Why do membranes of some unhealthy cells adopt a cubic architecture?

ACS Central Science

Volumn 2, Issue 12, 2016, Pages 943-953

  Xiao, Qi ^a   Wang, Zhichun ^b   Williams, Dewight ^c   Leowanawat, Pawaret ^a   Peterca, Mihai ^a   Sherman, Samuel E ^a   Zhang, Shaodong ^a   Hammer, Daniel A ^b   Heiney, Paul A ^a   King, Steven R ^d   Markovitz, David M ^d   André, Sabine ^e   Gabius, Hans Joachim ^e   Klein, Michael L ^f   Percec, Virgil ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^e UNIVERSITY OF MUNICH   (Germany)

^f Temple University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN-ANTIBODY REACTIONS; ELECTRIC IMPEDANCE TOMOGRAPHY;

BICONTINUOUS; BICONTINUOUS CUBIC STRUCTURE; CONCANAVALIN A; ELECTRON TOMOGRAPHY; GENETICALLY MODIFIED; GLYCODENDRIMERS; NANOSCALE PARTICLES; VIRAL INFECTIONS;

PROTEINS;

EID: 85017121095     PISSN: 23747943     EISSN: 23747951     Source Type: Journal    
DOI: 10.1021/acscentsci.6b00284     Document Type: Article

References (60)

1. Daniels, E. W.; Breyer, E. P. Starvation effects on the ultrastructure of amoeba mitochondria. Cell Tissue Res. 1968, 91, 159-169.
2. Almsherqi, Z. A.; Kohlwein, S. D.; Deng, Y. Cubic membranes: a legend beyond the Flatland∗ of cell membrane organization. J. Cell Biol. 2006, 173, 839-844.
3. Almsherqi, Z. A.; Landh, T.; Kohlwein, S. D.; Deng, Y. Cubic membranes: the missing dimension of cell membrane organization. Int. Rev. Cell Mol. Biol. 2009, 274, 275-342.
4. Deng, Y.; Almsherqi, Z. A.; Ng, M. M. L.; Kohlwein, S. D. Do viruses subvert cholesterol homeostasis to induce host cubic membranes? Trends Cell Biol. 2010, 20, 371-379.
5. Yamamoto, A.; Masaki, R.; Tashiro, Y. Formation of crystalloid endoplasmic reticulum in COS cells upon overexpression of microsomal aldehyde dehydrogenase by cDNA transfection. J. Cell Sci. 1996, 109, 1727-1738.
6. Snapp, E. L.; Hegde, R. S.; Francolini, M.; Lombardo, F.; Colombo, S.; Pedrazzini, E.; Borgese, N.; Lippincott-Schwartz, J. Formation of stacked ER cisternae by low affinity protein interactions. J. Cell Biol. 2003, 163, 257-269.
7. Deng, Y.; Almsherqi, Z. A. Evolution of cubic membranes as antioxidant defence system. Interface Focus 2015, 5, 20150012.
8. Caffrey, M. A comprehensive review of the lipid cubic phase or in meso method for crystallizing membrane and soluble proteins and complexes. Acta Crystallogr., Sect. F: Struct. Biol. Commun. 2015, 71, 3-18.
9. Thomas, E. L.; Alward, D. B.; Kinning, D. J.; Martin, D. C.; Handlin, D. L.; Fetters, L. J. Ordered bicontinuous double-diamond structure of star block copolymers: a new equilibrium microdomain morphology. Macromolecules 1986, 19, 2197-2202.
10. Hasegawa, H.; Tanaka, H.; Yamasaki, K.; Hashimoto, T. Bicontinuous microdomain morphology of block copolymers. Macromolecules 1987, 20, 1651-1662.
11. Thomas, E. L.; Anderson, D. M.; Henkee, C. S.; Hoffman, D. Periodic area-minimizing surfaces in block copolymers. Nature 1988, 334, 598-601.
12. Chvalun, S. N.; Shcherbina, M. A.; Yakunin, A. N.; Blackwell, J.; Percec, V. Structure of gyroid mesophase formed by monodendrons with fluorinated alkyl tails. Polym. Sci., Ser. A 2007, 49, 158-167.
13. Rosen, B. M.; Wilson, C. J.; Wilson, D. A.; Peterca, M.; Imam, M. R.; Percec, V. Dendron-mediated self-assembly, disassembly, and self-organization of complex systems. Chem. Rev. 2009, 109, 6275-6540.
14. Rosen, B. M.; Peterca, M.; Huang, C.; Zeng, X.; Ungar, G.; Percec, V. Deconstruction as a strategy for the design of libraries of self-assembling dendrons. Angew. Chem., Int. Ed. 2010, 49, 7002-7005.
15. Huang, M.; Hsu, C.-H.; Wang, J.; Mei, S.; Dong, X.; Li, Y.; Li, M.; Liu, H.; Zhang, W.; Aida, T.; Zhang, W.-B.; Yue, K.; Cheng, S. Z. D. Selective assemblies of giant tetrahedra via precisely controlled positional interactions. Science 2015, 348, 424-428.
16. Luzzati, V.; Husson, F. The structure of the liquid-crystalline phase of lipid-water systems. J. Cell Biol. 1962, 12, 207-219.
17. Luzzati, V.; Tardieu, A.; Gulik-Krzywicki, T. Polymorphism of lipids. Nature 1968, 217, 1028-1030.
18. Luzzati, V.; Tardieu, A.; Gulik-Krzywicki, T.; Rivas, E.; Reiss-Husson, F. Structure of the cubic phases of lipid-water systems. Nature 1968, 220, 485-488.
19. Larsson, K. Cubic lipid-water phases: structures and biomembrane aspects. J. Phys. Chem. 1989, 93, 7304-7314.
20. Landh, T. Phase behavior in the system pine needle oil monoglycerides-poloxamer 407-water at 20.degree. J. Phys. Chem. 1994, 98, 8453-8467.
21. La, Y.; Park, C.; Shin, T. J.; Joo, S. H.; Kang, S.; Kim, K. T. Colloidal inverse bicontinuous cubic membranes of block copolymers with tunable surface functional groups. Nat. Chem. 2014, 6, 534-541.
22. Spicer, P. T.; Hayden, K. L.; Lynch, M. L.; Ofori-Boateng, A.; Burns, J. L. Novel process for producing cubic liquid crystalline nanoparticles (cubosomes). Langmuir 2001, 17, 5748-5756.
23. Spicer, P. Cubosome processing: industrial nanoparticle technology development. Chem. Eng. Res. Des. 2005, 83, 1283-1286.
24. Garg, G.; Saraf, S.; Saraf, S. Cubosomes: an overview. Biol. Pharm. Bull. 2007, 30, 350-353.
25. Sagalowicz, L.; Michel, M.; Adrian, M.; Frossard, P.; Rouvet, M.; Watzke, H. J.; Yaghmur, A.; De Campo, L.; Glatter, O.; Leser, M. E. Crystallography of dispersed liquid crystalline phases studied by cryotransmission electron microscopy. J. Microsc. 2006, 221, 110-121.
26. Gustafsson, J.; Ljusberg-Wahren, H.; Almgren, M.; Larsson, K. Cubic lipid-water phase dispersed into submicron particles. Langmuir 1996, 12, 4611-4613.
27. Siekmann, B.; Bunjes, H.; Koch, M. H. J.; Westesen, K. Preparation and structural investigations of colloidal dispersions prepared from cubic monoglyceride-water phases. Int. J. Pharm. 2002, 244, 33-43.
28. Esposito, E.; Cortesi, R.; Drechsler, M.; Paccamiccio, L.; Mariani, P.; Contado, C.; Stellin, E.; Menegatti, E.; Bonina, F.; Puglia, C. Cubosome dispersions as delivery systems for percutaneous administration of indomethacin. Pharm. Res. 2005, 22, 2163-2173.
29. Spicer, P. T.; Small, W. B., II; Small, W. B.; Lynch, M. L.; Burns, J. L. Dry powder precursors of cubic liquid crystalline nanoparticles (cubosomes). J. Nanopart. Res. 2002, 4, 297-311.
30. Percec, V.; Wilson, D. A.; Leowanawat, P.; Wilson, C. J.; Hughes, A. D.; Kaucher, M. S.; Hammer, D. A.; Levine, D. H.; Kim, A. J.; Bates, F. S.; Davis, K. P.; Lodge, T. P.; Klein, M. L.; DeVane, R. H.; Aqad, E.; Rosen, B. M.; Argintaru, A. O.; Sienkowska, M. J.; Rissanen, K.; Nummelin, S.; Ropponen, J. Self-assembly of Janus dendrimers into uniform dendrimersomes and other complex architectures. Science 2010, 328, 1009-1014.
31. Angelov, B.; Angelova, A.; Filippov, S. K.; Drechsler, M.; Štěpánek, P.; Lesieur, S. Multicompartment lipid cubic nanoparticles with high protein upload: millisecond dynamics of formation. ACS Nano 2014, 8, 5216-5226.
32. Karami, Z.; Hamidi, M. Cubosomes: remarkable drug delivery potential. Drug Discovery Today 2016, 21, 789-801.
33. - ions pump via reconstitution of EcClC membrane proteins in lipidic cubic mesophases. Proc. Natl. Acad. Sci. U. S. A. 2016, 113, 7491-7496.
34. Aleandri, S.; Bandera, D.; Mezzenga, R.; Landau, E. M. Biotinylated cubosomes: a versatile tool for active targeting and codelivery of paclitaxel and a fluorescein-based lipid dye. Langmuir 2015, 31, 12770-12776.
35. Percec, V.; Leowanawat, P.; Sun, H.-J.; Kulikov, O.; Nusbaum, C. D.; Tran, T. M.; Bertin, A.; Wilson, D. A.; Peterca, M.; Zhang, S.; Kamat, N. P.; Vargo, K.; Moock, D.; Johnston, E. D.; Hammer, D. A.; Pochan, D. J.; Chen, Y.; Chabre, Y. M.; Shiao, T. C.; Bergeron-Brlek, M.; André, S.; Roy, R.; Gabius, H.-J.; Heiney, P. A. Modular synthesis of amphiphilic Janus glycodendrimers and their self-assembly into glycodendrimersomes and other complex architectures with bioactivity to biomedically relevant lectins. J. Am. Chem. Soc. 2013, 135, 9055-9077.
36. Zhang, S.; Moussodia, R.-O.; Sun, H.-J.; Leowanawat, P.; Muncan, A.; Nusbaum, C. D.; Chelling, K. M.; Heiney, P. A.; Klein, M. L.; André, S.; Roy, R.; Gabius, H.-J.; Percec, V. Mimicking biological membranes with programmable glycan ligands self-assembled from amphiphilic Janus glycodendrimers. Angew. Chem., Int. Ed. 2014, 53, 10899-10903.
37. Zhang, S.; Xiao, Q.; Sherman, S. E.; Muncan, A.; Ramos Vicente, A. D. M.; Wang, Z.; Hammer, D. A.; Williams, D.; Chen, Y.; Pochan, D. J.; Vértesy, S.; André, S.; Klein, M. L.; Gabius, H.-J.; Percec, V. Glycodendrimersomes from sequence-defined Janus glycodendrimers reveal high activity and sensor capacity for the agglutination by natural variants of human lectins. J. Am. Chem. Soc. 2015, 137, 13334-13344.
38. Xiao, Q.; Zhang, S.; Wang, Z.; Sherman, S. E.; Moussodia, R.- O.; Peterca, M.; Muncan, A.; Williams, D. R.; Hammer, D. A.; Vértesy, S.; André, S.; Gabius, H.-J.; Klein, M. L.; Percec, V. Onion-like glycodendrimersomes from sequence-defined Janus glycodendrimers and influence of architecture on reactivity to a lectin. Proc. Natl. Acad. Sci. U. S. A. 2016, 113, 1162-1167.
39. Xiao, Q.; Yadavalli, S. S.; Zhang, S.; Sherman, S. E.; Fiorin, E.; da Silva, L.; Wilson, D. A.; Hammer, D. A.; André, S.; Gabius, H.-J.; Klein, M. L.; Goulian, M.; Percec, V. Bioactive cell-like hybrids coassembled from (glyco)dendrimersomes with bacterial membranes. Proc. Natl. Acad. Sci. U. S. A. 2016, 113, E1134-E1141.
40. Peterca, M.; Percec, V.; Leowanawat, P.; Bertin, A. Predicting the size and properties of dendrimersomes from the lamellar structure of their amphiphilic Janus dendrimers. J. Am. Chem. Soc. 2011, 133, 20507-20520.
41. Xiao, Q.; Rubien, J. D.; Wang, Z.; Reed, E. H.; Hammer, D. A.; Sahoo, D.; Heiney, P. A.; Yadavalli, S. S.; Goulian, M.; Wilner, S. E.; Baumgart, T.; Vinogradov, S. A.; Klein, M. L.; Percec, V. Self-sorting and coassembly of fluorinated, hydrogenated, and hybrid Janus dendrimers into dendrimersomes. J. Am. Chem. Soc. 2016, 138, 12655-12663.
42. Zhang, S.; Moussodia, R.-O.; Murzeau, C.; Sun, H.-J.; Klein, M. L.; Vértesy, S.; André, S.; Roy, R.; Gabius, H.-J.; Percec, V. Dissecting molecular aspects of cell interactions using glycodendrimersomes with programmable glycan presentation and engineered human lectins. Angew. Chem., Int. Ed. 2015, 54, 4036-4040.
43. Zhang, S.; Moussodia, R.-O.; Vértesy, S.; André, S.; Klein, M. L.; Gabius, H.-J.; Percec, V. Unraveling functional significance of natural variations of a human galectin by glycodendrimersomes with programmable glycan surface. Proc. Natl. Acad. Sci. U. S. A. 2015, 112, 5585-5590.
44. Gabius, H.-J.; Kaltner, H.; Kopitz, J.; André, S. The glycobiology of the CD system: a dictionary for translating marker designations into glycan/lectin structure and function. Trends Biochem. Sci. 2015, 40, 360-376.
45. Loris, R.; Hamelryck, T.; Bouckaert, J.; Wyns, L. Legume lectin structure. Biochim. Biophys. Acta, Protein Struct. Mol. Enzymol. 1998, 1383, 9-36.
46. Meagher, J. L.; Winter, H. C.; Ezell, P.; Goldstein, I. J.; Stuckey, J. A. Crystal structure of banana lectin reveals a novel second sugar binding site. Glycobiology 2005, 15, 1033-1042.
47. Singh, D. D.; Saikrishnan, K.; Kumar, P.; Surolia, A.; Sekar, K.; Vijayan, M. Unusual sugar specificity of banana lectin from Musa paradisiaca and its probable evolutionary origin. Glycobiology 2005, 15, 1025-1032.
48. Swanson, M. D.; Boudreaux, D. M.; Salmon, L.; Chugh, J.; Winter, H. C.; Meagher, J. L.; André, S.; Murphy, P. V.; Oscarson, S.; Roy, R.; King, S.; Kaplan, M. H.; Goldstein, I. J.; Tarbet, E. B.; Hurst, B. L.; Smee, D. F.; de la Fuente, C.; Hoffmann, H.-H.; Xue, Y.; Rice, C. M.; Schols, D.; Garcia, J. V.; Stuckey, J. A.; Gabius, H.-J.; Al-Hashimi, H. M.; Markovitz, D. M. Engineering a therapeutic lectin by uncoupling mitogenicity from antiviral activity. Cell 2015, 163, 746-758.
49. Swanson, M. D.; Winter, H. C.; Goldstein, I. J.; Markovitz, D. M. A lectin isolated from bananas is a potent inhibitor of HIV replication. J. Biol. Chem. 2010, 285, 8646-8655.
50. Liu, F.-T.; Rabinovich, G. A. Galectins as modulators of tumour progression. Nat. Rev. Cancer 2005, 5, 29-41.
51. Yang, R.-Y.; Rabinovich, G. A.; Liu, F.-T. Galectins: structure, function and therapeutic potential. Expert Rev. Mol. Med. 2008, 10, e17.
52. Thurston, T. L. M.; Wandel, M. P.; von Muhlinen, N.; Foeglein, Á.; Randow, F. Galectin 8 targets damaged vesicles for autophagy to defend cells against bacterial invasion. Nature 2012, 482, 414-418.
53. Bhat, R.; Belardi, B.; Mori, H.; Kuo, P.; Tam, A.; Hines, W. C.; Le, Q.-T.; Bertozzi, C. R.; Bissell, M. J. Nuclear repartitioning of galectin-1 by an extracellular glycan switch regulates mammary morphogenesis. Proc. Natl. Acad. Sci. U. S. A. 2016, 113, E4820-E4827.
54. Sagalowicz, L.; Acquistapace, S.; Watzke, H. J.; Michel, M. Study of liquid crystal space groups using controlled tilting with cryogenic transmission electron microscopy. Langmuir 2007, 23, 12003-12009.
55. Davis, K. P.; Lodge, T. P.; Bates, F. S. Vesicle membrane thickness in aqueous dispersions of block copolymer blends. Macromolecules 2008, 41, 8289-8291.
56. Demurtas, D.; Guichard, P.; Martiel, I.; Mezzenga, R.; Hébert, C.; Sagalowicz, L. Direct visualization of dispersed lipid bicontinuous cubic phases by cryo-electron tomography. Nat. Commun. 2015, 6, 8915.
57. Cairo, C. W.; Gestwicki, J. E.; Kanai, M.; Kiessling, L. L. Control of multivalent interactions by binding epitope density. J. Am. Chem. Soc. 2002, 124, 1615-1619.
58. Blouin, C. M.; Hamon, Y.; Gonnord, P.; Boularan, C.; Kagan, J.; Viaris de Lesegno, C.; Ruez, R.; Mailfert, S.; Bertaux, N.; Loew, D.; Wunder, C.; Johannes, L.; Vogt, G.; Contreras, F.-X.; Marguet, D.; Casanova, J.-L.; Galès, C.; He, H.-T.; Lamaze, C. Glycosylation dependent IFN-γR partitioning in lipid and actin nanodomains is critical for JAK activation. Cell 2016, 166, 920-934.
59. Norlén, L. Skin barrier formation: the membrane folding model. J. Invest. Dermatol. 2001, 117, 823-829.
60. Kremer, J. R.; Mastronarde, D. N.; McIntosh, J. R. Computer visualization of three-dimensional image data using IMOD. J. Struct. Biol. 1996, 116, 71-76.