Historic Perspectives on Annonaceous Acetogenins from the Chemical Bench to Preclinical Trials

Chih-Chuang Liaw; Tung-Ying Wu; Fang-Rong Chang; Yang-Chang Wu

doi:10.1055/s-0030-1250006

Planta Medica, Inhaltsverzeichnis

Planta Med 2010; 76(13): 1390-1404
DOI: 10.1055/s-0030-1250006

Reviews

Historic Perspectives on Annonaceous Acetogenins from the Chemical Bench to Preclinical Trials

Chih-Chuang Liaw¹ ^, ² , Tung-Ying Wu³ , Fang-Rong Chang³ , Yang-Chang Wu³ ^, ⁴

¹Graduate Institute of Pharmaceutical Chemistry, College of Pharmacy, China Medical University, Taichung, Taiwan
²Department of Life Sciences, National Chung-Hsing University, Taichung, Taiwan
³Graduate Institute of Natural Products, Kaohsiung Medical University, Kaohsiung, Taiwan
⁴Cancer Center, Kaohsiung Medical University Hospital, Kaohsiung, Taiwan

Abstract

Studies on the Annonaceous acetogenins began after the first cytotoxic acetogenin, uvaricin, was isolated in 1982. This attractive finding made many medicinal and natural product chemists direct their efforts on the isolation and identification of these classes of compounds. As more Annonaceous acetogenins were isolated, more information about them was uncovered. From their structural identification to the total synthesis of natural product analogues and from cell-based screening and molecular-based targeting to animal testing, the mechanisms of action of the Annonaceous acetogenins became clearer. The purpose of this review is to give an account of recent studies on this class of compounds and their analogues, which will aid us not only in clarifying how the Annonaceous acetogenins act but also in establishing principles for the further development of this class of compounds.

Key words

Annonaceae - acetogenins - mitochondria complex I inhibitor - pesticidal activity - anticancer activity - apoptosis - acetogenin mimics

Volltext

Referenzen

References

1 Cragg G M, Newman D J, Snader K M. Natural products in drug discovery and development. J Nat Prod. 1997; 60 52-60
2 Wani M C, Taylor H L, Wall M E, Coggon P, McPhail A T. Plant antitumor agents. VI. Isolation and structure of taxol, a novel antileukemic and antitumor agent from Taxus brevifolia. J Am Chem Soc. 1971; 93 2325-2327
3 Wall M E, Wani M C, Cook C E, Palmer K H, McPhail A T, Sim G A. Plant antitumor agents. I. The isolation and structure of camptothecin, a novel alkaloidal leukemia and tumor inhibitor from Camptotheca acuminata. J Am Chem Soc. 1966; 88 3888-3890
4 Hartwell J L, Schrecker A W. Components of podophyllin. V. The constitution of podophyllotoxin. J Am Chem Soc. 1951; 73 2909-2916
5 Neuss N, Gorman M, Hargrove W, Cone N J, Biemann K, Buechi G, Manning R E. Vinca alkaloids. XXI. The structures of the oncolytic alkaloids vinblastine (VLB) and vincristine (VCR). J Am Chem Soc. 1964; 86 1440-1442
6 Arcamone F, Franceschi G, Penco S, Selva A. Adriamycin (14-hydroxydaunomycin), a novel antitumor antibiotic. Tetrahedron Lett. 1969; 13 1007-1010
7 Rupprecht J K, Hui Y H, McLaughlin J L. Annonaceous acetogenins: a review. J Nat Prod. 1990; 53 237-278
8 Zeng L, Ye Q, Oberlies H, Shi G, Gu Z M, He K, McLaughlin J L. Recent advances in annonaceous acetogenins. Nat Prod Rep. 1996; 13 275-306
9 Cave A, Figadere B, Laurens A, Cortes D. Acetogenins from Annonaceae. Progress in the chemistry of organic natural products, vol. 70. Berlin, Heidelberg; Springer Publisher 1997: 81-288
10 Bermejo A, Figadere B, Zafra-Polo M C, Barrachina I, Estornell E, Cortes D. Acetogenins from Annonaceae. Recent progress in isolation, synthesis, and mechanisms of action. Nat Prod Rep. 2005; 22 263-303
11 Leboeuf M, Cave A, Bhaumik P K, Mukherjee B, Mukherjee R. The phytochemistry of the Annonaceae. Phytochemistry. 1982; 21 2783-2813
12 Wu Y C. New research and development on the Formosan annonaceous plants. Atta-ur-Rahman Studies in natural products chemistry, vol. 33. Amsterdam; Elsevier B.V. 2006: 957-1024
13 Nakanishi Y, Chang F R, Liaw C C, Wu Y C, Bastow K F, Lee K H. Acetogenins as selective inhibitors of the human ovarian 1A9 tumor cell line. J Med Chem. 2003; 46 3185-3188
14 Jolad S D, Hoffmann J J, Schram K H, Cole J R. Uvaricin, a new antitumor agent from Uvaria accuminata (Annonaceae). J Org Chem. 1982; 47 3151-3153
15 McCloud T G, Smith D L, Chang C-J, Cassady J M. Annonacin, a novel, biologically active polyketide from Annona densicoma. Experientia. 1987; 43 947-949
16 Fujimoto Y, Eguchi T, Kakinuma K, Ikekawa N, Sahai M, Gupta Y K. Squamocin, a new cytotoxic bis-tetrahydrofuran containing acetogenin from Annona squamosa. Chem Pharm Bull. 1988; 36 4802-4806
17 Hui Y H, Rupprecht J K, Anderson J E, Liu Y M, Smith D L, Chang C J, McLaughlin J L. Bullatalicin, a novel bioactive acetogenin from Annona bullata (Annonaceae). Tetrahedron. 1989; 45 6941-6948
18 Cortes D, Rios J L, Villar A, Valverde S. Cherimoline et dihydrocherimoline: deux nouvelles γ-lactones bis-tetrahydrofuranniques possedant une activite antimicrobienne. Tetrahedron Lett. 1984; 25 3199-3202
19 Cortes D, Myint S H, Dupont B, Davoust D. Acetogenins of the Annonaceae. Part 20. Bioactive acetogenins from seeds of Annona cherimolia. Phytochemistry. 1993; 32 1475-1482
20 Rios J L, Cortes D, Valverde S. Acetogenins, aporphinoids, and azaanthraquinone from Annona cherimolia seeds. Planta Med. 1989; 55 321-323
21 Hoye T R, Suhadolnik J C. On the stereochemistry of the bistetrahydrofuranyl moiety of uvaricin. Proton chemical shifts can play a crucial role in complex structure determination. J Am Chem Soc. 1987; 109 4402-4403
22 Hoye T R, Zhuang Z P. Validation of the proton NMR chemical shift method for determination of stereochemistry in the bistetrahydrofuranyl moiety of uvaricin-related acetogenins from Annonaceae: rolliniastatin 1 (and asimicin). J Org Chem. 1988; 53 5578-5580
23 Pettit G R, Cragg G M, Polonsky J, Herald D L, Goswami A, Smith C R, Moretti C, Schmidt J M, Weisleder D. Isolation and structure of rolliniastat 1 from the South American tree Rollinia mucosa. Can J Chem. 1987; 65 1433-1435
24 Hui Y H, Rupprecht J K, Liu Y M, Anderson J E, Smith D L, Chang C J, McLaughlin J L. Bullatacin and bullatacinone: two highly potent bioactive acetogenins from Annona bullata. J Nat Prod. 1989; 52 463-477
25 Gawronski J, Wu Y C. A note on the determination of absolute configuration of acetogenins by circular dichroism. Polish J Chem. 1999; 73 241-243
26 Born L, Lieb F, Lorentzen J P, Moeschler H, Nonfon M, Soellner R, Wendisch D. The relative configuration of acetogenins isolated from Annona squamosa: annonin I (squamocin) and annonin VI. Planta Med. 1990; 56 312-316
27 Hoye T R, Suhadolnik J C. Symmetry-assisted synthesis of triepoxide stereoisomers of E,Z,E-dodeca-2,6,10-trien-1,12-diol and their cascade reactions to 2, 5-linked bistetrahydrofurans. J Am Chem Soc. 1985; 107 5312-5313
28 Huang T S. Flora of Taiwan, vol. 2. Taipei; Lungwei Printing Co. Ltd. 1996: 415-419
29 Liao J C. A list of scientific names of woody plants in Taiwan. Taipei; College of Agriculture, National Taiwan University 1993
30 Wu Y C, Chang G Y, Ko F N, Teng C M. Bioactive constituents from the stems of Annona montana. Planta Med. 1995; 61 146-149
31 Chen K S, Ko F N, Teng C M, Wu Y C. Antiplatelet and vasorelaxing actions of some aporphinoids. Planta Med. 1996; 62 133-136
32 Lin C H, Yang C M, Ko F N, Wu Y C, Teng C M. Antimuscarinic action of liriodenine, isolated form Fissistigma glaucescens, in canine tracheal smooth muscle. Br J Pharmacol. 1994; 113 1464-1470
33 Chang G J, Wu M H, Wu Y C, Su M J. Electrophysiological mechanisms for antiarrhythmic efficacy and positive inotropy of liriodenine, a natural aporphine alkaloid from Fissistigma glaucescens. Br J Pharmacol. 1996; 118 1571-1583
34 Ko F N, Yu S M, Su M J, Wu Y C, Teng C M. Pharmacological activity of (−)-discretamine, a novel vascular α-adrenoceptor and 5-hydroxytryptamine receptor antagonist, isolated from Fissistigma glaucescens. Br J Pharmacol. 1993; 110 882-888
35 Wu Y C, Chang F R, Duh C Y, Wang S K, Wu T S. Cytotoxic styrylpyrrones of Goniothalamus amuyon. Phytochemistry. 1992; 31 2851-2853
36 Wu Y C, Duh C Y, Chang F R, Chang G Y, Wang S K, Chang J J, McPhail D R, McPhail A T, Lee K H. The crystal structure and cytotoxicity of goniodiol-7-monoacetate from Goniothalamus amuyon. J Nat Prod. 1991; 54 1077-1081
37 Wu Y C, Chang F R, Chen K S, Liang S C, Lee M R. Studies on acetogenins from Formosan Annonaceous plants. 3. Diepoxymontin, a novel acetogenin from Annona montana. Heterocycles. 1994; 38 1475-1478
38 Wu Y C, Chang F R, Duh C Y, Wang S K. Annoreticuin and isoannoreticuin: two new cytotoxic acetogenins from Annona reticulata. Heterocycles. 1992; 34 667-674
39 Chang F R, Wu Y C, Duh C Y, Wang S K. Studies on the acetogenins of Formosan Annonaceous plants, II. Cytotoxic acetogenins from Annona reticulata. J Nat Prod. 1993; 56 1688-1694
40 Zhang L, Yang R, Wu X. Chemical compositions of Goniothalamus howii (I). Zhiwu Xuebao. 1993; 35 390-396
41 Yu J, Luo X, Sun L, Liu C, Hong S, Ma L. Squamostatin-B, a new polyketide from Annona squamosa (Annonaceae). Chin Chem Lett. 1993; 4 423-426
42 Li C M, Mu Q, Hao X J, Sun H D, Zheng H L, Wu Y C. Three new bioactive Annonaceous acetogeninins from Annona muricata. Chin Chem Lett. 1994; 5 747-750
43 Londershausen M, Leicht W, Lieb F, Moeschler H, Weiss H. Molecular mode of action of annonins. Pestic Sci. 1991; 33 427-438
44 Gu Z M, Fang X P, Miesbauer L R, Smith D L, McLaughlin J L. 30-, 31-, and 32-hydroxybullatacinones: bioactive terminally hydroxylated Annonaceous acetogenins from Annona bullata. J Nat Prod. 1993; 56 870-876
45 Gu Z M, Fang X P, Rieser M J, Hui Y H, Miesbauer L R, Smith D L, Wood K V, McLaughlin J L. New cytotoxic Annonaceous acetogenins: bullatanocin and cis- and trans-bullatanocinone, from Annona bullata (Annonaceae). Tetrahedron. 1993; 49 747-754
46 Gu Z M, Fang X P, Zeng L, Wood K V, McLaughlin J L. Bullacin: a new cytotoxic Annonaceous acetogenin from Annona bullata. Heterocycles. 1993; 36 2221-2228
47 Zafra-Polo M C, Figadere B, Gallardo T, Tormo J R, Cortes D. Natural acetogenins from Annonaceae, synthesis and mechanisms of action. Phytochemistry. 1998; 48 1087-1117
48 Rieser M J, Kozlowski J F, Wood K V, McLaughlin J L. Muricatacin: a simple biologically active acetogenin derivative from the seeds of Annona muricata (Annonaceae). Tetrahedron Lett. 1991; 32 1137-1140
49 Rieser M J, Hui Y H, Rupprecht J K, Kozlowski J F, Wood K V, McLaughlin J L, Hanson P R, Zhuang Z, Hoye T R. Determination of absolute configuration of stereogenic carbinol centers in Annonaceous acetogenins by proton and fluorine-19 NMR analysis of Mosher ester derivatives. J Am Chem Soc. 1992; 114 10203-10213
50 Fujimoto Y, Murasaki C, Shimada H, Nishioka S, Kakinuma K, Singh S, Singh M, Gupta Y K, Sahai M. Annonaceous acetogenins from the seeds of Annona squamosa. Non-adjacent bis-tetrahydrofuranic acetogenins. Chem Pharm Bull. 1994; 42 1175-1184
51 Yu J G, Hu X E, Ho D K, Bean M F, Stephens R E, Cassady J M, Brinen L S, Clardy J. Absolute stereochemistry of (+)-gigantecin from Annona coriacea (Annonaceae). J Org Chem. 2002; 59 1598-1599
52 Duret P, Laurens A, Hocquemiller R, Cortex D, Cave A. Acetogenins of Annonaceae. 34. Isoacetogenins, artifacts issued from translacationization from annonaceous acetogenins. Heterocycles. 1994; 39 741-749
53 Duret P, Figadere B, Hocquemiller R, Cave A. Epimerization of Annonaceous acetogenins under basic conditions. Tetrahedron Lett. 1997; 38 8849-8852
54 Hopp D C, Conway W D, McLaughlin J L. Using countercurrent chromatography to assist in the purification of new Annonaceous acetogenins from Annona squamosa. Phytochem Anal. 1999; 10 339-347
55 Duret P, Waechter A I, Margraff R, Foucault A, Hocquemiller R, Cave A. High-speed countercurrent chromatography: a promising method for the separation of the Annonaceous acetogenins. J Liq Chromatogr Relat Technol. 1997; 20 627-635
56 Duret P, Waechter A-I, Figadere B, Hocquemiller R, Cave A. Determination of absolute configurations of carbinols of Annonaceous acetogenins with 2-naphthylmethoxyacetic acid esters. J Org Chem. 1998; 63 4717-4720
57 Hirayama K, Akashi S, Yuji R, Niitsu U, Fujimoto Y. Structural studies of polyhydroxybis(tetrahydrofuran) acetogenins from Annona squamosa using the combination of chemical derivatization and precursor-ion scanning mass spectrometry. Org Mass Spectrom. 1993; 28 1516-1524
58 Gu Z M, Zhou D, Wu J, Shi G, Zeng L, McLaughlin J L. Screening for Annonaceous acetogenins in bioactive plant extracts by liquid chromatography/mass spectrometry. J Nat Prod. 1997; 60 242-248
59 Chang F R, Wu Y C. Novel cytotoxic Annonaceous acetogenins from Annona muricata. J Nat Prod. 2001; 64 925-931
60 Chang F R, Liaw C C, Lin C Y, Chou C J, Chiu H F, Wu Y C. New adjacent bis-tetrahydrofuran Annonaceous acetogenins from Annona muricata. Planta Med. 2003; 69 241-246
61 Liaw C C, Chang F R, Wu C C, Chen S L, Bastow Kenneth F, Hayashi K I, Nozaki H, Lee K H, Wu Y C. Nine new cytotoxic monotetrahydrofuranic Annonaceous acetogenins from Annona montana. Planta Med. 2004; 70 948-959
62 Liaw C C, Chang F R, Wu M J, Wu Y C. A novel constituent from Rollinia mucosa, rollicosin, and a new approach to develop Annonaceous acetogenins as potential antitumor agents. J Nat Prod. 2003; 66 279-281
63 Xie H H, Wei X Y, Wang J D, Liu M F, Yang R Z. A new cytotoxic acetogenin from the seeds of Annona squamosa. Chin Chem Lett. 2003; 14 588-590
64 Wolvetang E J, Johnson K L, Krauer K, Ralph S J, Linnane A W. Mitochondrial respiratory chain inhibitors induce apoptosis. FEBS Lett. 1994; 339 40-44
65 Chih H W, Chiu H F, Tang K S, Chang F R, Wu Y C. Bullatacin, a potent antitumor Annonaceous acetogenin, inhibits proliferation of human hepatocarcinoma cell line 2.2.15 by apoptosis induction. Life Sci. 2001; 69 1321-1331
66 Cartagena E, Colom O A, Neske A, Valdez J C, Bardon A. Effects of plant lactones on the production of biofilm of Pseudomonas aeruginosa. Chem Pharm Bull. 2007; 55 22-25
67 Ahammadsahib K I, Hollingworth R M, McGovren J P, Hui Y H, McLaughlin J L. Mode of action of bullatacin: a potent antitumor and pesticidal Anonaceous acetogenin. Life Sci. 1993; 53 1113-1120
68 Degli Esposti M, Ghelli A, Ratta M, Cortes D, Estornell E. Natural substances (acetogenins) from the family Annonaceae are powerful inhibitors of mitochondrial NADH dehydrogenase (complex I). Biochem J. 1994; 301 161-167
69 Oberlies N H, Jones J L, Corbett T H, Fotopoulos S S, McLaughlin J L. Tumor cell growth inhibition by several Anonaceous acetogenins in an in vitro disk diffusion assay. Cancer Lett. 1995; 96 55-62
70 Oberlies N H, Croy V L, Harrison M L, McLaughlin J L. The Anonaceous acetogenin bullatacin is cytotoxic against multidrug-resistant human mammary adenocarcinoma cells. Cancer Lett. 1997; 115 73-79
71 Shimada H, Grutzner J B, Kozlowski J F, McLaughlin J L. Membrane conformations and their relation to cytotoxicity of asimicin and its analogs. Biochemistry. 1998; 37 854-866
72 Kuwabara K, Takada M, Iwata J, Tatsumoto K, Sakamoto K, Iwamura H, Miyoshi H. Design syntheses and mitochondrial complex I inhibitory activity of novel acetogenin mimics. Eur J Biochem. 2000; 267 2538-2546
73 Yuan S S F, Chang H L, Chen H W, Yeh Y T, Kao Y H, Lin K H, Wu Y C, Su J H. Annonacin, a mono-tetrahydrofuran acetogenin, arrests cancer cells at the G1 phase and causes cytotoxicity in a Bax- and caspase-3-related pathway. Life Sci. 2003; 72 2853-2861
74 Yuan S S F, Chang H L, Chen H W, Kuo F C, Liaw C C, Su J H, Wu Y C. Selective cytotoxicity of squamocin on T24 bladder cancer cells at the S-phase via a Bax-, Bad-, and caspase-3-related pathways. Life Sci. 2006; 78 869-874
75 Lu M C, Yang S H, Hwang S L, Lu Y J, Lin Y H, Wang S R, Wu Y C, Lin S R. Induction of G2/M phase arrest by squamocin in chronic myeloid leukemia (K562) cells. Life Sci. 2006; 78 2378-2383
76 Rupprecht J K, Chang C J, Cassady J M, McLaughlin J L, Mikolajczak K L, Weisleder D. Asimicin, a new cytotoxic and pesticidal acetogenin from the pawpaw, Asimina triloba (Annonaceae). Heterocycles. 1986; 24 1197-1201
77 Ratnayake S, Rupprecht J K, Potter W M, McLaughlin J L. Evaluation of various parts of the paw paw tree, Asimina triloba (Annonaceae), as commercial sources of the pesticidal Anonaceous acetogenins. J Econ Entomol. 1992; 85 2353-2356
78 He K, Zeng L, Ye Q, Shi G, Oberlies N H, Zhao G X, Njoku C J, McLaughlin J L. Comparative structure-activity relationship evaluations of Anonaceous acetogenins for pesticidal activity. Pestic Sci. 1997; 49 372-378
79 Alali F Q, Kaakeh W, Bennett G W, McLaughlin J L. Annonaceous acetogenins as natural pesticides: potent toxicity against insecticide-susceptible and -resistant German cockroaches (Dictyoptera: Blattellidae). J Econ Entomol. 1998; 91 641-649
80 Ohsawa K, Atsuzawa S, Mitsui T, Yamamoto I. Isolation and insecticidal activity of three acetogenins from seeds of pond apple, Annona glabra L. Nippon Noyaku Gakkaishi. 1991; 16 93-96
81 Guadano A, Gutierrez C, De la Pena E, Cortes D, Gonzalez-Coloma A. Insecticidal and mutagenic evaluation of two Anonaceous acetogenins. J Nat Prod. 2000; 63 773-776
82 Lewis M A, Arnason J T, Philogene B J R, Rupprecht J K, McLaughlin J L. Inhibition of respiration at site I by asimicin, an insecticidal acetogenin of the pawpaw, Asimina triloba (Annonaceae). Pestic Biochem Physiol. 1993; 45 15-23
83 Friedrich T, Ohnishi T, Forche E, Kunze B, Jansen R, Trowitzsch W, Hoefle G, Reichenbach H, Weiss H. Two binding sites for naturally occurring inhibitors in mitochondrial and bacterial NADH : ubiquinone oxidoreductase (complex I). Biochem Soc Trans. 1994; 22 226-230
84 Hollingworth R M, Ahammadsahib K I, Gadelhak G, McLaughlin J L. New inhibitors of complex I of the mitochondrial electron transport chain with activity as pesticides. Biochem Soc Trans. 1994; 22 230-233
85 Miyoshi H, Ohshima M, Shimada H, Akagi T, Iwamura H, McLaughlin J L. Essential structural factors of Annonaceous acetogenins as potent inhibitors of mitochondrial complex I. Biochim Biophys Acta. 1998; 1365 443-452
86 Miyoshi H. Inhibitors of mitochondrial respiratory enzymes. J Pestic Sci. 2005; 30 120-121
87 Takada M, Kuwabara K, Nakato H, Tanaka A, Iwamura H, Miyoshi H. Definition of crucial structural factors of acetogenins, potent inhibitors of mitochondrial complex I. Biochim Biophys Acta. 2000; 1460 302-310
88 Murai M, Ichimaru N, Abe M, Nishioka T, Miyoshi H. Synthesis of photolabile Δlac-acetogenin for photoaffinity labeling of mitochondrial complex I. J Pestic Sci. 2006; 31 156-158
89 Ichimaru N, Yoshinaga N, Nishioka T, Miyoshi H. Effect of stereochemistry of Δlac-acetogenins on the inhibition of mitochondrial complex I (NADH-ubiquinone oxidoreductase). Tetrahedron. 2007; 63 1127-1139
90 Myint S H, Laurens A, Hocquemiller R, Cave A, Davoust D, Cortes D. Murisolin: a new cytotoxic mono-tetrahydrofuran-γ-lactone from Annona muricata. Heterocycles. 1990; 31 861-867
91 Hattori Y, Kimura Y, Moroda A, Konno H, Abe M, Miyoshi H, Goto T, Makabe H. Synthesis of murisolin, (15R,16R,19R,20S)-murisolin A, and (15R,16R,19S,20S)-16,19-cis-murisolin and their inhibitory action with bovine heart mitochondrial complex I. Chem Asian J. 2006; 1 894-904
92 Ye Q, Zeng L, Zhang Y, Zhao G X, McLaughlin J L, Woo M H, Evert D R. Longicin and goniothalamicinone: novel bioactive monotetrahydrofuran acetogenins from Asimina longifolia. J Nat Prod. 1995; 58 1398-1406
93 Hanessian S, Giroux S, Buffat M. Total synthesis and structural confirmation of (+)-longicin. Org Lett. 2005; 7 3989-3992
94 Gleye C, Duret P, Laurens A, Hocquemiller R, Cave A. cis-Monotetrahydrofuran acetogenins from the roots of Annona muricata. J Nat Prod. 1998; 61 576-579
95 Goksel H, Stark C B W. Total synthesis of cis-solamin: exploiting the RuO₄-catalyzed oxidative cyclization of dienes. Org Lett. 2006; 8 3433-3436
96 Zhao H, Gorman J S T, Pagenkopf B L. Advances in Lewis acid controlled carbon-carbon bond-forming reactions enable a concise and convergent total synthesis of bullatacin. Org Lett. 2006; 8 4379-4382
97 Keum G, Hwang C H, Kang S B, Kim Y, Lee E. Stereoselective syntheses of rolliniastatin 1, rollimembrin, and membranacin. J Am Chem Soc. 2005; 127 10396-10399
98 Gonzalez M C, Tormo J R, Bermejo A, Zafra-Polo M C, Estornell E, Cortes D. Rollimembrin, a novel acetogenin inhibitor of mammalian mitochondrial complex I. Bioorg Med Chem Lett. 1997; 7 1113-1118
99 He K, Shi G, Zhao G X, Ye Q, Schwedler J T, Wood K V, McLaughlin J L. Three new adjacent bis-tetrahydrofuran acetogenins with four hydroxyl groups from Asimina triloba. J Nat Prod. 1996; 59 1029-1034
100 Nattrass G L, Diez E, McLachlan M M, Dixon D J, Ley S V. The total synthesis of the Annonaceous acetogenin 10-hydroxyasimicin. Angew Chem Int Ed Engl. 2005; 44 580-584
101 Saez J, Sahpaz S, Villaescusa L, Hocquemiller R, Cave A, Cortes D. Acetogenins of the Annonaceae. 18. Rioclarin and membranacin, two new bis-tetrahydrofuran acetogenins of the seeds of Rollinia membranacea. J Nat Prod. 1993; 56 351-356
102 Marshall J A, Sabatini J J. An outside-in approach to adjacent bistetrahydrofuran Annonaceous acetogenins with C ₂ core symmetry. Total synthesis of asimicin and a C32 analogue. Org Lett. 2006; 8 3557-3560
103 Ye Q, He K, Oberlies N H, Zeng L, Shi G, Evert D, McLaughlin J L. Longimicins A – D: novel bioactive acetogenins from Asimina longifolia (Annonaceae) and structure-activity relationships of asimicin type of annonaceous acetogenins. J Med Chem. 1996; 39 1790-1796
104 Tominaga H, Maezaki N, Yanai M, Kojima N, Urabe D, Ueki R, Tanaka T. First total synthesis of longimicin D. Eur J Org Chem. 2006; 2006 1422-1429
105 Shi G, Kozlowski J F, Schwedler J T, Wood K V, MacDougal J M, McLaughlin J L. Muconin and mucoxin: additional nonclassical bioactive acetogenins from Rollinia mucosa. J Org Chem. 1996; 61 7988-7989
106 Narayan R S, Borhan B. Synthesis of the proposed structure of mucoxin via regio- and stereoselective tetrahydrofuran ring-forming strategies. J Org Chem. 2006; 71 1416-1429
107 Shi G, Zheng L, Gu Z-M, MacDougal J M, McLaughlin J L. Absolute stereochemistries of sylvaticin and 12,15-cis-sylvaticin, bioactive C-20,23-cis nonadjacent bistetrahydrofuran Annonaceous acetogenins, from Rollinia mucosa. Heterocycles. 1995; 41 1785-1796
108 Donohoe T J, Harris R M, Burrows J, Parker J. Total synthesis of (+)-cis-sylvaticin: double oxidative cyclization reactions catalyzed by osmium. J Am Chem Soc. 2006; 128 13704-13705
109 Alkofahi A, Rupprecht J K, Liu Y M, Chang C J, Smith D L, McLaughlin J L. Gigantecin: a novel antimitotic and cytotoxic acetogenin, with nonadjacent tetrahydrofuran rings, from Goniothalamus giganteus (Annonaceae). Experientia. 1990; 46 539-541
110 Hoye T R, Eklov B M, Jeon J, Khoroosi M. Sequencing of three-component olefin metatheses: total synthesis of either (+)-gigantecin or (+)-14-deoxy-9-oxygigantecin. Org Lett. 2006; 8 3383-3386
111 Chavez D, Acevedo L A, Mata R. Jimenezin, a novel Annonaceous acetogenin from the seeds of Rollinia mucosa containing adjacent tetrahydrofuran-tetrahydropyran ring systems. J Nat Prod. 1998; 61 419-421
112 Bandur N G, Bruckner D, Hoffmann R W, Koert U. Total synthesis of jimenezin via an intramolecular allylboration. Org Lett. 2006; 8 3829-3831
113 Shi G, Alfonso D, Fatope M O, Zeng L, Gu Z M, Zhao G X, He K, MacDougal J M, McLaughlin J L. Mucocin: a new Annonaceous acetogenin bearing a tetrahydropyran ring. J Am Chem Soc. 1995; 117 10409-10410
114 Crimmins M T, Zhang Y, Diaz F A. Total synthesis of (−)-mucocin. Org Lett. 2006; 8 2369-2372
115 Alali F Q, Rogers L, Zhang Y, McLaughlin J L. Unusual bioactive Annonaceous acetogenins from Goniothalamus giganteus. Tetrahedron. 1998; 54 5833-5844
116 Strand D, Rein T. Total synthesis of pyranicin. Org Lett. 2004; 7 199-202
117 Strand D, Rein T. Synthesis of pyragonicin. Org Lett. 2005; 7 2779-2781
118 Takahashi S, Ogawa N, Koshino H, Nakata T. Total synthesis of the proposed structure for pyragonicin. Org Lett. 2005; 7 2783-2786
119 Quinn K J, Isaacs A K, DeChristopher B A, Szklarz S C, Arvary R A. Asymmetric total synthesis of rollicosin. Org Lett. 2005; 7 1243-1245
120 Makabe H, Kimura Y, Higuchi M, Konno H, Murai M, Miyoshi H. Synthesis of (4R,15R,16R,21S)- and (4R,15S,16S,21S)-rollicosin, squamostolide, and their inhibitory action with bovine heart mitochondrial complex I. Bioorg Med Chem. 2006; 14 3119-3130
121 Hoppen S, Emde U, Friedrich T, Grubert L, Koert U. Natural-product hybrids: design, synthesis, and biological evaluation of quinone-Annonaceous acetogenins. Angew Chem Int Ed Engl. 2000; 39 2099-2102
122 Arndt S, Emde U, Baurle S, Friedrich T, Grubert L, Koert U. Quinone-Annonaceous acetogenins: synthesis and complex I inhibition studies of a new class of natural product hybrids. Chem Eur J. 2001; 7 993-1005
123 Duval R, Lewin G, Hocquemiller R. Semisynthesis of heterocyclic analogues of squamocin, a cytotoxic annonaceous acetogenin, by an unusual oxidative decarboxylation reaction. Bioorg Med Chem. 2003; 11 3439-3446
124 Duval R A, Lewin G, Peris E, Chahboune N, Garofano A, Droese S, Cortes D, Brandt U, Hocquemiller R. Heterocyclic analogues of squamocin as inhibitors of mitochondrial complex I. On the role of the terminal lactone of Annonaceous acetogenins. Biochemistry. 2006; 45 2721-2728
125 Duval R A, Poupon E, Romero V, Peris E, Lewin G, Cortes D, Brandt U, Hocquemiller R. Analogues of cytotoxic squamocin using reliable reactions: new insights into the reactivity and role of the α,β-unsaturated lactone of the Annonaceous acetogenins. Tetrahedron. 2006; 62 6248-6257
126 Kojima N, Fushimi T, Maezaki N, Tanaka T, Yamori T. Synthesis of hybrid acetogenins, α,β-unsaturated-γ-lactone-free nitrogen-containing heterocyclic analogues, and their cytotoxicity against human cancer cell lines. Bioorg Med Chem Lett. 2008; 18 1637-1641
127 Zeng B B, Wu Y, Yu Q, Wu Y L, Li Y, Chen X G. Enantiopure simple analogues of Annonaceous acetogenins with remarkable selective cytotoxicity towards tumor cell lines. Angew Chem Int Ed. 2000; 39 1934-1937
128 Rodier S, Le Huerou Y, Renoux B, Doyon J, Renard P, Pierre A, Gesson J P, Gree R. Synthesis and cytotoxic activity of acetogenin analogues. Bioorg Med Chem Lett. 2000; 10 1373-1375
129 Yao Z J, Wu H P, Wu Y L. Polyether mimics of naturally occurring cytotoxic Annonaceous acetogenins. J Med Chem. 2000; 43 2484-2487
130 Jiang S, Liu Z H, Sheng G, Zeng B B, Cheng X G, Wu Y L, Yao Z J. Mimicry of Annonaceous acetogenins: enantioselective synthesis of a (4R)-hydroxy analogue having potent antitumor activity. J Org Chem. 2002; 67 3404-3408
131 Zeng B B, Wu Y, Jiang S, Yu Q, Yao Z J, Liu Z H, Li H Y, Li Y, Chen X G, Wu Y L. Studies on mimicry of naturally occurring Annonaceous acetogenins: non-THF analogues leading to remarkable selective cytotoxicity against human tumor cells. Chem Eur J. 2003; 9 282-290
132 Rodier S, Le Huerou Y, Renoux B, Doyon J, Renard P, Pierre A, Gesson J P, Gree R. New cytotoxic analogues of Annonaceous acetogenins. Anticancer Drug Des. 2001; 16 109-117
133 Fujita D, Ichimaru N, Abe M, Murai M, Hamada T, Nishioka T, Miyoshi H. Synthesis of non-THF analogs of acetogenin toward simplified mimics. Tetrahedron Lett. 2005; 46 5775-5779
134 Liu H X, Huang G R, Zhang H M, Wu J R, Yao Z J. Annonaceous acetogenin mimics bearing a terminal lactam and their cytotoxicity against cancer cells. Bioorg Med Chem Lett. 2007; 17 3426-3430
135 Liu H X, Shao F, Li G Q, Xun G L, Yao Z J. Tuning the acyclic ether moiety of anticancer agent AA005 with conformationally constrained fragments. Chem Eur J. 2008; 14 8632-8639
136 Ye Q, Shi G, He K, McLaughlin J L. Chlorinated Annonaceous acetogenins and their bioactivities. J Nat Prod. 1996; 59 994-996
137 Kojima N, Hayashi H, Suzuki S, Tominaga H, Maezaki N, Tanaka T, Yamori T. Synthesis of C4-fluorinated solamins and their growth inhibitory activity against human cancer cell lines. Bioorg Med Chem Lett. 2008; 18 6451-6453
138 Gallardo T, Saez J, Granados H, Tormo J R, Velez I D, Brun N, Torres B, Cortes D. 10-Oximeguanacone, the first nitrogenated acetogenin derivative found to be a potent inhibitor of mitochondrial complex I. J Nat Prod. 1998; 61 1001-1005
139 Duret P, Hocquemiller R, Gantier J C, Figadere B. Semisynthesis and cytotoxicity of amino acetogenins and derivatives. Bioorg Med Chem. 1999; 7 1821-1826
140 Derbre S, Roue G, Poupon E, Susin Santos A, Hocquemiller R. Annonaceous acetogenins: the hydroxyl groups and THF rings are crucial structural elements for targeting the mitochondria, demonstration with the synthesis of fluorescent squamocin analogues. Chembiochem. 2005; 6 979-982
141 Alexander M D, Burkart M D, Leonard M S, Portonovo P, Liang B, Ding X, Joullie M M, Gulledge B M, Aggen J B, Chamberlin A R, Sandler J, Fenical W, Cui J, Gharpure S J, Polosukhin A, Zhang H R, Evans P A, Richardson A D, Harper M K, Ireland C M, Vong B G, Brady T P, Theodorakis E A, La Clair J J. A central strategy for converting natural products into fluorescent probes. Chembiochem. 2006; 7 409-416
142 Maezaki N, Urabe D, Yano M, Tominaga H, Morioka T, Kojima N, Tanaka T. Synthesis of fluorescent solamin for visualization of cell distribution. Heterocycles. 2007; 73 159-164
143 Kojima N, Morioka T, Yano M, Suga Y, Maezaki N, Tanaka T. Convergent synthesis of fluorescence labeled solamin. Heterocycles. 2009; 79 387-393
144 Liu H X, Huang G R, Zhang H M, Jiang S, Wu J R, Yao Z J. A structure-activity guided strategy for fluorescent labeling of Annonaceous acetogenin mimetics and their application in cell biology. Chembiochem. 2007; 8 172-177
145 Zafra-Polo M C, Gonzalez M C, Estornell E, Sahpaz S, Cortes D. Acetogenins from Annonaceae, inhibitors of mitochondrial complex I. Phytochemistry. 1996; 42 253-271
146 Sasaki S, Naito H, Maruta K, Kawahara E, Maeda M. Novel calcium ionophores: supramolecular complexation by the hydroxylated-bistetrahydrofuran skeleton of potent antitumor annocnaceous acetogenins. Tetrahedron Lett. 1994; 35 3337-3340
147 Araya H, Fujimoto Y, Hirayama K. Structural elucidation of tetrahydrofuranic acetogenins by means of precursor-ion scanning method. Yuki Gosei Kagaku Kyokaishi. 1994; 52 765-777
148 Sasaki S, Maruta K, Naito H, Sugihara H, Hiratani K, Maeda M. New calcium-selective electrodes based on Annonaceous acetogenins and their analogs with neighboring bistetrahydrofuran. Tetrahedron Lett. 1995; 36 5571-5574
149 Sasaki S, Maruta K, Naito H, Maemura R, Kawahara E, Maeda M. Novel acyclic ligands for metal cations based on the adjacent bistetrahydrofuran as analogs of natural Annonaceous acetogenins. Tetrahedron. 1998; 54 2401-2410
150 Peyrat J F, Mahuteau J, Figadere B, Cave A. NMR studies of Ca²⁺ complexes of Annonaceous acetogenins. J Org Chem. 1997; 62 4811-4815
151 Wu S N, Chiang H T, Chang F R, Liaw C C, Wu Y C. Stimulatory effects of squamocin, an Annonaceous acetogenin, on Ca²⁺-activated K⁺ current in cultured smooth muscle cells of human coronary artery. Chem Res Toxicol. 2003; 16 15-22
152 Liaw C C, Yang Y L, Chen M, Chang F R, Chen S L, Wu S H, Wu Y C. Mono-tetrahydrofuran Annonaceous acetogenins from Annona squamosa as cytotoxic agents and calcium ion chelators. J Nat Prod. 2008; 71 764-771
153 Gu Z M, Zhou D, Lewis N J, Wu J, Johnson H A, McLaughlin J L, Gordon J. Quantitative evaluation of Annonaceous acetogenins in monthly samples of paw paw (Asimina triloba) twigs by liquid chromatography/electrospray ionization/tandem mass spectrometry. Phytochem Anal. 1999; 10 32-38
154 McLaughlin J L. Paw paw and cancer: Annonaceous acetogenins from discovery to commercial products. J Nat Prod. 2008; 71 1311-1321
155 Cuendet M, Oteham C P, Moon R C, Keller W J, Peaden P A, Pezzuto J M. Dietary administration of Asimina triloba (Paw Paw) extract increases tumor latency in N-methyl-N-nitrosourea-treated rats. Pharm Biol. 2008; 46 3-7
156 Escobar-Khondiker M, Hoellerhage M, Muriel M P, Champy P, Bach A, Depienne C, Respondek G, Yamada E S, Lannuzel A, Yagi T, Hirsch Etienne C, Oertel W H, Jacob R, Michel P P, Ruberg M, Hoeglinger G U. Annonacin, a natural mitochondrial complex I inhibitor, causes Tau pathology in cultured neurons. J Neurosci. 2007; 27 7827-7837

Dr. Yang-Chang Wu

Graduate Institute of Natural Products
Kaohsiung Medical University

100 Shih-Chuan 1st Road

703 Kaohsiung

Taiwan

Republic of China

Telefon: + 88 6 73 12 11 01ext. 21 97

Fax: + 88 6 73 11 47 73

eMail: yachwu@kmu.edu.tw