Activity-dependent neuron–glial signaling by ATP and leukemia-inhibitory factor promotes hippocampal glial cell development

Cohen, Jeffrey K.; Fields, R. Douglas

doi:10.1017/s1740925x09000076

Cited by 26 publications

(18 citation statements)

References 54 publications

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“…However, LIF is a pleiotropic cytokine that also promotes glial cell differentiation [30, 31] and, under certain conditions, inhibits astrocyte proliferation [31]. These latter functions are consistent with our findings.…”

Section: Discussionsupporting

confidence: 92%

A nested case-control study of 277 prediagnostic serum cytokines and glioma

et al. 2017

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Recent research shows bidirectional communication between the normal brain and the peripheral immune system. Glioma is a primary brain tumor characterized by systemic immunosuppression. To better understand gliomagenesis, we evaluated associations between 277 prediagnostic serum cytokines and glioma. We used glioma (n = 487) and matched control (n = 487) specimens from the Janus Serum Bank Cohort in Oslo, Norway. Conditional logistic regression allowed us to identify those cytokines that were individually associated with glioma. Next, we used heat maps to compare case to control Pearson correlation matrices of 12 cytokines modeled in an in silico study of the interaction between the microenvironment and the tumor. We did the same for case-control correlation matrices of lasso-selected cytokines and all 277 cytokines in the data set. Cytokines related to glioma risk (P ≤ .05) more than 10 years before diagnosis are sIL10RB, VEGF, beta-Catenin and CCL22. LIF was associated with decreased glioma risk within five years before glioma diagnosis (odds ratio (OR) = 0.47, 95% confidence interval (CI) = 0.23, 0.94). After adjustment for cytokines above, the previously observed interaction between IL4 and sIL4RA persisted (> 20 years before diagnosis, OR = 1.72, 95% CI = 1.20, 2.47). In addition, during this period, case correlations among 12 cytokines were weaker than were those among controls. This pattern was also observed among 30 lasso- selected cytokines and all 277 cytokines. We identified four cytokines and one interaction term that were independently related to glioma risk. We have documented prediagnostic changes in serum cytokine levels that may reflect the presence of a preclinical tumor.

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Section: Discussionsupporting

confidence: 92%

A nested case-control study of 277 prediagnostic serum cytokines and glioma

et al. 2017

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“…In a subsequent study, LIF could be released from primary cultures of mouse hippocampal astrocytes by treatment with ATPγS and UTP. The pharmacological analysis suggested that P2Y 2 Rs were involved [170]. The study further provided evidence that LIF can be released through ATP from electrically active neurons via a P2Y 2 R-dependent mechanism.…”

Section: Leukemia-inhibitory Factormentioning

confidence: 65%

Extracellular ATP and other nucleotides—ubiquitous triggers of intercellular messenger release

Zimmermann

2015

Purinergic Signalling

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Extracellular nucleotides, and ATP in particular, are cellular signal substances involved in the control of numerous (patho)physiological mechanisms. They provoke nucleotide receptor-mediated mechanisms in select target cells. But nucleotides can considerably expand their range of action. They function as primary messengers in intercellular communication by stimulating the release of other extracellular messenger substances. These in turn activate additional cellular mechanisms through their own receptors. While this applies also to other extracellular messengers, its omnipresence in the vertebrate organism is an outstanding feature of nucleotide signaling. Intercellular messenger substances released by nucleotides include neurotransmitters, hormones, growth factors, a considerable variety of other proteins including enzymes, numerous cytokines, lipid mediators, nitric oxide, and reactive oxygen species. Moreover, nucleotides activate or co-activate growth factor receptors. In the case of hormone release, the initially paracrine or autocrine nucleotide-mediated signal spreads through to the entire organism. The examples highlighted in this commentary suggest that acting as ubiquitous triggers of intercellular messenger release is one of the major functional roles of extracellular nucleotides. While initiation of messenger release by nucleotides has been unraveled in many contexts, it may have been overlooked in others. It can be anticipated that additional nucleotide-driven messenger functions will be uncovered with relevance for both understanding physiology and development of therapy.

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“…In general, this is consistent with the transient appearance of other cytokines during nervous system development. We have shown recently that activity-dependent regulation of hippocampal astrocyte development is mediated in part by LIF signaling, stimulated by the activity-dependent release of ATP form neurons (Cohen and Fields,[2008]). Previous research showing that myelination is regulated by impulse activity in axons, in part through a mechanism involving LIF signaling (Ishibashi et al,[2006]), suggests the possibility that the developmental period when LIF influences OPC proliferation and myelination in optic nerve may be related to regulation of myelination by impulse activity in axons resulting from early visual experience (for review see Fields,[2008]).…”

Section: Discussionmentioning

confidence: 99%

Leukemia inhibitory factor regulates the timing of oligodendrocyte development and myelination in the postnatal optic nerve

Ishibashi

Lee

Baba

et al. 2009

J of Neuroscience Research

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Leukemia inhibitory factor (LIF) promotes the survival of oligodendrocytes both in vitro and in an animal model of multiple sclerosis, but the possible role of LIF signaling in myelination during normal development has not been investigated. We find that LIF -/-mice have a pronounced myelination defect in optic nerve at postnatal day 10. Myelin basic protein (MBP)-and proteolipid protein (PLP)-positive myelin was evident throughout the optic nerve in the wild-type mice, but staining was present only at the chiasmal region in LIF -/-mice of the same age. Further experiments suggest that the myelination defect was a consequence of a delay in maturation of oligodendrocyte precursor cell (OPC) population. The number of Olig2-positive cells was dramatically decreased in optic nerve of LIF -/-mice, and the distribution of Olig2-positive cells was restricted to the chiasmal region of the nerve in a steep gradient toward the retina. Gene expression profiling and cell culture experiments revealed that OPCs from P10 optic nerve of LIF -/-mice remained in a highly proliferative immature stage compared with littermate controls. Interestingly, by postnatal day 14, MBP immunostaining in the LIF -/-optic nerve was comparable to that of LIF +/+ mice. These results suggest that, during normal development of mouse optic nerve, there is a defined developmental time window when LIF is required for correct myelination. Myelination seems to recover by postnatal day 14, so LIF is not necessary for the completion of myelination during postnatal development. Keywords myelin; LIF; oligodendrocyte; astrocyte; optic nerve; transcription; OPC; differentiation Identifying the signals controlling oligodendrocyte differentiation and myelination is an important priority in current research in developmental neurobiology and in clinical research on demyelinating CNS disease. Cytokines have a well-appreciated role in inflammatory responses during nervous system injury and disease, but, in contrast to the case for growth factors and cell adhesion molecules, the possible role of cytokines in regulating oligodendrocyte development and myelination under normal physiological conditions is relatively unexplored. Based on recent research identifying LIF signaling between astrocytes and oligodendrocytes in regulating myelination in response to electrical activity in axons (Ishibashi et al.,[2006]), the present study was undertaken to investigate the possible role of *Correspondence to R. Douglas Fields, Nervous Systems Development and Plasticity Section, National Institutes of Health, NICHD Bldg. 35, Room 2A211, MSC 371335 Lincoln Drive, Bethesda, MD 20892. † The first two authors contributed equally to this work. LIF in regulating myelination of early postnatal optic nerve. Using genetic knockout mice, this study is the first analysis of LIF signaling on myelination during early postnatal development in the CNS. NIH Public AccessAlthough cytokines are generally associated with inflammatory disease, there is evidence that nervous system developmen...

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Activity-dependent neuron–glial signaling by ATP and leukemia-inhibitory factor promotes hippocampal glial cell development

Cited by 26 publications

References 54 publications

A nested case-control study of 277 prediagnostic serum cytokines and glioma

A nested case-control study of 277 prediagnostic serum cytokines and glioma

Extracellular ATP and other nucleotides—ubiquitous triggers of intercellular messenger release

Leukemia inhibitory factor regulates the timing of oligodendrocyte development and myelination in the postnatal optic nerve

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