Regulation of angiogenesis, mural cell recruitment and adventitial macrophage behavior by Toll-like receptors

Angiogenesis

Volumn 17, Issue 1, 2014, Pages 147-161

  Aplin, Alfred C ^a   Ligresti, Giovanni ^a   Fogel, Eric ^b   Zorzi, Penelope ^a   Smith, Kelly ^a   Nicosia, Roberto F ^a,b  

^a UNIVERSITY OF WASHINGTON   (United States)

^b VA PUGET SOUND HEALTH CARE SYSTEM   (United States)

Author keywords

Aorta; Atherosclerosis; Endothelial cells; Inflammation; Innate immunity; Pericytes; Vasculitis

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MYELOID DIFFERENTIATION FACTOR 88; PLATELET DERIVED GROWTH FACTOR A; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 1; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 5; TOLL LIKE RECEPTOR 6; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 8; TOLL LIKE RECEPTOR 9; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA; AORTA INJURY; ARTICLE; CELL ISOLATION; CELL MIGRATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENDOTHELIUM CELL; GIANT CELL; MACROPHAGE; MACROPHAGE FUNCTION; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PERICYTE; PRIORITY JOURNAL; PROTEIN SYNTHESIS; REGULATORY MECHANISM; UPREGULATION; VASCULARIZATION;

ADVENTITIA; ANIMALS; AORTA; CELL DIFFERENTIATION; LIPOPOLYSACCHARIDES; MACROPHAGES; MALE; MICE; MICE, KNOCKOUT; MYELOID DIFFERENTIATION FACTOR 88; NEOVASCULARIZATION, PHYSIOLOGIC; PROTO-ONCOGENE PROTEINS C-SIS; RATS; RATS, INBRED F344; TOLL-LIKE RECEPTORS; TUNICA INTIMA;

EID: 84892694756     PISSN: 09696970     EISSN: 15737209     Source Type: Journal    
DOI: 10.1007/s10456-013-9384-3     Document Type: Article

References (64)

1. Coultas L, Chawengsaksophak K, Rossant J (2005) Endothelial cells and VEGF in vascular development. Nature 438:937-945
2. Carmeliet P (2005) Angiogenesis in life, disease and medicine. Nature 438:932-936
3. Carmeliet P, Jain RK (2011) Molecular mechanisms and clinical applications of angiogenesis. Nature 473:298-307
4. Ferrara N (2009) VEGF-A: a critical regulator of blood vessel growth. Eur Cytokine Netw 20:158-163
5. Koh GY (2013) Orchestral actions of angiopoietin-1 in vascular regeneration. Trends Mol Med 19:31-39
6. Jin SW, Beis D, Mitchell T, Chen JN, Stainier DY (2005) Cellular and molecular analyses of vascular tube and lumen formation in zebrafish. Development 132:5199-5209
7. Lawson ND, Vogel AM, Weinstein BM (2002) Sonic hedgehog and vascular endothelial growth factor act upstream of the Notch pathway during arterial endothelial differentiation. Dev Cell 3:127-136
8. Fiedler U, Augustin HG (2006) Angiopoietins: a link between angiogenesis and inflammation. Trends Immunol 27:552-558
9. Kiefer F, Siekmann AF (2011) The role of chemokines and their receptors in angiogenesis. Cell Mol Life Sci 68:2811-2830
10. Nicosia RF, Ottinetti A (1990) Growth of microvessels in serum-free matrix culture of rat aorta. A quantitative assay of angiogenesis in vitro. Lab Invest 63:115-122
11. Gelati M, Aplin AC, Fogel E, Smith KD, Nicosia RF (2008) The angiogenic response of the aorta to injury and inflammatory cytokines requires macrophages. J Immunol 181:5711-5719
12. Aplin AC, Gelati M, Fogel E, Carnevale E, Nicosia RF (2006) Angiopoietin-1 and vascular endothelial growth factor induce expression of inflammatory cytokines before angiogenesis. Physiol Genomics 27:20-28
13. van Hinsbergh VW, Koolwijk P, Hanemaaijer R (1997) Role of fibrin and plasminogen activators in repair-associated angiogenesis: in vitro studies with human endothelial cells. EXS 79:391-411
14. Ligresti G, Aplin AC, Zorzi P, Morishita A, Nicosia RF (2011) Macrophage-derived tumor necrosis factor-alpha is an early component of the molecular cascade leading to angiogenesis in response to aortic injury. Arterioscler Thromb Vasc Biol 31:1151-1159
15. Kawai T, Akira S (2010) The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat Immunol 11:373-384
16. Beg AA (2002) Endogenous ligands of Toll-like receptors: implications for regulating inflammatory and immune responses. Trends Immunol 23:509-512
17. Jiang D, Liang J, Fan J, Yu S, Chen S, Luo Y, Prestwich GD, Mascarenhas MM, Garg HG, Quinn DA, Homer RJ, Goldstein DR, Bucala R, Lee PJ, Medzhitov R, Noble PW (2005) Regulation of lung injury and repair by Toll-like receptors and hyaluronan. Nat Med 11:1173-1179
18. Smith KD (2009) Toll-like receptors in kidney disease. Curr Opin Nephrol Hypertens 18:189-196
19. Cole JE, Georgiou E, Monaco C (2010) The expression and functions of Toll-Like receptors in atherosclerosis. Mediators Inflamm 2010:1-18
20. Pryshchep O, Ma-Krupa W, Younge BR, Goronzy JJ, Weyand CM (2008) Vessel-specific Toll-like receptor profiles in human medium and large arteries. Circulation 118:1276-1284
21. Fitzner N, Clauberg S, Essmann F, Liebmann J, Kolb-Bachofen V (2008) Human skin endothelial cells can express all 10 TLR genes and respond to respective ligands. Clin Vaccine Immunol 15:138-146
22. Kawai T, Akira S (2005) Toll-like receptor downstream signaling. Arthritis Res Ther 7:12-19
23. Han J (2006) MyD88 beyond Toll. Nat Immunol 7:370-371
24. O'Neill LA (2006) How Toll-like receptors signal: what we know and what we don't know. Curr Opin Immunol 18:3-9
25. Macedo L, Pinhal-Enfield G, Alshits V, Elson G, Cronstein BN, Leibovich SJ (2007) Wound healing is impaired in MyD88-deficient mice: a role for MyD88 in the regulation of wound healing by adenosine A2A receptors. Am J Pathol 171:1774-1788
26. Zhu WH, Nicosia RF (2002) The thin prep rat aortic ring assay: a modified method for the characterization of angiogenesis in whole mounts. Angiogenesis 5:81-86
27. Nicosia RF, Ligresti G, Aplin AC (2012) Preparation and analysis of aortic ring cultures for the study of angiogenesis ex vivo. In: Zudaire E, Cuttitta F (eds) The textbook of angiogenesis and lymphangiogenesis: methods and applications. Springer, Dordrecht, pp 127-148
28. Nicosia RF, Zhu WH (2004) Rat aortic ring assay of angiogenesis. In: Augustin H (ed) Methods in endothelial cell biology. Springer, Berlin, pp 125-144
29. Adachi O, Kawai T, Takeda K, Matsumoto M, Tsutsui H, Sakagami M, Nakanishi K, Akira S (1998) Targeted disruption of the MyD88 gene results in loss of IL-1- and IL-18-mediated function. Immunity 9:143-150
30. Aplin AC, Fogel E, Zorzi P, Nicosia RF (2008) The aortic ring model of angiogenesis. Methods Enzymol 443:119-136
31. Nicosia RF, Villaschi S (1995) Rat aortic smooth muscle cells become pericytes during angiogenesis in vitro. Lab Invest 73:658-666
32. Zhu WH, Han J, Nicosia RF (2003) Requisite role of p38 MAPK in mural cell recruitment during angiogenesis in the rat aorta model. J Vasc Res 40:140-148
33. Aplin AC, Fogel E, Nicosia RF (2010) MCP-1 promotes mural cell recruitment during angiogenesis in the aortic ring model. Angiogenesis 13:219-226
34. Nicosia RF, Villaschi S, Smith M (1994) Isolation and characterization of vasoformative endothelial cells from the rat aorta. In Vitro Cell Dev Biol Anim 30A:394-399
35. Villaschi S, Nicosia RF, Smith MR (1994) Isolation of a morphologically and functionally distinct smooth muscle cell type from the intimal aspect of the normal rat aorta. Evidence for smooth muscle cell heterogeneity. In Vitro Cell Dev Biol Anim 30A:589-595
36. Zorzi P, Aplin AC, Smith KD, Nicosia RF (2010) Technical advance: the rat aorta contains resident mononuclear phagocytes with proliferative capacity and proangiogenic properties. J Leukoc Biol 88:1051-1059
37. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25:402-408
38. Nicosia RF, Zorzi P, Ligresti G, Morishita A, Aplin AC (2011) Paracrine regulation of angiogenesis by different cell types in the aorta ring model. Int J Dev Biol 55:447-453
39. Zhang Q, Raoof M, Chen Y, Sumi Y, Sursal T, Junger W, Brohi K, Itagaki K, Hauser CJ (2010) Circulating mitochondrial DAMPs cause inflammatory responses to injury. Nature 464:104-107
40. Carnevale E, Fogel E, Aplin AC, Gelati M, Howson KM, Zhu WH, Nicosia RF (2007) Regulation of postangiogenic neovessel survival by beta1 and beta3 integrins in collagen and fibrin matrices. J Vasc Res 44:40-50
41. Klinman DM, Takeshita F, Gursel I, Leifer C, Ishii KJ, Verthelyi D, Gursel M (2002) CpG DNA: recognition by and activation of monocytes. Microbes Infect 4:897-901
42. Heynekamp JJ, Weber WM, Hunsaker LA, Gonzales AM, Orlando RA, Deck LM, Jagt DL (2006) Substituted trans-stilbenes, including analogues of the natural product resveratrol, inhibit the human tumor necrosis factor alpha-induced activation of transcription factor nuclear factor kappaB. J Med Chem 49:7182-7189
43. Nicosia RF (2009) The aortic ring model of angiogenesis: a quarter century of search and discovery. J Cell Mol Med 13:4113-4136
44. Grote K, Schutt H, Schieffer B (2011) Toll-like receptors in angiogenesis. ScientificWorldJournal 11:981-991
45. Schirbel A, Kessler S, Rieder F, West G, Rebert N, Asosingh K, McDonald C, Fiocchi C (2013) Pro-angiogenic activity of TLRs and NLRs: a novel link between gut microbiota and intestinal angiogenesis. Gastroenterology 144:613-623
46. Moreno PR, Purushothaman M, Purushothaman KR (2012) Plaque neovascularization: defense mechanisms, betrayal, or a war in progress. Ann N Y Acad Sci 1254:7-17
47. Michelsen KS, Wong MH, Shah PK, Zhang W, Yano J, Doherty TM, Akira S, Rajavashisth TB, Arditi M (2004) Lack of Toll-like receptor 4 or myeloid differentiation factor 88 reduces atherosclerosis and alters plaque phenotype in mice deficient in apolipoprotein E. Proc Natl Acad Sci USA 101:10679-10684
48. Mullick AE, Tobias PS, Curtiss LK (2005) Modulation of atherosclerosis in mice by Toll-like receptor 2. J Clin Invest 115:3149-3156
49. Yu M, Wang H, Ding A, Golenbock DT, Latz E, Czura CJ, Fenton MJ, Tracey KJ, Yang H (2006) HMGB1 signals through toll-like receptor (TLR) 4 and TLR2. Shock 26:174-179
50. Lotfi R, Eisenbacher J, Solgi G, Fuchs K, Yildiz T, Nienhaus C, Rojewski MT, Schrezenmeier H (2011) Human mesenchymal stem cells respond to native but not oxidized damage associated molecular pattern molecules from necrotic (tumor) material. Eur J Immunol 41:2021-2028
51. Lin Q, Yang XP, Fang D, Ren X, Zhou H, Fang J, Liu X, Zhou S, Wen F, Yao X, Wang JM, Su SB (2011) High-mobility group box-1 mediates toll-like receptor 4-dependent angiogenesis. Arterioscler Thromb Vasc Biol 31:1024-1032
52. Leibovich SJ, Chen JF, Pinhal-Enfield G, Belem PC, Elson G, Rosania A, Ramanathan M, Montesinos C, Jacobson M, Schwarzschild MA, Fink JS, Cronstein B (2002) Synergistic up-regulation of vascular endothelial growth factor expression in murine macrophages by adenosine A(2A) receptor agonists and endotoxin. Am J Pathol 160:2231-2244
53. Li WW, Grayson G, Folkman J, D'Amore PA (1991) Sustained-release endotoxin. A model for inducing corneal neovascularization. Invest Ophthalmol Vis Sci 32:2906-2911
54. Mattsby-Baltzer I, Jakobsson A, Sorbo J, Norrby K (1994) Endotoxin is angiogenic. Int J Exp Pathol 75:191-196
55. Polverini PJ, Leibovich SJ (1984) Induction of neovascularization in vivo and endothelial proliferation in vitro by tumor-associated macrophages. Lab Invest 51:635-642
56. Pollet I, Opina CJ, Zimmerman C, Leong KG, Wong F, Karsan A (2003) Bacterial lipopolysaccharide directly induces angiogenesis through TRAF6-mediated activation of NF-kappaB and c-Jun N-terminal kinase. Blood 102:1740-1742
57. Rodriguez-Martinez S, Cancino-Diaz ME, Miguel PS, Cancino-Diaz JC (2006) Lipopolysaccharide from Escherichia coli induces the expression of vascular endothelial growth factor via toll-like receptor 4 in human limbal fibroblasts. Exp Eye Res 83:1373-1377
58. Kim CO, Huh AJ, Kim MS, Chin BS, Han SH, Choi SH, Jeong SJ, Choi HK, Choi JY, Song YG, Kim JM (2008) LPS-induced vascular endothelial growth factor expression in rat lung pericytes. Shock 30:92-97
59. Xaus J, Comalada M, Valledor AF, Lloberas J, Lopez-Soriano F, Argiles JM, Bogdan C, Celada A (2000) LPS induces apoptosis in macrophages mostly through the autocrine production of TNF-alpha. Blood 95:3823-3831
60. Majde JA (1993) Microbial cell-wall contaminants in peptides: a potential source of physiological artifacts. Peptides 14:629-632
61. Watanabe A, Hashmi A, Gomes DA, Town T, Badou A, Flavell RA, Mehal WZ (2007) Apoptotic hepatocyte DNA inhibits hepatic stellate cell chemotaxis via toll-like receptor 9. Hepatology 46:1509-1518
62. Utaisincharoen P, Kespichayawattana W, Anuntagool N, Chaisuriya P, Pichyangkul S, Krieg AM, Sirisinha S (2003) CpG ODN enhances uptake of bacteria by mouse macrophages. Clin Exp Immunol 132:70-75
63. Deng J, Ma-Krupa W, Gewirtz AT, Younge BR, Goronzy JJ, Weyand CM (2009) Toll-like receptors 4 and 5 induce distinct types of vasculitis. Circ Res 104:488-495
64. Weyand CM, Liao YJ, Goronzy JJ (2012) The immunopathology of giant cell arteritis: diagnostic and therapeutic implications. J Neuroophthalmol 32:259-265