PBMC telomerase activity, but not leukocyte telomere length, correlates with hippocampal volume in major depression

Psychiatry Research - Neuroimaging

Volumn 232, Issue 1, 2015, Pages 58-64

  Wolkowitz, Owen M ^a   Mellon, Synthia H ^b   Lindqvist, Daniel ^c   Epel, Elissa S ^a   Blackburn, Elizabeth H ^b   Lin, Jue ^b   Reus, Victor I ^a   Burke, Heather ^a   Rosser, Rebecca ^a   Mahan, Laura ^a   Mackin, Scott ^a   Yang, Tony ^a   Weiner, Michael ^b,d   Mueller, Susanne ^b,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c LUND UNIVERSITY   (Sweden)

^d SAN FRANCISCO VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Brain; Depression; Hippocampus; Leukocytes; Telomerase; Telomeres

Indexed keywords

TELOMERASE;

ADULT; ARTICLE; BRAIN SIZE; CHROMOSOMAL PARAMETERS; CONTROLLED STUDY; ENZYME ACTIVITY; FACILITATION; FEMALE; HIPPOCAMPUS; HUMAN; LEUKOCYTE; LEUKOCYTE TELOMERE LENGTH; MAJOR DEPRESSION; MALE; NERVOUS SYSTEM DEVELOPMENT; NEUROIMAGING; NEUROPROTECTION; NUCLEAR MAGNETIC RESONANCE IMAGING; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; CELL AGING; ENZYMOLOGY; METABOLISM; MIDDLE AGED; MONONUCLEAR CELL; ORGAN SIZE; PATHOLOGY; PHYSIOLOGY; TELOMERE;

ADULT; CELL AGING; DEPRESSIVE DISORDER, MAJOR; FEMALE; HIPPOCAMPUS; HUMANS; LEUKOCYTES; LEUKOCYTES, MONONUCLEAR; MALE; MIDDLE AGED; ORGAN SIZE; TELOMERASE; TELOMERE;

EID: 84927910079     PISSN: 09254927     EISSN: 18727506     Source Type: Journal    
DOI: 10.1016/j.pscychresns.2015.01.007     Document Type: Article

References (68)

1. Arisi G.M. Nervous and immune systems signals and connections: cytokines in hippocampus physiology and pathology. Epilepsy & Behavior 2014, 38C:43-47.
2. Balaji T.M., Vettriselvi V., Paul S.F., Rao S.R. Evaluation of telomerase expression in chronic periodontitis. Indian Journal of Dental Research 2010, 21:185-188.
3. Beery A.K., Lin J., Biddle J.S., Francis D.D., Blackburn E.H., Epel E.S. Chronic stress elevates telomerase activity in rats. Biology Letters 2012, 8:1063-1066.
4. Blackburn E. The telomere and telomerase: how do they interact?. Mount Sinai Journal of Medicine 1999, 66:292-300.
5. Brydon L., Lin J., Butcher L., Hamer M., Erusalimsky J.D., Blackburn E.H., Steptoe A. Hostility and cellular aging in men from the Whitehall II cohort. Biological Psychiatry 2012, 71:767-773.
6. Calado R.T., Dumitriu B. Telomere dynamics in mice and humans. Seminars in Hematology 2013, 50:165-174.
7. Calado R.T., Young N.S. Telomere diseases. New England Journal of Medicine 2009, 361:2353-2365.
8. Canela A., Vera E., Klatt P., Blasco M.A. High-throughput telomere length quantification by FISH and its application to human population studies. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:5300-5305.
9. Cawthon R.M. Telomere measurement by quantitative PCR. Nucleic Acids Research 2002, 30:e47.
10. Cheng A., Shin-ya K., Wan R., Tang S.C., Miura T., Tang H., Khatri R., Gleichman M., Ouyang X., Liu D., Park H.R., Chiang J.Y., Mattson M.P. Telomere protection mechanisms change during neurogenesis and neuronal maturation: newly generated neurons are hypersensitive to telomere and DNA damage. Journal of Neuroscience 2007, 27:3722-3733.
11. Cheng G.L., Zeng H., Leung M.K., Zhang H.J., Lau B.W., Liu Y.P., Liu G.X., Sham P.C., Chan C.C., So K.F., Lee T.M. Heroin abuse accelerates biological aging: a novel insight from telomerase and brain imaging interaction. Translational Psychiatry 2013, 3:e260.
12. Choi J., Fauce S.R., Effros R.B. Reduced telomerase activity in human T lymphocytes exposed to cortisol. Brain, Behavior, and Immunity 2008, 22:600-605.
13. Czeh B., Lucassen P.J. What causes the hippocampal volume decrease in depression? Are neurogenesis, glial changes and apoptosis implicated?. European Archives of Psychiatry and Clinical Neuroscience 2007, 257:250-260.
14. Damjanovic A.K., Yang Y., Glaser R., Kiecolt-Glaser J.K., Nguyen H., Laskowski B., Zou Y., Beversdorf D.Q., Weng N.P. Accelerated telomere erosion is associated with a declining immune function of caregivers of Alzheimer's disease patients. Journal of Immunology 2007, 179:4249-4254.
15. Der G., Batty G.D., Benzeval M., Deary I.J., Green M.J., McGlynn L., McIntyre A., Robertson T., Shiels P.G. Is telomere length a biomarker for aging: cross-sectional evidence from the west of Scotland?. PLoS One 2012, 7:e45166.
16. Devore E.E., Prescott J., De Vivo I., Grodstein F. Relative telomere length and cognitive decline in the Nurses' Health Study. Neuroscience Letters 2011, 492:15-18.
17. Effros R.B. Loss of CD28 expression on T lymphocytes: a marker of replicative senescence. Developmental and Comparative Immunology 1997, 21:471-478.
18. Eitan E., Hutchison E.R., Mattson M.P. Telomere shortening in neurological disorders: an abundance of unanswered questions. Trends in Neurosciences 2014, 37:256-263.
19. Elvsashagen T., Vera E., Boen E., Bratlie J., Andreassen O.A., Josefsen D., Malt U.F., Blasco M.A., Boye B. The load of short telomeres is increased and associated with lifetime number of depressive episodes in bipolar II disorder. Journal of Affective Disorders 2011, 135:43-50.
20. Epel E.S., Lin J., Dhabhar F.S., Wolkowitz O.M., Puterman E., Karan L., Blackburn E.H. Dynamics of telomerase activity in response to acute psychological stress. Brain, Behavior, and Immunology 2010, 24:531-539.
21. First M.B., Spitzer R.L., Gibbon M. Structured Clinical Interview for DSM-IV-TR Axis I Disorders, Research Version, Patient Edition (SCID-I/P) 2002, New York State Psychiatric Institute, Biometrics Research, New York.
22. Fischl B., Salat D.H., Busa E., Albert M., Dieterich M., Haselgrove C., van der Kouwe A., Killiany R., Kennedy D., Klaveness S., Montillo A., Makris N., Rosen B., Dale A.M. Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 2002, 33:341-355.
23. Fischl B., Salat D.H., van der Kouwe A.J., Makris N., Segonne F., Quinn B.T., Dale A.M. Sequence-independent segmentation of magnetic resonance images. NeuroImage 2004, 23(Suppl. 1):S69-S84.
24. Fu W., Lee J., Guo Z., Mattson M.P. Seizures and tissue injury induce telomerase in hippocampal microglial cells. Experimental Neurology 2002, 178:294-300.
25. Fu W., Lu C., Mattson M.P. Telomerase mediates the cell survival-promoting actions of brain-derived neurotrophic factor and secreted amyloid precursor protein in developing hippocampal neurons. Journal of Neuroscience 2002, 22:10710-10719.
26. Gizard F., Heywood E.B., Findeisen H.M., Zhao Y., Jones K.L., Cudejko C., Post G.R., Staels B., Bruemmer D. Telomerase activation in atherosclerosis and induction of telomerase reverse transcriptase expression by inflammatory stimuli in macrophages. Arteriosclerosis, Thrombosis, and Vascular Biology 2011, 31:245-252.
27. Grodstein F., van Oijen M., Irizarry M.C., Rosas H.D., Hyman B.T., Growdon J.H., De Vivo I. Shorter telomeres may mark early risk of dementia: preliminary analysis of 62 participants from the nurses' health study. PLoS One 2008, 3:e1590.
28. Hamilton M. Development of a rating scale for primary depressive illness. British Journal of Social and Clinical Psychology 1967, 6:278-296.
29. Hartmann N., Boehner M., Groenen F., Kalb R. Telomere length of patients with major depression is shortened but independent from therapy and severity of the disease. Depression and Anxiety 2010, 27:1111-1116.
30. Hermann A., Maisel M., Liebau S., Gerlach M., Kleger A., Schwarz J., Kim K.S., Antoniadis G., Lerche H., Storch A. Mesodermal cell types induce neurogenesis from adult human hippocampal progenitor cells. Journal of Neurochemistry 2006, 98:629-640.
31. Hoen P.W., de Jonge P., Na B.Y., Farzaneh-Far R., Epel E., Lin J., Blackburn E., Whooley M.A. Depression and leukocyte telomere length in patients with coronary heart disease: data from the Heart and Soul Study. Psychosomatic Medicine 2011, 73:541-547.
32. Honig L.S., Schupf N., Lee J.H., Tang M.X., Mayeux R. Shorter telomeres are associated with mortality in those with APOE epsilon4 and dementia. Annals of Neurology 2006, 60:181-187.
33. Jacobs E.G., Epel E.S., Lin J., Blackburn E.H., Rasgon N.L. Relationship between leukocyte telomere length, telomerase activity and hippocampal volume in early aging. JAMA Neurology 2014, 71(7):921-923.
34. Jaskelioff M., Muller F.L., Paik J.H., Thomas E., Jiang S., Adams A.C., Sahin E., Kost-Alimova M., Protopopov A., Cadinanos J., Horner J.W., Maratos-Flier E., Depinho R.A. Telomerase reactivation reverses tissue degeneration in aged telomerase-deficient mice. Nature 2011, 469:102-106.
35. Kang H.J., Choi Y.S., Hong S.B., Kim K.W., Woo R.S., Won S.J., Kim E.J., Jeon H.K., Jo S.Y., Kim T.K., Bachoo R., Reynolds I.J., Gwag B.J., Lee H.W. Ectopic expression of the catalytic subunit of telomerase protects against brain injury resulting from ischemia and NMDA-induced neurotoxicity. Journal of Neuroscience 2004, 24:1280-1287.
36. King K.S., Kozlitina J., Rosenberg R.N., Peshock R.M., McColl R.W., Garcia C.K. Effect of leukocyte telomere length on total and regional brain volumes in a large population-based cohort. JAMA Neurology 2014, 71:1247-1254.
37. Lee J., Jo Y.S., Sung Y.H., Hwang I.K., Kim H., Kim S.Y., Yi S.S., Choi J.S., Sun W., Seong J.K., Lee H.W. Telomerase deficiency affects normal brain functions in mice. Neurochemical Research 2010, 35:211-218.
38. Li J., Tang B., Qu Y., Mu D. Telomerase reverse transcriptase: a novel neuroprotective mechanism involved in neonatal hypoxic-ischemic brain injury. International Journal of Developmental Neuroscience 2011, 29:867-872.
39. Liu M., Hu Y., Zhu L., Chen C., Zhang Y., Sun W., Zhou Q. Overexpression of the mTERT gene by adenoviral vectors promotes the proliferation of neuronal stem cells in vitro and stimulates neurogenesis in the hippocampus of mice. Journal of Biomedical Research 2012, 26:381-388.
40. Lung F.W., Chen N.C., Shu B.C. Genetic pathway of major depressive disorder in shortening telomeric length. Psychiatric Genetics 2007, 17:195-199.
41. Ma S.L., Lau E.S., Suen E.W., Lam L.C., Leung P.C., Woo J., Tang N.L. Telomere length and cognitive function in southern Chinese community-dwelling male elders. Age and Ageing 2013, 42:450-455.
42. Maeda T., Guan J.Z., Koyanagi M., Makino N. Telomerase activity and telomere length distribution in vascular endothelial cells in a short-term culture under the presence of hydrogen peroxide. Geriatrics and Gerontology International 2013, 13:774-782.
43. Martin-Ruiz C., Dickinson H.O., Keys B., Rowan E., Kenny R.A., Von Zglinicki T. Telomere length predicts poststroke mortality, dementia, and cognitive decline. Annals of Neurology 2006, 60:174-180.
44. Mather K.A., Jorm A.F., Anstey K.J., Milburn P.J., Easteal S., Christensen H. Cognitive performance and leukocyte telomere length in two narrow age-range cohorts: a population study. BMC Geriatrics 2010, 10:62.
45. Mattson M.P., Fu W., Zhang P. Emerging roles for telomerase in regulating cell differentiation and survival: a neuroscientist's perspective. Mechanisms of Ageing and Development 2001, 122:659-671.
46. Mattson M.P., Klapper W. Emerging roles for telomerase in neuronal development and apoptosis. Journal of Neuroscience Research 2001, 63:1-9.
47. Niu C., Yip H.K. Neuroprotective signaling mechanisms of telomerase are regulated by brain-derived neurotrophic factor in rat spinal cord motor neurons. Journal of Neuropathology and Experimental Neurology 2011, 70:634-652.
48. Price L.H., Kao H.T., Burgers D.E., Carpenter L.L., Tyrka A.R. Telomeres and early-life stress: an overview. Biological Psychiatry 2013, 73:15-23.
49. Qu Y., Duan Z., Zhao F., Wei D., Zhang J., Tang B., Li J., Yang C., Mu D. Telomerase reverse transcriptase upregulation attenuates astrocyte proliferation and promotes neuronal survival in the hypoxic-ischemic rat brain. Stroke 2011, 42:3542-3550.
50. Rentoukas E., Tsarouhas K., Kaplanis I., Korou E., Nikolaou M., Marathonitis G., Kokkinou S., Haliassos A., Mamalaki A., Kouretas D., Tsitsimpikou C. Connection between telomerase activity in PBMC and markers of inflammation and endothelial dysfunction in patients with metabolic syndrome. PLoS One 2012, 7:e35739.
51. Sahin E., Colla S., Liesa M., Moslehi J., Muller F.L., Guo M., Cooper M., Kotton D., Fabian A.J., Walkey C., Maser R.S., Tonon G., Foerster F., Xiong R., Wang Y.A., Shukla S.A., Jaskelioff M., Martin E.S., Heffernan T.P., Protopopov A., Ivanova E., Mahoney J.E., Kost-Alimova M., Perry S.R., Bronson R., Liao R., Mulligan R., Shirihai O.S., Chin L., DePinho R.A. Telomere dysfunction induces metabolic and mitochondrial compromise. Nature 2011, 470:359-365.
52. Saretzki G. Telomerase, mitochondria and oxidative stress. Experimental Gerontology 2009, 44:485-492.
53. Simon N.M., Smoller J.W., McNamara K.L., Maser R.S., Zalta A.K., Pollack M.H., Nierenberg A.A., Fava M., Wong K.K. Telomere shortening and mood disorders: preliminary support for a chronic stress model of accelerated aging. Biological Psychiatry 2006, 60:432-435.
54. Valdes A.M., Deary I.J., Gardner J., Kimura M., Lu X., Spector T.D., Aviv A., Cherkas L.F. Leukocyte telomere length is associated with cognitive performance in healthy women. Neurobiology of Aging 2010, 31:986-992.
55. Verhoeven J.E., Révész D., Epel E.S., Lin J., Wolkowitz O.M., Penninx B.W. Major depressive disorder and accelerated cellular aging: results from a large psychiatric cohort study. Molecular Psychiatry 2014, 19(8):895-901.
56. Watabe-Rudolph M., Begus-Nahrmann Y., Lechel A., Rolyan H., Scheithauer M.O., Rettinger G., Thal D.R., Rudolph K.L. Telomere shortening impairs regeneration of the olfactory epithelium in response to injury but not under homeostatic conditions. PloS one 2011, 6:e27801.
57. Wikgren M., Karlsson T., Lind J., Nilbrink T., Hultdin J., Sleegers K., Van Broeckhoven C., Roos G., Nilsson L.G., Nyberg L., Adolfsson R., Norrback K.F. Longer leukocyte telomere length is associated with smaller hippocampal volume among non-demented APOE epsilon3/epsilon3 subjects. PLoS One 2012, 7:e34292.
58. Wikgren M., Maripuu M., Karlsson T., Nordfjall K., Bergdahl J., Hultdin J., Del-Favero J., Roos G., Nilsson L.G., Adolfsson R., Norrback K.F. Short telomeres in depression and the general population are associated with a hypocortisolemic state. Biological Psychiatry 2012, 71:294-300.
59. Wolkowitz O.M., Epel E.S., Mellon S. When blue turns to grey: do stress and depression accelerate cell aging?. World Journal of Biological Psychiatry 2008, 9:2-5.
60. Wolkowitz O.M., Mellon S.H., Epel E.S., Lin J., Dhabhar F.S., Su Y., Reus V.I., Rosser R., Burke H.M., Kupferman E., Compagnone M., Nelson J.C., Blackburn E.H. Leukocyte telomere length in major depression: correlations with chronicity, inflammation and oxidative stress-preliminary findings. PLoS One 2011, 6:e17837.
61. Wolkowitz O.M., Mellon S.H., Epel E.S., Lin J., Reus V.I., Rosser R., Burke H., Compagnone M., Nelson J.C., Dhabhar F.S., Blackburn E.H. Resting leukocyte telomerase activity is elevated in major depression and predicts treatment response. Molecular Psychiatry 2012, 17:164-172.
62. Wolkowitz O.M., Reus V.I., Mellon S.H. Of sound mind and body: depression, disease, and accelerated aging. Dialogues in Clinical Neuroscience 2011, 13:25-39.
63. Yaffe K., Lindquist K., Kluse M., Cawthon R., Harris T., Hsueh W.C., Simonsick E.M., Kuller L., Li R., Ayonayon H.N., Rubin S.M., Cummings S.R., Health A.B.C.S. Telomere length and cognitive function in community-dwelling elders: findings from the Health ABC Study. Neurobiology of Aging 2011, 32:2055-2060.
64. Zalli A., Carvalho L.A., Lin J., Hamer M., Erusalimsky J.D., Blackburn E.H., Steptoe A. Shorter telomeres with high telomerase activity are associated with raised allostatic load and impoverished psychosocial resources. Proceedings of the National Academy of Sciences of the United States of America 2014, 111:4519-4524.
65. Zhang P., Dilley C., Mattson M.P. DNA damage responses in neural cells: focus on the telomere. Neuroscience 2007, 145(4):1439-1448.
66. Zhao F., Qu Y., Xiong T., Duan Z., Ye Q., Mu D. The neuroprotective role of TERT via an antiapoptotic mechanism in neonatal rats after hypoxia-ischemia brain injury. Neuroscience Letters 2012, 515:39-43.
67. Zhou Q.G., Hu Y., Wu D.L., Zhu L.J., Chen C., Jin X., Luo C.X., Wu H.Y., Zhang J., Zhu D.Y. Hippocampal telomerase is involved in the modulation of depressive behaviors. Journal of Neuroscience 2011, 31:12258-12269.
68. Zhu H., Fu W., Mattson M.P. The catalytic subunit of telomerase protects neurons against amyloid beta-peptide-induced apoptosis. Journal of Neurochemistry 2000, 75:117-124.