The pattern of β-catenin responsiveness within the mammary gland is regulated by progesterone receptor

Development

Volumn 134, Issue 20, 2007, Pages 3703-3712

  Hiremath, Minoti ^a   Lydon, John P ^b   Cowin, Pamela ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Beta catenin; Breast; Mammary gland; Mouse; Progesterone receptor; Stem cells; Wnt

Indexed keywords

BETA CATENIN; PROGESTERONE RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BREAST CELL; BREAST DEVELOPMENT; BREAST DUCT; CELL DIFFERENTIATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; FEMALE; MALE; MAMMARY GLAND; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; ORGANOGENESIS; PREGNANCY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION;

ANIMALS; BETA CATENIN; CELL DIFFERENTIATION; FEMALE; MALE; MAMMARY GLANDS, ANIMAL; MICE; MICE, KNOCKOUT; MILK PROTEINS; PREGNANCY; RECEPTORS, PROGESTERONE; SIGNAL TRANSDUCTION; TRANSGENES;

MUS;

EID: 36148973174     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.006585     Document Type: Article

References (96)

1. Atwood, C. S., Hovey, R. C., Glover, J. P., Chepko, G., Ginsburg, E., Robison, W. G. and Vonderhaar, B. K. (2000). Progesterone induces side-branching of the ductal epithelium in the mammary glands of peripubertal mice. J. Endocrinol. 167, 39-52.
2. Aupperlee, M. D. and Haslam, S. Z. (2007). Differential hormonal regulation and function of PR isoforms in normal adult mouse mammary gland. Endocrinology 148, 2290-2300.
3. Barker, N., Huls, G., Korinek, V. and Clevers, H. (1999). Restricted high level expression of Tcf-4 protein in intestinal and mammary gland epithelium. Am. J. Pathol. 154, 29-35.
4. Bocchinfuso, W. P. and Korach, K. S. (1997). Mammary gland development and tumorigenesis in estrogen receptor knockout mice. J. Mammary Gland Biol. Neoplasia 2, 323-334.
5. Bocchinfuso, W. P., Lindzey, J. K., Hewitt, S. C., Clark, J. A., Myers, P. H., Cooper, R. and Korach, K. S. (2000). Induction of mammary gland development in estrogen receptor-alpha knockout mice. Endocrinology 141, 2982-2994.
6. Boulanger, C. A., Wagner, K. U. and Smith, G. H. (2005). Parity-induced mouse mammary elpithelial cells are pluripotent, self-renewing and sensitive to TGF-beta 1 expression. Oncogene 24, 552-560.
7. Bradbury, J. M., Edwards, P. A., Niemeyer, C. C. and Dale, T. C. (1995). Wnt-4 expression induces a pregnancy-like growth pattern in reconstituted mammary glands in virgin mice. Dev Biol. 170, 553-563.
8. Brisken, C. (2002). Hormonal control of alveolar development and its implications for breast carcinogenesis. J. Mammary Gland Biol. Neoplasia 7, 39-48.
9. Brisken, C. and Rajaram, R. D. (2006). Alveolar and lactogenic differentiation. J. Mammary Gland Biol. Neoplasia 11, 239-248.
10. Brisken, C., Park, S., Vass, T., Lydon, J. P., O'Malley, B. W. and Weinberg, R. A. (1998). A paracrine role for the elpithelial progesterone receptor in mammary gland development. Proc. Natl. Acad. Sci. USA 95, 5076-5081.
11. Brisken, C., Kaur, S., Chavarria, T. E., Binart, N., Sutherland, R. L., Weinberg, R. A., Kelly, P. A. and Ormandy, C. J. (1999). Prolactin controls mammary gland development via direct and indirect mechanisms. Dev Biol. 210, 96-106.
12. Brisken, C., Heineman, A., Chavarra, T., Elenbaas, B., Tan, J., Dey, S. K., McMahon, A. P. and Weinberg, R. (2000). Essential function of Wnt-4 in mammary gland development downstream of progesterone signaling. Genes Dev 14, 650-654.
13. Brisken, C., Ayyannan, A., Nguyen, C., Heineman, A., Reinhardt, F., Tan, J., Dey, S. K., Dotto, G. P. and Weinberg, R. A. (2002). IGF-2 is a mediator of prolactin-incluced morphogenesis in the breast. Dev Cell 3, 877-887.
14. Brockman, J. L., Schroeder, M. D. and Schuler, L A. (2002). PRL activates the cyclin D1 promoter via the Jak2/Stat pathway. Mol. Endocrinol. 16, 774-784.
15. Buser, A. C., Gass-Handel, E. K., Wyszomierski, S. L., Doppler, W., Leonhardt, S. A., Schaack, J., Rosen, J. M., Watkin, H., Anderson, S. M. and Edwards, D. P. (2007). Progesterone receptor repression of prolactin/signal transducer and activator of transcription 5-mediated transcription of the beta-casein gene in mammary epithelial cells. Mol. Endocrinol. 21, 106-125.
16. Cao, Y., Bonizzi, G., Seagroves, T. N., Greten, F. R., Johnson, R., Schmidt, E. V. and Karin, M. (2001). IKKalpha provides an essential link between RANK signaling and cyclin D1 expression during mammary gland development. Cell 107, 763-775.
17. Clarke, R. B, Howell, A., Potten, C. S. and Anderson, E. (1997). Dissociation between steroid receptor expression and cell proliferation in the human breast. Cancer Res. 57, 4987-4991.
18. Clevers, H. (2006). Wnt/beta-catenin signaling in development and disease. Cell 127, 469-480.
19. Daniel, C. W. and Silberstein, G. B. (1987). Postnatal development of the rodent mammary gland. In The Mammary Gland (ed. M. C. Neville and C. W. Daniel), pp. 3-31. New York: Plenum Press.
20. DasGupta, R. and Fuchs, E. (1999). Multiple roles for activated LEF/TCF transcription complexes during hair follicle development and differentiation. Development 126, 4557-4568.
21. Deis, R. P. and Delouis, C. (1983). Lactogenesis induced by ovariectomy in pregnant rats and its regulation by oestrogen and progesterone. J. Steroid Biochem. 18, 687-690.
22. Edery, M., Imagawa, W., Larson, L. and Nandi, S. (1985). Regulation of estrogen and progesterone receptor levels in mouse mammary epithelial cells grown in serum-free collagen gel cultures. Endocrinology 116, 105-112.
23. Fantl, V., Edwards, P. A., Steel, J. H., Vonderhaar, B. K. and Dickson, C. (1999). Impaired mammary gland development in Cyl-1 (-/-) mice during pregnancy and lactation is epithelial cell autonomous. Dev Biol. 212, 1-11.
24. Fata, J. E., Kong, Y. Y., Li, J., Sasaki, T., Irie-Sasaki, J., Moorehead, R. A., Elliott, R., Scully, S., Voura, E. B., Lacey, D. L. et al. (2000). The osteoclast differentiation factor osteoprotegerin-ligand is essential for mammary gland development. Cell 103, 41-50.
25. Gat, U., Dasgupta, R., Degenstein, L. and Fuchs, E. (1998). De novo hair follicle morphogenesis and hair tumors in mice expressing a truncated β-catenin in skin. Cell 95, 605-614.
26. Gavin, B. J. and McMahon, A. P. (1992). Differential regulation of the Wnt gene family during pregnancy and lactation suggests a role in postnatal development of the mammary gland. Mol. Cell. Biol. 12, 2418-2423.
27. Gouilleux, F., Pallard, C., Dusanter-Fourt, I., Wakao, H., Haldosen, L. A., Norstedt, G., Levy, D. and Groner, B. (1995). Prolactin, growth hormone, erythropoietin and granulocyte-macrophage colony stimulating factor induce MGF-Stat5 DNA binding activity. EMBO J. 14, 2005-2013.
28. Graham, J. D. and Clarke, C. L. (1997). Physiological action of progesterone in target tissues. Endocr. Rev 18, 502-519.
29. Grimm, S. L., Seagroves, T. N., Kabotyanski, E. B., Hovey, R. C., Vonderhaar, B. K., Lydon, J. P., Miyoshi, K., Hennighausen, L., Ormandy, C. J., Lee, A. V. et al. (2002). Disruption of steroid and prolactin receptor patterning in the mammary gland correlates with a block in lobuloalveolar development. Mol. Endocrinol. 16, 2675-2691.
30. Groner, B. and Gouilleux, F. (1995). Prolactin-mediated gene activation in mammary elpithelial cells. Curr. Opin. Genet Dev 5, 587-594.
31. Haslam, S. Z. (1987). Role of sex steroid hormones in normal mammary gland function. In The Mammary Gland (ed. M. C. Neville and C. W. Daniel), pp. 499-533. New York: Plenum Press.
32. Hatsell, S., Rowlands, T, Hiremath, M. and Cowin, P. (2003). Beta-catenin and Tcfs in mammary development and cancer. J. Mammary Gland Biol. Neoplasia 8, 145-158.
33. Hens, J. R. and Wysolmerski, J. J. (2005). Key stages of mammary gland development: molecular mechanisms involved in the formation of the embryonic mammary gland. Breast Cancer Res. 7, 220-224.
34. Hoffmans, R. and Basler, K. (2004). Identification and in vivo role of the Armadillo-Legless interaction. Development 131, 4393-4400.
35. Hovey, R. C., Trott, J. F. and Vonderhaar, B. K. (2002). Establishing a framework for the functional mammary gland: from endocrinology to morphology. J. Mammary Gland Biol. Neoplasia 7, 17-38.
36. Hsu, W., Shakya, R. and Costantini, F. (2001). Impaired mammary gland and lymphoid development caused by inducible expression of Axin in transgenic mice. J. Cell Biol. 155, 1055-1064.
37. Humphreys, R. C., Lydon, J., O'Malley, B. W. and Rosen, J. M. (1997). Mammary gland development is mediated by both stromal and epithelial progesterone receptors. Mol. Endocrinol. 11, 801-811.
38. Imbert, A., Eelkema, R., Jordan, S., Feiner, H. and Cowin, P. (2001). Delta N89 beta-catenin induces precocious development, differentiation, and neoplasia in mammary gland. J. Cell Biol. 153, 555-568.
39. Ismail, P. M., Li, J., DeMayo, F. J., O'Malley, B. W. and Lydon, J. P. (2002). A novel LacZ reporter mouse reveals complex regulation of the progesterone receptor promoter during mammary gland development. Mol. Endocrinol. 16, 2475-2489.
40. Jho, E. H., Zhang, T., Domon, C., Joo, C. K., Freund, J. N. and Costantini, F. (2002). Wnt/beta-catenin/Tcf signaling induces the transcription of Axin2, a negative regulator of the signaling pathway. Mol. Cell. Biol. 22, 1172-1183.
41. Kleinberg, D. L., Feldman, M. and Ruan, W. (2000). IGF-I: an essential factor in terminal end bud formation and ductal morphogenesis. J. Mammary Gland Biol. Neoplasia 5, 7-17.
42. Korinek, V., Barker, N., Morin, P. J., van Wichen, D., de Weger, R., Kinzler, K., Vogelstein, B. and Clevers, H. (1997). Constitutive transcriptional activation by a β-catenin-tcf complex in APC-/- colon carcinoma. Science 275, 1784-1787.
43. Kramps, T., Peter, O., Brunner, E., Nellen, D., Froesch, B., Chatterjee, S., Murone, M., Zullig, S. and Basler, K. (2002). Wnt/ wingless signaling requires BCL9/legless-mediated recruitment of pygopus to the nuclear beta-catenin-TCF complex. Cell 109, 47-60.
44. Lamberti, C., Lin, K. M., Yamamoto, Y., Verma, U., Verma, I. M., Byers, S. and Gaynor, R. B. (2001). Regulation of beta-catenin function by the IkappaB kinases. J. Biol. Chem. 276, 42276-42286.
45. Liu, B. Y., Kim, Y. C., Leatherberry, V., Cowin, P. and Alexander, C. M. (2003). Mammary gland development requires syndecan-1 to create a beta-catenin/TCF-responsive mammary epithelial subpopulation. Oncogene 22, 9243-9253.
46. Liu, B. Y., McDermott, S. P., Khwaja, S. S. and Alexander, C. M. (2004). The transforming activity of Wnt effectors correlates with their ability to induce the accumulation of mammary progenitor cells. Proc. Natl. Acad. Sci. USA 101, 4158-4163.
47. Lund, L. R., Romer, J., Thomasset, N., Solberg, H., Pyke, C., Bissell, M. J., Dano, K. and Werb, Z. (1996). Two independent phases of apoptosis in mammary gland involution: proteinase-independent and -dependent pathways. Development 122, 181-193.
48. Lustig, B., Jerchow, B., Sachs, M., Weiler, S., Pietsch, T, Karsten, U., van de Wetering, M., Clevers, H., Schlag, P. M., Birchmeier, W. et al. (2002). Negative feedback loop of Wnt signaling through upregulation of conductin/axin2 in colorectal and liver tumors. Mol. Cell. Biol. 22, 1184-1193.
49. Lydon, J. P., DeMayo, F. J., Funk, C. R., Mani, S. K., Hughes, A. R., Montgomery, C. A., Jr, Shyamala, G., Conneely, O. M. and O'Malley, B. W. (1995). Mice lacking progesterone receptor exhibit pleiotropic reproductive abnormalities. Genes Dev. 9, 2266-2278.
50. Lyons, W. R., Li, C. H. and Johnson, R. E. (1958). The hormonal control of mammary growth and lactation. Recent Prog. Horm. Res. 14, 219-248; discussion 248-254.
51. Mallepell, S., Krust, A., Chambon, P. and Brisken, C. (2006). Paracrine signaling through the epithelial estrogen receptor alpha is required for proliferation and morphogenesis in the mammary gland. Proc. Natl. Acad. Sci. USA 103, 2196-2201.
52. Maretto, S., Cordenonsi, M., Dupont S., Braghetta, R. Broccoli, V., Hassan, A. B., Volpin, D., Bressan, G. M. and Piccolo, S. (2003). Mapping Wnt/betacatenin signaling during mouse development and in colorectal tumors. Proc. Natl. Acad. Sci. USA 100, 3299-3304.
53. Martin, C. E., Hartmann, P. E. and Gooneratne, A. (1978). Progesterone and corticosteroids in the initiation of lactation in the sow. Aust J. Biol. Sci. 31, 517-525.
54. Mather, I. H. and Keenan, T. W. (1998). Origin and secretion of milk lipids. J. Mammary Gland Biol. Neoplasia 3, 259-273.
55. Mulac-Jericevic, B., Mullinax, R. A., DeMayo, F. J., Lydon, J. P. and Conneely, O. M. (2000). Subgroup of reproductive functions of progesterone mediated by progesterone receptor-B isoform. Science 289, 1751-1754.
56. Mulac-Jericevic, B., Lydon, J. P., DeMayo, F. J. and Conneely, O. M. (2003). Defective mammary gland morphogenesis in mice lacking the progesterone receptor B isoform. Proc. Natl. Acad. Sci. USA 100, 9744-9749.
57. Nandi, S. (1958). Endocrine control of mammary gland development and function in the C3H/He Crgl mouse. J. Natl. Cancer Inst. 21, 1039-1063.
58. Neifert, M. R., McDonough, S. L. and Neville, M. C. (1981). Failure of lactogenesis associated with placental retention. Am. J. Obstet Gynecol. 140, 477-478.
59. Neville, M. C., McFadden, T. B. and Forsyth, I. (2002). Hormonal regulation of mammary differentiation and milk secretion. J. Mammary Gland Biol. Neoplasia 7, 49-66.
60. Nguyen, D. A. and Neville, M. C. (1998). Tight junction regulation in the mammary gland. J. Mammary Gland Biol. Neoplasia 3, 233-246,
61. Nguyen, D. A., Parlow, A. F. and Neville, M. C. (2001). Hormonal regulation of tight junction closure in the mouse mammary epithelium during the transition from pregnancy to lactation. J. Endocrinol. 170, 347-356.
62. Niemann, C. and Watt, F. M. (2002). Designer skin: lineage commitment in postnatal epidermis, Trends Cell Biol. 12, 185-192.
63. Niemann, C., Owens, D. M., Hulsken, J., Birchmeier, W. and Waft, F. M. (2002). Expression of DeltaNLef1 in mouse epidermis results in differentiation of hair follides into squamous epidermal cysts and formation of skin turnours. Development 129, 95-109.
64. Ormandy, C. J. and Sutherland, R. L. (1993). Mechanisms of prolactin receptor regulation in mammary gland. Mol. Cell. Endocrinol. 91, C1-C6.
65. Ormandy, C. J., Camus, A., Barra, J., Damotte, D., Lucas, B., Buteau, H., Edery, M., Brousse, N., Babinet, C., Binart, N. et al. (1997a). Null mutation of the prolactin receptor gene produces multiple reproductive defects in the mouse. Genes Dev. 11, 167-178.
66. Ormandy, C. J., Hall, R. E., Manning, D. L., Robertson, J. F., Blamey, R. W., Kelly, P.A., Nicholson, R. I. and Sutherland, R. L. (1997b). Coexpression and cross-regulation of the prolactin receptor and sex steroid hormone receptors in breast cancer. J. Clin. Endocrinol. Metab. 82, 3692-3699,
67. Oxelmark, E., Roth, J. M., Brooks, P. C., Braunstein, S. E., Schneider, R. J. and Garabedian, M. J. (2006). The cochaperone p23 differentially regulates estrogen receptor target genes and promotes tumor cell adhesion and invasion. Mol. Cell. Biol. 26, 5205-5213.
68. Plaut, K., Maple, R., Ginsburg, E. and Vonderhaar, B. (1999). Progesterone stimulates DNA synthesis and lobulo-alveolar development in mammary glands in ovariectomized mice. J. Cell. Physiol. 180, 298-304.
69. Purnell, D. M. and Saggers, G. C. (1974). Topologic assessment by use of wholemounts of mitotic activity in the hamster mammary gland during the estrous cycle. J. Natl. Cancer Inst. 53, 825-828.
70. Richer, J. K., Lange, C. A., Manning, N. G., Owen, G., Powell, R. and Horwitz, K. B. (1998). Convergence of progesterone with growth factor and cytokine signaling in breast cancer. Progesterone receptors regulate signal transducers and activators of transcription expression and activity. J. Biol. Chem. 273, 31317-31326.
71. Rider, V., lsuzugawa, K., Twarog, M., Jones, S., Cameron, B., Imakawa, K. and Fang, J. (2006). Progesterone initiates Wnt-{ibeta}-catenin signaling but estradiol is required for nuclear activation and synchronous proliferation of rat uterine stromal cells. J. Endocrinol. 191, 537-548.
72. Robinson, G. W., McKnight, R. A., Smith, G. H. and Hennighausen, L. (1995). Mammary epithelial cells undergo secretory differentiation in cycling virgins but require pregnancy for the establishment of terminal differentiation. Development 121, 2079-2090.
73. Roose, J., Huls, G., van Beest, M., Moerer, P., van der Horn, K., Goldschmeding, R., Logtenberg, T and Clevers, H. (1999). Synergy between tumor suppressor APC and the beta-catenin-Tcf4 target Tcf1. Science 285, 1923-1926.
74. Rowlands, T. M., Pechenkina, I. V., Hatsell, S. J., Pestell, R. G. and Cowin, P. (2003). Dissecting the roles of beta-catenin and cyclin D1 during mammary development and neoplasia. Proc. Natl. Acad. Sci. USA 100, 11400-11405.
75. Russo, I. H. and Russo, J. (1978). Developmental stage of the rat mammary gland as determinant of its susceptibility to 7,12-dimethyl benz[a]a nth racene. J. Natl. Cancer Inst. 61, 1439-1449.
76. Schneider, S., Steinbeisser, H., Warga, R. M. and Hausen, P. (1996). Betacatenin translocation into nuclei demarcates the dorsalizing centers in frog and fish embryos. Mech. Dev. 57, 191-198.
77. Seagroves, T. N., Lydon, J. P., Hovey, R. C., Vonderhaar, B. K. and Rosen, J. M. (2000). C/EBPbeta (CCAAT/enhancer binding protein) controls cell fate determination during mammary gland development. Mol. Enclocrinol. 14, 359-368.
78. Shillingford, J. M., Miyoshi, K., Flagella, M., Shull, G. E. and Hennighausen, L. (2002). Mouse mammary epithelial cells express the Na-K-Cl cotransporter, NKCC1: characterization, localization, and involvement in ductal development and morphogenesis. Mol. Endocrinol. 16, 1309-1321.
79. Shillingford, J. M., Miyoshi, K., Robinson, G. W., Bierie, B., Cao, Y., Karin, M. and Hennighausen, L. (2003). Proteotyping of mammary tissue from transgenic and gene knockout mice with immunohistochernical markers: a tool to define developmental lesions. J. Histochem. Cytochem. 51, 555-565.
80. Shtutman, M., Zhiurinsky, J., Simcha, I., Albanese, C., D'Amico, M., Pestell, R. and Ben-Ze'ev, A. (1999). The cyclin D1 gene is a target of the beta-catenin LEF1 pathway. Proc. Natl. Acad. Sci. USA 96, 5522-5527.
81. Shyamala, G. (1999). Progesterone signaling and mammary gland morphogenesis. J. Mammary Gland Biol. Neoplasia 4, 89-104.
82. Shyamala, G. and Dickson, C. (1976). Relationship between receptor and mammary tumour virus production after stimulation by glucocorticoid. Nature 262,107-112.
83. Shyamala, G., Yang, X., Cardiff, R. D. and Dale, E. (2000). impact of progesterone receptor on cell-fate decisions during mammary gland development. Proc Natl. Acad. Sci. USA 97, 3044-3049.
84. Shyamala, G., Chou, Y. C., Louie, S. G., Guzman, R. C., Smith, G. H. and Nandi, S. (2002). Cellular expression of estrogen and progesterone receptors in mammary glands: regulation by hormones, development and aging. J. Steroid Biochem. Mol. Biol. 80, 137-148.
85. Stadeli, R., Hoffmans, R. and Basler, K. (2006). Transcription under the control of nuclear Arm/beta-catenin. Curr. Biol. 16, R378-R385.
86. Tepera, S. B., McCrea, P.D. and Rosen, J. M. (2003). A beta-catenin survival signal is required for normal lobular development in the mammary gland. J. Cell Sci. 116, 1137-1149.
87. Tetsu, O. and McCormick, F. (1999). β-catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature 398, 422-426.
88. Teuliere, J., Faraldo, M. M., Deugnier, M. A., Shtutman, M., Ben-Ze'ev, A., Thiery, J. P. and Glukhova, M. A. (2005). Targeted activation of beta-catenin signaling in basal mammary epithelial cells affects mammary development and leads to hyperplasia. Development 132, 267-277.
89. Thompson, B., Townsley, F., Rosin-Arbesfeld, R., Musisi, H. and Bienz, M. (2002). A new nuclear component of the Wnt signalling pathway. Nat Cell Biol. 4,367-373.
90. Townsley, F. M., Cliffe, A. and Bienz, M. (2004). Pygopus and Legless target Armadillo/beta-catenin to the nucleus to enable its transcriptional co-activator function. Nat Cell Biol. 6, 626-633.
91. Truss, M., Chalepakis, G. and Beato, M. (1992). Interplay of steroid hormone receptors and transcription factors on the mouse mammary tumor virus promoter. J. Steroid Biochem. Mol. Biol. 43, 365-378.
92. van Genderen, C., Okamura, R. M., Farinas, I., Quo, R.-G., Parslow, T G., Bruhn, L. and Grosschedl, R. (1994). Development of several organs that require inductive epithelial-mesenchymal interactions is impaired in Lef-1 deficient mice. Genes Dev. 8, 2691-2704.
93. Wagner, K. U., Boulanger, C. A., Henry, M. D., Sgagias, M., Hennighausen, L. and Smith, G. H. (2002). An adjunct mammary epithelial cell population in parous females: its role in functional adaptation and tissue renewal. Development 129, 1377-1386.
94. Weber-Hall, S. J., Phippard, D. J., Niemeyer, C. C. and Dale, T. C. (1994). Developmental and hormonal regulation of Wnt gene expression in the mouse mammary gland. Differentiation 57, 205-214.
95. Witty, J. P., Wright, J. H. and Matrisian, L. M. (1995). Matrix metalloproteinases are expressed during ductal and alveolar mammary morphogenesis, and misregulation of stromelysin-1 in transgenic mice induces unscheduled alveolar development. Mol. Biol. Cell 6, 1287-1303.
96. Yu, H. M., Jerchow, B., Sheu, T. J., Liu, B., Costantini, F., Puzas, J. E., Birchmeier, W. and Hsu, W. (2005). The role of Axin2 in calvarial morphogenesis and craniosynostosis. Development 132, 1995-2005.