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PubMed1998

Cell proliferation in a peripheral target is required for the induction of central neurogenesis in the leech.

Several days after the completion of the early phase of cell proliferation that generates most of the leech central nervous system, the pair of "sex ganglia" in the two reproductive segments of the midbody undergo a second period of neurogenesis that gives rise to several hundred peripherally induced central (PIC) neurons. This proliferative phase, which begins on embryonic day 17 (E17), is induced by the interaction of a few specific neurons in the sex ganglia with a peripheral target, the male genitalia, during a critical period that extends from E13 to E16. The central nervous system (CNS) determines the critical period, since the male genitalia have the capacity to induce PIC neurons beginning on E10 and continuing throughout embryogenesis. Here we first show, by injecting hydroxyurea into staged embryos to ablate dividing cells, that PIC neuron precursors begin to divide at a low rate before E17, during the critical period. Then, through a series of homochronic and heterochronic male organ transplantations combined with hydroxyurea treatment of hosts and/or donors, we show that cell proliferation is required in the target itself for it to be competent to induce PIC neurons. These observations demonstrate that a nerve connection can couple cell proliferation in a peripheral target to cell proliferation in the CNS, providing a novel means for size adjustment of a central neuronal population relative to a peripheral target.

Animals↗

PubMed1999

Gliarin and macrolin, two novel intermediate filament proteins specifically expressed in sets and subsets of glial cells in leech central nervous system.

Using monoclonal antibodies, we have identified two novel intermediate filament (IF) proteins, Gliarin and Macrolin, which are specifically expressed in the central nervous system of an invertebrate. The two proteins both contain the coiled-coil rod domain typical of the superfamily of IF proteins flanked by unique N- and C-terminal domains. Gliarin was found in all glial cells including macro- and microglial cells, whereas Macrolin was expressed in only a single pair of giant connective glial cells. The identification of Macrolin and Gliarin together with the characterization of the strictly neuronal IF protein Filarin in leech central nervous system demonstrate that multiple neuron- and glial-specific IFs are not unique to the vertebrate nervous system but are also found in invertebrates. Interestingly, phylogenetic analysis based on maximum parsimony indicated that the presence of neuron- and glial cell-specific IFs in coelomate protostomes as well as in vertebrates is not of monophyletic origin, but rather represents convergent evolution and appears to have arisen independently.

Amino Acid Sequence↗

PubMed1999

Glial responses during evoked behaviors in the leech.

Glial cells can respond with membrane potential changes during electrically stimulated neuronal activity (Kuffler, Proc R Soc Lond B 168:1-21, 1967; Orkand, Oxford University Press, 1995). Their role in contributing to, or controlling, neural circuits underlying behaviors, however, is completely unknown. We have used semi-intact preparations of the leech Hirudo medicinalis, where behaviors can be elicited and monitored (Kristan et al., J Neurobiol 27:380-389, 1995), to record membrane responses of identified glial cells during whole-body shortening and during fictive swimming. Giant glial cells are located in the neuropil of segmental ganglia, where neuronal axons and dendrites establish numerous synaptic contacts (Coggeshall and Fawcett, J Neurophysiol 27:229-289, 1964). We report here that these glial cells hyperpolarize when the whole-body-shortening response is evoked but not during fictive swimming. To our knowledge, this is the first report that associates a specific behavior with glial cell responses.

Animals↗

PubMed2000

Possible role of the receptor protein tyrosine phosphatase HmLAR2 in interbranch repulsion in a leech embryonic cell.

Accumulating evidence indicates that receptor protein tyrosine phosphatases (rPTPs) play major roles in growth cone migration. We have previously shown that the growth cones of the multiple parallel processes of an identified leech embryonic cell, the Comb cell (CC), express high levels of a leukocyte antigen-related (LAR)-like rPTP, HmLAR2. Embryonic injection of a polyclonal antibody to the receptor's ectodomain resulted in reduced process outgrowth and in processes crossing over each other, a behavior that is seldom observed in normal or control animals. Here we present results of injecting a soluble Fc-HmLAR2 ectodomain fusion protein into embryos in order to bind the endogenous ligands of HmLAR2. Single injections of the Fc-chimeric protein into the developing embryo resulted, 12 to 24 h postinjection, in clear morphological abnormalities, ranging from abnormally directed CC processes and crossovers to apparent growth cone collapse. At later times, 2 to 5 days post injection, growth cones appeared to have recovered and processes had continued to extend, but effects of the earlier guidance errors remained, with the CCs displaying a relatively high incidence of proximal guidance errors. When injected into the germinal plate of developing embryos, the fusion protein was found to bind selectively to the processes of the CCs themselves, in contrast to control injections of Fc alone or closely related Fc-tagged proteins, which did not decorate the CCs. Double-labeling experiments revealed an early phase of Fc-HmLAR2 labeling (within 20 min after application), during which the growth cones and filopodia of the CC showed significant binding of the receptor ectodomain, and a later phase (1-2 h after injection), when most of the label was redistributed away from the growth cones and into the proximal processes of the CC. In culture, HmLAR2-transfected COS cells were found to selectively bind the Fc-recombinant protein, but not Fc-tagged proteins bearing other closely related receptor ectodomains, demonstrating that the HmLAR2 ectodomain is capable of interacting homophilically. Together, our observations demonstrate that the rPTP HmLAR2 is critically involved in CC process extension through its participation in the regulation of growth cone structure, migration, and navigation. Moreover, since our experiments also indicate that HmLAR2 can bind to itself, we hypothesize that HmLAR2 has a key role in the mechanism of mutual repulsion that maintains the parallel growth of adjacent CC projections.

Animals↗

PubMed2002

Reorganization and translocation of the ectoplasmic cytoskeleton in the leech zygote by condensation of cytasters and interactions of dynamic microtubules and actin filaments.

The formation and bipolar translocation of an ectoplasmic cytoskeleton of rings and meridional bands was studied in interphase zygotes of the glossiphoniid leech Theromyzon trizonare. Zygotes consisted of a peripheral organelle-rich ectoplasm and an internal yolk-rich endoplasm. After microinjection of labeled tubulin and/or actin, zygotes were examined by time-lapse video imaging, immunofluorescence and confocal microscopy. The rings and meridional bands were formed by condensation of a network of moving cytasters that represented ectoplasmic secondary centers of microtubule and actin filament nucleation. In some cases the network of cytasters persisted between the rings. The cytoskeleton had an outer actin layer and an inner microtubule layer that merged at the irregularly-shaped boundary zone. Bipolar translocation of the rings, meridional bands, or the network of cytasters led to accumulation of the cytoskeleton at both zygote poles. Translocation of the cytoskeleton was slowed or arrested by microinjected taxol or phalloidin, in a dose-dependent fashion. Results of drug treatment probably indicate differences in the degree and speed at which the cytoskeleton becomes stabilized. Moreover, drugs that selectively stabilized either microtubules or actin filaments stabilized and impaired movement of the entire cytoskeleton. Microtubule poisons and latrunculin-B failed to disrupt the cytoskeleton. It is concluded that the microtubule and actin cytoskeletons are dynamic, presumably cross-linked and resistant to depolymerizing drugs. They probably move along each other by a sliding mechanism that depends on the instability of microtubules and actin filaments.

Actin Cytoskeleton↗

PubMed1975

A multisomatic axon in the central nervous system of the leech.

There is one particularly large axon in the medial bundle of the nerve cord of the leech. It extends along the entire length of the cord and is connected to a single cell body in each ganglion. The cell bodies in adjacent ganglia are tightly electrically coupled, and dye injected into one cell body can diffuse along the axon and into the cell body of the next ganglion. If the nerve cord is cut between two ganglia, neither end of the axon degenerates. Repair of the axon appears to occur by end-to-end fusion.

Action Potentials↗

PubMed1977

The specificity of re-innervation by identified sensory and motor neurons in the leech.

Re-innervation of skin and muscle by identified sensory and motor neurons in segmental ganglia of the leech was studied using physiological techniques. After lesions of peripheral nerves, sensory axons which re-innervated the skin always regained sensitivity to their original stimulus modality (touch, pressure or noxious stimuli). Motor neurons invariably re-innervated the appropriate type of body wall muscle, such as longitudinal or circular muscle layers. Both sensory and motor axons usually returned to the appropriate region of the body wall (dorsal, lateral, or ventral) when regenerating after a nerve crush or cut. This capacity was lost, however, when growth along old nerve branches was prevented by evulsing long segments of the nerve. Re-innervation usually occurred by way of growth of new axons all the way to the periphery, but in a few cases reconnection with the surviving distal segment of the original axon had taken place. The specificity of re-innervation can be accounted for by a combination of selective growth along appropriate nerve branches and specific interactions with target tissues.

Action Potentials↗

PubMed1978

Structure of the leech nerve cord: distribution of neurons and organization of fiber pathways.

The abdominal nerve cord of the leech Macrobdella decora was studied under the light and electron microscopes. The ganglionic cortex consists of six hemicone-shaped packets of neuronal perikarya and apical processes regularly assembled in bilaterally symmetric rows. The orderly projection of the apical processes into the hilum of the packets is also followed by an orderly distribution of their branches across the neuropile. This part of the ganglion is made of two symmetrical halves or hemineuropiles enclosing two types of nerve tissue: coarse and fine neuropiles. The coarse neuropile has seven longitudinal and four commissural tracts of fibers and a distinctively segregated synaptic zone. Nerve processes in this neuropile mostly proceed from the neurons in the ganglia and some are the branches of giant afferent axons. The fine neuropile includes several longitudinal tracts of fibers and a non-segregated synaptic zone. Most nerve processes in this neuropile are small afferent axons and some come from neurons in the ganglia. Bundles of axons in the connectives result by the orderly projection of the neuropile longitudinal tracts and together form fiber pathways connecting the synaptic zones of successive ganglia. Pathways of through-ganglia giant axons, linking the coarse neuropile synaptic zones, and of small axons, linking the fine neuropile synaptic zones, are described.

Animals↗

PubMed1979

The morphological and physiological properties of a regenerating synapse in the C.N.S. of the leech.

Regeneration of an electrical synapse between particular interneurons in the medicinal leech was traced physiologically and morphologically using intracellular recording the horseradish peroxidase (HRP) injection. The synapse between S-cell interneurons lies in the connective midway between segmental ganglia, so crushing near one ganglion severs only one S-cell's axon. The severed distal stump remains connected to the adjacent uninjured S-cell and continues for weeks to conduct impulses. The injured cell regenerates, while its uninjured "target" neuron in the next ganglion does not grow. After the sprouts of the regenerating neuron cross the crush, one or a few branches grow along the surviving distal stump toward the original synapse. After about one month when the region of original synapse has been reached, regenerating neurons form electrical junctions and stop growing. Thereafter electrical coupling improves in stages. Within two months the regenerated neuron attains full caliber, the stump degenerates and function is normal. In some instances within days or weeks of crushing, the regenerating neuron forms a basket of synapses upon its severed distal stump and then continues growing to synapse with the target. When this occurs, electrical coupling and subsequent impulse transmission between S-cells rapidly resumes. These experiments indicated that the regenerating neuron is guided to its proper synaptic target by recognizing and following its severed distal stump. Sometimes the distal stump itself becomes an intermediate synaptic target.

Animals↗

PubMed1981

The structure, distribution, and quantitative relationships of the glia in the abdominal ganglia of the horse leech, Haemopis sanguisuga.

The glial cells in abdominal ganglia of the horse leech Haemopis sanguisuga were studied by electron microscopy and analysed quantitatively to evaluate the suitability of this easily obtainable carnivorous species for physiological studies. Each abdominal ganglion contains eight giant glial cells, 12,000-14,000 small glial cells, and approximately 300 neurons. The giant glial cells constituted 44.6% and the small glial cells 6.4% of the ganglion's volume. The giant glial cells contain glycogen and bundles of filaments that are chiefly located in their periphery, close to the neurons into which they send processes. The small glial cells are frequently surrounded by the giant glial cells but also occur around neuronal perikarya and axon tracts, as well as against the basal lamina and connective tissue layers. The small glial cells contain lysosomes and sometimes form a trophospongium with the neurons. A system of extracellular channels, which is continuous with the basal lamina, indents the giant glial cells and extends around parts of the neurons. The extracellular channels contain a matrix that appears very similar to the basal lamina and to the cytoplasm in the processes of the small glial cells. Some of the extracellular channels contain collagen fibrils. Hemidesmosomes join the matrix-filled extracellular channels to both the neurons and the giant glial cells. Ionic lanthanum has a free access to the neurons and glial cells via the extracellular spaces and matrix-filled channels. Areas of synaptic intermingling rarely contain glial cell processes.

Abdomen↗

PubMed1984

Axonal projections of mechanosensory neurons in the connectives and peripheral nerves of the leech, Haemopis marmorata.

The axonal projections of the seven mechanosensory neurons in the connectives and peripheral nerves were examined by horseradish peroxidase (HRP) injections. In the connective the closely functionally related mechanosensory neurons travel in two bilaterally symmetrical regions, which comprise less than 10% of the connective's cross-sectional area. This grouping may reflect the similar functional properties and synaptic connections of the cells. Serial sections through the neuropil-connective junction zone showed that the organization of the axons is independent of glial fasciculation. Fascicles are not rigid structures; they were found to part and fuse in a seemingly random manner. The glial cell seems therefore to have only a supportive structural function and not to play any role in axonal guidance or to define any specific nerve fascicles in the leech. The projections of the mechanosensory cells in the peripheral roots were not as stereotyped as in the connective. However, examination of the branching of the medial and lateral P cells in the posterior root showed that the roots are highly structured and that some axons may be confined to tracts which have specific positions related to the branching of the root. The possible role of the P cells in pioneering these tracts is discussed.

Animals↗

PubMed1984

Segmental variation in the arborization of identified neurons in the leech central nervous system.

Mechanosensory and motor neurons in the central nervous system of the leech have been examined by intracellular injection of horseradish peroxidase and electrophysiological mapping of their peripheral fields to determine how the arborizations of homologous cells are influenced by their segmental position. The branching patterns of annulus erector (AE) motoneurons in ganglia near the head and tail were found to be more extensive than those of cells in midbody ganglia. As in midbody ganglia, the peripheral fields of AE motoneurons in adjacent ganglia near the head and tail overlapped extensively, but the subfields innervated by individual branches of a single AE motoneuron showed little or no overlap. No AE motoneurons were found in the head ganglion or in the 20th and 21st free segmental ganglia. The branching pattern of touch-sensitive mechanosensory cells showed a similar segmental variation; touch cells in ganglia near the head and tail had more extensive arborizations than those in midbody ganglia. The rostrocaudal position along the cord at which the branching pattern changed from that characteristic of midbody ganglia to one with a more extensive arborization differed for different types of neurons. These findings demonstrate that a cell's pattern of arborization is not determined by a simple segmental difference between ganglia and suggest that during development neurons respond individually to cues that vary along the length of the cord.

Animals↗

PubMed1984

Selective loss of neurites during differentiation of cells in the leech central nervous system.

The arborizations of annulus erector (AE) motoneurons in the central nervous system of the leech, Hirudo medicinalis, have been examined during embryogenesis to determine how segmental differences in their branching patterns arise. Early in development AE motoneurons all along the ganglionic chain had a similar central arborization, with major branches extending both rostrally and caudally along the connectives that link adjacent ganglia. As the embryo grew, the processes in the connectives elongated but failed to increase significantly in caliber and eventually atrophied and were lost. This sequence of events did not occur uniformly along the cord, however. AE motoneurons in midbody ganglia lost both anterior and posterior branches, cells near the head lost only their posterior branch, while cells near the tail lost only their anterior branch. In this way, the selective atrophy of neurites during development produced a systematic segmental difference in the morphology of homologous cells.

Animals↗

PubMed1986

Segmental differentiation in the leech nervous system: the genesis of cell number in the segmental ganglia of Haemopis marmorata.

In hirudinid leeches, the segmental ganglia associated with the sexual organs contain several hundred more neurons than other midbody ganglia. To determine whether this difference arises by differential cell addition or by differential cell death, cell counts were made in several segmental ganglia during the course of embryonic and postembryonic development. The results show that all ganglia behave equally in early development. In each case, at least 10-20% more cells than will make up the adult complement of about 400 neurons is generated, and by about 20 days of embryonic development cell loss brings the number down to about 400 cells. By about 30 days, when animals emerge from their cocoons, additional cells have begun to appear in the sex ganglia. The number of extra cells continue to increase gradually over the next several months, until the adult number of 600-700 neurons is attained. These observations indicate that at least some segmental differences in the size of neuronal populations are due to differential cell proliferation and that these differences can arise quite late in the maturation of an animal.

Animals↗

PubMed1986

Development of segmental differences in the pressure mechanosensory neurons of the leech Haementeria ghilianii.

Using a monoclonal antibody specific for the pressure mechanosensory neurons (P cells) of the leech Haementeria ghilianii, we have examined the segmental differences between P cells in the adult nerve cord, as well as the development of these differences during embryogenesis. The standard segmental ganglion contains two pairs of P cells of about the same size and staining intensity. The sex ganglia appear to be missing the P cells that normally innervate ventral skin, and ganglia 20 and 21 have much smaller ventral P cells than most segments. The pattern of P cells in the head and tail ganglia also differs slightly from that of the standard ganglia. During embryogenesis, when the neurons are first stained by the antibody, there are two pairs of P cells of equal size in each segmental ganglion. Obvious segmental differences arise subsequently, modifying an initially identical set of cells.

Age Factors↗

PubMed1987

Transmitter localization and vesicle turnover at a serotoninergic synapse between identified leech neurons in culture.

An electron microscopic study has been made of chemical synapses that develop between identified nerve cells isolated from the CNS of the leech and maintained in culture. Structures resembling synapses were observed in pairs of Retzius cells and P sensory cells at which chemical transmission had been demonstrated by recording with microelectrodes. Vesicle recycling was shown by following the uptake of extracellular markers after stimulation. The membrane separation between the presynaptic Retzius cell (which is known to liberate serotonin) and the postsynaptic P cell was wider in synaptic than in extrasynaptic regions. The Retzius cell contained clusters of clear vesicles apposed to thickenings of the presynaptic membrane. These clear vesicle clusters were capped by a layer of dense core vesicles that did not contact the presynaptic membrane thickenings. Subsynaptic cisternae were found in the postsynaptic cell opposite the presynaptic membrane thickenings. Occasional slight postsynaptic membrane thickenings were seen. Extracellular material was observed within the synaptic cleft. Similar synaptic structures developed between pairs of Retzius cells in culture; even a single Retzius cell was able to form autapses upon itself. Structures resembling transmitter release sites were found in Retzius cells at a distance from any postsynaptic membranes. These are presumed to be locations for the diffuse release of transmitter. Presynaptic structures resembling release sites were never observed in P cells apposed to Retzius cells. Antibody to serotonin (5-HT) labelled with colloidal gold showed serotonin to be localized in the dense core vesicles in Retzius cells. Stimulation of pairs of Retzius and P cells by raised concentrations of K+ resulted in uptake of extracellular markers. Only Retzius cells became labelled. Ferritin was found in cisternae, in dense core vesicles, and in clear vesicles. HRP was found in cisternae and in clear vesicles. Colloidal gold was taken up by coated vesicles and was occasionally found in both clear and dense core vesicles. The uptake of extracellular markers following stimulation was blocked by high Mg++. These results show that structures develop between pairs of cells at which chemical transmission develops and that transmitter release leads to turnover of dense core and clear vesicles.

Animals↗

PubMed1991

Segmental differentiation in the leech central nervous system: proposed segmental homologs of the heart accessory neurons.

As part of an on-going study of segmental differentiation in the central nervous system (CNS) of the leech Hirudo medicinalis, a search was made for putative segmental homologs of the heart accessory (HA) neurons, which exist exclusively as a bilateral pair in the ganglia of the fifth and sixth body segments. As it is not yet feasible to obtain adequate cell lineage information in H. medicinalis, potential homologs of the HA neurons were determined using morphological, immunohistochemical, and electrophysiological criteria. Among cells in other body ganglia with somata in the same locations as HA neurons, a pair was found having extensive morphological and physiological similarities to HA neurons. These we have called HA-like (HAL) neurons. Adult HA and HAL neurons have closely related patterns of primary branching, in terms of shape, intraganglionic pathways taken, and extraganglionic projections. The number, location, and relative thickness of branches are also similar among these cells. In embryos 10 to 11 days old, HA and HAL neurons have virtually identical branching patterns, with primary and secondary branches of nearly uniform caliber. Differences in branch thickness develop gradually; by embryonic day 20, they resemble those found in adult neurons. Two features found to differ between HA and HAL neurons were the cell body diameter (larger for the HA cells) and the expression of antigens recognized by the monoclonal antibody Laz1-1 (absent at a detectable level in the HA neurons). At a physiological level, the HA and HAL neurons showed action potentials of similar size and shape, as well as inhibitory synaptic inputs from a common source, the heart interneurons (HN). The observations presented here suggest that there is a common developmental origin for the HA and HAL neurons, and hence that their fates are positionally determined by as yet unknown factors.

Aging↗

PubMed1988

Direct effects of carbachol on membrane potential and ion activities in leech glial cells.

Ion-selective double-barreled microelectrodes were used to measure the activities of intracellular K+ and Na+ (aKi, aNai) and the membrane potential (Em) in neuropile glial cells as well as extracellular K+ (aKe) in the neuropile of segmental ganglia in the leech, Hirudo medicinalis. Bath-application of carbachol resulted in a prominent membrane depolarization. This depolarization was accompanied by transient increases of aNai and aKe, whereas aKi decreased. It is suggested that the carbachol-induced depolarization and the underlying ion activity changes are due to activation of an acetylcholine receptor-coupled cation channel in the membrane of the neuropile glial cells.

Animals↗