Analysis of hindbrain neural crest migration in the long-tailed monkey (Macaca fascicularis)
Tóm tắt
Neural crest cells make a substantial contribution to normal craniofacial development. Despite advances made in identifying migrating neural crest cells in avian embryos and, more recently, rodent embryos, knowledge of crest cell migration in primates has been limited to what was obtained by conventional morphological techniques. In order to determine the degree to which the nonhuman primate fits the mammalian pattern, we studied the features of putative neural crest cell migration in the hindbrain of the long-tailed monkey (Macaca fascicularis) embryo. Cranial crest cells were identified on the basis of reported distributional and morphological criteria as well as by immunocytochemical detection of the neural cell adhesion molecule (N-CAM) that labels a subpopulation of these cells. The persistent labeling of a sufficient number of crest cells with antibodies to N-CAM following their exit from the rostral, preotic and post-otic regions of the hindbrain facilitated tracking them along subectodermal pathways to their respective destinations in the first, second and third pharyngeal arches. Peroxidase immunocytochemistry was also employed to localize laminin and collagen-IV in neuroepithelial basement membranes. At stage 10 (8–11 somites), crest emigration occurred in areas of unfused neural folds through focal disruptions in the neuroepithelial basement membrane in both the rostral and pre-otic regions, although there was little evidence of crest migration in the post-otic hindbrain. By stage 11 (16–17 somites), the neural folds were fused (pre- and post-otic hindbrain) or in the process of fusing (rostral hindbrain), yet crest cell emigration was apparent in all three areas through discontinuities in the basement membrane. Emigration was essentially complete at stage 12 (21 somites) as indicated by nearly continuous cranial neural tube basement membranes. At this stage the pre-ganglia (trigeminal, facioacoustic and glossopharyngeal) were consistently stained with N-CAM. The current study has provided new information on mammalian neural crest in a well-established experimental model for normal and abnormal human development, including its use as a model for the retinoic acid syndrome. In this regard, the current results provide the basis for probing the mechanisms of retinoid embryopathy which may involve perturbation of hindbrain neural crest development.
Tài liệu tham khảo
Akitaya T, Bronner-Fraser M (1992) Expression of cell adhesion molecules during initiation and cessation of neural crest cell migration. Dev Dyn 194:12–29
Anderson CB, Meier S (1981) The influence of the metameric pattern in the mesoderm on migration of cranial neural crest cells in the chick embryo. Dev Biol 85:385–402
Bartelmez GW, Evans HM (1926) Development of the human embryo during the period of somite formation, including embryos with 2 to 16 pairs of somites. Contrib Embryol 17:1–67
Baxter JS, Boyd JD (1939) Observations on the neural crest of a ten-somite human embryo. J Anat 73:318–326
Birgbauer E, Sechrist J, Bronner-Fraser M, Fraser S (1995) Rhombomeric origin and rostrocaudal reassortment of neural crest cells revealed by intravital microscopy. Development 121:935–945
Bronner-Fraser M (1994) Neural crest cell formation and migration in the developing embryo. FASEB J 8:699–706
Bronner-Fraser M, Wolf JJ, Murray BA (1992) Effects of antibodies against N-cadherin and N-CAM on the cranial neural crest and neural tube. Dev Biol 153:291–301
Chan WY, Tam PPL (1988) A morphological and experimental study of the mesencephalic neural crest cells in the mouse embryo using wheat germ agglutinin-gold conjugate as the cell marker. Development 102:427–442
Cole GJ, Burg M (1989) Characterization of a heparan sulfate proteoglycan that copurifies with the neural cell adhesion molecule. Exp Cell Res 182:44–60
Cole GJ, Loewy A, Glaser L (1986) Neuronal cell-cell adhesion depends on interactions of N-CAM with heparin-like molecules. Nature 320:445–447
de Virgilio G, Lavenda N, Worden JL (1967) Sequence of events in neural tube closure and the formation of neural crest in the chick embryo. Acta Anat 68:127–146
Edelman GM, Crossin KL (1991) Cell adhesion molecules: implications for a molecular histology. Annu Rev Biochem 60:155–190
Engvall E, Davis GE, Kickerson K, Ruoslahti E, Varon S, Manthorpe M (1986) Mapping of domains in human laminin using monoclonal antibodies: localization of the neurite-promoting site. J Cell Biol 103:2457–2465
Erickson CA, Perris R (1993) The role of cell-cell and cell-matrix interactions in the morphogenesis of the neural crest. Dev Biol 159:60–74
Foellmer HG, Madri JA, Furthmayr H (1983) Monoclonal antibodies to type IV collagen: probes for the study of structure and function of basement membranes. Lab Invest 48:639–649
Fukiishi Y, Morriss-Kay GM (1992) Migration of cranial neural crest cells to the pharyngeal arches and heart in rat embryos. Cell Tissue Res 268:1–8
Gasser RF (1975) Atlas of human embryos. Harper & Row, New York
Hall BK, Horstadius S (1988) The neural crest. Oxford University Press, Oxford, New York
Hendrickx AG, Binkerd PE (1990) Nonhuman primates and teratological research. J Med Primatol 19:81–108
Hendrickx AG, Cukierski MA (1987) Reproductive and developmental toxicology in nonhuman primates. In: Graham R (ed) Preclinical safety of biotechnology products intended for human use. Liss, New York, pp 73–88
Hendrickx AG, Hummler H (1992) Teratogenicity of all-trans retinoic acid during early embryonic development in the cynomolgus monkey (Macaca fascicularis). Teratology 45:65–74
Hummler H, Korte R, Hendrickx AG (1990) Induction of malformations in the cynomolgus monkey with 13-cis retinoic acid. Teratology 42:263–272
Innes PB (1985) The ultrastructure of early cephalic neural crest cell migration in the mouse. Anat Embryol 172:33–38
Kimura Y, Matsunami H, Inoue T, Shimamura K, Uchida N, Ueno T, Miyazaki T, Takeichi M (1995) Cadherin-11 expressed in association with mesenchymal morphogenesis in the head, somite, and limb bud of early mouse embryos. Dev Biol 169:347–358
Lammer EJ, Chen DT, Hoar RM, Agnish ND, Benke PJ, Braun JT, Curry CJ, Fernhoff PM, Grix AW, Lott IT, Richard JM, Sun SC (1985) Retinoic acid embryopathy. N Engl J Med 313:837–841
Lanier LL, Chang C, Azuma M, Ruitenberg JJ, Hemperly JJ, Phillips JH (1991) Molecular and functional analysis of human natural killer cell-associated neural-cell adhesion molecule (NCAM/CD56). J Immunol 146:4421–4426
Le Douarin N (1982) The neural crest. Cambridge University Press, Cambridge
Lee YM, Osumi-Yamashita N, Ninomiya Y, Moon CK, Eriksson U, Eto K (1995) Retinoic acid stage-dependently alters the migration pattern and identity of hindbrain neural crest cells. Development 121:825–837
Lumsden A, Sprawson N, Graham A (1991) Segmental origin and migration of neural crest cells in the hindbrain region of the chick embryo. Development 113:1281–1291
Morriss-Kay G, Tuckett F (1991) Early events in craniofacial morphogenesis. J Craniofac Genet Dev Biol 11:181–191
Morriss-Kay G, Ruberte E, Fukiishi Y (1993) Mammalian neural crest and neural crest derivatives. Ann Anat 175:501–507
Morriss-Kay G, Wood H, Chen W-H (1994) Normal neurulation in mammals. In: Neural tube defects. Ciba Foundation Symposium 181, Wiley, Chichester, New York, pp 51–69
Müller F, O'Rahilly R (1985) The first appearance of the neural tube and optic primordium in the human embryo at stage 10. Anat Embryol 172:157–169
Müller F, O'Rahilly R (1986) The development of the human brain and the closure of the rostral neuropore at stage 11. Anat Embryol 175:205–222
Müller F, O'Rahilly R (1987) The development of the human brain, the closure of the caudal neuropore, and the beginning of secondary neurulation at stage 12. Anat Embryol 176:413–430
Nakagawa S, Takeichi M (1995) Neural crest cell-cell adhesion controlled by sequential and subpopulation-specific expression of novel cadherins. Development 121:1321–1332
Newgreen DF, Tan SS (1993) Adhesion molecules in neural crest development. Pharmacol Ther 60:517–537
Nichols DH (1981) Neural crest formation in the head of the mouse embryo as observed using a new histological technique. J Embryol Exp Morphol 64:105–120
Nichols DH (1986) Formation and distribution of neural crest mesenchyme to the first pharyngeal arch region of the mouse embryo. Am J Anat 176:221–231
Nichols D (1987) Ultrastructure of neural crest formation in the midbrain/rostral hindbrain and preotic hindbrain regions of the mouse embryo. Am J Anat 179:143–154
O'Rahilly R (1965) The optic, vestibulocochlear, and terminal-vomernasal neural crest in staged human embryos. In: Rohen JW (eds) The structure of the eye. Schattauer, Stuttgart, pp 557–564
Peterson PE, Pow CST, Wilson DB, Hendrickx AG (1993) Distribution of extracellular matrix components during early embryonic development in the macaque. Acta Anat 146:3–13
Peterson PE, Pow CST, Wilson DB, Hendrickx AG (1995) Localisation of glycoproteins and glycosaminoglycans during early eye development in the macaque. J Anat 186:31–42
Poelmann RE, Gittenberger-de Groot AC, Mentink MMT, Delpech B, Girard N, Christ B (1990) The extracellular matrix during neural crest formation and migration in rat embryos. Anat Embryol 182:29–39
Pratt RM, Goulding EH, Abbott BD (1987) Retinoic acid inhibits migration of cranial neural crest cells in the cultured mouse embryo. J Craniofac Genet Dev Biol 7:205–217
Probstmeier R, Kühn K, Schachner M (1989) Binding properties of the neural cell adhesion molecule to different components of the extracellular matrix. J Neurochem 53:1794–1801
Probstmeier R, Fahrig T, Spiess E, Schachner M (1992) Interactions of the neural cell adhesion molecule and the myelin-associated glycoprotein with collagen type I: involvement in fibrillogenesis. J Cell Biol 116:1063–1070
Rutishauser U (1992) N-CAM and its polysialic acid moiety: a mechanism for pull/push regulation of cell interactions during development? Development [Suppl] 1992:99–104
Sainte-Marie G (1962) A paraffin embedding technique for studies employing immunofluorescence. J Histochem 10:250–256
Sechrist J, Serbedzija GN, Scherson T, Fraser SE, Bronner-Fraser M (1993) Segmental migration of the hindbrain neural crest does not arise from its segmental generation. Development 118:691–703
Serbedzija GN, Bronner-Fraser M, Fraser SE (1992) Vital dye analysis of cranial neural crest cell migration in the mouse embryo. Development 116:297–307
Sulik KK, Johnston MC, Smiley SJ, Speight HS, Jarvis BE (1987) Mandibulofacial dysostosis (Treacher Collins syndrome): a new proposal for its pathologenesis. Am J Med Genet 27:359–372
Tan SS, Morriss-Kay G (1985) The development and distribution of the cranial neural crest in the rat embryo. Cell Tissue Res 240:403–416
Tan SS, Morriss-Kay GM (1986) Analysis of cranial neural crest cell migration and early fates in postimplantation rat chimeras. J Embryol Exp Morphol 98:21–58
Thiery JP, Duband J-L, Rutishauser U, Edelman CM (1982) Cell adhesion molecules in early chicken embryogenesis. Proc Natl Acad Sci USA 79:6737–6741
Tosney KW (1982) The segregation and early migration of cranial neural crest cells in the avian embryo. Dev Biol 89:13–24
Trainor PA, Tam PPL (1995) Cranial paraxial mesoderm and neural crest cells of the mouse embryo: co-distribution in the craniofacial mesenchyme but distinct segregation in branchial arches. Development 121:2569–2582
Tuckett F, Morriss-Kay GM (1986) The distribution of fibronectin, laminin and entactin in the neurulating rat embryo studied by indirect immunofluorescence. J Embryol Exp Morphol 94:95–112
Waterman RE, Balian G (1980) Indirect immunofluorescent staining of fibronectin associated with the floor of the foregut during formation and rupture of the oral membrane in the chick embryo. Anat Rec 198:619–635
Webster WS, Johnston MC, Lammer EJ, Sulik KK (1986) Isotretinoin embryopathy and the cranial neural crest: an in vivo and in vitro study. J Craniofac Genet Dev Biol 6:211–222
