An octamer of enolase from <italic>Streptococcus suis

doi:10.1007/s13238-012-2040-7

Prot Cell

2012, Vol. 3

Issue (10) : 769-780 https://doi.org/10.1007/s13238-012-2040-7 PMID: 23055041

RESEARCH ARTICLE

An octamer of enolase from Streptococcus suis

Qiong Lu^1,2, Hao Lu¹, Jianxun Qi¹, Guangwen Lu¹(

), George F Gao^1,2,3,4(

)

1. CAS Key Laboratory of Pathogenic Microbiology and Immunology, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China; 2. Graduate University, Chinese Academy of Sciences, Beijing 100049, China; 3. Research Network of Immunity and Health (RNIH), Beijing Institutes of Life Science, Chinese Academy of Sciences, Beijing 100101, China; 4. Laboratory of Protein Engineering and Vaccines, Tianjin Institute of Industrial Biotechnology, Chinese Academy of Sciences, Tianjin 300308, China

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Abstract

Enolase is a conserved cytoplasmic metalloenzyme existing universally in both eukaryotic and prokaryotic cells. The enzyme can also locate on the cell surface and bind to plasminogen, via which contributing to the mucosal surface localization of the bacterial pathogens and assisting the invasion into the host cells. The functions of the eukaryotic enzymes on the cell surface expression (including T cells, B cells, neutrophils, monocytoes, neuronal cells and epithelial cells) are not known. Streptococcus suis serotype 2 (S. suis 2, SS2) is an important zoonotic pathogen which has recently caused two large-scale outbreaks in southern China with severe streptococcal toxic shock syndrome (STSS) never seen before in human sufferers. We recently identified the SS2 enolase as an important protective antigen which could protect mice from fatal S.suis 2 infection. In this study, a 2.4-angstrom structure of the SS2 enolase is solved, revealing an octameric arrangement in the crystal. We further demonstrated that the enzyme exists exclusively as an octamer in solution via a sedimentation assay. These results indicate that the octamer is the biological unit of SS2 enolase at least in vitro and most likely in vivo as well. This is, to our knowledge, the first comprehensive characterization of the SS2 enolase octamer both structurally and biophysically, and the second octamer enolase structure in addition to that of Streptococcus pneumoniae. We also investigated the plasminogen binding property of the SS2 enzyme.

Keywords enolase octamer Streptococcus suis structure plasminogen binding

Corresponding Author(s): Lu Guangwen,Email:luguangwen2001@126.com; Gao George F,Email:gaof@im.ac.cn

Issue Date: 01 October 2012

Cite this article:

Qiong Lu,Hao Lu,Jianxun Qi, et al. An octamer of enolase from Streptococcus suis[J]. Prot Cell, 2012, 3(10): 769-780.

URL:

https://academic.hep.com.cn/pac/EN/10.1007/s13238-012-2040-7
https://academic.hep.com.cn/pac/EN/Y2012/V3/I10/769

1	Adams, P.D., Afonine, P.V., Bunkoczi, G., Chen, V.B., Davis, I.W., Echols, N., Headd, J.J., Hung, L.W., Kapral, G.J., Grosse-Kunstleve, R.W., . (2010). PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66, 213-221 . doi: 10.1107/S0907444909052925
2	Agarwal, S., Kulshreshtha, P., Mukku, D.B., and Bhatnagar, R. (2008). alpha-Enolase binds to human plasminogen on the surface of Bacillus anthracis. Bba-Proteins Proteom 1784, 986-994 . doi: 10.1016/j.bbapap.2008.03.017
3	Andronicos, N.M., Ranson, M., Bognacki, J., and Baker, M.S. (1997). The human ENO1 gene product (recombinant human alpha-enolase) displays characteristics required for a plasminogen binding protein. Bba-Protein Struct M 1337, 27-39 . doi: 10.1016/S0167-4838(96)00146-X
4	Babbitt, P.C., Hasson, M.S., Wedekind, J.E., Palmer, D.R., Barrett, W.C., Reed, G.H., Rayment, I., Ringe, D., Kenyon, G.L., and Gerlt, J.A. (1996). The enolase superfamily: a general strategy for enzyme-catalyzed abstraction of the alpha-protons of carboxylic acids. Biochemistry-US 35, 16489-16501 . doi: 10.1021/bi9616413
5	Banner, D.W., Bloomer, A.C., Petsko, G.A., Phillips, D.C., Pogson, C.I., Wilson, I.A., Corran, P.H., Furth, A.J., Milman, J.D., Offord, R.E., . (1975). Structure of chicken muscle triose phosphate isomerase determined crystallographically at 2.5 angstrom resolution using amino acid sequence data. Nature 255, 609-614 . doi: 10.1038/255609a0
6	Baums, C.G., Kaim, U., Fulde, M., Ramachandran, G., Goethe, R., and Valentin-Weigand, P. (2006). Identification of a novel virulence determinant with serum opacification activity in Streptococcus suis. Infect Immun 74, 6154-6162 . doi: 10.1128/IAI.00359-06
7	Bergmann, S., Rohde, M., Chhatwal, G.S., and Hammerschmidt, S. (2001). alpha-Enolase of Streptococcus pneumoniae is a plasmin(ogen)-binding protein displayed on the bacterial cell surface. Mol Microbiol 40, 1273-1287 . doi: 10.1046/j.1365-2958.2001.02448.x
8	Bergmann, S., Wild, D., Diekmann, O., Frank, R., Bracht, D., Chhatwal, G.S., and Hammerschmidt, S. (2003). Identification of a novel plasmin(ogen)-binding motif in surface displayed alpha-enolase of Streptococcus pneumoniae. Mol Microbiol 49, 411-423 . doi: 10.1046/j.1365-2958.2003.03557.x
9	Brown, C.K., Kuhlman, P.L., Mattingly, S., Slates, K., Calie, P.J., and Farrar, W.W. (1998). A model of the quaternary structure of enolases, based on structural and evolutionary analysis of the octameric enolase from Bacillus subtilis. J Protein Chem 17, 855-866 . doi: 10.1023/A:1020790604887
10	Candela, M., Biagi, E., Centanni, M., Turroni, S., Vici, M., Musiani, F., Vitali, B., Bergmann, S., Hammerschmidt, S., and Brigidi, P. (2009). Bifidobacterial enolase, a cell surface receptor for human plasminogen involved in the interaction with the host. Microbiol-Sgm 155, 3294-3303 . doi: 10.1099/mic.0.028795-0
11	Chandran, V., and Luisi, B.F. (2006). Recognition of enolase in the Escherichia coli RNA degradosome. J Mol Biol 358, 8-15 . doi: 10.1016/j.jmb.2006.02.012
12	Chen, C., Tang, J., Dong, W., Wang, C., Feng, Y., Wang, J., Zheng, F., Pan, X., Liu, D., Li, M., . (2007). A glimpse of streptococcal toxic shock syndrome from comparative genomics of S. suis 2 Chinese isolates. Plos One 2, e315. doi: 10.1371/journal.pone.0000315
13	collaborative. (1994). The CCP4 suite:programs for protein crystallography. Acta Crystallogr D Biol crystallography 50, 760-763 . doi: 10.1107/S0907444994003112
14	Cork, A.J., Jergic, S., Hammerschmidt, S., Kobe, B., Pancholi, V., Benesch, J.L., Robinson, C.V., Dixon, N.E., Aquilina, J.A., and Walker, M.J. (2009). Defining the structural basis of human plasminogen binding by streptococcal surface enolase. J Biol Chem 284, 17129-17137 . doi: 10.1074/jbc.M109.004317
15	Derbise, A., Song, Y.P., Parikh, S., Fischetti, V.A., and Pancholi, V. (2004). Role of the C-terminal lysine residues of streptococcal surface enolase in Glu- and Lys-plasminogen-binding activities of group A streptococci. Infect Immun 72, 94-105 . doi: 10.1128/IAI.72.1.94-105.2004
16	Ehinger, S., Schubert, W.D., Bergmann, S., Hammerschmidt, S., and Heinz, D.W. (2004). Plasmin(ogen)-binding alpha-enolase from Streptococcus pneumoniae: Crystal structure and evaluation of plasmin(ogen)-binding sites. J Mol Biol 343, 997-1005 . doi: 10.1016/j.jmb.2004.08.088
17	Emsley, P., and Cowtan, K. (2004). Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60, 2126-2132 . doi: 10.1107/S0907444904019158
18	Esgleas, M., Li, Y., Hancock, M.A., Harel, J., Dubreuil, J.D., and Gottschalk, M. (2008). Isolation and characterization of alpha-enolase, a novel fibronectin-binding protein from Streptococcus suis. Microbiology 154, 2668-2679 . doi: 10.1099/mic.0.2008/017145-0
19	Feng, Y., Pan, X., Sun, W., Wang, C., Zhang, H., Li, X., Ma, Y., Shao, Z., Ge, J., Zheng, F., . (2009). Streptococcus suis enolase functions as a protective antigen displayed on the bacterial cell surface. J Infect Dis 200, 1583-1592 . doi: 10.1086/644602
20	Feng, Y., Zhang, H., Ma, Y., and Gao, G.F. (2010). Uncovering newly emerging variants of Streptococcus suis, an important zoonotic agent. Trends Microbiol 18, 124-131 . doi: 10.1016/j.tim.2009.12.003
21	Gerlt, J.A., Babbitt, P.C., Jacobson, M.P., and Almo, S.C. (2012). Divergent evolution in enolase superfamily: strategies for assigning functions. J Biol Chem 287, 29-34 . doi: 10.1074/jbc.R111.240945
22	Gerlt, J.A., Babbitt, P.C., and Rayment, I. (2005). Divergent evolution in the enolase superfamily: the interplay of mechanism and specificity. Arch Biochem Biophys 433, 59-70 . doi: 10.1016/j.abb.2004.07.034
23	Guo, Y., Wang, J., Niu, G., Shui, W., Sun, Y., Zhou, H., Zhang, Y., Yang, C., Lou, Z., and Rao, Z. (2011). A structural view of the antibiotic degradation enzyme NDM-1 from a superbug. Protein Cell 2, 384-394 . doi: 10.1007/s13238-011-1055-9
24	Han, H., Liu, C., Wang, Q., Xuan, C., Zheng, B., Tang, J., Yan, J., Zhang, J., Li, M., Cheng, H., . (2012). The two-component system Ihk/Irr contributes to the virulence of Streptococcus suis serotype 2 strain 05ZYH33 through alteration of the bacterial cell metabolism. Microbiology . (In Press) doi: 10.1099/mic.0.057448-0
25	Holm, L., and Sander, C. (1996). Mapping the protein universe. Science 273, 595-602 . doi: 10.1126/science.273.5275.595
26	Hosaka, T., Meguro, T., Yamato, I., and Shirakihara, Y. (2003). Crystal structure of Enterococcus hirae enolase at 2.8 A resolution. J Biochem 133, 817-823 . doi: 10.1093/jb/mvg104
27	Jones, M.N., and Holt, R.G. (2007). Cloning and characterization of an alpha-enolase of the oral pathogen Streptococcus mutans that binds human plasminogen. Biochem Bioph Res Co 364, 924-929 . doi: 10.1016/j.bbrc.2007.10.098
28	Kang, H.J., Jung, S.K., Kim, S.J., and Chung, S.J. (2008). Structure of human alpha-enolase (hENO1), a multifunctional glycolytic enzyme. Acta Crystallogr D Biol Crystallogr 64, 651-657 . doi: 10.1107/S0907444908008561
29	Karbassi, F., Quiros, V., Pancholi, V., and Kornblatt, M.J. (2010). Dissociation of the octameric enolase from S. pyogenes--one interface stabilizes another. Plos One 5, e8810. doi: 10.1371/journal.pone.0008810
30	Kuhnel, K., and Luisi, B.F. (2001). Crystal structure of the Escherichia coli RNA degradosome component enolase. J Mol Biol 313, 583-592 . doi: 10.1006/jmbi.2001.5065
31	Laskowski, R.A., MacArthur, M. W., Moss, D. S., & Thorton, J. M (1993). PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Crystallogr 26, 283-291 . doi: 10.1107/S0021889892009944
32	Li, M., Shen, X., Yan, J., Han, H., Zheng, B., Liu, D., Cheng, H., Zhao, Y., Rao, X., Wang, C., . (2011). GI-type T4SS-mediated horizontal transfer of the 89K pathogenicity island in epidemic Streptococcus suis serotype 2. Mol Microbiol 79, 1670-1683 . doi: 10.1111/j.1365-2958.2011.07553.x
33	Li, M., Wang, C., Feng, Y., Pan, X., Cheng, G., Wang, J., Ge, J., Zheng, F., Cao, M., Dong, Y., . (2008). SalK/SalR, a two-component signal transduction system, is essential for full virulence of highly invasive Streptococcus suis serotype 2. Plos One 3, e2080. doi: 10.1371/journal.pone.0002080
34	Lu, G., Qi, J., Gao, F., Yan, J., Tang, J., and Gao, G.F. (2011a). A novel "open-form" structure of sortaseC from Streptococcus suis2764-2769 . doi: 10.1002/prot.23093
35	Lu, G., Zhang, J., Li, Y., Li, Z., Zhang, N., Xu, X., Wang, T., Guan, Z., Gao, G.F., and Yan, J. (2011b). hNUDT16: a universal decapping enzyme for small nucleolar RNA and cytoplasmic mRNA. Protein Cell 2, 64-73 . doi: 10.1007/s13238-011-1009-2
36	Ma, Y., Feng, Y., Liu, D., and Gao, G.F. (2009). Avian influenza virus, Streptococcus suis serotype 2, severe acute respiratory syndrome-coronavirus and beyond: molecular epidemiology, ecology and the situation in China2725-2737 . doi: 10.1098/rstb.2009.0093
37	Murshudov, G.N., Vagin, A.A., and Dodson, E.J. (1997). Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53, 240-255 . doi: 10.1107/S0907444996012255
38	Nurmohamed, S., McKay, A.R., Robinson, C.V., and Luisi, B.F. (2010). Molecular recognition between Escherichia coli enolase and ribonuclease E. Acta Crystallogr D Biol Crystallogr 66, 1036-1040 . doi: 10.1107/S0907444910030015
39	Otwinowski, Z., Minor, W., and Charles W. Carter, Jr. (1997). Processing of X-ray diffraction data collected in oscillation mode. Methods in enzymology (Academic Press) , pp. 307-326 . doi: 10.1016/S0076-6879(97)76066-X
40	Pancholi, V. (2001).Multifunctional alpha-enolase: its role in diseases . Cell Mol Life Sci 58, 902-920 . doi: 10.1007/PL00000910
41	Schurig, H., Rutkat, K., Rachel, R., and Jaenicke, R. (1995). Octameric enolase from the hyperthermophilic bacterium Thermotoga maritima: purification, characterization, and image processing. Protein Sci 4, 228-236 . doi: 10.1002/pro.5560040209
42	Seweryn, E., Pietkiewicz, J., Szamborska, A., and Gamian, A. (2007). [Enolase on the surface of prockaryotic and eukaryotic cells is a receptor for human plasminogen]. Postepy Hig Med Dosw (Online) 61, 672-682 .
43	Smith, H.E., Damman, M., van der Velde, J., Wagenaar, F., Wisselink, H.J., Stockhofe-Zurwieden, N., and Smits, M.A. (1999). Identification and characterization of the cps locus of Streptococcus suis serotype 2: the capsule protects against phagocytosis and is an important virulence factor. Infect Immun 67, 1750-1756 .
44	Stec, B., and Lebioda, L. (1990). Refined structure of yeast apo-enolase at 2.25 A resolution. J Mol Biol 211, 235-248 . doi: 10.1016/0022-2836(90)90023-F
45	Tang, J., Wang, C., Feng, Y., Yang, W., Song, H., Chen, Z., Yu, H., Pan, X., Zhou, X., Wang, H., . (2006). Streptococcal toxic shock syndrome caused by Streptococcus suis serotype 2. PLoS Med 3, e151. doi: 10.1371/journal.pmed.0030151
46	Vagin, A., and Teplyakov, A. (1997). MOLREP: an automated program for molecular replacement. J Appl Crystallogr 30, 1022-1025 . doi: 10.1107/S0021889897006766
47	Vanier, G., Sekizaki, T., Dominguez-Punaro, M.C., Esgleas, M., Osaki, M., Takamatsu, D., Segura, M., and Gottschalk, M. (2008). Disruption of srtA gene in Streptococcus suis results in decreased interactions with endothelial cells and extracellular matrix proteins. Vet Microbiol 127, 417-424 . doi: 10.1016/j.vetmic.2007.08.032
48	Wang, C., Li, M., Feng, Y., Zheng, F., Dong, Y., Pan, X., Cheng, G., Dong, R., Hu, D., Feng, X., . (2009). The involvement of sortase A in high virulence of STSS-causing Streptococcus suis serotype 223-33 . doi: 10.1007/s00203-008-0425-z
49	Wierenga, R.K. (2001). The TIM-barrel fold: a versatile framework for efficient enzymes. Febs Lett 492, 193-198 . doi: 10.1016/S0014-5793(01)02236-0
50	Xu, L., Huang, B., Du, H., Zhang, X.C., Xu, J., Li, X., and Rao, Z. (2010). Crystal structure of cytotoxin protein suilysin from Streptococcus suis. Protein Cell 1, 96-105 . doi: 10.1007/s13238-010-0012-3
51	Zhang, A., Chen, B., Mu, X., Li, R., Zheng, P., Zhao, Y., Chen, H., and Jin, M. (2009). Identification and characterization of a novel protective antigen, Enolase of Streptococcus suis serotype 2. Vaccine 27, 1348-1353 . doi: 10.1016/j.vaccine.2008.12.047
52	Zheng, B., Tan, S., Gao, J., Han, H., Liu, J., Lu, G., Liu, D., Yi, Y., Zhu, B., and Gao, G.F. (2011). An unexpected similarity between antibiotic-resistant NDM-1 and beta-lactamase II from Erythrobacter litoralis. Protein Cell 2, 250-258 . doi: 10.1007/s13238-011-1027-0

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