Neuropilin-1 promotes cirrhosis of the rodent and human liver by enhancing PDGF/TGF-β signaling in hepatic stellate cells

Journal of Clinical Investigation

Volumn 120, Issue 7, 2010, Pages 2379-2394

  Cao, Sheng ^a   Yaqoob, Usman ^a   Das, Amitava ^a   Shergill, Uday ^a   Jagavelu, Kumaravelu ^a   Huebert, Robert C ^a   Routray, Chittaranjan ^a   Abdelmoneim, Soha ^a   Vasdev, Meher ^a   Leof, Edward ^b   Charlton, Michael ^a   Watts, Ryan J ^c   Mukhopadhyay, Debabrata ^b   Shah, Vijay H ^a  

^a MAYO CLINIC   (United States)

^b MAYO GRADUATE SCHOOL   (United States)

^c GENENTECH INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NEUROPILIN 1; PLATELET DERIVED GROWTH FACTOR; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; SMALL INTERFERING RNA; TRANSFORMING GROWTH FACTOR BETA; COLLAGEN; PLATELET DERIVED GROWTH FACTOR A; PLATELET-DERIVED GROWTH FACTOR A; SIGNAL PEPTIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BINDING AFFINITY; CELL MOTILITY; CHEMOTAXIS; CONTROLLED STUDY; DNA MODIFICATION; ENDOTHELIUM CELL; HEPATITIS C; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOPRECIPITATION; LIVER CIRRHOSIS; LIVER FIBROSIS; MYOFIBROBLAST; NONALCOHOLIC FATTY LIVER; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN LOCALIZATION; RAT; SIGNAL TRANSDUCTION; STELLATE CELL; UPREGULATION; ANIMAL; CELL CULTURE; CELL MOTION; DRUG EFFECT; EXTRACELLULAR MATRIX; FIBROSIS; LIVER; METABOLISM; MOUSE; PATHOLOGY; PHYSIOLOGY; RODENT;

ANIMALS; CELL MOVEMENT; CELLS, CULTURED; COLLAGEN; EXTRACELLULAR MATRIX; FIBROSIS; HEPATIC STELLATE CELLS; HUMANS; IMMUNOPRECIPITATION; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LIVER; LIVER CIRRHOSIS; MICE; NEUROPILIN-1; PLATELET-DERIVED GROWTH FACTOR; RECEPTOR, PLATELET-DERIVED GROWTH FACTOR BETA; RODENTIA; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA;

EID: 77954976056     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI41203     Document Type: Article

References (58)

1. Schuppan D, Afdhal NH. Liver cirrhosis. Lancet. 2008;371(9615):838-851.
2. Shah VH, Kamath PS. Portal hypertension and gastrointestinal bleeding. In Feldman M, Friedman LS, Brandt LJ, eds. Sleisenger and Fordtran's Gastrointestinal and Liver Disease. 8th ed. Philadelphia, Pennsylvania, USA: Elsevier Health Sciences; 2006:1899-1934.
3. Friedman SL. Mechanisms of hepatic fibrogenesis. Gastroenterology. 2008;134(6):1655-1669.
4. Rockey DC. Current and future anti-fibrotic therapies for chronic liver disease. Clin Liver Dis. 2008;12(4):939-962.
5. Jain R, Booth M. What brings pericytes to tumor vessels? J Clin Invest. 2003;112(8):1134-1136.
6. Lee JS, Semela D, Iredale J, Shah VH. Sinusoidal remodeling and angiogenesis: a new function for the liver-specific pericyte? Hepatology. 2007;45(3):817-825.
7. Claesson-Welsh L, et al. cDNA cloning and expression of a human platelet-derived growth factor (PDGF) receptor specific for B-chain-containing PDGF molecules. Mol Cell Biol. 1988;8(8):3476-3486.
8. Westermark B, Siegbahn A, Heldin CH, Claesson-Welsh L. B-type receptor for platelet-derived growth factor mediates a chemotactic response by means of ligand-induced activation of the receptor protein-tyrosine kinase. Proc Natl Acad Sci U S A. 1990;87(1):128-132. (Pubitemid 20033020)
9. Lai CC, Henningson C, DiMaio D. Bovine papillomavirus E5 protein induces oligomerization and trans-phosphorylation of the platelet-derived growth factor beta receptor. Proc Natl Acad Sci U S A. 1998;95(26):15241-15246. (Pubitemid 29018683)
10. Soriano P. Abnormal kidney development and hematological disorders in PDGF beta-receptor mutant mice. Genes Dev. 1994;8(16):1888-1896. (Pubitemid 24273889)
11. Abramsson A, Lindblom P, Betsholtz C. Endothelial and nonendothelial sources of PDGF-B regulate pericyte recruitment and influence vascular pattern formation in tumors. J Clin Invest. 2003;112(8):1142-1151. (Pubitemid 38056291)
12. Lindblom P, et al. Endothelial PDGF-B retention is required for proper investment of pericytes in the microvessel wall. Genes Dev. 2003;17(15):1835- 1840.
13. Wong L, Yamasaki G, Johnson RJ, Friedman SL. Induction of beta-platelet-derived growth factor receptor in rat hepatic lipocytes during cellular activation in vivo and in culture. J Clin Invest. 1994;94(4):1563-1569. (Pubitemid 2138802)
14. Friedman SL, Arthur MJ. Activation of cultured rat hepatic lipocytes by Kupffer cell conditioned medium. Direct enhancement of matrix synthesis and stimulation of cell proliferation via induction of platelet-derived growth factor receptors. J Clin Invest. 1989;84(6):1780-1785.
15. Iredale JP. Models of liver fibrosis: exploring the dynamic nature of inflammation and repair in a solid organ. J Clin Invest. 2007;117(3):539-548.
16. Kawasaki T, et al. A requirement for neuropilin-1 in embryonic vessel formation. Development. 1999;126(21):4895-4902.
17. Daniels C, et al. Imatinib mesylate inhibits the profibrogenic activity of TGF-beta and prevents bleomycin-mediated lung fibrosis. J Clin Invest. 2004;114(9):1308-1316. (Pubitemid 40385302)
18. Pan Q, et al. Blocking neuropilin-1 function has an additive effect with anti-VEGF to inhibit tumor growth. Cancer Cell. 2007;11(1):53-67.
19. Sancho-Bru P, et al. Genomic and functional characterization of stellate cells isolated from human cirrhotic livers. J Hepatol. 2005;43(2):272-282. (Pubitemid 40956880)
20. Hellerbrand C, Stefanovic B, Giordano F, Burchardt ER, Brenner DA. The role of TGFbeta1 in initiating hepatic stellate cell activation in vivo. J Hepatol. 1999;30(1):77-87. (Pubitemid 29023655)
21. Xu L, et al. Human hepatic stellate cell lines, LX-1 and LX-2: new tools for analysis of hepatic fibrosis. Gut. 2005;54(1):142-151.
22. Liu P, Ying Y, Ko YG, Anderson RG. Localization of platelet-derived growth factor-stimulated phosphorylation cascade to caveolae. J Biol Chem. 1996;271(17):10299-10303. (Pubitemid 26132521)
23. Veracini L, Franco M, Boureux A, Simon V, Roche S, Benistant C. Two distinct pools of Src family tyrosine kinases regulate PDGF-induced DNA synthesis and actin dorsal ruffles. J Cell Sci. 2006;119(pt 14):2921-2934. (Pubitemid 44177870)
24. Beardsley A, Fang K, Mertz H, Castranova V, Friend S, Liu J. Loss of caveolin-1 polarity impedes endothelial cell polarization and directional movement. J Biol Chem. 2005;280(5):3541-3547. (Pubitemid 40223819)
25. Greenberg JI, et al. A role for VEGF as a negative regulator of pericyte function and vessel maturation. Nature. 2008;456(7223):809-813.
26. Novo E, et al. Proangiogenic cytokines as hypoxia-dependent factors stimulating migration of human hepatic stellate cells. Am J Pathol. 2007;170(6):1942-1953. (Pubitemid 47339268)
27. Liu W, et al. Upregulation of neuropilin-1 by basic fibroblast growth factor enhances vascular smooth muscle cell migration in response to VEGF. Cytokine. 2005;32(5):206-212. (Pubitemid 43144652)
28. Gu C, et al. Neuropilin-1 conveys semaphorin and VEGF signaling during neural and cardiovascular development. Dev Cell. 2003;5(1):45-57. (Pubitemid 36827341)
29. Wang L, Zeng H, Wang P, Soker S, Mukhopadhyay D. Neuropilin-1-mediated vascular permeability factor/vascular endothelial growth factor-dependent endothelial cell migration. J Biol Chem. 2003;278(49):48848-48860.
30. Soker S, Takashima S, Miao HQ, Neufeld G, Klagsbrun M. Neuropilin-1 is expressed by endothelial and tumor cells as an isoform-specific receptor for vascular endothelial growth factor. Cell. 1998;92(6):735-745. (Pubitemid 28155313)
31. Andrae J, Gallini R, Betsholtz C. Role of plateletderived growth factors in physiology and medicine. Genes Dev. 2008;22(10):1276-1312. (Pubitemid 351717519)
32. De Donatis A, et al. Proliferation versus migra tion in platelet-derived growth factor signaling: the key role of endocytosis. J Biol Chem. 2008;283(29):19948-19956.
33. Sini P, Cannas A, Koleske AJ, Di Fiore PP, Scita G. Abl-dependent tyrosine phosphorylation of Sos-1 mediates growth-factor-induced Rac activation. Nat Cell Biol. 2004;6(3):268-274.
34. Rockey DC, Housset CN, Friedman SL. Activation-dependent contractility of rat hepatic lipocytes in culture and in vivo. J Clin Invest. 1993;92(4):1795-1804.
35. Semela D, Das A, Langer DA, Kang N, Leof E, Shah VH. Platelet-derived growth factor signaling through ephrin-B2 regulates hepatic vascular structure and function Gastroenterology. 2008;135(2):671-679.
36. Bataller R, Brenner DA. Liver fibrosis. J Clin Invest. 2005;115(2):209-218.
37. Kim WR, Brown RS Jr, Terrault NA, El-Serag H. Burden of liver disease in the United States: summary of a workshop. Hepatology. 2002;36(1):227-242. (Pubitemid 34700782)
38. Callewaert N, Van Vlierberghe H, Van Hecke A, Laroy W, Delanghe J, Contreras R. Noninvasive diagnosis of liver cirrhosis using DNA sequencer-based total serum protein glycomics. Nat Med. 2004;10(4):429-434. (Pubitemid 38508524)
39. Friedman SL. Reversibility of hepatic fibrosis and cirrhosis--is it all hype? Nat Clin Pract Gastroenterol Hepatol. 2007;4(5):236-237.
40. He Z, Tessier-Lavigne M. Neuropilin is a receptor for the axonal chemorepellent Semaphorin III. Cell. 1997;90(4):739-751. (Pubitemid 27357965)
41. Bates D, et al. Neurovascular congruence results from a shared patterning mechanism that utilizes Semaphorin3A and Neuropilin-1. Dev Biol. 2003;255(1):77-98. (Pubitemid 36287142)
42. Banerjee S, et al. Breast cancer cells secreted platelet-derived growth factor-induced motility of vascular smooth muscle cells is mediated through neuropilin-1. Mol Carcinog. 2006;45(11):871-880. (Pubitemid 44646339)
43. Cai H, Reed RR. Cloning and characterization of neuropilin-1-interacting protein: a PSD-95/Dlg/ ZO-1 domain-containing protein that interacts with the cytoplasmic domain of neuropilin-1. J Neurosci. 1999;19(15):6519-6527.
44. Prahst C, et al. Neuropilin-1-VEGFR-2 complexing requires the PDZ-binding domain of neuropilin-1. J Biol Chem. 2008;283(37):25110-25114.
45. Kawamura H, et al. Neuropilin-1 in regulation of VEGF-induced activation of p38MAPK and endothelial cell organization. Blood. 2008;112(9):3638-3649.
46. Yan W, Bentley B, Shao R. Distinct angiogenic mediators are required for basic fibroblast growth factor- and vascular endothelial growth factor-induced angiogenesis: the role of cytoplasmic tyrosine kinase c-Abl in tumor angiogenesis. Mol Biol Cell. 2008;19(5):2278-2288.
47. Klagsbrun M, Takashima S, Mamluk R. The role of neuropilin in vascular and tumor biology. Adv Exp Med Biol. 2002;515:33-48. (Pubitemid 36324180)
48. Shintani Y, et al. Glycosaminoglycan modification of neuropilin-1 modulates VEGFR2 signaling. EMBO J. 2006;25(13):3045-3055.
49. Frankel P, et al. Chondroitin sulphate-modified neuropilin 1 is expressed in human tumour cells and modulates 3D invasion in the U87MG human glioblastoma cell line through a p130Cas-mediated pathway. EMBO Rep. 2008;9(10):983-989.
50. Taura K, et al. Hepatic stellate cells secrete angiopoietin 1 that induces angiogenesis in liver fibrosis. Gastroenterology. 2008;135(5):1729-1738.
51. Kalluri R, Zeisberg M. Fibroblasts in cancer. Nat Rev Cancer. 2006;6(5):392-401.
52. Lee J, Decker N, Chatterjee S, Yao J, Friedman S, Shah V. Mechanisms of nitric oxide interplay with Rho GTPase family members in modulation of actin membrane dynamics in pericytes and fibroblasts. Am J Pathol. 2005;166(6):1861-1870. (Pubitemid 40734408)
53. Kang-Decker N, et al. Nitric oxide promotes endothelial cell survival signaling through S-nitrosylation and activation of dynamin-2. J Cell Sci. 2007;120(pt 3):492-501. (Pubitemid 46332512)
54. Zeng H, Zhao D, Mukhopadhyay D. KDR stimulates endothelial cell migration through heterotrimeric G protein Gq/11-mediated activation of a small GTPase RhoA. J Biol Chem. 2002;277(48):46791-46798. (Pubitemid 35417683)
55. Chatterjee S, Cao S, Petersen T, Simari R, Shah V. Inhibition of GTP-dependent vesicle trafficking impairs internalization of plasmalemmal eNOS and cellular nitric oxide production. J Cell Sci. 2003;116(pt 17):3645-3655. (Pubitemid 37063407)
56. Das A, et al. Disruption of an SP2/KLF6 Repression complex by SHP is required for farnesoid X receptor-induced endothelial cell migration. J Biol Chem. 2006;281(51):39105-39113. (Pubitemid 46041869)
57. Prigozhina NL, Waterman-Storer CM. Decreased polarity and increased random motility in PtK1 epithelial cells correlate with inhibition of endosomal recycling. J Cell Sci. 2006;119(pt 17):3571-3582.
58. Langer D, et al. Nitric oxide promotes caspase independent hepatic stellate cell apoptosis through generation of reactive oxygen species. Hepatology. 2008;47(6):1983-1993. (Pubitemid 351945565)