Curcumin-Loaded Iron Particle Improvement of Spermatogenesis in Azoospermic Mouse Induced by Long-Term Scrotal Hyperthermia.
Adaptor Proteins, Signal Transducing
/ genetics
Animals
Azoospermia
/ blood
Biomarkers
/ blood
Curcumin
/ chemistry
Disease Models, Animal
Drug Carriers
Drug Compounding
Fertility Agents, Male
/ chemistry
Hyperthermia, Induced
Magnetic Iron Oxide Nanoparticles
/ chemistry
Male
Mice
Proliferating Cell Nuclear Antigen
/ genetics
Proto-Oncogene Proteins c-kit
/ genetics
Spermatogenesis
/ drug effects
Spermatozoa
/ drug effects
Testis
/ drug effects
Testosterone
/ blood
Time Factors
Curcumin-loaded iron particles
Long-term scrotal hyperthermia
Spermatogenesis
Journal
Reproductive sciences (Thousand Oaks, Calif.)
ISSN: 1933-7205
Titre abrégé: Reprod Sci
Pays: United States
ID NLM: 101291249
Informations de publication
Date de publication:
02 2021
02 2021
Historique:
received:
05
05
2020
accepted:
02
08
2020
pubmed:
12
8
2020
medline:
24
11
2021
entrez:
12
8
2020
Statut:
ppublish
Résumé
Spermatogenesis process is sensitive to heat stress because the testicular temperature is 2 to 4 °C lower than the core body temperature. The current study aimed to investigate the effects of iron oxide nanoparticles containing curcumin on spermatogenesis in mice induced by long-term scrotal hyperthermia. In this experimental study, 18 mice were equally divided into the following three groups: control, scrotal hyperthermia, and scrotal hyperthermia + curcumin-loaded iron particles (NPs) (240 μL) (mice were treated for 20 days). Hyperthermia was induced by exposure to the temperature of 43 °C for 20 min every other day for 5 weeks. Afterward, the animals were euthanized; sperm samples were collected for sperm parameters analysis, and testis samples were taken for histopathology experiments, evaluation of serum testosterone level, and RNA extraction in order to examine the expression of c-kit, STRA8 and PCNA genes. Our study showed that curcumin-loaded iron particles could notably increase the volume of testis, length of seminiferous tubules, sperm parameters, and stereological parameters (i.e., spermatogonia, primary spermatocyte, round spermatid, and Leydig cells) thereby increasing serum testosterone level; in addition, TUNEL-positive cells showed a significant decrease in curcumin-loaded iron particle group. Thus, based on the obtained results, the expression of c-kit, STRA8, and PCNA genes was significantly increased in treatment groups by curcumin-loaded iron particles compared with scrotal hyperthermia-induced mice. In conclusion, curcumin-loaded iron particles can be considered an alternative treatment for improving the spermatogenesis process in scrotal hyperthermia-induced mice.
Identifiants
pubmed: 32780358
doi: 10.1007/s43032-020-00288-2
pii: 10.1007/s43032-020-00288-2
doi:
Substances chimiques
Adaptor Proteins, Signal Transducing
0
Biomarkers
0
Drug Carriers
0
Fertility Agents, Male
0
Proliferating Cell Nuclear Antigen
0
Stra8 protein, mouse
0
Testosterone
3XMK78S47O
Proto-Oncogene Proteins c-kit
EC 2.7.10.1
Curcumin
IT942ZTH98
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
371-380Références
Bonde JP. Male reproductive organs are at risk from environmental hazards. Asian J Androl. 2010;12(2):152–6.
doi: 10.1038/aja.2009.83
Ivell R. Lifestyle impact and the biology of the human scrotum. Reprod Biol Endocrinol. 2007;5(1):15.
doi: 10.1186/1477-7827-5-15
Zhu B, Walker SK, Oakey H, Setchell BP, Maddocks S. Effect of paternal heat stress on the development in vitro of preimplantation embryos in the mouse. Andrologia. 2004;36(6):384–94.
doi: 10.1111/j.1439-0272.2004.00635.x
Khorsandi L, Mirhoseini M, Mohamadpour M, Orazizadeh M, Khaghani S. Effect of curcumin on dexamethasone-induced testicular toxicity in mice. Pharm Biol. 2013;51(2):206–12.
doi: 10.3109/13880209.2012.716854
Ahmed-Farid OA, et al. Beneficial effects of curcumin nano-emulsion on spermatogenesis and reproductive performance in male rats under protein deficient diet model: enhancement of sperm motility, conservancy of testicular tissue integrity, cell energy and seminal plasma amino acids content. J Biomed Sci. 2017;24(1):66.
doi: 10.1186/s12929-017-0373-5
Cherukuvada S, Nangia A. Fast dissolving eutectic compositions of two anti-tubercular drugs. CrystEngComm. 2012;14(7):2579–88.
doi: 10.1039/c2ce06391c
Gao Y, Li Z, Sun M, Guo C, Yu A, Xi Y, et al. Preparation and characterization of intravenously injectable curcumin nanosuspension. Drug Deliv. 2011;18(2):131–42.
doi: 10.3109/10717544.2010.520353
Jahed V, Zarrabi A, Bordbar AK, Hafezi MS. NMR (1H, ROESY) spectroscopic and molecular modelling investigations of supramolecular complex of β-cyclodextrin and curcumin. Food Chem. 2014;165:241–6.
doi: 10.1016/j.foodchem.2014.05.094
Babaei E, Sadeghizadeh M, Hassan ZM, Feizi MAH, Najafi F, Hashemi SM. Dendrosomal curcumin significantly suppresses cancer cell proliferation in vitro and in vivo. Int Immunopharmacol. 2012;12(1):226–34.
doi: 10.1016/j.intimp.2011.11.015
Reddy LH, Arias JL, Nicolas J, Couvreur P. Magnetic nanoparticles: design and characterization, toxicity and biocompatibility, pharmaceutical and biomedical applications. Chem Rev. 2012;112(11):5818–78.
doi: 10.1021/cr300068p
Heydari Sheikh Hossein H, Zarrabi A, Zarepour A. Design and construction of curcumin–loaded targeted iron oxide nanoparticles for cancer treatment. J Babol Univ Med Sci. 2017;19(6):64–70.
Ziaeipour S, Rezaei F, Piryaei A, Abdi S, Moradi A, Ghasemi A, et al. Hyperthermia versus busulfan: finding the effective method in animal model of azoospermia induction. Andrologia. 2019;51(11):e13438.
doi: 10.1111/and.13438
Kim B, Park K, Rhee K. Heat stress response of male germ cells. Cell Mol Life Sci. 2013;70(15):2623–36.
doi: 10.1007/s00018-012-1165-4
Aitken RJ, Roman SD. Antioxidant systems and oxidative stress in the testes. Oxidative Med Cell Longev. 2008;1(1):15–24.
doi: 10.4161/oxim.1.1.6843
Fujisawa M, Hayashi A, Okada H, Arakawa S, Kamidono S. Enzymes involved in DNA synthesis in the testes are regulated by temperature in vitro. Eur Urol. 1997;31:237–42.
doi: 10.1159/000474457
Mahmoudi M, Hosseinkhani H, Hosseinkhani M, Boutry S, Simchi A, Journeay WS, et al. Magnetic resonance imaging tracking of stem cells in vivo using iron oxide nanoparticles as a tool for the advancement of clinical regenerative medicine. Chem Rev. 2011;111(2):253–80.
doi: 10.1021/cr1001832
Lodhia J, et al. Development and use of iron oxide nanoparticles (part 1): synthesis of iron oxide nanoparticles for magnetic resonance imaging [MRI]. Biomed Imaging Interv J. 2010;6(2):1–11.
doi: 10.2349/biij.6.2.e12
Vickers NJ. Animal communication: when I’m calling you, will you answer too? Curr Biol. 2017;27(14):R713–5.
doi: 10.1016/j.cub.2017.05.064
Panahi S, Karamian A, Sajadi E, Aliaghaei A, Nazarian H, Abdi S, et al. Sertoli cell–conditioned medium restores spermatogenesis in azoospermic mouse testis. Cell Tissue Res. 2020;379(3):577–87.
doi: 10.1007/s00441-019-03092-w
Ziaeipour S, Ahrabi B, Naserzadeh P, Aliaghaei A, Sajadi E, Abbaszadeh HA, et al. Effects of Sertoli cell transplantation on spermatogenesis in azoospermic mice. Cell Physiol Biochem. 2019;52:421–34.
doi: 10.33594/000000030
Reed M, Howard C, Yanés GSDE. One-stop stereology: the estimation of 3D parameters using isotropic rulers. J Microsc. 2010;239(1):54–65.
doi: 10.1111/j.1365-2818.2009.03356.x
Banks S, King SA, Irvine DS, Saunders PTK. Impact of a mild scrotal heat stress on DNA integrity in murine spermatozoa. Reproduction. 2005;129(4):505–14.
doi: 10.1530/rep.1.00531
Pérez-Crespo M, Pintado B, Gutiérrez-Adán A. Scrotal heat stress effects on sperm viability, sperm DNA integrity, and the offspring sex ratio in mice. Mol Reprod Dev. 2008;75(1):40–7.
doi: 10.1002/mrd.20759
Aggarwal BB, Harikumar KB. Potential therapeutic effects of curcumin, the anti-inflammatory agent, against neurodegenerative, cardiovascular, pulmonary, metabolic, autoimmune and neoplastic diseases. Int J Biochem Cell Biol. 2009;41(1):40–59.
doi: 10.1016/j.biocel.2008.06.010
Alsamydai A, Jaber N. Pharmacological aspects of curcumin: review article. Int J Pharmacogn. 2018;5:313–26.
Jovanovic SV, Boone CW, Steenken S, Trinoga M, Kaskey RB. How curcumin works preferentially with water soluble antioxidants. J Am Chem Soc. 2001;123(13):3064–8.
doi: 10.1021/ja003823x
LUE YH, et al. Mild testicular hyperthermia induces profound transitional spermatogenic suppression through increased germ cell apoptosis in adult cynomolgus monkeys (Macaca fascicularis). J Androl. 2002;23(6):799–805.
pubmed: 12399525
Lue Y, Wang C, Liu YX, Hikim APS, Zhang XS, Ng CM, et al. Transient testicular warming enhances the suppressive effect of testosterone on spermatogenesis in adult cynomolgus monkeys (Macaca fascicularis). J Clin Endocrinol Metab. 2006;91(2):539–45.
doi: 10.1210/jc.2005-1808
Wang C, Cui YG, Wang XH, Jia Y, Sinha Hikim A, Lue YH, et al. Transient scrotal hyperthermia and levonorgestrel enhance testosterone-induced spermatogenesis suppression in men through increased germ cell apoptosis. J Clin Endocrinol Metab. 2007;92(8):3292–304.
doi: 10.1210/jc.2007-0367
Garolla A, Torino M, Sartini B, Cosci I, Patassini C, Carraro U, et al. Seminal and molecular evidence that sauna exposure affects human spermatogenesis. Hum Reprod. 2013;28(4):877–85.
doi: 10.1093/humrep/det020
Lin C, Choi YS, Park SG, Gwon LW, Lee JG, Yon JM, et al. Enhanced protective effects of combined treatment with β-carotene and curcumin against hyperthermic spermatogenic disorders in mice. Biomed Res Int. 2016;2016:1–8.
Rashid K, Sil PC. Curcumin ameliorates testicular damage in diabetic rats by suppressing cellular stress-mediated mitochondria and endoplasmic reticulum-dependent apoptotic death. Biochim Biophys Acta. 2015;1852(1):70–82.
doi: 10.1016/j.bbadis.2014.11.007
Takhtfooladi MA, Asghari A, Takhtfooladi HA, Shabani S. The protective role of curcumin on testicular tissue after hindlimb ischemia reperfusion in rats. Int Urol Nephrol. 2015;47(10):1605–10.
doi: 10.1007/s11255-015-1101-2
Lonare M, Kumar M, Raut S, More A, Doltade S, Badgujar P, et al. Evaluation of ameliorative effect of curcumin on imidacloprid-induced male reproductive toxicity in wistar rats. Environ Toxicol. 2016;31(10):1250–63.
doi: 10.1002/tox.22132
Aktas C, Kanter M, Erboga M, Ozturk S. Anti-apoptotic effects of curcumin on cadmium-induced apoptosis in rat testes. Toxicol Ind Health. 2012;28(2):122–30.
doi: 10.1177/0748233711407242
Pino, J. Differential effects of temperature on reactive oxygen/nitrogen species production in rat pachytene spermatocytes and round spermatids. 2013.
Aktas C, Kanter M. A morphological study on Leydig cells of scrotal hyperthermia applied rats in short-term. J Mol Histol. 2009;40(1):31–9.
doi: 10.1007/s10735-009-9210-9
Choi Y-J, Ok DW, Kwon DN, Chung JI, Kim HC, Yeo SM, et al. Murine male germ cell apoptosis induced by busulfan treatment correlates with loss of c-kit-expression in a Fas/FasL-and p53-independent manner. FEBS Lett. 2004;575(1–3):41–51.
doi: 10.1016/j.febslet.2004.08.034
Esmaeilsani Z, et al. Effects of curcumin nanoparticles on the tissue oxidative stress following testicular torsion and detorsion in rat model. Iran J Vet Surg (IJVS). 2019;14(2):97–104.