The antinociceptive and anti-inflammatory activities of caulerpin, a bisindole alkaloid isolated from seaweeds of the genus Caulerpa

Marine Drugs

Volumn 7, Issue 4, 2009, Pages 689-704

  De Souza, Éverton Tenório ^a   De Lira, Daysianne Pereira ^b   De Queiroz, Aline Cavalcanti ^a   Da Silva, Diogo José Costa ^a   De Aquino, Anansa Bezerra ^a   Campessato Mella, Eliane A ^a   Lorenzo, Vitor Prates ^b   De Miranda, George Emmanuel C ^b   De Araújo Júnior, João Xavier ^a   De Oliveira Chaves, Maria Célia ^b   Barbosa Filho, José Maria ^b   De Athayde Filho, Petrônio Filgueiras ^b   De Oliveira Santos, Bárbara Viviana ^b   Alexandre Moreira, Magna Suzana ^a  

^a FEDERAL UNIVERSITY OF ALAGOAS   (Brazil)

^b FEDERAL UNIVERSITY OF PARAÍBA   (Brazil)

Author keywords

Anti inflammatory; Antinociceptive; Caulerpa racemosa; Caulerpin

Indexed keywords

ACETIC ACID; ALKALOID DERIVATIVE; ANTIINFLAMMATORY AGENT; ANTINOCICEPTIVE AGENT; CAPSAICIN; CARRAGEENAN; CAULERPIN; DIAZEPAM; DIPYRONE; FORMALDEHYDE; INDOLE DERIVATIVE; INDOMETACIN; PLANT EXTRACT; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIINFLAMMATORY ACTIVITY; ANTINOCICEPTION; ARTICLE; CAULERPA; CAULERPA RACEMOSA; CELL MIGRATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DISEASE MODEL; DRUG DETERMINATION; DRUG EFFECT; DRUG ISOLATION; DRUG STRUCTURE; EAR EDEMA; EDEMA; FEMALE; GENUS; IN VIVO STUDY; INFRARED SPECTROSCOPY; MALE; MOTOR ACTIVITY; MOUSE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PAIN; PERITONITIS; SEAWEED; TREATMENT OUTCOME;

CAULERPA; CAULERPA RACEMOSA;

EID: 75149115163     PISSN: None     EISSN: 16603397     Source Type: Journal    
DOI: 10.3390/md7040689     Document Type: Article

References (61)

1. Barbosa-Filho, J.M.; Cunha, E.V.L.; Gray, A.I. Alkaloids of the Menispermaceae. In The Alkaloids; Cordell, G.A., Ed.; Academic Press: Illinois, USA, 2000; Vol. 54; pp. 1-199.
2. Barbosa-Filho, J.M.; Sette, I.M.F.; Cunha, E.V.L.; Guedes, D.N.; Silva, M.S. Protoberberine alkaloids. In The Alkaloids; Cordell, G.A., Ed.; Elsevier Inc: San Diego, CA, USA, 2005; Vol. 62; pp. 1-75.
3. Conserva, L.M.; Pereira, C.A.B.; Barbosa-Filho, J.M. Alkaloids of the Hernandiaceae: Occurrence and a Compilation of their Biological Activities. In The Alkaloids; Cordell, G.A., Ed.; Elsevier: San Diego, CA, USA, 2005; Vol. 62; pp. 175-243.
4. Falcão, H.S.; Leite, J.A.; Barbosa-Filho, J.M.; Athayde-Filho, P.F.; Chaves, M.C.O.; Moura, M.D.; Ferreira, A.L.; Almeida, A.B.A.; Souza-Brito, A.R.M.; Diniz, M.F.F.M.; Batista, L.M. Gastric and duodenal antiulcer activity of alkaloids: A review. Molecules 2008, 13, 3198-3223.
5. Cunha, E.V.L.; Barbosa-Filho, J.M. Alcalóides derivados do núcleo isoquinolínico. In Química de Produtos Naturais, Novos Fármacos e a Moderna Farmacognosia, 2a. ed.; Yunes, R.A., Cechinel-Filho, V., Eds.; Univali Editora: Itajaí-PR, Brazil, 2009; pp. 279-319.
6. Williams, J.E. Review of antiviral and immunomodulating properties of plants of the Peruvian rainforest with a particular emphasis on uña de gato and sangre de grado. Altern. Med. Rev. 2001, 6, 567-579.
7. Fechine, I.M.; Navarro, V.R.; Cunha, E.V.L.; Silva, M.S.; Maia, J.G.S.; Barbosa-Filho, J.M. Alkaloids and volatile constituents from Duguetia flagellaris. Biochem. Syst. Ecol. 2002, 30, 267-269.
8. Melo, P.S.; Cavalcante, H.M.M.; Barbosa-Filho, J.M.; Diniz, M.F.F.M.; Medeiros, I.A.; Haun, M. Warifteine and milonine, alkaloids isolated from Cissampelos sympodialis Eichl: cytotoxicity on rat hepatocyte culture and in V79 cells. Toxicol. Lett. 2003, 142, 143-151.
9. Cano, A.; Alcaraz, O.; Arnao, M.B. Free radical-scavenging activity of indolic compounds in aqueous and ethanolic media. Anal. Bioanal. Chem. 2003, 376, 33-37.
10. St-Pierre, B.; Vazquez-Flota, F.A.; de Luca, V. Multicellular compartmentation of Catharanthus roseus alkaloid biosynthesis predicts intercellular translocation of a pathway intermediate. Plant Cell. 1999, 11, 887-900.
11. Wall, M.E.; Wani, M.; Cook, C.E.; Palmer, K.H.; Mc Phail, A.T.; Sim, G.A. Plant antitumor agents I. The isolation and structure elucidation of Camptothecin, a novel alkaloidal leukemia and tumor inhibitor from Camptotheca cuminata. J. Am. Chem. Soc. 1966, 88, 3888-3890.
12. Shaari, K.; Ling, K.C.; Rashid, Z.M.; Jean, T.P.; Abas, F.; Raof, S.M.; Zainal, Z.; Lajis, N.H.; Mohamad, H.; Ali, A.M. Cytotoxic aaptamines from Malaysian Aaptos aaptos. Mar. Drugs 2009, 7, 1-8.
13. Wu, W.H.; Hasumi, K.; Peng, H.; Hu, X.W.; Wang, X.C.; Bao, B. Fibrinolytic compounds isolated from a brown alga, Sargassum fulvellum. Mar. Drugs 2009, 7, 85-94.
14. Genovese, G.; Tedone, L.; Hamann, M.T.; Morabito, M. The Mediterranean red alga Asparagopsis: A source of compounds against leishmania. Mar. Drugs 2009, 7, 361-366.
15. Walsh, C.J.; Leggett, S.R.; Strohbehn, K.; Pierce, R.H.; Sleasman, J. Effects of in vitro brevetoxin exposure on apoptosis and cellular metabolism in a leukemic T cell line (Jurkat). Mar. Drugs 2008, 6, 291-307.
16. Courtois, A.; Simon-Colin, C.; Boisset, C.; Berthou, C.; Deslandes, E.; Guezennec, J.; Bordron, A. Floridoside extracted from the red alga Mastocarpus stellatus is a potent activator of the classical complement pathway. Mar. Drugs 2008, 6, 407-417.
17. Baunbk, D.; Trinkler, N.; Ferandin, Y.; Lozach, O.; Ploypradith, P.; Rucirawat, S.; Ishibashi, F.; Iwao, M.; Meijer, L. Anticancer alkaloid lamellarins inhibit protein kinases. Mar. Drugs 2008, 6, 514-527.
18. Kijjoa, A.; Wattanadilok, R.; Campos, N.; Nascimento, M.S.J.; Pinto, M.; Herz, W. Anticancer activity evaluation of kuanoniamines A and C isolated from the marine sponge Oceanapia sagittaria, collected from the gulf of Thailand. Mar. Drugs 2007, 5, 6-22.
19. Oda, T.; Wang, W.F.; Ukai, K.; Nakazawa, T.; Mochizuki, M. A sesquiterpene quinone, 5-epismenospongine, promotes TNF-alpha production in LPS-stimulated RAW 264.7 cells. Mar. Drugs 2007, 5, 151-156.
20. Bao, B.; Zhang, P.; Lee, Y.; Hong, J.; Lee, C.O.; Jung, J.H. Monoindole alkaloids from a marine sponge Spongosorites sp. Mar. Drugs 2007, 5, 31-39.
21. Souza, E.T.; Queiroz, A.C.; Miranda, G.E.C.; Lorenzo, V.P.; Silva, E.F.; Freire-Dias, T.L.M.; Cupertino-Silva, Y.K.; Melo, G.M.A.; Santos, B.V.O.; Chaves, M.C.O.; Alexandre-Moreira, M.S. Antinociceptive activities of crude methanolic extract and phases, n-butanolic, chloroformic and ethyl acetate from Caulerpa racemosa (Caulerpaceae). Braz. J. Pharmacogn. 2009, 19, 115-120.
22. Ayyad, S.E.N.; Badria, F.A. Caulerpin, an antitumor índole alkaloid from Caulerpa racemosa, Alex. J. Pharm. Sci. 1994, 8, 217.
23. Xu, X.H.; Su, J.G. The separation, identification and bioassay of caulerpin. Zhongshan Daxue Xuebao Ziran Kexueban 1996, 35, 64-66.
24. Raub, M.F.; Cardellina II, J.H.; Schwede, J.G. The green algal pigment caulerpin as a plant growth regulator. Phytochemistry 1987, 26, 619-620.
25. Vidal, J.P.; Laurent, D.; Kabore, A.; Rechencg, E.; Boucard, M.; Girard, J.P.; Escale, R.; Rossi, J.C. Caulerpin, caulerpicin, Caulerpa scalpelliformis: comparative acute toxicity study. Bot. Mar. 1984, 27, 533-537.
26. Du, J.; Yu, Y.; Ke, Y.; Wang, C.; Zhu, L.; Qian, Z.M. Ligustilide attenuates pain behavior induced by acetic acid or formalin. J. Ethnopharmacol. 2007, 112, 211-214.
27. Zeashana, H.; Amresha, G.; Raoa, C.V.; Singhb, S. Antinociceptive activity of Amaranthus spinosus in experimental animals. J. Ethnopharmacol. 2009, 122, 492-496.
28. Choi, E.M. Antinociceptive and antiinflammatory activities of pine (Pinus densiflora) pollen extract. Phytother. Res. 2007, 21, 471-475.
29. Collier, H.O.J.; Dinneen, J.C.; Johnson, C.A.; Schneider, C. The abdominal constriction response and its suppression by analgesic drugs in the mouse. Brit. J. Pharm. Chemoth. 1968, 32, 295-310.
30. Alexandre-Moreira, M.S.; Piuvezam, M.R.; Araújo, C.C.; Thomas, G. Studies on the anti-inflammatory and analgesic activity of Curatella americana L. J. Ethnopharmacol. 1999, 67, 171-177.
31. Miranda, F.G.G.; Vilar, J.C.; Alves, I.A.N.; Cavalcanti, S.C.H.; Antoniolli, A.R. Antinociceptive and antiedematogenic properties and acute toxicity of Tabebuia avellanedae Lor. ex Griseb. inner bark aqueous extract. BMC Pharmacol. 2001, 1, 1-16.
32. Moñoa, J.; Moscatelli, V.; Hnatyszyn, O.; Gorzalczany, S.; Acevedo, C.; Ferraro, G. Antinociceptive and antiinflammatory activities of Artemisia copa extracts. Pharmacol. Res. 2004, 50, 59-63.
33. García, M.D.; Fernández, M.A.; Alvarez, A.; Saenz, M.T. Antinociceptive and anti-inflammatory effect of the aqueous extract from leaves of Pimenta racemosa var. ozua (Mirtaceae). J. Ethnopharmacol. 2004, 91, 69-73.
34. Ojewole, J.A.O. Antinociceptive, anti-inflammatory and antidiabetic properties of Hypoxis hemerocallidea Fisch. & C.A. Mey. (Hypoxidaceae) corm ['African Potato'] aqueous extract in mice and rats. J. Ethnopharmacol. 2006, 103, 126-134.
35. Ballou, L.; Botting, R.M.; Goorha, S.; Zhang, J.; Vane, J.R. Nociception in cyclooxygenase isozyme-deficient mice. Proc. Natl. Acad. Sci. USA 2000, 97, 10272-10276.
36. Clunie, M.; Crone, L.A.; Klassen, L.; Yip, R. Psychiatric side effects of indomethacin in parturients. Can. J. Anesth. 2003, 50, 586-588.
37. Tjølsen, A.; Berger, O.G.; Hunskaar, S.; Rosland, J.H.; Hole, K. The formalin test: evaluation of the method. Pain 1992, 51, 5-17.
38. Inoue, H.; Nagata, N.; Koshihara, Y. Profile of capsaicin-induced mouse ear oedema as neurogenic inflammatory model: comparison with arachidonic acid-induced ear oedema. Brit. J. Pharmacol. 1993, 110, 1614-1620.
39. Tang, M.L.Y.; Haas, D.A.; Hu, J.W. Capsaicin-induced joint inflammation is not blocked by local anesthesia. Anesth. Prog. 2004, 51, 2-9.
40. Grant, A.D.; Gerard, N.P.; Brain, S.D. Evidence of a role for NK1 and CGRP receptors in mediating neurogenic vasodilatation in the mouse ear. Brit. J. Pharmacol. 2002, 135, 356-362.
41. Szallasia, A.; Blumbergb, P.M. Vanilloid receptors: New insights enhance potential as a therapeutic. Pain 1996, 68, 195-208.
42. Chizh, B.A.; Aylott, M.C.; Bullman, J.N.; Gray, E.J.; Lai, R.Y.; Williams, P.M.; Appleby, J.M. The effects of the TRPV1 antagonist SB-705498 on TRPV1 receptormediated activity and inflammatory hyperalgesia in humans. Pain 2007, 132, 132-141.
43. 4. Biochem. Pharmacol. 1986, 35, 1709-1717.
44. Yong-Fang, H.U.; Yong-Jie, W.U. Effect of recombinant human basic fibroblast growth factor on acute inflammation in mice and rats. Acta. Pharmacol. Sin. 2001, 22, 357-379.
45. Oktar, B.K.; Yuksel, M.; Alican, I. The role of cyclooxygenase inhibition in the effect of amelanocyte-stimulating hormone on reactive oxygen species production by rat peritoneal neutrophils. Prostag. Leukot. Essent. Fatty Acids 2004, 71, 1-5.
46. Calixto, J.B; Beirith, A.; Ferreira, J.; Santos, A.R.S.; Cechinel-Filho, V.; Yunes, R.A. Naturally occurring antinociceptive substances from plants. Phytother. Res. 2000, 14, 401-418.
47. Radwan, M.A.A.; Ragab, E.A.; Sabry, N.M.; El-Shenawy, S.M. Synthesis and biological evaluation of new 3-substituted indole derivatives as potential anti-inflammatory and analgesic agents. Biol. Med. Chem. 2007, 15, 3832-3841.
48. Bhati, S.K.; Kumar, A. Synthesis of new substituted azetidinoyl and thiazolidinoyl-1,3,4-thiadiazino (6,5-b) indoles as promising anti-inflammatory agents. Eur. J. Med. Chem. 2008, 43, 2323-2330.
49. Hata, A.N.; Lybrand, T.P.; Marnett, L.J.; Breyer, R.M. Structural determinants of arylacetic acid nonsteroidal anti- inflammatory drugs necessary for binding and activation of the prostaglandin D2 receptor CRTH2. Mol. Pharmacol. 2005, 67, 640-647.
50. Touhey, S.; O'Connor, R.; Plunkett, S.; Maguire, A.; Clynes, M. Structure-activity relationship of indomethacin analogues for MRP-1, COX-1 and COX-2 inhibition: identification of novel chemotherapeutic drug resistance modulators. Eur. J. Cancer 2002, 38, 1661-1670.
51. Stole, S. Indole derivatives as neuroprotectants. Life Sci. 1999, 65, 1943-1950.
52. Kang, K.; Park, S.; Kim, Y.S.; Lee, L.S.; Back, K. Biosynthesis and biotechnological production of serotonin derivatives. Appl. Microbiol. Biotechnol. 2009, 83, 27-34.
53. Maffei-Facino, R.; Carini, M.; Aldini, G.; Saibene, L.; Macciocchi, A. Antioxidant profile of nimesulide, indomethacin and diclofenac in phosphatidylcholine liposomes (PCL) as membrane model. Int. J. Tissue React. 1993, 15, 225-234.
54. Zimmermann, M. Ethical guidelines for investigation of experimental pain in conscious animals. Pain 1983, 16, 109-110.
55. Koster, R.; Anderson, M.; De-Beer, E.J. Acetic acid analgesic screen. Fed. Proc. 1959, 18, 418-420.
56. Eddy, N.B.; Leimbach, D. Synthetic analgesics. II. Dithienylbutenyland dithienylbutylamines. JPET 1953, 107, 385-393.
57. Godoy, M.C.M., Figueira, M.R., Flores, A.E., Rubin, M.A., Oliveira, M.R., Zanatta, N., Martins, M.A.P., Bonacorso, H.G., Mello, C.F. α2- Adrenoceptors and 5-HT receptors mediate the antinociceptive effect of new pyrazoles, but not of dipyrone. Eur. J. Pharmacol. 2004, 496, 93-97.
58. Hunskaar, S.; Hole, K. The formalin test in mice: dissociation between inflammatory and non-inflammatory pain. Pain 1987, 30, 103-114
59. Tjolsen, A.; Hole, K.1997. Animal models of analgesia. In The Pharmacology of Pain; Dickenson, A., Besson, J., Eds.; Springer Verlag: Berlin, Germany, 1997; 130, pp. 1-20.
60. 1-receptor antagonist blocks capsaicin-induced ear inflammation in mice. Brit. J. Pharmacol. 1990, 99, 516-518.
61. Ferrándiz, M.L.; Alcaraz, M.J. Antiinflammatory activity and inhibition of arachidonic acidmetabolism by flavonoids. Inflamm. Res. 1991, 32, 283-288.