Therapeutic Potential of Mesenchymal Stem Cells in PCOS


Дәйексөз келтіру

Толық мәтін

Аннотация

Polycystic ovary syndrome (PCOS) is a major reproductive endocrine disorder affecting different facets of a woman’s life, comprising reproduction, metabolism, and mental health. Recently, several research groups have brought attention to the therapeutic capacity of mesenchymal stem cells (MSCs) for the treatment of female reproductive disorders. It is highlighted that the treatment with bone marrow mesenchymal stem cells (BMMSCs) considerably diminishes the levels of some inflammatory markers as well as essential genes for ovarian production of androgens, which are considerably higher in theca cells of PCOS women than in those of healthy cases. In addition, studies show that BMMSCs improve in vitro maturation (IVM) of germinal vesicles (GVs) and the number of antral follicles while lessening the number of primary and preantral follicles in mice with PCOS compared to healthy controls. Regarding adipose- derived mesenchymal stem cells (AdMSCs), these cells restore the ovarian structure, enhance the number of oocytes and corpora luteum, and diminish the number of aberrant cystic follicles in PCOS rats. Some research also indicates that umbilical cord mesenchymal stem cells (UC-MSCs) alleviate the inflammation of granulosa cells in women with PCOS. Therefore, due to the limited research on MSC therapy in PCOS, in this review, we summarize the current knowledge on the therapeutic potential of three types of MSCs: BMMSCs, AdMSCs, UC-MSCs and their secretome in the treatment of PCOS.

Авторлар туралы

Hamid Nejabati

Stem Cell Research Center, Tabriz University of Medical Sciences

Хат алмасуға жауапты Автор.
Email: info@benthamscience.net

Sadeneh Nikzad

Department of Biology, Concordia University

Email: info@benthamscience.net

Leila Roshangar

Stem Cell Research Center, Tabriz University of Medical Sciences

Хат алмасуға жауапты Автор.
Email: info@benthamscience.net

Әдебиет тізімі

  1. Sirmans S, Pate K. Epidemiology, diagnosis, and management of polycystic ovary syndrome. Clin Epidemiol 2013; 6: 1-13. doi: 10.2147/CLEP.S37559 PMID: 24379699
  2. Stein IF, Leventhal ML. Amenorrhea associated with bilateral polycystic ovaries. Am J Obstet Gynecol 1935; 29(2): 181-91. doi: 10.1016/S0002-9378(15)30642-6
  3. Aversa A, La Vignera S, Rago R, et al. Fundamental concepts and novel aspects of polycystic ovarian syndrome: Expert consensus resolutions. Front Endocrinol 2020; 11: 516. doi: 10.3389/fendo.2020.00516 PMID: 32849300
  4. Escobar-Morreale HF. Polycystic ovary syndrome: Definition, aetiology, diagnosis and treatment. Nat Rev Endocrinol 2018; 14(5): 270-84. doi: 10.1038/nrendo.2018.24 PMID: 29569621
  5. Carvalho LML, dos Reis FM, Candido AL, Nunes FFC, Ferreira CN, Gomes KB. Polycystic ovary syndrome as a systemic disease with multiple molecular pathways: A narrative review. Endocr Regul 2018; 52(4): 208-21. doi: 10.2478/enr-2018-0026 PMID: 31517612
  6. Iervolino M, Lepore E, Forte G, Laganà AS. Natural molecules in the management of polycystic ovary syndrome (PCOS): An analytical review. Nutrients 2021; 13(5): 1677.
  7. McLuskie I, Newth A. New diagnosis of polycystic ovary syndrome. BMJ 2017; 356: i6456. doi: 10.1136/bmj.i6456 PMID: 28082338
  8. Palomba S, Santagni S, Falbo A, La Sala GB. Complications and challenges associated with polycystic ovary syndrome: current perspectives. Int J Womens Health 2015; 7: 745-63. doi: 10.2147/IJWH.S70314 PMID: 26261426
  9. Galipeau J, Sensébé L. Mesenchymal stromal cells: Clinical challenges and therapeutic opportunities. Cell Stem Cell 2018; 22(6): 824-33. doi: 10.1016/j.stem.2018.05.004 PMID: 29859173
  10. Naji A, Rouas-Freiss N, Durrbach A, Carosella ED, Sensébé L, Deschaseaux F. Concise review: Combining human leukocyte antigen G and mesenchymal stem cells for immunosuppressant biotherapy. Stem Cells 2013; 31(11): 2296-303. doi: 10.1002/stem.1494 PMID: 23922260
  11. Squillaro T, Peluso G, Galderisi U. Clinical trials with mesenchymal stem cells: An update. Cell Transplant 2016; 25(5): 829-48. doi: 10.3727/096368915X689622 PMID: 26423725
  12. Trounson A, McDonald C. Stem cell therapies in clinical trials: Progress and challenges. Cell Stem Cell 2015; 17(1): 11-22. doi: 10.1016/j.stem.2015.06.007 PMID: 26140604
  13. Fan XL, Zhang Y, Li X, Fu QL. Mechanisms underlying the protective effects of mesenchymal stem cell-based therapy. Cell Mol Life Sci 2020; 77(14): 2771-94. doi: 10.1007/s00018-020-03454-6
  14. Rungsiwiwut R, Virutamasen P, Pruksananonda K. Mesenchymal stem cells for restoring endometrial function: An infertility perspective. Reprod Med Biol 2021; 20(1): 13-9.
  15. Spitzhorn LS, Megges M, Wruck W, et al. Human iPSC-derived MSCs (iMSCs) from aged individuals acquire a rejuvenation signature. Stem Cell Res Ther 2019; 10(1): 100. doi: 10.1186/s13287-019-1209-x PMID: 30885246
  16. Ullah I, Subbarao RB, Rho GJ. Human mesenchymal stem cells - current trends and future prospective. Biosci Rep 2015; 35(2): e00191. doi: 10.1042/BSR20150025 PMID: 25797907
  17. Yoon SY. Mesenchymal stem cells for restoration of ovarian function. Clin Exp Reprod Med 2019; 46(1): 1-7. doi: 10.5653/cerm.2019.46.1.1 PMID: 30827071
  18. Liu F, Hu S, Yang H, Li Z, Huang K, Su T. Hyaluronic acid hydrogel integrated with mesenchymal stem cell-secretome to treat endometrial injury in a rat model of asherman’s syndrome. Adv Healthc Mater 2019; 8(14): e1900411.
  19. Mendt M, Rezvani K, Shpall E. Mesenchymal stem cell-derived exosomes for clinical use. Bone Marrow Transplant 2019; 54(S2): 789-92. doi: 10.1038/s41409-019-0616-z PMID: 31431712
  20. Patel DB, Gray KM, Santharam Y, Lamichhane TN, Stroka KM, Jay SM. Impact of cell culture parameters on production and vascularization bioactivity of mesenchymal stem cell-derived extracellular vesicles. Bioeng Transl Med 2017; 2(2): 170-9. doi: 10.1002/btm2.10065
  21. Zhao AG, Shah K. Mesenchymal stem cell-derived extracellular vesicles and their therapeutic potential. Stem Cells Int 2020; 2020: 8825771.
  22. Dominici M, Le Blanc K, Mueller I, et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006; 8(4): 315-7. doi: 10.1080/14653240600855905 PMID: 16923606
  23. Galipeau J, Krampera M, Barrett J, et al. International society for cellular therapy perspective on immune functional assays for mesenchymal stromal cells as potency release criterion for advanced phase clinical trials. Cytotherapy 2016; 18(2): 151-9. doi: 10.1016/j.jcyt.2015.11.008 PMID: 26724220
  24. Krampera M, Galipeau J, Shi Y, Tarte K, Sensebe L. Immunological characterization of multipotent mesenchymal stromal cells—The International Society for Cellular Therapy (ISCT) working proposal. Cytotherapy 2013; 15(9): 1054-61. doi: 10.1016/j.jcyt.2013.02.010 PMID: 23602578
  25. Zhao Y, Chen S, Su P, et al. Using mesenchymal stem cells to treat female infertility: An update on female reproductive diseases. Stem Cells Int 2019; 2019: 1-10. doi: 10.1155/2019/9071720 PMID: 31885630
  26. Altaner C, Altanerova V, Cihova M, et al. Characterization of mesenchymal stem cells of "no-options" patients with critical limb ischemia treated by autologous bone marrow mononuclear cells. PLoS One 2013; 8(9): e73722. doi: 10.1371/journal.pone.0073722 PMID: 24069226
  27. Owen M, Friedenstein AJ. Stromal stem cells: Marrow-derived osteogenic precursors. Ciba Found Symp 1988; 136: 42-60. PMID: 3068016
  28. Gao L, Huang Z, Lin H, Tian Y, Li P, Lin S. Bone marrow mesenchymal stem cells (BMSCs) restore functional endometrium in the rat model for severe asherman syndrome. Reprod Sci 2019; 26(3): 436-44. doi: 10.1177/1933719118799201 PMID: 30458678
  29. Liu Y, Tal R, Pluchino N, Mamillapalli R, Taylor HS. Systemic administration of bone marrow-derived cells leads to better uterine engraftment than use of uterine-derived cells or local injection. J Cell Mol Med 2018; 22(1): 67-76. doi: 10.1111/jcmm.13294 PMID: 28782281
  30. Tepper OM, Sealove BA, Murayama T, Asahara T. Newly emerging concepts in blood vessel growth: Recent discovery of endothelial progenitor cells and their function in tissue regeneration. J Investig Med 2003; 51(6): 353-9.
  31. Besikcioglu HE, Sarıbas GS, Ozogul C, et al. Determination of the effects of bone marrow derived mesenchymal stem cells and ovarian stromal stem cells on follicular maturation in cyclophosphamide induced ovarian failure in rats. Taiwan J Obstet Gynecol 2019; 58(1): 53-9. doi: 10.1016/j.tjog.2018.11.010 PMID: 30638481
  32. Badawy A, Sobh M, Ahdy M, Abdelhafez M. Bone marrow mesenchymal stem cell repair of cyclophosphamide-induced ovarian insufficiency in a mouse model. Int J Womens Health 2017; 9: 441-7. doi: 10.2147/IJWH.S134074 PMID: 28670143
  33. Fu X, He Y, Wang X, et al. Overexpression of miR-21 in stem cells improves ovarian structure and function in rats with chemotherapy-induced ovarian damage by targeting PDCD4 and PTEN to inhibit granulosa cell apoptosis. Stem Cell Res Ther 2017; 8(1): 187. doi: 10.1186/s13287-017-0641-z PMID: 28807003
  34. Zhang C. The roles of different stem cells in premature ovarian failure. Curr Stem Cell Res Ther 2020; 15(6): 473-81. doi: 10.2174/1574888X14666190314123006 PMID: 30868961
  35. Panchal SY, Patel H, Nagori CB. 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. doi: 10.4103/0974-1208.82360 PMID: 21772740
  36. Taylor HS. Endometrial cells derived from donor stem cells in bone marrow transplant recipients. JAMA 2004; 292(1): 81-5. doi: 10.1001/jama.292.1.81 PMID: 15238594
  37. Wang J, Ju B, Pan C, Gu Y, Zhang Y, Sun L. Application of bone marrow-derived mesenchymal stem cells in the treatment of intrauterine adhesions in rats. Cell Physiol Biochem 2016; 39(4): 1553-60. doi: 10.1159/000447857
  38. Lendeckel S, Jödicke A, Christophis P, Heidinger K, Wolff J, Fraser JK. Autologous stem cells (adipose) and fibrin glue used to treat widespread traumatic calvarial defects: Case report. J Craniomaxillofac Surg 2004; 32(6): 370-3.
  39. Ra JC, Jeong EC, Kang SK, Lee SJ, Choi KH. A prospective, nonrandomized, no placebo-controlled, phase i/ii clinical trial assessing the safety and efficacy of intramuscular injection of autologous adipose tissue-derived mesenchymal stem cells in patients with severe buerger’s disease. Cell Med 2017; 9(3): 87-102. doi: 10.3727/215517916X693069 PMID: 28713639
  40. Yang JA, Chung HM, Won CH, Sung JH. Potential application of adipose-derived stem cells and their secretory factors to skin: discussion from both clinical and industrial viewpoints. Expert Opin Biol Ther 2010; 10(4): 495-503. doi: 10.1517/14712591003610598 PMID: 20218919
  41. Choudhery MS, Badowski M, Muise A, Pierce J, Harris DT. Donor age negatively impacts adipose tissue-derived mesenchymal stem cell expansion and differentiation. J Transl Med 2014; 12(1): 8. doi: 10.1186/1479-5876-12-8 PMID: 24397850
  42. Damous LL, Nakamuta JS, Saturi de Carvalho AET, et al. Does adipose tissue-derived stem cell therapy improve graft quality in freshly grafted ovaries? Reprod Biol Endocrinol 2015; 13(1): 108. doi: 10.1186/s12958-015-0104-2 PMID: 26394676
  43. Sun M, Wang S, Li Y, et al. Adipose-derived stem cells improved mouse ovary function after chemotherapy-induced ovary failure. Stem Cell Res Ther 2013; 4(4): 80. doi: 10.1186/scrt231 PMID: 23838374
  44. Terraciano P, Garcez T. Cell therapy for chemically induced ovarian failure in mice. Stem Cells Int 2014; 2014: 720753. doi: 10.1155/2014/720753
  45. Nagamura-Inoue T, He H. Umbilical cord-derived mesenchymal stem cells: Their advantages and potential clinical utility. World J Stem Cells 2014; 6(2): 195-202. doi: 10.4252/wjsc.v6.i2.195 PMID: 24772246
  46. Mohamed SA, Shalaby S, Brakta S, Elam L. Umbilical cord blood mesenchymal stem cells as an infertility treatment for chemotherapy induced premature ovarian insufficiency. Biomedicines 2019; 7(1): 7. doi: 10.3390/biomedicines7010007
  47. Song D, Zhong Y, Qian C, Zou Q, Ou J, Shi Y. Human umbilical cord mesenchymal stem cells therapy in cyclophosphamide-induced premature ovarian failure rat model. BioMed Res Int 2016; 2016: 2517514.
  48. Zhu SF, Hu HB, Xu HY, et al. Human umbilical cord mesenchymal stem cell transplantation restores damaged ovaries. J Cell Mol Med 2015; 19(9): 2108-17. doi: 10.1111/jcmm.12571 PMID: 25922900
  49. Jalalie L, Rezaie MJ, Jalili A, et al. Distribution of the cm-dil-labeled human umbilical cord vein mesenchymal stem cells migrated to the cyclophosphamide-injured ovaries in C57BL/6 Mice. Iran Biomed J 2019; 23(3): 200-8. doi: 10.29252/ibj.23.3.200 PMID: 30797224
  50. Conway G, Dewailly D, Diamanti-Kandarakis E, et al. The polycystic ovary syndrome: A position statement from the European Society of Endocrinology. Eur J Endocrinol 2014; 171(4): 1-P29. doi: 10.1530/EJE-14-0253 PMID: 24849517
  51. Nejabati HR, Samadi N, Shahnazi V, et al. Nicotinamide and its metabolite N1-Methylnicotinamide alleviate endocrine and metabolic abnormalities in adipose and ovarian tissues in rat model of Polycystic Ovary Syndrome. Chem Biol Interact 2020; 324: 109093. doi: 10.1016/j.cbi.2020.109093 PMID: 32298659
  52. Azziz R, Carmina E, Chen Z, et al. Polycystic ovary syndrome. Nat Rev Dis Primers 2016; 2(1): 16057. doi: 10.1038/nrdp.2016.57 PMID: 27510637
  53. Escobar-Morreale HF. Diagnosis and management of hirsutism. Ann N Y Acad Sci 2010; 1205(1): 166-74. doi: 10.1111/j.1749-6632.2010.05652.x PMID: 20840269
  54. Miller WL, Auchus RJ. The molecular biology, biochemistry, and physiology of human steroidogenesis and its disorders. Endocr Rev 2011; 32(1): 81-151. doi: 10.1210/er.2010-0013 PMID: 21051590
  55. Wickenheisser JK, Nelson-DeGrave VL, McAllister JM. Dysregulation of cytochrome P450 17alpha-hydroxylase messenger ribonucleic acid stability in theca cells isolated from women with polycystic ovary syndrome. J Clin Endocrinol Metab 2005; 90(3): 1720-7. doi: 10.1210/jc.2004-1860 PMID: 15598676
  56. Legro RS, Arslanian SA, Ehrmann DA, et al. Diagnosis and treatment of polycystic ovary syndrome: an Endocrine Society clinical practice guideline. J Clin Endocrinol Metab 2013; 98(12): 4565-92. doi: 10.1210/jc.2013-2350 PMID: 24151290
  57. Mathur R, Levin O, Azziz R. Use of ethinylestradiol/drospirenone combination in patients with the polycystic ovary syndrome. Ther Clin Risk Manag 2008; 4(2): 487-92. doi: 10.2147/TCRM.S6864 PMID: 18728832
  58. Koulouri O, Conway GS. A systematic review of commonly used medical treatments for hirsutism in women. Clin Endocrinol 2008; 68(5): 800-5. doi: 10.1111/j.1365-2265.2007.03105.x PMID: 17980017
  59. Moghetti P, Tosi F, Tosti A, et al. Comparison of spironolactone, flutamide, and finasteride efficacy in the treatment of hirsutism: a randomized, double blind, placebo-controlled trial. J Clin Endocrinol Metab 2000; 85(1): 89-94. doi: 10.1210/jc.85.1.89 PMID: 10634370
  60. Naka KK, Kalantaridou SN, Kravariti M, et al. Effect of the insulin sensitizers metformin and pioglitazone on endothelial function in young women with polycystic ovary syndrome: a prospective randomized study. Fertil Steril 2011; 95(1): 203-9. doi: 10.1016/j.fertnstert.2010.06.058 PMID: 20684955
  61. Farquhar C, Brown J, Marjoribanks J. Laparoscopic drilling by diathermy or laser for ovulation induction in anovulatory polycystic ovary syndrome. Cochrane Libr 2012; (6): CD001122. doi: 10.1002/14651858.CD001122.pub4 PMID: 22696324
  62. Abu Hashim H, Al-Inany H, De Vos M, Tournaye H. Three decades after Gjönnaess’s laparoscopic ovarian drilling for treatment of PCOS; what do we know? An evidence-based approach. Arch Gynecol Obstet 2013; 288(2): 409-22. doi: 10.1007/s00404-013-2808-x PMID: 23543241
  63. Fox CW, Zhang L, Sohni A, et al. Inflammatory stimuli trigger increased androgen production and shifts in gene expression in theca-interstitial cells. Endocrinology 2019; 160(12): 2946-58. doi: 10.1210/en.2019-00588 PMID: 31599939
  64. González F, Sia CL, Bearson DM, Blair HE. Hyperandrogenism induces a proinflammatory TNFα response to glucose ingestion in a receptor-dependent fashion. J Clin Endocrinol Metab 2014; 99(5): E848-54. doi: 10.1210/jc.2013-4109 PMID: 24512496
  65. Lang Q, Yidong X, Xueguang Z, Sixian W, Wenming X, Tao Z. ETA-mediated anti-TNF-α therapy ameliorates the phenotype of PCOS model induced by letrozole. PLoS One 2019; 14(6): e0217495. doi: 10.1371/journal.pone.0217495 PMID: 31170164
  66. Nelson VL, Qin K, Rosenfield RL, et al. The biochemical basis for increased testosterone production in theca cells propagated from patients with polycystic ovary syndrome. J Clin Endocrinol Metab 2001; 86(12): 5925-33. doi: 10.1210/jcem.86.12.8088 PMID: 11739466
  67. Wickenheisser JK, Quinn PG, Nelson VL, Legro RS, Strauss JF III, McAllister JM. Differential activity of the cytochrome P450 17alpha-hydroxylase and steroidogenic acute regulatory protein gene promoters in normal and polycystic ovary syndrome theca cells. J Clin Endocrinol Metab 2000; 85(6): 2304-11. PMID: 10852468
  68. Chugh RM, Park HS, El Andaloussi A, Elsharoud A, Esfandyari S, Ulin M. Mesenchymal stem cell therapy ameliorates metabolic dysfunction and restores fertility in a PCOS mouse model through interleukin-10. Stem Cell Res Ther 2021; 12(1): 388. doi: 10.1186/s13287-021-02472-w
  69. Kyurkchiev D, Bochev I, Ivanova-Todorova E, et al. Secretion of immunoregulatory cytokines by mesenchymal stem cells. World J Stem Cells 2014; 6(5): 552-70. doi: 10.4252/wjsc.v6.i5.552 PMID: 25426252
  70. Qu X, Liu X, Cheng K, Yang R, Zhao RCH. Mesenchymal stem cells inhibit Th17 cell differentiation by IL-10 secretion. Exp Hematol 2012; 40(9): 761-70. doi: 10.1016/j.exphem.2012.05.006 PMID: 22634392
  71. Wang J, Ren H, Yuan X, Ma H, Shi X, Ding Y. Interleukin‐10 secreted by mesenchymal stem cells attenuates acute liver failure through inhibiting pyroptosis. Hepatol Res 2018; 48(3): E194-202. doi: 10.1111/hepr.12969 PMID: 28833919
  72. Iyer SS, Cheng G. Role of interleukin 10 transcriptional regulation in inflammation and autoimmune disease. Crit Rev Immunol 2012; 32(1): 23-63.
  73. Talaat RM, Mohamed YA, Mohamad EH, Elsharkawy M, Guirgis AA. Interleukin 10 (− 1082 G/A) and (− 819 C/T) gene polymorphisms in Egyptian women with polycystic ovary syndrome (PCOS). Meta Gene 2016; 9: 254-8. doi: 10.1016/j.mgene.2016.08.001 PMID: 27617227
  74. Hong EG, Ko HJ, Cho YR, et al. Interleukin-10 prevents diet-induced insulin resistance by attenuating macrophage and cytokine response in skeletal muscle. Diabetes 2009; 58(11): 2525-35. doi: 10.2337/db08-1261 PMID: 19690064
  75. Tarkun İ, Çetinarslan B, Türemen E, Cantürk Z, Biyikli M. Association between circulating tumor necrosis factor-alpha, interleukin-6, and insulin resistance in normal-weight women with polycystic ovary syndrome. Metab Syndr Relat Disord 2006; 4(2): 122-8. doi: 10.1089/met.2006.4.122 PMID: 18370758
  76. Chugh RM, Park H, Esfandyari S, Elsharoud A, Ulin M, Al-Hendy A. Mesenchymal stem cell-conditioned media regulate steroidogenesis and inhibit androgen secretion in a PCOS cell model via BMP-2. Int J Mol Sci 2021; 22(17): 9184. doi: 10.3390/ijms22179184 PMID: 34502090
  77. Legro RS, Brzyski RG, Diamond MP, et al. Letrozole versus clomiphene for infertility in the polycystic ovary syndrome. N Engl J Med 2014; 371(2): 119-29. doi: 10.1056/NEJMoa1313517 PMID: 25006718
  78. Polson DW, Mason HD, Saldahna MBY, Franks S. Ovulation of a single dominant follicle during treatment with low-dose pulsatile follicle stimulating hormone in women with polycystic ovary syndrome. Clin Endocrinol 1987; 26(2): 205-12. doi: 10.1111/j.1365-2265.1987.tb00778.x PMID: 3117445
  79. Sagle MA, Hamilton-Fairley D, Kiddy DS, Franks S. A comparative, randomized study of low-dose human menopausal gonadotropin and follicle-stimulating hormone in women with polycystic ovarian syndrome. Fertil Steril 1991; 55(1): 56-60. doi: 10.1016/S0015-0282(16)54059-X PMID: 1898891
  80. Homburg R, Hendriks ML, König TE, et al. Clomifene citrate or low-dose FSH for the first-line treatment of infertile women with anovulation associated with polycystic ovary syndrome: A prospective randomized multinational study. Hum Reprod 2012; 27(2): 468-73. doi: 10.1093/humrep/der401 PMID: 22128296
  81. Nahuis MJ, Kose N, Bayram N, et al. Long-term outcomes in women with polycystic ovary syndrome initially randomized to receive laparoscopic electrocautery of the ovaries or ovulation induction with gonadotrophins. Hum Reprod 2011; 26(7): 1899-904. doi: 10.1093/humrep/der141 PMID: 21576081
  82. Cha KY, Chung HM, Lee DR, et al. Obstetric outcome of patients with polycystic ovary syndrome treated by in vitro maturation and in vitro fertilization–embryo transfer. Fertil Steril 2005; 83(5): 1461-5. doi: 10.1016/j.fertnstert.2004.11.044 PMID: 15866585
  83. Siristatidis C, Sergentanis TN, Vogiatzi P, et al. In vitro maturation in women with vs. without polycystic ovarian syndrome: A systematic review and meta-analysis. PLoS One 2015; 10(8): e0134696. doi: 10.1371/journal.pone.0134696 PMID: 26241855
  84. Walls ML, Hunter T, Ryan JP, Keelan JA, Nathan E, Hart RJ. In vitro maturation as an alternative to standard in vitro fertilization for patients diagnosed with polycystic ovaries: A comparative analysis of fresh, frozen and cumulative cycle outcomes. Hum Reprod 2015; 30(1): 88-96. doi: 10.1093/humrep/deu248 PMID: 25355587
  85. Shi Y, Wei D, Liang X, et al. Live birth after fresh embryo transfer vs elective embryo cryopreservation/frozen embryo transfer in women with polycystic ovary syndrome undergoing IVF (FreFro-PCOS): study protocol for a multicenter, prospective, randomized controlled clinical trial. Trials 2014; 15(1): 154. doi: 10.1186/1745-6215-15-154 PMID: 24885793
  86. Jafarzadeh H, Nazarian H, Ghaffari Novin M, Shams Mofarahe Z, Eini F, Piryaei A. Improvement of oocyte in vitro maturation from mice with polycystic ovary syndrome by human mesenchymal stromal cell–conditioned media. J Cell Biochem 2018; 119(12): 10365-75. doi: 10.1002/jcb.27380 PMID: 30171726
  87. Kalhori Z, Azadbakht M, Soleimani MM, 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. doi: 10.1016/j.jcyt.2018.09.005 PMID: 30523787
  88. Zomer A, Vendrig T, Hopmans ES, van Eijndhoven M, Middeldorp JM, Pegtel DM. Exosomes. Commun Integr Biol 2010; 3(5): 447-50. doi: 10.4161/cib.3.5.12339 PMID: 21057637
  89. Pegtel DM, Cosmopoulos K, Thorley-Lawson DA, et al. Functional delivery of viral miRNAs via exosomes. Proc Natl Acad Sci 2010; 107(14): 6328-33. doi: 10.1073/pnas.0914843107 PMID: 20304794
  90. Lou G, Song X, Yang F, et al. Exosomes derived from miR-122-modified adipose tissue-derived MSCs increase chemosensitivity of hepatocellular carcinoma. J Hematol Oncol 2015; 8(1): 122. doi: 10.1186/s13045-015-0220-7 PMID: 26514126
  91. Qu Y, Zhang Q, Cai X, Li F, Ma Z, Xu M. Exosomes derived from miR-181-5p-modified adipose-derived mesenchymal stem cells prevent liver fibrosis via autophagy activation. J Cell Mol Med 2017; 2(10): 2491-502. doi: 10.1111/jcmm.13170 PMID: 28382720
  92. Xin H, Li Y, Buller B, et al. Exosome-mediated transfer of miR-133b from multipotent mesenchymal stromal cells to neural cells contributes to neurite outgrowth. Stem Cells 2012; 30(7): 1556-64. doi: 10.1002/stem.1129 PMID: 22605481
  93. Zhao Y, Tao M, Wei M, Du S, Wang H, Wang X. Mesenchymal stem cells derived exosomal miR-323-3p promotes proliferation and inhibits apoptosis of cumulus cells in polycystic ovary syndrome (PCOS). Artif Cells Nanomed Biotechnol 2019; 47(1): 3804-13.
  94. Xu T, Huang C, Chen Z, Li J. MicroRNA-323-3p: A new biomarker and potential therapeutic target for rheumatoid arthritis. Rheumatol Int 2014; 34(5): 721-2. doi: 10.1007/s00296-013-2767-3 PMID: 23615628
  95. Zhao Z, Zhao Q, Warrick J, et al. Circulating microRNA miR-323-3p as a biomarker of ectopic pregnancy. Clin Chem 2012; 58(5): 896-905. doi: 10.1373/clinchem.2011.179283 PMID: 22395025
  96. Cao M, Zhao Y, Chen T, et al. Adipose mesenchymal stem cell–derived exosomal microRNAs ameliorate polycystic ovary syndrome by protecting against metabolic disturbances. Biomaterials 2022; 288: 121739. doi: 10.1016/j.biomaterials.2022.121739 PMID: 35987860
  97. Moran LJ, Misso ML, Wild RA, Norman RJ. Impaired glucose tolerance, type 2 diabetes and metabolic syndrome in polycystic ovary syndrome: A systematic review and meta-analysis. Hum Reprod Update 2010; 16(4): 347-63. doi: 10.1093/humupd/dmq001 PMID: 20159883
  98. Carmina E. PCOS: Metabolic impact and long-term management. Minerva Ginecol 2012; 64(6): 501-5. PMID: 23232534
  99. Tang T, Lord JM, Norman RJ, Yasmin E, Balen AH. Insulin‐sensitising drugs (metformin, rosiglitazone, pioglitazone, D‐chiro‐inositol) for women with polycystic ovary syndrome, oligo amenorrhoea and subfertility. Cochrane Database Syst Rev 2012; 11(11): CD003053.
  100. Naderpoor N, Shorakae S, de Courten B, Misso ML, Moran LJ, Teede HJ. Metformin and lifestyle modification in polycystic ovary syndrome: Systematic review and meta-analysis. Hum Reprod Update 2015; 21(5): 560-74. doi: 10.1093/humupd/dmv025 PMID: 26060208
  101. Qiu J, Maekawa K, Kitamura Y, et al. Stimulation of glucose uptake by theasinensins through the AMP-activated protein kinase pathway in rat skeletal muscle cells. Biochem Pharmacol 2014; 87(2): 344-51. doi: 10.1016/j.bcp.2013.10.029 PMID: 24225153
  102. Abraham SG, Divakar PY, Valsala GA. Association of metabolic and inflammatory markers with polycystic ovarian syndrome (PCOS): An update. Arch Gynecol Obstet 2021; 303(3): 631-43. doi: 10.1007/s00404-020-05951-2 PMID: 33439300
  103. Orisaka M, Tajima K, Tsang BK, Kotsuji F. Oocyte-granulosa-theca cell interactions during preantral follicular development. J Ovarian Res 2009; 2(1): 9. doi: 10.1186/1757-2215-2-9 PMID: 19589134
  104. Xie Q, Xiong X. Mesenchymal stem cells alleviate DHEA-Induced polycystic ovary syndrome (PCOS) by inhibiting inflammation in mice. Stem Cells Int 2019; 2019: 9782373.
  105. Zhao Y, Pan S, Wu X. Human umbilical cord mesenchymal stem cell-derived exosomes inhibit ovarian granulosa cells inflammatory response through inhibition of NF-κB signaling in polycystic ovary syndrome. J Reprod Immunol 2022; 152: 103638. doi: 10.1016/j.jri.2022.103638 PMID: 35588629

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