Lysophosphatidic acid induces integrin activation in vascular smooth: Muscle and alters arteriolar myogenic vasoconstriction

Frontiers in Physiology

Volumn 5, Issue OCT, 2014, Pages

  Staiculescu, Marius C ^a   Ramirez Perez, Francisco I ^a,b   Castorena Gonzalez, Jorge A ^a,b   Hong, Zhongkui ^a   Sun, Zhe ^a   Meininger, Gerald A ^a,b,c   Martinez Lemus, Luis A ^a,b,c  

^a UNIVERSITY OF MISSOURI   (United States)

^b UNIVERSITY OF MISSOURI   (United States)

^c University of Missouri   (United States)

Author keywords

Basal tone; Fibronectin; Focal adhesion; Integrin activation; Myogenic response; Reactive oxygen species

Indexed keywords

FIBRONECTIN; INTEGRIN; LYSOPHOSPHATIDIC ACID; LYSOPHOSPHATIDIC ACID RECEPTOR; LYSOPHOSPHATIDIC ACID RECEPTOR 1; LYSOPHOSPHATIDIC ACID RECEPTOR 3; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTERIOLE; ARTICLE; BLOOD VESSEL TONE; CELL ADHESION; CONTROLLED STUDY; CREMASTER MUSCLE; EX VIVO STUDY; EXTRACELLULAR MATRIX; MALE; NONHUMAN; PROTEIN PROTEIN INTERACTION; RAT; RESISTANCE BLOOD VESSEL; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; VASCULAR SMOOTH MUSCLE; VASOCONSTRICTION;

EID: 84908383806     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2014.00413     Document Type: Article

References (67)

1. Balasubramanian, L., Ahmed, A., Lo, C.-M., Sham, J.S.K., and Yip, K.-P. (2007). Integrin-mediated mechanotransduction in renal vascular smooth muscle cells: activation of calcium sparks. American Journal of Physiology -Regulatory, Integrative and Comparative Physiology 293, R1586-R1594. doi: 10.1152/ajpregu.00025.2007.
2. Barillari, G., Albonici, L., Incerpi, S., Bogetto, L., Pistritto, G., Volpi, A., Ensoli, B., and Manzari, V. (2001). Inflammatory cytokines stimulate vascular smooth muscle cells locomotion and growth by enhancing alpha5beta1 integrin expression and function. Atherosclerosis 154, 377-385.
3. Begonja, A.J., Gambaryan, S., Geiger, J.R., Aktas, B., Pozgajova, M., Nieswandt, B., and Walter, U. (2005). Platelet NAD(P)H-oxidase-generated ROS production regulates aIIbb3-integrin activation independent of the NO/cGMP pathway. Blood 106, 2757-2760. doi: 10.1182/blood-2005-03-1047.
4. Charo, I.F., Nannizzi, L., Smith, J.W., and Cheresh, D.A. (1990). The vitronectin receptor alpha v beta 3 binds fibronectin and acts in concert with alpha 5 beta 1 in promoting cellular attachment and spreading on fibronectin. J Cell Biol 111, 2795-2800.
5. Cheng, Y., Makarova, N., Tsukahara, R., Guo, H., Shuyu, E., Farrar, P., Balazs, L., Zhang, C., and Tigyi, G. (2009). Lysophosphatidic acid-induced arterial wall remodeling: Requirement of PPARg but not LPA1 or LPA2 GPCR. Cellular Signalling 21, 1874-1884.
6. Choi, J.W., Herr, D.R., Noguchi, K., Yung, Y.C., Lee, C.W., Mutoh, T., Lin, M.E., Teo, S.T., Park, K.E., Mosley, A.N., and Chun, J. (2010). "LPA receptors: Subtypes and biological actions".).
7. Cipolla, M.J., Gokina, N.I., and Osol, G. (2002). Pressure-induced actin polymerization in vascular smooth muscle as a mechanism underlying myogenic behavior. Faseb J 16, 72-76.
8. Cui, M.Z. (2011). Lysophosphatidic acid effects on atherosclerosis and thrombosis. Clinical Lipidology 6, 413-426.
9. Delon, I., and Brown, N.H. (2007). Integrins and the actin cytoskeleton. Current Opinion in Cell Biology 19, 43-50. doi: http://dx.doi.org/10.1016/j.ceb.2006.12.013.
10. Eriksson, A.C., Whiss, P.A., and Nilsson, U.K. (2006). Adhesion of human platelets to albumin is synergistically increased by lysophosphatidic acid and adrenaline in a donor-dependent fashion. Blood Coagulation and Fibrinolysis 17, 359-368.
11. Falcone, J.C., Granger, H.J., and Meininger, G.A. (1993). Enhanced myogenic activation in skeletal muscle arterioles from spontaneously hypertensive rats. American Journal of Physiology -Heart and Circulatory Physiology 265, H1847-H1855.
12. Flavahan, N.A., Bailey, S.R., Flavahan, W.A., Mitra, S., and Flavahan, S. (2005). Imaging remodeling of the actin cytoskeleton in vascular smooth muscle cells after mechanosensitive arteriolar constriction. Am J Physiol Heart Circ Physiol 288, H660-669.
13. Gaaya, A., Poirier, O., Mougenot, N., Hery, T., Atassi, F., Marchand, A., Saulnier-Blache, J.S., Amour, J., Vogt, J., Lompre, A.M., Soubrier, F., and Nadaud, S. (2012). Plasticity-related gene-1 inhibits lysophosphatidic acid-induced vascular smooth muscle cell migration and proliferation and prevents neointima formation. American Journal of Physiology -Cell Physiology 303, C1104-C1114.
14. Gebremedhin, D., Terashvili, M., Wickramasekera, N., Zhang, D.X., Rau, N., Miura, H., and Harder, D.R. (2013). Redox signaling via oxidative inactivation of PTEN modulates pressure-dependent myogenic tone in rat middle cerebral arteries. PLoS ONE 8, e68498. doi: 10.1371/journal.pone.0068498.
15. Gerthoffer, W.T. (2007). Mechanisms of Vascular Smooth Muscle Cell Migration. Circulation Research 100, 607-621. doi: 10.1161/01.res.0000258492.96097.47.
16. Goldschmidt, M.E., Mcleod, K.J., and Taylor, W.R. (2001). Integrin-Mediated Mechanotransduction in Vascular Smooth Muscle Cells: Frequency and Force Response Characteristics. Circulation Research 88, 674-680. doi: 10.1161/hh0701.089749.
17. Gregg, D., De Carvalho, D.D., and Kovacic, H. (2004). Integrins and coagulation: A role for ROS/Redox signaling? Antioxidants and Redox Signaling 6, 757-764.
18. Hearkens, E.H.J., Shaw, L., Ryding, A., Brooker, G., Mullins, J.J., Austin, C., Ohanian, V., and Heagerty, A.M. (2006). aV integrins are necessary for eutrophic inward remodeling of small arteries in hypertension. Hypertension 47, 281-287.
19. Heerkens, E.H., Shaw, L., Ryding, A., Brooker, G., Mullins, J.J., Austin, C., Ohanian, V., and Heagerty, A.M. (2006). alphaV integrins are necessary for eutrophic inward remodeling of small arteries in hypertension. Hypertension 47, 281-287.
20. Heumuller, S., Wind, S., Barbosa-Sicard, E., Schmidt, H.H., Busse, R., Schroder, K., and Brandes, R.P. (2008). Apocynin is not an inhibitor of vascular NADPH oxidases but an antioxidant. Hypertension 51, 211-217.
21. Hill, M.A., and Meininger, G.A. (1993). Impaired arteriolar myogenic reactivity in early experimental diabetes. Diabetes 42, 1226-1232.
22. Hong, Z., Sun, Z., Li, M., Li, Z., Bunyak, F., Ersoy, I., Trzeciakowski, J.P., Staiculescu, M.C., Jin, M., Martinez-Lemus, L., Hill, M.A., Palaniappan, K., and Meininger, G.A. (2014). Vasoactive agonists exert dynamic and coordinated effects on vascular smooth muscle cell elasticity, cytoskeletal remodelling and adhesion. J Physiol 592, 1249-1266. doi: 10.1113/jphysiol.2013.264929.
23. Hong, Z., Sun, Z., Li, Z., Mesquitta, W.T., Trzeciakowski, J.P., and Meininger, G.A. (2012). Coordination of Fibronectin Adhesion with Contraction and Relaxation in Microvascular Smooth Muscle. Cardiovasc Res. doi: 10.1093/cvr/cvs239.
24. Hu, P., and Luo, B.H. (2013). Integrin bi-directional signaling across the plasma membrane. Journal of Cellular Physiology 228, 306-312. doi: 10.1002/jcp.24154.
25. Johansson, S., Svineng, G., Wennerberg, K., Armulik, A., and Lohikangas, L. (1997). Fibronectin-integrin interactions. Frontiers in bioscience: a journal and virtual library 2, d126-146.
26. Kaneyuki, U., Ueda, S., Yamagishi, S.I., Kato, S., Fujimura, T., Shibata, R., Hayashida, A., Yoshimura, J., Kojiro, M., Oshima, K., and Okuda, S. (2007). Pitavastatin inhibits lysophosphatidic acid-induced proliferation and monocyte chemoattractant protein-1 expression in aortic smooth muscle cells by suppressing Rac-1-mediated reactive oxygen species generation. Vascular Pharmacology 46, 286-292. doi: 10.1016/j.vph.2006.11.002.
27. Kim, E.K., Yun, S.J., Do, K.H., Kim, M.S., Cho, M., Sun, D.S., Kim, C.D., Kim, J.H., Birnbaum, M.J., and Bae, S.S. (2008). Lysophosphatidic acid induces cell migration through the selective activation of Akt1. Experimental and Molecular Medicine 40, 445-452. doi: 10.3858/emm.2008.40.4.445.
28. Kim, J., Keys, J.R., and Eckhart, A.D. (2006). Vascular smooth muscle migration and proliferation in response to lysophosphatidic acid (LPA) is mediated by LPA receptors coupling to Gq. Cellular Signalling 18, 1695-1701.
29. Lin, M.-E., Herr, D.R., and Chun, J. (2010). Lysophosphatidic acid (LPA) receptors: Signaling properties and disease relevance. Prostaglandins & Other Lipid Mediators 91, 130-138. doi: http://dx.doi.org/10.1016/j.prostaglandins.2009.02.002.
30. Ma, L., Matsumoto, M., Xie, W., Inoue, M., and Ueda, H. (2009). Evidence for lysophosphatidic acid 1 receptor signaling in the early phase of neuropathic pain mechanisms in experiments using Ki-16425, a lysophosphatidic acid 1 receptor antagonist. Journal of Neurochemistry 109, 603-610. doi: 10.1111/j.1471-4159.2009.05987.x.
31. Martinez-Lemus, L.A. (2008). Persistent Agonist-Induced Vasoconstriction Is Not Required for Angiotensin II to Mediate Inward Remodeling of Isolated Arterioles with Myogenic Tone. J Vasc Res 45, 211-221.
32. Martinez-Lemus, L.A., Crow, T., Davis, M.J., and Meininger, G.A. (2005a). {alpha}v{beta}3-and {alpha}5{beta}1-integrin blockade inhibits myogenic constriction of skeletal muscle resistance arterioles. Am J Physiol Heart Circ Physiol 289, H322-329.
33. Martinez-Lemus, L.A., Hill, M.A., Bolz, S.S., Pohl, U., and Meininger, G.A. (2004). Acute mechanoadaptation of vascular smooth muscle cells in response to continuous arteriolar vasoconstriction: implications for functional remodeling. Faseb J 18, 708-710.
34. Martinez-Lemus, L.A., Sun, Z., Trache, A., Trzciakowski, J.P., and Meininger, G.A. (2005b). Integrins and regulation of the microcirculation: from arterioles to molecular studies using atomic force microscopy. Microcirculation 12, 99-112.
35. Martinez-Lemus, L.A., Wu, X., Wilson, E., Hill, M.A., Davis, G.E., Davis, M.J., and Meininger, G.A. (2003). Integrins as unique receptors for vascular control. J Vasc Res 40, 211-233.
36. Martinez-Lemus, L.A., Zhao, G., Galinanes, E.L., and Boone, M. (2011). Inward remodeling of resistance arteries requires reactive oxygen species-dependent activation of matrix metalloproteinases. American Journal of Physiology -Heart and Circulatory Physiology 300, H2005-H2015. doi: 10.1152/ajpheart.01066.2010.
37. Nam, Y.S., Suh, J.S., Song, H.J., and Sohn, U.D. (2013). Signaling pathway of lysophosphatidic acid-induced contraction in feline esophageal smooth muscle cells. Korean Journal of Physiology and Pharmacology 17, 139-147.
38. Ohta, H., Sato, K., Murata, N., Damirin, A., Malchinkhuu, E., Kon, J., Kimura, T., Tobo, M., Yamazaki, Y., Watanabe, T., Yagi, M., Sato, M., Suzuki, R., Murooka, H., Sakai, T., Nishitoba, T., Im, D.-S., Nochi, H., Tamoto, K., Tomura, H., and Okajima, F. (2003). Ki16425, a Subtype-Selective Antagonist for EDG-Family Lysophosphatidic Acid Receptors. Molecular Pharmacology 64, 994-1005. doi: 10.1124/mol.64.4.994.
39. Pages, C., Simon, M.-F., Valet, P., and Saulnier-Blache, J.S. (2001). Lysophosphatidic acid synthesis and release. Prostaglandins & Other Lipid Mediators 64, 1-10. doi: http://dx.doi.org/10.1016/S0090-6980(01)00110-1.
40. Panchatcharam, M., Miriyala, S., Yang, F., Rojas, M., End, C., Vallant, C., Dong, A., Lynch, K., Chun, J., Morris, A.J., and Smyth, S.S. (2008). Lysophosphatidic acid receptors 1 and 2 play roles in regulation of vascular injury responses but not blood pressure. Circulation Research 103, 662-670.
41. Pua, T.L., Wang, F.Q., and Fishman, D.A. (2009). Roles of LPA in ovarian cancer development and progression. Future Oncol 5, 1659-1673.
42. Qiu, H., Zhu, Y., Sun, Z., Trzeciakowski, J.P., Gansner, M., Depre, C., Resuello, R.R.G., Natividad, F.F., Hunter, W.C., Genin, G.M., Elson, E.L., Vatner, D.E., Meininger, G.A., and Vatner, S.F. (2010). Short Communication: Vascular Smooth Muscle Cell Stiffness As a Mechanism for Increased Aortic Stiffness With Aging. Circulation Research 107, 615-619. doi: 10.1161/circresaha.110.221846.
43. Ren, Y., D'ambrosio, M.A., Liu, R., Pagano, P.J., Garvin, J.L., and Carretero, O.A. (2010). Enhanced myogenic response in the afferent arteriole of spontaneously hypertensive rats. American Journal of Physiology -Heart and Circulatory Physiology 298, H1769-H1775. doi: 10.1152/ajpheart.00537.2009.
44. Schleifenbaum, J., Kassmann, M., Szijarto, I.A., Hercule, H.C., Tano, J.Y., Weinert, S., Heidenreich, M., Pathan, A.R., Anistan, Y.M., Alenina, N., Rusch, N.J., Bader, M., Jentsch, T.J., and Gollasch, M. (2014). Stretch-activation of angiotensin II type 1a receptors contributes to the myogenic response of mouse mesenteric and renal arteries. Circ Res 115, 263-272. doi: 10.1161/CIRCRESAHA.115.302882.
45. Schluter, T., Steinbach, A.C., Steffen, A., Rettig, R., and Grisk, O. (2008). Apocynin-induced vasodilation involves Rho kinase inhibition but not NADPH oxidase inhibition. Cardiovascular Research 80, 271-279. doi: 10.1093/cvr/cvn185.
46. Schmitz, U., Thommes, K., Beier, I., and Vetter, H. (2002). Lysophosphatidic acid stimulates p21-activated kinase in vascular smooth muscle cells. Biochemical and Biophysical Research Communications 291, 687-691. doi: 10.1006/bbrc.2002.6493.
47. Sehgel, N.L., Zhu, Y., Sun, Z., Trzeciakowski, J.P., Hong, Z., Hunter, W.C., Vatner, D.E., Meininger, G.A., and Vatner, S.F. (2013). Increased vascular smooth muscle cell stiffness: A novel mechanism for aortic stiffness in hypertension. American Journal of Physiology -Heart and Circulatory Physiology 305, H1281-H1287. doi: 10.1152/ajpheart.00232.2013.
48. Smyth, S.S., Cheng, H.-Y., Miriyala, S., Panchatcharam, M., and Morris, A.J. (2008). Roles of lysophosphatidic acid in cardiovascular physiology and disease. Biochimica et Biophysica Acta (BBA) -Molecular and Cell Biology of Lipids 1781, 563-570. doi: 10.1016/j.bbalip.2008.05.008.
49. Staiculescu, M.C., Galinanes, E.L., Zhao, G., Ulloa, U., Jin, M., Beig, M.I., Meininger, G.A., and Martinez-Lemus, L.A. (2013). Prolonged vasoconstriction of resistance arteries involves vascular smooth muscle actin polymerization leading to inward remodelling. Cardiovascular Research 98, 428-436.
50. Subramanian, P., Karshovska, E., Reinhard, P., Megens, R.T.A., Zhou, Z., Akhtar, S., Schumann, U., Li, X., Van Zandvoort, M., Ludin, C., Weber, C., and Schober, A. (2010). Lysophosphatidic acid receptors LPA1 and LPA3 promote CXCL12-mediated smooth muscle progenitor cell recruitment in neointima formation. Circulation Research 107, 96-105.
51. Sumida, H., Noguchi, K., Kihara, Y., Abe, M., Yanagida, K., Hamano, F., Sato, S., Tamaki, K., Morishita, Y., Kano, M.R., Iwata, C., Miyazono, K., Sakimura, K., Shimizu, T., and Ishii, S. (2010). LPA4 regulates blood and lymphatic vessel formation during mouse embryogenesis. Blood 116, 5060-5070.
52. Sun, Z., Martinez-Lemus, L.A., Hill, M.A., and Meininger, G.A. (2008). Extracellular matrix-specific focal adhesions in vascular smooth muscle produce mechanically active adhesion sites. Am J Physiol Cell Physiol 295, C268-278. doi: 00516.2007 [pii] 10.1152/ajpcell.00516.2007.
53. Sun, Z., Martinez-Lemus, L.A., Trache, A., Trzeciakowski, J.P., Davis, G.E., Pohl, U., and Meininger, G.A. (2005). Mechanical properties of the interaction between fibronectin and alpha5beta1-integrin on vascular smooth muscle cells studied using atomic force microscopy. Am J Physiol Heart Circ Physiol 289, H2526-2535.
54. Swarthout, J.T., and Walling, H.W. (2000). Lysophosphatidic acid: receptors, signaling and survival. Cell Mol Life Sci 57, 1978-1985.
55. Tatler, A.L., John, A.E., Jolly, L., Habgood, A., Porte, J., Brightling, C., Knox, A.J., Pang, L., Sheppard, D., Huang, X., and Jenkins, G. (2011). Integrin avb5-mediated TGF-b activation by airway smooth muscle cells in asthma. Journal of Immunology 187, 6094-6107. doi: 10.4049/jimmunol.1003507.
56. Tigyi, G., Hong, L., Yakubu, M., Parfenova, H., Shibata, M., and Leffler, C.W. (1995). Lysophosphatidic acid alters cerebrovascular reactivity in piglets. American Journal of Physiology -Heart and Circulatory Physiology 268, H2048-H2055.
57. Tokumura, A., Fukuzawa, K., and Tsukatani, H. (1978). Effects of synthetic and natural lysophosphatidic acids on the arterial blood pressure of different animal species. Lipids 13, 572-574.
58. Tokumura, A., Maruyama, T., Fukuzawa, K., and Tsukatani, H. (1985). Effects of lysophosphatidic acids and their structural analogs on arterial blood pressure of cats. Arzneimittel-Forschung/Drug Research 35, 587-592.
59. Tokumura, A., Yotsumoto, T., Masuda, Y., and Tanaka, S. (1995). Vasopressor effect of lysophosphatidic acid on spontaneously hypertensive rats and Wistar Kyoto rats. Research Communications in Molecular Pathology and Pharmacology 90, 96-102.
60. Valenick, L.V., and Schwarzbauer, J.E. (2006). Ligand density and integrin repertoire regulate cellular response to LPA. Matrix Biology 25, 223-231.
61. Wilcox, C.S., and Pearlman, A. (2008). Chemistry and antihypertensive effects of tempol and other nitroxides. Pharmacol Rev 60, 418-469. doi: 10.1124/pr.108.000240.
62. Wilson, E., Sudhir, K., and Ives, H.E. (1995). Mechanical strain of rat vascular smooth muscle cells is sensed by specific extracellular matrix/integrin interactions. Journal of Clinical Investigation 96, 2364-2372.
63. Wu, C., Bauer, J.S., Juliano, R.L., and Mcdonald, J.A. (1993). The alpha 5 beta 1 integrin fibronectin receptor, but not the alpha 5 cytoplasmic domain, functions in an early and essential step in fibronectin matrix assembly. Journal of Biological Chemistry 268, 21883-21888.
64. Yanagida, K., and Ishii, S. (2011). Non-Edg family LPA receptors: The cutting edge of LPA research. Journal of Biochemistry 150, 223-232.
65. Yoshida, K., Nishida, W., Hayashi, K.I., Ohkawa, Y., Ogawa, A., Aoki, J., Arai, H., and Sobue, K. (2003). Vascular Remodeling Induced by Naturally Occurring Unsaturated Lysophosphatidic Acid In Vivo. Circulation 108, 1746-1752. doi: 10.1161/01.cir.0000089374.35455.f3.
66. Zhou, Z., Niu, J., and Zhang, Z. (2010). The role of lysophosphatidic acid receptors in phenotypic modulation of vascular smooth muscle cells. Molecular Biology Reports 37, 2675-2686.
67. Zhu Y., Qiu H., Trzeciakowski J.P., Sun Z., Li Z., Hong Z., Hill M.A., Hunter W.C., Vatner D.E., Vatner S.F., Meininger G.A. Temporal analysis of vascular smooth muscle cell elasticity and adhesion reveals oscillation waveforms that differ with aging. Aging Cell, 2012, 11, 741-750, 10.1111/j.1474-9726.2012.00840.x