Exploring the full potential of sperm function with nanotechnology tools
Serge Leugoué Kameni; Notsile Hleliwe Dlamini; Jean Magloire Feugang
Abstract
Keywords
References
Aalberts M, Stout TAE, Stoorvogel W. Prostasomes: extracellular vesicles from the prostate. Reproduction. 2014;147(1):R1-14.
Abedin F, Asmatulu E, Andalib MN. Nanomaterials and human health: an overview. In: Kumar V, Guleria P, Ranjan S, Dasgupta N, Lichtfouse E, editors. Nanotoxicology and nanoecotoxicology. Cham: Springer; 2021. p. 165-80.
Agnihotri SK, Agrawal AK, Hakim BA, Vishwakarma AL, Narender T, Sachan R, Sachdev M. Mitochondrial membrane potential (MMP) regulates sperm motility. In Vitro Cell Dev Biol Anim. 2016;52(9):953-60.
Aitken RJ, Baker MA. The role of proteomics in understanding sperm cell biology. Int J Androl. 2008;31(3):295-302.
Al-Bulushi S, Manjunatha BM, Bathgate R, Rickard JP, De Graaf SP. Liquid storage of dromedary camel semen in different extenders. Anim Reprod Sci. 2019;207:95-106.
Alpatov R, Lesch BJ, Nakamoto-Kinoshita M, Blanco A, Chen S, Stützer A, Armache KJ, Simon MD, Xu C, Ali M, Murn J, Prisic S, Kutateladze TG, Vakoc CR, Min J, Kingston RE, Fischle W, Warren ST, Page DC, Shi Y. A chromatin-dependent role of the fragile X mental retardation protein FMRP in the DNA damage response. Cell. 2014;157(4):869-81.
Alvarez-Rodriguez M, Martinez CA, Roca J, Rodriguez-Martinez H. mRNA expression of oxidative-reductive proteins in boars with documented different fertility can identify relevant prognostic biomarkers. Res Vet Sci. 2021;141:195-202.
Amann RP. The cycle of the seminiferous epithelium in humans: a need to revisit? J Androl. 2008;29(5):469-87.
Amidi F, Pazhohan A, Shabani Nashtaei M, Khodarahmian M, Nekoonam S. The role of antioxidants in sperm freezing: a review. Cell Tissue Bank. 2016;17(4):745-56.
Anjum S, Ishaque S, Fatima H, Farooq W, Hano C, Abbasi BH, Anjum I. Emerging applications of nanotechnology in healthcare systems: grand challenges and perspectives. Pharmaceuticals (Basel). 2021;14(8):707.
Ansari MS, Rakha BA, Akhter S, Ashiq M. OPTIXcell improves the postthaw quality and fertility of buffalo bull sperm. Theriogenology. 2016;85(3):528-32.
Arias LS, Pessan JP, Vieira APM, De Lima TMT, Delbem ACB, Monteiro DR. Iron oxide nanoparticles for biomedical applications: a perspective on synthesis, drugs, antimicrobial activity, and toxicity. Antibiotics (Basel). 2018;7(2):46.
Asadi Z, Safari-Faramani R, Aghaz F. Effects of adding antioxidant nanoparticles on sperm parameters of non-human species after the freezing and thawing process: a systematic review and meta-analysis. Anim Reprod Sci. 2023;257:107323.
Atessahin A, Numan Bucak M, Barbaros Tuncer P, Kızıl M. Effects of anti-oxidant additives on microscopic and oxidative parameters of Angora goat semen following the freeze-thawing process. Small Rumin Res. 2008;77(1):38-44.
Avendaño C, Franchi A, Taylor S, Morshedi M, Bocca S, Oehninger S. Fragmentation of DNA in morphologically normal human spermatozoa. Fertil Steril. 2009;91(4):1077-84.
Bae JW, Yi JK, Jeong EJ, Lee WJ, Hwang JM, Kim DH, Ha JJ, Kwon WS. Ras-related proteins (Rab) play significant roles in sperm motility and capacitation status. Reprod Biol. 2022;22(2):100617.
Baker MA, Reeves G, Hetherington L, Müller J, Baur I, Aitken RJ. Identification of gene products present in Triton X-100 soluble and insoluble fractions of human spermatozoa lysates using LC-MS/MS analysis. Proteomics Clin Appl. 2007;1(5):524-32.
Barranco I, Rubio CP, Tvarijonaviciute A, Rodriguez-Martinez H, Roca J. Measurement of oxidative stress index in seminal plasma can predict in vivo fertility of liquid-stored porcine artificial insemination semen doses. Antioxidants. 2021;10(8):1203.
Barwant MM, Rasool A, Mannam VK, Hussain A, Abdullah M, Memon Z, Ahamad MI, Shirani M, Maqbool KZ, Majeed M, Asif M, Khan UA. Nanotechnology applications in livestock farming and animal health. In: Rajput V, Singh A, Ghazaryan K, Alexiou A, Said Al-Tawaha A, editors. Harnessing nanoomics and nanozymes for sustainable agriculture. Hershey: IGI Global; 2024. p. 413–42.
Bera D, Qian L, Tseng TK, Holloway PH. Quantum dots and their multimodal applications: a review. Materials (Basel). 2010;3(4):2260-345.
Castiglioni VC, Felipe A, Siqueira P, Bicudo LDC, De Almeida TG, Rose T, Nichi M, Diego J, Losano DA, Visitin JA. Lipid peroxidation in bull semen influences sperm traits and oxidative potential of Percoll ® -selected sperm. Zygote. 2021;29(6):476-83.
Cecere JT. Eosin-nigrosin staining in the evaluation of sperm. In: Dascanio JJ, McCue PM, editors. Equine reproductive procedures. Hoboken: John Wiley and Sons; 2014. p 373–6.: http://doi.org/10.1002/9781118904398.ch114.
Chen Y, Cann MJ, Litvin TN, Iourgenko V, Sinclair ML, Levin LR, Buck J. Soluble adenylyl cyclase as an evolutionarily conserved bicarbonate sensor. Science. 2000;289(5479):625-8.
Cooper TG. Cytoplasmic droplets: the good, the bad or just confusing? Hum Reprod. 2005;20(1):9-11.
Coy P, Cánovas S, Mondéjar I, Saavedra MD, Romar R, Grullón L, Matás C, Avilés M. Oviduct-specific glycoprotein and heparin modulate sperm-zona pellucida interaction during fertilization and contribute to the control of polyspermy. Proc Natl Acad Sci USA. 2008;105(41):15809-14.
Dacheux JL, Dacheux F. New insights into epididymal function in relation to sperm maturation. Reproduction. 2014;147(2):27-42.
DasGupta MA, Kumaresan AA, Kishor Saraf KA, Karthikkeyan GB, Keshava Prasad BTS, Kumar Modi PB, Ramesha KC, Jeyakumar SC, Manimaran AC. Preliminary comparative deep metabolomic analysis of spermatozoa from zebu and crossbred cattle suggests associations between metabolites, sperm quality and fertility. Reprod Fertil Dev. 2021;33(6):427-36.
Deshpande PP, Biswas S, Torchilin VP. Current trends in the use of liposomes for tumor targeting. Nanomedicine (Lond). 2013;8(9):1509-28.
Díaz-Miranda EA, Maitan PP, Machado TP, Camilo BS, Lima DA, Okano DS, Penitente-Filho JM, Machado-Neves M, Oliveira LL, Guimarães SEF, Costa EP, Guimarães JD. Disruption of bovine sperm functions in the presence of aplastic midpiece defect. Andrology. 2020;8(1):201-10.
Dilsiz N. Hallmarks of exosomes. Future Sci OA. 2022;8(1):FSO764.
Dlamini NH, Nguyen T, Gad A, Tesfaye D, Liao SF, Willard ST, Ryan PL, Feugang JM. Characterization of extracellular vesicle-coupled mirna profiles in seminal plasma of boars with divergent semen quality status. Int J Mol Sci. 2023;24(4):3194.
Dogan S, Vargovic P, Oliveira R, Belser LE, Kaya A, Moura A, Sutovsky P, Parrish J, Topper E, Memili E. Sperm protamine-status correlates to the fertility of breeding bulls. Biol Reprod. 2015;92(4):92.
Domínguez E, Moreno-Irusta A, Castex HR, Bragulat AF, Ugaz C, Clemente H, Giojalas L, Losinno L. Sperm sexing mediated by magnetic nanoparticles in donkeys, a preliminary in vitro study. J Equine Vet Sci. 2018;65:123-7.
Donaldson K, Aitken R, Tran L, Stone V, Duffin R, Forrest G, Alexander A. Carbon nanotubes: a review of their properties in relation to pulmonary toxicology and workplace safety. Toxicol Sci. 2006;92(1):5-22.
Donaldson K, Tran CL. Inflammation caused by particles and fibers. Inhal Toxicol. 2002;14(1):5-27.
Du J, Shen J, Wang Y, Pan C, Pang W, Diao H, Dong W. Boar seminal plasma exosomes maintain sperm function by infiltrating into the sperm membrane. Oncotarget. 2016;7(37):58832-47.
Durairajanayagam D, Rengan AK, Sharma RK, Agarwal A. Sperm biology from production to ejaculation. In: Schattman G, Esteves S, Agarwal A, editors. Unexplained Infertility. New York: Springer; 2015. p. 29–42.
Durfey CL, Swistek SE, Liao SF, Crenshaw MA, Clemente HJ, Thirumalai RVKG, Steadman CS, Ryan PL, Willard ST, Feugang JM. Nanotechnology-based approach for safer enrichment of semen with best spermatozoa. J Anim Sci Biotechnol. 2019;10(1):14.
Elmi A, Banchelli F, Barone F, Fantinati P, Ventrella D, Forni M, Bacci ML. Semen evaluation and in vivo fertility in a Northern Italian pig farm: can advanced statistical approaches compensate for low sample size? An observational study. Anim Reprod Sci. 2018;192:61-8.
Falchi L, Galleri G, Dore GM, Zedda MT, Pau S, Bogliolo L, Ariu F, Pinna A, Nieddu S, Innocenzi P, Ledda S. Effect of exposure to CeO2 nanoparticles on ram spermatozoa during storage at 4°C for 96 hours. Reprod Biol Endocrinol. 2018a;16(1):19.
Falchi L, Galleri G, Zedda MT, Pau S, Bogliolo L, Ariu F, Ledda S. Liquid storage of ram semen for 96 hours: effects on kinematic parameters, membranes and DNA integrity, and ROS production. Livest Sci. 2018b;207:1-6.
Falchi L, Khalil WA, Hassan M, Marei WFA. Perspectives of nanotechnology in male fertility and sperm function. Int J Vet Sci Med. 2018c;6(2):265-9.
Ferrigno A, Ruvolo G, Capra G, Serra N, Bosco L. Correlation between the DNA fragmentation index (DFI) and sperm morphology of infertile patients. J Assist Reprod Genet. 2021;38(4):979-86.
Feugang JM, Ishak GM, Eggert MW, Arnold RD, Rivers OS, Willard ST, Ryan PL, Gastal EL. Intrafollicular injection of nanomolecules for advancing knowledge on folliculogenesis in livestock. Theriogenology. 2022;192:132-40.
Feugang JM, Liao SF, Crenshaw MA, Clemente H, Willard ST, Ryan PL. Lectin-functionalized magnetic iron oxide nanoparticles for reproductive improvement. Reprod Med Genet. 2015a;3(2):145.
Feugang JM, Rhoads CE, Mustapha PA, Tardif S, Parrish JJ, Willard ST, Ryan PL. Treatment of boar sperm with nanoparticles for improved fertility. Theriogenology. 2019;137:75-81.
Feugang JM, Youngblood RC, Greene JM, Fahad AS, Monroe WA, Willard ST, Ryan PL. Application of quantum dot nanoparticles for potential non-invasive bio-imaging of mammalian spermatozoa. J Nanobiotechnology. 2012;10(1):45.
Feugang JM, Youngblood RC, Greene JM, Willard ST, Ryan PL. Self-illuminating quantum dots for non-invasive bioluminescence imaging of mammalian gametes. J Nanobiotechnology. 2015b;13(1):38.
Feugang JM. Novel agents for sperm purification, sorting, and imaging. Mol Reprod Dev. 2017;84(9):832-41.
Finkelstein M, Etkovitz N, Breitbart H. Ca2+ signaling in mammalian spermatozoa. Mol Cell Endocrinol. 2020;516:110953.
Fitts CA, Ji N, Li Y, Tan C. Exploiting exosomes in cancer liquid biopsies and drug delivery. Adv Healthc Mater. 2019;8(6):e1801268.
Fraser L, Brym P, Pareek CS, Mogielnicka-brzozowska M, Paukszto Ł, Jastrze JP, Wasilewska-sakowska K, Ma A. Transcriptome analysis of boar spermatozoa with different freezability using RNA-Seq. Theriogenology. 2020;142:400-13.
Gadella BM, Luna C. Cell biology and functional dynamics of the mammalian sperm surface. Theriogenology. 2014;81(1):74-84.
Gaitskell-Phillips G, Martín-Cano FE, Ortiz-Rodríguez JM, Silva-Rodríguez A, Gil MC, Ortega-ferrusola C, Peña FJ. Differences in the proteome of stallion spermatozoa explain stallion-to-stallion variability in sperm quality post-thaw†. Biol Reprod. 2021a;104(5):1097-113.
Gaitskell-Phillips G, Martín-Cano FE, Ortiz-Rodríguez JM, Silva-Rodríguez A, Da Silva-Álvarez E, Rojo-Domínguez P, Tapia JA, Gil MC, Ortega-Ferrusola C, Peña FJ. Proteins involved in mitochondrial metabolic functions and fertilization predominate in stallions with better motility. J Proteomics. 2021b;247:104335.
Gallo A, Esposito MC, Tosti E, Boni R. Sperm motility, oxidative status, and mitochondrial activity: exploring correlation in different species. Antioxidants. 2021;10(7):1131.
Ganguly I, Gaur GK, Kumar S, Mandal DK, Kumar M, Singh U, Kumar S, Sharma A. Differential expression of protamine 1 and 2 genes in mature spermatozoa of normal and motility impaired semen producing crossbred Frieswal (HF×Sahiwal) bulls. Res Vet Sci. 2013;94(2):256-62.
Gibbons R, Adeoya-Osiguwa SA, Fraser LR. A mouse sperm decapacitation factor receptor is phosphatidylethanolamine-binding protein 1. Reproduction. 2005;130(4):497-508.
Gundogan M, Yeni D, Avdatek F, Fidan AF. Influence of sperm concentration on the motility, morphology, membrane and DNA integrity along with oxidative stress parameters of ram sperm during liquid storage. Anim Reprod Sci. 2010;122(3–4):200-7.
Han JW, Jeong J-K, Gurunathan S, Choi Y-J, Das J, Kwon D-N, Cho S-G, Park C, Seo HG, Park J-K, Kim J-H. Male- and female-derived somatic and germ cell-specific toxicity of silver nanoparticles in mouse. Nanotoxicology. 2016;10(3):361-73.
Hashem NM, Gonzales-Bulnes A. State-of-the-art and prospective of nanotechnologies. Animals (Basel). 2020;10(5):840.
He L, Bailey JL, Buhr MM. Incorporating lipids into boar sperm decreases chilling sensitivity but not capacitation potential. Biol Reprod. 2001;64(1):69-79.
Henkel RR, Schill WB. Sperm preparation for ART. Reprod Biol Endocrinol. 2003;1(1):108.
Hill EK, Li J. Current and future prospects for nanotechnology in animal production. J Anim Sci Biotechnol. 2017;8(1):26.
Hitit M, Memili E. Sperm signatures of fertility and freezability. Anim Reprod Sci. 2022;247:107147.
Hitit M, Özbek M, Ayaz-Guner S, Guner H, Oztug M, Bodu M, Kirbas M, Bulbul B, Bucak MN, Ataman MB, Memili E, Kaya A. Proteomic fertility markers in ram sperm. Anim Reprod Sci. 2021;235:106882.
Holstein AF, Schulze W, Davidoff M. Understanding spermatogenesis is a prerequisite for treatment. Reprod Biol Endocrinol. 2003;1(1):107.
Holt W, Morrell J. Sperm biology and maturation. In: Coward K, Wells D, editors, Textbook of clinical embryology. Cambridge: Cambridge University Press; 2013. p. 89–97.
Holt WV, Fazeli A. Do sperm possess a molecular passport? Mechanistic insights into sperm selection in the female reproductive tract. Mol Hum Reprod. 2015;21(6):491-501.
Hosseinmardi M, Siadat F, Sharafi M, Roodbari NH, Hezavehei M. Protective effect of cerium oxide nanoparticles on human sperm function during cryopreservation. Biopreserv Biobank. 2022;20(1):24-30.
Hungerford A, Bakos HW, Aitken RJ, Martin G. Sperm cryopreservation: current status and future developments. Reprod Fertil Dev. 2022;35(3):265-81.
Inanç ME, Çi̇l B, Teki̇n K, Alemdar H, Daşkin A. The combination of CASA kinetic parameters and fluorescein staining as a fertility tool in cryopreserved bull semen. Turk J Vet Anim Sci. 2018;42(5):452.
Jain S, Park SB, Pillai SR, Ryan PL, Willard ST, Feugang JM. Applications of fluorescent quantum dots for reproductive medicine and disease detection. In: Gomes AC, Sarria MP, editors. Unraveling the safety profile of nanoscale particles and materials - from biomedical to environmental applications. London: InTech; 2018. Chapter 6. http://doi.org/10.5772/intechopen.72978.
Jia B, Liang J, Lv C, Memon S, Fang Y, Wu G, Quan G. The characteristics of proteome and metabolome associated with contrasting sperm motility in goat seminal plasma. Sci Rep. 2021;11(1):15562.
Johnston DS, Wooters J, Kopf GS, Qiu Y, Roberts KP. Analysis of the human sperm proteome. Ann N Y Acad Sci. 2005;1061(1):190-202.
Jones RC. Evolution of the vertebrate epididymis. In: Robaire, B., Hinton, B.T., editors. The Epididymis: From Molecules to Clinical Practice. Boston: Springer; 2002.
Jurado-Campos A, Soria-Meneses PJ, Arenas-Moreira M, Alonso-Moreno C, Rodríguez-Robledo V, Soler AJ, Garde JJ, Del Rocío Fernández-Santos M. Minimizing sperm oxidative stress using nanotechnology for breeding programs in rams. J Anim Sci Biotechnol. 2023;14(1):106.
Kameni SL, Dongmo ABN, Tebug TT, Bomba FDT, Meutchieye F, Ngoula F. Spirulina (Arthrospira platensis) extract promotes motility, microscopic, and antioxidative parameters of ram semen during refrigerated storage. BSJ Agri. 2022;5(4):481-90.
Kameni SL, Meutchieye F, Ngoula F. Liquid storage of ram semen: associated damages and improvement. Open J Anim Sci. 2021;11(3):473-500.
Ka̧tska-Ksia̧zkiewicz L, Ryńska B, Gajda B, Smora̧g Z. Effect of donor stimulation, frozen semen and heparin treatment on the efficiency of in vitro embryo production in goats. Theriogenology. 2004;62(3–4):576-86.
Khalique MA, Andrabi SMH, Majeed KA, Yousaf MS, Ahmad N, Tahir SK, Fayyaz MH, Haider MS, Naz SS, Qureshi IZ, Sulaiman S, Zaneb H, Rehman H. Cerium oxide nanoparticles improve the post-thaw quality and in-vivo fertility of Beetal buck spermatozoa. Theriogenology. 2024;214:166-72.
Khalique MA, Rehman H, Andrabi SMH, Majeed KA, Ahmad N, Fayyaz MH, Haider MS, Naz SS, Qureshi IZ, Sulaiman S, Jammu A. Antioxidant effects of zinc-oxide nanoparticles on post-thaw quality and in vivo fertility of Beetal buck spermatozoa. Small Rumin Res. 2023;225:107012.
Khan GS, Tahir MZ, Zahoor MY, Rahman H, Riaz A. Ameliorative effect of crocin on post-thaw quality, fertility-associated gene expression and fertilization potential of buffalo (Bubalus bubalis) bull sperm. Reprod Domest Anim. 2024;59(1):e14519.
Kherzi A, Naraud B, Stenseth EB, Johannisson A, Myromslien FD, Gaustad AH, Wilson RC, Lyle R, Morell JM, Kommisrud E, Ahmad R. DNA methylation patterns vary in boar sperm cells with different levels of DNA fragmentation. BMC Genomics. 2019;20(1):897.
Khodaei-Motlagh M, Masoudi R, Karimi-Sabet MJ, Hatefi A. Supplementation of sperm cooling medium with Zinc and Zinc oxide nanoparticles preserves rooster sperm quality and fertility potential. Theriogenology. 2022;183:36-40.
Kim S, Lim YT, Soltesz EG, De Grand AM, Lee J, Nakayama A, Parker JA, Mihaljevic T, Laurence RG, Dor DM, Cohn LH, Bawendi MG, Frangioni JV. Near-infrared fluorescent type II quantum dots for sentinel lymph node mapping. Nat Biotechnol. 2004;22(1):93-7.
Kumar P, Saini M, Kumar D, Balhara AK, Yadav SP, Singh P, Yadav PS. Liposome-based semen extender is suitable alternative to egg yolk-based extender for cryopreservation of buffalo (Bubalus bubalis) semen. Anim Reprod Sci. 2015;159:38-45.
Kumaresan A, Das Gupta M, Datta TK, Morrell JM. Sperm DNA Integrity and male fertility in farm animals: a review. Front Vet Sci. 2020;7:321.
Kuo R, Saito E, Miller SD, Shea LD. Peptide-conjugated nanoparticles reduce positive co-stimulatory expression and T cell activity to induce tolerance. Mol Ther. 2017;25(7):1676-85.
Kwon W, Rahman S, Ryu D, Park Y, Pang M. Increased male fertility using fertility-related biomarkers. Sci Rep. 2015;5(1):15654.
Lacalle E, Consuegra C, Martínez CA, Hidalgo M, Dorado J, Martínez-Pastor F, Álvarez-Rodríguez M, Rodríguez-Martínez H. Bicarbonate-triggered in vitro capacitation of boar spermatozoa conveys an increased relative abundance of the canonical Transient Receptor Potential Cation (TRPC) Channels 3, 4, 6 and 7 and of CatSper-γ Subunit mRNA Transcripts. Animals (Basel). 2022;12(8):1012.
Lalancette C, Thibault C, Bachand I, Caron N, Bissonnette N. Transcriptome analysis of bull semen with extreme nonreturn rate: use of suppression-subtractive hybridization to identify functional markers for fertility. Biol Reprod. 2008;78(4):618-35.
Lee B, Park Y, Pang W, Ryu D, Rahman S, Lee D, Pang M. Boar fertility is controlled through systematic changes of mitochondrial protein expression during sperm capacitation. Int J Biol Macromol. 2023;248:125955.
Leite RF, Losano JDA, Kawai GKV, Rui BR, Nagai KK, Castiglioni VC, Siqueira AFP, D’Avila Assumpção MEO, Baruselli PS, Nichi M. Sperm function and oxidative status: effect on fertility in Bos taurus and Bos indicus bulls when semen is used for fixed-time artificial insemination. Anim Reprod Sci. 2022;237:106922.
Llavanera M, Ribas-maynou J, Delgado-bermúdez A, Recuero S, Muiño R, Hidalgo CO, Tamargo C, Bonet S, Mateo-otero Y, Yeste M. Sperm chromatin condensation as an in vivo fertility biomarker in bulls: a flow cytometry approach. J Anim Sci Biotechnol. 2021;12(1):115.
López-Úbeda R, García-Vázquez FA, Romar R, Gadea J, Muñoz M, Hunter RHF, Coy P. Oviductal transcriptome is modified after insemination during spontaneous ovulation in the sow. PLoS One. 2015;10(6):0130128.
Lu CH, Lee RKK, Hwu YM, Chu SL, Chen YJ, Chang WC, Lin SP, Li SH. SERPINE2, a serine protease inhibitor extensively expressed in adult male mouse reproductive tissues, may serve as a murine sperm decapacitation factor. Biol Reprod. 2011;84(3):514-25.
Lucca MS, Dal R, Gianluppi F, Paula A, Mellagi G, Pandolfo Bortolozzo F, Wentz I, Da R, Ulguim R. Effects of the classification of boars according to progressive sperm motility and the extender type on the reproductive performance of a single fixed-time insemination. Theriogenology. 2021;161:120-5.
Luna-Orozco JR, González-Ramos MA, Calderón-Leyva G, Gaytán-Alemán LR, Arellano-Rodríguez MA, Ángel-García O, Véliz-Deras FG. Comparison of different diluents based on liposomes and egg yolk for ram semen cooling and cryopreservation. IJVR. 2019;20(2):126-30. PMid:31531035.
Mafolo KS, Pilane CM, Chitura T, Nedambale TL. Use of phosphatidylcholine in Tris-based extender with or without egg yolk to freeze Bapedi ram semen. S Afr J Anim Sci. 2020;50(3):389-96.
Mateo-Otero Y, Madrid-gambin F, Llavanera M, Gomez-gomez A, Haro N, Pozo OJ, Yeste M. Sperm physiology and in vitro fertilising ability rely on basal metabolic activity: insights from the pig model. Commun Biol. 2023;6(1):344.
Medina-León AZ, Domínguez-mancera B, Cazalez-penino N, Cervantes-Acosta P, Jácome-Sosa E, Romero-Salas D, Barrientos-Morales M. Cryopreservation of horse semen with a liposome and trehalose added extender. Austral J Vet Sci. 2019;51(3):119-23.
Meles DK, Mustofa I, Hariadi M, Wurlina W, Susilowati S, Amaliya A, Suparto S, Rimayanti R. The enriched Y-bearing sperm combined with delayed fixed-time artificial insemination for obtaining male Simmental crossbred offspring. Vet World. 2022;15(1):102-9.
Menezes EB, Velho ALC, Santos F, Dinh T, Kaya A, Topper E, Moura AA, Memili E. Uncovering sperm metabolome to discover biomarkers for bull fertility. BMC Genomics. 2019;20(1):714.
Mo R, Jiang T, Gu Z. Recent progress in multidrug delivery to cancer cells by liposomes. Nanomedicine (Lond). 2014;9(8):1117-20.
Mokarizadeh A, Rezvanfar M, Dorostkar K, Abdollahi M. Mesenchymal stem cell derived microvesicles: trophic shuttles for enhancement of sperm quality parameters. Reprod Toxicol. 2013;42:78-84.
Montecalvo A, Larregina AT, Shufesky WJ, Stolz DB, Sullivan MLG, Karlsson JM, Baty CJ, Gibson GA, Erdos G, Wang Z, Milosevic J, Tkacheva OA, Divito SJ, Jordan R, Lyons-Weiler J, Watkins SC, Morelli AE. Mechanism of transfer of functional microRNAs between mouse dendritic cells via exosomes. Blood. 2012;119(3):756-66.
Mortazavi S, Eslami M, Farrokhi-ardabili F. Comparison of different carrier-compounds and varying concentrations of oleic acid on freezing tolerance of ram spermatozoa in tris-citric acid-egg yolk plasma semen diluent. Anim Reprod Sci. 2020;219:106533.
NNI [homepage on the Internet]. 2024 [cited 2024 Mar 16]. Available from: www.nano.gov
Neto FTL, Bach PV, Najari BB, Li PS, Goldstein M. Spermatogenesis in humans and its affecting factors. Semin Cell Dev Biol. 2016;59:10-26.
Odhiambo JF, Dejarnette JM, Geary TW, Kennedy CE, Suarez SS, Sutovsky P. Increased conception rates in beef cattle inseminated with nanopurified bull downloaded from downloaded from. Biol Reprod. 2014;91(4):97.
Paciotti GF, Kingston DGI, Tamarkin L. Colloidal gold nanoparticles: a novel nanoparticle platform for developing multifunctional tumor-targeted drug delivery vectors. Drug Dev Res. 2006;67(1):47-54.
Peddinti D, Nanduri B, Kaya A, Feugang JM, Burgess SC, Memili E. Comprehensive proteomic analysis of bovine spermatozoa of varying fertility rates and identification of biomarkers associated with fertility. BMC Syst Biol. 2008;2(1):19.
Pessoa ER, Roger Vasconcelos F, de Oliveira Paula‐Marinho S, de Menezes Daloso D, Damasceno Guerreiro D, Matias Martins JA, Gomes-Filho E, Alencar Moura A. Metabolomic profile of seminal plasma from Guzerá bulls (Bos indicus) with contrasting sperm freezability phenotypes. Reprod Domest Anim. 2023;58(10):1379-92.
Piehl LL, Fischman ML, Hellman U, Cisale H, Miranda PV. Boar seminal plasma exosomes: effect on sperm function and protein identification by sequencing. Theriogenology. 2013;79(7):1071-82.
Pillet E, Labbe C, Batellier F, Duchamp G, Beaumal V, Anton M, Desherces S, Schmitt E, Magistrini M. Liposomes as an alternative to egg yolk in stallion freezing extender. Theriogenology. 2012;77(2):268-79.
Purdy PH, Graham JK. Membrane modification strategies for cryopreservation. In: Wolkers W, Oldenhof H, editors. Cryopreservation and freeze-drying protocols. New York: Springer; 2015. p. 337-42.
Qamar AY, Fang X, Kim MJ, Cho J. Improved post-thaw quality of canine semen after treatment with exosomes from conditioned medium of adipose-derived mesenchymal stem cells. Animals (Basel). 2019;9(11):865.
Quelhas J, Pinto-Pinho P, Lopes G, Rocha A, Pinto-Leite R, Fardilha M, Colaço B, Feugang J, Chapwanya A, Bianchi M, Alves R. Sustainable animal production: exploring the benefits of sperm sexing technologies in addressing critical industry challenges. Front Vet Sci. 2023;10:1181659.
Quelhas J, Santiago J, Matos B, Rocha A, Lopes G, Fardilha M. Bovine semen sexing: sperm membrane proteomics as candidates for immunological selection of X‐ and Y‐chromosome‐bearing sperm. Vet Med Sci. 2021;7(5):1633-41.
Rodríguez-Martínez H, Kvist U, Ernerudh J, Sanz L, Calvete JJ. Seminal plasma proteins: what role do they play? Am J Reprod Immunol. 2011;66(Suppl 1):11-22.
Röpke T, Oldenhof H, Leiding C, Sieme H, Bollwein H, Wolkers WF. Liposomes for cryopreservation of bovine sperm. Theriogenology. 2011;76(8):1465-72.
Saadeldin IM, Khalil WA, Alharbi MG, Lee SH. The Current Trends in Using Nanoparticles, Liposomes, and Exosomes for Semen Cryopreservation. Animals (Basel). 2020;10(12):2281.
Sapanidou V, Tsantarliotou MP, Lavrentiadou SN. A review of the use of antioxidants in bovine sperm preparation protocols. Anim Reprod Sci. 2023;251:107215.
Saraf KK, Kumaresan A, Sinha MK, Datta TK. Spermatozoal transcripts associated with oxidative stress and mitochondrial membrane potential differ between high‐ and low‐fertile crossbred bulls. Andrologia. 2021;53(5):e14029.
Saravia F, Wallgren M, Johannisson A, Calvete JJ, Sanz L, Peña FJ, Roca J, Rodríguez-Martínez H. Exposure to the seminal plasma of different portions of the boar ejaculate modulates the survival of spermatozoa cryopreserved in MiniFlatPacks. Theriogenology. 2009;71(4):662-75.
Sellem E, Broekhuijse MLWJ, Chevrier L, Camugli S, Schmitt E, Schibler L, Koenen EPC. Use of combinations of in vitro quality assessments to predict fertility of bovine semen. Theriogenolog. 2015;84(9):1447-1454.e5.
Selokar NL, Dua S, Kumar D, Sharma B, Saini M. Application of nanotechnology in agricultural farm animals. In Ghorbanpour M, Bhargava P, Varma A, Choudhary D, editors. Biogenic nano-particles and their use in agro-ecosystem. New York: Springer; 2020. p. 1–8..
Sharma R, Agarwal A. Spermatogenesis: an overview. In: Zini A, Agarwal A, editors, Sperm chromatin. New York: Springer; 2011. p. 19–44.
Sharma U, Conine CC, Shea JM, Boskovic A, Derr AG, Bing XY, Belleannee C, Kucukural A, Serra RW, Sun F, Song L, Carone BR, Ricci EP, Li XZ, Fauquier L, Moore MJ, Sullivan R, Mello CC, Garber M, Rando OJ. Biogenesis and function of tRNA fragments during sperm maturation and fertilization in mammals. Science. 2016;351(6271):391-6.
Siu KK, Serrão VHB, Ziyyat A, Lee JE. The cell biology of fertilization: gamete attachment and fusion. J Cell Biol. 2021;220(10):e202102146.
Soggiu A, Piras C, Hussein HA, De Canio M, Gaviraghi A, Galli A, Urbani A, Bonizzi L, Roncada P. Unravelling the bull fertility proteome. Mol Biosyst. 2013;9(6):1188-95.
Song C, Chang L, Wang B, Zhang Z, Wei Y, Dou Y, Qi K, Yang F, Li X, Li X, Wang K, Qiao R, Han X. Seminal plasma metabolomics analysis of differences in liquid preservation ability of boar sperm. J Anim Sci. 2023;101:skad392.
Song C, Zhang Z, Wei Y, Dou Y, Qi K, Li X, Yang F, Li X, Wang K, Qiao R, Han X. Proteomic analysis of boar sperm with differential ability of liquid preservation at 17°C. Theriogenology. 2024;215:103-12.
Sostaric E, Dieleman SJ, Van De Lest CHA, Colenbrander B, Vos PLAM, Garcia-Gil N, Gadella BM. Sperm binding properties and secretory activity of the bovine oviduct immediately before and after ovulation. Mol Reprod Dev. 2008;75(1):60-74.
Souza ET, Silva CV, Augusto B, Travençolo N, Geraldo B, Emílio M. Sperm chromatin alterations in fertile and subfertile bulls. Reprod Biol. 2018;18(2):177-81.
Staub C, Johnson L. Review: spermatogenesis in the bull. Animal. 2018;12(1):s27-35.
Suchocki T, Szyda J. Genome-wide association study for semen production traits in Holstein-Friesian bulls. J Dairy Sci. 2015;98(8):5774-80.
Sui H, Sheng M, Luo H, Liu G, Meng F, Cao Z, Zhang Y. Characterization of freezability-associated metabolites in boar semen. Theriogenology. 2023;196:88-96.
Suk JS, Xu Q, Kim N, Hanes J, Ensign LM. PEGylation as a strategy for improving nanoparticle-based drug and gene delivery HHS Public Access Graphical abstract. Adv Drug Deliv Rev. 2016;99(Pt A):28-51.
Sullivan R, Saez F, Girouard J, Frenette G. Role of exosomes in sperm maturation during the transit along the male reproductive tract. Blood Cells Mol Dis. 2005;35(1):1-10.
Sun P, Zhang G, Xian M, Zhang G, Wen F, Hu Z, Hu J. Proteomic analysis of frozen–thawed spermatozoa with different levels of freezability in dairy goats. Int J Mol Sci. 2023;24(21):15550.
Sun T, Zhang YS, Pang B, Hyun DC, Yang M, Xia Y. Engineered nanoparticles for drug delivery in cancer therapy. Angew Chem Int Ed Engl. 2014;53(46):12320-64.
Sutovsky P, Hamilton LE, Zigo M, Ortiz DME, Assumpção A, Jones A, Tirpak F, Agca Y, Kerns K, Sutovsky M. Biomarker-based human and animal sperm phenotyping. Biol Reprod. 2024;110(6):1156-6.
Sutovsky P, Lovercamp K. Molecular markers of sperm quality. Soc Reprod Fertil Suppl. 2010;67:247-56.
Swelum AA-A, Saadeldin IM, Ba-Awadh H, Al-Mutary MG, Moumen AF, Alowaimer AN, Abdalla H. Efficiency of Commercial Egg Yolk-Free and Egg Yolk-Supplemented Tris-Based Extenders for Dromedary Camel Semen Cryopreservation. Animals (Basel). 2019;9(11):999.
Szczęch M, Szczepanowicz K. Polymeric core-shell nanoparticles prepared by spontaneous emulsification solvent evaporation and functionalized by the layer-by-layer method. Nanomaterials (Basel). 2020;10(3):496.
Talevi R, Gualtieri R. Molecules involved in sperm-oviduct adhesion and release. Theriogenology. 2010;73(6):796-801.
Tardif S, Dubé C, Chevalier S, Bailey JL. Capacitation is associated with tyrosine phosphorylation and tyrosine kinase-like activity of pig sperm proteins. Biol Reprod. 2001;65(3):784-92.
Torres MA, Pedrosa AC, Novais FJ, Alkmin DV, Cooper BR, Yasui GS, Fukumasu H, Machaty Z, Andrade AFCD. Metabolomic signature of spermatozoa established during holding time is responsible for differences in boar sperm†. Biol Reprod. 2022;106(1):213-26.
Touré A. Importance of slc26 transmembrane anion exchangers in sperm post-testicular maturation and fertilization potential. Front Cell Dev Biol. 2019;7:230.
Travis AJ, Kopf GS. The role of cholesterol efflux in regulating the fertilization potential of mammalian spermatozoa. J Clin Invest. 2002;110(6):731-6.
Trimeche A, Yvon JM, Vidament M, Palmer E, Magistrini M. Effects of glutamine, proline, histidine and betaine on post-thaw motility of stallion spermatozoa. Theriogenology. 1999;52(1):181-91.
Troedsson MHT, Desvousges A, Alghamdi AS, Dahms B, Dow CA, Hayna J, Valesco R, Collahan PT, Macpherson ML, Pozor M, Buhi WC. Components in seminal plasma regulating sperm transport and elimination. Anim Reprod Sci. 2005;89(1-4):1-4.
Ugur MR, Dinh T, Hitit M, Kaya A, Topper E, Didion B, Memili E. Amino acids of seminal plasma associated with freezability of bull sperm. Front Cell Dev Biol. 2020;7:347.
Ugur MR, Saber Abdelrahman A, Evans HC, Gilmore AA, Hitit M, Arifiantini RI, Purwantara B, Kaya A, Memili E. Advances in Cryopreservation of Bull Sperm. Front Vet Sci. 2019;6:268.
Ul Haq Z, Hamadani H, Khan AA, Ganai AM, Beigh YA, Gull Sheikh G, Farooq J, Ahmad Ganai I, Ahmad SM. Nanotechnology: changing the world of animal health and veterinary medicine. In: Sheikh FA, Majeed S, Beigh MA, editors. Interaction of nanomaterials with living cells.New York: Springer Nature; 2023. p. 167-96.
Valgimigli L, Baschieri A, Amorati R. Antioxidant activity of nanomaterials. J Mater Chem B Mater Biol Med. 2018;6(14):2036-51.
Vicente-Fiel S, Palacín I, Santolaria P, Fantova E, Quintín-casorrán FJ, Sevilla-Mur E, Yániz JL. In vitro assessment of sperm quality from rams of high and low field fertility. Anim Reprod Sci. 2014;146(1–2):15-20.
Virlan MJR, Miricescu D, Radulescu R, Sabliov CM, Totan A, Calenic B, Greabu M. Organic nanomaterials and their applications in the treatment of oral diseases. Molecules. 2016;21(2):207.
Wang L, Zhao W, Tan W. Bioconjugated silica nanoparticles: development and applications. Nano Res. 2008;1(2):99-115.
Wang Y, Quinsaat JEQ, Ono T, Maeki M, Tokeshi M, Isono T, Tajima K, Satoh T, Sato S, Miura Y, Yamamoto T. Enhanced dispersion stability of gold nanoparticles by the physisorption of cyclic poly(ethylene glycol). Nat Commun. 2020;11(1):6089.
Weng J, Ren J. Luminescent Quantum Dots: A Very Attractive and Promising Tool in Biomedicine. Curr Med Chem. 2006;13(8):897-909.
Wiebke M, Hensel B, Nitsche-Melkus E, Jung M, Schulze M. Cooled storage of semen from livestock animals (part I): boar, bull, and stallion. Anim Reprod Sci. 2022;246:106822.
Xu C, Nam J, Hong H, Xu Y, Moon JJ. Positron emission tomography-guided photodynamic therapy with biodegradable mesoporous silica nanoparticles for personalized cancer immunotherapy. ACS Nano. 2019;13(10):12148-61.
Yang C, Guo W-B, Zhang W-S, Bian J, Yang J-K, Zhou Q-Z, Chen M-K, Peng W, Qi T, Wang C-Y, Liu C-D. Comprehensive proteomics analysis of exosomes derived from human seminal plasma. Andrology. 2017;5(5):1007-15.
Yang W, Liang H, Ma S, Wang D, Huang J. Gold nanoparticle based photothermal therapy: development and application for effective cancer treatment. Sust Mat Tech. 2019;22:e00109.
Yata VK. Sperm sexing: methods, applications, and the possible role of microfluidics. In: Yata VK, editor. Microfluidics for assisted reproduction in animals. Singapore: Springer; 2021. p. 89-109..
Yeste M. Sperm cryopreservation update: Cryodamage, markers, and factors affecting the sperm freezability in pigs. Theriogenology. 2016;85(1):47-64.
Yoon S-J, Kwon W-S, Rahman MS, Lee J-S, Pang M-G. A novel approach to identifying physical markers of cryo-damage in bull spermatozoa. PLoS One. 2015;10(5):e0126232.
Yuan Y, Yu M, Chen L, Ren X, Qu Y, Shari A, Li G. Comparative analysis of different metabolites in semen of Guanzhong dairy goats with different motility rates. Theriogenology. 2023a;210:53-61.
Yuan Y, Wang G, Zou J, Zhang Y, Li D, Yu M, Chen L, Li G. Study on comparative analysis of differential metabolites in Guanzhong dairy goat semen before and after freezing. Theriogenology. 2023b;197:232-9.
Zeng F, Chen Y, Guo C, Li C, Wei H, Li L, Meng L, Zhang S. Analysis of differentially abundant proteins related to boar fertility in seminal plasma using iTRAQ-based quantitative proteomics. J Proteomics. 2021;236:104120.
Zhang H, Liu H, Kataoka S, Kinukawa M, Uchiyama K, Kambe J, Watanabe G, Jin W, Nagaoka K. L-amino acid oxidase 1 in sperm is associated with reproductive performance in male mice and bulls. Biol Reprod. 2021;104(5):1154-61.
Zhang Y, Yuan W, Liu Y, Liu Y, Liang H, Xu Q, Liu Z, Weng X. Plasma membrane lipid composition and metabolomics analysis of Yorkshire boar sperms with high and low resistance to cryopreservation. Theriogenology. 2023;206:28-39.
Zhao Y, Qin J, Sun J, He J, Sun Y, Yuan R, Li Z. Motility-related microRNAs identified in pig seminal plasma exosomes by high-throughput small RNA sequencing. Theriogenology. 2024;215:351-60.
Zhu W, Zhang Y, Ren C, Cheng X, Chen J, Ge Z, Sun ZP, Zhuo X, Sun FF, Chen YL, Jia XJ, Zhang Z. Identification of proteomic markers for ram spermatozoa motility using a tandem mass tag (TMT) approach. J Proteomics. 2020;210:103438.
Zielińska A, Carreiró F, Oliveira AM, Neves A, Pires B, Nagasamy Venkatesh D, Durazzo A, Lucarini M, Eder P, Silva AM, Santini A, Souto EB. Polymeric nanoparticles: production, characterization, toxicology and ecotoxicology. Molecules. 2020;25(16):3731.
Submitted date:
03/16/2024
Accepted date:
06/20/2024