Animal Reproduction (AR)
https://www.animal-reproduction.org/article/doi/10.1590/1984-3143-AR2020-0040
Animal Reproduction (AR)
Original Article

Pluripotent stem cells proliferation is associated with placentation in dogs

Juliana Barbosa Casals; Naira Caroline Godoy Pieri; Kelly Cristine Santos Roballo; Fabiana Fernandes Bressan; Phelipe Oliveira Favaron; Daniele dos Santos Martins; Carlos Eduardo Ambrósio

Downloads: 0
Views: 574

Abstract

Abstract: Pluripotent stem cells have been studied as source of cells for regenerative medicine and acquire or genetic diseases, as an innovative therapy. Most tissues have stem cells populations, however in few quantities or impossible to be used during adult life, which lead to scientists look for new sources. Thus, this study aimed to analyze the presence of pluripotent cells in the uterus and placenta, following up non-pregnant, pregnant (begin, middle, and final), and postpartum periods in dogs. The uteri were obtained from social castration programs for population control in Pirassununga, Sao Paulo, Brazil. It was collected 20 uteri at different stages. The samples were fixed and processed for immunohistochemical analysis of NANOG, OCT4 and SOX2 expression, knowing as pluripotent stem cells makers. Our results showed positive expression for NANOG, OCT4 and SOX2 in all stages of gestation and nonpregnant uterus; however, we highlight some quantitative different between stages. OCT4 showed more expression in non-pregnant uterus than NANOG and SOX2, and its expression increased in pregnant uterus. In pregnant uterus there was more expression of NANOG than OCT4 and SOX2. Interesting, no difference was found between these markers in the other periods. In conclusion, it was possible to identify pluripotent stem cells in all periods in dog placenta and uterus, however during the early stage of pregnancy we observed more pluripotent stem cells than in all the others periods confirming the high plasticity and regeneration capacity of the uterine tissue.

Keywords

stem cells, placenta, gestation, carnivores

References

Adachi K, Suemori H, Yasuda SY, Nakatsuji N, Kawase E. Role of SOX2 in maintaining pluripotency of human embryonic stem cells. Genes Cells. 2010;15(5):455-70. http://dx.doi.org/10.1111/j.1365-2443.2010.01400.x. PMid:20384793.

Antoniadou E, David A. Placental stem cells. Best Pract Res Clin Obstet Gynaecol. 2016;31:13-29. http://dx.doi.org/10.1016/j.bpobgyn.2015.08.014. PMid:26547389.

Borghesi J, Lima MF, Mario LC, Anunciação ARA, Rabelo ACS, Silva MGKC, Fernandes FA, Miglino MA, Carreira ACO, Favaron PO. Canine amniotic membrane mesenchymal stromal/stem cells: Isolation, characterization and differentiation. Tissue Cell. 2019;58:99-106. http://dx.doi.org/10.1016/j.tice.2019.04.007. PMid:31133253.

Brólio MP, Vidane AS, Zomer HD, Wenceslau CV, Ozório JJ, Martins DS, Miglino MA, Ambrósio CE. Morphological characterization of the progenitor blood cells in canine and feline umbilical cord. Microsc Res Tech. 2012;75(6):766-70. http://dx.doi.org/10.1002/jemt.21123. PMid:22131289.

Chan RW, Gargett CE. Identification of label-retaining cells in mouse endometrium. Stem Cells. 2006;24(6):1529-38. http://dx.doi.org/10.1634/stemcells.2005-0411. PMid:16456137.

Chang YJ, Hwang SM, Tseng CP, Cheng FC, Huang SH, Hsu LF, Hsu LW, Tsai MS. Isolation of mesenchymal stem cells with neurogenic potential from the mesoderm of the amniotic membrane. Cells Tissues Organs. 2010;192(2):93-105. http://dx.doi.org/10.1159/000295774. PMid:20215735.

Dyce KM, Sack WO, Wensing CJG. Textbook of veterinary anatomy. 3rd ed. London: Saunder; 2010.

Enders AC, Carter AM. The evolving placenta: convergent evolution of variations in the endotheliochorial relationship. Placenta. 2012;33(5):319-26. http://dx.doi.org/10.1016/j.placenta.2012.02.008. PMid:22364740.

Evans H, Sack WO. Prenatal development of domestic and laboratory mammals: growth curves, external features and selected references. Zentralbl Veterinar Med. 1973;2(1):11-45. http://dx.doi.org/10.1111/j.1439-0264.1973.tb00253.x. PMid:4745140.

Figueira PGM, Abrão MS, Krikun G, Taylor H. Stem cells in endometrium and their role in the pathogenesis of endometriosis. Ann N Y Acad Sci. 2011;1221(1):10-7. http://dx.doi.org/10.1111/j.1749-6632.2011.05969.x. PMid:21401624.

Furukawa S, Kuroda Y, Sugiyama A. A comparison of the histological structure of the placenta in experimental animals. J Toxicol Pathol. 2014;27(1):11-8. http://dx.doi.org/10.1293/tox.2013-0060. PMid:24791062.

Gargett CE, Nguyen HP, Ye L. Endometrial regeneration and endometrial stem/progenitor cells. Rev Endocr Metab Disord. 2012;13(4):235-51. http://dx.doi.org/10.1007/s11154-012-9221-9. PMid:22847235.

Gonçalves NJ, Bressan FF, Souza A, Martins DS, Miglino MA, Meirelles FV, Perecin F, Ambrósio CE. Canine fibroblasts expressing human transcription factors: what is in the route for the production of canine induced pluripotent stem cells. Reprod Domest Anim. 2012;47(Suppl 6):84-7. http://dx.doi.org/10.1111/rda.12002. PMid:23279472.

Gonçalves NN, Ambrósio CE, Piedrahita JA. Stem cells and regenerative medicine in domestic and companion animals: a multispecies perspective. Reprod Domest Anim. 2014;49(Suppl 4):2-10. http://dx.doi.org/10.1111/rda.12392. PMid:25277427.

Hyttel P, Sinowatz F, Vejlsted M, Betteridge K. Essentials of domestic animal embryology. 1st ed. London: Saunders; 2010.

Izumi M, Pazin BJ, Minervini CF, Gerlach J, Ross MA, Stolz DB, Turner ME, Thompson RL, Miki T. Quantitative comparison of stem cell marker-positive cells in fetal and term human amnion. J Reprod Immunol. 2009;81(1):39-43. http://dx.doi.org/10.1016/j.jri.2009.02.007. PMid:19501410.

Janzen DM, Cheng D, Schafenacker AM, Paik DY, Goldstein AS, Witte ON, Jaroszewicz A, Pellegrini M, Memarzadeh S. Estrogen and progesterone together expand murine endometrial epithelial progenitor cells. Stem Cells. 2013;31(4):808-22. http://dx.doi.org/10.1002/stem.1337. PMid:23341289.

Kuijk EW, Lopes SMCS, Geijsen N, Macklon N, Roelen BA. The different shades of mammalian pluripotent stem cells. Hum Reprod Update. 2011;17(2):254-71. http://dx.doi.org/10.1093/humupd/dmq035. PMid:20705693.

Lee J, Kim HK, Rho JY, Han YM, Kim J. The human oct-4 isoforms differ in their ability to confer self-renewal. J Biol Chem. 2006;281(44):33554-65. http://dx.doi.org/10.1074/jbc.M603937200. PMid:16951404.

Levi B, Morrison S. Stem cells use distinct self-renewal programs at different ages. Cold Spring Harb Symp Quant Biol. 2008;73(0):539-53. http://dx.doi.org/10.1101/sqb.2008.73.049. PMid:19150957.

Łupicka M, Bodek G, Shpigel N, Elnekave E, Korzekwa A. Identification of pluripotent cells in bovine uterus: in situ and in vitro studies. Reproduction. 2015;149(4):371. http://dx.doi.org/10.1530/REP-14-0348. PMid:25556182.

Matthai C, Horvat R, Noe M, Nagele F, Radjabi A, Van Trotsenburg M, Huber J, Kolbus A. Oct-4 expression in human endometrium. Mol Hum Reprod. 2006;12(1):7-10. http://dx.doi.org/10.1093/molehr/gah254. PMid:16421218.

Miglino MA, Ambrósio CE, Martins DS, Wenceslau CV, Pfarrer C, Leiser R. The Carnivore pregnancy: the development of the embryo and fetal membranes. Theriogenology. 2006;66(6-7):1699-702. http://dx.doi.org/10.1016/j.theriogenology.2006.02.027. PMid:16563485.

Niwa H, Sekita Y, Tsend-Ayush E, Grutzner F. Platypus Pou5f1 reveals the first steps in the evolution of trophectoderm differentiation and pluripotency in mammals. Evol Dev. 2008;10(6):671-82. http://dx.doi.org/10.1111/j.1525-142X.2008.00280.x. PMid:19021737.

Ono M, Kajitani T, Uchida H, Arase T, Oda H, Nishikawa-Uchida S, Masuda H, Nagashima T, Yoshimura Y, Maruyama T. Oct4 expression in human uterine myometrial stem/progenitor cells. Hum Reprod. 2010;25(8):2059-67. http://dx.doi.org/10.1093/humrep/deq163. PMid:20576635.

Pelosi E, Forabosco A, Schlessinger D. Germ Cell Formation from embryonic stem cell and the use somatic cell nuclei in oocytes. Ann N Y Acad Sci. 2011;1221(1):18-26. http://dx.doi.org/10.1111/j.1749-6632.2011.05982.x. PMid:21401625.

Pieri N, Souza AF, Casals JB, Roballo K, Ambrósio CE, Martins DS. Comparative development of embryonic age by organogenesis in domestic dogs and cats. Reprod Domest Anim. 2015;50(4):625-31. http://dx.doi.org/10.1111/rda.12539. PMid:25990819.

Portmann-Lanz CB, Schoeberlein A, Huber A, Sager R, Malek A, Holzgreve W, Surbek DV. Placental mesenchymal stem cells as potential autologous graft for pre- and perinatal neuroregeneration. Am J Obstet Gynecol. 2006;194(3):664-73. http://dx.doi.org/10.1016/j.ajog.2006.01.101. PMid:16522395.

Puscheck EE, Awonuga AO, Yang Y, Jiang Z, Rappolee DA. Molecular biology of the stress response in the early embryo and its stem cells. Adv Exp Med Biol. 2015;843:77-128. http://dx.doi.org/10.1007/978-1-4939-2480-6_4. PMid:25956296.

Reece WO, Erickson HH, Jesse PG, Etsuro EU. Dukes’ physiology of domestic animals. 13th ed. Ames: Wiley-Blackwell; 2013.

Roballo KC, Ercolin AC, Casals JB, Pieri NC, Barreto RS, Illera MJ, Martins DS, Miglino MA, Ambrósio CE. Domestic carnivore’s development: detection of Oct-4, a pluripotency marker, in pharyngeal arches. Reprod Domest Anim. 2013;48(3):e41-3. http://dx.doi.org/10.1111/rda.12147. PMid:23379423.

Verfaillie CM, Pera MF, Lansdorp PM. Stem cells: hype and reality. Hematology Am Soc Hematol Educ Program. 2002;1(1):369-91. http://dx.doi.org/10.1182/asheducation-2002.1.369. PMid:12446433.

Vidane AS, Souza AF, Sampaio RV, Bressan FF, Pieri NC, Martins DS, Meirelles FV, Miglino MA, Ambrósio CE. Cat amniotic membrane multipotent cells are nontumorigenic and are safe for use in cell transplantation. Stem Cells Cloning. 2014;7:71-8. http://dx.doi.org/10.2147/SCCAA.S67790. PMid:25249758.

Vidane AS, Zomer HD, Oliveira BM, Guimarães CF, Fernandes CB, Perecin F, Silva LA, Miglino MA, Meirelles FV, Ambrósio CE. Reproductive stem cell differentiation: extracellular matrix, tissue microenvironment, and growth factors direct the mesenchymal stem cell lineage commitment. Reprod Sci. 2013;20(10):1137-43. http://dx.doi.org/10.1177/1933719113477484. PMid:23420825.

Wang L, Duan E, Sung L, Jeong BS, Yang X, Tian XC. Generation and characterization of pluripotent stem cells from cloned bovine embryos. Biol Reprod. 2005;73(1):149-55. http://dx.doi.org/10.1095/biolreprod.104.037150. PMid:15744021.

Wenceslau CV, Miglino MA, Martins DS, Ambrósio CE, Lizier NF, Pignatari GC, Kerkis I. Mesenchymal progenitor cells from canine fetal tissues: yolk sac, liver, and bone marrow. Tissue Eng Part A. 2011;17(17-18):2165-76. http://dx.doi.org/10.1089/ten.tea.2010.0678. PMid:21529262.

Xu J, Hu FF, Cui YG, Luo J, Jiang C, Gao L, Qian XQ, Mao YD, Liu JY. Effect of estradiol on proliferation and differentiation of side population stem/progenitor cells from murine endometrium. Reprod Biol Endocrinol. 2011;9(1):103-9. http://dx.doi.org/10.1186/1477-7827-9-103. PMid:21801373.

Yamauchi Y, Nita A, Nishiyama M, Muto Y, Shimizu H, Nakatsumi H, Nakayama KI. Skp2 contributes to cell cycle progression in trophoblast stem cells and to placental development. Genes Cells. 2020;25(6):427-38. http://dx.doi.org/10.1111/gtc.12769.

Yen BL, Huang HI, Chien CC, Jui HY, Ko BS, Yao M, Shun CT, Yen ML, Lee MC, Chen YC. Isolation of multipotent cells from human term placenta. Stem Cells. 2005;23(1):3-9. http://dx.doi.org/10.1634/stemcells.2004-0098. PMid:15625118.

Zucconi E, Vieira NM, Bueno DF, Secco M, Jazedje T, Ambrosio CE, Passos-Bueno MR, Miglino MA, Zatz M. Mesenchymal stem cells derived from canine umbilical cord vein: a novel source for cell therapy studies. Stem Cells Dev. 2010;19(3):395-402. http://dx.doi.org/10.1089/scd.2008.0314. PMid:19290805.
 


Submitted date:
04/17/2020

Accepted date:
07/06/2020

5f36dffe0e88259754587299 animreprod Articles
Links & Downloads

Anim Reprod

Share this page
Page Sections