Euphorbia and Momordica metabolites for overcoming multidrug resistance

Phytochemistry Reviews

Volumn 13, Issue 4, 2014, Pages 915-935

  Ferreira, Maria José U ^a   Duarte, Noélia ^a   Reis, Mariana ^a   Madureira, Ana Margarida ^a   Molnár, Joseph ^b  

^a RESEARCH INSTITUTE FOR MEDICINES IMED ULISBOA   (Portugal)

^b UNIVERSITY OF SZEGED   (Hungary)

Author keywords

ent Abietane lactones; Euphorbia; Macrocyclic diterpenes; Momordica balsamina L; P glycoprotein; Triterpenes

Indexed keywords

ABIETANE DERIVATIVE; BALSAMINOL F; CUCURBITANE; DITERPENE; EUPHOPUBESCENE; EUPHOPUBESCENOL; EUPHORBIA EXTRACT; EUPHORBIA LAGASCAE EXTRACT; EUPHORBIA MELLIFERA EXTRACT; EUPHORBIA PISCATORIA EXTRACT; EUPHORBIA PORTLANDICA EXTRACT; EUPHORBIA PUBESCENS EXTRACT; EUPHORBIA SEGETALIS EXTRACT; EUPHORBIA TUCKEYANA EXTRACT; GLYCOPROTEIN P INHIBITOR; JATROPHANE; KARAVILAGENIN C; LACTONE; LATHYRANE; MOMORDICA BALSAMINA EXTRACT; MULTIDRUG RESISTANCE PROTEIN; PHENOL DERIVATIVE; PLANT EXTRACT; PUBESCENE A; PUBESCENE B; PUBESCENE C; PUBESCENE D; PUBESCENOL; TRITERPENE; UNCLASSIFIED DRUG; UNINDEXED DRUG;

ANTINEOPLASTIC ACTIVITY; CELL KILLING; DRUG STRUCTURE; DRUG TARGETING; DRUG TRANSPORT; EUPHORBIA; EUPHORBIA LAGASCAE; EUPHORBIA MELLIFERA; EUPHORBIA PISCATORIA; EUPHORBIA PORTLANDICA; EUPHORBIA PUBESCENS; EUPHORBIA SEGETALIS; EUPHORBIA TUCKEYANA; GENE OVEREXPRESSION; HUMAN; INHIBITION KINETICS; MALIGNANT NEOPLASTIC DISEASE; MASS SPECTROMETRY; MOMORDICA BALSAMINA; MULTIDRUG RESISTANCE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEAR OVERHAUSER EFFECT; PHENOTYPE; REVIEW; STRUCTURE ACTIVITY RELATION;

EUPHORBIA; MOMORDICA; MOMORDICA BALSAMINA;

EID: 84912045745     PISSN: 15687767     EISSN: 1572980X     Source Type: Journal    
DOI: 10.1007/s11101-014-9342-8     Document Type: Review

References (90)

1. Abdelgaleil S, Kassem M, Doe M, Baba M, Nakatani M (2001) Diterpenoids from Euphorbia paralias. Phytochemistry 58:1135–1139
2. Aller S, Yu J, Ward A, Weng Y, Chittaboina S, Zhuo R, Harrell P, Trinh Y, Zhang Q, Urbatsch I, Chang G (2009) Structure of P-glycoprotein reveals a molecular basis for poly-specific drug binding. Science 323:1718–1722
3. Barile E, Lanzotti V (2007) Biogenetical related highly oxygenated macrocyclic diterpenes from sea spurge Euphorbia paralias. Org Lett 9:3603–3606
4. Barile E, Fatorusso E, Ialenti A, Ianaroc A, Lanzotti V (2007) Paraliane and pepluane diterpenes as anti-inflammatory agents: first insights in structure–activity relationships. Bioorg Med Chem Lett 17:4196–4200
5. Barile E, Borrielo M, Di Pietro A, Doreau A, Fattorusso C, Fatorusso E, Lanzotti V (2008) Discovery of a new series of jatrophane and lathyrane diterpenes as potent and specific P-glycoprotein modulators. Org Biomol Chem 6:1756–1762
6. Bates D, Robinson R, Jeffrey C (1990) Biology and utilization of the Cucurbitaceae. In: Jeffrey C (ed) Systematics of the Cucurbitaceae: an overview. Cornell University Press, Ithaca, pp 3–9
7. Cahoon E, Ripp K, Hall S, McGonigle B (2002) Transgenic production of epoxy fatty acids by expression of a cytochrome P450 enzyme from Euphorbia lagascae seed. Plant Physiol 128:615–624
8. Castroviejo S, Aedo C, Benedí C, Laínz M, Muñoz F, Feliner G, Paiva J (1997) Euphorbiaceae. In: Castroviejo S, Aedo C, Benedí C, Laínz M, Muñoz F, Feliner G, Paiva J (eds) Flora Iberica: Plantas Vasculares de la Península Ibérica e Islas Baleares, Vol. 8. Real Jardín Botánico, CSIC, Madrid, pp 225, 229, 269, 270
9. Chen J, Chiu M, Nie R, Cordell G, Qiu S (2005) Cucurbitacins and cucurbitane glycosides: structures and biological activities. Nat Prod Rep 22:386–399
10. Corea G, Fattorusso E, Lanzotti V, Taglialatela-Scafati O, Appendino G, Simon P, Dumontet C, Di Pietro A (2003a) Modified jatrophane diterpenes as modulators of multidrug resistance from Euphorbia dendroides L. Bioorg Med Chem 11:5221–5227
11. Corea G, Fattorusso E, Lanzotti V, Taglialatela-Scafati O, Appendino G, Simon P, Dumontet C, Di Pietro A (2003b) Jatrophane diterpenes as P-glycoprotein inhibitors. First insights of structure–activity relationships and discovery of a new, powerful lead. J Med Chem 46:3395–3402
12. Corea G, Fattorusso E, Lanzotti V, Motti R, Simon P, Dumontet C, Di Pietro A (2004a) Jatrophane diterpenes as modulators of multidrug resistance. Advances of structure–activity relationships and discovery of the potent lead pepluanin A. J Med Chem 47:988–992
13. Corea G, Fattorusso E, Lanzotti V, Motti R, Simon P, Dumontet C, Di Pietro A (2004b) Structure–activity relationships for euphocharacins A-L, a new series of jatrophane diterpenes, as inhibitors of cancer cell P-glycoprotein. Planta Med 70:657–665
14. Corea G, Fattorusso C, Fattorusso E, Lanzotti V (2005a) Amygdaloidins A-L, twelve new 13α-OH jatrophane diterpenes from Euphorbia amygdaloides L. Tetrahedron 61:4485–4494
15. Corea G, Fattorusso E, Lanzotti V, Di Meglio P, Maffia P, Grassia G, Ialenti A, Ianaro A (2005b) Discovery and biological evaluation of the novel naturally occurring diterpene pepluanone as anti-inflammatory agent. J Med Chem 48:7055–7062
16. Corea G, Di Pietro A, Dumontet C, Fattorusso E, Lanzotti V (2009) Jatrophane diterpenes from Euphorbia spp. as modulators of multidrug resistance in cancer therapy. Phytochem Rev 8:431–447
17. Cripe L, Uno H, Paietta E, Litzow M, Ketterling R, Bennett J, Rowe J, Lazarus H, Luger S, Tallman M (2010) Zosuquidar, a novel modulator of P-glycoprotein, does not improve the outcome of older patients with newly diagnosed acute myeloid leukemia: a randomized, placebo-controlled trial of the Eastern Cooperative Oncology Group 3999. Blood 116:4077–4085
18. Duarte N, Ferreira MJU (2007) Lagaspholones A and B: two new jatropholane-type diterpenes from Euphorbia lagascae. Org Lett 9:489–492
19. Duarte N, Gyémánt N, Abreu P, Molnár J, Ferreira MJU (2006) New macrocyclic lathyrane diterpenes, from Euphorbia lagascae, as inhibitors of multidrug resistance of tumor cells. Planta Med 72:162–168
20. Duarte N, Varga A, Radics R, Molnár J, Ferreira MJU (2007a) Apoptosis induction and modulation of P-glycoprotein mediated multidrug resistance by new macrocyclic lathyrane-type diterpenoids. Bioorg Med Chem 15:546–554
21. Duarte N, Ferreira MJU, Martins M, Viveiros M, Amaral L (2007b) Antibacterial activity of ergosterol peroxide against Mycobacterium tuberculosis. Dependence upon system and medium employed. Phytother Res 21:601–604
22. Duarte N, Járdánházy A, Molnár J, Ferreira MJU (2008a) Synergistic interaction between p-glycoprotein modulators and epirubicine on resistant cancer cells. Bioorg Med Chem 16:9323–9330
23. Duarte N, Lage H, Ferreira MJU (2008b) Three new jatrophane diterpene polyesters and other constituents from Euphorbia tuckeyana. Planta Med 74:61–68
24. Duarte N, Ramalhete C, Varga A, Molnár J, Ferreira MJU (2009) Multidrug resistance modulation and apoptosis induction of cancer cells by terpenic compounds isolated from Euphorbia species. Anticancer Res 29:4467–4472
25. Duarte N, Lage H, Ferreira MJU (2010) Phenolic compounds as antineoplasic agents against drug-sensitive and multidrug resistant human cancer cells. Planta Med 76:1–6
26. Engi H, Sakagami H, Kawase M, Parecha A, Manvar D, Kothari H, Adlakha P, Shah A, Motohashi N, Ocsovszki I, Molnar J (2006) Tumour-specific cytotoxicity and MDR-reversal activity of dihydropyridines. In Vivo 20:637–643
27. Evans F, Taylor S (1983) Pro-inflammatory, tumor-promoting and antitumor diterpenes of the plant families Euphorbiaceae and Thymelaceae. Prog Chem Org Nat Prod 44:1–99
28. Ferreira MJU, Madureira A, Ascenso J (1998) A tetracyclic diterpene and triterpenes from Euphorbia segetalis. Phytochemistry 49:79–83
29. Ferreira MJU, Gyémánt N, Madureira A, Molnár J (2005) Inhibition of P-glycoprotein transport activity in a resistant mouse lymphoma cell line by diterpenic lactones. Anticancer Res 25:3259–3262
30. Ferreira MJU, Duarte N, Gyémánt N, Radics R, Chepernev G, Varga A, Molnár J (2006) Interaction between doxorubicin and the resistance modifier stilbene on multidrug resistant mouse lymphoma and human breast cancer cells. Anticancer Res 26:3541–3546
31. Ferreira RJ, dos Santos DJVA, Ferreira MJU, Guedes RC (2011) Toward a better pharmacophore description of P-glycoprotein modulators, based on macrocyclic diterpenes from Euphorbia species. J Chem Inf Model 51:1315–1324
32. Figueiredo E (1996) Flora de Cabo Verde: Plantas Vasculares. 54. Euphorbiaceae. Instituto de investigação científica Tropical, Lisboa
33. Genoux-Bastide E, Lorendeau D, Nicolle E, Yahiaoui S, Magnard S, Di Pietro A, Baubichon-Cortay H, Boumendjel A (2011) Identification of xanthones as selective killers of cancer cells overexpressing the ABC transporter MRP1. ChemMedChem 6:1478–1484
34. Gottesman M, Fojo T, Bates S (2002) Multidrug resistance in cancer: role of ATP-dependent transporters. Nat Rev Cancer 2:48–58
35. Hall M, Handley M, Gottesman M (2009) Is resistance useless? Multidrug resistance and collateral sensitivity. Trends Pharmacol Sci 30:546–556
36. Hohmann J, Evanics F, Dombi G, Molnár J, Szabo P (2001) Euphosalicin, a new diterpene polyester with multidrug resistance reversing activity from Euphorbia salicifolia. Tetrahedron 57:211–215
37. Hohmann J, Molnár J, Rédei D, Evanics F, Forgo P, Kálmán A, Argay G, Szabo P (2002) Discovery and biological evaluation of a new family of potent modulators of multidrug resistance: reversal of multidrug resistance of mouse lymphoma cells by natural jatrophane diterpenoids isolated from Euphorbia species. J Med Chem 45:2425–2431
38. Hohmann J, Rédei D, Forgo P, Molnár J, Dombi G, Zorig T (2003) Jatrophane diterpenoids from Euphorbia mongolica as modulators of the multidrug resistance of L5128 mouse lymphoma cells. J Nat Prod 66:976–979
39. Jakupovic J, Morgenstern T, Bittner M, Silva M (1998a) Diterpenes from Euphorbia peplus. Phytochemistry 47:1601–1609
40. Jakupovic J, Morgenstern T, Marco J, Berendohn W (1998b) Diterpenes from Euphorbia paralias. Phytochemistry 47:1611–1619
41. Jassbi A (2006) Chemistry and biological activity of secondary metabolites in Euphorbia from Iran. Phytochemistry 67:1977–1984
42. Kelly R, Draper D, Chen C, Robey R, Figg W, Piekarz R, Chen X, Gardner E, Balis F, Venkatesan A, Steinber S, Fojo T, Bates S (2011) A pharmacodynamic study of docetaxel in combination with the P-glycoprotein antagonist tariquidar (XR9576) in patients with lung, ovarian, and cervical cancer. Clin Cancer Res 17:569–580
43. Laberge RM, Ambadipudi R, Georges E (2009) P-glycoprotein (ABCB1) modulates collateral sensitivity of a multidrug resistant cell line to verapamil. Arch Biochem Biophys 491:53–60
44. Lage H (2008) An overview of cancer multidrug resistance: a still unsolved problem. Cell Mol Life Sci 65:3145–3167
45. Lage H, Duarte N, Ferreira MJU (2010) Antitumor activity of terpenoids against classical and atypical multidrug resistant cancer cells. Phytomedicine 17:441–448
46. Lee C (2010) Reversing agents for ATP-binding cassette drug transporters. Methods Mol Biol 596:325–340
47. Ling K, Zhi M, Jian S (1996) Chemical constituents from roots of Jatropha curcas. Acta Bot Sin 38:161–166
48. Madureira A, Ascenso J, Valdeira L, Duarte A, Frade J, Freitas G, Ferreira MJU (2003) Evaluation of the antiviral and antimicrobial activities of triterpenes isolated from Euphorbia segetalis. Nat Prod Res 17:375–380
49. Madureira A, Ferreira MJU, Gyémánt N, Ugocsai K, Ascenso J, Abreu P, Hohmann J, Molnár J (2004a) Rearranged jatrophane diterpenes from Euphorbia species. Evaluation of their effects on the reversal of multidrug resistance. Planta Med 70:45–49
50. Madureira A, Spengler G, Molnár A, Varga A, Molnár J, Abreu P, Ferreira MJU (2004b) Effect of cycloartanes on reversal of multidrug resistance and apoptosis induction on mouse lymphoma cells. Anticancer Res 24:859–864
51. Madureira A, Gyémánt N, Ascenso J, Abreu P, Molnár J, Ferreira MJU (2006) Euphoportlandols A and B, tetracyclic diterpene polyesters from Euphorbia portlandica and their anti-MDR effects in cancer cells. J Nat Prod 69:950–953
52. Marco J, Cervera J, Yuste A, Jakupovic J, Jeske F (1998) Jatrophane derivatives and a rearranged jatrophane from Euphorbia terracina. Phytochemistry 47:1621–1630
53. Michalak K, Wesolowska O, Motohashi N, Molnár J, Hendrich A (2006) Interactions of phenotiazines with lipid bilayer and their role in multidrug resistance reversal. Curr Drug Targets 7:1095–1105
54. Newman D, Cragg G (2012) Natural products as sources of new drugs over the 30 years from 1981 to 2010. J Nat Prod 75:311–335
55. Öksüz S, Gürek F, Shu-Wei Y, Long L, Cordell G, Pezzuto J, Wagner H, Lotter H (1997) Paralinones A and B, novel diterpene esters from Euphorbia paralias. Tetrahedron 53:3215–3222
56. Palmeira A, Sousa E, Vasconcelos M, Pinto M (2012) Three decades of P-gp inhibitors: skimming through several generations and scaffolds. Curr Med Chem 19:1946–2025
57. Pluchino K, Hall M, Goldsborough A, Callaghan R, Gottesman M (2012) Collateral sensitivity as a strategy against cancer multidrug resistance. Drug Resist Updat 15:98–105
58. Press J, Short M (1994) Flora of Madeira. The Natural History Museum, London
59. Purushothaman K, Chandrasekharan S, Cameron A, Connoly J, Labbé C, Maltz A, Rycroft D (1979) Jatropholones A and B, new diterpenoids from the roots of Jatropha gossypiifolia (Euphorbiaceae)—crystal structure analysis of jatropholone B. Tetrahedron Lett 20:979–980
60. Ramalhete C, Mansoor T, Mulhovo S, Molnar J, Ferreira MJU (2009a) Cucurbitane-type triterpenoids from the African plant Momordica balsamina. J Nat Prod 72:2009–2013
61. Ramalhete C, Molnar J, Mulhovo S, Rosário V, Ferreira MJU (2009b) New potent P-glycoprotein modulators with the cucurbitane scaffold and their synergistic interaction with doxorubicin on resistant cancer cells. Bioorg Med Chem 17:6942–6951
62. Ramalhete C, Lopes D, Mulhovo S, Molnár J, Rosário VE, Ferreira MJU (2010) New antimalarials with a triterpenic scaffold from Momordica balsamina. Bioorg Med Chem 18:5254–5260
63. Ramalhete C, da Cruz FP, Lopes D, Mulhovo S, Rosário V, Prudêncio M, Ferreira MJU (2011a) Triterpenoids as inhibitors of erythrocytic and liver stages of Plasmodium infections. Bioorg Med Chem 19:7474–7481
64. Ramalhete C, Lopes D, Molnár J, Mulhovo S, Rosário VE, Ferreira MJU (2011b) Karavilagenin C derivatives as antimalarials. Bioorg Med Chem 19:330–338
65. Ramalhete C, Spengler G, Martins A, Martins M, Viveiros M, Mulhovo S, Ferreira MJU, Amaral L (2011c) Inhibition of efflux pumps in meticillin-resistant Staphylococcusaureus and Enterococcusfaecalis resistant strains by triterpenoids from Momordicabalsamina. Int J Antimicrob Agents 37:70–74
66. Reis M, Ferreira R, Santos M, Santos D, Molnár J, Ferreira MJU (2013) Enhancing macrocyclic diterpenes as multidrug-resistance reversers: structure–activity studies on jolkinol D derivatives. J Med Chem 56:748–760
67. Reis M, Ferreira R, Serly J, Duarte N, Madureira AM, Santos DJ, Molnár J, Ferreira MJ (2012) Colon adenocarcinoma multidrug resistance reverted by Euphorbia diterpenes: structure-activity relationships and pharmacophore modeling. Anti-Cancer Agents Med Chem 12:1015–1024
68. Rios J, Escandell J, Recio M (2005) New insights into bioactivity of cucurbitacins. In: Atta-ur-Rahman (ed) Studies in natural products chemistry. Amsterdam, pp 429–469
69. Shaffer B, Gillet J, Patel C, Baer M, Bates S, Gottesman M (2012) Drug resistance: still a daunting challenge to the successful treatment of AML. Drug Resist Updat 15:62–69
70. Shi Q, Su X, Kiyota H (2008) Chemical and pharmacological research of the plants in genus Euphorbia. Chem Rev 108:4295–4327
71. Shukla S, Ohnuma S, Ambudkar S (2011) Improving cancer chemotherapy with modulators of ABC drug transportes. Curr Drug Targets 12:621–630
72. Siegel R, Naishadham D, Jemal A (2013) Cancer statistics. CA Cancer J Clin 63:11–30
73. Sousa IJ, Ferreira MJU, Molnár J, Fernandes MX (2013) QSAR studies of macrocyclic diterpenes with P-glycoprotein inhibitory activity. Eur J Pharm Sci 48:542–553
74. Srinivas E, Murthy J, Rao A, Sastry G (2006) Recent advances in molecular modeling and medicinal chemistry aspects of phospho-glycoprotein. Curr Drug Metab 7:205–217
75. Szakács G, Paterson J, Ludwig J, Genthe C, Gottesman M (2006) Targeting multidrug resistance in cancer. Nat Rev Drug Discov 5:219–234
76. Szybalski W, Bryson V (1952) Genetic studies on microbial cross resistance to toxic agents. I. Cross resistance of Escherichia coli to fifteen antibiotics. J Bacteriol 64:489–499
77. Teisseyre A, Duarte N, Ferreira MJU, Michalak K (2009) Influence of the multidrug transporter inhibitors on the activity of Kv1.3 on voltage gated potassium channels. J Physiol Pharmacol 60:69–76
78. Thakur G, Bag M, Sanodiya BS, Bhadauriya P, Debnath M, Prasad G, Bisen P (2009) Momordica balsamina: a medicinal and nutraceutical plant for health care management. Curr Pharm Biotechnol 10:667–682
79. Valente C, Ferreira MJU, Abreu P, Pedro M, Cerqueira F, Nascimento M (2003) Three new jatrophane diterpenes from Euphorbia pubescens. Planta Med 69:361–366
80. Valente C, Ferreira MJU, Abreu P, Gyémánt N, Ugocsai K, Hohmann J, Molnár J (2004) Pubescenes, jatrophane diterpenes from Euphorbia pubescens, with multidrug resistance reversing activity on mouse lymphoma cells. Planta Med 70:81–84
81. Valente I, Reis M, Duarte N, Serly J, Molnár J, Ferreira MJU (2012) Jatrophane diterpenes from Euphorbia mellifera and their activity as P-glycoprotein modulators on multidrug resistant mouse lymphoma and human colon adenocarcinoma cells. J Nat Prod 75:1915–1921
82. Vasas A, Sulyok E, Rédei D, Forgo P, Szabó P, Zupkó I, Berényi Á, Molnár J, Hohmann J (2011) Jatrophane diterpenes from Euphorbia esula as antiproliferative agents and potent chemosensitizers to overcome multidrug resistance. J Nat Prod 74:1453–1461
83. Vasas A, Rédei D, Csupor D, Molnár J, Hohmann J (2012) Diterpenes from european Euphorbia species serving as prototypes for natural-product-based drug discovery. Eur J Org Chem 27:5115–5130
84. Voigt B, Coburger C, Molnar J, Hilgeroth A (2007) Structure–activity relationships of novel N-acyloxy-1,4-dihydropyridines as P-glycoprotein inhibitors. Biorg Med Chem 15:5110–5113
85. Ward A, Szewczyk P, Grimard V, Vinciane C, Leed C, Martinez L, Doshi R, Caya A, Villaluz M et al (2013) Structures of P-glycoprotein reveal its conformational flexibility and an epitope on the nucleotide-binding domain. Proc Natl Acad Sci USA 110:13386–13391
86. Wesolowska O, Wiśniewski J, Duarte N, Ferreira MJU, Michalak K (2007) Inhibition of MRP1 transport activity by phenolic and terpenic compounds isolated from Euphorbia species. Anticancer Res 27:4127–4134
87. Wesolowska O, Wisniewski J, Pohl A, Paprocka M, Duarte N, Ferreira MJU, Dús D, Michalak K (2010) Stilbenes as multidrug resistance modulators and apoptosis inducers in human adenocarcinoma cells. Anticancer Res 30:4587–4594
88. Wesolowska O, Wisniewski J, Pomianek K, Pohl A, Paprocka M, Dús D, Duarte N, Ferreira MJU, Michalak K (2012) Multidrug resistance reversal and apoptosis induction in human colon cancer cells by some flavonoids present in citrus plants. J Nat Prod 75:1915–1921
89. Wiese M, Pajeva I (2001) Structure activity relationships of multidrug resistance reversers. Curr Med Chem 8:685–713
90. Zahreddine H, Borden K (2013) Mechanisms and insights into drug resistance in cancer. Front Pharmacol 4:1–8