Discrete and structurally unique proteins (ta¯pirins) mediate attachment of extremely thermophilic Caldicellulosiruptor species to cellulose

Journal of Biological Chemistry

Volumn 290, Issue 17, 2015, Pages 10645-10656

  Blumer Schuette, Sara E ^a,d   Alahuhta, Markus ^b   Conway, Jonathan M ^a   Lee, Laura L ^a   Zurawski, Jeffrey V ^a   Giannone, Richard J ^c   Hettich, Robert L ^c   Lunin, Vladimir V ^b   Himmel, Michael E ^b   Kelly, Robert M ^a  

^a North Carolina State University   (United States)

^b NATIONAL RENEWABLE ENERGY LABORATORY   (United States)

^c OAK RIDGE NATIONAL LABORATORY   (United States)

^d OAKLAND UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BACTERIA; BIOINFORMATICS; CARBOHYDRATES; CELLULOSE; ENZYMES; HYDROLASES; LIGNIN; MOLECULAR BIOLOGY;

ATP BINDING CASSETTE TRANSPORTERS; CARBOHYDRATE BINDING MODULES; CARBOHYDRATE CONTENT; EXTRACELLULAR PROTEINS; GLYCOSIDE HYDROLASES; HYPOTHETICAL PROTEIN; POLYPEPTIDE STRUCTURES; SUBSTRATE BINDING PROTEINS;

PROTEINS;

CELLULASE; CELLULOSE; PROTEIN; TAPARIN; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; RECOMBINANT PROTEIN;

ADSORPTION; AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL GROWTH; BINDING AFFINITY; BIODEGRADATION; BIOFUEL PRODUCTION; BIOINFORMATICS; CALDICELLULOSIRUPTOR; CALDICELLULOSIRUPTOR BESCII; CALDICELLULOSIRUPTOR HYDROTHERMALIS; CALDICELLULOSIRUPTOR KRISTJANSSONII; CALDICELLULOSIRUPTOR KRONOTSKYENSIS; CALDICELLULOSIRUPTOR LACTOACETICUS; CALDICELLULOSIRUPTOR OWENSENSIS; CALDICELLULOSIRUPTOR SACCHAROLYTICUS; CARBOXY TERMINAL SEQUENCE; CELL ADHESION; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLIZATION; ENZYME SUBSTRATE COMPLEX; HYPERTHERMOPHILIC BACTERIUM; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEOMICS; STRUCTURE ANALYSIS; BACTERIAL GENE; BACTERIUM; BACTERIUM ADHERENCE; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; FIMBRIA; GENETICS; METABOLISM; MICROBIOLOGY; PHYLOGENY; PHYSIOLOGY; PLANT; PROTEIN TERTIARY STRUCTURE; ULTRASTRUCTURE;

BACTERIA (MICROORGANISMS); CALDICELLULOSIRUPTOR;

ADSORPTION; BACTERIA; BACTERIAL ADHESION; BACTERIAL PROTEINS; BINDING SITES; CELLULOSE; FIMBRIAE, BACTERIAL; GENES, BACTERIAL; MODELS, MOLECULAR; PHYLOGENY; PLANTS; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS;

EID: 84928390955     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.641480     Document Type: Article

References (75)

1. Gilkes, N. R., Warren, R. A., Miller, R. C., Jr., and Kilburn, D. G. (1988) Precise excision of the cellulose binding domains from two Cellulomonas fimi cellulases by a homologous protease and the effect on catalysis. J. Biol. Chem. 263, 10401-10407
2. Tomme, P., Van Tilbeurgh, H., Pettersson, G., Van Damme, J., Vandekerckhove, J., Knowles, J., Teeri, T., and Claeyssens, M. (1988) Studies of the cellulolytic system of Trichoderma reesei QM 9414. Eur. J. Biochem. 170, 575-581
3. Boraston, A. B., Bolam, D. N., Gilbert, H. J., and Davies, G. J. (2004) Carbohydrate-binding modules: fine-tuning polysaccharide recognition. Biochem. J. 382, 769-781
4. Cantarel, B. L., Coutinho, P. M., Rancurel, C., Bernard, T., Lombard, V., and Henrissat, B. (2009) The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res. 37, D233-D238
5. Brulc, J. M., Antonopoulos, D. A., Miller, M. E., Wilson, M. K., Yannarell, A. C., Dinsdale, E. A., Edwards, R. E., Frank, E. D., Emerson, J. B., Wacklin, P., Coutinho, P. M., Henrissat, B., Nelson, K. E., and White, B. A. (2009) Gene-centric metagenomics of the fiber-adherent bovine rumen microbiome reveals forage specific glycoside hydrolases. Proc. Natl. Acad. Sci. U.S.A. 106, 1948-1953
6. Hess, M., Sczyrba, A., Egan, R., Kim, T. W., Chokhawala, H., Schroth, G., Luo, S., Clark, D. S., Chen, F., Zhang, T., Mackie, R. I., Pennacchio, L. A., Tringe, S. G., Visel, A., Woyke, T., et al. (2011) Metagenomic discovery of biomass-degrading genes and genomes from cow rumen. Science 331, 463-467
7. Warnecke, F., Luginbühl, P., Ivanova, N., Ghassemian, M., Richardson, T. H., Stege, J. T., Cayouette, M., McHardy, A. C., Djordjevic, G., Aboushadi, N., Sorek, R., Tringe, S. G., Podar, M., Martin, H. G., Kunin, V., et al. (2007) Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature 450, 560-565
8. Mello, L. V., Chen, X., and Rigden, D. J. (2010) Mining metagenomic data for novel domains: BACON, a new carbohydrate-binding module. FEBS Lett. 584, 2421-2426
9. Rigden, D. J., Eberhardt, R. Y., Gilbert, H. J., Xu, Q., Chang, Y., and Godzik, A. (2014) Structure- and context-based analysis of the GxGYxYP family reveals a new putative class of glycoside hydrolase. BMC Bioinformatics 15, 196
10. Suen, G., Weimer, P. J., Stevenson, D. M., Aylward, F. O., Boyum, J., Deneke, J., Drinkwater, C., Ivanova, N. N., Mikhailova, N., Chertkov, O., Goodwin, L. A., Currie, C. R., Mead, D., and Brumm, P. J. (2011) The complete genome sequence of Fibrobacter succinogenes S85 reveals a cellulolytic and metabolic specialist. PLoS ONE 6, e18814
11. Jun, H. S., Qi, M., Gong, J., Egbosimba, E. E., and Forsberg, C. W. (2007) Outer membrane proteins of Fibrobacter succinogenes with potential roles in adhesion to cellulose and in cellulose digestion. J. Bacteriol. 189, 6806-6815
12. Gong, J., Egbosimba, E. E., and Forsberg, C. W. (1996) Cellulose-binding proteins of Fibrobacter succinogenes and the possible role of a 180-kDa cellulose-binding glycoprotein in adhesion to cellulose. Can. J. Microbiol. 42, 453-460
13. Ezer, A., Matalon, E., Jindou, S., Borovok, I., Atamna, N., Yu, Z., Morrison, M., Bayer, E. A., and Lamed, R. (2008) Cell surface enzyme attachment is mediated by family 37 carbohydrate-binding modules, unique to Ruminococcus albus. J. Bacteriol. 190, 8220-8222
14. Xu, Q., Morrison, M., Nelson, K. E., Bayer, E. A., Atamna, N., and Lamed, R. (2004) A novel family of carbohydrate-binding modules identified with Ruminococcus albus proteins. FEBS Lett. 566, 11-16
15. Rakotoarivonina, H., Larson, M. A., Morrison, M., Girardeau, J. P., Gaillard-Martinie, B., Forano, E., and Mosoni, P. (2005) The Ruminococcus albus pilA1-pilA2 locus: expression and putative role of two adjacent pil genes in pilus formation and bacterial adhesion to cellulose. Microbiology 151, 1291-1299
16. Pegden, R. S., Larson, M. A., Grant, R. J., and Morrison, M. (1998) Adherence of the Gram-positive bacterium Ruminococcus albus to cellulose and identification of a novel form of cellulose-binding protein which belongs to the Pil family of proteins. J. Bacteriol. 180, 5921-5927
17. Mosoni, P., and Gaillard-Martinie, B. (2001) Characterization of a spontaneous adhesion-defective mutant of Ruminococcus albus strain 20. Arch. Microbiol. 176, 52-61
18. Vodovnik, M., Duncan, S. H., Reid, M. D., Cantlay, L., Turner, K., Parkhill, J., Lamed, R., Yeoman, C. J., Berg Miller, M. E., White, B. A., Bayer, E. A., Marinšek-Logar, R., and Flint, H. J. (2013) Expression of cellulosome components and type IV pili within the extracellular proteome of Ruminococcus flavefaciens 007. PLoS ONE 8, e65333
19. Te'o, V. S., Saul, D. J., and Bergquist, P. L. (1995) celA, another gene coding for a multidomain cellulase from the extreme thermophile Caldocellum saccharolyticum. Appl. Microbiol. Biotechnol. 43, 291-296
20. Gibbs, M. D., Saul, D. J., Lüthi, E., and Bergquist, P. L. (1992) The β-mannanase from "Caldocellum saccharolyticum" is part of a multidomain enzyme. Appl. Environ. Microbiol. 58, 3864-3867
21. Brunecky, R., Alahuhta, M., Xu, Q., Donohoe, B. S., Crowley, M. F., Kataeva, I. A., Yang, S. J., Resch, M. G., Adams, M. W., Lunin, V. V., Himmel, M. E., and Bomble, Y. J. (2013) Revealing nature's cellulase diversity: the digestion mechanism of Caldicellulosiruptor bescii CelA. Science 342, 1513-1516
22. Blumer-Schuette, S. E., Brown, S. D., Sander, K. B., Bayer, E. A., Kataeva, I., Zurawski, J. V., Conway, J. M., Adams, M. W., and Kelly, R. M. (2014) Thermophilic lignocellulose deconstruction. FEMS Microbiol. Rev. 38, 393-448
23. Gibbs, M. D., Reeves, R. A., Farrington, G. K., Anderson, P., Williams, D. P., and Bergquist, P. L. (2000) Multidomain and multifunctional glycosyl hydrolases from the extreme thermophile Caldicellulosiruptor isolate Tok7B.1. Curr. Microbiol. 40, 333-340
24. Blumer-Schuette, S. E., Giannone, R. J., Zurawski, J. V., Ozdemir, I., Ma, Q., Yin, Y., Xu, Y., Kataeva, I., Poole, F. L., 2nd, Adams, M. W., Hamilton-Brehm, S. D., Elkins, J. G., Larimer, F. W., Land, M. L., Hauser, L. J., et al. (2012) Caldicellulosiruptor core and pangenomes reveal determinants for noncellulosomal thermophilic deconstruction of plant biomass. J. Bacteriol. 194, 4015-4028
25. Blumer-Schuette, S. E., Lewis, D. L., and Kelly, R. M. (2010) Phylogenetic, microbiological, and glycoside hydrolase diversities within the extremely thermophilic, plant biomass-degrading genus Caldicellulosiruptor. Appl. Environ. Microbiol. 76, 8084-8092
26. Young, J., Chung, D., Bomble, Y. J., Himmel, M. E., and Westpheling, J. (2014) Deletion of Caldicellulosiruptor bescii CelA reveals its crucial role in the deconstruction of lignocellulosic biomass. Biotechnol. Biofuels 7, 142
27. Vanfossen, A. L., Lewis, D. L., Nichols, J. D., and Kelly, R. M. (2008) Polysaccharide degradation and synthesis by extremely thermophilic anaerobes. Ann. N.Y. Acad. Sci. 1125, 322-337
28. Dam, P., Kataeva, I., Yang, S. J., Zhou, F., Yin, Y., Chou, W., Poole, F. L., 2nd, Westpheling, J., Hettich, R., Giannone, R., Lewis, D. L., Kelly, R., Gilbert, H. J., Henrissat, B., Xu, Y., and Adams, M. W. (2011) Insights into plant biomass conversion from the genome of the anaerobic thermophilic bacterium Caldicellulosiruptor bescii DSM 6725. Nucleic Acids Res. 39, 3240-3254
29. Wang, Z. W., Lee, S. H., Elkins, J. G., and Morrell-Falvey, J. L. (2011) fSpatial and temporal dynamics of cellulose degradation and biofilm formation by Caldicellulosiruptor obsidiansis and Clostridium thermocellum. AMB Express 1, 30
30. Ozdemir, I., Blumer-Schuette, S. E., and Kelly, R. M. (2012) S-layer homology domain proteins Csac-0678 and Csac-2722 are implicated in plant polysaccharide deconstruction by the extremely thermophilic bacterium Caldicellulosiruptor saccharolyticus. Appl. Environ. Microbiol. 78, 768-777
31. Vanfossen, A. L., Verhaart, M. R., Kengen, S. M., and Kelly, R. M. (2009) Carbohydrate utilization patterns for the extremely thermophilic bacterium Caldicellulosiruptor saccharolyticus reveal broad growth substrate preferences. Appl. Environ. Microbiol. 75, 7718-7724
32. Yokoyama, H., Yamashita, T., Morioka, R., and Ohmori, H. (2014) Extracellular secretion of noncatalytic plant cell wall-binding proteins by the cellulolytic thermophile Caldicellulosiruptor bescii. J. Bacteriol. 196, 3784-3792
33. Camacho, C., Coulouris, G., Avagyan, V., Ma, N., Papadopoulos, J., Bealer, K., and Madden, T. L. (2009) BLAST+: architecture and applications. BMC Bioinformatics 10, 421
34. Edgar, R. C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792-1797
35. Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S. (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30, 2725-2729
36. Petersen, T. N., Brunak, S., von Heijne, G., and Nielsen, H. (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat. Methods 8, 785-786
37. Krogh, A., Larsson, B., von Heijne, G., and Sonnhammer, E. L. (2001) Predicting transmembrane protein topology with a hidden markov model: application to complete genomes. J. Mol. Biol. 305, 567-580
38. Mitchell, A., Chang, H. Y., Daugherty, L., Fraser, M., Hunter, S., Lopez, R., McAnulla, C., McMenamin, C., Nuka, G., Pesseat, S., Sangrador-Vegas, A., Scheremetjew, M., Rato, C., Yong, S. Y., Bateman, A., et al. (2015) The InterPro protein families database: the classification resource after 15 years. Nucleic Acids Res. 43, D213-D221
39. Studier, F. W. (2005) Protein production by auto-induction in high-density shaking cultures. Protein Expr. Purif. 41, 207-234
40. Boder, E. T., and Wittrup, K. D. (1997) Yeast surface display for screening combinatorial polypeptide libraries. Nat. Biotechnol. 15, 553-557
41. Nam, J.-M., Fujita, Y., Arai, T., Kondo, A., Morikawa, Y., Okada, H., Ueda, M., and Tanaka, A. (2002) Construction of engineered yeast with the ability of binding to cellulose. J. Mol. Catal. B Enzym. 17, 197-202
42. Sreenath, H. K., Bingman, C. A., Buchan, B. W., Seder, K. D., Burns, B. T., Geetha, H. V., Jeon, W. B., Vojtik, F. C., Aceti, D. J., Frederick, R. O., Phillips, G. N., Jr., and Fox, B. G. (2005) Protocols for production of selenomethionine-labeled proteins in 2-L polyethylene terephthalate bottles using auto-induction medium. Protein Expr. Purif. 40, 256-267
43. Winn, M. D., Ballard, C. C., Cowtan, K. D., Dodson, E. J., Emsley, P., Evans, P. R., Keegan, R. M., Krissinel, E. B., Leslie, A. G., McCoy, A., McNicholas, S. J., Murshudov, G. N., Pannu, N. S., Potterton, E. A., Powell, H. R., et al. (2011) Overview of the CCP4 suite and current developments. Acta Crystallogr. D Biol. Crystallogr. 67, 235-242
44. Grosse-Kunstleve, R. W., and Adams, P. D. (2003) Substructure search procedures for macromolecular structures. Acta Crystallogr. D Biol. Crystallogr. 59, 1966-1973
45. McCoy, A. J., Storoni, L. C., and Read, R. J. (2004) Simple algorithm for a maximum-likelihood SAD function. Acta Crystallogr. D Biol. Crystallogr. 60, 1220-1228
46. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007) Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674
47. Skubák, P., and Pannu, N. S. (2013) Automatic protein structure solution from weak X-ray data. Nat. Commun. 10.1038/ncomms3777
48. Murshudov, G. N., Skubák, P., Lebedev, A. A., Pannu, N. S., Steiner, R. A., Nicholls, R. A., Winn, M. D., Long, F., and Vagin, A. A. (2011) REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr. D Biol. Crystallogr. 67, 355-367
49. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501
50. Chen, V. B., Arendall, W. B., 3rd, Headd, J. J., Keedy, D. A., Immormino, R. M., Kapral, G. J., Murray, L. W., Richardson, J. S., and Richardson, D. C. (2010) MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr. 66, 12-21
51. Engh, R. A., and Huber, R. (1991) Accurate bond and angle parameters for x-ray protein-structure refinement. Acta Crystallogr. A Found. Crystallogr. 47, 392-400
52. VanFossen, A. L., Ozdemir, I., Zelin, S. L., and Kelly, R. M. (2011) Glycoside hydrolase inventory drives plant polysaccharide deconstruction by the extremely thermophilic bacterium Caldicellulosiruptor saccharolyticus. Biotechnol. Bioeng. 108, 1559-1569
53. Onyenwoke, R. U., Lee, Y. J., Dabrowski, S., Ahring, B. K., and Wiegel, J. (2006) Reclassification of Thermoanaerobium acetigenum as Caldicellulosiruptor acetigenus comb. nov and emendation of the genus description. Int. J. Syst. Evol. Microbiol. 56, 1391-1395
54. Gera, N., Hussain, M., Wright, R. C., and Rao, B. M. (2011) Highly stable binding proteins derived from the hyperthermophilic Sso7d scaffold. J. Mol. Biol. 409, 601-616
55. Ito, J., Fujita, Y., Ueda, M., Fukuda, H., and Kondo, A. (2004) Improvement of cellulose-degrading ability of a yeast strain displaying Trichoderma reesei endoglucanase II by recombination of cellulose-binding domains. Biotechnol. Prog. 20, 688-691
56. Fan, L.-H., Zhang, Z.-J., Yu, X.-Y., Xue, Y.-X., and Tan, T.-W. (2012) Self-surface assembly of cellulosomes with two miniscaffoldins on Saccharomyces cerevisiae for cellulosic ethanol production. Proc. Natl. Acad. Sci. U.S.A. 109, 13260-13265
57. Baek, S.-H., Kim, S., Lee, K., Lee, J.-K., and Hahn, J.-S. (2012) Cellulosic ethanol production by combination of cellulase-displaying yeast cells. Enzyme Microb. Technol. 51, 366-372
58. Tsai, S.-L., Goyal, G., and Chen, W. (2010) Surface display of a functional minicellulosome by intracellular complementation using a synthetic yeast consortium and its application to cellulose hydrolysis and ethanol production. Appl. Environ. Microbiol. 76, 7514-7520
59. Wen, F., Sun, J., and Zhao, H. (2010) Yeast surface display of trifunctional minicellulosomes for simultaneous saccharification and fermentation of cellulose to ethanol. Appl. Environ. Microbiol. 76, 1251-1260
60. Tomme, P., Boraston, A., McLean, B., Kormos, J., Creagh, A. L., Sturch, K., Gilkes, N. R., Haynes, C. A., Warren, R. A., and Kilburn, D. G. (1998) Characterization and affinity applications of cellulose-binding domains. J. Chromatogr. B Biomed. Sci. Appl. 715, 283-296
61. Georgelis, N., Yennawar, N. H., and Cosgrove, D. J. (2012) Structural basis for entropy-driven cellulose binding by a type-A cellulose-binding module (CBM) and bacterial expansin. Proc. Natl. Acad. Sci. U.S.A. 109, 14830-14835
62. Riedel, K., Ritter, J., Bauer, S., and Bronnenmeier, K. (1998) The modular cellulase CelZ of the thermophilic bacterium Clostridium stercorarium contains a thermostabilizing domain. FEMS Microbiol. Lett. 164, 261-267
63. Din, N., Forsythe, I. J., Burtnick, L. D., Gilkes, N. R., Miller, R. C., Jr., Warren, R. A., and Kilburn, D. G. (1994) The cellulose-binding domain of endoglucanase A (CenA) from Cellulomonas fimi: evidence for the involvement of tryptophan residues in binding. Mol. Microbiol. 11, 747-755
64. Jäger, G., Girfoglio, M., Dollo, F., Rinaldi, R., Bongard, H., Commandeur, U., Fischer, R., Spiess, A. C., and Büchs, J. (2011) How recombinant swollenin from Kluyveromyces lactis affects cellulosic substrates and accelerates their hydrolysis. Biotechnol. Biofuels 4, 33
65. Dong, A., Xu, X., Edwards, A. M., Midwest Center for Structural Genomics, Structural Genomics Consortium, Chang, C., Chruszcz, M., Cuff, M., Cymborowski, M., Di Leo, R., Egorova, O., Evdokimova, E., Filippova, E., Gu, J., Guthrie, J., et al. (2007) In situ proteolysis for protein crystallization and structure determination. Nat. Methods 4, 1019-1021
66. Wernimont, A., and Edwards, A. (2009) In situ proteolysis to generate crystals for structure determination: An update. PLoS ONE 4, e5094
67. Lombard, V., Bernard, T., Rancurel, C., Brumer, H., Coutinho, P. M., and Henrissat, B. (2010) A hierarchical classification of polysaccharide lyases for glycogenomics. Biochem. J. 432, 437-444
68. Krissinel, E., and Henrick, K. (2004) Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr. D Biol. Crystallogr. 60, 2256-2268
69. Close, D. W., D'Angelo, S., and Bradbury, A. R. (2014) A new family of β-helix proteins with similarities to the polysaccharide lyases. Acta Crystallogr. D Biol. Crystallogr. 70, 2583-2592
70. Bayer, E. A., Belaich, J. P., Shoham, Y., and Lamed, R. (2004) The cellulosomes: multienzyme machines for degradation of plant cell wall polysaccharides. Annu. Rev. Microbiol. 58, 521-554
71. Rakotoarivonina, H., Jubelin, G., Hebraud, M., Gaillard-Martinie, B., Forano, E., and Mosoni, P. (2002) Adhesion to cellulose of the Gram-positive bacterium Ruminococcus albus involves type IV pili. Microbiology 148, 1871-1880
72. Linder, M., Salovuori, I., Ruohonen, L., and Teeri, T. T. (1996) Characterization of a double cellulose-binding domain: synergistic high affinity binding to crystalline cellulose. J. Biol. Chem. 271, 21268-21272
73. Emsley, P., Charles, I. G., Fairweather, N. F., and Isaacs, N. W. (1996) Structure of Bordetella pertussis virulence factor P.69 pertactin. Nature 381, 90-92
74. Clantin, B., Hodak, H., Willery, E., Locht, C., Jacob-Dubuisson, F., and Villeret, V. (2004) The crystal structure of filamentous hemagglutinin secretion domain and its implications for the two-partner secretion pathway. Proc. Natl. Acad. Sci. U.S.A. 101, 6194-6199
75. Yeo, H.-J., Yokoyama, T., Walkiewicz, K., Kim, Y., Grass, S., and Geme, J. W., 3rd (2007) The structure of the Haemophilus influenzae HMW1 pro-piece reveals a structural domain essential for bacterial two-partner secretion. J. Biol. Chem. 282, 31076-31084