smith KR, O'Brien E, Sivatchenko A, Kerber RA, (2003) Association between telomere length in blood and mortality in people aged 60 years or older. Lancet 361: 393-395.
52. Njajou OT, Hsueh WC, Blackburn EH, Newman AB, Wu SH, et al. (2009) Association between telomere length, specific causes of death, and years of healthy life in health, aging, and body composition, a population-based cohort study. J Gerontol A Biol Sci Med Sci 64: 860-864.
53. Alder JK, Chen JJ, Lancaster L, Danoff S, Su SC, et al. (2008) Short telomeres are a risk factor for idiopathic pulmonary fibrosis. Proc Natl Acad Sci U S A 105: 13051-13056.
54. Calado RT, Regal JA, Hills M, Yewdell WT, Dalmazzo LF, et al. (2009) Constitutional hypomorphic telomerase mutations in patients with acute myeloid leukemia. Proc Natl Acad Sci U S A 106: 1187-1192.
55. Calado RT, Regal JA, Kajigaya S, Young NS, (2009) Erosion of telomeric single-stranded overhang in patients with aplastic anaemia carrying telomerase complex mutations. Eur J Clin Invest 39: 1025-1032.
56. Goldman FD, Aubert G, Klingelhutz AJ, Hills M, Cooper SR, et al. (2008) Characterization of primitive hematopoietic cells from patients with dyskeratosis congenita. Blood 111: 4523-4531.
57. Ly H, Schertzer M, Jastaniah W, Davis J, Yong SL, et al. (2005) Identification and functional characterization of two variant alleles of the telomerase RNA template gene (TERC) in a patient with Dyskeratosis Congenita. Blood 106: 1246-1252.
58. Yamaguchi H, Baerlocher GM, Lansdorp PM, Chanock SJ, Nunez O, et al. (2003) Mutations of the human telomerase RNA gene (TERC) in aplastic anemia and myelodysplastic syndrome. Blood 102: 916-918.
59. Yamaguchi H, Calado RT, Ly H, Kajigaya S, Baerlocher GM, et al. (2005) Mutations in TERT, the gene for telomerase reverse transcriptase, in aplastic anemia. N Engl J Med 352: 1413-1424.
60. Taneja KL, Chavez EA, Coull J, Lansdorp PM, (2001) Multicolor fluorescence in situ hybridization with peptide nucleic acid probes for enumeration of specific chromosomes in human cells. Genes Chromosomes Cancer 30: 57-63.
61. Baerlocher GM, Vulto I, de Jong G, Lansdorp PM, (2006) Flow cytometry and FISH to measure the average length of telomeres (flow FISH). Nat Protoc 1: 2365-2376.
62. Lopez-Verges S, Milush JM, Pandey S, York VA, Arakawa-Hoyt J, et al. (2010) CD57 defines a functionally distinct population of mature NK cells in the human CD56dimCD16+ NK-cell subset. Blood 116: 3865-3874.
63. Baerlocher GM, Lansdorp PM, (2003) Telomere length measurements in leukocyte subsets by automated multicolor flow-FISH. Cytometry A 55: 1-6.
64. Chambers JM, Hastie TJ, (1992) Statistical Models in S. Pacific Grove, CA: Wadsworth & Brooks/Cole.