The Dual Origin of the Peripheral Olfactory System: Placode and Neural Crest

Overview

Journal Mol Brain

Publisher Biomed Central

Specialties Molecular Biology
Neurology

Date 2011 Sep 28

PMID 21943152

Citations 48

Authors

Hiroyuki Katoh

Shinsuke Shibata

Kimiko Fukuda

Momoka Sato

Etsuko Satoh

Narihito Nagoshi

Takeo Minematsu

Yumi Matsuzaki

Chihiro Akazawa

Yoshiaki Toyama

Masaya Nakamura

Hideyuki Okano

Affiliations

Soon will be listed here.

Abstract

Background: The olfactory epithelium (OE) has a unique capacity for continuous neurogenesis, extending axons to the olfactory bulb with the assistance of olfactory ensheathing cells (OECs). The OE and OECs have been believed to develop solely from the olfactory placode, while the neural crest (NC) cells have been believed to contribute only the underlying structural elements of the olfactory system. In order to further elucidate the role of NC cells in olfactory development, we examined the olfactory system in the transgenic mice Wnt1-Cre/Floxed-EGFP and P0-Cre/Floxed-EGFP, in which migrating NC cells and its descendents permanently express GFP, and conducted transposon-mediated cell lineage tracing studies in chick embryos.

Results: Examination of these transgenic mice revealed GFP-positive cells in the OE, demonstrating that NC-derived cells give rise to OE cells with morphologic and antigenic properties identical to placode-derived cells. OECs were also positive for GFP, confirming their NC origin. Cell lineage tracing studies performed in chick embryos confirmed the migration of NC cells into the OE. Furthermore, spheres cultured from the dissociated cells of the olfactory mucosa demonstrated self-renewal and trilineage differentiation capacities (neurons, glial cells, and myofibroblasts), demonstrating the presence of NC progenitors in the olfactory mucosa.

Conclusion: Our data demonstrates that the NC plays a larger role in the development of the olfactory system than previously believed, and suggests that NC-derived cells may in part be responsible for the remarkable capacity of the OE for neurogenesis and regeneration.

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References

Bhattacharyya A, Frank E, Ratner N, Brackenbury R . P0 is an early marker of the Schwann cell lineage in chickens. Neuron. 1991; 7(5):831-44. DOI: 10.1016/0896-6273(91)90285-8. View

Yoshida S, Shimmura S, Nagoshi N, Fukuda K, Matsuzaki Y, Okano H . Isolation of multipotent neural crest-derived stem cells from the adult mouse cornea. Stem Cells. 2006; 24(12):2714-22. DOI: 10.1634/stemcells.2006-0156. View

Dupin E, Nataf V, Le Douarin N . The ontogeny of the neural crest. C R Acad Sci III. 1993; 316(9):1062-81. View

Dymecki S, Tomasiewicz H . Using Flp-recombinase to characterize expansion of Wnt1-expressing neural progenitors in the mouse. Dev Biol. 1998; 201(1):57-65. DOI: 10.1006/dbio.1998.8971. View

Amoh Y, Li L, Katsuoka K, Hoffman R . Multipotent hair follicle stem cells promote repair of spinal cord injury and recovery of walking function. Cell Cycle. 2008; 7(12):1865-9. DOI: 10.4161/cc.7.12.6056. View

Matsuoka T, Ahlberg P, Kessaris N, Iannarelli P, Dennehy U, Richardson W . Neural crest origins of the neck and shoulder. Nature. 2005; 436(7049):347-55. PMC: 1352163. DOI: 10.1038/nature03837. View

Paratore C, Goerich D, Suter U, Wegner M, Sommer L . Survival and glial fate acquisition of neural crest cells are regulated by an interplay between the transcription factor Sox10 and extrinsic combinatorial signaling. Development. 2001; 128(20):3949-61. DOI: 10.1242/dev.128.20.3949. View

Liu F, Uchugonova A, Kimura H, Zhang C, Zhao M, Zhang L . The bulge area is the major hair follicle source of nestin-expressing pluripotent stem cells which can repair the spinal cord compared to the dermal papilla. Cell Cycle. 2011; 10(5):830-9. DOI: 10.4161/cc.10.5.14969. View

Murrell W, Feron F, Wetzig A, Cameron N, Splatt K, Bellette B . Multipotent stem cells from adult olfactory mucosa. Dev Dyn. 2005; 233(2):496-515. DOI: 10.1002/dvdy.20360. View

10.

Selleck M, Scherson T, Bronner-Fraser M . Origins of neural crest cell diversity. Dev Biol. 1993; 159(1):1-11. DOI: 10.1006/dbio.1993.1217. View

11.

Amoh Y, Li L, Campillo R, Kawahara K, Katsuoka K, Penman S . Implanted hair follicle stem cells form Schwann cells that support repair of severed peripheral nerves. Proc Natl Acad Sci U S A. 2005; 102(49):17734-8. PMC: 1308908. DOI: 10.1073/pnas.0508440102. View

12.

Leung C, Coulombe P, Reed R . Contribution of olfactory neural stem cells to tissue maintenance and regeneration. Nat Neurosci. 2007; 10(6):720-6. DOI: 10.1038/nn1882. View

13.

Morrison S, White P, Zock C, Anderson D . Prospective identification, isolation by flow cytometry, and in vivo self-renewal of multipotent mammalian neural crest stem cells. Cell. 1999; 96(5):737-49. DOI: 10.1016/s0092-8674(00)80583-8. View

14.

Le Douarin N, Renaud D, Teillet M, Le Douarin G . Cholinergic differentiation of presumptive adrenergic neuroblasts in interspecific chimeras after heterotopic transplantations. Proc Natl Acad Sci U S A. 1975; 72(2):728-32. PMC: 432389. DOI: 10.1073/pnas.72.2.728. View

15.

Uchugonova A, Duong J, Zhang N, Konig K, Hoffman R . The bulge area is the origin of nestin-expressing pluripotent stem cells of the hair follicle. J Cell Biochem. 2011; 112(8):2046-50. DOI: 10.1002/jcb.23122. View

16.

Kuratani S, Ninomiya Y, Aoki K, Iseki S, Chareonvit S, Doi H . Cranial anomaly of homozygous rSey rat is associated with a defect in the migration pathway of midbrain crest cells. Dev Growth Differ. 1997; 39(1):53-67. DOI: 10.1046/j.1440-169x.1997.00007.x. View

17.

Toma J, Akhavan M, Fernandes K, Sadikot A, Kaplan D, Miller F . Isolation of multipotent adult stem cells from the dermis of mammalian skin. Nat Cell Biol. 2001; 3(9):778-84. DOI: 10.1038/ncb0901-778. View

18.

Ramon-Cueto A, Avila J . Olfactory ensheathing glia: properties and function. Brain Res Bull. 1998; 46(3):175-87. DOI: 10.1016/s0361-9230(97)00463-2. View

19.

Echelard Y, Vassileva G, McMahon A . Cis-acting regulatory sequences governing Wnt-1 expression in the developing mouse CNS. Development. 1994; 120(8):2213-24. DOI: 10.1242/dev.120.8.2213. View

20.

Morikawa S, Mabuchi Y, Niibe K, Suzuki S, Nagoshi N, Sunabori T . Development of mesenchymal stem cells partially originate from the neural crest. Biochem Biophys Res Commun. 2009; 379(4):1114-9. DOI: 10.1016/j.bbrc.2009.01.031. View