Transforming growth factor β1-induced astrocyte migration is mediated in part by activating 5-lipoxygenase and cysteinyl leukotriene receptor 1

Journal of Neuroinflammation

Volumn 9, Issue , 2012, Pages

  Huang, Xue Qin ^a   Zhang, Xia Yan ^a   Wang, Xiao Rong ^a   Yu, Shu Ying ^a   Fang, San Hua ^a   Lu, Yun Bi ^a   Zhang, Wei Ping ^a   Wei, Er Qing ^a  

^a ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

5 lipoxygenase; Astrocyte; Cysteinyl leukotriene; Cysteinyl leukotriene receptor; Glial scar; Migration; Transforming growth factor 1

Indexed keywords

ARACHIDONATE 5 LIPOXYGENASE; CYSTEINYL LEUKOTRIENE RECEPTOR 1; CYSTEINYL LEUKOTRIENE RECEPTOR 2; LEUKOTRIENE C4; LEUKOTRIENE D4; LEUKOTRIENE RECEPTOR; LEUKOTRIENE RECEPTOR STIMULATING AGENT; MONTELUKAST; SMALL INTERFERING RNA; TRANSFORMING GROWTH FACTOR BETA1; TRANSFORMING GROWTH FACTOR BETA1 AGONIST; UNCLASSIFIED DRUG; ZILEUTON;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; ASTROCYTE; CELL ASSAY; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME ACTIVATION; NEWBORN; NONHUMAN; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; RAT; RECEPTOR DOWN REGULATION; RECEPTOR UPREGULATION;

EID: 84862651167     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/1742-2094-9-145     Document Type: Article

References (86)

1. Fawcett JW, Asher RA. The glial scar and central nervous system repair. Brain Res Bull 1999, 49:377-391. 10.1016/S0361-9230(99)00072-6, 10483914.
2. Saadoun S, Papadopoulos MC, Watanabe H, Yan D, Manley GT, Verkman AS. Involvement of aquaporin-4 in astroglial cell migration and glial scar formation. J Cell Sci 2005, 118:5691-5698. 10.1242/jcs.02680, 16303850.
3. Faber-Elman A, Lavie V, Schvartz I, Shaltiel S, Schwartz M. Vitronectin overrides a negative effect of TNF-alpha on astrocyte migration. FASEB J 1995, 9:1605-1613.
4. Striedinger K, Scemes E. Interleukin-1beta affects calcium signaling and in vitro cell migration of astrocyte progenitors. J Neuroimmunol 2008, 196:116-123. 10.1016/j.jneuroim.2008.03.014, 2453308, 18462808.
5. Miao H, Crabb AW, Hernandez MR, Lukas TJ. Modulation of factors affecting optic nerve head astrocyte migration. Invest Ophthalmol Vis Sci 2010, 51:4096-4103. 10.1167/iovs.10-5177, 2910642, 20375339.
6. Hsieh HL, Wang HH, Wu WB, Chu PJ, Yang CM. Transforming growth factor-beta1 induces matrix metalloproteinase-9 and cell migration in astrocytes: roles of ROS-dependent ERK- and JNK-NF-kappaB pathways. J Neuroinflammation 2010, 7:88. 10.1186/1742-2094-7-88, 3002339, 21134288.
7. Flanders KC, Ren RF, Lippa CF. Transforming growth factor-betas in neurodegenerative disease. Prog Neurobiol 1998, 54:71-85. 10.1016/S0301-0082(97)00066-X, 9460794.
8. Unsicker K, Strelau J. Functions of transforming growth factor-beta isoforms in the nervous system. Cues based on localization and experimental in vitro and in vivo evidence. Eur J Biochem 2000, 267:6972-6975. 10.1046/j.1432-1327.2000.01824.x, 11106405.
9. Bottner M, Krieglstein K, Unsicker K. The transforming growth factor-betas: structure, signaling, and roles in nervous system development and functions. J Neurochem 2000, 75:2227-2240.
10. Massague J. How cells read TGF-beta signals. Nat Rev Mol Cell Biol 2000, 1:169-178.
11. Vivien D, Ali C. Transforming growth factor-beta signalling in brain disorders. Cytokine Growth Factor Rev 2006, 17:121-128. 10.1016/j.cytogfr.2005.09.011, 16271500.
12. Leivonen SK, Kahari VM. Transforming growth factor-beta signaling in cancer invasion and metastasis. Int J Cancer 2007, 121:2119-2124. 10.1002/ijc.23113, 17849476.
13. Pratt BM, McPherson JM. TGF-beta in the central nervous system: potential roles in ischemic injury and neurodegenerative diseases. Cytokine Growth Factor Rev 1997, 8:267-292. 10.1016/S1359-6101(97)00018-X, 9620642.
14. Lehrmann E, Kiefer R, Christensen T, Toyka KV, Zimmer J, Diemer NH, Hartung HP, Finsen B. Microglia and macrophages are major sources of locally produced transforming growth factor-beta1 after transient middle cerebral artery occlusion in rats. Glia 1998, 24:437-448. 10.1002/(SICI)1098-1136(199812)24:4<437::AID-GLIA9>3.0.CO;2-X, 9814824.
15. Ruocco A, Nicole O, Docagne F, Ali C, Chazalviel L, Komesli S, Yablonsky F, Roussel S, MacKenzie ET, Vivien D, Buisson A. A transforming growth factor-beta antagonist unmasks the neuroprotective role of this endogenous cytokine in excitotoxic and ischemic brain injury. J Cereb Blood Flow Metab 1999, 19:1345-1353.
16. Samuelsson B, Dahlen SE, Lindgren JA, Rouzer CA, Serhan CN. Leukotrienes and lipoxins: structures, biosynthesis, and biological effects. Science 1987, 237:1171-1176. 10.1126/science.2820055, 2820055.
17. Kanaoka Y, Boyce JA. Cysteinyl leukotrienes and their receptors: cellular distribution and function in immune and inflammatory responses. J Immunol 2004, 173:1503-1510.
18. Wenzel SE. The role of leukotrienes in asthma. Prostaglandins Leukot Essent Fatty Acids 2003, 69:145-155. 10.1016/S0952-3278(03)00075-9, 12895597.
19. Vannella KM, McMillan TR, Charbeneau RP, Wilke CA, Thomas PE, Toews GB, Peters-Golden M, Moore BB. Cysteinyl leukotrienes are autocrine and paracrine regulators of fibrocyte function. J Immunol 2007, 179:7883-7890.
20. Brink C, Dahlen SE, Drazen J, Evans JF, Hay DW, Nicosia S, Serhan CN, Shimizu T, Yokomizo T. International union of pharmacology XXXVII. Nomenclature for leukotriene and lipoxin receptors. Pharmacol Rev 2003, 55:195-227. 10.1124/pr.55.1.8, 12615958.
21. Rovati GE, Capra V. Cysteinyl-leukotriene receptors and cellular signals. Scientific World Journal 2007, 7:1375-1392.
22. Fang SH, Zhou Y, Chu LS, Zhang WP, Wang ML, Yu GL, Peng F, Wei EQ. Spatio-temporal expression of cysteinyl leukotriene receptor-2 mRNA in rat brain after focal cerebral ischemia. Neurosci Lett 2007, 412:78-83. 10.1016/j.neulet.2006.10.065, 17196746.
23. Zhang YJ, Zhang L, Ye YL, Fang SH, Zhou Y, Zhang WP, Lu YB, Wei EQ. Cysteinyl leukotriene receptors CysLT1 and CysLT2 are upregulated in acute neuronal injury after focal cerebral ischemia in mice. Acta Pharmacol Sin 2006, 27:1553-1560. 10.1111/j.1745-7254.2006.00458.x, 17112408.
24. Zhou Y, Wei EQ, Fang SH, Chu LS, Wang ML, Zhang WP, Yu GL, Ye YL, Lin SC, Chen Z. Spatio-temporal properties of 5-lipoxygenase expression and activation in the brain after focal cerebral ischemia in rats. Life Sci 2006, 79:1645-1656. 10.1016/j.lfs.2006.05.022, 16824548.
25. Fang SH, Wei EQ, Zhou Y, Wang ML, Zhang WP, Yu GL, Chu LS, Chen Z. Increased expression of cysteinyl leukotriene receptor-1 in the brain mediates neuronal damage and astrogliosis after focal cerebral ischemia in rats. Neuroscience 2006, 140:969-979. 10.1016/j.neuroscience.2006.02.051, 16650938.
26. Zhao CZ, Zhao B, Zhang XY, Huang XQ, Shi WZ, Liu HL, Fang SH, Lu YB, Zhang WP, Tang FD, Wei EQ. Cysteinyl leukotriene receptor 2 is spatiotemporally involved in neuron injury, astrocytosis and microgliosis after focal cerebral ischemia in rats. Neuroscience 2011, 189:1-11.
27. Yu GL, Wei EQ, Zhang SH, Xu HM, Chu LS, Zhang WP, Zhang Q, Chen Z, Mei RH, Zhao MH. Montelukast, a cysteinyl leukotriene receptor-1 antagonist, dose- and time-dependently protects against focal cerebral ischemia in mice. Pharmacology 2005, 73:31-40. 10.1159/000081072, 15452361.
28. Yu GL, Wei EQ, Wang ML, Zhang WP, Zhang SH, Weng JQ, Chu LS, Fang SH, Zhou Y, Chen Z, Zhang Q, Zhang LH. Pranlukast, a cysteinyl leukotriene receptor-1 antagonist, protects against chronic ischemic brain injury and inhibits the glial scar formation in mice. Brain Res 2005, 1053:116-125. 10.1016/j.brainres.2005.06.046, 16051204.
29. Ciccarelli R, D'Alimonte I, Santavenere C, D'Auro M, Ballerini P, Nargi E, Buccella S, Nicosia S, Folco G, Caciagli F, Di Iorio P. Cysteinyl-leukotrienes are released from astrocytes and increase astrocyte proliferation and glial fibrillary acidic protein via cys-LT1 receptors and mitogen-activated protein kinase pathway. Eur J Neurosci 2004, 20:1514-1524. 10.1111/j.1460-9568.2004.03613.x, 15355318.
30. Huang XJ, Zhang WP, Li CT, Shi WZ, Fang SH, Lu YB, Chen Z, Wei EQ. Activation of CysLT receptors induces astrocyte proliferation and death after oxygen-glucose deprivation. Glia 2008, 56:27-37. 10.1002/glia.20588, 17910051.
31. Woszczek G, Chen LY, Nagineni S, Kern S, Barb J, Munson PJ, Logun C, Danner RL, Shelhamer JH. Leukotriene D(4) induces gene expression in human monocytes through cysteinyl leukotriene type I receptor. J Allergy Clin Immunol 2008, 121:215-221. e211, 10.1016/j.jaci.2007.09.013, 18028998.
32. Thivierge M, Stankova J, Rola-Pleszczynski M. Toll-like receptor agonists differentially regulate cysteinyl-leukotriene receptor 1 expression and function in human dendritic cells. J Allergy Clin Immunol 2006, 117:1155-1162. 10.1016/j.jaci.2005.12.1342, 16675346.
33. Thivierge M, Stankova J, Rola-Pleszczynski M. Cysteinyl-leukotriene receptor type 1 expression and function is down-regulated during monocyte-derived dendritic cell maturation with zymosan: involvement of IL-10 and prostaglandins. J Immunol 2009, 183:6778-6787. 10.4049/jimmunol.0901800, 19846883.
34. Kaetsu Y, Yamamoto Y, Sugihara S, Matsuura T, Igawa G, Matsubara K, Igawa O, Shigemasa C, Hisatome I. Role of cysteinyl leukotrienes in the proliferation and the migration of murine vascular smooth muscle cells in vivo and in vitro. Cardiovasc Res 2007, 76:160-166. 10.1016/j.cardiores.2007.05.018, 17588553.
35. Paruchuri S, Broom O, Dib K, Sjolander A. The pro-inflammatory mediator leukotriene D4 induces phosphatidylinositol 3-kinase and Rac-dependent migration of intestinal epithelial cells. J Biol Chem 2005, 280:13538-13544. 10.1074/jbc.M409811200, 15657050.
36. Yuan YM, Fang SH, Qian XD, Liu LY, Xu LH, Shi WZ, Zhang LH, Lu YB, Zhang WP, Wei EQ. Leukotriene D4 stimulates the migration but not proliferation of endothelial cells mediated by the cysteinyl leukotriene cyslt(1) receptor via the extracellular signal-regulated kinase pathway. J Pharmacol Sci 2009, 109:285-292. 10.1254/jphs.08321FP, 19234368.
37. Espinosa K, Bosse Y, Stankova J, Rola-Pleszczynski M. CysLT1 receptor upregulation by TGF-beta and IL-13 is associated with bronchial smooth muscle cell proliferation in response to LTD4. J Allergy Clin Immunol 2003, 111:1032-1040. 10.1067/mai.2003.1451, 12743568.
38. Asakura T, Ishii Y, Chibana K, Fukuda T. Leukotriene D4 stimulates collagen production from myofibroblasts transformed by TGF-beta. J Allergy Clin Immunol 2004, 114:310-315. 10.1016/j.jaci.2004.04.037, 15316508.
39. Paiva LA, Maya-Monteiro CM, Bandeira-Melo C, Silva PM, El-Cheikh MC, Teodoro AJ, Borojevic R, Perez SA, Bozza PT. Interplay of cysteinyl leukotrienes and TGF-beta in the activation of hepatic stellate cells from Schistosoma mansoni granulomas. Biochim Biophys Acta 2010, 1801:1341-1348. 10.1016/j.bbalip.2010.08.014, 20817008.
40. Qi LL, Fang SH, Shi WZ, Huang XQ, Zhang XY, Lu YB, Zhang WP, Wei EQ. CysLT2 receptor-mediated AQP4 up-regulation is involved in ischemic-like injury through activation of ERK and p38 MAPK in rat astrocytes. Life Sci 2011, 88:50-56. 10.1016/j.lfs.2010.10.025, 21055410.
41. Deleyrolle LP, Harding A, Cato K, Siebzehnrubl FA, Rahman M, Azari H, Olson S, Gabrielli B, Osborne G, Vescovi A, Reynolds BA. Evidence for label-retaining tumour-initiating cells in human glioblastoma. Brain 2011, 134:1331-1343. 10.1093/brain/awr081, 3097894, 21515906.
42. Quah BJ, Parish CR. New and improved methods for measuring lymphocyte proliferation in vitro and in vivo using CFSE-like fluorescent dyes. J Immunol Methods 2012, 379:1-14. 10.1016/j.jim.2012.02.012, 22370428.
43. Bogie JF, Stinissen P, Hellings N, Hendriks JJ. Myelin-phagocytosing macrophages modulate autoreactive T cell proliferation. J Neuroinflammation 2011, 8:85. 10.1186/1742-2094-8-85, 3149992, 21781347.
44. Luo JY, Zhang Z, Yu SY, Zhao B, Zhao CZ, Wang XX, Fang SH, Zhang WP, Zhang LH, Wei EQ, Lu YB. Rotenone-induced changes of cysteinyl leukotriene receptor 1 expression in BV2 microglial cells. Zhejiang Da Xue Xue Bao Yi Xue Ban 2011, 40:131-138.
45. Zhang LP, Zhao CZ, Shi WZ, Qi LL, Lu YB, Zhang YM, Zhang LH, Fang SH, Bao JF, Shen JG, Wei EQ. Preparation and identification of polyclonal antibody against cysteinyl leukotriene receptor 2. Zhejiang Da Xue Xue Bao Yi Xue Ban 2009, 38:591-597.
46. Yan D, Stocco R, Sawyer N, Nesheim ME, Abramovitz M, Funk CD. Differential signaling of cysteinyl leukotrienes and a novel cysteinyl leukotriene receptor 2 (CysLT) agonist, N-methyl-leukotriene C, in calcium reporter and beta arrestin assays. Mol Pharmacol 2011, 79:270-278. 10.1124/mol.110.069054, 21078884.
47. Stipursky J, Gomes FC. TGF-beta1/SMAD signaling induces astrocyte fate commitment in vitro: implications for radial glia development. Glia 2007, 55:1023-1033. 10.1002/glia.20522, 17549683.
48. Schachtrup C, Ryu JK, Helmrick MJ, Vagena E, Galanakis DK, Degen JL, Margolis RU, Akassoglou K. Fibrinogen triggers astrocyte scar formation by promoting the availability of active TGF-beta after vascular damage. J Neurosci 2010, 30:5843-5854. 10.1523/JNEUROSCI.0137-10.2010, 2871011, 20427645.
49. Lindholm D, Castren E, Kiefer R, Zafra F, Thoenen H. Transforming growth factor-beta 1 in the rat brain: increase after injury and inhibition of astrocyte proliferation. J Cell Biol 1992, 117:395-400. 10.1083/jcb.117.2.395, 2289420, 1560032.
50. Klaver CL, Caplan MR. Bioactive surface for neural electrodes: decreasing astrocyte proliferation via transforming growth factor-beta1. J Biomed Mater Res A 2007, 81:1011-1016.
51. Ge QF, Wei EQ, Zhang WP, Hu X, Huang XJ, Zhang L, Song Y, Ma ZQ, Chen Z, Luo JH. Activation of 5-lipoxygenase after oxygen-glucose deprivation is partly mediated via NMDA receptor in rat cortical neurons. J Neurochem 2006, 97:992-1004. 10.1111/j.1471-4159.2006.03828.x, 16606359.
52. Li CT, Zhang WP, Lu YB, Fang SH, Yuan YM, Qi LL, Zhang LH, Huang XJ, Zhang L, Chen Z, Wei EQ. Oxygen-glucose deprivation activates 5-lipoxygenase mediated by oxidative stress through the p38 mitogen-activated protein kinase pathway in PC12 cells. J Neurosci Res 2009, 87:991-1001. 10.1002/jnr.21913, 18951527.
53. Song Y, Wei EQ, Zhang WP, Ge QF, Liu JR, Wang ML, Huang XJ, Hu X, Chen Z. Minocycline protects PC12 cells against NMDA-induced injury via inhibiting 5-lipoxygenase activation. Brain Res 2006, 1085:57-67. 10.1016/j.brainres.2006.02.042, 16574083.
54. Steinhilber D, Radmark O, Samuelsson B. Transforming growth factor beta upregulates 5-lipoxygenase activity during myeloid cell maturation. Proc Natl Acad Sci USA 1993, 90:5984-5988. 10.1073/pnas.90.13.5984, 46851, 8327471.
55. Brungs M, Radmark O, Samuelsson B, Steinhilber D. On the induction of 5-lipoxygenase expression and activity in HL-60 cells: effects of vitamin D3, retinoic acid, DMSO and TGF beta. Biochem Biophys Res Commun 1994, 205:1572-1580. 10.1006/bbrc.1994.2846, 7811238.
56. Brungs M, Radmark O, Samuelsson B, Steinhilber D. Sequential induction of 5-lipoxygenase gene expression and activity in Mono Mac 6 cells by transforming growth factor beta and 1,25-dihydroxyvitamin D3. Proc Natl Acad Sci USA 1995, 92:107-111. 10.1073/pnas.92.1.107, 42826, 7816797.
57. Harle D, Radmark O, Samuelsson B, Steinhilber D. Calcitriol and transforming growth factor-beta upregulate 5-lipoxygenase mRNA expression by increasing gene transcription and mRNA maturation. Eur J Biochem 1998, 254:275-281. 10.1046/j.1432-1327.1998.2540275.x, 9660180.
58. Seuter S, Sorg BL, Steinhilber D. The coding sequence mediates induction of 5-lipoxygenase expression by Smads3/4. Biochem Biophys Res Commun 2006, 348:1403-1410. 10.1016/j.bbrc.2006.08.011, 16919603.
59. Ni NC, Yan D, Ballantyne LL, Barajas-Espinosa A, St Amand T, Pratt DA, Funk CD. A selective cysteinyl leukotriene receptor 2 antagonist blocks myocardial ischemia/reperfusion injury and vascular permeability in mice. J Pharmacol Exp Ther 2011, 339:768-778. 10.1124/jpet.111.186031, 21903747.
60. Carnini C, Accomazzo MR, Borroni E, Vitellaro-Zuccarello L, Durand T, Folco G, Rovati GE, Capra V, Sala A. Synthesis of cysteinyl leukotrienes in human endothelial cells: subcellular localization and autocrine signaling through the CysLT2 receptor. FASEB J 2011, 25:3519-3528. 10.1096/fj.10-177030, 21753081.
61. Bosse Y, Thompson C, McMahon S, Dubois CM, Stankova J, Rola-Pleszczynski M. Leukotriene D4-induced, epithelial cell-derived transforming growth factor beta1 in human bronchial smooth muscle cell proliferation. Clin Exp Allergy 2008, 38:113-121.
62. Perng DW, Wu YC, Chang KT, Wu MT, Chiou YC, Su KC, Perng RP, Lee YC. Leukotriene C4 induces TGF-beta1 production in airway epithelium via p38 kinase pathway. Am J Respir Cell Mol Biol 2006, 34:101-107. 10.1165/rcmb.2005-0068OC, 16179583.
63. Eap R, Jacques E, Semlali A, Plante S, Chakir J. Cysteinyl leukotrienes regulate TGF-beta(1) and collagen production by bronchial fibroblasts obtained from asthmatic subjects. Prostaglandins Leukot Essent Fatty Acids 2012, 86:127-133. 10.1016/j.plefa.2011.11.001, 22316690.
64. Yamashita K, Gerken U, Vogel P, Hossmann K, Wiessner C. Biphasic expression of TGF-beta1 mRNA in the rat brain following permanent occlusion of the middle cerebral artery. Brain Res 1999, 836:139-145. 10.1016/S0006-8993(99)01626-1, 10415412.
65. Doyle KP, Cekanaviciute E, Mamer LE, Buckwalter MS. TGFbeta signaling in the brain increases with aging and signals to astrocytes and innate immune cells in the weeks after stroke. J Neuroinflammation 2010, 7:62. 10.1186/1742-2094-7-62, 2958905, 20937129.
66. Kohta M, Kohmura E, Yamashita T. Inhibition of TGF-beta1 promotes functional recovery after spinal cord injury. Neurosci Res 2009, 65:393-401. 10.1016/j.neures.2009.08.017, 19744530.
67. Massague J, Wotton D. Transcriptional control by the TGF-beta/Smad signaling system. EMBO J 2000, 19:1745-1754. 10.1093/emboj/19.8.1745, 302010, 10775259.
68. Kloos DU, Choi C, Wingender E. The TGF-beta-Smad network: introducing bioinformatic tools. Trends Genet 2002, 18:96-103. 10.1016/S0168-9525(02)02556-8, 11818142.
69. Wang H, Yang GH, Bu H, Zhou Q, Guo LX, Wang SL, Ye L. Systematic analysis of the TGF-beta/Smad signalling pathway in the rhabdomyosarcoma cell line RD. Int J Exp Pathol 2003, 84:153-163. 10.1046/j.1365-2613.2003.00347.x, 2517554, 12974945.
70. ten Dijke P, Hill CS. New insights into TGF-beta-Smad signalling. Trends Biochem Sci 2004, 29:265-273. 10.1016/j.tibs.2004.03.008, 15130563.
71. Levy L, Hill CS. Smad4 dependency defines two classes of transforming growth factor beta (TGF-{beta}) target genes and distinguishes TGF-{beta}-induced epithelial-mesenchymal transition from its antiproliferative and migratory responses. Mol Cell Biol 2005, 25:8108-8125. 10.1128/MCB.25.18.8108-8125.2005, 1234333, 16135802.
72. Kaminska B, Wesolowska A, Danilkiewicz M. TGF beta signalling and its role in tumour pathogenesis. Acta Biochim Pol 2005, 52:329-337.
73. Finnson KW, Parker WL, Chi Y, Hoemann CD, Goldring MB, Antoniou J, Philip A. Endoglin differentially regulates TGF-beta-induced Smad2/3 and Smad1/5 signalling and its expression correlates with extracellular matrix production and cellular differentiation state in human chondrocytes. Osteoarthr Cartil 2010, 18:1518-1527. 10.1016/j.joca.2010.09.002, 20833252.
74. Chen M, Lv Z, Jiang S. The effects of triptolide on airway remodelling and transforming growth factor-beta/Smad signalling pathway in ovalbumin-sensitized mice. Immunology 2011, 132:376-384. 10.1111/j.1365-2567.2010.03392.x, 3044903, 21214541.
75. Lampropoulos P, Zizi-Sermpetzoglou A, Rizos S, Kostakis A, Nikiteas N, Papavassiliou AG. TGF-beta signalling in colon carcinogenesis. Cancer Lett 2012, 314:1-7. 10.1016/j.canlet.2011.09.041, 22018778.
76. Park BJ, Park JI, Byun DS, Park JH, Chi SG. Mitogenic conversion of transforming growth factor-beta1 effect by oncogenic Ha-Ras-induced activation of the mitogen-activated protein kinase signaling pathway in human prostate cancer. Cancer Res 2000, 60:3031-3038.
77. Dai C, Yang J, Liu Y. Transforming growth factor-beta1 potentiates renal tubular epithelial cell death by a mechanism independent of Smad signaling. J Biol Chem 2003, 278:12537-12545. 10.1074/jbc.M300777200, 12560323.
78. Kim YK. TGF-beta1 induction of p21WAF1/cip1 requires Smad-independent protein kinase C signaling pathway. Arch Pharm Res 2007, 30:739-742. 10.1007/BF02977636, 17679552.
79. Niculescu-Duvaz I, Phanish MK, Colville-Nash P, Dockrell ME. The TGFbeta1-induced fibronectin in human renal proximal tubular epithelial cells is p38 MAP kinase dependent and Smad independent. Nephron Exp Nephrol 2007, 105:e108-e116. 10.1159/000100492, 17347580.
80. Kane NM, Jones M, Brosens JJ, Kelly RW, Saunders PT, Critchley HO. TGFbeta1 attenuates expression of prolactin and IGFBP-1 in decidualized endometrial stromal cells by both SMAD-dependent and SMAD-independent pathways. PLoS One 2010, 5:e12970. 10.1371/journal.pone.0012970, 2945765, 20885978.
81. Watkins SJ, Borthwick GM, Oakenfull R, Robson A, Arthur HM. Angiotensin II-induced cardiomyocyte hypertrophy in vitro is TAK1-dependent and Smad2/3-independent. Hypertens Res 2012, 35:393-398. 10.1038/hr.2011.196, 22072105.
82. Gomes FC, Sousa Vde O, Romao L. Emerging roles for TGF-beta1 in nervous system development. Int J Dev Neurosci 2005, 23:413-424. 10.1016/j.ijdevneu.2005.04.001, 15936920.
83. Buss A, Pech K, Kakulas BA, Martin D, Schoenen J, Noth J, Brook GA. TGF-beta1 and TGF-beta2 expression after traumatic human spinal cord injury. Spinal Cord 2008, 46:364-371. 10.1038/sj.sc.3102148, 18040277.
84. Komuta Y, Teng X, Yanagisawa H, Sango K, Kawamura K, Kawano H. Expression of transforming growth factor-beta receptors in meningeal fibroblasts of the injured mouse brain. Cell Mol Neurobiol 2010, 30:101-111. 10.1007/s10571-009-9435-x, 19653094.
85. Zhou Y, Fang SH, Ye YL, Chu LS, Zhang WP, Wang ML, Wei EQ. Caffeic acid ameliorates early and delayed brain injuries after focal cerebral ischemia in rats. Acta Pharmacol Sin 2006, 27:1103-1110. 10.1111/j.1745-7254.2006.00406.x, 16923329.
86. Zhang L, Zhang WP, Chen KD, Qian XD, Fang SH, Wei EQ. Caffeic acid attenuates neuronal damage, astrogliosis and glial scar formation in mouse brain with cryoinjury. Life Sci 2007, 80:530-537. 10.1016/j.lfs.2006.09.039, 17074364.