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Growth and Differentiation of Skin THE JOURNAL OF INVESTIGATI VE DERMATOLOGY, 67:8-14. 1976 Vol. 67 , No.1 Copyright © 1976 by The Williams & Wilkins Co. Printed in U.S.A. GROWTH AND DIFFERENTIATION OF SKIN B. ALLEN FLAXMAN, M.D., AND PAUL F. A. MADERSON, PH.D. Subsection of Dermatology, Department of Medicine, Brown University and the Miriam Hospital, Providence, Rhode Island, and Department of Biology , Brooklyn College, New York, New York, U. S. A . During the past 25 years, attention has turned from the morphologic aspects of skin development which are well known, to the mechanisms that control this development. Although our knowledge of these mechanisms is still limited, some avenues of investigation appear promising, e.g., epithelial-mesenchymal interactions, cell communication and other cell surface phenomena, and certain aspects of the proliferative process. In the analysis of what controls growth and differentiation, skin, as the experimental system, has played a major role. During the quarter century history of the Sym­ it serves as a useful preliminary identifying feature posia on the Biology of Skin, many aspects of skin for taxonomic purposes. Classical 19th century biology have been reviewed but, surprisingly light microscopic studies showed that at their enough, very little attention has been directed earliest stages, ectodermal (epidermal) and so­ toward the embryogenic aspects. Most of the matic mesodermal (dermal) structures were the current symposium concerns specific attributes of same in all vertebrate embryos. Only in the last 25 the mature system, so we shall confine ourselves years have sufficient data become available to mainly to "Growth and Differentiation" during the formulate hypotheses which adequately explain all embryonic period. Our increased knowledge of the aspects of the subsequent diversity of the adult dynamics of integumental development consti­ organ system. tutes an exciting recent chapter. The develop­ Successive divisions of the fertilized egg lead to ment of the vertebrate integument has provided an formation of a 3-layered embryo whose organiza­ especially good opportunity to study the control tion differs somewhat according to species. The mechanisms and their relation to the whole process outermost layer, or ectoderm, forms surface epider­ of embryogenesis. We will concentrate on the few mis and the epithelial component of all skin areas of skin development that have generated, appendages. The middle layer, or mesoderm, gives and will continue to generate, new answers and rise to cells that form mesenchyme (dermis in the questions. adult), whose interaction with ectoderm is signifi­ The sequence of our knowledge of how the cant throughout the entire life of the organism. vertebrate integument develops parallels that of The two germ layer constituents of the verte­ many other organ systems. Extensive morphologic brate integument have quite different potentials analyses by classical light microscopic studies have for development. The mesenchymal cells of the now been confirmed and elaborated by ultrastruc­ somatic mesoderm give rise to dermal fibroblasts tural studies and, to a limited degree, by biochemi­ which secrete the precursors of self-assembling, cal investigations. Recently, as a result of using the extracellular collagen, as well as elastin, glyco­ experimental approach to analyze development, a proteins, and glucosaminoglycans. Dermal blood considerable number of reports document findings vessels and fat cells also derive from the basic in skin that are relevant to development elsewhere mesodermal cell population. The resultant " skele­ in the organism. A fundamental problem of devel­ tal" and "nutrient" functions of the end-products opmental biology is exemplified by the formation of mesenchymal differentiation are ubiquitous of the integument: the genesis of eventual hetero­ among species. Recently we have come to realize geneity in structure and function from initially that, during development, mesoderm ally derived homogeneous embryonic cell populations. In this matrix material undergoes significant changes paper we will emphasize and review how our which are better detected at the biochemical than understanding of this phenomenon has advanced. at the morphologic level (1). The ectodermal cells DEVELOPMENT OF THE VERTEBRATE INTEGUMENT: which form the general body epidermis may even­ GENERAL CHARACTERISTICS tually synthesize predominantly mucoproteins (in Integumentary structure varies so much, not fish) or keratinaceous proteins. Further diversity is only within a species but also between species, that found within certain epidermal appendages such as the sebaceous glands whose main function is Supported in part by Grant CA 11536 from the lipid synthesis. In higher vertebrates, the correla­ National Cancer Institute. tion between the type of intracellular filaments Reprint requests to: Dr. B. A. Flaxman, Miriam Hospital, 164 Summit Avenue, Providence, Rhode Island seen under the electron microscope and the x-ray 02906. diffraction patterns obtained from mature epider- 8 July 1976 GROWTH AND DIFFERENTIATION OF SKIN 9 mal cells l2,3] indicates two distinct categories of of cell differentiation can be so altered that constit­ keratinaceous proteins: the hair or alpha-type and uent units of "differentiated" tissues can dedif­ the feather or beta-type l4J. Comparative studies ferentiate to provide a source of new cells. The suggest that the ability to synthesize alpha-keratin elegant experiments of Gurdon [7] have shown that is the most fundamental characteristic of the an adult amphibian can be obtained via appar­ vertebrate epidermis [2] . However, the reptilian ently normal embryonic and larval development lineages associated with the major Mesozoic radia­ which resulted from placing an adult epidermal tions (from which arose modern reptiles and birds) cell nucleus in an enucleated oocyte. These experi­ have an additional faculty, the ability to synthe­ ments indicate that the entire genome is present in size beta-keratin, which is differentially expressed each adult nucleus, that differential gene repres­ in different forms [4]. sion must occur during development, and that the During evolution, the vertebrate integument cytoplasm has important inf1uences on nuclear acquired the ability to form " appendages," which behavior. Apparently, therefore, whatever control have been defined as "localized centers of special­ factors may be demonstrated in embryos or adults, ized epidermal and/or dermal cell proliferation and they ultimately impinge on a fundamental, and differentiation, within an otherwise generalized probably continuous, nuclear- cytoplasmic interac­ integument" [5J. Ontogenetically, they seem to be tion. associated with the developmental fields which are The number of factors that may inf1uence nor­ believed to be associated with the scaled pattern of mal cell behavior continually increases as our the vertebrate integument. They ref1ect the evolu­ knowledge of cell biology is expanded by increas­ tionary predilection of the organ system for selec­ ingly sophisticated experimental tools. We do not tion in various environments. The formation of know with certainty the number and types of these structures involves similar basic mechanisms mechanism(s) that ultimately control cell behav­ and suggests an intimate relation between ecto­ ior. In addition, there probably are different con­ derm and mesoderm. (See review by Serri and trols for different aspects of behavior. These may Cerimele [6 J.) During embryogenesis, down­ be overlapping, e.g. , mesenchyme may regulate growths of ectoderm into mesenchyme provide the both organogenesis and cell differentiation, but epithelial component of the organ. For hair and there may also be other distinctly different control feather, the clear-cut formation of associated mes­ factors which may change with time. enchymal structures is characterized by a close The existence of epithelial-mesenchymal in­ aggregation of cells in relation to the overlying teractions as an empirically demonstrable category ectoderm. The ingrowth of ectoderm and adjacent of controlling factors in all of embryogenesis has condensing mesenchyme forms the basic organ. A been generally accepted for some time [8-10], and second ingrowth of the epithelium of the develop­ investigations in this field have been paramount ing hair follicle into the mesenchyme leads to the for many developmental biologists. The experi­ formation of sebaceous and apocrine glands. Ec­ mental findings for skin have been reviewed by crine sweat glands initially grow as solid cords of several authors lll,12J. The anatomy of develop­ epidermal cells which then develop a lumen by the ment of certain integumentary appendages sug­ formation and coalescence of intracytoplasmic gests both mesenchymal and ectodermal participa­ vacuoles. In this process, the morphologic associa­ tion, but morphology alone tells us little about the tion with the mesenchyme is not as clear as for hair nature of the interactions. Whatever they may be, and feather. These initial morphologic events are they may not always be the same, or even present followed by the establishment of distinctive pat­ at all, in some situations. It is generally assumed terns of cell differentiation in each appendage. that mesenchymal inf1uences on the ectoderm (or dermis on epidermis) are the more important, but CONTROLS OF GROWTH AND DIFFERENTIATION recent data strongly indicate that the ectodermal The foregoing brief review of the fundamentals potential
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