Mammary epithelial tubes elongate through MAPK-dependent coordination of cell migration

Development (Cambridge)

Volumn 143, Issue 6, 2016, Pages 983-993

  Huebner, Robert J ^a   Neumann, Neil M ^a   Ewald, Andrew J ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Branching morphogenesis; Collective cell migration; Epithelial evelopment; Mammary gland; MAPK signaling; Tubulogenesis

Indexed keywords

CRE RECOMBINASE; FIBROBLAST GROWTH FACTOR 2; GREEN FLUORESCENT PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN TYROSINE KINASE; RAC1 PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE KINASE;

ADIPOCYTE; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRANCHING MORPHOGENESIS; BREAST EPITHELIUM CELL; CELL ELONGATION; CELL FUNCTION; CELL METABOLISM; CELL MIGRATION; CELL MOTILITY; CELL PROLIFERATION; CELL SURVIVAL; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INDUCTION; ENZYME PHOSPHORYLATION; FEMALE; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; ANIMAL; ANISOTROPY; CELL MOTION; CYTOLOGY; CYTOPLASM; EPITHELIUM CELL; HUMAN; METABOLISM; MORPHOGENESIS; PHOSPHORYLATION; TRANSGENIC MOUSE; UDDER;

ANIMALS; ANISOTROPY; CELL MOVEMENT; CELL PROLIFERATION; EPITHELIAL CELLS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; HUMANS; MAMMARY GLANDS, ANIMAL; MICE, TRANSGENIC; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; MORPHOGENESIS; ORGANOIDS; PHOSPHORYLATION; RAC1 GTP-BINDING PROTEIN; SIGNAL TRANSDUCTION;

EID: 84960970171     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.127944     Document Type: Article

References (64)

1. Affolter, M., Zeller, R. and Caussinus, E. (2009). Tissue remodelling through branching morphogenesis. Nat. Rev. Mol. Cell Biol. 10, 831-842.
2. Alescio, T. and Di Michele, M. (1968). Relationship of epithelial growth to mitotic rate in mouse embryonic lung developing in vitro. J. Embryol. Exp. Morphol. 19, 227-237.
3. Andrew, D. J. and Ewald, A. J. (2010). Morphogenesis of epithelial tubes: insights into tube formation, elongation, and elaboration. Dev. Biol. 341, 34-55.
4. Cerchiari, A. E., Garbe, J. C. Jee, N. Y. Todhunter, M. E. Broaders, K. E. Peehl, D. M. Desai, T. A. Labarge, M. A. Thomson, M. Gartner, Z. J. (2015). A strategy for tissue self-organization that is robust to cellular heterogeneity and plasticity. Proc. Natl. Acad. Sci. USA 112, 2287-2292.
5. Cheshire, A. M., Kerman, B. E., Zipfel, W. R., Spector, A. A. and Andrew, D. J. (2008). Kinetic and mechanical analysis of live tube morphogenesis. Dev. Dyn. 237, 2874-2888.
6. Chi, X., Michos, O., Shakya, R., Riccio, P., Enomoto, H., Licht, J. D, Asai, N., Takahashi, M., Ohgami, N., Kato, M. et al. (2009). Ret-dependent cell rearrangements in the Wolffian duct epithelium initiate ureteric bud morphogenesis. Dev. Cell 17, 199-209.
7. Dhillon, A. S., Hagan, S., Rath, O. and Kolch, W. (2007). MAP kinase signalling pathways in cancer. Oncogene 26, 3279-3290.
8. Edelstein, A., Amodaj, N., Hoover, K., Vale, R. and Stuurman, N. (2010). Computer control of microscopes using microManager. Curr. Protoc. Mol. Biol. 92, 14201-14217.
9. Ewald, A. J. (2013). Practical considerations for long-term time-lapse imaging of epithelial morphogenesis in three-dimensional organotypic cultures. Cold Spring Harb. Protoc. 2013, 100-117.
10. Ewald, A. J., Brenot, A., Duong, M., Chan, B. S. and Werb, Z. (2008). Collective epithelial migration and cell rearrangements drive mammary branching morphogenesis. Dev. Cell 14, 570-581.
11. Ewald, A. J., Huebner, R. J, Palsdottir, H, Lee, J. K, Perez, M. J, Jorgens, D. M. Tauscher, A. N, Cheung, K. J, Werb, Z. and Auer, M. (2012). Mammary collective cell migration involves transient loss of epithelial features and individual cell migration within the epithelium. J. Cell Sci. 125, 2638-2654.
12. Fata, J. E., Mori, H., Ewald, A. J, Zhang, H., Yao, E., Werb, Z. and Bissell, M. J. (2007). The MAPKERK-1,2 pathway integrates distinct and antagonistic signals from TGFα and FGF7 in morphogenesis of mouse mammary epithelium. Dev. Biol. 306, 193-207.
13. Fisher, C. E., Michael, L., Barnett, M.W. and Davies, J. A. (2001). Erk MAP kinase regulates branching morphogenesis in the developing mouse kidney. Development 128, 4329-4338.
14. Ghabrial, A. S. and Krasnow, M. A. (2006). Social interactions among epithelial cells during tracheal branching morphogenesis. Nature 441, 746-749.
15. Goldin, G. V. and Wessells, N. K. (1979). Mammalian lung development: the possible role of cell proliferation in the formation of supernumerary tracheal buds and in branching morphogenesis. J. Exp. Zool. 208, 337-346.
16. Hadjantonakis, A.-K. and Papaioannou, V. E. (2004). Dynamic in vivo imaging and cell tracking using a histone fluorescent protein fusion in mice. BMC Biotechnol. 4, 33.
17. Hennighausen, L. and Robinson, G. W. (2005). Information networks in the mammary gland. Nat. Rev. Mol. Cell Biol. 6, 715-725.
18. Hinck, L. and Silberstein, G. B. (2005). Key stages in mammary gland development: the mammary end bud as a motile organ. Breast Cancer Res. 7, 245-251.
19. Hogg, N. A., Harrison, C. J. and Tickle, C. (1983). Lumen formation in the developing mouse mammary gland. J. Embryol. Exp. Morphol. 73, 39-57.
20. Hoshi, M., Batourina, E., Mendelsohn, C. and Jain, S. (2012). Novel mechanisms of early upper and lower urinary tract patterning regulated by RetY1015 docking tyrosine in mice. Development 139, 2405-2415.
21. Hsu, J. C., Koo, H., Harunaga, J. S, Matsumoto, K., Doyle, A. D. and Yamada, K. M. (2013). Region-specific epithelial cell dynamics during branching morphogenesis. Dev. Dyn. 242, 1066-1077.
22. Huebner, R. J. and Ewald, A. J. (2014). Cellular foundations of mammary tubulogenesis. Semin. Cell Dev. Biol. 31, 124-131.
23. Huebner, R. J., Lechler, T. and Ewald, A. J. (2014). Developmental stratification of the mammary epithelium occurs through symmetry-breaking vertical divisions of apically positioned luminal cells. Development 141, 1085-1094.
24. Ikegami, S., Taguchi, T., Ohashi, M, Oguro, M, Nagano, H. and Mano, Y. (1978). Aphidicolin prevents mitotic cell division by interfering with the activity of DNA polymerase-alpha. Nature 275, 458-460.
25. Kashimata, M., Sayeed, S., Ka, A., Onetti-Muda, A., Sakagami, H., Faraggiana, T. and Gresik, E. W. (2000). The ERK-1/2 signaling pathway is involved in the stimulation of branching morphogenesis of fetal mouse submandibular glands by EGF. Dev. Biol. 220, 183-196.
26. Kato, K., Chihara, T. and Hayashi, S. (2004). Hedgehog and Decapentaplegic instruct polarized growth of cell extensions in the Drosophila trachea. Development 131, 5253-5261.
27. Keller, R. (2002). Shaping the vertebrate body plan by polarized embryonic cell movements. Science 298, 1950-1954.
28. Kerman, B. E. and Andrew, D. J. (2010). Staying alive: Dalmatian mediated blocking of apoptosis is essential for tissue maintenance. Dev. Dyn. 239, 1609-1621.
29. Kim, H. Y., Varner, V. D. and Nelson, C. M. (2013). Apical constriction initiates new bud formation during monopodial branching of the embryonic chicken lung. Development 140, 3146-3155.
30. Kling, D. E., Lorenzo, H. K, Trbovich, A. M, Kinane, T. B., Donahoe, P. K. and Schnitzer, J. J. (2002). MEK-1/2 inhibition reduces branching morphogenesis and causes mesenchymal cell apoptosis in fetal rat lungs. Am. J. Physiol. Lung Cell. Mol. Physiol. 282, L370-L378.
31. Larsen, M., Wei, C. and Yamada, K. M. (2006). Cell and fibronectin dynamics during branching morphogenesis. J. Cell Sci. 119, 3376-3384.
32. Lauffenburger, D. A. and Horwitz, A. F. (1996). Cell migration: a physically integrated molecular process. Cell 84, 359-369.
33. Lebreton, G. and Casanova, J. (2014). Specification of leading and trailing cell features during collective migration in the Drosophila trachea. J. Cell Sci. 127, 465-474.
34. Lecaudey, V. and Gilmour, D. (2006). Organizing moving groups during morphogenesis. Curr. Opin. Cell Biol. 18, 102-107.
35. Liu, Y., Stein, E., Oliver, T., Li, Y., Brunken, W. J, Koch, M., Tessier-Lavigne, M. and Hogan, B. L. M. (2004). Novel role for Netrins in regulating epithelial behavior during lung branching morphogenesis. Curr. Biol. 14, 897-905.
36. Lubarsky, B. and Krasnow, M. A. (2003). Tube morphogenesis: making and shaping biological tubes. Cell 112, 19-28.
37. Luetteke, N. C., Qiu, T. H., Fenton, S. E., Troyer, K. L., Riedel, R. F., Chang, A. and Lee, D. C. (1999). Targeted inactivation of the EGF and amphiregulin genes reveals distinct roles for EGF receptor ligands in mouse mammary gland development. Development 126, 2739-2750.
38. Manning, B. D. and Cantley, L. C. (2007). AKT/PKB signaling: navigating downstream. Cell 129, 1261-1274.
39. McNally, S. and Martin, F. (2011). Molecular regulators of pubertal mammary gland development. Ann. Med. 43, 212-234.
40. Muzumdar, M. D., Tasic, B., Miyamichi, K., Li, L. and Luo, L. (2007). A global double-fluorescent Cre reporter mouse. Genesis 45, 593-605.
41. Nguyen-Ngoc, K.-V. and Ewald, A. J. (2013). Mammary ductal elongation and myoepithelial migration are regulated by the composition of the extracellular matrix. J. Microsc. 251, 212-223.
42. Nguyen-Ngoc, K.-V. Shamir, Eliah R., Huebner, Robert J., Beck, Jennifer N., Cheung, Kevin J. and Ewald, Andrew J., (2015). 3D culture assays of murine mammary branching morphogenesis and epithelial invasion. Methods Mol. Biol. 1189, 135-162.
43. Nobes, C. D. and Hall, A. (1995). Rho, rac and cdc42 GTPases: regulators of actin structures, cell adhesion and motility. Biochem. Soc. Trans. 23, 456-459.
44. O’Brien, L. E., Tang, K., Kats, E. S, Schutz-Geschwender, A., Lipschutz, J. H. and Mostov, K. E. (2004). ERK and MMPs sequentially regulate distinct stages of epithelial tubule development. Dev. Cell 7, 21-32.
45. Packard, A., Georgas, K., Michos, O., Riccio, P., Cebrian, C., Combes, A. N, Ju, A., Ferrer-Vaquer, A., Hadjantonakis, A.-K., Zong, H. et al. (2013). Luminal mitosis drives epithelial cell dispersal within the branching ureteric bud. Dev. Cell 27, 319-330.
46. Pearson, G. W. and Hunter, T. (2007). Real-time imaging reveals that noninvasive mammary epithelial acini can contain motile cells. J. Cell Biol. 179, 1555-1567.
47. Ribeiro, C., Ebner, A. and Affolter, M. (2002). In vivo imaging reveals different cellular functions for FGF and Dpp signaling in tracheal branching morphogenesis. Dev. Cell 2, 677-683.
48. Ridley, A. J. (2003). Cell migration: integrating signals from front to back. Science 302, 1704-1709.
49. Schlessinger, J. (2004). Common and distinct elements in cellular signaling via EGF and FGF receptors. Science 306, 1506-1507.
50. Schnatwinkel, C. and Niswander, L. (2013). Multiparametric image analysis of lung-branching morphogenesis. Dev. Dyn. 242, 622-637.
51. Seger, R. and Krebs, E. G. (1995). The MAPK signaling cascade. FASEB J. 9, 726-735.
52. Shamir, E. R. and Ewald, A. J. (2014). Three-dimensional organotypic culture: experimental models of mammalian biology and disease. Nat. Rev. Mol. Cell Biol. 15, 647-664.
53. Simian, M., Hirai, Y., Navre, M., Werb, Z., Lochter, A. and Bissell, M. J. (2001). The interplay of matrix metalloproteinases, morphogens and growth factors is necessary for branching of mammary epithelial cells. Development 128, 3117-3131
54. Srinivasan, L., Sasaki, Y., Calado, D. P., Zhang, B., Paik, J. H., DePinho, R. A, Kutok, J. L, Kearney, J. F, Otipoby, K. L. and Rajewsky, K. (2009). PI3 kinase signals BCR-dependent mature B cell survival. Cell 139, 573-586.
55. Sternlicht, M. D. (2005). Mammary ductal morphogenesis requires paracrine activation of stromal EGFR via ADAM17-dependent shedding of epithelial amphiregulin. Development 132, 3923-3933.
56. Sternlicht, M. D. (2006). Key stages in mammary gland development: the cues that regulate ductal branching morphogenesis. Breast Cancer Res. 8, 201.
57. Sternlicht, M. D., Kouros-Mehr, H., Lu, P. and Werb, Z. (2006). Hormonal and local control of mammary branching morphogenesis. Differentiation 74, 365-381.
58. Sutherland, D., Samakovlis, C. and Krasnow, M. A. (1996). branchless encodes a Drosophila FGF homolog that controls tracheal cell migration and the pattern of branching. Cell 87, 1091-1101.
59. Tang, N., Marshall, W. F., McMahon, M., Metzger, R. J. and Martin, G. R. (2011). Control of mitotic spindle angle by the RAS-regulated ERK1/2 pathway determines lung tube shape. Science 333, 342-345.
60. Valentin, G., Haas, P. and Gilmour, D. (2007). The chemokine SDF1a coordinates tissue migration through the spatially restricted activation of Cxcr7 and Cxcr4b. Curr. Biol. 17, 1026-1031.
61. Vasilyev, A., Liu, Y., Mudumana, S., Mangos, S., Lam, P.-Y., Majumdar, A., Zhao, J., Poon, K.-L., Kondrychyn, I., Korzh, V. et al. (2009). Collective cell migration drives morphogenesis of the kidney nephron. PLoS Biol. 7, e1000009.
62. Wang, X., He, L., Wu, Y. I., Hahn, K. M. and Montell, D. J. (2010). Light-mediated activation reveals a key role for Rac in collective guidance of cell movement in vivo. Nat. Cell Biol. 12, 591-597.
63. Watanabe, T. and Costantini, F. (2004). Real-time analysis of ureteric bud branching morphogenesis in vitro. Dev. Biol. 271, 98-108.
64. Whyte, J., Bergin, O., Bianchi, A., McNally, S. and Martin, F. (2009). Key signalling nodes in mammary gland development and cancer. Mitogen-activated protein kinase signalling in experimental models of breast cancer progression and in mammary gland development. Breast Cancer Res. 11, 209.