Different regulation of adult hippocampal neurogenesis in Western house mice (Mus musculus domesticus) and C57BL/6 mice

Behavioural Brain Research

Volumn 227, Issue 2, 2012, Pages 340-347

  Klaus, Fabienne ^a   Hauser, Thomas ^a   Lindholm, Anna K ^a   Cameron, Heather A ^b   Slomianka, Lutz ^a   Lipp, Hans Peter ^a   Amrein, Irmgard ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

Comparative; Context; Exercise; Motivation; Optical fractionator; Strain

Indexed keywords

DOUBLECORTIN;

ADULT HIPPOCAMPAL NEUROGENESIS; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; C57BL 6 MOUSE; CELL COUNT; CELL PROLIFERATION; CONTROLLED STUDY; FEMALE; MALE; MOUSE; MOUSE STRAIN; MUS MUSCULUS DOMESTICUS; NERVOUS SYSTEM DEVELOPMENT; NEUROBLAST; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; PROGENY; REGULATORY MECHANISM; RUNNING; STRAIN DIFFERENCE;

ANIMALS; CELL COUNT; CELL PROLIFERATION; FEMALE; HIPPOCAMPUS; MALE; MICE; MICE, INBRED C57BL; MOTIVATION; NEUROGENESIS; NEURONS; PHYSICAL CONDITIONING, ANIMAL; SPECIES SPECIFICITY;

EID: 84855930663     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2011.07.026     Document Type: Article

References (62)

1. Holmes M.M., Galea L.A.M., Mistlberger R.E., Kempermann G. Adult hippocampal neurogenesis and voluntary running activity: circadian and dose-dependent effects. J Neurosci Res 2004, 76:216-222.
2. Klaus F., Hauser T., Slomianka L., Lipp H.P., Amrein I. A reward increases running-wheel performance without changing cell proliferation, neuronal differentiation or cell death in the dentate gyrus of C57BL/6 mice. Behav Brain Res 2009, 204:175-181.
3. Olson A.K., Eadie B.D., Ernst C., Christie B.R. Environmental enrichment and voluntary exercise massively increase neurogenesis in the adult hippocampus via dissociable pathways. Hippocampus 2006, 16:250-260.
4. Van Praag H., Kempermann G., Gage F.H. Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci 1999, 2:266-270.
5. Kramer A.F., Erickson K.I., Colcombe S.J. Exercise, cognition, and the aging brain. J Appl Physiol 2006, 101:1237-1242.
6. Van Praag H., Christie B.R., Sejnowski T.J., Gage F.H. Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc Natl Acad Sci USA 1999, 96:13427-13431.
7. Van Praag H., Shubert T., Zhao C., Gage F.H. Exercise enhances learning and hippocampal neurogenesis in aged mice. J Neurosci 2005, 25:8680-8685.
8. Amrein I., Dechmann D.K., Winter Y., Lipp H.P. Absent or low rate of adult neurogenesis in the hippocampus of bats (Chiroptera). PLoS ONE 2007, 2:e455.
9. Bartkowska K., Djavadian R.L., Taylor J.R.E., Turlejski K. Generation recruitment and death of brain cells throughout the life cycle of Sorex shrews (Lipotyphla). Eur J Neurosci 2008, 27:1710-1721.
10. Adlard P.A., Perreau V.M., Pop V., Cotman C.W. Voluntary exercise decreases amyloid load in a transgenic model of Alzheimer's disease. J Neurosci 2005, 25:4217-4221.
11. Pietropaolo S., Sun Y., Li R., Brana C., Feldon J., Yee B.K. The impact of voluntary exercise on mental health in rodents: a neuroplasticity perspective. Behav Brain Res 2008, 192:42-60.
12. Solberg L.C., Horton T.H., Turek F.W. Circadian rhythms and depression: effects of exercise in an animal model. Am J Physiol Regul Integr Comp Physiol 1999, 276:R152-R161.
13. Lucassen P.J., Stumpel M.W., Wang Q., Aronica E. Decreased numbers of progenitor cells but no response to antidepressant drugs in the hippocampus of elderly depressed patients. Neuropharmacology 2010, 58:940-949.
14. Marlatt M.W., Lucassen P.J., Van Praag H. Comparison of neurogenic effects of fluoxetine, duloxetine and running in mice. Brain Res 2010, 1341:93-99.
15. Eriksson P.S., Perfilieva E., Björk-Eriksson T., Alborn A.M., Nordborg C., Peterson D.A., et al. Neurogenesis in the adult human hippocampus. Nat Med 1998, 4:1313-1317.
16. Kim Y.P., Kim H.B., Jang M.H., Lim B.V., Kim Y.J., Kim H., et al. Magnitude- and time-dependence of the effect of treadmill exercise on cell proliferation in the dentate gyrus of rats. Int J Sports Med 2003, 24:114-117.
17. Michaux J.R., Chevret P., Filippucci M.G., Macholan M. Phylogeny of the genus Apodemus with a special emphasis on the subgenus Sylvaemus using the nuclear IRBP gene and two mitochondrial markers: cytochrome b and 12S rRNA. Mol Phylogenet Evol 2002, 23:123-136.
18. Steppan S.J., Adkins R.M., Spinks P.Q., Hale C. Multigene phylogeny of the Old World mice, Murinae, reveals distinct geographic lineages and the declining utility of mitochondrial genes compared to nuclear genes. Mol Phylogenet Evol 2005, 37:370-388.
19. Hauser T., Klaus F., Lipp H.-P., Amrein I. No effect of running and laboratory housing on adult hippocampal neurogenesis in wild caught long-tailed wood mouse. BMC Neurosci 2009, 10:43.
20. Yang H., Bell T.A., Churchill G.A., de Villena F.P.M. On the subspecific origin of the laboratory mouse. Nat Genet 2007, 39:1100-1107.
21. Navailles S., Hof P.R., Schmauss C. Antidepressant drug-induced stimulation of mouse hippocampal neurogenesis is age-dependent and altered by early life stress. J Comp Neurol 2008, 509:372-381.
22. Eisch A.J., Mandyam C.D. Adult neurogenesis: can analysis of cell cycle proteins move us " Beyond Brdu"?. Curr Pharm Biotechnol 2007, 8:147-165.
23. Starborg M., Gell K., Brundell E., Höög C. The murine Ki-67 cell proliferation antigen accumulates in the nucleolar and heterochromatic regions of interphase cells and at the periphery of the mitotic chromosomes in a process essential for cell cycle progression. J Cell Sci 1996, 109:143-153.
24. Francis F., Koulakoff A., Boucher D., Chafey P., Schaar B., Vinet M.C., et al. Doublecortin is a developmentally regulated, microtubule-associated protein expressed in migrating and differentiating neurons. Neuron 1999, 23:247-256.
25. Koizumi H., Higginbotham H., Poon T., Tanaka T., Brinkman B.C., Gleeson J.G. Doublecortin maintains bipolar shape and nuclear translocation during migration in the adult forebrain. Nat Neurosci 2006, 9:779-786.
26. Koizumi H., Tanaka T., Gleeson J.G. doublecortin-like kinase functions with doublecortin to mediate fiber tract decussation and neuronal migration. Neuron 2006, 49:55-66.
27. Amrein I., Slomianka L., Lipp H.P. Granule cell number, cell death and cell proliferation in the dentate gyrus of wild-living rodents. Eur J Neurosci 2004, 20:3342-3350.
28. Heine V.M., Maslam S., Joels M., Lucassen P.J. Prominent decline of newborn cell proliferation, differentiation, and apoptosis in the aging dentate gyrus, in absence of an age-related hypothalamus-pituitary-adrenal axis activation. Neurobiol Aging 2004, 25:361-375.
29. Iñiguez C., Gayoso M.J., Carreres J. A versatile and simple method for staining nervous tissue using Giemsa dye. J Neurosci Methods 1985, 13:77-86.
30. West M.J., Slomianka L., Gundersen H.J. Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat Rec 1991, 231:482-497.
31. Gundersen H.J.G., Jensen E.B. The efficiency of systematic sampling in stereology and its prediction. J Microsc 1987, 147:229-263.
32. Gundersen H.J.G., Jensen E.B.V., Kieu K., Nielsen J. The efficiency of systematic sampling in stereology - reconsidered. J Microsc 1999, 193:199-211.
33. Slomianka L., West M.J. Estimators of the precision of stereological estimates: an example based on the CA1 pyramidal cell layer of rats. Neuroscience 2005, 136:757-767.
34. Redila V.A., Christie B.R. Exercise-induced changes in dendritic structure and complexity in the adult hippocampal dentate gyrus. Neuroscience 2006, 137:1299-1307.
35. Zhao C., Teng E.M., Summers R.G., Ming G.L., Gage F.H. Distinct morphological stages of dentate granule neuron maturation in the adult mouse hippocampus. J Neurosci 2006, 26:3-11.
36. Farmer J., Zhao X., Van Praag H., Wodtke K., Gage F.H., Christie B.R. Effects of voluntary exercise on synaptic plasticity and gene expression in the dentate gyrus of adult male Sprague-Dawley rats in vivo. Neuroscience 2004, 124:71-79.
37. O'Callaghan R.M., Ohle R., Kelly A.M. The effects of forced exercise on hippocampal plasticity in the rat: a comparison of LTP, spatial- and non-spatial learning. Behav Brain Res 2007, 176:362-366.
38. Adlard P.A., Perreau V.M., Engesser-Cesar C., Cotman C.W. The timecourse of induction of brain-derived neurotrophic factor mRNA and protein in the rat hippocampus following voluntary exercise. Neurosci Lett 2004, 363:43-48.
39. Eisenstein S.A., Holmes P.V. Chronic and voluntary exercise enhances learning of conditioned place preference to morphine in rats. Pharmacol Biochem Behav 2007, 86:607-615.
40. Samorajski T., Delaney C., Durham L., Ordy J.M., Johnson J.A., Dunlap W.P. Effect of exercise on longevity, body-weight, locomotor performance, and passive-avoidance memory of C57bl/6j mice. Neurobiol Aging 1985, 6:17-24.
41. Kempermann G., Gage F.H. Genetic determinants of adult hippocampal neurogenesis correlate with acquisition, but not probe trial performance, in the water maze task. Eur J Neurosci 2002, 16:129-136.
42. Kempermann G., Gage F.H. Genetic influence on phenotypic differentiation in adult hippocampal neurogenesis. Brain Res Dev Brain Res 2002, 134:1-12.
43. Kempermann G., Kuhn H.G., Gage F.H. Genetic influence on neurogenesis in the dentate gyrus of adult mice. Proc Natl Acad Sci USA 1997, 94:10409-10414.
44. Clark P.J., Brzezinska W.J., Puchalski E.K., Krone D.A., Rhodes J.S. Functional analysis of neurovascular adaptations to exercise in the dentate gyrus of young adult mice associated with cognitive gain. Hippocampus 2009, 19:937-950.
45. Thuret S., Toni N., Aigner S., Yeo G.W., Gage F.H. Hippocampus-dependent learning is associated with adult neurogenesis in MRL/MpJ mice. Hippocampus 2009, 19:658-669.
46. Snyder J.S., Glover L.R., Sanzone K.M., Kamhi J.F., Cameron A.H. The effects of exercise and stress on the survival and maturation of adult-generated granule cells. Hippocampus 2009, 19:898-906.
47. Berry R.J., Tattersall F.H., Hurst J. Genus Mus. Mammals of the British Isles: handbook 2008, 141-149. The Mammal Society, Southhampton, U.K. 4th ed. S. Harris, D.W. Yalden (Eds.).
48. Weidt A., Hofmann S.E., König B. Not only mate choice matters: fitness consequences of social partner choice in female house mice. Anim Behav 2008, 75:801-808.
49. Kempermann G. Why new neurons? Possible functions for adult hippocampal neurogenesis. J Neurosci 2002, 22:635-638.
50. Tong L.Q., Shen H., Perreau V.M., Balazs R., Cotman C.W. Effects of exercise on gene-expression profile in the rat hippocampus. Neurobiol Dis 2001, 8:1046-1056.
51. Clark P.J., Brzezinska W.J., Thomas M.W., Ryzhenko N.A., Toshkov S.A., Rhodes J.S. Intact neurogenesis is required for benefits of exercise on spatial memory but not motor performance or contextual fear conditioning in C57BL/6J mice. Neuroscience 2008, 155:1048-1058.
52. Lightfoot J.T., Leamy L., Pomp D., Turner M.J., Fodor A.A., Knab A., et al. Strain screen and haplotype association mapping of wheel running in inbred mouse strains. J Appl Physiol 2010, 109:623-634.
53. Lagace D.C., Fischer S.J., Eisch A.J. Gender and endogenous levels of estradiol do not influence adult hippocampal neurogenesis in mice. Hippocampus 2007, 17:175-180.
54. Ben Abdallah N.M.B., Slomianka L., Vyssotski A.L., Lipp H.-P. Early age-related changes in adult hippocampal neurogenesis in C57 mice. Neurobiol Aging 2010, 31:151-161.
55. Dohm M.R., Richardson C.S., Garland T. Exercise physiology of wild and random-bred laboratory house mice and their reciprocal hybrids. Am J Physiol Regul Integr Comp Physiol 1994, 36:R1098-R1108.
56. Snyder J.S., Choe J.S., Clifford M.A., Jeurling S.I., Hurley P., Brown A., et al. Adult-born hippocampal neurons are more numerous, faster maturing, and more involved in behavior in rats than in mice. J Neurosci 2009, 29:14484-14495.
57. Gould E., McEwen B.S., Tanapat P., Galea L.A.M., Fuchs E. Neurogenesis in the dentate gyrus of the adult tree shrew is regulated by psychosocial stress and NMDA receptor activation. J Neurosci 1997, 17:2492-2498.
58. Heine V.M., Maslam S., Zareno J., Joëls M., Lucassen P.J. Suppressed proliferation and apoptotic changes in the rat dentate gyrus after acute and chronic stress are reversible. Eur J Neurosci 2004, 19:131-144.
59. Malberg J.E., Duman R.S. Cell proliferation in adult hippocampus is decreased by inescapable stress: reversal by fluoxetine treatment. Neuropsychopharmacology 2003, 28:1562-1571.
60. Tanapat P., Hastings N.B., Rydel T.A., Galea L.A.M., Gould E. Exposure to fox odor inhibits cell proliferation in the hippocampus of adult rats via an adrenal hormone-dependent mechanism. J Comp Neurol 2001, 437:496-504.
61. Stranahan A.M., Khalil D., Gould E. Social isolation delays the positive effects of running on adult neurogenesis. Nat Neurosci 2006, 9:526-533.
62. Fiore M., Amedola T., Triaca V., Alleva E., Aloe L. Fighting in the aged male mouse increases the expression of TrkA and TrkB in the subventricular zone and in the hippocampus. Behav Brain Res 2005, 157:351-362.