Hepatocyte growth factor: A regulator of inflammation and autoimmunity

Autoimmunity Reviews

Volumn 14, Issue 4, 2015, Pages 293-303

  Molnarfi, Nicolas ^a,b   Benkhoucha, Mahdia ^a,b   Funakoshi, Hiroshi ^c   Nakamura, Toshikazu ^d   Lalive, Patrice H ^a,b  

^a UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

^b GENEVA UNIVERSITY HOSPITALS   (Switzerland)

^c ASAHIKAWA MEDICAL COLLEGE   (Japan)

^d Research and Development Inc   (Japan)

Author keywords

Autoimmune regulator; Autoimmunity; C Met; HGF; Inflammation; Therapy

Indexed keywords

SCATTER FACTOR; SCATTER FACTOR RECEPTOR;

ALLERGIC AIRWAY INFLAMMATION; AMINO TERMINAL SEQUENCE; ANTIGEN SPECIFICITY; ASTHMA; AUTOIMMUNE DISEASE; AUTOIMMUNE MYOCARDITIS; AUTOIMMUNE NEUROINFLAMMATION; AUTOIMMUNE SIALOADENITIS; AUTOIMMUNITY; B LYMPHOCYTE; BIOLOGICAL ACTIVITY; CARDIAC ALLOGRAFT VASCULOPATHY; CHOLANGITIS; DENDRITIC CELL; DISEASE MODEL; GRAFT SURVIVAL; GRAFT VERSUS HOST REACTION; HEART DISEASE; HUMAN; INFLAMMATION; INFLAMMATORY BOWEL DISEASE; INFLAMMATORY DISEASE; KIDNEY DISEASE; LIVER DISEASE; LUNG DISEASE; LUPUS ERYTHEMATOSUS NEPHRITIS; MACROPHAGE; MONOCYTE; NATURAL KILLER CELL; NERVOUS SYSTEM INFLAMMATION; NEUTROPHIL; NONHUMAN; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN STRUCTURE; REVIEW; RHEUMATOID ARTHRITIS; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; ULCERATIVE COLITIS; ANIMAL; IMMUNOLOGY; METABOLISM; SIGNAL TRANSDUCTION;

ANIMALS; AUTOIMMUNITY; HEPATOCYTE GROWTH FACTOR; HUMANS; INFLAMMATION; SIGNAL TRANSDUCTION;

EID: 84923040341     PISSN: 15689972     EISSN: 18730183     Source Type: Journal    
DOI: 10.1016/j.autrev.2014.11.013     Document Type: Review

References (189)

1. Sonnenberg E., Meyer D., Weidner K.M., Birchmeier C. 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 1993, 123:223-235.
2. Stoker M., Gherardi E., Perryman M., Gray J. Scatter factor is a fibroblast-derived modulator of epithelial cell mobility. Nature 1987, 327:239-242.
3. Nakamura T., Nishizawa T., Hagiya M., Seki T., Shimonishi M., Sugimura A., et al. Molecular cloning and expression of human hepatocyte growth factor. Nature 1989, 342:440-443.
4. Montesano R., Matsumoto K., Nakamura T., Orci L. Identification of a fibroblast-derived epithelial morphogen as hepatocyte growth factor. Cell 1991, 67:901-908.
5. Berdichevsky F., Alford D., D'Souza B., Taylor-Papadimitriou J. Branching morphogenesis of human mammary epithelial cells in collagen gels. J Cell Sci 1994, 107(Pt 12):3557-3568.
6. 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 1995, 376:768-771.
7. Schmidt C., Bladt F., Goedecke S., Brinkmann V., Zschiesche W., Sharpe M., et al. Scatter factor/hepatocyte growth factor is essential for liver development. Nature 1995, 373:699-702.
8. Uehara Y., Minowa O., Mori C., Shiota K., Kuno J., Noda T., et al. Placental defect and embryonic lethality in mice lacking hepatocyte growth factor/scatter factor. Nature 1995, 373:702-705.
9. Nakamura T., Sakai K., Nakamura T., Matsumoto K. Hepatocyte growth factor twenty years on: much more than a growth factor. J Gastroenterol Hepatol 2011, 26(Suppl. 1):188-202.
10. Nakamura T., Nawa K., Ichihara A. Partial purification and characterization of hepatocyte growth factor from serum of hepatectomized rats. Biochem Biophys Res Commun 1984, 122:1450-1459.
11. Michalopoulos G., Houck K.A., Dolan M.L., Leutteke N.C. Control of hepatocyte replication by two serum factors. Cancer Res 1984, 44:4414-4419.
12. Zarnegar R., Michalopoulos G.K. The many faces of hepatocyte growth factor: from hepatopoiesis to hematopoiesis. J Cell Biol 1995, 129:1177-1180.
13. Weidner K.M., Arakaki N., Hartmann G., Vandekerckhove J., Weingart S., Rieder H., et al. Evidence for the identity of human scatter factor and human hepatocyte growth factor. Proc Natl Acad Sci U S A 1991, 88:7001-7005.
14. Rubin J.S., Osada H., Finch P.W., Taylor W.G., Rudikoff S., Aaronson S.A. Purification and characterization of a newly identified growth factor specific for epithelial cells. Proc Natl Acad Sci U S A 1989, 86:802-806.
15. Ebens A., Brose K., Leonardo E.D., Hanson M.G., Bladt F., Birchmeier C., et al. Hepatocyte growth factor/scatter factor is an axonal chemoattractant and a neurotrophic factor for spinal motor neurons. Neuron 1996, 17:1157-1172.
16. Shima N., Itagaki Y., Nagao M., Yasuda H., Morinaga T., Higashio K. A fibroblast-derived tumor cytotoxic factor/F-TCF (hepatocyte growth factor/HGF) has multiple functions in vitro. Cell Biol Int Rep 1991, 15:397-408.
17. Donate L.E., Gherardi E., Srinivasan N., Sowdhamini R., Aparicio S., Blundell T.L. Molecular evolution and domain structure of plasminogen-related growth factors (HGF/SF and HGF1/MSP). Protein Sci 1994, 3:2378-2394.
18. Han S., Stuart L.A., Degen S.J. 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 1991, 30:9768-9780.
19. Skeel A., Yoshimura T., Showalter S.D., Tanaka S., Appella E., Leonard E.J. Macrophage stimulating protein: purification, partial amino acid sequence, and cellular activity. J Exp Med 1991, 173:1227-1234.
20. Bolanos-Garcia V.M. MET meet adaptors: functional and structural implications in downstream signalling mediated by the Met receptor. Mol Cell Biochem 2005, 276:149-157.
21. Nakamura T. Structure and function of hepatocyte growth factor. Prog Growth Factor Res 1991, 3:67-85.
22. Lee S.L., Dickson R.B., Lin C.Y. Activation of hepatocyte growth factor and urokinase/plasminogen activator by matriptase, an epithelial membrane serine protease. J Biol Chem 2000, 275:36720-36725.
23. Herter S., Piper D.E., Aaron W., Gabriele T., Cutler G., Cao P., et al. Hepatocyte growth factor is a preferred in vitro substrate for human hepsin, a membrane-anchored serine protease implicated in prostate and ovarian cancers. Biochem J 2005, 390:125-136.
24. Birchmeier C., Gherardi E. Developmental roles of HGF/SF and its receptor, the c-Met tyrosine kinase. Trends Cell Biol 1998, 8:404-410.
25. Matsumoto K., Kataoka H., Date K., Nakamura T. Cooperative interaction between alpha- and beta-chains of hepatocyte growth factor on c-Met receptor confers ligand-induced receptor tyrosine phosphorylation and multiple biological responses. J Biol Chem 1998, 273:22913-22920.
26. Seki T., Hagiya M., Shimonishi M., Nakamura T., Shimizu S. Organization of the human hepatocyte growth factor-encoding gene. Gene 1991, 102:213-219.
27. Bottaro D.P., Rubin J.S., Faletto D.L., Chan A.M., Kmiecik T.E., Vande Woude G.F., et al. Identification of the hepatocyte growth factor receptor as the c-met proto-oncogene product. Science 1991, 251:802-804.
28. Chen P., Xie H., Sekar M.C., Gupta K., Wells A. Epidermal growth factor receptor-mediated cell motility: phospholipase C activity is required, but mitogen-activated protein kinase activity is not sufficient for induced cell movement. J Cell Biol 1994, 127:847-857.
29. Ponzetto C., Bardelli A., Zhen Z., Maina F., dalla Zonca P., Giordano S., et al. A multifunctional docking site mediates signaling and transformation by the hepatocyte growth factor/scatter factor receptor family. Cell 1994, 77:261-271.
30. Pelicci G., Giordano S., Zhen Z., Salcini A.E., Lanfrancone L., Bardelli A., et al. The motogenic and mitogenic responses to HGF are amplified by the Shc adaptor protein. Oncogene 1995, 10:1631-1638.
31. Graziani A., Gramaglia D., Cantley L.C., Comoglio P.M. The tyrosine-phosphorylated hepatocyte growth factor/scatter factor receptor associates with phosphatidylinositol 3-kinase. J Biol Chem 1991, 266:22087-22090.
32. Boccaccio C., Ando M., Tamagnone L., Bardelli A., Michieli P., Battistini C., et al. Induction of epithelial tubules by growth factor HGF depends on the STAT pathway. Nature 1998, 391:285-288.
33. Weidner K.M., Behrens J., Vandekerckhove J., Birchmeier W. Scatter factor: molecular characteristics and effect on the invasiveness of epithelial cells. J Cell Biol 1990, 111:2097-2108.
34. Gual P., Giordano S., Williams T.A., Rocchi S., Van Obberghen E., Comoglio P.M. Sustained recruitment of phospholipase C-gamma to Gab1 is required for HGF-induced branching tubulogenesis. Oncogene 2000, 19:1509-1518.
35. Gaudino G., Follenzi A., Naldini L., Collesi C., Santoro M., Gallo K.A., et al. RON is a heterodimeric tyrosine kinase receptor activated by the HGF homologue MSP. EMBO J 1994, 13:3524-3532.
36. Crepaldi T., Gautreau A., Comoglio P.M., Louvard D., Arpin M. Ezrin is an effector of hepatocyte growth factor-mediated migration and morphogenesis in epithelial cells. J Cell Biol 1997, 138:423-434.
37. Trusolino L., Bertotti A., Comoglio P.M. A signaling adapter function for alpha6beta4 integrin in the control of HGF-dependent invasive growth. Cell 2001, 107:643-654.
38. Orian-Rousseau V., Chen L., Sleeman J.P., Herrlich P., Ponta H. CD44 is required for two consecutive steps in HGF/c-Met signaling. Genes Dev 2002, 16:3074-3086.
39. Wang X., DeFrances M.C., Dai Y., Pediaditakis P., Johnson C., Bell A., et al. A mechanism of cell survival: sequestration of Fas by the HGF receptor Met. Mol Cell 2002, 9:411-421.
40. Giordano S., Corso S., Conrotto P., Artigiani S., Gilestro G., Barberis D., et al. The semaphorin 4D receptor controls invasive growth by coupling with Met. Nat Cell Biol 2002, 4:720-724.
41. Matteucci E., Ridolfi E., Desiderio M.A. Hepatocyte growth factor differently influences Met-E-cadherin phosphorylation and downstream signaling pathway in two models of breast cells. Cell Mol Life Sci 2006, 63:2016-2026.
42. Prat M., Crepaldi T., Gandino L., Giordano S., Longati P., Comoglio P. C-terminal truncated forms of Met, the hepatocyte growth factor receptor. Mol Cell Biol 1991, 11:5954-5962.
43. Galvani A.P., Cristiani C., Carpinelli P., Landonio A., Bertolero F. Suramin modulates cellular levels of hepatocyte growth factor receptor by inducing shedding of a soluble form. Biochem Pharmacol 1995, 50:959-966.
44. Wajih N., Walter J., Sane D.C. Vascular origin of a soluble truncated form of the hepatocyte growth factor receptor (c-met). Circ Res 2002, 90:46-52.
45. Petrelli A., Circosta P., Granziero L., Mazzone M., Pisacane A., Fenoglio S., et al. Ab-induced ectodomain shedding mediates hepatocyte growth factor receptor down-regulation and hampers biological activity. Proc Natl Acad Sci U S A 2006, 103:5090-5095.
46. Athauda G., Giubellino A., Coleman J.A., Horak C., Steeg P.S., Lee M.J., et al. c-Met ectodomain shedding rate correlates with malignant potential. Clin Cancer Res 2006, 12:4154-4162.
47. Zhang Y.W., Graveel C., Shinomiya N., Vande Woude G.F. Met decoys: will cancer take the bait?. Cancer Cell 2004, 6:5-6.
48. Kmiecik T.E., Keller J.R., Rosen E., Vande Woude G.F. Hepatocyte growth factor is a synergistic factor for the growth of hematopoietic progenitor cells. Blood 1992, 80:2454-2457.
49. Nishino T., Hisha H., Nishino N., Adachi M., Ikehara S. Hepatocyte growth factor as a hematopoietic regulator. Blood 1995, 85:3093-3100.
50. Yu C.Z., Hisha H., Li Y., Lian Z., Nishino T., Toki J., et al. Stimulatory effects of hepatocyte growth factor on hemopoiesis of SCF/c-kit system-deficient mice. Stem Cells 1998, 16:66-77.
51. Futamatsu H., Suzuki J., Mizuno S., Koga N., Adachi S., Kosuge H., et al. Hepatocyte growth factor ameliorates the progression of experimental autoimmune myocarditis: a potential role for induction of T helper 2 cytokines. Circ Res 2005, 96:823-830.
52. Skibinski G., Skibinska A., James K. The role of hepatocyte growth factor and its receptor c-met in interactions between lymphocytes and stromal cells in secondary human lymphoid organs. Immunology 2001, 102:506-514.
53. Takai K., Hara J., Matsumoto K., Hosoi G., Osugi Y., Tawa A., et al. Hepatocyte growth factor is constitutively produced by human bone marrow stromal cells and indirectly promotes hematopoiesis. Blood 1997, 89:1560-1565.
54. Tamura S., Sugawara T., Tokoro Y., Taniguchi H., Fukao K., Nakauchi H., et al. Expression and function of c-Met, a receptor for hepatocyte growth factor, during T-cell development. Scand J Immunol 1998, 47:296-301.
55. van der Voort R., Taher T.E., Keehnen R.M., Smit L., Groenink M., Pals S.T. Paracrine regulation of germinal center B cell adhesion through the c-met-hepatocyte growth factor/scatter factor pathway. J Exp Med 1997, 185:2121-2131.
56. Matsumoto K., Okazaki H., Nakamura T. Up-regulation of hepatocyte growth factor gene expression by interleukin-1 in human skin fibroblasts. Biochem Biophys Res Commun 1992, 188:235-243.
57. Matsumoto K., Tajima H., Okazaki H., Nakamura T. Negative regulation of hepatocyte growth factor gene expression in human lung fibroblasts and leukemic cells by transforming growth factor-beta 1 and glucocorticoids. J Biol Chem 1992, 267:24917-24920.
58. Inaba M., Koyama H., Hino M., Okuno S., Terada M., Nishizawa Y., et al. Regulation of release of hepatocyte growth factor from human promyelocytic leukemia cells, HL-60, by 1,25-dihydroxyvitamin D3, 12-O-tetradecanoylphorbol 13-acetate, and dibutyryl cyclic adenosine monophosphate. Blood 1993, 82:53-59.
59. Galimi F., Cottone E., Vigna E., Arena N., Boccaccio C., Giordano S., et al. Hepatocyte growth factor is a regulator of monocyte-macrophage function. J Immunol 2001, 166:1241-1247.
60. Rutella S., Bonanno G., Procoli A., Mariotti A., de Ritis D.G., Curti A., et al. Hepatocyte growth factor favors monocyte differentiation into regulatory interleukin (IL)-10++IL-12low/neg accessory cells with dendritic-cell features. Blood 2006, 108:218-227.
61. Moghul A., Lin L., Beedle A., Kanbour-Shakir A., DeFrances M.C., Liu Y., et al. Modulation of c-MET proto-oncogene (HGF receptor) mRNA abundance by cytokines and hormones: evidence for rapid decay of the 8kb c-MET transcript. Oncogene 1994, 9:2045-2052.
62. Beilmann M., Odenthal M., Jung W., Vande Woude G.F., Dienes H.P., Schirmacher P. Neoexpression of the c-met/hepatocyte growth factor-scatter factor receptor gene in activated monocytes. Blood 1997, 90:4450-4458.
63. Kurz S.M., Diebold S.S., Hieronymus T., Gust T.C., Bartunek P., Sachs M., et al. The impact of c-met/scatter factor receptor on dendritic cell migration. Eur J Immunol 2002, 32:1832-1838.
64. Baek J.H., Birchmeier C., Zenke M., Hieronymus T. The HGF receptor/Met tyrosine kinase is a key regulator of dendritic cell migration in skin immunity. J Immunol 2012, 189:1699-1707.
65. Okunishi K., Dohi M., Nakagome K., Tanaka R., Mizuno S., Matsumoto K., et al. A novel role of hepatocyte growth factor as an immune regulator through suppressing dendritic cell function. J Immunol 2005, 175:4745-4753.
66. Kuroiwa T., Iwasaki T., Imado T., Sekiguchi M., Fujimoto J., Sano H. Hepatocyte growth factor prevents lupus nephritis in a murine lupus model of chronic graft-versus-host disease. Arthritis Res Ther 2006, 8:R123.
67. Okunishi K., Dohi M., Fujio K., Nakagome K., Tabata Y., Okasora T., et al. Hepatocyte growth factor significantly suppresses collagen-induced arthritis in mice. J Immunol 2007, 179:5504-5513.
68. Benkhoucha M., Santiago-Raber M.L., Schneiter G., Chofflon M., Funakoshi H., Nakamura T., et al. Hepatocyte growth factor inhibits CNS autoimmunity by inducing tolerogenic dendritic cells and CD25+ Foxp3+ regulatory T cells. Proc Natl Acad Sci U S A 2010, 107:6424-6429.
69. Singhal E., Kumar P., Sen P. A novel role for Bruton's tyrosine kinase in hepatocyte growth factor-mediated immunoregulation of dendritic cells. J Biol Chem 2011, 286:32054-32063.
70. Singhal E., Sen P. Hepatocyte growth factor-induced c-Src-phosphatidylinositol 3-kinase-AKT-mammalian target of rapamycin pathway inhibits dendritic cell activation by blocking IkappaB kinase activity. Int J Biochem Cell Biol 2011, 43:1134-1146.
71. Chen Q., DeFrances M.C., Zarnegar R. Induction of met proto-oncogene (hepatocyte growth factor receptor) expression during human monocyte-macrophage differentiation. Cell Growth Differ 1996, 7:821-832.
72. Beilmann M., Vande Woude G.F., Dienes H.P., Schirmacher P. Hepatocyte growth factor-stimulated invasiveness of monocytes. Blood 2000, 95:3964-3969.
73. Jiang Q., Azuma E., Tanaka M., Kobayashi M., Hirayama M., Kumamoto T., et al. Differential responsiveness of cord and adult blood monocytes to hepatocyte growth factor. Clin Exp Immunol 2001, 125:222-228.
74. Moransard M., Sawitzky M., Fontana A., Suter T. Expression of the HGF receptor c-met by macrophages in experimental autoimmune encephalomyelitis. Glia 2010, 58:559-571.
75. Yamada Y., Saito S., Morikawa H. Hepatocyte growth factor in human breast milk. Am J Reprod Immunol 1998, 40:112-120.
76. Sakai T., Satoh K., Matsushima K., Shindo S., Abe S., Abe T., et al. Hepatocyte growth factor in bronchoalveolar lavage fluids and cells in patients with inflammatory chest diseases of the lower respiratory tract: detection by RIA and in situ hybridization. Am J Respir Cell Mol Biol 1997, 16:388-397.
77. Morimoto K., Amano H., Sonoda F., Baba M., Senba M., Yoshimine H., et al. Alveolar macrophages that phagocytose apoptotic neutrophils produce hepatocyte growth factor during bacterial pneumonia in mice. Am J Respir Cell Mol Biol 2001, 24:608-615.
78. Flaquer M., Franquesa M., Vidal A., Bolanos N., Torras J., Lloberas N., et al. Hepatocyte growth factor gene therapy enhances infiltration of macrophages and may induce kidney repair in db/db mice as a model of diabetes. Diabetologia 2012, 55:2059-2068.
79. Coudriet G.M., He J., Trucco M., Mars W.M., Piganelli J.D. Hepatocyte growth factor modulates interleukin-6 production in bone marrow derived macrophages: implications for inflammatory mediated diseases. PLoS One 2010, 5:e15384.
80. Kusunoki H., Taniyama Y., Otsu R., Rakugi H., Morishita R. Anti-inflammatory effects of hepatocyte growth factor on the vicious cycle of macrophages and adipocytes. Hypertens Res 2014, 37:500-506.
81. Chen P.M., Liu K.J., Hsu P.J., Wei C.F., Bai C.H., Ho L.J., et al. Induction of immunomodulatory monocytes by human mesenchymal stem cell-derived hepatocyte growth factor through ERK1/2. J Leukoc Biol 2014, 96:295-303.
82. Scarpino S., Stoppacciaro A., Ballerini F., Marchesi M., Prat M., Stella M.C., et al. Papillary carcinoma of the thyroid: hepatocyte growth factor (HGF) stimulates tumor cells to release chemokines active in recruiting dendritic cells. Am J Pathol 2000, 156:831-837.
83. Benkhoucha M., Molnarfi N., Dunand-Sauthier I., Merkler D., Schneiter G., Bruscoli S., et al. Hepatocyte growth factor limits autoimmune neuroinflammation via glucocorticoid-induced leucine zipper expression in dendritic cells. J Immunol 2014, 193:2743-2752.
84. Molnarfi N., Benkhoucha M., Juillard C., Bjarnadottir K., Lalive P.H. The neurotrophic hepatocyte growth factor induces protolerogenic human dendritic cells. J Neuroimmunol 2014, 267:105-110.
85. Corinti S., Albanesi C., la Sala A., Pastore S., Girolomoni G. Regulatory activity of autocrine IL-10 on dendritic cell functions. J Immunol 2001, 166:4312-4318.
86. Berrebi D., Bruscoli S., Cohen N., Foussat A., Migliorati G., Bouchet-Delbos L., et al. Synthesis of glucocorticoid-induced leucine zipper (GILZ) by macrophages: an anti-inflammatory and immunosuppressive mechanism shared by glucocorticoids and IL-10. Blood 2003, 101:729-738.
87. Ayroldi E., Migliorati G., Bruscoli S., Marchetti C., Zollo O., Cannarile L., et al. Modulation of T-cell activation by the glucocorticoid-induced leucine zipper factor via inhibition of nuclear factor kappaB. Blood 2001, 98:743-753.
88. Hamdi H., Godot V., Maillot M.C., Prejean M.V., Cohen N., Krzysiek R., et al. Induction of antigen-specific regulatory T lymphocytes by human dendritic cells expressing the glucocorticoid-induced leucine zipper. Blood 2007, 110:211-219.
89. Cohen N., Mouly E., Hamdi H., Maillot M.C., Pallardy M., Godot V., et al. GILZ expression in human dendritic cells redirects their maturation and prevents antigen-specific T lymphocyte response. Blood 2006, 107:2037-2044.
90. Di Nicola M., Carlo-Stella C., Magni M., Milanesi M., Longoni P.D., Matteucci P., et al. Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood 2002, 99:3838-3843.
91. Adams D.H., Harvath L., Bottaro D.P., Interrante R., Catalano G., Tanaka Y., et al. Hepatocyte growth factor and macrophage inflammatory protein 1 beta: structurally distinct cytokines that induce rapid cytoskeletal changes and subset-preferential migration in T cells. Proc Natl Acad Sci U S A 1994, 91:7144-7148.
92. Benkhoucha M., Molnarfi N., Schneiter G., Walker P.R., Lalive P.H. The neurotrophic hepatocyte growth factor attenuates CD8+ cytotoxic T-lymphocyte activity. J Neuroinflammation 2013, 10:154.
93. Zhou D., Tan R.J., Lin L., Zhou L., Liu Y. Activation of hepatocyte growth factor receptor, c-met, in renal tubules is required for renoprotection after acute kidney injury. Kidney Int 2013, 84:509-520.
94. Delaney B., Koh W.S., Yang K.H., Strom S.C., Kaminski N.E. Hepatocyte growth factor enhances B-cell activity. Life Sci 1993, 53:L89-L93.
95. Gordin M., Tesio M., Cohen S., Gore Y., Lantner F., Leng L., et al. c-Met and its ligand hepatocyte growth factor/scatter factor regulate mature B cell survival in a pathway induced by CD74. J Immunol 2010, 185:2020-2031.
96. Tjin E.P., Bende R.J., Derksen P.W., van Huijstee A.P., Kataoka H., Spaargaren M., et al. Follicular dendritic cells catalyze hepatocyte growth factor (HGF) activation in the germinal center microenvironment by secreting the serine protease HGF activator. J Immunol 2005, 175:2807-2813.
97. Weimar I.S., de Jong D., Muller E.J., Nakamura T., van Gorp J.M., de Gast G.C., et al. Hepatocyte growth factor/scatter factor promotes adhesion of lymphoma cells to extracellular matrix molecules via alpha 4 beta 1 and alpha 5 beta 1 integrins. Blood 1997, 89:990-1000.
98. Jiang W., Puntis M.C., Nakamura T., Hallett M.B. Neutrophil priming by hepatocyte growth factor, a novel cytokine. Immunology 1992, 77:147-149.
99. Mine S., Tanaka Y., Suematu M., Aso M., Fujisaki T., Yamada S., et al. Hepatocyte growth factor is a potent trigger of neutrophil adhesion through rapid activation of lymphocyte function-associated antigen-1. Lab Invest 1998, 78:1395-1404.
100. Falenta K., Rodaway A., Jones G.E., Wells C.M. Imaging haematopoietic cells recruitment to an acute wound in vivo identifies a role for c-Met signalling. J Microsc 2013, 250:200-209.
101. Grenier A., Chollet-Martin S., Crestani B., Delarche C., El Benna J., Boutten A., et al. Presence of a mobilizable intracellular pool of hepatocyte growth factor in human polymorphonuclear neutrophils. Blood 2002, 99:2997-3004.
102. McCourt M., Wang J.H., Sookhai S., Redmond H.P. Activated human neutrophils release hepatocyte growth factor/scatter factor. Eur J Surg Oncol 2001, 27:396-403.
103. Matsushima A., Ogura H., Koh T., Fujita K., Yoshiya K., Sumi Y., et al. Hepatocyte growth factor in polymorphonuclear leukocytes is increased in patients with systemic inflammatory response syndrome. J Trauma 2004, 56:259-264.
104. Francavilla A., Vujanovic N.L., Polimeno L., Azzarone A., Iacobellis A., Deleo A., et al. The in vivo effect of hepatotrophic factors augmenter of liver regeneration, hepatocyte growth factor, and insulin-like growth factor-II on liver natural killer cell functions. Hepatology 1997, 25:411-415.
105. Yukioka K., Inaba M., Furumitsu Y., Yukioka M., Nishino T., Goto H., et al. Levels of hepatocyte growth factor in synovial fluid and serum of patients with rheumatoid arthritis and release of hepatocyte growth factor by rheumatoid synovial fluid cells. J Rheumatol 1994, 21:2184-2189.
106. Feuerherm A.J., Borset M., Seidel C., Sundan A., Leistad L., Ostensen M., et al. Elevated levels of osteoprotegerin (OPG) and hepatocyte growth factor (HGF) in rheumatoid arthritis. Scand J Rheumatol 2001, 30:229-234.
107. Grandaunet B., Syversen S.W., Hoff M., Sundan A., Haugeberg G., van Der Heijde D., et al. Association between high plasma levels of hepatocyte growth factor and progression of radiographic damage in the joints of patients with rheumatoid arthritis. Arthritis Rheum 2011, 63:662-669.
108. Koch A.E., Halloran M.M., Hosaka S., Shah M.R., Haskell C.J., Baker S.K., et al. Hepatocyte growth factor. A cytokine mediating endothelial migration in inflammatory arthritis. Arthritis Rheum 1996, 39:1566-1575.
109. Nagashima M., Hasegawa J., Kato K., Yamazaki J., Nishigai K., Ishiwata T., et al. Hepatocyte growth factor (HGF), HGF activator, and c-Met in synovial tissues in rheumatoid arthritis and osteoarthritis. J Rheumatol 2001, 28:1772-1778.
110. Paleolog E.M. Angiogenesis in rheumatoid arthritis. Arthritis Res 2002, 4(Suppl. 3):S81-S90.
111. Bendinelli P., Matteucci E., Dogliotti G., Corsi M.M., Banfi G., Maroni P., et al. Molecular basis of anti-inflammatory action of platelet-rich plasma on human chondrocytes: mechanisms of NF-kappaB inhibition via HGF. J Cell Physiol 2010, 225:757-766.
112. Bai L., Lennon D.P., Caplan A.I., DeChant A., Hecker J., Kranso J., et al. Hepatocyte growth factor mediates mesenchymal stem cell-induced recovery in multiple sclerosis models. Nat Neurosci 2012, 15:862-879.
113. Molnarfi N., Benkhoucha M., Bjarnadottir K., Juillard C., Lalive P.H. Interferon-beta induces hepatocyte growth factor in monocytes of multiple sclerosis patients. PLoS One 2012, 7:e49882.
114. Muller A.M., Jun E., Conlon H., Sadiq S.A. Cerebrospinal hepatocyte growth factor levels correlate negatively with disease activity in multiple sclerosis. J Neuroimmunol 2012, 251:80-86.
115. Yamaura K., Ito K., Tsukioka K., Wada Y., Makiuchi A., Sakaguchi M., et al. Suppression of acute and chronic rejection by hepatocyte growth factor in a murine model of cardiac transplantation: induction of tolerance and prevention of cardiac allograft vasculopathy. Circulation 2004, 110:1650-1657.
116. Saiura A., Mataki C., Murakami T., Umetani M., Wada Y., Kohro T., et al. A comparison of gene expression in murine cardiac allografts and isografts by means DNA microarray analysis. Transplantation 2001, 72:320-329.
117. Oku M., Okumi M., Shimizu A., Sahara H., Setoyama K., Nishimura H., et al. Hepatocyte growth factor sustains T regulatory cells and prolongs the survival of kidney allografts in major histocompatibility complex-inbred CLAWN-miniature swine. Transplantation 2012, 93:148-155.
118. Kuroiwa T., Kakishita E., Hamano T., Kataoka Y., Seto Y., Iwata N., et al. Hepatocyte growth factor ameliorates acute graft-versus-host disease and promotes hematopoietic function. J Clin Invest 2001, 107:1365-1373.
119. Imado T., Iwasaki T., Kataoka Y., Kuroiwa T., Hara H., Fujimoto J., et al. Hepatocyte growth factor preserves graft-versus-leukemia effect and T-cell reconstitution after marrow transplantation. Blood 2004, 104:1542-1549.
120. Gong R., Rifai A., Tolbert E.M., Centracchio J.N., Dworkin L.D. Hepatocyte growth factor modulates matrix metalloproteinases and plasminogen activator/plasmin proteolytic pathways in progressive renal interstitial fibrosis. J Am Soc Nephrol 2003, 14:3047-3060.
121. Inoue T., Okada H., Kobayashi T., Watanabe Y., Kanno Y., Kopp J.B., et al. Hepatocyte growth factor counteracts transforming growth factor-beta1, through attenuation of connective tissue growth factor induction, and prevents renal fibrogenesis in 5/6 nephrectomized mice. FASEB J 2003, 17:268-270.
122. Dworkin L.D., Gong R., Tolbert E., Centracchio J., Yano N., Zanabli A.R., et al. Hepatocyte growth factor ameliorates progression of interstitial fibrosis in rats with established renal injury. Kidney Int 2004, 65:409-419.
123. Yang J., Liu Y. Blockage of tubular epithelial to myofibroblast transition by hepatocyte growth factor prevents renal interstitial fibrosis. J Am Soc Nephrol 2002, 13:96-107.
124. Mizuno S., Matsumoto K., Nakamura T. Hepatocyte growth factor suppresses interstitial fibrosis in a mouse model of obstructive nephropathy. Kidney Int 2001, 59:1304-1314.
125. Mizuno S., Nakamura T. Suppressions of chronic glomerular injuries and TGF-beta 1 production by HGF in attenuation of murine diabetic nephropathy. Am J Physiol Renal Physiol 2004, 286:F134-F143.
126. Gong R., Rifai A., Dworkin L.D. Anti-inflammatory effect of hepatocyte growth factor in chronic kidney disease: targeting the inflamed vascular endothelium. J Am Soc Nephrol 2006, 17:2464-2473.
127. Gong R., Rifai A., Dworkin L.D. Hepatocyte growth factor suppresses acute renal inflammation by inhibition of endothelial E-selectin. Kidney Int 2006, 69:1166-1174.
128. Gong R., Rifai A., Ge Y., Chen S., Dworkin L.D. Hepatocyte growth factor suppresses proinflammatory NFkappaB activation through GSK3beta inactivation in renal tubular epithelial cells. J Biol Chem 2008, 283:7401-7410.
129. Gong R., Rifai A., Tolbert E.M., Biswas P., Centracchio J.N., Dworkin L.D. Hepatocyte growth factor ameliorates renal interstitial inflammation in rat remnant kidney by modulating tubular expression of macrophage chemoattractant protein-1 and RANTES. J Am Soc Nephrol 2004, 15:2868-2881.
130. Daha M.R., van Kooten C. Is the proximal tubular cell a proinflammatory cell?. Nephrol Dial Transplant 2000, 15(Suppl. 6):41-43.
131. Giannopoulou M., Dai C., Tan X., Wen X., Michalopoulos G.K., Liu Y. Hepatocyte growth factor exerts its anti-inflammatory action by disrupting nuclear factor-kappaB signaling. Am J Pathol 2008, 173:30-41.
132. Homsi E., Janino P., Amano M., Saraiva Camara N.O. Endogenous hepatocyte growth factor attenuates inflammatory response in glycerol-induced acute kidney injury. Am J Nephrol 2009, 29:283-291.
133. Shimizu K., Taniyama Y., Sanada F., Azuma J., Iwabayashi M., Iekushi K., et al. Hepatocyte growth factor inhibits lipopolysaccharide-induced oxidative stress via epithelial growth factor receptor degradation. Arterioscler Thromb Vasc Biol 2012, 32:2687-2693.
134. Nakamura T., Mizuno S., Matsumoto K., Sawa Y., Matsuda H. Myocardial protection from ischemia/reperfusion injury by endogenous and exogenous HGF. J Clin Invest 2000, 106:1511-1519.
135. Ueda H., Nakamura T., Matsumoto K., Sawa Y., Matsuda H., Nakamura T. A potential cardioprotective role of hepatocyte growth factor in myocardial infarction in rats. Cardiovasc Res 2001, 51:41-50.
136. Urbanek K., Rota M., Cascapera S., Bearzi C., Nascimbene A., De Angelis A., et al. Cardiac stem cells possess growth factor-receptor systems that after activation regenerate the infarcted myocardium, improving ventricular function and long-term survival. Circ Res 2005, 97:663-673.
137. Tang Q., Shen D., Huang Z., Xiong R., Wu H., Huang J., et al. Potential role of N-cadherin in hepatocyte growth factor (HGF) mediated improvement of the cardiac function of dilated cardiomyopathy mice. Int J Cardiol 2008, 127:442-443.
138. Taniyama Y., Morishita R., Aoki M., Hiraoka K., Yamasaki K., Hashiya N., et al. Angiogenesis and antifibrotic action by hepatocyte growth factor in cardiomyopathy. Hypertension 2002, 40:47-53.
139. Srivastava M., Zurakowski D., Cheifetz P., Leichtner A., Bousvaros A. Elevated serum hepatocyte growth factor in children and young adults with inflammatory bowel disease. J Pediatr Gastroenterol Nutr 2001, 33:548-553.
140. Nishimura S., Takahashi M., Ota S., Hirano M., Hiraishi H. Hepatocyte growth factor accelerates restitution of intestinal epithelial cells. J Gastroenterol 1998, 33:172-178.
141. Tahara Y., Ido A., Yamamoto S., Miyata Y., Uto H., Hori T., et al. Hepatocyte growth factor facilitates colonic mucosal repair in experimental ulcerative colitis in rats. J Pharmacol Exp Ther 2003, 307:146-151.
142. Numata M., Ido A., Moriuchi A., Kim I., Tahara Y., Yamamoto S., et al. Hepatocyte growth factor facilitates the repair of large colonic ulcers in 2,4,6-trinitrobenzene sulfonic acid-induced colitis in rats. Inflamm Bowel Dis 2005, 11:551-558.
143. Arthur L.G., Kuenzler K.A., Schwartz M.Z. Hepatocyte growth factor ameliorates inflammatory bowel disease in a rat model. J Gastrointest Surg 2003, 7:1062-1068. [discussion 1068].
144. Arthur L.G., Schwartz M.Z., Kuenzler K.A., Birbe R. Hepatocyte growth factor treatment ameliorates diarrhea and bowel inflammation in a rat model of inflammatory bowel disease. J Pediatr Surg 2004, 39:139-143. [discussion 139-43].
145. Oh K., Iimuro Y., Takeuchi M., Kaneda Y., Iwasaki T., Terada N., et al. Ameliorating effect of hepatocyte growth factor on inflammatory bowel disease in a murine model. Am J Physiol Gastrointest Liver Physiol 2005, 288:G729-G735.
146. Katz M.S., Thatch K.A., Schwartz M.Z. Hepatocyte growth factor and omega-3-enriched feeds have a synergistic effect on mucosal mass in an animal model of inflammatory bowel disease. J Pediatr Surg 2012, 47:194-198.
147. Ohda Y., Hori K., Tomita T., Hida N., Kosaka T., Fukuda Y., et al. Effects of hepatocyte growth factor on rat inflammatory bowel disease models. Dig Dis Sci 2005, 50:914-921.
148. Ware L.B., Matthay M.A. Keratinocyte and hepatocyte growth factors in the lung: roles in lung development, inflammation, and repair. Am J Physiol Lung Cell Mol Physiol 2002, 282:L924-L940.
149. Yaekashiwa M., Nakayama S., Ohnuma K., Sakai T., Abe T., Satoh K., et al. Simultaneous or delayed administration of hepatocyte growth factor equally represses the fibrotic changes in murine lung injury induced by bleomycin. A morphologic study. Am J Respir Crit Care Med 1997, 156:1937-1944.
150. Watanabe M., Ebina M., Orson F.M., Nakamura A., Kubota K., Koinuma D., et al. Hepatocyte growth factor gene transfer to alveolar septa for effective suppression of lung fibrosis. Mol Ther 2005, 12:58-67.
151. Lee Y.J., Moon C., Lee S.H., Park H.J., Seoh J.Y., Cho M.S., et al. Apoptotic cell instillation after bleomycin attenuates lung injury through hepatocyte growth factor induction. Eur Respir J 2012, 40:424-435.
152. Shukla M.N., Rose J.L., Ray R., Lathrop K.L., Ray A., Ray P. Hepatocyte growth factor inhibits epithelial to myofibroblast transition in lung cells via Smad7. Am J Respir Cell Mol Biol 2009, 40:643-653.
153. Ito W., Kanehiro A., Matsumoto K., Hirano A., Ono K., Maruyama H., et al. Hepatocyte growth factor attenuates airway hyperresponsiveness, inflammation, and remodeling. Am J Respir Cell Mol Biol 2005, 32:268-280.
154. Chakraborty S., Chopra P., Hak A., Dastidar S.G., Ray A. Hepatocyte growth factor is an attractive target for the treatment of pulmonary fibrosis. Expert Opin Investig Drugs 2013, 22:499-515.
155. Roos F., Terrell T.G., Godowski P.J., Chamow S.M., Schwall R.H. Reduction of alpha-naphthylisothiocyanate-induced hepatotoxicity by recombinant human hepatocyte growth factor. Endocrinology 1992, 131:2540-2544.
156. Ishiki Y., Ohnishi H., Muto Y., Matsumoto K., Nakamura T. Direct evidence that hepatocyte growth factor is a hepatotrophic factor for liver regeneration and has a potent antihepatitis effect in vivo. Hepatology 1992, 16:1227-1235.
157. Molnar C., Garcia-Trevijano E.R., Ludwiczek O., Talabot D., Kaser A., Mato J.M., et al. Anti-inflammatory effects of hepatocyte growth factor: induction of interleukin-1 receptor antagonist. Eur Cytokine Netw 2004, 15:303-311.
158. Morita M., Watanabe Y., Akaike T. Protective effect of hepatocyte growth factor on interferon-gamma-induced cytotoxicity in mouse hepatocytes. Hepatology 1995, 21:1585-1593.
159. Kosai K., Matsumoto K., Nagata S., Tsujimoto Y., Nakamura T. Abrogation of Fas-induced fulminant hepatic failure in mice by hepatocyte growth factor. Biochem Biophys Res Commun 1998, 244:683-690.
160. Aguilar-Valenzuela R., Carlsen E.D., Liang Y., Soong L., Sun J. Hepatocyte growth factor in dampening liver immune-mediated pathology in acute viral hepatitis without compromising antiviral activity. J Gastroenterol Hepatol 2014, 29:878-886.
161. Michalopoulos G.K., Appasamy R. Metabolism of HGF-SF and its role in liver regeneration. EXS 1993, 65:275-283.
162. Ozeki M., Ishii T., Hirano Y., Tabata Y. Controlled release of hepatocyte growth factor from gelatin hydrogels based on hydrogel degradation. J Drug Target 2001, 9:461-471.
163. Oe S., Fukunaka Y., Hirose T., Yamaoka Y., Tabata Y. A trial on regeneration therapy of rat liver cirrhosis by controlled release of hepatocyte growth factor. J Control Release 2003, 88:193-200.
164. Liu F., Song Y., Liu D. Hydrodynamics-based transfection in animals by systemic administration of plasmid DNA. Gene Ther 1999, 6:1258-1266.
165. Yang J., Chen S., Huang L., Michalopoulos G.K., Liu Y. Sustained expression of naked plasmid DNA encoding hepatocyte growth factor in mice promotes liver and overall body growth. Hepatology 2001, 33:848-859.
166. Payne N.L., Dantanarayana A., Sun G., Moussa L., Caine S., McDonald C., et al. Early intervention with gene-modified mesenchymal stem cells overexpressing interleukin-4 enhances anti-inflammatory responses and functional recovery in experimental autoimmune demyelination. Cell Adh Migr 2012, 6:179-189.
167. Wang H., Yang Y.F., Zhao L., Xiao F.J., Zhang Q.W., Wen M.L., et al. Hepatocyte growth factor gene-modified mesenchymal stem cells reduce radiation-induced lung injury. Hum Gene Ther 2013, 24:343-353.
168. Zhang J., Middleton K.K., Fu F.H., Im H.J., Wang J.H. HGF mediates the anti-inflammatory effects of PRP on injured tendons. PLoS One 2013, 8:e67303.
169. Funakoshi H., Nakamura T. Hepatocyte growth factor (HGF): neurotrophic functions and therapeutic implications for neuronal injury/diseases. Curr Signal Transduct Ther 2011, 6:156-167.
170. Fleming J.C., Norenberg M.D., Ramsay D.A., Dekaban G.A., Marcillo A.E., Saenz A.D., et al. The cellular inflammatory response in human spinal cords after injury. Brain 2006, 129:3249-3269.
171. Ueki T., Kaneda Y., Tsutsui H., Nakanishi K., Sawa Y., Morishita R., et al. Hepatocyte growth factor gene therapy of liver cirrhosis in rats. Nat Med 1999, 5:226-230.
172. Mizuno S., Kurosawa T., Matsumoto K., Mizuno-Horikawa Y., Okamoto M., Nakamura T. Hepatocyte growth factor prevents renal fibrosis and dysfunction in a mouse model of chronic renal disease. J Clin Invest 1998, 101:1827-1834.
173. Dohi M., Hasegawa T., Yamamoto K., Marshall B.C. Hepatocyte growth factor attenuates collagen accumulation in a murine model of pulmonary fibrosis. Am J Respir Crit Care Med 2000, 162:2302-2307.
174. Yasuda H., Imai E., Shiota A., Fujise N., Morinaga T., Higashio K. Antifibrogenic effect of a deletion variant of hepatocyte growth factor on liver fibrosis in rats. Hepatology 1996, 24:636-642.
175. Mellado-Gil J., Rosa T.C., Demirci C., Gonzalez-Pertusa J.A., Velazquez-Garcia S., Ernst S., et al. Disruption of hepatocyte growth factor/c-Met signaling enhances pancreatic beta-cell death and accelerates the onset of diabetes. Diabetes 2011, 60:525-536.
176. da Silva C.G., Maccariello E.R., Wilson S.W., Putheti P., Daniel S., Damrauer S.M., et al. Hepatocyte growth factor preferentially activates the anti-inflammatory arm of NF-kappaB signaling to induce A20 and protect renal proximal tubular epithelial cells from inflammation. J Cell Physiol 2012, 227:1382-1390.
177. Min J.K., Lee Y.M., Kim J.H., Kim Y.M., Kim S.W., Lee S.Y., et al. Hepatocyte growth factor suppresses vascular endothelial growth factor-induced expression of endothelial ICAM-1 and VCAM-1 by inhibiting the nuclear factor-kappaB pathway. Circ Res 2005, 96:300-307.
178. Hanawa T., Suzuki K., Kawauchi Y., Takamura M., Yoneyama H., Han G.D., et al. Attenuation of mouse acute colitis by naked hepatocyte growth factor gene transfer into the liver. J Gene Med 2006, 8:623-635.
179. Jayasankar V., Woo Y.J., Bish L.T., Pirolli T.J., Chatterjee S., Berry M.F., et al. Gene transfer of hepatocyte growth factor attenuates postinfarction heart failure. Circulation 2003, 108(Suppl. 1):II230-II236.
180. Date I., Takagi N., Takagi K., Kago T., Matsumoto K., Nakamura T., et al. Hepatocyte growth factor attenuates cerebral ischemia-induced learning dysfunction. Biochem Biophys Res Commun 2004, 319:1152-1158.
181. 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 U S A 1994, 91:4357-4361.
182. Fiaschi-Taesch N.M., Santos S., Reddy V., Van Why S.K., Philbrick W.F., Ortega A., et al. Prevention of acute ischemic renal failure by targeted delivery of growth factors to the proximal tubule in transgenic mice: the efficacy of parathyroid hormone-related protein and hepatocyte growth factor. J Am Soc Nephrol 2004, 15:112-125.
183. Miller S.B., Martin D.R., Kissane J., Hammerman M.R. Hepatocyte growth factor accelerates recovery from acute ischemic renal injury in rats. Am J Physiol 1994, 266:F129-F134.
184. Bevan D., Gherardi E., Fan T.P., Edwards D., Warn R. Diverse and potent activities of HGF/SF in skin wound repair. J Pathol 2004, 203:831-838.
185. Fierabracci A. Recent insights into the role and molecular mechanisms of the autoimmune regulator (AIRE) gene in autoimmunity. Autoimmun Rev 2011, 10:137-143.
186. Romo-Tena J., Gomez-Martin D., Alcocer-Varela J. CTLA-4 and autoimmunity: new insights into the dual regulator of tolerance. Autoimmun Rev 2013, 12:1171-1176.
187. Gianchecchi E., Delfino D.V., Fierabracci A. Recent insights into the role of the PD-1/PD-L1 pathway in immunological tolerance and autoimmunity. Autoimmun Rev 2013, 12:1091-1100.
188. Miller M.A., Meyer A.S., Beste M.T., Lasisi Z., Reddy S., Jeng K.W., et al. ADAM-10 and -17 regulate endometriotic cell migration via concerted ligand and receptor shedding feedback on kinase signaling. Proc Natl Acad Sci U S A 2013, 110:E2074-E2083.
189. Lalive P.H., Paglinawan R., Biollaz G., Kappos E.A., Leone D.P., Malipiero U., Relvas J.B., Moransard M., Suter T., Fontana A. TGF-beta-treated microglia induce oligodendrocyte precursor cell chemotaxis through the HGF-c-Met pathway. Eur J Immunol 2005, 35:727-737.