The Calcium-Dependent Interaction between S100B and the Mitochondrial AAA ATPase ATAD3A and the Role of This Complex in the Cytoplasmic Processing of ATAD3A

REFERENCES

• Baldisseri, D. M., R. R. Rustandi, Z. Zhang, C. Tang, C. L. Bair, A. Landar, A. Landar, D. B. Zimmer, and D. J. Weber. 1999. 1H, 13C and 15N NMR sequence-specific resonance assignments for rat apo-S100A1(alpha alpha). J. Biomol. NMR 14:91–92.
   PubMedGoogle Scholar
• Barber, K. R., K. A. McClintock, G. A. Jamieson, Jr., R. V. Dimlich, and G. S. Shaw. 1999. Specificity and Zn2+ enhancement of the S100B binding epitope TRTK-12. J. Biol. Chem. 274:1502–1508.
   PubMedGoogle Scholar
• Baudier, J., C. Delphin, D. Grunwald, S. Khochbin, and J. J. Lawrence. 1992. Characterization of the tumor suppressor protein p53 as a protein kinase C substrate and a S100b-binding protein. Proc. Natl. Acad. Sci. U. S. A. 89:11627–11631.
   PubMed Web of Science ®Google Scholar
• Baudier, J., and D. Gerard. 1986. Ions binding to S100 proteins. II. Conformational studies and calcium-induced conformational changes in S100 alpha alpha protein: the effect of acidic pH and calcium incubation on subunit exchange in S100a (alpha beta) protein. J. Biol. Chem. 261:8204–8212.
   PubMedGoogle Scholar
• Baudier, J., N. Glasser, and D. Gerard. 1986. Ions binding to S100 proteins. I. Calcium- and zinc-binding properties of bovine brain S100 alpha alpha, S100a (alpha beta), and S100b (beta beta) protein: Zn2+ regulates Ca2+ binding on S100b protein. J. Biol. Chem. 261:8192–8203.
   PubMedGoogle Scholar
• Bhattacharya, S., E. Large, C. W. Heizmann, B. Hemmings, and W. J. Chazin. 2003. Structure of the Ca2+/S100B/NDR kinase peptide complex: insights into S100 target specificity and activation of the kinase. Biochemistry 42:14416–14426.
   PubMedGoogle Scholar
• Csordas, G., A. P. Thomas, and G. Hajnoczky. 1999. Quasi-synaptic calcium signal transmission between endoplasmic reticulum and mitochondria. EMBO J. 18:96–108.
   PubMed Web of Science ®Google Scholar
• Delaglio, F., S. Grzesiek, G. W. Vuister, G. Zhu, J. Pfeifer, and A. Bax. 1995. NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6:277–293.
   PubMed Web of Science ®Google Scholar
• Deloulme, J. C., N. Assard, G. O. Mbele, C. Mangin, R. Kuwano, and J. Baudier. 2000. S100A6 and S100A11 are specific targets of the calcium- and zinc-binding S100B protein in vivo. J. Biol. Chem. 275:35302–35310.
   PubMedGoogle Scholar
• Deloulme, J. C., T. Janet, D. Au, D. R. Storm, M. Sensenbrenner, and J. Baudier. 1990. Neuromodulin (GAP43): a neuronal protein kinase C substrate is also present in 0-2A glial cell lineage. Characterization of neuromodulin in secondary cultures of oligodendrocytes and comparison with the neuronal antigen. J. Cell Biol. 111:1559–1569.
   PubMedGoogle Scholar
• Deloulme, J. C., E. Raponi, B. J. Gentil, N. Bertacchi, A. Marks, G. Labourdette, and J. Baudier. 2004. Nuclear expression of S100B in oligodendrocyte progenitor cells correlates with differentiation toward the oligodendroglial lineage and modulates oligodendrocytes maturation. Mol. Cell. Neurosci. 27:453–465.
   PubMedGoogle Scholar
• Delphin, C., M. Ronjat, J. C. Deloulme, G. Garin, L. Debussche, Y. Higashimoto, K. Sakaguchi, and J. Baudier. 1999. Calcium-dependent interaction of S100B with the C-terminal domain of the tumor suppressor p53. J. Biol. Chem. 274:10539–10544.
   PubMed Web of Science ®Google Scholar
• Donato, R. 2003. Intracellular and extracellular roles of S100 proteins. Microsc. Res. Tech. 60:540–551.
   PubMed Web of Science ®Google Scholar
• Du, X. J., T. J. Cole, N. Tenis, X. M. Gao, F. Kontgen, B. E. Kemp, and J. Heierhorst. 2002. Impaired cardiac contractility response to hemodynamic stress in S100A1-deficient mice. Mol. Cell. Biol. 22:2821–2829.
   PubMed Web of Science ®Google Scholar
• Dumont, P., J. I. Leu, A. C. Della Pietra III, D. L. George, and M. Murphy. 2003. The codon 72 polymorphic variants of p53 have markedly different apoptotic potential. Nat. Genet. 33:357–365.
   PubMed Web of Science ®Google Scholar
• Eckert, R. L., A. M. Broome, M. Ruse, N. Robinson, D. Ryan, and K. Lee. 2004. S100 proteins in the epidermis. J. Invest. Dermatol. 123:23–33.
   PubMed Web of Science ®Google Scholar
• Erzberger, J. P., and J. M. Berger. 2006. Evolutionary relationships and structural mechanisms of AAA+ proteins. Annu. Rev. Biophys. Biomol. Struct. 35:93–114.
   PubMedGoogle Scholar
• Fernandez-Fernandez, M. R., D. B. Veprintsev, and A. R. Fersht. 2005. Proteins of the S100 family regulate the oligomerization of p53 tumor suppressor. Proc. Natl. Acad. Sci. U. S. A. 102:4735–4740.
   PubMed Web of Science ®Google Scholar
• Gentil, B. J., C. Delphin, G. O. Mbele, J. C. Deloulme, M. Ferro, J. Garin, and J. Baudier. 2001. The giant protein AHNAK is a specific target for the calcium- and zinc-binding S100B protein: potential implications for Ca2+ homeostasis regulation by S100B. J. Biol. Chem. 276:23253–23261.
   PubMed Web of Science ®Google Scholar
• Geuijen, C. A., N. Bijl, R. C. Smit, F. Cox, M. Throsby, T. J. Visser, M. A. Jongeneelen, A. B. Bakker, A. M. Kruisbeek, J. Goudsmit, and J. de Kruif. 2005. A proteomic approach to tumour target identification using phage display, affinity purification and mass spectrometry. Eur. J. Cancer 41:178–187.
   PubMedGoogle Scholar
• Gilquin, B., E. Taillebourg, N. Cherradi, A. Hubstenberger, O. Gay, N. Merle, N. Assard, M. O. Fauvarque, S. Tomohiro, O. Kuge, and J. Baudier. 2010. The AAA+ ATPase ATAD3A controls mitochondrial dynamics at the interface of the inner and outer membranes. Mol. Cell. Biol. 30:1984–1996.
   Google Scholar
• Gires, O., M. Munz, M. Schaffrik, C. Kieu, J. Rauch, M. Ahlemann, D. Eberle, B. Mack, B. Wollenberg, S. Lang, T. Hofmann, W. Hammerschmidt, and R. Zeidler. 2004. Profile identification of disease-associated humoral antigens using AMIDA, a novel proteomics-based technology. Cell. Mol. Life Sci. 61:1198–1207.
   PubMed Web of Science ®Google Scholar
• Hanson, P. I., and S. W. Whiteheart. 2005. AAA+ proteins: have engine, will work. Nat. Rev. Mol. Cell Biol. 6:519–529.
   PubMed Web of Science ®Google Scholar
• He, J., C. C. Mao, A. Reyes, H. Sembongi, M. Di Re, C. Granycome, A. B. Clippingdale, I. M. Fearnley, M. Harbour, A. J. Robinson, S. Reichelt, J. N. Spelbrink, J. E. Walker, and I. J. Holt. 2007. The AAA+ protein ATAD3 has displacement loop binding properties and is involved in mitochondrial nucleoid organization. J. Cell Biol. 176:141–146.
   PubMed Web of Science ®Google Scholar
• Heizmann, C. W., G. Fritz, and B. W. Schafer. 2002. S100 proteins: structure, functions and pathology. Front. Biosci. 7:d1356–d1368.
   PubMed Web of Science ®Google Scholar
• Hoffmann, M., N. Bellance, R. Rossignol, W. J. Koopman, P. H. Willems, E. Mayatepek, O. Bossinger, and F. Distelmaier. 2009. C. elegans ATAD-3 is essential for mitochondrial activity and development. PLoS One 4:e7644.
   PubMedGoogle Scholar
• Hotokezaka, Y., U. Tobben, H. Hotokezaka, K. Van Leyen, B. Beatrix, D. H. Smith, T. Nakamura, and M. Wiedmann. 2002. Interaction of the eukaryotic elongation factor 1A with newly synthesized polypeptides. J. Biol. Chem. 277:18545–18551.
   PubMedGoogle Scholar
• Hubstenberger, A., G. Labourdette, J. Baudier, and D. Rousseau. 2008. ATAD 3A and ATAD 3B are distal 1p-located genes differentially expressed in human glioma cell lines and present in vitro anti-oncogenic and chemoresistant properties. Exp. Cell Res. 314:2870–2883.
   PubMedGoogle Scholar
• Inman, K. G., R. Yang, R. R. Rustandi, K. E. Miller, D. M. Baldisseri, and D. J. Weber. 2002. Solution NMR structure of S100B bound to the high-affinity target peptide TRTK-12. J. Mol. Biol. 324:1003–1014.
   PubMed Web of Science ®Google Scholar
• Kaltimbacher, V., C. Bonnet, G. Lecoeuvre, V. Forster, J. A. Sahel, and M. Corral-Debrinski. 2006. mRNA localization to the mitochondrial surface allows the efficient translocation inside the organelle of a nuclear recoded ATP6 protein. RNA 12:1408–1417.
   PubMedGoogle Scholar
• Kube, E., T. Becker, K. Weber, and V. Gerke. 1992. Protein-protein interaction studied by site-directed mutagenesis. Characterization of the annexin II-binding site on p11, a member of the S100 protein family. J. Biol. Chem. 267:14175–14182.
   PubMedGoogle Scholar
• Lelandais, G., Y. Saint-Georges, C. Geneix, L. Al-Shikhley, G. Dujardin, and C. Jacq. 2009. Spatio-temporal dynamics of yeast mitochondrial biogenesis: transcriptional and post-transcriptional mRNA oscillatory modules. PLoS Comput. Biol. 5:e1000409.
   PubMed Web of Science ®Google Scholar
• Lin, J., M. Blake, C. Tang, D. Zimmer, R. R. Rustandi, D. J. Weber, and F. Carrier. 2001. Inhibition of p53 transcriptional activity by the S100B calcium-binding protein. J. Biol. Chem. 276:35037–35041.
   PubMed Web of Science ®Google Scholar
• Marenholz, I., C. W. Heizmann, and G. Fritz. 2004. S100 proteins in mouse and man: from evolution to function and pathology (including an update of the nomenclature). Biochem. Biophys. Res. Commun. 322:1111–1122.
   PubMed Web of Science ®Google Scholar
• Markowitz, J., A. D. MacKerell, Jr., and D. J. Weber. 2007. A search for inhibitors of S100B, a member of the S100 family of calcium-binding proteins. Mini Rev. Med. Chem. 7:609–616.
   PubMedGoogle Scholar
• Markowitz, J., R. R. Rustandi, K. M. Varney, P. T. Wilder, R. Udan, S. L. Wu, W. D. Horrocks, and D. J. Weber. 2005. Calcium-binding properties of wild-type and EF-hand mutants of S100B in the presence and absence of a peptide derived from the C-terminal negative regulatory domain of p53. Biochemistry 44:7305–7314.
   PubMedGoogle Scholar
• Mbele, G. O., J. C. Deloulme, B. J. Gentil, C. Delphin, M. Ferro, J. Garin, M. Takahashi, and J. Baudier. 2002. The zinc- and calcium-binding S100B interacts and co-localizes with IQGAP1 during dynamic rearrangement of cell membranes. J. Biol. Chem. 277:49998–50007.
   PubMedGoogle Scholar
• Mihara, M., S. Erster, A. Zaika, O. Petrenko, T. Chittenden, P. Pancoska, and U. M. Moll. 2003. p53 has a direct apoptogenic role at the mitochondria. Mol. Cell 11:577–590.
   PubMed Web of Science ®Google Scholar
• Moroz, O. V., E. V. Blagova, A. J. Wilkinson, K. S. Wilson, and I. B. Bronstein. 2009. The crystal structures of human S100A12 in apo form and in complex with zinc: new insights into S100A12 oligomerisation. J. Mol. Biol. 391:536–551.
   PubMed Web of Science ®Google Scholar
• Moroz, O. V., W. Burkitt, H. Wittkowski, W. He, A. Ianoul, V. Novitskaya, J. Xie, O. Polyakova, I. K. Lednev, A. Shekhtman, P. J. Derrick, P. Bjoerk, D. Foell, and I. B. Bronstein. 2009. Both Ca2+ and Zn2+ are essential for S100A12 protein oligomerization and function. BMC Biochem. 10:11.
   PubMedGoogle Scholar
• Nielsen, J. A., D. Maric, P. Lau, J. L. Barker, and L. D. Hudson. 2006. Identification of a novel oligodendrocyte cell adhesion protein using gene expression profiling. J. Neurosci. 26:9881–9891.
   PubMedGoogle Scholar
• Okada, M., T. Hatakeyama, H. Itoh, N. Tokuta, H. Tokumitsu, and R. Kobayashi. 2004. S100A1 is a novel molecular chaperone and a member of the Hsp70/Hsp90 multichaperone complex. J. Biol. Chem. 279:4221–4233.
   PubMed Web of Science ®Google Scholar
• Pathmanathan, S., S. F. Elliott, S. McSwiggen, B. Greer, P. Harriott, G. B. Irvine, and D. J. Timson. 2008. IQ motif selectivity in human IQGAP1: binding of myosin essential light chain and S100B. Mol. Cell. Biochem. 318:43–51.
   PubMedGoogle Scholar
• Raponi, E., F. Agenes, C. Delphin, N. Assard, J. Baudier, C. Legraverend, and J. C. Deloulme. 2007. S100B expression defines a state in which GFAP-expressing cells lose their neural stem cell potential and acquire a more mature developmental stage. Glia 55:165–177.
   PubMed Web of Science ®Google Scholar
• Rizzuto, R., P. Pinton, W. Carrington, F. S. Fay, K. E. Fogarty, L. M. Lifshitz, R. A. Tuft, and T. Pozzan. 1998. Close contacts with the endoplasmic reticulum as determinants of mitochondrial Ca2+ responses. Science 280:1763–1766.
   PubMed Web of Science ®Google Scholar
• Rustandi, R. R., D. M. Baldisseri, and D. J. Weber. 2000. Structure of the negative regulatory domain of p53 bound to S100B(betabeta). Nat. Struct. Biol. 7:570–574.
   PubMedGoogle Scholar
• Rustandi, R. R., A. C. Drohat, D. M. Baldisseri, P. T. Wilder, and D. J. Weber. 1998. The Ca(2+)-dependent interaction of S100B(beta beta) with a peptide derived from p53. Biochemistry 37:1951–1960.
   PubMed Web of Science ®Google Scholar
• Santamaria-Kisiel, L., A. C. Rintala-Dempsey, and G. S. Shaw. 2006. Calcium-dependent and -independent interactions of the S100 protein family. Biochem. J. 396:201–214.
   PubMed Web of Science ®Google Scholar
• Scotto, C., J. C. Deloulme, D. Rousseau, E. Chambaz, and J. Baudier. 1998. Calcium and S100B regulation of p53-dependent cell growth arrest and apoptosis. Mol. Cell. Biol. 18:4272–4281.
   PubMedGoogle Scholar
• Scotto, C., C. Delphin, J. C. Deloulme, and J. Baudier. 1999. Concerted regulation of wild-type p53 nuclear accumulation and activation by S100B and calcium-dependent protein kinase C. Mol. Cell. Biol. 19:7168–7180.
   PubMedGoogle Scholar
• Shimamoto, S., M. Takata, M. Tokuda, F. Oohira, H. Tokumitsu, and R. Kobayashi. 2008. Interactions of S100A2 and S100A6 with the tetratricopeptide repeat proteins, Hsp90/Hsp70-organizing protein and kinesin light chain. J. Biol. Chem. 283:28246–28258.
   PubMedGoogle Scholar
• Spiechowicz, M., A. Zylicz, P. Bieganowski, J. Kuznicki, and A. Filipek. 2007. Hsp70 is a new target of Sgt1—an interaction modulated by S100A6. Biochem. Biophys. Res. Commun. 357:1148–1153.
   PubMed Web of Science ®Google Scholar
• van Dieck, J., M. R. Fernandez-Fernandez, D. B. Veprintsev, and A. R. Fersht. 2009. Modulation of the oligomerization state of p53 by differential binding of proteins of the S100 family to p53 monomers and tetramers. J. Biol. Chem. 284:13804–13811.
   PubMed Web of Science ®Google Scholar
• van Dieck, J., D. P. Teufel, A. M. Jaulent, M. R. Fernandez-Fernandez, T. J. Rutherford, A. Wyslouch-Cieszynska, and A. R. Fersht. 2009. Posttranslational modifications affect the interaction of S100 proteins with tumor suppressor p53. J. Mol. Biol. 394:922–930.
   PubMed Web of Science ®Google Scholar
• Wilder, P. T., J. Lin, C. L. Bair, T. H. Charpentier, D. Yang, M. Liriano, K. M. Varney, A. Lee, A. B. Oppenheim, S. Adhya, F. Carrier, and D. J. Weber. 2006. Recognition of the tumor suppressor protein p53 and other protein targets by the calcium-binding protein S100B. Biochim. Biophys. Acta 1763:1284–1297.
   PubMed Web of Science ®Google Scholar
• Wright, N. T., B. L. Prosser, K. M. Varney, D. B. Zimmer, M. F. Schneider, and D. J. Weber. 2008. S100A1 and calmodulin compete for the same binding site on ryanodine receptor. J. Biol. Chem. 283:26676–26683.
   PubMedGoogle Scholar
• Xiong, Z., D. O'Hanlon, L. E. Becker, J. Roder, J. F. MacDonald, and A. Marks. 2000. Enhanced calcium transients in glial cells in neonatal cerebellar cultures derived from S100B null mice. Exp. Cell Res. 257:281–289.
   PubMed Web of Science ®Google Scholar
• Yam, A. Y., Y. Xia, H. T. Lin, A. Burlingame, M. Gerstein, and J. Frydman. 2008. Defining the TRiC/CCT interactome links chaperonin function to stabilization of newly made proteins with complex topologies. Nat. Struct. Mol. Biol. 15:1255–1262.
   PubMed Web of Science ®Google Scholar
• Zhou, Z., and Y. Li. 2009. Molecular dynamics simulation of S100B protein to explore ligand blockage of the interaction with p53 protein. J. Comput. Aided Mol. Des. 23:705–714.
   PubMedGoogle Scholar