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The Corneal Endothelium in the Rat

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The Corneal Endothelium in the Rat Eye (1990) 4, 389-424 The Corneal Endothelium S. J. TUFT and D. J. COSTER London and Adelaide Summary The endothelium is a monolayer of cells on the posterior corneal surface that trans­ ports water from the stroma into the anterior chamber. This movement of water counters a natural tendency for the stroma to swell and is necessary to maintain a transparent cornea. Embryologic studies, in particular the demonstration of the derivation of the endothelium from the neural crest, have provided insight into the factors that govern the response of this tissue to disease. In some species the endo­ thelium can regenerate after injury, but in man cellular enlargement is the main mechanism of repair after cell loss. A clinical estimate of endothelial cell density and function is provided by specular microscopy, fluorophotometry and pachymetry. In this paper we review the development, structure and function of the corneal endo­ thelium, and then consider the pathological processes that can affect this tissue. There have been considerable advances The Normal Endothelium towards an understanding of the physiology of 1. Embryology the endothelium since its role in maintaining The eye and periocular structures are formed corneal clarity was first recognised. Clinical from cells that are derived from four distinct interest has been spurred by the refinement of embryologic tissues-surface ectoderm, complex intraocular surgical techniques, mesoderm, neural tube and the neural crest appreciation of the susceptability of the endo­ (Fig. 1).1 Many of the structural roles of meso­ thelium to surgical trauma and the develop­ derm in the rest of the body are assumed by ment of in vivo methods of evaluation that can Ectoderm (Epiblast) / ............. demonstrate the dramatic changes in mor­ Neurecloderm Epidermal Ectoderm Mesoderm phology which follow seemingly minor /\ Neural Crest Neural Tube injuries. In addition, a reassessment of the embryogenesis of the corneal endothelium Non-Ocular AOcular has influenced our interpretation of endothe­ I I lial pathology. We are at a point where the Corneal Epithelium E�lr.-ocular My.cle. V •• cular Endothelium current understanding of the development, Denial Papillae structure and function of the corneal endo­ M""anophoru thelium is providing an appreciation of the surprisingly diverse pathology which can Fig.1. A diagramatic representation af the derivation affect this apparently simply monolayer of of ocular tissues from embryonic precursors. The cells. corneal endothelium is a product of the neural crest. From Department of Clinical Ophthalmology, MoorfieldsEye Hospital, City Road, London, and Department of Ophthalmology, Flinders Medical Centre, Bedford Park, South Australia. Correspondence to: Professor D. J. Coster, Department of Ophthalmology, Flinders Medical Centre, Bedford Park, South Australia 5042. 390 S. J. TUFT AND D. J. COSTER the neural crest in the head and neck, and the The inducers that mediate these complex neural crest has a crucial role in the develop­ cellular interactions have not been identified ment of the eye. 2.3.4.5 but it appears that the histogenesis of each The fundamental studies of ocular embryo­ migrating cell is in part determined by its locus logy have been performed in birds, with of origin on the neural crest, with later modi­ movement of the neural crest being mapped fication by glycoproteins in the environment by transplanting labelled cells between through which it moves. 18.19,20 Needless to say, embryos and following their development in such a complex pattern may be modifed at the resulting chimera. 6 Radioactively labelled several levels. The eventual formation of a cells can be identified for a few cell divisions monolayer appears to be determined by con­ 7 during early oculogenesis, but, by using quail tact inhibition, with the lens and the primary cells that contain an intrinsic nuclear marker cornea acting as substrata. 21,22 Experiments which can be identified after transplantation show that the cells can move over any surface into chick embryos, it has been possible to fol­ made available to them, to the extent that an 8 low subsequent stages. This type of experi­ intact junction between the lens equator and ment has demonstrated the remarkable the optic cup is required to prevent backward mobility of neural crest cells in the embryo migration of endothelial cells over the neu­ and has shown that it is a popUlation of these roretina. 23 Removal of the lens vesicle results cells that ultimately forms the corneal in a loss of maturation control with persistent endothelium. multilayering of the endothelial cells on the Neural crest cells can first be identified as posterior corneal surface. 24 they separate from the neural plate, a thick­ Intercellular junctions begin to form when ening of the dorsal surface ectoderm. Prior to the endothelial monolayer is complete. Gap the closure of the neural folds at the anterior junctions develop first, the apical band is in neuropore, the neural crest cells begin to place by the sixteenth week of gestation and move peripherally as primary mesenchyme an adult configuration is achieved by twenty (Fig. In the primate, part of the migrating 2). weeks. 25 The formation of intercellular junc­ wave of neural crest cells comes to lie in a tions corresponds with the beginning of aque­ loose matrix at the rim of the optic cup and, at ous secretion and the maturation of the days post-ovulation, these cells stream cen­ 40 barrier and transport functions of the corneal trally through the loose fibrillar material of endothelium. In the avian model, the gradual the primary cornea that has formed in the cleft increase in corneal transparency during the between the lens vesicle and the surface ecto­ second half of gestation is dependent upon derm. 9.10.11.12 This centripetal movement of normal thyroid function.26.27 Thyroid hor­ neural crest cells is termed the first wave of mones may control the deposition of ground mesenchymal migration ; a second wave later substance, and thus the ability of the stroma contributes cells that form the keratocytes to bind water, or they may regulate the matu­ and stromal cells of the iris. 13 Macrophages precede the migration of crest cells, which ration of the endothelial pump function. move over a layer of fibronectin into the Beginning at the eighth week of gestation, primary corneal stroma to form a loosely endothelial cells deposit Descemet's mem­ arranged sheet of overlapping cells. 14 This brane. 28 This first appears as patches of lamel­ layer thins to a monolayer of endothelium by lar material and forms a complete layer by the eighth week of human gestation. sixteen weeks. Collagen is continuously Developmentally, it is not a true endothelium deposited thereafter until the eighth month of and should more correctly be called the pos­ gestation, by which time the membrane forms terior cell layer of the cornea or the posterior a layer approximately 3 [-lm thick. The col­ epithelium15 because its derivation is quite lagen of Descemet's membrane formed in distinct from that of vascular endothelium. utero has a banded appearance by electron Cells of a similar origin cover the anterior sur­ microscopy, with a micro periodicity of face of the iris and those in the anterior cham­ 110 [-lm. 29 In contrast, Descemet's membrane ber angle migrate peripherally to form the that is secreted subsequently is finely granular lining of the trabecular meshwork. 16,17 and consists largely of non-banded basement THE CORNEAL ENDOTHELIUM 391 Fig.2e. Fig.2a. Fig. 2. (a) Diagramatic representation of the migration of neural crest cells from a position dorsal to the neural tube to the posterior surface of the cornea, , { showing ectoderm (A), neural crest cells (B), neural � �"� ectoderm (C) and neural tube (D), (b) Outpouchings of :.\:��. the neuralectoderm at the level of the diencephalon form the optic vesicles which grow toward the surface ectoderm and induce the surface cells to elongate and form the lens placode, The diagram shows the optic vesicle (A), surface ectoderm ( B) and diencephalon (C). By a complex process of differential growth, the optic vesicles then invaginate to form the optic cups. The lens placode also invaginates and separates from the surface ectoderm to form the lens vesicle lying within the rim of the optic cup. The inner and outer cellular layers of the optic vesicles form the neuroretina and the retinal pigment epithelium respectively, and extend forward with the advancing rim of the optic cup to form elements of the iris. The epithelium of the cornea develops (following lens invagination) from surface ectoderm. (c) Crest cells move from a position between the surface Fig.2b. ectoderm and the neural tube to lie at the tip of the optic cup. They migrate over the posterior surface of the membrane. The granular portion of the mem­ cornea to form the corneal endothelium. The diagram shows the cornea (A), neural crest cells (B) and the lens brane accumulates throughout life and may (C). reach a thickness of between 10 and 40 flm. There is, however, a wide variation in the rate into old age.37,38.39 It has been estimated that at which Descemet's membrane is deposited, between the ages of and years the reduc­ and a measurement of its thickness does not 20 80 tion in cell density averages per year. 40 provide an accurate gauge as to a patients 0.52% As the mean age of a population sample age.30 increases, there is a spread in the range of their endothelial cell density counts,31 so that 2. Morphology the measurement of cell density is not a At birth, the human endothelium comprises a reliable index of the chronological age of a monolayer of up to 500,000 cells, with a cornea.
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