Publications

Published work:

Jimenez M, Kyoung CK, Nabukhotna K, Watkins D, Jain BK, Best JT, Graham TR. P4-ATPase endosomal recycling relies on multiple retromer-dependent localization signals. Mol Biol Cell (2024). doi: 10.1091/mbc.E24-05-0209

Duan HD, Jain BK, Li H, Graham TR, Li H. Structural insight into an Arl1–ArfGEF complex involved in Golgi recruitment of a GRIP-domain golgin. Nat Commun15, 1942 (2024). https://doi.org/10.1038/s41467-024-46304-w

Norris AC, Mansueto AJ, Jimenez M, Yazlovitskaya EM, Jain BK, Graham TR. Flipping the script: Advances in understanding how and why P4-ATPases flip lipid across membranes. Biochim Biophys Acta Mol Cell Res. (2024) 1871(4):119700. doi: 10.1016/j.bbamcr.2024.119700

Norris AC, Yazlovitskaya EM, Zhu E, Rose BS, May JC, Gibson-Corley KN,  McLean JA, Stafford JM, Graham TR. Deficiency of the lipid flippase ATP10A causes diet-induced dyslipidemia in female miceSci Rep14, 343 (2024). https://doi.org/10.1038/s41598-023-50360-5

Yazlovitskaya EM, Graham TR.Type IV P-Type ATPases: Recent Updates in Cancer Development, Progression, and Treatment.Cancers (2023), 15, 4327. https://doi.org/10.3390/cancers15174327

Steenwyk JL, Phillips MA, Yang F, Date SS, Graham TR, Berman J, Hittinger CT, Rokas A. An orthologous gene coevolution network provides insight into eukaryotic cellular and genomic structure and functionSci. Adv.8,eabn0105(2022). DOI:10.1126/sciadv.abn0105

Graham TR.AP-3 shows off its flexibility for the cryo-EM camera (2022) Journal of Biological Chemistry, 101491. doi: https://doi.org/10.1016/j.jbc.2021.101491

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

Bai L, You Q, Jain BK, Duan HD, Kovach A, Graham TR, Li H. Transport mechanism of P4 ATPase phosphatidylcholine flippases. Elife. 2020 Dec 15;9:e62163. doi: 10.7554/eLife.62163.

Jain BK, Roland BP, Graham TR.Exofacial membrane composition and lipid metabolism regulates plasma membrane P4-ATPase substrate specificity (2020) Journal of Biological Chemistry, Volume 295, Issue 52, 17997 – 18009

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

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

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

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

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

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

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

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. COPI mediates recycling of an exocytic SNARE by recognition of a ubiquitin sorting signal. Elife. (2017). doi:10.7554/eLife.2842.

Wu Y., Takar M., Cuentas-Condori AA, Graham T.R. Neo1 and phosphatidylethanolamine contribute to vacuole membrane fusion in Saccharomyces cerevisiae. Cell Logist. 2016 Aug 25;6(3):e1228791. eCollection 2016 Jul-Sep.

Roland B.P., Graham T.R.Decoding P4-ATPase substrate interactions. Crit Rev Biochem Mol Biol. (2016) Nov/Dec;51(6):513-527. doi: 10.1080/10409238.2016.1237934. Epub 2016 Oct 4. Review.

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

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

Hankins, H. M., Sere, Y. Y., Diab, N. S., Menon, A. K. & Graham, T. R.Phosphatidylserine translocation at the yeast trans-Golgi network regulates protein sorting into exocytic vesicles. Mol Biol Cell 26, 4674–4685 (2015).

Hankins, H. M., Baldridge, R. D., Xu, P. & Graham, T. R.Role of flippases, scramblases and transfer proteins in phosphatidylserine subcellular distribution. Traffic 16, 35–47 (2015).

Zhou, X., Sebastian, T. T. & Graham, T. R.Auto-inhibition of Drs2p, a yeast phospholipid flippase, by its carboxyl-terminal tail. J Biol Chem 288, 31807–31815 (2013).

Xu, P., Baldridge, R. D., Chi, R. J., Burd, C. G. & Graham, T. R.Phosphatidylserine flipping enhances membrane curvature and negative charge required for vesicular transport. J Cell Biol 202, 875–886 (2013).

Baldridge, R. D., Xu, P. & Graham, T. R. Type IV P-type ATPases distinguish mono- versus diacyl phosphatidylserine using a cytofacial exit gate in the membrane domain. J Biol Chem 288, 19516–19527 (2013).

Graham, T. R. Arl1 gets into the membrane remodeling business with a flippase and ArfGEF. Proc Natl Acad Sci U S A 110, 2691–2692 (2013).

Baldridge, R. D. & Graham, T. R. Two-gate mechanism for phospholipid selection and transport by type IV P-type ATPases. Proc Natl Acad Sci U S A 110, E358–367 (2013).

Sebastian, T. T., Baldridge, R. D., Xu, P. & Graham, T. R. Phospholipid flippases: building asymmetric membranes and transport vesicles. Biochim Biophys Acta 1821, 1068–1077 (2012).

Baldridge, R. D. & Graham, T. R. Identification of residues defining phospholipid flippase substrate specificity of type IV P-type ATPases. Proc Natl Acad Sci U S A 109, E290–298 (2012).

Graham, T. R. & Burd, C. G. Coordination of Golgi functions by phosphatidylinositol 4-kinases. Trends Cell Biol 21, 113–121 (2011).

Graham, T. R. & Kozlov, M. M. Interplay of proteins and lipids in generating membrane curvature. Curr Opin Cell Biol 22, 430–436 (2010).

Natarajan, P. et al. Regulation of a Golgi flippase by phosphoinositides and an ArfGEF. Nat Cell Biol 11, 1421–1426 (2009).

Zhou, X. & Graham, T. R. 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, 16586–16591 (2009).

Muthusamy, B.-P., Natarajan, P., Zhou, X. & Graham, T. R. Linking phospholipid flippases to vesicle-mediated protein transport. Biochim Biophys Acta 1791, 612–619 (2009).

Muthusamy, B.-P. et al. Control of protein and sterol trafficking by antagonistic activities of a type IV. Mol Biol Cell 20, 2920–2931 (2009).

Liu, K., Surendhran, K., Nothwehr, S. F. & Graham, T. R. P4-ATPase requirement for AP-1/clathrin function in protein transport from the trans-Golgi network and early endosomes. Mol Biol Cell 19, 3526–3535 (2008).

Liu, K., Hua, Z., Nepute, J. A. & Graham, T. R. Yeast P4-ATPases Drs2p and Dnf1p are essential cargos of the NPFXD/Sla1p endocytic pathway. Mol Biol Cell 18, 487–500 (2007).

Chen, S. et al. Roles for the Drs2p-Cdc50p complex in protein transport and phosphatidylserine asymmetry of the yeast plasma membrane. Traffic 7, 1503–1517 (2006).

Xiao, J., Kim, L. S. & Graham, T. R. Dissection of Swa2p/auxilin domain requirements for cochaperoning Hsp70 clathrin-uncoating activity in vivo. Mol Biol Cell 17, 3281–3290 (2006).

Natarajan, P. & Graham, T. R. Measuring translocation of fluorescent lipid derivatives across yeast Golgi membranes. Methods 39, 163–168 (2006).

Graham, T. R. Flippases and vesicle-mediated protein transport. Trends Cell Biol 14, 670–677 (2004).

Natarajan, P., Wang, J., Hua, Z. & Graham, T. R. Drs2p-coupled aminophospholipid translocase activity in yeast Golgi membranes and relationship to in vivo function. Proc Natl Acad Sci U S A 101, 10614–10619 (2004).

Graham, T. R. Membrane targeting: getting Arl to the Golgi. Curr Biol 14, R483–485 (2004).

Chim, N. et al. Solution structure of the ubiquitin-binding domain in Swa2p from Saccharomyces cerevisiae. Proteins 54, 784–793 (2004).

Hua, Z. & Graham, T. R. Requirement for neo1p in retrograde transport from the Golgi complex to the endoplasmic reticulum. Mol Biol Cell 14, 4971–4983 (2003).

Gall, W. E. et al. Drs2p-dependent formation of exocytic clathrin-coated vesicles in vivo. Curr Biol 12, 1623–1627 (2002).

Hua, Z., Fatheddin, P. & Graham, T. R. 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, 3162–3177 (2002).

Graham, T. R. Metabolic labeling and immunoprecipitation of yeast proteins. Curr Protoc Cell Biol Chapter 7, Unit 7.6 (2001).

Gall, W. E. et al. The auxilin-like phosphoprotein Swa2p is required for clathrin function in yeast. Curr Biol 10, 1349–1358 (2000).

Brigance, W. T., Barlowe, C. & Graham, T. R. Organization of the yeast Golgi complex into at least four functionally distinct compartments. Mol Biol Cell 11, 171–182 (2000).

Hopkins, B. D., Sato, K., Nakano, A. & Graham, T. R. Introduction of Kex2 cleavage sites in fusion proteins for monitoring localization and transport in yeast secretory pathway. Methods Enzymol 327, 107–118 (2000).

Chen, C. Y., Ingram, M. F., Rosal, P. H. & Graham, T. R. Role for Drs2p, a P-type ATPase and potential aminophospholipid translocase, in yeast late Golgi function. J Cell Biol 147, 1223–1236 (1999).

Reynolds, T. B., Hopkins, B. D., Lyons, M. R. & Graham, T. R. The high osmolarity glycerol response (HOG) MAP kinase pathway controls localization of a yeast golgi glycosyltransferase. J Cell Biol 143, 935–946 (1998).

Chen, C. Y. & Graham, T. R. An arf1Delta synthetic lethal screen identifies a new clathrin heavy chain conditional allele that perturbs vacuolar protein transport in Saccharomyces cerevisiae. Genetics 150, 577–589 (1998).

Graham, T. R. & 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, 809–824 (1995).

Graham, T. R., 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, 667–678 (1994).