Antifertility Potential of n-Butanol and Ethyl Acetate Extracts of Penicillium oxalicum OM282858 in Male Albino Rats as Biological Control Agents
DOI:
https://doi.org/10.18006/2022.10(6).1354.1365Keywords:
Antifertility, Biological control, Penicillium oxalicum, Testicular toxicityAbstract
Rodents cause significant damage to many crops, spread diseases, and pose a severe risk to public health. Several synthetic contraceptive agents are available for controlling rodents; however, their use is associated with toxic effects on non-target organisms. Penicillium oxalicum has several medical properties, but no reports were available on fertility. This study aimed to assess the antifertility potential of n-butanol and ethyl acetate extracts of P. oxalicum in adult male albino rats as biological control agents by lowering the population size of rodent pests. Rats were assigned into three groups (n = 36). The first control group (GI) was injected intraperitoneally with 0.5% dimethyl sulfoxide (DMSO). The second (GII) and third (GIII) groups were injected with a single dose of 200 mg/kg body weight (b.wt.) of n-butanol and ethyl acetate extracts of P. oxalicum intraperitoneally, respectively, after dissolving in 0.5% DMSO. Further, P. oxalicum was identified morphologically and molecularly and then submitted with accession number OM282858 to the National Center for Biotechnology Information (NCBI) GenBank. The antifertility potential of P. oxalicum was evaluated after 24 h (the injection period), 96 h, and 168 h (the recovery periods) of treatments. The effects of the treatments on organ weight, testicular histology, histomorphometry measurements, and sperm characteristics were assessed. Both P. oxalicum extracts caused changes in reproductive organ weights, testicular histology, histomorphometry measurements, and spermatogenic arrest accompanied by a significant decrease in the count of epididymal sperm and its motility and an increase in the percentage of sperm abnormalities during the injection and recovery periods. Thus, the results suggest that both P. oxalicum extract treatments cause suppression of fertility in adult male rats. Therefore, these outcomes are essential for public health, farming establishments, and vertebrate pest control managers.
References
Abdel- Azeem, M. I. (2008). Ecological studies on some commensal rodent species and their ectoparasites in different habitats at Sharkia governorate. M. Sc. Thesis, Faculty of Agriculture Sciences, Suez Canal University, Egypt. 193.
Aktar, M. T., Hossain, K. S., & Bashar, M. A. (2014). Antagonistic potential of rhizosphere fungi against leaf spot and fruit rot pathogens of brinjal. Bangladesh Journal of Botany, 43(2), 213-217. https://doi.org/10.3329/bjb.v43i2.21675 DOI: https://doi.org/10.3329/bjb.v43i2.21675
Arenas, M. I., Bethencourt, F. R., De Miguel, M. P., Fraile, B., Romo, E., & Paniagua, R. (1997). Immunocytochemical and quantitative study of actin, desmin and vimentin in the peritubular cells of the testes from elderly men. Reproduction, 110(1), 183–193. https://doi.org/10.1530/jrf.0.1100183 DOI: https://doi.org/10.1530/jrf.0.1100183
Asyura, C., Hasan, A., Hasim, Julistiono, H., Husnawati, Bermawie, N., & Riyanti, E. (2017). Effectiveness of ethyl acetate extract of endophytic fungi in soursop leaves towards the growth of mammary tumor induced by 7,12-dimethylbenz(α)anthracene in female rats. Annual Research & Review in Biology, 18(5), 1–8. https://doi.org/10.9734/arrb/2017/34656 DOI: https://doi.org/10.9734/ARRB/2017/34656
Bloom, E. (1950). Fertility in male animals. Journal of Fertility and Sterility, 1, 223-224. DOI: https://doi.org/10.1016/S0015-0282(16)30183-2
Charnley, A.K., & Collins, S.A. (2007). Entomopathogenic fungi and their role in pest control. In: C.P. Kubicek, & I.S. Druzhinina, (Eds.), The Mycota IV: Environmental and Microbial Relationships, 2nd Edition, Springer-Verlag, Berlin, pp. 159-187.
Creasy, D. M. (2003). Evaluation of testicular toxicology: A synopsis and discussion of the recommendations proposed by the society of toxicologic pathology. Birth Defects Research Part B: Developmental and Reproductive Toxicology, 68(5), 408–415. https://doi.org/10.1002/bdrb.10041 DOI: https://doi.org/10.1002/bdrb.10041
Currie, J. N., & Thom, C. (1915). An oxalic acid producing Penicillium. The Journal of Biological Chemistry, 22, 287–293. http://dx.doi.org/10.1016/S0021-9258(18)87646-3 DOI: https://doi.org/10.1016/S0021-9258(18)87646-3
De Souza Predes, F., Diamante, M. A. S., & Dolder, H. (2010). Testis response to low doses of cadmium in Wistar rats. International Journal of Experimental Pathology, 91(2), 125–131. https://doi.org/10.1111/j.1365-2613.2009.00692.x DOI: https://doi.org/10.1111/j.1365-2613.2009.00692.x
Dox, A. W. (1909). The intracellular enzymes of lower fungi, Especially those of Penicillium camemberti. Journal of Biological Chemistry, 6(5), 461–467. https://doi.org/10.1016/s0021-9258(18)91606-6 DOI: https://doi.org/10.1016/S0021-9258(18)91606-6
Felsenstein, J. (1985). Confidence limits on phylogenies: an approach using the bootstrap. Evolution, 39(4), 783–791. https://doi.org/10.1111/j.1558-5646.1985.tb00420.x DOI: https://doi.org/10.1111/j.1558-5646.1985.tb00420.x
Gardes, M., & Bruns, T. D. (1993). ITS primers with enhanced specificity for basidiomycetes application to the identification of mycorrhizae and rusts. Molecular Ecology, 2, 113-118. http://dx.doi.org/10.1111/j.1365-294X.1993.tb00005.x DOI: https://doi.org/10.1111/j.1365-294X.1993.tb00005.x
Gong, Y., & Han, X. D. (2006). Effect of nonylphenol on steroidogenesis of rat leydig cells. Journal of Environmental Science and Health, Part B: Pesticides, Food Contaminants, and Agricultural Wastes, 41(5), 705–715. https://doi.org/10.1080/ 03601230600701866 DOI: https://doi.org/10.1080/03601230600701866
Greco, C., Keller, N. P., & Rokas, A. (2019). Unearthing fungal chemodiversity and prospects for drug discovery. Current Opinion in Microbiology, 51, 22–29. https://doi.org/10.1016/ j.mib.2019.03.002 DOI: https://doi.org/10.1016/j.mib.2019.03.002
Hidayati, N. L. D., Tita, N., Nur, R., Yuliana, D., & Yani, S. (2018). Antifertility activities of ethanol extract of sugar apple leaves (Annona squamosa L.) in the reproductive system: spermatogenesis and sperm quality study. Pharmaciana, 8(2), 339-348. DOI: https://doi.org/10.12928/pharmaciana.v8i2.7543
Huether, S. E., & McCance, K. L. (2008). Understanding Pathophysiology, (3rd ed.). St. Louis, Mo. Mosby/Elsevier, pp. 488-501.
Johnsen, S. G. (1970). The stage of spermatogenesis involved in the testicular-hypophyseal feed-back mechanism in man. Acta Endocrinologica, 64(2), 193–210. https://doi.org/10.1530/ acta.0.0640193 DOI: https://doi.org/10.1530/acta.0.0640193
Johnson, L. F., & Curl, E. A. (1971). Methods for research on the ecology of soil-borne plant pathogens. Burgess International Group Incorporated
Kataria, S. K., Singh, P., Pandove, G., Kalia, A., & Chandi, R. S. (2018). Penicillum oxalicum spg1: A novel entomopathogenic fungus isolated from mummified Bemisia tabaci (Gennadius) of cotton. Journal of Applied and Natural Science, 10(1), 138-143. http://dx.doi.org/10.31018/jans.v10i1.1593 DOI: https://doi.org/10.31018/jans.v10i1.1593
Kaur, M., Chadha, P., Kaur, S., & Kaur, A. (2021). Aspergillus flavus induced oxidative stress and immunosuppressive activity in Spodoptera litura as well as safety for mammals. BMC Microbiology, 21(1), 180. https://doi.org/10.1186/s12866-021-02249-4 DOI: https://doi.org/10.1186/s12866-021-02249-4
Kubátová, A., Hujslová, M., Frisvad, J. C., Chudíková, M., & Kolaík, M. (2019). Taxonomic revision of the biotechnologically important species, Penicillium oxalicum with description of two new species from acidic and saline soils. Mycological Progress, 18(1-2), 215-228. https://doi.org/10.1007/s11557-018-1420-7 DOI: https://doi.org/10.1007/s11557-018-1420-7
Lucas, E. M., Castro, M. C., & Takahashi, J. A. (2007). Antimicrobial properties of sclerotiorin, isochromophilone VI and pencolide, metabolites from a Brazilian cerrado isolate of Penicillium sclerotiorum Van Beyma. Brazilian Journal of Microbiology, 38(4), 785-789.http://dx.doi.org/10.1590/S1517-83822007000400036 DOI: https://doi.org/10.1590/S1517-83822007000400036
Mahmoud, Y., Taha, A., & Soliman, S. (2018). 3-Monochloropropane-1,2-diol (alpha-chlorohydrin) disrupts spermatogenesis and causes spermatotoxicity in males of the Egyptian fruit-bat (Rousettus aegyptiacus). Biotechnic & Histochemistry, 93(4), 293–300. https://doi.org/10.1080/ 10520295.2018.1437471 DOI: https://doi.org/10.1080/10520295.2018.1437471
Mathur, N., Jain, G. C., & Pandey, G. (2010). Effect of tecoma stans leaves on the reproductive system of male albino rats. International Journal of Pharmacology, 6(2), 152–156. https://doi.org/10.3923/ijp.2010.152.156 DOI: https://doi.org/10.3923/ijp.2010.152.156
Memon, M. A., Bretzlaff, K. N., & Ott, R. S. (1986). Comparison of semen collection techniques in goats. Theriogenology, 26(6), 823–827. https://doi.org/10.1016/0093-691x(86)90011-7 DOI: https://doi.org/10.1016/0093-691X(86)90011-7
Mesbah, S. F., Shokri, S., Karbalay-Doust, S., & Mirkhani, H. (2008). Effects of nandrolone decanoate on ultrastructure of testis in male adult rats. Iranian Journal of Medical Sciences, 33, 94-100. https://doi.org/10.1016%2Fj.sjbs.2020.09.039
Muharni, M., & Heni, Y. (2018). A subchronic toxicity test of ethyl acetate extract from endophytic fungus Penicillium sp. of kunyitputih (Curcuma zedoaria) against Swiss albino mice. Journal of Chinese Pharmaceutical Sciences, 27(2),123–130. https://doi.org/10.5246/jcps.2018.02.014 DOI: https://doi.org/10.5246/jcps.2018.02.014
Paini, S. W., Tarsisius, D. W. B., Fenny, A. K., & Evelyn, L. W. (2014). Difference of solvent polarity to phytochemical content and antioxidant activity of Pluchea indicia less leaves extracts. International Journal of Pharmacognosy and Phytochemical Research, 6(4), 850–855.
Petit, P., Lucas, E. M. F., Abreu, L. M., Pfenning, L. H., & Takahashi, J. A. (2009). Novel antimicrobial secondary metabolites from a Penicillium sp. isolated from Brazilian cerrado soil. Electronic Journal of Biotechnology, 12(4), 1-9. https://doi.org/ 10.2225/vol12-issue4-fulltext-9 DOI: https://doi.org/10.2225/vol12-issue4-fulltext-9
Rambaut, A. (2020). Figtree, version 1.4.4; Available online: http//tree.bio.ed.ac.uk/software/figtree/.
Reddy, P. S., Rani, G. P., Sainath, S. B., Meena, R., & Supriya, CH. (2011). Protective effects of N-acetylcysteine against arsenic-induced oxidative stress and reprotoxicity in male mice. Journal of Trace Elements in Medicine and Biology, 25(4), 247–253. https://doi.org/10.1016/j.jtemb.2011.08.145 DOI: https://doi.org/10.1016/j.jtemb.2011.08.145
Rotem, J. (1994). The Genus Alternaria. Biology, Epidemiology and Pathogenicity. APS Press, Saint Paul.
Santamarina, M. P., Roselló, J., Llacer, R., & Sanchis, V. (2002). Antagonistic activity of Penicillium oxalicum Currie and Thom, Penicillium decumbens Thom and Trichoderma harzianum Rifai isolates against fungi, bacteria and insects in vitro. Revista Iberoamericana de Micologia, 19, 99-103.
Schumacher, J., & Moll, H. D. (2011). Collection of semen. In J. Schumacher, and H. D. Moll, (Eds.) A Manual of Equine Diagnostic Procedures. Teton New Media, Jackson, WY, International Veterinary Information Service, USA, No. A5420.1011.
Shankar, A., & Sharma, K. K. (2022). Fungal secondary metabolites in food and pharmaceuticals in the era of multi-omics. Applied Microbiology and Biotechnology, 106(9-10), 3465–3488. https://doi.org/10.1007/s00253-022-11945-8 DOI: https://doi.org/10.1007/s00253-022-11945-8
Soliman, S., Mahmoud, Y. M., & Taha, A. (2016). Evaluating the efficacy of the male chemosterilantalpha-chlorohydrin on three Egyptian wild rodent pests under laboratory conditions. Egyptian Journal of Zoology, 66, 71-84. http://dx.doi.org/10.12816/0034709 DOI: https://doi.org/10.12816/0034709
Stackebrandt, E., & Goebel, B. (1994). Taxonomic Note: A Place for DNA-DNA Reassociation and 16S rRNA Sequence Analysis in the Present Species Definition in Bacteriology. International Journal of Systematic Bacteriology, 44, 846-849.
http://dx.doi.org/10.1099/00207713-44-4-846 DOI: https://doi.org/10.1099/00207713-44-4-846
Taha, A. (2022). Assessment of non-target toxicity of profenofos insecticide on the aquatic bird; the white egret, Egretta alba. Egyptian Journal of Aquatic Biology and Fisheries, 26(2), 263 – 276. http://dx.doi.org/10.21608/ejabf.2022.228725 DOI: https://doi.org/10.21608/ejabf.2022.228725
Taha, A., & Soliman, S. (2019). Effect of α-chlorohydrin water-bait on the fertility of captive males of the Egyptian fruit-bat (Rousettus aegyptiacus) and the proper time for controlling its free-ranging populations in Egypt. Egyptian Journal of Aquatic Biology and Fisheries, 23(4), 27-237. http://dx.doi.org/ 10.21608/ejabf.2019.53599. DOI: https://doi.org/10.21608/ejabf.2019.53599
Tamura, K., Stecher, G., & Kumar, S. (2021). MEGA 11: Molecular Evolutionary Genetics Analysis Version 11. Molecular Biology and Evolution, 38 (7), 3022–3027. https://doi.org/10.1093/ molbev/msab120 DOI: https://doi.org/10.1093/molbev/msab120
Tirumale, S., Wani, N., & Khanday, W. (2020). Phytochemical analysis and evaluation of antibacterial activity of different extracts of soil-isolated fungus Chaetomium cupreum. Journal of Natural Science, Biology and Medicine, 11(1), 72. https://doi.org/10.4103/ jnsbm.jnsbm_150_19k DOI: https://doi.org/10.4103/jnsbm.JNSBM_150_19
Tobin, M.E., & Fall, M. W. (2004). Pest control: rodents. USDA National Wildlife Research Center - Staff Publications, pp. 67.
Umemoto, S., Odake, Y., Takeuchi, T., Yoshida, S., Tsushima, S., & Koitabashi, M. (2009). Blue mold of tomato caused by Penicillium oxalicum in Japan. Journal of General Plant Pathology, 75, 399-400. http://dx.doi.org/10.1007/s10327-009-0180-2. DOI: https://doi.org/10.1007/s10327-009-0180-2
Vainio, E. J., Ktwhiteorhonen, K., & Hantula, J. (1998). Genetic variation in Phlebiopsis gigantea as detected with random
amplified microsatellite (RAMS) markers. Mycological Research, 102(2), 187–192. https://doi.org/10.1017/s0953756297004577 DOI: https://doi.org/10.1017/S0953756297004577
Weng, W., Li, R., Zhang, Y., Pan, X., Jiang, S., et al. (2022). Polyketides isolated from an endophyte Penicillium oxalicum 2021CDF-3 inhibit pancreatictumor growth. Frontiers in Microbiology, 13, 1033823. https://doi.org/10.3389/ fmicb.2022.1033823 DOI: https://doi.org/10.3389/fmicb.2022.1033823
White, T. J., Bruns, T., Lee, S., & Taylor, J. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protocols, 315–322. https://doi.org/10.1016/ b978-0-12-372180-8.50042-flrpet DOI: https://doi.org/10.1016/B978-0-12-372180-8.50042-1
World Health Organization (2000). Laboratory manual: for the examination of human semen and sperm-cervical mucus interaction, 4thedn. Cambridge, Cambridge University Press.
Yang, L., Xie, J., Jiang, D., Fu, Y., Li, G., & Lin, F. (2008). Antifungal substances produced by Penicillium oxalicum strain PY-1—potential antibiotics against plant pathogenic fungi. World Journal of Microbiology & Biotechnology, 24, 909–915. http://dx.doi.org/10.1007/s11274-007-9626-x. DOI: https://doi.org/10.1007/s11274-007-9626-x
Zhang, P., Wei, Q., Yuan, X., & Xu, K. (2020). Newly reported alkaloids produced by marine-derived Penicillium species (covering 2014–2018). Bioorganic Chemistry, 99, 103840. https://doi.org/10.1016/j.bioorg.2020.103 DOI: https://doi.org/10.1016/j.bioorg.2020.103840
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