Structure of the F-spondin domain of mindin, an integrin ligand and pattern recognition molecule

EMBO Journal

Volumn 28, Issue 3, 2009, Pages 286-297

  Li, Yili ^a   Cao, Chunzhang ^b   Jia, Wei ^c   Yu, Lily ^a   Mo, Min ^a   Wang, Qian ^a   Huang, Yuping ^a   Lim, Jae Min ^d   Ishihara, Mayumi ^d   Wells, Lance ^d   Azadi, Parastoo ^d   Robinson, Howard ^e   He, You Wen ^c   Zhang, Li ^b   Mariuzza, Roy A ^a  

^a UNIVERSITY OF MARYLAND BIOTECHNOLOGY INSTITUTE   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^c DUKE UNIVERSITY MEDICAL CENTER   (United States)

^d UNIVERSITY OF GEORGIA   (United States)

^e BROOKHAVEN NATIONAL LABORATORY   (United States)

Author keywords

Extracellular matrix; Innate immunity; Integrin; Mindin (spondin 2); Structure

Indexed keywords

CALCIUM; INTEGRIN; LIPOPOLYSACCHARIDE; SCLEROPROTEIN; SCLEROPROTEIN F SPONDIN; SCLEROPROTEIN MINDIN; THROMBOSPONDIN 1; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CONTROLLED STUDY; HUMAN; HUMAN CELL; MOUSE; MUTAGENESIS; NONHUMAN; PATTERN RECOGNITION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN STRUCTURE;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CALCIUM; CELL ADHESION; CELL LINE; CRYSTALLOGRAPHY, X-RAY; EXTRACELLULAR MATRIX PROTEINS; HUMANS; INTEGRINS; LIPOPOLYSACCHARIDES; MANNOSE; MASS SPECTROMETRY; MICE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, PATTERN RECOGNITION; REPETITIVE SEQUENCES, AMINO ACID; STATIC ELECTRICITY;

EID: 59649103053     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2008.288     Document Type: Article

References (47)

1. Arnaout MA, Goodman SL, Xiong JP (2007) Structure and mechanics of integrin-based cell adhesion. Curr Opin Cell Biol 19: 495-507
2. Benvenuti F, Hughes S, Walmsley M, Ruf S, Fetler L, Popoff M, Tybulewicz VL, Amigorena S (2004) Requirement of Rac1 and Rac2 expression by mature dendritic cells for T cell priming. Science 305: 1150-1153
3. Burstyn-Cohen T, Tzarfaty V, Frumkin A, Feinstein Y, Stoeckli E, Klar A (1999) F-spondin is required for accurate pathfinding of commissural axons at the floor plate. Neuron 23: 233-246
4. Brünger AT, Adams PD, Clore GM, DeLano WL, Gros P, Grosse-Kunstleve RW, Jiang JS, Kuszewski J, Nilges M, Pannu NS, Read RJ, Rice LM, Simonson T, Warren GL (1998) Crystallography and NMR systems: a new software suite for macromolecular structure determination. Acta Crystallogr Sec D Biol Crystallogr 54: 905-921
5. Cho W, Stahelin RV (2005) Membrane-protein interactions in cell signaling and membrane trafficking. Annu Rev Biophys Biomol Struct 34: 119-151
6. Doucey M-A, Hess D, Cacan R, Hofsteenge J (1998) Protein C-mannosylation is enzyme-catalyzed and uses dolichylphosphate-mannose as a precursor. Mol Biol Cell 9: 291-300
7. Feinstein Y, Borrell V, Garcia C, Burstyn-Cohen T, Tzarfaty V, Frumkin A, Nose A, Okamoto H, Higashijima S, Soriano E, Klar A (1999) F-spondin and mindin: two structurally and functionally related genes expressed in the hippocampus that promote outgrowth of embryonic hippocampal neurons. Development 126: 3637-3648
8. Gonzalez de Peredo A, Klein D, Macek B, Hess D, Peter-Katalinic J, Hofsteenge J (2002) C-mannosylation and O-fucosylation of thrombospondin type 1 repeats. Mol Cell Proteomics 1: 11-18
9. He Y-W, Li H, Zhang J, Hsu C-L, Lin E, Zhang N, Guo J, Forbush KA, Bevan MJ (2004) The extracellular matrix protein mindin is a pattern-recognition molecule for microbial pathogens. Nat Immunol 5: 88-97
10. Higashijima S, Nose A, Eguchi G, Hotta Y, Okamoto H (1997) Mindin/F-spondin family: novel ECM proteins expressed in the zebrafish embryonic axis. Dev Biol 192: 211-227
11. Hofsteenge J, Huwiler KG, Macek B, Hess D, Lawler J, Mosher DF, Peter-Katalinic J (2001) C-mannosylation and O-fucosylation of the thrombospondin type 1 module. J Biol Chem 276: 6485-6498
12. Humphries JD, Byron A, Humphries MJ (2006) Integrin ligands at a glance. J Cell Sci 119: 3901-3903
13. Hynes RO (2002) Integrins: bidirectional, allosteric signaling machines. Cell 110: 673-687
14. Jia W, Li H, He Y-W (2005) The extracellular matrix protein mindin serves as an integrin ligand and is critical for inflammatory cell recruitment. Blood 106: 3854-3859
15. Jia W, Li H, He Y-W (2008) Pattern recognition molecule mindin promotes intranasal clearance of influenza viruses. J Immunol 180: 6255-6261
16. Klar A, Baldassare M, Jessell TM (1992) F-spondin: a gene expressed at high levels in the floor plate encodes a secreted protein that promotes neural cell adhesion and neurite extension. Cell 69: 95-110
17. Kreis T, Vale R (eds) (1999) Guidebook to the Extracellular Matrix, Anchor, and Adhesion Proteins, 2nd edn Oxford University Press: Oxford
18. Lasarte JJ, Casares N, Gorraiz M, Hervás-Stubbs S, Arribillaga L, Mansilla C, Durantez M, Llopiz D, Sarobe P, Borrás-Cuesta F, Prieto J, Leclerc C (2007) The extra domain A from fibronectin targets antigens to TLR4-expressing cells and induces cytotoxic T cell responses in vivo. J Immunol 178: 748-756
19. Laskowski RA, MacArthur MW, Moss DS, Thornton JM (1993) PROCHECK: a program to check the stereo chemical quality of protein structures. J Appl Crystallogr 26: 283-291
20. Li H, Oliver T, Jia W, He Y-W (2006) Efficient dendritic cell priming of T lymphocytes depends on the extracellular protein mindin. EMBO J 25: 4097-4107
21. 2. J Biol Chem 278: 34395-34402
22. Manda R, Kohno T, Matsuno Y, Takenoshita S, Kuwano H, Yokota J (1999) Identification of genes (SPON2 and C20orf2) differentially expressed between cancerous and noncancerous lung cells by mRNA differential display. Genomics 61: 5-14
23. McDonald C, Núñez G (2004) Mindin the fort. Nat Immunol 5: 16-18
24. McRee DE (1999) XtalView/Xfit-a versatile program for manipulating atomic coordinates and electron density. J Struct Biol 125: 156-165
25. Muchowski PJ, Zhang L, Chang ER, Soule HR, Plow EF, Moyle M (1994) Functional interaction between the integrin antagonist neutrophil inhibitory factor and the I domain of CD11b/CD18. J Biol Chem 269: 26419-26423
26. Muroi E, Manabe S, Ikezaki M, Urata Y, Sato S, Kondo T, Ito Y, Ihara Y (2007) C-mannosylated peptides derived from the thrombospondin type 1 repeat enhance lipopolysaccharide-induced signaling in macrophage-like RAW264.7 cells. Glycobiology 17: 1015-1028
27. Nalefski EA, Falke JJ (1996) The C2 domain calcium-binding motif: structural and functional diversity. Protein Sci 5: 2375-2390
28. Nicholls A, Sharp KA, Honig B (1991) Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins 11: 281-296
29. Okamura Y, Watari M, Jerud ES, Young DW, Ishizaka ST, Rose J, Chow JC, Strauss III JF (2001) The extra domain A of fibronectin activates Toll-like receptor 4. J Biol Chem 276: 10229-10233
30. Otwinowski Z, Minor W (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 276: 307-326
31. Pääkkönen K, Tossavainen H, Permi P, Rakkolainen H, Rauvala H, Raulo E, Kilpeläinen I., Güntert P (2006) Solution structures of the first and fourth TSR domains of F-spondin. Proteins 64: 665-672
32. Pape T, Schneider TR (2004) HKL2MAP: a graphical user interface for macromolecular phasing with SHELX programs. J Appl Cryst 37: 843-844
33. Patti JM, Allen B, McGavin MJ, Hook M (1994) MSCRAMM-mediated adherence of microorganisms to host tissues. Annu Rev Microbiol 48: 585-617
34. 2+-binding domain. J Biol Chem 273: 15879-15882
35. Shimaoka M, Springer TA (2003) Therapeutic antagonists and conformational regulation of integrin function. Nat Rev Drug Disc 2: 703-715
36. L I domain and its complex with ICAM-1 reveal a shape-shifting pathway for integrin regulation. Cell 112: 99-111
37. 2. Proc Natl Acad Sci USA 102: 3366-3371
38. Strynadka NCJ, James MNG (1989) Crystal structures of the helix-loop-helix calcium-binding proteins. Annu Rev Biochem 58: 951-998
39. Tan K, Duquette M, Liu J, Dong Y, Zhang R, Joachimiak A, Lawler J, Wang J-H (2002) Crystal structure of the TSP-1 type 1 repeats: a novel layered fold and its biological implication. J Cell Biol 159: 373-382
40. Terwilliger TC (2003) SOLVE and RESOLVE: automated structure solution and density modification. Methods Enzymol 374: 22-37
41. Tucker RP (2004) The thrombospondin type 1 repeat family. Int J Biochem Cell Biol 36: 969-974
42. Tzarfaty-Majar V, Burstyn-Cohen T, Klar A (2001) F-spondin is a contact-repellent molecule for embryonic motor neurons. Proc Natl Acad Sci USA 98: 4722-4727
43. Umemiya T, Takeichi M, Nose A (1997) M-spondin, a novel ECM protein highly homologous to vertebrate F-spondin, is located at the muscle attachment sites in the Drosophila embryo. Dev Biol 186: 165-176
44. Venter JC, Adams MD, Myers EW, Li PW, Mural RJ, Sutton GG, Smith HO, Yandell M, Evans CA, Holt RA, Gocayne JD, Amanatides P, Ballew RM, Huson DH, Wortman JR, Zhang Q, Kodira CD, Zheng XH, Chen L, Skupski M et al (2001) The sequence of the human genome. Science 291: 1304-1351
45. Walker EH, Perisic O, Ried C, Stephens L, Williams RL (1999) Structural insights into phosphoinositide 3-kinase catalysis and signaling. Nature 402: 313-320
46. 2 for a specific and high affinity ligand, NIF. J Biol Chem 272: 17558-17564
47. Zisman S, Marom K, Avraham O, Rinsky-Halivni L, Gai U, Kligun G, Tzarfaty-Majar V, Suzuki T, Klar A (2007) Proteolysis and membrane capture of F-spondin generates combinatorial guidance clues from a single molecule. J Cell Biol 178: 1237-1249