Register      Login
Australian Journal of Chemistry Australian Journal of Chemistry Society
An international journal for chemical science
Shopping Cart: ( empty )
You are here: Home > Journals > CH > CH19346
RESEARCH ARTICLE
Contents Vol 73(3)

The Crystal Structure of the Manganese Superoxide Dismutase from Geobacillus stearothermophilus: Parker and Blake (1988) Revisited*

Julian J. Adams A , Craig J. Morton https://orcid.org/0000-0001-5452-5193 B C and Michael W. Parker A B C
+ Author Affiliations
- Author Affiliations

A St Vincent’s Institute of Medical Research, 9 Princes Street, Fitzroy, Vic. 3065, Australia.

B Department of Biochemistry and Molecular Biology, Bio21 Molecular Science and Biotechnology Institute, The University of Melbourne, 30 Flemington Road, Parkville, Vic. 3010, Australia.

C Corresponding authors. Email: Craig.Morton@unimelb.edu.au; mwp@unimelb.edu.au

Australian Journal of Chemistry 73(3) 145-150 https://doi.org/10.1071/CH19346
Submitted: 23 July 2019  Accepted: 26 August 2019   Published: 2 October 2019

Abstract

Superoxide dismutase (SOD) is an almost ubiquitous metalloenzyme in aerobic organisms that catalyses the disproportionation of superoxide. Geobacillus stearothermophilus MnSOD is the only published MnSOD structure that does not have its coordinates publicly available, yet it is one of the more cited structures in the SOD literature. The structure has now been refined with modern programs, yielding a significantly improved structure which has been deposited in the Protein Data Bank. Importantly, the further refined structure reveals the presence of a catalytically important fifth ligand, water, to the metal centre, as observed in other SOD structures.


References

[1]  J. M. McCord, I. Fridovich, J. Biol. Chem. 1969, 244, 6049.
         | 5389100PubMed |

[2]  B. B. Keele, J. M. McCord, I. Fridovich, J. Biol. Chem. 1970, 245, 6176.
         | 4921969PubMed |

[3]  F. J. Yost, I. Fridovich, J. Biol. Chem. 1973, 248, 4905.
         | 4352182PubMed |

[4]  H. D. Youn, E. J. Kim, J. H. Roe, Y. C. Hah, S. O. Kang, Biochem. J. 1996, 318, 889.
         | Crossref | GoogleScholarGoogle Scholar | 8836134PubMed |

[5]  A. J. Case, Antioxidants 2017, 6, 82.
         | Crossref | GoogleScholarGoogle Scholar |

[6]  H. M. Berman, J. Westbrook, Z. Feng, G. Gilliland, T. N. Bhat, H. Weissig, I. N. Shindyalov, P. E. Bourne, Nucleic Acids Res. 2000, 28, 235.
         | Crossref | GoogleScholarGoogle Scholar | 10592235PubMed |

[7]  A. Drechsler, F. Separovic, IUBMB Life 2003, 55, 515.
         | Crossref | GoogleScholarGoogle Scholar | 14658757PubMed |

[8]  M. J. Knight, I. C. Felli, R. Pierattelli, L. Emsley, G. Pintacuda, Acc. Chem. Res. 2013, 46, 2108.
         | Crossref | GoogleScholarGoogle Scholar | 23506094PubMed |

[9]  W. C. Stallings, K. A. Pattridge, R. K. Strong, M. L. Ludwig, J. Biol. Chem. 1985, 260, 16424.
         | 4066716PubMed |

[10]  M. W. Parker, C. C. Blake, J. Mol. Biol. 1988, 199, 649.
         | Crossref | GoogleScholarGoogle Scholar | 3351946PubMed |

[11]  G. E. Borgstahl, H. E. Parge, M. J. Hickey, W. F. Beyer, R. A. Hallewell, J. A. Tainer, Cell 1992, 71, 107.
         | Crossref | GoogleScholarGoogle Scholar | 1394426PubMed |

[12]  W. Atzenhofer, G. Regelsberger, U. Jacob, G. Peschek, P. Furtmuller, R. Huber, C. Obinger, J. Mol. Biol. 2002, 321, 479.
         | Crossref | GoogleScholarGoogle Scholar | 12162960PubMed |

[13]  R. A. Edwards, H. M. Baker, M. M. Whittaker, J. W. Whittaker, G. B. Jameson, E. N. Baker, J. Biol. Inorg. Chem. 1998, 3, 161.
         | Crossref | GoogleScholarGoogle Scholar |

[14]  S. Fluckiger, P. R. Mittl, L. Scapozza, H. Fijten, G. Folkers, M. G. Grütter, K. Blaser, R. Crameri, J. Immunol. 2002, 168, 1267.
         | Crossref | GoogleScholarGoogle Scholar | 11801664PubMed |

[15]  T. Haikarainen, C. Frioux, L. Q. Zhnag, D. C. Li, A. C. Papageorgiou, Biochim. Biophys. Acta 2014, 1844, 422.
         | Crossref | GoogleScholarGoogle Scholar | 24316252PubMed |

[16]  C. H. Trinh, T. Hunter, E. E. Stewart, S. E. Phillips, G. J. Hunter, Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 2008, 64, 1110.
         | Crossref | GoogleScholarGoogle Scholar | 19052361PubMed |

[17]  R. J. Dennis, E. Micossi, J. McCarthy, E. Moe, E. J. Gordon, S. Kozielski-Stuhrmann, G. A. Leonard, S. McSweeney, Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 2006, 62, 325.
         | Crossref | GoogleScholarGoogle Scholar | 16582477PubMed |

[18]  D. S. Retnoningrum, H. Yoshida, S. Arumsari, S. Kamitori, W. T. Ismaya, Acta Crystallogr. F Struct. Biol. Commun. 2018, 74, 135.
         | Crossref | GoogleScholarGoogle Scholar | 29497016PubMed |

[19]  Y. Sheng, T. A. Stich, K. Barnese, E. B. Gralla, D. Cascio, R. D. Britt, D. E. Cabelli, J. Selverstone Valentine, J. Am. Chem. Soc. 2011, 133, 20878.
         | Crossref | GoogleScholarGoogle Scholar | 22077216PubMed |

[20]  C. J. Bond, J. Huang, R. Hajduk, K. E. Flick, P. J. Heath, B. L. Stoddard, Acta Crystallogr. D Biol. Crystallogr. 2000, 56, 1359.
         | Crossref | GoogleScholarGoogle Scholar | 11053832PubMed |

[21]  D. Ringe, G. A. Petsko, F. Yamakura, K. Suzuki, D. Ohmori, Proc. Natl. Acad. Sci. USA 1983, 80, 3879.
         | Crossref | GoogleScholarGoogle Scholar | 6575382PubMed |

[22]  W. C. Stallings, T. B. Powers, K. A. Pattridge, J. A. Fee, M. L. Ludwig, Proc. Natl. Acad. Sci. USA 1983, 80, 3884.
         | Crossref | GoogleScholarGoogle Scholar | 6346322PubMed |

[23]  J. B. Cooper, K. McIntyre, M. O. Badasso, S. P. Wood, Y. Zhang, T. R. Garbe, D. Young, J. Mol. Biol. 1995, 246, 531.
         | Crossref | GoogleScholarGoogle Scholar | 7877174PubMed |

[24]  M. Schmidt, B. Meier, F. Parak, J. Biol. Inorg. Chem. 1996, 1, 532.
         | Crossref | GoogleScholarGoogle Scholar |

[25]  J. H. Lim, Y. G. Yu, Y. S. Han, S. Cho, B. Y. Ahn, S.-H. Kim, Y. Cho, J. Mol. Biol. 1997, 270, 259.
         | Crossref | GoogleScholarGoogle Scholar | 9236127PubMed |

[26]  T. Ursby, B. S. Adinolfi, S. Al-Karadaghi, E. De Vendittis, V. Bocchini, J. Mol. Biol. 1999, 286, 189.
         | Crossref | GoogleScholarGoogle Scholar | 9931259PubMed |

[27]  S. Knapp, S. Kardinahl, N. Hellgren, G. Tibbelin, G. Schafer, R. Ladenstein, J. Mol. Biol. 1999, 285, 689.
         | Crossref | GoogleScholarGoogle Scholar | 9878438PubMed |

[28]  O. Dao, K. Asaithambi, B. K. Na, K. H. Lee, Acta Crystallogr. F Struct. Biol. Commun. 2019, 75, 480.
         | Crossref | GoogleScholarGoogle Scholar | 31282867PubMed |

[29]  I. Q. H. Phan, D. R. Davies, N. S. Moretti, D. Shanmugam, I. Cestari, A. Anupama, J. W. Fairman, T. E. Edwards, K. Stuart, S. Schenkman, P. J. Myler, Acta Crystallogr. F Struct. Biol. Commun. 2015, 71, 615.
         | Crossref | GoogleScholarGoogle Scholar |

[30]  I. G. Munoz, J. F. Moran, M. Becana, G. Montoya, Acta Crystallogr. D Biol. Crystallogr. 2003, 59, 1070.
         | Crossref | GoogleScholarGoogle Scholar | 12777777PubMed |

[31]  S. Sugio, B. Y. Hiraoka, F. Yamakura, Eur. J. Biochem. 2000, 267, 3487.
         | Crossref | GoogleScholarGoogle Scholar | 10848964PubMed |

[32]  F. Yamakura, J. Biochem. 1978, 83, 849.
         | Crossref | GoogleScholarGoogle Scholar |

[33]  F. Yamakura, K. Kobayashi, H. Ue, M. Konno, Eur. J. Biochem. 1995, 227, 700.
         | Crossref | GoogleScholarGoogle Scholar | 7867628PubMed |

[34]  F. Yamakura, K. Suzuki, J. Biochem. 1980, 88, 191.
         | 7410333PubMed |

[35]  W. F. Beyer, I. Fridovich, Biochemistry 1987, 26, 1251.
         | Crossref | GoogleScholarGoogle Scholar | 3552043PubMed |

[36]  M. M. Whittaker, J. W. Whittaker, Biochemistry 1997, 36, 8923.
         | Crossref | GoogleScholarGoogle Scholar | 9220980PubMed |

[37]  M. M. Whittaker, J. W. Whittaker, J. Biol. Chem. 1999, 274, 34751.
         | Crossref | GoogleScholarGoogle Scholar | 10574944PubMed |

[38]  S. Miriyala, I. Spasojevic, A. Tovmasyan, D. Salvemini, Z. Vujaskovic, D. St Clair, I. Batinic-Haberle, Biochim. Biophys. Acta, Mol. Basis Dis. 2012, 1822, 794.
         | Crossref | GoogleScholarGoogle Scholar |

[39]  B. Y. Hiraoka, F. Yamakura, S. Sugio, K. Nakayama, Biochem. J. 2000, 345, 345.
         | Crossref | GoogleScholarGoogle Scholar | 10620511PubMed |

[40]  C. D. Pennington, E. M. Gregory, J. Bacteriol. 1986, 166, 528.
         | Crossref | GoogleScholarGoogle Scholar | 3700336PubMed |

[41]  E. M. Gregory, C. H. Dapper, Arch. Biochem. Biophys. 1983, 220, 293.
         | Crossref | GoogleScholarGoogle Scholar | 6830240PubMed |

[42]  B. Meier, A. P. Sehn, M. E. Schinina, D. Barra, Eur. J. Biochem. 1994, 219, 463.
         | Crossref | GoogleScholarGoogle Scholar | 8307013PubMed |

[43]  M. M. Whittaker, J. W. Whittaker, J. Biol. Inorg. Chem. 2000, 5, 402.
         | 10907751PubMed |

[44]  S. Yamano, T. Maruyama, J. Biochem. 1999, 125, 186.
         | Crossref | GoogleScholarGoogle Scholar | 9880816PubMed |

[45]  R. Santos, S. Bocquet, A. Puppo, D. Touati, J. Bacteriol. 1999, 181, 4509.
         | 10419947PubMed |

[46]  M. E. Martin, B. R. Byers, M. O. Olson, M. L. Salin, J. E. Arceneaux, C. Tolbert, J. Biol. Chem. 1986, 261, 9361.
         | 3722201PubMed |

[47]  C. K. Vance, A. F. Miller, Biochemistry 1998, 37, 5518.
         | Crossref | GoogleScholarGoogle Scholar | 9548935PubMed |

[48]  C. K. Vance, A. F. Miller, Biochemistry 2001, 40, 13079.
         | Crossref | GoogleScholarGoogle Scholar | 11669646PubMed |

[49]  M. W. Parker, C. C. Blake, FEBS Lett. 1988, 229, 377.
         | Crossref | GoogleScholarGoogle Scholar | 3345848PubMed |

[50]  B. Meier, C. Scherk, M. Schmidt, F. Parak, Biochem. J. 1998, 331, 403.
         | Crossref | GoogleScholarGoogle Scholar | 9531477PubMed |

[51]  D. L. Tierney, J. A. Fee, M. L. Ludwig, J. E. Penner-Hahn, Biochemistry 1995, 34, 1661.
         | Crossref | GoogleScholarGoogle Scholar | 7849025PubMed |

[52]  D. W. Banner, P. R. Evans, D. J. Marsh, D. C. Phillips, J. Appl. Cryst. 1977, 10, 45.
         | Crossref | GoogleScholarGoogle Scholar |

[53]  G. C. Fox, K. C. Holmes, Acta Crystallogr. 1966, 20, 886.
         | Crossref | GoogleScholarGoogle Scholar |

[54]  S. French, K. Wilson, Acta Crystallogr. A 1978, 34, 517.
         | Crossref | GoogleScholarGoogle Scholar |

[55]  R. Huber, G. Kopfmann, Acta Crystallogr. A 1969, 25, 143.
         | Crossref | GoogleScholarGoogle Scholar |

[56]  T. A. Jones, Methods Enzymol. 1985, 115, 157.
         | Crossref | GoogleScholarGoogle Scholar | 3841179PubMed |

[57]  J. L. Sussman, Methods Enzymol. 1985, 115, 271.
         | Crossref | GoogleScholarGoogle Scholar | 2417093PubMed |

[58]  W. Furey, B. C. Wang, M. Sax, J. Appl. Cryst. 1982, 15, 160.
         | Crossref | GoogleScholarGoogle Scholar |

[59]  J. H. Konnert, W. A. Hendrickson, Acta Crystallogr. A 1980, 36, 344.
         | Crossref | GoogleScholarGoogle Scholar |

[60]  A. T. Brunger, P. D. Adams, G. M. Clore, W. L. DeLano, P. Gros, R. W. Grosse-Kunstleve, J.-S. Jiang, J. Kuszewski, M. Nilges, N. S. Pannu, R. J. Read, L. M. Rice, T. Simonson, G. L. Warren, Acta Crystallogr. D Biol. Crystallogr. 1998, 54, 905.
         | Crossref | GoogleScholarGoogle Scholar | 9757107PubMed |

[61]  A. Roussel, C. Cambillau, Silicon Graphics Geometry Partner Directory, Silicon Graphics 1989, 77–8.

[62]  P. D. Adams, P. V. Afonine, G. Bunkoczi, V. B. Chen, I. W. Davis, N. Echols, J. J. Headd, L.-W. Hung, G. J. Kapral, R. W. Grosse-Kunstleve, A. J. McCoy, N. W. Moriarty, R. Oeffner, R. J. Read, D. C. Richardson, J. S. Richardson, T. C. Terwilliger, P. H. Zwart, Acta Crystallogr. D Biol. Crystallogr. 2010, 66, 213.
         | Crossref | GoogleScholarGoogle Scholar | 20124702PubMed |

[63]  P. D. Adams, D. Baker, A. T. Brunger, R. Das, F. DiMaio, R. J. Read, D. C. Richardson, J. S. Richardson, T. C. Terwilliger, Annu. Rev. Biophys. 2013, 42, 265.
         | Crossref | GoogleScholarGoogle Scholar | 23451892PubMed |

[64]  M. D. Winn, M. N. Isupov, G. N. Murshudov, Acta Crystallogr. D Biol. Crystallogr. 2001, 57, 122.
         | Crossref | GoogleScholarGoogle Scholar | 11134934PubMed |

[65]  G. N. Ramachandran, V. Sasisekharan, Adv. Protein Chem. 1968, 23, 283.
         | Crossref | GoogleScholarGoogle Scholar | 4882249PubMed |

[66]  R. A. Laskowski, M. W. MacArthur, D. S. Moss, J. M. Thornton, J. Appl. Cryst. 1993, 26, 283.
         | Crossref | GoogleScholarGoogle Scholar |

[67]  G. E. O. Borgstahl, H. E. Parge, M. J. Hickey, M. J. Johnson, M. Boissinot, R. A. Hallewell, J. R. Lepock, D. E. Cabelli, J. A. Tainer, Biochemistry 1996, 35, 4287.
         | Crossref | GoogleScholarGoogle Scholar |

[68]  T. Hunter, R. Bonetta, A. Sacco, M. Vella, P.-M. Sultana, C. H. Trinh, H. B. R. Fadia, T. Borowski, R. Garcia‐Fandiño, T. Stockner, G. J. Hunter, Chem. – Eur. J. 2018, 24, 5303.
         | Crossref | GoogleScholarGoogle Scholar | 29178484PubMed |

[69]  W. Li, H. Wang, Z. Chen, Q. Ye, Y. Tian, X. Xu, Z. Huang, P. Li, X. Tan, Chem. Commun. 2014, 50, 584.
         | Crossref | GoogleScholarGoogle Scholar |

[70]  R. P. Joosten, J. Salzemann, V. Bloch, H. Stockinger, A. C. Berglund, C. Blanchet, E. Bongcam-Rudloff, C. Combet, A. L. Da Costa, G. Deleage, M. Diarena, R. Fabbretti, G. Fettahi, V. Flegel, A. Gisel, V. Kasam, T. Kervinen, E. Korpelainen, K. Mattila, M. Pagni, M. Reichstadt, V. Breton, I. J. Tickle, G. Vriend, J. Appl. Cryst. 2009, 42, 376.
         | Crossref | GoogleScholarGoogle Scholar |

[71]  R. P. Joosten, G. Vriend, Science 2007, 317, 195.
         | Crossref | GoogleScholarGoogle Scholar | 17626865PubMed |

[72]  I. Shabalin, Z. Dauter, M. Jaskolski, W. Minor, A. Wlodawer, Acta Crystallogr. D Biol. Crystallogr. 2015, 71, 1965.
         | Crossref | GoogleScholarGoogle Scholar | 26327386PubMed |