Age-dependent regional changes in the rostral migratory stream

Neurobiology of Aging

Volumn 34, Issue 7, 2013, Pages 1873-1881

  Mobley, Arie S ^a   Bryant, Alex K ^a   Richard, Marion B ^b,c   Brann, Jessica H ^d   Firestein, Stuart J ^d   Greer, Charles A ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITÉ LYON 1   (France)

^c UNIVERSITÉ DE LYON   (France)

^d Columbia University ^*  (United States)

Author keywords

Aging; BrdU; Migration; Periglomerular cells; Proliferation; Rostral migratory stream; Subventricular zone

Indexed keywords

AGE; AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CELL SUBPOPULATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOARCHITECTURE; GLOMERULOSA CELL; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEUROBLAST; NONHUMAN; PRIORITY JOURNAL; ROSTRAL MIGRATORY STREAM; SUBVENTRICULAR ZONE; ZONA GLOMERULOSA;

AGING; ANIMALS; CELL MOVEMENT; CELL PROLIFERATION; CEREBRAL VENTRICLES; MICE; MICE, INBRED C57BL; NEUROGENESIS; OLFACTORY BULB;

EID: 84875825967     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2013.01.015     Document Type: Article

References (71)

1. Ahlenius H., Visan V., Kokaia M., Lindvall O., Kokaia Z. Neural stem and progenitor cells retain their potential for proliferation and differentiation into functional neurons despite lower number in aged brain. J. Neurosci. 2009, 29:4408-4419.
2. Alvarez-Buylla A., Garcia-Verdugo J.M. Neurogenesis in adult subventricular zone. J. Neurosci. 2002, 22:629-634.
3. Aungst J.L., Heyward P.M., Puche A.C., Karnup S.V., Hayar A., Szabo G., Shipley M.T. Centre-surround inhibition among olfactory bulb glomeruli. Nature 2003, 426:623-629.
4. Belvindrah R., Nissant A., Lledo P.M. Abnormal neuronal migration changes the fate of developing neurons in the postnatal olfactory bulb. J. Neurosci. 2011, 31:7551-7562.
5. Bouab M., Paliouras G.N., Aumont A., Forest-Berard K., Fernandes K.J. Aging of the subventricular zone neural stem cell niche: evidence for quiescence-associated changes between early and mid-adulthood. Neuroscience 2011, 173:135-149.
6. Bozoyan L., Khlghatyan J., Saghatelyan A. Astrocytes control the development of the migration-promoting vasculature scaffold in the postnatal brain via VEGF signaling. J. Neurosci. 2012, 32:1687-1704.
7. Brann J.H., Firestein S. Regeneration of new neurons is preserved in aged vomeronasal epithelia. J. Neurosci. 2010, 30:15686-15694.
8. Carleton A., Petreanu L.T., Lansford R., Alvarez-Buylla A., Lledo P.M. Becoming a new neuron in the adult olfactory bulb. Nat. Neurosci. 2003, 6:507-518.
9. De Marchis S., Bovetti S., Carletti B., Hsieh Y.C., Garzotto D., Peretto P., Fasolo A., Puche A.C., Rossi F. Generation of distinct types of periglomerular olfactory bulb interneurons during development and in adult mice: implication for intrinsic properties of the subventricular zone progenitor population. J. Neurosci. 2007, 27:657-664.
10. De Marchis S., Fasolo A., Puche A.C. Subventricular zone-derived neuronal progenitors migrate into the subcortical forebrain of postnatal mice. J. Comp. Neurol. 2004, 476:290-300.
11. Doetsch F., Garcia-Verdugo J.M., Alvarez-Buylla A. Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J. Neurosci. 1997, 17:5046-5061.
12. Doty R.L., Petersen I., Mensah N., Christensen K. Genetic and environmental influences on odor identification ability in the very old. Psychol. Aging 2011, 26:864-871.
13. Duque A., Rakic P. Different effects of bromodeoxyuridine and [3H]thymidine incorporation into DNA on cell proliferation, position, and fate. J. Neurosci. 2011, 31:15205-15217.
14. Enwere E., Shingo T., Gregg C., Fujikawa H., Ohta S., Weiss S. Aging results in reduced epidermal growth factor receptor signaling, diminished olfactory neurogenesis, and deficits in fine olfactory discrimination. J. Neurosci. 2004, 24:8354-8365.
15. Francis F., Koulakoff A., Boucher D., Chafey P., Schaar B., Vinet M.C., Friocourt G., McDonnell N., Reiner O., Kahn A., McConnell S.K., Berwald-Netter Y., Denoulet P., Chelly J. Doublecortin is a developmentally regulated, microtubule-associated protein expressed in migrating and differentiating neurons. Neuron 1999, 23:247-256.
16. García-Marqués J., De Carlos J.A., Greer C.A., Lopez-Mascaraque L. Different astroglia permissivity controls the migration of olfactory bulb interneuron precursors. Glia 2010, 58:218-230.
17. García-Verdugo J.M., Ferron S., Flames N., Collado L., Desfilis E., Font E. The proliferative ventricular zone in adult vertebrates: a comparative study using reptiles, birds, and mammals. Brain Res. Bull. 2002, 57:765-775.
18. Giachino C., Taylor V. Lineage analysis of quiescent regenerative stem cells in the adult brain by genetic labelling reveals spatially restricted neurogenic niches in the olfactory bulb. Eur. J. Neurosci. 2009, 30:9-24.
19. Gire D.H., Schoppa N.E. Control of on/off glomerular signaling by a local GABAergic microcircuit in the olfactory bulb. J. Neurosci. 2009, 29:13454-13464.
20. Gleeson J.G., Lin P.T., Flanagan L.A., Walsh C.A. Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons. Neuron 1999, 23:257-271.
21. Gritti A., Bonfanti L., Doetsch F., Caille I., Alvarez-Buylla A., Lim D.A., Galli R., Verdugo J.M., Herrera D.G., Vescovi A.L. Multipotent neural stem cells reside into the rostral extension and olfactory bulb of adult rodents. J. Neurosci. 2002, 22:437-445.
22. Hurtado-Chong A., Yusta-Boyo M.J., Vergano-Vera E., Bulfone A., de Pablo F., Vicario-Abejon C. IGF-I promotes neuronal migration and positioning in the olfactory bulb and the exit of neuroblasts from the subventricular zone. Eur. J. Neurosci. 2009, 30:742-755.
23. Imamura F., Nagao H., Naritsuka H., Murata Y., Taniguchi H., Mori K. A leucine-rich repeat membrane protein, 5T4, is expressed by a subtype of granule cells with dendritic arbors in specific strata of the mouse olfactory bulb. J. Comp. Neurol. 2006, 495:754-768.
24. Jin K., Sun Y., Xie L., Batteur S., Mao X.O., Smelick C., Logvinova A., Greenberg D.A. Neurogenesis and aging: FGF-2 and HB-EGF restore neurogenesis in hippocampus and subventricular zone of aged mice. Aging Cell 2003, 2:175-183.
25. Kasowski H.J., Kim H., Greer C.A. Compartmental organization of the olfactory bulb glomerulus. J. Comp. Neurol. 1999, 407:261-274.
26. Kelsch W., Sim S., Lois C. Watching synaptogenesis in the adult brain. Annu. Rev. Neurosci. 2010, 33:131-149.
27. Kiyokage E., Pan Y.Z., Shao Z., Kobayashi K., Szabo G., Yanagawa Y., Obata K., Okano H., Toida K., Puche A.C., Shipley M.T. Molecular identity of periglomerular and short axon cells. J. Neurosci. 2010, 30:1185-1196.
28. Kosaka K., Aika Y., Toida K., Heizmann C.W., Hunziker W., Jacobowitz D.M., Nagatsu I., Streit P., Visser T.J., Kosaka T. Chemically defined neuron groups and their subpopulations in the glomerular layer of the rat main olfactory bulb. Neurosci. Res. 1995, 23:73-88.
29. Kosaka K., Toida K., Aika Y., Kosaka T. How simple is the organization of the olfactory glomerulus?: the heterogeneity of so-called periglomerular cells. Neurosci. Res. 1998, 30:101-110.
30. Lazarini F., Lledo P.M. Is adult neurogenesis essential for olfaction?. Trends Neurosci. 2011, 34:20-30.
31. Lemasson M., Saghatelyan A., Olivo-Marin J.C., Lledo P.M. Neonatal and adult neurogenesis provide two distinct populations of newborn neurons to the mouse olfactory bulb. J. Neurosci. 2005, 25:6816-6825.
32. Lledo P.M., Merkle F.T., Alvarez-Buylla A. Origin and function of olfactory bulb interneuron diversity. Trends Neurosci. 2008, 31:392-400.
33. Lledo P.M., Saghatelyan A. Integrating new neurons into the adult olfactory bulb: joining the network, life-death decisions, and the effects of sensory experience. Trends Neurosci. 2005, 28:248-254.
34. Lois C., Alvarez-Buylla A. Long-distance neuronal migration in the adult mammalian brain. Science 1994, 264:1145-1148.
35. Lois C., Garcia-Verdugo J.M., Alvarez-Buylla A. Chain migration of neuronal precursors. Science 1996, 271:978-981.
36. Loo A.T., Youngentob S.L., Kent P.F., Schwob J.E. The aging olfactory epithelium: neurogenesis, response to damage, and odorant-induced activity. Int. J. Dev. Neurosci. 1996, 14:881-900.
37. Lugert S., Basak O., Knuckles P., Haussler U., Fabel K., Gotz M., Haas C.A., Kempermann G., Taylor V., Giachino C. Quiescent and active hippocampal neural stem cells with distinct morphologies respond selectively to physiological and pathological stimuli and aging. Cell Stem Cell 2010, 6:445-456.
38. Luskin M.B. Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron 1993, 11:173-189.
39. Luskin M.B., Boone M.S. Rate and pattern of migration of lineally-related olfactory bulb interneurons generated postnatally in the subventricular zone of the rat. Chem. Senses 1994, 19:695-714.
40. Mandairon N., Jourdan F., Didier A. Deprivation of sensory inputs to the olfactory bulb up-regulates cell death and proliferation in the subventricular zone of adult mice. Neuroscience 2003, 119:507-516.
41. Mandairon N., Peace S.T., Boudadi K., Boxhorn C.E., Narla V.A., Suffis S.D., Cleland T.A. Compensatory responses to age-related decline in odor quality acuity: cholinergic neuromodulation and olfactory enrichment. Neurobiol. Aging 2011, 32:2254-2265.
42. Mandairon N., Sultan S., Nouvian M., Sacquet J., Didier A. Involvement of newborn neurons in olfactory associative learning? The operant or non-operant component of the task makes all the difference. J. Neurosci. 2011, 31:12455-12460.
43. Maslov A.Y., Barone T.A., Plunkett R.J., Pruitt S.C. Neural stem cell detection, characterization, and age-related changes in the subventricular zone of mice. J. Neurosci. 2004, 24:1726-1733.
44. Menezes J.R., Smith C.M., Nelson K.C., Luskin M.B. The division of neuronal progenitor cells during migration in the neonatal mammalian forebrain. Mol. Cell. Neurosci. 1995, 6:496-508.
45. Merkle F.T., Mirzadeh Z., Alvarez-Buylla A. Mosaic organization of neural stem cells in the adult brain. Science 2007, 317:381-384.
46. Moreno M.M., Bath K., Kuczewski N., Sacquet J., Didier A., Mandairon N. Action of the noradrenergic system on adult-born cells is required for olfactory learning in mice. J. Neurosci. 2012, 32:3748-3758.
47. Moreno M.M., Linster C., Escanilla O., Sacquet J., Didier A., Mandairon N. Olfactory perceptual learning requires adult neurogenesis. Proc. Natl. Acad. Sci. U. S. A 2009, 106:17980-17985.
48. Morshead C.M., van der Kooy D. Postmitotic death is the fate of constitutively proliferating cells in the subependymal layer of the adult mouse brain. J. Neurosci. 1992, 12:249-256.
49. Mouret A., Gheusi G., Gabellec M.M., de Chaumont F., Olivo-Marin J.C., Lledo P.M. Learning and survival of newly generated neurons: when time matters. J. Neurosci. 2008, 28:11511-11516.
50. Nie K., Molnar Z., Szele F.G. Proliferation but not migration is associated with blood vessels during development of the rostral migratory stream. Dev. Neurosci. 2010, 32:163-172.
51. Nunez-Parra A., Pugh V., Araneda R.C. Regulation of adult neurogenesis by behavior and age in the accessory olfactory bulb. Mol. Cell. Neurosci. 2011, 47:274-285.
52. Patel R.C., Larson J. Impaired olfactory discrimination learning and decreased olfactory sensitivity in aged C57Bl/6 mice. Neurobiol. Aging 2009, 30:829-837.
53. Poon A., Li Z., Wolfe G.W., Lu L., Williams R.W., Hayes N.L., Nowakowski R.S., Goldowitz D. Identification of a Chr 11 quantitative trait locus that modulates proliferation in the rostral migratory stream of the adult mouse brain. Eur. J. Neurosci. 2010, 32:523-537.
54. Rey N.L., Sacquet J., Veyrac A., Jourdan F., Didier A. Behavioral and cellular markers of olfactory aging and their response to enrichment. Neurobiol. Aging 2012, 33:626.e9-626.e23.
55. Richard M.B., Taylor S.R., Greer C.A. Age-induced disruption of selective olfactory bulb synaptic circuits. Proc. Natl. Acad. Sci. U. S. A 2010, 107:15613-15618.
56. Sakamoto M., Imayoshi I., Ohtsuka T., Yamaguchi M., Mori K., Kageyama R. Continuous neurogenesis in the adult forebrain is required for innate olfactory responses. Proc. Natl. Acad. Sci. U. S. A 2011, 108:8479-8484.
57. Schoppa N.E., Urban N.N. Dendritic processing within olfactory bulb circuits. Trends Neurosci. 2003, 26:501-506.
58. Shook B.A., Manz D.H., Peters J.J., Kang S., Conover J.C. Spatiotemporal changes to the subventricular zone stem cell pool through aging. J. Neurosci. 2012, 32:6947-6956.
59. Smith C.M., Luskin M.B. Cell cycle length of olfactory bulb neuronal progenitors in the rostral migratory stream. Dev. Dyn. 1998, 213:220-227.
60. Stenman J., Toresson H., Campbell K. Identification of two distinct progenitor populations in the lateral ganglionic eminence: implications for striatal and olfactory bulb neurogenesis. J. Neurosci. 2003, 23:167-174.
61. Sui Y., Horne M.K., Stanic D. Reduced proliferation in the adult mouse subventricular zone increases survival of olfactory bulb interneurons. PLoS One 2012, 7:e31549.
62. Sultan S., Rey N., Sacquet J., Mandairon N., Didier A. Newborn neurons in the olfactory bulb selected for long-term survival through olfactory learning are prematurely suppressed when the olfactory memory is erased. J. Neurosci. 2011, 31:14893-14898.
63. Tavazoie M., Van der Veken L., Silva-Vargas V., Louissaint M., Colonna L., Zaidi B., Garcia-Verdugo J.M., Doetsch F. A specialized vascular niche for adult neural stem cells. Cell. Stem Cell 2008, 3:279-288.
64. Tropepe V., Craig C.G., Morshead C.M., van der Kooy D. Transforming growth factor-alpha null and senescent mice show decreased neural progenitor cell proliferation in the forebrain subependyma. J. Neurosci. 1997, 17:7850-7859.
65. Valley M.T., Mullen T.R., Schultz L.C., Sagdullaev B.T., Firestein S. Ablation of mouse adult neurogenesis alters olfactory bulb structure and olfactory fear conditioning. Front. Neurosci. 2009, 3:51.
66. Whitman M.C., Fan W., Rela L., Rodriguez-Gil D.J., Greer C.A. Blood vessels form a migratory scaffold in the rostral migratory stream. J. Comp. Neurol. 2009, 516:94-104.
67. Whitman M.C., Greer C.A. Adult-generated neurons exhibit diverse developmental fates. Dev. Neurobiol. 2007, 67:1079-1093.
68. Whitman M.C., Greer C.A. Synaptic integration of adult-generated olfactory bulb granule cells: basal axodendritic centrifugal input precedes apical dendrodendritic local circuits. J. Neurosci. 2007, 27:9951-9961.
69. Whitman M.C., Greer C.A. Adult neurogenesis and the olfactory system. Prog. Neurobiol. 2009, 89:162-175.
70. Winner B., Cooper-Kuhn C.M., Aigner R., Winkler J., Kuhn H.G. Long-term survival and cell death of newly generated neurons in the adult rat olfactory bulb. Eur. J. Neurosci. 2002, 16:1681-1689.
71. Yang Z. Postnatal subventricular zone progenitors give rise not only to granular and periglomerular interneurons but also to interneurons in the external plexiform layer of the rat olfactory bulb. J. Comp. Neurol. 2008, 506:347-358.