Dystroglycan controls signaling of multiple hormones through modulation of STAT5 activity

Journal of Cell Science

Volumn 123, Issue 21, 2010, Pages 3683-3692

  Leonoudakis, Dmitri ^a   Singh, Manisha ^a   Mohajer, Roozbeh ^a   Mohajer, Pouya ^a   Fata, Jimmie E ^b   Campbell, Kevin P ^c   Muschler, John L ^a  

^a CALIFORNIA PACIFIC MEDICAL CENTER   (United States)

^b CITY UNIVERSITY OF NEW YORK   (United States)

^c UNIVERSITY OF IOWA   (United States)

Author keywords

Dystroglycan; Epithelial; Growth hormone; Laminin; Mammary; Prolactin; STAT5

Indexed keywords

DYSTROGLYCAN; GROWTH HORMONE; LAMININ; MEMBRANE PROTEIN; PROLACTIN; STAT5 PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BASEMENT MEMBRANE; BREAST EPITHELIUM; CELL SURFACE; CONTROLLED STUDY; CYTOPLASM; DAG1 GENE; FEMALE; HORMONAL REGULATION; MAMMARY GLAND; MOUSE; NONHUMAN; NULL ALLELE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; RECEPTOR BINDING; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TISSUE GROWTH;

ANIMALS; BASEMENT MEMBRANE; DYSTROGLYCANS; EPITHELIUM; FEMALE; GROWTH HORMONE; LACTATION; LAMININ; MAMMARY GLANDS, ANIMAL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MORPHOGENESIS; PREGNANCY; PROLACTIN; PROTEIN BINDING; SIGNAL TRANSDUCTION; STAT5 TRANSCRIPTION FACTOR;

MAMMALIA;

EID: 78149370128     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.070680     Document Type: Article

References (62)

1. Akhtar, N., Marlow, R., Lambert, E., Schatzmann, F., Lowe, E. T., Cheung, J., Katz, E., Li, W., Wu, C., Dedhar, S. et al. (2009). Molecular dissection of integrin signalling proteins in the control of mammary epithelial development and differentiation. Development 136, 1019-1027.
2. Bao, X., Kobayashi, M., Hatakeyama, S., Angata, K., Gullberg, D., Nakayama, J., Fukuda, M. N. and Fukuda, M. (2009). Tumor suppressor function of laminin-binding alpha-dystroglycan requires a distinct beta3-N- acetylglucosaminyltransferase. Proc. Natl. Acad. Sci. USA 106, 12109-12114.
3. Barresi, R. and Campbell, K. P. (2006). Dystroglycan: from biosynthesis to pathogenesis of human disease. J. Cell Sci. 119, 199-207.
4. Beggs, H. E., Schahin-Reed, D., Zang, K., Goebbels, S., Nave, K. A., Gorski, J., Jones, K. R., Sretavan, D. and Reichardt, L. F. (2003). FAK deficiency in cells contributing to the basal lamina results in cortical abnormalities resembling congenital muscular dystrophies. Neuron 40, 501-514.
5. Beltran-Valero de Bernabe, D., Inamori, K. I., Yoshida-Moriguchi, T., Weydert, C. J., Harper, H. A., Willer, T., Henry, M. D. and Campbell, K. P. (2009). Loss of alpha-dystroglycan laminin binding in epithelium-derived cancers is caused by silencing of large. J. Biol. Chem. 284, 11279-11284.
6. Bissell, M. J., Radisky, D. C., Rizki, A., Weaver, V. M. and Petersen, O. W. (2002). The organizing principle: microenvironmental influences in the normal and malignant breast. Differentiation 70, 537-546.
7. Calogero, A., Pavoni, E., Gramaglia, T., D'Amati, G., Ragona, G., Brancaccio, A. and Petrucci, T. C. (2006). Altered expression of alpha-dystroglycan subunit in human gliomas. Cancer Biol. Ther. 5, 441-448.
8. Cohn, R. D. and Campbell, K. P. (2000). Molecular basis of muscular dystrophies. Muscle Nerve 23, 1456-1471.
9. Cohn, R. D., Henry, M. D., Michele, D. E., Barresi, R., Saito, F., Moore, S. A., Flanagan, J. D., Skwarchuk, M. W., Robbins, M. E., Mendell, J. R. et al. (2002). Disruption of DAG1 in differentiated skeletal muscle reveals a role for dystroglycan in muscle regeneration. Cell 110, 639-648.
10. Cotarla, I., Ren, S., Zhang, Y., Gehan, E., Singh, B. and Furth, P. A. (2004). Stat5a is tyrosine phosphorylated and nuclear localized in a high proportion of human breast cancers. Int. J. Cancer 108, 665-671.
11. Cote, P. D., Moukhles, H., Lindenbaum, M. and Carbonetto, S. (1999). Chimaeric mice deficient in dystroglycans develop muscular dystrophy and have disrupted myoneural synapses. Nat. Genet. 23, 338-342.
12. Cui, Y., Riedlinger, G., Miyoshi, K., Tang, W., Li, C., Deng, C. X., Robinson, G. W. and Hennighausen, L. (2004). Inactivation of Stat5 in mouse mammary epithelium during pregnancy reveals distinct functions in cell proliferation, survival, and differentiation. Mol. Cell. Biol. 24, 8037-8047.
13. Dassule, H. R., Lewis, P., Bei, M., Maas, R. and McMahon, A. P. (2000). Sonic hedgehog regulates growth and morphogenesis of the tooth. Development 127, 4775-4785.
14. Durbeej, M. and Campbell, K. P. (2002). Muscular dystrophies involving the dystrophin-glycoprotein complex: an overview of current mouse models. Curr. Opin. Genet. Dev. 12, 349-361.
15. Durbeej, M., Henry, M. D., Ferletta, M., Campbell, K. P. and Ekblom, P. (1998). Distribution of dystroglycan in normal adult mouse tissues. J. Histochem. Cytochem. 46, 449-457.
16. Durbeej, M., Talts, J. F., Henry, M. D., Yurchenco, P. D., Campbell, K. P. and Ekblom, P. (2001). Dystroglycan binding to laminin alpha1LG4 module influences epithelial morphogenesis of salivary gland and lung in vitro. Differentiation 69, 121-134.
17. Ervasti, J. M. and Campbell, K. P. (1993). A role for the dystrophin-glycoprotein complex as a transmembrane linker between laminin and actin. J. Cell Biol. 122, 809-823.
18. Esser, A. K., Cohen, M. B. and Henry, M. D. (2010). Dystroglycan is not required for maintenance of the luminal epithelial basement membrane or cell polarity in the mouse prostate. Prostate 70, 777-787.
19. Graus-Porta, D., Blaess, S., Senften, M., Littlewood-Evans, A., Damsky, C., Huang, Z., Orban, P., Klein, R., Schittny, J. C. and Muller, U. (2001). Beta1-class integrins regulate the development of laminae and folia in the cerebral and cerebellar cortex. Neuron 31, 367-379.
20. Han, R., Kanagawa, M., Yoshida-Moriguchi, T., Rader, E. P., Ng, R. A., Michele, D. E., Muirhead, D. E., Kunz, S., Moore, S. A., Iannaccone, S. T. et al. (2009). Basal lamina strengthens cell membrane integrity via the laminin G domain-binding motif of {alpha}-dystroglycan. Proc. Natl. Acad. Sci. USA 106, 12573-12579.
21. Hennighausen, L. and Robinson, G. W. (2008). Interpretation of cytokine signaling through the transcription factors STAT5A and STAT5B. Genes Dev. 22, 711-721.
22. Henry, M. D. and Campbell, K. P. (1998). A role for dystroglycan in basement membrane assembly. Cell 95, 859-870.
23. Henry, M. D., Cohen, M. B. and Campbell, K. P. (2001a). Reduced expression of dystroglycan in breast and prostate cancer. Hum. Pathol. 32, 791-795.
24. Henry, M. D., Satz, J. S., Brakebusch, C., Costell, M., Gustafsson, E., Fassler, R. and Campbell, K. P. (2001b). Distinct roles for dystroglycan, 1 integrin and perlecan in cell surface laminin organization. J. Cell Sci. 114, 1137-1144.
25. Jonkers, J., Meuwissen, R., van der Gulden, H., Peterse, H., van der Valk, M. and Berns, A. (2001). Synergistic tumor suppressor activity of BRCA2 and p53 in a conditional mouse model for breast cancer. Nat. Genet. 29, 418-425.
26. Kelly, P. A., Bachelot, A., Kedzia, C., Hennighausen, L., Ormandy, C. J., Kopchick, J. J. and Binart, N. (2002). The role of prolactin and growth hormone in mammary gland development. Mol. Cell. Endocrinol. 197, 127-131.
27. Klover, P. and Hennighausen, L. (2007). Postnatal body growth is dependent on the transcription factors signal transducers and activators of transcription 5a/b in muscle: a role for autocrine/paracrine insulin-like growth factor I. Endocrinology 148, 1489-1497.
28. Lee, Y., Kameya, S., Cox, G. A., Hsu, J., Hicks, W., Maddatu, T. P., Smith, R. S., Naggert, J. K., Peachey, N. S. and Nishina, P. M. (2005). Ocular abnormalities in Large(myd) and Large(vls) mice, spontaneous models for muscle, eye, and brain diseases. Mol. Cell. Neurosci. 30, 160-172.
29. Levedakou, E. N., Chen, X. J., Soliven, B. and Popko, B. (2005). Disruption of the mouse Large gene in the enr and myd mutants results in nerve, muscle, and neuromuscular junction defects. Mol. Cell. Neurosci. 28, 757-769.
30. Li, N., Zhang, Y., Naylor, M. J., Schatzmann, F., Maurer, F., Wintermantel, T., Schuetz, G., Mueller, U., Streuli, C. H. and Hynes, N. E. (2005). Beta1 integrins regulate mammary gland proliferation and maintain the integrity of mammary alveoli. EMBO J. 24, 1942-1953.
31. Li, S., Harrison, D., Carbonetto, S., Fassler, R., Smyth, N., Edgar, D. and Yurchenco, P. D. (2002). Matrix assembly, regulation, and survival functions of laminin and its receptors in embryonic stem cell differentiation. J. Cell Biol. 157, 1279-1290.
32. Liu, X., Robinson, G. W., Wagner, K. U., Garrett, L., Wynshaw-Boris, A. and Hennighausen, L. (1997). Stat5a is mandatory for adult mammary gland development and lactogenesis. Genes Dev. 11, 179-186.
33. Markham, K., Schuurmans, C. and Weiss, S. (2007). STAT5A/B activity is required in the developing forebrain and spinal cord. Mol. Cell. Neurosci. 35, 272-282.
34. Martin, L. T., Glass, M., Dosunmu, E. and Martin, P. T. (2007). Altered expression of natively glycosylated alpha dystroglycan in pediatric solid tumors. Hum. Pathol. 38, 1657-1668.
35. Miner, J. H. and Yurchenco, P. D. (2004). Laminin functions in tissue morphogenesis. Annu. Rev. Cell Dev. Biol. 20, 255-284.
36. Miyagoe, Y., Hanaoka, K., Nonaka, I., Hayasaka, M., Nabeshima, Y., Arahata, K., Nabeshima, Y. and Takeda, S. (1997). Laminin alpha2 chain-null mutant mice by targeted disruption of the Lama2 gene: a new model of merosin (laminin 2)-deficient congenital muscular dystrophy. FEBS Lett. 415, 33-39.
37. Moore, S. A., Saito, F., Chen, J., Michele, D. E., Henry, M. D., Messing, A., Cohn, R. D., Ross-Barta, S. E., Westra, S., Williamson, R. A. et al. (2002). Deletion of brain dystroglycan recapitulates aspects of congenital muscular dystrophy. Nature 418, 422-425.
38. Muntoni, F., Torelli, S. and Brockington, M. (2008). Muscular dystrophies due to glycosylation defects. Neurotherapeutics 5, 627-632.
39. Muschler, J., Lochter, A., Roskelley, C. D., Yurchenco, P. and Bissell, M. J. (1999). Division of labor among the alpha6beta4 integrin, beta1 integrins, and an E3 laminin receptor to signal morphogenesis and beta-casein expression in mammary epithelial cells. Mol. Biol. Cell 10, 2817-2828.
40. Muschler, J., Levy, D., Boudreau, R., Henry, M., Campbell, K. and Bissell, M. J. (2002). A role for dystroglycan in epithelial polarization: loss of function in breast tumor cells. Cancer Res. 62, 7102-7109.
41. Nagy, T., Wei, H., Shen, T. L., Peng, X., Liang, C. C., Gan, B. and Guan, J. L. (2007). Mammary epithelial-specific deletion of the focal adhesion kinase gene leads to severe lobulo-alveolar hypoplasia and secretory immaturity of the murine mammary gland. J. Biol. Chem. 282, 31766-31776.
42. Naylor, M. J., Li, N., Cheung, J., Lowe, E. T., Lambert, E., Marlow, R., Wang, P., Schatzmann, F., Wintermantel, T., Schuetz, G. et al. (2005). Ablation of beta1 integrin in mammary epithelium reveals a key role for integrin in glandular morphogenesis and differentiation. J. Cell Biol. 171, 717-728.
43. Niewmierzycka, A., Mills, J., St-Arnaud, R., Dedhar, S. and Reichardt, L. F. (2005). Integrin-linked kinase deletion from mouse cortex results in cortical lamination defects resembling cobblestone lissencephaly. J. Neurosci. 25, 7022-7031.
44. Nishimune, H., Valdez, G., Jarad, G., Moulson, C. L., Muller, U., Miner, J. H. and Sanes, J. R. (2008). Laminins promote postsynaptic maturation by an autocrine mechanism at the neuromuscular junction. J. Cell Biol. 182, 1201-1215.
45. Oakes, S. R., Rogers, R. L., Naylor, M. J. and Ormandy, C. J. (2008). Prolactin regulation of mammary gland development. J. Mammary Gland Biol. Neoplasia 13, 13-28.
46. Philp, J. A., Burdon, T. G. and Watson, C. J. (1996). Differential activation of STATs 3 and 5 during mammary gland development. FEBS Lett. 396, 77-80.
47. Reed, U. C. (2009). Congenital muscular dystrophy. Part II: a review of pathogenesis and therapeutic perspectives. Arq. Neuropsiquiatr. 67, 343-362.
48. Robinson, G. W. (2007). Cooperation of signalling pathways in embryonic mammary gland development. Nat. Rev. Genet. 8, 963-972.
49. Satz, J. S., Barresi, R., Durbeej, M., Willer, T., Turner, A., Moore, S. A. and Campbell, K. P. (2008). Brain and eye malformations resembling Walker-Warburg syndrome are recapitulated in mice by dystroglycan deletion in the epiblast. J. Neurosci. 28, 10567-10575.
50. Sgambato, A., Migaldi, M., Montanari, M., Camerini, A., Brancaccio, A., Rossi, G., Cangiano, R., Losasso, C., Capelli, G., Trentini, G. P. et al. (2003). Dystroglycan expression is frequently reduced in human breast and colon cancers and is associated with tumor progression. Am. J. Pathol. 162, 849-860.
51. Sgambato, A., Camerini, A., Faraglia, B., Pavoni, E., Montanari, M., Spada, D., Losasso, C., Brancaccio, A. and Cittadini, A. (2004). Increased expression of dystroglycan inhibits the growth and tumorigenicity of human mammary epithelial cells. Cancer Biol. Ther. 3, 967-975.
52. Singh, J., Itahana, Y., Knight-Krajewski, S., Kanagawa, M., Campbell, K. P., Bissell, M. J. and Muschler, J. (2004). Proteolytic enzymes and altered glycosylation modulate dystroglycan function in carcinoma cells. Cancer Res. 64, 6152-6159.
53. Soriano, P. (1999). Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 21, 70-71.
54. Streuli, C. H., Schmidhauser, C., Bailey, N., Yurchenco, P., Skubitz, A. P., Roskelley, C. and Bissell, M. J. (1995). Laminin mediates tissue-specific gene expression in mammary epithelia. J. Cell Biol. 129, 591-603.
55. Tan, S. H. and Nevalainen, M. T. (2008). Signal transducer and activator of transcription 5A/B in prostate and breast cancers. Endocr. Relat. Cancer 15, 367-390.
56. Wagner, K. U., Young, W. S., 3rd, Liu, X., Ginns, E. I., Li, M., Furth, P. A. and Hennighausen, L. (1997). Oxytocin and milk removal are required for post-partum mammary-gland development. Genes Funct. 1, 233-244.
57. Wagner, K. U., Krempler, A., Triplett, A. A., Qi, Y., George, N. M., Zhu, J. and Rui, H. (2004). Impaired alveologenesis and maintenance of secretory mammary epithelial cells in Jak2 conditional knockout mice. Mol. Cell. Biol. 24, 5510-5520.
58. Weir, M. L., Oppizzi, M. L., Henry, M. D., Onishi, A., Campbell, K. P., Bissell, M. J. and Muschler, J. L. (2006). Dystroglycan loss disrupts polarity and β-casein induction in mammary epithelial cells by perturbing laminin anchoring. J. Cell Sci. 119, 4047-4058.
59. Xu, R., Nelson, C. M., Muschler, J. L., Veiseh, M., Vonderhaar, B. K. and Bissell, M. J. (2009). Sustained activation of STAT5 is essential for chromatin remodeling and maintenance of mammary-specific function. J. Cell Biol. 184, 57-66.
60. Yoshida-Moriguchi, T., Yu, L., Stalnaker, S. H., Davis, S., Kunz, S., Madson, M., Oldstone, M. B., Schachter, H., Wells, L. and Campbell, K. P. (2010). O-mannosyl phosphorylation of alpha-dystroglycan is required for laminin binding. Science 327, 88-92.
61. Yurchenco, P. D. and Patton, B. L. (2009). Developmental and pathogenic mechanisms of basement membrane assembly. Curr. Pharm. Des. 15, 1277-1294.
62. Yurchenco, P. D., Amenta, P. S. and Patton, B. L. (2004). Basement membrane assembly, stability and activities observed through a developmental lens. Matrix Biol. 22, 521-538.