Expression of genes involved in neurogenesis, and neuronal precursor cell proliferation and development: Novel pathways of human ovarian granulosa cell differentiation and transdifferentiation capability in vitro
- Authors:
- Maciej Brązert
- Wiesława Kranc
- Piotr Celichowski
- Maurycy Jankowski
- Hanna Piotrowska‑Kempisty
- Leszek Pawelczyk
- Małgorzata Bruska
- Maciej Zabel
- Michał Nowicki
- Bartosz Kempisty
-
Affiliations: Division of Infertility and Reproductive Endocrinology, Department of Gynecology, Obstetrics and Gynecological Oncology, Poznań University of Medical Sciences, 60‑535 Poznań, Poland, Department of Anatomy, Poznań University of Medical Sciences, 60‑781 Poznań, Poland, Department of Histology and Embryology, Poznań University of Medical Sciences, 60‑781 Poznań, Poland, Department of Toxicology, Poznań University of Medical Sciences, 60‑631 Poznań, Poland, Division of Histology and Embryology, Department of Human Morphology and Embryology, Wrocław Medical University, 50‑368 Wrocław, Poland - Published online on: January 31, 2020 https://doi.org/10.3892/mmr.2020.10972
- Pages: 1749-1760
-
Copyright : © Brązert et al. This is an open access article distributed under the terms of Creative Commons Attribution License [CC BY 4.0].
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Abstract
Rybska M, Knap S, Jankowski M, Jeseta M, Bukowska D, Antosik P, Nowicki M, Zabel M, Kempisty B and Jaśkowski JM: Characteristic of factors influencing the proper course of folliculogenesis in mammals. Med J Cell Biol. 6:33–38. 2018. View Article : Google Scholar | |
Dzafic E, Stimpfel M and Virant-Klun I: Plasticity of granulosa cells: On the crossroad of stemness and transdifferentiation potential. J Assist Reprod Genet. 30:1255–1261. 2013. View Article : Google Scholar : PubMed/NCBI | |
Brevini TAL, Pennarossa G, Rahman MM, Paffoni A, Antonini S, Ragni G, deEguileor M, Tettamanti G and Gandolfi F: Morphological and molecular changes of human granulosa cells exposed to 5-azacytidine and addressed toward muscular differentiation. Stem Cell Rev Reports. 10:633–642. 2014. View Article : Google Scholar | |
Kossowska-Tomaszczuk K, Pelczar P, Güven S, Kowalski J, Volpi E, De Geyter C and Scherberich A: A novel three-dimensional culture system allows prolonged culture of functional human granulosa cells and mimics the ovarian environment. Tissue Eng Part A. 16:2063–2073. 2010. View Article : Google Scholar : PubMed/NCBI | |
Kossowska-Tomaszczuk K, De Geyter C, De Geyter M, Martin I, Holzgreve W, Scherberich A and Zhang H: The multipotency of luteinizing granulosa cells collected from mature ovarian follicles. Stem Cells. 27:210–219. 2009. View Article : Google Scholar : PubMed/NCBI | |
Ming G and Song H: Adult neurogenesis in the mammalian central nervous system. Annu Rev Neurosci. 28:223–250. 2005. View Article : Google Scholar : PubMed/NCBI | |
Ming GL and Song H: Adult neurogenesis in the mammalian brain: Significant answers and significant questions. Neuron. 70:687–702. 2011. View Article : Google Scholar : PubMed/NCBI | |
Kriegstein A and Alvarez-Buylla A: The Glial nature of embryonic and adult neural stem cells. Annu Rev Neurosci. 32:149–184. 2009. View Article : Google Scholar : PubMed/NCBI | |
Pistorius LR: Imaging of the embryonic and fetal central nervous system. Facts Views Vis Obgyn. 1:66–71. 2009.PubMed/NCBI | |
Liu A and Niswander LA: Bone morphogenetic protein signalling and vertebrate nervous system development. Nat Rev Neurosci. 6:945–954. 2005. View Article : Google Scholar : PubMed/NCBI | |
Rybska M, Knap S, Stefańska K, Jankowski M, Chamier-Gliszczyńska A, Popis M, Jeseta M, Bukowska D, Antosik P, Kempisty B, et al: Transforming growth factor (TGF)-is it a key protein in mammalian reproductive biology? Med J Cell Biol. 6:125–130. 2018. View Article : Google Scholar | |
D'Aiuto L, Zhi Y, Kumar Das D, Wilcox MR, Johnson JW, McClain L, MacDonald ML, Di Maio R, Schurdak ME, Piazza P, et al: Large-scale generation of human iPSC-derived neural stem cells/early neural progenitor cells and their neuronal differentiation. Organogenesis. 10:365–377. 2014. View Article : Google Scholar : PubMed/NCBI | |
Denham M and Dottori M: Neural differentiation of induced pluripotent stem cells. Methods Mol Biol. 793:99–110. 2011. View Article : Google Scholar : PubMed/NCBI | |
Samoilova EM, Kalsin VA, Kushnir NM, Chistyakov DA, Troitskiy AV and Baklaushev VP: Adult neural stem cells: Basic research and production strategies for neurorestorative therapy. Stem Cells Int. 2018:48354912018. View Article : Google Scholar : PubMed/NCBI | |
Anchan R, Gerami-Naini B, Lindsey JS, Ho JW, Kiezun A, Lipskind S, Ng N, LiCausi JA, Kim CS, Brezina P, et al: Efficient differentiation of steroidogenic and germ-like cells from epigenetically-related iPSCs derived from ovarian granulosa cells. PLoS One. 10:e01192752015. View Article : Google Scholar : PubMed/NCBI | |
Son EY, Ichida JK, Wainger BJ, Toma JS, Rafuse VF, Woolf CJ and Eggan K: Conversion of mouse and human fibroblasts into functional spinal motor neurons. Cell Stem Cell. 9:205–218. 2011. View Article : Google Scholar : PubMed/NCBI | |
Miyoshi N, Ishii H, Nagano H, Haraguchi N, Dewi DL, Kano Y, Nishikawa S, Tanemura M, Mimori K, Tanaka F, et al: Reprogramming of mouse and human cells to pluripotency using mature microRNAs. Cell Stem Cell. 8:633–638. 2011. View Article : Google Scholar : PubMed/NCBI | |
Brouwer M, Zhou H and Nadif Kasri N: Choices for induction of pluripotency: Recent developments in human induced pluripotent stem cell reprogramming strategies. Stem Cell Rev Rep. 12:54–72. 2016. View Article : Google Scholar : PubMed/NCBI | |
Attwood SW and Edel MJ: iPS-cell technology and the problem of genetic instability-can it ever be safe for clinical use? J Clin Med. 8(pii): E2882019. View Article : Google Scholar : PubMed/NCBI | |
Hermann A, Liebau S, Gastl R, Fickert S, Habisch HJ, Fiedler J, Schwarz J, Brenner R and Storch A: Comparative analysis of neuroectodermal differentiation capacity of human bone marrow stromal cells using various conversion protocols. J Neurosci Res. 83:1502–1514. 2006. View Article : Google Scholar : PubMed/NCBI | |
Zheng B, Wang C, He L, Xu X, Qu J, Hu J and Zhang H: Neural differentiation of mesenchymal stem cells influences chemotactic responses to HGF. J Cell Physiol. 228:149–162. 2013. View Article : Google Scholar : PubMed/NCBI | |
Mollinari C, Zhao J, Lupacchini L, Garaci E, Merlo D and Pei G: Transdifferentiation: A new promise for neurodegenerative diseases. Cell Death Dis. 9:8302018. View Article : Google Scholar : PubMed/NCBI | |
Fujimoto Y, Abematsu M, Falk A, Tsujimura K, Sanosaka T, Juliandi B, Semi K, Namihira M, Komiya S, Smith A and Nakashima K: Treatment of a mouse model of spinal cord injury by transplantation of human induced pluripotent stem cell-derived long-term self-renewing neuroepithelial-like stem cells. Stem Cells. 30:1163–1173. 2012. View Article : Google Scholar : PubMed/NCBI | |
Song CG, Zhang YZ, Wu HN, Cao XL, Guo CJ, Li YQ, Zheng MH and Han H: Stem cells: A promising candidate to treat neurological disorders. Neural Regen Res. 13:1294–1304. 2018. View Article : Google Scholar : PubMed/NCBI | |
Gancheva MR, Kremer KL, Gronthos S and Koblar SA: Using dental pulp stem cells for stroke therapy. Front Neurol. 10:4222019. View Article : Google Scholar : PubMed/NCBI | |
Zhang B, Gaiteri C, Bodea LG, Wang Z, McElwee J, Podtelezhnikov AA, Zhang C, Xie T, Tran L, Dobrin R, et al: Integrated systems approach identifies genetic nodes and networks in late-onset Alzheimer's disease. Cell. 153:707–720. 2013. View Article : Google Scholar : PubMed/NCBI | |
Soldner F, Hockemeyer D, Beard C, Gao Q, Bell GW, Cook EG, Hargus G, Blak A, Cooper O, Mitalipova M, et al: Parkinson's disease patient-derived induced pluripotent stem cells free of viral reprogramming factors. Cell. 136:964–977. 2009. View Article : Google Scholar : PubMed/NCBI | |
Hess DC, Wechsler LR, Clark WM, Savitz SI, Ford GA, Chiu D, Yavagal DR, Uchino K, Liebeskind DS, Auchus AP, et al: Safety and efficacy of multipotent adult progenitor cells in acute ischaemic stroke (MASTERS): A randomised, double-blind, placebo-controlled, phase 2 trial. Lancet Neurol. 16:360–368. 2017. View Article : Google Scholar : PubMed/NCBI | |
Altman J and Das GD: Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol. 124:319–335. 1965. View Article : Google Scholar : PubMed/NCBI | |
Sorrells SF, Paredes MF, Cebrian-Silla A, Sandoval K, Qi D, Kelley KW, James D, Mayer S, Chang J, Auguste KI, et al: Human hippocampal neurogenesis drops sharply in children to undetectable levels in adults. Nature. 555:377–381. 2018. View Article : Google Scholar : PubMed/NCBI | |
van Praag H, Kempermann G and Gage FH: Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci. 2:266–270. 1999. View Article : Google Scholar : PubMed/NCBI | |
Spalding KL, Bergmann O, Alkass K, Bernard S, Salehpour M, Huttner HB, Boström E, Westerlund I, Vial C, Buchholz BA, et al: Dynamics of hippocampal neurogenesis in adult humans. Cell. 153:1219–1227. 2013. View Article : Google Scholar : PubMed/NCBI | |
Eriksson PS, Perfilieva E, Björk-Eriksson T, Alborn AM, Nordborg C, Peterson DA and Gage FH: Neurogenesis in the adult human hippocampus. Nat Med. 4:1313–1317. 1998. View Article : Google Scholar : PubMed/NCBI | |
Dennis CV, Suh LS, Rodriguez ML, Kril JJ and Sutherland GT: Human adult neurogenesis across the ages: An immunohistochemical study. Neuropathol Appl Neurobiol. 42:621–638. 2016. View Article : Google Scholar : PubMed/NCBI | |
Knoth R, Singec I, Ditter M, Pantazis G, Capetian P, Meyer RP, Horvat V, Volk B and Kempermann G: Murine features of neurogenesis in the human hippocampus across the lifespan from 0 to 100 years. PLoS One. 5:e88092010. View Article : Google Scholar : PubMed/NCBI | |
Kempermann G, Kuhn HG and Gage FH: More hippocampal neurons in adult mice living in an enriched environment. Nature. 386:493–495. 1997. View Article : Google Scholar : PubMed/NCBI | |
Kranc W, Brązert M, Budna J, Celichowski P, Bryja A, Nawrocki MJ, Ożegowska K, Jankowski M, Chermuła B, Dyszkiewicz-Konwińska M, et al: Genes responsible for proliferation, differentiation, and junction adhesion are significantly up-regulated in human ovarian granulosa cells during a long-term primary in vitro culture. Histochem Cell Biol. 151:125–143. 2019. View Article : Google Scholar : PubMed/NCBI | |
Kranc W, Brązert M, Ożegowska K, Nawrocki MJ, Budna J, Celichowski P, Dyszkiewicz-Konwińska M, Jankowski M, Jeseta M, Pawelczyk L, et al: Expression profile of genes regulating steroid biosynthesis and metabolism in human ovarian granulosa cells-A primary culture approach. Int J Mol Sci. 18(pii): E26732017. View Article : Google Scholar : PubMed/NCBI | |
Kranc W, Brązert M, Celichowski P, Bryja A, Nawrocki MJ, Ożegowska K, Jankowski M, Jeseta M, Pawelczyk L, Bręborowicz A, et al: ‘Heart development and morphogenesis’ is a novel pathway for human ovarian granulosa cell differentiation during long-term in vitro cultivation-a microarray approach. Mol Med Rep. 19:1705–1715. 2019.PubMed/NCBI | |
Bryja A, Dyszkiewicz-Konwińska M, Jankowski M, Celichowski P, Stefańska K, Chamier-Gliszczyńska A, Borowiec B, Mehr K, Bukowska D, Antosik P, et al: Cation homeostasis and transport related gene markers are differentially expressed in porcine buccal pouch mucosal cells during long-term cells primary culture in vitro. Med J Cell Biol. 6:83–90. 2018. View Article : Google Scholar | |
Borys-Wójcik S, Kocherova I, Celichowski P, Popis M, Jeseta M, Bukowska D, Antosik P, Nowicki M and Kempisty B: Protein oligomerization is the biochemical process highly up-regulated in porcine oocytes before in vitro maturation (IVM). Med J Cell Biol. 6:155–162. 2018. View Article : Google Scholar | |
Ferraretti AP, La Marca A, Fauser BCJM, Tarlatzis B, Nargund G and Gianaroli L; ESHRE working group on Poor Ovarian Response Definition, : ESHRE consensus on the definition of ‘poor response’ to ovarian stimulation for in vitro fertilization: The Bologna criteria. Hum Reprod. 26:1616–1624. 2011. View Article : Google Scholar : PubMed/NCBI | |
Kranc W, Budna J, Dudek M, Bryja A, Chachuła A, Ciesiółka S, Borys S, Dyszkiewicz-Konwińska M, Jeseta M, Porowski L, et al: The origin, in vitro differentiation, and stemness specificity of progenitor cells. J Biol Regul Homeost Agents. 31:365–369. 2017.PubMed/NCBI | |
Chomczynski P and Sacchi N: Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 162:156–159. 1987. View Article : Google Scholar : PubMed/NCBI | |
Brązert M, Iżycki D, Kranc W, Borowiec B, Popis M, Ożegowska K, Bręborowicz A, Rachoń D, Nowicki M and Kempisty B: Genes involved in hormone metabolism and cellular response in human ovarian granulosa cells. J Biol Regul Homeost Agents. 33:461–468. 2019.PubMed/NCBI | |
Huang DW, Sherman BT, Tan Q, Kir J, Liu D, Bryant D, Guo Y, Stephens R, Baseler MW, Lane HC and Lempicki RA: DAVID bioinformatics resources: Expanded annotation database and novel algorithms to better extract biology from large gene lists. Nucleic Acids Res. 35((Web Server Issue)): W169–W175. 2007. View Article : Google Scholar : PubMed/NCBI | |
Huang da W, Sherman BT and Lempicki RA: Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 4:44–57. 2009. View Article : Google Scholar : PubMed/NCBI | |
Huang da W, Sherman BT and Lempicki RA: Bioinformatics enrichment tools: Paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 37:1–13. 2009. View Article : Google Scholar : PubMed/NCBI | |
Walter W, Sánchez-Cabo F and Ricote M: GOplot: An R package for visually combining expression data with functional analysis. Bioinformatics. 31:2912–2914. 2015. View Article : Google Scholar : PubMed/NCBI | |
Livak KJ and Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 25:402–408. 2001. View Article : Google Scholar : PubMed/NCBI | |
Kossowska-Tomaszczuk K and De Geyter C: Cells with stem cell characteristics in somatic compartments of the ovary. Biomed Res Int. 2013:3108592013. View Article : Google Scholar : PubMed/NCBI | |
Dzafic E, Stimpfel M, Novakovic S, Cerkovnik P and Virant-Klun I: Expression of mesenchymal stem cells-related genes and plasticity of aspirated follicular cells obtained from infertile women. Biomed Res Int. 2014:5082162014. View Article : Google Scholar : PubMed/NCBI | |
Poloni A, Maurizi G, Foia F, Mondini E, Mattiucci D, Ambrogini P, Lattanzi D, Mancini S, Falconi M, Cinti S, et al: Glial-like differentiation potential of human mature adipocytes. J Mol Neurosci. 55:91–98. 2015. View Article : Google Scholar : PubMed/NCBI | |
Zhang L, Feng T and Spicer LJ: The role of tight junction proteins in ovarian follicular development and ovarian cancer. Reproduction. 155:183–198. 2018. View Article : Google Scholar : PubMed/NCBI | |
Wissing ML, Kristensen SG, Andersen CY, Mikkelsen AL, Høst T, Borup R and Grøndahl ML: Identification of new ovulation-related genes in humans by comparing the transcriptome of granulosa cells before and after ovulation triggering in the same controlled ovarian stimulation cycle. Hum Reprod. 29:997–1010. 2014. View Article : Google Scholar : PubMed/NCBI | |
Hatzirodos N, Hummitzsch K, Irving-Rodgers HF and Rodgers RJ: Transcriptome profiling of the theca interna in transition from small to large antral ovarian follicles. PLoS One. 9:e974892014. View Article : Google Scholar : PubMed/NCBI | |
Takayanagi Y, Yoshida M, Bielsky IF, Ross HE, Kawamata M, Onaka T, Yanagisawa T, Kimura T, Matzuk MM, Young LJ and Nishimori K: Pervasive social deficits, but normal parturition, in oxytocin receptor-deficient mice. Proc Natl Acad Sci USA. 102:16096–16101. 2005. View Article : Google Scholar : PubMed/NCBI | |
Gutkowska J and Jankowski M: Oxytocin revisited: Its role in cardiovascular regulation. J Neuroendocrinol. 24:599–608. 2012. View Article : Google Scholar : PubMed/NCBI | |
Briones BA and Gould E: Adult neurogenesis and stress. In Stress: Physiology, biochemistry, and pathology. Elsevier; 3. pp. pp79–92. 2019 | |
Peng L and Bonaguidi MA: Function and dysfunction of adult hippocampal neurogenesis in regeneration and disease. Am J Pathol. 188:23–28. 2018. View Article : Google Scholar : PubMed/NCBI | |
Yoo S and Blackshaw S: Regulation and function of neurogenesis in the adult mammalian hypothalamus. Prog Neurobiol. 170:53–66. 2018. View Article : Google Scholar : PubMed/NCBI | |
Soares R, Ribeiro FF, Xapelli S, Genebra T, Ribeiro MF, Sebastião AM, Rodrigues CMP and Solá S: Tauroursodeoxycholic acid enhances mitochondrial biogenesis, neural stem cell pool, and early neurogenesis in adult rats. Mol Neurobiol. 55:3725–3738. 2018.PubMed/NCBI | |
Boldrini M, Fulmore CA, Tartt AN, Simeon LR, Pavlova I, Poposka V, Rosoklija GB, Stankov A, Arango V, Dwork AJ, et al: Human hippocampal neurogenesis persists throughout aging. Cell Stem Cell. 22:589–599.e5. 2018. View Article : Google Scholar : PubMed/NCBI | |
Danzer SC: Adult neurogenesis in the human brain: Paradise lost? Epilepsy Curr. 18:329–331. 2018. View Article : Google Scholar : PubMed/NCBI | |
Lin YT, Chen CC, Huang CC, Nishimori K and Hsu KS: Oxytocin stimulates hippocampal neurogenesis via oxytocin receptor expressed in CA3 pyramidal neurons. Nat Commun. 8:5372017. View Article : Google Scholar : PubMed/NCBI | |
Zimmerman EA, Nilaver G, Hou-Yu A and Silverman AL: Vasopressinergic and oxytocinergic pathways in the central nervous system. Fed Proc. 43:91–96. 1984.PubMed/NCBI | |
Busch-Nentwich E, Söllner C, Roehl H and Nicolson T: The deafness gene dfna5 is crucial for ugdh expression and HA production in the developing ear in zebrafish. Development. 131:943–951. 2004. View Article : Google Scholar : PubMed/NCBI | |
Stoll G, Ma Y, Yang H, Kepp O, Zitvogel L and Kroemer G: Pro-necrotic molecules impact local immunosurveillance in human breast cancer. Oncoimmunology. 6:e12993022017. View Article : Google Scholar : PubMed/NCBI | |
Webb MS, Miller AL and Thompson EB: In CEM cells the autosomal deafness gene dfna5 is regulated by glucocorticoids and forskolin. J Steroid Biochem Mol Biol. 107:15–21. 2007. View Article : Google Scholar : PubMed/NCBI | |
Yao X, Buhi WC, Alvarez IM, Curtis LM and Rarey KE: De novo synthesis of glucocorticoid hormone regulated inner ear proteins in rats. Hear Res. 86:183–188. 1995. View Article : Google Scholar : PubMed/NCBI | |
Croes L, Beyens M, Fransen E, Ibrahim J, Vanden Berghe W, Suls A, Peeters M, Pauwels P, Van Camp G and Op de Beeck K: Large-scale analysis of DFNA5 methylation reveals its potential as biomarker for breast cancer. Clin Epigenetics. 10:512018. View Article : Google Scholar : PubMed/NCBI | |
Assou S, Haouzi D, Dechaud H, Gala A, Ferrières A and Hamamah S: Comparative gene expression profiling in human cumulus cells according to ovarian gonadotropin treatments. Biomed Res Int. 2013:3545822013. View Article : Google Scholar : PubMed/NCBI | |
Chen Y, Teng FY and Tang BL: Coaxing bone marrow stromal mesenchymal stem cells towards neuronal differentiation: Progress and uncertainties. Cell Mol Life Sci. 63:1649–1657. 2006. View Article : Google Scholar : PubMed/NCBI | |
Qin X, Han W and Yu Z: Neuronal-like differentiation of bone marrow-derived mesenchymal stem cells induced by striatal extracts from a rat model of Parkinson's disease. Neural Regen Res. 7:2673–2680. 2012.PubMed/NCBI | |
Lilja J and Ivaska J: Integrin activity in neuronal connectivity. J Cell Sci. 131(pii): jcs2128032018. View Article : Google Scholar : PubMed/NCBI | |
Loulier K, Lathia JD, Marthiens V, Relucio J, Mughal MR, Tang SC, Coksaygan T, Hall PE, Chigurupati S, Patton B, et al: beta1 integrin maintains integrity of the embryonic neocortical stem cell niche. PLoS Biol. 7:e10001762009. View Article : Google Scholar : PubMed/NCBI | |
Honda T, Fujiwara H, Ueda M, Maeda M and Mori T: Integrin alpha 6 is a differentiation antigen of human granulosa cells. J Clin Endocrinol Metab. 80:2899–2905. 1995. View Article : Google Scholar : PubMed/NCBI | |
Kolle G, Georgas K, Holmes GP, Little MH and Yamada T: CRIM1, a novel gene encoding a cysteine-rich repeat protein, is developmentally regulated and implicated in vertebrate CNS development and organogenesis. Mech Dev. 90:181–193. 2000. View Article : Google Scholar : PubMed/NCBI | |
Prenkert M, Uggla B, Tidefelt U and Strid H: CRIM1 is expressed at higher levels in drug-resistant than in drug-sensitive myeloid leukemia HL60 cells. Anticancer Res. 30:4157–4161. 2010.PubMed/NCBI | |
Iwasaki Y, Shiojima T, Tagaya N, Kobayashi T and Kinoshita M: Effect of transforming growth factor β1 on spinal motor neurons after axotomy. J Neurol Sci. 147:9–12. 1997. View Article : Google Scholar : PubMed/NCBI | |
Mira H, Andreu Z, Suh H, Lie DC, Jessberger S, Consiglio A, San Emeterio J, Hortigüela R, Marqués-Torrejón MA, Nakashima K, et al: Signaling through BMPR-IA regulates quiescence and long-term activity of neural stem cells in the adult hippocampus. Cell Stem Cell. 7:78–89. 2010. View Article : Google Scholar : PubMed/NCBI | |
Blázquez-Medela AM, Jumabay M and Boström KI: Beyond the bone: Bone morphogenetic protein signaling in adipose tissue. Obes Rev. 20:648–658. 2019. View Article : Google Scholar : PubMed/NCBI | |
Nilsson EE and Skinner MK: Bone morphogenetic protein-4 acts as an ovarian follicle survival factor and promotes primordial follicle development. Biol Reprod. 69:1265–1272. 2003. View Article : Google Scholar : PubMed/NCBI | |
Takao Y, Fujiwara H, Yamada S, Hirano T, Maeda M, Fujii S and Ueda M: CD9 is expressed on the cell surface of human granulosa cells and associated with integrin alpha61. Mol Hum Reprod. 5:303–310. 1999. View Article : Google Scholar : PubMed/NCBI | |
Hayati AR, Nur Fariha MM, Tan GC, Tan AE and Chua K: Potential of human decidua stem cells for angiogenesis and neurogenesis. Arch Med Res. 42:291–300. 2011. View Article : Google Scholar : PubMed/NCBI | |
Yang Y, Ye Y, Su X, He J, Bai W and He X: MSCs-derived exosomes and neuroinflammation, neurogenesis and therapy of traumatic brain injury. Front Cell Neurosci. 11:552017. View Article : Google Scholar : PubMed/NCBI | |
Virant-Klun I, Rožman P, Cvjeticanin B, Vrtacnik-Bokal E, Novakovic S, Rülicke T, Dovc P and Meden-Vrtovec H: Parthenogenetic embryo-like structures in the human ovarian surface epithelium cell culture in postmenopausal women with no naturally present follicles and oocytes. Stem Cells Dev. 18:137–150. 2009. View Article : Google Scholar : PubMed/NCBI | |
Asaoka-Taguchi M, Yamada M, Nakamura A, Hanyu K and Kobayashi S: Maternal Pumilio acts together with Nanos in germline development in Drosophila embryos. Nat Cell Biol. 1:431–437. 1999. View Article : Google Scholar : PubMed/NCBI | |
Wang Z and Lin H: Nanos maintains germline stem cell self-renewal by preventing differentiation. Science. 303:2016–2019. 2004. View Article : Google Scholar : PubMed/NCBI | |
Subramaniam K and Seydoux G: nos-1 and nos-2, two genes related to Drosophila nanos, regulate primordial germ cell development and survival in Caenorhabditis elegans. Development. 126:4861–4871. 1999.PubMed/NCBI | |
Jaruzelska J, Kotecki M, Kusz K, Spik A, Firpo M and Reijo Pera RA: Conservation of a Pumilio-Nanos complex from Drosophila germ plasm to human germ cells. Dev Genes Evol. 213:120–126. 2003. View Article : Google Scholar : PubMed/NCBI | |
Virant-Klun I, Knez K, Tomazevic T and Skutella T: Gene expression profiling of human oocytes developed and matured in vivo or in vitro. Biomed Res Int. 2013:8794892013. View Article : Google Scholar : PubMed/NCBI | |
Julaton VT and Reijo Pera RA: NANOS3 function in human germ cell development. Hum Mol Genet. 20:2238–2250. 2011. View Article : Google Scholar : PubMed/NCBI |