Physical interaction and assembly of Bacillus subtilis spore coat proteins CotE and CotZ studied by atomic force microscopy

Journal of Structural Biology

Volumn 195, Issue 2, 2016, Pages 245-251

  Liu, Huiqing ^a,b   Qiao, Haiyan ^c   Krajcikova, Daniela ^d   Zhang, Zhe ^a   Wang, Hongda ^a   Barak, Imrich ^d   Tang, Jilin ^a  

^a CHANGCHUN INSTITUTE OF APPLIED CHEMISTRY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c LIAONING SHIHUA UNIVERSITY   (China)

^d INSTITUTE OF CHEMISTRY   (Slovakia)

Author keywords

Atomic force microscopy; CotE; CotZ; Protein protein interaction; Self assembly; Single molecule force spectroscopy

Indexed keywords

COAT PROTEIN; PROTEIN COTE; PROTEIN COTZ; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; COTE PROTEIN, BACILLUS SUBTILIS;

ARTICLE; ATOMIC FORCE MICROSCOPY; BACILLUS SUBTILIS; BACTERIAL SPORE; CONTROLLED STUDY; FORCE; IN VITRO STUDY; KINETICS; MOLECULAR DYNAMICS; NONHUMAN; PHYSICAL PARAMETERS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SINGLE MOLECULE FORCE SPECTROSCOPY; SOLID LIQUID INTERFACE; SPECTROSCOPY; CELL WALL; CHEMISTRY; MORPHOGENESIS; ULTRASTRUCTURE;

BACILLUS SUBTILIS; BACTERIAL PROTEINS; CELL WALL; KINETICS; MICROSCOPY, ATOMIC FORCE; MORPHOGENESIS; SPORES, BACTERIAL;

EID: 84992135181     PISSN: 10478477     EISSN: 10958657     Source Type: Journal    
DOI: 10.1016/j.jsb.2016.06.010     Document Type: Article

References (54)

1. Bauer, T., Little, S., Stover, A.G., Driks, A., Functional regions of the Bacillus subtilis spore coat morphogenetic protein CotE. J. Bacteriol. 181 (1999), 7043–7051.
2. Baumgartner, W., Hinterdorfer, P., Schindler, H., Data analysis of interaction forces measured with the atomic force microscope. Ultramicroscopy 82 (2000), 85–95.
3. Baumgartner, W., Hinterdorfer, P., Ness, W., Raab, A., Vestweber, D., Schindler, H., Drenckhahn, D., Cadherin interaction probed by atomic force microscopy. Proc. Natl. Acad. Sci. U. S. A. 97 (2000), 4005–4010.
4. Bell, G.I., Models for specific adhesion of cells to cells. Science 200 (1978), 618–627.
5. Butt, H.J., Jaschke, M., Calculation of thermal noise in atomic-force microscopy. Nanotechnology 6 (1995), 1–7.
6. Cecchet, F., Lussis, P., Jerome, C., Gabriel, S., Silva-Goncalves, E., Jerome, R., Duwez, A.-S., A generic chemical platform for molecular recognition and stimuli-responsive probes based on scanning probe microscopy. Small 4 (2008), 1101–1104.
7. Chtcheglova, L.A., Wildling, L., Waschke, J., Drenckhahn, D., Hinterdorfer, P., AFM functional imaging on vascular endothelial cells. J. Mol. Recognit. 23 (2010), 589–596.
8. Costa, T., Isidro, A.L., Moran, C.P. Jr., Henriques, A.O., Interaction between coat morphogenetic proteins SafA and SpoVID. J. Bacteriol. 188 (2006), 7731–7741.
9. de Francesco, M., Jacobs, J.Z., Nunes, F., Serrano, M., McKenney, P.T., Chua, M.-H., Henriques, A.O., Eichenberger, P., Physical interaction between coat morphogenetic proteins SpoVID and CotE is necessary for spore encasement in Bacillus subtilis. J. Bacteriol. 194 (2012), 4941–4950.
10. De Paris, R., Strunz, T., Oroszlan, K., Güntherodt, H.-J., Hegner, M., Force spectroscopy and dynamics of the biotin-avidin bond studied by scanning force microscopy. Single Mol. 1 (2000), 285–290.
11. Donovan, W., Zheng, L., Sandman, K., Losick, R., Gene encoding spore coat polypeptides from Bacillus subtilis. J. Mol. Biol. 196 (1987), 1–10.
12. Driks, A., Bacillus subtilis spore coat. Microbiol. Mol. Biol. Rev. 63 (1999), 1–20.
13. Driks, A., Roels, S., Beall, B., Moran, C.P., Losick, R., Subcellular-localization of proteins involved in the assembly of the spore coat of Bacillus subtilis. Genes Dev. 8 (1994), 234–244.
14. Dufrene, Y.F., Hinterdorfer, P., Recent progress in AFM molecular recognition studies. Pflugers Arch. Eur. J. Phys. 456 (2008), 237–245.
15. Ebner, A., Wildling, L., Kamruzzahan, A.S.M., Rankl, C., Wruss, J., Hahn, C.D., Hoelzl, M., Zhu, R., Kienberger, F., Blaas, D., Hinterdorfer, P., Gruber, H.J., A new, simple method for linking of antibodies to atomic force microscopy tips. Bioconjugate Chem. 18 (2007), 1176–1184.
16. Fotiadis, D., Scheuring, S., Muller, S.A., Engel, A., Muller, D.J., Imaging and manipulation of biological structures with the AFM. Micron 33 (2002), 385–397.
17. Henriques, A.O., Moran, C.P., Structure and assembly of the bacterial endospore coat. Methods 20 (2000), 95–110.
18. Henriques, A.O., Moran, C.P. Jr., Structure, assembly, and function of the spore surface layers. Annu. Rev. Microbiol. 61 (2007), 555–588.
19. Hinterdorfer, P., Dufrene, Y.F., Detection and localization of single molecular recognition events using atomic force microscopy. Nat. Methods 3 (2006), 347–355.
20. Hutter, J.L., Bechhoefer, J., Calibration of atomic-force microscope tips. Rev. Sci. Instrum. 64 (1993), 1868–1873.
21. Imamura, D., Kuwana, R., Takamatsu, H., Watabe, K., Proteins involved in formation of the outermost layer of Bacillus subtilis spores. J. Bacteriol. 193 (2011), 4075–4080.
22. Isticato, R., Pelosi, A., De Felice, M., Ricca, E., CotE binds to CotC and CotU and mediates their interaction during spore coat formation in Bacillus subtilis. J. Bacteriol. 192 (2010), 949–954.
23. Jiang, S., Wan, Q., Krajcikova, D., Tang, J., Tzokov, S.B., Barak, I., Bullough, P.A., Diverse supramolecular structures formed by self-assembling proteins of the Bacillus subtilis spore coat. Mol. Microbiol. 97 (2015), 347–359.
24. Kim, H., Hahn, M., Grabowski, P., McPherson, D.C., Otte, M.M., Wang, R., Ferguson, C.C., Eichenberger, P., Driks, A., The Bacillus subtilis spore coat protein interaction network. Mol. Microbiol. 59 (2006), 487–502.
25. Krajcikova, D., Lukacova, M., Mullerova, D., Cutting, S.M., Barak, I., Searching for protein-protein interactions within the Bacillus subtilis spore coat. J. Bacteriol. 191 (2009), 3212–3219.
26. Little, S., Driks, A., Functional analysis of the morphogenetic spore coat Bacillus subtilis protein CotE. Mol. Microbiol. 42 (2001), 1107–1120.
27. Liu, H., Krajcikova, D., Zhang, Z., Wang, H., Barak, I., Tang, J., Investigating interactions of the Bacillus subtilis spore coat proteins CotY and CotZ using single molecule force spectroscopy. J. Struct. Biol. 192 (2015), 14–20.
28. Liu, H., Krajcikova, D., Wang, N., Zhang, Z., Wang, H., Barak, I., Tang, J., Forces and kinetics of the Bacillus subtilis spore coat proteins CotY and CotX binding to CotE inspected by single molecule force spectroscopy. J. Phys. Chem. B 120 (2016), 1041–1047.
29. McKenney, P.T., Eichenberger, P., Dynamics of spore coat morphogenesis in Bacillus subtilis. Mol. Microbiol. 83 (2012), 245–260.
30. McKenney, P.T., Driks, A., Eichenberger, P., The Bacillus subtilis endospore: assembly and functions of the multilayered coat. Nat. Rev. Microbiol. 11 (2013), 33–44.
31. McKenney, P.T., Driks, A., Eskandarian, H.A., Grabowski, P., Guberman, J., Wang, K.H., Gitai, Z., Eichenberger, P., A distance-weighted interaction map reveals a previously uncharacterized layer of the Bacillus subtilis spore coat. Curr. Biol. 20 (2010), 934–938.
32. Merkel, R., Nassoy, P., Leung, A., Ritchie, K., Evans, E., Energy landscapes of receptor-ligand bonds explored with dynamic force spectroscopy. Nature 397 (1999), 50–53.
33. Muellerova, D., Krajcikova, D., Barak, I., Interactions between Bacillus subtilis early spore coat morphogenetic proteins. FEMS Microbiol. Lett. 299 (2009), 74–85.
34. Nicholson, W.L., Munakata, N., Horneck, G., Melosh, H.J., Setlow, P., Resistance of Bacillus endospores to extreme terrestrial and extraterrestrial environments. Microbiol. Mol. Biol. Rev. 64 (2000), 548–572.
35. Ozin, A.J., Henriques, A.O., Yi, H., Moran, C.P., Morphogenetic proteins SpoVID and SafA form a complex during assembly of the Bacillus subtilis spore coat. J. Bacteriol. 182 (2000), 1828–1833.
36. Ozin, A.J., Samford, C.S., Henriques, A.O., Moran, C.P., SpoVID guides SafA to the spore coat in Bacillus subtilis. J. Bacteriol. 183 (2001), 3041–3049.
37. Piggot, P.J., Coote, J.G., Genetic aspects of bacterial endospore formation. Bacteriol. Rev. 40 (1976), 908–962.
38. Plomp, M., Carroll, A.M., Setlow, P., Malkin, A.J., Architecture and assembly of the Bacillus subtilis spore coat. PLoS One, 9, 2014, e108560.
39. Plomp, M., Rice, M.K., Wagner, E.K., McPherson, A., Malkin, A.J., Rapid visualization at high resolution of pathogens by atomic force microscopy: structural studies of herpes simplex virus-1. Am. J. Pathol. 160 (2002), 1959–1966.
40. Pogliano, K., Harry, E., Losick, R., Visualization of the subcellular location of sporulation proteins in Bacillus subtilis using immunofluorescence microscopy. Mol. Microbiol. 18 (1995), 459–470.
41. Qiao, H., Krajcikova, D., Liu, C., Li, Y., Wang, H., Barak, I., Tang, J., The interactions of spore-coat morphogenetic proteins studied by single-molecule recognition force spectroscopy. Chem. Asian J. 7 (2012), 725–731.
42. Qiao, H., Krajcikova, D., Xing, C., Lu, B., Hao, J., Ke, X., Wang, H., Barak, I., Tang, J., Study of the interactions between the key spore coat morphogenetic proteins CotE and SpoVID. J. Struct. Biol. 181 (2013), 128–135.
43. Ramamurthi, K.S., Clapham, K.R., Losick, R., Peptide anchoring spore coat assembly to the outer forespore membrane in Bacillus subtilis. Mol. Microbiol. 62 (2006), 1547–1557.
44. Riener, C.K., Stroh, C.M., Ebner, A., Klampfl, C., Gall, A.A., Romanin, C., Lyubchenko, Y.L., Hinterdorfer, P., Gruber, H.J., Simple test system for single molecule recognition force microscopy. Anal. Chim. Acta 479 (2003), 59–75.
45. Shao, Z.F., Mou, J., Czajkowsky, D.M., Yang, J., Yuan, J.Y., Biological atomic force microscopy: what is achieved and what is needed. Adv. Phys. 45 (1996), 1–86.
46. Tang, J., Ebner, A., Kraxberger, B., Leitner, M., Hykollari, A., Kepplinger, C., Grunwald, C., Gruber, H.J., Tampe, R., Sleytr, U.B., Ilk, N., Hinterdorfer, P., Detection of metal binding sites on functional S-layer nanoarrays using single molecule force spectroscopy. J. Struct. Biol. 168 (2009), 217–222.
47. Wang, K.H., Isidro, A.L., Domingues, L., Eskandarian, H.A., McKenney, P.T., Drew, K., Grabowski, P., Chua, M.-H., Barry, S.N., Guan, M., Bonneau, R., Henriques, A.O., Eichenberger, P., The coat morphogenetic protein SpoVID is necessary for spore encasement in Bacillus subtilis. Mol. Microbiol. 74 (2009), 634–649.
48. Wildling, L., Rankl, C., Haselgruebler, T., Gruber, H.J., Holy, M., Newman, A.H., Zou, M.-F., Zhu, R., Freissmuth, M., Sitte, H.H., Hinterdorfer, P., Probing binding pocket of serotonin transporter by single molecular force spectroscopy on living cells. J. Biol. Chem. 287 (2012), 105–113.
49. Wollschlaeger, K., Gaus, K., Koernig, A., Eckel, R., Wilking, S.-D., McIntosh, M., Majer, Z., Becker, A., Ros, R., Anselmetti, D., Sewald, N., Single-molecule experiments to elucidate the minimal requirement for DNA recognition by transcription factor epitopes. Small 5 (2009), 484–495.
50. Zhang, J., Fitzjames, P.C., Aronson, A.I., Cloning and charcterization of a cluster of genes encoding polypeptides present in the insoluble fraction of the spore coat of Bacillus subtilis. J. Bacteriol. 175 (1993), 3757–3766.
51. Zhang, J., Chtcheglova, L.A., Zhu, R., Hinterdorfer, P., Zhang, B., Tang, J., Nanoscale organization of human GnRH-R on human bladder cancer cells. Anal. Chem. 86 (2014), 2458–2464.
52. Zheng, L.B., Donovan, W.P., Fitzjames, P.C., Losick, R., Gene encoding a morphogenic protein required in the assembly of the outer coat of the Bacillus subtilis endospore. Genes Dev. 2 (1988), 1047–1054.
53. Zhu, R., Howorka, S., Proell, J., Kienberger, F., Preiner, J., Hesse, J., Ebner, A., Pastushenko, V.P., Gruber, H.J., Hinterdorfer, P., Nanomechanical recognition measurements of individual DNA molecules reveal epigenetic methylation patterns. Nat. Nanotechnol. 5 (2010), 788–791.
54. Zilhao, R., Serrano, M., Isticato, R., Ricca, E., Moran, C.P., Henriques, A.O., Interactions among CotB, CotG, and CotH during assembly of the Bacillus subtilis spore coat. J. Bacteriol. 186 (2004), 1110–1119.