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Open Access 01-12-2003 | Review

Chemokines in the corpus luteum: Implications of leukocyte chemotaxis

Authors: David H Townson, Amy R Liptak

Published in: Reproductive Biology and Endocrinology | Issue 1/2003

Abstract

Chemokines are small molecular weight peptides responsible for adhesion, activation, and recruitment of leukocytes into tissues. Leukocytes are thought to influence follicular atresia, ovulation, and luteal function. Many studies in recent years have focused attention on the characterization of leukocyte populations within the ovary, the importance of leukocyte-ovarian cell interactions, and more recently, the mechanisms of ovarian leukocyte recruitment. Information about the role of chemokines and leukocyte trafficking (chemotaxis) during ovarian function is important to understanding paracrine-autocrine relationships shared between reproductive and immune systems. Recent advances regarding chemokine expression and leukocyte accumulation within the ovulatory follicle and the corpus luteum are the subject of this mini-review.

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Bukovsky A, Presl J, Krabec Z, Bednarik T: Ovarian function in adult rats treated with antithymocyte serum. Experientia. 1977, 33: 280-281.CrossRefPubMed

Murdoch WJ: Treatment of sheep with prostaglandin F2 alpha enhances production of a luteal chemoattractant for eosinophils. Am J Reprod Immunol Microbiol. 1987, 15: 52-56.PubMed

Murdoch WJ, McCormick RJ: Production of low molecular weight chemoattractants for leukocytes by periovulatory ovine follicles. Biol Reprod. 1989, 41: 86-90.CrossRefPubMed

Adashi EY: The potential relevance of cytokines to ovarian physiology: the emerging role of resident ovarian cells of the white blood cell series. Endocr Rev. 1990, 11: 454-464.CrossRefPubMed

Mori T: Immuno-endocrinology of cyclic ovarian function. Am J Reprod Immunol. 1990, 24: 80-89.CrossRefPubMed

Hellberg P, Thomsen P, Janson PO, Brannstrom M: Leukocyte supplementation increases the luteinizing hormone-induced ovulation rate in the in vitro-perfused rat ovary. Biol Reprod. 1991, 44: 791-797.CrossRefPubMed

Lobel BL, Levy E: Enzymic correlates of development, secretory function and regression of follicles and corpora lutea in the bovine ovary. II. Formation, development and involution of corpora lutea. Acta Endocrinologica. 1968, 59: 35-51.

Standaert FE, Zamora CS, Chew BP: Quantitative and qualitative changes in blood leukocytes in the porcine ovary. Am J Reprod Immunol. 1991, 25: 163-168.CrossRefPubMed

Brannstrom M, Giesecke L., Moore IC, Van Den Heuvel CJ, Robertson SA: Leukocyte subpopulations in the rat corpus luteum during pregnancy and pseudopregnancy. Biol Reprod. 1994, 50: 1161-1167.CrossRefPubMed

10.

Brannstrom M, Pascoe V, Norman RJ, McClure N: Localization of leukocyte subsets in the follicle wall and in the corpus luteum throughout the human menstrual cycle. Fertil Steril. 1994, 61: 488-495.PubMed

11.

Suzuki T, Sasano H, Takaya R, Fukaya T, Yajima A, Date F, Nagura H: Leukocytes in normal-cycling human ovaries: immunohistochemical distribution and characterization. Hum Reprod. 1998, 13: 2186-2191. 10.1093/humrep/13.8.2186.CrossRefPubMed

12.

Lawler DF, Hopkins J, Watson ED: Immune cell populations in the equine corpus luteum throughout the oestrous cycle and early pregnancy: an immunohistochemical and flow cytometric study. J Reprod Fertil. 1999, 117: 281-290.CrossRefPubMed

13.

Reibiger I, Spanel-Borowski K: Difference in localization of eosinophils and mast cells in the bovine ovary. J Reprod Fertil. 2000, 118: 243-249. 10.1530/reprod/118.2.243.CrossRefPubMed

14.

Ramadan AA, Selim SA, Hassan HM, Wahba MA: Immune regulation of ovarian function in buffaloes (Bubalus bubalus). Theriogenology. 2001, 55: 661-669. 10.1016/S0093-691X(01)00434-4.CrossRefPubMed

15.

Townson DH, O'Connor CL, Pru JK: Expression of monocyte chemoattractant protein-1 and distribution of immune cell populations in the bovine corpus luteum throughout the estrous cycle. Biol Reprod. 2002, 66: 361-366.CrossRefPubMed

16.

Chun SY, Hsueh AJ: Paracrine mechanisms of ovarian follicle apoptosis. J Reprod Immunol. 1998, 39: 63-75. 10.1016/S0165-0378(98)00013-8.CrossRefPubMed

17.

Meidan R, Milvae RA, Weiss S, Levy N, Friedman A: Intraovarian regulation of luteolysis. J Reprod Fertil Suppl. 1999, 54: 217-228.PubMed

18.

Asselin E, Xiao CW, Wang YF, Tsang BK: Mammalian follicular development and atresia: role of apoptosis. Biol Signals Recept. 2000, 9: 87-95. 10.1159/000014627.CrossRefPubMed

19.

Pate JL, Landis Keyes P: Immune cells in the corpus luteum: friends or foes?. Reproduction. 2001, 122: 665-676. 10.1530/reprod/122.5.665.CrossRefPubMed

20.

Webb R, Woad KJ, Armstrong DG: Corpus luteum (CL) function: local control mechanisms. Domest Anim Endocrinol. 2002, 23: 277-285. 10.1016/S0739-7240(02)00163-7.CrossRefPubMed

21.

Rossi D, Zlotnik A: The biology of chemokines and their receptors. Annu Rev Immunol. 2000, 18: 217-242. 10.1146/annurev.immunol.18.1.217.CrossRefPubMed

22.

Garcia-Velasco JA, Arici A: Chemokines and human reproduction. Fertil Steril. 1999, 71: 983-993. 10.1016/S0015-0282(99)00120-X.CrossRefPubMed

23.

Ludwig A, Berkhout T, Moores K, Groot P, Chapman G: Fractalkine is expressed by smooth muscle cells in response to IFN-gamma and TNF-alpha and is modulated by metalloproteinase activity. J Immunol. 2002, 168: 604-612.CrossRefPubMed

24.

Baggiolini M: Chemokines and leukocyte traffic. Nature. 1998, 392: 565-568. 10.1038/33340.CrossRefPubMed

25.

Nelson PJ, Krensky AM: Chemokines, lymphocytes and viruses: what goes around, comes around. Curr Opin Immunol. 1998, 10: 265-270. 10.1016/S0952-7915(98)80164-7.CrossRefPubMed

26.

Herriot DM, Warnes GM, Kerin JF: Pregnancy-related chemotactic activity of human follicular fluid. Fertil Steril. 1986, 45: 196-201.PubMed

27.

Seow WK, Thong YH, Waters MJ, Walters M, Cummins JM: Isolation of a chemotactic protein for neutrophils from human ovarian follicular fluid. Int Arch Allergy Appl Immunol. 1988, 86: 331-336.CrossRefPubMed

28.

Harkin DG, Bignold LP, Herriot-Warnes DM, Kirby CA: Chemotaxis of polymorphonuclear leukocytes towards human pre-ovulatory follicular fluid and serum using a 'sparse-pore' polycarbonate filtration membrane. J Reprod Immunol. 1994, 27: 151-155. 10.1016/0165-0378(94)90030-2.CrossRefPubMed

29.

Sirotkin AV, Luck MR: Potential leukocyte attractants in the bovine peri-ovulatory ovary. Reprod Nutr Dev. 1995, 35: 675-683.CrossRefPubMed

30.

Murdoch WJ, McCormick RJ: Sequence analysis of leukocyte chemoattractant peptides secreted by periovulatory ovine follicles. Biochem Biophys Res Commun. 1992, 184: 848-852.CrossRefPubMed

31.

Gerdes U, Gafvels M, Bergh A, Cajander S: Localized increases in ovarian vascular permeability and leucocyte accumulation after induced ovulation in rabbits. J Reprod Fertil. 1992, 95: 539-550.CrossRefPubMed

32.

Brannstrom M, Mayrhofer G, Robertson SA: Localization of leukocyte subsets in the rat ovary during the periovulatory period. Biol Reprod. 1993, 48: 277-286.CrossRefPubMed

33.

Kerban A, Dore M, Sirois J: Characterization of cellular and vascular changes in equine follicles during hCG-induced ovulation. J Reprod Fertil. 1999, 117: 115-123.CrossRefPubMed

34.

Rohm F, Spanel-Borowski K, Eichler W, Aust G: Correlation between expression of selectins and migration of eosinophils into the bovine ovary during the periovulatory period. Cell Tissue Res. 2002, 309: 313-322. 10.1007/s00441-002-0602-3.CrossRefPubMed

35.

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. 10.1210/en.137.9.3762.PubMed

36.

Runesson E, Bostrom EK, Janson PO, Brannstrom M: The human preovulatory follicle is a source of the chemotactic cytokine interleukin-8. Mol Hum Reprod. 1996, 2: 245-250.CrossRefPubMed

37.

Oral E, Seli E, Bahtiyar MO, Jones EE, Arici A: Growth-regulated alpha expression in human preovulatory follicles and ovarian cells. Am J Reprod Immunol. 1997, 38: 19-25.CrossRefPubMed

38.

Karstrom-Encrantz L, Runesson E, Bostrom EK, Brannstrom M: Selective presence of the chemokine growth-regulated oncogene alpha (GROalpha) in the human follicle and secretion from cultured granulosa-lutein cells at ovulation. Mol Hum Reprod. 1998, 4: 1077-1083. 10.1093/molehr/4.11.1077.CrossRefPubMed

39.

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.CrossRefPubMed

40.

Runesson E, Ivarsson K, Janson PO, Brannstrom M: Gonadotropin- and cytokine-regulated expression of the chemokine interleukin 8 in the human preovulatory follicle of the menstrual cycle. J Clin Endocrinol Metab. 2000, 85: 4387-4395. 10.1210/jc.85.11.4387.PubMed

41.

Ushigoe K, Irahara M, Fukumochi M, Kamada M, Aono T: Production and regulation of cytokine-induced neutrophil chemoattractant in rat ovulation. Biol Reprod. 2000, 63: 121-126.CrossRefPubMed

42.

Wong KH, Negishi H, Adashi EY: Expression, hormonal regulation, and cyclic variation of chemokines in the rat ovary: key determinants of the intraovarian residence of representatives of the white blood cell series. Endocrinology. 2002, 143: 784-791. 10.1210/en.143.3.784.CrossRefPubMed

43.

Aust G, Brylla E, Lehmann I, Kiessling S, Spanel-Borowski K: Cloning of bovine RANTES mRNA and its expression and regulation in ovaries in the periovulatory period. FEBS Lett. 1999, 463: 160-164. 10.1016/S0014-5793(99)01599-9.CrossRefPubMed

44.

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. 10.1093/molehr/6.12.1085.CrossRefPubMed

45.

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. 10.1016/S0165-0378(97)82476-X.CrossRefPubMed

46.

Terranova PF, Rice VM: Review: cytokine involvement in ovarian processes. Am J Reprod Immunol. 1997, 37: 50-63.CrossRefPubMed

47.

Cavender JL, Murdoch WJ: Morphological studies of the microcirculatory system of periovulatory ovine follicles. Biol Reprod. 1988, 39: 989-997.CrossRefPubMed

48.

Barnes PJ, Karin M: Nuclear factor-kappaB: a pivotal transcription factor in chronic inflammatory diseases. N Engl J Med. 1997, 336: 1066-1071. 10.1056/NEJM199704103361506.CrossRefPubMed

49.

Hu J, You S, Li W, Wang D, Nagpal ML, Mi Y, Liang P, Lin T: Expression and regulation of interferon-gamma-inducible protein 10 gene in rat Leydig cells. Endocrinology. 1998, 139: 3637-3645. 10.1210/en.139.8.3637.PubMed

50.

Brannstrom M, Bonello N, Norman RJ, Robertson SA: Reduction of ovulation rate in the rat by administration of a neutrophil-depleting monoclonal antibody. J Reprod Immunol. 1995, 29: 265-270. 10.1016/0165-0378(95)00941-D.CrossRefPubMed

51.

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.CrossRefPubMed

52.

Chun SY, Daphna-Iken D, Calman D, Tsafriri A: Severe leukocyte depletion does not affect follicular rupture in the rat. Biol Reprod. 1993, 48: 905-909.CrossRefPubMed

53.

Murdoch WJ, McCormick RJ: Mechanisms and physiological implications of leucocyte chemoattraction into periovulatory ovine follicles. J Reprod Fertil. 1993, 97: 375-380.CrossRefPubMed

54.

Murdoch WJ, Van Kirk EA: Aetiology of attenuated luteal development in prednisolone-induced eosinopenic ewes. Reprod Fertil Dev. 2000, 12: 127-132.CrossRefPubMed

55.

Jasper MJ, Robertson SA, Van der Hoek KH, Bonello N, Brannstrom M, Norman RJ: Characterization of ovarian function in granulocyte-macrophage colony-stimulating factor-deficient mice. Biol Reprod. 2000, 62: 704-713.CrossRefPubMed

56.

Ferrara N, Chen H, Davis-Smyth T, Gerber HP, Nguyen TN, Peers D, Chisholm V, Hillan KJ, Schwall RH: Vascular endothelial growth factor is essential for corpus luteum angiogenesis. Nat Med. 1998, 4: 336-340.CrossRefPubMed

57.

Goede V, Schmidt T, Kimmina S, Kozian D, Augustin HG: Analysis of blood vessel maturation processes during cyclic ovarian angiogenesis. Lab Invest. 1998, 78: 1385-1394.PubMed

58.

Reynolds LP, Grazul-Bilska AT, Redmer DA: Angiogenesis in the corpus luteum. Endocrine. 2000, 12: 1-9. 10.1385/ENDO:12:1:1.CrossRefPubMed

59.

Belperio JA, Keane MP, Arenberg DA, Addison CL, Ehlert JE, Burdick MD, Strieter RM: CXC chemokines in angiogenesis. J Leukoc Biol. 2000, 68: 1-8.PubMed

60.

Ito WD, Arras M, Winkler B, Scholz D, Schaper J, Schaper W: Monocyte chemotactic protein-1 increases collateral and peripheral conductance after femoral artery occlusion. Circ Res. 1997, 80: 829-37.CrossRefPubMed

61.

Goede V, Brogelli L, Ziche M, Augustin HG: Induction of inflammatory angiogenesis by monocyte chemoattractant protein-1. Int J Cancer. 1999, 82: 765-770. 10.1002/(SICI)1097-0215(19990827)82:5<765::AID-IJC23>3.0.CO;2-F.CrossRefPubMed

62.

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.CrossRefPubMed

63.

Robertson SA, Mau VJ, Young IG, Matthaei KI: Uterine eosinophils and reproductive performance in interleukin 5-deficient mice. J Reprod Fertil. 2000, 120: 423-432. 10.1530/reprod/120.2.423.PubMed

64.

Gouon-Evans V, Pollard JW: Eotaxin is required for eosinophil homing into the stroma of the pubertal and cycling uterus. Endocrinology. 2001, 142: 4515-4521. 10.1210/en.142.10.4515.CrossRefPubMed

65.

Hosang K, Knoke I, Klaudiny J, Wempe F, Wuttke W, Scheit KH: Porcine luteal cells express monocyte chemoattractant protein-2 (MCP-2): analysis by cDNA cloning and northern analysis. Biochem Biophys Res Commun. 1994, 205: 148-153. 10.1006/bbrc.1994.2642.CrossRefPubMed

66.

Hosang K, Knoke I, Klaudiny J, Wempe F, Wuttke W, Scheit KH: Porcine luteal cells express monocyte chemoattractant protein-1 (MCP-1): analysis by polymerase chain reaction and cDNA cloning. Biochem Biophys Res Commun. 1994, 199: 962-968. 10.1006/bbrc.1994.1323.CrossRefPubMed

67.

Townson DH, Warren JS, Flory CM, Naftalin DM, Keyes PL: Expression of monocyte chemoattractant protein-1 in the corpus luteum of the rat. Biol Reprod. 1996, 54: 513-520.CrossRefPubMed

68.

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.CrossRefPubMed

69.

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. 10.1210/en.138.10.4517.CrossRefPubMed

70.

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 F2alpha. Biol Reprod. 1998, 58: 169-174.CrossRefPubMed

71.

Senturk LM, Seli E, Gutierrez LS, Mor G, Zeyneloglu HB, Arici A: Monocyte chemotactic protein-1 expression in human corpus luteum. Mol Hum Reprod. 1999, 5: 697-702. 10.1093/molehr/5.8.697.CrossRefPubMed

72.

Krusche CA, Vloet TD, Herrler A, Black S, Beier HM: Functional and structural regression of the rabbit corpus luteum is associated with altered luteal immune cell phenotypes and cytokine expression patterns. Histochem Cell Biol. 2002, 118: 479-489.PubMed

73.

Penny LA: Monocyte chemoattractant protein 1 in luteolysis. Rev Reprod. 2000, 5: 63-66. 10.1530/revreprod/5.2.63.CrossRefPubMed

74.

Davis JS, Rueda BR: The corpus luteum: an ovarian structure with maternal instincts and suicidal tendencies. Front Biosci. 2002, 7: d1949-1978.CrossRefPubMed

75.

Cavicchio VA, Pru JK, Davis BS, Davis JS, Rueda BR, Townson DH: Secretion of monocyte chemoattractant protein-1 by endothelial cells of the bovine corpus luteum: regulation by cytokines but not prostaglandin F2alpha. Endocrinology. 2002, 143: 3582-3589. 10.1210/en.2002-220388.CrossRefPubMed

76.

Tsai SJ, Kot K, Ginther OJ, Wiltbank MC: Temporal gene expression in bovine corpora lutea after treatment with PGF2alpha based on serial biopsies in vivo. Reproduction. 2001, 121: 905-913. 10.1530/reprod/121.6.905.CrossRefPubMed

77.

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.CrossRefPubMed

78.

Nagaosa K, Shiratsuchi A, Nakanishi Y: Determination of cell type specificity and estrous cycle dependency of monocyte chemoattractant protein-1 expression in corpora lutea of normally cycling rats in relation to apoptosis and monocyte/macrophage accumulation. Biol Reprod. 2002, 67: 1502-1508.CrossRefPubMed

79.

Choi C, Xu X, Oh JW, Lee SJ, Gillespie GY, Park H, Jo H, Benveniste EN: Fas-induced expression of chemokines in human glioma cells: involvement of extracellular signal-regulated kinase 1/2 and p38 mitogen-activated protein kinase. Cancer Res. 2001, 61: 3084-91.PubMed

80.

Yamaoka-Tojo M, Yamaguchi S, Nitobe J, Abe S, Inoue S, Nozaki N, Okuyama M, Sata M, Kubota I, Nakamura H, Tomoike H: Dual response to Fas ligation in human endothelial cells: apoptosis and induction of chemokines, interleukin-8 and monocyte chemoattractant protein-1. Coron Artery Dis. 2003, 14: 89-94. 10.1097/00019501-200302000-00010.CrossRefPubMed

81.

Lehmann I, Brylla E, Sittig D, Spanel-Borowski K, Aust G: Microvascular endothelial cells differ in their basal and tumour necrosis factor-alpha-regulated expression of adhesion molecules and cytokines. J Vasc Res. 2000, 37: 408-16. 10.1159/000025757.CrossRefPubMed

82.

Lawler DF, Brazil TJ, Dagleish MP, Watson ED: Chemoattractant properties of conditioned medium from equine corpora lutea collected at various stages of the oestrous cycle. Equine Vet J. 2002, 34: 279-282.CrossRefPubMed

83.

Duncan WC, Rodger FE, Illingworth PJ: The human corpus luteum: reduction in macrophages during simulated maternal recognition of pregnancy. Hum Reprod. 1998, 13: 2435-2442. 10.1093/humrep/13.9.2435.CrossRefPubMed

Title: Chemokines in the corpus luteum: Implications of leukocyte chemotaxis
Authors: David H Townson
Amy R Liptak
Publication date: 01-12-2003
Publisher: BioMed Central
Published in: Reproductive Biology and Endocrinology / Issue 1/2003
Electronic ISSN: 1477-7827
DOI: https://doi.org/10.1186/1477-7827-1-94

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Chemokines in the corpus luteum: Implications of leukocyte chemotaxis

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