Non-Terpenoid Biotransformations by Mucor Species

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Non-Terpenoid Biotransformations by Mucor Species Phytochem Rev (2015) 14:745–764 DOI 10.1007/s11101-014-9374-0 Non-terpenoid biotransformations by Mucor species Eliane de Oliveira Silva • Niege Arac¸ari Jacometti Cardoso Furtado • Josefina Aleu • Isidro Gonza´lez Collado Received: 18 March 2014 / Accepted: 21 July 2014 / Published online: 1 August 2014 Ó Springer Science+Business Media Dordrecht 2014 Abstract Biotransformation is an important tool for Introduction the structural modification of organic compounds, especially natural products with complex structures, Microbial transformation is regarded as an enzymatic which are difficult to achieve using ordinary methods. reaction by using the metabolic activities of microor- It is also useful as a model for mammalian metabolism ganisms to modify the chemical structures of bioactive due to similarities between mammalian and microbial substrates for finding the new chemical derivatives enzyme systems. The development of novel biocata- with the potent bioactivities and physical–chemical lytic methods is a continuously growing area of characteristics. It has a number of advantages over chemistry, microbiology, and genetic engineering, and chemical synthesis such as higher stereo- and regio- novel microorganisms and/or their enzymes are being selectivity, milder reaction conditions, lower cost and screened intensively. This review covers the transfor- less pollution. Furthermore, some reactions that do not mation of non-terpenoid compounds such as steroids, occur when using chemical approaches are easily coumarins, flavonoids, drugs, pesticides and others by carried out by microbial transformation (Chen et al. Mucor spp. up to the end of 2012. 2009). Microorganisms can be used as a reliable and Keywords Biotransformation Á Mucor sp. Á Non- efficient alternative to in vivo studies or to synthetic terpenoid chemistry to obtain sizable amounts of a number of drug derivatives in metabolism studies. Metabolism is the structural modification of drugs and chemicals by enzymatic systems which leads to the formation of E. d. O. Silva Á N. A. J. C. Furtado relatively polar substances which are easily excreted Departamento de Cieˆncias Farmaceˆuticas, Faculdade de from the organism. An important factor in the Cieˆncias Farmaceˆuticas, Universidade de Sa˜o Paulo, evaluation of the safety and effectiveness of any drug Avenida do Cafe´, s/n, Ribeira˜o Preˆto, Sa˜o Paulo 14040-903, Brazil is knowledge of its metabolism (Asha and Vidyavathi 2009). The use of microorganisms to simulate the J. Aleu (&) Á I. G. Collado (&) mammalian metabolism of many pharmacologically Departamento de Quı´mica Orga´nica, Facultad de important molecules is well documented (Rosazza and Ciencias, Universidad de Ca´diz, Campus Rı´o San Pedro, 11510 Puerto Real, Ca´diz, Spain Smith 1979; Smith and Rosazza 1975, 1983). e-mail: josefi[email protected] On the other hand, the use of the biotransformations I. G. Collado to carry out useful chemistry processes may be e-mail: [email protected] complicated by inhibitory and toxic properties of 123 746 Phytochem Rev (2015) 14:745–764 reactants and/or products, biocatalysts sensibility to the steroid skeleton which act as directing groups. environmental extremes of temperature and pH, and These groups facilitate the binding of the steroid to the low quantity to derivatives production. However, there hydroxylase, possibly by hydrogen bonding, and bring are biological and process solutions to many of these the centre which is to be hydroxylated within the problems and methods to compare strategies and sphere of the oxidative co-enzyme (Al-Fouti and techniques for biotransformation operation are being Hanson 2002). developed (Lilly 1994). Fungi from the Mucor genus very effectively carry From among the fungi used in biotransformation out hydroxylations of several C19 and C21 steroids at processes, Mucor species have the ability to metabo- the C-7 and C-14 positions to produce important lize a wide variety of compounds in manners that are intermediates used in the synthesis of pharmacolog- similar to those in mammalian enzyme systems. ically active steroid derivatives. The 14a-hydroxylase Microbial reactions have been used to achieve appears to have broad substrate specificity. However, chemical transformations as a part of synthetic proce- steroids with a bulky substitution at the C-17 a- dures integrating green chemistry principles into drug position or without the 4-en-3-one group are not design. The aim of this review is to trace the accepted as substrates by the 14a-hydroxylase system biotransformation of non-terpenoid compounds by (Madyastha 1994; Hu et al. 1995). Mucor species up to the end of 2012. Several fungi have been shown to introduce a hydroxyl group at the 14a-position of progesterone (1) and some other steroids in reasonable yields. Thus, Biotransformation of steroids Mucor parasiticus ATCC 6476 and Mucor griseocy- anus ATCC 1207 were found to oxygenate progester- Steroids are widely distributed in the animal and plant one (1), deoxycorticosterone (2), 11-deoxycortisol (3) kingdom. The basic skeleton consists of 17 carbon and testosterone (4) to the corresponding 14a-hydrox- atoms arranged in the form of a perhydrocyclopenta- ylated steroids (Fig. 1; Eppstein et al. 1958). The nophenanthrene. They vary widely in structure and biotransformation of the hydroxyl-derivatives from 1, contain vital compounds such as cholesterol, bile 2 and 4 by M. griseocyanus ATCC 1207 also mainly acids, sex hormones, vitamin D, corticoid hormones, produced 14a-hydroxy derivatives. However, in the cardiac aglycones, antibiotics, and insect molting case of 17a-methyl-substituted steroids, the main hormones (Bhatti and Khera 2012). transformation products were the 7a-hydroxy deriva- Fungi have proved to be powerful biocatalysts in tives (Singh et al. 1967). steroid biotransformations since their enzymatic and Progesterone (1) was converted by Mucor hiemalis metabolic systems can be used to modify a wide range NRRL 2684 to 7a,14a-dihydroxyprogesterone, which of this class of compounds. inhibited sodium retention induced by deoxycorticos- A variety of steroids are widely used as anti- terone (2) and this bioprocess generated a patent inflammatory, diuretic, anabolic, contraceptive, anti- (Dodson and Tweit 1960). Mucor piriformis was also androgenic, progestational and anticancer agents, as used to study the mode of transformation of proges- well as in other applications. Hydroxysteroids have terone (1). The major metabolites isolated and iden- been reported as having useful biological activities tified were 14a-hydroxyprogesterone, 7b,14a- and several microorganisms, e.g. Mucor spp., are dihydroxyprogesterone, 7a,14a-dihydroxyprogester- capable of bringing about these hydroxylations (Mah- one, and 6b,14a-dihydroxyprogesterone. Time-course ato and Mukherjee 1984; Mahato and Banerjee 1985; studies of transformation product formation showed Mahato and Majumdar 1993; Mahato and Garai 1997; that hydroxylation at the 14a-position is the first step Al-Footy 2008a, b). Steroid hydroxylation is also an in the formation of dihydroxyprogesterones (Madyas- important enzymatic reaction in mammalian organ- tha and Srivatsan 1987). isms due to the detoxification of exogenous steroid The first commercialized microbial process in the drugs (Lacroix et al. 1999). steroid field was in the production of 11a-hydroxy- The regio-chemistry of the microbiological hydrox- progesterone, a compound with antiandrogenic and ylation of steroids has been rationalized in terms of the blood-pressure-regulating activity. In this case, Mucor positions of existing hydroxyl or carbonyl groups on racemosus NRRL 3639 and mutants from M. 123 Phytochem Rev (2015) 14:745–764 747 Fig. 1 Steroids used in O HO O O OH biotransformations by 18 20 Mucor spp OH 19 11 13 17 1 14 10 8 15 3 O 5 6 O O 1 2 3 OH O O OH H O O O 4 5 6 racemosus NRRL 3639 efficiently hydroxylated pro- interesting tool to provide derivatives with pharma- gesterone (1)to11a-hydroxy progesterone (El Minofy cological potential. et al. 2000; Hamdi et al. 2000; Khattab and Abd-El Microbial models produce satisfactory results when Salam 2012). used to study mammalian steroid metabolism path- Screening of fungal cultures for their ability to ways. The ability of microbial species to produce monohydroxylate steroids at unusual sites showed that different metabolites which are sometimes not achiev- fungal strains were capable of dehydrogenating ring B able by chemical synthesis has made them indispens- of progesterone (1) and androstenedione (5) at posi- able to the pharmaceutical industry. Androst-4-ene- tions C6–C7. Smith et al. (1989) described the use of 3,17-dione (5) is among the most important interme- M. racemosus to produce 11a-hydroxy-6-dehydropro- diates in the production of some valuable pharmaceu- gesterone from progesterone (1), which would be tical steroid compounds. Several Mucor spp. have difficult and time-consuming to synthesize by con- been shown to carry out different kinds of transfor- ventional synthetic chemical methods. mations on that molecule. Thus, 14a,17b-dihydrox- 17-Methyltestosterone, an important anabolic yandrost-4-en-3-one monohydrate and 14a,17b- 17-methyl steroid derived from testosterone (4), has dihydroxyandrosta-1,4-dien-3-one monohydrate were therapeutic uses such as weight gain after surgery, identified in M. piriformis biotransformations from treatment of trauma, birth control, regulation of androst-4-ene-3,17-dione (5) (Krishnan et al. 1991). inflammation, and treatment of other diseases. The
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