Abstract
Interkinetic nuclear migration (INM) is a well-known phenomenon that accompanies progenitor expansion in the vertebrate neural tube and non-neural ectoderm-derived epithelial tissues. In INM, progenitor cell nuclei migrate along the apicobasal axis of the epithelial layer in synchrony with cell cycle progression, resulting in ‘pseudostratification’. Although INM has long been considered a general feature of epithelial development, detailed characteristics of INM in the gut and ureteric epithelia are little known. In this study, we observe pseudostratification in the developing midgut and ureteric epithelial progenitors by scanning electron microscopy and assess their cell cycle duration by 5-bromo-2′-deoxyuridine labeling. By applying multi-dimensional scaling, we demonstrate the roundtrip migration of nuclei between the basement membrane and the apical side in the developing midgut. Partial INM has been also shown for the ureteric epithelial nuclei. Our findings reveal INM in gut and ureteric progenitors that is similar to that in ventricular neurogenesis, and suggest that INM is a general strategy for the expansion of epithelial progenitors.
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References
Barcia E, Ayucar E, Huelin J, Ayucar L (1977) Interkinetic nuclear migration in nasal placode of chick embryo. Experientia 33:1515–1516
Baye LM, Link BA (2007) Interkinetic nuclear migration and the selection of neurogenic cell divisions during vertebrate retinogenesis. J Neurosci 27:10143–10152
Bort R, Signore M, Tremblay K, Martinez barbera JP, Zaret KS (2006) Hex homeobox gene controls the transition of the endoderm to a pseudostratified, cell emergent epithelium for liver bud development. Dev Biol 290:44–56
Cervantes S, Yamaguchi TP, Hebrok M (2009) Wnt5a is essential for intestinal elongation in mice. Dev Biol 326:285–294
Fish JL, Dehay C, Kennedy H, Huttner WB (2008) Making bigger brains-the evolution of neural-progenitor-cell division. J Cell Sci 121:2783–2793
Ge X, Frank CL, Calderon de Anda F, Tsai LH (2010) Hook3 interacts with PCM1 to regulate pericentriolar material assembly and the timing of neurogenesis. Neuron 65:191–203
Grosse AS, Pressprich MF, Curley LB, Hamilton KL, Margolis B, Hildebrand JD, Gumucio DL (2011) Cell dynamics in fetal intestinal epithelium: implications for intestinal growth and morphogenesis. Development 138:4423–4432
Hatta T, Moriyama K, Nakashima K, Taga T, Otani H (2002) The role of gp130 in cerebral cortical development: in vivo functional analysis in a mouse exo utero system. J Neurosci 22:5516–5524
Huelin J, Ayucar E (1977) Interkinetic migration of the auditory placode in the chick embryo. Bull Assoc Anat (Nancy) 61:147–154
Johnson RA, Wichern DW (2007) Applied multivariate statistical analysis. Pearson Prentice Hall, Upper Saddle River
Lai SL, Chien AJ, Moon RT (2009) Wnt/Fz signaling and the cytoskeleton: potential roles in tumorigenesis. Cell Res 19:532–545
Matsumoto A, Hashimoto K, Yoshioka T, Otani H (2002) Occlusion and subsequent re-canalization in early duodenal development of human embryos: integrated organogenesis and histogenesis through a possible epithelial–mesenchymal interaction. Anat Embryol (Berlin) 205:53–65
Matsuyama M, Aizawa S, Shimono A (2009) Sfrp controls apicobasal polarity and oriented cell division in developing gut epithelium. PLoS Genet 5:e1000427
Mellad JA, Warren DT, Shanahan CM (2011) Nesprins LINC the nucleus and cytoskeleton. Curr Opin Cell Biol 23:47–54
Merchant H, Zarco W, Bartolo R, Prado L (2008) The context of temporal processing is represented in the multidimensional relationships between timing tasks. PLoS ONE 3:e3169
Minami Y, Oishi I, Endo M, Nishita M (2010) Ror-family receptor tyrosine kinases in noncanonical Wnt signaling: their implications in developmental morphogenesis and human diseases. Dev Dyn 239:1–15
Nishita M, Yoo SK, Nomachi A, Kani S, Sougawa N, Ohta Y, Takada S, Kikuchi A, Minami Y (2006) Filopodia formation mediated by receptor tyrosine kinase Ror2 is required for Wnt5a-induced cell migration. J Cell Biol 175:555–562
Nomachi A, Nishita M, Inaba D, Enomoto M, Hamasaki M, Minami Y (2008) Receptor tyrosine kinase Ror2 mediates Wnt5a-induced polarized cell migration by activating c-Jun N-terminal kinase via actin-binding protein filamin A. J Biol Chem 283:27973–27981
Norden C, Young S, Link BA, Harris WA (2009) Actomyosin is the main driver of interkinetic nuclear migration in the retina. Cell 138:1195–1208
Otani H, Yoneyama T, Hashimoto R, Hatta T, Tanaka O (1993) Ultrastructure of the developing stomach in human embryos. Anat Embryol (Berlin) 187:145–151
Otani H, Udagawa J, Hatta T, Kagohashi Y, Hashimoto R, Matsumoto A, Satow F, Nimura M (2010) Individual variation in organ histogenesis as a causative factor in the developmental origins of health and disease: unnoticed congenital anomalies? Congenit Anom 50:205–211
Sauer FC (1935) Mitosis in the neural tube. J Comp Neurol 62:377–405
Sauer FC (1936) The interkinetic migration of embryonic epithelial nuclei. J Morphol 60:1–11
Schenk J, Wilsch-Brauninger M, Calegari F, Huttner WB (2009) Myosin II is required for interkinetic nuclear migration of neural progenitors. Proc Natl Acad Sci USA 106:16487–16492
Sidman RL, Miale IL, Feder N (1959) Cell proliferation and migration in the primitive ependymal zone: an autoradiographic study of histogenesis in the nervous system. Exp Neurol 1:322–333
Smart IH (1972) Proliferative characteristics of the ependymal layer during the early development of the mouse diencephalon, as revealed by recording the number, location, and plane of cleavage of mitotic figures. J Anat 113:109–129
Takahashi T, Nowakowski RS, Caviness VS Jr (1993) Cell cycle parameters and patterns of nuclear movement in the neocortical proliferative zone of the fetal mouse. J Neurosci 13:820–833
Takahashi T, Nowakowski RS, Caviness VS Jr (1995) The cell cycle of the pseudostratified ventricular epithelium of the embryonic murine cerebral wall. J Neurosci 15:6046–6057
Taverna E, Huttner WB (2010) Neural progenitor nuclei IN motion. Neuron 67:906–914
Udagawa J, Yasuda A, Naito K, Otani H (2010) Analysis of the harmonized growth pattern of fetal organs by multidimensional scaling and hierarchical clustering. Congenit Anom 50:175–185
Wake K, Hatta T, Udagawa J, Igawa M, Otani H (2004) Cell proliferation and migration in the developing human upper urinary tract. Anat Sci Int 79:367
Xie Z, Moy LY, Sanada K, Zhou Y, Buchman JJ, Tsai L-H (2007) Cep120 and TACCs control interkinetic nuclear migration and the neural progenitor pool. Neuron 56:79–93
Yamada M, Udagawa J, Matsumoto A, Hashimoto R, Hatta T, Nishita M, Minami Y, Otani H (2010a) Ror2 is required for midgut elongation during mouse development. Dev Dyn 239:941–953
Yamada M, Wake K, Udagawa J, Hatta T, Hashimoto R, Matsumoto A, Shiina H, Igawa M, Otani H (2010b) Epithelial cell rearrangement contributes to ureteral elongation in human and mouse embryos. Congenit Anom 50:A9–A10
Zwaan J, Bryan PR Jr, Pearce TL (1969) Interkinetic nuclear migration during the early stages of lens formation in the chicken embryo. J Embryol Exp Morphol 21:71–83
Acknowledgments
We thank Yumiko Takeda for her excellent tissue processing and Tsunao Yoneyama for his technical assistance with SEM. Grant sponsor: Ministry of Education, Culture, Sports, Science, and Technology, Japan; Grant number: Grant-in-Aid for Scientific Research (No. 23112006) (Hiroki Otani).
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Yamada, M., Udagawa, J., Hashimoto, R. et al. Interkinetic nuclear migration during early development of midgut and ureteric epithelia. Anat Sci Int 88, 31–37 (2013). https://doi.org/10.1007/s12565-012-0156-8
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DOI: https://doi.org/10.1007/s12565-012-0156-8