The proliferative ventricular zone in adult vertebrates: a comparative study using reptiles, birds, and mammals
Introduction
During embryonic development of the vertebrate brain, the vast majority of cells arise from multipotent stem cells located in the germinal layer of the telencephalic ventricles. The ventricles are formed by the folding of the epithelial ectoderm during the first stages of embryonic development. The cell layer surrounding the ventricles has been termed ventricular zone (VZ) [16]. The VZ consists of a pseudostratified columnar epithelium of proliferating radial cells adjacent to the brain ventricles. These radial cells give rise to almost all the neurons of the brain. The new neurons migrate both radially and tangentially to reach their final destinations. During radial migration, radial glial processes, which extend from the VZ to the pial surface, form a scaffolding used by migrating cells to reach their final destination in the brain parenchyma 18, 30, 38, 67. In contrast, in tangential migration cells disperse without following the radial pathways [62]. The mechanisms responsible for the new neurons’ commitment to one of these two migrating modes remain unknown. Both tangential and radial migration persist in all adult vertebrates for which data are available 23, 50, 73.
Until recently it was generally believed that the VZ disappeared as brain histogenesis came to an end and was transformed into the ependymal layer, which is composed of cells that do not divide 16, 40. However, it is now well established that in all major groups of vertebrates the VZ persists into adulthood albeit with a reduction in volume 1, 4, 65. Moreover, the actively proliferating zones responsible for adult neurogenesis in all vertebrate taxa studied to date are located, with few exceptions, in the VZ 5, 7, 49 (Fig. 1). While in reptiles and birds the area in contact with the ventricle is known as the VZ, in mammals a distinction is made between two regions: (1) the VZ, which is directly in contact with the ventricular lumen; and (2) the subventricular zone (SVZ), adjacent to the VZ, where the proliferating population of cells is found.
We present here a brief review of what is known about the organization and cellular composition of the walls of the lateral ventricles in the three living classes of amniotic vertebrates: reptiles, birds, and mammals. The identity of the primary neural precursors (stem cells) in the adult vertebrate brain is currently a much debated topic 13, 78. The comparative study of this structure might yield important clues about the morphology of the stem cells. These precursors are of interest not only for their role in adult neurogenesis, but also because of their potential use in therapeutic neuronal replacement [45].
Section snippets
Adult neurogenesis in vertebrates
Over the last decades, reports of abundant neurogenesis in all major vertebrate taxa have contributed to the demise of the long-held dogma that the brain is incapable of cell renewal during adulthood 5, 7, 37. In addition to the evidence for adult neurogenesis in a few areas of the mammalian brain 26, 35, 63, numerous studies have documented widespread neurogenesis in non-mammals, such as fish, 15, 69, 82, amphibians [70], reptiles 51, 52, and birds 33, 56, 57, 59, 74. Unfortunately, research
Reptiles
Data on the cellular composition and organization of the VZ in reptiles are available for three species of lizards and one turtle species 51, 52, 64, 65. The lizard VZ has been analyzed at the electron microscopic level using proliferation and immunocytochemical markers. Recently, serial ultrathin sections have also been used to reconstruct the composition and three-dimensional organization of the ventricular wall in the lizard Podarcis hispanica. The VZ ependyma displays regional variation and
Concluding remarks
The evidence reviewed above confirms that the epithelium lining the ventricular walls retains the functional and anatomical characteristics of a VZ in representatives of all major groups of amniotic vertebrates. The fact that ependymal cells (Type E) and neural stem cells (Type B) are present in the same epithelium suggests that neurogenic and ependymal functions can coexist. Our results suggest that these two functions may be segregated among two different kinds of cells within the same
Acknowledgements
This work has been supported by a grant from the Generalitat Valenciana (GV01-229).
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