Cell-Based Therapy Approaches in Treatment of Non-obstructive Azoospermia.
Cell therapy
Inflammation
Non-obstructive azoospermia
Paracrine effect
Regenerative medicine
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:
05 2023
05 2023
Historique:
received:
15
08
2022
accepted:
20
10
2022
medline:
8
5
2023
pubmed:
16
11
2022
entrez:
15
11
2022
Statut:
ppublish
Résumé
The rate of infertility has globally increased in recent years for a variety of reasons. One of the main causes of infertility in men is azoospermia that is defined by the absence of sperm in the ejaculate and classified into two categories: obstructive azoospermia and non-obstructive azoospermia. In non-obstructive azoospermia, genital ducts are not obstructed, but the testicles do not produce sperm at all, due to various reasons. Non-obstructive azoospermia in most cases has no therapeutic options other than assisted reproductive techniques, which in most cases require sperm donors. Here we discuss cell-based therapy approaches to restore fertility in men with non-obstructive azoospermia including cell-based therapies of non-obstructive azoospermia using regenerative medicine and cell-based therapies of non-obstructive azoospermia by paracrine and anti-inflammatory pathway, technical and ethical challenges for using different cell sources and alternative options will be described, and then the more effectual approaches will be mentioned as future trends.
Identifiants
pubmed: 36380137
doi: 10.1007/s43032-022-01115-6
pii: 10.1007/s43032-022-01115-6
pmc: PMC9666961
doi:
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
1482-1494Informations de copyright
© 2022. The Author(s), under exclusive licence to Society for Reproductive Investigation.
Références
Berookhim BM, Schlegel PN. Azoospermia due to spermatogenic failure. Urol Clin. 2014;41:97–113.
doi: 10.1016/j.ucl.2013.08.004
Jarow JP, Espeland MA, Lipshultz LI. Evaluation of the azoospermic patient. J Urol. 1989;142:62–5.
pubmed: 2499695
doi: 10.1016/S0022-5347(17)38662-7
Alkandari MH, Zini A. Medical management of non-obstructive azoospermia: a systematic review. Arab J Urol. 2021;19:215–20.
pubmed: 34552772
pmcid: 8451648
doi: 10.1080/2090598X.2021.1956233
Vij SC, Sabanegh E Jr, Agarwal A. Biological therapy for non-obstructive azoospermia. Expert Opin Biol Ther. 2018;18:19–23.
pubmed: 28927307
doi: 10.1080/14712598.2018.1380622
Bucay N, Yebra M, Cirulli V, Afrikanova I, Kaido T, Hayek A, et al. A novel approach for the derivation of putative primordial germ cells and sertoli cells from human embryonic stem cells. Stem cells. 2009;27:68–77.
pubmed: 18845765
doi: 10.1634/stemcells.2007-1018
Yang W, Mills JA, Sullivan S, Liu Y, French DL, Gadue P. iPSC reprogramming from human peripheral blood using Sendai virus mediated gene transfer. 2012; In: StemBook [Internet]. Cambridge (MA): Harvard Stem Cell Institute; 2008–. PMID: 23785736.
Nayernia K, Nolte J, Michelmann HW, Lee JH, Rathsack K, Drusenheimer N, et al. In vitro-differentiated embryonic stem cells give rise to male gametes that can generate offspring mice. Dev Cell. 2006;11:125–32.
pubmed: 16824959
doi: 10.1016/j.devcel.2006.05.010
Lim J, Sung SY, Kim H, Song SH, Hong J, Yoon T, et al. Long-term proliferation and characterization of human spermatogonial stem cells obtained from obstructive and non-obstructive azoospermia under exogenous feeder-free culture conditions. Cell Prolif. 2010;43:405–17.
pubmed: 20590666
pmcid: 6495878
doi: 10.1111/j.1365-2184.2010.00691.x
Marc Luetjens C, Stukenborg J-B, Nieschlag E, Simoni M, Wistuba J. Complete spermatogenesis in orthotopic but not in ectopic transplants of autologously grafted marmoset testicular tissue. Endocrinology. 2008;149:1736–47.
pubmed: 18174281
doi: 10.1210/en.2007-1325
Goossens E, Van Saen D, Tournaye H. Spermatogonial stem cell preservation and transplantation: from research to clinic. Human Reproduction. 2013;28: 897–907.
Keros V, Rosenlund B, Hultenby K, Aghajanova L, Levkov L, Hovatta O. Optimizing cryopreservation of human testicular tissue: comparison of protocols with glycerol, propanediol and dimethylsulphoxide as cryoprotectants. Hum Reprod. 2005;20:1676–87.
pubmed: 15860503
doi: 10.1093/humrep/deh797
Gul M, Hildorf S, Dong L, Thorup J, Hoffmann ER, Jensen CFS, et al. Review of injection techniques for spermatogonial stem cell transplantation. Hum Reprod Update. 2020;26:368–91.
pubmed: 32163572
doi: 10.1093/humupd/dmaa003
Hermann B, Sukhwani M, Winkler F, Pascarella J, Peters K, Sheng Y, et al. Spermatogonial stem cell transplantation into rhesus testes regenerates spermatogenesis producing functional sperm. Cell Stem Cell. 2012;11:715–26.
pubmed: 23122294
pmcid: 3580057
doi: 10.1016/j.stem.2012.07.017
Toyooka Y, Tsunekawa N, Akasu R, Noce T. Embryonic stem cells can form germ cells in vitro. Proc Natl Acad Sci. 2003;100:11457–62.
pubmed: 14504407
pmcid: 208779
doi: 10.1073/pnas.1932826100
Geijsen N, Horoschak M, Kim K, Gribnau J, Eggan K, Daley GQ. Derivation of embryonic germ cells and male gametes from embryonic stem cells. Nature. 2004;427:148–54.
pubmed: 14668819
doi: 10.1038/nature02247
West JA, Park I-H, Daley GQ, Geijsen N. In vitro generation of germ cells from murine embryonic stem cells. Nat Protoc. 2006;1:2026–36.
pubmed: 17487192
doi: 10.1038/nprot.2006.303
Kerkis A, Fonseca SA, Serafim RC, Lavagnolli TM, Abdelmassih S, Abdelmassih R, et al. In vitro differentiation of male mouse embryonic stem cells into both presumptive sperm cells and oocytes. Cloning Stem Cells. 2007;9:535–48.
pubmed: 18154514
doi: 10.1089/clo.2007.0031
Lin C-Y, Lee B-S, Liao C-C, Cheng W-J, Chang F-M, Chen M-H. Transdifferentiation of bone marrow stem cells into acinar cells using a double chamber system. J Formos Med Assoc. 2007;106:1–7.
pubmed: 17282964
doi: 10.1016/S0929-6646(09)60209-6
Zhu Y, Hu H-L, Li P, Yang S, Zhang W, Ding H, et al. Generation of male germ cells from induced pluripotent stem cells (iPS cells): an in vitro and in vivo study. Asian journal of andrology. 2012;14:574.
pubmed: 22504877
pmcid: 3720088
doi: 10.1038/aja.2012.3
Fang F, Li Z, Zhao Q, Ye Z, Gu X, Pan F, et al. Induced pluripotent stem cells derived from two idiopathic azoospermia patients display compromised differentiation potential for primordial germ cell fate. Frontiers Cell Dev Biol. 2020;8:432.
doi: 10.3389/fcell.2020.00432
Danner S, Kajahn J, Geismann C, Klink E, Kruse C. Derivation of oocyte-like cells from a clonal pancreatic stem cell line. Mol Hum Reprod. 2007;13:11–20.
pubmed: 17114208
doi: 10.1093/molehr/gal096
Wuputra K, Ku C-C, Wu D-C, Lin Y-C, Saito S, Yokoyama KK. Prevention of tumor risk associated with the reprogramming of human pluripotent stem cells. J Exp Clin Cancer Res. 2020;39:1–24.
doi: 10.1186/s13046-020-01584-0
Nayernia K, Lee JH, Drusenheimer N, Nolte J, Wulf G, Dressel R, et al. Derivation of male germ cells from bone marrow stem cells. Lab Invest. 2006;86:654–63.
pubmed: 16652109
doi: 10.1038/labinvest.3700429
Hajihoseini M, Vahdati A, Ebrahim Hosseini S, Mehrabani D, Tamadon A. Induction of spermatogenesis after stem cell therapy of azoospermic guinea pigs. Veterinarski arhiv. 2017;87:333–50.
doi: 10.24099/vet.arhiv.151209
Mehrabani D, Hassanshahi MA, Tamadon A, Zare S, Keshavarz S, Rahmanifar F, et al. Adipose tissue-derived mesenchymal stem cells repair germinal cells of seminiferous tubules of busulfan-induced azoospermic rats. J Human Reproductive Sci. 2015;8:103.
doi: 10.4103/0974-1208.158618
Tamadon A, Mehrabani D, Rahmanifar F, Jahromi AR, Panahi M, Zare S, et al. Induction of spermatogenesis by bone marrow-derived mesenchymal stem cells in busulfan-induced azoospermia in hamster. Int J Stem Cells. 2015;8:134–45.
pubmed: 26634062
pmcid: 4651278
doi: 10.15283/ijsc.2015.8.2.134
Rahmanifar F, Tamadon A, Mehrabani D, Zare S, Abasi S, Keshavarz S, et al. Histomorphometric evaluation of treatment of rat azoosper-mic seminiferous tubules by allotransplantation of bone marrow-derived mesenchymal stem cells. Iran J Basic Med Sci. 2016;19:653.
pubmed: 27482347
pmcid: 4951605
Karimaghai N, Tamadon A, Rahmanifar F, Mehrabani D, Jahromi AR, Zare S, et al. Spermatogenesis after transplantation of adipose tissue-derived mesenchymal stem cells in busulfan-induced azoospermic hamster. Iran J Basic Med Sci. 2018;21:660.
pubmed: 30140403
pmcid: 6098960
Cakici C, Buyrukcu B, Duruksu G, Haliloglu AH, Aksoy A, Isik A, et al. Recovery of fertility in azoospermia rats after injection of adipose-tissue-derived mesenchymal stem cells: the sperm generation. Biomed Res Int. 2013;2013:1–18.
doi: 10.1155/2013/529589
Lue Y, Erkkila K, Liu PY, Ma K, Wang C, Hikim AS, et al. Fate of bone marrow stem cells transplanted into the testis: potential implication for men with testicular failure. Am J Pathol. 2007;170:899–908.
pubmed: 17322375
pmcid: 1864883
doi: 10.2353/ajpath.2007.060543
Tamadon A, Zhan-Byrbekuly U, Kairgaliyev I, Khoradmehr A. Mesenchymal stem cell therapy of male infertility. Male Reproductive Health, IntechOpen. 2019;105–112.
Kinnaird T, Stabile E, Burnett M, Lee C, Barr S, Fuchs S, et al. Marrow-derived stromal cells express genes encoding a broad spectrum of arteriogenic cytokines and promote in vitro and in vivo arteriogenesis through paracrine mechanisms. Circ Res. 2004;94:678–85.
pubmed: 14739163
doi: 10.1161/01.RES.0000118601.37875.AC
Monsefi M, Fereydouni B, Rohani L, Talaei T. Mesenchymal stem cells repair germinal cells of seminiferous tubules of sterile rats. Iran J Reprod Med. 2013;11:537–44.
pubmed: 24639788
pmcid: 3941348
Vahdati A, Fathi A, Hajihoseini M, Aliborzi G, Hosseini E. The regenerative effect of bone marrow-derived stem cells in spermatogenesis of infertile hamster. World journal of plastic surgery. 2017;6:18.
pubmed: 28289609
pmcid: 5339605
Mital P, Kaur G, Dufour JM. Immunoprotective sertoli cells: making allogeneic and xenogeneic transplantation feasible. Reproduction. 2010;139:495–504.
pubmed: 19995832
doi: 10.1530/REP-09-0384
Luo Y, Xie L, Mohsin A, Ahmed W, Xu C, Peng Y, et al. Efficient generation of male germ-like cells derived during co-culturing of adipose-derived mesenchymal stem cells with Sertoli cells under retinoic acid and testosterone induction. Stem Cell Res Ther. 2019;10:1–18.
doi: 10.1186/s13287-019-1181-5
Meligy FY, Abo Elgheed AT, Alghareeb SM. Therapeutic effect of adipose-derived mesenchymal stem cells on Cisplatin induced testicular damage in adult male albino rat. Ultrastructural Pathol. 2019;43:28–55.
doi: 10.1080/01913123.2019.1572256
Hsiao CH, Ji AT, Chang CC, Cheng CJ, Lee LM, Ho JH. Local injection of mesenchymal stem cells protects testicular torsion-induced germ cell injury. Stem Cell Res Ther. 2015;6:113. https://doi.org/10.1186/s13287-015-0079-0 .
doi: 10.1186/s13287-015-0079-0
pubmed: 26025454
pmcid: 4449584
Qian C, Meng Q, Lu J, Zhang L, Li H, Huang B. Human amnion mesenchymal stem cells restore spermatogenesis in mice with busulfan-induced testis toxicity by inhibiting apoptosis and oxidative stress. Stem Cell Res Ther. 2020;11:1–12.
doi: 10.1186/s13287-020-01803-7
Kadam P, Ntemou E, Baert Y, Van Laere S, Van Saen D, Goossens E. Co-transplantation of mesenchymal stem cells improves spermatogonial stem cell transplantation efficiency in mice. Stem Cell Res Ther. 2018;9:1–11.
doi: 10.1186/s13287-018-1065-0
Sherif IO, Sabry D, Abdel-Aziz A, Sarhan OM. The role of mesenchymal stem cells in chemotherapy-induced gonadotoxicity. Stem Cell Res Ther. 2018;9:196. https://doi.org/10.1186/s13287-018-0946-6 .
doi: 10.1186/s13287-018-0946-6
pubmed: 30021657
pmcid: 6052634
Ghasemzadeh-Hasankolaei M, Batavani R, Eslaminejad MB, Sayahpour F. Transplantation of autologous bone marrow mesenchymal stem cells into the testes of infertile male rats and new germ cell formation. Int J Stem Cells. 2016;9:250–63. https://doi.org/10.15283/ijsc16010 .
doi: 10.15283/ijsc16010
pubmed: 27430978
pmcid: 5155721
Zhang D, Liu X, Peng J, He D, Lin T, Zhu J, et al. Potential spermatogenesis recovery with bone marrow mesenchymal stem cells in an azoospermic rat model. Int J Mol Sci. 2014;15:13151–65. https://doi.org/10.3390/ijms150813151 .
doi: 10.3390/ijms150813151
pubmed: 25062349
pmcid: 4159785
Badawy AA, El-Magd MA, AlSadrah SA, Alruwaili MM. Altered expression of some miRNAs and their target genes following mesenchymal stem cell treatment in busulfan-induced azoospermic rats. Gene. 2020;737:144481.
pubmed: 32070749
doi: 10.1016/j.gene.2020.144481
Zahkook S, Atwa A, Shahat M, Mansour AM, Bakry S. Mesenchymal stem cells restore fertility in induced azoospermic rats following chemotherapy administration. J Reprod Infertil. 2014;5:50–7.
Aziz MTA, Mostafa T, Atta H, Asaad S, Fouad HH, Mohsen G, et al. In vitro and in vivo lineage conversion of bone marrow stem cells into germ cells in experimental azoospermia in rat. Stem Cell Studies. 2011;1:e15–e15.
doi: 10.4081/scs.2011.e15
Abdelaziz MH, Salah El-Din EY, El-Dakdoky MH, Ahmed TA. The impact of mesenchymal stem cells on doxorubicin-induced testicular toxicity and progeny outcome of male prepubertal rats. Birth Defects Res. 2019;111:906–19. https://doi.org/10.1002/bdr2.1535 .
doi: 10.1002/bdr2.1535
pubmed: 31210400
Hassan AI, Alam SS. Evaluation of mesenchymal stem cells in treatment of infertility in male rats. Stem Cell Res Ther. 2014;5:131. https://doi.org/10.1186/scrt521 .
doi: 10.1186/scrt521
pubmed: 25422144
pmcid: 4528845
Sabbaghi MA, Bahrami AR, Feizzade B, Kalantar SM, Matin MM, Kalantari M, et al. Trial evaluation of bone marrow derived mesenchymal stem cells (MSCs) transplantation in revival of spermatogenesis in testicular torsion. Middle East Fertility Society Journal. 2012;17:243–9.
doi: 10.1016/j.mefs.2012.06.001
Fang W, Chao L, Zhang S-S, Liu W-S, Hua J-L. Transplantation of goat bone marrow mesenchymal stem cells (gMSCs) help restore spermatogenesis in endogenous germ cells-depleted mouse models. J Integrative Agric. 2013;12:483–94.
doi: 10.1016/S2095-3119(13)60249-X
Abdallah SH, Pasha HF, Abdelrahman AA, Mazen NF. Molecular effect of human umbilical cord blood CD34-positive and CD34-negative stem cells and their conjugate in azoospermic mice. Mol Cell Biochem. 2017;428:179–91. https://doi.org/10.1007/s11010-016-2928-2 .
doi: 10.1007/s11010-016-2928-2
Chen H, Tang QL, Wu XY, Xie LC, Lin LM, Ho GY, et al. Differentiation of human umbilical cord mesenchymal stem cells into germ-like cells in mouse seminiferous tubules. Mol Med Rep. 2015;12:819–28. https://doi.org/10.3892/mmr.2015.3528 .
doi: 10.3892/mmr.2015.3528
pubmed: 25815600
pmcid: 4438948
Yang R-F, Liu T-H, Zhao K, Xiong C-L. Enhancement of mouse germ cell-associated genes expression by injection of human umbilical cord mesenchymal stem cells into the testis of chemical-induced azoospermic mice. Asian J Androl. 2014;16:698.
pubmed: 24830694
pmcid: 4215652
doi: 10.4103/1008-682X.129209
Wang Y-J, Yan J, Zou X-L, Guo K-J, Zhao Y, Meng C-Y, et al. Bone marrow mesenchymal stem cells repair cadmium-induced rat testis injury by inhibiting mitochondrial apoptosis. Chem Biol Interact. 2017;271:39–47. https://doi.org/10.1016/j.cbi.2017.04.024 .
doi: 10.1016/j.cbi.2017.04.024
pubmed: 28457857
Zhankina R, Afshar A, Farrar Z, Khoradmehr A, Baghban M, Suleiman M et al. Restoration of spermatogenesis in azoospermic mice by bone marrow mesenchymal stromal/stem cells conditioned medium. 2022; https://doi.org/10.21203/rs.3.rs-169243/v2 .
Aghamir SMK, Salavati A, Yousefie R, Tootian Z, Ghazaleh N, Jamali M, et al. Does bone marrow–derived mesenchymal stem cell transfusion prevent antisperm antibody production after traumatic testis rupture? Urology. 2014;84:82–6.
pubmed: 24797037
doi: 10.1016/j.urology.2014.03.009
Yu Y, Valderrama AV, Han Z, Uzan G, Naserian S, Oberlin E. Human fetal liver MSCs are more effective than adult bone marrow MSCs for their immunosuppressive, immunomodulatory, and Foxp3+ T reg induction capacity. Stem Cell Res Ther. 2021;12:1–18.
doi: 10.1186/s13287-021-02176-1
ArefNezhad R, Motedayyen H, Mohammadi A. Therapeutic aspects of mesenchymal stem cell-based cell therapy with a focus on human amniotic epithelial cells in multiple sclerosis: a mechanistic review. Int J Stem Cells. 2021;14:241–51.
pubmed: 34158417
pmcid: 8429946
doi: 10.15283/ijsc21032
Lee JM, Jung J, Lee H-J, Jeong SJ, Cho KJ, Hwang S-G, et al. Comparison of immunomodulatory effects of placenta mesenchymal stem cells with bone marrow and adipose mesenchymal stem cells. Int Immunopharmacol. 2012;13:219–24.
pubmed: 22487126
doi: 10.1016/j.intimp.2012.03.024
Fijak M, Pilatz A, Hedger MP, Nicolas N, Bhushan S, Michel V, et al. Infectious, inflammatory and ‘autoimmune’ male factor infertility: how do rodent models inform clinical practice? Hum Reprod Update. 2018;24:416–41.
pubmed: 29648649
doi: 10.1093/humupd/dmy009
Kauerhof AC, Nicolas N, Bhushan S, Wahle E, Loveland KA, Fietz D, et al. Investigation of activin A in inflammatory responses of the testis and its role in the development of testicular fibrosis. Hum Reprod. 2019;34:1536–50. https://doi.org/10.1093/humrep/dez109 .
doi: 10.1093/humrep/dez109
pubmed: 31340036
Schuppe HC, Meinhardt A, Allam J, Bergmann M, Weidner W, Haidl G. Chronic orchitis: a neglected cause of male infertility? Andrologia. 2008;40:84–91.
pubmed: 18336456
doi: 10.1111/j.1439-0272.2008.00837.x
Hasan H, Bhushan S, Fijak M, Meinhardt A. Mechanism of inflammatory associated impairment of sperm function, spermatogenesis and steroidogenesis. Front Endocrinol. 2022;13:897029.
Pröbstl C, Umbach A, Beineke A, Körber H, Goericke-Pesch S. Immune cell characterization in spontaneous autoimmune orchitis in dogs. Theriogenology. 2022;187:219–26. https://doi.org/10.1016/j.theriogenology.2022.05.010 .
doi: 10.1016/j.theriogenology.2022.05.010
pubmed: 35633611
Bergmann M, Kliesch S. Testicular Biopsy and Histology. In Nieschlag E, Behre HM, Nieschlag S (eds) Andrology 2010:155–167. Springer, Berlin.
Hauptman D, Perić MH, Marić T, Bojanac AK, Sinčić N, Zimak Z et al. Leydig cells in patients with non-obstructive azoospermia: do they really proliferate? Life (Basel). 2021;11. https://doi.org/10.3390/life11111266
Nicolas N, Michel V, Bhushan S, Wahle E, Hayward S, Ludlow H, et al. Testicular activin and follistatin levels are elevated during the course of experimental autoimmune epididymo–orchitis in mice. Sci Rep. 2017;7:42391. https://doi.org/10.1038/srep42391 .
doi: 10.1038/srep42391
pubmed: 28205525
pmcid: 5304336
Rusz A, Pilatz A, Wagenlehner F, Linn T, Diemer T, Schuppe H, et al. Influence of urogenital infections and inflammation on semen quality and male fertility. World J Urol. 2012;30:23–30.
pubmed: 21748371
doi: 10.1007/s00345-011-0726-8
Cassim MI, Tasneem M. A novel therapy for the treatment of malefactor infertility due to non-obstructive azoospermia: a case report. Crescent Journal of Medical and Biological Sciences. 2019;6:129–131. https://www.sid.ir/en/Journal/ViewPaper.aspx?ID=775944
Van Saen D, Goossens E, De Block G, Tournaye H. Bone marrow stem cells transplanted to the testis of sterile mice do not differentiate into spermatogonial stem cells and have no protective effect on fertility. Fertil Steril. 2009;91:1549–52. https://doi.org/10.1016/j.fertnstert.2008.09.036 .
doi: 10.1016/j.fertnstert.2008.09.036
pubmed: 19006799
Bader R, Ibrahim J-N, Mourad A, Moussa M, Azoury J, Azoury J, et al. Improvement of human sperm vacuolization and DNA fragmentation co-cultured with adipose-derived mesenchymal stem cell secretome: in vitro effect. Int J Stem Cells. 2019;12:388–99. https://doi.org/10.15283/ijsc19047 .
doi: 10.15283/ijsc19047
pubmed: 31474028
pmcid: 6881046
Levy JA, Marchand M, Iorio L, Zribi G, Zahalsky MP. Effects of stem cell treatment in human patients with Peyronie disease. J Am Osteopath Assoc. 2015;115:e8-13. https://doi.org/10.7556/jaoa.2015.124 .
doi: 10.7556/jaoa.2015.124
pubmed: 26414724
Levy JA, Marchand M, Iorio L, Cassini W, Zahalsky MP. Determining the feasibility of managing erectile dysfunction in humans with placental-derived stem cells. J Am Osteopath Assoc. 2016;116:e1-5. https://doi.org/10.7556/jaoa.2016.007 .
doi: 10.7556/jaoa.2016.007
pubmed: 26745574
Ganguly P, El-Jawhari JJ, Giannoudis PV, Burska AN, Ponchel F, Jones EA. Age-related changes in bone marrow mesenchymal stromal cells: a potential impact on osteoporosis and osteoarthritis development. Cell Transplant. 2017;26:1520–9. https://doi.org/10.1177/0963689717721201 .
doi: 10.1177/0963689717721201
pubmed: 29113463
pmcid: 5680949
Park KS, Bandeira E, Shelke GV, Lässer C, Lötvall J. Enhancement of therapeutic potential of mesenchymal stem cell-derived extracellular vesicles. Stem Cell Res Ther. 2019;10:288. https://doi.org/10.1186/s13287-019-1398-3 .
doi: 10.1186/s13287-019-1398-3
pubmed: 31547882
pmcid: 6757418
Deng C, Xie Y, Zhang C, Ouyang B, Chen H, Lv L, et al. Urine-derived stem cells facilitate endogenous spermatogenesis restoration of busulfan-induced nonobstructive azoospermic mice by paracrine exosomes. Stem Cells Dev. 2019;28:1322–33. https://doi.org/10.1089/scd.2019.0026 .
doi: 10.1089/scd.2019.0026
pubmed: 31311428
Ibrahim A, Marbán E. Exosomes: fundamental biology and roles in cardiovascular physiology. Annu Rev Physiol. 2016;78:67–83. https://doi.org/10.1146/annurev-physiol-021115-104929 .
doi: 10.1146/annurev-physiol-021115-104929
pubmed: 26667071
Jiang N, Xiang L, He L, Yang G, Zheng J, Wang C, et al. Exosomes mediate epithelium-mesenchyme crosstalk in organ development. ACS Nano. 2017;11:7736–46. https://doi.org/10.1021/acsnano.7b01087 .
doi: 10.1021/acsnano.7b01087
pubmed: 28727410
pmcid: 5634743
Basu J, Ludlow JW. Exosomes for repair, regeneration and rejuvenation. Expert Opin Biol Ther. 2016;16:489–506. https://doi.org/10.1517/14712598.2016.1131976 .
doi: 10.1517/14712598.2016.1131976
pubmed: 26817494
Auyeung CL, Co NN, Tsuruga T, Yeung TL, Kwan SY, Leung CS, et al. Exosomal transfer of stroma-derived miR21 confers paclitaxel resistance in ovarian cancer cells through targeting APAF1. Nat Commun. 2016;7:11150. https://doi.org/10.1038/ncomms11150 .
doi: 10.1038/ncomms11150
Guo XB, Zhai JW, Xia H, Yang JK, Zhou JH, Guo WB, et al. Protective effect of bone marrow mesenchymal stem cell-derived exosomes against the reproductive toxicity of cyclophosphamide is associated with the p38MAPK/ERK and AKT signaling pathways. Asian J Androl. 2021;23:386–91. https://doi.org/10.4103/aja.aja_98_20 .
doi: 10.4103/aja.aja_98_20
pubmed: 33565424
pmcid: 8269825
Mobarak H, Heidarpour M, Rahbarghazi R, Nouri M, Mahdipour M. Amniotic fluid-derived exosomes improved spermatogenesis in a rat model of azoospermia. Life Sci. 2021;274:119336. https://doi.org/10.1016/j.lfs.2021.119336 .
doi: 10.1016/j.lfs.2021.119336
pubmed: 33716061
Zhankina R, Baghban N, Askarov M, Saipiyeva D, Ibragimov A, Kadirova B, et al. Mesenchymal stromal/stem cells and their exosomes for restoration of spermatogenesis in non-obstructive azoospermia: a systemic review. Stem Cell Res Ther. 2021;12:229. https://doi.org/10.1186/s13287-021-02295-9 .
doi: 10.1186/s13287-021-02295-9
pubmed: 33823925
pmcid: 8025392
Okada H, Tsuzuki T, Murata H. Decidualization of the human endometrium. Reprod Med Biol. 2018;17:220–7. https://doi.org/10.1002/rmb2.12088 .
doi: 10.1002/rmb2.12088
pubmed: 30013421
pmcid: 6046526
Karlsson H, Erkers T, Nava S, Ruhm S, Westgren M, Ringdén O. Stromal cells from term fetal membrane are highly suppressive in allogeneic settings in vitro. Clin Exp Immunol. 2012;167:543–55. https://doi.org/10.1111/j.1365-2249.2011.04540.x .
doi: 10.1111/j.1365-2249.2011.04540.x
pubmed: 22288598
pmcid: 3374287
Ringden O, Erkers T, Nava S, Uzunel M, Iwarsson E, Conrad R, et al. Fetal membrane cells for treatment of steroid-refractory acute graft-versus-host disease. Stem cells. 2013;31:592–601.
pubmed: 23307526
doi: 10.1002/stem.1314
Abumaree MH, Abomaray F, Alshehri N, Almutairi A, AlAskar A, Kalionis B, et al. Phenotypic and functional characterization of mesenchymal stem/multipotent stromal cells from decidua parietalis of human term placenta. Reprod Sci. 2016;23:1193–207.
pubmed: 26902429
doi: 10.1177/1933719116632924
Abomaray FM, Aljumah MA, Alsaad KO, Jawdat D, Alkhaldi A, Alaskar AS, et al. Phenotypic and functional characterization of mesenchymal stem/multipotent stromal cells from decidua basalis of human term placenta. Stem Cells Int. 2016;2016:5184601. https://doi.org/10.1155/2016/5184601 .
doi: 10.1155/2016/5184601
pubmed: 27087815
pmcid: 4764756
Intanker PS, Scherjon SA, Kleijburg-van der Keur C, de Groot-Swings GM, Claas FH, Fibbe WE, et al. Isolation of mesenchymal stem cells of fetal or maternal origin from human placenta. Stem Cells. 2004;22:1338–45. https://doi.org/10.1634/stemcells.2004-0058 .
doi: 10.1634/stemcells.2004-0058
Kazemi S, Parivar K, Roudbari NH, Yaghmaei P, Sadeghi B. Growth kinetic comparison of human mesenchymal stem cells from bone marrow, adipose tissue and decidua. Med Sci. 2020;24:223–34.
Semenov OV, Koestenbauer S, Riegel M, Zech N, Zimmermann R, Zisch AH, et al. Multipotent mesenchymal stem cells from human placenta: critical parameters for isolation and maintenance of stemness after isolation. Am J Obstet Gynecol. 2010;202:193.e191-193.e113. https://doi.org/10.1016/j.ajog.2009.10.869 .
doi: 10.1016/j.ajog.2009.10.869
Erkers T, Nava S, Yosef J, Ringdén O, Kaipe H. Decidual stromal cells promote regulatory T cells and suppress alloreactivity in a cell contact-dependent manner. Stem Cells Dev. 2013;22:2596–605.
pubmed: 23701127
doi: 10.1089/scd.2013.0079
Erkers T, Kaipe H, Nava S, Molldén P, Gustafsson B, Axelsson R, et al. Treatment of severe chronic graft-versus-host disease with decidual stromal cells and tracing with 111Indium radiolabeling. Stem cells Dev. 2015;24:253–63.
pubmed: 25162829
doi: 10.1089/scd.2014.0265
Ringden O, Baygan A, Remberger M, Gustafsson B, Winiarski J, Khoein B, et al. Placenta-derived decidua stromal cells for treatment of severe acute graft-versus-host disease. Stem Cells Transl Med. 2018;7:325–31.
pubmed: 29533533
pmcid: 5866941
doi: 10.1002/sctm.17-0167
Baygan A, Aronsson-Kurttila W, Moretti G, Tibert B, Dahllöf G, Klingspor L, et al. Safety and side effects of using placenta-derived decidual stromal cells for graft-versus-host disease and hemorrhagic cystitis. Front Immunol. 2017;8:795.
pubmed: 28744284
pmcid: 5504152
doi: 10.3389/fimmu.2017.00795
Ringdén O, Solders M, Erkers T, Nava S, Molldén P, Hultcrantz M, et al. Successful reversal of acute lung injury using placenta-derived decidual stromal cells. J Stem Cell Res Ther. 2014;4:1–5.
Alshareef GH, Mohammed AE, Abumaree M, Basmaeil YS. Phenotypic and functional responses of human decidua basalis mesenchymal stem/stromal cells to lipopolysaccharide of gram-negative bacteria. Stem Cells Cloning: Adv App. 2021;14:51.
Lublin FD, Bowen JD, Huddlestone J, Kremenchutzky M, Carpenter A, Corboy JR, et al. Human placenta-derived cells (PDA-001) for the treatment of adults with multiple sclerosis: a randomized, placebo-controlled, multiple-dose study. Multiple Sclerosis Related Disorders. 2014;3:696–704.
pubmed: 25891548
doi: 10.1016/j.msard.2014.08.002
Gustafsson B, Frisk P, Szakos A, Sadeghi B, Ringdén O, Frost BM. Successful treatment with placenta-derived decidual stromal cells in a pediatric patient with life-threatening acute gastrointestinal graft-versus-host disease. Pediatr Transplant. 2017;21:e12990.
doi: 10.1111/petr.12990
Kim T-H, Choi JH, Jun Y, Lim SM, Park S, Paek J-Y, et al. 3D-cultured human placenta-derived mesenchymal stem cell spheroids enhance ovary function by inducing folliculogenesis. Sci Rep. 2018;8:1–11.
Yin N, Zhao W, Luo Q, Yuan W, Luan X, Zhang H. Restoring ovarian function with human placenta-derived mesenchymal stem cells in autoimmune-induced premature ovarian failure mice mediated by Treg cells and associated cytokines. Reprod Sci. 2018;25:1073–82.
pubmed: 28954601
doi: 10.1177/1933719117732156
Choi JH, Seok J, Lim SM, Kim TH, Kim GJ. Microenvironmental changes induced by placenta-derived mesenchymal stem cells restore ovarian function in ovariectomized rats via activation of the PI3K-FOXO3 pathway. Stem Cell Res Ther. 2020;11:1–13.
doi: 10.1186/s13287-020-02002-0
Seok J, Park H, Choi JH, Lim J-Y, Kim KG, Kim GJ. Placenta-derived mesenchymal stem cells restore the ovary function in an ovariectomized rat model via an antioxidant effect. Antioxidants. 2020;9:591.
pubmed: 32640638
pmcid: 7402146
doi: 10.3390/antiox9070591
Lu J, Liu Z, Shu M, Zhang L, Xia W, Tang L, et al. Human placental mesenchymal stem cells ameliorate chemotherapy-induced damage in the testis by reducing apoptosis/oxidative stress and promoting autophagy. Stem Cell Res Ther. 2021;12:1–10.
doi: 10.1186/s13287-021-02275-z
Zhankina R, Baghban N, Askarov M, Saipiyeva D, Ibragimov A, Kadirova B, et al. Mesenchymal stromal/stem cells and their exosomes for restoration of spermatogenesis in non-obstructive azoospermia: a systemic review. Stem Cell Res Ther. 2021;12:1–12.
doi: 10.1186/s13287-021-02295-9
Abomaray F, Aljumah M, Alsaad K, Jawdat D, Alkhaldi A, Alaskar AS, et al. Phenotypic and functional characterization of mesenchymal stem/multipotent stromal cells from decidua basalis of human term placenta. Stem Cells Int. 2016;2016:5184601.
pubmed: 27087815
pmcid: 4764756
doi: 10.1155/2016/5184601
Intanker PS, Scherjon SA, Kleijburg-Van Der Keur C, de Groot-Swings GM, Claas FH, Fibbe WE, et al. Isolation of mesenchymal stem cells of fetal or maternal origin from human placenta. Stem cells. 2004;22:1338–45.
doi: 10.1634/stemcells.2004-0058
Semenov OV, Koestenbauer S, Riegel M, Zech N, Zimmermann R, Zisch AH, et al. Multipotent mesenchymal stem cells from human placenta: critical parameters for isolation and maintenance of stemness after isolation. Am J Obstet Gynecol. 2010;202:19. e391-193.e113.
doi: 10.1016/j.ajog.2009.10.869
Hettich BF, Ben-Yehuda Greenwald M, Werner S, Leroux JC. Exosomes for wound healing: purification optimization and identification of bioactive components. Advanced Science. 2020;7:2002596.
pubmed: 33304765
pmcid: 7709981
doi: 10.1002/advs.202002596