Skip to main content

Advertisement

SpringerLink
Log in

Therapeutic potential of menstrual blood-derived endometrial stem cells in cardiac diseases

  • Review
  • Published:
Cellular and Molecular Life Sciences Aims and scope Submit manuscript

Abstract

Despite significant developments in medical and surgical strategies, cardiac diseases remain the leading causes of morbidity and mortality worldwide. Numerous studies involving preclinical and clinical trials have confirmed that stem cell transplantation can help improve cardiac function and regenerate damaged cardiac tissue, and stem cells isolated from bone marrow, heart tissue, adipose tissue and umbilical cord are the primary candidates for transplantation. During the past decade, menstrual blood-derived endometrial stem cells (MenSCs) have gradually become a promising alternative for stem cell-based therapy due to their comprehensive advantages, which include their ability to be periodically and non-invasively collected, their abundant source material, their ability to be regularly donated, their superior proliferative capacity and their ability to be used for autologous transplantation. MenSCs have shown positive therapeutic potential for the treatment of various diseases. Therefore, aside from a brief introduction of the biological characteristics of MenSCs, this review focuses on the progress being made in evaluating the functional improvement of damaged cardiac tissue after MenSC transplantation through preclinical and clinical studies. Based on published reports, we conclude that the paracrine effect, transdifferentiation and immunomodulation by MenSC promote both regeneration of damaged myocardium and improvement of cardiac function.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Young PP, Schäfer R (2015) Cell-based therapies for cardiac disease: a cellular therapist’s perspective. Transfusion 55(2):441–451

    Article  PubMed  Google Scholar 

  2. Lloyd-Jones D, Adams R, Carnethon M et al (2009) Heart disease and stroke statistics-2009 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation 119(3):480–486

    Article  PubMed  Google Scholar 

  3. Laflamme MA, Murry CE (2011) Heart regeneration. Nature 473(7347):326

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Miranović V (2016) The incidence of congenital heart defects in the world regarding the severity of the defect. Vojnosanit Pregl 73(2):159–164

    Article  PubMed  Google Scholar 

  5. Breckwoldt K, Weinberger F, Eschenhagen T (2016) Heart regeneration. BBA-Mol. Cell Res 1863(7):1749–1759

    CAS  Google Scholar 

  6. Bergmann O, Zdunek S, Felker A et al (2015) Dynamics of cell generation and turnover in the human heart. Cell 161(7):1566–1575

    Article  CAS  PubMed  Google Scholar 

  7. Tongers J, Losordo DW, Landmesser U (2011) Stem and progenitor cell-based therapy in ischaemic heart disease: promise, uncertainties, and challenges. Eur Heart J 32(10):1197–1206

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Dixit P, Katare R (2015) Challenges in identifying the best source of stem cells for cardiac regeneration therapy. Stem Cell Res Ther 6(1):26

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Bolli R, Ghafghazi S (2017) Stem cells: cell therapy for cardiac repair: what is needed to move forward? Nat Rev Cardiol 14(5):257

    Article  PubMed  Google Scholar 

  10. Meng X, Ichim TE, Zhong J et al (2007) Endometrial regenerative cells: a novel stem cell population. J Transl Med 5(1):57

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Xu Y, Zhu H, Zhao D et al (2015) Endometrial stem cells: clinical application and pathological roles. Int J Clin Exp Med 8(12):22039

    CAS  PubMed  PubMed Central  Google Scholar 

  12. Gargett CE, Schwab KE, Deane JA (2015) Endometrial stem/progenitor cells: the first 10 years. Hum Reprod Update 22(2):137–163

    PubMed  PubMed Central  Google Scholar 

  13. Simoni M, Taylor HS (2018) Therapeutic strategies involving uterine stem cells in reproductive medicine. Curr Opin Obstet Gyn 30(3):209–216

    Google Scholar 

  14. Lemcke H, Voronina N, Steinhoff G et al (2018) Recent progress in stem cell modification for cardiac regeneration. Stem Cells Int. https://doi.org/10.1155/2018/1909346

    Article  PubMed  PubMed Central  Google Scholar 

  15. Minguell JJ, Erices A (2006) Mesenchymal stem cells and the treatment of cardiac disease. Expl Biol Med 231(1):39–49

    Article  CAS  Google Scholar 

  16. Iglesias-García O, Pelacho B, Prósper F (2013) Induced pluripotent stem cells as a new strategy for cardiac regeneration and disease modeling. J Mol Cell Cardiol 62:43–50

    Article  CAS  PubMed  Google Scholar 

  17. Rikhtegar R, Pezeshkian M, Dolati S et al (2019) Stem cells as therapy for heart disease: iPSCs, ESCs, CSCs, and skeletal myoblasts. Biomed Pharmacother 109:304–313

    Article  CAS  PubMed  Google Scholar 

  18. Berardi GRM, Rebelatto CK, Tavares HF et al (2011) Transplantation of SNAP-treated adipose tissue-derived stem cells improves cardiac function and induces neovascularization after myocardium infarct in rats. Exp Mol Pathol 90(2):149–156

    Article  CAS  PubMed  Google Scholar 

  19. Ou L, Li W, Liu Y et al (2010) Animal models of cardiac disease and stem cell therapy. Open Cardiovasc Med J 4:231–239

    Article  PubMed  PubMed Central  Google Scholar 

  20. Li W, Ma N, Ong LL et al (2007) Bcl-2 engineered MSCs inhibited apoptosis and improved heart function. Stem Cells 25:2118–2127

    Article  CAS  PubMed  Google Scholar 

  21. Menasché P, Vanneaux V, Hagège A et al (2015) Human embryonic stem cell-derived cardiac progenitors for severe heart failure treatment: first clinical case report. Eur Heart J 36:2011–2017

    Article  PubMed  Google Scholar 

  22. Menasché P, Vanneaux V, Hagège A et al (2018) Transplantation of human embryonic stem cell-derived cardiovascular progenitors for severe ischemic left ventricular dysfunction. J Am Coll Cardiol 71:429–438

    Article  PubMed  Google Scholar 

  23. Narita T, Suzuki K (2015) Bone marrow-derived mesenchymal stem cells for the treatment of heart failure. Heart Fail Rev 20(1):53–68

    Article  CAS  PubMed  Google Scholar 

  24. Wollert KC, Meyer GP, Lotz J et al (2004) Intracoronary autologous bone-marrow cell transfer after myocardial infarction: the BOOST randomised controlled clinical trial. Lancet 364(9429):141–148

    Article  PubMed  Google Scholar 

  25. Broughton KM, Sussman MA (2018) Enhancement strategies for cardiac regenerative cell therapy: focus on adult stem cells. Circ Res 123(2):177–187

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Nascimento DS, MosqueiraD Sousa LM et al (2014) Human umbilical cord tissue-derived mesenchymal stromal cells attenuate remodeling after myocardial infarction by proangiogenic, antiapoptotic, and endogenous cell-activation mechanisms. Stem Cell Res Ther 5(1):5

    Article  CAS  PubMed Central  Google Scholar 

  27. Banerjee MN, Bolli R, Hare JM (2018) Clinical studies of cell therapy in cardiovascular medicine: recent developments and future directions. Circ Res 123(2):266–287

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Gaebel R, Furlani D, Sorg H et al (2011) Cell origin of human mesenchymal stem cells determines a different healing performance in cardiac regeneration. PLoS One 6:e15652

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Ma N, Ladilov Y, Moebius JM et al (2006) Intramyocardial delivery of human CD133 + cells in a SCID mouse cryoinjury model: bone marrow vs. cord blood-derived cells. Cardiovasc Res 71:158–169

    Article  CAS  PubMed  Google Scholar 

  30. Nakamura Y, Suzuki S, Shimizu T et al (2015) High mobility group box 1 promotes angiogenesis from bone marrow-derived endothelial progenitor cells after myocardial infarction. J Atheroscler Thromb 22(6):570–581

    Article  CAS  PubMed  Google Scholar 

  31. Bianco P, Riminucci M, Gronthos S et al (2001) Bone marrow stromal stem cells: nature, biology, and potential applications. Stem Cells 19(3):180–192

    Article  CAS  PubMed  Google Scholar 

  32. Yu VWC, Scadden DT (2016) Heterogeneity of the bone marrow niche. Curr Opin Hematol 23(4):331–338

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Asahara T, Murohara T, Sullivan A et al (1997) Isolation of putative progenitor endothelial cells for angiogenesis. Science 275(5302):964–966

    Article  CAS  PubMed  Google Scholar 

  34. Nesselmann C, Li W, Ma N et al (2010) Stem cell-mediated neovascularization in heart repair. Ther Adv Cardiovasc Dis 4(1):27–42

    Article  PubMed  Google Scholar 

  35. Orlic D, Kajstura J, Chimenti S et al (2001) Bone marrow cells regenerate infarcted myocardium. Nature 410(6829):701–705

    Article  CAS  PubMed  Google Scholar 

  36. Miyahara Y, Nagaya N, Kataoka M et al (2006) Monolayered mesenchymal stem cells repair scarred myocardium after myocardial infarction. Nat Med 12(4):459–465

    Article  CAS  PubMed  Google Scholar 

  37. Amado LC, Saliaris AP, Schuleri KH et al (2005) Cardiac repair with intramyocardial injection of allogeneic mesenchymal stem cells after myocardial infarction. PNAS 102(32):11474–11479

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Ryan JM, Barry FP, Murphy JM et al (2005) Mesenchymal stem cells avoid allogeneic rejection. J Inflamm 2(1):8

    Article  CAS  Google Scholar 

  39. Strauer BE, Brehm M, Zeus T et al (2005) Regeneration of human infarcted heart muscle by intracoronary autologous bone marrow cell transplantation in chronic coronary artery disease: the IACT Study. J Am Coll Cardiol 46(9):1651–1658

    Article  PubMed  Google Scholar 

  40. Breitbach M, Bostani T, Roell W et al (2007) Potential risks of bone marrow cell transplantation into infarcted hearts. Blood 110(4):1362–1369

    Article  CAS  PubMed  Google Scholar 

  41. Mao C, Hou X, Wang B et al (2017) Intramuscular injection of human umbilical cord-derived mesenchymal stem cells improves cardiac function in dilated cardiomyopathy rats. Stem Cell Res Ther 8(1):18

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Bartolucci JG, Verdugo FJ, González PL et al (2017) Safety and efficacy of the intravenous infusion of umbilical cord mesenchymal stem cells in patients with heart failure: a phase 1/2 randomized controlled trial (RIMECARD Trial). Circ Res. https://doi.org/10.1161/circresaha.117.310712

    Article  PubMed  PubMed Central  Google Scholar 

  43. Mazo M, Gavira JJ, Pelacho B et al (2011) Adipose-derived stem cells for myocardial infarction. J Cardiovasc Transl 4(2):145–153

    Article  Google Scholar 

  44. Kastrup J, Haack-Sørensen M, Juhl M et al (2017) Cryopreserved off-the-shelf allogeneic adipose-derived stromal cells for therapy in patients with ischemic heart disease and heart failure-A Safety Study. Stem Cell Transl Med 6(11):1963–1971

    Article  CAS  Google Scholar 

  45. Matsuura K, Nagai T, Nishigaki N et al (2004) Adult cardiac Sca-1-positive cells differentiate into beating cardiomyocytes. J Biol Chem 279(12):11384–11391

    Article  CAS  PubMed  Google Scholar 

  46. Laugwitz KL, Moretti A, Lam J et al (2005) Postnatal isl1 + cardioblasts enter fully differentiated cardiomyocyte lineages. Nature 433(7026):647–652

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Yellamilli A, van Berlo JH (2016) The role of cardiac side population cells in cardiac regeneration. Front Cell Dev Biol 4:102

    Article  PubMed  PubMed Central  Google Scholar 

  48. Zhou B, Ma Q, Rajagopal S et al (2008) Epicardial progenitors contribute to the cardiomyocyte lineage in the developing heart. Nature 454(7200):109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Chong JJH, Chandrakanthan V, Xaymardan M et al (2011) Adult cardiac-resident MSC-like stem cells with a proepicardial origin. Cell Stem Cell 9(6):527–540

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Santini MP, Forte E, Harvey RP et al (2016) Developmental origin and lineage plasticity of endogenous cardiac stem cells. Development 143(8):1242–1258

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. van Berlo JH, Kanisicak O, Maillet M et al (2014) c-kit + Cells minimally contribute cardiomyocytes to the heart. Nature 509:337–341

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Sultana N, Zhang L, Yan J et al (2015) Resident c-kit + cells in the heart are not cardiac stem cells. Nat Commun 6:8701

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Maliken BD, Molkentin JD (2018) Undeniable evidence that the adult mammalian heart lacks an endogenous regenerative stem cell. Circulation 138(8):806–808

    Article  PubMed  PubMed Central  Google Scholar 

  54. Minteer D, Marra KG, Rubin JP (2013) Adipose derived mesenchymal stem cells: biology and potential applications. Adv Biochem Eng Biotechnol 129:59–71

    CAS  PubMed  Google Scholar 

  55. Dalous J, Larghero J, Baud O (2012) Transplantation of umbilical cord-derived mesenchymal stem cells as a novel strategy to protect the central nervous system: technical aspects, preclinical studies, and clinical perspectives. Pediatr Res 71:482–490

    Article  CAS  PubMed  Google Scholar 

  56. Tolar J, Nauta AJ, Osborn MJ et al (2007) Sarcoma derived from cultured mesenchymal stem cells. Stem Cells 25:371–379

    Article  CAS  PubMed  Google Scholar 

  57. Jeong JO, Han JW, Kim JM et al (2011) Malignant tumor formation after transplantation of short-term cultured bone marrow mesenchymal stem cells in experimental myocardial infarction and diabetic neuropathy. Circ Res 108:1340–1347

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Kamat P, Schweizer R, Kaenel P et al (2015) Human adipose-derived mesenchymal stromal cells may promote breast cancer progression and metastatic spread. Plast Reconstr Surg 136:76–84

    Article  CAS  PubMed  Google Scholar 

  59. Karnoub AE, Dash AB, Vo AP et al (2007) Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nature 449:557–563

    Article  CAS  PubMed  Google Scholar 

  60. Cui CH, Uyama T, Miyado K et al (2007) Menstrual blood-derived cells confer human dystrophin expression in the murine model of Duchenne muscular dystrophy via cell fusion and myogenic transdifferentiation. Mol Biol Cell 18(5):1586–1594

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Hida N, Nishiyama N, Miyoshi S et al (2008) Novel cardiac precursor-like cells from human menstrual blood-derived mesenchymal cells. Stem cells 26(7):1695–1704

    Article  CAS  PubMed  Google Scholar 

  62. Han X, Meng X, Yin Z et al (2009) Inhibition of intracranial glioma growth by endometrial regenerative cells. Cell Cycle 8(4):606–610

    Article  CAS  PubMed  Google Scholar 

  63. Borlongan CV, Kaneko Y, Maki M et al (2010) Menstrual blood cells display stem cell-like phenotypic markers and exert neuroprotection following transplantation in experimental stroke. Stem Cells Dev 19(4):439–452

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Peron JPS, Jazedje T, Brandao WN et al (2012) Human endometrial-derived mesenchymal stem cells suppress inflammation in the central nervous system of EAE mice. Stem Cell Rev Rep 8(3):940–952

    Article  CAS  PubMed  Google Scholar 

  65. Mou X, Lin J, Chen J et al (2013) Menstrual blood-derived mesenchymal stem cells differentiate into functional hepatocyte-like cells. J Zhejiang Univ Sci B 14(11):961–972

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Zhang Z, Wang J, Xu Y et al (2013) Menstrual blood derived mesenchymal cells ameliorate cardiac fibrosis via inhibition of endothelial to mesenchymal transition in myocardial infarction. Int J Cardiol 168(2):1711–1714

    Article  PubMed  Google Scholar 

  67. Liu T, Huang Y, Zhang J et al (2014) Transplantation of human menstrual blood stem cells to treat premature ovarian failure in mouse model. Stem Cells Dev 23(13):1548–1557

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Wu X, Luo Y, Chen J et al (2014) Transplantation of human menstrual blood progenitor cells improves hyperglycemia by promoting endogenous progenitor differentiation in type 1 diabetic mice. Stem Cells Dev 23(11):1245–1257

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Lv Y, Xu X, Zhang B et al (2014) Endometrial regenerative cells as a novel cell therapy attenuate experimental colitis in mice. J Transl Med 12(1):344

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Alcayaga-Miranda F, Cuenca J, Martin A et al (2015) Combination therapy of menstrual derived mesenchymal stem cells and antibiotics ameliorates survival in sepsis. Stem Cell Res Ther 6(1):1–13

    Article  CAS  Google Scholar 

  71. Sun P, Liu J, Li W et al (2016) Human endometrial regenerative cells attenuate renal ischemia reperfusion injury in mice. J Transl Med 14(1):1–13

    Article  CAS  Google Scholar 

  72. Lu S, Shi G, Xu X et al (2016) Human endometrial regenerative cells alleviate carbon tetrachloride-induced acute liver injury in mice. J Transl Med 14(1):300

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Chen L, Zhang C, Chen L et al (2017) Human menstrual blood-derived stem cells ameliorate liver fibrosis in mice by targeting hepatic stellate cells via paracrine mediators. Stem Cells Transl Med 6(1):272–284

    Article  CAS  PubMed  Google Scholar 

  74. Zhang Y, Lin X, Dai Y et al (2016) Endometrial stem cells repair injured endometrium and induce angiogenesis via AKT and ERK pathways. Reproduction 152(5):389–402

    Article  CAS  PubMed  Google Scholar 

  75. Xu X, Li X, Gu X et al (2017) Prolongation of cardiac allograft survival by endometrial regenerative cells: focusing on b-cell responses. Stem Cells Transl Med 6(3):778–787

    Article  CAS  PubMed  Google Scholar 

  76. Lan X, Wang G, Xu X et al (2017) Stromal cell-derived factor-1 mediates cardiac allograft tolerance induced by human endometrial regenerative cell-based therapy. Stem Cells Transl Med 6(11):1997–2008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Xiang B, Chen L, Wang X et al (2017) Transplantation of menstrual blood-derived mesenchymal stem cells promotes the repair of LPS-induced acute lung injury. Int J Mol Sci 18(4):689

    Article  CAS  PubMed Central  Google Scholar 

  78. Fathi-Kazerooni M, Tavoosidana G, Taghizadeh-Jahed M et al (2017) Comparative restoration of acute liver failure by menstrual blood stem cells compared with bone marrow stem cells in mice model. Cytotherapy 19(12):1474–1490

    Article  PubMed  Google Scholar 

  79. Domnina A, Novikova P, Obidina J et al (2018) Human mesenchymal stem cells in spheroids improve fertility in model animals with damaged endometrium. Stem Cell Res Ther 9(1):50

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Zhao Y, Chen X, Wu Y et al (2018) Transplantation of human menstrual blood-derived mesenchymal stem cells alleviates Alzheimer’s disease-like pathology in APP/PS1 transgenic mice. Front Mol Neurosci 11:140

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  81. Tan J, Li P, Wang Q et al (2016) Autologous menstrual blood-derived stromal cells transplantation for severe Asherman’s syndrome. Hum Reprod 31(12):2723–2729

    Article  PubMed  Google Scholar 

  82. Ichim TE, Alexandrescu DT, Solano F et al (2010) Mesenchymal stem cells as anti-inflammatories: implications for treatment of Duchenne muscular dystrophy. Cell Immunol 260(2):75–82

    Article  CAS  PubMed  Google Scholar 

  83. Ichim TE, Solano F, Lara F et al (2010) Combination stem cell therapy for heart failure. Int Arch Med 3(1):5

    Article  PubMed  PubMed Central  Google Scholar 

  84. Bockeria L, Bogin V, Bockeria O et al (2013) Endometrial regenerative cells for treatment of heart failure: a new stem cell enters the clinic. J Transl Med 11(5):56

    Article  PubMed  PubMed Central  Google Scholar 

  85. Mclennan CE, Rydell ALFH (1965) Extent of endometrial shedding during normal menstruation. Obst Gyn 26(5):605–621

    CAS  Google Scholar 

  86. Gargett CE (2007) Uterine stem cells: what is the evidence? Hum Reprod Update 13(1):87–101

    Article  CAS  PubMed  Google Scholar 

  87. Gargett CE, Masuda H (2010) Adult stem cells in the endometrium. Mol Hum Reprod 16(11):818–834

    Article  CAS  PubMed  Google Scholar 

  88. Liu Y, Niu R, Yang F et al (2018) Biological characteristics of human menstrual blood-derived endometrial stem cells. J Cell Mol Med 22(3):1627–1639

    Article  CAS  PubMed  Google Scholar 

  89. Bolli R (2017) Repeated cell therapy: a paradigm shift whose time has come. Circ Res 120(7):1072–1074

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Wang Y, Han ZB, Ma J et al (2011) A toxicity study of multiple-administration human umbilical cord mesenchymal stem cells in cynomolgus monkeys. Stem Cells Dev 21(9):1401–1408

    Article  CAS  PubMed  Google Scholar 

  91. Tokita Y, Tang XL, Li Q et al (2016) Repeated administrations of cardiac progenitor cells are markedly more effective than a single administration: a new paradigm in cell therapy. Circ Res 119(5):635–651

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Mann I, Rodrigo SF, van Ramshorst J et al (2015) Repeated intramyocardial bone marrow cell injection in previously responding patients with refractory angina again improves myocardial perfusion, anginal complaints, and quality of life. Circ Cardiovasc Int 8(8):e002740

    Google Scholar 

  93. Tang XL, Nakamura S, Li Q et al (2018) Repeated administrations of cardiac progenitor cells are superior to a single administration of an equivalent cumulative dose. J Am Heart Assoc 7(4):e007400

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Masuda H, Anwar SS, Bühring HJ et al (2012) A novel marker of human endometrial mesenchymal stem-like cells. Cell Transpl 21(10):2201–2214

    Article  Google Scholar 

  95. Schwab KE, Gargett CE (2007) Co-expression of two perivascular cell markers isolates mesenchymal stem-like cells from human endometrium. Hum Reprod 22(11):2903–2911

    Article  CAS  PubMed  Google Scholar 

  96. Cervelló I, Gil-Sanchis C, Mas A et al (2010) Human endometrial side population cells exhibit genotypic, phenotypic and functional features of somatic stem cells. PLoS One 5(6):e10964

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Masuda H, Matsuzaki Y, Hiratsu E et al (2010) Stem cell-like properties of the endometrial side population: implication in endometrial regeneration. PLoS One 5(4):e10387

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Kamp TJ (2011) Recognizing heart cells in a crowd. Nat Methods 8(12):1013

    Article  CAS  PubMed  Google Scholar 

  99. Li TS, Cheng K, Malliaras K et al (2012) Direct comparison of different stem cell types and subpopulations reveals superior paracrine potency and myocardial repair efficacy with cardiosphere-derived cells. J Am Coll Cardiol 59(10):942–953

    Article  PubMed  PubMed Central  Google Scholar 

  100. Patel AN, Park E, Kuzman M et al (2008) Multipotent menstrual blood stromal stem cells: isolation, characterization, and differentiation. Cell Transpl 17(3):303–311

    Article  Google Scholar 

  101. Calloni R, Cordero EAA, Henriques JAP et al (2013) Reviewing and updating the major molecular markers for stem cells. Stem Cells Dev 22(9):1455–1476

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Sani F, Borzooeian G, Kazemnejad S et al (2016) Differentiation of menstrual blood derived stem cell (MensSCs) to hepatocyte-liked cell on three dimensional nanofiberscaffold: poly caprolacton (PCL). J Biomed Sci Eng 9(04):216

    Article  CAS  Google Scholar 

  103. Faramarzi H, Mehrabani D, Fard M et al (2016) The potential of menstrual blood-derived stem cells in differentiation to epidermal lineage: a preliminary report. World J Plast Surg 5(1):26

    PubMed  PubMed Central  Google Scholar 

  104. Chen X, Kong X, Liu D et al (2016) In vitro differentiation of endometrial regenerative cells into smooth muscle cells: a potential approach for the management of pelvic organ prolapse. Int J Mol Med 38(1):95–104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Zheng SX, Wang J, Wang XL et al (2018) Feasibility analysis of treating severe intrauterine adhesions by transplanting menstrual blood-derived stem cells. Int J Mol Med 41(4):2201–2212

    CAS  PubMed  Google Scholar 

  106. Lai D, Guo Y, Zhang Q et al (2016) Differentiation of human menstrual blood-derived endometrial mesenchymal stem cells into oocyte-like cells. Acta Bioch Bioph Sin 48(11):998–1005

    Article  CAS  Google Scholar 

  107. Akhavan-Tavakoli M, Fard M, Khanjani S et al (2017) In vitro differentiation of menstrual blood stem cells into keratinocytes: a potential approach for management of wound healing. Biologicals 48:66–73

    Article  CAS  PubMed  Google Scholar 

  108. Jiang Z, Hu X, Yu H et al (2013) Human endometrial stem cells confer enhanced myocardial salvage and regeneration by paracrine mechanisms. J Cell Mol Med 17(10):1247–1260

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Szaraz P, Gratch YS, Iqbal F et al (2017) In vitro differentiation of human mesenchymal stem cells into functional cardiomyocyte-like cells. J Vis Exp 126:e55757

    Google Scholar 

  110. Pei Z, Zeng J, Song Y et al (2017) In vivo imaging to monitor differentiation and therapeutic effects of transplanted mesenchymal stem cells in myocardial infarction. Sci Rep 7(1):6296

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Balsam LB, Wagers AJ, Christensen JL et al (2004) Haematopoietic stem cells adopt mature haematopoietic fates in ischaemic myocardium. Nature 428(6983):668

    Article  CAS  PubMed  Google Scholar 

  112. Bagno L, Hatzistergos KE, Balkan W et al (2018) Mesenchymal stem cell-based therapy for cardiovascular disease: progress and challenges. Mol Ther 26(7):1610–1623

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Kardami E, Banerji S, Doble BW et al (2003) PKC-dependent phosphorylation may regulate the ability of connexin43 to inhibit DNA synthesis. Cell Commun Adhes 10:293–297

    Article  CAS  PubMed  Google Scholar 

  114. Hinrichsen R, Haunso S, Busk PK (2007) Different regulation of p27 and Akt during cardiomyocyte proliferation and hypertrophy. Growth Fact 25:132–140

    Article  CAS  Google Scholar 

  115. Zhou B, Honor LB, He H et al (2011) Adult mouse epicardium modulates myocardial injury by secreting paracrine factors. J Clin Invest 121:1894–1904

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Przybyt E, Krenning G, Brinker MG et al (2013) Adipose stromal cells primed with hypoxia and inflammation enhance cardiomyocyte proliferation rate in vitro through STAT3 and Erk1/2. J Transl Med 11:39

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Novoyatleva T, Diehl F, van Amerongen MJ et al (2010) TWEAK is a positive regulator of cardiomyocyte proliferation. Cardiovasc Res 85:681–690

    Article  CAS  PubMed  Google Scholar 

  118. Lemmens K, Doggen K, De Keulenaer GW (2007) Role of neuregulin-1/ErbB signaling in cardiovascular physiology and disease: implications for therapy of heart failure. Circulation 116:954–960

    Article  CAS  PubMed  Google Scholar 

  119. Kuhn B, del Monte F, Hajjar RJ et al (2007) Periostin induces proliferation of differentiated cardiomyocytes and promotes cardiac repair. Nat Med 13:962–969

    Article  CAS  PubMed  Google Scholar 

  120. Nygren JM, Jovinge S, Breitbach M et al (2004) Bone marrow-derived hematopoietic cells generate cardiomyocytes at a low frequency through cell fusion, but not transdifferentiation. Nat Med 10(5):494

    Article  CAS  PubMed  Google Scholar 

  121. Malliaras K, Marbán E (2011) Cardiac cell therapy: where we’ve been, where we are, and where we should be headed. Brit Med Bull 98(1):161–185

    Article  PubMed  PubMed Central  Google Scholar 

  122. Golpanian S, Wolf A, Hatzistergos KE et al (2016) Rebuilding the damaged heart: mesenchymal stem cells, cell-based therapy, and engineered heart tissue. Physiol Rev 96(3):1127–1168

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Beigi F, Schmeckpeper J, Pow-anpongkul P et al (2013) C3orf58, a novel paracrine protein, stimulates cardiomyocyte cell-cycle progression through the PI3K–AKT–CDK7 pathway. Circ Res 113(4):372–380

    Article  CAS  PubMed  Google Scholar 

  124. Chen L, Xiang B, Wang X et al (2017) Exosomes derived from human menstrual blood-derived stem cells alleviate fulminant hepatic failure. Stem Cell Res Ther 8(1):9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Hu X, Yu SP, Fraser JL et al (2008) Transplantation of hypoxia-preconditioned mesenchymal stem cells improves infarcted heart function via enhanced survival of implanted cells and angiogenesis. J Thorac Cardiovasc Surg 135(4):799–808

    Article  CAS  PubMed  Google Scholar 

  126. Yan F, Yao Y, Chen L et al (2012) Hypoxic preconditioning improves survival of cardiac progenitor cells: role of stromal cell derived factor-1α–CXCR4 axis. PLoS One 7(7):e37948

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Butler J, Epstein SE, Greene SJ et al (2017) Intravenous allogeneic mesenchymal stem cells for nonischemic cardiomyopathy: safety and efficacy results of a phase II—a randomized trial. Circ Res 120(2):332–340

    Article  CAS  PubMed  Google Scholar 

  128. Makrigiannakis A, Karamouti M, Drakakis P et al (2008) Fetomaternal immunotolerance. Am J Reprod Immunol 60(6):482–496

    Article  CAS  PubMed  Google Scholar 

  129. Nikoo S, Ebtekar M, Jeddi-Tehrani M et al (2012) Effect of menstrual blood-derived stromal stem cells on proliferative capacity of peripheral blood mononuclear cells in allogeneic mixed lymphocyte reaction. J Obstet Gynaecol Res 38(5):804–809

    Article  CAS  PubMed  Google Scholar 

  130. Murphy MP, Wang H, Patel AN et al (2008) Allogeneic endometrial regenerative cells: an “Off the shelf solution” for critical limb ischemia? J Transl Med 6(1):45

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  131. Weidner CI, Walenda T, Lin Q et al (2013) Hematopoietic stem and progenitor cells acquire distinct DNA-hypermethylation during in vitro culture. Sci Rep 3:3372

    Article  PubMed  PubMed Central  Google Scholar 

  132. Le Blanc K, Frassoni F, Ball L et al (2008) Mesenchymal stem cells for treatment of steroid-resistant, severe, acute graft-versus-host disease: a phase II study. Lancet 371(9624):1579–1586

    Article  CAS  PubMed  Google Scholar 

  133. Campisi J, di Fagagna FA (2007) Cellular senescence: when bad things happen to good cells. Nat Rev Mol Cell Biol 8(9):729

    Article  CAS  PubMed  Google Scholar 

  134. Quyyumi AA, Waller EK, Murrow J et al (2011) CD34 + cell infusion after ST elevation myocardial infarction is associated with improved perfusion and is dose dependent. Am Heart J 161(1):98–105

    Article  PubMed  Google Scholar 

  135. Florea V, Rieger AC, DiFede DL et al (2017) Dose comparison study of allogeneic mesenchymal stem cells in patients with ischemic cardiomyopathy (The TRIDENT Study). Circ Res 121(11):1279–1290

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Perin EC, Borow KM, Silva GV et al (2015) A phase II dose-escalation study of allogeneic mesenchymal precursor cells in patients with ischemic or nonischemic heart failure. Circ Res 117(6):576–584

    Article  CAS  PubMed  Google Scholar 

  137. Losordo DW, Henry TD, Davidson C et al (2011) Intramyocardial, autologous CD34 + cell therapy for refractory angina. Circ Res 109(4):428–436

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  138. Hare JM, Fishman JE, Gerstenblith G et al (2012) Comparison of allogeneic vs autologous bone marrow–derived mesenchymal stem cells delivered by transendocardial injection in patients with ischemic cardiomyopathy: the POSEIDON randomized trial. JAMA 308(22):2369–2379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  139. Golpanian S, Schulman IH, Ebert RF et al (2016) Concise review: review and perspective of cell dosage and routes of administration from preclinical and clinical studies of stem cell therapy for heart disease. Stem Cell Transl Med 5(2):186–191

    Article  Google Scholar 

  140. Price MJ, Chou CC, Frantzen M et al (2006) Intravenous mesenchymal stem cell therapy early after reperfused acute myocardial infarction improves left ventricular function and alters electrophysiologic properties. Int J Cardiol 111(2):231–239

    Article  PubMed  Google Scholar 

  141. Rigol M, Solanes N, Farré J et al (2010) Effects of adipose tissue-derived stem cell therapy after myocardial infarction: impact of the route of administration. J Card Fail 16(4):357–366

    Article  CAS  PubMed  Google Scholar 

  142. Huang P, Tian X, Li Q et al (2016) New strategies for improving stem cell therapy in ischemic heart disease. Heart Fail Rev 21(6):737–752

    Article  CAS  PubMed  Google Scholar 

  143. Vulliet PR, Greeley M, Halloran SM et al (2004) Intra-coronary arterial injection of mesenchymal stromal cells and microinfarction in dogs. Lancet 363(9411):783–784

    Article  PubMed  Google Scholar 

  144. Perin EC, Silva GV, Hare JA et al (2008) Comparison of intracoronary and transendocardial delivery of allogeneic mesenchymal cells in a canine model of acute myocardial infarction. J Mol Cell Cardiol 44(3):486–495

    Article  CAS  PubMed  Google Scholar 

  145. Vrtovec B, Poglajen G, Lezaic L et al (2013) Comparison of transendocardial and intracoronary CD34 + cell transplantation in patients with nonischemic dilated cardiomyopathy. Circulation 128(11 suppl 1):S42–S49

    Article  CAS  PubMed  Google Scholar 

  146. Vrtovec B, Poglajen G, Lezaic L et al (2013) Effects of intracoronary CD34 + stem cell transplantation in nonischemic dilated cardiomyopathy patients: 5-year follow-up. Circ Res 112(1):165–173

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We would like to acknowledge the China Scholarship Council, the National Natural Science Foundation of China (81671619 and 81771226) and the Xinxiang Foundation (20172DCG-03 and ZD17008) for their financial support.

Author information

Authors and Affiliations

  1. Stem Cell and Biotherapy Technology Research Center, College of Life Science and Technology, Henan Key Laboratory of Medical Tissue Regeneration, Xinxiang Medical University, Xinxiang, 453003, People’s Republic of China

    Yanli Liu, Rongcheng Niu & Juntang Lin

  2. Institute of Chemistry and Biochemistry, Free University Berlin, 14195, Berlin, Germany

    Yanli Liu, Wenzhong Li & Nan Ma

  3. Deutsches Herzzentrum Berlin (DHZB), Berlin, Germany

    Christof Stamm

  4. German Center for Cardiovascular Research (DZHK), Partner Site Berlin, Berlin, Germany

    Christof Stamm

  5. Berlin-Brandenburg Center for Regenerative Therapies (BCRT), Charité-Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin, Berlin, Germany

    Christof Stamm

  6. Berlin Institute of Health, Berlin, Germany

    Christof Stamm

  7. Department of Cardiac Surgery, Reference and Translation Center for Cardiac Stem Cell Therapy, University Rostock, 18055, Rostock, Germany

    Gustav Steinhoff & Nan Ma

  8. Institute of Biomaterial Science and Berlin-Brandenburg Center for Regenerative Therapies, Helmholtz-Zentrum Geesthacht, 14513, Teltow, Germany

    Nan Ma

Authors
  1. Yanli Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rongcheng Niu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Wenzhong Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Juntang Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Christof Stamm
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Gustav Steinhoff
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Nan Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Wenzhong Li or Juntang Lin.

Ethics declarations

Conflict of interest

The authors declare that there are no conflicts of interest regarding the publication of this paper.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, Y., Niu, R., Li, W. et al. Therapeutic potential of menstrual blood-derived endometrial stem cells in cardiac diseases. Cell. Mol. Life Sci. 76, 1681–1695 (2019). https://doi.org/10.1007/s00018-019-03019-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00018-019-03019-2

Keywords

Search

Navigation