Lysophosphatidic acid and sphingosine-1-phosphate promote morphogenesis and block invasion of prostate cancer cells in three-dimensional organotypic models

Oncogene

Volumn 31, Issue 16, 2012, Pages 2075-2089

  Harma V ^a   Knuuttila, M ^b   Virtanen, J ^a,b   Mirtti, T ^c,d   Kohonen, P ^b   Kovanen, P ^d   Happonen, A ^e   Kaewphan, S ^b   Ahonen, I ^b   Kallioniemi, O ^c   Grafstrom R ^a,f   Lotjonen J ^a   Nees, M ^a  

^a VTT TECHNICAL RESEARCH CENTRE OF FINLAND   (Finland)

^b UNIVERSITY OF TURKU   (Finland)

^c UNIVERSITY OF HELSINKI   (Finland)

^d HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

^e TAMPERE UNIVERSITY OF TECHNOLOGY   (Finland)

^f KAROLINSKA INSTITUTE   (Sweden)

Author keywords

bioactive lipids; epithelial plasticity; G protein coupled receptors; lysophosphatidic acid; prostate cancer; sphingosine 1 phosphate

Indexed keywords

ADENYLATE CYCLASE; G PROTEIN COUPLED RECEPTOR; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; LYSOPHOSPHATIDIC ACID; LYSOPHOSPHATIDIC ACID RECEPTOR; LYSOPHOSPHATIDIC ACID RECEPTOR 1; RAC1 PROTEIN; RHO KINASE; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; ROCK1 PROTEIN; ROCK2 PROTEIN; SMALL INTERFERING RNA; SPHINGOSINE 1 PHOSPHATE; TRANSCRIPTOME; UNCLASSIFIED DRUG;

ACINAR CELL; ARTICLE; CANCER CELL CULTURE; CANCER INHIBITION; CANCER INVASION; CELL CYCLE ARREST; CELL MATURATION; CELL STRUCTURE; CELL TRANSFORMATION; CONTROLLED STUDY; ENZYME INHIBITION; MORPHOGENESIS; PRIORITY JOURNAL; PROSTATE EPITHELIUM; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION;

CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELL MOVEMENT; EPITHELIUM; GTP-BINDING PROTEINS; HUMANS; LYSOPHOSPHOLIPIDS; MALE; PROSTATIC NEOPLASMS; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SPHINGOSINE; TUMOR CELLS, CULTURED;

EID: 84859910759     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2011.396     Document Type: Article

References (83)

1. Akbar H, Cancelas J, Williams DA, Zheng J, Zheng Y. (2006). Rational design and applications of a rac GTPase-specific small molecule inhibitor. Methods Enzymol 406: 554-565. (Pubitemid 43207468)
2. Aziziyeh AI, Li TT, Pape C, Pampillo M, Chidiac P, Possmayer F et al. (2009). Dual regulation of lysophosphatidic acid (LPA1) receptor signalling by ral and GRK. Cell Signal 21: 1207-1217.
3. Bagga S, Price KS, Lin DA, Friend DS, Austen KF, Boyce JA. (2004). Lysophosphatidic acid accelerates the development of human mast cells. Blood 104: 4080-4087. (Pubitemid 39620159)
4. Brekhman V, Neufeld G. (2009). A novel asymmetric 3D in-vitro assay for the study of tumor cell invasion. BMC Cancer 9: 415.
5. Brizuela L, Dayon A, Doumerc N, Ader I, Golzio M, Izard JC et al. (2010). The sphingosine kinase-1 survival pathway is a molecular target for the tumor-suppressive tea and wine polyphenols in prostate cancer. FASEB J 24: 3882-3894.
6. Chu JH, Yu S, Hayward SW, Chan FL. (2009). Development of a three-dimensional culture model of prostatic epithelial cells and its use for the study of epithelial-mesenchymal transition and inhibition of PI3K pathway in prostate cancer. Prostate 69: 428-442.
7. Daaka Y. (2002). Mitogenic action of LPA in prostate. Biochim Biophys Acta 1582: 265-269.
8. Deng W, Balazs L, Wang DA, Van Middlesworth L, Tigyi G, Johnson LR. (2002). Lysophosphatidic acid protects and rescues intestinal epithelial cells from radiation- and chemotherapy-induced apoptosis. Gastroenterology 123: 206-216. (Pubitemid 34747541)
9. Devine KM, Smicun Y, Hope JM, Fishman DA. (2008). S1P induced changes in epithelial ovarian cancer proteolysis, invasion, and attachment are mediated by gi and rac. Gynecol Oncol 110: 237-245.
10. Eichholtz T, Jalink K, Fahrenfort I, Moolenaar WH. (1993). The bioactive phospholipid lysophosphatidic acid is released from activated platelets. Biochem J 291(Pt 3): 677-680. (Pubitemid 23148436)
11. Eisen MB, Spellman PT, Brown PO, Botstein D. (1998). Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci U S A 95: 14863-14868. (Pubitemid 29003722)
12. Evelyn CR, Bell JL, Ryu JG, Wade SM, Kocab A, Harzdorf NL et al. (2010). Design, synthesis and prostate cancer cell-based studies of analogs of the Rho/MKL1 transcriptional pathway inhibitor, CCG-1423. Bioorg Med Chem Lett 20: 665-672.
13. Evelyn CR, Wade SM, Wang Q, Wu M, Iniguez-Lluhi JA, Merajver SD et al. (2007). CCG-1423: A small-molecule inhibitor of RhoA transcriptional signaling. Mol Cancer Ther 6: 2249-2260. (Pubitemid 47294753)
14. Fang X, Schummer M, Mao M, Yu S, Tabassam FH, Swaby R et al. (2002). Lysophosphatidic acid is a bioactive mediator in ovarian cancer. Biochim Biophys Acta 1582: 257-264. (Pubitemid 34634137)
15. Fishman DA, Liu Y, Ellerbroek SM, Stack MS. (2001). Lysophosphatidic acid promotes matrix metalloproteinase (MMP) activation and MMP-dependent invasion in ovarian cancer cells. Cancer Res 61: 3194-3199. (Pubitemid 32691975)
16. Fourcade O, Simon MF, Viode C, Rugani N, Leballe F, Ragab A et al. (1995). Secretory phospholipase A2 generates the novel lipid mediator lysophosphatidic acid in membrane microvesicles shed from activated cells. Cell 80: 919-927.
17. Fukami K, Takenawa T. (1992). Phosphatidic acid that accumulates in platelet-derived growth factor-stimulated Balb/c 3T3 cells is a potential mitogenic signal. J Biol Chem 267: 10988-10993.
18. Gibbs TC, Rubio MV, Zhang Z, Xie Y, Kipp KR, Meier KE. (2009). Signal transduction responses to lysophosphatidic acid and sphingosine 1-phosphate in human prostate cancer cells. Prostate 69: 1493-1506.
19. Gobeil F, Bernier SG, Vazquez-Tello A, Brault S, Beauchamp MH, Quiniou C et al. (2003). Modulation of pro-inflammatory gene expression by nuclear lysophosphatidic acid receptor type-1. J Biol Chem 278: 38875-38883. (Pubitemid 37221787)
20. Goetzl EJ, Dolezalova H, Kong Y, Zeng L. (1999a). Dual mechanisms for lysophospholipid induction of proliferation of human breast carcinoma cells. Cancer Res 59: 4732-4737. (Pubitemid 29428984)
21. Goetzl EJ, Kong Y, Mei B. (1999b). Lysophosphatidic acid and sphingosine 1-phosphate protection of T cells from apoptosis in association with suppression of bax. J Immunol 162: 2049-2056. (Pubitemid 29288824)
22. Groves-Kirkby N. (2010). Genomic profiling of prostate cancer. Nat Rev Urol 7: 420.
23. Guo R, Kasbohm EA, Arora P, Sample CJ, Baban B, Sud N et al. (2006). Expression and function of lysophosphatidic acid LPA1 receptor in prostate cancer cells. Endocrinology 147: 4883-4892. (Pubitemid 44402195)
24. Hao F, Tan M, Xu X, Han J, Miller DD, Tigyi G et al. (2007). Lysophosphatidic acid induces prostate cancer PC3 cell migration via activation of LPA(1), p42 and p38alpha. Biochim Biophys Acta 1771: 883-892. (Pubitemid 46891301)
25. Harma V, Virtanen J, Makela R, Happonen A, Mpindi JP, Knuuttila M et al. (2010). A comprehensive panel of three-dimensional models for studies of prostate cancer growth, invasion and drug responses. PLoS One 5: e10431.
26. Harper K, Arsenault D, Boulay-Jean S, Lauzier A, Lucien F, Dubois CM. (2010). Autotaxin promotes cancer invasion via the lysophosphatidic acid receptor 4: Participation of the cyclic AMP/EPAC/Rac1 signaling pathway in invadopodia formation. Cancer Res 70: 4634-4643.
27. Hasegawa Y, Murph M, Yu S, Tigyi G, Mills GB. (2008). Lysophosphatidic acid (LPA)-induced vasodilator-stimulated phosphoprotein mediates lamellipodia formation to initiate motility in PC-3 prostate cancer cells. Mol Oncol 2: 54-69.
28. Hong G, Baudhuin LM, Xu Y. (1999). Sphingosine-1-phosphate modulates growth and adhesion of ovarian cancer cells. FEBS Lett 460: 513-518. (Pubitemid 29518430)
29. Hope JM, Wang FQ, Whyte JS, Ariztia EV, Abdalla W, Long K et al. (2009). LPA receptor 2 mediates LPA-induced endometrial cancer invasion. Gynecol Oncol 112: 215-223.
30. Hwang YS, Hodge JC, Sivapurapu N, Lindholm PF. (2006). Lysophosphatidic acid stimulates PC-3 prostate cancer cell matrigel invasion through activation of RhoA and NF-kappaB activity. Mol Carcinog 45: 518-529.
31. Inman JL, Bissell MJ. (2010). Apical polarity in three-dimensional culture systems: Where to now? J Biol 9: 2.
32. Jeong KJ, Park SY, Seo JH, Lee KB, Choi WS, Han JW et al. (2008). Lysophosphatidic acid receptor 2 and Gi/Src pathway mediate cell motility through cyclooxygenase 2 expression in CAOV-3 ovarian cancer cells. Exp Mol Med 40: 607-616.
33. Kalluri R, Weinberg RA. (2009). The basics of epithelial-mesenchymal transition. J Clin Invest 119: 1420-1428.
34. Kawamori T, Osta W, Johnson KR, Pettus BJ, Bielawski J, Tanaka T et al. (2006). Sphingosine kinase 1 is up-regulated in colon carcinogenesis. FASEB J 20: 386-388. (Pubitemid 46671180)
35. Kim EK, Yun SJ, Do KH, Kim MS, Cho M, Suh DS et al. (2008). Lysophosphatidic acid induces cell migration through the selective activation of Akt1. Exp Mol Med 40: 445-452.
36. Kim J, Adam RM, Freeman MR. (2002). Activation of the erk mitogen-activated protein kinase pathway stimulates neuroendocrine differentiation in LNCaP cells independently of cell cycle withdrawal and STAT3 phosphorylation. Cancer Res 62: 1549-1554. (Pubitemid 34407821)
37. Lee MJ, Thangada S, Liu CH, Thompson BD, Hla T. (1998a). Lysophosphatidic acid stimulates the G-protein-coupled receptor EDG-1 as a low affinity agonist. J Biol Chem 273: 22105-22112. (Pubitemid 28405394)
38. Lee MJ, Van Brocklyn JR, Thangada S, Liu CH, Hand AR, Menzeleev R et al. (1998b). Sphingosine-1-phosphate as a ligand for the G protein-coupled receptor EDG-1. Science 279: 1552-1555. (Pubitemid 28217081)
39. Li H, Wang D, Zhang H, Kirmani K, Zhao Z, Steinmetz R et al. (2009a). 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.
40. Li S, Huang S, Peng SB. (2005). Overexpression of G protein-coupled receptors in cancer cells: Involvement in tumor progression. Int J Oncol 27: 1329-1339.
41. Li TT, Alemayehu M, Aziziyeh AI, Pape C, Pampillo M, Postovit LM et al. (2009b). Beta-arrestin/Ral signaling regulates lysophosphatidic acid-mediated migration and invasion of human breast tumor cells. Mol Cancer Res 7: 1064-1077.
42. Liu S, Murph M, Panupinthu N, Mills GB. (2009a). ATX-LPA receptor axis in inflammation and cancer. Cell Cycle 8: 3695-3701.
43. Liu S, Umezu-Goto M, Murph M, Lu Y, Liu W, Zhang F et al. (2009b). Expression of autotaxin and lysophosphatidic acid receptors increases mammary tumorigenesis, invasion, and metastases. Cancer Cell 15: 539-550.
44. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY et al. (2008). The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 133: 704-715. (Pubitemid 351636299)
45. McIntyre TM, Pontsler AV, Silva AR, St Hilaire A, Xu Y, Hinshaw JC et al. (2003). Identification of an intracellular receptor for lysophosphatidic acid (LPA): LPA is a transcellular PPARgamma agonist. Proc Natl Acad Sci U S A 100: 131-136. (Pubitemid 36078041)
46. Meyer zu Heringdorf D, Lass H, Alemany R, Laser KT, Neumann E, Zhang C et al. (1998). Sphingosine kinase-mediated Ca2+ signalling by G-protein-coupled receptors. EMBO J 17: 2830-2837.
47. Mootha VK, Lindgren CM, Eriksson KF, Subramanian A, Sihag S, Lehar J et al. (2003). PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat Genet 34: 267-273. (Pubitemid 36792858)
48. Morin P, Wickman G, Munro J, Inman GJ, Olson MF. (2011). Differing contributions of LIMK and ROCK to TGFbeta-induced transcription, motility and invasion. Eur J Cell Biol 90: 13-25.
49. Nava VE, Hobson JP, Murthy S, Milstien S, Spiegel S. (2002). Sphingosine kinase type 1 promotes estrogen-dependent tumorigenesis of breast cancer MCF-7 cells. Exp Cell Res 281: 115-127. (Pubitemid 35373788)
50. Nouh MA, Wu XX, Okazoe H, Tsunemori H, Haba R, Abou-Zeid AM et al. (2009). Expression of autotaxin and acylglycerol kinase in prostate cancer: Association with cancer development and progression. Cancer Sci 100: 1631-1638.
51. Olivera A, Spiegel S. (1993). Sphingosine-1-phosphate as second messenger in cell proliferation induced by PDGF and FCS mitogens. Nature 365: 557-560. (Pubitemid 23317779)
52. Olson EN, Nordheim A. (2010). Linking actin dynamics and gene transcription to drive cellular motile functions. Nat Rev Mol Cell Biol 11: 353-365.
53. Onesto C, Shutes A, Picard V, Schweighoffer F, Der CJ. (2008). Characterization of EHT 1864, a novel small molecule inhibitor of rac family small GTPases. Methods Enzymol 439: 111-129.
54. Pchejetski D, Bohler T, Brizuela L, Sauer L, Doumerc N, Golzio M et al. (2010). FTY720 (fingolimod) sensitizes prostate cancer cells to radiotherapy by inhibition of sphingosine kinase-1. Cancer Res 70: 8651-8661.
55. Pchejetski D, Doumerc N, Golzio M, Naymark M, Teissie J, Kohama T et al. (2008). Chemosensitizing effects of sphingosine kinase-1 inhibition in prostate cancer cell and animal models. Mol Cancer Ther 7: 1836-1845.
56. Pineiro R, Maffucci T, Falasca M. (2010). The putative cannabinoid receptor GPR55 defines a novel autocrine loop in cancer cell proliferation. Oncogene 30: 142-152.
57. Reuter JA, Ortiz-Urda S, Kretz M, Garcia J, Scholl FA, Pasmooij AM et al. (2009). Modeling inducible human tissue neoplasia identifies an extracellular matrix interaction network involved in cancer progression. Cancer Cell 15: 477-488.
58. Ridky TW, Chow JM, Wong DJ, Khavari PA. (2010). Invasive three-dimensional organotypic neoplasia from multiple normal human epithelia. Nat Med 16: 1450-1455.
59. Sawada K, Morishige K, Tahara M, Ikebuchi Y, Kawagishi R, Tasaka K et al. (2002). Lysophosphatidic acid induces focal adhesion assembly through Rho/Rho-associated kinase pathway in human ovarian cancer cells. Gynecol Oncol 87: 252-259. (Pubitemid 36034644)
60. Sekine Y, Suzuki K, Remaley AT. (2010). HDL and sphingosine-1-phosphate activate stat3 in prostate cancer DU145 cells via ERK1/2 and S1P receptors, and promote cell migration and invasion. Prostate 71: 690-699.
61. Seo JH, Jeong KJ, Oh WJ, Sul HJ, Sohn JS, Kim YK et al. (2010). Lysophosphatidic acid induces STAT3 phosphorylation and ovarian cancer cell motility: Their inhibition by curcumin. Cancer Lett 288: 50-56.
62. Sequeira L, Dubyk CW, Riesenberger TA, Cooper CR, van Golen KL. (2008). Rho GTPases in PC-3 prostate cancer cell morphology, invasion and tumor cell diapedesis. Clin Exp Metastasis 25: 569-579.
63. Shida D, Kitayama J, Yamaguchi H, Okaji Y, Tsuno NH, Watanabe T et al. (2003). Lysophosphatidic acid (LPA) enhances the metastatic potential of human colon carcinoma DLD1 cells through LPA1. Cancer Res 63: 1706-1711. (Pubitemid 36373664)
64. Shida D, Watanabe T, Aoki J, Hama K, Kitayama J, Sonoda H et al. (2004). Aberrant expression of lysophosphatidic acid (LPA) receptors in human colorectal cancer. Lab Invest 84: 1352-1362. (Pubitemid 40063699)
65. Shutes A, Onesto C, Picard V, Leblond B, Schweighoffer F, Der CJ. (2007). Specificity and mechanism of action of EHT 1864, a novel small molecule inhibitor of rac family small GTPases. J Biol Chem 282: 35666-35678. (Pubitemid 350277149)
66. Smicun Y, Gil O, Devine K, Fishman DA. (2007). S1P and LPA have an attachment-dependent regulatory effect on invasion of epithelial ovarian cancer cells. Gynecol Oncol 107: 298-309. (Pubitemid 47575728)
67. Snider AJ, Orr Gandy KA, Obeid LM. (2010a). Sphingosine kinase: Role in regulation of bioactive sphingolipid mediators in inflammation. Biochimie 92: 707-715.
68. Snider AJ, Zhang Z, Xie Y, Meier KE. (2010b). Epidermal growth factor increases lysophosphatidic acid production in human ovarian cancer cells: Roles for phospholipase D2 and receptor transactivation. Am J Physiol Cell Physiol 298: C163-C170.
69. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA et al. (2005). Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A 102: 15545-15550. (Pubitemid 41528093)
70. Sved P, Scott KF, McLeod D, King NJ, Singh J, Tsatralis T et al. (2004). Oncogenic action of secreted phospholipase A2 in prostate cancer. Cancer Res 64: 6934-6940. (Pubitemid 39331002)
71. Taylor BS, Schultz N, Hieronymus H, Gopalan A, Xiao Y, Carver BS et al. (2010). Integrative genomic profiling of human prostate cancer. Cancer Cell 18: 11-22.
72. Tigyi G, Miledi R. (1992). Lysophosphatidates bound to serum albumin activate membrane currents in xenopus oocytes and neurite retraction in PC12 pheochromocytoma cells. J Biol Chem 267: 21360-21367.
73. Valet P, Pages C, Jeanneton O, Daviaud D, Barbe P, Record M et al. (1998). Alpha2-adrenergic receptor-mediated release of lysophosphatidic acid by adipocytes. A paracrine signal for preadipocyte growth. J Clin Invest 101: 1431-1438. (Pubitemid 28166841)
74. van Dijk MC, Postma F, Hilkmann H, Jalink K, van Blitterswijk WJ, Moolenaar WH. (1998). Exogenous phospholipase D generates lysophosphatidic acid and activates ras, rho and Ca2+ signaling pathways. Curr Biol 8: 386-392. (Pubitemid 28173997)
75. van Golen KL, Ying C, Sequeira L, Dubyk CW, Reisenberger T, Chinnaiyan AM et al. (2008). CCL2 induces prostate cancer transendothelial cell migration via activation of the small GTPase rac. J Cell Biochem 104: 1587-1597.
76. Vogler R, Sauer B, Kim DS, Schafer-Korting M, Kleuser B. (2003). Sphingosine-1-phosphate and its potentially paradoxical effects on critical parameters of cutaneous wound healing. J Invest Dermatol 120: 693-700. (Pubitemid 36344015)
77. Wang D, Zhao Z, Caperell-Grant A, Yang G, Mok SC, Liu J et al. (2008). S1P differentially regulates migration of human ovarian cancer and human ovarian surface epithelial cells. Mol Cancer Ther 7: 1993-2002.
78. Wang FQ, Ariztia EV, Boyd LR, Horton FR, Smicun Y, Hetherington JA et al. (2010). Lysophosphatidic acid (LPA) effects on endometrial carcinoma in vitro proliferation, invasion, and matrix metalloproteinase activity. Gynecol Oncol 117: 88-95.
79. Waters CM, Saatian B, Moughal NA, Zhao Y, Tigyi G, Natarajan V et al. (2006). Integrin signalling regulates the nuclear localization and function of the lysophosphatidic acid receptor-1 (LPA1) in mammalian cells. Biochem J 398: 55-62. (Pubitemid 44231301)
80. Westermann AM, Havik E, Postma FR, Beijnen JH, Dalesio O, Moolenaar WH et al. (1998). Malignant effusions contain lysophosphatidic acid (LPA)-like activity. Ann Oncol 9: 437-442. (Pubitemid 28273038)
81. Yamaguchi H,Kitayama J, Takuwa N, ArikawaK, Inoki I, Takehara K et al. (2003). Sphingosine-1-phosphate receptor subtype-specific positive and negative regulation of rac and haematogenous metastasis of melanoma cells. Biochem J 374: 715-722. (Pubitemid 37163916)
82. Zeng Y, Kakehi Y, Nouh MA, Tsunemori H, Sugimoto M, Wu XX. (2009). Gene expression profiles of lysophosphatidic acid-related molecules in the prostate: Relevance to prostate cancer and benign hyperplasia. Prostate 69: 283-292.
83. Zhang C, Baker DL, Yasuda S, Makarova N, Balazs L, Johnson LR et al. (2004). Lysophosphatidic acid induces neointima formation through PPARgamma activation. J Exp Med 199: 763-774. (Pubitemid 38375196)