Pericytes and adaptive angioplasticity: The role of tumor necrosis factor-like weak inducer of apoptosis (TWEAK)

Methods in Molecular Biology

Volumn 1135, Issue , 2014, Pages 35-52

  Dore Duffy, Paula ^a  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Adaptation; Fn14; Hypoxia; Migration; Pericytes; Physiological angiogenesis; Tumor necrosis family; TWEAK

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; CHEMOKINE RECEPTOR CXCR3; FGF INDUCIBLE MOLECULE 14 PROTEIN; GAMMA INTERFERON; GLIAL FIBRILLARY ACIDIC PROTEIN; HEPARIN; I KAPPA B KINASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; MULTIDRUG RESISTANCE PROTEIN 6; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; SMOOTH MUSCLE ACTIN; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR AP 1; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR LIKE WEAK INDUCER OF APOPTOSIS PROTEIN; TUMOR NECROSIS FACTOR RECEPTOR; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 2; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6; UNCLASSIFIED DRUG; VASCULOTROPIN; FIBROBLAST GROWTH FACTOR 14; TUMOR NECROSIS FACTOR LIKE WEAK INDUCER OF APOPTOSIS;

ANGIOGENESIS; ARTICLE; ASTROCYTE; BLOOD BRAIN BARRIER; BLOOD VESSEL PERMEABILITY; CELL COUNT; CELL DIFFERENTIATION; CELL MATURATION; CELL MIGRATION; CELL POPULATION; CELL PROLIFERATION; CELL SURVIVAL; CELLULAR DISTRIBUTION; GENE PRODUCT; HUMAN; HYPOXIA; INTRACELLULAR SIGNALING; MIDDLE CEREBRAL ARTERY OCCLUSION; MITOGENESIS; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; OLIGODENDROGLIA; PERICYTE; PLEIOTROPY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; ADAPTIVE ANGIOPLASTICITY; ADAPTIVE IMMUNITY; APOPTOSIS; BRAIN PERICYTE; CELL FUNCTION; CYTOKINE RELEASE; CYTOKINE RESPONSE; MICROVASCULARIZATION; NERVE CELL PLASTICITY; REGULATORY MECHANISM;

EID: 84934438188     PISSN: 10643745     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-1-4939-320-7_4     Document Type: Article

References (132)

1. Rouget C (1874) Note sur le developpement de la tunique contractile des vaisseaux. Compt Rend Acad Sci 59:559-562
2. Dorè SE (1923) On the contractility and nervous supply of the capillaries. Brit J Dermatol 35:398-404
3. Fabry Z, Fitzsimmons KM, Herlein JA et al (1993) Production of the cytokines interleukin 1 and 6 by murine brain microvessel endothelium and smooth muscle pericytes. J Neuroimmunol 47:23-34
4. Spraycar M (ed) (1995) Stedman's medical dictionary, 6th edn. Williams and Wilkins, Baltimore, MD
5. Ding R, Darland DC, Parmacek MS et al (2004) Endothelial-mesenchymal interactions in vitro reveal molecular mechanisms of smooth muscle/pericyte differentiation. Stem Cells Dev 13:509-520
6. Hautekeete ML, Geerts A (1997) The hepatic stellate (Ito) cell: its role in human liver disease. Virchows Arch 430:195-207
7. Dore-Duffy P, Katychev A, Wang X et al (2006) CNS microvascular pericytes exhibit multipotential stem cell activity. J Cereb Blood Flow Metab 26:613-624
8. Andreeva ER, Pugach IM, Gordon D et al (1998) Continuous subendothelial network formed by pericyte-like cells in human vascular bed. Tissue Cell 30:127-135
9. Dore-Duffy P (2008) Pericytes: pluripotent cells of the blood brain barrier. Curr Pharm Des 14:1581-1593
10. Sims DE (1991) Recent advances in pericyte biology-implications for health and disease. Can J Cardiol 7:431-443
11. Dore-Duffy P, Owen C, Balabanov R et al (2000) Pericyte migration from the vascular wall in response to traumatic brain injury. Microvasc Res 60:55-69
12. Pfister F, Feng Y, vom Hagen F (2008) Pericyte migration: a novel mechanism of pericyte loss in experimental diabetic retinopathy. Diabetes 57:2495-2502
13. Joyce NC, Haire MF, Palade GE (1985) Contractile proteins in pericytes. II. Immunocytochemical evidence for the presence of two isomyosins in graded concentrations. J Cell Biol 100:1387-1395
14. Herman IM, D'Amore PA (1985) Microvascular pericytes contain muscle and nonmuscle actins. J Cell Biol 101:43-52
15. Skalli O, Pelte MF, Peclet MC et al (1989) Alpha-smooth muscle actin, a differentiation marker of smooth muscle cells, is present in microfilamentous bundles of pericytes. J Histochem Cytochem 37:315-321
16. Hamilton NB, Attwell D, Hall CN (2010) Pericyte-mediated regulation of capillary diameter: a component of neurovascular coupling in health and disease. Front Neuroenergetics. doi: 10.3389/fnene.2010.00005
17. Kennedy-Lydon TM, Crawford C, Wildman SS et al (2013) Renal pericytes: regulators of medullary blood flow. Acta Physiol (Oxf) 207:212-225
18. Kinner B, Zaleskas JM, Spector M (2002) Regulation of smooth muscle actin expression and contraction in adult human mesenchymal stem cells. Exp Cell Res 278:72-83
19. Dore-Duffy P, Mehedi A, Wang X et al (2011) Immortalized CNS pericytes are quiescent smooth muscle actin-negative and pluripotent. Microvasc Res 82:18-27
20. Dore-Duffy P, Wang S, Mehedi A et al (2011) Pericyte-mediated vasoconstriction underlies TBI-induced hypoperfusion. Neurol Res 33:176-186
21. Balabanov R, Dore-Duffy P (1998) Role of the CNS microvascular pericyte in the blood- brain barrier. J Neurosci Res 53:637-644
22. Schlingemann RO, Rietveld FJ, de Waal RM et al (1990) Expression of the high molecular weight melanoma-associated antigen by pericytes during angiogenesis in tumors and in healing wounds. Am J Pathol 136:1393-1405
23. Murfee WL, Skalak TC, Peirce SM (2005) Differential arterial/venous expression of NG2 proteoglycan in perivascular cells along microvessels: identifying a venule-specific phenotype. Microcirculation 12:151-160
24. Stallcup WB (2002) The NG2 proteoglycan: past insights and future prospects. J Neurocytol 31:423-435
25. Verbeek MM, Otte-Holler I, Wesseling P et al (1994) Induction of alpha-smooth muscle actin expression in cultured human brain pericytes by transforming growth factor-beta 1. Am J Pathol 144:372-382
26. Bandopadhyay R, Orte C, Lawrenson JG et al (2001) Contractile proteins in pericytes at the blood-brain and blood-retinal barriers. J Neurocytol 30:35-44
27. Kunz J, Krause D, Kremer M et al (1994) The 140-kDa protein of blood-brain barrierassociated pericytes is identical to aminopeptidase N. J Neurochem 62:2375-2386
28. Alliot F, Rutin J, Leenen PJ et al (1999) Pericytes and periendothelial cells of brain parenchyma vessels co-express aminopeptidase N, aminopeptidase A, and nestin. J Neurosci Res 58:367-378
29. Nayak RC, Berman AB, George KL et al (1988) A monoclonal antibody (3G5)- defined ganglioside antigen is expressed on the cell surface of microvascular pericytes. J Exp Med 167:1003-1015
30. Cho H, Kozasa T, Bondjers C et al (2003) Pericyte-specific expression of Rgs5: implications for PDGF and EDG receptor signaling during vascular maturation. FASEB J 17: 440-442
31. Crisan M, Yap S, Casteilla L et al (2008) A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 3:301-313
32. Paquet-Fifield S, Schluter H, Li A et al (2009) A role for pericytes as microenvironmental regulators of human skin tissue regeneration. J Clin Invest 119:2795-2806
33. Brachvogel B, Moch H, Pausch F et al (2005) Perivascular cells expressing annexin A5 define a novel mesenchymal stem cell-like population with the capacity to differentiate into multiple mesenchymal lineages. Development 132: 2657-2668
34. Schor AM, Allen TD, Canfield AE et al (1990) Pericytes derived from the retinal microvasculature undergo calcification in vitro. J Cell Sci 97(Pt 3):449-461
35. Dar A, Domev H, Ben-Yosef O et al (2012) Multipotent vasculogenic pericytes from human pluripotent stem cells promote recovery of murine ischemic limb. Circulation 125:87-99
36. Dore-Duffy P (2003) Isolation and characterization of cerebral microvascular pericytes. Methods Mol Med 89:375-382
37. Rucker HK, Wynder HJ, Thomas WE (2000) Cellular mechanisms of CNS pericytes. Brain Res Bull 51:363-369
38. Tilton RG (1991) Capillary pericytes: perspectives and future trends. J Electron Microsc Tech 19:327-344
39. Shepro D, Morel NM (1993) Pericyte physiology. FASEB J 7:1031-1038
40. Fisher M (2009) Pericyte signaling in the neurovascular unit. Stroke 40:S13-S15
41. Bergers G, Song S (2005) The role of pericytes in blood-vessel formation and maintenance. Neuro Oncol 7(4):452-464
42. Siao CJ, Lorentz CU, Kermani P et al (2012) ProNGF, a cytokine induced after myocardial infarction in humans, targets pericytes to promote microvascular damage and activation. J Exp Med 209:2291-2305
43. Armulik A, Abramsson A, Betsholtz C (2005) Endothelial/pericyte interactions. Circ Res 97:512-523
44. Armulik A, Genove G, Mae M et al (2010) Pericytes regulate the blood-brain barrier. Nature 468:557-561
45. Nawashiro H, Messing A, Azzam N et al (1998) Mice lacking GFAP are hypersensitive to traumatic cerebrospinal injury. Neuroreport 9:1691-1696
46. Bonkowski D, Katyshev V, Balabanov RD et al (2011) The CNS microvascular pericyte: pericyte-astrocyte crosstalk in the regulation of tissue survival. Fluids Barriers CNS 8(1):8
47. Daneman R, Zhou L, Kebede AA et al (2010) Pericytes are required for blood-brain barrier integrity during embryogenesis. Nature 468:562-566
48. Al Ahmad A, Taboada CB, Gassmann M et al (2011) Astrocytes and pericytes differentially modulate blood-brain barrier characteristics during development and hypoxic insult. J Cereb Blood Flow Metab 31:693-705
49. Berezowski V, Landry C, Dehouck MP et al (2004) Contribution of glial cells and pericytes to the mRNA profiles of P-glycoprotein and multidrug resistance-associated proteins in an in vitro model of the blood-brain barrier. Brain Res 1018:1-9
50. Dohgu S, Takata F, Yamauchi A et al (2005) Brain pericytes contribute to the induction and up-regulation of blood-brain barrier functions through transforming growth factor- beta production. Brain Res 1038:208-215
51. Bendayan R, Ronaldson PT, Gingras D et al (2006) In situ localization of P-glycoprotein (ABCB1) in human and rat brain. J Histochem Cytochem 54:1159-1167
52. Quaglino D, Boraldi F, Annovi G et al (2011) The multifaceted complexity of genetic diseases: a lesson from pseudoxanthoma elasticum. In: Kenji I (ed) Advances in the study of genetic disorders. Intech, Croatia. doi: 10.5772/22161 . ISBN 978-953-307-305-7
53. Lonigro AJ, McMurdo L, Stephenson AH et al (1996) Hypotheses regarding the role of pericytes in regulating movement of fluid, nutrients, and hormones across the microcirculatory endothelial barrier. Diabetes 45(Suppl 1):S38-S43
54. Dore-Duffy P, LaManna JC (2007) Physiologic angiodynamics in the brain. Antioxid Redox Signal 9(9):1363-1371
55. Seaman S, Stevens J, Yang MY et al (2007) Genes that distinguish physiological and pathological angiogenesis. Cancer Cell 11:539-554
56. Diaz-Flores L, Gutierrez R, Valladares F et al (1994) Intense vascular sprouting from rat femoral vein induced by prostaglandins E1 and E2. Anat Rec 238:68-76
57. Lai CH, Kuo KH (2005) The critical component to establish in vitro BBB model: pericyte. Brain Res Brain Res Rev 50:258-265
58. Virgintino D, Girolamo F, Errede M et al (2007) An intimate interplay between precocious, migrating pericytes and endothelial cells governs human fetal brain angiogenesis. Angiogenesis 10:35-45
59. Egginton S, Zhou AL, Brown MD et al (2000) The role of pericytes in controlling angiogenesis in vivo. Adv Exp Med Biol 476:81-99
60. Reynolds LP, Grazul-Bilska AT, Redmer DA (2000) Angiogenesis in the corpus luteum. Endocrine 12:1-9
61. Ozerdem U, Stallcup WB (2003) Early contribution of pericytes to angiogenic sprouting and tube formation. Angiogenesis 6:241-249
62. Gerhardt H, Betsholtz C (2003) Endothelialpericyte interactions in angiogenesis. Cell Tissue Res 314:15-23
63. Diaz-Flores L, Gutierrez R, Gonzalez P et al (1991) Inducible perivascular cells contribute to the neochondrogenesis in grafted perichondrium. Anat Rec 229:1-8
64. Gonul E, Duz B, Kahraman S (2002) Early pericyte response to brain hypoxia in cats: an ultrastructural study. Microvasc Res 64(1):116-119
65. Dore-Duffy P, Wang X, Mehedi A et al (2007) Differential expression of capillary VEGF isoforms following traumatic brain injury. Neurol Res 29:395-403
66. Melgar MA, Rafols J, Gloss D et al (2005) Postischemic reperfusion: ultrastructural blood- brain barrier and hemodynamic correlative changes in an awake model of transient forebrain ischemia. Neurosurgery 56:571-581
67. Duz B, Oztas E, Erginay T et al (2007) The effect of moderate hypothermia in acute ischemic stroke on pericyte migration: an ultrastructural study. Cryobiology 55: 279-284
68. Hellstrom M, Kalen M, Lindahl P et al (1999) Role of PDGF-B and PDGFR-beta in recruitment of vascular smooth muscle cells and pericytes during embryonic blood vessel formation in the mouse. Development 126:3047-3055
69. Jin K, Mao XO, Sun Y et al (2002) Heparinbinding epidermal growth factor-like growth factor: hypoxia-inducible expression in vitro and stimulation of neurogenesis in vitro and in vivo. J Neurosci 22:5365-5373
70. Rovida E, Navari N, Caligiuri A et al (2008) ERK5 differentially regulates PDGF-induced proliferation and migration of hepatic stellate cells. J Hepatol 48:107-115
71. Bonacchi A, Romagnani P, Romanelli RG et al (2001) Signal transduction by the chemokine receptor CXCR3: activation of Ras/ERK, Src, and phosphatidylinositol 3-kinase/Akt controls cell migration and proliferation in human vascular pericytes. J Biol Chem 276:9945-9954
72. Bernstein LR, Antoniades H, Zetter BR (1982) Migration of cultured vascular cells in response to plasma and platelet-derived factors. J Cell Sci 56:71-82
73. Tigges U, Boroujerdi A, Welser-Alves JV et al (2013) TNF-alpha promotes cerebral pericyte remodeling in vitro, via a switch from alpha1 to alpha2 integrins. J Neuroinflammation 10:33
74. Clark ER, Clark EL (2005) The development of adventitial (Rouget) cells on the blood capillaries of amphibian larvae. Am J Anat 35:239-264. doi: 10.1002/aja.1000350205
75. Carmeliet P (2004) Manipulating angiogenesis in medicine. J Intern Med 255(5):538-561
76. Distler O, Neidhart M, Gay RE et al (2002) The molecular control of angiogenesis. Int Rev Immunol 21:33-49
77. Hall AP (2006) Review of the pericyte during angiogenesis and its role in cancer and diabetic retinopathy. Toxicol Pathol 34: 763-775
78. Harik SI, Hritz MA, LaManna JC (1995) Hypoxia-induced brain angiogenesis in the adult rat. J Physiol 485(Pt 2):525-530
79. Chavez JC, Agani F, Pichiule P et al (2000) Expression of hypoxia-inducible factor-1alpha in the brain of rats during chronic hypoxia. J Appl Physiol 89:1937-1942
80. LaManna JC, Vendel LM, Farrell RM (1992) Brain adaptation to chronic hypobaric hypoxia in rats. J Appl Physiol 72:2238-2243
81. Pichiule P, LaManna JC (2002) Angiopoietin-2 and rat brain capillary remodeling during adaptation and deadaptation to prolonged mild hypoxia. J Appl Physiol 93:1131-1139
82. Vandenhaute E, Culot M, Gosselet F et al (2012) Brain pericytes from stress-susceptible pigs increase blood-brain barrier permeability in vitro. Fluids Barriers CNS 9:11
83. Manea A, Constantinescu E, Popov D et al (2004) Changes in oxidative balance in rat pericytes exposed to diabetic conditions. J Cell Mol Med 8:117-126
84. Paepe BD, Creus KK, Bleecker JLD (2012) The tumor necrosis factor superfamily of cytokines in the inflammatory myopathies: potential targets for therapy. Clin Dev Immunol 2012:369-432
85. Ando T, Ichikawa J, Wako M et al (2006) TWEAK/Fn14 interaction regulates RANTES production, BMP-2-induced differentiation, and RANKL expression in mouse osteoblastic MC3T3-E1 cells. Arthritis Res Ther 8:R146
86. Tweedie D, Sambamurti K, Greig NH (2007) TNF-alpha inhibition as a treatment strategy for neurodegenerative disorders: new drug candidates and targets. Curr Alzheimer Res 4:378-385
87. Frankola KA, Greig NH, Luo W et al (2011) Targeting TNF-α to elucidate and ameliorate neuroinflammation in neurodegenerative diseases. CNS Neurol Disord Drug Targets 10:391-403
88. Locksley RM, Killeen N, Lenardo MJ (2001) The TNF and TNF receptor superfamilies: integrating mammalian biology. Cell 104:487-501
89. Chicheportiche Y, Bourdon PR, Xu H et al (1997) TWEAK, a new secreted ligand in the tumor necrosis factor family that weakly induces apoptosis. J Biol Chem 272:32401-32410
90. Schneider P, Schwenzer R, Haas E et al (1999) TWEAK can induce cell death via endogenous TNF and TNF receptor 1. Eur J Immunol 29:1785-1792
91. Winkles JA (2008) The TWEAK-Fn14 cytokine- receptor axis: discovery, biology and therapeutic targeting. Nat Rev Drug Discov 7:411-425
92. Burkly LC, Michaelson JS, Hahm K et al (2007) TWEAKing tissue remodeling by a multifunctional cytokine: role of TWEAK/Fn14 pathway in health and disease. Cytokine 40:1-16
93. Brown SA, Ghosh A, Winkles JA (2010) Fulllength, membrane-anchored TWEAK can function as a juxtacrine signaling molecule and activate the NF-kappaB pathway. J Biol Chem 285:17432-17441
94. Pradet-Balade B, Medema JP, Lopez-Fraga M et al (2002) An endogenous hybrid mRNA encodes TWE-PRIL, a functional cell surface TWEAK-APRIL fusion protein. EMBO J 21:5711-5720
95. Wiley SR, Winkles JA (2003) TWEAK, a member of the TNF superfamily, is a multifunctional cytokine that binds the TweakR/Fn14 receptor. Cytokine Growth Factor Rev 14:241-249
96. Wiley SR, Cassiano L, Lofton T et al (2001) A novel TNF receptor family member binds TWEAK and is implicated in angiogenesis. Immunity 15:837-846
97. Bossen C, Ingold K, Tardivel A et al (2006) Interactions of tumor necrosis factor (TNF) and TNF receptor family members in the mouse and human. J Biol Chem 281:13964-13971
98. Nakayama M, Harada N, Okumura K et al (2003) Characterization of murine TWEAK and its receptor (Fn14) by monoclonal antibodies. Biochem Biophys Res Commun 306:819-825
99. Dogra C, Hall SL, Wedhas N et al (2007) Fibroblast growth factor inducible 14 (Fn14) is required for the expression of myogenic regulatory factors and differentiation of myoblasts into myotubes. Evidence for TWEAKindependent functions of Fn14 during myogenesis. J Biol Chem 282:15000-15010
100. Tran NL, McDonough WS, Savitch BA et al (2005) The tumor necrosis factor-like weak inducer of apoptosis (TWEAK)-fibroblast growth factor-inducible 14 (Fn14) signaling system regulates glioma cell survival via NFkappaB pathway activation and BCL-XL/BCL-W expression. J Biol Chem 280:3483-3492
101. Tran NL, McDonough WS, Donohue PJ et al (2003) The human Fn14 receptor gene is upregulated in migrating glioma cells in vitro and overexpressed in advanced glial tumors. Am J Pathol 162:1313-1321
102. Tran NL, McDonough WS, Savitch BA et al (2006) Increased fibroblast growth factorinducible 14 expression levels promote glioma cell invasion via Rac1 and nuclear factor-kappaB and correlate with poor patient outcome. Cancer Res 66:9535-9542
103. Nakayama M, Ishidoh K, Kayagaki N et al (2002) Multiple pathways of TWEAKinduced cell death. J Immunol 168:734-743
104. Chang HY, Sneddon JB, Alizadeh AA et al (2004) Gene expression signature of fibroblast serum response predicts human cancer progression: similarities between tumors and wounds. PLoS Biol 2:E7
105. Chang HY, Nuyten DS, Sneddon JB et al (2005) Robustness, scalability, and integration of a wound-response gene expression signature in predicting breast cancer survival. Proc Natl Acad Sci U S A 102:3738-3743
106. Yepes M, Brown SA, Moore EG et al (2005) A soluble Fn14-Fc decoy receptor reduces infarct volume in a murine model of cerebral ischemia. Am J Pathol 166:511-520
107. Lembo AJ, Neri B, Tolley J et al (2009) Use of serum biomarkers in a diagnostic test for irritable bowel syndrome. Aliment Pharmacol Ther 29:834-842
108. Serafini B, Magliozzi R, Rosicarelli B et al (2008) Expression of TWEAK and its receptor Fn14 in the multiple sclerosis brain: implications for inflammatory tissue injury. J Neuropathol Exp Neurol 67:1137-1148
109. Michaelson JS, Wisniacki N, Burkly LC et al (2012) Role of TWEAK in lupus nephritis: a bench-to-bedside review. J Autoimmun 39:130-142
110. Kamata K, Kamijo S, Nakajima A et al (2006) Involvement of TNF-like weak inducer of apoptosis in the pathogenesis of collageninduced arthritis. J Immunol 177:6433-6439
111. Perper SJ, Browning B, Burkly LC et al (2006) TWEAK is a novel arthritogenic mediator. J Immunol 177:2610-2620
112. Maecker H, Varfolomeev E, Kischkel F et al (2005) TWEAK attenuates the transition from innate to adaptive immunity. Cell 123:931-944
113. Han S, Yoon K, Lee K et al (2003) TNFrelated weak inducer of apoptosis receptor, a TNF receptor superfamily member, activates NF-kappa B through TNF receptor- associated factors. Biochem Biophys Res Commun 305:789-796
114. Saitoh T, Nakayama M, Nakano H et al (2003) TWEAK induces NF-kappaB2 p100 processing and long lasting NF-kappaB activation. J Biol Chem 278:36005-36012
115. Perkins ND (2007) Integrating cell-signalling pathways with NF-kappaB and IKK function. Nat Rev Mol Cell Biol 8:49-62
116. Hayden MS, West AP, Ghosh S (2006) NF-kappaB and the immune response. Oncogene 25:6758-6780
117. Fotin-Mleczek M, Henkler F, Hausser A et al (2004) Tumor necrosis factor receptorassociated factor (TRAF) 1 regulates CD40- induced TRAF2-mediated NF-kappaB activation. J Biol Chem 279:677-685
118. Hauer J, Puschner S, Ramakrishnan P et al (2005) TNF receptor (TNFR)-associated factor (TRAF) 3 serves as an inhibitor of TRAF2/5-mediated activation of the noncanonical NF-kappaB pathway by TRAFbinding TNFRs. Proc Natl Acad Sci U S A 102:2874-2879
119. Jakubowski A, Browning B, Lukashev M et al (2002) Dual role for TWEAK in angiogenic regulation. J Cell Sci 115:267-274
120. Girgenrath M, Weng S, Kostek CA et al (2006) TWEAK, via its receptor Fn14, is a novel regulator of mesenchymal progenitor cells and skeletal muscle regeneration. EMBO J 25:5826-5839
121. Polek TC, Talpaz M, Darnay BG et al (2003) TWEAK mediates signal transduction and differentiation of RAW264.7 cells in the absence of Fn14/TweakR. Evidence for a second TWEAK receptor. J Biol Chem 278:32317-32323
122. Bhatnagar S, Kumar A (2012) The TWEAK-Fn14 system: breaking the silence of cytokine-induced skeletal muscle wasting. Curr Mol Med 12:3-13
123. Bird T, Knight B, Boulter L et al (2010) P55 Syngenic bone marrow transfer stimulates hepatic progenitor cell expansion via TWEAK/Fn14 Signalling: implications for human autologous cell therapy. Gut 59:A33
124. Hamill CA, Michaelson JS, Hahm K et al (2007) Age-dependent effects of TWEAK/Fn14 receptor activation on neural progenitor cells. J Neurosci Res 85:3535-3544
125. Lynch CN, Wang YC, Lund JK et al (1999) TWEAK induces angiogenesis and proliferation of endothelial cells. J Biol Chem 274:8455-8459
126. Biancone L, Martino AD, Orlandi V et al (1997) Development of inflammatory angiogenesis by local stimulation of Fas in vivo. J Exp Med 186:147-152
127. Donohue PJ, Richards CM, Brown SA et al (2003) TWEAK is an endothelial cell growth and chemotactic factor that also potentiates FGF-2 and VEGF-A mitogenic activity. Arterioscler Thromb Vasc Biol 23:594-600
128. Tian XL, Kadaba R, You SA et al (2004) Identification of an angiogenic factor that when mutated causes susceptibility to Klippel- Trenaunay syndrome. Nature 427:640-645
129. Kawakita T, Shiraki K, Yamanaka Y et al (2005) Functional expression of TWEAK in human colonic adenocarcinoma cells. Int J Oncol 26:87-93
130. Shimada K, Fujii T, Tsujikawa K et al (2012) ALKBH3 contributes to survival and angiogenesis of human urothelial carcinoma cells through NADPH oxidase and tweak/Fn14/VEGF signals. Clin Cancer Res 18:5247-5255
131. Hahne M, Kataoka T, Schroter M et al (1998) APRIL, a new ligand of the tumor necrosis factor family, stimulates tumor cell growth. J Exp Med 188:1185-1190
132. Marmarou A, Foda MA, van den Campbell BW et al (1994) A new model of diffuse brain injury in rats. Part I: pathophysiology and biomechanics. J Neurosurg 80:291-300