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CD151 represses mammary gland development by maintaining the niches of progenitor cells

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Pages 2707-2722 | Received 26 Apr 2014, Accepted 08 Jun 2014, Published online: 30 Oct 2014

References

  • Watson CJ, Khaled WT. Mammary development in the embryo and adult: a journey of morphogenesis and commitment. Development 2008; 135:995-1003; PMID: 18296651; http://dx.doi.org/10.1242/dev.005439
  • Sternlicht MD. Key stages in mammary gland development - The cues that regulate ductal branching morphogenesis. Breast Cancer Res 2006; 8:201; PMID: 16524451; http://dx.doi.org/10.1186/bcr1368
  • McNally S, Martin F. Molecular regulators of pubertal mammary gland development. Ann Med 2011; 43:212-34; PMID: 21417804; http://dx.doi.org/10.3109/07853890.2011.554425
  • Asselin-Labat ML, Vaillant F, Shackleton M, Bouras T, Lindeman GJ, Visvader JE. Delineating the epithelial hierarchy in the mouse mammary gland. Cold Spring Harb Symp Quant Biol 2008; 73:469-78; PMID: 19022771; http://dx.doi.org/10.1101/sqb.2008.73.020
  • Lu P, Takai K, Weaver VM, Werb Z. Extracellular matrix degradation and remodeling in development and disease. Cold Spring Harb Perspect Biol 2011; 3:25; PMID: 21917992; http://dx.doi.org/10.1101/cshperspect.a005058
  • Muschler J, Streuli CH. Cell-matrix interactions in mammary gland development and breast cancer. Cold Spring Harb Perspect Bio 2010; 2:a003202; PMID: 20702598; http://dx.doi.org/10.1101/cshperspect.a003202
  • Raymond K, Faraldo MM, Deugnier MA, Glukhova MA. Integrins in mammary development. Semin Cell Dev Biol 2012; 23:599-605; PMID: 22430758; http://dx.doi.org/10.1016/j.semcdb.2012.03.008
  • Rooney N, Streuli CH. How integrins control mammary epithelial differentiation: a possible role for the ILK-PINCH-Parvin complex. FEBS Lett 2011; 585:1663-72; PMID: 21570968; http://dx.doi.org/10.1016/j.febslet.2011.05.014
  • Taddei I, Deugnier MA, Faraldo MM, Petit V, Bouvard D, Medina D, Fassler R, Thiery JP, Glukhova MA. beta 1 integrin deletion from the basal compartment of the mammary epithelium affects stem cells. Nat Cell Biol 2008; 10:716-22; PMID: 18469806; http://dx.doi.org/10.1038/ncb1734
  • Li N, Zhang Y, Naylor MJ, Schatzmann F, Maurer F, Wintermantel T, Schuetz G, Mueller U, Streuli CH, Hynes NE. beta 1 integrins regulate mammary gland proliferation and maintain the integrity of mammary alveoli. Embo J 2005; 24:1942-53; PMID: 15889143; http://dx.doi.org/10.1038/sj.emboj.7600674
  • Naylor MJ, Li N, Cheung J, Lowe ET, Lambert E, Marlow R, Wang P, Schatzmann F, Wintermantel T, Schuetz G, et al. Ablation of beta1 integrin in mammary epithelium reveals a key role for integrin in glandular morphogenesis and differentiation. J Cell Biol 2005; 171:717-28; PMID: 16301336; http://dx.doi.org/10.1083/jcb.200503144
  • Nagy T, Wei H, Shen TL, Peng X, Liang CC, Gan B, Guan JL. 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 2007; 282:31766-76; PMID: 17716968; http://dx.doi.org/10.1074/jbc.M705403200
  • Akhtar N, Marlow R, Lambert E, Schatzmann F, Lowe ET, Cheung J, Katz E, Li W, Wu C, Dedhar S, et al. Molecular dissection of integrin signalling proteins in the control of mammary epithelial development and differentiation. Development 2009; 136:1019-27; PMID: 19211680; http://dx.doi.org/10.1242/dev.028423
  • Hynes RO. Integrins: Bidirectional, allosteric signaling machines. Cell 2002; 110:673-87; PMID: 12297042; http://dx.doi.org/10.1016/S0092-8674(02)00971-6
  • Georges-Labouesse E, Messaddeq N, Yehia G, Cadalbert L, Dierich A, Le Meur M. Absence of integrin alpha 6 leads to epidermolysis bullosa and neonatal death in mice. Nat Genet 1996; 13:370-3; PMID: 8673141; http://dx.doi.org/10.1038/ng0796-370
  • DiPersio CM, Hodivala-Dilke KM, Jaenisch R, Kreidberg JA, Hynes RO. alpha3beta1 Integrin is required for normal development of the epidermal basement membrane. J Cell Biol 1997; 137:729-42; PMID: 9151677; http://dx.doi.org/10.1083/jcb.137.3.729
  • Kreidberg JA, Donovan MJ, Goldstein SL, Rennke H, Shepherd K, Jones RC, Jaenisch R. Alpha 3 beta 1 integrin has a crucial role in kidney and lung organogenesis. Development 1996; 122:3537-47; PMID: 8951069
  • Klinowska TC, Alexander CM, Georges-Labouesse E, Van der Neut R, Kreidberg JA, Jones CJ, Sonnenberg A, Streuli CH. Epithelial development and differentiation in the mammary gland is not dependent on alpha 3 or alpha 6 integrin subunits. Dev Biol 2001; 233:449-67; PMID: 11336507; http://dx.doi.org/10.1006/dbio.2001.0204
  • Raymond K, Cagnet S, Kreft M, Janssen H, Sonnenberg A, Glukhova MA. Control of mammary myoepithelial cell contractile function by alpha3beta1 integrin signalling. EMBO J 2011; 30:1896-906; PMID: 21487391; http://dx.doi.org/10.1038/emboj.2011.113
  • Stingl J, Eirew P, Ricketson I, Shackleton M, Vaillant F, Choi D, Li HI, Eaves CJ. Purification and unique properties of mammary epithelial stem cells. Nature 2006; 439:993-7; PMID: 16395311
  • Jeselsohn R, Brown NE, Arendt L, Klebba I, Hu MG, Kuperwasser C, Hinds PW. Cyclin D1 kinase activity is required for the self-renewal of mammary stem and progenitor cells that are targets of MMTV-ErbB2 tumorigenesis. Cancer Cell 2010; 17:65-76; PMID: 20129248; http://dx.doi.org/10.1016/j.ccr.2009.11.024
  • Shackleton M, Vaillant F, Simpson KJ, Stingl J, Smyth GK, Asselin-Labat ML, Wu L, Lindeman GJ, Visvader JE. Generation of a functional mammary gland from a single stem cell. Nature 2006; 439:84-8; PMID: 16397499; http://dx.doi.org/10.1038/nature04372
  • Hemler ME. Tetraspanin functions and associated microdomains. Nat Rev Mol Cell Biol 2005; 6:801-11; PMID: 16314869; http://dx.doi.org/10.1038/nrm1736
  • Deng X, Li Q, Hoff J, Novak M, Yang H, Jin H, Erfani SF, Sharma C, Zhou P, Rabinovitz I, et al. Integrin-associated CD151 drives ErbB2-evoked mammary tumor Onset and metastasis. Neoplasia 2012; 14:678-89; PMID: 22952421
  • Yang XWH, Richardson AL, Torres-Arzayus MI, Zhou PC, Sharma C, Kazarov AR, Andzelm MM, Strominger JL, Brown M, Hemler ME. CD151 accelerates breast cancer by regulating alpha(6) integrin function, signaling, and molecular organization. Cancer Res 2008; 68:3204-13; PMID: 18451146; http://dx.doi.org/10.1158/0008-5472.CAN-07-2949
  • Stipp CS. Laminin-binding integrins and their tetraspanin partners as potential antimetastatic targets. Expert RevMol Med 2010; 12:e3; PMID: 20078909; http://dx.doi.org/10.1017/S1462399409001355
  • Kazarov AR, Yang X, Stipp CS, Sehgal B, Hemler ME. An extracellular site on tetraspanin CD151 determines alpha 3 and alpha 6 integrin-dependent cellular morphology. J Cell Biol 2002; 158:1299-309; PMID: 12356873; http://dx.doi.org/10.1083/jcb.200204056
  • Sachs N, Kreft M, van den Bergh Weerman MA, Beynon AJ, Peters TA, Weening JJ, Sonnenberg A. Kidney failure in mice lacking the tetraspanin CD151. J Cell Biol 2006; 175:33-9; PMID: 17015618; http://dx.doi.org/10.1083/jcb.200603073
  • Crew VK, Burton N, Kagan A, Green CA, Levene C, Flinter F, Brady RL, Daniels G, Anstee DJ. CD 151, the first member of the tetraspanin (TM4) superfamily detected on erythrocytes, is essential for the correct assembly of human basement membranes in kidney and skin. Blood 2004; 104:2217-23; PMID: 15265795; http://dx.doi.org/10.1182/blood-2004-04-1512
  • Baleato RM, Guthrie PL, Gubler MC, Ashman LK, Roselli S. Deletion of Cd151 results in a strain-dependent glomerular disease due to severe alterations of the glomerular basement membrane. Am J Pathol 2008; 173:927-37; PMID: 18787104; http://dx.doi.org/10.2353/ajpath.2008.071149
  • Zhang XA, Kazarov AR, Yang X, Bontrager AL, Stipp CS, Hemler ME. Function of the tetraspanin CD151-a6b1 integrin complex during cellular morphogenesis. Mol Biol Cell 2004; 15
  • Xu D, Sharma C, Hemler ME. Tetraspanin12 regulates ADAM10-dependent cleavage of amyloid precursor protein. Faseb J 2009; 23:3674-81; PMID: 19587294; http://dx.doi.org/10.1096/fj.09-133462
  • Knoblich K, Wang HX, Sharma C, Fletcher AL, Turley SJ, Hemler ME. Tetraspanin TSPAN12 regulates tumor growth and metastasis and inhibits beta-catenin degradation. Cell Mol Life Sci 2013; 71:1305-14; PMID: 23955570
  • Van Keymeulen A, Rocha AS, Ousset M, Beck B, Bouvencourt G, Rock J, Sharma N, Dekoninck S, Blanpain C. Distinct stem cells contribute to mammary gland development and maintenance. Nature 2011; 479:189-93; PMID: 21983963; http://dx.doi.org/10.1038/nature10573
  • Liu K, Cheng L, Flesken-Nikitin A, Huang L, Nikitin AY, Pauli BU. Conditional knockout of fibronectin abrogates mouse mammary gland lobuloalveolar differentiation. Dev Biol 2010; 346:11-24; PMID: 20624380; http://dx.doi.org/10.1016/j.ydbio.2010.07.001
  • Park J, Schwarzbauer JE. Mammary epithelial cell interactions with fibronectin stimulate epithelial-mesenchymal transition. Oncogene 2013; 33(13):1649-57.
  • Guan JL. Integrin signaling through FAK in the regulation of mammary stem cells and breast cancer. IUBMB Life 2010; 62:268-76; PMID: 20101634; http://dx.doi.org/10.1002/iub.311
  • Zeisberg M, Neilson EG. Biomarkers for epithelial-mesenchymal transitions. J Clin Invest 2009; 119:1429-37; PMID: 19487819; http://dx.doi.org/10.1172/JCI36183
  • Nassour M, Idoux-Gillet Y, Selmi A, Come C, Faraldo ML, Deugnier MA, Savagner P. Slug controls stem/progenitor cell growth dynamics during mammary gland morphogenesis. PloS One 2012; 7:e53498; PMID: 23300933; http://dx.doi.org/10.1371/journal.pone.0053498
  • Guo W, Keckesova Z, Donaher JL, Shibue T, Tischler V, Reinhardt F, Itzkovitz S, Noske A, Zurrer-Hardi U, Bell G, et al. Slug and Sox9 cooperatively determine the mammary stem cell state. Cell 2012; 148:1015-28; PMID: 22385965; http://dx.doi.org/10.1016/j.cell.2012.02.008
  • Tsujino K, Takeda Y, Arai T, Shintani Y, Inagaki R, Saiga H, Iwasaki T, Tetsumoto S, Jin Y, Ihara S, et al. Tetraspanin CD151 protects against pulmonary fibrosis by maintaining epithelial integrity. Am J Respir Crit Care Med 2012; 186:170-80; PMID: 22592804; http://dx.doi.org/10.1164/rccm.201201-0117OC
  • Meyer SE, Zinser GM, Stuart WD, Pathrose P, Waltz SE. The Ron receptor tyrosine kinase negatively regulates mammary gland branching morphogenesis. Dev Biol 2009; 333:173-85; PMID: 19576199; http://dx.doi.org/10.1016/j.ydbio.2009.06.028
  • Wagh PK, Gray JK, Zinser GM, Vasiliauskas J, James L, Monga SP, Waltz SE. β-Catenin is required for Ron receptor-induced mammary tumorigenesis. Oncogene 2011; 30:3694-704; PMID: 21423209; http://dx.doi.org/10.1038/onc.2011.86
  • Wu ZQ, Li XY, Hu CY, Ford M, Kleer CG, Weiss SJ. Canonical Wnt signaling regulates Slug activity and links epithelial-mesenchymal transition with epigenetic Breast Cancer 1, Early Onset (BRCA1) repression. Proc Nat Acad Sci U S A 2012; 109:16654-9; PMID: 23011797; http://dx.doi.org/10.1073/pnas.1205822109
  • Macias H, Moran A, Samara Y, Moreno M, Compton JE, Harburg G, Strickland P, Hinck L. SLIT/ROBO1 signaling suppresses mammary branching morphogenesis by limiting basal cell number. Dev Cell 2011; 20:827-40; PMID: 21664580; http://dx.doi.org/10.1016/j.devcel.2011.05.012
  • Weaver VM, Lelievre S, Lakins JN, Chrenek MA, Jones JC, Giancotti F, Werb Z, Bissell MJ. beta4 integrin-dependent formation of polarized three-dimensional architecture confers resistance to apoptosis in normal and malignant mammary epithelium. Cancer Cell 2002; 2:205-16; PMID: 12242153; http://dx.doi.org/10.1016/S1535-6108(02)00125-3
  • Sachs N, Secades P, van Hulst L, Kreft M, Song JY, Sonnenberg A. Loss of integrin alpha3 prevents skin tumor formation by promoting epidermal turnover and depletion of slow-cycling cells. Proc Nat Acad Sci U S A 2012; 109(52):21468-73.
  • Hodivala-Dilke KM, DiPersio CM, Kreidberg JA, Hynes RO. Novel roles for alpha 3 beta 1 integrin as a regulator of cytoskeletal assembly and as a trans-dominant inhibitor of integrin receptor function in mouse keratinocytes. J Cell Biol 1998; 142:1357-69; PMID: 9732295; http://dx.doi.org/10.1083/jcb.142.5.1357
  • Proia TA, Keller PJ, Gupta PB, Klebba I, Jones AD, Sedic M, Gilmore H, Tung N, Naber SP, Schnitt S, et al. Genetic predisposition directs breast cancer phenotype by dictating progenitor cell fate. Cell Stem Cell 2011; 8:149-63; PMID: 21295272; http://dx.doi.org/10.1016/j.stem.2010.12.007
  • Turner FE, Broad S, Khanim FL, Jeanes A, Talma S, Hughes S, Tselepis C, Hotchin NA. Slug regulates integrin expression and cell proliferation in human epidermal keratinocytes. J Biol Chem 2006; 281:21321-31; PMID: 16707493; http://dx.doi.org/10.1074/jbc.M509731200
  • Santoro MM, Gaudino G, Marchisio PC. The MSP receptor regulates alpha6beta4 and alpha3beta1 integrins via 14-3-3 proteins in keratinocyte migration. Dev Cell 2003; 5:257-71; PMID: 12919677; http://dx.doi.org/10.1016/S1534-5807(03)00201-6
  • Romanska HM, Berditchevski F. Tetraspanins in human epithelial malignancies. J Pathol 2011; 223:4-14; PMID: 20938929; http://dx.doi.org/10.1002/path.2779
  • Sadej R, Romanska H, Kavanagh D, Baldwin G, Takahashi T, Kalia N, Berditchevski F. Tetraspanin CD151 regulates transforming growth factor beta signaling: implication in tumor metastasis. Cancer Res 2010; 70:6059-70; PMID: 20570898; http://dx.doi.org/10.1158/0008-5472.CAN-09-3497
  • Novitskaya V, Romanska H, Dawoud M, Jones JL, Berditchevski F. Tetraspanin CD151 regulates growth of mammary epithelial cells in three-dimensional extracellular matrix: implication for mammary ductal carcinoma in situ. Cancer Res 2010; 70:4698-708; PMID: 20501858; http://dx.doi.org/10.1158/0008-5472.CAN-09-4330
  • Minner S, De Silva C, Rink M, Dahlem R, Chun F, Fisch M, Hoppner W, Wagner W, Bokemeyer C, Terracciano L, et al. Reduced CD151 expression is related to advanced tumour stage in urothelial bladder cancer. Pathology 2012; 44:448-52; PMID: 22772340; http://dx.doi.org/10.1097/PAT.0b013e32835576ee
  • Semenza GL. Does loss of CD151 expression promote the metastasis of hypoxic colon cancer cells? Clinical Cancer Res 2008; 14:7969-70; PMID: 19088010; http://dx.doi.org/10.1158/1078-0432.CCR-08-2417
  • Voss MA, Gordon N, Maloney S, Ganesan R, Ludeman L, McCarthy K, Gornall R, Schaller G, Wei W, Berditchevski F, et al. Tetraspanin CD151 is a novel prognostic marker in poor outcome endometrial cancer. Brit J Cancer 2011; 104:1611-8; PMID: 21505452; http://dx.doi.org/10.1038/bjc.2011.80
  • Raymond K, Kreft M, Song JY, Janssen H, Sonnenberg A. Dual Role of alpha6beta4 integrin in epidermal tumor growth: tumor-suppressive versus tumor-promoting function. Mol Biol Cell 2007; 18:4210-21; PMID: 17699601; http://dx.doi.org/10.1091/mbc.E06-08-0720
  • Keely PJ. Mechanisms by which the extracellular matrix and integrin signaling act to regulate the switch between tumor suppression and tumor promotion. J Mammary Gland Biol Neoplasia 2011; 16:205-19; PMID: 21822945; http://dx.doi.org/10.1007/s10911-011-9226-0
  • Izumchenko E, Singh MK, Plotnikova OV, Tikhmyanova N, Little JL, Serebriiskii IG, Seo S, Kurokawa M, Egleston BL, Klein-Szanto A, et al. NEDD9 promotes oncogenic signaling in mammary tumor development. Cancer Res 2009; 69:7198-206; PMID: 19738060; http://dx.doi.org/10.1158/0008-5472.CAN-09-0795
  • Seo S, Nakamoto T, Takeshita M, Lu J, Sato T, Suzuki T, Kamikubo Y, Ichikawa M, Noda M, Ogawa S, et al. Crk-associated substrate lymphocyte type regulates myeloid cell motility and suppresses the progression of leukemia induced by p210Bcr/Abl. Cancer Sci 2011; 102:2109-17; PMID: 21848808; http://dx.doi.org/10.1111/j.1349-7006.2011.02066.x
  • Takeda Y, Kazarov AR, Butterfield CE, Hopkins BD, Benjamin LE, Kaipainen A, Hemler ME. Deletion of tetraspanin Cd151 results in decreased pathologic angiogenesis in vivo and in vitro. Blood 2007; 109:1524-32; PMID: 17023588; http://dx.doi.org/10.1182/blood-2006-08-041970
  • Yang XH, Richardson AL, Torres-Arzayus MI, Zhou P, Sharma C, Kazarov AR, Andzelm MM, Strominger JL, Brown M, Hemler ME. CD151 accelerates breast cancer by regulating alpha 6 integrin function, signaling, and molecular organization. Cancer Res 2008; 68:3204-13; PMID: 18451146; http://dx.doi.org/10.1158/0008-5472.CAN-07-2949z
  • Yang XH, Flores LM, Li Q, Zhou P, Xu F, Krop IE, Hemler ME. Disruption of laminin-integrin-CD151-focal adhesion kinase axis sensitizes breast cancer cells to ErbB2 antagonists. Cancer Res 2010; 70:2256-63; PMID: 20197472; http://dx.doi.org/10.1158/0008-5472.CAN-09-4032
  • Dontu G, Abdallah WM, Foley JM, Jackson KW, Clarke MF, Kawamura MJ, Wicha MS. In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Genes Dev 2003; 17:1253-70; PMID: 12756227; http://dx.doi.org/10.1101/gad.1061803
  • Debnath J, Muthuswamy SK, Brugge JS. Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in three-dimensional basement membrane cultures. Methods 2003; 30:256-68; PMID: 12798140; http://dx.doi.org/10.1016/S1046-2023(03)00032-X
  • Yang XH, Kovalenko OV, Kolesnikova TV, Andzelm MM, Rubinstein E, Strominger JL, Hemler ME. Contrasting effects of EWI proteins, integrins, and protein palmitoylation on cell surface CD9 organization. J Biol Chem 2006; 281:12976-85; PMID: 16537545; http://dx.doi.org/10.1074/jbc.M510617200

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