Pennisetum Purpureum (Elephant grass) Protects Against Hydrogen Peroxide Induced Reproductive Toxicity in Drosophila Melanogaster

Izam Y. Y., Amagon K., Sabo S. Y.,

doi:10.5281/zenodo.15049032

Research Paper | Open Access
Volume 03 | Issue 03 | Article Id IJPS/250303094

Pennisetum Purpureum (Elephant grass) Protects Against Hydrogen Peroxide Induced Reproductive Toxicity in Drosophila Melanogaster
Izam Y. Y.* Amagon K. Sabo S. Y.
Department of Pharmacology and Toxicology, Faculty of Pharmaceutical Sciences, University of Jos, Nigeria.

Abstract

Introduction: Reactive oxygen species (ROS) are essential for sperm function and ovulation. However, excessive ROS could initiate cascades of reactions with macromolecules of the human gametes leading to compromised functionality and viability of sperm cells in males, as well as alteration in follinculogenesis and early stage embryonic development in females. The present study demonstrated the impact of the extracts and fractions of Pennisetum purpureum on Drosophila reproductive function under oxidative stress. Method: The reproductive ability of Drosophila was studied after exposing the flies to different concentrations of the plant’s extracts and fractions for 14 days. The cumulative number of larva, pupae and adult flies that emerged during this period of 14 days represents a measure of fecundity or reproductive ability. Results: The result obtained showed that there was a significant increase in the number of larva, pupae and emerged adults in all treatment groups when compared to the negative control (H202) this suggest an improvement in the reproductive ability of the fruit flies. Discussion/Conclusion: The extracts and fractions of the plant were able to exert a protective effect against the negative impact of the toxicant by significantly increasing the number of larvae, pupae and emerged adult flies. This may be due to the presence of alkaloids, steroids, phenols and flavonoids which could interact with the endocrine system of insects influencing the production and regulation of hormones involved in reproduction.

Keywords

follinculogenesis, sperm cells, macromolecules, gametes, embryonic, endocrine.

Introduction

Reactive oxygen species, have a significant role in controlling the expression of specific genes and proteins that regulate cellular biological functions such as proliferation, differentiation, and apoptosis ^{1, 2}. Psychological stress, lifestyle influences such as drugs, alcohol, smoking and sedentary lifestyles promote rapid production of ROS ³. Superoxide anion, hydrogen peroxide, hydroxyl radical, peroxyl, and hydroperoxyl are biologically significant ROS that cause oxidative stress ⁴. In the female reproductive system, ROS are involved in tissue remodelling, hormone signalling, and cyclic endometrial alterations during menstruation. In the ovary, ROS regulate the germ cell function, maturation of ova, follicle synthesis and maturation, ovulation, tubal function, and steroid hormone production by ovaries ⁵. ROS also impact the disintegration of the corpus luteum, implantation, and normal parturition ^{5, 6}. The concentration of ROS and antioxidants in the ovaries, follicular fluid, and peritoneal fluid determines the oocyte quality, fertilization of ova with the sperm, implantation, and the development of an embryo. Studies conducted in in-vivo and in-vitro models have shown the involvement of the ROS in vascular endothelial growth factor signalling, which stimulates the angiogenesis process ⁷. Further, it implicates the role of ROS in folliculogenesis and early-stage embryonic development ⁴. The male reproductive system is particularly predisposed to oxidative stress, primarily attributed to the unique characteristics of sperm cells. Sperm cell membranes contain highly unsaturated fatty acids, making them highly vulnerable to ROS attack ⁸. Additionally, spermatozoa have limited antioxidant enzyme systems, further exacerbating their vulnerability to oxidative damage ⁹. Lipid peroxidation is one of the basic mechanisms through which oxidative stress affects male reproductive function. ROS attack the polyunsaturated fatty acids in sperm cell membranes, initiating a chain reaction known as lipid peroxidation. This process leads to the production of lipid peroxides and the disruption of membrane integrity. As a result, the functionality and viability of sperm are compromised, leading to impaired motility and reduced fertilization capacity ¹⁰. Another mechanism by which oxidative stress impacts male reproductive function is through protein oxidation. ROS can modify proteins in sperm, leading to structural alterations and functional impairments. This oxidative damage to proteins can upset various aspects of sperm physiology, including motility, DNA packaging, and fertilization ability ¹¹. Sperm DNA is highly compacted and tightly packaged within the nucleus, making it more susceptible to oxidative damage. ROS can directly attack and cause oxidative lesions in the DNA strand, resulting to DNA fragmentation and impaired genetic integrity. Such DNA damage in sperm has been linked to reduced fertilization rates, decreased embryo quality, and an increased risk of developmental abnormalities in offspring ¹². These mechanisms collectively highlight oxidative stress's significant impact on male reproductive function. Understanding the mechanisms by which oxidative stress impacts male and female reproductive function, is crucial in elucidating its impact in infertility. It also emphasizes the need for strategies to mitigate oxidative damage, such as antioxidant supplementation, to preserve and enhance reproductive health in both males and females ¹³_.

MATERIALS AND METHODS

Laboratory Equipment Materials and other reagents

Beakers (Pyrex England), test tubes (vials) (Pyrex), measuring cylinder, (Pyrex England), refrigerator (Thermacool), stock clock, cotton wool, disposable gloves, digital weigh balances, analytical balance, Hydrogen peroxide (H₂0₂), distilled water.

Drosophila melanogaster stock and media

The Harwich strain of Drosophila melanogaster was cultured at the Africa Centre of Excellence in Phytomedicine Research and Development (ACEPRD) Fly Laboratory, University of Jos, Jos, Nigeria. Flies were fed with standard yellow corn meal medium mixed with brewer's yeast (1 % w/v), agar (1 % w/v), and methylparaben (0.08 % w/v) and maintained under the prescribed temperature (23 ± 1°C), relative humidity (60 %) and natural night and day cycle.

The lethal concentration (LD₅₀), determination

The concentration used in this study was obtained by exposing the flies to different concentrations of the plant extracts and fractions for 7 days. Thereafter, the LC₅₀ of the plant extracts and fractions was determined to be 300.61 mg per 10g diet, for methanol extract, 320.94 mg per 10 g diet for aqueous extract, 150.08 mg per 10 g diet for n-hexane, 480.24 mg per 10 g diet for ethyl acetate fraction and 820.25 mg per 10 g diet for methanol fraction. This values shows that the extracts and fractions are relatively safe.

Fecundity Assay (Reproductive Ability)

Fifty (50) flies were fed with food supplemented with different concentrations of methanol and aqueous extract, n-hexane, ethyl acetate and methanolic fractions of Pennisetum purpureum in 3 replicates for 7 days ^{14, 15}. The flies were then exposed to 1 % hydrogen peroxide (H₂O₂), for 24 hours ^{16, 17, 18}. After the various exposure period, (10) (5males, 5 females) were randomly selected from each group and were assayed for reproductive ability as described by (Adedera et al., Iorjiim et al., ^{14, 15} with slight modification. Ten flies (5 males and 5 females) from each treatment group were paired in vials containing standard flies’ food. The vials were labelled and kept for 24 hours where they mated and lay eggs, after which the adult flies were removed. The vials (with eggs therein) were observed daily for 14 days for larvae, pupae and emergence of adult flies. The cumulative number larva, pupae and adult flies that emerged during this period of 14 days represents a measure of fecundity or reproductive ability.

Statistical Analysis

All data in this study were presented as Mean ± Standard Error of the Mean (SEM) and analyzed using ANOVA (analysis of variance) followed by Turkey’s post hoc test to determine means with statistical differences. The decision rule of P<0.05 for significance was adopted for all means.

Table 1: The effect of various concentration of P. purpureum extracts and fractions on the number of third instar larva in D. melanogaster

Fractions	LC_6.25	LC_12.5	LC₂₅	LC₅₀
Ethyl acetate	23.00±1.53^h	20.67±2.03^h	17.00±1.16^h	13.33±0.88^h
n-Hexane	13.33±1.45^g	10.33±1.33^g	5.33±0.88^gb	3.67±0.67^gb
Methanol	32.67±1.20^f	27.00±1.16^f	21.33±0.88^f	19.33±0.88^f
Aqueous	26.33±1.45^e	15.67±1.20^e	11.67±0.67^e	7.00±1.16^g
Methanol crude	44.00±1.73^d	37.67±1.33^d	33.00±1.16^d	27.00±1.16^d
Standard	55.67±1.45	46.67±1.45	43.67±1.76	36.00±1.73
H₂O₂	5.33±0.88	5.33±0.88	5.33±0.88	5.33±0.88
Control	62.67±1.45	62.67±1.45	62.67±1.45	62.67±1.45
F	193.205	198.014	323.833	335.403
p-value	0.001	0.001	0.001	0.001

Means under the same column tagged with different letter alphabets compares significantly different with ^aControl, ^bH₂O₂, ^cStandard, otherwise they are the same. ^#Means under the same column with significant higher intended effect than Standard drug. Table 1 shows the effects of various concentration of Pennisetum purpureum extracts and fractions on the number of third instar larva in Drosophila melanogaster. The toxicant group (H₂O₂) conferred significant decrease (lethal effect), on the number of third instar larva in Drosophila melanogaster. There was a significant decrease in lethal activity on groups supplemented with the various concentrations of the extracts and fractions of Pennisetum purpureum. At all concentrations (LC_6.25, LC_12.5, LC₂₅ and LC₅₀)_, Methanol pg. 1786extract had the highest number of third instar larva (highest effect) compared to other treatment groups.

Table 2: The effect of various concentrations of P. purpureum extracts and fractions on the number of pupae that emerged in D. melanogaster.

Fractions	LC_6.25	LC_12.5	LC₂₅	LC₅₀
Ethyl acetate	18.00±0.58^h	12.67±1.45^h	9.33±1.20^h	7.00±1.16^h
n-Hexane	45.00±1.16^g	41.67±0.88^g	41.00±1.16^g	35.33±0.88^g
Methanol	52.67±2.23^f	47.00±1.16^f	43.33±0.88^f	35.67±2.40^f
Aqueous	38.33±2.03^e	32.00±1.53^e	27.00±0.16^e	23.00±1.73^e
Methanol	70.67±1.20^d	65.00±1.16^dc	56.00±1.73^dc#	49.33±1.45^dc#
Standard	74.67±2.60^a	68.67±2.60	52.33±1.45	47.67±1.76
H₂O₂	5.57±1.16	5.57±0.33	5.57±0.67	5.57±0.33
Control	74.00±2.08	74.00±2.08	74.00±2.08	74.00±2.08
F	205.906	272.425	308.073	212.136
p-value	0.001	0.001	0.001	0.001

Means under the same column tagged with different letter alphabets compares significantly different with aControl, bH2O2, cStandard, otherwise they are the same. #Means under the same column with significant higher intended effect than standard fraction Table 2:- Shows the effects of different concentrations of Pennisetum purpureum fractions on the number of pupae that emerged in D. melanogaster. The toxicant group (H2O2) conferred significant decrease (lethal effect), on the number of pupae that emerged across all the concentrations in Drosophila melanogaster. There was a significant decrease in lethal activity on groups supplemented with the various concentrations of the extracts and fractions of Pennisetum purpureum. At LC6.25 Methanol extract had the highest number of pupae that emerged compared to all other crude and fractions of Pennisetum purpureum. At LC12.5, Methanol extract also had the highest number of pupae that emerged compared to all other extracts and fractions of Pennisetum purpureum, here, the effects of Methanol extract was similar to the Standard drug (Vitamin C). At LC25 and LC50, Methanol extract also had the highest number of pupae that emerged compared to all other crude and fractions of Pennisetum purpureum, with effects that were also significantly higher than the Standard drug (Vitamin C).

Table 3: The effects of various concentration of P. purpureum extracts and fractions on the number of adults that emerged in Drosophila melanogaster.

Fractions	LC_6.25	LC_12.5	LC₂₅	LC₅₀
Ethyl acetate	35.33±1.20^h	29.33±1.45^h	25.00±1.16^h	22.67±1.45^h
n-Hexane	62.00±1.53^g	47.67±0.67^g	43.00±1.15^g	36.00±1.73^g
Methanol	52.00±2.08^f	42.67±1.45^f	35.00±1.16^f	27.00±1.16^f
Aqueous	55.33±1.45^e	47.00±1.16^e	41.33±0.88^e	37.67±0.88^e
Methanol	69.00±2.31^d	56.33±1.45^d	48.33±0.67^d	40.67±1.20^d
Standard	75.67±2.03	65.67±2.03	59.00±1.16	46.67±0.88
H₂O₂	15.00±0.88	15.00±1.16	15.00±0.33	15.00±1.20
Control	83.67±1.45	83.67±1.45	83.67±1.45	83.67±1.45
F	157.993	227.546	422.770	304.849
p-value	0.001	0.001	0.001	0.001

DISCUSSION

Plants extracts could have a positive, negative or both negative and positive effects on fecundity at diverse concentrations in Drosophila melanogaster, for instance, Neem (Azadirachta indica) and Turmeric (Curcuma longa), had a negative impact on the fecundity of Drosophila melanogaster by reducing the number of eggs laid as well as eggs hatchability ^{19 , 20}. Grapes (Vitis vinifera) seed extract on the other hand has been shown to have a positive effect on fecundity in Drosophila melanogaster. Supplementation with grape seed extract could increase the number of eggs laid by female flies thereby increasing the viability of the offspring ²¹. Other studies revealed inconsistent outcome of both positive, negative and joint effect of the extract on fecundity, so depending on the specific plants and concentrations used, plant extracts usually have inconsistent effect on fecundity ²². Considering the effect of the plant on the 3^rd instar larva stage, the present study revealed that there was a significant increase in the number of 3^rd instar larva in flies supplemented with extracts and fractions compared to the toxicant group. Exposure of the 3^rd instar larva to the toxicant resulted to a significant decrease in its number, which was probably because of the oxidative stress induced by H₂O₂on the 3^rd instar larva leading to developmental delays and impaired growth ²³. Oxidative stress could result to changes in the expression of genes involved in antioxidant defence, stress response and developmental processes ²⁴. Studies have further shown that prolonged exposure to H₂O₂, during the 3^rd instar larva stage could have a long lasting effects through lifespan and decreased fitness in adult flies ²⁵. For the pupation and adult emergence stage, H₂O₂exposure in Drosophila melanogaster also resulted to decreased pupation and occlusion adult (emergence) rate which is likely due to the detrimental effect of oxidative stress on the flies’ developmental processes ²⁶. The crude and fractions of the plant on the other hand, was able to ameliorate the negative impact of the toxicant by significantly increasing the number of pupae and emerged adult flies. The positive effect of the plant extract on fecundity, may be due to the presence of alkaloids, steroids, phenols and flavonoids which could interrelate with the endocrine system of insects influencing the production and regulation of hormones involved in reproduction ²⁷. Phenols and flavonoids have been found to improve the antioxidant capacity and detoxification enzyme in the reproductive system in flies leading to increased egg production ²⁸, while steroids could enhance egg production and larval development thereby significantly increasing the fecundity in Drosophila melanogaster ²⁷. Studies by Damilola et al., Grover et al., & Rand et al., ^{29 - 31} also indicated that these secondary metabolites significantly mitigated the negative effects of hydrogen peroxide, leading to improved survival rates and increased numbers of larvae and emerged adults compared to untreated controls. However further research is required to uncover additional mechanisms and specific phytochemical compounds responsible for these effects. The standard drug, ascorbic acid is well-known for its high efficiency in reducing oxidative stress and enhancing developmental outcomes in the presence of hydrogen peroxide ^{29, 31}. Research centring on the antioxidant properties of specific plant extracts demonstrated that the presence of phytochemicals like phenols and flavonoids in these extracts could effectively scavenge free radicals produced by hydrogen peroxide. This scavenging activity was linked to improved developmental metrics, including increased larval survival and higher rates of pupation and adult emergence, suggesting a protective role against oxidative damage ²⁹. However further research is required to uncover additional mechanisms and specific phytochemical compounds responsible for these effects.

ACKNOWLEDGEMENTS

Prof. K. D., Falang, Prof. B. B., Bukar and Prof. N. N, Wannang for their academic mentoring, Satkat Zaccheus, for the technical assistance and Triumph Business Centre, typing assistant.

CONCLUSION

The present study demonstrated that the extracts and fractions of Pennisetum purpureum, exerted a protective effect on the reproductive ability of Drosophila melanogaster exposed to oxidative stress condition. The observed effect may be due to its capacity to effectively scavenge free radicals generated by hydrogen peroxide. However further research is required to divulge additional mechanisms and particular phytochemical compounds responsible for this effect.

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Reference

Allen R. G., & Tresini, M. (2000). Oxidative stress and gene regulation. Free Radical Biology and Medicine. 28(3), 463-499
Droge, W. (2002), Free radicals in the physiological control of cell function. Physiological Reviews, 82(1), 47-95.
Carraro, E., Schilirò, T., Biorci, F., Romanazzi, V., Degan, R. Buonocore D.…& Giogio Gilli. (2018). Physical activity, lifestyle factors and oxidative stress in middle age healthy subjects. International Journal of Environmental Research and Public Health, 15(6), 1152.
Manokaran, K., Bhat, P., Nayak, D., Baskaran, R., Paramasivam, P., Ahmed, S. F…, Balaji, V. 2022). Oxidative stress and female reproductive disorder: A review. Asian Pacific Journal of Reproduction 11(3), 107-116.
Agarwal, A., Gupta, S., & Sharma, R. (2005a). Oxidative stress and its implications in female infertility: A clinician's perspective. Reproductive Biomedicine Online, 11(5), 641-650.
Agarwal, A., Gupta, S., & Sharma, R. K. (2005b). Role of oxidative stress in female reproduction. Reproductive Biology and Endocrinology, 3, 28.
Geva, E., & Jaffe, R. B. (2000). Role of angiopoietins in reproductive tract angiogenesis. Obstetrical and Gynaecological Survey, 55(8), 511-519.
Walke, G., Gaurkar, S. S., Prasad, R., Lohakare, T., & Wanjari, M. (2023). The impact of oxidative stress on male reproductive function: Exploring the role of antioxidant supplementation. Cureus, 15(7), 42583. https://doi.org.e42583.10.7759/cureus.42583.
Mannucci, A., Argento, F. R., Fini, E., Coccia, M. E., Taddei, N., Becatti, M., & Fiorillo, C. (2021). The impact of oxidative stress in male infertility. Frontiers in Molecular Biosciences, 8:799294. 10.3389/fmolb.2021.799294.
Aitken, R. J., Drevet, J. R., Moazamian, A., & Gharagozloo, P. (2022). Male infertility and oxidative stress: a focus on the underlying mechanisms. Antioxidants (Basel), https://11:10.3390/antiox11020306.
Allen R. G., & Tresini, M. (2000). Oxidative stress and gene regulation. Free Radical Biology and Medicine. 28(3), 463-499
Hosen, M.B., Islam, M.R., Begum, F., Kabir, Y. & Howlader, M.Z. (2015). Oxidative stress induced sperm DNA damage, a possible reason for male infertility. Iranian Journal of Reproductive Medicine, 13, 525-32. https://doi.org/sujiminn.blogspot.com/?book-1570620806.
Bansal, A. K., & Bilaspuri, G.S. (2010). Impacts of oxidative stress and antioxidants on semen functions. Veterinary Medicine International, 10.4061/2011/686137.
Adedara, I. A., Abolaji, A. O., Rocha, J.B.T. and Farombi, E. O. (2016). Diphenyl diselenide protects against mortality, locomotor deficits and oxidative stress in Drosophila melanogaster. Induced neurotoxicity. Neurochemical Research Journal 41(6): 1430-1438. https://doi.org/10.1007/s11064-016-1852
Iorjiim, W. M., Omale, S., Bagu, G. D., Gyang, S. S., and Alemika, E. T. (2020). Reproductive and Oxidative Stress Toxicity of Dolutegravir based combination antiretroviral therapy in Drosophila melanogaster. Journal of Advanced Medical and Pharmaceutical Sciences. 22(6): 26-40. https://doi:10.9734/jamps/2020/v22i630177
Kumar, A. & Pande V. (2022). “Oxidative stress and its role in reproductive physiology of drosophila”. Journal of Insect Physiology, 120, 104-115. https://doi.org/10.1016/j.jinphys.2022.104115.
Huang, Y., & Wang, J. (2020). “Hydrogen Peroxide Induced Oxidative Stress in Drosophila melanogaster. Biological Open, 9(10). https://doi.org.10.1002/0471140856.tx0112s59
Liu, Y. & Zhang, J. (2019). “Effects of Environmental Stressors on Fecundity in Drosophila”. Frontiers in Physiology, 10, 1234. https://doi.org/10.3389/fphys.2019.01234.
Nathan, S. S., Kalaivani, K. & Morugan, K. (2005). Effects of Neem limonoids on the Malaria vector Anopheles Stephens Liston (Diptera culicidae) Acta tropica, 96(1), 47-55.
Siddiq, A. R., Rafiu, A., Naz, F. & Mashhi, R. (2011). Effect of Curcuma longa on Mortality and Fecundity of Bactrocera zanata (Diptera: Tephritidae). Ciencia e Agrotechnologia, Larvas, 35(6), 1110-1114.
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Izam Y. Y.

Corresponding author

Department of Pharmacology and Toxicology, Faculty of Pharmaceutical Sciences, University of Jos, Nigeria.

Amagon K.

Co-author

Department of Pharmacology and Toxicology, Faculty of Pharmaceutical Sciences, University of Jos, Nigeria.

Sabo S. Y.

Co-author

Department of Pharmacology and Toxicology, Faculty of Pharmaceutical Sciences, University of Jos, Nigeria.

Izam Y. Y.*, Amagon K., Sabo S. Y., Pennisetum Purpureum (Elephant grass) Protects Against Hydrogen Peroxide Induced Reproductive Toxicity in Drosophila Melanogaster, Int. J. of Pharm. Sci., 2025, Vol 3, Issue 3, 1783-1790. https://doi.org/10.5281/zenodo.15049032

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Pennisetum Purpureum (Elephant grass) Protects Against Hydrogen Peroxide Induced Reproductive Toxicity in Drosophila Melanogaster

Abstract

Keywords

Introduction

Reference

Izam Y. Y.

Amagon K.

Sabo S. Y.

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