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Neurulation and Neural Tube Defects

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Neurulation and Neural Tube Defects Chapter 4 Neurulation and Neural Tube Defects Hans J.ten Donkelaar,Reinier A.Mullaart,Akira Hori and Kohei Shiota 4.1 Introduction non-separation of neural and surface ectoderm,lead- ing to defects in the formation of the skull (Campbell Neurulation is usually described as the developmen- et al. 1986; Vermeij-Keers 1990). The term dysraphia tal process that results in the rolling up of a flat sheet is used for malformations appearing prenatally that of epithelial cells into an elongated tube (Gilbert involve a disturbance of neurulation and/or a defect 2000; Colas and Schoenwolf 2001). Neurulation has in the skeletal surroundings. The disturbance of a been extensively studied in amphibian, avian and median seam or raphe, whether neural or skeletal, mammalian embryos and occurs in four stages: for- which normally ensures closure of the CNS from the mation of the neural plate, shaping of the neural surface, may affect the cranial or the spinal region, or plate, bending of the neural plate and closure of the both. Four main types of NTDs are found at the cra- neural groove. The rostral part of the neural tube de- nial and spinal level (Norman et al. 1995; Naidich et velops into the brain, whereas the caudal part be- al. 1996; Aicardi 1998; Barkovich 2000; O’Rahilly and comes the spinal cord. This is the primary type of Müller 2001): (1) the neural plate remaining open neurulation. In fish, the neural tube does not form (anencephaly and myeloschisis, respectively); (2) the from an infolding of the overlying ectoderm, but in- neural tube being exteriorized (encephalomeningo- stead forms from a solid cord of cells. This cord sub- cele and myelomeningocele); (3) only meninges be- sequently becomes cavitated. In birds and mammals, ing exteriorized (cranial and spinal meningoceles); the most caudal part of the neural tube forms by ag- and (4) merely a skeletal defect being evident (crani- gregation of cells, as part of the caudal eminence, in- um bifidum occultum and spina bifida occulta). to a medullary cord which then cavitates and con- Spinal lipomas occur with occult spinal dysraphism nects to the main neural tube. This process is called as well as in cases of open NTDs, and lie dorsal to the secondary neurulation. defect. Split cord malformations may be associated Neural tube defects (NTDs) are among the most with NTDs and probably occur before neural tube clo- common human malformations,with an incidence of sure (Pang et al. 1992). They are discussed in Chap. 6. 1–5 per 1,000 live births. Striking variation in inci- This chapter presents an overview of primary dence exists between populations, varying from 1 in and secondary neurulation, a discussion of genetic 3,000 in the low-risk Finnish population to more than mouse models for NTDs, recognized causes of NTDs 1 in 300 in high-risk areas in Ireland and the UK and a discussion of the human NTDs, including cra- (Dolk et al. 1991). Approximately 85% of NTDs may nial NTDs, spinal NTDs, the Chiari malformations be the result of a combined influence of environmen- and caudal dysgenesis syndromes. tal and genetic factors, indicating a multifactorial ae- tiology (Copp and Bernfield 1994). Over the past few decades there has been a worldwide decline in the 4.2 Primary Neurulation number of NTD births, due mainly to the introduc- tion of ultrasound screening as part of routine prena- 4.2.1 Primary Neurulation in Chick tal care, followed by therapeutic termination of preg- and Mammalian Embryos nancies, and primary prevention through folic acid supplementation during early pregnancy (Czeizel The process of primary neurulation appears to be and Dudás 1992). No precise definition of NTDs ex- similar in amphibian, avian and mammalian em- ists, since they include a very heterogeneous group of bryos (Balinsky 1965; Karfunkel 1974; Gilbert 2000). defects. Usually, NTDs are defined as a group of de- With scanning electron microscopy the key events of fects in which the neural tube has failed to complete neural tube formation have been studied. In chick neurulation and one or more of the neural tube cov- embryos, Schoenwolf and co-workers (Schoenwolf erings are incomplete (Norman et al. 1995). In most and Smith 1990; Schoenwolf 1994; Smith and Schoen- cases this failure leads to exposure of a portion of the wolf 1997; Colas and Schoenwolf 2001; Lawson et al. neural tube at the body surface.This definition allows 2001) showed four distinct but spatially and tempo- inclusion of encephaloceles, cranial and spinal rally overlapping stages of neurulation (Fig. 4.1). meningoceles, and myelocystoceles. Most encephalo- First,formation of the neural plate is induced early in celes may arise after neural tube closure, owing to embryogenesis (Chap. 2) and the ectoderm thickens. 146 Chapter 4 Neural Tube Defects Fig. 4.1 Morphogenetic events during chick neurulation: a shap- ing, folding, elevation and conver- gence of the neural plate at the future midbrain/hindbrain level; b the hinge point model of bend- ing of the chick neural plate. Neu- roepithelial cell wedging (black) within the dorsolateral and medi- an hinge points is indicated. Arrows indicate the mediolateral expansion of the surface ecto- derm. DLHP dorsolateral hinge point, MHP median hinge point, nch notochord, se surface ecto- derm. (After Schoenwolf 1994; Smith and Schoenwolf 1997) During this stage, the neuroectodermal cells of the sent, brings the lateral walls of the developing neural forming neural plate increase in height and undergo tube into contact with the midline, leading to a slit- pseudostratification. Second, shaping of the neural like neural tube lumen. In contrast, at future brain plate begins, leading to rostrocaudal lengthening, levels, the neural folds undergo a second, convergent, mediolateral narrowing and further apicobasal medial folding along the longitudinal axis, which thickening, except in the midline, where it becomes brings them together in the dorsal midline and gen- anchored to the notochord and midline neuroepithe- erates a broad lumen. Fusion of the neural folds lial cells shorten and become wedge-shaped. Togeth- forms the fourth stage of neurulation. During this er, these form-shaping events modify the original flat stage, the non-neural or future surface ectoderm neural plate so that subsequent bending produces an from each fold detaches from the neuroepithelium elongated neural tube. Third, bending of the neural and fuses with the non-neural ectoderm of the other plate begins during shaping and involves the follow- fold. This process is known as disjunction.Both de- ing morphogenetic events: (1) formation of hinge tached neuroepithelial layers fuse deep to the surface points; (2) formation of the neural folds; and (3) fold- ectoderm and form the roof plate of the neural tube. ing of the neural plate. The hinge points, one median In chick embryos, the first closure of the neural tube and two dorsolateral, are areas of the neural plate at- occurs in the future mesencephalon, and a second tached to adjacent tissues. The median hinge point closure is found at the rhombo-cervical level as mul- (MHP) is attached to the underlying prechordal plate tiple contacts between the neural folds (van Straaten rostrally and the notochord caudally. In the avian et al. 1996, 1997). embryo, the paired dorsolateral hinge points (DLH- Neurulation is a multifactorial process that re- Ps) are present only at future brain and rhomboid quires both extrinsic and intrinsic forces acting in sinus levels. They are attached to adjacent epidermal concert (Schoenwolf and Smith 1990). Intrinsic ectoderm. Within the hinge points, the neuroepithe- forces arise within the neural plate and drive neural lial cells become wedge-shaped and the neural plate plate shaping and furrowing,whereas extrinsic forces undergoes longitudinal furrowing. The morphology arise outside the neural plate and drive neural plate of the neural folds differs rostrocaudally. At the fu- folding and neural groove closure. The intrinsic ture brain level, the neural (or head) folds are broad, forces responsible for neural plate shaping and fur- mediolaterally elongated structures, whereas at the rowing are generated by fundamental changes in cell future spinal cord level they are much narrower. shape, position and number of neuroepithelial cells Peculiar to avian embryos is the rhomboid sinus, (Schoenwolf and Smith 1990; Smith and Schoenwolf near the closing caudal neuropore, where the neural 1997). At the hinge points, the majority of neuro- folds are relatively broad compared with the width of epithelial cells become wedge-shaped (Fig. 4.1b). the neural plate. Folding of the neural plate occurs in Neuroepithelial cells also undergo two rounds of re- temporal and spatial relationship to formation of the arrangement during neurulation (Schoenwolf and hinge points (Fig. 4.1). After the MHP has formed, Alvarez 1989). The neural plate undergoes a halving both sides of the neural plate undergo dorsal eleva- of its width and a corresponding doubling of its tion along the longitudial axis,resulting in the forma- length during each round. In amphibian embryos, tion of the neural groove. Continued elevation at the this rearrangement of neuroepithelial cells probably future spinal cord level, where true DLHPs are ab- provides the major intrinsic force for rostrocaudal 4.2 Primary Neurulation 147 lengthening of the neural plate (Jacobson 1994). In initiation site is found at the rostral end of the neural birds and mammals, moreover, substantial cell divi- plate (closure 3). Therefore, in mouse embryos at sion occurs within the neural plate during neurula- some stage of development, two prominent openings tion (Tuckett and Morriss-Kay 1985; Smith and are recognized simultaneously, one over the prosen- Schoenwolf 1987, 1988). Tissue transplantation ex- cephalon, rostral to the second closure, and the other periments in chick embryos suggest that neural plate over the mesencephalon–rhombencephalon.
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