Endocytic trafficking of laminin is controlled by dystroglycan and is disrupted in cancers

Journal of Cell Science

Volumn 127, Issue 22, 2014, Pages 4894-4903

  Leonoudakis, Dmitri ^a   Huang, Ge ^b   Akhavan, Armin ^a   Fata, Jimmie E ^c   Singh, Manisha ^a   Gray, Joe W ^b,d   Muschler, John L ^a,b  

^a CALIFORNIA PACIFIC MEDICAL CENTER   (United States)

^b Oregon Health and Science University Department of Biomedical Engineering   (United States)

^c CITY UNIVERSITY OF NEW YORK   (United States)

^d OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Cancer; Dystroglycan; Endocytosis; Laminin

Indexed keywords

DYNAMIN; DYSTROGLYCAN; FLUORESCEIN ISOTHIOCYANATE DEXTRAN; LAMININ; LAMININ RECEPTOR; LEUPEPTIN;

ANIMAL CELL; ARTICLE; BREAST CANCER CELL LINE; BREAST EPITHELIUM; CANCER CELL; CELL COMMUNICATION; CELL MIGRATION; CELL SURFACE; CONTROLLED STUDY; ENDOCYTOSIS; ENDOSOME; GLIOBLASTOMA CELL LINE; HUMAN; HUMAN CELL; INTERNALIZATION; LYSOSOME; MOUSE; MULTIVESICULAR BODY; MUSCULAR DYSTROPHY; NEOPLASM; NONHUMAN; PROTEIN DEGRADATION; PROTEIN FUNCTION; ANIMAL; BASEMENT MEMBRANE; CYTOLOGY; FEMALE; KNOCKOUT MOUSE; MAMMARY GLAND; METABOLISM; PREGNANCY; UDDER;

ANIMALS; BASEMENT MEMBRANE; DYSTROGLYCANS; ENDOCYTOSIS; FEMALE; HUMANS; LAMININ; MAMMARY GLANDS, ANIMAL; MAMMARY GLANDS, HUMAN; MICE; MICE, KNOCKOUT; NEOPLASMS; PREGNANCY;

EID: 84911962511     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.152728     Document Type: Article

References (48)

1. Akhavan, A., Griffith, O. L., Soroceanu, L., Leonoudakis, D., Luciani-Torres, M. G., Daemen, A., Gray, J. W. and Muschler, J. L. (2012). Loss of cell-surface laminin anchoring promotes tumor growth and is associated with poor clinical outcomes. Cancer Res. 72, 2578-2588.
2. Atsma, D. E., Bastiaanse, E. M., Jerzewski, A., Van der Valk, L. J. and Van der Laarse, A. (1995). Role of calcium-activated neutral protease (calpain) in cell death in cultured neonatal rat cardiomyocytes during metabolic inhibition. Circ. Res. 76, 1071-1078.
3. Barresi, R. and Campbell, K. P. (2006). Dystroglycan: from biosynthesis to pathogenesis of human disease. J. Cell Sci. 119, 199-207.
4. Beltrán-Valero de Bernabé, D., Inamori, K., 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.
5. Caswell, P. T., Vadrevu, S. and Norman, J. C. (2009). Integrins: masters and slaves of endocytic transport. Nat. Rev. Mol. Cell Biol. 10, 843-853.
6. Choe, H., Jemielity, S., Abraham, J., Radoshitzky, S. R. and Farzan, M. (2011). Transferrin receptor 1 in the zoonosis and pathogenesis of New World hemorrhagic fever arenaviruses. Curr. Opin. Microbiol. 14, 476-482.
7. Colognato, H., Winkelmann, D. A. and Yurchenco, P. D. (1999). Laminin polymerization induces a receptor-cytoskeleton network. J. Cell Biol. 145, 619-631.
8. Coopman, P., Nuydens, R., Leunissen, J., De Brabander, M., Bortier, H., Foidart, J. M. and Mareel, M. (1991). Laminin binding and internalization by human and murine mammary gland cell lines in vitro. Eur. J. Cell Biol. 56, 251-259.
9. Daemen, A., Griffith, O. L., Heiser, L. M., Wang, N. J., Enache, O. M., Sanborn, Z., Pepin, F., Durinck, S., Korkola, J. E., Griffith, M. et al. (2013). Modeling precision treatment of breast cancer. Genome Biol. 14, R110.
10. Domogatskaya, A., Rodin, S. and Tryggvason, K. (2012). Functional diversity of laminins. Annu. Rev. Cell Dev. Biol. 28, 523-553.
11. Duclos, S., Corsini, R. and Desjardins, M. (2003). Remodeling of endosomes during lysosome biogenesis involves 'kiss and run' fusion events regulated by rab5. J. Cell Sci. 116, 907-918.
12. 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.
13. Harrison, D., Hussain, S. A., Combs, A. C., Ervasti, J. M., Yurchenco, P. D. and Hohenester, E. (2007). Crystal structure and cell surface anchorage sites of laminin alpha1LG4-5. J. Biol. Chem. 282, 11573-11581.
14. Heuser, J. E. and Anderson, R. G. (1989). Hypertonic media inhibit receptormediated endocytosis by blocking clathrin-coated pit formation. J. Cell Biol. 108, 389-400.
15. Hohenester, E. and Yurchenco, P. D. (2013). Laminins in basement membrane assembly. Cell Adh. Migr. 7, 56-63.
16. Jae, L. T., Raaben, M., Herbert, A. S., Kuehne, A. I., Wirchnianski, A. S., Soh, T. K., Stubbs, S. H., Janssen, H., Damme, M., Saftig, P. et al. (2014). Virus entry. Lassa virus entry requires a trigger-induced receptor switch. Science 344, 1506-1510.
17. Leonoudakis, D., Singh, M., Mohajer, R., Mohajer, P., Fata, J. E., Campbell, K. P. and Muschler, J. L. (2010). Dystroglycan controls signaling of multiple hormones through modulation of STAT5 activity. J. Cell Sci. 123, 3683-3692.
18. Liotta, L. A., Wewer, U., Rao, N. C., Schiffmann, E., Stracke, M., Guirguis, R., Thorgeirsson, U., Muschel, R. and Sobel, M. (1987). Biochemical mechanisms of tumor invasion and metastasis. Anticancer Drug Des. 2, 195-202.
19. Luo, B. H., Carman, C. V., Takagi, J. and Springer, T. A. (2005). Disrupting integrin transmembrane domain heterodimerization increases ligand binding affinity, not valency or clustering. Proc. Natl. Acad. Sci. USA 102, 3679-3684.
20. Macia, E., Ehrlich, M., Massol, R., Boucrot, E., Brunner, C. and Kirchhausen, T. (2006). Dynasore, a cell-permeable inhibitor of dynamin. Dev. Cell 10, 839-850.
21. Madsen, D. H., Ingvarsen, S., Jürgensen, H. J., Melander, M. C., Kjøller, L., Moyer, A., Honoré, C., Madsen, C. A., Garred, P., Burgdorf, S. et al. (2011). The non-phagocytic route of collagen uptake: a distinct degradation pathway. J. Biol. Chem. 286, 26996-27010.
22. Mellman, I. and Yarden, Y. (2013). Endocytosis and cancer. Cold Spring Harb. Perspect. Biol. 5, a016949.
23. Memmo, L. M. and McKeown-Longo, P. (1998). The alphavbeta5 integrin functions as an endocytic receptor for vitronectin. J. Cell Sci. 111, 425-433.
24. Mercuri, E. and Muntoni, F. (2012). The ever-expanding spectrum of congenital muscular dystrophies. Ann. Neurol. 72, 9-17.
25. Oldstone, M. B. and Campbell, K. P. (2011). Decoding arenavirus pathogenesis: essential roles for alpha-dystroglycan-virus interactions and the immune response. Virology 411, 170-179.
26. Oppizzi, M. L., Akhavan, A., Singh, M., Fata, J. E. and Muschler, J. L. (2008). Nuclear translocation of beta-dystroglycan reveals a distinctive trafficking pattern of autoproteolyzed mucins. Traffic 9, 2063-2072.
27. Pasqual, G., Rojek, J. M., Masin, M., Chatton, J. Y. and Kunz, S. (2011). Old world arenaviruses enter the host cell via the multivesicular body and depend on the endosomal sorting complex required for transport. PLoS Pathog. 7, e1002232.
28. Polo, S. and Di Fiore, P. P. (2006). Endocytosis conducts the cell signaling orchestra. Cell 124, 897-900.
29. Rambukkana, A., Yamada, H., Zanazzi, G., Mathus, T., Salzer, J. L., Yurchenco, P. D., Campbell, K. P. and Fischetti, V. A. (1998). Role of alpha-dystroglycan as a Schwann cell receptor for Mycobacterium leprae. Science 282, 2076-2079.
30. Rowe, R. G. and Weiss, S. J. (2008). Breaching the basement membrane: who, when and how? Trends Cell Biol. 18, 560-574.
31. Sambrook, J., Fritsch, E. F. andManiatis, T. (1989). Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
32. Sato, S., Omori, Y., Katoh, K., Kondo, M., Kanagawa, M., Miyata, K., Funabiki, K., Koyasu, T., Kajimura, N., Miyoshi, T. et al. (2008). Pikachurin, a dystroglycan ligand, is essential for photoreceptor ribbon synapse formation. Nat. Neurosci. 11, 923-931.
33. Schittny, J. C. and Yurchenco, P. D. (1990). Terminal short arm domains of basement membrane laminin are critical for its self-assembly. J. Cell Biol. 110, 825-832.
34. Scita, G. and Di Fiore, P. P. (2010). The endocytic matrix. Nature 463, 464-473.
35. Shi, F. and Sottile, J. (2008). Caveolin-1-dependent beta1 integrin endocytosis is a critical regulator of fibronectin turnover. J. Cell Sci. 121, 2360-2371.
36. Shi, F. and Sottile, J. (2011). MT1-MMP regulates the turnover and endocytosis of extracellular matrix fibronectin. J. Cell Sci. 124, 4039-4050.
37. Shi, F., Harman, J., Fujiwara, K. and Sottile, J. (2010). Collagen I matrix turnover is regulated by fibronectin polymerization. Am. J. Physiol. 298, C1265-C1275.
38. 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.
39. Singhal, N. and Martin, P. T. (2011). Role of extracellular matrix proteins and their receptors in the development of the vertebrate neuromuscular junction. Dev. Neurobiol. 71, 982-1005.
40. Sorkin, A. and von Zastrow, M. (2009). Endocytosis and signalling: intertwining molecular networks. Nat. Rev. Mol. Cell Biol. 10, 609-622.
41. Sottile, J. and Chandler, J. (2005). Fibronectin matrix turnover occurs through a caveolin-1-dependent process. Mol. Biol. Cell 16, 757-768.
42. Streuli, C. (1999). Extracellular matrix remodelling and cellular differentiation. Curr. Opin. Cell Biol. 11, 634-640.
43. 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.
44. Waite, A., Brown, S. C. and Blake, D. J. (2012). The dystrophin-glycoprotein complex in brain development and disease. Trends Neurosci. 35, 487-496.
45. 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 betacasein induction in mammary epithelial cells by perturbing laminin anchoring. J. Cell Sci. 119, 4047-4058.
46. 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.
47. Yurchenco, P. D. (2011). Basement membranes: cell scaffoldings and signaling platforms. Cold Spring Harb. Perspect. Biol. 3, a004911.
48. Yurchenco, P. D. and Patton, B. L. (2009). Developmental and pathogenic mechanisms of basement membrane assembly. Curr. Pharm. Des. 15, 1277-1294.