Macrophage migration inhibitory factor acts as a neurotrophin in the developing inner ear

Bank, Lisa M.; Bianchi, Lynne M.; Ebisu, Fumi; Lerman-Sinkoff, Dov B.; Smiley, Elizabeth; Shen, Yu Chi; Ramamurthy, Poornapriya; Thompson, Deborah; Roth, Therese M.; Beck, Christine R.; Flynn, Matthew; Teller, Ryan S.; Feng, Luming; Llewellyn, G. Nicholas; Holmes, Brandon B.; Sharples, Cyrrene; Coutinho-Budd, Jaeda; Linn, Stephanie A.; Chervenak, Andrew P.; Dolan, David F.; Benson, Jennifer; Kanicki, Ariane; Martin, Catherine A.; Altschuler, Richard A.; Koch, Alicia E.; Jewett, Ethan M.; Germiller, John A.; Barald, Kate F.

doi:10.1242/dev.066647

Cited by 37 publications

(61 citation statements)

References 47 publications

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“…Several highly conserved families of axon guidance molecules and their receptors are present during this pathfinding phase, including Ephs/ephrins (Siddiqui and Cramer, 2005), Semaphorins (Chilton and Guthrie, 2003), and Slits/Robos (Holmes and Niswander, 2001; Battisti and Fekete, 2008; Wang et al, 2013). Molecules that can influence otic axon outgrowth include neurotrophins (Tessarollo et al, 2004; Fritzsch et al, 2005), inflammatory cytokines (Bianchi et al, 2005; Banks et al, 2012), ephrins (Bianchi and Gray, 2002; Brors et al, 2003; Zhou et al, 2011; Coate et al, 2012), Semaphorins (Gu et al, 2003; Fantetti et al, 2011) and members of the BMP, Shh, and FGF morphogen families (Hossain et al, 1996; Hossain and Morest, 2000; Hossain et al, 2008; Fantetti and Fekete, 2012). Peripheral otic axon pathfinding has been the subject of recent reviews (Pauley et al, 2005; Webber and Raz, 2006; Fekete and Campero, 2007; Appler and Goodrich, 2011; Coate and Kelly, 2013).…”

Section: Introductionmentioning

confidence: 99%

A subset of chicken statoacoustic ganglion neurites are repelled by Slit1 and Slit2

Battisti¹,

Fantetti²,

Moyers³

et al. 2014

Hearing Research

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Mechanosensory hair cells in the chicken inner ear are innervated by bipolar afferent neurons of the statoacoustic ganglion (SAG). During development, individual SAG neurons project their peripheral process to only one of eight distinct sensory organs. These neuronal subtypes may respond differently to guidance cues as they explore the periphery in search of their target. Previous gene expression data suggested that Slit repellants might channel SAG neurites into the sensory primordia, based on the presence of robo transcripts in the neurons and the confinement of slit transcripts to the flanks of the prosensory domains. This led to the prediction that excess Slit proteins would impede the outgrowth of SAG neurites. As predicted, axonal projections to the primordium of the anterior crista were reduced 2-3 days after electroporation of either slit1 or slit2 expression plasmids into the anterior pole of the otocyst on embryonic day 3 (E3). The posterior crista afferents, which normally grow through and adjacent to slit expression domains as they are navigating towards the posterior pole of the otocyst, did not show Slit responsiveness when similarly challenged by ectopic delivery of slit to their targets. The sensitivity to ectopic Slits shown by the anterior crista afferents was more the exception than the rule: responsiveness to Slits was not observed when the entire E4 SAG was challenged with Slits for 40 hours in vitro. The corona of neurites emanating from SAG explants was unaffected by the presence of purified human Slit1 and Slit2 in the culture medium. Reduced axon outgrowth from E8 olfactory bulbs cultured under similar conditions for 24 hours confirmed bioactivity of purified human Slits on chicken neurons. In summary, differential sensitivity to Slit repellents may influence the directional outgrowth of otic axons toward either the anterior or posterior otocyst.

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Section: Introductionmentioning

confidence: 99%

A subset of chicken statoacoustic ganglion neurites are repelled by Slit1 and Slit2

Battisti¹,

Fantetti²,

Moyers³

et al. 2014

Hearing Research

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“…Previous studies highlighted that a CD40‐ and CD45‐deficiency may positively influence neuronal survival (Bak, Kim, Kim, & Choi, ; Carson, Thrash, & Walter, ; Giunta, Figueroa, Town, & Tan, ; Keilhoff, Schweizer, John, Langnaese, & Ebmeyer, ; Koshimizu et al, ; Michael, Gbolahan, Ansa, Abdulbasitand, & Azeez, ; Town, Tan, & Mullan, ). Encoded protein of CD74 plays an important role in the induction of selective pro‐inflammatory molecules (Bank et al, ; Beswick & Reyes, ). In addition, a low level of the CD14 gene, which is known to act as a co‐receptor for the endotoxin lipopolysaccharide (LPS), has been found to ameliorate inflammatory responses, thus suggesting a role in conserving life‐maintaining signals (Bate & Williams, ; Bate, Veerhuis, Eikelenboom, & Williams, ; Butovsky et al, ).…”

Section: Discussionmentioning

confidence: 99%

The trophic effect of nerve growth factor in primary cultures of rat hippocampal neurons is associated to an anti‐inflammatory and immunosuppressive transcriptional program

Maino

Spampinato

Severini

et al. 2018

Journal Cellular Physiology

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Nerve growth factor, the prototype of a family of neurotrophins, elicits differentiation and survival of peripheral and central neuronal cells. Although its neural mechanisms have been studied extensively, relatively little is known about the transcriptional regulation governing its effects. We have previously observed that in primary cultures of rat hippocampal neurons treatment with nerve growth factor for 72 hr increases neurite outgrowth and cell survival. To obtain a comprehensive view of the underlying transcriptional program, we performed whole-genome expression analysis by microarray technology. We identified 541 differentially expressed genes and characterized dysregulated pathways related to innate immunity: the complement system and neuro-inflammatory signaling. The exploitation of such genes and pathways may help interfering with the intracellular mechanisms involved in neuronal survival and guide novel therapeutic strategies for neurodegenerative diseases.

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“…Another reason an inner ear phenotype has not been characterized is that significant numbers of mutants die, either during embryonic stages (all Zic2 Ku/Ku , ~24% of Zic3 Bn ) or shortly after birth (50% of Zic1 −/− , all Zic2 kd/kd , some Zic5 −/− ) (Aruga et al, 1998; Klootwijk et al, 2000; Nagai et al, 2000; Elms et al, 2003; Inoue et al, 2004), making it impossible to detect signs of inner ear defects that affect the mature function of this sensory organ, such as changes in gait or posture, abnormal behaviors such as circling, and changes in the acoustic startle response or auditory brainstem responses (ABR) (Saul et al, 2008). Studies using these mice, including recording of ABRs in any animals, including heterozygotes, that live to postnatal stages, as we have done for other mouse mutations (Bank et al, 2012) could provide insights into how individual Zic genes function during inner ear development. Further, the generation of compound Zic mutants would be useful to address questions of redundancy among the Zic genes during inner ear development, as we have shown that the Zic genes are expressed in overlapping regions of the periotic mesenchyme in both chick and mouse.…”

Section: Discussionmentioning

confidence: 99%

Spatiotemporal expression of zic genes during vertebrate inner ear development

Chervenak

Hakim

Barald

2013

Developmental Dynamics

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Background Inner ear development involves signaling from surrounding tissues, including the adjacent hindbrain, periotic mesenchyme and notochord. These signals include SHH, FGFs, BMPs and WNTs from the hindbrain and SHH from the notochord. Zic genes, which are expressed in the dorsal neural tube and act during neural development, have been implicated as effectors of these pathways. This report examines whether Zic genes’ involvement in inner ear development is a tenable hypothesis based on their expression patterns. Results In the developing inner ear of both the chick and mouse, all of the Zic genes were expressed in the dorsal neural tube and variably in the periotic mesenchyme, but expression of the Zic genes in the otic epithelium was not found. The onset of expression differed among the Zic genes; within any given region surrounding the otic epithelium, multiple Zic genes were expressed in the same place at the same time. Conclusions Zic gene expression in the region of the developing inner ear is similar between mouse and chick. Zic expression domains overlap with sites of WNT and SHH signaling during otocyst patterning, suggesting a role for Zic genes in modulating signaling from these pathways.

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Macrophage migration inhibitory factor acts as a neurotrophin in the developing inner ear

Cited by 37 publications

References 47 publications

A subset of chicken statoacoustic ganglion neurites are repelled by Slit1 and Slit2

A subset of chicken statoacoustic ganglion neurites are repelled by Slit1 and Slit2

The trophic effect of nerve growth factor in primary cultures of rat hippocampal neurons is associated to an anti‐inflammatory and immunosuppressive transcriptional program

Spatiotemporal expression of zic genes during vertebrate inner ear development

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