NETosis: A new factor in tumor progression and cancer-associated thrombosis

Seminars in Thrombosis and Hemostasis

Volumn 40, Issue 3, 2014, Pages 277-283

  Demers, Melanie ^a,b   Wagner, Denisa D ^a,b  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

biomarkers; cancer; NETs; thrombosis

Indexed keywords

BLOOD CLOTTING FACTOR 12; HISTONE H3;

ARTICLE; CANCER GROWTH; CANCER SUSCEPTIBILITY; CELL SURVIVAL; HUMAN; METASTASIS; NEUTROPHIL; NEUTROPHIL EXTRACELLULAR TRAPS; NONHUMAN; PRIORITY JOURNAL; TUMOR MICROENVIRONMENT; TUMOR THROMBUS; ANIMAL; BLOOD; COMPLICATION; DISEASE COURSE; NEOPLASM; PATHOLOGY; THROMBOSIS;

ANIMALS; DISEASE PROGRESSION; HUMANS; NEOPLASMS; NEUTROPHILS; THROMBOSIS;

EID: 84898601855     PISSN: 00946176     EISSN: 10989064     Source Type: Journal    
DOI: 10.1055/s-0034-1370765     Document Type: Article

References (77)

1. Amulic B., Cazalet C., Hayes G. L., Metzler K. D., Zychlinsky A. Neutrophil function: from mechanisms to disease. Annu Rev Immunol: 2012; 30 459 489
2. Mócsai A. Diverse novel functions of neutrophils in immunity, inflammation, and beyond. J Exp Med: 2013; 210 7 1283 1299
3. Brinkmann V., Reichard U., Goosmann C., et al. Neutrophil extracellular traps kill bacteria. Science: 2004; 303 5663 1532 1535
4. Fuchs T. A., Abed U., Goosmann C., et al. Novel cell death program leads to neutrophil extracellular traps. J Cell Biol: 2007; 176 2 231 241
5. Pilsczek F. H., Salina D., Poon K. K., et al. A novel mechanism of rapid nuclear neutrophil extracellular trap formation in response to Staphylococcus aureus. J Immunol: 2010; 185 12 7413 7425
6. Yipp B. G., Petri B., Salina D., et al. Infection-induced NETosis is a dynamic process involving neutrophil multitasking in vivo. Nat Med: 2012; 18 9 1386 1393
7. Yipp B. G., Kubes P. NETosis: how vital is it? Blood: 2013; 122 16 2784 2794
8. Bianchi M., Hakkim A., Brinkmann V., et al. Restoration of NET formation by gene therapy in CGD controls aspergillosis. Blood: 2009; 114 13 2619 2622
9. Hakkim A., Fuchs T. A., Martinez N. E., et al. Activation of the Raf-MEK-ERK pathway is required for neutrophil extracellular trap formation. Nat Chem Biol: 2011; 7 2 75 77
10. Keshari R. S., Verma A., Barthwal M. K., Dikshit M. Reactive oxygen species-induced activation of ERK and p38 MAPK mediates PMA-induced NETs release from human neutrophils. J Cell Biochem: 2013; 114 3 532 540
11. Parker H., Dragunow M., Hampton M. B., Kettle A. J., Winterbourn C. C. Requirements for NADPH oxidase and myeloperoxidase in neutrophil extracellular trap formation differ depending on the stimulus. J Leukoc Biol: 2012; 92 4 841 849
12. Papayannopoulos V., Metzler K. D., Hakkim A., Zychlinsky A. Neutrophil elastase and myeloperoxidase regulate the formation of neutrophil extracellular traps. J Cell Biol: 2010; 191 3 677 691
13. Wang S., Wang Y. Peptidylarginine deiminases in citrullination, gene regulation, health and pathogenesis. Biochim Biophys Acta: 2013; 1829 10 1126 1135
14. Li P., Li M., Lindberg M. R., Kennett M. J., Xiong N., Wang Y. PAD4 is essential for antibacterial innate immunity mediated by neutrophil extracellular traps. J Exp Med: 2010; 207 9 1853 1862
15. Martinod K., Demers M., Fuchs T. A., et al. Neutrophil histone modification by peptidylarginine deiminase 4 is critical for deep vein thrombosis in mice. Proc Natl Acad Sci U S A: 2013; 110 21 8674 8679
16. Wang Y., Li M., Stadler S., et al. Histone hypercitrullination mediates chromatin decondensation and neutrophil extracellular trap formation. J Cell Biol: 2009; 184 2 205 213
17. Leshner M., Wang S., Lewis C., et al. PAD4 mediated histone hypercitrullination induces heterochromatin decondensation and chromatin unfolding to form neutrophil extracellular trap-like structures. Front Immunol: 2012; 3 307
18. Fuchs T. A., Brill A., Duerschmied D., et al. Extracellular DNA traps promote thrombosis. Proc Natl Acad Sci U S A: 2010; 107 36 15880 15885
19. Massberg S., Grahl L., von Bruehl M. L., et al. Reciprocal coupling of coagulation and innate immunity via neutrophil serine proteases. Nat Med: 2010; 16 8 887 896
20. Brill A., Fuchs T. A., Savchenko A. S., et al. Neutrophil extracellular traps promote deep vein thrombosis in mice. J Thromb Haemost: 2012; 10 1 136 144
21. Nakazawa D., Tomaru U., Yamamoto C., Jodo S., Ishizu A. Abundant neutrophil extracellular traps in thrombus of patient with microscopic polyangiitis. Front Immunol: 2012; 3 333
22. Diaz J. A., Fuchs T. A., Jackson T. O., et al. Plasma DNA is elevated in patients with deep vein thrombosis. J Vasc Surg Venous Lymphat Disord: 2013; 1 4 341 348
23. van Montfoort M. L., Stephan F., Lauw M. N., et al. Circulating nucleosomes and neutrophil activation as risk factors for deep vein thrombosis. Arterioscler Thromb Vasc Biol: 2013; 33 1 147 151
24. von Brühl M. L., Stark K., Steinhart A., et al. Monocytes, neutrophils, and platelets cooperate to initiate and propagate venous thrombosis in mice in vivo. J Exp Med: 2012; 209 4 819 835
25. Fuchs T. A., Kremer Hovinga J. A., Schatzberg D., Wagner D. D., Lämmle B. Circulating DNA and myeloperoxidase indicate disease activity in patients with thrombotic microangiopathies. Blood: 2012; 120 6 1157 1164
26. Borissoff J. I., Joosen I. A., Versteylen M. O., et al. Elevated levels of circulating DNA and chromatin are independently associated with severe coronary atherosclerosis and a prothrombotic state. Arterioscler Thromb Vasc Biol: 2013; 33 8 2032 2040
27. Kannemeier C., Shibamiya A., Nakazawa F., et al. Extracellular RNA constitutes a natural procoagulant cofactor in blood coagulation. Proc Natl Acad Sci U S A: 2007; 104 15 6388 6393
28. Swystun L. L., Mukherjee S., Liaw P. C. Breast cancer chemotherapy induces the release of cell-free DNA, a novel procoagulant stimulus. J Thromb Haemost: 2011; 9 11 2313 2321
29. Xu J., Zhang X., Pelayo R., et al. Extracellular histones are major mediators of death in sepsis. Nat Med: 2009; 15 11 1318 1321
30. Ammollo C. T., Semeraro F., Xu J., Esmon N. L., Esmon C. T. Extracellular histones increase plasma thrombin generation by impairing thrombomodulin- dependent protein C activation. J Thromb Haemost: 2011; 9 9 1795 1803
31. Semeraro F., Ammollo C. T., Morrissey J. H., et al. Extracellular histones promote thrombin generation through platelet-dependent mechanisms: involvement of platelet TLR2 and TLR4. Blood: 2011; 118 7 1952 1961
32. Fuchs T. A., Bhandari A. A., Wagner D. D. Histones induce rapid and profound thrombocytopenia in mice. Blood: 2011; 118 13 3708 3714
33. Kambas K., Chrysanthopoulou A., Vassilopoulos D., et al. Tissue factor expression in neutrophil extracellular traps and neutrophil derived microparticles in antineutrophil cytoplasmic antibody associated vasculitis may promote thromboinflammation and the thrombophilic state associated with the disease. Ann Rheum Dis: 2013;. doi:10.1136/annrheumdis-2013-203430 [e-pub ahead of print]
34. Kambas K., Mitroulis I., Apostolidou E., et al. Autophagy mediates the delivery of thrombogenic tissue factor to neutrophil extracellular traps in human sepsis. PLoS ONE: 2012; 7 9 e45427
35. Brandau S., Dumitru C. A., Lang S. Protumor and antitumor functions of neutrophil granulocytes. Semin Immunopathol: 2013; 35 2 163 176
36. Gregory A. D., Houghton A. M. Tumor-associated neutrophils: new targets for cancer therapy. Cancer Res: 2011; 71 7 2411 2416
37. Demers M., Wagner D. D. Neutrophil extracellular traps: A new link to cancer-associated thrombosis and potential implications for tumor progression. OncoImmunology: 2013; 2 2 e22946
38. Ho-Tin-Noé B., Carbo C., Demers M., Cifuni S. M., Goerge T., Wagner D. D. Innate immune cells induce hemorrhage in tumors during thrombocytopenia. Am J Pathol: 2009; 175 4 1699 1708
39. Berger-Achituv S., Brinkmann V., Abed U. A., et al. A proposed role for neutrophil extracellular traps in cancer immunoediting. Front Immunol: 2013; 4 48
40. McInturff A. M., Cody M. J., Elliott E. A., et al. Mammalian target of rapamycin regulates neutrophil extracellular trap formation via induction of hypoxia-inducible factor 1 α Blood: 2012; 120 15 3118 3125
41. Mishalian I., Bayuh R., Levy L., Zolotarov L., Michaeli J., Fridlender Z. G. Tumor-associated neutrophils (TAN) develop pro-tumorigenic properties during tumor progression. Cancer Immunol Immunother: 2013; 62 11 1745 1756
42. Cools-Lartigue J., Spicer J., McDonald B., et al. Neutrophil extracellular traps sequester circulating tumor cells and promote metastasis. J Clin Invest: 2013; doi: 10.1172/JCI67484
43. Clark S. R., Ma A. C., Tavener S. A., et al. Platelet TLR4 activates neutrophil extracellular traps to ensnare bacteria in septic blood. Nat Med: 2007; 13 4 463 469
44. McDonald B., Urrutia R., Yipp B. G., Jenne C. N., Kubes P. Intravascular neutrophil extracellular traps capture bacteria from the bloodstream during sepsis. Cell Host Microbe: 2012; 12 3 324 333
45. Green D., Karpatkin S. Role of thrombin as a tumor growth factor. Cell Cycle: 2010; 9 4 656 661
46. Hu L., Ibrahim S., Liu C., Skaar J., Pagano M., Karpatkin S. Thrombin induces tumor cell cycle activation and spontaneous growth by down-regulation of p27Kip1, in association with the up-regulation of Skp2 and MiR-222. Cancer Res: 2009; 69 8 3374 3381
47. Hu L., Lee M., Campbell W., Perez-Soler R., Karpatkin S. Role of endogenous thrombin in tumor implantation, seeding, and spontaneous metastasis. Blood: 2004; 104 9 2746 2751
48. Hu L., Roth J. M., Brooks P., Ibrahim S., Karpatkin S. Twist is required for thrombin-induced tumor angiogenesis and growth. Cancer Res: 2008; 68 11 4296 4302
49. Hu L., Roth J. M., Brooks P., Luty J., Karpatkin S. Thrombin up-regulates cathepsin D which enhances angiogenesis, growth, and metastasis. Cancer Res: 2008; 68 12 4666 4673
50. Varki A. Trousseau's syndrome: multiple definitions and multiple mechanisms. Blood: 2007; 110 6 1723 1729
51. Connolly G. C., Khorana A. A. Emerging risk stratification approaches to cancer-associated thrombosis: risk factors, biomarkers and a risk score. Thromb Res: 2010; 125 02 S1 S7
52. Connolly G. C., Khorana A. A., Kuderer N. M., Culakova E., Francis C. W., Lyman G. H. Leukocytosis, thrombosis and early mortality in cancer patients initiating chemotherapy. Thromb Res: 2010; 126 2 113 118
53. Shao B., Wahrenbrock M. G., Yao L., et al. Carcinoma mucins trigger reciprocal activation of platelets and neutrophils in a murine model of Trousseau syndrome. Blood: 2011; 118 15 4015 4023
54. Shoenfeld Y., Tal A., Berliner S., Pinkhas J. Leukocytosis in non hematological malignancies-a possible tumor-associated marker. J Cancer Res Clin Oncol: 1986; 111 1 54 58
55. Donskov F. Immunomonitoring and prognostic relevance of neutrophils in clinical trials. Semin Cancer Biol: 2013; 23 3 200 207
56. Paneesha S., McManus A., Arya R., et al. VERITY Investigators. Frequency, demographics and risk (according to tumour type or site) of cancer-associated thrombosis among patients seen at outpatient DVT clinics. Thromb Haemost: 2010; 103 2 338 343
57. DuPre' S. A., Hunter K. W. Jr. Murine mammary carcinoma 4T1 induces a leukemoid reaction with splenomegaly: association with tumor-derived growth factors. Exp Mol Pathol: 2007; 82 1 12 24
58. Demers M., Krause D. S., Schatzberg D., et al. Cancers predispose neutrophils to release extracellular DNA traps that contribute to cancer-associated thrombosis. Proc Natl Acad Sci U S A: 2012; 109 32 13076 13081
59. Joshita S., Nakazawa K., Sugiyama Y., et al. Granulocyte-colony stimulating factor-producing pancreatic adenosquamous carcinoma showing aggressive clinical course. Intern Med: 2009; 48 9 687 691
60. Kaira K., Ishizuka T., Tanaka H., et al. Lung cancer producing granulocyte colony-stimulating factor and rapid spreading to peritoneal cavity. J Thorac Oncol: 2008; 3 9 1054 1055
61. Kawaguchi M., Asada Y., Terada T., et al. Aggressive recurrence of gastric cancer as a granulocyte-colony-stimulating factor-producing tumor. Int J Clin Oncol: 2010; 15 2 191 195
62. Leon S. A., Shapiro B., Sklaroff D. M., Yaros M. J. Free DNA in the serum of cancer patients and the effect of therapy. Cancer Res: 1977; 37 3 646 650
63. Fleischhacker M., Schmidt B. Circulating nucleic acids (CNAs) and cancer-a survey. Biochim Biophys Acta: 2007; 1775 1 181 232
64. Jahr S., Hentze H., Englisch S., et al. DNA fragments in the blood plasma of cancer patients: quantitations and evidence for their origin from apoptotic and necrotic cells. Cancer Res: 2001; 61 4 1659 1665
65. García-Olmo D. C., Picazo M. G., Toboso I., Asensio A. I., García-Olmo D. Quantitation of cell-free DNA and RNA in plasma during tumor progression in rats. Mol Cancer: 2013; 12 8
66. García-Olmo D. C., Samos J., Picazo M. G., Asensio A. I., Toboso I., García-Olmo D. Release of cell-free DNA into the bloodstream leads to high levels of non-tumor plasma DNA during tumor progression in rats. Cancer Lett: 2008; 272 1 133 140
67. McMahon B. J., Kwaan H. C. Thrombotic and bleeding complications associated with chemotherapy. Semin Thromb Hemost: 2012; 38 8 808 817
68. Kwee S., Song M. A., Cheng I., Loo L., Tiirikainen M. Measurement of circulating cell-free DNA in relation to 18F-fluorocholine PET/CT imaging in chemotherapy-treated advanced prostate cancer. Clin Transl Sci: 2012; 5 1 65 70
69. Deligezer U., Eralp Y., Akisik E. E., et al. Size distribution of circulating cell-free DNA in sera of breast cancer patients in the course of adjuvant chemotherapy. Clin Chem Lab Med: 2008; 46 3 311 317
70. Van Den Berg Y. W., Reitsma P. H. Not exclusively tissue factor: neutrophil extracellular traps provide another link between chemotherapy and thrombosis. J Thromb Haemost: 2011; 9 11 2311 2312
71. Chang X., Han J. Expression of peptidylarginine deiminase type 4 (PAD4) in various tumors. Mol Carcinog: 2006; 45 3 183 196
72. Chang X., Han J., Pang L., Zhao Y., Yang Y., Shen Z. Increased PADI4 expression in blood and tissues of patients with malignant tumors. BMC Cancer: 2009; 9 40
73. Li P., Yao H., Zhang Z., et al. Regulation of p53 target gene expression by peptidylarginine deiminase 4. Mol Cell Biol: 2008; 28 15 4745 4758
74. Luo Y., Knuckley B., Lee Y. H., Stallcup M. R., Thompson P. R. A fluoroacetamidine-based inactivator of protein arginine deiminase 4: design, synthesis, and in vitro and in vivo evaluation. J Am Chem Soc: 2006; 128 4 1092 1093
75. Jones J. E., Slack J. L., Fang P., et al. Synthesis and screening of a haloacetamidine containing library to identify PAD4 selective inhibitors. ACS Chem Biol: 2012; 7 1 160 165
76. Li P., Wang D., Yao H., et al. Coordination of PAD4 and HDAC2 in the regulation of p53-target gene expression. Oncogene: 2010; 29 21 3153 3162
77. Wang Y., Li P., Wang S., et al. Anticancer peptidylarginine deiminase (PAD) inhibitors regulate the autophagy flux and the mammalian target of rapamycin complex 1 activity. J Biol Chem: 2012; 287 31 25941 25953