Towards the small and the beautiful: A small dibromotyrosine derivative from pseudoceratina sp. sponge exhibits potent apoptotic effect through targeting IKK/NFκB signaling pathway

Marine Drugs

Volumn 11, Issue 9, 2013, Pages 3168-3185

  Su, Jui Hsin ^a,b   Chen, Yu Cheng ^a   El Shazly, Mohamed ^c,d   Du, Ying Chi ^c   Su, Chiang Wen ^b   Tsao, Chia Wei ^a   Liu, Li Lian ^e   Chou, Yalan ^e   Chang, Wen Been ^a   Su, Yin Di ^a,e   Chiang, Michael Y ^e   Yeh, Yao Tsung ^f   Lu, Mei Chin ^a,b  

^a NATIONAL MUSEUM OF MARINE BIOLOGY AND AQUARIUM   (Taiwan)

^b NATIONAL DONG HWA UNIVERSITY   (Taiwan)

^c KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

^d African Union Organization St Abbassia   (Egypt)

^e NATIONAL SUN YAT SEN UNIVERSITY   (Taiwan)

^f FOOYIN UNIVERSITY   (Taiwan)

Author keywords

Apoptosis; Dibromotyrosine; Mitochondrial dysfunction; Oxidative stress; Topoisomerase

Indexed keywords

ACETONITRILE; ACETYLCYSTEINE; CASPASE 3; CASPASE 9; DIBROMOTYROSINE; DNA TOPOISOMERASE (ATP HYDROLYSING); ETOPOSIDE; I KAPPA B KINASE ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIPOCORTIN 5; REACTIVE OXYGEN METABOLITE; SCAVENGER; TYROSINE DERIVATIVE; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CATALYSIS; CELL FREE SYSTEM; CHEMICAL STRUCTURE; CHRONIC MYELOID LEUKEMIA; CONTROLLED STUDY; CYTOTOXICITY; DRUG MECHANISM; ENZYME ACTIVATION; FLOW CYTOMETRY; LEUKEMIA; MITOCHONDRIAL MEMBRANE POTENTIAL; NONHUMAN; OXIDATIVE STRESS; PROTEIN CLEAVAGE; PROTEIN TARGETING; PSEUDOCERATINA; SPONGE (PORIFERA);

PSEUDOCERATINA;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; CASPASE 3; CASPASE 9; CELL LINE, TUMOR; DNA TOPOISOMERASES, TYPE II; HELA CELLS; HUMANS; K562 CELLS; MCF-7 CELLS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; NF-KAPPA B; OXIDATIVE STRESS; PHOSPHATIDYLINOSITOL 3-KINASES; PORIFERA; PROTO-ONCOGENE PROTEINS C-AKT; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION;

EID: 84885082259     PISSN: None     EISSN: 16603397     Source Type: Journal    
DOI: 10.3390/md11093168     Document Type: Article

References (49)

1. Kunze, K.; Niemann, H.; Ueberlein, S.; Schulze, R.; Ehrlich, H.; Brunner, E.; Proksch, P.; Pee, K.H. Brominated skeletal components of the marine demosponges, Aplysina cavernicola and Ianthella basta: Analytical and biochemical investigations. Mar. Drugs 2013, 11, 1271-1287.
2. Ebada, S.S.; Lin, W.; Proksch, P. Bioactive sesterterpenes and triterpenes from marine sponges: Occurrence and pharmacological significance. Mar. Drugs 2010, 8, 313-346.
3. 13C NMR spectral data. Mar. Drugs 2011, 9, 2316-2368.
4. Isidori, A. Clinical experimental evaluation of the effect of dibromotyrosine on thyroid function. Int. J. Clin. Pharmacol. Biopharm. 1978, 16, 180-182.
5. Galeano, E.; Thomas, O.P.; Robledo, S.; Munoz, D.; Martinez, A. Antiparasitic bromotyrosine derivatives from the marine sponge Verongula rigida. Mar. Drugs 2011, 9, 1902-1913.
6. Hinterding, K.; Knebel, A.; Herrlich, P.; Waldmann, H. Synthesis and biological evaluation of aeroplysinin analogues: A new class of receptor tyrosine kinase inhibitors. Bioorg. Med. Chem. 1998, 6, 1153-1162.
7. Cordoba, R.; Tormo, N.S.; Medarde, A.F.; Plumet, J. Antiangiogenic versus cytotoxic activity in analogues of aeroplysinin-1. Bioorg. Med. Chem. 2007, 15, 5300-5315.
8. Martinez-Poveda, B.; Garcia-Vilas, J.A.; Cardenas, C.; Melgarejo, E.; Quesada, A.R.; Medina, M.A. The brominated compound aeroplysinin-1 inhibits proliferation and the expression of key pro-inflammatory molecules in human endothelial and monocyte cells. PLoS One 2013, 8, e55203.
9. Teeyapant, R.; Woerdenbag, H.J.; Kreis, P.; Hacker, J.; Wray, V.; Witte, L.; Proksch, P. Antibiotic and cytotoxic activity of brominated compounds from the marine sponge Verongia aerophoba. Z. Naturforsch C 1993, 48, 939-945.
10. Martinez-Poveda, B.; Rodriguez-Nieto, S.; Garcia-Caballero, M.; Medina, M.A.; Quesada, A.R. The antiangiogenic compound aeroplysinin-1 induces apoptosis in endothelial cells by activating the mitochondrial pathway. Mar. Drugs 2012, 10, 2033-2046.
11. Sallam, A.A.; Ramasahayam, S.; Meyer, S.A.; El Sayed, K.A. Design, synthesis, and biological evaluation of dibromotyrosine analogues inspired by marine natural products as inhibitors of human prostate cancer proliferation, invasion, and migration. Bioorg. Med. Chem. 2010, 18, 7446-7457.
12. 13C NMR assignment of cyclohexadienyl rings in bromotyrosine-derived metabolites from marine sponges. Magn. Reson. Chem. 2012, 50, 749-754.
13. Hillgren, J.M.; Oberg, C.T.; Elofsson, M. Syntheses of pseudoceramines A-D and a new synthesis of spermatinamine, bromotyrosine natural products from marine sponges. Org. Biomol. Chem. 2012, 10, 1246-1254.
14. Buchanan, M.S.; Carroll, A.R.; Fechner, G.A.; Boyle, A.; Simpson, M.; Addepalli, R.; Avery, V.M.; Hooper, J.N.; Cheung, T.; Chen, H.; et al. Aplysamine 6, an alkaloidal inhibitor of isoprenylcysteine carboxyl methyltransferase from the sponge Pseudoceratina sp. J. Nat. Prod. 2008, 71, 1066-1067.
15. Kon, Y.; Kubota, T.; Shibazaki, A.; Gonoi, T.; Kobayashi, J. Ceratinadins A-C, new bromotyrosine alkaloids from an Okinawan marine sponge Pseudoceratina sp. Bioorg. Med. Chem. Lett. 2010, 20, 4569-4572.
16. Lebouvier, N.; Jullian, V.; Desvignes, I.; Maurel, S.; Parenty, A.; Dorin-Semblat, D.; Doerig, C.; Sauvain, M.; Laurent, D. Antiplasmodial activities of homogentisic acid derivative protein kinase inhibitors isolated from a Vanuatu marine sponge Pseudoceratina sp. Mar. Drugs 2009, 7, 640-653.
17. Herter-Sprie, G.S.; Chen, S.; Hopker, K.; Reinhardt, H.C. Synthetic lethality as a new concept for the treatment of cancer. Ger. Med. Wkly. 2011, 136, 1526-1530.
18. Du, Y.C.; Chang, F.R.; Wu, T.Y.; Hsu, Y.M.; El-Shazly, M.; Chen, C.F. Sung, P.J.; Lin, Y.Y.; Lin, Y.H.; Wu, Y.C.; et al. Antileukemia component, dehydroeburicoic acid from Antrodia camphorata induces DNA damage and apoptosis in vitro and in vivo models. Phytomedicine 2012, 19, 788-796.
19. Nitiss, J.L. Targeting DNA topoisomerase II in cancer chemotherapy. Nat. Rev. Cancer 2009, 9, 338-350.
20. Sinha, K.; Das, J.; Pal, P.B.; Sil, P.C. Oxidative stress: The mitochondria-dependent and mitochondria-independent pathways of apoptosis. Arch. Toxicol. 2013, 87, 1157-1180.
21. Hutti, J.E.; Pfefferle, A.D.; Russell, S.C.; Sircar, M.; Perou, C.M.; Baldwin, A.S. Oncogenic PI3K mutations lead to NF-kappaB-dependent cytokine expression following growth factor deprivation. Cancer Res. 2012, 72, 3260-3269.
22. Kim, H.J.; Hawke, N.; Baldwin, A.S. NF-kappaB and IKK as therapeutic targets in cancer. Cell Death Differ. 2006, 13, 738-747.
23. Li, X.; Abdel-Mageed, A.B.; Mondal, D.; Kandil, E. The nuclear factor kappa-B signaling pathway as a therapeutic target against thyroid cancers. Thyroid 2013, 23, 209-218.
24. Lampiasi, N.; Azzolina, A.; Umezawa, K.; Montalto, G.; McCubrey, J.A.; Cervello, M. The novel NF-kappaB inhibitor DHMEQ synergizes with celecoxib to exert antitumor effects on human liver cancer cells by a ROS-dependent mechanism. Cancer Lett. 2012, 322, 35-44.
25. Madonna, G.; Ullman, C.D.; Gentilcore, G.; Palmieri, G.; Ascierto, P.A. NF-kappaB as potential target in the treatment of melanoma. J. Transl. Med. 2012, 10, 53.
26. Martelli, A.M.; Tabellini, G.; Bressanin, D.; Ognibene, A.; Goto, K.; Cocco, L.; Evangelisti, C. The emerging multiple roles of nuclear Akt. Biochim. Biophys. Acta 2012, 1823, 2168-2178.
27. Sawyers, C.L. Chronic myeloid leukemia. N. Engl. J. Med. 1999, 340, 1330-1340.
28. Rowley, J.D. Letter: A new consistent chromosomal abnormality in chronic myelogenous leukaemia identified by quinacrine fluorescence and Giemsa staining. Nature 1973, 243, 290-293.
29. Druker, B.J.; Guilhot, F.; O'Brien, S.G.; Gathmann, I.; Kantarjian, H.; Gattermann, N.; Deininger, M.W.; Silver, R.T.; Goldman, J.M.; Stone, R.M.; et al. Five-year follow-up of patients receiving imatinib for chronic myeloid leukemia. N. Engl. J. Med. 2006, 355, 2408-2417.
30. Ibrahim, A.R.; Eliasson, L.; Apperley, J.F.; Milojkovic, D.; Bua, M.; Szydlo, R.; Mahon, F.X.; Kozlowski, K.; Paliompeis, C.; Foroni, L.; et al. Poor adherence is the main reason for loss of CCyR and imatinib failure for chronic myeloid leukemia patients on long-term therapy. Blood 2011, 117, 3733-3736.
31. Georgiades, S.N.; Clardy, J. Total synthesis of psammaplysenes A and B, naturally occurring inhibitors of FOXO1a nuclear export. Org. Lett. 2005, 7, 4091-4094.
32. Myatt, S.S.; Brosens, J.J.; Lam, E.W. Sense and sensitivity: FOXO and ROS in cancer development and treatment. Antioxid. Redox Signal. 2011, 14, 675-687.
33. Greer, E.L.; Brunet, A. FOXO transcription factors at the interface between longevity and tumor suppression. Oncogene 2005, 24, 7410-7425.
34. Kryston, T.B.; Georgiev, A.B.; Pissis, P.; Georgakilas, A.G. Role of oxidative stress and DNA damage in human carcinogenesis. Mutat. Res. 2011, 711, 193-201.
35. Downward, J. PI 3-kinase, Akt and cell survival. Semin. Cell Dev. Biol. 2004, 15, 177-182.
36. Blanco-Aparicio, C.; Renner, O.; Leal, J.F.; Carnero, A. PTEN, more than the AKT pathway. Carcinogenesis 2007, 28, 1379-1386.
37. Ahn, J.; Won, M.; Choi, J.H.; Kim, Y.S.; Jung, C.R.; Im, D.S.; Kyun, M.L.; Lee, K.; Song, K.B.; Chung, K.S. Reactive oxygen species-mediated activation of the Akt/ASK1/p38 signaling cascade and p21 downregulation are required for shikonin-induced apoptosis. Apoptosis 2013, 18, 870-881.
38. Szanto, A.; Hellebrand, E.E.; Bognar, Z.; Tucsek, Z.; Szabo, A.; Gallyas, F. Jr.; Sumegi, B.; Varbiro, G. PARP-1 inhibition-induced activation of PI-3-kinase-Akt pathway promotes resistance to taxol. Biochem. Pharmacol. 2009, 77, 1348-1357.
39. Xing, H.; Weng, D.; Chen, G.; Tao, W.; Zhu, T.; Yang, X.; Meng, L.; Wang, S.; Lu, Y.; Ma, D. Activation of fibronectin/PI-3K/Akt2 leads to chemoresistance to docetaxel by regulating survivin protein expression in ovarian and breast cancer cells. Cancer Lett. 2008, 261, 108-119.
40. Ziegelbauer, K.; Gantner, F.; Lukacs, N.W.; Berlin, A.; Fuchikami, K.; Niki, T.; Sakai, K.; Inbe, H.; Takeshita, K.; Ishimori, M.; Komura, H.; Murata, T.; Lowinger, T.; Bacon, K.B. A selective novel low-molecular-weight inhibitor of IkappaB kinase-beta (IKK-beta) prevents pulmonary inflammation and shows broad anti-inflammatory activity. Br. J. Pharmacol. 2005, 145, 178-192.
41. Castro, A.C.; Dang, L.C.; Soucy, F.; Grenier, L.; Mazdiyasni, H.; Hottelet, M.; Parent, L.; Pien, C.; Palombella, V.; Adams, J. Novel IKK inhibitors: Beta-Carbolines. Bioorg. Med. Chem. Lett. 2003, 13, 2419-2422.
42. Kishore, N.; Sommers, C.; Mathialagan, S.; Guzova, J.; Yao, M.; Hauser, S.; Huynh, K.; Bonar, S.; Mielke, C.; Albee, L.; et al. A selective IKK-2 inhibitor blocks NF-kappa B-dependent gene expression in interleukin-1 beta-stimulated synovial fibroblasts. J. Biol. Chem. 2003, 278, 32861-32871.
43. Christopher, J.A.; Avitabile, B.G.; Bamborough, P.; Champigny, A.C.; Cutler, G.J.; Dyos, S.L.; Grace, K.G.; Kerns, J.K.; Kitson, J.D.; Mellor, G.W.; et al. The discovery of 2-amino-3,5-diarylbenzamide inhibitors of IKK-alpha and IKK-beta kinases. Bioorg. Med. Chem. Lett. 2007, 17, 3972-3977.
44. Gamble, C.; McIntosh, K.; Scott, R.; Ho, K.H.; Plevin, R.; Paul, A. Inhibitory kappa B Kinases as targets for pharmacological regulation. Br. J. Pharmacol. 2012, 165, 802-819.
45. Nam, S.Y.; Ko, Y.S.; Jung, J.; Yoon, J.; Kim, Y.H.; Choi, Y.J.; Park, J.W.; Chang, M.S.; Kim, W.H.; Lee, B.L. A hypoxia-dependent upregulation of hypoxia-inducible factor-1 by nuclear factor-kappa B promotes gastric tumour growth and angiogenesis. Br. J. Cancer 2011, 104, 166-174.
46. Kuphal, S.; Winklmeier, A.; Warnecke, C.; Bosserhoff, A.K. Constitutive HIF-1 activity in malignant melanoma. Eur. J. Cancer 2010, 46, 1159-1169.
47. Capon, R.; Macleod, J. Two epimeric dibromo nitriles from the australian sponge Aplysina laevis. Aust. J. Chem. 1987, 40, 341-346.
48. Santalova, E.A.; Denisenko, V.A.; Glazunov, V.P.; Kalinovskii, A.I.; Anastyuk, S.D.; Stonik, V.A. Dibromotyrosine derivatives from the ethanol extract of the marine sponge Aplysina sp.: Structures, transformations and origin. Russian Chem. Bull. 2011, 60, 570-580.
49. Huang, K.-J.; Chen, Y.-C.; El-Shazly, M.; Du, Y.-C.; Su, J.-H.; Tsao, C.-W.; Yen, W.-H.; Chang, W.-B.; Su, Y.-D.; Yeh, Y.-T.; et al. 5-Episinuleptolide acetate, a norcembranoidal diterpene from the formosan soft coral Sinularia sp., induces leukemia cell apoptosis through Hsp90 inhibition. Molecules 2013, 18, 2924-2933.