Skip to main content
Top
Published in: Anatomical Science International 1/2013

01-01-2013 | Original Article

Interkinetic nuclear migration during early development of midgut and ureteric epithelia

Authors: Makiko Yamada, Jun Udagawa, Ryuju Hashimoto, Akihiro Matsumoto, Toshihisa Hatta, Hiroki Otani

Published in: Anatomical Science International | Issue 1/2013

Login to get access

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.
Literature
go back to reference Barcia E, Ayucar E, Huelin J, Ayucar L (1977) Interkinetic nuclear migration in nasal placode of chick embryo. Experientia 33:1515–1516PubMedCrossRef Barcia E, Ayucar E, Huelin J, Ayucar L (1977) Interkinetic nuclear migration in nasal placode of chick embryo. Experientia 33:1515–1516PubMedCrossRef
go back to reference Baye LM, Link BA (2007) Interkinetic nuclear migration and the selection of neurogenic cell divisions during vertebrate retinogenesis. J Neurosci 27:10143–10152PubMedCrossRef Baye LM, Link BA (2007) Interkinetic nuclear migration and the selection of neurogenic cell divisions during vertebrate retinogenesis. J Neurosci 27:10143–10152PubMedCrossRef
go back to reference 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 290:44–56PubMedCrossRef 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 290:44–56PubMedCrossRef
go back to reference Cervantes S, Yamaguchi TP, Hebrok M (2009) Wnt5a is essential for intestinal elongation in mice. Dev Biol 326:285–294PubMedCrossRef Cervantes S, Yamaguchi TP, Hebrok M (2009) Wnt5a is essential for intestinal elongation in mice. Dev Biol 326:285–294PubMedCrossRef
go back to reference Fish JL, Dehay C, Kennedy H, Huttner WB (2008) Making bigger brains-the evolution of neural-progenitor-cell division. J Cell Sci 121:2783–2793PubMedCrossRef Fish JL, Dehay C, Kennedy H, Huttner WB (2008) Making bigger brains-the evolution of neural-progenitor-cell division. J Cell Sci 121:2783–2793PubMedCrossRef
go back to reference 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 65:191–203PubMedCrossRef 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 65:191–203PubMedCrossRef
go back to reference 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 138:4423–4432PubMedCrossRef 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 138:4423–4432PubMedCrossRef
go back to reference 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 22:5516–5524PubMed 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 22:5516–5524PubMed
go back to reference Huelin J, Ayucar E (1977) Interkinetic migration of the auditory placode in the chick embryo. Bull Assoc Anat (Nancy) 61:147–154 Huelin J, Ayucar E (1977) Interkinetic migration of the auditory placode in the chick embryo. Bull Assoc Anat (Nancy) 61:147–154
go back to reference Johnson RA, Wichern DW (2007) Applied multivariate statistical analysis. Pearson Prentice Hall, Upper Saddle River Johnson RA, Wichern DW (2007) Applied multivariate statistical analysis. Pearson Prentice Hall, Upper Saddle River
go back to reference Lai SL, Chien AJ, Moon RT (2009) Wnt/Fz signaling and the cytoskeleton: potential roles in tumorigenesis. Cell Res 19:532–545PubMedCrossRef Lai SL, Chien AJ, Moon RT (2009) Wnt/Fz signaling and the cytoskeleton: potential roles in tumorigenesis. Cell Res 19:532–545PubMedCrossRef
go back to reference 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) 205:53–65CrossRef 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) 205:53–65CrossRef
go back to reference Matsuyama M, Aizawa S, Shimono A (2009) Sfrp controls apicobasal polarity and oriented cell division in developing gut epithelium. PLoS Genet 5:e1000427PubMedCrossRef Matsuyama M, Aizawa S, Shimono A (2009) Sfrp controls apicobasal polarity and oriented cell division in developing gut epithelium. PLoS Genet 5:e1000427PubMedCrossRef
go back to reference Mellad JA, Warren DT, Shanahan CM (2011) Nesprins LINC the nucleus and cytoskeleton. Curr Opin Cell Biol 23:47–54PubMedCrossRef Mellad JA, Warren DT, Shanahan CM (2011) Nesprins LINC the nucleus and cytoskeleton. Curr Opin Cell Biol 23:47–54PubMedCrossRef
go back to reference 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:e3169PubMedCrossRef 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:e3169PubMedCrossRef
go back to reference 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 239:1–15PubMed 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 239:1–15PubMed
go back to reference 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 175:555–562PubMedCrossRef 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 175:555–562PubMedCrossRef
go back to reference 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 283:27973–27981PubMedCrossRef 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 283:27973–27981PubMedCrossRef
go back to reference Norden C, Young S, Link BA, Harris WA (2009) Actomyosin is the main driver of interkinetic nuclear migration in the retina. Cell 138:1195–1208PubMedCrossRef Norden C, Young S, Link BA, Harris WA (2009) Actomyosin is the main driver of interkinetic nuclear migration in the retina. Cell 138:1195–1208PubMedCrossRef
go back to reference Otani H, Yoneyama T, Hashimoto R, Hatta T, Tanaka O (1993) Ultrastructure of the developing stomach in human embryos. Anat Embryol (Berlin) 187:145–151CrossRef Otani H, Yoneyama T, Hashimoto R, Hatta T, Tanaka O (1993) Ultrastructure of the developing stomach in human embryos. Anat Embryol (Berlin) 187:145–151CrossRef
go back to reference 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 50:205–211CrossRef 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 50:205–211CrossRef
go back to reference Sauer FC (1936) The interkinetic migration of embryonic epithelial nuclei. J Morphol 60:1–11CrossRef Sauer FC (1936) The interkinetic migration of embryonic epithelial nuclei. J Morphol 60:1–11CrossRef
go back to reference 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 106:16487–16492PubMedCrossRef 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 106:16487–16492PubMedCrossRef
go back to reference 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 1:322–333PubMedCrossRef 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 1:322–333PubMedCrossRef
go back to reference 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 113:109–129PubMed 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 113:109–129PubMed
go back to reference 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 13:820–833PubMed 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 13:820–833PubMed
go back to reference Takahashi T, Nowakowski RS, Caviness VS Jr (1995) The cell cycle of the pseudostratified ventricular epithelium of the embryonic murine cerebral wall. J Neurosci 15:6046–6057PubMed Takahashi T, Nowakowski RS, Caviness VS Jr (1995) The cell cycle of the pseudostratified ventricular epithelium of the embryonic murine cerebral wall. J Neurosci 15:6046–6057PubMed
go back to reference 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 50:175–185CrossRef 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 50:175–185CrossRef
go back to reference 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 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
go back to reference 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 56:79–93PubMedCrossRef 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 56:79–93PubMedCrossRef
go back to reference 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 239:941–953PubMedCrossRef 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 239:941–953PubMedCrossRef
go back to reference 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 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
go back to reference 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 21:71–83PubMed 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 21:71–83PubMed
Metadata
Title
Interkinetic nuclear migration during early development of midgut and ureteric epithelia
Authors
Makiko Yamada
Jun Udagawa
Ryuju Hashimoto
Akihiro Matsumoto
Toshihisa Hatta
Hiroki Otani
Publication date
01-01-2013
Publisher
Springer Japan
Published in
Anatomical Science International / Issue 1/2013
Print ISSN: 1447-6959
Electronic ISSN: 1447-073X
DOI
https://doi.org/10.1007/s12565-012-0156-8

Other articles of this Issue 1/2013

Anatomical Science International 1/2013 Go to the issue