2f68 › Citations

A 'Collagen Hug' model for Staphylococcus aureus CNA binding to collagen.

Zong Y, Xu Y, Liang X, Keene DR, Höök A, Gurusiddappa S, Höök M, Narayana SV
EMBO J 24 4224-36 (2005)
Cited: 136 times
EuropePMC logo PMID: 16362049

Abstract

The structural basis for the association of eukaryotic and prokaryotic protein receptors and their triple-helical collagen ligand remains poorly understood. Here, we present the crystal structures of a high affinity subsegment of the Staphylococcus aureus collagen-binding CNA as an apo-protein and in complex with a synthetic collagen-like triple helical peptide. The apo-protein structure is composed of two subdomains (N1 and N2), each adopting a variant IgG-fold, and a long linker that connects N1 and N2. The structure is stabilized by hydrophobic inter-domain interactions and by the N2 C-terminal extension that complements a beta-sheet on N1. In the ligand complex, the collagen-like peptide penetrates through a spherical hole formed by the two subdomains and the N1-N2 linker. Based on these two structures we propose a dynamic, multistep binding model, called the 'Collagen Hug' that is uniquely designed to allow multidomain collagen binding proteins to bind their extended rope-like ligand.

Reviews - 2f68 mentioned but not cited (4)

  1. Adhesion, invasion and evasion: the many functions of the surface proteins of Staphylococcus aureus. Foster TJ, Geoghegan JA, Ganesh VK, Höök M. Nat Rev Microbiol 12 49-62 (2014)
  2. Structural biology of Gram-positive bacterial adhesins. Vengadesan K, Narayana SV. Protein Sci 20 759-772 (2011)
  3. Collagen Binding Proteins of Gram-Positive Pathogens. Arora S, Gordon J, Hook M. Front Microbiol 12 628798 (2021)
  4. Isopeptide bond in collagen- and fibrinogen-binding MSCRAMMs. Sridharan U, Ponnuraj K. Biophys Rev 8 75-83 (2016)

Articles - 2f68 mentioned but not cited (7)

  1. Molecular mechanics of Staphylococcus aureus adhesin, CNA, and the inhibition of bacterial adhesion by stretching collagen. Madani A, Garakani K, Mofrad MRK. PLoS One 12 e0179601 (2017)
  2. Bacterial nanocellulose stimulates mesenchymal stem cell expansion and formation of stable collagen-I networks as a novel biomaterial in tissue engineering. Vielreicher M, Kralisch D, Völkl S, Sternal F, Arkudas A, Friedrich O. Sci Rep 8 9401 (2018)
  3. Targeted protein engineering provides insights into binding mechanism and affinities of bacterial collagen adhesins. Ross CL, Liang X, Liu Q, Murray BE, Höök M, Ganesh VK. J Biol Chem 287 34856-34865 (2012)
  4. Role of hydration in collagen recognition by bacterial adhesins. Vitagliano L, Berisio R, De Simone A. Biophys J 100 2253-2261 (2011)
  5. 'Hot' macromolecular crystals. Koclega KD, Chruszcz M, Zimmerman MD, Bujacz G, Minor W. Cryst Growth Des 10 580 (2009)
  6. Antibacterial Activity and Mechanism of Canagliflozin against Methicillin-Resistant Staphylococcus aureus. Gu S, Fan B, Wan F, Gao T, Qi Y, Zhou J, Zhang Y, Gu D, Xie W. Molecules 28 5668 (2023)
  7. Cloning, expression, purification, crystallization and preliminary X-ray diffraction analysis of the collagen-binding region of RspB from Erysipelothrix rhusiopathiae. Devi AS, Ogawa Y, Shimoji Y, Ponnuraj K. Acta Crystallogr Sect F Struct Biol Cryst Commun 66 156-159 (2010)


Reviews citing this publication (38)

  1. Mammalian collagen receptors. Leitinger B, Hohenester E. Matrix Biol 26 146-155 (2007)
  2. Staphylococcus aureus biofilm: a complex developmental organism. Moormeier DE, Bayles KW. Mol Microbiol 104 365-376 (2017)
  3. Scenery of Staphylococcus implant infections in orthopedics. Montanaro L, Speziale P, Campoccia D, Ravaioli S, Cangini I, Pietrocola G, Giannini S, Arciola CR. Future Microbiol 6 1329-1349 (2011)
  4. The Staphylococcal Biofilm: Adhesins, Regulation, and Host Response. Paharik AE, Horswill AR. Microbiol Spectr 4 (2016)
  5. Human pathogens utilize host extracellular matrix proteins laminin and collagen for adhesion and invasion of the host. Singh B, Fleury C, Jalalvand F, Riesbeck K. FEMS Microbiol Rev 36 1122-1180 (2012)
  6. Listeria monocytogenes surface proteins: from genome predictions to function. Bierne H, Cossart P. Microbiol Mol Biol Rev 71 377-397 (2007)
  7. The changing faces of Streptococcus antigen I/II polypeptide family adhesins. Brady LJ, Maddocks SE, Larson MR, Forsgren N, Persson K, Deivanayagam CC, Jenkinson HF. Mol Microbiol 77 276-286 (2010)
  8. Neutrophils and Immunity: From Bactericidal Action to Being Conquered. Teng TS, Ji AL, Ji XY, Li YZ. J Immunol Res 2017 9671604 (2017)
  9. Triple-helical peptides: an approach to collagen conformation, stability, and self-association. Brodsky B, Thiagarajan G, Madhan B, Kar K. Biopolymers 89 345-353 (2008)
  10. Intramolecular isopeptide bonds: protein crosslinks built for stress? Kang HJ, Baker EN. Trends Biochem Sci 36 229-237 (2011)
  11. Structural and functional role of Staphylococcus aureus surface components recognizing adhesive matrix molecules of the host. Speziale P, Pietrocola G, Rindi S, Provenzano M, Provenza G, Di Poto A, Visai L, Arciola CR. Future Microbiol 4 1337-1352 (2009)
  12. LPxTG surface proteins of enterococci. Hendrickx AP, Willems RJ, Bonten MJ, van Schaik W. Trends Microbiol 17 423-430 (2009)
  13. Bacterial adhesion to animal tissues: protein determinants for recognition of extracellular matrix components. Chagnot C, Listrat A, Astruc T, Desvaux M. Cell Microbiol 14 1687-1696 (2012)
  14. Targeting and mimicking collagens via triple helical peptide assembly. Li Y, Yu SM. Curr Opin Chem Biol 17 968-975 (2013)
  15. Synthesis and biological applications of collagen-model triple-helical peptides. Fields GB. Org Biomol Chem 8 1237-1258 (2010)
  16. Survey of the year 2005 commercial optical biosensor literature. Rich RL, Myszka DG. J Mol Recognit 19 478-534 (2006)
  17. Targeting collagen for diagnostic imaging and therapeutic delivery. Wahyudi H, Reynolds AA, Li Y, Owen SC, Yu SM. J Control Release 240 323-331 (2016)
  18. Paramagnetic liposomes for molecular MRI and MRI-guided drug delivery. Langereis S, Geelen T, Grüll H, Strijkers GJ, Nicolay K. NMR Biomed 26 728-744 (2013)
  19. Surface Proteins of Staphylococcus epidermidis. Foster TJ. Front Microbiol 11 1829 (2020)
  20. Multi-disciplinary antimicrobial strategies for improving orthopaedic implants to prevent prosthetic joint infections in hip and knee. Getzlaf MA, Lewallen EA, Kremers HM, Jones DL, Bonin CA, Dudakovic A, Thaler R, Cohen RC, Lewallen DG, van Wijnen AJ. J Orthop Res 34 177-186 (2016)
  21. Collagen-binding proteins of Streptococcus mutans and related streptococci. Avilés-Reyes A, Miller JH, Lemos JA, Abranches J. Mol Oral Microbiol 32 89-106 (2017)
  22. Noninvasive imaging of myocardial extracellular matrix for assessment of fibrosis. Won S, Davies-Venn C, Liu S, Bluemke DA. Curr Opin Cardiol 28 282-289 (2013)
  23. Polyproline and triple helix motifs in host-pathogen recognition. Berisio R, Vitagliano L. Curr Protein Pept Sci 13 855-865 (2012)
  24. The cell wall architecture of Enterococcus faecium: from resistance to pathogenesis. Hendrickx AP, van Schaik W, Willems RJ. Future Microbiol 8 993-1010 (2013)
  25. Diverse microbial interactions with the basement membrane barrier. Steukers L, Glorieux S, Vandekerckhove AP, Favoreel HW, Nauwynck HJ. Trends Microbiol 20 147-155 (2012)
  26. Structure, Function, and Assembly of Adhesive Organelles by Uropathogenic Bacteria. Chahales P, Thanassi DG. Microbiol Spectr 3 (2015)
  27. Designed triple-helical peptides as tools for collagen biochemistry and matrix engineering. Koide T. Philos Trans R Soc Lond B Biol Sci 362 1281-1291 (2007)
  28. Role of side chains in collagen triple helix stabilization and partner recognition. Berisio R, De Simone A, Ruggiero A, Improta R, Vitagliano L. J Pept Sci 15 131-140 (2009)
  29. Colonization and Infection of Indwelling Medical Devices by Staphylococcus aureus with an Emphasis on Orthopedic Implants. Pietrocola G, Campoccia D, Motta C, Montanaro L, Arciola CR, Speziale P. Int J Mol Sci 23 5958 (2022)
  30. Design and Use of Chimeric Proteins Containing a Collagen-Binding Domain for Wound Healing and Bone Regeneration. Addi C, Murschel F, De Crescenzo G. Tissue Eng Part B Rev 23 163-182 (2017)
  31. Genetics, Structure, and Function of Group A Streptococcal Pili. Nakata M, Kreikemeyer B. Front Microbiol 12 616508 (2021)
  32. Biofilm Formation by Pathogenic Bacteria: Applying a Staphylococcus aureus Model to Appraise Potential Targets for Therapeutic Intervention. Sedarat Z, Taylor-Robinson AW. Pathogens 11 388 (2022)
  33. The Process of Osteoblastic Infection by Staphylococcus Aureus. Wen Q, Gu F, Sui Z, Su Z, Yu T. Int J Med Sci 17 1327-1332 (2020)
  34. The Role of Staphylococcal Biofilm on the Surface of Implants in Orthopedic Infection. Lu Y, Cai WJ, Ren Z, Han P. Microorganisms 10 1909 (2022)
  35. Collagen degradation in tuberculosis pathogenesis: the biochemical consequences of hosting an undesired guest. Squeglia F, Ruggiero A, Berisio R. Biochem J 475 3123-3140 (2018)
  36. C-terminal domains of bacterial proteases: structure, function and the biotechnological applications. Huang J, Wu C, Liu D, Yang X, Wu R, Zhang J, Ma C, He H. J Appl Microbiol 122 12-22 (2017)
  37. Phylogenetic analysis of the bacterial Pro-Pro-endopeptidase domain reveals a diverse family including secreted and membrane anchored proteins. van Leeuwen HC, Roelofs D, Corver J, Hensbergen P. Curr Res Microb Sci 2 100024 (2021)
  38. Non-antibiotic strategies for prevention and treatment of internalized Staphylococcus aureus. Li J, Wen Q, Gu F, An L, Yu T. Front Microbiol 13 974984 (2022)

Articles citing this publication (87)

  1. Stabilizing isopeptide bonds revealed in gram-positive bacterial pilus structure. Kang HJ, Coulibaly F, Clow F, Proft T, Baker EN. Science 318 1625-1628 (2007)
  2. Structure and pathogenicity of antibodies specific for citrullinated collagen type II in experimental arthritis. Uysal H, Bockermann R, Nandakumar KS, Sehnert B, Bajtner E, Engström A, Serre G, Burkhardt H, Thunnissen MM, Holmdahl R. J Exp Med 206 449-462 (2009)
  3. Genetic variation in Staphylococcus aureus surface and immune evasion genes is lineage associated: implications for vaccine design and host-pathogen interactions. McCarthy AJ, Lindsay JA. BMC Microbiol 10 173 (2010)
  4. A structural model of the Staphylococcus aureus ClfA-fibrinogen interaction opens new avenues for the design of anti-staphylococcal therapeutics. Ganesh VK, Rivera JJ, Smeds E, Ko YP, Bowden MG, Wann ER, Gurusiddappa S, Fitzgerald JR, Höök M. PLoS Pathog 4 e1000226 (2008)
  5. Structural basis of sequence-specific collagen recognition by SPARC. Hohenester E, Sasaki T, Giudici C, Farndale RW, Bächinger HP. Proc Natl Acad Sci U S A 105 18273-18277 (2008)
  6. The Corynebacterium diphtheriae shaft pilin SpaA is built of tandem Ig-like modules with stabilizing isopeptide and disulfide bonds. Kang HJ, Paterson NG, Gaspar AH, Ton-That H, Baker EN. Proc Natl Acad Sci U S A 106 16967-16971 (2009)
  7. Importance of the collagen adhesin ace in pathogenesis and protection against Enterococcus faecalis experimental endocarditis. Singh KV, Nallapareddy SR, Sillanpää J, Murray BE. PLoS Pathog 6 e1000716 (2010)
  8. Molecular mechanism of extreme mechanostability in a pathogen adhesin. Milles LF, Schulten K, Gaub HE, Bernardi RC. Science 359 1527-1533 (2018)
  9. An IgG-like domain in the minor pilin GBS52 of Streptococcus agalactiae mediates lung epithelial cell adhesion. Krishnan V, Gaspar AH, Ye N, Mandlik A, Ton-That H, Narayana SV. Structure 15 893-903 (2007)
  10. Collagen-binding microbial surface components recognizing adhesive matrix molecule (MSCRAMM) of Gram-positive bacteria inhibit complement activation via the classical pathway. Kang M, Ko YP, Liang X, Ross CL, Liu Q, Murray BE, Höök M. J Biol Chem 288 20520-20531 (2013)
  11. Intramolecular isopeptide bonds give thermodynamic and proteolytic stability to the major pilin protein of Streptococcus pyogenes. Kang HJ, Baker EN. J Biol Chem 284 20729-20737 (2009)
  12. Identification and phenotypic characterization of a second collagen adhesin, Scm, and genome-based identification and analysis of 13 other predicted MSCRAMMs, including four distinct pilus loci, in Enterococcus faecium. Sillanpää J, Nallapareddy SR, Prakash VP, Qin X, Höök M, Weinstock GM, Murray BE. Microbiology (Reading) 154 3199-3211 (2008)
  13. A collagen-binding adhesin, Acb, and ten other putative MSCRAMM and pilus family proteins of Streptococcus gallolyticus subsp. gallolyticus (Streptococcus bovis Group, biotype I). Sillanpää J, Nallapareddy SR, Qin X, Singh KV, Muzny DM, Kovar CL, Nazareth LV, Gibbs RA, Ferraro MJ, Steckelberg JM, Weinstock GM, Murray BE. J Bacteriol 191 6643-6653 (2009)
  14. High resolution imaging of collagen organisation and synthesis using a versatile collagen specific probe. Boerboom RA, Krahn KN, Megens RT, van Zandvoort MA, Merkx M, Bouten CV. J Struct Biol 159 392-399 (2007)
  15. 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)
  16. In vivo characterization of a new abdominal aortic aneurysm mouse model with conventional and molecular magnetic resonance imaging. Klink A, Heynens J, Herranz B, Lobatto ME, Arias T, Sanders HM, Strijkers GJ, Merkx M, Nicolay K, Fuster V, Tedgui A, Mallat Z, Mulder WJ, Fayad ZA. J Am Coll Cardiol 58 2522-2530 (2011)
  17. Molecular characterization of a Streptococcus gallolyticus genomic island encoding a pilus involved in endocarditis. Danne C, Entenza JM, Mallet A, Briandet R, Débarbouillé M, Nato F, Glaser P, Jouvion G, Moreillon P, Trieu-Cuot P, Dramsi S. J Infect Dis 204 1960-1970 (2011)
  18. Imaging collagen in intact viable healthy and atherosclerotic arteries using fluorescently labeled CNA35 and two-photon laser scanning microscopy. Megens RT, Oude Egbrink MG, Cleutjens JP, Kuijpers MJ, Schiffers PH, Merkx M, Slaaf DW, van Zandvoort MA. Mol Imaging 6 247-260 (2007)
  19. Structural and biochemical characterization of Staphylococcus aureus clumping factor B/ligand interactions. Ganesh VK, Barbu EM, Deivanayagam CC, Le B, Anderson AS, Matsuka YV, Lin SL, Foster TJ, Narayana SV, Höök M. J Biol Chem 286 25963-25972 (2011)
  20. Colorful protein-based fluorescent probes for collagen imaging. Aper SJ, van Spreeuwel AC, van Turnhout MC, van der Linden AJ, Pieters PA, van der Zon NL, de la Rambelje SL, Bouten CV, Merkx M. PLoS One 9 e114983 (2014)
  21. Crystal structure of the C-terminal region of Streptococcus mutans antigen I/II and characterization of salivary agglutinin adherence domains. Larson MR, Rajashankar KR, Crowley PJ, Kelly C, Mitchell TJ, Brady LJ, Deivanayagam C. J Biol Chem 286 21657-21666 (2011)
  22. Structural basis of mannan-binding lectin recognition by its associated serine protease MASP-1: implications for complement activation. Gingras AR, Girija UV, Keeble AH, Panchal R, Mitchell DA, Moody PC, Wallis R. Structure 19 1635-1643 (2011)
  23. Two intramolecular isopeptide bonds are identified in the crystal structure of the Streptococcus gordonii SspB C-terminal domain. Forsgren N, Lamont RJ, Persson K. J Mol Biol 397 740-751 (2010)
  24. Functional interactions among filamentous Epsilonproteobacteria and Bacteroidetes in a deep-sea hydrothermal vent biofilm. Stokke R, Dahle H, Roalkvam I, Wissuwa J, Daae FL, Tooming-Klunderud A, Thorseth IH, Pedersen RB, Steen IH. Environ Microbiol 17 4063-4077 (2015)
  25. The multifunctional LigB adhesin binds homeostatic proteins with potential roles in cutaneous infection by pathogenic Leptospira interrogans. Choy HA, Kelley MM, Croda J, Matsunaga J, Babbitt JT, Ko AI, Picardeau M, Haake DA. PLoS One 6 e16879 (2011)
  26. Mechanical Strength and Inhibition of the Staphylococcus aureus Collagen-Binding Protein Cna. Herman-Bausier P, Valotteau C, Pietrocola G, Rindi S, Alsteens D, Foster TJ, Speziale P, Dufrêne YF. mBio 7 e01529-16 (2016)
  27. A new method for describing the helical conformation of collagen: dependence of the triple helical twist on amino acid sequence. Bella J. J Struct Biol 170 377-391 (2010)
  28. First analysis of a bacterial collagen-binding protein with collagen Toolkits: promiscuous binding of YadA to collagens may explain how YadA interferes with host processes. Leo JC, Elovaara H, Bihan D, Pugh N, Kilpinen SK, Raynal N, Skurnik M, Farndale RW, Goldman A. Infect Immun 78 3226-3236 (2010)
  29. Targeted drug delivery utilizing protein-like molecular architecture. Rezler EM, Khan DR, Lauer-Fields J, Cudic M, Baronas-Lowell D, Fields GB. J Am Chem Soc 129 4961-4972 (2007)
  30. Staphylococcus aureus adhesion in endovascular infections is controlled by the ArlRS-MgrA signaling cascade. Kwiecinski JM, Crosby HA, Valotteau C, Hippensteel JA, Nayak MK, Chauhan AK, Schmidt EP, Dufrêne YF, Horswill AR. PLoS Pathog 15 e1007800 (2019)
  31. Healthcare- and Community-Associated Methicillin-Resistant Staphylococcus aureus (MRSA) and Fatal Pneumonia with Pediatric Deaths in Krasnoyarsk, Siberian Russia: Unique MRSA's Multiple Virulence Factors, Genome, and Stepwise Evolution. Khokhlova OE, Hung WC, Wan TW, Iwao Y, Takano T, Higuchi W, Yachenko SV, Teplyakova OV, Kamshilova VV, Kotlovsky YV, Nishiyama A, Reva IV, Sidorenko SV, Peryanova OV, Reva GV, Teng LJ, Salmina AB, Yamamoto T. PLoS One 10 e0128017 (2015)
  32. Sortases, Surface Proteins, and Their Roles in Staphylococcus aureus Disease and Vaccine Development. Schneewind O, Missiakas D. Microbiol Spectr 7 (2019)
  33. Stability and assembly of pilus subunits of Streptococcus pneumoniae. El Mortaji L, Terrasse R, Dessen A, Vernet T, Di Guilmi AM. J Biol Chem 285 12405-12415 (2010)
  34. Morphology, binding behavior and MR-properties of paramagnetic collagen-binding liposomes. Sanders HM, Strijkers GJ, Mulder WJ, Huinink HP, Erich SJ, Adan OC, Sommerdijk NA, Merkx M, Nicolay K. Contrast Media Mol Imaging 4 81-88 (2009)
  35. The Yersinia adhesin YadA binds to a collagenous triple-helical conformation but without sequence specificity. Leo JC, Elovaara H, Brodsky B, Skurnik M, Goldman A. Protein Eng Des Sel 21 475-484 (2008)
  36. The full-length Streptococcus pneumoniae major pilin RrgB crystallizes in a fibre-like structure, which presents the D1 isopeptide bond and provides details on the mechanism of pilus polymerization. El Mortaji L, Contreras-Martel C, Moschioni M, Ferlenghi I, Manzano C, Vernet T, Dessen A, Di Guilmi AM. Biochem J 441 833-841 (2012)
  37. Cyclic di-GMP contributes to adaption and virulence of Bacillus thuringiensis through a riboswitch-regulated collagen adhesion protein. Tang Q, Yin K, Qian H, Zhao Y, Wang W, Chou SH, Fu Y, He J. Sci Rep 6 28807 (2016)
  38. Fibronectin-binding protein B (FnBPB) from Staphylococcus aureus protects against the antimicrobial activity of histones. Pietrocola G, Nobile G, Alfeo MJ, Foster TJ, Geoghegan JA, De Filippis V, Speziale P. J Biol Chem 294 3588-3602 (2019)
  39. Assessment of cardiovascular fibrosis using novel fluorescent probes. Chen J, Lee SK, Abd-Elgaliel WR, Liang L, Galende EY, Hajjar RJ, Tung CH. PLoS One 6 e19097 (2011)
  40. Bullous impetigo in children infected with methicillin-resistant Staphylococcus aureus alone or in combination with methicillin-susceptible S. aureus: analysis of genetic characteristics, including assessment of exfoliative toxin gene carriage. Shi D, Higuchi W, Takano T, Saito K, Ozaki K, Takano M, Nitahara Y, Yamamoto T. J Clin Microbiol 49 1972-1974 (2011)
  41. The BBA33 lipoprotein binds collagen and impacts Borrelia burgdorferi pathogenesis. Zhi H, Weening EH, Barbu EM, Hyde JA, Höök M, Skare JT. Mol Microbiol 96 68-83 (2015)
  42. Identification and characterization of enolase as a collagen-binding protein in Lactobacillus plantarum. Salzillo M, Vastano V, Capri U, Muscariello L, Sacco M, Marasco R. J Basic Microbiol 55 890-897 (2015)
  43. Isopeptide bonds in bacterial pili and their characterization by X-ray crystallography and mass spectrometry. Kang HJ, Middleditch M, Proft T, Baker EN. Biopolymers 91 1126-1134 (2009)
  44. A new staphylococcal cassette chromosome mec IV encoding a novel cell-wall-anchored surface protein in a major ST8 community-acquired methicillin-resistant Staphylococcus aureus clone in Japan. Iwao Y, Takano T, Higuchi W, Yamamoto T. J Infect Chemother 18 96-104 (2012)
  45. Glycosylation modulates melanoma cell α2β1 and α3β1 integrin interactions with type IV collagen. Stawikowski MJ, Aukszi B, Stawikowska R, Cudic M, Fields GB. J Biol Chem 289 21591-21604 (2014)
  46. The Respiratory Pathogen Moraxella catarrhalis Targets Collagen for Maximal Adherence to Host Tissues. Singh B, Alvarado-Kristensson M, Johansson M, Hallgren O, Westergren-Thorsson G, Mörgelin M, Riesbeck K. mBio 7 e00066 (2016)
  47. The binding of CNA35 contrast agents to collagen fibrils. Sanders HM, Iafisco M, Pouget EM, Bomans PH, Nudelman F, Falini G, de With G, Merkx M, Strijkers GJ, Nicolay K, Sommerdijk NA. Chem Commun (Camb) 47 1503-1505 (2011)
  48. Structural basis of collagen recognition by human osteoclast-associated receptor and design of osteoclastogenesis inhibitors. Haywood J, Qi J, Chen CC, Lu G, Liu Y, Yan J, Shi Y, Gao GF. Proc Natl Acad Sci U S A 113 1038-1043 (2016)
  49. Augmenting the articular cartilage-implant interface: Functionalizing with a collagen adhesion protein. Allon AA, Ng KW, Hammoud S, Russell BH, Jones CM, Rivera JJ, Schwartz J, Hook M, Maher SA. J Biomed Mater Res A 100 2168-2175 (2012)
  50. Calcium stabilizes the strongest protein fold. Milles LF, Unterauer EM, Nicolaus T, Gaub HE. Nat Commun 9 4764 (2018)
  51. Inhibition of Enterococcus faecium adherence to collagen by antibodies against high-affinity binding subdomains of Acm. Nallapareddy SR, Sillanpää J, Ganesh VK, Höök M, Murray BE. Infect Immun 75 3192-3196 (2007)
  52. Characterization by high-resolution crystal structure analysis of a triple-helix region of human collagen type III with potent cell adhesion activity. Hua C, Zhu Y, Xu W, Ye S, Zhang R, Lu L, Jiang S. Biochem Biophys Res Commun 508 1018-1023 (2019)
  53. Variation and association of fibronectin-binding protein genes fnbA and fnbB in Staphylococcus aureus Japanese isolates. Murai M, Moriyama H, Hata E, Takeuchi F, Amemura-Maekawa J. Microbiol Immunol 60 312-325 (2016)
  54. Crystal structure of the MrkD1P receptor binding domain of Klebsiella pneumoniae and identification of the human collagen V binding interface. Rêgo AT, Johnson JG, Gelbel S, Enguita FJ, Clegg S, Waksman G. Mol Microbiol 86 882-893 (2012)
  55. Crystal structure of the functional region of Uro-adherence factor A from Staphylococcus saprophyticus reveals participation of the B domain in ligand binding. Matsuoka E, Tanaka Y, Kuroda M, Shouji Y, Ohta T, Tanaka I, Yao M. Protein Sci 20 406-416 (2011)
  56. Streptokinase Treatment Reverses Biofilm-Associated Antibiotic Resistance in Staphylococcus aureus. Jørgensen NP, Zobek N, Dreier C, Haaber J, Ingmer H, Larsen OH, Meyer RL. Microorganisms 4 E36 (2016)
  57. Crystal structure of ACE19, the collagen binding subdomain of Enterococus faecalis surface protein ACE. Ponnuraj K, Narayana SV. Proteins 69 199-203 (2007)
  58. Non-linearity of the collagen triple helix in solution and implications for collagen function. Walker KT, Nan R, Wright DW, Gor J, Bishop AC, Makhatadze GI, Brodsky B, Perkins SJ. Biochem J 474 2203-2217 (2017)
  59. Structural and functional analysis of the N-terminal domain of the Streptococcus gordonii adhesin Sgo0707. Nylander Å, Svensäter G, Senadheera DB, Cvitkovitch DG, Davies JR, Persson K. PLoS One 8 e63768 (2013)
  60. Crystal structure of linoleate 13R-manganese lipoxygenase in complex with an adhesion protein. Chen Y, Wennman A, Karkehabadi S, Engström Å, Oliw EH. J Lipid Res 57 1574-1588 (2016)
  61. Gum arabic modified Fe3O4 nanoparticles cross linked with collagen for isolation of bacteria. Chockalingam AM, Babu HK, Chittor R, Tiwari JP. J Nanobiotechnology 8 30 (2010)
  62. Immobilizing reporters for molecular imaging of the extracellular microenvironment in living animals. Xia Z, Xing Y, Jeon J, Kim YP, Gall J, Dragulescu-Andrasi A, Gambhir SS, Rao J. ACS Chem Biol 6 1117-1126 (2011)
  63. Methicillin resistance and selective genetic determinants of Staphylococcus aureus isolates with bovine mastitis milk origin. Ahangari Z, Ghorbanpoor M, Shapouri MRS, Gharibi D, Ghazvini K. Iran J Microbiol 9 152-159 (2017)
  64. The N-terminal domain of the thermo-regulated surface protein PrpA of Enterococcus faecium binds to fibrinogen, fibronectin and platelets. Guzmán Prieto AM, Urbanus RT, Zhang X, Bierschenk D, Koekman CA, van Luit-Asbroek M, Ouwerkerk JP, Pape M, Paganelli FL, Wobser D, Huebner J, Hendrickx AP, Bonten MJ, Willems RJ, van Schaik W. Sci Rep 5 18255 (2015)
  65. Binding to type I collagen is essential for the infectivity of Vibrio parahaemolyticus to host cells. Liu M, Yang S, Zheng C, Luo X, Bei W, Cai P. Cell Microbiol 20 e12856 (2018)
  66. Pathogen-related factors affecting outcome of catheter-related bacteremia due to methicillin-susceptible Staphylococcus aureus in a Spanish multicenter study. San-Juan R, Pérez-Montarelo D, Viedma E, Lalueza A, Fortún J, Loza E, Pujol M, Ardanuy C, Morales I, de Cueto M, Resino-Foz E, Morales-Cartagena MA, Fernández-Ruiz M, Rico A, Romero MP, Fernández de Mera M, López-Medrano F, Orellana MÁ, Aguado JM, Chaves F. Eur J Clin Microbiol Infect Dis 36 1757-1765 (2017)
  67. Semi-synthesis of a protease-activatable collagen targeting probe. Breurken M, Lempens EH, Meijer EW, Merkx M. Chem Commun (Camb) 47 7998-8000 (2011)
  68. Functional Analysis of the Collagen Binding Proteins of Streptococcus parasanguinis FW213. Chen YM, Tsai PH, Ye ZS, Huang YW, Shieh HR, Wu CH, Lin YJ, Miller JH, Abranches J, Chiu CH. mSphere 5 e00863-20 (2020)
  69. Pyruvate dehydrogenase subunit β of Lactobacillus plantarum is a collagen adhesin involved in biofilm formation. Salzillo M, Vastano V, Capri U, Muscariello L, Marasco R. J Basic Microbiol 57 353-357 (2017)
  70. Protease-activatable collagen targeting based on protein cyclization. Breurken M, Lempens EH, Merkx M. Chembiochem 11 1665-1668 (2010)
  71. RadA, a MSCRAMM Adhesin of the Dominant Symbiote Ruminococcus gnavus E1, Binds Human Immunoglobulins and Intestinal Mucins. Maresca M, Alatou R, Pujol A, Nicoletti C, Perrier J, Giardina T, Simon G, Méjean V, Fons M. Biomolecules 11 1613 (2021)
  72. Visualisation of Collagen in fixed skeletal muscle tissue using fluorescently tagged Collagen binding protein CNA35. Mohammadkhah M, Simms CK, Murphy P. J Mech Behav Biomed Mater 66 37-44 (2017)
  73. Bacillus thuringiensis CbpA is a collagen binding cell surface protein under c-di-GMP control. Finke S, Fagerlund A, Smith V, Krogstad V, Zhang MJ, Saragliadis A, Linke D, Nielsen-LeRoux C, Økstad OA. Cell Surf 5 100032 (2019)
  74. Choline dendrimers as generic scaffolds for the non-covalent synthesis of multivalent protein assemblies. Hernández-Rocamora VM, Reulen SW, de Waal B, Meijer EW, Sanz JM, Merkx M. Chem Commun (Camb) 47 5997-5999 (2011)
  75. Comment Is it feasible to control pathogen infection by competitive binding of probiotics to the host? Fukuda K. Virulence 8 1502-1505 (2017)
  76. Large-Scale Discovery of Microbial Fibrillar Adhesins and Identification of Novel Members of Adhesive Domain Families. Monzon V, Bateman A. J Bacteriol 204 e0010722 (2022)
  77. Adhesive Virulence Factors of Staphylococcus aureus Resist Digestion by Coagulation Proteases Thrombin and Plasmin. Risser F, López-Morales J, Nash MA. ACS Bio Med Chem Au 2 586-599 (2022)
  78. Genomic comparison between Staphylococcus aureus GN strains clinically isolated from a familial infection case: IS1272 transposition through a novel inverted repeat-replacing mechanism. Wan TW, Higuchi W, Khokhlova OE, Hung WC, Iwao Y, Wakayama M, Inomata N, Takano T, Lin YT, Peryanova OV, Kojima KK, Salmina AB, Teng LJ, Yamamoto T. PLoS One 12 e0187288 (2017)
  79. Interactions between the Trimeric Autotransporter Adhesin EmaA and Collagen Revealed by Three-Dimensional Electron Tomography. Azari F, Radermacher M, Mintz KP, Ruiz T. J Bacteriol 201 e00297-19 (2019)
  80. A convolutional neural network STIFMap reveals associations between stromal stiffness and EMT in breast cancer. Stashko C, Hayward MK, Northey JJ, Pearson N, Ironside AJ, Lakins JN, Oria R, Goyette MA, Mayo L, Russnes HG, Hwang ES, Kutys ML, Polyak K, Weaver VM. Nat Commun 14 3561 (2023)
  81. Interaction of the Staphylococcus aureus Surface Protein FnBPB with Corneodesmosin Involves Two Distinct, Extremely Strong Bonds. Paiva TO, Viljoen A, da Costa TM, Geoghegan JA, Dufrêne YF. ACS Nanosci Au 3 58-66 (2023)
  82. Mapping preferred sites for fluorescent labeling by combining fluorescence and MS analysis of tryptic CNA35 protein digests. Mingels AM, van Dongen JL, Merkx M. J Chromatogr B Analyt Technol Biomed Life Sci 863 293-297 (2008)
  83. Steered molecular dynamics study reveals insights into the function of the repetitive B region of collagen- and fibrinogen-binding MSCRAMMs. Jemima Beulin DS, Ponnuraj K. J Biomol Struct Dyn 35 535-550 (2017)
  84. Molecular docking reveals Chitosan nanoparticle protection mechanism for dentin against Collagen-binding bacteria. Zhou Z, Yang Y, He L, Wang J, Xiong J. J Mater Sci Mater Med 33 43 (2022)
  85. Pleural thickening induced by Glaesserella parasuis infection was linked to increased collagen and elastin. Gong H, Chen L, He Y, Hua K, Ma B, Gao Y, Xu X, Hu X, Jin H. Front Cell Infect Microbiol 12 952377 (2022)
  86. Utilization of commercial collagens for preparing well-differentiated human beta cells for confocal microscopy. Brennecke BR, Yang U, Liu S, Ilerisoy FS, Ilerisoy BN, Joglekar A, Kim LB, Peachee SJ, Richtsmeier SL, Stephens SB, Sander EA, Strack S, Moninger TO, Ankrum JA, Imai Y. Front Endocrinol (Lausanne) 14 1187216 (2023)
  87. Visualizing Collagen Fibrils in the Cochlea's Tectorial and Basilar Membranes Using a Fluorescently Labeled Collagen-Binding Protein Fragment. de Sousa Lobo Ferreira Querido R, Ji X, Lakha R, Goodyear RJ, Richardson GP, Vizcarra CL, Olson ES. J Assoc Res Otolaryngol 24 147-157 (2023)


Quick links