Clinical and Experimental Reproductive Medicine

The Korean Society for Reproductive Medicine (대한생식의학회)
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Bone marrow-derived stem cells contribute to regeneration of the endometrium

  • Lee, Youn Jeong (Department of Obstetrics and Gynecology, Korea University College of Medicine) ;
  • Yi, Kyong Wook (Department of Obstetrics and Gynecology, Korea University College of Medicine)
  • Received : 2018.10.15
  • Accepted : 2018.11.07
  • Published : 2018.12.31
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Abstract

Stem cells are undifferentiated cells capable of self-renewal and differentiation into various cell lineages. Stem cells are responsible for the development of organs and regeneration of damaged tissues. The highly regenerative nature of the human endometrium during reproductive age suggests that stem cells play a critical role in endometrial physiology. Bone marrow-derived cells migrate to the uterus and participate in the healing and restoration of functionally or structurally damaged endometrium. This review summarizes recent research into the potential therapeutic effects of bone marrow-derived stem cells in conditions involving endometrial impairment.

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References

  1. 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;22:67-76. https://doi.org/10.1111/jcmm.13294
  2. Jabbour HN, Kelly RW, Fraser HM, Critchley HO. Endocrine regulation of menstruation. Endocr Rev 2006;27:17-46. https://doi.org/10.1210/er.2004-0021
  3. Gargett CE, Schwab KE, Brosens JJ, Puttemans P, Benagiano G, Brosens I. Potential role of endometrial stem/progenitor cells in the pathogenesis of early-onset endometriosis. Mol Hum Reprod 2014;20:591-8. https://doi.org/10.1093/molehr/gau025
  4. Kato K, Yoshimoto M, Kato K, Adachi S, Yamayoshi A, Arima T, et al. Characterization of side-population cells in human normal endometrium. Hum Reprod 2007;22:1214-23. https://doi.org/10.1093/humrep/del514
  5. Masuda H, Matsuzaki Y, Hiratsu E, Ono M, Nagashima T, Kajitani T, et al. Stem cell-like properties of the endometrial side population: implication in endometrial regeneration. PLoS One 2010;5:e10387. https://doi.org/10.1371/journal.pone.0010387
  6. Du H, Naqvi H, Taylor HS. Ischemia/reperfusion injury promotes and granulocyte-colony stimulating factor inhibits migration of bone marrow-derived stem cells to endometrium. Stem Cells Dev 2012;21:3324-31. https://doi.org/10.1089/scd.2011.0193
  7. Togel F, Westenfelder C. Adult bone marrow-derived stem cells for organ regeneration and repair. Dev Dyn 2007;236:3321-31. https://doi.org/10.1002/dvdy.21258
  8. Lin CS, Ning H, Lin G, Lue TF. Is CD34 truly a negative marker for mesenchymal stromal cells? Cytotherapy 2012;14:1159-63. https://doi.org/10.3109/14653249.2012.729817
  9. Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, et al. Minimal criteria for defining multipotent mesenchymal stromal cells: the International Society for Cellular Therapy position statement. Cytotherapy 2006;8:315-7. https://doi.org/10.1080/14653240600855905
  10. Taylor HS. Endometrial cells derived from donor stem cells in bone marrow transplant recipients. JAMA 2004;292:81-5. https://doi.org/10.1001/jama.292.1.81
  11. Chan RW, Schwab KE, Gargett CE. Clonogenicity of human endometrial epithelial and stromal cells. Biol Reprod 2004;70:1738-50. https://doi.org/10.1095/biolreprod.103.024109
  12. Du H, Taylor HS. Contribution of bone marrow-derived stem cells to endometrium and endometriosis. Stem Cells 2007;25:2082-6. https://doi.org/10.1634/stemcells.2006-0828
  13. Orlic D, Kajstura J, Chimenti S, Jakoniuk I, Anderson SM, Li B, et al. Bone marrow cells regenerate infarcted myocardium. Nature 2001;410:701-5. https://doi.org/10.1038/35070587
  14. Poulsom R, Forbes SJ, Hodivala-Dilke K, Ryan E, Wyles S, Navaratnarasah S, et al. Bone marrow contributes to renal parenchymal turnover and regeneration. J Pathol 2001;195:229-35. https://doi.org/10.1002/path.976
  15. Alison MR, Poulsom R, Jeffery R, Dhillon AP, Quaglia A, Jacob J, et al. Hepatocytes from non-hepatic adult stem cells. Nature 2000;406:257. https://doi.org/10.1038/35018642
  16. Alawadhi F, Du H, Cakmak H, Taylor HS. Bone marrow-derived stem cell (BMDSC) transplantation improves fertility in a murine model of Asherman's syndrome. PLoS One 2014;9:e96662. https://doi.org/10.1371/journal.pone.0096662
  17. Sahin Ersoy G, Zolbin MM, Cosar E, Moridi I, Mamillapalli R, Taylor HS. CXCL12 promotes stem cell recruitment and uterine repair after injury in Asherman's syndrome. Mol Ther Methods Clin Dev 2017;4:169-77. https://doi.org/10.1016/j.omtm.2017.01.001
  18. Cervello I, Gil-Sanchis C, Santamaria X, Cabanillas S, Diaz A, Faus A, et al. Human CD133(+) bone marrow-derived stem cells promote endometrial proliferation in a murine model of Asherman syndrome. Fertil Steril 2015;104:1552-60.e1-3. https://doi.org/10.1016/j.fertnstert.2015.08.032
  19. Urman B, Mercan R, Alatas C, Balaban B, Isiklar A, Nuhoglu A. Low-dose aspirin does not increase implantation rates in patients undergoing intracytoplasmic sperm injection: a prospective randomized study. J Assist Reprod Genet 2000;17:586-90. https://doi.org/10.1023/A:1026491426423
  20. Frattarelli JL, Miller BT, Scott RT Jr. Adjuvant therapy enhances endometrial receptivity in patients undergoing assisted reproduction. Reprod Biomed Online 2006;12:722-9. https://doi.org/10.1016/S1472-6483(10)61084-X
  21. Glujovsky D, Pesce R, Fiszbajn G, Sueldo C, Hart RJ, Ciapponi A. Endometrial preparation for women undergoing embryo transfer with frozen embryos or embryos derived from donor oocytes. Cochrane Database Syst Rev 2010;(1):CD006359.
  22. Gleicher N, Kim A, Michaeli T, Lee HJ, Shohat-Tal A, Lazzaroni E, et al. A pilot cohort study of granulocyte colony-stimulating factor in the treatment of unresponsive thin endometrium resistant to standard therapies. Hum Reprod 2013;28:172-7. https://doi.org/10.1093/humrep/des370
  23. Jing Z, Qiong Z, Yonggang W, Yanping L. Rat bone marrow mesenchymal stem cells improve regeneration of thin endometrium in rat. Fertil Steril 2014;101:587-94. https://doi.org/10.1016/j.fertnstert.2013.10.053
  24. Yi KW, Mamillapalli R, Sahin C, Song J, Tal R, Taylor HS. Bone marrow-derived cells or C-X-C motif chemokine 12 (CXCL12) treatment improve thin endometrium in a mouse model. Biol Reprod 2018 Aug 1 [Epub]. https://doi.org/10.1093/biolre/ioy175.
  25. Santamaria X, Cabanillas S, Cervello 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;31:1087-96. https://doi.org/10.1093/humrep/dew042
  26. Rafii S, Lyden D. Therapeutic stem and progenitor cell transplantation for organ vascularization and regeneration. Nat Med 2003;9:702-12. https://doi.org/10.1038/nm0603-702
  27. 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;7:93-8. https://doi.org/10.4103/0974-1208.138864
  28. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, et al. Multilineage potential of adult human mesenchymal stem cells. Science 1999;284:143-7. https://doi.org/10.1126/science.284.5411.143
  29. Ong YR, Cousins FL, Yang X, Mushafi AA, Breault DT, Gargett CE, et al. Bone marrow stem cells do not contribute to endometrial cell lineages in chimeric mouse models. Stem Cells 2018;36:91-102. https://doi.org/10.1002/stem.2706
  30. Chen L, Tredget EE, Wu PY, Wu Y. Paracrine factors of mesenchymal stem cells recruit macrophages and endothelial lineage cells and enhance wound healing. PLoS One 2008;3:e1886. https://doi.org/10.1371/journal.pone.0001886
  31. Curley GF, Hayes M, Ansari B, Shaw G, Ryan A, Barry F, et al. Mesenchymal stem cells enhance recovery and repair following ventilator-induced lung injury in the rat. Thorax 2012;67:496-501. https://doi.org/10.1136/thoraxjnl-2011-201059
  32. Wang N, Li Q, Zhang L, Lin H, Hu J, Li D, et al. Mesenchymal stem cells attenuate peritoneal injury through secretion of TSG-6. PLoS One 2012;7:e43768. https://doi.org/10.1371/journal.pone.0043768
  33. Caplan AI, Dennis JE. Mesenchymal stem cells as trophic mediators. J Cell Biochem 2006;98:1076-84. https://doi.org/10.1002/jcb.20886
  34. Fu Y, Karbaat L, Wu L, Leijten J, Both SK, Karperien M. Trophic effects of mesenchymal stem cells in tissue regeneration. Tissue Eng Part B Rev 2017;23:515-28.
  35. Rabb H. Paracrine and differentiation mechanisms underlying stem cell therapy for the damaged kidney. Am J Physiol Renal Physiol 2005;289:F29-30. https://doi.org/10.1152/ajprenal.00102.2005
  36. Chien KR. Lost and found: cardiac stem cell therapy revisited. J Clin Invest 2006;116:1838-40. https://doi.org/10.1172/JCI29050
  37. Simoni M, Taylor HS. Therapeutic strategies involving uterine stem cells in reproductive medicine. Curr Opin Obstet Gynecol 2018;30:209-16.
  38. Hopman RK, DiPersio JF. Advances in stem cell mobilization. Blood Rev 2014;28:31-40. https://doi.org/10.1016/j.blre.2014.01.001
  39. Lai CY, Yamazaki S, Okabe M, Suzuki S, Maeyama Y, Iimura Y, et al. Stage-specific roles for CXCR4 signaling in murine hematopoietic stem/progenitor cells in the process of bone marrow repopulation. Stem Cells 2014;32:1929-42. https://doi.org/10.1002/stem.1670
  40. Kim CH, Broxmeyer HE. In vitro behavior of hematopoietic progenitor cells under the influence of chemoattractants: stromal cell-derived factor-1, steel factor, and the bone marrow environment. Blood 1998;91:100-10.
  41. Cheng JW, Sadeghi Z, Levine AD, Penn MS, von Recum HA, Caplan AI, et al. The role of CXCL12 and CCL7 chemokines in immune regulation, embryonic development, and tissue regeneration. Cytokine 2014;69:277-83. https://doi.org/10.1016/j.cyto.2014.06.007
  42. Askari AT, Unzek S, Popovic ZB, Goldman CK, Forudi F, Kiedrowski M, et al. Effect of stromal-cell-derived factor 1 on stem-cell homing and tissue regeneration in ischaemic cardiomyopathy. Lancet 2003;362:697-703. https://doi.org/10.1016/S0140-6736(03)14232-8
  43. Abbott JD, Huang Y, Liu D, Hickey R, Krause DS, Giordano FJ. Stromal cell-derived factor-1alpha plays a critical role in stem cell recruitment to the heart after myocardial infarction but is not sufficient to induce homing in the absence of injury. Circulation 2004;110:3300-5. https://doi.org/10.1161/01.CIR.0000147780.30124.CF
  44. Hill WD, Hess DC, Martin-Studdard A, Carothers JJ, Zheng J, Hale D, et al. SDF-1 (CXCL12) is upregulated in the ischemic penumbra following stroke: association with bone marrow cell homing to injury. J Neuropathol Exp Neurol 2004;63:84-96. https://doi.org/10.1093/jnen/63.1.84

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