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The goal of my research is to identify the regulatory proteins that control vesicle transport in the yeast Saccharomyces cerevisiae, in order to understand how underlying defects in protein and lipid trafficking contribute to human disease. Vesicle transport is required to switch off signaling receptors that would otherwise promote unregulated cell growth. Retrograde transport also carries signals that promote the continued survival of neurons, and defects in the machinery responsible for retrograde transport are believed to be a cause of motor neuron disease. Because vesicle transport processes are highly conserved, they can be studied in a very simple organism, and the findings applied directly to the study of human cells. Yeast genetics is therefore a powerful tool for the discovery of fundamental cellular mechanisms relevant to human health.
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Graduate Student Supervision
Doctoral Student Supervision (2008-2018)
No abstract available.
Cellular protein trafficking, the concerted action of moving proteins to the appropriate cellular location is important for the proper functioning of the cell. Proteins are sorted at hubs such as the endosome, where they are targeted either for degradation or for recycling to the Golgi. Yeast is an excellent model organism to study protein trafficking due to the conservation with higher eukaryotes and the ease of genetic manipulation. In this thesis, two different high-throughput approaches were used to study the protein machinery that controls the yeast endosomal sorting network.First, correlation analysis, which compares genome-wide phenotypic profiles, was used to uncover new aspects of endosomal sorting and two specific examples were chosen for further study. In the first example, we explored positive and negative genetic interaction profile correlations for members of the uncharacterized yeast complex, BLOC, which suggested a role in endosomal sorting. In particular, we found that BLOC was needed for proper downregulation of a manganese transporter similar to ESCRT (Endosomal Sorting Complex Required for Transport, a well-studied endosomal sorting complex. In the second example, we explored the predictive value of negatively correlated genetic interaction profiles for gene mutants within known protein complexes and found that these negative correlations described two types of regulatory interactions between the resulting proteins, direct inhibition and competition for shared subunits. We then showed that the previously uncharacterized VID Associated Factor 1 (Vaf1) was negatively correlated with respect to its genetic interactions and downregulated by the VID complex. In summary, correlation analysis provides a robust tool to identify the functional relationship between proteins.Second, a quantitative genome-wide endosomal sorting screen followed by a secondary high-throughput microscopy screen, uncovered novel endosomal regulators of the flippase, Neo1. Loss of these regulators caused three phenotypic outcomes: reduced recycling from endosomes, delayed endosomal progression, or reduced colocalization with known binding partners. In particular, a short motif in the N-terminus of Neo1 was found to be necessary for Snx3 dependent sorting, correct sorting of other Snx3 cargos, and full Neo1 function. Overall, this study illuminates the power of high-throughput screens to discover new regulators of endosomal sorting.
Protein palmitoylation represents the only reversible lipid modification in the cell. As a post-translational modification, it is highly dynamic and plays an important role in protein trafficking and localization. Two families of enzymes mediate dynamic palmitoylation: palmitoyl-acyl transferases (PATs) catalyze palmitate addition, and acyl-protein thioesterases (APTs) catalyze palmitate removal. In mammalian cells, twenty-three PATs have been identified; however, the mechanisms that regulate their enzymatic activity are largely unexplored. Only two APTs, APT1 and APT2, have been identified, but it is unclear if these enzymes act constitutively on all palmitoylated proteins, or if additional depalmitoylases exist. To determine if APT1 and APT2 are responsible for the depalmitoylation of all cytosolic substrates, in this dissertation, I first examined the roles of APT1 and APT2 in protein depalmitoylation. Using a dual pulse-chase strategy to compare protein and palmitate half-lives, I found that simultaneous knockdown or inhibition of APT1 and APT2 strongly blocked palmitate removal from the N-terminal domain of Huntingtin (N-HTT), but had no effect on the depalmitoylation of post-synaptic density-95 (PSD-95). By activity-based protein profiling (ABPP), I showed that the APT1/2 inhibitor Palmostatin B has additional serine hydrolase targets that may play a role in PSD-95 depalmitoylation. Moreover, Palmostatin B induced PSD-95-GFP re-distribution in COS-7 cells, a phenotype not observed with APT1- and APT2-selective inhibitors. These results demonstrate that serine hydrolases other than APT1 and APT2 mediate the substrate-specific removal of palmitate from cytosolic proteins. I also investigated a possible novel regulator of the PAT HTT-interacting protein 14 (HIP14), Optineurin (OPTN), a cargo adaptor known to interact with HTT to mediate post-Golgi vesicle trafficking. I validated this interaction by co-immunoprecipitation and showed that OPTN is not a palmitoylated substrate. Furthermore, HIP14, OPTN, and HTT formed a trimeric complex. I mapped the binding of OPTN and HTT to the HIP14 ankyrin repeat domain, and identified mutations that selectively destabilized the HIP14/OPTN interaction. I hypothesize that OPTN transports HIP14 to distinct subcellular compartments to regulate its access to substrates. In summary, these results reveal potential novel regulatory components in the dynamic palmitoylation cycle.
In Eukaryotes, luminal and transmembrane proteins are moved to their functional locations by conserved membrane trafficking machinery. In this process, cargo adaptors bind motifs present on cargo, indirectly linking the proteins to coats, which deform membranes and form transport vesicles. Here, cargo adaptor recruitment and cargo recognition was studied by characterizing associated factors in the budding yeast Saccharomyces cerevisiae. Possible cargo adaptor-associated factors were identified in a proteomics study that grouped protein-protein interactions into 501 putative membrane associated complexes using a Markov clustering algorithm. Two clusters were selected for this work.The first contained the uncharacterized protein Ssp120 with the endoplasmic reticulum-to-Golgi trafficking complex Emp46/Emp47. Ssp120 stably interacted with the Emp46/Emp47 complex and depended on Emp47 for its punctate localization. The C-terminus of Ssp120 mediated the interaction. Homology with human MCFD2 suggests that Ssp120 may link a subset of cargo to Emp46/Emp47.The second cluster was comprised of retromer, an endosome-to-Golgi trafficking complex, and the Rab5-family guanine nucleotide exchange factor (GEF) Muk1. Both Muk1 and the other known Rab5-family GEF, Vps9, interacted with retromer and the presence of at least one was required for retromer recruitment to endosomes. Additionally, a new VPS9 domain-containing protein present was identified and shown to complement loss of MUK1 and VPS9. Retromer recruitment was shown to be dependent on putative GEF catalytic residues and the presence of their target Rabs. Furthermore, loss of GEFs resulted in mislocalization of the potential Rab5-family GTPase effector, Vps34, and its lipid product, phosphatidylinositol 3-phosphate (PI3P), to the vacuolar membrane. As retromer is recruited by PI3P, the data support a positive feedback model whereby retromer interacts with GEFs to indirectly modify the lipid composition of the membrane allowing further localized recruitment.This study validates the approach of studying novel interactors of cargo recognition complexes to better understand their function. It suggests that Ssp120 may recognize a subset of Emp46-Emp47 cargo, indicating that an associated factor can diversify the proteins recognized by a given cargo adaptor. Furthermore, the work on retromer suggests a novel mechanism for the reinforcement of cargo selective complex recruitment that may be conserved in humans.
The process of endocytic recycling, in which cell surface proteins are internalized and re-delivered to the plasma membrane, is essential in all eukaryotes for maintaining plasma membrane composition and regulating the surface levels of signaling receptors. The applicability of Saccharomyces cerevisiae as a model to study endocytic recycling is a subject of debate, as there appears to be critical differences between yeast and mammalian cells. For example, while clathrin and its adaptors are critical for uptake in mammals, they do not seem to be essential in yeast. Endocytic recycling has not been comprehensively studied on a genetic level in yeast, and only limited cargo have been considered, making it difficult to accurately assess the similarity between the two systems. Furthermore, the transport of SNARE proteins is poorly understood, but appears to involve specialized mechanisms. This study uses a genome-wide screening approach to systematically and quantitatively identify genes required for the endocytic recycling of the yeast SNARE protein Snc1, homologous to the mammalian VAMP2/synaptobrevin.Endocytic defects for mutants of many yeast homologs of mammalian endocytosis genes were identified, for the first time. Significantly, a cargo-selective and partially-redundant role for clathrin and its adaptors yAP1801 and yAP1802 was identified. The lipid phosphatase Inp52 was found to mediate AP180 release from endocytic vesicles. Additionally, the previously uncharacterized protein Ldb17, homologous to the mammalian endocytic protein SPIN90, was identified as a new component of the endocytic machinery, and regulates both coat and actin dynamics at endocytic sites.Factors regulating Snc1 recycling were also identified, including the variant clathrin adaptor AP-1R. This is the first reported function for this complex. The previously uncharacterized protein Ima1 was found to be a putative enzyme that specifically binds to AP-1R, and may have activity related to AP-1R function.Overall, this study demonstrates that endocytic recycling in yeast and mammals is more similar than previously appreciated, and identifies new factors in this process. Furthermore, it raises awareness of the degree of cargo-selectivity underlying this pathway, and demonstrates quantitative methods that can be further applied to future studies in both systems.
Proteins and lipids are selectively transported between the Golgi, plasma membrane and endosomes by a network of vesicle-mediated endosomal transport pathways. Trafficking specificity requires the coordination of multiple protein assemblies and signals of compartment identity. Genetic screens, and molecular and biochemical techniques, have revealed many components for endosomal transport, but questions regarding the mechanisms of specificity and the coordination of trafficking pathways remain. The Golgi Associated Retrograde Protein (GARP) complex is required to tether vesicles derived from multiple types of endosomes with the Golgi. In the absence of GARP, retrograde transport from endosomes to the Golgi is abolished, and numerous cargoes are missorted. Mutation of the GARP subunit Vps54 causes motor neuron disease in the mouse, emphasizing the physiological importance of GARP. Tethering requires recognition of multiple membranes, but how GARP recognizes vesicles derived from multiple upstream compartments is not known. In my first body of work, the function of the GARP subunit Vps54 was addressed. The N-terminal portion of Vps54 was found to be important for GARP complex assembly and stability, while the C-terminal portion localized to a compartment with features of an early endosome. In the absence of the C-terminal domain, retrieval of early endosome cargo became dependent on late-endosome retrograde transport. This body of work supports the model that tethers recognize, and possibly distinguish between, upstream compartments. The machinery involved in retrograde transport from endosomes is not fully understood. In my second body of work, genes involved endosomal transport were systematically identified by screening mutant collections with a reporter of early endosome dysfunction. To evaluate the relationships between genes and pathways discovered in this screen, genetic interaction analyses with two phenotypes, growth and endosomal dysfunction, were performed. An analysis of genetic interactions based on trafficking dysfunction revealed interesting genetic relationships between endosomal coat proteins and their regulators. This body of work provides insight into the relationships between endosomal transport pathways and presents a framework to discover relationships between genes and pathways discovered in a genomic screen. Together, this thesis presents a molecular and pathway perspective of endosomal transport that provides insight into pathway specificity and the relationships between pathway components.
All secretory proteins must pass the strict quality control (QC) imposed by the endoplasmic reticulum (ER), where they are first synthesized. Various chaperones, degradation machinery, and vesicular transport factors act together to ensure only properly folded proteins can leave this compartment for subsequent sorting. Failure in QC contributes to misfolding, intracellular retention, and frequently degradation, all of which are known to cause disease. QC is particularly crucial for polytopic proteins, which often represent plasma membrane transporters and channels important for cell function. Recent work suggests ER surveillance systems for polytopic proteins are specialized towards substrates and specific misfolding defects. The underlying mechanisms, especially the roles of post-translational modifications, are poorly understood, thus necessitating examination of various model proteins. Here, the yeast chitin synthase Chs3 was used as a paradigm for polytopic protein trafficking. By high-throughput analysis of the yeast deletion collection, a novel Chs3 ER transport factor was identified. This protein, Pfa4, contains a conserved DHHC-domain, signifying its putative function as a protein acyltransferase. These enzymes of protein palmitoylation were only recently discovered, and few substrates are known. The work described here showed that Chs3 was palmitoylated by Pfa4, and this modification was required for ER export. Both palmitoylation and association with the chaperone Chs7 were necessary for preventing Chs3 aggregation at the ER, indicating that palmitoylation is required for Chs3 to attain an export-competent conformation. Retention of misfolded Chs3 appeared independent of known ER-associated degradation machinery. Instead, a high-throughput search identified the Ubp3 deubiquitination enzyme as a retention factor; deletion of UBP3 restored ER export of unpalmitoylated Chs3 through palmitoylation-independent means. Ubp3-mediated deubiquitination may be regulating the levels of proteins involved in both Chs3 folding and Golgi-to-ER retrieval of misfolded Chs3. The role of palmitoylation in folding at the ER is not well known, and many substrate-specific retention pathways for polytopic proteins have not been identified. These findings suggest palmitoylation can contribute to ERQC of polytopic proteins, and point to potentially novel QC factors that are regulated by deubiquitination. A better understanding of these fundamental molecular mechanisms could contribute to discovery of therapeutic targets for ER misfolding diseases.
Master's Student Supervision (2010-2017)
No abstract available.
- Competitive organelle-specific adaptors recruit Vps13 to membrane contact sites (2018)
BjÃ¶rn D.M. Bean and Samantha K. Dziurdzik and Kathleen L. Kolehmainen and Claire M.S. Fowler and Waldan K. Kwong and Leslie I. Grad and Michael Davey and Cayetana Schluter and Elizabeth Conibear
The Journal of Cell Biology 217 (10) 3593--3607
- The chaperone Chs7 forms a stable complex with Chs3 and promotes its activity at the cell surface (2018)
Sai T. Dharwada and Lauren E. Dalton and BjÃ¶rn D. M. Bean and Nirmala Padmanabhan and Catherine Choi and Cayetana Schluter and Michael Davey and Elizabeth Conibear
Traffic 19 (4) 285--295
- Cargo selectivity of yeast sorting nexins (2017)
BjÃ¶rn D.M. Bean and Michael Davey and Elizabeth Conibear
Traffic 18 (2) 110--122
- Quantitative high-content imaging identifies novel regulators of Neo1 trafficking at endosomes (2017)
Lauren E. Dalton and BjÃ¶rn D. M. Bean and Michael Davey and Elizabeth Conibear
Molecular Biology of the Cell 28 (11) 1539--1550
- Targeting the Ras palmitoylation/depalmitoylation cycle in cancer (2017)
David Tse Shen Lin and Nicholas G. Davis and Elizabeth Conibear
Biochemical Society Transactions 45 (4) 913--921
- ABHD17 proteins are novel protein depalmitoylases that regulate N-Ras palmitate turnover and subcellular localization (2015)
David Tse Shen Lin and Elizabeth Conibear
- Enzymatic protein depalmitoylation by acyl protein thioesterases (2015)
David~T.S. Lin and Elizabeth Conibear
Biochemical Society Transactions 43 (2) 193--198
- Rab5-family guanine nucleotide exchange factors bind retromer and promote its recruitment to endosomes (2015)
B. D. M. Bean and M. Davey and J. Snider and M. Jessulat and V. Deineko and M. Tinney and I. Stagljar and M. Babu and E. Conibear
Molecular Biology of the Cell 26 (6) 1119--1128
- The alternate AP-1 adaptor subunit Apm2 interacts with the Mil1 regulatory protein and confers differential cargo sorting (2015)
S. T. Whitfield and H. E. Burston and B. D. M. Bean and N. Raghuram and L. Maldonado-Baez and M. Davey and B. Wendland and E. Conibear
Molecular Biology of the Cell 27 (3) 588--598
- Large-Scale Analysis of Membrane Transport in Yeast Using Invertase Reporters (2014)
Lauren Dalton and Michael Davey and Elizabeth Conibear
Membrane Trafficking 395--409
- Single point mutation in Rabenosyn-5 in a female with intractable seizures and evidence of defective endocytotic trafficking (2014)
Sylvia Stockler and Silvia Corvera and David Lambright and Kevin Fogarty and Ekaterina Nosova and Deborah Leonard and Robert Steinfeld and Cameron Ackerley and Casper Shyr and Nicolas Au and Kathrin Selby and Margot van Allen and Hilary Vallance and Ron Wevers and David Watkins and David Rosenblatt and Colin J Ross and Elizabeth Conibear and Wyeth Wasserman and Clara van Karnebeek
Orphanet Journal of Rare Diseases 9 (1)
- The palmitoyl acyltransferase HIP14 shares a high proportion of interactors with huntingtin: implications for a role in the pathogenesis of Huntington's disease (2014)
Stefanie L. Butland and Shaun S. Sanders and Mandi E. Schmidt and Sean-Patrick Riechers and David T.S. Lin and Dale D.O. Martin and Kuljeet Vaid and Rona K. Graham and Roshni R. Singaraja and Erich E. Wanker and Elizabeth Conibear and Michael R. Hayden
Human Molecular Genetics 23 (15) 4142--4160
- Vesicle and organelle formation: making connections (2013)
E. Conibear and B. J. Nichols
Molecular Biology of the Cell 24 (6) 674--674
- Interaction landscape of membrane-protein complexes in Saccharomyces cerevisiae (2012)
Mohan Babu and James Vlasblom and Shuye Pu and Xinghua Guo and Chris Graham and BjÃ¶rn D. M. Bean and Helen E. Burston and Franco J. Vizeacoumar and Jamie Snider and Sadhna Phanse and Vincent Fong and Yuen Yi C. Tam and Michael Davey and Olha Hnatshak and Navgeet Bajaj and Shamanta Chandran and Thanuja Punna and Constantine Christopolous and Victoria Wong and Analyn Yu and Gouqing Zhong and Joyce Li and Igor Stagljar and Elizabeth Conibear and Shoshana J. Wodak and Andrew Emili and Jack F. Green
Nature 489 (7417) 585--589
- Organization and Assembly of the TRAPPII Complex (2011)
Catherine Choi and Michael Davey and Cayetana Schluter and Preet Pandher and Yuan Fang and Leonard J. Foster and Elizabeth Conibear
Traffic 12 (6) 715--725
- Vesicle Transport: Springing the TRAPP (2011)
Current Biology 21 (13) R506--R508
- VPS35 Mutations in Parkinson Disease (2011)
Carles Vilarino-GÃ¼ell and Christian Wider and Owen~A. Ross and Justus~C. Dachsel and Jennifer~M. Kachergus and Sarah~J. Lincoln and Alexandra~I. Soto-Ortolaza and Stephanie~A. Cobb and Greggory~J. Wilhoite and Justin~A. Bacon and Bahareh Behrouz and Heather~L. Melrose and Emna Hentati and Andreas Puschmann and Daniel~M. Evans and Elizabeth Conibear and Wyeth~W. Wasserman and Jan~O. Aasly and Pierre~R. Burkhard and Ruth Djaldetti and Joseph Ghika and Faycal Hentati and Anna Krygowska-Wajs and Ti
The American Journal of Human Genetics 89 (1) 162--167
- Converging views of endocytosis in yeast and mammals (2010)
Current Opinion in Cell Biology 22 (4) 513--518
- Palmitoylation and depalmitoylation dynamics at a glance (2010)
Elizabeth Conibear and Nicholas G. Davis
Journal of Cell Science 123 (23) 4007--4010
- Identification of the Novel TRAPP Associated Protein Tca17 (2009)
Ben Montpetit and Elizabeth Conibear
Traffic 10 (6) 713--723
- Regulators of yeast endocytosis identified by systematic quantitative analysis (2009)
Helen E. Burston and Lymarie Maldonado-Baez and Michael Davey and Benjamen Montpetit and Cayetana Schluter and Beverly Wendland and Elizabeth Conibear
The Journal of Cell Biology 185 (6) 1097--1110
- The Endocytic Pathway (2009)
Elizabeth Conibear and Yuen Yi C. Tam
Trafficking Inside Cells 67--83
- An endocytic mechanism for haemoglobin-iron acquisition inCandida albicans (2008)
Ziva Weissman and Revital Shemer and Elizabeth Conibear and Daniel Kornitzer
Molecular Microbiology 69 (1) 201--217
- Discovery and Expansion of Gene Modules by Seeking Isolated Groups in a Random Graph Process (2008)
Jochen Brumm and Elizabeth Conibear and Wyeth W. Wasserman and Jennifer Bryan
PLoS ONE 3 (10) e3358
- Evaluation of the Golgi trafficking protein VPS54 (wobbler) as a candidate for ALS (2008)
Miriam H. Meisler and Carsten Russ and Kate T. Montgomery and Matthew Greenway and Sean Ennis and Orla Hardiman and Denise A. Figlewicz and Nicole R. Quenneville and Elizabeth Conibear and Robert H. Brown
Amyotrophic Lateral Sclerosis 9 (3) 141--148
- Genome-Wide Analysis of Membrane Transport Using Yeast Knockout Arrays (2008)
Helen E. Burston and Michael Davey and Elizabeth Conibear
Membrane Trafficking 29--39
- Global Analysis of Yeast Endosomal Transport Identifies the Vps55/68 Sorting Complex (2008)
C. Schluter and K. K.Y. Lam and J. Brumm and B. W. Wu and M. Saunders and T. H. Stevens and J. Bryan and E. Conibear
Molecular Biology of the Cell 19 (4) 1282--1294
- Molecular Architecture and Functional Model of the Complete Yeast ESCRT-I Heterotetramer (2007)
Michael S. Kostelansky and Cayetana Schluter and Yuen Yi C. Tam and Sangho Lee and Rodolfo Ghirlando and Bridgette Beach and Elizabeth Conibear and James H. Hurley
Cell 129 (3) 485--498
- Domains within the GARP Subunit Vps54 Confer Separate Functions in Complex Assembly and Early Endosome Recognition (2006)
N. R. Quenneville
Molecular Biology of the Cell 17 (4) 1859--1870
- Palmitoylation by the DHHC protein Pfa4 regulates the ER exit of Chs3 (2006)
Karen K.Y. Lam and Michael Davey and Beimeng Sun and Amy F. Roth and Nicholas G. Davis and Elizabeth Conibear
The Journal of Cell Biology 174 (1) 19--25
- Toward the Systems Biology of Vesicle Transport (2006)
Nicole R. Quenneville and Elizabeth Conibear
Traffic 7 (7) 761--768
- An E-MAP of the ER (2005)
Cell 123 (3) 366--368
- Ykt6p Is a Multifunctional Yeast R-SNARE That Is Required for Multiple Membrane Transport Pathways to the Vacuole (2003)
Molecular Biology of the Cell 14 (5) 1868--1881
- An ESCRT into the Endosome (2002)
Molecular Cell 10 (2) 215--216
- Studying yeast vacuoles (2002)
Elizabeth Conibear and Tom H. Stevens
Guide to Yeast Genetics and Molecular and Cell Biology Part C 408--432
- Vps51p Mediates the Association of the GARP (Vps52/53/54) Complex with the Late Golgi t-SNARE Tlg1p (2002)
Molecular Biology of the Cell 14 (4) 1610--1623
- Identification of Rgp1p, a novel Golgi recycling factor, as a protein required for efficient localization of yeast casein kinase 1 to the plasma membrane (2000)
Panek, H.R. and Conibear, E. and Bryan, J.D. and Colvin, R.T. and Goshorn, C.D. and Robinson, L.C.
Journal of Cell Science 113 (24) 4545--4555
- Vps52p, Vps53p, and Vps54p Form a Novel Multisubunit Complex Required for Protein Sorting at the Yeast Late Golgi (2000)
E. Conibear and T. H. Stevens
Molecular Biology of the Cell 11 (1) 305--323
- Multiple sorting pathways between the late Golgi and the vacuole in yeast (1998)
Elizabeth Conibear and Tom H Stevens
Biochimica et Biophysica Acta (BBA) - Molecular Cell Research 1404 (1-2) 211--230
- Golgi and vacuolar membrane proteins reach the vacuole in vps1 mutant yeast cells via the plasma membrane (1995)
S. F. Nothwehr
The Journal of Cell Biology 129 (1) 35--46
- Vacuolar biogenesis in yeast: Sorting out the sorting proteins (1995)
Elizabeth Conibear and Tom H. Stevens
Cell 83 (4) 513--516
- A chimera of the cytoplasmic tail of the mannose 6-phosphate/IGF-II receptor and lysozyme localizes to the TGN rather than prelysosomes where the bulk of the endogenous receptor is found (1994)
Conibear, E. and Pearse, B.M.
Journal of Cell Science 107 (4) 923--932
- Specificity of binding of clathrin adaptors to signals on the mannose-6-phosphate/insulin-like growth factor II receptor (1989)
The EMBO Journal