Neutrophil NETs in reproduction: From infertility to preeclampsia and the possibility of fetal loss

Frontiers in Immunology

Volumn 3, Issue NOV, 2012, Pages

  Hahn, Sinuhe ^a   Giaglis, Stavros ^a,b   Hoesli, Irene ^a   Hasler, Paul ^b  

^a UNIVERSITY WOMEN S HOSPITAL   (Switzerland)

^b CANTONAL HOSPITAL AARAU   (Switzerland)

Author keywords

Infertility; Neutrophil extracellular traps (nets); Preeclampsia; Pregnancy; Recurrent fetal loss

Indexed keywords

EID: 84874199716     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2012.00362     Document Type: Article

References (79)

1. Alghamdi, A. S., and Foster, D. N. (2005). Seminal DNase frees spermatozoa entangled in neutrophil extracellular traps. Biol. Reprod. 73, 1174-1181.
2. Alghamdi, A. S., Foster, D. N., and Troedsson, M. H. (2004). Equine seminal plasma reduces sperm binding to polymorphonuclear neutrophils (PMNs) and improves the fertility of fresh semen inseminated into inflamed uteri. Reproduction 127, 593-600.
3. Alghamdi, A. S., Lovaas, B. J., Bird, S. L., Lamb, G.C., Rendahl, A.K., Taube, P. C., et al. (2009). Species-specific interaction of seminal plasma on sperm-neutrophil binding. Anim. Reprod. Sci. 114, 331-344.
4. Aly, A. S., Khandelwal, M., Zhao, J., Mehmet, A. H., Sammel, M. D., and Parry, S. (2004). Neutrophils are stimulated by syncytiotrophoblast microvillous membranes to generate superoxide radicals in women with preeclampsia. Am. J. Obstet. Gynecol. 190, 252-258.
5. Brill, A., Fuchs, T. A., Savchenko, A. S., Thomas, G. M., Martinod, K., De Meyer, S. F., et al. (2012). Neutrophil extracellular traps promote deep vein thrombosis in mice. J. Thromb. Haemost. 10, 136-144.
6. Brinkmann, V., Reichard, U., Goosmann, C., Fauler, B., Uhlemann, Y., Weiss, D. S., et al. (2004). Neutrophil extracellular traps kill bacteria. Science 303, 1532-1535.
7. Brinkmann, V., and Zychlinsky, A. (2007). Beneficial suicide: why neutrophils die to make NETs. Nat. Rev. Microbiol. 5, 577-582.
8. Brosens, I., Pijnenborg, R., Vercruysse, L., and Romero, R. (2011). The "Great Obstetrical Syndromes" are associated with disorders of deep placentation. Am. J. Obstet. Gynecol. 204, 193-201.
9. Burton, G. J., and Jauniaux, E. (2004). Placental oxidative stress: from miscarriage to preeclampsia. J. Soc. Gynecol. Investig. 11, 342-352.
10. Demers, M., Krause, D. S., Schatzberg, D., Martinod, K., Voorhees, J. R., Fuchs, T. A., et al. (2012). Cancers predispose neutrophils to release extracellular DNA traps that contribute to cancer-associated thrombosis. Proc. Natl. Acad. Sci. U.S.A. 109, 13076-13081.
11. Fuchs, T. A., Abed, U., Goosmann, C., Hurwitz, R., Schulze, I., Wahn, V., et al. (2007). Novel cell death program leads to neutrophil extracellular traps. J. Cell Biol. 176, 231-241.
12. Fuchs, T. A., Brill, A., Duerschmied, D., Schatzberg, D., Monestier, M., Myers, D. D. Jr., et al. (2010). Extracellular DNA traps promote thrombosis. Proc. Natl. Acad. Sci. U.S.A. 107, 15880-15885.
13. Fuchs, T. A., Brill, A., and Wagner, D. D. (2012). Neutrophil extracellular trap (NET) impact on deep vein thrombosis. Arterioscler. Thromb. Vasc. Biol. 32, 1777-1783.
14. Germain, S.J., Sacks, G.P., Sooranna, S. R., Sargent, I. L., and Redman, C. W. (2007). Systemic inflammatory priming in normal pregnancy and preeclampsia: the role of circulating syncytiotrophoblast microparticles. J. Immunol. 178, 5949-5956.
15. Girardi, G. (2011). Role of tissue factor in feto-maternal development: a xiphos. J. Thromb. Haemost. 9, 250-256.
16. Girardi, G., Berman, J., Redecha, P., Spruce, L., Thurman, J. M., Kraus, D., et al. (2003). Complement C5a receptors and neutrophils mediate fetal injury in the antiphospholipid syndrome. J. Clin. Invest. 112, 1644-1654.
17. Granne, I., Southcombe, J. H., Snider, J. V., Tannetta, D. S., Child, T., Redman, C. W., et al. (2011). ST2 and IL-33 in pregnancy and preeclampsia. PLoS ONE 6:e24463. doi: 10.1371/journal.pone.0024463
18. Gupta, A., Hasler, P., Gebhardt, S., Holzgreve, W., and Hahn, S. (2006). Occurrence of neutrophil extracellularsatztraps, DNA (NETs) in pre-eclampsia: a link with elevated levels of cell-free DNA? Ann. N.Y. Acad. Sci. 1075, 118-122.
19. Gupta, A. K., Gebhardt, S., Hillermann, R., Holzgreve, W., andHahn, S. (2006). Analysis of plasma elastase levels in early and late onset preeclampsia. Arch.Gynecol.Obstet. 273, 239-242.
20. Gupta, A. K., Hasler, P., Holzgreve, W., Gebhardt, S., and Hahn, S. (2005). Induction of neutrophil extracellular DNA lattices by placental microparticles and IL-8 and their presence in preeclampsia. Hum. Immunol. 66, 1146-1154.
21. Gupta, A. K., Rusterholz, C., Holzgreve, W., and Hahn, S. (2005). Syncytiotrophoblast micro-particles do not induce apoptosis in peripheralsatzlymphocytes, T, but differ in their activity depending on the mode of preparation. J. Reprod. Immunol. 68, 15-26.
22. Gupta, A. K., Hasler, P., Holzgreve, W., and Hahn, S. (2007). Neutrophil NETs: a novel contributor to preeclampsia-associated placental hypoxia? Semin. Immunopathol. 29, 163-167.
23. Gupta, A. K., Joshi, M. B., Philippova, M., Erne, P., Hasler, P., Hahn, S., et al. (2010). Activated endothelial cells induce neutrophil extracellular traps and are susceptible to NETosis-mediated cell death. FEBS Lett. 584, 3193-3197.
24. Gupta, G. K., and Bianchi, D. W. (1997). DNA diagnosis for the practicing obstetrician. Obstet. Gynecol. Clin. North Am. 24, 123-142.
25. Hahn, S., Gupta, A. K., Troeger, C., Rusterholz, C., and Holzgreve, W. (2006). Disturbances in placental immunology: ready for therapeutic interventions? Springer Semin. Immunopathol. 27, 477-493.
26. Hahn, S., Huppertz, B., and Holzgreve, W. (2005). Fetal cells and cell free fetal nucleic acids in maternal blood: new tools to study abnormal placentation? Placenta 26, 515-526.
27. Halim, A., Kanayama, N., El Maradny, E., Maehara, K., Bhuiyan, A. B., and Terao, T. (1996). Correlated plasma elastase and sera cytotoxicity in eclampsia. A possible role of endothelin-1 induced neutrophil activation in preeclampsiaeclampsia. Am. J. Hypertens. 9, 33-38.
28. Higuchi, D.A., Wun, T.C., Likert, K. M., and Broze, G. J. Jr. (1992). The effect of leukocyte elastase on tissue factor pathway inhibitor. Blood 79, 1712-1719.
29. Holers, V. M., Girardi, G., Mo, L., Guthridge, J.M., Molina, H., Pierangeli, S. S., et al. (2002). Complement C3 activation is required for antiphospholipid antibody-induced fetal loss. J. Exp. Med. 195, 211-220.
30. Huppertz, B. (2008). The anatomy of the normal placenta. J. Clin. Pathol. 61, 1296-1302.
31. Katila, T. (2012). Post-mating inflammatory responses of the uterus. Reprod. Domest. Anim. 47(Suppl. 5), 31-41.
32. King, A.E., Critchley, H.O., and Kelly, R. W. (2003). Innate immune defences in the human endometrium. Reprod. Biol. Endocrinol. 1, 116.
33. King, A. E., Critchley, H. O., Sallenave, J. M., and Kelly, R. W. (2003). Elafin in human endometrium: an antiprotease and antimicrobial molecule expressed during menstruation. J. Clin. Endocrinol. Metab. 88, 4426-4431.
34. Kitzmiller, J. L., and Benirschke, K. (1973). Immunofluorescent study of placental bed vessels in pre-eclampsia of pregnancy. Am. J. Obstet. Gynecol. 115, 248-251.
35. Knowles, H., Heizer, J. W., Li, Y., Chapman, K., Ogden, C. A., Andreasen, K., et al. (2011). Transient Receptor Potential Melastatin 2 (TRPM2) ion channel is required for innate immunity against Listeria monocytogenes. Proc. Natl. Acad. Sci. U.S.A. 108, 11578-11583.
36. Leung, T. N., Zhang, J., Lau, T. K., Chan, L.Y., andLo, Y.M. (2001). Increased maternal plasma fetal DNA concentrations in women who eventually develop preeclampsia. Clin. Chem. 47, 137-139.
37. Lynch, A. M., and Salmon, J. E. (2010). Dysregulated complement activation as a common pathway of injury in preeclampsia and other pregnancy complications. Placenta 31, 561-567.
38. Marcos, V., Nussbaum, C., Vitkov, L., Hector, A., Wiedenbauer, E. M., Roos, D., et al. (2009). Delayed but functional neutrophil extracellular trap formation in neonates. Blood 114, 4908-4911. author reply: 4911-4912.
39. Massberg, S., Grahl, L., von Bruehl, M.L., Manukyan, D., Pfeiler, S., Goosmann, C., et al. (2010). Reciprocal coupling of coagulation and innate immunity via neutrophil serine proteases. Nat. Med. 16, 887-896.
40. Mehta, R., and Petrova, A. (2006). Intrauterine neutrophil activation is associated with pulmonary haemorrhage in preterm infants. Arch. Dis. Child. Fetal Neonatal Ed. 91, F415-F418.
41. Mellembakken, J. R., Aukrust, P., Olafsen, M. K., Ueland, T., Hestdal, K., and Videm, V. (2002). Activation of leukocytes during the uteroplacental passage in preeclampsia. Hypertension 39, 155-160.
42. Messerli, M., May, K., Hansson, S. R., Schneider, H., Holzgreve, W., Hahn, S., et al. (2010). Feto-maternal interactions in pregnancies: placental microparticles activate peripheral blood monocytes. Placenta 31, 106-112.
43. Nathan, C. (2006). Neutrophils and immunity: challenges and opportunities. Nat. Rev. Immunol. 6, 173-182.
44. Neeli, I., Khan, S. N., and Radic, M. (2008). Histone deimination as a response to inflammatory stimuli in neutrophils. J. Immunol. 180, 1895-1902.
45. Papayannopoulos, V., Metzler, K. D., Hakkim, A., and Zychlinsky, A. (2010). Neutrophil elastase and myeloperoxidase regulate the formation of neutrophil extracellular traps. J. Cell Biol. 191, 677-691.
46. Pierangeli, S. S., Girardi, G., VegaOstertag, M., Liu, X., Espinola, R. G., and Salmon, J. (2005). Requirement of activation of complement C3 and C5 for antiphospholipid antibodymediated thrombophilia. Arthritis Rheum. 52, 2120-2124.
47. Pijnenborg, R., Vercruysse, L., and Brosens, I. (2011). Deep placentation. Best practice and research. Clin. Obstet. Gynaecol. 25, 273-285.
48. Plow, E. F. (1980). The major fibrinolytic proteases of human leukocytes. Biochim. Biophys. Acta 630, 47-56.
49. Powe, C. E., Levine, R. J., and Karumanchi, S. A. (2011). Preeclampsia, a disease of the maternal endothelium: the role of antiangiogenic factors and implications for later cardiovascular disease. Circulation 123, 2856-2869.
50. Rana, S., Powe, C. E., Salahuddin, S., Verlohren, S., Perschel, F. H., Levine, R. J., et al. (2012). Angiogenic factors and the risk of adverse outcomes in women with suspected preeclampsia. Circulation 125, 911-919.
51. Redecha, P., Tilley, R., Tencati, M., Salmon, J. E., Kirchhofer, D., Mackman, N., et al. (2007). Tissue factor: a link between C5a and neutrophil activation in antiphospholipid antibody induced fetal injury. Blood 110, 2423-2431.
52. Redman, C. W. (1997). Cytotrophoblasts: masters of disguise. Nat. Med. 3, 610-611.
53. Redman, C. W., and Sargent, I. L. (2005). Latest advances in understanding preeclampsia. Science 308, 1592-1594.
54. Redman, C. W., and Sargent, I. L. (2010). Immunology of preeclampsia. Am. J. Reprod. Immunol. 63, 534-543.
55. Robbins, J. R., and Bakardjiev, A. I. (2012). Pathogens and the placental fortress. Curr. Opin. Microbiol. 15, 36-43.
56. Roberts, J. M., and Hubel, C. A. (2009). The two stage model of preeclampsia: variations on the theme. Placenta 30(Suppl. A), S32-S37.
57. Roberts, J.M., andRedman, C.W. (1993). Pre-eclampsia: more than pregnancy-induced hypertension. Lancet 341, 1447-1451.
58. Rusterholz, C., Hahn, S., and Holzgreve, W. (2007). Role of placentally produced inflammatory and regulatory cytokines in pregnancy and the etiology of preeclampsia. Semin. Immunopathol. 29, 151-162.
59. Sacks, G. P., Studena, K., Sargent, K., and Redman, C. W. (1998). Normal pregnancy and preeclampsia both produce inflammatory changes in peripheral blood leukocytes akin to those of sepsis. Am. J. Obstet. Gynecol. 179, 80-86.
60. Saffarzadeh, M., Juenemann, C., Queisser, M. A., Lochnit, G., Barreto, G., Galuska, S.P., et al. (2012). Neutrophil extracellular traps directly induce epithelial and endothelial cell death: a predominant role of histones. PLoS ONE 7:e32366. doi: 10.1371/journal.pone.0032366
61. Salamonsen, L.A., andLathbury, L.J. (2000). Endometrial leukocytes and menstruation. Hum. Reprod. Update 6, 16-27.
62. Salamonsen, L. A., Zhang, J., Hampton, A., and Lathbury, L. (2000). Regulation of matrix metalloproteinases in human endometrium. Hum. Reprod. 15(Suppl. 3), 112-119.
63. Salmon, J. E., and Girardi, G. (2008). Antiphospholipid antibodies and pregnancy loss: a disorder of inflammation. J. Reprod. Immunol. 77, 51-56.
64. Sasaki, S., Nagata, K., and Kobayashi, Y. (2009). Regulation of the estrous cycle by neutrophil infiltration into the vagina. Biochem. Biophys. Res. Commun. 382, 35-40.
65. Sasaki, S., Tamaki, Y., Nagata, K., and Kobayashi, Y. (2011). Regulation of the estrous cycle by neutrophils via opioid peptides. J. Immunol. 187, 774-780.
66. Semeraro, F., Ammollo, C. T., Morrissey, J. H., Dale, G. L., Friese, P., Esmon, N. L., et al. (2011). Extracellular histones promote thrombin generation through platelet-dependent mechanisms: involvement of platelet TLR2 and TLR4. Blood 118, 1952-1961.
67. Smith, J. M., Shen, Z., Wira, C. R., Fanger, M. W., and Shen, L. (2007). Effects of menstrual cycle status and gender on human neutrophil phenotype. Am. J. Reprod. Immunol. 58, 111-119.
68. Strzemienski, P. J. (1989). Effect of bovine seminal plasma on neutrophil phagocytosis of bull spermatozoa. J. Reprod. Fertil. 87, 519-528.
69. Strzemienski, P. J., Dyer, R. M., Sertich, P. L., Garcia, M. C., and Kenney, R. M. (1987). Bactericidal activity of peripheral blood neutrophils during the oestrous cycle and early pregnancy in the mare. J. Reprod. Fertil. 80, 289-293.
70. vonBruhl, M.L., Stark, K., Steinhart, A., Chandraratne, S., Konrad, I., Lorenz, M., et al. (2012). Monocytes, neutrophils, and platelets cooperate to initiate and propagate venous thrombosis in mice in vivo. J. Exp. Med. 209, 819-835.
71. Wang, Y., Li, M., Stadler, S., Correll, S., Li, P., Wang, D., et al. (2009). Histone hypercitrullination mediates chromatin decondensation and neutrophil extracellular trap formation. J. Cell Biol. 184, 205-213.
72. Weiler, H. (2008). Tracing the molecular pathogenesis of antiphospholipid syndrome. J. Clin. Invest. 118, 3276-3278.
73. Wilkinson, H. (2011). Saving mothers' lives. Reviewing maternal deaths to make motherhood safer: 2006-2008. BJOG 118, 1402-1403. discussion: 1403-1404.
74. Wood, G. A., Fata, J. E., Watson, K. L., and Khokha, R. (2007). Circulating hormones and estrous stage predict cellular and stromal remodeling in murine uterus. Reproduction 133, 1035-1044.
75. Yost, C. C., Cody, M. J., Harris, E. S., Thornton, N. L., McInturff, A. M., Martinez, M. L., et al. (2009). Impaired neutrophil extracellular trap (NET) formation: a novel innate immune deficiency of human neonates. Blood 113, 6419-6427.
76. Zhong, X. Y., Gebhardt, S., Hillermann, R., Tofa, K. C., Holzgreve, W., and Hahn, S. (2005). Parallel assessment of circulatory fetal DNA and corticotropin-releasing hormone mRNA in earlyand late-onset preeclampsia. Clin. Chem. 51, 1730-1733.
77. Zhong, X. Y., Gebhardt, S., Hillermann, R., Tofa, K.C., Holzgreve, W., and Hahn, S. (2005). Circulatory nucleosome levels are significantly increased in early and late-onset preeclampsia. Prenat. Diagn. 25, 700-703.
78. Zhong, X. Y., Holzgreve, W., and Hahn, S. (2001). Circulatory fetal and maternal DNA in pregnancies at risk and those affected by preeclampsia. Ann. N.Y. Acad. Sci. 945, 138-140.
79. Zhong, X. Y., Laivuori, H., Livingston, J. C., Ylikorkala, O., Sibai, B. M., Holzgreve, W., et al. (2001). Elevation of both maternal and fetal extracellular circulating deoxyribonucleic acid concentrations in the plasma of pregnant women with preeclampsia. Am. J. Obstet. Gynecol. 184, 414-419.