All the samples were immediately fixed in a solution of 2% glutaraldehyde and 1.2% NaCl in 0.1M sodium cacodylate at 4C for at least 4h and then processed for ultrastructural analyses. https://doi.org/10.1126/science.1248228, Han J, Lee JD, Bibbs L, Ulevitch RJ (1994) A MAP kinase targeted by endotoxin and hyperosmolarity in mammalian cells. Indeed, the CE lines the perivisceral coelom, the echinoderm-exclusive water vascular system (e.g., the radial water canals, the inner side of ampullae, and tube feet), and the peri-haemal system (Hyman 1955), all these compartments displaying a multiplicity of functions. Interestingly, in our samples, a sub-layer of peculiar flagellated and vesicular cells, never described before, has been detected in the inner borders of the circular muscle layer. A similar phenomenon of apocrine secretion was observed also during arm tip regeneration in other echinoderm species, including crinoids (CandiaCarnevali et al. https://www.thefreedictionary.com/Celomic+epithelium. Triple white arrowheads indicate the site of EMT. Russ J Mar Biol 33:411416. Vesicular cells are characterized by electron-lucent vesicles and flagella (arrow), and are in direct contact with the longitudinal muscle layer (lm). Cell and Tissue Biology 4:280288. 2a, b, d), through which the apical portions of these cells (including cytoplasm and cell membrane) were released into the coelomic lumen. lom s-lm plural coeloms also coelomata si-l-m-t : the usually epithelium-lined space between the body wall and the digestive tract of metazoans above the lower worms coelomate s-l-mt adjective or noun coelomic si-l-mik -l- adjective Example Sentences J Pathol 214:149160. Google Scholar, Ariza L, Carmona R, Caete A et al (2016) Coelomic epithelium-derived cells in visceral morphogenesis. Coelomic cavities of vertebrates are lined by a mesothelium which develops from the lateral plate mesoderm. Interestingly, adjacent vesicular cells often formed together intercellular niches bordered by microvillar projections and hosting flagella (Fig. dTEM micrograph of the distal CE showing peritoneocytes (green); longitudinal muscle layer (blue); vesicular cell layer (red). Mar Genomics 37:9296. eSemithin longitudinal section of perivisceral CE showing an evident apocrine secretion. Cell Tiss Biol 3:477. https://doi.org/10.1134/S1990519X09050113, Gros J, Tabin CJ (2014) Vertebrate limb bud formation is initiated by localized epithelial to mesenchymal transition. https://doi.org/10.1089/wound.2013.0473, Pinsino A, Thorndyke MC, Matranga V (2007) Coelomocytes and post-traumatic response in the common sea star Asterias rubens. 2005; Pinsino et al. Evol Dev 7:351358. 1 ). The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. In the present work, we never observed a direct release of free wandering coelomocytes from the apical part of the CE toward the coelomic lumen, either in homeostatic non-regenerating or in regenerating conditions. https://doi.org/10.1016/j.jprot.2010.10.009, Ferrario C, Ben Khadra Y, Czarkwiani A et al (2018) Fundamental aspects of arm repair phase in two echinoderm models. The underlying muscle layers underwent an intense reorganization and remodeling. https://doi.org/10.1002/path.2287, Butt RH, Coorssen JR (2006) Pre-extraction sample handling by automated frozen disruption significantly improves subsequent proteomic analyses. PubMed 2009; CandiaCarnevali and Burighel 2010; Hernroth et al. 2018). Overall, the present study demonstrated that starfish CE is not simply a container of the coelomic fluid, defining and delimiting the coelomic environment from the surrounding body tissues. Which of the following microscopic findings in an ovary are indicators of a pathologic condition? FOIA Carnevali MD (eds) Body cavities: function and phylogeny. This work was performed in the framework of the EU COST Action MARISTEM (CA16203). CAS That article is substantially longer and more informative than this stub. Overall, proteins specific to hematopoiesis were not found, this result being explainable by the presence in the total protein extract analyzed by LCMS/MS of highly abundant proteins, which hampers the identification of lower abundant proteins. Fibers undergo rearrangement phenomena indicated by evident modifications of their contractile apparatus (arrows). The Software Tool for Rapid Annotation of Proteins (STRAP) was used to fully annotate the identified proteins using the UniProt and EBI QuickGO (http://www.ebi.ac.uk/QuickGO/) gene ontology information (Bhatia et al. fTEM micrograph of the new coelomic cavity tip, showing details of peritoneocytes. The total protein concentration of each replicate was determined using the QuantiPro BCA Assay Kit according with the manufacturers protocol. 2010) observed the production of roundish bodies of about 2-m diameter (described as anuclear cells), similar to those described in the present work, which could also be apocrine secretion products or the result of the in vitro conditions. 5a, Online Resource 3), whereas from SWATH analysis (Fig. The scavenger receptor, known to act as a phagocytic receptor, was also detected in sea urchin coelomocytes (Smith et al. Scale bar = 1m. 2000). 2f), whereas in the rest of the arm it was rarely detectable. https://doi.org/10.3390/ijms21010225, Gorshkov AN, Blinova MI, Pinaev GP (2009) Ultrastructure of coelomic epithelium and coelomocytes of the starfish Asterias rubens L. in norm and after wounding. 3a, b). Golgi vesicles are directly originated from the Golgi, where proteins received from the ER are further processed and sorted for transport to lysosomes, plasma membrane, or secretion. Samples were resolved by liquid chromatography (nanoLC Ultra 2D, Eksigent) on a MicroLC column ChromXP (300m ID 15cm length, 3m particles, 120 pore size, Eksigent) at 5 L/min with a multistep gradient: 02min linear gradient from 2 to 5%, 245min linear gradient from 5 to 30% and, 4546min to 35% of ACN in 0.1% formic acid and 5% dimethyl sulfoxide, and analyzed on a TripleTOF 5600 System (ABSciex). Overall, this strongly indicates the existence of a phylum-shared mechanism for the production of regeneration-competent cells relying on de-differentiation, proliferation, and subsequent EMT of coelothelial cells (Ben Khadra et al. Russ J Dev Biol 24:7281, Dolmatov IY, Ginanova TT (2001) Muscle regeneration in holothurians. jTEM micrograph of radial water canal (rwc) CE showing the presence of SLSs (asterisks) in peritoneocytes (p). Most identified proteins are cytoplasmic (26%) or cytoskeletal (19%) (Fig. 2021) and peritoneocytes. Please enable it to take advantage of the complete set of features! Andrade C, Oliveira B, Guatelli S et al (2021) Characterization of coelomic fluid cell types in the starfish Marthasterias glacialis using a flow cytometry/imaging combined approach. regenerating sample. These membrane receptors, important for innate immunity, are expressed in macrophages and recognize lipopolysaccharide (LPS), a ubiquitous pathogen membrane molecule (Yang et al. 2014), and has a key regulatory function in the inflammatory response (Bradley 2008). J Proteomics 74:127136. 2010; Garca-Arrars et al. The remaining proteins were involved in localization (5%), interaction with cells and organisms (4%), response to stimulus (2%), developmental process (2%), and immune system (<1%), whereas 9% of the proteins had no identified biological processes. 2011). https://doi.org/10.1007/s004410050883, Candia Carnevali MD, Bonasoro F, Lucca E, Thorndyke MC (1995a) Pattern of cell proliferation in the early stages of arm regeneration in the feather star Antedon mediterranea. (Anatomy) a thin translucent serous sac that lines the walls of the abdominal cavity and covers most of the viscera. [The characteristic of the coelomic fluid and coelomic epithelium cell populations of starfish Asterias rubens L., capable to attach and spread on various substrates]. Check out our new pathology themed Wordle. 2014; Ben Khadra et al. J Exp Zool 267:299317. cSemithin longitudinal section of proximal CE showing peritoneocyte layer (p); longitudinal (lm); and circular (cm) muscle layers separated by connective tissue (ct); dermis (d) infiltrated by muscle bundles (asterisk). 2018). Mar Drugs. The coelomic epithelium (in red) gives rise to mesenchymal cells diffusely throughout the body wall, coelomic septa and splanchnopleural mesoderm, but this process is more active in areas where endodermal (e.g., lungs, liver) and mesodermal organs (e.g., adrenals, gonads) are developing. 2021) showed that CE cells at the regenerating arm tip undergo partial dedifferentiation and subsequent epithelial-mesenchymal transition (EMT) to originate sclerocyte precursors. Mar Genomics 24:245248. To address these questions, we carried out an integrated analysis of this complex tissue by combining detailed microscopic and ultrastructural analyses with modern proteomics methods. allowing a better definition of the . 2012) and a set of 60 windows (see Online Resource 1) of variable width (containing a m/z of 1 for the window overlap) was constructed covering the precursor mass range of m/z 3501250. This process is the umbrella for the cell mobility protein cluster that includes several myosins and activating GTPases. Asterias rubens; Coelomic epithelium; Coelomocytes; Echinoderms; Progenitor cells; Proteome. dSemithin longitudinal section of CE at the level of the closure of the wound. M. glacialis coelomocytes have been recently characterized by means of different cytometry/microscopy (Andrade et al. According to Righettis protocol (Fasoli et al. 2011; Ben Khadra et al. The homogenate was ultra-centrifuged at 36000g for 10min at 4C using the Optima TLX Ultracentrifuge (4.N7/12) with the TLS-55 rotor (Beckman-Coulter) to separate the insoluble debris. Ballarin L, Karahan A, Salvetti A, Rossi L, Manni L, Rinkevich B, Rosner A, Voskoboynik A, Rosental B, Canesi L, Anselmi C, Pinsino A, Tohumcu BE, Jemec Kokalj A, Dolar A, Novak S, Sugni M, Corsi I, Drobne D. Front Immunol. (2) Is the CE a source of multipotent (stem) cells during regeneration? PubMed Although many structures such as the axial organ (Golconda et al. This information should not be considered complete, up to date, and is not intended to be used in place of a visit, consultation, or advice of a legal, medical, or any other professional. Microsc Res Tech 55:452463. FEBS J 287:45004524. The full annotation of the identified proteins using the UniProt Gene Ontology information by STRAP analysis is provided in Online Resource 5. Due to its histogenetic potential, CE is considered a key tissue characterized by unique features. 4g). iTEM micrograph of new radial water canal (rwc) CE. 2009). Additionally, in the Eastern oyster Crassostrea virginica, exosome-like vesicles relating to shell formation and repair have been observed (Auguste et al. Epub 2022 Sep 9. It constitutes the outermost layer of the male and female gonads, thus forming the germinal epithelium of the female or of the male. 2018). Register Upload it here to share it with the entire community. We compared the histological results obtained in standard physiological condition, i.e., in intact normal arms, with those obtained in post-traumatic regrowth condition, i.e., in regenerating arms at different stages. 2021). 2017). cSemithin longitudinal section of the regenerating radial water canal (rwc) lined by the CE. 2e), it was most evident in the radial water canal CE, particularly at the level of the terminal podium (Fig. Rate the pronunciation difficulty of coelomic. 1a) displayed the typical bi-layered structure of a pseudostratified myoepithelium described in the literature for other starfish (Wood and Cavey 1981; Rieger and Lombardi 1987), where apical squamous/cubic peritoneocytes and subapical longitudinally oriented myocytes are placed on the same basal lamina (Fig. PubMed hTEM micrograph of regenerating perivisceral CE (p) showing evident cell migration toward the mesenchymal tissue (mt). The analysis of the biological processes associated with the transcripts identified in these studies suggests the involvement of CE in the development of anatomical units. Neuron 17:353361 2009; Sharlaimova et al. Nucleic Acids Res 37:D750-754. Scale bar = 1m. Guatelli S, Ferrario C, Bonasoro F, Anjo SI, Manadas B, Candia Carnevali MD, Varela Coelho A, Sugni M. Cell Tissue Res. 2017). eSemithin longitudinal section of the regenerating CE at the level of the wound closure. Peritoneocytes are releasing apical cytoplasmic portions (asterisks). (2) The vesicular cells display an abundant cytoplasm, with massive presence of swollen endoplasmic reticulum (ER) cisternae and Golgi apparatuses (one or more), and a euchromatic nucleus. sharing sensitive information, make sure youre on a federal Check out the pronunciation, synonyms and grammar. The authors declare no competing interests. Scale bar A = 2m, scale bar inset = 500nm. https://doi.org/10.1002/jez.b.21352, Holm K, Dupont S, Skld H et al (2008) Induced cell proliferation in putative haematopoietic tissues of the sea star, Asterias rubens (L.). Oops! 2010), underlining the immune function of these cells. In non-regenerating samples, we never observed presumptive stem cells within the CE, although the possibility that these are located in other non-investigated part of the CE cannot be excluded. J Exp Biol 211:25512558. In fact, exo- and endocytosis work as coupled processes allowing the maintenance of the vesicle pool while preserving plasma membrane functionalities (Liang et al. gTEM micrograph of CE vesicular cell layer. Curr Opin Genet Dev 32:2430. (3) Does the CE display other key functions involved in regeneration as well as in overall animal physiology? Nat Cell Biol 2:246248. Coelomic fluid of asteroid echinoderms: Current knowledge and future perspectives on its utility for disease and mortality investigations. Federal government websites often end in .gov or .mil. 2019), Tiedemanns bodies (Kaneshiro and Karp 1980), and recently the pharynx (Golconda et al. 8600 Rockville Pike 2a, b, d). THE COMPARATIVE CHARACTERISTIC OF MORPHOLOGY AND PROLIFERATIVE ACTIVITY OF COELOMIC FLUID AND COELOMIC EPITHELIUM CELLS IN STARFISH ASTERIAS AMURENSIS AND STARFISH A. RUBENS. Start Free Trial Have a better pronunciation ? https://doi.org/10.1016/j.dci.2014.01.013. PubMed Central Catenin and actinin alpha 1 are other components of the adherent junction protein complexes (Yamada et al. The earliest sign of Mllerian duct formation is the thickening of the anterior mesonephric coelomic epithelium to form a placode of two distinct progenitor cells. Paramonov AS, Shulepko MA, Makhonin AM, Bychkov ML, Kulbatskii DS, Chernikov AM, Myshkin MY, Shabelnikov SV, Shenkarev ZO, Kirpichnikov MP, Lyukmanova EN. From a histological point of view, these vesicular cells belong to the circular muscle layer itself and can therefore be considered part of the myo-epithelial layer, as also suggested by the presence of scattered myocyte among them. Cells have high nucleus/cytoplasm ratio (asterisks). 2010 Jan;52(1):57-68. doi: 10.1111/j.1440-169X.2009.01159.x. Scale bar = 2m. Proteomics 15:757762. In: eLS. showing peritoneocytes (arrow); longitudinal muscle layer (lml); circular muscle layer (cml) with first signs of rearrangement; vesicular cells (asterisks). eTEM micrograph of vesicular cell layer showing several big phagosomes (asterisks). bDiagrammatic representation of perivisceral CE structure consisting of apical peritoneocytes (p); longitudinally oriented subapical myocytes (lm); common basal lamina (bl); basiepithelial nerve processes (np); and neurosecretory cells (nc). 2010), thus explaining their absence in the herein detected CE proteome. 2009). 2005). Log in to Pronouncekiwi https://doi.org/10.1002/pmic.201400221, Article In the distal-most arm tip where the circular muscle layer was not present, the vesicular layer was directly in contact with the longitudinal muscle layer (Fig. The perivisceral CE of M. glacialis arm (Fig. https://doi.org/10.1134/S1990519X12020113, Smith LC, Ghosh J, Buckley KM et al (2010) Echinoderm immunity. The Rab GDP dissociation inhibitor regulates the GDP/GTP exchange reaction by inhibiting the dissociation of GDP from them, and the subsequent binding of GTP. Overall, our work underlines that echinoderm CE is not a simple epithelial lining and that instead it plays multiple functions which span from immunity-related roles as well as being a source of regeneration-competent cells for arm growth/regrowth. Additionally, two arm tips were collected from each of three non-regenerating individuals. 137.187.44.188 . 2021). 1995a, 1997; Moss et al. Derived from the mesoderm, the coelom is found . CAS Stem Cells and Innate Immunity in Aquatic Invertebrates: Bridging Two Seemingly Disparate Disciplines for New Discoveries in Biology. Semithin (about 1m) and ultrathin (7090nm) sections were performed using a Reichert-Jung Ultracut E. Semithin sections were stained with crystal violet and basic fuchsin and photographed under a Jenaval light microscope provided with a Leica EC3 Camera and Leica Application Suite LAS EZ Software (Version 1.8.0). Part of this work was carried out at the imaging facility NOLIMITS (University of Milan). aSemithin longitudinal section of M. glacialis regenerating arm tip. The tryptic digestion was performed following a previously published protocol (Gomes et al. Our results show that CE cells share both ultrastructural and proteomic features with circulating coelomocytes (echinoderm immune cells). Congrats! At present, it is still an open question if de-differentiated/partially digested myocytes become a source of regeneration-competent multipotent cells, or if they are completely recycled (through phagocytosis) and used as a source of material/energy for the regenerative process, or if both pathways can occur (Candia Carnevali and Bonasoro 2001; Ben Khadra et al. (2018). Ultrathin sections were mounted on copper grids and stained with 1% uranyl acetate followed by lead citrate. 2005), namely in the sea urchin Strongylocentrotus purpuratus, the starfish Patiria miniata (Cameron et al. https://doi.org/10.1007/s00441-022-03678-x, DOI: https://doi.org/10.1007/s00441-022-03678-x. These circulating elements are considered the immune cells involved in the clearance of foreign materials, pathogens, and cell debris, as well in haemostatic functions, since they form clots at the wound sites (Pinsino et al. 2g). Before quantification, the protein extracts were diluted 1:300 to reduce the interference of DDT and EDTA. Briefly, the deep-frozen CE was placed in a previously chilled Teflon capsule containing 3 stainless steel beads (5mm in diameter). Despite these indications, the histological approach alone, microscopic or ultrastructural, is not sufficient to fully attribute a coelomocyte-producing role to the CE and even the presumptive production/release process of stem/pluripotent cells from coelothelium during regeneration needs to be confirmed as well. From BLASTp, we obtained a consistent number of identified proteins homologous to echinoderm proteins deposited on the searched protein databases (32%). Learn how to say Coelomic with EmmaSaying free pronunciation tutorials.Definition and meaning can be found here:https://www.google.com/search?q=define+Coelomic The site is secure. Scale bar = 2m. Adult specimens of Marthasterias glacialis with a size ranging from 15 to 35cm were collected at low tide on the west coast of Portugal (Estoril, Cascais). In order to partially unravel this gap, the present work is addressed to analyze the CE of the starfish Marthasterias glacialis in both standard physiological (homeostatic) and regenerating conditions, by combining histological/ultrastructural analyses with appropriate proteomics approaches, the former to provide a detailed cell and tissue perspective, the latter to contribute a baseline molecular view of CE multifunctional implications. https://doi.org/10.1016/j.immuni.2006.12.005, Yeo JC, Wall AA, Luo L, Stow JL (2016) Sequential recruitment of Rab GTPases during early stages of phagocytosis. Appearance of the ovary depends widely on the age / menopausal state: Newborn ovaries are elongated and approximately 1.3 cm in greatest dimension, Ovaries enlarge during infancy and childhood and reach adult size and shape by the time of puberty, Neonatal ovaries often have cysts, which resolve spontaneously (, 3 - 5 cm long and weigh 5 - 8 g; size and weight depend on the amount of follicular derivatives (cysts and corpora albicantia / lutea), Pink-white exterior is initially smooth but gradually becomes more convoluted, Cystic follicles and corpora lutea may be visible from outside, Cut section may exhibit 3 zones: cortex, medulla and hilus, with follicular derivatives usually in the cortex and medulla, Firm consistency with solid, pale cut surface, Occasional cysts measuring several millimeters in diameter (inclusion cysts) may be discernible within the cortex, Small white scars (corpora albicantia) are typically present within the medulla, Thick walled blood vessels may be appreciable within the medulla and the hilus, Arterial supply: approximately 10 arterial branches from anastomotic arcade of ovarian artery (branch of aorta) and ovarian branch of uterine artery penetrate hilus into medulla and cortex, Venous drainage: left ovarian vein drains to left renal vein, right ovarian vein drains to inferior vena cava, Lymphatic drainage: originates predominantly from theca layer of follicles, exiting through the hilus, to the mesovarium, along the infundibulopelvic ligament, into upper paraaortic lymph nodes; may bypass to internal iliac, external iliac, common iliac, sacral, obturator, pelvic, retroperitoneal or inguinal nodes, Enlarged corpus luteum cyst can trigger an intraoperative consultation; the cyst lining is yellow and has a convoluted appearance, Luteoma of pregnancy can be discovered incidentally during cesarean section or preoperatively on imaging study mimicking an ovarian mass (. Selected regenerating time-points were 24h, 48h, and 1week post-amputation (p.a.). Candidate ions with a charge state between +2 and +5 and counts above a minimum threshold of 10 counts/s were isolated for fragmentation and one MS/MS spectra was collected before adding those ions to the exclusion list (mass spectrometer operated by Analyst TF 1.7, ABSciex). However, proteomics investigations focused on echinoderm CE are quite limited. Stem Cells Transl Med 6:634646. Vet Pathol. (XLSX 62 KB), Supplementary file5 Online Resource 5 Full annotation of the identified proteins using the UniProt Gene Ontology information by STRAP analysis. 2011), which partially shed light on this heterogeneous cell population and its possible related functions in this species. Zoomorphology 129:119. Wound Rep Reg 23(4):611622, Ben Khadra Y, Ferrario C, Benedetto CD, Said K, Bonasoro F, Carnevali MD, Sugni M (2015b) Regrowth, morphogenesis, and differentiation during starfish arm regeneration. Cell and Tissue Research A rearranging ampulla (a) is recognizable. Scale bar = 400m. a Biological process; b cellular components; c molecular function. Correspondence to 2h), and few phagosomes (Fig. However, we cannot answer medical or research questions or give advice. In adults, it is involved in body fluid homeostasis and transport, in cooperation with immune system cells, and in cytokine and growth factor synthesis (Mutsaers and Wilkosz 2007; Ariza et al. https://doi.org/10.1007/s00441-020-03337-z, Sharlaimova N, Shabelnikov S, Petukhova O (2014) Small coelomic epithelial cells of the starfish Asterias rubens L. that are able to proliferate in vivo and in vitro. Another cell degradation system is the ubiquitinproteasome where, upon ubiquitination, proteins become degraded by the proteasome (a complex of proteases) (Kleiger and Mayor 2014). Introduction Intra-embryonic coelom week 3-4 ( - (Greek, = cavity) Term used to describe a fluid-filled cavity or space. https://doi.org/10.1093/nar/gku1003, Teixeira FG, Carvalho MM, Panchalingam KM et al (2017) Impact of the secretome of human mesenchymal stem cells on brain structure and animal behavior in a rat model of Parkinsons disease. Phagosomes are visible at the cell base (arrows). These membrane vesicles (30150nm in size) offer a potent mechanism for communication between nearby or distant cells or tissues in order to change their physiological functions and properties in specific innate and adaptive immune responses, as reported in several marine invertebrates. PubMedGoogle Scholar. https://doi.org/10.1242/jeb.018507, Hyman LH (1955) The invertebrates. 2005). https://doi.org/10.1016/j.cell.2005.09.020, Yang Y, Liu B, Dai J et al (2007) Heat shock protein gp96 is a master chaperone for toll-like receptors and is important in the innate function of macrophages. Scale bar = 10m. ajCE of 1week p.a. hTEM micrograph of vesicular cell containing small RER cisternae (black asterisks) and a presumptive phagosome (arrow). ahCE of stump in a regenerating sample: 2448h p.a. In other animals, such as molluscs, it remains undifferentiated. Several chaperons, like endoplasmic reticulum chaperone BiP, are members of the endoplasmic reticulum quality-control system tasked with detecting proteins that fail to mature properly and to target them for cytosolic degradation (Pobre et al. Indeed, both ultrastructural and proteomic investigations suggest that it is a highly complex tissue that plays diverse functions and is involved in several key physiological processes. The rearrangement of the cytoskeleton involves also the regulation of the aforementioned pathway by the Rho family of small GTPase, a group of key regulatory molecules that link surface receptors to the actin cytoskeleton (Goitre et al. Scale bar = 5m. This site needs JavaScript to work properly. However, it is important to note that in echinoderms, the term coelomocytes is used to refer to heterogeneous cell populations which can differ from class to class in terms of both morphology and function such as presumptive stem cells as well as immune cells (Smith et al. The identification of p38- in M. glacialis CE proteome might be also considered an indirect evidence of the expression of TNF-. The membrane that lines the inside of the abdomen and encloses the abdominal organs. Talin interacts with membrane integrins in these indirect cellular junctions that also include the lipoma-preferred partner protein, and both junction types contain the actin-binding protein vinculin (Miller et al. Gene expression of Ras-related protein Rab, a protein from the small GTPases Rab family, is induced by LPS to regulate the replenishing of the plasma membrane with TLRs (Yeo et al. Front Immunol 10:870. https://doi.org/10.3389/fimmu.2019.00870, Gomes LP, Anjo SI, Manadas B et al (2019) Proteomic analyses reveal new insights on the antimicrobial mechanisms of chitosan biopolymers and their nanosized particles against Escherichia coli.
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