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Transcriptional regulatory network during development in the olfactory epithelium
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  • Journal title : BMB Reports
  • Volume 48, Issue 11,  2015, pp.599-608
  • Publisher : Korean Society for Biochemistry and Molecular Biology
  • DOI : 10.5483/BMBRep.2015.48.11.177
 Title & Authors
Transcriptional regulatory network during development in the olfactory epithelium
Im, SeungYeong; Moon, Cheil;
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Regeneration, a process of reconstitution of the entire tissue, occurs throughout life in the olfactory epithelium (OE). Regeneration of OE consists of several stages: proliferation of progenitors, cell fate determination between neuronal and non-neuronal lineages, their differentiation and maturation. How the differentiated cell types that comprise the OE are regenerated, is one of the central questions in olfactory developmental neurobiology. The past decade has witnessed considerable progress regarding the regulation of transcription factors (TFs) involved in the remarkable regenerative potential of OE. Here, we review current state of knowledge of the transcriptional regulatory networks that are powerful modulators of the acquisition and maintenance of developmental stages during regeneration in the OE. Advance in our understanding of regeneration will not only shed light on the basic principles of adult plasticity of cell identity, but may also lead to new approaches for using stem cells and reprogramming after injury or degenerative neurological diseases.
Neurogenesis;Olfactory epithelium;Regeneration;Stem cell;Transcription factor;
 Cited by
Graziadei GA and Graziadei PP (1979) Neurogenesis and neuron regeneration in the olfactory system of mammals. II. Degeneration and reconstitution of the olfactory sensory neurons after axotomy. J Neurocytol 8, 197-213 crossref(new window)

Graziadei PP, Levine RR and Monti Graziadei GA (1979) Plasticity of connections of the olfactory sensory neuron: regeneration into the forebrain following bulbectomy in the neonatal mouse. Neuroscience 4, 713-727 crossref(new window)

Mackay-Sim A and Kittel PW (1991) On the Life Span of Olfactory Receptor Neurons. Eur J Neurosci 3, 209-215 crossref(new window)

Smart IH (1971) Location and orientation of mitotic figures in the developing mouse olfactory epithelium. J Anat 109, 243-251

Bodian D and Howe HA (1941) Experimental studies on intraneural spread of poliomyelitis virus. Bulletin of the Johns Hopkins Hospital 68, 248-267

Rawson NE, Gomez G, Cowart B and Restrepo D (1998) The use of olfactory receptor neurons (ORNs) from biopsies to study changes in aging and neurodegenerative diseases. Ann N Y Acad Sci 855, 701-707 crossref(new window)

Lane AP, Gomez G, Dankulich T, Wang H, Bolger WE and Rawson NE (2002) The superior turbinate as a source of functional human olfactory receptor neurons. Laryngoscope 112, 1183-1189 crossref(new window)

Rawson NE and Gomez G (2002) Cell and molecular biology of human olfaction. Microsc Res Tech 58, 142-151 crossref(new window)

Gross CG (2000) Neurogenesis in the adult brain: death of a dogma. Nat Rev Neurosci 1, 67-73 crossref(new window)

Kempermann G and Gage FH (1999) New nerve cells for the adult brain. Sci Am 280, 48-53 crossref(new window)

Lie DC, Song H, Colamarino SA, Ming GL and Gage FH (2004) Neurogenesis in the adult brain: new strategies for central nervous system diseases. Annu Rev Pharmacol Toxicol 44, 399-421 crossref(new window)

Bailey BJ and Barton S (1975) Olfactory neuroblastoma. Management and prognosis. Arch Otolaryngol 101, 1-5 crossref(new window)

Cau E, Gradwohl G, Fode C and Guillemot F (1997) Mash1 activates a cascade of bHLH regulators in olfactory neuron progenitors. Development 124, 1611-1621

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

Manglapus GL, Youngentob SL and Schwob JE (2004) Expression patterns of basic helix-loop-helix transcription factors define subsets of olfactory progenitor cells. J Comp Neurol 479, 216-233 crossref(new window)

Eggan K, Baldwin K, Tackett M et al (2004) Mice cloned from olfactory sensory neurons. Nature 428, 44-49 crossref(new window)

Li J, Ishii T, Feinstein P and Mombaerts P (2004) Odorant receptor gene choice is reset by nuclear transfer from mouse olfactory sensory neurons. Nature 428, 393-399 crossref(new window)

Lindvall O and Bjorklund A (2004) Cell replacement therapy: helping the brain to repair itself. NeuroRx 1, 379-381 crossref(new window)

Rossi F and Cattaneo E (2002) Opinion: neural stem cell therapy for neurological diseases: dreams and reality. Nat Rev Neurosci 3, 401-409 crossref(new window)

Graziadei PPC and Montigraziadei GA (1979) Neurogenesis and Neuron Regeneration in the Olfactory System of Mammals .1. Morphological Aspects of Differentiation and Structural Organization of the Olfactory Sensory Neurons. J Neurocytol 8, 1-18 crossref(new window)

Moulton DG (1967) Olfaction in mammals. Am Zool 7, 421-429 crossref(new window)

Moulton DG and Beidler LM (1967) Structure and function in the peripheral olfactory system. Physiol Rev 47, 1-52

Doty RL (2001) Olfaction. Annu Rev Psychol 52, 423-452 crossref(new window)

Menco BP and Farbman AI (1992) Ultrastructural evidence for multiple mucous domains in frog olfactory epithelium. Cell Tissue Res 270, 47-56 crossref(new window)

Farbman AI and Buchholz JA (1992) Growth of olfactory epithelial tissue in vitro: lectin staining of axons. Microsc Res Tech 23, 173-180 crossref(new window)

Kaupp UB (2010) Olfactory signalling in vertebrates and insects: differences and commonalities. Nat Rev Neurosci 11, 188-200

Graziadei PP and Metcalf JF (1971) Autoradiographic and ultrastructural observations on the frog's olfactory mucosa. Z Zellforsch Mikrosk Anat 116, 305-318 crossref(new window)

Graziadei PP (1973) Cell dynamics in the olfactory mucosa. Tissue Cell 5, 113-131 crossref(new window)

Graziadei PP and DeHan RS (1973) Neuronal regeneration in frog olfactory system. J Cell Biol 59, 525-530 crossref(new window)

Hunter DD, Caggiano M and Kauer JS (1994) Lineage analysis of the olfactory epithelium using a replication-incompetent retrovirus. Chem Senses 19, 683-693 crossref(new window)

Roskams AJ, Cai X and Ronnett GV (1998) Expression of neuron-specific beta-III tubulin during olfactory neurogenesis in the embryonic and adult rat. Neuroscience 83, 191-200 crossref(new window)

Farbman AI and Margolis FL (1980) Olfactory marker protein during ontogeny: immunohistochemical localization. Dev Biol 74, 205-215 crossref(new window)

Hirsch JD and Margolis FL (1980) Influence of unilateral olfactory bulbectomy on opiate and other binding sites in the contralateral bulb. Brain Res 199, 39-47 crossref(new window)

Getchell TV, Zielinski B and Getchell ML (1985) Pyrazine-Mediated Neural and Secretory Activity in the Olfactory Mucosa of the Salamander. Chemical Senses 10, 398-399

Getchell TV (1986) Functional-Properties of Vertebrate Olfactory Receptor Neurons. Physiol Rev 66, 772-818

Nomura T, Takahashi S and Ushiki T (2004) Cytoarchitecture of the normal rat olfactory epithelium: light and scanning electron microscopic studies. Arch Histol Cytol 67, 159-170 crossref(new window)

Gu J, Zhang QY, Genter MB et al (1998) Purification and characterization of heterologously expressed mouse CYP2A5 and CYP2G1: role in metabolic activation of acetaminophen and 2,6-dichlorobenzonitrile in mouse olfactory mucosal microsomes. J Pharmacol Exp Ther 285, 1287-1295

Whitby-Logan GK, Weech M and Walters E (2004) Zonal expression and activity of glutathione S-transferase enzymes in the mouse olfactory mucosa. Brain Res 995, 151-157 crossref(new window)

Ling G, Gu J, Genter MB, Zhuo X and Ding X (2004) Regulation of cytochrome P450 gene expression in the olfactory mucosa. Chem Biol Interact 147, 247-258 crossref(new window)

Ding XX and Coon MJ (1988) Purification and characterization of two unique forms of cytochrome P-450 from rabbit nasal microsomes. Biochemistry 27, 8330-8337 crossref(new window)

Chen Y, Getchell ML, Ding X and Getchell TV (1992) Immunolocalization of two cytochrome P450 isozymes in rat nasal chemosensory tissue. Neuroreport 3, 749-752 crossref(new window)

Weiler E and Farbman AI (1998) Supporting cell proliferation in the olfactory epithelium decreases postnatally. Glia 22, 315-328 crossref(new window)

Schwob JE, Youngentob SL and Mezza RC (1995) Reconstitution of the rat olfactory epithelium after methyl bromide-induced lesion. J Comp Neurol 359, 15-37 crossref(new window)

Goldstein BJ and Schwob JE (1996) Analysis of the globose basal cell compartment in rat olfactory epithelium using GBC-1, a new monoclonal antibody against globose basal cells. J Neurosci 16, 4005-4016

Huard JM, Youngentob SL, Goldstein BJ, Luskin MB and Schwob JE (1998) Adult olfactory epithelium contains multipotent progenitors that give rise to neurons and non-neural cells. J Comp Neurol 400, 469-486 crossref(new window)

Huard JM and Schwob JE (1995) Cell cycle of globose basal cells in rat olfactory epithelium. Dev Dyn 203, 17-26 crossref(new window)

Carter LA, MacDonald JL and Roskams AJ (2004) Olfactory horizontal basal cells demonstrate a conserved multipotent progenitor phenotype. J Neurosci 24, 5670-5683 crossref(new window)

Leung CT, Coulombe PA and Reed RR (2007) Contribution of olfactory neural stem cells to tissue maintenance and regeneration. Nat Neurosci 10, 720-726 crossref(new window)

Iwai N, Zhou Z, Roop DR and Behringer RR (2008) Horizontal basal cells are multipotent progenitors in normal and injured adult olfactory epithelium. Stem Cells 26, 1298-1306 crossref(new window)

Beites CL, Kawauchi S, Crocker CE and Calof AL (2005) Identification and molecular regulation of neural stem cells in the olfactory epithelium. Exp Cell Res 306, 309-316 crossref(new window)

Caggiano M, Kauer JS and 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 crossref(new window)

Cowan CM and Roskams AJ (2002) Apoptosis in the mature and developing olfactory neuroepithelium. Microsc Res Tech 58, 204-215 crossref(new window)

Hurtt ME, Thomas DA, Working PK, Monticello TM and Morgan KT (1988) Degeneration and regeneration of the olfactory epithelium following inhalation exposure to methyl bromide: pathology, cell kinetics, and olfactory function. Toxicol Appl Pharmacol 94, 311-328 crossref(new window)

Cancalon P (1982) Degeneration and regeneration of olfactory cells induced by ZnSO4 and other chemicals. Tissue Cell 14, 717-733 crossref(new window)

Calof AL and Chikaraishi DM (1989) Analysis of neurogenesis in a mammalian neuroepithelium: proliferation and differentiation of an olfactory neuron precursor in vitro. Neuron 3, 115-127 crossref(new window)

Gordon MK, Mumm JS, Davis RA, Holcomb JD and Calof AL (1995) Dynamics of MASH1 expression in vitro and in vivo suggest a non-stem cell site of MASH1 action in the olfactory receptor neuron lineage. Mol Cell Neurosci 6, 363-379 crossref(new window)

Chen X, Fang H and Schwob JE (2004) Multipotency of purified, transplanted globose basal cells in olfactory epithelium. J Comp Neurol 469, 457-474 crossref(new window)

Gokoffski KK, Wu HH, Beites CL et al (2011) Activin and GDF11 collaborate in feedback control of neuroepithelial stem cell proliferation and fate. Development 138, 4131-4142 crossref(new window)

Carr VM and 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 crossref(new window)

Li L and Clevers H (2010) Coexistence of quiescent and active adult stem cells in mammals. Science 327, 542-545 crossref(new window)

Fletcher RB, Prasol MS, Estrada J et al (2011) p63 regulates olfactory stem cell self-renewal and differentiation. Neuron 72, 748-759 crossref(new window)

Cuschieri A and Bannister LH (1975) The development of the olfactory mucosa in the mouse: electron microscopy. J Anat 119, 471-498

Marcucci F, Zou DJ and Firestein S (2009) Sequential onset of presynaptic molecules during olfactory sensory neuron maturation. J Comp Neurol 516, 187-198 crossref(new window)

Mombaerts P, Wang F, Dulac C et al (1996) Visualizing an olfactory sensory map. Cell 87, 675-686 crossref(new window)

Schwarzenbacher K, Fleischer J and Breer H (2005) Formation and maturation of olfactory cilia monitored by odorant receptor-specific antibodies. Histochem Cell Biol 123, 419-428 crossref(new window)

Shetty RS, Bose SC, Nickell MD et al (2005) Transcriptional changes during neuronal death and replacement in the olfactory epithelium. Mol Cell Neurosci 30, 583-600 crossref(new window)

Goldstein BJ, Fang H, Youngentob SL and Schwob JE (1998) Transplantation of multipotent progenitors from the adult olfactory epithelium. Neuroreport 9, 1611-1617 crossref(new window)

Davis RL and Turner DL (2001) Vertebrate hairy and Enhancer of split related proteins: transcriptional repressors regulating cellular differentiation and embryonic patterning. Oncogene 20, 8342-8357 crossref(new window)

Donner AL, Episkopou V and Maas RL (2007) Sox2 and Pou2f1 interact to control lens and olfactory placode development. Dev Biol 303, 784-799 crossref(new window)

Pevny LH and Lovell-Badge R (1997) Sox genes find their feet. Curr Opin Genet Dev 7, 338-344 crossref(new window)

Pevny L and Placzek M (2005) SOX genes and neural progenitor identity. Curr Opin Neurobiol 15, 7-13 crossref(new window)

Takahashi K and Yamanaka S (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126, 663-676 crossref(new window)

Brazel CY, Limke TL, Osborne JK et al (2005) Sox2 expression defines a heterogeneous population of neurosphere- forming cells in the adult murine brain. Aging Cell 4, 197-207 crossref(new window)

Walther C and Gruss P (1991) Pax-6, a murine paired box gene, is expressed in the developing CNS. Development 113, 1435-1449

Collinson JM, Quinn JC, Hill RE and West JD (2003) The roles of Pax6 in the cornea, retina, and olfactory epithelium of the developing mouse embryo. Dev Biol 255, 303-312 crossref(new window)

Davis JA and Reed RR (1996) Role of Olf-1 and Pax-6 transcription factors in neurodevelopment. J Neurosci 16, 5082-5094

Guo Z, Packard A, Krolewski RC, Harris MT, Manglapus GL and Schwob JE (2010) Expression of pax6 and sox2 in adult olfactory epithelium. J Comp Neurol 518, 4395-4418 crossref(new window)

Osada M, Ohba M, Kawahara C et al (1998) Cloning and functional analysis of human p51, which structurally and functionally resembles p53. Nat Med 4, 839-843 crossref(new window)

Yang A, Kaghad M, Wang Y et al (1998) p63, a p53 homolog at 3q27-29, encodes multiple products with transactivating, death-inducing, and dominant-negative activities. Mol Cell 2, 305-316 crossref(new window)

Packard A, Schnittke N, Romano RA, Sinha S and Schwob JE (2011) Delta Np63 Regulates Stem Cell Dynamics in the Mammalian Olfactory Epithelium. J Neurosci 31, 8748-8759 crossref(new window)

Ball DW, Azzoli CG, Baylin SB et al (1993) Identification of a human achaete-scute homolog highly expressed in neuroendocrine tumors. Proc Natl Acad Sci U S A 90, 5648-5652 crossref(new window)

Jasoni CL, Walker MB, Morris MD and Reh TA (1994) A chicken achaete-scute homolog (CASH-1) is expressed in a temporally and spatially discrete manner in the developing nervous system. Development 120, 769-783

Nelson BR, Hartman BH, Ray CA, Hayashi T, Bermingham-McDonogh O and Reh TA (2009) Acheate-scute like 1 (Ascl1) is required for normal delta-like (Dll) gene expression and notch signaling during retinal development. Dev Dyn 238, 2163-2178 crossref(new window)

Theriault FM, Nuthall HN, Dong Z et al (2005) Role for Runx1 in the proliferation and neuronal differentiation of selected progenitor cells in the mammalian nervous system. J Neurosci 25, 2050-2061 crossref(new window)

Noda M and Harada Y (1981) Development of Olfactory Epithelium in the Mouse - Scanning Electron-Microscopy. Biomedical Research-Tokyo 2, 449-454

Holbrook EH, Szumowski KE and Schwob JE (1995) An immunochemical, ultrastructural, and developmental characterization of the horizontal basal cells of rat olfactory epithelium. J Comp Neurol 363, 129-146 crossref(new window)

Nibu K, Li G, Zhang X et al (1999) Olfactory neuron-specific expression of NeuroD in mouse and human nasal mucosa. Cell Tissue Res 298, 405-414 crossref(new window)

Heron PM, Stromberg AJ, Breheny P and McClintock TS (2013) Molecular events in the cell types of the olfactory epithelium during adult neurogenesis. Mol Brain 6, 49 crossref(new window)

Suzuki J, Yoshizaki K, Kobayashi T and Osumi N (2013) Neural crest-derived horizontal basal cells as tissue stem cells in the adult olfactory epithelium. Neurosci Res 75, 112-120 crossref(new window)

Ikeda K, Kageyama R, Suzuki Y and Kawakami K (2010) Six1 is indispensable for production of functional progenitor cells during olfactory epithelial development. Int J Dev Biol 54, 1453-1464 crossref(new window)

Malgaretti N, Pozzoli O, Bosetti A et al (1997) Mmot1, a new helix-loop-helix transcription factor gene displaying a sharp expression boundary in the embryonic mouse brain. J Biol Chem 272, 17632-17639 crossref(new window)

Kudrycki K, Stein-Izsak C, Behn C, Grillo M, Akeson R and Margolis FL (1993) Olf-1-binding site: characterization of an olfactory neuron-specific promoter motif. Mol Cell Biol 13, 3002-3014 crossref(new window)

Wang MM, Tsai RY, Schrader KA and Reed RR (1993) Genes encoding components of the olfactory signal transduction cascade contain a DNA binding site that may direct neuronal expression. Mol Cell Biol 13, 5805-5813 crossref(new window)

Wang SS, Tsai RY and Reed RR (1997) The characterization of the Olf-1/EBF-like HLH transcription factor family: implications in olfactory gene regulation and neuronal development. J Neurosci 17, 4149-4158

Wang SS, Betz AG and Reed RR (2002) Cloning of a novel Olf-1/EBF-like gene, O/E-4, by degenerate oligo-based direct selection. Mol Cell Neurosci 20, 404-414 crossref(new window)

Wang SS, Lewcock JW, Feinstein P, Mombaerts P and Reed RR (2004) Genetic disruptions of O/E2 and O/E3 genes reveal involvement in olfactory receptor neuron projection. Development 131, 1377-1388 crossref(new window)

Lin H and Grosschedl R (1995) Failure of B-cell differentiation in mice lacking the transcription factor EBF. Nature 376, 263-267 crossref(new window)

Behrens M, Venkatraman G, Gronostajski RM, Reed RR and Margolis FL (2000) NFI in the development of the olfactory neuroepithelium and the regulation of olfactory marker protein gene expression. Eur J Neurosci 12, 1372-1384 crossref(new window)

Moon C, Yoo JY, Matarazzo V, Sung YK, Kim EJ and Ronnett GV (2002) Leukemia inhibitory factor inhibits neuronal terminal differentiation through STAT3 activation. Proc Natl Acad Sci U S A 99, 9015-9020 crossref(new window)