CLC number: R931
On-line Access: 2024-08-27
Received: 2023-10-17
Revision Accepted: 2024-05-08
Crosschecked: 2018-11-21
Cited: 0
Clicked: 4407
Citations: Bibtex RefMan EndNote GB/T7714
Supatcharee Arun, Jaturon Burawat, Supataechasit Yannasithinon, Wannisa Sukhorum, Akgpol Limpongsa, Sitthichai Iamsaard. Phyllanthus emblica leaf extract ameliorates testicular damage in rats with chronic stress[J]. Journal of Zhejiang University Science B, 2018, 19(12): 948-959.
@article{title="Phyllanthus emblica leaf extract ameliorates testicular damage in rats with chronic stress",
author="Supatcharee Arun, Jaturon Burawat, Supataechasit Yannasithinon, Wannisa Sukhorum, Akgpol Limpongsa, Sitthichai Iamsaard",
journal="Journal of Zhejiang University Science B",
volume="19",
number="12",
pages="948-959",
year="2018",
publisher="Zhejiang University Press & Springer",
doi="10.1631/jzus.B1800362"
}
%0 Journal Article
%T Phyllanthus emblica leaf extract ameliorates testicular damage in rats with chronic stress
%A Supatcharee Arun
%A Jaturon Burawat
%A Supataechasit Yannasithinon
%A Wannisa Sukhorum
%A Akgpol Limpongsa
%A Sitthichai Iamsaard
%J Journal of Zhejiang University SCIENCE B
%V 19
%N 12
%P 948-959
%@ 1673-1581
%D 2018
%I Zhejiang University Press & Springer
%DOI 10.1631/jzus.B1800362
TY - JOUR
T1 - Phyllanthus emblica leaf extract ameliorates testicular damage in rats with chronic stress
A1 - Supatcharee Arun
A1 - Jaturon Burawat
A1 - Supataechasit Yannasithinon
A1 - Wannisa Sukhorum
A1 - Akgpol Limpongsa
A1 - Sitthichai Iamsaard
J0 - Journal of Zhejiang University Science B
VL - 19
IS - 12
SP - 948
EP - 959
%@ 1673-1581
Y1 - 2018
PB - Zhejiang University Press & Springer
ER -
DOI - 10.1631/jzus.B1800362
Abstract: Stress affects the male reproductive system and can cause sub-fertility or infertility. Although Phyllanthus emblica L. (PE) extract has been shown to have high antioxidant capacity and protective properties in damaged tissue, the preventive effects of PE extract on testicular function from stress-related impairment have never been demonstrated. This study aimed to investigate the effects of PE aqueous leaf extract on testicular impairment and protein marker changes in rats suffering from chronic stress. Adult male rats were divided into four groups: a control group, a chronic stress (CS) group, and two groups with CS that received different doses of PE extract (50 or 100 mg/kg body weight (BW)). In the treatment groups, the animals were given PE extract daily before stress induction for 42 consecutive days. Stress was induced through immobilization (4 h/d) followed by forced cold swimming (15 min/d). Sperm quality and the histology of the testes and caudal epididymis were examined, as were levels of serum corticosterone, testosterone, and malondialdehyde (MDA). The expressions of testicular steroidogenic acute regulatory (StAR) and tyrosine-phosphorylated proteins were investigated using immuno-Western blot analysis, as these proteins are assumed to play important roles in spermatogenesis and androgen synthesis. The results showed that PE (50 mg/kg BW) significantly increased sperm concentration and testosterone levels, while decreasing corticosterone levels, MDA levels, sperm head abnormalities, and acrosome-reacted sperm in CS rats. In addition, PE at both doses was found to diminish testicular histopathology in the CS rats. We also found that 50 mg/kg BW of PE significantly improved StAR protein expression and altered the intensities of some tyrosine-phosphorylated proteins in testis. We conclude that PE leaf extract at 50 mg/kg BW can prevent testicular damage in rats with CS.
[1]Akinpelu BA, Oyedapo OO, Iwalewa EO, et al., 2012. Biochemical and histopathological profile of toxicity induced by saponin fraction of Erythrophleum suaveolens (Guill. & Perri.) bark extract. Phytopharmacology, 3(1):38-53.
[2]Al-Shafi SM, 2002. Toxic effect of tannic and related compounds on human plasma proteins. Saudi Med J, 23(2):221-225.
[3]Arad-Dann H, Beller U, Haimovitch R, et al., 1993. Immunohistochemistry of phosphotyrosine residues: identification of distinct intracellular patterns in epithelial and steroidogenic tissues. J Histochem Cytochem, 41(4):513-519.
[4]Arun S, Burawat J, Sukhorum W, et al., 2016a. Changes of testicular phosphorylated proteins in response to restraint stress in male rats. J Zhejiang Univ-Sci B (Biomed & Biotechnol), 17(1):21-29.
[5]Arun S, Burawat J, Sukhorum W, et al., 2016b. Chronic restraint stress induces sperm acrosome reaction and changes in testicular tyrosine phosphorylated proteins in rats. Int J Reprod Biomed (Yazd), 14(7):443-452.
[6]Aziz NM, Ragy MM, Gayyed MF, 2013. Effect of acute immobilization stress with or without a heme oxygenase inducer on testicular structure and function in male albino rats. J Basic Clin Physiol Pharmacol, 24(4):255-462.
[7]Bandyopadhyay SK, Pakrashi SC, Pakrashi A, 2000. The role of antioxidant activity of Phyllanthus emblica fruits on prevention from indomethacin induced gastric ulcer. J Ethnopharmacol, 70(2):171-176.
[8]Bhatia N, Jaggi AS, Singh N, et al., 2011. Adaptogenic potential of curcumin in experimental chronic stress and chronic unpredictable stress-induced memory deficits and alterations in functional homeostasis. J Nat Med, 65(3-4):532-543.
[9]Bitgul G, Tekmen I, Keles D, et al., 2013. Protective effects of resveratrol against chronic immobilization stress on testis. ISRN Urol, 2013:278720.
[10]Calixto JB, Santos ARS, Filho CV, et al., 1998. A review of the plants of the genus Phyllanthus: their chemistry, pharmacology, and therapeutic potential. Med Res Rev, 18(4):225-258.
[11]Chaichun A, Arun S, Burawat J, et al., 2017. Localization and identification of tyrosine phosphorylated proteins in adult sprague-dawley rat testis. Int J Morphol, 35(4):1322-1327.
[12]Chaphalkar R, Apte KG, Talekar Y, et al., 2017. Antioxidants of Phyllanthus emblica L. Bark extract provide hepatoprotection against ethanol-induced hepatic damage: a comparison with silymarin. Oxid Med Cell Longev, 2017: 3876040.
[13]Dhanabalan S, Jubendradass R, Latha P, et al., 2010. Effect of restraint stress on 2,3,7,8 tetrachloro dibenzo-p-dioxin induced testicular and epididymal toxicity in rats. Hum Exp Toxicol, 30(7):567-578.
[14]Everds NE, Snyder PW, Bailey KL, et al., 2013. Interpreting stress responses during routine toxicity studies: a review of the biology, impact, and assessment. Toxicol Pathol, 41(4):560-614.
[15]Hanks SK, Quinn AM, Hunter T, 1988. The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science, 241(4861):42-52.
[16]Huang CZ, Tung YT, Hsia SM, et al., 2017. The hepatoprotective effect of Phyllanthus emblica L. fruit on high fat diet-induced non-alcoholic fatty liver disease (NAFLD) in SD rats. Food Funct, 8(2):842-850.
[17]Hunter T, Cooper JA, 1985. Protein-tyrosine kinases. Annu Rev Biochem, 54(1):897-930.
[18]Iamsaard S, Prabsattroo T, Sukhorum W, et al., 2013. Anethum graveolens Linn. (dill) extract enhances the mounting frequency and level of testicular tyrosine protein phosphorylation in rats. J Zhejiang Univ-Sci B (Biomed & Biotechnol), 14(3):247-252.
[19]Iamsaard S, Arun S, Burawat J, et al., 2014. Phenolic contents and antioxidant capacities of Thai-Makham Pom (Phyllanthus emblica L.) aqueous extracts. J Zhejiang Univ-Sci B (Biomed & Biotechnol), 15(4):405-408.
[20]Iamsaard S, Arun S, Burawat J, et al., 2015. Phyllanthus emblica L. branch extract ameliorates testicular damage in valproic acid-Induced rats. Int J Morphol, 33(3):1016-1022.
[21]Iamsaard S, Welbat JU, Sukhorum W, et al., 2018. Methotrexate changes the testicular tyrosine phosphorylated protein expression and seminal vesicle epithelia of adult rats. Int J Morphol, 36(2):737-742.
[22]İzgüt-Uysal VN, Gemici B, Birsen İ, et al., 2014. The protective effect of apelin against water-immersion and restraint stress-induced gastric damage. J Physiol Sci, 64(4):279-289.
[23]Khandelwal S, Shukla LJ, Shanker R, 2002. Modulation of acute cadmium toxicity by emblica officinalis fruit in rat. Indian J Exp Biol, 40(5):564-570.
[24]Krishnaveni M, Mirunalini S, 2012. Chemopreventive efficacy of Phyllanthus emblica L. (amla) fruit extract on 7,12-dimethylbenz(a)anthracene induced oral carcinogenesis— a dose-response study. Environ Toxicol Pharmacol, 34(3):801-810.
[25]Kumnerdkhonkaen P, Saenglee S, Asgar MA, et al., 2018. Antiproliferative activities and phenolic acid content of water and ethanolic extracts of the powdered formula of Houttuynia cordata Thunb. Fermented broth and Phyllanthus emblica Linn. Fruit. BMC Complement Altern Med, 18:130.
[26]Lee SH, Choi KH, Cha KM, et al., 2017. Protective effects of Korean Red Ginseng against sub-acute immobilization stress-induced testicular damage in experimental rats. J Ginseng Res, in press.
[27]Lin H, Yuan KM, Zhou HY, et al., 2014. Time-course changes of steroidogenic gene expression and steroidogenesis of rat Leydig cells after acute immobilization stress. Int J Mol Sci, 15(11):21028-21044.
[28]Liu XL, Cui C, Zhao MM, et al., 2008. Identification of phenolics in the fruit of emblica (Phyllanthus emblica L.) and their antioxidant activities. Food Chem, 109(4):909-915.
[29]Lu CC, Yang SH, Hsia SM, et al., 2016. Inhibitory effects of Phyllanthus emblica L. on hepatic steatosis and liver fibrosis in vitro. J Funct Foods, 20:20-30.
[30]Luo W, Zhao MM, Yang B, et al., 2011. Antioxidant and antiproliferative capacities of phenolics purified from Phyllanthus emblica L. fruit. Food Chem, 126(1):277-282.
[31]Maneenin C, Burawat J, Maneenin N, et al., 2018. Antioxidant capacity of Momordica charantia extract and its protective effect on testicular damage in valproic acid-induced rats. Int J Morphol, 36(2):447-453.
[32]Matsuura N, Nagasawa K, Minagawa Y, et al., 2015. Restraint stress exacerbates cardiac and adipose tissue pathology via β-adrenergic signaling in rats with metabolic syndrome. Am J Physiol Heart Circ Physiol, 308(10):H1275-H1286.
[33]Naninck EFG, Hoeijmakers L, Kakava-Georgiadou N, et al., 2015. Chronic early life stress alters developmental and adult neurogenesis and impairs cognitive function in mice. Hippocampus, 25(3):309-328.
[34]Pertsov SS, Koplik EV, Kalinichenko LS, 2015. Effect of interleukin-4 on peripheral blood leukocytes in rats with various behavioral characteristics during acute stress. Bull Exp Biol Med, 158(5):595-599.
[35]Podolak I, Galanty A, Sobolewska D, 2010. Saponins as cytotoxic agents: a review. Phytochem Rev, 9(3):425-474.
[36]Popović N, Pajović SB, 2010. Lithium modulates the chronic stress-induced effect on blood glucose level of male rats. Arch Biol Sci, 62(2):289-295.
[37]Prabsattroo T, Wattanathorn J, Iamsaard S, et al., 2015. Moringa oleifera extract enhances sexual performance in stressed rats. J Zhejiang Univ-Sci B (Biomed & Biotechnol), 16(3):179-190.
[38]Pramyothin P, Samosorn P, Poungshompoo S, et al., 2006. The protective effects of Phyllanthus emblica Linn. extract on ethanol induced rat hepatic injury. J Ethnopharmacol, 107(3):361-364.
[39]Priya PH, Reddy PS, 2012. Effect of restraint stress on lead-induced male reproductive toxicity in rats. J Exp Zool A Ecol Genet Physiol, 317(7):455-465.
[40]Rai J, Pandey SN, Srivastava RK, 2003. Effect of immobilization stress on spermatogenesis of albino rats. J Anat Soc India, 52(1):55-57.
[41]Rai J, Pandey SN, Srivastava RK, 2004. Testosterone hormone level in albino rats following restraint stress of long duration. J Anat Soc India, 53(1):17-19.
[42]Rao M, Zhao XL, Yang J, et al., 2015. Effect of transient scrotal hyperthermia on sperm parameters, seminal plasma biochemical markers, and oxidative stress in men. Asian J Androl, 17(4):668-675.
[43]Reis DG, Scopinho AA, Guimarães FS, 2011. Behavioral and autonomic responses to acute restraint stress are segregated within the lateral septal area of rats. PLoS ONE, 6(8):e23171.
[44]Retana-Márquez S, Bonilla-Jaime H, Vázquez-Palacios G, et al., 2003. Changes in masculine sexual behavior, corticosterone and testosterone in response to acute and chronic stress in male rats. Horm Behav, 44(4):327-337.
[45]Richburg JH, 2000. The relevance of spontaneous- and chemically-induced alterations in testicular germ cell apoptosis to toxicology. Toxicol Lett, 112-113:79-86.
[46]Saha S, Verma RJ, 2015. Antioxidant activity of polyphenolic extract of Phyllanthus emblica against lead acetate induced oxidative stress. Toxicol Environ Health Sci, 7(1):82-90.
[47]Sakr SA, Zowail ME, Marzouk AM, 2014. Effect of saffron (Crocus sativus L.) on sodium valporate induced cytogenetic and testicular alterations in albino rats. Anat Cell Biol, 47(3):171-179.
[48]Sampannang A, Arun S, Sukhorum W, et al., 2017. Antioxidant and hypoglycemic effects of Momordica cochinchinensis Spreng. (Gac) aril extract on reproductive damages in streptozotocin (STZ)-induced hyperglycemia mice. Int J Morphol, 35(2):667-675.
[49]Sawant L, Pandita N, Prabhakar B, 2010. Determination of gallic acid in Phyllanthus emblica Linn. Dried fruit powder by HPTLC. J Pharm Bioallied Sci, 2(2):105-108.
[50]She GM, Cheng RY, Sha L, et al., 2013. A novel phenolic compound from Phyllanthus emblica. Nat Prod Commun, 8(4):461-462.
[51]Srinivasan P, Vijayakumar S, Kothandaraman S, et al., 2018. Anti-diabetic activity of quercetin extracted from Phyllanthus emblica L. fruit: in silico and in vivo approaches. J Pharm Anal, 8(2):109-118.
[52]Sripanidkulchai B, Junlatat J, 2014. Bioactivities of alcohol based extracts of Phyllanthus emblica branches: antioxidation, antimelanogenesis and anti-inflammation. J Nat Med, 68(3):615-622.
[53]Sukhorum W, Iamsaard S, 2017. Changes in testicular function proteins and sperm acrosome status in rats treated with valproic acid. Reprod Fertil Dev, 29(8):1585-1592.
[54]Tahir I, Khan MR, Shah NA, et al., 2016. Evaluation of phytochemicals, antioxidant activity and amelioration of pulmonary fibrosis with Phyllanthus emblica leaves. BMC Complement Altern Med, 16:406.
[55]Tasanarong A, Kongkham S, Itharat A, 2014. Antioxidant effect of Phyllanthus emblica extract prevents contrast-induced acute kidney injury. BMC Complement Altern Med, 14:138.
[56]Toyang NJ, Ateh EN, Keiser J, et al., 2012. Toxicity, antimicrobial and anthelmintic activities of Vernonia guineensis Benth. (Asteraceae) crude extracts. J Ethnopharmacol, 144(3):700-704.
[57]Ullrich A, Schlessinger J, 1990. Signal transduction by receptors with tyrosine kinase activity. Cell, 61(2):203-212.
[58]Verma R, Chakraborty D, 2008. Emblica officinalis aqueous extract ameliorates ochratoxin-induced lipid peroxidation in the testis of mice. Acta Pol Pharm, 65(2):187-194.
[59]Visconti PE, Kopf GS, 1998. Regulation of protein phosphorylation during sperm capacitation. Biol Reprod, 59(1):1-6.
[60]Xu ML, Wei QW, Zheng KZ, et al., 2014. Protective effects of Big-leaf mulberry and physiological roles of nitric oxide synthases in the testis of mice following water immersion and restraint stress. Acta Histochem, 116(8):1323-1330.
[61]Yanagimachi R, 1994. Mammalian fertilization. In: Knobil E (Ed.), The Physiology of Reproduction. Raven Press, New York, p.189-317.
[62]Zhang MH, Shi ZD, Yu JC, et al., 2015. Scrotal heat stress causes sperm chromatin damage and cysteinyl aspartate-spicific proteinases 3 changes in fertile men. J Assist Reprod Genet, 32(5):747-755.
[63]Zhao TJ, Sun Q, Marques M, et al., 2015. Anticancer properties of Phyllanthus emblica (Indian Gooseberry). Oxid Med Cell Longev, 2015:950890.
[64]Zhong ZG, Wu DP, Huang JL, et al., 2011. Progallin A isolated from the acetic ether part of the leaves of Phyllanthus emblica L. induces apoptosis of human hepatocellular carcinoma BEL-7404 cells by up-regulation of Bax expression and down-regulation of Bcl-2 expression. J Ethnopharmacol, 133(2):765-772.
Open peer comments: Debate/Discuss/Question/Opinion
<1>