Histidine-mediated pH-sensitive regulation of m-ficolin:GlcNAc binding activity in innate immunity examined by molecular dynamics simulations

PLoS ONE

Volumn 6, Issue 5, 2011, Pages

  Yang, Lifeng ^a,b   Zhang, Jing ^b   Ho, Bow ^c   Ding, Jeak Ling ^a,b  

^a SINGAPORE MIT ALLIANCE   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

FICOLIN; HISTIDINE; N ACETYLGLUCOSAMINE; LECTIN; MUTANT PROTEIN; PEPTIDE; PROTON; SOLVENT;

APOPTOSIS; ARTICLE; BINDING SITE; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME BINDING; ENZYME CONFORMATION; HYDROGEN BOND; HYDROPHOBICITY; IMMUNODETECTION; IMMUNOSURVEILLANCE; INNATE IMMUNITY; ISOMERIZATION; MOLECULAR DYNAMICS; PH; PROTON TRANSPORT; SIMULATION; CHEMISTRY; IMMUNOLOGY; ISOMERISM; METABOLISM; PROTEIN BINDING; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE;

ACETYLGLUCOSAMINE; HISTIDINE; HYDROGEN BONDING; HYDROGEN-ION CONCENTRATION; IMMUNITY, INNATE; ISOMERISM; LECTINS; MOLECULAR DYNAMICS SIMULATION; MUTANT PROTEINS; PEPTIDES; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PROTONS; SOLVENTS;

EID: 79955802579     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0019647     Document Type: Article

References (55)

1. Fujita T, (2002) Evolution of the lectin-complement pathway and its role in innate immunity. Nat Rev Immunol 2: 346-353.
2. Fujita T, Matsushita M, Endo Y, (2004) The lectin-complement pathway; its role in innate immunity and evolution. Immunol Rev 198: 185-202.
3. Runza VL, Schwaeble W, Männel DN, (2008) Ficolins: Novel pattern recognition molecules of the innate immune response. Immunobiology 213: 297-306.
4. Teh C, Le Y, Lee SH, Lu J, (2000) M-ficolin is expressed on monocytes and is a lectin binding to N-acetyl-D-glucosamine and mediates monocyte adhesion and phagocytosis of Escherichia coli. Immunology 101: 225-232.
5. Misao Matsushita TF, (2001) Ficolins and the lectin complement pathway. Immunological Reviews 180: 78-85.
6. Garlatti V, Martin L, Gout E, Reiser JB, Fujita T, et al. (2007) Structural basis for innate immune sensing by M-ficolin and its control by a pH-dependent conformational switch. J Biol Chem 282: 35814-35820.
7. Sugimoto R, Yae Y, Akaiwa M, Kitajima S, Shibata Y, et al. (1998) Cloning and characterization of the Hakata antigen, a member of the ficolin/opsonin p35 lectin family. J Biol Chem 273: 20721-20727.
8. Ma YG, Cho MY, Zhao M, Park JW, Matsushita M, et al. (2004) Human mannose-binding lectin and L-ficolin function as specific pattern recognition proteins in the lectin activation pathway of complement. J Biol Chem 279: 25307-25312.
9. Krarup A, Thiel S, Hansen A, Fujita T, Jensenius JC, (2004) L-ficolin is a pattern recognition molecule specific for acetyl groups. J Biol Chem 279: 47513-47519.
10. Krarup A, Sorensen UB, Matsushita M, Jensenius JC, Thiel S, (2005) Effect of capsulation of opportunistic pathogenic bacteria on binding of the pattern recognition molecules mannan-binding lectin, L-ficolin, and H-ficolin. Infect Immun 73: 1052-1060.
11. Endo Y, Sato Y, Matsushita M, Fujita T, (1996) Cloning and characterization of the human lectin P35 gene and its related gene. Genomics 36: 515-521.
12. Zhang J, Yang L, Ang Z, Yoong SL, Tran TTT, et al. (2010) Secreted M-ficolin Anchors onto Monocyte Transmembrane GPCR43 and Crosstalks with Plasma CRP to Mediate Immune Signaling and Regulate Host Defense. J Immunol 185: 6899-6910.
13. Honore C, Rorvig S, Munthe-Fog L, Hummelshoj T, Madsen HO, et al. (2008) The innate pattern recognition molecule Ficolin-1 is secreted by monocytes/macrophages and is circulating in human plasma. Mol Immunol 45: 2782-2789.
14. Wittenborn T, Thiel S, Jensen L, Nielsen HJ, Jensenius JC, (2010) Characteristics and biological variations of M-ficolin, a pattern recognition molecule, in plasma. J Innate Immun 2: 167-180.
15. Thiel S, (2007) Complement activating soluble pattern recognition molecules with collagen-like regions, mannan-binding lectin, ficolins and associated proteins. Mol Immunol 44: 3875-3888.
16. Endo Y, Matsushita M, Fujita T, (2007) Role of ficolin in innate immunity and its molecular basis. Immunobiology 212: 371-379.
17. Lynch NJ, Roscher S, Hartung T, Morath S, Matsushita M, et al. (2004) L-ficolin specifically binds to lipoteichoic acid, a cell wall constituent of Gram-positive bacteria, and activates the lectin pathway of complement. J Immunol 172: 1198-1202.
18. Liu Y, Endo Y, Iwaki D, Nakata M, Matsushita M, et al. (2005) Human M-ficolin is a secretory protein that activates the lectin complement pathway. J Immunol 175: 3150-3156.
19. Marnell L, Mold C, Du Clos TW, (2005) C-reactive protein: ligands, receptors and role in inflammation. Clin Immunol 117: 104-111.
20. Zhang J, Koh J, Lu J, Thiel S, Leong BSH, et al. (2009) Local inflammation induces complement crosstalk which amplifies the antimicrobial response. PLoS Pathogens 5: 1-15.
21. Ng PM, Le Saux A, Lee CM, Tan NS, Lu J, et al. (2007) C-reactive protein collaborates with plasma lectins to boost immune response against bacteria. EMBO J 26: 3431-3440.
22. Liu B, Zhang J, Tan PY, Hsu D, Blom AM, et al. (2011) A Computational and Experimental Study of the Regulatory Mechanisms of the Complement System. PLoS Comput Biol 7: 1-16.
23. Tanio M, Kondo S, Sugio S, Kohno T, (2007) Trivalent recognition unit of innate immunity system: crystal structure of trimeric human M-ficolin fibrinogen-like domain. J Biol Chem 282: 3889-3895.
24. Tanio M, Kondo S, Sugio S, Kohno T, (2006) Overexpression, purification and preliminary crystallographic analysis of human M-ficolin fibrinogen-like domain. Acta Crystallographica Section F 62: 652-655.
25. Tanio M, Kondo S, Sugio S, Kohno T, (2008) Trimeric structure and conformational equilibrium of M-ficolin fibrinogen-like domain. J Synchrotron Radiat 15: 243-245.
26. Garlatti V, Belloy N, Martin L, Lacroix M, Matsushita M, et al. (2007) Structural insights into the innate immune recognition specificities of L- and H-ficolins. EMBO J 26: 623-633.
27. Gout E, Garlatti V, Smith DF, Lacroix M, Dumestre-Perard C, et al. (2010) Carbohydrate recognition properties of human ficolins: glycan array screening reveals the sialic acid binding specificity of M-ficolin. J Biol Chem 285: 6612-6622.
28. Tanio M, Kohno T, (2009) Histidine-regulated activity of M-ficolin. Biochem J 417: 485-491.
29. Baptista AM, Teixeira VH, Soares CM, (2002) Constant-pH molecular dynamics using stochastic titration. J Chem Phys 117: 4184-4200.
30. Mongan J, Case DA, McCammon JA, (2004) Constant pH molecular dynamics in generalized Born implicit solvent. Journal of Computational Chemistry 25: 2038-2048.
31. Kyte J, (1995) Structure in protein chemistry. New York & London Garland Publishing.
32. Chen Y, Chen X, Deng Y, (2007) Simulating botulinum neurotoxin with constant pH molecular dynamics in Generalized Born implicit solvent. Computer Physics Communications 177: 210.
33. Case DA, Darden TA, T.E. Cheatham I, Simmerling CL, Wang J, et al. (2008) AMBER 10. San Francisco University of California.
34. Woods G, (2005) GLYCAM Web. Complex Carbohydrate Research Center Athens, GA University of Georgia.
35. Baptista AM, Martel PJ, Petersen SB, (1997) Simulation of protein conformational freedom as a function of pH: constant-pH molecular dynamics using implicit titration. Proteins 27: 523-544.
36. Börjesson U, Hünenberger PH, (2001) Explicit-solvent molecular dynamics simulation at constant pH: Methodology and application to small amines. J Chem Phys 114: 9706-9719.
37. Baptista AM, (2002) Comment on "Explicit-solvent molecular dynamics simulation at constant pH: Methodology and application to small amines". J Chem Phys 116: 7766-7768.
38. Burgi R, Kollman PA, Van Gunsteren WF, (2002) Simulating proteins at constant pH: An approach combining molecular dynamics and Monte Carlo simulation. Proteins 47: 469-480.
39. Börjesson U, Hünenberger PH, (2004) pH-Dependent Stability of a Decalysine α-Helix Studied by Explicit-Solvent Molecular Dynamics Simulations at Constant pH. J Phys Chem B 108: 13551-13559.
40. Dlugosz M, Antosiewicz JM, (2004) Constant-pH molecular dynamics simulations: a test case of succinic acid. Chemical Physics 302: 161-170.
41. Długosz M, Antosiewicz JM, Robertson AD, (2004) Constant-pH molecular dynamics study of protonation-structure relationship in a heptapeptide derived from ovomucoid third domain. Phys Rev E 69: 021915.
42. Mongan J, Case DA, (2005) Biomolecular simulations at constant pH. Current Opinion in Structural Biology 15: 157-163.
43. Machuqueiro M, Baptista AM, (2006) Constant-pH molecular dynamics with ionic strength effects: protonation-conformation coupling in decalysine. J Phys Chem B 110: 2927-2933.
44. Machuqueiro M, Baptista AM, (2007) The pH-dependent conformational states of kyotorphin: a constant-pH molecular dynamics study. Biophys J 92: 1836-1845.
45. Srivastava J, Barber DL, Jacobson MP, (2007) Intracellular pH sensors: design principles and functional significance. Physiology (Bethesda) 22: 30-39.
46. Chen J, Brooks CL, Khandogin J, (2008) Recent advances in implicit solvent-based methods for biomolecular simulations. Curr Opin Struct Biol 18: 140-148.
47. Machuqueiro M, Baptista AM, (2008) Acidic range titration of HEWL using a constant-pH molecular dynamics method. Proteins 72: 289-298.
48. Srivastava J, Barreiro G, Groscurth S, Gingras AR, Goult BT, et al. (2008) Structural model and functional significance of pH-dependent talin-actin binding for focal adhesion remodeling. Proc Natl Acad Sci U S A 105: 14436-14441.
49. Tjong H, Zhou HX, (2008) Prediction of protein solubility from calculation of transfer free energy. Biophys J 95: 2601-2609.
50. Machuqueiro M, Baptista AM, (2009) Molecular dynamics at constant pH and reduction potential: application to cytochrome c3. J Am Chem Soc 131: 12586-12594.
51. Swails JM, Meng Y, Walker FA, Marti MA, Estrin DA, et al. (2009) pH-dependent mechanism of nitric oxide release in nitrophorins 2 and 4. J Phys Chem B 113: 1192-1201.
52. Machuqueiro M, Campos SR, Soares CM, Baptista AM, (2010) Membrane-induced conformational changes of kyotorphin revealed by molecular dynamics simulations. J Phys Chem B 114: 11659-11667.
53. Meng Y, Roitberg AE, (2010) Constant pH Replica Exchange Molecular Dynamics in Biomolecules Using a Discrete Protonation Model. J Chem Theory Comput 6: 1401-1412.
54. Campos SRR, Machuqueiro M, Baptista AM, (2010) Constant-pH Molecular Dynamics Simulations Reveal a β-Rich Form of the Human Prion Protein. Journal of Physical Chemistry B 114: 12692-12700.
55. Khandogin J, Brooks CL, (2005) Constant pH molecular dynamics with proton tautomerism. Biophys J 89: 141-157.