Structural and functional analysis of botulinum neurotoxin subunits for pH-dependent membrane channel formation and translocation

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1854, Issue 10, 2015, Pages 1510-1516

  Chellappan, Gowri ^a   Kumar, Raj ^a,c   Santos, Erin ^a   Goyal, Dipak ^b   Cai, Shuowei ^a   Singh, Bal Ram ^a,c,d  

^a UNIVERSITY OF MASSACHUSETTS DARTMOUTH   (United States)

^b UNIVERSITY OF MASSACHUSETTS LOWELL   (United States)

^c Botulinum Research Center Institute of Advanced Sciences   (United States)

^d Prime Bio Inc   (United States)

Author keywords

BoNT; Circular dichroism; Clostridium botulinum; Heavy chain; Light chain; Molar ellipticity; pH; Thermal denaturation

Indexed keywords

BOTULINUM TOXIN A; LIPOSOME; PROTEINASE; SNARE PROTEIN; BOTULINUM TOXIN; ION CHANNEL; POTASSIUM; PROTEIN BINDING; PROTEIN SUBUNIT;

ARTICLE; CATALYSIS; CHANNEL GATING; CONTROLLED STUDY; CYTOSOL; ENZYME ACTIVITY; HEAVY CHAIN; LIGHT CHAIN; MEMBRANE CHANNEL; NERVE CELL; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN FUNCTION; PROTEIN SECONDARY STRUCTURE; THERMOSTABILITY; CHEMISTRY; CLOSTRIDIUM BOTULINUM; ION TRANSPORT; ISOLATION AND PURIFICATION; METABOLISM; PROTEIN DEGRADATION; PROTEIN FOLDING; PROTEIN STABILITY; PROTEIN SUBUNIT; PROTEIN TERTIARY STRUCTURE; PROTEIN TRANSPORT;

BOTULINUM TOXINS; CLOSTRIDIUM BOTULINUM; HYDROGEN-ION CONCENTRATION; ION CHANNELS; ION TRANSPORT; LIPOSOMES; POTASSIUM; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN STABILITY; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS; PROTEIN TRANSPORT; PROTEOLYSIS; SNARE PROTEINS;

EID: 84965087729     PISSN: 15709639     EISSN: 18781454     Source Type: Journal    
DOI: 10.1016/j.bbapap.2015.05.013     Document Type: Article

References (29)

1. [1] Singh, B.R., Kumar, R., Cai, S., Molecular mechanism and effects of Clostridial neurotoxins. Kostrzewa, R.M., (eds.) Handbook of Neurotoxicity, 2014, Springer, New York, 513–551.
2. [2] Montecucco, C., Schiavo, G., Mechanism of action of tetanus and botulinum neurotoxins. Mol. Microbiol. 13 (1994), 1–8.
3. [3] Koriazova, L.K., Montal, M., Translocation of botulinum neurotoxin light chain protease through the heavy chain channel. Nat. Struct. Biol. 10 (2003), 13–18.
4. [4] Singh, B.R., Botulinum neurotoxin structure, engineering, and novel cellular trafficking and targeting. Neurotox. Res. 9 (2006), 73–92.
5. [5] Lacy, D.B., Tepp, W., Cohen, A.C., DasGupta, B.R., Stevens, R.C., Crystal structure of botulinum neurotoxin type A and implications for toxicity. Nat. Struct. Biol. 5 (1998), 898–902.
6. [6] Li, L., Singh, B.R., Spectroscopic analysis of pH-induced changes in the molecular features of type A botulinum neurotoxin light chain. Biochemistry 39 (2000), 6466–6474.
7. [7] Puhar, A., Johnson, E.A., Rossetto, O., Montecucco, C., Comparison of the pH-induced conformational change of different clostridial neurotoxins. Biochem. Biophys. Res. Commun. 319 (2004), 66–71.
8. [8] Brunger, A.T., Breidenbach, M.A., Jin, R., Fischer, A., Santos, J.S., Montal, M., Botulinum neurotoxin heavy chain belt as an intramolecular chaperone for the light chain. PLoS Pathog. 3 (2007), 1191–1194.
9. [9] Blaustein, R.O., Germann, W.J., Finkelstein, A., DasGupta, B.R., The N-terminal half of the heavy chain of botulinum type A neurotoxin forms channels in planar phospholipid bilayers. FEBS Lett. 226 (1987), 115–120.
10. [10] Mushrush, D.J., Koteiche, H.A., Sammons, M.A., Link, A.J., McHaourab, H.S., Lacy, D.B., Studies of the mechanistic details of the pH-dependent association of botulinum neurotoxin with membranes. J. Biol. Chem. 286 (2011), 27011–27018.
11. [11] Cai, S., Kukreja, R., Shoesmith, S., Chang, T.W., Singh, B.R., Botulinum neurotoxin light chain refolds at endosomal pH for its translocation. Protein J. 25 (2006), 455–462.
12. [12] Fu, F.N., Busath, D.D., Singh, B.R., Spectroscopic analysis of low pH and lipid-induced structural changes in type A botulinum neurotoxin relevant to membrane channel formation and translocation. Biophys. Chem. 99 (2002), 17–29.
13. [13] DasGupta, B.R., Sathyamoorthy, V., Purification and amino acid composition of type A botulinum neurotoxin. Toxicon Off. J. Int. Soc. Toxinology 22 (1984), 415–424.
14. [14] Sathyamoorthy, V., DasGupta, B.R., Separation, purification, partial characterization and comparison of the heavy and light chains of botulinum neurotoxin types A, B, and E. J. Biol. Chem. 260 (1985), 10461–10466.
15. [15] Yang, J.T., Wu, C.S., Martinez, H.M., Calculation of protein conformation from circular dichroism. Methods Enzymol. 130 (1986), 208–269.
16. [16] Mayer, L.D., Hope, M.J., Cullis, P.R., Vesicles of variable sizes produced by a rapid extrusion procedure. Biochim. Biophys. Acta 858 (1986), 161–168.
17. [17] Thanongsaksrikul, J., Srimanote, P., Maneewatch, S., Choowongkomon, K., Tapchaisri, P., Makino, S., Kurazono, H., Chaicumpa, W., A V H H that neutralizes the zinc metalloproteinase activity of botulinum neurotoxin type A. J. Biol. Chem. 285 (2010), 9657–9666.
18. [18] Mayer, L.D., Bally, M.B., Hope, M.J., Cullis, P.R., Techniques for encapsulating bioactive agents into liposomes. Chem. Phys. Lipids 40 (1986), 333–345.
19. [19] Montecucco, C., Schiavo, G., Dasgupta, B.R., Effect of pH on the interaction of botulinum neurotoxins A, B and E with liposomes. Biochem. J. 259 (1989), 47–53.
20. [20] Fisher, A., Montal, M., Characterization of Clostridial botulinum neurotoxin channels in neuroblastoma cells. Neurotox. Res. 9 (2006), 93–100.
21. [21] Muraro, L., Tosatto, S., Motterlini, L., Rossetto, O., Montecucco, C., The N-terminal half of the receptor domain of botulinum neurotoxin A binds to microdomains of the plasma membrane. Biochem. Biophys. Res. Commun. 380 (2009), 76–80.
22. [22] Sun, S., Suresh, S., Liu, H., Tepp, W.H., Johnson, E.A., Edwardson, J.M., Chapman, E.R., Receptor binding enables botulinum neurotoxin B to sense low pH for translocation channel assembly. Cell Host Microbe 10 (2011), 237–247.
23. [23] Mao, D., Wallace, B.A., Differential light scattering and absorption flattening optical effects are minimal in the circular dichroism spectra of small unilamellar vesicles. Biochemistry 23 (1984), 2667–2673.
24. [24] Hoch, D.H., Romero-Mira, M., Ehrlich, B.E., Finkelstein, A., DasGupta, B.R., Simpson, L.L., Channels formed by botulinum, tetanus, and diphtheria toxins in planar lipid bilayers: relevance to translocation of proteins across membranes. Proc. Natl. Acad. Sci. U. S. A. 82 (1985), 1692–1696.
25. [25] Koehler, T.M., Collier, R.J., Anthrax toxin protective antigen: low-pH-induced hydrophobicity and channel formation in liposomes. Mol. Microbiol. 5 (1991), 1501–1506.
26. [26] Montal, M., Translocation of botulinum neurotoxin light chain protease by the heavy chain protein-conducting channel. Toxicon 54 (2009), 565–569.
27. [27] Fu, F.N., Singh, B.R., Calcein permeability of liposomes mediated by type A botulinum neurotoxin and its light and heavy chains. J. Protein Chem. 18 (1999), 701–707.
28. [28] Singh, B.R., Fuller, M.P., Schiavo, G., Molecular structure of tetanus neurotoxin as revealed by Fourier transform infrared and circular dichroic spectroscopy. Biophys. Chem. 36 (1990), 155–166.
29. [29] Kukreja, R., Singh, B., Biologically active novel conformational state of botulinum, the most poisonous poison. J. Biol. Chem. 280 (2005), 39346–39352.