High Pressures and Eukaryotes

  • Fumiyoshi AbeEmail author
Reference work entry

General Effects of High Hydrostatic Pressures in Biological Systems

The effects of high hydrostatic pressure in biological systems have been mainly investigated from the following perspectives: (1) structural perturbation of macromolecules such as proteins and lipids, and kinetic analysis of biochemical reactions; (2) microbial adaptation to high pressure in mesophiles and piezophiles; and (3) inactivation of food-spoiling microbes, and applications in nonthermal food processing. During the past decades, an increasing number of innovative high-pressure studies on biological processes have been performed by applying advanced techniques of genetics and molecular biology in bacteria and yeasts as model organisms (Horikoshi 1998; Abe et al. 1999; Abe and Horikoshi 2001; Bartlett 2002; Abe 2004, 2007a; Aertsen et al. 2009). Recent studies in this field have revealed the potential of a broad range of microbes to adapt and develop resistance to increasing hydrostatic pressure and have shown...


Hydrostatic Pressure High Hydrostatic Pressure Neutral Trehalase Tryptophan Uptake Tryptophan Availability 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Abe F, Horikoshi K (1995) Hydrostatic pressure promotes the acidification of vacuoles in Saccharomyces cerevisiae. FEMS Microbiol Lett 130:307–312PubMedCrossRefGoogle Scholar
  2. Abe F, Horikoshi K (1997) Vacuolar acidification in Saccharomyces cerevisiae induced by elevated hydrostatic pressure is transient and is mediated by vacuolar H+-ATPase. Extremophiles 1:89–93PubMedCrossRefGoogle Scholar
  3. Abe F (1998) Hydrostatic pressure enhances vital staining with carboxyfluorescein or carboxydichlorofluorescein in Saccharomyces cerevisiae: efficient detection of labeled yeasts by flow cytometry. Appl Environ Microbiol 64:1139–1142PubMedGoogle Scholar
  4. Abe F, Horikoshi K (1998) Analysis of intracellular pH in the yeast Saccharomyces cerevisiae under elevated hydrostatic pressure: a study in baro- (piezo-) physiology. Extremophiles 2:223–228PubMedCrossRefGoogle Scholar
  5. Abe F, Kato C, Horikoshi K (1999) Pressure-regulated metabolism in microorganisms. Trends Microbiol 7:447–453PubMedCrossRefGoogle Scholar
  6. Abe F, Horikoshi K (2000) Tryptophan permease gene TAT2 confers high-pressure growth in Saccharomyces cerevisiae. Mol Cell Biol 20:8093–8102PubMedCrossRefGoogle Scholar
  7. Abe F, Horikoshi K (2001) The biotechnological potential of piezophiles. Trends Biotechnol 19:102–108PubMedCrossRefGoogle Scholar
  8. Abe F, Iida H (2003) Pressure-induced differential regulation of the two tryptophan permeases Tat1 and Tat2 by ubiquitin ligase Rsp5 and its binding proteins, Bul1 and Bul2. Mol Cell Biol 23:7566–7584PubMedCrossRefGoogle Scholar
  9. Abe F (2004) Piezophysiology of yeast –Occurrence and significance. Cell Mol Biol 50:437–445PubMedGoogle Scholar
  10. Abe F (2007a) Exploration of the effects of high hydrostatic pressure on microbial growth, physiology and survival: perspectives from piezophysiology. Biosci Biotechnol Biochem 71:2347–2357PubMedCrossRefGoogle Scholar
  11. Abe F (2007b) Induction of DAN/TIR yeast cell wall mannoprotein genes in response to high hydrostatic pressure and low temperature. FEBS Lett 581:4993–4998PubMedCrossRefGoogle Scholar
  12. Abe F, Minegishi H (2008) Global screening of genes essential for growth in high-pressure and cold environments: searching for basic adaptive strategies using a yeast deletion library. Genetics 178:851–872PubMedCrossRefGoogle Scholar
  13. Abramova N, Sertil O, Mehta S, Lowry CV (2001a) Reciprocal regulation of anaerobic and aerobic cell wall mannoprotein gene expression in Saccharomyces cerevisiae. J Bacteriol 183:2881–2887PubMedCrossRefGoogle Scholar
  14. Abramova NE, Cohen BD, Sertil O, Kapoor R, Davies KJ, Lowry CV (2001b) Regulatory mechanisms controlling expression of the DAN/TIR mannoprotein genes during anaerobic remodeling of the cell wall in Saccharomyces cerevisiae. Genetics 157:1169–1177PubMedGoogle Scholar
  15. Aertsen A, Meersman F, Hendrickx ME, Vogel RF, Michiels CW (2009) Biotechnology under high pressure: applications and implications. Trends Biotechnol 27:434–441PubMedCrossRefGoogle Scholar
  16. Albert TK, Hanzawa H, Legtenberg YI, de Ruwe MJ, van den Heuvel FA, Collart MA, Boelens R, Timmers HT (2002) Identification of a ubiquitin-protein ligase subunit within the CCR4-NOT transcription repressor complex. EMBO J 21:355–364PubMedCrossRefGoogle Scholar
  17. Balny C, Masson P, Heremans K (2002) High pressure effects on biological macromolecules: from structural changes to alteration of cellular processes. Biochim Biophys Acta 1595:3–10PubMedCrossRefGoogle Scholar
  18. Bartlett DH (2002) Pressure effects on in vivo microbial processes. Biochim Biophys Acta 1595:367–381PubMedCrossRefGoogle Scholar
  19. Baudin A, Ozier-Kalogeropoulos O, Denouel A, Lacroute F, Cullin C (1993) A simple and efficient method for direct gene deletion in Saccharomyces cerevisiae. Nucleic Acids Res 21:3329–3330PubMedCrossRefGoogle Scholar
  20. Beck T, Schmidt A, Hall MN (1999) Starvation induces vacuolar targeting and degradation of the tryptophan permease in yeast. J Cell Biol 146:1227–1238PubMedCrossRefGoogle Scholar
  21. Chen CY, Ingram MF, Rosal PH, Graham TR (1999) Role for Drs2p, a P-type ATPase and potential aminophospholipid translocase, in yeast late Golgi function. J Cell Biol 147:1223–1236PubMedCrossRefGoogle Scholar
  22. Collart MA (2003) Global control of gene expression in yeast by the Ccr4-Not complex. Gene 313:1–16PubMedCrossRefGoogle Scholar
  23. de Smedt H, Borghgraef R, Ceuterick F, Heremans K (1979) Pressure effects on lipid-protein interactions in (Na+ + K+)-ATPase. Biochim Biophys Acta 556:479–489PubMedCrossRefGoogle Scholar
  24. Diehl P, Schmitt M, Blumelhuber G, Frey B, Van Laak S, Fischer S, Muehlenweg B, Meyer-Pittroff R, Gollwitzer H, Mittelmeier W (2003) Induction of tumor cell death by high hydrostatic pressure as a novel supporting technique in orthopedic surgery. Oncol Rep 10:1851–1855PubMedGoogle Scholar
  25. Diehl P, Schmitt M, Schauwecker J, Eichelberg K, Gollwitzer H, Gradinger R, Goebel M, Preissner KT, Mittelmeier W, Magdolen U (2005) Effect of high hydrostatic pressure on biological properties of extracellular bone matrix proteins. Int J Mol Med 16:285–289PubMedGoogle Scholar
  26. Domitrovic T, Fernandes CM, Boy-Marcotte E, Kurtenbach E (2006) High hydrostatic pressure activates gene expression through Msn2/4 stress transcription factors which are involved in the acquired tolerance by mild pressure precondition in Saccharomyces cerevisiae. FEBS Lett 580:6033–6038PubMedCrossRefGoogle Scholar
  27. Dubouloz F, Deloche O, Wanke V, Cameroni E, De Virgilio C (2005) The TOR and EGO protein complexes orchestrate microautophagy in yeast. Mol Cell 19:15–26PubMedCrossRefGoogle Scholar
  28. Fernandes PM, Domitrovic T, Kao CM, Kurtenbach E (2004) Genomic expression pattern in Saccharomyces cerevisiae cells in response to high hydrostatic pressure. FEBS Lett 556:153–160PubMedCrossRefGoogle Scholar
  29. Frey B, Franz S, Sheriff A, Korn A, Bluemelhuber G, Gaipl US, Voll RE, Meyer-Pittroff R, Herrmann M (2004) Hydrostatic pressure induced death of mammalian cells engages pathways related to apoptosis or necrosis. Cell Mol Biol 50:459–467 (Noisy-le-grand)PubMedGoogle Scholar
  30. Frey B, Janko C, Ebel N, Meister S, Schlucker E, Meyer-Pittroff R, Fietkau R, Herrmann M, Gaipl US (2008) Cells under pressure - treatment of eukaryotic cells with high hydrostatic pressure, from physiologic aspects to pressure induced cell death. Curr Med Chem 15:2329–2336PubMedCrossRefGoogle Scholar
  31. Gekko K (2002) Compressibility gives new insight into protein dynamics and enzyme function. Biochim Biophys Acta 1595:382–386PubMedCrossRefGoogle Scholar
  32. Giaever G, Chu AM, Ni L, Connelly C, Riles L, Veronneau S, Dow S, Lucau-Danila A, Anderson K, Andre B, Arkin AP, Astromoff A, El-Bakkoury M, Bangham R, Benito R, Brachat S, Campanaro S, Curtiss M, Davis K, Deutschbauer A, Entian KD, Flaherty P, Foury F, Garfinkel DJ, Gerstein M, Gotte D, Guldener U, Hegemann JH, Hempel S, Herman Z, Jaramillo DF, Kelly DE, Kelly SL, Kotter P, LaBonte D, Lamb DC, Lan N, Liang H, Liao H, Liu L, Luo C, Lussier M, Mao R, Menard P, Ooi SL, Revuelta JL, Roberts CJ, Rose M, Ross-Macdonald P, Scherens B, Schimmack G, Shafer B, Shoemaker DD, Sookhai-Mahadeo S, Storms RK, Strathern JN, Valle G, Voet M, Volckaert G, Wang CY, Ward TR, Wilhelmy J, Winzeler EA, Yang Y, Yen G, Youngman E, Yu K, Bussey H, Boeke JD, Snyder M, Philippsen P, Davis RW, Johnston M (2002) Functional profiling of the Saccharomyces cerevisiae genome. Nature 418:387–391PubMedCrossRefGoogle Scholar
  33. Hamada K, Nakatomi Y, Shimada S (1992) Direct induction of tetraploids or homozygous diploids in the industrial yeast Saccharomyces cerevisiae by hydrostatic pressure. Curr Genet 22:371–376PubMedCrossRefGoogle Scholar
  34. Heremans K, Smeller L (1998) Protein structure and dynamics at high pressure. Biochim Biophys Acta 1386:353–370PubMedCrossRefGoogle Scholar
  35. Hicke L (1999) Gettin’ down with ubiquitin: turning off cell-surface receptors, transporters and channels. Trends Cell Biol 9:107–112PubMedCrossRefGoogle Scholar
  36. Hiraki T, Abe F (2010) Overexpression of Sna3 stabilizes tryptophan permease Tat2, potentially competing for the WW domain of Rsp5 ubiquitin ligase with its binding protein Bul1. FEBS Lett 584:55–60PubMedCrossRefGoogle Scholar
  37. Horikoshi K (1998) Barophiles: deep-sea microorganisms adapted to an extreme environment. Curr Opin Microbiol 1:291–295PubMedCrossRefGoogle Scholar
  38. Ishimaru D, Sa-Carvalho D, Silva JL (2004) Pressure-inactivated FMDV: a potential vaccine. Vaccine 22:2334–2339PubMedCrossRefGoogle Scholar
  39. Iwahashi H, Kaul SC, Obuchi K, Komatsu Y (1991) Induction of barotolerance by heat shock treatment in yeast. FEMS Microbiol Lett 64:325–328PubMedCrossRefGoogle Scholar
  40. Iwahashi H, Obuchi K, Fujii S, Komatsu Y (1997) Effect of temperature on the role of Hsp104 and trehalose in barotolerance of Saccharomyces cerevisiae. FEBS Lett 416:1–5PubMedCrossRefGoogle Scholar
  41. Iwahashi H, Nwaka S, Obuchi K (2000) Evidence for contribution of neutral trehalase in barotolerance of Saccharomyces cerevisiae. Appl Environ Microbiol 66:5182–5185PubMedCrossRefGoogle Scholar
  42. Iwahashi H, Nwaka S, Obuchi K (2001) Contribution of Hsc70 to barotolerance in the yeast Saccharomyces cerevisiae. Extremophiles 5:417–421PubMedCrossRefGoogle Scholar
  43. Iwahashi H, Shimizu H, Odani M, Komatsu Y (2003) Piezophysiology of genome wide gene expression levels in the yeast Saccharomyces cerevisiae. Extremophiles 7:291–298PubMedCrossRefGoogle Scholar
  44. Iwahashi H, Odani M, Ishidou E, Kitagawa E (2005) Adaptation of Saccharomyces cerevisiae to high hydrostatic pressure causing growth inhibition. FEBS Lett 579:2847–2852PubMedCrossRefGoogle Scholar
  45. Kakinuma Y, Ohsumi Y, Anraku Y (1981) Properties of H+-translocating adenosine triphosphatase in vacuolar membranes of Saccharomyces cerevisiae. J Biol Chem 256:10859–10863PubMedGoogle Scholar
  46. Katzmann DJ, Babst M, Emr SD (2001) Ubiquitin-dependent sorting into the multivesicular body pathway requires the function of a conserved endosomal protein sorting complex, ESCRT-I. Cell 106:145–155PubMedCrossRefGoogle Scholar
  47. Kawai R, Fujita K, Iwahashi H, Komatsu Y (1999) Direct evidence for the intracellular localization of Hsp104 in Saccharomyces cerevisiae by immunoelectron microscopy. Cell Stress Chaperones 4:46–53PubMedGoogle Scholar
  48. Kishimoto T, Yamamoto T, Tanaka K (2005) Defects in structural integrity of ergosterol and the Cdc50p-Drs2p putative phospholipid translocase cause accumulation of endocytic membranes, onto which actin patches are assembled in yeast. Mol Biol Cell 16:5592–5609PubMedCrossRefGoogle Scholar
  49. Kobori H, Sato M, Tameike A, Hamada K, Shimada S, Osumi M (1995) Ultrastructural effects of pressure stress to the nucleus in Saccharomyces cerevisiae: a study by immunoelectron microscopy using frozen thin sections. FEMS Microbiol Lett 132:253–258PubMedCrossRefGoogle Scholar
  50. Liu HY, Badarinarayana V, Audino DC, Rappsilber J, Mann M, Denis CL (1998) The NOT proteins are part of the CCR4 transcriptional complex and affect gene expression both positively and negatively. EMBO J 17:1096–1106PubMedCrossRefGoogle Scholar
  51. Liu J, Zou L, Wang J, Schuler C, Zhao Z, Li X, Zhang J, Liu Y (2009) Hydrostatic pressure promotes Wnt10b and Wnt4 expression dependent and independent on ERK signaling in early-osteoinduced MSCs. Biochem Biophys Res Commun 379:505–509PubMedCrossRefGoogle Scholar
  52. Lorenz RT, Parks LW (1992) Cloning, sequencing, and disruption of the gene encoding sterol C-14 reductase in Saccharomyces cerevisiae. DNA Cell Biol 11:685–692PubMedCrossRefGoogle Scholar
  53. Maillet L, Tu C, Hong YK, Shuster EO, Collart MA (2000) The essential function of Not1 lies within the Ccr4-Not complex. J Mol Biol 303:131–143PubMedCrossRefGoogle Scholar
  54. Malki A, Caldas T, Abdallah J, Kern R, Eckey V, Kim SJ, Cha SS, Mori H, Richarme G (2005) Peptidase activity of the Escherichia coli Hsp31 chaperone. J Biol Chem 280:14420–14426PubMedCrossRefGoogle Scholar
  55. McNatt MW, McKittrick I, West M, Odorizzi G (2007) Direct binding to Rsp5 mediates ubiquitin-independent sorting of Sna3 via the multivesicular body pathway. Mol Biol Cell 18:697–706PubMedCrossRefGoogle Scholar
  56. Misu K, Fujimura-Kamada K, Ueda T, Nakano A, Katoh H, Tanaka K (2003) Cdc50p, a conserved endosomal membrane protein, controls polarized growth in Saccharomyces cerevisiae. Mol Biol Cell 14:730–747PubMedCrossRefGoogle Scholar
  57. Miura T, Abe F (2004) Multiple ubiquitin-specific protease genes are involved in degradation of yeast tryptophan permease Tat2 at high pressure. FEMS Microbiol Lett 239:171–179PubMedCrossRefGoogle Scholar
  58. Miura T, Minegishi H, Usami R, Abe F (2006) Systematic analysis of HSP gene expression and effects on cell growth and survival at high hydrostatic pressure in Saccharomyces cerevisiae. Extremophiles 10:279–284PubMedCrossRefGoogle Scholar
  59. Nagayama A, Kato C, Abe F (2004) The N- and C-terminal mutations in tryptophan permease Tat2 confer cell growth in Saccharomyces cerevisiae under high-pressure and low-temperature conditions. Extremophiles 8:143–149PubMedCrossRefGoogle Scholar
  60. Natarajan P, Wang J, Hua Z, Graham TR (2004) Drs2p-coupled aminophospholipid translocase activity in yeast Golgi membranes and relationship to in vivo function. Proc Natl Acad Sci USA 101:10614–10619PubMedCrossRefGoogle Scholar
  61. Otake T, Kawahata T, Mori H, Kojima Y, Hayakawa K (2005) Novel method of inactivation of human immunodeficiency virus type 1 by the freeze pressure generation method. Appl Microbiol Biotechnol 67:746–751PubMedCrossRefGoogle Scholar
  62. Palhano FL, Orlando MT, Fernandes PM (2004) Induction of baroresistance by hydrogen peroxide, ethanol and cold-shock in Saccharomyces cerevisiae. FEMS Microbiol Lett 233:139–145PubMedCrossRefGoogle Scholar
  63. Parks LW, Smith SJ, Crowley JH (1995) Biochemical and physiological effects of sterol alterations in yeast -a review. Lipids 30:227–230PubMedCrossRefGoogle Scholar
  64. Perrier-Cornet JM, Marechal PA, Gervais P (1995) A new design intended to relate high pressure treatment to yeast cell mass transfer. J Biotechnol 41:49–58PubMedCrossRefGoogle Scholar
  65. Perrier-Cornet JM, Hayert M, Gervais P (1999) Yeast cell mortality related to a high-pressure shift: occurrence of cell membrane permeabilization. J Appl Microbiol 87:1–7PubMedCrossRefGoogle Scholar
  66. Reggiori F, Pelham HR (2001) Sorting of proteins into multivesicular bodies: ubiquitin-dependent and -independent targeting. EMBO J 20:5176–5186PubMedCrossRefGoogle Scholar
  67. Rosin MP, Zimmerman AM (1977) The induction of cytoplasmic petite mutants of Saccharomyces cerevisiae by hydrostatic pressure. J Cell Sci 26:373–385PubMedGoogle Scholar
  68. Royer CA (2002) Revisiting volume changes in pressure-induced protein unfolding. Biochim Biophys Acta 1595:201–209PubMedCrossRefGoogle Scholar
  69. Saito K, Fujimura-Kamada K, Furuta N, Kato U, Umeda M, Tanaka K (2004) Cdc50p, a protein required for polarized growth, associates with the Drs2p P-type ATPase implicated in phospholipid translocation in Saccharomyces cerevisiae. Mol Biol Cell 15:3418–3432PubMedCrossRefGoogle Scholar
  70. Sasaki S, Funamoto S, Hashimoto Y, Kimura T, Honda T, Hattori S, Kobayashi H, Kishida A, Mochizuki M (2009) In vivo evaluation of a novel scaffold for artificial corneas prepared by using ultrahigh hydrostatic pressure to decellularize porcine corneas. Mol Vis 15:2022–2028PubMedGoogle Scholar
  71. Sato M, Kobori H, Ishijima SA, Feng ZH, Hamada K, Shimada S, Osumi M (1996) Schizosaccharomyces pombe is more sensitive to pressure stress than Saccharomyces cerevisiae. Cell Struct Funct 21:167–174PubMedCrossRefGoogle Scholar
  72. Sato M, Hasegawa K, Shimada S, Osumi M (1999) Effects of pressure stress on the fission yeast Schizosaccharomyces pombe cold-sensitive mutant nda3. FEMS Microbiol Lett 176:31–38PubMedCrossRefGoogle Scholar
  73. Serrano R (1993) Structure, function and regulation of plasma membrane H(+)-ATPase. FEBS Lett 325:108–111PubMedCrossRefGoogle Scholar
  74. Shimada S, Andou M, Naito N, Yamada N, Osumi M, Hayashi R (1993) Effects of hydrostatic pressure on the ultrastructure and leakage of internal substances in the yeast Saccharomyces cerevisiae. Appl Microbiol Biotechnol 40:123–131CrossRefGoogle Scholar
  75. Simons K, Ikonen E (1997) Functional rafts in cell membranes. Nature 387:569–572PubMedCrossRefGoogle Scholar
  76. Singer MA, Lindquist S (1998) Thermotolerance in Saccharomyces cerevisiae: the Yin and Yang of trehalose. Trends Biotechnol 16:460–468PubMedCrossRefGoogle Scholar
  77. Stawiecka-Mirota M, Pokrzywa W, Morvan J, Zoladek T, Haguenauer-Tsapis R, Urban-Grimal D, Morsomme P (2007) Targeting of Sna3p to the endosomal pathway depends on its interaction with Rsp5p and multivesicular body sorting on its ubiquitylation. Traffic 8:1280–1296PubMedCrossRefGoogle Scholar
  78. Tucker M, Valencia-Sanchez MA, Staples RR, Chen J, Denis CL, Parker R (2001) The transcription factor associated Ccr4 and Caf1 proteins are components of the major cytoplasmic mRNA deadenylase in Saccharomyces cerevisiae. Cell 104:377–386PubMedCrossRefGoogle Scholar
  79. Wach A, Brachat A, Pohlmann R, Philippsen P (1994) New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae. Yeast 10:1793–1808PubMedCrossRefGoogle Scholar
  80. Winter R, Dzwolak W (2004) Temperature-pressure configurational landscape of lipid bilayers and proteins. Cell Mol Biol 50:397–417 (Noisy-le-grand)PubMedGoogle Scholar
  81. Yashiroda H, Oguchi T, Yasuda Y, Toh-E A, Kikuchi Y (1996) Bul1, a new protein that binds to the Rsp5 ubiquitin ligase in Saccharomyces cerevisiae. Mol Cell Biol 16:3255–3263PubMedGoogle Scholar

Copyright information

© Springer 2011

Authors and Affiliations

  1. 1.Molecular Evolution and Adaptation Research, Institute of BiogeosciencesJapan Agency for Marine-Earth Science and Technology (JAMSTEC)YokosukaJapan
  2. 2.Aoyama Gakuin UniversitySagamiharaJapan

Personalised recommendations