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Journal of Mammary Gland Biology and Neoplasia

Published in:

01-09-2010

Extracellular Matrix Composition Reveals Complex and Dynamic Stromal-Epithelial Interactions in the Mammary Gland

Authors: Ori Maller, Holly Martinson, Pepper Schedin

Published in: Journal of Mammary Gland Biology and Neoplasia | Issue 3/2010

Abstract

The mammary gland is an excellent model system to study the interplay between stroma and epithelial cells because of the gland’s unique postnatal development and its distinct functional states. This review focuses on the contribution of the extracellular matrix (ECM) to stromal-epithelial interactions in the mammary gland. We describe how ECM physical properties, protein composition, and proteolytic state impact mammary gland architecture as well as provide instructive cues that influence the function of mammary epithelial cells during pubertal gland development and throughout adulthood. Further, based on recent proteomic analyses of mammary ECM, we describe known mammary ECM proteins and their potential functions, as well as describe several ECM proteins not previously recognized in this organ. ECM proteins are discussed in the context of the morphologically-distinct stromal subcompartments: the basal lamina, the intra- and interlobular stroma, and the fibrous connective tissue. Future studies aimed at in-depth qualitative and quantitative characterization of mammary ECM within these various subcompartments is required to better elucidate the function of ECM in normal as well as in pathological breast tissue.

Schedin P, Mitrenga T, Kaeck M. Estrous cycle regulation of mammary epithelial cell proliferation, differentiation, and death in the Sprague-Dawley rat: a model for investigating the role of estrous cycling in mammary carcinogenesis. J Mammary Gland Biol Neoplasia. 2000;5(2):211–25.PubMedCrossRef

Fata JE, Chaudhary V, Khokha R. Cellular turnover in the mammary gland is correlated with systemic levels of progesterone and not 17beta-estradiol during the estrous cycle. Biol Reprod. 2001;65(3):680–8.PubMedCrossRef

Ferguson DJ, Anderson TJ. Morphological evaluation of cell turnover in relation to the menstrual cycle in the “resting” human breast. Br J Cancer. 1981;44(2):177–81.PubMed

Ferguson JE, Schor AM, Howell A, Ferguson MW. Changes in the extracellular matrix of the normal human breast during the menstrual cycle. Cell Tissue Res. 1992;268(1):167–77.PubMedCrossRef

Robinson GW, McKnight RA, Smith GH, Hennighausen L. Mammary epithelial cells undergo secretory differentiation in cycling virgins but require pregnancy for the establishment of terminal differentiation. Development. 1995;121(7):2079–90.PubMed

Bissell MJ, Barcellos-Hoff MH. The influence of extracellular matrix on gene expression: is structure the message? J Cell Sci Suppl. 1987;8:327–43.PubMed

Butcher DT, Alliston T, Weaver VM. A tense situation: forcing tumour progression. Nat Rev Cancer. 2009;9(2):108–22.PubMedCrossRef

Vogel WF, Aszodi A, Alves F, Pawson T. Discoidin domain receptor 1 tyrosine kinase has an essential role in mammary gland development. Mol Cell Biol. 2001;21(8):2906–17.PubMedCrossRef

Scheele S, Falk M, Franzen A, Ellin F, Ferletta M, Lonai P, et al. Laminin alpha1 globular domains 4–5 induce fetal development but are not vital for embryonic basement membrane assembly. Proc Natl Acad Sci USA. 2005;102(5):1502–6.PubMedCrossRef

10.

Midwood KS, Valenick LV, Hsia HC, Schwarzbauer JE. Coregulation of fibronectin signaling and matrix contraction by tenascin-C and syndecan-4. Mol Biol Cell. 2004;15(12):5670–7.PubMedCrossRef

11.

Shattil SJ, Kim C, Ginsberg MH. The final steps of integrin activation: the end game. Nat Rev Mol Cell Biol 11(4):288–300.

12.

Takada Y, Ye X, Simon S. The integrins. Genome Biol. 2007;8(5):215.PubMedCrossRef

13.

Desgrosellier JS, Cheresh DA. Integrins in cancer: biological implications and therapeutic opportunities. Nat Rev Cancer 10(1):9-22.

14.

Larsen M, Artym VV, Green JA, Yamada KM. The matrix reorganized: extracellular matrix remodeling and integrin signaling. Curr Opin Cell Biol. 2006;18(5):463–71.PubMedCrossRef

15.

Ekblom P, Lonai P, Talts JF. Expression and biological role of laminin-1. Matrix Biol. 2003;22(1):35–47.PubMedCrossRef

16.

Kalluri R. Basement membranes: structure, assembly and role in tumour angiogenesis. Nat Rev Cancer. 2003;3(6):422–33.PubMedCrossRef

17.

Jalkanen M, Rapraeger A, Bernfield M. Mouse mammary epithelial cells produce basement membrane and cell surface heparan sulfate proteoglycans containing distinct core proteins. J Cell Biol. 1988;106(3):953–62.PubMedCrossRef

18.

Bissell MJ, Hall HG, Parry G. How does the extracellular matrix direct gene expression? J Theor Biol. 1982;99(1):31–68.PubMedCrossRef

19.

Masso-Welch PA, Darcy KM, Stangle-Castor NC, Ip MM. A developmental atlas of rat mammary gland histology. J Mammary Gland Biol Neoplasia. 2000;5(2):165–85.PubMedCrossRef

20.

Silberstein GB, Daniel CW. Glycosaminoglycans in the basal lamina and extracellular matrix of the developing mouse mammary duct. Dev Biol. 1982;90(1):215–22.PubMedCrossRef

21.

Nandi S, Guzman RC, Yang J. Hormones and mammary carcinogenesis in mice, rats, and humans: a unifying hypothesis. Proc Natl Acad Sci USA. 1995;92(9):3650–7.PubMedCrossRef

22.

Hattar R, Maller O, McDaniel S, Hansen KC, Hedman KJ, Lyons TR, et al. Tamoxifen induces pleiotrophic changes in mammary stroma resulting in extracellular matrix that suppresses transformed phenotypes. Breast Cancer Res. 2009;11(1):R5.PubMedCrossRef

23.

Schedin P, Mitrenga T, McDaniel S, Kaeck M. Mammary ECM composition and function are altered by reproductive state. Mol Carcinog. 2004;41(4):207–20.PubMedCrossRef

24.

Woodward TL, Mienaltowski AS, Modi RR, Bennett JM, Haslam SZ. Fibronectin and the alpha(5)beta(1) integrin are under developmental and ovarian steroid regulation in the normal mouse mammary gland. Endocrinology. 2001;142(7):3214–22.PubMedCrossRef

25.

DeMali KA, Wennerberg K, Burridge K. Integrin signaling to the actin cytoskeleton. Curr Opin Cell Biol. 2003;15(5):572–82.PubMedCrossRef

26.

Paszek MJ, Zahir N, Johnson KR, Lakins JN, Rozenberg GI, Gefen A, et al. Tensional homeostasis and the malignant phenotype. Cancer Cell. 2005;8(3):241–54.PubMedCrossRef

27.

Provenzano PP, Inman DR, Eliceiri KW, Keely PJ. Matrix density-induced mechanoregulation of breast cell phenotype, signaling and gene expression through a FAK-ERK linkage. Oncogene. 2009;28(49):4326–43.PubMedCrossRef

28.

Levental KR, Yu H, Kass L, Lakins JN, Egeblad M, Erler JT, et al. Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell. 2009;139(5):891–906.PubMedCrossRef

29.

Engler AJ, Sen S, Sweeney HL, Discher DE. Matrix elasticity directs stem cell lineage specification. Cell. 2006;126(4):677–89.PubMedCrossRef

30.

Taddei I, Deugnier MA, Faraldo MM, Petit V, Bouvard D, Medina D, et al. Beta1 integrin deletion from the basal compartment of the mammary epithelium affects stem cells. Nat Cell Biol. 2008;10(6):716–22.PubMedCrossRef

31.

Mecham RP, Heuser JE. The elastic fiber. In: Hay ED (ed). Cell Biology of Extracellular Matrix: Plenum 1991; p. 79–109.

32.

Linsenmayer TF. Collagen. In: Hay ED, editor. Cell biology of extracellular matrix. NY: Plenum; 1991. p. 7–44.

33.

Szauter KM, Cao T, Boyd CD, Csiszar K. Lysyl oxidase in development, aging and pathologies of the skin. Pathol Biol (Paris). 2005;53(7):448–56.

34.

Lorand L, Graham RM. Transglutaminases: crosslinking enzymes with pleiotropic functions. Nat Rev Mol Cell Biol. 2003;4(2):140–56.PubMedCrossRef

35.

Nunes I, Gleizes PE, Metz CN, Rifkin DB. Latent transforming growth factor-beta binding protein domains involved in activation and transglutaminase-dependent cross-linking of latent transforming growth factor-beta. J Cell Biol. 1997;136(5):1151–63.PubMedCrossRef

36.

Williams JM, Daniel CW. Mammary ductal elongation: differentiation of myoepithelium and basal lamina during branching morphogenesis. Dev Biol. 1983;97(2):274–90.PubMedCrossRef

37.

Fata JE, Werb Z, Bissell MJ. Regulation of mammary gland branching morphogenesis by the extracellular matrix and its remodeling enzymes. Breast Cancer Res. 2004;6(1):1–11.PubMed

38.

Discher DE, Mooney DJ, Zandstra PW. Growth factors, matrices, and forces combine and control stem cells. Science. 2009;324(5935):1673–7.PubMedCrossRef

39.

Hynes RO. The extracellular matrix: not just pretty fibrils. Science. 2009;326(5957):1216–9.PubMedCrossRef

40.

Taipale J, Miyazono K, Heldin CH, Keski-Oja J. Latent transforming growth factor-beta 1 associates to fibroblast extracellular matrix via latent TGF-beta binding protein. J Cell Biol. 1994;124(1–2):171–81.PubMedCrossRef

41.

Yu Q, Stamenkovic I. Cell surface-localized matrix metalloproteinase-9 proteolytically activates TGF-beta and promotes tumor invasion and angiogenesis. Genes Dev. 2000;14(2):163–76.PubMed

42.

Munger JS, Huang X, Kawakatsu H, Griffiths MJ, Dalton SL, Wu J, et al. The integrin alpha v beta 6 binds and activates latent TGF beta 1: a mechanism for regulating pulmonary inflammation and fibrosis. Cell. 1999;96(3):319–28.PubMedCrossRef

43.

Wipff PJ, Rifkin DB, Meister JJ, Hinz B. Myofibroblast contraction activates latent TGF-beta1 from the extracellular matrix. J Cell Biol. 2007;179(6):1311–23.PubMedCrossRef

44.

Sawhney RK, Howard J. Slow local movements of collagen fibers by fibroblasts drive the rapid global self-organization of collagen gels. J Cell Biol. 2002;157(6):1083–91.PubMedCrossRef

45.

Harris AK, Stopak D, Wild P. Fibroblast traction as a mechanism for collagen morphogenesis. Nature. 1981;290(5803):249–51.PubMedCrossRef

46.

Silberstein GB, Strickland P, Coleman S, Daniel CW. Epithelium-dependent extracellular matrix synthesis in transforming growth factor-beta 1-growth-inhibited mouse mammary gland. J Cell Biol. 1990;110(6):2209–19.PubMedCrossRef

47.

Daniel CW, Silberstein GB, Van Horn K, Strickland P, Robinson S. TGF-beta 1-induced inhibition of mouse mammary ductal growth: developmental specificity and characterization. Dev Biol. 1989;135(1):20–30.PubMedCrossRef

48.

Robinson SD, Silberstein GB, Roberts AB, Flanders KC, Daniel CW. Regulated expression and growth inhibitory effects of transforming growth factor-beta isoforms in mouse mammary gland development. Development. 1991;113(3):867–78.PubMed

49.

Pierce Jr DF, Johnson MD, Matsui Y, Robinson SD, Gold LI, Purchio AF, et al. Genes Dev. 1993;7(12A):2308–17.PubMedCrossRef

50.

Robinson SD, Roberts AB, Daniel CW. TGF beta suppresses casein synthesis in mouse mammary explants and may play a role in controlling milk levels during pregnancy. J Cell Biol. 1993;120(1):245–51.PubMedCrossRef

51.

Wu WJ, Lee CF, Hsin CH, Du JY, Hsu TC, Lin TH, et al. TGF-beta inhibits prolactin-induced expression of beta-casein by a Smad3-dependent mechanism. J Cell Biochem. 2008;104(5):1647–59.PubMedCrossRef

52.

Schedin P, O’Brien J, Rudolph M, Stein T, Borges V. Microenvironment of the involuting mammary gland mediates mammary cancer progression. J Mammary Gland Biol Neoplasia. 2007;12(1):71–82.PubMedCrossRef

53.

Faure E, Heisterkamp N, Groffen J, Kaartinen V. Differential expression of TGF-beta isoforms during postlactational mammary gland involution. Cell Tissue Res. 2000;300(1):89–95.PubMed

54.

Kim ES, Sohn YW, Moon A. TGF-beta-induced transcriptional activation of MMP-2 is mediated by activating transcription factor (ATF)2 in human breast epithelial cells. Cancer Lett. 2007;252(1):147–56.PubMedCrossRef

55.

Bierie B, Moses HL. Transforming growth factor beta (TGF-beta) and inflammation in cancer. Cytokine Growth Factor Rev 21(1):49–59.

56.

Adair-Kirk TL, Senior RM. Fragments of extracellular matrix as mediators of inflammation. Int J Biochem Cell Biol. 2008;40(6–7):1101–10.PubMedCrossRef

57.

Schenk S, Quaranta V. Tales from the crypt[ic] sites of the extracellular matrix. Trends Cell Biol. 2003;13(7):366–75.PubMedCrossRef

58.

Schedin P, Strange R, Mitrenga T, Wolfe P, Kaeck M. Fibronectin fragments induce MMP activity in mouse mammary epithelial cells: evidence for a role in mammary tissue remodeling. J Cell Sci. 2000;113(Pt 5):795–806.PubMed

59.

Williams CM, Engler AJ, Slone RD, Galante LL, Schwarzbauer JE. Fibronectin expression modulates mammary epithelial cell proliferation during acinar differentiation. Cancer Res. 2008;68(9):3185–92.PubMedCrossRef

60.

Friedland JC, Lee MH, Boettiger D. Mechanically activated integrin switch controls alpha5beta1 function. Science. 2009;323(5914):642–4.PubMedCrossRef

61.

Liang X, Huuskonen J, Hajivandi M, Manzanedo R, Predki P, Amshey JR, et al. Identification and quantification of proteins differentially secreted by a pair of normal and malignant breast-cancer cell lines. Proteomics. 2009;9(1):182–93.PubMedCrossRef

62.

Hansen KC, Kiemele L, Maller O, O’Brien J, Shankar A, Fornetti J, et al. An in-solution ultrasonication-assisted digestion method for improved extracellular matrix proteome coverage. Mol Cell Proteomics. 2009;8(7):1648–57.PubMedCrossRef

63.

Farquhar MG. The glomerular basement membrane: A selective macromolecular fliter. In: Hay ED, editor. Cell biology extracellular matrix. NY: Plenum; 1991.

64.

Li S, Edgar D, Fassler R, Wadsworth W, Yurchenco PD. The role of laminin in embryonic cell polarization and tissue organization. Dev Cell. 2003;4(5):613–24.PubMedCrossRef

65.

Tzu J, Marinkovich MP. Bridging structure with function: structural, regulatory, and developmental role of laminins. Int J Biochem Cell Biol. 2008;40(2):199–214.PubMedCrossRef

66.

Hallmann R, Horn N, Selg M, Wendler O, Pausch F, Sorokin LM. Expression and function of laminins in the embryonic and mature vasculature. Physiol Rev. 2005;85(3):979–1000.PubMedCrossRef

67.

Francoeur C, Escaffit F, Vachon PH, Beaulieu JF. Proinflammatory cytokines TNF-alpha and IFN-gamma alter laminin expression under an apoptosis-independent mechanism in human intestinal epithelial cells. Am J Physiol Gastrointest Liver Physiol. 2004;287(3):G592–8.PubMedCrossRef

68.

Kleinman HK, Martin GR. Matrigel: basement membrane matrix with biological activity. Semin Cancer Biol. 2005;15(5):378–86.PubMedCrossRef

69.

Timpl R, Rohde H, Robey PG, Rennard SI, Foidart JM, Martin GR. Laminin–a glycoprotein from basement membranes. J Biol Chem. 1979;254(19):9933–7.PubMed

70.

Miner JH, Li C, Mudd JL, Go G, Sutherland AE. Compositional and structural requirements for laminin and basement membranes during mouse embryo implantation and gastrulation. Development. 2004;131(10):2247–56.PubMedCrossRef

71.

Smyth N, Vatansever HS, Murray P, Meyer M, Frie C, Paulsson M, et al. Absence of basement membranes after targeting the LAMC1 gene results in embryonic lethality due to failure of endoderm differentiation. J Cell Biol. 1999;144(1):151–60.PubMedCrossRef

72.

Hohenester E, Tisi D, Talts JF, Timpl R. The crystal structure of a laminin G-like module reveals the molecular basis of alpha-dystroglycan binding to laminins, perlecan, and agrin. Mol Cell. 1999;4(5):783–92.PubMedCrossRef

73.

Streuli CH, Bailey N, Bissell MJ. 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. 1991;115(5):1383–95.PubMedCrossRef

74.

Li ML, Aggeler J, Farson DA, Hatier C, Hassell J, Bissell MJ. Influence of a reconstituted basement membrane and its components on casein gene expression and secretion in mouse mammary epithelial cells. Proc Natl Acad Sci USA. 1987;84(1):136–40.PubMedCrossRef

75.

Bissell MJ, Kenny PA, Radisky DC. Microenvironmental regulators of tissue structure and function also regulate tumor induction and progression: the role of extracellular matrix and its degrading enzymes. Cold Spring Harb Symp Quant Biol. 2005;70:343–56.PubMedCrossRef

76.

Gudjonsson T, Ronnov-Jessen L, Villadsen R, Rank F, Bissell MJ, Petersen OW. Normal and tumor-derived myoepithelial cells differ in their ability to interact with luminal breast epithelial cells for polarity and basement membrane deposition. J Cell Sci. 2002;115(Pt 1):39–50.PubMed

77.

Debnath J, Muthuswamy SK, Brugge JS. Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in three-dimensional basement membrane cultures. Methods. 2003;30(3):256–68.PubMedCrossRef

78.

Petersen OW, Ronnov-Jessen L, Howlett AR, Bissell MJ. Interaction with basement membrane serves to rapidly distinguish growth and differentiation pattern of normal and malignant human breast epithelial cells. Proc Natl Acad Sci USA. 1992;89(19):9064–8.PubMedCrossRef

79.

Marinkovich MP. Tumour microenvironment: laminin 332 in squamous-cell carcinoma. Nat Rev Cancer. 2007;7(5):370–80.PubMedCrossRef

80.

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.PubMedCrossRef

81.

Schenk S, Hintermann E, Bilban M, Koshikawa N, Hojilla C, Khokha R, et al. Binding to EGF receptor of a laminin-5 EGF-like fragment liberated during MMP-dependent mammary gland involution. J Cell Biol. 2003;161(1):197–209.PubMedCrossRef

82.

Giannelli G, Falk-Marzillier J, Schiraldi O, Stetler-Stevenson WG, Quaranta V. Induction of cell migration by matrix metalloprotease-2 cleavage of laminin-5. Science. 1997;277(5323):225–8.PubMedCrossRef

83.

Yurchenco PD, Ruben GC. Basement membrane structure in situ: evidence for lateral associations in the type IV collagen network. J Cell Biol. 1987;105(6 Pt 1):2559–68.PubMedCrossRef

84.

Poschl E, Schlotzer-Schrehardt U, Brachvogel B, Saito K, Ninomiya Y, Mayer U. Collagen IV is essential for basement membrane stability but dispensable for initiation of its assembly during early development. Development. 2004;131(7):1619–28.PubMedCrossRef

85.

Yurchenco PD, Schittny JC. Molecular architecture of basement membranes. Faseb J. 1990;4(6):1577–90.PubMed

86.

Kalluri R, Shield CF, Todd P, Hudson BG, Neilson EG. Isoform switching of type IV collagen is developmentally arrested in X-linked Alport syndrome leading to increased susceptibility of renal basement membranes to endoproteolysis. J Clin Invest. 1997;99(10):2470–8.PubMedCrossRef

87.

Khoshnoodi J, Pedchenko V, Hudson BG. Mammalian collagen IV. Microsc Res Tech. 2008;71(5):357–70.PubMedCrossRef

88.

Wicha MS, Liotta LA, Vonderhaar BK, Kidwell WR. Effects of inhibition of basement membrane collagen deposition on rat mammary gland development. Dev Biol. 1980;80(2):253–6.PubMedCrossRef

89.

Wicha MS, Liotta LA, Garbisa S, Kidwell WR. Basement membrane collagen requirements for attachment and growth of mammary epithelium. Exp Cell Res. 1979;124(1):181–90.PubMedCrossRef

90.

Marneros AG, Olsen BR. The role of collagen-derived proteolytic fragments in angiogenesis. Matrix Biol. 2001;20(5–6):337–45.PubMedCrossRef

91.

Mundel TM, Kalluri R. Type IV collagen-derived angiogenesis inhibitors. Microvasc Res. 2007;74(2–3):85–9.PubMedCrossRef

92.

Djonov V, Andres AC, Ziemiecki A. Vascular remodelling during the normal and malignant life cycle of the mammary gland. Microsc Res Tech. 2001;52(2):182–9.PubMedCrossRef

93.

Nischt R, Schmidt C, Mirancea N, Baranowsky A, Mokkapati S, Smyth N, et al. Lack of nidogen-1 and -2 prevents basement membrane assembly in skin-organotypic coculture. J Invest Dermatol. 2007;127(3):545–54.PubMedCrossRef

94.

Bose K, Nischt R, Page A, Bader BL, Paulsson M, Smyth N. Loss of nidogen-1 and -2 results in syndactyly and changes in limb development. J Biol Chem. 2006;281(51):39620–9.PubMedCrossRef

95.

Kohling R, Nischt R, Vasudevan A, Ho M, Weiergraber M, Schneider T, et al. Nidogen and nidogen-associated basement membrane proteins and neuronal plasticity. Neurodegener Dis. 2006;3(1–2):56–61.PubMed

96.

Ekblom P, Ekblom M, Fecker L, Klein G, Zhang HY, Kadoya Y, et al. Role of mesenchymal nidogen for epithelial morphogenesis in vitro. Development. 1994;120(7):2003–14.PubMed

97.

Fox JW, Mayer U, Nischt R, Aumailley M, Reinhardt D, Wiedemann H, et al. Recombinant nidogen consists of three globular domains and mediates binding of laminin to collagen type IV. Embo J. 1991;10(11):3137–46.PubMed

98.

Mayer U, Nischt R, Poschl E, Mann K, Fukuda K, Gerl M, et al. A single EGF-like motif of laminin is responsible for high affinity nidogen binding. Embo J. 1993;12(5):1879–85.PubMed

99.

Reinhardt D, Mann K, Nischt R, Fox JW, Chu ML, Krieg T, et al. Mapping of nidogen binding sites for collagen type IV, heparan sulfate proteoglycan, and zinc. J Biol Chem. 1993;268(15):10881–7.PubMed

100.

Murshed M, Smyth N, Miosge N, Karolat J, Krieg T, Paulsson M, et al. The absence of nidogen 1 does not affect murine basement membrane formation. Mol Cell Biol. 2000;20(18):7007–12.PubMedCrossRef

101.

Miosge N, Sasaki T, Timpl R. Evidence of nidogen-2 compensation for nidogen-1 deficiency in transgenic mice. Matrix Biol. 2002;21(7):611–21.PubMedCrossRef

102.

Bader BL, Smyth N, Nedbal S, Miosge N, Baranowsky A, Mokkapati S, et al. Compound genetic ablation of nidogen 1 and 2 causes basement membrane defects and perinatal lethality in mice. Mol Cell Biol. 2005;25(15):6846–56.PubMedCrossRef

103.

Pujuguet P, Simian M, Liaw J, Timpl R, Werb Z, Bissell MJ. Nidogen-1 regulates laminin-1-dependent mammary-specific gene expression. J Cell Sci. 2000;113(Pt 5):849–58.PubMed

104.

Friedrich MV, Gohring W, Morgelin M, Brancaccio A, David G, Timpl R. Structural basis of glycosaminoglycan modification and of heterotypic interactions of perlecan domain V. J Mol Biol. 1999;294(1):259–70.PubMedCrossRef

105.

Handler M, Yurchenco PD, Iozzo RV. Developmental expression of perlecan during murine embryogenesis. Dev Dyn. 1997;210(2):130–45.PubMedCrossRef

106.

Costell M, Gustafsson E, Aszodi A, Morgelin M, Bloch W, Hunziker E, et al. Perlecan maintains the integrity of cartilage and some basement membranes. J Cell Biol. 1999;147(5):1109–22.PubMedCrossRef

107.

Arikawa-Hirasawa E, Watanabe H, Takami H, Hassell JR, Yamada Y. Perlecan is essential for cartilage and cephalic development. Nat Genet. 1999;23(3):354–8.PubMedCrossRef

108.

Bix G, Fu J, Gonzalez EM, Macro L, Barker A, Campbell S, et al. Endorepellin causes endothelial cell disassembly of actin cytoskeleton and focal adhesions through alpha2beta1 integrin. J Cell Biol. 2004;166(1):97–109.PubMedCrossRef

109.

Smith SM, West LA, Govindraj P, Zhang X, Ornitz DM, Hassell JR. Heparan and chondroitin sulfate on growth plate perlecan mediate binding and delivery of FGF-2 to FGF receptors. Matrix Biol. 2007;26(3):175–84.PubMedCrossRef

110.

Datta S, Pierce M, Datta MW. Perlecan signaling: helping hedgehog stimulate prostate cancer growth. Int J Biochem Cell Biol. 2006;38(11):1855–61.PubMedCrossRef

111.

Gelse K, Poschl E, Aigner T. Collagens–structure, function, and biosynthesis. Adv Drug Deliv Rev. 2003;55(12):1531–46.PubMedCrossRef

112.

Church RL, Pfeiffer SE, Tanzer ML. Collagen biosynthesis: synthesis and secretion of a high molecular weight collagen precursor (procollagen). Proc Natl Acad Sci USA. 1971;68(11):2638–42.PubMedCrossRef

113.

Berdichevsky F, Alford D, D’Souza B, Taylor-Papadimitriou J. Branching morphogenesis of human mammary epithelial cells in collagen gels. J Cell Sci. 1994;107(Pt 12):3557–68.PubMed

114.

Krause S, Maffini MV, Soto AM, Sonnenschein C. A novel 3D in vitro culture model to study stromal-epithelial interactions in the mammary gland. Tissue Eng Part C Methods. 2008;14(3):261–71.PubMedCrossRef

115.

Chen J, Diacovo TG, Grenache DG, Santoro SA, Zutter MM. The alpha(2) integrin subunit-deficient mouse: a multifaceted phenotype including defects of branching morphogenesis and hemostasis. Am J Pathol. 2002;161(1):337–44.PubMed

116.

Kalluri R, Zeisberg M. Fibroblasts in cancer. Nat Rev Cancer. 2006;6(5):392–401.PubMedCrossRef

117.

McDaniel SM, Rumer KK, Biroc SL, Metz RP, Singh M, Porter W, et al. Remodeling of the Mammary Microenvironment after Lactation Promotes Breast Tumor Cell Metastasis. Am J Pathol 2006;168(2).

118.

O’Brien J, Lyons T, Monks J, Lucia MS, Wilson RS, Hines L, et al. Alternatively activated macrophages and collagen remodeling characterize the postpartum involuting mammary gland across species. Am J Pathol. 2010;176(3):1241–55.PubMedCrossRef

119.

Ferreira AM, Takagawa S, Fresco R, Zhu X, Varga J, DiPietro LA. Diminished induction of skin fibrosis in mice with MCP-1 deficiency. J Invest Dermatol. 2006;126(8):1900–8.PubMedCrossRef

120.

George EL, Georges-Labouesse EN, Patel-King RS, Rayburn H, Hynes RO. Defects in mesoderm, neural tube and vascular development in mouse embryos lacking fibronectin. Development. 1993;119(4):1079–91.PubMed

121.

Yamada KM. Fibronectin and other cell interactive glycoproteins. In: Hay ED, editor. Cell biology of extracellular matrix. NY: Plenum; 1991. p. 111–46.

122.

Blaustein M, Pelisch F, Coso OA, Bissell MJ, Kornblihtt AR, Srebrow A. Mammary epithelial-mesenchymal interaction regulates fibronectin alternative splicing via phosphatidylinositol 3-kinase. J Biol Chem. 2004;279(20):21029–37.PubMedCrossRef

123.

George J, Wang SS, Sevcsik AM, Sanicola M, Cate RL, Koteliansky VE, et al. Transforming growth factor-beta initiates wound repair in rat liver through induction of the EIIIA-fibronectin splice isoform. Am J Pathol. 2000;156(1):115–24.PubMed

124.

Sakai T, Larsen M, Yamada KM. Fibronectin requirement in branching morphogenesis. Nature. 2003;423(6942):876–81.PubMedCrossRef

125.

Jones PL, Jones FS. Tenascin-C in development and disease: gene regulation and cell function. Matrix Biol. 2000;19(7):581–96.PubMedCrossRef

126.

Pas J, Wyszko E, Rolle K, Rychlewski L, Nowak S, Zukiel R, et al. Analysis of structure and function of tenascin-C. Int J Biochem Cell Biol. 2006;38(9):1594–602.PubMedCrossRef

127.

Chiquet-Ehrismann R, Kalla P, Pearson CA, Beck K, Chiquet M. Tenascin interferes with fibronectin action. Cell. 1988;53(3):383–90.PubMedCrossRef

128.

Huang W, Chiquet-Ehrismann R, Moyano JV, Garcia-Pardo A, Orend G. Interference of tenascin-C with syndecan-4 binding to fibronectin blocks cell adhesion and stimulates tumor cell proliferation. Cancer Res. 2001;61(23):8586–94.PubMed

129.

Wehrle-Haller B, Chiquet M. Dual function of tenascin: simultaneous promotion of neurite growth and inhibition of glial migration. J Cell Sci. 1993;106(Pt 2):597–610.PubMed

130.

Saga Y, Yagi T, Ikawa Y, Sakakura T, Aizawa S. Mice develop normally without tenascin. Genes Dev. 1992;6(10):1821–31.PubMedCrossRef

131.

Fukamauchi F, Mataga N, Wang YJ, Sato S, Yoshiki A, Kusakabe M. Tyrosine hydroxylase activity and its mRNA level in dopaminergic neurons of tenascin gene knockout mouse. Biochem Biophys Res Commun. 1997;231(2):356–9.PubMedCrossRef

132.

Fukamauchi F, Mataga N, Wang YJ, Sato S, Youshiki A, Kusakabe M. Abnormal behavior and neurotransmissions of tenascin gene knockout mouse. Biochem Biophys Res Commun. 1996;221(1):151–6.PubMedCrossRef

133.

Chiquet-Ehrismann R, Chiquet M. Tenascins: regulation and putative functions during pathological stress. J Pathol. 2003;200(4):488–99.PubMedCrossRef

134.

Latijnhouwers M, Bergers M, Ponec M, Dijkman H, Andriessen M, Schalkwijk J. Human epidermal keratinocytes are a source of tenascin-C during wound healing. J Invest Dermatol. 1997;108(5):776–83.PubMedCrossRef

135.

Chiquet-Ehrismann R, Mackie EJ, Pearson CA, Sakakura T. Tenascin: an extracellular matrix protein involved in tissue interactions during fetal development and oncogenesis. Cell. 1986;47(1):131–9.PubMedCrossRef

136.

Jones PL, Boudreau N, Myers CA, Erickson HP, Bissell MJ. Tenascin-C inhibits extracellular matrix-dependent gene expression in mammary epithelial cells. Localization of active regions using recombinant tenascin fragments. J Cell Sci. 1995;108(Pt 2):519–27.PubMed

137.

Kalembey I, Yoshida T, Iriyama K, Sakakura T. Analysis of tenascin mRNA expression in the murine mammary gland from embryogenesis to carcinogenesis: an in situ hybridization study. Int J Dev Biol. 1997;41(4):569–73.PubMed

138.

Koukoulis GK, Gould VE, Bhattacharyya A, Gould JE, Howeedy AA, Virtanen I. Tenascin in normal, reactive, hyperplastic, and neoplastic tissues: biologic and pathologic implications. Hum Pathol. 1991;22(7):636–43.PubMedCrossRef

139.

Bristow J, Tee MK, Gitelman SE, Mellon SH, Miller WL. Tenascin-X: a novel extracellular matrix protein encoded by the human XB gene overlapping P450c21B. J Cell Biol. 1993;122(1):265–78.PubMedCrossRef

140.

Burch GH, Gong Y, Liu W, Dettman RW, Curry CJ, Smith L, et al. Tenascin-X deficiency is associated with Ehlers-Danlos syndrome. Nat Genet. 1997;17(1):104–8.PubMedCrossRef

141.

Wong SY, Crowley D, Bronson RT, Hynes RO. Analyses of the role of endogenous SPARC in mouse models of prostate and breast cancer. Clin Exp Metastasis. 2008;25(2):109–18.PubMedCrossRef

142.

Brekken RA, Sage EH. SPARC, a matricellular protein: at the crossroads of cell-matrix communication. Matrix Biol. 2001;19(8):816–27.PubMedCrossRef

143.

Hohenester E, Engel J. Domain structure and organisation in extracellular matrix proteins. Matrix Biol. 2002;21(2):115–28.PubMedCrossRef

144.

Bradshaw AD, Puolakkainen P, Dasgupta J, Davidson JM, Wight TN. Helene Sage E. SPARC-null mice display abnormalities in the dermis characterized by decreased collagen fibril diameter and reduced tensile strength J Invest Dermatol. 2003;120(6):949–55.

145.

Sweetwyne MT, Brekken RA, Workman G, Bradshaw AD, Carbon J, Siadak AW, et al. Functional analysis of the matricellular protein SPARC with novel monoclonal antibodies. J Histochem Cytochem. 2004;52(6):723–33.PubMedCrossRef

146.

Barker TH, Baneyx G, Cardo-Vila M, Workman GA, Weaver M, Menon PM, et al. SPARC regulates extracellular matrix organization through its modulation of integrin-linked kinase activity. J Biol Chem. 2005;280(43):36483–93.PubMedCrossRef

147.

Schaefer L, Iozzo RV. Biological functions of the small leucine-rich proteoglycans: from genetics to signal transduction. J Biol Chem. 2008;283(31):21305–9.PubMedCrossRef

148.

Wight TN, Heinegard DK, Hascall VC. Proteoglycans Structure and Function. In: Hay ED (ed). Cell Biology of Extracellular Matrix, 1991, p. 45–78.

149.

Coppock DL, Kopman C, Scandalis S, Gilleran S. Preferential gene expression in quiescent human lung fibroblasts. Cell Growth Differ. 1993;4(6):483–93.PubMed

150.

Minor K, Tang X, Kahrilas G, Archibald SJ, Davies JE, Davies SJ. Decorin promotes robust axon growth on inhibitory CSPGs and myelin via a direct effect on neurons. Neurobiol Dis. 2008;32(1):88–95.PubMedCrossRef

151.

Danielson KG, Baribault H, Holmes DF, Graham H, Kadler KE, Iozzo RV. Targeted disruption of decorin leads to abnormal collagen fibril morphology and skin fragility. J Cell Biol. 1997;136(3):729–43.PubMedCrossRef

152.

Reed CC, Waterhouse A, Kirby S, Kay P, Owens RT, McQuillan DJ, et al. Decorin prevents metastatic spreading of breast cancer. Oncogene. 2005;24(6):1104–10.PubMedCrossRef

153.

Zhu JX, Goldoni S, Bix G, Owens RT, McQuillan DJ, Reed CC, et al. Decorin evokes protracted internalization and degradation of the epidermal growth factor receptor via caveolar endocytosis. J Biol Chem. 2005;280(37):32468–79.PubMedCrossRef

154.

Grant DS, Yenisey C, Rose RW, Tootell M, Santra M, Iozzo RV. Decorin suppresses tumor cell-mediated angiogenesis. Oncogene. 2002;21(31):4765–77.PubMedCrossRef

155.

Yamaguchi Y, Mann DM, Ruoslahti E. Negative regulation of transforming growth factor-beta by the proteoglycan decorin. Nature. 1990;346(6281):281–4.PubMedCrossRef

156.

Xu T, Bianco P, Fisher LW, Longenecker G, Smith E, Goldstein S, et al. Targeted disruption of the biglycan gene leads to an osteoporosis-like phenotype in mice. Nat Genet. 1998;20(1):78–82.PubMedCrossRef

157.

Fust A, LeBellego F, Iozzo RV, Roughley PJ, Ludwig MS. Alterations in lung mechanics in decorin-deficient mice. Am J Physiol Lung Cell Mol Physiol. 2005;288(1):L159–66.PubMedCrossRef

158.

Schaefer L, Mihalik D, Babelova A, Krzyzankova M, Grone HJ, Iozzo RV, et al. Regulation of fibrillin-1 by biglycan and decorin is important for tissue preservation in the kidney during pressure-induced injury. Am J Pathol. 2004;165(2):383–96.PubMed

159.

Salgado RM, Favaro RR, Martin SS, Zorn TM. The estrous cycle modulates small leucine-rich proteoglycans expression in mouse uterine tissues. Anat Rec (Hoboken). 2009;292(1):138–53.

160.

San Martin S, Soto-Suazo M, De Oliveira SF, Aplin JD, Abrahamsohn P, Zorn TM. Small leucine-rich proteoglycans (SLRPs) in uterine tissues during pregnancy in mice. Reproduction. 2003;125(4):585–95.PubMedCrossRef

161.

Fleming WW, Sullivan CE, Torchia DA. Characterization of molecular motions in 13C-labeled aortic elastin by 13C-1H magnetic double resonance. Biopolymers. 1980;19(3):597–617.PubMedCrossRef

162.

Yanagisawa H, Davis EC, Starcher BC, Ouchi T, Yanagisawa M, Richardson JA, et al. Fibulin-5 is an elastin-binding protein essential for elastic fibre development in vivo. Nature. 2002;415(6868):168–71.PubMedCrossRef

163.

Choi J, Bergdahl A, Zheng Q, Starcher B, Yanagisawa H, Davis EC. Analysis of dermal elastic fibers in the absence of fibulin-5 reveals potential roles for fibulin-5 in elastic fiber assembly. Matrix Biol. 2009;28(4):211–20.PubMedCrossRef

164.

Reinboth B, Hanssen E, Cleary EG, Gibson MA. Molecular interactions of biglycan and decorin with elastic fiber components: biglycan forms a ternary complex with tropoelastin and microfibril-associated glycoprotein 1. J Biol Chem. 2002;277(6):3950–7.PubMedCrossRef

165.

Trask BC, Trask TM, Broekelmann T, Mecham RP. The microfibrillar proteins MAGP-1 and fibrillin-1 form a ternary complex with the chondroitin sulfate proteoglycan decorin. Mol Biol Cell. 2000;11(5):1499–507.PubMed

166.

Boyd NF, Lockwood GA, Byng JW, Tritchler DL, Yaffe MJ. Mammographic densities and breast cancer risk. Cancer Epidemiol Biomarkers Prev. 1998;7(12):1133–44.PubMed

167.

Provenzano PP, Inman DR, Eliceiri KW, Knittel JG, Yan L, Rueden CT, et al. Collagen density promotes mammary tumor initiation and progression. BMC Med. 2008;6:11.PubMedCrossRef

168.

Mydel P, Shipley JM, Adair-Kirk TL, Kelley DG, Broekelmann TJ, Mecham RP, et al. Neutrophil elastase cleaves laminin-332 (laminin-5) generating peptides that are chemotactic for neutrophils. J Biol Chem. 2008;283(15):9513–22.PubMedCrossRef

169.

Senior RM, Gresham HD, Griffin GL, Brown EJ, Chung AE. Entactin stimulates neutrophil adhesion and chemotaxis through interactions between its Arg-Gly-Asp (RGD) domain and the leukocyte response integrin. J Clin Invest. 1992;90(6):2251–7.PubMedCrossRef

170.

Senior RM, Hinek A, Griffin GL, Pipoly DJ, Crouch EC, Mecham RP. Neutrophils show chemotaxis to type IV collagen and its 7 S domain and contain a 67 kD type IV collagen binding protein with lectin properties. Am J Respir Cell Mol Biol. 1989;1(6):479–87.PubMed

171.

Adair-Kirk TL, Atkinson JJ, Broekelmann TJ, Doi M, Tryggvason K, Miner JH, et al. A site on laminin alpha 5, AQARSAASKVKVSMKF, induces inflammatory cell production of matrix metalloproteinase-9 and chemotaxis. J Immunol. 2003;171(1):398–406.PubMed

172.

Stein T, Morris JS, Davies CR, Weber-Hall SJ, Duffy MA, Heath VJ, et al. Involution of the mouse mammary gland is associated with an immune cascade and an acute-phase response, involving LBP, CD14 and STAT3. Breast Cancer Res. 2004;6(2):R75–91.PubMedCrossRef

173.

Vaday GG, Lider O. Extracellular matrix moieties, cytokines, and enzymes: dynamic effects on immune cell behavior and inflammation. J Leukoc Biol. 2000;67(2):149–59.PubMed

174.

Lilla JN, Joshi RV, Craik CS, Werb Z. Active plasma kallikrein localizes to mast cells and regulates epithelial cell apoptosis, adipocyte differentiation, and stromal remodeling during mammary gland involution. J Biol Chem. 2009;284(20):13792–803.PubMedCrossRef

175.

Babelova A, Moreth K, Tsalastra-Greul W, Zeng-Brouwers J, Eickelberg O, Young MF, et al. Biglycan, a danger signal that activates the NLRP3 inflammasome via toll-like and P2X receptors. J Biol Chem. 2009;284(36):24035–48.PubMedCrossRef

176.

Johnson GB, Brunn GJ, Kodaira Y, Platt JL. Receptor-mediated monitoring of tissue well-being via detection of soluble heparan sulfate by Toll-like receptor 4. J Immunol. 2002;168(10):5233–9.PubMed

177.

Termeer C, Benedix F, Sleeman J, Fieber C, Voith U, Ahrens T, et al. Oligosaccharides of Hyaluronan activate dendritic cells via toll-like receptor 4. J Exp Med. 2002;195(1):99–111.PubMedCrossRef

178.

Elenstrom-Magnusson C, Chen W, Clinchy B, Obrink B, Severison E. IL-4-induced B cell migration involves transient interactions between beta 1 integrins and extracellular matrix components. Int Immunol. 1995;7(4):567–73.PubMedCrossRef

Title: Extracellular Matrix Composition Reveals Complex and Dynamic Stromal-Epithelial Interactions in the Mammary Gland
Authors: Ori Maller
Holly Martinson
Pepper Schedin
Publication date: 01-09-2010
Publisher: Springer US
Published in: Journal of Mammary Gland Biology and Neoplasia / Issue 3/2010
Print ISSN: 1083-3021
Electronic ISSN: 1573-7039
DOI: https://doi.org/10.1007/s10911-010-9189-6

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