Adult neurogenesis in non-mammalian vertebrates

Adult neurogenesis is an exciting and rapidly advancing field of research. It addresses basic biological questions, such as the how and why of de novo neuronal production during adulthood, as well as medically relevant issues, including the potential link between adult neural stem cells and psychiatric disorders, or how stem cell manipulation might be used as a strategy for neuronal replacement. Current research mainly focuses on rodents, but we review here recent examination of non-mammalian vertebrates, which demonstrates that bona fide adult neural stem cells exist in these species. Importantly, especially in teleost fish, these cells can be abundant and located in various brain areas. Hence, non-mammalian vertebrate species provide invaluable comparative material for extracting core mechanisms of adult neural stem cell maintenance and fate.     

Molecular mechanisms of early neurogenesis in vertebrates

Recent studies revealed a great variety of genes which control the early development of the central nervous system in vertebrates, including neural induction and differentiation of primary neurons. Most of these genes were first identified inDrosophila melanogaster, then their structural and functional homologs were found in vertebrates. Modern data on the molecular-genetic mechanisms of vertebrate neurogenesis are reviewed. The neurogenetic mechanisms are compared for vertebrates and invertebrates. Widely discussed hypotheses are considered along with the commonly accepted mechanisms.     

The common properties of neurogenesis in the adult brain: from invertebrates to vertebrates

Until recently, it was believed that adult brains were unable to generate any new neurons. However, it is now commonly known that stem cells remain in the adult central nervous system and that adult vertebrates as well as adult invertebrates are currently adding new neurons in some specialized structures of their central nervous system. In vertebrates, the subventricular zone and the dentate gyrus of the hippocampus are the sites of neuronal precursor proliferation. In some insects, persistent neurogenesis occurs in the mushroom bodies, which are brain structures involved in learning and memory and considered as functional analogues of the hippocampus. In both vertebrates and invertebrates, secondary neurogenesis (including neuroblast proliferation and neuron differentiation) appears to be regulated by hormones, transmitters, growth factors and environmental cues. The functional implications of adult neurogenesis have not yet been clearly demonstrated and comparative study of the various model systems could contribute to better understand this phenomenon. Here, we review and discuss the common characteristics of adult neurogenesis in the various animal models studied so far.     

Early development and neurogenesis of Temnopleurus reevesii

Sea urchins are model non‐chordate deuterostomes, and studying the nervous system of their embryos can aid in the understanding of the universal mechanisms of neurogenesis. However, despite the long history of sea urchin embryology research, the molecular mechanisms of their neurogenesis have not been well investigated, in part because neurons appear relatively late during embryogenesis. In this study, we used the species Temnopleurus reevesii as a new sea urchin model and investigated the detail of its development and neurogenesis during early embryogenesis. We found that the embryos of T. reevesii were tolerant of high temperatures and could be cultured successfully at 15–30°C during early embryogenesis. At 30°C, the embryos developed rapidly enough that the neurons appeared at just after 24 h. This is faster than the development of other model urchins, such as Hemicentrotus pulcherrimus or Strongylocentrotus purpuratus. In addition, the body of the embryo was highly transparent, allowing the details of the neural network to be easily captured by ordinary epifluorescent and confocal microscopy without any additional treatments. Because of its rapid development and high transparency during embryogenesis, T. reevesii may be a suitable sea urchin model for studying neurogenesis. Moreover, the males and females are easily distinguishable, and the style of early cleavages is intriguingly unusual, suggesting that this sea urchin might be a good candidate for addressing not only neurology but also cell and developmental biology.     

Error in Estimation of Rate and Time Inferred from the Early Amniote Fossil Record and Avian Molecular Clocks

The best reconstructions of the history of life will use both molecular time estimates and fossil data. Errors in molecular rate estimation typically are unaccounted for and no attempts have been made to quantify this uncertainty comprehensively. Here, focus is primarily on fossil calibration error because this error is least well understood and nearly universally disregarded. Our quantification of errors in the synapsid–diapsid calibration illustrates that although some error can derive from geological dating of sedimentary rocks, the absence of good stem fossils makes phylogenetic error the most critical. We therefore propose the use of calibration ages that are based on the first undisputed synapsid and diapsid. This approach yields minimum age estimates and standard errors of 306.1±8.5 MYR for the divergence leading to birds and mammals. Because this upper bound overlaps with the recent use of 310 MYR, we do not support the notion that several metazoan divergence times are significantly overestimated because of serious miscalibration (sensu Lee 1999). However, the propagation of relevant errors reduces the statistical significance of the pre-K–T boundary diversification of many bird lineages despite retaining similar point time estimates. Our results demand renewed investigation into suitable loci and fossil calibrations for constructing evolutionary timescales.[Reviewing Editor: Martin Kreitman]     

Evolution and Development of Ventricular Septation in the Amniote Heart

During cardiogenesis the epicardium, covering the surface of the myocardial tube, has been ascribed several functions essential for normal heart development of vertebrates from lampreys to mammals. We investigated a novel function of the epicardium in ventricular development in species with partial and complete septation. These species include reptiles, birds and mammals. Adult turtles, lizards and snakes have a complex ventricle with three cava, partially separated by the horizontal and vertical septa. The crocodilians, birds and mammals with origins some 100 million years apart, however, have a left and right ventricle that are completely separated, being a clear example of convergent evolution. In specific embryonic stages these species show similarities in development, prompting us to investigate the mechanisms underlying epicardial involvement. The primitive ventricle of early embryos becomes septated by folding and fusion of the anterior ventricular wall, trapping epicardium in its core. This folding septum develops as the horizontal septum in reptiles and the anterior part of the interventricular septum in the other taxa. The mechanism of folding is confirmed using DiI tattoos of the ventricular surface. Trapping of epicardium-derived cells is studied by transplanting embryonic quail pro-epicardial organ into chicken hosts. The effect of decreased epicardium involvement is studied in knock-out mice, and pro-epicardium ablated chicken, resulting in diminished and even absent septum formation. Proper folding followed by diminished ventricular fusion may explain the deep interventricular cleft observed in elephants. The vertical septum, although indistinct in most reptiles except in crocodilians and pythonidsis apparently homologous to the inlet septum. Eventually the various septal components merge to form the completely septated heart. In our attempt to discover homologies between the various septum components we aim to elucidate the evolution and development of this part of the vertebrate heart as well as understand the etiology of septal defects in human congenital heart malformations.     

Early stress affects neurogenesis in the rat rostral migratory stream

Stressful experience during the early postnatal period may influence processes associated with neurogenesis (i.e. proliferation, cell death, appearance of astrocytes or cell differentiation) in the neonatal rat rostral migratory stream (RMS). To induce stress, pups were subjected to maternal deprivation daily for three hours, starting from the first postnatal day till the seventh postnatal day. Immunohistochemical methods were used to visualize proliferating cells and astrocytes; dying cells and nitrergic cells were visualized using histochemical staining. Quantitative analysis showed that maternal deprivation decreased the number of proliferating cells and significantly increased the number of dying cells in the RMS. Maternal deprivation did not influence the appearance of astrocytes in the RMS, but caused premature differentiation of nitrergic cells. In control rats, nitrergic cells can be observed in the RMS as early as the tenth postnatal day. In maternally deprived pups, these cells were detected as early as the seventh postnatal day. The observed earlier appearance of nitrergic cells in the RMS was associated with altered proliferation and increased cell dying and this observation supports the hypothesis that nitric oxide has an anti-proliferative role in the RMS. Our study demonstrates that maternal deprivation represents a stressful condition with a profound impact on early postnatal neurogenesis.     

Early Miocene vertebrates from Montagna della Maiella,Italy

Vertebrate remains from the lower Burdigalian (early Miocene) carbonates of Montagna della Maiella, central Italy, are described. These remains mostly consist of teeth belonging to 11 elasmobranch taxa (Carcharias acutissima, Carcharias cuspidata, Carcharodon subauriculatus, Isurushastalis, Isurus oxyrinchus, Isurus sp., Parotodus benedeni, Hemipristis serra, Galeocerdo aduncus, Galeocerdo contortus, Negaprion cf. eurybathrodon), eight teleost taxa (Diplodus sp. and two indeterminate sparids, Labrodon sp., Trigonodon jugleri, Sphyraena sp., Chilomycterus sp., Diodon sp.), an indeterminate crocodile, and two odontocete cetaceans (Squalodon sp. and an indeterminate kentriodontid). Paleoenvironmental and paleogeographical implications are discussed.     

Early neural development in vertebrates is also a matter of calcium

The calcium (Ca²⁺) signaling pathways have crucial roles in development from fertilization through differentiation to organogenesis. In the nervous system, Ca²⁺ signals are important regulators for various neuronal functions, including formation and maturation of neuronal circuits and long-term memory. However, Ca²⁺ signals are mainly involved in the earliest steps of nervous system development including neural induction, differentiation of neural progenitors into neurons, and the neuro-glial switch. This review examines when and how Ca²⁺ signals are generated during each of these steps with examples taken from in vivo studies in vertebrate embryos and from in vitro assays using embryonic and neural stem cells. Also discussed is the highly specific nature of the Ca²⁺ signaling pathway and its interaction with the other signaling pathways involved in early neural development.     

Early endoderm development in vertebrates: lineage differentiation and morphogenetic function

Gastrulation of the vertebrate embryo culminates in the formation of three primary germ layers: ectoderm, mesoderm and endoderm. The endoderm contributes to the lining of the gut and the associated organs. New components of the molecular pathway for endoderm specification have been identified in the zebrafish and Xenopus. In the mouse, the activity of orthologous factors is involved with the allocation and differentiation of the definitive endoderm. Morphogenetic interactions between the endoderm and the other germ layer derivatives are critical for the morphogenesis of head structures and organogenesis of gut derivatives.     

Early neurogenesis during caudal spinal cord regeneration in adult Gekko japonicus

Gekko japonicus undergoes dramatic changes in the caudal spinal cord after tail amputation. The amputation induces cell proliferation in the caudal ependymal tube. We performed hematoxylin and eosin staining at different time points in the regeneration process to investigate the morphological characterization of the regenerated appendages. The central canal extended to the blastema post-amputation and the cartilage and muscle tissue appeared 3 weeks after injury. We performed the bromodeoxyuridine (BrdU) incorporation assay to detect proliferating cells during the regeneration process. BrdU positive cells were detected in the peri-central canal. Furthermore, nestin and neuron-specific enolase (NSE) immunocytochemistry were applied to detect neural stem/progenitor cells and neurons. Two weeks after injury, nestin-positive cells undergoing proliferation were located outside of the ependymal tube, and NSE positive cells appeared after 3 weeks of amputation. These data suggest that neurogenesis is an early event during caudal spinal cord regeneration in gecko.