Animal Reproduction (AR)
Animal Reproduction (AR)
Conference papers

Potential application of aminiotic stem cells in veterinary medicine

Carlos Eduardo Ambrósio, Jéssica Rodrigues Orlandin, Vanessa Cristina Oliveira, Lina Castelo Branco Motta, Priscilla Avelino Ferreira Pinto, Vitória Mattos Pereira, Letícia Ribeiro Padoveze, Rafael Garcia Karam, Alessandra de Oliveira Pinheiro

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In regenerative medicine stem cell biology has become one of the most interesting and more often studied subject. The amniotic membrane is the innermost layer of the fetal membranes and is considered a potential tool to treat many pathologies. It is used because it can be collected from discarded fetal material and is a rich source of stem cells with high proliferation and plasticity ratio capable of proliferating and differentiate in vitro. We propose to elucidate the characteristics and potencial clinical application of cells derived of amniotic membrane in veterinary medicine.


amniotic membrane, stem cells, therapy.


Avila M, Espanha H, Moreno C, Pena C. 2001. Reconstruction of ocular surface with heterologous limbal epithelium and amniotic membrane in a rabbit model. Cornea, 20:414-420.

Barlow S, Brooke G, Chatterjee K, Price G, Pelekanos R, Rossetti T, Doody M, Venter D, Pain S, Gilshenan K, Atkinson K. 2008. Comparison of human placenta- and bone marrow–derived multipotent mesenchymal stem cells. Stem Cells Dev, 17:1095-1108.

Becker AJ, Mcculloch EA, Till JE. 1963. Cytological demonstration of the clonal nature of spleen colonies derived from transplanted mouse marrow cells. Nature, 197: 452-454.

Bossolasco P, Montemurro T, Cova L, Zangrossi S, Calzarossa C, Buiatiotis S, Soligo D, Soligo D, Bosari S, Silani V, Deliliers GL, Rebulla P, Lazzari L. 2006. Molecular and phenotypic characterization of human amniotic fluid cells and their differentiation potential. Cell Res, 16:329-336.

Cardoso M, Pinheiro AO, Vidane AS, Casals JB, de Oliveira VC, Gonçalves N, Martins DS, Ambrósio CE. 2016. Characterization of teratogenic potential and gene expression in canine and feline amniotic

membrane-derived stem cells. Reprod Domest Anim, 52:58-64.

Casteilla L, Benard VP, Laharrague P, Cousin B. 2011. Adipose-derived stromal cells: their identity and uses in clinical trials, an update. World J Stem Cells, 3:25-33.

Chang YJ, Hwang, SM, Tseng, CP, Cheng FC, Huang SH, Hsu LF, Hsu LW, Tsai M. 2010. Isolation of mesenchymal stem cells with neurogenic potential from the mesoderm of the amniotic membrane. Cells Tissues Organs, 192:93-105.

Corradetti B, Corradetti B, Correani A, Romaldini A, Marini MG, Bizzaro D, Perrini C, Cremonesi C, Lange-Consiglio A. 2014. Amniotic membrane-derived mesenchymal cells and their conditioned media: potential candidates for uterine regenerative therapy in the horse. Plos One. 9:1-9.

Cremonesi F, Corradetti B, Lange-Consiglio A. 2011. Fetal adnexa derived stem cells from domestic animal: progress and perspectives. Theriogenology, 75:1400-1415.

Dai R, Wang Z, Samanipour R, Koo K, Kim K. 2016. Adipose derived stem cells for tissue engineering and regenerative medicine applications. Stem Cells International, 2016:1-19.

Díaz-Prado S, Muinõs-López E, Hermida-Gómez T, Cicione C, Rendal-Vázquez E, Fuentes-Boquete I, De Toro FJ, Blanco FJ. 2011. Human amniotic membrane as an alternative source of stem cells for regenerative medicine. Differentiation, 81:162-171.

Dizaji Asl K, Shafaei H, Soleimani Rad J, Nozad Ho. 2017. Comparison of characteristics of human amniotic membrane and human adipose tissue derived mesenchymal stem cells. World J Plast Surg, 6:33-39.

Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini M, Krause D, Deans R, Keating A, Prockop DJ, Horwitz E. 2006. Minimal criteria for defining multipotent mesenchymal stromal cells. The international society for cellular therapy position statement. Cytotherapy, 8:315-317.

de Souza AF, Pieri NCG, Roballo KCS, Bressan FF, Casals JB, Ambrósio CE, Perecin F, Martins DS. 2018. Dynamics of male canine germ cell development. PLoS One. 28:13(2):e0193026.

Dua HS, Gomes JA, King AJ, Maharajan VS. 2004. The amniotic membrane in ophthalmology. Surv Ophthalmol, 49:51-77.

Faita T, Silva VN, Sattin WR, Pinheiro AO, Ambrósio CE. 2016. Amniotic membrane: an alternative source of mesenchymal stem cells in several animal species [in Portuguese]. Pesq Vet Bras, 3:520-525.

Favaron PO, Carvalho RC, Borghesi J, Anunciação ARA, Miglino MA. 2015. The amniotic membrane: development and potential applications – a review. Reprod Dom Anim, 50:881-892.

Fernandes RA, Wenceslau CV, Reginato AL, Kerkis I, Miglino MA. 2012. Derivation and characterization of progenitor stem cells from canine allantois and amniotic fluids at the third trimester of gestation. Placenta, 33:640-644.

Friedenstein AJ, Chailakhjan RK, Lalykina KS. 1970. The development of fibroblast colonies in monolayer cultures of guinea-pig bone marrow and spleen cells. Cell Tissue Kinet, 3:393-403.

Gomes JAP, Romano A, Santos MS, Dua HS. 2005. Amniotic membrane use in ophthalmology. Curr Opin Ophthalmol, 16:233-240.

Gonçalves NJN, Bressan FF, Roballo KCS, Meirelles FV, Xavier PLP, Fukumasu H, Williams C, Breen M, Koh S, Sper R, Piedrahita J, Ambrósio CE. 2017. Generation of LIF-independent induced pluripotent stem cells from canine fetal fibroblasts. Theriogenology, 92:75-82.

Gonçalves NN, Ambrósio CE, Piedrahita JA. 2014. Stem cells and regenerative medicine in domestic and companion animals: a multispecies perspective. Reprod Domest Anim, 49(Suppl 4):2-10.

Hortensius RA, Ebens JH, Arley BA. 2016. Immunomodulatory effects of amniotic membrane matrix incorporated into collagen scaffolds. J Biomed Mater Res 104:1332-1342.

Kakishita K, Nakao N, Sakuragawa N, Itakura T. 2003. Implantation of human amniotic epithelial cells prevents the degeneration of nigral dopamine neurons in rats with 6-hydroxydopamine lesions. Brain Res, 980:48-56.

Kamiya K, Wang M, Ichida S, Amano S, Oshika T, Sakuragawa N, Hori J. 2005. Topical application of culture supernatant from human amniotic epithelial cells suppresses inflammatory reactions in cornea. Exp Eye Res, 80:6771-6779.

Kastrinaki MC, Andreakou I, Charbord P, Papadaki HA. 2008. Isolation of human bone marrow mesenchymal stem cells using different membrane markers: comparison of colony cloning efficiency, differentiation potential, and molecular profile. Tissue Eng Part C Methods, 14:333-339.

Khanlarkhani N, Baazm M, Mohammadzadeh F, Najafi A, Mehdinejadiani S, Sobhani A. 2016. Multipotent stem cell and reproduction. J Stem Cells, 4:219-229.

Kim EY, Lee K-B, Kim MK. 2014. The potential of mesenchymal stem cells derived from amniotic membrane and amniotic fluid for neuronal regenerative therapy. BMB Rep, 47:135-140.

Kim HG, Choi OH. 2011. Neovascularization in a mouse model via stem cells derived from human fetal amniotic membranes. Heart Vessels, 26:196-205.

Kita K, Gauglitz GG, Phan TT, Herndon DN, Jeschke MG. 2010. Isolation and characterization of mesenchymal stem cells from the sub-amniotic human umbilical cord lining membrane. Stem Cells and Dev, 19:491-502.

Klein D. 2016. Vascular wall-resident multipotent stem cells of mesenchymal nature within the process of vascular remodeling: cellular basis, clinical relevance, and implication for stem cell therapy. Stem cell int, doi: 10.1155/2016/1905846.

Kogan S, Sood A, Granick MS. 2018. Amniotic membrane adjuncts and clinical applications in wound healing: a review of the literature. Wounds, 30:168-173.

Koob TJ, Lim JJ, Massee M, Zabek N, Denozière G. 2014. Properties of dehydrated human amnion/chorion

composite grafts: implications for wound repair and soft tissue regeneration. J Biomed Mater Res B Appl Biomater, 102:1353-62.

Kumar D, Talluri TR, Anand T, Kues WA. 2015. Induced pluripotent stem cells: Mechanisms, achievements and perspectives in farm animals. World J Stem Cells, 7:315-328.

Lange‐Consiglio, Corradetti B, Meucci A, Perego R, Bizzaro D, Cremonesi F. 2013a. Characteristics of equine mesenchymal stem cells derived from amnion and bone marrow: in vitro proliferative and multilineage potential assessment. Equine Vet J, 45:737-744.


Lange-Consiglio, Tassan S, Corradetti B, Meucci A, Perego R, Bizzaro D, Cremonesi F. 2013b. Investigating the efficacy of amnion-derived compared with bone marrow–derived mesenchymal stromal cells in equine tendon and ligament injuries. Cytotherapy, 15:1011-1020.

Lange-Consiglio, Corradetti B, Bertani S, Notarstefano V, Perrini C, Marini MG, Arrighi S, Bosi G, Belloli A, Pravettoni D, Locatelli V, Cremonesi F, Bizzaro D. 2015. Peculiarity of porcine amniotic membrane and its derived cells: a contribution to the study of cell therapy from a large animal model. Cloning Stem Cells, 17:472-483.

Largeault AF. 2004. Embryos, stem cells and cell therapies: philosophical and anthropological issues [in Portuguese]. Estud Av, 18:227-245.

Leiser R, Kaufmann P. 1994. Placetal structure: in a comparative aspect. Exp Clin Endocrinol, 102:122-34.

Liao SY, Tse HF. 2013. Multipotent (adult) and pluripotent stem cells for heart regeneration: what are the pros and cons? Stem Cell Res Ther, 4:151-162.

Magatti M, Vertua, E, Munari S, Aro M, Caruso M, Silini A, Delgado M, Parolini O. 2016. Human amnion favours tissue repair by inducing the m1-to-m2 switch and enhancing m2 macrophage features. J Tissue Eng Regen Med, 11:2895-2911.

Malak TM, Bell SC. 1994. Differential expression of the integrin subunits in human fetal membranes. J Reprod Fertil Abbreviation, 102:269-276.

Mamede AC, Carvalho MJ, Abrantes AM, Laranjo M, Maia CJ, Botelho MF. 2012. Amniotic membrane: from structure and functions to clinical applications. Cell and Tissue Res, 349:447-58.

Mançanares CAF, Oliveira VC, Oliveira LJ, Carvalho AF, Sampaio RV, Mançanares AC, Souza AF, Perecin F, Meirelles FV, Miglino MA, Ambrosio CE. 2015. Isolation and characterization of mesenchymal stem cells from the yolk sacs of bovine embryos. Theriogenology, 84:887-898.

Martins DS, Ambrósio CE, Saraiva NZ, Wenceslau CV, Morini AC, Kerkis I, Garcia JM, Miglino MA. 2011. Early development and putative primordial germ cells characterization in dogs. Reprod Domest Anim. 46(1):e62-6.

Martins GR, Marinho RC, Bezerra-Junior RQ, Câmara LMC, Albuquerque-Pinto LC, Teixeira MFS. 2017. Isolation, culture and characterization of multipotent mesenchymal stem cells from goat umbilical cord blood. Pesq Vet Bras, 37:643-649.

Meng XT, Li C, Dong ZY, Liu JM, Li W, Liu Y, Xue H, Chen D. 2008. Co-transplantation of bfgf-expressing amniotic epithelial cells and neural stem cells promotes functional recovery in spinal cord-injured rats. Cell Bio Int, 32:1546-1558.

Miglino MA, Ambrósio CE, Martins DS, Wenceslau CV, Pfarrer C, Leiser R. 2006. The carnivore pregnancy: the development of the embryo and fetal membranes. Theriogenology, 66:1699-1702.

Miki T. 2016. A rational strategy for the use of amniotic epithelial stem cell therapy for liver diseases. Stem Cells Transl Med, 5:405-409.

Mirzaei H, Sahebkar A, Sichani LS, Moridikia A, Nazari S, Nahand JS, Salehi H, Stenvang J, Masoudifar A, Mizaei HR, Jaafari MR. 2018. Therapeutic application of multipotent stem cells. J Cell Physiol, 233(4):2815-2823.

Moore KL, Persaud TVN. 2008. Placenta and fetal membranes [in Portuguese]. 8.ed. Rio de Janeiro: Elsevier. p.41.

Morgani SM, Canham MA, Nichols J, Sharov AA, Migueles RP, Ko MSH, Brickman JM. 2013. Totipotent embryonic stem cells arise in ground-state culture conditions. Cell Rep, 6:1954-1957.

Mossman HW. 1987. Vertebrate fetal membranes: comparative ontogeny and morphology, evolution, phylogenetic significance, basic functions, research opportunities. 1.ed. London: Rutgers University Press, p.383.

Nardi BN, Meirelles LS. 2006. Mesenchymal stem cells: isolation, in vitro expansion and characterization. Handb Exp Pharmacol, 174:249-82.

Oliveira VC, Souza AF, Cury FS, Perecin F, Martins DS, Ambrósio CE. 2014. Stem cells derived from bone marrow and preclinical trials in veterinary medicine. Rev Bras Ci Vet, 21:143-149.

Parolini O, Alviano F, Bagnara GP, Bilic G, Buhring HJ, Evangelista M, Hennerbichler S, Liu B, Magatti M, Mao N, Miki T, Marongiu F, Nakajima H, Nikaido T, Portmann-Lanz CB, Sankar V, Soncini M, Atadler G, Surbek D, Takahashi TA, Redl H, Sakuragawa N, Wolbank S, Zeisberger S, Zisch A, Strom SC. 2008. Concise review: isolation and characterization of stem cells from human term placenta: outcome of the first international workshop on placenta derived stem cells. Stem Cells, 2:300-311.

Park D, Lim J, Park JY, Lee SH. 2015. Concise review: stem cell microenvironment on a chip: current technologies for tissue engineering and stem cell biology. Stem Cells Trans Med, 11:1352-1368.

Park SB, Seo SM, Kim SK, Kang SK. 2012. Isolation and characterization of canine amniotic membrane-derived multipotent stem cells. Plos One, 7(9):e44693.

Perin L, Giuliani S, Jin D, Sedrakyan S, Carraro G, Habibian R, Warburton D, Atala A, De Filippo RE. 2007. Renal differentiation of amniotic fluid stem cells. Cell Proliferation, 40:936-948.

Pieri N, Souza AF, Casals JB, Roballo K, Ambrósio CE, Martins DS. 2015. Comparative Development of Embryonic Age by Organogenesis in Domestic Dogs and Cats. Reprod Domest Anim. 50(4):625-631.

Rada T, Reis RL, Gomes ME. 2011. Distinct stem cells subpopulations isolated from human adipose tissue

exhibit different chondrogenic and osteogenic differentiation potential. Stem Cell Rev and Rep, 7:64-76.

Ratajczak MZ, Marycz K, Poniewierska-Baran A, Fiedorowicz K, Zbucka-Kretowska M, Moniuszko M. 2014. Very small embryonic-like stem cells as a novel development concept and the hierarchy of the stem cell compartment. Adv Med Sci, 59:273-280.

Reich CM, Raabe O, Wenisch S, Bridger PS, Kramer M, Arnhold S. 2012. Isolation culture and chondrogenic differentiation of canine adipose tissue and bone marrow derived mesenchymal stem cells – a comparative study. Vet Res Commun, 31:139-148.

Samsoraj RM, Raghunath M, Nucombe V, Hui JH, van Wijnen AJ, Cool SM. 2017. Concise review: multifaceted characterization of human mesenchymal stem cells for use in regenerative medicine. Stem Cells Transl Med, 6:2173-2185.

Sankar V, Muthusamy R. 2003. Letter to neuroscience role of human amniotic epithelial cell transplantation in spinal cord injury repair research. Neuroscience, 118:11-17.

Saulnier N, Loriaua J, Febrea 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? Vet Immunol Immunopathol, 171:47-55.

Seo MS, Jeong YH, Park JR, Parksb, Rho KH, Kim HS, Yu KR, Lee SH, Jung KW, Lee YS, Kang KS. 2009. Isolation and characterization of canine umbilical cord blood-derived mesenchymal stem cells. J Vet Sci, 10:181-187.

Slack JMW. 2018. What is a stem cell? Wires Wev Biol, 7:1-15.

Sobhani A, Khanlarkhani N, Baazm M, Mohammadzadeh F, Najafi A, Mehdinejadiani S, Aval FS. 2017. Multipotent stem cell and current application. Acta Medica Iranica, 55:6-23.

Steigman SA, Fauza DO. 2007. Isolation of mesenchymal stem cells from amniotic fluid and placenta. Curr Protoc Stem Cell Biol, Chapter 1:Unit 1E.2. doi: 10.1002/9780470151808.sc01e02s1.

Takahashi K, Yamanaka S. 2006. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell, 126:663-76.

Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S. 2007. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell, 131:861-872

Tao J, Ji F, Liu B, Wang F, Dong F, Zhu Y. 2012. Improvement of deficits by transplantation of lentiviral vector-modified human amniotic mesenchymal cells after cerebral ischemia in rats. Brain Res, 1448:1-10.

Tharasanit T, Phuticanit N, Wangdee C, Soontornvipart K, Tantrajak S, Kaewamatawong T, Suwimonteerabutr J, upaphol P, Techakumphu M. 2011. Differentiation potentials of canine bone marrow mesenchymal stem cells. J Vet Med, 41:79-86.

Uranio FM, Valentini L, Lange-Consiglio A, Caira M, Guaricci AC, Labbate A, Catachio CR, Ventura M, Cremonesi F, Dellaquila ME. 2011. Isolation, proliferation, cytogenetic and molecular characterization and in vritro differentiation potency of canine stem cells from foetal adnexa: a comparative study of amniotic fluid, amnion, and umbilical cord matrix. Mol Reprod Dev, 78:361-373.

Vidane AS, Pinheiro AO, Casals JB, Passarelli D, Hage M, Bueno RS, Martins DS, Ambrosio CE. 2017. Transplantation of amniotic membrane-derived multipotent cells ameliorates and delays the progression of chronic kidney disease in cats. Reprod Domest Anim, 52:316-326.

Vidane AS, Souza AF, Sampaio RV, Bressan FF, Pieri NC, Martins DS, Meirelles FV, Miglino MA, Ambrósio CE. 2014. Cat amniotic membrane cells are non tumorigenic and safe for use in cell transplantation. Stem Cells Cloning, 7:71-78.

Villaron EM, Almeida J, López-Holgado N, Alcoceba M, Sánchez-Abarca LI, Sanchez-Guijo FM, Alberca M, Pérez-Simon JA, San Miguel JF, Del Cañizo MC. 2004. Mesenchymal stem cells are present in peripheral blood and can engraft after allogeneic hematopoietic stem cell transplantation. Haematologica, 89:1421-1427.

Violini S, Gorni C, Pisani LF, Ramelli P, Caniatti M, Mariani P. 2012. Isolation and differentiation potential of an equine amnion-derived stromal cell line. Cytotechnology, 64:1-7.

Vita BD, Campos LL, Listoni, AJ, Maia L, Freitas NPPF, Lvarenga FL, Prestes NC. 2012. Fetal attachments: an alternative source of mesenchymal ct for equine veterinary medicine [in Portuguese]. Veterinária e Zootecnia, 19:8-22.

Ward DJ, Bennett JP. 1984. The long-term results of the use of human amnion in the treatment of leg ulcers. Br J Plast Surg, 37:191-193.

Wenceslau CV, Miglino MA, Martins DS, Ambrósio CE, Lizier NF, Pignatari GC, Kerkis I. 2011. Mesenchymal progenitor cells canine fetal tissues: yolk sac, liver and boné marrow. Tissue Engineer, 17:2165-2176.

Yang XX, Xue SR, Dong WL, Kong Y. 2009. Therapeutic effect of human amniotic epithelial cell transplantation into the lateral ventricle of hemiparkinsonian rats. Chin Med J, 122:2449-2454.

You Q, Cai L, Zheng J, Tong X, Zhang D, Zhang Y. 2008.Isolation of human mesenchymal stem cells from third-trimester amniotic fluid. Int J Gynaecol Obstet, 103:149-152.

Zhang S, Guo Y, Cui Y, Liu Y, Yu T, Wang H. 2015. Generation of intermediate porcine iPS cells under culture condition favorable for mesenchymal-to-epithelial transition. Stem Cell Rev, 11:24-38.

Zhi-Yuan W, Guo-Zhen H, Yi L, Xin W, Li-He G. 2006. Transplantation of human amniotic epithelial cells improves hindlimb function in rats with spinal cord injury. Chin Med J, 119:2101-2107.

Zuk PA, Zhu M, Ashjian P, De Ugarte DA, Huang JI, Mizuno H, Alfonso ZC, Fraser, Benhaim P, Hedrick MH. 2002. Human adipose tissue is a source of multipotent stem cells. Mol Bio Cell, 13:4279-4295.

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