Skin field formation: morphogenetic events DANIELLE DHOUAILLY*, ISABEL OLIVERA-MARTINEZ α , INGRID FLINIAUX β , SYLVAIN MISSIER, JEAN P. VIALLET and JACQUES THELU Equipe Biologie de la Différenciation Epithéliale, UMR CNRS 5538, Institut Albert Bonniot, Université Joseph Fourier, Grenoble, France ABSTRACT This chapter is mostly a review of the pioneering work of the Philippe Sengel school in Grenoble carried out in the late sixties and the seventies. The questions raised concerning the morphogenesis of feather tracts were approached by means of microsurgery on chick embryos. P. Sengel and his wife M. Kieny had the feeling that proteins synthesized by the neural tube were required for the formation of feather fields. It was my pleasure to carry on the story from the beginning. Although some clarifications concerning this morphogenesis have been contributed by my group and by a few other laboratories interested in this subject, the most important contributions to recent research have been the elucidation of the nature of the required messages, which will be explored further in other papers in this Issue. KEY WORDS: chick, cutaneous appendage, dermis, differentiation, epidermis, feather, neural tube, pteryla Int. J. Dev. Biol. 48: 85-91 (2004) 0214-6282/2004/$25.00 © UBC Press Printed in Spain www.ijdb.ehu.es *Address correspondence to: Dr. Danielle Dhouailly. BDE-LEDAC, UMR CNRS 5538, Institut Albert Bonniot, Domaine de la Merci, 38706, La Tronche Cedex, France. Fax: +33-4-76-54-94-25. e-mail: danielle.dhouailly@ujf-grenoble.fr Note α α α α α Present address: Division of Cell and Developmental Biology, School of Life Sciences, University of Dundee, Wellcome Trust Biocentre, Dow St., Dundee, DD1 5EH, U.K. Note β Present address: Atelier de Transgenèse, CEA, Grenoble, DRDC/AT 17 rue des martyrs, 38054 Grenoble cedex, France. Introduction One of the significant steps during skin morphogenesis in birds and mammals is the establishment of the cutaneous appendage fields, these are initially homogeneous and develop into heterogeneous feather- or hair-bearing fields. In the avian embryo, the different feather tracts, or pterylae, arise sequentially following a dorso-lateral and a latero-ventral morphogenic wave (Fig. 1, and Mayerson and Fallon, 1985). The way in which the distinct pterylae are laid out is called the macropattern (Sengel, 1976). In chick, the dorsal trunk feather macropattern is composed of the spinal and scapular pterylae (Fig. 2A), while that of the ventral side is comprised of the pectoral and ventral pterylae (Fig. 2B). Each tract, in addition to its location and time of appearance, is characterized by its contour, the size and number of feathers. In each tract the design formed by the feathers is called the micropattern (Sengel, 1976). The same distinction between skin macropattern and micropattern occurs for mammals. In mouse, four main types of skin fields can be distinguished. The first hair follicles to develop are those of the tactile hairs or vibrissae. They arise in sequence along five rows on right and left pads formed by upper-lip skin. At a later stage, primary pelage hairs differentiate almost concomitantly and cover most of the body surface. The two last skin fields to differentiate are those of the tail, where pelage hairs are ranged and intermingled with “scales”, and the plantar surface, where sparse hairs are present between the foot pads which have sweat glands. Numerous experiments have been conducted using the technique of heterotopic transplantations (Kieny and Brugal, 1977; Mauger, 1972a and b) and dermal-epidermal heterotopic and heterospecific recombinations (Dhouailly, 1973; Dhouailly, 1977; Dhouailly and Sengel, 1975; Dhouailly, unpublished data on heterospecific mouse/ chick limbs), and these showed that the information relating to the formation of chick and mouse macropattern and micropattern resides first in the mesoderm and then in the dermis. In chick, the different pterylae are separated by semi-apteria, which are characterized by unorganized and scarce feathers. In the trunk, except for a tiny middorsal featherless region, the only true glabrous area is the midventral apterium, which forms a ribbon on each side of the midventral closure. This apterium is surrounded by the ventral pteryla and is contiguous to the amnion via the umbilical cord. The first morphological indication of the formation of a pteryla as opposed to an apterium, or semi-apterium, is the early densification of the upper part of the predermal mesenchyme to form what is called a dense superficial dermis (2.6 nuclei/1000μm 3 ) (Sengel, 1976; Wessels, 1965), and the subsequent differentiation of its overlying ectoderm into an epidermis (Wessells, 1965). This dermal densification occurs by day 6 in the spinal pteryla and the ventral pteryla, but only several days later in the semi-apteria. In the midventral apterium, by contrast, the dermal fibroblasts remain sparse (1.98 nuclei/1000 μm 3 ), and extra-cellular material accumulates (Sengel et al., 1969). The superficial dense dermis is redistributed into dermal condensations by day 7 in the dorsal pteryla (Viallet et al., 1998), with