Exploring the full potential of sperm function with nanotechnology tools

Kameni, Serge Leugoué; Dlamini, Notsile Hleliwe; Feugang, Jean Magloire

doi:10.1590/1984-3143-AR2024-0033

Serge Leugoué Kameni

Methodology

Writing-Editing

Mississippi State University, Department of Animal and Dairy Sciences, Mississippi State, MS, USA

https://orcid.org/0000-0001-5450-7518

Notsile Hleliwe Dlamini

Methodology

Writing-Editing

Mississippi State University, Department of Animal and Dairy Sciences, Mississippi State, MS, USA

https://orcid.org/0000-0003-3644-6576

Jean Magloire Feugang ^**Corresponding author: j.feugang@msstate.edu

Conceptualization

Supervision

Writing

Reviewing

Funding acquisition

Mississippi State University, Department of Animal and Dairy Sciences, Mississippi State, MS, USA

https://orcid.org/0000-0002-1376-5059

*Corresponding author: j.feugang@msstate.edu

Conflicts of interest: The authors have no conflict of interest to declare.

Figures (3)
Tables (2)

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Figure 1
Structure of a typical nanoparticle. Metal nanoparticles (MNPs) have a metal core and a shell. The core can be made of an inorganic metal (zinc, iron, silver, gold, etc.) or metal oxide (Aluminum, copper, magnesium, titanium, zinc, silica, iron oxides, etc.). The shell can be made of an organic (e.g., polymers) or inorganic material (e.g., gold), or metal oxide (e.g., silane). Nanoparticles made of metallic cores surrounded by oxide shells, also known as metal oxide core-shell nanoparticles, have become popular due to their unique properties and high stability. Diverse metal-oxide interactions in metal oxide core-shell nanoparticles enable tuning their electronic structure (shape and size), spectroscopic properties, and surface reactivity for bioapplications (e.g., sensing, drug/gene delivery, and targeted imaging and selection).

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Figure 2
Overview of commonly used inorganic and organic nanoparticles. The presented inorganic nanoparticles can be coated with single or multiple layers of organic or inorganic materials before biofunctionalization for bioapplications. Among the organic nanoparticles, liposomes are the most widely used for bioapplications, such as targeted bioimaging, drug delivery (hydrophobic and hydrophilic), and drug and nucleic acid intracellular delivery. The possibility of coating the external surface of nanoparticles with polyethylene glycol (PEG), or PEGylation, increases nanoparticle’s stability and decreases immunogenicity during in vivo delivery.

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Figure 3
Schematic representation of a biofunctionalized nanoparticle. Ready-to-use nanoparticles for bioapplications include a (nano)core surrounded by single or multiple coating layers providing stability and decreasing immunogenicity and an outer surface layer functionalized based on planned unimodal (e.g., imaging) or multimodal (e.g., imaging and drug administration) applications.

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Table 1
Candidate biomarkers of sperm phenotypes for nanotechnology applications.

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Table 2
Examples of nanoparticles for sperm manipulation.

Phenotype	Sources	Biomarker candidates	Animals	References
Motility	Sperm	Proteins:	Rams	Zhu et al. (2020)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. http://doi.org/10.1016/j.jprot.2019.103438. PMid:31271902. http://doi.org/10.1016/j.jprot.2019.1034...
		Phosphatidylethanolamine binding protein 4, Spermatogenesis associated 18, Carboxypeptidase, Acrosin	Rams
		Proteins:	Horses	Gaitskell-Phillips et al. (2021a)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. http://doi.org/10.1093/biolre/ioab003. PMid:33438027. http://doi.org/10.1093/biolre/ioab003...
		Mannosidase alpha class 2C member 1, Ubiquinone 1 alpha sucomplex subunit 9-like protein, isoleucyl-tRNA synthetase2, mitochondrial acethyl-CoA acetyl transferase 1, Latherin, Ubiquitin-specific peptidase 43	Horses
		Proteins:	Horses	Gaitskell-Phillips et al. (2021b)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. http://doi.org/10.1016/j.jprot.2021.104335. PMid:34298182. http://doi.org/10.1016/j.jprot.2021.1043...
		Hexokinase 1, Aconitase hydratase mitochondrial, Phosphoinositide phospholipase C, Elongation factor Tu, F actin capping protein subunit alpha	Horses
		Metabolites:	Bucks	Yuan et al. (2023a)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. http://doi.org/10.1016/j.theriogenology.2023.07.009. PMid:37473596. http://doi.org/10.1016/j.theriogenology....
		Butyric acid, 1-(2-Methoxy-13-methyl-pentadecanyl)-sn-glycero-3-phosphoetanolamine, 2-O-benzoyl-D-glucose, Trehalulose, Glutamylphenylalanine, Vulgaxanthin-I	Bucks
		Transcripts:	Bulls	Ganguly et al. (2013)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. http://doi.org/10.1016/j.rvsc.2012.09.001. PMid:23044178. http://doi.org/10.1016/j.rvsc.2012.09.00...
		PRM1 mRNAs	Bulls
Liquid preservation ability/Freezability		Proteins: NUDFB8, SDHC, PDIA4, HSPB1	Bucks	Sun et al. (2023)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. http://doi.org/10.3390/ijms242115550. PMid:37958534. http://doi.org/10.3390/ijms242115550...
		Proteins:	Boars	Song et al. (2024)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. http://doi.org/10.1016/j.theriogenology.2023.11.017. PMid:38029685. http://doi.org/10.1016/j.theriogenology....
		GPX5, GLRX, ENO4, QPCT, BBS7, OXR1, DHRS4, AP2S1	Boars
		Metabolites:	Boars	Zhang et al. (2023)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. http://doi.org/10.1016/j.theriogenology.2023.04.016. PMid:37178672. http://doi.org/10.1016/j.theriogenology....
		Oleic acid, Oleamide, N8-acetylspermidine	Boars
		Metabolites:	Boars	Torres et al. (2022)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. http://doi.org/10.1093/biolre/ioab200. PMid:34725678. http://doi.org/10.1093/biolre/ioab200...
		Inosine, Hypoxanthine, Creatine, ADP, Niacinamide, Spermine, 2-methylbutyrylcarnitine	Boars
		Metabolites:	Boars	Sui et al. (2023)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. http://doi.org/10.1016/j.theriogenology.2022.11.013. PMid:36401936. http://doi.org/10.1016/j.theriogenology....
		L-citruline	Boars
		Transcripts:	Boars	Fraser et al. (2020)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. http://doi.org/10.1016/j.theriogenology.2019.11.001. PMid:31711689. http://doi.org/10.1016/j.theriogenology....
		FOS, NFATC3, EAF2, BAMBI, PTPRU, PTPN2, ND6, ACADM,	Boars
Fertility		Proteins: Calmodulin,	Bulls	Soggiu et al. (2013)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. http://doi.org/10.1039/c3mb25494a. PMid:23392320. http://doi.org/10.1039/c3mb25494a...
		ATP synthase mitochondrial subunits alpha and delta, Malate dehydrogenase and Sperm equatorial segment protein 1	Bulls
		Proteins:	Boars	Kwon et al. (2015)Kwon W, Rahman S, Ryu D, Park Y, Pang M. Increased male fertility using fertility-related biomarkers. Sci Rep. 2015;5(1):15654. http://doi.org/10.1038/srep15654. PMid:26489431. http://doi.org/10.1038/srep15654...
		Ras-related protein Rab-2A, Cytochrome b-c1 complex subunit 1, Cytochrome b-c1 complex subunit 2	Boars
		Proteins: Acyl-CoA thioesterase 9, Albumin, Casein kinase 2, K voltage-gated channel shaker-related	Bulls	Peddinti et al. (2008)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. http://doi.org/10.1186/1752-0509-2-19. PMid:18294385. http://doi.org/10.1186/1752-0509-2-19...
		Proteins:	Bulls	Zhang et al. (2021)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. http://doi.org/10.1093/biolre/ioab024. PMid:33590844. http://doi.org/10.1093/biolre/ioab024...
		L amino acid oxidase 1	Bulls
		Metabolites:	Bulls	Menezes et al. (2019)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. http://doi.org/10.1186/s12864-019-6074-6. PMid:31533629. http://doi.org/10.1186/s12864-019-6074-6...
		Gamma-aminobutyric acid, Carbamate, Benzoic acid, Lactic acid, Palmitic acid	Bulls
		Metabolites:	Bulls	DasGupta et al. (2021)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. http://doi.org/10.1071/RD20304. PMid:33775276. http://doi.org/10.1071/RD20304...
		Taurine, Hypotaurine	Bulls
		Transcripts:	Bulls	Lalancette et al. (2008)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. http://doi.org/10.1095/biolreprod.106.059030. PMid:18003951. http://doi.org/10.1095/biolreprod.106.05...
		rRNA genes (18S, 12S, and Large chain R)	Bulls
Mitochondrial activity		Proteins:	Stallions	Gaitskell-Phillips et al. (2021b)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. http://doi.org/10.1016/j.jprot.2021.104335. PMid:34298182. http://doi.org/10.1016/j.jprot.2021.1043...
Mitochondrial activity		Phosphoglycerate mutase, peroxiredoxin 6-like proteins, actin-1 analogue, transmembrane protein analogue	Stallions
Viability		Chaperonin TCP1 subunit 8, Testis expressed 101	Stallions
Motility	Seminal plasma	Proteins:	Bucks	Jia et al. (2021)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. http://doi.org/10.1038/s41598-021-95138-9. PMid:34330982. http://doi.org/10.1038/s41598-021-95138-...
		Zonadhesin, Superoxide dismutase, Sperm equatorial segment protein 1, Mitochondrial thioredoxin reductase, Zona pellucida binding protein, Aquaporin 7	Bucks
		Metabolites:
		Thioetheramide-PC, Adenosine, N,N-Dimethylguanosine, Isocitric acid
		Transcripts:	Boars	Zhao et al. (2024)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. http://doi.org/10.1016/j.theriogenology.2023.11.028. PMid:38150851. http://doi.org/10.1016/j.theriogenology....
		miRNAs (ssc-miR-
		122–5p, ssc-miR-486, ssc-miR-451, ssc-miR-345–3p, ssc-miR-362, and ssc-miR-500–5p)
Liquid preservation ability/Freezability		Metabolites:	Bulls	Pessoa et al. (2023)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. http://doi.org/10.1111/rda.14453. PMid:37592767. http://doi.org/10.1111/rda.14453...
		Propanoic acid, D-ribose, glycine	Bulls
		Metabolites:	Boars	Song et al. (2023)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. http://doi.org/10.1093/jas/skad392. http://doi.org/10.1093/jas/skad392...
		D-proline, Arginine, L-citruline, Phenylalanine, Leucine, DL-proline, DL-serine, Indole	Boars
		Metabolites:	Boars	Sui et al. (2023)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. http://doi.org/10.1016/j.theriogenology.2022.11.013. PMid:36401936. http://doi.org/10.1016/j.theriogenology....
		Tryptophan	Boars
Fertility		Proteins:	Boars	Zeng et al. (2021)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. http://doi.org/10.1016/j.jprot.2021.104120. PMid:33540064. http://doi.org/10.1016/j.jprot.2021.1041...
Fertility		Ceruloplasmin, Carboxypeptidase E, Serine protease inhibitor family A member 12	Boars

Nanoparticles				Biological applications	References
Classes	Types	Shape	Size (nm)	Biological applications	References
Organic	Liposomes	Sphere	50-500	Active tumor targeting, drug gene delivery, intracellular delivery, sperm cryopreservation.	Röpke et al. (2011)Röpke T, Oldenhof H, Leiding C, Sieme H, Bollwein H, Wolkers WF. Liposomes for cryopreservation of bovine sperm. Theriogenology. 2011;76(8):1465-72. http://doi.org/10.1016/j.theriogenology.2011.06.015. PMid:21820724. http://doi.org/10.1016/j.theriogenology.... ; Deshpande et al. (2013)Deshpande PP, Biswas S, Torchilin VP. Current trends in the use of liposomes for tumor targeting. Nanomedicine (Lond). 2013;8(9):1509-28. http://doi.org/10.2217/nnm.13.118. PMid:23914966. http://doi.org/10.2217/nnm.13.118... ; Mo et al. (2014)Mo R, Jiang T, Gu Z. Recent progress in multidrug delivery to cancer cells by liposomes. Nanomedicine (Lond). 2014;9(8):1117-20. http://doi.org/10.2217/nnm.14.62. PMid:25118703. http://doi.org/10.2217/nnm.14.62... ; Ansari et al. (2016)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. http://doi.org/10.1016/j.theriogenology.2015.09.035. PMid:26522702. http://doi.org/10.1016/j.theriogenology.... ; Feugang et al. (2022)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. http://doi.org/10.1016/j.theriogenology.2022.08.032. PMid:36099803. http://doi.org/10.1016/j.theriogenology....
	Exosomes	Sphere	40 to 120	Sperm function, immune response, cancer therapy, drug delivery	Montecalvo et al. (2012)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. http://doi.org/10.1182/blood-2011-02-338004. PMid:22031862. http://doi.org/10.1182/blood-2011-02-338... ; Du et al. (2016)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. http://doi.org/10.18632/oncotarget.11315. PMid:27542209. http://doi.org/10.18632/oncotarget.11315... ; Fitts et al. (2019)Fitts CA, Ji N, Li Y, Tan C. Exploiting exosomes in cancer liquid biopsies and drug delivery. Adv Healthc Mater. 2019;8(6):e1801268. http://doi.org/10.1002/adhm.201801268. PMid:30663276. http://doi.org/10.1002/adhm.201801268...
	Carbon-based: Single-walled (SWCNT)/Multi-walled (MWNT)	Nanotubes	1-200	Gene delivery, sensing, pathogenicity, oxidative stress, inflammation	Donaldson et al. (2006)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. http://doi.org/10.1093/toxsci/kfj130. PMid:16484287. http://doi.org/10.1093/toxsci/kfj130... ; Donaldson and Tran (2002)Donaldson K, Tran CL. Inflammation caused by particles and fibers. Inhal Toxicol. 2002;14(1):5-27. http://doi.org/10.1080/089583701753338613. PMid:12122558. http://doi.org/10.1080/08958370175333861...
	Polymeric: Nanocapsules/nanospheres (polylactides, polylactide-co-glycolide, chitosan, albumin, gelatin)	Sphere	1-1000	Drug delivery, theragnostics, bioimaging	Szczęch and Szczepanowicz (2020)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. http://doi.org/10.3390/nano10030496. PMid:32164194. http://doi.org/10.3390/nano10030496... ; Zielińska et al. (2020)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. http://doi.org/10.3390/molecules25163731. PMid:32824172. http://doi.org/10.3390/molecules25163731...
Inorganic	Metal nanoparticles: e.g. Gold (Au)	Sphere	2-250	Biomedical imaging, photothermal therapy	Paciotti et al. (2006)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. http://doi.org/10.1002/ddr.20066. http://doi.org/10.1002/ddr.20066... ; Yang et al. (2019)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. http://doi.org/10.1016/j.susmat.2019.e00109. http://doi.org/10.1016/j.susmat.2019.e00...
	Metal oxide nanoparticles: e.g. Fe₂O_3, CeO₂	Sphere	15-60	Sperm nanopurification, drug delivery vehicles, thermal-based therapy, sperm bio-imaging	Feugang et al. (2015ª); Falchi et al. (2018a)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. http://doi.org/10.1186/s12958-018-0339-9. PMid:29510737. http://doi.org/10.1186/s12958-018-0339-9... ; Arias et al. (2018)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. http://doi.org/10.3390/antibiotics7020046. PMid:29890753. http://doi.org/10.3390/antibiotics702004...
	Non-metal oxide nanoparticles: e.g. Silica (Si)	Sphere	40-100	Purification, gene and drug delivery, biomedical imaging	Wang et al. (2008)Wang L, Zhao W, Tan W. Bioconjugated silica nanoparticles: development and applications. Nano Res. 2008;1(2):99-115. http://doi.org/10.1007/s12274-008-8018-3. http://doi.org/10.1007/s12274-008-8018-3... ; Xu et al. (2019)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. http://doi.org/10.1021/acsnano.9b06691. PMid:31556987. http://doi.org/10.1021/acsnano.9b06691...
	Quantum dots	Sphere	1-10	Drug delivery, photodynamic therapy, biomedical imaging, biosensing	Kim et al. (2004)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. http://doi.org/10.1038/nbt920. PMid:14661026. http://doi.org/10.1038/nbt920... ; Weng and Ren (2006)Weng J, Ren J. Luminescent Quantum Dots: A Very Attractive and Promising Tool in Biomedicine. Curr Med Chem. 2006;13(8):897-909. http://doi.org/10.2174/092986706776361076. PMid:16611074. http://doi.org/10.2174/09298670677636107... ; Bera et al. (2010)Bera D, Qian L, Tseng TK, Holloway PH. Quantum dots and their multimodal applications: a review. Materials (Basel). 2010;3(4):2260-345. http://doi.org/10.3390/ma3042260. http://doi.org/10.3390/ma3042260... ; Feugang et al. (2012)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. http://doi.org/10.1186/1477-3155-10-45. PMid:23241497. http://doi.org/10.1186/1477-3155-10-45...

[1] *Corresponding author: j.feugang@msstate.edu

Brasil

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Exploring the full potential of sperm function with nanotechnology tools

Abstract