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Neurocan Developmental Expression and Function During Early Avian Embryogenesis

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Neurocan Developmental Expression and Function During Early Avian Embryogenesis Research Journal of Developmental Biology ISSN 2055-4796 | Volume 1 | Article 3 Original Open Access Neurocan developmental expression and function during early avian embryogenesis Katerina Georgadaki and Nikolas Zagris* *Correspondence: [email protected] CrossMark ← Click for updates Division of Genetics and Cell and Developmental Biology, Department of Biology, University of Patras, Patras, Greece. Abstract Background: Neurocan is the most abundant lectican considered to be expressed exclusively in the central nervous system. Neurocan interacts with other matrix components, with cell adhesion molecules, growth factors, enzymes and cell surface receptors. The interaction repertoire and evidence from cellular studies indicated an active role in signal transduction and major cellular programs. Relatively little is known about the neurocan tissue-specific distribution and function during embryonic development. This study examined the time of appearance and subsequent spatio-temporal expression pattern of neurocan and its functional activities during the earliest stages of development in the chick embryo. Methods: To detect the first expression and spatio-temporal distribution of neurocan in the early embryo, strand- specific reverse transcription-polymerase chain reaction (RT-PCR), immunoprecipitation and immunofluorescence were performed. An anti-neurocan blocking antibody transient pulse was applied to embryos at the onset of the neurula stage to perturb neurocan activities in the background of the current cellular signaling state of the developing embryo. Results: Neurocan was first detected in the inchoate neural plate and the extracellular matrix in embryos at the definitive streak stage (late gastrula). During early organogenesis, neurocan fluorescence was very intense in the neural tube, notochord, neural crest cells, pharyngeal arches, foregut lower wall, presumptive pronephric tubules, blood islands, dorsal mesocardium, intense in myocardium and distinct in endocardium, very intense in the presumptive cornea and intense in retina and lens, intense in somite and nephrotome. Antibody perturbation of neurocan function resulted in three predominant defects: (1) abnormal expansion of neuroepithelium in the surface ectoderm flanking the neural tube; (2) neural crest cells formed epithelial pockets located on the ectoderm apical surface; and (3) surface ectoderm cells (presumptive epidermis) acquired mesenchymal cell properties, invaded into the subectodermal space and interacted with neuroectoderm. Conclusions: Neurocan was first expressed in the inchoate neural plate at the late gastrula stage. Neurocan expression was very intense in the developing central nervous system as well as in many non-neural tissues. Neurocan seems to modulate signalling in the neural-non-neural tissue specification and the adhesive and signalling activities of epithelial-mesenchymal cells and neural crest cell motility in the early embryo. Keywords: Cell adhesion, growth factors, neural-non-neural specification, neural crest, tenascin, hyaluronan, morphogenesis Background Subsequent work reported that neurocan was also detected Neurocan is a member of the lecticans, a structurally similar in the endocardium of 4-day-old chick embryos [7], in the chondroitin sulfate proteoglycan family, which includes agg- embryonic heart and vasculature in quail embryos at the HH recan, versican and brevican [1-3]. Neurocan has been identified (Hamburger and Hamilton) stage 11 (13 somites) [8], and in by molecular cloning in the brain and was considered to mouse lymphoid cells [9] and mammary tumors [10]. Both the be a brain–specific chondroitin sulfate proteoglycan [4-6]. carbohydrate side chains and the polypeptide backbone of © 2014 Zagris et al; licensee Herbert Publications Ltd. This is an Open Access article distributed under the terms of Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0). This permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Georgadaki et al. Research Journal of Developmental Biology 2014, http://www.hoajonline.com/journals/pdf/2055-4796-1-3.pdf doi: 10.7243/2055-4796-1-3 neurocan interact with the cell adhesion molecules Ng-CAM/ pattern in the chick embryo from stage X (homologous to L1 (neuron glia- cell adhesion molecule), axonin, and N-CAM the morula in amphibia), when the embryo is histologically (neural cell adhesion molecule) [11,12]. Through the interaction simple, to the early stages of organogenesis (stage HH17, 29 with cell surface GalNAcPTase (N-acetylgalactosaminyl somites). We then used blocking antibodies directed against phosphotransferase), neurocan regulates N-cadherin and β1 neurocan to perturb neurocan activities when neurocan is integrin function co-ordinately [13,14]. Neurocan interacts first detected in embryos at the onset of the neurula stage. with other extracellular matrix molecules, such as heparin, tenascins [3,15,16] and with growth factors and cytokines Methods FGF-2, HB-GAM (heparin-binding growth-associated molecule), Animal studies and amphoterin [3,17]. The neurocan N-terminal domain Fertilized chicken eggs (supplied by the Epirus Poultry Co., interacts with hyaluronan through the link proteins and the Ioannina, Greece) were incubated at 37.5°C under high hu- C-type lectin neurocan C-terminal domain interacts with midity. The chick embryo studies and all procedures were sulfatides, and sulfated cell surface glycolipids. The wide preformed in accordance with the guidelines of the National range of interactions enable neurocan to participate in a Ethical Commission for Animal Research (Ministry of Education, network consisting of tenascin-hyaluronan and cell surface Greece) and the Institutional Animal Care and Use Committee receptors [2,3,18]. (University of Patras). Many studies have emphasized that the interaction reper- toire of neurocan through distinct domains and the evidence RT-PCR from cellular studies suggest that neurocan has evolved as The presence of neurocan mRNA at various stages of the early an modular extracellular regulator of cell-cell and cell-matrix chick embryo was assessed by PCR amplification from mRNA interactions that guide the cellular rearrangements essential derived cDNA. Total RNA was prepared (RNeasy Mini Kit proto- to the formation and function of the nervous system [1-3,13]. col, Qiagen) from chick embryos at stages XI (morula), XIII (late Neurocan knockout mice [19] showed only some behav- blastula), HH2 (initial streak/early gastrula), HH3 (intermediate ioural abnormalities without visible abnormal anatomical streak), HH4-5 (definitive streak to head process) and HH6 features. There are a number of developmentally significant (head fold). Attention was paid to the exact developmental genes, such as tenascin, that on targeted disruption show stage of the embryos according to Hamburger and Hamilton mild mutations or no observably aberrant phenotypes (HH symbol) [28]. PCR primers were 5’-ACA CCA GCA ACA [20-22]. The apparent dispensability of tenascin, neurocan GCA GCC AGC-3’ (sense, position 2955) and 5’-GCA GAT GTA or of other genes during development was interpreted in a GGG CAG GTT GTA G-3’ (antisense, position 3561) specific for number of interesting ways [19,21,23,24]. As has been well a fragment of 607-bp (from 2955 to 3561) of quail neurocan stated [21,23-26], cautious interpretation should be exercised mRNA. For β-actin, a fragment of 187-bp was amplified with when examining the effects of gene deletions in view of the the following primers: sense 5’-CGG TAT TGT CAC CAA CTG large number of variables that can operate during embryo- G-3’ and antisense 5’-TGG CTA CAT ACA TGG CTG G-3’ were genesis, the existence of compensatory mechanisms during used in a parallel reaction as the neurocan primers. The quail regulative development, and the pleiotropy and variable neurocan [8] and chick β-actin [29,30] primers were the same penetrance resulting from mutation or deletion of a single as those published previously. Single stranded cDNA was gene. Zimmermann and Dours-Zimmermann [25] remarked synthesized employing as template 2μg of total RNA from that although the highest matrix protein expression in the embryos according to the manufacturer OneStep RT-PCR Kit central nervous system during early neural development has protocol (Qiagen); the RNA was omitted from the reaction in been attributed to tenascin and neurocan, their in vivo func- the negative control samples. Amplification conditions were tions in the juvenile-type of matrix are still largely unknown. started at 95°C for 15 min, and then subjected to 35 and 31 Most studies with neurocan have been conducted in rat cycles for neurocan and β-actin, respectively, of [denaturation and mouse, mainly in the late embryonic stages, in postnatal 94°C for 30 sec, annealing 65°C (55°C for β-actin) for 1 min, development and the adult and in cell cultures. The neurocan elongation 72°C for 1 min], and one cycle of extension 72°C function is elusive [4-8,25]. In vitro studies have shown that for 10 min. PCR amplification products (5μl/lane and 3μl/lane neurocan is able to modulate cell-binding, axon guidance for neurocan and β-actin, respectively) were separated on a and synapse formation during the development of the nerv- 5% polyacrylamide gel and stained with ethidium bromide. ous system via adhesion molecules [3,11,13,27]. Despite the A 100-10,000bp ladder was used as a marker (GeneRuler DNA great amount of information available
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