Pathophysiological Roles of Chemokines in Human Reproduction: An Overview

American Journal of Reproductive Immunology

Volumn 65, Issue 5, 2011, Pages 449-459

  Kitaya, Kotaro ^a,b   Yamada, Hisao ^b  

^a KYOTO PREFECTURAL UNIVERSITY OF MEDICINE   (Japan)

^b KANSAI MEDICAL UNIVERSITY   (Japan)

Author keywords

Chemokines; Fallopian tube; Ovary; Testis; Uterus

Indexed keywords

CHEMOKINE; CHEMOKINE RECEPTOR CX3CR1; CXCL1 CHEMOKINE; CXCL13 CHEMOKINE; CXCL2 CHEMOKINE; CXCL3 CHEMOKINE; CXCL9 CHEMOKINE; EOTAXIN; EPITHELIAL DERIVED NEUTROPHIL ACTIVATING FACTOR 78; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GRANULOCYTE CHEMOTACTIC PROTEIN 2; GRANULOCYTE COLONY STIMULATING FACTOR; INTERLEUKIN 15; INTERLEUKIN 18; INTERLEUKIN 8; MACROPHAGE DERIVED CHEMOKINE; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 3BETA; MONOCYTE CHEMOTACTIC PROTEIN 1; MONOCYTE CHEMOTACTIC PROTEIN 2; MONOCYTE CHEMOTACTIC PROTEIN 3; RANTES; SECONDARY LYMPHOID TISSUE CHEMOKINE; STROMAL CELL DERIVED FACTOR 1; THYMUS AND ACTIVATION REGULATED CHEMOKINE;

ASTHENOSPERMIA; ENDOMETRIOSIS; ENDOMETRITIS; FEMALE GENITAL SYSTEM; GENITAL SYSTEM DISEASE; HUMAN; LUTEAL INSUFFICIENCY; LUTEINIZATION; LUTEOLYSIS; MALE GENITAL SYSTEM; MALE INFERTILITY; OVARY FOLLICLE ATRESIA; OVARY FOLLICLE DEVELOPMENT; OVARY HYPERSTIMULATION; OVARY POLYCYSTIC DISEASE; PATHOPHYSIOLOGY; PREMATURE OVARIAN FAILURE; PRIORITY JOURNAL; REVIEW; SALPINGITIS; SPERMATOGENESIS; SPERMATOZOON MOTILITY; SPONTANEOUS ABORTION; UTERUS MYOMA;

ABORTION, SPONTANEOUS; CHEMOKINES; FALLOPIAN TUBES; FEMALE; GENITAL DISEASES, FEMALE; HUMANS; INFERTILITY, MALE; INFLAMMATION; LEUKOCYTES; MALE; OVARY; REPRODUCTION; TESTIS; UTERUS;

EID: 79953688539     PISSN: 10467408     EISSN: 16000897     Source Type: Journal    
DOI: 10.1111/j.1600-0897.2010.00928.x     Document Type: Review

References (99)

1. Bonecchi R, Galliera E, Borroni EM, Corsi MM, Locati M, Mantovani A: Chemokines and chemokine receptors: an overview. Front Biosci 2009; 14:540-551.
2. Wilkinson PC, Komai-Koma M, Newman I: Locomotion and chemotaxis of lymphocytes. Autoimmunity 1997; 26:55-72.
3. Kitaya K, Yamaguchi T, Honjo H: Central role of interleukin-15 in postovulatory recruitment of peripheral blood CD16(-) natural killer cells into human endometrium. J Clin Endocrinol Metab 2005; 90:2932-2940.
4. Takenaka K, Mizuno SI, Harada M, Nagafuji K, Miyamoto T, Iwasaki H, Fujisaki T, Kubota A, Ohno Y, Arima F, Shigematsu H, Gondo H, Okamura T, Okamura S, Inaba S, Niho Y: Generation of human natural killer cells from peripheral blood CD34+ cells mobilized by granulocyte colony-stimulating factor. Br J Hematol 1996; 92:788-794.
5. Coulam CB, Adamson SC, Annegers JF: Incidence of premature ovarian failure. Obstet Gynecol 1986; 67:604-606.
6. Kezele PR, Ague JM, Nilsson E, Skinner MK: Alterations in the ovarian transcriptome during primordial follicle assembly and development. Biol Reprod 2005; 72:241-255.
7. Yoon SJ, Kim KH, Chung HM, Choi DH, Lee WS, Cha KY, Lee KA: Gene expression profiling of early follicular development in primordial, primary, and secondary follicles. Fertil Steril 2006; 85:193-203.
8. Crisponi L, Deiana M, Loi A, Chiappe F, Uda M, Amati P, Bisceglia L, Zelante L, Nagaraja R, Porcu S, Ristaldi MS, Marzella R, Rocchi M, Nicolino M, Lienhardt-Roussie A, Nivelon A, Verloes A, Schlessinger D, Gasparini P, Bonneau D, Cao A, Pilia G: The putative forkhead transcription factor FOXL2 is mutated in blepharophimosis/ptosis/epicanthus inversus syndrome. Nat Genet 2001; 27:159-166.
9. Batista F, Vaiman D, Dausset J, Fellous M, Veitia RA: Potential targets of FOXL2, a transcription factor involved in craniofacial and follicular development, identified by transcriptomics. Proc Natl Acad Sci USA 2007; 104:3330-3335.
10. Knauff EA, Franke L, van Es MA, van den Berg LH, van der Schouw YT, Laven JS, Lambalk CB, Hoek A, Goverde AJ, Christin-Maitre S, Hsueh AJ, Wijmenga C, Fauser BC, Dutch POF Consortium: Genome-wide association study in premature ovarian failure patients suggests ADAMTS19 as a possible candidate gene. Hum Reprod 2009; 24:2372-2378.
11. Doitsidou M, Reichman-Fried M, Stebler J, Köprunner M, Dörries J, Meyer D, Esguerra CV, Leung T, Raz E: Guidance of primordial germ cell migration by the chemokine SDF-1. Cell 2002; 111:647-659.
12. Ara T, Nakamura Y, Egawa T, Sugiyama T, Abe K, Kishimoto T, Matsui Y, Nagasawa T: Impaired colonization of the gonads by primordial germ cells in mice lacking a chemokine, stromal cell-derived factor-1 (CXCL12). Proc Natl Acad Sci U S A 2003; 100:5319-5323.
13. Holt JE, Jackson A, Roman SD, Aitken RJ, Koopman P, McLaughlin EA: CXCR4/SDF1 interaction inhibits the primordial to primary follicle transition in the neonatal mouse ovary. Dev Biol 2006; 293:449-460.
14. Kryczek I, Frydman N, Gaudin F, Krzysiek R, Fanchin R, Emilie D, Chouaib S, Zou W, Machelon V: The chemokine SDF-1/CXCL12 contributes to T lymphocyte recruitment in human pre-ovulatory follicles and coordinates with lymphocytes to increase granulosa cell survival and embryo quality. Am J Reprod Immunol 2005; 54:270-283.
15. Malizia BA, Wook YS, Penzias AS, Usheva A: The human ovarian follicular fluid level of interleukin-8 is associated with follicular size and patient age. Fertil Steril 2010; 93:537-543.
16. Goto J, Kanayama N, Asahina T, Okada Y, Kobayashi T, Terao T: Induction of follicular growth by exogenous interleukin-8. Hum Reprod 1997; 12:2729-2734.
17. Arici A, Oral E, Bukulmez O, Buradagunta S, Engin O, Olive DL: Interleukin-8 expression and modulation in human preovulatory follicles and ovarian cells. Endocrinology 1996; 137:3762-3769.
18. Gazvani MR, Bates M, Vince G, Christmas S, Lewis-Jones DI, Kingsland C: Follicular fluid concentrations of interleukin-12 and interleukin-8 in IVF cycles. Fertil Steril 2000; 74:953-958.
19. Hammadeh ME, Fischer-Hammadeh C, Georg T, Rosenbaum P, Schmidt W: Comparison between cytokine concentration in follicular fluid of poor and high responder patients and their influence of ICSI-outcome. Am J Reprod Immunol 2003; 50:131-136.
20. Goto J, Suganuma N, Takata K, Kitamura K, Asahina T, Kobayashi H, Muranaka Y, Furuhashi M, Kanayama N: Morphological analyses of interleukin-8 effects on rat ovarian follicles at ovulation and luteinization in vivo. Cytokine 2002; 20:168-173.
21. Chang RJ, Gougeon A, Erickson GF: Evidence for a neutrophil-interleukin-8 system in human folliculogenesis. Am J Obstet Gynecol 1998; 178:650-657.
22. brightCD16(-) natural killer cells accumulate in the ovarian follicular fluid of patients undergoing in vitro fertilization. Fertil Steril 2010; 94:1918-1921.
23. Krizan J, Cuchalova L, Sima P, Kralickova M, Madar J, Vetvicka V: Altered distribution of NK and NKT cells in follicular fluid is associated with IVF outcome. J Reprod Immunol 2009; 82:84-88.
24. Delvigne A, Rozenberg S: Review of clinical course and treatment of ovarian hyperstimulation syndrome (OHSS). Hum Reprod Update 2003; 9:77-96.
25. Chen SU, Chou CH, Lin CW, Lee H, Wu JC, Lu HF, Chen CD, Yang YS: Signal mechanisms of vascular endothelial growth factor and interleukin-8 in ovarian hyperstimulation syndrome: dopamine targets their common pathways. Hum Reprod 2010; 25:757-767.
26. Ujioka T, Matsukawa A, Tanaka N, Matsuura K, Yoshinaga M, Okamura H: Interleukin-8 as an essential factor in the human chorionic gonadotropin-induced rabbit ovulatory process: interleukin-8 induces neutrophil accumulation and activation in ovulation. Biol Reprod 1998; 58:526-530.
27. Chen CD, Chen HF, Lu HF, Chen SU, Ho HN, Yang YS: Value of serum and follicular fluid cytokine profile in the prediction of moderate to severe ovarian hyperstimulation syndrome. Hum Reprod 2000; 15:1037-1042.
28. Cohen PE, Zhu L, Pollard JW: Absence of colony stimulating factor-1 in osteopetrotic (csfmop/csfmop) mice disrupts estrous cycles and ovulation. Biol Reprod 1997; 56:110-118.
29. Arici A, Oral E, Bukulmez O, Buradagunta S, Bahtiyar O, Jones EE: Monocyte chemotactic protein-1 expression in human preovulatory follicles and ovarian cells. J Reprod Immunol 1997; 32:201-219.
30. Dahm-Kähler P, Ghahremani M, Lind AK, Sundfeldt K, Brännström M: Monocyte chemotactic protein-1 (MCP-1), its receptor, and macrophages in the perifollicular stroma during the human ovulatory process. Fertil Steril 2009; 91:231-239.
31. Stamatovic SM, Keep RF, Wang MM, Jankovic I, Andjelkovic AV: Caveolae-mediated internalization of occludin and claudin-5 during CCL2-induced tight junction remodeling in brain endothelial cells. J Biol Chem 2009; 284:19053-19066.
32. Rodewald M, Herr D, Duncan WC, Fraser HM, Hack G, Konrad R, Gagsteiger F, Kreienberg R, Wulff C: Molecular mechanisms of ovarian hyperstimulation syndrome: paracrine reduction of endothelial claudin 5 by hCG in vitro is associated with increased endothelial permeability. Hum Reprod 2009; 24:1191-1199.
33. Humaidan P, Quartarolo J, Papanikolaou EG: Preventing ovarian hyperstimulation syndrome: guidance for the clinician. Fertil Steril 2010; 94:389-400.
34. Wu R, Fujii S, Ryan NK, Van der Hoek KH, Jasper MJ, Sini I, Robertson SA, Robker RL, Norman RJ: Ovarian leukocyte distribution and cytokine/chemokine mRNA expression in follicular fluid cells in women with polycystic ovary syndrome. Hum Reprod 2007; 22:527-535.
35. Oksjoki S, Söderström M, Inki P, Vuorio E, Anttila L: Molecular profiling of polycystic ovaries for markers of cell invasion and matrix turnover. Fertil Steril 2005; 83:937-944.
36. Jansen E, Laven JS, Dommerholt HB, Polman J, van Rijt C, van den Hurk C, Westland J, Mosselman S, Fauser BC: Abnormal gene expression profiles in human ovaries from polycystic ovary syndrome patients. Mol Endocrinol 2004; 18:3050-3063.
37. Zhou C, Wu J, Borillo J, Torres L, McMahon J, Lou YH: Potential roles of a special CD8αα + cell population and CC chemokine thymus-expressed chemokine in ovulation related inflammation. J Immunol 2009; 182:596-603.
38. Murdoch WJ, Steadman LE: Investigations concerning the relationship of ovarian eosinophilia to ovulation and luteal function in the sheep. Am J Reprod Immunol 1991; 25:81-87.
39. Aust G, Simchen C, Heider U, Hmeidan FA, Blumenauer V, Spanel-Borowski K: Eosinophils in the human corpus luteum: the role of RANTES and eotaxin in eosinophil attraction into periovulatory structures. Mol Hum Reprod 2000; 6:1085-1091.
40. Zhao P, De A, Hu Z, Li J, Mulders SM, Sollewijn Gelpke MD, Duan EK, Hsueh AJ: Gonadotropin stimulation of ovarian fractalkine expression and fractalkine augmentation of progesterone biosynthesis by luteinizing granulosa cells. Endocrinology 2008; 149:2782-2789.
41. Qublan H, Amarin Z, Nawasreh M, Diab F, Malkawi S, Al-Ahmad N, Balawneh M: Luteinized unruptured follicle syndrome: incidence and recurrence rate in infertile women with unexplained infertility undergoing intrauterine insemination. Hum Reprod 2006; 21:2110-2113.
42. White R, Leonardsson G, Rosewell I, Ann Jacobs M, Milligan S, Parker M: The nuclear receptor co-repressor nrip1 (RIP140) is essential for female fertility. Nat Med 2000; 6:1368-1374.
43. Tsai SJ, Juengel JL, Wiltbank MC: Hormonal regulation of monocyte chemoattractant protein-1 messenger ribonucleic acid expression in corpora lutea. Endocrinology 1997; 138:4517-4520.
44. Haworth JD, Rollyson MK, Silva P, McIntush EW, Niswender GD: Messenger ribonucleic acid encoding monocyte chemoattractant protein-1 is expressed by the ovine corpus luteum in response to prostaglandin F2α. Biol Reprod 1998; 58:169-174.
45. Bowen JM, Keyes PL, Warren JS, Townson DH: Prolactin-induced regression of the rat corpus luteum: expression of monocyte chemoattractant protein-1 and invasion of macrophages. Biol Reprod 1996; 54:1120-1127.
46. Penny LA, Armstrong DG, Baxter G, Hogg C, Kindahl H, Bramley T, Watson ED, Webb R: Expression of monocyte chemoattractant protein-1 in the bovine corpus luteum around the time of natural luteolysis. Biol Reprod 1998; 59:1464-1469.
47. Muciaccia B, Padula F, Vicini E, Gandini L, Lenzi A, Stefanini M: β-chemokine receptors 5 and 3 are expressed on the head region of human spermatozoon. FASEB J 2005; 19:2048-2050.
48. Barbonetti A, Vassallo MR, Pelliccione F, D'Angeli A, Santucci R, Muciaccia B, Stefanini M, Francavilla F, Francavilla S: β-chemokine receptor CCR5 in human spermatozoa and its relationship with seminal parameters. Hum Reprod 2009; 24:2979-2987.
49. Januchowski R, Breborowicz AK, Ofori H, Jedrzejczak P, Pawelczyk L, Jagodzinski PP: Detection of a short CCR5 messenger RNA isoform in human spermatozoa. J Androl 2004; 25:757-760.
50. Isobe T, Minoura H, Tanaka K, Shibahara T, Hayashi N, Toyoda N: The effect of RANTES on human sperm chemotaxis. Hum Reprod 2002; 17:1441-1446.
51. Naz RK, Leslie MH: Immunobiologic implication of RANTES in seminal plasma of fertile, infertile and immunoinfertile men. Am J Reprod Immunol 2000; 44:197-204.
52. Hakovirta H, Vierula M, Wolpe SD, Parvinen M: MIP-1α is a regulator of mitotic and meiotic DNA synthesis during spermatogenesis. Mol Cell Endocrinol 1994; 99:119-124.
53. Gopichandran N, Ekbote UV, Walker JJ, Brooke D, Orsi NM: Multiplex determination of murine seminal fluid cytokine profiles. Reproduction 2006; 131:613-621.
54. Koumantakis E, Matalliotakis I, Kyriakou D, Fragouli Y, Relakis K: Increased levels of interleukin-8 in human seminal plasma. Andrologia 1998; 30:339-343.
55. Le Goffic R, Mouchel T, Ruffault A, Patard JJ, Jégou B, Samson M: Mumps virus decreases testosterone production and gamma interferon-induced protein 10 secretion by human leydig cells. J Virol 2003; 77:3297-3300.
56. Maegawa M, Kamada M, Irahara M, Yamamoto S, Yoshikawa S, Kasai Y, Ohmoto Y, Gima H, Thaler CJ, Aono T: A repertoire of cytokines in human seminal plasma. J Reprod Immunol 2002; 54:33-42.
57. Zhang Q, Shimoya K, Ohta Y, Chin R, Tenma K, Isaka S, Nakamura H, Koyama M, Azuma C, Murata Y: Detection of fractalkine in human seminal plasma and its role in infertile patients. Hum Reprod 2002; 17:1560-1564.
58. Guazzone VA, Jacobo P, Theas MS, Lustig L: Cytokines and chemokines in testicular inflammation: a brief review. Microsc Res Tech 2009; 72:620-628.
59. Lue Y, Wang C, Cui Y, Wang X, Sha J, Zhou Z, Xu J, Wang C, Hikim AP, Swerdloff RS: Levonorgestrel enhances spermatogenesis suppression by testosterone with greater alteration in testicular gene expression in men. Biol Reprod 2009; 80:484-492.
60. Lédée N, Lombroso R, Lombardelli L, Selva J, Dubanchet S, Chaouat G, Frankenne F, Foidart JM, Maggi E, Romagnani S, Ville Y, Piccinni MP: Cytokines and chemokines in follicular fluids and potential of the corresponding embryo: the role of granulocyte colony-stimulating factor. Hum Reprod 2008; 23:2001-2009.
61. Tamba S, Yodoi R, Segi-Nishida E, Ichikawa A, Narumiya S, Sugimoto Y: Timely interaction between prostaglandin and chemokine signaling is a prerequisite for successful fertilization. Proc Natl Acad Sci U S A 2008; 105:14539-14544.
62. Debattista J, Timms P, Allan J, Allan J: Immunopathogenesis of Chlamydia trachomatis infections in women. Fertil Steril 2003; 79:1273-1287.
63. King M, Poya H, Rao J, Natarajan S, Butch AW, Aziz N, Kok S, Chang MH, Lyons JM, Ault K, Kelly KA: CXCL13 expression in Chlamydia trachomatis infection of the female reproductive tract. Drugs Today 2009; 45(Suppl B):125-134.
64. Hvid M, Baczynska A, Deleuran B, Fedder J, Knudsen HJ, Christiansen G, Birkelund S: Interleukin-1 is the initiator of Fallopian tube destruction during Chlamydia trachomatis infection. Cell Microbiol 2007; 9:2795-2803.
65. King M, Kok S, Chan AM, Kelly KA: Lymphoid neogenesis occurs within fallopian tubes after infection with Chlamydia. Am J Reprod Immunol 2006; 55:394.
66. Dominguez F, Galan A, Luna Martin JJ, Remohi J, Pellicer A, Simón C: Hormonal and embryonic regulation of chemokine receptors CXCR1, CXCR4, CCR5 and CCR2B in the human endometrium and the human blastocyst. Mol Hum Reprod 2003; 9:189-198.
67. Kitaya K, Yasuda J, Yagi I, Tada Y, Fushiki S, Honjo H: IL-15 expression at human endometrium and decidua. Biol Reprod 2000; 63:683-687.
68. Kitaya K, Nakayama T, Daikoku N, Fushiki S, Honjo H: Spatial and temporal expression of ligands for CXCR3 and CXCR4 in human endometrium. J Clin Endocrinol Metab 2004; 89:2470-2476.
69. Daikoku N, Kitaya K, Nakayama T, Fushiki S, Honjo H: Expression of macrophage inflammatory protein-3β in human endometrium throughout the menstrual cycle. Fertil Steril 2004; 81(Suppl 1):876-881.
70. Jones RL, Kelly RW, Critchley HO: Chemokine and cyclooxygenase-2 expression in human endometrium coincides with leukocyte accumulation. Hum Reprod 1997; 12:1300-1306.
71. 3CL1, CCL14, and CCL4, promote human trophoblast migration at the feto-maternal interface. Biol Reprod 2006; 74:896-904.
72. Hanna J, Goldman-Wohl D, Hamani Y, Avraham I, Greenfield C, Natanson-Yaron S, Prus D, Cohen-Daniel L, Arnon TI, Manaster I, Gazit R, Yutkin V, Benharroch D, Porgador A, Keshet E, Yagel S, Mandelboim O: Decidual NK cells regulate key developmental processes at the human fetal-maternal interface. Nat Med 2006; 12:1065-1074.
73. Yasuo T, Kitaya K: Effect of ovarian steroids on gene expression profile in human uterine microvascular endothelial cells. Fertil Steril 2009; 92:709-721.
74. bright natural killer cells in women with infertility. Am J Reprod Immunol 2009; 62:118-124.
75. Kitaya K, Nakayama T, Okubo T, Kuroboshi H, Fushiki S, Honjo H: Expression of macrophage inflammatory protein-1β in human endometrium: its role in endometrial recruitment of natural killer cells. J Clin Endocrinol Metab 2003; 88:809-814.
76. Nakayama T, Kitaya K, Okubo T, Kuroboshi H, Daikoku N, Fushiki S, Honjo H: Fluctuation of 6Ckine expression in human endometrium during the menstrual cycle. Fertil Steril 2003; 80:1461-1465.
77. Sentman CL, Meadows SK, Wira CR, Eriksson M: Recruitment of uterine NK cells: induction of CXC chemokine ligands 10 and 11 in human endometrium by estradiol and progesterone. J Immunol 2004; 173:6760-6766.
78. Kitaya K: Accumulation of uterine CD16(-) natural killer (NK) cells: friends, foes, or Jekyll-and-Hyde relationship for the conceptus? Immunol Invest 2008; 37:467-481.
79. Kuang H, Chen Q, Zhang Y, Zhang L, Peng H, Ning L, Cao Y, Duan E: The cytokine gene CXCL14 restricts human trophoblast cell invasion by suppressing gelatinase activity. Endocrinology 2009; 150:5596-5605.
80. Johnston-MacAnanny EB, Hartnett J, Engmann LL, Nulsen JC, Sanders MM, Benadiva CA: Chronic endometritis is a frequent finding in women with recurrent implantation failure after in vitro fertilization. Fertil Steril 2010; 93:437-441.
81. Kitaya K, Yasuo T: Aberrant expression of selectin E, CXCL1, and CXCL13 in chronic endometritis. Mod Pathol 2010; 23:1136-1146.
82. Kitaya K, Yasuo T: Dermatan sulfate proteoglycan biglycan as a potential selectin L/CD44 ligand involved in selective recruitment of peripheral blood CD16(-) natural killer cells into human endometrium. J Leukoc Biol 2009; 85:391-400.
83. Cicinelli E, De Ziegler D, Nicoletti R, Colafiglio G, Saliani N, Resta L, Rizzi D, De Vito D: Chronic endometritis: correlation among hysteroscopic, histologic, and bacteriologic findings in a prospective trial with 2190 consecutive office hysteroscopies. Fertil Steril 2008; 89:677-684.
84. Pritts EA, Parker WH, Olive DL: Fibroids and infertility: an updated systematic review of the evidence. Fertil Steril 2009; 91:1215-1523.
85. Sozen I, Senturk LM, Arici A: Effect of gonadotropin-releasing hormone agonists on monocyte chemotactic protein-1 production and macrophage infiltration in leiomyomatous uterus. Fertil Steril 2001; 76:792-796.
86. Arslan AA, Gold LI, Mittal K, Suen TC, Belitskaya-Levy I, Tang MS, Toniolo P: Gene expression studies provide clues to the pathogenesis of uterine leiomyoma: new evidence and a systematic review. Hum Reprod 2005; 20:852-863.
87. Miura S, Khan KN, Kitajima M, Hiraki K, Moriyama S, Masuzaki H, Samejima T, Fujishita A, Ishimaru T: Differential infiltration of macrophages and prostaglandin production by different uterine leiomyomas. Hum Reprod 2006; 21:2545-2554.
88. Kitaya K, Yasuo T: Leukocyte density and composition in human cycling endometrium with uterine fibroids. Hum Immunol 2010; 71:158-163.
89. Syssoev KA, Kulagina NV, Chukhlovin AB, Morozova EB, Totolian AA: Expression of mRNA for chemokines and chemokine receptors in tissues of the myometrium and uterine leiomyoma. Bull Exp Biol Med 2008; 145:84-89.
90. Zhu XQ, Lv JQ, Lin Y, Xiang M, Gao BH, Shi YF: Expression of chemokines CCL5 and CCL11 by smooth muscle tumor cells of the uterus and its possible role in the recruitment of mast cells. Gynecol Oncol 2007; 105:650-656.
91. Khorram O, Taylor RN, Ryan IP, Schall TJ, Landers DV: Peritoneal fluid concentrations of the cytokine RANTES correlate with the severity of endometriosis. Am J Obstet Gynecol 1993; 169:1545-1549.
92. Iwabe T, Harada T, Tsudo T, Tanikawa M, Onohara Y, Terakawa N: Pathogenetic significance of increased levels of interleukin-8 in the peritoneal fluid of patients with endometriosis. Fertil Steril 1998; 69:924-930.
93. Bondza PK, Maheux R, Akoum A: Insights into endometriosis-associated endometrial dysfunctions: a review. Front Biosci 2009; 1:415-428.
94. Wang Y, Yu J, Luo X, Wang X, Li M, Wang L, Li D: Abnormal regulation of chemokine TECK and its receptor CCR9 in the endometriotic milieu is involved in pathogenesis of endometriosis by way of enhancing invasiveness of endometrial stromal cells. Cell Mol Immunol 2010; 7:51-60.
95. Shi YL, Luo XZ, Zhu XY, Li DJ: Combination of 17β-estradiol with the environmental pollutant TCDD is involved in pathogenesis of endometriosis via up-regulating the chemokine I-309-CCR8. Fertil Steril 2007; 88:317-325.
96. Madhappan B, Kempuraj D, Christodoulou S, Tsapikidis S, Boucher W, Karagiannis V, Athanassiou A, Theoharides TC: High levels of intrauterine corticotropin-releasing hormone, urocortin, tryptase, and interleukin-8 in spontaneous abortions. Endocrinology 2003; 144:2285-2290.
97. Chegini N, Ma C, Roberts M, Williams RS, Ripps BA: Differential expression of interleukins (IL) IL-13 and IL-15 throughout the menstrual cycle in endometrium of normal fertile women and women with recurrent spontaneous abortion. J Reprod Immunol 2002; 56:93-110.
98. Toth B, Haufe T, Scholz C, Kuhn C, Friese K, Karamouti M, Makrigiannakis A, Jeschke U: Placental interleukin-15 expression in recurrent miscarriage. Am J Reprod Immunol (in press).
99. Chaiworapongsa T, Romero R, Tolosa JE, Yoshimatsu J, Espinoza J, Kim YM, Kim JC, Bujold E, Kalache K, Edwin S: Elevated monocyte chemotactic protein-1 in amniotic fluid is a risk factor for pregnancy loss. J Matern Fetal Neonatal Med 2002; 12:159-164.