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Pure and Applied Chemistry

The Scientific Journal of IUPAC

Ed. by Burrows, Hugh / Weir, Ron / Stohner, Jürgen

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Volume 81, Issue 4 (Jan 2009)

Issues

Mapping catalytic promiscuity in the alkaline phosphatase superfamily

Stefanie Jonas
  • Corresponding author
  • Department of Biochemistry, University of Cambridge, 80 Tennis Court Road, Cambridge, CB2 1GA, UK
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Florian Hollfelder
  • Corresponding author
  • Department of Biochemistry, University of Cambridge, 80 Tennis Court Road, Cambridge, CB2 1GA, UK
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
Published Online: 2009-01-01 | DOI: https://doi.org/10.1351/PAC-CON-08-10-20

"Promiscuous" enzymes possess activities in addition to their native ones. Promiscuous activities could be remnants from an evolutionary ancestor that has been adapted to fulfil a new function following gene duplication. Alternatively, the observation of promiscuity could indicate that an enzyme has the potential to evolve into a new catalyst. Thus, the observation of promiscuity defines functional relationships in enzyme superfamilies. Crosswise promiscuity can provide an additional layer of connectivity between members of a - usually structurally defined - superfamily to establish a system for tracking the emergence and interconversion of enzymatic function. The systematic analysis of measured promiscuous rates may serve as a basis for drawing up phylogenetic relationships based on the potential for catalysis and may be useful for active use in directed evolution, suggesting evolutionary "short cuts". We review recent observations of catalytic promiscuity in members of the alkaline phosphatase (AP) superfamily that exhibit reciprocal relationships of crosswise promiscuity with rate accelerations (kcat/KM)/k2 between 106 and 1018. Specifically, we focus on the mechanistic features that appear to form the basis of catalytic promiscuity in this superfamily.

Keywords: catalytic promiscuity; enzymology; formylglycine; hydrolase; metalloenzyme; phosphate transfer; sulfate transfer; superfamily

Conference

International Conference on Physical Organic Chemistry (ICPOC-19), International Conference on Physical Organic Chemistry, ICPOC, Physical Organic Chemistry, 19th, Santiago de Compostela, Spain, 2008-07-13–2008-07-18

References

  • 1.

    , L. Jiang, E. A. Althoff, F. R. Clemente, L. Doyle, D. Rothlisberger, A. Zanghellini, J. L. Gallaher, J. L. Betker, F. Tanaka, C. F. Barbas, 3rd, D. Hilvert, K. N. Houk, B. L. Stoddard, D. Baker. Science 319, 1387 (2008).CrossrefGoogle Scholar

  • 2.

    , D. Rothlisberger, O. Khersonsky, A. M. Wollacott, L. Jiang, J. DeChancie, J. Betker, J. L. Gallaher, E. A. Althoff, A. Zanghellini, O. Dym, S. Albeck, K. N. Houk, D. S. Tawfik, D. Baker. Nature 453, 190 (2008).CrossrefGoogle Scholar

  • 3.

    , C. A. Orengo, J. M. Thornton. Annu. Rev. Biochem. 74, 867 (2005).CrossrefGoogle Scholar

  • 4.

    A. G. Murzin, S. E. Brenner, T. Hubbard, C. Chothia. J. Mol. Biol. 247, 536 (1995).Google Scholar

  • 5.

    , C. A. Orengo, A. D. Michie, S. Jones, D. T. Jones, M. B. Swindells, J. M. Thornton. Structure 5, 1093 (1997).CrossrefGoogle Scholar

  • 6.

    , F. Pearl, A. Todd, I. Sillitoe, M. Dibley, O. Redfern, T. Lewis, C. Bennett, R. Marsden, A. Grant, D. Lee, A. Akpor, M. Maibaum, A. Harrison, T. Dallman, G. Reeves, I. Diboun, S. Addou, S. Lise, C. Johnston, A. Sillero, J. Thornton, C. Orengo. Nucleic Acids Res. 33, D247 (2005).CrossrefGoogle Scholar

  • 7.

    , D. Wilson, M. Madera, C. Vogel, C. Chothia, J. Gough. Nucleic Acids Res. 35, D308 (2007).CrossrefGoogle Scholar

  • 8.

    , S. D. Brown, J. A. Gerlt, J. L. Seffernick, P. C. Babbitt. Genome Biol. 7, R8 (2006).CrossrefGoogle Scholar

  • 9.

    , M. E. Glasner, J. A. Gerlt, P. C. Babbitt. Curr. Opin. Chem. Biol. 10, 492 (2006).CrossrefGoogle Scholar

  • 10.

    , O. Khersonsky, C. Roodveldt, D. S. Tawfik. Curr. Opin. Chem. Biol. 10, 498 (2006).CrossrefGoogle Scholar

  • 11.

    , P. J. O'Brien, D. Herschlag. Chem. Biol. 6, R91 (1999).CrossrefGoogle Scholar

  • 12.

    , U. T. Bornscheuer, R. J. Kazlauskas. Angew. Chem., Int. Ed. 43, 6032 (2004).CrossrefGoogle Scholar

  • 13.

    S. Jonas, F. Hollfelder. In The Protein Engineering Handbook, U. Bornscheuer, S. Lutz, (Eds.), pp. 47-79, Wiley-VCH, Weinhein (2008).Google Scholar

  • 14.

    , R. A. Jensen. Annu. Rev. Microbiol. 30, 409 (1976).CrossrefGoogle Scholar

  • 15.

    , S. Bershtein, D. S. Tawfik. Mol. Biol. Evol. 25, 2311 (2008).CrossrefGoogle Scholar

  • 16.

    S. Ohno. Evolution by Gene Duplication, Springer, New York (1970).Google Scholar

  • 17.

    , S. Bershtein, M. Segal, R. Bekerman, N. Tokuriki, D. S. Tawfik. Nature 444, 929 (2006).CrossrefGoogle Scholar

  • 18.

    , C. Roodveldt, D. S. Tawfik. Biochemistry 44, 12728 (2005).CrossrefGoogle Scholar

  • 19.

    , J. E. Vick, D. M. Schmidt, J. A. Gerlt. Biochemistry 44, 11722 (2005).CrossrefGoogle Scholar

  • 20.

    A. Aharoni, L. Gaidukov, O. Khersonsky, Q. Mc, S. Gould, C. Roodveldt, D. S. Tawfik. Nat. Genet. 37, 73 (2005).Google Scholar

  • 21.

    , S. M. Gould, D. S. Tawfik. Biochemistry 44, 5444 (2005).CrossrefGoogle Scholar

  • 22.

    , G. J. Poelarends, C. P. Whitman. Bioorg. Chem. 32, 376 (2004).CrossrefGoogle Scholar

  • 23.

    , D. M. Schmidt, E. C. Mundorff, M. Dojka, E. Bermudez, J. E. Ness, S. Govindarajan, P. C. Babbitt, J. Minshull, J. A. Gerlt. Biochemistry 42, 8387 (2003).CrossrefGoogle Scholar

  • 24.

    , W. M. Patrick, I. Matsumura. J. Mol. Biol. 377, 323 (2008).CrossrefGoogle Scholar

  • 25.

    , W. M. Patrick, E. M. Quandt, D. B. Swartzlander, I. Matsumura. Mol. Biol. Evol. 24, 2716 (2007).CrossrefGoogle Scholar

  • 26.

    , M. Y. Galperin, A. Bairoch, E. V. Koonin. Protein Sci. 7, 1829 (1998).CrossrefGoogle Scholar

  • 27.

    , P. J. O'Brien, D. Herschlag. J. Am. Chem. Soc. 120, 12369 (1998).CrossrefGoogle Scholar

  • 28.

    , P. J. O'Brien, D. Herschlag. Biochemistry 40, 5691 (2001).CrossrefGoogle Scholar

  • 29.

    , L. F. Olguin, S. E. Askew, A.-M. O'Donoghue, F. Hollfelder. J. Am. Chem. Soc. 130, 16547 (2008).CrossrefGoogle Scholar

  • 30.

    A. C. Babtie, S. Bandyopadhyay, L. F. Olguin, F. Hollfelder. Angew. Chem., Int. Ed. (2009). In press (DOI: 10.1002/anie.200805843).CrossrefGoogle Scholar

  • 31.

    , J. G. Zalatan, T. D. Fenn, A. T. Brunger, D. Herschlag. Biochemistry 45, 9788 (2006).CrossrefGoogle Scholar

  • 32.

    , J. K. Lassila, D. Herschlag. Biochemistry 47, 12853 (2008).CrossrefGoogle Scholar

  • 33.

    B. van Loo, S. Jonas, A. C. Babtie, M. Hyvonen, F. Hollfelder. (2008). Submitted for publication.Google Scholar

  • 34.

    R. Bhadra, N. Srinivasan, S. B. Pandit. In Silico Biol. 5, 379 (2005).Google Scholar

  • 35.

    T. W. Reid, I. B. Wilson. In The Enzymes, P. D. Boyer (Ed.), pp. 373-415, Academic Press, New York (1971).Google Scholar

  • 36.

    , J. E. Coleman. Annu. Rev. Biophys. Biomol. Struct. 21, 441 (1992).CrossrefGoogle Scholar

  • 37.

    , K. M. Holtz, E. R. Kantrowitz. FEBS Lett. 462, 7 (1999).CrossrefGoogle Scholar

  • 38.

    , M. Y. Galperin, M. J. Jedrzejas. Proteins 45, 318 (2001).CrossrefGoogle Scholar

  • 39.

    , R. Gijsbers, H. Ceulemans, W. Stalmans, M. Bollen. J. Biol. Chem. 276, 1361 (2001).CrossrefGoogle Scholar

  • 40.

    , S. R. Hanson, M. D. Best, C. H. Wong. Angew. Chem., Int. Ed. 43, 5736 (2004).CrossrefGoogle Scholar

  • 41.

    , G. Lukatela, N. Krauss, K. Theis, T. Selmer, V. Gieselmann, K. von Figura, W. Saenger. Biochemistry 37, 3654 (1998).CrossrefGoogle Scholar

  • 42.

    , B. Stec, K. M. Holtz, E. R. Kantrowitz. J. Mol. Biol. 299, 1303 (2000).CrossrefGoogle Scholar

  • 43.

    , I. Boltes, H. Czapinska, A. Kahnert, R. von Bulow, T. Dierks, B. Schmidt, K. von Figura, M. A. Kertesz, I. Uson. Structure 9, 483 (2001).CrossrefGoogle Scholar

  • 44.

    , S. Jonas, B. van Loo, M. Hyvonen, F. Hollfelder. J. Mol. Biol. 384, 120 (2008).CrossrefGoogle Scholar

  • 45.

    , C. S. Bond, P. R. Clements, S. J. Ashby, C. A. Collyer, S. J. Harrop, J. J. Hopwood, J. M. Guss. Structure 5, 277 (1997).CrossrefGoogle Scholar

  • 46.

    , C.-I. Braenden. Q. Rev. Biophys. 13, 317 (1980).CrossrefGoogle Scholar

  • 47.

    , S. B. Dotson, C. E. Smith, C. S. Ling, G. F. Barry, G. M. Kishore. J. Biol. Chem. 271, 25754 (1996).CrossrefGoogle Scholar

  • 48.

    , M. J. Jedrzejas, M. Chander, P. Setlow, G. Krishnasamy. EMBO J. 19, 1419 (2000).CrossrefGoogle Scholar

  • 49.

    J. E. Coleman, K. Nakamura, J. F. Chlebowski. J. Biol. Chem. 258, 386 (1983).Google Scholar

  • 50.

    , E. E. Kim, H. W. Wyckoff. J. Mol. Biol. 218, 449 (1991).CrossrefGoogle Scholar

  • 51.

    , B. Schmidt, T. Selmer, A. Ingendoh, K. von Figura. Cell 82, 271 (1995).CrossrefGoogle Scholar

  • 52.

    , C. Szameit, C. Miech, M. Balleininger, B. Schmidt, K. von Figura, T. Dierks. J. Biol. Chem. 274, 15375 (1999).CrossrefGoogle Scholar

  • 53.

    , N. H. Williams, B. Takasaki, M. Wall, J. Chin. Acc. Chem. Res. 32, 485 (1999).CrossrefGoogle Scholar

  • 54.

    , D. E. Wilcox. Chem. Rev. 96, 2435 (1996).CrossrefGoogle Scholar

  • 55.

    , J. A. Cowan. Chem. Rev. 98, 1067 (1998).CrossrefGoogle Scholar

  • 56.

    , T. A. Steitz, J. A. Steitz. Proc. Natl. Acad. Sci. USA 90, 6498 (1993).CrossrefGoogle Scholar

  • 57.

    , A. Waldow, B. Schmidt, T. Dierks, R. von Bulow, K. von Figura. J. Biol. Chem. 274, 12284 (1999).CrossrefGoogle Scholar

  • 58.

    , R. von Bulow, B. Schmidt, T. Dierks, K. von Figura, I. Uson. J. Mol. Biol. 305, 269 (2001).CrossrefGoogle Scholar

  • 59.

    , P. J. O'Brien, J. K. Lassila, T. D. Fenn, J. G. Zalatan, D. Herschlag. Biochemistry 47, 7663 (2008).CrossrefGoogle Scholar

  • 60.

    , J. G. Zalatan, T. D. Fenn, D. Herschlag. J. Mol. Biol. 384, 1174 (2008).CrossrefGoogle Scholar

  • 61.

    , M. Recksiek, T. Selmer, T. Dierks, B. Schmidt, K. von Figura. J. Biol. Chem. 273, 6096 (1998).CrossrefGoogle Scholar

  • 62.

    , J. Wang, E. R. Kantrowitz. Protein Sci. 15, 2395 (2006).CrossrefGoogle Scholar

  • 63.

    , K. Yang, W. W. Metcalf. Proc. Natl. Acad. Sci. USA 101, 7919 (2004).CrossrefGoogle Scholar

  • 64.

    , F. Hollfelder, D. Herschlag. Biochemistry 34, 12255 (1995).CrossrefGoogle Scholar

  • 65.

    , A. J. Kirby, W. P. Jencks. J. Am. Chem. Soc. 87, 3209 (1965).CrossrefGoogle Scholar

  • 66.

    , A. C. Hengge, I. Onyido. Curr. Org. Chem. 9, 61 (2005).CrossrefGoogle Scholar

  • 67.

    , J. G. Zalatan, D. Herschlag. J. Am. Chem. Soc. 128, 1293 (2006).CrossrefGoogle Scholar

  • 68.

    , P. J. O'Brien, D. Herschlag. Biochemistry 41, 3207 (2002).CrossrefGoogle Scholar

  • 69.

    J. G. Zalatan, I. Catrina, R. Mitchell, P. K. Grzyska, J. O'Brien P, D. Herschlag, A. C. Hengge. J. Am. Chem. Soc. 129, 9789 (2007).Google Scholar

  • 70.

    , R. Wolfenden. Chem. Rev. 106, 3379 (2006).CrossrefGoogle Scholar

  • 71.

    , R. Wolfenden, M. J. Snider. Acc. Chem. Res. 34, 938 (2001).CrossrefGoogle Scholar

  • 72.

    , A. Radzicka, R. Wolfenden. Science 267, 90 (1995).CrossrefGoogle Scholar

  • 73.

    , I. Nikolic-Hughes, J. O'Brien, P. D. Herschlag. J. Am. Chem. Soc. 127, 9314 (2005).CrossrefGoogle Scholar

  • 74.

    , I. Catrina, P. J. O'Brien, J. Purcell, I. Nikolic-Hughes, J. G. Zalatan, A. C. Hengge, D. Herschlag. J. Am. Chem. Soc. 129, 5760 (2007).CrossrefGoogle Scholar

  • 75.

    , L. Sun, D. C. Martin, E. R. Kantrowitz. Biochemistry 38, 2842 (1999).CrossrefGoogle Scholar

  • 76.

    , J. Chin, M. Banaszczyk, V. Jubian, X. Zou. J. Am. Chem. Soc. 111, 186 (1989).CrossrefGoogle Scholar

  • 77.

    , S. J. Benkovic, P. A. Benkovic. J. Am. Chem. Soc. 88, 5504 (1966).CrossrefGoogle Scholar

  • 78.

    , J. Purcell, A. C. Hengge. J. Org. Chem. 70, 8437 (2005).CrossrefGoogle Scholar

  • 79.

    , A. J. Kirby, A. G. Vargolis. J. Am. Chem. Soc. 89, 415 (1967).CrossrefGoogle Scholar

  • 80.

    , E. J. Fendler, J. H. Fendler. J. Org. Chem. 33, 3852 (1968).CrossrefGoogle Scholar

  • 81.

    , G. Feng, D. Natale, R. Prabaharan, J. C. Mareque-Rivas, N. H. Williams. Angew. Chem., Int. Ed. 45, 7056 (2006).CrossrefGoogle Scholar

  • 82.

    , J. R. Morrow, O. Iranzo. Curr. Opin. Chem. Biol. 8, 192 (2004).CrossrefGoogle Scholar

  • 83.

    N. H. Williams. Biochim. Biophys. Acta 1697, 279 (2004).Google Scholar

  • 84.

    , J. Kofoed, J.-L. Reymond. Curr. Opin. Chem. Biol. 9, 656 (2005).CrossrefGoogle Scholar

  • 85.

    , A. Aharoni, L. Gaidukov, S. Yagur, L. Toker, I. Silman, D. S. Tawfik. Proc. Natl. Acad. Sci. USA 101, 482 (2004).CrossrefGoogle Scholar

  • 86.

    , M. Harel, A. Aharoni, L. Gaidukov, B. Brumshtein, O. Khersonsky, R. Meged, H. Dvir, R. B. Ravelli, A. McCarthy, L. Toker, I. Silman, J. L. Sussman, D. S. Tawfik. Nat. Struct. Mol. Biol. 11, 412 (2004).CrossrefGoogle Scholar

  • 87.

    , C. Roodveldt, D. S. Tawfik. Protein Eng. Des. Sel. 18, 51 (2005).CrossrefGoogle Scholar

  • 88.

    , H. Shim, S. B. Hong, F. M. Raushel. J. Biol. Chem. 273, 17445 (1998).CrossrefGoogle Scholar

  • 89.

    , D. W. Christianson, J. D. Cox. Annu. Rev. Biochem. 68, 33 (1999).CrossrefGoogle Scholar

About the article

Published Online: 2009-01-01

Published in Print: 2009-01-01


Citation Information: Pure and Applied Chemistry, ISSN (Online) 1365-3075, ISSN (Print) 0033-4545, DOI: https://doi.org/10.1351/PAC-CON-08-10-20.

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