Skip to main content
Log in

The contribution of adhesion signaling to lactogenesis

  • Review
  • Published:
Journal of Cell Communication and Signaling Aims and scope

Abstract

The mammary gland undergoes hormonally controlled cycles of pubertal maturation, pregnancy, lactation, and involution, and these processes rely on complex signaling mechanisms, many of which are controlled by cell–cell and cell–matrix adhesion. The adhesion of epithelial cells to the extracellular matrix initiates signaling mechanisms that have an impact on cell proliferation, survival, and differentiation throughout lactation. The control of integrin expression on the mammary epithelial cells, the composition of the extracellular matrix and the presence of secreted matricellular proteins all contribute to essential adhesion signaling during lactogenesis. In vitro and in vivo studies, including the results from genetically engineered mice, have shed light on the regulation of these processes at the cell and tissue level and have led to increased understanding of the essential signaling components that are regulated in temporal and cell specific manner during lactogenesis. Recent studies suggest that a secreted matricellular protein, CTGF/CCN2, may play a role in lactogenic differentiation through binding to β1 integrin complexes, enhancing the production of extracellular matrix components and contributions to cell adhesion signaling.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Abreu JG, Ketpura NI et al (2002) Connective-tissue growth factor (CTGF) modulates cell signalling by BMP and TGF-beta. Nat Cell Biol 4(8):599–604

    CAS  PubMed  Google Scholar 

  • Akhtar N, Streuli CH (2006) Rac1 links integrin-mediated adhesion to the control of lactational differentiation in mammary epithelia. J Cell Biol 173(5):781–793

    Article  CAS  PubMed  Google Scholar 

  • Akhtar N, Marlow R et al (2009) Molecular dissection of integrin signalling proteins in the control of mammary epithelial development and differentiation. Development 136(6):1019–1027

    Article  CAS  PubMed  Google Scholar 

  • Atwood CS, Hovey RC et al (2000) Progesterone induces side-branching of the ductal epithelium in the mammary glands of peripubertal mice. J Endocrinol 167(1):39–52

    Article  CAS  PubMed  Google Scholar 

  • Babic AM, Chen CC et al (1999) Fisp12/mouse connective tissue growth factor mediates endothelial cell adhesion and migration through integrin alphavbeta3, promotes endothelial cell survival, and induces angiogenesis in vivo. Mol Cell Biol 19(4):2958–2966

    CAS  PubMed  Google Scholar 

  • Ball DK, Rachfal AW et al (2003) The heparin-binding 10 kDa fragment of connective tissue growth factor (CTGF) containing module 4 alone stimulates cell adhesion. J Endocrinol 176(2):R1–R7

    Article  CAS  PubMed  Google Scholar 

  • Barcellos-Hoff MH, Aggeler J et al (1989) Functional differentiation and alveolar morphogenesis of primary mammary cultures on reconstituted basement membrane. Development 105(2):223–235

    CAS  PubMed  Google Scholar 

  • Blakely CM, Stoddard AJ et al (2006) Hormone-induced protection against mammary tumorigenesis is conserved in multiple rat strains and identifies a core gene expression signature induced by pregnancy. Cancer Res 66(12):6421–6431

    Article  CAS  PubMed  Google Scholar 

  • Blom IE, van Dijk AJ et al (2001) In vitro evidence for differential involvement of CTGF, TGFbeta, and PDGF-BB in mesangial response to injury. Nephrol Dial Transplant 16(6):1139–1148

    Article  CAS  PubMed  Google Scholar 

  • Bonnette SG, Hadsell DL (2001) Targeted disruption of the IGF-I receptor gene decreases cellular proliferation in mammary terminal end buds. Endocrinology 142(11):4937–4945

    Article  CAS  PubMed  Google Scholar 

  • Bork P (1993) The modular architecture of a new family of growth regulators related to connective tissue growth factor. FEBS Lett 327(2):125–130

    Article  CAS  PubMed  Google Scholar 

  • Bouchard V, Demers MJ et al (2007) Fak/Src signaling in human intestinal epithelial cell survival and anoikis: differentiation state-specific uncoupling with the PI3-K/Akt-1 and MEK/Erk pathways. J Cell Physiol 212(3):717–728

    Article  CAS  PubMed  Google Scholar 

  • Boxer RB, Stairs DB et al (2006) Isoform-specific requirement for Akt1 in the developmental regulation of cellular metabolism during lactation. Cell Metab 4(6):475–490

    Article  CAS  PubMed  Google Scholar 

  • Bradham DM, Igarashi A et al (1991) Connective tissue growth factor: a cysteine-rich mitogen secreted by human vascular endothelial cells is related to the SRC-induced immediate early gene product CEF-10. J Cell Biol 114(6):1285–1294

    Article  CAS  PubMed  Google Scholar 

  • Brigstock DR (2003) The CCN family: a new stimulus package. J Endocrinol 178(2):169–175

    Article  CAS  PubMed  Google Scholar 

  • Brigstock D, Lau L et al (2005) Report and abstracts of the 3rd International Workshop on the CCN Family of Genes. St Malo, France, 20–23 October 2004. J Clin Pathol 58(5):463–478

    Article  CAS  PubMed  Google Scholar 

  • Brisken C, Kaur S et al (1999) Prolactin controls mammary gland development via direct and indirect mechanisms. Dev Biol 210(1):96–106

    Article  CAS  PubMed  Google Scholar 

  • Brisken C, Socolovsky M et al (2002) The signaling domain of the erythropoietin receptor rescues prolactin receptor-mutant mammary epithelium. Proc Natl Acad Sci USA 99(22):14241–14245

    Article  CAS  PubMed  Google Scholar 

  • Cabodi S, Tinnirello A et al (2006) p130Cas as a new regulator of mammary epithelial cell proliferation, survival, and HER2-neu oncogene-dependent breast tumorigenesis. Cancer Res 66(9):4672–4680

    Article  CAS  PubMed  Google Scholar 

  • Chen CC, Lau LF (2009) Functions and mechanisms of action of CCN matricellular proteins. Int J Biochem Cell Biol 41(4):771–783

    Google Scholar 

  • Chen CC, Chen N et al (2001) The angiogenic factors Cyr61 and connective tissue growth factor induce adhesive signaling in primary human skin fibroblasts. J Biol Chem 276(13):10443–10452

    Article  CAS  PubMed  Google Scholar 

  • Chen Y, Blom IE et al (2002) CTGF expression in mesangial cells: involvement of SMADs, MAP kinase, and PKC. Kidney Int 62(4):1149–1159

    Article  CAS  PubMed  Google Scholar 

  • Chen Y, Abraham DJ et al (2004) CCN2 (connective tissue growth factor) promotes fibroblast adhesion to fibronectin. Mol Biol Cell 15(12):5635–5646

    Article  CAS  PubMed  Google Scholar 

  • Crean JK, Finlay D et al (2002) The role of p42/44 MAPK and protein kinase B in connective tissue growth factor induced extracellular matrix protein production, cell migration, and actin cytoskeletal rearrangement in human mesangial cells. J Biol Chem 277(46):44187–44194

    Article  CAS  PubMed  Google Scholar 

  • Debnath J, Brugge JS (2005) Modelling glandular epithelial cancers in three-dimensional cultures. Nat Rev Cancer 5(9):675–688

    Article  CAS  PubMed  Google Scholar 

  • Doppler W, Welte T et al (1995) CCAAT/enhancer-binding protein isoforms beta and delta are expressed in mammary epithelial cells and bind to multiple sites in the beta-casein gene promoter. J Biol Chem 270(30):17962–17969

    Article  CAS  PubMed  Google Scholar 

  • Faraldo MM, Deugnier MA et al (2001) Growth defects induced by perturbation of beta1-integrin function in the mammary gland epithelium result from a lack of MAPK activation via the Shc and Akt pathways. EMBO Rep 2(5):431–437

    CAS  PubMed  Google Scholar 

  • Faraldo MM, Deugnier MA et al (2002) Perturbation of beta1-integrin function in involuting mammary gland results in premature dedifferentiation of secretory epithelial cells. Mol Biol Cell 13(10):3521–3531

    Article  CAS  PubMed  Google Scholar 

  • Farrelly N, Lee YJ et al (1999) Extracellular matrix regulates apoptosis in mammary epithelium through a control on insulin signaling. J Cell Biol 144(6):1337–1348

    Article  CAS  PubMed  Google Scholar 

  • Forde N, Spencer TE et al (2010) Effect of pregnancy and progesterone concentration on expression of genes encoding for transporters or secreted proteins in the bovine endometrium. Physiol Genomics 41(1):53–62

    Article  CAS  PubMed  Google Scholar 

  • Frazier K, Williams S et al (1996) Stimulation of fibroblast cell growth, matrix production, and granulation tissue formation by connective tissue growth factor. J Invest Dermatol 107(3):404–411

    Article  CAS  PubMed  Google Scholar 

  • Frisch SM, Francis H (1994) Disruption of epithelial cell–matrix interactions induces apoptosis. J Cell Biol 124(4):619–626

    Article  CAS  PubMed  Google Scholar 

  • Gallego MI, Binart N et al (2001) Prolactin, growth hormone, and epidermal growth factor activate Stat5 in different compartments of mammary tissue and exert different and overlapping developmental effects. Dev Biol 229(1):163–175

    Article  CAS  PubMed  Google Scholar 

  • Geiger B, Bershadsky A et al (2001) Transmembrane crosstalk between the extracellular matrix–cytoskeleton crosstalk. Nat Rev Mol Cell Biol 2(11):793–805

    Article  CAS  PubMed  Google Scholar 

  • Gilmore AP (2005) Anoikis. Cell Death Differ 12(Suppl 2):1473–1477

    Article  CAS  PubMed  Google Scholar 

  • Gilmore AP, Metcalfe AD et al (2000) Integrin-mediated survival signals regulate the apoptotic function of Bax through its conformation and subcellular localization. J Cell Biol 149(2):431–446

    Article  CAS  PubMed  Google Scholar 

  • Graness A, Cicha I et al (2006a) Contribution of Src-FAK signaling to the induction of connective tissue growth factor in renal fibroblasts. Kidney Int 69(8):1341–1349

    CAS  PubMed  Google Scholar 

  • Graness A, Giehl K et al (2006b) Differential involvement of the integrin-linked kinase (ILK) in RhoA-dependent rearrangement of F-actin fibers and induction of connective tissue growth factor (CTGF). Cell Signal 18(4):433–440

    Article  CAS  PubMed  Google Scholar 

  • Grzeszkiewicz TM, Kirschling DJ et al (2001) CYR61 stimulates human skin fibroblast migration through Integrin alpha vbeta 5 and enhances mitogenesis through integrin alpha vbeta 3, independent of its carboxyl-terminal domain. J Biol Chem 276(24):21943–21950

    Article  CAS  PubMed  Google Scholar 

  • Hishikawa K, Oemar BS et al (2001) Static pressure regulates connective tissue growth factor expression in human mesangial cells. J Biol Chem 276(20):16797–16803

    Article  CAS  PubMed  Google Scholar 

  • Hobbs AA, Richards DA et al (1982) Complex hormonal regulation of rat casein gene expression. J Biol Chem 257(7):3598–3605

    CAS  PubMed  Google Scholar 

  • Hoshijima M, Hattori T et al (2006) CT domain of CCN2/CTGF directly interacts with fibronectin and enhances cell adhesion of chondrocytes through integrin alpha5beta1. FEBS Lett 580(5):1376–1382

    Article  CAS  PubMed  Google Scholar 

  • Humphreys RC, Lydon JP et al (1997) Use of PRKO mice to study the role of progesterone in mammary gland development. J Mammary Gland Biol Neoplasia 2(4):343–354

    Article  CAS  PubMed  Google Scholar 

  • Ivkovic S, Yoon BS et al (2003) Connective tissue growth factor coordinates chondrogenesis and angiogenesis during skeletal development. Development 130(12):2779–2791

    Article  CAS  PubMed  Google Scholar 

  • Jiang J, Levine M (1993) Binding affinities and cooperative interactions with bHLH activators delimit threshold responses to the dorsal gradient morphogen. Cell 72(5):741–752

    Article  CAS  PubMed  Google Scholar 

  • Jolivet G, Pantano T et al (2005) Regulation by the extracellular matrix (ECM) of prolactin-induced alpha s1-casein gene expression in rabbit primary mammary cells: role of STAT5, C/EBP, and chromatin structure. J Cell Biochem 95(2):313–327

    Article  CAS  PubMed  Google Scholar 

  • Kennedy L, Liu S et al (2007) CCN2 is necessary for the function of mouse embryonic fibroblasts. Exp Cell Res 313(5):952–964

    Article  CAS  PubMed  Google Scholar 

  • Kim H, Laing M et al (2005) c-Src-null mice exhibit defects in normal mammary gland development and ERalpha signaling. Oncogene 24(36):5629–5636

    Article  CAS  PubMed  Google Scholar 

  • Kireeva ML, Latinkic BV et al (1997) Cyr61 and Fisp12 are both ECM-associated signaling molecules: activities, metabolism, and localization during development. Exp Cell Res 233(1):63–77

    Article  CAS  PubMed  Google Scholar 

  • Klinowska TC, Alexander CM et al (2001) Epithelial development and differentiation in the mammary gland is not dependent on alpha 3 or alpha 6 integrin subunits. Dev Biol 233(2):449–467

    Article  CAS  PubMed  Google Scholar 

  • Kouros-Mehr H, Slorach EM et al (2006) GATA-3 maintains the differentiation of the luminal cell fate in the mammary gland. Cell 127(5):1041–1055

    Article  CAS  PubMed  Google Scholar 

  • Kubota S, Takigawa M (2007) CCN family proteins and angiogenesis: from embryo to adulthood. Angiogenesis 10(1):1–11

    Article  CAS  PubMed  Google Scholar 

  • Lau LF, Lam SC (1999) The CCN family of angiogenic regulators: the integrin connection. Exp Cell Res 248(1):44–57

    Article  CAS  PubMed  Google Scholar 

  • Lechner J, Welte T et al (1997) Promoter-dependent synergy between glucocorticoid receptor and Stat5 in the activation of beta-casein gene transcription. J Biol Chem 272(33):20954–20960

    Article  CAS  PubMed  Google Scholar 

  • Lee YJ, Streuli CH (1999) Extracellular matrix selectively modulates the response of mammary epithelial cells to different soluble signaling ligands. J Biol Chem 274(32):22401–22408

    Article  CAS  PubMed  Google Scholar 

  • Lee YJ, Hsu TC et al (2009) Extracellular matrix controls insulin signaling in mammary epithelial cells through the RhoA/Rok pathway. J Cell Physiol 220(2):476–484

    Article  CAS  PubMed  Google Scholar 

  • Leu SJ, Lam SC et al (2002) Pro-angiogenic activities of CYR61 (CCN1) mediated through integrins alphavbeta3 and alpha6beta1 in human umbilical vein endothelial cells. J Biol Chem 277(48):46248–46255

    Article  CAS  PubMed  Google Scholar 

  • Leu SJ, Liu Y et al (2003) Identification of a novel integrin alpha 6 beta 1 binding site in the angiogenic inducer CCN1 (CYR61). J Biol Chem 278(36):33801–33808

    Article  CAS  PubMed  Google Scholar 

  • Li N, Zhang Y et al (2005) Beta1 integrins regulate mammary gland proliferation and maintain the integrity of mammary alveoli. EMBO J 24(11):1942–1953

    Article  CAS  PubMed  Google Scholar 

  • Lin CG, Leu SJ et al (2003) CCN3 (NOV) is a novel angiogenic regulator of the CCN protein family. J Biol Chem 278(26):24200–24208

    Article  CAS  PubMed  Google Scholar 

  • Lin CG, Chen CC et al (2005) Integrin-dependent functions of the angiogenic inducer NOV (CCN3): implication in wound healing. J Biol Chem 280(9):8229–8237

    Article  CAS  PubMed  Google Scholar 

  • Lindberg K, Strom A et al (2010) Expression of estrogen receptor beta increases integrin alpha1 and integrin beta1 levels and enhances adhesion of breast cancer cells. J Cell Physiol 222(1):156–167

    Article  CAS  PubMed  Google Scholar 

  • Liu X, Robinson GW et al (1997) Stat5a is mandatory for adult mammary gland development and lactogenesis. Genes Dev 11(2):179–186

    Article  CAS  PubMed  Google Scholar 

  • Liu K, Cheng L et al (2010) Conditional knockout of fibronectin abrogates mouse mammary gland lobuloalveolar differentiation. Dev Biol 346(1)11–24

    Google Scholar 

  • Luo M, Fan H et al (2009) Mammary epithelial-specific ablation of the focal adhesion kinase suppresses mammary tumorigenesis by affecting mammary cancer stem/progenitor cells. Cancer Res 69(2):466–474

    Article  CAS  PubMed  Google Scholar 

  • Maroulakou IG, Oemler W et al (2008) Distinct roles of the three Akt isoforms in lactogenic differentiation and involution. J Cell Physiol 217(2):468–477

    Article  CAS  PubMed  Google Scholar 

  • McManaman JL, Palmer CA et al (2004) Regulation of milk lipid formation and secretion in the mouse mammary gland. Adv Exp Med Biol 554:263–279

    CAS  PubMed  Google Scholar 

  • Meier VS, Groner B (1994) The nuclear factor YY1 participates in repression of the beta-casein gene promoter in mammary epithelial cells and is counteracted by mammary gland factor during lactogenic hormone induction. Mol Cell Biol 14(1):128–137

    CAS  PubMed  Google Scholar 

  • Mercurio AM (1995) Laminin receptors: achieving specificity through cooperation. Trends Cell Biol 5(11):419–423

    Article  CAS  PubMed  Google Scholar 

  • Mo FE, Lau LF (2006) The matricellular protein CCN1 is essential for cardiac development. Circ Res 99(9):961–969

    Article  CAS  PubMed  Google Scholar 

  • Mo FE, Muntean AG et al (2002) CYR61 (CCN1) is essential for placental development and vascular integrity. Mol Cell Biol 22(24):8709–8720

    Article  CAS  PubMed  Google Scholar 

  • Morgan MR, Humphries MJ et al (2007) Synergistic control of cell adhesion by integrins and syndecans. Nat Rev Mol Cell Biol 8(12):957–969

    Article  CAS  PubMed  Google Scholar 

  • Mori T, Kawara S et al (1999) Role and interaction of connective tissue growth factor with transforming growth factor-beta in persistent fibrosis: a mouse fibrosis model. J Cell Physiol 181(1):153–159

    Article  CAS  PubMed  Google Scholar 

  • Morrison BL, Jose CC et al (2010) Connective tissue growth factor (CTGF/CCN2) enhances lactogenic differentiation of mammary epithelial cells via integrin-mediated cell adhesion. BMC Cell Biol 11:35

    PubMed  Google Scholar 

  • Muschler J, Lochter A et al (1999) Division of labor among the alpha6beta4 integrin, beta1 integrins, and an E3 laminin receptor to signal morphogenesis and beta-casein expression in mammary epithelial cells. Mol Biol Cell 10(9):2817–2828

    CAS  PubMed  Google Scholar 

  • Myers CA, Schmidhauser C et al (1998) Characterization of BCE-1, a transcriptional enhancer regulated by prolactin and extracellular matrix and modulated by the state of histone acetylation. Mol Cell Biol 18(4):2184–2195

    CAS  PubMed  Google Scholar 

  • Nagy T, Wei H et al (2007) Mammary epithelial-specific deletion of the focal adhesion kinase gene leads to severe lobulo-alveolar hypoplasia and secretory immaturity of the murine mammary gland. J Biol Chem 282(43):31766–31776

    Article  CAS  PubMed  Google Scholar 

  • Naylor MJ, Li N et al (2005) Ablation of beta1 integrin in mammary epithelium reveals a key role for integrin in glandular morphogenesis and differentiation. J Cell Biol 171(4):717–728

    Article  CAS  PubMed  Google Scholar 

  • Neville MC, McFadden TB et al (2002) Hormonal regulation of mammary differentiation and milk secretion. J Mammary Gland Biol Neoplasia 7(1):49–66

    Article  PubMed  Google Scholar 

  • Oakes SR, Hilton HN et al (2006) The alveolar switch: coordinating the proliferative cues and cell fate decisions that drive the formation of lobuloalveoli from ductal epithelium. Breast Cancer Res 8(2):207

    Article  PubMed  CAS  Google Scholar 

  • Perbal B (2004) CCN proteins: multifunctional signalling regulators. Lancet 363(9402):62–64

    Article  CAS  PubMed  Google Scholar 

  • Plaut K, Maple R et al (1999) Progesterone stimulates DNA synthesis and lobulo-alveolar development in mammary glands in ovariectomized mice. J Cell Physiol 180(2):298–304

    Article  CAS  PubMed  Google Scholar 

  • Prince JM, Klinowska TC et al (2002) Cell–matrix interactions during development and apoptosis of the mouse mammary gland in vivo. Dev Dyn 223(4):497–516

    Article  CAS  PubMed  Google Scholar 

  • Pullan S, Wilson J et al (1996) Requirement of basement membrane for the suppression of programmed cell death in mammary epithelium. J Cell Sci 109(Pt 3):631–642

    CAS  PubMed  Google Scholar 

  • Raught B, Khursheed B et al (1994) YY1 represses beta-casein gene expression by preventing the formation of a lactation-associated complex. Mol Cell Biol 14(3):1752–1763

    CAS  PubMed  Google Scholar 

  • Raught B, Liao WS et al (1995) Developmentally and hormonally regulated CCAAT/enhancer-binding protein isoforms influence beta-casein gene expression. Mol Endocrinol 9(9):1223–1232

    Article  CAS  PubMed  Google Scholar 

  • Rijnkels M, Wheeler DA et al (1997) Structure and expression of the mouse casein gene locus. Mamm Genome 8(1):9–15

    Article  CAS  PubMed  Google Scholar 

  • Robinson GW, Johnson PF et al (1998) The C/EBPbeta transcription factor regulates epithelial cell proliferation and differentiation in the mammary gland. Genes Dev 12(12):1907–1916

    Article  CAS  PubMed  Google Scholar 

  • Roskelley CD, Srebrow A et al (1995) A hierarchy of ECM-mediated signalling regulates tissue-specific gene expression. Curr Opin Cell Biol 7(5):736–747

    Article  CAS  PubMed  Google Scholar 

  • Schlaepfer DD, Broome MA et al (1997) Fibronectin-stimulated signaling from a focal adhesion kinase-c-Src complex: involvement of the Grb2, p130cas, and Nck adaptor proteins. Mol Cell Biol 17(3):1702–1713

    CAS  PubMed  Google Scholar 

  • Schmidhauser C, Casperson GF et al (1992) A novel transcriptional enhancer is involved in the prolactin- and extracellular matrix-dependent regulation of beta-casein gene expression. Mol Biol Cell 3(6):699–709

    CAS  PubMed  Google Scholar 

  • Schmitt-Ney M, Doppler W et al (1991) Beta-casein gene promoter activity is regulated by the hormone-mediated relief of transcriptional repression and a mammary-gland-specific nuclear factor. Mol Cell Biol 11(7):3745–3755

    CAS  PubMed  Google Scholar 

  • Schwertfeger KL, McManaman JL et al (2003) Expression of constitutively activated Akt in the mammary gland leads to excess lipid synthesis during pregnancy and lactation. J Lipid Res 44(6):1100–1112

    Article  CAS  PubMed  Google Scholar 

  • Seagroves TN, Krnacik S et al (1998) C/EBPbeta, but not C/EBPalpha, is essential for ductal morphogenesis, lobuloalveolar proliferation, and functional differentiation in the mouse mammary gland. Genes Dev 12(12):1917–1928

    Article  CAS  PubMed  Google Scholar 

  • Segarini PR, Nesbitt JE et al (2001) The low density lipoprotein receptor-related protein/alpha2-macroglobulin receptor is a receptor for connective tissue growth factor. J Biol Chem 276(44):40659–40667

    Article  CAS  PubMed  Google Scholar 

  • Stelwagen K, McFadden HA et al (1999) Prolactin, alone or in combination with glucocorticoids, enhances tight junction formation and expression of the tight junction protein occludin in mammary cells. Mol Cell Endocrinol 156(1–2):55–61

    Article  CAS  PubMed  Google Scholar 

  • Streuli CH (2003) Cell adhesion in mammary gland biology and neoplasia. J Mammary Gland Biol Neoplasia 8(4):375–381

    Article  PubMed  Google Scholar 

  • Streuli CH, Bailey N et al (1991) Control of mammary epithelial differentiation: basement membrane induces tissue-specific gene expression in the absence of cell–cell interaction and morphological polarity. J Cell Biol 115(5):1383–1395

    Article  CAS  PubMed  Google Scholar 

  • Taddei I, Faraldo MM et al (2003) Integrins in mammary gland development and differentiation of mammary epithelium. J Mammary Gland Biol Neoplasia 8(4):383–394

    Article  PubMed  Google Scholar 

  • Tettamanti G, Malagoli D et al (2006) Growth factors and chemokines: a comparative functional approach between invertebrates and vertebrates. Curr Med Chem 13(23):2737–2750

    Article  CAS  PubMed  Google Scholar 

  • Tong ZY, Brigstock DR (2006) Intrinsic biological activity of the thrombospondin structural homology repeat in connective tissue growth factor. J Endocrinol 188(3):R1–R8

    Article  CAS  PubMed  Google Scholar 

  • Topper YJ, Freeman CS (1980) Multiple hormone interactions in the developmental biology of the mammary gland. Physiol Rev 60(4):1049–1106

    CAS  PubMed  Google Scholar 

  • Turner MD, Rennison ME et al (1992) Proteins are secreted by both constitutive and regulated secretory pathways in lactating mouse mammary epithelial cells. J Cell Biol 117(2):269–278

    Article  CAS  PubMed  Google Scholar 

  • van Miltenburg MH, Lalai R et al (2009) Complete focal adhesion kinase deficiency in the mammary gland causes ductal dilation and aberrant branching morphogenesis through defects in Rho kinase-dependent cell contractility. FASEB J 23(10):3482–3493

    Article  PubMed  CAS  Google Scholar 

  • Wahab N, Cox D et al (2007) Connective tissue growth factor (CTGF) promotes activated mesangial cell survival via up-regulation of mitogen-activated protein kinase phosphatase-1 (MKP-1). Biochem J 406(1):131–138

    Article  CAS  PubMed  Google Scholar 

  • Wakao H, Gouilleux F et al (1994) Mammary gland factor (MGF) is a novel member of the cytokine regulated transcription factor gene family and confers the prolactin response. EMBO J 13(9):2182–2191

    CAS  PubMed  Google Scholar 

  • Wang W, Morrison B et al (2008) Glucocorticoid induced expression of connective tissue growth factor contributes to lactogenic differentiation of mouse mammary epithelial cells. J Cell Physiol 214(1):38–46

    Article  CAS  PubMed  Google Scholar 

  • Watkin H, Richert MM et al (2008) Lactation failure in Src knockout mice is due to impaired secretory activation. BMC Dev Biol 8:6

    Article  PubMed  CAS  Google Scholar 

  • Weston BS, Wahab NA et al (2003) CTGF mediates TGF-beta-induced fibronectin matrix deposition by upregulating active alpha5beta1 integrin in human mesangial cells. J Am Soc Nephrol 14(3):601–610

    Article  CAS  PubMed  Google Scholar 

  • Williams JM, Daniel CW (1983) Mammary ductal elongation: differentiation of myoepithelium and basal lamina during branching morphogenesis. Dev Biol 97(2):274–290

    Article  CAS  PubMed  Google Scholar 

  • Wiseman BS, Werb Z (2002) Stromal effects on mammary gland development and breast cancer. Science 296(5570):1046–1049

    Article  CAS  PubMed  Google Scholar 

  • Wiseman BS, Sternlicht MD et al (2003) Site-specific inductive and inhibitory activities of MMP-2 and MMP-3 orchestrate mammary gland branching morphogenesis. J Cell Biol 162(6):1123–1133

    Article  CAS  PubMed  Google Scholar 

  • Wynick D, Small CJ et al (1998) Galanin regulates prolactin release and lactotroph proliferation. Proc Natl Acad Sci USA 95(21):12671–12676

    Article  CAS  PubMed  Google Scholar 

  • Xie J, Haslam SZ (1997) Extracellular matrix regulates ovarian hormone-dependent proliferation of mouse mammary epithelial cells. Endocrinology 138(6):2466–2473

    Article  CAS  PubMed  Google Scholar 

  • Xu R, Spencer VA et al (2007) Extracellular matrix-regulated gene expression requires cooperation of SWI/SNF and transcription factors. J Biol Chem 282(20):14992–14999

    Article  CAS  PubMed  Google Scholar 

  • Xu R, Nelson CM et al (2009) Sustained activation of STAT5 is essential for chromatin remodeling and maintenance of mammary-specific function. J Cell Biol 184(1):57–66

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors acknowledge support from the United States Military Cancer Institute.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mary Lou Cutler.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Morrison, B., Cutler, M.L. The contribution of adhesion signaling to lactogenesis. J. Cell Commun. Signal. 4, 131–139 (2010). https://doi.org/10.1007/s12079-010-0099-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12079-010-0099-6

Keywords

Navigation