Experimental 'jet lag' inhibits adult neurogenesis and produces long-term cognitive deficits in female hamsters

PLoS ONE

Volumn 5, Issue 12, 2010, Pages

  Gibson, Erin M ^a   Wang, Connie ^a   Tjho, Stephanie ^a   Khattar, Neera ^a   Kriegsfeld, Lance J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOCORTICOID; SEX HORMONE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN FUNCTION; CELL PROLIFERATION; CIRCADIAN RHYTHM; COGNITIVE DEFECT; CONTROLLED STUDY; DENTATE GYRUS; DISEASE ASSOCIATION; FEMALE; HAMSTER; HIPPOCAMPUS; JET LAG; LIGHT DARK CYCLE; MENTAL STRESS; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PLACE PREFERENCE; ANIMAL; BRAIN; DISEASE MODEL; HYPOTHALAMUS HYPOPHYSIS SYSTEM; MEMORY; METABOLISM; NERVE CELL; PATHOLOGY; PATHOPHYSIOLOGY; SLEEP;

CRICETINAE;

ANIMALS; BRAIN; CELL PROLIFERATION; COGNITION DISORDERS; CRICETINAE; DISEASE MODELS, ANIMAL; FEMALE; GLUCOCORTICOIDS; HIPPOCAMPUS; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; JET LAG SYNDROME; MEMORY; NEURONS; SLEEP;

EID: 78649933286     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0015267     Document Type: Article

References (81)

1. Davidson AJ, Castanon-Cervantes O, Leise TL, Molyneux PC, Harrington ME (2009) Visualizing jet lag in the mouse suprachiasmatic nucleus and peripheral circadian timing system. Eur J Neurosci 29:171-180
2. Maywood ES, O'Neill J, Wong GK, Reddy AB, Hastings MH (2006) Circadian timing in health and disease. Prog Brain Res 153:253-269
3. Reddy AB, Field MD, Maywood ES, Hastings MH (2002) Differential resynchronisation of circadian clock gene expression within the suprachiasmatic nuclei of mice subjected to experimental jet lag. J Neurosci 22: 7326-7330.
4. Wittmann M, Dinich J, Merrow M, Roenneberg T (2006) Social jetlag: misalignment of biological and social time. Chronobiol Int 23:497-509
5. Hansen J (2006) Risk of breast cancer after night-and shift work: current evidence and ongoing studies in Denmark. Cancer Causes Control 17: 531-537.
6. Conlon M, Lightfoot N, Kreiger N (2007) Rotating shift work and risk of prostate cancer. Epidemiology 18:182-183
7. Poole CJ, Wright AD, Nattrass M (1992) Control of diabetes mellitus in shift workers. Br J Ind Med 49:513-515
8. Ha M, Park J (2005) Shiftwork and metabolic risk factors of cardiovascular disease. J Occup Health 47:89-95
9. Kivimaki M, Virtanen M, Elovainio M, Vaananen A, Keltikangas-Jarvinen L, et al. (2006) Prevalent cardiovascular disease, risk factors and selection out of shift work. Scand J Work Environ Health 32:204-208
10. Ahlborg G, Axelsson G, Bodin L (1996) Shift work, nitrous oxide exposure and subfertility among Swedish Midwives. Int J Epidemiology 25:783-790
11. Zhu JL, Hjollund NH, Olsen J (2004) Shift work, duration of pregnancy, and birth weight: the National Birth Cohort in Denmark. Am J Obstet Gynecol 191:285-291
12. Skipper JK, Jr., Jung FD, Coffey LC (1990) Nurses and shiftwork: effects on physical health and mental depression. J Adv Nurs 15:835-842
13. Bildt C, Michelsen H (2002) Gender differences in the effects from working conditions on mental health: a 4-year follow-up. Int Arch Occup Environ Health 75:252-258
14. Tapp WN, Holloway FA (1981) Phase shifting circadian rhythms produces retrograde amnesia. Science 211:1056-1058
15. Ralph MR, Ko CH, Antoniadis EA, Seco P, Irani F, et al. (2002) The significance of circadian phase for performance on a reward-based learning task in hamsters. Behav Brain Res 136:179-184
16. Cho K (2001) Chronic 'jet lag' produces temporal lobe atrophy and spatial cognitive deficits. Nat Neurosci 4:567-568
17. Cho K, Ennaceur A, Cole JC, Suh CK (2000) Chronic jet lag produces cognitive deficits. J Neurosci 20: RC66.
18. Moore RY, Eichler VB (1972) Loss of a circadian adrenal corticosterone rhythm following suprachiasmatic lesions in the rat. Brain Res 42:201-206
19. Stephan FK, Zucker I (1972) Rat drinking rhythms: central visual pathways and endocrine factors mediating responsiveness to environmental illumination. Physiol Behav 8:315-326
20. Dibner C, Schibler U, Albrecht U (2010) The mammalian circadian timing system: organization and coordination of central and peripheral clocks. Annu Rev Physiol 72:517-549
21. Reppert SM, Weaver DR (2002) Coordination of circadian timing in mammals. Nature 418:935-941
22. Chen R, Schirmer A, Lee Y, Lee H, Kumar V, et al. (2009) Rhythmic PER abundance defines a critical nodal point for negative feedback within the circadian clock mechanism. Mol Cell 36:417-430
23. Van Gelder RN, Herzog ED, Schwartz WJ, Taghert PH (2003) Circadian rhythms: in the loop at last. Science 300:1534-1535
24. Maywood ES, O'Neill JS, Reddy AB, Chesham JE, Prosser HM, et al. (2007) Genetic and molecular analysis of the central and peripheral circadian clockwork of mice. Cold Spring Harb Symp Quant Biol 72:85-94
25. Gould E, Beylin A, Tanapat P, Reeves A, Shors TJ (1999) Learning enhances adult neurogenesis in the hippocampal formation. Nat Neurosci 2:260-265
26. Ambrogini P, Cuppini R, Cuppini C, Ciaroni S, Cecchini T, et al. (2000) Spatial learning affects immature granule cell survival in adult rat dentate gyrus. Neurosci Lett 286:21-24
27. Leuner B, Gould E, Shors TJ (2006) Is there a link between adult neurogenesis and learning? Hippocampus 16:216-224
28. Van der Borght K, Meerlo P, Luiten PG, Eggen BJ, Van der Zee EA (2005) Effects of active shock avoidance learning on hippocampal neurogenesis and plasma levels of corticosterone. Behav Brain Res 157:23-30
29. Clelland CD, Choi M, Romberg C, Clemenson GD Jr, Fragniere A, et al. (2009) A functional role for adult hippocampal neurogenesis in spatial pattern separation. Science 325:210-213
30. Madsen TM, Kristjansen PE, Bolwig TG, Wortwein G (2003) Arrested neuronal proliferation and impaired hippocampal function following fractionated brain irradiation in the adult rat. Neuroscience 119:635-642
31. Madsen TM, Newton SS, Eaton ME, Russell DS, Duman RS (2003) Chronic electroconvulsive seizure up-regulates beta-catenin expression in rat hippocampus: role in adult neurogenesis. Biol Psychiatry 54:1006-1014
32. Shors TJ, Miesegaes G, Beylin A, Zhao M, Rydel T, et al. (2001) Neurogenesis in the adult is involved in the formation of trace memories. Nature 410:372-376
33. Mirescu C, Gould E (2006) Stress and adult neurogenesis. Hippocampus 16:233-238
34. Galea LA (2008) Gonadal hormone modulation of neurogenesis in the dentate gyrus of adult male and female rodents. Brain Res Rev 57:332-341
35. Dagyte G, Van der Zee EA, Postema F, Luiten PG, Den Boer JA, et al. (2009) Chronic but not acute foot-shock stress leads to temporary suppression of cell proliferation in rat hippocampus. Neuroscience 162:904-913
36. Shors TJ (2006) Stressful experience and learning across the lifespan. Annu Rev Psychol 57:55-85
37. Daniel JM, Fader AJ, Spencer AL, Dohanich GP (1997) Estrogen enhances performance of female rats during acquisition of a radial arm maze. Horm Behav 32:217-225
38. Galea LA, Uban KA, Epp JR, Brummelte S, Barha CK, et al. (2008) Endocrine regulation of cognition and neuroplasticity: our pursuit to unveil the complex interaction between hormones, the brain, and behaviour. Can J Exp Psychol 62:247-260
39. Gould E, Tanapat P (1999) Stress and hippocampal neurogenesis. Biol Psychiatry 46:1472-1479
40. Borgs L, Beukelaers P, Vandenbosch R, Nguyen L, Moonen G, et al. (2009) Period 2 regulates neural stem/progenitor cell proliferation in the adult hippocampus. BMC Neurosci 10: 30.
41. Borgs L, Beukelaers P, Vandenbosch R, Belachew S, Nguyen L, et al. (2009) Cell ''circadian'' cycle: new role for mammalian core clock genes. Cell Cycle 8:832-837
42. Davidson AJ, Sellix MT, Daniel J, Yamazaki S, Menaker M, et al. (2006) Chronic jet-lag increases mortality in aged mice. Curr Biol 16: R914-916.
43. Filipski E, Delaunay F, King VM, Wu MW, Claustrat B, et al. (2004) Effects of chronic jet lag on tumor progression in mice. Cancer Res 64:7879-7885
44. Yamazaki S, Numano R, Abe M, Hida A, Takahashi R, et al. (2000) Resetting central and peripheral circadian oscillators in transgenic rats. Science 288:682-685
45. Takamure M, Murakami N, Takahashi K, Kuroda H, Etoh T (1991) Rapid reentrainment of the circadian clock itself, but not the measurable activity rhythms to a new light-dark cycle in the rat. Physiol Behav 50:443-449
46. Loh DH, Navarro J, Hagopian A, Wang LM, Deboer T, et al. (2010) Rapid changes in the light/dark cycle disrupt memory of conditioned fear in mice. PLoS One 5.
47. Orsini M (1961) The external vaginal phenomena characterizing the stages of the estrous cycle, pregnancy, pseudopregnancy, lactation and anestrous hamster, Mesocricetus auratus Waterhouse. Proceedings of Animal Care Panel 14:193-206
48. Meyer-Bernstein EL, Jetton AE, Matsumoto SI, Markuns JF, Lehman MN, et al. (1999) Effects of suprachiasmatic transplants on circadian rhythms of neuroendocrine function in golden hamsters. Endocrinology 140:207-218
49. Ottenweller JE, Tapp WN, Burke JM, Natelson BH (1985) Plasma cortisol and corticosterone concentrations in the golden hamster, (Mesocricetus auratus). Life Sci 37:1551-1558
50. Mirescu C, Peters JD, Gould E (2004) Early life experience alters response of adult neurogenesis to stress. Nat Neurosci 7:841-846
51. Kempermann G, Kuhn HG, Gage FH (1997) Genetic influence on neurogenesis in the dentate gyrus of adult mice. Proc Natl Acad Sci U S A 94:10409-10414
52. Glenn MJ, Gibson EM, Kirby ED, Mellott TJ, Blusztajn JK, et al. (2007) Prenatal choline availability modulates hippocampal neurogenesis and neurogenic responses to enriching experiences in adult female rats. Eur J Neurosci 25:2473-2482
53. Gundersen HJ, Jensen EB (1987) The efficiency of systematic sampling in stereology and its prediction. J Microsc 147:229-263
54. Epp JR, Spritzer MD, Galea LA (2007) Hippocampus-dependent learning promotes survival of new neurons in the dentate gyrus at a specific time during cell maturation. Neuroscience 149:273-285
55. Ferbinteanu J, McDonald RJ (2001) Dorsal/ventral hippocampus, fornix, and conditioned place preference. Hippocampus 11:187-200
56. Cain SW, Karatsoreos I, Gautam N, Konar Y, Funk D, et al. (2004) Blunted cortisol rhythm is associated with learning impairment in aged hamsters. Physiol Behav 82:339-344
57. Frick KM, Berger-Sweeney J (2001) Spatial reference memory and neocortical neurochemistry vary with the estrous cycle in C57BL/6 mice. Behav Neurosci 115:229-237
58. Anand S, Losee-Olson S, Turek FW, Horton TH (2002) Differential regulation of luteinizing hormone and follicle-stimulating hormone in male siberian hamsters by exposure to females and photoperiod. Endocrinology 143:2178-2188
59. Anand S, Turek FW, Horton TH (2004) Chemosensory stimulation of luteinizing hormone secretion in male Siberian hamsters (Phodopus sungorus). Biol Reprod 70:1033-1040
60. Cameron HA, Gould E (1994) Adult neurogenesis is regulated by adrenal steroids in the dentate gyrus. Neuroscience 61:203-209
61. Barker JM, Galea LA (2008) Repeated estradiol administration alters different aspects of neurogenesis and cell death in the hippocampus of female, but not male, rats. Neuroscience 152:888-902
62. Tanapat P, Hastings NB, Rydel TA, Galea LA, Gould E (2001) Exposure to fox odor inhibits cell proliferation in the hippocampus of adult rats via an adrenal hormone-dependent mechanism. J Comp Neurol 437:496-504
63. Lee KJ, Kim SJ, Kim SW, Choi SH, Shin YC, et al. (2006) Chronic mild stress decreases survival, but not proliferation, of new-born cells in adult rat hippocampus. Exp Mol Med 38:44-54
64. Jessberger S, Clark RE, Broadbent NJ, Clemenson GD Jr, Consiglio A, et al. (2009) Dentate gyrus-specific knockdown of adult neurogenesis impairs spatial and object recognition memory in adult rats. Learn Mem 16:147-154
65. Golombek DA, Cardinali DP (1993) Melatonin accelerates reentrainment after phase advance of the light-dark cycle in Syrian hamsters: antagonism by flumazenil. Chronobiol Int 10:435-441
66. Anderson MC (2003) Rethinking interference theory: Executive control and the mechanisms of forgetting. J Mem Lang 49:415-445
67. Jasnow AM, Drazen DL, Huhman KL, Nelson RJ, Demas GE (2001) Acute and chronic social defeat suppresses humoral immunity of male Syrian hamsters (Mesocricetus auratus). Horm Behav 40:428-433
68. Ruby NF, Hwang CE, Wessells C, Fernandez F, Zhang P, et al. (2008) Hippocampal-dependent learning requires a functional circadian system. Proc Natl Acad Sci U S A 105:15593-15598
69. Mirescu C, Peters JD, Noiman L, Gould E (2006) Sleep deprivation inhibits adult neurogenesis in the hippocampus by elevating glucocorticoids. Proc Natl Acad Sci U S A 103:19170-19175
70. Mueller AD, Pollock MS, Lieblich SE, Epp JR, Galea LA, et al. (2008) Sleep deprivation can inhibit adult hippocampal neurogenesis independent of adrenal stress hormones. Am J Physiol Regul Integr Comp Physiol 294: R1693-1703.
71. Barha CK, Lieblich SE, Galea LA (2009) Different forms of oestrogen rapidly upregulate cell proliferation in the dentate gyrus of adult female rats. J Neuroendocrinol 21:155-166
72. Cameron HA, Hazel TG, McKay RD (1998) Regulation of neurogenesis by growth factors and neurotransmitters. J Neurobiol 36:287-306
73. Frielingsdorf H, Simpson DR, Thal LJ, Pizzo DP (2007) Nerve growth factor promotes survival of new neurons in the adult hippocampus. Neurobiol Dis 26:47-55
74. Sei H, Fujihara H, Ueta Y, Morita K, Kitahama K, et al. (2003) Single eighthour shift of light-dark cycle increases brain-derived neurotrophic factor protein levels in the rat hippocampus. Life Sci 73:53-59
75. Pizzio GA, Hainich EC, Plano SA, Ralph MR, Golombek DA (2005) Nerve growth factor-induced circadian phase shifts and MAP kinase activation in the hamster suprachiasmatic nuclei. Eur J Neurosci 22:665-671
76. Hunt T, Sassone-Corsi P (2007) Riding tandem: circadian clocks and the cell cycle. Cell 129:461-464
77. Walisser JA, Bradfield CA (2006) A time to divide: does the circadian clock control cell cycle? Dev Cell 10:539-540
78. Raber J, Rola R, LeFevour A, Morhardt D, Curley J, et al. (2004) Radiationinduced cognitive impairments are associated with changes in indicators of hippocampal neurogenesis. Radiat Res 162:39-47
79. Raber J, Fan Y, Matsumori Y, Liu Z, Weinstein PR, et al. (2004) Irradiation attenuates neurogenesis and exacerbates ischemia-induced deficits. Ann Neurol 55:381-389
80. Snyder JS, Hong NS, McDonald RJ, Wojtowicz JM (2005) A role for adult neurogenesis in spatial long-term memory. Neuroscience 130:843-852
81. Walker MP, Stickgold R (2006) Sleep, memory, and plasticity. Annu Rev Psychol 57:139-166