The role of telomeres in the ageing of human skin: Telomeres and skin ageing

Buckingham, Erin M.; Klingelhutz, Aloysius J.

doi:10.1111/j.1600-0625.2010.01242.x

Cited by 109Telomeres, Telomerase, and SenescenceSkin Protection and AgingGenetics, Aging, and Longevity in Model Organisms

The role of telomeres in the ageing of human skin: Telomeres and skin ageing

Open access

Buckingham, Erin M., Klingelhutz, Aloysius J.·2011·Experimental Dermatology

DOI 10.1111/j.1600-0625.2010.01242.xPMC PMC3690281

Open this paper in CoChat — free account Open PDF

Abstract

Skin is a self-renewing tissue that is required to go through extensive proliferation throughout the lifespan of an organism. Telomere shortening acts as a mitotic clock that prevents aberrant proliferation such as cancer. A consequence of this protection is cellular senescence and ageing. The telomerase enzyme complex maintains telomere length in germline cells and in cancer cells. Telomerase is also active in certain somatic cells such as those in the epidermis but is almost undetectable in the dermis. Increasing evidence indicates that telomerase plays a significant role in maintenance of skin function and proliferation. Mutations in telomerase component genes in the disease dyskeratosis congenita result in numerous epidermal abnormalities. Studies also indicate that telomerase activity in epidermal stem cells might have roles that go beyond telomere elongation. Telomeres in skin cells may be particularly susceptible to accelerated shortening because of both proliferation and DNA-damaging agents such as reactive oxygen species. Skin might present an accessible tissue for manipulation of telomerase activity and telomere length with the potential of ameliorating skin diseases associated with ageing.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Integrity signals

Registry

Crossref · 10.1111/j.1600-0625.2010.01242.x

Cites

120 of 120 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

UV radiation induces excessive ROS production, resulting in telomere mutations and further cell death.
“UV radiation is known to induce excessive ROS production, resulting in telomere mutations and further cell death [72].”
From Boosting the Photoaged Skin: The Potential Role of Dietary Components (2021) · cites this paper as [72]
Reactive oxygen generated by UV radiation induces telomere mutation, cell death, or senescence.
“The reactive oxygen generated by UV radiation induces telomere mutation, cell death, or senescence.”
From Diet and Skin Aging—From the Perspective of Food Nutrition (2020) · cites this paper as [41]

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Specific Association of Human Telomerase Activity with Immortal Cells and Cancer
Kim, N. W., Piatyszek, M. A., Prowse, K. R., Harley, C. B., West, M. D., Ho, P. L. C., Coviello, G. M., Wright, W. E., Weinrich, S. L., & Shay, J. W. (1994) · Science · doi:10.1126/science.7605428 · Cited by 7,091 · see citing works
Extension of Life-Span by Introduction of Telomerase into Normal Human Cells
Bodnar, A. G., Ouellette, M., Frolkis, M., Holt, S. E., Chiu, C.-P., Morin, G. B., Harley, C. B., Shay, J. W., Lichtsteiner, S., & Wright, W. E. (1998) · Science · doi:10.1126/science.279.5349.349 · Cited by 4,975 · see citing works
Identification of a specific telomere terminal transferase activity in tetrahymena extracts
Greider, C. W., & Blackburn, E. H. (1985) · Cell · doi:10.1016/0092-8674(85)90170-9 · Cited by 3,400 · see citing works
Shelterin: the protein complex that shapes and safeguards human telomeres
de Lange, T. (2005) · Genes & Development · doi:10.1101/gad.1346005 · Cited by 3,056 · see citing works
A DNA damage checkpoint response in telomere-initiated senescence
Fagagna, F. D. D., Reaper, P. M., Clay-Farrace, L., Fiegler, H., Carr, P., von Zglinicki, T., Saretzki, G., Carter, N. P., & Jackson, S. P. (2003) · Nature · doi:10.1038/nature02118 · Cited by 2,855 · see citing works
Oxidative stress shortens telomeres
von Zglinicki, T. (2002) · Trends in Biochemical Sciences · doi:10.1016/s0968-0004(02)02110-2 · Cited by 2,524 · see citing works
A highly conserved repetitive DNA sequence, (TTAGGG)n, present at the telomeres of human chromosomes.
Moyzis, R. K., Buckingham, J. M., Cram, L. S., Dani, M. A. C., Deaven, L. L., Jones, M. D., Meyne, J., Ratliff, R. L., & Wu, J. R. (1988) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.85.18.6622 · Cited by 2,326 · see citing works
Telomere Shortening and Tumor Formation by Mouse Cells Lacking Telomerase RNA
Blasco, M. A., Lee, H.-W., Hande, M. P., Samper, E., Lansdorp, P. M., DePinho, R. A., & Greider, C. W. (1997) · Cell · doi:10.1016/s0092-8674(01)80006-4 · Cited by 2,108 · see citing works
A telomeric sequence in the RNA of Tetrahymena telomerase required for telomere repeat synthesis
Greider, C. W., & Blackburn, E. H. (1989) · Nature · doi:10.1038/337331a0 · Cited by 1,643 · see citing works
Telomerase Mutations in Families with Idiopathic Pulmonary Fibrosis
Armanios, M. Y., Chen, J. J.-L., Cogan, J. D., Alder, J. K., Ingersoll, R. G., Markin, C., Lawson, W. E., Xie, M., Vulto, I., Phillips, J. A., et al. (2007) · New England Journal of Medicine · doi:10.1056/nejmoa066157 · Cited by 1,357 · see citing works
Longevity, Stress Response, and Cancer in Aging Telomerase-Deficient Mice
Rudolph, K. L., Chang, S., Lee, H.-W., Blasco, M., Gottlieb, G. J., Greider, C., & DePinho, R. A. (1999) · Cell · doi:10.1016/s0092-8674(00)80580-2 · Cited by 1,349 · see citing works
Telomere elongation in immortal human cells without detectable telomerase activity
Bryan, T. M., Englezou, A., Gupta, J., Bacchetti, S., & Reddel, R. R. (1995) · The EMBO Journal · doi:10.1002/j.1460-2075.1995.tb00098.x · Cited by 1,279 · see citing works
Both Rb/p16INK4a inactivation and telomerase activity are required to immortalize human epithelial cells
Kiyono, T., Foster, S. A., Koop, J. I., McDougall, J. K., Galloway, D. A., & Klingelhutz, A. J. (1998) · Nature · doi:10.1038/23962 · Cited by 1,206 · see citing works
Self-citation
Telomeres and Aging
Aubert, G., & Lansdorp, P. M. (2008) · Physiological Reviews · doi:10.1152/physrev.00026.2007 · Cited by 1,188 · see citing works
A telomerase component is defective in the human disease dyskeratosis congenita
Mitchell, J. R., Wood, E., & Collins, K. (1999) · Nature · doi:10.1038/990141 · Cited by 1,168 · see citing works
Telomere loss: mitotic clock or genetic time bomb?
Harley, C. B. (1991) · Mutation Research/DNAging · doi:10.1016/0921-8734(91)90018-7 · Cited by 1,139 · see citing works
Human Keratinocytes That Express hTERT and Also Bypass a p16 INK4a -Enforced Mechanism That Limits Life Span Become Immortal yet Retain Normal Growth and Differentiation Characteristics
Dickson, M. A., Hahn, W. C., Ino, Y., Ronfard, V., Wu, J. Y., Weinberg, R. A., Louis, D. N., Li, F. P., & Rheinwald, J. G. (2000) · Molecular and Cellular Biology · doi:10.1128/mcb.20.4.1436-1447.2000 · Cited by 1,104 · see citing works
Telomere end-replication problem and cell aging
Levy, M. Z., Allsopp, R. C., Futcher, A. B., Greider, C. W., & Harley, C. B. (1992) · Journal of Molecular Biology · doi:10.1016/0022-2836(92)90096-3 · Cited by 1,069 · see citing works
Alternative lengthening of telomeres: models, mechanisms and implications
Cesare, A. J., & Reddel, R. R. (2010) · Nature Reviews Genetics · doi:10.1038/nrg2763 · Cited by 1,022 · see citing works
Telomeres: protecting chromosomes against genome instability
O’Sullivan, R. J., & Karlseder, J. (2010) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2848 · Cited by 994 · see citing works
X-linked dyskeratosis congenita is caused by mutations in a highly conserved gene with putative nucleolar functions
Heiss, N. S., Knight, S. W., Vulliamy, T. J., Klauck, S. M., Wiemann, S., Mason, P. J., Poustka, A., & Dokal, I. (1998) · Nature Genetics · doi:10.1038/ng0598-32 · Cited by 976 · see citing works
The RNA component of telomerase is mutated in autosomal dominant dyskeratosis congenita
Vulliamy, T., Marrone, A., Goldman, F., Dearlove, A., Bessler, M., Mason, P. J., & Dokal, I. (2001) · Nature · doi:10.1038/35096585 · Cited by 960 · see citing works
Adult-onset pulmonary fibrosis caused by mutations in telomerase
Tsakiri, K. D., Cronkhite, J. T., Kuan, P. J., Xing, C., Raghu, G., Weissler, J. C., Rosenblatt, R. L., Shay, J. W., & Garcia, C. K. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0701009104 · Cited by 894 · see citing works
Regulation of telomerase by telomeric proteins.
Smogorzewska, A., & de Lange, T. (2004) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.73.071403.160049 · Cited by 857 · see citing works
Mild hyperoxia shortens telomeres and inhibits proliferation of fibroblasts: a model for senescence?
von Zglinicki, T., Saretzki, G., Döcke, W., & Lotze, C. (1995) · Experimental Cell Research · doi:10.1006/excr.1995.1305 · Cited by 856 · see citing works
Telomerase activation by the E6 gene product of human papillomavirus type 16
Klingelhutz, A. J., Foster, S. A., & McDougall, J. K. (1996) · Nature · doi:10.1038/380079a0 · Cited by 823 · see citing works
Self-citation
Mutations in TERT, the Gene for Telomerase Reverse Transcriptase, in Aplastic Anemia
Yamaguchi, H., Calado, R. T., Ly, H., Kajigaya, S., Baerlocher, G. M., Chanock, S. J., Lansdorp, P. M., & Young, N. S. (2005) · New England Journal of Medicine · doi:10.1056/nejmoa042980 · Cited by 723 · see citing works
Developmental and tissue-specific regulation of mouse telomerase and telomere length.
Prowse, K. R., & Greider, C. W. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.11.4818 · Cited by 686 · see citing works
Telomerase in the human organism
Collins, K., & Mitchell, J. R. (2002) · Oncogene · doi:10.1038/sj.onc.1205083 · Cited by 600 · see citing works
Telomere Shortening in Familial and Sporadic Pulmonary Fibrosis
Cronkhite, J. T., Xing, C., Raghu, G., Chin, K. M., Torres, F., Rosenblatt, R. L., & Kim Garcia, C. (2008) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.200804-550oc · Cited by 573 · see citing works
Mechanism of telomere shortening by oxidative stress
KAWANISHI, S., & OIKAWA, S. (2004) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1297.047 · Cited by 522 · see citing works
Telomerase activity in the regenerative basal layer of the epidermis inhuman skin and in immortal and carcinoma-derived skin keratinocytes.
Härle-Bachor, C., & Boukamp, P. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.13.6476 · Cited by 492 · see citing works
Telomerase Reverse Transcriptase Delays Aging in Cancer-Resistant Mice
Tomás-Loba, A., Flores, I., Fernández-Marcos, P. J., Cayuela, M. L., Maraver, A., Tejera, A., Borrás, C., Matheu, A., Klatt, P., Flores, J. M., et al. (2008) · Cell · doi:10.1016/j.cell.2008.09.034 · Cited by 484 · see citing works
Haploinsufficiency of t e lomerase reverse transcriptase leads to anticipation in autosomal dominant dyskeratosis congenita
Armanios, M., Chen, J.-L., Chang, Y.-P. C., Brodsky, R. A., Hawkins, A., Griffin, C. A., Eshleman, J. R., Cohen, A. R., Chakravarti, A., Hamosh, A., et al. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0508124102 · Cited by 452 · see citing works
Effects of Telomerase and Telomere Length on Epidermal Stem Cell Behavior
Flores, I., Cayuela, M. L., & Blasco, M. A. (2005) · Science · doi:10.1126/science.1115025 · Cited by 448 · see citing works
Putative telomere-independent mechanisms of replicative aging reflect inadequate growth conditions
Ramirez, R. D., Morales, C. P., Herbert, B.-S., Rohde, J. M., Passons, C., Shay, J. W., & Wright, W. E. (2001) · Genes & Development · doi:10.1101/gad.859201 · Cited by 444 · see citing works
Conditional telomerase induction causes proliferation of hair follicle stem cells
Sarin, K. Y., Cheung, P., Gilison, D., Lee, E., Tennen, R. I., Wang, E., Artandi, M. K., Oro, A. E., & Artandi, S. E. (2005) · Nature · doi:10.1038/nature03836 · Cited by 425 · see citing works
TINF2, a Component of the Shelterin Telomere Protection Complex, Is Mutated in Dyskeratosis Congenita
Savage, S. A., Giri, N., Baerlocher, G. M., Orr, N., Lansdorp, P. M., & Alter, B. P. (2008) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2007.10.004 · Cited by 414 · see citing works
A randomized comparison of indwelling pleural catheter and doxycycline pleurodesis in the management of malignant pleural effusions
Putnam, J. B., Light, R. W., Rodriguez, R. M., Ponn, R. B., Olak, J., Pollak, J. S., Lee, R. B., Payne, D. K., Graeber, G., & Kovitz, K. L. (1999) · Cancer · doi:10.1002/(sici)1097-0142(19991115)86:10 · Cited by 385 · see citing works
Increased epidermal tumors and increased skin wound healing in transgenic mice overexpressing the catalytic subunit of telomerase, mTERT, in basal keratinocytes
González‐Suárez, E., Samper, E., Ramírez, A., Flores, J. M., Martín‐Caballero, J., Jorcano, J. L., & Blasco, M. A. (2001) · The EMBO Journal · doi:10.1093/emboj/20.11.2619 · Cited by 372 · see citing works
Increased telomere fragility and fusions resulting from TRF1 deficiency lead to degenerative pathologies and increased cancer in micePreprint
Martínez, P., Thanasoula, M., Muñoz, P., Liao, C., Tejera, Á. M., McNees, C. J., Flores, J. M., Fernández-Capetillo, Ó., Tarsounas, M., & Blasco, M. A. (2009) · Genes & Development · doi:10.1101/gad.543509 · Cited by 367 · see citing works
Functional Characterization and Developmental Regulation of Mouse Telomerase RNA
Blasco, M. A., Funk, W. D., Villeponteau, B., & Greider, C. W. (1995) · Science · doi:10.1126/science.7544492 · Cited by 361 · see citing works
The longest telomeres: a general signature of adult stem cell compartments
Flores, I., Canela, A., Vera, E., Tejera, A., Cotsarelis, G., & Blasco, M. A. (2008) · Genes & Development · doi:10.1101/gad.451008 · Cited by 352 · see citing works
Mutations in the telomerase component NHP2 cause the premature ageing syndrome dyskeratosis congenita
Vulliamy, T., Beswick, R., Kirwan, M., Marrone, A., Digweed, M., Walne, A., & Dokal, I. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0800042105 · Cited by 334 · see citing works
Telomere length in different tissues of elderly patients
Friedrich, U., Griese, E.-U., Schwab, M., Fritz, P., Thon, K.-P., & Klotz, U. (2000) · Mechanisms of Ageing and Development · doi:10.1016/s0047-6374(00)00173-1 · Cited by 325 · see citing works
Syndromes of Telomere Shortening
Armanios, M. (2009) · Annual Review of Genomics and Human Genetics · doi:10.1146/annurev-genom-082908-150046 · Cited by 317 · see citing works
TINF2 mutations result in very short telomeres: analysis of a large cohort of patients with dyskeratosis congenita and related bone marrow failure syndromes
Walne, A. J., Vulliamy, T., Beswick, R., Kirwan, M., & Dokal, I. (2008) · Blood · doi:10.1182/blood-2008-05-153445 · Cited by 317 · see citing works
Genetic heterogeneity in autosomal recessive dyskeratosis congenita with one subtype due to mutations in the telomerase-associated protein NOP10
Walne, A. J., Vulliamy, T., Marrone, A., Beswick, R., Kirwan, M., Masunari, Y., Al-Qurashi, F.-H., Aljurf, M., & Dokal, I. (2007) · Human Molecular Genetics · doi:10.1093/hmg/ddm111 · Cited by 316 · see citing works
Short Telomeres, even in the Presence of Telomerase, Limit Tissue Renewal Capacity
Hao, L.-Y., Armanios, M., Strong, M. A., Karim, B., Feldser, D. M., Huso, D., & Greider, C. W. (2005) · Cell · doi:10.1016/j.cell.2005.11.020 · Cited by 302 · see citing works
Mutations of the human telomerase RNA gene (TERC) in aplastic anemia and myelodysplastic syndrome
Yamaguchi, H., Baerlocher, G. M., Lansdorp, P. M., Chanock, S. J., Nunez, O., Sloand, E., & Young, N. S. (2003) · Blood · doi:10.1182/blood-2003-01-0335 · Cited by 301 · see citing works
Telomerase Regulation, Cell Cycle, and Telomere Stability in Primitive Hematopoietic Cells
Engelhardt, M. M., Kumar, R., Albanell, J., Pettengell, R., Han, W., & Moore, M. A. S. (1997) · Blood · doi:10.1182/blood.v90.1.182 · Cited by 297 · see citing works
Transcriptional Activation of the Telomerase hTERT Gene by Human Papillomavirus Type 16 E6 Oncoprotein
Veldman, T., Horikawa, I., Barrett, J. C., & Schlegel, R. (2001) · Journal of Virology · doi:10.1128/jvi.75.9.4467-4472.2001 · Cited by 280 · see citing works
Detection of Telomerase Activity in Malignant and Nonmalignant Skin Conditions
Taylor, R. S., Ramirez, R. D., Ogoshi, M., Chaffins, M. L., Piatyszek, M. A., & Shay, J. W. (1996) · Journal of Investigative Dermatology · doi:10.1111/1523-1747.ep12345811 · Cited by 267 · see citing works
Identification of a novel telomerase repressor that interacts with the human papillomavirus type-16 E6/E6-AP complexPreprint
Gewin, L. C., Myers, H. E., Kiyono, T., & Galloway, D. A. (2004) · Genes & Development · doi:10.1101/gad.1214704 · Cited by 267 · see citing works
Short Telomeres are Sufficient to Cause the Degenerative Defects Associated with Aging
Armanios, M., Alder, J. K., Parry, E. M., Karim, B., Strong, M. A., & Greider, C. W. (2009) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2009.10.028 · Cited by 257 · see citing works
Studies of the molecular mechanisms in the regulation of telomerase activity
Liu, J. (1999) · The FASEB Journal · doi:10.1096/fasebj.13.15.2091 · Cited by 253 · see citing works
A Spectrum of Severe Familial Liver Disorders Associate with Telomerase Mutations
Calado, R. T., Regal, J. A., Kleiner, D. E., Schrump, D. S., Peterson, N. R., Pons, V., Chanock, S. J., Lansdorp, P. M., & Young, N. S. (2009) · PLoS ONE · doi:10.1371/journal.pone.0007926 · Cited by 252 · see citing works
Telomerase activity in normal human epithelial cells.
Yasumoto, S., Kunimura, C., Kikuchi, K., Tahara, H., Ohji, H., Yamamoto, H., Ide, T., & Utakoji, T. (1996) · PubMed · Cited by 247 · see citing works
Human papillomavirus E6 and Myc proteins associate in vivo and bind to and cooperatively activate the telomerase reverse transcriptase promoter
Veldman, T., Liu, X., Yuan, H., & Schlegel, R. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1435900100 · Cited by 246 · see citing works
Dyskeratosis congenita: a genetic disorder of many faces
Kirwan, M., & Dokal, I. S. (2007) · Clinical Genetics · doi:10.1111/j.1399-0004.2007.00923.x · Cited by 238 · see citing works
Fifty years of skin aging
Yaar, M., Eller, M. S., & Gilchrest, B. A. (2002) · Journal of Investigative Dermatology Symposium Proceedings · doi:10.1046/j.1523-1747.2002.19636.x · Cited by 233 · see citing works
Unexplained aplastic anaemia, immunodeficiency, and cerebellar hypoplasia (Hoyeraal‐Hreidarsson syndrome) due to mutations in the dyskeratosis congenita gene, DKC1
Knight, S. W., Heiss, N. S., Vulliamy, T., Aalfs, C. M., McMahon, C., Richmond, P., Jones, A., Hennekam, R. C. M., Poustka, A., Mason, P. J., et al. (1999) · British Journal of Haematology · doi:10.1046/j.1365-2141.1999.01690.x · Cited by 230 · see citing works
Wild-derived inbred mouse strains have short telomeres
Hemann, M. T. (2000) · Nucleic Acids Research · doi:10.1093/nar/28.22.4474 · Cited by 227 · see citing works
Mutations in the reverse transcriptase component of telomerase (TERT) in patients with bone marrow failure
Vulliamy, T., Walne, A. J., Baskaradas, A., Mason, P. J., Marrone, A., & Dokal, I. S. (2005) · Blood Cells Molecules and Diseases · doi:10.1016/j.bcmd.2004.12.008 · Cited by 207 · see citing works
Telomerase RNA level limits telomere maintenance in X-linked dyskeratosis congenitaPreprint
Wong, J. M. Y., & Collins, K. (2006) · Genes & Development · doi:10.1101/gad.1476206 · Cited by 201 · see citing works
The role of telomeres in skin aging/photoaging
Kosmadaki, M., & Gilchrest, B. A. (2003) · Micron · doi:10.1016/j.micron.2003.11.002 · Cited by 198 · see citing works
Regulation of the human telomerase reverse transcriptase gene
Ducrest, A., Szutorisz, H., Lingner, J., & Nabholz, M. (2002) · Oncogene · doi:10.1038/sj.onc.1205081 · Cited by 184 · see citing works
Constitutional hypomorphic telomerase mutations in patients with acute myeloid leukemia
Calado, R. T., Regal, J. A., Hills, M., Yewdell, W. T., Dalmazzo, L. F., Zago, M. A., Lansdorp, P. M., Hogge, D., Chanock, S. J., Estey, E. H., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0807057106 · Cited by 184 · see citing works
Increased copy number of the TERT and TERC telomerase subunit genes in cancer cells
Cao, Y., Bryan, T. M., & Reddel, R. R. (2008) · Cancer Science · doi:10.1111/j.1349-7006.2008.00815.x · Cited by 180 · see citing works
Telomerase Activity Concentrates in the Mitotically Active Segments of Human Hair Follicles
Ramirez, R. D., Wright, W. E., Shay, J. W., & Taylor, R. S. (1997) · Journal of Investigative Dermatology · doi:10.1111/1523-1747.ep12285654 · Cited by 174 · see citing works
The IGF-1/IGF-1R signaling axis in the skin: a new role for the dermis in aging-associated skin cancer
Lewis, D. A., Travers, J. B., Somani, A.-K., & Spandau, D. F. (2009) · Oncogene · doi:10.1038/onc.2009.440 · Cited by 166 · see citing works
TERC and TERT gene mutations in patients with bone marrow failure and the significance of telomere length measurements
Du, H.-Y., Pumbo, E., Ivanovich, J., An, P., Maziarz, R. T., Reiss, U. M., Chirnomas, D., Shimamura, A., Vlachos, A., Lipton, J. M., et al. (2009) · Blood · doi:10.1182/blood-2008-07-166421 · Cited by 158 · see citing works
Human diseases of telomerase dysfunction: insights into tissue aging
Garcia, C. K., Wright, W. E., & Shay, J. W. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkm644 · Cited by 156 · see citing works
Telomerase Expression Restores Dermal Integrity to in Vitro-Aged Fibroblasts in a Reconstituted Skin Model
Funk, W. D., Wang, C. K., Shelton, D. N., Harley, C. B., Pagon, G. D., & Hoeffler, W. K. (2000) · Experimental Cell Research · doi:10.1006/excr.2000.4945 · Cited by 154 · see citing works
Senescent Stromal-Derived Osteopontin Promotes Preneoplastic Cell Growth
Pazolli, E., Luo, X., Brehm, S., Carbery, K., Chung, J.-J., Prior, J. L., Doherty, J. M., Demehri, S., Salavaggione, L., Piwnica-Worms, D. R., et al. (2009) · Cancer Research · doi:10.1158/0008-5472.can-08-2970 · Cited by 146 · see citing works
TERT promotes cellular and organismal survival independently of telomerase activity
Lee, J., Sung, Y. H., Cheong, C., Choi, Y. S., Jeon, H. K., Sun, W., Hahn, W. C., Ishikawa, F., & Lee, H.-W. (2008) · Oncogene · doi:10.1038/sj.onc.1211037 · Cited by 145 · see citing works
TPP1 Is Required for TERT Recruitment, Telomere Elongation during Nuclear Reprogramming, and Normal Skin Development in Mice
Tejera, Á. M., d’Alcontres, M. S., Thanasoula, M., Marión, R. M., Martínez, P., Liao, C., Flores, J. M., Tarsounas, M., & Blasco, M. A. (2010) · Developmental Cell · doi:10.1016/j.devcel.2010.03.011 · Cited by 144 · see citing works
Dyskeratosis Congenita - A Disease of Dysfunctional Telomere Maintenance
Mason, P., Wilson, D., & Bessler, M. (2005) · Current Molecular Medicine · doi:10.2174/1566524053586581 · Cited by 129 · see citing works
A Syndrome of Progressive Pancytopenia with Microcephaly, Cerebellar Hypoplasia and Growth Failure
Hreiðarsson, S., Kristjánsson, K., JOHANNESSON, G., & Jóhannsson, J. H. (1988) · Acta Paediatrica · doi:10.1111/j.1651-2227.1988.tb10751.x · Cited by 125 · see citing works
Comparison of Chromosome Telomere Integrity in Multiple Tissues from Subjects at Different Ages
Butler, M. G., Tilburt, J. C., DeVries, A., Muralidhar, B., Aue, G., Hedges, L. K., Atkinson, J. T., & Schwartz, H. S. (1998) · Cancer Genetics and Cytogenetics · doi:10.1016/s0165-4608(98)00029-6 · Cited by 124 · see citing works
Genomic integration of oncogenic HPV and gain of the human telomerase gene TERC at 3q26 are strongly associated events in the progression of uterine cervical dysplasia to invasive cancer
Hopman, A. H. N., Theelen, W., Hommelberg, P. P. H., Kamps, M. A. F., Herrington, C. S., Morrison, L., Speel, E. M., Smedts, F. M. M., & Ramaekers, F. C. S. (2006) · The Journal of Pathology · doi:10.1002/path.2070 · Cited by 112 · see citing works
Antagonistic effects of telomerase on cancer and aging in K5-mTert transgenic mice
González-Suárez, E., Geserick, C., Flores, J. M., & Blasco, M. A. (2005) · Oncogene · doi:10.1038/sj.onc.1208413 · Cited by 109 · see citing works
Inherited aplastic anaemias/bone marrow failure syndromes
Dokal, I. S., & Vulliamy, T. (2008) · Blood Reviews · doi:10.1016/j.blre.2007.11.003 · Cited by 109 · see citing works
Expression of Telomerase RNA Template, but Not Telomerase Reverse Transcriptase, Is Limiting for Telomere Length Maintenance In Vivo
Chiang, Y. J., Hemann, M. T., Hathcock, K. S., Tessarollo, L., Feigenbaum, L., Hahn, W. C., & Hodes, R. J. (2004) · Molecular and Cellular Biology · doi:10.1128/mcb.24.16.7024-7031.2004 · Cited by 107 · see citing works
Telomere length mediates the effects of telomerase on the cellular response to genotoxic stress
Rubio, M. Á., Davalos, A. R., & Campisi, J. (2004) · Experimental Cell Research · doi:10.1016/j.yexcr.2004.04.004 · Cited by 105 · see citing works
Functional characterization of natural telomerase mutations found in patients with hematologic disorders
Xin, Z.-T., Beauchamp, A. D., Calado, R. T., Bradford, J. W., Regal, J. A., Shenoy, A. G., Liang, Y., Lansdorp, P. M., Young, N. S., & Ly, H. (2006) · Blood · doi:10.1182/blood-2006-07-035089 · Cited by 104 · see citing works
Regulation of Telomerase and Telomeres: Human Tumor Viruses Take Control
Bellon, M., & Nicot, C. (2008) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djm269 · Cited by 103 · see citing works
Telomerase Activity and Expression of Telomerase RNA Component and Telomerase Catalytic Subunit Gene in Cervical Cancer
Nakano, K., Watney, E., & McDougall, J. K. (1998) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)65627-1 · Cited by 102 · see citing works
Dual regulation of telomerase activity through c-Myc-dependent inhibition and alternative splicing of hTERT
Cerezo, A., Kalthoff, H., Schuermann, M., Schäfer, B., & Boukamp, P. (2002) · Journal of Cell Science · doi:10.1242/jcs.115.6.1305 · Cited by 99 · see citing works
Cell type and DNA damage specific response of human skin cells to environmental agents
D’Errico, M., Lemma, T., Calcagnile, A., Santis, L. P. D., & Dogliotti, E. (2007) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/j.mrfmmm.2006.06.009 · Cited by 98 · see citing works
Dyskeratosis congenita: its link to telomerase and aplastic anaemia
Dokal, I. S., & Vulliamy, T. (2003) · Blood Reviews · doi:10.1016/s0268-960x(03)00020-1 · Cited by 96 · see citing works
Telomerase: regulation, function and transformation
Dong, C. K., Masutomi, K., & Hahn, W. C. (2005) · Critical Reviews in Oncology/Hematology · doi:10.1016/j.critrevonc.2004.12.005 · Cited by 94 · see citing works
Comparative Analysis of Telomere Lengths and Erosion with Age in Human Epidermis and Lingual Epithelium
Nakamura, K., Izumiyama‐Shimomura, N., Takubo, K., Sawabe, M., Arai, T., Aoyagi, Y., Fujiwara, M., Tsuchiya, E., Kobayashi, Y., Kato, M., et al. (2002) · Journal of Investigative Dermatology · doi:10.1046/j.1523-1747.2002.19523.x · Cited by 90 · see citing works
Telomere length of the skin in association with chronological aging and photoaging
Sugimoto, M., Yamashita, R., & Ueda, M. (2006) · Journal of Dermatological Science · doi:10.1016/j.jdermsci.2006.02.004 · Cited by 86 · see citing works
The E6 Oncoproteins from Human Betapapillomaviruses Differentially Activate Telomerase through an E6AP-Dependent Mechanism and Prolong the Lifespan of Primary Keratinocytes
Bedard, K., Underbrink, M. P., Howie, H. L., & Galloway, D. A. (2008) · Journal of Virology · doi:10.1128/jvi.01818-07 · Cited by 85 · see citing works
Telomerase is Not an Epidermal Stem Cell Marker and is Downregulated by Calcium
Bickenbach, J. R., Vormwald‐Dogan, V., Bachor, C., Bleuel, K., Schnapp, G., & Boukamp, P. (1998) · Journal of Investigative Dermatology · doi:10.1046/j.1523-1747.1998.00420.x · Cited by 81 · see citing works
Dyskeratosis congenita fibroblasts are abnormal and have unbalanced chromosomal rearrangements
Dokal, I. S., Bungey, J., Williamson, P., Oscier, D. G., Hows, J., & Luzzatto, L. (1992) · Blood · doi:10.1182/blood.v80.12.3090.3090 · Cited by 79 · see citing works
Epidermal stem cells are resistant to cellular aging
Stern, M. M., & Bickenbach, J. R. (2007) · Aging Cell · doi:10.1111/j.1474-9726.2007.00318.x · Cited by 79 · see citing works
HPV16‐E6 associated hTERT promoter acetylation is E6AP dependent, increased in later passage cells and enhanced by loss of p300
James, M. A., Lee, J. H., & Klingelhutz, A. J. (2006) · International Journal of Cancer · doi:10.1002/ijc.22064 · Cited by 75 · see citing works
Self-citation
Keratinocyte growth conditions modulate telomerase expression, senescence, and immortalization by human papillomavirus type 16 E6 and E7 oncogenes.
Fu, B., Quintero, J., & Baker, C. C. (2003) · PubMed · Cited by 74 · see citing works
Dyskeratosis congenita, telomeres and human ageing
Marciniak, R. A., Johnson, F. B., & Guarente, L. (2000) · Trends in Genetics · doi:10.1016/s0168-9525(00)01984-3 · Cited by 74 · see citing works
In Brief
(2010) · Nature Reviews Genetics · doi:10.1038/nrg2761 · Cited by 74 · see citing works
NFX1 Interacts with mSin3A/Histone Deacetylase To Repress hTERT Transcription in Keratinocytes
Xu, M., Luo, W., Elzi, D. J., Grandori, C., & Galloway, D. A. (2008) · Molecular and Cellular Biology · doi:10.1128/mcb.01969-07 · Cited by 70 · see citing works
Slow‐down of age‐dependent telomere shortening is executed in human skin keratinocytes by hormesis‐like‐effects of trace hydrogen peroxide or by anti‐oxidative effects of pro‐vitamin C in common concurrently with reduction of intracellular oxidative stress
Yokoo, S., Furumoto, K., Hiyama, E., & Miwa, N. (2004) · Journal of Cellular Biochemistry · doi:10.1002/jcb.20208 · Cited by 67 · see citing works
Telomere restoration and extension of proliferative lifespan in dyskeratosis congenita fibroblasts
Westin, E. R., Chavez, E. A., Lee, K. M., Gourronc, F. A., Riley, S., Lansdorp, P. M., Goldman, F. D., & Klingelhutz, A. J. (2007) · Aging Cell · doi:10.1111/j.1474-9726.2007.00288.x · Cited by 67 · see citing works
Self-citation
Telomerase reverses epidermal hair follicle stem cell defects and loss of long-term survival associated with critically short telomeres
Siegl-Cachedenier, I., Flores, I., Klatt, P., & Blasco, M. A. (2007) · The Journal of Cell Biology · doi:10.1083/jcb.200704141 · Cited by 64 · see citing works
Skin Aging: A Role for Telomerase and Telomere Dynamics?
Boukamp, P. (2005) · Current Molecular Medicine · doi:10.2174/1566524053586644 · Cited by 52 · see citing works
Tissue context-activated telomerase in human epidermis correlates with little age-dependent telomere loss
Krunic, D., Moshir, S., Greulich‐Bode, K. M., Figueroa, R., Cerezo, A., Stammer, H., Stark, H., Gray, S. G., Nielsen, K. V., Hartschuh, W., et al. (2009) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2009.02.005 · Cited by 40 · see citing works
Proliferative defects in dyskeratosis congenita skin keratinocytes are corrected by expression of the telomerase reverse transcriptase, TERT, or by activation of endogenous telomerase through expression of papillomavirus E6/E7 or the telomerase RNA component, TERC
Gourronc, F. A., Robertson, M. M., Herrig, A. K., Lansdorp, P. M., Goldman, F. D., & Klingelhutz, A. J. (2009) · Experimental Dermatology · doi:10.1111/j.1600-0625.2009.00916.x · Cited by 39 · see citing works
Self-citation
In Situ Hybridization Analysis of the Expression of Human Telomerase RNA in Normal and Pathologic Conditions of the Skin
Ogoshi, M., Le, T., Shay, J. W., & Taylor, R. S. (1998) · Journal of Investigative Dermatology · doi:10.1046/j.1523-1747.1998.00180.x · Cited by 36 · see citing works
Telomere shortening in cultured autografts of patients with burns
Counter, C. M., Press, W., & Compton, C. C. (2003) · The Lancet · doi:10.1016/s0140-6736(03)13042-5 · Cited by 35 · see citing works
Methylation of the p16INK4a promoter region in telomerase immortalized human keratinocytes co-cultured with feeder cells
Darbro, B., Lee, K. M., Nguyen, N., Domann, F., & Klingelhutz, A. (2006) · Oncogene · doi:10.1038/sj.onc.1209729 · Cited by 34 · see citing works
Self-citation
3q26 Amplification and Polysomy of Chromosome 3 in Squamous Cell Lesions of the Lung: A Fluorescence In situ Hybridization Study
Pelosi, G., Curto, B. D., Trubia, M., et al. (2007) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-06-2483 · Cited by 32 · see citing works
Adenoviral Human Telomerase Reverse Transcriptase Dramatically Improves Ischemic Wound Healing Without Detrimental Immune Response in an Aged Rabbit Model
Mogford, J. E., Liu, W. R., Reid, R. R., Chiu, C., Said, H. K., Chen, S.-J., Harley, C. B., & Mustoe, T. A. (2006) · Human Gene Therapy · doi:10.1089/hum.2006.17.651 · Cited by 26 · see citing works
Telomere dysfunction results in enhanced organismal sensitivity to the alkylating agent N-methyl-N-nitrosourea.
González‐Suárez, E., Goytisolo, F. A., Flores, J. M., & Blasco, M. A. (2003) · PubMed · Cited by 23 · see citing works
Genetic dissection of the mechanisms underlying telomere-associated diseases: impact of the TRF2 telomeric protein on mouse epidermal stem cells
Stout, G. J., & Blasco, M. A. (2009) · Disease Models & Mechanisms · doi:10.1242/dmm.002121 · Cited by 21 · see citing works
Late manifestation of dyskeratosis congenita presenting as chronic dermal ulcer in a 37‐year‐old man
Reimann, C., Kloeckener‐Gruissem, B., Niemeyer, C. M., & Vanscheidt, W. (2008) · Journal of the European Academy of Dermatology and Venereology · doi:10.1111/j.1468-3083.2007.02530.x · Cited by 14 · see citing works
The effect of the long-term cultivation on telomere length and morphology of cultured epidermis
Miyata, Y., Okada, K., Fujimoto, A., Hata, K., Kagami, H., Tomita, Y., & Ueda, M. (2004) · Journal of Dermatological Science · doi:10.1016/j.jdermsci.2004.02.004 · Cited by 11 · see citing works
The role of telomerase activity in psoriatic skin lesions
Jurišić, D., Kirin, I., Rabic, D., Dojčinović, B., Čoklo, M., & Zamolo, G. (2006) · Medical Hypotheses · doi:10.1016/j.mehy.2006.09.037 · Cited by 5 · see citing works
Telomerase activity in human germline and embryonic tissues and cells
Wright, W. E., Piatyszek, M. A., Rainey, W. E., Byrd, W., & Shay, J. W. (1996) · Developmental Genetics · doi:10.1002/(sici)1520-6408(1996)18:2

Flagged first, then by citations

Research works printed but not linked: 3

[24]Yasumoto S Kunimura C Kikuchi K Oncogene 1996 13 433 439 8710384
[80]Fu B Quintero J Baker CC Cancer Res 2003 63 7815 7824 14633708
[115]Gonzalez-Suarez E Goytisolo FA Flores JM Cancer Res 2003 63 7047 7050 14612493

Sorted by citations

Fighting against Skin Aging: The Way from Bench to Bedside
Zhang, S., & Duan, E. (2018) · Cell Transplantation · doi:10.1177/0963689717725755 · Cited by 739 · see citing works
Aging of the cells: Insight into cellular senescence and detection Methods.
Mohamad Kamal, N. S., Safuan, S., Shamsuddin, S., & Foroozandeh, P. (2020) · European Journal of Cell Biology · doi:10.1016/j.ejcb.2020.151108 · Cited by 287 · see citing works
Diet and Skin Aging—From the Perspective of Food Nutrition
Cao, C., Xiao, Z., Wu, Y., & Ge, C. (2020) · Nutrients · doi:10.3390/nu12030870 · Cited by 231 · see citing works
Unravelling UVA-induced mutagenesis
Sage, E., Girard, P.-M., & Francesconi, S. (2012) · Photochemical & Photobiological Sciences · doi:10.1039/c1pp05219e · Cited by 167 · see citing works
Boosting the Photoaged Skin: The Potential Role of Dietary Components
Geng, R., Kang, S.-G., Huang, K., & Tong, T. (2021) · Nutrients · doi:10.3390/nu13051691 · Cited by 116 · see citing works
The Impact of Sunlight on Skin Aging
Kaddurah, H., Braunberger, T. L., Vellaichamy, G., Nahhas, A. F., Lim, H. W., & Hamzavi, I. H. (2018) · Current Geriatrics Reports · doi:10.1007/s13670-018-0262-0 · Cited by 11 · see citing works

[Relationship between telomere length and clinical and biological characteristics of the cancers with telomerase reactivation].
Hiyama, E., Yokoyama, T., Hiyama, K., et al. (1998) · PubMed · Cited by 3 · see citing works
Effects of reconstitution of telomerase activity on telomere maintenance by the alternative lengthening of telomeres (ALT) pathway
Grobelny, J. V. (2001) · Human Molecular Genetics · doi:10.1093/hmg/10.18.1953 · Cited by 89 · see citing works
Immortalized cells with no detectable telomerase activity. A review.
Reddel, R. R., Bryan, T. M., & Murnane, J. P. (1997) · PubMed · Cited by 91 · see citing works
Telomere Length Dynamics in Telomerase-Positive Immortal Human Cell Populations
Bryan, T. M., Englezou, A., Dunham, M. A., & Reddel, R. R. (1998) · Experimental Cell Research · doi:10.1006/excr.1997.3907 · Cited by 104 · see citing works
Telomere maintenance and cancer ? look, no telomerase
Neumann, A. A., & Reddel, R. R. (2002) · Nature reviews. Cancer · doi:10.1038/nrc929 · Cited by 148 · see citing works

Authors: Buckingham, E. M., & Klingelhutz, A. J.
Affiliations: University of Iowa (US)
Corresponding author: Klingelhutz, Aloysius J.
ORCID: Klingelhutz, Aloysius J.
Venue: Experimental Dermatology
Publisher: Wiley
Published: 2011-03-03
Volume: 20
Issue: 4
Pages: 297-302
ISSN: 0906-6705 (ISSN-L)
DOI: 10.1111/j.1600-0625.2010.01242.x
PMC: PMC3690281
OpenAlex: W1500703123
Cited by: 109
References: 120
Citations by year: 2026: 4 · 2025: 13 · 2024: 11 · 2023: 4 · 2022: 9 · 2021: 10 · 2020: 10 · 2019: 7 · 2018: 5 · 2017: 4 · 2016: 7 · 2015: 4 · 2014: 6 · 2013: 1 · 2012: 10
FWCI: 0.72
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: doi.wiley.com/10.1002/tdm_license_1.1 (tdm, 1643 d)
Locations: Experimental Dermatology (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Institute on Aging (R01AG027388, R01AG27388)
Topics: Health Sciences › Medicine › Physiology › Telomeres, Telomerase, and Senescence
Health Sciences › Medicine › Dermatology › Skin Protection and Aging
Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
Keywords: telomeres, skin aging, telomere shortening, cellular senescence, telomerase, epidermal stem cells, dyskeratosis congenita, reactive oxygen species, DNA damage, epidermis, dermis, skin diseases
MeSH terms: Animals, Humans, Skin, Skin Aging, Telomere, Oxidative Stress, Telomerase

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

The role of telomeres in the ageing of human skin: Telomeres and skin ageing

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Self-check

Cites

Cited by

Related

Record

About these checks