Loss of G2A promotes macrophage accumulation in atherosclerotic lesions of low density lipoprotein receptor-deficient mice

Journal of Lipid Research

Volumn 46, Issue 7, 2005, Pages 1405-1415

  Parks, Brian W ^a   Gambill, Ginger P ^a   Lusis, Aldons J ^b   Kabarowski, Janusz H S ^a  

^a University of Alabama at Birmingham   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Apoptosis; Atherosclerosis; Chemotaxis; Lysophosphatidylcholine; T cells

Indexed keywords

COLLAGEN; G PROTEIN COUPLED RECEPTOR; G PROTEIN COUPLED RECEPTOR G2A; LOW DENSITY LIPOPROTEIN RECEPTOR; LYSOPHOSPHATIDYLCHOLINE; UNCLASSIFIED DRUG; CELL CYCLE PROTEIN; G2A RECEPTOR; LIPID;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATHEROGENESIS; ATHEROSCLEROSIS; CELL DEATH; CELL LABELING; CELL STIMULATION; CHEMOTAXIS; CONTROLLED STUDY; FEMALE; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; KNOCKOUT MOUSE; LYMPHOCYTIC INFILTRATION; MACROPHAGE; MALE; MOUSE; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE; ANIMAL; ARTERIOSCLEROSIS; BIOSYNTHESIS; BLOOD; LYMPHOCYTE COUNT; METABOLISM; MOUSE MUTANT; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; ARTERIOSCLEROSIS; CELL CYCLE PROTEINS; FEMALE; IN SITU NICK-END LABELING; LIPIDS; LYMPHOCYTE COUNT; LYSOPHOSPHATIDYLCHOLINES; MACROPHAGES; MICE; MICE, KNOCKOUT; RECEPTORS, G-PROTEIN-COUPLED; RECEPTORS, LDL; T-LYMPHOCYTES;

EID: 24744461403     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M500085-JLR200     Document Type: Article

References (51)

1. Lusis, A. J. 2000. Atherosclerosis. Nature. 407: 233-241.
2. Parthasarathy, S., and J. Barnett. 1990. Phospholipase A2 activity of low density lipoprotein: evidence for an intrinsic phospholipase A2 activity of apoprotein B-100. Proc. Natl. Acad. Sci. USA. 87: 9741-9745.
3. Kume, N., H. Ochi, E. Nishi, M. A. Gimbrone, Jr., and T. Kita. 1995. Involvement of protein kinase C-independent mechanisms in endothelial ICAM-1 up-regulation by lysophosphatidylcholine. Ann. N. Y. Acad. Sci. 748: 541-542.
4. Murugesan, G., M. R. Sandhya Rani, C. E. Gerber, C. Mukhopadhyay, R. M. Ransohoff, G. M. Chisolm, and K. Kottke-Marchant. 2003. Lysophosphatidylcholine regulates human microvascular endothelial cell expression of chemokines. J. Mol. Cell. Cardiol. 35: 1375-1384.
5. Quinn, M. T., S. Parthasarathy, and D. Steinberg. 1988. Lysophosphatidylcholine: a chemotactic factor for human monocytes and its potential role in atherogenesis. Proc. Natl. Acad. Sci. USA. 85: 2805-2809.
6. Lin, P., and R. D. Ye. 2003. The lysophospholipid receptor G2A activates a specific combination of G proteins and promotes apoptosis. J. Biol. Chem. 278: 14379-14386.
7. Radu, C. G., L. V. Yang, M. Riedinger, M. Au, and O. N. Witte. 2004. T cell chemotaxis to lysophosphatidylcholine through the G2A receptor. Proc. Natl. Acad. Sci. USA. 101: 245-250.
8. Han, K. H., K. H. Hong, J. Ko, K. S. Rhee, M. K. Hong, J. J. Kim, Y. H. Kim, and S. J. Park. 2004. Lysophosphatidylcholine up-regulates CXCR4 chemokine receptor expression in human CD4 T cells. J. Leukoc. Biol. 76: 195-202.
9. Yang, L. V., C. G. Radu, L. Wang, M. Riedinger, and O. N. Witte. 2004. Gi-independent macrophage chemotaxis to lysophosphatidylcholine via the immunoregulatory GPCR G2A. Blood. 105: 1127-1134.
10. Chen, G., J. Li, X. Qiang, C. J. Czura, M. Ochani, K. Ochani, L. Ulloa, H. Yang, K. J. Tracey, P. Wang, et al. 2005. Suppression of HMGB1 release by stearoyl lysophosphatidylcholine: an additional mechanism for its therapeutic effects in experimental sepsis. J. Lipid Res. 46: 623-627.
11. Wang, L., C. G. Radu, L. V. Yang, L. A. Bentolila, M. Riedinger, and O. N. Witte. 2005. Lysophosphatidylcholine-induced surface redistribution regulates signaling of the murine G-protein-coupled receptor G2A. Mol. Biol. Cell. 16: 2234-2247.
12. Kabarowski, J. H., J. D. Feramisco, L. Q. Le, J. L. Gu, S. W. Luoh, M. I. Simon, and O. N. Witte. 2000. Direct genetic demonstration of G alpha 13 coupling to the orphan G protein-coupled receptor G2A leading to RhoA-dependent actin rearrangement. Proc. Natl. Acad. Sci. USA. 97: 12109-12114.
13. Zohn, I. E., M. Klinger, X. Karp, H. Kirk, M. Symons, M. Chrzanowska-Wodnicka, C. J. Der, and R. J. Kay. 2000. G2A is an oncogenic G protein-coupled receptor. Oncogene. 19: 3866-3877.
14. Kabarowski, J. H., K. Zhu, L. Q. Le, O. N. Witte, and Y. Xu. 2001. Lysophosphatidylcholine as a ligand for the immunoregulatory receptor G2A. Science. 293: 702-705.
15. Witte, O. N., J. H. Kabarowski, Y. Xu, L. Q. Le, and K. Zhu. 2005. Retraction. Science. 307: 206.
16. Ludwig, M. G., M. Vanek, D. Guerini, J. A. Gasser, C. E. Jones, U. Junker, H. Hofstetter, R. M. Wolf, and K. Seuwen. 2003. Proton-sensing G-protein-coupled receptors. Nature. 425: 93-98.
17. Wang, J. Q., J. Kon, C. Mogi, M. Tobo, A. Damirin, K. Sato, M. Komachi, E. Malchinkhuu, N. Murata, T. Kimura, et al. 2004. TDAG8 is a proton-sensing and psychosine-sensitive G-protein-coupled receptor. J. Biol. Chem. 279: 45626-45633.
18. Murakami, N., T. Yokomizo, T. Okuno, and T. Shimizu. 2004. G2A is a proton-sensing G-protein coupled receptor antagonized by lysophosphatidylcholine. J. Biol. Chem. 279: 42484-42491.
19. Radu, C. G., A. Nijagal, J. McLaughlin, L. Wang, and O. N. Witte. 2005. Differential proton sensitivity of related G protein-coupled receptors T cell death-associated gene 8 and G2A expressed in immune cells. Proc. Natl. Acad. Sci. USA. 102: 1632-1637.
20. Hedrick, C. C., L. W. Castellani, C. H. Warden, D. L. Puppione, and A. J. Lusis. 1993. Influence of mouse apolipoprotein A-II on plasma lipoproteins in transgenic mice. J. Biol. Chem. 268: 20676-20682.
21. Xiao, Y., Y. Chen, A. W. Kennedy, J. Belinson, and Y. Xu. 2000. Evaluation of plasma lysophospholipids for diagnostic significance using electrospray ionization mass spectrometry (ESI-MS) analyses. Ann. N. Y. Acad. Sci. 905: 242-259.
22. Sutphen, R., Y. Xu, G. D. Wilbanks, J. Fiorica, E. C. Grendys, Jr., J. P. LaPolla, H. Arango, M. S. Hoffman, M. Martino, K. Wakeley, et al. 2004. Lysophospholipids are potential biomarkers of ovarian cancer. Cancer Epidemiol. Biomarkers Prev. 13: 1185-1191.
23. Zhu, K., L. M. Baudhuin, G. Hong, F. S. Williams, K. L. Cristina, J. H. Kabarowski, O. N. Witte, and Y. Xu. 2001. Sphingosylphosphorylcholine and lysophosphatidylcholine are ligands for the G protein-coupled receptor GPR4. J. Biol. Chem. 276: 41325-41335.
24. Lum, H., J. Qiao, R. J. Walter, F. Huang, P. V. Subbaiah, K. S. Kim, and O. Holian. 2003. Inflammatory stress increases receptor for lysophosphatidylcholine in human microvascular endothelial cells. Am. J. Physiol. Heart Circ. Physiol. 285: H1786-H1789.
25. Weng, Z., A. C. Fluckiger, S. Nisitani, M. I. Wahl, L. Q. Le, C. A. Hunter, A. A. Fernal, M. M. Le Beau, and O. N. Witte. 1998. A DNA damage and stress inducible G protein-coupled receptor blocks cells in G2/M. Proc. Natl. Acad. Sci. USA. 95: 12334-12339.
26. Thukkani, A. K., J. McHowat, F. F. Hsu, M. L. Brennan, S. L. Hazen, and D. A. Ford. 2003. Identification of {alpha}-chloro fatty aldehydes and unsaturated lysophosphatidylcholine molecular species in human atherosclerotic lesions. Circulation. 108: 3128-3133.
27. Thukkani, A. K., C. J. Albert, K. R. Wildsmith, M. C. Messner, B. D. Martinson, F. F. Hsu, and D. A. Ford. 2003. Myeloperoxidase-derived reactive chlorinating species from human monocytes target plasmalogens in low density lipoprotein. J. Biol. Chem. 278: 36365-36372.
28. Brennan, M. L., M. M. Anderson, D. M. Shih, X. D. Qu, X. Wang, A. C. Mehta, L. L. Lim, W. Shi, S. L. Hazen, J. S. Jacob, et al. 2001. Increased atherosclerosis in myeloperoxidase-deficient mice. J. Clin. Invest. 107: 419-430.
29. Sakai, M., A. Miyazaki, H. Hakamata, Y. Sato, T. Matsumura, S. Kobori, M. Shichiri, and S. Horiuchi. 1996. Lysophosphatidylcholine potentiates the mitogenic activity of modified LDL for human monocyte-derived macrophages. Arterioscler. Thromb. Vasc. Biol. 16: 600-605.
30. Carpenter, K. L., I. F. Dennis, I. R. Challis, D. P. Osborn, C. H. Macphee, D. S. Leake, M. J. Arends, and M. J. Mitchinson. 2001. Inhibition of lipoprotein-associated phospholipase A2 diminishes the death-inducing effects of oxidised LDL on human monocyte-macrophages. FEBS Lett. 505: 357-363.
31. Le, L. Q., J. H. Kabarowski, Z. Weng, A. B. Satterthwaite, E. T. Harvill, E. R. Jensen, J. F. Miller, and O. N. Witte. 2001. Mice lacking the orphan G protein-coupled receptor G2A develop a late-onset autoimmune syndrome. Immunity. 14: 561-571.
32. Galis, Z. S., G. K. Sukhova, M. W. Lark, and P. Libby. 1994. Increased expression of matrix metalloproteinases and matrix degrading activity in vulnerable regions of human atherosclerotic plaques. J. Clin. Invest. 94: 2493-2503.
33. Libby, P., and M. Aikawa. 2002. Stabilization of atherosclerotic plaques: new mechanisms and clinical targets. Nat. Med. 8: 1257-1262.
34. Ivandic, B., L. W. Castellani, X. P. Wang, J. H. Qiao, M. Mehrabian, M. Navab, A. M. Fogelman, D. S. Grass, M. E. Swanson, M. C. de Beer, et al. 1999. Role of group II secretory phospholipase A2 in atherosclerosis. 1. Increased atherogenesis and altered lipoproteins in transgenic mice expressing group IIa phospholipase A2. Arterioscler. Thromb. Vasc. Biol. 19: 1284-1290.
35. Webb, N. R., M. A. Bostrom, S. J. Szilvassy, D. R. van der Westhuyzen, A. Daugherty, and F. C. de Beer. 2003. Macrophage-expressed group IIA secretory phospholipase A2 increases atherosclerotic lesion formation in LDL receptor-deficient mice. Arterioscler. Thromb. Vasc. Biol. 23: 263-268.
36. Kockx, M. M., and A. G. Herman. 1998. Apoptosis in atherogenesis: implications for plaque destabilization. Eur. Heart J. 19 (Suppl. G): 23-28.
37. Rosenfeld, M. E., P. Polinsky, R. Virmani, K. Kauser, G. Rubanyi, and S. M. Schwartz. 2000. Advanced atherosclerotic lesions in the innominate artery of the ApoE knockout mouse. Arterioscler. Thromb. Vasc. Biol. 20: 2587-2592.
38. Johnson, J. L., and C. L. Jackson. 2001. Atherosclerotic plaque rupture in the apolipoprotein E knockout mouse. Atherosclerosis. 154: 399-406.
39. Rosenfeld, M. E., K. G. Carson, J. L. Johnson, H. Williams, C. L. Jackson, and S. M. Schwartz. 2002. Animal models of spontaneous plaque rupture: the holy grail of experimental atherosclerosis research. Curr. Atheroscler. Rep. 4: 238-242.
40. Le, L. Q., J. H. Kabarowski, S. Wong, K. Nguyen, S. S. Gambhir, and O. N. Witte. 2002. Positron emission tomography imaging analysis of G2A as a negative modifier of lymphoid leukemogenesis initiated by the BCR-ABL oncogene. Cancer Cell. 1: 381-391.
41. Llodra, J., V. Angeli, J. Liu, E. Trogan, E. A. Fisher, and G. J. Randolph. 2004. Emigration of monocyte-derived cells from atherosclerotic lesions characterizes regressive, but not progressive, plaques. Proc. Natl. Acad. Sci. USA. 101: 11779-11784.
42. Angeli, V., J. Llodra, J. X. Rong, K. Satoh, S. Ishii, T. Shimizu, E. A. Fisher, and G. J. Randolph. 2004. Dyslipidemia associated with atherosclerotic disease systemically alters dendritic cell mobilization. Immunity. 21: 561-574.
43. Bektas, M., L. S. Barak, P. S. Jolly, H. Liu, K. R. Lynch, E. Lacana, K. B. Suhr, S. Milstien, and S. Spiegel. 2003. The G protein-coupled receptor GPR4 suppresses ERK activation in a ligand-independent manner. Biochemistry. 42: 12181-12191.
44. Lardner, A. 2001. The effects of extracellular pH on immune function. J. Leukoc. Biol. 69: 522-530.
45. Chai, Y. C., D. G. Binion, R. Macklis, and G. M. Chisolm 3rd. 2002. Smooth muscle cell proliferation induced by oxidized LDL-borne lysophosphatidylcholine. Evidence for FGF-2 release from cells not extracellular matrix. Vascul. Pharmacol. 38: 229-237.
46. Kogure, K., S. Nakashima, A. Tsuchie, A. Tokumura, and K. Fukuzawa. 2003. Temporary membrane distortion of vascular smooth muscle cells is responsible for their apoptosis induced by platelet-activating factor-like oxidized phospholipids and their degradation product, lysophosphatidylcholine. Chem. Phys. Lipids. 126: 29-38.
47. Boggs, K. P., C. O. Rock, and S. Jackowski. 1995. Lysophosphatidylcholine and 1-O-octadecyl-2-O-methyl-rac-glycero-3-phosphocholine inhibit the CDP-choline pathway of phosphatidylcholine synthesis at the CTP:phosphocholine cytidylyltransferase step. J. Biol. Chem. 270: 7757-7764.
48. Van Der Luit, A. H., M. Budde, M. Verheij, and W. J. Van Blitterswijk. 2003. Different modes of internalization of apoptotic alkyl-lysophospholipid and cell-rescuing lysophosphatidylcholine. Biochem. J. 374: 747-753.
49. Boggs, K. P., C. O. Rock, and S. Jackowski. 1995. Lysophosphatidylcholine attenuates the cytotoxic effects of the antineoplastic phospholipid 1-O-octadecyl-2-O-methyl-rac-glycero-3-phosphocholine. J. Biol. Chem. 270: 11612-11618.
50. Chambers, K., and W. J. Brown. 2004. Characterization of a novel CI-976-sensitive lysophospholipid acyltransferase that is associated with the Golgi complex. Biochem. Biophys. Res. Commun. 313: 681-686.
51. Schmid, B., M. J. Finnen, J. L. Harwood, and S. K. Jackson. 2003. Acylation of lysophosphatidylcholine plays a key role in the response of monocytes to lipopolysaccharide. Eur. J. Biochem. 270: 2782-2788.