1czt › Citations

Crystal structures of the membrane-binding C2 domain of human coagulation factor V.

Macedo-Ribeiro S, Bode W, Huber R, Quinn-Allen MA, Kim SW, Ortel TL, Bourenkov GP, Bartunik HD, Stubbs MT, Kane WH, Fuentes-Prior P
Nature 402 434-9 (1999)
Related entries: 1czs, 1czv

Cited: 139 times
EuropePMC logo PMID: 10586886

Abstract

Rapid and controlled clot formation is achieved through sequential activation of circulating serine proteinase precursors on phosphatidylserine-rich procoagulant membranes of activated platelets and endothelial cells. The homologous complexes Xase and prothrombinase, each consisting of an active proteinase and a non-enzymatic cofactor, perform critical steps within this coagulation cascade. The activated cofactors VIIIa and Va, highly specific for their cognate proteinases, are each derived from precursors with the same A1-A2-B-A3-C1-C2 architecture. Membrane binding is mediated by the C2 domains of both cofactors. Here we report two crystal structures of the C2 domain of human factor Va. The conserved beta-barrel framework provides a scaffold for three protruding loops, one of which adopts markedly different conformations in the two crystal forms. We propose a mechanism of calcium-independent, stereospecific binding of factors Va and VIIIa to phospholipid membranes, on the basis of (1) immersion of hydrophobic residues at the apices of these loops in the apolar membrane core; (2) specific interactions with phosphatidylserine head groups in the groove enclosed by these loops; and (3) favourable electrostatic contacts of basic side chains with negatively charged membrane phosphate groups.

Articles - 1czt mentioned but not cited (15)

  1. A consensus view of protein dynamics. Rueda M, Ferrer-Costa C, Meyer T, Pérez A, Camps J, Hospital A, Gelpí JL, Orozco M. Proc Natl Acad Sci U S A 104 796-801 (2007)
  2. Crystal structure of the bovine lactadherin C2 domain, a membrane binding motif, shows similarity to the C2 domains of factor V and factor VIII. Lin L, Huai Q, Huang M, Furie B, Furie BC. J Mol Biol 371 717-724 (2007)
  3. Trp2313-His2315 of factor VIII C2 domain is involved in membrane binding: structure of a complex between the C2 domain and an inhibitor of membrane binding. Liu Z, Lin L, Yuan C, Nicolaes GA, Chen L, Meehan EJ, Furie B, Furie B, Huang M. J Biol Chem 285 8824-8829 (2010)
  4. Design of protein membrane interaction inhibitors by virtual ligand screening, proof of concept with the C2 domain of factor V. Segers K, Sperandio O, Sack M, Fischer R, Miteva MA, Rosing J, Nicolaes GA, Villoutreix BO. Proc Natl Acad Sci U S A 104 12697-12702 (2007)
  5. Conservative mutations in the C2 domains of factor VIII and factor V alter phospholipid binding and cofactor activity. Gilbert GE, Novakovic VA, Kaufman RJ, Miao H, Pipe SW. Blood 120 1923-1932 (2012)
  6. Molecular analysis of muskelin identifies a conserved discoidin-like domain that contributes to protein self-association. Prag S, Collett GD, Adams JC. Biochem J 381 547-559 (2004)
  7. Analysis of the "thermodynamic information content" of a Homo sapiens structural database reveals hierarchical thermodynamic organization. Larson SA, Hilser VJ. Protein Sci 13 1787-1801 (2004)
  8. Denatured-state energy landscapes of a protein structural database reveal the energetic determinants of a framework model for folding. Wang S, Gu J, Larson SA, Whitten ST, Hilser VJ. J Mol Biol 381 1184-1201 (2008)
  9. Cryo-EM structures of human coagulation factors V and Va. Ruben EA, Rau MJ, Fitzpatrick JAJ, Di Cera E. Blood 137 3137-3144 (2021)
  10. Theoretical and experimental study of the D2194G mutation in the C2 domain of coagulation factor V. Miteva MA, Brugge JM, Rosing J, Nicolaes GA, Villoutreix BO. Biophys J 86 488-498 (2004)
  11. Exploring early stages of the chemical unfolding of proteins at the proteome scale. Candotti M, Pérez A, Ferrer-Costa C, Rueda M, Meyer T, Gelpí JL, Orozco M. PLoS Comput Biol 9 e1003393 (2013)
  12. TRIFORCE: Tessellated Semianalytical Solvent Exposed Surface Areas and Derivatives. Drechsel NJ, Fennell CJ, Dill KA, Villà-Freixa J. J Chem Theory Comput 10 4121-4132 (2014)
  13. The dipeptidyl peptidase IV inhibitors vildagliptin and K-579 inhibit a phospholipase C: a case of promiscuous scaffolds in proteins. Chakraborty S, Rendón-Ramírez A, Ásgeirsson B, Dutta M, Ghosh AS, Oda M, Venkatramani R, Rao BJ, Dandekar AM, Goñi FM. F1000Res 2 286 (2013)
  14. Conformational change path between closed and open forms of C2 domain of coagulation factor V on a two-dimensional free-energy surface. Wu S, Lee CJ, Pedersen LG. Phys Rev E Stat Nonlin Soft Matter Phys 79 041909 (2009)
  15. In silico evidence of Remdesivir action in blood coagulation cascade modulation in COVID-19 treatment. Pagliarin LG, de Oliveira LM, Dos Anjos VNF, de Souza CBT, Peiter GC, Façanha Wendel C, Dillmann Groto A, Freire de Melo F, Teixeira KN. World J Biol Chem 14 72-83 (2023)


Reviews citing this publication (33)

  1. Membrane recognition by phospholipid-binding domains. Lemmon MA. Nat Rev Mol Cell Biol 9 99-111 (2008)
  2. The distribution and function of phosphatidylserine in cellular membranes. Leventis PA, Grinstein S. Annu Rev Biophys 39 407-427 (2010)
  3. Mammalian collagen receptors. Leitinger B, Hohenester E. Matrix Biol 26 146-155 (2007)
  4. Exposure of platelet membrane phosphatidylserine regulates blood coagulation. Lentz BR. Prog Lipid Res 42 423-438 (2003)
  5. Getting to the Outer Leaflet: Physiology of Phosphatidylserine Exposure at the Plasma Membrane. Bevers EM, Williamson PL. Physiol Rev 96 605-645 (2016)
  6. Regulation of blood coagulation by the protein C anticoagulant pathway: novel insights into structure-function relationships and molecular recognition. Dahlbäck B, Villoutreix BO. Arterioscler Thromb Vasc Biol 25 1311-1320 (2005)
  7. The anticoagulant protein C pathway. Dahlbäck B, Villoutreix BO. FEBS Lett 579 3310-3316 (2005)
  8. X-linked juvenile retinoschisis: clinical diagnosis, genetic analysis, and molecular mechanisms. Molday RS, Kellner U, Weber BH. Prog Retin Eye Res 31 195-212 (2012)
  9. SED1/MFG-E8: a bi-motif protein that orchestrates diverse cellular interactions. Raymond A, Ensslin MA, Shur BD. J Cell Biochem 106 957-966 (2009)
  10. Factor V and thrombotic disease: description of a janus-faced protein. Nicolaes GA, Dahlbäck B. Arterioscler Thromb Vasc Biol 22 530-538 (2002)
  11. Structural and functional diversity of lectin repertoires in invertebrates, protochordates and ectothermic vertebrates. Vasta GR, Ahmed H, Odom EW. Curr Opin Struct Biol 14 617-630 (2004)
  12. Phosphatidylserine in the brain: metabolism and function. Kim HY, Huang BX, Spector AA. Prog Lipid Res 56 1-18 (2014)
  13. The intriguing world of prothrombin activators from snake venom. Kini RM. Toxicon 45 1133-1145 (2005)
  14. Structure and mechanism of human cytosolic phospholipase A(2). Dessen A. Biochim Biophys Acta 1488 40-47 (2000)
  15. Progress in the understanding of the protein C anticoagulant pathway. Dahlbäck B. Int J Hematol 79 109-116 (2004)
  16. Inherited defects of coagulation factor V: the hemorrhagic side. Asselta R, Tenchini ML, Duga S. J Thromb Haemost 4 26-34 (2006)
  17. Molecular recognition in the protein C anticoagulant pathway. Dahlbäck B, Villoutreix BO. J Thromb Haemost 1 1525-1534 (2003)
  18. Mild/moderate haemophilia A: new insights into molecular mechanisms and inhibitor development. d'Oiron R, Pipe SW, Jacquemin M. Haemophilia 14 Suppl 3 138-146 (2008)
  19. Coagulation factor V. Duga S, Asselta R, Tenchini ML. Int J Biochem Cell Biol 36 1393-1399 (2004)
  20. Identification of novel gamete receptors that mediate sperm adhesion to the egg coat. Shur BD, Rodeheffer C, Ensslin MA, Lyng R, Raymond A. Mol Cell Endocrinol 250 137-148 (2006)
  21. Activated protein C resistance (FV(Leiden)) and thrombosis: factor V mutations causing hypercoagulable states. Nicolaes GA, Dahlbäck B. Hematol Oncol Clin North Am 17 37-61, vi (2003)
  22. Humoral immune response to ADAMTS13 in acquired thrombotic thrombocytopenic purpura. Pos W, Luken BM, Sorvillo N, Kremer Hovinga JA, Voorberg J. J Thromb Haemost 9 1285-1291 (2011)
  23. Diversity in recognition of glycans by F-type lectins and galectins: molecular, structural, and biophysical aspects. Vasta GR, Ahmed H, Bianchet MA, Fernández-Robledo JA, Amzel LM. Ann N Y Acad Sci 1253 E14-26 (2012)
  24. SED1 function during mammalian sperm-egg adhesion. Shur BD, Ensslin MA, Rodeheffer C. Curr Opin Cell Biol 16 477-485 (2004)
  25. The structure of thrombin, a chameleon-like proteinase. Bode W. J Thromb Haemost 3 2379-2388 (2005)
  26. Blood coagulation factor Va's key interactive residues and regions for prothrombinase assembly and prothrombin binding. Schreuder M, Reitsma PH, Bos MHA. J Thromb Haemost 17 1229-1239 (2019)
  27. Pathogenic antibodies to coagulation factors. Part II. Fibrinogen, prothrombin, thrombin, factor V, factor XI, factor XII, factor XIII, the protein C system and von Willebrand factor. Lollar P. J Thromb Haemost 3 1385-1391 (2005)
  28. F-Type Lectins: A Highly Diversified Family of Fucose-Binding Proteins with a Unique Sequence Motif and Structural Fold, Involved in Self/Non-Self-Recognition. Vasta GR, Amzel LM, Bianchet MA, Cammarata M, Feng C, Saito K. Front Immunol 8 1648 (2017)
  29. Structure determination of membrane-associated proteins from nuclear magnetic resonance data. Baleja JD. Anal Biochem 288 1-15 (2001)
  30. The role of phosphatidylserine on the membrane in immunity and blood coagulation. Wang J, Yu C, Zhuang J, Qi W, Jiang J, Liu X, Zhao W, Cao Y, Wu H, Qi J, Zhao RC. Biomark Res 10 4 (2022)
  31. Optimization of factor VIII replacement therapy: can structural studies help in evading antibody inhibitors? Spiegel PC, Stoddard BL. Br J Haematol 119 310-322 (2002)
  32. Blood coagulation: The outstanding hydrophobic residues. Pellequer JL, Gale AJ, Getzoff ED. Curr Biol 10 R237-40 (2000)
  33. Uncovering Membrane-Bound Models of Coagulation Factors by Combined Experimental and Computational Approaches. Ohkubo YZ, Madsen JJ. Thromb Haemost 121 1122-1137 (2021)

Articles citing this publication (91)

  1. Identification of mouse sperm SED1, a bimotif EGF repeat and discoidin-domain protein involved in sperm-egg binding. Ensslin MA, Shur BD. Cell 114 405-417 (2003)
  2. The tertiary structure and domain organization of coagulation factor VIII. Shen BW, Spiegel PC, Chang CH, Huh JW, Lee JS, Kim J, Kim YH, Stoddard BL. Blood 111 1240-1247 (2008)
  3. Crystal structure and biochemical analyses reveal Beclin 1 as a novel membrane binding protein. Huang W, Choi W, Hu W, Mi N, Guo Q, Ma M, Liu M, Tian Y, Lu P, Wang FL, Deng H, Liu L, Gao N, Yu L, Shi Y. Cell Res 22 473-489 (2012)
  4. Structural studies of neuropilin/antibody complexes provide insights into semaphorin and VEGF binding. Appleton BA, Wu P, Maloney J, Yin J, Liang WC, Stawicki S, Mortara K, Bowman KK, Elliott JM, Desmarais W, Bazan JF, Bagri A, Tessier-Lavigne M, Koch AW, Wu Y, Watts RJ, Wiesmann C. EMBO J 26 4902-4912 (2007)
  5. A study of the membrane-water interface region of membrane proteins. Granseth E, von Heijne G, Elofsson A. J Mol Biol 346 377-385 (2005)
  6. Secretion of a peripheral membrane protein, MFG-E8, as a complex with membrane vesicles. Oshima K, Aoki N, Kato T, Kitajima K, Matsuda T. Eur J Biochem 269 1209-1218 (2002)
  7. The crystal structure of activated protein C-inactivated bovine factor Va: Implications for cofactor function. Adams TE, Hockin MF, Mann KG, Everse SJ. Proc Natl Acad Sci U S A 101 8918-8923 (2004)
  8. Retinoschisin (RS1), the protein encoded by the X-linked retinoschisis gene, is anchored to the surface of retinal photoreceptor and bipolar cells through its interactions with a Na/K ATPase-SARM1 complex. Molday LL, Wu WW, Molday RS. J Biol Chem 282 32792-32801 (2007)
  9. Expression of developmental endothelial locus-1 in a subset of macrophages for engulfment of apoptotic cells. Hanayama R, Tanaka M, Miwa K, Nagata S. J Immunol 172 3876-3882 (2004)
  10. The C2B domain of synaptotagmin is a Ca(2+)-sensing module essential for exocytosis. Desai RC, Vyas B, Earles CA, Littleton JT, Kowalchyck JA, Martin TF, Chapman ER. J Cell Biol 150 1125-1136 (2000)
  11. Defective discoidin domain structure, subunit assembly, and endoplasmic reticulum processing of retinoschisin are primary mechanisms responsible for X-linked retinoschisis. Wu WW, Molday RS. J Biol Chem 278 28139-28146 (2003)
  12. Sorting of GPI-anchored proteins into ER exit sites by p24 proteins is dependent on remodeled GPI. Fujita M, Watanabe R, Jaensch N, Romanova-Michaelides M, Satoh T, Kato M, Riezman H, Yamaguchi Y, Maeda Y, Kinoshita T. J Cell Biol 194 61-75 (2011)
  13. Crystal structure of an ATPase-active form of Rad51 homolog from Methanococcus voltae. Insights into potassium dependence. Wu Y, Qian X, He Y, Moya IA, Luo Y. J Biol Chem 280 722-728 (2005)
  14. Caspr3 and caspr4, two novel members of the caspr family are expressed in the nervous system and interact with PDZ domains. Spiegel I, Salomon D, Erne B, Schaeren-Wiemers N, Peles E. Mol Cell Neurosci 20 283-297 (2002)
  15. Crystal structure of lactadherin C2 domain at 1.7A resolution with mutational and computational analyses of its membrane-binding motif. Shao C, Novakovic VA, Head JF, Seaton BA, Gilbert GE. J Biol Chem 283 7230-7241 (2008)
  16. Crystal structure of vesicular stomatitis virus matrix protein. Gaudier M, Gaudin Y, Knossow M. EMBO J 21 2886-2892 (2002)
  17. Structural basis of the collagen-binding mode of discoidin domain receptor 2. Ichikawa O, Osawa M, Nishida N, Goshima N, Nomura N, Shimada I. EMBO J 26 4168-4176 (2007)
  18. Molecular pathology of X linked retinoschisis: mutations interfere with retinoschisin secretion and oligomerisation. Wang T, Zhou A, Waters CT, O'Connor E, Read RJ, Trump D. Br J Ophthalmol 90 81-86 (2006)
  19. Crystal structure of the human neuropilin-1 b1 domain. Lee CC, Kreusch A, McMullan D, Ng K, Spraggon G. Structure 11 99-108 (2003)
  20. The crystal structure of D-lactate dehydrogenase, a peripheral membrane respiratory enzyme. Dym O, Pratt EA, Ho C, Eisenberg D. Proc Natl Acad Sci U S A 97 9413-9418 (2000)
  21. PHOSPHATIDYLSERINE SYNTHASE1 is required for microspore development in Arabidopsis thaliana. Yamaoka Y, Yu Y, Mizoi J, Fujiki Y, Saito K, Nishijima M, Lee Y, Nishida I. Plant J 67 648-661 (2011)
  22. Distinct structural and adhesive roles of Ca2+ in membrane binding of blood coagulation factors. Ohkubo YZ, Tajkhorshid E. Structure 16 72-81 (2008)
  23. Phosphotidylserine exposure and neutrophil extracellular traps enhance procoagulant activity in patients with inflammatory bowel disease. He Z, Si Y, Jiang T, Ma R, Zhang Y, Cao M, Li T, Yao Z, Zhao L, Fang S, Yu B, Dong Z, Thatte HS, Bi Y, Kou J, Yang S, Piao D, Hao L, Zhou J, Shi J. Thromb Haemost 115 738-751 (2016)
  24. Exploring the collagen-binding site of the DDR1 tyrosine kinase receptor. Abdulhussein R, McFadden C, Fuentes-Prior P, Vogel WF. J Biol Chem 279 31462-31470 (2004)
  25. Characterization of a binary tandem domain F-type lectin from striped bass (Morone saxatilis). Odom EW, Vasta GR. J Biol Chem 281 1698-1713 (2006)
  26. A membrane-interactive surface on the factor VIII C1 domain cooperates with the C2 domain for cofactor function. Lü J, Pipe SW, Miao H, Jacquemin M, Gilbert GE. Blood 117 3181-3189 (2011)
  27. Discoidin domain of Del1 protein contributes to its deposition in the extracellular matrix. Hidai C, Kawana M, Kitano H, Kokubun S. Cell Tissue Res 330 83-95 (2007)
  28. Interdomain engineered disulfide bond permitting elucidation of mechanisms of inactivation of coagulation factor Va by activated protein C. Gale AJ, Xu X, Pellequer JL, Getzoff ED, Griffin JH. Protein Sci 11 2091-2101 (2002)
  29. Implications for the ubiquitination reaction of the anaphase-promoting complex from the crystal structure of the Doc1/Apc10 subunit. Au SW, Leng X, Harper JW, Barford D. J Mol Biol 316 955-968 (2002)
  30. Weaning-induced expression of a milk-fat globule protein, MFG-E8, in mouse mammary glands, as demonstrated by the analyses of its mRNA, protein and phosphatidylserine-binding activity. Nakatani H, Aoki N, Nakagawa Y, Jin-No S, Aoyama K, Oshima K, Ohira S, Sato C, Nadano D, Matsuda T. Biochem J 395 21-30 (2006)
  31. A phosphatidylserine binding site in factor Va C1 domain regulates both assembly and activity of the prothrombinase complex. Majumder R, Quinn-Allen MA, Kane WH, Lentz BR. Blood 112 2795-2802 (2008)
  32. Factor VIII C1 domain spikes 2092-2093 and 2158-2159 comprise regions that modulate cofactor function and cellular uptake. Bloem E, van den Biggelaar M, Wroblewska A, Voorberg J, Faber JH, Kjalke M, Stennicke HR, Mertens K, Meijer AB. J Biol Chem 288 29670-29679 (2013)
  33. Paired octamer rings of retinoschisin suggest a junctional model for cell-cell adhesion in the retina. Tolun G, Vijayasarathy C, Huang R, Zeng Y, Li Y, Steven AC, Sieving PA, Heymann JB. Proc Natl Acad Sci U S A 113 5287-5292 (2016)
  34. The cation-π box is a specific phosphatidylcholine membrane targeting motif. Cheng J, Goldstein R, Gershenson A, Stec B, Roberts MF. J Biol Chem 288 14863-14873 (2013)
  35. Discovery of novel membrane binding structures and functions. Kufareva I, Lenoir M, Dancea F, Sridhar P, Raush E, Bissig C, Gruenberg J, Abagyan R, Overduin M. Biochem Cell Biol 92 555-563 (2014)
  36. Membrane-binding properties of the Factor VIII C2 domain. Novakovic VA, Cullinan DB, Wakabayashi H, Fay PJ, Baleja JD, Gilbert GE. Biochem J 435 187-196 (2011)
  37. Oligomeric lipoprotein PelC guides Pel polysaccharide export across the outer membrane of Pseudomonas aeruginosa. Marmont LS, Rich JD, Whitney JC, Whitfield GB, Almblad H, Robinson H, Parsek MR, Harrison JJ, Howell PL. Proc Natl Acad Sci U S A 114 2892-2897 (2017)
  38. Effects of pathological mutations on the stability of a conserved amino acid triad in retinoschisin. Fraternali F, Cavallo L, Musco G. FEBS Lett 544 21-26 (2003)
  39. Novel FV mutation (W1920R, FVNara) associated with serious deep vein thrombosis and more potent APC resistance relative to FVLeiden. Nogami K, Shinozawa K, Ogiwara K, Matsumoto T, Amano K, Fukutake K, Shima M. Blood 123 2420-2428 (2014)
  40. Thirty-four novel mutations detected in factor VIII gene by multiplex CSGE: modeling of 13 novel amino acid substitutions. Habart D, Kalabova D, Novotny M, Vorlova Z. J Thromb Haemost 1 773-781 (2003)
  41. Computational modeling of laminin N-terminal domains using sparse distance constraints from disulfide bonds and chemical cross-linking. Kalkhof S, Haehn S, Paulsson M, Smyth N, Meiler J, Sinz A. Proteins 78 3409-3427 (2010)
  42. Discoidin I from Dictyostelium discoideum and Interactions with oligosaccharides: specificity, affinity, crystal structures, and comparison with discoidin II. Mathieu SV, Aragão KS, Imberty A, Varrot A. J Mol Biol 400 540-554 (2010)
  43. Molecular modeling indicates distinct classes of missense variants with mild and severe XLRS phenotypes. Sergeev YV, Vitale S, Sieving PA, Vincent A, Robson AG, Moore AT, Webster AR, Holder GE. Hum Mol Genet 22 4756-4767 (2013)
  44. Combined homology modelling and evolutionary significance evaluation of missense mutations in blood clotting factor VIII to highlight aspects of structure and function. Markoff A, Gerke V, Bogdanova N. Haemophilia 15 932-941 (2009)
  45. Defining the structure of membrane-bound human blood coagulation factor Va. Stoilova-McPhie S, Parmenter CD, Segers K, Villoutreix BO, Nicolaes GA. J Thromb Haemost 6 76-82 (2008)
  46. Mutation of hydrophobic residues in the factor Va C1 and C2 domains blocks membrane-dependent prothrombin activation. Peng W, Quinn-Allen MA, Kane WH. J Thromb Haemost 3 351-354 (2005)
  47. Structure determination of Discoidin II from Dictyostelium discoideum and carbohydrate binding properties of the lectin domain. Aragão KS, Satre M, Imberty A, Varrot A. Proteins 73 43-52 (2008)
  48. A novel role for SED1 (MFG-E8) in maintaining the integrity of the epididymal epithelium. Raymond AS, Shur BD. J Cell Sci 122 849-858 (2009)
  49. Modulation of factor V levels in plasma by polymorphisms in the C2 domain. Scanavini D, Girelli D, Lunghi B, Martinelli N, Legnani C, Pinotti M, Palareti G, Bernardi F. Arterioscler Thromb Vasc Biol 24 200-206 (2004)
  50. Proposed structural models of human factor Va and prothrombinase. Lee CJ, Lin P, Chandrasekaran V, Duke RE, Everse SJ, Perera L, Pedersen LG. J Thromb Haemost 6 83-89 (2008)
  51. Characterization and purification of the discoidin domain-containing protein retinoschisin and its interaction with galactose. Dyka FM, Wu WW, Pfeifer TA, Molday LL, Grigliatti TA, Molday RS. Biochemistry 47 9098-9106 (2008)
  52. Severe factor V deficiency: exon skipping in the factor V gene causing a partial deletion of the C1 domain. Asselta R, Montefusco MC, Duga S, Malcovati M, Peyvandi F, Mannucci PM, Tenchini ML. J Thromb Haemost 1 1237-1244 (2003)
  53. Rational design of small molecules targeting the C2 domain of coagulation factor VIII. Nicolaes GA, Kulharia M, Voorberg J, Kaijen PH, Wroblewska A, Wielders S, Schrijver R, Sperandio O, Villoutreix BO. Blood 123 113-120 (2014)
  54. Factor 5 mutation profile in German patients with homozygous and heterozygous factor V deficiency. Delev D, Pavlova A, Heinz S, Seifried E, Oldenburg J. Haemophilia 15 1143-1153 (2009)
  55. Membrane Interaction of the Factor VIIIa Discoidin Domains in Atomistic Detail. Madsen JJ, Ohkubo YZ, Peters GH, Faber JH, Tajkhorshid E, Olsen OH. Biochemistry 54 6123-6131 (2015)
  56. NMR solution structure of C2 domain of MFG-E8 and insights into its molecular recognition with phosphatidylserine. Ye H, Li B, Subramanian V, Choi BH, Liang Y, Harikishore A, Chakraborty G, Baek K, Yoon HS. Biochim Biophys Acta 1828 1083-1093 (2013)
  57. Screening Outside the Catalytic Site: Inhibition of Macromolecular Inter-actions Through Structure-Based Virtual Ligand Screening Experiments. Sperandio O, Miteva MA, Segers K, Nicolaes GA, Villoutreix BO. Open Biochem J 2 29-37 (2008)
  58. Dynamics of nitric oxide controlled by protein complex in bacterial system. Terasaka E, Yamada K, Wang PH, Hosokawa K, Yamagiwa R, Matsumoto K, Ishii S, Mori T, Yagi K, Sawai H, Arai H, Sugimoto H, Sugita Y, Shiro Y, Tosha T. Proc Natl Acad Sci U S A 114 9888-9893 (2017)
  59. Identification of 31 novel mutations in the F8 gene in Spanish hemophilia A patients: structural analysis of 20 missense mutations suggests new intermolecular binding sites. Venceslá A, Corral-Rodríguez MA, Baena M, Cornet M, Domènech M, Baiget M, Fuentes-Prior P, Tizzano EF. Blood 111 3468-3478 (2008)
  60. Loss of SED1/MFG-E8 results in altered luminal physiology in the epididymis. Raymond AS, Elder B, Ensslin M, Shur BD. Mol Reprod Dev 77 550-563 (2010)
  61. Bacillus thuringiensis Cry toxins bound specifically to various proteins via domain III, which had a galactose-binding domain-like fold. Kitami M, Kadotani T, Nakanishi K, Atsumi S, Higurashi S, Ishizaka T, Watanabe A, Sato R. Biosci Biotechnol Biochem 75 305-312 (2011)
  62. Phylogenetic analysis and homology modelling of Paracentrotus lividus nectin. Costa C, Cavalcante C, Zito F, Yokota Y, Matranga V. Mol Divers 14 653-665 (2010)
  63. Identification of three F5 gene mutations associated with inherited coagulation factor V deficiency in two Chinese pedigrees. Fu QH, Zhou RF, Liu LG, Wang WB, Wu WM, Ding QL, Hu YQ, Wang XF, Wang ZY, Wang HL. Haemophilia 10 264-270 (2004)
  64. Cog-Wheel Octameric Structure of RS1, the Discoidin Domain Containing Retinal Protein Associated with X-Linked Retinoschisis. Bush M, Setiaputra D, Yip CK, Molday RS. PLoS One 11 e0147653 (2016)
  65. Factor Va alternative conformation reconstruction using atomic force microscopy. Chaves RC, Dahmane S, Odorico M, Nicolaes GA, Pellequer JL. Thromb Haemost 112 1167-1173 (2014)
  66. Interactions of the C2 domain of human factor V with a model membrane. Mollica L, Fraternali F, Musco G. Proteins 64 363-375 (2006)
  67. Binding of factor VIII inhibitors to discrete regions of the factor VIII C2 domain disrupt phospholipid binding. Lewis DA, Moore KD, Ortel TL. Blood Coagul Fibrinolysis 14 361-368 (2003)
  68. Functional analysis of conserved aromatic amino acids in the discoidin domain of Paenibacillus beta-1,3-glucanase. Cheng YM, Hsieh FC, Meng M. Microb Cell Fact 8 62 (2009)
  69. Phosphoinositide-binding proteins mark, shape and functionally modulate highly-diverged endocytic compartments in the parasitic protist Giardia lamblia. Cernikova L, Faso C, Hehl AB. PLoS Pathog 16 e1008317 (2020)
  70. Changes in the Factor VIII C2 domain upon membrane binding determined by hydrogen-deuterium exchange MS. Pantazatos D, Gessner CR, Woods VL, Gilbert GE. Biochem J 461 443-451 (2014)
  71. Controllable engineering of asymmetric phosphatidylserine-containing lipid vesicles using calcium cations. Sun HY, Deng G, Jiang YW, Zhou Y, Xu J, Wu FG, Yu ZW. Chem Commun (Camb) 53 12762-12765 (2017)
  72. Differential contributions of Glu96, Asp102 and Asp111 to coagulation factor V/Va metal ion binding and subunit stability. Song J, Talbot K, Hewitt J, MacGillivray RT, Pryzdial EL. Biochem J 422 257-264 (2009)
  73. Modeling and functional analysis of AEBP1, a transcriptional repressor. Lyons PJ, Mattatall NR, Ro HS. Proteins 63 1069-1083 (2006)
  74. Molecular cloning and expression analysis of a F-type lectin gene from Japanese sea perch (Lateolabrax japonicus). Qiu L, Lin L, Yang K, Zhang H, Li J, Zou F, Jiang S. Mol Biol Rep 38 3751-3756 (2011)
  75. Factor V C2 domain contains a major thrombin-binding site responsible for thrombin-catalyzed factor V activation. Suzuki H, Shima M, Nogami K, Sakurai Y, Nishiya K, Saenko EL, Tanaka I, Yoshioka A. J Thromb Haemost 4 1354-1360 (2006)
  76. Adhesion activity of fetal gonadal cells to EGF and discoidin domains of milk fat globule-EGF factor 8 (MFG-E8), a secreted integrin-binding protein which is transiently expressed in mouse early gonadogenesis. Ishii M, Kanai Y, Kanai-Azuma M, Tajima Y, Wei TT, Kidokoro T, Sanai Y, Kurohmaru M, Hayashi Y. Anat Embryol (Berl) 209 485-494 (2005)
  77. Coagulation function and mechanisms in various clinical phenotypes of patients with acquired factor V inhibitors. Matsumoto T, Nogami K, Shima M. J Thromb Haemost 12 1503-1512 (2014)
  78. Letter The discovery of Mary's mutation. Asselta R, Tenchini ML, Holme R, Brosstad F, Stormorken H. J Thromb Haemost 1 397-398 (2003)
  79. Location of the multimerin 1 binding site in coagulation factor V: an update. Jeimy SB, Quinn-Allen MA, Fuller N, Kane WH, Hayward CP. Thromb Res 123 352-354 (2008)
  80. Structure of the monotopic membrane protein (S)-mandelate dehydrogenase at 2.2 Å resolution. Sukumar N, Liu S, Li W, Mathews FS, Mitra B, Kandavelu P. Biochimie 154 45-54 (2018)
  81. The roles of factor Va and protein S in formation of the activated protein C/protein S/factor Va inactivation complex. Gierula M, Salles-Crawley II, Santamaria S, Teraz-Orosz A, Crawley JTB, Crawley JTB, Lane DA, Ahnström J. J Thromb Haemost 17 2056-2068 (2019)
  82. A novel in-frame deletion in the factor V C1 domain associated with severe coagulation factor V deficiency in a Korean family. Song J, Guella I, Kwon KY, Cho H, Park R, Asselta R, Choi JR. Blood Coagul Fibrinolysis 20 150-156 (2009)
  83. Aggregation of maternal pigment granules is induced by the cytosolic discoidin domain of the Xenopus Del1 protein. Tsabar N, Gefen A, Elias S, Frank D. Dev Dyn 233 224-232 (2005)
  84. Cryo-EM structure of the prothrombin-prothrombinase complex. Ruben EA, Summers B, Rau MJ, Fitzpatrick JAJ, Di Cera E. Blood 139 3463-3473 (2022)
  85. Functional characterization of a novel missense mutation identified in a Turkish patient affected by severe coagulation factor V deficiency. Paraboschi EM, Kayiran SM, Özbek N, Gürakan B, Peyvandi F, Guella I, Duga S, Asselta R. Haemophilia 18 205-210 (2012)
  86. Generation of an anticoagulant aptamer that targets factor V/Va and disrupts the FVa-membrane interaction in normal and COVID-19 patient samples. Soule EE, Yu H, Olson L, Naqvi I, Kumar S, Krishnaswamy S, Sullenger BA. Cell Chem Biol 29 215-225.e5 (2022)
  87. In silico investigation of the disease-associated retinoschisin C110Y and C219G mutants. Wu JW, Liu HL. J Biomol Struct Dyn 29 937-959 (2012)
  88. Cryo-EM structure of coagulation factor V short. Mohammed BM, Pelc LA, Rau MJ, Di Cera E. Blood 141 3215-3225 (2023)
  89. Dissecting peripheral protein-membrane interfaces. Tubiana T, Sillitoe I, Orengo C, Reuter N. PLoS Comput Biol 18 e1010346 (2022)
  90. Membrane curvature and PS localize coagulation proteins to filopodia and retraction fibers of endothelial cells. Carman CV, Nikova DN, Sakurai Y, Shi J, Novakovic VA, Rasmussen JT, Lam WA, Gilbert GE. Blood Adv 7 60-72 (2023)
  91. Stable binding to phosphatidylserine-containing membranes requires conserved arginine residues in tandem C domains of blood coagulation factor VIII. Peters SC, Childers KC, Mitchell CE, Avery NG, Reese SS, Mitchell C, Wo SW, Swanson CD, Brison CM, Spiegel PC. Front Mol Biosci 9 1040106 (2022)


Quick links