Dynamics of olfactory and hippocampal neurogenesis in adult sheep

Journal of Comparative Neurology

Volumn 521, Issue 1, 2013, Pages 169-188

  Brus, M ^a,b,c,d   Meurisse, M ^a,b,c,d   Gheusi, G ^b,e   Keller, M ^a,b,c,d   Lledo, P M ^b,e   Levy F ^a,b,c,d  

^a UMR85 PHYSIOLOGIE DE LA REPRODUCTION ET DES COMPORTEMENTS   (France)

^b CNRS   (France)

^c UNIVERSITÉ DE TOURS   (France)

^d Haras Nationaux   (France)

^e INSTITUT PASTEUR   (France)

Author keywords

Adeno associated virus; Gliogenesis; Migratory stream; Neuroblasts; Neuronal maturation

Indexed keywords

BIOLOGICAL MARKER; BROXURIDINE; DOUBLECORTIN; GLIAL FIBRILLARY ACIDIC PROTEIN; NEURON SPECIFIC NUCLEAR PROTEIN; PROTEIN C FOS; PROTEIN S 100; TRANSCRIPTION FACTOR SOX2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOLOGICAL MODEL; CELL DENSITY; CELL DIVISION; CELL MATURATION; CELL MIGRATION; CELL SURVIVAL; COMPARATIVE STUDY; DENTATE GYRUS; FEMALE; HIPPOCAMPAL NEUROGENESIS; NERVE CONDUCTION; NERVOUS SYSTEM DEVELOPMENT; NEUROBLAST; NEWBORN; NONHUMAN; OLFACTORY BULB; OLFACTORY NEUROGENESIS; PHENOTYPE; PRIMATE; PRIORITY JOURNAL; RAT; SHEEP; SUBVENTRICULAR ZONE; SURVIVAL TIME;

ADULT STEM CELLS; AGE FACTORS; ANIMALS; BROMODEOXYURIDINE; CELL COUNT; CELL DIFFERENTIATION; CELL MOVEMENT; FEMALE; GREEN FLUORESCENT PROTEINS; HIPPOCAMPUS; HUMANS; LATERAL VENTRICLES; NERVE TISSUE PROTEINS; NEUROGENESIS; OLFACTORY BULB; PROTO-ONCOGENE PROTEINS C-FOS; SHEEP; SOXB1 TRANSCRIPTION FACTORS; TRANSDUCTION, GENETIC;

EID: 84867090525     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.23169     Document Type: Article

References (76)

1. Alonso M, Ortega-Pérez I, Grubb MS, Bourgeois J-P, Charneau P, Lledo P-M. 2008. Turning astrocytes from the rostral migratory stream into neurons: a role for the olfactory sensory organ. J Neurosci 28: 11089-11102.
2. Altman J. 1969. Autoradiographic and histological studies of postnatal neurogenesis. IV. Cell proliferation and migration in the anterior forebrain, with special reference to persisting neurogenesis in the olfactory bulb. J Comp Neurol 137: 433-457.
3. Banasr M, Hery M, Brezun JM, Daszuta A. 2001. Serotonin mediates oestrogen stimulation of cell proliferation in the adult dentate gyrus. Eur J Neurosci 14: 1417-1424.
4. Belnoue L, Grosjean N, Abrous DN, Koehl M. 2011. A critical time window for the recruitment of bulbar newborn neurons by olfactory discrimination learning. J Neurosci 31: 1010-1016.
5. Bosch TJ, Maslam S, Roberts BL. 2001. Fos-like immunohistochemical identification of neurons active during the startle response of the rainbow trout. J Comp Neurol 439: 306-314.
6. Broadwell RD. 1975. Olfactory relationships of telencephalon and diencephalon in rabbit. 2. Autoradiographic and horseradish-peroxidase study of efferent connections of anterior olfactory nucleus. J Comp Neurol 164: 389-409.
7. Brown JP, Couillard-Despres S, Cooper-Kuhn CM, Winkler J, Aigner L, Kuhn HG. 2003. Transient expression of doublecortin during adult neurogenesis. J Comp Neurol 467: 1-10.
8. Brus M, Meurisse M, Franceschini I, Keller M, Levy F. 2010. Evidence for cell proliferation in the sheep brain and its down-regulation by parturition and interactions with the young. Horm Behav 58: 737-746.
9. Cameron HA, Woolley CS, McEwen BS, Gould E. 1993. Differentiation of newly born neurons and glia in the dentate gyrus of the adult rat. Neuroscience 56: 337-344.
10. Castellano B, Gonzalez B, Jensen MB, Pedersen EB, Finsen BR, Zimmer J. 1991. A double staining technique for simultaneous demonstration of astrocytes and microglia in brain sections and astroglial cell cultures. J Histochem Cytochem 39: 561-568.
11. Chaillou E, Baumont R, Tramu G, Tillet Y. 2000. Effect of feeding on Fos protein expression in sheep hypothalamus with special reference to the supraoptic and paraventricular nuclei: an immunohistochemical study. Eur J Neurosci 12: 4515-4524.
12. Curtis MA, Kam M, Nannmark U, Anderson MF, Axell MZ, Wikkelso C, Holtas S, van Roon-Mom WMC, Bjork-Eriksson T, Nordborg C, Frisen J, Dragunow M, Faull RLM, Eriksson PS. 2007. Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension. Science 315: 1243-1249.
13. Dayer AG, Ford AA, Cleaver KM, Yassaee M, Cameron HA. 2003. Short-term and long-term survival of new neurons in the rat dentate gyrus. J Comp Neurol 460: 563-572.
14. Doetsch F, Alvarez-Buylla A. 1996. Network of tangential pathways for neuronal migration in adult mammalian brain. Proc Natl Acad Sci U S A 93: 14895-14900.
15. Doetsch F, Garcia-Verdugo JM, Alvarez-Buylla A. 1997. Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J Neurosci 17: 5046-5061.
16. Dufourny L, Migaud M, Thiery J-C, Malpaux B. 2008. Development of an in vivo adeno-associated virus-mediated siRNA approach to knockdown tyrosine hydroxylase in the lateral retrochiasmatic area of the ovine brain. J Neurosci Methods 170: 56-66.
17. Ennis M, Hamilton, KA, Hayar A. 2007. Neurochemistry of the main olfactory system. In: Handbook of neurochemistry and molecular neurobiology. Heidelberg: Springer. p 137-204.
18. Episkopou V. 2005. SOX2 functions in adult neural stem cells. Trends Neurosci 28: 219-221.
19. Epp JR, Scott NA, Galea LAM. 2011. Strain differences in neurogenesis and activation of new neurons in the dentate gyrus in response to spatial learning. Neuroscience 172: 342-354.
20. Eriksson PS, Perfilieva E, Bjork-Eriksson T, Alborn AM, Nordborg C, Peterson DA, Gage FH. 1998. Neurogenesis in the adult human hippocampus. Nat Med 4: 1313-1317.
21. Ferri ALM, Cavallaro M, Braida D, Di Cristofano A, Canta A, Vezzani A, Ottolenghi S, Pandolfi PP, Sala M, DeBiasi S, Nicolis SK. 2004. Sox2 deficiency causes neurodegeneration and impaired neurogenesis in the adult mouse brain. Development 131: 3805-3819.
22. Furuta M, Bridges RS. 2005. Gestation-induced cell proliferation in the rat brain. Brain Res Dev Brain Res 156: 61-66.
23. Gelez H, Fabre-Nys C. 2006. Role of the olfactory systems and importance of learning in the ewes' response to rams or their odors. Reprod Nutr Dev 46: 401-415.
24. Geraerts M, Eggermont K, Hernandez-Acosta P, Garcia-Verdugo J-M, Baekelandt V, Debyser Z. 2006. Lentiviral vectors mediate efficient and stable gene transfer in adult neural stem cells in vivo. Hum Gene Ther 17: 635-650.
25. Gil-Perotin S, Duran-Moreno M, Belzunegui S, Luquin MR, Garcia-Verdugo JM. 2009. Ultrastructure of the subventricular zone in Macaca fascicularis and evidence of a mouse-like migratory stream. J Comp Neurol 514: 533-554.
26. Gleeson JG, Lin PT, Flanagan LA, Walsh CA. 1999. Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons. Neuron 23: 257-271.
27. Gould E, Reeves AJ, Fallah M, Tanapat P, Gross CG, Fuchs E. 1999. Hippocampal neurogenesis in adult Old World primates. Proc Natl Acad Sci U S A 96: 5263-5267.
28. Hansen SH, Stagaard M, Mollgard K. 1989. Neurofilament-like pattern of reactivity in human foetal PNS and spinal cord following immunostaining with polyclonal anti-glial fibrillary acidic protein antibodies. J Neurocytol 18: 427-436.
29. Hill T, Lewicki P. 2007. Statistics: methods and applications. Tulsa, OK: Statsoft.
30. Imayoshi I, Sakamoto M, Ohtsuka T, Takao K, Miyakawa T, Yamaguchi M, Mori K, Ikeda T, Itohara S, Kageyama R. 2008. Roles of continuous neurogenesis in the structural and functional integrity of the adult forebrain. Nat Neurosci 11: 1153-1161.
31. Ishii Y, Matsumoto Y, Watanabe R, Elmi M, Fujimori T, Nissen J, Cao Y, Nabeshima Y-I, Sasahara M, Funa K. 2008. Characterization of neuroprogenitor cells expressing the PDGF beta-receptor within the subventricular zone of postnatal mice. Mol Cell Neurosci 37: 507-518.
32. Jackson EL, Garcia-Verdugo JM, Gil-Perotin S, Roy M, Quinones-Hinojosa A, VandenBerg S, Alvarez-Buylla A. 2006. PDGFR alpha-positive B cells are neural stem cells in the adult SVZ that form glioma-like growths in response to increased PDGF signaling. Neuron 51: 187-199.
33. Jessberger S, Kempermann G. 2003. Adult-born hippocampal neurons mature into activity-dependent responsiveness. Eur J Neurosci 18: 2707-2712.
34. Keller M, Meurisse M, Levy F. 2004. Mapping the neural substrates involved in maternal responsiveness and lamb olfactory memory in parturient ewes using Fos imaging. Behav Neurosci 118: 1274-1284.
35. Kempermann G, Gast D, Kronenberg G, Yamaguchi M, Gage FH. 2003. Early determination and long-term persistence of adult-generated new neurons in the hippocampus of mice. Development 130: 391-399.
36. Kohler SJ, Williams NI, Stanton GB, Cameron JL, Greenough WT. 2011. Maturation time of new granule cells in the dentate gyrus of adult macaque monkeys exceeds six months. Proc Natl Acad Sci U S A 108: 10326-10331.
37. Kornack DR, Rakic P. 1999. Continuation of neurogenesis in the hippocampus of the adult macaque monkey. Proc Natl Acad Sci U S A 96: 5768-5773.
38. Kornack DR, Rakic P. 2001. The generation, migration, and differentiation of olfactory neurons in the adult primate brain. Proc Natl Acad Sci U S A 98: 4752-4757.
39. Lai B, Mao XO, Xie L, Jin K, Greenberg DA. 2008. Electrophysiological neurodifferentiation of subventricular zone-derived precursor cells following stroke. Neurosci Lett 442: 305-308.
40. Larsen CM, Grattan DR. 2010. Prolactin-induced mitogenesis in the subventricular zone of the maternal brain during early pregnancy is essential for normal postpartum behavioral responses in the mother. Endocrinology 151: 3805-3814.
41. Lévy F, Keller M. 2009. Olfactory mediation of maternal behavior in selected mammalian species. Behav Brain Res 200: 336-345.
42. Llorens-Martin M, Trejo JL. 2011. Multiple birthdating analyses in adult neurogenesis: a line-up of the usual suspects. Front Neurosci 5: 76.
43. Lois C, GarciaVerdugo JM, AlvarezBuylla A. 1996. Chain migration of neuronal precursors. Science 271: 978-981.
44. Luskin MB. 1993. Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron 11: 173-189.
45. Luzzati F, Peretto P, Aimar P, Ponti G, Fasolo A, Bonfanti L. 2003. Glia-independent chains of neuroblasts through the subcortical parenchyma of the adult rabbit brain. Proc Natl Acad Sci U S A 100: 13036-13041.
46. Malaeb SN, Hovanesian V, Sarasin MD, Hartmann SM, Sadowska GB, Stonestreet BS. 2009. Effects of maternal antenatal glucocorticoid treatment on apoptosis in the ovine fetal cerebral cortex. J Neurosci Res 87: 179-189.
47. Mamber C, Verhaagen J, Hol EM. 2010. In vivo targeting of subventricular zone astrocytes. Prog Neurobiol 92: 19-32.
48. Marín-Burgin A, Schinder AF. 2011. Requirement of adult-born neurons for hippocampus-dependent learning. Behav Brain Res (in press).
49. McDonald HY, Wojtowicz JM. 2005. Dynamics of neurogenesis in the dentate gyrus of adult rats. Neurosci Lett 385: 70-75.
50. Migaud M, Batailler M, Segura S, Duittoz A, Franceschini I, Pillon D. 2010. Emerging new sites for adult neurogenesis in the mammalian brain: a comparative study between the hypothalamus and the classical neurogenic zones. Eur J Neurosci 32: 2042-2052.
51. Migaud M, Batailler M, Pillon D, Franceschini I, Malpaux B. 2011. Seasonal changes in cell proliferation in the adult sheep brain and pars tuberalis. J Biol Rhythms 26: 486-496.
52. Morgan JI, Curran T. 1989. Stimulus-transcription coupling in neurons-role of cellular immediate-early gene. Trends Neurosci 12: 459-462.
53. Mullen RJ, Buck CR, Smith AM. 1992. NeuN, a neuronal specific nuclear-protein in vertebrates. Development 116: 201-211.
54. Nacher J, Crespo C, McEwen BS. 2001. Doublecortin expression in the adult rat telencephalon. Eur J Neurosci 14: 629-644.
55. Nissant A, Bardy C, Katagiri H, Murray K, Lledo P-M. 2009. Adult neurogenesis promotes synaptic plasticity in the olfactory bulb. Nat Neurosci 12: 728-730.
56. Pawluski JL, Barakauskas VE, Galea LAM. 2010. Pregnancy decreases oestrogen receptor α expression and pyknosis, but not cell proliferation or survival, in the hippocampus. J Neuroendocrinol 22: 248-257.
57. Pawluski JL, van den Hove DLA, Rayen I, Prickaerts J, Steinbusch HWM. 2011. Stress and the pregnant female: Impact on hippocampal cell proliferation, but not affective-like behaviors. Horm Behav 59: 572-580.
58. Peretto P, Giachino C, Aimar P, Fasolo A, Bonfanti L. 2005. Chain formation and glial tube assembly in the shift from neonatal to adult subventricular zone of the rodent forebrain. J Comp Neurol 487: 407-427.
59. Petreanu L, Alvarez-Buylla A. 2002. Maturation and death of adult-born olfactory bulb granule neurons: role of olfaction. J Neurosci 22: 6106-6113.
60. Ponti G, Aimar P, Bonfanti L. 2006. Cellular composition and cytoarchitecture of the rabbit subventricular zone and its extensions in the forebrain. J Comp Neurol 498: 491-507.
61. Quinones-Hinojosa A, Sanai N, Soriano-Navarro M, Gonzalez-Perez O, Mirzadeh Z, Gil-Perotin S, Romero-Rodriguez R, Berger MS, Garcia-Verdugo JM, Alvarez-Buylla A. 2006. Cellular composition and cytoarchitecture of the adult human subventricular zone: a niche of neural stem cells. J Comp Neurol 494: 415-434.
62. Rodriguez-Perez LM, Perez-Martin M, Jimenez AJ, Fernandez-Llebrez P. 2003. Immunocytochemical characterisation of the wall of the bovine lateral ventricle. Cell Tissue Res 314: 325-335.
63. Salvetti A, Oreve S, Chadeuf G, Favre D, Cherel Y, Champion-Arnaud P, David-Ameline J, Moullier P. 1998. Factors influencing recombinant adeno-associated virus production. Hum Gene Ther 9: 695-706.
64. Sanai N, Tramontin AD, Quinones-Hinojosa A, Barbaro NM, Gupta N, Kunwar S, Lawton MT, McDermott MW, Parsa AT, Verdugo JMG, Berger MS, Alvarez-Buylla A. 2004. Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature 427: 740-744.
65. Sanai N, Nguyen T, Ihrie RA, Mirzadeh Z, Tsai H-H, Wong M, Gupta N, Berger MS, Huang E, Garcia-Verdugo J-M, Rowitch DH, Alvarez-Buylla A. 2011. Corridors of migrating neurons in the human brain and their decline during infancy. Nature [E-pub ahead of print].
66. Sawamoto K, Hirota Y, Alfaro-Cervello C, Soriano-Navarro M, He XP, Hayakawa-Yano Y, Yamada M, Hikishima K, Tabata H, Iwanami A, Nakajima K, Toyama Y, Itoh T, Alvarez-Buylla A, Garcia-Verdugo JM, Okano H. 2011. Cellular composition and organization of the subventricular zone and rostral migratory stream in the adult and neonatal common marmoset brain. J Comp Neurol 519: 690-713.
67. Shepherd GM. 1972. Synaptic organization of the mammalian olfactory bulb. Physiol Rev 52: 864-917.
68. Shingo T, Gregg C, Enwere E, Fujikawa H, Hassam R, Geary C, Cross JC, Weiss S. 2003. Pregnancy-stimulated neurogenesis in the adult female forebrain mediated by prolactin. Science 299: 117-120.
69. Siegel S. 1956. Nonparametric Statistics for the Behavioral Sciences. Tokyo: McGraw-Hill.
70. Sliwowska JH, Billings HJ, Goodman RL, Coolen LM, Lehman MN. 2004. The premammillary hypothalamic area of the ewe: anatomical characterization of a melatonin target area mediating seasonal reproduction. Biol Reprod 70: 1768-1775.
71. Steiner B, Kronenberg G, Jessberger S, Brandt MD, Reuter K, Kempermann G. 2004. Differential regulation of gliogenesis in the context of adult hippocampal neurogenesis in mice. Glia 46: 41-52.
72. + neural stem cells in the adult hippocampus. Cell Stem Cell 1: 515-528.
73. Wang C, Liu F, Liu Y-Y, Zhao C-H, You Y, Wang L, Zhang J, Wei B, Ma T, Zhang Q, Zhang Y, Chen R, Song H, Yang Z. 2011. Identification and characterization of neuroblasts in the subventricular zone and rostral migratory stream of the adult human brain. Cell Res (in press).
74. Whitman MC, Greer CA. 2009. Adult neurogenesis and the olfactory system. Prog Neurobiol 89: 162-175.
75. Winner B, Cooper-Kuhn CM, Aigner R, Winkler J, Kuhn HG. 2002. Long-term survival and cell death of newly generated neurons in the adult rat olfactory bulb. Eur J Neurosci 16: 1681-1689.
76. Zhao C, Teng EM, Summers RG, Ming G-L, Gage FH. 2006. Distinct morphological stages of dentate granule neuron maturation in the adult mouse hippocampus. J Neurosci 26: 3-11.