Dictyostelium differentiation-inducing factor-1 binds to mitochondrial malate dehydrogenase and inhibits its activity

Journal of Pharmacological Sciences

Volumn 112, Issue 3, 2010, Pages 320-326

  Matsuda, Tomoko ^a   Takahashi Yanaga, Fumi ^a   Yoshihara, Tatsuya ^a   Maenaka, Katsumi ^b   Watanabe, Yutaka ^c   Miwa, Yoshikazu ^a   Morimoto, Sachio ^a   Kubohara, Yuzuru ^d   Hirata, Masato ^b   Sasaguri, Toshiyuki ^a  

^a KYUSHU UNIVERSITY   (Japan)

^b KYUSHU UNIVERSITY   (Japan)

^c EHIME UNIVERSITY   (Japan)

^d GUNMA UNIVERSITY   (Japan)

Author keywords

ATP content; Cell proliferation; Differentiation inducing factor; Energy production; Mitochondrial malate dehydrogenase (mMDH)

Indexed keywords

2 METHOXY DIFFERENTIATION INDUCING FACTOR 1; 6 METHOXY DIFFERENTIATION INDUCING FACTOR 3; ADENOSINE TRIPHOSPHATE; ANTINEOPLASTIC AGENT; BETA CATENIN; DIFFERENTIATION INDUCING FACTOR; DIFFERENTIATION INDUCING FACTOR 1; DIFFERENTIATION INDUCING FACTOR 3; MALATE DEHYDROGENASE; UNCLASSIFIED DRUG; WNT PROTEIN;

ARTICLE; CELL ENERGY; CELL PROLIFERATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DICTYOSTELIUM DISCOIDEUM; DRUG MECHANISM; DRUG SCREENING; DRUG STRUCTURE; DRUG SYNTHESIS; ENZYME ACTIVITY; ENZYME INHIBITION; FEMALE; HELA CELL; HUMAN; HUMAN CELL; MITOCHONDRIAL MEMBRANE; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN MODIFICATION; SIGNAL TRANSDUCTION;

EID: 77950660859     PISSN: 13478613     EISSN: 13478648     Source Type: Journal    
DOI: 10.1254/jphs.09348FP     Document Type: Article

References (26)

1. Morris HR, Taylor GW, Masento MS, Jermyn KA, Kay RR. Chemical structure of the morphogen differentiation inducing factor from Dictyostelium discoideum. Nature. 1987;328: 811-814.
2. Morris HR, Masento MS, Taylor GW, Jermyn KA, Kay RR. Structure elucidation of two differentiation inducing factors (DIF-2 and DIF-3) from the cellular slime mould Dictyostelium discoideum. Biochem J. 1988;249:903-906.
3. Wurster B, Kay RR. New roles for DIF? Effects on early development in Dictyostelium. Dev Biol. 1990;140:189-195.
4. Morandini P, Offer J, Traynor D, Nayler O, Neuhaus D, Taylor GW, et al. The proximal pathway of metabolism of the chlorinated signal molecule differentiation-inducing factor-1 (DIF-1) in the cellular slime mould Dictyostelium. Biochem J. 1995:306: 735-743.
5. Kubohara Y. DIF-1, Putative morphogen of D. discoideum, suppresses cell growth and promotes retinoic acid-induced cell differentiation in HL-60. Biochem Biophys Res Commun. 1997;236: 418-422.
6. Kubohara Y. Effect of differentiation-inducing factors of Dictyostelium discoideum on human leukemia K562 cells: DIF-3 is the most potent anti-leukemic agent. Eur J Pharmacol. 1999;381: 57-62.
7. Gokan N, Kikuchi H, Nakamura K, Oshima Y, Hosaka K, Kubohara Y. Structural requirements of Dictyostelium differentiation- inducing factors for their stalk-cell-inducing activity in Dictyostelium cells and anti-proliferative activity in K562 human leukemic cells. Biochem Pharm. 2005;70:676-685.
8. Miwa Y, Sasaguri T, Kosaka C, Taba Y, Ishida A, Abumiya T, et al. Differentiation-inducing factor-1, a morphogen of dictyostelium, induces G(1) arrest and differentiation of vascular smooth muscle cells. Circ Res. 2000;86:68-75.
9. Takahashi-Yanaga F, Taba Y, Miwa Y, Kubohara Y, Watanabe Y, Hirata M, et al. Dictyostelium differentiation-inducing factor-3 activates glycogen synthase kinase-3β and degrades cyclin D1 in mammalian cells. J Biol Chem. 2003; 278:9663-9670.
10. Yasmin T, Takahashi-Yanaga F, Mori J, Miwa Y, Hirata M, Watanabe Y, et al. Differentiation-inducing factor-1 suppresses gene expression of cyclin D1 in tumor cells. Biochem Biophys Res Commun. 2005;338:903-909.
11. Mori J, Takahashi-Yanaga F, Miwa Y, Watanabe Y, Hirata M, Morimoto S, et al. Differentiation-inducing factor-1 induces cyclin D1 degradation through the phosphorylation of Thr 286 in squamous cell carcinoma. Exp Cell Res. 2005;310:426-433.
12. Takahashi-Yanaga F, Mori J, Matsuzaki E, Watanabe Y, Hirata M, Miwa Y, et al. Involvement of GSK-3β and DYRK1B in differentiation- inducing factor-3-induced phosphorylation of cyclin D1 in HeLa cells. J Biol Chem. 2006;281:38489-38497.
13. Matsuzaki E, Takahashi-Yanaga F, Miwa Y, Hirata M, Watanabe Y, Sato N, et al. Differentiation-inducing factor-1 alters canonical Wnt signaling and suppresses alkaline phosphatase expression in osteoblast-like cell lines. J Bone Miner Res. 2006;21:1307-1316.
14. Barker N, Clevers H. Mining the Wnt pathway for cancer therapeutics. Nat Rev Drug Discov. 2006;5:997-1014.
15. Fodde R, Brabletz T. Wnt/β-catenin signaling in cancer stemness and malignant behavior. Curr Opin Cell Biol. 2007;19:150-158.
16. Shimizu K, Murata T, Tagawa T, Takahashi K, Ishikawa R, Abe Y, et al. Calmodulin-dependent cyclic nucleotide phosphatase (PDE1) is a pharmacological target of differentiation-inducing factor-1, an antitumor agent isolated from Dictyostelium. Cancer Res. 2004;64:2568-2571.
17. Goward CR, Nicholls DJ. Malate dehydrogenase: a model for structure, evolution, and catalysis. Protein Sci. 1994;3:1883-1888.
18. LaNoue KF, Bryla J, Bassett DJ. Energy-driven aspartate efflux from heart and liver mitochondria. J Biol Chem. 1974;249:7514-7521.
19. Joh T, Takeshima H, Tsuzuk T, Setoyama C, Shimada K, Tanase S, et al. Cloning and sequence analysis of cDNAs encoding mammalian cytosolic malate dehydrogenase. Comparison of the amino acid sequences of mammalian and bacterial malate dehydrogenase. J Biol Chem. 1987;262:15127-15131.
20. Masento MS, Morris HR, Taylor G, Johnson SJ, Skapski AC, Kay RR. Differentiation-inducing factor from the slime mould Dictyostelium discoideum and its analogues. Synthesis, structure and biological activity. Biochem J. 1988;256:23-28.
21. Matsumoto M, Hatakeyama S, Oyamada K, Oda Y, Nishimura T, Nakayama KI. Large-scale analysis of the human ubiquitin-related proteome. Proteomics. 2005;5:4145-4151.
22. Lu Q-W, Morimoto S, Harada K, Du C-K, Takahashi-Yanaga F, Miwa Y, et al. Cardiac troponin T mutation R141W found in dilated cardiomyopathy stabilizes the troponin T-tropomyosin interaction and causes Ca2+ deswnsitization. J Mol Cell Cardiol. 2003;35:1421-1427.
23. Omata W, Shibata H, Nagasawa M, Kojima I, Kikuchi H, Oshima Y, et al. Dictyostelium differentiation-inducing factor-1 induces glucose transporter 1 translocation and promotes glucose uptake in mammalian cells. FEBS J. 2007;274:3392-3404.
24. Warburg O. On the origin of cancer cells. Science. 1956;123: 309-314.
25. Shaw RJ. Glucose metabolism and cancer. Curr Opin Cell Biol. 2006;18:598-608.
26. Ganapathy V, Thangaraju M, Prasad PD. Nutrient transporters in cancer: relevance to Warburg hypothesis and beyond. Pharmacol Ther. 2009;121:29-40.