{"id":32,"date":"2014-08-20T16:01:31","date_gmt":"2014-08-20T21:01:31","guid":{"rendered":"https:\/\/my.vanderbilt.edu\/grahamlab\/?page_id=32"},"modified":"2025-04-10T16:46:05","modified_gmt":"2025-04-10T21:46:05","slug":"publications-2","status":"publish","type":"page","link":"https:\/\/my.vanderbilt.edu\/grahamlab\/publications-2\/","title":{"rendered":"Publications"},"content":{"rendered":"
\n

Preprint work:<\/strong><\/p>\n

P4-ATPase control over phosphoinositide membrane asymmetry and neomycin resistance
\nBhawik K. Jain, H. Diessel Duan, Christina Valentine, Ariana Samiha, Huilin Li, Todd R. Graham<\/strong>. bioRxiv 2025.03.03.641220; doi: https:\/\/doi.org\/10.1101\/2025.03.03.641220<\/p>\n

Published work:<\/strong><\/p>\n

Jimenez M, Kyoung CK, Nabukhotna K, Watkins D, Jain BK, Best JT,\u00a0Graham TR.<\/strong>\u00a0P4-ATPase endosomal recycling relies on multiple retromer-dependent localization signals<\/a>.\u00a0Mol Biol Cell<\/em> (2024). doi: 10.1091\/mbc.E24-05-0209<\/p>\n<\/div>\n

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Duan HD, Jain BK, Li H,\u00a0<\/i>Graham TR,<\/strong> Li H.\u00a0Structural insight into an Arl1\u2013ArfGEF complex involved in Golgi recruitment of a GRIP-domain golgin<\/a>.\u00a0Nat Commun<\/i>15<\/b>, 1942 (2024). https:\/\/doi.org\/10.1038\/s41467-024-46304-w<\/p>\n<\/div>\n

Norris AC, Yazlovitskaya EM, Yang TS, Mansueto A, Stafford JM,\u00a0Graham TR.<\/strong>\u00a0ATP10A deficiency results in male-specific infertility in mice. Front Cell Dev Biol<\/a> (2024). DOI:10.3389\/fcell.2024.1310593<\/p>\n

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Norris AC, Mansueto AJ, Jimenez M, Yazlovitskaya EM, Jain BK,\u00a0Graham TR<\/strong>.\u00a0Flipping the script: Advances in understanding how and why P4-ATPases flip lipid across membranes<\/a>. Biochim Biophys Acta Mol Cell Res.<\/em> (2024) 1871(4):119700. doi: 10.1016\/j.bbamcr.2024.119700<\/p>\n

Norris AC, Yazlovitskaya EM, Zhu E, Rose BS, May JC, Gibson-Corley KN,\u00a0 McLean JA, Stafford JM, Graham TR<\/strong>. Deficiency of the lipid flippase ATP10A causes diet-induced dyslipidemia in female mice<\/a>Sci Rep<\/i>14<\/b>, 343 (2024). https:\/\/doi.org\/10.1038\/s41598-023-50360-5<\/p>\n

Yazlovitskaya EM, Graham TR.<\/strong>Type IV P-Type ATPases: Recent Updates in Cancer Development, Progression, and Treatment.<\/a>Cancers<\/em>\u00a0(2023),\u00a015<\/em>, 4327. https:\/\/doi.org\/10.3390\/cancers15174327<\/p>\n

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Xie B, Guillem C, Date SS, Cohen CI, Jung C, Kendall AK, Best JT, Graham TR, Jackson LP. An interaction between B’-COP and the ArfGAP, Glo3, maintains post-Golgi cargo recycling.<\/a>J Cell Biol. (2023)\u00a0<\/em>222 (4): e202008061. doi:\u00a0https:\/\/doi.org\/10.1083\/jcb.202008061<\/p>\n

Date SS, Xu P, Hepowit NL, Diab NS, Best JT, Xie B, Du J, Strieter ER, Jackson LP, MacGurn JA, Graham TR<\/strong>.\u00a0Ubiquitination drives COPI priming and Golgi SNARE localization<\/a>\u00a0(2022) E<\/em>Life<\/i>11<\/b>:e80911. doi: https:\/\/doi.org\/10.7554\/eLife.80911<\/p>\n<\/div>\n

Steenwyk JL, Phillips MA, Yang F, Date SS, Graham TR<\/strong>, Berman J, Hittinger CT, Rokas A.\u00a0An orthologous gene coevolution network provides insight into eukaryotic cellular and genomic structure and function<\/a>Sci. Adv.<\/i><\/span>8<\/b>,<\/span>eabn0105<\/span>(2022).\u00a0<\/span>DOI:10.1126\/sciadv.abn0105<\/a><\/span><\/p>\n

Graham TR.<\/strong>AP-3 shows off its flexibility for the cryo-EM camera<\/a>\u00a0(2022) Journal of Biological Chemistry, 101491. doi:\u00a0https:\/\/doi.org\/10.1016\/j.jbc.2021.101491<\/p>\n

Bai L, Jain BK, You Q, Duan HD, Takar M, Graham TR<\/strong>, Li H. Structural basis of the P4B ATPase lipid flippase activity.<\/a> Nat Commun. 2021 Oct 13;12(1):5963. doi: 10.1038\/s41467-021-26273-0.<\/p>\n

Bai L, You Q, Jain BK, Duan HD, Kovach A, Graham TR<\/strong>, Li H. Transport mechanism of P4 ATPase phosphatidylcholine flippases.<\/a>\u00a0Elife. 2020 Dec 15;9:e62163. doi: 10.7554\/eLife.62163.<\/p>\n

Jain BK, Roland BP, Graham TR.<\/strong>Exofacial membrane composition and lipid metabolism regulates plasma membrane P4-ATPase substrate specificity<\/a>\u00a0(2020) Journal of Biological Chemistry, Volume 295, Issue 52, 17997 – 18009<\/p>\n

Roland BP, Graham TR<\/strong>. Exofacial membrane composition and lipid metabolism regulates plasma membrane P4-ATPase substrate specificity<\/a>. J Biol Chem. 2020 Dec 25;295(52):17997-18009. <\/span>doi<\/span>: 10.1074\/jbc.RA120.014794. <\/span>Epub<\/span> 2020 Oct 15.<\/span>\u00a0<\/span><\/span>\u00a0<\/span><\/p>\n

Best JT, Xu P, McGuire JG, Leahy SN, Graham TR<\/strong>. Yeast synaptobrevin, Snc1, engages distinct routes of postendocytic recycling mediated by a sorting nexin, Rcy1-COPI, and retromer. <\/a>Mol Biol Cell. 2020 Apr 15;31(9):944-962. doi: 10.1091\/mbc.E19-05-0290. Epub 2020 Feb 19.<\/p>\n

Kendall AK, Xie B, Xu P, Wang J, Burcham R, Frazier MN, Binshtein E, Wei H, Graham TR<\/strong>, Nakagawa T, Jackson LP. Mammalian Retromer Is an Adaptable Scaffold for Cargo Sorting from Endosomes. <\/a>Structure. 2020 Apr 7;28(4):393-405.e4. doi: 10.1016\/j.str.2020.01.009. Epub 2020 Feb 5.<\/p>\n

Huang Y, Takar M, Best JT, Graham TR<\/strong>. Conserved mechanism of phospholipid substrate recognition by the P4-ATPase Neo1 from Saccharomyces cerevisiae. <\/a>Biochim Biophys Acta Mol Cell Biol Lipids. 2020 Feb;1865(2):158581. doi: 10.1016\/j.bbalip.2019.158581. Epub 2019 Nov 28.<\/p>\n

Best JT, Xu P, Graham TR<\/strong>. Phospholipid flippases in membrane remodeling and transport carrier biogenesis. <\/a>Curr Opin Cell Biol. 2019 Aug;59:8-15. doi: 10.1016\/j.ceb.2019.02.004. Epub 2019 Mar 18.<\/p>\n

Takar M, Huang Y, Graham TR<\/strong>. The PQ-loop protein Any1 segregates Drs2 and Neo1 functions required for viability and plasma membrane phospholipid asymmetry. <\/a>J Lipid Res. 2019 May;60(5):1032-1042. doi: 10.1194\/jlr.M093526. Epub 2019 Mar 1.<\/p>\n

Roland B.P., Naito T., Best J.T., Arnaiz-Yepez C., Takatsu H., Yu R.J., Shin H.W., Graham T.R.<\/strong>Yeast and human p4-ATPases transport glycosphingolipids using conserved structural motifs<\/a>. J Biol Chem. (2018). doi: 10.1074\/jbc.RA118.005876.<\/p>\n

Xu P., Hankins H.M., MacDonald C., Erlinger S.J., Frazier M.N., Diab N.S., Piper R.C., Jackson L.P., MacGurn J.A., Graham T.R<\/strong>. COPI mediates recycling of an exocytic SNARE by recognition of a ubiquitin sorting signal<\/a>. Elife. (2017). doi:10.7554\/eLife.2842.<\/p>\n

Wu Y., Takar M., Cuentas-Condori AA,\u00a0Graham T.R<\/strong>.\u00a0Neo1 and phosphatidylethanolamine contribute to vacuole membrane fusion in\u00a0Saccharomyces cerevisiae<\/i><\/a>.\u00a0Cell Logist<\/span>. 2016 Aug 25;6(3):e1228791. eCollection 2016 Jul-Sep.<\/p>\n

Roland B.P.,\u00a0Graham T.R.<\/strong>Decoding P4-ATPase substrate interactions<\/a>.\u00a0Crit Rev Biochem Mol Biol<\/span>. (2016) Nov\/Dec;51(6):513-527. doi: 10.1080\/10409238.2016.1237934. Epub 2016 Oct 4. Review.<\/p>\n

Roland B.P.,\u00a0Graham T.R<\/strong>. Directed evolution of a sphingomyelin flippase reveals mechanism of substrate backbone discrimination by a P4-ATPase.<\/a>Proc Natl Acad Sci U S A<\/span>. (2016) Aug 2;113(31):E4460-6. doi: 10.1073\/pnas.1525730113. Epub 2016 Jul 18.<\/p>\n

Takar M., Wu Y.,\u00a0Graham T.R.<\/strong>The Essential Neo1 Protein from Budding Yeast Plays a Role in Establishing Aminophospholipid Asymmetry of the Plasma Membrane.<\/a>J Biol Chem<\/span>. (2016) Jul 22;291(30):15727-39. doi: 10.1074\/jbc.M115.686253. Epub 2016 May 26.<\/p>\n

Hankins, H. M., Sere, Y. Y., Diab, N. S., Menon, A. K. & Graham, T. R.<\/strong>Phosphatidylserine translocation at the yeast trans-Golgi network regulates protein sorting into exocytic vesicles.<\/a> Mol Biol Cell 26, 4674\u20134685 (2015).<\/p>\n

Hankins, H. M., Baldridge, R. D., Xu, P. & Graham, T. R.<\/strong>Role of flippases, scramblases and transfer proteins in phosphatidylserine subcellular distribution<\/a>. Traffic 16, 35\u201347 (2015).<\/p>\n

Zhou, X., Sebastian, T. T. & Graham, T. R.<\/strong>Auto-inhibition of Drs2p, a yeast phospholipid flippase, by its carboxyl-terminal tail.<\/a> J Biol Chem 288, 31807\u201331815 (2013).<\/p>\n

Xu, P., Baldridge, R. D., Chi, R. J., Burd, C. G. & Graham, T. R.<\/strong>Phosphatidylserine flipping enhances membrane curvature and negative charge required for vesicular transport<\/a>. J Cell Biol 202, 875\u2013886 (2013).<\/p>\n

Baldridge, R. D., Xu, P. & Graham, T. R.<\/strong> Type IV P-type ATPases distinguish mono- versus diacyl phosphatidylserine using a cytofacial exit gate in the membrane domain. J Biol Chem 288, 19516\u201319527 (2013).<\/p>\n

Graham, T. R.<\/strong> Arl1 gets into the membrane remodeling business with a flippase and ArfGEF. Proc Natl Acad Sci U S A 110, 2691\u20132692 (2013).<\/p>\n

Baldridge, R. D. & Graham, T. R.<\/strong> Two-gate mechanism for phospholipid selection and transport by type IV P-type ATPases. Proc Natl Acad Sci U S A 110, E358\u2013367 (2013).<\/p>\n

Sebastian, T. T., Baldridge, R. D., Xu, P. & Graham, T. R.<\/strong> Phospholipid flippases: building asymmetric membranes and transport vesicles. Biochim Biophys Acta 1821, 1068\u20131077 (2012).<\/p>\n

Baldridge, R. D. & Graham, T. R.<\/strong> Identification of residues defining phospholipid flippase substrate specificity of type IV P-type ATPases. Proc Natl Acad Sci U S A 109, E290\u2013298 (2012).<\/p>\n

Graham, T. R.<\/strong> & Burd, C. G. Coordination of Golgi functions by phosphatidylinositol 4-kinases. Trends Cell Biol 21, 113\u2013121 (2011).<\/p>\n

Graham, T. R.<\/strong> & Kozlov, M. M. Interplay of proteins and lipids in generating membrane curvature. Curr Opin Cell Biol 22, 430\u2013436 (2010).<\/p>\n

Natarajan, P. et al. Regulation of a Golgi flippase by phosphoinositides and an ArfGEF. Nat Cell Biol 11, 1421\u20131426 (2009).<\/p>\n

Zhou, X. & Graham, T. R.<\/strong> Reconstitution of phospholipid translocase activity with purified Drs2p, a type-IV P-type ATPase from budding yeast. Proc Natl Acad Sci U S A 106, 16586\u201316591 (2009).<\/p>\n

Muthusamy, B.-P., Natarajan, P., Zhou, X. & Graham, T. R.<\/strong> Linking phospholipid flippases to vesicle-mediated protein transport. Biochim Biophys Acta 1791, 612\u2013619 (2009).<\/p>\n

Muthusamy, B.-P. et al. Control of protein and sterol trafficking by antagonistic activities of a type IV. Mol Biol Cell 20, 2920\u20132931 (2009).<\/p>\n

Liu, K., Surendhran, K., Nothwehr, S. F. & Graham, T. R.<\/strong> P4-ATPase requirement for AP-1\/clathrin function in protein transport from the trans-Golgi network and early endosomes. Mol Biol Cell 19, 3526\u20133535 (2008).<\/p>\n

Liu, K., Hua, Z., Nepute, J. A. & Graham, T. R<\/strong>. Yeast P4-ATPases Drs2p and Dnf1p are essential cargos of the NPFXD\/Sla1p endocytic pathway. Mol Biol Cell 18, 487\u2013500 (2007).<\/p>\n

Chen, S. et al. Roles for the Drs2p-Cdc50p complex in protein transport and phosphatidylserine asymmetry of the yeast plasma membrane. Traffic 7, 1503\u20131517 (2006).<\/p>\n

Xiao, J., Kim, L. S. & Graham, T. R.<\/strong> Dissection of Swa2p\/auxilin domain requirements for cochaperoning Hsp70 clathrin-uncoating activity in vivo. Mol Biol Cell 17, 3281\u20133290 (2006).<\/p>\n

Natarajan, P. & Graham, T. R.<\/strong> Measuring translocation of fluorescent lipid derivatives across yeast Golgi membranes. Methods 39, 163\u2013168 (2006).<\/p>\n

Graham, T. R.<\/strong> Flippases and vesicle-mediated protein transport. Trends Cell Biol 14, 670\u2013677 (2004).<\/p>\n

Natarajan, P., Wang, J., Hua, Z. & Graham, T. R.<\/strong> Drs2p-coupled aminophospholipid translocase activity in yeast Golgi membranes and relationship to in vivo function. Proc Natl Acad Sci U S A 101, 10614\u201310619 (2004).<\/p>\n

Graham, T. R.<\/strong> Membrane targeting: getting Arl to the Golgi. Curr Biol 14, R483\u2013485 (2004).<\/p>\n

Chim, N. et al. Solution structure of the ubiquitin-binding domain in Swa2p from Saccharomyces cerevisiae. Proteins 54, 784\u2013793 (2004).<\/p>\n

Hua, Z. & Graham, T. R<\/strong>. Requirement for neo1p in retrograde transport from the Golgi complex to the endoplasmic reticulum. Mol Biol Cell 14, 4971\u20134983 (2003).<\/p>\n

Gall, W. E. et al. Drs2p-dependent formation of exocytic clathrin-coated vesicles in vivo. Curr Biol 12, 1623\u20131627 (2002).<\/p>\n

Hua, Z., Fatheddin, P. & Graham, T. R.<\/strong> An essential subfamily of Drs2p-related P-type ATPases is required for protein trafficking between Golgi complex and endosomal\/vacuolar system. Mol Biol Cell 13, 3162\u20133177 (2002).<\/p>\n

Graham, T. R.<\/strong> Metabolic labeling and immunoprecipitation of yeast proteins. Curr Protoc Cell Biol Chapter 7, Unit 7.6 (2001).<\/p>\n

Gall, W. E. et al. The auxilin-like phosphoprotein Swa2p is required for clathrin function in yeast. Curr Biol 10, 1349\u20131358 (2000).<\/p>\n

Brigance, W. T., Barlowe, C. & Graham, T. R.<\/strong> Organization of the yeast Golgi complex into at least four functionally distinct compartments. Mol Biol Cell 11, 171\u2013182 (2000).<\/p>\n

Hopkins, B. D., Sato, K., Nakano, A. & Graham, T. R.<\/strong> Introduction of Kex2 cleavage sites in fusion proteins for monitoring localization and transport in yeast secretory pathway. Methods Enzymol 327, 107\u2013118 (2000).<\/p>\n

Chen, C. Y., Ingram, M. F., Rosal, P. H. & Graham, T. R.<\/strong> Role for Drs2p, a P-type ATPase and potential aminophospholipid translocase, in yeast late Golgi function. J Cell Biol 147, 1223\u20131236 (1999).<\/p>\n

Reynolds, T. B., Hopkins, B. D., Lyons, M. R. & Graham, T. R.<\/strong> The high osmolarity glycerol response (HOG) MAP kinase pathway controls localization of a yeast golgi glycosyltransferase. J Cell Biol 143, 935\u2013946 (1998).<\/p>\n

Chen, C. Y. & Graham, T. R.<\/strong> An arf1Delta synthetic lethal screen identifies a new clathrin heavy chain conditional allele that perturbs vacuolar protein transport in Saccharomyces cerevisiae. Genetics 150, 577\u2013589 (1998).<\/p>\n

Graham, T. R.<\/strong> & Krasnov, V. A. Sorting of yeast alpha 1,3 mannosyltransferase is mediated by a lumenal domain interaction, and a transmembrane domain signal that can confer clathrin-dependent Golgi localization to a secreted protein. Mol Biol Cell 6, 809\u2013824 (1995).<\/p>\n

Graham, T. R.<\/strong>, Seeger, M., Payne, G. S., MacKay, V. L. & Emr, S. D. Clathrin-dependent localization of alpha 1,3 mannosyltransferase to the Golgi complex of Saccharomyces cerevisiae. J Cell Biol 127, 667\u2013678 (1994).<\/p>\n<\/div>\n","protected":false},"excerpt":{"rendered":"

Preprint work: P4-ATPase control over phosphoinositide membrane asymmetry and neomycin resistance Bhawik K. Jain, H. Diessel Duan, Christina Valentine, Ariana Samiha, Huilin Li, Todd R. Graham. bioRxiv 2025.03.03.641220; doi: https:\/\/doi.org\/10.1101\/2025.03.03.641220 Published work: Jimenez M, Kyoung CK, Nabukhotna K, Watkins D, … Continue reading →<\/span><\/a><\/p>\n","protected":false},"author":3076,"featured_media":0,"parent":0,"menu_order":4,"comment_status":"closed","ping_status":"closed","template":"onecolumn-page.php","meta":{"footnotes":"","_links_to":"","_links_to_target":""},"class_list":["post-32","page","type-page","status-publish","hentry"],"_links":{"self":[{"href":"https:\/\/my.vanderbilt.edu\/grahamlab\/wp-json\/wp\/v2\/pages\/32","targetHints":{"allow":["GET"]}}],"collection":[{"href":"https:\/\/my.vanderbilt.edu\/grahamlab\/wp-json\/wp\/v2\/pages"}],"about":[{"href":"https:\/\/my.vanderbilt.edu\/grahamlab\/wp-json\/wp\/v2\/types\/page"}],"author":[{"embeddable":true,"href":"https:\/\/my.vanderbilt.edu\/grahamlab\/wp-json\/wp\/v2\/users\/3076"}],"replies":[{"embeddable":true,"href":"https:\/\/my.vanderbilt.edu\/grahamlab\/wp-json\/wp\/v2\/comments?post=32"}],"version-history":[{"count":38,"href":"https:\/\/my.vanderbilt.edu\/grahamlab\/wp-json\/wp\/v2\/pages\/32\/revisions"}],"predecessor-version":[{"id":698,"href":"https:\/\/my.vanderbilt.edu\/grahamlab\/wp-json\/wp\/v2\/pages\/32\/revisions\/698"}],"wp:attachment":[{"href":"https:\/\/my.vanderbilt.edu\/grahamlab\/wp-json\/wp\/v2\/media?parent=32"}],"curies":[{"name":"wp","href":"https:\/\/api.w.org\/{rel}","templated":true}]}}