Extension of Cell Life-Span and Telomere Length in Animals Cloned from Senescent Somatic Cells
Abstract
The potential of cloning depends in part on whether the procedure can reverse cellular aging and restore somatic cells to a phenotypically youthful state. Here, we report the birth of six healthy cloned calves derived from populations of senescent donor somatic cells. Nuclear transfer extended the replicative life-span of senescent cells (zero to four population doublings remaining) to greater than 90 population doublings. Early population doubling level complementary DNA-1 (EPC-1, an age-dependent gene) expression in cells from the cloned animals was 3.5- to 5-fold higher than that in cells from age-matched (5 to 10 months old) controls. Southern blot and flow cytometric analyses indicated that the telomeres were also extended beyond those of newborn (<2 weeks old) and age-matched control animals. The ability to regenerate animals and cells may have important implications for medicine and the study of mammalian aging.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
Cloning from senescent fibroblasts of old cows produced calves whose fibroblasts had regained population doubling and better telomere maintenance than age-matched controls.
“Somatic cell nuclear transfer of senescent fibroblasts from aged bovine donors results in cloned calves with fibroblasts that have restored population doubling and increased telomere maintenance compared to age-matched control animals180.”
From Stem cell aging: mechanisms, regulators and therapeutic opportunities (2014) · cites this paper as [180]
Cites
Single-Step Method of RNA Isolation by Acid Guanidinium Thiocyanate–Phenol–Chloroform Extraction
Chomczynski, P., & Sacchi, N. (1987) · Analytical Biochemistry · doi:10.1006/abio.1987.9999 · Cited by 65,240 · see citing works
Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction
Chomczyński, P., & Sacchi, N. (1987) · Analytical Biochemistry · doi:10.1016/0003-2697(87)90021-2 · Cited by 47,092 · see citing works
The serial cultivation of human diploid cell strains
Hayflick, L., & Moorhead, P. S. (1961) · Experimental Cell Research · doi:10.1016/0014-4827(61)90192-6 · Cited by 8,508 · see citing works
A biomarker that identifies senescent human cells in culture and in aging skin in vivo.
Dimri, G. P., Lee, X., Basile, G., Acosta, M., Scott, G., Roskelley, C., Medrano, E. E., Linskens, M., Rubelj, I., & Pereira-Smith, O. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.20.9363 · Cited by 7,477 · see citing works
The limited in vitro lifetime of human diploid cell strains
Hayflick, L. (1965) · Experimental Cell Research · doi:10.1016/0014-4827(65)90211-9 · Cited by 5,876 · see citing works
Telomeres shorten during ageing of human fibroblasts
Harley, C. B., Futcher, A. B., & Greider, C. W. (1990) · Nature · doi:10.1038/345458a0 · Cited by 5,750 · see citing works
Viable offspring derived from fetal and adult mammalian cells
Wilmut, I., Schnieke, A., McWhir, J., Kind, A., & Campbell, K. (1997) · Nature · doi:10.1038/385810a0 · Cited by 4,976 · 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
Full-term development of mice from enucleated oocytes injected with cumulus cell nuclei
Wakayama, T., Perry, A. C. F., Zuccotti, M., Johnson, K. R., & Yanagimachi, R. (1998) · Nature · doi:10.1038/28615 · Cited by 2,250 · see citing works
Telomere length predicts replicative capacity of human fibroblasts.
Allsopp, R. C., Vaziri, H., Patterson, C., Goldstein, S., Younglai, E. V., Futcher, A. B., Greider, C. W., & Harley, C. B. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.21.10114 · Cited by 2,200 · see citing works
Cloned Transgenic Calves Produced from Nonquiescent Fetal Fibroblasts
Cibelli, J. B., Stice, S. L., Golueke, P. J., Kane, J. J., Jerry, J., Blackwell, C., de León, F. A. P., & Robl, J. M. (1998) · Science · doi:10.1126/science.280.5367.1256 · Cited by 1,396 · see citing works
Self-citationKiyono, 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
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
Eight Calves Cloned from Somatic Cells of a Single Adult
Kato, Y., Tani, T., Sotomaru, Y., Kurokawa, K., Kato, J.-Y., Doguchi, H., Yasue, H., & Tsunoda, Y. (1998) · Science · doi:10.1126/science.282.5396.2095 · Cited by 1,055 · see citing works
Vaziri, H., & Benchimol, S. (1998) · Current Biology · doi:10.1016/s0960-9822(98)70109-5 · Cited by 1,003 · see citing works
Production of goats by somatic cell nuclear transfer
Baguisi, A. B., Behboodi, E., Melican, D. T., Pollock, J. S., Destrempes, M. M., Cammuso, C., Williams, J. L., Nims, S., Porter, C. A., Midura, P., et al. (1999) · Nature Biotechnology · doi:10.1038/8632 · Cited by 999 · see citing works
Control of Human Telomere Length by TRF1 and TRF2
Smogorzewska, A., van Steensel, B., Bianchi, A., Oelmann, S., Schaefer, M. R., Schnapp, G., & de Lange, T. (2000) · Molecular and Cellular Biology · doi:10.1128/mcb.20.5.1659-1668.2000 · Cited by 768 · see citing works
Rufer, N., Brümmendorf, T. H., Kolvraa, S., Bischoff, C., Christensen, K., Wadsworth, L., Schulzer, M., & Lansdorp, P. M. (1999) · The Journal of Experimental Medicine · doi:10.1084/jem.190.2.157 · Cited by 709 · see citing works
Self-citationTelomere length dynamics in human lymphocyte subpopulations measured by flow cytometry
Rufer, N., Dragowska, W. H., Thornbury, G., Roosnek, E. E., & Lansdorp, P. M. (1998) · Nature Biotechnology · doi:10.1038/nbt0898-743 · Cited by 547 · see citing works
Self-citationCellular senescence and DNA synthesis
Cristofalo, V. J., & Sharf, B. B. (1973) · Experimental Cell Research · doi:10.1016/0014-4827(73)90394-7 · Cited by 537 · see citing works
Self-citationSix cloned calves produced from adult fibroblast cells after long-term culture
Kubota, C., Yamakuchi, H., Todoroki, J., Mizoshita, K., Tabara, N., Barber, M. R., & Yang, X. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.3.990 · Cited by 487 · see citing works
Evidence for a Critical Telomere Length in Senescent Human Fibroblasts
Allsopp, R., & Harley, C. B. (1995) · Experimental Cell Research · doi:10.1006/excr.1995.1213 · Cited by 391 · see citing works
Clinical and pathologic features of cloned transgenic calves and fetuses (13 case studies)
Hill, J. R., Roussel, A. J., Cibelli, J. B., Edwards, J. F., Hooper, N. L., Miller, M. W., Thompson, J. A., Looney, C. R., Westhusin, M. E., Robl, J. M., et al. (1999) · Theriogenology · doi:10.1016/s0093-691x(99)00089-8 · Cited by 385 · see citing works
Self-citationVaziri, H., West, M. D., Allsopp, R., Davison, T. S., Wu, Y., Arrowsmith, C. H., Poirier, G. G., & Benchimol, S. (1997) · The EMBO Journal · doi:10.1093/emboj/16.19.6018 · Cited by 384 · see citing works
Self-citationAnalysis of telomere lengths in cloned sheep
Shiels, P. G., Kind, A., Campbell, K., Waddington, D., Wilmut, I., Colman, A., & Schnieke, A. (1999) · Nature · doi:10.1038/20580 · Cited by 350 · see citing works
Replicative senescence of human fibroblast-like cells in culture
Cristofalo, V. J., & Pignolo, R. J. (1993) · Physiological Reviews · doi:10.1152/physrev.1993.73.3.617 · Cited by 286 · see citing works
Self-citationLymphoid hypoplasia and somatic cloning
Renard, J. P. J. P., Chastant‐Maillard, S., Chesné, P., Richard, C., Marchal, J., Cordonnier, N., Chavatte‐Palmer, P., & Vignon, X. (1999) · The Lancet · doi:10.1016/s0140-6736(98)12173-6 · Cited by 254 · see citing works
West, M. D., Pereira‐Smith, O. M., & Smith, J. R. (1989) · Experimental Cell Research · doi:10.1016/0014-4827(89)90372-8 · Cited by 242 · see citing works
Self-citationRhesus Monkeys Produced by Nuclear Transfer1
Li, M., Ely, J. J., Stouffer, R. L., & Wolf, D. P. (1997) · Biology of Reproduction · doi:10.1095/biolreprod57.2.454 · Cited by 239 · see citing works
Ultrastructural changes accompanying the aging of human diploid cells in culture
Lipetz, J., & Cristofalo, V. J. (1972) · Journal of Ultrastructure Research · doi:10.1016/s0022-5320(72)80005-4 · Cited by 178 · see citing works
Self-citationLanza, R., Cibelli, J. B., & West, M. D. (1999) · Nature Medicine · doi:10.1038/12404 · Cited by 156 · see citing works
Self-citationProspects for the use of nuclear transfer in human transplantation
Lanza, R., Cibelli, J. B., & West, M. D. (1999) · Nature Biotechnology · doi:10.1038/70709 · Cited by 143 · see citing works
Self-citationThe cellular and molecular biology of skin aging.
West, M. D. (1994) · PubMed · Cited by 130 · see citing works
Self-citationPignolo, R. J., Cristofalo, V. J., & Rotenberg, M. O. (1993) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)52964-1 · Cited by 126 · see citing works
Self-citationGalli, C., Duchi, R., Moor, R. M., & Lazzari, G. (1999) · Cloning · doi:10.1089/15204559950019924 · Cited by 117 · see citing works
The Cellular and Molecular Biology of Skin Aging
West, M. D. (1994) · Archives of Dermatology · doi:10.1001/archderm.1994.01690010091014 · Cited by 107 · see citing works
Self-citationWest, M. D., Shay, J. W., Wright, W. E., & Linskens, M. H. K. (1996) · Experimental Gerontology · doi:10.1016/0531-5565(95)02013-6 · Cited by 94 · see citing works
Self-citationUnlimited Mileage from Telomerase?
de Lange, T., & DePinho, R. A. (1999) · Science · doi:10.1126/science.283.5404.947 · Cited by 71 · see citing works
Aging and Cellular Defense Mechanisms
Giacomoni, P. U. (1992) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1992.tb38642.x · Cited by 59 · see citing works
Molecular markers of senescence in fibroblast-like cultures
Cristofalo, V. J., & Pignolo, R. J. (1996) · Experimental Gerontology · doi:10.1016/0531-5565(95)02018-7 · Cited by 59 · see citing works
Self-citationPignolo, R. J., Martin, B. G., Horton, J. H., Kalbach, A., & Cristofalo, V. J. (1998) · Experimental Gerontology · doi:10.1016/s0531-5565(97)00090-9 · Cited by 46 · see citing works
Self-citationGorman, S. D., & Cristofalo, V. J. (1986) · Experimental Cell Research · doi:10.1016/0014-4827(86)90206-5 · Cited by 34 · see citing works
Self-citationMolecular Changes with in Vitro Cellular Senescence
Cristofalo, V. J., Pignolo, R. J., & Rotenberg, M. O. (1992) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1992.tb38662.x · Cited by 19 · see citing works
Self-citationPhinney, D. G., Keiper, C. L., Francis, M. K., & Ryder, K. (1994) · PubMed · Cited by 17 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Jaenisch, R., & Bird, A. (2003) · Nature Genetics · doi:10.1038/ng1089 · Cited by 6,325 · see citing works
Genomic imprinting: parental influence on the genome
Reik, W., & Walter, J. (2001) · Nature Reviews Genetics · doi:10.1038/35047554 · Cited by 2,288 · see citing works
Switching and Signaling at the Telomere
Blackburn, E. H. (2001) · Cell · doi:10.1016/s0092-8674(01)00492-5 · Cited by 2,097 · see citing works
Telomeres and human disease: ageing, cancer and beyond
Blasco, M. A. (2005) · Nature Reviews Genetics · doi:10.1038/nrg1656 · Cited by 1,690 · see citing works
Aubert, G., & Lansdorp, P. M. (2008) · Physiological Reviews · doi:10.1152/physrev.00026.2007 · Cited by 1,188 · see citing works
Self-citationHuman Telomerase and Its Regulation
Cong, Y.-S., Wright, W. E., & Shay, J. W. (2002) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.66.3.407-425.2002 · Cited by 898 · see citing works
Stem cell aging: mechanisms, regulators and therapeutic opportunities
Oh, J., Lee, Y. D., & Wagers, A. J. (2014) · Nature Medicine · doi:10.1038/nm.3651 · Cited by 796 · see citing works
Hayflick, his limit, and cellular ageing
Shay, J. W., & Wright, W. E. (2000) · Nature Reviews Molecular Cell Biology · doi:10.1038/35036093 · Cited by 764 · see citing works
Nuclear Cloning and Epigenetic Reprogramming of the Genome
Rideout, W. M., Eggan, K. C., & Jaenisch, R. (2001) · Science · doi:10.1126/science.1063206 · Cited by 756 · see citing works
Eggan, K. C., Akutsu, H., Loring, J. M., Jackson‐Grusby, L., Klemm, M., Rideout, W. M., Yanagimachi, R., & Jaenisch, R. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.101118898 · Cited by 613 · see citing works
Rejuvenating senescent and centenarian human cells by reprogramming through the pluripotent state
Lapasset, L., Milhavet, O., Prieur, A., Besnard, E., Babled, A., Aït-Hamou, N., Leschik, J., Pellestor, F., Ramirez, J.-M., De Vos, J., et al. (2011) · Genes & Development · doi:10.1101/gad.173922.111 · Cited by 570 · see citing works
García‐Cao, M., O’Sullivan, R. J., Peters, A. H. F. M., Jenuwein, T., & Blasco, M. A. (2003) · Nature Genetics · doi:10.1038/ng1278 · Cited by 557 · see citing works
Telomeres Acquire Embryonic Stem Cell Characteristics in Induced Pluripotent Stem Cells
Marión, R. M., Strati, K., Li, H., Tejera, Á. M., Schoeftner, S., Ortega, S., Serrano, M., & Blasco, M. A. (2009) · Cell stem cell · doi:10.1016/j.stem.2008.12.010 · Cited by 509 · see citing works
Gomes, N. M. V., Ryder, O. A., Houck, M. L., Charter, S. J., Walker, W., Forsyth, N. R., Austad, S. N., Venditti, C., Pagel, M., Shay, J. W., et al. (2011) · Aging Cell · doi:10.1111/j.1474-9726.2011.00718.x · Cited by 464 · see citing works
Production of cloned pigs from in vitro systems
Betthauser, J., Forsberg, E., Augenstein, M. L., Childs, L. A., Eilertsen, K. J., Enos, J. M., Forsythe, T. M., Golueke, P. J., Jurgella, G., Koppang, R. W., et al. (2000) · Nature Biotechnology · doi:10.1038/80242 · Cited by 489 · see citing works
Reprogramming of genome function through epigenetic inheritance
Surani, M. A. (2001) · Nature · doi:10.1038/35102186 · Cited by 453 · see citing works
Telomere lengthening early in development
Liu, L., Bailey, S. M., Okuka, M., Muñoz, P., Li, C., Zhou, L., Wu, C., Czerwiec, E., Sandler, L., Seyfang, A., et al. (2007) · Nature Cell Biology · doi:10.1038/ncb1664 · Cited by 396 · see citing works
The presence, role and clinical use of spermatozoal RNAs
Jodar, M., Selvaraju, S., Sendler, E. D., Diamond, M. P., Krawetz, S. A., & for the Reproductive Medicine Network (2013) · Human Reproduction Update · doi:10.1093/humupd/dmt031 · Cited by 371 · see citing works
PEDF: a multifaceted neurotrophic factor
Tombran‐Tink, J., & Barnstable, C. J. (2003) · Nature reviews. Neuroscience · doi:10.1038/nrn1176 · Cited by 369 · see citing works
Cloned mice have an obese phenotype not transmitted to their offspring
Tamashiro, K. L., Wakayama, T., Akutsu, H., Yamazaki, Y., Lachey, J. L., Wortman, M. D., Seeley, R. J., D’Alessio, D. A., Woods, S. C., Yanagimachi, R., et al. (2002) · Nature Medicine · doi:10.1038/nm0302-262 · Cited by 356 · see citing works
Nuclear Transplantation, Embryonic Stem Cells, and the Potential for Cell Therapy
Hochedlinger, K., & Jaenisch, R. (2003) · New England Journal of Medicine · doi:10.1056/nejmra035397 · Cited by 322 · see citing works
Genes involved in senescence and immortalization
Lundberg, A. S., Hahn, W. C., Gupta, P., & Weinberg, R. A. (2000) · Current Opinion in Cell Biology · doi:10.1016/s0955-0674(00)00155-1 · Cited by 313 · see citing works
Nuclear Transfer Protocol Affects Messenger RNA Expression Patterns in Cloned Bovine Blastocysts
Wrenzycki, C., Wells, D. N., Herrmann, D., Miller, A. L., Oliver, J. E., Tervit, R., & Niemann, H. J. (2001) · Biology of Reproduction · doi:10.1095/biolreprod65.1.309 · Cited by 290 · see citing works
Replicative senescence: a critical review
Cristofalo, V. J., Lorenzini, A., Allen, R. G., Torres, C. A., & Tresini, M. (2004) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2004.07.010 · Cited by 275 · see citing works
Self-citationDeletion of the α(1,3)galactosyl transferase (GGTA1) gene and the prion protein (PrP) gene in sheep
Denning, C. N., Burl, S., Ainslie, A., Bracken, J., Dinnyés, A., Fletcher, J. M., King, T., Ritchie, M., Ritchie, W. A., Rollo, M., et al. (2001) · Nature Biotechnology · doi:10.1038/89313 · Cited by 273 · see citing works
From cells to organisms: can we learn about aging from cells in culture?
Campisi, J. (2001) · Experimental Gerontology · doi:10.1016/s0531-5565(00)00230-8 · Cited by 263 · see citing works
Mammalian cloning: advances and limitations
Solter, D. (2000) · Nature Reviews Genetics · doi:10.1038/35042066 · Cited by 249 · see citing works
Antioxidants, reactive oxygen and nitrogen species, gene induction and mitochondrial function
Jackson, M. J. (2002) · Molecular Aspects of Medicine · doi:10.1016/s0098-2997(02)00018-3 · Cited by 238 · see citing works
Barnstable, C. J. (2004) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2004.05.002 · Cited by 240 · see citing works
Site-Specific DNA Damage at the GGG Sequence by UVA Involves Acceleration of Telomere Shortening
Oikawa, S., Tada‐Oikawa, S., & Kawanishi, S. (2001) · Biochemistry · doi:10.1021/bi002721g · Cited by 238 · see citing works
Cloning of mice to six generations
Wakayama, T., Shinkai, Y., Tamashiro, K. L., Niida, H., Blanchard, D. C., Blanchard, R. J., Ogura, A., Tanemura, K., Tachibana, M., Perry, A. C. F., et al. (2000) · Nature · doi:10.1038/35030301 · Cited by 228 · see citing works
Mediators of reprogramming: transcription factors and transitions through mitosis
Egli, D. M., Birkhoff, G., & Eggan, K. C. (2008) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2439 · Cited by 225 · see citing works
DNA methylation variation in cloned mice
Ohgane, J., Wakayama, T., Kogo, Y., Senda, S., Hattori, N., Tanaka, S., Yanagimachi, R., & Shiota, K. (2001) · genesis · doi:10.1002/gene.1031 · Cited by 219 · see citing works
Telomere length is reset during early mammalian embryogenesis
Schaetzlein, S., Lucas‐Hahn, A., Lemme, E., Kues, W. A., Dorsch, M. M., Manns, M. P., Niemann, H., & Rudolph, K. L. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0402400101 · Cited by 219 · see citing works
A ‘higher order’ of telomere regulation: telomere heterochromatin and telomeric RNAs
Schoeftner, S., & Blasco, M. A. (2009) · The EMBO Journal · doi:10.1038/emboj.2009.197 · Cited by 214 · see citing works
The effects of PEDF on cancer biology: mechanisms of action and therapeutic potential
Becerra, S. P., & Notario, V. (2013) · Nature reviews. Cancer · doi:10.1038/nrc3484 · Cited by 211 · see citing works
Kang, Y., Park, J. S., Koo, D., Choi, Y., Kim, S., Lee, K., & Han, Y. (2002) · The EMBO Journal · doi:10.1093/emboj/21.5.1092 · Cited by 202 · see citing works
Koo, D., Kang, Y., Choi, Y., Park, J. S., Kim, H.-N., Oh, K. B., Son, D., Park, H., Lee, K.-K., & Han, Y. (2002) · Biology of Reproduction · doi:10.1095/biolreprod67.2.487 · Cited by 201 · see citing works
Epigenetic marks by DNA methylation specific to stem, germ and somatic cells in mice
Shiota, K., Kogo, Y., Ohgane, J., Imamura, T., Urano, A., Nishino, K., Tanaka, S., & Hattori, N. (2002) · Genes to Cells · doi:10.1046/j.1365-2443.2002.00574.x · Cited by 196 · see citing works
The first half-century of nuclear transplantation
Gurdon, J. B., & Byrne, J. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1337135100 · Cited by 189 · see citing works
Programming and Reprogramming Cellular Age in the Era of Induced Pluripotency
Studer, L., Vera, E., & Cornacchia, D. (2015) · Cell stem cell · doi:10.1016/j.stem.2015.05.004 · Cited by 186 · see citing works
The essential mechanisms of aging: Irreparable damage accumulation of biochemical side-reactions
Yin, D., & Chen, K. (2005) · Experimental Gerontology · doi:10.1016/j.exger.2005.03.012 · Cited by 186 · see citing works
Somatic cell nuclear transfer: Past, present and future perspectives
Campbell, K., Fisher, P., Chen, W., Choi, I., Kelly, R. D., Lee, J., & Xhu, J. (2007) · Theriogenology · doi:10.1016/j.theriogenology.2007.05.059 · Cited by 184 · see citing works
Normal telomere lengths found in cloned cattle
Tian, X. C., Xu, J., & Yang, X. (2000) · Nature Genetics · doi:10.1038/81559 · Cited by 183 · see citing works
Cloned Cattle Can Be Healthy and Normal
Lanza, R., Cibelli, J. B., Faber, D., Sweeney, R. W., Henderson, B., Nevala, W. K., West, M. D., & Wettstein, P. J. (2001) · Science · doi:10.1126/science.1063440 · Cited by 183 · see citing works
Self-citationRufer, N., Migliaccio, M., Antonchuk, J., Humphries, R. K., Roosnek, E. E., & Lansdorp, P. M. (2001) · Blood · doi:10.1182/blood.v98.3.597 · Cited by 180 · see citing works
Self-citationThe contribution of farm animals to human health
Kues, W. A. (2004) · Trends in biotechnology · doi:10.1016/j.tibtech.2004.04.003 · Cited by 208 · see citing works
Enhanced Survivability of Cloned Calves Derived from Roscovitine-Treated Adult Somatic Cells
Gibbons, J. R., Arat, S., Rzucidlo, J., Miyoshi, K., Waltenburg, R., Respess, D. S., Venable, A., & Stice, S. L. (2002) · Biology of Reproduction · doi:10.1095/biolreprod66.4.895 · Cited by 164 · see citing works
Reprogramming of telomerase activity and rebuilding of telomere length in cloned cattle
Betts, D. H., Bordignon, V., Hill, J. R., Winger, Q. A., Westhusin, M. E., Smith, L. C., & King, W. A. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.98.3.1077 · Cited by 176 · see citing works
Human embryonic stem cell research: ethical and legal issues
Robertson, J. A. (2001) · Nature Reviews Genetics · doi:10.1038/35047594 · Cited by 158 · see citing works
Producing proteins in transgenic plants and animals
Larrick, J. W., & Thomas, D. W. (2001) · Current Opinion in Biotechnology · doi:10.1016/s0958-1669(00)00236-6 · Cited by 158 · see citing works
Lanza, R., Cibelli, J. B., & West, M. D. (1999) · Nature Medicine · doi:10.1038/12404 · Cited by 156 · see citing works
Self-citationTelomere instability in the male germline
Baird, D. M., Britt‐Compton, B., Rowson, J., Amso, N. N., Gregory, L., & Kipling, D. (2005) · Human Molecular Genetics · doi:10.1093/hmg/ddi424 · Cited by 152 · see citing works
Baerlocher, G. M., Mak, J., Tien, T., & Lansdorp, P. M. (2002) · Cytometry · doi:10.1002/cyto.10053 · Cited by 156 · see citing works
Self-citationGarbage catastrophe theory of aging: imperfect removal of oxidative damage?
Terman, A. (2001) · Redox Report · doi:10.1179/135100001101535996 · Cited by 151 · see citing works
Mice with bad ends: mouse models for the study of telomeres and telomerase in cancer and aging
Blasco, M. A. (2005) · The EMBO Journal · doi:10.1038/sj.emboj.7600598 · Cited by 147 · see citing works
DNA methylation profiles of CpG islands for cellular differentiation and development in mammals
Shiota, K. (2004) · Cytogenetic and Genome Research · doi:10.1159/000078205 · Cited by 146 · see citing works
Nuclear Transfer to Eggs and OocytesPreprint
Gurdon, J. B., & Wilmut, I. (2011) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a002659 · Cited by 144 · see citing works
Cumulative stress in research animals: Telomere attrition as a biomarker in a welfare context?
Melissa Bateson, B. (2015) · BioEssays · doi:10.1002/bies.201500127 · Cited by 140 · see citing works
Epigenetic reprogramming in mammalian nuclear transfer
Shi, W., Zakhartchenko, V., & Wolf, E. (2003) · Differentiation · doi:10.1046/j.1432-0436.2003.710201.x · Cited by 138 · see citing works
Remarkable Differences in Telomere Lengths among Cloned Cattle Derived from Different Cell Types1
Miyashita, N., Shiga, K., YONAI, M., Kaneyama, K., Kobayashi, S., Kojima, T., Goto, Y., Kishi, M., Aso, H., Suzuki, T., et al. (2002) · Biology of Reproduction · doi:10.1095/biolreprod66.6.1649 · Cited by 136 · see citing works
Telomere biology in mammalian germ cells and during development
Bekaert, S., Derradji, H., & Baatout, S. (2004) · Developmental Biology · doi:10.1016/j.ydbio.2004.06.023 · Cited by 129 · see citing works
Cellular reprogramming and epigenetic rejuvenation
Simpson, D. J., Olova, N. N., & Chandra, T. (2021) · Clinical Epigenetics · doi:10.1186/s13148-021-01158-7 · Cited by 123 · see citing works
PAX6 expression identifies progenitor cells for corneal keratocytes
Funderburgh, M. L., Du, Y., Mann, M. M., SundarRaj, N., & Funderburgh, J. L. (2005) · The FASEB Journal · doi:10.1096/fj.04-2770fje · Cited by 127 · see citing works
Generation of cloned calves and transgenic chimeric embryos from bovine embryonic stem-like cells
Saito, S., Sawai, K., Ugai, H., Moriyasu, S., MINAMIHASHI, A., Yamamoto, Y., Hirayama, H., KAGEYAMA, S., Pan, J., Murata, T., et al. (2003) · Biochemical and Biophysical Research Communications · doi:10.1016/s0006-291x(03)01536-5 · Cited by 123 · see citing works
Nuclear reprogramming of cloned embryos produced in vitro
Han, Y., Kang, Y. K., Koo, D., & Lee, K. K. (2002) · Theriogenology · doi:10.1016/s0093-691x(02)01271-2 · Cited by 123 · see citing works
Nuclear transplantation: lessons from frogs and mice
Hochedlinger, K., & Jaenisch, R. (2002) · Current Opinion in Cell Biology · doi:10.1016/s0955-0674(02)00380-0 · Cited by 123 · see citing works
Whitworth, K. M., & Prather, R. S. (2010) · Molecular Reproduction and Development · doi:10.1002/mrd.21242 · Cited by 121 · see citing works
Meissner, A., & Jaenisch, R. (2006) · Developmental Dynamics · doi:10.1002/dvdy.20915 · Cited by 121 · see citing works
Telomere Dynamics in Human Cells Reprogrammed to Pluripotency
Suhr, S. T., Chang, E. A., Rodríguez, R. M. A., Wang, K., Ross, P. J., Beyhan, Z., Murthy, S., & Cibelli, J. B. (2009) · PLoS ONE · doi:10.1371/journal.pone.0008124 · Cited by 121 · see citing works
Self-citationTelomere length measurements in leukocyte subsets by automated multicolor flow‐FISH
Baerlocher, G. M., & Lansdorp, P. M. (2003) · Cytometry Part A · doi:10.1002/cyto.a.10064 · Cited by 112 · see citing works
Self-citationDonor Cells for Nuclear Cloning: Many Are Called, but Few Are Chosen
Oback, B. J., & Wells, D. N. (2002) · Cloning and Stem Cells · doi:10.1089/153623002320253328 · Cited by 111 · see citing works
Hao, Y., Lai, L., Mao, J., Im, G., Bonk, A., & Prather, R. S. (2003) · Biology of Reproduction · doi:10.1095/biolreprod.103.016170 · Cited by 110 · see citing works
Therapeutic prospects for PEDF: more than a promising angiogenesis inhibitor
Tombran‐Tink, J., & Barnstable, C. J. (2003) · Trends in Molecular Medicine · doi:10.1016/s1471-4914(03)00074-1 · Cited by 109 · see citing works
Cloning endangered gray wolves (Canis lupus) from somatic cells collected postmortem
Oh, H. J., Kim, M., Jang, G., Kim, H. J., Hong, S. G., Park, J. E., Park, K., Park, C., Sohn, S. H., Kim, D. Y., et al. (2008) · Theriogenology · doi:10.1016/j.theriogenology.2008.04.032 · Cited by 109 · see citing works
Kasinathan, P., Knott, J. G., Moreira, P. N., Burnside, A., Jerry, D. J., & Robl, J. M. (2001) · Biology of Reproduction · doi:10.1095/biolreprod64.5.1487 · Cited by 108 · see citing works
Regeneration of the Infarcted Heart With Stem Cells Derived by Nuclear Transplantation
Lanza, R., Moore, M. A. S., Wakayama, T., Perry, A. C. F., Shieh, J.-H., Hendrikx, J., Leri, A., Chimenti, S., Monsen, A., Nurzyńska, D., et al. (2004) · Circulation Research · doi:10.1161/01.res.0000120863.53562.df · Cited by 103 · see citing works
Self-citationWeinstein, B. S., & Ciszek, D. (2002) · Experimental Gerontology · doi:10.1016/s0531-5565(02)00012-8 · Cited by 100 · see citing works
Estimating human hematopoietic stem cell kinetics using granulocyte telomere lengths
Shepherd, B. E., Guttorp, P. M., Lansdorp, P. M., & Abkowitz, J. L. (2004) · Experimental Hematology · doi:10.1016/j.exphem.2004.07.023 · Cited by 98 · see citing works
Self-citationNuclear Cloning, Stem Cells, and Genomic Reprogramming
Jaenisch, R., Eggan, K. C., Humpherys, D., Rideout, W. M., & Hochedlinger, K. (2002) · Cloning and Stem Cells · doi:10.1089/153623002321025069 · Cited by 100 · see citing works
Animal transgenesis: state of the art and applications
Melo, E. O., Canavessi, Á. M. O., Franco, M. M., & Rumpf, R. (2007) · Journal of Applied Genetics · doi:10.1007/bf03194657 · Cited by 95 · see citing works
Recent progress and problems in animal cloning
Tsunoda, Y., & Kato, Y. (2002) · Differentiation · doi:10.1046/j.1432-0436.2002.690405.x · Cited by 98 · see citing works
Ohgane, J., Wakayama, T., Senda, S., Yamazaki, Y., Inoue, K., Ogura, A., Marh, J., Tanaka, S., Yanagimachi, R., & Shiota, K. (2004) · Genes to Cells · doi:10.1111/j.1356-9597.2004.00720.x · Cited by 91 · see citing works
Cellular Senescence and Tissue Aging In Vivo
Hornsby, P. J. (2002) · The Journals of Gerontology Series A · doi:10.1093/gerona/57.7.b251 · Cited by 91 · see citing works
Arat, S., Gibbons, J. R., Rzucidlo, S. J., Respess, D. S., Tumlin, M., & Stice, S. L. (2002) · Biology of Reproduction · doi:10.1095/biolreprod66.6.1768 · Cited by 90 · see citing works
Reproductive Characteristics of Cloned Heifers Derived from Adult Somatic Cells1
Enright, B. P., Taneja, M., Schreiber, D. T., Riesen, J. W., Tian, X. C., Fortune, J. E., & Yang, X. (2002) · Biology of Reproduction · doi:10.1095/biolreprod66.2.291 · Cited by 89 · see citing works
Chromatin regulation and non-coding RNAs at mammalian telomeres
Schoeftner, S., & Blasco, M. A. (2009) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2009.09.015 · Cited by 87 · see citing works
Transgenic Technology in Farm Animals – Progress and Perspectives
Wolf, E., Schernthaner, W., Zakhartchenko, V., Prelle, K., Stojković, M., & Brem, G. (2000) · Experimental Physiology · doi:10.1017/s0958067000021102 · Cited by 89 · see citing works
Cloning: experience from the mouse and other animals
Yanagimachi, R. (2002) · Molecular and Cellular Endocrinology · doi:10.1016/s0303-7207(01)00697-9 · Cited by 88 · see citing works
Repair of telomeric DNA prior to replicative senescence
Lansdorp, P. M. (2000) · Mechanisms of Ageing and Development · doi:10.1016/s0047-6374(00)00151-2 · Cited by 87 · see citing works
Self-citationFertilizable oocytes reconstructed from patient's somatic cell nuclei and donor ooplasts
Tesařík, J., Nagy, Z., Sousa, M., Mendoza, C., & Abdelmassih, R. (2001) · Reproductive BioMedicine Online · doi:10.1016/s1472-6483(10)61950-5 · Cited by 88 · see citing works
Joyce, T.-T. (2005) · Frontiers in bioscience · doi:10.2741/1686 · Cited by 87 · see citing works
Successful Serial Recloning in the Mouse over Multiple Generations
Wakayama, S., Kohda, T., Obokata, H., Tokoro, M., Li, C., Terashita, Y., Mizutani, E., Nguyen, V. T., Kishigami, S., Ishino, F., et al. (2013) · Cell stem cell · doi:10.1016/j.stem.2013.01.005 · Cited by 87 · see citing works
Shi, W., Hoeflich, A., Flaswinkel, H., Stojković, M., Wolf, E., & Zakhartchenko, V. (2003) · Biology of Reproduction · doi:10.1095/biolreprod.102.012112 · Cited by 86 · see citing works
Problemas y perspectivas de la clonación de animales
Wells, D. N. (2005) · Scientific and Technical Review (World Organisation for Animal Health) · doi:10.20506/rst.24.1.1566 · Cited by 86 · see citing works
Cloning to reproduce desired genotypes
Westhusin, M. E., Long, C. R., Shin, T., Hill, J. R., Looney, C. R., Pryor, J. H., & Piedrahita, J. A. (2001) · Theriogenology · doi:10.1016/s0093-691x(00)00444-1 · Cited by 85 · see citing works
Living forever and dying in the attempt
Hayflick, L. (2003) · Experimental Gerontology · doi:10.1016/j.exger.2003.09.003 · Cited by 82 · see citing works
Stem cell therapy and the retina
MacLaren, R. E., & Pearson, R. A. (2007) · Eye · doi:10.1038/sj.eye.6702842 · Cited by 80 · see citing works
Is There an Antiaging Medicine?
Butler, R. N., Fossel, M., Harman, S. M., Heward, C. B., Olshansky, S. J., Perls, T. T., Rothman, D. J., Rothman, S. M., Warner, H. R., West, M. D., et al. (2002) · The Journals of Gerontology Series A · doi:10.1093/gerona/57.9.b333 · Cited by 76 · see citing works
Self-citationSerial bull cloning by somatic cell nuclear transfer
Kubota, C., Tian, X., & Yang, X. (2004) · Nature Biotechnology · doi:10.1038/nbt975 · Cited by 77 · see citing works
- Authors
- Lanza, R. P., Cibelli, J. B., Blackwell, C., Cristofalo, V. J., Francis, M. K., Baerlocher, G. M., Mak, J., Schertzer, M., Chavez, E. A., Sawyer, N., Lansdorp, P. M., & West, M. D.
- Affiliations
- Advanced Cell Technology (United States) (US)
- Thomas Jefferson University (US)
- Terry Fox Research Institute (CA)
- University of British Columbia (CA)
- Corresponding author
- Lanza, Robert P.
- ORCID
- Venue
- Science
- Published
- 2000-04-28
- Volume
- 288
- Issue
- 5466
- Pages
- 665-669
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- OpenAlex
- W2141926462
- Cited by
- 466
- References
- 44
- Citations by year
- 2025: 4 · 2024: 2 · 2023: 10 · 2022: 8 · 2021: 10 · 2020: 4 · 2019: 9 · 2018: 3 · 2017: 7 · 2016: 7 · 2015: 7 · 2014: 13 · 2013: 16 · 2012: 16
- FWCI
- 34.86
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- ScholarWorks@UMassAmherst (University of Massachusetts Amherst) (submittedVersion)
- Funders
- National Institutes of Health (1r01gm056162-01)
- National Institute on Aging (AG00378)
- National Institute of General Medical Sciences (GM56162)
- National Institute of Allergy and Infectious Diseases (AI 29524)
- Topics
- Health Sciences › Medicine › Physiology › Telomeres, Telomerase, and Senescence
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Animal Genetics and Reproduction
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Pluripotent Stem Cells Research
- Keywords
- somatic cell nuclear transfer, cloning, cellular aging, replicative lifespan, telomere length, telomere elongation, cloned calves, age-related gene expression, regenerative medicine, mammalian aging
- MeSH terms
- Pigment Epithelium-Derived Factor, Animals, Cattle, Cell Division, Cells, Cultured, Clone Cells, Embryo Transfer, Eye Proteins, Female, Fibroblasts, Flow Cytometry, Longevity, Nerve Growth Factors, Proteins, RNA, Messenger, Blotting, Southern, Serpins, Matched-Pair Analysis, Telomere, Cellular Senescence, In Situ Hybridization, Fluorescence, DNA, Complementary, Cloning, Organism, Nuclear Transfer Techniques
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