Marine natural products as inhibitors of hypoxic signaling in tumors

Phytochemistry Reviews

Volumn 8, Issue 2, 2009, Pages 415-429

  Nagle, Dale G ^a   Zhou, Yu Dong ^a  

^a UNIVERSITY OF MISSISSIPPI   (United States)

Author keywords

Cellular signaling; Crinoids; Gene expression; HIF 1 inhibitors; Hypoxia inducible factor 1; Marine natural products; Molecular targeted antitumor agents; Sponges; Transcription factor; Tumor hypoxia; Tunicates

Indexed keywords

3 EPI SODWANONE K; 7 HYDROXYNEOLAMELLARIN A; ANTINEOPLASTIC AGENT; DEHYDRODIDEMNIN B; DIACARNOXIDE B; FUROSPONGOLIDE; HYPOXIA INDUCIBLE FACTOR 1; LATRUNCULIN A; NATURAL PRODUCT; REACTIVE OXYGEN METABOLITE; SODWANONE A; SODWANONE T; SODWANONE V; STRONGYLOPHORINE 2; STRONGYLOPHORINE 3; STRONGYLOPHORINE 8; UNCLASSIFIED DRUG; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 1;

ADAPTATION; ADVANCED CANCER; ALGA; ANAPLASTIC THYROID CARCINOMA; ANTIANGIOGENIC ACTIVITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER PATIENT; CANCER RESISTANCE; CANCER STAGING; CANCER SURVIVAL; CELL HYPOXIA; DRUG ISOLATION; DRUG MECHANISM; DRUG MEGADOSE; DRUG POTENCY; ECHINODERM; GENE EXPRESSION REGULATION; GENE INDUCTION; GENE TARGETING; HUMAN; HYPOXIA; LOW DRUG DOSE; MARINE SPECIES; METASTASIS; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SOLID TUMOR; SPONGE (PORIFERA); STRUCTURE ACTIVITY RELATION; THYROID CARCINOMA; TUMOR CELL; TUMOR GROWTH; VASCULARIZATION;

ALGAE; INVERTEBRATA; PELMATOZOA; UROCHORDATA;

EID: 67651152631     PISSN: 15687767     EISSN: 1572980X     Source Type: Journal    
DOI: 10.1007/s11101-009-9120-1     Document Type: Article

References (95)

1. D Ahuja MD Vera BV Sir Deshpande 2000 Inhibition of protein synthesis by didemnin B: how EF-1α mediates inhibition of translocation Biochemistry 39 4339 4346 10.1021/bi992202h
2. H Axelson E Fredlund M Ovenberger 2005 Hypoxia-induced dedifferentiation of tumor cells-a mechanism behind heterogeneity and aggressiveness of solid tumors Semin Cell Dev Biol 16 554 563 10.1016/j.semcdb.2005.03.007
3. SM Baby A Roy S Lahiri 2005 Role of mitochondria in the regulation of hypoxia-inducible factor-1α in the rat carotid body glomus cells Histochem Cell Biol 124 69 76 10.1007/s00418-005-0028-6
4. EL Bell TA Klimova J Eisenbart 2007 The Qo site of the mitochondrial complex III is required for the transduction of hypoxic signaling via reactive oxygen species production J Cell Biol 177 1029 1036 10.1083/jcb.200609074
5. EL Bell TA Klimova NS Chandel 2008 Targeting the mitochondria for cancer therapy: regulation of hypoxia-inducible factor by mitochondria Antioxid Redox Signal 10 635 640 10.1089/ars.2007.1655
6. P Birner M Schindl A Obermair 2000 Overexpression of hypoxia-inducible factor 1 is a marker for an unfavorable prognosis in early-stage invasive cervical cancer Cancer Res 60 4693 4696 (Pubitemid 30701471)
7. R Bos H Zhong CF Hanrahan 2001 Levels of hypoxia-inducible factor-1α during breast carcinogenesis J Natl Cancer Inst 93 309 314 10.1093/jnci/93.4.309 (Pubitemid 32219818)
8. JC Braekman D Daloze G Hulot 1978 Chemical studies of marine invertebrates. XXXVII. Three novel meroditerpenoids from the sponge Strongylophora durissima Bull Soc Chim Belg 87 917 926
9. M Broggini SV Marchini E Galliera 2003 Aplidine, a new anticancer agent of marine origin, inhibits vascular endothelial growth factor (VEGF) secretion and blocks VEGF-VEGFR-1 (flt-1) autocrine loop in human leukemia cells MOLT-4 Leukemia 17 52 59 10.1038/sj.leu.2402788
10. JM Brown WR Wilson 2004 Exploiting tumour hypoxia in cancer treatment Nat Rev Cancer 4 437 447 10.1038/nrc1367 (Pubitemid 38745529)
11. J Caers E Menu H De Raeve 2008 Antitumour and antiangiogenic effects of Aplidin in the 5TMM syngeneic models of multiple myeloma Br J Cancer 98 1966 1974 10.1038/sj.bjc.6604388
12. RA Cairns I Papandreou PD Sutphin 2007 Metabolic targeting of hypoxia and HIF1 in solid tumors can enhance cytotoxic chemotherapy Proc Natl Acad Sci USA 104 9445 9450 10.1073/pnas.0611662104
13. NS Chandel E Maltepe E Goldwasser 1998 Mitochondrial reactive oxygen species trigger hypoxia-induced transcription Proc Natl Acad Sci USA 95 11715 11720 10.1073/pnas.95.20.11715
14. NM Chau P Rogers W Aherne 2005 Identification of novel small molecule inhibitors of hypoxia-inducible factor-1 that differentially block hypoxia-inducible factor-1 activity and hypoxia-inducible factor-1α induction in response to hypoxic stress and growth factors Cancer Res 65 4918 4928 10.1158/0008-5472.CAN-04-4453
15. AG Chittiboyina MK Gundluru P Carvalho 2007 Total synthesis and absolute configuration of laurenditerpenol: a HIF-1 activation inhibitor J Med Chem 50 6299 6302 10.1021/jm7011062
16. A Covens J Blessing D Bender 2006 A phase II evaluation of tirapazamine plus cisplatin in the treatment of recurrent platinum-sensitive ovarian or primary peritoneal cancer: a Gynecologic Oncology Group Study Gynecol Oncol 100 586 590 10.1016/j.ygyno.2005.09.032
17. CM Crews JL Collins WS Lane 1994 GTP-dependent binding of the antiproliferative agent didemnin to elongation factor 1α J Biol Chem 269 15411 15414 (Pubitemid 24202118)
18. J Dai JA Fishback Y-D Zhou 2006 Sodwanone and yardenone triterpenes from a South African species of the marine sponge Axinella inhibit hypoxia-inducible factor-1 (HIF-1) activation in both breast and prostate tumor cells J Nat Prod 69 1715 1720 10.1021/np060278q
19. J Dai Y Liu H Jia 2007 Benzochromenones from the marine crinoid Comantheria rotula inhibit hypoxia-inducible factor-1 (HIF-1) reporter activity and differentially suppress the growth of certain tumor cell lines J Nat Prod 70 1462 1466 10.1021/np070224w
20. J Dai Y Liu Y-D Zhou 2007 Cytotoxic metabolites from an Indonesian sponge Lendenfeldia sp. J Nat Prod 70 1824 1826 10.1021/np070337f
21. J Dai Y Liu Y-D Zhou 2007 Hypoxia-selective antitumor Agents: norsesterterpene peroxides from the marine sponge Diacarnus levii preferentially suppress the growth of tumor cells under hypoxic conditions J Nat Prod 70 130 133 10.1021/np0604883
22. KA El Sayed DTA Youssef D Marchetti 2006 Bioactive natural and semisynthetic latrunculins J Nat Prod 69 219 223 10.1021/np050372r
23. KA El Sayed HM Shallal M Khanfar 2008 Latrunculin A and its 17-O-carbamates inhibit prostate tumor cell invasion and HIF-1 activation in breast tumor cells J Nat Prod 71 396 402 10.1021/np070587w
24. E Erba L Bassano G Di Liberti 2002 Cell cycle phase perturbations and apoptosis in tumour cells induced by aplidine Br J Cancer 86 1510 1517 10.1038/sj.bjc.6600265
25. JS Fang RD Gillies RA Gatenby 2008 Adaptation to hypoxia and acidosis in carcinogenesis and tumor progression Semin Cancer Biol 18 330 337 10.1016/j.semcancer.2008.03.011
26. Y Gachet S Tournier JB Millar 2001 A MAP kinase-dependent actin checkpoint ensures proper spindle orientation in fission yeast Nature 412 352 355 10.1038/35085604
27. Y Gong FH Agani 2005 Oligomycin inhibits HIF-1α expression in hypoxic tumor cells Am J Physiol 288 C1023 C1029 10.1152/ajpcell.00443.2004
28. L González-Santiago Y Suárez N Zarich 2006 Aplidin induces JNK-dependent apoptosis in human breast cancer cells via alteration of glutathione homeostasis, Rac1 GTPase activation, and MKP-1 phosphatase downregulation Cell Death Differ 13 1968 1981 10.1038/sj.cdd.4401898
29. TG Graeber C Osmanian T Jacks 1996 Hypoxia-mediated selection of cells with diminished apoptotic potential in solid tumours Nature 379 88 91 10.1038/379088a0
30. LM Greenberger ID Horak D Filpula 2008 A RNA antagonist of hypoxia-inducible factor-1α, EZN-2968, inhibits tumor cell growth Mol Cancer Ther 7 3598 3608 10.1158/1535-7163.MCT-08-0510
31. AE Greijer P van der Groep D Kemming 2005 Up-regulation of gene expression by hypoxia is mediated predominantly by hypoxia-inducible factor 1 (HIF-1) J Pathol 206 291 304 10.1002/path.1778
32. RD Guzy B Hoyos E Robin 2005 Mitochondrial complex III is required for hypoxia-induced ROS production and cellular oxygen sensing Cell Metab 1 401 408 10.1016/j.cmet.2005.05.001
33. TW Hodges CF Hossain Y-P Kim 2004 Molecular-targeted antitumor agents: the Saururus cernuus dineolignans manassantin B and 4-O-demethylmanassantin B are potent inhibitors of hypoxia-activated HIF-1 J Nat Prod 67 767 771 10.1021/np030514m
34. CF Hossain YP Kim SR Baerson 2005 Saururus cernuus lignans-potent small molecule inhibitors of hypoxia-inducible factor-1 Biochem Biophys Res Commun 333 1026 1033 10.1016/j.bbrc.2005.05.191
35. JS Isaacs YJ Jung EG Mimnaugh 2002 Hsp90 regulates a von Hippel Lindau-independent hypoxia-inducible factor-1α-degradative pathway J Biol Chem 277 29936 29944 10.1074/jbc.M204733200
36. 2 sensing Science 292 464 468 10.1126/science.1059817 (Pubitemid 32335941)
37. 2-regulated prolyl hydroxylation Science 292 468 472 10.1126/science.1059796 (Pubitemid 32335942)
38. DT Jones AL Harris 2006 Identification of novel small-molecule inhibitors of hypoxia-inducible factor-1 transactivation and DNA binding Mol Cancer Ther 5 2193 2202 10.1158/1535-7163.MCT-05-0443
39. ME Jung G-YJ Im 2008 Convergent total synthesis of the racemic HIF-1 inhibitor laurenditerpenol Tetrahedron Lett 49 4962 4964 10.1016/j.tetlet.2008. 05.116
40. Y Kashman A Groweiss U Shmueli 1980 Latrunculin, a new 2-thiazolidinone macrolide from the marine sponge Latrunculia magnifica Tetrahedron Lett 21 3629 3632 10.1016/0040-4039(80)80255-3
41. T Klimova NS Chandel 2008 Mitochondrial complex III regulates hypoxic activation of HIF Cell Death Differ 15 660 666 10.1038/sj.cdd.4402307
42. D Kong EJ Park AG Stephen 2005 Echinomycin, a small-molecule inhibitor of hypoxia-inducible factor-1 DNA-binding activity Cancer Res 65 9047 9055 10.1158/0008-5472.CAN-05-1235
43. AL Kung SD Zabludoff DS France 2004 Small molecule blockade of transcriptional coactivation of the hypoxia-inducible factor pathway Cancer Cell 6 33 43 10.1016/j.ccr.2004.06.009
44. D Lando DJ Peet DA Whelan 2002 Asparagine hydroxylation of the HIF transactivation domain a hypoxic switch Science 295 858 861 10.1126/science. 1068592
45. L Li X Lin AR Shoemaker 2006 Hypoxia-inducible factor-1 inhibition in combination with temozolomide treatment exhibits robust antitumor efficacy in vivo Clin Cancer Res 12 4747 4754 10.1158/1078-0432.CCR-05-2842
46. X Lin CA David JB Donnelly 2008 A chemical genomics screen highlights the essential role of mitochondria in HIF-1 regulation Proc Natl Acad Sci USA 105 174 179 10.1073/pnas.0706585104
47. 2-independent and HSP90 inhibitor-induced degradation of HIF-1α Mol Cell 25 207 217 10.1016/j.molcel.2007.01.001
48. R Liu Y Liu Y-D Zhou 2007 Molecular-targeted antitumor agents 15: neolamellarins from the marine sponge Dendrilla nigra inhibit hypoxia-inducible factor-1 (HIF-1) activation and secreted vascular endothelial growth factor (VEGF) production in breast tumor cells J Nat Prod 70 1741 1745 10.1021/np070206e
49. Y Liu R Liu SC Mao 2008 Molecular-targeted antitumor agents. 19. Furospongolide from a Marine Lendenfeldia sp. sponge inhibits hypoxia-Inducible factor-1 activation in breast tumor cells J Nat Prod 71 1854 1860 10.1021/np800342s
50. FC Maluf AL Leiser C Aghajanian 2006 Phase II study of tirapazamine plus cisplatin in patients with advanced or recurrent cervical cancer Int J Gynecol Cancer 16 1165 1171 10.1111/j.1525-1438.2006.00454.x
51. L Marcu I Olver 2006 Tirapazamine: from bench to clinical trials Curr Clin Pharmacol 1 71 79 10.2174/157488406775268192
52. PH Maxwell MS Wiesener GW Chang 1999 The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis Nature 399 271 275 10.1038/20459
53. MedTRACK Biomedical Corporate Intelligence Database (2008) Life Science Analytics, Inc., Scranton. http://www.medtrack.net. Accessed 8 October 2008
54. G Melillo 2007 Targeting hypoxia cell signaling for cancer therapy Cancer Metastasis Rev 26 41 352 10.1007/s10555-007-9059-x
55. CS Mitsiades EM Ocio A Pandiella 2008 Aplidin, a marine organism-derived compound with potent antimyeloma activity in vitro and in vivo Cancer Res 68 5216 5225 10.1158/0008-5472.CAN-07-5725
56. K Mizokami Y Kakeji S Oda 2006 Clinicopathologic significance of hypoxia-inducible factor 1α overexpression in gastric carcinomas J Surg Oncol 94 149 154 10.1002/jso.20568
57. BJ Moeller MR Dreher ZN Rabbani 2005 Pleiotropic effects of HIF-1 blockade on tumor radiosensitivity Cancer Cell 8 99 110 10.1016/j.ccr.2005.06. 016
58. KA Mohammed CF Hossain L Zhang 2004 Laurenditerpenol, a new diterpene from the tropical marine alga Laurencia intricata potently inhibits HIF-1 mediated hypoxic signaling in breast tumor cells J Nat Prod 67 2002 2007 10.1021/np049753f
59. KA Mohammed RC Jadulco TS Bugni 2008 Strongylophorines: natural product inhibitors of hypoxia-inducible factor-1 transcriptional pathway J Med Chem 51 1402 1405 10.1021/jm7010854
60. MJ Muñoz-Alonso L González-Santiago N Zarich 2008 Plitidepsin has a dual effect inhibiting cell cycle and inducing apoptosis via Rac1/c-Jun NH2-terminal kinase activation in human melanoma cells J Pharmacol Exp Ther 324 1093 1101 10.1124/jpet.107.132662
61. DG Nagle Y-D Zhou 2006 Natural product-based inhibitors of hypoxia-inducible factor-1 (HIF-1) Curr Drug Targets 7 355 369 10.2174/138945006776054979
62. DG Nagle Y-D Zhou 2006 Natural product-derived small molecule activators of hypoxia-inducible factor-1 (HIF-1) Curr Pharm Des 12 2673 2688 10.2174/138161206777698783
63. DG Nagle Y-D Zhou FD Mora 2004 Mechanism targeted discovery of antitumor marine natural products Curr Med Chem 11 1725 1756 (Pubitemid 38821341)
64. Y Nakaseko M Yanagida 2001 Cell biology cytoskeleton in the cell cycle Nature 412 291 292 10.1038/35085684
65. DJ Newman GM Cragg 2004 Marine natural products and related compounds in clinical and advanced preclinical trials J Nat Prod 67 1216 1238 10.1021/np040031y
66. DJ Newman GM Cragg 2007 Natural products as sources of new drugs over the last 25 years J Nat Prod 70 461 477 10.1021/np068054v
67. Y Pan KD Mansfield CC Bertozzi 2007 Multiple factors affecting cellular redox status and energy metabolism modulate hypoxia-inducible factor prolyl hydroxylase activity in vivo and in vitro Mol Cell Biol 27 912 925 10.1128/MCB.01223-06
68. SK Park AM Dadak VH Haase 2003 Hypoxia-induced gene expression occurs solely through the action of hypoxia-inducible factor 1α (HIF-1α): role of cytoplasmic trapping of HIF-2α Mol Cell Biol 23 4959 4971 10.1128/MCB.23.14.4959-4971.2003
69. A Rapisarda B Uranchimeg DA Scudiero 2002 Identification of small molecule inhibitors of hypoxia-inducible factor 1 transcriptional activation pathway Cancer Res 62 4316 4324 (Pubitemid 34827288)
70. A Rapisarda J Zalek M Hollingshead 2004 Schedule-dependent inhibition of hypoxia-inducible factor-1α protein accumulation, angiogenesis, and tumor growth by topotecan in U251-HRE glioblastoma xenografts Cancer Res 64 6845 6848 10.1158/0008-5472.CAN-04-2116
71. RR Raval KW Lau MG Tran 2005 Contrasting properties of hypoxia-inducible factor 1 (HIF-1) and HIF-2 in von Hippel-Lindau-associated renal cell carcinoma Mol Cell Biol 25 5675 5686 10.1128/MCB.25.13.5675-5686.2005
72. D Rischin L Peters R Fisher 2005 Tirapazamine, cisplatin, and radiation, versus fluorouracil cisplatin and radiation in patients with locally advanced head and neck cancer: a randomized phase II trial of the Trans-Tasman Radiation Oncology Group (TROG) 98.02 J Clin Oncol 23 79 87 10.1200/JCO.2005.01.072
73. HE Ryan M Poloni W McNulty 2000 Hypoxia-inducible factor-1α is a positive factor in solid tumor growth Cancer Res 60 4010 4015 (Pubitemid 30636574)
74. J Salva DJ Faulkner 1990 Metabolites of the sponge Strongylophora durissima from Maricaban Island, Philippines J Org Chem 55 1941 1943 10.1021/jo00293a047
75. GL Semenza 2003 Targeting HIF-1 for cancer therapy Nat Rev Cancer 3 721 732 10.1038/nrc1187 (Pubitemid 37328811)
76. GL Semenza 2006 Development of novel therapeutic strategies that target HIF-1 Expert Opin Ther Targets 10 267 280 10.1517/14728222.10.2.267
77. GL Semenza 2007 Evaluation of HIF-1 inhibitors as anticancer agents Drug Discov Today 12 853 859 10.1016/j.drudis.2007.08.006
78. GL Semenza 2007 Oxygen-dependent regulation of mitochondrial respiration by hypoxia-inducible factor 1 Biochem J 405 1 9 (Pubitemid 46999919)
79. GL Semenza GL Wang 1992 A nuclear factor induced by hypoxia via de novo protein synthesis binds to the human erythropoietin gene enhancer at a site required for transcriptional activation Mol Cell Biol 12 5447 5454
80. MC Simon 2006 Mitochondrial reactive oxygen species are required for hypoxic HIFα stabilization Adv Exp Med Biol 588 165 170 10.1007/978-0-387-34817-9-15
81. JA Sipos EL Mazzaferri 2008 The therapeutic management of differentiated thyroid cancer Expert Opin Pharmacother 9 2627 2637 10.1517/14656566.9.15.2627
82. HM Sowter R Raval J Moore 2003 Predominant role of hypoxia-inducible transcription factor (Hif)-1α versus Hif-2α in regulation of the transcriptional response to hypoxia Cancer Res 63 6130 6134 (Pubitemid 37255150)
83. I Spector NR Shochet Y Kashman 1983 Latrunculins: novel marine toxins that disrupt microfilament organization in cultured cells Science 219 493 495 10.1126/science.6681676 (Pubitemid 13189272)
84. I Spector NR Shochet D Blasberger 1989 Latrunculins-novel marine macrolides that disrupt microfilament organization and affect cell growth: I. Comparison with cytochalasin D Cell Motil Cytoskeleton 13 127 144 10.1002/cm.970130302 (Pubitemid 19197366)
85. AM Straight K Oakley R Moores 2006 Aplidin reduces growth of anaplastic thyroid cancer xenografts and the expression of several angiogenic genes Cancer Chemother Pharmacol 57 7 14 10.1007/s00280-005-0014-7
86. C Tan RG de Noronha AJ Roecker 2005 Identification of a novel small-molecule inhibitor of the hypoxia-inducible factor 1 pathway Cancer Res 65 605 612
87. JL Tatum GJ Kelloff RJ Gillies 2006 Hypoxia: importance in tumor biology, noninvasive measurement by imaging, and value of its measurement in the management of cancer therapy Int J Radiat Biol 82 699 757 10.1080/ 09553000601002324
88. A Unruh A Ressel HG Mohamed 2003 The hypoxia-inducible factor-1α is a negative factor for tumor therapy Oncogene 22 3213 3220 10.1038/sj.onc. 1206385
89. JL Urdiales P Morata I Núñez De Castro 1996 Antiproliferative effect of dehydrodidemnin B (DDB), a depsipeptide isolated from Mediterranean tunicates Cancer Lett 102 31 37 10.1016/0304-3835(96)04151-1
90. EC Vaux E Metzen KM Yeates 2001 Regulation of hypoxia-inducible factor is preserved in the absence of a functioning mitochondrial respiratory chain Blood 98 296 302 10.1182/blood.V98.2.296
91. J von Pawel R von Roemeling U Gatzemeier 2000 Tirapazamine plus cisplatin versus cisplatin in advanced non-small-cell lung cancer: a report of the International CATAPULT I Study Group. Cisplatin and tirapazamine in subjects with advanced previously untreated non-small-cell lung tumors J Clin Oncol 18 1351 1359
92. GL Wang GL Semenza 1993 Characterization of hypoxia-inducible factor 1 and regulation of DNA binding activity by hypoxia J Biol Chem 268 21513 21518
93. K Warabi LM McHardy L Matainaho 2004 Strongylophorine-26, a new meroditerpenoid isolated from the marine sponge Petrosia (Strongylophora) corticata that exhibits anti-invasion activity J Nat Prod 67 1387 1389 10.1021/np0340246
94. H Zhong AM De Marzo E Laughner 1999 Overexpression of hypoxia-inducible factor 1α in common human cancers and their metastases Cancer Res 59 5830 5835
95. Y-D Zhou Y-P Kim KA Mohammed 2005 The terpenoid tetrahydroisoquinoline alkaloids emetine, klugine, and isocephaeline inhibit the activation of hypoxia-inducible factor-1 (HIF-1) in breast tumor cells J Nat Prod 68 947 950 10.1021/np050029m