Specificity of Staphyloferrin B Recognition by the SirA Receptor from Staphylococcus aureus

Grigg, Jason C.; Cheung, Johnson; Heinrichs, David E.; Murphy, Michael E.  P.

doi:10.1074/jbc.m110.172924

Specificity of Staphyloferrin B Recognition by the SirA Receptor from Staphylococcus aureus

Journal Article · Mon Nov 01 00:00:00 EDT 2010 · Journal of Biological Chemistry

DOI:https://doi.org/10.1074/jbc.m110.172924· OSTI ID:1625072

Grigg, Jason C. ^[1]; Cheung, Johnson ^[2]; Heinrichs, David E. ^[2]; Murphy, Michael E. P. ^[3]

Univ. of British Columbia, Vancouver, BC (Canada). Life Sciences Inst., Dept. of Microbiology and Immunology; DOE/OSTI
Univ. of Western Ontario, London, ON (Canada). Dept. of Microbiology and Immunology
Univ. of British Columbia, Vancouver, BC (Canada). Life Sciences Inst., Dept. of Microbiology and Immunology

Many organisms use sophisticated systems to acquire growth-limiting iron. Iron limitation is especially apparent in bacterial pathogens of mammalian hosts where free iron concentrations are physiologically negligible. A common strategy is to secrete low molecular weight iron chelators, termed siderophores, and express high affinity receptors for the siderophore-iron complex. Staphylococcus aureus, a widespread pathogen, produces two siderophores, staphyloferrin A (SA) and staphyloferrin B (SB). We have determined the crystal structure of the staphyloferrin B receptor, SirA, at high resolution in both the apo and Fe(III)-SB (FeSB)-bound forms. SirA, a member of the class III binding protein family of metal receptors, has N- and C-terminal domains, each composed of mainly a β-stranded core and α-helical periphery. The domains are bridged by a single α-helix and together form the FeSB binding site. SB coordinates Fe(III) through five oxygen atoms and one nitrogen atom in distorted octahedral geometry. SirA undergoes conformational change upon siderophore binding, largely securing two loops from the C-terminal domain to enclose FeSB with a low nanomolar dissociation constant. The staphyloferrin A receptor, HtsA, homologous to SirA, also encloses its cognate siderophore (FeSA); however, the largest conformational rearrangements involve a different region of the C-terminal domain. FeSB is uniquely situated in the binding pocket of SirA with few of the contacting residues being conserved with those of HtsA interacting with FeSA. Although both SirA and HtsA bind siderophores from the same α-hydroxycarboxylate class, the unique structural features of each receptor provides an explanation for their distinct specificity.

View Accepted Manuscript (DOE)

Research Organization:: SLAC National Accelerator Laboratory, Menlo Park, CA (United States). Stanford Synchrotron Radiation Lightsource (SSRL)

Sponsoring Organization:: Canadian Institutes of Health Research (CIHR); Michael Smith Foundation for Health Research; National Center for Research Resources (NCRR); National Institute of General Medical Sciences (NIGMS); National Institutes of Health (NIH); Natural Sciences and Engineering Research Council of Canada (NSERC); USDOE Office of Science (SC), Basic Energy Sciences (BES); USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-76SF00515

OSTI ID:: 1625072

Journal Information:: Journal of Biological Chemistry, Journal Name: Journal of Biological Chemistry Journal Issue: 45 Vol. 285; ISSN 0021-9258

Publisher:: American Society for Biochemistry and Molecular BiologyCopyright Statement

Country of Publication:: United States

Language:: English

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Discovery of an Iron-Regulated Citrate Synthase in Staphylococcus aureus Cheung, Johnson; Murphy, Michael E. P.; Heinrichs, David E. Chemistry & Biology, Vol. 19, Issue 12 https://doi.org/10.1016/j.chembiol.2012.10.003	journal	December 2012
Synthesis of L-2,3-Diaminopropionic Acid, a Siderophore and Antibiotic Precursor Kobylarz, Marek J.; Grigg, Jason C.; Takayama, Shin-ichi J. Chemistry & Biology, Vol. 21, Issue 3 https://doi.org/10.1016/j.chembiol.2013.12.011	journal	March 2014
Mutation of L-2,3-diaminopropionic acid synthase genes blocks staphyloferrin B synthesis in Staphylococcus aureus Beasley, Federico C.; Cheung, Johnson; Heinrichs, David E. BMC Microbiology, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2180-11-199	journal	January 2011
The iron-regulated staphylococcal lipoproteins Sheldon, Jessica R.; Heinrichs, David E. Frontiers in Cellular and Infection Microbiology, Vol. 2 https://doi.org/10.3389/fcimb.2012.00041	journal	January 2012
Additional file 1 of Immunoproteomic analysis of the serum IgG response to cell wall-associated proteins of Staphylococcus aureus strains belonging to CC97 and CC151 Drumm, Shauna D.; Cormican, Paul; Owens, Rebecca A. figshare https://doi.org/10.6084/m9.figshare.24159357	dataset	January 2023
Additional file 2 of Immunoproteomic analysis of the serum IgG response to cell wall-associated proteins of Staphylococcus aureus strains belonging to CC97 and CC151 Drumm, Shauna D.; Cormican, Paul; Owens, Rebecca A. figshare https://doi.org/10.6084/m9.figshare.24159360	dataset	January 2023
Additional file 3 of Immunoproteomic analysis of the serum IgG response to cell wall-associated proteins of Staphylococcus aureus strains belonging to CC97 and CC151 Drumm, Shauna D.; Cormican, Paul; Owens, Rebecca A. figshare https://doi.org/10.6084/m9.figshare.24159363	dataset	January 2023
Drug delivery systems designed to overcome antimicrobial resistance Pham, Thanh‐Nhat; Loupias, Pauline; Dassonville‐Klimpt, Alexandra Medicinal Research Reviews, Vol. 39, Issue 6 https://doi.org/10.1002/med.21588	journal	April 2019
Effect of combined oxidative and nitrosative stresses on Staphylococcus aureus transcriptome Nobre, Lígia S.; Saraiva, Lígia M. Applied Microbiology and Biotechnology, Vol. 97, Issue 6 https://doi.org/10.1007/s00253-013-4730-3	journal	February 2013
Metal ion acquisition in Staphylococcus aureus: overcoming nutritional immunity Cassat, James E.; Skaar, Eric P. Seminars in Immunopathology, Vol. 34, Issue 2 https://doi.org/10.1007/s00281-011-0294-4	journal	November 2011
Exploring Staphylococcus aureus pathways to disease for vaccine development DeDent, Andrea; Kim, Hwan Keun; Missiakas, Dominique Seminars in Immunopathology, Vol. 34, Issue 2 https://doi.org/10.1007/s00281-011-0299-z	journal	December 2011
Staphylococcus aureus heme and siderophore-iron acquisition pathways Conroy, Brigid S.; Grigg, Jason C.; Kolesnikov, Maxim BioMetals, Vol. 32, Issue 3 https://doi.org/10.1007/s10534-019-00188-2	journal	March 2019
Involvement of major facilitator superfamily proteins SfaA and SbnD in staphyloferrin secretion in Staphylococcus aureus Hannauer, Mélissa; Sheldon, Jessica R.; Heinrichs, David E. FEBS Letters, Vol. 589, Issue 6 https://doi.org/10.1016/j.febslet.2015.02.002	journal	February 2015
Structural and functional characterization of the Staphylococcus aureus virulence factor and vaccine candidate FhuD2 Mariotti, Paolo; Malito, Enrico; Biancucci, Marco Biochemical Journal, Vol. 449, Issue 3 https://doi.org/10.1042/bj20121426	journal	January 2013
The Solution Structure, Binding Properties, and Dynamics of the Bacterial Siderophore-binding Protein FepB Chu, Byron C. H.; Otten, Renee; Krewulak, Karla D. Journal of Biological Chemistry, Vol. 289, Issue 42 https://doi.org/10.1074/jbc.m114.564021	journal	October 2014
Recent developments in understanding the iron acquisition strategies of gram positive pathogens Sheldon, Jessica R.; Heinrichs, David E. FEMS Microbiology Reviews, Vol. 39, Issue 4 https://doi.org/10.1093/femsre/fuv009	journal	April 2015
Involvement of reductases IruO and NtrA in iron acquisition by S taphylococcus aureus: IruO and NtrA involvement in iron acquisition Hannauer, Mélissa; Arifin, Andrew J.; Heinrichs, David E. Molecular Microbiology, Vol. 96, Issue 6 https://doi.org/10.1111/mmi.13000	journal	April 2015
The Staphylococcus aureus ArlRS two‐component system regulates virulence factor expression through MgrA Crosby, Heidi A.; Tiwari, Nitija; Kwiecinski, Jakub M. Molecular Microbiology, Vol. 113, Issue 1 https://doi.org/10.1111/mmi.14404	journal	November 2019
Staphylococcus aureus Transporters Hts, Sir, and Sst Capture Iron Liberated from Human Transferrin by Staphyloferrin A, Staphyloferrin B, and Catecholamine Stress Hormones, Respectively, and Contribute to Virulence Beasley, Federico C.; Marolda, Cristina L.; Cheung, Johnson Infection and Immunity, Vol. 79, Issue 6 https://doi.org/10.1128/iai.00117-11	journal	March 2011

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