Olfactory ensheathing cells are the main phagocytic cells that remove axon debris during early development of the olfactory system

Lynnmaria Nazareth, Katie E. Lineburg, Meng Inn Chuah, Johana Tello Velasquez, Fatemeh Chehrehasa, James A. St John, Jenny A K Ekberg

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Abstract

During development of the primary olfactory system, axon targeting is inaccurate and axons inappropriately project within the target layer or overproject into the deeper layers of the olfactory bulb. As a consequence there is considerable apoptosis of primary olfactory neurons during embryonic and postnatal development and axons of the degraded neurons need to be removed. Olfactory ensheathing cells (OECs) are the glia of the primary olfactory nerve and are known to phagocytose axon debris in the adult and postnatal animal. However, it is unclear when phagocytosis by OECs first commences. We investigated the onset of phagocytosis by OECs in the developing mouse olfactory system by utilizing two transgenic reporter lines: OMP-ZsGreen mice which express bright green fluorescent protein in primary olfactory neurons, and S100β-DsRed mice which express red fluorescent protein in OECs. In crosses of these mice, the fate of the degraded axon debris is easily visualized. We found evidence of axon degradation at embryonic day (E)13.5. Phagocytosis of the primary olfactory axon debris by OECs was first detected at E14.5. Phagocytosis of axon debris continued into the postnatal animal during the period when there was extensive mistargeting of olfactory axons. Macrophages were often present in close proximity to OECs but they contributed only a minor role to clearing the axon debris, even after widespread degeneration of olfactory neurons by unilateral bulbectomy and methimazole treatment. These results demonstrate that from early in embryonic development OECs are the primary phagocytic cells of the primary olfactory nerve. J. Comp. Neurol. 523:479-494, 2015.

Original languageEnglish
Pages (from-to)479-494
Number of pages16
JournalJournal of Comparative Neurology
Volume523
Issue number3
DOIs
Publication statusPublished - 15 Feb 2015
Externally publishedYes

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Phagocytes
Axons
Phagocytosis
Olfactory Nerve
Neurons
Embryonic Development
Methimazole
Nerve Degeneration
Olfactory Bulb
Green Fluorescent Proteins
Neuroglia
Macrophages
Apoptosis

Cite this

Nazareth, L., Lineburg, K. E., Chuah, M. I., Tello Velasquez, J., Chehrehasa, F., St John, J. A., & Ekberg, J. A. K. (2015). Olfactory ensheathing cells are the main phagocytic cells that remove axon debris during early development of the olfactory system. Journal of Comparative Neurology, 523(3), 479-494. https://doi.org/10.1002/cne.23694
Nazareth, Lynnmaria ; Lineburg, Katie E. ; Chuah, Meng Inn ; Tello Velasquez, Johana ; Chehrehasa, Fatemeh ; St John, James A. ; Ekberg, Jenny A K. / Olfactory ensheathing cells are the main phagocytic cells that remove axon debris during early development of the olfactory system. In: Journal of Comparative Neurology. 2015 ; Vol. 523, No. 3. pp. 479-494.
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abstract = "During development of the primary olfactory system, axon targeting is inaccurate and axons inappropriately project within the target layer or overproject into the deeper layers of the olfactory bulb. As a consequence there is considerable apoptosis of primary olfactory neurons during embryonic and postnatal development and axons of the degraded neurons need to be removed. Olfactory ensheathing cells (OECs) are the glia of the primary olfactory nerve and are known to phagocytose axon debris in the adult and postnatal animal. However, it is unclear when phagocytosis by OECs first commences. We investigated the onset of phagocytosis by OECs in the developing mouse olfactory system by utilizing two transgenic reporter lines: OMP-ZsGreen mice which express bright green fluorescent protein in primary olfactory neurons, and S100β-DsRed mice which express red fluorescent protein in OECs. In crosses of these mice, the fate of the degraded axon debris is easily visualized. We found evidence of axon degradation at embryonic day (E)13.5. Phagocytosis of the primary olfactory axon debris by OECs was first detected at E14.5. Phagocytosis of axon debris continued into the postnatal animal during the period when there was extensive mistargeting of olfactory axons. Macrophages were often present in close proximity to OECs but they contributed only a minor role to clearing the axon debris, even after widespread degeneration of olfactory neurons by unilateral bulbectomy and methimazole treatment. These results demonstrate that from early in embryonic development OECs are the primary phagocytic cells of the primary olfactory nerve. J. Comp. Neurol. 523:479-494, 2015.",
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Nazareth, L, Lineburg, KE, Chuah, MI, Tello Velasquez, J, Chehrehasa, F, St John, JA & Ekberg, JAK 2015, 'Olfactory ensheathing cells are the main phagocytic cells that remove axon debris during early development of the olfactory system' Journal of Comparative Neurology, vol. 523, no. 3, pp. 479-494. https://doi.org/10.1002/cne.23694

Olfactory ensheathing cells are the main phagocytic cells that remove axon debris during early development of the olfactory system. / Nazareth, Lynnmaria; Lineburg, Katie E.; Chuah, Meng Inn; Tello Velasquez, Johana; Chehrehasa, Fatemeh; St John, James A.; Ekberg, Jenny A K.

In: Journal of Comparative Neurology, Vol. 523, No. 3, 15.02.2015, p. 479-494.

Research output: Contribution to journalArticleResearchpeer-review

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T1 - Olfactory ensheathing cells are the main phagocytic cells that remove axon debris during early development of the olfactory system

AU - Nazareth, Lynnmaria

AU - Lineburg, Katie E.

AU - Chuah, Meng Inn

AU - Tello Velasquez, Johana

AU - Chehrehasa, Fatemeh

AU - St John, James A.

AU - Ekberg, Jenny A K

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AB - During development of the primary olfactory system, axon targeting is inaccurate and axons inappropriately project within the target layer or overproject into the deeper layers of the olfactory bulb. As a consequence there is considerable apoptosis of primary olfactory neurons during embryonic and postnatal development and axons of the degraded neurons need to be removed. Olfactory ensheathing cells (OECs) are the glia of the primary olfactory nerve and are known to phagocytose axon debris in the adult and postnatal animal. However, it is unclear when phagocytosis by OECs first commences. We investigated the onset of phagocytosis by OECs in the developing mouse olfactory system by utilizing two transgenic reporter lines: OMP-ZsGreen mice which express bright green fluorescent protein in primary olfactory neurons, and S100β-DsRed mice which express red fluorescent protein in OECs. In crosses of these mice, the fate of the degraded axon debris is easily visualized. We found evidence of axon degradation at embryonic day (E)13.5. Phagocytosis of the primary olfactory axon debris by OECs was first detected at E14.5. Phagocytosis of axon debris continued into the postnatal animal during the period when there was extensive mistargeting of olfactory axons. Macrophages were often present in close proximity to OECs but they contributed only a minor role to clearing the axon debris, even after widespread degeneration of olfactory neurons by unilateral bulbectomy and methimazole treatment. These results demonstrate that from early in embryonic development OECs are the primary phagocytic cells of the primary olfactory nerve. J. Comp. Neurol. 523:479-494, 2015.

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