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WIREs Dev Biol
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Gonad morphogenesis and distal tip cell migration in the Caenorhabditis elegans hermaphrodite

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Abstract Cell migration and morphogenesis are key events in tissue development and organogenesis. In Caenorhabditis elegans, the migratory path of the distal tip cells determines the morphology of the hermaphroditic gonad. The distal tip cells undergo a series of migratory phases interspersed with turns to form the gonad. A wide variety of genes have been identified as crucial to this process, from genes that encode components and modifiers of the extracellular matrix to signaling proteins and transcriptional regulators. The connections between extracellular and transmembrane protein functions and intracellular pathways are essential for distal tip cell migration, and the integration of this information governs gonad morphogenesis and determines gonad size and shape. WIREs Dev Biol 2012, 1:519–531. doi: 10.1002/wdev.45 This article is categorized under: Establishment of Spatial and Temporal Patterns > Regulation of Size, Proportion, and Timing Early Embryonic Development > Development to the Basic Body Plan Invertebrate Organogenesis > Worms

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Schematic representation of the adult hermaphrodite. Gonadal structures are featured in a lateral view4 (a) and a cross‐sectional view (b). (a) The anterior gonad arm (left) depicts germ cells in the distal gonad; proximal gonad structures are labeled. The posterior arm (right) depicts the somatic structures of the gonad including a distal tip cell (purple) and sheath cells (yellow). The dotted line running through the posterior gonad arm represents the approximate location of the schematic cross‐sectional slice. (b) The cross‐sectional view depicts the basement membranes (red) that surround the body wall muscles (M), hypodermis (H), intestine (I), distal gonad (DG), and proximal gonad (PG). This schematic is based on an electron micrograph.

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A summary of genes crucial for distal tip cell (DTC) migration. Solid line arrows represent direct interactions and dotted line arrows represent indirect or speculative interactions. PAT‐3 is represented by integrin β and INA‐1 or PAT‐2 is represented by integrin α. UNC‐6/netrin; CED‐2/CrkII; CED‐5/Dock180; CED‐12/ELMO; UNC‐73/Trio GEF (guanine nucleotide exchange factor); UNC‐112/kindlin; PAT‐4/ILK; MIG‐2/Rac; CED‐10/Rac; VAB‐10/spectraplakin; VAB‐3/Pax6; MIG‐6/papilin; FBL‐1/fibulin; PAK/PAK‐1; or MAX‐2.

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A molecular model for the commencement of distal tip cell (DTC) migration. Both GON‐1 and MIG‐6L are crucial for DTC migration, and we speculate that MIG‐6L positively regulates GON‐1 activity or localization (dotted arrows). Mutant phenotypes suggest that FBL‐1 may act to maintain the integrity of the basement membrane (BM, dotted arrows) and this effect of FBL‐1 might limit GON‐1 activity (dotted repression). Because GON‐1 and MIG‐6L are expressed by the DTC, their expression levels are potentially higher than that of FBL‐1 in the DTC basement membrane. We propose that this imbalance in expression results in an optimum level of GON‐1 activation and matrix remodeling, perhaps at the front of the DTC (light orange BM), to allow DTC migration. By contrast, higher levels of FBL‐1 in the gonadal basement membrane limit the ability of GON‐1 to remodel the matrix or to support migration.

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Distal tip cell migration defects. Arrows show the direction of migration. Sections represented by dotted lines indicate potential variability in migration paths. A wild‐type U‐shaped migratory path is shown in (a). Defects are grouped according to the migration stages: commencement (b, no migration), turning (c, ventralized; d, no turn; e, wrong turn), pathfinding (f, meandering on dorsal; g, change in direction), and cessation (h, perpetual migration; i, overshoot). Only posterior gonads are represented, although these defects also occur in the anterior gonad arms.

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The U‐shaped migratory path of the distal tip cell shapes the hermaphrodite gonad arm during larval development. Schematic representation of a posterior gonad arm shows the distal tip cell (crescent shapes) at different stages of migration. Arrows depict the direction of distal tip cell migration and colored arrows show the extent of distal tip cell migration during each phase and larval stage: phase 1/larval stage 2 (red), phase 2/larval stage 3 (yellow) and phase 3/larval stage 4 (blue). The key genes associated with the indicated distal tip cell activities are listed in Table 1.

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Early Embryonic Development > Development to the Basic Body Plan
Establishment of Spatial and Temporal Patterns > Regulation of Size, Proportion, and Timing
Invertebrate Organogenesis > Worms