The endometrium as a source of mesenchymal stem cells in domestic animals and possible applications in veterinary medicine
Article Sidebar
Main Article Content
Abstract
ISSN: 2448-6760
Cite this as:
- Serrato López AG, Montesinos Montesinos JJ, Anzaldúa Arce SR. The endometrium as a source of mesenchymal stem cells in domestic animals and possible applications in veterinary medicine. Veterinaria México OA. 2017;4(3). doi: 10.21753/vmoa.4.3.441.
Mesenchymal stem cells (MSCs) have been isolated from the endometrium of humans, mice, cows, pigs and ewes. Typically, these cells are detected in the deep regions of the endometrium, closer to the union with the myometrium. MSCs possess characteristics such as clonogenicity and multipotentiality since they can differentiate in vitro into adipogenic, chondrogenic and osteogenic lineages. These cells can be induced to differentiate in vitro not only into the mesodermal lineage but also into the endodermal and ectodermal lineages. Therefore, MSCs show a great regenerative capacity for various organs and tissues, including the endometrium. Some advantages of endometrial MSCs compared with other MSC sources are their immune modulating activity, their ease of obtainment, and the amount of sample that may be collected. The study of endometrial MSCs in domestic animals is a new and promising field because increasing our understanding of the physiology and biology of these cells may lead to a better understanding of the physiopathology of reproductive diseases, and the development of treatment methods for infertility problems. In other veterinary medicine fields, MSCs can be used for the treatment of autoimmune diseases, cardiac affections, musculoskeletal and articular lesions, muscle degeneration, type 1 diabetes, urinary tract diseases, neurodegenerative processes and tumours. Finally, MSCs are also an important clinical tool for tissue engineering and regenerative medicine. The aim of this review is to present an updated outlook of the knowledge regarding endometrial MSCs and their possible applications in veterinary medicine.
Article Details
References
Gargett CE, Schwab KE, Zillwood RM, Nguyen HPT, Wu D. Isolation and culture of epithelial progenitors and mesenchymal stem cells from human endometrium. Biol Reprod. 2009;80:1136-45. doi: 10.1095/biolreprod.108.075226.
McLennan CE, Rydell AH. Extent of endometrial shedding during normal menstruation. Obstet Gynecol. 1965;26:605-21.
Slayden OD, Brenner RM. Hormonal regulation and localization of estrogen, progestin and androgen receptors in the endometrium of nonhuman primates: effects of progesterone receptor antagonists. Arch Histol Cytol. 2004;67:393-409.
Gargett CE. Uterine stem cells: What is the evidence? Hum Reprod Update. 2007;13:87-101. doi: 10.1093/humupd/dml045.
Prianishnikov VA. On the concept of stem cell and a model of functional-morphological structure of the endometrium. Contraception. 1978;18:213-23.
Hartman CG. Regeneration of the monkey uterus after surgical removal of the endometrium and accidental endometriosis. West J Surg. 1944;52:87-102.
Tresserra F, Grases P, Ubeda A, Pascual MA, Grases PJ, Labastida R. Morphological changes in hysterectomies after endometrial ablation. Hum Reprod. 1999;14:1473-77.
Abbott JA, Garry R. The surgical management of menorrhagia. Hum Reprod Update. 2002;8:68-78.
Wood C, Rogers P. A pregnancy after planned partial endometrial resection. Aust N Z J Obstet Gynaecol. 1993;33:316-8. doi: 10.1111/j.1479-828X.1993. tb02097.x.
Bird CC, Willis RA. The production of smooth muscle by the endometrial stroma of the adult human uterus. J Pathol Bacteriol. 1965;90:75-81.
Mazur MT, Kraus FT. Histogenesis of morphologic variations in tumors of the uterine wall. Am J Surg Pathol. 1980;4:59-74.
Roth E, Taylor HB. Heterotopic cartilage in the uterus. Obstet Gynecol. 1966;27:838-44.
Chan RWS. Clonogenicity of Human Endometrial Epithelial and Stromal Cells. Biol Reprod. 2004;70:1738-50. doi: 10.1095/biolreprod.103.024109.
Gazit Z, Pelled G, Sheyn D, Kimelman N, Gazit D. Mesenchymal Stem Cells. In: Lanza R, Atala A, editors. Essentials of Stem Cell Biology. 3rd ed. San Diego, CA (US): Academic Press; 2013. p. 255-66.
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. doi: 10.1126/science.284.5411.143.
Zuk PA, Zhu M, Ashjian P, De Ugarte DA, Huang JI, Mizuno H, et al. Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell. 2002;13:4279–95.
Verdi J, Tan A, Shoae-Hassani A, Seifalian AM. Endometrial stem cells in regenerative medicine. J Biol Eng. 2014;8:20.
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. doi: 10.1080/14653240600855905.
Montesinos JJ, Castro-Manrreza E. Células troncales mesenquimales. In: Pelayo R, Santa-Olalla J, Velasco I, editors. Células troncales y medicina regenerativa. Ciudad de México (MX): Universidad Nacional Autónoma de México; 2011. p. 119-41.
Ulrich D, Muralitharan R, Gargett CE. Toward the use of endometrial and menstrual blood mesenchymal stem cells for cell-based therapies. Expert Opin Biol Ther. 2013;13:1387-400. doi: 10.1517/14712598.2013.826187.
Kobayashi A, Behringer RR. Developmental genetics of the female reproductive tract in mammals. Nat Rev Genet. 2003;4:969-80. doi: 10.1038/nrg1225.
Snyder EY, Loring JF. A role for stem cell biology in the physiological and pathological aspects of aging: Role for stem cell biology in aging. J Am Geriatr Soc. 2005;53:S287-S91. doi: 10.1111/j.1532-5415.2005.53491.x.
Blau HM, Brazelton TR, Weimann JM. The evolving concept of a stem cell: entity or function? Cell. 2001;105:829–41.
Körbling M, Estrov Z. Adult stem cells for tissue repair—a new therapeutic concept? New England Journal of Medicine. 2003;349:570–82.
Taylor HS. Endometrial cells derived from donor stem cells in bone marrow transplant recipients. JAMA. 2004;292:81–5.
Cervelló I, Gil-Sanchis C, Mas A, Faus A, Sanz J, Moscardó F, et al. Bone marrow-derived cells from male donors do not contribute to the endometrial side population of the recipient. PLoS ONE. 2012;7:e30260. doi: 10.1371/journal. pone.0030260.
Gargett CE, Nguyen HPT, Ye L. Endometrial regeneration and endometrial stem/ progenitor cells. Rev Endocr Metab Disord. 2012;13:235-51. doi: 10.1007/ s11154-012-9221-9.
Shirian S, Ebrahimi-Barough S, Saberi H, Norouzi-Javidan A, Mousavi SMM, Derakhshan MA, et al. Comparison of capability of human bone marrow mesenchymal stem cells and endometrial stem cells to differentiate into motor neurons on electrospun poly(ε-caprolactone) scaffold. Mol Neurobiol. 2016;53:5278- 87. doi: 10.1007/s12035-015-9442-5.
Dimitrov R, Timeva T, Kyurkchiev D, Stamenova M, Shterev A, Kostova P, et al. Characterization of clonogenic stromal cells isolated from human endometrium. Reproduction. 2008;135:551-8. doi: 10.1530/REP-07-0428.
Cho NH, Park YK, Kim YT, Yang H, Kim SK. Lifetime expression of stem cell markers in the uterine endometrium. Fertil Steril. 2004;81:403-7. doi: 10.1016/j. fertnstert.2003.07.015.
Matthai C. Oct-4 expression in human endometrium. Mol Hum Reprod. 2006;12:7-10. doi: 10.1093/molehr/gah254.
Bodek G, Bukowska J, Wisniewska J, Ziecik AJ. Evidence for the presence of stem/progenitor cells in porcine endometrium: stem/progenitor cells in porcine endometrium. Mol Reprod Dev. 2015;82:182-90. doi: 10.1002/mrd.22459.
Lynch L, Golden-Mason L, Eogan M, O’Herlihy C, O’Farrelly C. Cells with haematopoietic stem cell phenotype in adult human endometrium: relevance to infertility? Hum Reprod. 2007;22:919-26. doi: 10.1093/humrep/del456.
Meng X, Ichim TE, Zhong J, Rogers A, Yin Z, Jackson J, et al. Endometrial regenerative cells: a novel stem cell population. J Transl Med. 2007;5:57. doi: 10.1186/1479-5876-5-57.
Schwab KE, Gargett CE. Co-expression of two perivascular cell markers isolates mesenchymal stem-like cells from human endometrium. Hum Reprod. 2007;22:2903-11. doi: 10.1093/humrep/dem265.
Masuda H, Anwar SS, Bühring H-J, Rao JR, Gargett CE. A Novel Marker of Human Endometrial Mesenchymal Stem-Like Cells. Cell Transplant. 2012;21:2201-14. doi: 10.3727/096368911X637362.
Ishikawa M, Nakayama K, Yeasmin S, Katagiri A, Iida K, Nakayama N, et al. NAC1, a potential stem cell pluripotency factor expression in normal endometrium, endometrial hyperplasia and endometrial carcinoma. Int J Oncol. 2010;36:1097-103.
Wang J, Rao S, Chu J, Shen X, Levasseur DN, Theunissen TW, et al. A protein interaction network for pluripotency of embryonic stem cells. Nature. 2006;444:364-8. doi: 10.1038/nature05284.
Gargett CE, Zillwood RM, Schwab KE, Naqvi SZ. 236. Characterising the stem cell activity of human endometrial epithelial and stromal cells. Reprod Fertil Dev. 2005;17(9):93-. doi: 10.1071/SRB05Abs236.
Cervelló I, Gil-Sanchis C, Mas A, Delgado-Rosas F, Martínez-Conejero JA, Galán A, et al. Human endometrial side population cells exhibit genotypic, phenotypic and functional features of somatic stem cells. PLoS ONE. 2010;5:e10964. doi: 10.1371/journal.pone.0010964.
Bockeria L, Bogin V, Bockeria O, Le T, Alekyan B, Woods EJ, et al. Endometrial regenerative cells for treatment of heart failure: a new stem cell enters the clinic. J Transl Med. 2013;11(1):56. doi: 10.1186/1479-5876-11-56.
Cervelló I, Mas A, Gil-Sanchis C, Peris L, Faus A, Saunders PTK, et al. Reconstruction of endometrium from human endometrial side population cell lines. PLoS ONE. 2011;6:e21221. doi: 10.1371/journal.pone.0021221.
Wada-Hiraike O, Hiraike H, Okinaga H, Imamov O, Barros RPA, Morani A, et al. Role of estrogen receptor β in uterine stroma and epithelium: Insights from estrogen receptor β−/− mice. PNAS. 2006;103(4):18350–5. doi: 10.1073/ pnas.0608861103.
Masuda H, Maruyama T, Hiratsu E, Yamane J, Iwanami A, Nagashima T, et al. Noninvasive and real-time assessment of reconstructed functional human endometrium in NOD/SCID/γcnull immunodeficient mice. PNAS. 2007;104:1925–30.
Goodell MA, Brose K, Paradis G, Conner AS, Mulligan RC. Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. J Exp Med. 1996;183:1797-806.
Bunting KD, Zhou S, Lu T, Sorrentino BP. Enforced P-glycoprotein pump function in murine bone marrow cells results in expansion of side population stem cells in vitro and repopulating cells in vivo. Blood. 2000;96:902–9.
Scharenberg CW, Harkey MA, Torok-Storb B. The ABCG2 transporter is an efficient Hoechst 33342 efflux pump and is preferentially expressed by immature human hematopoietic progenitors. Blood. 2002;99:507–12.
Smalley MJ, Clarke RB. The mammary gland “side population”: a putative stem/ progenitor cell marker? J Mammary Gland Biol Neoplasia. 2005;10:37-47. doi: 10.1007/s10911-005-2539-0.
Miyazaki K, Maruyama T, Masuda H, Yamasaki A, Uchida S, Oda H, et al. Stem cell-like differentiation potentials of endometrial side population cells as revealed by a newly developed in vivo endometrial stem cell assay. PLoS ONE. 2012;7:e50749. doi: 10.1371/journal.pone.0050749.
Chan RWS, Kaitu’u-Lino Tu, Gargett CE. Role of label-retaining cells in estrogen-induced endometrial regeneration. Reprod Sci. 2012;19:102-14. doi: 10.1177/1933719111414207.
Chan RWS, Gargett CE. Identification of label-retaining cells in mouse endometrium. Stem Cells. 2006;24:1529-38. doi: 10.1634/stemcells.2005-0411.
Martin L, Finn CA. Interactions of oestradiol and progestins in the mouse uterus. J Endocrinol. 1970;48:109–15.
Deane JA, Ong YR, Cain JE, Jayasekara WSN, Tiwari A, Carlone DL, et al. The mouse endometrium contains epithelial, endothelial and leucocyte populations expressing the stem cell marker telomerase reverse transcriptase. Mol Hum Reprod. 2016;22:272-84. doi: 10.1093/molehr/gav076.
Cervelló I, Martínez-Conejero JA, Horcajadas JA, Pellicer A, Simón C. Identification, characterization and co-localization of label-retaining cell population in mouse endometrium with typical undifferentiated markers. Hum Reprod. 2007;22:45-51. doi: 10.1093/humrep/del332.
Braun KM, Watt FM. Epidermal label-retaining cells: background and recent applications. J Investig Dermatol Symp Proc. 2004;9(3):196–201. doi: 10.1111/j.1087-0024.2004.09313.x.
Li Y, Rosen JM. Stem/progenitor cells in mouse mammary gland development and breast cancer. J Mammary Gland Biol Neoplasia. 2005;10:17-24. doi: 10.1007/s10911-005-2537-2.
Szotek PP, Chang HL, Zhang L, Preffer F, Dombkowski D, Donahoe PK, et al. Adult mouse myometrial label-retaining cells divide in response to gonadotropin stimulation. Stem Cells. 2007;25:1317-25. doi: 10.1634/stemcells.2006-0204.
Donofrio G, Franceschi V, Capocefalo A, Cavirani S, Sheldon I. Bovine endometrial stromal cells display osteogenic properties. Reproductive Biology and Endocrinology. 2008;6:65. doi: 10.1186/1477-7827-6-65.
Cabezas J, Lara E, Pacha P, Rojas D, Veraguas D, Saravia F, et al. The endometrium of cycling cows contains populations of putative mesenchymal progenitor cells. Reprod Domest Anim. 2014;49:550-9. doi: 10.1111/rda.12309.
Miernik K, Karasinski J. Porcine uterus contains a population of mesenchymal stem cells. Reproduction. 2012;143:203-9. doi: 10.1530/REP-11-0202.
Letouzey V, Tan KS, Deane JA, Ulrich D, Gurung S, Ong YR, et al. Isolation and characterisation of mesenchymal stem/stromal cells in the ovine endometrium. PLos ONE. 2015;10:e0127531. doi: 10.1371/journal.pone.0127531.
Arck P, Solano ME, Walecki M, Meinhardt A. The immune privilege of testis and gravid uterus: Same difference? Mol Cell Endocrinol. 2014;382:509-20. doi: 10.1016/j.mce.2013.09.022.
Popp FC, Renner P, Eggenhofer E, Slowik P, Geissler EK, Piso P, et al. Mesenchymal stem cells as immunomodulators after liver transplantation. Liver Transpl. 2009;15:1192-8. doi: 10.1002/lt.21862.
Ma S, Xie N, Li W, Yuan B, Shi Y, Wang Y. Immunobiology of mesenchymal stem cells. Cell Death Differ. 2014;21:216. doi: 10.1038/cdd.2013.158.
Prockop DJ, Youn Oh J. Mesenchymal stem/stromal cells (MSCs): role as guardians of inflammation. Mol Ther. 2012;20:14-20. doi: 10.1038/mt.2011.211.
Castro-Manrreza ME, Montesinos JJ. Immunoregulation by mesenchymal stem cells: Biological aspects and clinical applications. J Immunol Res. 2015;2015:1- 20. doi: 10.1155/2015/394917.
Sotiropoulou PA, Perez SA, Gritzapis AD, Baxevanis CN, Papamichail M. Interactions between human mesenchymal stem cells and natural killer cells. Stem Cells. 2006;24:74-85. doi: 10.1634/stemcells.2004-0359.
Bozorgmehr M, Moazzeni SM, Salehnia M, Sheikhian A, Nikoo S, Zarnani A-H. Menstrual blood-derived stromal stem cells inhibit optimal generation and maturation of human monocyte-derived dendritic cells. Immunol Lett. 2014;162:239-46. doi: 10.1016/j.imlet.2014.10.005.
Ghannam S, Bouffi C, Djouad F, Jorgensen C, Noël D. Immunosuppression by mesenchymal stem cells: mechanisms and clinical applications. Stem Cell Res Ther. 2010;1:2. doi: 10.1186/scrt2.
Montesinos JJ, Mora-García MdL, Mayani H, Flores-Figueroa E, García-Rocha R, Fajardo-Orduña GR, et al. In vitro evidence of the presence of mesenchymal stromal cells in cervical cancer and their role in protecting cancer cells from cytotoxic T cell activity. Stem Cells Dev. 2013;22:2508-19. doi: 10.1089/ scd.2013.0084.
Fajardo-Orduña GR, Mayani H, Castro-Manrreza ME, Flores-Figueroa E, Flores-Guzmán P, Arriaga-Pizano L, et al. Bone marrow mesenchymal stromal cells from clinical scale culture: in vitro evaluation of their differentiation, hematopoietic support, and immunosuppressive capacities Stem Cells Dev. 2016;25(17):1299-310. doi: 10.1089/scd.2016.0071.
Ding L, Li Xa, Sun H, Su J, Lin N, Péault B, et al. Transplantation of bone marrow mesenchymal stem cells on collagen scaffolds for the functional regeneration of injured rat uterus. Biomaterials. 2014;35:4888-900. doi: 10.1016/j. biomaterials.2014.02.046.
Cervelló I, Santamaría X, Miyazaki K, Maruyama T, Simón C. Cell therapy and tissue engineering from and toward the uterus. Semin Reprod Med. 2015;33:366- 72. doi: 10.1055/s-0035-1559581.
Donnez J, Nisolle M. An Atlas of Laser Operative Laparoscopy and Hysteroscopy (Encyclopedia of Visual Medicine Series). Chicago, IL (US): Parthenon Pub; 1994.
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;31:1087-96. doi: 10.1093/humrep/dew042.
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. doi: 10.1371/journal.pone.0096662.
Gargett CE, Healy DL. Generating receptive endometrium in Asherman’s syndrome. J Hum Reprod Sci. 2011;4(1):49-52.
Ettinger B, Bainton L, Upmails DH, Citron JT, VanGessel A. Comparison of endometrial growth produced by unopposed conjugated estrogens or by micronized estradiol in postmenopausal women. Am J Obstet Gynecol. 1997;176:112-7.
Paulson RJ, Boostanfar R, Saadat P, Mor E, Tourgeman DE, Slater CC, et al. Pregnancy in the sixth decade of life: obstetric outcomes in women of advanced reproductive age. JAMA. 2002;288:2320-3. doi: 10.1001/jama.288.18.2320.
Aresu L, Benali S, Giannuzzi D, Mantovani R, Castagnaro M, Falomo ME. The role of inflammation and matrix metalloproteinases in equine endometriosis. J Vet Sci. 2012;13:171-7. doi: 10.4142/jvs.2012.13.2.171.
Hoffmann C, Ellenberger C, Mattos RC, Aupperle H, Dhein S, Stief B, et al. The equine endometrosis: new insights into the pathogenesis. Anim Reprod Sci. 2009;111:261-78. doi: 10.1016/j.anireprosci.2008.03.019.
Kenney RM. The etiology, diagnosis and classification of chronic degenerative endometritis. Equine Vet J. 1992;25:186.
Mambelli LI, Mattos RC, Winter GHZ, Madeiro DS, Morais BP, Malschitzky E, et al. Changes in expression pattern of selected endometrial proteins following mesenchymal stem cells infusion in mares with endometrosis. PLoS ONE. 2014;9:e97889. doi: 10.1371/journal.pone.0097889.
Seli E, Berkkanoglu M, Arici A. Pathogenesis of endometriosis. Obstet Gynecol Clin North Am. 2003;30:41-61.
Arora N, Sandford J, Browning GF, Sandy JR, Wright PJ. A model for cystic endometrial hyperplasia/pyometra complex in the bitch. Theriogenology. 2006;66:1530-6. doi: 10.1016/j.theriogenology.2006.02.019.
Cui C-H, Uyama T, Miyado K, Terai M, Kyo S, Kiyono T, et al. 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. 2007;18(5):1586-94. doi: 10.1091/mbc.E06-09-0872.
Hida N, Nishiyama N, Miyoshi S, Kira S, Segawa K, Uyama T, et al. Novel cardiac precursor-like cells from human menstrual blood-derived mesenchymal cells. Stem Cells. 2008;26(7):1695-704. doi: 10.1634/stemcells.2007-0826.
Santamaria X, Massasa EE, Feng Y, Wolff E, Taylor HS. Derivation of insulin producing cells from human endometrial stromal stem cells and use in the treatment of murine diabetes. Mol Ther. 2011;19:2065-71. doi: 10.1038/ mt.2011.173.
Shoae-Hassani A, Mortazavi-Tabatabaei SA, Sharif S, Seifalian AM, Azimi A, Samadikuchaksaraei A, et al. Differentiation of human endometrial stem cells into urothelial cells on a three-dimensional nanofibrous silk-collagen scaffold: an autologous cell resource for reconstruction of the urinary bladder wall: human endometrial stem cell differentiation into urothelial cells. J Tissue Eng Regen Med. 2015;9:1268-76. doi: 10.1002/term.1632.
Bayat N, Ebrahimi-Barough S, Ardakan MMM, Ai A, Kamyab A, Babaloo N, et al. Differentiation of human endometrial stem cells into Schwann cells in fibrin hydrogel as 3D culture. Mol Neurobiol. 2016;53:7170-6. doi: 10.1007/ s12035-015-9574-7.
Wolff EF, Gao XB, Yao KV, Andrews ZB, Du H, Elsworth JD, et al. Endometrial stem cell transplantation restores dopamine production in a Parkinson’s disease model. J Cell Mol Med. 2011;15(4):747-55. doi: 10.1111/j.1582-4934.2010.01068.x.
Fayazi M, Salehnia M, Ziaei S. Differentiation of human CD146-positive endometrial stem cells to adipogenic-, osteogenic-, neural progenitor-, and glial-like cells. In Vitro Cell Dev Biol Anim. 2015;51:408-14. doi: 10.1007/ s11626-014-9842-2.
Patel AN, Park E, Kuzman M, Benetti F, Silva FJ, Allickson JG. Multipotent menstrual blood stromal stem cells: isolation, characterization, and differentiation. Cell Transplant. 2008;17:303–11.
Wolff EF, Mutlu L, Massasa EE, Elsworth JD, Redmond Jr DE, Taylor HS. Endometrial stem cell transplantation in MPTP- exposed primates: an alternative cell source for treatment of Parkinson’s disease. J Cell Mol Med. 2014;19:249-56. doi: 10.1111/jcmm.12433.
Han X, Meng X, Yin Z, Rogers A, Zhong J, Rillema P, et al. Inhibition of intracranial glioma growth by endometrial regenerative cells. Cell Cycle. 2009;8:606-10. doi: 10.4161/cc.8.4.7731.
Ludke A, Wu J, Nazari M, Hatta K, Shao Z, Li S-H, et al. Uterine-derived progenitor cells are immunoprivileged and effectively improve cardiac regeneration when used for cell therapy. J Mol Cell Cardiol. 2015;84:116-28. doi: 10.1016/j. yjmcc.2015.04.019.
Huang ML, Tian H, Wu J, Matsubayashi K, Weisel RD, Li RK. Myometrial cells induce angiogenesis and salvage damaged myocardium. Am J Physiol Heart Circ Physiol. 2006;291:H2057-H66. doi: 10.1152/ajpheart.00494.2006.
Ito T, Meyer KC, Ito N, Paus R. Immune privilege and the skin. Curr Dir Autoimmun. 2008;10:27-52. doi: 10.1159/000131412.
Lai D, Wang F, Yao X, Zhang Q, Wu X, Xiang C. Human endometrial mesenchymal stem cells restore ovarian function through improving the renewal of germline stem cells in a mouse model of premature ovarian failure. J Transl Med. 2015;13:155. doi: 10.1186/s12967-015-0516-y.
Baiguera S, Jungebluth P, Mazzanti B, Macchiarini P. Mesenchymal stromal cells for tissue-engineered tissue and organ replacements: Tissue engineering and stem cells. Transpl Int. 2012;25:369-82. doi: 10.1111/j.1432-2277.2011.01426.x.
Gattegno-Ho D, Argyle S-A, Argyle DJ. Stem cells and veterinary medicine: tools to understand diseases and enable tissue regeneration and drug discovery. Vet J. 2012;191:19-27. doi: 10.1016/j.tvjl.2011.08.007.
Gonçalves N, Ambrósio C, Piedrahita J. Stem cells and regenerative medicine in domestic and companion animals: a multispecies perspective. Reprod Domest Anim. 2014;49:2-10. doi: 10.1111/rda.12392.
License
Veterinaria México OA by Facultad de Medicina Veterinaria y Zootecnia - Universidad Nacional Autónoma de México is licensed under a Creative Commons Attribution 4.0 International Licence.
Based on a work at http://www.revistas.unam.mx
- All articles in Veterinaria México OA re published under the Creative Commons Attribution 4.0 Unported (CC-BY 4.0). With this license, authors retain copyright but allow any user to share, copy, distribute, transmit, adapt and make commercial use of the work, without needing to provide additional permission as long as appropriate attribution is made to the original author or source.
- By using this license, all Veterinaria México OAarticles meet or exceed all funder and institutional requirements for being considered Open Access.
- Authors cannot use copyrighted material within their article unless that material has also been made available under a similarly liberal license.