The Invs Gene Encodes a Microtubule-Associated Protein

Nürnberger, Jens; Kribben, Andreas; Saez, Anabelle Opazo; Heusch, Gerd; Philipp, Thomas; Phillips, Carrie L.

doi:10.1097/01.asn.0000128291.30249.d0

Cited by 35 publications

(30 citation statements)

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“…Genes implicated in mouse nodal cilia function have not been knocked out exclusively in the mouse node, and it is clear from the pleiotropic mutant phenotypes that some of these genes have other roles in development that, when perturbed, could lead to defects in LR development (reviewed by Wagner and Yost, 2000). Second, Inversin protein is found not only in cilia but in other intracellular locations (Eley et al, 2004;Morgan et al, 2002a;Nurnberger et al, 2002;Nurnberger et al, 2004), suggesting it has non-ciliary functions. Third, cilia are found in other embryonic tissues such as the embryonic midline (Sulik et al, 1994), which has been implicated in LR development in frogs, zebrafish and mice (Danos and Yost, 1995; Danos and Yost, 1996;Meno et al, 1998), suggesting functions ascribed to cilia genes in LR development might occur in non-node cells.…”

Section: Discussionmentioning

confidence: 99%

Kupffer's vesicle is a ciliated organ of asymmetry in the zebrafish embryo that initiates left-right development of the brain, heart and gut

et al. 2005

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SummaryKupffer's vesicle is a ciliated organ of asymmetry in the zebrafish embryo that initiates left-right development of the brain, heart and gut Research article Development 1248However, genes implicated in ciliated node cell function are also expressed in non-node cells, and mutations of these genes give rise to a variety of laterality phenotypes and more pleiotropic phenotypes, making it impossible to exclude other mechanisms for LR development during early embryogenesis (for reviews, see Tabin and Vogan, 2003;Wagner and Yost, 2000;Yost, 2003). Furthermore, it is not known whether nodal flow is a murine-specific mechanism. Cilia formation and expression of lrd homologues have recently been observed in structures analogous to the node in chick, frog (Xenopus laevis) and zebrafish embryos (Essner et al., 2002), but the existence of motile cilia and nodal flow has not been demonstrated in non-murine embryos. Further confounding the issue, there are molecular asymmetries that precede the appearance of lrd expression and monocilia in Xenopus Levin et al., 2002) and perhaps in chick (Levin et al., 1995;Stern et al., 1995). This raises the issue of whether ciliated cells in other vertebrate embryos generate fluid flow and have a conserved function for ciliogenesis genes in LR development. In zebrafish, ciliated cells arise in the tailbud at the end of gastrulation (Essner et al., 2002) in a transient spherical organ called Kupffer's vesicle (KV). KV, first described in 1868 (Kupffer, 1868), is a conserved structure among teleost fishes. Electron microscopy studies in the bait fish Fundulus heteroclitus have shown that a single cilium (i.e. monocilium) protrudes from each cell lining KV into the lumen (Brummett and Dumont, 1978). In zebrafish, KV is formed from a group of approximately two-dozen cells, known as dorsal forerunner cells (DFCs), that migrate at the leading edge of the embryonic shield (the zebrafish equivalent of the mouse node) during gastrulation. In contrast to other cells in this region, DFCs do not involute during gastrulation, but remain at the leading edge of epibolic movements. At the end of gastrulation, DFCs migrate deep into the embryo and organize to form KV (Cooper and D'Amico, 1996; D'Amico and Cooper, 1997;Melby et al., 1996). During subsequent somite stages, KV is found ventral to the forming notochord in the tailbud and adjacent to the yolk cell. Although KV was first described well over 100 years ago, it remains unknown whether DFCs and KV are mesodermal or endodermal in origin, and it is unclear what role they play during development, leading to the categorization of KV as an embryonic 'organ of ambiguity ' (Warga and Stainier, 2002).Recently, using a novel technique to knockdown gene expression specifically in DFCs, we reported the first evidence that DFCs and/or KV function in LR patterning (Amack and Yost, 2004). Here, we show that cilia that arise inside KV are motile and generate a consistent counterclockwise fluid flow. A combination of laser ablations, embryological manipul...

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Section: Discussionmentioning

confidence: 99%

Kupffer's vesicle is a ciliated organ of asymmetry in the zebrafish embryo that initiates left-right development of the brain, heart and gut

et al. 2005

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“…Cilia may provide information that help cells to remain in a differentiated state. Because cystoproteins change their subcellular localization according to the cell-cycle stage (Mollet et al, 2005;Morgan et al, 2002;Nurnberger et al, 2004;Sayer et al, 2006), cilia resorption may permit the redistribution of IFT proteins and/or ciliary proteins in the rest of the cell and, thus, promote cell-cycle progression. This model is fully compatible with our results on IFT88/polaris and suggests the existence of a mechanism that regulates proteins by shuttling them to the nucleus, the centrosome or to cilia.…”

Section: Discussionmentioning

confidence: 99%

The intraflagellar transport component IFT88/polaris is a centrosomal protein regulating G1-S transition in non-ciliated cells

Robert

Margall-Ducos

Guidotti

et al. 2007

Journal of Cell Science

166

119

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Loss of normal primary cilia function in mammals is linked to proliferative diseases, such as polycystic kidney disease, suggesting a regulatory relationship between cilia and cell cycle. The primary cilium expressed by most mammalian cells is nucleated from the elder centriole of the centrosome. The relationship between centrosome and cilia suggests that these structures share functions and components. We now show that IFT88/polaris, a component of the intraflagellar transport, remains associated to the centrosome in a proliferative state. IFT88/polaris is tightly associated with the centrosome throughout the cell cycle in a microtubule- and dynein-independent manner. IFT88/polaris tetratricopeptide repeat motifs are essential for this localization. Overexpression of IFT88/polaris prevents G1-S transition and induces apoptotic cell death. By contrast, IFT88/polaris depletion induced by RNA interference promotes cell-cycle progression to S, G2, and M phases. Finally, we demonstrate that IFT88/polaris interacts with Che-1, an Rb-binding protein that inhibits the Rb growth suppressing function. We propose that IFT88/polaris, a protein essential for ciliogenesis, is also crucial for G1-S transition in non-ciliated cells.

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“…Invs mutations also cause cystic renal tubules and progressive renal failure in both mice and humans (nephronophthisis type 2, NPHP2) (Otto et al, 2003;Bisgrove and Yost, 2006). The subcellular localization of inversin is complex and dynamic, but includes the basal bodies, primary cilia and, during metaphase and anaphase, the spindle poles (Morgan et al, 2002;Watanabe et al, 2003;Eley et al, 2004;Nurnberger, 2004). In transfected cells, inversin binds Dvl and accelerates its degradation, and in Xenopus embryos it is required for CE (Simons et al, 2005).…”

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confidence: 99%

Tissue/planar cell polarity in vertebrates: new insights and new questions

2007

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This review focuses on the tissue/planar cell polarity (PCP) pathway and its role in generating spatial patterns in vertebrates. Current evidence suggests that PCP integrates both global and local signals to orient diverse structures with respect to the body axes. Interestingly, the system acts on both subcellular structures, such as hair bundles in auditory and vestibular sensory neurons, and multicellular structures, such as hair follicles. Recent work has shown that intriguing connections exist between the PCP-based orienting system and left-right asymmetry, as well as between the oriented cell movements required for neural tube closure and tubulogenesis. Studies in mice, frogs and zebrafish have revealed that similarities, as well as differences, exist between PCP in Drosophila and vertebrates. IntroductionThe genetic and molecular dissection of what is now referred to as planar cell polarity (PCP) began 25 years ago with the realization by Gubb and Garcia-Bellido (Gubb and Garcia-Bellido, 1982) that a small set of genes controls the polarity of cuticular hairs and bristles in Drosophila. Morphologists and embryologists had long appreciated the precise orientation of cuticular structures with respect to the body axes, but Gubb and Garcia-Bellido's work represented a conceptual departure in that it suggested the existence of a genetically defined system dedicated to coordinating these patterns. The genes that they studied are now known to be players in a complex system of developmental regulation that governs cell and tissue movements and patterns in both invertebrates and vertebrates. Although this phenomenon is now commonly referred to as PCP, Gubb and Garcia-Bellido's original and somewhat more general name 'tissue polarity' might ultimately prove more appropriate as its role is revealed in ever more diverse developmental processes.As is often the case in developmental biology, the vertebrate PCP field owes a large debt to its Drosophila counterpart, which has served as the source for many of the components and concepts in this system. However, the numerous differences between vertebrates and invertebrates in anatomy, tissue types and morphogenetic processes, together with the existence of a number of distinct PCP components in vertebrates, have made the study of vertebrate PCP uniquely interesting. In this review, we highlight recent work on vertebrate PCP and discuss several developmental processes in which there is suggestive, but still incomplete, evidence for PCP signaling or for the activity of a subset of PCP components. We have not attempted to cover the PCP field in a comprehensive manner because many excellent and detailed reviews have recently been published in this area [reviews with an emphasis on Drosophila PCP (Adler, 2002;Strutt, 2002;Tree et al., 2002;Klein and Mlodzik, 2005;Strutt and Strutt, 2005); reviews on various aspects of vertebrate PCP (Wallingford et al., 2002;Barrow, 2006;Karner et al., 2006;Montcouquiol et al., 2006a); a review on the very different mechanisms of planar polarit...

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The Invs Gene Encodes a Microtubule-Associated Protein

Abstract: Abstract. Microtubule networks are important for many vital processes such as mitosis, cell polarity, and differentiation.

Cited by 35 publications

References 55 publications

Kupffer's vesicle is a ciliated organ of asymmetry in the zebrafish embryo that initiates left-right development of the brain, heart and gut

Kupffer's vesicle is a ciliated organ of asymmetry in the zebrafish embryo that initiates left-right development of the brain, heart and gut

The intraflagellar transport component IFT88/polaris is a centrosomal protein regulating G1-S transition in non-ciliated cells

Tissue/planar cell polarity in vertebrates: new insights and new questions

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