Bioactive Phospholipids Enhance Migration and Adhesion of Human Leukemic Cells by Inhibiting Heme Oxygenase 1 (HO-1) and Inducible Nitric Oxygenase Synthase (iNOS) in a p38 MAPK-Dependent Manner

Proia, R. L., & Hla, T. (2015). Emerging biology of sphingosine-1-phosphate: its role in pathogenesis and therapy. The Journal of Clinical Investigation, 125, 1379–1387. Schneider, G., Bryndza, E., Abdel-Latif, A., Ratajczak, J., Maj, M., Tarnowski, M., Klyachkin, Y. M., Houghton, P., Morris, A. J., Vater, A., Klussmann, S., Kucia, M., & Ratajczak, M. Z. (2013). Bioactive lipids S1P and C1P are prometastatic factors in human rhabdomyosarcoma, and their tissue levels increase in response to radio/chemotherapy. Molecular Cancer Research, 11, 793–807. Rivera, I. G., Ordonez, M., Presa, N., Gangoiti, P., Gomez-Larrauri, A., Trueba, M., Fox, T., Kester, M., & Gomez-Munoz, A. (2016). Ceramide 1-phosphate regulates cell migration and invasion of human pancreatic cancer cells. Biochemical Pharmacology, 102, 107–119. Ratajczak, M. Z., Suszynska, M., Borkowska, S., Ratajczak, J., & Schneider, G. (2014). The role of sphingosine-1 phosphate and ceramide-1 phosphate in trafficking of normal stem cells and cancer cells. Expert Opinion on Therapeutic Targets, 18, 95–107. Ratajczak, M. Z., Lee, H., Wysoczynski, M., Wan, W., Marlicz, W., Laughlin, M. J., Kucia, M., Janowska-Wieczorek, A., & Ratajczak, J. (2010). Novel insight into stem cell mobilization-plasma sphingosine-1-phosphate is a major chemoattractant that directs the egress of hematopoietic stem progenitor cells from the bone marrow and its level in peripheral blood increases during mobilization due to activation of complement cascade/membrane attack complex. Leukemia, 24, 976–985. Kim, C., Schneider, G., Abdel-Latif, A., Mierzejewska, K., Sunkara, M., Borkowska, S., Ratajczak, J., Morris, A. J., Kucia, M., & Ratajczak, M. Z. (2013). Ceramide-1-phosphate regulates migration of multipotent stromal cells and endothelial progenitor cells--implications for tissue regeneration. Stem Cells, 31, 500–510. Karapetyan, A. V., Klyachkin, Y. M., Selim, S., Sunkara, M., Ziada, K. M., Cohen, D. A., Zuba-Surma, E. K., Ratajczak, J., Smyth, S. S., Ratajczak, M. Z., Morris, A. J., & Abdel-Latif, A. (2013). Bioactive lipids and cationic antimicrobial peptides as new potential regulators for trafficking of bone marrow-derived stem cells in patients with acute myocardial infarction. Stem Cells and Development, 22, 1645–1656. Schneider, G., Sellers, Z. P., Abdel-Latif, A., Morris, A. J., & Ratajczak, M. Z. (2014). Bioactive lipids, LPC and LPA, are novel prometastatic factors and their tissue levels increase in response to radio/chemotherapy. Molecular Cancer Research, 12, 1560–1573. Pappu, R., Schwab, S. R., Cornelissen, I., Pereira, J. P., Regard, J. B., Xu, Y., Camerer, E., Zheng, Y. W., Huang, Y., Cyster, J. G., & Coughlin, S. R. (2007). Promotion of lymphocyte egress into blood and lymph by distinct sources of sphingosine-1-phosphate. Science, 316, 295–298. 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, 227–233. 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, 39436–39442. Huang, W. R., Wang, L. S., Wang, H., Duan, H. F., Li, Q. F., Gao, C. J., & Da, W. M. (2008). SphK-1/S1P signal pathway in CML cells. Zhongguo Shi Yan Xue Ye Xue Za Zhi, 16, 730–733. Powell, J. A., Lewis, A. C., Zhu, W., Toubia, J., Pitman, M. R., Wallington-Beddoe, C. T., Moretti, P. A., Iarossi, D., Samaraweera, S. E., Cummings, N., Ramshaw, H. S., Thomas, D., & Wei, A. H. (2017). Targeting sphingosine kinase 1 induces MCL1-dependent cell death in acute myeloid leukemia. Blood, 129, 771–782. Wallington-Beddoe, C. T., Powell, J. A., Tong, D., Pitson, S. M., Bradstock, K. F., & Bendall, L. J. (2014). Sphingosine kinase 2 promotes acute lymphoblastic leukemia by enhancing MYC expression. Cancer Research, 74, 2803–2815. Xu, X. Q., Huang, C. M., Zhang, Y. F., Chen, L., Cheng, H., & Wang, J. M. (2016). S1PR1 mediates antiapoptotic/proproliferative processes in human acute myeloid leukemia cells. Molecular Medicine Reports, 14, 3369–3375. Katz, S., Ernst, O., Avni, D., Athamna, M., Philosoph, A., Arana, L., Ouro, A., Hoeferlin, L. A., Meijler, M. M., Chalfant, C. E., Gomez-Munoz, A., & Zor, T. (2016). Exogenous ceramide-1-phosphate (C1P) and phospho-ceramide analogue-1 (PCERA-1) regulate key macrophage activities via distinct receptors. Immunology Letters, 169, 73–81. Adamiak, M., Chelvarajan, L., Lynch, K. R., Santos, W. L., Abdel-Latif, A., & Ratajczak, M. Z. (2017). Mobilization studies in mice deficient in sphingosine kinase 2 support a crucial role of the plasma level of sphingosine-1-phosphate in the egress of hematopoietic stem progenitor cells. Oncotarget, 8, 65588–65600. Evangelisti, C., Evangelisti, C., Buontempo, F., Lonetti, A., Orsini, E., Chiarini, F., Barata, J. T., Pyne, S., Pyne, N. J., & Martelli, A. M. (2016). Therapeutic potential of targeting sphingosine kinases and sphingosine 1-phosphate in hematological malignancies. Leukemia, 30, 2142–2151. Zhong, W., Yi, Q., Xu, B., Li, S., Wang, T., Liu, F., Zhu, B., Hoffmann, P. R., Ji, G., Lei, P., Li, G., Li, J., & Li, J. (2016). ORP4L is essential for T-cell acute lymphoblastic leukemia cell survival. Nature Communications, 7, 12702. Paugh, S. W., Paugh, B. S., Rahmani, M., Kapitonov, D., Almenara, J. A., Kordula, T., Milstien, S., Adams, J. K., Zipkin, R. E., Grant, S., & Spiegel, S. (2008). A selective sphingosine kinase 1 inhibitor integrates multiple molecular therapeutic targets in human leukemia. Blood, 112, 1382–1391. Xu, L., Zhang, Y., Gao, M., Wang, G., & Fu, Y. (2016). Concurrent targeting Akt and sphingosine kinase 1 by A-674563 in acute myeloid leukemia cells. Biochemical and Biophysical Research Communications, 472, 662–668. Yang, L., Weng, W., Sun, Z. X., Fu, X. J., Ma, J., & Zhuang, W. F. (2015). SphK1 inhibitor II (SKI-II) inhibits acute myelogenous leukemia cell growth in vitro and in vivo. Biochemical and Biophysical Research Communications, 460, 903–908. Seitz, G., Boehmler, A. M., Kanz, L., & Mohle, R. (2005). The role of sphingosine 1-phosphate receptors in the trafficking of hematopoietic progenitor cells. Annals of the New York Academy of Sciences, 1044, 84–89. 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., & Chun, J. (2010). LPA receptors: subtypes and biological actions. Annual Review of Pharmacology and Toxicology, 50, 157–186. Yanagida, K., & Ishii, S. (2011). Non-Edg family LPA receptors: the cutting edge of LPA research. Journal of Biochemistry, 150, 223–232. Yung, Y. C., Stoddard, N. C., & Chun, J. (2014). LPA receptor signaling: pharmacology, physiology, and pathophysiology. Journal of Lipid Research, 55, 1192–1214. Khan, S. Y., McLaughlin, N. J., Kelher, M. R., Eckels, P., Gamboni-Robertson, F., Banerjee, A., & Silliman, C. C. (2010). Lysophosphatidylcholines activate G2A inducing G(alphai)(−)(1)−/G(alphaq/)(1)(1)- Ca(2)(+) flux, G(betagamma)-Hck activation and clathrin/beta-arrestin-1/GRK6 recruitment in PMNs. The Biochemical Journal, 432, 35–45. Qiao, J., Huang, F., Naikawadi, R. P., Kim, K. S., Said, T., & Lum, H. (2006). Lysophosphatidylcholine impairs endothelial barrier function through the G protein-coupled receptor GPR4. American Journal of Physiology. Lung Cellular and Molecular Physiology, 291, L91–L101. Allende, M. L., Sasaki, T., Kawai, H., Olivera, A., Mi, Y., van Echten-Deckert, G., Hajdu, R., Rosenbach, M., Keohane, C. A., Mandala, S., Spiegel, S., & Proia, R. L. (2004). Mice deficient in sphingosine kinase 1 are rendered lymphopenic by FTY720. The Journal of Biological Chemistry, 279, 52487–52492. Escalante-Alcalde, D., Hernandez, L., Le Stunff, H., Maeda, R., Lee, H. S., Gang Jr., C., Sciorra, V. A., Daar, I., Spiegel, S., Morris, A. J., & Stewart, C. L. (2003). The lipid phosphatase LPP3 regulates extra-embryonic vasculogenesis and axis patterning. Development, 130, 4623–4637. Ishii, I., Friedman, B., Ye, X., Kawamura, S., McGiffert, C., Contos, J. J., Kingsbury, M. A., Zhang, G., Brown, J. H., & Chun, J. (2001). Selective loss of sphingosine 1-phosphate signaling with no obvious phenotypic abnormality in mice lacking its G protein-coupled receptor, LP(B3)/EDG-3. The Journal of Biological Chemistry, 276, 33697–33704. Liu, Y., Wada, R., Yamashita, T., Mi, Y., Deng, C. X., Hobson, J. P., Rosenfeldt, H. M., Nava, V. E., Chae, S. S., Lee, M. J., Liu, C. H., Hla, T., & Spiegel, S. (2000). Edg-1, the G protein-coupled receptor for sphingosine-1-phosphate, is essential for vascular maturation. The Journal of Clinical Investigation, 106, 951–961. Lorenz, J. N., Arend, L. J., Robitz, R., Paul, R. J., & MacLennan, A. J. (2007). Vascular dysfunction in S1P2 sphingosine 1-phosphate receptor knockout mice. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, 292, R440–R446. Ratajczak, M. Z., Kim, C. H., Abdel-Latif, A., Schneider, G., Kucia, M., Morris, A. J., Laughlin, M. J., & Ratajczak, J. (2012). A novel perspective on stem cell homing and mobilization: review on bioactive lipids as potent chemoattractants and cationic peptides as underappreciated modulators of responsiveness to SDF-1 gradients. Leukemia, 26, 63–72. Abdelbaset-Ismail, A., Borkowska-Rzeszotek, S., Kubis, E., Bujko, K., Brzezniakiewicz-Janus, K., Bolkun, L., Kloczko, J., Moniuszko, M., Basak, G. W., Wiktor-Jedrzejczak, W., & Ratajczak, M. Z. (2017). Activation of the complement cascade enhances motility of leukemic cells by downregulating expression of HO-1. Leukemia, 31, 446–458. Adamiak, M., Moore, J. B., Zhao, J., Abdelbaset-Ismail, A., Grubczak, K., Rzeszotek, S., Wysoczynski, M., & Ratajczak, M. Z. (2016). Downregulation of Heme oxygenase 1 (HO-1) activity in hematopoietic cells enhances their engraftment after transplantation. Cell Transplantation, 25, 1265–1276. Ratajczak, M. Z. (2017). HO-1 inhibits migration of leukemic cells. Oncotarget, 8, 89429–89430. Wysoczynski, M., Ratajczak, J., Pedziwiatr, D., Rokosh, G., Bolli, R., & Ratajczak, M. Z. (2015). Identification of heme oxygenase 1 (HO-1) as a novel negative regulator of mobilization of hematopoietic stem/progenitor cells. Stem Cell Reviews, 11, 110–118. Adamiak, M., Abdelbaset-Ismail, A., JBt, M., Zhao, J., Abdel-Latif, A., Wysoczynski, M., & Ratajczak, M. Z. (2017). Inducible nitric oxide synthase (iNOS) is a novel negative regulator of hematopoietic stem/progenitor cell trafficking. Stem Cell Reviews, 13, 92–103. Vardiman, J. W., Thiele, J., Arber, D. A., Brunning, R. D., Borowitz, M. J., Porwit, A., Harris, N. L., Le Beau, M. M., Hellstrom-Lindberg, E., Tefferi, A., & Bloomfield, C. D. (2009). The 2008 revision of the World Health Organization (WHO) classification of myeloid neoplasms and acute leukemia: Rationale and important changes. Blood, 114, 937–951. Abdelbaset-Ismail, A., Borkowska, S., Janowska-Wieczorek, A., Tonn, T., Rodriguez, C., Moniuszko, M., Bolkun, L., Koloczko, J., Eljaszewicz, A., Ratajczak, J., Ratajczak, M. Z., & Kucia, M. (2016). Novel evidence that pituitary gonadotropins directly stimulate human leukemic cells-studies of myeloid cell lines and primary patient AML and CML cells. Oncotarget, 7, 3033–3046. Adamiak, M., Borkowska, S., Wysoczynski, M., Suszynska, M., Kucia, M., Rokosh, G., Abdel-Latif, A., Ratajczak, J., & Ratajczak, M. Z. (2015). Evidence for the involvement of sphingosine-1-phosphate in the homing and engraftment of hematopoietic stem cells to bone marrow. Oncotarget, 6, 18819–18828. Kim, C. H., Wu, W., Wysoczynski, M., Abdel-Latif, A., Sunkara, M., Morris, A., Kucia, M., Ratajczak, J., & Ratajczak, M. Z. (2012). Conditioning for hematopoietic transplantation activates the complement cascade and induces a proteolytic environment in bone marrow: a novel role for bioactive lipids and soluble C5b-C9 as homing factors. Leukemia, 26, 106–116. Ousman, S. S., & David, S. (2000). Lysophosphatidylcholine induces rapid recruitment and activation of macrophages in the adult mouse spinal cord. Glia, 30, 92–104. Lauber, K., Bohn, E., Krober, S. M., Xiao, Y. J., Blumenthal, S. G., Lindemann, R. K., Marini, P., Wiedig, C., Zobywalski, A., Baksh, S., Xu, Y., Autenrieth, I. B., & Schulze-Osthoff, K. (2003). Apoptotic cells induce migration of phagocytes via caspase-3-mediated release of a lipid attraction signal. Cell, 113, 717–730. Radu, C. G., Yang, L. V., Riedinger, M., Au, M., & Witte, O. N. (2004). T cell chemotaxis to lysophosphatidylcholine through the G2A receptor. Proceedings of the National Academy of Sciences of the United States of America, 101, 245–250. Ortlepp, C., Steudel, C., Heiderich, C., Koch, S., Jacobi, A., Ryser, M., Brenner, S., Bornhauser, M., Brors, B., Hofmann, W. K., Ehninger, G., & Thiede, C. (2013). Autotaxin is expressed in FLT3-ITD positive acute myeloid leukemia and hematopoietic stem cells and promotes cell migration and proliferation. Experimental Hematology, 41, 444–461. Hu, X., Mendoza, F. J., Sun, J., Banerji, V., Johnston, J. B., & Gibson, S. B. (2008). Lysophosphatidic acid (LPA) induces the expression of VEGF leading to protection against apoptosis in B-cell derived malignancies. Cellular Signalling, 20, 1198–1208. Kumar, S. A., Hu, X., Brown, M., Kuschak, B., Hernandez, T. A., Johnston, J. B., & Gibson, S. B. (2009). Lysophosphatidic acid receptor expression in chronic lymphocytic leukemia leads to cell survival mediated though vascular endothelial growth factor expression. Leukemia & Lymphoma, 50, 2038–2048. Chen, H., Shen, Y. F., Gong, F., Yang, G. H., Jiang, Y. Q., & Zhang, R. (2015). Expression of VEGF and its effect on cell proliferation in patients with chronic myeloid leukemia. European Review for Medical and Pharmacological Sciences, 19, 3569–3573. Podar, K., & Anderson, K. C. (2005). The pathophysiologic role of VEGF in hematologic malignancies: Therapeutic implications. Blood, 105, 1383–1395. Budkowska, M., Ostrycharz, E., Wojtowicz, A., Marcinowska, Z., Woźniak, J., Ratajczak, M. Z., & Dołęgowska, B. (2018). A circadian rhythm in both complement Cascade (ComC) activation and Sphingosine-1-phosphate (S1P) levels in human peripheral blood supports a role for the ComC–S1P Axis in circadian changes in the number of stem cells circulating in peripheral blood. Stem Cell Reviews, 14, 677–685. https://doi.org/10.1007/s12015-018-9836-7 2018 Jun 17, [Epub ahead of print]. Bhartiya, D. (2017). Pluripotent stem cells in adult tissues: Struggling to be acknowledged over two decades. Stem Cell Reviews, 13, 713–724. Smadja, D. M. (2017). Bone marrow very small embryonic-like stem cells: new generation of autologous cell therapy soon ready for prime time? Stem Cell Reviews, 13, 198–201. Ratajczak, M. Z. (2017). Why are hematopoietic stem cells so 'sexy'? On a search for developmental explanation. Leukemia, 31(8), 1671–1677. Shaikh, A., Anand, S., Kapoor, S., Ganguly, R., & Bhartiya, D. (2017). Mouse bone marrow VSELs exhibit differentiation into three embryonic germ lineages and germ & hematopoietic cells in culture. Stem Cell Reviews, 13(2), 202–216.