Selected publications

Larsson E, Morén B, McMahon KA, Parton RG, Lundmark R; Dynamin2 functions as an accessory protein to reduce the rate of caveola internalization. Journal of Cell Biology. Apr 3;222(4):e202205122. doi: 10.1083/jcb.202205122. Epub 2023 Feb 2.PMID: 36729022 (2023).

Here, we show that the GTPase Dynamin2 does not perform caveolae scission, but instead confine caveolae to the cell surface, which is in contrast to what has been the general belief for over 20 years.

LiuK-C, PaceH, LarssonE, HossainS, KabedevA, ShuklaA, JerschabekV, MohanJ, BergströmC AS, BallyM, Schwieger C, Hubert Mand Lundmark R; Membrane insertion mechanism of the caveola coat protein Cavin1. Proceedings of the National Academy of Sciences, USA. Jun 21;119(25):e2202295119. doi: 10.1073/pnas.2202295119. Epub 2022 Jun 13. PMID: 35696574 (2022)

This paper determine how the trimeric helical region of Cavin1 interacts with lipid membranes and show that this region of the protein inserts into membranes through a mechanism that require uncoiling of this trimeric domain.

Hubert M, Larsson E, Vegesna NVG, Ahnlund M, Johansson AI, Moodie LWK and Lundmark R; Lipid accumulation controls the balance between surface connection and scission of caveolae eLife. May 4;9:e55038. doi:10.7554/eLife.55038. (2020).

This study demonstrates that that sphingomyelin stabilizes caveolae to the cell surface, while cholesterol and glycosphingolipids drive caveolae scission from the PM. Whilst all three lipids accumulated specifically in caveolae, cholesterol and sphingomyelin were actively sequestered, whereas glycosphingolipids diffused freely. The ATPase EHD2 restricts lipid diffusion and counteracts lipid-induced scission. We propose that specific lipid accumulation in caveolae generates an intrinsically unstable domain prone to scission if not restrained by EHD2 at the caveolae neck. This provides a mechanistic link between caveolae and their ability to sense the PM lipid composition.

Daste F*, Walrant A*, Holst MR*, Gadsby JR*, Mason J, Lee, J, Brook D, Mettlen M, Larsson E, Lee SF, Lundmark R and Gallop JL; Control of actin polymerization via the coincidence of phosphoinositides and high membrane curvature. Journal of Cell Biology, 216, 3745-3765, (2017). ^* These authors contributed equally to this work.

This paper demonstrates a novel coincidence detection mechanism used by the coat-protein SNX9 to progress the bending and scission of membranes vesicles during endocytosis.

HolstMR, Vidal-Quadras M, LarssonE, SongJ, Hubert M, Blomberg J, Lundborg M, Landström M and Lundmark R; Clathrin-independent endocytosis suppresses cancer cell blebbing and invasion. Cell Reports, 20, 1893-1905, (2017).

This paper shows that how endocytosis is regulated by membrane tension and reveals the mechanistic details for how this is sensed by the protein GRAF1. Furthermore, we show that this endocytic response suppress cancer cell blebbing and metastasis.

Hoernke M, Mohan J, Larsson E, Blomberg J, Kahra D, Westenhoff S, Schwieger C, Lundmark R; EHD2 restrains dynamics of caveolae by an ATP‑dependent, membrane-bound, open conformation Proceedings of the National Academy of Sciences, USA,114(22), E4360-E4369 (2017).

Here, we reveal the active, membrane-bound conformation of EHD2 using a novel structural approach and provide a detailed mechanistic understanding of the various steps of the mechanistic cycle that control caveolae dynamics in cells. We demonstrate that EHD2 cycles between an inactive closed conformation and an open active conformation in an ATP and membrane dependent manner.

Vidal-QuadrasM, HolstM, R, FrancisM, K, Larssson E, HachimiM, YauW, L, PeränenJ, Martín-Belmonte Fand Lundmark R; Endocytic turnover of Rab8 controls cell polarization; Journal of Cell Science, 130, 1147-1157. (2017).

This paper demonstrates that the equilibrium between endo- and exocytosis is regulated by direct coupling of internalisation of the key secretory protein Rab8 by the endocytic protein GRAF1. Furthermore, we demonstrate that this is essential for the control of cell polarisation.

Mohan J, Morén B, Larsson E, Holst MR, Lundmark R; Cavin3 interacts with cavin1 and caveolin1 to increase surface dynamics of caveolae. Journal of Cell Science, 128, 979-91 (2015).

This paper shows how the cavin-coat proteins form homo- and hetero-complexes via a conserved domain and how cavin3 interacts with the caveolae protein caveolin to destabilise caveolae at the cell surface.

Morén B, Shah C, Howes MT, Schieber NL, McMahon HT, Parton RG, DaumkeO, Lundmark R; EHD2 regulates caveola dynamics via ATP-driven targeting and oligomerization. Molecular Biology of the Cell, 23, 1316-29 (2012).

This is the first paper demonstrating that EHD2 is a key molecular component of caveolae and that this protein assembles at the neck region and stabilises caveolae to the cell surface.

Lundmark R, Doherty GJ, Vallis Y, Howes M, Cortese K, Parton R, McMahon H.T; The GTPase activating protein GRAF1 regulates the CLIC/GEEC endocytic pathway. Current Biology, 18, 1802-8, (2008).

This paper shows that the protein GRAF1 bends membranes into a novel type of dynamic endocytic carriers which are important for fast internalisation of large amounts of fluid.

Daumke O¹, Lundmark R¹, Vallis Y, Martens S, Butler PJ, McMahon H.T; Architecture and mechanistic insight into an EHD ATPase involved in membrane remodeling. Nature, 449, 923-927, (2007). ¹ These authors contributed equally to this work.

This study revealed the structure of EHD2 and showed how this family of proteins assemble into ring-like structure on membranes in order to drive membrane curvature.

Full publicationlist

Peer-reviewed original articles

Pulkkinen LIA, Barrass SV, Lindgren M, Pace H, Överby AK, Anastasia M, Bally M, Lundmark R, Butcher SJ. Simultaneous membrane and RNA binding by Tick-Borne Encephalitis Virus capsid protein. PLOS pathogens, Feb 14;19(2):e1011125. doi: 10.1371/journal.ppat.1011125. Online ahead of print. PMID: 36787339 (2023)

Co-corresponding senior author

Larsson E, Morén B, McMahon KA, Parton RG, Lundmark R; Dynamin2 functions as an accessory protein to reduce the rate of caveola internalization. J Cell Biol. Apr 3;222(4):e202205122. doi: 10.1083/jcb.202205122. Epub 2023 Feb 2.PMID: 36729022 (2023)

Fryklund C, Neuhaus M, Morén B, Borreguero-Muñoz A, Lundmark R, Stenkula KG; Expansion of the Inguinal Adipose Tissue Depot Correlates With Systemic Insulin Resistance in C57BL/6J Mice. Front Cell Dev Biol. Sep 7;10:942374. doi: 10.3389/fcell.2022.942374. eCollection 2022.PMID: 36158197 (2022)

Wang T, Sarwar M, Whitchurch JB, Collins HM, Green T, Semenas J, Ali A, Roberts CJ, Morris RD, Hubert M, Chen S, El-Schich Z, Wingren AG, Grundström T, Lundmark R, Mongan NP, Gunhaga L, Heery DM, Persson JL; PIP5K1α is Required for Promoting Tumor Progression in Castration-Resistant Prostate Cancer. Front Cell Dev Biol. Mar 21;10:798590. doi: 10.3389/fcell.2022.798590. eCollection 2022.PMID: 35386201 (2022)

Pastuła A, Lundmark R; Induction of Epithelial-mesenchymal Transition in MDCK II Cells Bio Protoc. Feb 5;11(3):e3903. doi: 10.21769/BioProtoc.3903. eCollection 2021 Feb 5. PMID: 33732790. (2021)

Wright L, Joyce P, Barnes TJ, Lundmark R, Bergström CAS, Hubert M, Prestidge CA; A Comparison of Chitosan, Mesoporous Silica and Poly(lactic-co-glycolic) Acid Nanocarriers for Optimising Intestinal Uptake of Oral Protein Therapeutics

J Pharm Sci. Jan;110(1):217-227. doi: 10.1016/j.xphs.2020.09.026. (2021)

Wesén E, Lundmark R, Esbjörner EK; Role of Membrane Tension Sensitive Endocytosis and Rho GTPases in the Uptake of the Alzheimer's Disease Peptide Aβ(1-42) ACS Chem Neurosci. Jul 1;11(13):1925-1936. doi: 10.1021/acschemneuro.0c00053. (2020)

Matthaeus C, Lahmann I, Kunz S, Jonas W, Melo AA, Lehmann M, Larsson E, Lundmark, R, Kern M, Blüher M, Olschowski H, Kompa J, Brügger B, Müller DN, Haucke V, Schürmann A, Birchmeier C, Daumke, O; EHD2-mediated restriction of caveolar dynamics regulates cellular fatty acid uptake. Proceedings of the National Academy of Sciences, USA, Mar 31;117(13):7471-7481. doi: 10.1073/pnas.1918415117. Epub 2020 Mar 13. PMID: 32170013 (2020).

Yau WL, Nguyen-Dinh V, Larsson E, Lindqvist R, Överby AK, Lundmark R; Model System for the Formation of Tick-Borne Encephalitis Virus Replication Compartments without Viral RNA Replication. Journal of Virology, Jun 26, JVI.00292-19. doi: 10.1128/JVI.00292-19, (2019)

Rodrigues L, Schneider F, Zhang X, Larsson E, Moodie L, Dietz H, Papadakis CM, Gerhard Winter G, Lundmark R, Hubert M; Cellular uptake of self-assembled phytantriol-based hexosomes is independent of major endocytic machineries. Journal of Colloid and interphase science, 553, 820-833. doi: 10.1016/j.jcis.2019.06.045. (2019)

Morén B, Hansson B, Lundmark R, Göransson O, Stenkula KG; EHD2 regulates adipocyte function and is enriched at cell surface-associated lipid droplets in primary human adipocytes. Molecular Biology of the Cell, 30, 1147-59, doi: 10.1091/mbc.E18-10-0680 (2019).

Moodie LWK, Hubert M, Zhou X, Albers MF, Lundmark R, Wanrooij S and Christian Hedberg; Photoactivated Colibactin Probes Induce Cellular DNA Damage. Angewandte Chemie international edition, 58, 1417-22, doi: 10.1002/ange.201812326, (2019).

Nygard-Skalman L, Holst MR, Larsson E, Lundmark R; Plasma membrane damage caused by Listeriolysin O is not repaired through endocytosis of the membrane pore. Biology Open, 7, doi: 10.1242/bio.03528, (2018).

Kong Z, Jia S, Chabes AL, Appelblad P, Lundmark R, Moritz T, Chabes A; Simultaneous determination of ribonucleoside and deoxyribonucleoside triphosphates in biological samples by hydrophilic interaction liquid chromatography coupled with tandem mass spectrometry. Nucleic Acids Research. 46(11), doi: 10.1093/nar/gky203. (2018).

Vonderstein K, Nilsson E, Hubel P, Nygård Skalman L, Upadhyay A, Pasto J, Andreas Pichlmair A, Lundmark R, and Överby A; Viperin targets flavivirus virulence by inducing assembly of non-infectious capsid particles. Journal of Virology, 92. JVI.01751-17. (2017).

Kindstedt E, Koskinen Holm C, Sulniute R, Martinez-Carrasco I, Lundmark R, and Lundberg P; CCL11, a novel mediator of inflammatory bone resorption. Scientific Reports, 7(1):5334. (2017).

MeloAA, HegdeBG, ShahC, LarssonE, IsasJM, KunzS, LundmarkR, LangenR, Daumke O; Structural insights into the activation mechanism of dynamin-like Eps15-homology domain proteins; Proceedings of the National Academy of Sciences, USA, 114(22), 5629-5634 (2017).

Vdovikova S, Luhr M, Szalai P, Nygård Skalman L, Francis MK, Lundmark R, Engedal N, Johansson J, Nyunt Wai S; A novel role of Listeria monocytogenes membrane vesicles in inhibition of autophagy and cell death. Frontiers in Cellular and Infection Microbiology, 7:154. (2017).

Bagnato P, CastagninoA, Cortese K, BonoM, GrassoS, BelleseG, DanieleT, LundmarkR, DefilippiP, CastagnolaP and TacchettiC; Cooperative but distinct early co-signaling events originate from ERBB2 and ERBB1 receptors upon trastuzumab treatment in breast cancer cells. Oncotarget, 8(36), 60109-60122. (2017).

Storm RJ, Persson BD, Nygård Skalman L, Frängsmyr L, Lindström M, Rankin G, Lundmark R, Pedrosa Domellöf F, Arnberg N; Human adenovirus type 37 uses αVβ1 and α3β1 integrins for infection of human corneal cells. Journal of Virology, 91(5) (2017).

Francis MK, Holst MR, Vidal-Quadras M, Henriksson S, Sandblad L and Lundmark R; Endocytic membrane turnover at the leading edge is driven by a transient interaction between Cdc42 and GRAF1. Journal of Cell Science, 128, 4183-95 (2015).

Rompikuntal PK, Vdovikova S, Duperthuy M, Johnson TL, Monika Åhlund M, Lundmark R, Oscarsson J, Sandkvist M, Uhlin BE, Wai SN; Outer membrane vesicle-mediated export of processed PrtV protease from Vibrio cholera; PLOS one, 10(7) (2015).

Mohan J, Morén B, Larsson E, Holst MR, Lundmark R; Cavin3 interacts with cavin1 and caveolin1 to increase surface dynamics of caveolae. Journal of Cell Science, 128, 979-91 (2015).

Olofsson A¹, Nygård Skalman L¹, Ikenna O, Lundmark R, and Arnqvist A; Uptake of Helicobacter pylori vesicles is facilitated by clathrin-dependent and clathrin-independent endocytic pathways; mBio, 5, e00979-14 (2014) ¹ These authors contributed equally to this work.

Shah C, Hegde B,Morén B, Behrmann E, Mielke T, Moenke G, Spahn C, Richard Lundmark R, Daumke O, Ralf Langen R;Structural insights into membrane interaction and caveolar targeting of dynamin-like EHD2. Structure, 22, 409-20 (2014).

Cortese K, Howes M.T, Lundmark R, Tagliatti E, Bagnato P, Petrelli A, Bono M, McMahon H.T, Parton R.G, Tacchetti C; The HSP90 inhibitor geldanamycin perturbs endosomal structure and drives recycling ErbB2 and Transferrin to modified MVBs/lysosomal compartments. Molecular Biology of the Cell, 24, 129-44 (2013).

Doherty GJ, Åhlund MK, Howes M, Morén B, Parton RG, McMahon HT, Lundmark R;The endocytic protein GRAF1 is directed to cell matrix adhesion sites and regulates cell spreading. Molecular Biology of the Cell, 22, 4380-9 (2011).

Howes MT, Kirkham M, Riches J, Cortese K, Walser PJ, Simpson F, Hill MM, Jones A, Lundmark R, Lindsay MR, Hernandez-Deviez DJ, Hadzic G, McCluskey A, Bashir R, Liu L, Pilch P, McMahon H, Robinson PJ, Hancock JF, Mayor S, Parton RG; Clathrin-independent carriers form a high capacity endocytic sorting system at the leading edge of migrating cells. Journal of Cell Biology, 190, 675-91 (2010).

Eberth A, Lundmark R, Gremer L, Dvorsky R, Koessmeier KT, McMahon HT, Ahmadian MR; A BAR domain-mediated auto inhibitory mechanism for the GRAF-family of RhoGAPs. Biochemical Journal, 417, 371-7, (2009).

Lundmark R, Doherty GJ, Vallis Y, Howes M, Cortese K, Parton R, McMahon H.T; The GTPase activating protein GRAF1 regulates the CLIC/GEEC endocytic pathway. Current Biology, 18, 1802-8, (2008).

Lundmark R, Doherty GJ, Vallis Y, Peter BJ, McMahon H.T; Arf family GTP loading is activated by, and generates, positive membrane curvature. Biochemical Journal, 414, 189-194, (2008).

Håberg K, Lundmark R, & Carlsson S.R; SNX18 is an SNX9 paralog that acts as a membrane tubulator in AP-1-positive endosomal trafficking. Journal of Cell Science, 121, 1495-505, (2008).

Pylypenko O, Ignatev A, Lundmark R, Rasmuson E, Carlsson SR, Rak A; A combinatorial approach to crystallization of PX-BAR unit of the human Sorting Nexin 9. Journal of Structural Biology, 162, 356-60, (2008).

Pylypenko O, Lundmark R, Rasmuson E, Carlsson SR, Rak A; Structure of the PX-BAR- membrane remodeling unit of SNX9. EMBO journal, 26, 4788-8000, (2007)

Marchès. O, Batchelor. M, Shaw. R.K, Patel. A, Cummings. N, Nagai^.T, Sasakawa^.C, Carlsson^.S.R, Lundmark. R, Cougoule.C, Caron. E, Knutton. S, Connerton. I, and Frankel G; EspF of enteropathogenic E. coli binds sorting nexin 9. Journal of Bacteriology, 188, 3110-3115, (2006).

Lundmark. R, Carlsson S; Expression and properties of sorting nexin 9 in dynamin-mediated endocytosis. Methods in Enzymology, 404, 545-556, (2005).

Lundmark. R Carlsson. S; Regulated membrane recruitment of Dynamin-2 is mediated by sorting nexin 9. Journal of Biological Chemistry, 279, 42694-702, (2004).

Lundmark. R Carlsson. S; Sorting nexin 9 participates in clathrin-mediated endocytosis through interactions with the core components. Journal of Biological Chemistry, 278, 46772-81, (2003).

Lundmark. R Carlsson. S.; The b-Appendages of the four adaptor-protein (AP) complexes: structure and binding properties, and identification of sorting nexin 9 as an accessory protein to AP-2 Domains. Biochemical Journal, 362, 597-607, (2002).

Research review articles

Hubert M, Larsson E and Lundmark R; Keeping in touch with the membrane; protein- and lipid-mediated confinement of caveolae to the cell surface. Biochemical Society Transactions. Accepted. invited peer-reviewed. (2020).

Parton RG, del Pozo MA, Vassilopoulos S, Nabi I, Le Lay S, Lundmark R, Kenworthy AK, Camus A, Blouin CM, Sessa WC, and Lamaze C; Caveolae: The FAQs. Traffic, Jan;21(1):181-185. doi: 10.1111/tra.12689. Epub 2019 Sep 9. (2020).

Lundmark R and Carlsson S, R; Driving membrane curvature in clathrin-dependent and clathrin-independent endocytosis. Seminars in Cell and Developmental Biology, Jun;21(4):363-70. invited peer-reviewed. (2010).

Doherty G and Lundmark R; GRAF-dependent endocytosis. Biochemical Society Transactions. Oct;37, 1061-5. invited peer-reviewed. (2009).

Lundmark R and Carlsson S,R; SNX9: A prelude to vesicular release. Journal of Cell Science 122, 5-11. (2009) invited peer-reviewed.

Book chapters

Larsson E., Hubert M., Lundmark R.; Analysis of protein and lipid interactions using liposome co-sedimentation assays. In: Blouin C.M. (eds) Caveolae. Methods in Molecular Biology, in press, Humana, New York, NY.

(For full publication list see below)

Lundmark-lab

Selected publications