Lipid phosphate phosphatase-1 regulates lysophosphatidic acid-induced calcium release, NF-κB activation and interleukin-8 secretion in human bronchial epithelial cells

Biochemical Journal

Volumn 385, Issue 2, 2005, Pages 493-502

  Zhao, Yutong ^a   Usatyuk, Peter V ^a   Cummings, Rhett ^a   Saatian, Bahman ^a   He, Donghong ^a   Watkins, Tonya ^a   Morris, Andrew ^b   Spannhake, Ernst Wm ^c   Brindley, David N ^d   Natarajan, Viswanathan ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^c The Johns Hopkins University   (United States)

^d UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Bioactive phospholipid; Cytokine; Inflammation; Interleukin 8 secretion; Lipid phosphate phosphatase 1 (LPP 1); Lysophosphatidic acid (LPA)

Indexed keywords

CELL CULTURE; GENES; HYDROLYSIS; PHOSPHOLIPIDS; PROTEINS;

HUMAN BRONCHIAL EPITHELIAL CELLS (HBEPC); LIPID PHOSPHATE PHOSPHATASES (LPP); LYSOPHOSPHATIDIC ACID (LPA); PHOSPHORYLATION;

ENZYME KINETICS;

ADENOVIRUS VECTOR; CALCIUM; G PROTEIN COUPLED RECEPTOR; I KAPPA B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 8; LIPID PHOSPHATE PHOSPHATASE 1; LYSOPHOSPHATIDIC ACID; PHOSPHATASE; UNCLASSIFIED DRUG;

ARTICLE; BRONCHUS MUCOSA; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CELL NUCLEUS; CHEMOTAXIS; CONTROLLED STUDY; CYTOKINE RELEASE; GENE EXPRESSION; HUMAN; HUMAN CELL; INFLAMMATION; NORMAL HUMAN; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ADENOVIRIDAE; ARGININE; BRONCHI; CALCIUM; CELL EXTRACTS; CELLS, CULTURED; EPITHELIAL CELLS; HUMANS; INTERLEUKIN-8; LUNG TRANSPLANTATION; LYSINE; LYSOPHOSPHOLIPIDS; MUTATION, MISSENSE; NF-KAPPA B; PHOSPHATIDATE PHOSPHATASE; RECEPTORS, LYSOPHOSPHATIDIC ACID; TISSUE DONORS;

ADENOVIRIDAE; BRONCHUS;

EID: 19944432760     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20041160     Document Type: Article

References (51)

1. Tokumura, A. (2002) Physiological and pathophysiological roles of lysophosphatidic acids produced by secretory lysophospholipase D in body fluids. Biochim. Biophys. Acta 1582, 18-25
2. Goetzl, E. J., Dolezalova, H., Kong, Y. and Zeng, L. (1999) Dual mechanisms for lysophospholipid induction of proliferation of human breast carcinoma cells. Cancer Res. 59, 4732-4737
3. Huang, M. C., Graeler, M., Shankar, G., Spencer, J. and Goetzl, E. J. (2002) Lysophospholipid mediators of immunity and neoplasia. Biochim. Biophys. Acta 1582, 161-167
4. Gennero, I., Xuereb, J. and Simon, M. (1999) Effects of lysophosphatidic acid on proliferation and cytosol Ca++ of human adult vascular smooth muscle cells in culture. Thromb. Res. 94, 317-326
5. 2+ mobilization in human A431 cells: structure-activity analysis. Biochem. J. 307, 609-616
6. Moolenaar, W. H. (1995) Lysophosphatidic acid, a multifunctional phospholipid messenger. J. Biol. Chem. 270, 12949-12952
7. g/GPR23 as a novel G protein-coupled receptor for lysophosphatidic acid, structurally distant from the Edg family. J. Biol. Chem. 278, 25600-25606
8. Retzer, M. and Essler, M. (2000) Lysophosphatidic acid-induced platelet shape change proceeds via Rho/Rho kinase-mediated myosin light-chain and moesin phosphorylation. Cell Signaling 12, 645-648
9. 2+ mobilization requires intracellular sphingosine 1-phosphate production. Potential involvement of endogenous EDG-4 receptors. J. Biol. Chem. 275, 38532-38539
10. McIntyre, T. M., Pontsler, A. V., Silva, A. R., Hilaire, A. S., Xu, Y., Hinshaw, J. C., Zimmerman, G. A., Hama, K., Aoki, H. and Prestwich, G. D. (2003) Identification of an intracellular receptor for lysophosphatidic acid (LPA): LPA is a transcellular PPARγ agonist. Proc. Natl. Acad. Sci. U.S.A. 100, 131-136
11. Wang, L., Cummings, R., Zhao, Y., Kazlauskas, A., Sham, J., Morris, A., Georas, S., Brindley, D. N. and Natarajan, V. (2003) Involvement of phospholipase D2 in lysophosphatidate-induced transactivation of platelet-derived growth factor receptor-β in human bronchial epithelial cell. J. Biol. Chem. 278, 39931-39940
12. Bousquet, J., Jeffery, P. K., Busse, W. W., Johnson, M. and Vignola, A. M. (2000) Asthma from bronchoconstriction to airways inflammation and remodeling. Am. J. Respir. Crit. Care Med. 161, 1720-1745
13. Toews, M. L., Ediger, T. L., Romberger, D. J. and Rennard, S. I. (2002) Lysophosphatidic acid in airway function and disease. Biochim. Biophys. Acta 1582, 240-250
14. Cummings, R. J., Parinandi, N. L., Zaiman, A., Wang, L., Usatyuk, P. V., Garcia, J. G. N. and Natarajan, V. (2002) Phospholipase D activation by sphingosine-1-phosphate regulates interleukin-8 secretion in human bronchial epithelial cells. J. Biol. Chem. 277, 30227-30235
15. Wang, L., Cummings, R., Usatyuk, P., Morris, A., Irani, K. and Natarajan, V. (2002) Involvement of phospholipases D1 and D2 in sphingosine 1-phosphate-induced ERK (extracellular-signal-regulated kinase) activation and interleukin-8 secretion in human bronchial epithelial cells. Biochem. J. 367, 751-760
16. Fang, X., Yu, S., Bast, R. C., Liu, S., Xu, H., Hu, S., LaPushin, R., Claret, F. X., Aggarwal, B. B., Lu, Y. and Mills, G. B. (2004) Mechanisms for lysophosphatidic acid-induced cytokine production in ovarian cancer cells. J. Biol. Chem. 279, 9653-9661
17. Schwartz, B. M., Hong, G., Morrison, B. H., Wu, W., Baudhuin, L. M., Xiao, Y., Mok, S. C. and Xu, Y. (2001) Lysophospholipids increase interleukin-8 expression in ovarian cancer cells. Gynecol. Oncol. 81, 291-300
18. Palmetshofer, A., Robson, S. C. and Nehls, V. (1999) Lysophosphatidic acid activates nuclear factor kappa B and induces proinflammatory gene expression in endothelial cells. Thromb. Haemostasis 82, 1532-1537
19. Shida, D., Kitayama, J., Yamaguchi, H., Okaji, Y., Tsuno, N. H., Watanabe, T., Takuwa, Y. and Nagawa, H. (2003) Lysophosphatidic acid (LPA) enhances the metastatic potential of human colon carcinoma DLD1 cells through LPA1. Cancer Res. 63, 1706-1711
20. Baggiolini, M., Walz, A. and Kunkel, S. L. (1989) Neutrophil-activating peptide-1/interleukin 8, a novel cytokine that activates neutrophils. J. Clin. Invest. 84, 1045-1049
21. Huber, A. R., Kunkel, S. L., Todd, R. F. D. and Weiss, S. J. (1991) Regulation of transendothelial neutrophil migration by endogenous interleukin-8. Science 254, 99-102
22. Strieter, R. M. (2002) Interleukin-8: a very important chemokine of the human airway epithelium. Am. J. Physiol. Lung Cell Mol. Physiol. 283, L688-L689
23. Albelda, S. M., Smith, C. W. and Ward, P. A. (1994) Adhesion molecules and inflammatory injury. FASEB J. 8, 504-512
24. Brasier, A. R., Jamaluddin, M., Casola, A., Wang, D., Shen, Q. and Garofalo, R. P. (1998) A promoter recruitment mechanism for tumor necrosis factor-α-induced interleukin-8 transcripiton in type II pulmonary epithelial cells. J. Biol. Chem. 273, 3551-3561
25. Hooks, S. B., Ragan, S. P. and Lynch, K. R. (1998) Identification of a novel human phosphatidic acid phosphatase type 2 isoform. FEBS Lett. 427, 188-192
26. 2+-independent phosphatidic acid phosphatase. J. Biol. Chem. 272, 24572-24578
27. Roberts, R., Sciorra, V. A. and Morris, A. J. (1998) Human type 2 phosphatidic acid phosphohydrolases. Substrate specificity of the type 2a, 2b, and 2c enzymes and cell surface activity of the 2a isoform. J. Biol. Chem. 273, 22059-22067
28. Stunff, H. L., Peterson, C., Thornton, R., Milstien, S., Mandala, S. M. and Spiegel, S. (2002) Characterization of murine sphingosine-1-phosphate phosphohydrolase. J. Biol. Chem. 277, 8920-8927
29. Brindley, D. N., English, D., Pilquil, C., Buri, K. and Ling, Z. (2002) Lipid phosphate phosphatases regulate signal transduction through glycerolipids and sphingolipids. Biochim. Biophys. Acta 1582, 33-44
30. Ishikawa, T., Kai, M., Wada, I. and Kanoh, H. (2000) Cell surface activities of human type 2 phosphatidic acid phosphatase. J. Biochem. (Tokyo) 127, 645-651
31. Sciorra, V. A. and Morris, A. J. (2002) Roles of lipid phosphate phosphatases in regulation of cellular signaling. Biochim. Biophys. Acta 1582, 45-51
32. Alderton, F., Darroch, P., Sambi, B., McKie, A., Ahmed, I. S., Pyne, N. and Pyne, S. (2001) G-protein coupled receptor stimulation of p42/p44 mitogen activated protein kinase pathway is attenuated by lipid phosphatase 1, 1a, and 2 in HEK 293 cells. J. Biol. Chem. 276, 13452-13460
33. Pilquil, C., Singh, I., Zhang, Q., Ling, Z., Buri, K., Stromberg, L. M., Dewald, J. and Brindley, D. N. (2001) Lipid phosphate phosphatase-1 dephosphorylates exogenous lysophosphatidate and thereby attenuates its effects on cell signaling. Prostagladins Other Lipid Mediators 64, 83-92
34. Tanyi, J. L., Hasegawa, Y., Lapushin, R., Morris, A. J., Wolf, J. K., Berchuck, A., Lu, K., Smith, D. I., Kalli, K., Hartmann, L. C. et al. (2003) Role of decreased levels of lipid phosphate phosphatase-1 in accumulation of lysophosphatidic acid in ovarian cancer. Clin. Cancer Res. 9, 3534-3545
35. Tanyi, J. L., Morris, A. J., Wolf, J. K., Fang, X., Hasegawa, Y., Lapushin, R., Auersperg, N., Sigal, Y. J., Newman, R. A., Felix, E. A. et al. (2003) The human lipid phosphate phosphatase-3 decreases the growth, survival, and tumorigenesis of ovarian cancer cells: validation of the lysophosphatidic acid signaling cascade as a target for therapy in ovarian cancer. Cancer Res. 63, 1073-1082
36. Humtsoe, J. O., Feng, S., Thakker, G. D., Yang, J., Hong, J. and Wary, K. K. (2003) Regulation of cell-cell interactions by phosphatidic acid phosphatase 2b/VCIP. EMBO J. 22, 1539-1554
37. Escalante-Alcalde, D., Hernandez, L., Stunff, H. L., Maeda, R., Lee, H., Cheng, J. G., Sciorra, V. A., Daar, I., Spiegel, S., Morris, A. J. and Stewart, C. L. (2003) The lipid phosphatase LPP3 regulates extra-embryonic vasculogenesis and axis patterning. Development 130, 4623-4637
38. Bernacki, S. H., Nelson, A. L., Abdullah, L., Sheehan, J. K., Harris, A., Davis, C. W. and Randell, S. H. (1999) Mucin gene expression during differentiation of human airway epithelia in vitro. Muc4 and muc5b are strongly induced. Am. J. Respir. Cell Mol. Biol. 20, 595-604
39. Usatyuk, P. V., Fomin, V. P., Shi, S., Garcia, J. G., Schaphorst, K. and Natarajan, V. (2003) Role of Ca2+ in diperoxovanadate-induced cytoskeletal remodeling and endothelial cell barrier function. Am. J. Physiol. Lung Cell. Mol. Physiol. 285, L1006-L1017
40. Luquain, C., Singh, A., Wang, L., Natarajan, V. and Morris, A. J. (2003) Role of phospholipase D in agonist-stimulated lysophosphatidic acid synthesis by ovarian cancer cells. J. Lipid Res. 44, 1963-1975
41. Smyth, S. S., Sciorra, V. A., Sigal, Y. J., Pamulkar, Z., Wang, Z., Xu, Y., Prestwich, G. D. and Morris, A. J. (2003) Lipid phosphate phosphatases regulate lysophosphatidic acid production and signaling in platelets: studies using chemical inhibitors of lipid phosphate phosphatase activity. J. Biol. Chem. 278, 43214-43223
42. Jasinska, R., Zhang, Q. X., Pilquil, C. S., Singh, I., Xu, J., Dewald, J., Dillon, D. A., Berthiaume, L. G., Carman, G. M., Waggoner, D. W. and Brindley, D. N. (1999) Lipid phosphate phosphohydrolase-1 degrades exogenous glycerolipid and sphingolipid phosphate esters. Biochem. J. 340, 677-686
43. Cummings, R., Zhao, Y., Jacoby, D., Spannhake, E. W., Ohba, M., Garcia, J. G. N., Watkins, T., He, D., Saatian, B. and Natarajan, V. (2004) Protein kinase Cδ mediates lysophosphatidic acid-induced NF-κB activation and interleukin-8 secretion in human bronchial epithelial cells. J. Biol. Chem. 279, 41085-41094
44. Hasegawa, Y., Erickson, J. R., Goddard, G. J., Yu, S., Liu, S., Cheng, K. W., Eder, A., Bandoh, K., Aoki, J., Jarosz, R. et al. (2003) Identification of a phosphothionate analogue of lysophosphatidic acid (LPA) as a selective agonist of the LPA3 receptor. J. Biol. Chem. 278, 11962-11969
45. Qian, L., Xu, Y., Hasegawa, Y., Aoki, J., Mills, G. B. and Prestwich, G. D. (2003) Enantioselective responses to a phosphorothioate analogue of lysophosphatidic acid with LPA3 receptor-selective agonist activity. J. Med. Chem. 46, 5575-5578
46. Ogawa, C., Kihara, A., Gokoh, M. and Igarashi, Y. (2003) Identification and characterization of a novel human sphingosine-1-phosphate phosphohydrolase, hSPP2. J. Biol. Chem. 278, 1268-1272
47. Burnett, C. and Howard, K. (2003) Fly and mammalian lipid phosphate phosphatase isoforms differ in activity both in vitro and in vivo. EMBO Rep. 4, 793-799
48. Yue, J., Yokoyama, K., Balazs, L., Baker, D. L., Smalley, D., Pilquil, C., Brindley, D. N. and Tigyi, G. (2004) Mice with transgenic overexpression of lipid phosphate phosphatase-1 display multiple organotypic deficits without alteration in circulating lysophosphatidate level. Cell Sigalling 16, 385-399
49. Zhang, N., Sundberg, J. P. and Gridley, T. (2000) Mice mutant for Ppap2c, a homolog of the germ cell migration regulator Wunen, are viable and fertile. Genesis 27, 137-140
50. Ammit, A. J., Hastie, A. T., Edsall, L. C., Hoffman, R. K., Amrani, Y., Krymskaya, V. P., Kane, S. A., Peters, S. P., Penn, R. B., Spiegel, S. and Panettieri, R. A. (2001) Sphingosine 1-phosphate modulates human airway smooth muscle cell functions that promote inflammation and airway remodeling in asthma. FASEB J. 15, 1212-1214
51. Georas, S., Liu, M., Cummings, R., Chen, R., Morris, A., Berdyshev, E. and Natarajan, V. (2004) Lysophosphatidic acid (LPA) levels and LPA-receptor signaling in airway inflammation and asthma. Am. J. Respir. Crit. Care Med. 169, A569