Cholera Toxin as a Probe for Membrane Biology
Abstract
:1. Introduction
2. CTxB as a Probe for Membrane Organization
3. CTxB as a Sensor and Inducer of Membrane Curvature
4. CTxB as a Reporter of Clathrin-Independent Endocytosis
5. CTxB as a Probe of Retrograde Trafficking Mechanisms
6. Alternative Membrane Glycoprotein Receptors Affecting CTx Biology
7. Take-Homes and Open Questions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- De, S.N. Enterotoxicity of bacteria-free culture-filtrate of Vibrio cholerae. Nature 1959, 183, 1533–1534. [Google Scholar] [CrossRef]
- Herrington, D.A.; Hall, R.H.; Losonsky, G.; Mekalanos, J.J.; Taylor, R.K.; Levine, M.M. Toxin, toxin-coregulated pili, and the toxR regulon are essential for Vibrio cholerae pathogenesis in humans. J. Exp. Med. 1988, 168, 1487–1492. [Google Scholar] [CrossRef]
- Bharati, K.; Ganguly, N.K. Cholera toxin: A paradigm of a multifunctional protein. Indian J. Med. Res. 2011, 133, 179–187. [Google Scholar]
- O’Neal, C.J.; Amaya, E.I.; Jobling, M.G.; Holmes, R.K.; Hol, W.G. Crystal structures of an intrinsically active cholera toxin mutant yield insight into the toxin activation mechanism. Biochemistry 2004, 43, 3772–3782. [Google Scholar] [CrossRef] [PubMed]
- Turnbull, W.B.; Precious, B.L.; Homans, S.W. Dissecting the cholera toxin-ganglioside GM1 interaction by isothermal titration calorimetry. J. Am. Chem. Soc. 2004, 126, 1047–1054. [Google Scholar] [CrossRef]
- Krishnan, P.; Singla, A.; Lee, C.A.; Weatherston, J.D.; Worstell, N.C.; Wu, H.J. Hetero-multivalent binding of cholera toxin subunit B with glycolipid mixtures. Colloids Surf. B Biointerfaces 2017, 160, 281–288. [Google Scholar] [CrossRef]
- Chiricozzi, E.; Mauri, L.; Ciampa, M.G.; Prinetti, A.; Sonnino, S. On the use of cholera toxin. Glycoconj. J. 2018, 35, 161–163. [Google Scholar] [CrossRef] [PubMed]
- Merritt, E.A.; Sarfaty, S.; van den Akker, F.; L’Hoir, C.; Martial, J.A.; Hol, W.G. Crystal structure of cholera toxin B-pentamer bound to receptor GM1 pentasaccharide. Protein Sci. 1994, 3, 166–175. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lencer, W.I. Retrograde transport of cholera toxin into the ER of host cells. Int. J. Med. Microbiol. 2004, 293, 491–494. [Google Scholar] [CrossRef]
- Luong, P.; Li, Q.; Chen, P.F.; Wrighton, P.J.; Chang, D.; Dwyer, S.; Bayer, M.T.; Snapper, S.B.; Hansen, S.H.; Thiagarajah, J.R.; et al. A quantitative single-cell assay for retrograde membrane traffic enables rapid detection of defects in cellular organization. Mol. Biol. Cell 2020, 31, 511–519. [Google Scholar] [CrossRef] [PubMed]
- Spooner, R.A.; Smith, D.C.; Easton, A.J.; Roberts, L.M.; Lord, J.M. Retrograde transport pathways utilised by viruses and protein toxins. Virol. J. 2006, 3, 26. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chinnapen, D.J.; Hsieh, W.T.; te Welscher, Y.M.; Saslowsky, D.E.; Kaoutzani, L.; Brandsma, E.; D’Auria, L.; Park, H.; Wagner, J.S.; Drake, K.R.; et al. Lipid sorting by ceramide structure from plasma membrane to ER for the cholera toxin receptor ganglioside GM1. Dev. Cell 2012, 23, 573–586. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Schmieder, S.S.; Tatituri, R.; Anderson, A.; Kelly, K.; Lencer, W.I. Structural basis for acyl chain control over glycosphingolipid sorting and vesicular trafficking. bioRxiv 2021. [Google Scholar] [CrossRef]
- Wernick, N.L.; Chinnapen, D.J.; Cho, J.A.; Lencer, W.I. Cholera toxin: An intracellular journey into the cytosol by way of the endoplasmic reticulum. Toxins 2010, 2, 310–325. [Google Scholar] [CrossRef] [Green Version]
- Lencer, W.I.; Tsai, B. The intracellular voyage of cholera toxin: Going retro. Trends Biochem. Sci. 2003, 28, 639–645. [Google Scholar] [CrossRef] [PubMed]
- Chaudhuri, A.; DasAdhikary, C.R. Possible role of blood-group secretory substances in the aetiology of cholera. Trans. R. Soc. Trop. Med. Hyg. 1978, 72, 664–665. [Google Scholar] [CrossRef]
- Harris, J.B.; LaRocque, R.C. Cholera and ABO blood group: Understanding an ancient association. Am. J. Trop. Med. Hyg. 2016, 95, 263–264. [Google Scholar] [CrossRef] [Green Version]
- Heggelund, J.E.; Haugen, E.; Lygren, B.; Mackenzie, A.; Holmner, A.; Vasile, F.; Reina, J.J.; Bernardi, A.; Krengel, U. Both El Tor and classical cholera toxin bind blood group determinants. Biochem. Biophys. Res. Commun. 2012, 418, 731–735. [Google Scholar] [CrossRef]
- Kuhlmann, F.M.; Santhanam, S.; Kumar, P.; Luo, Q.; Ciorba, M.A.; Fleckenstein, J.M. Blood Group O-Dependent Cellular Responses to Cholera Toxin: Parallel Clinical and Epidemiological Links to Severe Cholera. Am. J. Trop. Med. Hyg. 2016, 95, 440–443. [Google Scholar] [CrossRef] [Green Version]
- Mandal, P.K.; Branson, T.R.; Hayes, E.D.; Ross, J.F.; Gavin, J.A.; Daranas, A.H.; Turnbull, W.B. Towards a structural basis for the relationship between blood group and the severity of El Tor cholera. Angew. Chem. Int. Ed. Engl. 2012, 51, 5143–5146. [Google Scholar] [CrossRef]
- Sircar, B.K.; Dutta, P.; De, S.P.; Sikdar, S.N.; Deb, B.C.; Pal, S.C.; Mitra, S.S. ABO blood group distributions in diarrhoea cases including cholera in Calcutta. Ann. Hum. Biol. 1981, 8, 289–291. [Google Scholar] [CrossRef]
- Swerdlow, D.L.; Mintz, E.D.; Rodriguez, M.; Tejada, E.; Ocampo, C.; Espejo, L.; Barrett, T.J.; Petzelt, J.; Bean, N.H.; Seminario, L.; et al. Severe life-threatening cholera associated with blood group O in Peru: Implications for the Latin American epidemic. J. Infect. Dis. 1994, 170, 468–472. [Google Scholar] [CrossRef] [PubMed]
- Vasile, F.; Reina, J.J.; Potenza, D.; Heggelund, J.E.; Mackenzie, A.; Krengel, U.; Bernardi, A. Comprehensive analysis of blood group antigen binding to classical and El Tor cholera toxin B-pentamers by NMR. Glycobiology 2014, 24, 766–778. [Google Scholar] [CrossRef] [Green Version]
- Wands, A.M.; Fujita, A.; McCombs, J.E.; Cervin, J.; Dedic, B.; Rodriguez, A.C.; Nischan, N.; Bond, M.R.; Mettlen, M.; Trudgian, D.C.; et al. Fucosylation and protein glycosylation create functional receptors for cholera toxin. eLife 2015, 4, e09545. [Google Scholar] [CrossRef] [PubMed]
- Heggelund, J.E.; Burschowsky, D.; Bjornestad, V.A.; Hodnik, V.; Anderluh, G.; Krengel, U. High-resolution crystal structures elucidate the molecular basis of cholera blood group dependence. PLoS Pathog. 2016, 12, e1005567. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Heim, J.B.; Hodnik, V.; Heggelund, J.E.; Anderluh, G.; Krengel, U. Crystal structures of cholera toxin in complex with fucosylated receptors point to importance of secondary binding site. Sci. Rep. 2019, 9, 12243. [Google Scholar] [CrossRef] [Green Version]
- Cervin, J.; Wands, A.M.; Casselbrant, A.; Wu, H.; Krishnamurthy, S.; Cvjetkovic, A.; Estelius, J.; Dedic, B.; Sethi, A.; Wallom, K.L.; et al. GM1 ganglioside-independent intoxication by cholera toxin. PLoS Pathog. 2018, 14, e1006862. [Google Scholar] [CrossRef] [Green Version]
- Lingwood, D.; Simons, K. Lipid rafts as a membrane-organizing principle. Science 2010, 327, 46–50. [Google Scholar] [CrossRef] [Green Version]
- Sezgin, E.; Levental, I.; Mayor, S.; Eggeling, C. The mystery of membrane organization: Composition, regulation and roles of lipid rafts. Nat. Rev. Mol. Cell Biol. 2017, 18, 361–374. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Simons, K.; Toomre, D. Lipid rafts and signal transduction. Nat. Rev. Mol. Cell Biol. 2000, 1, 31–41. [Google Scholar] [CrossRef]
- Simons, K.; Sampaio, J.L. Membrane organization and lipid rafts. Cold Spring Harb. Perspect. Biol. 2011, 3, a004697. [Google Scholar] [CrossRef]
- Badizadegan, K.; Wolf, A.A.; Rodighiero, C.; Jobling, M.; Hirst, T.R.; Holmes, R.K.; Lencer, W.I. Floating cholera toxin into epithelial cells: Functional association with caveolae-like detergent-insoluble membrane microdomains. Int. J. Med. Microbiol. 2000, 290, 403–408. [Google Scholar] [CrossRef]
- Fujinaga, Y.; Wolf, A.A.; Rodighiero, C.; Wheeler, H.; Tsai, B.; Allen, L.; Jobling, M.G.; Rapoport, T.; Holmes, R.K.; Lencer, W.I. Gangliosides that associate with lipid rafts mediate transport of cholera and related toxins from the plasma membrane to endoplasmic reticulm. Mol. Biol. Cell 2003, 14, 4783–4793. [Google Scholar] [CrossRef] [PubMed]
- Lencer, W.I.; Saslowsky, D. Raft trafficking of AB5 subunit bacterial toxins. Biochim. Biophys. Acta 2005, 1746, 314–321. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chinnapen, D.J.; Chinnapen, H.; Saslowsky, D.; Lencer, W.I. Rafting with cholera toxin: Endocytosis and trafficking from plasma membrane to ER. FEMS Microbiol. Lett. 2007, 266, 129–137. [Google Scholar] [CrossRef] [Green Version]
- Day, C.A.; Kenworthy, A.K. Functions of cholera toxin B-subunit as a raft cross-linker. Essays Biochem. 2015, 57, 135–145. [Google Scholar] [PubMed] [Green Version]
- Raghunathan, K.; Kenworthy, A.K. Dynamic pattern generation in cell membranes: Current insights into membrane organization. Biochim. Biophys. Acta Biomembr. 2018, 1860, 2018–2031. [Google Scholar] [CrossRef]
- Levental, I.; Levental, K.R.; Heberle, F.A. Lipid rafts: Controversies resolved, mysteries remain. Trends Cell Biol. 2020, 30, 341–353. [Google Scholar] [CrossRef] [PubMed]
- Klotzsch, E.; Schutz, G.J. A critical survey of methods to detect plasma membrane rafts. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2013, 368, 20120033. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sevcsik, E.; Schutz, G.J. With or without rafts? Alternative views on cell membranes. Bioessays 2016, 38, 129–139. [Google Scholar] [CrossRef] [PubMed]
- Lu, S.M.; Fairn, G.D. Mesoscale organization of domains in the plasma membrane—Beyond the lipid raft. Crit. Rev. Biochem. Mol. Biol. 2018, 53, 192–207. [Google Scholar] [CrossRef] [PubMed]
- Wesolowska, O.; Michalak, K.; Maniewska, J.; Hendrich, A.B. Giant unilamellar vesicles—A perfect tool to visualize phase separation and lipid rafts in model systems. Acta Biochim. Pol. 2009, 56, 33–39. [Google Scholar] [CrossRef] [Green Version]
- Sezgin, E.; Kaiser, H.J.; Baumgart, T.; Schwille, P.; Simons, K.; Levental, I. Elucidating membrane structure and protein behavior using giant plasma membrane vesicles. Nat. Protoc. 2012, 7, 1042–1051. [Google Scholar] [CrossRef]
- Bacia, K.; Schwille, P.; Kurzchalia, T. Sterol structure determines the separation of phases and the curvature of the liquid-ordered phase in model membranes. Proc. Natl. Acad. Sci. USA 2005, 102, 3272–3277. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hammond, A.T.; Heberle, F.A.; Baumgart, T.; Holowka, D.; Baird, B.; Feigenson, G.W. Crosslinking a lipid raft component triggers liquid ordered-liquid disordered phase separation in model plasma membranes. Proc. Natl. Acad. Sci. USA 2005, 102, 6320–6325. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lingwood, D.; Ries, J.; Schwille, P.; Simons, K. Plasma membranes are poised for activation of raft phase coalescence at physiological temperature. Proc. Natl. Acad. Sci. USA 2008, 105, 10005–10010. [Google Scholar] [CrossRef] [Green Version]
- Sezgin, E.; Levental, I.; Grzybek, M.; Schwarzmann, G.; Mueller, V.; Honigmann, A.; Belov, V.N.; Eggeling, C.; Coskun, U.; Simons, K.; et al. Partitioning, diffusion, and ligand binding of raft lipid analogs in model and cellular plasma membranes. Biochim. Biophys. Acta 2012, 1818, 1777–1784. [Google Scholar] [CrossRef] [Green Version]
- Sengupta, P.; Baird, B.; Holowka, D. Lipid rafts, fluid/fluid phase separation, and their relevance to plasma membrane structure and function. Semin. Cell Dev. Biol. 2007, 18, 583–590. [Google Scholar] [CrossRef] [Green Version]
- Johnson, S.A.; Stinson, B.M.; Go, M.S.; Carmona, L.M.; Reminick, J.I.; Fang, X.; Baumgart, T. Temperature-dependent phase behavior and protein partitioning in giant plasma membrane vesicles. Biochim. Biophys. Acta 2010, 1798, 1427–1435. [Google Scholar] [CrossRef] [Green Version]
- Kaiser, H.J.; Lingwood, D.; Levental, I.; Sampaio, J.L.; Kalvodova, L.; Rajendran, L.; Simons, K. Order of lipid phases in model and plasma membranes. Proc. Natl. Acad. Sci. USA 2009, 106, 16645–16650. [Google Scholar] [CrossRef] [Green Version]
- Levental, I.; Lingwood, D.; Grzybek, M.; Coskun, U.; Simons, K. Palmitoylation regulates raft affinity for the majority of integral raft proteins. Proc. Natl. Acad. Sci. USA 2010, 107, 22050–22054. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Levental, I.; Byfield, F.J.; Chowdhury, P.; Gai, F.; Baumgart, T.; Janmey, P.A. Cholesterol-dependent phase separation in cell-derived giant plasma-membrane vesicles. Biochem. J. 2009, 424, 163–167. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kahya, N.; Scherfeld, D.; Bacia, K.; Poolman, B.; Schwille, P. Probing lipid mobility of raft-exhibiting model membranes by fluorescence correlation spectroscopy. J. Biol. Chem. 2003, 278, 28109–28115. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Baumgart, T.; Hammond, A.T.; Sengupta, P.; Hess, S.T.; Holowka, D.A.; Baird, B.A.; Webb, W.W. Large-scale fluid/fluid phase separation of proteins and lipids in giant plasma membrane vesicles. Proc. Natl. Acad. Sci. USA 2007, 104, 3165–3170. [Google Scholar] [CrossRef] [Green Version]
- Raghunathan, K.; Wong, T.H.; Chinnapen, D.J.; Lencer, W.I.; Jobling, M.G.; Kenworthy, A.K. Glycolipid crosslinking is required for cholera toxin to partition into and stabilize ordered domains. Biophys. J. 2016, 111, 2547–2550. [Google Scholar] [CrossRef] [Green Version]
- Arumugam, S.; Schmieder, S.; Pezeshkian, W.; Becken, U.; Wunder, C.; Chinnapen, D.; Ipsen, J.H.; Kenworthy, A.K.; Lencer, W.; Mayor, S.; et al. Ceramide structure dictates glycosphingolipid nanodomain assembly and function. Nat. Commun. 2021, 12, 3675. [Google Scholar] [CrossRef]
- Schumann, J.; Leichtle, A.; Thiery, J.; Fuhrmann, H. Fatty acid and peptide profiles in plasma membrane and membrane rafts of PUFA supplemented RAW264.7 macrophages. PLoS ONE 2011, 6, e24066. [Google Scholar] [CrossRef] [Green Version]
- Fujita, A.; Cheng, J.; Hirakawa, M.; Furukawa, K.; Kusunoki, S.; Fujimoto, T. Gangliosides GM1 and GM3 in the living cell membrane form clusters susceptible to cholesterol depletion and chilling. Mol. Biol. Cell 2007, 18, 2112–2122. [Google Scholar] [CrossRef] [Green Version]
- Fujita, A.; Cheng, J.; Fujimoto, T. Segregation of GM1 and GM3 clusters in the cell membrane depends on the intact actin cytoskeleton. Biochim. Biophys. Acta 2009, 1791, 388–396. [Google Scholar] [CrossRef]
- Sarmento, M.J.; Ricardo, J.C.; Amaro, M.; Sachl, R. Organization of gangliosides into membrane nanodomains. FEBS Lett. 2020, 594, 3668–3697. [Google Scholar] [CrossRef]
- Raghupathy, R.; Anilkumar, A.A.; Polley, A.; Singh, P.P.; Yadav, M.; Johnson, C.; Suryawanshi, S.; Saikam, V.; Sawant, S.D.; Panda, A.; et al. Transbilayer lipid interactions mediate nanoclustering of lipid-anchored proteins. Cell 2015, 161, 581–594. [Google Scholar] [CrossRef] [Green Version]
- Badizadegan, K.; Wheeler, H.E.; Fujinaga, Y.; Lencer, W.I. Trafficking of cholera toxin-ganglioside GM1 complex into Golgi and induction of toxicity depend on actin cytoskeleton. Am. J. Physiol. Cell Physiol. 2004, 287, C1453–C1462. [Google Scholar] [CrossRef] [PubMed]
- McMahon, H.T.; Boucrot, E. Membrane curvature at a glance. J. Cell Sci. 2015, 128, 1065–1070. [Google Scholar] [CrossRef] [Green Version]
- Zimmerberg, J.; Kozlov, M.M. How proteins produce cellular membrane curvature. Nat. Rev. Mol. Cell Biol. 2006, 7, 9–19. [Google Scholar] [CrossRef]
- Stachowiak, J.C.; Brodsky, F.M.; Miller, E.A. A cost-benefit analysis of the physical mechanisms of membrane curvature. Nat. Cell Biol. 2013, 15, 1019–1027. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Baumgart, T.; Capraro, B.R.; Zhu, C.; Das, S.L. Thermodynamics and mechanics of membrane curvature generation and sensing by proteins and lipids. Annu. Rev. Phys. Chem. 2011, 62, 483–506. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Shi, Z.; Baumgart, T. Membrane tension and peripheral protein density mediate membrane shape transitions. Nat. Commun. 2015, 6, 5974. [Google Scholar] [CrossRef] [PubMed]
- Ewers, H.; Römer, W.; Smith, A.E.; Bacia, K.; Dmitrieff, S.; Chai, W.; Mancini, R.; Kartenbeck, J.; Chambon, V.; Berland, L.; et al. GM1 structure determines SV40-induced membrane invagination and infection. Nat. Cell Biol. 2010, 12, 11–18. [Google Scholar] [CrossRef] [PubMed]
- Kabbani, A.M.; Kelly, C.V. Nanoscale membrane budding induced by CTxB and detected via polarized localization microscopy. Biophys. J. 2017, 113, 1795–1806. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hsieh, W.T.; Hsu, C.J.; Capraro, B.R.; Wu, T.; Chen, C.M.; Yang, S.; Baumgart, T. Curvature sorting of peripheral proteins on solid-supported wavy membranes. Langmuir 2012, 28, 12838–12843. [Google Scholar] [CrossRef] [Green Version]
- Groza, R.; Ewers, H. Membrane deformation by the cholera toxin beta subunit requires more than one binding site. Proc. Natl. Acad. Sci. USA 2020, 117, 17467–17469. [Google Scholar] [CrossRef]
- Pezeshkian, W.; Nabo, L.J.; Ipsen, J.H. Cholera toxin B subunit induces local curvature on lipid bilayers. FEBS Open Bio 2017, 7, 1638–1645. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tian, A.; Baumgart, T. Sorting of lipids and proteins in membrane curvature gradients. Biophys. J. 2009, 96, 2676–2688. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sens, P.; Johannes, L.; Bassereau, P. Biophysical approaches to protein-induced membrane deformations in trafficking. Curr. Opin Cell Biol. 2008, 20, 476–482. [Google Scholar] [CrossRef] [PubMed]
- Römer, W.; Berland, L.; Chambon, V.; Gaus, K.; Windschiegl, B.; Tenza, D.; Aly, M.R.; Fraisier, V.; Florent, J.C.; Perrais, D.; et al. Shiga toxin induces tubular membrane invaginations for its uptake into cells. Nature 2007, 450, 670–675. [Google Scholar] [CrossRef]
- Pezeshkian, W.; Hansen, A.G.; Johannes, L.; Khandelia, H.; Shillcock, J.C.; Kumar, P.B.; Ipsen, J.H. Membrane invagination induced by Shiga toxin B-subunit: From molecular structure to tube formation. Soft Matter 2016, 12, 5164–5171. [Google Scholar] [CrossRef] [Green Version]
- Johannes, L. Shiga toxin-a model for glycolipid-dependent and lectin-driven endocytosis. Toxins 2017, 9, 340. [Google Scholar] [CrossRef]
- Watkins, E.B.; Majewski, J.; Chi, E.Y.; Gao, H.; Florent, J.C.; Johannes, L. Shiga toxin induces lipid compression: A mechanism for generating membrane curvature. Nano Lett. 2019, 19, 7365–7369. [Google Scholar] [CrossRef]
- Kabbani, A.M.; Raghunathan, K.; Lencer, W.I.; Kenworthy, A.K.; Kelly, C.V. Structured clustering of the glycosphingolipid GM1 is required for membrane curvature induced by cholera toxin. Proc. Natl. Acad. Sci. USA 2020, 117, 14978–14986. [Google Scholar] [CrossRef] [PubMed]
- Kabbani, A.M.; Kelly, C.V. The detection of nanoscale membrane bending with polarized localization microscopy. Biophys. J. 2017, 113, 1782–1794. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sridhar, A.; Kumar, A.; Dasmahapatra, A.K. Multi-scale molecular dynamics study of cholera pentamer binding to a GM1-phospholipid membrane. J. Mol. Graph. Model. 2016, 68, 236–251. [Google Scholar] [CrossRef] [PubMed]
- Basu, I.; Mukhopadhyay, C. Insights into binding of cholera toxin to GM1 containing membrane. Langmuir 2014, 30, 15244–15252. [Google Scholar] [CrossRef]
- Rissanen, S.; Grzybek, M.; Orlowski, A.; Rog, T.; Cramariuc, O.; Levental, I.; Eggeling, C.; Sezgin, E.; Vattulainen, I. Phase partitioning of GM1 and its Bodipy-labeled analog determine their different binding to cholera toxin. Front. Physiol. 2017, 8, 252. [Google Scholar] [CrossRef] [Green Version]
- Humphrey, W.; Dalke, A.; Schulten, K. VMD: Visual molecular dynamics. J. Mol. Graph. 1996, 14, 33–38. [Google Scholar] [CrossRef]
- Merritt, E.A.; Sarfaty, S.; Jobling, M.G.; Chang, T.; Holmes, R.K.; Hirst, T.R.; Hol, W.G. Structural studies of receptor binding by cholera toxin mutants. Protein Sci. 1997, 6, 1516–1528. [Google Scholar] [CrossRef] [Green Version]
- Kuzmin, P.I.; Akimov, S.A.; Chizmadzhev, Y.A.; Zimmerberg, J.; Cohen, F.S. Line tension and interaction energies of membrane rafts calculated from lipid splay and tilt. Biophys. J. 2005, 88, 1120–1133. [Google Scholar] [CrossRef] [Green Version]
- Rozycki, B.; Lipowsky, R. Spontaneous curvature of bilayer membranes from molecular simulations: Asymmetric lipid densities and asymmetric adsorption. J. Chem. Phys. 2015, 142, 054101. [Google Scholar] [CrossRef]
- Yang, S.T.; Kiessling, V.; Tamm, L.K. Line tension at lipid phase boundaries as driving force for HIV fusion peptide-mediated fusion. Nat. Commun. 2016, 7, 11401. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Vind-Kezunovic, D.; Nielsen, C.H.; Wojewodzka, U.; Gniadecki, R. Line tension at lipid phase boundaries regulates formation of membrane vesicles in living cells. Biochim. Biophys. Acta 2008, 1778, 2480–2486. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Woodward, X.; Kelly, C.V. Coexisting lipid phases alter lipid dynamics and sort on nanoscale membrane curvature. bioRxiv 2020. [Google Scholar] [CrossRef]
- Stachowiak, J.C.; Hayden, C.C.; Sasaki, D.Y. Steric confinement of proteins on lipid membranes can drive curvature and tubulation. Proc. Natl. Acad. Sci. USA 2010, 107, 7781–7786. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cohen, A.E.; Shi, Z. Do Cell Membranes Flow Like Honey or Jiggle Like Jello? Bioessays 2020, 42, e1900142. [Google Scholar] [CrossRef] [PubMed]
- Reynwar, B.J.; Illya, G.; Harmandaris, V.A.; Muller, M.M.; Kremer, K.; Deserno, M. Aggregation and vesiculation of membrane proteins by curvature-mediated interactions. Nature 2007, 447, 461–464. [Google Scholar] [CrossRef] [PubMed]
- Ryu, Y.S.; Lee, I.H.; Suh, J.H.; Park, S.C.; Oh, S.; Jordan, L.R.; Wittenberg, N.J.; Oh, S.H.; Jeon, N.L.; Lee, B.; et al. Reconstituting ring-rafts in bud-mimicking topography of model membranes. Nat. Commun. 2014, 5, 4507. [Google Scholar] [CrossRef]
- Simunovic, M.; Voth, G.A. Membrane tension controls the assembly of curvature-generating proteins. Nat. Commun. 2015, 6, 7219. [Google Scholar] [CrossRef]
- Muller, M.M.; Deserno, M.; Guven, J. Interface-mediated interactions between particles: A geometrical approach. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 2005, 72, 061407. [Google Scholar] [CrossRef] [Green Version]
- Bradley, R.P.; Radhakrishnan, R. Curvature-undulation coupling as a basis for curvature sensing and generation in bilayer membranes. Proc. Natl. Acad. Sci. USA 2016, 113, E5117–E5124. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Johannes, L.; Pezeshkian, W.; Ipsen, J.H.; Shillcock, J.C. Clustering on membranes: Fluctuations and more. Trends Cell Biol. 2018, 28, 405–415. [Google Scholar] [CrossRef]
- Simunovic, M.; Evergren, E.; Golushko, I.; Prevost, C.; Renard, H.F.; Johannes, L.; McMahon, H.T.; Lorman, V.; Voth, G.A.; Bassereau, P. How curvature-generating proteins build scaffolds on membrane nanotubes. Proc. Natl. Acad. Sci. USA 2016, 113, 11226–11231. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sigismund, S.; Lanzetti, L.; Scita, G.; Di Fiore, P.P. Endocytosis in the context-dependent regulation of individual and collective cell properties. Nat. Rev. Mol. Cell Biol. 2021. [Google Scholar] [CrossRef]
- Antonescu, C.N.; McGraw, T.E.; Klip, A. Reciprocal regulation of endocytosis and metabolism. Cold Spring Harb. Perspect. Biol. 2014, 6, a016964. [Google Scholar] [CrossRef] [PubMed]
- Di Fiore, P.P.; von Zastrow, M. Endocytosis, signaling, and beyond. Cold Spring Harb. Perspect. Biol. 2014, 6, a016865. [Google Scholar] [CrossRef] [Green Version]
- Barbieri, E.; Di Fiore, P.P.; Sigismund, S. Endocytic control of signaling at the plasma membrane. Curr. Opin Cell Biol. 2016, 39, 21–27. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cossart, P.; Helenius, A. Endocytosis of viruses and bacteria. Cold Spring Harb. Perspect. Biol. 2014, 6, a016972. [Google Scholar] [CrossRef] [Green Version]
- Bonazzi, M.; Cossart, P. Bacterial entry into cells: A role for the endocytic machinery. FEBS Lett. 2006, 580, 2962–2967. [Google Scholar] [CrossRef] [Green Version]
- Barrow, E.; Nicola, A.V.; Liu, J. Multiscale perspectives of virus entry via endocytosis. Virol. J. 2013, 10, 177. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Veiga, E.; Cossart, P. The role of clathrin-dependent endocytosis in bacterial internalization. Trends Cell Biol. 2006, 16, 499–504. [Google Scholar] [CrossRef] [PubMed]
- Thottacherry, J.J.; Sathe, M.; Prabhakara, C.; Mayor, S. Spoiled for choice: Diverse endocytic pathways function at the cell surface. Annu. Rev. Cell Dev. Biol. 2019, 35, 55–84. [Google Scholar] [CrossRef] [PubMed]
- Doherty, G.J.; McMahon, H.T. Mechanisms of endocytosis. Annu. Rev. Biochem. 2009, 78, 857–902. [Google Scholar] [CrossRef] [Green Version]
- Conner, S.D.; Schmid, S.L. Regulated portals of entry into the cell. Nature 2003, 422, 37–44. [Google Scholar] [CrossRef] [PubMed]
- Kaksonen, M.; Roux, A. Mechanisms of clathrin-mediated endocytosis. Nat. Rev. Mol. Cell Biol. 2018, 19, 313–326. [Google Scholar] [CrossRef]
- McMahon, H.T.; Boucrot, E. Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nat. Rev. Mol. Cell Biol. 2011, 12, 517–533. [Google Scholar] [CrossRef] [PubMed]
- Mettlen, M.; Chen, P.H.; Srinivasan, S.; Danuser, G.; Schmid, S.L. Regulation of clathrin-mediated endocytosis. Annu. Rev. Biochem. 2018, 87, 871–896. [Google Scholar] [CrossRef]
- Johannes, L.; Parton, R.G.; Bassereau, P.; Mayor, S. Building endocytic pits without clathrin. Nat. Rev. Mol. Cell Biol. 2015, 16, 311–321. [Google Scholar] [CrossRef]
- Shafaq-Zadah, M.; Dransart, E.; Johannes, L. Clathrin-independent endocytosis, retrograde trafficking, and cell polarity. Curr. Opin Cell Biol. 2020, 65, 112–121. [Google Scholar] [CrossRef]
- Renard, H.F.; Boucrot, E. Unconventional endocytic mechanisms. Curr. Opin Cell Biol. 2021, 71, 120–129. [Google Scholar] [CrossRef]
- Sandvig, K.; Kavaliauskiene, S.; Skotland, T. Clathrin-independent endocytosis: An increasing degree of complexity. Histochem. Cell Biol. 2018, 150, 107–118. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ferreira, A.P.A.; Boucrot, E. Mechanisms of carrier formation during clathrin-independent endocytosis. Trends Cell Biol. 2018, 28, 188–200. [Google Scholar] [CrossRef]
- Hemalatha, A.; Mayor, S. Recent advances in clathrin-independent endocytosis. F1000Research 2019, 8, 138. [Google Scholar] [CrossRef]
- Howes, M.T.; Mayor, S.; Parton, R.G. Molecules, mechanisms, and cellular roles of clathrin-independent endocytosis. Curr. Opin. Cell Biol. 2010, 22, 519–527. [Google Scholar] [CrossRef] [PubMed]
- Mayor, S.; Parton, R.G.; Donaldson, J.G. Clathrin-independent pathways of endocytosis. Cold Spring Harb. Perspect. Biol. 2014, 6, a016758. [Google Scholar] [CrossRef] [Green Version]
- Mayor, S.; Pagano, R.E. Pathways of clathrin-independent endocytosis. Nat. Rev. Mol. Cell Biol. 2007, 8, 603–612. [Google Scholar] [CrossRef] [PubMed]
- Torgersen, M.L.; Skretting, G.; van Deurs, B.; Sandvig, K. Internalization of cholera toxin by different endocytic mechanisms. J. Cell Sci. 2001, 114, 3737–3747. [Google Scholar] [CrossRef] [PubMed]
- Massol, R.H.; Larsen, J.E.; Fujinaga, Y.; Lencer, W.I.; Kirchhausen, T. Cholera toxin toxicity does not require functional Arf6- and dynamin-dependent endocytic pathways. Mol. Biol. Cell 2004, 15, 3631–3641. [Google Scholar] [CrossRef] [Green Version]
- Kirkham, M.; Fujita, A.; Chadda, R.; Nixon, S.J.; Kurzchalia, T.V.; Sharma, D.K.; Pagano, R.E.; Hancock, J.F.; Mayor, S.; Parton, R.G. Ultrastructural identification of uncoated caveolin-independent early endocytic vehicles. J. Cell Biol. 2005, 168, 465–476. [Google Scholar] [CrossRef] [PubMed]
- Pelkmans, L.; Kartenbeck, J.; Helenius, A. Caveolar endocytosis of simian virus 40 reveals a new two-step vesicular-transport pathway to the ER. Nat. Cell Biol. 2001, 3, 473–483. [Google Scholar] [CrossRef] [PubMed]
- Pelkmans, L.; Zerial, M. Kinase-regulated quantal assemblies and kiss-and-run recycling of caveolae. Nature 2005, 436, 128–133. [Google Scholar] [CrossRef]
- Pelkmans, L.; Burli, T.; Zerial, M.; Helenius, A. Caveolin-stabilized membrane domains as multifunctional transport and sorting devices in endocytic membrane traffic. Cell 2004, 118, 767–780. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lundmark, R.; Doherty, G.J.; Howes, M.T.; Cortese, K.; Vallis, Y.; Parton, R.G.; McMahon, H.T. The GTPase-activating protein GRAF1 regulates the CLIC/GEEC endocytic pathway. Curr. Biol. 2008, 18, 1802–1808. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Thottacherry, J.J.; Kosmalska, A.J.; Kumar, A.; Vishen, A.S.; Elosegui-Artola, A.; Pradhan, S.; Sharma, S.; Singh, P.P.; Guadamillas, M.C.; Chaudhary, N.; et al. Mechanochemical feedback control of dynamin independent endocytosis modulates membrane tension in adherent cells. Nat. Commun. 2018, 9, 4217. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Howes, M.T.; Kirkham, M.; Riches, J.; Cortese, K.; Walser, P.J.; Simpson, F.; Hill, M.M.; Jones, A.; Lundmark, R.; Lindsay, M.R.; et al. Clathrin-independent carriers form a high capacity endocytic sorting system at the leading edge of migrating cells. J. Cell Biol. 2010, 190, 675–691. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kalia, M.; Kumari, S.; Chadda, R.; Hill, M.M.; Parton, R.G.; Mayor, S. Arf6-independent GPI-anchored protein-enriched early endosomal compartments fuse with sorting endosomes via a Rab5/phosphatidylinositol-3’-kinase-dependent machinery. Mol. Biol. Cell 2006, 17, 3689–3704. [Google Scholar] [CrossRef]
- Nonnenmacher, M.; Weber, T. Adeno-associated virus 2 infection requires endocytosis through the CLIC/GEEC pathway. Cell Host Microbe 2011, 10, 563–576. [Google Scholar] [CrossRef] [Green Version]
- Radhakrishna, H.; Donaldson, J.G. ADP-ribosylation factor 6 regulates a novel plasma membrane recycling pathway. J. Cell Biol. 1997, 139, 49–61. [Google Scholar] [CrossRef] [Green Version]
- Naslavsky, N.; Weigert, R.; Donaldson, J.G. Characterization of a nonclathrin endocytic pathway: Membrane cargo and lipid requirements. Mol. Biol. Cell 2004, 15, 3542–3552. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Renard, H.F.; Simunovic, M.; Lemiere, J.; Boucrot, E.; Garcia-Castillo, M.D.; Arumugam, S.; Chambon, V.; Lamaze, C.; Wunder, C.; Kenworthy, A.K.; et al. Endophilin-A2 functions in membrane scission in clathrin-independent endocytosis. Nature 2015, 517, 493–496. [Google Scholar] [CrossRef]
- Boucrot, E.; Ferreira, A.P.; Almeida-Souza, L.; Debard, S.; Vallis, Y.; Howard, G.; Bertot, L.; Sauvonnet, N.; McMahon, H.T. Endophilin marks and controls a clathrin-independent endocytic pathway. Nature 2015, 517, 460–465. [Google Scholar] [CrossRef] [PubMed]
- Casamento, A.; Boucrot, E. Molecular mechanism of Fast Endophilin-Mediated Endocytosis. Biochem. J. 2020, 477, 2327–2345. [Google Scholar] [CrossRef] [PubMed]
- Watanabe, S.; Boucrot, E. Fast and ultrafast endocytosis. Curr. Opin. Cell Biol. 2017, 47, 64–71. [Google Scholar] [CrossRef] [Green Version]
- Simunovic, M.; Manneville, J.B.; Renard, H.F.; Evergren, E.; Raghunathan, K.; Bhatia, D.; Kenworthy, A.K.; Voth, G.A.; Prost, J.; McMahon, H.T.; et al. Friction mediates scission of tubular membranes scaffolded by BAR proteins. Cell 2017, 170, 172.e11–184.e11. [Google Scholar] [CrossRef] [Green Version]
- Day, C.A.; Baetz, N.W.; Copeland, C.A.; Kraft, L.J.; Han, B.; Tiwari, A.; Drake, K.R.; De Luca, H.; Chinnapen, D.J.; Davidson, M.W.; et al. Microtubule motors power plasma membrane tubulation in clathrin-independent endocytosis. Traffic 2015, 16, 572–590. [Google Scholar] [CrossRef]
- Ferreira, A.P.A.; Casamento, A.; Carrillo Roas, S.; Halff, E.F.; Panambalana, J.; Subramaniam, S.; Schutzenhofer, K.; Chan Wah Hak, L.; McGourty, K.; Thalassinos, K.; et al. Cdk5 and GSK3beta inhibit fast endophilin-mediated endocytosis. Nat. Commun. 2021, 12, 2424. [Google Scholar] [CrossRef] [PubMed]
- Mercier, V.; Laporte, M.H.; Destaing, O.; Blot, B.; Blouin, C.M.; Pernet-Gallay, K.; Chatellard, C.; Saoudi, Y.; Albiges-Rizo, C.; Lamaze, C.; et al. ALG-2 interacting protein-X (Alix) is essential for clathrin-independent endocytosis and signaling. Sci. Rep. 2016, 6, 26986. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wolf, A.A.; Jobling, M.G.; Saslowsky, D.E.; Kern, E.; Drake, K.R.; Kenworthy, A.K.; Holmes, R.K.; Lencer, W.I. Attenuated endocytosis and toxicity of a mutant cholera toxin with decreased ability to cluster GM1. Infect. Immun. 2008, 76, 1476–1484. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jobling, M.G.; Yang, Z.; Kam, W.R.; Lencer, W.I.; Holmes, R.K. A single native ganglioside GM1-binding site is sufficient for cholera toxin to bind to cells and complete the intoxication pathway. mBio 2012, 3, e00401-12. [Google Scholar] [CrossRef] [Green Version]
- Johannes, L.; Wunder, C.; Shafaq-Zadah, M. Glycolipids and lectins in endocytic uptake pocesses. J. Mol. Biol. 2016, 428, 4792–4818. [Google Scholar] [CrossRef]
- Ebrahimkutty, M.P.; Galic, M. Receptor-free signaling at curved cellular membranes. Bioessays 2019, 41, e1900068. [Google Scholar] [CrossRef] [Green Version]
- Galic, M.; Begemann, I.; Viplav, A.; Matis, M. Force-control at cellular membranes. Bioarchitecture 2014, 4, 164–168. [Google Scholar]
- Klokk, T.I.; Kavaliauskiene, S.; Sandvig, K. Cross-linking of glycosphingolipids at the plasma membrane: Consequences for intracellular signaling and traffic. Cell Mol. Life Sci. 2016, 73, 1301–1316. [Google Scholar] [CrossRef]
- Utskarpen, A.; Massol, R.; van Deurs, B.; Lauvrak, S.U.; Kirchhausen, T.; Sandvig, K. Shiga toxin increases formation of clathrin-coated pits through Syk kinase. PLoS ONE 2010, 5, e10944. [Google Scholar] [CrossRef] [Green Version]
- Hehnly, H.; Sheff, D.; Stamnes, M. Shiga toxin facilitates its retrograde transport by modifying microtubule dynamics. Mol. Biol. Cell 2006, 17, 4379–4389. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Johannes, L.; Popoff, V. Tracing the retrograde route in protein trafficking. Cell 2008, 135, 1175–1187. [Google Scholar] [CrossRef] [Green Version]
- Cho, J.A.; Chinnapen, D.J.; Aamar, E.; Te Welscher, Y.M.; Lencer, W.I.; Massol, R. Insights on the trafficking and retro-translocation of glycosphingolipid-binding bacterial toxins. Front. Cell. Infect. Microbiol. 2012, 2, 51. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zuverink, M.; Barbieri, J.T. Protein toxins that utilize gangliosides as host receptors. Prog. Mol. Biol. Transl. Sci. 2018, 156, 325–354. [Google Scholar]
- Sandvig, K.; Garred, O.; Prydz, K.; Kozlov, J.V.; Hansen, S.H.; van Deurs, B. Retrograde transport of endocytosed Shiga toxin to the endoplasmic reticulum. Nature 1992, 358, 510–512. [Google Scholar] [CrossRef] [PubMed]
- Johannes, L.; Tenza, D.; Antony, C.; Goud, B. Retrograde transport of KDEL-bearing B-fragment of Shiga toxin. J. Biol. Chem. 1997, 272, 19554–19561. [Google Scholar] [CrossRef] [Green Version]
- Simpson, M.S.; Lencer, W.I.; Luong, P. A quantitative single-cell flow cytometry assay for retrograde membrane trafficking using engineered cholera toxin. Bio-Protocol 2020, 10, e3707. [Google Scholar] [CrossRef]
- Saslowsky, D.E.; te Welscher, Y.M.; Chinnapen, D.J.; Wagner, J.S.; Wan, J.; Kern, E.; Lencer, W.I. Ganglioside GM1-mediated transcytosis of cholera toxin bypasses the retrograde pathway and depends on the structure of the ceramide domain. J. Biol. Chem. 2013, 288, 25804–25809. [Google Scholar] [CrossRef] [Green Version]
- Maxfield, F.R.; McGraw, T.E. Endocytic recycling. Nat. Rev. Mol. Cell Biol. 2004, 5, 121–132. [Google Scholar] [CrossRef] [PubMed]
- Sandvig, K.; Ryd, M.; Garred, O.; Schweda, E.; Holm, P.K.; van Deurs, B. Retrograde transport from the Golgi complex to the ER of both Shiga toxin and the nontoxic Shiga B-fragment is regulated by butyric acid and cAMP. J. Cell Biol. 1994, 126, 53–64. [Google Scholar] [CrossRef]
- Garcia-Castillo, M.D.; Chinnapen, D.J.; Te Welscher, Y.M.; Gonzalez, R.J.; Softic, S.; Pacheco, M.; Mrsny, R.J.; Kahn, C.R.; von Andrian, U.H.; Lau, J.; et al. Mucosal absorption of therapeutic peptides by harnessing the endogenous sorting of glycosphingolipids. eLife 2018, 7, e34469. [Google Scholar] [CrossRef]
- Lencer, W.I.; Moe, S.; Rufo, P.A.; Madara, J.L. Transcytosis of cholera toxin subunits across model human intestinal epithelia. Proc. Natl. Acad. Sci. USA 1995, 92, 10094–10098. [Google Scholar] [CrossRef] [Green Version]
- Nelms, B.; Dalomba, N.F.; Lencer, W. A targeted RNAi screen identifies factors affecting diverse stages of receptor-mediated transcytosis. J. Cell Biol. 2017, 216, 511–525. [Google Scholar] [CrossRef] [PubMed]
- Garcia-Castillo, M.D.; Lencer, W.I.; Chinnapen, D.J. Transcytosis assay for transport of glycosphingolipids across MDCK-II cells. Bio-Protocol 2018, 8, e3049. [Google Scholar] [CrossRef] [PubMed]
- Cuatrecasas, P. Interaction of Vibrio cholerae enterotoxin with cell membranes. Biochemistry 1973, 12, 3547–3558. [Google Scholar] [CrossRef] [PubMed]
- Holmgren, J.; Lonnroth, I.; Svennerholm, L. Tissue receptor for cholera exotoxin: Postulated structure from studies with GM1 ganglioside and related glycolipids. Infect. Immun. 1973, 8, 208–214. [Google Scholar] [CrossRef] [Green Version]
- Schengrund, C.L.; Ringler, N.J. Binding of Vibrio cholera toxin and the heat-labile enterotoxin of Escherichia coli to GM1, derivatives of GM1, and nonlipid oligosaccharide polyvalent ligands. J. Biol. Chem. 1989, 264, 13233–13237. [Google Scholar] [CrossRef]
- Jobling, M.G.; Holmes, R.K. Mutational analysis of ganglioside GM(1)-binding ability, pentamer formation, and epitopes of cholera toxin B (CTB) subunits and CTB/heat-labile enterotoxin B subunit chimeras. Infect. Immun. 2002, 70, 1260–1271. [Google Scholar] [CrossRef] [Green Version]
- Pang, H.; Le, P.U.; Nabi, I.R. Ganglioside GM1 levels are a determinant of the extent of caveolae/raft-dependent endocytosis of cholera toxin to the Golgi apparatus. J. Cell Sci. 2004, 117, 1421–1430. [Google Scholar] [CrossRef] [Green Version]
- Holmgren, J.; Lonnroth, I.; Mansson, J.; Svennerholm, L. Interaction of cholera toxin and membrane GM1 ganglioside of small intestine. Proc. Natl. Acad. Sci. USA 1975, 72, 2520–2524. [Google Scholar] [CrossRef] [Green Version]
- Moss, J.; Fishman, P.H.; Manganiello, V.C.; Vaughan, M.; Brady, R.O. Functional incorporation of ganglioside into intact cells: Induction of choleragen responsiveness. Proc. Natl. Acad. Sci. USA 1976, 73, 1034–1037. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wolf, A.A.; Jobling, M.G.; Wimer-Mackin, S.; Ferguson-Maltzman, M.; Madara, J.L.; Holmes, R.K.; Lencer, W.I. Ganglioside structure dictates signal transduction by cholera toxin and association with caveolae-like membrane domains in polarized epithelia. J. Cell Biol. 1998, 141, 917–927. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fishman, P.H.; Pacuszka, T.; Hom, B.; Moss, J. Modification of ganglioside GM1. Effect of lipid moiety on choleragen action. J. Biol. Chem. 1980, 255, 7657–7664. [Google Scholar] [CrossRef]
- Pacuszka, T.; Bradley, R.M.; Fishman, P.H. Neoglycolipid analogues of ganglioside GM1 as functional receptors of cholera toxin. Biochemistry 1991, 30, 2563–2570. [Google Scholar] [CrossRef] [PubMed]
- Holmgren, J.; Fredman, P.; Lindblad, M.; Svennerholm, A.M.; Svennerholm, L. Rabbit intestinal glycoprotein receptor for Escherichia coli heat-labile enterotoxin lacking affinity for cholera toxin. Infect. Immun. 1982, 38, 424–433. [Google Scholar] [CrossRef] [Green Version]
- Holmgren, J.; Lindblad, M.; Fredman, P.; Svennerholm, L.; Myrvold, H. Comparison of receptors for cholera and Escherichia coli enterotoxins in human intestine. Gastroenterology 1985, 89, 27–35. [Google Scholar] [CrossRef]
- Fukuta, S.; Magnani, J.L.; Twiddy, E.M.; Holmes, R.K.; Ginsburg, V. Comparison of the carbohydrate-binding specificities of cholera toxin and Escherichia coli heat-labile enterotoxins LTh-I, LT-IIa, and LT-IIb. Infect. Immun. 1988, 56, 1748–1753. [Google Scholar] [CrossRef] [Green Version]
- Pacuszka, T.; Fishman, P.H. Generation of cell surface neoganglioproteins. GM1-neoganglioproteins are non-functional receptors for cholera toxin. J. Biol. Chem. 1990, 265, 7673–7678. [Google Scholar] [CrossRef]
- Orlandi, P.A.; Critchley, D.R.; Fishman, P.H. The heat-labile enterotoxin of Escherichia coli binds to polylactosaminoglycan-containing receptors in CaCo-2 human intestinal epithelial cells. Biochemistry 1994, 33, 12886–12895. [Google Scholar] [CrossRef]
- Kuziemko, G.M.; Stroh, M.; Stevens, R.C. Cholera toxin binding affinity and specificity for gangliosides determined by surface plasmon resonance. Biochemistry 1996, 35, 6375–6384. [Google Scholar] [CrossRef] [PubMed]
- Masserini, M.; Freire, E.; Palestini, P.; Calappi, E.; Tettamanti, G. Fuc-GM1 ganglioside mimics the receptor function of GM1 for cholera toxin. Biochemistry 1992, 31, 2422–2426. [Google Scholar] [CrossRef] [PubMed]
- Sethi, A.; Wands, A.M.; Mettlen, M.; Krishnamurthy, S.; Wu, H.; Kohler, J.J. Cell type and receptor identity regulate cholera toxin subunit B (CTB) internalization. Interface Focus 2019, 9, 20180076. [Google Scholar] [CrossRef] [Green Version]
- Aigal, S.; Claudinon, J.; Romer, W. Plasma membrane reorganization: A glycolipid gateway for microbes. Biochim. Biophys. Acta 2015, 1853, 858–871. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Johannes, L.; Billet, A. Glycosylation and raft endocytosis in cancer. Cancer Metastasis Rev. 2020, 39, 375–396. [Google Scholar] [CrossRef] [PubMed]
- Johannes, L. The cellular and chemical biology of endocytic trafficking and intracellular delivery-the GL-Lect hypothesis. Molecules 2021, 26, 3299. [Google Scholar] [CrossRef] [PubMed]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Kenworthy, A.K.; Schmieder, S.S.; Raghunathan, K.; Tiwari, A.; Wang, T.; Kelly, C.V.; Lencer, W.I. Cholera Toxin as a Probe for Membrane Biology. Toxins 2021, 13, 543. https://doi.org/10.3390/toxins13080543
Kenworthy AK, Schmieder SS, Raghunathan K, Tiwari A, Wang T, Kelly CV, Lencer WI. Cholera Toxin as a Probe for Membrane Biology. Toxins. 2021; 13(8):543. https://doi.org/10.3390/toxins13080543
Chicago/Turabian StyleKenworthy, Anne K., Stefanie S. Schmieder, Krishnan Raghunathan, Ajit Tiwari, Ting Wang, Christopher V. Kelly, and Wayne I. Lencer. 2021. "Cholera Toxin as a Probe for Membrane Biology" Toxins 13, no. 8: 543. https://doi.org/10.3390/toxins13080543