Lysophosphatidic acid suppresses endothelial cell CD36 expression and promotes angiogenesis via a PKD-1-dependent signaling pathway

Blood

Volumn 117, Issue 22, 2011, Pages 6036-6045

  Ren, Bin ^a   Hale, James ^a,b   Srikanthan, Sowmya ^a,c   Silverstein, Roy L ^a,c  

^a LERNER RESEARCH INSTITUTE   (United States)

^b CLEVELAND STATE UNIVERSITY   (United States)

^c CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD36 ANTIGEN; FIBROBLAST GROWTH FACTOR 2; LYSOPHOSPHATIDIC ACID; MATRIGEL; POLYCYSTIN 1; THROMBOSPONDIN 1; VASCULOTROPIN RECEPTOR 2;

ANGIOGENESIS; ANIMAL CELL; ANTIANGIOGENIC ACTIVITY; ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; MICROVASCULAR ENDOTHELIAL CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; RECEPTOR DOWN REGULATION; SIGNAL TRANSDUCTION;

EID: 79957982626     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2010-12-326017     Document Type: Article

References (48)

1. Folkman J. Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat Med. 1995;1(1):27-31.
2. Ren B, Yee KO, Lawler J, Khosravi-Far R. Regulation of tumor angiogenesis by thrombospondin-1. Biochim Biophys Acta. 2006;1765(2):178-188.
3. Simantov R, Febbraio M, Crombie R, Asch AS, Nachman RL, Silverstein RL. Histidine-rich glycoprotein inhibits the antiangiogenic effect of thrombospondin-1. J Clin Invest. 2001;107(1):45-52. (Pubitemid 32047413)
4. Jiménez B, Volpert OV, Crawford SE, Febbraio M, Silverstein RL, Bouck N. Signals leading to apoptosis-dependent inhibition of neovascularization by thrombospondin-1. Nat Med. 2000;6(1):41-48. (Pubitemid 30048524)
5. Simantov R, Febbraio M, Silverstein RL. The anti-angiogenic effect of thrombospondin-2 is mediated by CD36 and inhibited by histidinerich glycoprotein. Matrix Biol. 2005;24(1):27-34. (Pubitemid 40320896)
6. Kaur B, Cork SM, Sandberg EM, et al. Vasculostatin inhibits intracranial glioma growth and negatively regulates in vivo angiogenesis through a CD36-dependent mechanism. Cancer Res. 2009;69(3):1212-1220.
7. Klenotic PA, Huang P, Palomo J, et al. Histidinerich glycoprotein modulates the anti-angiogenic effects of vasculostatin. Am J Pathol. 2010;176(4):2039-2050.
8. DawsonDW, Pearce SF, Zhong R, Silverstein RL, Frazier WA, Bouck NP. CD36 mediates the in vitro inhibitory effects of thrombospondin-1 on endothelial cells. J Cell Biol. 1997;138(3):707-717. (Pubitemid 27349849)
9. Silverstein RL, Febbraio M. CD36, a scavenger receptor involved in immunity, metabolism, angiogenesis, and behavior. Sci Signal. 2009;2(72):re3.
10. Febbraio M, Hajjar DP, Silverstein RL. CD36: a class B scavenger receptor involved in angiogenesis, atherosclerosis, inflammation and lipid metabolism. J Clin Invest. 2001;108(6):785-791. (Pubitemid 32880285)
11. Febbraio M, Podrez EA, Smith JD, et al. Targeted disruption of the class B scavenger receptor, CD36, protects against atherosclerotic lesion development in mice. J Clin Invest. 2000;105(8):1049-1056. (Pubitemid 30217689)
12. Podrez EA, Byzova TV, Febbraio M, et al. Platelet CD36 links hyperlipidemia, oxidant stress and a pro-thrombotic phenotype. Nat Med. 2007;13(9):1086-1095. (Pubitemid 47517507)
13. Kennedy DJ, Kuchibhotla S, Westfall KM, Silverstein RL, Morton RE, Febbraio M. CD36 mediates a pro-inflammatory signaling loop in fat and contributes to insulin resistance. Cardiovasc Res. 2011;89(3):604-613.
14. Rege TA, Stewart J Jr, Dranka B, Benveniste EN, Silverstein RL, Gladson CL. Thrombospondin-1-induced apoptosis of brain microvascular endothelial cells can be mediated by TNF-R1. J Cell Physiol. 2009;218(1):94-103.
15. Volpert OV, Zaichuk T, Zhou W, et al. Inducer-stimulated Fas targets activated endothelium for destruction by anti-angiogenic thrombospondin-1 and pigment epithelium-derived factor. Nat Med. 2002;8(4):349-357. (Pubitemid 34407029)
16. Ren B, Song K, Parangi S, et al. A double hit to kill tumor and endothelial cells by TRAIL and antiangiogenic 3TSR. Cancer Res. 2009;69(9):3856-3865.
17. Huh HY, Pearce SF, Yesner LM, Schindler JL, Silverstein RL. Regulated expression of CD36 during monocyte-to-macrophage differentiation: potential role of CD36 in foam cell formation. Blood. 1996;87(5):2020-2028. (Pubitemid 26068918)
18. Feng J, Han J, Pearce SF, et al. Induction of CD36 expression by oxidized LDL and IL-4 by a common signaling pathway dependent on protein kinase C and PPAR-gamma. J Lipid Res. 2000;41(5):688-696.
19. Mwaikambo BR, Yang C, Chemtob S, Hardy P. Hypoxia up-regulates CD36 expression and function via hypoxia-inducible factor-1- and phosphatidylinositol 3-kinase-dependent mechanisms. J Biol Chem. 2009;284(39):26695-26707.
20. Morris AJ, Panchatcharam M, Cheng HY, et al. Regulation of blood and vascular cell function by bioactive lysophospholipids. J Thromb Haemost. 2009;7(S1):38-43.
21. Rivera-Lopez CM, Tucker AL, Lynch KR. Lysophosphotidic acid (LPA) and angiogenesis. Angiogenesis. 2008;11(3):301-310.
22. Nam SW, Clair T, Kim YS, et al. Autotaxin (NPP-2), a metastasis-enhancing motogen, is an angiogenic factor. Cancer Res. 2001;61(18):6938-6944. (Pubitemid 32896522)
23. Ren B, Deng Y, Mukhopadhyay A, et al. ERK1/2-Akt1 crosstalk regulates arteriogenesis in mice and zebrafish. J Clin Invest. 2010;120(4):1217-1228.
24. Zhang MX, Ou H, Shen YH, et al. Regulation of endothelial nitric oxide synthase by small RNA. Proc Natl Acad Sci U S A. 2005;102(47):16967-16972. (Pubitemid 41692667)
25. Tigyi G, Parrill A. Molecular mechanisms of lysophosphatidic acid action. Prog. Lipid Res. 2003;42(6):498-526. (Pubitemid 37237637)
26. Taylor CJ, Motamed K, Lilly B. Protein kinase C and downstream signaling pathways in a three-dimensional model of phorbol ester-induced angiogenesis. Angiogenesis. 2006;9(2):39-51. (Pubitemid 44444802)
27. Ha CH, Wang W, Jhun BS, et al. Protein kinase D-dependent phosphorylation and nuclear export of histone deacetylase 5 mediates vascular endothelial growth factor-induced gene expression and angiogenesis. J Biol Chem. 2008;283(21):14590-14599.
28. Sharlow ER, Giridhar KV, LaValle CR, et al. Potent and selective disruption of protein kinase D functionality by a benzoxoloazepinolone. J Biol Chem. 2008;283(48):33516-33526.
29. Ruiz-Velasco N, Domínguez A, Vega MA. Statins upregulate CD36 expression in human monocytes, an effect strengthened when combined with PPAR-gamma ligands putative contribution of Rho GTPases in statin-induced CD36 expression. Biochem Pharmacol. 2004;67(2):303-313. (Pubitemid 38112761)
30. Murakami M, Simons M. Fibroblast growth factor regulation of neovascularization. Curr Opin Hematol. 2008;15(3):215-220. (Pubitemid 351507574)
31. Zhang X, Kazerounian S, Duquette M, et al. Thrombospondin-1 modulates vascular endothelial growth factor activity at the receptor level. FASEB J. 2009;23(10):3368-3376.
32. Tsuchida T, Kijima H, Tokunaga T, et al. Expression of the thrombospondin-1 receptor CD36 is correlated with decreased stromal vascularization in colon cancer. Int J Oncol. 1999;14(1):47-51.
33. Chen CN, Lin JJ, Chen JJ, et al. Gene expression profile predicts patient survival of gastric cancer after surgical resection. J Clin Oncol. 2005;23(29):7286-7295. (Pubitemid 46202342)
34. Aoki J. Mechanisms of lysophosphatidic acid production. Semin Cell Dev Biol. 2004;15(5):477-489. (Pubitemid 38953944)
35. Liu S, Umezu-Goto M, Murph M, et al. Expression of autotaxin and lysophosphatidic acid receptors increases mammary tumorigenesis, invasion, and metastases. Cancer Cell. 2009;15(6):539-550.
36. Mills BG, Moolenaar WH. The emerging role of lysophosphatidic acid in cancer. Nat Rev Cancer. 2003;3(8):582-591. (Pubitemid 37328830)
37. Siess W, Zangl KJ, Essler M, et al. Lysophosphatidic acid mediates the rapid activation of platelets and endothelial cells by mildly oxidized low density lipoprotein and accumulates in human atherosclerotic lesions. Proc Natl Acad Sci U S A. 1999;96(12):6931-6936. (Pubitemid 29274987)
38. Zhang C, Baker DL, Yasuda S, et al. Lysophosphatidic acid induces neointima formation through PPARgamma activation. J Exp Med. 2004;199(6):763-774. (Pubitemid 38375196)
39. Lee H, Goetzl EJ, An S. Lysophosphatidic acid and sphingosine 1-phosphate stimulate endothelial cell wound healing. Am J Physiol Cell Physiol. 2000;278(3):C612-C618. (Pubitemid 30154941)
40. English D, Kovala AT, Welch Z, et al. Induction of endothelial cell chemotaxis by sphingosine 1-phosphate and stabilization of endothelial monolayer barrier function by lysophosphatidic acid, potential mediators of hematopoietic angiogenesis. J Hematother Stem Cell Res. 1999;8(6):627-634. (Pubitemid 30041245)
41. Hu X, Mendoza FJ, Sun J, Banerji V, Johnston JB, Gibson SB. Lysophosphatidic acid (LPA) induces the expression of VEGF leading to protection against apoptosis in B-cell derived malignancies. Cell Signal. 2008;20(6):1198-1208.
42. An S, Bleu T, Hallmark OG, Goetzl EJ. Characterization of a novel subtype of human G protein coupled receptor for lysophosphatidic acid. J Biol Chem. 1998;273(14):7906-7910.
43. Bandoh K, Aoki J, Hosono H, et al. Molecular cloning and characterization of a novel human G-protein-coupled receptor, EDG7, for lysophosphatidic acid. J Biol Chem. 1999;274(39):27776-27785.
44. Chiu T, Rozengurt E. PKD in intestinal epithelial cells: rapid activation by phorbol esters, LPA, and angiotensin through PKC. Am J Physiol Cell Physiol. 2001;280(4):C929-C942.
45. Matthews SA, Navarro MN, Sinclair LV, Emslie E, Feijoo-Carnero C, Cantrell DA. Unique functions for protein kinase D1 and protein kinase D2 in mammalian cells. Biochem J. 2010;432(1):153-163.
46. Rozengurt E, Rey O, Waldron RT. Protein kinase D signaling. J Biol Chem. 2005;280(14):13205-13208. (Pubitemid 40517202)
47. Qin L, Zeng H, Zhao D. Requirement of protein kinase D tyrosine phosphorylation for VEGF-A165-induced angiogenesis through its interaction and regulation of phospholipase Cgamma phosphorylation. J Biol Chem. 2006;281(43):32550-32558. (Pubitemid 46036810)
48. Wong C, Jin ZG. Protein kinase C-dependent protein kinase D activation modulates ERK signal pathway and endothelial cell proliferation by vascular endothelial growth factor. J Biol Chem. 2005;280(39):33262-33269. (Pubitemid 41397122)