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Expert Review of Gastroenterology & Hepatology Volume 7, 2013 - Issue 8
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Reviews

Telomeres and telomere dynamics: relevance to cancers of the GI tract

Nivedita BasuDepartment of Medicine, Division of Gastroenterology and Hepatology, Mayo Clinic, 200 First Street SW, Rochester, MN 55905, USA
,
Halcyon G SkinnerDepartment of Population Health Sciences, School of Medicine and Public Health, University of Wisconsin, Madison, WI 53726, USA;Department of Biostatistics and Medical Informatics, School of Medicine and Public Health, University of Wisconsin, Madison, WI 53726, USA
,
Kristin LitzelmanDepartment of Population Health Sciences, School of Medicine and Public Health, University of Wisconsin, Madison, WI 53726, USA;Department of Biostatistics and Medical Informatics, School of Medicine and Public Health, University of Wisconsin, Madison, WI 53726, USA
,
Russell VanderboomDepartment of Medicine, Division of Gastroenterology and Hepatology, Mayo Clinic, 200 First Street SW, Rochester, MN 55905, USA
,
Esha BaichooDepartment of Medicine, Division of Gastroenterology and Hepatology, Mayo Clinic, 200 First Street SW, Rochester, MN 55905, USA
&
Lisa A BoardmanDepartment of Medicine, Division of Gastroenterology and Hepatology, Mayo Clinic, 200 First Street SW, Rochester, MN 55905, USACorrespondence[email protected]
Pages 733-748 | Published online: 10 Jan 2014

References

  • Harley CB, Futcher AB, Greider CW. Telomeres shorten during ageing of human fibroblasts. Nature 345(6274), 458–460 (1990).
  • Cawthon R, Smith K, O'Brien E, Sivatchenko A, Kerber R. Association between telomere length in blood and mortality in people aged 60 years or older. Lancet 361, 393–395 (2003).
  • Wentzensen IM, Mirabello L, Pfeiffer RM, Savage SA. The association of telomere length and cancer: a meta-analysis. Cancer Epidemiol. Biomarkers Prev. 20(6), 1238–1250 (2011).
  • Ma H, Zhou Z, Wei S et al. Shortened telomere length is associated with increased risk of cancer: a meta-analysis. PLoS ONE 6(6), e20466 (2011).
  • Greider CW, Blackburn EH. Telomeres, telomerase and cancer. Sci. Am. 274(2), 92–97 (1996).
  • DePinho RA. The age of cancer. Nature 408(6809), 248–254 (2000).
  • Butler RN, Sprott R, Warner H et al. Biomarkers of aging: from primitive organisms to humans. J. Gerontol. A Biol. Sci. Med. Sci. 59(6), B560–567 (2004).
  • Johnson TE. Recent results: biomarkers of aging. Exp. Gerontol. 41(12), 1243–1246 (2006).
  • Ingram DK, Nakamura E, Smucny D, Roth GS, Lane MA. Strategy for identifying biomarkers of aging in long-lived species. Exp. Gerontol. 36(7), 1025–1034 (2001).
  • Skinner HG, Gangnon R, Boardman LA. Using biomarkers of aging to identify modifiable mechanisms underlying age-related risk for cancer. WMJ 108(5), 280–281 (2009).
  • Sahin E, DePinho RA. Axis of ageing: telomeres, p53 and mitochondria. Nat. Rev. Mol. Cell Biol. 13(6), 397–404 (2012).
  • Kimura M, Stone RC, Hunt SC et al. Measurement of telomere length by the Southern blot analysis of terminal restriction fragment lengths. Nat. Protoc. 5(9), 1596–1607 (2010).
  • Cawthon RM. Telomere measurement by quantitative PCR. Nucleic Acids Res. 30(10), e47 (2002).
  • Baerlocher GM, Lansdorp PM. Telomere length measurements using fluorescence in situ hybridization and flow cytometry. Methods Cell Biol. 75, 719–750 (2004).
  • Martens UM, Zijlmans JM, Poon SS et al. Short telomeres on human chromosome 17p. Nat. Genet. 18(1), 76–80 (1998).
  • Poon SS, Lansdorp PM. Quantitative fluorescence in situ hybridization (Q-FISH). Curr. Protoc. Cell Biol. Chapter 18, Unit 18.4 (2001).
  • Baird DM, Rowson J, Wynford-Thomas D, Kipling D. Extensive allelic variation and ultrashort telomeres in senescent human cells. Nat. Genet. 33(2), 203–207 (2003).
  • Bendix L, Horn PB, Jensen UB, Rubelj I, Kolvraa S. The load of short telomeres, estimated by a new method, Universal STELA , correlates with number of senescent cells. Aging Cell 9(3), 383–397 (2010).
  • O'Callaghan NJ, Fenech M. A quantitative PCR method for measuring absolute telomere length. Biol. Proc. Online 13, 3 (2011).
  • Aviv A, Hunt SC, Lin J, Cao X, Kimura M, Blackburn E. Impartial comparative analysis of measurement of leukocyte telomere length/DNA content by Southern blots and qPCR. Nucleic Acids Res. 39(20), e134 (2011).
  • Olsen MT, Berube M, Robbins J, Palsboll PJ. Empirical evaluation of humpback whale telomere length estimates; quality control and factors causing variability in the singleplex and multiplex qPCR methods. BMC Genet. 13, 77 (2012).
  • Puterman E, Lin J, Blackburn E, O'Donovan A, Adler N, Epel E. The power of exercise: buffering the effect of chronic stress on telomere length. PLoS ONE 5(5), e10837 (2010).
  • Parks CG, Miller DB, McCanlies EC et al. Telomere length, current perceived stress, and urinary stress hormones in women. Cancer Epidemiol. Biomarkers Prev. 18(2), 551–560 (2009).
  • Epel ES, Blackburn EH, Lin J et al. Accelerated telomere shortening in response to life stress. Proc. Natl Acad. Sci. USA 101(49), 17312–17315 (2004).
  • Daubenmier J, Lin J, Blackburn E et al. Changes in stress, eating, and metabolic factors are related to changes in telomerase activity in a randomized mindfulness intervention pilot study. Psychoneuroendocrinology 37(7), 917–928 (2012).
  • Humphreys J, Epel ES, Cooper BA, Lin J, Blackburn EH, Lee KA. Telomere shortening in formerly abused and never abused women. Biol. Res. Nurs. 14(2), 115–123 (2012).
  • Shalev I, Moffitt TE, Sugden K et al. Exposure to violence during childhood is associated with telomere erosion from 5 to 10 years of age: a longitudinal study. Mol. Psychiatry 18(5), 576–581 (2013).
  • Surtees PG, Wainwright NW, Pooley KA et al. Life stress, emotional health, and mean telomere length in the European Prospective Investigation into Cancer (EPIC)-Norfolk population study. J. Gerontol. A Biol. Sci. Med. Sci. 66(11), 1152–1162 (2011).
  • Needham BL, Adler N, Gregorich S et al. Socioeconomic status, health behavior, and leukocyte telomere length in the National Health and Nutrition Examination Survey, 1999-2002. Soc. Sci. Med. 85, 1–8 (2013).
  • Cherkas LF, Aviv A, Valdes AM et al. The effects of social status on biological aging as measured by white-blood-cell telomere length. Aging Cell 5(5), 361–365 (2006).
  • Carroll JE, Diez-Roux AV, Adler NE, Seeman TE. Socioeconomic factors and leukocyte telomere length in a multi-ethnic sample: findings from the multi-ethnic study of atherosclerosis (MESA). Brain Behav. Immun. 28, 108–114 (2013).
  • Robertson T, Batty GD, Der G, Fenton C, Shiels PG, Benzeval M. Is socioeconomic status associated with biological aging as measured by telomere length? Epidemiol. Rev. ( doi:10.1093/epirev/mxs001) (2012) ( Epub ahead of print).
  • Theall KP, Brett ZH, Shirtcliff EA, Dunn EC, Drury SS. Neighborhood disorder and telomeres: connecting children's exposure to community level stress and cellular response. Soc. Sci. Med. 85, 50–58 (2013).
  • Carroll JE, Diez Roux AV, Fitzpatrick AL, Seeman T. Low social support is associated with shorter leukocyte telomere length in late life: multi-ethnic study of atherosclerosis. Psychosom. Med. 75(2), 171–177 (2013).
  • Lin J, Epel E, Blackburn E. Telomeres and lifestyle factors: roles in cellular aging. Mutat. Res. 730(1–2), 85–89 (2012).
  • von Zglinicki T. Oxidative stress shortens telomeres. Trends Biochem. Sci. 27(7), 339–344 (2002).
  • Choi J, Fauce SR, Effros RB. Reduced telomerase activity in human T lymphocytes exposed to cortisol. Brain Behav. Immun. 22(4), 600–605 (2008).
  • Tomiyama AJ, O'Donovan A, Lin J et al. Does cellular aging relate to patterns of allostasis? An examination of basal and stress reactive HPA axis activity and telomere length. Physiol. Behav. 106(1), 40–45 (2012).
  • Paul L. Diet, nutrition and telomere length. J. Nutr. Biochem. 22(10), 895–901 (2011).
  • Du M, Prescott J, Kraft P et al. Physical activity, sedentary behavior, and leukocyte telomere length in women. Am. J. Epidemiol. 175(5), 414–422 (2012).
  • Savela S, Saijonmaa O, Strandberg TE et al. Physical activity in midlife and telomere length measured in old age. Exp. Gerontol. 48(1), 81–84 (2013).
  • Jackowska M, Hamer M, Carvalho LA, Erusalimsky JD, Butcher L, Steptoe A. Short sleep duration is associated with shorter telomere length in healthy men: findings from the Whitehall II cohort study. PLoS ONE 7(10), e47292 (2012).
  • Prather AA, Puterman E, Lin J et al. Shorter leukocyte telomere length in midlife women with poor sleep quality. J. Aging Res. 2011, 721390 (2011).
  • Valdes AM, Andrew T, Gardner JP et al. Obesity, cigarette smoking, and telomere length in women. Lancet 366(9486), 662–664 (2005).
  • Mirabello L, Huang WY, Wong JY et al. The association between leukocyte telomere length and cigarette smoking, dietary and physical variables, and risk of prostate cancer. Aging Cell 8(4), 405–413 (2009).
  • Sun Q, Shi L, Prescott J et al. Healthy lifestyle and leukocyte telomere length in U.S. women. PLoS ONE 7(5), e38374 (2012).
  • Puterman E, Epel ES, Lin J et al. Multisystem resiliency moderates the major depression-Telomere length association: Findings from the Heart and Soul Study. Brain Behav. Immun. 33, 65–73 (2013).
  • Ornish D, Lin J, Daubenmier J et al. Increased telomerase activity and comprehensive lifestyle changes: a pilot study. Lancet Oncol. 9(11), 1048–1057 (2008).
  • Lavretsky H, Epel ES, Siddarth P et al. A pilot study of yogic meditation for family dementia caregivers with depressive symptoms: effects on mental health, cognition, and telomerase activity. Int. J. Geriatr. Psychiatry 28(1), 57–65 (2013).
  • Jacobs TL, Epel ES, Lin J et al. Intensive meditation training, immune cell telomerase activity, and psychological mediators. Psychoneuroendocrinology 36(5), 664–681 (2011).
  • Hoge EA, Chen MM, Orr E et al. Loving-Kindness Meditation practice associated with longer telomeres in women. Brain Behav. Immun. 32, 159–163 (2013).
  • Bhasin MK, Dusek JA, Chang BH et al. Relaxation response induces temporal transcriptome changes in energy metabolism, insulin secretion and inflammatory pathways. PLoS ONE 8(5), e62817 (2013).
  • Epel E. How "reversible" is telomeric aging? Cancer Prev. Res. (Phila.) 5(10), 1163–1168 (2012).
  • Biegler KA, Anderson AK, Wenzel LB, Osann K, Nelson EL. Longitudinal change in telomere length and the chronic stress response in a randomized pilot biobehavioral clinical study: implications for cancer prevention. Cancer Prev. Res. (Phila.) 5(10), 1173–1182 (2012).
  • Olivieri F, Mazzanti I, Abbatecola AM et al. Telomere/Telomerase system: a new target of statins pleiotropic effect? Curr. Vasc. Pharmacol. 10(2), 216–224 (2012).
  • Boccardi V, Barbieri M, Rizzo MR et al. A new pleiotropic effect of statins in elderly: modulation of telomerase activity. FASEB J. 27(9), 3879–3885 (2013).
  • Bellon M, Nicot C. Regulation of telomerase and telomeres: human tumor viruses take control. J. Natl Cancer Inst. 100(2), 98–108 (2008).
  • Deng Z, Wang Z, Lieberman PM. Telomeres and viruses: common themes of genome maintenance. Front. Oncol. 2, 201 (2012).
  • Arbuckle JH, Medveczky PG. The molecular biology of human herpesvirus-6 latency and telomere integration. Microbes Infect. 13(8–9), 731–741 (2011).
  • Arbuckle JH, Medveczky MM, Luka J et al. The latent human herpesvirus-6A genome specifically integrates in telomeres of human chromosomes in vivo and in vitro. Proc. Natl Acad. Sci. USA 107(12), 5563–5568 (2010).
  • Young LS, Murray PG. Epstein-Barr virus and oncogenesis: from latent genes to tumours. Oncogene 22(33), 5108–5121 (2003).
  • Silva-Sousa R, Lopez-Panads E, Casacuberta E. Drosophila telomeres: an example of co-evolution with transposable elements. Genome Dyn. 7, 46–67 (2012).
  • Terrin L, Dal Col J, Rampazzo E et al. Latent membrane protein 1 of Epstein-Barr virus activates the hTERT promoter and enhances telomerase activity in B lymphocytes. J. Virol. 82(20), 10175–10187 (2008).
  • Murnane JP. Telomere dysfunction and chromosome instability. Mutat. Res. 730(1–2), 28–36 (2012).
  • Kaufer BB, Arndt S, Trapp S, Osterrieder N, Jarosinski KW. Herpesvirus telomerase RNA (vTR) with a mutated template sequence abrogates herpesvirus-induced lymphomagenesis. PLoS Pathog. 7(10), e1002333 (2011).
  • Block TM, Mehta AS, Fimmel CJ, Jordan R. Molecular viral oncology of hepatocellular carcinoma. Oncogene 22(33), 5093–5107 (2003).
  • Zhu Z, Wilson AT, Gopalakrishna K, Brown KE, Luxon BA, Schmidt WN. Hepatitis C virus core protein enhances Telomerase activity in Huh7 cells. J. Med. Virol. 82(2), 239–248 (2010).
  • Lee YH, Oh BK, Yoo JE et al. Chromosomal instability, telomere shortening, and inactivation of p21(WAF1/CIP1) in dysplastic nodules of hepatitis B virus-associated multistep hepatocarcinogenesis. Mod. Pathol. 22(8), 1121–1131 (2009).
  • Zhong YH, Liao ZK, Zhou FX et al. Telomere length inversely correlates with radiosensitivity in human carcinoma cells with the same tissue background. Biochem. Biophys. Res. Commun. 367(1), 84–89 (2008).
  • Wu AH, Yu MC, Mack TM. Smoking, alcohol use, dietary factors and risk of small intestinal adenocarcinoma. Int. J. Cancer 70(5), 512–517 (1997).
  • McGrath M, Wong JY, Michaud D, Hunter DJ, De Vivo I. Telomere length, cigarette smoking, and bladder cancer risk in men and women. Cancer Epidemiol. Biomarkers Prev. 16(4), 815–819 (2007).
  • Broberg K, Bjork J, Paulsson K, Hoglund M, Albin M. Constitutional short telomeres are strong genetic susceptibility markers for bladder cancer. Carcinogenesis 26(7), 1263–1271 (2005).
  • Shao L, Wood CG, Zhang D et al. Telomere dysfunction in peripheral lymphocytes as a potential predisposition factor for renal cancer. J. Urol. 178(4 Pt 1), 1492–1496 (2007).
  • Jang JS, Choi YY, Lee WK et al. Telomere length and the risk of lung cancer. Cancer Sci. 99(7), 1385–1389 (2008).
  • Risques RA, Vaughan TL, Li X et al. Leukocyte telomere length predicts cancer risk in Barrett's esophagus. Cancer Epidemiol. Biomarkers Prev. 16(12), 2649–2655 (2007).
  • Van Ziffle JA, Baerlocher GM, Lansdorp PM. Telomere length in subpopulations of human hematopoietic cells. Stem Cells 21(6), 654–660 (2003).
  • Baerlocher GM, Lansdorp PM. Telomere length measurements in leukocyte subsets by automated multicolor flow-FISH. Cytometry A 55(1), 1–6 (2003).
  • Cunningham JM, Johnson RA, Litzelman KR et al. Telomere length varies by DNA extraction method: implications for epidemiologic research. Cancer Epidemiol. Biomarkers Prev. ( doi:10.1158/1055-9965.EPI-13-0409) (2013) ( Epub ahead of print).
  • Chen CH, Chen RJ. Prevalence of telomerase activity in human cancer. J Formos. Med. Assoc. 110(5), 275–289 (2011).
  • Myung SJ, Yang SK, Chang HS et al. Clinical usefulness of telomerase for the detection of colon cancer in ulcerative colitis patients. J. Gastroenterol. Hepatol. 20(10), 1578–1583 (2005).
  • Bronner MP, O'Sullivan JN, Rabinovitch PS et al. Genomic biomarkers to improve ulcerative colitis neoplasia surveillance. Am. J. Pathol. 173(6), 1853–1860 (2008).
  • Garcia-Aranda C, de Juan C, Diaz-Lopez A et al. Correlations of telomere length, telomerase activity, and telomeric-repeat binding factor 1 expression in colorectal carcinoma. Cancer 106(3), 541–551 (2006).
  • Gertler R, Rosenberg R, Stricker D et al. Telomere length and human telomerase reverse transcriptase expression as markers for progression and prognosis of colorectal carcinoma. J. Clin. Oncol. 22(10), 1807–1814 (2004).
  • Kawanishi-Tabata R, Lopez F, Fratantonio S et al. Telomerase activity in stage II colorectal carcinoma. Cancer 95(9), 1834–1839 (2002).
  • Bertorelle R, Briarava M, Rampazzo E et al. Telomerase is an independent prognostic marker of overall survival in patients with colorectal cancer. Br. J. Cancer 108(2), 278–284 (2013).
  • Bryan TM, Englezou A, Gupta J, Bacchetti S, Reddel RR. Telomere elongation in immortal human cells without detectable telomerase activity. EMBO J. 14(17), 4240–4248 (1995).
  • Xing J, Ajani JA, Chen M et al. Constitutive short telomere length of chromosome 17p and 12q but not 11q and 2p is associated with an increased risk for esophageal cancer. Cancer Prev. Res. (Phila.) 2(5), 459–465 (2009).
  • Shi J, Sun F, Peng L et al. Leukocyte telomere length-related genetic variants in 1p34.2 and 14q21 loci contribute to the risk of esophageal squamous cell carcinoma. Int. J. Cancer 132(12), 2799–2807 (2013).
  • Takubo K, Fujita M, Izumiyama N et al. Q-FISH analysis of telomere and chromosome instability in the oesophagus with and without squamous cell carcinoma in situ. J. Pathol. 221(2), 201–209 (2010).
  • Aida J, Izumo T, Shimomura N et al. Telomere lengths in the oral epithelia with and without carcinoma. Eur. J. Cancer 46(2), 430–438 (2010).
  • Yu HP, Xu SQ, Lu WH et al. Telomerase activity and expression of telomerase genes in squamous dysplasia and squamous cell carcinoma of the esophagus. J. Surg. Oncol. 86(2), 99–104 (2004).
  • Hsu CP, Lee LW, Shai SE, Chen CY. Clinical significance of telomerase and its associate genes expression in the maintenance of telomere length in squamous cell carcinoma of the esophagus. World J. Gastroenterol. 11(44), 6941–6947 (2005).
  • Syrjanen K, Syrjanen S. Detection of human papillomavirus in esophageal papillomas: systematic review and meta-analysis. APMIS 121(5), 363–374 (2013).
  • Asai A, Kiyozuka Y, Yoshida R, Fujii T, Hioki K, Tsubura A. Telomere length, telomerase activity and telomerase RNA expression in human esophageal cancer cells: correlation with cell proliferation, differentiation and chemosensitivity to anticancer drugs. Anticancer Res. 18(3A), 1465–1472 (1998).
  • Gallo A, Cha C. Updates on esophageal and gastric cancers. World J. Gastroenterol. 12(20), 3237–3242 (2006).
  • Sharma P, Sidorenko EI. Are screening and surveillance for Barrett's oesophagus really worthwhile? Gut 54( Suppl. 54), i27–32 (2005).
  • Shammas MA, Koley H, Beer DG, Li C, Goyal RK, Munshi NC. Growth arrest, apoptosis, and telomere shortening of Barrett's-associated adenocarcinoma cells by a telomerase inhibitor. Gastroenterology 126(5), 1337–1346 (2004).
  • Hou L, Savage SA, Blaser MJ et al. Telomere length in peripheral leukocyte DNA and gastric cancer risk. Cancer Epidemiol. Biomarkers Prev. 18(11), 3103–3109 (2009).
  • Liu X, Bao G, Huo T, Wang Z, He X, Dong G. Constitutive telomere length and gastric cancer risk: case-control analysis in Chinese Han population. Cancer Sci. 100(7), 1300–1305 (2009).
  • Leung SY, Yuen ST, Chung LP, Chu KM, Chan AS, Ho JC. hMLH1 promoter methylation and lack of hMLH1 expression in sporadic gastric carcinomas with high-frequency microsatellite instability. Cancer Res. 59(1), 159–164 (1999).
  • An C, Choi IS, Yao JC et al. Prognostic significance of CpG island methylator phenotype and microsatellite instability in gastric carcinoma. Clin. Cancer Res. 11(2 Pt 1), 656–663 (2005).
  • Bevilacqua RA, Simpson AJ. Methylation of the hMLH1 promoter but no hMLH1 mutations in sporadic gastric carcinomas with high-level microsatellite instability. Int. J. Cancer 87(2), 200–203 (2000).
  • Lindor NM, Rabe K, Petersen GM et al. Lower cancer incidence in Amsterdam-I criteria families without mismatch repair deficiency: familial colorectal cancer type X. JAMA 293(16), 1979–1985 (2005).
  • Cunningham JM, Kim CY, Christensen ER et al. The frequency of hereditary defective mismatch repair in a prospective series of unselected colorectal carcinomas. Am. J. Hum. Genet. 69(4), 780–790 (2001).
  • Omori Y, Nakayama F, Li D et al. Alternative lengthening of telomeres frequently occurs in mismatch repair system-deficient gastric carcinoma. Cancer Sci. 100(3), 413–418 (2009).
  • Chin L, Artandi SE, Shen Q et al. p53 deficiency rescues the adverse effects of telomere loss and cooperates with telomere dysfunction to accelerate carcinogenesis. Cell 97(4), 527–538 (1999).
  • Mu Y, Zhang Q, Mei L, Liu X, Yang W, Yu J. Telomere shortening occurs early during gastrocarcinogenesis. Med. Oncol. 29(2), 893–898 (2012).
  • Aslan R, Bektas A, Bedir A et al. Helicobacter pylori eradication increases telomere length in gastric mucosa. Hepatogastroenterology 60(123) (2012).
  • Henson JD, Reddel RR. Assaying and investigating Alternative Lengthening of Telomeres activity in human cells and cancers. FEBS Lett. 584(17), 3800–3811 (2010).
  • Skinner HG, Gangnon RE, Litzelman K et al. Telomere length and pancreatic cancer: a case-control study. Cancer Epidemiol. Biomarkers Prev. 21(11), 2095–2100 (2012).
  • Lynch SM, Major JM, Cawthon R et al. A prospective analysis of telomere length and pancreatic cancer in the Alpha-Tocopherol B eta-Carotene cancer prevention (ATBC) study. Int. J. Cancer ( doi:10.1002/ijc.28272) (2013) ( Epub ahead of print).
  • Baird DM. Variation at the TERT locus and predisposition for cancer. Expert Rev. Mol. Med. 12, e16 (2010).
  • van Heek NT, Meeker AK, Kern SE et al. Telomere shortening is nearly universal in pancreatic intraepithelial neoplasia. Am. J. Pathol. 161(5), 1541–1547 (2002).
  • Gisselsson D, Jonson T, Petersen A et al. Telomere dysfunction triggers extensive DNA fragmentation and evolution of complex chromosome abnormalities in human malignant tumors. Proc. Natl Acad. Sci. USA 98(22), 12683–12688 (2001).
  • Hashimoto Y, Murakami Y, Uemura K et al. Telomere shortening and telomerase expression during multistage carcinogenesis of intraductal papillary mucinous neoplasms of the pancreas. J. Gastrointest. Surg. 12(1), 17–28; discussion 28–19 (2008).
  • Liu J, Yang Y, Zhang H et al. Longer leukocyte telomere length predicts increased risk of hepatitis B virus-related hepatocellular carcinoma: a case-control analysis. Cancer 117(18), 4247–4256 (2011).
  • Oh BK, Um TH, Choi GH, Park YN. Frequent changes in subtelomeric DNA methylation patterns and its relevance to telomere regulation during human hepatocarcinogenesis. Int. J. Cancer 128(4), 857–868 (2011).
  • Fu X, Wan S, Hann HW et al. Relative telomere length: a novel non-invasive biomarker for the risk of non-cirrhotic hepatocellular carcinoma in patients with chronic hepatitis B infection. Eur. J. Cancer 48(7), 1014–1022 (2012).
  • Liu HQ, An JZ, Liu J et al. Leukocyte telomere length predicts overall survival in hepatocellular carcinoma treated with transarterial chemoembolization. Carcinogenesis 33(5), 1040–1045 (2012).
  • Oh BK, Kim H, Park YN et al. High telomerase activity and long telomeres in advanced hepatocellular carcinomas with poor prognosis. Lab. Invest. 88(2), 144–152 (2008).
  • de Groen PC, Gores GJ, LaRusso NF, Gunderson LL, Nagorney DM. Biliary tract cancers. N. Engl. J. Med. 341(18), 1368–1378 (1999).
  • Duarte I, Llanos O, Domke H, Harz C, Valdivieso V. Metaplasia and precursor lesions of gallbladder carcinoma. Frequency, distribution, and probability of detection in routine histologic samples. Cancer 72(6), 1878–1884 (1993).
  • Hansel DE, Meeker AK, Hicks J et al. Telomere length variation in biliary tract metaplasia, dysplasia, and carcinoma. Mod. Pathol. 19(6), 772–779 (2006).
  • Lazcano-Ponce EC, Miquel JF, Munoz N et al. Epidemiology and molecular pathology of gallbladder cancer. CA Cancer J. Clin. 51(6), 349–364 (2001).
  • Watanapa P. Cholangiocarcinoma in patients with opisthorchiasis. Br. J. Surg. 83(8), 1062–1064 (1996).
  • Shin HR, Lee CU, Park HJ et al. Hepatitis B and C virus, Clonorchis sinensis for the risk of liver cancer: a case-control study in Pusan, Korea. Int. J. Epidemiol. 25(5), 933–940 (1996).
  • Udomchaiprasertkul W, Narong S, Kongsema M, Leelawat K. Detection of hTERT mRNA in gastrointestinal tract cancer specimens. Southeast Asian J. Trop. Med. Public Health 39(2), 324–327 (2008).
  • Siegel R, Naishadham D, Jemal A. Cancer statistics, 2013. CA Cancer J. Clin. 63(1), 11–30 (2013).
  • Howe JR, Karnell LH, Menck HR, Scott-Conner C. The American College of Surgeons Commission on Cancer and the American Cancer Society. Adenocarcinoma of the small bowel: review of the National Cancer Data Base, 1985–1995. Cancer 86(12), 2693–2706 (1999).
  • Scelo G, Boffetta P, Hemminki K et al. Associations between small intestine cancer and other primary cancers: an international population-based study. Int. J. Cancer 118(1), 189–196 (2006).
  • Zar N, Garmo H, Holmberg L, Hellman P. Risk of second primary malignancies and causes of death in patients with adenocarcinoma and carcinoid of the small intestine. Eur. J. Cancer 44(5), 718–725 (2008).
  • Warth A, Kloor M, Schirmacher P, Blaker H. Genetics and epigenetics of small bowel adenocarcinoma: the interactions of CIN, MSI, and CIMP. Mod. Pathol. 24(4), 564–570 (2011).
  • Abrahams NA, Halverson A, Fazio VW, Rybicki LA, Goldblum JR. Adenocarcinoma of the small bowel: a study of 37 cases with emphasis on histologic prognostic factors. Dis. Colon Rectum 45(11), 1496–1502 (2002).
  • Rodriguez-Bigas MA, Vasen HF, Lynch HT et al. Characteristics of small bowel carcinoma in hereditary nonpolyposis colorectal carcinoma. International Collaborative Group on HNPCC. Cancer 83(2), 240–244 (1998).
  • Giardiello FM, Brensinger JD, Tersmette AC et al. Very high risk of cancer in familial Peutz-Jeghers syndrome. Gastroenterology 119(6), 1447–1453 (2000).
  • Neugut AI, Jacobson JS, Suh S, Mukherjee R, Arber N. The epidemiology of cancer of the small bowel. Cancer Epidemiol. Biomarkers Prev. 7(3), 243–251 (1998).
  • Green PH, Cellier C. Celiac disease. N. Engl. J. Med. 357(17), 1731–1743 (2007).
  • Chow WH, Linet MS, McLaughlin JK, Hsing AW, Chien HT, Blot WJ. Risk factors for small intestine cancer. Cancer Causes Control 4(2), 163–169 (1993).
  • Balcom JHt, Keck T, Warshaw AL, Antoniu B, Graeme-Cook F, Fernandez-del Castillo C. Telomerase activity in periampullary tumors correlates with aggressive malignancy. Ann. Surg. 234(3), 344–350; discussion 350–341 (2001).
  • Riegert-Johnson DL, Boardman LA, Crook JE, Thomas CS, Johnson RA, Roberts ME. Shorter peripheral blood telomeres are a potential biomarker for patients with advanced colorectal adenomas. Int. J. Biol. Markers 27(4), e375–380 (2012).
  • Pooley KA, Sandhu MS, Tyrer J et al. Telomere length in prospective and retrospective cancer case-control studies. Cancer Res. 70(8), 3170–3176 (2010).
  • Zee RYL, Castonguay AJ, Barton NS, Buring JE. Mean telomere length and risk of incident colorectal carcinoma: a prospective, nested case-control approach. Cancer Epidemiol. Biomarkers Prev. 18(8), 2280–2282 (2009).
  • Lee IM, Lin J, Castonguay AJ, Barton NS, Buring JE, Zee RY. Mean leukocyte telomere length and risk of incident colorectal carcinoma in women: a prospective, nested case-control study. Clin. Chem. Lab. Med. 48(2), 259–262 (2010).
  • Jones AM, Beggs AD, Carvajal-Carmona L et al. TERC polymorphisms are associated both with susceptibility to colorectal cancer and with longer telomeres. Gut 61(2), 248–254 (2012).
  • Engelhardt M, Drullinsky P, Guillem J, Moore MA. Telomerase and telomere length in the development and progression of premalignant lesions to colorectal cancer. Clin. Cancer Res. 3(11), 1931–1941 (1997).
  • Raynaud CM, Jang SJ, Nuciforo P et al. Telomere shortening is correlated with the DNA damage response and telomeric protein down-regulation in colorectal preneoplastic lesions. Ann. Oncol. 19(11), 1875–1881 (2008).
  • O'Callaghan NJ, Clifton PM, Noakes M, Fenech M. Weight loss in obese men is associated with increased telomere length and decreased abasic sites in rectal mucosa. Rejuvenation Res. 12(3), 169–176 (2009).
  • O'Sullivan J, Risques RA, Mandelson MT et al. Telomere length in the colon declines with age: a relation to colorectal cancer? Cancer Epidemiol. Biomarkers Prev. 15(3), 573–577 (2006).
  • Risques RA, Lai LA, Brentnall TA et al. Ulcerative colitis is a disease of accelerated colon aging: evidence from telomere attrition and DNA damage. Gastroenterology 135(2), 410–418 (2008).
  • Boldrini L, Faviana P, Gisfredi S et al. Evaluation of telomerase in the development and progression of colon cancer. Int. J. Mol. Med. 10(5), 589–592 (2002).
  • Ghori A, Usselmann B, Ferryman S, Morris A, Fraser I. Telomerase expression of malignant epithelial cells correlates with Dukes' stage in colorectal cancer. Colorectal Dis. 4(6), 441–446 (2002).
  • Malaska J, Kunicka Z, Borsky M et al. Telomerase as a diagnostic and predictive marker in colorectal carcinoma. Neoplasma 51(2), 90–96 (2004).
  • Okayasu I, Mitomi H, Yamashita K et al. Telomerase activity significantly correlates with cell differentiation, proliferation and lymph node metastasis in colorectal carcinomas. J. Cancer Res. Clin. Oncol. 124(8), 444–449 (1998).
  • Sanz-Casla MT, Vidaurreta M, Sanchez-Rueda D, Maestro ML, Arroyo M, Cerdan FJ. Telomerase activity as a prognostic factor in colorectal cancer. Onkologie 28(11), 553–557 (2005).
  • Frias C, Moran A, de Juan C et al. Telomere function in colorectal cancer. World J. Gastrointest. Oncol. 1(1), 3–11 (2009).
  • Orchard M, Roman A, Parvaiz AC. Anal intraepithelial neoplasia - Is treatment better than observation? Int. J. Surg. 11(6), 438–441 (2013).
  • Pineda CE, Berry JM, Jay N, Palefsky JM, Welton ML. High-resolution anoscopy targeted surgical destruction of anal high-grade squamous intraepithelial lesions: a ten-year experience. Dis. Colon Rectum 51(6), 829–835; discussion 835–827 (2008).
  • Frisch M, Fenger C, van den Brule AJ et al. Variants of squamous cell carcinoma of the anal canal and perianal skin and their relation to human papillomaviruses. Cancer Res. 59(3), 753–757 (1999).
  • Melbye M, Frisch M. The role of human papillomaviruses in anogenital cancers. Semin. Cancer Biol. 8(4), 307–313 (1998).
  • Nelson RA, Levine AM, Bernstein L, Smith DD, Lai LL. Changing patterns of anal canal carcinoma in the United States. J. Clin. Oncol. 31(12), 1569–1575 (2013).
  • Ajani JA, Wang X, Izzo JG et al. Molecular biomarkers correlate with disease-free survival in patients with anal canal carcinoma treated with chemoradiation. Dig. Dis. Sci. 55(4), 1098–1105 (2010).
  • Zaffaroni N, Villa R, Pastorino U et al. Lack of telomerase activity in lung carcinoids is dependent on human telomerase reverse transcriptase transcription and alternative splicing and is associated with long telomeres. Clin. Cancer Res. 11(8), 2832–2839 (2005).
  • Tang SJ, Dumot JA, Wang L et al. Telomerase activity in pancreatic endocrine tumors. Am. J. Gastroenterol. 97(4), 1022–1030 (2002).
  • Aviv A, Valdes A, Gardner JP, Swaminathan R, Kimura M, Spector TD. Menopause modifies the association of leukocyte telomere length with insulin resistance and inflammation. J. Clin. Endocrinol. Metab. 91(2), 635–640 (2006).
  • Jeanclos E, Krolewski A, Skurnick J et al. Shortened telomere length in white blood cells of patients with IDDM. Diabetes 47(3), 482–486 (1998).
  • Gardner JP, Li S, Srinivasan SR et al. Rise in insulin resistance is associated with escalated telomere attrition. Circulation 111(17), 2171–2177 (2005).
  • Morlá M, Busquets X, Pons J, Sauleda J, MacNee W, Agusti AGN. Telomere shortening in smokers with and without COPD. Eur. Respir. J. 27(3), 525–528 (2006).
  • Graakjaer J, Bischoff C, Korsholm L et al. The pattern of chromosome-specific variations in telomere length in humans is determined by inherited, telomere-near factors and is maintained throughout life. Mech. Ageing Dev. 124(5), 629–640 (2003).
  • Munoz P, Blanco R, Blasco MA. Role of the TRF2 telomeric protein in cancer and ageing. Cell Cycle 5(7), 718–721 (2006).
  • Nakamura K, Furugori E, Esaki Y et al. Correlation of telomere lengths in normal and cancers tissue in the large bowel. Cancer Lett. 158(2), 179–184 (2000).
  • Plentz RR, Wiemann SU, Flemming P et al. Telomere shortening of epithelial cells characterises the adenoma-carcinoma transition of human colorectal cancer. Gut 52(9), 1304–1307 (2003).

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