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Research Article

Differentiation of neonate mouse spermatogonial stem cells on three-dimensional agar/polyvinyl alcohol nanofiber scaffold

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Pages 202-215 | Received 18 Sep 2019, Accepted 26 Jan 2020, Published online: 06 Mar 2020

References

  • Abazari MF, Soleimanifar F, Nouri Aleagha M, Torabinejad S, Nasiri N, Khamisipour G, Amini Mahabadi J, Mahboudi H, Enderami SE, Saburi E, et al. 2018. PCL/PVA nanofibrous scaffold improve insulin-producing cells generation from human induced pluripotent stem cells. Gene. 671:50–57. Eng.
  • Abu Elhija M, Lunenfeld E, Schlatt S, Huleihel M. 2012. Differentiation of murine male germ cells to spermatozoa in a soft agar culture system. Asian J Androl. 14(2):285–293. eng.
  • Antoni D, Burckel H, Josset E, Noel G. 2015. Three-dimensional cell culture: a breakthrough in vivo. Int J Mol Sci. 16(3):5517–5527. Eng.
  • Aponte PM, van Bragt MP, de Rooij DG, van Pelt AM. 2005. Spermatogonial stem cells: characteristics and experimental possibilities. APMIS. 113(11–12):727–742. Eng.
  • Azadian E, Arjmand B, Ardeshirylajimi A, Hosseinzadeh S, Omidi M, Khojasteh A. 2019. Polyvinyl alcohol modified polyvinylidene fluoride-graphene oxide scaffold promotes osteogenic differentiation potential of human induced pluripotent stem cells. J Cell Biochem. Eng. 1–12
  • Azizollahi S, Aflatoonian R, Sadighi Gilani MA, Behnam B, Tajik N, Asghari-Jafarabadi M, Asgari HR, Koruji M. 2016. Alteration of spermatogenesis following spermatogonial stem cells transplantation in testicular torsion-detorsion mice. J Assist Reprod Genet. 33(6):771–781.
  • Barnes CJ, Distaso CT, Spitz KM, Verdun VA, Haramati A. 2016. Comparison of stem cell therapies for acute kidney injury. Am J Stem Cells. 5(1):1–10. Eng.
  • Bisig CG, Guiraldelli MF, Kouznetsova A, Scherthan H, Hoog C, Dawson DS, Pezza RJ. 2012. Synaptonemal complex components persist at centromeres and are required for homologous centromere pairing in mouse spermatocytes. PLoS Genet. 8(6):e1002701. Eng.
  • Boyer A, Yeh JR, Zhang X, Paquet M, Gaudin A, Nagano MC, Boerboom D. 2012. CTNNB1 signaling in sertoli cells downregulates spermatogonial stem cell activity via WNT4. PLoS One. 7(1):e29764. Eng.
  • Clermont Y, Bustos-Obregon E. 1968. Re-examination of spermatogonial renewal in the rat by means of seminiferous tubules mounted “in toto”. Am J Anat. 122(2):237–247. eng.
  • da Silva TN, Goncalves RP, Rocha CL, Archanjo BS, Barboza CAG, Pierre MBR, Reynaud F, de Souza Picciani PH. 2019. Controlling burst effect with PLA/PVA coaxial electrospun scaffolds loaded with BMP-2 for bone guided regeneration. Mater Sci Eng C Mater Biol Appl. 97:602–612. Eng.
  • Dan YY, Riehle KJ, Lazaro C, Teoh N, Haque J, Campbell JS, Fausto N. 2006. Isolation of multipotent progenitor cells from human fetal liver capable of differentiating into liver and mesenchymal lineages. Proc Natl Acad Sci U S A. 103(26):9912–9917. Eng.
  • de Michele F, Vermeulen M, Wyns C. 2017. Fertility restoration with spermatogonial stem cells. Curr Opin Endocrinol Diabetes Obes. 24(6):424–431. Eng.
  • Donnelly H, Salmeron-Sanchez M, Dalby MJ. 2018. Designing stem cell niches for differentiation and self-renewal. J R Soc Interface. 15(145):20180388.
  • Drumond AL, Meistrich ML, Chiarini-Garcia H. 2011. Spermatogonial morphology and kinetics during testis development in mice: a high-resolution light microscopy approach. Reproduction. 142(1):145–155. Eng.
  • Dym M, Kokkinaki M, He Z. 2009. Spermatogonial stem cells: mouse and human comparisons. Birth Defects Res C Embryo Today. 87(1):27–34. Eng.
  • Ehmcke J, Wistuba J, Schlatt S. 2006. Spermatogonial stem cells: questions, models and perspectives. Hum Reprod Update. 12(3):275–282. Eng.
  • Enayati MS, Behzad T, Sajkiewicz P, Rafienia M, Bagheri R, Ghasemi-Mobarakeh L, Kolbuk D, Pahlevanneshan Z, Bonakdar SH. 2018. Development of electrospun poly (vinyl alcohol)-based bionanocomposite scaffolds for bone tissue engineering. J Biomed Mater Res A. 106(4):1111–1120. Eng.
  • Enderami SE, Soleimani M, Mortazavi Y, Nadri S, Salimi A. 2018. Generation of insulin-producing cells from human adipose-derived mesenchymal stem cells on PVA scaffold by optimized differentiation protocol. J Cell Physiol. 233(5):4327–4337. Eng.
  • Entezam M, Daneshian H, Nasirizadeh N, Khonakdar HA, Jafari SH. 2017. Hybrid hydrogels based on Poly (vinyl alcohol)(PVA)/Agar/Poly (ethylene glycol)(PEG) prepared by high energy electron beam irradiation: investigation of physico‐mechanical and rheological properties. Macromol Mater Eng. 302(2):1600397.
  • Eslahi N, Hadjighassem MR, Joghataei MT, Mirzapour T, Bakhtiyari M, Shakeri M, Pirhajati V, Shirinbayan P, Koruji M. 2013. The effects of poly L-lactic acid nanofiber scaffold on mouse spermatogonial stem cell culture. Int J Nanomed. 8:4563–4576.
  • Fagoonee S, Pellicano R, Silengo L, Altruda F. 2011. Potential applications of germline cell-derived pluripotent stem cells in organ regeneration. Organogenesis. 7(2):116–122. Eng.
  • Fayomi AP, Orwig KE. 2018. Spermatogonial stem cells and spermatogenesis in mice, monkeys and men. Stem Cell Res. 29:207–214.
  • Forbes CM, Flannigan R, Schlegel PN. 2018. Spermatogonial stem cell transplantation and male infertility: current status and future directions. Arab J Urol. 16(1):171–180. Eng.
  • Gaaz TS, Sulong AB, Akhtar MN, Kadhum AA, Mohamad AB, Al-Amiery AA. 2015. Properties and applications of polyvinyl alcohol, halloysite nanotubes and their nanocomposites. Molecules. 20(12):22833–22847. Eng.
  • Ganjibakhsh M, Mehraein F, Koruji M, Aflatoonian R, Farzaneh P. 2019. Three-dimensional decellularized amnion membrane scaffold as a novel tool for cancer research; cell behavior, drug resistance and cancer stem cell content. Mater Sci Eng C Mater Biol Appl. 100:330–340.
  • Gao T, Jiang M, Liu X, You G, Wang W, Sun Z, Ma A, Chen J. 2019. Patterned polyvinyl alcohol hydrogel dressings with stem cells seeded for wound healing. Polymers (Basel). 11(1):171. Eng.
  • Gholami K, Pourmand G, Koruji M, Ashouri S, Abbasi M. 2018a. Organ culture of seminiferous tubules using a modified soft agar culture system. Stem Cell Res Ther. 9(1):249.
  • Gholami K, Pourmand G, Koruji M, Sadighigilani M, Navid S, Izadyar F, Abbasi M. 2018b. Efficiency of colony formation and differentiation of human spermatogenic cells in two different culture systems. Reprod Biol. 18(4):397–403.
  • Goossens E, Van Saen D, Tournaye H. 2013. Spermatogonial stem cell preservation and transplantation: from research to clinic. Hum Reprod. 28(4):897–907. Eng.
  • Grasso M, Fuso A, Dovere L, de Rooij DG, Stefanini M, Boitani C, Vicini E. 2012. Distribution of GFRA1-expressing spermatogonia in adult mouse testis. Reproduction. 143(3):325–332. Eng.
  • Greiner A, Wendorff JH. 2007. Electrospinning: a fascinating method for the preparation of ultrathin fibers. Angew Chem Int Ed Engl. 46(30):5670–5703. Eng.
  • Guo Y, Hai Y, Gong Y, Li Z, He Z. 2014. Characterization, isolation, and culture of mouse and human spermatogonial stem cells. J Cell Physiol. 229(4):407–413. Eng.
  • Hayashi M, Kawaguchi T, Durcova-Hills G, Imai H. 2018. Generation of germ cells from pluripotent stem cells in mammals. Reprod Med Biol. 17(2):107–114. Eng.
  • Helsel AR, Yang QE, Oatley MJ, Lord T, Sablitzky F, Oatley JM. 2017. ID4 levels dictate the stem cell state in mouse spermatogonia. Development. 144(4):624–634. Eng.
  • Hermann BP, Sukhwani M, Hansel MC, Orwig KE. 2010. Spermatogonial stem cells in higher primates: are there differences from those in rodents? Reproduction. 139(3):479–493. Eng.
  • Hermann BP, Sukhwani M, Winkler F, Pascarella JN, Peters KA, Sheng Y, Valli H, Rodriguez M, Ezzelarab M, Dargo G, et al. 2012. Spermatogonial stem cell transplantation into rhesus testes regenerates spermatogenesis producing functional sperm. Cell Stem Cell. 11(5):715–726. Eng
  • Higuchi A, Ling Q-D, Chang Y, Hsu S-T, Umezawa A. 2013. Physical cues of biomaterials guide stem cell differentiation fate. Chem Rev. 113(5):3297–3328.
  • Hofmann MC. 2008. Gdnf signaling pathways within the mammalian spermatogonial stem cell niche. Mol Cell Endocrinol. 288(1–2):95–103. Eng.
  • Iwamori N. 2014. Regulation of spermatogonial stem cell compartment in the mouse testis. Fukuoka Igaku Zasshi. 105(1):1–10. Eng.
  • Izadyar F, den Ouden K, Creemers LB, Posthuma G, Parvinen M, de Rooij DG. 2003. Proliferation and differentiation of bovine type A spermatogonia during long-term culture. Biol Reprod. 68(1):272–281.
  • Jiang X, Cao HQ, Shi LY, Ng SY, Stanton LW, Chew SY. 2012. Nanofiber topography and sustained biochemical signaling enhance human mesenchymal stem cell neural commitment. Acta Biomater. 8(3):1290–1302. Eng.
  • Kanatsu-Shinohara M, Shinohara T. 2013. Spermatogonial stem cell self-renewal and development. Annu Rev Cell Dev Biol. 29:163–187.
  • Khanehzad M, Abolhasani F, Koruji SM, Ragerdi Kashani I, Aliakbari F. 2016. The roles of sertoli cells in fate determinations of spermatogonial stem cells [Original Article]. Tehran Univ Med J. 73(12):878–887. eng %@ 1683-1764 %[2016.
  • Koruji M, Movahedin M, Mowla SJ, Gourabi H, Arfaee AJ. 2009. Efficiency of adult mouse spermatogonial stem cell colony formation under several culture conditions. In Vitro Cell Dev Biol Anim. 45(5–6):281–289. Eng.
  • Kostereva N, Hofmann MC. 2008. Regulation of the spermatogonial stem cell niche. Reprod Domest Anim. 43(Suppl 2):386–392. Eng.
  • Kubota H, Avarbock MR, Brinster RL. 2004a. Culture conditions and single growth factors affect fate determination of mouse spermatogonial stem cells. Biol Reprod. 71(3):722–731. Eng.
  • Kubota H, Avarbock MR, Brinster RL. 2004b. Growth factors essential for self-renewal and expansion of mouse spermatogonial stem cells. Proc Natl Acad Sci U S A. 101(47):16489–16494. Eng.
  • Larsson M, Norrander J, Graslund S, Brundell E, Linck R, Stahl S, Hoog C. 2000. The spatial and temporal expression of Tekt1, a mouse tektin C homologue, during spermatogenesis suggest that it is involved in the development of the sperm tail basal body and axoneme. Eur J Cell Biol. 79(10):718–725. Eng.
  • Lee WY, Park HJ, Lee R, Lee KH, Kim YH, Ryu BY, Kim NH, Kim JH, Moon SH, Park JK, et al. 2013. Establishment and in vitro culture of porcine spermatogonial germ cells in low temperature culture conditions. Stem Cell Res. 11(3):1234–1249. Eng
  • Li Y, Guo G, Li L, Chen F, Bao J, Shi YJ, Bu H. 2015. Three-dimensional spheroid culture of human umbilical cord mesenchymal stem cells promotes cell yield and stemness maintenance. Cell Tissue Res. 360(2):297–307. Eng.
  • Li Y, Wang X, Feng X, Liao S, Zhang D, Cui X, Gao F, Han C. 2014. Generation of male germ cells from mouse induced pluripotent stem cells in vitro. Stem Cell Res. 12(2):517–530. Eng.
  • Lim JJ, Kim HJ, Kim KS, Hong JY, Lee DR. 2013. In vitro culture-induced pluripotency of human spermatogonial stem cells. Biomed Res Int. 2013:143028. Eng.
  • Lin HS, Kuhn C, Kuo T. 1975. Clonal growth of hamster free alveolar cells in soft agar. J Exp Med. 142(4):877–886. Eng.
  • Mahmoud H. 2012. Concise review: spermatogenesis in an artificial three-dimensional system. Stem Cells. 30(11):2355–2360. Eng.
  • Mark M, Jacobs H, Oulad-Abdelghani M, Dennefeld C, Feret B, Vernet N, Codreanu CA, Chambon P, Ghyselinck NB. 2008. STRA8-deficient spermatocytes initiate, but fail to complete, meiosis and undergo premature chromosome condensation. J Cell Sci. 121(Pt19)):3233–3242. Eng.
  • Meng X, Lindahl M, Hyvonen ME, Parvinen M, de Rooij DG, Hess MW, Raatikainen-Ahokas A, Sainio K, Rauvala H, Lakso M, et al. 2000. Regulation of cell fate decision of undifferentiated spermatogonia by GDNF. Science (New York, NY). 287(5457):1489–1493. Eng
  • Miyamoto T, Minase G, Okabe K, Ueda H, Sengoku K. 2015. Male infertility and its genetic causes. J Obstet Gynaecol Res. 41(10):1501–1505. Eng.
  • Mohammadzadeh E, Mirzapour T, Nowroozi MR, Nazarian H, Piryaei A, Alipour F, Modarres Mousavi SM, Ghaffari Novin M. 2019. Differentiation of spermatogonial stem cells by soft agar three-dimensional culture system. Artif Cells Nanomed Biotechnol. 47(1):1772–1781. Eng.
  • Muduli S, Chen L-H, Li M-P, Heish Z-W, Liu C-H, Kumar S, Alarfaj AA, Munusamy MA, Benelli G, Murugan K. 2017. Stem cell culture on polyvinyl alcohol hydrogels having different elasticity and immobilized with ECM-derived oligopeptides. J Poly Eng. 37(7):647–660.
  • Navid S, Abbasi M, Hoshino Y. 2017. The effects of melatonin on colonization of neonate spermatogonial mouse stem cells in a three-dimensional soft agar culture system. Stem Cell Res Ther. 8(1):233. Eng.
  • Nur EKA, Ahmed I, Kamal J, Schindler M, Meiners S. 2006. Three-dimensional nanofibrillar surfaces promote self-renewal in mouse embryonic stem cells. Stem Cells. 24(2):426–433. Eng.
  • Oatley JM, Avarbock MR, Brinster RL. 2007. Glial cell line-derived neurotrophic factor regulation of genes essential for self-renewal of mouse spermatogonial stem cells is dependent on Src family kinase signaling. J Biol Chem. 282(35):25842–25851. Eng.
  • Oatley JM, Avarbock MR, Telaranta AI, Fearon DT, Brinster RL. 2006. Identifying genes important for spermatogonial stem cell self-renewal and survival. Proc Natl Acad Sci U S A. 103(25):9524–9529. Eng.
  • Oatley JM, Oatley MJ, Avarbock MR, Tobias JW, Brinster RL. 2009. Colony stimulating factor 1 is an extrinsic stimulator of mouse spermatogonial stem cell self-renewal. Development. 136(7):1191–1199. Eng.
  • Oatley MJ, Kaucher AV, Racicot KE, Oatley JM. 2011. Inhibitor of DNA binding 4 is expressed selectively by single spermatogonia in the male germline and regulates the self-renewal of spermatogonial stem cells in mice. Biol Reprod. 85(2):347–356. Eng.
  • Ojaghi M, Soleimanifar F, Kazemi A, Ghollasi M, Soleimani M, Nasoohi N, Enderami SE. 2019. Electrospun poly-l-lactic acid/polyvinyl alcohol nanofibers improved insulin-producing cell differentiation potential of human adipose-derived mesenchymal stem cells. J Cell Biochem. 120(6):9917–9926. Eng.
  • Park JE, Park MH, Kim MS, Park YR, Yun JI, Cheong HT, Kim M, Choi JH, Lee E, Lee ST. 2017. Porcine spermatogonial stem cells self-renew effectively in a three dimensional culture microenvironment. Cell Biol Int. 41(12):1316–1324. Eng.
  • Picton HM, Wyns C, Anderson RA, Goossens E, Jahnukainen K, Kliesch S, Mitchell RT, Pennings G, Rives N, Tournaye H, et al. 2015. A European perspective on testicular tissue cryopreservation for fertility preservation in prepubertal and adolescent boys. Hum Reprod. 30(11):2463–2475. Eng
  • Reda A, Hou M, Landreh L, Kjartansdottir KR, Svechnikov K, Soder O, Stukenborg JB. 2014. In vitro spermatogenesis - optimal culture conditions for testicular cell survival, germ cell differentiation, and steroidogenesis in rats. Front Endocrinol (Lausanne). 5:21. Eng.
  • Reda A, Hou M, Winton TR, Chapin RE, Soder O, Stukenborg JB. 2016. In vitro differentiation of rat spermatogonia into round spermatids in tissue culture. Mol Hum Reprod. 22(9):601–612. Eng.
  • Sankar S, Sharma CS, Rath SN, Ramakrishna S. 2017. Electrospun fibers for recruitment and differentiation of stem cells in regenerative medicine. Biotechnol J. 12(12):1700263.
  • Sato T, Katagiri K, Kubota Y, Ogawa T. 2013. In vitro sperm production from mouse spermatogonial stem cell lines using an organ culture method. Nat Protoc. 8(11):2098–2104. Eng.
  • Sato Y, Taniguchi M, Otoi T. 2012. Studying spermatogenesis by using in vivo and in vitro models: advantages and disadvantages of these models for practical use. J Vet Sci Technol. 3:3.
  • Shabani R, Ashtari K, Behnam B, Izadyar F, Asgari H, Asghari Jafarabadi M, Ashjari M, Asadi E, Koruji M. 2016. In vitro toxicity assay of cisplatin on mouse acute lymphoblastic leukaemia and spermatogonial stem cells. Andrologia. 48(5):584–594.
  • Shakeri M, Kohram H, Shahverdi A, Shahneh AZ, Tavakolifar F, Pirouz M, Shahrebabak HM, Koruji M, Baharvand H. 2013. Behavior of mouse spermatogonial stem-like cells on an electrospun nanofibrillar matrix. J Assist Reprod Genet. 30(3):325–332. Eng.
  • Shams A, Eslahi N, Movahedin M, Izadyar F, Asgari H, Koruji M. 2017. Future of spermatogonial stem cell culture: application of nanofiber scaffolds. Curr Stem Cell Res Ther. 12(7):544–553. eng.
  • Shetty G, Meistrich ML. 2007. The missing niche for spermatogonial stem cells: do blood vessels point the way? Cell Stem Cell. 1(4):361–363. Eng.
  • Simon L, Ekman GC, Tyagi G, Hess RA, Murphy KM, Cooke PS. 2007. Common and distinct factors regulate expression of mRNA for ETV5 and GDNF, Sertoli cell proteins essential for spermatogonial stem cell maintenance. Exp Cell Res. 313(14):3090–3099. Eng.
  • Sousa AM, Souza HK, Uknalis J, Liu SC, Goncalves MP, Liu L. 2015. Electrospinning of agar/PVA aqueous solutions and its relation with rheological properties. Carbohydr Polym. 115:348–355. Eng.
  • Stukenborg JB, Schlatt S, Simoni M, Yeung CH, Elhija MA, Luetjens CM, Huleihel M, Wistuba J. 2009. New horizons for in vitro spermatogenesis? An update on novel three-dimensional culture systems as tools for meiotic and post-meiotic differentiation of testicular germ cells. Mol Hum Reprod. 15(9):521–529. Eng.
  • Stukenborg JB, Wistuba J, Luetjens CM, Elhija MA, Huleihel M, Lunenfeld E, Gromoll J, Nieschlag E, Schlatt S. 2008. Coculture of spermatogonia with somatic cells in a novel three-dimensional soft-agar-culture-system. J Androl. 29(3):312–329. Eng.
  • Talebi A, Gilani MAS, Koruji M, Ai J, Rezaie MJ, Navid S, Salehi M, Abbasi MJGMJ. 2019. Colonization of mouse spermatogonial cells in modified soft agar culture system utilizing nanofibrous scaffold: a new approach. Galen Med J. 8. 1319.
  • Tegelenbosch RA, de Rooij DG. 1993. A quantitative study of spermatogonial multiplication and stem cell renewal in the C3H/101 F1 hybrid mouse. Mutat Res. 290(2):193–200. Eng.
  • Vacanti JP, Langer R. 1999. Tissue engineering: the design and fabrication of living replacement devices for surgical reconstruction and transplantation. Lancet. 354(Suppl 1):SI32–34. Eng.
  • van Pelt AM, Morena AR, van Dissel-emiliani FM, Boitani C, Gaemers IC, de Rooij DG, Stefanini M. 1996. Isolation of the synchronized A spermatogonia from adult vitamin A-deficient rat testes. Biol Reprod. 55(2):439–444. Eng.
  • Weaver VM, Petersen OW, Wang F, Larabell CA, Briand P, Damsky C, Bissell MJ. 1997. Reversion of the malignant phenotype of human breast cells in three-dimensional culture and in vivo by integrin blocking antibodies. J Cell Biol. 137(1):231–245. Eng.
  • Yamauchi K, Hasegawa K, Chuma S, Nakatsuji N, Suemori H. 2009. In vitro germ cell differentiation from cynomolgus monkey embryonic stem cells. PLoS One. 4(4):e5338. Eng.
  • Yoshida S. 2010. Stem cells in mammalian spermatogenesis. Dev Growth Differ. 52(3):311–317. Eng.
  • Yoshida S. 2012. Elucidating the identity and behavior of spermatogenic stem cells in the mouse testis. Reproduction. 144(3):293–302. Eng.
  • Yoshida S, Sukeno M, Nabeshima Y. 2007. A vasculature-associated niche for undifferentiated spermatogonia in the mouse testis. Science (New York, NY). 317(5845):1722–1726. Eng.
  • Zhang S. 2004. Beyond the Petri dish. Nat Biotechnol. 22(2):151–152. Eng.

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