Enhancing Spermatogenesis in Non-obstructive Azoospermia Through Mesenchymal Stem Cell Therapy22
- 作者: Margiana R.1
-
隶属关系:
- Andrology Program, Faculty of Medicine, Universitas Airlangga
- 期: 卷 19, 编号 11 (2024)
- 页面: 1429-1441
- 栏目: Medicine
- URL: https://ruspoj.com/1574-888X/article/view/645569
- DOI: https://doi.org/10.2174/011574888X283311231226081845
- ID: 645569
如何引用文章
全文:
详细
:Stem cells hold great promise as novel and encouraging therapeutic tools in the treatment of degenerative disorders due to their differentiation potential while maintaining the capability to self-renewal and their unlimited ability to divide and regenerate tissue. A variety of different types of stem cells can be used in cell therapy. Among these, mesenchymal stem cell (MSC) therapy has gradually established itself as a novel method for treating damaged tissues that need restoration and renewal. Male infertility is an important health challenge affecting approximately 8-12% of people around the world. This abnormality can be caused by primary, congenital, acquired, or idiopathic reasons. Men with no sperm in their semen have a condition called azoospermia, caused by non-obstructive (NOA) causes and post-testicular obstructive causes. Accumulating evidence has shown that various types of MSCs can differentiate into germ cells and improve spermatogenesis in the seminiferous tubules of animal models. In addition, recent studies in animal models have exhibited that extracellular vesicles derived from MSCs can stimulate the progression of spermatogenesis and germ cell regeneration in the recipient testes. In spite of the fact that various improvements have been made in the treatment of azoospermia disorder in animal models by MSC or their extracellular vesicles, no clinical trials have been carried out to test their therapeutic effect on the NOA. In this review, we summarize the potential of MSC transplantation for treating infertility caused by NOA.
作者简介
Ria Margiana
Andrology Program, Faculty of Medicine, Universitas Airlangga
编辑信件的主要联系方式.
Email: info@benthamscience.net
参考
- Zegers-Hochschild, F.; Adamson, G.D.; Dyer, S.; Racowsky, C.; de Mouzon, J.; Sokol, R.; Rienzi, L.; Sunde, A.; Schmidt, L.; Cooke, I.D.; Simpson, J.L.; van der Poel, S. The international glossary on infertility and fertility care, 2017. Fertil. Steril., 2017, 108(3), 393-406. doi: 10.1016/j.fertnstert.2017.06.005 PMID: 28760517
- Agarwal, A.; Mulgund, A.; Hamada, A.; Chyatte, M.R. A unique view on male infertility around the globe. Reprod. Biol. Endocrinol., 2015, 13(1), 37. doi: 10.1186/s12958-015-0032-1 PMID: 25928197
- Vander Borght, M.; Wyns, C. Fertility and infertility: Definition and epidemiology. Clin. Biochem., 2018, 62, 2-10. doi: 10.1016/j.clinbiochem.2018.03.012 PMID: 29555319
- Carlsen, E.; Giwercman, A.; Keiding, N.; Skakkebaek, N.E. Evidence for decreasing quality of semen during past 50 years. BMJ, 1992, 305(6854), 609-613. doi: 10.1136/bmj.305.6854.609 PMID: 1393072
- Swan, S.H.; Elkin, E.P.; Fenster, L. The question of declining sperm density revisited: an analysis of 101 studies published 1934-1996. Environ. Health Perspect., 2000, 108(10), 961-966. doi: 10.1289/ehp.00108961 PMID: 11049816
- Mishra, P.; Negi, M.P.S.; Srivastava, M.; Singh, K.; Rajender, S. Decline in seminal quality in Indian men over the last 37 years. Reprod. Biol. Endocrinol., 2018, 16(1), 103. doi: 10.1186/s12958-018-0425-z PMID: 30352581
- Levine, H.; Jørgensen, N.; Martino-Andrade, A.; Mendiola, J.; Weksler-Derri, D.; Mindlis, I.; Pinotti, R.; Swan, S.H. Temporal trends in sperm count: A systematic review and meta-regression analysis. Hum. Reprod. Update, 2017, 23(6), 646-659. doi: 10.1093/humupd/dmx022 PMID: 28981654
- Krausz, C. Male infertility: Pathogenesis and clinical diagnosis. Best Pract. Res. Clin. Endocrinol. Metab., 2011, 25(2), 271-285. doi: 10.1016/j.beem.2010.08.006 PMID: 21397198
- Zhankina, R.; Baghban, N.; Askarov, M.; Saipiyeva, D.; Ibragimov, A.; Kadirova, B.; Khoradmehr, A.; Nabipour, I.; Shirazi, R.; Zhanbyrbekuly, U.; Tamadon, A. 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), 229. doi: 10.1186/s13287-021-02295-9 PMID: 33823925
- Cai, Z.; Li, H. Congenital bilateral absence of the vas deferens. Front. Genet., 2022, 13, 775123. doi: 10.3389/fgene.2022.775123 PMID: 35222530
- Gao, G.; Fan, C.; Li, W.; Liang, R.; Wei, C.; Chen, X.; Yang, Y.; Zhong, Y.; Shao, Y.; Kong, Y.; Li, Z.; Zhu, X. Mesenchymal stem cells: Ideal seeds for treating diseases. Hum. Cell, 2021, 34(6), 1585-1600. doi: 10.1007/s13577-021-00578-0 PMID: 34272720
- Fukutake, M.; Ochiai, D.; Masuda, H.; Abe, Y.; Sato, Y.; Otani, T.; Sakai, S.; Aramaki-Hattori, N.; Shimoda, M.; Matsumoto, T.; Miyakoshi, K.; Kanai, Y.; Kishi, K.; Tanaka, M. Human amniotic fluid stem cells have a unique potential to accelerate cutaneous wound healing with reduced fibrotic scarring like a fetus. Hum. Cell, 2019, 32(1), 51-63. doi: 10.1007/s13577-018-0222-1 PMID: 30506493
- Gupta, A.; Kashte, S.; Gupta, M.; Rodriguez, H.C.; Gautam, S.S.; Kadam, S. Mesenchymal stem cells and exosome therapy for COVID-19: current status and future perspective. Hum. Cell, 2020, 33(4), 907-918. doi: 10.1007/s13577-020-00407-w PMID: 32780299
- Yamada, A.; Yokoo, T.; Yokote, S.; Yamanaka, S.; Izuhara, L.; Katsuoka, Y.; Shimada, Y.; Shukuya, A.; Okano, H.J.; Ohashi, T.; Ida, H. Comparison of multipotency and molecular profile of MSCs between CKD and healthy rats. Hum. Cell, 2014, 27(2), 59-67. doi: 10.1007/s13577-013-0082-7 PMID: 24496821
- Liang, H.; Suo, H.; Wang, Z.; Feng, W. Progress in the treatment of osteoarthritis with umbilical cord stem cells. Hum. Cell, 2020, 33(3), 470-475. doi: 10.1007/s13577-020-00377-z PMID: 32447573
- Fei, X.; Cai, Y.; Lin, F.; Huang, Y.; Liu, T.; Liu, Y. Amniotic fluid mesenchymal stem cells repair mouse corneal cold injury by promoting mRNA N4-acetylcytidine modification and ETV4/JUN/CCND2 signal axis activation. Hum. Cell, 2021, 34(1), 86-98. doi: 10.1007/s13577-020-00442-7 PMID: 33010000
- Jovic, D.; Yu, Y.; Wang, D.; Wang, K.; Li, H.; Xu, F.; Liu, C.; Liu, J.; Luo, Y. A brief overview of global trends in MSC-based cell therapy. Stem Cell Rev. Rep., 2022, 18(5), 1525-1545. doi: 10.1007/s12015-022-10369-1 PMID: 35344199
- Margiana, R.; Markov, A.; Zekiy, A.O.; Hamza, M.U.; Al-Dabbagh, K.A.; Al-Zubaidi, S.H.; Hameed, N.M.; Ahmad, I.; Sivaraman, R.; Kzar, H.H.; Al-Gazally, M.E.; Mustafa, Y.F.; Siahmansouri, H. Clinical application of mesenchymal stem cell in regenerative medicine: A narrative review. Stem Cell Res. Ther., 2022, 13(1), 366. doi: 10.1186/s13287-022-03054-0 PMID: 35902958
- Musiał-Wysocka, A.; Kot, M.; Majka, M. The pros and cons of mesenchymal stem cell-based therapies. Cell Transplant., 2019, 28(7), 801-812. doi: 10.1177/0963689719837897 PMID: 31018669
- Xv, J.; Ming, Q.; Wang, X.; Zhang, W.; Li, Z.; Wang, S.; Li, Y.; Li, L. Mesenchymal stem cells moderate immune response of type 1 diabetes. Cell Tissue Res., 2017, 368(2), 239-248. doi: 10.1007/s00441-016-2499-2 PMID: 27726027
- Han, Y.; Yang, J.; Fang, J.; Zhou, Y.; Candi, E.; Wang, J.; Hua, D.; Shao, C.; Shi, Y. The secretion profile of mesenchymal stem cells and potential applications in treating human diseases. Signal Transduct. Target. Ther., 2022, 7(1), 92. doi: 10.1038/s41392-022-00932-0 PMID: 35314676
- Durairajanayagam, D. Lifestyle causes of male infertility. Arab J. Urol., 2018, 16(1), 10-20. doi: 10.1016/j.aju.2017.12.004 PMID: 29713532
- Wosnitzer, M.; Goldstein, M.; Hardy, M.P. Review of azoospermia. Spermatogenesis, 2014, 4(1), e28218. doi: 10.4161/spmg.28218 PMID: 25105055
- Kang, C.; Punjani, N.; Schlegel, P.N. Reproductive chances of men with azoospermia due to spermatogenic dysfunction. J. Clin. Med., 2021, 10(7), 1400. doi: 10.3390/jcm10071400 PMID: 33807489
- Tao, Y. Endocrine aberrations of human nonobstructive azoospermia. Asian J. Androl., 2022, 24(3), 274-286. doi: 10.4103/aja202181 PMID: 35042310
- Ring, J.; Welliver, C.; Parenteau, M.; Markwell, S.; Brannigan, R.E.; Köhler, T.S. The utility of sex hormone-binding globulin in hypogonadism and infertile males. J. Urol., 2017, 197(5), 1326-1331. doi: 10.1016/j.juro.2017.01.018 PMID: 28087298
- Gauthier-Fisher, A.; Kauffman, A.; Librach, C.L. Potential use of stem cells for fertility preservation. Andrology, 2020, 8(4), 862-878. doi: 10.1111/andr.12713 PMID: 31560823
- Vieira, M.; Bispo de Andrade, M.A.; Santana-Santos, E. Is testicular microdissection the only way to retrieve sperm for non-obstructive azoospermic men? Front Reprod Health., 2022, 4, 980824. doi: 10.3389/frph.2022.980824
- Esteves, S.C.; Ramasamy, R.; Colpi, G.M.; Carvalho, J.F.; Schlegel, P.N. Sperm retrieval rates by micro-TESE versus conventional TESE in men with non-obstructive azoospermiathe assumption of independence in effect sizes might lead to misleading conclusions. Hum. Reprod. Update, 2020, 26(4), 603-605. doi: 10.1093/humupd/dmaa006 PMID: 32436569
- Yalcin, I.; Berker, B.; Sukur, Y.E.; Kahraman, K.; Ates, C. Comparison of intracytoplasmic sperm injection with testicular spermatozoa success in infertile men with obstructive and non-obstructive azoospermia; a retrospective analysis. Hum. Fertil., 2017, 20(3), 186-191. doi: 10.1080/14647273.2016.1264632 PMID: 27931129
- Oses, R.J.; Zappacosta Villarroel, M.; Medel, P.; Garcia Ojeda, M.; Viola, J.; Valcarcel, A. TESE-ICSI in couples with non obstructive azoospermia: comparison between fresh or previously cryopreserved testicular sperm. Fertil. Steril., 2018, 110(4), e289. doi: 10.1016/j.fertnstert.2018.07.817
- Elena, E. AJ Friedenstein, founder of the mesenchymal stem cell concept. Cell. Ther. Transplant., 2009, 1(3), 35-38.
- Friedenstein, A.J.; Piatetzky-Shapiro, I.I.; Petrakova, K.V. Osteogenesis in transplants of bone marrow cells. Development, 1966, 16(3), 381-390. doi: 10.1242/dev.16.3.381 PMID: 5336210
- Zakrzewski, W.; Dobrzyński, M.; Szymonowicz, M.; Rybak, Z. Stem cells: Past, present, and future. Stem Cell Res. Ther., 2019, 10(1), 68. doi: 10.1186/s13287-019-1165-5 PMID: 30808416
- Wu, X.; Jiang, J.; Gu, Z.; Zhang, J.; Chen, Y.; Liu, X. Mesenchymal stromal cell therapies: Immunomodulatory properties and clinical progress. Stem Cell Res. Ther., 2020, 11(1), 345. doi: 10.1186/s13287-020-01855-9 PMID: 32771052
- Kholodenko, I.V.; Kurbatov, L.K.; Kholodenko, R.V.; Manukyan, G.V.; Yarygin, K.N. Mesenchymal stem cells in the adult human liver: Hype or hope? Cells, 2019, 8(10), 1127. doi: 10.3390/cells8101127 PMID: 31546729
- Hernández, R.; Jiménez-Luna, C.; Perales-Adán, J.; Perazzoli, G.; Melguizo, C.; Prados, J. Differentiation of human mesenchymal stem cells towards neuronal lineage: Clinical trials in nervous system disorders. Biomol. Ther., 2020, 28(1), 34-44. doi: 10.4062/biomolther.2019.065 PMID: 31649208
- Longhini, A.L.F.; Salazar, T.E.; Vieira, C.; Trinh, T.; Duan, Y.; Pay, L.M.; Li Calzi, S.; Losh, M.; Johnston, N.A.; Xie, H.; Kim, M.; Hunt, R.J.; Yoder, M.C.; Santoro, D.; McCarrel, T.M.; Grant, M.B. Peripheral blood-derived mesenchymal stem cells demonstrate immunomodulatory potential for therapeutic use in horses. PLoS One, 2019, 14(3), e0212642. doi: 10.1371/journal.pone.0212642 PMID: 30870461
- Huang, C.; Liu, Y.; Ding, J.; Dai, Y.; Le, L.; Wang, L.; Ding, E.; Yang, J. Thermosensitive quaternized chitosan hydrogel scaffolds promote neural differentiation in bone marrow mesenchymal stem cells and functional recovery in a rat spinal cord injury model. Cell Tissue Res., 2021, 385(1), 65-85. doi: 10.1007/s00441-021-03430-x PMID: 33760948
- Rohani, Z.; Ghollasi, M.; Aghamollaei, H.; Saidi, H.; Halabian, R.; Kheirollahzadeh, F.; Poormoghadam, D. A new hydrogel with fluorapatite nanoparticles for osteogenic differentiation of human adipose-derived stem cells in tissue engineering field. Cell Tissue Res., 2022, 390(3), 399-411. doi: 10.1007/s00441-022-03691-0 PMID: 36152061
- Bonaventura, G.; Incontro, S.; Iemmolo, R.; La Cognata, V.; Barbagallo, I.; Costanzo, E.; Barcellona, M.L.; Pellitteri, R.; Cavallaro, S. Dental mesenchymal stem cells and neuro-regeneration: A focus on spinal cord injury. Cell Tissue Res., 2020, 379(3), 421-428. doi: 10.1007/s00441-019-03109-4 PMID: 31776822
- Skliutė, G.; Bauytė, R.; Borutinskaitė, V.; Valiulienė, G.; Kaupinis, A.; Valius, M.; Ramaauskaitė, D.; Navakauskienė, R. Menstrual blood-derived endometrial stem cells impact for the treatment perspective of female infertility. Int. J. Mol. Sci., 2021, 22(13), 6774. doi: 10.3390/ijms22136774 PMID: 34202508
- Chen, Y.; Hu, Y.; Zhou, X.; Zhao, Z.; Yu, Q.; Chen, Z.; Wang, Y.; Xu, P.; Yu, Z.; Guo, C.; Zhang, X.; Shi, Y. Human umbilical cord-derived mesenchymal stem cells ameliorate psoriasis-like dermatitis by suppressing IL-17-producing γδ T cells. Cell Tissue Res., 2022, 388(3), 549-563. doi: 10.1007/s00441-022-03616-x PMID: 35347409
- Lee, S.H.; Choung, J.S.; Kim, J.M.; Kim, H.; Kim, M. Distribution of embryonic stem cell-derived mesenchymal stem cells after intravenous infusion in hypoxicischemic encephalopathy. Life, 2023, 13(1), 227. doi: 10.3390/life13010227 PMID: 36676176
- Moonshi, S.S.; Adelnia, H.; Wu, Y.; Ta, H.T. Placenta-derived mesenchymal stem cells for treatment of diseases: A clinically relevant source. Adv. Ther., 2022, 5(10), 2200054. doi: 10.1002/adtp.202200054
- Mebarki, M.; Abadie, C.; Larghero, J.; Cras, A. Human umbilical cord-derived mesenchymal stem/stromal cells: a promising candidate for the development of advanced therapy medicinal products. Stem Cell Res. Ther., 2021, 12(1), 152. doi: 10.1186/s13287-021-02222-y PMID: 33637125
- Dominici, M.; Le Blanc, K.; Mueller, I.; Slaper-Cortenbach, I.; Marini, F.C.; Krause, D.S.; Deans, R.J.; Keating, A.; Prockop, D.J.; Horwitz, E.M. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy, 2006, 8(4), 315-317. doi: 10.1080/14653240600855905 PMID: 16923606
- Attia, N.; Mashal, M. Mesenchymal stem cells: The past present and future. Adv. Exp. Med. Biol., 2020, 1312, 107-129. doi: 10.1007/5584_2020_595 PMID: 33159306
- Andrzejewska, A.; Lukomska, B.; Janowski, M. Concise review: Mesenchymal stem cells: From roots to boost. Stem Cells, 2019, 37(7), 855-864. doi: 10.1002/stem.3016 PMID: 30977255
- Pittenger, M.F.; Discher, D.E.; Péault, B.M.; Phinney, D.G.; Hare, J.M.; Caplan, A.I. Mesenchymal stem cell perspective: Cell biology to clinical progress. NPJ Regen. Med., 2019, 4(1), 22. doi: 10.1038/s41536-019-0083-6 PMID: 31815001
- Hsiao, C.H.; Ji, A.T.Q.; Chang, C.C.; Chien, M.H.; Lee, L.M.; Ho, J.H.C. Mesenchymal stem cells restore the sperm motility from testicular torsion-detorsion injury by regulation of glucose metabolism in sperm. Stem Cell Res. Ther., 2019, 10(1), 270. doi: 10.1186/s13287-019-1351-5 PMID: 31445515
- Adriansyah, R.F.; Margiana, R.; Supardi, S.; Narulita, P. Current progress in stem cell therapy for male infertility. Stem Cell Rev. Rep., 2023, 19(7), 2073-2093. doi: 10.1007/s12015-023-10577-3 PMID: 37440145
- Wei, Y.; Fang, J.; Cai, S.; Lv, C.; Zhang, S.; Hua, J. Primordial germ celllike cells derived from canine adipose mesenchymal stem cells. Cell Prolif., 2016, 49(4), 503-511. doi: 10.1111/cpr.12271 PMID: 27374854
- Fang, J.; Wei, Y.; Lv, C.; Peng, S.; Zhao, S.; Hua, J. CD61 promotes the differentiation of canine ADMSCs into PGC-like cells through modulation of TGF-β signaling. Sci. Rep., 2017, 7(1), 43851. doi: 10.1038/srep43851 PMID: 28256590
- Liu, H.; Chen, M.; Liu, L.; Ren, S.; Cheng, P.; Zhang, H. Induction of human adipose-derived mesenchymal stem cells into germ lineage using retinoic acid. Cell. Reprogram., 2018, 20(2), 127-134. doi: 10.1089/cell.2017.0063 PMID: 29620445
- Ghatreh, K.; Eliyasi, M.; Alaei, S.; Saki, G. Differentiation potential of adipose tissue-derived mesenchymal stem cells into germ cells with and without growth factors. Andrologia, 2021, 53(1), e13892. doi: 10.1111/and.13892 PMID: 33167071
- Luo, Y.; Xie, L.; Mohsin, A.; Ahmed, W.; Xu, C.; Peng, Y.; Hang, H.; Zhuang, Y.; Chu, J.; Guo, M. 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), 91. doi: 10.1186/s13287-019-1181-5 PMID: 30867048
- Li, P.; Yan, G.; Han, L.; Pang, J.; Zhong, B.; Zhang, G.; Wang, F.; Zhang, Y. Overexpression of STRA8, BOULE, and DAZL genes promotes goat bone marrow-derived mesenchymal stem cells in vitro transdifferentiation toward putative male germ cells. Reprod. Sci., 2017, 24(2), 300-312. doi: 10.1177/1933719116654990 PMID: 27342271
- Ghasemzadeh-Hasankolaei, M.; Sedighi-Gilani, M.A.; Eslaminejad, M.B. Induction of ram bone marrow mesenchymal stem cells into germ cell lineage using transforming growth factor-β superfamily growth factors. Reprod. Domest. Anim., 2014, 49(4), 588-598. doi: 10.1111/rda.12327 PMID: 24888234
- Jouni, F.J.; Abdolmaleki, P.; Behmanesh, M.; Movahedin, M. An in vitro study of the impact of 4mT static magnetic field to modify the differentiation rate of rat bone marrow stem cells into primordial germ cells. Differentiation, 2014, 87(5), 230-237. doi: 10.1016/j.diff.2014.06.001 PMID: 25037498
- Afsartala, Z.; Rezvanfar, M.A.; Hodjat, M.; Tanha, S.; Assadollahi, V.; Bijangi, K.; Abdollahi, M.; Ghasemzadeh-Hasankolaei, M. Amniotic membrane mesenchymal stem cells can differentiate into germ cells in vitro. In vitro Cell Dev Biol Anim 2016, 52(10), 1060-1071. doi: 10.1007/s11626-016-0073-6 PMID: 27503516
- Alifi, F.; Asgari, H.R. Alteration in expression of primordial germ cell (PGC) markers during induction of human amniotic mesenchymal stem cells (hAMSCs). J. Reprod. Infertil., 2020, 21(1), 59-64. PMID: 32175266
- Li, B.; Liu, W.; Zhuang, M.; Li, N.; Wu, S.; Pan, S.; Hua, J. Overexpression of CD61 promotes hUC-MSC differentiation into male germ-like cells. Cell Prolif., 2016, 49(1), 36-47. doi: 10.1111/cpr.12236 PMID: 26840189
- Majidi, F.; Bamehr, H.; Shalchian, Z.; Kouchakian, M.R.; Mohammadzadeh, N.; Khalili, A. Differentiation of human umbilical cord mesenchymal stem cell into germ-like cell under effect of co-culture with testicular cell tissue. Anat. Histol. Embryol., 2020, 49(3), 359-364. doi: 10.1111/ahe.12537 PMID: 32034794
- Amidi, F.; Ataie Nejad, N.; Agha Hoseini, M.; Nayernia, K.; Mazaheri, Z.; Yamini, N.; Saeednia, S. In vitro differentiation process of human Whartons jelly mesenchymal stem cells to male germ cells in the presence of gonadal and non-gonadal conditioned media with retinoic acid. In vitro Cell. Dev. Biol. Anim 2015, 51(10), 1093-1101. doi: 10.1007/s11626-015-9929-4 PMID: 26427713
- Huang, P.; Lin, L.M.; Wu, X.Y.; Tang, Q.L.; Feng, X.Y.; Lin, G.Y.; Lin, X.; Wang, H.W.; Huang, T.H.; Ma, L. Differentiation of human umbilical cord Whartons jelly-derived mesenchymal stem cells into germ-like cells in vitro. J. Cell. Biochem., 2010, 109(4), 747-754. doi: 10.1002/jcb.22453 PMID: 20052672
- Xie, L.; Lin, L.; Tang, Q.; Li, W.; Huang, T.; Huo, X.; Liu, X.; Jiang, J.; He, G.; Ma, L. Sertoli cell-mediated differentiation of male germ cell-like cells from human umbilical cord Whartons jelly-derived mesenchymal stem cells in an in vitro co-culture system. Eur. J. Med. Res., 2015, 20(1), 9. doi: 10.1186/s40001-014-0080-6 PMID: 25644284
- Karimaghai, N.; Tamadon, A.; Rahmanifar, F.; Mehrabani, D.; Raayat Jahromi, A.; Zare, S.; Khodabandeh, Z.; Razeghian Jahromi, I.; Koohi-Hoseinabadi, O.; Dianatpour, M. Spermatogenesis after transplantation of adipose tissue-derived mesenchymal stem cells in busulfan-induced azoospermic hamster. Iran. J. Basic Med. Sci., 2018, 21(7), 660-667. PMID: 30140403
- Zhankina, R. Restoration of spermatogenesis in azoospermic mice by bone marrow mesenchymal stromal. stem cells conditioned medium, 2022.
- Cakici, C. Recovery of fertility in azoospermia rats after injection of adipose-tissue-derived mesenchymal stem cells: the sperm generation. Biomed Res Int, 2013, 2013, 529589. doi: 10.1155/2013/529589
- Meligy, F.Y.; Abo Elgheed, A.T.; Alghareeb, S.M. Therapeutic effect of adipose-derived mesenchymal stem cells on Cisplatin induced testicular damage in adult male albino rat. Ultrastruct. Pathol., 2019, 43(1), 28-55. doi: 10.1080/01913123.2019.1572256 PMID: 30741078
- Ganjibakhsh, M.; Mehraein, F.; Koruji, M.; Bashiri, Z. The therapeutic potential of adipose tissue-derived mesenchymal stromal cells in the treatment of busulfan-induced azoospermic mice. J. Assist. Reprod. Genet., 2022, 39(1), 153-163. doi: 10.1007/s10815-021-02309-8 PMID: 34519944
- Hsiao, C.H.; Ji, A.T.Q.; Chang, C.C.; Cheng, C.J.; Lee, L.M.; Ho, J.H.C. Local injection of mesenchymal stem cells protects testicular torsion-induced germ cell injury. Stem Cell Res. Ther., 2015, 6(1), 113. doi: 10.1186/s13287-015-0079-0 PMID: 26025454
- Hajihoseini, M.; Vahdati, A.; Hosseini, S.E.; Mehrabani, D.; Tamadon, A. Induction of spermatogenesis after stem cell therapy of azoospermic guinea pigs. Vet. Arh., 2017, 87(3), 333-350. doi: 10.24099/vet.arhiv.151209
- Badawy, A.A.; El-Magd, M.A.; AlSadrah, S.A.; Alruwaili, M.M. Altered expression of some miRNAs and their target genes following mesenchymal stem cell treatment in busulfan-induced azoospermic rats. Gene, 2020, 737, 144481. doi: 10.1016/j.gene.2020.144481 PMID: 32070749
- Abdelaziz, M.H.; Salah EL-Din, E.Y.; El-Dakdoky, M.H.; Ahmed, T.A. The impact of mesenchymal stem cells on doxorubicin-induced testicular toxicity and progeny outcome of male prepubertal rats. Birth Defects Res., 2019, 111(13), 906-919. doi: 10.1002/bdr2.1535 PMID: 31210400
- Khanmohammadi, N.; Malek, F.; Takzaree, N.; Malekzadeh, M.; Khanehzad, M.; Akanji, O.D.; Rastegar, T. Sertoli cellconditioned medium induces differentiation of bone marrowderived mesenchymal stem cells to male germ-like cells in busulfan-induced azoospermic mouse model. Reprod. Sci., 2024; 31(2): 372-92. doi: 10.1007/s43032-023-01332-7 PMID: 37737972
- Sabbaghi, M.A.; Bahrami, A.R.; Feizzade, B.; Kalantar, S.M.; Matin, M.M.; Kalantari, M.; Aflatoonian, A.; Saeinasab, M. Trial evaluation of bone marrow derived mesenchymal stem cells (MSCs) transplantation in revival of spermatogenesis in testicular torsion. Middle East Fertil. Soc. J., 2012, 17(4), 243-249. doi: 10.1016/j.mefs.2012.06.001
- Zhang, D.; Liu, X.; Peng, J.; He, D.; Lin, T.; Zhu, J.; Li, X.; Zhang, Y.; Wei, G. Potential spermatogenesis recovery with bone marrow mesenchymal stem cells in an azoospermic rat model. Int. J. Mol. Sci., 2014, 15(8), 13151-13165. doi: 10.3390/ijms150813151 PMID: 25062349
- Abd Allah, S.H.; Pasha, H.F.; Abdelrahman, A.A.; Mazen, N.F. 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(1-2), 179-191. doi: 10.1007/s11010-016-2928-2 PMID: 28120211
- Chen, H.; Tang, Q.L.; Wu, X.Y.; Xie, L.C.; Lin, L.M.; Ho, G.Y.; Ma, L. Differentiation of human umbilical cord mesenchymal stem cells into germ-like cells in mouse seminiferous tubules. Mol. Med. Rep., 2015, 12(1), 819-828. doi: 10.3892/mmr.2015.3528 PMID: 25815600
- Xiong, C-L.; Yang, R-F.; Liu, T-H.; Zhao, K. 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(5), 698-704. doi: 10.4103/1008-682X.129209 PMID: 24830694
- 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), 290. doi: 10.1186/s13287-020-01803-7 PMID: 32678012
- Zhang, W.; Yang, C.; Guo, W.; Guo, X.; Bian, J.; Zhou, Q.; Chen, M.; Zhou, J.; Chen, Z.; Wang, P.; Lv, X.; Xiao, Z.; Liu, C. Rotective effect of bone marrow mesenchymal stem cells-derived exosomes against testicular ischemia-reperfusion injury in rats. Nan Fang Yi Ke Da Xue Xue Bao, 2018, 38(8), 910-916. PMID: 30187884
- Deng, C.; Xie, Y.; Zhang, C.; Ouyang, B.; Chen, H.; Lv, L.; Yao, J.; Liang, X.; Zhang, Y.; Sun, X.; Deng, C.; Liu, G. Urine-derived stem cells facilitate endogenous spermatogenesis restoration of busulfan-induced nonobstructive azoospermic mice by paracrine exosomes. Stem Cells Dev., 2019, 28(19), 1322-1333. doi: 10.1089/scd.2019.0026 PMID: 31311428
- Zhou, T.; Yuan, Z.; Weng, J.; Pei, D.; Du, X.; He, C.; Lai, P. Challenges and advances in clinical applications of mesenchymal stromal cells. J. Hematol. Oncol., 2021, 14(1), 24. doi: 10.1186/s13045-021-01037-x PMID: 33579329
- Hoang, D.M.; Pham, P.T.; Bach, T.Q.; Ngo, A.T.L.; Nguyen, Q.T.; Phan, T.T.K.; Nguyen, G.H.; Le, P.T.T.; Hoang, V.T.; Forsyth, N.R.; Heke, M.; Nguyen, L.T. Stem cell-based therapy for human diseases. Signal Transduct. Target. Ther., 2022, 7(1), 272. doi: 10.1038/s41392-022-01134-4 PMID: 35933430
- Mastrolia, I.; Foppiani, E.M.; Murgia, A.; Candini, O.; Samarelli, A.V.; Grisendi, G.; Veronesi, E.; Horwitz, E.M.; Dominici, M. Challenges in clinical development of mesenchymal stromal/stem cells: Concise review. Stem Cells Transl. Med., 2019, 8(11), 1135-1148. doi: 10.1002/sctm.19-0044 PMID: 31313507
- Yan, G.; Fan, Y.; Li, P.; Zhang, Y.; Wang, F. Ectopic expression of DAZL gene in goat bone marrow-derived mesenchymal stem cells enhances the trans-differentiation to putative germ cells compared to the exogenous treatment of retinoic acid or bone morphogenetic protein 4 signalling molecules. Cell Biol. Int., 2015, 39(1), 74-83. doi: 10.1002/cbin.10348 PMID: 25052690
- Salem, M.; Mirzapour, T.; Bayrami, A.; Sagha, M. Germ cell differentiation of bone marrow mesenchymal stem cells. Andrologia, 2019, 51(4), e13229. doi: 10.1111/and.13229 PMID: 30746735
- Drusenheimer, N.; Wulf, G.; Nolte, J.; Lee, J.H.; Dev, A.; Dressel, R.; Gromoll, J.; Schmidtke, J.; Engel, W.; Nayernia, K. Putative human male germ cells from bone marrow stem cells. Soc. Reprod. Fertil. Suppl., 2007, 63, 69-76. PMID: 17566262
- Mazaheri, Z.; Movahedin, M.; Rahbarizadeh, F.; Amanpour, S. Different doses of bone morphogenetic protein 4 promote the expression of early germ cell-specific gene in bone marrow mesenchymal stem cells. In vitro Cell. Dev. Biol. Anim., 2011, 47(8), 521-525. doi: 10.1007/s11626-011-9429-0 PMID: 21717271
- Shirazi, R.; Zarnani, A.H.; Soleimani, M.; Abdolvahabi, M.A.; Nayernia, K.; Kashani, I.R. BMP4 can generate primordial germ cells from bone-marrow-derived pluripotent stem cells. Cell Biol. Int., 2012, 36(12), 1185-1193. doi: 10.1042/CBI20110651 PMID: 22988836
- Shirzeyli, M.H.; Khanlarkhani, N.; Amidi, F.; Shirzeyli, F.H.; Aval, F.S.; Sobhani, A. Bones Morphogenic Protein-4 and retinoic acid combined treatment comparative analysis for in vitro differentiation potential of murine mesenchymal stem cells derived from bone marrow and adipose tissue into germ cells. Microsc. Res. Tech., 2017, 80(11), 1151-1160. doi: 10.1002/jemt.22880 PMID: 28921810
- Behzadi Fard, S.; Mazaheri, Z.; Ghorbanmehr, N.; Movahedin, M.; Behzadi Fard, M.; Gholampour, M.A. Analysis of MiRNA-17 and MiRNA-146 expression during differentiation of spermatogonial stem like cells derived from mouse bone marrow mesenchymal stem cells. Int. J. Mol. Cell. Med., 2019, 8(1), 14-23. PMID: 32195202
- Nayernia, K.; Lee, J.H.; Drusenheimer, N.; Nolte, J.; Wulf, G.; Dressel, R.; Gromoll, J.; Engel, W. Derivation of male germ cells from bone marrow stem cells. Lab. Invest., 2006, 86(7), 654-663. doi: 10.1038/labinvest.3700429 PMID: 16652109
- Shirazi, R.; Zarnani, A.H.; Soleimani, M.; Nayernia, K.; Ragerdi Kashani, I. Differentiation of bone marrow-derived stage-specific embryonic antigen 1 positive pluripotent stem cells into male germ cells. Microsc. Res. Tech., 2017, 80(4), 430-440. doi: 10.1002/jemt.22812 PMID: 27990704
- Monfared, M.H.; Minaee, B.; Rastegar, T.; Khrazinejad, E.; Barbarestani, M. Sertoli cell condition medium can induce germ like cells from bone marrow derived mesenchymal stem cells. Iran. J. Basic Med. Sci., 2016, 19(11), 1186-1192. PMID: 27917274
- Ghorbanlou, M.; Abdanipour, A.; Shirazi, R.; Malekmohammadi, N.; Shokri, S.; Nejatbakhsh, R. Indirect co-culture of testicular cells with bone marrow mesenchymal stem cells leads to male germ cell-specific gene expressions. Cell J., 2019, 20(4), 505-512. PMID: 30123996
- Abdel Aziz, M.T.; Mostafa, T.; Atta, H.; Asaad, S.; Fouad, H.H.; Mohsen, G.; Rashed, L.; Sabry, D.; Abbas, M. In vitro and in vivo lineage conversion of bone marrow stem cells into germ cells in experimental Azoospermia in rat. Stem Cell Stud., 2011, 1(1), 15. doi: 10.4081/scs.2011.e15
- Kumar, K. Rat bone marrow derived mesenchymal stem cells differentiate to germ cell like cells. bioRxiv, 2018, 418962. doi: 10.1101/418962
- Ghasemzadeh-Hasankolaei, M.; Eslaminejad, M.B.; Sedighi-Gilani, M. Derivation of male germ cells from ram bone marrow mesenchymal stem cells by three different methods and evaluation of their fate after transplantation into the testis. In Vitro Cell Dev Biol Anim., 2016, 52(1), 49-61. doi: 10.1007/s11626-015-9945-4 PMID: 26395124
- Ghasemzadeh-Hasankolaei, M.; Eslaminejad, M.B.; Batavani, R.; Sedighi-Gilani, M. Comparison of the efficacy of three concentrations of retinoic acid for transdifferentiation induction in sheep marrow-derived mesenchymal stem cells into male germ cells. Andrologia, 2014, 46(1), 24-35. doi: 10.1111/and.12037 PMID: 23131047
- Hua, J.; Pan, S.; Yang, C.; Dong, W.; Dou, Z.; Sidhu, K.S. Derivation of male germ cell-like lineage from human fetal bone marrow stem cells. Reprod. Biomed. Online, 2009, 19(1), 99-105. doi: 10.1016/S1472-6483(10)60052-1 PMID: 19573297
- Bräunig, P.; Glanzner, W.G.; Rissi, V.B.; Gonçalves, P.B.D. The differentiation potential of adipose tissue-derived mesenchymal stem cells into cell lineage related to male germ cells. Arq. Bras. Med. Vet. Zootec., 2018, 70(1), 160-168. doi: 10.1590/1678-4162-9132
- Jinlian, H. Multipotent mesenchymal stem cells (MSCs) from human umbilical cord: potential differentiation of germ cells. Afr. J. Biochem. Res., 2011, 5(4), 113-123.
- Latifpour, M.; Shakiba, Y.; Amidi, F.; Mazaheri, Z.; Sobhani, A. Differentiation of human umbilical cord matrix-derived mesenchymal stem cells into germ-like cells. Avicenna J. Med. Biotechnol., 2014, 6(4), 218-227. PMID: 25414784
- Li, N.; Pan, S.; Zhu, H.; Mu, H.; Liu, W.; Hua, J. BMP4 promotes SSEA-1 +HUC-MSC differentiation into male germ-like cells in vitro. Cell Prolif., 2014, 47(4), 299-309. doi: 10.1111/cpr.12115 PMID: 24923741
- Nejad, N.A.; Amidi, F.; Hoseini, M.A.; Nia, K.N.; Habibi, M.; Kajbafzadeh, A.M.; Mazaheri, Z.; Yamini, N. Male germ-like cell differentiation potential of human umbilical cord Whartons jelly-derived mesenchymal stem cells in co-culture with human placenta cells in presence of BMP4 and retinoic acid. Iran. J. Basic Med. Sci., 2015, 18(4), 325-333. PMID: 26019794
- Dissanayake, D.M.A.B.; Patel, H.; Wijesinghe, P.S. Differentiation of human male germ cells from Whartons jelly-derived mesenchymal stem cells. Clin. Exp. Reprod. Med., 2018, 45(2), 75-81. doi: 10.5653/cerm.2018.45.2.75 PMID: 29984207
- Ghaem Maghami, R.; Mirzapour, T.; Bayrami, A. Differentiation of mesenchymal stem cells to germ-like cells under induction of Sertoli cell-conditioned medium and retinoic acid. Andrologia, 2018, 50(3), e12887. doi: 10.1111/and.12887 PMID: 28944567
- Hua, J.; Yu, H.; Dong, W.; Yang, C.; Gao, Z.; Lei, A.; Sun, Y.; Pan, S.; Wu, Y.; Dou, Z. Characterization of mesenchymal stem cells (MSCs) from human fetal lung: Potential differentiation of germ cells. Tissue Cell, 2009, 41(6), 448-455. doi: 10.1016/j.tice.2009.05.004 PMID: 19651422
- Tamadon, A.; Mehrabani, D.; Rahmanifar, F.; Jahromi, A.R.; Panahi, M.; Zare, S.; Khodabandeh, Z.; Jahromi, I.R.; Tanideh, N.; Dianatpour, M.; Ramzi, M.; Koohi-Hoseinabadi, O. Induction of spermatogenesis by bone marrow-derived mesenchymal stem cells in busulfan-induced azoospermia in hamste. Int. J. Stem Cells, 2015, 8(2), 134-145. doi: 10.15283/ijsc.2015.8.2.134 PMID: 26634062
- Lue, Y.; Erkkila, K.; Liu, P.Y.; Ma, K.; Wang, C.; Hikim, A.S.; Swerdloff, R.S. Fate of bone marrow stem cells transplanted into the testis: potential implication for men with testicular failure. Am. J. Pathol., 2007, 170(3), 899-908. doi: 10.2353/ajpath.2007.060543 PMID: 17322375
- Sherif, I.O.; Sabry, D.; Abdel-Aziz, A.; Sarhan, O.M. The role of mesenchymal stem cells in chemotherapy-induced gonadotoxicity. Stem Cell Res. Ther., 2018, 9(1), 196. doi: 10.1186/s13287-018-0946-6 PMID: 30021657
- Ghasemzadeh-Hasankolaei, M.; Batavani, R.; Eslaminejad, M.B.; 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(2), 250-263. doi: 10.15283/ijsc16010 PMID: 27430978
- Zahkook, S. Mesenchymal stem cells restore fertility in induced azoospermic rats following chemotherapy administration. J. Reprod. Infertil., 2014, 5(2), 50-57.
- Rahmanifar, F.; Tamadon, A.; Mehrabani, D.; Zare, S.; Abasi, S.; Keshavarz, S.; Dianatpour, M.; Khodabandeh, Z.; Jahromi, I.R.; Koohi-Hoseinabadi, O. 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(6), 653-661. PMID: 27482347
- Zhou, X.Y.; Ma, Y.Z.; Wang, X.H.; Liu, D.J.; Ren, Y.; Ji, X.P. Bone marrow mesenchymal stem cells to repair the reproductive system of male azoospermia rats. Zhonghua Nan Ke Xue, 2015, 21(8), 692-697. PMID: 26442294
- 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(7), 537-544. PMID: 24639788
- Hassan, A.I.; Alam, S.S. Evaluation of mesenchymal stem cells in treatment of infertility in male rats. Stem Cell Res. Ther., 2014, 5(6), 131. doi: 10.1186/scrt521 PMID: 25422144
- Wang, F.; Liu, C.; Zhang, S.; Liu, W.; Hua, J. Transplantation of goat bone marrow mesenchymal stem cells (gMSCs) help restore spermatogenesis in endogenous germ cells-depleted mouse models. J. Integr. Agric., 2013, 12(3), 483-494. doi: 10.1016/S2095-3119(13)60249-X
- Tamadon, A.; Mehrabani, D.; Hassanshahi, M.A.; Zare, S.; Keshavarz, S.; Rahmanifar, F.; Dianatpour, M.; Khodabandeh, Z.; Jahromi, I.; Tanideh, N.; Ramzi, M.; Aqababa, H.; Kuhi-Hoseinabadi, O. Adipose tissue-derived mesenchymal stem cells repair germinal cells of seminiferous tubules of busulfan-induced azoospermic rats. J. Hum. Reprod. Sci., 2015, 8(2), 103-110. doi: 10.4103/0974-1208.158618 PMID: 26157302
补充文件
