Polyproline and triple helix motifs in Host-Pathogen recognition

Current Protein and Peptide Science

Volumn 13, Issue 8, 2012, Pages 855-865

  Berisio, Rita ^a   Vitagliano, Luigi ^a  

^a CNR   (Italy)

Author keywords

Collagen; Host pathogen interaction; Triple helix

Indexed keywords

BACTERIAL PROTEIN; CHAPERONE; COLLAGEN; HEAT SHOCK PROTEIN 47; INTERSTITIAL COLLAGENASE; OSTEONECTIN; VON WILLEBRAND FACTOR;

CRYSTAL STRUCTURE; HOST PATHOGEN INTERACTION; HUMAN; MOLECULAR RECOGNITION; NONHUMAN; POLYPROLINE II HELIX MOTIF; PROTEIN DATA BANK; PROTEIN PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; REVIEW; TRIPLE HELIX;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; COLLAGEN; HOST-PATHOGEN INTERACTIONS; HUMANS; MOLECULAR SEQUENCE DATA; PEPTIDES; PROTEIN BINDING;

EID: 84874856515     PISSN: 13892037     EISSN: 18755550     Source Type: Journal    
DOI: 10.2174/138920312804871157     Document Type: Review

References (123)

1. Richardson, J.S. The anatomy and taxonomy of protein structure. Adv. Prot. Chem., 1981, 34, 167-339.
2. Kabsch, W.; Sander, C. Dictionary of protein secondary structure: Pattern recognition of hydrogen-bonded and geometrical features. Biopolymers, 1983, 22, 2577-2637.
3. Unger, R.; Sussman, J.L. The importance of short structural motifs in protein structure analysis. J. Comp.-Aid. Mol. Des., 1993, 7, 457-472.
4. Brenner, S.E.; Chothia, C.; Hubbard, T.J. Population statistics of protein structures: Lessons from structural classifications. Curr. Opin. Struct. Biol., 1997, 7, 369-376.
5. De Simone, A.; Berisio, R.; Zagari, A.; Vitagliano, L. Limited tendency of alpha-helical residues to form disulfide bridges: A structural explanation. J. Pept. Sci., 2006, 12, 740-747.
6. Adzhubei, A.A.; Sternberg, M.J. Left-handed polyproline ii helices commonly occur in globular proteins. J. Mol. Biol., 1993, 229, 472-493.
7. Stapley, B.J.; Creamer, T.P. A survey of left-handed polyproline ii helices. Prot. Sci., 1999, 8, 587-595.
8. Cubellis, M.V.; Caillez, F.; Blundell, T.L.; Lovell, S.C. Properties of polyproline ii, a secondary structure element implicated in protein-protein interactions. Proteins, 2005, 58, 880-892.
9. Berisio, R.; Loguercio, S.; De Simone, A.; Zagari, A.; Vitagliano, L. Polyproline helices in protein structures: A statistical survey. Prot. Pept. Lett., 2006, 13, 847-854.
10. Barlow, D.J.; Thornton, J.M. Helix geometry in proteins. J. Mol. Biol., 1988, 201, 601-619.
11. Richardson, J.S.; Richardson, D.C. Helix lap-joints as ion-binding sites: DNA-binding motifs and ca-binding ef hands are related by charge and sequence reversal. Proteins, 1988, 4, 229-239.
12. Okuyama, K. Revisiting the molecular structure of collagen. Connect. Tiss. Res., 2008, 49, 299-310.
13. Brodsky, B.; Persikov, A.V. Molecular structure of the collagen triple helix. Adv. Prot. Chem., 2005, 70, 301-339.
14. Shoulders, M.D.; Raines, R.T. Collagen structure and stability. Ann. Rev. Biochem., 2009, 78, 929-958.
15. Berisio, R.; Vitagliano, L.; Mazzarella, L.; Zagari, A. Recent progress on collagen triple helix structure, stability and assembly. Prot. Pept. Lett., 2002, 9, 107-116.
16. Richardson, J.S.; Richardson, D.C. Natural beta-sheet proteins use negative design to avoid edge-to-edge aggregation. Proc. Nat. Acad. Sci. USA, 2002, 99, 2754-2759.
17. De Simone, A.; Esposito, L.; Pedone, C.; Vitagliano, L. Insights into stability and toxicity of amyloid-like oligomers by replica exchange molecular dynamics analyses. Biophys. J., 2008, 95, 1965-1973.
18. Esposito, L.; Paladino, A.; Pedone, C.; Vitagliano, L. Insights into structure, stability, and toxicity of monomeric and aggregated polyglutamine models from molecular dynamics simulations. Biophys. J., 2008, 94, 4031-4040.
19. De Simone, A.; Dodson, G.G.; Fraternali, F.; Zagari, A. Water molecules as structural determinants among prions of low sequence identity. FEBS lett., 2006, 580, 2488-2494.
20. Nagai, Y.; Popiel, H.A. Conformational changes and aggregation of expanded polyglutamine proteins as therapeutic targets of the polyglutamine diseases: Exposed beta-sheet hypothesis. Curr. Pharmaceut. Des., 2008, 14, 3267-3279.
21. de Vega, M.J.; Martin-Martinez, M.; Gonzalez-Muniz, R. Modulation of protein-protein interactions by stabilizing/mimicking protein secondary structure elements. Curr. Topics Med. Chem., 2007, 7, 33-62.
22. Tsai, C.J.; Lin, S.L.; Wolfson, H.J.; Nussinov, R. Protein-protein interfaces: Architectures and interactions in protein-protein interfaces and in protein cores. Their similarities and differences. Crit. Rev. Biochem. Mol. Biol., 1996, 31, 127-152.
23. Kay, B.K.; Williamson, M.P.; Sudol, M. The importance of being proline: The interaction of proline-rich motifs in signaling proteins with their cognate domains. FASEB J., 2000, 14, 231-241.
24. Siligardi, G.; Drake, A.F. The importance of extended conformations and, in particular, the pii conformation for the molecular recognition of peptides. Biopolymers, 1995, 37, 281-292.
25. MacArthur, M.W.; Thornton, J.M. Influence of proline residues on protein conformation. J. Mol. Biol., 1991, 218, 397-412.
26. Rath, A.; Davidson, A.R.; Deber, C.M. The structure of unstructured regions in peptides and proteins: Role of the polyproline ii helix in protein folding and recognition. Biopolymers, 2005, 80, 179-185.
27. Vitagliano, L.; Berisio, R.; Mastrangelo, A.; Mazzarella, L.; Zagari, A. Preferred proline puckerings in cis and trans peptide groups: Implications for collagen stability. Prot. Sci., 2001, 10, 2627-2632.
28. Creamer, T.P.; Campbell, M.N. Determinants of the polyproline ii helix from modeling studies. Adv. Prot. Chem., 2002, 62, 263-282.
29. Shi, Z.; Woody, R.W.; Kallenbach, N.R. Is polyproline ii a major backbone conformation in unfolded proteins? Adv. Prot. Chem., 2002, 62, 163-240.
30. Shi, Z.; Olson, C.A.; Rose, G.D.; Baldwin, R.L.; Kallenbach, N.R. Polyproline ii structure in a sequence of seven alanine residues. Proc. Nat. Acad. Sci. USA., 2002, 99, 9190-9195.
31. Eker, F.; Cao, X.; Nafie, L.; Schweitzer-Stenner, R. Tripeptides adopt stable structures in water. A combined polarized visible raman, ftir, and vcd spectroscopy study. J. Am. Chem. Soc., 2002, 124, 14330-14341.
32. Avbelj, F.; Grdadolnik, S.G.; Grdadolnik, J.; Baldwin, R.L. Intrinsic backbone preferences are fully present in blocked amino acids. Proc. Nat. Acad. Sci. USA., 2006, 103, 1272-1277.
33. Zagrovic, B.; Lipfert, J.; Sorin, E.J.; Millett, I.S.; van Gunsteren, W.F.; Doniach, S.; Pande, V.S. Unusual compactness of a polyproline type ii structure. Proc. Nat. Acad. Sci. USA., 2005, 102, 11698-11703.
34. Bartlett, G.J.; Choudhary, A.; Raines, R.T.; Woolfson, D.N. N-- >pi* interactions in proteins. Nat. Chem. Biol., 2010, 6, 615-620.
35. Zafra-Ruano, A.; Luque, I. Interfacial water molecules in sh3 interactions: Getting the full picture on polyproline recognition by protein-protein interaction domains. FEBS lett., 2012, 586, 2619-2630.
36. Agrawal, V.; Kishan, K.V. Promiscuous binding nature of sh3 domains to their target proteins. Prot. Pept. Lett., 2002, 9, 185-193.
37. Srinivasan, M.; Dunker, A.K. Proline rich motifs as drug targets in immune mediated disorders. Int. J. Pept., 2012, 2012, 634769.
38. Niebuhr, K.; Ebel, F.; Frank, R.; Reinhard, M.; Domann, E.; Carl, U.D.; Walter, U.; Gertler, F.B.; Wehland, J.; Chakraborty, T. A novel proline-rich motif present in acta of listeria monocytogenes and cytoskeletal proteins is the ligand for the evh1 domain, a protein module present in the ena/vasp family. EMBO J., 1997, 16, 5433-5444.
39. Gertler, F.B.; Niebuhr, K.; Reinhard, M.; Wehland, J.; Soriano, P. Mena, a relative of vasp and drosophila enabled, is implicated in the control of microfilament dynamics. Cell, 1996, 87, 227-239.
40. Ball, L.J.; Kuhne, R.; Hoffmann, B.; Hafner, A.; Schmieder, P.; Volkmer-Engert, R.; Hof, M.; Wahl, M.; Schneider-Mergener, J.; Walter, U.; Oschkinat, H.; Jarchau, T. Dual epitope recognition by the vasp evh1 domain modulates polyproline ligand specificity and binding affinity. EMBO J., 2000, 19, 4903-4914.
41. Hunke, C.; Hirsch, T.; Eichler, J. Structure-based synthetic mimicry of discontinuous protein binding sites: Inhibitors of the interaction of mena evh1 domain with proline-rich ligands. Chembiochem, 2006, 7, 1258-1264.
42. Vermeire, J.; Vanbillemont, G.; Witkowski, W.; Verhasselt, B. The nef-infectivity enigma: Mechanisms of enhanced lentiviral infection. Curr. HIV Res., 2011, 9, 474-489.
43. Kuo, L.S.; Baugh, L.L.; Denial, S.J.; Watkins, R.L.; Liu, M.; Garcia, J.V.; Foster, J.L. Overlapping effector interfaces define the multiple functions of the hiv-1 nef polyproline helix. Retrovirology, 2012, 9, 47.
44. Hale, B.G.; Kerry, P.S.; Jackson, D.; Precious, B.L.; Gray, A.; Killip, M.J.; Randall, R.E.; Russell, R.J. Structural insights into phosphoinositide 3-kinase activation by the influenza a virus ns1 protein. Proc. Nat. Acad. Sci. USA., 2010, 107, 1954-1959.
45. Shin, Y.K.; Li, Y.; Liu, Q.; Anderson, D.H.; Babiuk, L.A.; Zhou, Y. Sh3 binding motif 1 in influenza a virus ns1 protein is essential for pi3k/akt signaling pathway activation. J. Virol., 2007, 81, 12730-12739.
46. Larson, M.R.; Rajashankar, K.R.; Patel, M.H.; Robinette, R.A.; Crowley, P.J.; Michalek, S.; Brady, L.J.; Deivanayagam, C. Elongated fibrillar structure of a streptococcal adhesin assembled by the high-affinity association of alpha- and ppii-helices. Proc. Nat. Acad. Sci. USA., 2010, 107, 5983-5988.
47. Brady, L.J.; Maddocks, S.E.; Larson, M.R.; Forsgren, N.; Persson, K.; Deivanayagam, C.C.; Jenkinson, H.F. The changing faces of streptococcus antigen i/ii polypeptide family adhesins. Mol. Microbiol., 2010, 77, 276-286.
48. Linke, C.; Young, P.G.; Kang, H.J.; Bunker, R.D.; Middleditch, M.J.; Caradoc-Davies, T.T.; Proft, T.; Baker, E.N. Crystal structure of the minor pilin fctb reveals determinants of group a streptococcal pilus anchoring. J. Biol. Chem., 2010, 285, 20381-20389.
49. Solovyova, A.S.; Pointon, J.A.; Race, P.R.; Smith, W.D.; Kehoe, M.A.; Banfield, M.J. Solution structure of the major (spy0128) and minor (spy0125 and spy0130) pili subunits from streptococcus pyogenes. Euro. Biophys. J.: EBJ., 2010, 39, 469-480.
50. Holmgren, S.K.; Taylor, K.M.; Bretscher, L.E.; Raines, R.T. Code for collagen's stability deciphered. Nature, 1998, 392, 666-667.
51. Vitagliano, L.; Berisio, R.; Mazzarella, L.; Zagari, A. Structural bases of collagen stabilization induced by proline hydroxylation. Biopolymers, 2001, 58, 459-464.
52. Berisio, R.; Granata, V.; Vitagliano, L.; Zagari, A. Imino acids and collagen triple helix stability: Characterization of collagen-like polypeptides containing hyp-hyp-gly sequence repeats. J. Am. Chem. Soc., 2004, 126, 11402-11403.
53. Doi, M.; Nishi, Y.; Uchiyama, S.; Nishiuchi, Y.; Nakazawa, T.; Ohkubo, T.; Kobayashi, Y. Characterization of collagen model peptides containing 4-fluoroproline; (4(s)-fluoroproline-pro-gly)10 forms a triple helix, but (4(r)-fluoroproline-pro-gly)10 does not. J. Am. Chem. Soc., 2003, 125, 9922-9923.
54. De Simone, A.; Vitagliano, L.; Berisio, R. Role of hydration in collagen triple helix stabilization. Biochem. Biophys. Res. Communicat., 2008, 372, 121-125.
55. Persikov, A.V.; Ramshaw, J.A.; Kirkpatrick, A.; Brodsky, B. Triple-helix propensity of hydroxyproline and fluoroproline: Comparison of host-guest and repeating tripeptide collagen models. J. Am. Chem. Soc., 2003, 125, 11500-11501.
56. Okuyama, K.; Miyama, K.; Mizuno, K.; Bachinger, H.P. Crystal structure of (gly-pro-hyp)(9): Implications for the collagen molecular model. Biopolymers, 2012, 97, 607-616.
57. Okuyama, K.; Arnott, S.; Takayanagi, M.; Kakudo, M. Crystal and molecular structure of a collagen-like polypeptide (pro-pro-gly)10. J. Mol. Biol., 1981, 152, 427-443.
58. Okuyama, K.; Xu, X.; Iguchi, M.; Noguchi, K. Revision of collagen molecular structure. Biopolymers, 2006, 84, 181-191.
59. Shoulders, M.D.; Raines, R.T. Interstrand dipole-dipole interactions can stabilize the collagen triple helix. J. Biol. Chem., 2011, 286, 22905-22912.
60. Bella, J. A new method for describing the helical conformation of collagen: Dependence of the triple helical twist on amino acid sequence. J. Struct. Biol., 2010, 170, 377-391.
61. Fields, G.B. Synthesis and biological applications of collagenmodel triple-helical peptides. Org. Biomol. Chem., 2010, 8, 1237-1258.
62. Berisio, R.; De Simone, A.; Ruggiero, A.; Improta, R.; Vitagliano, L. Role of side chains in collagen triple helix stabilization and partner recognition. J. Pept. Sci., 2009, 15, 131-140.
63. Vitagliano, L.; Nemethy, G.; Zagari, A.; Scheraga, H.A. Stabilization of the triple-helical structure of natural collagen by side-chain interactions. Biochemistry, 1993, 32, 7354-7359.
64. Improta, R.; Berisio, R.; Vitagliano, L. Contribution of dipoledipole interactions to the stability of the collagen triple helix. Prot. Sci., 2008, 17, 955-961.
65. Persikov, A.V.; Ramshaw, J.A.; Brodsky, B. Collagen model peptides: Sequence dependence of triple-helix stability. Biopolymers, 2000, 55, 436-450.
66. Fallas, J.A.; Lee, M.A.; Jalan, A.A.; Hartgerink, J.D. Rational design of single-composition abc collagen heterotrimers. J. Am. Chem. Soc., 2012, 134, 1430-1433.
67. Orgel, J.P.; Irving, T.C.; Miller, A.; Wess, T.J. Microfibrillar structure of type i collagen in situ. Proc. Nat. Acad. Sci. USA., 2006, 103, 9001-9005.
68. Okuyama, K.; Bachinger, H.P.; Mizuno, K.; Boudko, S.; Engel, J.; Berisio, R.; Vitagliano, L. Re: Microfibrillar structure of type i collagen in situ. Acta crystallographica. Section D, Biol. Crystallograph., 2009, 65, 1007-1008; author reply 1009-1010.
69. Berisio, R.; Vitagliano, L.; Mazzarella, L.; Zagari, A. Crystal structure of a collagen-like polypeptide with repeating sequence pro-hyp-gly at 1.4 a resolution: Implications for collagen hydration. Biopolymers, 2000, 56, 8-13.
70. Bella, J.; Eaton, M.; Brodsky, B.; Berman, H.M. Crystal and molecular structure of a collagen-like peptide at 1.9 a resolution. Science, 1994, 266, 75-81.
71. Kramer, R.Z.; Bella, J.; Mayville, P.; Brodsky, B.; Berman, H.M. Sequence dependent conformational variations of collagen triplehelical structure. Nat. Struct. Biol., 1999, 6, 454-457.
72. Shoulders, M.D.; Satyshur, K.A.; Forest, K.T.; Raines, R.T. Stereoelectronic and steric effects in side chains preorganize a protein main chain. Proc. Nat. Acad. Sci. USA., 2010, 107, 559-564.
73. Boudko, S.P.; Engel, J.; Okuyama, K.; Mizuno, K.; Bachinger, H.P.; Schumacher, M.A. Crystal structure of human type iii collagen gly991-gly1032 cystine knot-containing peptide shows both 7/2 and 10/3 triple helical symmetries. J. Biol. Chem., 2008, 283, 32580-32589.
74. Okuyama, K.; Miyama, K.; Morimoto, T.; Masakiyo, K.; Mizuno, K.; Bachinger, H.P. Stabilization of triple-helical structures of collagen peptides containing a hyp-thr-gly, hyp-val-gly, or hyp-sergly sequence. Biopolymers, 2011, 95, 628-640.
75. Kawahara, K.; Nishi, Y.; Nakamura, S.; Uchiyama, S.; Nishiuchi, Y.; Nakazawa, T.; Ohkubo, T.; Kobayashi, Y. Effect of hydration on the stability of the collagen-like triple-helical structure of [4(r)- hydroxyprolyl-4(r)-hydroxyprolylglycine]10. Biochemistry, 2005, 44, 15812-15822.
76. Gordon, M.K.; Hahn, R.A. Collagens. Cell Tiss. Res., 2010, 339, 247-257.
77. Leitinger, B.; Hohenester, E. Mammalian collagen receptors. Mat. Biol., 2007, 26, 146-155.
78. Gronwald, W.; Bomke, J.; Maurer, T.; Domogalla, B.; Huber, F.; Schumann, F.; Kremer, W.; Fink, F.; Rysiok, T.; Frech, M.; Kalbitzer, H.R. Structure of the leech protein saratin and characterization of its binding to collagen. J. Mol. Biol., 2008, 381, 913-927.
79. Ishikawa, Y.; Vranka, J.; Wirz, J.; Nagata, K.; Bachinger, H.P. The rough endoplasmic reticulum-resident fk506-binding protein fkbp65 is a molecular chaperone that interacts with collagens. J. Biol. Chem., 2008, 283, 31584-31590.
80. Leo, J.C.; Elovaara, H.; Brodsky, B.; Skurnik, M.; Goldman, A. The yersinia adhesin yada binds to a collagenous triple-helical conformation but without sequence specificity. Prot. Eng. Des. Select.,: PEDS., 2008, 21, 475-484.
81. Emsley, J.; Knight, C.G.; Farndale, R.W.; Barnes, M.J.; Liddington, R.C. Structural basis of collagen recognition by integrin alpha2beta1. Cell, 2000, 101, 47-56.
82. Zong, Y.; Xu, Y.; Liang, X.; Keene, D.R.; Hook, A.; Gurusiddappa, S.; Hook, M.; Narayana, S.V. A 'collagen hug' model for staphylococcus aureus cna binding to collagen. EMBO J., 2005, 24, 4224-4236.
83. Hohenester, E.; Sasaki, T.; Giudici, C.; Farndale, R.W.; Bachinger, H.P. Structural basis of sequence-specific collagen recognition by sparc. Proc. Nat. Acad. Sci. USA., 2008, 105, 18273-18277.
84. Carafoli, F.; Bihan, D.; Stathopoulos, S.; Konitsiotis, A.D.; Kvansakul, M.; Farndale, R.W.; Leitinger, B.; Hohenester, E. Crystallographic insight into collagen recognition by discoidin domain receptor 2. Structure, 2009, 17, 1573-1581.
85. Gingras, A.R.; Girija, U.V.; Keeble, A.H.; Panchal, R.; Mitchell, D.A.; Moody, P.C.; Wallis, R. Structural basis of mannan-binding lectin recognition by its associated serine protease masp-1: Implications for complement activation. Structure, 2011, 19, 1635-1643.
86. Brondijk, T.H.; Bihan, D.; Farndale, R.W.; Huizinga, E.G. Implications for collagen i chain registry from the structure of the collagen von willebrand factor a3 domain complex. Proc. Nat. Acad. Sci. USA., 2012, 109, 5253-5258.
87. Manka, S.W.; Carafoli, F.; Visse, R.; Bihan, D.; Raynal, N.; Farndale, R.W.; Murphy, G.; Enghild, J.J.; Hohenester, E.; Nagase, H. Structural insights into triple-helical collagen cleavage by matrix metalloproteinase 1. Proc. Nat. Acad. Sci. USA., 2012, 109, 12461-12466.
88. Widmer, C.; Gebauer, J.M.; Brunstein, E.; Rosenbaum, S.; Zaucke, F.; Drogemuller, C.; Leeb, T.; Baumann, U. Molecular basis for the action of the collagen-specific chaperone hsp47/serpinh1 and its structure-specific client recognition. Proc. Nat. Acad. Sci. USA., 2012, 109, 13243-13247.
89. Bertini, I.; Fragai, M.; Luchinat, C.; Melikian, M.; Toccafondi, M.; Lauer, J.L.; Fields, G.B. Structural basis for matrix metalloproteinase 1-catalyzed collagenolysis. J. Am. Chem. Soc., 2012, 134, 2100-2110.
90. Liu, Q.; Ponnuraj, K.; Xu, Y.; Ganesh, V.K.; Sillanpaa, J.; Murray, B.E.; Narayana, S.V.; Hook, M. The enterococcus faecalis mscramm ace binds its ligand by the collagen hug model. J. Biol. Chem., 2007, 282, 19629-19637.
91. Visai, L.; Xu, Y.; Casolini, F.; Rindi, S.; Hook, M.; Speziale, P. Monoclonal antibodies to cna, a collagen-binding microbial surface component recognizing adhesive matrix molecules, detach staphylococcus aureus from a collagen substrate. J. Biol. Chem., 2000, 275, 39837-39845.
92. Elasri, M.O.; Thomas, J.R.; Skinner, R.A.; Blevins, J.S.; Beenken, K.E.; Nelson, C.L.; Smeltzer, M.S. Staphylococcus aureus collagen adhesin contributes to the pathogenesis of osteomyelitis. Bone, 2002, 30, 275-280.
93. Hienz, S.A.; Schennings, T.; Heimdahl, A.; Flock, J.I. Collagen binding of staphylococcus aureus is a virulence factor in experimental endocarditis. J. Infect. Dis., 1996, 174, 83-88.
94. Ponnuraj, K.; Bowden, M.G.; Davis, S.; Gurusiddappa, S.; Moore, D.; Choe, D.; Xu, Y.; Hook, M.; Narayana, S.V. A dock, lock, and latch structural model for a staphylococcal adhesin binding to fibrinogen. Cell, 2003, 115, 217-228.
95. Zong, Y.; Xu, Y.; Liang, X.; Keene, D.R.; Hook, A.; Gurusiddappa, S.; Hook, M.; Narayana, S.V. A 'collagen hug' model for staphylococcus aureus cna binding to collagen. Embo J., 2005, 24, 4224-4236.
96. Ganesh, V.K.; Rivera, J.J.; Smeds, E.; Ko, Y.P.; Bowden, M.G.; Wann, E.R.; Gurusiddappa, S.; Fitzgerald, J.R.; Hook, M. A structural model of the staphylococcus aureus clfa-fibrinogen interaction opens new avenues for the design of anti-staphylococcal therapeutics. PLoS Pathog., 2008, 4, e1000226.
97. Deivanayagam, C.C.; Wann, E.R.; Chen, W.; Carson, M.; Rajashankar, K.R.; Hook, M.; Narayana, S.V. A novel variant of the immunoglobulin fold in surface adhesins of staphylococcus aureus: Crystal structure of the fibrinogen-binding mscramm, clumping factor A. EMBO J., 2002, 21, 6660-6672.
98. Symersky, J.; Patti, J.M.; Carson, M.; House-Pompeo, K.; Teale, M.; Moore, D.; Jin, L.; Schneider, A.; DeLucas, L.J.; Hook, M.; Narayana, S.V. Structure of the collagen-binding domain from a staphylococcus aureus adhesin. Nat. Struct. Biol., 1997, 4, 833-838.
99. Berisio, R.; Ciccarelli, L.; Squeglia, F.; De Simone, A.; Vitagliano, L. Structural and dynamic properties of incomplete immunoglobulin- like fold domains. Prot. Pept. Lett., 2012, 19, 1045-53.
100. Vitagliano, L.; Berisio, R.; De Simone, A. Role of hydration in collagen recognition by bacterial adhesins. Biophys. J., 2011, 100, 2253-2261.
101. Rich, R.L.; Kreikemeyer, B.; Owens, R.T.; LaBrenz, S.; Narayana, S.V.; Weinstock, G.M.; Murray, B.E.; Hook, M. Ace is a collagenbinding mscramm from enterococcus faecalis. J. Biol. Chem., 1999, 274, 26939-26945.
102. Westerlund, B.; Korhonen, T.K. Bacterial proteins binding to the mammalian extracellular matrix. Mol. Microbiol., 1993, 9, 687-694.
103. Foster, T.J.; McDevitt, D. Surface-associated proteins of staphylococcus aureus: Their possible roles in virulence. FEMS Microbiol. Lett., 1994, 118, 199-205.
104. Mohamed, N.; Teeters, M.A.; Patti, J.M.; Hook, M.; Ross, J.M. Inhibition of Staphylococcus aureus adherence to collagen under dynamic conditions. Infect. Immunit., 1999, 67, 589-594.
105. Nallapareddy, S.R.; Sillanpaa, J.; Ganesh, V.K.; Hook, M.; Murray, B.E. Inhibition of enterococcus faecium adherence to collagen by antibodies against high-affinity binding subdomains of acm. Infect.immunit., 2007, 75, 3192-3196.
106. Myllyharju, J.; Kivirikko, K.I. Collagens, modifying enzymes and their mutations in humans, flies and worms. Trends in genetics: TIG, 2004, 20, 33-43.
107. Humtsoe, J.O.; Kim, J.K.; Xu, Y.; Keene, D.R.; Hook, M.; Lukomski, S.; Wary, K.K. A streptococcal collagen-like protein interacts with the alpha2beta1 integrin and induces intracellular signaling. J. Biol. Chem., 2005, 280, 13848-13857.
108. Rasmussen, M.; Bjorck, L. Unique regulation of sclb - a novel collagen-like surface protein of streptococcus pyogenes. Mol. Microbiol., 2001, 40, 1427-1438.
109. Caswell, C.C.; Oliver-Kozup, H.; Han, R.; Lukomska, E.; Lukomski, S. Scl1, the multifunctional adhesin of group a streptococcus, selectively binds cellular fibronectin and laminin, and mediates pathogen internalization by human cells. FEMS Microbiol. lett., 2010, 303, 61-68.
110. Chen, S.M.; Tsai, Y.S.; Wu, C.M.; Liao, S.K.; Wu, L.C.; Chang, C.S.; Liu, Y.H.; Tsai, P.J. Streptococcal collagen-like surface protein 1 promotes adhesion to the respiratory epithelial cell. BMC Microbiol., 2010, 10, 320.
111. Vandersmissen, L.; De Buck, E.; Saels, V.; Coil, D.A.; Anne, J. A legionella pneumophila collagen-like protein encoded by a gene with a variable number of tandem repeats is involved in the adherence and invasion of host cells. FEMS Microbiol. lett., 2010, 306, 168-176.
112. Boydston, J.A.; Chen, P.; Steichen, C.T.; Turnbough, C.L., Jr. Orientation within the exosporium and structural stability of the collagen-like glycoprotein bcla of bacillus anthracis. J Bacteriol., 2005, 187, 5310-5317.
113. Han, R.; Zwiefka, A.; Caswell, C.C.; Xu, Y.; Keene, D.R.; Lukomska, E.; Zhao, Z.; Hook, M.; Lukomski, S. Assessment of prokaryotic collagen-like sequences derived from streptococcal scl1 and scl2 proteins as a source of recombinant gxy polymers. Appl. Microbiol. Biotechnol., 2006, 72, 109-115.
114. Yu, Z.; Brodsky, B.; Inouye, M. Disscting a bacterial collagen domain from Streptococcus pyogenes. J. Biol. Chem., 2011, 286, 18960-18968.
115. Lukomski, S.; Nakashima, K.; Abdi, I.; Cipriano, V.J.; Ireland, R.M.; Reid, S.D.; Adams, G.G.; Musser, J.M. Identification and characterization of the scl gene encoding a group a streptococcus extracellular protein virulence factor with similarity to human collagen. Infect. Immunit., 2000, 68, 6542-6553.
116. Mohs, A.; Silva, T.; Yoshida, T.; Amin, R.; Lukomski, S.; Inouye, M.; Brodsky, B. Mechanism of stabilization of a bacterial collagen triple helix in the absence of hydroxyproline. J. Biol. Chem., 2007, 282, 29757-29765.
117. Xu, Y.; Keene, D.R.; Bujnicki, J.M.; Hook, M.; Lukomski, S. Streptococcal scl1 and scl2 proteins form collagen-like triple helices. J. Biol. Chem., 2002, 277, 27312-27318.
118. Caswell, C.C.; Barczyk, M.; Keene, D.R.; Lukomska, E.; Gullberg, D.E.; Lukomski, S. Identification of the first prokaryotic collagen sequence motif that mediates binding to human collagen receptors, integrins alpha2beta1 and alpha11beta1. J. Biol. Chem., 2008, 283, 36168-36175.
119. Caswell, C.C.; Lukomska, E.; Seo, N.S.; Hook, M.; Lukomski, S. Scl1-dependent internalization of group a streptococcus via direct interactions with the alpha2beta(1) integrin enhances pathogen survival and re-emergence. Mol. Microbiol., 2007, 64, 1319-1331.
120. Gao, Y.; Liang, C.; Zhao, R.; Lukomski, S.; Han, R. The scl1 of m41-type group a streptococcus binds the high-density lipoprotein. FEMS Microbiol. lett., 2010, 309, 55-61.
121. Caswell, C.C.; Han, R.; Hovis, K.M.; Ciborowski, P.; Keene, D.R.; Marconi, R.T.; Lukomski, S. The scl1 protein of m6-type group a streptococcus binds the human complement regulatory protein, factor h, and inhibits the alternative pathway of complement. Mol. Microbiol., 2008, 67, 584-596.
122. Reuter, M.; Caswell, C.C.; Lukomski, S.; Zipfel, P.F. Binding of the human complement regulators cfhr1 and factor h by streptococcal collagen-like protein 1 (scl1) via their conserved c termini allows control of the complement cascade at multiple levels. J. Biol. Chem., 2010, 285, 38473-38485.
123. Biedermann, F.; Uzunova, V.D.; Scherman, O.A.; Nau, W.M.; De Simone, A. Release of high-energy water as an essential driving force for the high-affinity binding of cucurbit[n]urils. J. Am. Chem. Soc., 2012, 134, 15318-15323.