Bikunin down-regulates heterodimerization between CD44 and growth factor receptors and subsequently suppresses agonist-mediated signaling

Journal of Cellular Biochemistry

Volumn 94, Issue 5, 2005, Pages 995-1009

  Wakahara, Kiyoshi ^a   Kobayashi, Hiroshi ^b   Yagyu, Tatsuo ^a   Matsuzaki, Hidenori ^a   Kondo, Toshiharu ^c   Kurita, Noriyuki ^d   Sekino, Hideo ^d   Inagaki, Kiyokazu ^a   Suzuki, Mika ^b   Kanayama, Naohiro ^b   Terao, Toshihiko ^b  

^a NetForce Co Ltd   (Japan)

^b HAMAMATSU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c Chuden CTI Co Ltd   (Japan)

^d TOYOHASHI UNIVERSITY OF TECHNOLOGY   (Japan)

Author keywords

Bikunin; CD44; Dimer formation; Growth factor receptors; Signal transduction; Urokinase

Indexed keywords

APROTININ; EPIDERMAL GROWTH FACTOR RECEPTOR; FIBROBLAST GROWTH FACTOR RECEPTOR; GROWTH FACTOR RECEPTOR; HERMES ANTIGEN; LIGAND; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; SCATTER FACTOR RECEPTOR; TRANSFORMING GROWTH FACTOR BETA RECEPTOR; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 2; ULINASTATIN; VASCULOTROPIN RECEPTOR; MEMBRANE PROTEIN; SOYBEAN TRYPSIN INHIBITOR; SPINT2 PROTEIN, HUMAN;

ARTICLE; CANCER CELL; CELL STRAIN HCS 2 8; CELL STRAIN HRA; CELL TYPE; CHONDROSARCOMA; COMPLEX FORMATION; CONTROLLED STUDY; DIMERIZATION; DOWN REGULATION; ENZYME ACTIVATION; GENE FUNCTION; HUMAN; HUMAN CELL; LIGAND BINDING; OVARY CANCER; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RECEPTOR BINDING; SIGNAL TRANSDUCTION; DRUG EFFECT; FEMALE; FLOW CYTOMETRY; IMMUNOPRECIPITATION; METABOLISM; PHOSPHORYLATION; TUMOR CELL LINE;

ANTIGENS, CD44; CELL LINE, TUMOR; DIMERIZATION; DOWN-REGULATION; ENZYME ACTIVATION; FEMALE; FLOW CYTOMETRY; HUMANS; IMMUNOPRECIPITATION; MEMBRANE GLYCOPROTEINS; MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; SIGNAL TRANSDUCTION; TRYPSIN INHIBITOR, KUNITZ SOYBEAN;

EID: 24944584031     PISSN: 07302312     EISSN: None     Source Type: Journal    
DOI: 10.1002/jcb.20364     Document Type: Article

References (52)

1. Aruffo A, Stamenkovic I, Melnick M, Underhill CB, Seed B. 1990. CD44 is the principal cell surface receptor for hyaluronate. Cell 61:1303-1313.
2. Beall MJ, Pearce EJ. 2001. Human transforming growth factor-beta activates a receptor serine/threonine kinase from the intravascular parasite Schistosoma mansoni. J Biol Chem 276:31613-31619.
3. Bertotti A, Comoglio PM. 2003. Tyrosine kinase signal specificity: Lessons from the HGF receptor. Trends Biochem Sci 28:527-533.
4. Boulougouris P, Elder JB. 2002. Epidermal growth factor receptor and transformation. Surg Today 32:667-671.
5. Bourguignon LYW, Lokeshwar VB, He J, Chen X, Bourguignon GJ. 1992. A CD44-like endothelial cell transmembrane glycoprotein (GP116) interacts with extracellular matrix and ankyrin. Mol Cell Biol 12:4464-4471.
6. Bourguignon LYW, Zhu H, Chu A, Iida N, Zhang L, Hung MC. 1997. Interaction between the adhesion receptor, CD44, and the oncogene product, p185HER2, promotes human ovarian tumor cell activation. J Biol Chem 272:27913-27918.
7. Bourguignon LYW, Zhu H, Shao L, Zhu D, Chen YW. 1999. Rho-kinase (ROK) promotes CD44v(3,8-10)-ankyrin interaction and tumor cell migration in metastatic breast cancer cells. Cell Motil Cytoskeleton 43:269-287.
8. Bourguignon LYW, Zhu H, Shao L, Chen YW. 2001. CD44 interaction with c-Src kinase promotes cortactin-mediated cytoskeleton function and hyaluronic acid-dependent ovarian tumor cell migration. J Biol Chem 276:7327-7336.
9. Bourguignon LYW, Singleton PA, Zhu H, Zhou B. 2002. Hyaluronan promotes signaling interaction between CD44 and the transforming growth factor beta receptor I in metastatic breast tumor cells. J Biol Chem 277:39703-39712.
10. Bunn PA, Jr., Franklin W. 2002. Epidermal growth factor receptor expression, signal pathway, and inhibitors in non-small cell lung cancer. Semin Oncol 29(5 Suppl 14):38-44.
11. Carter WG, Wayner EA. 1998. Characterization of the class III collagen receptor, a phosphorylated, transmembrane glycoprotein expressed in nucleated human cells. J Biol Chem 263:4193-4201.
12. Frolik CA, Wakefield LM, Smith DM, Sporn MB. 1984. Characterization of a membrane receptor for transforming growth factor-beta in normal rat kidney fibroblasts. J Biol Chem 259:10995-11000.
13. Guo YJ, Liu G, Wang X, Jin D, Wu M, Ma J, Sy MS. 1994. Potential use of soluble CD44 in serum as indicator of tumor burden and metastasis in patients with gastric or colon cancer. Cancer Res 54:422-426.
14. Hirashima Y, Kobayashi H, Suzuki M, Tanaka Y, Kanayama N, Fujie M, Nishida T, Takigawa M, Terao T. 2001. Characterization of binding properties of urinary trypsin inhibitor to cell-associated binding sites on human chondrosarcoma cell line HCS-2/8. J Biol Chem 276:13650-13656.
15. Hirashima Y, Kobayashi H, Suzuki M, Tanaka Y, Kanayama N, Terao T. 2003. Transforming growth factor-beta1 produced by ovarian cancer cell line HRA stimulates attachment and invasion through an upregulation of plasminogen activator inhibitor type-1 in human peritoneal mesothelial cells. J Biol Chem 278:26793-26802.
16. Jo M, Stolz DB, Esplen JE, Dorko K, Michalopoulos GK, Strom SC. 2000. Cross-talk between epidermal growth factor receptor and c-Met signal pathways in transformed cells. J Biol Chem 275:8806-8811.
17. Kalomiris EL, Bourguignon LYW. 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.
18. Knudson W, Biswas C, Toole BP. 1984. Stimulation of glycosaminoglycan production in murine tumors. J Cell Biochem 25:183-196.
19. Kobayashi H, Shinohara H, Takeuchi K, Itoh M, Fujie M, Saitoh M, Terao T. 1994a. Inhibition of the soluble and the tumor cell receptor-bound plasmin by urinary trypsin inhibitor and subsequent effects on tumor cell invasion and metastasis. Cancer Res 54:844-849.
20. Kobayashi H, Shinohara H, Ohi H, Sugimura M, Terao T, Fujie M. 1994b. Urinary trypsin inhibitor (UTI) and fragments derived from UTI by limited proteolysis efficiently inhibit tumor cell invasion. Clin Exp Metast 12:117-128.
21. Kobayashi H, Fujie M, Shinohara H, Ohi H, Sugimura M, Terao T. 1994c. Effects of urinary trypsin inhibitor on the invasion of reconstituted basement membranes by ovarian cancer cells. Int J Cancer 57:378-384.
22. Kobayashi H, Gotoh J, Fujie M, Terao T. 1994d. Characterization of the cellular binding site for the urinary trypsin inhibitor. J Biol Chem 269:20642-20647.
23. Kobayashi H, Gotoh J, Hirashima Y, Fujie M, Sugino D, Terao T. 1995a. Inhibitory effect of a conjugate between human urokinase and urinary trypsin inhibitor on tumor cell invasion in vitro. J Biol Chem 270:8361-8366.
24. Kobayashi H, Gotoh J, Kanayama N, Hirashima Y, Terao T, Sugino D. 1995b. Inhibition of tumor cell invasion through matrigel by a peptide derived from the domain II region in urinary trypsin inhibition. Cancer Res 55:1847-1852.
25. Kobayashi H, Shinohara H, Gotoh J, Fujie M, Fujishiro S, Terao T. 1995c. Anti-metastatic therapy by urinary trypsin inhibitor in combination with an anti-cancer agent. Br J Cancer 72:1131-1137.
26. Kobayashi H, Shinohara H, Fujie M, Gotoh J, Itoh M, Takeuchi K, Terao T. 1995d. Inhibition of metastasis of Lewis lung carcinoma by urinary trypsin inhibitor in experimental and spontaneous metastasis models. Int J Cancer 63:455-462.
27. Kobayashi H, Gotoh J, Terao T. 1996a. Urinary trypsin inhibitor efficiently inhibits urokinase production in tumor necrosis factor-stimulated ceils. Eur J Cell Biol 71:380-386.
28. Kobayashi H, Gotoh J, Hirashima Y, Terao T. 1996b. Inter-alpha-trypsin inhibitor bound to tumor cells is cleaved into the heavy chains and the light chain on the cell surface. J Biol Chem 271:11362-11367.
29. Kobayashi H, Sugino D, She MY, Ohi H, Hirashima Y, Shinohara H, Fujie M, Shibata K, Terao T. 1998a. A bifunctional hybrid molecule of the amino-terminal fragment of urokinase and domain II of bikunin efficiently inhibits tumor cell invasion and metastasis. Eur J Biochem 253:817-826.
30. Kobayashi H, Sugino D, Terao T. 1998b. Urinary trypsin inhibitor, a Kunitz-type protease inhibitor, modulates tumor necrosis factor-stimulated activation and translocation of protein kinase C in U937 cells. Int J Oncol 12:95-105.
31. Kobayashi H, Hirashima Y, Sun GW, Fujie M, Shibata K, Tamotsu S, Miura K, Sugino D, Tanaka Y, Kondo S, Terao T. 1998c. Identification and characterization of the cell-associated binding protein for urinary trypsin inhibitor. Biochim Biophys Acta 1383:253-268.
32. Kobayashi H, Suzuki M, Sun GW, Hirashima Y, Terao T. 200Oa. Suppression of urokinase-type plasminogen activator expression from human ovarian cancer cells by urinary trypsin inhibitor. Biochim Biophys Acta 1481:310-316.
33. Kobayashi H, Hirashima Y, Sun GW, Fujie M, Nishida T, Takigawa M, Terao T. 200Ob. Identity of urinary trypsin inhibitor-binding protein to link protein. J Biol Chem 275:21185-21191.
34. Kobayashi H, Hirashima Y, Terao T. 200Oc. Human myometrial cells in culture express specific binding sites for urinary trypsin inhibitor. Mol Hum Reprod 6:735-742.
35. Kobayashi H, Suzuki M, Tanaka Y, Hirashima Y, Terao T. 2001. Suppression of urokinase expression and invasiveness by urinary trypsin inhibitor is mediated through inhibition of protein kinase C- and MEK/ERK/c-Jun-dependent signaling pathways. J Biol Chem 276:2015-2022.
36. Kobayashi H, Suzuki M, Kanayama N, Nishida T, Takigawa M, Terao T. 2002. Suppression of urokinase receptor expression by bikunin is associated with inhibition of upstream targets of extracellular signal-regulated kinase-dependent cascade. Eur J Biochem 269:3945-3957.
37. Kobayashi H, Suzuki M, Tanaka Y, Kanayama N, Terao T. 2003. A Kunitz-type protease inhibitor, bikunin, inhibits ovarian cancer cell invasion by blocking the calcium-dependent transforming growth factor-beta 1 signaling cascade. J Biol Chem 278:7790-7799.
38. Kohda D, Morton CJ, Parkar AA, Hatanaka H, Inagaki FM, Campbell ID, Day AJ. 1996. Solution structure of the link module: A hyaluronan-binding domain involved in extracellular matrix stability and cell migration. Cell 86:767-775.
39. Liu D, Sy MS. 1996. A cysteine, residue located in the transmembrane domain of CD44 is important in binding of CD44 to hyaluronic acid. J Exp Med 183:1987-1994.
40. Liu D, Sy MS. 1997. Phorbol myristate acetate stimulates the dimerization of CD44 involving a cysteine in the transmembrane domain. J Immunol 159:2702-2711.
41. Murai T, Miyazaki Y, Nishinakamura H, Sugahara KN, Miyauchi T, Sako Y, Yanagida T, Miyasaka M. 2004. Engagement of CD44 promotes Rac activation and CD44 cleavage during tumor cell migration. J Biol Chem 279:4541-4550.
42. Pauli BU, Knudson W. 1988. Tumor invasion: A consequence of destructive and compositional matrix alterations. Hum Pathol 19:628-639.
43. Sherman LS, Rizvi TA, Karyala S, Ratner N. 2000. CD44 enhances neuregulin signaling by Schwann cells. J Cell Biol 150:1071-1084.
44. Sugino D, Okushima M, Kobayashi H, Terao T. 1998. Production of a hybrid protein consisting of the N-terminal fragment of urokinase and the C-terminal domain of urinary trypsin inhibitor in Escherichia coli. Biotechnol Appl Biochem 27:145-152.
45. Suzuki M, Kobayashi H, Fujie M, Nishida T, Takigawa M, Kanayama N, Terao T. 2002. Kunitz-type protease inhibitor bikunin disrupts phorbol ester-induced oligomerization of CD44 variant isoforms containing epitope v9 and subsequently suppresses expression of urokinase-type plasminogen activator in human chondrosarcoma cells. J Biol Chem 277:8022-8032.
46. Suzuki M, Kobayashi H, Tanaka Y, Hirashima Y, Kanayama N, Takei Y, Saga Y, Suzuki M, Itoh H, Terao T. 2003. A Kunitz-type protease inhibitor, bikunin, inhibits ovarian cancer cell invasion by blocking the calcium-dependent transforming growth factor-beta 1 signaling cascade. J Biol Chem 278:14640-14646.
47. Takigawa M, Okawa T, Pan H, Aoki C, Takahashi K, Zue J, Suzuki F, Kinoshita A. 1997. Insulin-like growth factors I and II are autocrine factors in stimulating proteoglycan synthesis, a marker of differentiated chondrocytes, acting through their respective receptors on a clonal human chondrosarcoma- derived chondrocyte cell line, HCS-2/8. Endocrinol 138:4390-4400.
48. Underhill CB, Chi-Rosso G, Toole BP. 1983. Effects of detergent solubilization on the hyaluronate-binding protein from membranes of simian virus 40-transformed 3T3 cells. J Biol Chem 258:8086-8091.
49. Wobus M, Kuns R, Wolf C, Horn LC, Kohler U, Sheyn I, Werness BA, Sherman LS. 2001. CD44 mediates constitutive type I receptor signaling in cervical carcinoma cells. Gynecol Oncol 83:227-234.
50. Wobus M, Rangwala R, Sheyn I, Hennigan R, Coila B, Lower EE, Yassin RS, Sherman LS. 2002. CD44 associates with EGFR and erbB2 in metastasizing mammary carcinoma cells. Appl Immunohistochem Mol Morphol 10:34-39.
51. Zhang M, Singh RK, Wang MH, Wells A, Siegal GP. 1996. Epidermal growth factor induces CD44 gene expression through a novel regulatory element in mouse fibroblasts. Clin Exp Metastasis 14:268-276.
52. Zhang M, Wang MH, Singh RK, Wells A, Siegal GP. 1997. Epidermal growth factor induces CD44 gene expression through a novel regulatory element in mouse fibroblasts. J Biol Chem 272:14139-14146.