Interaction between peroxisomes and mitochondria in fatty acid metabolism

Françoise Le Borgne, Jean Demarquoy

.
Université de Bourgogne, Inserm U866, Laboratory of Metabolic Biochemistry and Nutrition, Dijon, France.

DOI: 10.4236/ojmip.2012.21005                

Abstract

Peroxisomes and mitochondria are ubiquitously found organelles. They both are dynamic structures able to divide, to fuse and to undergo autophagic processes. Their activities are dependent on proteins that are, for most (mitochondria) or all (peroxisome) of them, synthesized in the cytosol from the nuclear genome. Nevertheless, the membrane structures and the DNA content differ between these two organelles. Mitochondria possess a small circular genome while peroxisomes don’t. The control of their dynamic is dependent on specific factors even if some of those are able to affect both. These two organelles are metabolically connected: they are both involved in lipid metabolism. They are both able to beta oxidize fatty acids and are implicated in ROS production. However, their precise function in these metabolic pathways and their physiological functions are different. While mitochondrial metabolism is closely related to energy production, peroxisome does not seem to be associated with energy production but with the production of bioactive molecules and in detoxification processes.

Keywords

Peroxisome; Mitochondria; Fatty Acid Metabolism; Beta Oxidation

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1]	Montoya, J., Lopez-Gallardo, E., Diez-Sanchez, C., Lopez-Perez, M.J. and Ruiz-Pesini, E. (2009) 20 years of human mtDNA pathologic point mutations: Carefully reading the pathogenicity criteria. Biochimica et Biophysica Acta, 1787, 476-483. doi:10.1016/j.bbabio.2008.09.003
[2]	Howell, N., Elson, J.L., Chinnery, P.F. and Turnbull, D.M. (2005) MtDNA mutations and common neurodegenerative disorders. Trends in Genetics, 21, 583-586. doi:10.1016/j.tig.2005.08.012
[3]	Schmidt, O., Pfanner, N. and Meisinger, C. (2010) Mitochondrial protein import: From proteomics to functional mechanisms. Nature Reviews Molecular Cell Biology, 11, 655-667. doi:10.1038/nrm2959
[4]	Kukat, A. and Trifunovic, A. (2009) Somatic mtDNA mutations and aging—Facts and fancies. Experimental Gerontology, 44, 101-105. doi:10.1016/j.exger.2008.05.006
[5]	Pang, C.Y., Ma, Y.S. and Wei, Y.U. (2008) MtDNA mutations, functional decline and turnover of mitochondria in aging. Frontiers in Bioscience, 13, 3661-3675. doi:10.2741/2957
[6]	Okamoto, K. and Shaw, J.M. (2005) Mitochondrial morphology and dynamics in yeast and multicellular eukaryotes. Annual Reviews Genetics, 39, 503-536. doi:10.1146/annurev.genet.38.072902.093019
[7]	Chen, H. and Chan, D.C. (2009) Mitochondrial dynamics—fusion, fission, movement, and mitophagy—in neurodegenerative diseases. Human Molecular Genetics, 18, R169-R176. doi:10.1093/hmg/ddp326
[8]	Chan, D.C. (2006) Mitochondria: Dynamic organelles in disease, aging, and development. Cell, 125, 1241-1252. doi:10.1016/j.cell.2006.06.010
[9]	Olichon, A., Guillou, E., Delettre, C., Landes, T., Arnaune-Pelloquin, L., Emorine, L.J., Mils, V., Daloyau, M., Hamel, C., Amati-Bonneau, P., et al. (2006) Mitochondrial dynamics and disease, OPA1. Biochimica et Biophysica Acta, 1763, 500-509. doi:10.1016/j.bbamcr.2006.04.003
[10]	Detmer, S.A. and Chan, D.C. (2007) Functions and dysfunctions of mitochondrial dynamics. Nature Reviews Molecular Cell Biology, 8, 870-879. doi:10.1038/nrm2275
[11]	Chen, H., Detmer, S.A., Ewald, A.J., Griffin, E.E., Fraser, S.E. and Chan, D.C. (2003) Mitofusins Mfn1 and Mfn2 coordinately regulate mitochondrial fusion and are essential for embryonic development. The Journal of Cell Bio- logy, 160, 189-200. doi:10.1083/jcb.200211046
[12]	Detmer, S.A., Van de Velde, C., Cleveland, D.W. and Chan, D.C. (2008) Hindlimb gait defects due to motor axon loss and reduced distal muscles in a transgenic mouse model of Charcot-Marie-Tooth type 2A. Human Molecular Genetics, 17, 367-375. doi:10.1093/hmg/ddm314
[13]	Davies, V.J., Hollins, A.J., Piechota, M.J., Yip, W., Davies, J.R., White, K.E., Nicols, P.P., Boulton, M.E. and Votruba, M. (2007) Opa1 deficiency in a mouse model of autosomal dominant optic atrophy impairs mitochondrial morphology, optic nerve structure and visual function. Human Molecular Genetics, 16, 1307-1318. doi:10.1093/hmg/ddm079
[14]	Wakabayashi, J., Zhang, Z., Wakabayashi, N., Tamura, Y., Fukaya, M., Kensler, T.W., Iijima, M. and Sesaki, H. (2009) The dynamin-related GTPase Drp1 is required for embryonic and brain development in mice. The Journal of Cell Biology, 186, 805-816. doi:10.1083/jcb.200903065
[15]	Otsuga, D., Keegan, B.R., Brisch, E., Thatcher, J.W., Hermann, G.J., Bleazard, W. and Shaw, J.M. (1998) The dynamin-related GTPase, Dnm1p, controls mitochondrial morphology in yeast. The Journal of Cell Biology, 143, 333-349. doi:10.1083/jcb.143.2.333
[16]	Smirnova, E., Shurland, D.L., Ryazantsev, S.N. and Van de Bliek, A.M. (1998) A human dynamin-related protein controls the distribution of mitochondria. The Journal of Cell Biology, 143, 351-358. doi:10.1083/jcb.143.2.351
[17]	Cho, D.H., Nakamura, T., Fang, J., Cieplak, P., Godzik, A., Gu, Z. and Lipton, S.A. (2009) S-nitrosylation of Drp1 mediates β-amyloid-related mitochondrial fission and neuronal injury. Science, 324, 102-105. doi:10.1126/science.1171091
[18]	Ishihara, N., Nomura, M., Jofuku, A., Kato, H., Suzuki, S.O., Masuda, K., Otera, H., Nakanishi, Y., Nonaka, I., Goto, Y., et al. (2009) Mitochondrial fission factor Drp1 is essential for embryonic development and synapse formation in mice. Nature Cell Biology, 11, 958-966. doi:10.1038/ncb1907
[19]	MacAskill, A.F. and Kittler, J.T. (2010) Control of mitochondrial transport and localization in neurons. Trends in Cell Biology, 20, 102-112. doi:10.1016/j.tcb.2009.11.002
[20]	Zinsmaier, K.E., Babic, M. and Russo, G.J. (2009) Mitochondrial transport dynamics in axons and dendrites. Results Problems in Cell Differentiation, 48, 107-139. doi:10.1007/400_2009_20
[21]	Pathak, D., Sepp, K.J. and Hollenbeck, P.J. (2010) Evidence that myosin activity opposes microtubule-based axonal transport of mitochondria. The Journal of Neuroscience, 30, 8984-8992. doi:10.1523/JNEUROSCI.1621-10.2010
[22]	Burman, C. and Ktistakis, N.T. (2010) Autophagosome formation in mammalian cells. Seminars in Immunopathology, 32, 397-413. doi:10.1007/s00281-010-0222-z
[23]	Kanki, T. and Klionsky, D.J. (2008) Mitophagy in yeast occurs through a selective mechanism. The Journal of Biological Chemistry, 283, 32386-32393. doi:10.1074/jbc.M802403200
[24]	Smith, J.J. and Aitchison, J.D. (2009) Regulation of peroxisome dynamics. Current Opinion in Cell Biology, 21, 119-126. doi:10.1016/j.ceb.2009.01.009
[25]	Titorenko, V.I. and Mullen, R.T. (2006) Peroxisome biogenesis: the peroxisomal endomembrane system and the role of the ER. The Journal of Cell Biology, 174, 11-17. doi:10.1083/jcb.200604036
[26]	South, S.T. and Gould, S.J. (1999) Peroxisome synthesis in the absence of preexisting peroxisomes. The Journal of Cell Biology, 144, 255-266. doi:10.1083/jcb.144.2.255
[27]	Koch, A., Schneider, G., Luers, G.H. and Schrader, M. (2004) Peroxisome elongation and constriction but not fission can occur independently of dynamin-like protein 1. Journal of Cell Science, 117, 3995-4006. doi:10.1242/jcs.01268
[28]	Li, X. and Gould, S.J. (2003) The dynamin-like GTPase DLP1 is essential for peroxisome division and is recruited to peroxisomes in part by PEX11. The Journal of Biological Chemistry, 278, 17012-17020. doi:10.1074/jbc.M212031200
[29]	Sakai, Y., Oku, M., Van der Klei, I.J. and Kiel, J. A. (2006) Pexophagy: Autophagic degradation of peroxisomes. Biochimica et Biophysica Acta, 1763, 1767-1775. doi:10.1016/j.bbamcr.2006.08.023
[30]	Schmidt, O., Pfanner, N. and Meisinger, C. (2010) Mitochondrial protein import: From proteomics to functional mechanisms. Nature Review Molecular Cell Biology, 11, 655-667. doi:10.1038/nrm2959
[31]	Brown, L.A. and Baker, A. (2008) Shuttles and cycles: Transport of proteins into the peroxisome matrix (review). Molecular Membrane Biology, 25, 363-375. doi:10.1080/09687680802130583
[32]	Poirier, Y., Antonenkov, V.D., Glumoff, T. and Hiltunen, J.K. (2006) Peroxisomal β-oxidation—A metabolic pathway with multiple functions. Biochimica et Biophysica Acta, 1763, 1413-1426. doi:10.1016/j.bbamcr.2006.08.034
[33]	Wanders, R.J., Ferdinandusse, S., Brites, P. and Kemp, S. (2010) Peroxisomes, lipid metabolism and lipotoxicity. Biochimica Biophysica Acta, 1801, 272-280.
[34]	Goepfert, S. and Poirier, Y. (2007) Beta-oxidation in fatty acid degradation and beyond. Current Opinion Plant Biology, 10, 245-251. doi:10.1016/j.pbi.2007.04.007
[35]	Eaton, S., Bartlett, K. and Pourfarzam, M. (1996) Mammalian mitochondrial beta-oxidation. Biochemical Journal, 320, 345-357.
[36]	Van Roermund, C.W., Visser, W.F., Ijlst, L., Waterham, H.R. and Wanders, R.J. (2011) Differential substrate specificities of human ABCD1 and ABCD2 in peroxisomal fatty acid beta-oxidation. Biochimica et Biophysica Acta, 1811, 148-152.
[37]	Mannaerts, G.P., Van Veldhoven, P.P. and Casteels, M. (2000) Peroxisomal lipid degradation via β- and α-oxidation in mammals. Cell Biochemistry and Biophysics, 32, 73-87. doi:10.1385/CBB:32:1-3:73
[38]	Le Borgne, F., Ben Mohamed, A., Logerot, M., Garnier, E. and Demarquoy, J. (2011) Changes in carnitine octanoyltransferase activity induce alteration in fatty acid metabolism. Biochemical and Biophysical Research Communications, 409, 699-704. doi:10.1016/j.bbrc.2011.05.068
[39]	Caroppi, P., Sinibaldi, F., Fiorucci, L. and Santucci, R. (2009) Apoptosis and human diseases: Mitochondrion damage and lethal role of released cytochrome c as proapoptotic protein. Current Medicinal Chemistry, 16, 4058-4065.
[40]	Gogvadze, V., Orrenius, S. and Zhivotovsky, B. (2006) Multiple pathways of cytochrome c release from mitochondria in apoptosis. Biochimica et Biophysica Acta, 1757, 639-647. doi:10.1016/j.bbabio.2006.03.016
[41]	Jezek, P. and Hlavata, L. (2005) Mitochondria in homeostasis of reactive oxygen species in cell, tissues, and organism. The International Journal of Biochemistry and Cell Biology, 37, 2478-2503. doi:10.1016/j.biocel.2005.05.013
[42]	Angermuller, S. (1989) Peroxisomal oxidases: Cytochemical localization and biological relevance. Progress Histochemistry and Cytochemistry, 20, 1-65.
[43]	Le Borgne, F., Ben Mohamed, A., Logerot, M., Garnier, E. and Demarquoy, J. (2011) Changes in carnitine octanoyltransferase activity induces alteration in fatty acid metabolism. Biochemical and Biophysical Research Communications, 409, 669-704. doi:10.1016/j.bbrc.2011.05.068