Lysophosphatidic acid targets vascular and oncogenic pathways via RAGE signaling

Journal of Experimental Medicine

Volumn 209, Issue 13, 2012, Pages 2339-2350

  Rai, Vivek ^a   Touré, Fatouma ^a   Chitayat, Seth ^b   Pei, Renjun ^c   Song, Fei ^a   Li, Qing ^a   Zhang, Jinghua ^a   Rosario, Rosa ^a   Ramasamy, Ravichandran ^a   Chazin, Walter J ^b   Schmidt, Ann Marie ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c NewYork Presbyterian Hospital   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADVANCED GLYCATION END PRODUCT RECEPTOR; CYCLIN D1; LYSOPHOSPHATIDIC ACID; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE B; SMALL INTERFERING RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; AORTA MEDIA; ARTICLE; BINDING SITE; CANCER INHIBITION; CANCER SUSCEPTIBILITY; CELL MIGRATION; CELL PROLIFERATION; CELL STIMULATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; FEMALE; GENE DELETION; GLIOMA CELL; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR SIGNALING; MOUSE; NONHUMAN; OVARY TUMOR; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; RAT; RECEPTOR BINDING; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER;

ANIMALS; CELL LINE, TUMOR; CYCLIN D1; FEMALE; HUMANS; LYSOPHOSPHOLIPIDS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MUSCLE, SMOOTH, VASCULAR; NEOPLASMS; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RECEPTORS, IMMUNOLOGIC; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION;

EID: 84871909158     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20120873     Document Type: Article

References (34)

1. Bu, D.X., V. Rai, X. Shen, R. Rosario, Y. Lu, V. D'Agati, S.F. Yan, R.A. Friedman, E. Nuglozeh, and A.M. Schmidt. 2010. Activation of the ROCK1 branch of the transforming growth factor-beta pathway contributes to RAGE-dependent acceleration of atherosclerosis in diabetic ApoE-null mice. Circ. Res. 106:1040-1051. http://dx.doi.org/10.1161/CIRCRESAHA.109.201103
2. Cechin, S.R., P.R. Dunkley, and R. Rodnight. 2005. Signal transduction mechanisms involved in the proliferation of C6 glioma cells induced by lysophosphatidic acid. Neurochem. Res. 30:603-611. http://dx.doi.org/10.1007/s11064-005-2747-4
3. Chen, Y., S.S. Yan, J. Colgan, H.P. Zhang, J. Luban, A.M. Schmidt, D. Stern, and K.C. Herold. 2004. Blockade of late stages of autoimmune diabetes by inhibition of the receptor for advanced glycation end products. J. Immunol. 173:1399-1405.
4. Choi, J.W., D.R. Herr, K. Noguchi, Y.C. Yung, C.W. Lee, T. Mutoh, M.E. Lin, S.T. Teo, K.E. Park, A.N. Mosley, and J. Chun. 2010. LPA receptors: subtypes and biological actions. Annu. Rev. Pharmacol. Toxicol. 50:157-186. http://dx.doi.org/10.1146/annurev.pharmtox.010909.105753
5. Chun, J., T. Hla, K.R. Lynch, S. Spiegel, and W.H. Moolenaar. 2010. International Union of Basic and Clinical Pharmacology. LXXVIII. Lysophospholipid receptor nomenclature. Pharmacol. Rev. 62:579-587. http://dx.doi.org/10.1124/pr.110.003111
6. Copeland, J.W., and R. Treisman. 2002. The diaphanous-related formin mDia1 controls serum response factor activity through its effects on actin polymerization. Mol. Biol. Cell. 13:4088-4099. http://dx.doi.org/10.1091/mbc.02-06-0092
7. Dattilo, B.M., G. Fritz, E. Leclerc, C.W. Kooi, C.W. Heizmann, and W.J. Chazin. 2007. The extracellular region of the receptor for advanced glycation end products is composed of two independent structural units. Biochemistry. 46:6957-6970. http://dx.doi.org/10.1021/bi7003735
8. Eng, C.H., T.M. Huckaba, and G.G. Gundersen. 2006. The formin mDia regulates GSK3beta through novel PKCs to promote microtubule stabilization but not MTOC reorientation in migrating fibroblasts. Mol. Biol. Cell. 17:5004-5016. http://dx.doi.org/10.1091/mbc.E05-10-0914
9. Georas, S.N. 2009. Lysophosphatidic acid and autotaxin: emerging roles in innate and adaptive immunity. Immunol. Res. 45:229-238. http://dx.doi.org/10.1007/s12026-009-8104-y
10. Hofmann, M.A., S. Drury, C. Fu, W. Qu, A. Taguchi, Y. Lu, C. Avila, N. Kambham, A. Bierhaus, P. Nawroth, et al. 1999. RAGE mediates a novel proinflammatory axis: a central cell surface receptor for S100/calgranulin polypeptides. Cell. 97:889-901. http://dx.doi.org/10.1016/S0092-8674(00)80801-6
11. Hudson, B.I., A.Z. Kalea, M. Del Mar Arriero, E. Harja, E. Boulanger, V. D'Agati, and A.M. Schmidt. 2008. Interaction of the RAGE cytoplasmic domain with diaphanous-1 is required for ligand-stimulated cellular migration through activation of Rac1 and Cdc42. J. Biol. Chem. 283:34457-34468. http://dx.doi.org/10.1074/jbc.M801465200
12. Kim, J., J.R. Keys, and A.D. Eckhart. 2006. Vascular smooth muscle migration and proliferation in response to lysophosphatidic acid (LPA) is mediated by LPA receptors coupling to Gq. Cell. Signal. 18:1695-1701. http://dx.doi.org/10.1016/j.cellsig.2006.01.009
13. Kitzing, T.M., A.S. Sahadevan, D.T. Brandt, H. Knieling, S. Hannemann, O.T. Fackler, J. Grosshans, and R. Grosse. 2007. Positive feedback between Dia1, LARG, and RhoA regulates cell morphology and invasion. Genes Dev. 21:1478-1483. http://dx.doi.org/10.1101/gad.424807
14. Koch, M., S. Chitayat, B.M. Dattilo, A. Schiefner, J. Diez, W.J. Chazin, and G. Fritz. 2010. Structural basis for ligand recognition and activation of RAGE. Structure. 18:1342-1352. http://dx.doi.org/10.1016/j.str.2010.05.017
15. Leclerc, E., G. Fritz, M. Weibel, C.W. Heizmann, and A. Galichet. 2007. S100B and S100A6 differentially modulate cell survival by interacting with distinct RAGE (receptor for advanced glycation end products) immunoglobulin domains. J. Biol. Chem. 282:31317-31331. http://dx.doi.org/10.1074/jbc.M703951200
16. Li, H., D. Wang, H. Zhang, K. Kirmani, Z. Zhao, R. Steinmetz, and Y. Xu. 2009. Lysophosphatidic acid stimulates cell migration, invasion, and colony formation as well as tumorigenesis/metastasis of mouse ovarian cancer in immunocompetent mice. Mol. Cancer Ther. 8:1692-1701. http://dx.doi.org/10.1158/1535-7163.MCT-08-1106
17. Lin, M.E., D.R. Herr, and J. Chun. 2010. Lysophosphatidic acid (LPA) receptors: signaling properties and disease relevance. Prostaglandins Other Lipid Mediat. 91:130-138. http://dx.doi.org/10.1016/j.prostaglandins.2009.02.002
18. Liu, S., M. Umezu-Goto, M. Murph, Y. Lu, W. Liu, F. Zhang, S. Yu, L.C. Stephens, X. Cui, G. Murrow, et al. 2009. Expression of autotaxin and lysophosphatidic acid receptors increases mammary tumorigenesis, invasion, and metastases. Cancer Cell. 15:539-550. http://dx.doi.org/10.1016/j.ccr.2009.03.027
19. McIntyre, T.M., A.V. Pontsler, A.R. Silva, A. St Hilaire, Y. Xu, J.C. Hinshaw, G.A. Zimmerman, K. Hama, J. Aoki, H. Arai, and G.D. Prestwich. 2003. Identification of an intracellular receptor for lysophosphatidic acid (LPA): LPA is a transcellular PPARgamma agonist. Proc. Natl. Acad. Sci. USA. 100:131-136. http://dx.doi.org/10.1073/pnas.0135855100
20. Moolenaar, W.H., L.A. van Meeteren, and B.N. Giepmans. 2004. The ins and outs of lysophosphatidic acid signaling. Bioessays. 26:870-881. http://dx.doi.org/10.1002/bies.20081
21. Pamuklar, Z., L. Federico, S. Liu, M. Umezu-Goto, A. Dong, M. Panchatcharam, Z. Fulkerson, E. Berdyshev, V. Natarajan, X. Fang, et al. 2009. Autotaxin/lysopholipase D and lysophosphatidic acid regulate murine hemostasis and thrombosis. J. Biol. Chem. 284:7385-7394. http://dx.doi.org/10.1074/jbc.M807820200
22. Panchatcharam, M., S. Miriyala, F. Yang, M. Rojas, C. End, C. Vallant, A. Dong, K. Lynch, J. Chun, A.J. Morris, and S.S. Smyth. 2008. Lysophosphatidic acid receptors 1 and 2 play roles in regulation of vascular injury responses but not blood pressure. Circ. Res. 103:662-670. http://dx.doi.org/10.1161/CIRCRESAHA.108.180778
23. Park, L., K.G. Raman, K.J. Lee, Y. Lu, L.J. Ferran Jr., W.S. Chow, D. Stern, and A.M. Schmidt. 1998. Suppression of accelerated diabetic atherosclerosis by the soluble receptor for advanced glycation endproducts. Nat. Med. 4:1025-1031. http://dx.doi.org/10.1038/2012
24. Roby, K.F., C.C. Taylor, J.P. Sweetwood, Y. Cheng, J.L. Pace, O. Tawfik, D.L. Persons, P.G. Smith, and P.F. Terranova. 2000. Development of a syngeneic mouse model for events related to ovarian cancer. Carcinogenesis. 21:585-591. http://dx.doi.org/10.1093/carcin/21.4.585
25. Sakaguchi, T., S.F. Yan, S.D. Yan, D. Belov, L.L. Rong, M. Sousa, M. Andrassy, S.P. Marso, S. Duda, B. Arnold, et al. 2003. Central role of RAGE-dependent neointimal expansion in arterial restenosis. J. Clin. Invest. 111:959-972.
26. Shang, L., R. Ananthakrishnan, Q. Li, N. Quadri, M. Abdillahi, Z. Zhu, W. Qu, R. Rosario, F. Touré, S.F. Yan, et al. 2010. RAGE modulates hypoxia/reoxygenation injury in adult murine cardiomyocytes via JNK and GSK-3beta signaling pathways. PLoS ONE. 5:e10092. http://dx.doi.org/10.1371/journal.pone.0010092
27. Smyth, S.S., H.Y. Cheng, S. Miriyala, M. Panchatcharam, and A.J. Morris. 2008. Roles of lysophosphatidic acid in cardiovascular physiology and disease. Biochim. Biophys. Acta. 1781:563-570. http://dx.doi.org/10.1016/j.bbalip.2008.05.008
28. Taguchi, A., D.C. Blood, G. del Toro, A. Canet, D.C. Lee, W. Qu, N. Tanji, Y. Lu, E. Lalla, C. Fu, et al. 2000. Blockade of RAGE-amphoterin signalling suppresses tumour growth and metastases. Nature. 405:354-360. http://dx.doi.org/10.1038/35012626
29. Touré, F., G. Fritz, Q. Li, V. Rai, G. Daffu, Y.S. Zou, R. Rosario, R. Ramasamy, A.S. Alberts, S.F. Yan, and A.M. Schmidt. 2012. Formin mDia1 mediates vascular remodeling via integration of oxidative and signal transduction pathways. Circ. Res. 110:1279-1293. http://dx.doi.org/10.1161/CIRCRESAHA.111.262519
30. Valentine, W.J., Y. Fujiwara, R. Tsukahara, and G. Tigyi. 2008. Lysophospholipid signaling: beyond the EDGs. Biochim. Biophys. Acta. 1780: 597-605. http://dx.doi.org/10.1016/j.bbagen.2007.08.008
31. Xu, Y., F. Toure, W. Qu, L. Lin, F. Song, X. Shen, R. Rosario, J. Garcia, A.M. Schmidt, and S.F. Yan. 2010. Advanced glycation end product (AGE)-receptor for AGE (RAGE) signaling and up-regulation of Egr-1 in hypoxic macrophages. J. Biol. Chem. 285:23233-23240. http://dx.doi.org/10.1074/jbc.M110.117457
32. Xue, J., V. Rai, D. Singer, S. Chabierski, J. Xie, S. Reverdatto, D.S. Burz, A.M. Schmidt, R. Hoffmann, and A. Shekhtman. 2011. Advanced glycation end product recognition by the receptor for AGEs. Structure. 19:722-732. http://dx.doi.org/10.1016/j.str.2011.02.013
33. Yan, S.F., R. Ramasamy, and A.M. Schmidt. 2010. The RAGE axis: a fundamental mechanism signaling danger to the vulnerable vasculature. Circ. Res. 106:842-853. http://dx.doi.org/10.1161/CIRCRESAHA.109.212217
34. Zhou, Z., K. Wang, M.S. Penn, S.P. Marso, M.A. Lauer, F. Forudi, X. Zhou, W. Qu, Y. Lu, D.M. Stern, et al. 2003. Receptor for AGE (RAGE) mediates neointimal formation in response to arterial injury. Circulation. 107:2238-2243. http://dx.doi.org/10.1161/01.CIR.0000063577.32819.23