Signaling Roadmap Modulating Chicken Primordial Germ Cells Proliferation and Self-Renewal

Subject Areas : Camel

M. Zare ¹ , S.Z. Mirhoseini ² , S.N. Hassani ³ , S. Ghovvati ⁴

1 - Department of Animal Science, Faculty of Agricultural Science, University of Guilan, Rasht, Iran
2 - Department of Animal Science, Faculty of Agricultural Science, University of Guilan,Guilan, Rasht, Iran
3 - Department of Stem Cells and Developmental Biology, Cell Science Research Center, Royan Institute for Stem Cell Biology and Technology, Academic Center for Education, Culture and Research (ACECR), Tehran, Iran
4 - Department of Animal Science, Faculty of Agricultural Science, University of Guilan, Rasht, Iran

Received: 2021-06-28 Accepted : 2021-12-15 Published : 2023-03-01

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References:

Aramaki S., Hayashi K., Kurimoto K., Ohta H., Yabuta Y., Iwanari H., Mochizuki Y., Hamakubo T., Kato Y., Shirahige K. and Saitou M. (2013). A mesodermal factor, T, specifies mouse germ cell fate by directly activating germline determinants. Dev. Cell. 27, 516-529.

Astick M.R. (2012). Fgf regulated cadherin expression in cranial nucleogenesis. PhD Thesis. University College London, London, United Kingdom.

Besmer P. (1993). The kit- ligand (steel factor) and its receptor c-kit/W: Pleiotropic roles in gametogenesis and melanogenesis. Development. 1, 125-137.

Bialecka M., Young T., de Sousa Lopes S.C., ten Berge D., Sanders A., Beck F. and Deschamps J. (2012). Cdx2 contributes to the expansion of the early primordial germ cell population in the mouse. Dev. Biol. 371, 227-234.

Blume-Jensen P., Siegbahn A., Stabel S., Heldin C.H. and Rönnstrand L. (1993). Increased Kit/SCF receptor induced mitogenicity but abolished cell motility after inhibition of protein kinase C. EMBO J. 12, 4199-4209.

Brazil D.P., Park J. and Hemmings B.A. (2002). PKB binding proteins. Getting in on the Akt cell. J. Cell. 111, 293-303.

Cantley L.C. (2002). The phosphoinositide 3-kinase pathway. Science. 296, 1655-1657.

Chang H. and Matzuk M.M. (2001). Smad5 is required for mouse primordial germ cell development. Mech. Dev. 104, 61-7.

Chang J.S., Fernand V., Zhang Y., Shin J., Jun H.J., Joshi Y. and Gettys T.W. (2012). NT-PGC-1α protein is sufficient to link β3-adrenergic receptor activation to transcriptional and physiological components of adaptive thermogenesis. J. Biol. Chem. 287, 9100-9111.

Chassot A.A., Bradford S.T., Auguste A., Gregoire E.P., Pailhoux E., De Rooij D.G., Schedl A. and Chaboissier M.C. (2012). WNT4 and RSPO1 together are required for cell proliferation in the early mouse gonad. Development. 139, 4461-4472.

Chatfield J., O'Reilly M.A., Bachvarova R.F., Ferjentsik Z., Redwood C., Walmsley M., Patient R., Loose M. and Johnson A.D. (2014). Stochastic specification of primordial germ cells from mesoderm precursors in axolotl embryos. Development. 141, 2429-2440.

Chawengsaksophak K., Svingen T., Ng E.T., Epp T., Spiller C.M., Clark C., Cooper H. and Koopman P. (2012). Loss of Wnt5a disrupts primordial germ cell migration and male sexual development in mice. Biol. Rep. 86, 4-11.

Chen L. and Khillan J.S. (2010). A novel signaling by vitamin A/retinol promotes self renewal of mouse embryonic stem cells by activating PI3K/Akt signaling pathway via insulin-like growth factor-1 receptor. Stem Cells. 28, 57-63.

Choi J.W., Kim S., Kim T.M., Kim Y.M., Seo H.W., Park T.S., Jeong J.W., Song G. and Han J.Y. (2010). Basic fibroblast growth factor activates MEK/ERK cell signaling pathway and stimulates the proliferation of chicken primordial germ cells. PLoS One . 5, e12968.

De Felici M., Carlo A.D., Pesce M., Iona S., Farrace M.G. and Piacentini M. (1999). Bcl-2 and Bax regulation of apoptosis in germ cells during prenatal oogenesis in the mouse embryo. Cell Death Differ. 6, 908-915.

De Felici M., Farini D. and Dolci S. (2009). In or out stemness: comparing growth factor signalling in mouse embryonic stem cells and primordial germ cells. Curr. Stem. Cell. Res. Ther. 4, 87-97.

De Sousa Lopes S.M., Roelen B.A., Monteiro R.M., Emmens R., Lin H.Y., Li E., Lawson K.A. and Mummery C.L. (2004). BMP signaling mediated by ALK2 in the visceral endoderm is necessary for the generation of primordial germ cells in the mouse embryo. Genes Dev. 18, 1838-1849.

Delaune E., Lemaire P. and Kodjabachian L. (2005). Neural induction in Xenopus requires early FGF signalling in addition to BMP inhibition. Development. 132, 299-310.

Ding V.M., Ling L., Natarajan S., Yap M.G., Cool S.M. and Choo A.B. (2010). FGF-2 modulates Wnt signaling in undifferentiated hESC and iPS cells through activated PI3‐K/GSK3β signaling. J. Cell. Physiol. 225, 417-428.

Dionne C.A., Crumley G., Bellot F., Kaplow J.M., Searfoss G., Ruta M., Burgess W.H., Jaye M. and Schlessinger J. (1990). Cloning and expression of two distinct high-affinity receptors cross-reacting with acidic and basic fibroblast growth factors. EMBO J. 9, 2685-2692.

Dolci S., Williams D.E., Ernst M.K., Resnick J.L., Brannan C.I., Lock L.F., Lyman S.D., Boswell H.S. and Donovan P.J. (1991). Requirement for mast cell growth factor for primordial germ cell survival in culture. Nature. 352, 809-811.

Dolci S., Pesce M. and De Felici M. (1993). Combined action of stem cell factor, leukemia inhibitory factor, and cAMP on in vitro proliferation of mouse primordial germ cells. Mol. Reprod. Dev. 35, 134-139.

Dolci S., Pellegrini M., Di A.S., Geremia R. and Rossi P. (2001). Signaling through extracellular signal-regulated kinase is required for spermatogonial proliferative response to stem cell factor. J. Biol. Chem. 276, 40225-40233.

Farini D., Scaldaferri M.L., Iona S., La Sala G. and De Felici M. (2005). Growth factors sustain primordial germ cell survival, proliferation and entering into meiosis in the absence of somatic cells. Dev. Biol. 285, 49-56.

Feldman B., Poueymirou W., Papaioannou V.E., DeChiara T.M. and Goldfarb M. (1995). Requirement of FGF-4 for postimplantationmouse development. Science. 267, 246-249.

Fu Y., Zheng S., An N., Athanasopoulos T., Popplewell L., Liang A., Li K., Hu C. and Zhu Y. (2011). Β-Catenin as a potential key target for tumor suppression. Int. J. Cancer. 129, 1541-1551.

Ge S., Yang C.H., Hsu K.S., Ming G.L. and Song H. (2007). A critical period for enhanced synaptic plasticity in newly generated neurons of the adult brain. Neuron. 54, 559-566.

Ge C., Yu M. and Zhang C. (2012). G protein-coupled receptor 30 mediates estrogen-induced proliferation of primordial germ cells via EGFR/Akt/β-catenin signaling pathway. Endocrinology. 153, 3504-3516.

Glover J.D. and McGrew M.J. (2012). Primordial germ cells technologies for avian germplasm cryopreservation and investigating germ cell development. J. Poult. Sci. 49, 155-162.

Godin I. and Wylie C.C. (1991). TGF beta 1 inhibits proliferation and has a chemotropic effect on mouse primordial germ cells in culture. Development. 113, 1451-1457.

Gu Y., Runyan C., Shoemaker A., Surani A. and Wylie C. (2009). Steel factor controls primordial germ cell survival and motility from the time of their specification in the allantois, and provides a continuous niche throughout their migration. J. Dev. Sci. 136, 1295-1303.

Han J.Y. (2009). Germ cells and transgenesis in chickens. Comp. Immunol. Microbiol. Infect. Dis. 32, 61-80.

Han L., Yang Y., Yue X., Huang K., Liu X., Pu P., Jiang H., Yan W., Jiang T. and Kang C. (2010). Inactivation of PI3K/AKT signaling inhibits glioma cell growth through modulation of β-catenin-mediated transcription. Brain Res. 1366, 9-17.

Hassani S.N., Totonchi M., Sharifi-Zarchi A., Mollamohammadi S., Pakzad M., Moradi S., Samadian A., Masoudi N., Mirshahvaladi S., Farrokhi A. and Greber B. (2014). Inhibition of TGFβ signaling promotes ground state pluripotency. Stem Cell Rev. Rep. 10, 16-30.

Hayashi K., Kobayashi T., Umino T., Goitsuka R., Matsui Y. and Kitamura D. (2002). SMAD1 signaling is critical for initial commitment of germ cell lineage from mouse epiblast. Mech. Dev. 118, 99-109.

Horiuchi H., Tategaki A., Yamashita Y., Hisamatsu H., Ogawa M., Noguchi T., Aosasa M., Kawashima T., Akita S., Nishimichi N. and Mitsui N. (2004). Chicken leukemia inhibitory factor maintains chicken embryonic stem cells in the undifferentiated state. J. Biol. Chem. 279, 24514-24520.

Imamura M., Hikabe O., Lin Z.Y.C. and Okano H. (2014). Generation of germ cells in vitro in the era of induced pluripotent stem cells. Mol. Reprod. Dev. 81, 2-19.

Israsena N., Hu M., Fu W., Kan L. and Kessler J.A. (2004). The presence of FGF2 signaling determines whether beta-catenin exerts effects on proliferation or neuronal differentiation of neural stem cells. Dev. Biol. 268, 220-231.

Itoh N. (2007). The Fgf families in humans, mice, and zebrafish: their evolutional processes and roles in development, metabolism, and disease. Biol. Pharm. Bull. 30, 1819-1825.

Johnson A.D., Crother B., White M.E., Patient R., Bachvarova R.F., Drum M. and Masi T. (2003). Regulative germ cell specification in axolotl embryos: a primitive trait conserved in the mammalian lineage. Biol. Sci. 358, 1371-1379.

Karagenç L. and Petitte J.N. (2000). Soluble factors and the emergence of chick primordial germ cells in vitro. Poult. Sci. 79, 80-85.

Kawabata M., Inoue H., Hanyu A., Imamura T. and Miyazono K. (1998). Smad proteins exist as monomers in vivo and undergo homo-and hetero-oligomerization upon activation by serine/threonine kinase receptors. EMBO J. 17, 4056-4065.

Kawase E., Hashimoto K. and Pedersen R.A. (2004). Autocrine and paracrine mechanisms regulating primordial germ cell proliferation. Mol. Reprod. Dev. 68, 5-16.

Kim H.S. (1998). Assignment1 of the human basic fibroblast growth factor gene FGF2 to chromosome 4 band q26 by radiation hybrid mapping . Cytogenet. Cell. Genet. 83, 73-81.

Kimura T., Nakamura T., Murayama K., Umehara H.. Yamano N., Watanabe S., Taketo M.M. and Nakano T. (2006). The stabilization of β-catenin leads to impaired primordial germ cell development via aberrant cell cycle progression. Dev. Biol. 300, 545-553.

Kimura T., Tomooka M., Yamano N., Murayama K., Matoba S., Umehara H., Kanai Y. and Nakano T. (2008). AKT signaling promotes derivation of embryonic germ cells from primordial germ cells. Development. 135, 869-879.

Kimura T., Kaga Y., Ohta H., Odamoto M., Sekita Y., Li K., Yamano N., Fujikawa K., Isotani A. and Sasaki N. (2014). Induction of primordial germ cell-like cells from mouse embryonic stem cells by ERK signal inhibition. Stem Cells. 32, 2668-2672.

Koshimizu U., Watanabe M. and Nakatsuji N. (1995). Retinoic acid is a potent growth activator of mouse primordial germ cells in vitro. Dev. Biol. 168, 683-685.

Kurimoto S., Jung J., Tapadia M., Waterman M., Mozaffar T. and Gupta R. (2014). Targeting the Wnt/ß-Catenin signaling pathway after traumatic nerve injury to improve functional recovery: N/A-Not a clinical study. J. Hand Surg. Am. 39, 13-17.

Laird D.J., Altshuler-Keylin S., Kissner M.D., Zhou X. and Anderson K.V. (2011). Ror2 enhances polarity and directional migration of primordial germ cells. PLoS Genet. 7, e1002428.

Lawson K.A., Dunn N.R., Roelen B.A., Zeinstra L.M., Davis A.M., Wright C.V., Korving J.P. and Hogan B.L. (1999). Bmp4 is required for the generation of primordial germ cells in the mouse embryo. Genes Dev. 13, 424-36. 

Lee H.C., Lim S. and Han J.Y. (2016). Wnt/β-catenin signaling pathway activation is required for proliferation of chicken primordial germ cells in vitro. Sci. Rep. 6, 1-8.

Logan C.Y. and Nusse R. (2004). The Wnt signaling pathway in development and disease. Annu. Rev. Cell Dev. Biol. 20, 781-810.

Macdonald J., Glover J.D., Taylor L., Sang H.M. and McGrew M.J. (2010). Characterisation and germline transmission of cultured avian primordial germ cells. PLoS One. 5, e15518.

Matsui Y., Zsebo K. and Hogan B.L. (1992). Derivation of pluripotential embryonic stem cells from murine primordial germ cells in culture. Cell. 70, 841-847.

Miyahara D., Mori T., Makino R., Nakamura Y., Oishi I., Ono T., Nirasawa K., Tagami T. and Kagami H. (2014). Culture conditions for maintain propagation, long-term survival and germline transmission of chicken primordial germ cell-like cells. J. Poult. Sci. 51, 87-95.

Miyahara D., Oishi I., Makino R., Kurumisawa N., Nakaya R., Ono T., Kagami H. and Tagami T. (2016). Chicken stem cell factor enhances primordial germ cell proliferation cooperatively with fibroblast growth factor 2. J. Rep. Dev. 62, 143-149.

Naito M., Harumi T. and Kuwana T. (2012). Expression of GFP gene in cultured PGCs isolated from embryonic blood and incorporation into gonads of recipient embryos. J. Poult. Sci. 2, 116-121.

Nakano M., Arisawa K., Yokoyama S., Nishimoto. M., Yamashita Y., Sakashita M., Ezaki R., Matsuda H., Furusawa S. and Horiuchi H. (2011). Characteristics of novel chicken embryonic stem cells established using chicken leukemia inhibitory factor. J. Poult. Sci. 48, 64-72.

Nicola N.A. and Hilton D.J. (1997). Growth Factors and Cytokines in Health and Disease. JAI Press, Greenwich, United Kingdom.

Oatley J.M., Kaucher A.V., Avarbock M.R. and Brinster R.L. (2010). Regulation of mouse spermatogonial stem cell differentiation by STAT3 signaling. Biol. Rep. 83, 427-433.

Ohinata Y., Ohta H., Shigeta M., Yamanaka K., Wakayama T. and Saitou M. (2009). A signaling principle for the specification of the germ cell lineage in mice. Cell. 137, 571-584.

Otero J.J., Fu W., Kan L., Cuadra A.E. and Kessler J.A. (2004). β-Catenin signaling is required for neural differentiation of embryonic stem cells. Development. 131, 3545-3557

Paling N.R.D., Wheadon H., Bone H.K. and Welham M.J. (2004). Regulation of embryonic stem cell self-renewal by phosphoinositide 3-kinase-dependent signaling. J. Biol. Chem. 279, 48063-48070.

Park H.J., Park T.S., Kim T.M., Kim J.N., Shin S.S., Lim J.M. and Han J.Y. (2006). Establishment of an in vitro culture system for chicken preblastodermal cells. Mol. Reprod. Dev. 73, 452-461.

Park T.S. and Han J.Y. (2000). Derivation and characterization of pluripotent embryonic germ cells in chicken. Mol. Reprod. Dev. 56, 475-482 .

Petitte J., Liu G. and Yang Z. (2004). Avian pluripotent stem cells. Mech. Dev. 121, 1159-1168.

Polakis P. (2012). Wnt signaling in cancer. Cold Spring Harb. Perspect. Biol. 4, a008052.

Rameh L.E. and Cantley L.C. (1999). The role of phosphoinositide 3-kinase lipid products in cell function. J. Biol. Chem. 274, 8347-8350.

Resnick J.L., Bixler L.S., Cheng L. and Donovan P.J. (1992). Long-term proliferation of mouse primordial germ cells in culture. Nature. 359, 550-551.

Resnick J.L., Ortiz M., Keller J.R. and Donovan P.J. (1998). Role of fibroblast growth factors and their receptors in mouse primordial germ cell growth. Biol. Reprod. 59, 1224-1229.

Sato N., Meijer L., Skaltsounis L., Greengard P. and Brivanlou A.H. (2004). Maintenance of pluripotency in human and mouse embryonic stem cells through activation of Wnt signaling by a pharmacological GSK-3-specific inhibitor. Nat. Med. 10, 55-63.

Sheng X.R., Posenau T., Gumulak-Smith J.J., Matunis E., Van Doren M. and Wawersik M. (2009). Jak–STAT regulation of male germline stem cell establishment during Drosophila embryogenesis. Dev. Biol. 334, 335-344.

Smith A.G., Heath J.K., Donaldson D.D., Wong G.G., Moreau J., Stahl M. and Rogers D. (1988). Inhibition of pluripotential embryonic stem cell differentiation by purified polypeptides. Nature. 336, 688-690.

Sun F., Fu H., Liu Q., Tie Y., Zhu J., Xing R., Sun Z. and Zheng X. (2008). Downregulation of CCND1 and CDK6 by miR-34a induces cell cycle arrest. FEBS Lett. 582, 1564-1568.

Taga T. and Kishimoto T. (1997). Gp130 and the interleukin-6 family of cytokines. Annu. Rev. Immunol. 15, 797-805.

Takeuchi Y., Molyneaux K., Runyan C., Schaible K. and Wylie C. (2005). The roles of FGF signaling in germ cell migration in the mouse. Development. 132, 5399-5409.

Tanaka S.S., Nakane A., Yamaguchi Y.L., Terabayashi T., Abe T., Nakao K., Asashima M., Steiner K.A., Tam P.P. and Nishinakamura R. (2013). Dullard/Ctdnep1 modulates WNT signalling activity for the formation of primordial germ cells in the mouse embryo. PLoS One. 8, e57428.

Tang X., Zhang C., Zeng W., Mi Y. and Liu H. (2006). Proliferating effects of the flavonoids daidzein and quercetin on cultured chicken primordial germ cells through antioxidant action. Cell Biol. Int. 30, 445-451.

Tomida M., Yamamoto-Yamaguchi Y. and Hozumi M. (1984). Purification of a factor inducing differentiation of mouse myeloid leukemic M1 cells from conditioned medium of mouse fibroblast L929 cells. J. Biol. Chem. 259, 10978-10982.

Tremblay K.D., Dunn N.R. and Robertson E.J. (2001). Mouse embryos lacking Smad1 signals display defects in extra-embryonic tissues and germ cell formation. Development. 128, 3609-3621.

Ueda S., Mizuki M., Ikeda H., Tsujimura T., Matsumura I., Nakano K., Daino H., Hondaz I.Z., Sonoyama J., Shibayama H. and Sugahara H. (2002). Critical roles of c-Kit tyrosine residues 567 and 719 in stem cell factor–induced chemotaxis: contribution of src family kinase and PI3-kinase on calcium mobilization and cell migration. Blood. 99, 3342-3349.

Ulu F., Kim S.M., Yokoyama T. and Yamazaki Y. (2017). Dose-dependent functions of fibroblast growth factor 9 regulate the fate of murine XY primordial germ cells. Biol. Reprod. 96, 122-129.

Vainio S., Heikkilä M., Kispert A., Chin N. and McMahon A.P. (1999). Female development in mammals is regulated by Wnt-4 signalling. Nature. 397, 405-409.

Valenta T., Gay M., Steiner S., Draganova K., Zemke M., Hoffmans R., Cinelli P., Aguet M., Sommer L. and Basler K. (2011). Probing transcription-specific outputs of β-catenin in vivo. Genes Dev. 25, 2631-2643.

Valenta T.. Hausmann G. and Basler K. (2012). The many faces and functions of β-catenin. EMBO J. 31, 2714-2736.

Van de Lavoir M.C., Diamond J.H., Leighton P.A., Mather‑Love C., Heyer B.S., Bradshaw R., Kerchner A., Hooi L.T., Gessaro T.M., Swanberg S.E. and Delany M.E. (2006). Germline transmission of genetically modified primordial germ cells. Nature. 441, 766-769.

Wang M., Zhang C., Huang C., Cheng S., He N., Wang Y., Ahmed M.F., Zhao R., Jin J., Zuo Q. and Zhang Y. (2018). Regulation of fibroblast growth factor 8 (FGF8) in chicken embryonic stem cells differentiation into spermatogonial stem cells. J. Cell. Biochem. 119, 2396-2407.

Whyte J., Glover J.D., Woodcock M., Brzeszczynska J., Taylor L., Sherman A., Kaiser P. and McGrew M.J. (2015). FGF, insulin, and SMAD signaling cooperate for avian primordial germ cell self-renewal. Stem Cell Rep. 5, 1-12.

Yakhkeshi S., Rahimi S., Sharafi M., Hassani S.N., Taleahmad S., Shahverdi A. and Baharvand H. (2018). In vitro improvement of quail primordial germ cell expansion through activation of TGF-beta signaling pathway. J. Cell. Biochem. 119, 4309-4319.

Ying Y. and Zhao G.Q. (2000). Detection of multiple bone morphogenetic protein messenger ribonucleic acids and their signal transducer, Smad1, during mouse decidualization. Biol. Rep. 63, 1781-1786.

Ying Y. and Zhao G.Q. (2001). Cooperation of endoderm-derived BMP2 and extraembryonic ectoderm-derived BMP4 in primordial germ cell generation in the mouse. Dev. Biol. 232, 484-492.

Yu X., Shen N., Zhang M.L., Pan F.Y., Wang C., Jia W.P., Liu C., Gao Q., Gao X., Xue B. and Li C.J. (2011). Egr‐1 decreases adipocyte insulin sensitivity by tilting PI3K/Akt and MAPK signal balance in mice. EMBO J. 30, 3754-3765.

Zhang Y., Zhang L., Zuo Q., Wang Y., Zhang Y., Xu Q., Li B. and Chen G. (2017). JAK-STAT signaling regulation of chicken embryonic stem cell differentiation into male germ cells. In vitro Cell. Dev. Biol. 53, 728-743.

Zuo Q., Jin J., Jin K., Sun C., Song J., Zhang Y., Chen G. and Li B. (2019). Distinct roles of retinoic acid and BMP4 pathways in the formation of chicken primordial germ cells and spermatogonial stem cells. Food Funct. 10, 7152-7163.