{ "labelLang" : "hun", "responseDate" : "2024-03-29 12:54", "content" : { "otype" : "JournalArticle", "mtid" : 32006395, "status" : "APPROVED", "published" : true, "comment" : "Cited By :86 \n Export Date: 10 May 2021 \n Correspondence Address: Kam, T.-S.; Department of Chemistry, , 50603 Kuala Lumpur, Malaysia \n Chemicals/CAS: Indole Alkaloids \n Funding details: 342 \n Funding details: Spectrum Pharmaceuticals \n Funding text 1: Bisiboga-type alkaloids are rare. The first member, the symmetrical dimer, bis(11-hydroxycoronaridin-12-yl) ( 511 ) isolated from Bonafousia tetrastachya ( T. siphilitica ) (313) , has been discussed previously ( 1 ). In the intervening years, only one other example has been encountered, obovatine ( 512 ), from Stemmadenia obovata , which is a derivative of 511 , in which one of the aromatic hydroxy substituents has been replaced by methoxy (314) . This is evident on comparison of the mass spectra and NMR spectral data with those of 512 . The loss of symmetry has resulted in a near doubling of the signals in both the 1 H and 13 C NMR spectra, with some of the signals coincident. The C(12) to C(12′) linkage was confirmed by a HMBC experiment, while methylation of 511 (CH 2 N 2 /Et 2 O) yielded both the monomethyl derivative 512 as well as the dimethyl derivative 513 . Alkaloid 511 and the monomer alkaloid, 11-hydroxycoronaridine were also present in this plant. XXIV Aspidosperma –Vobasine Type Bisindoles of this group appear to be rare. Capuvosidine ( 514 ), a pseudoaspidosperma–vobasine-type bisindole was isolated from Capuronetta elegans (1,315) . In the intervening period, only two bisindoles of the Aspidosperma –vobasine type, viz., tabernaemontabovine and tabernaemontavine, have been reported from Tabernaemontana bovina , occurring in Vietnam, in addition to two Aspidosperma – Aspidosperma bisindoles, methylenebismehranine and tabernaebovine, which were also isolated from the plant ( vide infra ). The structures which were initially attributed to tabernaemontabovine and tabernaemontavine (316) were subsequently revised to 515 and 516 , respectively, based on additional NMR data obtained (317) . Inspection of the 13 C NMR data revealed that a common mehranine unit is present in both alkaloids, while the vobasinyl parts in 515 and 516 were deduced by analogy to the vobasinyl parts of conoduramine and conodiparine A ( vide supra ), respectively. XXV Aspidosperma –Vincorine Type Vincarubine ( nm, and the appearance of a shoulder at 320 nm, compared to the original absorption maxima at 259 and 347 nm in the UV spectrum of 517 ), characterized by a dark-red color reminiscent of flexicorine ( 372 ), was isolated from Vinca minor (318,319) . As with flexicorine ( 372 ), vincarubine ( 517 ) on reduction with NaBH 4 in methanol afforded a yellow compound, presumably the phenol, which reverted spontaneously to the iminoquinone form 517 on exposure to air. Reduction of 517 with sodium dithionate followed by direct in situ acetylation of the product, allowed the phenol to be isolated as the stable acetate 518 . Addition of acid resulted in a hypsochromic shift to 343 518 . This behavior is diagnostic of vincorane-type compounds possessing a C 6 H 5 –N–C–N function and is consistent with the observed shift of the C(2′) resonance, from 104.0 in 517 to 94.7 in 518 , the latter value being close to that in vincorine ( 268 ) and N -demethylvincorine (320) . Comparison of the 13 C NMR spectral data of 517 and 518 with those of flexicorine ( 372 ) and dihydroflexicorine indicated a similarity of the vincorine moiety between these two groups of alkaloids. The other half of vincarubine ( 517 ) was readily identified from the remaining signals as belonging to 11-methoxy- N (1)-methylvincadifformine, by comparison with the 13 C NMR spectrum of vincadifformine ( 529 ). The assignment of the 13 C NMR data of 517 was facilitated by the application of 2-D NMR methods. Vincarubine inhibited incorporation of precursors of protein and nucleic acid synthesis into murine leukemia P388 cells. The effect was less compared to vincadifformine, but greater than that of vinblastine (319) . XXVI Aspidosperma –Macroline Type Pandicine ( nm) underwent a bathochromic shift above 350 nm with no appreciable change below 300 nm. Treatment of cm nm. 519 ) was isolated from Pandacastrum saccharatum as a brown amorphous solid. HREIMS yielded the formula C 44 H 50 N 4 O 7 , indicating a highly oxygenated molecule, while characteristic peaks at m/z 170 and 190 are typical of the N(1)-Me and N(4)-Me macroline skeleton. In alkaline medium, the UV spectrum (231, 234, 297, 307, 342 519 with MnO 2 in CHCl 3 resulted in quantitaive conversion into the iminoquinone 520 , which did not show the OH/NH band at 3400 −1 present in the IR spectrum of 519 . The UV spectrum of 520 was also markedly different from that of 519 , with absorption maxima at 233, 260, 288 (sh), and 396 The complete structure elucidation was based on analysis of the Hz), 5.85 (d, Hz), and 6.41 (s), are in agreement with an exocyclic 13 C NMR spectral data by comparison with the known bisindoles, criophylline ( 521 ) and villalstonine ( 322 ). The former contains a 3-substituted 14,15-tabersonine- β -epoxide moiety, while the latter contains a macroline unit. The 13 C NMR spectrum of 519 showed correspondence of all the non-aromatic 13 C shifts with those of criophylline, with the exception of C(3) which is shifted slightly upfield. Similarly, comparison of the remaining 13 C NMR shifts of 519 revealed analogy with the macroline half of villalstonine, with the exception of signals due to C(18′), C(19′), C(20′), and C(21′), reflecting the structural changes in this part of the molecule compared with villalstonine. The 1 H signals for H(18′), H(19′), and H(21′) at δ 5.05 (dd, J 16, 8 J 16 trans -disubstituted 18′, 19′ double bond as part of a diene system with the 20′, 21′ olefinic bond, as in 519 . The excellent correlation of the ring E carbons of the tabersonine epoxide unit in 519 with those of criophylline, is also consistent with the stereochemistry of the epoxide ring and the 3 α -substitution, while the substitution pattern on the aromatic moiety is consistent with the observed aromatic carbon shift values, the facile oxidation to the iminoquinone 520 as well as the change of the H(9) shift from δ 6.34 in 519 to 5.63 in 520 . The proposed relative stereochemistry of the constituent moieties in 519 was predicated on a presumed correspondence with the configurations of talcarpine ( 522 ) and hazuntinine ( 523 ) (321) . XXVII Aspidosperma –Iboga Type The isomeric tetrastachyne ( 524 ) and tetrastachynine ( 525 ) were isolated from Bonafousia tetrastachya ( T. siphilitica ), in addition to the previously known iboga–canthinone alkaloids, bonafousine ( 526 ) and isobonafousine ( 527 ) (322) . Both alkaloids showed a molecular ion at m/z 704, together with a higher mass fragment at m/z 720, attributed to intramolecular transmethylation. The base peak at m/z 124 was a characteristic of the mass spectrum of 12-hydroxyvincadifformine ( 528 ), which was also present in the plant, and indicated the presence of a similar aspidospermane moiety. The molecular formula of 524 (C 42 H 50 N 4 O 6 ) was confirmed from microanalytical data. The UV spectra of both alkaloids were similar to that of 528 (hydroxyindole and β -anilinoacrylate chromophores) and showed characteristic bathochromic shifts on addition of alkali. Both 524 and 525 were shown by 13 C NMR to be constituted from the union of a 12-hydroxyvincadifformine unit and a 11-hydroxycoronaridine unit, by comparison with 12-hydroxyvincadifformine ( 528 ) and bis(11-hydroxycoronaridin-12-yl) ( 511 ). Both alkaloids were also isolated from the plant. The 13 C shifts of the non-aromatic part of both compounds were virtually identical, with differences confined to the aromatic carbons, suggesting a variation in the structures involving aromatic substitution as the main difference between 524 and 525 . The 1 H NMR of 524 showed two sets of signals in the aromatic region, a pair of AB doublets corresponding to two adjacent ortho -coupled hydrogens, and another set corresponding to three contiguous aromatic hydrogens. Methylation (CH 2 N 2 ) of 524 resulted in a monomethyl derivative 530 (M + m/z 720), with the appearance of a methoxy singlet at δ 3.79 in the 1 H NMR spectrum, indicating that the other oxygen must be part of an ether function, consistent with the proposed structure and the 13 C NMR shifts ( δ C12 143.6, δ C12′ 127.9 vs. δ C12 140.8 and 100.0 in 528 and 511 , respectively). The 1 H NMR of tetrastachynine on the other hand showed two sets of aromatic AB doublets corresponding to two pairs of ortho -coupled aromatic hydrogens. Furthermore, methylation afforded the dimethoxy derivative 531 (M + m/z 734), in agreement with the proposed structure 525 for tetrastachynine ( δ C12 139.0, δ C12′ 100.5 vs. δ C12 140.8 and 100.0 in 528 and 511 , respectively). The dehydroderivatives of 524 and 525 , 14,15-dehydrotetrastachyne ( 532 ) and 14,15-dehydrotetrastachynine ( 533 ), respectively, in addition to bis(11-hydroxycoronaridin-12-yl) ( 511 ), were later isolated from T. citrifolia (323) . The former alkaloid 532 was also isolated from Peschiera echinata ( T. echinata ) (324) , while the latter alkaloid 533 was also isolated from Stemmadenia grandiflora (325) . The change in the 13 C shifts for C(14) and C(15), to δ 125.0 and 133.2, respectively, coupled with the appearance of the corresponding olefinic hydrogen shifts at δ 5.85 and 5.78, respectively, when compared to the NMR spectra of 524 , indicated the location of the unsaturation in the aspidosperma half in 532 . The same considerations apply to 533 , except that the olefinic hydrogens were observed as a multiplet at δ 5.78. In any case, catalytic hydrogenation of 533 gave the parent alkaloid 525 . Doubling of the signals was observed in the 1 H NMR spectrum of 533 due to atropisomerism, as a result of the highly and non-symmetrically substituted biphenyl unit, with coalescence observed at 60 o C in CD 3 OD (325) . XXVIII Aspidosperma – Aspidosperma Type Voacanga grandifolia (Apocynaceae) from India, provided a new bisindole, voacinol ( 534 ), in addition to vobtusine, deoxyvobtusine, and amataine (326) . The UV spectrum indicated the presence of a β -anilinoacrylate chromophore as in tabersonine ( 535 ). The molecular ion was detected by FABMS, showing an MH + at m/z 717 (C 43 H 48 N 4 O 6 ). The 13 C NMR spectral data showed a close correspondence for all the carbon shifts with those of tabersonine, except for some of the ring D carbons. The downfield shift of C(14) to δ 129.7 from 124.8 in 535 , is consistent with it being a quaternary center in 534 , while the signal at δ 39.0 was attributed to the methylene C(22) linking the two tabersonine moieties. This is also in agreement with the observation of only one olefinic H at δ 5.5 in the 1 H NMR spectrum of 534 , which was a broadened singlet due to allylic coupling with the two H(22). The ethyl side chain has also been modified to 18-hydroxyethyl, as indicated by the shifts for C(18) at δ 58.8 in 534 compared to 7.3 in 535 . Another bisindole with a methylene bridge linking two Aspidosperma -type units is methylenebismehranine ( 536 ) which was isolated, together with tabernaebovine ( 537 ) from T. bovina from Vietnam (327) . Alkaloid 536 is constituted from the linking of two (−)-mehranine units by a methylene bridge ( δ C 41.1; δ H 3.79). The monomeric unit (−)-mehranine ( 538 ), was also isolated from the same plant. The other bisindole, tabernaebovine ( 537 ) is also consitituted from the union of two (−)-mehranine moieties, but in a different manner from 536 . In 537 , the bisindole is branched from the aromatic C(10) of one, to C(2′) of the other mehranine unit. Pterotaberna inconspicua yielded kisantine ( 539 ), an unstable bisindole constituted from the union of two highly oxidized tabersonine units, as shown by its 13 C NMR spectrum. The UV spectrum showed the presence of β -anilinoacrylate chromophores, while the molecular formula, C 44 H 50 N 4 O 11 , was established from HRFABMS. The 1 H NMR spectrum (analyzed by COSY and delayed COSY experiments) showed two aromatic hydrogens as singlets at δ 6.67 and 5.53, two sets of two coupled olefinic hydrogens, one ethyl side chain linked to C(20), and four methoxy groups. The other side chain takes the form of an 18-hydroxy-substituted ethyl, linked to the other C(20′). One of the olefinic pair showed coupling to the aminomethylene hydrogens on C(3′) at δ 3.4, while the other olefinic pair showed coupling to a single allylic H ( δ 4.16) attached to the other C(3), which is an oxymethine from its observed shift at δ 84.8. The presence of two β -anilinoacrylate moieties was confirmed from the characteristic 13 C shifts, and taken with the other data, indicated the involvement of two tabersonine type halves. The aromatic shifts of one of the tabersonine units showed correspondence to the 10-hydroxy-11,12-dimethoxy tabersonine unit in pandicine ( Hz observed for 519 ), while the other aromatic moiety required substitution by three oxygens to accommodate the molecular formula and the presence of only one aromatic hydrogen. Since all four methoxyls have been accounted for, this left two OH and an ether as likely subsituents on the second aromatic moiety. In the mass spectrum, the observation of the m/z 390 fragment from retro -Diels–Alder cleavage is consistent with the aromatic substitution of the pandicine-like tabersonine unit, while the m/z 138 ion, derived from fragmentation of the other tabersonine unit, indicated that the 18′-hydroxyethyl side chain was attached to this moiety. The branching from the first tabersonine moiety is from C(3) since it is an oxymethine as shown by its 1 H and 13 C shifts, with the substitution likely to be α , from the low value of 3.8 J 3−14 . The lone aromatic hydrogen at δ 5.53 has to be placed at C(9′) of the second aromatic moiety to account for the observed N(1′)-H to H(9′) long range coupling. Its substantial shielding compared to the other H(9) at δ 6.67 was attributed to proximity of the second tabersonine moiety. These considerations led to structure 539 for kisantine (328) . nm) could be interpreted as a composite of the chromophores of aspidospermidine and tabersonine. The Melodinus morsei from China provided melomorsine ( 540 ), which analyzed for C 41 H 48 N 4 O 3 by HREIMS. The UV spectrum (206, 253, 315, 327 1 H NMR spectrum indicated the presence of one unsubstituted aromatic ring, a 10,11-disubstituted aromatic ring, and a methylene linked to an aromatic carbon and an indoline nitrogen. Comparison of the 13 C NMR spectral data of melomorsine with those of aspidospermidine and tabersonine showed a close correspondence of most of the signals, except for changes in the shifts and multiplicity of C(10) and C(11) of the tabersonine unit, and C(2′) of the aspidospermidine unit, indicating these positions as points of attachment of the monomeric moieties. The substantial downfield shift of C(2′) to δ 96.9 in melomorsine is indicative of an oxygenated quaternary carbon, and is consistent with the proposed structure of melomorsine in which N(1′) and C(2′) of the aspidospermidine unit are linked to C(10) and C(11) of the tabersonine unit, respectively, with the former linkage mediated by a methylene, and the latter by an oxygen. The proposed structure as well as the relative configuration of 540 , received additional support from the results of NOE experiments. Irradiation of H(22′ α ) caused enhancement of the H(12′) and H(9) signals, while irradiation of H(16′ α ) resulted in enhancement of the H(22′ β ) signal, indicating bridging of N(1′) and C(11) by the 22′-methylene group as well as α -substitution at C(2′) (329) . Hz), while strong NOEs between H(16) and H(21) are indicative of their H. modesta ( T. coffeoides ) from Madagascar provided three bisindoles, hazuntiphylline ( 541 ), hazuntiphyllidine ( 542 or 543 ), and anhydrohazuntiphyllidine ( 544 ). Hazuntiphylline ( 541 ) presented an indoline chromophore in the UV spectrum, while the NMR spectral data indicated a symmetrical bisindole. In addition to the M + at m/z 630 (C 40 H 46 N 4 O 3 ), the mass spectrum showed fragments ( m/z 138, 108, and M–138), which indicated the presence of a 14,15-epoxy substituted Aspidosperma -type moiety as found in lochnericine, pachysiphine, and hazuntine. The absence of NH, OH or C=O absorptions in the IR spectrum suggested involvement of the indolic nitrogens in the linking of the two monomeric halves, as well as the presence of an ether linkage to account for the third oxygen. These features led to the structure 541 for hazuntiphylline which is in agreement with the 13 C NMR spectral data, the assignment of which was facilitated by comparison with the spectra of folicangine ( 545 ) and ervafoline ( vide infra ). The observation of a quaternary carbon signal at δ 94.2 indicating a linkage to two heteroatoms, can be attributed to C(2) of an Aspidosperma -type unit, while the correspondence of the piperidine ring D carbon signals with those of pachysiphine rather than lochnericine pointed to a β stereochemistry of the epoxide function. Analysis of the coupling constants for H(16) indicated that it is axially oriented ( J 16−17 13.8 syn relationship. In addition, examination of models required the oxygen bridge linking C(2) and C(2′) to be β , to be consistent with the NOE data (330) . Hazuntiphyllidine ( 542 , 543 ) was isomeric with 541 . The NMR spectrum in CDCl 3 was complicated by the existence of two equilibrating forms resulting in apparent doubling of the signals. These two forms were shown to comprise the indoline form 542 , which predominates in C 6 D 6 , or the ring-opened, indolenine form 543 , which predominates in DMSO- d 6 solution. In either solvent, the signals of all the 40 carbons were distinguishable, although the shifts were slightly, but significantly different in the two solvents. In particular, the C(2) shift at δ 190.7 in DMSO- d 6 due to an indolenine, was seen at δ 102.2 in C 6 D 6 . The 1 H NMR spectrum in C 6 D 6 showed features due to two 14,15-epoxy substituted Aspidosperma -type moieties, in common with 541 . The main departure was the loss of symmetry indicating a change in the manner of branching of the constituent moieties. Other notable differences included the upfield shift of H(22′) to δ 1.68, and the presence of an isolated aminomethylene at δ 2.97 attributed to C(22). These features are accommodated in 542 , which is also consistent with the 13 C NMR data. It is to be noted that in a freshly prepared solution of hazuntiphyllidine in C 6 D 6 , the NMR spectrum corresponded with the indolenine form 543 , and only after several hours did the equilibrium shift in favor of the indoline form 542 , suggesting that the open indolenine-form probably represents the initial structure of hazuntiphyllidine. Anhydrohazuntiphyllidine ( 544 ) analyzed for C 40 H 44 N 4 O 2 , differing from hazuntiphyllidine by loss of H 2 O. The structure was readily deduced from examination of the spectral data, as well as by its identity with the product obtained from hazuntiphyllidine by acid-induced dehydration. The depicted configuration of the spirocarbon C(16) in these compounds ( 542 – 544 ) was based on the observed NOE between H(22) and H(6) (331) . The Malaysian T. divaricata provided a series of bisindoles, constituted from the union of tabersonine type units, but linked in a manner different from those considered above. Conophylline ( 546 ) (332–334) showed an MH + in the FABMS at m/z 795 (C 44 H 50 N 4 O 10 ). The UV spectrum was characteristic of alkaloids with β -anilinoacrylate chromophores and the IR spectrum showed the presence of NH, OH, and conjugated carbonyl functions. The 1 H and 13 C NMR spectral data indicated a bisindole constituted from highly oxygenated vincadifformine–tabersonine epoxide moieties. The 1 H NMR spectrum showed the presence of two indole NH, three isolated aromatic hydrogens one of which was significantly shielded ( δ 5.55), an OH function, four methoxy groups, of which two were associated with the presence of two ester carbomethoxy functions, and two ethyl groups. The presence of only three aromatic singlets indicated highly substituted indole rings, where one indole ring was substituted at the 10, 11, and 12 positions, while the other was substituted at the 10′ and 11′ positions. This was confirmed by the NOE interactions observed between one of the indole NH and the aromatic MeO at C(12), and between the other indole NH′ and the aromatic H(12′). The unusually low-field aromatic MeO carbon absorptions ( δ C 60.5, 61.0) suggested that they were in an ortho arrangement and indicated that the other aromatic MeO group was at C(11) with C(10) substituted by a OH group ( δ C 138.7), an arrangement reminiscent of that in the bisindole pandicine (519) (321) . Comparison of the spectral data with those of pandicine (519), in fact revealed generally good agreement of the aromatic 13 C shifts in particular as well as those of the non-aromatic carbons, with the exception of the piperidine ring D carbons. The other unit of the bisindole was clearly shown to be a 10-alkyl-11-oxy-tabersonine- β -epoxide from the excellent correlation of the non-aromatic 13 C shifts with those of pachysiphine ( 547 ), and the aromatic 13 C shifts with those of vandrikine and the bisindole alkaloid vincarubine ( 517 ). The mode of attachment of the monomer units was deduced from examination of the H(3), H(14), and H(15) resonances of the piperidine ring of the vincadifformine unit, which were clear and well resolved in the region from ca. Hz) collapsed to a doublet ( Hz). The mode of attachment of the monomeric units is thus δ 4 to 5. The OH function was placed on C(15), since, when exchanged with deuterium, the H(15) doublet of doublets ( J 11.0, 3.7 J 3.7 via C(3) and C(14) of the vincadifformine unit to C(10′) and C(11′) of the pachysiphine unit, respectively, the C(14) to C(11′) connection being mediated by an ether oxygen. The substitution at C(3) and C(14) has to be cis , this being dictated by the fact that carbons 3 and 14 form part of a dihydrofuran unit. The similarity of the C(3) shift to those in the dimers criophylline ( 521 ) (335) and pandicine ( 519 ) (321) suggested that conophylline also has a 3 α substitution. This was further confirmed by the observation that H(9) of conophylline ( δ 5.55) was significantly shielded compared with H(9) of pandicine ( δ 6.34) in the 1 H NMR spectrum, owing to its being affected by the anisotropy of the aromatic ring of the tabersonine–epoxide unit, a feature which would only be possible if the tabersonine epoxide unit was attached on the α -face at C(3) and C(14). The configuration of the remaining stereocenter, viz., that of the C(15)–OH, was readily deduced to be β from the NOE interaction observed between H(15) and the C(18) hydrogens of the C(20) α -ethyl substituent. The structure deduced from spectroscopic data has been subsequently confirmed by X-ray analysis (333) . Conophyllidine ( 548 ) is identical in all respects with conophylline except for replacement of the epoxide function at positions 14′ and 15′ of the tabersonine epoxide unit by a double bond (333) . Conophylline has also been subsequently isolated from the South American species, Tabernaemontana glandulosa (336) , and from the Thai species, Ervatamia microphylla (in all probability T. divaricata ) (337) . It has also been reported from another Malaysian species, Ervatamia polyneura ( T. dichotoma ), under the name polyervine (338) . The leaf extract of E. polyneura also yielded the related bisindole, polyervinine ( 549 ), which is similar to conophylline, except for the aromatic portion of the vincadifformine unit, which in the case of 549 incorporates an indoline dione chromophore, existing predominantly in its zwitterionic quinoniminium form. Conofoline ( Hz and the observed NOEs for H(15′)/H(18′), H(19′), H(21′). 550 ), which occurs only in the double flower variety of T. divaricata , has the same 10-hydroxy-11,12-dimethoxy-tabersonine- β -epoxide unit as in conophylline, but differs in the identity of the other monomeric unit as well as in the mode of attachment of the monomers (339) . This was shown by the 1 H and 13 C NMR data which also revealed the other unit to be a 10-alkylmehranine moiety from the excellent agreement of the non-aromatic 13 C NMR resonances with those of (−)-mehranine ( 538 ), which also occurs in the plant ( vide supra ). The NMR data also showed that the dimer was branched from C(3) of the oxygenated tabersonine- β -epoxide moiety to the aromatic C(10′) of the mehranine unit. The stereochemistry at C(3) was readily ascertained from the NMR signal attributed to H(3) ( δ 4.52) which was a singlet, requiring the H(3)/H(14) dihedral angle to be ca. 90°, an arrangement possible only if H(3) is β . The structure has also been subsequently confirmed by X-ray analysis (340) . Another bisindole from the same plant is conophyllinine ( 551 ) which shares the same pandicine-like tabersonine unit with 546 , 548 , and 550 , as well as a similar mode of linking via a central dihydrofuran ring (334) . The difference is in the other monomeric unit which is now an opened form of tabersonine- β -epoxide, with a trans diol functionality at positions 14′ and 15′ instead of a β -epoxide function. The epoxide ring opening by a water molecule is anticipated to occur preferentially at the less hindered C(14′) resulting in a H(14′ β ), H(15′ α ) configuration. This proposal was supported by the J 14′−15′ value of 9 Conofoline has also been isolated from another Malaysian Tabernaemontana species ( T. peduncularis ) under the name pedunculine (341) as well as from T. bovina (342) . The former plant also furnished another bisindole alkaloid, peduncularidine ( 552 ), which shares the common oxygenated tabersonine- β -epoxide moiety of conofoline, but differs in the second unit which is now an opened form of (−)-mehranine, with a trans diol functionality at positions 14′ and 15′. The stereochemistry at C(14′) and C(15′) was determined from the ROESY spectrum which showed correlations between the axial H(2′) and H(17′) with H(14′), indicating that the latter has a β stereochemistry. The common, highly oxygenated tabersonine/pachysiphine unit which occurs in conophylline ( ) 546 ), conophyllidine ( 548 ), conofoline ( 550 ), conophyllinine ( 551 ), peduncularidine ( 552 ), kisantine ( 539 ), and pandicine ( 519 ), has been finally isolated from T. divaricata , and named taberhanine (334) . The co-occurrence of taberhanine and conophylline in the same plant suggested a biogenetic pathway involving electrophilic attack of the taberhanine iminium ion ( 553 ) on the activated position 10′ of the hypothetical 11′-hydroxypachysiphine acceptor unit ( 554 ), followed by intramolecular epoxide ring opening to form the central dihydrofuran unit ( Scheme 33 (334) . Conophylline ( 546 ) has been shown to possess important biological activity. It has been shown to induce morphological normalization in ras -overexpressing cell lines such as K- ras -NRK and K- ras -NIH3T3 (337) . In both in vitro as well as in vivo experiments using K- ras -NRK cells, conophylline was shown to inhibit tumor infiltration and metastasis (343,344) . Its antitumor effects were later demonstrated in human cancer cells when it was shown to inhibit attachment and chemotactic invasion of human uterine endometrial cancer cells (345) . Other biological effects of conophylline include the suppression of TGF- β signaling (346) and the downregulation of TNF- α receptors in human T-cell leukemia cells (347) . Recently, conophylline has also been shown to induce morphological change, as well as insulin production, in rat pancreatic acinar carcinoma cells (348,349) . In a structure-activity study it was shown that the highest effect was shown by conophylline ( 546 ), followed by conophyllidine ( 548 ). Conofoline ( 550 ), which has a single bond connecting the monomeric moieties was ineffective, indicating that an intact central dihydrofuran ring is essential for manifestation of the biological activity. The putative monomeric precursors of the bisindoles, taberhanine, pachysiphine, and mehranine were themselves ineffective. The respective semisynthetic iminoquinone derivatives of the bisindoles (e.g., 555 – 557 ) were also examined where it was found that of a pair of active bisindoles, the iminoquinone derivative invariably showed the higher potency (348) . In a subsequent study of the effect of conophylline on the differentiation of pancreatic precursor cells, it was found that conophylline inhibited the formation of cystic structure and increased the number of insulin-positive cells in the rat pancreatic rudiment in organ culture. Conophylline was also found to increase the expression of mRNA for insulin and the number of homeobox-1-positive cells. In vivo studies using neonatal streptozotocin-induced diabetic rats showed that conophylline-treatment resulted in significant reduction of the plasma glucose concentration and improved glucose tolerance on glucose loading. In addition, the insulin content, the β -cell mass, the number of islet-like cell clusters, and pancreatic duodenal homeobox-1-positive ductal cells, were all significantly increased in conophylline-treated rats. These results suggest that conophylline induces differentiation of pancreatic precursor cells and increases the formation of β -cells (350) . The structures of the alkaloids of Melodinus scandens , viz., scandomeline, scandomelonine, and their C(19)-epimers have been reported previously (351) . From the concentrated mother liquors of scandomeline, another bisindole scandomelidine ( 558 ) has been obtained, which was shown by the spectral data to be constituted from tabersonine- and aspidofractinine-type halves (352) . Examination of the 13 C NMR spectral data and comparison with those of venalstonine ( 559 ), pachysiphine ( 547 ), and scandomelonine ( 560 ) led to structure 558 for scandomelidine, in which venalstonine is linked via C(10) to C(3′) of pachysiphine, in the same manner as in scandomelonine (3′ α -substitution). Voafrines A ( 561 ) and B ( 562 ), isolated from cell suspension cultures of Voacanga africana , represent the first instance of fully characterized bisindole alkaloids produced by plant cell cultures (353) . HRMS showed that 561 and 562 are isomers with molecular formula C 42 H 46 N 4 O 4 , while the UV spectra indicated the presence of β -anilinoacrylate chromophores. The fragment ions observed at m/z 214 and 228, which are typical of tabersonine ( 535 ), and the fact that the molecular formula corresponds to a dehydrodimer of tabersonine, suggested strongly that both alkaloids are constituted from the union of two tabersonine units. Interpretation of the NMR spectral data was facilitated by comparison with that of tabersonine as well as application of 2-D techniques. The 1 H NMR spectrum showed the presence of eight aromatic hydrogens and two NH signals, excluding these positions as possible sites of attachment of the monomeric units. However, only three olefinic hydrogens, two diastereotopic aminomethylene hydrogens, and a single aminomethine H, were observed, indicating branching from an olefinic carbon of one unit to C(3′) of the other tabersonine unit. The attachment point on the olefinic carbon was deduced to be C(14), since H(3) in both compounds showed only small allylic coupling with H(15). The other two olefinic hydrogens form part of an ABX system with the lone H(3′). Analysis of the vicinal coupling constants of these hydrogens indicated an arrangement in which H(3′) is nearly orthogonal to the plane of the double bond in voafrine A (H(3′ α )), and nearly coplanar to the plane of the double bond in voafrine B (H(3′ β )). These conclusions led to the structures depicted in 561 and 562 for voafrines A and B, respectively, which also represent their absolute stereochemistry, in view of the similarity of the chiroptical characteristics (CD spectra) with those of (−)-tabersonine ( 535 ). Dimerization of tabersonine ( 535 ) in the presence of oxygen by a crude enzyme preparation from C. roseus yielded 3-hydroxyvoafrines A ( 563 ) and B ( 564 ), which were reduced enzymatically or by NaBH 4 to voafrines A and B, respectively (354) . The 1 H NMR spectrum of 3-hydroxyvoafrine B ( 564 ) in DMSO- d 6 or acetone- d 6 was complicated by the existence of equilibrating epimers of 564 (3 α -hydroxyvoafrine B and 3 β -hydroxyvoafrine B). Addition of water shifted the equilibrium toward the 3 α -hydroxy epimer, which was the sole species observed in DMSO- d 6 -H 2 O or acetone- d 6 -H 2 O mixed solvents. The involvement of the tabersonine iminium ion as an intermediate was suggested by the isolation of 3 α -acetonyltabersonine and 3 α -acetonylvoafrine B when the enzyme-mediated conversion was carried out in the presence of acetone. A third polar product which was also isolated was subsequently identified to be a trimeric alkaloid ( 565 ), constituted from three tabersonine units, and, like the hydroxyvoafrines, was readily reduced by NaBH 4 to 566 (355) . The dimerization of tabersonine ( 535 ) was also probed by anodic oxidation (Pt/LiClO 4 /MeCN) which produced a different result compared to the enzyme-mediated process, yielding instead the 16,10′-linked dimeric product 567 as the major product accompanied by minor amounts of the 10,10′-linked dimer 568 , and the trimers 569 and 570 (356) . Anodic oxidation of 3-oxotabersonine gave the corresponding 16,10′-linked didehydrodimer 571 as the major product (356) as did reaction of 3-oxotabersonine with nitrosonium tetrafluoroborate (NOBF 4 ) (357) . Nitaphylline ( ppm. The bulk of the overlapped signals were readily assigned to the aromatic portions of the alkaloid as well as the methoxy, carbamate, and ester groups which were similar to those of kopsingine. The remaining signals could also be assigned based on 2-D NMR data and by comparison with kopsingine. The observation that the resonances of the piperidine ring carbons showed greater departure from kopsingine suggested that attachment of the monomeric entities involved the piperidine ring carbons. 572 ), was the only bisindole isolated from Kopsia teoi which otherwise provided a large number of new indole alkaloids. The mass spectrum showed a molecular ion at m/z 910 with a significant peak at m/z 455 suggesting symmetrical cleavage of the parent ion along the bond bridging the monomeric moieties. This, together with the observation that the UV spectrum of nitaphylline was virtually superimposable with that of kopsingine ( 573 ) provided an early indication that nitaphylline is constituted from union of two kopsingine units. This was further reinforced by the NMR spectral data. The 13 C NMR spectrum accounted for only 33 peaks, indicating overlap of 15 carbon resonances. In addition, four pairs of signals although distinguishable were only just so, differing in chemical shift by only 0.1 or 0.2 The Hz) with no evidence of coupling to any adjacent olefinic hydrogen, the dimer was therefore deduced to be bridged from C(3) of one kopsingine unit to C(14′) of the other. The stereochemistry of the point of branching could not be ascertained directly from the NMR spectrum due to overlap of the aminomethylene signal and poor resolution of the olefinic signals, but could be assigned by analogy to the bistabersonine alkaloids voafrine A ( 1 H NMR spectrum showed six aromatic hydrogens, three olefinic hydrogens, two geminal hydrogens of an aminomethylene group and only one H due to an aminomethine, indicating branching of the dimer from C(3) of one kopsingine unit to the olefinic C(14′) or C(15′) of the other kopsingine unit. Since the geminal hydrogens of C(3′) were doublets ( J 16 561 ) ( β -branching) and voafrine B ( 562 ) ( α -branching), which possess the same mode of attachment of the monomeric units (353) . In nitaphylline ( 572 ), the carbon shifts of C(21) and C(21′) are identical (overlapped) and are similar to the value in the monomer indicating that the substitution is β , with the pseudoequatorially oriented second kopsingine unit pointing away from the first by analogy to voafrine A. In the α -branched voafrine B, the resulting greater spatial proximity between the two monomeric units is reflected in the very different shifts observed for C(21). Nitaphylline ( 572 ) represents the first example of an aspidofractinine–aspidofractinine-type bisindole alkaloid (358,359) . Tenuiphylline ( MHz NMR spectra since extensive overlap was encountered with lower field instruments. 574 ) was isolated in minute amounts, together with the tenuisines ( vide infra ) from Kopsia tenuis occurring in Malaysian Borneo (360) . The FABMS showed a MH + peak at m/z 717 and high-resolution measurements provided the formula C 42 H 44 N 4 O 7 . The UV spectrum indicated the presence of dihydroindole chromophores and the IR spectrum indicated the presence of hydroxyl, urethane, ester, and lactone functions. In view of the small amount obtained, definitive structure elucidation of tenuiphylline required resort to 600 The NMR spectral data showed the presence of one carbamate and one methyl ester function. The aromatic region integrated for seven hydrogens indicating branching of the dimer from an aromatic carbon of one monomeric unit. Absence of an NH signal and the presence of only one urethane function indicated the dihydroindole nitrogen of the other monomeric moiety as the other site of attachment. The NMR spectral data also showed the presence of four olefinic hydrogens, two associated with a six-membered ring and two with a five-membered ring. One unit of the bisindole was readily deduced to be identical to lapidilectine B ( 575 ) from the excellent correlation of the 13 C shifts, in particular the non-aromatic shifts, with those of lapidilectine B. The other monomeric unit can be considered as having a novel carbon skeleton or a rearranged venalstonine. The carbon shifts of this second unit generally resembled those of venalstonine ( 559 ), except for changes involving carbons (2), (12), (16), (17), (18), (20), and (21). The COSY spectrum indicated the presence of the same groups as in venalstonine and the downfield shifts of C(20) and C(21) were reminiscent of those of the vindolinine derivatives (e.g., N -methylvindolinine 576 ), suggesting a change in the connectivity involving the C(18)–C(19) fragment. The presence of a hydroxyl group on C(2) was supported by its downfield shift at δ 99.8 due to its being linked to an oxygen and a nitrogen and by the observed three-bond correlations from C(2) to H(6) and H(21) in HMBC. The presence of an OH on C(2) required that C(18) be now linked to C(16) which was consistent with the downfield shift of C(16) when compared with venalstonine as well as with the observed correlations from both C(18) and C(19) to H(17) in the HMBC spectrum. From the 1 H NMR spectrum (COSY, NOE), it could be established that the aromatic portion associated with this unit was unsubstituted. Furthermore, the upfield shift of H(12), when compared with venalstonine, was consistent with the change from NH in venalstonine to N–C(11′) in tenuiphylline. The attachment site on the lactone-containing monomer can be at either C(10′) or C(11′) from the coupling pattern of the aromatic hydrogens. The observed NOE between the aromatic doublet at δ 7.33 and H(6′ β ), and a C(7′)/H(9′) correlation in HMBC allowed assignment of this signal to H(9′) which must be coupled to H(10′), furnishing proof of C(11′) branching. The bisindole is thus linked from N(1) of one unit to C(11′) of the other. 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