Skip to content
1887

Microbiology Society logo Microbiology

Volume 153, Issue 5

Transduction of centrifugation-induced gravity forces through mitogen-activated protein kinase pathways in the fission yeast Free

Abstract

Centrifugation of cells of in liquid medium prompted a marked activation of Sty1 and Pmk1, which are the effector mitogen-activated protein kinases (MAPKs) of the stress-activated protein kinase pathway and the cell-integrity pathway, respectively. Transduction of the centrifugation signals showed a sensitivity threshold above which the response was dependent on time and temperature. Centrifugation-induced phosphorylation of Sty1 and Pmk1 required the presence of the main functional components of the respective signalling cascades, i.e. Wak1 or Win1 plus Wis1, and Mkh1 plus Pek1. The transcription factor Atf1 also became phosphorylated in a Sty1-dependent way upon centrifugation. Hypergravity was an important factor in the activation of Sty1 induced by centrifugation, whilst activation of Pmk1 was mostly due to gravity-associated shear forces. Centrifugation did not increase cell survival against other stresses. Rather, the increased gravitational forces produced a delay in the cell cycle, probably related to alterations in the actin-polarization pattern. Phosphorylation of the MAPK Sty1 was needed for the depolarization of actin patches induced by the centrifugation stress.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
Keyword(s): Ha6H, epitope comprising haemagglutinin antigen plus six histidine residues , MAPK, mitogen-activated protein kinase , MAPKK, mitogen-activated protein kinase kinase , MAPKKK, mitogen-activated protein kinase kinase kinase , SAPK, stress-activated protein kinase and YES, yeast extract plus supplements
SGM
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.2006/004283-0
2007-05-01
2025-04-30
Loading full text...

Full text loading...

/deliver/fulltext/micro/153/5/1519.html?itemId=/content/journal/micro/10.1099/mic.0.2006/004283-0&mimeType=html&fmt=ahah

References

  1. Alfa C., Fantes P., Hyams J., McLeod M., Warbrick E. 1993 Experiments with Fission Yeast: a Laboratory Course Manual Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
     [Google Scholar]
  2. Arnold W. N. 1972; The structure of the yeast cell wall: solubilization of a marker enzyme, β -fructofuranosidase, by the autolytic enzyme system. J Biol Chem 247:1161–1169
     [Google Scholar]
  3. Attfield P. V. 1997; Stress tolerance: the key to effective strains of industrial baker's yeast. Nat Biotechnol 15:1351–1357 [CrossRef]
     [Google Scholar]
  4. Buck V., Quinn J., Soto Pino T., Martin H., Saldanha J., Makino K., Morgan B. A., Millar J. B. A. 2001; Peroxide sensors for the fission yeast stress-activated mitogen-activated protein kinase pathway. Mol Biol Cell 12:407–419 [CrossRef]
     [Google Scholar]
  5. Daga R. R., Chang F. 2005; Dynamic positioning of the fission yeast cell division plane. Proc Natl Acad Sci U S A 102:8228–8232 [CrossRef]
     [Google Scholar]
  6. Degols G., Shiozaki K., Russell P. 1996; Activation and regulation of the Spc1 stress-activated protein kinase in Schizosaccharomyces pombe. Mol Cell Biol 16:2870–2877
     [Google Scholar]
  7. Goldermann M., Hanke W. 2001; Ion channel are sensitive to gravity changes. Microgravity Sci Technol 13:35–38 [CrossRef]
     [Google Scholar]
  8. Ingber D. E. 2006; Cellular mechanotransduction: putting all the pieces together again. FASEB J 20:811–827 [CrossRef]
     [Google Scholar]
  9. Johanson K., Allen P. L., Lewis F., Cubano L. A., Hyman L. E., Hammond T. G. 2002; Saccharomyces cerevisiae gene expression changes during rotating wall vessel suspension culture. J Appl Physiol 93:2171–2180 [CrossRef]
     [Google Scholar]
  10. Kyriakis J. M., Avruch J. 2001; Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol Rev 81:807–869
     [Google Scholar]
  11. Lai S. K., Lai C. H., Yung K. K., Shum D. K., Chan Y. S. 2006; Maturation of otolith-related brainstem neurons in the detection of vertical linear acceleration in rats. Eur J Neurosci 23:2431–2446 [CrossRef]
     [Google Scholar]
  12. Lewis M. L., Reynolds J. L., Cubano L. A., Hatton J. P., Lawless B. D., Piepmeier E. H. 1998; Spaceflight alters microtubules and increases apoptosis in human lymphocytes (Jurkat. FASEB J 12:1007–1018
     [Google Scholar]
  13. Madrid M., Soto T., Franco A., Paredes V., Vicente J., Hidalgo E., Gacto M., Cansado J. 2004; A cooperative role for Atf1 and Pap1 in the detoxification of the oxidative stress induced by glucose deprivation in Schizosaccharomyces pombe. J Biol Chem 279:41594–41602 [CrossRef]
     [Google Scholar]
  14. Madrid M., Soto T., Khong H. K., Franco A., Vicente J., Gacto M., Cansado J., Pérez P. 2006; Stress-induced response, localization, and regulation of the Pmk1 cell integrity pathway in Schizosaccharomyces pombe. J Biol Chem 281:2033–2043 [CrossRef]
     [Google Scholar]
  15. Marshall C. J. 1995; Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation. Cell 80:179–185 [CrossRef]
     [Google Scholar]
  16. Monshausen G. B., Sievers A. 2002; Basipetal propagation of gravity-induced surface pH changes along primary roots of Lepidium sativum L. Planta 215:980–988 [CrossRef]
     [Google Scholar]
  17. Moreno S., Klar A., Nurse P. 1991; Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol 194:795–823
     [Google Scholar]
  18. Nakamura K. D., Schlenk F. 1973; Stability of Candida utilis cells and spheroplasts toward gravitational forces. J Bacteriol 116:1472–1473
     [Google Scholar]
  19. Nickerson C. A., Ott C. M., Wilson J. V., Ramamurthy M., Pierson D. L. 2004; Microbial responses to microgravity and other low-shear environments. Microbiol Mol Biol Rev 68:345–361 [CrossRef]
     [Google Scholar]
  20. Okaichi K., Ide M., Usui A., Okumura Y. 2004; Hypergravity induces phosphorylation of p53 at serine 15, but not an expression of p53-downstream genes. J Radiat Res 45:399–403 [CrossRef]
     [Google Scholar]
  21. Petersen J., Hagan I. M. 2005; Polo kinase links the stress pathway to cell cycle control and tip growth in fission yeast. Nature 435:507–512 [CrossRef]
     [Google Scholar]
  22. Quinn J., Findlay V. J., Dawson K., Millar J. B. A., Jones N., Morgan B. A., Toone W. M. 2002; Distinct regulatory proteins control the graded transcriptional response to increasing H2O2 levels in fission yeast Schizosaccharomyces pombe. Mol Biol Cell 13:805–816 [CrossRef]
     [Google Scholar]
  23. Rupes I., Jia Z., Young P. G. 1999; Ssp1 promotes actin depolymerization and is involved in stress response and new end take-off control in fission yeast. Mol Biol Cell 10:1495–1510 [CrossRef]
     [Google Scholar]
  24. Shiozaki K., Russell P. 1995; Cell-cycle control linked to extracellular environment by MAP kinase pathway in fission yeast. Nature 378:739–743 [CrossRef]
     [Google Scholar]
  25. Shiozaki K., Russell P. 1997; Stress-activated protein kinase pathway in cell cycle control of fission yeast. Methods Enzymol 283:506–520
     [Google Scholar]
  26. Shiozaki K., Shiozaki M., Russell P. 1998; Heat stress activates fission yeast Spc1/Sty1 MAPK by a MEKK-independent mechanism. Mol Biol Cell 9:1339–1349 [CrossRef]
     [Google Scholar]
  27. Soto T., Beltran F. F., Paredes V., Madrid M., Millar J. B. A., Vicente-Soler J., Cansado J., Gacto M. 2002; Cold induces stress-activated protein kinase-mediated response in the fission yeast Schizosaccharomyces pombe. Eur J Biochem 269:5056–5065 [CrossRef]
     [Google Scholar]
  28. Tabony J., Pochon N., Papaseit C. 2001; Microtubule self-organisation depends upon gravity. Adv Space Res 28:529–535 [CrossRef]
     [Google Scholar]
  29. Tairbekov M. G. 2004; Mechanisms of the gravitational sensitivity of cells. J Gravit Physiol 11:P181–P183
     [Google Scholar]
  30. Toda T., Shimanuki M., Yanagida M. 1991; Fission yeast genes that confer resistance to staurosporine encode an AP-1-like transcription factor and a protein kinase related to the mammalian ERK1/MAP2 and budding yeast FUS3 and KSS1 kinases. Genes Dev 5:60–73 [CrossRef]
     [Google Scholar]
  31. Treisman R. 1996; Regulation of transcription by MAP kinase cascades. Curr Opin Cell Biol 8:205–215 [CrossRef]
     [Google Scholar]
  32. van Loon J. J., Folgering E. H., Bouten C. V., Smit T. H. 2004; Centrifuges and inertial shear forces. J Gravit Physiol 11:29–38
     [Google Scholar]
  33. Waskiewicz A. J., Cooper J. A. 1995; Mitogen and stress response pathways: MAP kinase cascades and phosphatase regulation in mammals and yeast. Curr Opin Cell Biol 7:798–805 [CrossRef]
     [Google Scholar]
  34. Wilkinson M. G., Millar J. B. A. 1998; SAPKs and transcription factors do the nucleocytoplasmic tango. Genes Dev 12:1391–1397 [CrossRef]
     [Google Scholar]
  35. Yoshida N., Minamimura T., Yoshida T., Ogawa K. 1999; Effect of hypergravitational stress on microbial cell viability. J Biosci Bioeng 88:342–344 [CrossRef]
     [Google Scholar]
  36. Zaitsevskaya-Carter T., Cooper J. A. 1997; Spm1, a stress-activated MAP kinase that regulates morphogenesis in S. pombe. EMBO J 16:1318–1331 [CrossRef]
     [Google Scholar]
  37. Zayzafoon M., Meyers V. E., McDonald J. M. 2005; Microgravity: the immune response and bone. Immunol Rev 208:267–280 [CrossRef]
     [Google Scholar]
/content/journal/micro/10.1099/mic.0.2006/004283-0
Loading
Transduction of centrifugation-induced gravity forces through mitogen-activated protein kinase pathways in the fission yeast Schizosaccharomyces pombe
Microbiology 153, 1519 (2007); https://doi.org/10.1099/mic.0.2006/004283-0
/content/journal/micro/10.1099/mic.0.2006/004283-0
/content/journal/micro/10.1099/mic.0.2006/004283-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error