Lysophosphatidic acid stimulates ovarian cancer cell migration via a Ras-MEK kinase 1 pathway

Cancer Research

Volumn 64, Issue 12, 2004, Pages 4209-4217

  Bian, Dafang ^a   Su, Shibing ^a   Mahanivong, Chitladda ^a   Cheng, Robert K ^a   Han, Qiwei ^a   Pan, Zhixing K ^b   Sun, Peiqing ^a   Huang, Shuang ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b MEDICAL COLLEGE OF OHIO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENIC FACTOR; FOCAL ADHESION KINASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LYSOPHOSPHATIDIC ACID; MITOGEN ACTIVATED PROTEIN KINASE KINASE; PERTUSSIS TOXIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEINASE; RAF PROTEIN; RAL PROTEIN; RAS PROTEIN;

ARTICLE; ASCITES; CANCER INVASION; CELL MIGRATION; CHEMOKINESIS; CHEMOTAXIS; CONTROLLED STUDY; ENZYME ACTIVITY; EXPERIMENTAL MODEL; HUMAN; HUMAN CELL; METASTASIS; ONCOGENE H RAS; OVARY CANCER; PLASMA; PRIORITY JOURNAL; PROTEIN EXPRESSION;

CELL MOVEMENT; FEMALE; FOCAL ADHESION KINASE 1; FOCAL ADHESION PROTEIN-TYROSINE KINASES; FOCAL ADHESIONS; G1 PHASE; HUMANS; LYSOPHOSPHOLIPIDS; MAP KINASE KINASE KINASE 1; MAP KINASE KINASE KINASES; MAP KINASE SIGNALING SYSTEM; OVARIAN NEOPLASMS; PROTEIN-TYROSINE KINASES; RAS PROTEINS; STIMULATION, CHEMICAL;

EID: 3042523481     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-04-0060     Document Type: Article

References (80)

1. Moolenaar WH. Bioactive lysophospholipids and their G protein-coupled receptors. Exp Cell Res 1999;253:230-8.
2. Fang X, Schummer M, Mao M, et al. Lysophosphatidic acid is a bioactive mediator in ovarian cancer. Biochim Biophys Acta 2002;1582:257-64.
3. Daaka Y. Mitogenic action of LPA in prostate. Biochim Biophys Acta 2002;1582:265-9.
4. Toews ML, Ediger TL, Romberger DJ, Rennard SI. Lysophosphatidic acid in airway function and disease. Biochim Biophys Acta 2002;1582:240-50.
5. Gräler MH, Goetzl EJ. Lysophospholipids and their G protein-coupled receptors in inflammation and immunity. Biochim Biophys Acta 2002;1582:168-74.
6. Contos JJA, Ishii I, Chun J. Lysophosphatidic acid receptors. Mol Pharmacol 2000; 58:1188-96.
7. Shen Z, Wu M, Elson P, et al. Fatty acid composition of lysophosphatidic acid and lysophosphatidylinositol in plasma from patients with ovarian cancer and other gynecological diseases. Gynecol Oncol 2001;83:25-30.
8. Xu Y, Shen Z, Wiper DW, et al. Lysophosphatidic acid as a potential biomarker for ovarian and other gynecologic cancers. J Am Med Assoc 1998;280:719-23.
9. Westerman AM, Havik E, Postma FR, et al. Malignant effusions contain lysophosphatidic acid (LPA)-like activity. Ann Oncol 1998;9:437-42.
10. Eder AM, Sasagawa T, Mao M, Aoki J, Mills GB. Constitutive and lysophosphatidic acid (LPA)-induced LPA production: role of phosholipase D and phospholipase A2. Clin Cancer Res 2000;6:2482-91.
11. Shen Z, Belinson J, Morton RE, Xu Y, Xu Y. Phorbol 12-myristate 13-acetate stimulates lysophosphatidic acid secretion from ovarian and cervical cancer cells but not from breast or leukemia cells. Gynecol Oncol 1998;71:364-8.
12. Hu Y-L, Tee M-K, Goetzl EJ, Auersperg N, Mills GB, Ferrara N. Lysophosphatidic acid induction of vascular endothelial growth factor expression in human ovarian cancer cells. J Natl Cancer Inst (Bethesda) 2003;93:762-8.
13. Fujita T, Miyamoto S, Onoyama I, Sonoda K, Mekada E, Nakano H. Expression of lysophosphatidic acid receptors and vascular endothelial growth factor mediating lysophosphatidic acid in the development of human ovarian cancer. Cancer Lett 2003;192:161-9.
14. Goetzl EJ, Dolezalova H, Kong Y, et al. Distinctive expression and functions of the type 4 endothelial differentiation gene-encoded G protein-coupled receptor for lysophosphatidic acid in ovarian cancer. Cancer Res 1999;59:5370-5.
15. Fang X, Gaudette D, Furui T, et al. Lysophospholipid growth factors in the initiation, progression, metastases, and management of ovarian cancer. Ann NY Acad Sci 2000;905:188-208.
16. Xu Y, Fang XJ, Casey G, Mills GB. Lysophospholipids activate ovarian and breast cancer cells. Biochem J 1995;309:933-40.
17. Pustilnik TB, Estrella V, Wiener JR, et al. Lysophosphatidic acid induces urokinase secretion by ovarian cancer cells. Clin Cancer Res 1999;5:3704-10.
18. Fishman DA, Liu Y, Ellerbroek SM, Stack S. Lysophosphatidic acid promotes matrix metalloproteinase (MMP) activation and MMP-dependent invasion in ovarian cancer cells. Cancer Res 2001;61:3194-9.
19. Mukai M, Imamura F, Ayaki M, et al. Inhibition of tumor invasion and metastasis by a novel lysophosphatidic acid (Cyclic LPA). Int J Cancer 1999;81:918-22.
20. Tanyi JL, Morris AJ, Wolf JK, et al. 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 2003;63:1073-82.
21. Downward J. Targeting Ras signaling pathways in cancer therapy. Nature Rev Cancer 2003;3:11-22.
22. Silvius JR. Mechanisms of Ras protein targeting in mammalian cells. J Membr Biol 2002;190:83-92.
23. Macaluso M, Russo G, Cinti C, Bazan V, Gebbia N, Russo A. Ras family genes: an interesting link between cell cycle and cancer. J Cell Physiol 2002;192:125-30.
24. Lucus L, Penalva V, Ramirez de Molina A, del Peso L, Lacal JC. Modulation of phospholipase D by Ras proteins mediated by its effectors Ral-GDS, PI3K and Raf-1. Int J Oncol 2002;21:477-85.
25. White MA, Vale T, Camonis JH, Schaefer E, Wigler MH. A role for the Ral guanine nucleotide dissociation stimulator in mediating Ras-induced transformation. J Biol Chem 1996;271:16439-42.
26. Ramirez de Molina A, Penalva V, Lucas L, Lacal JC. Regulation of choline kinase activity by Ras proteins involves Ral-GDS and PI3K. Oncogene 2002;21:937-46.
27. White MA, Nicolette C, Minden A, et al. Multiple Ras functions can contribute to mammalian cell transformation. Cell 1995;80:533-41.
28. Joneson T, White MA, Wigler MH, Bar-Sagi D. Stimulation of membrane ruffling and MAP kinase activation by distinct effectors of RAS. Science (Wash. DC) 1996;271:810-2.
29. Russell M, Lange-Carter CA, Johnson GL. Direct interaction between Ras and kinase domain of mitogen-activated protein kinase kinase kinase (MEKK1). J Biol Chem 1995;270:11757-60.
30. Lange-Carter CA, Johnson GL. Ras-dependent growth factor regulation of MEK kinase in PC12 cells. Science (Wash. DC) 1994;265:1458-61.
31. Schlesinger TK, Fanger GR, Yujiri T, Johnson GL. The TAO of MEKK. Front Biosci 1998;3:1181-6.
32. 2-terminal kinase regulation but does not cause a measurable defect in NF-kappaB activation. J Biol Chem 2003;274:12605-10.
33. Minden A, Lin A, McMahon M, et al. Differential activation of ERK and JNK mitogen-activated protein kinases by Raf-1 and MEKK. Science (Wash. DC) 2004; 266:1719-23.
34. Xia Y, Wu Z, Su B, Muray B, Karin M. JNKK1 organizes a MAP kinase module through specific and sequential interactions with upstream and downstream components mediated by its amino-terminal extension. Genes Dev 1998;12:3369-81.
35. Xu S, Robbins DJ, Christerson LB, English JM, Vanderbilt CA, Cobb MH. Cloning of rat MEK kinase 1 cDNA reveals an endogenous membrane-associated 195-kDa protein with a large regulatory domain. Proc Natl Acad Sci USA 1996;93:5291-5.
36. Lee FS, Hagler J, Chen ZJ, Maniatis T. Activation of the IkappaBalpha kinase complex by MEKK1, a kinase of the JNK pathway. Cell 1997;88:213-22.
37. Sánchez-Pérez I, Benitah SA, Martfnez-Gomariz M, Lacal JC, Perona R. Cell stress and MEKK1-mediated c-Jun activation modulate NFkappaB activity and cell viability. Mol Cell 2002;13:2933-45.
38. Hirano T, Shino Y, Saito T, et al. Dominant negative MEKK1 inhibits survival of pancreatic cancer cells. Oncogene 2002;21:5923-8.
39. Xia Y, Makris C, Su B, et al. MEK kinase 1 is critically required for c-Jun N-terminal kinase activation by proinflammatory stimuli and growth factor-induced cell migration. Proc Natl Acad Sci USA 2000;97:5243-8.
40. 2-terminal kinase regulation but does not cause a measurable defect in NF-kappaB activation. Proc Natl Acad Sci USA 2003;97:7271-7.
41. Zhang L, Wang W, Hayashi Y, et al. A role for MEK kinase 1 in TGF-beta/activin-induced epithelium movement and embryonic eyelid closure. EMBO J 2003;22:4443-54.
42. Fanger GR, Lassignal Johnson N, Johnson GL. MEK kinases are regulated by EGF and selectively interact with Rac/Cdc42. EMBO J 1997;16:4961-72.
43. Christerson LB, Vanderbilt CA, Cobb MH. MEKKI interacts with alpha-actinin and localizes to stress fibers and focal adhesions. Cell Motil Cytoskeleton 1999;43:186-98.
44. Yujiri T, Nawata R, Takahashi T, et al. MEK kinase 1 interacts with focal adhesion kinase and regulates insulin receptor substrate-1 expression. J Biol Chem 2003;278:3846-51.
45. Christerson LB, Gallagher E, Vanderbilt CA, et al. p115 Rho GTPase activating protein interacts with MEKK1. J Cell Physiol 2002;192:200-8.
46. FAK, a structurally distinctive protein-tyrosine kinase associated with focal adhesions. Proc Natl Acad Sci USA 1992;89:5192-6.
47. Ilic D, Furuta Y, Kanazawa S, et al. Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice. Nature (Lond.) 1995; 377:539-44.
48. Ren XD, Kiosses WB, Sieg DJ, Otey CA, Schlaepfer DD, Schwartz MA. Focal adhesion kinase suppresses Rho activity to promote focal adhesion turnover. J Cell Sci 2003;113:3673-8.
49. Sieg DJ, Hauck CR, Ilic D, et al. FAK integrates growth-factor and integrin signals to promote cell migration. Nat Cell Biol 2000;2:249-56.
50. Han DC, Guan JL. Association of focal adhesion kinase with Grb7 and its role in cell migration. J Biol Chem 1999;274:24425-30.
51. Manes S, Mira E, Gomez-Mouton C, Zhao ZJ, Lacalle RA, Martinez AC. Concerted activity of tyrosine phosphatase SHP-2 and focal adhesion kinase in regulation of cell motility. Mol Cell Biol 1999;19:3125-35.
52. Cas as a mediator of focal adhesion kinase-promoted cell migration. J Cell Biol 1998;140:211-21.
53. Richardson A, Malik RK, Hildebrand JD, Parsons JT. Inhibition of cell spreading by expression of the C-terminal domain of focal adhesion kinase (FAK) is rescued by coexpression of Src or catalytically inactive FAK: a role for paxillin tyrosine phosphorylation. Mol Cell Biol 1997;17:6906-14.
54. Hauck CR, Hsia DA, Ilic D, Schlaepfer DD. v-Src SH3-enhanced interaction with focal adhesion kinase at beta I integrin-containing invadopodia promotes cell invasion. J Biol Chem 2002;12:12487-90.
55. Feniger-Barish R, Yron I, Meshel T, Matityahu E, Ben-Baruch A. IL-8-induced migratory responses through CXCR1 and CXRC2: association with phosphorylation and cellular redistribution of focal adhesion kinase. Biochemistry 2003;42:2874-86.
56. Huang S, Jiang Y, Li Z, et al. Apoptosis signaling pathway in T cells is composed of ICE/Ced-3 family proteases and MAP kinase kinase 6b. Immunity 1997;6:739-49.
57. Huang S, Stupack DG, Mathias P, Wang Y, Nemerow G. Growth arrest of Epstein-Barr virus immortalized B lymphocytes by adenovirus-delivered ribozymes. Proc Natl Acad Sci USA 1997;94:8156-61.
58. Lin AW, Barradas M, Stone JC, Van Aelst L, Serrano M, Lowe SW. Premature senescence involving p53 and p16 is activated in response to constitutive MEK/MAPK mitogenic signaling. Genes Dev 1998;12:3008-19.
59. Sun P, Dong P, Dai K, Hannon GJ, Beach D. p53-independent role of MDM2 in TGF-beta1 resistance. Science (Wash. DC) 1998;282:2270-2.
60. Kranenburg O, Moolenaar WH. Ras-MAP kinase signaling by lysophosphatidic acid and other G protein-coupled receptor agonists. Oncogene 2001;20:1540-6.
61. NagDas SK, Winfrey VP, Olson GE. Identification of ras and its downstream signaling elements and their potential role in hamster sperm motility. Biol Reprod 2002;67:1058-66.
62. Oxford G, Theodorescu D. Ras superfamily monomeric G proteins in carcinoma cell motility. Cancer Lett 2003;189:117-28.
63. Janda E, Lehmann K, Killisch I, et al. Ras and TGF-beta cooperatively regulate epithelial cell plasticity and metastasis: dissection of Ras signaling pathways. J Cell Biol 2002;156:219-313.
64. Ridley AJ, Comoglio PM, Hall A. Regulation of scatter factor/hepatocyte growth factor responses by Ras, Rac, and Rho in MDCK cells. Mol Cell Biol 1995;15:1110-22.
65. Hall A, Nobes CD. Rho GTPases: molecular switches that control the organization and dynamics of the actin cytoskeleton. Philos Trans R Soc Lond 2000;355:965-70.
66. Kikuchi A, Demo SD, Ye ZH, Chen YW, Williams LT. ralGDS family members interact with the effector loop of ras p21. Mol Cell Biol 1994;14:7483-91.
67. Tangkijvanich P, Melton AC, Chitapanarux T, Han J, Yee HF Jr. Platelet-derived growth factor-BB and lysophosphatidic acid distinctly regulate hepatic myofibroblast migration through focal adhesion kinase. Exp Cell Res 2002;281:140-7.
68. Sawada K, Morishige K, Tahara M, et al. Lysophosphatidic acid induces focal adhesion assembly through Rho/Rho-associated kinase pathway in human ovarian cancer cells. Gynecol Oncol 2002;87:252-9.
69. Mukai M, Iwasaki T, Tatsuta M, et al. Cyclic phosphatidic acid inhibits RhoA-mediated autophosphorylation on FAK at Tyr-397 and subsequent tumor-cell invasion. Int J Oncol 2003;22:1247-56.
70. Hines OJ, Ryder N, Chu J, McFadden D. Lysophosphatidic acid stimulates intestinal restitution via cytoskeletal activation and remodeling. J Surg Res 2000;92:23-8.
71. Goetzl EJ, Lee H, Dolezalova H, et al. Mechanisms of lysolipid phosphate effects on cellular survival and proliferation. Ann NY Acad Sci 2000;905:177-87.
72. ras by G protein-coupled receptor agonists in fibroblasts. Proc Natl Acad Sci USA 1993;90:1257-61.
73. Della Rocca GJ, van Biesen T, Daaka Y, Luttrell DK, Luttrell LM, Lefkowitz RJ. Ras-dependent mitogen-activated protein kinase activation by G protein-coupled receptors. J Biol Chem 1997;272:19125-32.
74. Luttrell LM, Hawes BE, van Biesen T, Luttrell DK, Lansing TJ, Lefkowitz RJ. Role of c-Src tyrosine kinase in G protein-coupled receptor-and Gbetagamma subunit-mediated activation of mitogen-activated protein. J Biol Chem 1996;271:19443-50.
75. Hordijk PL, Verlaan I, van Corven EJ, Moolenaar WH. Protein tyrosine phosphorylation induced by lysophosphatidic acid in Rat-1 fibroblasts. J Biol Chem 1994;269:645-51.
76. Rocca GJD, Maudsley S, Daaka Y, Lefkowitz RJ, Luttrell LM. Pleiotropic coupling of G protein-coupled receptors to the mitogen-activated protein kinase cascade. J Biol Chem 1999;274:13978-84.
77. Yart A, Roche S, Wetzker R, et al. A function for phosphoinositide 3-kinase beta lipid products in coupling beta gamma to ras activation in response to lysophosphatidic acid. J Biol Chem 2002;277:21167-78.
78. van Leeuwen FN, Olivo C, Grivell S, Giepmans BNG, Collard JG, Moolenaar WH. Rac activation by lysophosphatidic acid LPA receptors through the guanine nucleotide exchange factor Tiam1. J Biol Chem 2003;278:400-6.
79. Stähle M, Veit C, Bachfischer U, et al. Mechanisms in LPA-induced tumor cell migration: critical role of phosphorylated ERK. J Cell Sci 2003;116:3835-46.
80. Avdi NJ, Winston BW, Russel M, Young SK, Johnson GL, Worthen GS. Activation of MEKK by formyl-methionyl-leucyl-phenylalanine in human neutrophils. J Biol Chem 1996;271:33598-606.