The oblique muscle organizer in Hirudo medicinalis, an identified embryonic cell projecting multiple parallel growth cones in an orderly array

Jellies, John; Kristan, William B.

doi:10.1016/0012-1606(91)90342-z

Cited by 54 publications

(46 citation statements)

References 90 publications

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“…Studies of the comb cell in leech have identified LAR as a mediator of self-recognition and/or repulsion. Comb cells are transient cells that may serve as a scaffold for muscle cells (Jellies and Kristan 1991). These cells possess numerous parallel extensions with regular spacing between them (Baker and Macagno 2007).…”

Section: Mechanisms Of Self-avoidancementioning

confidence: 99%

“…However, the principles regulating process spacing in these regions likely also apply in three dimensions, most prominently where processes are segregated into nonoverlapping domains or columns (Huckfeldt et al 2009). It is also notable that nonneuronal cell types might similarly engage in selfavoidance and form tiling arrangements, including leech comb cells (Jellies and Kristan 1991) and mammalian astrocytes (Bushong et al 2002;Ogata and Kosaka 2002;Livet et al 2007). Elucidating the mechanisms of process spacing during development is therefore relevant for understanding principles of tissue organization inside and outside of the nervous system.…”

mentioning

confidence: 99%

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Self-avoidance and Tiling: Mechanisms of Dendrite and Axon Spacing

Grueber¹,

Sagasti²

2010

Cold Spring Harbor Perspectives in Biology

149

148

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The spatial pattern of branches within axonal or dendritic arbors and the relative arrangement of neighboring arbors with respect to one another impact a neuron's potential connectivity. Although arbors can adopt diverse branching patterns to suit their functions, evenly spread branches that avoid clumping or overlap are a common feature of many axonal and dendritic arbors. The degree of overlap between neighboring arbors innervating a surface is also characteristic within particular neuron types. The arbors of some populations of neurons innervate a target with a comprehensive and nonoverlapping "tiled" arrangement, whereas those of others show substantial territory overlap. This review focuses on cellular and molecular studies that have provided insight into the regulation of spatial arrangements of neurite branches within and between arbors. These studies have revealed principles that govern arbor arrangements in dendrites and axons in both vertebrates and invertebrates. Diverse molecular mechanisms controlling the spatial patterning of sister branches and neighboring arbors have begun to be elucidated.

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Section: Mechanisms Of Self-avoidancementioning

confidence: 99%

mentioning

confidence: 99%

Self-avoidance and Tiling: Mechanisms of Dendrite and Axon Spacing

Grueber¹,

Sagasti²

2010

Cold Spring Harbor Perspectives in Biology

149

148

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“…In this series of images, and in the corresponding movie (see movie in Supplemental data online), the diagonal processes of the contralateral CC homolog were also dyefilled. As previously described (Jellies and Kristan, 1991), older CC processes extended rapidly. Out of eight timelapse series made from embryos at E11 or older, growth cones were seen to advance almost three times faster than those from embryos just 1 day younger, with an average rate of 12.21 Ϯ 1.24 m/h.…”

Section: Late Comb Cell Dynamicsmentioning

confidence: 68%

“…When a single CC was deleted early in development, the remaining adjacent homologs expanded to occupy the vacated territory and the interprocess distance increased (Jellies and Kristan, 1991). Such competitive interactions, either within a cell's own arbor or between neighboring neurons, has been described for peripheral sensory arbors of leech and fly embryos (Blackshaw et al, 1982;Gan and Macagno, 1997;Grueber et al, 2003), zebrafish peripheral sensory arbors (Sagasti et al, 2005), and some types of mammalian retinal cells (e.g., Perry and Linden, 1982;Lin et al, 2004).…”

Section: Indexing Terms: Pathfinding; Development; Filopodial Retractmentioning

confidence: 95%

“…As mentioned above, when a single CC was ablated early enough in development there was an expansion of the neighboring, undamaged cell's processes into the vacated territory (Jellies and Kristan, 1991). This expansion was suggested to result from a specific avoidance process whereby the parallel, nonoverlapping arrays of the CCs may be established.…”

Section: Ablation Leads To Filopodial Lengthening and Branch Formamentioning

confidence: 95%

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In vivo imaging of growth cone and filopodial dynamics: Evidence for contact‐mediated retraction of filopodia leading to the tiling of sibling processes

Baker

Macagno

2006

J of Comparative Neurology

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In the leech embryo, the peripheral comb cell (CC) sends out many nonoverlapping, growth cone-tipped processes that grow in parallel and serve as a scaffold for the migrating myocytes of the later-developing oblique muscle layer. To explore how the parallel arrangement is generated we first examined the arrangement of CC cytoskeletal components by expressing a tubulin-binding protein and actin, both tagged with fluorescent reporters. This revealed that the growth cones were compartmentalized into F-actin-rich filopodia and a microtubule-rich central region. Time-lapse analysis with a 2-photon laser scanning microscope revealed that the growth cones of the CC are highly dynamic, undergoing rapid filopodial extension and retraction. Measurements of filopodial lifespan and length revealed that most filopodia at the leading edge of the growth cone achieved significantly longer lifespans and length than lateral filopodia. Furthermore, for the short-lived lateral filopodia, apparent interaction with a neighboring process was found to be a significant predictor of their nearly immediate (within 2-4 minutes) retraction. When contact was experimentally prevented by ablating individual CCs, the filopodia from the growth cones of adjacent segmental neighbors were found to be significantly lengthened in the direction of the removed homolog. Treatment with low doses of cytochalasin D to disrupt F-actin assembly led to filopodial retraction and growth cone collapse and resulted in the bifurcation of many CC processes, numerous crossover errors, and the loss of parallelism. These findings indicate the existence of a contact-mediated repulsive interaction between processes of the CC.

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Initial formation and secondary condensation of nerve pathways in the medicinal leech

1996

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Invertebrates have proved to be important experimental systems for examining questions related to growth cone navigation and nerve formation, in large part because of their simpler nervous systems. However, such apparent simplicity can be deceiving because the final stereotyped patterns may be the result of multiple developmental mechanisms and not necessarily the sole consequence of the pathway choices of individual growth cones. We have examined the normal sequence of events that are involved in the formation of the major peripheral nerves in leech embryos by employing (1) an antibody directed against acetylated tubulin to label neurons growing out from the central nervous system, (2) the Lan3-2 antibody to label a specific population of peripheral neurons growing into the central nervous system, and (3) intracellular dye filling of single cells. We found that the mature pattern of nerves was characterized by a pair of large nerve roots, each of which branched into two major tracts. The earliest axonal projections did not, however, establish this pattern definitively. Rather, each of the four nerves initially formed as discrete, roughly parallel tracts without bifurcation, with the final branching pattern of the nerve roots being generated by a secondary condensation. In addition, we found that some of the nerves were pioneered in different ways and by different groups of neurons. One of the nerves was established by central neurons growing peripherally, another by peripheral neurons growing centrally. These results suggest that the formation of common nerves and neuronal pathfinding in the leech involves multiple sets of growth cone guidance strategies and morphogenetic mechanisms that belie its apparent simplicity.

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The oblique muscle organizer in Hirudo medicinalis, an identified embryonic cell projecting multiple parallel growth cones in an orderly array

Cited by 54 publications

References 90 publications

Self-avoidance and Tiling: Mechanisms of Dendrite and Axon Spacing

Self-avoidance and Tiling: Mechanisms of Dendrite and Axon Spacing

In vivo imaging of growth cone and filopodial dynamics: Evidence for contact‐mediated retraction of filopodia leading to the tiling of sibling processes

Initial formation and secondary condensation of nerve pathways in the medicinal leech

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