Angiogenesis Modulation by Arachidonic Acid-derived Lipids: Positive and Negative Regulators of Angiogenesis

  • Robert C. Block
  • Murat Yalcin
  • Mathangi Srinivasan
  • Steve Georas
  • Shaker A. Mousa
Chapter

Abstract

Arachidonic acid-derived lipids such as 15 deoxy-PGJ2 or 15 epi-lipoxin A4 have been shown to be potent anti-angiogenesis agents regardless of the angiogenesis stimulus. Other arachidonic acid-derived mediators differentially stimulate angiogenesis and the balance among the different arachidonic acid metabolites along their interactions might play an important role in angiogenesis hemostasis in various angiogenesis-associated disorders.

Keywords

Sudden Cardiac Death Human Umbilical Vein Endothelial Cell Lipid Mediator Vascular Endothelial Cell Growth Factor Epoxyeicosatrienoic Acid 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. 1.
    Smith SC Jr, Allen J, Blair SN, Bonow RO, Brass LM, Fonarow GC, Grundy SM, Hiratzka L, Jones D, Krumholz HM, Mosca L, Pasternak RC, Pearson T, Pfeffer MA, Taubert KA (2006) AHA/ACC guidelines for secondary prevention for patients with coronary and other atherosclerotic vascular disease: 2006 update: endorsed by the National Heart, Lung, and Blood Institute. Circulation 113(19):2363–2372PubMedCrossRefGoogle Scholar
  2. 2.
    Yusuf S, Reddy S, Ounpuu S, Anand S (2001) Global burden of cardiovascular diseases: Part I: general considerations, the epidemiologic transition, risk factors, and impact of urbanization. Circulation 104(22):2746–2753PubMedCrossRefGoogle Scholar
  3. 3.
    Grundy SM, Cleeman JI, Merz CN, Brewer HB Jr, Clark LT, Hunninghake DB, Pasternak RC, Smith SC Jr, Stone NJ (2004) Implications of recent clinical trials for the national cholesterol education program adult treatment panel III guidelines. Circulation 110(2):227–239PubMedCrossRefGoogle Scholar
  4. 4.
    Zheng ZJ, Croft JB, Giles WH, Mensah GA (2001) Sudden cardiac death in the United States, 1989–1998. Circulation 104(18):2158–2163PubMedCrossRefGoogle Scholar
  5. 5.
    Albert CM, Chae CU, Grodstein F, Rose LM, Rexrode KM, Ruskin JN, Stampfer MJ, Manson JE (2003) Prospective study of sudden cardiac death among women in the United States. Circulation 107(16):2096–2101PubMedCrossRefGoogle Scholar
  6. 6.
    Anderson RN (2001) Deaths: leading causes for 1999. Natl Vital Stat Rep 49(11):1–87Google Scholar
  7. 7.
    Fuster V, Moreno PR, Fayad ZA, Corti R, Badimon JJ (2005) Atherothrombosis and high-risk plaque: Part I: evolving concepts. J Am Coll Cardiol 46(6):937–954PubMedCrossRefGoogle Scholar
  8. 8.
    Jemal A, Ward E, Hao Y, Thun M (2005) Trends in the leading causes of death in the United States, 1970–2002. JAMA 294(10):1255–1259PubMedCrossRefGoogle Scholar
  9. 9.
    Jemal A, Tiwari RC, Murray T, Ghafoor A, Samuels A, Ward E, Feuer EJ, Thun MJ (2004) Cancer statistics. CA Cancer J Clin 54(1):8–29PubMedCrossRefGoogle Scholar
  10. 10.
    Gralow J, Ozols RF, Bajorin DF, Cheson BD, Sandler HM, Winer EP, Bonner J, Demetri GD, Curran W Jr, Ganz PA, Kramer BS, Kris MG, Markman M, Mayer RJ, Raghavan D, Ramsey S, Reaman GH, Sawaya R, Schuchter LM, Sweetenham JW, Vahdat LT, Davidson NE, Schilsky RL, Lichter AS (2008) Clinical cancer advances 2007: major research advances in cancer treatment, prevention, and screening–a report from the American Society of Clinical Oncology. J Clin Oncol 26(2):313–325PubMedCrossRefGoogle Scholar
  11. 11.
    Ishii I, Fukushima N, Ye X, Chun J (2004) Lysophospholipid receptors: signaling and biology. Annu Rev Biochem 73:321–354PubMedCrossRefGoogle Scholar
  12. 12.
    Khurana R, Simons M, Martin JF, Zachary IC (2005) Role of angiogenesis in cardiovascular disease: a critical appraisal. Circulation 112(12):1813–1824PubMedCrossRefGoogle Scholar
  13. 13.
    O’Brien ER, Garvin MR, Dev R, Stewart DK, Hinohara T, Simpson JB, Schwartz SM (1994) Angiogenesis in human coronary atherosclerotic plaques. Am J Pathol 145(4):883–894PubMedGoogle Scholar
  14. 14.
    Sueishi K, Yonemitsu Y, Nakagawa K, Kaneda Y, Kumamoto M, Nakashima Y (1997) Atherosclerosis and angiogenesis. Its pathophysiological significance in humans as well as in an animal model induced by the gene transfer of vascular endothelial growth factor. Ann N Y Acad Sci 811(311–322):322–314Google Scholar
  15. 15.
    Simons M, Ware JA (2003) Therapeutic angiogenesis in cardiovascular disease. Nat Rev Drug Discov 2(11):863–871PubMedCrossRefGoogle Scholar
  16. 16.
    Celletti FL, Waugh JM, Amabile PG, Brendolan A, Hilfiker PR, Dake MD (2001) Vascular endothelial growth factor enhances atherosclerotic plaque progression. Nat Med 7(4):425–429PubMedCrossRefGoogle Scholar
  17. 17.
    Moulton KS, Heller E, Konerding MA, Flynn E, Palinski W, Folkman J (1999) Angiogenesis inhibitors endostatin or TNP-470 reduce intimal neovascularization and plaque growth in apolipoprotein E-deficient mice. Circulation 99(13):1726–1732PubMedCrossRefGoogle Scholar
  18. 18.
    Cuthbertson WF (1976) Essential fatty acid requirements in infancy. Am J Clin Nutr 29(5):559–568PubMedGoogle Scholar
  19. 19.
    Tapiero H, Ba GN, Couvreur P, Tew KD (2002) Polyunsaturated fatty acids (PUFA) and eicosanoids in human health and pathologies. Biomed Pharmacother 56(5):215–222PubMedCrossRefGoogle Scholar
  20. 20.
    Iniguez MA, Cacheiro-Llaguno C, Cuesta N, Diaz-Munoz MD, Fresno M (2008) Prostanoid function and cardiovascular disease. Arch Physiol Biochem 114(3):201–209PubMedCrossRefGoogle Scholar
  21. 21.
    Calder PC (2006) N-3 polyunsaturated fatty acids, inflammation, and inflammatory diseases. Am J Clin Nutr 83(6 Suppl):1505S–1519SPubMedGoogle Scholar
  22. 22.
    Gauthier KM, Yang W, Gross GJ, Campbell WB (2007 Dec) Roles of epoxyeicosatrienoic acids in vascular regulation and cardiac preconditioning. J Cardiovasc Pharmacol 50(6):601–608PubMedCrossRefGoogle Scholar
  23. 23.
    Wray J, Bishop-Bailey D (2008) Epoxygenases and peroxisome proliferator-activated receptors in mammalian vascular biology. Exp Physiol 93(1):148–154PubMedCrossRefGoogle Scholar
  24. 24.
    Levick SP, Loch DC, Taylor SM, Janicki JS (2007) Arachidonic acid metabolism as a potential mediator of cardiac fibrosis associated with inflammation. J Immunol 178(2):641–646PubMedGoogle Scholar
  25. 25.
    Aoki J (2004) Mechanisms of lysophosphatidic acid production. Semin Cell Dev Biol 15(5):477–489PubMedCrossRefGoogle Scholar
  26. 26.
    Serhan CN, Chiang N, Van Dyke TE (2008) Resolving inflammation: dual anti-inflammatory and pro-resolution lipid mediators. Nat Rev Immunol 8(5):349–361PubMedCrossRefGoogle Scholar
  27. 27.
    Hjelte LE, Nilsson A (2005) Arachidonic acid and ischemic heart disease. J Nutr 135(9):2271–2273PubMedGoogle Scholar
  28. 28.
    Glew RH, Okolie H, Huang YS, Chuang LT, Suberu O, Crossey M, VanderJagt DJ (2004) Abnormalities in the fatty-acid composition of the serum phospholipids of stroke patients. J Natl Med Assoc 96(6):826–832PubMedGoogle Scholar
  29. 29.
    Pozzi A, Macias-Perez I, Abair T, Wei S, Su Y, Zent R, Falck JR, Capdevila JH (2005) Characterization of 5,6- and 8,9-epoxyeicosatrienoic acids (5,6- and 8,9-EET) as potent in vivo angiogenic lipids. J Biol Chem 280(29):27138–27146PubMedCrossRefGoogle Scholar
  30. 30.
    Mills GB, Moolenaar WH (2003) The emerging role of lysophosphatidic acid in cancer. Nat Rev Cancer 3(8):582–591PubMedCrossRefGoogle Scholar
  31. 31.
    Cezar-de-Mello PF, Vieira AM, Nascimento-Silva V, Villela CG, Barja-Fidalgo C, Fierro IM (2008) ATL-1, an analogue of aspirin-triggered lipoxin A4, is a potent inhibitor of several steps in angiogenesis induced by vascular endothelial growth factor. Br J Pharmacol 153(5):956–965PubMedCrossRefGoogle Scholar
  32. 32.
    Xin X, Yang S, Kowalski J, Gerritsen ME (1999) Peroxisome proliferator-activated receptor gamma ligands are potent inhibitors of angiogenesis in vitro and in vivo. J Biol Chem 274(13):9116–9121PubMedCrossRefGoogle Scholar
  33. 33.
    Fleming I (2007) Epoxyeicosatrienoic acids, cell signaling and angiogenesis. Prostaglandins Other Lipid Mediat 82(1–4):60–67PubMedCrossRefGoogle Scholar
  34. 34.
    Spector AA (2009) Arachidonic acid cytochrome P450 epoxygenase pathway. J Lipid Res 50(Suppl):S52–56PubMedCrossRefGoogle Scholar
  35. 35.
    Pozzi A, Popescu V, Yang S, Mei S, Shi M, Puolitaival SM, Caprioli RM, Capdevila JH (2010) The anti-tumorigenic properties of peroxisomal proliferator-activated receptor alpha are arachidonic acid epoxygenase-mediated. J Biol Chem 285(17):12840–12850PubMedCrossRefGoogle Scholar
  36. 36.
    Webler AC, Michaelis UR, Popp R, Barbosa-Sicard E, Murugan A, Falck JR, Fisslthaler B, Fleming I (2008) Epoxyeicosatrienoic acids are part of the VEGF-activated signaling cascade leading to angiogenesis. Am J Physiol Cell Physiol 295(5):C1292–1301PubMedCrossRefGoogle Scholar
  37. 37.
    Michaelis UR, Falck JR, Schmidt R, Busse R, Fleming I (2005) Cytochrome P4502C9-derived epoxyeicosatrienoic acids induce the expression of cyclooxygenase-2 in endothelial cells. Arterioscler Thromb Vasc Biol 25(2):321–326PubMedCrossRefGoogle Scholar
  38. 38.
    Wu WT, Chen CN, Lin CI, Chen JH, Lee H (2005) Lysophospholipids enhance matrix metalloproteinase-2 expression in human endothelial cells. Endocrinology 146(8):3387–3400PubMedCrossRefGoogle Scholar
  39. 39.
    Gerrard JM, Robinson P (1989) Identification of the molecular species of lysophosphatidic acid produced when platelets are stimulated by thrombin. Biochim Biophys Acta 1001(3):282–285PubMedCrossRefGoogle Scholar
  40. 40.
    Gaits F, Fourcade O, Le Balle F, Gueguen G, Gaige B, Gassama-Diagne A, Fauvel J, Salles JP, Mauco G, Simon MF, Chap H (1997) Lysophosphatidic acid as a phospholipid mediator: pathways of synthesis. FEBS Lett 410(1):54–58PubMedCrossRefGoogle Scholar
  41. 41.
    Lee H, Liao JJ, Graeler M, Huang MC, Goetzl EJ (2002) Lysophospholipid regulation of mononuclear phagocytes. Biochim Biophys Acta 1582(1–3):175–177PubMedGoogle Scholar
  42. 42.
    Shen Z, Belinson J, Morton RE, Xu Y (1998) Phorbol 12-myristate 13-acetate stimulates lysophosphatidic acid secretion from ovarian and cervical cancer cells but not from breast or leukemia cells. Gynecol Oncol 71(3):364–368PubMedCrossRefGoogle Scholar
  43. 43.
    Zhang C, Baker DL, Yasuda S, Makarova N, Balazs L, Johnson LR, Marathe GK, McIntyre TM, Xu Y, Prestwich GD, Byun HS, Bittman R, Tigyi G (2004) Lysophosphatidic acid induces neointima formation through PPARgamma activation. J Exp Med 199(6):763–774PubMedCrossRefGoogle Scholar
  44. 44.
    Zhao Y, Natarajan V (2009) Lysophosphatidic acid signaling in airway epithelium: role in airway inflammation and remodeling. Cell Signal 21(3):367–377PubMedCrossRefGoogle Scholar
  45. 45.
    Prestwich GD, Gajewiak J, Zhang H, Xu X, Yang G, Serban M (2008) Phosphatase-resistant analogues of lysophosphatidic acid: agonists promote healing, antagonists and autotaxin inhibitors treat cancer. Biochim Biophys Acta 1781(9):588–594PubMedCrossRefGoogle Scholar
  46. 46.
    Bektas M, Payne SG, Liu H, Goparaju S, Milstien S, Spiegel S (2005) A novel acylglycerol kinase that produces lysophosphatidic acid modulates cross talk with EGFR in prostate cancer cells. J Cell Biol 169(5):801–811PubMedCrossRefGoogle Scholar
  47. 47.
    Spiegel S, Merrill AH Jr (1996) Sphingolipid metabolism and cell growth regulation. FASEB J 10(12):1388–1397PubMedGoogle Scholar
  48. 48.
    Panchatcharam M, Miriyala S, Yang F, Rojas M, End C, Vallant C, Dong A, Lynch K, Chun J, Morris AJ, Smyth SS (2008) Lysophosphatidic acid receptors 1 and 2 play roles in regulation of vascular injury responses but not blood pressure. Circ Res 103(6):662–670PubMedCrossRefGoogle Scholar
  49. 49.
    Moolenaar WH (1999) Bioactive lysophospholipids and their G protein-coupled receptors. Exp Cell Res 253(1):230–238PubMedCrossRefGoogle Scholar
  50. 50.
    An S, Bleu T, Zheng Y, Goetzl EJ (1998) Recombinant human G protein-coupled lysophosphatidic acid receptors mediate intracellular calcium mobilization. Mol Pharmacol 54(5):881–888PubMedGoogle Scholar
  51. 51.
    Tigyi G, Fischer DJ, Sebok A, Marshall F, Dyer DL, Miledi R (1996) Lysophosphatidic acid-induced neurite retraction in PC12 cells: neurite-protective effects of cyclic amp signaling. J Neurochem 66(2):549–558PubMedCrossRefGoogle Scholar
  52. 52.
    Stahle M, Veit C, Bachfischer U, Schierling K, Skripczynski B, Hall A, Gierschik P, Giehl K (2003) Mechanisms in LPA-induced tumor cell migration: critical role of phosphorylated ERK. J Cell Sci 116(Pt 18):3835–3846PubMedCrossRefGoogle Scholar
  53. 53.
    Seewald S, Schmitz U, Seul C, Ko Y, Sachinidis A, Vetter H (1999) Lysophosphatidic acid stimulates protein kinase C isoforms alpha, beta, epsilon, and zeta in a pertussis toxin sensitive pathway in vascular smooth muscle cells. Am J Hypertens 12(5):532–537PubMedCrossRefGoogle Scholar
  54. 54.
    Hayashi K, Takahashi M, Nishida W, Yoshida K, Ohkawa Y, Kitabatake A, Aoki J, Arai H, Sobue K (2001) Phenotypic modulation of vascular smooth muscle cells induced by unsaturated lysophosphatidic acids. Circ Res 89(3):251–258PubMedCrossRefGoogle Scholar
  55. 55.
    Yoshida K, Nishida W, Hayashi K, Ohkawa Y, Ogawa A, Aoki J, Arai H, Sobue K (2003) Vascular remodeling induced by naturally occurring unsaturated lysophosphatidic acid in vivo. Circulation 108(14):1746–1752PubMedCrossRefGoogle Scholar
  56. 56.
    Fierro IM, Kutok JL, Serhan CN (2002) Novel lipid mediator regulators of endothelial cell proliferation and migration: aspirin-triggered-15R-lipoxin A(4) and lipoxin A(4). J Pharmacol Exp Ther 300(2):385–392PubMedCrossRefGoogle Scholar
  57. 57.
    Cezar-de-Mello PF, Nascimento-Silva V, Villela CG, Fierro IM (2006) Aspirin-triggered lipoxin A4 inhibition of VEGF-induced endothelial cell migration involves actin polymerization and focal adhesion assembly. Oncogene 25(1):122–129PubMedGoogle Scholar
  58. 58.
    Pouliot M, Serhan CN (1999) Lipoxin A4 and aspirin-triggered 15-epi-LXA4 inhibit tumor necrosis factor-alpha-initiated neutrophil responses and trafficking: novel regulators of a cytokine-chemokine axis relevant to periodontal diseases. J Periodontal Res 34(7):370–373PubMedCrossRefGoogle Scholar
  59. 59.
    Hachicha M, Pouliot M, Petasis NA, Serhan CN (1999) Lipoxin (LX)A4 and aspirin-triggered 15-epi-LXA4 inhibit tumor necrosis factor 1alpha-initiated neutrophil responses and trafficking: regulators of a cytokine-chemokine axis. J Exp Med 189(12):1923–1930PubMedCrossRefGoogle Scholar
  60. 60.
    Gewirtz AT, McCormick B, Neish AS, Petasis NA, Gronert K, Serhan CN, Madara JL (1998) Pathogen-induced chemokine secretion from model intestinal epithelium is inhibited by lipoxin A4 analogs. J Clin Invest 101(9):1860–1869PubMedCrossRefGoogle Scholar
  61. 61.
    Teutsch SM, Cohen JT (2005) Health trade-offs from policies to alter fish consumption. Am J Prev Med 29(4):324PubMedCrossRefGoogle Scholar
  62. 62.
    Takano T, Clish CB, Gronert K, Petasis N, Serhan CN (1998) Neutrophil-mediated changes in vascular permeability are inhibited by topical application of aspirin-triggered 15-epi-lipoxin A4 and novel lipoxin B4 stable analogues. J Clin Invest 101(4):819–826PubMedCrossRefGoogle Scholar
  63. 63.
    Imaizumi T, Matsumiya T, Tamo W, Shibata T, Fujimoto K, Kumagai M, Yoshida H, Cui XF, Tanji K, Hatakeyama M, Wakabayashi K, Satoh K (2002) 15-Deoxy-D12,14-prostaglandin J2 inhibits CX3CL1/fractalkine expression in human endothelial cells. Immunol Cell Biol 80(6):531–536PubMedCrossRefGoogle Scholar
  64. 64.
    Kim EH, Na HK, Surh YJ (2006) Upregulation of VEGF by 15-deoxy-delta12,14-prostaglandin J2 via heme oxygenase-1 and ERK1/2 signaling in MCF-7 cells. Ann N Y Acad Sci 1090:375–384PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Robert C. Block
    • 1
    • 2
  • Murat Yalcin
    • 3
    • 4
  • Mathangi Srinivasan
    • 3
  • Steve Georas
    • 5
  • Shaker A. Mousa
    • 3
  1. 1.Department of Public Health SciencesUniversity of Rochester School of Medicine and DentistryRochesterUSA
  2. 2.Division of Cardiology, Department of MedicineUniversity of Rochester School of Medicine and DentistryRochesterUSA
  3. 3.The Pharmaceutical Research Institute at Albany College of Pharmacy and Health SciencesRensselaerUSA
  4. 4.Veterinary Medicine Faculty, Department of PhysiologyUludag UniversityGorukle, BursaTurkey
  5. 5.Division of Pulmonary and Critical Care Medicine, Department of MedicineUniversity of Rochester School of Medicine and DentistryRochesterUSA

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