Solution structure of the motile major sperm protein (MSP) of Ascaris suum - Evidence for two manganese binding sites and the possible role of bivalent cations in filament formation

Journal of Molecular Biology

Volumn 284, Issue 5, 1998, Pages 1611-1624

  Haaf, Andreas ^a   LeClaire III, Lawrence ^b   Roberts, Gregory ^b   Kent, Helen M ^a   Roberts, Thomas M ^b   Stewart, Murray ^a   Neuhaus, David ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^b FLORIDA STATE UNIVERSITY   (United States)

Author keywords

Amoeboid motility; Filaments; Major sperm protein; NMR structure; Polymerization

Indexed keywords

DIMER; DIVALENT CATION; MAGNESIUM ION; MANGANESE; PROTEIN;

ARTICLE; ASCARIS SUUM; BINDING SITE; CELL MOTILITY; CONTROLLED STUDY; CYTOSKELETON; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN BINDING; SPERM;

ASCARIS SUUM;

EID: 0032545168     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1998.2291     Document Type: Article

References (38)

1. Bork, P., Holm, L. & Sander, C. (1994). The immunoglobulin fold-structural classification, sequence patterns and a common core. J. Mol. Biol. 242, 309-320.
2. Brunger, A. T. (1992). X-PLOR version 3.1: A System for Crystallography and NMR, Yale University Press, New Haven.
3. Bullock, T. L., Parthasarathy, G., King, K. L., Kent, H. M., Roberts, T. M. & Stewart, M. (1996a). New crystal forms of the motile major sperm protein (MSP) of Ascaris suum. J. Struct. Biol. 116, 432-437.
4. Bullock, T. L., Roberts, T. M. & Stewart, M. (1996b). 2.5 A Resolution crystal structure of the motile major sperm protein (MSP) of Ascaris suum. J. Mol. Biol. 263, 284-296.
5. Bullock, T. M., McCoy, A. J., Kent, H. M., Roberts, T. M. & Stewart, M. (1998). Structural basis for amoeboid motility in nematode sperm. Nature Struct. Biol. 5, 184-189.
6. Diamond, R. (1992). On the multiple simultaneous superposition of molecular structures by rigid body transformation. Protein Sci. 1, 1279-1287.
7. Diamond, R. (1995). Coordinate-based cluster analysis. Acta Crystallog. 51, 127-135.
8. Fletcher, C. M., Harrison, R. A., Lachmann, P. J. & Neuhaus, D. (1994). Structure of a soluble, glycosylated form of the human complement regulatory protein CD59. Structure, 2, 185-199.
9. Fletcher, C. M., Jones, D. N. M., Diamond, R. & Neuhaus, D. (1996). Treatment of NOE constraints involving equivalent or nonstereoassigned protons in calculations of biomolecular structures. J. Biomol. NMR, 8, 292-310.
10. Folkers, P. J. M., Folmer, R. H. A., Konings, R. N. H. & Hilbers, C. W. (1993). Overcoming the ambiguity problem encountered in the analysis of nuclear Overhauser magnetic resonance spectra of symmetrical dimer proteins. J. Am. Chem. Soc. 115, 3798-3799.
11. Folmer, R. H. A., Hilbers, C. W., Konings, R. N. H. & Hallenga, K. (1995). A 13C double-filtered NOESY with strongly reduced artifacts and improved sensitivity. J. Biomol. NMR, 5, 427-432.
12. Haaf, A., Butler, P. J. G., Kent, H. M., Fearnley, I. M., Roberts, T. M., Neuhaus, D. & Stewart, M. (1996). The motile major sperm protein (MSP) from Ascaris suum is a symmetric dimer in solution. J. Mol. Biol. 260, 251-260.
13. Hommel, U., Harvey, T. S., Driscoll, P. C. & Campbell, I. D. (1992). Human epidermal growth factor: high resolution solution structure and comparison with human transforming growth factor α. J. Mol. Biol. 227, 271-282.
14. Italiano, J. E., Roberts, T. M., Stewart, M. & Fontana, C. A. (1996). Reconstitution in vitro of the motile apparatus from the amoeboid sperm of Ascaris shows that filament assembly can move membranes. Cell, 84, 105-114.
15. Joshi, H. C. (1998). Microtubule dynamics in living cells. Curr. Opin. Cell Biol. 10, 35-44.
16. King, K. L., Stewart, M., Roberts, T. M. & Seavy, M. (1992). Structure and macromolecular assembly of two isoforms of the major sperm protein (MSP) from the amoeboid sperm of the nematode, Ascaris suum. J. Cell Sci. 101, 847-857.
17. King, K. L., Essig, J., Roberts, T. M. & Moerland, T. S. (1994). Regulation of the Ascaris major sperm protein (MSP) cytoskeleton by intracellular pH. Cell Motil. Cytoskel. 27, 193-205.
18. Kraulis, P. J. (1991). A program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallog. 24, 946-950.
19. Machesky, L. M. & Pollard, T. D. (1993). Profilin as a potential mediator of membrane-cytoskeleton communication. J. Appl. Crystallog. 3, 381-385.
20. Merritt, E. A. & Murphy, M. E. P. (1994). Raster 3D Version 2.0 - A prgram for photorealistic molecular graphics. Acta Crystallog. sect. D, 50, 869-873.
21. 1H NMR spectroscopy: a zinc finger with a third strand of β-sheet. J. Mol. Biol. 228, 637-651.
22. 1H NMR. Proteins: Struct. Funct. Genet. 17, 297-309.
23. Nilges, M. (1995). Calculations of protein structures with ambiguous distance restraints. Automated assignment of ambiguous NOE cross-peaks and disulphide connectivities. J. Mol. Biol. 245, 645-660.
24. Nilges, M., Gronenborn, A. M., Brunger, A. T. & Clore, G. M. (1988). Determination of 3-dimensional structures of proteins by simulated annealing with interproton distance restraints - application to crambin, potato carboxypeptidase inhibitor and barley serine proteinase inhibitor. Protein Eng. 22, 27-38.
25. 1H) NMR spectroscopy - combined use with isotope labelling for studies of macromolecular conformation and intermolecular interactions. Quart. Rev. Biophys. 23, 39-96.
26. Roberts, T. M. & King, K. L. (1991). Centripetal flow and directional reassembly of the major sperm protein (MSP) cytoskeleton in the amoeboid sperm of the nematode Ascaris suum. Cell Motil. Cytoskel. 20, 228-241.
27. Roberts, T. M. & Stewart, M. (1995). Nematode sperm locomotion. Curr. Opin. Cell Biol. 7, 13-17.
28. Roberts, T. M. & Stewart, M. (1997). Nematode sperm: amoeboid movement without actin. Trends Cell Biol. 7, 368-373.
29. Roberts, T. M., Salmon, E. D. & Stewart, M. (1998). Hydrostatic pressure shows that lamellipodial motility in Ascaris sperm requires membrane-associated major sperm protein filament nucleation and elongation. J. Cell Biol. 140, 367-375.
30. Sepsenwol, S. & Taft, S. J. (1990). In vitro induction of crawling in the ameboid sperm of the nematode parasite, Ascaris suum. Cell Motil. Cytoskel. 15, 99-110.
31. Sepsenwol, S., Nguyen, M. & Braun, T. (1986). Adenylate cyclase activity is absent in inactive and motile sperm of the nematode parasite, Ascaris suum. J. Parasitol. 72, 962-964.
32. Sepsenwol, S., Ris, H. & Roberts, T. M. (1989). A unique cytoskeleton associated with crawling in the ameboid sperm of the nematode, Ascaris suum. J. Cell Biol. 108, 55-66.
33. Stewart, M., King, K. L. & Roberts, T. M. (1994). The motile major sperm protein (MSP) of Ascaris suum forms filaments constructed from two helical subfilaments. J. Mol. Biol. 242, 60-71.
34. Stonehouse, J., Shaw, G. L., Keeler, J. & Laue, E. D. (1994). Minimising sensitivity losses in gradient-selected 15N-1H HSQC spectra of proteins. J. Magn. Reson. 107, 178-184.
35. Studier, F. W., Rosenberg, A. H., Dunn, J. J. & Dubendorf, J. W. (1990). Use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzymol. 242 60-71.
36. Sze, K. H., Barsukov, I. L. & Roberts, G. (1995). Quantitative evaluation of cross-peak volumes in multidimensional spectra by nonlinear-least-squares curve-fitting. J. Magn. Reson. ser. A, 113, 185-195.
37. Theriot, J. A. (1995). The cell biology of infection by intracellular bacterial pathogens. Annu. Rev. Cell Biol. 11, 213-239.
38. Theriot, J. A. (1996). Worm sperm and advances in cell locomotion. Cell, 84, 1-4.