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Mediators of Inflammation
Volume 2015, Article ID 101987, 8 pages
http://dx.doi.org/10.1155/2015/101987
Research Article

The Hen or the Egg: Inflammatory Aspects of Murine MPN Models

1Division of Molecular Hematology, University Hospital Freiburg, Center for Clinical Research, Breisacher Straße 66, 79106 Freiburg, Germany
2Spemann Graduate School of Biology and Medicine (SGBM), University of Freiburg, Albertstraße 19A, 79104 Freiburg, Germany
3Faculty of Biology, University of Freiburg, Schänzlestraße 1, 79104 Freiburg, Germany

Received 30 June 2015; Accepted 16 August 2015

Academic Editor: Vladan P. Čokić

Copyright © 2015 Jonas S. Jutzi and Heike L. Pahl. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. R. Virchow, Archiv für Pathologische Anatomie und Physiologie und für Klinische Medicin, Georg Reimer, Berlin, Germany, 1869.
  2. D. Hanahan and R. A. Weinberg, “Hallmarks of cancer: the next generation,” Cell, vol. 144, no. 5, pp. 646–674, 2011. View at Publisher · View at Google Scholar · View at Scopus
  3. C. Catassi, I. Bearzi, and G. K. T. Holmes, “Association of celiac disease and intestinal lymphomas and other cancers,” Gastroenterology, vol. 128, supplement 1, no. 4, pp. S79–S86, 2005. View at Publisher · View at Google Scholar · View at Scopus
  4. M. Lukas, “Inflammatory bowel disease as a risk factor for colorectal cancer,” Digestive Diseases, vol. 28, no. 4-5, pp. 619–624, 2010. View at Publisher · View at Google Scholar · View at Scopus
  5. Y. Shinomura, K. Kinoshita, S. Tsutsui, and S. Hirota, “Pathophysiology, diagnosis, and treatment of gastrointestinal stromal tumors,” Journal of Gastroenterology, vol. 40, no. 8, pp. 775–780, 2005. View at Publisher · View at Google Scholar · View at Scopus
  6. M. H. G. P. Raaijmakers, S. Mukherjee, S. Guo et al., “Bone progenitor dysfunction induces myelodysplasia and secondary leukaemia,” Nature, vol. 464, no. 7290, pp. 852–857, 2010. View at Publisher · View at Google Scholar · View at Scopus
  7. H. C. Hasselbalch, “Perspectives on chronic inflammation in essential thrombocythemia, polycythemia vera, and myelofibrosis: is chronic inflammation a trigger and driver of clonal evolution and development of accelerated atherosclerosis and second cancer?” Blood, vol. 119, no. 14, pp. 3219–3225, 2012. View at Publisher · View at Google Scholar · View at Scopus
  8. H. C. Hasselbalch, “A role of NF-E2 in chronic inflammation and clonal evolution in essential thrombocythemia, polycythemia vera and myelofibrosis?” Leukemia Research, vol. 38, no. 2, pp. 263–266, 2014. View at Publisher · View at Google Scholar · View at Scopus
  9. S. Y. Kristinsson, M. Björkholm, M. Hultcrantz, Å. R. Derolf, O. Landgren, and L. R. Goldin, “Chronic immune stimulation might act as a trigger for the development of acute myeloid leukemia or myelodysplastic syndromes,” Journal of Clinical Oncology, vol. 29, no. 21, pp. 2897–2903, 2011. View at Publisher · View at Google Scholar · View at Scopus
  10. H. Takizawa, S. Boettcher, and M. G. Manz, “Demand-adapted regulation of early hematopoiesis in infection and inflammation,” Blood, vol. 119, no. 13, pp. 2991–3002, 2012. View at Publisher · View at Google Scholar · View at Scopus
  11. X. Li, K. M. Kolltveit, L. Tronstad, and I. Olsen, “Systemic diseases caused by oral infection,” Clinical Microbiology Reviews, vol. 13, no. 4, pp. 547–558, 2000. View at Publisher · View at Google Scholar · View at Scopus
  12. B. L. Esplin, T. Shimazu, R. S. Welner et al., “Chronic exposure to a TLR ligand injures hematopoietic stem cells,” The Journal of Immunology, vol. 186, no. 9, pp. 5367–5375, 2011. View at Publisher · View at Google Scholar · View at Scopus
  13. K. Sudo, H. Ema, Y. Morita, and H. Nakauchi, “Age-associated characteristics of murine hematopoietic stern cells,” The Journal of Experimental Medicine, vol. 192, no. 9, pp. 1273–1280, 2000. View at Publisher · View at Google Scholar · View at Scopus
  14. S. J. Morrison, A. M. Wandycz, K. Akashi, A. Globerson, and I. L. Weissman, “The aging of hematopoietic stem cells,” Nature Medicine, vol. 2, no. 9, pp. 1011–1016, 1996. View at Publisher · View at Google Scholar · View at Scopus
  15. M. Kim, H.-B. Moon, and G. J. Spangrude, “Major age-related changes of mouse hematopoietic stem/progenitor cells,” Annals of the New York Academy of Sciences, vol. 996, pp. 195–208, 2003. View at Publisher · View at Google Scholar · View at Scopus
  16. R. A. J. Signer, E. Montecino-Rodriguez, O. N. Witte, J. McLaughlin, and K. Dorshkind, “Age-related defects in B lymphopoiesis underlie the myeloid dominance of adult leukemia,” Blood, vol. 110, no. 6, pp. 1831–1839, 2007. View at Publisher · View at Google Scholar · View at Scopus
  17. Y. Lin, S. Chen, and J. Wang, “Critical role of IL-6 in dendritic cell-induced allergic inflammation of asthma,” Journal of Molecular Medicine, 2015. View at Publisher · View at Google Scholar
  18. S. Y. Kristinsson, O. Landgren, J. Samuelsson, M. Björkholm, and L. R. Goldin, “Autoimmunity and the risk of myeloproliferative neoplasms,” Haematologica, vol. 95, no. 7, pp. 1216–1220, 2010. View at Publisher · View at Google Scholar · View at Scopus
  19. G. Barosi, U. Magrini, and R. P. Gale, “Does auto-immunity contribute to anemia in myeloproliferative neoplasms (MPN)-associated myelofibrosis?” Leukemia Research, vol. 34, no. 9, pp. 1119–1120, 2010. View at Publisher · View at Google Scholar · View at Scopus
  20. W. Barcellini, A. Iurlo, T. Radice et al., “Increased prevalence of autoimmune phenomena in myelofibrosis: relationship with clinical and morphological characteristics, and with immunoregulatory cytokine patterns,” Leukemia Research, vol. 37, no. 11, pp. 1509–1515, 2013. View at Publisher · View at Google Scholar · View at Scopus
  21. M.-C. Martyre, H. Magdelenat, M.-C. Bryckaert, C. Laine-Bidron, and F. Calvo, “Increased intraplatelet levels of platelet-derived growth factor and transforming growth factor-β in patients with myelofibrosis with myeloid metaplasia,” British Journal of Haematology, vol. 77, no. 1, pp. 80–86, 1991. View at Publisher · View at Google Scholar · View at Scopus
  22. S. Hermouet, A. Godard, D. Pineau et al., “Abnormal production of interleukin (IL)-11 and IL-8 in polycythaemia vera,” Cytokine, vol. 20, no. 4, pp. 178–183, 2002. View at Publisher · View at Google Scholar · View at Scopus
  23. K. E. Panteli, E. C. Hatzimichael, P. K. Bouranta et al., “Serum interleukin (IL)-1, IL-2, sIL-2Ra, IL-6 and thrombopoietin levels in patients with chronic myeloproliferative diseases,” British Journal of Haematology, vol. 130, no. 5, pp. 709–715, 2005. View at Publisher · View at Google Scholar · View at Scopus
  24. A. Allegra, A. Alonci, G. Bellomo et al., “Evaluation of Interleukin-17 serum levels in patients with chronic myeloproliferative diseases,” Tumori, vol. 95, no. 3, pp. 404–405, 2009. View at Google Scholar · View at Scopus
  25. M. Boissinot, C. Cleyrat, M. Vilaine, Y. Jacques, I. Corre, and S. Hermouet, “Anti-inflammatory cytokines hepatocyte growth factor and interleukin-11 are over-expressed in Polycythemia vera and contribute to the growth of clonal erythroblasts independently of JAK2V617F,” Oncogene, vol. 30, no. 8, pp. 990–1001, 2011. View at Publisher · View at Google Scholar · View at Scopus
  26. A. Tefferi, R. Vaidya, D. Caramazza, C. Finke, T. Lasho, and A. Pardanani, “Circulating interleukin (IL)-8, IL-2R, IL-12, and IL-15 levels are independently prognostic in primary myelofibrosis: a comprehensive cytokine profiling study,” Journal of Clinical Oncology, vol. 29, no. 10, pp. 1356–1363, 2011. View at Publisher · View at Google Scholar · View at Scopus
  27. S. Verstovsek, H. Kantarjian, R. A. Mesa et al., “Safety and efficacy of INCB018424, a JAK1 and JAK2 inhibitor, in myelofibrosis,” The New England Journal of Medicine, vol. 363, no. 12, pp. 1117–1127, 2010. View at Publisher · View at Google Scholar · View at Scopus
  28. A. G. Fleischman, K. J. Aichberger, S. B. Luty et al., “TNFα facilitates clonal expansion of JAK2V617F positive cells in myeloproliferative neoplasms,” Blood, vol. 118, no. 24, pp. 6392–6398, 2011. View at Publisher · View at Google Scholar · View at Scopus
  29. A. M. Vannucchi, L. Bianchi, C. Cellai et al., “Development of myelofibrosis in mice genetically impaired for GATA-1 expression (GATA-1low mice),” Blood, vol. 100, no. 4, pp. 1123–1132, 2002. View at Publisher · View at Google Scholar · View at Scopus
  30. M. Zingariello, F. Martelli, F. Ciaffoni et al., “Characterization of the TGF-β1 signaling abnormalities in the Gata1low mouse model of myelofibrosis,” Blood, vol. 121, no. 17, pp. 3345–3363, 2013. View at Publisher · View at Google Scholar · View at Scopus
  31. H. Chagraoui, E. Komura, M. Tulliez, S. Giraudier, W. Vainchenker, and F. Wendung, “Prominent role of TGF-β1 in thrombopoietin-induced myelofibrosis in mice,” Blood, vol. 100, no. 10, pp. 3495–3503, 2002. View at Publisher · View at Google Scholar · View at Scopus
  32. K. B. Kaufmann, A. Gründer, T. Hadlich et al., “A novel murine model of myeloproliferative disorders generated by overexpression of the transcription factor NF-E2,” Journal of Experimental Medicine, vol. 209, no. 1, pp. 35–50, 2012. View at Publisher · View at Google Scholar · View at Scopus
  33. J. S. Jutzi, R. Bogeska, G. Nikoloski et al., “MPN patients harbor recurrent truncating mutations in transcription factor NF-E2,” Journal of Experimental Medicine, vol. 210, no. 5, pp. 1003–1019, 2013. View at Publisher · View at Google Scholar · View at Scopus
  34. H. Oshima and M. Oshima, “The inflammatory network in the gastrointestinal tumor microenvironment: lessons from mouse models,” Journal of Gastroenterology, vol. 47, no. 2, pp. 97–106, 2012. View at Publisher · View at Google Scholar · View at Scopus
  35. M. Oshima, J. E. Dinchuk, S. L. Kargman et al., “Suppression of intestinal polyposis in ApcΔ716 knockout mice by inhibition of cyclooxygenase 2 (COX-2),” Cell, vol. 87, no. 5, pp. 803–809, 1996. View at Publisher · View at Google Scholar
  36. M. Sonoshita, K. Takaku, N. Sasaki et al., “Acceleration of intestinal polyposis through prostaglandin receptor EP2 in ApcΔ716 knockout mice,” Nature Medicine, vol. 7, no. 9, pp. 1048–1051, 2001. View at Publisher · View at Google Scholar · View at Scopus
  37. M. Nakanishi, D. C. Montrose, P. Clark et al., “Genetic deletion of mPGES-1 suppresses intestinal tumorigenesis,” Cancer Research, vol. 68, no. 9, pp. 3251–3259, 2008. View at Publisher · View at Google Scholar · View at Scopus
  38. S.-J. Myung, R. M. Rerko, M. Yan et al., “15-Hydroxyprostaglandin dehydrogenase is an in vivo suppressor of colon tumorigenesis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 32, pp. 12098–12102, 2006. View at Publisher · View at Google Scholar · View at Scopus
  39. W.-J. Chae, T. F. Gibson, D. Zelterman, L. Hao, O. Henegariu, and A. L. M. Bothwell, “Ablation of IL-17A abrogates progression of spontaneous intestinal tumorigenesis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 12, pp. 5540–5544, 2010. View at Publisher · View at Google Scholar · View at Scopus
  40. S. Grivennikov, E. Karin, J. Terzic et al., “IL-6 and Stat3 are required for survival of intestinal epithelial cells and development of colitis-associated cancer,” Cancer Cell, vol. 15, no. 2, pp. 103–113, 2009. View at Publisher · View at Google Scholar · View at Scopus
  41. B. K. Popivanova, F. I. Kostadinova, K. Furuichi et al., “Blockade of a chemokine, CCL2, reduces chronic colitis-associated carcinogenesis in mice,” Cancer Research, vol. 69, no. 19, pp. 7884–7892, 2009. View at Publisher · View at Google Scholar · View at Scopus
  42. B. K. Popivanova, K. Kitamura, Y. Wu et al., “Blocking TNF-α in mice reduces colorectal carcinogenesis associated with chronic colitis,” The Journal of Clinical Investigation, vol. 118, no. 2, pp. 560–570, 2008. View at Publisher · View at Google Scholar · View at Scopus
  43. M. A. Al-Salihi, A. Terrece Pearman, T. Doan et al., “Transgenic expression of cyclooxygenase-2 in mouse intestine epithelium is insufficient to initiate tumorigenesis but promotes tumor progression,” Cancer Letters, vol. 273, no. 2, pp. 225–232, 2009. View at Publisher · View at Google Scholar · View at Scopus
  44. T.-O. Ishikawa, M. Oshima, and H. R. Herschman, “Cox-2 deletion in myeloid and endothelial cells, but not in epithelial cells, exacerbates murine colitis,” Carcinogenesis, vol. 32, no. 3, pp. 417–426, 2011. View at Publisher · View at Google Scholar · View at Scopus
  45. V. M. Zaleskas, D. S. Krause, K. Lazarides et al., “Molecular pathogenesis and therapy of polycythemia induced in mice by JAK2 V617F,” PLoS ONE, vol. 1, article e18, 2006. View at Publisher · View at Google Scholar · View at Scopus
  46. Y. Pikman, B. H. Lee, T. Mercher et al., “MPLW515L is a novel somatic activating mutation in myelofibrosis with myeloid metaplasia,” PLoS Medicine, vol. 3, no. 7, article e270, 2006. View at Publisher · View at Google Scholar · View at Scopus
  47. C. Marty, C. Lacout, A. Martin et al., “Myeloproliferative neoplasm induced by constitutive expression of JAK2V617F in knock-in mice,” Blood, vol. 116, no. 5, pp. 783–787, 2010. View at Publisher · View at Google Scholar · View at Scopus
  48. R. Tiedt, H. Hao-Shen, M. A. Sobas et al., “Ratio of mutant JAK2-V617F to wild-type Jak2 determines the MPD phenotypes in transgenic mice,” Blood, vol. 111, no. 8, pp. 3931–3940, 2008. View at Publisher · View at Google Scholar · View at Scopus
  49. Z. Li, X. Cai, C.-L. Cai et al., “Deletion of Tet2 in mice leads to dysregulated hematopoietic stem cells and subsequent development of myeloid malignancies,” Blood, vol. 118, no. 17, pp. 4509–4518, 2011. View at Publisher · View at Google Scholar · View at Scopus
  50. S. Hasan, C. Lacout, C. Marty et al., “JAK2V617F expression in mice amplifies early hematopoietic cells and gives them a competitive advantage that is hampered by IFNalpha,” Blood, vol. 122, no. 8, pp. 1464–1477, 2013. View at Publisher · View at Google Scholar · View at Scopus
  51. J. Wang, Z. Li, Y. He et al., “Loss of Asxl1 leads to myelodysplastic syndrome-like disease in mice,” Blood, vol. 123, no. 4, pp. 541–553, 2014. View at Publisher · View at Google Scholar · View at Scopus
  52. T. Muto, G. Sashida, N. Hasegawa et al., “Myelodysplastic syndrome with extramedullary erythroid hyperplasia induced by loss of Tet2 in mice,” Leukemia & Lymphoma, vol. 56, no. 2, pp. 520–523, 2015. View at Publisher · View at Google Scholar
  53. P. S. Goerttler, C. Kreutz, J. Donauer et al., “Gene expression profiling in polycythaemia vera: overexpression of transcription factor NF-E2,” British Journal of Haematology, vol. 129, no. 1, pp. 138–150, 2005. View at Publisher · View at Google Scholar · View at Scopus
  54. W. Wang, S. Schwemmers, E. O. Hexner, and H. L. Pahl, “AML1 is overexpressed in patients with myeloproliferative neoplasms and mediates JAK2V617F-independent overexpression of NF-E2,” Blood, vol. 116, no. 2, pp. 254–266, 2010. View at Publisher · View at Google Scholar · View at Scopus
  55. C. K. Y. Chuen, K. Li, M. Yang et al., “Interleukin-1β up-regulates the expression of thrombopoietin and transcription factors c-Jun, c-Fos, GATA-1, and NF-E2 in megakaryocytic cells,” Journal of Laboratory and Clinical Medicine, vol. 143, no. 2, pp. 75–88, 2004. View at Publisher · View at Google Scholar · View at Scopus
  56. J. Wehrle, T. Seeger, S. Schwemmers, D. Pfeifer, A. Bulashevska, and H. Pahl, “Transcription factor nuclear factor erythroid-2 mediates expression of the cytokine interleukin 8, a known predictor of inferior outcome in patients with myeloproliferative neoplasms,” Haematologica, vol. 98, no. 7, pp. 1073–1080, 2013. View at Publisher · View at Google Scholar
  57. R. Roelz, I. H. Pilz, M. Mutschler, and H. L. Pahl, “Of mice and men: human RNA polymerase III promoter U6 is more efficient than its murine homologue for shRNA expression from a lentiviral vector in both human and murine progenitor cells,” Experimental Hematology, vol. 38, no. 9, pp. 792–797, 2010. View at Publisher · View at Google Scholar · View at Scopus
  58. A. B. Sparks, P. J. Morin, B. Vogelstein, and K. W. Kinzler, “Mutational analysis of the APC/β-catenin/Tcf pathway in colorectal cancer,” Cancer Research, vol. 58, no. 6, pp. 1130–1134, 1998. View at Google Scholar · View at Scopus
  59. J. Groden, A. Thliveris, W. Samowitz et al., “Identification and characterization of the familial adenomatous polyposis coli gene,” Cell, vol. 66, no. 3, pp. 589–600, 1991. View at Publisher · View at Google Scholar · View at Scopus
  60. A. Mullally, S. W. Lane, B. Ball et al., “Physiological Jak2V617F expression causes a lethal myeloproliferative neoplasm with differential effects on hematopoietic stem and progenitor cells,” Cancer Cell, vol. 17, no. 6, pp. 584–596, 2010. View at Publisher · View at Google Scholar · View at Scopus
  61. T.-O. Ishikawa and H. R. Herschman, “Tumor formation in a mouse model of colitis-associated colon cancer does not require COX-1 or COX-2 expression,” Carcinogenesis, vol. 31, no. 4, pp. 729–736, 2010. View at Publisher · View at Google Scholar · View at Scopus
  62. E. Gounaris, S. E. Erdman, C. Restaino et al., “Mast cells are an essential hematopoietic component for polyp development,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 50, pp. 19977–19982, 2007. View at Publisher · View at Google Scholar · View at Scopus
  63. P. Ramos, C. Casu, S. Gardenghi et al., “Macrophages support pathological erythropoiesis in polycythemia vera and beta-thalassemia,” Nature Medicine, vol. 19, no. 4, pp. 437–445, 2013. View at Publisher · View at Google Scholar · View at Scopus
  64. I. Corre-Buscail, D. Pineau, M. Boissinot, and S. Hermouet, “Erythropoietin-independent erythroid colony formation by bone marrow progenitors exposed to interleukin-11 and interleukin-8,” Experimental Hematology, vol. 33, no. 11, pp. 1299–1308, 2005. View at Publisher · View at Google Scholar · View at Scopus
  65. M. Howlett, A. S. Giraud, H. Lescesen et al., “The interleukin-6 family cytokine interleukin-11 regulates homeostatic epithelial cell turnover and promotes gastric tumor development,” Gastroenterology, vol. 136, no. 3, pp. 967.e3–977.e3, 2009. View at Publisher · View at Google Scholar · View at Scopus
  66. S. Hermouet, I. Corre, and E. Lippert, “Interleukin-8 and other agonists of gi2 proteins: autocrine paracrine growth factors for human hematopoietic progenitors acting in synergy with colony stimulating factors,” Leukemia and Lymphoma, vol. 38, no. 1-2, pp. 39–48, 2000. View at Google Scholar · View at Scopus
  67. A. M. Vannucchi, A. Pancrazzi, P. Guglielmelli et al., “Abnormalities of GATA-1 in megakaryocytes from patients with idiopathic myelofibrosis,” The American Journal of Pathology, vol. 167, no. 3, pp. 849–858, 2005. View at Publisher · View at Google Scholar · View at Scopus
  68. F. Ciaffoni, E. Cassella, L. Varricchio, M. Massa, G. Barosi, and A. R. Migliaccio, “Activation of non-canonical TGF-beta1 signaling indicates an autoimmune mechanism for bone marrow fibrosis in primary myelofibrosis,” Blood Cells, Molecules, and Diseases, vol. 54, no. 3, pp. 234–241, 2015. View at Publisher · View at Google Scholar
  69. N. Sanderson, V. Factor, P. Nagy et al., “Hepatic expression of mature transforming growth factor β1 in transgenic mice results in multiple tissue lesions,” Proceedings of the National Academy of Sciences of the United States of America, vol. 92, no. 7, pp. 2572–2576, 1995. View at Publisher · View at Google Scholar · View at Scopus
  70. M. Lu, L. Xia, Y. C. Liu et al., “Lipocalin produced by myelofibrosis cells affects the fate of both hematopoietic and marrow microenvironmental cells,” Blood, 2015. View at Publisher · View at Google Scholar
  71. J. B. Cowland, O. E. Sørensen, M. Sehested, and N. Borregaard, “Neutrophil gelatinase-associated lipocalin is up-regulated in human epithelial cells by IL-1β, but not by TNF-α,” The Journal of Immunology, vol. 171, no. 12, pp. 6630–6639, 2003. View at Publisher · View at Google Scholar · View at Scopus
  72. F. Shen, M. J. Ruddy, P. Plamondon, and S. L. Gaffen, “Cytokines link osteoblasts and inflammation: Microarray analysis of interleukin-17- and TNF-α-induced genes in bone cells,” Journal of Leukocyte Biology, vol. 77, no. 3, pp. 388–399, 2005. View at Publisher · View at Google Scholar · View at Scopus
  73. M.-J. Xu, D. Feng, H. Wu et al., “Liver is the major source of elevated serum lipocalin-2 levels after bacterial infection or partial hepatectomy: a critical role for IL-6/STAT3,” Hepatology, vol. 61, no. 2, pp. 692–702, 2015. View at Publisher · View at Google Scholar · View at Scopus
  74. M. J. Thun, M. M. Namboodiri, and C. W. Heath Jr., “Aspirin use and reduced risk of fatal colon cancer,” The New England Journal of Medicine, vol. 325, no. 23, pp. 1593–1596, 1991. View at Publisher · View at Google Scholar · View at Scopus
  75. R. Landolfi, R. Marchioli, J. Kutti et al., “Efficacy and safety of low-dose aspirin in polycythemia vera,” The New England Journal of Medicine, vol. 350, no. 2, pp. 114–124, 2004. View at Publisher · View at Google Scholar · View at Scopus