publication . Article . 2017

LPP3 mediates self-generation of chemotactic LPA gradients by melanoma cells

Susanto, Olivia; Koh, Yvette W. H.; Morrice, Nick; Tumanov, Sergey; Thomason, Peter A.; Nielson, Matthew; Tweedy, Luke; Muinonen-Martin, Andrew J.; Kamphorst, Jurre J.; Mackay, Gillian M.; ...
Open Access English
  • Published: 15 Oct 2017 Journal: Journal of Cell Science, volume 130, issue 20, pages 3,455-3,466 (issn: 0021-9533, eissn: 1477-9137, Copyright policy)
  • Publisher: The Company of Biologists Ltd
Abstract
ABSTRACT Melanoma cells steer out of tumours using self-generated lysophosphatidic acid (LPA) gradients. The cells break down LPA, which is present at high levels around the tumours, creating a dynamic gradient that is low in the tumour and high outside. They then migrate up this gradient, creating a complex and evolving outward chemotactic stimulus. Here, we introduce a new assay for self-generated chemotaxis, and show that raising LPA levels causes a delay in migration rather than loss of chemotactic efficiency. Knockdown of the lipid phosphatase LPP3 – but not of its homologues LPP1 or LPP2 – diminishes the cell's ability to break down LPA. This is specific f...
Subjects
mesheuropmc: biological phenomena, cell phenomena, and immunitylipids (amino acids, peptides, and proteins)
free text keywords: Research Article, Metastasis, LPP3, Melanoma, Self-generated gradients, LPA, Chemotaxis
39 references, page 1 of 3

American Cancer Society (2014). Cancer Facts and Figures. Atlanta, GA: American Cancer Society.

Baker, D. L., Desiderio, D. M., Miller, D. D., Tolley, B. D. and Tigyi, G. J. (2001). Direct quantitative analysis of lysophosphatidic acid molecular species by stable isotope dilution electrospray ionization liquid chromatography-mass spectrometry. Anal. Biochem. 292, 287-295.

Benesch, M. G., Tang, X., Venkatraman, G., Bekele, R. T. and Brindley, D. N. (2016). Recent advances in targeting the auto-taxin-lysophosphatidate-lipid phosphate phosphatase axis in vivo. J. Biomed. Res. 30, 272-284. [OpenAIRE]

Bennett, D. C. (2008). How to make a melanoma: what do we know of the primary clonal events? Pigment Cell Melanoma Res. 21, 27-38.

Breart, B., Ramos-Perez, W., Mendoza, A., Salous, A., Gobert, M., Huang, Y., Adams, R., Lafaille, J., Escalante-Alcalde, D., Morris, A. et al. (2011). Lipid phosphate phosphatase 3 enables efficient thymic egress. J. Exp. Med. 208, 1267-1278. [OpenAIRE]

Choi, J. W., Herr, D. R., Noguchi, K., Yung, Y. C., Lee, C.-W., Mutoh, T., Lin, M.-E., Teo, S. T., Park, K. E., Mosley, A. N. et al. (2010). LPA receptors: subtypes and biological actions. Annu. Rev. Pharmacol. Toxicol. 50, 157-186.

Clasquin, M. F., Melamud, E. and Rabinowitz, J. D. (2012). LC-MS data processing with MAVEN: a metabolomic analysis and visualization engine. Curr. Protoc. Bioinformatics 37, 14.11.11-14.11.23. [OpenAIRE]

Eichholtz, T., Jalink, K., Fahrenfort, I. and Moolenaar, W. (1993). The bioactive phospholipid lysophosphatidic acid is released from activated platelets. Biochem. J. 291, 677-680. [OpenAIRE]

Elder, D. (2015). Pathology of melanoma. Surg. Oncol. Clin. N Am. 24, 229-237.

Escalante-Alcalde, D., Hernandez, L., Le Stunff, H., Maeda, R., Lee, H.-S., Jr-Gang-Cheng, Sciorra, V. A., Daar, I., Spiegel, S., Morris, A. J. et al. (2003). The lipid phosphatase LPP3 regulates extra-embryonic vasculogenesis and axis patterning. Development 130, 4623-4637.

Fang, X., Schummer, M., Mao, M., Yu, S., Tabassam, F. H., Swaby, R., Hasegawa, Y., Tanyi, J. L., LaPushin, R., Eder, A. et al. (2002). Lysophosphatidic acid is a bioactive mediator in ovarian cancer. Biochim. Biophys. Acta 1582, 257-264.

Humtsoe, J., Liu, M., Malik, A. and Wary, K. (2010). Lipid phosphate phosphatase 3 stabilization of β-catenin induces endothelial cell migration and formation of branching point structures. Mol. Cell. Biol. 30, 1593-1606.

Insall, R. and Andrew, N. (2007). Chemotaxis in Dictyostelium: how to walk straight using parallel pathways. Curr. Opin. Microbiol. 10, 578-581.

Jalink, K., Hengeveld, T., Mulder, S., Postma, F. R., Simon, M. F., Chap, H., van der Marel, G. A., van Boom, J. H., van Blitterswijk, W. J. and Moolenaar, W. H. (1995). Lysophosphatidic acid-induced Ca2+ mobilization in human A431 cells: structure-activity analysis. Biochem. J. 307, 609-616. [OpenAIRE]

Li, F. Z., Dhillon, A. S., Anderson, R. L., McArthur, G. and Ferrao, P. T. (2015). Phenotype switching in melanoma: implications for progression and therapy. Front. Oncol. 5, 31.

39 references, page 1 of 3
Abstract
ABSTRACT Melanoma cells steer out of tumours using self-generated lysophosphatidic acid (LPA) gradients. The cells break down LPA, which is present at high levels around the tumours, creating a dynamic gradient that is low in the tumour and high outside. They then migrate up this gradient, creating a complex and evolving outward chemotactic stimulus. Here, we introduce a new assay for self-generated chemotaxis, and show that raising LPA levels causes a delay in migration rather than loss of chemotactic efficiency. Knockdown of the lipid phosphatase LPP3 – but not of its homologues LPP1 or LPP2 – diminishes the cell's ability to break down LPA. This is specific f...
Subjects
mesheuropmc: biological phenomena, cell phenomena, and immunitylipids (amino acids, peptides, and proteins)
free text keywords: Research Article, Metastasis, LPP3, Melanoma, Self-generated gradients, LPA, Chemotaxis
39 references, page 1 of 3

American Cancer Society (2014). Cancer Facts and Figures. Atlanta, GA: American Cancer Society.

Baker, D. L., Desiderio, D. M., Miller, D. D., Tolley, B. D. and Tigyi, G. J. (2001). Direct quantitative analysis of lysophosphatidic acid molecular species by stable isotope dilution electrospray ionization liquid chromatography-mass spectrometry. Anal. Biochem. 292, 287-295.

Benesch, M. G., Tang, X., Venkatraman, G., Bekele, R. T. and Brindley, D. N. (2016). Recent advances in targeting the auto-taxin-lysophosphatidate-lipid phosphate phosphatase axis in vivo. J. Biomed. Res. 30, 272-284. [OpenAIRE]

Bennett, D. C. (2008). How to make a melanoma: what do we know of the primary clonal events? Pigment Cell Melanoma Res. 21, 27-38.

Breart, B., Ramos-Perez, W., Mendoza, A., Salous, A., Gobert, M., Huang, Y., Adams, R., Lafaille, J., Escalante-Alcalde, D., Morris, A. et al. (2011). Lipid phosphate phosphatase 3 enables efficient thymic egress. J. Exp. Med. 208, 1267-1278. [OpenAIRE]

Choi, J. W., Herr, D. R., Noguchi, K., Yung, Y. C., Lee, C.-W., Mutoh, T., Lin, M.-E., Teo, S. T., Park, K. E., Mosley, A. N. et al. (2010). LPA receptors: subtypes and biological actions. Annu. Rev. Pharmacol. Toxicol. 50, 157-186.

Clasquin, M. F., Melamud, E. and Rabinowitz, J. D. (2012). LC-MS data processing with MAVEN: a metabolomic analysis and visualization engine. Curr. Protoc. Bioinformatics 37, 14.11.11-14.11.23. [OpenAIRE]

Eichholtz, T., Jalink, K., Fahrenfort, I. and Moolenaar, W. (1993). The bioactive phospholipid lysophosphatidic acid is released from activated platelets. Biochem. J. 291, 677-680. [OpenAIRE]

Elder, D. (2015). Pathology of melanoma. Surg. Oncol. Clin. N Am. 24, 229-237.

Escalante-Alcalde, D., Hernandez, L., Le Stunff, H., Maeda, R., Lee, H.-S., Jr-Gang-Cheng, Sciorra, V. A., Daar, I., Spiegel, S., Morris, A. J. et al. (2003). The lipid phosphatase LPP3 regulates extra-embryonic vasculogenesis and axis patterning. Development 130, 4623-4637.

Fang, X., Schummer, M., Mao, M., Yu, S., Tabassam, F. H., Swaby, R., Hasegawa, Y., Tanyi, J. L., LaPushin, R., Eder, A. et al. (2002). Lysophosphatidic acid is a bioactive mediator in ovarian cancer. Biochim. Biophys. Acta 1582, 257-264.

Humtsoe, J., Liu, M., Malik, A. and Wary, K. (2010). Lipid phosphate phosphatase 3 stabilization of β-catenin induces endothelial cell migration and formation of branching point structures. Mol. Cell. Biol. 30, 1593-1606.

Insall, R. and Andrew, N. (2007). Chemotaxis in Dictyostelium: how to walk straight using parallel pathways. Curr. Opin. Microbiol. 10, 578-581.

Jalink, K., Hengeveld, T., Mulder, S., Postma, F. R., Simon, M. F., Chap, H., van der Marel, G. A., van Boom, J. H., van Blitterswijk, W. J. and Moolenaar, W. H. (1995). Lysophosphatidic acid-induced Ca2+ mobilization in human A431 cells: structure-activity analysis. Biochem. J. 307, 609-616. [OpenAIRE]

Li, F. Z., Dhillon, A. S., Anderson, R. L., McArthur, G. and Ferrao, P. T. (2015). Phenotype switching in melanoma: implications for progression and therapy. Front. Oncol. 5, 31.

39 references, page 1 of 3
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publication . Article . 2017

LPP3 mediates self-generation of chemotactic LPA gradients by melanoma cells

Susanto, Olivia; Koh, Yvette W. H.; Morrice, Nick; Tumanov, Sergey; Thomason, Peter A.; Nielson, Matthew; Tweedy, Luke; Muinonen-Martin, Andrew J.; Kamphorst, Jurre J.; Mackay, Gillian M.; ...