Relative roles of GM1 ganglioside, N-acylneuraminic acids, and α2β1 integrin in mediating rotavirus infection

Journal of Virology

Volumn 88, Issue 8, 2014, Pages 4558-4571

  Fleming, Fiona E ^a   Böhm, Raphael ^b   Dang, Vi T ^a   Holloway, Gavan ^a   Haselhorst, Thomas ^b   Madge, Paul D ^b   Deveryshetty, Jaigeeth ^b   Yu, Xing ^b   Blanchard, Helen ^b   Von Itzstein, Mark ^b   Coulson, Barbara S ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b GRIFFITH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ACERAMIDO GANGLIOSIDE GM1; CHOLERA TOXIN B SUBUNIT; GANGLIOSIDE GM1; METHYL ALPHA DEXTRO N ACETYLNEURAMINIDE; N ACETYLNEURAMINIC ACID; N GLYCOLOYLNEURAMINIC ACID; PROTEIN VP4; PROTEIN VP8; SIALIC ACID; UNCLASSIFIED DRUG; VERY LATE ACTIVATION ANTIGEN 2; VIRUS PROTEIN;

ARTICLE; CELL INVASION; CELL SURFACE; CONTROLLED STUDY; HUMAN ROTAVIRUS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; ROTAVIRUS INFECTION; SATURATION TRANSFER DIFFERENCE NUCLEAR MAGNETIC RESONANCE; SEROTYPE; VIRUS ATTACHMENT; VIRUS INFECTIVITY; VIRUS STRAIN;

CAPSID PROTEINS; GANGLIOSIDES; HUMANS; INTEGRIN ALPHA2BETA1; N-ACETYLNEURAMINIC ACID; NEURAMINIC ACIDS; PROTEIN BINDING; RECEPTORS, VIRUS; ROTAVIRUS; ROTAVIRUS INFECTIONS;

EID: 84896971905     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.03431-13     Document Type: Article

References (79)

1. Li Z, Baker ML, Jiang W, Estes MK, Prasad BV. 2009. Rotavirus architecture at subnanometer resolution. J. Virol. 83:1754-1766. http://dx.doi.org/10.1128/JVI.01855-08.
2. Prasad BV, Wang GJ, Clerx JP, Chiu W. 1988. Three-dimensional structure of rotavirus. J. Mol. Biol. 199:269-275. http://dx.doi.org/10.1016/0022-2836(88)90313-0.
3. Settembre EC, Chen JZ, Dormitzer PR, GrigorieffN, Harrison SC. 2011. Atomic model of an infectious rotavirus particle. EMBO J. 30:408-416. http://dx.doi.org/10.1038/emboj.2010.322.
4. Yeager M, Dryden KA, Olson NH, Greenberg HB, Baker TS. 1990. Three-dimensional structure of rhesus rotavirus by cryoelectron microscopy and image reconstruction. J. Cell Biol. 110:2133-2144. http://dx.doi.org/10.1083/jcb.110.6.2133.
5. Estes MK, Cohen J. 1989. Rotavirus gene structure and function. Microbiol. Rev. 53:410-449.
6. Gorziglia M, Larralde G, Kapikian AZ, Chanock RM. 1990. Antigenic relationships among human rotaviruses as determined by outer capsid protein VP4. Proc. Natl. Acad. Sci. U. S. A. 87:7155-7159. http://dx.doi.org/10.1073/pnas.87.18.7155.
7. Haselhorst T, Fiebig T, Dyason JC, Fleming FE, Blanchard H, Coulson BS, von Itzstein M. 2011. Recognition of the GM3 ganglioside glycan by Rhesus rotavirus particles. Angew. Chem. Int. Ed. Engl. 50:1055-1058. http://dx.doi.org/10.1002/anie.201004116.
8. Coulson BS, Londrigan SL, Lee DJ. 1997. Rotavirus contains integrin ligand sequences and a disintegrin-like domain that are implicated in virus entry into cells. Proc. Natl. Acad. Sci. U. S. A. 94:5389-5394. http://dx.doi.org/10.1073/pnas.94.10.5389.
9. Dormitzer PR, Nason EB, Prasad BV, Harrison SC. 2004. Structural rearrangements in the membrane penetration protein of a non-enveloped virus. Nature 430:1053-1058. http://dx.doi.org/10.1038/nature02836.
10. Kim IS, Trask SD, Babyonyshev M, Dormitzer PR, Harrison SC. 2010. Effect of mutations in VP5 hydrophobic loops on rotavirus cell entry. J. Virol. 84:6200-6207. http://dx.doi.org/10.1128/JVI.02461-09.
11. Gutierrez M, Isa P, Sanchez-San Martin C, Perez-Vargas J, Espinosa R, Arias CF, Lopez S. 2010. Different rotavirus strains enter MA104 cells through different endocytic pathways: the role of clathrin-mediated endocytosis. J. Virol. 84:9161-9169. http://dx.doi.org/10.1128/JVI.00731-10.
12. Diaz-Salinas MA, Romero P, Espinosa R, Hoshino Y, Lopez S, Arias CF. 2013. The spike protein VP4 defines the endocytic pathway used by rotavirus to enter MA104 cells. J. Virol. 87:1658-1663. http://dx.doi.org/10.1128/JVI.02086-12.
13. Wolf M, Vo PT, Greenberg HB. 2011. Rhesus rotavirus entry into a polarized epithelium is endocytosis dependent and involves sequential VP4 conformational changes. J. Virol. 85:2492-2503. http://dx.doi.org/10.1128/JVI.02082-10.
14. Rolsma MD, Kuhlenschmidt TB, Gelberg HB, Kuhlenschmidt MS. 1998. Structure and function of a ganglioside receptor for porcine rotavirus. J. Virol. 72:9079-9091.
15. Graham KL, Halasz P, Tan Y, Hewish MJ, Takada Y, Mackow ER, Robinson MK, Coulson BS. 2003. Integrin-using rotaviruses bind α2β1 integrin α2 I domain via VP4 DGE sequence and recognize αXβ2 and αVβ3 by using VP7 during cell entry. J. Virol. 77:9969-9978. http://dx.doi.org/10.1128/JVI.77.18.9969-9978.2003.
16. Graham KL, Zeng W, Takada Y, Jackson DC, Coulson BS. 2004. Effects on rotavirus cell binding and infection of monomeric and polymeric peptides containing α2β1 and αxβ2 integrin ligand sequences. J. Virol. 78: 11786-11797. http://dx.doi.org/10.1128/JVI.78.21.11786-11797.2004.
17. Halasz P, Holloway G, Turner SJ, Coulson BS. 2008. Rotavirus replication in intestinal cells differentially regulates integrin expression by a phosphatidylinositol 3-kinase-dependent pathway, resulting in increased cell adhesion and virus yield. J. Virol. 82:148-160. http://dx.doi.org/10.1128/JVI.01980-07.
18. Londrigan SL, Graham KL, Takada Y, Halasz P, Coulson BS. 2003. Monkey rotavirus binding to α2β1 integrin requires the α2 I domain and is facilitated by the homologous β1 subunit. J. Virol. 77:9486-9501. http://dx.doi.org/10.1128/JVI.77.17.9486-9501.2003.
19. Londrigan SL, Hewish MJ, Thomson MJ, Sanders GM, Mustafa H, Coulson BS. 2000. Growth of rotaviruses in continuous human and monkey cell lines that vary in their expression of integrins. J. Gen. Virol. 81: 2203-2213.
20. Ciarlet M, Crawford SE, Estes MK. 2001. Differential infection of polarized epithelial cell lines by sialic acid-dependent and sialic acidindependent rotavirus strains. J. Virol. 75:11834-11850. http://dx.doi.org/10.1128/JVI.75.23.11834-11850.2001.
21. Hu L, Crawford SE, Czako R, Cortes-Penfield NW, Smith DF, Le Pendu J, Estes MK, Prasad BV. 2012. Cell attachment protein VP8* of a human rotavirus specifically interacts with A-type histo-blood group antigen. Nature 485:256-259. http://dx.doi.org/10.1038/nature10996.
22. Huang P, Xia M, Tan M, Zhong W, Wei C, Wang L, Morrow A, Jiang X. 2012. Spike protein VP8* of human rotavirus recognizes histo-blood group antigens in a type-specific manner. J. Virol. 86:4833-4843. http://dx.doi.org/10.1128/JVI.05507-11.
23. Guerrero CA, Mendez E, Zarate S, Isa P, Lopez S, Arias CF. 2000. Integrin αvβ3 mediates rotavirus cell entry. Proc. Natl. Acad. Sci. U. S. A. 97:14644-14649. http://dx.doi.org/10.1073/pnas.250299897.
24. Guerrero CA, Zarate S, Corkidi G, Lopez S, Arias CF. 2000. Biochemical characterization of rotavirus receptors in MA104 cells. J. Virol. 74:9362-9371. http://dx.doi.org/10.1128/JVI.74.20.9362-9371.2000.
25. Gualtero DF, Guzman F, Acosta O, Guerrero CA. 2007. Amino acid domains 280-297 of VP6 and 531-554 of VP4 are implicated in heat shock cognate protein hsc70-mediated rotavirus infection. Arch. Virol. 152: 2183-2196. http://dx.doi.org/10.1007/s00705-007-1055-5.
26. Perez-Vargas J, Romero P, Lopez S, Arias CF. 2006. The peptidebinding and ATPase domains of recombinant hsc70 are required to interact with rotavirus and reduce its infectivity. J. Virol. 80:3322-3331. http://dx.doi.org/10.1128/JVI.80.7.3322-3331.2006.
27. Ciarlet M, Estes MK. 1999. Human and most animal rotavirus strains do not require the presence of sialic acid on the cell surface for efficient infectivity. J. Gen. Virol. 80:943-948.
28. Fleming FE, Graham KL, Takada Y, Coulson BS. 2011. Determinants of the specificity of rotavirus interactions with the α2β1 integrin. J. Biol. Chem. 286:6165-6174. http://dx.doi.org/10.1074/jbc. M110.142992.
29. Fukudome K, Yoshie O, Konno T. 1989. Comparison of human, simian, and bovine rotaviruses for requirement of sialic acid in hemagglutination and cell adsorption. Virology 172:196-205. http://dx.doi.org/10.1016/0042-6822(89)90121-9.
30. Graham KL, Takada Y, Coulson BS. 2006. Rotavirus spike protein VP5* binds α2β1 integrin on the cell surface and competes with virus for cell binding and infectivity. J. Gen. Virol. 87:1275-1283. http://dx.doi.org/10.1099/vir.0.81580-0.
31. Haselhorst T, Fleming FE, Dyason JC, Hartnell RD, Yu X, Holloway G, Santegoets K, Kiefel MJ, Blanchard H, Coulson BS, von Itzstein M. 2009. Sialic acid dependence in rotavirus host cell invasion. Nat. Chem. Biol. 5:91-93. http://dx.doi.org/10.1038/nchembio.134.
32. Ciarlet M, Crawford SE, Cheng E, Blutt SE, Rice DA, Bergelson JM, Estes MK. 2002. VLA-2 (α2β1) integrin promotes rotavirus entry into cells but is not necessary for rotavirus attachment. J. Virol. 76:1109-1123. http://dx.doi.org/10.1128/JVI.76.3.1109-1123.2002.
33. Hemler ME, Jacobson JG, Strominger JL. 1985. Biochemical characterization of VLA-1 and VLA-2. Cell surface heterodimers on activated T cells. J. Biol. Chem. 260:15246-15252.
34. Ludert JE, Feng N, Yu JH, Broome RL, Hoshino Y, Greenberg HB. 1996. Genetic mapping indicates that VP4 is the rotavirus cell attachment protein in vitro and in vivo. J. Virol. 70:487-493.
35. Zarate S, Espinosa R, Romero P, Guerrero CA, Arias CF, Lopez S. 2000. Integrin α2β1 mediates the cell attachment of the rotavirus neuraminidase-resistant variant nar3. Virology 278:50-54. http://dx.doi.org/10.1006/viro.2000.0660.
36. Mendez E, Arias CF, Lopez S. 1993. Binding to sialic acids is not an essential step for the entry of animal rotaviruses to epithelial cells in culture. J. Virol. 67:5253-5259.
37. Haselhorst T, Blanchard H, Frank M, Kraschnefski MJ, Kiefel MJ, Szyczew AJ, Dyason JC, Fleming F, Holloway G, Coulson BS, von Itzstein M. 2007. STD NMR spectroscopy and molecular modeling investigation of the binding of N-acetylneuraminic acid derivatives to rhesus rotavirus VP8* core. Glycobiology 17:68-81. http://dx.doi.org/10.1093/glycob/cwl051.
38. Yu X, Dang VT, Fleming FE, von Itzstein M, Coulson BS, Blanchard H. 2012. Structural basis of rotavirus strain preference towards N-acetyl-or N-glycolylneuraminic acid-containing receptors. J. Virol. 86:13456-13466. http://dx.doi.org/10.1128/JVI.06975-11.
39. Saito M, Sugano K, Nagai Y. 1979. Action of Arthrobacter ureafaciens sialidase on sialoglycolipid substrates. Mode of action and highly specific recognition of the oligosaccharide moiety of ganglioside GM1. J. Biol. Chem. 254:7845-7854.
40. Venerando B, Cestaro B, Fiorilli A, Ghidoni R, Preti A, Tettamanti G. 1982. Kinetics of Vibrio cholerae sialidase action on gangliosidic substrates at different supramolecular-organizational levels. Biochem. J. 203: 735-742.
41. Isa P, Arias CF, Lopez S. 2006. Role of sialic acids in rotavirus infection. Glycoconj. J. 23:27-37. http://dx.doi.org/10.1007/s10719-006-5435-y.
42. Mendez E, Lopez S, Cuadras MA, Romero P, Arias CF. 1999. Entry of rotaviruses is a multistep process. Virology 263:450-459. http://dx.doi.org/10.1006/viro.1999.9976.
43. Nagafuku M, Okuyama K, Onimaru Y, Suzuki A, Odagiri Y, Yamashita T, Iwasaki K, Fujiwara M, Takayanagi M, Ohno I, Inokuchi J. 2012. CD4 and CD8 T cells require different membrane gangliosides for activation. Proc. Natl. Acad. Sci. U. S. A. 109:E336-342. http://dx.doi.org/10.1073/pnas.1114965109.
44. Angstrom J, Backstrom M, Berntsson A, Karlsson N, Holmgren J, Karlsson KA, Lebens M, Teneberg S. 2000. Novel carbohydrate binding site recognizing blood group A and B determinants in a hybrid of cholera toxin and Escherichia coli heat-labile enterotoxin B-subunits. J. Biol. Chem. 275:3231-3238. http://dx.doi.org/10.1074/jbc.275.5.3231.
45. Woode GN, Bridger JC, Hall G, Dennis MJ. 1974. The isolation of a reovirus-like agent associated with diarrhoea in colostrum-deprived calves in Great Britain. Res. Vet. Sci. 16:102-105.
46. Beisner B, Kool D, Marich A, Holmes IH. 1998. Characterisation of G serotype dependent non-antibody inhibitors of rotavirus in normal mouse serum. Arch. Virol. 143:1277-1294. http://dx.doi.org/10.1007/s007050050375.
47. Coulson BS. 1993. Typing of human rotavirus VP4 by an enzyme immunoassay using monoclonal antibodies. J. Clin. Microbiol. 31:1-8.
48. Kirkwood CD, Bishop RF, Coulson BS. 1998. Attachment and growth of human rotaviruses RV-3 and S12/85 in Caco-2 cells depend on VP4. J. Virol. 72:9348-9352.
49. Kalica AR, Flores J, Greenberg HB. 1983. Identification of the rotaviral gene that codes for hemagglutination and protease-enhanced plaque formation. Virology 125:194-205. http://dx.doi.org/10.1016/0042-6822(83)90073-9.
50. Kiefel MJ, Beisner B, Bennett S, Holmes IH, von Itzstein M. 1996. Synthesis and biological evaluation of N-acetylneuraminic acid-based rotavirus inhibitors. J. Med. Chem. 39:1314-1320. http://dx.doi.org/10.1021/jm950611f.
51. Sherman AA, Yudina ON, Shashkov AS, Menshov VM, Nifantiev NE. 2002. Preparative route to N-glycolylneuraminic acid phenyl 2-thioglycoside donor and synthesis of Neu5Gc-α-(2→3')-lactosamine 3-aminopropyl glycoside. Carbohydr. Res. 337:451-457. http://dx.doi.org/10.1016/S0008-6215(02)00003-4.
52. Padilla-Noriega L, Dunn SJ, Lopez S, Greenberg HB, Arias CF. 1995. Identification of two independent neutralization domains on the VP4 trypsin cleavage products VP5* and VP8* of human rotavirus ST3. Virology 206:148-154. http://dx.doi.org/10.1016/S0042-6822(95)80029-8.
53. Coulson BS, Tursi JM, McAdam WJ, Bishop RF. 1986. Derivation of neutralizing monoclonal antibodies to human rotaviruses and evidence that an immunodominant neutralization site is shared between serotypes 1 and 3. Virology 154:302-312. http://dx.doi.org/10.1016/0042-6822(86)90456-3.
54. Sonza S, Breschkin AM, Holmes IH. 1983. Derivation of neutralizing monoclonal antibodies against rotavirus. J. Virol. 45:1143-1146.
55. Sonza S, Breschkin AM, Holmes IH. 1984. The major surface glycoprotein of simian rotavirus (SA11) contains distinct epitopes. Virology 134: 318-327. http://dx.doi.org/10.1016/0042-6822(84)90300-3.
56. Hewish MJ, Takada Y, Coulson BS. 2000. Integrins α2β1 and α4β1 can mediate SA11 rotavirus attachment and entry into cells. J. Virol. 74:228-236. http://dx.doi.org/10.1128/JVI.74.1.228-236.2000.
57. Scott SA, Holloway G, Coulson BS, Szyczew AJ, Kiefel MJ, von Itzstein M, Blanchard H. 2005. Crystallization and preliminary X-ray diffraction analysis of the sialic acid-binding domain (VP8*) of porcine rotavirus strain CRW-8. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 61: 617-620. http://dx.doi.org/10.1107/S1744309105013849.
58. Yu X, Guillon A, Szyczew AJ, Kiefel MJ, Coulson BS, von Itzstein M, Blanchard H. 2008. Crystallization and preliminary X-ray diffraction analysis of the carbohydrate-recognizing domain (VP8*) of bovine rotavirus strain NCDV. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 64:509-511. http://dx.doi.org/10.1107/S1744309108011949.
59. Kraschnefski MJ, Scott SA, Holloway G, Coulson BS, von Itzstein M, Blanchard H. 2005. Cloning, expression, purification, crystallization and preliminary X-ray diffraction analysis of the VP8* carbohydrate-binding protein of the human rotavirus strain Wa. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 61:989-993. http://dx.doi.org/10.1107/S1744309105032999.
60. Rippinger CM, Patton JT, McDonald SM. 2010. Complete genome sequence analysis of candidate human rotavirus vaccine strains RV-3 and 116E. Virology 405:201-213. http://dx.doi.org/10.1016/j.virol.2010.06.005.
61. Blanchard H, Yu X, Coulson BS, von Itzstein M. 2007. Insight into host cell carbohydrate-recognition by human and porcine rotavirus from crystal structures of the virion spike associated carbohydrate-binding domain (VP8*). J. Mol. Biol. 367:1215-1226. http://dx.doi.org/10.1016/j.jmb.2007.01.028.
62. Low JA, Magnuson B, Tsai B, Imperiale MJ. 2006. Identification of gangliosides GD1b and GT1b as receptors for BK virus. J. Virol. 80:1361-1366. http://dx.doi.org/10.1128/JVI.80.3.1361-1366.2006.
63. Warner S, Hartley CA, Stevenson RA, Ficorilli N, Varrasso A, Studdert MJ, Crabb BS. 2001. Evidence that Equine rhinitis A virus VP1 is a target of neutralizing antibodies and participates directly in receptor binding. J. Virol. 75:9274-9281. http://dx.doi.org/10.1128/JVI.75.19.9274-9281.2001.
64. Miller-Podraza H, Bradley RM, Fishman PH. 1982. Biosynthesis and localization of gangliosides in cultured cells. Biochemistry 21:3260-3265. http://dx.doi.org/10.1021/bi00257a002.
65. Fleming FE, Graham KL, Taniguchi K, Takada Y, Coulson BS. 2007. Rotavirus-neutralizing antibodies inhibit virus binding to integrins α2β1 and α4β1. Arch. Virol. 152:1087-1101. http://dx.doi.org/10.1007/s00705-007-0937-x.
66. Ciarlet M, Ludert JE, Iturriza-Gomara M, Liprandi F, Gray JJ, Desselberger U, Estes MK. 2002. Initial interaction of rotavirus strains with N-acetylneuraminic (sialic) acid residues on the cell surface correlates with VP4 genotype, not species of origin. J. Virol. 76:4087-4095. http://dx.doi.org/10.1128/JVI.76.8.4087-4095.2002.
67. Dormitzer PR, Sun ZY, Blixt O, Paulson JC, Wagner G, Harrison SC. 2002. Specificity and affinity of sialic acid binding by the rhesus rotavirus VP8* core. J. Virol. 76:10512-10517. http://dx.doi.org/10.1128/JVI.76.20.10512-10517.2002.
68. Yu X, Coulson BS, Fleming FE, Dyason JC, von Itzstein M, Blanchard H. 2011. Novel structural insights into rotavirus recognition of ganglioside glycan receptors. J. Mol. Biol. 413:929-939. http://dx.doi.org/10.1016/j.jmb.2011.09.005.
69. del Pozo MA, Alderson NB, Kiosses WB, Chiang HH, Anderson RG, Schwartz MA. 2004. Integrins regulate Rac targeting by internalization of membrane domains. Science 303:839-842. http://dx.doi.org/10.1126/science.1092571.
70. Guo CT, Nakagomi O, Mochizuki M, Ishida H, Kiso M, Ohta Y, Suzuki T, Miyamoto D, Hidari KI, Suzuki Y. 1999. Ganglioside GM(1a) on the cell surface is involved in the infection by human rotavirusKUNandMOstrains. J. Biochem. 126:683-688. http://dx.doi.org/10.1093/oxfordjournals.jbchem.a022503.
71. Delorme C, Brussow H, Sidoti J, Roche N, Karlsson K-A, Neeser J-R, Teneberg S. 2001. Glycosphingolipid binding specifities of rotavirus: identification of a sialic acid-binding epitope. J. Virol. 75:2276-2287. http://dx.doi.org/10.1128/JVI.75.5.2276-2287.2001.
72. Martinez MA, Lopez S, Arias CF, Isa P. 2012. Gangliosides have a functional role during rotavirus cell entry. J. Virol. 87:1115-1122. http://dx.doi.org/10.1128/JVI.01964-12.
73. Magaldi TG, Buch MH, Murata H, Erickson KD, Neu U, Garcea RL, Peden K, Stehle T, DiMaio D. 2012. Mutations in the GM1 binding site of simian virus 40 VP1 alter receptor usage and cell tropism. J. Virol. 86:7028-7042. http://dx.doi.org/10.1128/JVI.00371-12.
74. Chinnapen DJ, Hsieh WT, te Welscher YM, Saslowsky DE, Kaoutzani L, Brandsma E, D'Auria L, Park H, Wagner JS, Drake KR, Kang M, Benjamin T, Ullman MD, Costello CE, Kenworthy AK, Baumgart T, Massol RH, Lencer WI. 2012. Lipid sorting by ceramide structure from plasma membrane to ER for the cholera toxin receptor ganglioside GM1. Dev. Cell 23:573-586. http://dx.doi.org/10.1016/j.devcel.2012.08.002.
75. Dormitzer PR, Sun ZY, Wagner G, Harrison SC. 2002. The rhesus rotavirus VP4 sialic acid binding domain has a galectin fold with a novel carbohydrate binding site. EMBO J. 21:885-897. http://dx.doi.org/10.1093/emboj/21.5.885.
76. Kirkwood CD, Coulson BS, Bishop RF. 1996. G3P2 rotaviruses causing diarrhoeal disease in neonates differ in VP4, VP7 and NSP4 sequence from G3P2 strains causing asymptomatic neonatal infection. Arch. Virol. 141: 1661-1676. http://dx.doi.org/10.1007/BF01718290.
77. Pan D, Song Y. 2010. Role of altered sialylation of the I-like domain of β1 integrin in the binding of fibronectin to β1 integrin: thermodynamics and conformational analyses. Biophys. J. 99:208-217. http://dx.doi.org/10.1016/j.bpj.2010.03.063.
78. Fujita A, Cheng J, Hirakawa M, Furukawa K, Kusunoki S, Fujimoto T. 2007. Gangliosides GM1 and GM3 in the living cell membrane form clusters susceptible to cholesterol depletion and chilling. Mol. Biol. Cell 18: 2112-2122. http://dx.doi.org/10.1091/mbc. E07-01-0071.
79. Frisz JF, Lou K, Klitzing HA, Hanafin WP, Lizunov V, Wilson RL, Carpenter KJ, Kim R, Hutcheon ID, Zimmerberg J, Weber PK, Kraft ML. 2013. Direct chemical evidence for sphingolipid domains in the plasma membranes of fibroblasts. Proc. Natl. Acad. Sci. U. S. A. 110:E613-E622. http://dx.doi.org/10.1073/pnas.1216585110.