Synaptic Hyaluronan Synthesis and CD44-Mediated Signaling Coordinate Neural Circuit Development

Wilson, Emily S; Litwa, Karen

doi:10.3390/cells10102574

Cited by 10 publications

(9 citation statements)

References 81 publications

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“…In the embryo, the HA forms a loosely packed network in the interstitium of the developing brain where it spread into the synaptic cleft of the immature synapses to attenuate synaptogenesis (Wilson et al 2020). During maturation of the synapses the hyaluronan, via its interaction with the CD44 receptor, initiates the formation of the postsynaptic density and stabilization of the synaptic contact (Wilson and Litwa 2021). During postnatal development of the cerebellum, HA showed very weak diffuse labeling at P7 and displayed in the perineuronal net at P14 (Carulli et al 2007).…”

Section: Temporal Distribution Of Extracellular Molecules In the Embr...mentioning

confidence: 99%

Developmental patterns of extracellular matrix molecules in the embryonic and postnatal mouse hindbrain

Wéber,

Dakos,

Mészár

et al. 2023

Preprint

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Normal brain development requires continuous communication between developing neurons and their environment filled by a complex network referred to as extracellular matrix (ECM). The ECM is divided into distinct families of molecules including hyaluronic acid, proteoglycans, and glycoproteins such as tenascins, and link proteins. In this study, we characterize the temporal and spatial distribution of the extracellular matrix molecules in the embryonic and postnatal mouse hindbrain by using antibodies and lectin histochemistry. In the embryo, hyaluronan and neurocan were found in high amounts until the time of birth whereas versican and tenascin-R were detected in lower intensities during the whole embryonic period. After birth, both hyaluronic acid and neurocan still produced intense staining in almost all areas of the hindbrain, while tenascin-R labeling showed a continuous increase during postnatal development. The reaction with WFA and aggrecan was revealed first at P4 with low staining intensities, while HAPLN was detected at P14. The perineuronal net appeared first around the facial and vestibular neurons at P4 with hyaluronic acid cytochemistry. One week after birth aggrecan, neurocan, tenascin-R, and WFA were also accumulated around the neurons located in several hindbrain nuclei, but HAPLN1 was detected on the second postnatal week. Our results provide further evidence that many extracellular macromolecules that will be incorporated into the perineuronal net are already expressed at embryonic and early postnatal stages of development to control differentiation, migration, and synaptogenesis of neurons. In late postnatal period, the experience-driven neuronal activity induces formation of perineuronal net to stabilize synaptic connections.

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Section: Temporal Distribution Of Extracellular Molecules In the Embr...mentioning

confidence: 99%

Developmental patterns of extracellular matrix molecules in the embryonic and postnatal mouse hindbrain

Wéber,

Dakos,

Mészár

et al. 2023

Preprint

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“…Despite their size, these factors can reside in narrow spaces. CNS synapses 20 nm wide harbor HA and its CD44 receptor (Roszkowska et al 2016;Wilson and Litwa, 2021), and the string-like FN protein likewise occurs in synaptic clefts (Thalhammer and Cingolani, 2014). HA chains thousands of nm long occupy large volumes when randomly coiled, but when attached to a surface can form 0.3 nm thin layers (Jacoboni et al 1999).…”

Section: Cell-cell Contact Types In the Chordamesodermmentioning

confidence: 99%

Cell contacts and pericellular matrix in the Xenopus gastrula chordamesoderm

Luu

Winklbauer

2023

Preprint

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Convergent extension of the chordamesoderm is the best-examined gastrulation movement in Xenopus. Here we study general features of cell-cell contacts in this tissue by combining depletion of adhesion factors C-cadherin, Syndecan-4, fibronectin, and hyaluronic acid, the analysis of respective contact width spectra and contact angles, and La3+ staining of the pericellular matrix. We provide evidence that like in other gastrula tissues, cell-cell adhesion in the chordamesoderm is largely mediated by different types of pericellular matrix. Specific glycocalyx structures previously identified in Xenopus gastrula tissues are absent in chordamesoderm but other contact types like 10-20 nm wide La3+ stained structures are present instead. Knockdown of any of the adhesion factors reduces the abundance of cell contacts but not the average relative adhesiveness of the remaining ones: a decrease of adhesiveness at low contact widths is compensated by an increase of contact widths and an increase of adhesiveness proportional to width. From the adhesiveness-width relationship, we derive a model of chordamesoderm cell adhesion that involves the interdigitation of distinct pericellular matrix units. Quantitative description of pericellular matrix deployment suggests that reduced contact abundance upon adhesion factor depletion is due to some contact types becoming non-adhesive and others being lost.

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“…1,2 HA is abundant in the extracellular matrix of cells, with the most distribution around skin cells, connective tissue, joint tissue, and vitreous body. 3,4 A distinct difference between the high-molecular-weight HA polymers (HMW-HAs, ∼2 × 10 3 kDa) and the low-molecularweight HAs (LMW-HAs, 4−120 kDa) and HA oligosaccharides (O-HAs, <4 kDa) is the unique biological properties exhibited by the latter two. 5,6 While LMW-HAs reportedly play an important role in the anti-inflammatory response, chronic wound healing, and HA cross-linker development, 7,8 O-HAs selectively kill tumor cells by breaking the HA−receptor interaction.…”

Section: Introductionmentioning

confidence: 99%

“…Hyaluronic acid (HA) is a nonsulfated linear glycosaminoglycan (GAG) with a negative charge and comprising a tandem repeating unit of the disaccharide β-1,4- d -glucuronic acid-β-1,3- d - N -acetylglucosamine-β-1,4. , HA is abundant in the extracellular matrix of cells, with the most distribution around skin cells, connective tissue, joint tissue, and vitreous body. , A distinct difference between the high-molecular-weight HA polymers (HMW-HAs, ∼2 × 10 3 kDa) and the low-molecular-weight HAs (LMW-HAs, 4–120 kDa) and HA oligosaccharides (O-HAs, <4 kDa) is the unique biological properties exhibited by the latter two. , While LMW-HAs reportedly play an important role in the anti-inflammatory response, chronic wound healing, and HA cross-linker development, , O-HAs selectively kill tumor cells by breaking the HA–receptor interaction. In addition, O-HAs are reported to improve the sensitivity of cancer cells to drugs and facilitate angiogenesis/osteoanagenesis, while their HMW counterparts are ineffective in this regard. , These unique physicochemical properties and bioactivities of HA fragments are chain length specific .…”

Section: Introductionmentioning

confidence: 99%

Enzymatic Production of Low-Molecular-Weight Hyaluronan and Its Oligosaccharides: A Review and Prospects

Pang

Wang²,

Huang

et al. 2022

J. Agric. Food Chem.

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Hyaluronic acid (HA) is a nonsulfated linear glycosaminoglycan with a negative charge. Different from the high-molecular-weight HAs, the low-molecular-weight HAs (LMW-HAs, 4–120 kDa) and hyaluronan oligosaccharides (O-HAs, <4 kDa) exhibit certain unique biological properties, owing to which these have a wide range of applications in the field of medicine. However, the chemical synthesis of high-purity LMW-HAs and O-HAs requires complex procedures, which renders this process difficult to achieve. The degradation of HA is achieved under the catalysis of hyaluronidases. In recent years, various hyaluronidase genes have been identified, and their enzymatic properties have been analyzed. In this context, the present review summarizes the hyaluronidases from different sources, which have been characterized. The review focuses on the crystal structure and the catalytic mechanism underlying the biological properties of hyaluronidases. In addition, the molecular weight distributions and the preparation approaches of the enzymatic products LMW-HAs and O-HAs are described. The general orientation of the research on hyaluronidases was speculated based on the existing literature. Accordingly, the efficient large-scale production of LMW-HAs and O-HAs using the green enzymatic approach was anticipated.

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Synaptic Hyaluronan Synthesis and CD44-Mediated Signaling Coordinate Neural Circuit Development

Cited by 10 publications

References 81 publications

Developmental patterns of extracellular matrix molecules in the embryonic and postnatal mouse hindbrain

Developmental patterns of extracellular matrix molecules in the embryonic and postnatal mouse hindbrain

Cell contacts and pericellular matrix in the Xenopus gastrula chordamesoderm

Enzymatic Production of Low-Molecular-Weight Hyaluronan and Its Oligosaccharides: A Review and Prospects

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