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Cancer and Metastasis Reviews

, Volume 37, Issue 2–3, pp 509–518 | Cite as

Role of autotaxin in cancer stem cells

  • Dongjun Lee
  • Dong-Soo Suh
  • Sue Chin Lee
  • Gabor J. Tigyi
  • Jae Ho Kim
Article

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.

Keywords

Lysophosphatidic acid Lysophosphatidic acid receptor Autotaxin Cancer stem cells 

Abbreviations

ATX

Autotaxin

CSCs

Cancer stem cells

LPA

Lysophosphatidic acid

Notes

Acknowledgments

This work was supported by the MRC program (NRF-2015R1A5A2009656 to J.K.), the National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIT) (NRF-2018R1C1B6001290 to D.L.; NRF-2016R1D1A1B03935769 to D.S.), the National Cancer Institute of the USA (CA092160 to G.T.), and the Korea Health Technology R&D Project, Ministry of Health and Welfare (HI17C1635 to J.K.).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    Visvader, J. E., & Lindeman, G. J. (2008). Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nature Reviews. Cancer, 8(10), 755–768.  https://doi.org/10.1038/nrc2499.PubMedCrossRefGoogle Scholar
  2. 2.
    Lapidot, T., Sirard, C., Vormoor, J., Murdoch, B., Hoang, T., Cacerescortes, J., et al. (1994). A cell initiating human acute myeloid-leukemia after transplantation into Scid mice. Nature, 367(6464), 645–648.  https://doi.org/10.1038/367645a0.PubMedCrossRefGoogle Scholar
  3. 3.
    Bonnet, D., & Dick, J. E. (1997). Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nature Medicine, 3(7), 730–737.  https://doi.org/10.1038/nm0797-730.PubMedCrossRefGoogle Scholar
  4. 4.
    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.PubMedGoogle Scholar
  5. 5.
    Kreso, A., & Dick, J. E. (2014). Evolution of the cancer stem cell model. Cell Stem Cell, 14(3), 275–291.  https://doi.org/10.1016/j.stem.2014.02.006.PubMedCrossRefGoogle Scholar
  6. 6.
    Al-Hajj, M., Wicha, M. S., Benito-Hernandez, A., Morrison, S. J., & Clarke, M. F. (2003). Prospective identification of tumorigenic breast cancer cells. Proceedings of the National Academy of Sciences of the United States of America, 100(7), 3983–3988.  https://doi.org/10.1073/pnas.0530291100.PubMedPubMedCentralCrossRefGoogle Scholar
  7. 7.
    Collins, A. T., Berry, P. A., Hyde, C., Stower, M. J., & Maitland, N. J. (2005). Prospective identification of tumorigenic prostate cancer stem cells. Cancer Research, 65(23), 10946–10951.  https://doi.org/10.1158/0008-5472.CAN-05-2018.PubMedCrossRefGoogle Scholar
  8. 8.
    Hermann, P. C., Huber, S. L., Herrler, T., Aicher, A., Ellwart, J. W., Guba, M., Bruns, C. J., & Heeschen, C. (2007). Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell, 1(3), 313–323.  https://doi.org/10.1016/j.stem.2007.06.002.PubMedCrossRefGoogle Scholar
  9. 9.
    O'Brien, C. A., Pollett, A., Gallinger, S., & Dick, J. E. (2007). A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature, 445(7123), 106–110.  https://doi.org/10.1038/nature05372.PubMedCrossRefGoogle Scholar
  10. 10.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  11. 11.
    Eramo, A., Lotti, F., Sette, G., Pilozzi, E., Biffoni, M., Di Virgilio, A., et al. (2008). Identification and expansion of the tumorigenic lung cancer stem cell population. Cell Death and Differentiation, 15(3), 504–514.  https://doi.org/10.1038/sj.cdd.4402283.PubMedCrossRefGoogle Scholar
  12. 12.
    Ishizawa, K., Rasheed, Z. A., Karisch, R., Wang, Q., Kowalski, J., Susky, E., Pereira, K., Karamboulas, C., Moghal, N., Rajeshkumar, N. V., Hidalgo, M., Tsao, M., Ailles, L., Waddell, T. K., Maitra, A., Neel, B. G., & Matsui, W. (2010). Tumor-initiating cells are rare in many human tumors. Cell Stem Cell, 7(3), 279–282.  https://doi.org/10.1016/j.stem.2010.08.009.PubMedPubMedCentralCrossRefGoogle Scholar
  13. 13.
    Beck, B., & Blanpain, C. (2013). Unravelling cancer stem cell potential. Nature Reviews. Cancer, 13(10), 727–738.  https://doi.org/10.1038/nrc3597.PubMedCrossRefGoogle Scholar
  14. 14.
    Morrison, R., Schleicher, S. M., Sun, Y., Niermann, K. J., Kim, S., Spratt, D. E., Chung, C. H., & Lu, B. (2011). Targeting the mechanisms of resistance to chemotherapy and radiotherapy with the cancer stem cell hypothesis. Journal of Oncology, 2011, 941876.  https://doi.org/10.1155/2011/941876.PubMedCrossRefGoogle Scholar
  15. 15.
    Wang, Y. H., Israelsen, W. J., Lee, D., Yu, V. W., Jeanson, N. T., Clish, C. B., et al. (2014). Cell-state-specific metabolic dependency in hematopoiesis and leukemogenesis. Cell, 158(6), 1309–1323.  https://doi.org/10.1016/j.cell.2014.07.048.PubMedPubMedCentralCrossRefGoogle Scholar
  16. 16.
    Warburg, O. (1956). On the origin of cancer cells. Science, 123(3191), 309–314.PubMedCrossRefGoogle Scholar
  17. 17.
    Wang, Y. H., & Scadden, D. T. (2015). Harnessing the apoptotic programs in cancer stem-like cells. EMBO Reports, 16(9), 1084–1098.  https://doi.org/10.15252/embr.201439675.PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    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.CrossRefGoogle Scholar
  19. 19.
    Alvero, A. B., Montagna, M. K., Holmberg, J. C., Craveiro, V., Brown, D., & Mor, G. (2011). Targeting the mitochondria activates two independent cell death pathways in ovarian Cancer stem cells. Molecular Cancer Therapeutics, 10(8), 1385–1393.  https://doi.org/10.1158/1535-7163.Mct-11-0023.PubMedPubMedCentralCrossRefGoogle Scholar
  20. 20.
    Leal, J. A., & Lleonart, M. E. (2013). MicroRNAs and cancer stem cells: therapeutic approaches and future perspectives. Cancer Letters, 338(1), 174–183.  https://doi.org/10.1016/j.canlet.2012.04.020.PubMedCrossRefGoogle Scholar
  21. 21.
    Yu, F., Yao, H., Zhu, P., Zhang, X., Pan, Q., Gong, C., Huang, Y., Hu, X., Su, F., Lieberman, J., & Song, E. (2007). Let-7 regulates self renewal and tumorigenicity of breast cancer cells. Cell, 131(6), 1109–1123.  https://doi.org/10.1016/j.cell.2007.10.054.PubMedCrossRefGoogle Scholar
  22. 22.
    Kumar, M. S., Erkeland, S. J., Pester, R. E., Chen, C. Y., Ebert, M. S., Sharp, P. A., & Jacks, T. (2008). Suppression of non-small cell lung tumor development by the let-7 microRNA family. Proceedings of the National Academy of Sciences of the United States of America, 105(10), 3903–3908.  https://doi.org/10.1073/pnas.0712321105.PubMedPubMedCentralCrossRefGoogle Scholar
  23. 23.
    Huynh, C., Segura, M. F., Gaziel-Sovran, A., Menendez, S., Darvishian, F., Chiriboga, L., Levin, B., Meruelo, D., Osman, I., Zavadil, J., Marcusson, E. G., & Hernando, E. (2011). Efficient in vivo microRNA targeting of liver metastasis. Oncogene, 30(12), 1481–1488.  https://doi.org/10.1038/onc.2010.523.PubMedCrossRefGoogle Scholar
  24. 24.
    Valdes-Rives, S. A., & Gonzalez-Arenas, A. (2017). Autotaxin-lysophosphatidic acid: from inflammation to Cancer development. Mediators of Inflammation, 2017, 9173090–9173015.  https://doi.org/10.1155/2017/9173090.PubMedPubMedCentralCrossRefGoogle Scholar
  25. 25.
    Mills, G. B., & Moolenaar, W. H. (2003). The emerging role of lysophosphatidic acid in cancer. Nature Reviews. Cancer, 3(8), 582–591.  https://doi.org/10.1038/nrc1143.PubMedCrossRefGoogle Scholar
  26. 26.
    van Meeteren, L. A., & Moolenaar, W. H. (2007). Regulation and biological activities of the autotaxin-LPA axis. Progress in Lipid Research, 46(2), 145–160.  https://doi.org/10.1016/j.plipres.2007.02.001.PubMedCrossRefGoogle Scholar
  27. 27.
    Yung, Y. C., Stoddard, N. C., & Chun, J. (2014). LPA receptor signaling: pharmacology, physiology, and pathophysiology. Journal of Lipid Research, 55(7), 1192–1214.  https://doi.org/10.1194/jlr.R046458.PubMedPubMedCentralCrossRefGoogle Scholar
  28. 28.
    Leblanc, R., & Peyruchaud, O. (2015). New insights into the autotaxin/LPA axis in cancer development and metastasis. Experimental Cell Research, 333(2), 183–189.  https://doi.org/10.1016/j.yexcr.2014.11.010.PubMedCrossRefGoogle Scholar
  29. 29.
    Jonkers, J., & Moolenaar, W. H. (2009). Mammary tumorigenesis through LPA receptor signaling. Cancer Cell, 15(6), 457–459.  https://doi.org/10.1016/j.ccr.2009.05.003.PubMedCrossRefGoogle Scholar
  30. 30.
    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.PubMedGoogle Scholar
  31. 31.
    Umezu-Goto, M., Kishi, Y., Taira, A., Hama, K., Dohmae, N., Takio, K., Yamori, T., Mills, G. B., Inoue, K., Aoki, J., & Arai, H. (2002). Autotaxin has lysophospholipase D activity leading to tumor cell growth and motility by lysophosphatidic acid production. The Journal of Cell Biology, 158(2), 227–233.  https://doi.org/10.1083/jcb.200204026.PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    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.PubMedCrossRefGoogle Scholar
  33. 33.
    Benesch, M. G. K., Ko, Y. M., McMullen, T. P. W., & Brindley, D. N. (2014). Autotaxin in the crosshairs: Taking aim at cancer and other inflammatory conditions. FEBS Letters, 588(16), 2712–2727.  https://doi.org/10.1016/j.febslet.2014.02.009.PubMedCrossRefGoogle Scholar
  34. 34.
    Barbayianni, E., Kaffe, E., Aidinis, V., & Kokotos, G. (2015). Autotaxin, a secreted lysophospholipase D, as a promising therapeutic target in chronic inflammation and cancer. Progress in Lipid Research, 58, 76–96.  https://doi.org/10.1016/j.plipres.2015.02.001.PubMedCrossRefGoogle Scholar
  35. 35.
    Federico, L., Jeong, K. J., Vellano, C. P., & Mills, G. B. (2016). Autotaxin, a lysophospholipase D with pleomorphic effects in oncogenesis and cancer progression. Journal of Lipid Research, 57(1), 25–35.  https://doi.org/10.1194/jlr.R060020.PubMedPubMedCentralCrossRefGoogle Scholar
  36. 36.
    Kanda, H., Newton, R., Klein, R., Morita, Y., Gunn, M. D., & Rosen, S. D. (2008). Autotaxin, an ectoenzyme that produces lysophosphatidic acid, promotes the entry of lymphocytes into secondary lymphoid organs. Nature Immunology, 9(4), 415–423.  https://doi.org/10.1038/ni1573.PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  38. 38.
    Nakamura, K., Ohkawa, R., Okubo, S., Yokota, H., Ikeda, H., Yatomi, Y., et al. (2009). Autotaxin enzyme immunoassay in human cerebrospinal fluid samples. Clinica Chimica Acta, 405(1–2), 160–162.  https://doi.org/10.1016/j.cca.2009.04.025.CrossRefGoogle Scholar
  39. 39.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  40. 40.
    Koike, S., Keino-Masu, K., & Masu, M. (2010). Deficiency of autotaxin/lysophospholipase D results in head cavity formation in mouse embryos through the LPA receptor-rho-ROCK pathway. Biochemical and Biophysical Research Communications, 400(1), 66–71.  https://doi.org/10.1016/j.bbrc.2010.08.008.PubMedCrossRefGoogle Scholar
  41. 41.
    Moolenaar, W. H., Houben, A. J., Lee, S. J., & van Meeteren, L. A. (2013). Autotaxin in embryonic development. Biochimica et Biophysica Acta, 1831(1), 13–19.  https://doi.org/10.1016/j.bbalip.2012.09.013.PubMedCrossRefGoogle Scholar
  42. 42.
    Sasagawa, T., Okita, M., Murakami, J., Kato, T., & Watanabe, A. (1999). Abnormal serum lysophospholipids in multiple myeloma patients. Lipids, 34(1), 17–21.PubMedCrossRefGoogle Scholar
  43. 43.
    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.PubMedGoogle Scholar
  44. 44.
    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.PubMedCrossRefGoogle Scholar
  45. 45.
    Li, T. T., Alemayehu, M., Aziziyeh, A. I., Pape, C., Pampillo, M., Postovit, L. M., Mills, G. B., Babwah, A. V., & Bhattacharya, M. (2009). Beta-Arrestin/Ral signaling regulates lysophosphatidic acid-mediated migration and invasion of human breast tumor cells. Molecular Cancer Research, 7(7), 1064–1077.  https://doi.org/10.1158/1541-7786.Mcr-08-0578. PubMedCrossRefGoogle Scholar
  46. 46.
    Yang, D. Z., Yang, W. H., Zhang, Q., Hu, Y., Bao, L., & Damirin, A. (2013). Migration of gastric cancer cells in response to lysophosphatidic acid is mediated by LPA receptor 2. Oncology Letters, 5(3), 1048–1052.  https://doi.org/10.3892/ol.2013.1107.PubMedPubMedCentralCrossRefGoogle Scholar
  47. 47.
    Mahanivong, C., Chen, H. M., Yee, S. W., Pan, Z. K., Dong, Z., & Huang, S. (2008). Protein kinase C alpha-CARMA3 signaling axis links Ras to NF-kappa B for lysophosphatidic acid-induced urokinase plasminogen activator expression in ovarian cancer cells. Oncogene, 27(9), 1273–1280.  https://doi.org/10.1038/sj.onc.1210746.PubMedCrossRefGoogle Scholar
  48. 48.
    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.PubMedGoogle Scholar
  49. 49.
    Yu, S., Murph, M. M., Lu, Y., Liu, S., Hall, H. S., Liu, J., Stephens, C., Fang, X., & Mills, G. B. (2008). Lysophosphatidic acid receptors determine tumorigenicity and aggressiveness of ovarian cancer cells. Journal of the National Cancer Institute, 100(22), 1630–1642.  https://doi.org/10.1093/jnci/djn378.PubMedPubMedCentralCrossRefGoogle Scholar
  50. 50.
    Ishii, I., Fukushima, N., Ye, X. Q., & Chun, J. (2004). Lysophospholipid receptors: signaling and biology. Annual Review of Biochemistry, 73, 321–354.  https://doi.org/10.1146/annurev.biochem.73.011303.073731.PubMedCrossRefGoogle Scholar
  51. 51.
    An, S. Z., Bleu, T., Hallmark, O. G., & Goetzl, E. J. (1998). Characterization of a novel subtype of human G protein-coupled receptor for lysophosphatidic acid. The Journal of Biological Chemistry, 273(14), 7906–7910.  https://doi.org/10.1074/jbc.273.14.7906.PubMedCrossRefGoogle Scholar
  52. 52.
    Sun, K., Duan, X. Y., Cai, H., Liu, X. H., Yang, Y., Li, M., et al. (2016). Curcumin inhibits LPA-induced invasion by attenuating RhoA/ROCK/MMPs pathway in MCF7 breast cancer cells. Clinical and Experimental Medicine, 16(1), 37–47.  https://doi.org/10.1007/s10238-015-0336-7.PubMedCrossRefGoogle Scholar
  53. 53.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  54. 54.
    Yang, M., Zhong, W. W., Srivastava, N., Slavin, A., Yang, J. X., Hoey, T., et al. (2005). G protein-coupled lysophosphatidic acid receptors stimulate proliferation of colon cancer cells through the beta-catenin pathway. Proceedings of the National Academy of Sciences of the United States of America, 102(17), 6027–6032.  https://doi.org/10.1073/pnas.0501535102.PubMedPubMedCentralCrossRefGoogle Scholar
  55. 55.
    Brusevold, I. J., Tveteraas, I. H., Aasrum, M., Odegard, J., Sandnes, D. L., & Christoffersen, T. (2014). Role of LPAR3, PKC and EGFR in LPA-induced cell migration in oral squamous carcinoma cells. BMC Cancer, 14.  https://doi.org/10.1186/1471-2407-14-432.
  56. 56.
    Boucharaba, A., Serre, C. M., Gres, S., Saulnier-Blache, J. S., Bordet, J. C., Guglielmi, J., et al. (2004). Platelet-derived lysophosphatidic acid supports the progression of osteolytic bone metastases in breast cancer. The Journal of Clinical Investigation, 114(12), 1714–1725.  https://doi.org/10.1172/JCI22123.PubMedPubMedCentralCrossRefGoogle Scholar
  57. 57.
    Taghavi, P., Verhoeven, E., Jacobs, J. J., Lambooij, J. P., Stortelers, C., Tanger, E., et al. (2008). In vitro genetic screen identifies a cooperative role for LPA signaling and c-Myc in cell transformation. Oncogene, 27(54), 6806–6816.  https://doi.org/10.1038/onc.2008.294.PubMedCrossRefGoogle Scholar
  58. 58.
    Kitayama, J., Shida, D., Sako, A., Ishikawa, M., Hama, K., Aoki, J., Arai, H., & Nagawa, H. (2004). Over-expression of lysophosphatidic acid receptor-2 in human invasive ductal carcinoma. Breast Cancer Research, 6(6), R640–R646.  https://doi.org/10.1186/bcr935.PubMedPubMedCentralCrossRefGoogle Scholar
  59. 59.
    Lin, S., Wang, D., Iyer, S., Ghaleb, A. M., Shim, H., Yang, V. W., Chun, J., & Yun, C. C. (2009). The absence of LPA2 attenuates tumor formation in an experimental model of colitis-associated cancer. Gastroenterology, 136(5), 1711–1720.  https://doi.org/10.1053/j.gastro.2009.01.002.PubMedPubMedCentralCrossRefGoogle Scholar
  60. 60.
    Liu, S., Umezu-Goto, M., Murph, M., Lu, Y., Liu, W., Zhang, F., Yu, S., Stephens, L. C., Cui, X., Murrow, G., Coombes, K., Muller, W., Hung, M. C., Perou, C. M., Lee, A. V., Fang, X., & Mills, G. B. (2009). Expression of autotaxin and lysophosphatidic acid receptors increases mammary tumorigenesis, invasion, and metastases. Cancer Cell, 15(6), 539–550.  https://doi.org/10.1016/j.ccr.2009.03.027.PubMedPubMedCentralCrossRefGoogle Scholar
  61. 61.
    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. PubMedCrossRefGoogle Scholar
  62. 62.
    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.PubMedGoogle Scholar
  63. 63.
    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.PubMedGoogle Scholar
  64. 64.
    Stassar, M. J., Devitt, G., Brosius, M., Rinnab, L., Prang, J., Schradin, T., et al. (2001). Identification of human renal cell carcinoma associated genes by suppression subtractive hybridization. British Journal of Cancer, 85(9), 1372–1382.  https://doi.org/10.1054/bjoc.2001.2074.PubMedPubMedCentralCrossRefGoogle Scholar
  65. 65.
    Kehlen, A., Englert, N., Seifert, A., Klonisch, T., Dralle, H., Langner, E., et al. (2004). Expression, regulation and function of autotaxin in thyroid carcinomas. International Journal of Cancer, 109(6), 833–838.  https://doi.org/10.1002/ijc.20022.PubMedCrossRefGoogle Scholar
  66. 66.
    Hoelzinger, D. B., Mariani, L., Weis, J., Woyke, T., Berens, T. J., McDonough, W. S., Sloan, A., Coons, S. W., & Berens, M. E. (2005). Gene expression profile of glioblastoma multiforme invasive phenotype points to new therapeutic targets. Neoplasia, 7(1), 7–16.  https://doi.org/10.1593/neo.04535.PubMedPubMedCentralCrossRefGoogle Scholar
  67. 67.
    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.PubMedCrossRefGoogle Scholar
  68. 68.
    Nam, S. W., Clair, T., Campo, C. K., Lee, H. Y., Liotta, L. A., & Stracke, M. L. (2000). Autotaxin (ATX), a potent tumor motogen, augments invasive and metastatic potential of ras-transformed cells. Oncogene, 19(2), 241–247.  https://doi.org/10.1038/sj.onc.1203263.PubMedCrossRefGoogle Scholar
  69. 69.
    Banerjee, S., Norman, D. D., Lee, S. C., Parrill, A. L., Pham, T. C., Baker, D. L., et al. (2017). Highly potent non-carboxylic acid Autotaxin inhibitors reduce melanoma metastasis and chemotherapeutic resistance of breast Cancer stem cells. Journal of Medicinal Chemistry, 60(4), 1309–1324.  https://doi.org/10.1021/acs.jmedchem.6b01270.PubMedCrossRefGoogle Scholar
  70. 70.
    Hanahan, D., & Coussens, L. M. (2012). Accessories to the crime: functions of cells recruited to the tumor microenvironment. Cancer Cell, 21(3), 309–322.  https://doi.org/10.1016/j.ccr.2012.02.022.PubMedCrossRefGoogle Scholar
  71. 71.
    Charles, N., Ozawa, T., Squatrito, M., Bleau, A. M., Brennan, C. W., Hambardzumyan, D., & Holland, E. C. (2010). Perivascular nitric oxide activates notch signaling and promotes stem-like character in PDGF-induced glioma cells. Cell Stem Cell, 6(2), 141–152.  https://doi.org/10.1016/j.stem.2010.01.001.PubMedCrossRefGoogle Scholar
  72. 72.
    Vermeulen, L., Melo, F. D. S. E., van der Heijden, M., Cameron, K., de Jong, J. H., Borovski, T., et al. (2010). Wnt activity defines colon cancer stem cells and is regulated by the microenvironment. Nature Cell Biology, 12(5), 468–U121.  https://doi.org/10.1038/ncb2048. PubMedCrossRefGoogle Scholar
  73. 73.
    Benesch, M. G. K., Yang, Z., Tang, X., Meng, G., & Brindley, D. N. (2017). Lysophosphatidate signaling: the tumor Microenvironment's new nemesis. Trends in Cancer, 3(11), 748–752.  https://doi.org/10.1016/j.trecan.2017.09.004.PubMedCrossRefGoogle Scholar
  74. 74.
    Benesch, M. G., Zhao, Y. Y., Curtis, J. M., McMullen, T. P., & Brindley, D. N. (2015). Regulation of autotaxin expression and secretion by lysophosphatidate and sphingosine 1-phosphate. Journal of Lipid Research, 56(6), 1134–1144.  https://doi.org/10.1194/jlr.M057661.PubMedPubMedCentralCrossRefGoogle Scholar
  75. 75.
    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.PubMedCrossRefGoogle Scholar
  76. 76.
    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.PubMedCrossRefGoogle Scholar
  77. 77.
    Lee, S. C., Fujiwara, Y., & Tigyi, G. J. (2015). Uncovering unique roles of LPA receptors in the tumor microenvironment. Receptors & Clinical Investigation, 2(1).  https://doi.org/10.14800/rci.440.
  78. 78.
    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. PubMedCrossRefGoogle Scholar
  79. 79.
    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.
  80. 80.
    Huang, W. H., Chang, M. C., Tsai, K. S., Hung, M. C., Chen, H. L., & Hung, S. C. (2013). Mesenchymal stem cells promote growth and angiogenesis of tumors in mice. Oncogene, 32(37), 4343–4354.  https://doi.org/10.1038/onc.2012.458.PubMedCrossRefGoogle Scholar
  81. 81.
    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.PubMedCrossRefGoogle Scholar
  82. 82.
    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.CrossRefGoogle Scholar
  83. 83.
    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.PubMedCrossRefGoogle Scholar
  84. 84.
    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.CrossRefGoogle Scholar
  85. 85.
    Kudo, Y., Siriwardena, B. S., Hatano, H., Ogawa, I., & Takata, T. (2007). Periostin: novel diagnostic and therapeutic target for cancer. Histology and Histopathology, 22(10), 1167–1174.  https://doi.org/10.14670/HH-22.1167. PubMedCrossRefGoogle Scholar
  86. 86.
    Mosher, D. F., Johansson, M. W., Gillis, M. E., & Annis, D. S. (2015). Periostin and TGF-beta-induced protein: two peas in a pod? Critical Reviews in Biochemistry and Molecular Biology, 50(5), 427–439.  https://doi.org/10.3109/10409238.2015.1069791. PubMedPubMedCentralCrossRefGoogle Scholar
  87. 87.
    Kim, B. R., Jang, I. H., Shin, S. H., Kwon, Y. W., Heo, S. C., Choi, E. J., Lee, J. S., & Kim, J. H. (2014). Therapeutic angiogenesis in a murine model of limb ischemia by recombinant periostin and its fasciclin I domain. Biochimica et Biophysica Acta, 1842(9), 1324–1332.  https://doi.org/10.1016/j.bbadis.2014.05.004.PubMedCrossRefGoogle Scholar
  88. 88.
    Kim, B. R., Kwon, Y. W., Park, G. T., Choi, E. J., Seo, J. K., Jang, I. H., Kim, S. C., Ko, H. C., Lee, S. C., & Kim, J. H. (2017). Identification of a novel angiogenic peptide from periostin. PLoS One, 12(11), e0187464.  https://doi.org/10.1371/journal.pone.0187464.PubMedPubMedCentralCrossRefGoogle Scholar
  89. 89.
    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.PubMedCrossRefGoogle Scholar
  90. 90.
    Fukushima, N., Kikuchi, Y., Nishiyama, T., Kudo, A., & Fukayama, M. (2008). Periostin deposition in the stroma of invasive and intraductal neoplasms of the pancreas. Modern Pathology, 21(8), 1044–1053.  https://doi.org/10.1038/modpathol.2008.77.PubMedCrossRefGoogle Scholar
  91. 91.
    Kikuchi, Y., Kashima, T. G., Nishiyama, T., Shimazu, K., Morishita, Y., Shimazaki, M., Kii, I., Horie, H., Nagai, H., Kudo, A., & Fukayama, M. (2008). Periostin is expressed in pericryptal fibroblasts and cancer-associated fibroblasts in the colon. The Journal of Histochemistry and Cytochemistry, 56(8), 753–764.  https://doi.org/10.1369/jhc.2008.951061.PubMedPubMedCentralCrossRefGoogle Scholar
  92. 92.
    Soltermann, A., Tischler, V., Arbogast, S., Braun, J., Probst-Hensch, N., Weder, W., Moch, H., & Kristiansen, G. (2008). Prognostic significance of epithelial-mesenchymal and mesenchymal-epithelial transition protein expression in non-small cell lung cancer. Clinical Cancer Research, 14(22), 7430–7437.  https://doi.org/10.1158/1078-0432.CCR-08-0935.PubMedCrossRefGoogle Scholar
  93. 93.
    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.PubMedCrossRefGoogle Scholar
  94. 94.
    Kudo, Y., Ogawa, I., Kitajima, S., Kitagawa, M., Kawai, H., Gaffney, P. M., Miyauchi, M., & Takata, T. (2006). Periostin promotes invasion and anchorage-independent growth in the metastatic process of head and neck cancer. Cancer Research, 66(14), 6928–6935.  https://doi.org/10.1158/0008-5472.CAN-05-4540.PubMedCrossRefGoogle Scholar
  95. 95.
    Shao, R., Bao, S. D., Bai, X. F., Blanchette, C., Anderson, R. M., Dang, T. Y., et al. (2004). Acquired expression of periostin by human breast cancers promotes tumor angiogenesis through up-regulation of vascular endothelial growth factor receptor 2 expression. Molecular and Cellular Biology, 24(9), 3992–4003.  https://doi.org/10.1128/Mcb.24.9.3992-4003.2004.PubMedPubMedCentralCrossRefGoogle Scholar
  96. 96.
    Contie, S., Voorzanger-Rousselot, N., Litvin, J., Clezardin, P., & Garnero, P. (2011). Increased expression and serum levels of the stromal cell-secreted protein periostin in breast cancer bone metastases. International Journal of Cancer, 128(2), 352–360.  https://doi.org/10.1002/ijc.25591.PubMedCrossRefGoogle Scholar
  97. 97.
    Malanchi, I., Santamaria-Martinez, A., Susanto, E., Peng, H., Lehr, H. A., Delaloye, J. F., et al. (2012). Interactions between cancer stem cells and their niche govern metastatic colonization. Nature, 481(7379), 85–U95.  https://doi.org/10.1038/nature10694. CrossRefGoogle Scholar
  98. 98.
    Ptaszynska, M. M., Pendrak, M. L., Stracke, M. L., & Roberts, D. D. (2010). Autotaxin signaling via lysophosphatidic acid receptors contributes to vascular endothelial growth factor-induced endothelial cell migration. Molecular Cancer Research, 8(3), 309–321.  https://doi.org/10.1158/1541-7786.MCR-09-0288.PubMedCrossRefGoogle Scholar
  99. 99.
    Xu, X., & Prestwich, G. D. (2010). Inhibition of tumor growth and angiogenesis by a lysophosphatidic acid antagonist in an engineered three-dimensional lung cancer xenograft model. Cancer, 116(7), 1739–1750.  https://doi.org/10.1002/cncr.24907.PubMedPubMedCentralCrossRefGoogle Scholar
  100. 100.
    Boucher, J., Quilliot, D., Praderes, J. P., Simon, M. F., Gres, S., Guigne, C., et al. (2005). Potential involvement of adipocyte insulin resistance in obesity-associated up-regulation of adipocyte lysophospholipase D/autotaxin expression. Diabetologia, 48(3), 569–577.  https://doi.org/10.1007/s00125-004-1660-8.PubMedPubMedCentralCrossRefGoogle Scholar
  101. 101.
    Dusaulcy, R., Rancoule, C., Gres, S., Wanecq, E., Colom, A., Guigne, C., et al. (2011). Adipose-specific disruption of autotaxin enhances nutritional fattening and reduces plasma lysophosphatidic acid. Journal of Lipid Research, 52(6), 1247–1255.  https://doi.org/10.1194/jlr.M014985.PubMedPubMedCentralCrossRefGoogle Scholar
  102. 102.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  103. 103.
    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.PubMedCrossRefGoogle Scholar
  104. 104.
    Georas, S. N. (2009). Lysophosphatidic acid and autotaxin: emerging roles in innate and adaptive immunity. Immunologic Research, 45(2–3), 229–238.  https://doi.org/10.1007/s12026-009-8104-y.PubMedCrossRefGoogle Scholar
  105. 105.
    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.PubMedCrossRefGoogle Scholar
  106. 106.
    Lou, L. Q., Chen, Y. X., Jin, L. Z., Li, X. F., Tao, X. F., Zhu, J. H., et al. (2013). Enhancement of invasion of hepatocellular carcinoma cells through lysophosphatidic acid receptor. The Journal of International Medical Research, 41(1), 55–63.  https://doi.org/10.1177/0300060512474124.PubMedCrossRefGoogle Scholar
  107. 107.
    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.PubMedCrossRefGoogle Scholar
  108. 108.
    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.PubMedCrossRefGoogle Scholar
  109. 109.
    Bhave, S. R., Dadey, D. Y., Karvas, R. M., Ferraro, D. J., Kotipatruni, R. P., Jaboin, J. J., et al. (2013). Autotaxin inhibition with PF-8380 enhances the Radiosensitivity of human and murine glioblastoma cell lines. Frontiers in Oncology, 3, 236.  https://doi.org/10.3389/fonc.2013.00236.PubMedPubMedCentralCrossRefGoogle Scholar
  110. 110.
    Benesch, M. G., Tang, X., Maeda, T., Ohhata, A., Zhao, Y. Y., Kok, B. P., et al. (2014). Inhibition of autotaxin delays breast tumor growth and lung metastasis in mice. The FASEB Journal, 28(6), 2655–2666.  https://doi.org/10.1096/fj.13-248641.PubMedCrossRefGoogle Scholar
  111. 111.
    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.PubMedCrossRefGoogle Scholar
  112. 112.
    Zhang, H., Xu, X., Gajewiak, J., Tsukahara, R., Fujiwara, Y., Liu, J., Fells, J. I., Perygin, D., Parrill, A. L., Tigyi, G., & Prestwich, G. D. (2009). Dual activity lysophosphatidic acid receptor pan-antagonist/autotaxin inhibitor reduces breast cancer cell migration in vitro and causes tumor regression in vivo. Cancer Research, 69(13), 5441–5449.  https://doi.org/10.1158/0008-5472.CAN-09-0302.PubMedPubMedCentralCrossRefGoogle Scholar
  113. 113.
    Schleicher, S. M., Thotala, D. K., Linkous, A. G., Hu, R., Leahy, K. M., Yazlovitskaya, E. M., & Hallahan, D. E. (2011). Autotaxin and LPA receptors represent potential molecular targets for the radiosensitization of murine glioma through effects on tumor vasculature. PLoS One, 6(7), e22182.  https://doi.org/10.1371/journal.pone.0022182.PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Dongjun Lee
    • 1
  • Dong-Soo Suh
    • 2
  • Sue Chin Lee
    • 3
  • Gabor J. Tigyi
    • 3
  • Jae Ho Kim
    • 4
  1. 1.Department of Medical SciencePusan National University School of MedicineYangsanSouth Korea
  2. 2.Department of Obstetrics and GynecologyPusan National University School of MedicineYangsanSouth Korea
  3. 3.Department of PhysiologyUniversity of Tennessee Health Science CenterMemphisUSA
  4. 4.Department of PhysiologyPusan National University School of MedicineYangsanRepublic of Korea

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