Lysophosphatidic acid signals through specific lysophosphatidic acid receptor subtypes to control key regenerative responses of human gingival and periodontal ligament fibroblasts

Journal of Periodontology

Volumn 80, Issue 8, 2009, Pages 1338-1347

  George, Joju ^a   Headen, Karmel V ^b   Ogunleye, Afolabi O ^b   Perry, Greg A ^a   Wilwerding, Terrence M ^b   Parrish, Lawrence C ^b   Mcvaney, Timothy P ^b   Mattson, John S ^b   Cerutis, D Roselyn ^b  

^a CREIGHTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b CREIGHTON UNIVERSITY   (United States)

Author keywords

Fibroblasts; Growth factors; Molecular biology; Periodontal regeneration; Pharmacology

Indexed keywords

1 OLEOYL 2 O METHYL RAC GLYCEROPHOSPHOTHIONATE; 1-OLEOYL-2-O-METHYL-RAC-GLYCEROPHOSPHOTHIONATE; 3 (4 (4 ((1 (2 CHLOROPHENYL)ETHOXY)CARBONYL AMINO) 3 METHYL 5 ISOXAZOLYL) BENZYLSULFANYL) PROPANOIC ACID; 3-(4-(4-((1-(2-CHLOROPHENYL)ETHOXY)CARBONYL AMINO)-3-METHYL-5-ISOXAZOLYL) BENZYLSULFANYL) PROPANOIC ACID; DIAGNOSTIC AGENT; FLUORESCENT DYE; ISOXAZOLE DERIVATIVE; LYSOPHOSPHATIDIC ACID; LYSOPHOSPHATIDIC ACID RECEPTOR; LYSOPHOSPHOLIPID; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PHOSPHATIDIC ACID; PHOSPHOROTHIOIC ACID DERIVATIVE; PROPIONIC ACID DERIVATIVE;

ADULT; ARTICLE; CALCIUM SIGNALING; CELL CULTURE; CHEMOTAXIS; CLASSIFICATION; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; DRUG POTENTIATION; FEMALE; FIBROBLAST; GINGIVA; HUMAN; MALE; PERIODONTAL LIGAMENT; PHOSPHORYLATION; PHYSIOLOGY; REGENERATION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; WOUND HEALING;

ADULT; BLOTTING, WESTERN; CALCIUM SIGNALING; CELLS, CULTURED; CHEMOTAXIS; FEMALE; FIBROBLASTS; FLUORESCENT DYES; GINGIVA; HUMANS; ISOXAZOLES; LYSOPHOSPHOLIPIDS; MALE; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; PERIODONTAL LIGAMENT; PHOSPHATIDIC ACIDS; PHOSPHORYLATION; PROPIONIC ACIDS; RECEPTORS, LYSOPHOSPHATIDIC ACID; REGENERATION; SIGNAL TRANSDUCTION; THIOPHOSPHORIC ACID ESTERS; WOUND HEALING; YOUNG ADULT;

EID: 68749119524     PISSN: 00223492     EISSN: None     Source Type: Journal    
DOI: 10.1902/jop.2009.080624     Document Type: Article

References (51)

1. Garrett S. Early wound healing stability and its importance in periodontal regeneration. In: Polson AM, ed. Periodontal Regeneration: Current Status and Directions. Chicago: Quintessence Publishing; 1994: 42-44.
2. Anusaksathien O., Webb S. A., Jin Q. M., Giannobile W. V. Platelet-derived growth factor gene delivery stimulates ex vivo gingival repair. Tissue Eng 2003;9:745-756.
3. Rother E., Brandl R., Baker D. L., et al. Subtype-selective antagonists of lysophosphatidic acid receptors inhibit platelet activation triggered by the lipid core of atherosclerotic plaques. Circulation 2003;108:741-747.
4. Moolenaar W. H., Kranenburg O., Postma F. R., Zondag G. C. Lysophosphatidic acid: G-protein signaling and cellular responses. Curr Opin Cell Biol 1997;9:168-173.
5. Sugiura T., Nakane S., Kishimoto S., Waku K., Yoshioka Y., Tokumura A. Lysophosphatidic acid, a growth factorlike lipid, in the saliva. J Lipid Res 2002;43:2049-2055.
6. Westermann A. M., Havik E., Postma F. R., et al. Malignant effusions contain lysophosphatidic acid (LPA-like) activity. Ann Oncol 1998;9:437-442.
7. Sano T., Baker D., Virag T., et al. Multiple mechanisms linked to platelet activation result in lysophosphatidic acid and sphingosine-1-phosphate generation in blood. J Biol Chem 2002;277:21197-21206.
8. Pages C., Simon M. F., Valet P., Saulnier-Blache J. S. Lysophosphatidic acid synthesis and release. Prosta-glandins Other Lipid Mediat 2001;64:1-10.
9. Gendaszewska-Darmach E. Lysophosphatidic acids, cyclic phosphatidic acids and autotaxin as promising targets in therapies of cancer and other diseases. Acta Biochim Pol 2008;55:227-240.
10. Murph M., Tanaka T., Liu S., Mills G. B. Of spiders and crabs: The emergence of lysophospholipids and their metabolic pathways as targets for therapy in cancer. Clin Cancer Res 2006;12:6598-6602.
11. Lee C. W., Rivera S., Gardell A. E., Dubin J., Chun J. GPR92 as a new G12/13 and Gq-coupled lysophos-phatidic acid receptor that increases cAMP, LPA5. J Biol Chem 2006;281:23589-23597.
12. Pasternack S. M., von Kugelgen I., Aboud AK, et al. G protein-coupled receptor P2Y5 and its ligand LPA are involved in maintenance of human hair growth. Nat Genet 2008;40:329-334.
13. Shimizu T. Lipid mediators in health and disease: Enzymes and receptors as therapeutic targets for the regulation of immunity and inflammation. Annu Rev Pharmacol Toxicol 2009;49:123-150.
14. Ye X., Hama K., Contos J. J., et al. LPA3-mediated lysophosphatidic acid signaling in embryo implantation and spacing. Nature 2005;435:104-108.
15. Lee Z., Ching-Teng C., Zhang H., et al. Role of LPA4/P2Y9/GPR23 in negative regulation of cell motility. Mol Biol Cell 2008;19:5435-5445.
16. van Meeteren L. A., Ruurs P., Stortelers C., et al. Auto-taxin, a secreted phospholipase D, is essential for blood vessel formation during development. Mol Cell Biol 2006;26:5015-5022.
17. Lin F. T., Lai Y. J. Regulation of the LPA2 receptor signaling through the carboxylterminal tail-mediated protein-protein interactions. Biochim Biophys Acta 2008;1781:558-562.
18. Meyer Zu Heringdorf D., Jakobs K. H. Lysophospholipid receptors: Signalling, pharmacology and regulation by lysophospholipid metabolism. Biochim Biophys Acta 2007;1768:923-940.
19. Liliom K., Guan Z., Tseng J. L., Desiderio D. M., Tigyi G, Watsky MA. Growth factor-like phospholipids generated after corneal injury. Am J Physiol 1998; 274: C1065-C1074.
20. Watsky M. A., Griffith M., Wang D.-A., Tigyi G. J. Phospho-lipid growth factors and corneal wound healing. Ann N Y Acad Sci 2000;905:142-158.
21. Balazs L., Okolicany J., Ferrebee M., Tolley B., Tigyi G. Topical application of the phospholipid growth factor lysophosphatidic acid promotes wound healing in vivo. Am J Physiol Regul Integr Comp Physiol 2001; 280: R466-R472.
22. Fukushima N., Ishii I., Contos J. J. A., Weiner J., Chun J. Lysophospholipid receptors. Annu Rev Pharmacol Toxicol 2001;41:507-534.
23. Herrlich A., Daub H., Knebel A., Herrlich P., Schultz G, Gudermann T. Ligand-independent activation of PDGF receptor is a necessary intermediate in lyso-phosphatidic, acid-stimulated mitogenic activity in L cells. Proc Natl Acad Sci USA 1998;95:8985-8990.
24. Cerutis D. R., Dreyer A., Cordini F., et al. Lysophospha-tidic acid modulates the regenerative responses of human gingival fibroblasts and enhances the actions of platelet-derived growth factor. J Periodontol 2004;75:297-305.
25. Cerutis D. R., Dreyer A. C., Vierra M. J., et al. Lysophos-phatidic acid modulates the regenerative responses of human periodontal ligament fibroblasts and enhances the actions of platelet-derived growth factor. J Peri-odontol 2007;78:1136-1145.
26. Gruber R., Kandler B., Jindra C., Watzak G., Watzek G. Dental pulp fibroblasts contain target cells for lyso-phosphatidic acid. J Dent Res 2004;83:491-495.
27. Haugland R. P. Fluorescent Ca (2+) indicators excited with visible light. In: Spence MTZ, ed. The Handbook - A Guide to Fluorescent Probes and Labeling Technologies. Carlsbad, CA: Invitrogen; 2005: 889-902.
28. Walker S. A., Cullen P. J., Taylor J. A., Lockyer P. J. Control of Ras cycling by Ca2+. FEBS Lett 2003;546:6-10.
29. Lawrence H. P. Salivary markers of systemic disease: Noninvasive diagnosis of disease and monitoring of general health. J Can Dent Assoc 2002;68:170-174.
30. Baker D. L., Desiderio D. M., Miller D. D., Tolley B., Tigyi G. J. Direct quantitative analysis of lysophosphatidic acid molecular species by stable isotope dilution electrospray ionization liquid chromatography-mass spec-trometry. Anal Biochem 2001;292:287-295.
31. Fujiwara Y., Sardar V., Tokumura A., et al. Identification of residues responsible for ligand recognition and regioisomeric selectivity of lysophosphatidic acid receptors expressed in mammalian cells. J Biol Chem 2005;280:35038-35050.
32. Parrill A. L. Lysophospholipid interactions with protein targets. Biochim Biophys Acta 2008;1781:540-546.
33. 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;274:27776-27785.
34. Im D. S., Heise C. E., Harding M. A., et al. Molecular cloning of a lysophospholipid acid receptor, edg-7, expressed in prostate. Mol Pharmacol 2000;57:753-759.
35. Yoon S., Seger R. The extracellular signal-regulated kinase: Multiple substrates regulate diverse cellular functions. Growth Factors 2006;24:21-44.
36. Pullikuth A. K., Catling A. D. Scaffold-mediated regulation of MAPK signaling and cytoskeletal dynamics: A perspective. Cell Signal 2007;19:1621-1632.
37. Alderton F., Sambi B., Tate R., Pyne N. J., Pyne S. Assessment of agonism at G-protein coupled receptors by phosphatidic acid and lysophosphatidic acid in human embryonic kidney 293 cells. Br J Pharmacol 2001;134:6-9.
38. Moughal N. A., Waters C., Sambi B., Pyne S., Pyne N. J. Nerve growth factor signaling involves interaction between the Trk A receptor and lysophosphatidate receptor 1 systems: Nuclear translocation of the lysophosphati-date receptor 1 and TrkA receptors in pheochromocy-toma 12 cells. Cell Signal 2004;16:127-136.
39. Anliker B., Chun J. Cell surface receptors in lysophos-pholipid signaling. Semin Cell Dev Biol 2004;15:457-465.
40. Yun C. C., Sun H., Wang D., et al. LPA2 receptor mediates mitogenic signals in human colon cancer cells. Am J Physiol Cell Physiol 2005; 289: C2-C11.
41. Luttrell L. M., Van Biesen T., Hawes B. E., Koch W. J., Touhara K., Lefkowitz R. J. G. (βγ) subunits mediate mitogen-activated protein kinase activation by the tyrosine kinase insulin-like growth factor 1 receptor. J Biol Chem 1995;270:16495-16498.
42. Conway A. M., Rakhit S., Pyne S., Pyne N. Platelet-derived-growth-factor stimulation of the p42/p44 mi-togen-activated protein kinase pathway in airway smooth muscle: Role of pertussis-toxin-sensitive G proteins, c-Src tyrosine kinases and phosphoinositide 3-kinase. Biochem J 1999;337:171-177.
43. Van Leeuwen F. N., Giepmans B. N. G., Van Meeteren L. A., Moolenaar W. H. Lysophosphatidic acid: Mitogen and motility factor. Biochem Soc Trans 2003;31:1209-1212.
44. Chen M., Towers N. L., O'Connor K. L. LPA2 (Edg4) mediates Rho-dependent chemotaxis with lower efficacy than LPA1 (Edg2) in breast carcinoma cells. Am J Physiol Cell Physiol 2007; 292: C 1927-1933.
45. Shida D., Kitayama J., Yamaguchi H., et al. Lysophos-phatidic acid (LPA) enhances the metastatic potential of human colon carcinoma cells through LPA1. Cancer Res 2003;63:1706-1711.
46. Chan L. C., Peters W., Xu Y., Chun J., Farese R. V. Jr., Cases S. LPA3 receptor mediates chemotaxis of immature murine dendritic cells to unsaturated lysophosphatidic acid (LPA). J Leukoc Biol 2007;82:1193-1200.
47. Masiello L. M., Fotos J. S., Galileo D. S., Karin N. J. Lyso-phosphatidic acid induces chemotaxis in MC3T3-E1 osteoblastic cells. Bone 2006;39:72-82.
48. Sammak P. J., Hinman L. E., Tran P. O., Sjaastad M. D., Machen T. E. How do injured cells communicate with the surviving cell monolayer? J Cell Sci 1997;110:465-475.
49. Lichte K., Rossi R., Danneberg K., et al. Lysophospholipid receptor-mediated calcium signaling in human keratino-cytes. J Invest Dermatol 2008;128:1487-1498.
50. Chang Y. J., Kim Y. L., Lee Y. K., et al. Dioleoyl phosphatidic acid increases intracellular Ca2+ through endogenous LPA receptors in C6 glioma and L2071 fibroblasts. Prostaglandins Other Lipid Mediat 2007;83:268-276.
51. Arita Y., Ito T., Oono T., Kawabe K., Hisano T., Takayanagi R. Lysophosphatidic acid induced nuclear translocation of nuclear factor-κB in Panc-1 cells by mobilizing free cytosolic calcium. World J Gastroenterol 2008;14:4473-4479.