2pms › Citations

Structure of a complex of human lactoferrin N-lobe with pneumococcal surface protein a provides insight into microbial defense mechanism.

Senkovich O, Cook WJ, Mirza S, Hollingshead SK, Protasevich II, Briles DE, Chattopadhyay D
J Mol Biol 370 701-13 (2007)
Cited: 44 times
EuropePMC logo PMID: 17543335

Abstract

Human lactoferrin, a component of the innate immune system, kills a wide variety of microorganisms including the Gram positive bacteria Streptococcus pneumoniae. Pneumococcal surface protein A (PspA) efficiently inhibits this bactericidal action. The crystal structure of a complex of the lactoferrin-binding domain of PspA with the N-lobe of human lactoferrin reveals direct and specific interactions between the negatively charged surface of PspA helices and the highly cationic lactoferricin moiety of lactoferrin. Binding of PspA blocks surface accessibility of this bactericidal peptide preventing it from penetrating the bacterial membrane. Results of site-directed mutagenesis, in vitro protein binding assays and isothermal titration calorimetry measurements corroborate that the specific electrostatic interactions observed in the crystal structure represent major associations between PspA and lactoferrin. The structure provides a snapshot of the protective mechanism utilized by pathogens against the host's first line of defense. PspA represents a major virulence factor and a promising vaccine candidate. Insights from the structure of the complex have implications for designing therapeutic strategies for treatment and prevention of pneumococcal diseases that remain a major public health problem worldwide.

Reviews - 2pms mentioned but not cited (1)

  1. Choline Binding Proteins from Streptococcus pneumoniae: A Dual Role as Enzybiotics and Targets for the Design of New Antimicrobials. Maestro B, Sanz JM. Antibiotics (Basel) 5 E21 (2016)

Articles - 2pms mentioned but not cited (5)

  1. Structure of a complex of human lactoferrin N-lobe with pneumococcal surface protein a provides insight into microbial defense mechanism. Senkovich O, Cook WJ, Mirza S, Hollingshead SK, Protasevich II, Briles DE, Chattopadhyay D. J Mol Biol 370 701-713 (2007)
  2. Antimicrobial Functions of Lactoferrin Promote Genetic Conflicts in Ancient Primates and Modern Humans. Barber MF, Kronenberg Z, Yandell M, Elde NC. PLoS Genet 12 e1006063 (2016)
  3. Structural attributes for the recognition of weak and anomalous regions in coiled-coils of myosins and other motor proteins. Sunitha MS, Nair AG, Charya A, Jadhav K, Mukhopadhyay S, Sowdhamini R. BMC Res Notes 5 530 (2012)
  4. In-silico design and evaluation of an epitope-based serotype-independent promising vaccine candidate for highly cross-reactive regions of pneumococcal surface protein A. Afshari E, Cohan RA, Sotoodehnejadnematalahi F, Mousavi SF. J Transl Med 21 13 (2023)
  5. Immunoinformatics-aided design of a new multi-epitope vaccine adjuvanted with domain 4 of pneumolysin against Streptococcus pneumoniae strains. Shafaghi M, Bahadori Z, Madanchi H, Ranjbar MM, Shabani AA, Mousavi SF. BMC Bioinformatics 24 67 (2023)


Reviews citing this publication (15)

  1. Pathogenesis and pathophysiology of pneumococcal meningitis. Mook-Kanamori BB, Geldhoff M, van der Poll T, van de Beek D. Clin Microbiol Rev 24 557-591 (2011)
  2. Buried Treasure: Evolutionary Perspectives on Microbial Iron Piracy. Barber MF, Elde NC. Trends Genet 31 627-636 (2015)
  3. Pneumococcal surface proteins: when the whole is greater than the sum of its parts. Pérez-Dorado I, Galan-Bartual S, Hermoso JA. Mol Oral Microbiol 27 221-245 (2012)
  4. A structural perspective on lactoferrin function. Baker HM, Baker EN. Biochem Cell Biol 90 320-328 (2012)
  5. Lactoferrin and cancer disease prevention. Rodrigues L, Teixeira J, Schmitt F, Schmitt F, Paulsson M, Månsson HL. Crit Rev Food Sci Nutr 49 203-217 (2009)
  6. Versatility of choline metabolism and choline-binding proteins in Streptococcus pneumoniae and commensal streptococci. Hakenbeck R, Madhour A, Denapaite D, Brückner R. FEMS Microbiol Rev 33 572-586 (2009)
  7. Resistance Mechanisms to Antimicrobial Peptides in Gram-Positive Bacteria. Assoni L, Milani B, Carvalho MR, Nepomuceno LN, Waz NT, Guerra MES, Converso TR, Darrieux M. Front Microbiol 11 593215 (2020)
  8. Mucosal Immune Development in Early Life: Setting the Stage. Brugman S, Perdijk O, van Neerven RJ, Savelkoul HF. Arch Immunol Ther Exp (Warsz) 63 251-268 (2015)
  9. A survey of the year 2007 literature on applications of isothermal titration calorimetry. Bjelić S, Jelesarov I. J Mol Recognit 21 289-312 (2008)
  10. Reciprocal interactions between lactoferrin and bacterial endotoxins and their role in the regulation of the immune response. Latorre D, Puddu P, Valenti P, Gessani S. Toxins (Basel) 2 54-68 (2010)
  11. The lactoferrin receptor complex in Gram negative bacteria. Beddek AJ, Schryvers AB. Biometals 23 377-386 (2010)
  12. Immunoregulatory role of lactoferrin-lipopolysaccharide interactions. Puddu P, Latorre D, Valenti P, Gessani S. Biometals 23 387-397 (2010)
  13. Towards Identifying Protective B-Cell Epitopes: The PspA Story. Khan N, Jan AT. Front Microbiol 8 742 (2017)
  14. Occurrence and potential mechanism of holin-mediated non-lytic protein translocation in bacteria. Brüser T, Mehner-Breitfeld D. Microb Cell 9 159-173 (2022)
  15. Pneumococcal Surface Proteins as Virulence Factors, Immunogens, and Conserved Vaccine Targets. Aceil J, Avci FY. Front Cell Infect Microbiol 12 832254 (2022)

Articles citing this publication (23)

  1. Ceruloplasmin: macromolecular assemblies with iron-containing acute phase proteins. Samygina VR, Sokolov AV, Bourenkov G, Petoukhov MV, Pulina MO, Zakharova ET, Vasilyev VB, Bartunik H, Svergun DI. PLoS One 8 e67145 (2013)
  2. Mucosal immunization with an unadjuvanted vaccine that targets Streptococcus pneumoniae PspA to human Fcγ receptor type I protects against pneumococcal infection through complement- and lactoferrin-mediated bactericidal activity. Bitsaktsis C, Iglesias BV, Li Y, Colino J, Snapper CM, Hollingshead SK, Pham G, Gosselin DR, Gosselin EJ. Infect Immun 80 1166-1180 (2012)
  3. Protective properties of a fusion pneumococcal surface protein A (PspA) vaccine against pneumococcal challenge by five different PspA clades in mice. Piao Z, Akeda Y, Takeuchi D, Ishii KJ, Ubukata K, Briles DE, Tomono K, Oishi K. Vaccine 32 5607-5613 (2014)
  4. Structural insight into the lactoferrin receptors from pathogenic Neisseria. Noinaj N, Cornelissen CN, Buchanan SK. J Struct Biol 184 83-92 (2013)
  5. Thermodynamic characterization of the interactions between the immunoregulatory proteins osteopontin and lactoferrin. Yamniuk AP, Burling H, Vogel HJ. Mol Immunol 46 2395-2402 (2009)
  6. Mapping of epitopes recognized by antibodies induced by immunization of mice with PspA and PspC. Vadesilho CF, Ferreira DM, Gordon SB, Briles DE, Moreno AT, Oliveira ML, Ho PL, Miyaji EN. Clin Vaccine Immunol 21 940-948 (2014)
  7. The role of lactoferrin binding protein B in mediating protection against human lactoferricin. Morgenthau A, Livingstone M, Adamiak P, Schryvers AB. Biochem Cell Biol 90 417-423 (2012)
  8. Lactoferrin binding protein B - a bi-functional bacterial receptor protein. Ostan NK, Yu RH, Ng D, Lai CC, Pogoutse AK, Sarpe V, Hepburn M, Sheff J, Raval S, Schriemer DC, Moraes TF, Schryvers AB. PLoS Pathog 13 e1006244 (2017)
  9. A Synthetic Virus-Like Particle Streptococcal Vaccine Candidate Using B-Cell Epitopes from the Proline-Rich Region of Pneumococcal Surface Protein A. Tamborrini M, Geib N, Marrero-Nodarse A, Jud M, Hauser J, Aho C, Lamelas A, Zuniga A, Pluschke G, Ghasparian A, Robinson JA. Vaccines (Basel) 3 850-874 (2015)
  10. Interaction of pneumococcal phase variation, host and pressure/gas composition: virulence expression of NanA, HylA, PspA and CbpA in simulated otitis media. Li-Korotky HS, Lo CY, Banks JM. Microb Pathog 49 204-210 (2010)
  11. Structural characterization of the interaction of human lactoferrin with calmodulin. Gifford JL, Ishida H, Vogel HJ. PLoS One 7 e51026 (2012)
  12. Streptococcus pneumoniae binds to host GAPDH on dying lung epithelial cells worsening secondary infection following influenza. Park SS, Gonzalez-Juarbe N, Riegler AN, Im H, Hale Y, Platt MP, Croney C, Briles DE, Orihuela CJ. Cell Rep 35 109267 (2021)
  13. Lactoferrin Isolation Using Monolithic Column Coupled with Spectrometric or Micro-Amperometric Detector. Adam V, Zitka O, Dolezal P, Zeman L, Horna A, Hubalek J, Sileny J, Krizkova S, Trnkova L, Kizek R. Sensors (Basel) 8 464-487 (2008)
  14. Production and purification of an untagged recombinant pneumococcal surface protein A (PspA4Pro) with high-purity and low endotoxin content. Figueiredo DB, Carvalho E, Santos MP, Kraschowetz S, Zanardo RT, Campani G, Silva GG, Sargo CR, Horta ACL, de C Giordano R, Miyaji EN, Zangirolami TC, Cabrera-Crespo J, Gonçalves VM. Appl Microbiol Biotechnol 101 2305-2317 (2017)
  15. Broadly Reactive Human Monoclonal Antibodies Targeting the Pneumococcal Histidine Triad Protein Protect against Fatal Pneumococcal Infection. Huang J, Gingerich AD, Royer F, Paschall AV, Pena-Briseno A, Avci FY, Mousa JJ. Infect Immun 89 e00747-20 (2021)
  16. Structures of the L27 Domain of Disc Large Homologue 1 Protein Illustrate a Self-Assembly Module. Ghosh A, Ramagopal UA, Bonanno JB, Brenowitz M, Almo SC. Biochemistry 57 1293-1305 (2018)
  17. Identification of glycosylated regions in pneumococcal PspA conjugated to serotype 6B capsular polysaccharide. Barazzone GC, Pinto V, Donnarumma D, Tanizaki MM, Norais N, Berti F. Glycoconj J 31 259-269 (2014)
  18. Impaired mucociliary motility enhances antigen-specific nasal IgA immune responses to a cholera toxin-based nasal vaccine. Lan H, Suzuki H, Nagatake T, Hosomi K, Ikegami K, Setou M, Kunisawa J. Int Immunol 32 559-568 (2020)
  19. Molecular analyses identifies new domains and structural differences among Streptococcus pneumoniae immune evasion proteins PspC and Hic. Du S, Vilhena C, King S, Sahagún-Ruiz A, Hammerschmidt S, Skerka C, Zipfel PF. Sci Rep 11 1701 (2021)
  20. The Modified Surface Killing Assay Distinguishes between Protective and Nonprotective Antibodies to PspA. Genschmer KR, Vadesilho CFM, McDaniel LS, Park SS, Hale Y, Miyaji EN, Briles DE. mSphere 4 e00589-19 (2019)
  21. Development of a bivalent protein-based vaccine candidate against invasive pneumococcal diseases based on novel pneumococcal surface protein A in combination with pneumococcal histidine triad protein D. Afshari E, Ahangari Cohan R, Shams Nosrati MS, Mousavi SF. Front Immunol 14 1187773 (2023)
  22. Peptide linker increased the stability of pneumococcal fusion protein vaccine candidate. Zane L, Kraschowetz S, Trentini MM, Alves VDS, Araujo SC, Goulart C, Leite LCC, Gonçalves VM. Front Bioeng Biotechnol 11 1108300 (2023)
  23. Pneumococcal Surface Protein A-Hybrid Nanoparticles Protect Mice from Lethal Challenge after Mucosal Immunization Targeting the Lungs. Figueiredo DB, Kaneko K, Rodrigues TDC, MacLoughlin R, Miyaji EN, Saleem I, Gonçalves VM. Pharmaceutics 14 1238 (2022)


Quick links