Hyaluronan-induced masking of ErbB2 and CD44-enhanced trastuzumab internalisation in trastuzumab resistant breast cancer

European Journal of Cancer

Volumn 43, Issue 16, 2007, Pages 2423-2433

  Pályi Krekk, Zsuzsanna ^a   Barok, Márk ^a   Isola, Jorma ^d   Tammi, Markku ^c   Szöllosi, János ^a,b   Nagy, Peter ^a  

^a UNIVERSITY OF DEBRECEN   (Hungary)

^b UNIVERSITY OF DEBRECEN   (Hungary)

^c UNIVERSITY OF EASTERN FINLAND   (Finland)

^d TAMPERE UNIVERSITY HOSPITAL   (Finland)

Author keywords

CD44; ErbB2; Hyaluronan; Masking; Trastuzumab resistance

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR 2; HERMES ANTIGEN; HYALURONIC ACID; MUCIN 4; TRASTUZUMAB;

ARTICLE; BREAST CANCER; CELL PROLIFERATION; CONTROLLED STUDY; CYTOTOXICITY; DRUG EFFECT; HUMAN; HUMAN CELL; IN VITRO STUDY; PRIORITY JOURNAL;

ANTIBODIES, MONOCLONAL; ANTIGENS, CD44; ANTINEOPLASTIC AGENTS; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL PROLIFERATION; DOWN-REGULATION; DRUG RESISTANCE, NEOPLASM; FEMALE; HUMANS; HYALURONIC ACID; RECEPTOR, ERBB-2;

EID: 35448969823     PISSN: 09598049     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ejca.2007.08.018     Document Type: Article

References (49)

1. Ross J.S., Fletcher J.A., Linette G.P., et al. The Her-2/neu gene and protein in breast cancer 2003: biomarker and target of therapy. Oncologist 8 (2003) 307-325
2. Citri A., and Yarden Y. EGF-ERBB signalling: towards the systems level. Nat Rev Mol Cell Biol 7 (2006) 505-516
3. Mocanu M.M., Fazekas Z., Petrás M., et al. Associations of ErbB2, beta1-integrin and lipid rafts on Herceptin (Trastuzumab) resistant and sensitive tumor cell lines. Cancer Lett 227 (2005) 201-212
4. Nagy P., Friedländer E., Tanner M., et al. Decreased accessibility and lack of activation of ErbB2 in JIMT-1, a Herceptin-resistant, MUC4-expressing breast cancer cell line. Cancer Res 65 (2005) 473-482
5. Bourguignon L.Y., Zhu H., Chu A., Iida N., Zhang L., and Hung M.C. Interaction between the adhesion receptor, CD44, and the oncogene product, p185HER2, promotes human ovarian tumor cell activation. J Biol Chem 272 (1997) 27913-27918
6. Bourguignon L.Y. CD44-mediated oncogenic signaling and cytoskeleton activation during mammary tumor progression. J Mammary Gland Biol Neoplasia 6 (2001) 287-297
7. Carraway K.L., Ramsauer V.P., and Carraway C.A. Glycoprotein contributions to mammary gland and mammary tumor structure and function: roles of adherens junctions, ErbBs and membrane MUCs. J Cell Biochem 96 (2005) 914-926
8. Holbro T., Civenni G., and Hynes N.E. The ErbB receptors and their role in cancer progression. Exp Cell Res 284 (2003) 99-110
9. Naor D., Sionov R.V., and Ish-Shalom D. CD44: structure, function, and association with the malignant process. Adv Cancer Res 71 (1997) 241-319
10. Bourguignon L.Y., Zhu H., Zhou B., Diedrich F., Singleton P.A., and Hung M.C. Hyaluronan promotes CD44v3-Vav2 interaction with Grb2-p185(HER2) and induces Rac1 and Ras signaling during ovarian tumor cell migration and growth. J Biol Chem 276 (2001) 48679-48692
11. Ghatak S., Misra S., and Toole B.P. Hyaluronan constitutively regulates ErbB2 phosphorylation and signaling complex formation in carcinoma cells. J Biol Chem 280 (2005) 8875-8883
12. Misra S., Toole B.P., and Ghatak S. Hyaluronan constitutively regulates activation of multiple receptor tyrosine kinases in epithelial and carcinoma cells. J Biol Chem 281 (2006) 34936-34941
13. Ghatak S., Misra S., and Toole B.P. Hyaluronan oligosaccharides inhibit anchorage-independent growth of tumor cells by suppressing the phosphoinositide 3-kinase/Akt cell survival pathway. J Biol Chem 277 (2002) 38013-38020
14. Marhaba R., and Zoller M. CD44 in cancer progression: adhesion, migration and growth regulation. J Mol Histol 35 (2004) 211-231
15. Auvinen P., Tammi R., Tammi M., Johansson R., and Kosma V.M. Expression of CD44s, CD44v3 and CD44v6 in benign and malignant breast lesions: correlation and colocalization with hyaluronan. Histopathology 47 (2005) 420-428
16. Lopez J.I., Camenisch T.D., Stevens M.V., Sands B.J., McDonald J., and Schroeder J.A. CD44 attenuates metastatic invasion during breast cancer progression. Cancer Res 65 (2005) 6755-6763
17. Auvinen P., Tammi R., Parkkinen J., et al. Hyaluronan in peritumoral stroma and malignant cells associates with breast cancer spreading and predicts survival. Am J Pathol 156 (2000) 529-536
18. Simpson M.A., Wilson C.M., and McCarthy J.B. Inhibition of prostate tumor cell hyaluronan synthesis impairs subcutaneous growth and vascularization in immunocompromised mice. Am J Pathol 161 (2002) 849-857
19. Peterson R.M., Yu Q., Stamenkovic I., and Toole B.P. Perturbation of hyaluronan interactions by soluble CD44 inhibits growth of murine mammary carcinoma cells in ascites. Am J Pathol 156 (2000) 2159-2167
20. Camenisch T.D., Schroeder J.A., Bradley J., Klewer S.E., and McDonald J.A. Heart-valve mesenchyme formation is dependent on hyaluronan-augmented activation of ErbB2-ErbB3 receptors. Nat Med 8 (2002) 850-855
21. Slamon D.J., Leyland-Jones B., Shak S., et al. Use of chemotherapy plus a monoclonal antibody against HER2 for metastatic breast cancer that overexpresses HER2. N Engl J Med 344 (2001) 783-792
22. Tokunaga E., Oki E., Nishida K., et al. Trastuzumab and breast cancer: developments and current status. Int J Clin Oncol 11 (2006) 199-208
23. Cardoso F., Piccart M.J., Durbecq V., and Di L.A. Resistance to trastuzumab: a necessary evil or a temporary challenge?. Clin Breast Cancer 3 (2002) 247-257
24. Nahta R., and Esteva F.J. Herceptin: mechanisms of action and resistance. Cancer Lett 232 (2006) 123-138
25. Clynes R.A., Towers T.L., Presta L.G., and Ravetch J.V. Inhibitory Fc receptors modulate in vivo cytoxicity against tumor targets. Nat Med 6 (2000) 443-446
26. Barok M., Isola J., Pályi-Krekk Z., et al. Trastuzumab causes ADCC-mediated growth inhibition of submacroscopic JIMT-1 breast cancer xenografts despite intrinsic drug resistance. Mol Cancer Ther 6 (2007) 2065-2072
27. Motoyama A.B., Hynes N.E., and Lane H.A. The efficacy of ErbB receptor-targeted anticancer therapeutics is influenced by the availability of epidermal growth factor-related peptides. Cancer Res 62 (2002) 3151-3158
28. Nagata Y., Lan K.H., Zhou X., et al. PTEN activation contributes to tumor inhibition by trastuzumab, and loss of PTEN predicts trastuzumab resistance in patients. Cancer Cell 6 (2004) 117-127
29. Kono K., Takahashi A., Ichihara F., Sugai H., Fujii H., and Matsumoto Y. Impaired antibody-dependent cellular cytotoxicity mediated by herceptin in patients with gastric cancer. Cancer Res 62 (2002) 5813-5817
30. Tanner M., Kapanen A.I., Junttila T., et al. Characterization of a novel cell line established from a patient with Herceptin-resistant breast cancer. Mol Cancer Ther 3 (2004) 1585-1592
31. Nakazawa H., Yoshihara S., Kudo D., et al. 4-methylumbelliferone, a hyaluronan synthase suppressor, enhances the anticancer activity of gemcitabine in human pancreatic cancer cells. Cancer Chemother Pharmacol 57 (2006) 165-170
32. Toole B.P. Hyaluronan: from extracellular glue to pericellular cue. Nat Rev Cancer 4 (2004) 528-539
33. Yoshihara S., Kon A., Kudo D., et al. A hyaluronan synthase suppressor, 4-methylumbelliferone, inhibits liver metastasis of melanoma cells. FEBS Lett 579 (2005) 2722-2726
34. Tammi R., Ripellino J.A., Margolis R.U., and Tammi M. Localization of epidermal hyaluronic acid using the hyaluronate binding region of cartilage proteoglycan as a specific probe. J Invest Dermatol 90 (1988) 412-414
35. Gonzalez R.C., Woods R.E., and Eddins S.L. Segmentation using the watershed transform. Digital image processing using Matlab (2004), Pearson Prentice Hall 417-425
36. Sebestyén Z., Nagy P., Horváth G., et al. Long wavelength fluorophores and cell-by-cell correction for autofluorescence significantly improves the accuracy of flow cytometric energy transfer measurements on a dual-laser benchtop flow cytometer. Cytometry 48 (2002) 124-135
37. Szentesi G., Horváth G., Bori I., et al. Computer program for determining fluorescence resonance energy transfer efficiency from flow cytometric data on a cell-by-cell basis. Computer Methods and Programs in Biomedicine 75 (2004) 201-211
38. Horváth G., Petrás M., Szentesi G., et al. Selecting the right fluorophores and flow cytometer for fluorescence resonance energy transfer measurements. Cytometry A 65 (2005) 148-157
39. Nagy P., Arndt-Jovin D.J., and Jovin T.M. Small interfering RNAs suppress the expression of endogenous and GFP-fused epidermal growth factor receptor (erbB1) and induce apoptosis in erbB1-overexpressing cells. Exp Cell Res 285 (2003) 39-49
40. Szöllo{combining double acute accent}si J., Trón L., Damjanovich S., Helliwell S.H., Arndt Jovin D., and Jovin T.M. Fluorescence energy transfer measurements on cell surfaces: a critical comparison of steady-state fluorimetric and flow cytometric methods. Cytometry 5 (1984) 210-216
41. Austin C.D., De Maziere A.M., Pisacane P.I., et al. Endocytosis and sorting of ErbB2 and the site of action of cancer therapeutics trastuzumab and geldanamycin. Mol Biol Cell 15 (2004) 5268-5282
42. Nagy P., Vereb G., Sebestyén Z., et al. Lipid rafts and the local density of ErbB proteins influence the biological role of homo- and heteroassociations of ErbB2. J Cell Sci 115 (2002) 4251-4262
43. Knudson W., Chow G., and Knudson C.B. CD44-mediated uptake and degradation of hyaluronan. Matrix Biol 21 (2002) 15-23
44. Nagy P., Bene L., Balázs M., et al. EGF-induced redistribution of erbB2 on breast tumor cells: Flow and image cytometric energy transfer measurements. Cytometry 32 (1998) 120-131
45. Al-Hajj M., Wicha M.S., Benito-Hernandez A., Morrison S.J., and Clarke M.F. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A 100 (2003) 3983-3988
46. Rodriguez-Boulan E., Kreitzer G., and Musch A. Organization of vesicular trafficking in epithelia. Nat Rev Mol Cell Biol 6 (2005) 233-247
47. Bruno R., Washington C.B., Lu J.F., Lieberman G., Banken L., and Klein P. Population pharmacokinetics of trastuzumab in patients with HER2 + metastatic breast cancer. Cancer Chemother Pharmacol 56 (2005) 361-369
48. Toole B.P., Wight T.N., and Tammi M.I. Hyaluronan-cell interactions in cancer and vascular disease. J Biol Chem 277 (2002) 4593-4596
49. Rilla K., Pasonen-Seppanen S., Rieppo J., Tammi M., and Tammi R. The hyaluronan synthesis inhibitor 4-methylumbelliferone prevents keratinocyte activation and epidermal hyperproliferation induced by epidermal growth factor. J Invest Dermatol 123 (2004) 708-714