Role of heterotypic tissue interactions in deer pedicle and first antler formation—revealed via a membrane insertion approach

Abstract

Heterotypic tissue interactions play an indispensable role in organ generation and regeneration. In contrast to the classic examples of tissue interactions prevailing in the formation of tetrapod limbs or pectoral fins that can only take place when the interactive tissues are in intimate contacts, the interactions in deer antler formation are novel in that the inducer and the responder are separated by a distance of 1-2 mm. This feature offers a unique opportunity to explore the mechanism underlying tissue interactions by permitting membrane insertion between the two interactive tissues. Four experiments were conducted in this study. The results showed that the impermeable membranes inhibited antler formation. In contrast, the permeable membrane (0.45 microm in pore size) substantially slowed pedicle growth and antler initiation but did not stop them. Interestingly, the impermeable membrane/sheath only slightly retarded antler elongation. Overall, our results demonstrate that interactions between the two interactive tissues, antlerogenic tissue and the overlying skin, are indispensable for first antler initiation and are achieved through diffusible molecules rather than direct physical contact. As the heterotypic tissue interactions are only required during antler initiation but not elongation, they must be transient in nature, and thus differ from those operating in limb/fin formation that can only be sustained by continuous interactions. A system in which organ development is achieved only through transient tissue interactions must be novel, if not completely unique. Understanding this system will undoubtedly enrich the knowledge in the field of tissue interactions and organogenesis.

Evolution of ruminant headgear: a review

“…The apical periosteum undergoes a partial transformation to a perichondrium, resulting in apical deposition of highly vascularized bony and cartilaginous tissues. Although intensification of pedicle growth typically coincides with male puberty and an increase in testosterone [42,64], additional molecular signalling between the periosteum and integument is required to initiate pedicle formation [63]. Pedicle growth is completed and antlerogenesis begins during the stage of endochondral ossification.…”

Development of a nude mouse model for the study of antlerogenesis—mechanism of tissue interactions and ossification pathway

“…Although AP fibrous layer is naturally adjacent to skin, there is reason to believe that it is the cellular layer that secretes these putative molecules (Goss, '95;Li et al, 2008). The ideal way to test this would be to transplant one layer (cellular or fibrous) at a time together with deer skin on the nude mouse forehead to determine which layer can induce somatic skin to transform into velvet skin.…”

“…Tissue interactions involved in antler development are unique in that they take place in postnatal life between two interactive tissue types (periosteum and epidermis of the overlying skin) separated by distances that, on a histological scale, are exceedingly long (over 1 mm), and yet these interactions are potent enough to transform the adult deer scalp skin into a unique pelage, known as antler velvet (Li and Suttie, 2000;Li et al, 2008). In our previous studies we demonstrated that both antler generation (Li et al, 2008) and regeneration (Li et al, 2007) only require transient tissue interactions, achieved via diffusible molecules. However, those studies neither established whether all tissue types (subcutaneous connective tissue and dermis) interposed between AP (inducer) and epidermis of the overlying skin (responder) are necessary for the establishment of these interactions, nor the precise tissue origin (AP fibrous or cellular layer) of the initial inductive signals.…”

“…To gain further insights into the nature of the tissue interactions that prevail in first antler generation, recently Li et al (2008) carried out an experiment in which a piece of either impermeable or permeable membrane (0.45 mm pore size) was physically interposed between AP and the overlying skin before pedicle initiation. It was found that the impermeable membrane permanently inhibited antler formation, whereas the permeable membrane only slowed pedicle and antler initiation, but did not prevent these processes.…”

Deer Antlers – A Model of Mammalian Appendage Regeneration: An Extensive Review

“…Velvet transformation of skin is assumed to be induced by diffusible molecules produced by cells of the AP or their derivatives [23,30] . Support for this view comes from an experimental study in which insertion of an impermeable membrane between subcutaneously transplanted AP and overlying forehead skin prevented velvet transformation of the skin in male sika deer (Cervus nippon) fawns [31] . A recent investigation using the nude mouse model provided circumstantial evidence that the presumed inductive molecules are derived from the cambium (as opposed to the fibrous) layer of the AP [32] .…”