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Erschienen in: Cancer and Metastasis Reviews 2-3/2018

20.06.2018

Role of autotaxin in cancer stem cells

verfasst von: Dongjun Lee, Dong-Soo Suh, Sue Chin Lee, Gabor J. Tigyi, Jae Ho Kim

Erschienen in: Cancer and Metastasis Reviews | Ausgabe 2-3/2018

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Abstract

Stem cells are a rare subpopulation defined by the potential to self-renew and differentiate into specific cell types. A population of stem-like cells has been reported to possess the ability of self-renewal, invasion, metastasis, and engraftment of distant tissues. This unique cell subpopulation has been designated as cancer stem cells (CSC). CSC were first identified in leukemia, and the contributions of CSC to cancer progression have been reported in many different types of cancers. The cancer stem cell hypothesis attempts to explain tumor cell heterogeneity based on the existence of stem cell-like cells within solid tumors. The elimination of CSC is challenging for most human cancer types due to their heightened genetic instability and increased drug resistance. To combat these inherent abilities of CSC, multi-pronged strategies aimed at multiple aspects of CSC biology are increasingly being recognized as essential for a cure. One of the most challenging aspects of cancer biology is overcoming the chemotherapeutic resistance in CSC. Here, we provide an overview of autotaxin (ATX), lysophosphatidic acid (LPA), and their signaling pathways in CSC. Increasing evidence supports the role of ATX and LPA in cancer progression, metastasis, and therapeutic resistance. Several studies have demonstrated the ATX-LPA axis signaling in different cancers. This lipid mediator regulatory system is a novel potential therapeutic target in CSC. In this review, we summarize the evidence linking ATX-LPA signaling to CSC and its impact on cancer progression and metastasis. We also provide evidence for the efficacy of cancer therapy involving the pharmacological inhibition of this signaling pathway.
Literatur
4.
Zurück zum Zitat Singh, S. K., Clarke, I. D., Terasaki, M., Bonn, V. E., Hawkins, C., Squire, J., & Dirks, P. B. (2003). Identification of a cancer stem cell in human brain tumors. Cancer Research, 63(18), 5821–5828.PubMed Singh, S. K., Clarke, I. D., Terasaki, M., Bonn, V. E., Hawkins, C., Squire, J., & Dirks, P. B. (2003). Identification of a cancer stem cell in human brain tumors. Cancer Research, 63(18), 5821–5828.PubMed
10.
Zurück zum Zitat Prince, M. E., Sivanandan, R., Kaczorowski, A., Wolf, G. T., Kaplan, M. J., Dalerba, P., Weissman, I. L., Clarke, M. F., & Ailles, L. E. (2007). Identification of a subpopulation of cells with cancer stem cell properties in head and neck squamous cell carcinoma. Proceedings of the National Academy of Sciences of the United States of America, 104(3), 973–978. https://doi.org/10.1073/pnas.0610117104.PubMedPubMedCentralCrossRef Prince, M. E., Sivanandan, R., Kaczorowski, A., Wolf, G. T., Kaplan, M. J., Dalerba, P., Weissman, I. L., Clarke, M. F., & Ailles, L. E. (2007). Identification of a subpopulation of cells with cancer stem cell properties in head and neck squamous cell carcinoma. Proceedings of the National Academy of Sciences of the United States of America, 104(3), 973–978. https://​doi.​org/​10.​1073/​pnas.​0610117104.PubMedPubMedCentralCrossRef
14.
16.
18.
Zurück zum Zitat Janiszewska, M., Suva, M. L., Riggi, N., Houtkooper, R. H., Auwerx, J., Clement-Schatlo, V., Radovanovic, I., Rheinbay, E., Provero, P., & Stamenkovic, I. (2012). Imp2 controls oxidative phosphorylation and is crucial for preserving glioblastoma cancer stem cells. Genes & Development, 26(17), 1926–1944. https://doi.org/10.1101/gad.188292.112.CrossRef Janiszewska, M., Suva, M. L., Riggi, N., Houtkooper, R. H., Auwerx, J., Clement-Schatlo, V., Radovanovic, I., Rheinbay, E., Provero, P., & Stamenkovic, I. (2012). Imp2 controls oxidative phosphorylation and is crucial for preserving glioblastoma cancer stem cells. Genes & Development, 26(17), 1926–1944. https://​doi.​org/​10.​1101/​gad.​188292.​112.CrossRef
23.
30.
Zurück zum Zitat Stracke, M. L., Krutzsch, H. C., Unsworth, E. J., Arestad, A., Cioce, V., Schiffmann, E., & Liotta, L. A. (1992). Identification, purification, and partial sequence analysis of autotaxin, a novel motility-stimulating protein. The Journal of Biological Chemistry, 267(4), 2524–2529.PubMed Stracke, M. L., Krutzsch, H. C., Unsworth, E. J., Arestad, A., Cioce, V., Schiffmann, E., & Liotta, L. A. (1992). Identification, purification, and partial sequence analysis of autotaxin, a novel motility-stimulating protein. The Journal of Biological Chemistry, 267(4), 2524–2529.PubMed
32.
Zurück zum Zitat Tokumura, A., Majima, E., Kariya, Y., Tominaga, K., Kogure, K., Yasuda, K., & Fukuzawa, K. (2002). Identification of human plasma lysophospholipase D, a lysophosphatidic acid-producing enzyme, as autotaxin, a multifunctional phosphodiesterase. The Journal of Biological Chemistry, 277(42), 39436–39442. https://doi.org/10.1074/jbc.M205623200.PubMedCrossRef Tokumura, A., Majima, E., Kariya, Y., Tominaga, K., Kogure, K., Yasuda, K., & Fukuzawa, K. (2002). Identification of human plasma lysophospholipase D, a lysophosphatidic acid-producing enzyme, as autotaxin, a multifunctional phosphodiesterase. The Journal of Biological Chemistry, 277(42), 39436–39442. https://​doi.​org/​10.​1074/​jbc.​M205623200.PubMedCrossRef
37.
Zurück zum Zitat Nakasaki, T., Tanaka, T., Okudaira, S., Hirosawa, M., Umemoto, E., Otani, K., Jin, S., Bai, Z., Hayasaka, H., Fukui, Y., Aozasa, K., Fujita, N., Tsuruo, T., Ozono, K., Aoki, J., & Miyasaka, M. (2008). Involvement of the lysophosphatidic acid-generating enzyme autotaxin in lymphocyte-endothelial cell interactions. The American Journal of Pathology, 173(5), 1566–1576. https://doi.org/10.2353/ajpath.2008.071153.PubMedPubMedCentralCrossRef Nakasaki, T., Tanaka, T., Okudaira, S., Hirosawa, M., Umemoto, E., Otani, K., Jin, S., Bai, Z., Hayasaka, H., Fukui, Y., Aozasa, K., Fujita, N., Tsuruo, T., Ozono, K., Aoki, J., & Miyasaka, M. (2008). Involvement of the lysophosphatidic acid-generating enzyme autotaxin in lymphocyte-endothelial cell interactions. The American Journal of Pathology, 173(5), 1566–1576. https://​doi.​org/​10.​2353/​ajpath.​2008.​071153.PubMedPubMedCentralCrossRef
39.
Zurück zum Zitat van Meeteren, L. A., Ruurs, P., Stortelers, C., Bouwman, P., van Rooijen, M. A., Pradere, J. P., Pettit, T. R., Wakelam, M. J. O., Saulnier-Blache, J. S., Mummery, C. L., Moolenaar, W. H., & Jonkers, J. (2006). Autotaxin, a secreted lysophospholipase D, is essential for blood vessel formation during development. Molecular and Cellular Biology, 26(13), 5015–5022. https://doi.org/10.1128/Mcb.02419-05.PubMedPubMedCentralCrossRef van Meeteren, L. A., Ruurs, P., Stortelers, C., Bouwman, P., van Rooijen, M. A., Pradere, J. P., Pettit, T. R., Wakelam, M. J. O., Saulnier-Blache, J. S., Mummery, C. L., Moolenaar, W. H., & Jonkers, J. (2006). Autotaxin, a secreted lysophospholipase D, is essential for blood vessel formation during development. Molecular and Cellular Biology, 26(13), 5015–5022. https://​doi.​org/​10.​1128/​Mcb.​02419-05.PubMedPubMedCentralCrossRef
42.
Zurück zum Zitat Sasagawa, T., Okita, M., Murakami, J., Kato, T., & Watanabe, A. (1999). Abnormal serum lysophospholipids in multiple myeloma patients. Lipids, 34(1), 17–21.PubMedCrossRef Sasagawa, T., Okita, M., Murakami, J., Kato, T., & Watanabe, A. (1999). Abnormal serum lysophospholipids in multiple myeloma patients. Lipids, 34(1), 17–21.PubMedCrossRef
43.
Zurück zum Zitat Eder, A. M., Sasagawa, T., Mao, M., Aoki, J., & Mills, G. B. (2000). Constitutive and lysophosphatidic acid (LPA)-induced LPA production: role of phospholipase D and phospholipase A2. Clinical Cancer Research, 6(6), 2482–2491.PubMed Eder, A. M., Sasagawa, T., Mao, M., Aoki, J., & Mills, G. B. (2000). Constitutive and lysophosphatidic acid (LPA)-induced LPA production: role of phospholipase D and phospholipase A2. Clinical Cancer Research, 6(6), 2482–2491.PubMed
44.
Zurück zum Zitat Hu, Y. L., Tee, M. K., Goetzl, E. J., Auersperg, N., Mills, G. B., Ferrara, N., & Jaffe, R. B. (2001). Lysophosphatidic acid induction of vascular endothelial growth factor expression in human ovarian cancer cells. Journal of the National Cancer Institute, 93(10), 762–768.PubMedCrossRef Hu, Y. L., Tee, M. K., Goetzl, E. J., Auersperg, N., Mills, G. B., Ferrara, N., & Jaffe, R. B. (2001). Lysophosphatidic acid induction of vascular endothelial growth factor expression in human ovarian cancer cells. Journal of the National Cancer Institute, 93(10), 762–768.PubMedCrossRef
45.
47.
48.
Zurück zum Zitat Fishman, D. A., Liu, Y., Ellerbroek, S. M., & Stack, M. S. (2001). Lysophosphatidic acid promotes matrix metalloproteinase (MMP) activation and MMP-dependent invasion in ovarian cancer cells. Cancer Research, 61(7), 3194–3199.PubMed Fishman, D. A., Liu, Y., Ellerbroek, S. M., & Stack, M. S. (2001). Lysophosphatidic acid promotes matrix metalloproteinase (MMP) activation and MMP-dependent invasion in ovarian cancer cells. Cancer Research, 61(7), 3194–3199.PubMed
53.
Zurück zum Zitat Sun, H., Ren, J., Zhu, Q., Kong, F. Z., Wu, L., & Pan, B. R. (2009). Effects of lysophosphatidic acid on human colon cancer cells and its mechanisms of action. World Journal of Gastroenterology, 15(36), 4547–4555.PubMedPubMedCentralCrossRef Sun, H., Ren, J., Zhu, Q., Kong, F. Z., Wu, L., & Pan, B. R. (2009). Effects of lysophosphatidic acid on human colon cancer cells and its mechanisms of action. World Journal of Gastroenterology, 15(36), 4547–4555.PubMedPubMedCentralCrossRef
55.
60.
61.
Zurück zum Zitat Seo, E. J., Kwon, Y. W., Jang, I. H., Kim, D. K., Lee, S. I., Choi, E. J., Kim, K. H., Suh, D. S., Lee, J. H., Choi, K. U., Lee, J. W., Mok, H. J., Kim, K. P., Matsumoto, H., Aoki, J., & Kim, J. H. (2016). Autotaxin regulates maintenance of ovarian Cancer stem cells through lysophosphatidic acid-mediated autocrine mechanism. Stem Cells, 34(3), 551–564. https://doi.org/10.1002/stem.2279. PubMedCrossRef Seo, E. J., Kwon, Y. W., Jang, I. H., Kim, D. K., Lee, S. I., Choi, E. J., Kim, K. H., Suh, D. S., Lee, J. H., Choi, K. U., Lee, J. W., Mok, H. J., Kim, K. P., Matsumoto, H., Aoki, J., & Kim, J. H. (2016). Autotaxin regulates maintenance of ovarian Cancer stem cells through lysophosphatidic acid-mediated autocrine mechanism. Stem Cells, 34(3), 551–564. https://​doi.​org/​10.​1002/​stem.​2279.​ PubMedCrossRef
62.
Zurück zum Zitat Kawagoe, H., Stracke, M. L., Nakamura, H., & Sano, K. (1997). Expression and transcriptional regulation of the PD-Ialpha/autotaxin gene in neuroblastoma. Cancer Research, 57(12), 2516–2521.PubMed Kawagoe, H., Stracke, M. L., Nakamura, H., & Sano, K. (1997). Expression and transcriptional regulation of the PD-Ialpha/autotaxin gene in neuroblastoma. Cancer Research, 57(12), 2516–2521.PubMed
63.
Zurück zum Zitat Zhang, G., Zhao, Z., Xu, S., Ni, L., & Wang, X. (1999). Expression of autotaxin mRNA in human hepatocellular carcinoma. Chinese Medical Journal, 112(4), 330–332.PubMed Zhang, G., Zhao, Z., Xu, S., Ni, L., & Wang, X. (1999). Expression of autotaxin mRNA in human hepatocellular carcinoma. Chinese Medical Journal, 112(4), 330–332.PubMed
67.
Zurück zum Zitat Masuda, A., Nakamura, K., Izutsu, K., Igarashi, K., Ohkawa, R., Jona, M., Higashi, K., Yokota, H., Okudaira, S., Kishimoto, T., Watanabe, T., Koike, Y., Ikeda, H., Kozai, Y., Kurokawa, M., Aoki, J., & Yatomi, Y. (2008). Serum autotaxin measurement in haematological malignancies: a promising marker for follicular lymphoma. British Journal of Haematology, 143(1), 60–70. https://doi.org/10.1111/j.1365-2141.2008.07325.x.PubMedCrossRef Masuda, A., Nakamura, K., Izutsu, K., Igarashi, K., Ohkawa, R., Jona, M., Higashi, K., Yokota, H., Okudaira, S., Kishimoto, T., Watanabe, T., Koike, Y., Ikeda, H., Kozai, Y., Kurokawa, M., Aoki, J., & Yatomi, Y. (2008). Serum autotaxin measurement in haematological malignancies: a promising marker for follicular lymphoma. British Journal of Haematology, 143(1), 60–70. https://​doi.​org/​10.​1111/​j.​1365-2141.​2008.​07325.​x.PubMedCrossRef
75.
Zurück zum Zitat Benesch, M. G., Tang, X., Dewald, J., Dong, W. F., Mackey, J. R., Hemmings, D. G., et al. (2015). Tumor-induced inflammation in mammary adipose tissue stimulates a vicious cycle of autotaxin expression and breast cancer progression. The FASEB Journal, 29(9), 3990–4000. https://doi.org/10.1096/fj.15-274480.PubMedCrossRef Benesch, M. G., Tang, X., Dewald, J., Dong, W. F., Mackey, J. R., Hemmings, D. G., et al. (2015). Tumor-induced inflammation in mammary adipose tissue stimulates a vicious cycle of autotaxin expression and breast cancer progression. The FASEB Journal, 29(9), 3990–4000. https://​doi.​org/​10.​1096/​fj.​15-274480.PubMedCrossRef
76.
Zurück zum Zitat Tager, A. M., LaCamera, P., Shea, B. S., Campanella, G. S., Selman, M., Zhao, Z., Polosukhin, V., Wain, J., Karimi-Shah, B. A., Kim, N. D., Hart, W. K., Pardo, A., Blackwell, T. S., Xu, Y., Chun, J., & Luster, A. D. (2008). The lysophosphatidic acid receptor LPA1 links pulmonary fibrosis to lung injury by mediating fibroblast recruitment and vascular leak. Nature Medicine, 14(1), 45–54. https://doi.org/10.1038/nm1685.PubMedCrossRef Tager, A. M., LaCamera, P., Shea, B. S., Campanella, G. S., Selman, M., Zhao, Z., Polosukhin, V., Wain, J., Karimi-Shah, B. A., Kim, N. D., Hart, W. K., Pardo, A., Blackwell, T. S., Xu, Y., Chun, J., & Luster, A. D. (2008). The lysophosphatidic acid receptor LPA1 links pulmonary fibrosis to lung injury by mediating fibroblast recruitment and vascular leak. Nature Medicine, 14(1), 45–54. https://​doi.​org/​10.​1038/​nm1685.PubMedCrossRef
78.
Zurück zum Zitat Kanehira, M., Fujiwara, T., Nakajima, S., Okitsu, Y., Onishi, Y., Fukuhara, N., Ichinohasama, R., Okada, Y., & Harigae, H. (2017). An lysophosphatidic acid receptors 1 and 3 Axis governs cellular senescence of mesenchymal stromal cells and promotes growth and vascularization of multiple myeloma. Stem Cells, 35(3), 739–753. https://doi.org/10.1002/stem.2499. PubMedCrossRef Kanehira, M., Fujiwara, T., Nakajima, S., Okitsu, Y., Onishi, Y., Fukuhara, N., Ichinohasama, R., Okada, Y., & Harigae, H. (2017). An lysophosphatidic acid receptors 1 and 3 Axis governs cellular senescence of mesenchymal stromal cells and promotes growth and vascularization of multiple myeloma. Stem Cells, 35(3), 739–753. https://​doi.​org/​10.​1002/​stem.​2499.​ PubMedCrossRef
79.
Zurück zum Zitat Wu, X. B., Liu, Y., Wang, G. H., Xu, X., Cai, Y., Wang, H. Y., Li, Y. Q., Meng, H. F., Dai, F., & Jin, J. D. (2016). Mesenchymal stem cells promote colorectal cancer progression through AMPK/mTOR-mediated NF-kappa B activation. Scientific Reports, 6. https://doi.org/10.1038/srep21420. Wu, X. B., Liu, Y., Wang, G. H., Xu, X., Cai, Y., Wang, H. Y., Li, Y. Q., Meng, H. F., Dai, F., & Jin, J. D. (2016). Mesenchymal stem cells promote colorectal cancer progression through AMPK/mTOR-mediated NF-kappa B activation. Scientific Reports, 6. https://​doi.​org/​10.​1038/​srep21420.
81.
Zurück zum Zitat Jeon, E. S., Moon, H. J., Lee, M. J., Song, H. Y., Kim, Y. M., Cho, M., Suh, D. S., Yoon, M. S., Chang, C. L., Jung, J. S., & Kim, J. H. (2008). Cancer-derived lysophosphatidic acid stimulates differentiation of human mesenchymal stem cells to myofibroblast-like cells. Stem Cells, 26(3), 789–797. https://doi.org/10.1634/stemcells.2007-0742.PubMedCrossRef Jeon, E. S., Moon, H. J., Lee, M. J., Song, H. Y., Kim, Y. M., Cho, M., Suh, D. S., Yoon, M. S., Chang, C. L., Jung, J. S., & Kim, J. H. (2008). Cancer-derived lysophosphatidic acid stimulates differentiation of human mesenchymal stem cells to myofibroblast-like cells. Stem Cells, 26(3), 789–797. https://​doi.​org/​10.​1634/​stemcells.​2007-0742.PubMedCrossRef
82.
Zurück zum Zitat Jeon, E. S., Heo, S. C., Lee, I. H., Choi, Y. J., Park, J. H., Choi, K. U., Park, D. Y., Suh, D. S., Yoon, M. S., & Kim, J. H. (2010). Ovarian cancer-derived lysophosphatidic acid stimulates secretion of VEGF and stromal cell-derived factor-1 alpha from human mesenchymal stem cells. Experimental & Molecular Medicine, 42(4), 280–293. https://doi.org/10.3858/emm.2010.42.4.027.CrossRef Jeon, E. S., Heo, S. C., Lee, I. H., Choi, Y. J., Park, J. H., Choi, K. U., Park, D. Y., Suh, D. S., Yoon, M. S., & Kim, J. H. (2010). Ovarian cancer-derived lysophosphatidic acid stimulates secretion of VEGF and stromal cell-derived factor-1 alpha from human mesenchymal stem cells. Experimental & Molecular Medicine, 42(4), 280–293. https://​doi.​org/​10.​3858/​emm.​2010.​42.​4.​027.CrossRef
83.
Zurück zum Zitat Heo, S. C., Lee, K. O., Shin, S. H., Kwon, Y. W., Kim, Y. M., Lee, C. H., Kim, Y. D., Lee, M. K., Yoon, M. S., & Kim, J. H. (2011). Periostin mediates human adipose tissue-derived mesenchymal stem cell-stimulated tumor growth in a xenograft lung adenocarcinoma model. Biochimica et Biophysica Acta, 1813(12), 2061–2070. https://doi.org/10.1016/j.bbamcr.2011.08.004.PubMedCrossRef Heo, S. C., Lee, K. O., Shin, S. H., Kwon, Y. W., Kim, Y. M., Lee, C. H., Kim, Y. D., Lee, M. K., Yoon, M. S., & Kim, J. H. (2011). Periostin mediates human adipose tissue-derived mesenchymal stem cell-stimulated tumor growth in a xenograft lung adenocarcinoma model. Biochimica et Biophysica Acta, 1813(12), 2061–2070. https://​doi.​org/​10.​1016/​j.​bbamcr.​2011.​08.​004.PubMedCrossRef
84.
Zurück zum Zitat Shin, S. H., Kim, J., Heo, S. C., Kwon, Y. W., Kim, Y. M., Kim, I. S., Lee, T. G., & Kim, J. H. (2012). Proteomic identification of Betaig-h3 as a lysophosphatidic acid-induced secreted protein of human mesenchymal stem cells: paracrine activation of A549 lung adenocarcinoma cells by Betaig-h3. Molecular & Cellular Proteomics, 11(2), M111.012385. https://doi.org/10.1074/mcp.M111.012385.CrossRef Shin, S. H., Kim, J., Heo, S. C., Kwon, Y. W., Kim, Y. M., Kim, I. S., Lee, T. G., & Kim, J. H. (2012). Proteomic identification of Betaig-h3 as a lysophosphatidic acid-induced secreted protein of human mesenchymal stem cells: paracrine activation of A549 lung adenocarcinoma cells by Betaig-h3. Molecular & Cellular Proteomics, 11(2), M111.012385. https://​doi.​org/​10.​1074/​mcp.​M111.​012385.CrossRef
89.
Zurück zum Zitat Choi, K. U., Yun, J. S., Lee, I. H., Heo, S. C., Shin, S. H., Jeon, E. S., Choi, Y. J., Suh, D. S., Yoon, M. S., & Kim, J. H. (2011). Lysophosphatidic acid-induced expression of periostin in stromal cells: prognoistic relevance of periostin expression in epithelial ovarian cancer. International Journal of Cancer, 128(2), 332–342. https://doi.org/10.1002/ijc.25341.PubMedCrossRef Choi, K. U., Yun, J. S., Lee, I. H., Heo, S. C., Shin, S. H., Jeon, E. S., Choi, Y. J., Suh, D. S., Yoon, M. S., & Kim, J. H. (2011). Lysophosphatidic acid-induced expression of periostin in stromal cells: prognoistic relevance of periostin expression in epithelial ovarian cancer. International Journal of Cancer, 128(2), 332–342. https://​doi.​org/​10.​1002/​ijc.​25341.PubMedCrossRef
92.
93.
Zurück zum Zitat Bao, S., Ouyang, G., Bai, X., Huang, Z., Ma, C., Liu, M., Shao, R., Anderson, R. M., Rich, J. N., & Wang, X. F. (2004). Periostin potently promotes metastatic growth of colon cancer by augmenting cell survival via the Akt/PKB pathway. Cancer Cell, 5(4), 329–339.PubMedCrossRef Bao, S., Ouyang, G., Bai, X., Huang, Z., Ma, C., Liu, M., Shao, R., Anderson, R. M., Rich, J. N., & Wang, X. F. (2004). Periostin potently promotes metastatic growth of colon cancer by augmenting cell survival via the Akt/PKB pathway. Cancer Cell, 5(4), 329–339.PubMedCrossRef
96.
102.
Zurück zum Zitat Ferry, G., Tellier, E., Try, A., Gres, S., Naime, I., Simon, M. F., et al. (2003). Autotaxin is released from adipocytes, catalyzes lysophosphatidic acid synthesis, and activates preadipocyte proliferation - up-regulated expression with adipocyte differentiation and obesity. The Journal of Biological Chemistry, 278(20), 18162–18169. https://doi.org/10.1074/jbc.M301158200.PubMedPubMedCentralCrossRef Ferry, G., Tellier, E., Try, A., Gres, S., Naime, I., Simon, M. F., et al. (2003). Autotaxin is released from adipocytes, catalyzes lysophosphatidic acid synthesis, and activates preadipocyte proliferation - up-regulated expression with adipocyte differentiation and obesity. The Journal of Biological Chemistry, 278(20), 18162–18169. https://​doi.​org/​10.​1074/​jbc.​M301158200.PubMedPubMedCentralCrossRef
103.
Zurück zum Zitat Nishimura, S., Nagasaki, M., Okudaira, S., Aoki, J., Ohmori, T., Ohkawa, R., Nakamura, K., Igarashi, K., Yamashita, H., Eto, K., Uno, K., Hayashi, N., Kadowaki, T., Komuro, I., Yatomi, Y., & Nagai, R. (2014). ENPP2 contributes to adipose tissue expansion and insulin resistance in diet-induced obesity. Diabetes, 63(12), 4154–4164. https://doi.org/10.2337/db13-1694.PubMedCrossRef Nishimura, S., Nagasaki, M., Okudaira, S., Aoki, J., Ohmori, T., Ohkawa, R., Nakamura, K., Igarashi, K., Yamashita, H., Eto, K., Uno, K., Hayashi, N., Kadowaki, T., Komuro, I., Yatomi, Y., & Nagai, R. (2014). ENPP2 contributes to adipose tissue expansion and insulin resistance in diet-induced obesity. Diabetes, 63(12), 4154–4164. https://​doi.​org/​10.​2337/​db13-1694.PubMedCrossRef
105.
Zurück zum Zitat Yamada, T., Sato, K., Komachi, M., Malchinkhuu, E., Tobo, M., Kimura, T., Kuwabara, A., Yanagita, Y., Ikeya, T., Tanahashi, Y., Ogawa, T., Ohwada, S., Morishita, Y., Ohta, H., Im, D. S., Tamoto, K., Tomura, H., & Okajima, F. (2004). Lysophosphatidic acid (LPA) in malignant ascites stimulates motility of human pancreatic cancer cells through LPA1. The Journal of Biological Chemistry, 279(8), 6595–6605. https://doi.org/10.1074/jbc.M308133200.PubMedCrossRef Yamada, T., Sato, K., Komachi, M., Malchinkhuu, E., Tobo, M., Kimura, T., Kuwabara, A., Yanagita, Y., Ikeya, T., Tanahashi, Y., Ogawa, T., Ohwada, S., Morishita, Y., Ohta, H., Im, D. S., Tamoto, K., Tomura, H., & Okajima, F. (2004). Lysophosphatidic acid (LPA) in malignant ascites stimulates motility of human pancreatic cancer cells through LPA1. The Journal of Biological Chemistry, 279(8), 6595–6605. https://​doi.​org/​10.​1074/​jbc.​M308133200.PubMedCrossRef
107.
Zurück zum Zitat North, E. J., Howard, A. L., Wanjala, I. W., Pham, T. C. T., Baker, D. L., & Parrill, A. L. (2010). Pharmacophore development and application toward the identification of novel, small-molecule Autotaxin inhibitors. Journal of Medicinal Chemistry, 53(8), 3095–3105. https://doi.org/10.1021/jm901718z.PubMedCrossRef North, E. J., Howard, A. L., Wanjala, I. W., Pham, T. C. T., Baker, D. L., & Parrill, A. L. (2010). Pharmacophore development and application toward the identification of novel, small-molecule Autotaxin inhibitors. Journal of Medicinal Chemistry, 53(8), 3095–3105. https://​doi.​org/​10.​1021/​jm901718z.PubMedCrossRef
108.
Zurück zum Zitat Gierse, J., Thorarensen, A., Beltey, K., Bradshaw-Pierce, E., Cortes-Burgos, L., Hall, T., Johnston, A., Murphy, M., Nemirovskiy, O., Ogawa, S., Pegg, L., Pelc, M., Prinsen, M., Schnute, M., Wendling, J., Wene, S., Weinberg, R., Wittwer, A., Zweifel, B., & Masferrer, J. (2010). A novel Autotaxin inhibitor reduces lysophosphatidic acid levels in plasma and the site of inflammation. The Journal of Pharmacology and Experimental Therapeutics, 334(1), 310–317. https://doi.org/10.1124/jpet.110.165845.PubMedCrossRef Gierse, J., Thorarensen, A., Beltey, K., Bradshaw-Pierce, E., Cortes-Burgos, L., Hall, T., Johnston, A., Murphy, M., Nemirovskiy, O., Ogawa, S., Pegg, L., Pelc, M., Prinsen, M., Schnute, M., Wendling, J., Wene, S., Weinberg, R., Wittwer, A., Zweifel, B., & Masferrer, J. (2010). A novel Autotaxin inhibitor reduces lysophosphatidic acid levels in plasma and the site of inflammation. The Journal of Pharmacology and Experimental Therapeutics, 334(1), 310–317. https://​doi.​org/​10.​1124/​jpet.​110.​165845.PubMedCrossRef
111.
Zurück zum Zitat Hirane, M., Ishii, S., Tomimatsu, A., Fukushima, K., Takahashi, K., Fukushima, N., Honoki, K., & Tsujiuchi, T. (2016). Different induction of LPA receptors by chemical liver carcinogens regulates cellular functions of liver epithelial WB-F344 cells. Molecular Carcinogenesis, 55(11), 1573–1583. https://doi.org/10.1002/mc.22410.PubMedCrossRef Hirane, M., Ishii, S., Tomimatsu, A., Fukushima, K., Takahashi, K., Fukushima, N., Honoki, K., & Tsujiuchi, T. (2016). Different induction of LPA receptors by chemical liver carcinogens regulates cellular functions of liver epithelial WB-F344 cells. Molecular Carcinogenesis, 55(11), 1573–1583. https://​doi.​org/​10.​1002/​mc.​22410.PubMedCrossRef
112.
Metadaten
Titel
Role of autotaxin in cancer stem cells
verfasst von
Dongjun Lee
Dong-Soo Suh
Sue Chin Lee
Gabor J. Tigyi
Jae Ho Kim
Publikationsdatum
20.06.2018
Verlag
Springer US
Erschienen in
Cancer and Metastasis Reviews / Ausgabe 2-3/2018
Print ISSN: 0167-7659
Elektronische ISSN: 1573-7233
DOI
https://doi.org/10.1007/s10555-018-9745-x

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