Mapping ultra-weak protein-protein interactions between heme transporters of Staphylococcus aureus

Journal of Biological Chemistry

Volumn 287, Issue 20, 2012, Pages 16477-16487

  Abe, Ryota ^a   Caaveiro, Jose M M ^a   Kozuka Hata, Hiroko ^a   Oyama, Masaaki ^a   Tsumoto, Kouhei ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL INFECTIONS; CELL WALLS; ESSENTIAL NUTRIENTS; HOST ORGANISM; IRON PORPHYRIN; PHOTOCROSS-LINKING; PROTEIN STRUCTURAL MOTIFS; PROTEIN-PROTEIN INTERACTIONS; RELAY POINTS; S. AUREUS; STAPHYLOCOCCUS AUREUS; STRUCTURAL ELEMENTS; STRUCTURAL MODELS; TRANSIENT INTERACTIONS; UPDATED MODEL;

BACTERIA; IRON; MODEL STRUCTURES; PROTEINS;

PORPHYRINS;

BACTERIAL PROTEIN; HEME; HEME TRANSPORTER; IRON REGULATED SURFACE DETERMINANT A TRANSPORTER; IRON REGULATED SURFACE DETERMINANT C TRANSPORTER; IRON REGULATED SURFACE DETERMINANT E TRANSPORTER; IRON REGULATED SURFACE DETERMINANT PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL WALL; CHIMERA; DIMERIZATION; MOLECULAR MODEL; MOLECULAR PROBE; NONHUMAN; PHOTOREACTIVITY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN CROSS LINKING; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN TRANSPORT; STAPHYLOCOCCUS AUREUS;

AMINO ACID MOTIFS; ANTIGENS, BACTERIAL; BIOLOGICAL TRANSPORT; CARRIER PROTEINS; HEME; STAPHYLOCOCCUS AUREUS;

BACTERIA (MICROORGANISMS); STAPHYLOCOCCUS AUREUS;

EID: 84860875494     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.346700     Document Type: Article

References (54)

1. Lowy, F. D. (1998) Staphylococcus aureus infections. N. Engl. J. Med. 339, 520-532
2. Streit, J. M., Jones, R. N., Sader, H. S., and Fritsche, T. R. (2004) Assessment of pathogen occurrences and resistance profiles among infected patients in the intensive care unit: report from the SENTRY Antimicrobial Surveillance Program (North America, 2001). Int. J. Antimicrob. Agents 24, 111-118 (Pubitemid 38993688)
3. Springer, B., Orendi, U., Much, P., Höger, G., Ruppitsch, W., Krziwanek, K., Metz-Gercek, S., and Mittermayer, H. (2009) Methicillin-resistant Staphylococcus aureus: a new zoonotic agent? Wien. Klin. Wochenschr. 121, 86-90
4. Cheng, A. G., DeDent, A. C., Schneewind, O., and Missiakas, D. (2011) A play in four acts: Staphylococcus aureus abscess formation. Trends Microbiol. 19, 225-232
5. Smith, T. L., Pearson, M. L., Wilcox, K. R., Cruz, C., Lancaster, M. V., Robinson-Dunn, B., Tenover, F. C., Zervos, M. J., Band, J. D., White, E., and Jarvis, W. R. (1999) Emergence of vancomycin resistance in Staphylococcus aureus. N. Engl. J. Med. 340, 493-501 (Pubitemid 29093284)
6. Rybak, M. J., and Akins, R. L. (2001) Emergence of methicillin-resistant Staphylococcus aureus with intermediate glycopeptide resistance: clinical significance and treatment options. Drugs 61, 1-7 (Pubitemid 32108318)
7. Klevens, R. M., Morrison, M. A., Nadle, J., Petit, S., Gershman, K., Ray, S., Harrison, L. H., Lynfield, R., Dumyati, G., Townes, J. M., Craig, A. S., Zell, E. R., Fosheim, G. E., McDougal, L. K., Carey, R. B., and Fridkin, S. K. (2007) Invasive methicillin-resistant Staphylococcus aureus infections in the United States. JAMA 298, 1763-1771 (Pubitemid 47598444)
8. Kuklin, N. A., Clark, D. J., Secore, S., Cook, J., Cope, L. D., McNeely, T., Noble, L., Brown, M. J., Zorman, J. K., Wang, X. M., Pancari, G., Fan, H., Isett, K., Burgess, B., Bryan, J., Brownlow, M., George, H., Meinz, M., Liddell, M. E., Kelly, R., Schultz, L., Montgomery, D., Onishi, J., Losada, M., Martin, M., Ebert, T., Tan, C. Y., Schofield, T. L., Nagy, E., Meineke, A., Joyce, J. G., Kurtz, M. B., Caulfield, M. J., Jansen, K. U., McClements, W., and Anderson, A. S. (2006) A novel Staphylococcus aureus vaccine: iron surface determinant B induces rapid antibody responses in rhesus macaques and specific increased survival in a murine S. aureus sepsis model. Infect. Immun. 74, 2215-2223
9. Stranger-Jones, Y. K., Bae, T., and Schneewind, O. (2006) Vaccine assembly from surface proteins of Staphylococcus aureus. Proc. Natl. Acad. Sci. U.S.A. 103, 16942-16947 (Pubitemid 44737357)
10. Kim, H. K., DeDent, A., Cheng, A. G., McAdow, M., Bagnoli, F., Missiakas, D. M., and Schneewind, O. (2010) IsdA and IsdB antibodies protect mice against Staphylococcus aureus abscess formation and lethal challenge. Vaccine 28, 6382-6392
11. Mazmanian, S. K., Skaar, E. P., Gaspar, A. H., Humayun, M., Gornicki, P., Jelenska, J., Joachmiak, A., Missiakas, D. M., and Schneewind, O. (2003) Passage of heme iron across the envelope of Staphylococcus aureus. Science 299, 906-909 (Pubitemid 36182452)
12. Grigg, J. C., Ukpabi, G., Gaudin, C. F., and Murphy, M. E. (2010) Structural biology of heme binding in the Staphylococcus aureus Isd system. J. Inorg. Biochem. 104, 341-348
13. Skaar, E. P., and Schneewind, O. (2004) Iron-regulated surface determinants (Isd) of Staphylococcus aureus: stealing iron from heme. Microbes Infect. 6, 390-397 (Pubitemid 38393820)
14. Mazmanian, S. K., Ton-That, H., Su, K., and Schneewind, O. (2002) An iron-regulated sortase anchors a class of surface protein during Staphylococcus aureus pathogenesis. Proc. Natl. Acad. Sci. U.S.A. 99, 2293-2298 (Pubitemid 34169054)
15. Sharp, K. H., Schneider, S., Cockayne, A., and Paoli, M. (2007) Crystal structure of the heme-IsdC complex, the central conduit of the Isd iron/ heme uptake system in Staphylococcus aureus. J. Biol. Chem. 282, 10625-10631 (Pubitemid 47093412)
16. Grigg, J. C., Vermeiren, C. L., Heinrichs, D. E., and Murphy, M. E. (2007) Heme recognition by a Staphylococcus aureus NEAT domain. Mol. Microbiol. 63, 139-149 (Pubitemid 44968115)
17. Villareal, V. A., Pilpa, R. M., Robson, S. A., Fadeev, E. A., and Clubb, R. T. (2008) The IsdC protein from Staphylococcus aureus uses a flexible binding pocket to capture heme. J. Biol. Chem. 283, 31591-31600
18. Watanabe, M., Tanaka, Y., Suenaga, A., Kuroda, M., Yao, M., Watanabe, N., Arisaka, F., Ohta, T., Tanaka, I., and Tsumoto, K. (2008) Structural basis for multimeric heme complexation through a specific protein-heme interaction: the case of the third NEAT domain of IsdH from Staphylococcus aureus. J. Biol. Chem. 283, 28649-28659
19. Moriwaki, Y., Caaveiro, J. M., Tanaka, Y., Tsutsumi, H., Hamachi, I., and Tsumoto, K. (2011) Molecular basis of recognition of antibacterial porphyrins by heme transporter IsdH-NEAT3 of Staphylococcus aureus. Biochemistry 50, 7311-7320
20. Gaudin, C. F., Grigg, J. C., Arrieta, A. L., and Murphy, M. E. (2011) Unique heme iron coordination by the hemoglobin receptor IsdB of Staphylococcus aureus. Biochemistry 50, 5443-5452
21. Grigg, J. C., Mao, C. X., and Murphy, M. E. (2011) Iron-coordinating tyrosine is a key determinant of NEAT domain heme transfer. J. Mol. Biol. 413, 684-698
22. Fabian, M., Solomaha, E., Olson, J. S., and Maresso, A. W. (2009) Heme transfer to the bacterial cell envelope occurs via a secreted hemophore in the Gram-positive pathogen Bacillus anthracis. J. Biol. Chem. 284, 32138-32146
23. Ouattara, M., Cunha, E. B., Li, X., Huang, Y. S., Dixon, D., and Eichenbaum, Z. (2010) Shr of group A streptococcus is a new type of composite NEAT protein involved in sequestering heme from methemoglobin. Mol. Microbiol. 78, 739-756
24. Grigg, J. C., Vermeiren, C. L., Heinrichs, D. E., and Murphy, M. E. (2007) Heme coordination by Staphylococcus aureus IsdE. J. Biol. Chem. 282, 28815-28822 (Pubitemid 47606047)
25. Ho, W. W., Li, H., Eakanunkul, S., Tong, Y., Wilks, A., Guo, M., and Poulos, T. L. (2007) Holo- and apo-bound structures of bacterial periplasmic heme-binding proteins. J. Biol. Chem. 282, 35796-35802 (Pubitemid 350277105)
26. Berntsson, R. P., Smits, S. H., Schmitt, L., Slotboom, D. J., and Poolman, B. (2010) A structural classification of substrate-binding proteins. FEBS Lett. 584, 2606-2617
27. Villareal, V. A., Spirig, T., Robson, S. A., Liu, M., Lei, B., and Clubb, R. T. (2011) Transient weak protein-protein complexes transfer heme across the cell wall of Staphylococcus aureus. J. Am. Chem. Soc. 133, 14176-14179
28. Beveridge, T. J., and Matias, V. R. (2006) in Gram-positive Pathogens (Fischetti, V. A., Novick, R. P., Ferretti, J. J., Portnoy, D. A., and Rood, J. I., eds) 2nd Ed., pp. 3-11, ASM Press, Washington, D.C.
29. Zhu, H., Xie, G., Liu, M., Olson, J. S., Fabian, M., Dooley, D. M., and Lei, B. (2008) Pathway for heme uptake from human methemoglobin by the iron-regulated surface determinants system of Staphylococcus aureus. J. Biol. Chem. 283, 18450-18460
30. Muryoi, N., Tiedemann, M. T., Pluym, M., Cheung, J., Heinrichs, D. E., and Stillman, M. J. (2008) Demonstration of the iron-regulated surface determinant (Isd) heme transfer pathway in Staphylococcus aureus. J. Biol. Chem. 283, 28125-28136
31. Miroux, B., and Walker, J. E. (1996) Overproduction of proteins in Escherichia coli: mutant hosts that allow synthesis of some membrane proteins and globular proteins at high levels. J. Mol. Biol. 260, 289-298 (Pubitemid 26254109)
32. Kawai, T., Caaveiro, J. M., Abe, R., Katagiri, T., and Tsumoto, K. (2011) Catalytic activity of MsbA reconstituted in nanodisc particles is modulated by remote interactions with the bilayer. FEBS Lett. 585, 3533-3537
33. Burkhard, K. A., and Wilks, A. (2007) Characterization of the outer membrane receptor ShuA from the heme uptake system of Shigella dysenteriae. Substrate specificity and identification of the heme protein ligands. J. Biol. Chem. 282, 15126-15136 (Pubitemid 47093339)
34. Young, T. S., Ahmad, I., Yin, J. A., and Schultz, P. G. (2010) An enhanced system for unnatural amino acid mutagenesis in E. coli. J. Mol. Biol. 395, 361-374
35. Farrell, I. S., Toroney, R., Hazen, J. L., Mehl, R. A., and Chin, J. W. (2005) Photo-cross-linking interacting proteins with a genetically encoded benzophenone. Nat. Methods 2, 377-384 (Pubitemid 41130984)
36. Olsen, J. V., de Godoy, L. M., Li, G., Macek, B., Mortensen, P., Pesch, R., Makarov, A., Lange, O., Horning, S., and Mann, M. (2005) Parts per million mass accuracy on an Orbitrap mass spectrometer via lock mass injection into a C-trap. Mol. Cell. Proteomics 4, 2010-2021 (Pubitemid 41830195)
37. Maiolica, A., Cittaro, D., Borsotti, D., Sennels, L., Ciferri, C., Tarricone, C., Musacchio, A., and Rappsilber, J. (2007) Structural analysis of multiprotein complexes by cross-linking, mass spectrometry, and database searching. Mol. Cell. Proteomics 6, 2200-2211
38. Liu, M., Tanaka, W. N., Zhu, H., Xie, G., Dooley, D. M., and Lei, B. (2008) Direct hemin transfer from IsdA to IsdC in the iron-regulated surface determinant (Isd) heme acquisition system of Staphylococcus aureus. J. Biol. Chem. 283, 6668-6676
39. Ran, Y., Zhu, H., Liu, M., Fabian, M., Olson, J. S., Aranda, R., 4th, Phillips, G. N., Jr., Dooley, D. M., and Lei, B. (2007) Bis-methionine ligation to heme iron in the streptococcal cell surface protein Shp facilitates rapid hemin transfer to HtsA of the HtsABC transporter. J. Biol. Chem. 282, 31380-31388 (Pubitemid 350044855)
40. Nygaard, T. K., Blouin, G. C., Liu, M., Fukumura, M., Olson, J. S., Fabian, M., Dooley, D. M., and Lei, B. (2006) The mechanism of direct heme transfer from the streptococcal cell surface protein Shp to HtsA of the HtsABC transporter. J. Biol. Chem. 281, 20761-20771 (Pubitemid 44115417)
41. Dormán, G., and Prestwich, G. D. (1994) Benzophenone photophores in biochemistry. Biochemistry 33, 5661-5673 (Pubitemid 24184566)
42. Sato, S., Mimasu, S., Sato, A., Hino, N., Sakamoto, K., Umehara, T., and Yokoyama, S. (2011) Crystallographic study of a site-specifically cross-linked protein complex with a genetically incorporated photoreactive amino acid. Biochemistry 50, 250-257
43. Kusano, S., Kukimoto-Niino, M., Hino, N., Ohsawa, N., Okuda, K., Sakamoto, K., Shirouzu, M., Shindo, T., and Yokoyama, S. (2012) Structural basis for extracellular interactions between calcitonin receptor-like receptor and receptor activity-modifying protein 2 for adrenomedullin-specific binding. Protein Sci. 21, 199-210
44. Majmudar, C. Y., Wang, B., Lum, J. K., Håkansson, K., and Mapp, A. K. (2009) A high-resolution interaction map of three transcriptional activation domains with a key coactivator from photo-cross-linking and multiplexed mass spectrometry. Angew. Chem. Int. Ed Engl. 48, 7021-7024
45. Ye, S., Köhrer, C., Huber, T., Kazmi, M., Sachdev, P., Yan, E. C., Bhagat, A., RajBhandary, U. L., and Sakmar, T. P. (2008) Site-specific incorporation of keto amino acids into functional G protein-coupled receptors using unnatural amino acid mutagenesis. J. Biol. Chem. 283, 1525-1533
46. Mori, H., and Ito, K. (2006) Different modes of SecY-SecA interactions revealed by site-directed in vivo photo-cross-linking. Proc. Natl. Acad. Sci. U.S.A. 103, 16159-16164 (Pubitemid 44715167)
47. Okuda, S., and Tokuda, H. (2009) Model of mouth-to-mouth transfer of bacterial lipoproteins through inner membrane LolC, periplasmic LolA, and outer membrane LolB. Proc. Natl. Acad. Sci. U.S.A. 106, 5877-5882
48. Shiota, T., Mabuchi, H., Tanaka-Yamano, S., Yamano, K., and Endo, T. (2011) In vivo protein interaction mapping of mitochondrial translocator protein Tom22 at work. Proc. Natl. Acad. Sci. U.S.A. 108, 15179-15183
49. Krishnamurthy, M., Dugan, A., Nwokoye, A., Fung, Y. H., Lancia, J. K., Majmudar, C. Y., and Mapp, A. K. (2011) Caught in the act: covalent cross-linking captures activator-coactivator interactions in vivo. ACS Chem. Biol. 6, 1321-1326
50. Krissinel, E., and Henrick, K. (2007) Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 372, 774-797 (Pubitemid 47321791)
51. Reniere, M. L., Torres, V. J., and Skaar, E. P. (2007) Intracellular metalloporphyrin metabolism in Staphylococcus aureus. Biometals 20, 333-345 (Pubitemid 46776560)
52. Tiedemann, M. T., Muryoi, N., Heinrichs, D. E., and Stillman, M. J. (2008) Iron acquisition by the heme-binding Isd proteins in Staphylococcus aureus: studies of the mechanism using magnetic circular dichroism. Biochem. Soc. Trans. 36, 1138-1143
53. Rowe, A. J. (2011) Ultra-weak reversible protein-protein interactions. Methods 54, 157-166
54. Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., and Ferrin, T. E. (2004) UCSF chimera: a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612