Social isolation shortens telomeres in African Grey parrots (Psittacus erithacus erithacus)

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

  Aydinonat, Denise ^a   Penn, Dustin J ^a   Smith, Steve ^a   Moodley, Yoshan ^a   Hoelzl, Franz ^a   Knauer, Felix ^a   Schwarzenberger, Franz ^a  

^a UNIVERSITY OF VETERINARY MEDICINE   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; DNA; PRIMER DNA;

ANIMAL EXPERIMENT; ARTICLE; BIRDS BY NESTING BEHAVIOR; CHROMOSOMAL INSTABILITY; CHRONIC STRESS; CONTROLLED STUDY; FEMALE; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PARROT; PSITTACUS ERITHACUS ERITHACUS; REAL TIME POLYMERASE CHAIN REACTION; RELATIVE TELOMERE LENGTH; SENESCENCE; SOCIAL EVOLUTION; SOCIAL ISOLATION; TELOMERE HOMEOSTASIS; TELOMERE SHORTENING; AGE; ANIMAL; CHEMISTRY; ERYTHROCYTE; GENETICS; MENTAL STRESS; PATHOPHYSIOLOGY; PHYSIOLOGY; PSYCHOLOGY;

AGE FACTORS; ANIMALS; BIOLOGICAL MARKERS; DNA PRIMERS; ERYTHROCYTES; PARROTS; SOCIAL ISOLATION; STRESS, PSYCHOLOGICAL; TELOMERE SHORTENING;

EID: 84899459618     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0093839     Document Type: Article

References (62)

1. Monaghan P, Haussmann MF (2006) Do telomere dynamics link lifestyle and lifespan? Trends Ecol Evol 21: 47-53. (doi:10.1016/j.tree.2005.11.007).
2. Blackburn EH (1991) Structure and function of telomeres. Nature 350: 569-573. (doi:10.1038/350569a0)
3. Blasco MA (2007) Telomere length, stem cells and aging. Nat Chem Biol 3: 640-649. (doi:10.1038/nchembio.2007.38)
4. Campisi J, d'Adda di Fagagna F (2007) Cellular senescence: when bad things happen to good cells. Nat Rev Mol Cell Biol 8: 729-740. (doi:10.1038/nrm2233)
5. Nalapareddy K, Jiang H, Guachalla Gutierrez LM, Rudolph KL (2008) Determining the influence of telomere dysfunction and DNA damage on stem and progenitor cell aging - what markers can we use? Exp Gerontol 43: 998-1004. (doi:10.1016/j.exger.2008.09.002)
6. Sanders JL, Newman AB (2013) Telomere Length in Epidemiology: A Biomarker of aging, age-related disease, both, or neither? Epidemiol Rev 35: 112-131. (doi:10.1093/epirev/mxs008)
7. Bize P, Criscuolo F, Metcalfe NB, Nasir L, Monaghan P (2009) Telomere dynamics rather than age predict life expectancy in the wild. Proc R Soc B 276: 1679-1683. (doi:10.1098/rspb.2008.1817)
8. Cawthon RM, Smith KR, O'Brien E, Sivatchenko A, Kerber RA (2003) Association between telomere length in blood and mortality in people aged 60 years or older. Lancet 361: 393-395. (doi:10.1016/S0140-6736(03)12384-7)
9. Haussmann MF, Winkler DW, Vleck CM (2005) Longer telomeres associated with higher survival in birds. Biol Lett 1: 212-214. (doi:10.1098/rsbl.2005. 0301)
10. Joeng KS, Song EJ, Lee K, Lee J (2004) Long lifespan in worms with long telomeric DNA. Nat Genet 36: 607-611. (doi:10.1038/ng1356)
11. Epel ES, Blackburn EH, Lin J, Dhabhar FS, Adler NE, et al. (2004) Accelerated telomere shortening in response to life stress. PNAS 101: 17312-17315. (doi:10.1073/pnas.0407162101)
12. Song Z, Von Figura G, Liu Y, Kraus JM, Torrice C, et al. (2010) Lifestyle impacts on the aging-associated expression of biomarkers of DNA damage and telomere dysfunction in human blood. Aging Cell 9: 607-615. (doi:10.1111/j.1474- 9726.2010.00583.x)
13. Epel ES (2009) Psychological and metabolic stress: a recipe for accelerated cellular aging. Hormones (Athens) 8: 7-22.
14. Correia-Melo C, Hewitt G, Passos JF (2014) Telomeres, oxidative stress and inflammatory factors: partners in cellular senescence? Longev Healthspan 3:1. (doi: 10.1186/2046-2395-3-1)
15. Hewitt G, Jurk D, Marques FD, Correia-Melo C, Hardy T, et al. (2012) Telomeres are favoured targets of a persistent DNA damage response in ageing and stress-induced senescence. Nat Commun 3: 708. (doi:10.1038/ncomms1708)
16. Opresko PL, Fan J, Danzy S, Wilson DM, Bohr VA (2005) Oxidative damage in telomeric DNA disrupts recognition by TRF1 and TRF2. Nucleic Acids Res 33: 1230-1239. (doi:10.1093/nar/gki273)
17. Damjanovic AK, Yang Y, Glaser R, Kiecolt-Glaser JK, Nguyen H, et al. (2007) Accelerated Telomere Erosion Is Associated with a Declining Immune Function of Caregivers of Alzheimer's Disease Patients. J Immunol 179: 4249-4254.
18. Beery AK, Lin J, Biddle JS, Francis DD, Blackburn EH, et al. (2012) Chronic stress elevates telomerase activity in rats. Biol Lett 8: 1063-1066. (doi:10.1098/rsbl.2012.0747)
19. Rudolph KL, Chang S, Lee HW, Blasco M, Gottlieb GJ, et al. (1999) Longevity, stress response, and cancer in aging telomerase-deficient mice. Cell, 96: 701-712. (doi:10.1016/S0092-8674(00)80580-2)
20. Henriques CM, Carneiro MC, Tenente IM, Jacinto A, Ferreira MG (2013) Telomerase is required for zebrafish lifespan. PLoS genet 9: e1003214. (doi: 10.1371/journal.pgen.1003214)
21. Wolkowitz OM, Epel ES, Reus VI, Mellon SH (2010) Depression gets old fast: do stress and depression accelerate cell aging? Depress anxiety 27: 327-338. (doi: 10.1002/da.20686)
22. Simon NM, Smoller JW, McNamara KL, Maser RS, Zalta AK, et al. (2006) Telomere shortening and mood disorders: preliminary support for a chronic stress model of accelerated aging. Biol psychiat 60: 432-435. (doi: 10.1016/j.biopsych.2006.02.004)
23. Valdes A, Andrew T, Gardner J, Kimura M, Oelsner E, et al. (2005) Obesity, cigarette smoking, and telomere length in women. Lancet 366: 662-664. (doi:10.1016/S0140-6736(05)66630-5)
24. Vallejo AN, Weyand CM, Goronzy JJ (2004) T-cell senescence: a culprit of immune abnormalities in chronic inflammation and persistent infection. Trends mol med 10: 119-124. (doi: 10.1016/j.molmed.2004.01.002)
25. Kotrschal A, Ilmonen P, Penn DJ (2007) Stress impacts telomere dynamics. Biol Lett 3: 128-130. (doi:10.1098/rsbl.2006.0594)
26. Ilmonen P, Kotrschal A, Penn D J (2008) Telomere attrition due to infection. PLoS One 3: e2143. (doi:10.1371/journal.pone.0002143)
27. Bize P, Criscuolo F, Metcalfe NB, Nasir L, Monaghan P (2009) Telomere dynamics rather than age predict life expectancy in the wild. Proc R Soc B 276: 1679-1683. (doi:10.1098/rspb.2008.1817)
28. Pauliny A, Wagner RH, Augustin J, Szep T, Blomqvist D (2006) Age-independent telomere length predicts fitness in two bird species. Mol Ecol 15: 1681-1687. (doi:10.1111/j.1365-294X.2006.02862.x)
29. Martin-Ruiz CM, Gussekloo J, van Heemst D, von Zglinicki T, Westendorp RGJ (2005) Telomere length in white blood cells is not associated with morbidity or mortality in the oldest old: a population-based study. Aging Cell 4: 287-290. (doi: 10.1111/j.1474-9726.2005.00171.x)
30. Haussmann MF, Winkler DW, O'Reilly KM, Huntington CE, Nisbet IC, et al. (2003) Telomeres shorten more slowly in long-lived birds and mammals than in short-lived ones. Proc R Soc Lond B 270: 1387-1392. (doi:10.1098/rspb.2003.2385)
31. Ujvari B, Madsen T (2009) Short telomeres in hatchling snakes: erythrocyte telomere dynamics and longevity in tropical pythons. PloS one, 4: e7493. (doi: 10.1371/journal.pone.0007493)
32. Kikusui T, Winslow JT, Mori Y (2006) Social buffering: relief from stress and anxiety. Philos Trans R Soc Lond B Biol Sci 361: 2215-2228. (doi:10.1098/rstb.2006.1941)
33. Serra M, Pisu MG, Floris I, Cara V, Purdy RH, et al. (2003) Social isolation-induced increase in the sensitivity of rats to the steroidogenic effect of ethanol. J Neurochem 85: 257-263. (doi:10.1046/j.1471-4159.2003.01680. x)
34. Heidbreder CA, Weiss IC, Domeney AM, Pryce C, Homberg J, et al. (2000) Behavioral, neurochemical and endocrinological characterization of the early social isolation syndrome. Neuroscience 100: 749-768. (doi:10.1016/S0306- 4522(00)00336-5)
35. Juniper T, Parr M (1998) Parrots: A Guide To Parrots Of The World. New Haven, CT: Yale University Press. 584 p.
36. Davis CS (1991) Parrot psychology and behavior problems. Vet Clin North Am Small Anim Pract 21: 1281-1288.
37. van Zeeland YRA, Spruit BM, Rodenburg TB, Riedstra B, van Hierden YM, et al. (2009) Feather damaging behaviour in parrots: A review with consideration of comparative aspects. Appl Anim Behav Sci 121: 75-95. (doi:10.1016/j.applanim. 2009.09.006)
38. Meehan CL, Garner JP, Mench JA (2004) Environmental enrichment and development of cage stereotypy in Orange-winged Amazon parrots (Amazona amazonica). Dev Psychobiol 44: 209-218. (doi:10.1002/dev.20007)
39. Garner JP, Meehan CL, Mench JA (2003) Stereotypies in caged parrots, schizophrenia and autism: evidence for a common mechanism. Behav Brain Res 145: 125-134. (doi:10.1016/S0166-4328(03)00115-3)
40. Garner JP, Meehan CL, Famula TR, Mench JA (2006) Genetic, environmental, and neighbor effects on the severity of stereotypies and feather picking in Orange-winged Amazon parrots (Amazona amazonica): An epidemiological study. Appl Anim Behav Sci 96: 153-168. (doi:10.1016/j.applanim.2005.09.009)
41. Schmid R, Doherr MG, Steiger A (2006) The influence of the breeding method on the behaviour of adult African grey parrots (Psittacus erithacus). Appl Anim Behav Sci 98: 293-307. (doi; 10.1016/j.applanim.2005.09.002)
42. Brouwer K, Jones M, King C, Schifter H (2000) Longevity records for Psittaciformes in captivity. Int Zoo Yearb 37: 299-316.
43. Cawthon RM (2002) Telomere measurement by quantitative PCR. Nucleic Acids Res 30: e47. (doi:10.1093/nar/30.10.e47)
44. Criscuolo F, Bize P, Nasir L, Metcalfe NB, Foote CG, et al. (2009) Real-time quantitative PCR assay for measurement of avian telomeres. J Avian Biol 40: 342-347. (doi:10.1111/j.1600-048X.2008.04623.x)
45. Turbill C, Smith S, Deimel C, Ruf T (2012) Daily torpor is associated with telomere length change over winter in Djungarian hamsters. Biol Lett 8: 304-307. (doi:10.1098/rsbl.2011.0758)
46. Foote CG, Vleck D, Vleck CM (2013) Extent and variability of interstitial telomeric sequences and their effects on estimates of telomere length. Mol ecol 13: 417-428. (doi: 10.1111/1755-0998.12079)
47. Smith S, Turbill C, Penn DJ (2011) Chasing telomeres, not red herrings, in evolutionary ecology. Heredity 107: 372-373. (doi:10.1038/hdy.2011.14)
48. Ruijter JM, Ramakers C, Hoogaars WMH, Karlen Y, et al. (2009) Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data. Nucleic Acids Res 37: e45. (doi:10.1093/nar/gkp045)
49. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45. (doi: 10.1093/nar/29.9.e45)
50. Ehrlenbach S, Willeit P, Kiechl S, Willeit J, Reindl M, et al. (2009) Influences on the reduction of relative telomere length over 10 years in the population-based Bruneck Study: introduction of a well-controlled high-throughput assay. Int J Epidemiol 38: 1725-1734. (doi: 10.1093/ije/dyp273)
51. D'haene B, Vandesompele J, Hellemans J (2010) Accurate and objective copy number profiling using real-time quantitative PCR. Methods 50: 262-270. (doi: 10.1016/j.ymeth.2009.12.007)
52. Fridolfsson AK, Ellegren H (1999) A simple and universal method for molecular sexing of non-ratite birds. J Avian Biol 30: 116-121. (doi:10.2307/3677252)
53. Burnham KP, Anderson DR (2002) Model selection and multi-model inference: a practical information-theoretic approach 2nd edn. New York, NY: Springer. 488 p.
54. Wood SN (2011) Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models. J Roy Stat Soc B 73: 3-36. (doi: 10.1111/j.1467-9868.2010.00749.x)
55. Bartoń K (2009) MuMIn: multi-model inference. R package, version 0.12.2. Available: http://r-forge.r-project.org/projects/mumin/.
56. Price LH, Kao H, Burgers DE, CarpenterLL, Tyrka AR (2013) Telomeres and Early-Life Stress: An Overview. Biol Psychiatry 73: 15-23. (doi:10.1016/j. biopsych.2012.06.025)
57. Barrett EL, Burke TA, Hammers M, Komdeur J, Richardson DS (2013) Telomere length and dynamics predict mortality in a wild longitudinal study. Mol Ecol 22: 249-259. (doi:10.1111/mec.12110)
58. Drury S, Theall K, Gleason M, Smyke A, De Vivo I, et al. (2011) Telomere length and early severe social deprivation: linking early adversity and cellular aging. Mol Psychiatry 17: 719-727. (doi:10.1038/mp.2011.53)
59. Carroll JE, Diez Roux AV, Fitzpatrick AL, Seeman T (2013) Low Social Support Is Associated With Shorter Leukocyte Telomere Length in Late Life: Multi-Ethnic Study of Atherosclerosis. Psychosom Med 75: 171-177. (doi:10.1097/PSY.0b013e31828233bf)
60. Wikelski M, Cooke SJ (2006) Conservation physiology. Trends Ecol Evol 21: 38-46. (doi:10.1016/j.tree.2005.10.018)
61. Dickens MJ, Romero LM (2013) A consensus endocrine profile for chronically stressed wild animals does not exist. Gen Comp Endocrinol 191: 177-189. (doi:10.1016/j.ygcen.2013.06.014)
62. Johnstone CP, Reina RD, Lill A (2012) Interpreting indices of physiological stress in free-living vertebrates. J Comp Physiol B 182: 861-879. (doi:10.1007/s00360-012-0656-9)