Hyaluronic acid/silicon nanoparticle scaffold induces proliferation and differentiation of mouse spermatogonial stem cells transplanted to epididymal adipose tissue.

Hyaluronic acid Silicon nanoparticle Spermatogenesis Spermatogonia stem cell

Journal

Cell and tissue banking
ISSN: 1573-6814
Titre abrégé: Cell Tissue Bank
Pays: Netherlands
ID NLM: 100965121

Informations de publication

Date de publication:
07 Sep 2023
Historique:
received: 31 10 2022
accepted: 18 04 2023
medline: 7 9 2023
pubmed: 7 9 2023
entrez: 7 9 2023
Statut: aheadofprint

Résumé

Spermatogonia stem cells (SSCs) are a unique cell population maintaining male spermatogenesis during life, through their potential for proliferation and differentiation. The application of silicon nanoparticles (SNs) and hyaluronic acid (HA) to induce the differentiation of SSCs seems promising. Herein, we investigate the effect of SN and HA scaffolds on the progression of SSCs spermatogenesis in mice. Initially SSCs were isolated from healthy immature mice and cultured on prepared scaffolds (HA, SN, and HA/SN) in a 3D culture system. Then viability of SSCs cultured on scaffolds was examined using MTT assay and Acridine Orange staining. Then SSCs cultured on scaffolds were transplanted into epididymal adipose tissue (EAT) in mature mice and the result was studied by H&E and IHC staining 8 weeks after transplantation. MTT and Acridine Orange analysis revealed that among three different scaffolds HA/SN based scaffold causes considerable toxicity on SSCs (P < 0.05) while H&E staining showed that culture of SSCs on HA, SN, and HA/SN scaffolds has a positive effect on the progression of SSCs spermatogenesis after transplantation into EAT. IHC staining identified TP1, TEKT1, and PLZF as crucial biomarkers in the spermatogenesis development of SSCs transplanted to EAT. According to the presence of these biomarkers in different experimental groups, we found the most spermatogenesis development in SSCs cultured on HA/SN scaffold (PLZF, P < 0.01) (TEKT1, P < 0.01) (TP1, P < 0.001). Our study showed that, although the cytotoxic effect of the HA/SN scaffold decreases the viability rate of SSCs; however, SSCs that survive on HA/SN scaffold showed more ability to progress in spermatogenesis after transplantation into EAT.

Identifiants

pubmed: 37676366
doi: 10.1007/s10561-023-10093-1
pii: 10.1007/s10561-023-10093-1
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2023. The Author(s), under exclusive licence to Springer Nature B.V.

Références

Abatangelo G, Vindigni V, Avruscio G, Pandis L, Brun P (2020) Hyaluronic acid: redefining its role. Cells 9(7):1743
doi: 10.3390/cells9071743 pubmed: 32708202 pmcid: 7409253
Abdul Aziz MY, Omar AR, Subramani T, Yeap SK, Ho WY, Ismail NH, Alitheen NB (2014) Damnacanthal is a potent inducer of apoptosis with anticancer activity by stimulating p53 and p21 genes in MCF-7 breast cancer cells. Oncol Lett 7(5):1479–1484
doi: 10.3892/ol.2014.1898
Abeer MM, Rewatkar P, Qu Z, Talekar M, Kleitz F, Schmid R, Popat A (2020) Silica nanoparticles: a promising platform for enhanced oral delivery of macromolecules. J Controll Release 326:544–555
doi: 10.1016/j.jconrel.2020.07.021
Alrahel A, Movahedin M, Mazaheri Z, Amidi F (2018) Study of Tnp1, Tekt1, and Plzf genes expression during an in vitro three-dimensional neonatal male mice testis culture. Iran Biomed J 22(4):258
doi: 10.29252/ibj.22.4.258 pubmed: 29397043 pmcid: 5949128
Anjam RS, Movahedin M, Pourbeyranvand S, Moula SJ (2007) Assessment of morphological and functional changes in the mouse testis and epididymal sperms following busulfan treatment.
Chalkley H (1943) Method for the quantitative morphologic analysis of tissues. J Natl Cancer Inst 4(1):47–53
Costoya JA, Hobbs RM, Barna M, Cattoretti G, Manova K, Sukhwani M, Pandolfi PP (2004) Essential role of Plzf in maintenance of spermatogonial stem cells. Nat Genet 36(6):653–659
doi: 10.1038/ng1367 pubmed: 15156143
Geng X, Liu B, Liu J, Liu D, Lu Y, Sun X, Kong B (2018) Interfacial tissue engineering of heart regenerative medicine based on soft cell-porous scaffolds. J Thorac Disease 10(Suppl 20):S2333
doi: 10.21037/jtd.2018.01.117
Gisbert-Garzarán M, Lozano D, Vallet-Regí M (2020) Mesoporous silica nanoparticles for targeting subcellular organelles. Int J Mol Sci 21(24):9696
doi: 10.3390/ijms21249696 pubmed: 33353212 pmcid: 7766291
Guo C, Liu Y, Li Y (2021) Adverse effects of amorphous silica nanoparticles: focus on human cardiovascular health. J Hazard Mater 406:124626
doi: 10.1016/j.jhazmat.2020.124626 pubmed: 33296760
Hosseinabadi M, Abdolmaleki Z, Beheshtiha SHS (2021) Cardiac aorta-derived extracellular matrix scaffold enhances critical mediators of angiogenesis in isoproterenol-induced myocardial infarction mice. J Mater Sci Mater Med 32(11):1–10
doi: 10.1007/s10856-021-06611-w
Huang R, Shen YW, Guan YY, Jiang YX, Wu Y, Rahman K, Zhang LJ, Liu HJ, Luan X (2020) Mesoporous silica nanoparticles: facile surface functionalization and versatile biomedical applications in oncology. Acta Biomater 116:1–15
doi: 10.1016/j.actbio.2020.09.009 pubmed: 32911102
Jahnukainen K, Stukenborg J-B (2012) Present and future prospects of male fertility preservation for children and adolescents. J Clin Endocrinol Metab 97(12):4341–4351
doi: 10.1210/jc.2012-3065 pubmed: 23038680
Koruji M, Movahedin M, Mowla SJ, Gourabi H, Pour-Beiranvand S, Arfaee AJ (2012) Autologous transplantation of adult mice spermatogonial stem cells into gamma irradiated testes. Cell J 14(2):82
pubmed: 23507977 pmcid: 3584422
Liu X-H, Xue S, Ma J-Z (2020) Mesoporous silica nanoparticles for bone tissue engineering. Zhongguo Gu Shang= China J Orthop Traumatol 33(8):784–787
Ma L, Song X, Yu Y, Chen Y (2021) Two-dimensional Silicene/silicon Nanosheets: an emerging silicon-composed nanostructure in biomedicine. Adv Mater 33(31):2008226
doi: 10.1002/adma.202008226
Majidi Gharenaz N, Movahedin M, Majidi S, Mazaheri Z (2020) A review on application of three dimensional culture and testicular scaffolds to induction of in-vitro spermatogenesis. SSU J 28(7):2794–2805
Medina-Reyes EI, Rodríguez-Ibarra C, Déciga-Alcaraz A, Díaz-Urbina D, Chirino YI, Pedraza-Chaverri J (2020) Food additives containing nanoparticles induce gastrotoxicity, hepatotoxicity and alterations in animal behavior: The unknown role of oxidative stress. Food Chem Toxicol 146:111814
doi: 10.1016/j.fct.2020.111814 pubmed: 33068655
Mohand-Kaci F, Assoul N, Martelly I, Allaire E, Zidi M (2013) Optimized hyaluronic acid–hydrogel design and culture conditions for preservation of mesenchymal stem cell properties. Tissue Eng Part C Methods 19(4):288–298
doi: 10.1089/ten.tec.2012.0144 pubmed: 22992013
Mohaqiq M, Movahedin M, Mazaheri Z, Amirjannati N (2019) In vitro transplantation of spermatogonial stem cells isolated from human frozen–thawed testis tissue can induce spermatogenesis under 3-dimensional tissue culture conditions. Biol Res 52(1):1–9
doi: 10.1186/s40659-019-0223-x
Molgaard-Hansen L, Glosli H, Jahnukainen K, Jarfelt M, Jónmundsson GK, Malmros-Svennilson J (2011) Quality of health in survivors of childhood acute myeloid leukemia treated with chemotherapy only: a NOPHO-AML study. Pediatric Blood Cancer 57(7):1222–1229
doi: 10.1002/pbc.22931 pubmed: 22095929
Nishimura H, L’Hernault SW (2017) Spermatogenesis. Curr Biol 27(18):R988–R994
doi: 10.1016/j.cub.2017.07.067 pubmed: 28950090
Park J-Y, DiPalma DT, Kwon J, Fink J, Park J-H (2019) Quantitative difference in PLZF protein expression determines iNKT lineage fate and controls innate CD8 T cell generation. Cell Rep 27(9):2548-2557. e2544
doi: 10.1016/j.celrep.2019.05.012 pubmed: 31141681 pmcid: 8274958
Pereira H, Sousa DA, Cunha A, Andrade R, Espregueira-Mendes J, Oliveira JM, Reis RL (2018) Hyaluronic acid. Osteochondral Tissue Eng 137–153
Reda A, Hou M, Landreh L, Kjartansdóttir KR, Svechnikov K, Söder O, Stukenborg J-B (2014) In vitro spermatogenesis–optimal culture conditions for testicular cell survival, germ cell differentiation, and steroidogenesis in rats. Front Endocrinol 5:21
doi: 10.3389/fendo.2014.00021
Sharma N, Jha S (2020) Amorphous nanosilica induced toxicity, inflammation and innate immune responses: a critical review. Toxicology 441:152519
doi: 10.1016/j.tox.2020.152519 pubmed: 32525085
Skakkebaek NE (2017). Sperm counts, testicular cancers, and the environment: British Medical Journal Publishing Group.
Xu Y, Wang N, Yu Y, Li Y, Li Y-B, Yu Y-B, Sun Z-W (2014) Exposure to silica nanoparticles causes reversible damage of the spermatogenic process in mice. PLoS ONE 9(7):e101572
doi: 10.1371/journal.pone.0101572 pubmed: 25003337 pmcid: 4086902
Yang Y, Lin Q, Zhou C, Li Q, Li Z, Cao Z, Zhang Q (2020) A testis-derived hydrogel as an efficient feeder-free culture platform to promote mouse spermatogonial stem cell proliferation and differentiation. Front Cell Dev Biol 8:250
doi: 10.3389/fcell.2020.00250 pubmed: 32509769 pmcid: 7248195
Zhao M, Shirley CR, Mounsey S, Meistrich ML (2004) Nucleoprotein transitions during spermiogenesis in mice with transition nuclear protein Tnp1 and Tnp2 mutations. Biol Reprod 71(3):1016–1025
doi: 10.1095/biolreprod.104.028191 pubmed: 15163613

Auteurs

Saber Saharkhiz (S)

Department of cellular and Molecular medicine, Faculty of Medicine, University of Ottawa, Ottawa, Canada.

Zohreh Abdolmaleki (Z)

Department of Pharmacology, Karaj Branch, Islamic Azad University, Karaj, Iran.

Mohammad Amin Eslampour (MA)

Department of Clinical Sciences, Faculty of Veterinary Medicine, Science and Research Branch, Islamic Azad University, Tehran, Iran. maeslampour@srbiau.ac.ir.

Classifications MeSH