The Chlamydomonas reinhardtii BBSome is an IFT cargo required for export of specific signaling proteins from flagella

Department of Cell Biology, University of Massachusetts Medical School, Worcester, 01655, USA.
The Journal of Cell Biology (Impact Factor: 9.83). 12/2009; 187(7):1117-32. DOI: 10.1083/jcb.200909183
Source: PubMed


In humans, seven evolutionarily conserved genes that cause the cilia-related disorder Bardet-Biedl syndrome (BBS) encode proteins that form a complex termed the BBSome. The function of the BBSome in the cilium is not well understood. We purified a BBSome-like complex from Chlamydomonas reinhardtii flagella and found that it contains at least BBS1, -4, -5, -7, and -8 and undergoes intraflagellar transport (IFT) in association with a subset of IFT particles. C. reinhardtii insertional mutants defective in BBS1, -4, and -7 assemble motile, full-length flagella but lack the ability to phototax. In the bbs4 mutant, the assembly and transport of IFT particles are unaffected, but the flagella abnormally accumulate several signaling proteins that may disrupt phototaxis. We conclude that the BBSome is carried by IFT but is an adapter rather than an integral component of the IFT machinery. C. reinhardtii BBS4 may be required for the export of signaling proteins from the flagellum via IFT.

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    • "ust after cell division genes ( Wood et al . , 2012 ) , we wanted to conduct a comprehensive analysis of basal body and flagella gene expression during the cell cycle . We first curated a core set of 193 basal body and flagella genes ( Basal Body , Axoneme , IFT , and BBsome ) that have been identified in previous studies ( Keller et al . , 2005 ; Lechtreck et al . , 2009 ; Dutcher , 2009 ; Shiratsuchi et al . , 2011 ; Bower et al . , 2013 ) ( Figures 5A to 5C ; Supplemental Data Set 6 ) . Clusters c11 to c14 are significantly enriched for the MapMan ontology term " cell motility " ( z - score > 2 . 5 ) ( Figure 2B ; Supplemental Data Set 3 ) and contain an overrepresentation of known flagella and basal "
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    ABSTRACT: The green alga Chlamydomonas reinhardtii is a useful model organism for investigating diverse biological processes, such as photosynthesis and chloroplast biogenesis, flagella and basal body structure/function, cell growth and division, and many others. We combined a highly synchronous photobioreactor culture system with frequent temporal sampling to characterize genome-wide diurnal gene expression in Chlamydomonas. Over 80% of the measured transcriptome was expressed with strong periodicity, forming 18 major clusters. Genes associated with complex structures and processes, including cell cycle control, flagella and basal bodies, ribosome biogenesis, and energy metabolism, all had distinct signatures of coexpression with strong predictive value for assigning and temporally ordering function. Importantly, the frequent sampling regime allowed us to discern meaningful fine-scale phase differences between and within subgroups of genes and enabled the identification of a transiently expressed cluster of light stress genes. Coexpression was further used both as a data-mining tool to classify and/or validate genes from other data sets related to the cell cycle and to flagella and basal bodies and to assign isoforms of duplicated enzymes to their cognate pathways of central carbon metabolism. Our diurnal coexpression data capture functional relationships established by dozens of prior studies and are a valuable new resource for investigating a variety of biological processes in Chlamydomonas and other eukaryotes.
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    • "These findings raised the question which proteins are the actual cargoes of IFT. Several TRP channels were reported to move by IFT and the BBSome cycles through cilia by associating to IFT trains (Blacque et al., 2004; Qin et al., 2004; Huang et al., 2007; Lechtreck et al., 2009 "
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    ABSTRACT: The assembly of the axoneme, the structural scaffold of cilia and flagella, requires translocation of a vast quantity of tubulin into the growing cilium, but the mechanisms that regulate the targeting, quantity, and timing of tubulin transport are largely unknown. In Chlamydomonas, GFP-tagged α-tubulin enters cilia as an intraflagellar transport (IFT) cargo and by diffusion. IFT-based transport of GFP-tubulin is elevated in growing cilia and IFT trains carry more tubulin. Cells possessing both nongrowing and growing cilia selectively target GFP-tubulin into the latter. The preferential delivery of tubulin boosts the concentration of soluble tubulin in the matrix of growing versus steady-state cilia. Cilia length mutants show abnormal kinetics of tubulin transport. We propose that cells regulate the extent of occupancy of IFT trains by tubulin cargoes. During ciliary growth, IFT concentrates soluble tubulin in cilia and thereby promotes elongation of the axonemal microtubules. © 2015 Craft et al.
    Full-text · Article · Jan 2015 · The Journal of Cell Biology
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    • "In addition to IFT-A and IFT-B, a third complex called the BBSome is connected to the IFT particle. Mutations in BBSome components do not typically block ciliary assembly but prevent the delivery of specific receptors to the cilium (Berbari et al., 2008) and cause accumulations of abnormal membrane-associated proteins in the cilium (Lechtreck et al., 2009). "
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    ABSTRACT: Vertebrate hedgehog signaling is coordinated by the differential localization of the receptors patched-1 and Smoothened in the primary cilium. Cilia assembly is mediated by intraflagellar transport (IFT), and cilia defects disrupt hedgehog signaling, causing many structural birth defects. We generated Ift25 and Ift27 knockout mice and show that they have structural birth defects indicative of hedgehog signaling dysfunction. Surprisingly, ciliary assembly is not affected, but abnormal hedgehog signaling is observed in conjunction with ciliary accumulation of patched-1 and Smoothened. Similarly, Smoothened accumulates in cilia on cells mutated for BBSome components or the BBS binding protein/regulator Lztfl1. Interestingly, the BBSome and Lztfl1 accumulate to high levels in Ift27 mutant cilia. Because Lztfl1 mutant cells accumulate BBSome but not IFT27, it is likely that Lztfl1 functions downstream of IFT27 to couple the BBSome to the IFT particle for coordinated removal of patched-1 and Smoothened from cilia during hedgehog signaling. Copyright © 2014 Elsevier Inc. All rights reserved.
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