Uses and abuses of macropinocytosis

Bloomfield, Gareth; Kay, Robert R.

doi:10.1242/jcs.176149

Cited by 193Cellular transport and secretionAutophagy in Disease and TherapyNanoparticle-Based Drug Delivery

Uses and abuses of macropinocytosis

Bloomfield, Gareth, Kay, Robert R.·2016·Journal of Cell Science

DOI 10.1242/jcs.176149

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Abstract

Macropinocytosis is a means by which eukaryotic cells ingest extracellular liquid and dissolved molecules. It is widely conserved amongst cells that can take on amoeboid form and, therefore, appears to be an ancient feature that can be traced back to an early stage of evolution. Recent advances have highlighted how this endocytic process can be subverted during pathology – certain cancer cells use macropinocytosis to feed on extracellular protein, and many viruses and bacteria use it to enter host cells. Prion and prion-like proteins can also spread and propagate from cell to cell through macropinocytosis. Progress is being made towards using macropinocytosis therapeutically, either to deliver drugs to or cause cell death by inducing catastrophically rapid fluid uptake. Mechanistically, the Ras signalling pathway plays a prominent and conserved activating role in amoebae and in mammals; mutant amoebae with abnormally high Ras activity resemble tumour cells in their increased capacity for growth using nutrients ingested through macropinocytosis. This Commentary takes a functional and evolutionary perspective to highlight progress in understanding and use of macropinocytosis, which is an ancient feeding process used by single-celled phagotrophs that has now been put to varied uses by metazoan cells and is abused in disease states, including infection and cancer.

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Release of growth factors from macrophages, such as CSF-1, induces macropinocytosis.
“In fact, release of growth factors from macrophages, such as colony-stimulating factor-1 (CSF-1), induces macropinocytosis [34].”
From Insights of Endocytosis Signaling in Health and Disease (2023) · cites this paper as [34]

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Dasgupta, S. B., & Pieters, J. (2014) · PLoS Pathogens · doi:10.1371/journal.ppat.1003879 · Cited by 90 · see citing works
PIP3-dependent macropinocytosis is incompatible with chemotaxis
Veltman, D. M., Lemieux, M. G., Knecht, D. A., & Insall, R. H. (2014) · The Journal of Cell Biology · doi:10.1083/jcb.201309081 · Cited by 89 · see citing works
Actin dynamics regulates dendritic cell-mediated transfer of HIV-1 to T cells
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Visualization of Actin Dynamics During Macropinocytosis and Exocytosis
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Neuropilin-1 and heparan sulfate proteoglycans cooperate in cellular uptake of nanoparticles functionalized by cationic cell-penetrating peptides
Pang, H., Braun, G. B., & Ruoslahti, E. I. (2015) · Science Advances · doi:10.1126/sciadv.1500821 · Cited by 83 · see citing works
Pinocytosis by Malignant Cells
Lewis, W. H. (1937) · American Journal of Cancer · doi:10.1158/ajc.1937.666 · Cited by 81 · see citing works
SOD1 protein aggregates stimulate macropinocytosis in neurons to facilitate their propagation
Zeineddine, R., Pundavela, J., Corcoran, L., Stewart, E. M., Do‐Ha, D., Bax, M., Guillemin, G. J., Vine, K. L., Hatters, D. M., Ecroyd, H. W., et al. (2015) · Molecular Neurodegeneration · doi:10.1186/s13024-015-0053-4 · Cited by 75 · see citing works
Sequential Activities of Phosphoinositide 3-Kinase, PKB/Akt, and Rab7 during Macropinosome Formation inDictyostelium
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A growth factor signaling cascade confined to circular ruffles in macrophages
Welliver, T. P., & Swanson, J. A. (2012) · Biology Open · doi:10.1242/bio.20121784 · Cited by 72 · see citing works
Myosin I Links PIP 3 Signaling to Remodeling of the Actin Cytoskeleton in Chemotaxis
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Extracellular wildtype and mutant SOD1 induces ER–Golgi pathology characteristic of amyotrophic lateral sclerosis in neuronal cells
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Negative Guidance Factor-Induced Macropinocytosis in the Growth Cone Plays a Critical Role in Repulsive Axon Turning
Kolpak, A., Jiang, J., Guo, D., Standley, C., Bellve, K. D., Fogarty, K. E., & Bao, Z. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.2355-09.2009 · Cited by 66 · see citing works
The role of macropinocytosis in the propagation of protein aggregation associated with neurodegenerative diseases
Zeineddine, R., & Yerbury, J. J. (2015) · Frontiers in Physiology · doi:10.3389/fphys.2015.00277 · Cited by 64 · see citing works
Nerve growth factor activation of the TrkA receptor induces cell death, by macropinocytosis, in medulloblastoma Daoy cells
Li, C., MacDonald, J. I., Hryciw, T., & Meakin, S. O. (2009) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2009.06507.x · Cited by 62 · see citing works
Dictyostelium uses ether‐linked inositol phospholipids for intracellular signalling
Clark, J. P., Kay, R. R., Kielkowska, A., Niewczas, I. S., Fets, L., Oxley, D., Stephens, L., & Hawkins, P. T. (2014) · The EMBO Journal · doi:10.15252/embj.201488677 · Cited by 56 · see citing works
Self-citation
Self-organizing actin waves that simulate phagocytic cup structures
Gerisch, G. (2010) · PMC Biophysics · doi:10.1186/1757-5036-3-7 · Cited by 54 · see citing works
Salmonella infects B cells by macropinocytosis and formation of spacious phagosomes but does not induce pyroptosis in favor of its survival
Rosales-Reyes, R., Pérez-López, A., Sánchez‐Gómez, C., Hernández-Mote, R. R., Castro-Eguiluz, D., Ortiz-Navarrete, V. F., & Alpuche-Aranda, C. M. (2012) · Microbial Pathogenesis · doi:10.1016/j.micpath.2012.03.007 · Cited by 52 · see citing works
Ruffles limit diffusion in the plasma membrane during macropinosome formation
Welliver, T. P., Chang, S. L., Linderman, J. J., & Swanson, J. A. (2011) · Journal of Cell Science · doi:10.1242/jcs.091538 · Cited by 51 · see citing works
Sucker-like structures on the pathogenic amoeba Naegleria fowleri
John, D. T., Cole, T. B., & Marciano‐Cabral, F. (1984) · Applied and Environmental Microbiology · doi:10.1128/aem.47.1.12-14.1984 · Cited by 50 · see citing works
Antigen stored in dendritic cells after macropinocytosis is released unprocessed from late endosomes to target B cells
Roux, D. L., Bon, A. L., Dumas, A., Taleb, K., Sachse, M., Sikora, R., Julithe, M., Benmerah, A., Bismuth, G., & Niedergang, F. (2011) · Blood · doi:10.1182/blood-2011-02-336123 · Cited by 48 · see citing works
Arf6 controls beta-amyloid production by regulating macropinocytosis of the Amyloid Precursor Protein to lysosomes
Tang, W., Tam, J. H. K., Seah, C., Chiu, J., Tyrer, A. E., Cregan, S. P., Meakin, S. O., & Pasternak, S. (2015) · Molecular Brain · doi:10.1186/s13041-015-0129-7 · Cited by 42 · see citing works
The ins-and-outs of endosomal antigens for cross-presentation
Schuette, V., & Burgdorf, S. (2013) · Current Opinion in Immunology · doi:10.1016/j.coi.2013.11.001 · Cited by 41 · see citing works
Dynamics of Actin Waves on Patterned Substrates: A Quantitative Analysis of Circular Dorsal Ruffles
Bernitt, E., Koh, C.-G., Gov, N. S., & Döbereiner, J. (2015) · PLoS ONE · doi:10.1371/journal.pone.0115857 · Cited by 41 · see citing works
Syntaxin 1B Suppresses Macropinocytosis and Semaphorin 3A-Induced Growth Cone Collapse
Kabayama, H., Takeuchi, M., Taniguchi, M., Tokushige, N., Kozaki, S., Mizutani, A., Nakamura, T., & Mikoshiba, K. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.2718-10.2011 · Cited by 41 · see citing works
Phosphoinositides and engulfment
Swanson, J. A. (2014) · Cellular Microbiology · doi:10.1111/cmi.12334 · Cited by 39 · see citing works
The Arf GTPase-Activating Protein Family Is Exploited by Salmonella enterica Serovar Typhimurium To Invade Nonphagocytic Host Cells
Davidson, A. C., Humphreys, D., Brooks, A. B. E., Hume, P. J., & Koronakis, V. E. (2015) · mBio · doi:10.1128/mbio.02253-14 · Cited by 36 · see citing works
Selective localization of myosin‐ I proteins in macropinosomes and actin waves
Brzeska, H., Koech, H., Pridham, K. J., Korn, E. D., & Titus, M. A. (2016) · Cytoskeleton · doi:10.1002/cm.21275 · Cited by 35 · see citing works
An Acto-Myosin II Constricting Ring Initiates the Fission of Activity-Dependent Bulk Endosomes in Neurosecretory Cells
Gormal, R. S., Nguyen, T. H., Martin, S., Papadopulos, A., & Meunier, F. A. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.3228-14.2015 · Cited by 35 · see citing works
Pinocytosis of inorganic salts by Amoeba proteus (Chaos diffluens).
Chapman-Andresen, C. (1958) · PubMed · Cited by 34 · see citing works
RAB7 counteracts PI3K-driven macropinocytosis activated at early stages of melanoma development
Alonso‐Curbelo, D., Osterloh, L., Cañón, E., Calvo, T. G., Martínez-Herranz, R., Karras, P., Martı́nez, S., Riveiro‐Falkenbach, E., Romero, P. L. O., Rodríguez‐Peralto, J. L., et al. (2015) · Oncotarget · doi:10.18632/oncotarget.4055 · Cited by 26 · see citing works
Micropinocytosis and Rhopheocytosis
Policard, A., & BESSIS, M. C. (1962) · Nature · doi:10.1038/194110a0 · Cited by 25 · see citing works

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Cellular Adaptation to Hypoxia through Hypoxia Inducible Factors and beyond
Lee, P., Chandel, N. S., & Simon, M. C. (2020) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-020-0227-y · Cited by 1,272 · see citing works
Metabolic regulation of cell growth and proliferation
Zhu, J., & Thompson, C. B. (2019) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-019-0123-5 · Cited by 1,106 · see citing works
Understanding nanoparticle endocytosis to improve targeting strategies in nanomedicine
de Almeida, M. S., Sušnik, E., Drašler, B., Taladriz‐Blanco, P., Petri‐Fink, A., & Rothen‐Rutishauser, B. (2021) · Chemical Society Reviews · doi:10.1039/d0cs01127d · Cited by 1,108 · see citing works
New aspects of amino acid metabolism in cancer
Vettore, L. A., Westbrook, R. L., & Tennant, D. A. (2019) · British Journal of Cancer · doi:10.1038/s41416-019-0620-5 · Cited by 504 · see citing works
Brief update on endocytosis of nanomedicines
Patel, S., Kim, J., Herrera‐Barrera, M., Mukherjee, A., Kabanov, A. V., & Sahay, G. (2019) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2019.08.004 · Cited by 402 · see citing works
Nutrient acquisition strategies of mammalian cells
Palm, W., & Thompson, C. B. (2017) · Nature · doi:10.1038/nature22379 · Cited by 388 · see citing works
Cell-Surface Interactions on Arginine-Rich Cell-Penetrating Peptides Allow for Multiplex Modes of Internalization
Futaki, S., & Nakase, I. (2017) · Accounts of Chemical Research · doi:10.1021/acs.accounts.7b00221 · Cited by 277 · see citing works
The Non-Essential Amino Acid Cysteine Becomes Essential for Tumor Proliferation and Survival
Combs, J. A., & DeNicola, G. M. (2019) · Cancers · doi:10.3390/cancers11050678 · Cited by 272 · see citing works
Bacterial Membrane Vesicles as Mediators of Microbe – Microbe and Microbe – Host Community Interactions
Caruana, J. C., & Walper, S. A. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2020.00432 · Cited by 267 · see citing works
A Comparison of Cellular Uptake Mechanisms, Delivery Efficacy, and Intracellular Fate between Liposomes and Extracellular Vesicles
Gandek, T. B., van der Koog, L., & Nagelkerke, A. (2023) · Advanced Healthcare Materials · doi:10.1002/adhm.202300319 · Cited by 242 · see citing works
Nanocarriers address intracellular barriers for efficient drug delivery, overcoming drug resistance, subcellular targeting and controlled release
Liu, J., Cabral, H., & Mi, P. (2024) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2024.115239 · Cited by 239 · see citing works
Cancer cells escape autophagy inhibition via NRF2-induced macropinocytosis
Su, H., Yang, F., Fu, R., Li, X., French, R. P., Mose, E. S., Pu, X., Trinh, B., Kumar, A., Liu, J., et al. (2021) · Cancer Cell · doi:10.1016/j.ccell.2021.02.016 · Cited by 215 · see citing works
Eat Prey, Live: Dictyostelium discoideum As a Model for Cell-Autonomous Defenses
Dunn, J. D., Bosmani, C., Barisch, C., Raykov, L., Lefrançois, L. H., Cardenal‐Muñoz, E., López-Jiménez, A. T., & Soldati, T. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2017.01906 · Cited by 186 · see citing works
A plasma membrane template for macropinocytic cups
Veltman, D. M., Williams, T. D., Bloomfield, G., Chen, B., Betzig, E., Insall, R. H., & Kay, R. R. (2016) · eLife · doi:10.7554/elife.20085 · Cited by 160 · see citing works
Self-citation
The origins and evolution of macropinocytosis
King, J., & Kay, R. R. (2018) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2018.0158 · Cited by 150 · see citing works
Self-citation
Extracellular Vesicle Transportation and Uptake by Recipient Cells: A Critical Process to Regulate Human Diseases
Kwok, Z. H., Wang, C., & Jin, Y. (2021) · Processes · doi:10.3390/pr9020273 · Cited by 157 · see citing works
New insights into the formation and the function of lamellipodia and ruffles in mesenchymal cell migration
Innocenti, M. (2018) · Cell Adhesion & Migration · doi:10.1080/19336918.2018.1448352 · Cited by 150 · see citing works
Drinking problems: mechanisms of macropinosome formation and maturation
Buckley, C. M. F., & King, J. (2017) · FEBS Journal · doi:10.1111/febs.14115 · Cited by 132 · see citing works
Nanocarriers transport across the gastrointestinal barriers: The contribution to oral bioavailability via blood circulation and lymphatic pathway
Wang, D., Jiang, Q., Dong, Z., Meng, T., Hu, F., Wang, J., & Yuan, H. (2023) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2023.115130 · Cited by 140 · see citing works
Macropinocytosis: Biology and mechanisms
Kay, R. R. (2021) · Cells and Development · doi:10.1016/j.cdev.2021.203713 · Cited by 113 · see citing works
Self-citation
Macropinocytosis, mTORC1 and cellular growth control
Yoshida, S., Pacitto, R., Inoki, K., & Swanson, J. (2018) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-017-2710-y · Cited by 114 · see citing works
Metabolic functions of macropinocytosis
Palm, W. (2018) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2018.0285 · Cited by 111 · see citing works
Wnt canonical pathway activates macropinocytosis and lysosomal degradation of extracellular proteins
Tejeda‐Muñoz, N., Albrecht, L. V., Bui, M. H., & Robertis, E. M. D. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1903506116 · Cited by 107 · see citing works
Revealing macropinocytosis using nanoparticles
Means, N., Elechalawar, C. K., Chen, W. R., Bhattacharya, R., & Mukherjee, P. (2021) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2021.100993 · Cited by 109 · see citing works
The macrophage-expressed gene ( mpeg ) 1 identifies a subpopulation of B cells in the adult zebrafish
Ferrero, G., Gomez, E., lyer, S., Rovira, M., Miserocchi, M., Langenau, D. M., Bertrand, J. Y., & Wittamer, V. (2020) · Journal of Leukocyte Biology · doi:10.1002/jlb.1a1119-223r · Cited by 102 · see citing works
Nanoparticle entry into cells; the cell biology weak link
Griffiths, G. W., Grüenberg, J., Marsh, M., Wohlmann, J., Jones, A. T., & Parton, R. G. (2022) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2022.114403 · Cited by 99 · see citing works
Septin Mutations in Human Cancers
Angelis, D., & Spiliotis, E. T. (2016) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2016.00122 · Cited by 92 · see citing works
Macropinocytosis: mechanisms and regulation
Salloum, G., Bresnick, A. R., & Backer, J. (2023) · Biochemical Journal · doi:10.1042/bcj20210584 · Cited by 90 · see citing works
Phagocytosis in cellular defense and nutrition: a food-centered approach to the evolution of macrophages
Hartenstein, V., & Martı́nez, P. (2019) · Cell and Tissue Research · doi:10.1007/s00441-019-03096-6 · Cited by 86 · see citing works
Macropinocytosis as a cell entry route for peptide-functionalized and bystander nanoparticles
Li, Y., & Pang, H. (2020) · Journal of Controlled Release · doi:10.1016/j.jconrel.2020.10.049 · Cited by 84 · see citing works
Macropinocytosis drives T cell growth by sustaining the activation of mTORC1
Charpentier, J. C., Chen, D., Lapinski, P. E., Turner, J. S., Grigorova, I., Swanson, J. A., & King, P. D. (2020) · Nature Communications · doi:10.1038/s41467-019-13997-3 · Cited by 83 · see citing works
Critical role for PI3-kinase in regulating the use of proteins as an amino acid source
Palm, W., Araki, J., King, B., Dematteo, R. G., & Thompson, C. B. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1712726114 · Cited by 79 · see citing works
A Diaphanous -related formin links Ras signaling directly to actin assembly in macropinocytosis and phagocytosis
Junemann, A., Filić, V., Winterhoff, M., Nordholz, B., Litschko, C., Schwellenbach, H., Stephan, T., Weber, I. T., & Faix, J. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1611024113 · Cited by 70 · see citing works
The breadth of macropinocytosis research
Swanson, J. A., & King, J. (2018) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2018.0146 · Cited by 66 · see citing works
Regulation of Ferroptosis by Amino Acid Metabolism in Cancer
Yang, J., Dai, X., Xu, H., Tang, Q., & Bi, F. (2022) · International Journal of Biological Sciences · doi:10.7150/ijbs.64982 · Cited by 69 · see citing works
Insights of Endocytosis Signaling in Health and Disease
Pathak, C., Vaidya, F. U., Waghela, B. N., Jaiswara, P. K., Gupta, V. K., Kumar, A., Rajendran, B. K., & Ranjan, K. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24032971 · Cited by 59 · see citing works
“In fact, release of growth factors from macrophages, such as colonystimulating factor-1 (CSF-1), induces macropinocytosis [34].”
Background
The physiological regulation of macropinocytosis during Dictyostelium growth and development
Williams, T. D., & Kay, R. R. (2018) · Journal of Cell Science · doi:10.1242/jcs.213736 · Cited by 58 · see citing works
Self-citation
Arf GAPs as Regulators of the Actin Cytoskeleton—An Update
Tanna, C. E., Goss, L. B., Ludwig, C., & Chen, P.-W. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20020442 · Cited by 61 · see citing works
Rewiring chaperone-mediated autophagy in cancer by a prion-like chemical inducer of proximity to counteract adaptive immune resistance
Yan, J., Liu, D., Wang, J., You, W., Yang, W., Yan, S., & He, W. (2023) · Drug Resistance Updates · doi:10.1016/j.drup.2023.101037 · Cited by 59 · see citing works
Differential ability of proinflammatory and anti-inflammatory macrophages to perform macropinocytosis
Redka, D. S., Gütschow, M., Grinstein, S., & Canton, J. (2018) · Molecular Biology of the Cell · doi:10.1091/mbc.e17-06-0419 · Cited by 58 · see citing works
The role of endolysosomal trafficking in anticancer drug resistance
Hussein, N. A., Malla, S., Pasternak, M. A., Terrero, D., Brown, N. G., Ashby, C. R., Assaraf, Y. G., Chen, Z., & Tiwari, A. K. (2021) · Drug Resistance Updates · doi:10.1016/j.drup.2021.100769 · Cited by 57 · see citing works
Fronts and waves of actin polymerization in a bistability-based mechanism of circular dorsal ruffles
Bernitt, E., Döbereiner, J., Gov, N. S., & Yochelis, A. (2017) · Nature Communications · doi:10.1038/ncomms15863 · Cited by 54 · see citing works
Morphodynamics of the Actin-Rich Cytoskeleton in Entamoeba histolytica
Manich, M., Hernández‐Cuevas, N. A., Ospina‐Villa, J. D., Syan, S., Marchat, L. A., Olivo‐Marín, J., & Guillén, N. (2018) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2018.00179 · Cited by 52 · see citing works
SLIT2/ROBO1-signaling inhibits macropinocytosis by opposing cortical cytoskeletal remodeling
Bhosle, V. K., Mukherjee, T., Huang, Y.-W., Patel, S., Pang, B. W., Liu, G., Glogauer, M., Wu, J. Y., Philpott, D. J., Grinstein, S., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-17651-1 · Cited by 56 · see citing works
The structural dynamics of macropinosome formation and PI3-kinase-mediated sealing revealed by lattice light sheet microscopy
Quinn, S. E., Huang, L., Kerkvliet, J. G., Swanson, J. A., Smith, S., Hoppe, A. D., Anderson, R. B., Thiex, N. W., & Scott, B. L. (2021) · Nature Communications · doi:10.1038/s41467-021-25187-1 · Cited by 50 · see citing works
From actin waves to mechanism and back: How theory aids biological understanding
Beta, C., Leah Edelstein-keshet, A., Gov, N. S., & Yochelis, A. (2023) · eLife · doi:10.7554/elife.87181 · Cited by 46 · see citing works
PFKFB3 inhibition reprograms malignant pleural mesothelioma to nutrient stress-induced macropinocytosis and ER stress as independent binary adaptive responses
Bhattacharya, S. S., Thirusangu, P., Jin, L., Roy, D., Jung, D., Xiao, Y., Staub, J. K., Roy, B., Molina, J. R., & Shridhar, V. (2019) · Cell Death and Disease · doi:10.1038/s41419-019-1916-3 · Cited by 50 · see citing works
Hijacking Endocytosis and Autophagy in Extracellular Vesicle Communication: Where the Inside Meets the Outside
Pedrioli, G., & Paganetti, P. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.595515 · Cited by 48 · see citing works
Macropinosomes as units of signal transduction
Swanson, J. A., & Yoshida, S. (2018) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2018.0157 · Cited by 47 · see citing works
From Pinocytosis to Methuosis—Fluid Consumption as a Risk Factor for Cell Death
Ritter, M., Bresgen, N., & Kerschbaum, H. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.651982 · Cited by 49 · see citing works
Noncationic Material Design for Nucleic Acid Delivery
Jiang, Z., & Thayumanavan, S. (2020) · Advanced Therapeutics · doi:10.1002/adtp.201900206 · Cited by 45 · see citing works
Ubiquitous macropinocytosis in anthozoans
Ganot, P., Tambutté, É., Caminiti-Segonds, N., Toullec, G., Allemand, D., & Tambutté, S. (2020) · eLife · doi:10.7554/elife.50022 · Cited by 44 · see citing works
Cell surface nucleolin interacts with and internalizes Bothrops asper Lys49 phospholipase A2 and mediates its toxic activity
Massimino, M. L., Simonato, M., Spolaore, B., Franchin, C., Arrigoni, G., Marin, O., Monturiol‐Gross, L., Fernández, J., Lomonte, B., & Tonello, F. (2018) · Scientific Reports · doi:10.1038/s41598-018-28846-4 · Cited by 44 · see citing works
Coordinated Ras and Rac Activity Shapes Macropinocytic Cups and Enables Phagocytosis of Geometrically Diverse Bacteria
Buckley, C. M. F., Pots, H., Guého, A., Vines, J. H., Munn, C. J., Phillips, B. A., Gilsbach, B. K., Traynor, D., Nikolaev, A., Soldati, T., et al. (2020) · Current Biology · doi:10.1016/j.cub.2020.05.049 · Cited by 45 · see citing works
Systematic interaction of plasma albumin with the efficacy of chemotherapeutic drugs
Yu, L., Hua, Z., Luo, X., Zhao, T., & Liu, Y. (2021) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2021.188655 · Cited by 43 · see citing works
The endocytic pathways of Dictyostelium discoideum
Vines, J. H., & King, J. (2019) · The International Journal of Developmental Biology · doi:10.1387/ijdb.190236jk · Cited by 41 · see citing works
Macropinocytosis and Cancer: From Tumor Stress to Signaling Pathways
Lambies, G., & Commisso, C. (2022) · Sub-cellular biochemistry/Subcellular biochemistry · doi:10.1007/978-3-030-94004-1_2 · Cited by 41 · see citing works
An acute decrease in plasma membrane tension induces macropinocytosis via PLD2 activation
Loh, J., Chuang, M., Lin, S., Joseph, J. G., Su, Y., Hsieh, T.-L., Chang, Y., Liu, A. P., & Liu, Y. (2019) · Journal of Cell Science · doi:10.1242/jcs.232579 · Cited by 40 · see citing works
Macropinocytosis: mechanism and targeted therapy in cancers.
Xiao, F., Li, J., Huang, K., Li, X., Xiong, Y., Wu, M., Wu, L., Kuang, W., Lv, S., Wu, L., et al. (2021) · PubMed Central · Cited by 38 · see citing works
CYRI-A limits invasive migration through macropinosome formation and integrin uptake regulation
Le, H. A., Yelland, T., Paul, N. R., Fort, L., Nikolaou, S., Ismail, S., & Machesky, L. M. (2021) · The Journal of Cell Biology · doi:10.1083/jcb.202012114 · Cited by 38 · see citing works
Survival strategies of cancer cells: the role of macropinocytosis in nutrient acquisition, metabolic reprogramming, and therapeutic targeting
Xu, G., Zhang, Q., Cheng, R., Qu, J., & Li, W. (2025) · Autophagy · doi:10.1080/15548627.2025.2452149 · Cited by 38 · see citing works
Intracellular Transport in Cancer Metabolic Reprogramming
Sneeggen, M., Guadagno, N. A., & Progida, C. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.597608 · Cited by 37 · see citing works
Extracellular vesicles biogenesis and uptake concepts: A comprehensive guide to studying host–pathogen communication
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Dorsal ruffles enhance activation of Akt by growth factors
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Authors: Bloomfield, G., & Kay, R. R.
Affiliations: MRC Laboratory of Molecular Biology (GB)
Corresponding author: Bloomfield, Gareth
ORCID: Bloomfield, Gareth
Kay, Robert R.
Venue: Journal of Cell Science
Publisher: The Company of Biologists
Published: 2016-07-15
Volume: 129
Issue: 14
Pages: 2697-2705
ISSN: 0021-9533 (ISSN-L)
1477-9137
DOI: 10.1242/jcs.176149
OpenAlex: W2467880345
Cited by: 193
References: 112
Citations by year: 2026: 6 · 2025: 10 · 2024: 16 · 2023: 17 · 2022: 20 · 2021: 31 · 2020: 28 · 2019: 28 · 2018: 20 · 2017: 12 · 2016: 4
FWCI: 2.30
Type: journal article
Language: en
Open access: closed
Licence: www.biologists.com/user-licence-1-1 (vor, 184 d)
Locations: Journal of Cell Science (publishedVersion)
PubMed (publishedVersion)
HighWire Press Open Archive (submittedVersion)
Funders: Medical Research Council (MC_U105115237)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
Physical Sciences › Materials Science › Biomaterials › Nanoparticle-Based Drug Delivery
Keywords: macropinocytosis, endocytosis, amoeboid movement, Ras signaling, viral entry, bacterial invasion, prion propagation, prion-like proteins, drug delivery, cell death, phagotrophy
MeSH terms: Animals, Communicable Diseases, Humans, Immunity, Pinocytosis, Prions, Cell Death, Macromolecular Substances

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