Genetic downregulation of pregnancy-associated plasma protein-A (PAPP-A) by bikunin reduces IGF-I-dependent Akt and ERK1/2 activation and subsequently reduces ovarian cancer cell growth, invasion and metastasis

International Journal of Cancer

Volumn 109, Issue 3, 2004, Pages 336-347

  Tanaka, Yoshiko ^a   Kobayashi, Hiroshi ^a   Suzuki, Mika ^a   Hirashima, Yasuyuki ^a   Kanayama, Naohiro ^a   Terao, Toshihiko ^a  

^a HAMAMATSU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Antisense; Bikunin; IGF binding protein 4 protease; Insulin like growth factor; Invasion; Ovarian cancer; Pregnancy associated plasma protein A

Indexed keywords

COMPLEMENTARY DNA; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; PHOSPHATIDYLINOSITOL 3 KINASE; PREGNANCY ASSOCIATED PLASMA PROTEIN A; PROTEIN KINASE B; PROTEINASE INHIBITOR; SOMATOMEDIN BINDING PROTEIN 4; SOMATOMEDIN C; ULINASTATIN; UROKINASE; UROKINASE RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CELL CULTURE; CANCER GROWTH; CANCER INHIBITION; CANCER INVASION; CELL PROLIFERATION; CONTROLLED STUDY; CORRELATION ANALYSIS; DNA MICROARRAY; DOWN REGULATION; DRUG EFFECT; DRUG EFFICACY; DRUG POTENCY; DRUG TARGETING; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GROWTH RATE; HUMAN; HUMAN CELL; METASTASIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OVARY CANCER; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION;

CELL DIVISION; DOWN-REGULATION; ENZYME ACTIVATION; FEMALE; HUMANS; INSULIN-LIKE GROWTH FACTOR BINDING PROTEIN 4; INSULIN-LIKE GROWTH FACTOR I; MAP KINASE SIGNALING SYSTEM; MEMBRANE GLYCOPROTEINS; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MITOGEN-ACTIVATED PROTEIN KINASES; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; OLIGONUCLEOTIDES, ANTISENSE; OVARIAN NEOPLASMS; PREGNANCY-ASSOCIATED PLASMA PROTEIN-A; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; RNA, MESSENGER; SERINE PROTEINASE INHIBITORS; TRYPSIN INHIBITOR, KUNITZ SOYBEAN; TUMOR CELLS, CULTURED; URINARY PLASMINOGEN ACTIVATOR;

EID: 1342309624     PISSN: 00207136     EISSN: None     Source Type: Journal    
DOI: 10.1002/ijc.11700     Document Type: Article

References (42)

1. Schmitt M, Harbeck N, Thomssen C, Wilhelm O, Magdolen V, Reuning U. Clinical impact of the plasminogen activation system in tumor invasion and metastasis: prognostic relevance and target for therapy. Thromb Haemost 1997;78:285-96.
2. Ellenrieder V, Alber B, Lacher U, Hendler SF, Menke A, Boeck W, Wagner M, Wilda M, Friess H, Buchler M, Adler G, Gress TM. Role of MT-MMPs and MMP-2 in pancreatic cancer progression. Int J Cancer 2000;85:14-20.
3. Achbarou A, Kaiser S, Tremblay G, Ste-Marie LG, Brodt P, Goltzman D, Rabbani SA. Urokinase overproduction results in increased skeletal metastasis by prostate cancer cells in vivo. Cancer Res 1994;54:2372-7.
4. Bernhard EJ, Gruber SB, Muschel RJ. Direct evidence linking expression of matrix metalloproteinase 9 (92-kDa gelatinase/collagenase) to the metastatic phenotype in transformed rat embryo cells. Proc Natl Acad Sci USA 1994;91:4293-7.
5. Suzuki M, Kobayashi H, Tanaka Y, Hirashima Y, Terao T. Structure and function analysis of urinary trypsin inhibitor (UTI): identification of binding domains and signaling property of UTI by analysis of truncated proteins. Biochim Biophys Acta 2001;1547:26-36.
6. Kobayashi H, Suzuki M, Tanaka Y, Hirashima Y, Terao T. 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 2001;276:2015-22.
7. Kobayashi H, Suzuki M, Kanayama N, Nishida T, Takigawa M, Terao T. Suppression of urokinase receptor expression by bikunin is associated with inhibition of upstream targets of extracellular signal-regulated kinase-dependent cascade. Eur J Biochem 2002;269:3945-57.
8. Kobayashi H, Suzuki M, Tanaka Y, Kanayama N, Terao T. 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 2003;278:7790-9.
9. Suzuki M, Kobayashi H, Tanaka Y, Hirashima Y, Kanayama N, Takei Y, Saga Y, Suzuki M, Itoh H, Terao T. Suppression of invasion and peritoneal carcinomatosis of ovarian cancer cell line by overexpression of bikunin. Int J Cancer 2003;104:289-302.
10. Suzuki M, Kobayashi H, Tanaka Y, Hirashima Y, Kanayama N, Takei Y, Saga Y, Suzuki M, Itoh H, Terao T. Bikunin target genes in ovarian cancer cells identified by microarray analysis. J Biol Chem 2003;278:14640-6.
11. Lawrence JB, Oxvig C, Overgaard MT, Sottrup-Jensen L, Gleich GJ, Hays LG, Yates JR III, Conover CA. The insulin-like growth factor (IGF)-dependent IGF binding protein-4 protease secreted by human fibroblasts is pregnancy associated plasma protein-A. Proc Natl Acad Sci USA 1999;96:3149-53.
12. Conover CA, Oxvig C, Overgaard MT, Christiansen M, Giudice LC. Evidence that the insulin-like growth factor binding protein-4 protease in human ovarian follicular fluid is pregnancy associated plasma protein-A. J Clin Endocrinol Metab 1999;84:4742-5.
13. Kaleko M, Rutter WJ, Miller AD. Overexpression of the human insulin like growth factor I receptor promotes ligand-dependent neoplastic transformation. Mol Cell Biol 1990;10:464-73.
14. Sell C, Baserga R, Rubin R. Insulin-like growth factor I (IGF-I) and the IGF-I receptor prevent etoposide-induced apoptosis. Cancer Res 1995;55:303-6.
15. Wu Y, Tewari M, Cui S, Rubin R. Activation of the insulin-like growth factor-I receptor inhibits tumor necrosis factor-induced cell death. J Cell Physiol 1996;168:499-509.
16. Bergmann U, Funatomi H, Yokoyama M, Beger HG, Korc M. Insulin-like growth factor I overexpression in human pancreatic cancer: evidence for autocrine and paracrine roles. Cancer Res 1995;55:2007-11.
17. 5 to promote tumor cell dissemination in vivo. J Clin Invest 1997;99:1390-8.
18. Mazerbourg S, Zapf J, Bar RS, Brigstock DR, Lalou C, Binoux M, Monget P. Insulin-like growth factor binding protein-4 proteolytic degradation in ovine preovulatory follicles: studies of underlying mechanism. Endocrinology 1999;140:4175-84.
19. Dunn SE, Torres JV, Nihei N, Barrett JC. The insulin-like growth factor-1 elevates urokinase-type plasminogen activator-1 in human breast cancer cells: a new avenue for breast cancer therapy. Mol Carcinog 2000;27:10-7.
20. Shimasaki S, Ling N. Identification and molecular characterization of insulin-like growth factor binding protein (IGFBP-1, -2, -3, -4, -5, and -6). Prog Growth Factor Res 1991;3:243-66.
21. Fowlkes JL. Insulinlike growth factor-binding protein proteolysis: all emerging paradigm in insulinlike growth factor physiology. Trends Endocrinol Metab 1997;8:299-306.
22. Rees C, Clemmons DR, Horvitz GD, Clarke JB, Busby WH. A protease-resistant form of insulin-like growth factor (IGF) binding protein 4 inhibits IGF-1 actions. Endocrinology 1998;139:4182-8.
23. Overgaard MT, Oxvig C, Christiansen M, Lawrence JB, Conover CA, Gleich GJ, Sottrup-Jensen L, Haaning J. Messenger ribonucleic acid levels of pregnancy-associated plasma protein-A and the proform of eosinophil major basic protein: expression in human reproductive and nonreproductive tissues. Biol Reprod 1999;61:1083-9.
24. Zhu JD, Pan HO, Suzuki F, Takigawa M. Proto-oncogene expression in a human chondrosarcoma cell line: HCS-2/8. Jpn J Cancer Res 1994;85:364-71.
25. Takigawa M, Okawa T, Pan H, Aoki C, Takahashi K, Zue J, Suzuki F, Kinoshita A. 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. Endocrinology 1997;138:4390-400.
26. Damon SE, Maddison L, Ware JL, Plymate SR. Overexpression of an inhibitory insulin-like growth factor binding protein (IGFBP), IGFBP-4, delays onset of prostate tumor formation. Endocrinology 1998;139:3456-64.
27. Shimasaki S, Uchiyama F. Molecular cloning of the cDNAs encoding a novel insulin-like growth factor-binding protein from rat and human. Mol Endocrinol 1990;4:1451-8.
28. 131I-labelled human growth hormone of high specific radioactivity. Biochem J 1963;89:114-23.
29. Oxvig C, Sand O, Kristensen T, Kristensen L, Sottrup-Jensen L. Isolation and characterization of circulating complex between human pregnancy-associated plasma protein-A and proform of eosinophil major basic protein. Biochim Biophys Acta 1994;1201:415-23.
30. Basbaum CB, Werb Z. Focalized proteolysis: spatial and temporal regulation of extracellular matrix degradation at the cell surface. Curr Opin Cell Biol 1996;8:731-8.
31. Laursen LS, Overgaard MT, Søe R, Boldt HB, Sottrup-Jensen L, Giudice LC, Conover CA, Oxvig C. Pregnancy-associated plasma protein-A (PAPP- A) cleaves insulin-like growth factor binding protein (IGFBP)-5 independent of IGF: implications for the mechanism of IGFBP-4 proteolysis by PAPP-A. FEBS Lett 2001;504:36-40.
32. Monget P, Mazerbourg S, Delpuech T, Maurel MC, Maniere S, Zapf J, Lalmanach G, Oxvig C, Overgaard MT. Pregnancy-associated plasma protein-A is involved in insulin-like growth factor binding protein-2 (IGFBP-2) proteolytic degradation in bovine and porcine preovulatory follicles: identification of cleavage site and characterization of IGFBP-2 degradation. Biol Reprod 2003;68:77-86.
33. Chen W-T. Membrane proteases: roles in tissue remodeling and tumour invasion. Curr Opin Cell Biol 1992;4:802-9.
34. Dunn SE, Torres JV, Oh JS, Cykert DM, Barrett JC. Up-regulation of urokinase-type plasminogen activator by insulin-like growth factor-I depends upon phosphatidylinositol-3 kinase and mitogen-activated protein kinase kinase. Cancer Res 2001;61:1367-74.
35. Dufourny B, Alblas J, van Teeffelen HA, van Schaik FM, van der Burg B, Steenbergh PH, Sussenbach JS. Mitogenic signaling of insulin-like growth factor-1 in MCF-7 human breast cancer cells requires phosphatidylinositol 3-kinase and is independent of mitogen-activated protein kinase. J Biol Chem 1997;272:31163-371.
36. Datta SR, Dudek H, Tao X, Masters S, Fu H, Gotoh Y, Greenberg ME. Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 1997;91:231-41.
37. Cardone MH, Roy N, Stennicke HR, Salvesen GS, Franke TF, Stanbridge E, Frisch S, Reed JC. Regulation of cell death protease caspase-9 by phosphorylation. Science 1998;282:1318-21.
38. Chen TK, Smith LM, Gebhardt DK, Birrer MJ, Brown PH. Activation and inhibition of the AP-1 complex in human breast cancer cells. Mol Carcinog 1996;15:215-26.
39. Tanno S, Tanno S, Mitsuuchi Y, Altomare DA, Xiao GH, Testa JR. AKT activation up-regulates insulin-like growth factor I receptor expression and promotes invasiveness of human pancreatic cancer cells. Cancer Res 2001;61:589-93.
40. Miwa W, Yasuda J, Murakami Y, Yashima K, Sugano K, Sekine T, Kono A, Egawa S, Yamaguchi K, Hayashizaki Y, Sekiya T. Isolation of DNA sequences amplified at chromosome 19q13.1-q13.2 including the AKT2 locus in human pancreatic cancer. Biochem Biophys Res Commun 1996;225:968-74.
41. Ruggeri BA, Huang L, Wood M, Cheng JQ, Testa JR. Amplification and overexpression of the AKT2 oncogene in a subset of human pancreatic ductal adenocarcinomas. Mol Carcinog 1998;21:81-6.
42. Kotelevets L, Noe V, Bruyneel E, Myssiakine E, Chastre E, Mareel M, Gespach C. Inhibition by platelet-activating factor of Src- and hepatocyte growth factor-dependent invasiveness of intestinal and kidney epithelial cells: phosphatidylinositol 3′-kinase is a critical mediator of tumor invasion. J Biol Chem 1998;273:14138-45.