Molecular Events in the Cell Types of the Olfactory Epithelium during Adult Neurogenesis

Authors

Paula M. Heron, University of KentuckyFollow
Arnold J. Stromberg, University of KentuckyFollow
Patrick Breheny, University of Iowa
Timothy S. McClintock, University of KentuckyFollow

Abstract

BACKGROUND: Adult neurogenesis, fundamental for cellular homeostasis in the mammalian olfactory epithelium, requires major shifts in gene expression to produce mature olfactory sensory neurons (OSNs) from multipotent progenitor cells. To understand these dynamic events requires identifying not only the genes involved but also the cell types that express each gene. Only then can the interrelationships of the encoded proteins reveal the sequences of molecular events that control the plasticity of the adult olfactory epithelium.

RESULTS: Of 4,057 differentially abundant mRNAs at 5 days after lesion-induced OSN replacement in adult mice, 2,334 were decreased mRNAs expressed by mature OSNs. Of the 1,723 increased mRNAs, many were expressed by cell types other than OSNs and encoded proteins involved in cell proliferation and transcriptional regulation, consistent with increased basal cell proliferation. Others encoded fatty acid metabolism and lysosomal proteins expressed by infiltrating macrophages that help scavenge debris from the apoptosis of mature OSNs. The mRNAs of immature OSNs behaved dichotomously, increasing if they supported early events in OSN differentiation (axon initiation, vesicular trafficking, cytoskeletal organization and focal adhesions) but decreasing if they supported homeostatic processes that carry over into mature OSNs (energy production, axon maintenance and protein catabolism). The complexity of shifts in gene expression responsible for converting basal cells into neurons was evident in the increased abundance of 203 transcriptional regulators expressed by basal cells and immature OSNs.

CONCLUSIONS: Many of the molecular changes evoked during adult neurogenesis can now be ascribed to specific cellular events in the OSN cell lineage, thereby defining new stages in the development of these neurons. Most notably, the patterns of gene expression in immature OSNs changed in a characteristic fashion as these neurons differentiated. Initial patterns were consistent with the transition into a neuronal morphology (neuritogenesis) and later patterns with neuronal homeostasis. Overall, gene expression patterns during adult olfactory neurogenesis showed substantial similarity to those of embryonic brain.

Document Type

Article

Publication Date

11-22-2013

Notes/Citation Information

Published in Molecular Brain, v. 6, 49, p. 1-14.

© 2013 Heron et al.; licensee BioMed Central Ltd.

This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Digital Object Identifier (DOI)

http://dx.doi.org/10.1186/1756-6606-6-49

Funding Information

Funded by R01 DC007194 and R21 DC009624 to T.Mc., F32 DC011427 to P.M.H. and UL1TR000117 to A.J.S.

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Repository Citation

Heron, Paula M.; Stromberg, Arnold J.; Breheny, Patrick; and McClintock, Timothy S., "Molecular Events in the Cell Types of the Olfactory Epithelium during Adult Neurogenesis" (2013). Physiology Faculty Publications. 18.
https://uknowledge.uky.edu/physiology_facpub/18