A Possible Role of Neuroglobin in the Retina After Optic Nerve Injury: A Comparative Study of Zebrafish and Mouse Retina

Sugitani, Kayo; Koriyama, Yoshiki; Ogai, Kazuhiro; Wakasugi, Keisuke; Kato, Satoru

doi:10.1007/978-3-319-17121-0_89

Cited by 13 publications

(11 citation statements)

References 14 publications

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“…Previously, we found that in the zebrafish retina, Ngb mRNA is expressed in amacrine cells, whereas Ngb proteins are expressed in both amacrine cells and the inner plexiform layer [16]. In the present study, we confirmed that Ngb proteins are only expressed in the RGCs of the mouse retina [27,38]. The localization of Ngb proteins in the inner plexiform layer of the zebrafish is easily imaged due to the secretion of Ngb from the amacrine cells and the cell membrane-penetrating module of zebrafish Ngb.…”

Section: Comparative Studies Of the Ngb System In The Mouse And Zebrasupporting

confidence: 89%

“…In a previous study, we found that Ngb mRNA and Ngb proteins were transiently upregulated in the zebrafish retina 3 days after optic nerve injury, only to return to control levels 7 days later [16]. In vitro studies have shown that overexpression of mouse Ngb protein enhances cell viability under hypoxia / reoxygenation conditions [27]. Additionally, we have confirmed that chimeric human Ngb promotes neurite outgrowth activity in rat pheochromocytoma PC12 cells [28].…”

Section: Introductionsupporting

confidence: 64%

“…The localization of Ngb proteins in the inner plexiform layer of the zebrafish is easily imaged due to the secretion of Ngb from the amacrine cells and the cell membrane-penetrating module of zebrafish Ngb. Moreover, optic nerve injury induces a transient increase in Ngb protein levels within amacrine cells and the inner plexiform layer of the zebrafish retina 3-5 days after axotomy [16,27]. This period is considered to be the early stage of the zebrafish optic nerve regeneration process (the preparation period, [19]).…”

Section: Comparative Studies Of the Ngb System In The Mouse And Zebramentioning

confidence: 99%

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A novel function of neuroglobin for neuroregeneration in mice after optic nerve injury

Sugitani

Koriyama

Sera

et al. 2017

Biochemical and Biophysical Research Communications

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Neuroglobin (Ngb) is a recently discovered heme protein in the vertebrate brain that can bind to oxygen molecules. Mammalian Ngb plays a crucial role in neuroprotection under conditions of oxidative stress. To investigate other potential functions of Ngb, we investigated the mouse retinal Ngb system following optic nerve injury. In the retina of control mice, Ngb immunoreactivity was limited to the retinal ganglion cell (RGC) layer, and this immunoreactivity rapidly decreased to less than 50% of the control level 5 days after optic nerve injury. On the basis of this decrease, we designed in vivo experiments with enhanced expression of Ngb using adult mouse retina. The enhanced expression of Ngb was achieved by injecting chimeric human Ngb protein, which included the cell membrane-penetrating module of fish Ngb. One-day pretreatment with chimeric Ngb increased immunoreactivity levels of Ngb two-fold in mouse RGCs and increased the number of surviving RGCs three-fold by 14 days after optic nerve injury compared with vehicle controls. Furthermore, in the mouse retinas showing enhanced Ngb expression, several regenerating central optic axons exhibited outgrowth and were found to pass through the nerve crush site 14 days after nerve injury. No such regenerating optic axons were observed in the control mouse optic nerve during the same time frame. The data obtained from in vivo experiments strongly indicate that mammalian Ngb has neuroprotective and neuroregenerative properties.

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Section: Comparative Studies Of the Ngb System In The Mouse And Zebrasupporting

confidence: 89%

Section: Introductionsupporting

confidence: 64%

Section: Comparative Studies Of the Ngb System In The Mouse And Zebramentioning

confidence: 99%

See 1 more Smart Citation

A novel function of neuroglobin for neuroregeneration in mice after optic nerve injury

Sugitani

Koriyama

Sera

et al. 2017

Biochemical and Biophysical Research Communications

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“…Recently, it was reported that overexpression of human Ngb promotes neurite outgrowth in mouse neuroblastoma N2a cells and in primary cultured rat cortical neurons [30] and that the overexpression of mouse Ngb in RGC-5 cells significantly increases the length of neurite outgrowth [31]. In addition, it was also noted that Ngb is expressed during neuronal differentiation of human embryonic stem cells in vitro and in the neurogenic subventricular zone of adult rats in vivo [37].…”

Section: Discussionmentioning

confidence: 99%

Chimeric ZHHH neuroglobin acts as a cell membrane‐penetrating inducer of neurite outgrowth

et al. 2017

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Neuroglobin (Ngb) is a heme protein expressed in the vertebrate brain. We previously engineered a chimeric Ngb protein, in which module M1 of human Ngb is replaced by that of zebrafish Ngb, and showed that the chimeric ZHHH Ngb has a cell membrane‐penetrating activity similar to that of zebrafish Ngb and also rescues cells from death caused by hypoxia/reoxygenation as does human Ngb. Recently, it was reported that overexpression of mammalian Ngb in neuronal cells induces neurite outgrowth. In this study, we performed neurite outgrowth assays of chimeric Ngb using rat pheochromocytoma PC 12 cells. Addition of chimeric Ngb, but not human or zebrafish Ngb, exogenously to the cell medium induces neurite outgrowth. On the other hand, the K7A/K9Q chimeric Ngb double mutant, which cannot translocate into cells, did not induce neurite outgrowth, suggesting that the cell membrane‐penetrating activity of the chimeric Ngb is crucial for its neurite outgrowth‐promoting activity. We also prepared several site‐directed chimeric Ngb mutants and demonstrated that residues crucial for neurite outgrowth‐inducing activity of the chimeric Ngb are not exactly the same as those for its neuroprotective activity.

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“…These simplified systems with strict control of environmental factors are beneficial in terms of time and cost-savings and often required to gain further insights in findings emerging from in vivo investigations (Koechling et al 2011). Within the field of in vitro studies, two main approaches can be distinguished: the use of an immortalized cell line, and primary RGC cultures (Goritz et al 2007;Koriyama et al 2011;Gupta et al 2013;Steketee et al 2014;Sugitani et al 2016). Immortalized cell lines offer the advantage of easy culturing and rapid growth.…”

Section: In Vitro Cellular Studies In Rodentsmentioning

confidence: 99%

Complementary research models and methods to study axonal regeneration in the vertebrate retinofugal system

et al. 2017

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Due to the lack of axonal regeneration, age-related deterioration in the central nervous system (CNS) poses a significant burden on the wellbeing of a growing number of elderly. To overcome this regenerative failure and to improve the patient's life quality, the search for novel regenerative treatment strategies requires valuable (animal) models and techniques. As an extension of the CNS, the retinofugal system, consisting of retinal ganglion cells that send their axons along the optic nerve to the visual brain areas, has importantly contributed to the current knowledge on mechanisms underlying the restricted regenerative capacities and to the development of novel strategies to enhance axonal regeneration. It provides an extensively used research tool, not only in amniote vertebrates including rodents, but also in anamniote vertebrates, such as zebrafish. Indeed, the latter show robust regeneration capacities, thereby providing insights into the factors that contribute to axonal regrowth and proper guidance, complementing studies in mammals. This review provides an integrative and critical overview of the classical and state-of-the-art models and methods that have been employed in the retinofugal system to advance our knowledge on the signaling pathways underlying the restricted versus robust axonal regeneration in rodents and zebrafish, respectively. In vitro, ex vivo and in vivo models and techniques to improve the visualization and analysis of regenerating axons are summarized. As such, the retinofugal system is presented as a valuable model to further facilitate research on axonal regeneration and to open novel therapeutic avenues for CNS pathologies.

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A Possible Role of Neuroglobin in the Retina After Optic Nerve Injury: A Comparative Study of Zebrafish and Mouse Retina

Cited by 13 publications

References 14 publications

A novel function of neuroglobin for neuroregeneration in mice after optic nerve injury

A novel function of neuroglobin for neuroregeneration in mice after optic nerve injury

Chimeric ZHHH neuroglobin acts as a cell membrane‐penetrating inducer of neurite outgrowth

Complementary research models and methods to study axonal regeneration in the vertebrate retinofugal system

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