Is It Possible to Treat Infertility with Stem Cells?
Adult Germline Stem Cells
/ transplantation
Animals
Cell Culture Techniques, Three Dimensional
Fallopian Tubes
/ physiology
Female
Humans
Infertility
/ therapy
Infertility, Female
/ etiology
Infertility, Male
/ therapy
Male
Mesenchymal Stem Cells
Mitochondria
/ transplantation
Oocytes
/ physiology
Oogenesis
Pregnancy
Primary Ovarian Insufficiency
/ complications
Regeneration
Spermatogenesis
Stem Cell Transplantation
Stem Cells
/ physiology
Uterus
/ physiology
Cell transplantation
Fertilization in vitro
Gametogenesis in vitro
Infertility
Reproductive medicine
Stem cells
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:
06 2021
06 2021
Historique:
received:
23
01
2021
accepted:
31
03
2021
pubmed:
10
4
2021
medline:
15
12
2021
entrez:
9
4
2021
Statut:
ppublish
Résumé
Infertility is a major health problem, and despite improved treatments over the years, there are still some conditions that cannot be treated successfully using a conventional approach. Therefore, new options are being considered and one of them is cell therapy using stem cells. Stem cell treatments for infertility can be divided into two major groups, the first one being direct transplantation of stem cells or their paracrine factors into reproductive organs and the second one being in vitro differentiation into germ cells or gametes. In animal models, all of these approaches were able to improve the reproductive potential of tested animals, although in humans there is still too little evidence to suggest successful use. The reasons for lack of evidence are unavailability of proper material, the complexity of explored biological processes, and ethical considerations. Despite all of the above-mentioned hurdles, researchers were able to show that in women, it seems to be possible to improve some conditions, but in men, no similar clinically important improvement was achieved. To conclude, the data presented in this review suggest that the treatment of infertility with stem cells seems plausible, because some types of treatments have already been tested in humans, achieving live births, while others show great potential only in animal studies, for now.
Identifiants
pubmed: 33834375
doi: 10.1007/s43032-021-00566-7
pii: 10.1007/s43032-021-00566-7
doi:
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
1733-1745Références
Zegers-Hochschild F, Adamson GD, Dyer S, Racowsky C, de Mouzon J, Sokol R, et al. The international glossary on infertility and fertility care. Fertil Steril. 2017;108(3):393–406.
pubmed: 28760517
Beke A. Genetic causes of female infertility. Exp Suppl. 2019;111:367–83.
pubmed: 31588540
Deroux A, Dumestre-Perard C, Dunand-Faure C, Bouillet L, Female HP. Infertility and serum auto-antibodies: a systematic review. Clin Rev Allergy Immunol. 2017;53(1):78–86.
pubmed: 27628237
Zhao YX, Chen SR, Su PP, Huang FH, Shi YC, Shi QY, et al. Using mesenchymal stem cells to treat female infertility: an update on female reproductive diseases. Stem Cells Int. 2019;2019:9071720.
pubmed: 31885630
pmcid: 6925937
Jahanbani Y, Davaran S, Ghahremani-Nasab M, Aghebati-Maleki L, Yousefi M. Scaffold-based tissue engineering approaches in treating infertility. Life Sci. 2020;240:117066.
pubmed: 31738881
Vander Borght M, Wyns C. Fertility and infertility: definition and epidemiology. Clin Biochem. 2018;62:2–10.
pubmed: 29555319
Watt FM, Driskell RR. The therapeutic potential of stem cells. Philos Trans R Soc Lond B Biol Sci. 2010;365(1537):155–63.
pubmed: 20008393
pmcid: 2842697
Odorico JS, Kaufman DS, Thomson JA. Multilineage differentiation from human embryonic stem cell lines. Stem Cells. 2001;19(3):193–204.
pubmed: 11359944
Lazarini F, Gabellec MM, Moigneu C, de Chaumont F, Olivo-Marin JC, Lledo PM. Adult neurogenesis restores dopaminergic neuronal loss in the olfactory bulb. J Neurosci. 2014;34(43):14430–42.
pubmed: 25339754
pmcid: 6608394
Ozakpinar OB, Maurer AM, Ozsavci D. Ovarian stem cells: from basic to clinical applications. World J Stem Cells. 2015;7(4):757–68.
pubmed: 26029346
pmcid: 4444615
Bao R, Xu P, Wang Y, Wang J, Xiao L, Li G, et al. Bone marrow derived mesenchymal stem cells transplantation rescues premature ovarian insufficiency induced by chemotherapy. Gynecol Endocrinol. 2018;34(4):320–6.
pubmed: 29073798
Song D, Zhong Y, Qian C, Zou Q, Ou J, Shi Y, et al. Human umbilical cord mesenchymal stem cells therapy in cyclophosphamide-induced premature ovarian failure rat model. Biomed Res Int. 2016;2016:2517514.
pubmed: 27047962
pmcid: 4800076
Liu R, Zhang X, Fan Z, Wang Y, Yao G, Wan X, et al. Human amniotic mesenchymal stem cells improve the follicular microenvironment to recover ovarian function in premature ovarian failure mice. Stem Cell Res Ther. 2019;10(1):299.
pubmed: 31578152
pmcid: 6775662
Herraiz S, Pellicer N, Romeu M, Pellicer A. Treatment potential of bone marrow-derived stem cells in women with diminished ovarian reserves and premature ovarian failure. Curr Opin Obstet Gynecol. 2019;31(3):156–62.
pubmed: 30855290
Yang Z, Du X, Wang C, Zhang J, Liu C, Li Y, et al. Therapeutic effects of human umbilical cord mesenchymal stem cell-derived microvesicles on premature ovarian insufficiency in mice. Stem Cell Res Ther. 2019;10(1):250.
pubmed: 31412919
pmcid: 6693188
Li J, Mao Q, He J, She H, Zhang Z, Yin C. Human umbilical cord mesenchymal stem cells improve the reserve function of perimenopausal ovary via a paracrine mechanism. Stem Cell Res Ther. 2017;8(1):55.
pubmed: 28279229
pmcid: 5345137
Shen J, Cao D, Sun JL. Ability of human umbilical cord mesenchymal stem cells to repair chemotherapy-induced premature ovarian failure. World J Stem Cells. 2020;12(4):277–87.
pubmed: 32399136
pmcid: 7202924
Zhang X, Zhang L, Li Y, Yin Z, Feng Y, Ji Y. Human umbilical cord mesenchymal stem cells (hUCMSCs) promotes the recovery of ovarian function in a rat model of premature ovarian failure (POF). Gynecol Endocrinol. 2021:1–5. https://doi.org/10.1080/09513590.2021.1878133 Epub ahead of print.
Zheng Q, Fu X, Jiang J, Zhang N, Zou L, Wang W, et al. Umbilical cord mesenchymal stem cell transplantation prevents chemotherapy-induced ovarian failure via the NGF/TrkA pathway in rats. Biomed Res Int. 2019;2019:6539294.
pubmed: 31240219
pmcid: 6556346
Cui L, Bao H, Liu Z, Man X, Liu H, Hou Y, et al. hUMSCs regulate the differentiation of ovarian stromal cells via TGF-β
pubmed: 32894203
pmcid: 7487655
Wang Z, Wei Q, Wang H, Han L, Dai H, Qian X, et al. Mesenchymal stem cell therapy using human umbilical cord in a rat model of autoimmune-induced premature ovarian failure. Stem Cells Int. 2020;2020:3249495.
pubmed: 32714395
pmcid: 7355366
Sun L, Li D, Song K, Wei J, Yao S, Li Z, et al. Exosomes derived from human umbilical cord mesenchymal stem cells protect against cisplatin-induced ovarian granulosa cell stress and apoptosis in vitro. Sci Rep. 2017;7(1):2552.
pubmed: 28566720
pmcid: 5451424
Hong L, Yan L, Xin Z, Hao J, Liu W, Wang S, et al. Protective effects of human umbilical cord mesenchymal stem cell-derived conditioned medium on ovarian damage. J Mol Cell Biol. 2020;12(5):372–85.
pubmed: 31742349
Zhang Q, Bu S, Sun J, Xu M, Yao X, He K, et al. Paracrine effects of human amniotic epithelial cells protect against chemotherapy-induced ovarian damage. Stem Cell Res Ther. 2017;8(1):270.
pubmed: 29179771
pmcid: 5704397
Ding C, Zou Q, Wang F, Wu H, Chen R, Lv J, et al. Human amniotic mesenchymal stem cells improve ovarian function in natural aging through secreting hepatocyte growth factor and epidermal growth factor. Stem Cell Res Ther. 2018;9(1):55.
pubmed: 29523193
pmcid: 5845161
Ling L, Feng X, Wei T, Wang Y, Wang Y, Wang Z, et al. Human amnion-derived mesenchymal stem cell (hAD-MSC) transplantation improves ovarian function in rats with premature ovarian insufficiency (POI) at least partly through a paracrine mechanism. Stem Cell Res Ther. 2019;10(1):46.
pubmed: 30683144
pmcid: 6347748
Feng X, Ling L, Zhang W, Liu X, Wang Y, Luo Y, et al. Effects of human amnion-derived mesenchymal stem cell (hAD-MSC) transplantation in situ on primary ovarian insufficiency in SD rats. Reprod Sci. 2020;27(7):1502–12.
pubmed: 31953773
Cho J, Kim TH, Seok J, Jun JH, Park H, Kweon M, et al. Vascular remodeling by placenta-derived mesenchymal stem cells restores ovarian function in ovariectomized rat model via the VEGF pathway. Lab Invest. 2021;101(3):304–17.
pubmed: 33303971
Seok J, Park H, Choi JH, Lim JY, Kim KG, Kim GJ. Placenta-derived mesenchymal stem cells restore the ovary function in an ovariectomized rat model via an antioxidant effect. Antioxidants (Basel). 2020;9(7):591.
Li H, Zhao W, Wang L, Luo Q, Yin N, Lu X, et al. Human placenta-derived mesenchymal stem cells inhibit apoptosis of granulosa cells induced by IRE1α pathway in autoimmune POF mice. Cell Biol Int. 2019;43(8):899–909.
pubmed: 31081266
Kim KH, Kim EY, Kim GJ, Ko JJ, Cha KY, Koong MK, et al. Human placenta-derived mesenchymal stem cells stimulate ovarian function via miR-145 and bone morphogenetic protein signaling in aged rats. Stem Cell Res Ther. 2020;11(1):472.
pubmed: 33153492
pmcid: 7643421
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):486.
pubmed: 33198818
pmcid: 7667861
Ding C, Zou Q, Wang F, Wu H, Wang W, Li H, et al. HGF and BFGF secretion by human adipose-derived stem cells improves ovarian function during natural aging via activation of the SIRT1/FOXO1 signaling pathway. Cell Physiol Biochem. 2018;45(4):1316–32.
pubmed: 29462806
Terraciano P, Garcez T, Ayres L, Durli I, Baggio M, Kuhl CP, et al. Cell therapy for chemically induced ovarian failure in mice. Stem Cells Int. 2014;2014:720753.
pubmed: 25548574
pmcid: 4274854
Sun M, Wang S, Li Y, Yu L, Gu F, Wang C, et al. Adipose-derived stem cells improved mouse ovary function after chemotherapy-induced ovary failure. Stem Cell Res Ther. 2013;4(4):80.
pubmed: 23838374
pmcid: 3854877
Takehara Y, Yabuuchi A, Ezoe K, Kuroda T, Yamadera R, Sano C, et al. The restorative effects of adipose-derived mesenchymal stem cells on damaged ovarian function. Lab Invest. 2013;93(2):181–93.
pubmed: 23212100
Su J, Ding L, Cheng J, Yang J, Li X, Yan G, et al. Transplantation of adipose-derived stem cells combined with collagen scaffolds restores ovarian function in a rat model of premature ovarian insufficiency. Hum Reprod. 2016;31(5):1075–86.
pubmed: 26965432
Shojafar E, Soleimani Mehranjani M, Shariatzadeh SMA. Adipose derived mesenchymal stem cells improve the structure and function of autografted mice ovaries through reducing oxidative stress and inflammation: a stereological and biochemical analysis. Tissue Cell. 2019;56:23–30.
pubmed: 30736901
Manavella DD, Cacciottola L, Payen VL, Amorim CA, Donnez J, Dolmans MM. Adipose tissue-derived stem cells boost vascularization in grafted ovarian tissue by growth factor secretion and differentiation into endothelial cell lineages. Mol Hum Reprod. 2019;25(4):184–93.
pubmed: 30824937
Mehdinia Z, Ashrafi M, Fathi R, Taheri P, Valojerdi MR. Restoration of estrous cycles by co-transplantation of mouse ovarian tissue with MSCs. Cell Tissue Res. 2020;381(3):509–25.
pubmed: 32424509
Gabr H, Rateb MA, El Sissy MH, Ahmed Seddiek H, Ali Abdelhameed Gouda S. The effect of bone marrow-derived mesenchymal stem cells on chemotherapy induced ovarian failure in albino rats. Microsc Res Tech. 2016;79(10):938–47.
pubmed: 27453009
Badawy A, Sobh MA, Ahdy M, Abdelhafez MS. Bone marrow mesenchymal stem cell repair of cyclophosphamide-induced ovarian insufficiency in a mouse model. Int J Womens Health. 2017;9:441–7.
pubmed: 28670143
pmcid: 5479293
Mohamed SA, Shalaby SM, Abdelaziz M, Brakta S, Hill WD, Ismail N, et al. Human mesenchymal stem cells partially reverse infertility in chemotherapy-induced ovarian failure. Reprod Sci. 2018;25(1):51–63.
pubmed: 28460567
Wang Z, Yang T, Liu S, Chen Y. Effects of bone marrow mesenchymal stem cells on ovarian and testicular function in aging Sprague-Dawley rats induced by D-galactose. Cell Cycle. 2020;20:1–11.
Grady ST, Watts AE, Thompson JA, Penedo MCT, Konganti K, Hinrichs K. Effect of intra-ovarian injection of mesenchymal stem cells in aged mares. J Assist Reprod Genet. 2019;36(3):543–56.
pubmed: 30470961
Zarbakhsh S, Safari R, Sameni HR, Yousefi B, Safari M, Khanmohammadi N, et al. Effects of co-administration of bone marrow stromal cells and L-carnitine on the recovery of damaged ovaries by performing chemotherapy model in rat. Int J Fertil Steril. 2019;13(3):196–202.
pubmed: 31310073
pmcid: 6642421
Sameni HR, Seiri M, Safari M, Tabrizi Amjad MH, Khanmohammadi N, Zarbakhsh S. Bone marrow stromal cells with the granulocyte colony-stimulating factor in the management of chemotherapy-induced ovarian failure in a rat model. Iran J Med Sci. 2019;44(2):135–45.
pubmed: 30936600
Volkova N, Yukhta M, Goltsev A. Mesenchymal stem cells in restoration of fertility at experimental pelvic inflammatory disease. Stem Cells Int. 2017;2017:2014132.
pubmed: 28928773
pmcid: 5591961
Kalhori Z, Azadbakht M, Soleimani Mehranjani M, Shariatzadeh MA. Improvement of the folliculogenesis by transplantation of bone marrow mesenchymal stromal cells in mice with induced polycystic ovary syndrome. Cytotherapy. 2018;20(12):1445–58.
pubmed: 30523787
Edessy M, Hosni HN, Shady Y, Waf Y, Bakr S, Kamel M. Autologous stem cells therapy, the first baby of idiopathic premature ovarian failure. Acta Med Int. 2016;3:19–23.
Gupta S, Lodha P, Karthick MS, Tandulwadkar SR. Role of autologous bone marrow-derived stem cell therapy for follicular recruitment in premature ovarian insufficiency: review of literature and a case report of world’s first baby with ovarian autologous stem cell therapy in a perimenopausal woman of age 45 year. J Hum Reprod Sci. 2018;11(2):125–30.
pubmed: 30158807
pmcid: 6094531
Igboeli P, El Andaloussi A, Sheikh U, Takala H, ElSharoud A, McHugh A, et al. Intraovarian injection of autologous human mesenchymal stem cells increases estrogen production and reduces menopausal symptoms in women with premature ovarian failure: two case reports and a review of the literature. J Med Case Rep. 2020;14(1):108.
pubmed: 32680541
pmcid: 7368722
Herraiz S, Romeu M, Buigues A, Martínez S, Díaz-García C, Gómez-Seguí I, et al. Autologous stem cell ovarian transplantation to increase reproductive potential in patients who are poor responders. Fertil Steril. 2018;110(3):496–505.
pubmed: 29960701
Shin DM, Liu R, Klich I, Wu W, Ratajczak J, Kucia M, et al. Molecular signature of adult bone marrow-purified very small embryonic-like stem cells supports their developmental epiblast/germ line origin. Leukemia. 2010;24(8):1450–61.
pubmed: 20508611
Magnúsdóttir E, Surani MA. How to make a primordial germ cell. Development. 2014;141(2):245–52.
pubmed: 24381195
Hackett JA, Zylicz JJ, Surani MA. Parallel mechanisms of epigenetic reprogramming in the germline. Trends Genet. 2012;28(4):164–74.
pubmed: 22386917
Morohaku K, Tanimoto R, Sasaki K, Kawahara-Miki R, Kono T, Hayashi K, et al. Complete in vitro generation of fertile oocytes from mouse primordial germ cells. Proc Natl Acad Sci U S A. 2016;113(32):9021–6.
pubmed: 27457928
pmcid: 4987791
Hayashi K, Ogushi S, Kurimoto K, Shimamoto S, Ohta H, Saitou M. Offspring from oocytes derived from in vitro primordial germ cell-like cells in mice. Science. 2012;338(6109):971–5.
pubmed: 23042295
Hikabe O, Hamazaki N, Nagamatsu G, Obata Y, Hirao Y, Hamada N, et al. Reconstitution in vitro of the entire cycle of the mouse female germ line. Nature. 2016;539(7628):299–303.
pubmed: 27750280
Ohta H, Kurimoto K, Okamoto I, Nakamura T, Yabuta Y, Miyauchi H, et al. In vitro expansion of mouse primordial germ cell-like cells recapitulates an epigenetic blank slate. EMBO J. 2017;36(13):1888–907.
pubmed: 28559416
pmcid: 5494472
Irie N, Weinberger L, Tang WW, Kobayashi T, Viukov S, Manor YS, et al. SOX17 is a critical specifier of human primordial germ cell fate. Cell. 2015;160(1-2):253–68.
pubmed: 25543152
pmcid: 4310934
Sasaki K, Yokobayashi S, Nakamura T, Okamoto I, Yabuta Y, Kurimoto K, et al. Robust in vitro induction of human germ cell fate from pluripotent stem cells. Cell Stem Cell. 2015;17(2):178–94.
pubmed: 26189426
White YA, Woods DC, Takai Y, Ishihara O, Seki H, Tilly JL. Oocyte formation by mitotically active germ cells purified from ovaries of reproductive-age women. Nat Med. 2012;18(3):413–21.
pubmed: 22366948
pmcid: 3296965
Zhang H, Panula S, Petropoulos S, Edsgärd D, Busayavalasa K, Liu L, et al. Adult human and mouse ovaries lack DDX4-expressing functional oogonial stem cells. Nat Med. 2015;21(10):1116–8.
pubmed: 26444631
Silvestris E, Cafforio P, D’Oronzo S, Felici C, Silvestris F, Loverro G. In vitro differentiation of human oocyte-like cells from oogonial stem cells: single-cell isolation and molecular characterization. Hum Reprod. 2018;33(3):464–73.
pubmed: 29304224
Virant-Klun I, Rozman P, Cvjeticanin B, Vrtacnik-Bokal E, Novakovic S, Rülicke T, et al. Parthenogenetic embryo-like structures in the human ovarian surface epithelium cell culture in postmenopausal women with no naturally present follicles and oocytes. Stem Cells Dev. 2009;18(1):137–49.
pubmed: 18605894
Esmaeilian Y, Atalay A, Erdemli E. Putative germline and pluripotent stem cells in adult mouse ovary and their in vitro differentiation potential into oocyte-like and somatic cells. Zygote. 2017;25(3):358–75.
pubmed: 28669362
Bhartiya D, Sharma D. Ovary does harbor stem cells - size of the cells matter! J Ovarian Res. 2020;13(1):39.
pubmed: 32303227
pmcid: 7164193
Bharti D, Jang SJ, Lee SY, Lee SL, Rho GJ. In vitro generation of oocyte like cells and their in vivo efficacy: how far we have been succeeded. Cells. 2020;9(3):557.
pmcid: 7140496
Zuo W, Xie B, Li C, Yan Y, Zhang Y, Liu W, et al. The clinical applications of endometrial mesenchymal stem cells. Biopreserv Biobank. 2018;16(2):158–64 29265881.
pubmed: 29265881
pmcid: 5906727
Cervelló I, Mas A, Gil-Sanchis C, Peris L, Faus A, Saunders PT, et al. Reconstruction of endometrium from human endometrial side population cell lines. PLoS One. 2011;6(6):e21221.
pubmed: 21712999
pmcid: 3119688
Gargett CE, Schwab KE, Zillwood RM, Nguyen HP, Wu D. Isolation and culture of epithelial progenitors and mesenchymal stem cells from human endometrium. Biol Reprod. 2009;80(6):1136–45.
pubmed: 19228591
pmcid: 2849811
Gargett CE, Nguyen HP, Ye L. Endometrial regeneration and endometrial stem/progenitor cells. Rev Endocr Metab Disord. 2012;13(4):235–51.
pubmed: 22847235
Liu Y, Zhang Z, Yang F, Wang H, Liang S, Wang H, et al. The role of endometrial stem cells in the pathogenesis of endometriosis and their application to its early diagnosis†. Biol Reprod. 2020;102(6):1153–9.
pubmed: 31965165
Simoni M, Taylor HS. Therapeutic strategies involving uterine stem cells in reproductive medicine. Curr Opin Obstet Gynecol. 2018;30(3):209–16.
pubmed: 29652725
Aghajanova L, Horcajadas JA, Esteban FJ, Giudice LC. The bone marrow-derived human mesenchymal stem cell: potential progenitor of the endometrial stromal fibroblast. Biol Reprod. 2010;82(6):1076–87.
pubmed: 20147733
pmcid: 2874495
Nagori CB, Panchal SY, Patel H. Endometrial regeneration using autologous adult stem cells followed by conception by in vitro fertilization in a patient of severe Asherman’s syndrome. J Hum Reprod Sci. 2011;4(1):43–8.
pubmed: 21772740
pmcid: 3136069
Singh N, Mohanty S, Seth T, Shankar M, Bhaskaran S, Dharmendra S. Autologous stem cell transplantation in refractory Asherman’s syndrome: a novel cell based therapy. J Hum Reprod Sci. 2014;7(2):93–8.
pubmed: 25191021
pmcid: 4150149
Santamaria X, Cabanillas S, Cervelló I, Arbona C, Raga F, Ferro J, et al. Autologous cell therapy with CD133+ bone marrow-derived stem cells for refractory Asherman’s syndrome and endometrial atrophy: a pilot cohort study. Hum Reprod. 2016;31(5):1087–96.
pubmed: 27005892
Cao Y, Sun H, Zhu H, Zhu X, Tang X, Yan G, et al. Allogeneic cell therapy using umbilical cord MSCs on collagen scaffolds for patients with recurrent uterine adhesion: a phase I clinical trial. Stem Cell Res Ther. 2018;9(1):192.
pubmed: 29996892
pmcid: 6042450
Tan J, Li P, Wang Q, Li Y, Li X, Zhao D, et al. Autologous menstrual blood-derived stromal cells transplantation for severe Asherman’s syndrome. Hum Reprod. 2016;31(12):2723–9.
pubmed: 27664218
Sudoma I, Pylyp L, Kremenska Y, Goncharova Y. Application of autologous adipose-derived stem cells for thin endometrium treatment in patients with failed ART programs. J Stem Cell Ther Transplant. 2019;3:001–8.
Lee SY, Shin JE, Kwon H, Choi DH, Kim JH. Effect of autologous adipose-derived stromal vascular fraction transplantation on endometrial regeneration in patients of Asherman’s syndrome: a pilot study. Reprod Sci. 2020;27(2):561–8.
pubmed: 32046396
Jazedje T, Perin PM, Czeresnia CE, Maluf M, Halpern S, Secco M, et al. Human fallopian tube: a new source of multipotent adult mesenchymal stem cells discarded in surgical procedures. J Transl Med. 2009;7:46.
pubmed: 19538712
pmcid: 2714040
Snegovskikh V, Mutlu L, Massasa E, Taylor HS. Identification of putative fallopian tube stem cells. Reprod Sci. 2014;21(12):1460–4.
pubmed: 25305130
pmcid: 4231131
Chang YH, Chu TY, Ding DC. Human fallopian tube epithelial cells exhibit stemness features, self-renewal capacity, and Wnt-related organoid formation. J Biomed Sci. 2020;27(1):32.
pubmed: 32035490
pmcid: 7007656
Zhu M, Iwano T, Takeda S. Fallopian tube basal stem cells reproducing the epithelial sheets in vitro-stem cell of fallopian epithelium. Biomolecules. 2020;10(9):1270.
pmcid: 7565394
Kessler M, Hoffmann K, Brinkmann V, Thieck O, Jackisch S, Toelle B, et al. The notch and Wnt pathways regulate stemness and differentiation in human fallopian tube organoids. Nat Commun. 2015;6:8989.
pubmed: 26643275
pmcid: 4686873
Yucer N, Holzapfel M, Jenkins Vogel T, Lenaeus L, Ornelas L, Laury A, et al. Directed differentiation of human induced pluripotent stem cells into fallopian tube epithelium. Sci Rep. 2017;7(1):10741.
pubmed: 28878359
pmcid: 5587694
Li Z, Zhang Z, Chen X, Zhou J, Xiao XM. Treatment evaluation of Wharton’s jelly-derived mesenchymal stem cells using a chronic salpingitis model: an animal experiment. Stem Cell Res Ther. 2017;8(1):232.
pubmed: 29041961
pmcid: 5645885
Liao W, Tang X, Li X, Li T. Therapeutic effect of human umbilical cord mesenchymal stem cells on tubal factor infertility using a chronic salpingitis murine model. Arch Gynecol Obstet. 2019;300(2):421–9.
pubmed: 31190174
Li Z, Zhang Z, Ming WK, Chen X, Xiao XM. Tracing GFP-labeled WJMSCs in vivo using a chronic salpingitis model: an animal experiment. Stem Cell Res Ther. 2017;8(1):272.
pubmed: 29191249
pmcid: 5709981
Almasry SM, Elfayomy AK, El-Sherbiny MH. Regeneration of the fallopian tube mucosa using bone marrow mesenchymal stem cell transplantation after induced chemical injury in a rat model. Reprod Sci. 2018;25(5):773–81.
pubmed: 28826366
Labarta E, de Los Santos MJ, Escribá MJ, Pellicer A, Herraiz S. Mitochondria as a tool for oocyte rejuvenation. Fertil Steril. 2019;111(2):219–26.
pubmed: 30611551
Barritt JA, Brenner CA, Malter HE, Cohen J. Mitochondria in human offspring derived from ooplasmic transplantation. Hum Reprod. 2001;16(3):513–6.
pubmed: 11228222
Cohen J, Scott R, Alikani M, Schimmel T, Munné S, Levron J, et al. Ooplasmic transfer in mature human oocytes. Mol Hum Reprod. 1998;4(3):269–80.
pubmed: 9570273
Lanzendorf SE, Mayer JF, Toner J, Oehninger S, Saffan DS, Muasher S. Pregnancy following transfer of ooplasm from cryopreserved-thawed donor oocytes into recipient oocytes. Fertil Steril. 1999;71(3):575–7.
pubmed: 10065803
Woods DC, Tilly JL. Autologous germline mitochondrial energy transfer (AUGMENT) in human assisted reproduction. Semin Reprod Med. 2015;33(6):410–21.
pubmed: 26574741
pmcid: 5545901
Labarta E, de Los Santos MJ, Herraiz S, Escribá MJ, Marzal A, Buigues A, Pellicer A (2019) Autologous mitochondrial transfer as a complementary technique to intracytoplasmic sperm injection to improve embryo quality in patients undergoing in vitro fertilization-a randomized pilot study. Fertil Steril 111(1):86-96
Fakih MH, El Shmoury M, Szeptycki J, dela Cruz DB, Lux C, Verjee S, et al. The AUGMENTSM treatment: physician reported outcomes of the initial global patient experience. JFIV Reprod Med Genet. 2015;3:154.
Oktay K, Baltaci V, Sonmezer M, Turan V, Unsal E, Baltaci A, et al. Oogonial precursor cell-derived autologous mitochondria injection to improve outcomes in women with multiple IVF failures due to low oocyte quality: a clinical translation. Reprod Sci. 2015;22(12):1612–7.
pubmed: 26567266
Amann RP, Howards SS. Daily spermatozoal production and epididymal spermatozoal reserves of the human male. J Urol. 1980;124(2):211–5.
pubmed: 6772801
Cocuzza M, Alvarenga C, Pagani R. The epidemiology and etiology of azoospermia. Clinics (Sao Paulo) 68 Suppl. 2013;1(Suppl 1):15–26.
Mehmood S, Aldaweesh S, Junejo NN, Altaweel WM, Kattan SA, Alhathal N. Microdissection testicular sperm extraction: overall results and impact of preoperative testosterone level on sperm retrieval rate in patients with nonobstructive azoospermia. Urol Ann. 2019;11(3):287–93.
pubmed: 31413508
pmcid: 6676821
Taitson PF, Filho MA, Radaelli MRM. Testicular sperm extraction in men with Sertoli cell-only testicular histology - 1680 cases. JBRA Assist Reprod. 2019;23(3):246–9.
pubmed: 30969740
pmcid: 6724385
von Eckardstein S, Simoni M, Bergmann M, Weinbauer GF, Gassner P, Schepers AG, et al. Serum inhibin B in combination with serum follicle-stimulating hormone (FSH)is a more sensitive marker than serum FSH alone for impaired spermatogenesis in men, but cannot predict the presence of sperm in testicular tissue samples. J Clin Endocrinol Metab. 1999;84(7):2496–501.
Hung AJ, King P, Schlegel PN. Uniform testicular maturation arrest: a unique subset of men with nonobstructive azoospermia. J Urol. 2007;178(2):608–12.
pubmed: 17570432
Brinster RL, Avarbock MR. Germline transmission of donor haplotype following spermatogonial transplantation. Proc Natl Acad Sci U S A. 1994;91(24):11303–7.
pubmed: 7972054
pmcid: 45219
Jafarian A, Lakpour N, Sadeghi MR, Salehkhou S, Akhondi MM. Transplantation of spermatogonial stem cells suspension into rete testis of azoospermia mouse model. Urol J. 2018;15(1):40–7.
pubmed: 29250763
Kanatsu-Shinohara M, Ogonuki N, Matoba S, Ogura A, Shinohara T. Autologous transplantation of spermatogonial stem cells restores fertility in congenitally infertile mice. Proc Natl Acad Sci U S A. 2020;117(14):7837–44.
pubmed: 32229564
pmcid: 7149444
Nagano M, Patrizio P, Brinster RL. Long-term survival of human spermatogonial stem cells in mouse testes. Fertil Steril. 2002;78(6):1225–33.
pubmed: 12477516
Mulder CL, Catsburg LAE, Zheng Y, de Winter-Korver CM, van Daalen SKM, van Wely M, et al. Long-term health in recipients of transplanted in vitro propagated spermatogonial stem cells. Hum Reprod. 2018;33(1):81–90.
pubmed: 29165614
Kanatsu-Shinohara M, Ogonuki N, Inoue K, Miki H, Ogura A, Toyokuni S, et al. Long-term proliferation in culture and germline transmission of mouse male germline stem cells. Biol Reprod. 2003;69(2):612–6.
pubmed: 12700182
Sadri-Ardekani H, Mizrak SC, van Daalen SK, Korver CM, Roepers-Gajadien HL, Koruji M, et al. Propagation of human spermatogonial stem cells in vitro. JAMA. 2009;302(19):2127–34.
pubmed: 19920237
Liu S, Tang Z, Xiong T, Tang W. Isolation and characterization of human spermatogonial stem cells. Reprod Biol Endocrinol. 2011;9:141.
pubmed: 22018465
pmcid: 3235066
Dong L, Gul M, Hildorf S, Pors SE, Kristensen SG, Hoffmann ER, et al. Xeno-free propagation of spermatogonial stem cells from infant boys. Int J Mol Sci. 2019;20(21):5390.
pmcid: 6862004
Goharbakhsh L, Mohazzab A, Salehkhou S, Heidari M, Zarnani AH, Parivar K, et al. Isolation and culture of human spermatogonial stem cells derived from testis biopsy. Avicenna J Med Biotechnol. 2013;5(1):54–61.
pubmed: 23626877
pmcid: 3572707
Valli H, Sukhwani M, Dovey SL, Peters KA, Donohue J, Castro CA, et al. Fluorescence- and magnetic-activated cell sorting strategies to isolate and enrich human spermatogonial stem cells. Fertil Steril. 2014;102(2):566-580.e7.
pubmed: 24890267
pmcid: 4128386
Cai Y, Wang J, Zou K. The progresses of spermatogonial stem cells sorting using fluorescence-activated cell sorting. Stem Cell Rev Rep. 2020;16(1):94–102.
pubmed: 31792769
Sadri-Ardekani H, Akhondi MA, van der Veen F, Repping S, van Pelt AM. In vitro propagation of human prepubertal spermatogonial stem cells. JAMA. 2011;305(23):2416–8.
pubmed: 21673293
Shetty G, Mitchell JM, Meyer JM, Wu Z, Lam TNA, Phan TT, et al. Restoration of functional sperm production in irradiated pubertal rhesus monkeys by spermatogonial stem cell transplantation. Andrology https://doi. 2020;8:1428–41. https://doi.org/10.1111/andr.12807 .
doi: 10.1111/andr.12807
Forbes CM, Flannigan R, Schlegel PN. Spermatogonial stem cell transplantation and male infertility: current status and future directions. Arab J Urol. 2017;16(1):171–80.
pubmed: 29713548
pmcid: 5922182
Sato T, Katagiri K, Gohbara A, Inoue K, Ogonuki N, Ogura A, et al. In vitro production of functional sperm in cultured neonatal mouse testes. Nature. 2011;471(7339):504–7.
pubmed: 21430778
Oblette A, Rives N, Dumont L, Rives A, Verhaeghe F, Jumeau F, et al. Assessment of sperm nuclear quality after in vitro maturation of fresh or frozen/thawed mouse pre-pubertal testes. Mol Hum Reprod. 2017;23(10):674–84.
pubmed: 28962037
Abu Elhija M, Lunenfeld E, Schlatt S, Huleihel M. Differentiation of murine male germ cells to spermatozoa in a soft agar culture system. Asian J Androl. 2012;14(2):285–93.
pubmed: 22057383
Huleihel M, Nourashrafeddin S, Plant TM. Application of three-dimensional culture systems to study mammalian spermatogenesis, with an emphasis on the rhesus monkey (Macaca mulatta). Asian J Androl. 2015;17(6):972–80.
pubmed: 26067870
pmcid: 4814948
Ishikura Y, Yabuta Y, Ohta H, Hayashi K, Nakamura T, Okamoto I, et al. In vitro derivation and propagation of spermatogonial stem cell activity from mouse pluripotent stem cells. Cell Rep. 2016;17(10):2789–804.
pubmed: 27926879
de Michele F, Poels J, Weerens L, Petit C, Evrard Z, Ambroise J, et al. Preserved seminiferous tubule integrity with spermatogonial survival and induction of Sertoli and Leydig cell maturation after long-term organotypic culture of prepubertal human testicular tissue. Hum Reprod. 2016;32(1):32–45.
pubmed: 27927847
Sun M, Yuan Q, Niu M, Wang H, Wen L, Yao C, et al. Efficient generation of functional haploid spermatids from human germline stem cells by three-dimensional-induced system. Cell Death Differ. 2018;25(4):749–66.
pubmed: 29305586
Cremades N, Bernabeu R, Barros A, Sousa M. In-vitro maturation of round spermatids using co-culture on Vero cells. Hum Reprod. 1999;14(5):1287–93.
pubmed: 10325279
Tanaka A, Nagayoshi M, Awata S, Tanaka I, Kusunoki H. Differentiation of human round spermatids into motile spermatozoa through in vitro coculture with Vero cells. Reprod Med Biol. 2009;8(4):169–75.
pubmed: 29699323
pmcid: 5904850
Kadam P, Ntemou E, Onofre J, Van Saen D, Goossens E. Does co-transplantation of mesenchymal and spermatogonial stem cells improve reproductive efficiency and safety in mice? Stem Cell Res Ther. 2019;10(1):310.
pubmed: 31640769
pmcid: 6805426
Karimaghai N, Tamadon A, Rahmanifar F, Mehrabani D, Raayat Jahromi A, 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(7):660–7.
pubmed: 30140403
pmcid: 6098960
Li X, Xu A, Li K, Zhang J, Li Q, Zhao G, et al. CXCR4-SF1 bifunctional adipose-derived stem cells benefit for the treatment of Leydig cell dysfunction-related diseases. J Cell Mol Med. 2020;24(8):4633–45.
pubmed: 32181567
pmcid: 7176872
Curley M, Gonzalez ZN, Milne L, Hadoke P, Handel I, Péault B, et al. Human adipose-derived pericytes display steroidogenic lineage potential in vitro and influence Leydig cell regeneration in vivo in rats. Sci Rep. 2019;9(1):15037.
pubmed: 31636275
pmcid: 6803635
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;737:14448.
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(13):906–19.
pubmed: 31210400
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. Ultrastruct Pathol. 2019;43(1):28–55.
pubmed: 30741078
Cakici C, Buyrukcu B, Duruksu G, Haliloglu AH, Aksoy A, Isık 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;2013:529589.
pubmed: 23509736
pmcid: 3590610