Bioactive lipids lysophosphatidic acid and sphingosine 1-phosphate mediate breast cancer cell biological functions through distinct mechanisms

Oncology Research

Volumn 18, Issue 4, 2009, Pages 173-184

  Boucharaba, Ahmed ^a   Guillet, Benoit ^b   Menaa, Farid ^c   Hneino, Mohamed ^d,e   Van Wijnen, Andre J ^f   Clézardin, Philippe ^d,e   Peyruchaud, Oliver ^d,e  

^a EPFL   (Switzerland)

^b Department of Pediatric Hematology   (France)

^c SIDNEY KIMMEL CANCER CENTER   (United States)

^d INSERM   (France)

^e UNIVERSITÉ LYON 1   (France)

^f UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

Angiogenesis; Breast cancer cells; Invasion; Lysophosphatidic acid (LPA); Migration; Osteoclastogenesis; Proliferation; Sphingosine 1 phosphate (S1P)

Indexed keywords

GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 6; LYSOPHOSPHATIDIC ACID; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MONOCYTE CHEMOTACTIC PROTEIN 1; SPHINGOSINE 1 PHOSPHATE; VASCULOTROPIN A; CCL2 PROTEIN, HUMAN; CXCL1 CHEMOKINE; CXCL1 PROTEIN, HUMAN; DRUG DERIVATIVE; INTERLEUKIN 8; LYSOPHOSPHOLIPID; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; SPHINGOSINE; SPHINGOSINE 1-PHOSPHATE; VEGFA PROTEIN, HUMAN;

ARTICLE; BONE METASTASIS; BREAST CANCER; CELL FUNCTION; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; ANGIOGENESIS; BONE MARROW CELL; BREAST TUMOR; CELL ADHESION; CELL CULTURE; CELL MOTION; CYTOLOGY; DRUG EFFECT; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; GENETICS; METABOLISM; OSTEOCLAST; PATHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UMBILICAL VEIN; VASCULAR ENDOTHELIUM;

1-PHOSPHATIDYLINOSITOL 3-KINASE; BONE MARROW CELLS; BREAST NEOPLASMS; CELL ADHESION; CELL MOVEMENT; CELL PROLIFERATION; CELLS, CULTURED; CHEMOKINE CCL2; CHEMOKINE CXCL1; ENDOTHELIUM, VASCULAR; ENZYME-LINKED IMMUNOSORBENT ASSAY; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; HUMANS; INTERLEUKIN-6; INTERLEUKIN-8; LYSOPHOSPHOLIPIDS; NEOVASCULARIZATION, PHYSIOLOGIC; OSTEOCLASTS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SPHINGOSINE; UMBILICAL VEINS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 77649221616     PISSN: 09650407     EISSN: None     Source Type: Journal    
DOI: 10.3727/096504009790217399     Document Type: Article

References (43)

1. Boucharaba, A.; Serre, C. M.; Gres, S.; Saulnier-Blache, J. S.; Bordet, J. C.; Guglielmi, J.; Clezardin, P.; Peyruchaud, O. J. Platelet-derived lysophosphatidic acid supports the progression of osteolytic bone metastases in breast cancer. Clin. Invest. 114:1714-1725; 2004.
2. Visentin, B.; Vekich, J. A.; Sibbald, B. J.; Cavalli, A. L.; Moreno, K. M.; Matteo, R. G.; Garland, W. A.; Lu, Y.; Yu, S.; Hall, H. S.; Kundra, V.; Mills, G. B.; Sabbadini, R. A. Validation of an anti-sphingosine-1-phosphate antibody as a potnetial therapeutic in reducing growth, invasion, and angiogenesis in multiple tumor lineages. Cancer Cell 9:225-238; 2006.
3. Boucharaba, A.; Serre, C. M.; Guglielmi, J.; Bordet, J. C.; Clezardin, P.; Peyruchaud, O. Tye type 1 lysophosphatidic acid receptor is a target for therapy in bone metastases. Proc. Natl. Acad. Sci. USA 103:9643-9648; 2006.
4. Ishii, I.; Fukushima, N.; Ye, X.; Chun, J. Lysophospholipid receptors: Signaling and biology. Annu. Rev. Biochem. 73:321-354; 2004.
5. Birgbauer, E.; Chun, J. New developments in the biological functions of lysophospholipids. Cell. Mol. Life Sci. 63:2695-2701; 2006.
6. Umezu-Goto, M.; Kishi, Y.; Taira, A.; Hama, K.; Dohmae, N.; Takio, K.; Yamori, T.; Mills, G. B.; Inoue, K.; Aoki, J.; Arai, H. Autotaxin has lysophospholipase D activity leading to tumor cell growth and motility by lysophosphatidic acid production. J. Cell. Biol. 158:227-233; 2002.
7. Maceyka, M.; Sankala, H.; Hait, N. C.; Le Stunff, H.; Liu, H.; Toman, R.; Collier, C.; Zhang, M.; Satin, L. S.; Merrill, Jr., A. H.; Milstien, S.; Spiegel, S. SphK1 and SphK2, sphingosine kinase isoenzymes with opposing functions in sphingolipid metabolism. J. Biol. Chem. 280:37118-37129; 2005.
8. Eichholtz, T.; Jalink, K.; Fahrenfort, I.; Moolenaar, W. H. The bioactive phospholipid lysophosphatidic acid is released from activated platelets. Biochem. J. 291:677-680; 1993.
9. Yatomi, Y.; Ohmori, T.; Rile, G.; Kazama, F.; Okamoto, H.; Sano, T.; Satoh, K.; Kume, S.; Tigyi, G.; Igarashi, Y.; Ozaki, Y. Sphingosine 1-phosphate as a major bioactive oysophospholipid that is released from platelets and interacts with endothelial cells. Blood 96:3431-3438; 2000.
10. Meyer Zu Heringdorf, D. Lysophospholipid receptor-dependent and -independent calcium signaling. J. Cell. Biochem. 92:937-948; 2004.
11. Kotarsky, K.; Boketoft, A.; Bristulf, J.; Nilsson, N. E.; Norberg, A.; Hansson, S.; Owman, C.; Sillard, R.; Leeb-Lundberg, L. M.; Olde, B. Lysophosphatidic acid binds to and activates GPR92, a G protein-coupled receptor highly expressed in gastrointestinal lymphocytes. J. Pharmacol. Exp. Ther. 318:619-628; 2006.
12. Noguchi, K.; Ishii, S.; Shimizu, T. Identification of p2y/GPR23 as a novel G protein-coupled receptor for lysophosphaticid acid, structurally distant from the Edg family. J. Biol. Chem. 278:25600-25606; 2003.
13. Tabata, K.; Baba, K.; Shiraishi, A.; Ito, M.; Fujita, N. The orphan GPCR GPR87 was deorphanized and shown to be a lysophosphatidic acid receptor. Biochem. Biophys. Res. Commun. 363:861-866; 2007.
14. Siess, W.; Tigyi, G. Thrombogenic and atherogenic activities of lysophosphatidic acid. J. Cell. Biochem. 92:1086-1094; 2004.
15. Pasternack, S. M.; von Kugelgen, I.; Aboud, K. A.; Lee, Y. A.; Ruschendorf, F.; Voss, K.; Hillmer, A. M.; Molderings, G. J.; Franz, T.; Ramirez, A.; Nurnberg, P.; Nothen, M. M.; Betz, R. C. G protein-coupled receptor P2&5 and its ligand LPA are involved in maintenance of human hair growth. Nat. Genet. 40:329-334; 2008.
16. Pecheur, I.; Peyruchaud, O.; Serre, C. M.; Guglielmi, J.; Voland, C.; Bourre, F.; Margue, C.; Cohen-Solal, M.; Buffet, A.; Kieffer, N.; Clezardin, P. Integrin alpha(v) beta3 expression confers on tumor cells a greater propensity to metastasize to bone. FASEB J. 16:1266-1268; 2002.
17. Peyruchaud, O.; Winding, B.; Pecheur, I.; Serre, C. M.; Delmas, P.; Clezardin, P. Early detection of bone metastases in a murine model using fluorescent human breast cancer cells: Application to the use of the bisphosphonate zoledronic acid in the the treatment of osteolytic lesions. J. Bone Miner. Res. 16:2027-2034; 2001.
18. Peyruchaud, O.; Mosher, D. F. Differential simulation of signaling pathways initiated by Edg-2 in response to lysophosphaticid acid or sphingosine-1-phosphate. Cell. Mol. Life Sci. 57:1109-1116; 2000.
19. Goetzl, E. J.; Dolezalova, H.; Kong, Y.; Zeng, L. Dual mechanisms for lysophospholipid induction of proliferation of human breast carcinoma cells. Cancer Res. 59:4732-4737; 1999.
20. Boissier, S.; Ferreras, M.; Peyruchaud, O.; Magnetto, S.; Ebetino, F. H.; Colombel, M.; Delmas, P.; Delaisse, J. M.; Clezardin, P. Bisphosphonates inhibit breast and prostate carcinoma cell invasion, an early event in the formation of bone metastases. Cancer Res. 60:2949-2954; 2000.
21. Fang, X.; Yu, S.; Bast, R. C.; Liu, S.; Xu, H. J.; Hu, S. X.; LaPushin, R.; Claret, F. X.; Aggarwal, B. B.; Lu, Y.; Mills, G. B. Mechanisms for lysophosphaticid acid-induced cytokine production in ovarian cancer cells. J. Biol. Chem. 279:9653-9661; 2004.
22. Sukocheva, O.; Wadham, C.; Holmes, A.; Albanese, N.; Verrier, E.; Feng, F.; Bernal, A.; Derian, C. K.; Ullrich, A.; Vadas, M. A.; Xia, P. Estrogen transactivates EGFR via the sphingosine 1-phosphate receptor Edg-3: The role of sphingosine kinase-1. J. Cell Biol. 173:301-310; 2006.
23. Shida, D.; Fang, X.; Kordula, T.; Takabe, K.; Lepine, S.; Alvarez, S. E.; Milstien, S.; Spiegel, S. Cross-talk between LPA1 and epidermal growth factor receptors mediates up-regulation of sphingosine kinase 1 to promote gastric cancer cell motility and invasion. Cancer Res. 68:6569-6577; 2008.
24. Graler, M. H.; Goetzl, E. J. Lysophospholipids and their G protein-coupled receptors in inflammation and immunity. Biochim. Biophys. Acta 1582:168-174; 2002.
25. Panetti, T. S. Differential effects of sphingosine 1-phosphate and lysophosphatidic acid on endothelial cells. Biochim. Biophys. Acta 1582:190-196; 2002.
26. Hama, K.; Aoki, J.; Fukaya, M.; Kishi, Y.; Sakai, T.; Suzuki, R.; Ohta, H.; Yamori, T.; Watanabe, M.; Chun, J.; Arai, H. Lysophosphatidic acid and autotaxin stimulate cell motility of neoplastic and non-neoplastic cells through LPA1. J. Biol. Chem. 279:17634-17639; 2004.
27. Pantel, K.; Brakenhoff, R. H. Dissecting the metastatic cascade. Nat. Rev. Cancer 4:448-456; 2004.
28. Hanahan, D.; Folkman, J. Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell 86:353-364; 1996.
29. Hu, Y. L.; Tee, M. K.; Goetzl, E. J.; Auersperg, N.; Mills, G. B.; Ferrara, N.; Jaffe, R. B. Lysophosphaticid acid induction of vascular endothelial growth factor expression in human ovarian cancer cells. J. Natl. Cancer Inst. 93:762-768; 2001.
30. Coleman, R. E. Skeletal complications of malignancy. Cancer 80:1588-1594; 1997.
31. Aoki, J.; Taira, A.; Takanezawa, Y.; Kishi, Y.; Hama, K.; Kishimoto, T.; Mizuno, K.; Saku, K.; Taguchi, R.; Arai, H. Seum lysophosphaticid acid is produced through diverse phospholipase pathways. J. Biol. Chem. 277:48737-48744; 2002.
32. Yatomi, Y.; Igarashi, Y.; Yang, L.; Hisano, N.; Qi, R.; Asazuma, N.; Satoh, K.; Ozaki, Y.; Kume, S. Sphingosine 1-phosphate, a bioactive sphingolipid abundantly stored in platelets, is a normal constituent of human plasma and serum. J. Biochem. (Tokyo) 121:969-973; 1997.
33. Mills, G. B.; Moolenaar, W. H. The emerging role of lysophosphatidic acid in cancer. Nat. Rev. Cancer 3:582-591; 2003.
34. Taghavi, P.; Verhoeven, E.; Jacobs, J. J.; Lambooij, J. P.; Stortelers, C.; Tanger, E.; Moolenaar, W. H.; van Lohuizen, M. In vitro genetic screen identifies a cooperative role for LPA signaling and c-Myc in cell transformation. Oncogene 27:6806-6816; 2008.
35. Zwick, E.; Hackel, P. O.; Prenzel, N.; Ullrich, A. The EGF receptor as central transducer of heterologous signaling systems. Trends Pharmacol. Sci. 20:408-412; 1999.
36. Roudabush, F. L.; Pierce, K. L.; Maudsley, S.; Khan, K. D.; Luttrell, L. M. Transactivation of the EGF receptor mediates IGF-1-stimulated shc phosphorylation and ERK1/2 activation in COS-7 cells. J. Biol. Chem. 275:22583-22589; 2000.
37. Rodland, K. D.; Bollinger, N.; Ippolito, D.; Opresko, L. K.; Coffey, R. J.; Zangar, R.; Wiley, H. S. Multiple mechanisms are responsible for transactivation of the epidermal growth factor receptor in mammary epithelial cells. J. Biol. Chem. 283:31477-31487; 2008.
38. Fegley, A. J.; Tanski, W. J.; Roztocil, E.; Davies, M. G. Sphingosine-1-phosphate stimulates smooth muscle cell migration through galpha(i)- and pi3-kinase-dependent p38(MAPK) activation. J. Surg. Res. 113:32-41; 2003.
39. Lee, J.; Park, S. Y.; Lee, E. K.; Park, C. G.; Chung, H. C.; Rha, S. Y.; Kim, Y. K.; Bae, G. U.; Kim, B. K.; Han, J. W.; Lee, H. Y. Activation of hypoxia-inducible factor-1alpha is necessary for lysophosphatidic acid-induced vascular endothelial growth factor expression. Clin. Cancer Res. 12:6351-6358; 2006.
40. Motro, B.; Itin, A.; Sachs, L.; Keshet, E. Pattern of interleukin 6 gene expression in vivo suggests a role for this cytokine in angiogenesis. Proc. Natl. Acad. Sci. USA 87:3092-3096; 1990.
41. Koch, A. E.; Polverini, P. J.; Kunkel, S. L.; Harlow, L. A.; DiPietro, L. A.; Elner, V. M.; Elner, S. G.; Strieter, R. M. Interleukin-8 as a macrophage-derived mediator of angiogenesis. Science 258:1798-1801; 1992.
42. de la Mata, J.; Uy, H. L.; Guise, T. A.; Story, B.; Boyce, B. F.; Mundy, G. R.; Roodman, G. D. Interleukin-6 enhances hypercalcemia and bone resorption mediated by parathyroid hormone-related protein in vivo. J. Clin. Invest. 95:2846-2852; 1995.
43. Bendre, M. S.; Gaddy-Kurten, D.; Mon-Foote, T.; Akel, N. S.; Skinner, R. A.; Nicholas, R. W.; Suva, L. J. Expression of interleukin 8 and not parathyroid hormone-related protein by human breast cancer cells correlates with bone metastasis in vivo. Cancer Res. 62:5571-5579; 2002.