Identification and characterization of Xenopus tropicalis common progenitors of Sertoli and peritubular myoid cell lineages
Status PubMed-not-MEDLINE Jazyk angličtina Země Velká Británie, Anglie Médium electronic
Typ dokumentu časopisecké články
PubMed
27464670
PubMed Central
PMC5051652
DOI
10.1242/bio.019265
PII: bio.019265
Knihovny.cz E-zdroje
- Klíčová slova
- Common progenitor, Migration potential, Testicular somatic cells, Xenopus tropicalis,
- Publikační typ
- časopisecké články MeSH
The origin of somatic cell lineages during testicular development is controversial in mammals. Employing basal amphibian tetrapod Xenopus tropicalis we established a cell culture derived from testes of juvenile male. Expression analysis showed transcription of some pluripotency genes and Sertoli cell, peritubular myoid cell and mesenchymal cell markers. Transcription of germline-specific genes was downregulated. Immunocytochemistry revealed that a majority of cells express vimentin and co-express Sox9 and smooth muscle α-actin (Sma), indicating the existence of a common progenitor of Sertoli and peritubular myoid cell lineages. Microinjection of transgenic, red fluorescent protein (RFP)-positive somatic testicular cells into the peritoneal cavity of X. tropicalis tadpoles resulted in cell deposits in heart, pronephros and intestine, and later in a strong proliferation and formation of cell-to-cell net growing through the tadpole body. Immunohistochemistry analysis of transplanted tadpoles showed a strong expression of vimentin in RFP-positive cells. No co-localization of Sox9 and Sma signals was observed during the first three weeks indicating their dedifferentiation to migratory-active mesenchymal cells recently described in human testicular biopsies.
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Abe T., Mikekado T., Haga S., Kisara Y., Watanabe K., Kurokawa T. and Suzuki T. (2007). Identification, cDNA cloning, and mRNA localization of a zebrafish ortholog of leukemia inhibitory factor. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 147, 38-44. 10.1016/j.cbpb.2006.12.019 PubMed DOI
Baker P. J., Sha J. A., McBride M. W., Peng L., Payne A. H. and O'Shaughnessy P. J. (1999). Expression of 3beta-hydroxysteroid dehydrogenase type I and type VI isoforms in the mouse testis during development. Eur. J. Biochem. 260, 911-917. 10.1046/j.1432-1327.1999.00245.x PubMed DOI
Berndtson W. E. and Thompson T. L. (1990). Changing relationships between testis size, Sertoli cell number and spermatogenesis in Sprague-Dawley rats. J. Androl. 11, 429-435. PubMed
Bott R., McFee R., Clopton D., Toombs C. and Cupp A. (2006). Vascular endothelial growth factor and kinase domain region receptor are involved in both seminiferous cord formation and vascular development during testis morphogenesis in the rat. Biol. Reprod. 75, 56-67. 10.1095/biolreprod.105.047225 PubMed DOI PMC
Campagnolo L., Russo M. A., Puglianiello A., Favale A. and Siracusa G. (2001). Mesenchymal cell precursors of peritubular smooth muscle cells of the mouse testis can be identified by the presence of the p75 neurotrophin receptor. Biol. Reprod. 64, 464-472. 10.1095/biolreprod64.2.464 PubMed DOI
Chikhovskaya J. V., Jonker M. J., Meissner A., Breit T. M., Repping S. and van Pelt A. M. M. (2012). Human testis-derived embryonic stem cell-like cells are not pluripotent, but possess potential of mesenchymal progenitors. Hum. Reprod. 27, 210-221. 10.1093/humrep/der383 PubMed DOI
Chikhovskaya J. V., van Daalen S. K. M., Korver C. M., Repping S. and van Pelt A. M. M. (2014). Mesenchymal origin of multipotent human testis-derived stem cells in human testicular cell cultures. Mol. Hum. Reprod. 20, 155-167. 10.1093/molehr/gat076 PubMed DOI
Chowdhury F., Li Y., Poh Y.-C., Yokohama-Tamaki T., Wang N. and Tanaka T. S. (2010). Soft substrates promote homogeneous self-renewal of embryonic stem cells via downregulating cell-matrix tractions. PLoS ONE 5, e15655 10.1371/journal.pone.0015655 PubMed DOI PMC
Combes A. N., Wilhelm D., Davidson T., Dejana E., Harley V., Sinclair A. and Koopman P. (2009). Endothelial cell migration directs testis cord formation. Dev. Biol. 326, 112-120. 10.1016/j.ydbio.2008.10.040 PubMed DOI
Conrad S., Renninger M., Hennenlotter J., Weisner T., Just L., Bonin M., Aicher W., Bühring H.-J., Mattheus U., Mack A. et al. (2008). Generation of pluripotent stem cells from adult human testis. Nature 456, 344-349. 10.1038/nature07404 PubMed DOI
Cool J., DeFalco T. and Capel B. (2012). Testis formation in the fetal mouse: dynamic and complex de novo tubulogenesis. Wiley Interdiscip. Rev. Dev. Biol. 1, 847-859. 10.1002/wdev.62 PubMed DOI
Cornelissen A. S., Maijenburg M. W., Nolte M. A. and Voermans C. (2015). Organ-specific migration of mesenchymal stromal cells: who, when, where and why? Immunol. Lett. 168, 159-169. 10.1016/j.imlet.2015.06.019 PubMed DOI
De Miguel M. P., De Boer-Brouwer M., Paniagua R., van den Hurk R., de Rooij D. G. and Van Dissel-Emiliani F. M. (1996). Leukemia inhibitory factor and ciliary neurotropic factor promote the survival of Sertoli cells and gonocytes in coculture system. Endocrinology 137, 1885-1893. PubMed
De Rooij D. G. (2009). The spermatogonial stem cell niche. Microsc. Res. Tech. 72, 580-585. 10.1002/jemt.20699 PubMed DOI
Dufour J., Hamilton M., Rajotte R. V. and Korbutt G. (2005). Neonatal Porcine Sertoli cells inhibit human natural antibody-mediated lysis. Biol. Reprod. 72, 1224-1231. 10.1095/biolreprod.104.038315 PubMed DOI
El Jamil A., Kanhoush R., Magre S., Boizet-Bonhoure B. and Penrad-Mobayed M. (2008). Sex-specific expression of SOX9 during gonadogenesis in the amphibian Xenopus tropicalis. Dev. Dyn. 237, 2996-3005. 10.1002/dvdy.21692 PubMed DOI
Flachsova M., Sindelka R. and Kubista M. (2013). Single blastomere expression profiling of Xenopus laevis embryos of 8 to 32-cells reveals developmental asymmetry. Sci. Rep. 3, 2278 10.1038/srep02278 PubMed DOI PMC
Frankenberg S. R., Frank D., Harland R., Johnson A. D., Nichols J., Niwa H., Schöler H. R., Tanaka E., Wylie C. and Brickman J. M. (2014). The POU-er of gene nomenclature. Development 141, 2921-2923. 10.1242/dev.108407 PubMed DOI
Fujiki K., Nakao M. and Dixon B. (2003). Molecular cloning and characterisation of a carp (Cyprinus carpio) cytokine-like cDNA that shares sequence similarity with IL-6 subfamily cytokines CNTF, OSM and LIF. Dev. Comp. Immunol. 27, 127-136. 10.1016/S0145-305X(02)00074-5 PubMed DOI
Geach T. and Zimmerman L. B. (2011). Developmental genetics in Xenopus tropicalis. Methods Mol. Biol. 770, 77-117. 10.1007/978-1-61779-210-6_4 PubMed DOI
Golestaneh N., Kokkinaki M., Pant D., Jiang J., DeStefano D., Fernandez-Bueno C., Rone J. D., Haddad B. R., Gallicano G. I. and Dym M. (2009). Pluripotent stem cells derived from adult human testes. Stem Cells Dev. 18, 1115-1125. 10.1089/scd.2008.0347 PubMed DOI PMC
Guan K., Nayernia K., Maier L. S., Wagner S., Dressel R., Lee J. H., Nolte J., Wolf F., Li M., Engel W. et al. (2006). Pluripotency of spermatogonial stem cells from adult mouse testis. Nature 440, 1199-1203. 10.1038/nature04697 PubMed DOI
Hanington P. C. and Belosevic M. (2007). Interleukin-6 family cytokine M17 induces differentiation and nitric oxide response of goldfish (Carassius auratus L.) macrophages. Dev. Comp. Immunol. 31, 817-829. 10.1016/j.dci.2006.12.001 PubMed DOI
Hanington P. C., Patten S. A., Reaume L. M., Waskiewicz A. J., Belosevic M. and Ali D. W. (2008). Analysis of leukemia inhibitory factor and leukemia inhibitory factor receptor in embryonic and adult zebrafish (Danio rerio). Dev. Biol. 314, 250-260. 10.1016/j.ydbio.2007.10.012 PubMed DOI
Hellsten U., Harland R. M., Gilchrist M. J., Hendrix D., Jurka J., Kapitonov V., Ovcharenko I., Putnam N. H., Shu S., Taher L. et al. (2010). The genome of the Western clawed frog Xenopus tropicalis. Science 328, 633-636. 10.1126/science.1183670 PubMed DOI PMC
Horiuchi H., Furusawa S. and Matsuda H. (2006). Maintenance of chicken embryonic stem cells in vitro. Methods Mol. Biol. 329, 17-34. 10.1385/1-59745-037-5:17 PubMed DOI
Hyliš M., Oborník M., Nebesářová J. and Vávra J. (2007). Aquatic tetrasporoblastic microsporidia from caddis flies (Insecta, Trichoptera): characterisation, phylogeny and taxonomic reevaluation of the genera Episeptum Larsson, 1986, Pyrotheca Hesse, 1935 and Cougourdella Hesse, 1935. Eur. J. Protistol. 43, 205-224. 10.1016/j.ejop.2007.03.004 PubMed DOI
Inoue M., Shima Y., Miyabayashi K., Tokunaga K., Sato T., Baba T., Ohkawa Y., Akiyama H., Suyama M. and Morohashi K.-i. (2016). Isolation and characterization of fetal Leydig progenitor cells of male mice. Endocrinology 157, 1222-1233. 10.1210/en.2015-1773 PubMed DOI
Jenab S. and Morris P. L. (1998). Testicular leukemia inhibitory factor (LIF) and LIF receptor mediate phosphorylation of signal transducers and activators of transcription (STAT)-3 and STAT-1 and induce c-fos transcription and activator protein-1 activation in rat Sertoli but not germ cells. Endocrinology 139, 1883-1890. 10.1210/en.139.4.1883 PubMed DOI
Johnson L., Zane R. S., Petty C. S. and Neaves W. B. (1984). Quantification of the human Sertoli cell population: its distribution, relation to germ cell numbers, and age-related decline. Biol. Reprod. 31, 785-795. 10.1095/biolreprod31.4.785 PubMed DOI
Kanatsu-Shinohara M., Ogonuki N., Inoue K., Miki H., Ogura A., Toyokuni S. and Shinohara T. (2003). Long-term proliferation in culture and germline transmission of mouse male germline stem cells. Biol. Reprod. 69, 612-616. 10.1095/biolreprod.103.017012 PubMed DOI
Kanatsu-Shinohara M., Inoue K., Lee J., Yoshimoto M., Ogonuki N., Miki H., Baba S., Kato T., Kazuki Y., Toyokuni S. et al. (2004). Generation of pluripotent stem cells from neonatal mouse testis. Cell 119, 1001-1012. 10.1016/j.cell.2004.11.011 PubMed DOI
Kanatsu-Shinohara M., Lee J., Inoue K., Ogonuki N., Miki H., Toyokuni S., Ikawa M., Nakamura T., Ogura A. and Shinohara T. (2008). Pluripotency of a single spermatogonial stem cell in mice. Biol. Reprod. 78, 681-687. 10.1095/biolreprod.107.066068 PubMed DOI
Karl J. and Capel B. (1998). Sertoli cells of the mouse testis originate from the coelomic epithelium. Dev. Biol. 203, 323-333. 10.1006/dbio.1998.9068 PubMed DOI
Kim Y.-S., Yi B.-R., Kim N.-H. and Choi K.-C. (2014). Role of the epithelial–mesenchymal transition and its effects on embryonic stem cells. Exp. Mol. Med. 46, e108 10.1038/emm.2014.44 PubMed DOI PMC
Ko K., Tapia N., Wu G., Kim J. B., Bravo M. J. A., Sasse P., Glaser T., Ruau D., Han D. W., Greber B. et al. (2009). Induction of pluripotency in adult unipotent germline stem cells. Cell Stem Cell 5, 87-96. 10.1016/j.stem.2009.05.025 PubMed DOI
Koopman P., Münsterberg A., Capel B., Vivian N. and Lovell-Badge R. (1990). Expression of a candidate sex-determining gene during mouse testis differentiation. Nature 348, 450-452. 10.1038/348450a0 PubMed DOI
Kossack N., Meneses J., Shefi S., Nguyen H. N., Chavez S., Nicholas C., Gromoll J., Turek P. J. and Reijo-Pera R. A. (2009). Isolation and characterization of pluripotent human spermatogonial stem cell-derived cells. Stem Cells 27, 138-149. 10.1634/stemcells.2008-0439 PubMed DOI PMC
Mathieu M.-E., Saucourt C., Mournetas V., Gauthereau X., Thézé N., Praloran V., Thiébaud P. and Boeuf H. (2012). LIF-dependent signaling: new pieces in the Lego. Stem Cell Rev. Rep. 8, 1-15. 10.1007/s12015-011-9261-7 PubMed DOI PMC
Mizrak S. C., Chikhovskaya J. V., Sadri-Ardekani H., van Daalen S., Korver C. M., Hovingh S. E., Roepers-Gajadien H. L., Raya A., Fluiter K., de Reijke T. M. et al. (2010). Embryonic stem cell-like cells derived from adult human testis. Hum. Reprod. 25, 158-167. 10.1093/humrep/dep354 PubMed DOI
Morrison G. M. and Brickman J. M. (2006). Conserved roles for Oct4 homologues in maintaining multipotency during early vertebrate development. Development 133, 2011-2022. 10.1242/dev.02362 PubMed DOI
Nef S., Shipman T. and Parada L. F. (2000). A molecular basis for estrogen-induced cryptorchidism. Dev. Biol. 224, 354-361. 10.1006/dbio.2000.9785 PubMed DOI
Nieuwkoop P. D. and Faber J. (1994). Normal Table of Xenopus laevis (Daudin). New York: Garland Publishing Inc.
Nishino K., Kato M., Yokouchi K., Yamanouchi K., Naito K. and Tojo H. (2000). Establishment of fetal gonad/mesonephros coculture system using EGFP transgenic mice. J. Exp. Zool. 286, 320-327. 10.1002/(SICI)1097-010X(20000215)286:3<320::AID-JEZ11>3.0.CO;2-8 PubMed DOI
O'Shaughnessy P. J., Morris I. D. and Baker P. J. (2008). Leydig cell re-generation and expression of cell signaling molecules in the germ cell-free testis. Reproduction 135, 851-858. 10.1530/REP-07-0529 PubMed DOI
Piquet-Pellorce C., Dorval-Coiffec I., Pham M.-D. and Jégou B. (2000). Leukemia inhibitory factor expression and regulation within the testis. Endocrinology 141, 1136-1141. 10.1210/endo.141.3.7399 PubMed DOI
Shan L. X. and Hardy M. P. (1992). Developmental changes in levels of luteinizing hormone receptor and androgen receptor in rat Leydig cells. Endocrinology 131, 1107-1114. PubMed
Shcherbo D., Merzlyak E. M., Chepurnykh T. V., Fradkov A. F., Ermakova G. V., Solovieva E. A., Lukyanov K. A., Bogdanova E. A., Zaraisky A. G., Lukyanov S. et al. (2007). Bright far-red fluorescent protein for whole-body imaging. Nat. Methods 4, 741-746. 10.1038/nmeth1083 PubMed DOI
Sidova M., Sindelka R., Castoldi M., Benes V. and Kubista M. (2015). Intracellular microRNA profiles form in the Xenopus laevis oocyte that may contribute to asymmetric cell division. Sci. Rep. 5, 11157 10.1038/srep11157 PubMed DOI PMC
Silva J., Nichols J., Theunissen T. W., Guo G., van Oosten A. L., Barrandon O., Wray J., Yamanaka S., Chambers I. and Smith A. (2009). Nanog is the gateway to the pluripotent ground state. Cell 138, 722-737. 10.1016/j.cell.2009.07.039 PubMed DOI PMC
Skinner M. K., Tung P. S. and Fritz I. B. (1985). Cooperativity between Sertoli cells and testicular peritubular cells in the production and deposition of extracellular matrix components. J. Cell Biol. 100, 1941-1947. 10.1083/jcb.100.6.1941 PubMed DOI PMC
Stanley E. L., Johnston D. S., Fan J., Papadopoulos V., Chen H., Ge R.-S., Zirkin B. and Jelinsky S. (2011). Stem Leydig cell differentiation: gene expression during development of the adult rat population of Leydig cells. Biol. Reprod. 85, 1161-1166. 10.1095/biolreprod.111.091850 PubMed DOI PMC
Tymowska J. (1973). Karyotype analysis of Xenopus tropicalis Gray, Pipidae. Cytogenet. Cell Genet. 12, 297-304. 10.1159/000130468 PubMed DOI
Wells D. E., Gutierrez L., Xu Z., Krylov V., Macha J., Blankenburg K. P., Hitchens M., Bellot L. J., Spivey M., Stemple D. L. et al. (2011). A genetic map of Xenopus tropicalis. Dev. Biol. 354, 1-8. 10.1016/j.ydbio.2011.03.022 PubMed DOI PMC