Platelet-derived growth factor β-receptor, transforming growth factor β type I receptor, and CD44 protein modulate each other's signaling and stability

Journal of Biological Chemistry

Volumn 289, Issue 28, 2014, Pages 19747-19757

  Porsch, Helena ^a   Mehić, Merima ^a   Olofsson, Berit ^a   Heldin, Paraskevi ^a   Heldin, Carl Henrik ^a  

^a UPPSALA UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CULTURE; CROSSTALK; ENZYMES; FIBROBLASTS; PHOSPHORYLATION; PLATELETS; PROTEINS;

CELLULAR FUNCTION; CONTEXT DEPENDENT; DERMAL FIBROBLASTS; KINASE ACTIVITY; PLATELET-DERIVED GROWTH FACTORS; RECEPTOR PROTEINS; SIGNALING PATHWAYS; TRANSFORMING GROWTH FACTORS;

SIGNALING;

HERMES ANTIGEN; PLATELET DERIVED GROWTH FACTOR BB; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; SMAD2 PROTEIN; SMALL INTERFERING RNA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 1;

ARTICLE; CELL MIGRATION; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; HUMAN; HUMAN CELL; INTERNALIZATION; INTRACELLULAR SIGNALING; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; SIGNAL TRANSDUCTION; SKIN FIBROBLAST;

CD44; CELL SIGNALING; CELL SURFACE RECEPTOR; CELLULAR REGULATION; PDGF; TRANSFORMING GROWTH FACTOR Β (TGF-Β);

ANIMALS; ANTIGENS, CD44; CERCOPITHECUS AETHIOPS; COS CELLS; HUMANS; PROTEIN BINDING; PROTEIN STABILITY; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS C-SIS; RECEPTOR, PLATELET-DERIVED GROWTH FACTOR BETA; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA;

EID: 84904154934     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.547273     Document Type: Article

References (58)

1. Heldin, C. H., and Westermark, B. (1999) Mechanism of action and in vivo role of platelet-derived growth factor. Physiol. Rev. 79, 1283-1316
2. Andrae, J., Gallini, R., and Betsholtz, C. (2008) Role of platelet-derived growth factors in physiology and medicine. Genes Dev. 22, 1276-1312 (Pubitemid 351717519)
3. Hellberg, C., Schmees, C., Karlsson, S., Ahgren, A., and Heldin, C. H. (2009) Activation of protein kinase Cα is necessary for sorting the PDGFβ-receptor to Rab4a-dependent recycling. Mol. Biol. Cell 20, 2856-2863
4. Shi, Y., and Massagué, J. (2003) Mechanisms of TGF-β signaling from cell membrane to the nucleus. Cell 113, 685-700 (Pubitemid 36724933)
5. Zhang, Y. E. (2009) Non-Smad pathways in TGF-β signaling. Cell Res. 19, 128-139
6. Shibanaka, Y., Hayashi, H., Umemura, I., Fujisawa, Y., Okamoto, M., Takai, M., and Fujita, N. (1994) Eclosion hormone-mediated signal transduction in the silkworm abdominal ganglia: Involvement of a cascade from inositol(1,4,5)trisphosphate to cyclic GMP. Biochem. Biophys. Res. Commun. 198, 613-618 (Pubitemid 24178412)
7. Chen, Y. G. (2009) Endocytic regulation of TGF-β signaling. Cell Res. 19, 58-70
8. Tsukazaki, T., Chiang, T. A., Davison, A. F., Attisano, L., and Wrana, J. L. (1998) SARA, a FYVE domain protein that recruits Smad2 to the TGFβ receptor. Cell 95, 779-791 (Pubitemid 29014458)
9. Di Guglielmo, G. M., Le Roy, C., Goodfellow, A. F., and Wrana, J. L. (2003) Distinct endocytic pathways regulate TGF-β receptor signalling and turnover. Nat. Cell Biol. 5, 410-421 (Pubitemid 36592263)
10. Feng, X. H., and Derynck, R. (2005) Specificity and versatility in tgf-β signaling through Smads. Annu. Rev. Cell Dev. Biol. 21, 659-693
11. Heldin, C. H., Vanlandewijck, M., and Moustakas, A. (2012) Regulation of EMT by TGFβ in cancer. FEBS Lett. 586, 1959-1970
12. Moustakas, A., and Heldin, P. (2014) TGFβ and matrix-regulated epithelial to mesenchymal transition. Biochim. Biophys. Acta 10.1016/j.bbagen.2014.02.004
13. Rifkin, D. B. (2005) Latent transforming growth factor-β (TGF-β) binding proteins: orchestrators of TGF-β availability. J. Biol. Chem. 280, 7409-7412
14. Ponta, H., Sherman, L., and Herrlich, P. A. (2003) CD44: from adhesion molecules to signalling regulators. Nat. Rev. Mol. Cell Biol. 4, 33-45 (Pubitemid 36077255)
15. Toole, B. P. (2009) Hyaluronan-CD44 interactions in cancer: paradoxes and possibilities. Clin. Cancer Res. 15, 7462-7468
16. Bourguignon, L. Y. (2008) Hyaluronan-mediated CD44 activation of RhoGTPase signaling and cytoskeleton function promotes tumor progression. Semin. Cancer Biol. 18, 251-259
17. Skandalis, S. S., Kozlova, I., Engström, U., Hellman, U., and Heldin, P. (2010) Proteomic identification of CD44 interacting proteins. IUBMB Life 62, 833-840
18. Morrison, H., Sherman, L. S., Legg, J., Banine, F., Isacke, C., Haipek, C. A., Gutmann, D. H., Ponta, H., and Herrlich, P. (2001) The NF2 tumor suppressor gene product, merlin, mediates contact inhibition of growth through interactions with CD44. Genes Dev. 15, 968-980 (Pubitemid 32323547)
19. Lee, J. L., Wang, M. J., and Chen, J. Y. (2009) Acetylation and activation of STAT3 mediated by nuclear translocation of CD44. J. Cell Biol. 185, 949-957
20. Ghatak, S., Misra, S., and Toole, B. P. (2005) Hyaluronan constitutively regulates ErbB2 phosphorylation and signaling complex formation in carcinoma cells. J. Biol. Chem. 280, 8875-8883 (Pubitemid 40409577)
21. Kim, Y., Lee, Y. S., Choe, J., Lee, H., Kim, Y. M., and Jeoung, D. (2008) CD44-epidermal growth factor receptor interaction mediates hyaluronic acid-promoted cell motility by activating protein kinase C signaling involving Akt, Rac1, Phox, reactive oxygen species, focal adhesion kinase, and MMP-2. J. Biol. Chem. 283, 22513-22528
22. Li, L., Heldin, C. H., and Heldin, P. (2006) Inhibition of platelet-derived growth factor-BB-induced receptor activation and fibroblast migration by hyaluronan activation of CD44. J. Biol. Chem. 281, 26512-26519 (Pubitemid 44401860)
23. Bourguignon, L. Y., Singleton, P. A., Zhu, H., and Zhou, B. (2002) Hyaluronan promotes signaling interaction between CD44 and the transforming growth factor β receptor I in metastatic breast tumor cells. J. Biol. Chem. 277, 39703-39712 (Pubitemid 35190953)
24. Ito, T., Williams, J. D., Fraser, D., and Phillips, A. O. (2004) Hyaluronan attenuates transforming growth factor-β1-mediated signaling in renal proximal tubular epithelial cells. Am. J. Pathol. 164, 1979-1988 (Pubitemid 38669347)
25. Orian-Rousseau, V., Chen, L., Sleeman, J. P., Herrlich, P., and Ponta, H. (2002) CD44 is required for two consecutive steps in HGF/c-Met signaling. Genes Dev. 16, 3074-3086 (Pubitemid 35424194)
26. Wakahara, K., Kobayashi, H., Yagyu, T., Matsuzaki, H., Kondo, T., Kurita, N., Sekino, H., Inagaki, K., Suzuki, M., Kanayama, N., and Terao, T. (2005) Bikunin down-regulates heterodimerization between CD44 and growth factor receptors and subsequently suppresses agonist-mediated signaling. J. Cell. Biochem. 94, 995-1009 (Pubitemid 41420259)
27. Yu, Q., and Stamenkovic, I. (1999) Localization of matrix metalloproteinase 9 to the cell surface provides a mechanism for CD44-mediated tumor invasion. Genes Dev. 13, 35-48 (Pubitemid 29045114)
28. Yu, Q., and Stamenkovic, I. (2000) Cell surface-localized matrix metalloproteinase-9 proteolytically activates TGF-β and promotes tumor invasion and angiogenesis. Genes Dev. 14, 163-176 (Pubitemid 30070982)
29. Yu, Q., and Stamenkovic, I. (2004) Transforming growth factor-β facilitates breast carcinoma metastasis by promoting tumor cell survival. Clin. Exp. Metastasis 21, 235-242 (Pubitemid 39158500)
30. Battegay, E. J., Raines, E. W., Seifert, R. A., Bowen-Pope, D. F., and Ross, R. (1990) TGF-β induces bimodal proliferation of connective tissue cells via complex control of an autocrine PDGF loop. Cell 63, 515-524
31. Seymour, L., Dajee, D., and Bezwoda, W. R. (1993) Tissue platelet derived-growth factor (PDGF) predicts for shortened survival and treatment failure in advanced breast cancer. Breast Cancer Res. Treat. 26, 247-252 (Pubitemid 23304240)
32. Jechlinger, M., Grunert, S., Tamir, I. H., Janda, E., Lüdemann, S., Waerner, T., Seither, P., Weith, A., Beug, H., and Kraut, N. (2003) Expression profiling of epithelial plasticity in tumor progression. Oncogene 22, 7155-7169 (Pubitemid 37378548)
33. Steller, E. J., Raats, D. A., Koster, J., Rutten, B., Govaert, K. M., Emmink, B. L., Snoeren, N., van Hooff, S. R., Holstege, F. C., Maas, C., Borel Rinkes, I. H., and Kranenburg, O. (2013) PDGFRB promotes liver metastasis formation of mesenchymal-like colorectal tumor cells. Neoplasia 15, 204-217
34. Jechlinger, M., Sommer, A., Moriggl, R., Seither, P., Kraut, N., Capodiecci, P., Donovan, M., Cordon-Cardo, C., Beug, H., and Grünert, S. (2006) Autocrine PDGFR signaling promotes mammary cancer metastasis. J. Clin. Invest. 116, 1561-1570
35. Gotzmann, J., Fischer, A. N., Zojer, M., Mikula, M., Proell, V., Huber, H., Jechlinger, M., Waerner, T., Weith, A., Beug, H., and Mikulits, W. (2006) A crucial function of PDGF in TGF-β-mediated cancer progression of hepatocytes. Oncogene 25, 3170-3185 (Pubitemid 43881558)
36. Ito, T., Williams, J. D., Fraser, D. J., and Phillips, A. O. (2004) Hyaluronan regulates transforming growth factor-β1 receptor compartmentalization. J. Biol. Chem. 279, 25326-25332 (Pubitemid 38756787)
37. Kovalenko, M., Denner, K., Sandström, J., Persson, C., Gross, S., Jandt, E., Vilella, R., Böhmer, F., and Ostman, A. (2000) Site-selective dephosphorylation of the platelet-derived growth factor β-receptor by the receptor-like protein-tyrosine phosphatase DEP-1. J. Biol. Chem. 275, 16219-16226 (Pubitemid 30366934)
38. Lammich, S., Okochi, M., Takeda, M., Kaether, C., Capell, A., Zimmer, A. K., Edbauer, D., Walter, J., Steiner, H., and Haass, C. (2002) Presenilin-dependent intramembrane proteolysis of CD44 leads to the liberation of its intracellular domain and the secretion of an Aβ-like peptide. J. Biol. Chem. 277, 44754-44759 (Pubitemid 36159067)
39. Yao, D., Ehrlich, M., Henis, Y. I., and Leof, E. B. (2002) Transforming growth factor-β receptors interact with AP2 by direct binding to β2 subunit. Mol. Biol. Cell 13, 4001-4012 (Pubitemid 35398566)
40. Franzén, P., ten Dijke, P., Ichijo, H., Yamashita, H., Schulz, P., Heldin, C. H., and Miyazono, K. (1993) Cloning of a TGF β type I receptor that forms a heteromeric complex with the TGF β type II receptor. Cell 75, 681-692
41. Hahn, W. C., Counter, C. M., Lundberg, A. S., Beijersbergen, R. L., Brooks, M. W., and Weinberg, R. A. (1999) Creation of human tumour cells with defined genetic elements. Nature 400, 464-468 (Pubitemid 29361801)
42. Jalkanen, S., Bargatze, R. F., de los Toyos, J., and Butcher, E. C. (1987) Lymphocyte recognition of high endothelium: antibodies to distinct epitopes of an 85-95 kDa glycoprotein antigen differentially inhibit lymphocyte binding to lymph node, mucosal, or synovial endothelial cells. J. Cell Biol. 105, 983-990 (Pubitemid 18043858)
43. Karlsson, S., Kowanetz, K., Sandin, A., Persson, C., Ostman, A., Heldin, C. H., and Hellberg, C. (2006) Loss of T-cell protein tyrosine phosphatase induces recycling of the platelet-derived growth factor (PDGF) β-receptor but not the PDGFα-receptor. Mol. Biol. Cell 17, 4846-4855 (Pubitemid 44665753)
44. Piek, E., Moustakas, A., Kurisaki, A., Heldin, C. H., and ten Dijke, P. (1999) TGF-(β) type I receptor/ALK-5 and Smad proteins mediate epithelial to mesenchymal transdifferentiation in NMuMG breast epithelial cells. J. Cell Sci. 112, 4557-4568 (Pubitemid 30034805)
45. Turkson, J., Bowman, T., Garcia, R., Caldenhoven, E., De Groot, R. P., and Jove, R. (1998) Stat3 activation by Src induces specific gene regulation and is required for cell transformation. Mol. Cell. Biol. 18, 2545-2552 (Pubitemid 28183424)
46. Jarvius, M., Paulsson, J., Weibrecht, I., Leuchowius, K. J., Andersson, A.-C., Wählby, C., Gullberg, M., Botling, J., Sjöblom, T., Markova, B., Ostman, A., Landegren, U., and Söderberg, O. (2007) In situ detection of phosphorylated PDGF receptor β using a generalized proximity ligation method. Mol. Cell Proteomics 6, 1500-1509 (Pubitemid 47506163)
47. Söderberg, O., Gullberg, M., Jarvius, M., Ridderstråle, K., Leuchowius, K. J., Jarvius, J., Wester, K., Hydbring, P., Bahram, F., Larsson, L. G., and Landegren, U. (2006) Direct observation of individual endogenous protein complexes in situ by proximity ligation. Nat. Methods 3, 995-1000 (Pubitemid 44782698)
48. Bruna, A., Darken, R. S., Rojo, F., Ocaña, A., Peñuelas, S., Arias, A., Paris, R., Tortosa, A., Mora, J., Baselga, J., and Seoane, J. (2007) High TGFβ-Smad activity confers poor prognosis in glioma patients and promotes cell proliferation depending on the methylation of the PDGF-B gene. Cancer Cell 11, 147-160 (Pubitemid 46209848)
49. Lyons, R. M., Keski-Oja, J., and Moses, H. L. (1988) Proteolytic activation of latent transforming growth factor-β from fibroblast- conditioned medium. J. Cell Biol. 106, 1659-1665
50. Ludbrook, S. B., Barry, S. T., Delves, C. J., and Horgan, C. M. (2003) The integrin αvβ3 is a receptor for the latency-associated peptides of transforming growth factors β1 and β3. Biochem. J. 369, 311-318 (Pubitemid 36174200)
51. Woodard, A. S., García-Cardeña, G., Leong, M., Madri, J. A., Sessa, W. C., and Languino, L. R. (1998) The synergistic activity of αvβ3 integrin and PDGF receptor increases cell migration. J. Cell Sci. 111, 469-478 (Pubitemid 28098396)
52. Roberts, M., Barry, S., Woods, A., van der Sluijs, P., and Norman, J. (2001) PDGF-regulated rab4-dependent recycling of αvβ3 integrin from early endosomes is necessary for cell adhesion and spreading. Curr. Biol. 11, 1392-1402 (Pubitemid 32863188)
53. Ishigaki, T., Imanaka-Yoshida, K., Shimojo, N., Matsushima, S., Taki, W., and Yoshida, T. (2011) Tenascin-C enhances cross-talk signaling of integrin αvβ3/PDGFR-β complex by SRC recruitment promoting PDGF-induced proliferation and migration in smooth muscle cells. J. Cell Physiol. 226, 2617-2624
54. Ding, Q., Stewart, J., Jr., Olman, M. A., Klobe, M. R., and Gladson, C. L. (2003) The pattern of enhancement of Src kinase activity on platelet-derived growth factor stimulation of glioblastoma cells is affected by the integrin engaged. J. Biol. Chem. 278, 39882-39891 (Pubitemid 37248551)
55. Murray-Rust, J., McDonald, N. Q., Blundell, T. L., Hosang, M., Oefner, C., Winkler, F., and Bradshaw, R. A. (1993) Topological similarities in TGF-β2, PDGF-BB, and NGF define a superfamily of polypeptide growth factors. Structure 1, 153-159
56. Galliher, A. J., and Schiemann, W. P. (2007) Src phosphorylates Tyr284 in TGF-β type II receptor and regulates TGF-β stimulation of p38 MAPK during breast cancer cell proliferation and invasion. Cancer Res. 67, 3752-3758 (Pubitemid 46762161)
57. Galliher, A. J., and Schiemann, W. P. (2006) β3 integrin and Src facilitate transforming growth factor-β-mediated induction of epithelial-mesenchymal transition in mammary epithelial cells. Breast Cancer Res. 8, R42
58. Misra, S., Toole, B. P., and Ghatak, S. (2006) Hyaluronan constitutively regulates activation of multiple receptor tyrosine kinases in epithelial and carcinoma cells. J. Biol. Chem. 281, 34936-34941 *This work was supported in part by grants from the Swedish Cancer Society, the Agnes and Mac Rudberg Foundation, and the Gurli and Edward Brunnberg Foundation. (Pubitemid 46036532)