Globins in <i>Caenorhabditis elegans</i>

Tilleman, Lesley; Germani, Francesca; Henau, Sasha De; Geuens, Eva; Hoogewijs, David; Braeckman, Bart P.; Vanfleteren, Jacques R.; Moëns, Luc; Dewilde, Sylvia

doi:10.1002/iub.443

Cited by 23 publications

(22 citation statements)

References 35 publications

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“…The C. elegans genome encodes a variety of other neurally expressed globins that may similarly modify neural function (8). It would be interesting to investigate whether neuroglobin alters information processing in vertebrate neural circuits.…”

Section: Discussionmentioning

confidence: 99%

“…They have been proposed to metabolize reactive oxygen species (ROS), signal redox state, store O 2 , control apoptosis, and negatively regulate Gi/o signaling (7). The genome of Caenorhabditis elegans encodes an unusually large family of globins, and many are expressed in neurons (8). One of these, GLOBIN-5 (GLB-5), is expressed in the oxygen sensing neurons URX, AQR, PQR, and BAG, where it accumulates at dendritic endings (9,10).…”

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confidence: 99%

“…The URX O 2 receptors exhibit phasic-tonic signaling properties and, in response to changes in O 2 concentration, evoke both transient behavioral responses that are coupled to the rate of change of O 2 , dO 2 /dt, and more persistent behavioral responses coupled to O 2 levels (8,13). The transient responses are reversals and turns that allow C. elegans to navigate O 2 gradients.…”

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confidence: 99%

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Modulation of sensory information processing by a neuroglobin in Caenorhabditis elegans

Oda

Toyoshima

Bono

2017

Proc. Natl. Acad. Sci. U.S.A.

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T he response properties of sensory neurons can be characterized by tuning curves that relate stimulus parameters to the evoked response (1, 2). Some sensory neurons show dynamic ranges that span several orders of stimulus magnitude (e.g., odor concentration), whereas others show remarkably narrow tuning curves. For example, glomus cells of the carotid body show oxygenevoked responses that are tuned to a twofold to threefold change in O 2 levels at the physiologically appropriate O 2 concentration range (3, 4). How such sharp tuning is achieved is poorly understood.Neuroglobins are members of the globin family of hemebinding proteins expressed mainly in neurons (5). They have been described throughout metazoa, from cnidarians to man (6). Their physiological functions are unclear. They have been proposed to metabolize reactive oxygen species (ROS), signal redox state, store O 2 , control apoptosis, and negatively regulate Gi/o signaling (7). The genome of Caenorhabditis elegans encodes an unusually large family of globins, and many are expressed in neurons (8). One of these, GLOBIN-5 (GLB-5), is expressed in the oxygen sensing neurons URX, AQR, PQR, and BAG, where it accumulates at dendritic endings (9, 10). C. elegans avoids both normoxia (21% O 2 ) and hypoxia (11). Avoidance of 21% O 2 enables the animal to escape the surface and is mediated by O 2 receptors, most importantly the glb-5-expressing URX, AQR, and PQR neurons (12). Like vertebrate neuroglobins, GLB-5 has the spectroscopic fingerprints of a hexa-coordinated heme iron and rapidly oxidizes to the ferric state in normoxia (9). The glb-5 gene is defective in the domesticated reference strain of C. elegans, N2 (Bristol), but natural isolates encode a functional allele, glb-5(Haw) (9, 10) (Haw refers to Hawaii, the geographical origin of the natural isolate in which this allele was first described). Behavioral and Ca 2+ imaging studies suggest that functional GLB-5 alters the properties of the O 2 receptors and C. elegans' O 2 responses (9, 10). However, how GLB-5 alters the representation of environmental information in these neurons leading to behavioral change is unknown.The URX O 2 receptors exhibit phasic-tonic signaling properties and, in response to changes in O 2 concentration, evoke both transient behavioral responses that are coupled to the rate of change of O 2 , dO 2 /dt, and more persistent behavioral responses coupled to O 2 levels (8, 13). The transient responses are reversals and turns that allow C. elegans to navigate O 2 gradients. The sustained responses involve persistent changes in the rate of movement that enable feeding animals to escape 21% O 2 or to accumulate in preferred lower O 2 environments. Besides GLB-5, the URX neurons express another putative molecular O 2 sensor, a soluble guanylate cyclase composed of GCY-35 and GCY-36 (guanylate cyclase) subunits (11,13,14). These soluble guanylate cyclases have a heme-nitric oxide/oxygen (H-NOX) binding domain that appears to stimulate cGMP production upon binding molecular O 2 (10, ...

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Section: Discussionmentioning

confidence: 99%

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confidence: 99%

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confidence: 99%

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Modulation of sensory information processing by a neuroglobin in Caenorhabditis elegans

Oda

Toyoshima

Bono

2017

Proc. Natl. Acad. Sci. U.S.A.

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“…C. elegans has 302 neuronal cells, which comprise one-third of somatic cells. Interestingly, the globin-like proteins are mainly expressed in neurons of C. elegans (10,11). It was reported that behavioral responses of C. elegans to chemicals and gases are controlled by gene activities that are mostly deployed in neurons (12)(13)(14).…”

Section: Introductionmentioning

confidence: 99%

GLB‐13 is associated with oxidative stress resistance in caenorhabditis elegans

Ren

Han

et al. 2013

IUBMB Life

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Globins constitute a superfamily of heme-binding proteins that is widely present in many species. There are 33 putative globins in the genome of Caenorhabditis elegans, where glb-13 is a homolog of neuroglobin (Ngb) based on sequence analysis and specific expression in neurons. Here we examined whether glb-13 as well as Ngb is also associated with resistance to reactive oxygen species (ROS) induced by paraquat. Our results showed that the mRNA level of glb-13 was significantly upregulated after paraquat exposure. Expression of a green fluorescent protein (GFP) reporter gene directed by the glb-13 promoter was increased by paraquat exposure. The mutant C. elegans strain glb-13(tm2825) was sensitive to paraquat-induced oxidative stress. Overexpression of human Ngb (hNgb) in C. elegans neuronal cells can rescue the paraquat sensitive phenotype of the mutant strain. glb-13 mutation or hNgb overexpression did not affect the expression of antioxidant enzymes such as superoxide dismutase (SOD). To examine the ROS-scavenging capabilities of hNgb and glb-13, we further examined the level of ROS in glb-13 mutant and hNgb transgenic (hNgb-Tg) worms. There was no statistical difference in ROS levels in the untreated controls; however in paraquattreated worms, the ROS level was statistically repressed in the hNgb-Tg relative to enhanced green fluorescent protein (EGFP)-Tg worms or wildtype animals. Additionally, the ROS level of glb-13 mutant was statistically higher than the wildtype animals. Furthermore, hNgb overexpression diminished the ROS level of glb-13 mutant. In conclusion, hNgb can rescue the ROS sensitive phenotype of the glb-13 mutant strain. The protein GLB-13 seems to have an hNgb-like function, suggesting the importance of the globin protein family in maintaining the homeostasis of ROS signals. Our data provided evidence for the first time that glb-13 is associated with the resistance against oxidative stress-induced toxicity.

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“…In silico analysis of the genome of the free-living nematode Caenorhabditis elegans resulted in the identification of a family of 33 globin genes, labeled glb-1 to glb- 33, that are all transcribed. The encoded globins, GLB-1 to GLB-33, are localized in a specific subset of cells (2)(3)(4)(5). Characterization of some of these globins indicated that they are involved in a wide variety of cellular processes.…”

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confidence: 99%