[en] In this study a quantitative comparative proteomics approach has been used to analyze the D.
discoideum mitochondrial proteome variations during vegetative growth, starvation and the early stages of development. Application of 2D-DIGE technology allowed the detection of around 2000 protein spots on each two-dimensional gel with 180 proteins exhibiting significant changes in their expression level. In total, 96 proteins (51 unique and 45 redundant) were unambiguously identified. We show that the D. discoideum mitochondrial proteome adaptations mainly affect energy metabolism enzymes (the Krebs cycle, anaplerotic pathways, the oxidative phosphorylation system and energy dissipation), proteins involved in developmental and signalling processes as well as in protein biosynthesis and fate. The most striking observations were the opposite regulation of expression of citrate synthase and aconitase and the very large variation in the expression of the alternative oxidase (AOX) that highlighted the importance of citrate and AOX in the physiology of the development of D. discoideum. Mitochondrial energy states measured in vivo with MitoTracker Orange CMTMRos showed an increase in mitochondrial membrane polarisation during D. discoideum starvation and starvation-induced development.
Disciplines :
Biochemistry, biophysics & molecular biology
Author, co-author :
Czarna, Malgorzata
Mathy, Grégory ; Université de Liège - ULiège > Département des sciences de la vie > Bioénergétique et physiologie cellulaire
Mac Cord, Allan ; Université de Liège - ULiège > Doct. sc. (bioch., bioch. mol.&cell., bioinf.&mod.-Bologne)
Dobson, Rowan ; Université de Liège - ULiège > Département de chimie (sciences) > GIGA-R : Laboratoire de spectrométrie de masse (L.S.M.)
Jarmuszkiewicz, Wieslawa
Sluse-Goffart, Claudine
Leprince, Pierre ; Université de Liège - ULiège > CNCM/ Centre fac. de rech. en neurobiologie cell. et moléc.
De Pauw, Edwin ; Université de Liège - ULiège > Département de chimie (sciences) > GIGA-R : Laboratoire de spectrométrie de masse (L.S.M.)
Sluse, Francis ; Université de Liège - ULiège > Département des sciences de la vie > Bioénergétique et physiologie cellulaire
Language :
English
Title :
Dynamics of the Dictyostelium discoideum mitochondrial proteome during vegetative growth, starvation and early stages of development
Publication date :
January 2010
Journal title :
Proteomics
ISSN :
1615-9853
eISSN :
1615-9861
Publisher :
Wiley-VCH Verlag Gmbh, Weinheim, Germany
Volume :
9
Pages :
1-16
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
FRFC - Fonds de la Recherche Fondamentale Collective [BE]
Barth, C., Le, P., Fisher, P. R., Mitochondrial biology and disease in Dictyostelium. Int. Rev. Cytol. 2007, 263, 207-252.
Eichinger, L., Pachebat, J. A., Glöckner, G., Rajandream, M. A. et al., The genome of the social amoeba Dictyostelium discoideum. Nature 2005, 435, 43-57.
Srinivasan, S., Traini, M., Herbert, B., Sexton, D. et al., Proteomic analysis of a developmentally regulated secretory vesicle. Proteomics 2001, 1, 1119-1127.
Reinders, Y., Schulz, I., Gr. af, R., Sickmann, A., Identification of novel centrosomal proteins in Dictyostelium discoideum by comparative proteomic approach. J. Proteome Res. 2005, 5, 589-598.
Gotthardt, D., Blancheteau, V., Bosserhoff, A., Ruppert, T. et al., Proteomic fingerprinting of phagosome maturation and evidence for the role of a Gáduring uptake. Mol. Cell. Proteom. 2006, 5, 2228-2243.
Mohamad, N., Gutierrez, A., Nunez, M., Cocca, C. et al., Mitochondrial apoptotic pathways. Biocell 2005, 29, 149-161.
Navarro, A., Boveris, S., The mitochondrial energy transduction system and the aging process. Am. J. Physiol. Cell Physiol. 2007, 292, 670-686.
McKenzie, M., Liolitsa, D., Hanna, M. G., Mitochondrial disease: mutations and mechanisms. Neurochem. Res. 2004, 29, 589-600.
Onyango, I., Khan, S., Miller, B., Swerdlow, R. et al., Mitochondrial genomic contribution tomitochondrial dysfunction in Alzheimer's disease. J. Alzheimers Dis. 2006, 9, 183-193.
Douette, P., Gerkens, P., Navet, R., Leprince, P. et al., Uncoupling protein 1 affects the yeast mitoproteome and oxygen free radical production. Free Rad. Biol. Med. 2006, 40, 303-315.
Mathy, G., Navet, R., Gerkens, P., Leprince, P. et al., Saccharomyces cerevisiae mitoproteome plasticity in response to recombinant alternative ubiquinol oxidase. J. Proteome Res. 2006, 5, 339-348.
Douette, P., Navet, R., Gerkens, P., de Pauw, E. et al., Steatosis-induced proteomic changes in liver mitochondria evidenced by two-dimensional differential in-gel electrophoresis. J. Proteome Res. 2005, 4, 2024-2031.
Navet, R., Mathy, G., Douette, P., Dobson, R. L. et al., Mitoproteome plasticity of rat brown adipocytes in response to cold aclimation. J. Proteome Res. 2007, 6, 25-33.
Wilczynska, Z., Barth, C., Fisher, P. R., Mitochondrial mutations impair signal transduction in Dictyostelium discoideum slugs. Biochem. Biophys. Res. Commun. 1997, 234, 39-43.
Kotsifas, M., Barth, C., de Lozanne, A., Lay, S. T., Fisher, P. R., Chaperonin 60 and mitochondrial disease in Dictyostelium. J. Muscle Res. Cell Motil. 2002, 23, 839-852.
Maeda, Y., Regulation of growth and differentiation in Dictyostelium. Int. Rev. Cytol. 2005, 244, 287-332.
Van Es, S., Wessels, D., Soll, D. R., Borleis, J., Devreotes, P. N., Tortoise, a novel mitochondrial protein, is required for directional responses of Dictyostelium in chemotactic gradients. J. Cell Biol. 2001, 152, 621-632.
Inazu, Y., Chae, S. -C., Maeda, Y., Transient expression of a mitochondria gene cluster including rps4 is essential for the phase-shift of Dictyostelium cells from growth to differentiation. Dev. Genet. 1999, 25, 339-352.
Matsuyama, S. I., Maeda, Y., Involvement of cyanide-resistant respiration in cell-type proportioning during Dictyostelium development. Dev. Biol. 1995, 172, 182-191.
Morita, T., Yamaguchi, H., Amagai, A., Maeda, Y., Involvement of the TRAP-1 homologue, DdTRAP1, in spore differentiation during Dictyostelium development. Exp. Cell Res. 2005, 303, 425-431.
Robert, F., Hevor, T. K., Abnormal organelles in cultured astrocytes are largely enhanced by streptomycin and intensively by gentamicin. Neuroscience 2007, 144, 191-197.
Maeda, Y., A new method for inducing synchronous growth of Dictyostelium discoideum cells using temperature shifts. J. Gen. Microbiol. 1986, 132, 1189-1196.
Meisinger, C., Sommer, T., Pfanner, N., Purification of Saccharomyces cerevisiae mitochondria devoid of microsomal and cytosolic contaminations. Anal. Biochem. 2000, 187, 339-342.
Lowry, O. H., Rosenbrough, N. J., Farr, A. L., Randall, R. J., Protein measurement with the Folin phenol reagent. J. Biol. Chem. 1951, 193, 265-275.
Alban, A., David, S. O., Bjorkesten, L., Andersson, C. et al., A novel experimental design for comparative two-dimensional gel analysis: two-dimensional difference gel electrophoresis incorporating a pooled internal standard. Proteomics 2003, 3, 36-44.
Knowles, M. R., Cervino, S., Skynner, H. A., Hunt, S. P. et al., Multiplex proteomic analysis by two-dimensional differential in-gel electrophoresis. Proteomics 2003, 3, 1162-1171.
Görg, A., Weiss, W., Dunn, M. J., Current two-dimensional electrophoresis technology for proteomics. Proteomics 2004, 4, 3665-3685.
Kajimoto, K., Terada, H., Baba, Y., Shinohara, Y., Essential role of citrate export from mitochondria at early differentiation stage of 3T3-L1 cells for their effective differentiation into fat cells, as revealed by studies using specific inhibitors of mitochondrial di- and tricarboxylate carriers. Mol. Genet. Metab. 2005, 85, 46-53.
Legisa, M., Mattey, M., Changes in primary metabolism leading to citric acid overflow in Aspergillus niger. Biotechnol. Lett. 2007, 29, 181-190.
Ruprich-Robert, G., Zickler, D., Berteaux-Lecellier, V., Velot, Ch., Picard, M., Lack of mitochondrial citrate synthase discloses a new meiotic checkpoint in a strict aerobe. EMBO J. 2002, 23, 6440-6451.
Huang, Y. -Ch., Chen, Y. -H., Lo, S. -R., Lin, Ch. -I. et al., Disruption of the peroxisomal citrate synthase CshA affects cell growth and multicellular development in Dictyostelium discoideum. Mol. Microbiol. 2004, 53, 81-91.
Roos, W., Nanjundiah, V., Malchow, D., Gerisch, G., Amplification of cyclic-AMP signals in aggregating cells of Dictyostelium discoideum. FEBS Lett. 1975, 53, 139-142.
Roos, W., Malchow, D., Gerisch, G., Adenylyl cyclase and the control of cell differentiation in Dictyostelium discoideum. Cell Differ. 1977, 6, 229-239.
Nagayama, K., Itono, S., Yoshida, T., Ishiguro, S. -I. et al., Antisense RNA inhibition of the b subunit of the Dictyostelium discoideum mitochondrial processing peptidase induces the expression of mitochondrial proteins. Biosci. Biotechnol. Biochem. 2008, 72, 1836-1846.
Morita, T., Amagai, A., Maeda, Y., Translocation of the Dictyostelium TRAP1 homologue to mitochondria induces a novel prestarvation response. J. Cell Sci. 2004, 117, 5759-5770.
Yamaguchi, H., Morita, T., Amgai, A., Maeda, Y., Changes in spatial and temporal localization of Dictyostelium homologues of TRAP1 and GRP94 revealed by immunoelectron microscopy. Exp. Cell Res. 2005, 303, 415-424.
Gomer, R. H., Yuen, L. S., Firtel, R. A., A secreted 80 x10 (3) Mr protein mediates sensing of cell density and the onset of development in Dictyostelium. Development 1991, 112, 269-278.
Deery, W. J., Gao, T., Amman, R., Gomer, R. H., A single-cell density-sensing factor stimulates distinct signal transduction pathways through two different receptors. J. Biol. Chem. 2002, 277, 31972-31979.
Deery, W. J., Gomer, R. H., A putative receptor mediating cell-density sensing in Dictyostelium. J. Biol. Chem. 1999, 274, 34476-34482.
Bomblies, L., Biegelmann, E., Döring, V., Gerisch, G. et al., Membrane-enclosed crystals in Dictyostelium discoideum cells, consisting of developmentally regulated proteins with sequence similarities to known esterases. J. Cell. Biol. 1990, 110, 669-679.
Alto, N. M., Soderling, J., Scott, J. D., Rab32 is an A-kinase anchoring protein and participates in mitochondrial dynamics. J. Cell Biol. 2002, 158, 659-668.
Hopper, R. K., Carroll, S., Aponte, A. M., Johnson, D. T. et al., Mitochondria matrix phosphoproteome: effect of extra mitochondrial calcium. Biochemistry 2006, 45, 2524-2536.
Schieke, S. M., Phillips, D., McCoy, J. P., Aponte, A. M. et al., The mammalian target of rapamycin (mTOR) pathway regulates mitochondrial oxygen consumption and oxidative capacity. J. Biol. Chem. 2006, 281, 27643-27652.
Palmisano, G., Sardanelli, A. M., Signorile, A., Papa, S. and Larsen, M. R., The phosphorylation pattern of bovine heart complex I subunits. Proteomics 2007, 7, 1575-1583.
Reinders, J., Wagner, K., Zahedi, R. P., Stojanovski, D. et al., Profiling phosphoproteins of yeast mitochondria reveals a role of phosphorylation in assembly of the ATP synthase. Mol. Cell Proteom. 2007, 6, 1896-1906.
Poot, M., Zhang, Y. Z., Krämer, J. A., Wells, K. S. et al., Analysis of mitochondrial morphology and function with novel fixable fluorescent stains. J. Histochem. Cytochem. 1996, 44, 1363-1372.