Conditional knockout of telomerase reverse transcriptase in mesenchymal cells impairs mouse pulmonary fibrosis

PLoS ONE

Volumn 10, Issue 11, 2015, Pages

  Liu, Tianju ^a   Yu, Hongfeng ^a   Ding, Lin ^a   Wu, Zhe ^a   De Los Santos, Francina Gonzalez ^a   Liu, Jianhua ^a   Ullenbruch, Matthew ^a   Hu, Biao ^a   Martins, Vanessa ^b   Phan, Sem H ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; COLLAGEN TYPE 1; HYDROXYPROLINE; MESSENGER RNA; TELOMERASE REVERSE TRANSCRIPTASE; TELOMERASE; TERT PROTEIN, MOUSE;

ALLELE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL ACTIVITY; CELL DIFFERENTIATION; CELL POPULATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME DEFICIENCY; ENZYME REGULATION; ENZYME SPECIFICITY; KNOCKOUT MOUSE; LUNG FIBROBLAST; LUNG FIBROSIS; MESENCHYME CELL; MOUSE; MYOFIBROBLAST; NONHUMAN; PATHOPHYSIOLOGY; PROTEIN CONTENT; PROTEIN EXPRESSION; STEM CELL; TISSUE REACTION; TRANSGENIC MOUSE; ANIMAL; C57BL MOUSE; GENETICS; MESENCHYMAL STROMA CELL; PATHOLOGY;

ANIMALS; MESENCHYMAL STROMAL CELLS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PULMONARY FIBROSIS; TELOMERASE;

EID: 84953283517     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0142547     Document Type: Article

References (50)

1. Greider CW. Telomere length regulation. Annu Rev Biochem. 1996; 65:337-65. Epub 1996/01/01. doi: 10.1146/annurev.bi.65.070196.002005 .
2. Morrison SJ, Prowse KR, Ho P, Weissman IL. Telomerase activity in hematopoietic cells is associated with self-renewal potential. Immunity. 1996; 5(3):207-16. Epub 1996/09/01. doi: S1074-7613(00) 80316-7 [pii]. .
3. Yui J, Chiu CP, Lansdorp PM. Telomerase activity in candidate stem cells from fetal liver and adult bone marrow. Blood. 1998; 91(9):3255-62. Epub 1998/05/23. .
4. Nozaki Y, Liu T, Hatano K, Gharaee-Kermani M, Phan SH. Induction of telomerase activity in fibroblasts from bleomycin-injured lungs. Am J Respir Cell Mol Biol. 2000; 23(4):460-5. Epub 2000/10/06. doi: 10. 1165/ajrcmb.23.4.3958 .
5. Driscoll B, Buckley S, Bui KC, Anderson KD, Warburton D. Telomerase in alveolar epithelial development and repair. Am J Physiol Lung Cell Mol Physiol. 2000; 279(6):L1191-8. Epub 2000/11/15.
6. Bernardes de Jesus B, Blasco MA. Telomerase at the intersection of cancer and aging. Trends Genet. 2013; 29(9):513-20. Epub 2013/07/24. doi: 10.1016/j.tig.2013.06.007 S0168-9525(13)00108-X [pii]
7. Hackett JA, Greider CW. Balancing instability: dual roles for telomerase and telomere dysfunction in tumorigenesis. Oncogene. 2002; 21(4):619-26. Epub 2002/02/19. doi: 10.1038/sj.onc.1205061 .
8. Hoffmeyer K, Raggioli A, Rudloff S, Anton R, Hierholzer A, Del Valle I, et al. Wnt/beta-catenin signaling regulates telomerase in stem cells and cancer cells. Science. 2012; 336(6088):1549-54. Epub 2012/06/23. doi: 10.1126/science.1218370 336/6088/1549 [pii]. .
9. Cao K, Blair CD, Faddah DA, Kieckhaefer JE, Olive M, Erdos MR, et al. Progerin and telomere dysfunction collaborate to trigger cellular senescence in normal human fibroblasts. J Clin Invest. 2011; 121 (7):2833-44. Epub 2011/06/15. doi: 10.1172/JCI43578 43578 [pii]
10. Gonzalez-Suarez E, Samper E, Ramirez A, Flores JM, Martin-Caballero J, Jorcano JL, et al. Increased epidermal tumors and increased skin wound healing in transgenic mice overexpressing the catalytic subunit of telomerase, mTERT, in basal keratinocytes. EMBO J. 2001; 20(11):2619-30. Epub 2001/06/02. doi: 10.1093/emboj/20.11.2619 ; PubMed Central PMCID: PMC125492.
11. Rudolph KL, Chang S, Lee HW, Blasco M, Gottlieb GJ, Greider C, et al. Longevity, stress response, and cancer in aging telomerase-deficient mice. Cell. 1999; 96(5):701-12. Epub 1999/03/25. doi: S0092-8674(00)80580-2 [pii]. .
12. Armanios MY, Chen JJ, Cogan JD, Alder JK, Ingersoll RG, Markin C, et al. Telomerase mutations in families with idiopathic pulmonary fibrosis. N Engl J Med. 2007; 356(13):1317-26. Epub 2007/03/30. doi: 356/13/1317 [pii] doi: 10.1056/NEJMoa066157 .
13. Tsakiri KD, Cronkhite JT, Kuan PJ, Xing C, Raghu G, Weissler JC, et al. Adult-onset pulmonary fibrosis caused by mutations in telomerase. Proc Natl Acad Sci U S A. 2007; 104(18):7552-7. Epub 2007/04/27. doi: 0701009104 [pii] doi: 10.1073/pnas.0701009104
14. Sarin KY, Cheung P, Gilison D, Lee E, Tennen RI, Wang E, et al. Conditional telomerase induction causes proliferation of hair follicle stem cells. Nature. 2005; 436(7053):1048-52. Epub 2005/08/19. doi: nature03836 [pii] doi: 10.1038/nature03836 ; PubMed Central PMCID: PMC1361120.
15. Park JI, Venteicher AS, Hong JY, Choi J, Jun S, Shkreli M, et al. Telomerase modulates Wnt signalling by association with target gene chromatin. Nature. 2009; 460(7251):66-72. Epub 2009/07/03. doi: 10. 1038/nature08137 nature08137 [pii]. .
16. Choi J, Southworth LK, Sarin KY, Venteicher AS, Ma W, Chang W, et al. TERT promotes epithelial proliferation through transcriptional control of a Myc-And Wnt-related developmental program. PLoS Genet. 2008; 4(1):e10. Epub 2008/01/23. doi: 10.1371/journal.pgen.0040010 07-PLGE-RA-0657 [pii]
17. Gordon DM, Santos JH. The emerging role of telomerase reverse transcriptase in mitochondrial DNA metabolism. J Nucleic Acids. 2010; 2010. Epub 2010/10/12. doi: 10.4061/2010/390791 390791 [pii]. ; PubMed Central PMCID: PMC2945669.
18. Saretzki G. Extra-Telomeric functions of human telomerase: cancer, mitochondria and oxidative stress. Curr Pharm Des. 2014; 20(41):6386-403. Epub 2014/07/01. doi: CPD-EPUB-61153 [pii]. .
19. Seimiya H, Sawada H, Muramatsu Y, Shimizu M, Ohko K, Yamane K, et al. Involvement of 14-3-3 proteins in nuclear localization of telomerase. EMBO J. 2000; 19(11):2652-61. Epub 2000/06/03. doi: 10. 1093/emboj/19.11.2652
20. Santos JH, Meyer JN, Skorvaga M, Annab LA, Van Houten B. Mitochondrial hTERT exacerbates freeradical-mediated mtDNA damage. Aging Cell. 2004; 3(6):399-411. Epub 2004/12/01. doi: ACE124 [pii] doi: 10.1111/j.1474-9728.2004.00124.x .
21. Simonicova L, Dudekova H, Ferenc J, Prochazkova K, Nebohacova M, Dusinsky R, et al. Saccharomyces cerevisiae as a model for the study of extranuclear functions of mammalian telomerase. Curr Genet. 2015. Epub 2015/01/09. doi: 10.1007/s00294-014-0472-8 .
22. Buseman CM, Wright WE, Shay JW. Is telomerase a viable target in cancer? Mutat Res. 2012; 730(1-2):90-7. Epub 2011/08/02. doi: 10.1016/j.mrfmmm.2011.07.006 S0027-5107(11)00182-5 [pii]. ; PubMed Central PMCID: PMC3375693.
23. Sirma H, Kumar M, Meena JK, Witt B, Weise JM, Lechel A, et al. The promoter of human telomerase reverse transcriptase is activated during liver regeneration and hepatocyte proliferation. Gastroenterology. 2011; 141(1):326-37, 37 e1-3. Epub 2011/03/31. doi: 10.1053/j.gastro.2011.03.047 S0016-5085 (11)00418-5 [pii]. .
24. Kim JK, Lim Y, Kim KA, Seo MS, Kim JD, Lee KH, et al. Activation of telomerase by silica in rat lung. Toxicol Lett. 2000; 111(3):263-70. Epub 2000/01/22. doi: S0378427499001952 [pii]. .
25. Liu T, Chung MJ, Ullenbruch M, Yu H, Jin H, Hu B, et al. Telomerase activity is required for bleomycininduced pulmonary fibrosis in mice. J Clin Invest. 2007; 117(12):3800-9. Epub 2007/11/17. doi: 10. 1172/JCI32369 ; PubMed Central PMCID: PMC2075478.
26. Mouraret N, Houssaini A, Abid S, Quarck R, Marcos E, Parpaleix A, et al. Role for Telomerase in Pulmonary Hypertension. Circulation. 2014. Epub 2015/01/01. doi: CIRCULATIONAHA.114.013258 [pii] doi: 10.1161/CIRCULATIONAHA.114.013258 .
27. Alder JK, Chen JJ, Lancaster L, Danoff S, Su SC, Cogan JD, et al. Short telomeres are a risk factor for idiopathic pulmonary fibrosis. Proc Natl Acad Sci U S A. 2008; 105(35):13051-6. Epub 2008/08/30. doi: 10.1073/pnas.0804280105 0804280105 [pii]
28. Cronkhite JT, Xing C, Raghu G, Chin KM, Torres F, Rosenblatt RL, et al. Telomere shortening in familial and sporadic pulmonary fibrosis. Am J Respir Crit Care Med. 2008; 178(7):729-37. Epub 2008/07/19. doi: 10.1164/rccm.200804-550OC 200804-550OC [pii]. ; PubMed Central PMCID: PMC2556455.
29. Alder JK, Stanley SE, Wagner CL, Hamilton M, Hanumanthu VS, Armanios M. Exome sequencing identifies mutant TINF2 in a family with pulmonary fibrosis. Chest. 2015; 147(5):1361-8. Epub 2014/12/doi: 10.1378/chest.14-1947 2087933 [pii]. ; PubMed Central PMCID: PMC4420184.
30. Cogan JD, Kropski JA, Zhao M, Mitchell DB, Rives L, Markin C, et al. Rare variants in RTEL1 are associated with familial interstitial pneumonia. Am J Respir Crit Care Med. 2015; 191(6):646-55. Epub 2015/01/22. doi: 10.1164/rccm.201408-1510OC ; PubMed Central PMCID: PMC4384777.
31. Stuart BD, Choi J, Zaidi S, Xing C, Holohan B, Chen R, et al. Exome sequencing links mutations in PARN and RTEL1 with familial pulmonary fibrosis and telomere shortening. Nat Genet. 2015; 47 (5):512-7. Epub 2015/04/08. doi: 10.1038/ng.3278 ng.3278 [pii]. ; PubMed Central PMCID: PMC4414891.
32. Kropski JA, Mitchell DB, Markin C, Polosukhin VV, Choi L, Johnson JE, et al. A novel dyskerin (DKC1) mutation is associated with familial interstitial pneumonia. Chest. 2014; 146(1):e1-7. Epub 2014/02/08. doi: 1828400 [pii] doi: 10.1378/chest.13-2224 ; PubMed Central PMCID: PMC4077414.
33. Liu T, Ullenbruch M, Young Choi Y, Yu H, Ding L, Xaubet A, et al. Telomerase and telomere length in pulmonary fibrosis. Am J Respir Cell Mol Biol. 2013; 49(2):260-8. Epub 2013/03/26. doi: 10.1165/rcmb.2012-0514OC rcmb.2012-0514OC [pii]
34. Liu T, Yu H, Ullenbruch M, Jin H, Ito T, Wu Z, et al. The in vivo fibrotic role of FIZZ1 in pulmonary fibrosis. PLoS One. 2014; 9(2):e88362. Epub 2014/02/12. doi: 10.1371/journal.pone.0088362 PONE-D-13-34403 [pii]. ; PubMed Central PMCID: PMC3916640.
35. Hu B, Wu Z, Nakashima T, Phan SH. Mesenchymal-specific deletion of C/EBPbeta suppresses pulmonary fibrosis. Am J Pathol. 2012; 180(6):2257-67. Epub 2012/04/17. doi: 10.1016/j.ajpath.2012.02.010 S0002-9440(12)00229-5 [pii].
36. Huaux F, Liu T, McGarry B, Ullenbruch M, Phan SH. Dual roles of IL-4 in lung injury and fibrosis. J Immunol. 2003; 170(4):2083-92. Epub 2003/02/08. .
37. Yang J, Wheeler SE, Velikoff M, Kleaveland KR, LaFemina MJ, Frank JA, et al. Activated alveolar epithelial cells initiate fibrosis through secretion of mesenchymal proteins. Am J Pathol. 2013; 183 (5):1559-70. Epub 2013/09/10. doi: 10.1016/j.ajpath.2013.07.016 S0002-9440(13)00537-3 [pii]. ; PubMed Central PMCID: PMC3814683.
38. Gazzaniga FS, Blackburn EH. An antiapoptotic role for telomerase RNA in human immune cells independent of telomere integrity or telomerase enzymatic activity. Blood. 2014; 124(25):3675-84. Epub 2014/10/17. doi: 10.1182/blood-2014-06-582254 blood-2014-06-582254 [pii]. ; PubMed Central PMCID: PMC4263978.
39. Liu T, Hu B, Chung MJ, Ullenbruch M, Jin H, Phan SH. Telomerase regulation of myofibroblast differentiation. Am J Respir Cell Mol Biol. 2006; 34(5):625-33. Epub 2006/01/21. doi: 2005-0252OC [pii] doi: 10.1165/rcmb.2005-0252OC ; PubMed Central PMCID: PMC2644224.
40. Richardson GD, Breault D, Horrocks G, Cormack S, Hole N, Owens WA. Telomerase expression in the mammalian heart. FASEB J. 2012; 26(12):4832-40. Epub 2012/08/25. doi: 10.1096/fj.12-208843 fj.12-208843 [pii]. ; PubMed Central PMCID: PMC3509052.
41. Ujike-Asai A, Okada A, Du Y, Maruyama M, Yuan X, Ishikawa F, et al. Large defects of type I allergic response in telomerase reverse transcriptase knockout mice. J Leukoc Biol. 2007; 82(2):429-35. Epub 2007/04/26. doi: jlb.1006638 [pii] doi: 10.1189/jlb.1006638 .
42. Peng R, Sridhar S, Tyagi G, Phillips JE, Garrido R, Harris P, et al. Bleomycin induces molecular changes directly relevant to idiopathic pulmonary fibrosis: a model for "active" disease. PLoS One. 2013; 8(4):e59348. Epub 2013/04/09. doi: 10.1371/journal.pone.0059348 PONE-D-12-30099 [pii]. ; PubMed Central PMCID: PMC3614979.
43. Bauer Y, Tedrow J, de Bernard S, Birker-Robaczewska M, Gibson KF, Guardela BJ, et al. A novel genomic signature with translational significance for human idiopathic pulmonary fibrosis. Am J Respir Cell Mol Biol. 2015; 52(2):217-31. Epub 2014/07/17. doi: 10.1165/rcmb.2013-0310OC ; PubMed Central PMCID: PMC4370242.
44. Thannickal VJ, Horowitz JC. Evolving concepts of apoptosis in idiopathic pulmonary fibrosis. Proc Am Thorac Soc. 2006; 3(4):350-6. Epub 2006/06/02. doi: 3/4/350 [pii] doi: 10.1513/pats.200601-001TK ; PubMed Central PMCID: PMC2231523.
45. Phan SH. Genesis of the myofibroblast in lung injury and fibrosis. Proc Am Thorac Soc. 2012; 9 (3):148-52. Epub 2012/07/18. doi: 10.1513/pats.201201-011AW 9/3/148 [pii]. .
46. Westin ER, Chavez E, Lee KM, Gourronc FA, Riley S, Lansdorp PM, et al. Telomere restoration and extension of proliferative lifespan in dyskeratosis congenita fibroblasts. Aging Cell. 2007; 6(3):383-94. Epub 2007/03/27. doi: ACE288 [pii] doi: 10.1111/j.1474-9726.2007.00288.x ; PubMed Central PMCID: PMC2225626.
47. Wong JM, Collins K. Telomerase RNA level limits telomere maintenance in X-linked dyskeratosis congenita. Genes Dev. 2006; 20(20):2848-58. Epub 2006/10/04. doi: gad.1476206 [pii] doi: 10.1101/gad. 1476206 ; PubMed Central PMCID: PMC1619937.
48. Shang Y, Yu D, Hao L. Liposome-Adenoviral hTERT-siRNA Knockdown in Fibroblasts from Keloids Reduce Telomere Length and Fibroblast Growth. Cell Biochem Biophys. 2015. Epub 2015/01/07. doi: 10.1007/s12013-014-0476-5 .
49. Fridlender ZG, Cohen PY, Golan O, Arish N, Wallach-Dayan S, Breuer R. Telomerase activity in bleomycin-induced epithelial cell apoptosis and lung fibrosis. Eur Respir J. 2007; 30(2):205-13. Epub 2007/05/17. doi: 09031936.00009407 [pii] doi: 10.1183/09031936.00009407 .
50. Waisberg DR, Parra ER, Barbas-Filho JV, Fernezlian S, Capelozzi VL. Increased fibroblast telomerase expression precedes myofibroblast alpha-smooth muscle actin expression in idiopathic pulmonary fibrosis. Clinics (Sao Paulo). 2012; 67(9):1039-46. Epub 2012/09/29. doi: S1807-59322012000900010 [pii]. ; PubMed Central PMCID: PMC3438244.