Lead Exposure Induces Telomere Instability in Human Cells

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Pottier, Géraldine ^a   Viau, Muriel ^a   Ricoul, Michelle ^a   Shim, Grace ^a   Bellamy, Marion ^a   Cuceu, Corina ^a   Hempel, William M ^a   Sabatier, Laure ^a  

^a INSTITUT DE RADIOPROTECTION ET DE SÛRETÉ NUCLÉAIRE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

LEAD;

ARTICLE; CHROMOSOME ABERRATION; CHROMOSOME DAMAGE; CONTROLLED STUDY; DNA REPAIR; DNA STRAND; DOUBLE STRANDED DNA BREAK; HUMAN; HUMAN CELL; NEUROTOXICITY; TELOMERE; TELOMERE HOMEOSTASIS; TELOMERE REPLICATION; TELOMERE SHORTENING; ADVERSE EFFECTS; BLADDER TUMOR; CELL CULTURE; CHEMICALLY INDUCED; CHROMOSOMAL INSTABILITY; COMPLICATION; DRUG EFFECTS; ENVIRONMENTAL EXPOSURE; GENETICS; LEAD POISONING; LYMPHOCYTE; PATHOLOGY;

CELLS, CULTURED; CHROMOSOMAL INSTABILITY; ENVIRONMENTAL EXPOSURE; HUMANS; LEAD; LEAD POISONING; LYMPHOCYTES; TELOMERE; TELOMERE HOMEOSTASIS; URINARY BLADDER NEOPLASMS;

EID: 84879484599     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0067501     Document Type: Article

References (51)

1. Gilbert SG, Weiss B, (2006) A rationale for lowering the blood lead action level from 10 to 2 microg/dL. Neurotoxicology 27: 693-701.
2. Needleman H, (2004) Lead poisoning. Annu Rev Med 55: 209-222.
3. White LD, Cory-Slechta DA, Gilbert ME, Tiffany-Castiglioni E, Zawia NH, et al. (2007) New and evolving concepts in the neurotoxicology of lead. Toxicol Appl Pharmacol 225: 1-27.
4. Bellinger DC, Bellinger AM, (2006) Childhood lead poisoning: the torturous path from science to policy. J Clin Invest 116: 853-857.
5. Sanders T, Liu Y, Buchner V, Tchounwou PB, (2009) Neurotoxic effects and biomarkers of lead exposure: a review. Rev Environ Health 24: 15-45.
6. Brown MJ, Margolis S, (2012) Lead in drinking water and human blood lead levels in the United States. MMWR Surveill Summ 61: 1-9.
7. Silbergeld EK, (2003) Facilitative mechanisms of lead as a carcinogen. Mutat Res 533: 121-133.
8. Verstraeten SV, Aimo L, Oteiza PI, (2008) Aluminium and lead: molecular mechanisms of brain toxicity. Arch Toxicol 82: 789-802.
9. Garcia-Leston J, Mendez J, Pasaro E, Laffon B, (2010) Genotoxic effects of lead: an updated review. Environ Int 36: 623-636.
10. Gastaldo J, Viau M, Bencokova Z, Joubert A, Charvet AM, et al. (2007) Lead contamination results in late and slowly repairable DNA double-strand breaks and impacts upon the ATM-dependent signaling pathways. Toxicol Lett 173: 201-214.
11. Redon C, Pilch D, Rogakou E, Sedelnikova O, Newrock K, et al. (2002) Histone H2A variants H2AX and H2AZ. Curr Opin Genet Dev 12: 162-169.
12. 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.
13. Verdun RE, Karlseder J, (2007) Replication and protection of telomeres. Nature 447: 924-931.
14. Counter CM, Avilion AA, LeFeuvre CE, Stewart NG, Greider CW, et al. (1992) Telomere shortening associated with chromosome instability is arrested in immortal cells which express telomerase activity. EMBO J 11: 1921-1929.
15. Lo AW, Sabatier L, Fouladi B, Pottier G, Ricoul M, et al. (2002) DNA amplification by breakage/fusion/bridge cycles initiated by spontaneous telomere loss in a human cancer cell line. Neoplasia 4: 531-538.
16. Rothkamm K, Lobrich M, (2003) Evidence for a lack of DNA double-strand break repair in human cells exposed to very low x-ray doses. Proc Natl Acad Sci U S A 100: 5057-5062.
17. Ye J, Lenain C, Bauwens S, Rizzo A, Saint-Leger A, et al. (2010) TRF2 and apollo cooperate with topoisomerase 2alpha to protect human telomeres from replicative damage. Cell 142: 230-242.
18. Williams ES, Cornforth MN, Goodwin EH, Bailey SM, (2011) CO-FISH, COD-FISH, ReD-FISH, SKY-FISH. Methods Mol Biol 735: 113-124.
19. Takai H, Smogorzewska A, de Lange T, (2003) DNA damage foci at dysfunctional telomeres. Curr Biol 13: 1549-1556.
20. Nakamura AJ, Redon CE, Bonner WM, Sedelnikova OA, (2009) Telomere-dependent and telomere-independent origins of endogenous DNA damage in tumor cells. Aging (Albany NY) 1: 212-218.
21. Ayouaz A, Raynaud C, Heride C, Revaud D, Sabatier L, (2008) Telomeres: hallmarks of radiosensitivity. Biochimie 90: 60-72.
22. Magyar JS, Weng TC, Stern CM, Dye DF, Rous BW, et al. (2005) Reexamination of lead(II) coordination preferences in sulfur-rich sites: implications for a critical mechanism of lead poisoning. J Am Chem Soc 127: 9495-9505.
23. Maizels N, (2006) Dynamic roles for G4 DNA in the biology of eukaryotic cells. Nat Struct Mol Biol 13: 1055-1059.
24. London TB, Barber LJ, Mosedale G, Kelly GP, Balasubramanian S, et al. (2008) FANCJ is a structure-specific DNA helicase associated with the maintenance of genomic G/C tracts. J Biol Chem 283: 36132-36139.
25. Salvati E, Leonetti C, Rizzo A, Scarsella M, Mottolese M, et al. (2007) Telomere damage induced by the G-quadruplex ligand RHPS4 has an antitumor effect. J Clin Invest 117: 3236-3247.
26. Tahara H, Shin-Ya K, Seimiya H, Yamada H, Tsuruo T, et al. (2006) G-Quadruplex stabilization by telomestatin induces TRF2 protein dissociation from telomeres and anaphase bridge formation accompanied by loss of the 3′ telomeric overhang in cancer cells. Oncogene 25: 1955-1966.
27. Pennarun G, Granotier C, Gauthier LR, Gomez D, Hoffschir F, et al. (2005) Apoptosis related to telomere instability and cell cycle alterations in human glioma cells treated by new highly selective G-quadruplex ligands. Oncogene 24: 2917-2928.
28. Kotch FW, Fettinger JC, Davis JT, (2000) A lead-filled G-quadruplex: insight into the G-Quartet's selectivity for Pb(2+) over K(+). Org Lett 2: 3277-3280.
29. Li T, Wang E, Dong S, (2009) Potassium-lead-switched G-quadruplexes: a new class of DNA logic gates. J Am Chem Soc 131: 15082-15083.
30. Crabbe L, Verdun RE, Haggblom CI, Karlseder J, (2004) Defective telomere lagging strand synthesis in cells lacking WRN helicase activity. Science 306: 1951-1953.
31. Blasco MA, Lee HW, Hande MP, Samper E, Lansdorp PM, et al. (1997) Telomere shortening and tumor formation by mouse cells lacking telomerase RNA. Cell 91: 25-34.
32. Liu Y, Snow BE, Hande MP, Yeung D, Erdmann NJ, et al. (2000) The telomerase reverse transcriptase is limiting and necessary for telomerase function in vivo. Curr Biol 10: 1459-1462.
33. Lee HW, Blasco MA, Gottlieb GJ, Horner JW, 2nd, Greider CW, et al (1998) Essential role of mouse telomerase in highly proliferative organs. Nature 392: 569-574.
34. Hao LY, Armanios M, Strong MA, Karim B, Feldser DM, et al. (2005) Short telomeres, even in the presence of telomerase, limit tissue renewal capacity. Cell 123: 1121-1131.
35. Herrera E, Samper E, Blasco MA, (1999) Telomere shortening in mTR-/- embryos is associated with failure to close the neural tube. EMBO J 18: 1172-1181.
36. Ferron SR, Marques-Torrejon MA, Mira H, Flores I, Taylor K, et al. (2009) Telomere shortening in neural stem cells disrupts neuronal differentiation and neuritogenesis. J Neurosci 29: 14394-14407.
37. Jaskelioff M, Muller FL, Paik JH, Thomas E, Jiang S, et al. (2011) Telomerase reactivation reverses tissue degeneration in aged telomerase-deficient mice. Nature 469: 102-106.
38. Zhou QG, Hu Y, Wu DL, Zhu LJ, Chen C, et al. (2011) Hippocampal telomerase is involved in the modulation of depressive behaviors. J Neurosci 31: 12258-12269.
39. 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.
40. Okereke OI, Prescott J, Wong JY, Han J, Rexrode KM, et al. (2012) High phobic anxiety is related to lower leukocyte telomere length in women. PLoS One 7: e40516.
41. Canela A, Vera E, Klatt P, Blasco MA, (2007) High-throughput telomere length quantification by FISH and its application to human population studies. Proc Natl Acad Sci U S A 104: 5300-5305.
42. Wu Y, Liu Y, Ni N, Bao B, Zhang C, et al. (2012) High lead exposure is associated with telomere length shortening in Chinese battery manufacturing plant workers. Occup Environ Med 69: 557-563.
43. Fouladi B, Sabatier L, Miller D, Pottier G, Murnane JP, (2000) The relationship between spontaneous telomere loss and chromosome instability in a human tumor cell line. Neoplasia 2: 540-554.
44. Bai Y, Murnane JP, (2003) Telomere instability in a human tumor cell line expressing NBS1 with mutations at sites phosphorylated by ATM. Mol Cancer Res 1: 1058-1069.
45. Sabatier L, Ricoul M, Pottier G, Murnane JP, (2005) The loss of a single telomere can result in instability of multiple chromosomes in a human tumor cell line. Mol Cancer Res 3: 139-150.
46. Kulkarni A, Zschenker O, Reynolds G, Miller D, Murnane JP, (2010) Effect of telomere proximity on telomere position effect, chromosome healing, and sensitivity to DNA double-strand breaks in a human tumor cell line. Mol Cell Biol 30: 578-589.
47. Kato T, Irwin RJ Jr, Prout GR Jr, (1977) Cell cycles in two cell lines of human bladder carcinoma. Tohoku J Exp Med 121: 157-164.
48. O'Toole CM, Povey S, Hepburn P, Franks LM, (1983) Identity of some human bladder cancer cell lines. Nature 301: 429-430.
49. Leonhardt EA, Trinh M, Forrester HB, Johnson RT, Dewey WC, (1997) Comparisons of the frequencies and molecular spectra of HPRT mutants when human cancer cells were X-irradiated during G1 or S phase. Radiat Res 148: 548-560.
50. Dutrillaux B, Viegas Pequignot E, Aurias A, Prod'homme M, Sportes M, et al. (1981) Tentative estimate of the risk of chromosomal disease due to radiation-induced translocations in man. Mutat Res 82: 191-200.
51. 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.