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Dynamics of telomere length in the chicken

Published online by Cambridge University Press:  13 November 2014

S.H. SOHN  and
V.K. SUBRAMANI
S.H. SOHN*
Affiliation:
Department of Animal Science and Biotechnology, Gyeongnam National University of Science and Technology, Jinju 660-758, Republic of Korea
V.K. SUBRAMANI
Affiliation:
Department of Animal Science and Biotechnology, Gyeongnam National University of Science and Technology, Jinju 660-758, Republic of Korea
*
Corresponding author: shsohn@gntech.ac.kr
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Abstract

Telomeres are specialised nucleoprotein end structures of eukaryotic chromosomes and protect and maintain genome integrity from recombination, exonuclease degradation and end-to-end fusion. Because of the end replication problem, telomere length in somatic cells tends to decrease with organismal age. Telomere shortening is known to occur in chicken somatic tissues and correlates with advanced developmental age. However, age is not the only determinant of telomere length in an individual. Several factors at the genetic and epigenetic levels are known to affect telomere length in different ways. Herein, we review several factors that affect telomere length in the chicken. Genetic factors include breed and sex, while the epigenetic factors include environmental and stochastic influences. Age, stocking density and living or housing systems were reviewed as environmental factors pertaining to the habitat of the organism. Factors such as oxidative stress, antioxidants in feed and restriction feeding were the stochastic factors that we reviewed.

Keywords

chickentelomeregenetic factorsepigenetic factorsenvironmental factors
Type
Review Article
Information
World's Poultry Science Journal , Volume 70 , Issue 4 , December 2014 , pp. 721 - 736
Copyright
Copyright © World's Poultry Science Association 2014 

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References

ABIDIN, Z. and KHATOON, A. (2013) Heat stress on poultry and the beneficial effects of ascorbic acid (vitamin C) supplementation during periods of heat stress. World's Poultry Science Journal 69: 135-151.Google Scholar
AL-AQIL, A. and ZULKIFLI, I. (2009) Changes in heat shock protein 70 expression and blood characteristics in transported broiler chickens as affected by housing and early age feed restriction. Poultry Science 88: 1358-1364.Google Scholar
ALBENTOSA, M.J. and COOPER, J.J. (2004) Effects of cage light and stocking on the frequency of comfort behaviors performed by laying hens in furnished cages. Animal Welfare 13: 419-424.Google Scholar
ALLSOPP, R.C., VAZIRI, H., PATTERSON, C., GOLDSTEIN, S., YOUNGLAI, E.V., FUTCHER, A.B., GREIDER, C.W. and HARLEY, C.B. (1992) Telomere length predicts replicative capacity of human fibroblasts. Proceedings of the National Academy of Sciences U.S.A. 89: 10114-10118.Google Scholar
ANDREW, T., AVIV, A., FALCHI, M., SURDULESCU, G.L., GARDNER, J.P., LU, X., KIMURA, M., KATO, B.S., VALDES, A.M. and SPECTOR. T.D. (2006) Mapping genetic loci that determine leukocyte telomere length in a large sample of unselected female sibling pairs. American Journal of Human Genetics 78: 480-486.Google Scholar
BAIRD, D.M. (2006) Telomeres. Experimental Gerontology 41: 1223-1227.Google Scholar
BARJA, G., CADENAS, S., ROJAS, C., PEREZ-CAMPO, R. and LOPEZ-TORRES, M. (1994) Low mitochondrial free radical production per unit O2 consumption can explain the simultaneous presence of high longevity and high aerobic metabolic rate in birds. Free Radical Research 21: 317-327.Google Scholar
BAXTER, M.R. (1994) The welfare problems of laying hens in battery cages. Veterinary Record 134: 614-619.Google Scholar
BELOOR, J., KANG, H.K., KIM, Y.J., SUBRAMANI, V.K., JANG, I.S., SOHN, S.H. and MOON, Y.S. (2010) The effect of stocking density on stress related genes and telomeric length in broiler chickens. Asian-Australasian Journal of Animal Sciences 23: 437-443.Google Scholar
BENETOS, A., OKUDA, K., LAJEMI, M., KIMURA, M., THOMAS, F., SKURNICK, J., LABAT, C., BEAN, K. and AVIV, A. (2001) Telomere length as an indicator of biological aging: The gender effect and relation with pulse pressure and pulse wave velocity. Hypertension 37: 381-385.Google Scholar
BLACKBURN, E.H. and GALL, J.G. (1978) A tandemly repeated sequence at the termini of the extrachromosomal ribosomal RNA genes in Tetrahymena. Journal of Molecular Biology 120: 33-53.Google Scholar
BLACKBURN, E.H., CHAN, S., CHANG, J., FULTON, T.B., KRAUSKOPF, A., MCEACHERN, M., PRESCOTT, J., ROY, J., SMITH, C. and WANG, H. (2000) Molecular manifestations and molecular determinants of telomere capping. Cold Spring Harbor Symposia on Quantitative Biology 65: 253-263.Google Scholar
BRITT-COMPTON, B., ROWSON, J., LOCKE, M., MACKENZIE, I., KIPLING, D. and BAIRD, D.M. (2006) Structural stability and chromosome-specific telomere length is governed by cis-acting determinants in humans. Human Molecular Genetics 15: 725-733.Google Scholar
BRUMMENDORF, T.H., MAK, J., SABO, K.M., BAERLOCHER, G.M., DIETZ, K., ABKOWITZ, J.L. and LANSDORP, P.M. (2002) Longitudinal studies of telomere length in feline blood cells: implications for hematopoietic stem cell turnover in vivo. Experimental Hematology 30: 1147-1152.Google Scholar
CHERIF, H., TARRY, J.L., OZANNE, S.E. and HALES, C.N. (2003) Ageing and telomeres: a study into organ- and gender-specific telomere shortening. Nucleic Acids Research 31: 1576-1583.Google Scholar
CHIU, C.P. and HARLEY, C.B. (1997) Replicative senescence and cell immortality: the role of telomeres and telomerase. Proceedings of the Society for Experimental Biology and Medicine 214: 99-106.Google Scholar
CHO, E.J., CHOI, C.H. and SOHN, S.H. (2005) The amount of telomeres and telomerase activity on chicken embryonic cells during developmental stages. Journal of Animal Science and Technology 47: 187-794.Google Scholar
CHOI, N.E., KIM, H.S., CHOE, C.Y., JEON, G.J. and SOHN, S.H. (2010) Cattle age prediction by leukocytes telomere quantification. Journal of Animal Science and Technology 52: 367-374.Google Scholar
COOK, M.E. (1991) Nutrition and immune response of the domestic fowl. Critical Reviews in Poultry Biology 3: 167-189.Google Scholar
COUNTER, C.M., AVILION, A.A., LEFEUVRE, C.E., STEWART, N.G., GREIDER, C.W., HARLEY, C.B. and BACCHETTI, S. (1992) Telomere shortening associated with chromosome instability is arrested in immortal cells which express telomerase activity. The EMBO Journal 11: 1921-1929.Google Scholar
DE JONG, I.C., VAN VOORST, S., EHLHARDT, D.A. and BLOKHUIS, H.J. (2002) Effects of restricted feeding on physiological stress parameters in growing broiler breeders. British Poultry Science 43: 157-168.Google Scholar
DELANY, M.E., DANIELS, L.M., SWANBERG, S.E. and TAYLOR, H.A. (2003) Telomeres in the chicken: genome stability and chromosome ends. Poultry Science 82: 917-926.Google Scholar
DELANY, M.E., KRUPKIN, A.B. and MILLER, M.M. (2000) Organisation of telomere sequences in birds: evidence for arrays of extreme length and for in vivo shortening. Cytogenetics Cell Genetics 90: 139-145.Google Scholar
DELEZIE, E., SWENNEN, Q., BUYSE, J. and DECUYPERE, E. (2007) The effect of feed withdrawal and crating density in transit on metabolism and meat quality of broilers at slaughter weight. Poultry Science 86: 1414-1423.Google Scholar
EPEL, E.S., BLACKBURN, E.H., LIN, J., DHABHAR, F.S., ADLER, N.E., MORROW, J.D. and CAWTHON, R.M. (2004) Accelerated telomere shortening in response to life stress. Proceedings of the National Academy of Sciences U.S.A. 101: 17312-17315.Google Scholar
FASSBINDER-ORTH, C.A. and KARASOV, W.H. (2006) Effects of feed restriction and realimentation on digestive and immune function in the leghorn chick. Poultry Science 80: 1449-1456.Google Scholar
FLANARY, B.E. and KLETETSCHKA, G. (2005) Analysis of telomere length and telomerase activity in tree species of various life-spans, and with age in the bristlecone pine Pinus longaeva. Biogerontology 6: 101-111.Google Scholar
FRANCHINI, A., CANTI, M., MANFREDA, G., BERTUZZI, S., ASDRUBALI, G. and FRANCIOSI, C. (1991) Vitamin E as adjuvant in emulsified vaccine for chicks. Poultry Science 70: 1709-1715.Google Scholar
FRANCIS, N., GREGG, T., OWEN, R., EBERT, T. and BODNAR, A. (2006) Lack of age-associated telomere shortening in long- and short-lived species of sea urchins. FEBS Letters 580: 4713-4717.Google Scholar
FREIRE, R., WILKINS, L.J., SHORT, F. and NICOL, C.J. (2003) Behaviour and welfare of individual laying hens in a non-cage system. British Poultry Science 44: 22-29.Google Scholar
GONZALEZ-VEGA-AGUIRRE, D., CONTRERAS, B.P.A., KLEIN, R. and BOHMWALD, H. (1995) Effect of vitamin C and E supplementation in the diet of broilers chicks on performance and immune response. Veterinaria 26: 333-340.Google Scholar
GOUS, R.M. and MORRIS, T.R. (2005) Nutritional interventions in alleviating the effects of high temperatures in broiler production. World's Poultry Science Journal 61: 463-475.Google Scholar
GREIDER, C.W. and BLACKBURN, E.H. (1985) Identification of a specific telomere terminal transferase activity in Tetrahymena extracts. Cell 43: 405-413.Google Scholar
GUESDON, V., AHMED, A.M., MALLET, S., FAURE, J.M. and NYS, Y. (2006) Effects of beak trimming and cage design on laying hen performance and egg quality. British Poultry Science 47: 1-12.Google Scholar
HALL, M.E., NASIR, L., DAUNT, F., GAULT, E.A., CROXALL, J.P., WANLESS, S. and MONAGHAN, P. (2004) Telomere loss in relation to age and early environment in long-lived birds. Proceedings of the Royal Society B: Biological Sciences 271: 1571-1576.Google Scholar
HALLIWELL, B. and GUTTERIDGE, J.M.C. (1989) Lipid peroxidation: A radical chain reaction, in: Free Radicals in Biology and Medicine (2nd Eds), pp. 188-218 (New York, Oxford University Press).Google Scholar
HARLEY, C.B., FUTCHER, A.B. and GREIDER, C.W. (1990) Telomeres shorten during ageing of human fibroblasts. Nature 345: 458-460.Google Scholar
HAUSSMANN, M.F. and MAUCK, R.A. (2008) Telomeres and longevity: testing an evolutionary hypothesis. Molecular Biology and Evolution 25: 220-228.Google Scholar
HAUSSMANN, M.F., WINKLER, D.W., HUNTINGTON, C.E., NISBET, I.C. and VLECK, C.M. (2007) Telomerase activity is maintained throughout the lifespan of long-lived birds. Experimental Gerontology 42: 610-618.Google Scholar
HAUSSMANN, M.F., WINKLER, D.W., O'REILLY, K.M., HUNTINGTON, C.E., NISBET, I.C. and VLECK, C.M. (2003) Telomeres shorten more slowly in long-lived birds and mammals than in short-lived ones. Proceedings of the Royal Society B: Biological Sciences 270: 1387-1392.Google Scholar
HEIDINGER, B.J., BLOUNT, J.D., BONER, W., GRIFFITHS, K., METCALFE, N.B. and MONAGHAN, P. (2012) Telomere length in early life predicts lifespan. Proceedings of the National Academy of Sciences U.S.A. 109: 1743-1748.Google Scholar
HEMANN, M.T. and GREIDER, C.W. (2000) Wild-derived inbred mouse strains have short telomeres. Nucleic Acids Research 28: 4474-4478.Google Scholar
HENDERSON, E. (1995) Telomere DNA structure. in: BLACKBURN, E.H. & GREIDER, C.W. (Eds) Telomeres, pp. 11-34 (New York, Cold Spring Harbor Laboratory Press).Google Scholar
HEWAKAPUGE, S., VAN OORSCHOT, R.A., LEWANDOWSKI, P. and BAINDUR-HUDSON, S. (2008) Investigation of telomere lengths measurement by quantitative real-time PCR to predict age. Leg Medicine 10: 236-242.Google Scholar
HOCKING, P.M., MAXWELL, M.H. and MITCHELL, M.A. (1994) Haematology and blood composition at two ambient temperatures in genetically fat and lean adult broiler breeder females fed ad libitum or restricted throughout life. British Poultry Science 35: 799-807.Google Scholar
HOLMES, D.J. and AUSTAD, S.N. (1995) Birds as animal models for the comparative biology of aging: a prospectus. The Journals of Gerontology Series A: Biological Sciences and Medical Sciences 50: B59-B66.Google Scholar
HOLMES, D.J. and OTTINGER, M.A. (2003) Birds as long-lived animal models for the study of aging. Experimental Gerontology 38: 1365-1375.Google Scholar
HOLMES, D.J., FLUCKIGER, R. and AUSTAD, S.N. (2001) Comparative biology of aging in birds: an update. Experimental Gerontology 36: 869-883.Google Scholar
HORN, T., ROBERTSON, B.C., WILL, M., EASON, D.K., ELLIOTT, G.P. and GEMMELL, N.J. (2011) Inheritance of telomere length in a bird. PLoS One 6: e17199.Google Scholar
JANG, I.S., KANG, S.Y., KO, Y.H., MOON, Y.S. and SOHN, S.H. (2009) Effect of qualitative and quantitative feed restriction on growth performance and immune function in broiler chickens. Asian-Australasian Journal of Animal Sciences 22: 388-395.Google Scholar
JEMIELITY, S., KIMURA, M., PARKER, K.M., PARKER, J.D., CAO, X., AVIV, A. and KELLER, L. (2007) Short telomeres in short-lived males: what are the molecular and evolutionary causes? Aging Cell 6: 225-233.Google Scholar
JULIAN, R.J. (1993) Ascites in poultry. Avian Pathology 22: 419-454.Google Scholar
JUNG, G.S., CHO, E.J., CHOI, D.S., LEE, M.J., PARK, C., JEON, I.S. and SOHN, S.H. (2006) Analysis of telomere length and telomerase activity of tissues in Korean Native Chicken. Korean Journal of Poultry Science 33: 97-103.Google Scholar
KAKUO, S., ASAOKA, K. and IDE, T. (1999) Human is a unique species among primates in terms of telomere length. Biochemical and Biophysical Research Communications 263: 308-314.Google Scholar
KANG, S.Y., KO, Y.H., MOON, Y.S., SOHN, S.H. and JANG, I.S. (2011) Effects of the combined stress induced by stocking density and feed restriction on hematological and cytokine parameters as stress indicators in laying hens. Asian-Australasian Journal of Animal Sciences 24: 414-420.Google Scholar
KELES, H., FIDAN, A.F., CIGERCI, I.H., KUCUKKURT, I., KARADAS, E. and DUNDAR, Y. (2010) Increased DNA damage and oxidative stress in chickens with natural Marek's disease. Veterinary Immunology and Immunopathology 133: 51-58.Google Scholar
KESTIN, S.C., KNOWLES, T.G., TINCH, A.E. and GREGORY, N.G. (1992) Prevalence of leg weakness in broiler chickens and its relationship with genotype. Veterinary Record 131: 190-194.Google Scholar
KIM, Y.J., SUBRAMANI, V.K. and SOHN, S.H. (2011) Age prediction in the chickens using telomere quantity by quantitative fluorescence in situ hybridisation technique. Asian-Australasian Journal of Animal Sciences 24: 603-609.Google Scholar
KOTRSCHAL, A., ILMONEN, P. and PENN, D.J. (2007) Stress impacts telomere dynamics. Biology Letters 3: 128-130.Google Scholar
KU, H.H. and SOHAL, R.S. (1993) Comparison of mitochondrial pro-oxidant generation and anti-oxidant defenses between rat and pigeon: possible basis of variation in longevity and metabolic potential. Mechanisms of Ageing and Development 72: 67-76.Google Scholar
LAY, D.C. Jr, FULTON, R.M., HESTER, P.Y., KARCHER, D.M., KJAER, J.B., MENCH, J.A., MULLENS, B.A., NEWBERRY, R.C., NICOL, C.J., O'SULLIVAN, N.P. and PORTER, R.E. (2011) Hen welfare in different housing systems. Poultry Science 90: 278-294.Google Scholar
LEE, M.H., LEE, S.H., KIM, Y.J., KO, Y.H., JANG, I.S., MOON, Y.S., CHOI, Y.H. and SOHN, S.H. (2008) Effect of dietary anti-oxidant supplementation on telomere length and egg quality in laying hens. Korean Journal of Poultry Science 35: 267-274.Google Scholar
LEVY, M.Z., ALLSOPP, R.C., FUTCHER, A.B., GREIDER, C.W. and HARLEY, C.B. (1992) Telomere end-replication problem and cell aging. Journal of Molecular Biology 225: 951-960.Google Scholar
LOUIS, E.J. and VERSHININ, A.V. (2005) Chromosome ends: different sequences may provide conserved functions. BioEssays 27: 685-697.Google Scholar
MAHMOUD, K.Z., EDENS, F.W., EISEN, E.J. and HAVENSTEIN, G.B. (2004) Ascorbic acid decreases heat shock protein 70 and plasma corticosterone in broilers (Gallus gallus domesticus) subjected to cyclic heat stress. Comparative Biochemistry and Physiology B 137: 35-42.Google Scholar
MASHALY, M.M., HENDRICKS, G.L. 3rd, KALAMA, M.A., GEHAD, A.E., ABBAS, A.O. and PATTERSON, P.H. (2004) Effect of heat stress on production parameters and immune responses of commercial laying hens. Poultry Science 83: 889-894.Google Scholar
MASHALY, M.M., WEBB, M.L., YOUTZ, S.L., ROUSH, W.B. and GRAVES, H.B. (1984) Changes in serum corticosterone concentration of laying hens as a response to increased population density. Poultry Science 63: 2271-2274.Google Scholar
MAURICE, D., LIGHTSEY, S.F., TOLER, J.E. and CANTY, S. (2007) Effect of chronic oxidative/corticosterone-induced stress on ascorbic acid metabolism and total antioxidant capacity in chickens (Gallus gallus domesticus). Journal of Animal Physiology and Animal Nutrition 91: 355-360.Google Scholar
MCDANIEL, G.R. (1983) Factors affecting broiler breeder performance. 5. Effects of preproduction feeding regimens on reproductive performance. Poultry Science 62: 1949-1953.Google Scholar
MCKEVITT, T.P., NASIR, L., DEVLIN, P. and ARGYLE, D.J. (2002) Telomere lengths in dogs decrease with increasing donor age. Journal of Nutrition 132: 1604S-1606S.Google Scholar
MEYDANI, S.N. and BLUMBERG, J.B. (1993) Vitamin E and the immune response, in: CUNNINGHAM-RUNDLES, S. (Ed.) Nutrient Modulation of the Immune Response, pp. 223-238 (New York).Google Scholar
MILES, S.A. and LEESON, S. (1990) Effect of feed restriction during the rearing period on the growth rate and carcass composition of turkey breeder hens. Poultry Science 69: 1753-1758.Google Scholar
MONNIER, V.M. (1990) Nonenzymatic glycosylation, the Maillard reaction and the aging process. The Journal of Gerontology 45: B105-B111.Google Scholar
MORIN, G.B. (1989) The human telomere terminal transferase enzyme is a ribonucleoprotein that synthesizes TTAGGG repeats. Cell 59: 521-529.Google Scholar
MOYZIS, R.K., BUCKINGHAM, J.M., CRAM, L.S., DANI, M., DEAVEN, L.L., JONES, M.D., MEYNE, J., RATLIFF, R.L. and WU, J.R. (1988) A highly conserved repetitive DNA sequence, (TTAGGG)n, present at the telomeres of human chromosomes. Proceedings of the National Academy of Sciences U.S.A. 85: 6622-6626.Google Scholar
MUNSHI-SOUTH, J. and WILKINSON, G.S. (2010) Bats and birds: Exceptional longevity despite high metabolic rates. Ageing Research Reviews 9: 12-19.Google Scholar
NAKAGAWA, S., GEMMELL, N.J. and BURKE, T. (2004) Measuring vertebrate telomeres: applications and limitations. Molecular Ecology 13: 2523-2533.Google Scholar
NAKAMURA, K., TAKUBO, K., IZUMIYAMA-SHIMOMURA, N., SAWABE, M., ARAI, T., KISHIMOTO, H., FUJIWARA, M., KATO, M., OSHIMURA, M., ISHII, A. and ISHIKAWA, N. (2007) Telomeric DNA length in cerebral gray and white matter is associated with longevity in individuals aged 70 years or older. Experimental Gerontology 42: 944-950.Google Scholar
NANDA, I. and SCHMID, M. (1994) Localisation of the telomeric (TTAGGG)n sequence in chicken (Gallus domesticus) chromosomes. Cytogenetics Cell Genetics 65: 190-193.Google Scholar
NAWROT, T.S., STAESSEN, J.A., GARDNER, J.P. and AVIV, A. (2004) Telomere length and possible link to X chromosome. Lancet 363: 507-510.Google Scholar
NICOL, C.J. (1987) Behavioural responses of laying hens following a period of spatial restriction. Animal Behaviour 35: 522-527.Google Scholar
NJAJOU, O.T., CAWTHON, R.M., DAMCOTT, C.M., WU, S.H., OTT, S., GARANT, M.J., BLACKBURN, E.H., MITCHELL, B.D., SHULDINER, A.R. and HSUEH, W.C. (2007) Telomere length is paternally inherited and is associated with parental lifespan. Proceedings of the National Academy of Sciences U. S. A. 104: 12135-12139.Google Scholar
NORDFJALL, K., ELIASSON, M., STEGMAYR, B., MELANDER, O., NILSSON, P. and ROOS, G. (2008) . Telomere length is associated with obesity parameters but with a gender difference. Obesity 16: 2682-2689.Google Scholar
NORDFJALL, K., LAREFALK, A., LINDGREN, P., HOLMBERG, D. and ROOS, G. (2005) Telomere length and heredity: Indications of paternal inheritance. Proceedings of the National Academy of Sciences U.S.A. 102: 16374-16378.Google Scholar
OGBURN, C.E., AUSTAD, S.N., HOLMES, D.J., KIKLEVICH, J.V., GOLLAHON, K., RABINOVITCH, P.S. and MARTIN, G.M. (1998) Cultured renal epithelial cells from birds and mice: enhanced resistance of avian cells to oxidative stress and DNA damage. The Journals of Gerontology Series A: Biological Sciences and Medical Sciences 53: B287-B292.Google Scholar
OLKOWSKI, A.A., WOJNAROWICZ, C., NAIN, S., LING, B., ALCORN, J.M. and LAARVELD, B. (2008) A study on pathogenesis of sudden death syndrome in broiler chickens. Research in Veterinary Science 85: 131-140.Google Scholar
PAMPLONA, R., PRAT, J., CADENAS, S., ROJAS, C., PEREZ-CAMPO, R., LOPEZ TORRES, M. and BARJA, G. (1996) Low fatty acid unsaturation protects against lipid peroxidation in liver mitochondria from long-lived species: the pigeon and human case. Mechanisms of Ageing and Development 86: 53-66.Google Scholar
PARDUE, S.L. and THAXTON, J.P. (1984) Evidence for amelioration of steroid-mediated immunosuppression by ascorbic acid. Poultry Science 63: 1262-1268.Google Scholar
PAULINY, A., WAGNER, R.H., AUGUSTIN, J., SZEP, T. and BLOMQVIST, D. (2006) Age-independent telomere length predicts fitness in two bird species. Molecular Ecology 15: 1681-1687.Google Scholar
PLATZ, S., HEYN, E., HERGT, F., WEIGL, B. and ERHARD, M. (2009) Comparative study on the behaviour, health and productivity of laying hens in a furnished cage and an aviary system. Berliner und Munchener Tierarztliche Wochenschrift 122: 235-240.Google Scholar
POHLE, K. and CHENG, H.W. (2009) Comparative effects of furnished and battery cages on egg production and physiological parameters in White Leghorn hens. Poultry Science 88: 2042-2051.Google Scholar
PUTHPONGSIRIPORN, U., SCHEIDELER, S.E., SELL, J.L. and BECK, M.M. (2001) Effects of vitamin E and C supplementation on performance, in vitro lymphocyte proliferation, and antioxidant status of laying hens during heat stress. Poultry Science 80: 1190-1200.Google Scholar
PUVADOLPIROD, S. and THAXTON, J.P. (2000) Model of physiological stress in chickens 1. Response parameters. Poultry Science 79: 363-369.Google Scholar
RENEMA, R.A., ROBINSON, F.E., MELNYCHUK, V.L., HARDIN, R.T., BAGLEY, L.G., EMMERSON, D.A. and BLACKMAN, J.R. (1994) The use of feed restriction for improving reproductive traits in male-line large white turkey hens. 1. Growth and carcass characteristics. Poultry Science 73: 1724-1738.Google Scholar
RICHTER, T. and PROCTOR, C. (2007) The role of intracellular peroxide levels on the development and maintenance of telomere-dependent senescence. Experimental Gerontology 42: 1043-1052.Google Scholar
RODENBURG, T.B., TUYTTENS, F.A., SONCK, B., DE REU, K., HERMAN, L. and ZOONS, J. (2005) Welfare, health, and hygiene of laying hens housed in furnished cages and in alternative housing systems. Journal of Applied Animal Welfare Science 8: 211-226.Google Scholar
ROUX, A.V., RANJIT, N., JENNY, N.S., SHEA, S., CUSHMAN, M., FITZPATRICK, A. and SEEMAN, T. (2009) Race/ethnicity and telomere length in the multi-ethnic study of atherosclerosis. Aging Cell 8: 251-257.Google Scholar
SARETZKI, G. and VON ZGLINICKI, T. (1999) Replicative senescence as a model of aging: the role of oxidative stress and telomere shortening . Zeitschrift für Gerontologie und Geriatrie 32: 69-75.Google Scholar
SEXTON, K.J., RENDEN, J.A., MARPLE, D.N. and KEMPAINEN, R.J. (1989) Effects of dietary energy on semen production, fertility, plasma testosterone, and carcass composition of broiler-breeder males in cages. Poultry Science 68: 1688-1694.Google Scholar
SHANAWANY, M.M. (1988) Broiler performance under high stocking densities. British Poultry Science 29: 43-52.Google Scholar
SHERWIN, C.M., RICHARDS, G.J. and NICOL, C. (2010) Comparison of the welfare of layer hens in 4 housing systems in the UK. British Poultry Science 51: 488-499.Google Scholar
SHINI, S. (2003) Physiological responses of laying hens to the alternative housing system. International Journal of Poultry Science 2: 357-360.Google Scholar
SHIPPEN-LENTZ, D. and BLACKBURN, E.H. (1990) Functional evidence for an RNA template in telomerase. Science 247: 546-552.Google Scholar
SINGH, R., CHENG, K.M. and SILVERSIDES, F.G. (2009) Production performance and egg quality of four strains of laying hens kept in conventional cages and floor pens. Poultry Science 88: 256-264.Google Scholar
SOHN, S.H. and CHO, E.J. (2010) Distribution of telomeric DNA in Korean Native Chicken chromosomes. Korean Journal of Poultry Science 37: 247-253.Google Scholar
SOHN, S.H., CHO, E.J., JANG, I.S. and MOON, Y.S. (2013) The effects of dietary supplementation of vitamin C and E on the growth performance and the stress response in broiler chickens. Korean Journal of Poultry Science 40: 31-40.Google Scholar
SOHN, S.H., JANG, I.S. and SON, B.R. (2011a) Effect of housing systems of cage and floor on the production performance and stress response in layer. Korean Journal of Poultry Science 38: 305-313.Google Scholar
SOHN, S.H., JANG, I.S., MOON, Y.S., KIM, Y.J., LEE, S.H., KO, Y.H., KANG, S.Y. and KANG, H.K. (2008b) Effect of dietary Siberian ginseng and Eucommia on broiler performance, serum biochemical profiles and telomere length. Korean Journal of Poultry Science 35: 283-290Google Scholar
SOHN, S.H., JUNG, H.J. and CHOI, D.S. (2008a) Amount of telomeric DNA on pig lymphocytes by quantitative fluorescence in situ hybridisation. Journal of Animal Science and Technology 50: 465-474.Google Scholar
SOHN, S.H., SUBRAMANI, V.K., CHO, E.J. and SON, B.R. (2011b) Genetic, epigenetic and environmental factors affecting chicken telomere length. Proceedings of the 9th Asia Pacific Poultry Conference, Taipei, pp. 339.Google Scholar
SOHN, S.H., SUBRAMANI, V.K., MOON, Y.S. and JANG, I.S. (2012) Telomeric DNA quantity, DNA damage and heat shock protein gene expression as physiological stress markers in chickens. Poultry Science 91: 829-836.Google Scholar
SWANBERG, S.E. and DELANY, M.E. (2005) Differential expression of genes associated with telomere length homeostasis and oncogenesis in an avian model. Mechanisms of Ageing and Development 126: 1060-1070.Google Scholar
SWANBERG, S.E., O'HARE, T.H., ROBB, E.A., ROBINSON, C.M., CHANG, H. and DELANY, M.E. (2010) Telomere biology of the chicken: a model for aging research. Experimental Gerontology 45: 647-654.Google Scholar
TACTACAN, G.B., GUENTER, W., LEWIS, N.J., RODRIGUEZ-LECOMPTE, J.C. and HOUSE, J.D. (2009) Performance and welfare of laying hens in conventional and enriched cages. Poultry Science 88: 698-707.Google Scholar
TAUSON, R. (2005) Management and housing systems for layers-Effects of welfare and production. World's Poultry Science Journal 61: 467-490.Google Scholar
TAYLOR, A.A. and HURNIK, J.F. (1996) The long-term productivity of hens housed in battery cages and an aviary. Poultry Science 75: 47-51.Google Scholar
TAYLOR, H.A. and DELANY, M.E. (2000) Ontogeny of telomerase in chicken: impact of downregulation on pre- and postnatal telomere length in vivo. Development, Growth & Differentiation 42: 613-621.Google Scholar
THAXTON, J.P., DOZIER, W.A. 3rd, BRANTON, S.L., MORGAN, G.W., MILES, D.W., ROUSH, W.B., LOTT, B.D. and VIZZIER-THAXTON, Y. (2006) Stocking density and physiological adaptive response of broilers. Poultry Science 85: 819-824.Google Scholar
TOLKAMP, B.J., SANDILANDS, V. and KYRIAZAKIS, I. (2005) Effects of qualitative feed restriction during rearing on the performance of broiler breeders during rearing and lay. Poultry Science 84: 1286-1293.Google Scholar
TSUJI, A., ISHIKO, A. and IKEDA, N. (2005) Telomere shortening and age estimation in forensic medicine. Gerontology 51: 416.Google Scholar
TSUJI, A., ISHIKO, A., TAKASAKI, T. and IKEDA, N. (2002) Estimating age of humans based on telomere shortening. Forensic Science International 126: 197-199.Google Scholar
TUYTTENS, F.A., SONCK, B., STAES, M., VAN GANSBEKE, S., VAN DEN BOGAERT, T. and AMPE, B. (2011) Survey of egg producers on the introduction of alternative housing systems for laying hens in Flanders, Belgium. Poultry Science 90: 941-950.Google Scholar
VENKATESAN, R. and PRICE, C. (1998) Telomerase expression in chickens: Constitutive activity in somatic tissues and down- regulation in culture. Proceedings of the National Academy of Sciences U.S.A. 95: 14763-14768.Google Scholar
VITS, A., WEITZENBÜRGER, D. and DISTL, O. (2005) Comparison of different housing systems for laying hens in respect to economic, health and welfare parameters with special regard to organised cages. Deutsche Tierarztliche Wochenschrift 112: 332-342.Google Scholar
VON ZGLINICKI, T. (2002) Oxidative stress shortens telomeres. Trends in Biochemical Sciences 27: 339-344.Google Scholar
WALSH, T.J. and BRAKE, J. (1999) Effects of feeding program and crude protein intake during rearing on fertility of broiler breeder females. Poultry Science 78: 827-832.Google Scholar
WALTER, M.F., BIESSMANN, M.R., BENITEZ, C., TOROK, T., MASON, J.M. and BIESSMANN, H. (2007) Effects of telomere length in Drosophila melanogaster on life span, fecundity, and fertility. Chromosoma 116: 41-51.Google Scholar
WHITEHEAD, C.C. and KELLER, T. (2003) An update on ascorbic acid in poultry. World's Poultry Science Journal 59: 161-184.Google Scholar
YU, B.P. (1994) Cellular defenses against damage from reactive oxygen species. Physiological Reviews 74: 139-162.Google Scholar
ZEICHNER, S.L., PALUMBO, P., FENG, Y., XIAO, X., GEE, D., SLEASMAN, J., GOODENOW, M., BIGGAR, R. and DIMITROV, D. (1999) Rapid telomere shortening in children. Blood 93: 2824-2830.Google Scholar
ZIMMERMAN, P.H., LINDBERG, A.C., POPE, S.J., GLEN, E., BOLHUIS, J.E. and NICOL, C.J. (2006) The effect of stocking density, flock size and modified management on laying hen behavior and welfare in a non-cage system. Applied Animal Behaviour Science 101: 111-124.Google Scholar
ZUBAIR, A.K. and LEESON, S. (1994) Effect of varying period of early nutrient restriction on growth compensation and carcass characteristics of male broilers. Poultry Science 73: 129-136.Google Scholar
ZUIDHOF, M.J., ROBINSON, F.E., FEDDES, J.J., HARDIN, R.T., WILSON, J.L., MCKAY, R.I. and NEWCOMBE, M. (1995) The effects of nutrient dilution on the well-being and performance of female broiler breeders. Poultry Science 74: 441-456.Google Scholar
ZULKIFLI, I., CHE NORMA, M.T., ISRAF, D.A. and OMAR, A.R. (2002) The effect of early-age food restriction on heat shock protein 70 response in heat-stressed female broiler chickens. British Poultry Science 43: 141-145.Google Scholar