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Frontiers in immunology2012; 3; 362; doi: 10.3389/fimmu.2012.00362

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

Abstract: The intention of this review is to provide an overview of the potential role of neutrophil extracellular traps (NETs) in mammalian reproduction. Neutrophil NETs appear to be involved in various stages of the reproductive cycle, starting with fertility and possibly ending with fetal loss. The first suggestion that NETs may play a role in pregnancy-related disorders was in preeclampsia, where vast numbers were detected in the intervillous space of affected placentae. The induction of NETosis involved an auto-inflammatory component, mediated by the increased release of placental micro-debris in preeclampsia. This report was the first indicating that NETs may be associated with a human pathology not involving infection. Subsequently, NETs have since then been implicated in bovine or equine infertility, in that semen may become entrapped in the female reproductive tract during their passage to the oocyte. In this instance interesting species-specific differences are apparent, in that equine sperm evade entrapment via expression of a DNAse-like molecule, whereas highly motile bovine sperm, once free from seminal plasma (SP) that promotes interaction with neutrophils, appear impervious to NETs entrapment. Although still in the realm of speculation it is plausible that NETs may be involved in recurrent fetal loss mediated by anti-phospholipid antibodies, or perhaps even in fetal abortion triggered by infections with microorganisms such as L. monocytogenes or B. abortus.
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Publication Date: 2012-11-27 PubMed ID: 23205021PubMed Central: PMC3506920DOI: 10.3389/fimmu.2012.00362Google Scholar: Lookup
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Summary

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This article reviews the possible role of neutrophil extracellular traps (NETs) in the complex process of mammalian reproduction, from fertility to potential fetal loss, with a focus on their connection to certain pregnancy-related disorders like preeclampsia and infertility.

Role of Neutrophil Extracellular Traps (NETs) in Reproduction

Neutrophil extracellular traps, or NETs, are web-like structures, released by neutrophils, a type of white blood cell. They are primarily recognized for their role in trapping and killing pathogens.

  • The paper investigates the potential involvement of NETs in various components of the reproductive cycle, beginning with fertility and potentially culminating in fetal loss.
  • The first indication that NETs might have a role in pregnancy-related disorders came from a study on preeclampsia. This condition is characterised by high blood pressure during pregnancy and can lead to severe complications for both mother and child. A significantly higher number of NETs were found in the intervillous space of affected placentae in preeclampsia patients.
  • The activation of NETs, referred as NETosis, occurring in preeclampsia was revealed to involve an auto-inflammatory component, driven by an increased release of placental micro-debris.
  • This was the first time that NETs were linked to a human pathology that does not revolve around infection.

Cross-Species Comparison of NETs Interaction With Sperm

NETs also appear to play a role in bovine and equine infertility.

  • The researchers noted an interesting phenomenon wherein semen could become ensnared in the female reproductive tract by NETs, potentially preventing it from reaching the oocyte and causing infertility.
  • However, there were significant species-specific differences. Equine sperm, for instance, can avoid this entrapment through the expression of a DNAse-like molecule.
  • Conversely, bovine sperm seemed immune to NETs entrapment once they were free from the seminal plasma that promotes interaction with neutrophils.

Potential Role of NETs in Fetal Loss

The researchers explore the possibility of the implication of NETs in recurrent fetal loss and abortion.

  • There’s speculation that NETs may play a part in recurrent fetal loss mediated by anti-phospholipid antibodies, which, in some instances can cause complications in pregnancy.
  • The review also suggests the possibility of NETs being involved in fetal abortion triggered by infections with certain microorganisms like L. monocytogenes or B. abortus.

Cite This Article

APA
Hahn S, Giaglis S, Hoesli I, Hasler P. (2012). Neutrophil NETs in reproduction: from infertility to preeclampsia and the possibility of fetal loss. Front Immunol, 3, 362. https://doi.org/10.3389/fimmu.2012.00362

Publication

Frontiers in immunology
ISSN: 1664-3224
NlmUniqueID: 101560960
Country: Switzerland
Language: English
Volume: 3
Pages: 362
PII: 362

Researcher Affiliations

Hahn, Sinuhe
  • Department of Biomedicine, University of Basel/Laboratory for Prenatal Medicine, University Clinics, University Women's Hospital Basel, Switzerland.
Giaglis, Stavros
    Hoesli, Irene
      Hasler, Paul

        References

        This article includes 79 references
        1. Alghamdi AS, Foster DN. Seminal DNase frees spermatozoa entangled in neutrophil extracellular traps.. Biol Reprod 2005 Dec;73(6):1174-81.
          doi: 10.1095/biolreprod.105.045666pubmed: 16107606google scholar: lookup
        2. Alghamdi AS, Foster DN, Troedsson MH. Equine seminal plasma reduces sperm binding to polymorphonuclear neutrophils (PMNs) and improves the fertility of fresh semen inseminated into inflamed uteri.. Reproduction 2004 May;127(5):593-600.
          doi: 10.1530/rep.1.00096pubmed: 15129015google scholar: lookup
        3. Alghamdi AS, Lovaas BJ, Bird SL, Lamb GC, Rendahl AK, Taube PC, Foster DN. Species-specific interaction of seminal plasma on sperm-neutrophil binding.. Anim Reprod Sci 2009 Sep;114(4):331-44.
          doi: 10.1016/j.anireprosci.2008.10.015pubmed: 19081210google scholar: lookup
        4. Aly AS, Khandelwal M, Zhao J, Mehmet AH, Sammel MD, Parry S. Neutrophils are stimulated by syncytiotrophoblast microvillous membranes to generate superoxide radicals in women with preeclampsia.. Am J Obstet Gynecol 2004 Jan;190(1):252-8.
          doi: 10.1016/j.ajog.2003.07.003pubmed: 14749668google scholar: lookup
        5. Brill A, Fuchs TA, Savchenko AS, Thomas GM, Martinod K, De Meyer SF, Bhandari AA, Wagner DD. Neutrophil extracellular traps promote deep vein thrombosis in mice.. J Thromb Haemost 2012 Jan;10(1):136-44.
          doi: 10.1111/j.1538-7836.2011.04544.xpmc: PMC3319651pubmed: 22044575google scholar: lookup
        6. Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, Weiss DS, Weinrauch Y, Zychlinsky A. Neutrophil extracellular traps kill bacteria.. Science 2004 Mar 5;303(5663):1532-5.
          doi: 10.1007/978-1-61779-527-5_7pubmed: 15001782google scholar: lookup
        7. Brinkmann V, Zychlinsky A. Beneficial suicide: why neutrophils die to make NETs.. Nat Rev Microbiol 2007 Aug;5(8):577-82.
          doi: 10.1038/nrmicro1710pubmed: 17632569google scholar: lookup
        8. Brosens I, Pijnenborg R, Vercruysse L, Romero R. The "Great Obstetrical Syndromes" are associated with disorders of deep placentation.. Am J Obstet Gynecol 2011 Mar;204(3):193-201.
          doi: 10.1016/j.ajog.2010.08.009pmc: PMC3369813pubmed: 21094932google scholar: lookup
        9. Burton GJ, Jauniaux E. Placental oxidative stress: from miscarriage to preeclampsia.. J Soc Gynecol Investig 2004 Sep;11(6):342-52.
          doi: 10.1016/j.jsgi.2004.03.003pubmed: 15350246google scholar: lookup
        10. Demers M, Krause DS, Schatzberg D, Martinod K, Voorhees JR, Fuchs TA, Scadden DT, Wagner DD. Cancers predispose neutrophils to release extracellular DNA traps that contribute to cancer-associated thrombosis.. Proc Natl Acad Sci U S A 2012 Aug 7;109(32):13076-81.
          doi: 10.1073/pnas.1200419109pmc: PMC3420209pubmed: 22826226google scholar: lookup
        11. Fuchs TA, Abed U, Goosmann C, Hurwitz R, Schulze I, Wahn V, Weinrauch Y, Brinkmann V, Zychlinsky A. Novel cell death program leads to neutrophil extracellular traps.. J Cell Biol 2007 Jan 15;176(2):231-41.
          doi: 10.1083/jcb.200606027pmc: PMC2063942pubmed: 17210947google scholar: lookup
        12. Fuchs TA, Brill A, Duerschmied D, Schatzberg D, Monestier M, Myers DD Jr, Wrobleski SK, Wakefield TW, Hartwig JH, Wagner DD. Extracellular DNA traps promote thrombosis.. Proc Natl Acad Sci U S A 2010 Sep 7;107(36):15880-5.
          doi: 10.1073/pnas.1005743107pmc: PMC2936604pubmed: 20798043google scholar: lookup
        13. Fuchs TA, Brill A, Wagner DD. Neutrophil extracellular trap (NET) impact on deep vein thrombosis.. Arterioscler Thromb Vasc Biol 2012 Aug;32(8):1777-83.
          doi: 10.1161/ATVBAHA.111.242859pmc: PMC3495595pubmed: 22652600google scholar: lookup
        14. Germain SJ, Sacks GP, Sooranna SR, Sargent IL, Redman CW. Systemic inflammatory priming in normal pregnancy and preeclampsia: the role of circulating syncytiotrophoblast microparticles.. J Immunol 2007 May 1;178(9):5949-56.
          pubmed: 17442979doi: 10.4049/jimmunol.178.9.5949google scholar: lookup
        15. Girardi G. Role of tissue factor in feto-maternal development: a xiphos.. J Thromb Haemost 2011 Feb;9(2):250-6.
          doi: 10.1111/j.1538-7836.2010.04135.xpubmed: 21070593google scholar: lookup
        16. Girardi G, Berman J, Redecha P, Spruce L, Thurman JM, Kraus D, Hollmann TJ, Casali P, Caroll MC, Wetsel RA, Lambris JD, Holers VM, Salmon JE. Complement C5a receptors and neutrophils mediate fetal injury in the antiphospholipid syndrome.. J Clin Invest 2003 Dec;112(11):1644-54.
          doi: 10.1172/JCI18817pmc: PMC281643pubmed: 14660741google scholar: lookup
        17. Granne I, Southcombe JH, Snider JV, Tannetta DS, Child T, Redman CW, Sargent IL. ST2 and IL-33 in pregnancy and pre-eclampsia.. PLoS One 2011;6(9):e24463.
          doi: 10.1371/journal.pone.0024463pmc: PMC3174956pubmed: 21949719google scholar: lookup
        18. Gupta A, Hasler P, Gebhardt S, Holzgreve W, Hahn S. Occurrence of neutrophil extracellular DNA traps (NETs) in pre-eclampsia: a link with elevated levels of cell-free DNA?. Ann N Y Acad Sci 2006 Sep;1075:118-22.
          doi: 10.1196/annals.1368.015pubmed: 17108200google scholar: lookup
        19. Gupta AK, Gebhardt S, Hillermann R, Holzgreve W, Hahn S. Analysis of plasma elastase levels in early and late onset preeclampsia.. Arch Gynecol Obstet 2006 Jan;273(4):239-42.
          doi: 10.1007/s00404-005-0093-zpubmed: 16292578google scholar: lookup
        20. Gupta AK, Hasler P, Holzgreve W, Gebhardt S, Hahn S. Induction of neutrophil extracellular DNA lattices by placental microparticles and IL-8 and their presence in preeclampsia.. Hum Immunol 2005 Nov;66(11):1146-54.
          doi: 10.1016/j.humimm.2005.11.003pubmed: 16571415google scholar: lookup
        21. Gupta AK, Rusterholz C, Holzgreve W, Hahn S. Syncytiotrophoblast micro-particles do not induce apoptosis in peripheral T lymphocytes, but differ in their activity depending on the mode of preparation.. J Reprod Immunol 2005 Dec;68(1-2):15-26.
          doi: 10.1016/j.jri.2005.05.003pubmed: 16233919google scholar: lookup
        22. Gupta AK, Hasler P, Holzgreve W, Hahn S. Neutrophil NETs: a novel contributor to preeclampsia-associated placental hypoxia?. Semin Immunopathol 2007 Jun;29(2):163-7.
          doi: 10.1007/s00281-007-0073-4pubmed: 17621701google scholar: lookup
        23. Gupta AK, Joshi MB, Philippova M, Erne P, Hasler P, Hahn S, Resink TJ. Activated endothelial cells induce neutrophil extracellular traps and are susceptible to NETosis-mediated cell death.. FEBS Lett 2010 Jul 16;584(14):3193-7.
          doi: 10.1016/j.febslet.2010.06.006pubmed: 20541553google scholar: lookup
        24. Gupta GK, Bianchi DW. DNA diagnosis for the practicing obstetrician.. Obstet Gynecol Clin North Am 1997 Mar;24(1):123-42.
          pubmed: 9086522doi: 10.1016/s0889-8545(05)70293-xgoogle scholar: lookup
        25. Hahn S, Gupta AK, Troeger C, Rusterholz C, Holzgreve W. Disturbances in placental immunology: ready for therapeutic interventions?. Springer Semin Immunopathol 2006 Jun;27(4):477-93.
          doi: 10.1007/s00281-006-0016-5pubmed: 16738957google scholar: lookup
        26. Hahn S, Huppertz B, Holzgreve W. Fetal cells and cell free fetal nucleic acids in maternal blood: new tools to study abnormal placentation?. Placenta 2005 Aug;26(7):515-26.
          doi: 10.1016/j.placenta.2004.10.017pubmed: 15993701google scholar: lookup
        27. Halim A, Kanayama N, El Maradny E, Maehara K, Bhuiyan AB, Terao T. Correlated plasma elastase and sera cytotoxicity in eclampsia. A possible role of endothelin-1 induced neutrophil activation in preeclampsia-eclampsia.. Am J Hypertens 1996 Jan;9(1):33-8.
          pubmed: 8834704doi: 10.1016/0895-7061(95)00185-9google scholar: lookup
        28. Higuchi DA, Wun TC, Likert KM, Broze GJ Jr. The effect of leukocyte elastase on tissue factor pathway inhibitor.. Blood 1992 Apr 1;79(7):1712-9.
          pubmed: 1558967
        29. Holers VM, Girardi G, Mo L, Guthridge JM, Molina H, Pierangeli SS, Espinola R, Xiaowei LE, Mao D, Vialpando CG, Salmon JE. Complement C3 activation is required for antiphospholipid antibody-induced fetal loss.. J Exp Med 2002 Jan 21;195(2):211-20.
          doi: 10.1084/jem.200116116pmc: PMC2193604pubmed: 11805148google scholar: lookup
        30. Huppertz B. The anatomy of the normal placenta.. J Clin Pathol 2008 Dec;61(12):1296-302.
          doi: 10.1136/jcp.2008.055277pubmed: 18755720google scholar: lookup
        31. Katila T. Post-mating inflammatory responses of the uterus.. Reprod Domest Anim 2012 Aug;47 Suppl 5:31-41.
          doi: 10.1111/j.1439-0531.2012.02120.xpubmed: 22913558google scholar: lookup
        32. King AE, Critchley HO, Kelly RW. Innate immune defences in the human endometrium.. Reprod Biol Endocrinol 2003 Nov 28;1:116.
          doi: 10.1186/1477-7827-1-116pmc: PMC305332pubmed: 14641912google scholar: lookup
        33. King AE, Critchley HO, Sallenave JM, Kelly RW. Elafin in human endometrium: an antiprotease and antimicrobial molecule expressed during menstruation.. J Clin Endocrinol Metab 2003 Sep;88(9):4426-31.
          doi: 10.1210/jc.2003-030239pubmed: 12970320google scholar: lookup
        34. Kitzmiller JL, Benirschke K. Immunofluorescent study of placental bed vessels in pre-eclampsia of pregnancy.. Am J Obstet Gynecol 1973 Jan 15;115(2):248-51.
          pubmed: 4570955doi: 10.1016/0002-9378(73)90293-7google scholar: lookup
        35. Knowles H, Heizer JW, Li Y, Chapman K, Ogden CA, Andreasen K, Shapland E, Kucera G, Mogan J, Humann J, Lenz LL, Morrison AD, Perraud AL. Transient Receptor Potential Melastatin 2 (TRPM2) ion channel is required for innate immunity against Listeria monocytogenes.. Proc Natl Acad Sci U S A 2011 Jul 12;108(28):11578-83.
          doi: 10.1073/pnas.1010678108pmc: PMC3136283pubmed: 21709234google scholar: lookup
        36. Leung TN, Zhang J, Lau TK, Chan LY, Lo YM. Increased maternal plasma fetal DNA concentrations in women who eventually develop preeclampsia.. Clin Chem 2001 Jan;47(1):137-9.
          pubmed: 11148193
        37. Lynch AM, Salmon JE. Dysregulated complement activation as a common pathway of injury in preeclampsia and other pregnancy complications.. Placenta 2010 Jul;31(7):561-7.
          doi: 10.1016/j.placenta.2010.03.010pmc: PMC2900404pubmed: 20427084google scholar: lookup
        38. Marcos V, Nussbaum C, Vitkov L, Hector A, Wiedenbauer EM, Roos D, Kuijpers T, Krautgartner WD, Genzel-Boroviczény O, Sperandio M, Hartl D. Delayed but functional neutrophil extracellular trap formation in neonates.. Blood 2009 Nov 26;114(23):4908-11; author reply 4911-2.
          doi: 10.1182/blood-2009-09-242388pubmed: 19965699google scholar: lookup
        39. Massberg S, Grahl L, von Bruehl ML, Manukyan D, Pfeiler S, Goosmann C, Brinkmann V, Lorenz M, Bidzhekov K, Khandagale AB, Konrad I, Kennerknecht E, Reges K, Holdenrieder S, Braun S, Reinhardt C, Spannagl M, Preissner KT, Engelmann B. Reciprocal coupling of coagulation and innate immunity via neutrophil serine proteases.. Nat Med 2010 Aug;16(8):887-96.
          doi: 10.1038/nm.2184pubmed: 20676107google scholar: lookup
        40. Mehta R, Petrova A. Intrauterine neutrophil activation is associated with pulmonary haemorrhage in preterm infants.. Arch Dis Child Fetal Neonatal Ed 2006 Nov;91(6):F415-8.
          doi: 10.1136/adc.2005.092288pmc: PMC2672745pubmed: 16705006google scholar: lookup
        41. Mellembakken JR, Aukrust P, Olafsen MK, Ueland T, Hestdal K, Videm V. Activation of leukocytes during the uteroplacental passage in preeclampsia.. Hypertension 2002 Jan;39(1):155-60.
          doi: 10.1161/hy0102.100778pubmed: 11799095google scholar: lookup
        42. Messerli M, May K, Hansson SR, Schneider H, Holzgreve W, Hahn S, Rusterholz C. Feto-maternal interactions in pregnancies: placental microparticles activate peripheral blood monocytes.. Placenta 2010 Feb;31(2):106-12.
          doi: 10.1016/j.placenta.2009.11.011pubmed: 20005571google scholar: lookup
        43. Nathan C. Neutrophils and immunity: challenges and opportunities.. Nat Rev Immunol 2006 Mar;6(3):173-82.
          doi: 10.1038/nri1785pubmed: 16498448google scholar: lookup
        44. Neeli I, Khan SN, Radic M. Histone deimination as a response to inflammatory stimuli in neutrophils.. J Immunol 2008 Feb 1;180(3):1895-902.
          pubmed: 18209087doi: 10.4049/jimmunol.180.3.1895google scholar: lookup
        45. Papayannopoulos V, Metzler KD, Hakkim A, Zychlinsky A. Neutrophil elastase and myeloperoxidase regulate the formation of neutrophil extracellular traps.. J Cell Biol 2010 Nov 1;191(3):677-91.
          doi: 10.1083/jcb.201006052pmc: PMC3003309pubmed: 20974816google scholar: lookup
        46. Pierangeli SS, Girardi G, Vega-Ostertag M, Liu X, Espinola RG, Salmon J. Requirement of activation of complement C3 and C5 for antiphospholipid antibody-mediated thrombophilia.. Arthritis Rheum 2005 Jul;52(7):2120-4.
          doi: 10.1002/art.21157pubmed: 15986360google scholar: lookup
        47. Pijnenborg R, Vercruysse L, Brosens I. Deep placentation.. Best Pract Res Clin Obstet Gynaecol 2011 Jun;25(3):273-85.
          doi: 10.1016/j.bpobgyn.2010.10.009pubmed: 21212025google scholar: lookup
        48. Plow EF. The major fibrinolytic proteases of human leukocytes.. Biochim Biophys Acta 1980 Jun 5;630(1):47-56.
          doi: 10.1016/0304-4165(80)90136-1pubmed: 6901507google scholar: lookup
        49. Powe CE, Levine RJ, Karumanchi SA. Preeclampsia, a disease of the maternal endothelium: the role of antiangiogenic factors and implications for later cardiovascular disease.. Circulation 2011 Jun 21;123(24):2856-69.
          doi: 10.1161/CIRCULATIONAHA.109.853127pmc: PMC3148781pubmed: 21690502google scholar: lookup
        50. Rana S, Powe CE, Salahuddin S, Verlohren S, Perschel FH, Levine RJ, Lim KH, Wenger JB, Thadhani R, Karumanchi SA. Angiogenic factors and the risk of adverse outcomes in women with suspected preeclampsia.. Circulation 2012 Feb 21;125(7):911-9.
          doi: 10.1161/CIRCULATIONAHA.111.054361pmc: PMC3319742pubmed: 22261192google scholar: lookup
        51. Redecha P, Tilley R, Tencati M, Salmon JE, Kirchhofer D, Mackman N, Girardi G. Tissue factor: a link between C5a and neutrophil activation in antiphospholipid antibody induced fetal injury.. Blood 2007 Oct 1;110(7):2423-31.
          doi: 10.1182/blood-2007-01-070631pmc: PMC1988945pubmed: 17536017google scholar: lookup
        52. Redman CW. Cytotrophoblasts: masters of disguise.. Nat Med 1997 Jun;3(6):610-1.
          pubmed: 9176484doi: 10.1038/nm0697-610google scholar: lookup
        53. Redman CW, Sargent IL. Latest advances in understanding preeclampsia.. Science 2005 Jun 10;308(5728):1592-4.
          doi: 10.1126/science.1111726pubmed: 15947178google scholar: lookup
        54. Redman CW, Sargent IL. Immunology of pre-eclampsia.. Am J Reprod Immunol 2010 Jun;63(6):534-43.
          doi: 10.1111/j.1600-0897.2010.00831.xpubmed: 20331588google scholar: lookup
        55. Robbins JR, Bakardjiev AI. Pathogens and the placental fortress.. Curr Opin Microbiol 2012 Feb;15(1):36-43.
          doi: 10.1016/j.mib.2011.11.006pmc: PMC3265690pubmed: 22169833google scholar: lookup
        56. Roberts JM, Hubel CA. The two stage model of preeclampsia: variations on the theme.. Placenta 2009 Mar;30 Suppl A(Suppl A):S32-7.
          doi: 10.1016/j.placenta.2008.11.009pmc: PMC2680383pubmed: 19070896google scholar: lookup
        57. Roberts JM, Redman CW. Pre-eclampsia: more than pregnancy-induced hypertension.. Lancet 1993 Jun 5;341(8858):1447-51.
          doi: 10.1016/0140-6736(93)90889-Opubmed: 8099148google scholar: lookup
        58. Rusterholz C, Hahn S, Holzgreve W. Role of placentally produced inflammatory and regulatory cytokines in pregnancy and the etiology of preeclampsia.. Semin Immunopathol 2007 Jun;29(2):151-62.
          doi: 10.1007/s00281-007-0071-6pubmed: 17621700google scholar: lookup
        59. Sacks GP, Studena K, Sargent K, Redman CW. Normal pregnancy and preeclampsia both produce inflammatory changes in peripheral blood leukocytes akin to those of sepsis.. Am J Obstet Gynecol 1998 Jul;179(1):80-6.
          pubmed: 9704769doi: 10.1016/s0002-9378(98)70254-6google scholar: lookup
        60. Saffarzadeh M, Juenemann C, Queisser MA, Lochnit G, Barreto G, Galuska SP, Lohmeyer J, Preissner KT. Neutrophil extracellular traps directly induce epithelial and endothelial cell death: a predominant role of histones.. PLoS One 2012;7(2):e32366.
          doi: 10.1371/journal.pone.0032366pmc: PMC3289648pubmed: 22389696google scholar: lookup
        61. Salamonsen LA, Lathbury LJ. Endometrial leukocytes and menstruation.. Hum Reprod Update 2000 Jan-Feb;6(1):16-27.
          doi: 10.1093/humupd/6.1.16pubmed: 10711826google scholar: lookup
        62. Salamonsen LA, Zhang J, Hampton A, Lathbury L. Regulation of matrix metalloproteinases in human endometrium.. Hum Reprod 2000 Aug;15 Suppl 3:112-9.
          pubmed: 11041227doi: 10.1093/humrep/15.suppl_3.112google scholar: lookup
        63. Salmon JE, Girardi G. Antiphospholipid antibodies and pregnancy loss: a disorder of inflammation.. J Reprod Immunol 2008 Jan;77(1):51-6.
          doi: 10.1016/j.jri.2007.02.007pmc: PMC2247372pubmed: 17418423google scholar: lookup
        64. Sasaki S, Nagata K, Kobayashi Y. Regulation of the estrous cycle by neutrophil infiltration into the vagina.. Biochem Biophys Res Commun 2009 Apr 24;382(1):35-40.
          doi: 10.1016/j.bbrc.2009.02.112pubmed: 19249292google scholar: lookup
        65. Sasaki S, Tamaki Y, Nagata K, Kobayashi Y. Regulation of the estrous cycle by neutrophils via opioid peptides.. J Immunol 2011 Jul 15;187(2):774-80.
          doi: 10.4049/jimmunol.1002489pubmed: 21677129google scholar: lookup
        66. Semeraro F, Ammollo CT, Morrissey JH, Dale GL, Friese P, Esmon NL, Esmon CT. Extracellular histones promote thrombin generation through platelet-dependent mechanisms: involvement of platelet TLR2 and TLR4.. Blood 2011 Aug 18;118(7):1952-61.
          doi: 10.1182/blood-2011-03-343061pmc: PMC3158722pubmed: 21673343google scholar: lookup
        67. Smith JM, Shen Z, Wira CR, Fanger MW, Shen L. Effects of menstrual cycle status and gender on human neutrophil phenotype.. Am J Reprod Immunol 2007 Aug;58(2):111-9.
          doi: 10.1111/j.1600-0897.2007.00494.xpubmed: 17631004google scholar: lookup
        68. Strzemienski PJ. Effect of bovine seminal plasma on neutrophil phagocytosis of bull spermatozoa.. J Reprod Fertil 1989 Nov;87(2):519-28.
          doi: 10.1530/jrf.0.0870519pubmed: 2689641google scholar: lookup
        69. Strzemienski PJ, Dyer RM, Sertich PL, Garcia MC, Kenney RM. Bactericidal activity of peripheral blood neutrophils during the oestrous cycle and early pregnancy in the mare.. J Reprod Fertil 1987 May;80(1):289-93.
          doi: 10.1530/jrf.0.0800289pubmed: 3598962google scholar: lookup
        70. von Brühl ML, Stark K, Steinhart A, Chandraratne S, Konrad I, Lorenz M, Khandoga A, Tirniceriu A, Coletti R, Köllnberger M, Byrne RA, Laitinen I, Walch A, Brill A, Pfeiler S, Manukyan D, Braun S, Lange P, Riegger J, Ware J, Eckart A, Haidari S, Rudelius M, Schulz C, Echtler K, Brinkmann V, Schwaiger M, Preissner KT, Wagner DD, Mackman N, Engelmann B, Massberg S. Monocytes, neutrophils, and platelets cooperate to initiate and propagate venous thrombosis in mice in vivo.. J Exp Med 2012 Apr 9;209(4):819-35.
          doi: 10.1084/jem.20112322pmc: PMC3328366pubmed: 22451716google scholar: lookup
        71. Wang Y, Li M, Stadler S, Correll S, Li P, Wang D, Hayama R, Leonelli L, Han H, Grigoryev SA, Allis CD, Coonrod SA. Histone hypercitrullination mediates chromatin decondensation and neutrophil extracellular trap formation.. J Cell Biol 2009 Jan 26;184(2):205-13.
          doi: 10.1083/jcb.200806072pmc: PMC2654299pubmed: 19153223google scholar: lookup
        72. Weiler H. Tracing the molecular pathogenesis of antiphospholipid syndrome.. J Clin Invest 2008 Oct;118(10):3276-8.
          doi: 10.1172/JCI37243pmc: PMC2542859pubmed: 18802489google scholar: lookup
        73. Wilkinson H. Saving mothers' lives. Reviewing maternal deaths to make motherhood safer: 2006-2008.. BJOG 2011 Oct;118(11):1402-3; discussion 1403-4.
          doi: 10.1111/j.1471-0528.2011.03097.xpubmed: 21906238google scholar: lookup
        74. Wood GA, Fata JE, Watson KL, Khokha R. Circulating hormones and estrous stage predict cellular and stromal remodeling in murine uterus.. Reproduction 2007 May;133(5):1035-44.
          doi: 10.1530/REP-06-0302pubmed: 17616732google scholar: lookup
        75. Yost CC, Cody MJ, Harris ES, Thornton NL, McInturff AM, Martinez ML, Chandler NB, Rodesch CK, Albertine KH, Petti CA, Weyrich AS, Zimmerman GA. Impaired neutrophil extracellular trap (NET) formation: a novel innate immune deficiency of human neonates.. Blood 2009 Jun 18;113(25):6419-27.
          doi: 10.1182/blood-2008-07-171629pmc: PMC2710935pubmed: 19221037google scholar: lookup
        76. Zhong XY, Gebhardt S, Hillermann R, Tofa KC, Holzgreve W, Hahn S. Parallel assessment of circulatory fetal DNA and corticotropin-releasing hormone mRNA in early- and late-onset preeclampsia.. Clin Chem 2005 Sep;51(9):1730-3.
          doi: 10.1373/clinchem.2005.053959pubmed: 16120955google scholar: lookup
        77. Zhong XY, Gebhardt S, Hillermann R, Tofa KC, Holzgreve W, Hahn S. Circulatory nucleosome levels are significantly increased in early and late-onset preeclampsia.. Prenat Diagn 2005 Aug;25(8):700-3.
          doi: 10.1002/pd.1204pubmed: 16050002google scholar: lookup
        78. Zhong XY, Holzgreve W, Hahn S. Circulatory fetal and maternal DNA in pregnancies at risk and those affected by preeclampsia.. Ann N Y Acad Sci 2001 Sep;945:138-40.
          doi: 10.1111/j.1749-6632.2001.tb03874.xpubmed: 11708467google scholar: lookup
        79. Zhong XY, Laivuori H, Livingston JC, Ylikorkala O, Sibai BM, Holzgreve W, Hahn S. Elevation of both maternal and fetal extracellular circulating deoxyribonucleic acid concentrations in the plasma of pregnant women with preeclampsia.. Am J Obstet Gynecol 2001 Feb;184(3):414-9.
          doi: 10.1067/mob.2001.109594pubmed: 11228496google scholar: lookup

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