Fate of marginal neuroblasts in the vomeronasal epithelium of adult mice

Journal of Comparative Neurology

Volumn 517, Issue 5, 2009, Pages 723-736

  De La Rosa Prieto, C ^a   Saiz Sanchez, D ^a   Ubeda Banon I ^a   Argandona Palacios L ^b   Garcia Munozguren S ^b   Martinez Marcos, Alino ^a  

^a UNIVERSITY OF CASTILLA LA MANCHA   (Spain)

^b HOSPITAL GENERAL UNIVERSITARIO DE ALBACETE   (Spain)

Author keywords

Apoptosis; Bromodeoxyuridine; Caspase 3; Chemical senses; Neurogenesis; Pheromone

Indexed keywords

BROXURIDINE; CASPASE 3; OLFACTORY MARKER PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL FATE; CELL MATURATION; CELLULAR DISTRIBUTION; EPITHELIUM; EXPERIMENTAL MOUSE; FEMALE; GENE LOCATION; GENETIC MARKER; MALE; NERVOUS SYSTEM DEVELOPMENT; NEUROBLASTOMA; NISSL STAINING; NONHUMAN; PRIORITY JOURNAL; VOMERONASAL ORGAN;

ADULT STEM CELLS; ANIMALS; APOPTOSIS; CELL DIFFERENTIATION; CELL MOVEMENT; EPITHELIAL CELLS; FEMALE; MALE; MICE; NEUROGENESIS; STEM CELL NICHE; VOMERONASAL ORGAN;

EID: 70449459182     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.22188     Document Type: Article

References (68)

1. Abercrombie M. 1946. Estimation of nuclear population from microtome sections. Anat Rec 94:239-247.
2. Bagley J, LaRocca G, Jimenez DA, Urban NN. 2007. Adult neurogenesis and specific replacement of interneuron subtypes in the mouse main olfactory bulb. BMC Neurosci 8:92. (Pubitemid 351234740)
3. Barber PC, Raisman G. 1978a. Cell division in the vomeronasal organ of the adult mouse. Brain Res 141:57-66. (Pubitemid 8259781)
4. Barber PC, Raisman G. 1978b. Replacement of receptor neurones after section of the vomeronasal nerves in the adult mouse. Brain Res 147:297-313. (Pubitemid 8334140)
5. Beites CL, Kawauchi S, Crocker CE, Calof AL. 2005. Identification and molecular regulation of neural stem cells in the olfactory epithelium. Exp Cell Res 306:309-316. (Pubitemid 40732754)
6. Belluscio L, Koentges G, Axel R, Dulac C. 1999. A map of pheromone receptor activation in the mammalian brain. Cell 97:209-220. (Pubitemid 29194272)
7. Berghard A, Buck LB. 1996. Sensory transduction in vomeronasal neurons: evidence for G alpha o, G alpha i2, and adenylyl cyclase II as major components of a pheromone signaling cascade. J Neurosci 16:909-918. (Pubitemid 26140846)
8. Buck L, Axel R. 1991. A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65:175-187. (Pubitemid 121001224)
9. Buck LB. 1996. Information coding in the vertebrate olfactory system. Ann Rev Neurosci 19:517-544. (Pubitemid 26080838)
10. Calof AL, Hagiwara N, Holcomb JD, Mumm JS, Shou J. 1996. Neurogenesis and cell death in olfactory epithelium. J Neurobiol 30:67-81. (Pubitemid 26118734)
11. Calof AL, Mumm JS, Rim PC, Shou J. 1998a. The neuronal stem cell of the olfactory epithelium. J Neurobiol 36:190-205. (Pubitemid 28363231)
12. Calof AL, Rim PC, Askins KJ, Mumm JS, Gordon MK, Iannuzzelli P, Shou J. 1998b. Factors regulating neurogenesis and programmed cell death in mouse olfactory epithelium. Ann N Y Acad Sci 855:226-229. (Pubitemid 29109983)
13. Cappello P, Tarozzo G, Benedetto A, Fasolo A. 1999. Proliferation and apoptosis in the mouse vomeronasal organ during ontogeny. Neurosci Lett 266:37-40. (Pubitemid 29219750)
14. Cobos I, Borello U, Rubenstein JL. 2007. Dlx transcription factors promote migration through repression of axon and dendrite growth. Neuron 54:873-888. (Pubitemid 46907500)
15. Crews L, Hunter D. 1994. Neurogenesis in the olfactory epithelium. Perspect Dev Neurobiol 2:151-161.
16. Del Punta K, Puche A, Adams NC, Rodriguez I, Mombaerts P. 2002. A divergent pattern of sensory axonal projections is rendered convergent by second-order neurons in the accessory olfactory bulb. Neuron 35:1057-1066. (Pubitemid 35279534)
17. Dulac C, Axel R. 1995. A novel family of genes encoding putative pheromone receptors in mammals. Cell 83:195-206.
18. Dulac C, Wagner S. 2006. Genetic analysis of brain circuits underlying pheromone signaling. Annu Rev Genet 40:449-467. (Pubitemid 44970425)
19. Farbman AI. 1990. Olfactory neurogenesis: genetic or environmental controls? Trends Neurosci 13:362-365.
20. Geuna S. 2000. Appreciating the difference between design-based and model-based sampling strategies in quantitative morphology of the nervous system. J Comp Neurol 427:333-339. (Pubitemid 30803467)
21. 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. (Pubitemid 30742569)
22. Gratzner HG. 1982. Monoclonal antibody to 5-bromo-and 5-iododeoxyuridine: a new reagent for detection of DNA replication. Science 218:474-475.
23. Graziadei PP, Monti-Graziadei GA. 1979. Neurogenesis and neuron regeneration in the olfactory system of mammals. I. Morphological aspects of differentiation and structural organization of the olfactory sensory neurons. J Neurocytol 8:1-18. (Pubitemid 9116185)
24. Guillery RW. 2002. On counting and counting errors. J Comp Neurol 447:1-7.
25. Halpern M, Martinez-Marcos A. 2003. Structure and function of the vomeronasal system: an update. Prog Neurobiol 70:245-318. (Pubitemid 37287601)
26. Halpern M, Shapiro LS, Jia C. 1995. Differential localization of G proteins in the opossum vomeronasal system. Brain Res 677:157-161.
27. He J, Ma L, Kim S, Nakai J, Yu CR. 2008. Encoding gender and individual information in the mouse vomeronasal organ. Science 320:535-538. (Pubitemid 351590667)
28. Herrada G, Dulac C. 1997. A novel family of putative pheromone receptors in mammals with a topographically organized and sexually dimorphic distribution. Cell 90:763-773. (Pubitemid 27357967)
29. Holekamp TF, Turaga D, Holy TE. 2008. Fast three-dimensional fluorescence imaging of activity in neural populations by objective-coupled planar illumination microscopy. Neuron 57:661-672. (Pubitemid 351337670)
30. Hu BR, Liu CL, Ouyang Y, Blomgren K, Siesjo BK. 2000. Involvement of caspase-3 in cell death after hypoxia-ischemia declines during brain maturation. J Cereb Blood Flow Metab 20:1294-1300. (Pubitemid 30676728)
31. Ichikawa M. 1999. Axonal growth of newly formed vomeronasal receptor neurons after nerve transection. Anat Embryol 200:413-417. (Pubitemid 29425706)
32. Ichikawa M, Osada T, Costanzo RM. 1998. Replacement of receptor cells in the hamster vomeronasal epithelium after nerve transection. Chem Senses 23:171-179. (Pubitemid 28159961)
33. Inamura K, Sakamoto H, Honda N, Kashiwayanagi M. 2000. Cluster of proliferating cells in rat vomeronasal sensory epithelium. Neuroreport 11:477-479. (Pubitemid 30120460)
34. Ishii T, Mombaerts P. 2008. Expression of nonclassical class I major histocompatibility genes defines a tripartite organization of the mouse vomeronasal system. J Neurosci 28:2332-2341. (Pubitemid 351348179)
35. Jia C, Halpern M. 1996. Subclasses of vomeronasal receptor neurons: differential expression of G proteins (Gi alpha 2 and G(o alpha)) and segregated projections to the accessory olfactory bulb. Brain Res 719:117-128. (Pubitemid 126334262)
36. Jia C, Halpern M. 1998. Neurogenesis and migration of receptor neurons in the vomeronasal sensory epithelium in the opossum, Monodelphis domestica. J Comp Neurol 400:287-297. (Pubitemid 28440749)
37. Kimoto H, Haga S, Sato K, Touhara K. 2005. Sex-specific peptides from exocrine glands stimulate mouse vomeronasal sensory neurons. Nature 437:898-901. (Pubitemid 41486766)
38. Koo JH, Gill S, Pannell LK, Menco BP, Margolis JW, Margolis FL. 2004. The interaction of Bex and OMP reveals a dimer of OMP with a short half-life. J Neurochem 90:102-116. (Pubitemid 38879166)
39. Leinders-Zufall T, Lane AP, Puche AC, Ma W, Novotny MV, Shipley MT, Zufall F. 2000. Ultrasensitive pheromone detection by mammalian vomeronasal neurons. Nature 405:792-796. (Pubitemid 30407851)
40. Margolis FL. 1980. A marker protein for the olfactory chemoreceptor neuron. In: Bradshaw RA, Schneider DM, editors. Proteins in the nervous system. New York: Raven. p 59-84.
41. Martinez-Marcos A. 2009. On the organization of olfactory and vomeronasal cortices. Prog Neurobiol 87:21-30.
42. Martinez-Marcos A, Halpern M. 1999a. Differential centrifugal afferents to the anterior and posterior accessory olfactory bulb. Neuroreport 10:2011-2015. (Pubitemid 29394039)
43. Martinez-Marcos A, Halpern M. 1999b. Differential projections from the anterior and posterior divisions of the accessory olfactory bulb to the medial amygdala in the opossum, Monodelphis domestica. Eur J Neurosci 11:3789-3799. (Pubitemid 29537559)
44. Martinez-Marcos A, Ubeda-Banon I, Deng L, Halpern M. 2000a. Neurogenesis in the vomeronasal epithelium of adult rats: evidence for different mechanisms for growth and neuronal turnover. J Neurobiol 44:423-435. (Pubitemid 30679407)
45. Martinez-Marcos A, Ubeda-Banon I, Halpern M. 2000b. 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)
46. Martinez-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)
47. Matsunami H, Buck LB. 1997. A multigene family encoding a diverse array of putative pheromone receptors in mammals. Cell 90:775-784. (Pubitemid 27357968)
48. 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. (Pubitemid 34804704)
49. Mohedano-Moriano A, Pro-Sistiaga P, Ubeda-Banon I, Crespo C, Insausti R, Martinez-Marcos A. 2007. Segregated pathways to the vomeronasal amygdala: differential projections from the anterior and posterior divisions of the accessory olfactory bulb. Eur J Neurosci 25:2065-2080. (Pubitemid 46581744)
50. Mohedano-Moriano A, Pro-Sistiaga P, Ubeda-Banon I, de la Rosa-Prieto C, Saiz-Sanchez D, Martinez-Marcos A. 2008. V1R and V2R segregated vomeronasal pathways to the hypothalamus. Neuroreport 19:1623-1626.
51. Mombaerts P. 1999. Molecular biology of odorant receptors in vertebrates. Annu Rev Neurosci 22:487-509. (Pubitemid 29144895)
52. Monti-Graziadei GA, Margolis FL, Harding JW, Graziadei PP. 1977. Immunocytochemistry of the olfactory marker protein. J Histochem Cytochem 25:1311-1316.
53. Moulton DG, Celebi G, Fink RP. 1970. Olfaction in mammals-two aspects: proliferation of cells in the olfactory epithelium and sensitivity to odours. In: Wolstenholme GEW, Knight J, editors. Ciba Foundation Symposium on Taste and Smell in Vertebrates. London: Churchill. p 227-250.
54. Munger SD, Leinders-Zufall T, Zufall F. 2008. Subsystem organization of the mammalian sense of smell. Annu Rev Physiol 71:115-140.
55. Olney JW, Tenkova T, Dikranian K, Muglia LJ, Jermakowicz WJ, D'Sa C, Roth KA. 2002. Ethanol-induced caspase-3 activation in the in vivo developing mouse brain. Neurobiol Dis 9:205-219. (Pubitemid 34261215)
56. Osada T, Ichikawa M, Costanzo RM. 1995. Is nestin a marker for chemosensory precursor cells? Brain Res 683:254-257.
57. Phuphanich S, Levin VA. 1985. Bioavailability of bromodeoxyuridine in dogs and toxicity in rats. Cancer Res 45:2387-2389. (Pubitemid 15024357)
58. Rodriguez I, Feinstein P, Mombaerts P. 1999. Variable patterns of axonal projections of sensory neurons in the mouse vomeronasal system. Cell 97:199-208. (Pubitemid 29194271)
59. Ryba NJ, Tirindelli R. 1997. A new multigene family of putative pheromone receptors. Neuron 19:371-379. (Pubitemid 27374235)
60. Schwob JE. 2002. Neural regeneration and the peripheral olfactory system. Anat Rec 269:33-49.
61. Suzuki Y. 2004. Fine structural aspects of apoptosis in the olfactory epithelium. J Neurocytol 33:693-702. (Pubitemid 41434141)
62. Suzuki Y, Takeda M, Obara N, Suzuki N. 1998. Colchicine-induced cell death and proliferation in the olfactory epithelium and vomeronasal organ of the mouse. Anat Embryol 198:43-51. (Pubitemid 28333915)
63. Takami S. 2002. Recent progress in the neurobiology of the vomeronasal organ. Microsc Res Techn 58:228-250. (Pubitemid 34832828)
64. Tanaka M, Treloar H, Kalb RG, Greer CA, Strittmatter SM. 1999. G(o) protein-dependent survival of primary accessory olfactory neurons. Proc Natl Acad Sci U S A 96:14106-14111.
65. Weiler E. 2005. Postnatal development of the rat vomeronasal organ. Chem Senses 30(Suppl 1):i127-128. (Pubitemid 43298184)
66. Weiler E, Apfelbach R, Farbman AI. 1999a. The vomeronasal organ of the male ferret. Chem Senses 24:127-136.
67. Weiler E, McCulloch MA, Farbman AI. 1999b. Proliferation in the vomeronasal organ of the rat during postnatal development. Eur J Neurosci 11:700-711. (Pubitemid 29050472)
68. Wilson KC, Raisman G. 1980. Age-related changes in the neurosensory epithelium of the mouse vomeronasal organ: extended period of postnatal growth in size and evidence for rapid cell turnover in the adult. Brain Res 185:103-113. (Pubitemid 10128661)