The making of an octopus arm

Abstract

BackgroundMost of our current findings on appendage formation and patterning stem from studies on chordate and ecdysozoan model organisms. However, in order to fully understand the evolution of animal appendages, it is essential to include information on appendage development from lophotrochozoan representatives. Here, we examined the basic dynamics of the Octopus vulgaris arm’s formation and differentiation - as a highly evolved member of the lophotrochozoan super phylum - with a special focus on the formation of the arm’s musculature.ResultsThe octopus arm forms during distinct phases, including an early outgrowth from an epithelial thickening, an elongation, and a late differentiation into mature tissue types. During early arm outgrowth, uniform proliferation leads to the formation of a rounded bulge, which subsequently elongates along its proximal-distal axis by means of actin-mediated epithelial cell changes. Further differentiation of all tissue layers is initiated but end-differentiation is postponed to post-hatching stages. Interestingly, muscle differentiation shows temporal differences in the formation of distinct muscle layers. Particularly, first myocytes appear in the area of the future transverse prior to the longitudinal muscle layer, even though the latter represents the more dominant muscle type at hatching stage. Sucker rudiments appear as small epithelial outgrowths with a mesodermal and ectodermal component on the oral part of the arm. During late differentiation stages, cell proliferation becomes localized to a distal arm region termed the growth zone of the arm.ConclusionsO. vulgaris arm formation shows both, similarities to known model species as well as species-specific patterns of arm formation. Similarities include early uniform cell proliferation and actin-mediated cell dynamics, which lead to an elongation along the proximal-distal axis. Furthermore, the switch to an adult-like progressive distal growth mode during late differentiation stages is reminiscent of the vertebrate progress zone. However, tissue differentiation shows a species-specific delay, which is correlated to a paralarval pelagic phase after hatching and concomitant emerging behavioral modifications. By understanding the general dynamics of octopus arm formation, we established a basis for further studies on appendage patterning, growth, and differentiation in a representative of the lophotrochozoan super phylum.Electronic supplementary materialThe online version of this article (doi:10.1186/s13227-015-0012-8) contains supplementary material, which is available to authorized users.

Small-Animal 18F-FDG PET for Research on Octopus vulgaris: Applications and Future Directions in Invertebrate Neuroscience and Tissue Regeneration

“…Overall, our data indicate that after vena cava injection the radioactive solution efficiently circulates throughout the body, reaches all organs, and is efficiently retained by organs with a higher metabolic rate. 18 F-FDG Uptake in Regenerating Arm 18 F-FDG PET scanning of the 2 animals with a regenerating arm showed that activity in the nonregenerating arms was higher at the central arm axes. This finding could be due to the massive population of neuronal cells that forms the peripheral nervous system of the arm and is located at its center.…”

“…This finding could be due to the massive population of neuronal cells that forms the peripheral nervous system of the arm and is located at its center. Like other neural structures, neurons of the peripheral nervous system consume a large amount of glucose to sustain their function and thus show high 18 F-FDG uptake. Activity in the regenerating arm was measured at 2 locations-the base and the tip-and was compared with activity in the nonregenerating arms of the same animal.…”

“…Octopuses are easily maintained and handled and are of an appropriate size for a canonical highresolution small-animal PET system. 18 F-FDG PET is a widely used tool for the in vivo study of oncologic, cardiovascular, and neurologic disorders and of cerebral glucose metabolism (6)(7)(8)(9). In view of the interest in developing novel strategies to repair bone and cardiovascular muscle, 18 F-FDG PET is also becoming relevant to studies of bone regeneration and cardiac repair and regeneration, because it allows following of tissue regeneration through noninvasive measurements of metabolic processes (10)(11)(12).…”

“…Cephalopods can regenerate lost or injured structures such as the shell, the appendages (arms and tentacles), the cornea, peripheral nerves, and brain centers (13). In particular, the arms of the octopus have a complex structure and physiology (14)(15)(16)) that share similarities with early arm development and regeneration in some vertebrate models (13,17,18). These similarities make the octopus an ideal model for studying limb regeneration and for finding conserved pathways that might be triggered in various animal species (including mammals) to induce regeneration of injured tissue.…”

Molecular Determinants of Cephalopod Muscles and Their Implication in Muscle Regeneration

“…However, studies focusing on species-specific gene expression (Navet et al, 2008; Nödl et al, 2015) have shown that certain features of cephalopod muscle development seem to be specific to this molluscan class. Therefore, more information will be necessary in order to understand the molecular basis of this highly complex and adapted tissue type.…”