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Dynamics of Thin Filopodia

  After work published in Jeffrey Miller, Scott E. Fraser and David McClay (1995), Dynamics of thin filopodia during sea urchin gastrulation, Development 121: 2501-2511.
   
  Background Information
Sea urchins are favorite organisms to study gastrulation because their early embryos are transparent, and we can watch what's going on during this important phase of development. Gastrulation begins in earnest with the ingression of primary mesenchyme cells in the center of the vegetal plate. Once inside the blastocoel, they migrate by extending filopodia. After a period of migration, they organize into a ring in the vegetal half of the blastocoel; they fuse to form a syncytium that secretes the skeleton of spicules. When primary mesenchyme cells begin to migrate, remaining cells of the vegetal plate invaginate to form the archenteron (future gut). The archenteron elongates by convergent extension. While archenteron elongation is still under way, another group of mesenchyme cells at the tip of the archenteron becomes motile and extends filopodia. These are the secondary mesenchyme cells; their filopodia contact and pull the archenteron to the ectoderm of the future mouth. The dimensions of the filopodia of migrating primary mesenchyme cells and secondary mesenchyme cells pulling the tip of the archenteron are 1 Ám, or more, in diameter.

The authors used Nomarski differential interference contrast microscopy and electronic image enhancement to capture the following sequences. These sequences show that there are thin filopodia (0.2 - 0.4 Ám in diameter) extending from, and to, primary mesenchyme cells, ectodermal cells, and secondary mesenchyme cells. These thin filopodia don't seem to be used for locomotion. Rather, they appear to assess their environment like the thin filopodia seen at the tips of axon growth cones.

 

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Miller Fig. 1

  Labeled diagram of sea urchin embryo at midgastrula stage for reference when you view sequences.
After Fig. 1 in Miller, J., et al., Development 121: 2501-2511 (1995).
 

Images collected at 1 frame/second.

GENERAL FILOPODIAL DYNAMICS

  Miller 01 Primary mesenchyme cells in subequatorial ring send thin filopodia along the basal surface of ectodermal cells.

QuickTime (359 K)

     
 

FILOPODIAL GROWTH
(Extension of thin filopodia occurs at a rate of 8.6±3.6 Ám/minute.)

  Miller 02 Primary mesenchyme cells in subequatorial ring extending filopodia. A middle primary mesenchyme cell extends a filopod which kinks several times then appears to begin retracting.

QuickTime (495 K)

  Miller 03 Primary mesenchyme cell in subequatorial ring extending a filopod.

QuickTime (258 K)

  Miller 04 Primary mesenchyme cell extending a thin filopod. Notice the membrane flow which moves toward the cell body. A migrating pigment cell displays blebbling behavior (lower left).

QuickTime (413 K)

     

FILOPODIAL RETRACTION
(Retraction of thin filopodia occurs at a rate of 11.4±5.1 Ám/minute.)

  Miller 05 Primary mesenchyme cell in subequatorial ring resorbs a thin filopod. Notice how the filopod kinks just prior to and during retraction.

QuickTime (259 K)

  Miller 06 Filopod of a primary mesenchyme cell retracting.

QuickTime (287 K)

     

CELL-CELL INTERACTIONS MEDIATED BY THIN FILOPODIA

PRIMARY MESENCHYME CELL MIGRATION

  Miller 07 Primary mesenchyme cells during their migratory phase extend small, short-lived filopodia that may contact the ectoderm or other primary mesenchyme cells as they assemble into the subequatorial ring.

QuickTime (527 K)

  Miller 08 Migrating primary mesenchyme cell sends out two filopodia that contact ectodermal cells. Primary mesenchyme cells may use filopodia to gather positional information that will determine the site(s) of spiculogenesis.

QuickTime (645 K)

     

PRIMARY MESENCHYME CELL-ECTODERM INTERACTIONS
(exchange of skeletal patterning cues)

  Miller 09 Primary mesenchyme cell-ectoderm interactions occur after the subequatorial ring forms, during the time the spicules grow. The filopodia may enable primary mesenchyme cells to survey their environment, gathering positional information that specifies skeletal morphology.

QuickTime (699 K)

  Miller 10 More primary mesenchyme cell-ectoderm interactions. This sequence also shows an ectodermal cell extending a short, stubby filopod (lower center). This behavior can also be seen in some of the other sequences.

QuickTime (391 K)

  Miller 11 A very long primary mesenchyme cell filopod contacting and ectodermal cell at the animal pole. The amazing length of the thin filopod allows a primary mesenchyme cell to interact with cells at any other position within the embryo.

QuickTime (521 K)

     

SECONDARY MESENCHYME CELL-ECTODERM INTERACTIONS

  Miller 12 A secondary mesenchyme cell extends a filopod that rapidly becomes a lamellapod. Secondary mesenchyme cells display a much wider range of filopod/lamellopod morphologies than primary mesenchyme cells.

QuickTime (402 K)

     

PRIMARY MESENCHYME CELL-SECONDARY MESENCHYME CELL INTERACTIONS

  Miller 13 A primary mesenchyme cell extends a filopod that contacts a secondary mesenchyme cell, bends and then retracts.

QuickTime (468 K)

  Miller 14 Extensive cell-cell interactions between secondary mesenchyme cells (to the left) and primary mesenchyme cells (to the right) occur throughout gastrulation. These direct interactions may be used to communicate cell fate information that suppresses the ability of secondary mesenchyme cells to convert to primary mesenchyme cell fate.

QuickTime (1.6 MB)

     
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