Monocyte chemoattractant protein-1 (CCL-2) integrates mechanical and endocrine signals that mediate term and preterm labor

Journal of Immunology

Volumn 181, Issue 2, 2008, Pages 1470-1479

  Shynlova, Oksana ^a   Tsui, Prudence ^a,b   Dorogin, Anna ^a   Lye, Stephen J ^a,b  

^a MOUNT SINAI HOSPITAL   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; MIFEPRISTONE; MONOCYTE CHEMOTACTIC PROTEIN 1; PROGESTERONE; PROGESTERONE RECEPTOR; RNA; HORMONE ANTAGONIST;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ELONGATION; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FETUS CONTROL; FETUS GROWTH; GENE EXPRESSION; IN VIVO STUDY; MALE; MECHANICAL STRESS; MYOMETRIUM; NONHUMAN; PREGNANCY; PREMATURE LABOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; RAT; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; UPREGULATION; UTERUS; ANIMAL; CYTOLOGY; DRUG ANTAGONISM; IMMUNOLOGY; LABOR; MACROPHAGE; METABOLISM; WISTAR RAT;

ANIMALS; CHEMOKINE CCL2; FEMALE; GRAVIDITY; HORMONE ANTAGONISTS; LABOR, OBSTETRIC; MACROPHAGES; MIFEPRISTONE; MYOMETRIUM; OBSTETRIC LABOR, PREMATURE; PREGNANCY; PROGESTERONE; RATS; RATS, WISTAR; SIGNAL TRANSDUCTION; UP-REGULATION;

EID: 49049111873     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.181.2.1470     Document Type: Article

References (54)

1. Sacks, G. P., K. Studena, K. Sargent, and C. W. Redman. 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.
2. Osman, I., A. Young, M. A. Ledingham, A. J. Thomson, F. Jordan, I. A. Greer, and J. E. Norman. 2003. Leukocyte density and pro-inflammatory cytokine expression in human fetal membranes, decidua, cervix and myometrium before and during labour at term. Mol. Hum. Reprod. 9: 41-45. (Pubitemid 36285142)
3. Keski-Nisula, L. T., M. L. Aalto, P. P. Kirkinen, V. M. Kosma, and S. T. Heinonen. 2003. Myometrial inflammation in human delivery and its association with labor and infection. Am. J. Clin. Pathol. 120: 217-224.
4. Young, A., A. J. Thomson, M. Ledingham, F. Jordan, I. A. Greer, and J. E. Norman. 2002. Immunolocalization of proinflammatory cytokines in myometrium, cervix, and fetal membranes during human parturition at term. Biol. Reprod. 66: 445-449. (Pubitemid 34101843)
5. Romero, R., J. Espinoza, L. F. Goncalves, J. P. Kusanovic, L. A. Friel, and J. K. Nien. 2006. Inflammation in preterm and term labour and delivery. Semin. Fetal Neonatal Med. 11: 317-326. (Pubitemid 44038705)
6. Thomson, A. J., J. F. Telfer, A. Young, S. Campbell, C. J. Stewart, I. T. Cameron, I. A. Greer, and J. E. Norman. 1999. Leukocytes infiltrate the myometrium during human parturition: further evidence that labour is an inflammatory process. Hum. Reprod. 14: 229-236.
7. Romero, R., R. Gomez, T. Chaiworapongsa, G. Conoscenti, J. C. Kim, and Y. M. Kim. 2001. The role of infection in preterm labour and delivery. Paediatr. Perinat. Epidemiol. 15(Suppl. 2): 41-56. (Pubitemid 33719617)
8. Keelan, J. A., M. Blumenstein, R. J. Helliwell, T. A. Sato, K. W. Marvin, and M. D. Mitchell. 2003. Cytokines, prostaglandins and parturition: a review. Placenta 24(Suppl. A): S33-S46.
9. Hunt, J. S. 1994. Immunologically relevant cells in the uterus. Biol. Reprod. 50: 461-466.
10. Hunt, J. S., L. S. Manning, D. Mitchell, J. R. Selanders, and G. W. Wood. 1985. Localization and characterization of macrophages in murine uterus. J. Leukocyte Biol. 38: 255-265.
11. Bulmer, J. N., and P. M. Johnson. 1984. Macrophage populations in the human placenta and amniochorion. Clin. Exp. Immunol. 57: 393-403.
12. Mackler, A. M., G. Iezza, M. R Akin, P. McMillan, and S. M. Yellon. 1999. Macrophage trafficking in the uterus and cervix precedes parturition in the mouse. Biol. Reprod. 61: 879-883.
13. Esplin, M. S., M. R. Peltier, S. Hamblin, S. Smith, M. B. Fausett, G. A. Dildy, D. W. Branch, R. M. Silver, and E. Y. Adashi. 2005. Monocyte chemotactic protein-1 expression is increased in human gestational tissues during term and preterm labor. Placenta 26: 661-671.
14. Esplin, M. S., R. Romero, T. Chaiworapongsa, Y. M. Kim, S. Edwin, R. Gomez, M. Mazor, and E. Y. Adashi. 2005. Monocyte chemotactic protein-1 is increased in the amniotic fluid of women who deliver preterm in the presence or absence of intra-amniotic infection. J. Matern. Fetal Neonatal Med. 17: 365-373.
15. Esplin, M. S., R. Romero, T. Chaiworapongsa, Y. M. Kim, S. Edwin, R. Gomez, R. Gonzalez, and E. Y. Adashi. 2003. Amniotic fluid levels of immunoreactive monocyte chemotactic protein-1 increase during term parturition. J. Matern. Fetal Neonatal Med. 14: 51-56.
16. Jacobsson, B., R. M. Holst, U. B. Wennerholm, B. Andersson, H. Lilja, and H. Hagberg. 2003. Monocyte chemotactic protein-1 in cervical and amniotic fluid: relationship to microbial invasion of the amniotic cavity, intra-amniotic inflammation, and preterm delivery. Am. J. Obstet. Gynecol. 189: 1161-1167. (Pubitemid 37373914)
17. Gruden, G., G. Setti, A. Hayward, D. Sugden, S. Duggan, D. Burt, R. E. Buckingham, L. Gnudi, and G. Viberti. 2005. Mechanical stretch induces monocyte chemoattractant activity via an NF-κB-dependent monocyte chemoattractant protein-1-mediated pathway in human mesangial cells: inhibition by rosiglitazone. J. Am. Soc. Nephrol. 16: 688-696. (Pubitemid 41725105)
18. Lockwood, C. J., P. Matta, G. Krikun, L. A. Koopman, R. Masch, P. Toti, F. Arcuri, S. T. Huang, E. F. Funai, and F. Schatz. 2006. Regulation of monocyte chemoattractant protein-1 expression by tumor necrosis factor-α and interleukin- 1β in first trimester human decidual cells: implications for preeclampsia. Am. J. Pathol. 168: 445-452.
19. He, Y. Y., M. R. Du, P. F. Guo, X. J. He, W. H. Zhou, X. Y. Zhu, and D. J. Li. 2007. Regulation of C-C motif chemokine ligand 2 and its receptor in human decidual stromal cells by pregnancy-associated hormones in early gestation. Hum. Reprod. 22: 2733-2742.
20. De Rossi, M., P. Bernasconi, F. Baggi, M. R. de Waal, and R. Mantegazza. 2000. Cytokines and chemokines are both expressed by human myoblasts: possible relevance for the immune pathogenesis of muscle inflammation. Int. Immunol. 12: 1329-1335. (Pubitemid 30657777)
21. Yoshimura, T., E. A. Robinson, S. Tanaka, E. Appella, J. Kuratsu, and E. J. Leonard. 1989. Purification and amino acid analysis of two human gliomaderived monocyte chemoattractants. J. Exp. Med. 169: 1449-1459. (Pubitemid 19104974)
22. Shynlova, O., P. Tsui, A. Dorogin, B. L. Langille, and S. J. Lye. 2007. Insulinlike growth factors and their binding proteins define specific phases of myometrial differentiation during pregnancy in the rat. Biol. Reprod. 76: 571-578. (Pubitemid 46466513)
23. Shynlova, O., J. A. Mitchell, A. Tsampalieros, B. L. Langille, and S. J. Lye. 2004. Progesterone and gravidity differentially regulate expression of extracellular matrix components in the pregnant rat myometrium. Biol. Reprod. 70: 986-992. (Pubitemid 38387707)
24. Shynlova, O., P. Tsui, A. Dorogin, B. L. Langille, and S. J. Lye. 2007. The expression of transforming growth factor β in pregnant rat myometrium is hormone and stretch dependent. Reproduction 134: 503-511. (Pubitemid 47386897)
25. Mitchell, J. A., and S. J. Lye. 2002. Differential expression of activator protein-1 transcription factors in pregnant rat myometrium. Biol. Reprod. 67: 240-246.
26. Ou, C. W., Z. Q. Chen, S. Qi, and S. J. Lye. 1998. Increased expression of the rat myometrial oxytocin receptor messenger ribonucleic acid during labor requires both mechanical and hormonal signals. Biol. Reprod. 59: 1055-1061.
27. Piersanti, M., and S. J. Lye. 1995. Increase in messenger ribonucleic acid encoding the myometrial gap junction protein, connexin-43, requires protein synthesis and is associated with increased expression of the activator protein-1, c-fos. Endocrinology 136: 3571-3578.
28. Shynlova, O. P., A. D. Oldenhof, M. Liu, L. Langille, and S. J. Lye. 2002. Regulation of c-fos expression by static stretch in rat myometrial smooth muscle cells. Am. J. Obstet. Gynecol. 186: 1358-1365.
29. Oldenhof, A. D., O. P. Shynlova, M. Liu, B. L. Langille, and S. J. Lye. 2002. Mitogen-activated protein kinases mediate stretch-induced c-fos mRNA expression in myometrial smooth muscle cells. Am. J. Physiol. 283: C1530-C1539.
30. Mitchell, J. A., O. Shynlova, B. L. Langille, and S. J. Lye. 2004. Mechanical stretch and progesterone differentially regulate activator protein-1 transcription factors in primary rat myometrial smooth muscle cells. Am. J. Physiol. 287: E439-E445.
31. Maeda, I., N. Mizoiri, M. P. Briones, and K. Okamoto. 2007. Induction of macrophage migration through lactose-insensitive receptor by elastin-derived nonapeptides and their analog. J. Pept. Sci. 13: 263-268. (Pubitemid 46638197)
32. Conover, C. A., S. C. Harrington, L. K. Bale, and C. Oxvig. 2007. Surface association of pregnancy-associated plasma protein-A accounts for its colocalization with activated macrophages. Am. J. Physiol. 292: H994-H1000.
33. Gu, L., B. Rutledge, J. Fiorillo, C. Ernst, I. Grewal, R. Flavell, C. Gladue, and B. Rollins. 1997. In vivo properties of monocyte chemoattractant protein-1. J. Leukocyte Biol. 62: 577-580. (Pubitemid 27519767)
34. Pollard, J. W., E. Y. Lin, and L. Zhu. 1998. Complexity in uterine macrophage responses to cytokines in mice. Biol. Reprod. 58: 1469-1475.
35. Caballero-Campo, P., F. Dominguez, J. Coloma, M. Meseguer, J. Remohi, A. Pellicer, and C. Simon. 2002. Hormonal and embryonic regulation of chemokines IL-8, MCP-1 and RANTES in the human endometrium during the window of implantation. Mol. Hum. Reprod. 8: 375-384. (Pubitemid 34303246)
36. Denison, F. C., R. W. Kelly, A. A. Calder, and S. C. Riley. 1998. Cytokine secretion by human fetal membranes, decidua and placenta at term. Hum. Reprod. 13: 3560-3565. (Pubitemid 29002658)
37. Asselin, E., G. A. Johnson, T. E. Spencer, and F. W. Bazer. 2001. Monocyte chemotactic protein-1 and -2 messenger ribonucleic acids in the ovine uterus: regulation by pregnancy, progesterone, and interferon-τ. Biol. Reprod. 64: 992-1000. (Pubitemid 32174073)
38. Townson, D. H., J. S. Warren, C. M. Flory, D. M. Naftalin, and P. L. Keyes. 1996. Expression of monocyte chemoattractant protein-1 in the corpus luteum of the rat. Biol. Reprod. 54: 513-520. (Pubitemid 26031423)
39. Sozen, I., D. L. Olive, and A. Arici. 1998. Expression and hormonal regulation of monocyte chemotactic protein-1 in myometrium and leiomyomata. Fertil. Steril. 69: 1095-1102. (Pubitemid 28274900)
40. Pype, J. L., L. J. Dupont, P. Menten, E. Van Coillie, G. Opdenakker, J. Van Damme, K. F. Chung, M. G. Demedts, and G. M. Verleden. 1999. Expression of monocyte chemotactic protein (MCP)-1. MCP-2, and MCP-3 by human airway smooth-muscle cells: modulation by corticosteroids and T-helper 2 cytokines. Am. J. Respir. Cell Mol. Biol. 21: 528-536.
41. Ou, C. W., A. Orsino, and S. J. Lye. 1997. Expression of connexin-43 and connexin- 26 in the rat myometrium during pregnancy and labor is differentially regulated by mechanical and hormonal signals. Endocrinology 138: 5398-5407.
42. Diamond, J. R., D. Kees-Folts, G. Ding, J. E. Frye, and N. C. Restrepo. 1994. Macrophages, monocyte chemoattractant peptide-1, and TGF-β1 in experimental hydronephrosis. Am. J. Physiol. 266: F926-F933. (Pubitemid 2111735)
43. Okada, M., A. Matsumori, K. Ono, Y. Furukawa, T. Shioi, A. Iwasaki, K. Matsushima, and S. Sasayama. 1998. Cyclic stretch upregulates production of interleukin-8 and monocyte chemotactic and activating factor/monocyte chemoattractant protein-1 in human endothelial cells. Arterioscler. Thromb. Vasc. Biol. 18: 894-901. (Pubitemid 28272582)
44. Beck, C. G., C. Studer, J. F. Zuber, B. J. Demange, U. Manning, and R. Urfer. 2001. The viral CC chemokine-binding protein vCCI inhibits monocyte chemoattractant protein-1 activity by masking its CCR2B-binding site. J. Biol. Chem. 276: 43270-43276. (Pubitemid 37371014)
45. Merlino, A. A., T. N. Welsh, H. Tan, L. J. Yi, V. Cannon, B. M. Mercer, S. Mesiano. 2007. Nuclear progesterone receptors in the human pregnancy myometrium: evidence that parturition involves functional progesterone withdrawal mediated by increased expression of progesterone receptor-A. J. Clin. Endocrinol. Metab. 92: 1927-1933.
46. Condon, J. C., D. B. Hardy, K. Kovaric, and C. R. Mendelson. 2006. Up-regulation of the progesterone receptor (PR)-C isoform in laboring myometrium by activation of nuclear factor-κB may contribute to the onset of labor through inhibition of PR function. Mol. Endocrinol. 20: 764-775.
47. Dong, X., O. Shylnova, J. R. Challis, and S. J. Lye. 2005. Identification and characterization of the protein-associated splicing factor as a negative co-regulator of the progesterone receptor. J. Biol. Chem. 280: 13329-13340. (Pubitemid 40517219)
48. Graham, J. D., and C. L. Clarke. 1997. Physiological action of progesterone in target tissues. Endocr. Rev. 18: 502-519.
49. Loudon, J. A., C. L. Elliott, F. Hills, and P. R. Bennett. 2003. Progesterone represses interleukin-8 and cyclo-oxygenase-2 in human lower segment fibroblast cells and amnion epithelial cells. Biol. Reprod. 69: 331-337.
50. Kelly, R. W., P. Illingworth, G. Baldie, R. Leask, S. Brouwer, and A. A. Calder. 1994. Progesterone control of interleukin-8 production in endometrium and chorio-decidual cells underlines the role of the neutrophil in menstruation and parturition. Hum. Reprod. 9: 253-258.
51. Jones, R. L., N. J. Hannan, T. J. Kaitu'u, J. Zhang, and L. A. Salamonsen. 2004. Identification of chemokines important for leukocyte recruitment to the human endometrium at the times of embryo implantation and menstruation. J. Clin. Endocrinol. Metab. 89: 6155-6167.
52. Alam, R., M. A. Lett-Brown, P. A. Forsythe, D. J. Anderson-Walters, C. Kenamore, C. Kormos, and J. A. Grant. 1992. Monocyte chemotactic and activating factor is a potent histamine-releasing factor for basophils. J. Clin. Invest. 89: 723-728.
53. Ledingham, M. A., A. J. Thomson, F. Jordan, A. Young, M. Crawford, and J. E. Norman. 2001. Cell adhesion molecule expression in the cervix and myometrium during pregnancy and parturition. Obstet. Gynecol. 97: 235-242. (Pubitemid 32126339)
54. Osmers, R. G., J. Blaser, W. Kuhn, and H. Tschesche. 1995. Interleukin-8 synthesis and the onset of labor. Obstet. Gynecol. 86: 223-229.