Ernest Guenther award in chemistry of natural products. Amphibian skin: A remarkable source of biologically active arthropod alkaloids

Journal of Medicinal Chemistry

Volumn 46, Issue 4, 2003, Pages 445-452

  Daly, John W ^a  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 (2 AZETIDINYLMETHOXY) 2 CHLOROPYRIDINE; ALKALOID; ALLOPUMILIOTOXIN; ANALGESIC AGENT; BATRACHOTOXIN; BIOGENIC AMINE; CERULETIDE; DECAHYDROQUINOLINE DERIVATIVE; DENDROBATE; DERMORPHIN; EPIBATIDINE; EPIPEDOBATE; FORSKOLIN; GEPHYROTOXIN; HISTRIONICOTOXIN; INDOLIZIDINE ALKALOID; MAGAININ DERIVATIVE; MINYOBATE; MORPHINE; NATURAL PRODUCT; NICOTINIC AGENT; PHYSALAEMIN; PIPERIDINE DERIVATIVE; PUMILIOTOXIN; PYRROLIDINE DERIVATIVE; QUINOLIZIDINE DERIVATIVE; SAUVAGINE; TETRODOTOXIN; TRYPTAMINE DERIVATIVE; UNCLASSIFIED DRUG; UNINDEXED DRUG;

AMPHIBIA; ANALGESIA; CLINICAL TRIAL; DRUG ACTIVITY; DRUG ISOLATION; DRUG MECHANISM; DRUG POTENCY; DRUG STRUCTURE; DRUG SYNTHESIS; FROG; HUMAN; INFRARED SPECTROMETRY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; REVIEW; SALAMANDER; SKIN; STRUCTURE ACTIVITY RELATION; TOXICITY;

ALKALOIDS; AMPHIBIA; ANIMALS; ARTHROPODS; AWARDS AND PRIZES; BIOLOGICAL PRODUCTS; CHEMISTRY, ORGANIC; HISTORY, 20TH CENTURY; PORTRAITS; SKIN;

EID: 0037434512     PISSN: 00222623     EISSN: None     Source Type: Journal    
DOI: 10.1021/jm0204845     Document Type: Review

References (56)

1. Erspamer, V. Comparative histochemistry as a springboard for the discovery of biogenic amines and active peptides in molluscan tissues and amphibian skin. Basic Appl. Histochem. 1981, 25, 3-14.
2. Berkowitz, B. A.; Bevins, C. L.; Zasloff, M. A. Magainins: A new family of membrane-active host defense peptides. Biochem. Pharmacol. 1990, 39, 625-629.
3. Meyer, K.; Linde, H. Collection of toad venoms and the chemistry of the toad venom steroids. In Venomous Animals and Their Venoms; Bücherl, W., Buckley, E. E., Eds.; Academic Press: New York, 1971; Chapter 40, pp 521-556.
4. Kim, Y. H.; Brown, G. H.; Mosher, H. S.; Fuhrman, F. A. Tetrodotoxin: Occurrence in Atelopid frogs of Costa Rica. Science 1975, 189, 151-152.
5. Habermehl, G. The steroid alkaloids: The Salamandra group. In The Alkaloids; Manske, R. H. F., Ed.; Academic Press: New York, 1967; Vol. 9, pp 427-439.
6. Tokuyama, T.; Daly, J. W.; Witkop, B. The structure of batra-chotoxin, a steroidal alkaloid from the Colombian arrow poison frog Phyllobates aurotaenia and partial synthesis of batra-chotoxin and its analogs and homologs. J. Am. Chem. Soc. 1969, 91, 3931-3938.
7. Dumbacher, J. P.; Beehler, B. M.; Spande, T. F.; Garraffo, H. M.; Daly, J. W. Homobatrachotoxin in the genus Pitohui: Chemical defense in birds? Science 1992, 258, 799-801.
8. Dumbacher, J. P.; Spande, T. F.; Daly, J. W. Batrachotoxin alkaloids from passerine birds: A second toxic bird genus (Ifrita kowaldi) from New Guinea. Proc. Natl. Acad. Sci. U.S.A. 2000, 97, 12970-12975.
9. Daly, J. W.; Myers, C. W. Toxicity of Panamanian poison frogs (Dendrobates): Some biological and chemical aspects. Science 1967, 156, 970-973.
10. Daly, J. W.; Tokuyama, T.; Fujiwara, T.; Highet, R. J.; Karle, I. L. A new class of indolizidine alkaloids from the poison frog, Dendrobates tricolor. X-ray analysis of 8-hydroxy-8-methyl-6-(2′-methylhexylidene)-1-azabicyclo[4.3.0]nonane. J. Am. Chem. Soc. 1980, 102, 830-836.
11. Daly, J. W. Thirty years of discovering arthropod alkaloids in amphibian skin. J. Nat. Prod. 1998, 61, 162-172.
12. Daly, J. W.; McNeal, E.; Gusovksy, F.; Ito, F.; Overman, L. E. Pumiliotoxin alkaloids: Relationship of cardiotonic activity to sodium channel activity and phosphatidylinositol turnover. J. Med. Chem. 1988, 31, 477-480.
13. Daly, J. W.; Gusovsky, F.; McNeal, E. T.; Secunda, S.; Bell, M.; Creveling, C. R.; Nishizawa, Y.; Overman, L. E.; Sharp, M. J.; Rossignol, D. P. Pumiliotoxin alkaloids: A new class of sodium channel agents. Biochem. Pharmacol. 1990, 40, 315-326.
14. Gusovsky, F.; Padgett, W. L.; Creveling, C. R.; Daly, J. W. Interaction of pumiliotoxin B with an "alkaloid-binding domain" on the voltage-dependent sodium channel. Mol. Pharmacol. 1992, 42, 1104-1108.
15. Daly, J. W.; Karle, I.; Myers, C. W.; Tokuyama, T.; Waters, J. A.; Witkop, B. Histrionicotoxins: Roentgen-ray analysis of the novel allenic and acetylenic spiroalkaloids isolated from a Colombian frog, Dendrobates histrionicus. Proc. Natl. Acad. Sci. U.S.A. 1971, 68, 1870-1875.
16. Spivak, C. E.; Maleque, M. A.; Oliveira, A. C.; Masukawa, L. M.; Tokuyama, T.; Daly, J. W.; Albuquerque, E. X. Actions of the histrionicotoxins at the ion channel of the nicotinic acetylcholine receptor and at the voltage-sensitive ion channels of muscle membranes. Mol. Pharmacol. 1982, 21, 351-361.
17. 3H]perhy-drohistrionicotoxin binding to Torpedo ocellata electroplax by effectors of the acetylcholine receptor. J. Biol. Chem. 1981, 256, 2843-2850.
18. Seamon, K. B.; Padgett, W. L.; Daly, J. W. Forskolin: Unique diterpene activator of adenylate cyclase in membranes and in intact cells. Proc. Natl. Acad. Sci. U.S.A. 1981, 78, 3363-3367.
19. Spande, T. F.; Edwards, M. W.; Pannell, L. K.; Daly, J. W. Pseudophrynamine A: An unusual prenyl pyrrolo[2,3-b]indole ester from an Australian frog, Pseudophryne coriacea (Myobatrachidae). J. Org. Chem. 1988, 53, 1222-1226.
20. Badio, B.; Garraffo, H. M.; Padgett, W. L.; Greig, N. H.; Daly, J. W. Pseudophrynaminol: A potent noncompetitive blocker of nicotinic receptor-channels. Biochem. Pharmacol. 1997, 53, 671-676.
21. Daly, J. W.; Nishizawa, Y.; Edwards, M. W.; Waters, J. A.; Aronstam, R. S. Nicotinic receptor-elicited sodium flux in rat pheochromocytoma PC12 cells: Effects of agonists, antagonists, and noncompetitive blockers. Neurochem. Res. 1991, 16, 489-500.
22. Badio, B.; Shi, D.; Shin, Y.; Hutchinson, K. D.; Padgett, W. L.; Daly, J. W. Spiropyrrolizidines: A new class of blockers of nicotinic receptors. Biochem. Pharmacol. 1996, 52, 933-939.
23. Daly, J. W.; Garraffo, H. M.; Pannell, L. K.; Spande, T. F. Alkaloids from Australian frogs (Myobatrachidae): Pseudo-phrynamines and pumiliotoxins. J. Nat. Prod. 1990, 53, 407-421.
24. Smith, B. P.; Tyler, K. M. J.; Kaneko, T.; Garraffo, H. M.; Spande, T. F.; Daly, J. W. Evidence for biosynthesis of pseudophrynamine alkaloids by an Australian myobatrachid frog (Pseudophryne) and sequestration of dietary pumiliotoxins. Proc. Natl. Acad. Sci. U.S.A. 2002, 65, 439-447.
25. Spande, T. F.; Garraffo, H. M.; Edwards, M. W.; Yeh, H. J. C.; Pannell, L.; Daly, J. W. Epibatidine: A novel (chloropyridyl)-azabicycloheptane with potent analgesic activity from an Ecuadoran poison frog. J. Am. Chem. Soc. 1992, 114, 3475-3478.
26. Corey, E. J.; Leh, T.-P.; AchyuthaRao, S.; Daley, D. C.; Sarshar, S. Stereocontrolled total synthesis of (+)- and (-)-epibatidine. J. Org. Chem. 1993, 58, 5600-5602.
27. Badio, B.; Garraffo, H. M.; Spande, T. F.; Daly, J. W. Epibatidine: Discovery and definition as a potent analgesic and nicotinic agonist. Med. Chem. Res. 1994, 4, 440-448.
28. Daly, J. W.; Garraffo, H. M.; Spande, T. F.; Decker, M. W.; Sullivan, J. P.; Williams, M. Alkaloids from frog skin: the discovery of epibatidine and the potential for developing novel non-opioid analgesics. Nat. Prod. Rep. 2000, 17, 131-135.
29. Daly, J. W.; Garraffo, H. M.; Spande, T. F. Amphibian Alkaloids. In The Alkaloids; Cordell, G. A., Ed.; Academic Press: San Diego, CA, 1993; Vol. 43, 185-288.
30. Hutchinson, K. D.; Silverton, J. V.; Daly, J. W. Synthesis of pyrrolizidine oximes 222 and 236: Novel alkaloids of a dendrobatid poison frog. Tetrahedron 1994, 50, 6129-6136.
31. Garraffo, H. M.; Jain, P.; Spande, T. F.; Daly, J. W.; Jones, T. H.; Smith, L. J.; Zottig, V. E. Structure of alkaloid 275A, a novel 1-azabicyclo[5.3.0]decane from a dendrobatid frog, Dendrobates lehmanni: Synthesis of the tetrahydrodiastereomers. J. Nat. Prod. 2001, 64, 421-427.
32. Overman, L. E. New reactions for forming heterocycles and their use in natural products synthesis. Aldrichimica Acta 1995, 28, 107-120.
33. +-ATPase. Science 1980, 208, 503-505.
34. Daly, J. W.; Padgett, W. L.; Saunders, R. L.; Cover, J. F., Jr. Absence of tetrodotoxins in a captive-raised riparian frog, Atelopus varius. Toxicon 1997, 35, 705-709.
35. Daly, J. W.; Gusovsky, F.; Myers, C. W.; Yotsu-Yamashita, M.; Yasumoto, T. First occurrence of tetrodotoxin in a dendrobatid frog (Colostethus inguinalis), with further reports for the bufonid genus Atelopus. Toxicon 1994, 32, 279-285.
36. Daly, J. W.; Caceres, J.; Moni, R. W.; Gusovsky, F.; Moos, M., Jr.; Seamon, K. B.; Milton, K.; Myers, C. W. Frog secretions and hunting magic in the upper Amazon: Identification of a peptide that interacts with an adenosine receptor. Proc. Natl. Acad. Sci. U.S.A. 1992, 89, 10960-10963.
37. 35S]GTPγS to brain membranes. Cell. Mol. Neurobiol. 1995, 15, 465-493.
38. Daly, J. W.; Garraffo, H. M.; Spande, T. F. Alkaloids from Amphibian Skin. In Alkaloids: Chemical and Biological Perspectives; Pelletier, S. W., Ed.; Pergamon: New York, 1999; Vol. 13, pp 1-161.
39. Daly, J. W.; Garraffo, H. M.; Myers, C. W. The origin of frog skin alkaloids: An enigma. Pharm. News 1997, 4, 9-14.
40. Daly, J. W.; Secunda, S. I.; Garraffo, H. M.; Spande, T. F.; Wisnieski, A.; Cover, J. F. An uptake system for dietary alkaloids in poison frogs (Dendrobatidae). Toxicon 1994, 32, 657-663.
41. Daly, J. W.; Garraffo, H. M.; Hall, G. S. E.; Cover, J. F., Jr. Absence of skin alkaloids in captive-raised Madagascan mantelline frogs (Mantella) and sequestration of dietary alkaloids. Toxicon 1997, 35, 1131-1135.
42. Jones, T. H.; Gorman, J. S. T.; Snelling, R. R.; Delabie, J. H. C.; Blum, M. S.; Garraffo, H. M.; Jain, P.; Daly, J. W.; Spande, T. F. Further alkaloids common to ants and frogs: Decahydroquinolines and a quinolizidine. J. Chem. Ecol. 1999, 25, 1179-1193.
43. Daly, J. W.; Kaneko, T.; Wilham, J.; Garraffo, H. M.; Spande, T. F.; Espinosa, A.; Donnelly, M. A. Bioactive alkaloids of frog skin: Combinatorial bioprospecting reveals that pumiliotoxins have an arthropod source. Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 13996-14001.
44. Garraffo, H. M.; Spande, T. F.; Jones, T. H.; Daly, J. W. Ammonia chemical ionization tandem mass spectrometry in structure determination of alkaloids. I. Pyrrolidines, piperidines, decahydroquinolines, pyrrolizidines, indolizidines, quinolizidines and an azabicyclo[5.3.0]decane. Rapid Commun. Mass Spectrom. 1999, 13, 1553-1563.
45. Garraffo, H. M.; Spande, T. F.; Jain, P.; Kaneko, T.; Jones, T. H.; Blum, M. S.; Ali, T. M. M.; Snelling, R. R.; Isbell, L. A.; Robertson, H. G.; Daly, J. W. Ammonia chemical ionizationtandem mass spectrometry in structure determination of alkaloids. II. Tetraponerines from pseudomyrmicine ants. Rapid Commun. Mass Spectrom. 2001, 15, 1409-1415.
46. Garraffo, H. M.; Simon, L. D.; Daly, J. W.; Spande, T. F.; Jones, T. H. Cis- and trans-configurations of α,α′-disubstituted piperidines and pyrrolidines by GC-FTIR; Application to decahydroquinoline stereochemistry. Tetrahedron 1994, 50, 11329-11338.
47. 13C NMR in their conformational analysis. J. Nat. Prod. 1999, 62, 5-21.
48. Garraffo, H. M.; Spande, T. F.; Daly, J. W.; Baldessari, A.; Gros, E. G. Alkaloids from bufonid toads (Melanophryniscus): Decahydroquinolines, pumiliotoxins and homopumiliotoxins, indoliz-idines, pyrrolizidines, and quinolizidines. J. Nat. Prod. 1993, 56, 357-373.
49. Garraffo, H. M.; Caceres, J.; Daly, J. W.; Spande, T. F.; Andriamaharavo, N. R.; Andriantsiferana, M. Alkaloids in Madagascan frogs (Mantella): Pumiliotoxins, indolizidines, quinolizidines, and pyrrolizidines. J. Nat. Prod. 1993, 56, 1016-1038.
50. Daly, J. W.; Andriamaharavo, N. R.; Andriantsiferana, M.; Myers, C. W. Madagascan poison frogs (Mantella) and their skin alkaloids. Am. Mus. Novit. 1996, No. 3177, 1-34.
51. Toyooka, N.; Fukutome, A.; Nemoto, H.; Daly, J. W.; Spande, T. F.; Garraffo, H. M.; Kaneko, T. Synthesis of alkaloid 223A and a structural revision. Org. Lett. 2002, 4, 1715-1717.
52. Jain, P.; Garraffo, M. H.; Yeh, H. J. C.; Spande, T. F.; Daly, J. W. A 1,4-disubstituted quinolizidine from a Madagascan mantelline frog (Mantella). J. Nat. Prod. 1996, 59, 1174-1178.
53. Jain, P.; Garraffo, H. M.; Spande, T. F.; Yeh, H. J. C.; Daly, J. W. A new subclass of alkaloids from a dendrobatid poison frog: A structure for deoxypumiliotoxin 251H. J. Nat. Prod. 1995, 58, 100-104.
54. Tokuyama, T.; Garraffo, H. M.; Spande, T. F.; Daly, J. W. A revised structure for alkaloid 205B, a novel 8β-azaacenaphthylene from a poison frog. Anal. Asoc. Quim. Argent. 1998, 86, 291-298.
55. Jain, P.; Spande, T. F.; Garraffo, H. M.; Daly, J. W. The isolation and structure of pumiliotoxin 341A: A novel cyclic ether from the frog Epipedobates tricolor. Heterocycles 1999, 50, 903-912.
56. Daly, J. W.; Myers, C. W.; Whittaker, N. Further classification of skin alkaloids from neotropical poison frogs (Dendrobatidae), with a general survey of toxic/noxious substances in the Amphibia. Toxicon 1987, 25, 1023-1095.