Abstract
Fetal tissue-derived stem cells have been the subject of several studies. Among them, the yolk sac (YS) nourishes the embryo, synthesizes proteins and vitamins, and is the first hematopoietic site of the embryo. Stem cells derived from the YS can benefit several animal species as therapies aimed at tissue regeneration and immunological diseases. This review aims to describe the development, function, and possible dysfunctions of YS in different species, and consolidate the findings presented in the literature on the isolation, culture, and application of YS-derived stem cells from different mammals in regenerative medicine. Hematopoietic and mesenchymal stem cells have been previously investigated in the YS of different mammals; however, the culture media and isolation protocols differ between species. To date, no studies have been conducted using stem cells derived from the YS for cell therapy. Nevertheless, several domestic mammals have shown cellular markers characteristic of mesenchymal stem cells derived from the YS.
References
Abumaree, M. H., Abomaray, F. M., Alshabibi, M. A., AlAskar, A. S., & Kalionis, B. (2017). Immunomodulatory properties of human placental mesenchymal stem/stromal cells. Placenta, 59, 87-95. http://dx.doi.org/10.1016/j. placenta.2017.04.003. PMid:28411943.
Ambrósio, C. E., Orlandin, J. R., Oliveira, V. C., Motta, L., Pinto, P., Pereira, V. M., Padoveze, L. R., Karam, R. G., & Pinheiro, A. O. (2020). Potential application of aminiotic stem cells in veterinary medicine. Animal Reproduction, 16(1), 24-30. http://dx.doi.org/10.21451/1984-3143-AR2018-0124. PMid:33299475.
Bentin-Ley, U., Pedersen, B., Lindenberg, S., Larsen, J. F., Hamberger, L., & Horn, T. (1994). Isolation and culture of human endometrial cells in a three-dimensional culture system. Journal of Reproduction and Fertility, 101(2), 327-332. http://dx.doi.org/10.1530/jrf.0.1010327. PMid:7932366.
Bertassoli, B. M., Santos, A. C., Fratini, P., Will, S. E. A. L., Rodrigues, M. N., Chaves, A., & Assis Neto , A. C. (2015). Isolamento e caracterização de células-tronco do saco vitelino de suínos domésticos (Sus scrofa). Archives of Veterinary Science, 20(3), 1-10.
Bian, Z., Gong, Y., Huang, T., Lee, C., Bian, L., Bai, Z., Shi, H., Zeng, Y., Liu, C., He, J., Zhou, J., Li, X., Li, Z., Ni, Y., Ma, C., Cui, L., Zhang, R., Chan, J., Ng, L. G., Lan, Y., Ginhoux, F., & Liu, B. (2020). Deciphering human macrophage development at single-cell resolution. Nature, 582(7813), 571-576. http://dx.doi.org/10.1038/s41586-020-2316- 7. PMid:32499656.
Bobis, S., Jarocha, D., & Majka, M. (2006). Mesenchymal stem cells: characteristics and clinical applications. Folia Histochemica et Cytobiologica, 44(4), 215-230. PMid:17219716.
Borghesi, J., Ferreira Lima, M., Mario, L. C., de Almeida da Anunciação, A. R., Silveira Rabelo, A. C., Giancoli Kato Cano da Silva, M., Assunpção Fernandes, F., Miglino, M. A., Oliveira Carreira, A. C., & Oliveira Favaron, P. (2019). Canine amniotic membrane mesenchymal stromal/stem cells: isolation, characterization and differentiation. Tissue & Cell, 58, 99-106. http://dx.doi.org/10.1016/j.tice.2019.04.007. PMid:31133253.
Brent, R. L., & Fawcett, L. B. (1998). Nutritional studies of the embryo during early organogenesis with normal embryos and embryos exhibiting yolk sac dysfunction. The Journal of Pediatrics, 132(3 Pt 2), S6-S16. http:// dx.doi.org/10.1016/S0022-3476(98)70522-0. PMid:9546031.
Burton, G. J., Watson, A. L., Hempstock, J., Skepper, J. N., & Jauniaux, E. (2002). Uterine glands provide histiotrophic nutrition for the human fetus during the first trimester of pregnancy. The Journal of Clinical Endocrinology and Metabolism, 87(6), 2954-2959. http://dx.doi.org/10.1210/jcem.87.6.8563. PMid:12050279.
Carter, A. M., & Enders, A. C. (2016). Placentation in mammals: definitive placenta, yolk sac, and paraplacenta. Theriogenology, 86(1), 278-287. http://dx.doi.org/10.1016/j.theriogenology.2016.04.041. PMid:27155730.
Choi, K., Kennedy, M., Kazarov, A., Papadimitriou, J. C., & Keller, G. (1998). A common precursor for hematopoietic and endothelial cells. Development, 125(4), 725-732. http://dx.doi.org/10.1242/dev.125.4.725. PMid:9435292.
Cremonesi, F., Corradetti, B., & Lange Consiglio, A. (2011). Fetal adnexa derived stem cells from domestic animal: progress and perspectives. Theriogenology, 75(8), 1400-1415. http://dx.doi.org/10.1016/j.theriogenology.2010.12.032. PMid:21463720.
Crivelli, B., Chlapanidas, T., Perteghella, S., Lucarelli, E., Pascucci, L., Brini, A. T., Ferrero, I., Marazzi, M., Pessina, A., & Torre, M. L. (2017). Mesenchymal stem/stromal cell extracellular vesicles: From active principle to next generation drug delivery system. Journal of Controlled Release, 262, 104-117. http://dx.doi.org/10.1016/j. jconrel.2017.07.023.
Cumano, A., Furlonger, C., & Paige, C. J. (1993). Differentiation and characterization of B-cell precursors detected in the yolk sac and embryo body of embryos beginning at the 10- to 12-somite stage. Proceedings of the National Academy of Sciences of the United States of America, 90(14), 6429-6433. http://dx.doi.org/10.1073/ pnas.90.14.6429. PMid:8341650.
Dominici, M., Le Blanc, K., Mueller, I., Slaper-Cortenbach, I., Marini, F., Krause, D., Deans, R., Keating, A., Prockop, D., & Horwitz, E. (2006). Minimal criteria for defining multipotent mesenchymal stromal cells. Cytotherapy, 8(4), 315-317. http://dx.doi.org/10.1080/14653240600855905. PMid:16923606.
Dong, D., Reece, E. A., Lin, X., Wu, Y., AriasVillela, N., & Yang, P. (2016). New development of the yolk sac theory in diabetic embryopathy: Molecular mechanism and link to structural birth defects. American Journal of Obstetrics and Gynecology, 214(2), 192-202. http://dx.doi.org/10.1016/j.ajog.2015.09.082. PMid:26432466.
Dzierzak, E., & Robin, C. (2010). Placenta as a source of hematopoietic stem cells. Trends in Molecular Medicine, 16(8), 361-367. http://dx.doi.org/10.1016/j.molmed.2010.05.005. PMid:20580607.
Favaron, P. O., Mess, A., Will, S. E., Maiorka, P. C., Oliveira, M. F., & Miglino, M. A. (2014). Yolk sac mesenchymal progenitor cells from New World mice (Necromys lasiurus) with multipotent differential potential. PLoS One, 9(2), e95575. http://dx.doi.org/10.1371/journal.pone.0095575. PMid:24918429.
Filioli Uranio, M., Valentini, L., Lange-Consiglio, A., Caira, M., Guaricci, A. C., L’Abbate, A., Catacchio, C. R., Ventura, M., Cremonesi, F., & Dell’Aquila, M. E. (2011). Isolation, proliferation, cytogenetic, and molecular characterization and in vitro differentiation potency of canine stem cells from foetal adnexa: a comparative study of amniotic fluid, amnion, and umbilical cord matrix. Molecular Reproduction and Development, 78(5), 361-373. http:// dx.doi.org/10.1002/mrd.21311. PMid:21491540.
Franciolli, A. L. R., Barreto, R. S. N., Matias, G., Carvalho, R. C., Rodrigues, M. N., Fratini, P., Pignatari, G. C., Rechsteiner, S. M. E. F., Mess, A. M., & Miglino, M. A. (2020). Equine yolk sac: a stem cells source. International Journal of Morphology, 38(5), 1412-1420. http://dx.doi.org/10.4067/S0717-95022020000501412.
Fratini, P., Carreira, A. C., Alcântara, D., de Oliveira e Silva, F. M., Rodrigues, M. N., & Miglino, M. A. (2016). Endothelial differentiation of canine yolk sac cells transduced with VEGF. Research in Veterinary Science, 104, 71-76. http:// dx.doi.org/10.1016/j.rvsc.2015.11.010. PMid:26850540.
Freyer, C., & Renfree, M. B. (2009). The mammalian yolk sac placenta. Journal of Experimental Zoology. Part B, Molecular and Developmental Evolution, 312(6), 545-554. http://dx.doi.org/10.1002/jez.b.21239. PMid:18985616.
Galdos-Riveros, A., Rezende, L. C., Pessolato, A., Zogno, M. A., Rici, R. E. M., & Miglino, A., (2012). The structure of the bovine yolk sac: a study microscopic. In A. Méndez-Vilas (Ed.), Current microscopy contributions to advances in science and technology. Badajoz: Formatex.
Gasper, P. W. (2000). The hemopoietic system. In B. F. Feldman (Ed.), Schalm’s veterinary hematology (pp. 63-68). London: Lippincott Williams & Wilkins.
Giacomini, E., Vago, R., Sanchez, A. M., Podini, P., Zarovni, N., Murdica, V., Rizzo, R., Bortolotti, D., Candiani, M., & Viganò, P. (2017). Secretome of in vitro cultured human embryos contains extracellular vesicles that are uptaken by the maternal side. Scientific Reports, 7(1), 1-13. http://dx.doi.org/10.1038/s41598-017-05549-w. PMid:28701751.
Grotto, H. Z. W., & Noronha, J. F. A. (2003). Identificação de células tronco hematopoiéticas: Citometria de fluxo convencional versus contador hematológico automatizado. Revista Brasileira de Hematologia e Hemoterapia, 25(3), 169-172. http://dx.doi.org/10.1590/S1516-84842003000300008.
Guercio, A., Di Marco, P., Casella, S., Cannella, V., Russotto, L., Purpari, G., Di Bella, S., & Piccione, G. (2012). Production of canine mesenchymal stem cells from adipose tissue and their application in dogs with chronic osteoarthritis of the humeroradial joints. Cell Biology International, 36(2), 189-194. http://dx.doi.org/10.1042/ CBI20110304. PMid:21936851.
Gulbis, B., Jauniaux, E., Cotton, F., & Stordeur, P. (1998). Protein and enzyme patterns in the fluid cavities of the first trimester gestational sac: Relevance to the absorptive role of secondary yolk sac. Molecular Human Reproduction, 4(9), 857-862. http://dx.doi.org/10.1093/molehr/4.9.857. PMid:9783845.
Hafez, S. (2017). Comparative placental anatomy: Divergent structures serving a common purpose. Progress in Molecular Biology and Translational Science, 145, 1-28. http://dx.doi.org/10.1016/bs.pmbts.2016.12.001. PMid:28110748.
Herzog, E. L., Chai, L., & Krause, D. S. (2003). Plasticity of marrow-derived stem cells. Blood, 102(10), 3483-3493. http://dx.doi.org/10.1182/blood-2003-05-1664. PMid:12893756.
Huang, H., & Auerbach, R. (1993). Identification and characterization of hematopoietic stem cells from the yolk sac of the early mouse embryo. Proceedings of the National Academy of Sciences of the United States of America, 90(21), 10110-10114. http://dx.doi.org/10.1073/pnas.90.21.10110. PMid:8234265.
Hyttel, P., Sinowatz, F., Vejlsted, M., & Betteridge, K. (2009). Essentials of domestic animal embryology. Edinburgh: Elsevier Health Sciences.
Hyzewicz, J., Tanihata, J., Kuraoka, M., Nitahara-Kasahara, Y., Beylier, T., Ruegg, U. T., Vater, A., & Takeda, S. (2017). Low-Intensity Training and the C5a Complement Antagonist NOX-D21 Rescue the mdx Phenotype through Modulation of Inflammation. American Journal of Pathology, 187(5), 1147-1161. http://dx.doi.org/10.1016/j. ajpath.2016.12.019. PMid:28315675.
Jang, M. J., Kim, H.-S., Lee, H.-G., Kim, G. J., Jeon, H. G., Shin, H.-S., Chang, S.-K., Hur, G.-H., Chong, S. Y., Oh, D., & Chung, H.-M. (2013). Placenta-derived mesenchymal stem cells have an immunomodulatory effect that can control acute graft-versus-host disease in mice. Acta Haematologica, 129(4), 197-206. http://dx.doi. org/10.1159/000345267. PMid:23257958.
Jones, C. J., & Jauniaux, E. (1995). Ultrastructure of the materno-embryonic interface in the first trimester of pregnancy. Micron, 26(2), 145-173. http://dx.doi.org/10.1016/0968-4328(95)00002-L. PMid:7767634.
Kadam, S., Muthyala, S., Nair, P., & Bhonde, R. (2010). Human placenta-derived mesenchymal stem cells and islet-like cell clusters generated from these cells as a novel source for stem cell therapy in diabetes. The Review of Diabetic Studies, 7(2), 168-182. http://dx.doi.org/10.1900/RDS.2010.7.168. PMid:21060975.
Kim, S. K., Pak, H. N., Park, J. H., Fang, Y. F., Kim, G. I., Park, Y. D., Hwang, C., Kim, Y. H., & Kim, B. S. (2010). Cardiac cell therapy with mesenchymal stem cell induces cardiac nerve sprouting, angiogenesis, and reduced connexin43-positive gap junctions, but concomitant electrical pacing increases connexin43-positive gap junctions in canine heart. Cardiology in the Young, 20(3), 308-317. http://dx.doi.org/10.1017/S1047951110000132. PMid:20346202.
Kim, Y., Jo, S. H., Kim, W. H., & Kweon, O. K. (2015). Antioxidant and anti-inflammatory effects of intravenously injected adipose derived mesenchymal stem cells in dogs with acute spinal cord injury. Stem Cell Research & Therapy, 6(1), 229. http://dx.doi.org/10.1186/s13287-015-0236-5. PMid:26612085.
King, B. F., & Enders, A. C. (1970). Protein absorption and transport by the guinea pig visceral yolk sac placenta. The American Journal of Anatomy, 129(3), 261-287. http://dx.doi.org/10.1002/aja.1001290303. PMid:5476175.
Kolf, C. M., Cho, E., & Tuan, R. S. (2007). Mesenchymal stromal cells. Biology of adult mesenchymal stem cells: Regulation of niche, self-renewal and differentiation. Arthritis Research & Therapy, 9(1), 204. http://dx.doi. org/10.1186/ar2116. PMid:17316462.
Lee, J. M., Jung, J., Lee, H. J., Jeong, S. J., Cho, K. J., Hwang, S. G., & Kim, G. J. (2012). Comparison of immunomodulatory effects of placenta mesenchymal stem cells with bone marrow and adipose mesenchymal stem cells. International Immunopharmacology, 13(2), 219-224. http://dx.doi.org/10.1016/j.intimp.2012.03.024. PMid:22487126.
Lin, L., Yee, S. W., Kim, R. B., & Giacomini, K. M. (2015). SLC transporters as therapeutic targets: Emerging opportunities. Nature Reviews. Drug Discovery, 14(8), 543-560. http://dx.doi.org/10.1038/nrd4626. PMid:26111766.
Mançanares, C. A. F., Oliveira, V. C., Oliveira, L. J., Carvalho, A. F., Sampaio, R. V., Mançanares, A. C. F., Souza, A. F., Perecin, F., Meirelles, F. V., Miglino, M. A., & Ambrósio, C. E. (2015). Isolation and characterization of mesenchymal stem cells from the yolk sacs of bovine embryos. Theriogenology, 84(6), 887-898. http://dx.doi. org/10.1016/j.theriogenology.2015.05.031. PMid:26143361.
Mançanares, A., Oliveira, V. C., Oliveira, L. J., Miglino, M. A., Meirelles, F. V., & Ambrósio, C. E. (2019). Morphological and molecular analysis of in vitro tubular structures from bovine yolk sac-derived MSCs. Stem Cells International, 2019, 5073745. http://dx.doi.org/10.1155/2019/5073745.
McGrath, K. E., & Palis, J. (2005). Hematopoiesis in the yolk sac: More than meets the eye. Experimental Hematology, 33(9), 1021-1028. http://dx.doi.org/10.1016/j.exphem.2005.06.012. PMid:16140150.
Mess, A. M., Carreira, A. C. O., Marinovic de Oliveira, C., Fratini, P., Favaron, P. O., Barreto, R., Pfarrer, C., Meirelles, F. V., & Miglino, M. A. (2017). Vascularization and VEGF expression altered in bovine yolk sacs from IVF and NT technologies. Theriogenology, 87, 290-297. http://dx.doi.org/10.1016/j.theriogenology.2016.09.012. PMid:27729111.
Miao, Z., Jin, J., Chen, L., Zhu, J., Huang, W., Zhao, J., Qian, H., & Zhang, X. (2006). Isolation of mesenchymal stem cells from human placenta: Comparison with human bone marrow mesenchymal stem cells. Cell Biology International, 30(9), 681-687. http://dx.doi.org/10.1016/j.cellbi.2006.03.009. PMid:16870478.
Miglino, M. A., Ambrósio, C. E., Martins, D. DOS S., Wenceslau, C. V., Pfarrer, C., & Leiser, R. (2006). The carnivore pregnancy: The development of the embryo and fetal membranes. Theriogenology, 66(6-7), 1699-1702. http:// dx.doi.org/10.1016/j.theriogenology.2006.02.027. PMid:16563485.
Mikkola, H. K., & Orkin, S. H. (2006). The journey of developing hematopoietic stem cells. Development, 133(19), 3733-3744. http://dx.doi.org/10.1242/dev.02568. PMid:16968814.
Motta, L. C. B. (2019). Geração de organóides intestinais a partir de células-tronco derivadas do saco vitelino canino [Dissertação de mestrado]. Universidade de São Paulo. https://doi.org/10.11606/D.10.2020.tde-02122019-163753.
Moyle, L. A., Tedesco, F. S., & Benedetti, S. (2019). Pericytes in muscular dystrophies. Advances in Experimental Medicine and Biology, 1147, 319-344. http://dx.doi.org/10.1007/978-3-030-16908-4_15. PMid:31147885.
Myren, M., Mose, T., Mathiesen, L., & Knudsen, L. E. (2007). The human placenta: An alternative for studying foetal exposure. Toxicology In Vitro, 21(7), 1332-1340. http://dx.doi.org/10.1016/j.tiv.2007.05.011. PMid:17624715.
Oliveira, V. C., Mançanares, C. A., Oliveira, L. J., Gonçalves, N. J., Miglino, M. A., Perecin, F., Meirelles, F. V., Piedrahita, J., & Ambrósio, C. E. (2017). Characterization of putative haematopoietic cells from bovine yolk sac. Journal of Tissue Engineering and Regenerative Medicine, 11(4), 1132-1140. http://dx.doi.org/10.1002/term.2016. PMid:25712733.
Özen, I., Boix, J., & Paul, G. (2012). Perivascular mesenchymal stem cells in the adult human brain: A future target for neuroregeneration? Clinical and Translational Medicine, 1(1), 30. http://dx.doi.org/10.1186/2001-1326-1-30. PMid:23369339.
Palis, J., & Yoder, M. C. (2001). Yolk-sac hematopoiesis: The first blood cells of mouse and man. Experimental Hematology, 29(8), 927-936. http://dx.doi.org/10.1016/S0301-472X(01)00669-5. PMid:11495698.
Penha, E. M., Aguiar, P. H. P., Barrouin-Melo, S. M., Lima, R. S., Silveira, A. C. C., Otelo, A. R. S., Pinheiro, C. M. B., Ribeiro-dos-Santos, R., & Soares, M. B. P. (2012). Clinical neurofunctional rehabilitation of a cat with spinal cord injury after hemilaminectomy and autologous stem cell transplantation. International Journal of Stem Cells, 5(2), 146-150. http://dx.doi.org/10.15283/ijsc.2012.5.2.146. PMid:24298368.
Pessolato, A. G. T., Martins, D. S., Galdos-Riveros, A., Fontes, A. M., Ambrósio, C. E., Grassi, R. E., & Miglino, M. A. (2012). Microscopic aspects of the yolk sac hematopoiesis from ovine embryos. In A. Méndez-Vilas (Ed.), Current microscopy contributions to advances in science and technology. Badajoz: Formatex.
Pop, D. M., Soriţău, O., Şuşman, S., Rus-Ciucă, D., Groza, I. Ş., Ciortea, R., Mihu, D., & Mihu, C. M. (2015). Potential of placental-derived human mesenchymal stem cells for osteogenesis and neurogenesis. Romanian Journal of Morphology and Embryology, 56(3), 989-996. PMid:26662130.
Quimby, J. M., Webb, T. L., Randall, E., Marolf, A., Valdes-Martinez, A., & Dow, S. W. (2016). Assessment of intravenous adipose-derived allogeneic mesenchymal stem cells for the treatment of feline chronic kidney disease: A randomized, placebo-controlled clinical trial in eight cats. Journal of Feline Medicine and Surgery, 18(2), 165-171. http://dx.doi.org/10.1177/1098612X15576980. PMid:25784460.
Raeside, J. I., Christie, H. L., Renaud, R. L., Waelchli, R. O., & Betteridge, K. J. (2004). Estrogen metabolism in the equine conceptus and endometrium during early pregnancy in relation to estrogen concentrations in yolk-sac fluid. Biology of Reproduction, 71(4), 1120-1127. http://dx.doi.org/10.1095/biolreprod.104.028712. PMid:15163615.
Robb, L., Lyons, I., Li, R., Hartley, L., Köntgen, F., Harvey, R. P., Metcalf, D., & Begley, C. G. (1995). Absence of yolk sac hematopoiesis from mice with a targeted disruption of the scl gene. Proceedings of the National Academy of Sciences of the United States of America, 92(15), 7075-7079. http://dx.doi.org/10.1073/pnas.92.15.7075. PMid:7624372.
Rossi, M. I. D., & Bonfim, D. C. (2020). Mesenchymal stromal/stem cells: historical perspective and ongoing challenges. Revista Brasileira de Medicina Veterinária, 52(1), 1-16. http://dx.doi.org/10.29374/2527-2179.bjvm112020.
Saulnier, N., Loriau, J., Febre, M., Robert, C., Rakic, R., Bonte, T., Buff, S., & Maddens, S. (2016). Canine placenta: A promising potential source of highly proliferative and immunomodulatory mesenchymal stromal cells? Veterinary Immunology and Immunopathology, 171, 47-55. http://dx.doi.org/10.1016/j.vetimm.2016.02.005. PMid:26964717.
Seifert, J. (2014). Changes in mouse liver and chicken embryo yolk sac membrane soluble proteins due to an organophosphorous insecticide (OPI) diazinon linked to several noncholinergic OPI effects in mice and chicken embryos. Pesticide Biochemistry and Physiology, 116, 74-82. http://dx.doi.org/10.1016/j.pestbp.2014.09.016. PMid:25454523.
Shivdasani, R. A., Mayer, E. L., & Orkin, S. H. (1995). Absence of blood formation in mice lacking the T-cell leukaemia oncoprotein tal-1/SCL. Nature, 373(6513), 432-434. http://dx.doi.org/10.1038/373432a0. PMid:7830794.
Soncini, M., Vertua, E., Gibelli, L., Zorzi, F., Denegri, M., Albertini, A., Wengler, G. S., & Parolini, O. (2007). Isolation and characterization of mesenchymal cells from human fetal membranes. Journal of Tissue Engineering and Regenerative Medicine, 1(4), 296-305. http://dx.doi.org/10.1002/term.40. PMid:18038420.
Sousa, C., Biber, K., & Michelucci, A. (2017). Cellular and Molecular Characterization of Microglia: A Unique Immune Cell Population. Frontiers in Immunology, 8, 198. http://dx.doi.org/10.3389/fimmu.2017.00198. PMid:28303137.
Stremmel, C., Schuchert, R., Wagner, F., Thaler, R., Weinberger, T., Pick, R., Mass, E., Ishikawa-Ankerhold, H. C., Margraf, A., Hutter, S., Vagnozzi, R., Klapproth, S., Frampton, J., Yona, S., Scheiermann, C., Molkentin, J. D., Jeschke, U., Moser, M., Sperandio, M., Massberg, S., Geissmann, F., & Schulz, C. (2018). Yolk sac macrophage progenitors traffic to the embryo during defined stages of development. Nature Communications, 9(1), 1-14. http://dx.doi.org/10.1038/s41467-017-02492-2. PMid:29317637.
Thomas, T., Southwell, B. R., Schreiber, G., & Jaworowski, A. (1990). Plasma protein synthesis and secretion in the visceral yolk sac of the fetal rat: Gene expression, protein synthesis and secretion. Placenta, 11(5), 413-430. http://dx.doi.org/10.1016/S0143-4004(05)80216-4. PMid:1707170.
Tiedemann, K., & Minuth, W. W. (1980). The pig yolk sac I - Fine structure of the posthaematopoietic organ. Histochemistry, 68(2), 133-146. http://dx.doi.org/10.1007/BF00489509. PMid:7419438.
Trohatou, O., & Roubelakis, M. G. (2017). Mesenchymal stem/stromal cells in regenerative medicine: past, present, and future. Cellular Reprogramming, 19(4), 217-224. http://dx.doi.org/10.1089/cell.2016.0062. PMid:28520465.
Tyndall, A., & Uccelli, A. (2009). Multipotent mesenchymal stromal cells for autoimmune diseases: Teaching new dogs old tricks. Bone Marrow Transplantation, 43(11), 821-828. http://dx.doi.org/10.1038/bmt.2009.63. PMid:19308035.
Umezawa, A., Hasegawa, A., Inoue, M., Tanuma-Takahashi, A., Kajiwara, K., Makino, H., Chikazawa, E., & Okamoto, A. (2019). Amnion-derived cells as a reliable resource for next-generation regenerative medicine. Placenta, 84, 50-56. http://dx.doi.org/10.1016/j.placenta.2019.06.381. PMid:31272680.
Uranio, M. F., Valentini, L., Lange-Consiglio, A., Caira, M., Guaricci, A. C., L’Abbate, A., Catacchio, C. R., Ventura, M., Cremonesi, F., & Dell’Aquila, M. E. (2011). Isolation, proliferation, cytogenetic, and molecular characterization and in vitro differentiation potency of canine stem cells from foetal adnexa: A comparative study of amniotic fluid, amnion, and umbilical cord matrix. Molecular Reproduction and Development, 78(5), 361-373. http:// dx.doi.org/10.1002/mrd.21311. PMid:21491540.
Vanover, M., Wang, A., & Farmer, D. (2017). Potential clinical applications of placental stem cells for use in fetal therapy of birth defects. Placenta, 59, 107-112. http://dx.doi.org/10.1016/j.placenta.2017.05.010. PMid:28651900.
Vidane, A. S., Pinheiro, A. O., Casals, J. B., Passarelli, D., Hage, M. C. F. N. S., Bueno, R. S., Martins, D. S., & Ambrósio, C. E. (2017). Transplantation of amniotic membrane-derived multipotent cells ameliorates and delays the progression of chronic kidney disease in cats. Reproduction in Domestic Animals, 52(Suppl 2), 316-326. http:// dx.doi.org/10.1111/rda.12846. PMid:27774657.
Wang, X. Y., Lan, Y., He, W. Y., Zhang, L., Yao, H. Y., Hou, C. M., Tong, Y., Liu, Y. L., Yang, G., Liu, X. D., Yang, X., Liu, B., & Mao, N. (2008). Identification of mesenchymal stem cells in aorta-gonad-mesonephros and yolk sac of human embryos. Blood, 111(4), 2436-2443. http://dx.doi.org/10.1182/blood-2007-07-099333. PMid:18045971.
Weiskopf, K., Schnorr, P. J., Pang, W. W., Chao, M. P., Chhabra, A., Seita, J., Feng, M., & Weissman, I. L. (2016). Myeloid cell origins, differentiation, and clinical implications. Microbiology Spectrum, 4(5). PMid:27763252.
Weiss, M. L., Anderson, C., Medicetty, S., Seshareddy, K. B., Weiss, R. J., VanderWerff, I., Troyer, D., & McIntosh, K. R. (2008). Immune properties of human umbilical cord wharton’s jelly-derived cells. Stem Cells, 26(11), 2865-2874. http://dx.doi.org/10.1634/stemcells.2007-1028. PMid:18703664.
Wenceslau, C. V., Miglino, M. A., Martins, D. S., Ambrósio, C. E., Lizier, N. F., Pignatari, G. C., & Kerkis, I. (2011). Mesenchymal progenitor cells from canine fetal tissues: yolk sac, liver, and bone marrow. Tissue Engineering. Part A, 17(17-18), 2165-2176. http://dx.doi.org/10.1089/ten.tea.2010.0678. PMid:21529262.
Yamane, T. (2018). Mouse yolk sac hematopoiesis. Frontiers in Cell and Developmental Biology, 6, 80. http://dx.doi. org/10.3389/fcell.2018.00080. PMid:30079337.
Yamasaki, S., Nobuhisa, I., Ramadan, A., & Taga, T. (2011). Identification of a yolk sac cell population with hematopoietic activity in view of CD45/c-Kit expression. Development, Growth & Differentiation, 53(7), 870- 877. http://dx.doi.org/10.1111/j.1440-169X.2011.01293.x. PMid:21883169.
Young, P. E., Baumhueter, S., & Lasky, L. A. (1995). The sialomucin CD34 is expressed on hematopoietic cells and blood vessels during murine development. Blood, 85(1), 96-105. http://dx.doi.org/10.1182/blood.V85.1.96. bloodjournal85196. PMid:7528578.
Zambidis, E. T., Peault, B., Park, T. S., Bunz, F., & Civin, C. I. (2005). Hematopoietic differentiation of human embryonic stem cells progresses through sequential hematoendothelial, primitive, and definitive stages resembling human yolk sac development. Blood, 106(3), 860-870. http://dx.doi.org/10.1182/blood-2004-11- 4522. PMid:15831705.
Zohn, I. E., & Sarkar, A. A. (2010). The visceral yolk sac endoderm provides for absorption of nutrients to the embryo during neurulation. Birth Defects Research. Part A, Clinical and Molecular Teratology, 88(8), 593-600. http://dx.doi.org/10.1002/bdra.20705. PMid:20672346.
This work is licensed under a Creative Commons Attribution 4.0 International License.
Copyright (c) 2021 Priscilla Avelino Ferreira Pinto, Vitória Mattos Pereira, Lina Castelo Branco Motta, Matheus Ferreira de Almeida, Tiago Gonçalves dos Santos, Vanessa Cristina Oliveira, Luciana Cristina Machado, Carlos Eduardo Ambrósio