Regeneration of new neurons is preserved in aged vomeronasal epithelia

Journal of Neuroscience

Volumn 30, Issue 46, 2010, Pages 15686-15694

  Brann, Jessica H ^a   Firestein, Stuart ^a  

^a Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL PROLIFERATION; MOUSE; NERVE INJURY; NERVE REGENERATION; NEURAL STEM CELL; NONHUMAN; OLFACTORY BULBECTOMY; PRIORITY JOURNAL; SENSORY NERVE CELL; VOMERONASAL ORGAN;

ANIMALS; CELL AGING; CELL PROLIFERATION; MICE; MICE, INBRED C57BL; NASAL MUCOSA; NERVE REGENERATION; NEUROGENESIS; NEURONS; OLFACTORY MUCOSA; VOMERONASAL ORGAN;

EID: 78449260733     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4316-10.2010     Document Type: Article

References (69)

1. Ahlenius H, Visan V, Kokaia M, Lindvall O, Kokaia Z (2009) Neural stem and progenitor cells retain their potential for proliferation and differentiation into functional neurons despite lower number in aged brain. J Neurosci 29:4408-4419.
2. Bailey KJ, Maslov AY, Pruitt SC (2004) Accumulation of mutations and somatic selection in aging neural stem/progenitor cells. Aging Cell 3:391-397.
3. Bauer S, Patterson PH (2005) The cell cycle-apoptosis connection revisited in the adult brain. J Cell Biol 171:641-650. (Pubitemid 41668723)
4. Caggiano M, Kauer JS, Hunter DD (1994) Globose basal cells are neuronal progenitors in the olfactory epithelium: a lineage analysis using a replication-incompetent retrovirus. Neuron 13:339-352.
5. Calof AL, Bonnin A, Crocker C, Kawauchi S, Murray RC, Shou J, Wu HH (2002) Progenitor cells of the olfactory receptor neuron lineage. Microsc Res Tech 58:176-188.
6. Cameron HA, McKay RD (2001) Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J Comp Neurol 435:406-417.
7. Carr VM, Farbman AI (1992) Ablation of the olfactory bulb up-regulates the rate of neurogenesis and induces precocious cell death in olfactory epithelium. Exp Neurol 115:55-59.
8. Carter LA, MacDonald JL, Roskams AJ (2004) Olfactory horizontal basal cells demonstrate a conserved multipotent progenitor phenotype. J Neurosci 24:5670-5683.
9. Costanzo RM, Graziadei PP (1983) A quantitative analysis of changes in the olfactory epithelium following bulbectomy in hamster. J Comp Neurol 215:370-381. (Pubitemid 13083061)
10. Dahl AR, Lewis JL (1993) Respiratory tract uptake of inhalants and metabolism of xenobiotics. Annu Rev Pharmacol Toxicol 33:383-407.
11. Darsalia V, Heldmann U, Lindvall O, Kokaia Z (2005) Stroke-induced neurogenesis in aged brain. Stroke 36:1790-1795.
12. De La Rosa-Prieto C, Saiz-Sanchez D, Ubeda-Bañon I, Argandoña-Palacios L, Garcia-Muñozguren S, Martinez-Marcos A (2009) Fate of marginal neuroblasts in the vomeronasal epithelium of adult mice. J Comp Neurol 517:723-736.
13. Ducray A, Bondier JR, Michel G, Bon K, Millot JL, Propper A, Kastner A (2002) Recovery following peripheral destruction of olfactory neurons in young and adult mice. Eur J Neurosci 15:1907-1917.
14. Farbman AI (1990) Olfactory neurogenesis: genetic or environmental controls? Trends Neurosci 13:362-365.
15. Firestein S (2001) How the olfactory system makes sense of scents. Nature 413:211-218.
16. Fung KM, Peringa J, Venkatachalam S, Lee VM, Trojanowski JQ (1997) Coordinate reduction in cell proliferation and cell death in mouse olfactory epithelium from birth to maturity. Brain Res 761:347-351.
17. Gaskell BA (1990) Nonneoplastic changes in the olfactory epithelium: experimental studies. Environ Health Perspect 85:275-289.
18. Getchell TV, Shah DS, Partin JV, Subhedar NK, Getchell ML (2002) Leukemia inhibitory factor mRNA expression is upregulated in macrophages and olfactory receptor neurons after target ablation. J Neurosci Res 67:246-254.
19. Giacobini P, Benedetto A, Tirindelli R, Fasolo A (2000) Proliferation and migration of receptor neurons in the vomeronasal organ of the adult mouse. Brain Res Dev Brain Res 123:33-40.
20. Graziadei PP, Monti Graziadei AG (1983) Regeneration in the olfactory system of vertebrates. Am J Otolaryngol 4:228-233.
21. Halpern M, Martínez-Marcos A (2003) Structure and function of the vomeronasal system: an update. Prog Neurobiol 70:245-318.
22. Hinds JW, Hinds PL, McNelly NA (1984) An autoradiographic study of the mouse olfactory epithelium: evidence for long-lived receptors. Anat Rec 210:375-383.
23. Holtzman DA (1998) Cell dynamics in the embryonic and postnatal vomeronasal epithelium of snakes. Microsc Res Tech 41:471-482.
24. Huard JM, Schwob JE (1995) Cell cycle of globose basal cells in rat olfactory epithelium. Dev Dyn 203:17-26.
25. Kastner A, Moyse E, Bauer S, Jourdan F, Brun G (2000) Unusual regulation of cyclin D1 and cyclin-dependent kinases cdk2 and cdk4 during in vivo mitotic stimulation of olfactory neuron progenitors in adult mouse. J Neurochem 74:2343-2349. (Pubitemid 30314209)
26. Konen TG, Smith GS, Walford RL (1973) Decline in mixed lymphocyte reactivity of spleen cells from aged mice of a long-lived strain. J Immunol 110:1216-1221.
27. Lander AD, Gokoffski KK, Wan FY, Nie Q, Calof AL (2009) Cell lineages and the logic of proliferative control. PLoS Biol 7:e15.
28. Legrier ME, Ducray A, Propper A, Chao M, Kastner A (2001) Cell cycle regulation during mouse olfactory neurogenesis. Cell Growth Differ 12:591-601.
29. Liu F, You Y, Li X, Ma T, Nie Y, Wei B, Li T, Lin H, Yang Z (2009) Brain injury does not alter the intrinsic differentiation potential of adult neuroblasts. J Neurosci 29:5075-5087.
30. Luo J, Daniels SB, Lennington JB, Notti RQ, Conover JC (2006) The aging neurogenic subventricular zone. Aging Cell 5:139-152.
31. Macas J, Nern C, Plate KH, Momma S (2006) Increased generation of neuronal progenitors after ischemic injury in the aged adult human forebrain. J Neurosci 26:13114-13119.
32. Mackay-Sim A, Kittel P (1991) Cell dynamics in the adult mouse olfactory epithelium: a quantitative autoradiographic study. J Neurosci 11:979-984.
33. Martínez-Marcos A, Ubeda-Bañón I, Halpern M (2000a) Cell turnover in the vomeronasal epithelium: evidence for differential migration and maturation of subclasses of vomeronasal neurons in the adult opossum. J Neurobiol 43:50-63. (Pubitemid 30191180)
34. Martínez-Marcos A, Ubeda-Bañón I, Deng L, Halpern M (2000b) Neurogenesis in the vomeronasal epithelium of adult rats: evidence for different mechanisms for growth and neuronal turnover. J Neurobiol 44:423-435.
35. Martínez-Marcos A, Jia C, Quan W, Halpern M (2005) Neurogenesis, migration, and apoptosis in the vomeronasal epithelium of adult mice. J Neurobiol 63:173-187. (Pubitemid 40656772)
36. Maslov AY, Barone TA, Plunkett RJ, Pruitt SC (2004) Neural stem cell detection, characterization, and age-related changes in the subventricular zone of mice. J Neurosci 24:1726-1733.
37. Matsuoka M, Yoshida-Matsuoka J, Iwasaki N, Norita M, Costanzo RM, Ichikawa M (2001) Immunocytochemical study of G(i)2alpha and G(o)alpha on the epithelium surface of the rat vomeronasal organ. Chem Senses 26:161-166.
38. Matsuoka M, Osada T, Yoshida-Matsuoka J, Ikai A, Ichikawa M, Norita M, Costanzo RM (2002) A comparative immunocytochemical study of development and regeneration of chemosensory neurons in the rat vomeronasal system. Brain Res 946:52-63.
39. Medrano S, Burns-Cusato M, Atienza MB, Rahimi D, Scrable H (2009) Regenerative capacity of neural precursors in the adult mammalian brain is under the control of p53. Neurobiol Aging 30:483-497.
40. Mendoza AS (1993) Morphological studies on the rodent main and accessory olfactory systems: the regio olfactoria and vomeronasal organ. Ann Anat 175:425-446.
41. Mimeault M, Batra SK (2009) Recent insights into the molecular mechanisms involved in aging and the malignant transformation of adult stem/progenitor cells and their therapeutic implications. Ageing Res Rev 8:94-112.
42. Minovi A, Witt M, Prescher A, Gudziol V, Dazert S, Hatt H, Benecke H (2010) Expression and distribution of the intermediate filament protein nestin and other stem cell related molecules in the human olfactory epithelium. Histol Histopathol 25:177-187.
43. Mombaerts P (2004) Genes and ligands for odorant, vomeronasal and taste receptors. Nat Rev Neurosci 5:263-278. (Pubitemid 38478654)
44. Morgenstern NA, Lombardi G, Schinder AF (2008) Newborn granule cells in the ageing dentate gyrus. J Physiol 586:3751-3757.
45. Morrison SJ, Spradling AC (2008) Stem cells and niches: mechanisms that promote stem cell maintenance throughout life. Cell 132:598-611.
46. Muskhelishvili L, Latendresse JR, Kodell RL, Henderson EB (2003) Evaluation of cell proliferation in rat tissues with BrdU, PCNA, Ki-67(MIB-5) immunohistochemistry and in situ hybridization for histone mRNA. J Histochem Cytochem 51:1681-1688.
47. Nakamura H, Fujiwara M, Kawasaki M, Nonomura N, Takahashi S (1998) Age-related changes in dividing cells of the olfactory epithelium of the maturing guinea pig. Eur Arch Otorhinolaryngol 255:289-292.
48. Nan B, Getchell ML, Partin JV, Getchell TV (2001) Leukemia inhibitory factor, interleukin-6, and their receptors are expressed transiently in the olfactory mucosa after target ablation. J Comp Neurol 435:60-77. (Pubitemid 32448722)
49. Ohta Y, Ichimura K (2000) Proliferation markers, proliferating cell nuclear antigen, Ki67, 5-bromo-2′-deoxyuridine, and cyclin D1 in mouse olfactory epithelium. Ann Otol Rhinol Laryngol 109:1046-1048.
50. Olariu A, Cleaver KM, Cameron HA (2007) Decreased neurogenesis in aged rats results from loss of granule cell precursors without lengthening of the cell cycle. J Comp Neurol 501:659-667.
51. Popa-Wagner A, Buga AM, Kokaia Z (2009) Perturbed cellular response to brain injury during aging. Ageing Res Rev. Advance online publication. Retrieved April 6, 2010. doi:10.1016/j.arr.2009.10.008.
52. Rao MS, Hattiangady B, Abdel-Rahman A, Stanley DP, Shetty AK (2005) Newly born cells in the ageing dentate gyrus display normal migration, survival and neuronal fate choice but endure retarded early maturation. Eur J Neurosci 21:464-476.
53. Rao MS, Hattiangady B, Shetty AK (2006) The window and mechanisms of major age-related decline in the production of new neurons within the dentate gyrus of the hippocampus. Aging Cell 5:545-558. (Pubitemid 44782623)
54. Schwartz Levey M, Chikaraishi DM, Kauer JS (1991) Characterization of potential precursor populations in the mouse olfactory epithelium using immunocytochemistry and autoradiography. J Neurosci 11:3556-3564.
55. Shetty AK, Hattiangady B, Rao MS, Shuai B (2010) Deafferentation enhances neurogenesis in the young and middle aged hippocampus but not in the aged hippocampus. Hippocampus. Advance online publication. Retrieved August 6, 2010. doi:10.1002/hipo.20776.
56. Suzuki Y, Schafer J, Farbman AI (1995) Phagocytic cells in the rat olfactory epithelium after bulbectomy. Exp Neurol 136:225-233.
57. Taupin P (2007) BrdU immunohistochemistry for studying adult neurogenesis: paradigms, pitfalls, limitations, and validation. Brain Res Rev 53:198-214.
58. Upadhyay UD, Holbrook EH (2004) Olfactory loss as a result of toxic exposure. Otolaryngol Clin North Am 37:1185-1207.
59. Valley MT, Mullen TR, Schultz LC, Sagdullaev BT, Firestein S (2009) Ablation of mouse adult neurogenesis alters olfactory bulb structure and olfactory fear conditioning. Front Neurosci 3:51.
60. Wagner W, Bork S, Horn P, Krunic D, Walenda T, Diehlmann A, Benes V, Blake J, Huber FX, Eckstein V, Boukamp P, Ho AD (2009) Aging and replicative senescence have related effects on human stem and progenitor cells. PLoS One 4:e5846.
61. Wakabayashi Y, Ichikawa M (2007) Distribution of Notch1-expressing cells and proliferating cells in mouse vomeronasal organ. Neurosci Lett 411:217-221.
62. Weiler E (2005) Postnatal development of the rat vomeronasal organ. Chem Senses 30[Suppl 1]:i127-i128.
63. Weiler E, Farbman AI (1997) Proliferation in the rat olfactory epithelium: age-dependent changes. J Neurosci 17:3610-3622. (Pubitemid 27200588)
64. Weiler E, Farbman AI (1998) Proliferation decrease in the olfactory epithelium during postnatal development. Ann N Y Acad Sci 855:230-234. (Pubitemid 29109984)
65. Weiler E, McCulloch MA, Farbman AI (1999) Proliferation in the vomeronasal organ of the rat during postnatal development. Eur J Neurosci 11:700-711.
66. Whitman MC, Greer CA (2009) Adult neurogenesis and the olfactory system. Prog Neurobiol 89:162-175.
67. Wu HH, Ivkovic S, Murray RC, Jaramillo S, Lyons KM, Johnson JE, Calof AL (2003) Autoregulation of neurogenesis by GDF11. Neuron 37:197-207.
68. Yankner BA, Lu T, Loerch P (2008) The aging brain. Annu Rev Pathol 3:41-66.
69. Yoshida-Matsuoka J, Matsuoka M, Costanzo RM, Ichikawa M (2000) Morphological and histochemical changes in the regenerating vomeronasal epithelium. J Vet Med Sci 62:1253-1261.