Canonical Wnt signaling promotes the proliferation and neurogenesis of peripheral olfactory stem cells during postnatal development and adult regeneration

Journal of Cell Science

Volumn 124, Issue 9, 2011, Pages 1553-1563

  Wang, Ya Zhou ^a,b,e   Yamagami, Takashi ^a,b   Gan, Qini ^a,b   Wang, Yongping ^a,b   Zhao, Tianyu ^a,b   Hamad, Salaheddin ^c   Lott, Paul ^c   Schnittke, Nikolai ^d   Schwob, James E ^d   Zhou, Chengji J ^a,b,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SHRINERS HOSPITALS FOR CHILDREN NORTHERN CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e FOURTH MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

Neurogenesis; Olfactory epithelial stem cells; Regeneration; Sox2; Wnt

Indexed keywords

TRANSCRIPTION FACTOR SOX2; WNT PROTEIN; WNT3A PROTEIN; WNT7B PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BASAL CELL; CANONICAL ANALYSIS; CELL DIFFERENTIATION; CELL MATURATION; CELL PROLIFERATION; CELL REGENERATION; CONTROLLED STUDY; EPITHELIUM CELL; FLUORESCENCE ACTIVATED CELL SORTING; IN VIVO STUDY; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; OLFACTORY EPITHELIUM; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STEM CELL;

ANIMALS; APOPTOSIS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; FLOW CYTOMETRY; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MICE; MICE, TRANSGENIC; NEUROGENESIS; NEURONS; OLFACTORY MUCOSA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SOXB1 TRANSCRIPTION FACTORS; STEM CELLS; WNT PROTEINS;

ANIMALIA; MAMMALIA; MUS MUSCULUS;

EID: 79955542317     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.080580     Document Type: Article

References (73)

1. Agathocleous, M., Iordanova, I., Willardsen, M. I., Xue, X. Y., Vetter, M. L., Harris, W. A. and Moore, K. B. (2009). A directional Wnt/beta-catenin-Sox2-proneural pathway regulates the transition from proliferation to differentiation in the Xenopus retina. Development 136, 3289-3299.
2. Bandyopadhyay, U., Biswas, K. and Banerjee, R. K. (2002). Extrathyroidal actions of antithyroid thionamides. Toxicol. Lett. 128, 117-127.
3. Barraud, P., He, X., Zhao, C., Ibanez, C., Raha-Chowdhury, R., Caldwell, M. A. and Franklin, R. J. (2007). Contrasting effects of basic fibroblast growth factor and epidermal growth factor on mouse neonatal olfactory mucosa cells. Eur. J. Neurosci. 26, 3345-3357.
4. Bergman, U., Ostergren, A., Gustafson, A. L. and Brittebo, B. (2002). Differential effects of olfactory toxicants on olfactory regeneration. Arch. Toxicol. 76, 104-112.
5. Bergstrom, U., Giovanetti, A., Piras, E. and Brittebo, E. B. (2003). Methimazoleinduced damage in the olfactory mucosa: effects on ultrastructure and glutathione levels. Toxicol. Pathol. 31, 379-387.
6. Booker-Dwyer, T., Hirsh, S. and Zhao, H. (2008). A unique cell population in the mouse olfactory bulb displays nuclear beta-catenin signaling during development and olfactory sensory neuron regeneration. Dev. Neurobiol. 68, 859-869.
7. Brittebo, E. B. (1995). Metabolism-dependent toxicity of methimazole in the olfactory nasal mucosa. Pharmacol. Toxicol. 76, 76-79.
8. Calof, A. L., Bonnin, A., Crocker, C., Kawauchi, S., Murray, R. C., Shou, J. and Wu, H. H. (2002). Progenitor cells of the olfactory receptor neuron lineage. Microsc. Res. Tech. 58, 176-188.
9. Carter, L. A., MacDonald, J. L. and Roskams, A. J. (2004). Olfactory horizontal basal cells demonstrate a conserved multipotent progenitor phenotype. J. Neurosci. 24, 5670-5683.
10. Cau, E., Casarosa, S. and Guillemot, F. (2002). Mash1 and Ngn1 control distinct steps of determination and differentiation in the olfactory sensory neuron lineage. Development 129, 1871-1880.
11. Cavallaro, M., Mariani, J., Lancini, C., Latorre, E., Caccia, R., Gullo, F., Valotta, M., DeBiasi, S., Spinardi, L., Ronchi, A. et al. (2008). Impaired generation of mature neurons by neural stem cells from hypomorphic Sox2 mutants. Development 135, 541-557.
12. Cheng, L. E. and Reed, R. R. (2007). Zfp423/OAZ participates in a developmental switch during olfactory neurogenesis. Neuron 54, 547-557.
13. Chien, A. J., Conrad, W. H. and Moon, R. T. (2009). A Wnt survival guide: from flies to human disease. J. Invest. Dermatol. 129, 1614-1627.
14. Ciani, L. and Salinas, P. C. (2005). WNTs in the vertebrate nervous system: from patterning to neuronal connectivity. Nat. Rev. Neurosci. 6, 351-362.
15. Clevers, H. (2006). Wnt/beta-catenin signaling in development and disease. Cell 127, 469-480.
16. Deleyrolle, L. P. and Reynolds, B. A. (2009). Isolation, expansion, and differentiation of adult Mammalian neural stem and progenitor cells using the neurosphere assay. Methods Mol. Biol. 549, 91-101.
17. Donner, A. L., Episkopou, V. and Maas, R. L. (2007). Sox2 and Pou2f1 interact to control lens and olfactory placode development. Dev. Biol. 303, 784-799.
18. Fuchs, E. (2009). Finding one's niche in the skin. Cell Stem Cell 4, 499-502.
19. Gelebart, P., Anand, M., Armanious, H., Peters, A. C., Dien Bard, J., Amin, H. M. and Lai, R. (2008). Constitutive activation of the Wnt canonical pathway in mantle cell lymphoma. Blood 112, 5171-5179.
20. Genter, M. B., Deamer, N. J., Blake, B. L., Wesley, D. S. and Levi, P. E. (1995). Olfactory toxicity of methimazole: dose-response and structure-activity studies and characterization of flavin-containing monooxygenase activity in the Long-Evans rat olfactory mucosa. Toxicol. Pathol. 23, 477-486.
21. Goessling, W., North, T. E., Loewer, S., Lord, A. M., Lee, S., Stoick-Cooper, C. L., Weidinger, G., Puder, M., Daley, G. Q., Moon, R. T. et al. (2009). Genetic interaction of PGE2 and Wnt signaling regulates developmental specification of stem cells and regeneration. Cell 136, 1136-1147.
22. Greene, N. D., Bamidele, A., Choy, M., de Castro, S. C., Wait, R., Leung, K. Y., Begum, S., Gadian, D. G., Scott, R. C. and Lythgoe, M. F. (2007). Proteome changes associated with hippocampal MRI abnormalities in the lithium pilocarpine-induced model of convulsive status epilepticus. Proteomics 7, 1336-1344.
23. Grigoryan, T., Wend, P., Klaus, A. and Birchmeier, W. (2008). Deciphering the function of canonical Wnt signals in development and disease: conditional loss- and gain-of-function mutations of beta-catenin in mice. Genes Dev. 22, 2308-2341.
24. Hirabayashi, Y., Itoh, Y., Tabata, H., Nakajima, K., Akiyama, T., Masuyama, N. and Gotoh, Y. (2004). The Wnt/beta-catenin pathway directs neuronal differentiation of cortical neural precursor cells. Development 131, 2791-2801.
25. Huang, S. M., Mishina, Y. M., Liu, S., Cheung, A., Stegmeier, F., Michaud, G. A., Charlat, O., Wiellette, E., Zhang, Y., Wiessner, S. et al. (2009). Tankyrase inhibition stabilizes axin and antagonizes Wnt signalling. Nature 461, 614-620.
26. Ille, F. and Sommer, L. (2005). Wnt signaling: multiple functions in neural development. Cell. Mol. Life Sci. 62, 1100-1108.
27. Iwai, N., Zhou, Z., Roop, D. R. and Behringer, R. R. (2008). Horizontal basal cells are multipotent progenitors in normal and injured adult olfactory epithelium. Stem Cells 26, 1298-1306.
28. Jagtap, S., Meganathan, K., Wagh, V., Winkler, J., Hescheler, J. and Sachinidis, A. (2009). Chemoprotective mechanism of the natural compounds, epigallocatechin-3-Ogallate, quercetin and curcumin against cancer and cardiovascular diseases. Curr. Med. Chem. 16, 1451-1462.
29. Jang, W., Youngentob, S. L. and Schwob, J. E. (2003). Globose basal cells are required for reconstitution of olfactory epithelium after methyl bromide lesion. J. Comp. Neurol. 460, 123-140.
30. Jho, E. H., Zhang, T., Domon, C., Joo, C. K., Freund, J. N. and Costantini, F. (2002). Wnt/beta-catenin/Tcf signaling induces the transcription of Axin2, a negative regulator of the signaling pathway. Mol. Cell. Biol. 22, 1172-1183.
31. Kalani, M. Y., Cheshier, S. H., Cord, B. J., Bababeygy, S. R., Vogel, H., Weissman, I. L., Palmer, T. D. and Nusse, R. (2008). Wnt-mediated self-renewal of neural stem/progenitor cells. Proc. Natl. Acad. Sci. USA 105, 16970-16975.
32. Kuwabara, T., Hsieh, J., Muotri, A., Yeo, G., Warashina, M., Lie, D. C., Moore, L., Nakashima, K., Asashima, M. and Gage, F. H. (2009). Wnt-mediated activation of NeuroD1 and retro-elements during adult neurogenesis. Nat. Neurosci. 12, 1097-1105.
33. Leung, C. T., Coulombe, P. A. and Reed, R. R. (2007). Contribution of olfactory neural stem cells to tissue maintenance and regeneration. Nat. Neurosci. 10, 720-726.
34. Li, L. and Clevers, H. (2010). Coexistence of quiescent and active adult stem cells in mammals. Science 327, 542-545.
35. Lie, D. C., Colamarino, S. A., Song, H. J., Desire, L., Mira, H., Consiglio, A., Lein, E. S., Jessberger, S., Lansford, H., Dearie, A. R. et al. (2005). Wnt signalling regulates adult hippocampal neurogenesis. Nature 437, 1370-1375.
36. Logan, C. Y. and Nusse, R. (2004). The Wnt signaling pathway in development and disease. Annu. Rev. Cell Dev. Biol. 20, 781-810.
37. Loseva, E., Yuan, T. F. and Karnup, S. (2009). Neurogliogenesis in the mature olfactory system: a possible protective role against infection and toxic dust. Brain Res. Rev. 59, 374-387.
38. Lustig, B., Jerchow, B., Sachs, M., Weiler, S., Pietsch, T., Karsten, U., van de Wetering, M., Clevers, H., Schlag, P. M., Birchmeier, W. et al. (2002). Negative feedback loop of Wnt signaling through upregulation of conductin/axin2 in colorectal and liver tumors. Mol. Cell. Biol. 22, 1184-1193.
39. Lyu, J., Yamamoto, V. and Lu, W. (2008). Cleavage of the Wnt receptor Ryk regulates neuronal differentiation during cortical neurogenesis. Dev. Cell 15, 773-780.
40. Michaelidis, T. M. and Lie, D. C. (2008). Wnt signaling and neural stem cells: caught in the Wnt web. Cell Tissue Res. 331, 193-210.
41. Moon, R. T., Kohn, A. D., De Ferrari, G. V. and Kaykas, A. (2004). WNT and betacatenin signalling: diseases and therapies. Nat. Rev. Genet. 5, 691-701.
42. Murakami, A., Ashida, H. and Terao, J. (2008). Multitargeted cancer prevention by quercetin. Cancer Lett. 269, 315-325.
43. Murdoch, B. and Roskams, A. J. (2007). Olfactory epithelium progenitors: insights from transgenic mice and in vitro biology. J. Mol. Histol. 38, 581-599.
44. Muroyama, Y., Kondoh, H. and Takada, S. (2004). Wnt proteins promote neuronal differentiation in neural stem cell culture. Biochem. Biophys. Res. Commun. 313, 915-921.
45. Murrell, J. R. and Hunter, D. D. (1999). An olfactory sensory neuron line, odora, properly targets olfactory proteins and responds to odorants. J. Neurosci. 19, 8260-8270.
46. Nordstrom, U., Jessell, T. M. and Edlund, T. (2002). Progressive induction of caudal neural character by graded Wnt signaling. Nat. Neurosci. 5, 525-532.
47. Nusse, R. (2008). Wnt signaling and stem cell control. Cell Res. 18, 523-527.
48. Park, C. H., Chang, J. Y., Hahm, E. R., Park, S., Kim, H. K. and Yang, C. H. (2005). Quercetin, a potent inhibitor against beta-catenin/Tcf signaling in SW480 colon cancer cells. Biochem. Biophys. Res. Commun. 328, 227-234.
49. Piper, M., Barry, G., Hawkins, J., Mason, S., Lindwall, C., Little, E., Sarkar, A., Smith, A. G., Moldrich, R. X., Boyle, G. M. et al. (2010). NFIA controls telencephalic progenitor cell differentiation through repression of the Notch effector Hes1. J. Neurosci. 30, 9127-9139.
50. Ren, M., Senatorov, V. V., Chen, R. W. and Chuang, D. M. (2003). Postinsult treatment with lithium reduces brain damage and facilitates neurological recovery in a rat ischemia/reperfusion model. Proc. Natl. Acad. Sci. USA 100, 6210-6215.
51. Reya, T. and Clevers, H. (2005). Wnt signalling in stem cells and cancer. Nature 434, 843-850.
52. Reynolds, B. A. and Weiss, S. (1996). Clonal and population analyses demonstrate that an EGF-responsive mammalian embryonic CNS precursor is a stem cell. Dev. Biol. 175, 1-13.
53. Rodriguez-Gil, D. J. and Greer, C. A. (2008). Wnt/Frizzled family members mediate olfactory sensory neuron axon extension. J. Comp. Neurol. 511, 301-317.
54. Roman-Gomez, J., Cordeu, L., Agirre, X., Jimenez-Velasco, A., San Jose-Eneriz, E., Garate, L., Calasanz, M. J., Heiniger, A., Torres, A. and Prosper, F. (2007). Epigenetic regulation of Wnt-signaling pathway in acute lymphoblastic leukemia. Blood 109, 3462-3469.
55. Sakamoto, T., Kondo, K., Kashio, A., Suzukawa, K. and Yamasoba, T. (2007). Methimazole-induced cell death in rat olfactory receptor neurons occurs via apoptosis triggered through mitochondrial cytochrome c-mediated caspase-3 activation pathway. J. Neurosci. Res. 85, 548-557.
56. Schlachterman, A., Valle, F., Wall, K. M., Azios, N. G., Castillo, L., Morell, L., Washington, A. V., Cubano, L. A. and Dharmawardhane, S. F. (2008). Combined resveratrol, quercetin, and catechin treatment reduces breast tumor growth in a nude mouse model. Transl. Oncol. 1, 19-27.
57. Schwob, J. E. (2002). Neural regeneration and the peripheral olfactory system. Anat. Rec. 269, 33-49.
58. Sommer, L. (2004). Multiple roles of canonical Wnt signaling in cell cycle progression and cell lineage specification in neural development. Cell Cycle 3, 701-703.
59. Song, L., Li, Y., Wang, K., Wang, Y. Z., Molotkov, A., Gao, L., Zhao, T., Yamagami, T., Wang, Y., Gan, Q. et al. (2009). Lrp6-mediated canonical Wnt signaling is required for lip formation and fusion. Development 136, 3161-3171.
60. Song, L., Li, Y., Wang, K. and Zhou, C. J. (2010). Cardiac neural crest and outflow tract defects in Lrp6 mutant mice. Dev. Dyn. 239, 200-210.
61. Tome, M., Lindsay, S. L., Riddell, J. S. and Barnett, S. C. (2009). Identification of nonepithelial multipotent cells in the embryonic olfactory mucosa. Stem Cells 27, 2196-2208.
62. Tseng, A. S., Engel, F. B. and Keating, M. T. (2006). The GSK-3 inhibitor BIO promotes proliferation in mammalian cardiomyocytes. Chem. Biol. 13, 957-963.
63. Van Raay, T. J., Moore, K. B., Iordanova, I., Steele, M., Jamrich, M., Harris, W. A. and Vetter, M. L. (2005). Frizzled 5 signaling governs the neural potential of progenitors in the developing Xenopus retina. Neuron 46, 23-36.
64. Wang, Y. Z., Molotkov, A., Song, L., Li, Y., Pleasure, D. E. and Zhou, C. J. (2008). Activation of the Wnt/beta-catenin signaling reporter in developing mouse olfactory nerve layer marks a specialized subgroup of olfactory ensheathing cells. Dev. Dyn. 237, 3157-3168.
65. Wang, Y., Song, L. and Zhou, C. J. (2011). The canonical Wnt/β-catenin signaling pathway regulates Fgf signaling for early facial development. Dev. Biol. 349, 250-260.
66. Weeraratne, S. D., Valentine, M., Cusick, M., Delay, R. and Van Houten, J. L. (2006). Plasma membrane calcium pumps in mouse olfactory sensory neurons. Chem. Senses 31, 725-730.
67. Wexler, E. M., Geschwind, D. H. and Palmer, T. D. (2008). Lithium regulates adult hippocampal progenitor development through canonical Wnt pathway activation. Mol. Psychiatry 13, 285-292.
68. Yan, D., Wiesmann, M., Rohan, M., Chan, V., Jefferson, A. B., Guo, L., Sakamoto, D., Caothien, R. H., Fuller, J. H., Reinhard, C. et al. (2001). Elevated expression of axin2 and hnkd mRNA provides evidence that Wnt/beta-catenin signaling is activated in human colon tumors. Proc. Natl. Acad. Sci. USA 98, 14973-14978.
69. Zaghetto, A. A., Paina, S., Mantero, S., Platonova, N., Peretto, P., Bovetti, S., Puche, A., Piccolo, S. and Merlo, G. R. (2007). Activation of the Wnt-beta catenin pathway in a cell population on the surface of the forebrain is essential for the establishment of olfactory axon connections. J. Neurosci. 27, 9757-9768.
70. Zhou, C. J., Pinson, K. I. and Pleasure, S. J. (2004a). Severe defects in dorsal thalamic development in low-density lipoprotein receptor-related protein-6 mutants. J. Neurosci. 24, 7632-7639.
71. Zhou, C. J., Zhao, C. and Pleasure, S. J. (2004b). Wnt signaling mutants have decreased dentate granule cell production and radial glial scaffolding abnormalities. J. Neurosci. 24, 121-126.
72. Zhou, C. J., Borello, U., Rubenstein, J. L. and Pleasure, S. J. (2006). Neuronal production and precursor proliferation defects in the neocortex of mice with loss of function in the canonical Wnt signaling pathway. Neuroscience 142, 1119-1131.
73. Zhou, C. J., Molotkov, A., Song, L., Li, Y., Pleasure, D. E., Pleasure, S. J. and Wang, Y. Z. (2008). Ocular coloboma and dorsoventral neuroretinal patterning defects in Lrp6 mutant eyes. Dev. Dyn. 237, 3681-3689.