Telomeres are the specialized ends of chromosomes consisting of highly conserved repeat (5′-TTAGGG-3′)n sequences. Lack of information regarding the existence of an in vivo telomere clock function in birds, conflicting data regarding telomere array length in the chicken model, and the paucity of molecular telomere information for other avian species led us to study telomere array organization within and among 18 species and subspecies of birds. Most of the species contained between 2% and 4% telomere sequence per diploid genome. Arrays spanning 0.5–10 kb (Class I) and 10–40 kb (Class II) were observed in all of the species studied. Extremely long arrays, ranging from hundreds of kilobases to 1–2 Mb (Class III) were observed in all except two raptor species, the northern goshawk and American bald eagle. In chicken, there was evidence for shortening of the Class II arrays in vivo, based on intraindividual comparisons of somatic versus germline tissues in birds of different ages; terminally differentiated erythrocyte arrays were, on average, 2.3 kb shorter than sperm (germline) arrays. This study provides the first evidence for the existence of telomere arrays significantly larger than have been described for any vertebrate species to date and for developmentally programmed in vivo telomere shortening in the Aves taxa. The novel finding of megabase-sized telomere arrays may be an important feature of avian karyotypes that contain a large number of very small genetic units, the microchromosomes.   

1.
Allshire RC, Dempster M, Hastie ND: Human telomeres contain at least three types of G-rich repeat distributed non-randomly. Nucl Acids Res 17:4611–4627 (1989).
2.
Allshire RC, Gosden, JR, Cross SH, Cranston G, Rout D, Sugaware N, Szostak JW, Fantes PA, Hastie ND: Telomeric repeat from T. thermophila cross hybridizes with human telomeres. Nature 332:656–659 (1988).
3.
Bassham S, Beam A, Shampay J: Telomere variation in Xenopus laevis. Mol Cell Biol 18:269–275 (1998).
4.
Blasco MA, Lee H-W, Hande MP, Samper E, Lansdorp PM, DePinho RA, Greider CW: Telomere shortening and tumor formation by mouse cells lacking telomerase RNA. Cell 91:25–34 (1997).
5.
Bloom SE, Delany ME, Muscarella DM: Constant and variable features of avian chromosomes, in Etches RJ, Verrinder Gibbins AM (eds): Manipulation of the Avian Genome, pp 39–59 (CRC Press, Boca Raton 1993).
6.
Bodnar AG, Ouellette M, Frolkis M, Holt SE, Chiu C-P, Morin GB, Harley CB, Shay JW, Lichtsteiner S, Wright WE: Extension of life-span by introduction of telomerase into normal human cells. Science 279:349–352 (1998).
7.
Carman TA, Afshari CA, Barrett JC: Cellular senescence in telomerase-expressing Syrian hamster embryo cells. Expl Cell Res 244:33–42 (1998).
8.
Chu G, Vollrath D, Davis RW: Separation of large DNA molecules by contour-clamped homogeneous electric fields. Science 234:1582–1585 (1986).
9.
Counter CM, Avilion AA, LeFeuvre CE, Stewart NG, Greider CW, Harley CB, Bacchetti S: Telomere shortening associated with chromosome stability is arrested in immortal cells which express telomerase activity. EMBO J 11:1921–1929 (1992).
10.
Counter CM, Hirte HW, Bacchetti S, Harley CB: Telomerase activity in human ovarian carcinoma. Proc natl Acad Sci, USA 91:2900–2904 (1994).
11.
Coviello-McLaughlin GM, Prowse KR: Telomere length regulation during postnatal development and ageing in Mus spretus. Nucl Acids Res 25:3051–3058 (1997).
12.
De Boer LEM: The somatic chromosome complements of 16 species of Falconiformes (Aves) and the karyological relationships of the order. Genetica 46:77–113 (1976).
13.
Fang G, Cech TR: Telomere proteins, in Blackburn EH, Greider CW (eds): Telomeres, pp 69–105 (Cold Spring Harbor Laboratory Press, Cold Spring Harbor 1995).
14.
Greider CW, Blackburn EH: Identification of a specific telomere terminal transferase activity in Tetrahymena cell extracts. Cell 43:405–413 (1985).
15.
Greider CW, Blackburn EH: A telomeric sequence in the RNA of Tetrahymena telomerase is required for telomere repeat synthesis. Nature 337:331–337 (1989).
16.
Groenen MAM, Cheng HH, Bumstead N, Benkel BF, Briles WE, Burke T, Burt DW, Crittenden LB, Dodgson J, Hillel J, Lamont S, Ponce de Leon A, Soller M, Takahaski H, Vignal A: A consensus linkage map of the chicken genome. Genome Res 10:137–147 (2000).
17.
Harley CB: Telomere loss: mitotic clock or genetic time bomb? Mutat Res 256:271–281 (1991).
18.
Harley CB: Telomeres and aging, in Blackburn EH, Greider CW (eds): Telomeres, pp 247–263 (Cold Spring Harbor Laboratory Press, Cold Spring Harbor 1995).
19.
Hastie ND, Dempster M, Dunlop MG, Thompson AM, Green DK, Allshire RC: Telomere reduction in human colorectal carcinoma and with ageing. Nature 346:866–868 (1990).
20.
Henderson E: Telomere DNA structure, in Blackburn EH, Greider CW (eds): Telomeres, pp 11–34 (Cold Spring Harbor Laboratory Press, Cold Spring Harbor 1995).
21.
Holmes DJ, Austad SN: The evolution of avian senescence patterns: implications for understanding primary aging processes. Am Zool 35:307–317 (1995).
22.
Kim NW, Piatyszek MA, Prowse KR, Harley CB, West MD, Ho PLC, Coviello M, Wright WE, Weinrich SL, Shay JW: Specific association of human telomerase activity with immortal cells and cancer. Science 266:2011–2015 (1994).
23.
Kipling D: Telomere structure and telomerase expression during mouse development and tumorigenesis. Eur J Cancer 33:792–800 (1997).
24.
Kipling D, Cooke HJ: Specific association of human telomerase activity with immortal cells and cancer. Nature 347:400–402 (1990).
25.
Lee H-W, Blasco MA, Gottliev GJ, Horner II JW, Greider CW, DePinho RA: Essential role of mouse telomerase in highly proliferative organs. Nature 392:569–574 (1998).
26.
Lejnine S, Vladimir L, Langmore JP: Conserved nucleoprotein structure at the ends of vertebrate and invertebrate chromosomes. Proc natl Acad Sci, USA 92:2393–2397 (1995).
27.
Lima L, Macieira-Coelho A: Parameters of aging in chicken embryo fibroblasts cultivated in vitro. Expl Cell Res 70:279–284 (1972).
28.
Lima L, Malaise E, Macieira-Coelho A: Aging in vitro: effect of low dose irradiation on the division potential of chick embryonic fibroblasts. Exp Cell Res 73:345–350 (1972).
29.
Mantell LL, Geider CW: Telomerase activity in germline and embryonic cells of Xenopus. EMBO J 13:3211–3217 (1994).
30.
Meyne J, Tatliff R, Moyzis RK: Conservation of the human telomere sequence (TTAGGG)n among vertebrates. Proc natl Acad Sci, USA 86:7049–7053 (1989).
31.
Moyzis RK, Buckingham JM, Cram LS, Dani M, Deaven LL, Jones MD, Meyne J, Ratliff RL, Wu J-R: A highly conserved repetitive DNA sequence, (TTAGGG)n, present at the telomeres of human chromosomes. Proc natl Acad Sci, USA 85: 6622–6626 (1988).
32.
Nanda I, Schmid M: Localization of the telomeric (TTAGGG)n sequence in chicken (Gallus domesticus) chromosomes. Cytogenet Cell Genet 65:190–193 (1994).
33.
Niida H, Matsumoto T, Satoh H, Shiwa M, Tokutake Y, Furuichi Y, Shinkai Y: Severe growth defect in mouse cells lacking the telomerase RNA component. Nature Genet 19:203–206 (1998).
34.
Nugent CI, Lundblad V: The telomerase reverse transcriptase: components and regulation. Genes Dev 12:1083–1085 (1998).
35.
Ponten J: Spontaneous and virus-induced transformation in cell culture. Virol Monogr 8:4–186 (1971).
36.
Prowse KR, Greider CW: Developmental and tissue-specific regulation of mouse telomerase and telomere length. Proc natl Acad Sci, USA 92:4818–4822 (1995).
37.
Renzoni A., Vegni-Talluri, M: The karyograms of some Falconiformes and Strigiformes. Chromosoma 20:133–150 (1966).
38.
Rudolph KL, Chang S, Lee HW, Blasco M, Gottlieb GJ, Grieder C, DePinho RA: Longevity, stress response, and cancer in aging telomerase-deficient mice. Cell 96:701–712 (1999).
39.
Shaw EM, Guise KS, Shoffner RN: Chromosomal localization of chicken sequences homologous to the B-actin gene by in situ hybridization. J Hered 80:475–478 (1989).
40.
Starling JA, Maule J, Hastie ND, Allshire RC: Extensive telomere repeat arrays in mouse are hypervariable. Nucl Acids Res 18:6881–6888 (1990).
41.
Tagaki N, Sasaki M: A phylogenetic study of bird karyotypes. Chromosoma 46:91–120 (1974).
42.
Venkatasen RN, Price C: Telomerase expression in chickens: constitutive activity in somatic tissues and down-regulation in culture. Proc natl Acad Sci, USA 95:14763–14768 (1998).
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