Self-organization and branching morphogenesis of primary salivary epithelial cells

Tissue Engineering

Volumn 13, Issue 4, 2007, Pages 721-735

  Wei, Cindy ^a,b,c   Larsen, Melinda ^a,d   Hoffman, Matthew P ^a   Yamada, Kenneth M ^a,b  

^a NATIONAL INSTITUTE OF DENTAL AND CRANIOFACIAL RESEARCH   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d STATE UNIVERSITY OF NEW YORK   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPITHELIAL CELLS; MORPHOGENESIS; REGENERATION; SALIVARY GLAND;

BIOASSAY; CELL PROLIFERATION; ENDOCRINOLOGY; GENE EXPRESSION; RATS; SELF ASSEMBLY; TISSUE;

CELL GROWTH;

ACTIN; AQUAPORIN 5; BETA CATENIN; BETA1 INTEGRIN; PROLACTIN INDUCIBLE PROTEIN; PROTEIN; UNCLASSIFIED DRUG; UVOMORULIN;

ANIMAL CELL; ARTICLE; CELL AGGREGATION; CELL DIFFERENTIATION; CELL STRUCTURE; CONTROLLED STUDY; EPITHELIUM CELL; FEMALE; IMMUNOHISTOCHEMISTRY; MESENCHYME; MORPHOGENESIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SALIVARY GLAND; TISSUE REGENERATION;

ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; EPITHELIAL CELLS; MICE; MICE, INBRED ICR; MORPHOGENESIS; SALIVARY GLANDS; STEM CELLS; TISSUE ENGINEERING;

EID: 34247479967     PISSN: 10763279     EISSN: None     Source Type: Journal    
DOI: 10.1089/ten.2006.0123     Document Type: Article

References (62)

1. Hieda, Y., and Nakanishi, Y. Epithelial morphogenesis in mouse embryonic submandibular gland: its relationships to the tissue organization of epithelium and mesenchyme. Dev Growth Differ 39, 1, 1997.
2. Nakanishi, Y., Morita, T., and Nogawa, H. Cell proliferation is not required for the initiation of early cleft formation in mouse embryonic submandibular epithelium in vitro. Development 99, 429, 1987.
3. Morita, K., and Nogawa, H. EGF-dependent lobule formation and FGF7-dependent stalk elongation in branching morphogenesis of mouse salivary epithelium in vitro. Dev Dyn 215, 148, 1999.
4. Larsen, M., Wei, C., and Yamada, K.M. Cell migration and fibronectin dynamics during branching morphogenesis. J Cell Science 119, 3376, 2006.
5. Partanen, A.M., and Thesleff, I. Localization and quantitation of 125I-epidermal growth factor binding in mouse embryonic tooth and other embryonic tissues at different developmental stages. Dev Biol 120, 186, 1987.
6. Kashimata, M., and Gresik, E.W. Epidermal growth factor system is a physiological regulator of development of the mouse fetal submandibular gland and regulates expression of the alpha6-integrin subunit. Dev Dyn 208, 149, 1997.
7. Hoffman, M.P., Kidder, B.L., Steinberg, Z.L., Lakhani, S., Ho, S., Kleinman, H.K., and Larsen, M. Gene expression profiles of mouse submandibular gland development: FGFR1 regulates branching morphogenesis in vitro through BMP- and FGF-dependent mechanisms. Development 129, 5767, 2002.
8. Nogawa, H., and Takahashi, Y. Substitution for mesenchyme by basement-membrane-like substratum and epidermal growth factor in inducing branching morphogenesis of mouse salivary epithelium. Development 112, 855, 1991.
9. Hosokawa, Y., Takahashi, Y., Kadoya, Y., Yamashina, S., Nomizu, M., Yamada, Y., and Nogawa, H. Significant role of laminin-1 in branching morphogenesis of mouse salivary epithelium cultured in basement membrane matrix. Dev Growth Differ 41, 207, 1999.
10. Sakai, T., Larsen, M., and Yamada, K.M. Fibronectin requirement in branching morphogenesis. Nature 423, 876, 2003.
11. Grobstein, C., and Cohen, J. Collagenase: effect on the morphogenesis of embryonic salivary epithelium in vitro. Science 150, 626, 1965.
12. Bernfield, M.R., and Wessells, N.K. Intra- and extracellular control of epithelial morphogenesis. Symp Soc Dev Biol 29, 195, 1970.
13. Spooner, B.S., and Wessells, N.K. An analysis of salivary gland morphogenesis: role of cytoplasmic microfilaments and microtubules. Dev Biol 27, 38, 1972.
14. Schuger, L., O'Shea, K.S., Nelson, B.B., and Varani, J. Organotypic arrangement of mouse embryonic lung cells on a basement membrane extract: involvement of laminin. Development 110, 1091, 1990.
15. Mondrinos, M.J., Koutzaki, S., Jiwanmall, E., Li, M., Dechadarevian, J.P., Lelkes, P.I., and Finck, C.M. Engineering three-dimensional pulmonary tissue constructs. Tissue Eng 12, 717, 2006.
16. Montesano, R., Schaller, G., and Orci, L. Induction of epithelial tubular morphogenesis in vitro by fibroblast-derived soluble factors. Cell 66, 697, 1991.
17. Sakurai, H., Barros, E.J., Tsukamoto, T., Barasch, J., and Nigam, S.K. An in vitro tubulogenesis system using cell lines derived from the embryonic kidney shows dependence on multiple soluble growth factors. Proc Natl Acad Sci U S A 94, 6279, 1997.
18. Aframian, D.J., David, R., Ben-Bassat, H., Shai, E., Deutsch, D., Baum, B.J., and Palmon, A. Characterization of murine autologous salivary gland graft cells: a model for use with an artificial salivary gland. Tissue Eng 10, 914, 2004.
19. Tran, S.D., Wang, J., Bandyopadhyay, B.C., Redman, R.S., Dutra, A., Pak, E., Swaim, W.D., Gerstenhaber, J.A., Bryant, J.M., Zheng, C., Goldsmith, C.M., Kok, M.R., Wellner, R.B., and Baum, B.J. Primary culture of polarized human salivary epithelial cells for use in developing an artificial salivary gland. Tissue Eng 11, 172, 2005.
20. Chen, M.H., Chen, R.S., Hsu, Y.H., Chen, Y.J., and Young, T.H. Proliferation and phenotypic preservation of rat parotid acinar cells. Tissue Eng 11, 526, 2005.
21. Aframian, D.J., Cukierman, E., Nikolovski, J., Mooney, D.J., Yamada, K.M., and Baum, B.J. The growth and morphological behavior of salivary epithelial cells on matrix protein-coated biodegradable substrata. Tissue Eng 6, 209, 2000.
22. Larsen, M., Hoffman, M.P., Sakai, T., Neibaur, J.C., Mitchell, J.M., and Yamada, K.M. Role of PI 3-kinase and PIP3 in submandibular gland branching morphogenesis. Dev Biol 255, 178, 2003.
23. Akiyama, H., Chaboissier, M.C., Martin, J.F., Schedl, A., and de Crombrugghe, B. The transcription factor Sox9 has essential roles in successive steps of the chondrocyte differentiation pathway and is required for expression of Sox5 and Sox6. Genes Dev 16, 2813, 2002.
24. Kadoya, Y., Kadoya, K., Durbeej, M., Holmvall, K., Sorokin, L., and Ekblom, P. Antibodies against domain E3 of laminin-1 and integrin alpha 6 subunit perturb branching epithelial morphogenesis of submandibular gland, but by different modes. J Cell Biol 129, 521, 1995.
25. Cutler, L.S., and Gremski, W. Epithelial-mesenchymal interactions in the development of salivary glands. Crit Rev Oral Biol Med 2, 1, 1991.
26. Lee, B., Modha, G., Watson, P.H., Dodd, J., Troup, S., Blanchard, A., and Myal, Y. Expression of the mouse homologue for the human GCDFP-15/PIP gene during pre- and early post-natal development. Mol Cell Endocrinol 205, 33, 2003.
27. Windass, J.D., Mullins, J.J., Beecroft, L.J., George, H., Meacock, P.A., Williams, B.R., and Brammar, W.J. Molecular cloning of cDNAs from androgen-independent mRNA species of DBA/2 mouse sub-maxillary glands. Nucleic Acids Res 12, 1361, 1984.
28. Myal, Y., Iwasiow, B., Yarmill, A., Harrison, E., Paterson, J.A., and Shiu, R.P. Tissue-specific androgen-inhibited gene expression of a submaxillary gland protein, a rodent homolog of the human prolactin-inducible protein/GCDFP-15gene. Endocrinology 135, 1605, 1994.
29. Ball, W.D., Hand, A.R., Moreira, J.E., and Johnson, A.O. A secretory protein restricted to type I cells in neonatal rat submandibular glands, Dev Biol 129, 464, 1988.
30. Moreira, J.E., Hand, A.R., and Ball, W.D. Localization of neonatal secretory proteins in different cell types of the rat submandibular gland from embryogenesis to adulthood. Dev Biol 139, 370, 1990.
31. Giudice, G. Restitution of whole larvae from disaggregated cells of sea urchin embryos. Dev Biol 5, 402, 1962.
32. Giudice, G., and Mutolo, V. Reaggregation of dissociated cells of sea urchin embryos. Adv Morphog 8, 115, 1970.
33. Moscona, A., and Moscona, H. The dissociation and aggregation of cells from organ rudiments of the early chick embryo. J Anat 86, 287, 1952.
34. Moscona, A.A. Cellular interactions in experimental histogenesis. Int Rev Exp Pathol 1, 371, 1962.
35. Emerman, J.T., and Pitelka, D.R. Maintenance and induction of morphological differentiation in dissociated mammary epithelium on floating collagen membranes. In Vitro 13, 316, 1977.
36. Yang, J., Richards, J., Guzman, R., Imagawa, W., and Nandi, S. Sustained growth in primary culture of normal mammary epithelial cells embedded in collagen gels. Proc Natl Acad Sci U S A 77, 2088, 1980.
37. Barcellos-Hoff, M.H., Aggeler, J., Ram, T.G., and Bissell, M.J. Functional differentiation and alveolar morphogenesis of primary mammary cultures on reconstituted basement membrane. Development 105, 223, 1989.
38. Petersen, O.W., Ronnov-Jessen, L., Howlett, A.R., and Bissell, M.J. Interaction with basement membrane serves to rapidly distinguish growth and differentiation pattern of normal and malignant human breast epithelial cells. Proc Natl Acad Sci U S A 89, 9064, 1992.
39. Niemann, C., Brinkmann, V., Spitzer, E., Hartmann, G., Sachs, M., Naundorf, H., and Birchmeier, W. Reconstitution of mammary gland development in vitro: requirement of c-met and c-erbB2 signaling for branching and alveolar morphogenesis. J Cell Biol 143, 533, 1998.
40. Debnath, J., Muthuswamy, S.K., and Brugge, J.S. Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in three-dimensional basement membrane cultures. Methods 30, 256, 2003.
41. Schedin, P.J., Eckel-Mahan, K.L., McDaniel, S.M., Prescott, J.D., Brodsky, K.S., Tender, J.J., and Gutierrez-Hartmann, A. ESX induces transformation and functional epithelial to mesenchymal transition in MCF-12A mammary epithelial cells. Oncogene 23, 1766, 2004.
42. Soriano, J.V., Pepper, M.S., Nakamura, T., Orci, L., and Montesano, R. Hepatocyte growth factor stimulates extensive development of branching duct-like structures by cloned mammary gland epithelial cells. J Cell Sci 108 (Pt 2), 413, 1995.
43. Hall, H.G., Farson, D.A., and Bissell, M.J. Lumen formation by epithelial cell lines in response to collagen overlay: a morphogenetic model in culture. Proc Natl Acad Sci U S A 79, 4672, 1982.
44. McAteer, J.A., Evan, A.P., and Gardner, K.D. Morphogenetic clonal growth of kidney epithelial cell line MDCK. Anat Rec 217, 229, 1987.
45. Royce, L.S., Kibbey, M.C., Mertz, P., Kleinman, H.K., and Baum, B.J. Human neoplastic submandibular intercalated duct cells express an acinar phenotype when cultured on a basement membrane matrix. Differentiation 52, 247, 1993.
46. Montesano, R., Matsumoto, K., Nakamura, T., and Orci, L. Identification of a fibroblast-derived epithelial morphogen as hepatocyte growth factor. Cell 67, 901, 1991.
47. Joraku, A., Sullivan, C.A., Yoo, J.J., and Atala, A. Tissue engineering of functional salivary gland tissue. Laryngoscope 115, 244, 2005.
48. Steinberg, Z., Myers, C., Heim, V.M., Lathrop, C.A., Rebustini, I.T., Stewart, J.S., Larsen, M., and Hoffman, M.P. FGFR2b signaling regulates ex vivo submandibular gland epithelial cell proliferation and branching morphogenesis. Development 132, 1223, 2005.
49. Sakakura, T., Nishizuka, Y., and Dawe, C.J. Mesenchyme-dependent morphogenesis and epithelium-specific cytodifferentiation in mouse mammary gland. Science 194, 1439, 1976.
50. Iwai, K., Hieda, Y., and Nakanishi, Y. Effects of mesenchyme on epithelial tissue architecture revealed by tissue recombination experiments between the submandibular gland and lung of embryonic mice. Dev Growth Differ 40, 327, 1998.
51. Jaskoll, T., Witcher, D., Toreno, L., Bringas, P., Moon, A.M., and Melnick, M. FGF8 dose-dependent regulation of embryonic submandibular salivary gland morphogenesis. Dev Biol 268, 457, 2004.
52. Jaskoll, T., Abichaker, G., Witcher, D., Sala, F.G., Bellusci, S., Hajihosseini, M.K., and Melnick, M. FGF10/FGFR2b signaling plays essential roles during in vivo embryonic submandibular salivary gland morphogenesis. BMC Dev Biol 5, 11, 2005.
53. Ikari, T., Hiraki, A., Seki, K., Sugiura, T., Matsumoto, K., and Shirasuna, K. Involvement of hepatocyte growth factor in branching morphogenesis of murine salivary gland. Dev Dyn 228, 173, 2003.
54. Hoffman, M.P., Kibbey, M.C., Letterio, J.J., and Kleinman, H.K. Role of laminin-1 and TGF-beta 3 in acinar differentiation of a human submandibular gland cell line (HSG). J Cell Sci 109 (Pt 8), 2013, 1996.
55. Lin, R.Z., Chou, L.F., Chien, C.C., and Chang, H.Y. Dynamic analysis of hepatoma spheroid formation: roles of E-cadherin and beta1-integrin. Cell Tissue Res, 324, 411, 2006.
56. Nogawa, H. Determination of the curvature of epithelial cell mass by mesenchyme in branching morphogenesis of mouse salivary gland. J Embryol Exp Morphol 73, 221, 1983.
57. Richa, J., Damsky, C.H., Buck, C.A., Knowles, B.B., and Solter, D. Cell surface glycoproteins mediate compaction, trophoblast attachment, and endoderm formation during early mouse development. Dev Biol 108, 513, 1985.
58. Adams, C.L., Chen, Y.T., Smith, S.J., and Nelson, W.J. Mechanisms of epithelial cell-cell adhesion and cell compaction revealed by high-resolution tracking of E-cadherin-green fluorescent protein. J Cell Biol 142, 1105, 1998.
59. Shackleton, M., Vaillant, F., Simpson, K.J., Stingl, J., Smyth, G.K., Asselin-Labat, M.L., Wu, L., Lindeman, G.J., and Visvader, J.E. Generation of a functional mammary gland from a single stem cell. Nature 439, 84, 2006.
60. Takahashi, S., Schoch, E., and Walker, N.I. Origin of acinar cell regeneration after atrophy of the rat parotid induced by duct obstruction. Int J Exp Pathol 79, 293, 1998.
61. Man, Y.G., Ball, W.D., Marchetti, L., and Hand, A.R. Contributions of intercalated duct cells to the normal parenchyma of submandibular glands of adult rats. Anat Rec 263, 202, 2001.
62. Okumura, K., Nakamura, K., Hisatomi, Y., Nagano, K., Tanaka, Y., Terada, K., Sugiyama, T., Umeyama, K., Matsumoto, K., Yamamoto, T., and Endo, F. Salivary gland progenitor cells induced by duct ligation differentiate into hepatic and pancreatic lineages. Hepatology 38, 104, 2003.