Regeneration in Crustaceans and Insects

Abstract

Many animal species have the capability to regenerate lost body parts. How regeneration takes place and why animals have varying potentials for regeneration remain active questions for biologists. The field of regenerative biology has witnessed unprecedented advances in the last several years owing to the availability of molecular and genomics tools and the establishment of many animal models. Regeneration research in arthropods has a long history, with extensive insights achieved from using model organisms from the taxa Crustacea and Insecta. Studies in animals ranging from fiddler crabs to crickets have revealed much about the different stages of regeneration, such as wound healing, blastema formation, growth, proliferation and patterning, as well as how hormonal control and systemic signalling impact regenerative capacity. The molecular and genetic insights achieved from studying these simpler model organisms have the potential to impact the field of regenerative biology by identifying conserved mechanisms of regeneration.

Key Concepts

  • Regeneration studies use the fiddler crab, crayfish, sand hopper, red flour beetle, fruit fly, cockroach, cricket and silverfish.
  • For amputated limbs, wounds heal by a combination of rapid closure of the wound with a scab or autotomy membrane, and migration of cells into the wound.
  • Imaginal disc wound closure involves cytoskeletal‚Äźdriven cell shape changes and zippering together of the epithelium, without cell migration.
  • A regeneration blastema, or zone of proliferating cells, forms after both external limb amputation and imaginal disc damage.
  • Growth of the blastema requires similar signals in multiple model organisms, including growth factor signalling in response to FGFs and EGFR activity, Wg/WNT signalling and Hippo signalling.
  • Many developmental patterning genes are also required for patterning during regeneration. However, knockdown of these patterning genes revealed additional roles in regeneration beyond those observed during normal development.
  • Some plasticity in cell fate enables replacement of lost cell types.
  • Signals at the wound can alter pattern and cell fate, generating ectopic eye spots in butterflies and requiring the activity of a protective factor that stabilises cell fate gene expression during regeneration in fruit flies.
  • Hormonal signalling, which controls moulting and metamorphosis, limits regenerative capacity. In some model organisms, tissue damage can influence hormone production and the timing of moults and metamorphosis.

Keywords: regeneration; insects; crustaceans; wound healing; blastema; proliferation; growth; patterning; systemic signalling

Figure 1. Wound healing. (a) Wound healing during regeneration following autotomy in the crustacean Uca pugilator is marked by formation of an autotomy membrane (AM) at the wound site and a melanised scab beneath the AM. The severed nerve fibre secretes the fibroblast growth factor‐2 (FGF‐2), which attracts granulocytes and epidermal cells. The activated epidermis migrates centripetally and will eventually secrete a cuticle and form the blastema (Hopkins, ). (b) The top panel shows a cut wound in the wing imaginal disc of the insect Drosophila melanogaster, and the cellular events are depicted in the bottom panel. Actin‐rich filopodial extensions bring the columnar epithelial cells at the wound edge together to heal the wound. Jun N‐terminal kinase (JNK) signalling is required for filopodia formation (Bosch et al., ).
Figure 2. Blastema formation and regenerative growth. (a) During leg regeneration in the hemimetabolous insect Gryllus bimaculatus, blastema formation involves expression of Wingless (Wg), Decapentaplagic (Dpp), Hedgehog (Hh), Epidermal growth factor receptor (EGFR) and Janus Kinase Signal Transducer and Activator of Transcription (JAK‐STAT) signalling molecules, with functional roles established for Wg, EGFR and JAK‐STAT signalling. The Hippo signalling pathway is important for growth along the proximal–distal axis (Bando et al., ; Nakamura et al., , , ). (b) A blastema is formed at the edge of a wound generated by cutting or tissue ablation of wing imaginal discs in the holometabolous insect Drosophila melanogaster. Reactive oxygen species (ROS) are generated in the damaged disc, and the JNK, Wg, Hippo and JAK‐STAT signalling pathways are important for regenerative growth. Green arrows indicate the direction of growth (Bosch et al., ; Katsuyama et al., ; Santabárbara‐Ruiz et al., ; Smith‐Bolton et al., ; Sun and Irvine, ).
Figure 3. Patterning. (a) Proximal–distal (PD) patterning during leg regeneration in a Gryllus bimaculatus 5 dpa (days post‐amputation) blastema. The distal fate determinant Distalless (Dll) is expressed at the distal tip. Dachshund (Dac) is required for specification of medial fate and its expression is restricted from the distal region through Enhancer of zeste (E(z)) activity. The chromatin modifier Utx regulates medial cell fate through EGFR expression, which prevents duplication of the medial segment (Hamada et al., ; Ishimaru et al., ; Nakamura et al., ). (b) PD patterning during Drosophila melanogaster leg regeneration is different from normal development. During normal development PD patterning is established from the distal‐most region to the proximal parts. During regeneration after removal of the central (distal) portion of the disc, patterning is established in the proximal to distal direction (Bosch et al., ). (c) The patterning gene Taranis (Tara) protects cells from cell fate changes that can occur during regenerative growth in the Drosophila wing imaginal disc. When Tara is reduced, wing cells undergo posterior‐to‐anterior fate changes due to misregulation of the posterior selector gene engrailed (en) by damage‐induced JNK signalling (Schuster and Smith‐Bolton, ). (d) Cell fate plasticity is a feature of regenerative growth during D. melanogaster wing imaginal disc regeneration. When the vein region is removed through ablation, the adjacent intervein cells are re‐specified and proliferate to replace the missing vein tissue (Repiso et al., ).
Figure 4. Hormonal control and systemic signalling. (a) In Uca pugilator the moult cycle and regenerative growth cycle are coordinated through cross‐communication among the X‐organ (XO), the Y‐organ (YO) and peripheral tissues. Moulting is under the control of the two ecdysteroid hormones: ecdysone and 25‐deoxyecdysone, which are secreted by the YO located in the cephalothorax, which are converted into the active forms, ponasterone A and 20‐hydroxyecdysone respectively, in the peripheral tissues. The XO is located in the eye‐stalk and produces the moult inhibitory hormone (MIH) that inhibits ecdysteroid production in the YO (Chang and Mykles, ). (b) During wing imaginal disc regeneration in Drosophila melanogaster, the injured discs secrete Drosophila insulin‐like peptide 8 (Dilp8), which coordinates the systemic signalling that induces a developmental delay in the animal and growth retardation in the undamaged organs. Dilp8 acts by binding to its receptor Lgr3, expressed in the two pairs of Lgr3 neurons located in the brain lobes. Lgr3 neurons signal to the prothoracicotropic hormone (PTTH) neurons, located in the prothoracic gland (PG), which secretes ecdysone. The PG is a part of the bilobed structure, the ring gland, attached to the brain lobes. In response to Dilp8, the Lgr3 neurons suppress ecdysone release from the PG, triggering developmental delay of the whole animal so that the damaged tissue has time to regrow, and restricting the growth of undamaged tissue during this extended growth phase (Colombani et al., ; Garelli et al., ; Vallejo et al., ). Note: The A↔P axis denotes the anterior–posterior axis of the animal.
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Further reading

Bely AE and Nyberg KG (2010) Evolution of animal regeneration: re‐emergence of a field. Trends in Ecology and Evolution (Amsterdam) 25: 161–170.

Brockes JP and Kumar A (2008) Comparative aspects of animal regeneration. Annual Review of Cell and Developmental Biology 24: 525–549.

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Worley MI, Setiawan L and Hariharan IK (2012) Regeneration and transdetermination in Drosophila imaginal discs. Annual Review of Genetics 46: 289–310.

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Khan, Sumbul J, Schuster, Keaton J, and Smith‐Bolton, Rachel K(Jun 2016) Regeneration in Crustaceans and Insects. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0001098.pub2]