Lipidomic analysis of patients with microbial invasion of the amniotic cavity reveals up-regulation of leukotriene B4

FASEB Journal

Volumn 30, Issue 10, 2016, Pages 3296-3307

  Maddipati, Krishna Rao ^a,b   Romero, Roberto ^a,c,d,f   Chaiworapongsa, Tinnakorn ^a,c   Chaemsaithong, Piya ^a,c   Zhou, Sen Lin ^a,b   Xu, Zhonghui ^c   Tarca, Adi L ^b,c,e   Kusanovic, Juan Pedro ^c,g,h   Gomez, Ricardo ^h,i   Chaiyasit, Noppadol ^a,c   Honn, Kenneth V ^a  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

^c EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^d UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^e Wayne State University   (United States)

^f MICHIGAN STATE UNIVERSITY   (United States)

^g HOSPITAL DR SÓTERO DEL RÍO   (Chile)

^h PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

ⁱ Hospital Clínico La Florida   (Chile)

Author keywords

5 lipoxygenase; Amniotic Fluid; Clinical chorioamnionitis; Infection; Inflammation

Indexed keywords

5 HYDROXYICOSATETRAENOIC ACID; ARACHIDONATE 5 LIPOXYGENASE; BIOLOGICAL MARKER; LEUKOTRIENE B4;

ADULT; AMNION FLUID; ARTICLE; BACTERIAL INFECTION; CHORIOAMNIONITIS; FEMALE; HUMAN; INFLAMMATION; LABOR; LIPIDOMICS; LIQUID CHROMATOGRAPHY; MAJOR CLINICAL STUDY; MASS SPECTROMETRY; NONHUMAN; PREMATURE LABOR; PRIORITY JOURNAL; REAL TIME ULTRASOUND SCANNER; TRANSVAGINAL ECHOGRAPHY; UPREGULATION; BLOOD; GESTATIONAL AGE; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; PREGNANCY; PREGNANCY COMPLICATION; TERM BIRTH;

ADULT; AMNIOTIC FLUID; ARACHIDONATE 5-LIPOXYGENASE; BIOMARKERS; FEMALE; GESTATIONAL AGE; HUMANS; LABOR, OBSTETRIC; LEUKOTRIENE B4; OBSTETRIC LABOR, PREMATURE; PREGNANCY; PREGNANCY COMPLICATIONS, INFECTIOUS; TERM BIRTH; UP-REGULATION;

EID: 84990863997     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.201600583R     Document Type: Article

References (91)

1. Romero, R., Dey, S. K., and Fisher, S. J. (2014) Preterm labor: one syndrome, many causes. Science 345, 760-765
2. Gravett, M. G., Hummel, D., Eschenbach, D. A., and Holmes, K. K. (1986) Preterm labor associated with subclinical amniotic fluid infection and with bacterial vaginosis. Obstet. Gynecol. 67, 229-237
3. Gibbs, R. S., Romero, R., Hillier, S. L., Eschenbach, D. A., and Sweet, R. L. (1992) A review of premature birth and subclinical infection. Am. J. Obstet. Gynecol. 166, 1515-1528
4. Yoon, B.H.,Romero,R.,Moon, J.B., Shim, S. S.,Kim,M.,Kim,G., and Jun, J. K. (2001) Clinical significance of intra-Amniotic inflammation in patients with preterm labor and intact membranes. Am. J. Obstet. Gynecol. 185, 1130-1136
5. Romero, R., Miranda, J., Chaiworapongsa, T., Korzeniewski, S. J., Chaemsaithong, P., Gotsch, F., Dong, Z., Ahmed, A. I., Yoon, B. H., Hassan, S. S., Kim, C. J., and Yeo, L. (2014) Prevalence and clinical significance of sterile intra-Amniotic inflammation in patients with preterm labor and intact membranes. Am. J. Reprod. Immunol. 72, 458-474
6. Combs, C. A., Gravett, M., Garite, T. J., Hickok, D. E., Lapidus, J., Porreco, R., Rael, J., Grove, T., Morgan, T. K., Clewell, W., Miller,H., Luthy, D., Pereira, L., Nageotte, M., Robilio, P. A., Fortunato, S., Simhan, H., Baxter, J. K., Amon, E., Franco, A., Trofatter, K., and Heyborne, K. (2014) Amniotic fluid infection, inflammation, and colonization in preterm labor with intact membranes. Am. J. Obstet. Gynecol. 210, 125.e121-125.e115
7. Cobo, T., Kacerovsky, M., and Jacobsson, B. (2014) Amniotic fluid infection, inflammation, and colonization in preterm labor with intact membranes. Am. J. Obstet. Gynecol. 211, 708
8. Gibbs, R. S., Dinsmoor, M. J., Newton, E. R., and Ramamurthy, R. S. (1988) A randomized trial of intrapartum versus immediate postpartum treatment of women with intra-Amniotic infection. Obstet. Gynecol. 72, 823-828
9. National Institute of Child Health and Human Development Maternal-Fetal Medicine Units Network. (1997) Antibiotic therapy for reduction of infantmorbidity after preterm premature rupture of the membranes. A randomized controlled trial. JAMA 278, 989-995
10. Lee, J., Romero, R., Kim, S.M., Chaemsaithong, P., Park, C. W., Park, J. S., Jun, J. K., and Yoon, B.H. (2016) A new antibiotic regimen treats and prevents intra-Amniotic inflammation/infection in patients with preterm PROM. J. Matern. Fetal Neonatal Med. 29, 707-720
11. Funk, C. D. (2001) Prostaglandins and leukotrienes: advances in eicosanoid biology. Science 294, 1871-1875
12. Harris, S. G., Padilla, J., Koumas, L., Ray, D., and Phipps, R. P. (2002) Prostaglandins as modulators of immunity. Trends Immunol. 23, 144-150
13. Serhan, C. N., and Savill, J. (2005) Resolution of inflammation: the beginning programs the end. Nat. Immunol. 6, 1191-1197
14. Serhan, C. N., Chiang, N., and Van Dyke, T. E. (2008) Resolving inflammation: dual anti-inflammatory and pro-resolution lipid mediators. Nat. Rev. Immunol. 8, 349-361
15. Serhan, C. N. (2008) Systems approach with inflammatory exudates uncovers novel anti-inflammatory and pro-resolving mediators. Prostaglandins Leukot. Essent. Fatty Acids 79, 157-163
16. Shimizu, T. (2009) Lipid mediators in health and disease: enzymes and receptors as therapeutic targets for the regulation of immunity and inflammation. Annu. Rev. Pharmacol. Toxicol. 49, 123-150
17. Ricciotti, E., and FitzGerald, G. A. (2011) Prostaglandins and inflammation. Arterioscler. Thromb. Vasc. Biol. 31, 986-1000
18. Chiang, N., Fredman, G., Bäckhed, F.,Oh, S. F., Vickery, T., Schmidt, B. A., and Serhan, C. N. (2012) Infection regulates pro-resolving mediators that lower antibiotic requirements. Nature 484, 524-528
19. Buckley, C. D., Gilroy, D. W., and Serhan, C. N. (2014) Proresolving lipid mediators and mechanisms in the resolution of acute inflammation. Immunity 40, 315-327
20. Karim, S.M. (1971)The role of prostaglandins in human parturition. Proc. R. Soc. Med. 64, 10-12
21. Mitchell, M. D. (1981) Prostaglandins during pregnancy and the perinatal period. J. Reprod. Fertil. 62, 305-315
22. Nieder, J., and Augustin, W. (1983) Increase of prostaglandin E and F equivalents in amniotic fluid during late pregnancy and rapid PG F elevation after cervical dilatation. Prostaglandins Leukot.Med. 12, 289-297
23. Berryman, G.K., Strickland, D.M.,Hankins, G.D., and Mitchell,M. D. (1987) Amniotic fluid prostaglandin D2 in spontaneous and augmented labor. Life Sci. 41, 1611-1614
24. Romero, R., Gonzalez, R., Baumann, P., Behnke, E., Rittenhouse, L., Barberio, D., Cotton, D. B., and Mitchell, M. D. (1994) Topographic differences in amniotic fluid concentrations of prostanoids in women in spontaneous labor at term. Prostaglandins Leukot. Essent. Fatty Acids 50, 97-104
25. Romero, R., Baumann, P., Gonzalez, R., Gomez, R., Rittenhouse, L., Behnke, E., and Mitchell, M. D. (1994) Amniotic fluid prostanoid concentrations increase early during the course of spontaneous labor at term. Am. J. Obstet. Gynecol. 171, 1613-1620
26. Mitchell, M. D., Romero, R. J., Edwin, S. S., and Trautman, M. S. (1995) Prostaglandins and parturition. Reprod. Fertil. Dev. 7, 623-632
27. Romero, R.,Munoz,H., Gomez, R., Parra,M., Polanco,M., Valverde, V., Hasbun, J., Garrido, J., Ghezzi, F., Mazor, M., Tolosa, J. E., and Mitchell, M. D. (1996) Increase in prostaglandin bioavailability precedes the onset of human parturition. ProstaglandinsLeukot. Essent. Fatty Acids 54, 187-191
28. Gibb, W. (1998) The role of prostaglandins in human parturition. Ann. Med. 30, 235-241
29. Keelan, J. A.,Blumenstein,M., Helliwell,R. J., Sato,T.A.,Marvin,K. W., and Mitchell, M. D. (2003) Cytokines, prostaglandins and parturition: a review. Placenta 24(Suppl A), S33-S46 doi:10.1053/plac.2002.0948
30. Olson, D. M. (2003) The role of prostaglandins in the initiation of parturition. Best Pract. Res. Clin. Obstet. Gynaecol. 17, 717-730
31. Mitchell, M. D., Chang, M. C., Chaiworapongsa, T., Lan, H. Y., Helliwell, R. J., Romero, R., and Sato, T. A. (2005) Identification of 9alpha,11beta-prostaglandin F2 in human amniotic fluid and characterization of its production by human gestational tissues. J. Clin. Endocrinol. Metab. 90, 4244-4248
32. Lee, S. E., Romero, R., Park, I. S., Seong,H. S., Park, C. W., and Yoon, B. H. (2008) Amniotic fluid prostaglandin concentrations increase before the onset of spontaneous labor at term. J.Matern. Fetal Neonatal Med. 21, 89-94
33. Menon, R., Fortunato, S. J., Milne, G. L., Brou, L., Carnevale, C., Sanchez, S. C., Hubbard, L., Lappas, M., Drobek, C. O., and Taylor, R. N. (2011) Amniotic fluid eicosanoids in preterm and term births: effects of risk factors for spontaneous preterm labor. Obstet. Gynecol. 118, 121-134
34. Romero, R., Quintero, R., Emamian, M., Wan, M., Grzyboski, C., Hobbins, J.C., and Mitchell,M. D. (1987)Arachidonate lipoxygenase metabolites in amniotic fluid of women with intra-Amniotic infection and preterm labor. Am. J. Obstet. Gynecol. 157, 1454-1460
35. Van der Elst,C. W., Ĺopez Bernal, A., and Sinclair-Smith, C. C. (1991) The role of chorioamnionitis and prostaglandins in preterm labor. Obstet. Gynecol. 77, 672-676
36. Hsu, C. D., Meaddough, E., Aversa, K., Hong, S. F., Lee, I. S., Bahodo-Singh, R.O., Lu, L. C., and Copel, J.A. (1998) Dual roles of amniotic fluid nitric oxide and prostaglandin E2 in preterm labor with intra-Amniotic infection. Am. J. Perinatol. 15, 683-687
37. Romero, R., Miranda, J., Chaiworapongsa, T., Chaemsaithong, P., Gotsch, F.,Dong,Z.,Ahmed,A. I., Yoon, B.H.,Hassan, S. S.,Kim,C. J., Korzeniewski, S. J., and Yeo, L. (2014) A novel molecular microbiologic technique for the rapid diagnosis of microbial invasion of the amniotic cavity and intra-Amniotic infection in preterm labor with intact membranes. Am. J. Reprod. Immunol. 71, 330-358
38. Romero, R., Miranda, J., Kusanovic, J. P., Chaiworapongsa, T., Chaemsaithong, P., Martinez, A., Gotsch, F.,Dong, Z., Ahmed, A. I., Shaman, M., Lannaman, K., Yoon, B. H., Hassan, S. S., Kim, C. J., Korzeniewski, S. J., Yeo, L., and Kim, Y. M. (2015) Clinical chorioamnionitis at term I: microbiology of the amniotic cavity using cultivation andmolecular techniques. J. Perinat. Med. 43, 19-36
39. Romero, R., Chaemsaithong, P., Korzeniewski, S. J., Tarca, A. L., Bhatti, G., Xu, Z., Kusanovic, J. P., Dong, Z., Docheva, N., Martinez-Varea, A., Yoon, B. H., Hassan, S. S., Chaiworapongsa, T., and Yeo, L. (2016) Clinical chorioamnionitis at term II: the intraamniotic inflammatory response. J. Perinat. Med. 44, 5-22
40. Romero, R., Chaemsaithong, P., Korzeniewski, S. J., Kusanovic, J. P., Docheva, N., Martinez-Varea, A., Ahmed, A. I., Yoon, B. H., Hassan, S. S., Chaiworapongsa, T., and Yeo, L. (2016) Clinical chorioamnionitis at term III: how well do clinical criteria perform in the identification of proven intra-Amniotic infection? J. Perinat. Med. 44, 23-32
41. Romero, R., Chaemsaithong, P., Docheva, N., Korzeniewski, S. J., Tarca, A. L., Bhatti, G., Xu, Z., Kusanovic, J. P., Dong, Z., Chaiyasit,N., Ahmed,A. I., Yoon, B. H., Hassan, S. S., Chaiworapongsa, T., and Yeo, L. (2016) Clinical chorioamnionitis at term IV: the maternal plasma cytokine profile. J. Perinat. Med. 44, 77-98
42. Romero, R., Chaemsaithong, P., Docheva, N., Korzeniewski, S. J., Tarca, A. L., Bhatti, G.,Xu, Z., Kusanovic, J. P., Chaiyasit,N., Dong, Z., Yoon,B.H.,Hassan, S. S., Chaiworapongsa, T.,Yeo, L., and Kim, Y.M. (2016) Clinical chorioamnionitis at term V: umbilical cord plasma cytokine profile in the context of a systemic maternal inflammatory response. J. Perinat. Med. 44, 53-76
43. Romero, R., Chaemsaithong, P., Docheva, N., Korzeniewski, S. J., Kusanovic, J. P., Yoon, B. H., Kim, J. S., Chaiyasit, N., Ahmed, A. I., Qureshi, F., Jacques, S. M., Kim,C. J.,Hassan, S. S., Chaiworapongsa, T., Yeo,L., and Kim, Y.M. (2016)Clinical chorioamnionitis at termVI: acute chorioamnionitis and funisitis according to the presence or absence ofmicroorganisms and inflammation in the amniotic cavity. J. Perinat. Med. 44, 33-51
44. Gervasi,M.T., Romero, R., Bracalente,G., Erez, O.,Dong, Z., Hassan, S. S., Yeo, L., Yoon, B. H., and Chaiworapongsa, T. (2012) Midtrimester amniotic fluid concentrations of interleukin-6 and interferon-gamma-inducible protein-10: evidence for heterogeneity of intra-Amniotic inflammation and associations with spontaneous early (,32 weeks) and late (.32 weeks) preterm delivery. J. Perinat. Med. 40, 329-343
45. Chaemsaithong, P., Romero, R., Korzeniewski, S. J., Dong, Z., Yeo, L., Hassan, S. S., Kim, Y.M., Yoon, B.H., and Chaiworapongsa, T. (2015) A point of care test for the determination of amniotic fluid interleukin-6 and the chemokine CXCL-10/IP-10. J. Matern. Fetal Neonatal Med. 28, 1510-1519
46. Andersen,H. F.,Nugent,C.E.,Wanty, S. D., and Hayashi,R.H. (1990) Prediction of risk for preterm delivery by ultrasonographic measurement of cervical length. Am. J. Obstet. Gynecol. 163, 859-867
47. National Institute of Child Health and Human Development Maternal FetalMedicineUnitNetwork. (1996)The length of the cervix and the risk of spontaneous premature delivery. N. Engl. J. Med. 334, 567-573
48. Romero, R.,Quintero, R., Nores, J., Avila, C.,Mazor,M.,Hanaoka, S., Hagay, Z., Merchant, L., and Hobbins, J. C. (1991) Amniotic fluid white blood cell count: a rapid and simple test to diagnosemicrobial invasion of the amniotic cavity and predict preterm delivery. Am. J. Obstet. Gynecol. 165, 821-830
49. Romero,R., Jimenez,C., Lohda,A.K.,Nores, J.,Hanaoka, S.,Avila,C., Callahan, R., Mazor, M., Hobbins, J. C., and Diamond, M. P. (1990) Amniotic fluid glucose concentration: a rapid and simplemethod for thedetectionof intraamniotic infectioninpretermlabor.Am. J.Obstet. Gynecol. 163, 968-974
50. Romero, R., Emamian, M., Quintero, R., Wan, M., Hobbins, J. C., Mazor, M., and Edberg, S. (1988) The value and limitations of the Gram stain examination in the diagnosis of intraamniotic infection. Am. J. Obstet. Gynecol. 159, 114-119
51. Eshoo, M. W., Crowder, C. C., Rebman, A. W., Rounds, M. A., Matthews,H.E., Picuri, J.M., Soloski,M. J., Ecker, D. J., Schutzer, S. E., and Aucott, J. N. (2012) Direct molecular detection and genotyping of Borrelia burgdorferi fromwhole blood of patients with early Lyme disease. PLoS One 7, e36825
52. Shin, J.H.,Ranken, R., Sefers, S. E., Lovari, R.,Quinn, C. D.,Meng, S., Carolan, H. E., Toleno, D., Li, H., Lee, J. N., Stratton, C. W., Massire, C., and Tang, Y. W. (2013) Detection, identification, and distribution of fungi in bronchoalveolar lavage specimens by use of multilocus PCR coupled with electrospray ionization/mass spectrometry. J. Clin. Microbiol. 51, 136-141
53. Ecker, D. J., Sampath, R., Li, H., Massire, C., Matthews, H. E., Toleno, D., Hall, T. A., Blyn, L. B., Eshoo, M. W., Ranken, R., Hofstadler, S. A., and Tang, Y. W. (2010) New technology for rapid molecular diagnosis of bloodstream infections. Expert Rev. Mol. Diagn. 10, 399-415
54. Metzgar,D., Frinder,M.,Lovari,R.,Toleno,D.,Massire,C.,Blyn,L.B., Ranken, R., Carolan, H. E., Hall, T. A., Moore, D., Hansen, C. J., Sampath, R., and Ecker, D. J. (2013) Broad-spectrum biosensor capable of detecting and identifying diverse bacterial and Candida species in blood. J. Clin. Microbiol. 51, 2670-2678
55. Maddipati, K. R., and Zhou, S. L. (2011) Stability and analysis of eicosanoids and docosanoids in tissue culture media. Prostaglandins Other Lipid Mediat. 94, 59-72
56. Maddipati,K.R.,Romero,R.,Chaiworapongsa,T., Zhou, S.L.,Xu, Z., Tarca, A. L., Kusanovic, J. P., Munoz, H., and Honn, K. V. (2014) Eicosanomic profiling reveals dominance of the epoxygenase pathway in human amniotic fluid at term in spontaneous labor. FASEB J. 28, 4835-4846
57. Benjamini, Y., and Hochberg, Y. (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. B 57, 289-300
58. Henningsen, A. (2011) censReg: Censored Regression (Tobit) Models. pp. R package, Version 0.5, http://CRAN.R-project.org/package=censReg
59. Liggins, G. (1981) Cervical ripening as an inflammatory reaction. In The Cervix in Pregnancy and Labor: Clinical and Biochemical Investigations (Ellwood, E., and Anderson, A., eds), pp. 1-9, Churchill Livingstone, Edinburgh, UK
60. Osman, I., Young, A., Ledingham, M. A., Thomson, A. J., Jordan, F., Greer, I. A., and Norman, J. E. (2003) Leukocyte density and proinflammatory cytokine expression in human fetal membranes, decidua, cervix andmyometriumbefore and during labour at term. Mol. Hum. Reprod. 9, 41-45
61. Gomez-Lopez, N., Estrada-Gutierrez, G., Jimenez-Zamudio, L., Vega-Sanchez, R., and Vadillo-Ortega, F. (2009) Fetal membranes exhibit selective leukocyte chemotaxic activity during human labor. J. Reprod. Immunol. 80, 122-131
62. Gomez-Lopez, N., Vadillo-Perez, L., Nessim, S., Olson, D. M., and Vadillo-Ortega, F. (2011) Choriodecidua and amnion exhibit selective leukocyte chemotaxis during term human labor. Am. J. Obstet. Gynecol. 204, 364.e369-364.e316
63. Romero, R., Brody, D.T.,Oyarzun, E.,Mazor,M.,Wu, Y.K.,Hobbins, J. C., and Durum, S. K. (1989) Infection and labor: III, interleukin-1: a signal for the onset of parturition. Am. J. Obstet. Gynecol. 160, 1117-1123
64. Romero, R., Mazor, M., Brandt, F., Sepulveda, W., Avila, C., Cotton, D.B., and Dinarello,C.A. (1992) Interleukin-1 alpha and interleukin-1beta inpretermandtermhumanparturition.Am. J.Reprod. Immunol. 27, 117-123
65. Romero,R., Sepulveda,W.,Kenney, J. S.,Archer,L.E.,Allison, and A.C., Sehgal, P. B. (1992) Interleukin 6 determination in the detection of microbial invasionof the amniotic cavity.Ciba Found. Symp. 167, 205-220; discussion 220-203
66. Andrews,W.W.,Hauth, J. C.,Goldenberg, R. L., Gomez, R., Romero, R., and Cassell, G.H. (1995) Amniotic fluid interleukin-6: correlation with upper genital tractmicrobial colonization and gestational age in women delivered after spontaneous labor versus indicated delivery. Am. J. Obstet. Gynecol. 173, 606-612
67. Romero, R.,Mazor, M., Sepulveda, W., Avila, C., Copeland, D., and Williams, J. (1992) Tumor necrosis factor in pretermand term labor. Am. J. Obstet. Gynecol. 166, 1576-1587
68. Maymon, E., Ghezzi, F., Edwin, S. S.,Mazor,M., Yoon, B. H., Gomez, R., and Romero, R. (1999) The tumor necrosis factor alpha and its soluble receptor profile in term and preterm parturition.Am. J.Obstet. Gynecol. 181, 1142-1148
69. Romero, R., Ceska, M., Avila, C., Mazor, M., Behnke, E., and Lindley, I. (1991) Neutrophil attractant/activating peptide-1/interleukin-8 in term and preterm parturition. Am. J. Obstet. Gynecol. 165, 813-820
70. Saito, S., Kasahara, T., Kato, Y., Ishihara, Y., and Ichijo, M. (1993) Elevation of amniotic fluid interleukin 6 (IL-6), IL-8 and granulocyte colony stimulating factor (G-CSF) in term and preterm parturition. Cytokine 5, 81-88
71. Esplin,M. S.,Romero, R., Chaiworapongsa,T.,Kim, Y.M.,Edwin, S., Gomez, R., Gonzalez, R., and Adashi, E. Y. (2003) Amniotic fluid levels of immunoreactive monocyte chemotactic protein-1 increase during term parturition. J. Matern. Fetal Neonatal Med. 14, 51-56
72. Shynlova, O., Tsui, P., Dorogin, A., and Lye, S. J. (2008) Monocyte chemoattractant protein-1 (CCL-2) integrates mechanical and endocrine signals that mediate termand pretermlabor. J. Immunol. 181, 1470-1479
73. Strickland, D. M., Saeed, S. A., Casey, M. L., and Mitchell, M. D. (1983) Stimulation of prostaglandin biosynthesis by urine of the human fetus may serve as a trigger for parturition. Science 220, 521-522
74. Lee, S. E., Park, I. S., Romero, R., and Yoon, B. H. (2009) Amniotic fluid prostaglandin F2 increases even in sterile amniotic fluid and is an independent predictor of impending delivery in preterm premature rupture of membranes. J. Matern. Fetal Neonatal Med. 22, 880-886
75. Romero, R., Miranda, J., Chaiworapongsa, T., Chaemsaithong, P., Gotsch, F.,Dong,Z.,Ahmed,A. I., Yoon, B.H.,Hassan, S. S.,Kim,C. J., Korzeniewski, S. J., Yeo, L., and Kim, Y. M. (2015) Sterile intraamniotic inflammation in asymptomatic patients with a sonographic short cervix: prevalence and clinical significance. J. Matern. Fetal Neonatal Med. 28, 1394-1409
76. Samuelsson, B. (1983) Leukotrienes: mediators of immediate hypersensitivity reactions and inflammation. Science 220, 568-575
77. Kumlin, M., Falck, J. R., Raud, J., Harada, Y., Dahlén, S. E., and Granström, E. (1990) Identification and biological activity of dihydroleukotriene B4: a prominent metabolite of leukotriene B4 in the human lung. Biochem. Biophys. Res. Commun. 170, 23-29
78. Ford-Hutchinson, A. W. (1990) LeukotrieneB4 in inflammation. Crit. Rev. Immunol. 10, 1-12
79. Zarini, S., Gijón, M. A., Ransome, A. E., Murphy, R. C., and Sala, A. (2009) Transcellular biosynthesis of cysteinyl leukotrienes in vivo duringmouse peritoneal inflammation. Proc. Natl. Acad. Sci. USA 106, 8296-8301
80. Grant, G. E., Rokach, J., and Powell, W. S. (2009) 5-Oxo-ETE and the OXE receptor. Prostaglandins Other Lipid Mediat. 89, 98-104
81. Peters-Golden, M., Canetti, C., Mancuso, P., and Coffey, M. J. (2005) Leukotrienes: underappreciated mediators of innate immune responses. J. Immunol. 174, 589-594
82. Nakamura, M., and Shimizu, T. (2011) Leukotriene receptors. Chem. Rev. 111, 6231-6298
83. O'Flaherty, J. T., Taylor, J. S., and Thomas,M. J. (1998) Receptors for the 5-oxo class of eicosanoids in neutrophils. J. Biol. Chem. 273, 32535-32541
84. Jones, C. E., Holden, S., Tenaillon, L., Bhatia, U., Seuwen, K., Tranter, P., Turner, J., Kettle, R., Bouhelal, R., Charlton, S., Nirmala, N. R., Jarai, G., and Finan, P. (2003) Expression and characterization of a 5-oxo-6E,8Z,11Z,14Z-eicosatetraenoic acid receptor highly expressed on human eosinophils and neutrophils. Mol. Pharmacol. 63, 471-477
85. Patel, P., Cossette, C., Anumolu, J. R., Erlemann, K.-R., Grant, G. E., Rokach, J., and Powell, W. S. (2009) Substrate selectivity of 5-hydroxyeicosanoiddehydrogenase andits inhibitionby 5-hydroxy-D6-long-chain fatty acids. J. Pharmacol. Exp. Ther. 329, 335-341
86. Bowers, R. C., Hevko, J., Henson, P. M., and Murphy, R. C. (2000) A novel glutathione containing eicosanoid (FOG7) chemotactic for human granulocytes. J. Biol. Chem. 275, 29931-29934
87. Hevko, J. M., and Murphy, R. C. (2002) Formation of murine macrophage-derived 5-oxo-7-glutathionyl-8,11,14-eicosatrienoic acid (FOG7) is catalyzed by leukotriene C4 synthase. J. Biol. Chem. 277, 7037-7043
88. Lee, T. H., Horton, C. E., Kyan-Aung, U., Haskard, D., Crea, A. E., and Spur, B. W. (1989) Lipoxin A4 and lipoxin B4 inhibit chemotactic responses of human neutrophils stimulated by leukotriene B4 and N-formyl-L-methionyl-L-leucyl-L-phenylalanine. Clin. Sci. 77, 195-203
89. Serhan, C. N. (1994) Lipoxin biosynthesis and its impact in inflammatory and vascular events. Biochim. Biophys. Acta 1212, 1-25
90. Papayianni, A., Serhan, C. N., and Brady, H. R. (1996) Lipoxin A4 and B4 inhibit leukotriene-stimulated interactions of human neutrophils and endothelial cells. J. Immunol. 156, 2264-2272
91. Serhan, C. N. (2005) Lipoxins and aspirin-triggered 15-epi-lipoxins are the first lipid mediators of endogenous anti-inflammation and resolution. Prostaglandins Leukot. Essent. Fatty Acids 73, 141-162