Salternamide a suppresses hypoxia-induced accumulation of HIF-1α and induces apoptosis in human colorectal cancer cells

Marine Drugs

Volumn 13, Issue 11, 2015, Pages 6962-6976

  Bach, Duc Hiep ^a   Kim, Seong Hwan ^a   Hong, Ji Young ^a   Park, Hyen Joo ^a   Oh, Dong Chan ^a   Lee, Sang Kook ^a  

^a Seoul National University   (South Korea)

Author keywords

Cell death; HIF 1 ; P42 p44 MAPK; PI3K Akt mTOR; Salternamide A (SA); STAT3

Indexed keywords

ANTINEOPLASTIC AGENT; CYTOTOXIC AGENT; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MAMMALIAN TARGET OF RAPAMYCIN; MICROBIAL PRODUCTS NOT CLASSIFIED ELSEWHERE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; SALTERNAMIDE; STAT3 PROTEIN; UNCLASSIFIED DRUG; AMIDE; POLYENE; SALTERNAMIDE A;

ANTINEOPLASTIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; BIOACCUMULATION; CELL CYCLE REGULATION; CELLULAR DISTRIBUTION; COLORECTAL CANCER CELL LINE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOSE TIME EFFECT RELATION; DRUG MECHANISM; DRUG STRUCTURE; G2 PHASE CELL CYCLE CHECKPOINT; HCT116 CELL LINE; HUMAN; HUMAN CELL; HYPOXIA INDUCED ACCUMULATION; INTRACELLULAR SIGNALING; MOLECULAR DYNAMICS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; REGULATORY MECHANISM; CELL HYPOXIA; COLORECTAL NEOPLASMS; DOSE RESPONSE; DRUG EFFECTS; ISOLATION AND PURIFICATION; M PHASE CELL CYCLE CHECKPOINT; METABOLISM; PATHOLOGY; SIGNAL TRANSDUCTION; STREPTOMYCES; TIME FACTOR; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS; APOPTOSIS; CELL HYPOXIA; CELL LINE, TUMOR; COLORECTAL NEOPLASMS; DOSE-RESPONSE RELATIONSHIP, DRUG; G2 PHASE CELL CYCLE CHECKPOINTS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; M PHASE CELL CYCLE CHECKPOINTS; POLYENES; POLYUNSATURATED ALKAMIDES; SIGNAL TRANSDUCTION; STREPTOMYCES; TIME FACTORS;

EID: 84958963072     PISSN: None     EISSN: 16603397     Source Type: Journal    
DOI: 10.3390/md13116962     Document Type: Article

References (36)

1. Feldser, D.; Agani, F.; Iyer, N.V.; Pak, B.; Ferreira, G.; Semenza, G.L. Reciprocal positive regulation of hypoxia-inducible factor 1alpha and insulin-like growth factor 2. Cancer Res. 1999, 59, 3915-3918.
2. Krishnamachary, B.; Berg-Dixon, S.; Kelly, B.; Agani, F.; Feldser, D.; Ferreira, G.; LaRusch, J.; Iyer, N.; Pak, B.; Taghavi, P.; et al. Regulation of colon carcinoma cell invasion by hypoxia-inducible factor 1. Cancer Res. 2003, 63, 1138-1143.
3. Pugh, C.W.; Ratcliffe, P.J. Regulation of angiogenesis by hypoxia: Role of the HIF system. Nat. Med. 2003, 9, 677-684.
4. Semenza, G.L. Targeting HIF-1 for cancer therapy. Nat. Rev. Cancer 2003, 3, 721-732.
5. Chen, C.; Pore, N.; Behrooz, A.; Ismail-Beigi, F.; Maity, A. Regulation of glut1 mRNA by hypoxia-inducible factor-1. Interaction between H-ras and hypoxia. J. Biol. Chem. 2001, 276, 9519-9525.
6. Semenza, G.L.; Shimoda, L.A.; Prabhakar, N.R. Regulation of gene expression by HIF-1. Novartis Found. Symp. 2006, 272, 2-8.
7. Zhong, H.; de Marzo, A.M.; Laughner, E.; Lim, M.; Hilton, D.A.; Zagzag, D.; Buechler, P.; Isaacs, W.B.; Semenza, G.L.; Simons, J.W. Overexpression of hypoxia-inducible factor 1alpha in common human cancers and their metastases. Cancer Res. 1999, 59, 5830-5835.
8. Talks, K.L.; Turley, H.; Gatter, K.C.; Maxwell, P.H.; Pugh, C.W.; Ratcliffe, P.J.; Harris, A.L. The expression and distribution of the hypoxia-inducible factors HIF-1alpha and HIF-2alpha in normal human tissues, cancers, and tumor-associated macrophages. Am. J. Pathol. 2000, 157, 411-421.
9. Semenza, G.L. HIF-1 and human disease: One highly involved factor. Genes Dev. 2000, 14, 1983-1991.
10. Zhong, H.; Chiles, K.; Feldser, D.; Laughner, E.; Hanrahan, C.; Georgescu, M.M.; Simons, J.W.; Semenza, G.L. Modulation of hypoxia-inducible factor 1alpha expression by the epidermal growth factor/phosphatidylinositol 3-kinase/PTEN/AKT/FRAP pathway in human prostate cancer cells: Implications for tumor angiogenesis and therapeutics. Cancer Res. 2000, 60, 1541-1545.
11. Richard, D.E.; Berra, E.; Gothie, E.; Roux, D.; Pouyssegur, J. p42/p44 mitogen-activated protein kinases phosphorylate hypoxia-inducible factor 1alpha (HIF-1alpha) and enhance the transcriptional activity of HIF-1. J. Biol. Chem. 1999, 274, 32631-32637.
12. Sang, N.; Stiehl, D.P.; Bohensky, J.; Leshchinsky, I.; Srinivas, V.; Caro, J. MAPK signaling up-regulates the activity of hypoxia-inducible factors by its effects on p300. J. Biol. Chem. 2003, 278, 14013-14019.
13. Yee Koh, M.; Spivak-Kroizman, T.R.; Powis, G. HIF-1 regulation: Not so easy come, easy go. Trends Biochem. Sci. 2008, 33, 526-534.
14. Jung, J.E.; Lee, H.G.; Cho, I.H.; Chung, D.H.; Yoon, S.H.; Yang, Y.M.; Lee, J.W.; Choi, S.; Park, J.W.; Ye, S.K.; et al. STAT3 is a potential modulator of HIF-1-mediated VEGF expression in human renal carcinoma cells. FASEB J. 2005, 19, 1296-1298.
15. Jung, J.E.; Kim, H.S.; Lee, C.S.; Shin, Y.J.; Kim, Y.N.; Kang, G.H.; Kim, T.Y.; Juhnn, Y.S.; Kim, S.J.; Park, J.W.; et al. STAT3 inhibits the degradation of HIF-1alpha by pVHL-mediated ubiquitination. Exp. Mol. Med. 2008, 40, 479-485.
16. Kim, S.H.; Shin, Y.; Lee, S.H.; Oh, K.B.; Lee, S.K.; Shin, J.; Oh, D.C. Salternamides A-D from a Halophilic Streptomyces sp. Actinobacterium. J. Nat. Prod. 2015, 78, 836-843.
17. Hansson, L.O.; Friedler, A.; Freund, S.; Rudiger, S.; Fersht, A.R. Two sequence motifs from HIF-1alpha bind to the DNA-binding site of p53. Proc. Natl. Acad. Sci. USA 2002, 99, 10305-10309.
18. Creighton-Gutteridge, M.; Cardellina, J.H., 2nd; Stephen, A.G.; Rapisarda, A.; Uranchimeg, B.; Hite, K.; Denny, W.A.; Shoemaker, R.H.; Melillo, G. Cell type-specific, topoisomerase II-dependent inhibition of hypoxia-inducible factor-1alpha protein accumulation by NSC 644221. Clin. Cancer Res. 2007, 13, 1010-1018.
19. Liu, Y.V.; Baek, J.H.; Zhang, H.; Diez, R.; Cole, R.N.; Semenza, G.L. RACK1 competes with HSP90 for binding to HIF-1alpha and is required for O(2)-independent and HSP90 inhibitor-induced degradation of HIF-1alpha. Mol. Cell 2007, 25, 207-217.
20. Zundel, W.; Schindler, C.; Haas-Kogan, D.; Koong, A.; Kaper, F.; Chen, E.; Gottschalk, A.R.; Ryan, H.E.; Johnson, R.S.; Jefferson, A.B.; et al. Loss of PTEN facilitates HIF-1-mediated gene expression. Genes Dev. 2000, 14, 391-396.
21. Noman, M.Z.; Buart, S.; van Pelt, J.; Richon, C.; Hasmim, M.; Leleu, N.; Suchorska, W.M.; Jalil, A.; Lecluse, Y.; el Hage, F.; et al. The cooperative induction of hypoxia-inducible factor-1 alpha and STAT3 during hypoxia induced an impairment of tumor susceptibility to CTL-mediated cell lysis. J. Immunol. 2009, 182, 3510-3521.
22. Pawlus, M.R.; Wang, L.; Hu, C.J. STAT3 and HIF1alpha cooperatively activate HIF1 target genes in MDA-MB-231 and RCC4 cells. Oncogene 2014, 33, 1670-1679.
23. Shrivastava, A.; Kuzontkoski, P.M.; Groopman, J.E.; Prasad, A. Cannabidiol induces programmed cell death in breast cancer cells by coordinating the cross-talk between apoptosis and autophagy. Mol. Cancer Ther. 2011, 10, 1161-1172.
24. Mack, F.A.; Rathmell, W.K.; Arsham, A.M.; Gnarra, J.; Keith, B.; Simon, M.C. Loss of pVHL is sufficient to cause HIF dysregulation in primary cells but does not promote tumor growth. Cancer Cell 2003, 3, 75-88.
25. Maranchie, J.K.; Vasselli, J.R.; Riss, J.; Bonifacino, J.S.; Linehan, W.M.; Klausner, R.D. The contribution of VHL substrate binding and HIF1-alpha to the phenotype of VHL loss in renal cell carcinoma. Cancer Cell 2002, 1, 247-255.
26. Van den Beucken, T.; Koritzinsky, M.; Wouters, B.G. Translational control of gene expression during hypoxia. Cancer Biol. Ther. 2006, 5, 749-755.
27. Niu, G.; Briggs, J.; Deng, J.; Ma, Y.; Lee, H.; Kortylewski, M.; Kujawski, M.; Kay, H.; Cress, W.D.; Jove, R.; et al. Signal transducer and activator of transcription 3 is required for hypoxia-inducible factor-1alpha RNA expression in both tumor cells and tumor-associated myeloid cells. Mol. Cancer Res. 2008, 6, 1099-1105.
28. Pawlus, M.R.; Wang, L.; Murakami, A.; Dai, G.; Hu, C.J. STAT3 or USF2 contributes to HIF target gene specificity. PLoS ONE 2013, 8, e72358.
29. Huang, W.W.; Ko, S.W.; Tsai, H.Y.; Chung, J.G.; Chiang, J.H.; Chen, K.T.; Chen, Y.C.; Chen, H.Y.; Chen, Y.F.; Yang, J.S. Cantharidin induces G2/M phase arrest and apoptosis in human colorectal cancer colo 205 cells through inhibition of CDK1 activity and caspase-dependent signaling pathways. Int. J. Oncol. 2011, 38, 1067-1073.
30. Doree, M.; Galas, S. The cyclin-dependent protein kinases and the control of cell division. FASEB J. 1994, 8, 1114-1121.
31. Peng, C.Y.; Graves, P.R.; Thoma, R.S.; Wu, Z.; Shaw, A.S.; Piwnica-Worms, H. Mitotic and G2 checkpoint control: Regulation of 14-3-3 protein binding by phosphorylation of Cdc25C on serine-216. Science 1997, 277, 1501-1505.
32. Dai, Y.; Grant, S. New insights into checkpoint kinase 1 in the DNA damage response signaling network. Clin. Cancer Res. 2010, 16, 376-383.
33. Safarzadeh, E.; Sandoghchian Shotorbani, S.; Baradaran, B. Herbal medicine as inducers of apoptosis in cancer treatment. Adv. Pharm. Bull. 2014, 4, 421-427.
34. Dasari, S.; Tchounwou, P.B. Cisplatin in cancer therapy: Molecular mechanisms of action. Eur. J. Pharmacol. 2014, 740, 364-378.
35. Gump, J.M.; Thorburn, A. Autophagy and apoptosis: What is the connection? Trends Cell Biol. 2011, 21, 387-392.
36. Livesey, K.M.; Kang, R.; Vernon, P.; Buchser, W.; Loughran, P.; Watkins, S.C.; Zhang, L.; Manfredi, J.J.; Zeh, H.J., 3rd; Li, L.; et al. p53/HMGB1 complexes regulate autophagy and apoptosis. Cancer Res. 2012, 72, 1996-2005.