BMP-binding protein twisted gastrulation is required in mammary gland epithelium for normal ductal elongation and myoepithelial compartmentalization

Developmental Biology

Volumn 373, Issue 1, 2013, Pages 95-106

  Forsman, Cynthia L ^a,b,c   Ng, Brandon C ^a,b   Heinze, Rachel K ^a,b   Kuo, Claire ^a,b   Sergi, Consolato ^d   Gopalakrishnan, Rajaram ^a   Yee, Douglas ^b,c   Graf, Daniel ^e   Schwertfeger, Kathryn L ^b,c   Petryk, Anna ^a,b,c  

^a UNIVERSITY OF MINNESOTA   (United States)

^b UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF MINNESOTA   (United States)

^d UNIVERSITY OF ALBERTA   (Canada)

^e UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

BMP; Breast; Mammary gland development; Myoepithelium; TWSG1

Indexed keywords

BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 6; BONE MORPHOGENETIC PROTEIN RECEPTOR 1A; SMAD1 PROTEIN; SMAD4 PROTEIN; SMAD5 PROTEIN; SMAD8 PROTEIN; TRANSCRIPTION FACTOR GATA 3;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BREAST EPITHELIUM; CELL COMPARTMENTALIZATION; CELL COUNT; CELL PROLIFERATION; CONTROLLED STUDY; FEMALE; GASTRULATION; GENE EXPRESSION; GENE TARGETING; MOUSE; MYOEPITHELIUM CELL; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS REGULATION; PUBERTY; SIGNAL TRANSDUCTION; TWISTED GASTRULATION;

EID: 84870055106     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2012.10.007     Document Type: Article

References (83)

1. Asselin-Labat M.-L., Sutherland K.D., Vaillant F., Gyorki D.E., Wu D., Holroyd S., Breslin K., Ward T., Shi W., Bath M.L., Deb S., Fox S.B., Smyth G.K., Lindeman G.J., Visvader J.E. Gata-3 negatively regulates the tumor-initiating capacity of mammary luminal progenitor cells and targets the putative tumor suppressor caspase-14. Mol. Cell. Biol. 2011, (MCB.05766-11).
2. Asselin-Labat M.L., Sutherland K.D., Barker H., Thomas R., Shackleton M., Forrest N.C., Hartley L., Robb L., Grosveld F.G., van der Wees J., Lindeman G.J., Visvader J.E. Gata-3 is an essential regulator of mammary-gland morphogenesis and luminal-cell differentiation. Nat. Cell Biol. 2007, 9:201-209.
3. Bailey J.M., Singh P.K., Hollingsworth M.A. Cancer metastasis facilitated by developmental pathways: sonic hedgehog, notch, and bone morphogenic proteins. J. Cell. Biochem. 2007, 102:829-839.
4. Balemans W., Van Hul W. Extracellular regulation of BMP signaling in vertebrates: a cocktail of modulators. Dev. Biol. 2002, 250:231-250.
5. Beppu H., Mwizerwa O.N., Beppu Y., Dattwyler M.P., Lauwers G.Y., Bloch K.D., Goldstein A.M. Stromal inactivation of BMPRII leads to colorectal epithelial overgrowth and polyp formation. Oncogene 2008, 27:1063-1070.
6. Billington C.J., Fiebig J.E., Forsman C.L., Pham L., Burbach N., Sun M., Jaskoll T., Mansky K., Gopalakrishnan R., O'Connor M.B., Mueller T.D., Petryk A. Glycosylation of twisted gastrulation is required for BMP binding and activity during craniofacial development. Front. Physiol. 2011, 2:59.
7. Billington C.J., Ng B., Forsman C., Schmidt B., Bagchi A., Symer D.E., Schotta G., Gopalakrishnan R., Sarver A.L., Petryk A. The molecular and cellular basis of variable craniofacial phenotypes and their genetic rescue in twisted gastrulation mutant mice. Dev. Biol. 2011, 355:21-31.
8. Blitz I.L., Cho K.W., Chang C. Twisted gastrulation loss-of-function analyses support its role as a BMP inhibitor during early Xenopus embryogenesis. Development 2003, 130:4975-4988.
9. Bonilla-Claudio M., Wang J., Bai Y., Klysik E., Selever J., Martin J.F. BMP signaling regulates a dose-dependent transcriptional program to control facial skeletal development. Development 2012, 139:709-719.
10. 2-catenin nuclear translocation and promotes glioma tumorigenesis. Cancer Cell 2011, 20:415-416.
11. Buijs J.T., van der Horst G., van den Hoogen C., Cheung H., de Rooij B., Kroon J., Petersen M., van Overveld P.G.M., Pelger R.C.M., van der Pluijm G. The BMP2/7 heterodimer inhibits the human breast cancer stem cell subpopulation and bone metastases formation. Oncogene 2012, 31, 2164-2174.
12. Chang C., Holtzman D.A., Chau S., Chickering T., Woolf E.A., Holmgren L.M., Bodorova J., Gearing D.P., Holmes W.E., Brivanlou A.H. Twisted gastrulation can function as a BMP antagonist. Nature 2001, 410:483-487.
13. Cho K.W., Kim J.Y., Song S.J., Farrell E., Eblaghie M.C., Kim H.J., Tickle C., Jung H.S. Molecular interactions between Tbx3 and Bmp4 and a model for dorsoventral positioning of mammary gland development. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:16788-16793.
14. Danielson K.G., Oborn C.J., Durban E.M., Butel J.S., Medina D. Epithelial mouse mammary cell line exhibiting normal morphogenesis in vivo and functional differentiation in vitro. Proc. Natl. Acad. Sci. U. S. A. 1984, 81:3756-3760.
15. DeOme K.B., Faulkin L.J., Bern H.A., Blair P.B. Development of mammary tumors from hyperplastic alveolar nodules transplanted into gland-free mammary fat pads of female C3H mice. Cancer Res. 1959, 19:515.
16. Dulbecco R., Henahan M., Armstrong B. Cell types and morphogenesis in the mammary gland. Proc. Natl. Acad. Sci. 1982, 79:7346-7350.
17. Finak G., Bertos N., Pepin F., Sadekova S., Souleimanova M., Zhao H., Chen H., Omeroglu G., Meterissian S., Omeroglu A., Hallett M., Park M. Stromal gene expression predicts clinical outcome in breast cancer. Nat. Med. 2008, 14:518-527.
18. Fleming, J.M., Ginsburg, E., Goldhar, A.S., Plant, J., Vonderhaar, B.K. 2012. Progesterone receptor activates Msx2 expression by downregulating TNAP/Akp2 and activating the Bmp pathway in EpH4 mouse mammary epithelial cells. PLoS ONE 7, e34058.
19. Gavrieli Y., Sherman Y., Ben-Sasson S.A. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol. 1992, 119:493-501.
20. Gazzerro E., Deregowski V., Stadmeyer L., Gale N.W., Economides A.N., Canalis E. Twisted gastrulation, a bone morphogenetic protein agonist/antagonist, is not required for post-natal skeletal function. Bone 2006, 39:1252-1260.
21. Graham A., Koentges G., Lumsden A. Neural crest apoptosis and the establishment of craniofacial pattern: an honorable death. Mol. Cell. Neurosci. 1996, 8:76-83.
22. Hens J.R., Dann P., Zhang J.P., Harris S., Robinson G.W., Wysolmerski J. BMP4 and PTHrP interact to stimulate ductal outgrowth during embryonic mammary development and to inhibit hair follicle induction. Development 2007, 134:1221-1230.
23. Hens J.R., Wysolmerski J.J. Key stages of mammary gland development: molecular mechanisms involved in the formation of the embryonic mammary gland. Breast Cancer Res. 2005, 7:220-224.
24. Hovey R.C., Trott J.F. Morphogenesis of mammary gland development. Adv. Exp. Med. Biol. 2004, 554:219-228.
25. Humphreys R.C., Krajewska M., Krnacik S., Jaeger R., Weiher H., Krajewski S., Reed J.C., Rosen J.M. Apoptosis in the terminal endbud of the murine mammary gland: a mechanism of ductal morphogenesis. Development 1996, 122:4013-4022.
26. Jardé T., Dale T. Wnt signalling in murine postnatal mammary gland development. Acta Physiol 2012, 204, 118-27.
27. Khialeeva E., Lane T.F., Carpenter E.M. Disruption of reelin signaling alters mammary gland morphogenesis. Development 2011, 138:767-776.
28. Kobielak K., Pasolli H.A., Alonso L., Polak L., Fuchs E. Defining BMP functions in the hair follicle by conditional ablation of BMP receptor IA. J. Cell Biol. 2003, 163:609-623.
29. Kouros-Mehr H., Bechis S.K., Slorach E.M., Littlepage L.E., Egeblad M., Ewald A.J., Pai S.-Y., Ho I.C., Werb Z. GATA-3 links tumor differentiation and dissemination in a luminal breast cancer model. Cancer Cell 2008, 13:141-152.
30. Kouros-Mehr H., Slorach E.M., Sternlicht M.D., Werb Z. GATA-3 maintains the differentiation of the luminal cell fate in the mammary gland. Cell 2006, 127:1041-1055.
31. Kwon H.-J., Bhat N., Sweet E.M., Cornell R.A., Riley B.B. Identification of early requirements for preplacodal ectoderm and sensory organ development. PLoS Genet. 2010, 6:e1001133.
32. Larman B.W., Karolak M.J., Adams D.C., Oxburgh L. Chordin-like 1 and twisted gastrulation 1 regulate BMP signaling following kidney injury. J. Am. Soc. Nephrol. 2009, 20:1020-1031.
33. Larrain J., Oelgeschlager M., Ketpura N.I., Reversade B., Zakin L., De Robertis E.M. Proteolytic cleavage of Chordin as a switch for the dual activities of Twisted gastrulation in BMP signaling. Development 2001, 128:4439-4447.
34. Lawson K.A., Dunn N.R., Roelen B.A.J., Zeinstra L.M., Davis A.M., Wright C.V.E., Korving J.P.W.F.M., Hogan B.L.M. Bmp4 is required for the generation of primordial germ cells in the mouse embryo. Genes Dev. 1999, 13:424-436.
35. Li G., Robinson G.W., Lesche R., Martinez-Diaz H., Jiang Z., Rozengurt N., Wagner K.U., Wu D.C., Lane T.F., Liu X., Hennighausen L., Wu H. Conditional loss of PTEN leads to precocious development and neoplasia in the mammary gland. Development 2002, 129:4159-4170.
36. Little S.C., Mullins M.C. Twisted gastrulation promotes BMP signaling in zebrafish dorsal-ventral axial patterning. Development 2004, 131:5825-5835.
37. Liu F., Bloch N., Bhushan K.R., De Grand A.M., Tanaka E., Solazzo S., Mertyna P.M., Goldberg N., Frangioni J.V., Lenkinski R.E. Humoral bone morphogenetic protein 2 is sufficient for inducing breast cancer microcalcification. Mol. Imaging 2008, 7:175-186.
38. Loh K., Chia J.A., Greco S., Cozzi S.-J., Buttenshaw R.L., Bond C.E., Simms L.A., Pike T., Young J.P., Jass J.R., Spring K.J., Leggett B.A., Whitehall V.L.J. Bone morphogenic protein 3 inactivation is an early and frequent event in colorectal cancer development. Genes Chromosomes Cancer 2008, 47:449-460.
39. MacKenzie B., Wolff R., Lowe N., Billington C.J., Peterson A., Schmidt B., Graf D., Mina M., Gopalakrishnan R., Petryk A. Twisted gastrulation limits apoptosis in the distal region of the mandibular arch in mice. Dev. Biol. 2009, 328:13-23.
40. Mailleux A.A., Overholtzer M., Schmelzle T., Bouillet P., Strasser A., Brugge J.S. BIM regulates apoptosis during mammary ductal morphogenesis, and its absence reveals alternative cell death mechanisms. Dev. Cell 2007, 12:221-234.
41. Malewski T., Milewicz T., Krzysiek J., Gregoraszczuk E.L., Augustowska K. Regulation of Msx2 gene expression by steroid hormones in human nonmalignant and malignant breast cancer explants cultured in vitro. Cancer Invest. 2005, 23:222-228.
42. Massague J., Seoane J., Wotton D. Smad transcription factors. Genes Dev. 2005, 19:2783-2810.
43. McCaffrey L.M., Macara I.G. The Par3/aPKC interaction is essential for end bud remodeling and progenitor differentiation during mammary gland morphogenesis. Genes Dev. 2009, 23:1450-1460.
44. McEvoy J., Flores-Otero J., Zhang J., Nemeth K., Brennan R., Bradley C., Krafcik F., Rodriguez-Galindo C., Wilson M., Xiong S., Lozano G., Sage J., Fu L., Louhibi L., Trimarchi J., Pani A., Smeyne R., Johnson D., Dyer Michael, A. Coexpression of normally incompatible developmental pathways in retinoblastoma genesis. Cancer Cell 2011, 20:260-275.
45. McNally S., Martin F. Molecular regulators of pubertal mammary gland development. Ann. Med. 2011, 43:212-234.
46. Melnick M., Petryk A., Abichaker G., Witcher D., Person A.D., Jaskoll T. Embryonic salivary gland dysmorphogenesis in Twisted gastrulation deficient mice. Arch. Oral. Biol. 2006, 51:433-438.
47. Metallo C.M., Ji L., de Pablo J.J., Palecek S.P. Retinoic acid and bone morphogenetic protein signaling synergize to efficiently direct epithelial differentiation of human embryonic stem cells. Stem Cells 2008, 26:372-380.
48. Miyazono K., Maeda S., Imamura T. BMP receptor signaling: transcriptional targets, regulation of signals, and signaling cross-talk. Cytokine Growth Factor Rev. 2005, 16:251-263.
49. Montesano R. Bone morphogenetic protein-4 abrogates lumen formation by mammary epithelial cells and promotes invasive growth. Biochem. Biophys. Res. Commun. 2007, 353:817-822.
50. Nelson J.F., Karelus K., Felicio L.S., Johnson T.E. Genetic influences on the timing of puberty in mice. Biol. Reprod. 1990, 42:649-655.
51. Nosaka T., Morita S., Kitamura H., Nakajima H., Shibata F., Morikawa Y., Kataoka Y., Ebihara Y., Kawashima T., Itoh T., Ozaki K., Senba E., Tsuji K., Makishima F., Yoshida N., Kitamura T. Mammalian twisted gastrulation is essential for skeleto-lymphogenesis. Mol. Cell. Biol. 2003, 23:2969-2980.
52. Oelgeschlager M., Larrain J., Geissert D., De Robertis E.M. The evolutionarily conserved BMP-binding protein Twisted gastrulation promotes BMP signalling. Nature 2000, 405:757-763.
53. Owens P., Pickup M.W., Novitskiy S.V., Chytil A., Gorska A.E., Aakre M.E., West J., Moses H.L. Disruption of bone morphogenetic protein receptor 2 (BMPR2) in mammary tumors promotes metastases through cell autonomous and paracrine mediators. Proc. Natl. Acad. Sci. 2012, 109, 2814-2819.
54. Petryk A., Anderson R.M., Jarcho M.P., Leaf I., Carlson C.S., Klingensmith J., Shawlot W., O'Connor M.B. The mammalian twisted gastrulation gene functions in foregut and craniofacial development. Dev. Biol. 2004, 267:374-386.
55. Phippard D.J., Weber-Hall S.J., Sharpe P.T., Naylor M.S., Jayatalake H., Maas R., Woo I., Roberts-Clark D., Francis-West P.H., Liu Y.H., Maxson R., Hill R.E., Dale T.C. Regulation of Msx-1, Msx-2, Bmp-2 and Bmp-4 during foetal and postnatal mammary gland development. Development 1996, 122:2729-2737.
56. Pierce D.F., Johnson M.D., Matsui Y., Robinson S.D., Gold L.I., Purchio A.F., Daniel C.W., Hogan B.L., Moses H.L. Inhibition of mammary duct development but not alveolar outgrowth during pregnancy in transgenic mice expressing active TGF-beta 1. Genes Dev. 1993, 7:2308-2317.
57. Rasband W.S. ImageJ 1997-2011, U.S. National Institutes of Health, Bethesda, Maryland, USA, (Vol).
58. Richards R.G., Klotz D.M., Walker M.P., DiAugustine R.P. Mammary gland branching morphogenesis is diminished in mice with a deficiency of insulin-like growth factor-I (IGF-I), but not in mice with a liver-specific deletion of IGF-I. Endocrinology 2004, 145:3106-3110.
59. Ross J.J., Shimmi O., Vilmos P., Petryk A., Kim H., Gaudenz K., Hermanson S., Ekker S.C., O'Connor M.B., Marsh J.L. Twisted gastrulation is a conserved extracellular BMP antagonist. Nature 2001, 410:479-483.
60. Satoh K., Ginsburg E., Vonderhaar B.K. Msx-1 and Msx-2 in mammary gland development. J. Mammary Gland Biol. Neoplasia 2004, 9:195-205.
61. Satokata I., Ma L., Ohshima H., Bei M., Woo I., Nishizawa K., Maeda T., Takano Y., Uchiyama M., Heaney S., Peters H., Tang Z., Maxson R., Maas R. Msx2 deficiency in mice causes pleiotropic defects in bone growth and ectodermal organ formation. Nat. Genet. 2000, 24:391-395.
62. Schwertfeger K.L. Fibroblast growth factors in development and cancer: insights from the mammary and prostate glands. Curr. Drug Targets 2009, 10:632-644.
63. Scott I.C., Blitz I.L., Pappano W.N., Maas S.A., Cho K.W., Greenspan D.S. Homologues of Twisted gastrulation are extracellular cofactors in antagonism of BMP signalling. Nature 2001, 410:475-478.
64. Shimmi O., Umulis D., Othmer H., O'Connor M.B. Facilitated transport of a Dpp/Scw heterodimer by Sog/Tsg leads to robust patterning of the drosophila blastoderm embryo. Cell 2005, 120:873-886.
65. Singh A., Morris R.J. The Yin and Yang of bone morphogenetic proteins in cancer. Cytokine Growth Factor Rev. 2010, 21:299-313.
66. Sotillo Rodriguez J.E., Mansky K.C., Jensen E.D., Carlson A.E., Schwarz T., Pham L., MacKenzie B., Prasad H., Rohrer M.D., Petryk A., Gopalakrishnan R. Enhanced osteoclastogenesis causes osteopenia in twisted gastrulation-deficient mice through increased BMP signaling. J. Bone Miner. Res. 2009, 24:1917-1926.
67. Stingl J., Emerman J.T., Eaves C.J., Kuusk U. Phenotypic and functional characterization in vitro of a multipotent epithelial cell present in the normal adult human breast. Differentiation 1998, 63:201-213.
68. Sun M., Forsman C., Sergi C., Gopalakrishnan R., O'Connor M.B., Petryk A. The expression of twisted gastrulation in postnatal mouse brain and functional implications. Neuroscience 2010, 169:920-931.
69. Tsalavos S., Segklia K., Passa O., Petryk A., O'Connor M.B., Graf D. Involvement of twisted gastrulation in T cell-independent plasma cell production. J. Immunol. 2011, 186:6860-6870.
70. van Genderen C., Okamura R.M., Fariñas I., Quo R.G., Parslow T.G., Bruhn L., Grosschedl R. Development of several organs that require inductive epithelial-mesenchymal interactions is impaired in LEF-1-deficient mice. Genes Dev. 1994, 8:2691-2703.
71. Virtanen S., Alarmo E.-L., Sandstrã¶m S., Ampuja M., Kallioniemi A. Bone morphogenetic protein -4 and -5 in pancreatic cancer-novel bidirectional players. Exp. Cell Res. 2011, 317:2136-2146.
72. Wagner D.O., Sieber C., Bhushan R., Borgermann J.H., Graf D., Knaus P. BMPs: from bone to body morphogenetic proteins. Sci. Signal 2010, 3. p. mr1.
73. Wang K., Feng H., Ren W., Sun X., Luo J., Tang M., Zhou L., Weng Y., He T.-C., Zhang Y. BMP9 inhibits the proliferation and invasiveness of breast cancer cells MDA-MB-231. J. Cancer Res. Clin. Oncol. 2011, 137:1687-1696.
74. Wang N.J., Sanborn Z., Arnett K.L., Bayston L.J., Liao W., Proby C.M., Leigh I.M., Collisson E.A., Gordon P.B., Jakkula L., Pennypacker S., Zou Y., Sharma M., North J.P., Vemula S.S., Mauro T.M., Neuhaus I.M., LeBoit P.E., Hur J.S., Park K., Huh N., Kwok P.-Y., Arron S.T., Massion P.P., Bale A.E., Haussler D., Cleaver J.E., Gray J.W., Spellman P.T., South A.P., Aster J.C., Blacklow S.C., Cho R.J. Loss-of-function mutations in Notch receptors in cutaneous and lung squamous cell carcinoma. Proc. Natl. Acad. Sci. 2011, 108:17761-17766.
75. Watson C.J., Oliver C.H., Khaled W.T. Cytokine signalling in mammary gland development. J. Reprod. Immunol. 2011, 88:124-129.
76. Wilson P.A., Hemmati-Brivanlou A. Induction of epidermis and inhibition of neural fate by Bmp-4. Nature 1995, 376:331-333.
77. Xie J., Fisher S. Twisted gastrulation enhances BMP signaling through chordin dependent and independent mechanisms. Development 2005, 132:383-391.
78. Ye L., Kynaston H., Jiang W.G. Bone morphogenetic protein-10 suppresses the growth and aggressiveness of prostate cancer cells through a Smad independent pathway. J. Urol. 2009, 181:2749-2759.
79. Zakin L., De Robertis E.M. Inactivation of mouse Twisted gastrulation reveals its role in promoting Bmp4 activity during forebrain development. Development 2004, 131:413-424.
80. Zhang H., Bradley A. Mice deficient for BMP2 are nonviable and have defects in amnion/chorion and cardiac development. Development 1996, 122:2977-2986.
81. Zhang J.-L., Patterson L.J., Qiu L.-Y., Graziussi D., Sebald W., Hammerschmidt M. Binding between crossveinless-2 and Chordin Von Willebrand factor type C domains promotes BMP signaling by blocking chordin activity. PLoS ONE 2010, 5:e12846.
82. Zhang Z., Song Y., Zhao X., Zhang X., Fermin C., Chen Y. Rescue of cleft palate in Msx1-deficient mice by transgenic Bmp4 reveals a network of BMP and Shh signaling in the regulation of mammalian palatogenesis. Development 2002, 129:4135-4146.
83. Zusman S.B., Wieschaus E.F. Requirements for zygotic gene activity during gastrulation in Drosophila melanogaster. Dev. Biol. 1985, 111:359-371.