Disassociation of Met-mediated biological responses in vivo: The natural hepatocyte growth factor/scatter factor splice variant NK2 antagonizes growth but facilitates metastasis

Molecular and Cellular Biology

Volumn 20, Issue 6, 2000, Pages 2055-2065

  Otsuka, Toshiyuki ^a   Jakubczak, John ^a   Vieira, Wilfred ^a   Bottaro, Donald P ^a   Breckenridge, Diane ^a   Larochelle, William J ^a   Merlino, Glenn ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SCATTER FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CANCER INVASION; CELL MOTILITY; CONTROLLED STUDY; IMMUNOHISTOCHEMISTRY; KIDNEY; LIVER; MELANOMA; METASTASIS POTENTIAL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTO ONCOGENE; SIGNAL TRANSDUCTION; TRANSGENE;

ANIMALS; CELL DIVISION; GENE EXPRESSION REGULATION, NEOPLASTIC; HEPATOCYTE GROWTH FACTOR; LIVER; LIVER NEOPLASMS, EXPERIMENTAL; MICE; MICE, TRANSGENIC; NEOPLASM METASTASIS; PROTEIN ISOFORMS; RNA SPLICING;

ANIMALIA; MUS MUSCULUS;

EID: 0033999314     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.20.6.2055-2065.2000     Document Type: Article

References (75)

1. Bardelli, A., M. L. Basile, E. Audero, S. Giordano, S. Wennstrom, S. Menard, P. M. Comoglio, and C. Ponzetto. 1999. Concomitant activation of pathways downstream of Grh2 and PI 3-kinase is required for MET-mediated metastasis. Oncogene 18:1139-1146.
2. Bellusci, S., G. Moens, G. Gaudino, P. Comoglio, T. Nakamura, J.-P. Thiery, and J. Jouanneau. 1994. Creation of a hepatocyte growth factor/scatter factor autocrine loop in carcinoma cells induces invasive properties associated with increased tumorigenicity. Oncogene 9:1091-1099.
3. Bladt, F., D. Riethmacher, S. Isenmann, A. Aguzzi, and C. Birchmeier. 1995. Essential role for the c-met receptor in the migration of myogenic precursor cells into the limb bud. Nature 376:768-771.
4. Bottaro, D. P., J. S. Rubin, D. L. Faletto, A. M. Chan, T. E. Kmiecik, G. F. Vande Woude, and S. A. Aaronson. 1991. Identification of the hepatocyte growth factor receptor as the c-met proto-oncogene product. Science 251: 802-804.
5. Castagnino, P., J. V. Soriano, R. Montesano, and D. P. Bottaro. 1998. Induction of tissue inhibitor of metalloproteinases-3 is a delayed early cellular response to hepatocyte growth factor. Oncogene 17:481-492.
6. Chan, A. M.-L., J. S. Rubin, D. P. Bottaro, D. W. Hirschfield, M. Chedid, and S. A. Aaronson. 1991. Identification of a competitive HGF antagonist encoded by an alternative transcript. Science 254:1382-1385.
7. Chirgadze, D. Y., J. Hepple, R. A. Byrd, R. Sowdhamini, T. L. Blundell, and E. Gherardi. 1998. Insights into the structure of hepatocyte growth factor/ scatter factor (HGF/SF) and implications for receptor activation. FEBS Lett. 430:126-129.
8. Chirgadze, D. Y., J. P. Hepple, H. Zhou, A. Byrd, T. L. Blundell, and E. Gherardi. 1999. Crystal structure of the NK1 fragment of HGF/SF suggests a novel mode for growth factor dimerization and receptor binding. Nat. Struct. Biol. 6:72-79.
9. Cioce, V., K. G. Csaky, A. M.-L. Chan, D. P. Bottaro, W. G. Taylor, R. Jensen, S. A. Aaronson, and J. S. Rubin. 1996. Hepatocyte growth factor (HGF)/NK1 is a naturally occurring HGF/scatter factor variant with partial agonist/antagonist activity. J. Biol. Chem. 271:13110-13115.
10. Date, K., K. Matsumoto, H. Shimura, M. Tanaka, and T. Nakamura. 1997. HGF/NK4 is a specific antagonist for pleiotrophic actions of hepatocyte growth factor. FEBS Lett. 420:1-6.
11. Day, R. M., V. Cioce, D. Breckenridge, P. Castagnino, and D. P. Bottaro. 1999. Differential signaling by alternative HGF isoforms through c-Met: activation of both MAP kinase and PI 3-kinase pathways is insufficient for mitogenesis. Oncogene 18:3399-3406.
12. Dean, M., M. Park, and G. F. Vande Woude. 1987. Characterization of the rearranged tpr-met oncogene breakpoint. Mol. Cell. Biol. 7:921-924.
13. Ferracini, R., M. F. Di Renzo, K. Scotlandi, N. Baldini, M. Olivero, P. Lollini, O. Cremona, M. Campanacci, and P. M. Comoglio. 1995. The Met/ HGF receptor is over-expressed in human osteosarcomas and is activated by either a paracrine or an autocrine circuit. Oncogene 10:739-749.
14. Ferracini, R., M. Olivero, M. F. Di Renzo, M. Martano, C. De Giovanni, P. Nanni, G. Basso, K. Scotlandi, P.-L. Lollini, and P. M. Comoglio. 1996. Retroviral expression of the MET proto-oncogene correlates with the invasive phenotype of human rhabdomyosarcomas. Oncogene 11:1697-1705.
15. Gherardi, E., and M. Stoker. 1991. Hepatocyte growth factor-scatter factor: mitogen, motogen, and Met. Cancer Cells 3:227-232.
16. Giordano, S., A. Bardelli, Z. Zhen, S. Menard, C. Ponzetto, and P. M. Comoglio. 1997. A point mutation in the MET oncogene abrogates metastasis without affecting transformation. Proc. Natl. Acad. Sci. USA 94:13868-13872.
17. Ban, S., L. A. Stuart, and S. J. Degen. 1991. Characterization of the DNF15S2 locus on human chromosome 3: identification of a gene coding for four kringle domains with homology to hepatocyte growth factor. Biochemistry 30:9768-9780.
18. Hartmann, G., L. Naldini, K. M. Weidner, M. Sachs, E. Vigna, P. M. Comoglio, and W. Birchmeier. 1992. A functional domain in the heavy chain of scatter factor/hepatocyte growth factor binds the c-Met receptor and induces cell dissociation but no mitogenesis. Proc. Natl. Acad. Sci. USA 89:11574-11578.
19. Iyer, A., T. E. Kmiecik, M. Park, I. Daar, D. Blair, K. J. Dunn, P. Sutrave, J. N. Ihle, M. Bodescot, and G. F. Vande Woude. 1990. Structure, tissue-specific expression, and transforming activity of the mouse met protooncogene. Cell Growth Differ. 1:87-95.
20. Jakubczak, J., W. J. LaRochelle, and G. Merlino. 1998. NK1, a natural splice variant of hepatocyte growth factor/scatter factor, is a partial agonist in vivo. Mol. Cell. Biol. 18:1275-1283.
21. Jeffers, M., S. Rong, and G. F. Vande Woude. 1996. Hepatocyte growth factor/scatter factor-Met signaling in tumorigenicity and invasion/metastasis. J. Mol. Med. 74:505-513.
22. Jeffers, M., S. Rong, M. Anver, and G. F. Vande Woude. 1996. Autocrine hepatocyte growth factor/scatter factor-Met signaling induces transformation and the invasive/metastatic phenotype in C127 cells. Oncogene 13:853-861.
23. Jeffers, M., S. Rong, and G. F. Vande Woude. 1996. Enhanced tumorigenicity and invasion-metastasis by hepatocyte growth factor/scatter factor-Met signalling in human cells concomitant with induction of the urokinase proteolysis network. Mol. Cell. Biol. 16:1115-1125.
24. Jeffers, M., L. Schmidt, N. Nakaigawa, C. P. Webb, G. Weirich, T. Kishida, B. Zbar, and G. F. Vande Woude. 1997. Activating mutations for the MET tyrosine kinase receptor in human cancer. Proc. Natl. Acad. Sci. USA 94: 11445-11450.
25. Jhappan, C., C. Stahle, R. N. Harkins, N. Fausto, G. H. Smith, and G. T. Merlino. 1990. TGFα overexpression in transgenic mice induces liver neoplasia and abnormal development of the mammary gland and pancreas. Cell 61:1137-1146.
26. Keely, P. J., J. K. Westwick, I. P. Whitehead, C. J. Der, and L. V. Parise. 1997. Cdc42 and Rac1 induce integrin-mediated cell motility and invasive-ness through PI(3)K. Nature 390:632-636.
27. Khwaja, A., K. Lehmann, B. M. Marte, and J. Downward. 1998. Phosphoinositide 3-kinase induces scattering and tubulogenesis in epithelial cells through a novel pathway. J. Biol. Chem. 273:18793-18801.
28. Lokker, N. A., and P. J. Godowski. 1993. Generation and characterization of a competitive antagonist of human hepatocyte growth factor, HGF/NK1. J. Biol. Chem. 268:17145-17150.
29. Matsumoto, K., and T. Nakamura. 1996. Emerging multipotent aspects of hepatocyte growth factor. J. Biochem. 119:591-600.
30. Miyazawa, K., A. Kitamura, D. Naka, and N. Kitamura. 1991. An alternatively processed mRNA generated from human hepatocyte growth factor gene. Eur. J. Biochem. 197:15-22.
31. Montesano, R., J. V. Soriano, K. M. Malinda, M. L. Ponce, A. Bafico, H. K. Kleinman, D. P. Bottaro, and S. A. Aaronson. 1998. Differential effects of hepatocyte growth factor isoforms on epithelial and endothelial tubulogenesis. Cell Growth Differ. 9:355-365.
32. Naldini, L., E. Vigna, R. P. Narsimhan, G. Gaudino, R. Zarnegar, G. K. Michalopoulos, and P. M. Comoglio. 1991. Hepatocyte growth factor (HGF) stimulates the tyrosine kinase activity of the receptor encoded by the proto-oncogene c-MET. Oncogene 6:501-504.
33. Natali, P. G., M. R. Nicotra, M. R. Di Renzo, M. Prat, A. Bigotti, R. Cavaliere, and P. M. Comoglio. 1993. Expression of the c-MET/HGF receptor in human melanocytic neoplasms: demonstration of the relationship to malignant melanoma tumour progression. Br. J. Cancer 68:746-750.
34. National Academy of Sciences. 1996. Guide for the care and use of laboratory animals. Institute for Laboratory Animal Resources, National Research Council, National Academy of Sciences, Washington, D.C.
35. Okigaki, M., M. Komada, Y. Uehara, K. Miyazawa, and N. Kitamura. 1992 Functional characterization of human hepatocyte growth factor mutants obtained by deletion of structural domains. Biochemistry 31:9555-9561.
36. Otsuka, T., H. Takayama, R. Sharp, G. Celli, W. J. LaRochelle, D. Bottaro, N. Ellmore, W. Vieira, J. W. Owens, M. Anver, and G. Merlino. 1998. c-Met autocrine activation induces development of malignant melanoma and acquisition of the metastatic phenotype. Cancer Res. 58:5157-5167.
37. Palmiter, R. D., E. P. Sandgren, D. M. Koeller, and R. L. Brinster. 1993. Distal regulatory elements from the mouse metallothionein locus stimulate gene expression in transgenic mice. Mol. Cell. Biol. 13:5266-5275.
38. Park, M., M. Dean, C. S. Cooper, M. Schmidt, S. J. O'Brien, D. G. Blair, and G. F. Vande Woude. 1986. Mechanism of met oncogene activation. Cell 45:895-904.
39. Ponzetto, C., A. Bardelli, F. Maina, P. Longati, G. Panayotou, R. Dhand, M. D. Waterfield, and P. M. Comoglio. 1993. A novel recognition motif for phosphatidylinositol 3-kinase binding mediates its association with the hepatocyte growth factor/scatter factor receptor. Mol. Cell. Biol. 13:4600-4608.
40. Ponzetto, C., A. Bardelli, Z. Zhen, F. Maina, P. dalla Zonca, S. Giordano, A. Graziani, G. Panayotou, and P. M. Comoglio. 1994. A multifunctional docking site mediates signaling and transformation by the hepatocyte growth factor/scatter factor receptor family. Cell 77:261-271.
41. Ponzetto, C., Z. Zhen, E. Audero, F. Maina, A. Bardelli, M. L. Basile, S. Giordano, R. Narsimhan, and P. M. Comoglio. 1996. Specific uncoupling of GRB2 from the Met receptor. Differential effects on transformation and motility. J. Biol. Chem. 271:14119-14123.
42. Prat, M., R. P. Narsimhan, T. Crepaldi, M. R. Nicotra, P. G. Natali, and P. M. Comoglio. 1991. The receptor encoded by the human c-MET oncogene is expressed in hepatocytes, epithelial cells and solid tumors. Int. J. Cancer 49:323-328.
43. Prat, M., T. Crepaldi, S. Pennacchietti, F. Bussolino, and P. M. Comoglio. 1998. Agonistic monoclonal antibodies against the Met receptor dissect the biological responses to HGF. J. Cell Sci. 111:237-247.
44. Rong, S., M. Bodescot, D. Blair, J. Dunn, T. Nakamura, K. Mizuno, M. Park, A. Chan, S. Aaronson, and G. F. Vande Woude. 1992. Tumorigenicity of the met proto-oncogene and the gene for hepatocyte growth factor. Mol. Cell. Biol. 12:5152-5158.
45. Rong, S., M. Jeffers, J. H. Resau, I. Tsarfaty, M. Oskarsson, and G. F. Vande Woude. 1993. Met expression and sarcoma tumorigenicity. Cancer Res. 53: 5355-5360.
46. Rong, S., M. Oskarsson, D. L. Faletto, I. Tsarfaty, J. Resau, T. Nakamura, E. Rosen, R. Hopkins, and G. F. Vande Woude. 1993. Tumorigenesis induced by coexpression of human hepatocyte growth factor and the human MET protooncogene leads to high levels of expression of the ligand and receptor. Cell Growth Differ. 4:563-569.
47. Rong, S., S. Segal, M. Anver, J. H. Resau, and G. F. Vande Woude. 1994. Invasiveness and metastasis of NIH/3T3 cells induced by Met-HGF/SF autocrine stimulation. Proc. Natl. Acad. Sci. USA 91:4731-4735.
48. Rong, S., L. A. Donehower, M. F. Hansen, L. Strong, M. Tainsky, M. Jeffers, J. H. Resau, E. Hudson, I. Tsarfaty, and G. F. Vande Woude. 1995. Met proto-oncogene product is overexpressed in tumors of p53-deficient mice and tumors of Li-Fraumeni patients. Cancer Res. 55:1963-1970.
49. Rosen, E. M., K. Lamszus, J. Laterra, P. J. Polverini, J. S. Rubin, and I. D. Goldberg. 1997. HGF/SF in angiogenesis. Ciba Found. Symp. 212:215-226.
50. Royal, I., and M. Park. 1995. Hepatocyte growth factor-induced scatter of Madin-Darby canine kidney cells requires phosphatidylinositol 3-kinase. J. Biol. Chem. 270:27780-27787.
51. Rubin, J. S., A. M. Chan, D. P. Bottaro, W. H. Burgess, W. G. Taylor, A. C. Cech, D. W. Hirschfield, J. Wong, T. Miki, P. W. Finch, and S. A. Aaronson. 1991. A broad-spectrum human lung fibroblast-derived mitogen is a variant of hepatocyte growth factor. Proc. Natl. Acad. Sci. USA 88:415-419.
52. Rubin, J. S., D. P. Bottaro, and S. A. Aaronson. 1993 Hepatocyte growth factor/scatter factor and its receptor, the c-met proto-oncogene product. Biochim. Biophys. Acta 1155:357-371.
53. Sakata, H., H. Takayama, R. Sharp, J. S. Rubin, G. Merlino, and W. J. LaRochelle. 1996. Hepatocyte growth factor/scatter factor overexpression induces growth, abnormal development, and tumor formation in transgenic mouse livers. Cell Growth Differ. 7:1513-1523.
54. Schmidt, C., F. Bladt, S. Goedecke, V. Brinkman, W. Zschiesche, M. Sharpe, E. Gherardi, and C. Birchmeier. 1995. Scatter factor/hepatocyte growth factor is essential for liver development. Nature 373:699-702.
55. Schmidt, L., F. M. Duh, F. Chen, T. Kishida, G. Glenn, P. Choyke, S. W. Scherer, Z. Zhuang, I. Lubensky, M. Dean, R. Allikmets, A. Chidambaram, U. R. Bergerheim, J. T. Feltis, C. Casadevall, A. Zamarron, M. Bernues, S. Richard, C. J. Lips, M. M. Walther, L. C. Tsui, L. Geil, M. L. Orcutt, T. Stackhouse, J. Lipan, L. Slife, H. Brauch, J. Decker, G. Niehans, M. D. Hughson, H. Moch, S. Storkel, M. I. Urman, W. M. Linehan, and B. Zbar. 1997. Germline and somatic mutations in the tyrosine kinase domain of the MET proto-oncogene in papillary renal carcinomas. Nat. Genet. 16:68-73.
56. Schwall, R. H., L. Y. Chang, P. J. Godowski, D. W. Kahn, K. J. Hillan, K. D. Bauer, and T. F. Zioncheck. 1996. Heparin induces dimerization and confers proliferative activity onto the hepatocyte growth factor antagonists NK1 and NK2. J. Cell Biol. 133:709-718.
57. Sharp, R., M. W. Babyatsky, H. Takagi, S. Tagerud, T. C. Wang, D. E. Bockman, S. J. Brand, and G. Merlino. 1995. Transforming growth factor-α disrupts the normal program of cellular differentiation in the gastric mucosa of transgenic mice. Development 121:149-161.
58. Shaw, L. M., I. Rabinovitz, H. H. Wang, A. Toker, and A. M. Mercurio. 1997. Activation of phosphoinositide 3-OH kinase by the alpha6beta4 integrin promotes carcinoma invasion. Cell 91:949-960.
59. Silvagno, F., A. Follenzi, M. Arese, M. Prat, E. Giraudo, G. Gaudino, G. Camussi, P. M. Comoglio, and F. Bussolino. 1995. In vivo activation of met tyrosine kinase by heterodimeric hepatocyte growth factor molecule promotes angiogenesis. Arterioscler. Thromb. Vasc. Biol. 15:1857-1865.
60. Sonnenberg, E., D. Meyer, K. M. Weidner, and C. Birchmeier. 1993. Scatter factor/hepatocyte growth factor and its receptor, the c-Met tyrosine kinase, can mediate a signal exchange between mesenchyme and epithelia during mouse development. J. Cell Biol. 123:223-235.
61. Stahl, S. J., P. T. Wingfield, J. D. Kaufman, L. K. Pannell, V. Cloce, H. Sakala, W. G. Taylor, J. S. Rubin, and D. P. Bottaro. 1997. Functional and biophysical characterization of recombinant human hepatocyte growth factor isoforms produced in Escherichia coli. Biochem. J. 326:763-772.
62. Takayama, H., W. J. LaRochelle, M. Anver, D. E. Bookman, and G. Merlino. 1996. Scatter factor/hepatocyte growth factor as a regulator of skeletal muscle and neural crest development. Proc. Natl. Acad. Sci. USA 93:5866-5871.
63. Takayama, H., W. J. LaRochelle, R. Sharp, T. Otsuka, P. Kriebel, M. Anver, S. A. Aaronson, and G. Merlino. 1997. Diverse tumorigenesis associated with aberrant development in mice overexpressing hepatocyte growth factor/scatter factor. Proc. Natl. Acad. Sci. USA 94:701-706.
64. Takayama, H., W. J. LaRochelle, S. G. Sabnis, T. Otsuka, and G. Merlino. 1997. Renal tubular hyperplasia, polycystic disease and glomerulosclerosis in transgenic mice overexpressing hepatocyte growth factor/scatter factor. Lab. Investig. 77:131-138.
65. Tsarfaty, I., S. Rong, J. H. Resau, S. Rulong, P. Pinto da Silva, and G. F. Vande Woude. 1994. Met mediated signaling in mesenchymal to epithelial cell conversion. Science 263:98-101.
66. Tuck, A. B., M. Park, E. E. Sterns, A. Boag, and B. E. Elliott. 1996. Coexpression of hepatocyte growth factor and receptor (Met) in human breast carcinoma. Am. J. Pathol. 148:225-232.
67. Tulinsky, A. 1991. The structures of domains of blood proteins. Thromb. Haemostasis 66:16-31.
68. Uehara, Y., O. Minowa, C. Mori, K. Shiota, J. Kuno, T. Noda, and N. Kitamura. 1995. Placental defect and embryonic lethality in mice lacking hepatocyte growth factor/scatter factor. Nature 373:702-705.
69. Ultsch, M., N. A. Lokker, P. J. Godowski, and A. M. de Vos. 1998. Crystal structure of the NK1 fragment of human hepatocyte growth factor at 2.0 A resolution. Structure 6:1383-1393.
70. Weidner, K. M., M. Sachs, D. Riethmacher, and W. Birchmeier. 1995. Mutation of juxtamembrane tyrosine residue 1001 suppresses loss-of-function mutations of the met receptor in epithelial cells. Proc. Natl. Acad. Sci. USA 92:2597-2601.
71. Weidner, K. M., S. Di Cesare, M. Sachs, V. Brinkmann, J. Behrens, and W. Birchmeier. 1996. Interaction between Gab1 and the c-Met receptor tyrosine kinase is responsible for epithelial morphogenesis. Nature 384:173-176.
72. Weiss, A., and J. Schlessinger. 1998. Switching signals on or off by receptor dimerization. Cell 94:277-280.
73. Yoshimura, T., N. Yuhki, M. H. Wang, A. Skeel, and E. J. Leonard. 1993. Cloning, sequencing and expression of human macrophage stimulating protein (MSP, MST1) confirms MSP as a member of the family of kringle proteins and locates the MSP gene on chromosome 3. J. Biol. Chem. 268: 15461-15468.
74. Zarnegar, R., and G. K. Michalopoulos. 1995. The many faces of hepatocyte growth factor: from hepatopoiesis to hematopoiesis. J. Cell Biol. 129:1177-1180.
75. Zhuang, Z., W. S. Park, S. Pack, L. Schmidt, A. O. Vortmeyer, E. Pak, T. Pham, R. J. Weil, S. Candidus, I. A. Lubensky, W. M. Linehan, B. Zbar, and G. Weirich. 1998. Trisomy 7-harbouring non-random duplication of the mutant MET allele in hereditary papillary renal carcinomas. Nat. Genet. 20:66-69.