Hostname: page-component-586b7cd67f-l7hp2 Total loading time: 0 Render date: 2024-11-22T17:27:59.889Z Has data issue: false hasContentIssue false
  • English
  • Français

Two-Photon Imaging of Cellular Activities in Oxygen Sensing Tissues

Published online by Cambridge University Press:  06 November 2008

Christoph Wotzlaw ,
Utta Berchner-Pfannschmidt ,
Joachim Fandrey  and
Helmut Acker
Christoph Wotzlaw
Affiliation:
Institut für Physiologie, Universität Duisburg-Essen, Hufelandstraße 55, D-45122 Essen, Germany
Utta Berchner-Pfannschmidt
Affiliation:
Institut für Physiologie, Universität Duisburg-Essen, Hufelandstraße 55, D-45122 Essen, Germany
Joachim Fandrey
Affiliation:
Institut für Physiologie, Universität Duisburg-Essen, Hufelandstraße 55, D-45122 Essen, Germany
Helmut Acker*
Affiliation:
Institut für Physiologie, Universität Duisburg-Essen, Hufelandstraße 55, D-45122 Essen, Germany
*
Corresponding author. E-mail: [email protected]
Get access

Abstract

The cellular oxygen sensing system of the body ensures appropriate adaptation of cellular functions toward hypoxia by regulating gene expression and ion channel activity. Two-photon laser microscopy is an ideal tool to study and prove the relevance of the molecular mechanisms within oxygen sensing pathways on the cellular and complex tissue or organ level. Images of hypoxia inducible factor 1 (HIF-1) subunit nuclear mobility and protein-protein interaction in living cells, of hypoxia-induced changes in membrane potential and intracellular calcium of live ex vivo carotid bodies as well as of rat kidney proximal tubulus function in vivo, will be shown.

Keywords

oxygen sensingHIFmembrane potential(Ca++)iU2OS cellcarotid bodykidneyFRETFRAP3D imaging
Type
Multiphoton Microscopy–Special Section
Information
Microscopy and Microanalysis , Volume 14 , Issue 6 , December 2008 , pp. 519 - 525
Copyright
Copyright © Microscopy Society of America 2008

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Abudara, V. & Eyzaguirre, C. (1998). Modulation of junctional conductance between rat carotid body glomus cells by hypoxia, cAMP and acidity. Brain Res 792, 114–125.Google Scholar
Acker, H. (2005). The oxygen sensing signal cascade under the influence of reactive oxygen species. Philos Trans R Soc Lond B Biol Sci 360, 2201–2210.CrossRefGoogle ScholarPubMed
Acker, H. & O'Regan, R.G. (1979). Autonomic nervous influences upon total flow, local flow, tissue PO2 and chemosensory activity of the cat carotid body [Proceedings]. J Physiol (Lond) 295, 95P–96P.Google ScholarPubMed
Acker, T., Fandrey, J. & Acker, H. (2006). The good, the bad and the ugly in oxygen-sensing: ROS, cytochromes and prolyl-hydroxylases. Cardiovasc Res 71, 195–207.Google Scholar
Appelhoff, R.J., Tian, Y.M., Raval, R.R., Turley, H., Harris, A.L., Pugh, C.W., Ratcliffe, P.J. & Gleadle, J.M. (2004). Differential function of the prolyl hydroxylases PHD1, PHD2, and PHD3 in the regulation of hypoxia-inducible factor. J Biol Chem 279, 38458–38465.CrossRefGoogle ScholarPubMed
Baysal, B.E., Ferrell, R.E., Willett-Brozick, J.E., Lawrence, E.C., Myssiorek, D., Bosch, A., van der May, A., Taschner, P.E., Rubinstein, W.S., Myers, E.N., Richard, C.W. III, Cornelisse, C.J., Devilee, P. & Devlin, B. (2000). Mutations in SDHD, a mitochondrial complex II gene, in hereditary paraganglioma. Science 287, 848–851.Google Scholar
Berchner-Pfannschmidt, U., Wotzlaw, C., Merten, E., Acker, H. & Fandrey, J. (2004). Visualization of the three-dimensional organization of hypoxia-inducible factor-1 alpha and interacting cofactors in subnuclear structures. Biol Chem 385, 231–237.CrossRefGoogle ScholarPubMed
Berra, E., Ginouves, A. & Pouyssegur, J. (2006). The hypoxia-inducible-factor hydroxylases bring fresh air into hypoxia signalling. EMBO Rep 7, 41–45.Google Scholar
Cross, A.R., Henderson, L., Jones, O.T., Delpiano, M.A., Hentschel, J. & Acker, H. (1990). Involvement of an NAD(P)H oxidase as a PO2 sensor protein in the rat carotid body. Biochem J 272, 743–747.CrossRefGoogle ScholarPubMed
Erbel, P.J., Card, P.B., Karakuzu, O., Bruick, R.K. & Gardner, K.H. (2003). Structural basis for PAS domain heterodimerization in the basic helix–loop–helix-PAS transcription factor hypoxia-inducible factor. Proc Natl Acad Sci USA 100, 15504–15509.CrossRefGoogle ScholarPubMed
Fandrey, J., Gorr, T.A. & Gassmann, M. (2006). Regulating cellular oxygen sensing by hydroxylation. Cardiovasc Res 71, 642–651.Google Scholar
Fisher, J.A.N., Salzberg, B.M. & Yodh, A.G. (2005). Near infrared two-photon excitation cross-sections of voltage-sensitive dyes. J Neurosci Meth 148, 102.CrossRefGoogle ScholarPubMed
Fu, X.W., Wang, D., Nurse, C.A., Dinauer, M.C. & Cutz, E. (2000). NADPH oxidase is an O2 sensor in airway chemoreceptors: Evidence from K+ current modulation in wild-type and oxidase-deficient mice. Proc Natl Acad Sci USA 97, 4374–4379.Google Scholar
Furness, J.B. & Costa, M. (1975). The use of glyoxylic acid for the fluorescence histochemical demonstration of peripheral stores of noradrenaline and 5-hydroxytryptamine in whole mounts. Histochem 41, 335–352.CrossRefGoogle ScholarPubMed
Hockberger, P.E., Skimia, T.A., Centonze, V.E., Lavin, C., Chu, S., Dadras, S., Reddy, J.K. & White, J.G. (1999). Activation of flavin-containing oxidases underlies light-induced production of H2O2 in mammalian cells. Proc Natl Acad Sci USA 96, 6255–6260.CrossRefGoogle ScholarPubMed
Hörbelt, M., Wotzlaw, C., Sutton, T.A., Molitoris, B.A., Philipp, T., Kribben, A., Fandrey, J. & Pietruck, F. (2007). Organic cation transport in the rat kidney in vivo visualized by time-resolved two-photon microscopy. Kidney Int 72, 422–429.Google Scholar
Kemp, P.J. (2005). Hemeoxygenase-2 as an O-2 sensor in K+ channel-dependent chemotransduction [Review]. Biochem Biophys Res Comm 338, 648–652.CrossRefGoogle Scholar
Lahiri, S. (2000). Historical perspectives of cellular oxygen sensing and responses to hypoxia. J Appl Physiol 88, 1467–1473.Google Scholar
Liu, Q., Berchner-Pfannschmidt, U., Moller, U., Brecht, M., Wotzlaw, C., Acker, H., Jungermann, K. & Kietzmann, T. (2004). A Fenton reaction at the endoplasmic reticulum is involved in the redox control of hypoxia-inducible gene expression. Proc Natl Acad Sci USA 101, 4302–4307.CrossRefGoogle ScholarPubMed
Metzen, E., Berchner-Pfannschmidt, U., Stengel, P., Marxsen, J.H., Stolze, I., Klinger, M., Huang, W.Q., Wotzlaw, C., Hellwig-Burgel, T., Jelkmann, W., Acker, H. & Fandrey, J. (2003). Intracellular localisation of human HIF-1 alpha hydroxylases: Implications for oxygen sensing. J Cell Sci 116, 1319–1326.CrossRefGoogle ScholarPubMed
Pardal, R., Ortega-Saenz, P., Duran, R. & Lopez-Barneo, J. (2007). Glia-like stem cells sustain physiologic neurogenesis in the adult mammalian carotid body. Cell 131, 364–377.CrossRefGoogle ScholarPubMed
Plotkin, M.D. & Goligorsky, M.S. (2006). Mesenchymal cells from adult kidney support angiogenesis and differentiate into multiple interstitial cell types including erythropoietin-producing fibroblasts. Am J Physiol Renal Physiol 291, F902–F912.CrossRefGoogle ScholarPubMed
Seidl, E., Acker, H. & Teckhaus, L. (1979). Quantitative determination of the vascular volume of the cat carotid body under normoxia, hyperoxia, hypoxia and hypercapnia (author's transl). Microsc Acta Suppl185–187.Google Scholar
Streller, T., Huckstorf, C., Pfeiffer, C. & Acker, H. (2002). Unusual cytochrome a(592) with low PO2 affinity correlates as putative oxygen sensor with rat carotid body chemoreceptor discharge. FASEB J 16, 1277–1279.Google Scholar
Wang, G.L. & Semenza, G.L. (1995). Purification and characterization of hypoxia-inducible factor 1. J Biol Chem 270, 1230–1237.CrossRefGoogle ScholarPubMed
Weir, E.K., Lopez-Barneo, J., Buckler, K.J. & Archer, S.L. (2005). Acute oxygen-sensing mechanisms. N Engl J Med 353, 2042–2055.Google Scholar
Wiesener, M.S., Jurgensen, J.S., Rosenberger, C., Scholze, C.K., Horstrup, J.H., Warnecke, C., Mandriota, S., Bechmann, I., Frei, U.A., Pugh, C.W., Ratcliffe, P.J., Bachmann, S. & Eckardt, K.U. (2003). Widespread hypoxia-inducible expression of HIF-2alpha in distinct cell populations of different organs. FASEB J 17, 271–273.CrossRefGoogle ScholarPubMed
Wilson, D.F., Mokashi, A., Chugh, D., Vinogradov, S., Osanai, S. & Lahiri, S. (1994). The primary oxygen sensor of the cat carotid body is cytochrome a 3 of the mitochondrial respiratory chain. FEBS Lett 351, 370–374.CrossRefGoogle ScholarPubMed
Wotzlaw, C., Otto, T., Berchner-Pfannschmidt, U., Metzen, E., Acker, H. & Fandrey, J. (2007). Optical analysis of the HIF-1 complex in living cells by FRET and FRAP. FASEB J 21, 700–707.CrossRefGoogle ScholarPubMed