Scatter-factor and semaphorin receptors: cell signalling for invasive growth

Nature Reviews Cancer - Tập 2 Số 4 - Trang 289-300 - 2002
Livio Trusolino1, Paolo M. Comoglio1
1Istituto per la Ricerca e la Cura del Cancro, (Institute for Cancer Research and Treatment), University of Torino School of Medicine, Candiolo (Torino), Italy

Tóm tắt

Từ khóa


Tài liệu tham khảo

Hanahan, D. & Weinberg, R. A. The hallmarks of cancer. Cell 100, 57–70 (2000).

Evan, G. I. & Vousden, K. H. Proliferation, cell cycle and apoptosis in cancer. Nature 411, 342–348 (2001).

Bissell, M. J. & Radisky, D. Outting tumours in context. Nature Rev. Cancer 1, 46–54 (2001).

Stoker, M. Gherardi, E., Perryman, M. & Gray, J. Scatter factor is a fibroblast-derived modulator of epithelial cell motility. Nature 327, 239–242 (1987).

Nakamura, T. et al. Molecular cloning and expression of human hepatocyte growth factor. Nature 342, 440–443 (1989).

Montesano, R., Matsumoto, K., Nakamura, T. & Orci, L. Identification of a fibroblast-derived epithelial morphogen as hepatocyte growth factor. Cell 67, 901–908 (1991).

Naldini, L. et al. Scatter factor and hepatocyte growth factor are indistinguishable ligands for the Met receptor. EMBO J. 10, 2867–2878 (1991).

Skeel, A. et al. Macrophage stimulating protein: purification, partial amino acid sequence, and cellular activity. J. Exp. Med. 173, 1227–1234 (1991).

Giordano, S., Ponzetto, C., Di Renzo, M. F., Cooper, C. S. & Comoglio, P. M. Tyrosine kinase receptor indistinguishable from the c-Met protein. Nature 339, 155–156 (1989).

Gaudino, G. et al. RON is a heterodimeric tyrosine kinase receptor activated by the HGF homologue MSP. EMBO J. 13, 3524–3532 (1994).

Wang, M. H. et al. Identification of the RON gene product as the receptor for the human macrophage stimulating protein. Science 266, 117–119 (1994).

Kolodkin, A. L., Matthes, D. J. & Goodman, C. S. The semaphorin genes encode a family of transmembrane and secreted growth cone guidance molecules. Cell 75, 1389–1399 (1993).

Winberg, M. L. et al. Plexin A is a neuronal semaphorin receptor that controls axon guidance. Cell 95, 903–916 (1998).

Tamagnone, L. et al. Plexins are a large family of receptors for transmembrane, secreted, and GPI-anchored semaphorins in vertebrates. Cell 99, 71–80 (1999).

Tamagnone, L. & Comoglio, P. M. Signalling by semaphorin receptors: cell guidance and beyond. Trends Cell Biol. 10, 377–383 (2000).

Montesano, R., Schaller, G. & Orci, L. Induction of epithelial tubular morphogenesis in vitro by fibroblast-derived soluble factors. Cell 66, 697–711 (1991).

Berdichevsky, F., Alford, D., Souza B. & Taylor-Papadimitriou, J. Branching morphogenesis of human mammary epithelial cells in collagen gels. J. Cell Sci. 107, 3557–3568 (1994).

Soriano, J. V., Pepper, M. S., Nakamura, T., Orci, L. & Montesano, R. Hepatocyte growth factor stimulates extensive development of branching duct-like structures by cloned mammary gland epithelial cells. J. Cell Sci. 108, 413–430 (1995).

Niemann, C. et al. Reconstitution of mammary gland development in vitro: requirement of c-Met and c-ErbB2 signaling for branching and alveolar morphogenesis. J. Cell Biol. 143, 533–545 (1998).Shows that HGF promotes the formation of branched tubules in mouse mammary epithelial cells that are cultured in matrigel, as well as in human mammary carcinoma tissue, in explant culture. The same morphogenetic response can be observed following transfection of GAB1, MET's main intracellular substrate.

Brinkmann, V., Foroutan, H., Sachs, H., Weidner, K. M. & Birchmeier, W. Hepatocyte growth factor/scatter factor induces a variety of tissue specific morphogenic programs in epithelial cells. J. Cell Biol. 131, 1573–1586 (1995).

Bussolino, F. et al. Hepatocyte growth factor is a potent angiogenic factor which stimulates endothelial cell motility and growth. J. Cell Biol. 119, 629–640 (1992).

Schmidt, C. et al. Scatter factor/hepatocyte growth factor is essential for liver development. Nature 373, 699–702 (1995).

Uehara, Y. et al. Placental defect and embryonal lethality in mice lacking hepatocyte growth factor/scatter factor. Nature 373, 702–705 (1995).

Bladt, F., Riethmacher, D., Isenmann, S., Aguzzi, A. & Birchmeier, C. Essential role for the c-Met receptor in the migration of myogenic precursor cells into the limb bud. Nature 376, 768–771 (1995).

Yu, T. W. & Bargmann, C. I. Dynamic regulation of axon guidance. Nature Neurosci. 4, 1169–1176 (2001).

Ebens, A. et al. Hepatocyte growth factor/scatter factor is an axonal chemoattractant and a neurotrophic factor for spinal motor neurons. Neuron 17, 1157–1172 (1996).

Wong, V. et al. Hepatocyte growth factor promotes motor neuron survival and synergizes with ciliary neurotrophic factor. J. Biol. Chem. 272, 5187–5191 (1997).

Yamamoto, Y. et al. Hepatocyte growth factor (HGF/SF) is a muscle-derived survival factor for a subpopulation of embryonic motoneurons. Development 124, 2903–2913 (1997).

Maina, F., Hilton, M. C., Ponzetto, C., Davies, A. M. & Klein, R. Met receptor signaling is required for sensory nerve development and HGF promotes axonal growth and survival of sensory neurons. Genes Dev. 11, 3341–3350 (1997).

Maina, F. et al. Multiple roles for hepatocyte growth factor in sympathetic neuron development. Neuron 20, 835–846 (1998).

Luo, Y., Raible, D. & Raper, J. A. Collapsin: a protein in brain that induces the collapse and paralysis of neuronal growth cones. Cell 75, 217–227 (1993).

Wong, J. T., Wong, S. T. & O'Connor, T. P. Ectopic semaphorin-1a functions as an attractive guidance cue for developing peripheral neurons. Nature Neurosci. 2, 798–803 (1999).

de Castro, F., Hu, L., Drabkin, H., Sotelo, C. & Chedotal, A. Chemoattraction and chemorepulsion of olfactory bulb axons by different secreted semaphorins. J. Neurosci. 19, 4428–4436 (1999).

Polleux, F., Morrow, T. & Ghosh, A. Semaphorin 3A is a chemoattractant for cortical apical dendrites. Nature 404, 567–573 (2000).

Miao, H. Q. et al. Neuropilin-1 mediates collapsin-1/semaphorin III inhibition of endothelial cell motility: functional competition of collapsin-1 and vascular endothelial growth factor-165. J. Cell Biol. 146, 233–242 (1999).

Cooper, C. S. et al. Molecular cloning of a new transforming gene from a chemically transformed human cell line. Nature 311, 29–33 (1984).

Rong, S., Segal, S., Anver, M., Resau, J. H. & Vande Woude, G. F. Invasiveness and metastasis of NIH3T3 cells induced by Met-hepatocyte growth factor/scatter factor autocrine stimulation. Proc. Natl Acad. Sci. USA 91, 4731–4735 (1994).

Bellusci, S. et al. Creation of an hepatocyte growth factor/scatter factor autocrine loop in carcinoma cells induces invasive properties associated with increased tumorigenicity. Oncogene 9, 1091–1099 (1994).

Jeffers, M., Rong, S., Anver, M. & Vande Woude, G. F. Autocrine hepatocyte growth factor/scatter factor signalling induces transformation and the invasive/metastatic phenotype in C127 cells. Oncogene 13, 853–861 (1996).

Meiners, S., Brinkmann, V., Naundorf, H. & Birchmeier, W. Role of morphogenetic factors in metastasis of mammary carcinoma cells. Oncogene 16, 9–20 (1998).

Liang, T. J., Reid, A. E., Xavier, R., Cardiff, R. D. & Wang, T. C. Transgenic expression of Tpr–Met oncogene leads to development of mammary hyperplasia and tumors. J. Clin. Invest. 97, 2872–2877 (1996).

Jeffers, M. et al. The mutationally activated Met receptor mediates motility and metastasis. Proc. Natl Acad. Sci. USA 95, 14417–14422 (1998).

Wang, R., Ferrell, L. D., Faouzi, S., Maher, J. J. & Bishop, M. J. Activation of the Met receptor by cell attachment induces and sustains hepatocellular carcinomas in transgenic mice. J. Cell Biol. 153, 1023–1034 (2001).The first in vivo demonstration that transgenic overexpression of wild-type Met in hepatocytes of mice allows HGF-independent activation of the receptor, leading to development of hepatocellular carcinomas. Inactivation of the transgene results in regression of even highly advanced tumours.

Takayama, H. et al. Diverse tumorigenesis associated with aberrant development in mice overexpressing hepatocyte growth factor/scatter factor. Proc. Natl Acad. Sci. USA 94, 701–706 (1997).

Otsuka, T. et al. c-Met autocrine activation induces development of malignant melanoma and acquisition of the metastatic phenotype. Cancer Res. 58, 5157–5167 (1998).

Ferracini, R. et al. 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 (1995).

Ferracini, R. et al. Retrogenic expression of the MET proto-oncogene correlates with the invasive phenotype of human rhabdomyosarcomas. Oncogene 12, 1697–1705 (1996).

Scotlandi, K. et al. Expression of Met/hepatocyte growth factor receptor gene and malignant behavior of musculoskeletal tumors. Am. J. Pathol. 149, 1209–1219 (1996).

Di Renzo, M. F. et al. Overexpression of the c-MET/HGF receptor gene in human thyroid carcinomas. Oncogene 7, 2549–2553 (1992).

Di Renzo, M. F. et al. Overexpression of the MET/HGF receptor in ovarian cancer. Int. J. Cancer 58, 658–662 (1994).

Di Renzo, M. F., Poulsom, R., Olivero, M., Comoglio, P. M. & Lemoine, N. R. Expression of the Met/hepatocyte growth factor receptor in human pancreatic cancer. Cancer Res. 55, 1129–1138 (1995).

Humphrey, P. A. et al. Hepatocyte growth factor and its receptor (c-MET) in prostatic carcinoma. Am. J. Pathol. 147, 386–396 (1995).

Natali, P. G. et al. Overexpression of the MET/HGF receptor in renal cell carcinomas. Int. J. Cancer 69, 212–217 (1996).

Ruco, L. et al. Expression of Met protein in thyroid tumours. J. Pathol. 180, 266–270 (1996).

Tuck, A. B., Park, M., Sterns, E. E., Boag, A. & Elliott, B. E. Coexpression of hepatocyte growth factor and receptor (Met) in human breast carcinoma. Am. J. Pathol. 148, 225–232 (1996).

Ueki, T., Fujimoto, J., Suzuki, T., Yamamoto, H. & Okamoto, E. Expression of hepatocyte growth factor and its receptor, the c-Met proto-oncogene, in hepatocellular carcinoma. Hepatology 25, 619–623 (1997).

Jin, L. et al. Expression of scatter factor and c-met receptor in benign and malignant breast tissue. Cancer 79, 749–760 (1997).

Toniguchi, K. et al. The relation between the growth patterns of gastric carcinoma and the expression of hepatocyte growth factor receptor (c-Met), autocrine motility factor receptor, and urokinase-type plasminogen activator receptor. Cancer 82, 2112–2122 (1998).

Porte, H. et al. Overexpression of stromelysin-3, BM-40/SPARC, and MET genes in human esophageal carcinoma: implications for prognosis. Clin. Cancer Res. 4, 1375–1382 (1998).

Zanetti, A. et al. Expression of Met protein and urokinase-type plasminogen activator receptor (uPA-R) in papillary carcinoma of the thyroid. J. Pathol. 186, 287–291 (1998).

Camp, R. L., Rimm, E. B. & Rimm, D. L. Met expression is associated with poor outcome in patients with axillary lymph node negative breast carcinoma. Cancer 86, 2259–2265 (1999).

Chen, B. K. et al. Overexpression of c-Met protein in human thyroid tumors correlated with lymph node metastasis and clinicopathologic state. Pathol. Res. Pract. 195, 427–433 (1999).

Tavian, D. et al. U-PA and c-MET mRNA expression is co-ordinately enhanced while hepatocyte growth factor mRNA is down-regulated in human hepatocellular carcinoma. Int. J. Cancer 87, 644–649 (2000).

Wielenga, V. J. et al. Expression of c-MET and heparan-sulfate proteoglycan forms of CD44 in colorectal cancer. Am. J. Pathol. 157, 1563–1573 (2000).

Ramirez, R. et al. Over-expression of hepatocyte growth factor/scatter factor (HGF/SF) and the HGF/SF receptor (c-MET) are associated with a high risk of metastasis and recurrence for children and young adults with papillary thyroid carcinoma. Clin. Endocrinol. 53, 635–644 (2000).

Edakuni, G., Sasatomi, E., Satoh, T., Tokunaga, O. & Miyazaki, K. Expression of the hepatocyte growth factor/ c-Met pathway is increased at the cancer front in breast carcinoma. Pathol. Int. 51, 172–178 (2001).

Tapper, J. et al. Changes in gene expression during progression of ovarian carcinoma. Cancer Genet. Cytogenet. 128, 1–6 (2001).

Huang, T. J., Wang, J. Y., Lin, S. R., Lian, S. T. & Hsieh, J. S. Overexpression of the c-Met protooncogene in human gastric carcinoma — correlation to clinical features. Acta Oncol. 40, 638–643 (2001).

Takeo, S. et al. Examination of oncogene amplification by genomic DNA microarray in hepatocellular carcinomas: comparison with comparative genomic hybridisation analysis. Cancer Genet. Cytogenet. 130, 127–132 (2001).

Morello, S. et al. MET receptor is overexpressed but not mutated in oral squamous cell carcinomas. J. Cell. Physiol. 189, 285–290 (2001).

Huang, Y. et al. Gene expression in papillary thyroid carcinoma reveals highly consistent profiles. Proc. Natl Acad. Sci. USA 98, 15044–15049 (2001).

Schmidt, L. et al. Germline and somatic mutations in the tyrosine kinase domain of the MET proto-oncogene in papillary renal carcinomas. Nature Genet. 16, 68–73 (1997).The first report of naturally occurring oncogenic mutations of MET in humans. Missense mutations were identified that are located in the tyrosine kinase domain of the MET gene in the germ line of patients who suffer from hereditary papillary renal-cell carcinomas and in a subset of sporadic papillary renal carcinomas.

Fischer, J. et al. Duplication and overexpression of the mutant allele of the MET proto-oncogene in multiple hereditary papillary renal cell tumours. Oncogene 17, 733–739 (1998).

Schmidt, L. et al. Novel mutations of the MET proto-oncogene in papillary renal carcinomas. Oncogene 18, 2343–2350 (1999).

Olivero, M. et al. Novel mutation in the ATP-binding site of the MET oncogene tyrosine kinase in a HPRCC family. Int. J. Cancer 82, 640–643 (1999).

Park, W. S. et al. Somatic mutations in the kinase domain of the MET/hepatocyte growth factor receptor gene in childhood hepatocellular carcinomas. Cancer Res. 59, 307–310 (1999).

Lee, J. H. et al. A novel germ line juxtamembrane MET mutation in human gastric cancer. Oncogene 19, 4947–4953 (2000).

Jeffers, M. et al. Activating mutations for the MET tyrosine kinase receptor in human cancer. Proc. Natl Acad. Sci. USA 94, 11445–11450 (1997).

Michieli, P. et al. Mutant Met-mediated transformation is ligand-dependent and can be inhibited by HGF antagonists. Oncogene 18, 5221–5231 (1999).Shows that the transforming potential displayed by mutant forms of MET found in human cancer is not only sensitive to, but entirely contingent on, the presence of HGF. This finding indicates that mutant MET-driven tumour development relies on local availability and tissue distribution of active HGF and provides proof-of-concept for the treatment of MET-dependent neoplasms by HGF antagonists.

Yao, Y. et al. Scatter factor protein levels in human breast cancers: clinicopathological and biological correlations. Am. J. Pathol. 149, 1707–1717 (1996).

Di Renzo, M. F. et al. Overexpression and amplification of the MET/HGF receptor gene during the progression of colorectal cancer. Clin. Cancer Res. 1, 147–154 (1995).

Di Renzo, M. F. et al. Somatic mutations of the MET oncogene are selected during metastatic spread of human HNSC carcinomas. Oncogene 19, 1547–1555 (2000).The first report of a direct involvement of MET in tumour metastasis in humans. Neoplastic cells that harbour activating mutations of the MET gene undergo clonal expansion during the metastatic spreading of head and neck squamous-cell carcinomas.

Eagles, G. et al. Hepatocyte growth factor/scatter factor is present in most pleural effusion fluids from cancer patients. Br. J. Cancer 73, 377–381 (1996).

Nagafuchi, A. Molecular architecture of adherens junctions. Curr. Opin. Cell Biol. 13, 600–603 (2001).

Tannapfel, A., Yasui, W., Yokozaki, H., Wittekind, C. & Tahara, E. Effect of hepatocyte growth factor on the expression of E- and P-cadherin in gastric carcinoma cell lines. Virchows Arch. 425, 139–144 (1994).

Miura, H. et al. Effects of hepatocyte growth factor on E-cadherin-mediated cell–cell adhesion in DU145 prostate cancer cells. Urology 58, 1064–1069 (2001).

Balkovetz, D. F., Pollack, A. L. & Mostov, K. E. Hepatocyte growth factor alters the polarity of Madin–Darby canine kidney cell monolayers. J. Biol. Chem. 272, 3471–3477 (1997).

Balkovetz, D. F. & Sambandam, V. Dynamics of E-cadherin and γ-catenin complexes during dedifferentiation of polarized MDCK cells. Kidney Int. 56, 910–921 (1999).

Davies, G., Jiang, W. G. & Mason, M. D. Matrilysin mediates extracellular cleavage of E-cadherin from prostate cancer cells: a key mechanism in hepatocyte growth factor/scatter factor-induced cell–cell dissociation and in vitro invasion. Clin. Cancer Res. 7, 3289–3297 (2001).

Shibamoto, S. et al. Tyrosine phosphorylation of β-catenin and plakoglobin enhanced by hepatocyte growth factor and epidermal growth factor in human carcinoma cells. Cell Adhes. Commun. 1, 295–305 (1994).

Frisch, S. M. & Screaton, R. A. Anoikis mechanisms. Curr. Opin. Cell Biol. 13, 555–562 (2001).

Plow, E. F., Haas, T. A., Zhang, L., Loftus, J. & Smith, J. W. Ligand binding to integrins. J. Biol. Chem. 275, 21785–21788 (2000).

Woods, A. & Couchman, J. R. Integrin modulation by lateral association. J. Biol. Chem. 275, 24233–24236 (2000).

Nebe, B., Sanftleben, H., Pommerenke, H., Peters, A. & Rychly, J. Hepatocyte growth factor enables enhanced integrin-cytoskeleton linkage by affecting integrin expression in subconfluent epithelial cells. Exp. Cell Res. 243, 263–273 (1998).

Liang, C. C. & Chen, H. C. Sustained activation of extracellular signal-regulated kinase stimulated by hepatocyte growth factor leads to integrin α2 expression that is involved in cell scattering. J. Biol. Chem. 276, 21146–21152 (2001).

Trusolino, L. et al. Growth factor-dependent activation of αvβ3 integrin in normal epithelial cells: implications for tumor invasion. J. Cell Biol. 142, 1145–1156 (1998).

Trusolino, L. et al. HGF/scatter factor selectively promotes cell invasion by increasing integrin avidity. FASEB J. 14, 1629–1640 (2000).

Brooks, P. C. et al. Localization of matrix metalloproteinase MMP-2 to the surface of invasive cells by interaction with integrin αvβ Cell 85, 683–693 (1996).

Giannelli, G., Falk-Marzillier, J., Schiraldi, O., Stetler-Stevenson, W. G. & Quaranta, V. Induction of cell migration by matrix metalloprotease-2 cleavage of laminin-5. Science 277, 225–228 (1997).

Rosenthal, E. L. et al. Role of the plasminogen activator and matrix metalloproteinase systems in epidermal growth factor- and scatter factor-stimulated invasion of carcinoma cells. Cancer Res. 58, 5221–5230 (1998).

Nabeshima, K. et al. Front-cell-specific expression of membrane-type 1 matrix metalloproteinase and gelatinase A during cohort migration of colon carcinoma cells induced by hepatocyte growth factor/scatter factor. Cancer Res. 60, 3364–3369 (2000).

Monvoisin, A. et al. Involvement of matrix metalloproteinase type-3 in hepatocyte growth factor-induced invasion of human hepatocellular carcinoma cells. Int. J. Cancer 97, 157–162 (2002).

Carmeliet, P. Mechanisms of angiogenesis and arteriogenesis. Nature Med. 6, 389–395 (2000).

Martin-Satue, M. & Blanco, J. Identification of semaphorin E gene expression in metastatic human lung adenocarcinoma cells by mRNA differential display. J. Surg. Oncol. 72, 18–23 (1999).

Yamada, T., Endo, R., Gotoh, M. & Hirohashi, S. Identification of semaphorin E as a non-MDR drug resistance gene of human cancer. Proc. Natl Acad. Sci. USA 94, 14713–14718 (1997).

Christensen, C. R. et al. Transcription of a novel mouse semaphorin gene, M-semaH, correlates with the metastatic ability of mouse tumor cell lines. Cancer Res. 58, 1238–1244 (1998).

Schlessinger, J. Cell signaling by receptor tyrosine kinases. Cell 103, 211–225 (2000).

Ponzetto, C. et al. A multifunctional docking site mediates signaling and transformation by the hepatocyte growth factor/scatter factor receptor family. Cell 77, 261–271 (1994).

Pelicci, G. et al. The motogenic and mitogenic responses to HGF are amplified by the Shc adaptor protein. Oncogene 10, 1631–1638 (1995).

Weidner, K. M. et al. Interaction between Gab1 and the c-Met receptor tyrosine kinase is responsible for epithelial morphogenesis. Nature 384, 173–176 (1996).

Gual, P. et al. Sustained recruitment of phospholipase c-γ to Gab1 is required for HGF-induced branching tubulogenesis. Oncogene 19, 1509–1518 (2000).

Maroun, C. R., Naujokas, M. A., Holgado-Madruga, M., Wong, A. J. & Park, M. The tyrosine phosphatase SHP-2 is required for sustained activation of extracellular signal-regulated kinase and epithelial morphogenesis downstream from the met receptor tyrosine kinase. Mol. Cell. Biol. 20, 8513–8525 (2000).

Schaeper, U. et al. Coupling of Gab1 to c-Met, Grb2, and Shp2 mediates biological responses. J. Cell Biol. 149, 1419–1432 (2000).

Boccaccio, C. et al. Induction of epithelial tubules by growth factor HGF depends on the STAT pathway. Nature 391, 285–288 (1998).

Bardelli, A. et al. Uncoupling signal transducers from oncogenic MET mutants abrogates cell transformation and inhibits invasive growth. Proc. Natl Acad. Sci. USA 95, 14379–14383 (1998).

Maina, F. et al. Uncoupling of Grb2 from the Met receptor in vivo reveals complex roles in muscle development. Cell 87, 531–542 (1996).

Sachs, M. et al. Motogenic and morphogenic activity of epithelial receptor tyrosine kinases. J. Cell Biol. 133, 1095–1107 (1996).

Giordano, S. et al. A point mutation in the MET oncogene abrogates metastasis without affecting transformation. Proc. Natl Acad. Sci. USA 94, 13868–13872 (1997).

Bardelli, A. et al. Concomitant activation of pathways downstream of Grb2 and PI3-kinase is required for MET-mediated metastasis. Oncogene 18, 1139–1146 (1999).

Trusolino, L., Bertotti, A. & Comoglio, P. M. A signaling adapter function for α6β4 integrin in the control of HGF-dependent invasive growth. Cell 107, 643–654 (2001).

Peschard, P. et al. Mutation of the c-Cbl TKB domain binding site on the Met receptor tyrosine kinase converts it into a transforming protein. Mol. Cell 8, 995–1004 (2001).A new mechanism of MET-dependent oncogenic transformation. The c-CBL adaptor protein binds a juxtamembrane tyrosine residue on MET and drives it to ubiquitin-mediated proteasomal degradation. A MET receptor in which this tyrosine is replaced by phenylalanine does not undergo polyubiquitylation and displays transforming activity in fibroblasts and epithelial cells.

Petrelli, A. et al. The endophilin/CIN85/CBL complex mediates ligand-dependent down-regulation of c-Met. Nature 416, 187–190 (2002).

Brodin, L., Low, P. & Shupliakov, O. Sequential steps in clathrin-mediated synaptic vesicle endocytosis. Curr. Opin. Neurobiol. 10, 312–320 (2000).

Winberg, M. L. et al. The transmembrane protein Off-Track associates with plexins and functions downstream of semaphorin signaling during axon guidance. Neuron 32, 53–62 (2001).

Luo, L. RHO–GTPases in neuronal morphogenesis. Nature Rev. Neurosci. 1, 173–180 (2000).

Dickson, B. J. RHO–GTPases in growth cone guidance. Curr. Opin. Neurobiol. 11, 103–110 (2001).

Rohm, B., Rahim, B., Kleiber, B., Hovatta, I. & Pueschel, A. W. The semaphorin 3A receptor may directly regulate the activity of small GTPases. FEBS Lett. 486, 68–72 (2000).

Vikis, H. G., Li, W., He, Z. & Guan, K.-L. The semaphorin receptor plexin-B1 specifically interacts with active Rac in a ligand-dependent manner. Proc. Natl Acad. Sci. USA 97, 12457–12462 (2000).

Driessens, M. H. et al. Plexin-B semaphorin receptors interact directly with active Rac and regulate the actin cytoskeleton by activating Rho. Curr. Biol. 11, 339–344 (2001).

Hu, H., Marton, T. F. & Goodman, C. S. Plexin B mediates axon guidance in Drosophila by simultaneously inhibiting active Rac and enhancing RhoA signalling. Neuron 32, 39–51 (2001).

Simon, M. A. Receptor tyrosine kinases: specific outcomes from general signals. Cell 103, 13–15 (2000).

Pawson, T. & Saxton, T. M. Signaling networks — do all roads lead to the same genes? Cell 97, 675–678 (1999).

Maina, F. et al. Coupling Met to specific pathways results in distinct developmental outcomes. Mol. Cell 7, 1293–1306 (2001).Addresses, in vivo , the issue of whether the specificity of tyrosine-kinase-receptor-dependent responses is determined by qualitative or quantitative differences in signalling outputs. Knockin Met mutants with optimal PI3K or Src binding motifs result in loss of function, but display different phenotypes and rescue of specific cell types, indicating that specific signalling pathways are necessary to achieve specific biological responses.

Karihaloo, A., O'Rourke, D. A., Nickel, C. H., Spokes, K. & Cantley, L. G. Differential MAPK pathways utilized for HGF- and EGF-dependent renal epithelial morphogenesis. J. Biol. Chem. 276, 9166–9173 (2001).

Boccaccio, C., Andò, M. & Comoglio, P. M. A differentiation switch for genetically modified hepatocytes. FASEB J. 16, 120–122 (2002).

Chan, A. M. et al. Identification of a competitive HGF antagonist encoded by an alternative transcript. Science 254, 1382–1385 (1991).

Hartmann, G. et al. A functional domain in the heavy chain of scatter factor/hepatocyte growth factor binds the c-Met receptor and induces cell dissociation but not mitogenesis. Proc. Natl Acad. Sci. USA 89, 11574–11578 (1992).

Lokker, N. A. et al. Structure–function analysis of hepatocyte growth factor: identification of variants that lack mitogenic activity yet retain high affinity receptor binding. EMBO J. 11, 2503–2510 (1992).

Cioce, V. et al. Hepatocyte growth factor (HGF)/NK1 is a naturally occurring HGF/scatter factor variant with partial agonist/antagonist activity. J. Biol. Chem. 271, 13110–13115 (1996).

Waltz, S. E. et al. Functional characterization of domains contained in hepatocyte growth factor-like protein. J. Biol. Chem. 272, 30526–30537 (1997).

Matsumoto, K., Kataoka, H., Date, K. & Nakamura, T. Cooperative interaction between α- and β-chains of hepatocyte growth factor on c-Met receptor confers ligand-induced receptor tyrosine phosphorylation and multiple biological responses. J. Biol. Chem. 273, 22913–22920 (1998).

Danilkovitch, A., Miller, M. & Leonard, E. J. Interaction of macrophage-stimulating protein with its receptor. Residues critical for β-chain binding and evidence for independent alpha chain binding. J. Biol. Chem. 274, 29937–29943 (1999).

Michieli, P. et al. An HGF-MSP chimaera disassociates the trophic properties of scatter factors from their pro-invasive activity. Nature Biotechnol. (in the press).

Kawaida, K., Matsumoto, K., Shimazu, H. & Nakamura, T. Hepatocyte growth factor prevents acute renal failure and accelerates renal regeneration in mice. Proc. Natl Acad. Sci. USA 91, 4357–4361 (1994).

Tsubouchi, H. et al. Clinical significance of human hepatocyte growth factor in blood from patients with fulminant hepatic failure. Hepatology 9, 875–881 (1989).

Yaekashi, M. et al. Simultaneous or delayed administration of hepatocyte growth factor (HGF) equally repress the fibrotic changes in murine lung injury by bleomycin: a morphological study. Am. J. Respir. Clin. Care Med. 156, 1937–1944 (1997).

Ueki, T. et al. Hepatocyte growth factor gene therapy of liver cirrhosis in rats. Nature Med. 5, 226–230 (1999).An example of how the beneficial trophic properties of HGF can be exploited for therapeutic applications. In a rat model of lethal liver cirrhosis, transduction of skeletal muscles with the human HGF gene increases HGF plasma levels and produces the complete resolution of fibrosis in the cirrhotic livers, thereby improving the survival rate of rats.

Kuba, K. et al. HGF/NK4, a four-kringle antagonist of hepatocyte growth factor, is an angiogenesis inhibitor that suppresses tumor growth and metastasis in mice. Cancer Res. 60, 6737–6743 (2000).

Cao, B. et al. Neutralizing monoclonal antibodies to hepatocyte growth factor/scatter factor (HGF/SF) display antitumor activity in animal models. Proc. Natl Acad. Sci. USA 98, 7443–7448 (2001).

Abounader, R. et al. In vivo targeting of SF/HGF and c-MET expression via U1snRNA/ribozymes inhibits glioma growth and angiogenesis and promotes apoptosis. FASEB J. 16, 108–110 (2002).

The Semaphorin Nomenclature Committee. Unified nomenclature for the semaphorin/collapsins. Cell 97, 551–552 (1999).

Ponzetto, C. et al. c-Met is amplified but not mutated in a cell line with an activated Met tyrosine kinase. Oncogene 6, 553–559 (1991).