Gap Junctions and Wnt Signaling in the Mammary Gland: a Cross-Talk? (original) (raw)
Chua AC, Hodson LJ, Moldenhauer LM, Robertson SA, Ingman WV. Dual roles for macrophages in ovarian cycle-associated development and remodelling of the mammary gland epithelium. Development. 2010;137(24):4229–38. ArticleCASPubMed Google Scholar
Gouon-Evans V, Rothenberg ME, Pollard JW. Postnatal mammary gland development requires macrophages and eosinophils. Development. 2000;127(11):2269–82. CASPubMed Google Scholar
Keely PJ, Wu JE, Santoro SA. The spatial and temporal expression of the α2β1 integrin and its ligands, collagen I, collagen IV, and laminin, suggest important roles in mouse mammary morphogenesis. Differentiation. 1995;59(1):1–13. ArticleCASPubMed Google Scholar
Koledova Z, Lu P. A 3D Fibroblast-Epithelium Co-culture Model for Understanding Microenvironmental Role in Branching Morphogenesis of the Mammary Gland. Mammary Gland Development. Berlin: Springer; 2017. p. 217–31. Google Scholar
O'Brien J, Martinson H, Durand-Rougely C, Schedin P. Macrophages are crucial for epithelial cell death and adipocyte repopulation during mammary gland involution. Development. 2012;139(2):269–75. ArticleCASPubMed Google Scholar
Taddei I, Deugnier M-A, Faraldo MM, Petit V, Bouvard D, Medina D, et al. β1 integrin deletion from the basal compartment of the mammary epithelium affects stem cells. Nat Cell Biol. 2008;10(6):716. ArticleCASPubMedPubMed Central Google Scholar
Woodward T, Mienaltowski A, Modi R, Bennett J, Haslam S. Fibronectin and the α5β1 integrin are under developmental and ovarian steroid regulation in the normal mouse mammary gland. Endocrinology. 2001;142(7):3214–22. ArticleCASPubMed Google Scholar
Insua-Rodríguez J, Oskarsson T. The extracellular matrix in breast cancer. Adv Drug Deliv Rev. 2016;97:41–55. ArticleCASPubMed Google Scholar
Majidinia M, Yousefi B. Breast tumor stroma: a driving force in the development of resistance to therapies. Chem Biol Drug Des. 2017;89(3):309–18. ArticleCASPubMed Google Scholar
Soysal SD, Tzankov A, Muenst SE. Role of the tumor microenvironment in breast cancer. Pathobiology. 2015;82(3–4):142–52. ArticleCASPubMed Google Scholar
Knudsen KA, Wheelock MJ. Cadherins and the mammary gland. J Cell Biochem. 2005;95(3):488–96. ArticleCASPubMed Google Scholar
McLachlan E, Shao Q, Laird DW. Connexins and gap junctions in mammary gland development and breast cancer progression. J Membr Biol. 2007;218(1–3):107–21. ArticleCASPubMed Google Scholar
Hirschi KK, Xu C, Tsukamoto T, Sager R. Gap junction genes Cx26 and Cx43 individually suppress the cancer phenotype of human mammary carcinoma cells and restore differentiation potential. Cell Growth Differ. 1996;7(7):861–70. CASPubMed Google Scholar
Laird DW, Fistouris P, Batist G, Alpert L, Huynh HT, Carystinos GD, et al. Deficiency of connexin43 gap junctions is an independent marker for breast tumors. Cancer Res. 1999;59(16):4104–10. CASPubMed Google Scholar
Singal R, Tu Z, Vanwert J, Ginder G, Kiang D. Modulation of the connexin26 tumor suppressor gene expression through methylation in human mammary epithelial cell lines. Anticancer Res. 2000;20(1A):59–64. CASPubMed Google Scholar
Qin H, Shao Q, Curtis H, Galipeau J, Belliveau DJ, Wang T, et al. Retroviral delivery of connexin genes to human breast tumor cells inhibits in vivo tumor growth by a mechanism that is independent of significant gap junctional intercellular communication. J Biol Chem. 2002;277(32):29132–8. ArticleCASPubMed Google Scholar
Kańczuga-Koda L, Sulkowska M, Koda M, Reszeć J, Famulski W, Baltaziak M, et al. Expression of connexin 43 in breast cancer in comparison with mammary dysplasia and the normal mammary gland. Folia Morphol (Warsz). 2003;62(4):439–42. Google Scholar
Momiyama M, Omori Y, Ishizaki Y, Nishikawa Y, Tokairin T, Ogawa J, et al. Connexin26-mediated gap junctional communication reverses the malignant phenotype of MCF-7 breast cancer cells. Cancer Sci. 2003;94(6):501–7. ArticleCASPubMed Google Scholar
Shao Q, Wang H, McLachlan E, Veitch GI, Laird DW. Down-regulation of Cx43 by retroviral delivery of small interfering RNA promotes an aggressive breast cancer cell phenotype. Cancer Res. 2005;65(7):2705–11. ArticleCASPubMed Google Scholar
Kalra J, Shao Q, Qin H, Thomas T, Alaoui-Jamali MA, Laird DW. Cx26 inhibits breast MDA-MB-435 cell tumorigenic properties by a gap junctional intercellular communication-independent mechanism. Carcinogenesis. 2006;27(12):2528–37. ArticleCASPubMed Google Scholar
Plante I, Laird DW. Decreased levels of connexin43 result in impaired development of the mammary gland in a mouse model of oculodentodigital dysplasia. Dev Biol. 2008;318(2):312–22. ArticleCASPubMed Google Scholar
Plante I, Wallis A, Shao Q, Laird DW. Milk secretion and ejection are impaired in the mammary gland of mice harboring a Cx43 mutant while expression and localization of tight and adherens junction proteins remain unchanged. Biol Reprod. 2010;82(5):837–47. ArticleCASPubMed Google Scholar
Plante I, Stewart M, Barr K, Allan A, Laird D. Cx43 suppresses mammary tumor metastasis to the lung in a Cx43 mutant mouse model of human disease. Oncogene. 2011;30(14):1681. ArticleCASPubMed Google Scholar
Talhouk RS, Fares M-B, Rahme GJ, Hariri HH, Rayess T, Dbouk HA, et al. Context dependent reversion of tumor phenotype by connexin-43 expression in MDA-MB231 cells and MCF-7 cells: role of β-catenin/connexin43 association. Exp Cell Res. 2013;319(20):3065–80. ArticleCASPubMed Google Scholar
Stewart MK, Plante I, Bechberger JF, Naus CC, Laird DW. Mammary gland specific knockdown of the physiological surge in Cx26 during lactation retains normal mammary gland development and function. PLoS One. 2014;9(7):e101546. ArticleCASPubMedPubMed Central Google Scholar
Stewart MK, Bechberger JF, Welch I, Naus CC, Laird DW. Cx26 knockout predisposes the mammary gland to primary mammary tumors in a DMBA-induced mouse model of breast cancer. Oncotarget. 2015;6(35):37185. ArticlePubMedPubMed Central Google Scholar
Mroue R, Inman J, Mott J, Budunova I, Bissell MJ. Asymmetric expression of connexins between luminal epithelial-and myoepithelial-cells is essential for contractile function of the mammary gland. Dev Biol. 2015;399(1):15–26. ArticleCASPubMed Google Scholar
Ferrati S, Gadok AK, Brunaugh AD, Zhao C, Heersema LA, Smyth HD, et al. Connexin membrane materials as potent inhibitors of breast cancer cell migration. J R Soc Interface. 2017;14(133):20170313. ArticleCASPubMedPubMed Central Google Scholar
Monaghan P, Perusinghe N, Carlile G, Evans WH. Rapid modulation of gap junction expression in mouse mammary gland during pregnancy, lactation, and involution. J Histochem Cytochem. 1994;42(7):931–8. ArticleCASPubMed Google Scholar
Locke D, Perusinghe N, Newman T, Jayatilake H, Evans WH, Monaghan P. Developmental expression and assembly of connexins into homomeric and heteromeric gap junction hemichannels in the mouse mammary gland. J Cell Physiol. 2000;183(2):228–37. ArticleCASPubMed Google Scholar
Locke D, Stein T, Davies C, Morris J, Harris AL, Evans WH, et al. Altered permeability and modulatory character of connexin channels during mammary gland development. Exp Cell Res. 2004;298(2):643–60. ArticleCASPubMed Google Scholar
Locke D, Jamieson S, Stein T, Liu J, Hodgins MB, Harris AL, et al. Nature of Cx30-containing channels in the adult mouse mammary gland. Cell Tissue Res. 2007;328(1):97–107. ArticleCASPubMed Google Scholar
Talhouk RS, Elble RC, Bassam R, Daher M, Sfeir A, Mosleh LA, et al. Developmental expression patterns and regulation of connexins in the mouse mammary gland: expression of connexin30 in lactogenesis. Cell Tissue Res. 2005;319(1):49–59. ArticleCASPubMed Google Scholar
Dianati E, Poiraud J, Weber-Ouellette A, Plante I. Connexins, E-cadherin, Claudin-7 and β-catenin transiently form junctional nexuses during the post-natal mammary gland development. Dev Biol. 2016;416(1):52–68. ArticleCASPubMed Google Scholar
El-Sabban ME, Sfeir AJ, Daher MH, Kalaany NY, Bassam RA, Talhouk RS. ECM-induced gap junctional communication enhances mammary epithelial cell differentiation. J Cell Sci. 2003;116(17):3531–41. ArticleCASPubMed Google Scholar
Talhouk RS, Mroue R, Mokalled M, Abi-Mosleh L, Nehme R, Ismail A, et al. Heterocellular interaction enhances recruitment of α and β-catenins and ZO-2 into functional gap-junction complexes and induces gap junction-dependant differentiation of mammary epithelial cells. Exp Cell Res. 2008;314(18):3275–91. ArticleCASPubMed Google Scholar
van Genderen C, Okamura RM, Farinas I, Quo R-G, Parslow TG, Bruhn L, et al. Development of several organs that require inductive epithelial-mesenchymal interactions is impaired in LEF-1-deficient mice. Genes Dev. 1994;8(22):2691–703. ArticlePubMed Google Scholar
Fritz G, Just I, Kaina B. Rho GTPases are over-expressed in human tumors. Int J Cancer. 1999;81(5):682–7. ArticleCASPubMed Google Scholar
Fritz G, Brachetti C, Bahlmann F, Schmidt M, Kaina B. Rho GTPases in human breast tumours: expression and mutation analyses and correlation with clinical parameters. Br J Cancer. 2002;87(6):635. ArticleCASPubMedPubMed Central Google Scholar
Lin S-Y, Xia W, Wang JC, Kwong KY, Spohn B, Wen Y, et al. β-Catenin, a novel prognostic marker for breast cancer: its roles in cyclin D1 expression and cancer progression. Proc Natl Acad Sci. 2000;97(8):4262–6. ArticleCASPubMed Google Scholar
Imbert A, Eelkema R, Jordan S, Feiner H, Cowin P. ΔN89β-catenin induces precocious development, differentiation, and neoplasia in mammary gland. J Cell Biol. 2001;153(3):555–68. ArticleCASPubMedPubMed Central Google Scholar
Milovanovic T, Planutis K, Nguyen A, Marsh JL, Lin F, Hope C, et al. Expression of Wnt genes and frizzled 1 and 2 receptors in normal breast epithelium and infiltrating breast carcinoma. Int J Oncol. 2004;25(5):1337–42. CASPubMed Google Scholar
Ewald AJ, Brenot A, Duong M, Chan BS, Werb Z. Collective epithelial migration and cell rearrangements drive mammary branching morphogenesis. Dev Cell. 2008;14(4):570–81. ArticleCASPubMedPubMed Central Google Scholar
Prasad CP, Mirza S, Sharma G, Prashad R, DattaGupta S, Rath G, et al. Epigenetic alterations of CDH1 and APC genes: relationship with activation of Wnt/β-catenin pathway in invasive ductal carcinoma of breast. Life Sci. 2008;83(9–10):318–25. ArticleCASPubMed Google Scholar
Lindvall C, Zylstra CR, Evans N, West RA, Dykema K, Furge KA, et al. The Wnt co-receptor Lrp6 is required for normal mouse mammary gland development. PLoS One. 2009;4(6):e5813. ArticleCASPubMedPubMed Central Google Scholar
Raymond K, Cagnet S, Kreft M, Janssen H, Sonnenberg A, Glukhova MA. Control of mammary myoepithelial cell contractile function by α3β1 integrin signalling. EMBO J. 2011;30(10):1896–906. ArticleCASPubMedPubMed Central Google Scholar
Bray K, Gillette M, Young J, Loughran E, Hwang M, Sears JC, et al. Cdc42 overexpression induces hyperbranching in the developing mammary gland by enhancing cell migration. Breast Cancer Res. 2013;15(5):R91. ArticleCASPubMedPubMed Central Google Scholar
Bagci H, Laurin M, Huber J, Muller W, Cote J. Impaired cell death and mammary gland involution in the absence of Dock1 and Rac1 signaling. Cell Death Dis. 2014;5(8):e1375. ArticleCASPubMedPubMed Central Google Scholar
Van der Heyden M, Rook MB, Hermans M, Rijksen G, Boonstra J, Defize L, et al. Identification of connexin43 as a functional target for Wnt signalling. J Cell Sci. 1998;111(12):1741–9. PubMed Google Scholar
Constantinou T, Baumann F, Lacher MD, Saurer S, Friis R, Dharmarajan A. SFRP-4 abrogates Wnt-3a-induced β-catenin and Akt/PKB signalling and reverses a Wnt-3a-imposed inhibition of in vitro mammary differentiation. J Mol Signal. 2008;3(1):10. ArticleCASPubMedPubMed Central Google Scholar
Baxley SE, Jiang W, Serra R. Misexpression of wingless-related MMTV integration site 5A in mouse mammary gland inhibits the milk ejection response and regulates connexin43 phosphorylation. Biol Reprod. 2011;85(5):907–15. ArticleCASPubMedPubMed Central Google Scholar
Wang H-X, Gillio-Meina C, Chen S, Gong X-Q, Li TY, Bai D, et al. The canonical WNT2 pathway and FSH interact to regulate gap junction assembly in mouse granulosa cells. Biol Reprod. 2013;89(2):39. 1-7 ArticleCASPubMed Google Scholar
Zhai Y, Wu R, Schwartz DR, Darrah D, Reed H, Kolligs FT, et al. Role of β-catenin/T-cell factor-regulated genes in ovarian endometrioid adenocarcinomas. Am J Pathol. 2002;160(4):1229–38. ArticleCASPubMedPubMed Central Google Scholar
Ai Z, Fischer A, Spray DC, Brown AM, Fishman GI. Wnt-1 regulation of connexin43 in cardiac myocytes. J Clin Invest. 2000;105(2):161–71. ArticleCASPubMedPubMed Central Google Scholar
Mureli S, Gans CP, Bare DJ, Geenen DL, Kumar NM, Banach K. Mesenchymal stem cells improve cardiac conduction by upregulation of connexin 43 through paracrine signaling. Am J Phys Heart Circ Phys. 2012;304(4):H600–H9. Google Scholar
Kamei J, Toyofuku T, Hori M. Negative regulation of p21 by β-catenin/TCF signaling: a novel mechanism by which cell adhesion molecules regulate cell proliferation. Biochem Biophys Res Commun. 2003;312(2):380–7. ArticleCASPubMed Google Scholar
Sirnes S, Bruun J, Kolberg M, Kjenseth A, Lind GE, Svindland A, et al. Connexin43 acts as a colorectal cancer tumor suppressor and predicts disease outcome. Int J Cancer. 2012;131(3):570–81. ArticleCASPubMed Google Scholar
Yu SC, Xiao HL, Jiang XF, Wang QL, Li Y, Yang XJ, et al. Connexin 43 reverses malignant phenotypes of glioma stem cells by modulating E-cadherin. Stem Cells. 2012;30(2):108–20. ArticleCASPubMed Google Scholar
Musumeci G, Castrogiovanni P, Szychlinska MA, Aiello FC, Vecchio GM, Salvatorelli L, et al. Mammary gland: from embryogenesis to adult life. Acta Histochem. 2015;117(4–5):379–85. ArticleCASPubMed Google Scholar
Veltmaat JM, Van Veelen W, Thiery JP, Bellusci S. Identification of the mammary line in mouse by Wnt10b expression. Dev Dyn. 2004;229(2):349–56. ArticleCASPubMed Google Scholar
Gjorevski N, Nelson CM. Integrated morphodynamic signalling of the mammary gland. Nat Rev Mol Cell Biol. 2011;12(9):581. ArticleCASPubMed Google Scholar
Parsa S, Ramasamy SK, De Langhe S, Gupte VV, Haigh JJ, Medina D, et al. Terminal end bud maintenance in mammary gland is dependent upon FGFR2b signaling. Dev Biol. 2008;317(1):121–31. ArticleCASPubMed Google Scholar
Hinck L, Silberstein GB. Key stages in mammary gland development: the mammary end bud as a motile organ. Breast Cancer Res. 2005;7(6):245. ArticleCASPubMedPubMed Central Google Scholar
Atwood C, Hovey R, Glover J, Chepko G, Ginsburg E, Robison W, et al. Progesterone induces side-branching of the ductal epithelium in the mammary glands of peripubertal mice. J Endocrinol. 2000;167(1):39–52. ArticleCASPubMed Google Scholar
Brisken C. Hormonal control of alveolar development and its implications for breast carcinogenesis. J Mammary Gland Biol Neoplasia. 2002;7(1):39–48. ArticlePubMed Google Scholar
Howard BA, Gusterson BA. Human breast development. J Mammary Gland Biol Neoplasia. 2000;5(2):119–37. ArticleCASPubMed Google Scholar
Zhu J, Xiong G, Trinkle C, Xu R. Integrated extracellular matrix signaling in mammary gland development and breast cancer progression. Histol Histopathol. 2014;29(9):1083. CASPubMedPubMed Central Google Scholar
Xu R, Boudreau A, Bissell MJ. Tissue architecture and function: dynamic reciprocity via extra-and intra-cellular matrices. Cancer Metastasis Rev. 2009;28(1–2):167–76. ArticlePubMedPubMed Central Google Scholar
Talhouk RS, Bissell MJ, Werb Z. Coordinated expression of extracellular matrix-degrading proteinases and their inhibitors regulates mammary epithelial function during involution. J Cell Biol. 1992;118(5):1271–82. ArticleCASPubMed Google Scholar
Wiseman BS, Sternlicht MD, Lund LR, Alexander CM, Mott J, Bissell MJ, et al. Site-specific inductive and inhibitory activities of MMP-2 and MMP-3 orchestrate mammary gland branching morphogenesis. J Cell Biol. 2003;162(6):1123–33. ArticleCASPubMedPubMed Central Google Scholar
Dermietzel R, Hwang T, Spray D. The gap junction family: structure, function and chemistry. Anat Embryol. 1990;182(6):517–28. ArticleCASPubMed Google Scholar
Söhl G, Willecke K. Gap junctions and the connexin protein family. Cardiovasc Res. 2004;62(2):228–32. ArticleCASPubMed Google Scholar
Dbouk HA, Mroue RM, El-Sabban ME, Talhouk RS. Connexins: a myriad of functions extending beyond assembly of gap junction channels. Cell Commun Signal. 2009;7(1):4. ArticleCASPubMedPubMed Central Google Scholar
Leithe E, Mesnil M, Aasen T. The connexin 43 C-terminus: A tail of many tales. Biochim Biophys Acta. 2018;1860(1):48–64.
Kelly JJ, Simek J, Laird DW. Mechanisms linking connexin mutations to human diseases. Cell Tissue Res. 2015;360(3):701–21. ArticleCASPubMed Google Scholar
Naus CC, Laird DW. Implications and challenges of connexin connections to cancer. Nat Rev Cancer. 2010;10(6):435. ArticleCASPubMed Google Scholar
El-Saghir JA, El-Habre ET, El-Sabban ME, Talhouk RS. Connexins: a junctional crossroad to breast cancer. Int J Dev Biol. 2011;55(7-8-9):773–80. ArticlePubMed Google Scholar
Monaghan P, Clarke C, Perusinghe NP, Moss DW, Chen X-Y, Evans WH. Gap junction distribution and connexin expression in human breast. Exp Cell Res. 1996;223(1):29–38. ArticleCASPubMed Google Scholar
Jamieson S, Going JJ, D'Arcy R, George WD. Expression of gap junction proteins connexin 26 and connexin 43 in normal human breast and in breast tumours. J Pathol. 1998;184(1):37–43. ArticleCASPubMed Google Scholar
Pozzi A, Risek B, Kiang DT, Gilula NB, Kumar NM. Analysis of multiple gap junction gene products in the rodent and human mammary gland. Exp Cell Res. 1995;220(1):212–9. ArticleCASPubMed Google Scholar
Lambe T, Finlay D, Murphy M, Martin F. Differential expression of connexin 43 in mouse mammary cells. Cell Biol Int. 2006;30(5):472–9. ArticleCASPubMed Google Scholar
Reaume AG, de Sousa PA, Kulkarni S, Langille BL, Zhu D, Davies TC, et al. Cardiac malformation in neonatal mice lacking connexin43. Science. 1995;267(5205):1831–4. ArticleCASPubMed Google Scholar
Gabriel H-D, Jung D, Bützler C, Temme A, Traub O, Winterhager E, et al. Transplacental uptake of glucose is decreased in embryonic lethal connexin26-deficient mice. J Cell Biol. 1998;140(6):1453–61. ArticleCASPubMedPubMed Central Google Scholar
Stewart MK, Gong X-Q, Barr KJ, Bai D, Fishman GI, Laird DW. The severity of mammary gland developmental defects is linked to the overall functional status of Cx43 as revealed by genetically modified mice. Biochem J. 2013;449(2):401–13. ArticleCASPubMed Google Scholar
Plum A, Hallas G, Magin T, Dombrowski F, Hagendorff A, Schumacher B, et al. Unique and shared functions of different connexins in mice. Curr Biol. 2000;10(18):1083–91. ArticleCASPubMed Google Scholar
Winterhager E, Pielensticker N, Freyer J, Ghanem A, Schrickel JW, Kim J-S, et al. Replacement of connexin43 by connexin26 in transgenic mice leads to dysfunctional reproductive organs and slowed ventricular conduction in the heart. BMC Dev Biol. 2007;7(1):26. ArticleCASPubMedPubMed Central Google Scholar
Bry C, Maass K, Miyoshi K, Willecke K, Ott T, Robinson GW, et al. Loss of connexin 26 in mammary epithelium during early but not during late pregnancy results in unscheduled apoptosis and impaired development. Dev Biol. 2004;267(2):418–29. ArticleCASPubMed Google Scholar
Ormandy CJ, Naylor M, Harris J, Robertson F, Horseman ND, Lindeman GJ, et al. Investigation of the transcriptional changes underlying functional defects in the mammary glands of prolactin receptor knockout mice. Recent Prog Horm Res. 2003;58:297–324. ArticleCASPubMed Google Scholar
Mroue R, El-Sabban M, Talhouk R. Connexins and the gap in context. Integr Biol. 2011;3(4):255–66. ArticleCAS Google Scholar
Talhouk RS, Khalil AA, Bajjani R, Rahme GJ, El-Sabban ME. Gap junctions mediate STAT5-independent β-casein expression in CID-9 mammary epithelial cells. Cell Commun Adhes. 2011;18(5):104–16. ArticleCASPubMed Google Scholar
Teleki I, Szasz AM, Maros ME, Gyorffy B, Kulka J, Meggyeshazi N, et al. Correlations of differentially expressed gap junction connexins Cx26, Cx30, Cx32, Cx43 and Cx46 with breast cancer progression and prognosis. PLoS One. 2014;9(11):e112541. ArticleCASPubMedPubMed Central Google Scholar
Zardawi SJ, O'Toole SA, Sutherland RL, Musgrove EA. Dysregulation of hedgehog, Wnt and notch signalling pathways in breast cancer. Histol Histopathol. 2009;24(3):385–98. CASPubMed Google Scholar
Rao TP, Kühl M. An updated overview on Wnt signaling pathways: a prelude for more. Circ Res. 2010;106(12):1798–806. ArticleCASPubMed Google Scholar
Turashvili G, Bouchal J, Burkadze G, Kolar Z. Wnt signaling pathway in mammary gland development and carcinogenesis. Pathobiology. 2006;73(5):213–23. ArticleCASPubMed Google Scholar
Incassati A, Chandramouli A, Eelkema R, Cowin P. Key signaling nodes in mammary gland development and cancer: β-catenin. Breast Cancer Res. 2010;12(6):213. ArticleCASPubMedPubMed Central Google Scholar
Boras-Granic K, Hamel PA. Wnt-signalling in the embryonic mammary gland. J Mammary Gland Biol Neoplasia. 2013;18(2):155–63. ArticlePubMed Google Scholar
Jarde T, Dale T. Wnt signalling in murine postnatal mammary gland development. Acta Physiol. 2012;204(1):118–27. ArticleCAS Google Scholar
Cai C, Yu QC, Jiang W, Liu W, Song W, Yu H, et al. R-spondin1 is a novel hormone mediator for mammary stem cell self-renewal. Genes Dev. 2014; https://doi.org/10.1101/gad.245142.114.
Chu EY, Hens J, Andl T, Kairo A, Yamaguchi TP, Brisken C, et al. Canonical WNT signaling promotes mammary placode development and is essential for initiation of mammary gland morphogenesis. Development. 2004;131(19):4819–29. ArticleCASPubMed Google Scholar
Kouros-Mehr H, Werb Z. Candidate regulators of mammary branching morphogenesis identified by genome-wide transcript analysis. Dev Dyn. 2006;235(12):3404–12. ArticleCASPubMedPubMed Central Google Scholar
Lane TF, Leder P. Wnt-10b directs hypermorphic development and transformation in mammary glands of male and female mice. Oncogene. 1997;15(18):2133. ArticleCASPubMed Google Scholar
Weber-Hall SJ, Phippard DJ, Niemeyer CC, Dale TC. Developmental and hormonal regulation of Wnt gene expression in the mouse mammary gland. Differentiation. 1994;57(3):205–14. ArticleCASPubMed Google Scholar
Roarty K, Shore AN, Creighton CJ, Rosen JM. Ror2 regulates branching, differentiation, and actin-cytoskeletal dynamics within the mammary epithelium. J Cell Biol. 2015;208(3):351–66. ArticleCASPubMedPubMed Central Google Scholar
Ji H, Goode RJ, Vaillant F, Mathivanan S, Kapp EA, Mathias RA, et al. Proteomic profiling of secretome and adherent plasma membranes from distinct mammary epithelial cell subpopulations. Proteomics. 2011;11(20):4029–39. ArticleCASPubMed Google Scholar
Lindvall C, Evans NC, Zylstra CR, Li Y, Alexander CM, Williams BO. The Wnt signaling receptor Lrp5 is required for mammary ductal stem cell activity and Wnt1-induced tumorigenesis. J Biol Chem. 2006;281(46):35081–7. ArticleCASPubMed Google Scholar
Brisken C, Heineman A, Chavarria T, Elenbaas B, Tan J, Dey SK, et al. Essential function of Wnt-4 in mammary gland development downstream of progesterone signaling. Genes Dev. 2000;14(6):650–4. CASPubMedPubMed Central Google Scholar
Dolled-Filhart M, McCabe A, Giltnane J, Cregger M, Camp RL, Rimm DL. Quantitative in situ analysis of β-catenin expression in breast cancer shows decreased expression is associated with poor outcome. Cancer Res. 2006;66(10):5487–94. ArticleCASPubMed Google Scholar
Sørlie T, Bukholm I, Børresen-Dale A. Truncating somatic mutation in exon 15 of the APC gene is a rare event in human breast carcinomas. Mutations in brief no. 179. Online. Hum Mutat. 1998;12(3):215. PubMed Google Scholar
Schlosshauer PW, Brown SA, Eisinger K, Yan Q, Guglielminetti ER, Parsons R, et al. APC truncation and increased β-catenin levels in a human breast cancer cell line. Carcinogenesis. 2000;21(7):1453–6. ArticleCASPubMed Google Scholar
Jönsson M, Borg Å, Nilbert M, Andersson T. Involvement of adenomatous polyposis coli (APC)/β-catenin signalling in human breast cancer. Eur J Cancer. 2000;36(2):242–8. ArticlePubMed Google Scholar
Sawyer EJ, Hanby AM, Rowan AJ, Gillett CE, Thomas RE, Poulsom R, et al. The Wnt pathway, epithelial–stromal interactions, and malignant progression in phyllodes tumours. J Pathol. 2002;196(4):437–44. ArticleCASPubMed Google Scholar
Abraham SC, Reynolds C, Lee J-H, Montgomery EA, Baisden BL, Krasinskas AM, et al. Fibromatosis of the breast and mutations involving the APC/β-catenin pathway. Hum Pathol. 2002;33(1):39–46. ArticleCASPubMed Google Scholar
Ozaki S, Ikeda S, Ishizaki Y, Kurihara T, Tokumoto N, Iseki M, et al. Alterations and correlations of the components in the Wnt signaling pathway and its target genes in breast cancer. Oncol Rep. 2005;14(6):1437–43. CASPubMed Google Scholar
Hayes MJ, Thomas D, Emmons A, Giordano TJ, Kleer CG. Genetic changes of Wnt pathway genes are common events in metaplastic carcinomas of the breast. Clin Cancer Res. 2008;14(13):4038–44. ArticleCASPubMedPubMed Central Google Scholar
Huguet EL, McMahon JA, McMahon AP, Bicknell R, Harris AL. Differential expression of human Wnt genes 2, 3, 4, and 7B in human breast cell lines and normal and disease states of human breast tissue. Cancer Res. 1994;54(10):2615–21. CASPubMed Google Scholar
Lejeune S, Huguet EL, Hamby A, Poulsom R, Harris AL. Wnt5a cloning, expression, and up-regulation in human primary breast cancers. Clin Cancer Res. 1995;1(2):215–22. CASPubMed Google Scholar
Björklund P, Svedlund J, Olsson A-K, Åkerström G, Westin G. The internally truncated LRP5 receptor presents a therapeutic target in breast cancer. PLoS One. 2009;4(1):e4243. ArticleCASPubMedPubMed Central Google Scholar
Liu C-C, Prior J, Piwnica-Worms D, Bu G. LRP6 overexpression defines a class of breast cancer subtype and is a target for therapy. Proc Natl Acad Sci. 2010;107(11):5136–41. ArticlePubMed Google Scholar
Nagahata T, Shimada T, Harada A, Nagai H, Onda M, Yokoyama S, et al. Amplification, up-regulation and over-expression of DVL-1, the human counterpart of the Drosophila disheveled gene, in primary breast cancers. Cancer Sci. 2003;94(6):515–8. ArticleCASPubMed Google Scholar
Van der Auwera I, Van Laere SJ, Van den Bosch S, Van den Eynden G, Trinh B, Van Dam P, et al. Aberrant methylation of the adenomatous polyposis coli (APC) gene promoter is associated with the inflammatory breast cancer phenotype. Br J Cancer. 2008;99(10):1735. ArticleCASPubMedPubMed Central Google Scholar
Ai L, Tao Q, Zhong S, Fields CR, Kim W-J, Lee MW, et al. Inactivation of Wnt inhibitory factor-1 (WIF1) expression by epigenetic silencing is a common event in breast cancer. Carcinogenesis. 2006;27(7):1341–8. ArticleCASPubMed Google Scholar
Suzuki H, Toyota M, Caraway H, Gabrielson E, Ohmura T, Fujikane T, et al. Frequent epigenetic inactivation of Wnt antagonist genes in breast cancer. Br J Cancer. 2008;98(6):1147. ArticleCASPubMedPubMed Central Google Scholar
Shulewitz M, Soloviev I, Wu T, Koeppen H, Polakis P, Sakanaka C. Repressor roles for TCF-4 and Sfrp1 in Wnt signaling in breast cancer. Oncogene. 2006;25(31):4361. ArticleCASPubMed Google Scholar
Bivi N, Pacheco-Costa R, Brun LR, Murphy TR, Farlow NR, Robling AG, et al. Absence of Cx43 selectively from osteocytes enhances responsiveness to mechanical force in mice. J Orthop Res. 2013;31(7):1075–81. ArticleCASPubMed Google Scholar
Rinaldi F, Hartfield E, Crompton L, Badger J, Glover C, Kelly C, et al. Cross-regulation of Connexin43 and β-catenin influences differentiation of human neural progenitor cells. Cell Death Dis. 2015;5(1):e1017. ArticleCAS Google Scholar
Pacheco-Costa R, Kadakia JR, Atkinson EG, Wallace JM, Plotkin LI, Reginato RD. Connexin37 deficiency alters organic bone matrix, cortical bone geometry, and increases Wnt/β-catenin signaling. Bone. 2017;97:105–13. ArticleCASPubMed Google Scholar
Ishikawa M, Iwamoto T, Fukumoto S, Yamada Y. Pannexin 3 inhibits proliferation of osteoprogenitor cells by regulating Wnt and p21 signaling. J Biol Chem. 2014;289(5):2839–51. ArticleCASPubMed Google Scholar
Czyz J, Guan K, Zeng Q, Wobus AM. Loss of beta1 integrin function results in upregulation of connexin expression in embryonic stem cell-derived cardiomyocytes. Int J Dev Biol. 2003;49(1):33–41. ArticleCAS Google Scholar
Du W, Li J, Du W, Li J, Wang Q, Hou J, et al. Lithium chloride regulates Connexin43 in skeletal myoblasts in vitro: possible involvement in Wnt/β-Catenin signaling. Cell Commun Adhes. 2008;15(3):261–71. ArticleCASPubMed Google Scholar
Heo JS, Lee JC. β-Catenin mediates cyclic strain-stimulated cardiomyogenesis in mouse embryonic stem cells through ROS-dependent and integrin-mediated PI3K/Akt pathways. J Cell Biochem. 2011;112(7):1880–9. ArticleCASPubMed Google Scholar
Guger KA, Gumbiner BM. β-Catenin has Wnt-like activity and mimics the Nieuwkoop signaling center inXenopusDorsal–ventral patterning. Dev Biol. 1995;172(1):115–25. ArticleCASPubMed Google Scholar
Samarzija I, Sini P, Schlange T, MacDonald G, Hynes NE. Wnt3a regulates proliferation and migration of HUVEC via canonical and non-canonical Wnt signaling pathways. Biochem Biophys Res Commun. 2009;386(3):449–54. ArticleCASPubMed Google Scholar
Prunskaite-Hyyryläinen R, Shan J, Railo A, Heinonen KM, Miinalainen I, Yan W, et al. Wnt4, a pleiotropic signal for controlling cell polarity, basement membrane integrity, and antimüllerian hormone expression during oocyte maturation in the female follicle. FASEB J. 2014;28(4):1568–81. ArticleCASPubMed Google Scholar
Umazume K, Tsukahara R, Liu L, de Castro JPF, McDonald K, Kaplan HJ, et al. Role of retinal pigment epithelial cell β-catenin signaling in experimental proliferative vitreoretinopathy. Am J Pathol. 2014;184(5):1419–28. ArticleCASPubMed Google Scholar
Phillips SL, Williams CB, Zambrano JN, Williams CJ, Yeh ES. Connexin 43 in the development and progression of breast cancer: What's the connection? Int J Oncol. 2017;51(4):1005–13. ArticleCASPubMedPubMed Central Google Scholar
Banerjee D. Connexin’s connection in breast cancer growth and progression. Int J Cell Biol. 2016;2016
Komiya Y, Habas R. Wnt signal transduction pathways. Organ. 2008;4(2):68–75. Google Scholar
Segalen M, Bellaïche Y, editors. Cell division orientation and planar cell polarity pathways. Seminars in cell & developmental biology; 2009: Elsevier.
Gómez-Orte E, Sáenz-Narciso B, Moreno S, Cabello J. Multiple functions of the noncanonical Wnt pathway. Trends Genet. 2013;29(9):545–53. ArticleCASPubMed Google Scholar
Sokol SY, editor. Spatial and temporal aspects of Wnt signaling and planar cell polarity during vertebrate embryonic development. Seminars in cell & developmental biology; 2015: Elsevier.
Sedgwick AE, D’Souza-Schorey C. Wnt signaling in cell motility and invasion: drawing parallels between development and cancer. Cancers. 2016;8(9):80. ArticleCASPubMed Central Google Scholar
Dunn NR, Tolwinski NS. Ptk7 and Mcc, unfancied components in non-canonical wnt signaling and cancer. Cancers. 2016;8(7):68. ArticleCASPubMed Central Google Scholar
De A. Wnt/Ca2+ signaling pathway: a brief overview. Acta Biochim Biophys Sin. 2011;43(10):745–56. ArticleCASPubMed Google Scholar
Green J, Nusse R, van Amerongen R. The role of Ryk and Ror receptor tyrosine kinases in Wnt signal transduction. Cold Spring Harbor Perspect Biol. 2013; https://doi.org/10.1101/cshperspect.a009175.
Angers S, Moon RT. Proximal events in Wnt signal transduction. Nat Rev Mol Cell Biol. 2009;10(7):468. ArticleCASPubMed Google Scholar
Debebe Z, Rathmell WK. Ror2 as a therapeutic target in cancer. Pharmacol Ther. 2015;150:143–8. ArticleCASPubMed Google Scholar
Clark CE, Nourse CC, Cooper HM. The tangled web of non-canonical Wnt signalling in neural migration. Neurosignals. 2012;20(3):202–20. ArticleCASPubMed Google Scholar
Schlessinger K, Hall A, Tolwinski N. Wnt signaling pathways meet Rho GTPases. Genes Dev. 2009;23(3):265–77. ArticleCASPubMed Google Scholar
Hanna S, El-Sibai M. Signaling networks of Rho GTPases in cell motility. Cell Signal. 2013;25(10):1955–61. ArticleCASPubMed Google Scholar
Mack NA, Georgiou M. The interdependence of the Rho GTPases and apicobasal cell polarity. Small GTPases. 2014;5(2):e973768. ArticlePubMed Central Google Scholar
Burbelo P, Wellstein A, Pestell RG. Altered Rho GTPase signaling pathways in breast cancer cells. Breast Cancer Res Treat. 2004;84(1):43–8. ArticleCASPubMed Google Scholar
Zuo Y, Oh W, Ulu A, Frost JA. Minireview: mouse models of Rho GTPase function in mammary gland development, tumorigenesis, and metastasis. Mol Endocrinol. 2016;30(3):278–89. ArticleCASPubMed Google Scholar
Bray K, Brakebusch C, Vargo-Gogola T. The Rho GTPase Cdc42 is required for primary mammary epithelial cell morphogenesis in vitro. Small GTPases. 2011;2(5):247–58. ArticlePubMedPubMed Central Google Scholar
Druso JE, Endo M, Lin M-CJ, Peng X, Antonyak MA, Meller S, et al. An essential role for Cdc42 in the functioning of the adult mammary gland. J Biol Chem. 2016;291(17):8886–95. ArticleCASPubMedPubMed Central Google Scholar
Ahn S-J, Chung K-W, Lee R-A, Park I-A, Lee S-H, Park DE, et al. Overexpression of βPix-a in human breast cancer tissues. Cancer Lett. 2003;193(1):99–107. ArticleCASPubMed Google Scholar
Lane J, Martin TA, Mansel RE, Jiang WG, editors. The expression and prognostic value of the guanine nucleotide exchange factors (GEFs) Trio, Vav1 and TIAM-1 in human breast cancer. International Seminars in Surgical Oncology; 2008: BioMed Central.
Hanna S, Khalil B, Nasrallah A, Saykali BA, Sobh R, Nasser S, et al. StarD13 is a tumor suppressor in breast cancer that regulates cell motility and invasion. Int J Oncol. 2014;44(5):1499–511. ArticleCASPubMedPubMed Central Google Scholar
El-Sibai M, Pertz O, Pang H, Yip S-C, Lorenz M, Symons M, et al. RhoA/ROCK-mediated switching between Cdc42-and Rac1-dependent protrusion in MTLn3 carcinoma cells. Exp Cell Res. 2008;314(7):1540–52. ArticleCASPubMedPubMed Central Google Scholar
El-Sibai M, Nalbant P, Pang H, Flinn RJ, Sarmiento C, Macaluso F, et al. Cdc42 is required for EGF-stimulated protrusion and motility in MTLn3 carcinoma cells. J Cell Sci. 2007;120(19):3465–74. ArticleCASPubMedPubMed Central Google Scholar
Pillé J-Y, Denoyelle C, Varet J, Bertrand J-R, Soria J, Opolon P, et al. Anti-RhoA and anti-RhoC siRNAs inhibit the proliferation and invasiveness of MDA-MB-231 breast cancer cells in vitro and in vivo. Mol Ther. 2005;11(2):267–74. ArticleCASPubMed Google Scholar
Wyckoff JB, Pinner SE, Gschmeissner S, Condeelis JS, Sahai E. ROCK-and myosin-dependent matrix deformation enables protease-independent tumor-cell invasion in vivo. Curr Biol. 2006;16(15):1515–23. ArticleCASPubMed Google Scholar
Bravo-Cordero JJ, Sharma VP, Roh-Johnson M, Chen X, Eddy R, Condeelis J, et al. Spatial regulation of RhoC activity defines protrusion formation in migrating cells. J Cell Sci. 2013; https://doi.org/10.1242/jcs.123547.
Bravo-Cordero JJ, Oser M, Chen X, Eddy R, Hodgson L, Condeelis J. A novel spatiotemporal RhoC activation pathway locally regulates cofilin activity at invadopodia. Curr Biol. 2011;21(8):635–44. ArticleCASPubMedPubMed Central Google Scholar
Moshfegh Y, Bravo-Cordero JJ, Miskolci V, Condeelis J, Hodgson L. A Trio–Rac1–Pak1 signalling axis drives invadopodia disassembly. Nat Cell Biol. 2014;16(6):571. ArticleCAS Google Scholar
Yip S-C, El-Sibai M, Coniglio SJ, Mouneimne G, Eddy RJ, Drees BE, et al. The distinct roles of Ras and Rac in PI 3-kinase-dependent protrusion during EGF-stimulated cell migration. J Cell Sci. 2007;120(17):3138–46. ArticleCASPubMedPubMed Central Google Scholar
Zhao X, Lu L, Pokhriyal N, Ma H, Duan L, Lin S, et al. Overexpression of RhoA induces preneoplastic transformation of primary mammary epithelial cells. Cancer Res. 2009;69(2):483–91. ArticleCASPubMedPubMed Central Google Scholar
Chan C-H, Lee S-W, Li C-F, Wang J, Yang W-L, Wu C-Y, et al. Deciphering the transcriptional complex critical for RhoA gene expression and cancer metastasis. Nat Cell Biol. 2010;12(5):457. ArticleCASPubMed Google Scholar
Castillo-Pichardo L, Humphries-Bickley T, De La Parra C, Forestier-Roman I, Martinez-Ferrer M, Hernandez E, et al. The Rac inhibitor EHop-016 inhibits mammary tumor growth and metastasis in a nude mouse model. Transl Oncol. 2014;7(5):546–55. ArticlePubMedPubMed Central Google Scholar
Citi S, Guerrera D, Spadaro D, Shah J. Epithelial junctions and Rho family GTPases: the zonular signalosome. Small GTPases. 2014;5(4):e973760. ArticleCASPubMed Central Google Scholar
Yagi S, Matsuda M, Kiyokawa E. Suppression of Rac1 activity at the apical membrane of MDCK cells is essential for cyst structure maintenance. EMBO Rep. 2012;13(3):237–43. ArticleCASPubMedPubMed Central Google Scholar
Timmerman I, Heemskerk N, Kroon J, Schaefer A, van Rijssel J, Hoogenboezem M, et al. A local VE-cadherin and trio-based signaling complex stabilizes endothelial junctions through Rac1. J Cell Sci. 2015;128(16):3041–54. ArticleCASPubMed Google Scholar
K-i K, Melendez J, Baumann JM, Leslie JR, Chauhan BK, Nemkul N, et al. Loss of RhoA in neural progenitor cells causes the disruption of adherens junctions and hyperproliferation. Proc Natl Acad Sci. 2011;108(18):7607–12. Article Google Scholar
Herder C, Swiercz JM, Müller C, Peravali R, Quiring R, Offermanns S, et al. ArhGEF18 regulates RhoA-Rock2 signaling to maintain neuro-epithelial apico-basal polarity and proliferation. Development. 2013;140(13):2787–97. ArticleCASPubMed Google Scholar
Wu X, Li S, Chrostek-Grashoff A, Czuchra A, Meyer H, Yurchenco PD, et al. Cdc42 is crucial for the establishment of epithelial polarity during early mammalian development. Dev Dyn. 2007;236(10):2767–78. ArticleCASPubMed Google Scholar
Wei L, Taffet GE, Khoury DS, Bo J, Li Y, Yatani A, et al. Disruption of Rho signaling results in progressive atrioventricular conduction defects while ventricular function remains preserved. FASEB J. 2004;18(7):857–9. ArticleCASPubMed Google Scholar
Maddala R, Deng P-F, Costello JM, Wawrousek EF, Zigler JS, Rao VP. Impaired cytoskeletal organization and membrane integrity in lens fibers of a Rho GTPase functional knockout transgenic mouse. Lab Investig. 2004;84(6):679. ArticleCASPubMed Google Scholar
Wang L, Liu S, Zhang H, Hu S, Wei Y. RhoA activity increased in myocardium of arrhythmogenic cardiomyopathy patients and affected connexin 43 protein expression in HL-1 cells. Int J Clin Exp Med. 2015;8(8):12906. CASPubMedPubMed Central Google Scholar
Matsuda T, Fujio Y, Nariai T, Ito T, Yamane M, Takatani T, et al. N-cadherin signals through Rac1 determine the localization of connexin 43 in cardiac myocytes. J Mol Cell Cardiol. 2006;40(4):495–502. ArticleCASPubMed Google Scholar
Van Hengel J, D’Hooge P, Hooghe B, Wu X, Libbrecht L, De Vos R, et al. Continuous cell injury promotes hepatic tumorigenesis in cdc42-deficient mouse liver. Gastroenterology. 2008;134(3):781–92. ArticleCASPubMed Google Scholar
Anderson SC, Stone C, Tkach L, SundarRaj N. Rho and Rho-kinase (ROCK) signaling in adherens and gap junction assembly in corneal epithelium. Invest Ophthalmol Vis Sci. 2002;43(4):978–86. PubMed Google Scholar
Derangeon M, Bourmeyster N, Plaisance I, Pinet-Charvet C, Chen Q, Duthe F, et al. RhoA GTPase and F-actin dynamically regulate the permeability of Cx43-made channels in rat cardiac myocytes. J Biol Chem. 2008;283(45):30754–65. ArticleCASPubMedPubMed Central Google Scholar
Geletu M, Guy S, Greer S, Raptis L. Differential effects of polyoma virus middle tumor antigen mutants upon gap junctional, intercellular communication. Exp Cell Res. 2015;336(2):223–31. ArticleCASPubMed Google Scholar
Ito S, Ito Y, Senga T, Hattori S, Matsuo S, Hamaguchi M. v-Src requires Ras signaling for the suppression of gap junctional intercellular communication. Oncogene. 2006;25(16):2420. ArticleCASPubMed Google Scholar
Stains JP, Civitelli R. Gap junctions regulate extracellular signal-regulated kinase signaling to affect gene transcription. Mol Biol Cell. 2005;16(1):64–72. ArticleCASPubMedPubMed Central Google Scholar
Somekawa S, Fukuhara S, Nakaoka Y, Fujita H, Saito Y, Mochizuki N. Enhanced functional gap junction neoformation by protein kinase A–dependent and Epac-dependent signals downstream of cAMP in cardiac myocytes. Circ Res. 2005;97(7):655–62. ArticleCASPubMed Google Scholar
Hayashi T, Nomata K, Chang C-C, Ruch RJ, Trosko JE. Cooperative effects of v-myc and c-Ha-ras oncogenes on gap junctional intercellular communication and tumorigenicity in rat liver epithelial cells. Cancer Lett. 1998;128(2):145–54. ArticleCASPubMed Google Scholar
Chen X, Shuzo O, Li Y, Han R. Effect of d-limonene, Salvia miltiorrhiza and turmeric derivatives on membrane association of Ras gene product and gap junction intercellular communication. Yao xue xue bao= Acta Pharmaceutica Sinica. 1998;33(11):821–7.
Brownell HL, Whitfield JF, Raptis L. Cellular Ras partly mediates gap junction closure by the polyoma virus middle tumor antigen. Cancer Lett. 1996;103(1):99–106. ArticleCASPubMed Google Scholar
Brownell HL, Whitfield JF, Raptis L. Elimination of intercellular junctional communication requires lower Ras (leu61) levels than stimulation of anchorage-independent proliferation. Cancer Detect Prev. 1997;21(4):289–94. CASPubMed Google Scholar
Brownell HL, Narsimhan RP, Corbley MJ, Mann VM, Whitfield JF, Raptis L. Ras is involved in gap junction closure in proliferating fibroblasts or preadipocytes but not in differentiated adipocytes. DNA Cell Biol. 1996;15(6):443–51. ArticleCASPubMed Google Scholar
Zhang J, Yang G-M, Zhu Y, Peng X-Y, Liu L-M, Li T. Bradykinin induces vascular contraction after hemorrhagic shock in rats. J Surg Res. 2015;193(1):334–43. ArticleCASPubMed Google Scholar
Sin W-C, Tse M, Planque N, Perbal B, Lampe PD, Naus CC. Matricellular protein CCN3 (NOV) regulates actin cytoskeleton reorganization. J Biol Chem. 2009;284(43):29935–44. ArticleCASPubMedPubMed Central Google Scholar
Liu X, Hashimoto-Torii K, Torii M, Ding C, Rakic P. Gap junctions/hemichannels modulate interkinetic nuclear migration in the forebrain precursors. J Neurosci. 2010;30(12):4197–209. ArticleCASPubMedPubMed Central Google Scholar
Mendoza-Naranjo A, Cormie P, Serrano AE, Hu R, O'Neill S, Wang CM, et al. Targeting Cx43 and N-cadherin, which are abnormally upregulated in venous leg ulcers, influences migration, adhesion and activation of Rho GTPases. PLoS One. 2012;7(5):e37374. ArticleCASPubMedPubMed Central Google Scholar
Machtaler S, Choi K, Dang-Lawson M, Falk L, Pournia F, Naus CC, et al. The role of the gap junction protein connexin43 in B lymphocyte motility and migration. FEBS Lett. 2014;588(8):1249–58. ArticleCASPubMed Google Scholar
Machtaler S, Dang-Lawson M, Choi K, Jang C, Naus CC, Matsuuchi L. The gap junction protein Cx43 regulates B-lymphocyte spreading and adhesion. J Cell Sci. 2011;124(15):2611–21. ArticleCASPubMed Google Scholar