Regeneration in Planaria Secondary Article
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Regeneration in Planaria Secondary article Phillip A Newmark, Carnegie Institution of Washington, Baltimore, Maryland, USA Article Contents Alejandro Sa´nchez Alvarado, Carnegie Institution of Washington, Baltimore, Maryland, . Introduction USA . Brief Historical Note . Natural History . Classical Experimental Analyses of Planarian Planarians possess remarkable regenerative abilities enabling them to replace parts of the Regeneration body removed by amputation or naturally occurring fission. The regenerative process is . Proposed Mechanisms of Regeneration: The Role of mediated by the formation and eventual differentiation of a specialized structure known as Neoblasts the regeneration blastema. Projections and Summary Introduction these animals (see Brøndsted, 1969). The results of these In metazoans, regeneration of lost body parts requiring the experiments led Dalyell to conclude that planarians may formation of a blastema is known as epimorphic regenera- ‘almost be called immortal under the edge of the knife’ (see tion. A blastema is composed primarily of two cell Brøndsted, 1969). A rigorous description of planarian populations: an outer cell layer or ectoderm, derived from morphology, physiology and even behaviour is not found the epidermis that covers the wound surface after amputa- until the publication of Duge` s’ classic work in 1828 (as tion/fission; and mesenchymal cells that proliferate and cited by Randolph, 1897; see Brøndsted, 1969 for accumulate beneath this wound epidermis, eventually reference). In his work, Duge` s laid the foundations of differentiating into the lost body parts (Figure 1). Even modern planarian systematics. Between 1828 and the 1890s though the architecture of both planarian and vertebrate planarians attracted the attention of Michael Faraday, blastemas is the same, the mechanism of blastema Charles Darwin and W.H. Harvey among others, but their formation in planarians differs from that of vertebrates work on this subject is mostly descriptive. in two basic aspects. First, the wound epithelium forms by It was not until the early to mid-1890s that a renewed epidermal cell shape modifications rather than by cell experimental interest in the process of planarian regenera- proliferation. Second, the mesenchymal cells are derived tion emerged, fuelled primarily by the ongoing arguments from pre-existing undifferentiated cells (neoblasts), instead of vitalism versus reductionism engulfing the relatively new of the cellular dedifferentation observed in vertebrates. field of embryology. To Harriet Randolph, Jacques Loeb Such relative simplicity of blastema formation, combined and Hans Driesch, planarian regeneration presented an with the planarian’s basic body plan, developmental intriguing dilemma in which isolated parts of an adult plasticity and evolutionary position, make these free-living could recreate and regulate the characteristics of an members of the phylum Platyhelminthes a very attractive entirely new and whole organism, a process they thought model system in which to study and understand the akin to embryogenesis. It was this body of work that led molecular principles governing metazoan regeneration. Thomas Hunt Morgan and Charles Manning Child to study planarian regeneration in the late 1890s and early 1900s. It is interesting to note, however, that even after more than 200 years of studies, most of the biological Brief Historical Note questions raised by planarian regeneration still remain unanswered. The regenerative abilities of planarians have been known for over 230 years. In 1766, Peter Simon Pallas first described how a small piece dissected from a planarian head was capable of regenerating a complete organism (see Natural History Brøndsted, 1969). This observation was confirmed a few years later by Shaw and then by Draparnauld, when they The planarians commonly used for regeneration experi- noted the ability of these animals to propagate asexually by ments are free-living members (class Turbellaria; order fission (as cited by Randolph, 1897; see Brøndsted, 1969 for Seriata) of the phylum Platyhelminthes, the flatworms. reference). However, the experimental analysis of regen- They are assigned to the suborder Tricladida based on the eration in planarians begins with the work of Dalyell in three main branches of their digestive system (Figure 2a). 1814 and Johnson in 1822. These investigators inflicted The Tricladida may be further subdivided based upon partial or complete incisions, both longitudinally and ecological habitat: there are freshwater, marine and meridionally, along the axes of a variety of planarian terrestrial forms (the classification of these different forms species in order to ascertain the regenerative potencies of is controversial and beyond the scope of this review). The ENCYCLOPEDIA OF LIFE SCIENCES / & 2001 Nature Publishing Group / www.els.net 1 Regeneration in Planaria Figure 1 The process of head regeneration in Dugesia dorotocephala. (a) Schematic representation of blastemal components. The round cells correspond to the zone of neoblast proliferation in the vicinity of the wound (e, epithelium; m, neoblast-derived mesenchymal cells; n, neoblast; ex, extracellular matrix). (b) The same animal photographed every 24 hours after amputation. The numbers refer to days after amputation. Notice the marked cellular proliferation as evidenced by the growth of the blastema between days 2 and 3. freshwater planarians are the most commonly studied. form the cerebral ganglia (Figure 2b), which process They are traditionally subdivided into three families: the information received from the sensory structures (e.g. Planariidae, Dendrocoelidae and Dugesiidae, and exhibit photoreceptors, rheoreceptors and chemoreceptors) that some differences in regenerative abilities. For example, the are also concentrated in the head. Planarians lack a Dendrocoelidae can only regenerate anterior structures circulatory system and must rely upon diffusion to provide when transected anterior to the pharynx. the required oxygen; the highly branched digestive system, Planarians are triploblastic (possessing three tissue with one anterior and two posterior branches (Figure 2a), layers) acoelomates, with a bilaterally symmetrical body transports food throughout the entire body. Food enters plan that is dorsoventrally flattened. They range in size the animal through the muscular pharynx, which is from a few millimetres to 4–5 cm. The epidermal layer situated in the middle of the body and is extruded through surrounding the flatworm is ciliated on the ventral surface; the mouth opening during feeding. The digestive system these cilia propel the animal in a gliding motion along a lacks an anus, thus food enters and leaves the animal ventrally secreted mucous trail. Beneath the epidermal through the opening of the pharynx. layer (and the basal lamina to which it attaches) is a There are two modes of reproduction in planarians: (1) complex body wall musculature composed of circular, asexual reproduction by fission and (2) sexual reproduc- diagonal and longitudinal muscle fibres. The planarian tion involving pairwise mating. Asexual reproduction nervous system is composed of two ventral nerve cords that occurs by transverse fission, usually posterior to the run longitudinally along the length of the organism. These pharynx; the missing pieces are then regenerated. Planar- nerve cords aggregate in the anterior of the flatworm to ians that reproduce sexually, on the other hand, are 2 ENCYCLOPEDIA OF LIFE SCIENCES / & 2001 Nature Publishing Group / www.els.net Regeneration in Planaria Figure 2 The planarian gastrovascular and nervous systems. (a) Visualization of the three gut branches (1, 2, 3) by feeding the animals fluorescent latex beads. Notice the intricate web of fasciculations of each of the secondary branches. This allows the transport of both oxygen and nutrients to all partsof the body. (b) The planarian brain consisting of two cerebral ganglia (+) seen at a  40 magnification. (c) The two nerve cords, each originating in one of the two cerebral ganglia are seen here at the trunk level (*) running parallel to the pharynx (  20 magnification). (d) The nerve cords at the tail tip of the planarian displaying commissural neurons (arrow) which connect the cords along the entire AP axis of the animal (  40 magnification). The nervous system in panels b, c and d was visualized by labelling neurons with an anti-FMRF amide primary antibody (a neuropeptide) detected with a secondary fluorescent-conjugated antibody.We acknowledge the expert confocal microscopy assistance provided by Susanna Castel. hermaphroditic with cross-fertilization being the norm. marine polyclad planarians, a fact reflected by the Some species combine these two modalities, alternating ectolecithal eggs (with yolk on the outside of the egg) between sexual and asexual reproduction during different observed in the triclads (Hyman, 1951). A single cocoon, or seasons, while others utilize only a single mode of egg capsule, contains between 5 and 20 eggs (depending reproduction. upon the species) surrounded by tens of thousands of yolk Embryonic development in the sexual triclad planarians cells. During early cleavages, the embryonic cells show no is highly modified from the spiral cleavage observed in the ordered pattern of cleavage and may even separate from ENCYCLOPEDIA OF LIFE SCIENCES / & 2001 Nature Publishing Group / www.els.net 3 Regeneration in Planaria each other. Eventually, some embryonic cells migrate of planarian regeneration (his wife,