Telomerase mutations in smokers with severe emphysema.

Mutations in the essential telomerase genes TERT and TR cause familial pulmonary fibrosis; however, in telomerase-null mice, short telomeres predispose to emphysema after chronic cigarette smoke exposure. Here, we tested whether telomerase mutations are a risk factor for human emphysema by examining their frequency in smokers with chronic obstructive pulmonary disease (COPD). Across two independent cohorts, we found 3 of 292 severe COPD cases carried deleterious mutations in TERT (1%). This prevalence is comparable to the frequency of alpha-1 antitrypsin deficiency documented in this population. The TERT mutations compromised telomerase catalytic activity, and mutation carriers had short telomeres. Telomerase mutation carriers with emphysema were predominantly female and had an increased incidence of pneumothorax. In families, emphysema showed an autosomal dominant inheritance pattern, along with pulmonary fibrosis and other telomere syndrome features, but manifested only in smokers. Our findings identify germline mutations in telomerase as a Mendelian risk factor for COPD susceptibility that clusters in autosomal dominant families with telomere-mediated disease including pulmonary fibrosis.

[1]  S. Boulton,et al.  RTEL1: functions of a disease-associated helicase. , 2014, Trends in cell biology.

[2]  P. Shah,et al.  Lung transplantation in telomerase mutation carriers with pulmonary fibrosis , 2014, European Respiratory Journal.

[3]  D. Sin,et al.  Longer Telomere Length in COPD Patients with α1-Antitrypsin Deficiency Independent of Lung Function , 2014, PloS one.

[4]  D. Valeyre,et al.  Is telomeropathy the explanation for combined pulmonary fibrosis and emphysema syndrome?: report of a family with TERT mutation. , 2014, American journal of respiratory and critical care medicine.

[5]  A. Auerbach,et al.  Telomere Phenotypes in Females with Heterozygous Mutations in the Dyskeratosis Congenita 1 (DKC1) Gene , 2013, Human mutation.

[6]  N. Laird,et al.  Heritability of chronic obstructive pulmonary disease and related phenotypes in smokers. , 2013, American journal of respiratory and critical care medicine.

[7]  A. Bertuch,et al.  A homozygous telomerase T-motif variant resulting in markedly reduced repeat addition processivity in siblings with Hoyeraal Hreidarsson syndrome. , 2013, Blood.

[8]  E. Montgomery,et al.  The gastrointestinal manifestations of telomere‐mediated disease , 2013, Aging cell.

[9]  M. Armanios Telomeres and age-related disease: how telomere biology informs clinical paradigms. , 2013, The Journal of clinical investigation.

[10]  B. Celli,et al.  Comorbidities and risk of mortality in patients with chronic obstructive pulmonary disease. , 2012, American journal of respiratory and critical care medicine.

[11]  E. Blackburn,et al.  The telomere syndromes , 2012, Nature Reviews Genetics.

[12]  M. Rieder,et al.  Exome sequencing of extreme phenotypes identifies DCTN4 as a modifier of chronic Pseudomonas aeruginosa infection in cystic fibrosis , 2012, Nature Genetics.

[13]  N. Laird,et al.  Exome Sequencing In Severe COPD Cases And Resistant Smoking Controls From COPDGene , 2012, ATS 2012.

[14]  Joshua D. Podlevsky,et al.  RNA/DNA hybrid binding affinity determines telomerase template‐translocation efficiency , 2012, The EMBO journal.

[15]  Jiaquan Xu,et al.  Deaths: final data for 2009. , 2011, National vital statistics reports : from the Centers for Disease Control and Prevention, National Center for Health Statistics, National Vital Statistics System.

[16]  W. Mitzner,et al.  Telomere length is a determinant of emphysema susceptibility. , 2011, American journal of respiratory and critical care medicine.

[17]  M. G. Reese,et al.  A probabilistic disease-gene finder for personal genomes. , 2011, Genome research.

[18]  Xiaodong Qi,et al.  Syndrome complex of bone marrow failure and pulmonary fibrosis predicts germline defects in telomerase. , 2011, Blood.

[19]  P. Lansdorp,et al.  Ancestral Mutation in Telomerase Causes Defects in Repeat Addition Processivity and Manifests As Familial Pulmonary Fibrosis , 2011, PLoS genetics.

[20]  E. Regan,et al.  Genetic Epidemiology of COPD (COPDGene) Study Design , 2011, COPD.

[21]  D. Altshuler,et al.  A map of human genome variation from population-scale sequencing , 2010, Nature.

[22]  R. Wise,et al.  Mortality in COPD: Causes, Risk Factors, and Prevention , 2010, COPD.

[23]  G. Raghu,et al.  Telomere Lengths, Pulmonary Fibrosis and Telomerase (TERT) Mutations , 2010, PloS one.

[24]  Joshua D. Podlevsky,et al.  A novel motif in telomerase reverse transcriptase regulates telomere repeat addition rate and processivity , 2009, Nucleic Acids Research.

[25]  Margaret A. Strong,et al.  Short telomeres are sufficient to cause the degenerative defects associated with aging. , 2009, American journal of human genetics.

[26]  E. Silverman,et al.  Genetics of COPD and emphysema. , 2009, Chest.

[27]  M. Armanios Syndromes of telomere shortening. , 2009, Annual review of genomics and human genetics.

[28]  Edwin K Silverman,et al.  Clinical practice. Alpha1-antitrypsin deficiency. , 2009, New England Journal of Medicine.

[29]  Richard M. Cawthon,et al.  Telomere length measurement by a novel monochrome multiplex quantitative PCR method , 2009, Nucleic acids research.

[30]  P. Lansdorp,et al.  Short telomeres are a risk factor for idiopathic pulmonary fibrosis , 2008, Proceedings of the National Academy of Sciences.

[31]  P. Lansdorp,et al.  Telomerase mutations in families with idiopathic pulmonary fibrosis. , 2007, The New England journal of medicine.

[32]  S. Chanock,et al.  Mutations in TERT, the gene for telomerase reverse transcriptase, in aplastic anemia. , 2005, The New England journal of medicine.

[33]  C. Bergsten Causes, Risk Factors, and Prevention of Laminitis and Related Claw Lesions , 2003, Acta veterinaria Scandinavica. Supplementum.

[34]  T R Hughes,et al.  Reverse transcriptase motifs in the catalytic subunit of telomerase. , 1997, Science.

[35]  W. Bailey,et al.  Effects of Smoking Intervention and the Use of an Inhaled Anticholinergic Bronchodilator on the Rate of Decline of FEV1 , 1994 .

[36]  A. Buist,et al.  The Lung Health Study. Baseline characteristics of randomized participants. , 1993, Chest.

[37]  C. Harley,et al.  Telomeres shorten during ageing of human fibroblasts , 1990, Nature.

[38]  E. Blackburn,et al.  A telomeric sequence in the RNA of Tetrahymena telomerase required for telomere repeat synthesis , 1989, Nature.

[39]  Carol W. Greider,et al.  The telomere terminal transferase of tetrahymena is a ribonucleoprotein enzyme with two kinds of primer specificity , 1987, Cell.

[40]  Carol W. Greider,et al.  Identification of a specific telomere terminal transferase activity in tetrahymena extracts , 1985, Cell.

[41]  S. Kojima,et al.  Mutations in telomerase catalytic protein in Japanese children with aplastic anemia. , 2006, Haematologica.

[42]  J. Heffner,et al.  Spontaneous pneumothorax. , 2000, The New England journal of medicine.