A new role for monocytes in modulating myometrial inflammation during human labor

Biology of Reproduction

Volumn 91, Issue 1, 2014, Pages

  Srikhajon, Khetsopon ^a   Shynlova, Oksana ^c,d   Preechapornprasert, Anyarin ^b,e   Chanrachakul, Boonsri ^b,e   Lye, Stephen ^c,d  

^a Faculty of Science Mahidol University ^*  (Thailand)

^b MAHIDOL UNIVERSITY   (Thailand)

^c MOUNT SINAI HOSPITAL   (Canada)

^d UNIVERSITY OF TORONTO   (Canada)

^e BUMRUNGRAD INTERNATIONAL HOSPITAL   (Thailand)

Author keywords

chemotaxis; cytokines; labor; leukocyte infiltration; monocytes; myometrium; pregnancy; uterus

Indexed keywords

CHEMOKINE; CHEMOKINE RECEPTOR CCR2; CXCL7 CHEMOKINE; GELATINASE A; GELATINASE B; INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 18; INTERLEUKIN 6; INTERLEUKIN 8; INTERLEUKIN 9; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; MONOCYTE CHEMOTACTIC PROTEIN 3; PROTEIN CSF 3; RNA; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; CYTOKINE;

ADULT; ARTICLE; BIOPSY; CLINICAL ARTICLE; COCULTURE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOCOMPETENT CELL; INFLAMMATION; LABOR; LABOR ONSET; MONOCYTE; MYOMETRIUM; NEGATIVE FEEDBACK; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; SUPERNATANT; IMMUNOLOGY; METABOLISM; PREGNANCY;

ADULT; CYTOKINES; FEMALE; HUMANS; INFLAMMATION; LABOR, OBSTETRIC; MONOCYTES; MYOMETRIUM; PREGNANCY;

EID: 84906256965     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.113.114975     Document Type: Article

References (40)

1. Christiaens I, Zaragoza DB, Guilbert L, Robertson SA, Mitchell BF, Olson DM. Inflammatory processes in preterm and term parturition. J Reprod Immunol 2008; 79:50-57.
2. Norman JE, Bollapragada S, Yuan M, Nelson SM. Inflammatory pathways in the mechanism of parturition. BMC Pregnancy Childbirth 2007; 7(suppl 1):S7.
3. Shynlova O, Tsui P, Dorogin A, Lye SJ. Monocyte chemoattractant protein-1 (CCL-2) integrates mechanical and endocrine signals that mediate term and preterm labor. J Immunol 2008; 181:1470-1479.
4. Shynlova O, Lee YH, Srikhajon K, Lye SJ. Physiologic uterine inflammation and labor onset: integration of endocrine and mechanical signals. Reprod Sci 2013; 20:154-167.
5. Thomson AJ, Telfer JF, Young A, Campbell S, Stewart CJ, Cameron IT, Greer IA, Norman JE. Leukocytes infiltrate the myometrium during human parturition: further evidence that labour is an inflammatory process. Hum Reprod 1999; 14:229-236.
6. Osman I, Young A, Ledingham MA, Thomson AJ, Jordan F, Greer IA, Norman JE. Leukocyte density and pro-inflammatory cytokine expression in human fetal membranes, decidua, cervix and myometrium before and during labour at term. Mol Hum Reprod 2003; 9:41-45.
7. Keski-Nisula LT, Aalto ML, Kirkinen PP, Kosma VM, Heinonen ST. Myometrial inflammation in human delivery and its association with labor and infection. Am J Clin Pathol 2003; 120:217-224.
8. Bollapragada S, Youssef R, Jordan F, Greer I, Norman J, Nelson S. Term labor is associated with a core inflammatory response in human fetal membranes, myometrium, and cervix. Am J Obstet Gynecol 2009; 200: 104-111.
9. Hamilton S, Oomomian Y, Stephen G, Shynlova O, Tower CL, Garrod A, Lye SJ, Jones RL. Macrophages infiltrate the human and rat decidua during term and preterm labor: evidence that decidual inflammation precedes labor. Biol Reprod 2012; 86:39.
10. Alam R, Lett-Brown MA, Forsythe PA, Anderson-Walters DJ, Kenamore C, Kormos C, Grant JA. Monocyte chemotactic and activating factor is a potent histamine-releasing factor for basophils. J Clin Invest 1992; 89: 723-728.
11. Hunt JS, Manning LS, Mitchell D, Selanders JR, Wood GW. Localization and characterization of macrophages in murine uterus. J Leukoc Biol 1985; 38:255-265.
12. Hunt JS. Immunologically relevant cells in the uterus. Biol Reprod 1994; 50:461-466.
13. Esplin MS, Peltier MR, Hamblin S, Smith S, Fausett MB, Dildy GA, Branch DW, Silver RM, Adashi EY. Monocyte chemotactic protein-1 expression is increased in human gestational tissues during term and preterm labor. Placenta 2005; 26:661-671.
14. Orsi NM, Tribe RM. Cytokine networks and the regulation of uterine function in pregnancy and parturition. J Neuroendocrinol 2008; 20: 462-469.
15. Osmers RG, Blaser J, Kuhn W, Tschesche H. Interleukin-8 synthesis and the onset of labor. Obstet Gynecol 1995; 86:223-229.
16. Shynlova O, Nedd-Roderique T, Li Y, Dorogin A, Lye SJ. Myometrial immune cells contribute to term parturition, preterm labour and postpartum involution in mice. J Cell Mol Med 2013; 17:90-102.
17. Moser B, Wolf M, Walz A, Loetscher P. Chemokines: multiple levels of leukocyte migration control. Trends Immunol 2004; 25:75-84.
18. Berchiche YA, Gravel S, Pelletier ME, St-Onge G, Heveker N. Different effects of the different natural CC chemokine receptor 2b ligands on betaarrestin recruitment, Gai signaling, and receptor internalization. Mol Pharmacol 2011; 79:488-498.
19. Neel NF, Schutyser E, Sai J, Fan GH, Richmond A. Chemokine receptor internalization and intracellular trafficking. Cytokine Growth Factor Rev 2005; 16:637-658.
20. Zhang N, Yang D, Dong H, Chen Q, Dimitrova DI, Rogers TJ, Sitkovsky M, Oppenheim JJ. Adenosine A2a receptors induce heterologous desensitization of chemokine receptors. Blood 2006; 108:38-44.
21. Volpe S, Cameroni E, Moepps B, Thelen S, Apuzzo T, Thelen M. CCR2 acts as scavenger for CCL2 during monocyte chemotaxis. PLoS One 2012; 7:e37208.
22. Maus UA, Wellmann S, Hampl C, Kuziel WA, Srivastava M, Mack M, Everhart MB, Blackwell TS, Christman JW, Schlondorff D, Bohle RM, Seeger W, et al. CCR2-positive monocytes recruited to inflamed lungs downregulate local CCL2 chemokine levels. Am J Physiol Lung Cell Mol Physiol 2005; 288:L350-L358.
23. Menzies FM, Khan AH, Higgins CA, Nelson SM, Nibbs RJ. The chemokine receptor CCR2 is not required for successful initiation of labor in mice. Biol Reprod 2012; 86:118.
24. Moser B, Willimann K. Chemokines: role in inflammation and immune surveillance. Ann Rheum Dis 2004; 63(suppl 2):ii84-ii89.
25. Sallerfors B, Olofsson T. Granulocyte-macrophage colony-stimulating factor (GM-CSF) and granulocyte colony-stimulating factor (G-CSF) secretion by adherent monocytes measured by quantitative immunoassays. Eur J Haematol 1992; 49:199-207.
26. Kayisli UA, Mahutte NG, Arici A. Uterine chemokines in reproductive physiology and pathology. Am J Reprod Immunol 2002; 47:213-221.
27. Fitzgibbon J, Morrison JJ, Smith TJ, O'Brien M. Modulation of human uterine smooth muscle cell collagen contractility by thrombin, Y-27632, TNF alpha and indomethacin. Reprod Biol Endocrinol 2009; 7:2.
28. Bry K, Hallman M. Transforming growth factor-beta 2 prevents preterm delivery induced by interleukin-1 alpha and tumor necrosis factor-alpha in the rabbit. Am J Obstet Gynecol 1993; 168:1318-1322.
29. Winkler M, Kemp B, Fischer DC, Maul H, Hlubek M, Rath W. Tissue concentrations of cytokines in the lower uterine segment during preterm parturition. J Perinat Med 2001; 29:519-527.
30. Kemp B, Winkler M, Maas A, Maul H, Ruck P, Reineke T, Rath W. Cytokine concentrations in the amniotic fluid during parturition at term: correlation to lower uterine segment values and to labor. Acta Obstet Gynecol Scand 2002; 81:938-942.
31. Prins JR, Gomez-Lopez N, Robertson SA. Interleukin-6 in pregnancy and gestational disorders. J Reprod Immunol 2012; 95:1-14.
32. Friebe-Hoffmann U, Chiao JP, Rauk PN. Effect of IL-1beta and IL-6 on oxytocin secretion in human uterine smooth muscle cells. Am J Reprod Immunol 2001; 46:226-231.
33. Rauk PN, Friebe-Hoffmann U, Winebrenner LD, Chiao JP. Interleukin-6 up-regulates the oxytocin receptor in cultured uterine smooth muscle cells. Am J Reprod Immunol 2001; 45:148-153.
34. Robertson SA, Christiaens I, Dorian CL, Zaragoza DB, Care AS, Banks AM, Olson DM. Interleukin-6 is an essential determinant of on-time parturition in the mouse. Endocrinology 2010; 151:3996-4006.
35. Hurst SM, Wilkinson TS, McLoughlin RM, Jones S, Horiuchi S, Yamamoto N, Rose-John S, Fuller GM, Topley N, Jones SA. IL-6 and its soluble receptor orchestrate a temporal switch in the pattern of leukocyte recruitment seen during acute inflammation. Immunity 2001; 14:705-714.
36. Naugler WE, Karin M. The wolf in sheep's clothing: the role of interleukin-6 in immunity, inflammation and cancer. Trends Mol Med 2008; 14:109-119.
37. Chevalier MF, Petitjean G, Dunyach-Rémy C, Didier C, Girard PM, Manea ME, Campa P, Meyer L, Rouzioux C, Lavigne JP, Barré-Sinoussi F, Scott-Algara D, Weiss L. The Th17/Treg ratio, IL-1RA and sCD14 levels in primary HIV infection predict the T-cell activation set point in the absence of systemic microbial translocation. PLoS Pathog 2013; 9(6): e1003453.
38. Bouhlel MA, Derudas B, Rigamonti E, Dièvart R, Brozek J, Haulon S, Zawadzki C, Jude B, Torpier G, Marx N, Staels B, Chinetti-Gbaguidi G. PPARc activation primes human monocytes into alternative M2 macrophages with anti-inflammatory properties. Cell Metab 2007; 6(2): 137-143.
39. Lee Y-H, Shynlova O, Lye SJ. Mechanical stretch induces proinflammatory cytokine expression and leukocyte transendothelial migration into the myometrium. Reprod Sci 2012; 19(3 suppl):A189-A190.
40. Gomez-Lopez N, Guilbert LJ, Olson DM. Invasion of the leukocytes into the fetal-maternal interface during pregnancy. J Leukoc Biol 2010; 88: 625-633.