Structural organization and interactions of transmembrane domains in tetraspanin proteins

BMC Structural Biology

Volumn 5, Issue , 2005, Pages

  Kovalenko, Oleg V ^a,b   Metcalf, Douglas G ^c   DeGrado, William F ^c   Hemler, Martin E ^a,b  

^a DANA FARBER CANCER INSTITUTE   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; CYSTEINE; GLYCINE; ISOLEUCINE; LEUCINE; MEMBRANE PROTEIN; PHENYLALANINE; TETRASPANIN; THREONINE; TYROSINE; VALINE;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; DISULFIDE BOND; MUTAGENESIS; NUCLEOTIDE SEQUENCE; PROTEIN AGGREGATION; PROTEIN CROSS LINKING; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; STRUCTURAL PROTEOMICS; STRUCTURE ANALYSIS;

ALGORITHMS; AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANTIGENS, CD; ANTIGENS, CD9; BLOTTING, WESTERN; CLONING, MOLECULAR; CONSERVED SEQUENCE; CROSS-LINKING REAGENTS; CYSTEINE; DIMERIZATION; DISULFIDES; DNA MUTATIONAL ANALYSIS; ETHYLMALEIMIDE; GLYCINE; HUMANS; LEUCINE; MEMBRANE GLYCOPROTEINS; MODELS, MOLECULAR; MOLECULAR CONFORMATION; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; MUTATION; PHENYLALANINE; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 24044539236     PISSN: 14726807     EISSN: 14726807     Source Type: Journal    
DOI: 10.1186/1472-6807-5-11     Document Type: Article

References (72)

1. Stipp CS, Kolesnikova TV, Hemler ME: Functional domains in tetraspanin proteins. Trends Biochem Sci 2003, 28:106-112.
2. Hemler ME: Tetraspanin proteins mediate cellular penetration, invasion and fusion events, and define a novel type of membrane microdomain. Ann Rev Cell Dev Biol 2003, 19:397-422.
3. Berditchevski F: Complexes of tetraspanins with integrins: more than meets the eye. J Cell Sci 2001, 114:4143-4151.
4. Tarrant JM, Robb L, van Spriel AB, Wright MD: Tetraspanins: molecular organisers of the leukocyte surface. Trends Immunol 2003, 24:610-617.
5. Le Naour F, Rubinstein E, Jasmin C, Prenant M, Boucheix C: Severely reduced female fertility in CD9-deficient mice. Science 2000, 287:319-321.
6. Kaji K, Oda S, Shikano T, Ohnuki T, Uematsu Y, Sakagami J, Tada N, Miyazaki S, Kudo A: The gamete fusion process is defective in eggs of CD9-deficient mice. Nature Genet 2000, 24:279-282.
7. Miyado K, Yamada G, Yamada S, Hasuma H, Nakamura Y, Ryu F, Suzuki K, Kosai K, Inoue K, Ogura A, Okabe M, Mekada E: Requirement of CD9 on the egg plasma membrane for fertilization. Science 2000, 287:321-324.
8. Maecker HT, Levy S: Normal lymphocyte development but delayed humoral immune response in CD81-null mice. J Exp Med 1997, 185:1505-1510.
9. Miyazaki T, Muller U, Campbell KS: Normal development but differentially altered proliferative responses of lymphocytes in mice lacking CD81. EMBO J 1997, 16:4217-4225.
10. Wright MD, Geary SM, Fitter S, Moseley GW, Lau LM, Sheng KC, Apostolopoulos V, Stanley EG, Jackson DE, Ashman LK: Characterization of mice lacking the tetraspanin superfamily member CD151. Mol Cell Biol 2004, 24:5978-5988.
11. Kazarov AR, Yang X, Stipp CS, Sehgal B, Hemler ME: An extracellular site on tetraspanin CD151 determines α 3 and α 6 integrin-dependent cellular morphology. J Cell Biol 2002, 158:1299-1309.
12. Zhu GZ, Miller BJ, Boucheix C, Rubinstein E, Liu CC, Hynes RO, Myles DG, Primakoff P: Residues SFQ (173-175) in the large extracellular loop of CD9 are required for gamete fusion. Development 2002, 129:1995-2002.
13. Kitadokoro K, Bordo D, Galli G, Petracca R, Falugi F, Abrignani S, Grandi G, Bolognesi M: CD81 extracellular domain 3D structure: insight into the tetraspanin superfamily structural motifs. EMBO J 2001, 20:12-18.
14. Seigneuret M, Delaguillaumie A, Lagaudriere-Gesbert C, Conjeaud H: Structure of the tetraspanin main extracellular domain. A partially conserved fold with a structurally variable domain insertion. J Biol Chem 2001, 276:40055-40064.
15. Maecker HT, Todd SC, Levy S: The tetraspanin superfamily: molecular facilitators. FASEB J 1997, 11:428-442.
16. Rubinstein E, Le Naour F, Lagaudrière-Gesbert C, Billard M, Conjeaud H, Boucheix C: CD9, CD63, CD81, and CD82 are components of a surface tetraspan network connected to HLA-DR and VLA antigens. Eur J Immunol 1996, 26:2657-2665.
17. Claas C, Stipp CS, Hemler ME: Evaluation of prototype TM4SF protein complexes and their relation to lipid rafts. J Biol Chem 2001, 276:7974-7984.
18. Charrin S, Manie S, Billard M, Ashman L, Gerlier D, Boucheix C, Rubinstein E: Multiple levels of interactions within the tetraspanin web. Biochem Biophys Res Commun 2003, 304:107-112.
19. Berditchevski F, Odintsova E, Sawada S, Gilbert E: Expression of the palmitoylation-deficient CD151 weakens the association of alpha 3beta 1 integrin with the tetraspanin-enriched microdomains and affects integrin-dependent signalling. J Biol Chem 2002, 277:36991-37000.
20. Charrin S, Manie S, Oualid M, Billard M, Boucheix C, Rubinstein E: Differential stability of tetraspanin/tetraspanin interactions: role of palmitoylation. FEBS Lett 2002, 516:139-144.
21. Yang X, Claas C, Kraeft SK, Chen LB, Wang Z, Kreidberg JA, Hemler ME: Palmitoylation of tetraspanin proteins: modulation of CD151 lateral interactions, subcellular distribution, and integrin-dependent cell morphology. Mol Biol Cell 2002, 13:767-781.
22. Berditchevski F, Gilbert E, Griffiths MR, Fitter S, Ashman L, Jenner SJ: Analysis of the CD151-alpha3beta1 integrin and CD151-tetraspanin interactions by mutagenesis. J Biol Chem 2001, 276:41165-41174.
23. Cannon KS, Cresswell P: Quality control of transmembrane domain assembly in the tetraspanin CD82. EMBO J 2001, 20:2443-2453.
24. Toyo-Oka K, Yashiro-Ohtani Y, Park CS, Tai XG, Miyake K, Hamaoka T, Fujiwara H: Association of a tetraspanin CD9 with CD5 on the T cell surface: role of particular transmembrane domains in the association. Int Immunol 1999, 11:2043-2052.
25. Kovalenko OV, Yang X, Kolesnikova TV, Hemler ME: Evidence for specific tetraspanin homodimers: inhibition of palmitoylation makes cysteine residues available for cross-linking. Biochem J 2004, 377:407-417.
26. Boucheix C, Thien Duc GH, Jasmin C, Rubinstein E: Tetraspanins and malignancy. Exp Rev Mol Med 2001 [http://www.expertreviews.org/01002381h.htm].
27. Hemler ME: Specific tetraspanin functions. J Cell Biol 2001, 155:1103-1107.
28. Bienstock RJ, Barrett JC: KAI1, a prostate metastasis suppressor: prediction of solvated structure and interactions with binding partners; integrins, cadherins, and cell-surface receptor proteins. Mol Carcinog 2001, 32:139-153.
29. Burkhard P, Stetefeld J, Strelkov SV: Coiled coils: a highly versatile protein folding motif. Trends Cell Biol 2001, 11:82-88.
30. Langosch D, Heringa J: Interaction of transmembrane helices by a knobs-into-holes packing characteristic of soluble coiled coils. Proteins 1998, 31:150-159.
31. Lupas A: Coiled coils: new structures and new functions. Trends Biochem Sci 1996, 21:375-382.
32. Walshaw J, Woolfson DN: Extended knobs-into-holes packing in classical and complex coiled-coil assemblies. J Struct Biol 2003, 144:349-361.
33. O'Shea EK, Klemm JD, Kim PS, Alber T: X-ray structure of the GCN4 leucine zipper, a two-stranded, parallel coiled coil. Science 1991, 254:539-544.
34. Zacharias DA, Violin JD, Newton AC, Tsien RY: Partitioning of lipid-modified monomeric GFPs into membrane microdomains of live cells. Science 2002, 296:913-916.
35. Bowie JU: Helix packing in membrane proteins. J Mol Biol 1997, 272:780-789.
36. Snapp EL, Hegde RS, 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.
37. Eilers M, Shekar SC, Shieh T, Smith SO, Fleming PJ: Internal packing of helical membrane proteins. Proc Natl Acad Sci USA 2000, 97:5796-5801.
38. Javadpour MM, Eilers M, Groesbeek M, Smith SO: Helix packing in polytopic membrane proteins: role of glycine in transmembrane helix association. Biophys J 1999, 77:1609-1618.
39. Russ WP, Engelman DM: The GxxxG motif: a framework for transmembrane helix-helix association. J Mol Biol 2000, 296:911-919.
40. Senes A, Gerstein M, Engelman DM: Statistical analysis of amino acid patterns in transmembrane helices: the GxxxG motif occurs frequently and in association with beta-branched residues at neighboring positions. J Mol Biol 2000, 296:921-936.
41. Lemmon MA, Flanagan JM, Hunt JF, Adair BD, Bormann BJ, Dempsey CE, Engelman DM: Glycophorin A dimerization is driven by specific interactions between transmembrane alpha-helices. J Biol Chem 1992, 267:7683-7689.
42. Lemmon MA, Treutlein HR, Adams PD, Brunger AT, Engelman DM: A dimerization motif for transmembrane alpha-helices. Nature Struct Biol 1994, 1:157-163.
43. MacKenzie KR, Prestegard JH, Engelman DM: A transmembrane helix dimer: structure and implications. Science 1997, 276:131-133.
44. Senes A, Ubarretxena-Belandia I, Engelman DM: The Calpha - H⋯O hydrogen bond: a determinant of stability and specificity in transmembrane helix interactions. Proc Natl Acad Sci USA 2001, 98:9056-9061.
45. Deber CM, Khan AR, Li Z, Joensson C, Glibowicka M, Wang J: Val→Ala mutations selectively alter helix-helix packing in the transmembrane segment of phage M13 coat protein. Proc Natl Acad Sci USA 1993, 90:11648-11652.
46. Overton MC, Chinault SL, Blumer KJ: Oligomerization, biogenesis, and signaling is promoted by a glycophorin A-like dimerization motif in transmembrane domain 1 of a yeast G protein-coupled receptor. J Biol Chem 2003, 278:49369-49377.
47. Li R, Gorelik R, Nanda V, Law PB, Lear JD, DeGrado WF, Bennett JS: Dimerization of the transmembrane domain of integrin alphaIIb subunit in cell membranes. J Biol Chem 2004, 279:26666-26673.
48. Gerber D, Sal-Man N, Shai Y: Two motifs within a transmembrane domain, one for homodimerization and the other for heterodimerization. J Biol Chem 2004, 279:21177-21182.
49. Kleiger G, Grothe R, Mallick P, Eisenberg D: GXXXG and AXXXA: common alpha-helical interaction motifs in proteins, particularly in extremophiles. Biochemistry 2002, 41:5990-5997.
50. Liu Y, Engelman DM, Gerstein M: Genomic analysis of membrane protein families: abundance and conserved motifs. Genome Biol 2002, 3:research0054.
51. Lear JD, Stouffer A, Gratkowski H, Nanda V, DeGrado WF: Association of a model transmembrane peptide containing Gly in a heptad sequence motif. Biophys J 2004, 87:3421-3429.
52. Cosson P, Bonifacino JS: Role of transmembrane domain interactions in the assembly of class II MHC molecules. Science 1992, 258:659-662.
53. Adamian L, Liang J: Helix-helix packing and interfacial pairwise interactions of residues in membrane proteins. J Mol Biol 2001, 311:891-907.
54. 2+-ATPase structure in the E1 and E2 conformations: mechanism, helix-helix and helix-lipid interactions. Biochim Biophys Acta 2002, 1565:246-266.
55. Doyle DA, Morais CJ, Pfuetzner RA, Kuo A, Gulbis JM, Cohen SL, Chait BT, MacKinnon R: The structure of the potassium channel: molecular basis of K+ conduction and selectivity. Science 1998, 280:69-77.
56. Zhou FX, Cocco MJ, Russ WP, Brunger AT, Engelman DM: Interhelical hydrogen bonding drives strong interactions in membrane proteins. Nature Struct Biol 2000, 7:154-160.
57. Choma C, Gratkowski H, Lear JD, DeGrado WF: Asparagine-mediated self-association of a model transmembrane helix. Nature Struct Biol 2000, 7:161-166.
58. Gratkowski H, Lear JD, DeGrado WF: Polar side chains drive the association of model transmembrane peptides. Proc Natl Acad Sci USA 2001, 98:880-885.
59. Ruan W, Lindner E, Langosch D: The interface of a membrane-spanning leucine zipper mapped by asparagine-scanning mutagenesis. Protein Sci 2004, 13:555-559.
60. Partridge AW, Therien AG, Deber CM: Polar mutations in membrane proteins as a biophysical basis for disease. Biopolymers 2002, 66:350-358.
61. Sanders CR, Myers JK: Disease-related misassembly of membrane proteins. Annu Rev Biophys Biomol Struct 2004, 33:25-51.
62. Cai SJ, Khorchid A, Ikura M, Inouye M: Probing catalytically essential domain orientation in histidine kinase EnvZ by targeted disulfide crosslinking. J Mol Biol 2003, 328:409-418.
63. Hamdan FF, Ward SD, Siddiqui NA, Bloodworth LM, Wess J: Use of an in situ disulfide cross-linking strategy to map proximities between amino acid residues in transmembrane domains I and VII of the M3 muscarinic acetylcholine receptor. Biochemistry 2002, 41:7647-7658.
64. Guan L, Murphy FD, Kaback HR: Surface-exposed positions in the transmembrane helices of the lactose permease of Escherichia coli determined by intermolecular thiol crosslinking. Proc Natl Acad Sci USA 2002, 99:3475-3480.
65. Roy R, Laage R, Langosch D: Synaptobrevin transmembrane domain dimerization-revisited. Biochemistry 2004, 43:4964-4970.
66. Luo B-H, Springer TA, Takagi J: A specific interface between integrin transmembrane helices and affinity for ligand. PLoS Biol 2004, 2:e153.
67. Yauch RL, Hemler ME: Specific interactions among transmembrane 4 superfamily (TM4SF) proteins and phosphatidylinositol 4-kinase. Biochem J 2000, 351:629-637.
68. Zhang XA, Bontrager AL, Hemler ME: TM4SF proteins associate with activated PKC and link PKC to specific beta1 integrins. J Biol Chem 2001, 276:25005-25013.
69. Li W, Metcalf D, Gorelik R, Li R, Mitra N, Nanda V, Law PB, Lear JD, DeGrado WF, Bennett JS: A push-pull mechanism for regulating integrin function. Proc Natl Acad Sci USA 2005, 102:1424-1429.
70. Weiner SJ, Kollman PA, Case DA, Singh UC, Ghio C, Alagona G, Profeta S, Weiner P: A new force field for molecular mechanical simulation of nucleic acids and proteins. J Am Chem Soc 1984, 106:765.
71. Kuhlman B, Baker D: Native protein sequences are close to optimal for their structures. Proc Natl Acad Sci USA 2000, 97:10383-10388.
72. Desmet J, De Maeyer M, Hazes B, Lasters I: The dead-end elimination theorem and its use in protein side-chain positioning. Nature 1992, 356:539-542.