Progress in Neurobiology, 1979, Vol. 12, pp. 115-179. Pergamon Press. Printed in Great Britain.

INVERTEBRATE GLIA TRICIA RADOJClC and V. W. PENTREATH Department of Biolo#y, University of Salford, Salford M5 4WT (Received 1 November 1978) Contents

1. Introduction 2. Criteria for the identification of gila 3. The glia in invertebrate nervous systems 3.1. Coelenterata 3.2. Echinodermata 3.3. Platyhelmintha 3.4. Aschelmintha 3.5. Annelida 3.6. Arthropoda 3.6.1. Insecta 3.6.2. Crustacea 3.7. Mollusca 4. Conclusions 5. Comparisons with vertebrate neuroglia 6. Acknowledgements 7. References

115 116 117 117 117 118 118 119 123 123 135 141 155 159 160 160 1. Introduction

The glial cells in the mammalian brain have been studied by neuroanatomists since the classical work of del Rio Hortega and Cajal demonstrated their special and complex relationship with neurons. It is evident that they make up to half the volume of the central nervous system, and may greatly outnumber the neurons. The electron microscope has shown several morphologically distinct types; namely, the astrocytes (protoplasmic and fibrous), oligodendrocytes and ependymal of the central nervous system, and the Schwann cells of the peripheral nervous system. Some authors include microglial cells. A definite functional role has been assigned to some glial cells; oligodendrocytes and Schwann cells form myelin around axons and speed up conduction of nerve impulses. Several functions have been suggested for other glial cells (e.g. structural support, repair and regeneration of neurons, uptake and release of chemical transmitters, isolation and insulation of neurons, nutrition and transfer of substances to neurons) but these await clarification. Relatively little is known about the numbers, types and physiological roles of glial cells either in normal or diseased states. Among invertebrates the situation is complex, for not only are the functions of glia again generally unknown, but also the morphological types are indistinct and show great variation. In addition the appearance of glia varies widely among the different phyla, and identification is complicated by the presence of mesodermally derived elements in the ganglia of some animals. For example, blood vessels, connective tissue and mesenchymal elements have been observed in the ganglia of a variety of animals. The relatively unspecialized mesenchymal cells are very difficult to distinguish from "true glia". A survey of the literature gives the impression that in many anatomical studies cells have been named glia because they are not obviously neuronal. While this negative categorization is inevitable in the absence of positive criteria, and is not necessarily wrong, it has tended for glia to be a convenient title under which to group unrecognizable cell types within nervous tissue. The purpose of this review is to summarize the recent studies on invertebrate glia. There are several works which thoroughly cover mammalian glia (Glees, 1955; Windle, 1958; De Robertis and Gersehenfeld, 1961; Kuffier and Nicholls, 1966; Johnson and Roots, 1972; 115

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Watson, 1974) some of which include selected aspects of the cells in some invertebrates. There are two reviews on invertebrate glia, one which describes the early literature (Clayton, 1932) and one which covers specifically molluscan glia (Nicaise, 1973). In this article we attempt to update, tabulate and evaluate the information on invertebrate glia.

2. Criteria for the Identification of Glia There is no adequate definition of "true glia". In the mammalian CNS anatomical identification is comparatively easy, and in the absence of known functions, a variety of relatively imprecise statements have been adopted in the literature. For example, a fairly suitable definition in vertebrate systems is "the connective tissue of the brain". The cellular morphology of the invertebrate nervous systems is often very different from that of mammals; the problem confronting the anatomist is how to tell whether or not a particular cell is a glial cell and a possible counterpart of the mammalian neuroglial cell.* At present this problem cannot be easily resolved, but several authors have advanced solutions for particular situations. For example, "Other cells besides the nerve cells are found in insect ganglia. Since they are not nerve cells and since they occur between and among the nerve cells and fibres, they are probably neuroglia..." (Hess, 1958b). and referring to a gastropod mollusc, "globular cells are not intimately related to the neurons of the ganglion and there is no reason to include these cells in the neuroglia" (Rogers, 1969b). Although these definitions are of some value for the glia in more complex invertebrates, they are inadequate for simpler invertebrates. Some of the simpler nervous systems not only contain many undifferentiated cells, but also may lack aggregation into ganglia, making it difficult to judge what belongs inside the nervous system and what belongs outside. Perhaps this is one reason why positive information on the glia of these animals is so scarce. However, it is important to have suitable criteria for the identification of glia and neuroglia, applicable to lower invertebrates as well as mammals. We propose that cells regarded as glia and neuroglia should conform to criteria 1 and 2 listed below, although in certain situations discussed in the text criterion 3 may take the place of 1. (1) The cells should have an intimate morphological relationship with neurons; they should ensheath, invest or surround neuronal perikarya or their processes, be separated from them by narrow extracellular spaces of approximately 10-20 nm, and thus provide the immediate non-neuronal cellular environment. It is important that non-glial types of cell which occasionally occur adjacent to neurons (e.g. the migratory macrophages in the vertebrate brain) are not erroneously included; however these are generally recognizable as specialized for other functions. (2) They should originate from embryonic ectoderm. Although the vertebrate microglia are an exception to the rule, their mesodermal origin has not been clearly established. Several authors choose not to consider them strictly comparable to other neuroglial types due to their transitory nature and erratic staining properties. (3) Certain glial cells and/or their processes may separate neuronal elements from mesodermal cellular layers and/or their products, and thus form a layer (generally incomplete) surrounding an area of nervous tissue. These criteria, based on existing anatomical and embryological considerations are put forward as a basis for the following review. As new microbiochemical, immunological and physiological investigations advance our understanding of glia, other more valuable criteria based on their physiological and functional properties will undoubtedly be added. In relation to this Soreide et al. (1978) have recently suggested that selective uptake of beta alanine is a characteristic of mammalian glia, although it is not yet clear whether this is the case in invertebrates. * The term neuroglia is applied only to vertebrates; for invertebrates the term glia is used. This distinction will avoid any preconceptions about homologous structure and function between the different animal groups.

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3. The Glia in Invertebrate Nervous Systems

3.1. COELENTERATA Coelenterates possess the simplest recognizable nervous systems among the invertebrate phyla. They consist of bi- or multipolar neurons arranged in intercommunicating plexuses between the ectodermal layers and the muscle layers (Hyman, 1940). The nerve plexus supplies the gastrodermaJ layer and may also extend into the mesogloea in some species (Hyman, 1940). Only in some of the medusoid forms does any concentration of the nervous system appear. This takes the form of a loose gathering of neuronal cell bodies and axons into what could be termed a nerve ring at the velar attachment. The differentiation and demarcation of this nerve ring is not obvious (Bullock and Horridge, 1965), and hence the applicability of the term central nervous system in any sense is questionable. Ganglia have been noted in some higher species. Sarsia, an anthomedusan, has four ganglia at the base of the tentacle ring. Although the ganglia have a loosely arranged cortex and neuropile, they lack a connective tissue covering. There have been no descriptions of glia. There is agreement that glial tissue does not exist in this phylum (Chapman, 1974). Horridge and MacKay (1962) did not find glia in either Cyanea capillata or Phialidium hemispherium. Axons are loosely surrounded by membranes of cells that are "clearly specialized for other functions" and have no intimate relationship with the axons, i.e. do not "creep around the nerve fibres" (Horridge and MacKay, 1962). Thus, it appears that in these animals, neuronal function does not require glia, but more work is necessary to prove their absence. 3.2. ECHINODERMATA Echinoderms have circular and radial nerve cords which are sufficiently specialized to be termed a central nervous system. These central tracts give rise to a series of bilaterally and metamerically repeated series of nerves, some of which run to the musculature and are purely motor, while others are of mixed composition. The animals also possess an extensive system of nerve plexuses which underlies most of the body surface. There are no true ganglionic complexes of nerve cells; it appears that neuron perikarya are scattered along the nerve trunks or located in the epithelium (Pentreath and Cobb, 1972). It is generally accepted that the nervous tissue of each class consists of three more or less separate parts (Hyman, 1940; Smith, 1965; Nichols, 1967). The ectoneural system, of ectodermal origin is chiefly sensory and comprises a large proportion of the general skin plexus and central pathways. The hyponeural tissue, which is always in close association with the radial cords and circumoral ring, is exclusively motor, while the apical nerve is of presumed mesodermal origin, and is also regarded as motor. There do not appear to be any cells in echinoderms similar in structure or organization to those described as typical glial cells in other invertebrate and vertebrate groups. Two cell types have been reported that may be glial in function. First, there are cells situated below the epithelium of the radial nerve. These send long, thin, inward-projecting processes through the main trunk of axons, dividing it into bundles each containing some hundreds of axons. The detailed anatomy of these fibrous processes has been discussed by Kawaguti (1965), Kawaguti et al. (1965), Cobb and Laverack (1966) and Cobb (1970). Bargmann et al. (1962) suggested that these cells (termed "Stfitzzellen") play a supportive role in the nervous system and have termed them glial. However these cells neither closely surround nor ensheath neurons in the cord, nor has a supportive function for the nervous tissue been proven. Should an as yet undetermined glial function be demonstrated for these cells they will be the most primitive glia amongst invertebrates, because they are not differentiated from epidermal tissues of ectodermal derivation. Second, von Hehn (1970) concurred that the Stfitzzellen were glial, and in addition suggested that the coelomic epithelial cells which cover the hyponeural ganglion cells may be glial cells. Although both cell types have an obvious structural role in the nerve cords,

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there is no evidence to suggest that they are involved functionally in any aspect of the metabolism of the nerve cells. Indeed the sparcity of these cell types in the main axon trunks suggests that their function(s) is limited to a small proportion of the nervous tissue. 3.3. PLATYHELMINTHA The platyhelminths are the lowest animals that exhibit cephalization and a distinguishable central and peripheral nervous system. "While the peripheral nervous system is made up of a complex network of nerve plexuses, the central nervous system in the majority of these animals consists of well-defined but varying numbers of nerve cords, nerve rings, connectives and cerebral ganglia (Kuhlenbeck, 1967). The cerebral ganglia, which are potential sites of glia in these animals, show variation amongst the three classes in this phylum: Cestoda: The ganglia are not clearly organized into cell body and neuropile regions and lack any sort of sheath. Trematoda: The ganglia have poorly differentiated cortex and neuropile but are surrounded by a connective tissue sheath. There is no obvious demarcation between ganglion and sheath. Turbellaria: The ganglia exhibit considerable variation. The range is from a relatively diffuse collection of nerve fibres to fairly compacted ganglia with recognizable cortex and neuropile. The ganglional ensheathment varies from nearly absent to complete encapsulation (Bullock and Horridge 1965). Unfortunately no fine structural study of glia has been undertaken in this group. The available information dates from the early 1900s and has been reviewed by Bullock and Horridge (1965). All three classes contain cells surrounding the neurons. These have been termed parenchyma (Johnstone, 1912) mesenchyme (Bullock and Horridge, 1965) neuroglia (Bullock and Horridge, 1965) and supporting cells (Turner, 1946) amongst others. There is little agreement concerning the nature of glia in any of the classes, and this is reflected in the wide variation in nomenclature. The presence of muscle cells (in the Turbellaria), connective tissue (in the Trematoda) and mesenchyme (in the Cestoda) which are continuous with and often similar to the tissue surrounding the ganglia complicates the identification of glia. There do not appear to be any developmental studies to allow distinction of ectodermal elements from mesodermal. However light microscopy has not revealed cells that ensheath neurons, penetrate neurons in the form of trophospongium, or form any other close morphological or possible functional relationship with neurons (Kuhlenbeck, 1967). Work with the electron microscope is necessary to clarify the situation. 3.4. ASCHELMINTHA(NEMATODA)

Nematodes, like platyhelminths, have a simple cephalized nervous system. Chitwood and Chitwood (1950) described the central nervous system as composed of a perioesophaseal nerve ring, ventral nerve trunks exhibiting various degrees of fusion, and a collection of loosely organized ganglia. The peripheral nervous system consists of nerves supplying the sensory structures and the rest of the body. Nematode ganglia lack a well defined cortex and neuropile as well as a discrete ensheathing connective tissue capsule. The number of neurons and glial cells vary from species to species. The glia/neuron ratio (as well as the size of the glial cells surrounding the nerve ring; see Chitwood and Chitwood, 1950) is similar to the glia occurring in leeches. To date, information on nematode glia is scanty. Most data is in Goldschmidt's (1907, 1908, 1909, 1910) study on Ascaris completed in 1910. There has been no comprehensive electron microscopic study of the central nervous system, and, therefore, descriptions of the ultrastructural features are incomplete. However, intimate relationships between neurons and glia have been observed. Glial cells not only enwrap axons as they leave the ganglia or the nerve ring, but also invest neuronal cell bodies with numerous invaginations into a trophospongium (Chitwood and Chitwood, 1950; Bird, 1971). Most authors agree on the glial nature of the cells located on the outer surface of the nerve ring. They are generally referred to as glial cells (Hyman, 1940; Chitwood and

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Chitwood, 1950; De Coninck in Grassr, 1965) although McLaren (1972) in her study of Dipetalonema vitae refers to them as "ensheathing cells". She describes the following ultrastructural features: Nucleus, large, round and pale with a prominent nucleolus; Shape, flattened; Cytoplasm, dark and granular; Organelles, mitochondria, Golgi structures, rough endoplasmic reticulum; Inclusions, ribosomes, fibre bundles. In a similar fashion Siddiqui and Vigliercio (1971) noted the following organelles and inclusions in the glia of the peripheral nervous system of Deontostoma californicum; mitochondria, smooth ER, Golgi structures, membrane-bound lamellate bodies (diameters 200-640 nm), granular bodies resembling gliosomes (diameters 0.2-0.4 and 0.7-1.0 #m) and lysosome--like inclusions, gliofilaments and microtubules. Other cells, not so closely associated with the nervous system may also be found to have a glial nature. These include the so-called escort and clavate cells (Chitwood and Chitwood, 1950) of the central nervous system, as well as a variety of cells in the peripheral nervous system, especially the cells associated with the cephalic sense organs. These are the multivesicular cells and supporting cells (McLaren, 1972), the companion cells (Wright, 1974) and the gland ceils (Baldwin and Herschmann, 1975). However, many of these cells do not occur consistently in all species and their glial nature awaits confirmation. Only in Ascaris have glial processes in the cephalic sensory structures been clearly traced to their nuclei located on the nerve ring, thus verifying their glial nature (Chitwood and Chitwood, 1950). Due to the lack of data on glial cells in the nematode central nervous system, generalizations concerning their structure and possible functions cannot be made. Further research into their ultra-structure, development and physiology is necessary. 3.5. ANNELIDA The central nervous system in annelids consists of a pair of ventral nerve cords which exhibit various degrees of fusion. Along the nerve cords there is a segmental arrangement of compact ganglia. In the anterior region several fused ganglia give marked cephalization (Bullock and Horridge, 1965). The ganglia have the following common features: (1) A morphologically distinct cortex and neuropile. The neuropile is bounded by a layer of tissue that has been called glial in some species, for example Nereis (Baskin, 1971a, c), and connective tissue in others, for example Lumbricus (Coggeshall, 1965) and the leech (Coggeshall and Fawcett, 1964). (2) A connective tissue capsule of varying thickness (6-30 pm) in different animals. This capsule not only covers the ganglia, but also the nerves and connectives (Hagadorn et al., 1963; Levi et al., 1966). (3) Connective tissue trabeculae which dip into the ganglia (Hagadorn et al., 1963; Gray and Guillery, 1963b; Coggeshall and Fawcett, 1964; Holmes, 1930). (4) The connective tissue is composed of layers which are mesodermal in nature, i.e. muscle cells and fibroblasts (Coggeshall and Fawcett, 1964; Coggeshall, 1965; Levi et al., 1966; Buskin, 1971b). In addition there are distinctive features of two of the classes which are important in the present discussion. First, the Oligochaeta have a vascular supply inside the ganglion. (Holmes, 1930; Coggeshall, 1965; Levi et al., 1966). These animals, together with Crustacea and cephalopods are the only invertebrates to have this arrangement (Stephenson, 1930). Second, the Hirudinea possess distinct glial cells. They are exceptionally large but few in number and contain nuclei with uncharacteristic glial morphology; the nuclear membrane is fibrous and chromatin is sparse (Gray and Guillery, 1963b). These glia divide the neurons into "packets" which encircle the neuropile (Coggeshall and Fawcett, 1964). In the cerebral ganglia however there are numerous relatively small glia which resemble those in most other invertebrates (Kai-Kai, unpublished observation). The reason for this difference is not yet clear. Thus the annelids possess compact, ensheathed ganglia, making the separation of the nervous system from surrounding tissues more obvious than in the simpler phyla, and so aiding the analysis of their glia. However, the presence of mesodermal elements, such as fibroblasts, and in some cases blood vessels within the ganglion does not make this easy.

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In many cases, excluding the leeches, the nucleus of the glial cells is similar to that of mesodermal elements, both in size as well as peripheral chromatin distribution (Holmes, 1930). Unfortunately, few authors (with the exception of Holmes, 1930) have defined the characteristics which distinguish the two groups of cells, though they are thought to be of different embryological origin (Johnson and Roots, 1972). Hermans (1969), in his study of Armandia brevis, has found that a basal lamina exists between the tissues of mesodermal and ectodermal derivation. This situation has not been noted in other members of this phylum. The anatomical relationship between neurons and glia in annelids is close (see Figs 1-3). Glial tissue forms a trophospongium as well as a wrapping around the neurons that some authors have compared to the loose myelin of vertebrates (Stephenson, 1930; Gray and Guillery, 1963a; Golding, 1967). The space between the neurons and gila consists of a narrow extracellular space of approximately 15 nm (Gray and Guillery, 1963a; Kuffler and Potter, 1964; Coggeshall, 1965) and is scattered with desmosomes (Gray and Guillery, 1963a; Levi et al., 1966; Coggeshall and Fawcett, 1967) which join glia to glia and glia to neuron. Several studies have been made of the morphology of glial cells of representatives of this phylum. Detailed information has been obtained on the glia ofLumbricus terrestris, Nereis virens and Hirudo medicinalis. The results are summarized in Table 1. It appears that there are certain important features which are common to glia in this phylum, and they are briefly described as follows: (1) Gliofilaments (also termed microfilaments, microfibrils, gliofibrils and tonofilaments) are always present in glia associated with axonal processes. They are therefore a distinguishing feature of glia found in neuropile, connectives and peripheral nerves. These filaments are all reported to be 5 nm in diameter (see Table 1 for references). A reason for the presence of this extensive fibrillar system in Nereis, as well as other members of the phylum, has been proposed by Baskin (1971c). It is that since annelids possess a hydrostatic skeleton and undergo extensive alterations of body length and thickness, the nervous system of these animals is subjected to many shearing forces and other stresses. The gliofilaments function to counteract these stresses. In relation to this Coggeshall (1966) described in the leech another stress-resistant specialization which occurs in addition to filamentous glia. These are a form of glia occurring at the nerve/ganglional junction which he called fasicular glia. He suggested that these glia absorb the stress exerted at this junction by the changes in body shape (Coggeshall, 1966). (2) Desmosomes and hemi-desmosomes serve to attach glia to glia, glia to neuron and glia to ganglional sheath. Although in some glia desmosomes have not been reported, such glia have been postulated to be migratory (e.g. the small glia in the leech and the migratory glia in Lumbricus). However there is no evidence of their occurrence outside the ganglion, nor have they been observed entering or leaving the ganglion (Coggeshall and Fawcett, 1964; Coggeshall, 1965). Perhaps embryological studies will clarify this point. (3) Some glial cells appear to be metabolically active. They occur principally in the ganglion cortex but also abut the collagenous ganglional sheath, e.g. the packet glia of the leech (Coggeshall and Fawcett, 1964), and the cortical glia of Lumbricus (Levi et al., 1966). Glial filaments are either reduced or lacking and are replaced by various assortments of dilated cisternae of endoplasmic reticulum, prominent Golgi structures, numerous mitochondria, and different types of vesicles. Because of the absence of filaments, and to avoid confusion, it is convenient to term these cells plasmatic glia. Such cells are usually associated with neuronal cell bodies in the cortex of the ganglion. Although some authors have suggested that these cells are concerned with the transfer of nutrients and metabolites to the interior of the ganglion, work with the leech indicates otherwise (Nicholls and Kuffler, 1964; Globus et al., 1973). It has been demonstrated that nutrients enter the ganglion too fast to be accounted for by intracellular transfer. Findings also indicate that nutrients diffuse very adequately through the extensive extracellular channels that occur in the ganglion. Though glial cells do take up nutrients, they may well be storage sites, from which the nutrients can be released in time of need (Nicholls and Wolfe, 1967; Wolfe

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and Nicholls, 1967; see below). However, it must be borne in mind that the glial system of the leech is itself exceptional in both cell size as well as certain of the ultrastructural features, and hence the results may not have general significance. Work of a similar nature on other animals (both vertebrates and invertebrates) is necessary to clarify this point. At present there are no data on the role ofglia, trophic or otherwise, in the Oligochaeta and Polychaeta. However, although the ganglion of Lumbricus is no larger than that of Nereis or the leech, it has a vascular supply, which may reflect differences in the route(s) of ganglional nutrition. (4) Types of glia intermediate between those described in I and 3 above have been reported. These cells possess filamentous processes as well as having an active metabolic appearance (Baskin, 1971b; see Table 1). Although both characteristic features are present, they are reduced in comparison to the more extreme cases described in 1 and 2. Some authors have suggested that there is specialization into the extremes because of the functional demands put upon a particular glial cell by its immediate surroundings; in other words the specialization may depend upon its location in the ganglion. This is reflected in the differences in glial ultrastructure between the cortex and core of the ganglia and the nerves and commissures (Levi et al., 1966). Several aspects of the physiology of the large and easily accessible glial cells in the leech ganglia have been elegantly studied by Nicholls and Kuffler (see Kuffler and Nicholls, 1966, for references). Mention of some of these has already been made but they deserve further description. The glial cells have been impaled with microelectrodes, and it has been found that they have greater membrane potentials than neurons, that they do not fire action potentials, and that they are connected to one another by low resistance electrical pathways. Electrical activity in the adjacent neurons induced by applied depolarization resulted in an increase in potassium in the extracellular space between neurons and glia. This in turn resulted in a glial depolarization with an associated redistribution of potassium in the ganglion from areas of high concentration via the low resistance pathways (assumed to be gap junctions) between adjacent glial cells (Nicholls and Kuifler, 1964; Kuttter and Potter, 1964). It has also been shown that neurons could readily take up nutrients such as sugars and amino acids from the extracellular space. However, long-term activity may require the transfer of nutrients (e.g. glycogen) stored in glia, which could be triggered by glial depolarization in response to potassium build-up (Wolfe and Nicholls, 1967; Nicholls and Wolfe, 1967; Globus et al., 1973). Finally, ablation of the glial cells did not effect short-term electrical activity in the adjacent neurons, although this might not be true for sustained neuronal activity (Kuffler, 1967). Taken together the results suggest that the large glial cells in leech ganglia may be concerned with the long-term back-up and maintenance of the neurons rather than supply their immediate demands. In summary, several features are evident about annelid glia. The glia are more easily identifiable than those in the previously described phyla. This is largely because the annelid nervous system is compact and encapsulated. In the Hirudinea some glial cells are unusually large. Intimate morphological relationships are evident between glia and neurons. The presently accepted functions of annelid glia are mechanical support and long range maintenance of neurons, but others may soon be found. 3.6. ARTHROPODA 3.6.1. Insecta

Several features of the organization of the insect nervous system are pertinent to the following discussion: (1) The ganglia consist of rinds of neuronal cell bodies, with neuropile in the core. The neuropile is bounded and invaded by glial tissue. There is distinct cephalization; the anterior ganglia are often fused and lobed in complex masses. (2) Each ganglion is surrounded by a connective tissue sheath, termed the neural lamella or neurilemma, which is composed of a homogenous ground substance (probably a neutral mucopolysaccharide) together with fibres similar to collagen but exhibiting a different periodicity

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Progress in Neurobiology, 1979, Vol. 12, pp. 115-179. Pergamon Press. Printed in Great Britain. INVERTEBRATE GLIA TRICIA RADOJClC and V. W. PENTREATH...
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