PKCζ regulates cell polarisation and proliferation restriction during mammary acinus formation

Journal of Cell Science

Volumn 123, Issue 19, 2010, Pages 3316-3328

  Whyte, Jacqueline ^a,c   Thornton, Laura ^a   McNally, Sara ^a   McCarthy, Sarah ^a   Lanigan, Fiona ^a   Gallagher, William M ^a   Stein, Torsten ^b   Martin, Finian ^a  

^a UNIVERSITY COLLEGE DUBLIN   (Ireland)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

^c ROYAL COLLEGE OF SURGEONS IN IRELAND   (Ireland)

Author keywords

Breast cancer; Cell polarity; Epithelial; Mammary gland; PKC ; Proliferation

Indexed keywords

PROTEIN KINASE C ZETA; MUTANT PROTEIN; PROTEIN KINASE C; PROTEIN KINASE C ZETA, MOUSE;

ACINAR CELL; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; BREAST DEVELOPMENT; CELL POLARITY; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; FEMALE; HUMAN; HUMAN TISSUE; MAMMARY GLAND; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROGNOSIS; PROTEIN EXPRESSION; TISSUE DISTRIBUTION; ADULT; ANIMAL; BREAST TUMOR; CELL DIFFERENTIATION; CELL TRANSFORMATION; DISEASE COURSE; EPITHELIUM CELL; GENETICS; GROWTH, DEVELOPMENT AND AGING; HYPERPLASIA; METABOLISM; MICROARRAY ANALYSIS; MORTALITY; MOUSE STRAIN; ORGANOGENESIS; PATHOLOGY; PATHOPHYSIOLOGY; PHOSPHORYLATION; PREGNANCY; SURVIVAL; TRANSGENE; TUMOR CELL LINE; UDDER;

ADULT; ANIMALS; BREAST NEOPLASMS; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELL POLARITY; CELL TRANSFORMATION, NEOPLASTIC; DISEASE PROGRESSION; EPITHELIAL CELLS; FEMALE; HUMANS; HYPERPLASIA; MAMMARY GLANDS, ANIMAL; MAMMARY GLANDS, HUMAN; MICE; MICE, INBRED STRAINS; MICROARRAY ANALYSIS; MUTANT PROTEINS; ORGANOGENESIS; PHOSPHORYLATION; PREGNANCY; PROTEIN KINASE C; SURVIVAL ANALYSIS; TRANSGENES;

EID: 77956940449     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.065243     Document Type: Article

References (61)

1. Aranda, V., Haire, T., Nolan, M. E., Calarco, J. P., Rosenberg, A. Z., Fawcett, J. P., Pawson, T. and Muthuswamy, S. K. (2006). Par6-aPKC uncouples ErbB2 induced disruption of polarized epithelial organization from proliferation control. Nat. Cell Biol. 8, 1235-1245.
2. Aranda, V., Nolan, M. E. and Muthuswamy, S. K. (2008). Par complex in cancer: a regulator of normal cell polarity joins the dark side. Oncogene 27, 6878-6887.
3. Baranwal, S. and Alahari, S. K. (2009). Molecular mechanisms controlling E-cadherin expression in breast cancer. Biochem. Biophys. Res. Commun. 384, 6-11.
4. Barcellos-Hoff, M. H., Aggeler, J., Ram, T. G. and Bissell, M. J. (1989). Functional differentiation and alveolar morphogenesis of primary mammary cultures on reconstituted basement membrane. Development 105, 223-235.
5. Bilder, D., Schober, M. and Perrimon, N. (2003). Integrated activity of PDZ protein complexes regulates epithelial polarity. Nat. Cell Biol. 5, 53-58. (Pubitemid 36054329)
6. Blatchford, D. R., Hendry, K. A., Turner, M. D., Burgoyne, R. D. and Wilde, C. J. (1995). Vectorial secretion by constitutive and regulated secretory pathways in mammary epithelial cells. Epithelial Cell Biol. 4, 8-16.
7. Blatchford, D. R., Quarrie, L. H., Tonner, E., McCarthy, C., Flint, D. J. and Wilde, C. J. (1999). Influence of microenvironment on mammary epithelial cell survival in primary culture. J. Cell Physiol. 181, 304-311.
8. Brembeck, F. H., Rosario, M. and Birchmeier, W. (2006). Balancing cell adhesion and Wnt signaling, the key role of beta-catenin. Curr. Opin. Genet. Dev. 16, 51-59.
9. Bundy, L., Wells, S. and Sealy, L. (2005). C/EBPbeta-2 confers EGF-independent growth and disrupts the normal acinar architecture of human mammary epithelial cells. Mol. Cancer 4, 43. (Pubitemid 43046100)
10. Capaldo, C. T. and Macara, I. G. (2007). Depletion of E-cadherin disrupts establishment but not maintenance of cell junctions in Madin-Darby canine kidney epithelial cells. Mol. Biol. Cell 18, 189-200.
11. Cenni, V., Doppler, H., Sonnenburg, E. D., Maraldi, N., Newton, A. C. and Toker, A. (2002). Regulation of novel protein kinase C epsilon by phosphorylation. Biochem. J. 363, 537-545.
12. Chou, M. M., Hou, W., Johnson, J., Graham, L. K., Lee, M. H., Chen, C. S., Newton, A. C., Schaffhausen, B. S. and Toker, A. (1998). Regulation of protein kinase C zeta by PI 3-kinase and PDK-1. Curr. Biol. 8, 1069-1077.
13. Debnath, J. and Brugge, J. S. (2005). Modelling glandular epithelial cancers in three-dimensional cultures. Nat. Rev. Cancer 5, 675-688. (Pubitemid 41486361)
14. Debnath, J., Mills, K. R., Collins, N. L., Reginato, M. J., Muthuswamy, S. K. and Brugge, J. S. (2002). The role of apoptosis in creating and maintaining luminal space within normal and oncogene-expressing mammary acini. Cell 111, 29-40.
15. Debnath, J., Muthuswamy, S. K. and Brugge, J. S. (2003). Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in three-dimensional basement membrane cultures. Methods 30, 256-268.
16. Etienne-Manneville, S. and Hall, A. (2001). Integrin-mediated activation of Cdc42 controls cell polarity in migrating astrocytes through PKCzeta. Cell 106, 489-498.
17. Fukata, M., Nakagawa, M., Itoh, N., Kawajiri, A., Yamaga, M., Kuroda, S. and Kaibuchi, K. (2001a). Involvement of IQGAP1, an effector of Rac1 and Cdc42 GTPases, in cell-cell dissociation during cell scattering. Mol. Cell. Biol. 21, 2165-2183. (Pubitemid 32479637)
18. Fukata, Y., Amano, M. and Kaibuchi, K. (2001b). Rho-Rho-kinase pathway in smooth muscle contraction and cytoskeletal reorganization of non-muscle cells. Trends Pharmacol. Sci. 22, 32-39.
19. Galvez, A. S., Duran, A., Linares, J. F., Pathrose, P., Castilla, E. A., Abu-Baker, S., Leitges, M., Diaz-Meco, M. T. and Moscat, J. (2009). Protein kinase Czeta represses the interleukin-6 promoter and impairs tumorigenesis in vivo. Mol. Cell. Biol. 29, 104-115.
20. Goldstein, B. and Macara, I. G. (2007). The PAR proteins: fundamental players in animal cell polarization. Dev. Cell 13, 609-622.
21. Gotta, M., Abraham, M. C. and Ahringer, J. (2001). CDC-42 controls early cell polarity and spindle orientation in C. elegans. Curr. Biol. 11, 482-488.
22. Gschwendt, M., Kittstein, W. and Marks, F. (1991). Protein kinase C activation by phorbol esters: do cysteine-rich regions and pseudosubstrate motifs play a role? Trends Biochem. Sci. 16, 167-169. (Pubitemid 121004427)
23. Hirai, T. and Chida, K. (2003). Protein kinase Czeta (PKCzeta): activation mechanisms and cellular functions. J. Biochem. 133, 1-7.
24. Hirohashi, S. and Kanai, Y. (2003). Cell adhesion system and human cancer morphogenesis. Cancer Sci. 94, 575-581. (Pubitemid 36975010)
25. Hirose, T., Izumi, Y., Nagashima, Y., Tamai-Nagai, Y., Kurihara, H., Sakai, T., Suzuki, Y., Yamanaka, T., Suzuki, A., Mizuno, K. et al. (2002). Involvement of ASIP/PAR-3 in the promotion of epithelial tight junction formation. J. Cell Sci. 115, 2485-2495.
26. Irie, H. Y., Pearline, R. V., Grueneberg, D., Hsia, M., Ravichandran, P., Kothari, N., Natesan, S. and Brugge, J. S. (2005). Distinct roles of Akt1 and Akt2 in regulating cell migration and epithelial-mesenchymal transition. J. Cell Biol. 171, 1023-1034.
27. Isakoff, S. J., Engelman, J. A., Irie, H. Y., Luo, J., Brachmann, S. M., Pearline, R. V., Cantley, L. C. and Brugge, J. S. (2005). Breast cancer-associated PIK3CA mutations are oncogenic in mammary epithelial cells. Cancer Res. 65, 10992-11000. (Pubitemid 41713369)
28. Izumi, Y., Hirose, T., Tamai, Y., Hirai, S., Nagashima, Y., Fujimoto, T., Tabuse, Y., Kemphues, K. J. and Ohno, S. (1998). An atypical PKC directly associates and colocalizes at the epithelial tight junction with ASIP, a mammalian homologue of Caenorhabditis elegans polarity protein PAR-3. J. Cell Biol. 143, 95-106.
29. Joberty, G., Petersen, C., Gao, L. and Macara, I. G. (2000). The cell-polarity protein Par6 links Par3 and atypical protein kinase C to Cdc42. Nat. Cell Biol. 2, 531-539.
30. Kass, L., Erler, J. T., Dembo, M. and Weaver, V. M. (2007). Mammary epithelial cell: influence of extracellular matrix composition and organization during development and tumorigenesis. Int. J. Biochem. Cell Biol. 39, 1987-1994.
31. Kemphues, K. (2000). PARsing embryonic polarity. Cell 101, 345-348.
32. Kemphues, K. J., Priess, J. R., Morton, D. G. and Cheng, N. S. (1988). Identification of genes required for cytoplasmic localization in early C. elegans embryos. Cell 52, 311-320.
33. Keranen, L. M., Dutil, E. M. and Newton, A. C. (1995). Protein kinase C is regulated in vivo by three functionally distinct phosphorylations. Curr. Biol. 5, 1394-1403.
34. Lin, D., Edwards, A. S., Fawcett, J. P., Mbamalu, G., Scott, J. D. and Pawson, T. (2000). A mammalian PAR-3-PAR-6 complex implicated in Cdc42/Rac1 and aPKC signalling and cell polarity. Nat. Cell Biol. 2, 540-547.
35. Macara, I. G. (2004). Par proteins: partners in polarization. Curr. Biol. 14, R160-R162.
36. Margolis, B. and Borg, J. P. (2005). Apicobasal polarity complexes. J. Cell Sci. 118, 5157-5159.
37. Mohankumar, K. M., Perry, J. K., Kannan, N., Kohno, K., Gluckman, P. D., Emerald, B. S. and Lobie, P. E. (2008). Transcriptional activation of signal transducer and activator of transcription (STAT) 3 and STAT5B partially mediate homeobox A1-stimulated oncogenic transformation of the immortalized human mammary epithelial cell. Endocrinology 149, 2219-2229.
38. Murtagh, J., McArdle, E., Gilligan, E., Thornton, L., Furlong, F. and Martin, F. (2004). Organization of mammary epithelial cells into 3D acinar structures requires glucocorticoid and JNK signaling. J. Cell Biol. 166, 133-143. (Pubitemid 38931923)
39. Muthuswamy, S. K., Li, D., Lelievre, S., Bissell, M. J. and Brugge, J. S. (2001). ErbB2, but not ErbB1, reinitiates proliferation and induces luminal repopulation in epithelial acini. Nat. Cell Biol. 3, 785-792.
40. Nagai-Tamai, Y., Mizuno, K., Hirose, T., Suzuki, A. and Ohno, S. (2002). Regulated protein-protein interaction between aPKC and PAR-3 plays an essential role in the polarization of epithelial cells. Genes Cells 7, 1161-1171.
41. Nguyen, D. A. and Neville, M. C. (1998). Tight junction regulation in the mammary gland. J. Mammary Gland Biol. Neoplasia 3, 233-246.
42. Nolan, M. E., Aranda, V., Lee, S., Lakshmi, B., Basu, S., Allred, D. C. and Muthuswamy, S. K. (2008). The polarity protein Par6 induces cell proliferation and is overexpressed in breast cancer. Cancer Res. 68, 8201-8209.
43. Petersen, O. W., Ronnov-Jessen, L., Howlett, A. R. and Bissell, M. J. (1992). Interaction with basement membrane serves to rapidly distinguish growth and differentiation pattern of normal and malignant human breast epithelial cells. Proc. Natl. Acad. Sci. USA 89, 9064-9068.
44. Plant, P. J., Fawcett, J. P., Lin, D. C., Holdorf, A. D., Binns, K., Kulkarni, S. and Pawson, T. (2003). A polarity complex of mPar-6 and atypical PKC binds, phosphorylates and regulates mammalian Lgl. Nat. Cell Biol. 5, 301-308. (Pubitemid 36432294)
45. Qiu, R. G., Abo, A. and Steven Martin, G. (2000). A human homolog of the C. elegans polarity determinant Par-6 links Rac and Cdc42 to PKCzeta signaling and cell transformation. Curr. Biol. 10, 697-707.
46. Reginato, M. J., Mills, K. R., Becker, E. B., Lynch, D. K., Bonni, A., Muthuswamy, S. K. and Brugge, J. S. (2005). Bim regulation of lumen formation in cultured mammary epithelial acini is targeted by oncogenes. Mol. Cell. Biol. 25, 4591-4601.
47. Sequeira, S. J., Ranganathan, A. C., Adam, A. P., Iglesias, B. V., Farias, E. F. and Aguirre-Ghiso, J. A. (2007). Inhibition of proliferation by PERK regulates mammary acinar morphogenesis and tumor formation. PLoS ONE 2, e615.
48. Seton-Rogers, S. E., Lu, Y., Hines, L. M., Koundinya, M., LaBaer, J., Muthuswamy, S. K. and Brugge, J. S. (2004). Cooperation of the ErbB2 receptor and transforming growth factor beta in induction of migration and invasion in mammary epithelial cells. Proc. Natl. Acad. Sci. USA 101, 1257-1262. (Pubitemid 38182676)
49. Shin, K., Fogg, V. C. and Margolis, B. (2006). Tight junctions and cell polarity. Annu. Rev. Cell Dev. Biol. 22, 207-235.
50. Standaert, M. L., Galloway, L., Karnam, P., Bandyopadhyay, G., Moscat, J. and Farese, R. V. (1997). Protein kinase C-zeta as a downstream effector of phosphatidylinositol 3-kinase during insulin stimulation in rat adipocytes. Potential role in glucose transport. J. Biol. Chem. 272, 30075-30082.
51. Standaert, M. L., Bandyopadhyay, G., Perez, L., Price, D., Galloway, L., Poklepovic, A., Sajan, M. P., Cenni, V., Sirri, A., Moscat, J. et al. (1999). Insulin activates protein kinases C-zeta and C-lambda by an autophosphorylation- dependent mechanism and stimulates their translocation to GLUT4 vesicles and other membrane fractions in rat adipocytes. J. Biol. Chem. 274, 25308-25316.
52. Suzuki, A., Yamanaka, T., Hirose, T., Manabe, N., Mizuno, K., Shimizu, M., Akimoto, K., Izumi, Y., Ohnishi, T. and Ohno, S. (2001). Atypical protein kinase C is involved in the evolutionarily conserved par protein complex and plays a critical role in establishing epithelia-specific junctional structures. J. Cell Biol. 152, 1183-1196.
53. Tsutakawa, S. E., Medzihradszky, K. F., Flint, A. J., Burlingame, A. L. and Koshland, D. E., Jr (1995). Determination of in vivo phosphorylation sites in protein kinase C. J. Biol. Chem. 270, 26807-26812.
54. Tunggal, J. A., Helfrich, I., Schmitz, A., Schwarz, H., Gunzel, D., Fromm, M., Kemler, R., Krieg, T. and Niessen, C. M. (2005). E-cadherin is essential for in vivo epidermal barrier function by regulating tight junctions. EMBO J. 24, 1146-1156.
55. van de Vijver, M. J., He, Y. D., van't Veer, L. J., Dai, H., Hart, A. A., Voskuil, D. W., Schreiber, G. J., Peterse, J. L., Roberts, C., Marton, M. J. et al. (2002). A gene-expression signature as a predictor of survival in breast cancer. N. Engl. J. Med. 347, 1999-2009.
56. Weaver, V. M., Petersen, O. W., Wang, F., Larabell, C. A., Briand, P., Damsky, C. and Bissell, M. J. (1997). Reversion of the malignant phenotype of human breast cells in three-dimensional culture and in vivo by integrin blocking antibodies. J. Cell Biol. 137, 231-245.
57. Weaver, V. M., Lelievre, S., Lakins, J. N., Chrenek, M. A., Jones, J. C., Giancotti, F., Werb, Z. and Bissell, M. J. (2002). beta4 integrin-dependent formation of polarized three-dimensional architecture confers resistance to apoptosis in normal and malignant mammary epithelium. Cancer Cell 2, 205-216.
58. Wodarz, A. (2000). Tumor suppressors: linking cell polarity and growth control. Curr. Biol. 10, R624-R626.
59. Wodarz, A. and Nathke, I. (2007). Cell polarity in development and cancer. Nat. Cell Biol. 9, 1016-1024.
60. Yamanaka, T., Horikoshi, Y., Suzuki, A., Sugiyama, Y., Kitamura, K., Maniwa, R., Nagai, Y., Yamashita, A., Hirose, T., Ishikawa, H. et al. (2001). PAR-6 regulates aPKC activity in a novel way and mediates cell-cell contact-induced formation of the epithelial junctional complex. Genes Cells 6, 721-731.
61. Zhan, L., Rosenberg, A., Bergami, K. C., Yu, M., Xuan, Z., Jaffe, A. B., Allred, C. and Muthuswamy, S. K. (2008). Deregulation of scribble promotes mammary tumorigenesis and reveals a role for cell polarity in carcinoma. Cell 135, 865-878.