A homologous form of human interleukin 16 is implicated in microglia recruitment following nervous system injury in leech <i>Hirudo medicinalis</i>

Croq, Françoise; Vizioli, Jacopo; Tuzova, Marina; Tahtouh, Muriel; Sautière, Pierre-Éric; Camp, Christelle Van; Salzet, Michel; Cruikshank, William W.; Pestel, Joël; Lefebvre, Christophe

doi:10.1002/glia.21036

Cited by 36 publications

(46 citation statements)

References 57 publications

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“…The optimal effect was observed by using 8 μl of r Hm C1q supernatant while a higher amount (15 μl) caused a decreased migration of the microglia. This effect is a characteristic of cytokines having chemotactic activity and has been described for other chemoattractant factors of leech CNS conditioned medium [22]. Of interest, similar dose-dependent results were obtained by using purified r Hm C1q (data not shown).…”

Section: Resultssupporting

confidence: 82%

“…Nerve cells, neurons and microglial cells were mechanically resuspended by gentle scraping (total nerve cells). After a filtration through 7 μm nylon mesh as described [17,22], the enriched microglial cell population was then collected and centrifuged at 1,000 g for 10 minutes at RT. The cell pellet was resuspended in L-15 medium (100 μl per nerve cord) for migration assays.…”

Section: Methodsmentioning

confidence: 99%

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Interaction of HmC1q with leech microglial cells: involvement of C1qBP-related molecule in the induction of cell chemotaxis

Tahtouh

Garçon-Bocquet

Croq

et al. 2012

J Neuroinflammation

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BackgroundIn invertebrates, the medicinal leech is considered to be an interesting and appropriate model to study neuroimmune mechanisms. Indeed, this non-vertebrate animal can restore normal function of its central nervous system (CNS) after injury. Microglia accumulation at the damage site has been shown to be required for axon sprouting and for efficient regeneration. We characterized HmC1q as a novel chemotactic factor for leech microglial cell recruitment. In mammals, a C1q-binding protein (C1qBP alias gC1qR), which interacts with the globular head of C1q, has been reported to participate in C1q-mediated chemotaxis of blood immune cells. In this study, we evaluated the chemotactic activities of a recombinant form of HmC1q and its interaction with a newly characterized leech C1qBP that acts as its potential ligand.MethodsRecombinant HmC1q (rHmC1q) was produced in the yeast Pichia pastoris. Chemotaxis assays were performed to investigate rHmC1q-dependent microglia migration. The involvement of a C1qBP-related molecule in this chemotaxis mechanism was assessed by flow cytometry and with affinity purification experiments. The cellular localization of C1qBP mRNA and protein in leech was investigated using immunohistochemistry and in situ hybridization techniques.ResultsrHmC1q-stimulated microglia migrate in a dose-dependent manner. This rHmC1q-induced chemotaxis was reduced when cells were preincubated with either anti-HmC1q or anti-human C1qBP antibodies. A C1qBP-related molecule was characterized in leech microglia.ConclusionsA previous study showed that recruitment of microglia is observed after HmC1q release at the cut end of axons. Here, we demonstrate that rHmC1q-dependent chemotaxis might be driven via a HmC1q-binding protein located on the microglial cell surface. Taken together, these results highlight the importance of the interaction between C1q and C1qBP in microglial activation leading to nerve repair in the medicinal leech.

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Section: Resultssupporting

confidence: 82%

Section: Methodsmentioning

confidence: 99%

Interaction of HmC1q with leech microglial cells: involvement of C1qBP-related molecule in the induction of cell chemotaxis

Tahtouh

Garçon-Bocquet

Croq

et al. 2012

J Neuroinflammation

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“…A high dose inhibition of chemotaxis is characteristic of chemokines [10] and is consistent with the inhibitory effect recently described for other chemoattractant factors in the leech central nervous system. [36,37] The results also showed that the different concentrations of IL-8 did not influence the types of cells migrating into the MG. Ultrastructural analysis using scanning (SEM, Figure 2E-G) and transmission (TEM, Figure 2H-J) electron microscopy showed that the MG pellets were infiltrated by cells characterized by a cytoplasm containing numerous small highly electron-dense granules ( Figure 2F and 2I) and by cells showing an electron-dense cytoplasm containing a few large granules ( Figure 2G and 2L). These two types of cells can be found both strictly associated with each other or isolated ( Figure 2E and 2H).…”

Section: Light and Electron Microscopic Examination Of Mg Pellets Supsupporting

confidence: 56%

Cytokine Loaded Biopolymers as a Novel Strategy to Study Stem Cells during Wound‐Healing Processes

Grimaldi

Banfi

Vizioli

et al. 2011

Macromolecular Bioscience

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The biopolymer matrigel loaded with cytokine can be used for the recruitment in vivo of specific cell populations and as a vector for the preparation of cell cultures. Data demonstrate that the injection of the matrigel biopolymer supplemented with interleukin-8 (IL-8) in the leech Hirudo medicinalis can be used to purify cell populations showing the same morphofunctional and molecular mechanisms of specific populations of vertebrate hematopoietic precursor cells involved in tissue repair. These cells spontaneously differentiated into myofibroblasts. This approach highlights how the innovative use of a cytokine-loaded biopolymer for an in vivo cell sorting method, applied to a simple invertebrate model, can be a tool for studying myofibroblast cell biology and its regulation, step by step.

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“…It is a potent chemoattractant and also has a regulatory function in the induction of cytokines including IL-6, TNF-α, and IL-1β [26] . IL-16 is produced by microglia in response to CNS injury and, in turn, activates microglial migration to the site of injury and repair [27] . Following ischaemic infarction, it reacts with CD4+ receptors and activates T cell migration, through the up-regulation of receptors such as T cell CD25 and MHC class 2 molecules.…”

Section: Discussionmentioning

confidence: 99%

Cord Blood IL-16 Is Associated with 3-Year Neurodevelopmental Outcomes in Perinatal Asphyxia and Hypoxic-Ischaemic Encephalopathy

Ahearne¹,

Chang

Walsh

et al. 2017

Dev Neurosci

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Activation of the inflammatory pathway is increasingly recognized as an important mechanism of injury following neonatal asphyxia and encephalopathy. This process may contribute to the poor prognosis seen in some cases, despite therapeutic hypothermia. Our group has previously identified raised interleukin (IL)-6 and IL-16, measured in umbilical cord blood at birth, to be predictive of grade of hypoxic-ischaemic encephalopathy (HIE). Our aim in this study was to examine the ability of these cytokines to predict the 3-year neurodevelopmental outcome in the same cohort. As part of a prospective, longitudinal cohort study set in a single tertiary maternity unit, term infants with biochemical and clinical evidence of perinatal asphyxia were recruited at birth. Umbilical cord blood was collected and analyzed for IL-6 and IL-16 using a Luminex assay. The neurodevelopmental outcome of these infants was assessed at 3 years using the Bayley Scales of Infant and Toddler Development (Edition 3). Early cord blood measurement of IL-6 and IL-16 and long-term outcome were available in 33/69 infants. Median (IQR) IL-16 differentiated infants with a severely abnormal outcome (n = 6) compared to all others (n = 27), (646 [466-1,085] vs. 383.5 [284-494] pg/mL; p = 0.012). IL-16 levels were able to predict a severe outcome with an area under the receiver-operating characteristic (ROC) curve of 0.827 (95% CI 0.628-1.000; p = 0.014). Levels ≥514 pg/mL predicted a severe outcome with a sensitivity of 83% and a specificity of 81%. IL-16 also outperformed other routine biochemical markers available at birth for the prediction of severe outcome. APGAR scores at 1 and 10 min were also predictive of a severe outcome (p = 0.022 and p = 0.036, respectively). A combination of IL-16 with these clinical markers did not improve predictive value, but IL-16 combined with electroencephalogram grading increased the area under the ROC curve. IL-6 did not show any association with 3-year outcome. This is the first report studying the association of IL-16 measured at birth with long-term outcome in a cohort of neonates with perinatal asphyxia. IL-16 may be an early biomarker of severe injury and aid in the long-term prognostication in infants with HIE.

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A homologous form of human interleukin 16 is implicated in microglia recruitment following nervous system injury in leech Hirudo medicinalis

Cited by 36 publications

References 57 publications

Interaction of HmC1q with leech microglial cells: involvement of C1qBP-related molecule in the induction of cell chemotaxis

Interaction of HmC1q with leech microglial cells: involvement of C1qBP-related molecule in the induction of cell chemotaxis

Cytokine Loaded Biopolymers as a Novel Strategy to Study Stem Cells during Wound‐Healing Processes

Cord Blood IL-16 Is Associated with 3-Year Neurodevelopmental Outcomes in Perinatal Asphyxia and Hypoxic-Ischaemic Encephalopathy

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