High density lipoprotein stimulated migration of macrophages depends on the scavenger receptor class B, Type I, PDZK1 and Akt1 and is blocked by sphingosine 1 phosphate receptor antagonists

PLoS ONE

Volumn 9, Issue 9, 2014, Pages

  Al Jarallah, Aishah ^a   Chen, Xing ^a   González, Leticia ^a   Trigatti, Bernardo L ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

2 AMINO 2 (3 OCTYLPHENYLCARBAMOYL)ETHYL PHOSPHATE; 5 (4 PHENYL 5 TRIFLUOROMETHYL 2 THIENYL) 3 (3 TRIFLUOROMETHYLPHENYL) 1,2,4 OXADIAZOLE; AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; AKT1 PROTEIN; FINGOLIMOD; HIGH DENSITY LIPOPROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; MONOCYTE CHEMOTACTIC PROTEIN 1; PDZ PROTEIN; PDZK1 PROTEIN; PERTUSSIS TOXIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN KINASE C; RHO KINASE; SCAVENGER RECEPTOR; SCAVENGER RECEPTOR B; SCAVENGER RECEPTOR CLASS TYPE 1; SPHINGOSINE 1 PHOSPHATE RECEPTOR ANTAGONIST; UNCLASSIFIED DRUG; W 146; AKT1 PROTEIN, MOUSE; OXADIAZOLE DERIVATIVE; PDZK1 PROTEIN, MOUSE; PROPANEDIOL DERIVATIVE; SCARB1 PROTEIN, MOUSE; SIGNAL PEPTIDE; SPHINGOSINE; SPHINGOSINE 1 PHOSPHATE RECEPTOR; THIOPHENE DERIVATIVE;

ANIMAL CELL; ARTICLE; CELL ADHESION; CELL MIGRATION; CONTROLLED STUDY; ENZYME ACTIVITY; GENE TARGETING; MACROPHAGE; MOUSE; NONHUMAN; PERITONEUM MACROPHAGE; PROTEIN PROTEIN INTERACTION; RAT; SIGNAL TRANSDUCTION; AGONISTS; ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CELL CULTURE; CELL LINE; CELL MOTION; CYTOLOGY; DRUG EFFECTS; GENETICS; KNOCKOUT MOUSE; METABOLISM;

ANIMALS; CELL LINE; CELL MOVEMENT; CELLS, CULTURED; FINGOLIMOD HYDROCHLORIDE; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LIPOPROTEINS, HDL; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; OXADIAZOLES; PERTUSSIS TOXIN; PROPYLENE GLYCOLS; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTORS, LYSOSPHINGOLIPID; SCAVENGER RECEPTORS, CLASS B; SPHINGOSINE; THIOPHENES;

EID: 84906997281     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone     Document Type: Article

References (131)

1. Taylor PR, Martinez-Pomares L, Stacey M, Lin HH, Brown GD, et al. (2005) Macrophage receptors and immune recognition. Annu Rev Immunol 23: 901-944
2. Libby P (2002) Inflammation in atherosclerosis. Nature 420: 868-874
3. Steinberg D (1997) Low density lipoprotein oxidation and its pathobiological significance. J Biol Chem 272: 20963-20966
4. Tabas I, Williams KJ, Boren J (2007) Subendothelial lipoprotein retention as the initiating process in atherosclerosis: update and therapeutic implications. Circulation 116: 1832-1844
5. Nagao T, Qin C, Grosheva I, Maxfield FR, Pierini LM (2007) Elevated cholesterol levels in the plasma membranes of macrophages inhibit migration by disrupting RhoA regulation. Arterioscler Thromb Vasc Biol 27: 1596-1602
6. Park YM, Drazba JA, Vasanji A, Egelhoff T, Febbraio M, et al. (2012) Oxidized LDL/CD36 interaction induces loss of cell polarity and inhibits macrophage locomotion. Mol Biol Cell 23: 3057-3068
7. Qin C, Nagao T, Grosheva I, Maxfield FR, Pierini LM (2006) Elevated plasma membrane cholesterol content alters macrophage signaling and function. Arterioscler Thromb Vasc Biol 26: 372-378
8. Ramkhelawon B, Yang Y, van Gils JM, Hewing B, Rayner KJ, et al. (2013) Hypoxia induces netrin-1 and Unc5b in atherosclerotic plaques: mechanism for macrophage retention and survival. Arterioscler Thromb Vasc Biol 33: 1180-1188
9. Feig JE, Pineda-Torra I, Sanson M, Bradley MN, Vengrenyuk Y, et al. (2010) LXR promotes the maximal egress of monocyte-derived cells from mouse aortic plaques during atherosclerosis regression. J Clin Invest 120: 4415-4424
10. Feig JE, Rong JX, Shamir R, Sanson M, Vengrenyuk Y, et al. (2011) HDL promotes rapid atherosclerosis regression in mice and alters inflammatory properties of plaque monocyte-derived cells. Proc Natl Acad Sci U S A 108: 7166-7171
11. Llodra J, Angeli V, Liu J, Trogan E, Fisher EA, et al. (2004) Emigration of monocyte-derived cells from atherosclerotic lesions characterizes regressive, but not progressive, plaques. Proc Natl Acad Sci U S A 101: 11779-11784
12. Randolph GJ (2008) Emigration of monocyte-derived cells to lymph nodes during resolution of inflammation and its failure in atherosclerosis. Curr Opin Lipidol 19: 462-468
13. Trogan E, Feig JE, Dogan S, Rothblat GH, Angeli V, et al. (2006) Gene expression changes in foam cells and the role of chemokine receptor CCR7 during atherosclerosis regression in ApoE-deficient mice. Proc Natl Acad Sci U S A 103: 3781-3786
14. Williams KJ, Feig JE, Fisher EA (2008) Rapid regression of atherosclerosis: Insights from the clinical and experimental literature. Nat Clin Pract Cardiovasc Med 5: 91-102
15. Feig JE, Quick JS, Fisher EA (2009) The role of a murine transplantation model of atherosclerosis regression in drug discovery. Curr Opin Investig Drugs 10: 232-238
16. Nissen SE, Tsunoda T, Tuzcu EM, Schoenhagen P, Cooper CJ, et al. (2003) Effect of recombinant ApoA-I Milano on coronary atherosclerosis in patients with acute coronary syndromes: A randomized controlled trial. Jama 290: 2292-2300
17. Raffai RL, Loeb SM, Weisgraber KH (2005) Apolipoprotein E promotes the regression of atherosclerosis independently of lowering plasma cholesterol levels. Arterioscler Thromb Vasc Biol 25: 436-441
18. Reis ED, Li J, Fayad ZA, Rong JX, Hansoty D, et al. (2001) Dramatic remodeling of advanced atherosclerotic plaques of the apolipoprotein Edeficient mouse in a novel transplantation model. J Vasc Surg 34: 541-547
19. Rong JX, Li J, Reis ED, Choudhury RP, Dansky HM, et al. (2001) Elevating high-density lipoprotein cholesterol in apolipoprotein E-deficient mice remodels advanced atherosclerotic lesions by decreasing macrophage and increasing smooth muscle cell content. Circulation 104: 2447-2452
20. Gordon DJ, Rifkind BM (1989) High-density lipoprotein-the clinical implications of recent studies. N Engl J Med 321: 1311-1316
21. Assmann G, Schulte H (1992) Relation of high-density lipoprotein cholesterol and triglycerides to incidence of atherosclerotic coronary artery disease (the PROCAM experience). Prospective Cardiovascular Munster study. Am J Cardiol 70: 733-737
22. Assmann G, Schulte H, von Eckardstein A, Huang Y (1996) High-density lipoprotein cholesterol as a predictor of coronary heart disease risk. The PROCAM experience and pathophysiological implications for reverse cholesterol transport. Atherosclerosis 124 Suppl: S11-20
23. Florentin M, Liberopoulos EN, Wierzbicki AS, Mikhailidis DP (2008) Multiple actions of high-density lipoprotein. Curr Opin Cardiol 23: 370-378
24. Nofer J, Kehrel B., Fobker M., Levkau B., Assmann G., von Eckardstein, A. (2002) HDL and arteriosclerosis: beyond reverse cholesterol transport. Atherosclerosis 161: 1-16
25. Mineo C, Deguchi H, Griffin JH, Shaul PW (2006) Endothelial and antithrombotic actions of HDL. Circ Res 98: 1352-1364
26. Assmann G, Nofer JR (2003) Atheroprotective effects of high-density lipoproteins. Annu Rev Med 54: 321-341
27. Hersberger M, von Eckardstein A (2005) Modulation of high-density lipoprotein cholesterol metabolism and reverse cholesterol transport. Handb Exp Pharmacol: 537-561
28. Cuchel M, Rader DJ (2006) Macrophage reverse cholesterol transport: key to the regression of atherosclerosis? Circulation 113: 2548-2555
29. Cho KH (2009) A reconstituted high density lipoprotein containing the V156E mutant of apolipoprotein A-I exhibits anti-atherosclerotic activity in Apo-E deficient mice. J Atheroscler Thromb 16: 217-229
30. Cho KH, Kim JR (2009) A reconstituted HDL containing V156K or R173C apoA-I exhibited anti-inflammatory activity in apo-E deficient mice and showed resistance to myeloperoxidase-mediated oxidation. Exp Mol Med 41: 417-428
31. Acton S, Rigotti A, Landschulz KT, Xu S, Hobbs HH, et al. (1996) Identification of scavenger receptor SR-BI as a high density lipoprotein receptor. Science 271: 518-520
32. Covey SD, Krieger M, Wang W, Penman M, Trigatti BL (2003) Scavenger receptor class B type I-mediated protection against atherosclerosis in LDL receptor-negative mice involves its expression in bone marrow-derived cells. Arterioscler Thromb Vasc Biol 23: 1589-1594
33. Kozarsky KF, Donahee MH, Rigotti A, Iqbal SN, Edelman ER, et al. (1997) Overexpression of the HDL receptor SR-BI alters plasma HDL and bile cholesterol levels. Nature 387: 414-417
34. Trigatti B, Rayburn H, Vinals M, Braun A, Miettinen H, et al. (1999) Influence of the high density lipoprotein receptor SR-BI on reproductive and cardiovascular pathophysiology. Proc Natl Acad Sci U S A 96: 9322-9327
35. Ji Y, Jian B, Wang N, Sun Y, Moya ML, et al. (1997) Scavenger receptor BI promotes high density lipoprotein-mediated cellular cholesterol efflux. J Biol Chem 272: 20982-20985
36. Norata GD, Catapano AL (2005) Molecular mechanisms responsible for the antiinflammatory and protective effect of HDL on the endothelium. Vasc Health Risk Manag 1: 119-129
37. Zhang Y, Ahmed AM, McFarlane N, Capone C, Boreham DR, et al. (2007) Regulation of SR-BI-mediated selective lipid uptake in Chinese hamster ovaryderived cells by protein kinase signaling pathways. J Lipid Res 48: 405-416
38. Rentero C, Evans R, Wood P, Tebar F, Vila de Muga S, et al. (2006) Inhibition of H-Ras and MAPK is compensated by PKC-dependent pathways in annexin A6 expressing cells. Cell Signal 18: 1006-1016
39. Brunet R, How M, Trigatti BL (2011) Modulators of Protein Kinase C Affect SR-BI-Dependent HDL Lipid Uptake in Transfected HepG2 Cells. Cholesterol 2011: 687939
40. Kimura T, Tomura H, Mogi C, Kuwabara A, Damirin A, et al. (2006) Role of scavenger receptor class B type I and sphingosine 1-phosphate receptors in high density lipoprotein-induced inhibition of adhesion molecule expression in endothelial cells. J Biol Chem 281: 37457-37467
41. Assanasen C, Mineo C, Seetharam D, Yuhanna IS, Marcel YL, et al. (2005) Cholesterol binding, efflux, and a PDZ-interacting domain of scavenger receptor-BI mediate HDL-initiated signaling. J Clin Invest 115: 969-977
42. Al-Jarallah A, Trigatti BL (2010) A role for the scavenger receptor, class B type I in high density lipoprotein dependent activation of cellular signaling pathways. Biochim Biophys Acta 1801: 1239-1248
43. Mineo C, Shaul PW (2012) Functions of scavenger receptor class B, type I in atherosclerosis. Curr Opin Lipidol 23: 487-493
44. Kocher O, Comella N, Tognazzi K, Brown LF (1998) Identification and partial characterization of PDZK1: A novel protein containing PDZ interaction domains. Lab Invest 78: 117-125
45. Silver DL (2002) A carboxyl-terminal PDZ-interacting domain of scavenger receptor B, type I is essential for cell surface expression in liver. J Biol Chem 277: 34042-34047
46. Yesilaltay A, Kocher O, Pal R, Leiva A, Quinones V, et al. (2006) PDZK1 is required for maintaining hepatic scavenger receptor, class B, type I (SR-BI) steady state levels but not its surface localization or function. J Biol Chem 281: 28975-28980
47. Ikemoto M, Arai H, Feng D, Tanaka K, Aoki J, et al. (2000) Identification of a PDZ-domain-containing protein that interacts with the scavenger receptor class B type I. Proc Natl Acad Sci U S A 97: 6538-6543
48. Kocher O, Birrane G, Yesilaltay A, Shechter S, Pal R, et al. (2011) Identification of the PDZ3 Domain of the Adaptor Protein PDZK1 as a Second, Physiologically Functional Binding Site for the C Terminus of the High Density Lipoprotein Receptor Scavenger Receptor Class B Type I. J Biol Chem286: 25171-25186
49. Gong M, Wilson M, Kelly T, Su W, Dressman J, et al. (2003) HDL-associated estradiol stimulates endothelial NO synthase and vasodilation in an SR-BIdependent manner. J Clin Invest 111: 1579-1587
50. Azhar S, Nomoto A, Reaven E (2002) Hormonal regulation of adrenal microvillar channel formation. J Lipid Res 43: 861-871
51. Okajima F, Sato K, Kimura T (2009) Anti-atherogenic actions of high-density lipoprotein through sphingosine 1-phosphate receptors and scavenger receptor class B type I. Endocr J 56: 317-334
52. Argraves KM, Argraves WS (2007) HDL serves as an S1P signaling platform mediating a multitude of cardiovascular effects. J Lipid Res
53. Murata N, Sato K, Kon J, Tomura H, Yanagita M, et al. (2000) Interaction of sphingosine 1-phosphate with plasma components, including lipoproteins, regulates the lipid receptor-mediated actions. Biochem J 352 Pt 3: 809-815
54. Nofer JR, van der Giet M, Tolle M, Wolinska I, von Wnuck Lipinski K, et al. (2004) HDL induces NO-dependent vasorelaxation via the lysophospholipid receptor S1P3. J Clin Invest 113: 569-581
55. Sattler K, Levkau B (2009) Sphingosine-1-phosphate as a mediator of highdensity lipoprotein effects in cardiovascular protection. Cardiovasc Res 82: 201-211
56. Frias MA, James RW, Gerber-Wicht C, Lang U (2009) Native and reconstituted HDL activate Stat3 in ventricular cardiomyocytes via ERK1/2: role of sphingosine-1-phosphate. Cardiovasc Res 82: 313-323
57. Matsuo Y, Miura S, Kawamura A, Uehara Y, Rye KA, et al. (2007) Newly developed reconstituted high-density lipoprotein containing sphingosine-1- phosphate induces endothelial tube formation. Atherosclerosis 194: 159-168
58. Rivera J, Proia RL, Olivera A (2008) The alliance of sphingosine-1-phosphate and its receptors in immunity. Nat Rev Immunol 8: 753-763
59. Takabe K, Paugh SW, Milstien S, Spiegel S (2008) "Inside-out" signaling of sphingosine-1-phosphate: Therapeutic targets. Pharmacol Rev 60: 181-195
60. Hughes JE, Srinivasan S, Lynch KR, Proia RL, Ferdek P, et al. (2008) Sphingosine-1-phosphate induces an antiinflammatory phenotype in macrophages. Circ Res 102: 950-958
61. Kimura T, Sato K, Malchinkhuu E, Tomura H, Tamama K, et al. (2003) High-density lipoprotein stimulates endothelial cell migration and survival through sphingosine 1-phosphate and its receptors. Arterioscler Thromb Vasc Biol 23: 1283-1288
62. Argraves KM, Gazzolo PJ, Groh EM, Wilkerson BA, Matsuura BS, et al. (2008) High density lipoprotein-associated sphingosine 1-phosphate promotes endothelial barrier function. J Biol Chem 283: 25074-25081
63. Liu F, Verin AD, Wang P, Day R, Wersto RP, et al. (2001) Differential regulation of sphingosine-1-phosphate- and VEGF-induced endothelial cell chemotaxis. Involvement of G(ialpha2)-linked Rho kinase activity. Am J Respir Cell Mol Biol 24: 711-719
64. Kimura T, Watanabe T, Sato K, Kon J, Tomura H, et al. (2000) Sphingosine 1-phosphate stimulates proliferation and migration of human endothelial cells possibly through the lipid receptors, Edg-1 and Edg-3. Biochem J 348 Pt 1: 71-76
65. Morales-Ruiz M, Lee MJ, Zollner S, Gratton JP, Scotland R, et al. (2001) Sphingosine 1-phosphate activates Akt, nitric oxide production, and chemotaxis through a Gi protein/phosphoinositide 3-kinase pathway in endothelial cells. J Biol Chem 276: 19672-19677
66. Rikitake Y, Hirata K, Kawashima S, Ozaki M, Takahashi T, et al. (2002) Involvement of endothelial nitric oxide in sphingosine-1-phosphate-induced angiogenesis. Arterioscler Thromb Vasc Biol 22: 108-114
67. Ryu Y, Takuwa N, Sugimoto N, Sakurada S, Usui S, et al. (2002) Sphingosine- 1-phosphate, a platelet-derived lysophospholipid mediator, negatively regulates cellular Rac activity and cell migration in vascular smooth muscle cells. Circ Res 90: 325-332
68. Krieger M, Brown MS, Goldstein JL (1981) Isolation of Chinese hamster cell mutants defective in the receptor-mediated endocytosis of low density lipoprotein. J Mol Biol 150: 167-184
69. Theilmeier G, De Geest B, Van Veldhoven PP, Stengel D, Michiels C, et al. (2000) HDL-associated PAF-AH reduces endothelial adhesiveness in apoE-/- mice. Faseb J 14: 2032-2039
70. Muller H, Hofer S, Kaneider N, Neuwirt H, Mosheimer B, et al. (2005) The immunomodulator FTY720 interferes with effector functions of human monocyte-derived dendritic cells. Eur J Immunol 35: 533-545
71. Zhang X, Liu X, Shang H, Xu Y, Qian M (2011) Monocyte chemoattractant protein-1 induces endothelial cell apoptosis in vitro through a p53-dependent mitochondrial pathway. Acta Biochim Biophys Sin (Shanghai) 43: 787-795
72. Gu X, Kozarsky K, Krieger M (2000) Scavenger receptor class B, type Imediated [3H]cholesterol efflux to high and low density lipoproteins is dependent on lipoprotein binding to the receptor. J Biol Chem 275: 29993-30001
73. Nieland TJ, Penman M, Dori L, Krieger M, Kirchhausen T (2002) Discovery of chemical inhibitors of the selective transfer of lipids mediated by the HDL receptor SR-BI. Proc Natl Acad Sci U S A 99: 15422-15427
74. Murakami A, Takasugi H, Ohnuma S, Koide Y, Sakurai A, et al. (2010) Sphingosine 1-phosphate (S1P) regulates vascular contraction via S1P3 receptor: Investigation based on a new S1P3 receptor antagonist. Mol Pharmacol 77: 704-713
75. Jajoo S, Mukherjea D, Pingle S, Sekino Y, Ramkumar V (2006) Induction of adenosine A1 receptor expression by pertussis toxin via an adenosine 5'- diphosphate ribosylation-independent pathway. J Pharmacol Exp Ther 317: 1-10
76. Chung EY, Psathas JN, Yu D, Li Y, Weiss MJ, et al. (2012) CD19 is a major B cell receptor-independent activator of MYC-driven B-lymphomagenesis. J Clin Invest 122: 2257-2266
77. Andreadi CK, Howells LM, Atherfold PA, Manson MM (2006) Involvement of Nrf2, p38, B-Raf, and nuclear factor-kappaB, but not phosphatidylinositol 3- kinase, in induction of hemeoxygenase-1 by dietary polyphenols. Mol Pharmacol 69: 1033-1040
78. Kim SK, Abdelmegeed MA, Novak RF (2006) The mitogen-activated protein kinase kinase (mek) inhibitor PD98059 elevates primary cultured rat hepatocyte glutathione levels independent of inhibiting mek. Drug Metab Dispos 34: 683-689
79. Verspohl EJ, Wienecke A (1998) The role of protein kinase C in the desensitization of rat pancreatic islets to cholinergic stimulation. J Endocrinol 159: 287-295
80. Mair KM, Robinson E, Kane KA, Pyne S, Brett RR, et al. (2010) Interaction between anandamide and sphingosine-1-phosphate in mediating vasorelaxation in rat coronary artery. Br J Pharmacol 161: 176-192
81. Sanna MG, Liao J, Jo E, Alfonso C, Ahn MY, et al. (2004) Sphingosine 1- phosphate (S1P) receptor subtypes S1P1 and S1P3, respectively, regulate lymphocyte recirculation and heart rate. J Biol Chem 279: 13839-13848
82. Ayman S, Wallace P, Wayman CP, Gibson A, McFadzean I (2003) Receptorindependent activation of Rho-kinase-mediated calcium sensitisation in smooth muscle. Br J Pharmacol 139: 1532-1538
83. Julien B, Grenard P, Teixeira-Clerc F, Van Nhieu JT, Li L, et al. (2005) Antifibrogenic role of the cannabinoid receptor CB2 in the liver. Gastroenterology 128: 742-755
84. Li C, Yang G, Ruan J (2012) Sphingosine kinase-1/sphingosine-1-phosphate receptor type 1 signaling axis is induced by transforming growth factor-beta1 and stimulates cell migration in RAW264.7 macrophages. Biochem Biophys Res Commun 426: 415-420
85. Bookout AL, Mangelsdorf DJ (2003) Quantitative real-time PCR protocol for analysis of nuclear receptor signaling pathways. Nucl Recept Signal 1: e012
86. Kocher O, Yesilaltay A, Shen CH, Zhang S, Daniels K, et al. (2008) Influence of PDZK1 on lipoprotein metabolism and atherosclerosis. Biochim Biophys Acta 1782: 310-316
87. Katada T (2012) The inhibitory G protein G(i) identified as pertussis toxincatalyzed ADP-ribosylation. Biol Pharm Bull 35: 2103-2111
88. Charo IF, Myers SJ, Herman A, Franci C, Connolly AJ, et al. (1994) Molecular cloning and functional expression of two monocyte chemoattractant protein 1 receptors reveals alternative splicing of the carboxyl-terminal tails. Proc Natl Acad Sci U S A 91: 2752-2756
89. Davis MD, Clemens JJ, Macdonald TL, Lynch KR (2005) Sphingosine 1- phosphate analogs as receptor antagonists. J Biol Chem 280: 9833-9841
90. Keul P, Lucke S, von Wnuck Lipinski K, Bode C, Graler M, et al. (2011) Sphingosine-1-phosphate receptor 3 promotes recruitment of monocyte/ macrophages in inflammation and atherosclerosis. Circ Res 108: 314-323
91. Michaud J, Im DS, Hla T (2011) Inhibitory role of sphingosine 1-phosphate receptor 2 in macrophage recruitment during inflammation. J Immunol 184: 1475-1483
92. Jones GE (2000) Cellular signaling in macrophage migration and chemotaxis. J Leukoc Biol 68: 593-602
93. Jones GE, Ridley AJ, Zicha D (2000) Rho GTPases and cell migration: measurement of macrophage chemotaxis. Methods Enzymol 325: 449-462
94. Ridley AJ (2004) Rho proteins and cancer. Breast Cancer Res Treat 84: 13-19
95. Ridley AJ, Allen WE, Peppelenbosch M, Jones GE (1999) Rho family proteins and cell migration. Biochem Soc Symp 65: 111-123
96. Ridley AJ (2001) Rho GTPases and cell migration. J Cell Sci 114: 2713-2722
97. Chodniewicz D, Zhelev DV (2003) Chemoattractant receptor-stimulated Factin polymerization in the human neutrophil is signaled by 2 distinct pathways. Blood 101: 1181-1184
98. Burgering BM, Coffer PJ (1995) Protein kinase B (c-Akt) in phosphatidylinositol- 3-OH kinase signal transduction. Nature 376: 599-602
99. Manning BD, Cantley LC (2007) AKT/PKB signaling: navigating downstream. Cell 129: 1261-1274
100. Sotsios Y, Ward SG (2000) Phosphoinositide 3-kinase: A key biochemical signal for cell migration in response to chemokines. Immunol Rev 177: 217-235
101. Stephens L, Ellson C, Hawkins P (2002) Roles of PI3Ks in leukocyte chemotaxis and phagocytosis. Curr Opin Cell Biol 14: 203-213
102. Vanhaesebroeck B, Leevers SJ, Ahmadi K, Timms J, Katso R, et al. (2001) Synthesis and function of 3-phosphorylated inositol lipids. Annu Rev Biochem 70: 535-602
103. Baranova IN, Vishnyakova TG, Bocharov AV, Kurlander R, Chen Z, et al. (2005) Serum amyloid A binding to CLA-1 (CD36 and LIMPII analogous-1) mediates serum amyloid A protein-induced activation of ERK1/2 and p38 mitogen-activated protein kinases. J Biol Chem 280: 8031-8040
104. Mineo C, Yuhanna IS, Quon MJ, Shaul PW (2003) High density lipoproteininduced endothelial nitric-oxide synthase activation is mediated by Akt and MAP kinases. J Biol Chem 278: 9142-9149
105. Mendez AJ, Oram JF, Bierman EL (1991) Protein kinase C as a mediator of high density lipoprotein receptor-dependent efflux of intracellular cholesterol. J Biol Chem 266: 10104-10111
106. Gorshkova I, He D, Berdyshev E, Usatuyk P, Burns M, et al. (2008) Protein kinase C-epsilon regulates sphingosine 1-phosphate-mediated migration of human lung endothelial cells through activation of phospholipase D2, protein kinase C-zeta, and Rac1. J Biol Chem 283: 11794-11806
107. Martiny-Baron G, Kazanietz MG, Mischak H, Blumberg PM, Kochs G, et al. (1993) Selective inhibition of protein kinase C isozymes by the indolocarbazole Go 6976. J Biol Chem 268: 9194-9197
108. Nixon JS, Bishop J, Bradshaw D, Davis PD, Hill CH, et al. (1992) The design and biological properties of potent and selective inhibitors of protein kinase C. Biochem Soc Trans 20: 419-425
109. Trach CC, Wulfroth PM, Severs NJ, Robenek H (1996) Influence of native and modified lipoproteins on migration of mouse peritoneal macrophages and the effect of the antioxidants vitamin E and Probucol. Eur J Cell Biol 71: 199-205
110. Yuhanna IS, Zhu Y, Cox BE, Hahner LD, Osborne-Lawrence S, et al. (2001) High-density lipoprotein binding to scavenger receptor-BI activates endothelial nitric oxide synthase. Nat Med 7: 853-857
111. Nieland TJ, Chroni A, Fitzgerald ML, Maliga Z, Zannis VI, et al. (2004) Crossinhibition of SR-BI- and ABCA1-mediated cholesterol transport by the small molecules BLT-4 and glyburide. J Lipid Res 45: 1256-1265
112. Billich A, Bornancin F, Devay P, Mechtcheriakova D, Urtz N, et al. (2003) Phosphorylation of the immunomodulatory drug FTY720 by sphingosine kinases. J Biol Chem 278: 47408-47415
113. Seetharam D, Mineo C, Gormley AK, Gibson LL, Vongpatanasin W, et al. (2006) High-density lipoprotein promotes endothelial cell migration and reendothelialization via scavenger receptor-B type I. Circ Res 98: 63-72
114. Guo H, Zhao Z, Yang Q, Wang M, Bell RD, et al. (2013) An activated protein C analog stimulates neuronal production by human neural progenitor cells via a PAR1-PAR3-S1PR1-Akt pathway. J Neurosci 33: 6181-6190
115. Shiratsuchi H, Basson MD (2007) Akt2, but not Akt1 or Akt3 mediates pressure-stimulated serum-opsonized latex bead phagocytosis through activating mTOR and p70 S6 kinase. J Cell Biochem 102: 353-367
116. Zhou GL, Tucker DF, Bae SS, Bhatheja K, Birnbaum MJ, et al. (2006) Opposing roles for Akt1 and Akt2 in Rac/Pak signaling and cell migration. J Biol Chem 281: 36443-36453
117. Arboleda MJ, Lyons JF, Kabbinavar FF, Bray MR, Snow BE, et al. (2003) Overexpression of AKT2/protein kinase Bbeta leads to up-regulation of beta1 integrins, increased invasion, and metastasis of human breast and ovarian cancer cells. Cancer Res 63: 196-206
118. Irie HY, Pearline RV, Grueneberg D, Hsia M, Ravichandran P, et al. (2005) Distinct roles of Akt1 and Akt2 in regulating cell migration and epithelialmesenchymal transition. J Cell Biol 171: 1023-1034
119. Yoeli-Lerner M, Yiu GK, Rabinovitz I, Erhardt P, Jauliac S, et al. (2005) Akt blocks breast cancer cell motility and invasion through the transcription factor NFAT. Mol Cell 20: 539-550
120. Ackah E, Yu J, Zoellner S, Iwakiri Y, Skurk C, et al. (2005) Akt1/protein kinase Balpha is critical for ischemic and VEGF-mediated angiogenesis. J Clin Invest 115: 2119-2127
121. Androulidaki A, Iliopoulos D, Arranz A, Doxaki C, Schworer S, et al. (2009) The kinase Akt1 controls macrophage response to lipopolysaccharide by regulating microRNAs. Immunity 31: 220-231
122. Fernandez-Hernando C, Ackah E, Yu J, Suarez Y, Murata T, et al. (2007) Loss of Akt1 leads to severe atherosclerosis and occlusive coronary artery disease. Cell Metab 6: 446-457
123. Fernandez-Hernando C, Jozsef L, Jenkins D, Di Lorenzo A, Sessa WC (2009) Absence of Akt1 reduces vascular smooth muscle cell migration and survival and induces features of plaque vulnerability and cardiac dysfunction during atherosclerosis. Arterioscler Thromb Vasc Biol 29: 2033-2040
124. Grewal T, Evans R, Rentero C, Tebar F, Cubells L, et al. (2005) Annexin A6 stimulates the membrane recruitment of p120GAP to modulate Ras and Raf-1 activity. Oncogene 24: 5809-5820
125. Nofer JR, Fobker M, Hobbel G, Voss R, Wolinska I, et al. (2000) Activation of phosphatidylinositol-specific phospholipase C by HDL-associated lysosphingolipid. Involvement in mitogenesis but not in cholesterol efflux. Biochemistry 39: 15199-15207
126. Porn MI, Akerman KE, Slotte JP (1991) High-density lipoproteins induce a rapid and transient release of Ca2+ in cultured fibroblasts. Biochem J 279 (Pt 1): 29-33
127. Bochkov V, Tkachuk V, Buhler F, Resink T (1992) Phosphoinositide and calcium signaling responses in smooth muscle cells: Comparison between lipoproteins, Ang II, and PDGF. Biochem Biophys Res Commun 188: 1295-1304
128. Honda HM, Wakamatsu BK, Goldhaber JI, Berliner JA, Navab M, et al. (1999) High-density lipoprotein increases intracellular calcium levels by releasing calcium from internal stores in human endothelial cells. Atherosclerosis 143: 299-306
129. Pilon A, Martin G, Bultel-Brienne S, Junquero D, Delhon A, et al. (2003) Regulation of the scavenger receptor BI and the LDL receptor by activators of aldosterone production, angiotensin II and PMA, in the human NCI-H295R adrenocortical cell line. Biochim Biophys Acta 1631: 218-228
130. Ridley AJ (2001) Rho family proteins: Coordinating cell responses. Trends Cell Biol 11: 471-477
131. Ridley AJ (2001) Rho proteins: linking signaling with membrane trafficking. Traffic 2: 303-310