Inhibition of TPPP3 attenuates β-catenin/NF-κB/COX-2 signaling in endometrial stromal cells and impairs decidualization

in Journal of Endocrinology
Correspondence should be addressed to A Dwivedi: anila.dwivedi@rediffmail.com
Restricted access

Embryo implantation and decidualization are critical events that occur during early pregnancy. Decidualization is synchronized by the crosstalk of progesterone and the cAMP signaling pathway. Previously, we confirmed the role of TPPP3 during embryo implantation in mice, but the underlying role and mechanism of TPPP3 in decidualization has not yet been understood. The current study was aimed to investigate the role of TPPP3 in decidualization in vivo and in vitro. For in vivo experiments, decidual reaction was artificially induced in the uteri of BALB/c mice. TPPP3 was found to be highly expressed during decidualization, whereas in the uteri receiving TPPP3 siRNA, decidualization was suppressed and the expression of β-catenin and decidual marker prolactin was reduced. In human endometrium, TPPP3 protein was found to be predominantly expressed in the mid-secretory phase (LH+7). In the primary culture of human endometrial stromal cells (hESCs), TPPP3 siRNA knockdown inhibited stromal-to-decidual cell transition and decreased the expression of the decidualization markers prolactin and IGFBP-1. Immunofluorescence and immunoblotting experiments revealed that TPPP3 siRNA knockdown suppressed the expression of β-catenin, NF-κB and COX-2 in hESCs during decidualization. TPPP3 inhibition also decreased NF-kB nuclear accumulation in hESCs and suppressed NF-κB transcriptional promoter activity. COX-2 expression was significantly decreased in the presence of a selective NF-kB inhibitor (QNZ) implicating that NF-kB is involved in COX-2 expression in hESCs undergoing decidualization. TUNEL assay and FACS analysis revealed that TPPP3 knockdown induced apoptosis and caused loss of mitochondrial membrane potential in hESCs. The study suggested that TPPP3 plays a significant role in decidualization and its inhibition leads to the suppression of β-catenin/NF-κB/COX-2 signaling along with the induction of mitochondria-dependent apoptosis.

 

      Society for Endocrinology

Related Articles

Article Information

Metrics

All Time Past Year Past 30 Days
Abstract Views 1227 1227 204
Full Text Views 283 283 17
PDF Downloads 26 26 5

Altmetrics

Figures

  • View in gallery

    Effect of TPPP3 knockdown during artificial decidualization in mice. (A) Representation of stimulated decidualization procedures. (B) Gross morphology of un-stimulated (UH) or stimulated (SH) uterine horn. (C) Protein expressions of TPPP3, β-catenin and decidual marker prolactin were examined by Western blotting (left panel). Densitometric quantitation of protein expression levels is shown as fold changes (right panel). Data are presented as mean ± s.e.m. P values: aP < 0.001, bP < 0.01, cP < 0.05 and dP > 0.05 vs un-stimulated or non-decidual horn (number of animals per group=5). A full color version of this figure is available at https://doi.org/10.1530/JOE-18-0459.

  • View in gallery

    TPPP3 knockdown in hESCs seized stromal to decidual cells transformation. (A) Immunohistochemical staining of TPPP3 in the mid-secretory phase endometrium samples from fertile women and unexplained infertile patients (LH+7). Nonspecific rabbit IgG was used as a negative control. Brown represents positive staining. (B) Immunostaining with vimentin, a stromal cell biomarker and cytokeratin, an epithelial cell biomarker. Vimentin was visualized as green. Cell nuclei were counterstained with 4′,6-diamidino-2-phenylindole (DAPI). (C) The TPPP3 was significantly increased during decidualization i.e. in the presence of MPA and db-cAMP which was suppressed in the cells transfected with TPPP3 siRNA. Data are presented as mean ± s.e.m. P values: aP < 0.001, bP < 0.01, cP < 0.05 and dP > 0.05 vs hESCs. (D) hESCs were transfected with TPPP3 siRNA or scrambled siRNA (control) on day 1 and day 6 and were cultured with db-cAMP and MPA for 9 days with medium changes at every 3 days. (E) TPPP3 knockdown in hESCs suppressed the mRNA level of decidualization markers prolactin and IGFBP-1. (F) Representative micrographs demonstrating the fluorescein isothiocyanate-labeled phalloidin to label F-actin filaments, and immunofluorescence was used to analyze the morphological transformation of hESCs during in vitro decidualization. (G) Co-localization of β-catenin and TPPP3 during in vitro decidualization. Each experiment was performed three times with three tissue samples.

  • View in gallery

    Protein expression and nuclear translocation of NF-κB p65 during in vitro decidualization. (A) TPPP3 knockdown suppressed NF-κB p65 protein expression. (B) TPPP3 knockdown in decidual cells inhibits NF-κB p65 nuclear translocation. Representative micrographs demonstrating the distribution of NF-kB p65 are shown. Cell images were grasped using a confocal fluorescence microscope (×63). (C) Transcriptional activation of the NF-κB promoter in decidual cells analyzed after TPPP3 knockdown and then transiently transfected with pNF-kB-luc reporter plasmid. pRL-luc plasmid was used as an internal control, and normalized relative luciferase activity was determined. Data are presented as mean ± s.e.m. P values: aP < 0.001, bP < 0.01, cP < 0.05 and dP > 0.05 vs scrambled siRNA control. Each experiment was performed three times with three tissue samples. A full color version of this figure is available at https://doi.org/10.1530/JOE-18-0459.

  • View in gallery

    TPPP3 inhibition reduces COX-2 expression. (A) Protein expression of COX-2 was examined by Western blotting (left panel). Densitometric quantitation of protein expression levels is shown as fold changes (right panel). Data are presented as mean ± s.e.m. P values: aP < 0.001, bP < 0.01, cP < 0.05 and dP > 0.05 vs scrambled siRNA control. (B). Representative micrographs demonstrating the distribution of COX-2 are shown. NF-kB inhibitor QNZ inhibited COX-2 expression. Cell images were grasped using a Nikon fluorescence microscope (×40). Each experiment was performed three times with three tissue samples.

  • View in gallery

    TPPP3 knockdown during in vitro decidualization in hESCs induce apoptosis and promote mitochondrial membrane potential (Δψm) loss. (A) TUNEL assay performed in scrambled siRNA or TPPP3 siRNA-transfected cells during in vitro decidualization. Cells were fixed and permeabilized, and the procedure was followed as described in the ‘Materials and Methods’ section. Representative figures stained for TUNEL showing a large number of TUNEL-positive cells in TPPP3 siRNA-transfected cells as compared with scrambled siRNA-transfected cells. Cell images were grasped using a Nikon fluorescence microscope at ×10. (B) Flow cytometric analysis of apoptosis in scrambled siRNA or TPPP3 siRNA-transfected cells stained with Annexin-V/PI (AV+/PI-intact cells; AV/PI+-nonviable/necrotic cells; AV+/PI and Av+/PI+-apoptotic cells). Representative images of flow cytometry of transfected cells are shown in the upper panel and the percentage of apoptosis with mean ± s.e.m. is shown in the lower panel. (C) Δψm was assessed by JC-1 staining using flow cytometry analysis. Representative images of flow cytometry of scrambled siRNA or TPPP3 siRNA-transfected cells are shown in the upper panel and the percentage loss of Δψm with mean ± s.e.m. (D) Effect of TPPP3 knockdown on apoptotic markers. Representative blots are shown (left panels) and densitometric quantitation of protein expression levels are shown as fold change (right panel). The experiments were performed three times. P values: aP < 0.001, bP < 0.01, cP < 0.05 and dP > 0.05 vs scrambled siRNA control. Each experiment was performed three times with three tissue samples.

References

AchacheHRevelA 2006 Endometrial receptivity markers, the journey to successful embryo implantation. Human Reproduction Update 12 731746. (https://doi.org/10.1093/humupd/dml004)

ArckPCHecherK 2013 Fetomaternal immune cross-talk and its consequences for maternal and offspring’s health. Nature Medicine 19 548556. (https://doi.org/10.1038/nm.3160)

CaoSZhangXEdwardsJPMosserDM 2006 NF-kappaB1 (p50) homodimers differentially regulate pro- and anti-inflammatory cytokines in macrophages. Journal of Biological Chemistry 281 2604126050. (https://doi.org/10.1074/jbc.M602222200)

CookePSBuchananDLYoungPSetiawanTBrodyJKorachKSTaylorJLubahnDBCunhaGR 1997 Stromal estrogen receptors mediate mitogenic effects of estradiol on uterine epithelium. PNAS 94 65356540. (https://doi.org/10.1073/pnas.94.12.6535)

DuQGellerDA 2010 Cross-regulation between Wnt and NF-kappaBsignaling pathways. Forum on Immunopathological Diseases and Therapeutics 1 155181. (https://doi.org/10.1615/ForumImmunDisTher.v1.i3)

FluhrHSpratteJBredowMHeidrichSZygmuntM 2013 Constitutive activity of ERK1/2 and NF-κB protects human endometrial stromal cells from death receptor-mediated apoptosis. Reproductive Biology 13 113121. (https://doi.org/10.1016/j.repbio.2013.03.001)

FrolovaAIO’NeillKMoleyKH 2011 Dehydroepiandrosterone inhibits glucose flux through the pentose phosphate pathway in human and mouse endometrial stromal cells, preventing decidualization and implantation. Molecular Endocrinology 25 14441455. (https://doi.org/10.1210/me.2011-0026)

Garrido-GomezTDominguezFLopezJACamafeitaEQuiñoneroAMartinez-ConejeroJAPellicerAConesaASimónC 2011 Modeling human endometrial decidualization from the interaction between proteome and secretome. Journal of Clinical Endocrinology and Metabolism 96 706716. (https://doi.org/10.1210/jc.2010-1825)

Garrido-GomezTDominguezFQuiñoneroADiaz-GimenoPKapidzicMGormleyMOnaKPadilla-IsertePMcMasterMGenbacevOet al. 2017 Defective decidualization during and after severe preeclampsia reveals a possible maternal contribution to the etiology. PNAS 114 E8468E8477. (https://doi.org/10.1073/pnas.1706546114)

GellersenBBrosensJ 2003 Cyclic AMP and progesterone receptor cross-talk in human endometrium: a decidualizing affair. Journal of Endocrinology 178 357372. (https://doi.org/10.1677/joe.0.1780357)

GellersenBBrosensJJ 2014 Cyclic decidualization of the human endometrium in reproductive health and failure. Endocrine Reviews 35 851905. (https://doi.org/10.1210/er.2014-1045)

GrassoEPapariniDAgueroMMorGLeirósCPRamhorstR 2014 VIP contribution to the decidualization program: regulatory T cells recruitment. Journal of Endocrinology 221 121131. (https://doi.org/10.1530/JOE-13-0565)

GriniusLKesslerCSchroederJHandwergerS 2006 Forkhead transcription factor FOXO1A is critical for induction of human decidualization. Journal of Endocrinology 189 179187. (https://doi.org/10.1677/joe.1.06451)

HayesMAQuinnBALillieBCôtéOBienzleDWaelchliRBetteridgeK 2012 Changes in various endometrial proteins during cloprostenol-induced failure of early pregnancy in mares. Animal Reproduction Science 9 723741.

HeringtonJLBiJMartinJDBanyBM 2007 β-catenin (CTNNB1) in the mouse uterus during decidualization and the potential role of two pathways in regulating its degradation. Journal of Histochemistry and Cytochemistry 55 963974. (https://doi.org/10.1369/jhc.7A7199.2007)

InoueHTanabeT 1998 Transcriptional role of the nuclear factor kB site in the induction by lipopolysaccharide and suppression by dexamethasone of cyclooxygenase-2 in U937 cells. Biochemical and Biophysical Research Communications 244 143148. (https://doi.org/10.1006/bbrc.1998.8222)

IrwinJCSuenLFFaessenGHPopoviciRMGiudiceLC 2001 Insulin-like growth factor (IGF)-II inhibition of endometrial stromal cell tissue inhibitor of metalloproteinase-3 and IGF-binding protein-1 suggests paracrine interactions at the decidua: trophoblast interface during human implantation. Journal of Clinical Endocrinology and Metabolism 86 20602064. (https://doi.org/10.1210/jc.86.5.2060)

JabbourHNCritchleyHO 2001 Potential roles of decidual prolactin in early pregnancy. Reproduction 121 197205. (https://doi.org/10.1530/rep.0.1210197)

KarinMLinA 2002 NF-kB at the crossroads of life and death. Nature Immunology 3 221227. (https://doi.org/10.1038/nbib302-221)

KaushalJBSankhwarPKumariSPopliPShuklaVHussainMKHajelaKDwivediA 2017 The regulation of Hh/Gli1 signaling cascade involves GSK3β-mediated mechanism in estrogen-derived endometrial hyperplasia. Scientific Reports 7 6557. (https://doi.org/10.1038/s41598-017-06370-1)

KaushalJBPopliPSankhwarPShuklaVDwivediA 2018 Sonic hedgehog protects endometrial hyperplasial cells against oxidative stress via suppressing mitochondrial fission protein dynamin-like GTPase (Drp1). Free Radical Biology and Medicine 129 582599. (https://doi.org/10.1016/j.freeradbiomed.2018.10.427)

KingAECritchleyHOKellyRW 2001 The NF-κB pathway in human endometrium and first trimester decidua. Molecular Human Reproduction 7 175183. (https://doi.org/10.1093/molehr/7.2.175)

KleinCScogginKEEalyADTroedssonMH 2010 Transcriptional profiling of equine endometrium during the time of maternal recognition of pregnancy. Biology of Reproduction 83 102113. (https://doi.org/10.1095/biolreprod.109.081612)

KriegSAFanXHongYSangQXGiacciaAWestphalLMLathiRBKriegAJNayakNR 2012 Global alteration in gene expression profiles of deciduas from women with idiopathic recurrent pregnancy loss. Molecular Human Reproduction 18 442450. (https://doi.org/10.1093/molehr/gas017)

LairdSMTuckermanEMLiTC 2006 Cytokine expression in the endometrium of Women with implantation failure and recurrent miscarriage. Reproductive Biomedicine Online 13 1323. (https://doi.org/10.1016/S1472-6483(10)62011-1)

LiQKannanADeMayoFJLydonJPCookePSYamagishiHSrivastavaDBagchiMKBagchiIC 2011 The antiproliferative action of progesterone in uterine epithelium is mediated by Hand2. Science 331 912916. (https://doi.org/10.1126/science.1197454)

LiBChenMLiuXGuoSW 2013a Constitutive and tumor necrosis factor-α-induced activation of nuclear factor-κB in adenomyosis and its inhibition by andrographolide. Fertility and Sterility 100 568577. (https://doi.org/10.1016/j.fertnstert.2013.04.028)

LiQKannanADasADeMayoFJHornsbyPJYoungSLTaylorRNBagchiMKBagchiIC 2013b WNT4 acts downstream of BMP2 and functions via β-catenin signaling pathway to regulate human endometrial stromal cell differentiation. Endocrinology 154 446457. (https://doi.org/10.1210/en.2012-1585)

LiYXuYYeKWuNLiJLiuNHeMLuBZhouWHuR 2016 Knockdown of tubulin polymerization promoting protein family Member 3 suppresses proliferation and induces apoptosis in non-small-cell lung cancer. Journal of Cancer 7 11891196. (https://doi.org/10.7150/jca.14790)

LiaoXGLiYLGaoRFGengYQChenXMLiuXQDingYBMuXYWangYXHeJL 2015 Folate deficiency decreases apoptosis of endometrium decidual cells in pregnant mice via the mitochondrial pathway. Nutrients 7 19161932. (https://doi.org/10.3390/nu7031916)

LimHPariaBCDasSKDinchukJELangenbachRTrzaskosJMDeySK 1997 Multiple female reproductive failures in cyclooxygenase 2–deficient mice. Cell 91 197208. (https://doi.org/10.1016/S0092-8674(00)80402-X)

LiuJGaoFLiuYFDouHTYanJQFanZMYangZM 2017 HB-EGF regulates Prss56 expression during mouse decidualization via EGFR/ERK/EGR2 signaling pathway. Journal of Endocrinology 234 247254. (https://doi.org/10.1530/JOE-16-0636)

MaBHottigerMO 2016 Crosstalk between Wnt/β-catenin and NF-κB signaling pathway during inflammation. Frontiers in immunology 7 378. (https://doi.org/10.3389/fimmu.2016.00378)

ManoharMKhanHSirohiVKDasVAgarwalAPandeyASiddiquiWADwivediA 2014a Alteration in endometrial proteins during early-and mid-secretory phases of the cycle in women with unexplained infertility. PLoS One 9 e111687. (https://doi.org/10.1371/journal.pone.0111687)

ManoharMKhanHShuklaVDasVAgarwalAPandeyASiddiquiWA 2014b Proteomic identification and analysis of human endometrial proteins associated with unexplained infertility. Journal of Proteomics and Bioinformatics 07 359366. (https://doi.org/10.4172/jpb.1000340)

MaruyamaTYoshimuraY 2008 Molecular and cellular mechanisms for differentiation and regeneration of the uterine endometrium. Endocrine Journal 55 795810. (https://doi.org/10.1507/endocrj.K08E-067)

NakaoSOgtataYShimizuEYamazakiMFuruyamaSSugiyaH 2002 Tumor necrosis factor a (TNF-a)-induced prostaglandin E2 release is mediated by the activation of cyclooxygenase-2 (COX-2) transcription via NFkB in human gingival fibroblasts. Molecular and Cellular Biochemistry 238 1118. (https://doi.org/10.1023/A:1019927616000)

Nejak-BowenKKikuchiAMongaSP 2013 Beta-catenin-NF-kappaB interactions in murine hepatocytes: a complex to die for. Hepatology 57 763774. (https://doi.org/10.1002/hep.26042)

PalazzoAFCookTAAlbertsASGundersenGG 2001 mDia mediates Rho- regulated formation and orientation of stable microtubules. Nature Cell Biology 3 723729. (https://doi.org/10.1038/35087035)

PattersonALPirochtaJTufanoSYTeixeiraJM 2017 Gain-of-function β-catenin in the uterine mesenchyme leads to impaired implantation and decidualization. Journal of Endocrinology 233 119130. (https://doi.org/10.1530/JOE-16-0502)

PedramARazandiMAitkenheadMHughesCCLevinER 2002 Integration of the non-genomic and genomic actions of estrogen, membrane-initiated signaling by steroid to transcription and cell biology. Journal of Biological Chemistry 277 5076850775. (https://doi.org/10.1074/jbc.M210106200)

PengJMonsivaisDYouRZhongHPangasSAMatzukMM 2015 Uterine activin receptor-like kinase 5 is crucial for blastocyst implantation and placental development. PNAS 112 E5098E5107. (https://doi.org/10.1073/pnas.1514498112)

Peter DurairajRRAberkaneAPolanskiLMaruyamaYBaumgartenMLucasESQuenbySChanJKYRaine-FenningNBrosensJJet al. 2017 Deregulation of the endometrial stromal cell secretome precedes embryo implantation failure. Molecular Human Reproduction 23 478487. (https://doi.org/10.1093/molehr/gax023)

PopliPSirohiVKManoharMShuklaVKaushalJBGuptaKDwivediA 2015 Regulation of cyclooxygenase-2 expression in rat oviductal epithelial cells: evidence for involvement of GPR30/Src kinase-mediated EGFR signaling. Journal of Steroid Biochemistry and Molecular Biology 154 130141. (https://doi.org/10.1016/j.jsbmb.2015.07.019)

RyanKMErnstMKRiceNRVousdenKH 2000 Role of NF-kappaB in p53-mediated programmed cell death. Nature 404 892897. (https://doi.org/10.1038/35009130)

SaegusaMHashimuraMKuwataTHamanoMOkayasuI 2007 Crosstalk between NF-κB/p65 and β-catenin/TCF4/p300 signalling pathways through alterations in GSK-3β expression during trans -differentiation of endometrial carcinoma cells. Journal of Pathology 213 3545. (https://doi.org/10.1002/path.2198).

SakowiczA 2018 The role of NFĸB in the three stages of pregnancy: implantation, maintenance and labour: a review article. BJOG 125 13791387. (https://doi.org/10.1111/1471-0528)

SalamonsenLADimitriadisEJonesRLNieG 2003 Complex regulation of decidualization: a role for cytokines and proteases-a review. Placenta 24 S76S85. (https://doi.org/10.1053/plac.2002.0928)

Schmedtje JrJFJiYSLiuWLDuBoisRNRungeMS 1997 Hypoxia induces cyclooxygenase-2 via the NF-kappaB p65 transcription factor in human vascular endothelial cells. Journal of Biological Chemistry 272 601608. (https://doi.org/10.1074/jbc.272.1.601)

ShindohHOkadaHTsuzukiTNishigakiAKanzakiH 2014 Requirement of heart and neural crest derivatives–expressed transcript 2 during decidualization of human endometrial stromal cells in vitro. Fertility and Sterility 101 1781.e11790.e1. (https://doi.org/10.1016/j.fertnstert.2014.03.013)

ShuklaVChandraVSankhwarPPopliPKaushalJBSirohiVKDwivediA 2015 Phytoestrogen genistein inhibits EGFR/PI3K/NF-kB activation and induces apoptosis in human endometrial hyperplasial cells. RSC Advances 5 5607556085. (https://doi.org/10.1039/C5RA06167A)

ShuklaVPopliPKaushalJBGuptaKDwivediA 2018 Uterine TPPP3 plays important role in embryo implantation via modulation of β-catenin. Biology of Reproduction 99 982999. (https://doi.org/10.1093/biolre/ioy136)

StefanoskaIJovanovicKrivokucaMVasilijicSCujicDVicovacL 2013 Prolactin stimulates cell migration and invasion by human trophoblast in vitro. Placenta 34 775783. (https://doi.org/10.1016/j.placenta.2013.06.305)

SuRWStrugMRJoshiNRJeongJWMieleLLesseyBAYoungSLFazleabasAT 2015 Decreased Notch pathway signaling in the endometrium of women with endometriosis impairs decidualization. Journal of Clinical Endocrinology and Metabolism 100 E433E442. (https://doi.org/10.1210/jc.2014-3720)

SuginoNKarube-HaradaATaketaniTSakataANakamuraY 2004 Withdrawal of ovarian steroids stimulates prostaglandin F2alpha production through nuclear factor-kappaB activation via oxygen radicals in human endometrial stromal cells: potential relevance to menstruation. Journal of Reproduction and Development 50 215225. (https://doi.org/10.1262/jrd.50.215)

TanabeTTohnaiN 2002 Cyclooxygenase isozymes and their gene structures and expression. Prostaglandins and Other Lipid Mediators 68–69 95114. (https://doi.org/10.1016/S0090-6980(02)00024-2)

TangBGullerSGurpideE 1994 Mechanisms of human endometrial stromal cell decidualization. Annals of the New York Academy of Sciences 734 1925. (https://doi.org/10.1111/j.1749-6632.1994.tb21731.x)

TsaiSHLiangYCChenLHoFMHsiehMSLinJK 2002 Arsenite stimulates cyclooxygenase‐2 expression through activating IκB kinase and nuclear factor κB in primary and ECV304 endothelial cells. Journal of Cellular Biochemistry 84 750758. (https://doi.org/10.1002/jcb.10096)

VinczeOTökésiNOláhJHlavandaEZotterAHorváthILehotzkyATiriánLMedzihradszkyKFKovácsJet al. 2006 Tubulin polymerization promoting proteins (TPPPs): members of a new family with distinct structures and functions. Biochemistry 45 1381813826. (https://doi.org/10.1021/bbib61305e)

WagleyYHwangCKLinHYKamAFYLawPYLohHHWeiLN 2013 Inhibition of c-Jun NH2-terminal kinase stimulates mu-opioid receptor expression via p38 MAPK-mediated nuclear NF-kB activation in neuronal and non-neuronal cells. Biochimica et Biophysica Acta 1833 14761488. (https://doi.org/10.1016/j.bbamcr.2013.02.017)

WeimarCHMacklonNSPost UiterweerEDBrosensJJGellersenB 2013 The motile and invasive capacity of human endometrial stromal cells: implications for normal and impaired reproductive function. Human Reproduction Update 19 542557. (https://doi.org/10.1093/humupd/dmbib25)

YenCFKimSHLiaoSKAtabekogluCUckacSAriciAArlierSLeeCLWangHSKayisliUA 2017 Increased expression of integrin-linked kinase during decidualization regulates the morphological transformation of endometrial stromal cells. Fertility and Sterility 107 803812. (https://doi.org/10.1016/j.fertnstert.2016.11.025)

YuHFYueZPWangKYangZQZhangHLGengSGuoB 2017 Gja1 acts downstream of Acvr1 to regulate uterine decidualization via Hand2 in mice. Journal of Endocrinology 233 145157. (https://doi.org/10.1530/JOE-16-0583)

ZhangLPattersonALZhangLTeixeiraJMPruJK 2012 Endometrial stromal beta-catenin is required for steroid-dependent mesenchymal-epithelial cross talk and decidualization. Reproductive Biology and Endocrinology 10 75. (https://doi.org/10.1186/1477-7827-10-75)

ZhouWLiJWangXHuR 2010a Stable knockdown of TPPP3 by RNA interference in Lewis lung carcinoma cell inhibits tumor growth and metastasis. Molecular and Cellular Biochemistry 343 231238. (https://doi.org/10.1007/s11010-010-0518-2)

ZhouWWangXLiLFengXYangZZhangWHuR 2010b Depletion of tubulin polymerization promoting protein family member 3 suppresses HeLa cell proliferation. Molecular and Cellular Biochemistry 333 9198. (https://doi.org/10.1007/s11010-009-0208-0)

PubMed

Google Scholar