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High pressure macromolecular crystallography for structural biology: a review

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Central European Journal of Biology

Abstract

In recent years, significant progress in high pressure macromolecular crystallography has been observed. It can be attributed both to the developments in experimental techniques, as well as to recognition of importance of high pressure protein studies in biochemistry and biophysics. The number of protein structures determined at pressure up to 1 GPa is growing. The unique advantages of this method can greatly improve the investigation of higher energy conformers of functional significance and our understanding of functionally important conformers, protein folding processes and the structural base of conformational diseases.

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References

  1. Winter R., High pressure effects in molecular bioscience, In: Riad Manaa M., (Ed.), Chemistry at extreme conditions, Elsevier B.V., 2005, 29–82

  2. Katrusiak A., High-pressure crystallography, Acta Cryst., 2008, A64, 135–148

    CAS  Google Scholar 

  3. Paszkowicz W., High-pressure powder X-ray diffraction at the turn of the century, Nucl. Instr. Meth. Phys. Res. B, 2002, 198, 142–182

    Article  CAS  Google Scholar 

  4. McMillan P.C.F., Crystallography and solid state chemistry at high pressure, In: Katrusiak A., McMillan P.F., (Eds.), High Pressure Crystallography, Kluwer, Dordrecht, 2004, 367–392

    Google Scholar 

  5. Liebermann R.C., Li B.S., Ultrahigh-pressure mineralogy:physics and chemistry of the Earth’s deep interior, In: Hemley R.J., Mao H.-K., (Eds.), Reviews in Mineralogy, Mineralogical Society of America, Washington, DC, 1998, 37, 459–492

    Google Scholar 

  6. Duffy T.S., Synchrotron facilities and the study of the Earth’s deep interior, Rep. Prog. Phys., 2005, 68, 1811–1859

    Article  CAS  Google Scholar 

  7. Gauzzi A., Gilioli E., Licci F., Prodi A., Bolzoni F., Marezio M., et al., Pressure effects on structural and electronic properties of superconductors, In: Katrusiak A., McMillan P.F., (Eds.), High-Pressure Crystallography, Kluwer Academic Publishers, Dordrecht, 2004, 429–446

    Google Scholar 

  8. Edvards P.P., Hensel F., Will solid hydrogen ever be a maetal?, Nature (London), 1997, 388, 621–622

    Article  CAS  Google Scholar 

  9. Huppertz H., Multianvil high-pressure/high-temperature synthesis in solid state chemistry, Z. Kristallogr., 2004, 219, 330–338

    Article  CAS  Google Scholar 

  10. Kim E., Pang T., Utsumi W., Solozhenko V. L., Zhao Y., Cubic phases of BC2N, Phys. Rev. B, 2007, 75, 184115 (1–4)

    Article  CAS  Google Scholar 

  11. Gajda R., Katrusiak A., In-situ high-pressure study of the ordered phase of ethyl propionate, Acta Cryst. Sect. B — Structural Science, 2007, 63, 111–117

    Article  CAS  Google Scholar 

  12. Fabbiani F.P.A., Pulham C.R., High-pressure studies of pharmaceutical compounds and energetic materials, Chem. Soc. Rev., 2006, 35, 932–942

    Article  PubMed  CAS  Google Scholar 

  13. Boldyreva E.V., Shakhtshneider T.P., Ahsbahs H., Uchtmann H., Burgina E.B., Baltakhinov V.P., The role of hydrogen bonds in the pressure-induced structural distortion of 4-hydroxyacetanilide crystals, Pol. J. Chem., 2002, 76, 1333–1346

    CAS  Google Scholar 

  14. Kundrot C.E, Richards F.M., Crystal structure of hen egg-white lysozyme at a hydrostatic pressure of 1000 atmospheres, J. Mol. Biol., 1987, 193, 157–170

    Article  PubMed  CAS  Google Scholar 

  15. Fourme R., Girard E., Kahn R., Dhaussy A.-C., Mezouar M., Colloc’h N., et al., High-pressure macromolecular crystallography (HPMX): Status and prospects, BBA-Proteins Proteomics, 2006, 1764, 384–390

    CAS  Google Scholar 

  16. Girard E., Kahn R., Dhaussy A.-C., Ascone I., Mezouar M., Fourme R., In: Choi J.-Y., Rah S., (Eds.), Synchrotron Radiation Instrumentation: Ninth International Conference on Synchrotron Radiation Instrumentation, American Institute of Physics Conference Proceedings, 2007, 879, 1883–1886

  17. Fourme R., Ascone I., Kahn R., Mezouar M., Bouvier P., Girard E., et al., Opening the high-pressure domain beyond 2 kbar to protein and virus crystallography-technical advance, Structure, 2002, 10, 1409–1414

    Article  PubMed  CAS  Google Scholar 

  18. Girard E., Kahn R., Mezouar M., Dhaussy A.-C., Lin T., Johnson J.E., et al., The first crystal structure of a macromolecular assembly under high pressure: CpMV at 330 MPa, Biophys. J., 2005, 88, 3562–3571

    Article  PubMed  CAS  Google Scholar 

  19. Akasaka K., Probing Conformational Fluctuation of Proteins by Pressure Perturbation, Chem. Rev., 2006, 106, 1814–1835

    Article  PubMed  CAS  Google Scholar 

  20. Heremans K., Smeller L., Protein structure and dynamics at high pressure, BBA-Protein Structure and Molecular Enzymology, 1998, 1368, 353–370

    Article  Google Scholar 

  21. Balny C., Pressure effects on weak interactions in biological systems, J. Phys.-Condens. Matter, 2004, 16, 1245–1253

    Article  CAS  Google Scholar 

  22. Kornblatt M.J., Lange R., Balny C., Can monomers of yeast enolase have enzymatic activity?, Eur. J. Biochem., 1998, 251, 775–780

    Article  PubMed  CAS  Google Scholar 

  23. Athes V., Combes D., Zwick A., Raman spectroscopic studies of native and pressure-or temperature-denaturated invertase, J. Raman Spectrosc., 1998, 29, 373–378

    Article  CAS  Google Scholar 

  24. Tanaka N., Mitani D., Kunugi S., Pressureinduced perturbation on the active site of β-amylase monitored from the sulfhydryl reaction, Biochemistry, 2001, 40, 5914–5920

    Article  PubMed  CAS  Google Scholar 

  25. Suarez M.C., Lehrer S.S., Silva J.L., Local heterogeneity in the pressure denaturation of the coiled-coil tropomyosin because of subdomain folding units, Biochemistry, 2001, 40, 1300–1307

    Article  PubMed  CAS  Google Scholar 

  26. Lullien-Pellerin V., Balny C., High-pressure as a tool to study some proteins’ properties: conformational modification, activity and oligomeric dissociation, Innov. Food Sci. Emerg. Technol., 2002, 3, 209–221

    Article  CAS  Google Scholar 

  27. Northrop D.B., Effects of high pressure on enzymatic activity, BBA-Protein Structure and Molecular Enzymology, 2002, 159, 71–79

    Article  Google Scholar 

  28. Cléry C., Heiber-Langer I., Channac L., David L., Balny C., Masson P., Substrate dependence of amiloride- and soman-induced conformation changes of butyrylcholinesterase as evidenced by high-pressure perturbation, BBA-Protein Structure and Molecular Enzymology, 1995, 1250, 19–28

    Article  PubMed  Google Scholar 

  29. Lange R., Bec N., Anzenbacher P., Munro A.W., Gorren A.C.F., Mayer B., Use of high pressure to study elementary steps in P450 and nitric oxide synthase, J. Inorg. Biochem., 2001, 87, 191–195

    Article  PubMed  CAS  Google Scholar 

  30. Kunugi S., Kitayaki M., Yanagi Y., Tanaka N., Lange R., Balny C., The effect of high pressure on thermolysin, Eur. J. Biochem., 1997, 248, 567–574

    Article  PubMed  CAS  Google Scholar 

  31. Rariy R.V., Bec N., Saldana J.L., Nametkin S.N., Mozhaev V.V., Klyachko N.L., et al., High-pressure stabilization of α-chymotrypsyn entrapped in reversed micelles of aerosol OT in octane against thermal inactivation, FEBS Lett., 1995, 364, 98–100

    Article  PubMed  CAS  Google Scholar 

  32. Dahlhoff E., Somero G.N., Pressure and temperature adaptation of cytosolic malate dehydrogenases of shallow- and deep-living marine invertebrates: Evidence for high body temperatures in hydrothermal vent animals, J. Exp. Biol., 1991, 159, 473–487

    CAS  Google Scholar 

  33. Dumoulin M., Ueno H., Hayashi R., Balny C., Contribution of the carbohydrate moiety to conformational stability of carboxypeptidase Y., High pressure study, Eur. J. Biochem., 1999, 262, 475–483

    Article  PubMed  CAS  Google Scholar 

  34. Kornblatt J.A., Kornblatt M.J., Hui Bon Hoa G., Mauk A.G., Responses of two protein-protein complexes to solvent stress: does water play a role at the interface?, Biophys. J., 1993, 65, 1059–1065

    Article  PubMed  CAS  Google Scholar 

  35. Aertsen A., Meersman F., Hendrickx M.E.G., Vogel R.F., Michiels C., Biotechnology under high pressure: applications and implications, Trends Biotechnol., 2009, 27, 434–441

    Article  PubMed  CAS  Google Scholar 

  36. Hayashi R., High pressure in bioscience and biotechnology: pure science encompassed in pursuit of value, BBA-Protein Structure and Molecular Enzymology, 2002, 1595, 397–399

    Article  PubMed  CAS  Google Scholar 

  37. Olsen K., Ipsen R., Otte J., Skibsted L.H., Effect of high pressure on aggregation and thermal gelation of β-lactoglobulin, Milchwissenschaft, 1999, 54, 543–546

    CAS  Google Scholar 

  38. Spinozzi F., Mariani P., Saturni L., Carsughi F., Bernstroff S., Cinelli S., et al., Met-myoglobin association in dilute solution during pressureinduced denaturation: an analysis at pH 4.5 by high-pressure small-angle X-ray scattering, J. Phys. Chem., 2007, 111, 3822–3830

    CAS  Google Scholar 

  39. Dzwolak W., Pressure tuning of insulin aggregation pathways, High Pressure Res., 2004, 24, 511–516

    Article  CAS  Google Scholar 

  40. Gu Z., Zhu X., Ni S., Su Z., Zhou H.-M., Conformational changes of lysozyme refolding intermediates and implications for aggregation and renaturation, Int. J. Biochem. Cell Biol., 2004, 36, 795–805

    Article  PubMed  CAS  Google Scholar 

  41. Torrent J., Alvarez-Martinez M.T., Heitz F., Liautard J.P., Balny C., Lange R., Alternative prion structural changes revealed by high pressure, Biochemistry, 2003, 42, 1318–1325

    Article  PubMed  CAS  Google Scholar 

  42. Ferrao-Gonzales A.D., Souto S.O., Silva, J.L., Foguel D., The preaggregated state of an amyloidogenic protein: Hydrostatic pressure converts native transthyretin into the amyloidogenic state, Proc. Natl. Acad. Sci. USA, 2000, 97, 6445–6450

    Article  PubMed  CAS  Google Scholar 

  43. Foguel D., Suarez M.C., Ferrao-Gonzales A.D, Porto T.C.R., Palmieri L., Einsiedler C.M., et al., Dissociation of amyloid fibrils of {alpha}-synuclein and transthyretin by pressure reveals their reversible nature and the formation of water-excluded cavities, Proc. Natl. Acad. Sci. USA, 2003, 100, 9831–9836

    Article  PubMed  CAS  Google Scholar 

  44. Marchal S., Shehi E., Harricane M.-C., Fusi P., Heitz F., Tortora P., et al., Structural instability and fibrillar aggregation of non-expanded human ataxin-3 revealed under high pressure and temperature, J. Biol. Chem., 2003, 278, 31554–31563

    Article  PubMed  CAS  Google Scholar 

  45. Foguel D., Silva J.L., New insights into the mechanisms of protein misfolding and aggregation in amyloidogenic diseases derived from pressure studies, Biochemistry, 2004, 43, 11361–11370

    Article  PubMed  CAS  Google Scholar 

  46. Torrent J., Balny C., Lange R., High pressure modulates amyloid formation, Protein Pept. Lett., 2006, 13, 271–277

    Article  PubMed  CAS  Google Scholar 

  47. Baker E., Solvent interactions with proteins as revealed by X-ray crystallographic studies In: Gregory R.B., (Ed.), Protein-solvent interactions, Marcel Dekker, New York, 1995, 143–185

    Google Scholar 

  48. Katrusiak A., Dauter Z., Compressibility of lysozyme protein crystals by X-ray diffraction, Acta Crystallogr. Sect. D-Biol. Crystallogr., 1996, 52, 607–608

    Article  CAS  Google Scholar 

  49. Suzuki Y., Sazaki G., Miyashita S., Sawada T., Tamura K., Komatsu H., Protein crystallization under high pressure, BBA-Protein Structure and Molecular Enzymology, 2002, 1595, 345–356

    Article  PubMed  CAS  Google Scholar 

  50. Kadri A., Lorber B., Charron C., Robert M.C., Capelle B., Damak M., et al., Crystal quality and differential crystal-growth behaviour of three proteins crystallized in gel at high hydrostatic pressure, Acta Crystallogr. Sect. D-Biol. Crystallogr., 2005, 61, 784–788

    Article  CAS  Google Scholar 

  51. Groß M., Jaenicke R., Growth inhibition of lysozyme crystals at high hydrostatic pressure, FEBS Lett., 1991, 284, 87–90

    Article  PubMed  Google Scholar 

  52. Charron C., Robert M.C., Capelle B., Kadri A., Jenner G., Giege R., et al., X-ray diffraction properties of protein crystals prepared in agarose gel under hydrostatic pressure, J. Cryst. Growth, 2002, 245, 321–333

    Article  CAS  Google Scholar 

  53. Sazaki G., Nagatoshi Y., Suzuki Y., Durbin S.D., Miyashita S., Nakada T., et al., Solubility of tetragonal and orthorhombic lysozyme crystals under high pressure, J. Cryst. Growth, 1999, 196, 204–209

    Article  CAS  Google Scholar 

  54. Waghmare R.Y., Pan X.J., Glatz C.E., Pressure and concentration dependence of nucleation kinetics for crystallization of subtilisin, J. Cryst. Growth, 2000, 210, 746–757

    Article  CAS  Google Scholar 

  55. Suzuki Y., Sazaki, Sawada T., Miyashita S., Komatsu H., Tamura K., Protein crystallization under high hydrostatic pressure, Nucl. Instr. Meth. Phys. Res. B, 2003, 13, 149–157

    CAS  Google Scholar 

  56. Weir C.E., Lippincott E.R., Van Valkenburg A., Bunting E.N., Infrared studies in the 1- to 15-micron region to 30,000 atmospheres, J. Natl. Bur. Stand., Sec. A, 1959, 63, 55–62

    Google Scholar 

  57. Ferraro J.R., Van Valkenburg E., Origins of the diamond anvil cell: The versatile sampling accessory marks its 40th year, Spectroscopy, 1999, 14, 19–23

    Google Scholar 

  58. Merrill L., Bassett W.A., Miniature diamond anvil pressure cell for single crystal X-ray diffraction studies, Rev. Sci. Instrum., 1974, 45, 290–294

    Article  Google Scholar 

  59. Keller R., Holzapfel W.B., Diamond anvil device for x-ray diffraction on single crystals under pressures up to 100 kilobar, Rev. Sci. Instrum., 1977, 48, 517–523

    Article  CAS  Google Scholar 

  60. Le Toullec R., Pinceaux J.-P., Loubeyre P., The membrane diamond anvil cell: A new device for generating continuous pressure and temperature variations, High Press. Res., 1988, 1, 77–90

    Article  Google Scholar 

  61. Chervin J.C., Canny B., Besson J.M., Pruzan Ph., A diamond anvil cell for IR microspectroscopy, Rev. Sci. Instrum., 1995, 66, 2595–2598

    Article  CAS  Google Scholar 

  62. Piermarini G.J., High pressure X-ray crystallography with the diamond cell at NIST/NBS, J. Res. Natl. Inst. Stand. Technol., 2001, 106, 889–920

    CAS  Google Scholar 

  63. Girard E., Dhaussy A.-C., Couzinet B., Chervin J.C., Mezouar M., Kahn R., et al., Toward fully fledged high-pressure macromolecular crystallography, J. Appl. Crystallogr., 2007, 40, 912–918

    Article  CAS  Google Scholar 

  64. Urayama P., Phipils G.N., Gruner S.M. Probing substates in sperm whale myoglobin using highpressure crystallography, Structure, 2002, 10, 51–60

    Article  PubMed  CAS  Google Scholar 

  65. Ekstrom J.L., Ealick S.E., Osterberg F.H.O., Gruner S., Effect of pressure on protein dynamics: a crystallographic study, Am. Cryst. Assoc. Meet., 1995, Abstract A319, Montreal, Canada

  66. Collins M.D., Hummer G., Quillin M.L., Matthews B.W., Gruner S.M., Cooperative water filling of a nonpolar protein cavity observed by high-pressure crystallography and simulation, Proc. Natl. Acad. Sci. USA, 2004, 102, 16668–16671

    Article  CAS  Google Scholar 

  67. Ando N., Barstow A.N., Baase W.A., Fields A., Matthews B.W., Gruner S.M., Structural and thermodynamic characterization of T4 lysozyme mutants and the contribution of internal cavities to pressure denaturation, Biochemistry, 2008, 47, 11097–11109

    Article  PubMed  CAS  Google Scholar 

  68. Fourme R., Kahn R., Mezouar M., Girard E., Hoerentrup C., Prange T., et al., High-pressure protein crystallography (HPPX): instrumentation, methodology and results on lysozyme crystals, J. Synchrotron Rad., 2001, 8, 1149–1156

    Article  CAS  Google Scholar 

  69. Fourme R., Girard E., Kahn R., Dhaussy A.C., Ascone I., Advances in high-pressure biophysics: status and prospects of macromolecular crystallography, Ann. Rev. Biophys., 2009, 38, 153–171

    Article  CAS  Google Scholar 

  70. Girard E., Kahn R., Mezouar M., Dhaussy A.-C., Lin T., Johnson J.E., et al., The first crystal structure of a macromolecular assembly under high pressure: CpMV at 330 MPa, Biophys. J., 2005, 88, 3562–3571

    Article  PubMed  CAS  Google Scholar 

  71. Colloc’h N., Girard E., Dhaussy A.-C., Kahn R., Ascone I., Mezouar M., et al., High pressure macromolecular crystallography: The 140-MPa crystal structure at 2.3 angstrom resolution of urate oxidase, a 135-kDa tetrameric assembly, BBAProteins Proteomics, 2006, 1764, 391–397

    Google Scholar 

  72. Girard E., Prange T., Dhaussy A.-C., Migianu-Griffoni E., Lecouvey M., Chervin J.C., et al., Adaptation of the base-paired double-helix molecular architecture to extreme pressure, Nucl. Acids Res., 2007, 35, 4800–4808

    Article  PubMed  CAS  Google Scholar 

  73. Kim C.U., Hao Q., Gruner S.M., Solution of protein crystallographic structures by high-pressure cryocooling and noble-gas phasing, Acta Crystallogr. Sect. D-Biol. Crystallogr., 2006, 62, 687–694

    Article  CAS  Google Scholar 

  74. Kim C.U., Kapfer R., Gruner S.M., High-pressure cooling of protein crystals without cryoprotectants, Acta Crystallogr. Sect. D-Biol. Crystallogr., 2005, 61, 881–890

    Article  CAS  Google Scholar 

  75. Kim C.U., Chen Y.F., Tate M.W., Gruner S.M., Pressure induced high-density amorphous ice in protein crystals, J. Appl. Crystallogr., 2008, 41, 1–7

    Article  CAS  Google Scholar 

  76. Barstow B., Ando N., Kim C.U., Gruner S.M., Alternation of citrine structure by hydrostatic pressure explains the accompanying spectral shift, Proc. Natl. Acad. Sci. USA, 2008, 105, 13362–13366

    Article  PubMed  Google Scholar 

  77. Colloc’h N., Sopkova-de Oliveira Santos J., Retailleau P., Lanlois d’Estainto B., Gallois B., Brisson A., et al., Protein crystallography under xenon and nitrous oxide pressure: Comparison with in vivo pharmacology studies and implications for the mechanism of inhaled anesthetic action, Biophys. J., 2007, 92, 217–224

    Article  PubMed  CAS  Google Scholar 

  78. Prange T., Schiltz M., Pernot L., Colloc’h N., Longhi S., Bourguet W., et al., Exploring hydrophobic sites in proteins with Xenon or Krypton, Proteins, 1998, 30, 61–73

    Article  PubMed  CAS  Google Scholar 

  79. Nienhaus K., Maes E.M., Weichsel A., Montfort W.R., Nienhaus G.U., Structural dynamics controls nitric oxide affinity in Nitrophorin 4, J. Biol. Chem., 2004, 279, 39401–39407

    Article  PubMed  CAS  Google Scholar 

  80. Schlitz M., Shepard W., Fourme R., Prange T., de la Fortelle E., Bricogne G., High-pressure krypton gas and statistical heavy-atom refinement: a successful combination of tools for macromolecular structure determination, Acta Crystallogr. Sect. D-Biol. Crystallogr., 1997, 53, 78–92

    Article  Google Scholar 

  81. Fourme R., Ascone I., Kahn R., Girard E., Mezouar M., Lin T., et al., New trends in macromolecular crystallography at high hydrostatic pressure In: Winter R., (Ed.), Advances in High Pressure Bioscience and Biotechnology II, Springer-Verlag, Berlin, 2002, 161–70

    Google Scholar 

  82. Kim C.U., Hao Q., Gruner S.M., High-pressure cryocooling for capillary sample cryoprotection and diffraction phasing at long wavelengths, Acta Crystallogr. Sect. D-Biol. Crystallogr., 2007, 63, 653–659

    Article  CAS  Google Scholar 

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  1. Protein Crystallography Group, Department of Crystal Physics and Crystal Chemistry, Faculty of Chemistry, Jagiellonian University, 30-060, Kraków, Poland

    Katarzyna Kurpiewska & Krzysztof Lewiński

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  1. Katarzyna Kurpiewska
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  2. Krzysztof Lewiński
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Correspondence to Katarzyna Kurpiewska.

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Kurpiewska, K., Lewiński, K. High pressure macromolecular crystallography for structural biology: a review. cent.eur.j.biol. 5, 531–542 (2010). https://doi.org/10.2478/s11535-010-0044-y

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