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PubMed2003

A hedgehog homolog regulates gut formation in leech (Helobdella).

Signaling by the hedgehog (hh)-class gene pathway is essential for embryogenesis in organisms ranging from Drosophila to human. We have isolated a hh homolog (Hro-hh) from a lophotrochozoan species, the glossiphoniid leech, Helobdella robusta, and examined its expression by reverse transcription polymerase chain reaction (RT-PCR) and whole-mount in situ hybridization. The peak of Hro-hh expression occurs during organogenesis (stages 10-11). No patterned expression was detected within the segmented portion of the germinal plate during the early stages of segmentation. In stage 10-11 embryos, Hro-hh is expressed in body wall, foregut, anterior and posterior midgut, reproductive organs and in a subset of ganglionic neurons. Evidence that Hro-hh regulates gut formation was obtained using the steroidal alkaloid cyclopamine, which specifically blocks HH signaling. Cyclopamine induced malformation of both foregut and anterior midgut in Helobdella embryos, and no morphologically recognizable gonads were seen. In contrast, no gross abnormalities were observed in the posterior midgut. Segmental ectoderm developed normally, as did body wall musculature and some other mesodermal derivatives, but the mesenchymal cells that normally come to fill most of the coelomic cavities failed to develop. Taken with data from Drosophila and vertebrates, our data suggest that the role of hh-class genes in gut formation and/or neural differentiation is ancestral to the bilaterians, whereas their role in segmentation evolved secondarily within the Ecdysozoa.

Amino Acid Sequence↗
PubMed2003

A distinct patterning mechanism of O and P cell fates in the development of the rostral segments of the leech Helobdella robusta: implications for the evolutionary dissociation of developmental pathway and morphological outcome.

Despite a high degree of homonomy in the segmental organization of the ectoderm, the body plan of the leech is divided into two zones based on the distinct cell lineage patterns that give rise to the O/P portion of the segmental ectoderm. In the midbody and caudal segments, each segmental repeat of ectoderm arises in part from one 'o' blast cell and one 'p' blast cell. These two blast cells are positionally specified to distinct O and P fates, and give rise to differentiated descendant cells called O and P pattern elements, respectively. In the rostral segments, each segmental repeat of O and P pattern elements arises from a single 'op' blast cell. Based on their developmental fates and their responses to the ablation of neighboring cells, the granddaughters of the primary op blast cell are categorized into two O-type cells and two P-type cells. The O-type cells do not require the presence of the rest of the op blast cell clone for their normal development. By contrast, normal development of the P-type cells depends upon interactions with the other OP sublineages. Additional experiments showed that the O-type cells are the source of a repressive signal involved in the normal fate specification of the P-type cells. Our data suggest that the cell interactions involved in fate specification differ substantially in the rostral and midbody segments, even though the set of differentiated descendants produced by the rostral OP pathway and the midbody O and P pathways are very similar.

Animals↗
PubMed1988

Segmentation in leech development.

Segments in glossiphoniid leeches, such as Helobdella triserialis, are the products of sterotyped cell lineages that yield identifiable cells from first cleavage. Cell lines generating segmental tissues are separated from those generating prostomial tissues early in development. Segments arise from five bilateral pairs of longitudinal columns of primary blast cells that are generated by five bilateral pairs of embryonic stem cells called teloblasts. There are four ectodermal cell lines (N, O, P and Q) and one mesodermal cell line (M) on each side of the embryo. In normal development, each cell line generates a segmentally iterated set of identified definitive progeny comprising a mixture of cell types. In the M, O and P cell lines, each blast cell generates one segment's worth of definitive progeny (segmental complement). But the clones of blast cells in each of these three cell lines interdigitate longitudinally with cells of the adjacent clones from the same line, so that the clone of an individual m, o and p blast cell is distributed across more than one segment. Thus, there is no simple clonal basis for morphologically defined segments. In the N and Q cell lines, two blast cells are required to produce one segmental complement of definitive progeny; in each of these two cell lines, two classes of blast cells (nf and ns, qf and qs) are produced in exact alternation. Primary n and q blast cells are about the same size and are produced at the same rate as blast cells for the o and p bandlets, but the longitudinal extent of their clones is roughly half that of the o and p blast cells' clones.(ABSTRACT TRUNCATED AT 250 WORDS)

Animals↗
PubMed1991

Positional cues governing cell migration in leech neurogenesis.

The stereotyped distribution of identified neurons and glial cells in the leech nervous system is the product of stereotyped cell migrations and rearrangements during embryogenesis. To examine the dependence of long-distance cell migrations on positional cues provided by other tissues, embryos of Theromyzon rude were examined for the effects of selective ablation of various embryonic cell lines on the migration and final distribution of neural and glial precursor cells descended from the bilaterally paired ectodermal cell lines designated q bandlets. The results suggest that neither the commitment of q-bandlet cells to migrate nor the general lateral-to-medial direction of their migration depend on interactions with any other cell line. However, the ability of the migrating cells to follow their normal pathways and to find their normal destinations does depend on interactions with cells of the mesodermal cell line, which appears to provide positional cues that specify the migration pathways.

Animals↗
PubMed1992

Cytoplasmic and cortical determinants interact to specify ectoderm and mesoderm in the leech embryo.

In leech embryos, segmental ectoderm and mesoderm are produced by a pair of sister cells located near the animal and vegetal poles, respectively. We have investigated the mechanism that localizes ectodermal and mesodermal fates along the animal-vegetal axis. The results of cleavage arrest and cell ablation experiments suggest that the full range of normal cell interactions are not required for this process. However, when the animal and vegetal hemispheres are separated by re-orientation of the first cleavage plane from meridional to equatorial, the ectodermal fate co-segregates with the animal hemisphere and the mesodermal fate with the vegetal hemisphere. Two pools of yolk-deficient cytoplasm, called teloplasm, are located at the animal and vegetal poles of the zygote, but separation of the animal and vegetal teloplasms is not sufficient for the segregation of ectodermal and mesodermal fates. Rather, complete segregation of fates requires an equatorial cleavage orientation that separates not only the two teloplasms, but also the animal and vegetal cortical regions. This, in conjunction with previous findings, indicates that ectodermal determinants are localized to the cell cortex in the animal hemisphere of the zygote. We propose that these determinants segregate to the ectodermal precursor and interact with factors in teloplasm to transform the fate of this cell from a mesodermal ground state to ectoderm.

Animals↗
PubMed1993

Cell lineage analysis of the expression of an engrailed homolog in leech embryos.

ht-en is an engrailed-class gene that is expressed during early development and neurogenesis in embryos of the leech Helobdella triserialis. During the early development of this annelid (stages 7-9), ht-en is expressed in each of the ectodermal and mesodermal teloblast lineages that contributes progeny to the definitive segments. ht-en is expressed transiently by individually identified cells within the segmentally iterated primary blast cell clones. Its expression is correlated with the age of the primary blast cell clone. After consegmental primary blast cell clones from the different teloblast lineages have come into segmental register, cells that express ht-en during stages 7-9 are clearly confined to a transverse region corresponding to the posterior portion of the segmental anlage, but not all cells within this region express ht-en. Only a minority of the identified cells that express ht-en during terminal differentiation of the segmental ganglia and body wall (stages 10-11) are descendants of cells that express ht-en in early development (stages 7-9).

Animals↗
PubMed1995

Target-induced neurogenesis in the leech CNS involves efferent projections to the target.

During a critical period in leech embryogenesis, the sex nerves that connect the 5th and 6th midbody ganglia (MG5 and MG6) to the primordium of the male sexual organ carry a spatially localized signal that induces the birth of several hundred neurons specific to these ganglia. We examined particular cellular elements (afferents, efferents, non-neuronal components) within these nerves as potential conveyors of the inductive signal. We show that axons of peripheral sensory neurons in the male genitalia travel along the sex nerves and into MG5 and MG6, but reach the CNS after the critical period has elapsed and cannot, therefore, be involved in the induction. Of the six sex nerves, four contain non-neuronal cells that span the entire distance between the male genitalia and the sex ganglia. However, when male genitalia were transplanted to ectopic locations close to MG6, induction occurred frequently but only in MG6, mediated by ectopic nerves that do not contain these cells. Thus, non-neuronal cells specific to the normal sex nerves are not necessary for induction. In addition, dye injections into the target during the critical period failed to reveal migrating cells in the sex nerves that could convey the inductive signal to the CNS. Finally, we show that 11 pairs of central neurons in each ganglion project to the male organ early during the critical period. In the adult, at least 3 additional pairs of neurons in MG6 also innervate this target. We conclude that the only components of the sex nerves that connect the sex ganglia to the target during the critical period that could be associated with induced central mitogenesis are the axons of central neurons that innervate the male genitalia.

Animals↗
PubMed1996

Unequal cleavage in leech embryos: zygotic transcription is required for correct spindle orientation in subset of early blastomeres.

Leech embryos undergo invariant sequences of equal and unequal cell divisions to give rise to identifiable progeny cells. While many of the early cleavages are under maternal control, the divisions of a subset of early blastomeres (the large cells of the D' lineage) are perturbed after the inhibition of zygotic transcription. Analysis of the different types of cells produced in embryos injected with the transcriptional inhibitor, alpha-amanitin, revealed that the symmetry of cell division is perturbed in these large D'-derived cells during this early period of development. These cells, which would normally undergo a series of equal and unequal cleavages, always undergo equal cleavages after the inhibition of zygotic transcription. It appears that zygotically transcribed gene product(s) are required in the large cells of the D' lineage to orient the mitotic spindles properly for these unequal cell cleavages.

Amanitins↗
PubMed1999

Inductive regulation of cell fusion in leech.

Cell-cell fusion is a component of many different developmental processes, but little is known about how cell-cell fusion is regulated. Here we investigate the regulation of a stereotyped cell-cell fusion event that occurs among the endodermal precursor cells of the glossiphoniid leech Helobdella robusta. We find that this fusion event is regulated inductively by a cell that does not itself fuse. We also show that biochemical arrest (by microinjection with ricin A chain or ribonuclease A) of the inducer or either of the fusion partners prevents fusion, but only if the arrest is initiated during a critical period long before the time at which fusion normally occurs. If the arrest occurs after this critical period, fusion occurs on schedule. These results suggest that both fusion partners play active roles in the process and that neither the induction nor the fusion itself requires concomitant protein synthesis.

Animals↗
PubMed2006

Beyond the central pattern generator: amine modulation of decision-making neural pathways descending from the brain of the medicinal leech.

The biological mechanisms of behavioral selection, as it relates to locomotion, are far from understood, even in relatively simple invertebrate animals. In the medicinal leech, Hirudo medicinalis, the decision to swim is distributed across populations of swim-activating and swim-inactivating neurons descending from the subesophageal ganglion of the compound cephalic ganglion, i.e. the brain. In the present study, we demonstrate that the serotonergic LL and Retzius cells in the brain are excited by swim-initiating stimuli and during spontaneous swim episodes. This activity likely influences or resets the neuromodulatory state of neural circuits involved in the activation or subsequent termination of locomotion. When serotonin (5-HT) was perfused over the brain, multi-unit recordings from descending brain neurons revealed rapid and substantial alterations. Subsequent intracellular recordings from identified command-like brain interneurons demonstrated that 5-HT, especially in combination with octopamine, inhibited swim-triggering neuron Tr1, as well as swim-inactivating neurons Tr2 and SIN1. Although 5-HT inhibited elements of the swim-inactivation pathway, rather than promoting them, the indirect and net effect of the amine was a reliable and sustained reduction in the firing of the segmental swim-gating neuron 204. This modulation caused cell 204 to relinquish its excitatory drive to the swim central pattern generator. The activation pattern of serotonergic brain neurons that we observed during swimming and the 5-HT-immunoreactive staining pattern obtained, suggest that within the head brain 5-HT secretion is massive. Over time, 5-HT secretion may provide a homeostatic feedback mechanism to limit swimming activity at the level of the head brain.

Adrenergic alpha-Agonists↗
PubMed1984

Calcium-dependent action potentials in leech giant salivary cells.

Two pairs of discrete salivary glands are located at the base of the muscular proboscis of the sanguivorous Glossiphoniid leeches Haementeria ghilianii and Haementeria officinalis. Each anterior gland is 0.8 cm to 2 cm in length, and comprises over 200 giant salivary cell bodies ranging from 150 microns to over 1000 microns in diameter, depending on the size of the animal. The salivary cells are neither electrically nor dye coupled, and there is no acinar structure or common duct, but instead each cell extends an individual ductule. The cells fire action potentials of 100-200 ms duration and 70-100 mV amplitude in response to depolarizing pulses, or at the cessation of a hyperpolarizing pulse. The impulse is abolished by procedures known to antagonize calcium currents, and persists in sodium-free solution, or when calcium is replaced with strontium or barium. Our results support the hypothesis of a purely calcium-dependent impulse.

Action Potentials↗
PubMed1986

Swim initiation in the leech by serotonin-containing interneurones, cells 21 and 61.

Two pairs of serotonin-containing neurones, designated cells 21 and 61, were characterized physiologically and anatomically in the hirudinid leeches Macrobdella decora and Hirudo medicinalis. Both of these cells are bilaterally paired interneurones and each cell is weakly electrically coupled to the other serotonin-containing cells both intra- and interganglionically. Cells 21 and 61 are excited polysynaptically by individual identified mechano-sensory neurones. Segmental nerve shock sufficient to elicit an episode of swimming strongly excites cells 21 and 61, which then tend to generate bursts of impulses that are phase-locked to the swim motor pattern. Intracellular stimulation of either cell 21 or cell 61 often causes the initiation of swimming, acting in parallel with the nonserotonergic swim-initiator cell 204. Cells 61 and 204 are also weakly electrically coupled. The latency to swim onset by stimulating cell 21 or 61 is similar to that of cell 204 and different from that of the serotonergic Retzius cell. This result, with those in the accompanying paper (Nusbaum, 1986), suggests that unlike the Retzius cell and similar to cell 204, cells 21 and 61 synaptically contact cells of the swim central pattern generator (CPG).

Animals↗
PubMed1986

Synaptic basis of swim initiation in the leech. III. Synaptic effects of serotonin-containing interneurones (cells 21 and 61) on swim CPG neurones (cells 18 and 208).

Serotonin-containing cells 21 and 61 strongly excite a swim central pattern generator (CPG) neurone, cell 208, in nearby segmental ganglia in the leech Macrobdella decora. This excitatory effect is apparently independent of activity in the swim-initiating neurone cell 204, which monosynaptically excites cell 208 (Weeks, 1982b). Cell 208 excites cell 21, apparently directly. This is the first identified direct pathway for feedback from the swim central pattern generator to a swim initiator neurone. Focally applied serotonin has no effect on the soma of cell 208, but causes both excitatory and inhibitory responses in cell 208 when applied to different places within the neuropile. Cell 61 polysynaptically excites distant, posterior cells 208. This excitation is mediated at least in part by the activation of nearby cells 208, which polysynaptically excite posterior cells 208. Cell 208 is dye-coupled intraganglionically to a newly identified pair of neurones, designated cells 18. Cell 208 also excites posterior cells 18, apparently directly. This interaction may be the pathway whereby cell 61 polysynaptically excites posterior cells 208. During swimming, cell 18's membrane potential oscillates in phase with cell 208. Intracellular current injection into cell 18 during swimming perturbs the swim motor pattern. Therefore, cell 18 qualifies as a candidate swim CPG neurone.

Animals↗
PubMed1986

Influence of oxygen on the heartbeat rhythm of the leech.

Raising and lowering the oxygen content in the fluid bathing the skin of the leech modified the frequency of the heartbeat. In raised concentrations of oxygen, the period between bursts of impulses in the heart excitor motoneurones (HE cells) was reduced. Conversely, with lowered oxygen concentrations bathing the skin, the heart rate was slowed, with longer periods between bursts of firing in the HE motoneurones. Changes in oxygen concentration did not affect HE motoneurone firing patterns in preparations in which the CNS was dissected from the skin and surrounding body tissues. Various other stimuli were tried, including stroking, pinching, stretching the skin, blood vessels and gut, as well as changing the temperature. None of these stimuli mimicked the specific effects of oxygen on rhythmicity. It is concluded that peripheral receptors sensitive to changes in oxygen tension are able to influence the central neuronal circuits responsible for generating the rhythm of the heartbeat.

Animals↗
PubMed1986

Cholinergic action on the heart of the leech, Hirudo medicinalis.

Experiments were performed to determine the role of acetylcholine (ACh) in neuromuscular transmission in the heart of the leech Hirudo medicinalis. Superfused or iontophoretically applied ACh rapidly depolarized both isolated heart muscle cells and muscle cells in isolated hearts in a dose-dependent manner. the depolarization was associated with a conductance increase of the muscle membrane that had a reversal potential of -9 mV. Eserine potentiated the response to superfused ACh, reducing the threshold from 10(-6) to 10(-8) mol l-1. Acetylcholinesterase was localized histochemically to be in the immediate area of neuromuscular terminals. Superfused nicotinic agonists mimicked the effects of ACh, while superfused nicotinic antagonists reversibly blocked the iontophoretic response of heart muscle fibres to ACh. 5 X 10(-7) mol l-1 curare, 5 X 10(-5) mol l-1 nicotine and 1 X 10(-4) mol l-1 atropine reduced the iontophoretic response to half its original amplitude. Alpha-bungarotoxin did not block the response of heart muscle cells to iontophoretically applied ACh. Curare was used to determine whether the neurones that innervate the heart-HE motor neurones and HA modulatory neurone--use ACh as a neuromuscular transmitter. The fast depolarizing component of the HE cell's neuromuscular transmission was reversibly blocked by 10(-4) mol l-1 curare, while the HA cell's modulatory effects on the heart were apparently unaffected by 10(-4) mol l-1 curare. Our results indicate that heart muscle cells have nicotinic acetylcholine receptors that open in the presence of ACh, thereby increasing membrane conductance. The HE motor neurone is probably cholinergic and engages these receptors in its neuromuscular transmission, while the HA modulatory neurone is probably not cholinergic.

Acetylcholine↗
PubMed1989

Depression of excitatory motoneurones by a single neurone in the leech central nervous system.

Intracellular staining techniques have been used to characterize the morphology of a newly identified neurone, cell 151, in the segmental ganglia of the leech. This neurone ramifies extensively within the neuropile and sends multiple extensions into roots and connectives. Strong dye coupling and non-rectifying electrical coupling were observed between the contralateral homologues. No action potentials were recorded from the cell body, but postsynaptic potentials and slow potential changes (greater than 1 s, greater than 15 mV) were observed. Upon injection of hyperpolarizing currents, the efferent spike activity, recorded extracellularly, was depressed in both the ipsi- and the contralateral roots of the ganglion. The depression was gradual and non-adapting and occurred reliably only within the ganglion where cell 151 is situated. Depolarization of cell 151 was without consequence for the tonic firing of isolated ganglia. Many identified excitatory motoneurones follow the hyperpolarization of cell 151. Currents can be exchanged between cell 151 and motoneurones via rectifying electrical synapses. Spontaneous hyperpolarizations of cell 151 were correlated with depression of spike frequencies, recorded in whole nerves as well as in identified motoneurones. The membrane potential of cell 151 was drastically altered by bursts from mechanosensory cells. The ability of cell 151 to distribute inhibition onto a great number of motoneurones and to curtail excessive neuronal activity is discussed.

Animals↗
PubMed1989

Presynaptic calcium currents and facilitation of serotonin release at synapses between cultured leech neurones.

1. The role of presynaptic Ca2+ entry in facilitation of transmitter release has been analysed by voltage-clamp measurements at synapses formed in culture by Retzius and P neurones isolated from the central nervous system (CNS) of the leech. The transmitter released by Retzius cells is serotonin. 2. Synaptic transmission persisted in solutions containing raised concentrations of divalent cations, reduced concentrations of Na+, and tetraethylammonium (TEA+) and 4-AP (to block K+ currents). Ca2+ and Sr2+ were more effective in promoting transmitter release than Ba2+, as assessed by the postsynaptic potentials in P cells. The degree and time course of facilitation in Ca2+- and Sr2+-containing solutions were similar to those observed for synapses bathed in normal L-15 medium. 3. Transmitter release depended upon the amplitude and the duration of presynaptic depolarization and inward Ca2+ current. Peak Ca2+ currents and postsynaptic potentials occurred with depolarizing steps to +15 mV. Frequent or prolonged pulses depressed the postsynaptic potentials. 4. Pairs of depolarizing pulses that caused facilitation were accompanied by identical inward Ca2+ currents. These results indicate that the mechanism responsible for facilitated serotonin release must occur following Ca2+ entry and that residual Ca2+ plays a role.

4-Aminopyridine↗
PubMed1990

Reduction in extrasynaptic acetylcholine sensitivity of axotomized anterior pagoda neurones in the leech.

1. The effects of axotomy on the sensitivity of the leech anterior pagoda (AP) neurone to acetylcholine (ACh) and carbamylcholine (CCh) have been studied 1-5 days after axon interruption. 2. Hyperpolarizing responses to ionophoretically applied ACh and CCh have been recorded intracellularly from desheathed cell bodies of normal and axotomized neurones. The electrical properties of the membrane have also been measured in the same neurones. 3. Axotomy produced a progressive loss of sensitivity to both ACh and CCh with a similar percentage reduction. 4. No significant changes have been found in the time to peak and in the reversal potential of the responses to agonists, or in the number of drug molecules needed to combine with a single receptor to produce a response. 5. Interruption of nerve roots and connectives which do not contain the AP axon did not induce the alterations of ACh sensitivity observed after axotomy. 6. It is concluded that the loss of ACh sensitivity following axotomy is due to a reduction in density of functional ACh receptors (AChRs).

Acetylcholine↗