Coexpression of CD44 variant (v10/ex14) and CD44S in human mammary epithelial cells promotes tumorigenesis

Journal of Cellular Physiology

Volumn 171, Issue 2, 1997, Pages 152-160

  Iida, Naoko ^a   Bourguignon, Lilly Y W ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENIC FACTOR; CELL ADHESION MOLECULE; CELL SURFACE RECEPTOR; HERMES ANTIGEN; HYALURONIC ACID;

ANIMAL MODEL; ANTIGEN EXPRESSION; ARTICLE; BREAST CANCER; BREAST EPITHELIUM; CARCINOGENESIS; CELL ADHESION; CELL MIGRATION; CONTROLLED STUDY; FEMALE; GENE TRANSFER; HUMAN; HUMAN CELL; METASTASIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN VARIANT;

ANGIOGENESIS INDUCING AGENTS; ANIMALS; ANTIGENS, CD44; BREAST; CARCINOGENICITY TESTS; CELL ADHESION; CELL TRANSFORMATION, NEOPLASTIC; CELLS, CULTURED; CHROMOSOME MAPPING; CLONING, MOLECULAR; DNA, COMPLEMENTARY; EPITHELIAL CELLS; EPITHELIUM; EXONS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; HYALURONIC ACID; IMMUNOHISTOCHEMISTRY; ISOMERISM; MICE; MICE, NUDE; NEOPLASM INVASIVENESS; TRANSFECTION;

EID: 0030927534     PISSN: 00219541     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4652(199705)171:2<152::AID-JCP5>3.0.CO;2-N     Document Type: Article

References (71)

1. Aruffo, A., Stamenkovic, I., Melnick, M., Underhill, C.B., and Seed, B. (1990) CD44 is the principle cell surface receptor for hyaluronate. Cell, 61:1303-1313.
2. Bertrand, P., Girard, N., Delpech, B., Duval, C., D'Anjou, J., and Dauce, J.P. (1992) Hyaluronan (hyaluronic acid) and hyaluronectin in the extracellular matrix of human breast carcinomas: Comparison between invasive and non-invasive areas. Int. J. Cancer, 52:1-6.
3. Bourguignon, L.Y.W. (1996) Interaction between the membrane-cytoskeleton and CD44 during lymphocyte signal transduction and cell adhesion. In: Current Topics In Membranes: The Plasma Membrane-Cytoskeleton Interface: Template for Protein Domains, Vesicle Trafficking, and Signal Transduction. W.J. Nelson, ed. 43:293-312.
4. Bourguignon, L.Y.W., Kalomiris, E.L., and Lokeshwar, V.B. (1991) Acylation of the lymphoma transmembrane glycoprotein, GP85, may be required for GP85-ankyrin interaction. J. Biol. Chem., 266:11761-11765.
5. Bourguignon, L.Y.W., Lokeshwar, V.B., He, X., Chen, X., and Bourguignon, G.J. (1992) A CD44-like endothelial cell transmembrane glycoprotein (GP116) interacts with extracellular matrix and ankyrin. Mol. Cell Biol., 12:4464-4471.
6. Bourguignon, L.Y.W., Lokeshwar, V.B., Chen, X., and Kerrick, W.G.L. (1993) Hyaluronic acid (HA)-induced lymphocyte signal transduction and HA receptor (GP85/CD44)-cytoskeleton interaction. J. Immunol., 151:6634-6644.
7. Bourguignon, L.Y.W., Iida, N., Welsh, C.F., Zhu, D., Krongrad, A., and Pasquale, D. (1995) Involvement of CD44 and its variant isoforms in membrane-cytoskeleton interaction, cell adhesion and tumor metastasis. J. Neurooncol., 26:201-208.
8. Brackman, D., Trydal, T., Lillehaug, J.R., and Aarskog, D. (1992) Reorganization of the cytoskeleton and morphological changes induced by 1,25-dihydroxyvitamin D3 in C3H/10T/2 mouse embryo fibroblasts: Relation to inhibition of proliferation. Exp. Cell Res., 201:485-493.
9. Brown, T.A., Bouchard, T., St. John, T., Wayner, E., and Carter, W.G. (1991) Human keratinocytes express a new CD44 core protein (CD44E) as a heparin-sulfate intrinsic membrane proteoglycan with additional exons. J. Cell Biol., 113:207-221.
10. Carter, W.G., and Wayner, E.A. (1988) Characterization of the class III collagen receptor, a phosphorylated transmembrane glycoprotein expressed in nucleated human cells. J. Biol. Chem., 263:4193-4201.
11. Chaitin, M.H., Wortham, H.S., and Grun-Zinkernagel, A.M. (1994) Immunocytochemical localization of CD44 in the mouse retina. Exp. Eye Res., 58:359-365.
12. Culty, M., Miyake, K., Kincade, P.W., Silorski, E., Butcher, E.C., and Underhill, C.B. (1990) The hyaluronate receptor is a member of the CD44 (H-CAM) family of cell surface glycoproteins. J. Cell Biol., 111:2765-2774.
13. Culty, M., Shizari, M., Thompson, E.W., and Underhill, C.B. (1994) Binding and degradation of hyaluronan by human breast cancer cell lines expressing different forms of CD44: Correlation with invasive potential. J. Cell. Physiol., 160:275-286.
14. Dall, P., Heider, K.-H., Sinn, H.-P., Skroch-Angel, P., Adolf, G., Kaufmann, M., Herrlich, P., and Ponta, H. (1995) Comparison of immunotostochemistry and RT-PCR for detection of CD44v-expression, a new prognostic factor in human breast cancer. Int. J. Cancer, 60:471-477.
15. de la Tore, M., Wells, A.F., Bergh, J., and Lindgren, A. (1993) Localization of hyaluronan in normal breast tissue, radical scar, and tubular breast carcinoma. Hum. Pathol., 24:1294-1297.
16. Dougherty, G.J., Lansdorp, P.M., Cooper, D.L., and Humphries, R.K. (1991) Molecular cloning of CD44R1 and CD44R2, two novel isoforms of the human CD44 lymphocyte "homing" receptor expressed by hemopoietic cells. J. Exp. Med., 174:1-5.
17. Droll, A., Doughery, S.T., Chiu, R.D., Dirks, J.F., Mcbride, W.H., Cooper, D.L., and Dougherty, G.J. (1995) Adhesive interactions between alternatively spliced CD44 isoforms. J. Biol. Chem., 270:11567-11573.
18. Dvorak, H.F., Brown, L.F., Detmar, M., and Dvorak, A.M. (1995) Review: Vascular permeability factor/vascular endothelial growth factor, microvascular hyperpermeability, and angiogenesis. Am. J. Pathol., 146:1029-1039.
19. Folkman, J. (1985) Tumor angiogenesis. Adv. Cancer Res., 43:175-203.
20. Folkman, J., and Klagsbrun, M. (1987) Angiogenic factors. Science, 235:442-447.
21. Friedrichs, K., Franke, F., Lisboa, B.-W., Kugler, G., Gille, I., Terpe, H.-J., Holzel, F., Maass, H., and Gunthert, U. (1995) CD44 isoforms correlate with cellular differentiation but not with prognosis in human breast cancer. Cancer Res., 55:5424-5433.
22. Gaffney, E.V. (1982) A cell line (HBL100) established from human breast milk. Cell Tissue Res., 227:563-568.
23. Green, S.J., Tarone, G., and Underhill, C.B. (1988) Aggregation of macrophages and fibroblasts is inhibited by a monoclonal antibody to the hyaluronate receptor. Exp. Cell Res., 178:224-232.
24. Gunthert, U. (1993) CD44: A multitude of isoforms with diverse functions. Curr. Top. Microbiol. Immunol., 184:47-64.
25. Gunthert, U., Hoffman, M., Rudy, W., Reber, S., Zoller, M., Haubmann, I., Matzku, S., Wenzel, A., Ponta, H., and Herrlich, P. (1993) A new variant of glycoprotein CD44 confers metastatic potential to rat carcinoma cells. Cell, 65:13-24.
26. Haggerty, J.G., Bretton, R.H., and Milstone, L.M. (1992) Identification and characterization of a cell surface proteoglycan on keratinocytes. J. Invest. Dermatol., 99:374-380.
27. Haynes, B.F., Telen, M.J., Hale, L.P., and Denning, S.M. (1989) CD44-a molecule involved in leukocyte adherence and T-cell activation. Immunol. Today, 10:423-428.
28. He, Q., Lesley, J., Hyman, R., Ishihara, K., and Kincade, P.W. (1992) Molecular isoforms of murine CD44 and evidence that the membrane proximal domain is not critical for hyaluronate recognition. J. Cell. Biol., 119:1711-1719.
29. Herrlich, P., Zollar, M., Pals, S.T., and Ponta, H. (1993) CD44 splice variants: Metastases meet lymphocytes. Immunol. Today, 14:395-399.
30. Iida, N., and Bourguignon, L.Y.W. (1995) New CD44 splice variants associated with human breast cancers. J. Cell. Physiol., 162:127-133.
31. Jackson, D.G., Bell, J.I., Dickinson, R., Timans, J., Shields, J., and Whittle, N. (1995) Proteoglycan forms of the lymphocyte homing receptor CD44 are alternatively spliced variants containing the v3 exon. J. Cell Biol., 128:673-685.
32. Jalkanen, S.P., and Jalkanen, M. (1992) Lymphocyte CD44 binds the COOH-terminal heparin-binding domain of fibronectin. J. Cell Biol., 116:817-825.
33. Joensuu, H., Klemi, P.J., Toikkane, S., and Jalkanen, S. (1993) Glycoprotein CD44 expression and its association with survival in breast cancer. Am. J. Pathol., 143:867-874.
34. Kalomiris, E.L., and Bourguignon, L.Y.W. (1988) Mouse T-lymphoma cells contain a transmembrane glycoprotein (GP85) which binds ankyrin. J. Cell Biol., 106:319-327.
35. Kalomiris, E.L., and Bourguignon, L.Y.W. (1989) Lymphoma protein kinase C is associated with the transmembrane glycoprotein, GP85, and may function in GP85-ankyrin binding. J. Biol. Chem., 264:8113-8119.
36. Kaufmann, M., Meider, K.-H., Sinn, H.-P., von Minckwitz, G., Ponta, H., and Herrlich, P. (1995) CD44 variant exon epitopes in primary breast cancer and length of survival. Lancet, 345:615-619.
37. Kock, A.E., Polverini, P.J., Kunkel, S.L., Harlow, L.A., DiPietro, L.A., Elner, V.M., Elner, S.G., and Strieter, R.M. (1992) Interleukin-8 as a macrophage-derived mediator of angiogenesis. Science, 258:1798-1801.
38. Lesley, J., Hyman, R., and Kincade, P.W. (1993) CD44 and its interaction with extracellular matrix. Adv. Immunol., 54:271-335.
39. Liao, H.X., Lee, D.M., and Haynes, B.F. (1995) N-terminal and central regions of the human CD44 extracellular domain participated in cell surface hyaluronan binding. J. Immunol., 155:3938-3945.
40. Liotta, L.A., Steeg, P.S., and Stetler-Stevenson, W.G. (1991) Cancer metastasis and angiogenesis: An imbalance of positive and negative regulation. Cell, 64:327-336.
41. Lokeshwar, V.B., and Bourguignon, L.Y.W. (1991) Post-translational protein modification and expression of ankyrin-binding site(s) in GP85 and its biosynthetic precursors during T-lymphoma membrane biosyntheses. J. Biol. Chem., 266:17983-17989.
42. Lokeshwar, V.B., and Bourguignon, L.Y.W. (1992) The lymphoma glycoprotein GP85 (CD44) is a novel G-protein which regulates GP85 (CD44)-ankyrin interaction. J. Biol. Chem., 267:22073-22078.
43. Lokeshwar, V.B., Fregien, N., and Bourguignon, L.Y.W. (1994) Ankyrin binding domain of CD44 (GP85) is required for the expression of hyaluronic acid-mediated adhesion function. J. Cell Biol., 126:1099-1109.
44. Lokeshwar, V.B., Iida, N., and Bourguignon, L.Y.W. (1996) The cell adhesion molecule, GP116, is a new CD44 variant (ex14/v10) involved in hyaluronic acid binding and endothelial cell proliferation. J. Biol. Chem., 271:23853-23864.
45. Matsumura, Y., and Tarin, D. (1992) Significance of CD44 gene products for cancer diagnosis and disease evaluation. Lancet, 340:1053-1058.
46. Miyake, K., and Kincade, P.W. (1990a) A new cell adhesion mechanism involving hyaluronate and CD44. Curr. Top. Microbiol. Immunol., 166:87-90.
47. Miyake, K., Underhill, C.B., Lesley, J., and Kincade, P.W. (1990b) Hyaluronate can function as a cell adhesion molecule and CD44 participates in hyaluronate recognition. J. Exp. Med., 172:69-75.
48. Monsky, W.L., Kelly, T., Lin, C.-Y., Yeh, Y., Stetler-Stevenson, W.G., Mueller, S.C., and Chen, W.-T. (1993) Binding and localization of Mr 72,000 matrix metalloproteinase at cell surface invadopodia. Cancer Res., 53:3159-3164.
49. Morrison, M. (1980) Lactoperoxidase-catalyzed iodination as a tool for investigation of proteins. Methods Enzymol., 70:214-220.
50. Mulder, J.-W.R., Kruyt, P., Sewnath, M., Oosting, J., Seldenrijk, C.A., Weidema, W.F., Offerhaus, J., and Pals, S.T. (1994) Colorectal cancer prognosis and expression of exon-v6-containing CD44 proteins. Lancet, 344:1470-1472.
51. Naujokas, M.F., Morin, M., Anderson, M.S., Peterson, M., and Miller, J. (1993) The chondroitin sulfate form of invariant chain can enhance stimulation of T cell responses through interaction with CD44. Cell, 74:257-268.
52. Nuovo, G.J. (1994) RT in situ PCR with direct incorporation of digoxigenin-11-dUTP: Protocol and applications. Biochemica, 11:4-6.
53. Peach, R.J., Hollenbaugh, D., Stamenkovic, I., and Aruffo, A. (1993) Identification of hyaluronic acid binding sites in the extracellular domain of CD44. J. Cell Biol., 122:257-264.
54. Picker, L.J., Nakache, M., and Butcher, E.C. (1989) Monoclonal antibodies to human lymphocyte homing receptors define a novel class of adhesion molecules on diverse cell type. J. Cell Biol. 109:927-937.
55. Rodriguez, C., Monges, G., Rouanet, P., Dutrillaux, B., Lefrancois, D., and Theillet, C. (1995) CD44 expression patterns in breast and colon tumors: A PCR-based study of splice variants. Int. J. Cancer, 64:347-354.
56. Rooney, P., Kumar, S., Ponting, J., and Wang, M. (1995) The role of hyaluronan in tumor neovascularization. Int. J. Cancer, 60:632-636.
57. Salmi, M., Gron-Virta, K., Sointu, P., Grenman, R., Kalimo, H., and Jalkanen, S. (1993) Regulated expression of exon v6 containing isoforms of CD44 in man: Downregulation during malignant transformation of tumors of squamocellular origin. J. Cell Biol., 122:431-442.
58. Satterwhite, L.L., and Pollard, T.D. (1992) Cytokinesis. Curr. Opin. Cell. Biol., 4:43-52.
59. Screaton, G.R., Bell, M.V., Jackson, D.G., Cornelis, F.B., Gerth, U., and Bell, J.I. (1992) Genomic structure of DNA coding the lymphocyte homing receptor CD44 reveals at least 12 alternative spliced exons. Proc. Natl. Acad. Sci. U.S.A., 89:12160-12164.
60. Stauder, R., Eisterer, W., Thaler, J., and Gunthert, U. (1995) CD44 variant isoforms in non-Hodgkin's lymphoma: A new independent prognostic factor. Blood, 85:2885-2899.
61. Stamenkovic, I., Amiot, M., Pesando, J.M., and Seed, B. (1991) The hemopoietic and epithelial forms of CD44 are distinct polypeptides with different adhesion potentials for hyalurononan-bearing cells. EMBO J., 10:343-347.
62. Strieter, R.M., Polverini, P.J., Arenberg, D.A., Walz, A., Opdenakker, G., Van Damme, J., and Kunkel, S.L. (1995) Role of C-X-C chemokines as regulators of angiogenesis in lung cancer. J. Leukoc. Biol., 57:752-762.
63. Tanabe, K.K., Ellis, L.M., and Saya, H. (1993) Expression of CD44R1 adhesion molecule in colon carcinoma and metastases. Lancet, 341:725-726.
64. Toyama-Sorimachi, N., Sorimachi, H., Tobita, Y., Kitamura, F., Yagita, H., Suzuki, K., and Miyasaka, M. (1995) A novel ligand for CD44 is serglycin, a hematopoietic cell lineage-specific proteoglycan. J. Biol. Chem., 270:7437-7444.
65. Trifaro, J.-M., and Vitale, M.L. (1993) Cytoskeleton dynamics during neurotransmitter release. Trends Neurosci., 16:466-472.
66. Turley, E.A., Austen, L., Vandeligt, K., and Clary, C. (1991) Hyaluronan and a cell-associated hyaluronan binding protein regulate the locomotion of ras-transformed cells. J. Cell Biol., 112:1041-1047.
67. van der Voort, R., Manten-Horst, E., Smit, L., Ostermann, E., van den Gerg, F., and Pals, S.T. (1995) Binding of cell-surface expressed CD44 to hyaluronate is dependent on splicing and cell type. Biochem. Biophys. Res. Commun., 214:137-144.
68. Wayner, E.A., and Carter, W.G. (1982) Transformation-dependent alterations is glycoproteins of extracellular matrix of human fibroblasts. Characterization of GP250 and the collagen-like GP140. J. Biol. Chem., 257:13805-13015.
69. West, D.C., and Kumar, S. (1989) The effect of hyaluronate and its oligosaccharides on endothelial cell proliferation and monolayer integrity. Exp. Cell Res., 183:179-196.
70. Yang, B., Yang, B.L., Savani, R.C., and Turley, E.A. (1994) Identification of a common hyaluronan binding motif in the hyaluronan binding proteins RHAMM. CD44, and link protein. EMBO J., 13:286-296.
71. neu-transfected NIH3T3 cells promotes an up-regulation of hyaluronic acid-mediated membrane-cytoskeleton interaction and cell adhesion. Oncogene, 12:2309-2314.