Solute traffic across mammalian peroxisomal membrane - Single-channel conductance monitoring reveals pore-forming activities in peroxisomes

Cellular and Molecular Life Sciences

Volumn 62, Issue 23, 2005, Pages 2886-2895

  Antonenkov, V D ^a   Rokka, A ^a   Sormunen, R T ^a   Benz, R ^b   Hiltunen, J K ^a  

^a UNIVERSITY OF OULU   (Finland)

^b UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

Mammalian peroxisome; Membrane; Pore forming channel; Single channel analysis

Indexed keywords

ANIMAL CELL; ARTICLE; CELL ISOLATION; CELL ORGANELLE; CENTRIFUGATION; CONDUCTANCE; CONTROLLED STUDY; DENSITY GRADIENT CENTRIFUGATION; ELECTRON MICROSCOPY; ENDOPLASMIC RETICULUM; ENZYME ASSAY; IMMUNOBLOTTING; LYSOSOME; MALE; MITOCHONDRION; MOUSE; NONHUMAN; PEROXISOME; POLYACRYLAMIDE GEL ELECTROPHORESIS; POROSITY; PROTEIN CONTENT; SOLUTE;

ANIMALIA; MAMMALIA;

EID: 28844503851     PISSN: 1420682X     EISSN: 15691632     Source Type: Journal    
DOI: 10.1007/s00018-005-5233-x     Document Type: Article

References (49)

1. Masters C. and Crane D. (1995) The Peroxisomes: A Vital Organelle. Cambrige University Press, Cambridge
2. Mannaerts G. P., Van Veldhoven P. P. and Casteels M. (2000) Peroxisomal lipid degradation via beta- and alpha-oxidation in mammals. Cell Biochem. Biophys. 32: 73-87
3. Hiltunen J. K., Mursula A. M., Rottensteiner H., Wierenga R. K., Kastaniotis A. J. and Gurvitz A. (2003) The biochemistry of peroxisomal beta-oxidation in the yeast Saccharomyces cerevisiae. FEMS Microbiol. Rev. 27: 35-64
4. Wanders R. J., Schutgens R. B. and Barth P. G. (1995) Peroxisomal disorders: a review. J. Neuropathol. Exp. Neurol. 54: 726-739
5. Wanders R. J., Vreken P., Ferdinandusse S., Jansen G. A., Waterham H. R., Roermund C. W. T. van et al. (2001) Peroxisomal fatty acid alpha- and beta-oxidation in humans: enzymology, peroxisomal metabolite transporters and peroxisomal diseases. Biochem. Soc. Trans. 29: 250-267
6. Roermund C. W. van, Waterham H. R., Ijlst L. and Wanders R. J. (2003) Fatty acid metabolism in Saccharomyces cerevisiae. Cell. Mol. Life Sci. 60: 1838-1851
7. Antonenkov V. D., Sormunen R. T. and Hiltunen J. K. (2004) The rat liver peroxisomal membrane forms a permeability barrier for cofactors but not for small metabolites in vitro. J. Cell Sci. 117: 5633-5642
8. Antonenkov V. D., Sormunen R. T. and Hiltunen J. K. (2004) The behavior of peroxisomes in vitro: mammalian peroxisomes are osmotically sensitive particles. Am. J. Physiol. Cell Physiol. 287: C1623-C1635
9. Reumann S., Maier E., Benz R. and Heldt H. W. (1995) The membrane of leaf peroxisomes contains a porin-like channel. J. Biol. Chem. 270: 17559-17565
10. Reumann S., Bettermann M., Benz R. and Heldt H. W. (1997) Evidence for the presence of a porin in the membrane of glyoxysomes of castor bean. Plant Physiol. 115: 891-899
11. Reumann S., Maier E., Heldt H. W. and Benz R. (1998) Permeability properties of the porin of spinach leaf peroxisomes. Eur. J. Biochem. 251: 359-366
12. Sulter G. J., Verheyden K., Mannaerts G., Harder W. and Veenhuis M. (1993) The in vitro permeability of yeast peroxisomal membranes is caused by a 31 kDa integral membrane protein. Yeast 9: 733-742
13. Labarca P., Wolff D., Soto U., Necochea C. and Leighton F. (1986) Large cation-selective pores from rat liver peroxisomal membranes incorporated to planar lipid bilayers. J. Membr. Biol. 94: 285-291
14. Lemmens M., Verheyden K., Van Veldhoven P., Vereecke J., Mannaerts G. P. and Carmeliet E. (1989) Single-channel analysis of a large conductance channel in peroxisomes from rat liver. Biochim. Biophys. Acta 984: 351-359
15. Van Veldhoven P. P., Just W. W. and Mannaerts G. P. (1987) Permeability of the peroxisomal membrane to cofactors of beta-oxidation: evidence for the presence of a pore-forming protein. J. Biol. Chem. 262: 4310-4318
16. Nicolay K., Veenhuis M., Douma A. C. and Harder W. (1987) A 31P NMR study of the internal pH of yeast peroxisomes. Arch. Microbiol. 147: 37-41
17. Roermund C. W. van, Elgersma Y., Singh N., Wanders R. J. and Tabak H. F. (1995) The membrane of peroxisomes in Saccharomyces cerevisiae is impermeable to NAD(H) and acetyl-CoA under in vivo conditions. EMBO J. 14: 3480-3486
18. Roermund C. W. van, Hettema E. H., Kal A. J., Berg M. van den, Tabak H. F. and Wanders R. J. (1998) Peroxisomal beta-oxidation of polyunsaturated fatty acids in Saccharomyces cerevisiae: isocitrate dehydrogenase provides NADPH for reduction of double bonds at even positions. EMBO J. 17: 677-687
19. Roermund C. W. van, Hettema E. H., Berg M. van den, Tabak H. F. and Wanders R. J. (1999) Molecular characterization of carnitine-dependent transport of acetyl-CoA from peroxisomes to mitochondria in Saccharomyces cerevisiae and identification of a plasma membrane carnitine transporter, Agp2p. EMBO J. 18: 5843-5852
20. Dansen T. B., Wirtz K. W., Wanders R. J. and Pap E. H. (2000) Peroxisomes in human fibroblasts have a basic pH. Nat. Cell Biol. 2: 51-53
21. Palmieri L., Rottensteiner H., Girzalsky W., Scarcia P., Palmieri F. and Erdmann R. (2001) Identification and functional reconstitution of the yeast peroxisomal adenine nucleotide transporter. EMBO J. 20: 5049-5059
22. Visser W. F., Roermund C. W. van, Waterham H. R. and Wanders R. J. (2002) Identification of human PMP34 as a peroxisomal ATP transporter. Biochem. Biophys. Res. Commun. 299: 494-497
23. Visser W. F., Roermund C. W. van, Ijlst L., Hellingwerf K. J., Wanders R. J. and Waterham H. R. (2005) Demonstration and characterization of phosphate transport in mammalian peroxisomes. Biochem. J. 389: 717-722
24. Antonenkov V. D. (1989) Dehydrogenases of the pentose phosphate pathway in rat liver peroxisomes. Eur. J. Biochem. 183: 75-82
25. Graham J. M. (1999) Purification of a crude mitochondrial fraction by density-gradient centrifugation. In: Current Protocols in Cell Biology, Suppl. 4, pp. 3.4.1-3.4.3, Wiley, New York
26. Leighton F., Poole B., Beaufay H., Baudhuin P., Coffey J. W., Fowler S. et al. (1968) The large-scale separation of peroxisomes, mitochondria, and lysosomes from the livers of rats injected with triton WR-1339: improved isolation procedures, automated analysis, biochemical and morphological properties of fractions. J. Cell Biol. 37: 482-513
27. Fujiki Y., Hubbard A. L., Fowler S. and Lazarow P. B. (1982) Isolation of intracellular membranes by means of sodium carbonate treatment: application to endoplasmic reticulum. J. Cell Biol. 93: 97-102
28. Ludwig O., De Pinto V., Palmieri F. and Benz R. (1986) Pore formation by the mitochondrial porin of rat brain in lipid bilayer membranes. Biochim. Biophys. Acta 860: 268-276
29. Novikov D. K., Vanhove G. F., Carchon H., Asselberghs S., Eyssen H. J., Van Veldhoven P. P. et al. (1994) Peroxisomal beta-oxidation: purification of four novel 3-hydroxyacyl-CoA dehydrogenases from rat liver peroxisomes. J. Biol. Chem. 269: 27125-27135
30. Sambrook J., Fritsch E. F. and Maniatis T. (1989) Molecular Cloning: A Laboratory Manual, 2nd edn, pp. 18.3-18.10., Cold Spring Harbor Laboratory Press, Cold Spring Harbor
31. Stoscheck C. M. (1990) Quantitation of protein. Methods Enzymol. 182: 50-68
32. Alexson S. E., Fujiki Y., Shio H. and Lazarow P. B. (1985) Partial disassembly of peroxisomes. J. Cell Biol. 101: 294-304
33. Bodnar A. G. and Rachubinski R. A. (1991) Characterization of the integral membrane polypeptides of rat liver peroxisomes isolated from untreated and clofibrate-treated rats. Biochem. Cell Biol. 69: 499-508
34. Benz R. (1994) Permeation of hydrophilic solutes through mitochondrial outer membranes: review on mitochondrial porins. Biochim. Biophys. Acta 1197: 167-96
35. Bullock J.O., Kolen, E.R. and Shear, J.L. (1992) Ion selectivity of colicin E1. II. Permeability to organic cations. J. Membrane Biol. 128: 1-16
36. De Pinto V., Ludwig O., Krause J., Benz R. and Palmieri F. (1987) Porin pores of mitochondrial outer membranes from high and low eukaryotic cells: biochemical and biophysical characterization. Biochim. Biophys. Acta 894: 109-119
37. Baudhuin P. (1969) Liver peroxisomes, cytology and function. Ann. N. Y. Acad. Sci. 168: 214-228
38. Lasorsa F. M., Scarcia P., Erdmann R., Palmieri F., Rottensteiner H. and Palmieri L. (2004) The yeast peroxisomal adenine nucleotide transporter: characterization of two transport modes and involvement in DeltapH formation across peroxisomal membranes. Biochem. J. 381: 581-585
39. Roermund C. W. van, Jong M. de, Ijlst L., Marie J. van, Dansen T. B., Wanders R. J. et al. (2004) The peroxisomal lumen in Saccharomyces cerevisiae is alkaline. J. Cell Sci. 117: 4231-4237
40. Jankowski A., Kim J. H., Collins R. F., Daneman R., Walton P. and Grinstein S. (2001) In situ measurements of the pH of mammalian peroxisomes using the fluorescent protein pHluorin. J. Biol. Chem. 276: 48748-48753
41. Alberts B., Johnson A., Lewis J., Raff M., Roberts K. and Walter P. (2002) Molecular Biology of the Cell, 4nd edn, pp. 615-657, Garland Science, New York
42. Price N. C., Dwek R. A., Ratcliffe R. G. and Wormald M. R. (2001) Principles and Problems in Physical Chemistry for Biochemists, 3nd edn, pp. 132-134, Oxford University Press, Oxford
43. Moriyama Y., Maeda M. and Futai M. (1992) Involvement of a non-proton pump factor (possibly Donnan-type equilibrium) in maintenance of an acidic pH in lysosomes. FEBS Lett. 302: 18-20
44. Morrill G. A., Kostellow A. B., Osterlow K. and Gupta R. K. (1996) Differences in hydration state of nucleus and cytoplasm of the amphibian oocyte. J. Membr. Biol. 153: 45-51
45. Wong P. (2002) A hypothesis of haemolysis in haemolytic anaemias associated with enzymopathies. Med. Hypoth. 59: 105-109
46. Hettema E. H. and Tabak H. F. (2000) Transport of fatty acids and metabolites across the peroxisomal membrane. Biochim. Biophys. Acta 1486: 18-27
47. Borst P. and Elferink R. O. (2002) Mammalian ABC transporters in health and disease. Annu. Rev. Biochem. 71: 537-592
48. Fraser F., Corstorphine C. G., Price N. T. and Zammit V. A. (1999) Evidence that carnitine palmitoyltransferase I (CPT I) is expressed in microsomes and peroxisomes of rat liver: distinct immunoreactivity of the N-terminal domain of the microsomal protein. FEBS Lett. 446: 69-74
49. McClelland G. B., Khanna S., Gonzalez G. F., Butz C. E. and Brooks G. A. (2003) Peroxisomal membrane monocarboxylate transporters: evidence for a redox shuttle system? Biochem. Biophys. Res. Commun. 304: 130-135