Food Science and Biotechnology

Korean Society of Food Science and Technology (한국식품과학회)
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Limonene and Its Oxyfunctionalized Compounds: Biotransformation by Microorganisms and Their Role as Functional Bioactive Compounds

  • Published : 2009.08.31
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Abstract

Monoterpenes, in special limonene and its derivatives, are well studied in the literature due to their several properties. They are well recognized as major components of essential oils; some of them, are important industry residues, and others present some important biological activities. In this review, the biotransformation of the inexpensive limonene into flavor compounds was briefly reviewed and the main pathways for limonene biotransformation are presented. Furthermore, some important biological properties of these compounds were also considered, like bactericidal activity, induction of immune response, and role in disease prevention, with a little emphasis on some possibilities related to the mechanisms of anticancer action.

Keywords

References

  1. U.S. Ag, LLC-100% Nature Friendly Agriculture. Available from: http://www.unitedstatesag.org. Accessed on Sep. 9, 2008
  2. Duetz WA, Bouwmeester H, Beilen JB, Witholt B. Biotransformation of limonene by bacteria, fungi, yeasts, and plants. Appl. Microbiol. Biot. 61: 269-277 (2003) https://doi.org/10.1007/s00253-003-1221-y
  3. Carvalho CCCR, Fonseca MMR. Biotransformation of terpenes. Biot. Adv. 24: 134-142 (2006) https://doi.org/10.1016/j.biotechadv.2005.08.004
  4. Dhavalikar RS, Bhattacharyya PK. Microbiological transformations of terpenes. VIII. Fermentation of limonene in a soil pseudomonad. Ind. J. Biochem. 3: 144-157 (1966)
  5. Dhavalikar RS, Rangachari PN, Bhattacharyya PK. Microbiological transformations of terpenes. IX. Pathways of degradation of limonene in a soil pseudomonad. Ind. J. Biochem. 3: 158-164 (1966)
  6. Marostica-Jr MR, Past$\'{o}$re GM. Production of R-(+)-α-terpineol by the biotransformation of limonene from orange essential oil, using cassava waste water as medium. Food Chem. 101: 345-350 (2007) https://doi.org/10.1016/j.foodchem.2005.12.056
  7. Braddock RJ, Cadwallader KR. Bioconversion of citrus d-limonene. pp. 142-148. In: Fruit Flavors: Biogenesis, Characterization, and Authentication. Rouseff RL, Leahy MM (eds). ACS Symp. Series No. 596. American Chemical Society, Washington, DC, USA (1995)
  8. Mar$\'{o}$stica-Jr MR, Pastore GM. Biotransformation of limonene: A review of the main metabolic pathways. Quim. Nova 30: 382-387 (2007) https://doi.org/10.1590/S0100-40422007000200027
  9. Crowell PL. Prevention and therapy of cancer by dietary monoterpenes J. Nutr. 129: 775S-778S (1999) https://doi.org/10.1093/jn/129.3.775S
  10. Van der Werf MJ, Swarts HJ, De Bont JAM. Rhodococcus erythropolis DCL14 contains a novel degradation pathway for limonene. Appl. Environ. Microb. 65: 2092-2102 (1999)
  11. Van der Werf, MJ, Keijzer PM, Van der Schaft PH. Xanthobacter sp C20 contains a novel bioconversion pathway for limonene. J. Biotechnol. 84: 133-143 (2000) https://doi.org/10.1016/S0168-1656(00)00348-5
  12. University of Minnesota. Biocatalysis, biodegradation Database. Available from: http://umbbd.msi.umn.edu/. Accessed on Sep. 9, 2008
  13. Speelmans G, Bijlsma A, Eggink G. Limonene bioconversion to high concentrations of a single and stable product, perillic acid, by a solvent-resistant Pseudomonas putida strain. Appl. Microbiol. Biot. 50: 538-544 (1998) https://doi.org/10.1007/s002530051331
  14. Chatterjee T, Bhattacharyya DK. Biotransformation of limonene by Pseudomonas putida. Appl. Microbiol. Biot. 55: 541-546 (2001) https://doi.org/10.1007/s002530000538
  15. Noma Y, Yamasaki S, Asakawa Y. Biotransformation of limonene and related compounds by Aspergillus cellulosae. Phytochemistry 31: 2725-2727 (1992) https://doi.org/10.1016/0031-9422(92)83619-A
  16. Trytek M, Fiedurek J. A novel psychrotrophic fungus, Mortierella minutissima, for d-limonene biotransformation. Biotechnol. Lett. 27: 149-153 (2005) https://doi.org/10.1007/s10529-004-7347-x
  17. Marostica-Jr MR, Mota NO, Baudet N, Pastore GM. Fungal biotransformation of monoterpenes found in agroiindustrial residues from orange and pulp industries into aroma compounds: Screening using solid phase microextraction. Food Sci. Biotechnol. 16: 37-42 (2007)
  18. Abraham WR, Stumpf B, Kieslich K. Microbial transformations of terpenoids with 1-p-menthene skeleton. Appl. Microbiol. Biot. 24: 24-30 (1986)
  19. Demyttenaere JCR, van Belleghem K, De Kimpe N. Biotransformation of (R)-(+)- and (S)-(-)-limonene by fungi and the use of solid phase microextraction for screening. Phytochemistry 57: 199-208 (2001) https://doi.org/10.1016/S0031-9422(00)00499-4
  20. Onken J, Berger RG. Biotransformation of citronellol by the basidiomycete Cystoderma carcharias in a aerated-membrane bioreactor. Appl. Microbiol. Biot. 51: 158-163 (1999) https://doi.org/10.1007/s002530051376
  21. Bowen ER. Potential by-products from microbial transformation of D-limonene. Florida State Horticult. Soc., USA 88: 304-308 (1975)
  22. Lupien S, Karp F, Wildung M, Croteau R. Regiospecific cytochrome P450 limonene hydroxylases from mint (mentha) species: cDNA isolation, characterization, and functional expression of (-)-4Slimonene-3-hydroxylase and (-)-4S-limonene-6-hydroxylase. Arch. Biochem. Biophys. 368: 181-192 (1999) https://doi.org/10.1006/abbi.1999.1298
  23. Vank T, Valterov$\'{a}$ I, Vakov$\'{a}$ R, Vaisar T. Biotransformation of (-)- limonene using Solanum aviculare and Dioscorea deltoidea immobilized plant cells. Biotechnol. Lett. 21: 625-628 (1999) https://doi.org/10.1023/A:1005541820668
  24. Duetz WA, Fjallm$\"{a}$n AHM, Ren S, Jourdat C, Witholt B. Biotransformation of D-limonene to (+) trans-carveol by toluenegrown Rhodococcus opacus PWD4 cells. Appl. Environ. Microb. 67: 2829-2832 (2001) https://doi.org/10.1128/AEM.67.6.2829-2832.2001
  25. Kraidman G, Mukherjee BB, Hill ID. Conversion of D-limonene into an optically active isomer of α-terpineol by a Cladosporium species. Bacteriol. Proc. 69: 63 (1969)
  26. Tan Q, Day DF, Cadwallader KR. Bioconversion of (R)-(+)- limonene by P. digitatum (NRRL 1202). Process Biochem. 33: 29-37 (1998) https://doi.org/10.1016/S0032-9592(97)00048-4
  27. Tan Q, Day DF. Bioconversion of limonene to α-terpineol by immobilized Penicillium digitatum. Appl. Microbiol. Biot. 49: 96-101 (1998) https://doi.org/10.1007/s002530051143
  28. Tan Q, Day DF. Organic co-solvent effects on the bioconversion of (R)-(+)-limonene to (R)-(+)-alpha-terpineol. Process Biochem 33: 755-761 (1998) https://doi.org/10.1016/S0032-9592(98)00046-6
  29. Adams A, Demyttenaere JCR, De Kimpe N. Biotransformation of (R)-(+)- and (S)-(-)-limonene to α-terpineol by Penicillium digitatum - investigation of the culture conditions. Food Chem. 80: 525-534 (2003) https://doi.org/10.1016/S0308-8146(02)00322-9
  30. Mar$\'{o}$stica-Jr MR, Pastore GM. Biotransformation of citronellol in rose-oxide using cassava wastewater as a medium. Cienc. Tecnol. Aliment. 26: 609-696 (2006) https://doi.org/10.1590/S0101-20612006000300032
  31. Bicas JL, Barros FFC, Wagner R, Godoy HT, Pastore GM. Optimization of R-(+)-α-terpineol production by the biotransformation of R-(+)-limonene. J. Ind. Microbiol. Biot. 35: 1061-1070 (2008) https://doi.org/10.1007/s10295-008-0383-0
  32. Bakkali F, Averbeck S, Averbeck D, Idaomar M. Biological effects of essential oils - A review. Food Chem. Toxicol. 46: 446-475 (2008) https://doi.org/10.1016/j.fct.2007.09.106
  33. Turina AV, Nolan MV, Zygadlo JA, Perillo MA. Natural terpenes: Self-assembly and membrane partitioning. Biophys. Chem. 122: 101-113 (2006) https://doi.org/10.1016/j.bpc.2006.02.007
  34. Soylu EM, Soylu S, Kurt S. Antimicrobial activity of the essential oils of various plants against tomato late blight disease agent Phytophthora infestans. Mycopathology 161: 119-128 (2006) https://doi.org/10.1007/s11046-005-0206-z
  35. H$\"{o}$gnad$\'{o}$ttir A, Rouseff RL. Identification of aroma active compounds in orange essence oil using gas chromatography-olfactometry and gas chromatography-mass spectrometry. J. Chromatogr. A 998: 201-211 (2003) https://doi.org/10.1016/S0021-9673(03)00524-7
  36. Selli S, Cabaroglu T, Canbas A. Volatile flavour components of orange juice obtained from the cv. Kozan of Turkey. J. Food Compos. Anal. 17: 789-796 (2004) https://doi.org/10.1016/j.jfca.2003.10.005
  37. Sonboli A, Eftekhar F, Yousefzadi M, Kanani MR. Antibacterial activity and chemical composition of the essential oil of Grammosciadium platycarpum Boiss. from Iran. Z. Naturforsch C 60: 30-34 (2005)
  38. Mourey A, Canillac N. Anti-Listeria monocytogenes activity of essential oils components of conifers. Food Control 13: 289-292 (2002) https://doi.org/10.1016/S0956-7135(02)00026-9
  39. Van Sonsbeck HM, Beeftink HH, Tramper J. Two-liquid phase bioreactors. Enzyme Microb. Tech. 15: 722-729 (1993) https://doi.org/10.1016/0141-0229(93)90001-I
  40. L$\'{o}$pez-Varela S, Gonz$\'{a}$lez-Gross M, Marcos A. Functional foods and the immune system: A review. Eur. J. Clin. Nutr. 56: S29-S33 (2002) https://doi.org/10.1038/sj.ejcn.1601481
  41. Raphael TJ, Kuttan G. Immunomodulatory activity of naturally occurring monoterpenes carvone, limonene, and perillic acid. Immunopharm. Immunot. 25: 285-294 (2003) https://doi.org/10.1081/IPH-120020476
  42. Evans DL, Miller DM, Jacobsen KL, Bush PB. Modulation of immune responses in mice by d-limonene. J. Toxicol. Env. Health 20: 51-66 (1987) https://doi.org/10.1080/15287398709530961
  43. Hamada M, Uezu K, Matsushita J, Yamamoto S, Kishino Y. Distribution and immune responses resulting from oral administration of d-limonene in rats. J. Nutr. Sci. Vitaminol. 48: 155-160 (2002) https://doi.org/10.3177/jnsv.48.155
  44. Del Toro-Arreola S, Flores-Torales E, Torres-Lozano C, Del Toro-Arreola A, Tostado-Pelayo K, Ramirez-Due$\~{n}$as MG, Daneri-Navarro A. Effect of d-limonene on immune response in BALB/c mice with lymphoma. Int. Immunopharmacol. 5: 829-838 (2005) https://doi.org/10.1016/j.intimp.2004.12.012
  45. Gould MN. Cancer chemoprevention and therapy by monoterpenes. Environ. Health Persp. 105: 977-979 (1997) https://doi.org/10.2307/3433313
  46. Watson WH, Cai J, Jones DP. Diet and apoptosis. Annu. Rev. Nutr. 20: 485-505 (2000) https://doi.org/10.1146/annurev.nutr.20.1.485
  47. Paduch R, KandeferSzersze$\~{n}$ M, Trytek M, Fiedurek J. Terpenes: Substances useful in human healthcare. Arch. Immunol. Ther. Ex. 55: 315-327 (2007) https://doi.org/10.1007/s00005-007-0039-1
  48. Samaila D, Toy BJ, Wang RC, Elegbede AJ. Monoterpenes enhanced the sensitivity of head and neck cancer cells to radiation treatment in vitro. Anticancer Res. 24: 3089-3095 (2004)
  49. Da Fonseca CO, Masini M, Futuro D, Caetano R, Gattass CR, Quirico-Santos T. Anaplastic oligodendroglioma responding favorably to intranasal delivery of perillyl alcohol: A case report and literature review. Surg. Neurol. 66: 611-615 (2006) https://doi.org/10.1016/j.surneu.2006.02.034
  50. Da Fonseca CO, Landeiro JA, Clark SS, Quirico-Santos T, Carvalho MGC, Gattass CR. Recent advances in the molecular genetics of malignant gliomas disclose targets for antitumor agent perillyl alcohol. Surg. Neurol. 65: 2-9 (2006) https://doi.org/10.1016/j.surneu.2005.06.030
  51. Da Fonseca CO, Schwartsmann G, Fischer J, Nagel J, Futuro D, Quirico-Santos T, Gattass CR. Preliminary results from a phase I/II study of perillyl alcohol intranasal administration in adults with recurrent malignant gliomas. Surg. Neurol. 70: 259-267 (2008) https://doi.org/10.1016/j.surneu.2007.07.040
  52. Bailey HH, Attia S, Love RR, Fass T, Tutsch, RCK, Harris L, Jumonville A, Hansen R, Shapiro GR, Stewart JA. Phase II trial of daily oral perillyl alcohol (NSC 641066) in treatment-refractory metastatic breast cancer. Cancer Chemoth. Pharm. 62: 149-157 (2008) https://doi.org/10.1007/s00280-007-0585-6
  53. Mills JJ, Chari RS, Boyer IJ, Gould MN, Jirtle RL. Induction of apoptosis in liver tumors by the monoterpene perillyl alcohol. Cancer Res. 55: 979-983 (1995)
  54. Elegbede JA, Floresa R, Wang RC. Perillyl alcohol and perillaldehyde induced cell cycle arrest and cell death in BroTo and A549 cells cultured in vitro. Life Sci. 73: 2831-2840 (2003) https://doi.org/10.1016/S0024-3205(03)00701-X
  55. Clark SS. Perillyl alcohol induces c-Myc-dependent apoptosis in Bcr/Abl-transformed leukemia cells. Oncology 70: 13-18 (2006) https://doi.org/10.1159/000091181
  56. Clark SS, Zhong L, Filiault D, Perman S, Ren Z, Gould M, Yang X. Anti-leukemia effect of perillyl alcohol in Bcr/Abl-transformed cells indirectly inhibits signaling through Mek in a Ras- and Rafindependent fashion. Clin. Cancer Res. 9: 4494-4504 (2003)
  57. Wiseman DA, Werner SR, Crowell PL. Cell cycle arrest by the isoprenoids perillyl alcohol, geraniol, and farnesol is mediated by $p21^{Cip1}$ and $p27^{Kip1}$ in human pancreatic adenocarcinoma cells. J. Pharmacol. Exp. Ther. 320: 1163-1170 (2007) https://doi.org/10.1124/jpet.106.111666
  58. Cox AD. Farnesyltransferase inhibitors: Potential role in the treatment of cancer. Drugs 61: 723-732 (2001) https://doi.org/10.2165/00003495-200161060-00002
  59. Lebedeva IV, Su ZZ, Vozhilla N, Chatman L, Sarkar D, Dent P, Athar M, Fisher PB. Chemoprevention by perillyl alcohol coupled with viral gene therapy reduces pancreatic cancer pathogenesis. Mol. Cancer Ther. 7: 2042-2050 (2008) https://doi.org/10.1158/1535-7163.MCT-08-0245
  60. Ariazi EA, Gould MN. Identifying differential gene expression in monoterpene-treated mammary carcinomas using subtractive display. J. Biol. Chem. 271: 29286-29294 (1996) https://doi.org/10.1074/jbc.271.46.29286
  61. Ahn KJ, Lee CK, Choi EK, Griffin R, Song CW, Park HJ. Cytotoxicity of perillyl alcohol against cancer cells is potentiated by hyperthermia. Int. J. Radiat. Oncol. 57: 813-819 (2003) https://doi.org/10.1016/S0360-3016(03)00737-5
  62. Holstein SA, Hohl RJ. Monoterpene regulation of Ras and Rasrelated protein expression. J. Lipid Res. 44: 1209-1215 (2003) https://doi.org/10.1194/jlr.M300057-JLR200
  63. Loutrari H, Hatziapostolou M, Skouridou V, Papadimitriou E, Roussos C, Kolisis FN, Papapetropoulos A. Perillyl alcohol is an angiogenesis inhibitor. J. Pharmacol. Exp. Ther. 311: 568-575 (2004) https://doi.org/10.1124/jpet.104.070516