Download PDF
Planta Med 2014; 80(07): 550-556
DOI: 10.1055/s-0034-1368441
Biological and Pharmacological Activity
Original Papers
Georg Thieme Verlag KG Stuttgart · New York

Effects of 7-Hydroxycalamenene Isolated from Croton cajucara Essential Oil on Growth, Lipid Content and Ultrastructural Aspects of Rhizopus oryzae

Mariana M. B. Azevedo   *
1   Instituto de Química, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, Brazil
2   Instituto de Microbiologia Paulo de Góes, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, Brazil
,
Catia A. Almeida   *
2   Instituto de Microbiologia Paulo de Góes, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, Brazil
,
Francisco C. M. Chaves
3   EMBRAPA Amazônia Ocidental, Manaus, AM, Brazil
,
Galba M. Campos-Takaki
4   Núcleo de Pesquisas em Ciências Ambientais, Departamento de Química, Universidade Católica de Pernambuco, Recife, PE, Brazil
,
Sonia Rozental
5   Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, Brazil
,
Humberto R. Bizzo
6   EMBRAPA Agroindústria de Alimentos, Rio de Janeiro, RJ, Brazil
,
Celuta S. Alviano
2   Instituto de Microbiologia Paulo de Góes, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, Brazil
,
Daniela S. Alviano
2   Instituto de Microbiologia Paulo de Góes, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, Brazil
› Author Affiliations
Further Information

Publication History

received 22 January 2014
revised 14 March 2014

accepted 22 March 2014

Publication Date:
19 May 2014 (online)

Also available at
    Permissions and Reprints

Abstract

The leaves and bark of Croton cajucara, a shrub from the Amazon region, have been used in folk medicine to treat diabetes, malaria, and gastrointestinal and liver disorders. The essential oil from the leaves, rich in linalool, presented antileishmanial and antimicrobial activities. A chemotype of this species was found with an essential oil rich in 7-hydroxycalamenene. During our studies of the C. cajucara essential oil, we isolated 7-hydroxycalamenene at > 98 % purity. The minimum inhibitory concentration of 7-hydroxycalamenene against Absidia cylindrospora, Cunninghamella elegans, Mucor circinelloides, Mucor circinelloides f. circinelloides, Mucor mucedo, Mucor plumbeus, Mucor ramosissimus, Rhizopus microsporus, Rhizopus oryzae, and Syncephalastrum racemosum ranged from 19.53 to 2500 µg/mL. The reference drug used, amphotericin B, presented a minimum inhibitory concentration ranging from 0.085 µg/mL to 43.87 µg/mL. 7-Hydroxycalamenene also altered spore differentiation and total lipid content. Ultrastructural analysis by transmission electron microscopy showed significant alterations in the cellular structure of R. oryzae.

Key words

7-Hydroxycalamenene - Rhizopus oryzae - zygomycetes - Croton cajucara - Euphorbiaceae - essential oil

* Mariana M. B. Azevedo and Catia A. Almeida contributed equally to this study.


 

  • References

  • 1 Tullio V, Nostro A, Mandras N, Dugo P, Banche G, Cannatelli MA, Cuffini AM, Alonzo V, Carlone NA. Antifungal activity of essential oils against filamentous fungi determined by broth microdilution and vapour contact methods. J Appl Microbiol 2007; 102: 1544-1550
    CrossrefPubMedGoogle Scholar
  • 2 Alviano DS, Alviano CS. Plant extracts: search for new alternatives to treat microbial diseases. Curr Pharm Biotechnol 2009; 10: 106-121
    CrossrefPubMedGoogle Scholar
  • 3 Hiruma-Lima CA, Gracioso JS, Bighetti EJB, Grassi-Kassisse DM, Nunes DS, Souza Brito ARM. Effect of essential oil obtained from Croton cajucara Benth. on gastric ulcer healing and protective factors of the gastric mucosa. Phytomedicine 2002; 9: 523-529
    CrossrefPubMedGoogle Scholar
  • 4 Perazzo FF, Carvalho JCT, Rodrigues M, Morais EKL, Maciel MAM. Comparative anti-inflammatory and antinociceptive effects of terpenoids and an aqueous extract obtained from Croton cajucara Benth. Rev Bras Farmacogn 2007; 17: 521-528
    CrossrefPubMedGoogle Scholar
  • 5 Chaves FCM, Bizzo HR, Angelo PMC, Xavier JJBN, Sá-Sobrinho AF. Rendimento e Composição Química do Óleo Essencial de Folha de Dois Morfotipos de Sacaca (Croton cajucara Benth.). Rev Bras Pl Med 2006; 8: 117-119
    PubMedGoogle Scholar
  • 6 Pereira AQ, Chaves FCM, Pinto SC, Leitão SG, Bizzo HR. Isolation and identification of cis-7-hydroxycalamenene from the essential oil of Croton cajucara Benth. J Essent Oil Res 2011; 23: 20-23
    PubMedGoogle Scholar
  • 7 Alviano WS, Mendonça-Filho RR, Alviano DS, Bizzo HR, Souto-Padrón T, Rodrigues ML, Bolognese AM, Alviano CS, Souza MMG. Antimicrobial activity of Croton cajucara Benth. linalool-rich essential oil on artificial biofilms and planktonic microorganisms. Oral Microbiol Immunol 2005; 20: 101-105
    CrossrefPubMedGoogle Scholar
  • 8 Rosa MSCS, Mendonça-Filho RR, Bizzo HR, Rodrigues IA, Soares RMA, Souto-Padrón T, Alviano CS, Lopes AHCS. Antileishmanial activity of linalool-rich essential oil from Croton cajucara Benth. Antimicrob Agents Chemother 2003; 47: 1895-1901
    CrossrefPubMedGoogle Scholar
  • 9 Azevedo MMB, Chaves FCM, Almeida CA, Bizzo HR, Duarte RS, Campos-Takaki GM, Alviano CS, Alviano DS. Antioxidant and antimicrobial activities of 7-hydroxy-calamenene-rich essential oils from Croton cajucara Benth. Molecules 2013; 18: 1128-1137
    CrossrefPubMedGoogle Scholar
  • 10 Almyroudis NG, Sutton DA, Fothergill AW, Rinaldi MG, Kusne S. In vitro susceptibilities of 217 clinical isolates of zygomycetes to conventional and new antifungal agents. Antimicrob Agents Chemother 2007; 51: 2587-2590
    CrossrefPubMedGoogle Scholar
  • 11 Ameen M, Arenas R, Martinez-Luna E, Reyes M, Zacarias R. The emergence of mucormycosis as an important opportunistic fungal infection: five cases presenting to a tertiary referral center for mycology. Int J Dermatol 2007; 46: 380-384
    CrossrefPubMedGoogle Scholar
  • 12 Dannaoui E, Meletiadis J, Mouton JW, Meis JFGM, Verweij PE, Network E. In vitro susceptibilities of zygomycetes to conventional and new antifungals. J Antimicrob Chemother 2003; 51: 45-52
    CrossrefPubMedGoogle Scholar
  • 13 Croft KD, Ghisalberti EL, Hocart CH, Jefferies PR, Raston CL, White AH. Absolute configuration of the (+)-calamenenes: crystal structure of 7-hydroxycalamenene. J Chem Soc Perkin 1 1978; 1: 1267-1270
    PubMedGoogle Scholar
  • 14 Davila-Huerta G, Hamada H, Davis GD, Stipanovic RD, Adams CM, Essenberg M. Cadinane-type sesquiterpenes induced in Gossypium cotyledons by bacterial inoculation. Phytochemistry 1995; 39: 531-536
    CrossrefPubMedGoogle Scholar
  • 15 Grayer RJ, Harborne JB. A survey of antifungal compounds from higher plants, 1982–1993. Phytochemistry 1994; 37: 19-42
    CrossrefPubMedGoogle Scholar
  • 16 Melcher E, Jüngel P, Möllendorf B, Schmitt U. Identification of a hydroxy substituted calamenene – a sesquiterpene associated with wound reactions in non-infected xylem of Tilia spp. Phytochemistry 2003; 62: 707-713
    CrossrefPubMedGoogle Scholar
  • 17 Paterson RRM. Ganoderma – a therapeutic fungal biofactory. Phytochemistry 2006; 67: 1985-2001
    CrossrefPubMedGoogle Scholar
  • 18 Scher JM, Speakman JB, Zapp J, Becker H. Bioactivity guided isolation of antifungal compounds from the liverwort Bazzania trilobata (L.) SF Gray. Phytochemistry 2004; 65: 2583-2588
    CrossrefPubMedGoogle Scholar
  • 19 Sikder MAA, Kaisar MA, Rahman MS, Hasan CM, Al-Rehaily AJ, Rashid MA. Secondary metabolites from seed extracts of Syzygium cumini (L.). J Phys Sci 2012; 23: 83-87
    PubMedGoogle Scholar
  • 20 Azevedo MM, Almeida CA, Bizzo HR, Chaves FC, Alviano DS, Alviano CS. Anti-zygomycetes activity of 7-hydroxycalamenene isolated from Croton cajucara . Planta Med 2011; 77: 1449-1449
    PubMedGoogle Scholar
  • 21 Azevedo MMB, Pereira AQ, Chaves FCM, Bizzo HR, Alviano CS, Alviano DS. Antimicrobial activity of the essential oils from the leaves of two morphotypes of Croton cajucara Benth. J Essent Oil Res 2012; 24: 351-357
    CrossrefPubMedGoogle Scholar
  • 22 Sartoratto A, Machado ALM, Delarmelina C, Figueira GM, Duarte MCT, Rehder VLG. Composition and antimicrobial activity of essential oils from aromatic plants used in Brazil. Braz J Microbiol 2004; 35: 275-280
    CrossrefPubMedGoogle Scholar
  • 23 Meletiadis J, Antachopoulos C, Stergiopoulou T, Pournaras S, Roilides E, Walsh TJ. Differential fungicidal activities of amphotericin B and voriconazole against Aspergillus species determined by microbroth methodology. Antimicrob Agents Chemother 2007; 51: 3329-3337
    CrossrefPubMedGoogle Scholar
  • 24 Buckley PM, Sommer NF, Matsumoto TT. Ultrastructural details in germinating sporangiospores of Rhizopus stolonifer and Rhizopus arrhizus . J Bacteriol 1968; 95: 2365-2373
    PubMedGoogle Scholar
  • 25 Rodrigues IA, Azevedo MM, Chaves FC, Bizzo HR, Corte-Real S, Alviano DS, Alviano CS, Rosa MSS, Vermelho AB. In vitro cytocidal effects of the essential oil from Croton cajucara (red sacaca) and its major constituent 7-hydroxycalamenene against Leishmania chagasi . BMC Complement Altern Med 2013; 13: 249
    CrossrefPubMedGoogle Scholar
  • 26 Kontoyiannis DP, Lewis RE. How I treat mucormycosis. Blood 2011; 118: 1216-1224
    CrossrefPubMedGoogle Scholar
  • 27 Hess WM, Weber DJ. Ultrastructure of dormant and germinated sporangiospores of Rhizopus arrhizus . Protoplasma 1973; 77: 15-33
    CrossrefPubMedGoogle Scholar
  • 28 Ekundayo JA. Further studies on germination of sporangiospores of Rhizopus arrhizus . J Gen Microbiol 1966; 42: 283-291
    CrossrefPubMedGoogle Scholar
  • 29 de Lira Mota KS, de Oliveira Pereira F, de Oliveira WA, Lima IO, de Oliveira Lima E. Antifungal activity of Thymus vulgaris L. essential oil and its vonstituent phytochemicals against Rhizopus oryzae: interaction with ergosterol. Molecules 2012; 17: 14418-14433
    CrossrefPubMedGoogle Scholar
  • 30 Weete JD, Gandhi SR. Sterols of the phylum Zygomycota: phylogenetic implications. Lipids 1997; 32: 1309-1316
    CrossrefPubMedGoogle Scholar
  • 31 Zhai B, Zhou H, Yang L, Zhang J, Jung K, Giam CZ, Xiang X, Lin X. Polymyxin B, in combination with fluconazole, exerts a potent fungicidal effect. J Antimicrob Chemother 2010; 65: 931-938
    CrossrefPubMedGoogle Scholar
  • 32 Arthington-Skaggs BA, Jradi H, Desai T, Morrison CJ. Quantitation of ergosterol content: novel method for determination of fluconazole susceptibility of Candida albicans . J Clin Microbiol 1999; 37: 3332-3337
    PubMedGoogle Scholar
  • 33 Greenspan P, Mayer EP, Fowler SD. Nile red: a selective fluorescent stain for intracellular lipid droplets. J Cell Biol 1985; 100: 965-973
    CrossrefPubMedGoogle Scholar
  • 34 Gunasekaran M, Weber DJ, Hess WM. Changes in lipid composition during spore germination of Rhizopus arrhizus . Trans Br Mycol Soc 1972; 59: 241-248
    CrossrefPubMedGoogle Scholar
  • 35 Weete JD, Lawler GC, Laseter JL. Total lipid and sterol components of Rhizopus arrhizus: identification and metabolism. Arch Biochem Biophys 1973; 155: 411-419
    CrossrefPubMedGoogle Scholar
  • 36 Gottlieb OR, Guimarães MT. Modified distillation trap . Chem Anal 1960; 49: 114-116
    PubMedGoogle Scholar
  • 37 Adams RP. Identification of essential oil components by gas chromatography/mass spectrometry, 4th edition. Carol Stream: Allured Publ. Corp.; 2007: 1-804
    Google Scholar
  • 38 Clinical and Laboratory Standards Institute (CLSI). Reference method for broth dilution antifungal susceptibility testing of filamentous fungi; approved standard M38-A. Wayne: National Committee for Clinical Laboratory Standards; 2002: 1-21
    CrossrefGoogle Scholar
  • 39 Weete JD, Weber DJ, Laseter JL. Lipids of Rhizopus arrhizus Fischer. J Bacteriol 1970; 103: 536-540
    PubMedGoogle Scholar