Mast cells as novel mediators of reproductive processes

Frontiers in Immunology

Volumn 4, Issue FRB, 2013, Pages

  Woidacki, Katja ^a   Jensen, Federico ^a   Zenclussen, Ana C ^a  

^a OTTO VON GUERICKE UNIVERSITY   (Germany)

Author keywords

Implantation; Mast cells; Placenta; Pregnancy; Uterus

Indexed keywords

CONNECTIVE TISSUE GROWTH FACTOR; ESTRADIOL; PROGESTERONE; TRANSFORMING GROWTH FACTOR BETA;

BLASTOCYST; CELL DIFFERENTIATION; DISEASE ASSOCIATION; DISEASE EXACERBATION; ESTRUS CYCLE; HUMAN; IMMUNE RESPONSE; INTRAUTERINE GROWTH RETARDATION; MAST CELL; MAST CELL DEGRANULATION; NONHUMAN; PHENOTYPE; REPRODUCTION; REVIEW;

EID: 84883228301     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2013.00029     Document Type: Review

References (74)

1. Aluvihare, V. R., Kallikourdis, M., and Betz, A. G. (2004). Regulatory T cells mediate maternal tolerance to the fetus. Nat. Immunol. 5, 266-271.
2. Aydin, Y., Tunccel, N., Gürer, F., Tuncel, M., Koşar, M., and Oflaz, G. (1998). Ovarian, uterine and brain mast cells in female rats: cyclic changes and contribution to tissue histamine. Comp. Biochem. Physiol. 120, 255-262.
3. Batth, B. K., and Parshad, R. K. (2000). Mast cell dynamics in the house rat (Rattus rattus) ovary during estrus cycle, pregnancy and lactation. Eur. J. Morphol. 38, 17-23.
4. Bilinski, M. J., Thorne, J. G., Oh, M. J., Leonard, S., Murrant, C., Tayade, C., et al. (2008). Uterine NK cells in murine pregnancy. Reprod. Biomed. Online 16, 218-226.
5. Blois, S. M., Alba Soto, C. D., Tometten, M., Klapp, B. F., Margni, R. A., and Arck, P. C. (2004). Lineage, maturity, and phenotype of uterine murine dendritic cells throughout gestation indicate a protective role in maintaining pregnancy. Biol. Reprod. 70, 1018-1023.
6. Bosquiazzo, V. L., Ramos, J. G., Varayoud, J., Muñoz-de-Toro, M., and Luque, E. H. (2007). Mast cell degranulation in rat uterine cervix during pregnancy correlates with expression of vascular endothelial growth factor mRNA and angiogenesis. Reproduction 133, 1045-1055.
7. Bytautiene, E., Romero, R., Vedernikov, Y. P., El-Zeky, F., Saade, G. R., and Garfield, R. E. (2004). Induction of premature labor and delivery by allergic reaction and prevention by histamine H1 receptor antagonist. Am. J. Obstet. Gynecol. 191, 1356-1361.
8. Bytautiene, E., Vedernikov, Y. P., Saade, G. R., Romero, R., and Garfield, R. E. (2008). IgE-independent mast cell activation augments contractility of nonpregnant and pregnant guinea pig myometrium. Int. Arch. Allergy Immunol. 147, 140-146.
9. Cocchiara, R., Albeggiani, G., Di Trapani, G., Azzolina, A., Lampiasi, N., Rizzo, F., et al. (1992). Oestradiol enhances in vitro the histamine release induced by embryonic histamine-releasing factor (EHRF) from uterine mast cells. Hum. Reprod. 7, 1036-1041.
10. Cocchiara, R., Di Trapani, G., Azzolina, A., Albeggiani, G., and Geraci, D. (1986). Early embryonic histamine-releasing factor: a new model for human implantation. Hum. Reprod. 1, 445-447.
11. Drudy, L., Sheppard, B., and Bonnar, J. (1991a). Mast cells in the normal uterus and in dysfunctional uterine bleeding. Eur. J. Obstet. Gynecol. Reprod. Biol. 39, 193-201.
12. Drudy, L., Sheppard, B. L., and Bonnar, J. (1991b). The ultrastructure of mast cells in the uterus throughout the normal menstrual cycle and the postmenopause. J. Anat. 175, 51-63.
13. Fata, J. E., Chaudhary, V., and Khokha, R. (2001). Cellular turnover in the mammary gland is correlated with systemic levels of progesterone and not 17beta-estradiol during the estrous cycle. Biol. Reprod. 65, 680-688.
14. Garfield, R. E., Irani, A. M., Schwartz, L. B., Bytautiene, E., and Romero, R. (2006). Structural and functional comparison of mast cells in the pregnant versus nonpregnant human uterus. Am. J. Obstet. Gynecol. 194, 261-267.
15. Gaytan, F., Aceitero, J., Bellido, C., Sánchez-Criado, J. E., and Aguilar, E. (1991). Estrous cycle-related changes in mast cell numbers in several ovarian compartments in the rat. Biol. Reprod. 45, 27-33.
16. Ghildyal, N., Friend, D. S., Freelund, R., Austen, K. F., McNeil, H. P., Schiller, V., et al. (1994). Lack of expression of the tryptase mouse mast cell protease 7 in mast cells of the C57BL/6J mouse. J. Immunol. 153, 2624-2630.
17. Gibbons, A. F., and Chang, M. C. (1972). Number of mast cells in the rat uterus with special reference to its relation to hormonal treatment and decidual response. Biol. Reprod. 6, 193-203.
18. Greenwood, J. D., Minhas, K., di Santo, J. P., Makita, M., Kiso, Y., and Croy, B. A. (2000). Ultrastructural studies of implantation sites from mice deficient in uterine natural killer cells. Placenta 21, 693-702.
19. Habek, D., Cerkez-Habek, J., and Jalsovec, D. (2000). Anaphylactic shock in response to wasp sting in pregnancy. Zentralbl. Gynäkol. 122, 393-394.
20. Harvey, E. B. (1964). Mast cell distribution in the uterus of cycling and pregnant hamsters. Anat. Rec. 148, 507-516.
21. Humphries, D. E., Wong, G. W., Friend, D. S., Gurish, M. F., Qiu, W. T., Huang, C., et al. (1999). Heparin is essential for the storage of specific granule proteases in mast cells. Nature 400, 769-772.
22. Jensen, F., Woudwyk, M., Teles, A., Woidacki, K., Taran, F., Costa, S., et al. (2010). Estradiol and progesterone regulate the migration of mast cells from the periphery to the uterus and induce their maturation and degranulation. PLoS ONE 5:e14409. doi: 10.1371/journal.pone.0014409
23. Jones, R. E., Duvall, D., and Guillette, L. J. Jr. (1980). Rat ovarian mast cells: distribution and cyclic changes. Anat. Rec. 197, 489-493.
24. Karaca, T., Arikan, S., Kalender, H., and Yoruk, M. (2008). Distribution and heterogeneity of mast cells in female reproductive tract and ovary on different days of the oestrus cycle in Angora goats. Reprod. Domest. Anim. 43, 451-456.
25. Karaca, T., and Simşek, N. (2007). Effects of spirulina on the number of ovary mast cells in lead-induced toxicity in rats. Phytother. Res. 21, 44-46.
26. Kitamura, Y. (1989). Heterogeneity of mast cells and phenotypic change between subpopulations. Annu. Rev. Immunol. 7, 59-76.
27. Krishna, A., and Terranova, P. F. (1991). Compartmentalized mast cell degranulations in the ovarian hilum, fat pad, bursa and blood vessel regions of the cyclic hamster: relationships to ovarian histamine and blood flow. Acta Anat. (Basel) 141, 18-25.
28. Levi-Schaffer, F., Austen, K. F., Gravallese, P. M., and Stevens, R. L. (1986). Coculture of interleukin 3-dependent mouse mast cells with fibroblasts results in a phenotypic change of the mast cells. Proc. Natl. Acad. Sci. U.S.A. 83, 6485-6488.
29. Likar, I. N., and Likar, L. J. (1964). Acid mucopolysaccharides and mast cells in the bovine uterus at different stages of the sexual cycle. Acta Endocrinol. 46, 493-506.
30. Liu, Z., Kilburn, B. A., Leach, R. E., Romero, R., Paria, B. C., and Armant, D. R. (2004). Histamine enhances cytotrophoblast invasion by inducing intracellular calcium transients through the histamine type-1 receptor. Mol. Reprod. Dev. 68, 345-353.
31. Madeja, Z., Yadi, H., Apps, R., Boulenouar, S., Roper, S. J., Gardner, L., et al. (2011). Paternal MHC expression on mouse trophoblast affects uterine vascularization and fetal growth. Proc. Natl. Acad. Sci. U.S.A. 108, 4012-4017.
32. Martínez, L., Gimeno, M. F., Villán, L., Villar, M., and Rudolph, M. I. (1999). Nitroprusside stimulates contractility and the synthesis of 14C-acetylated PAF-like substances in estrogen primed-mouse uterine horns. Prostaglandins Other Lipid Mediat. 57, 49-62.
33. Menzies, F. M., Higgins, C. A., Shepherd, M. C., Nibbs, R. J., and Nelson, S. M. (2012). Mast cells reside in myometrium and cervix, but are dispensable in mice for successful pregnancy and labor. Immunol. Cell Biol. 90, 321-329.
34. Metcalfe, D. D., and Akin, C. (2001). Mastocytosis: molecular mechanisms and clinical disease heterogeneity. Leuk. Res. 25, 577-582.
35. Metcalfe, D. D., Baram, D., and Mekori, Y. A. (1997). Mast cells. Physiol. Rev. 77, 1033-1079.
36. Michaloudi, H. C., and Papadopoulos, G. C. (1999). Mast cells in the sheep, hedgehog and rat forebrain. J. Anat. 195, 577-586.
37. Mitani, R., Maeda, K., Fukui, R., Endo, S., Saijo, Y., Shinohara, K., et al. (2002). Production of human mast cell chymase in human myometrium and placenta in cases of normal pregnancy and preeclampsia. Eur. J. Obstet. Gynecol. Reprod. Biol. 101, 155-160.
38. Moon, T. C., St Laurent, C. D., Morris, K. E., Marcet, C., Yoshimura, T., Sekar, Y., et al. (2010). Advances in mast cell biology: new understanding of heterogeneity and function. Mucosal Immunol. 3, 111-128.
39. Mori, A., Zhai, Y. L., Toki, T., Nikaido, T., and Fujii, S. (1997a). Distribution and heterogeneity of mast cells in the human uterus. Hum. Reprod. 12, 368-372.
40. Mori, A., Nakayama, K., Suzuki, J., Nikaido, T., Isobe, M., and Fujii, S. (1997b). Analysis of stem cell factor for mast cell proliferation in the human myometrium. Mol. Hum. Reprod. 3, 411-418.
41. Murphy, V. E., Clifton, V. L., and Gibson, P. G. (2006). Asthma exacerbations during pregnancy: incidence and association with adverse pregnancy outcomes. Thorax 61, 169-176.
42. Murphy, V. E., Namazy, J. A., Powell, H., Schatz, M., Chambers, C., Attia, J., et al. (2011). A meta-analysis of adverse perinatal outcomes in women with asthma. BJOG 118, 1314-1323.
43. Nalbandov, E. V. (1971). "Endocrine control of implantation," in Biology of the Blastocyst. ed. R. J. Blandau (Chicago: University of Chicago Press).
44. Padilla, L., Reinicke, K., Montesino, H., Villena, F., Asencio, H., Cruz, M., et al. (1990). Histamine content and mast cells distribution in mouse uterus: the effect of sexual hormones, gestation and labor. Cell. Mol. Biol. 36, 93-100.
45. Parshad, R. K., and Kathpalia, K. (1993). Distribution and characteristics of mast cells in the chick ovary. Br. Poult. Sci. 34, 65-71.
46. Perlow, J. H., Montgomery, D., Morgan, M. A., Towers, C. V., and Porto, M. (1992). Severity of asthma and perinatal outcome. Am. J. Obstet. Gynecol. 167, 963-967.
47. Plaks, V., Birnberg, T., Berkutzki, T., Sela, S., BenYashar, A., Kalchenko, V., et al. (2008). Uterine DCs are crucial for decidua formation during embryo implantation in mice. J. Clin. Invest. 118, 3954-3965.
48. Pyzlak, M., Szewczyk, G., Szukiewicz, D., and Szczesniak, A. (2010). Histamine influence on apoptosis in trophoblast cell cultures. Inflamm. Res. 59(Suppl. 2), S213-S215.
49. Reibiger, I., and Spanel-Borowski, K. (2000). Difference in localization of eosinophils and mast cells in the bovine ovary. J. Reprod. Fertil. 118, 243-249.
50. Reynolds, D. S., Serafin, W. E., Faller, D. V., Wall, D. A., Abbas, A. K., Dvorak, A. M., et al. (1988). Immortalization of murine connective tissue-type mast cells at multiple stages of their differentiation by coculture of splenocytes with fibroblasts that produce Kirsten sarcoma virus. J. Biol. Chem. 263, 12783-12791.
51. Robinson-White, A., and Beaven, M. A. (1982). Presence of histamine and histamine-metabolizing enzyme in rat and guinea-pig microvascular endothelial cells. J. Pharmacol. Exp. Ther. 223, 440-445.
52. Rudolph, M. I., Rojas, I. G., and Penissi, A. B. (2004). Uterine mast cells: a new hypothesis to understand how we are born. Biocell 28, 1-11.
53. Salamonsen, L. A., Jeziorska, M., Newlands, G. F., Dey, S. K., and Woolley, D. E. (1996). Evidence against a significant role for mast cells in blastocyst implantation in the rat and mouse. Reprod. Fertil. Dev. 8, 1157-1164.
54. Schrey, M. P., Hare, A. L., Ilson, S. L., and Walters, M. P. (1995). Decidual histamine release and amplification of prostaglandin F2 alpha production by histamine in interleukin-1 beta-primed decidual cells: potential interactive role for inflammatory mediators in uterine function at term. J. Clin. Endocrinol. Metab. 80, 648-653.
55. Schumacher, A. (2013). Human Chorionic Gonadotropin as a central regulator of pregnancy immune tolerance. J. Immunol. (in press).
56. Shelesnyak, MC. (1957). Some experimental studies on the mechanism of ova-implantation in the rat. Recent Prog. Horm. Res. 13, 269-317.
57. Shelesnyak, M. C. (1959). Fall in uterine histamine associated with ovum implantation in pregnant rat. Proc. Soc. Exp. Biol. Med. 100, 380-381.
58. Shinohara, H., Nakatani, T., Morisawa, S., Matsuda, T., and Naruse, Y. (1987). Mast cells in the ovarian bursa of the golden hamster. Biol. Reprod. 36, 445-450.
59. Siddiqui, S., Goodman, N., McKenna, S., Goldie, M., Waugh, J., and Brightling, C. E. (2008). Pre-eclampsia is associated with airway hyperresponsiveness. BJOG 115, 520-522.
60. Skalko, R. G., Ruby, J. R., and Dyer, R. F. (1968). Demonstration of mast cells in the postnatal mouse ovary. Anat. Rec. 161, 459-463.
61. Song, H., Lim, H., Paria, B. C., Matsumoto, H., Swift, L. L., Morrow, J., et al. (2002). Cytosolic phospholipase A2alpha is crucial [correction of A2alpha deficiency is crucial] for 'on-time' embryo implantation that directs subsequent development. Development 129, 2879-2889.
62. Sorensen, T. K., Dempsey, J. C., Xiao, R., Frederick, I. O., Luthy, D. A., and Williams, M. A. (2003). Maternal asthma and risk of preterm delivery. Ann. Epidemiol. 13, 267-272.
63. Spicer, S. S. (1960). Siderosis associated with increased lipofuscins and mast cells in aging mice. Am. J. Pathol. 37, 457-475.
64. Szewczyk, G., Szukiewicz, D., Klimkiewicz, J., Pyzlak, M., Szewczyk, A., and Krajewska, K. (2005). Influence of histamine on the process of human trophoblast differentiation. Inflamm. Res. 54(Suppl. 1), S78-S79.
65. Szukiewicz, D., Szukiewicz, A., Maslinska, D., Gujski, M., Poppe, P., and Mazurek-Kantor, J. (1999a). Mast cell number, histamine concentration and placental vascular response to histamine in preeclampsia. Inflamm. Res. 48(Suppl. 1), S39-S40.
66. Szukiewicz, D., Szukiewicz, A., Maslinska, D., Poppe, P., Gujski, M., and Olszewski, M. (1999b). Mast cells and histamine in intrauterine growth retardation-relation to the development of placental microvessels. Inflamm. Res. 48(Suppl. 1), S41-S42.
67. Tsuji, K., Nakahata, T., Takagi, M., Kobayashi, T., Ishiguro, A., Kikuchi, T., et al. (1990). Effects of interleukin-3 and interleukin-4 on the development of "connective tissue-type" mast cells: interleukin-3 supports their survival and interleukin-4 triggers and supports their proliferation synergistically with interleukin-3. Blood 75, 421-427.
68. van Overveld, F. J. (1990). Some aspects of mast cell subtypes from human lung tissue. Agents Actions 30, 24-29.
69. Varayoud, J., Ramos, J. G., Bosquiazzo, V. L., Muñoz-de-Toro, M., and Luque, E. H. (2004). Mast cells degranulation affects angiogenesis in the rat uterine cervix during pregnancy. Reproduction 127, 379-387.
70. Wintroub, B. U., Schechter, N. B., Lazarus, G. S., Kaempfer, C. E., and Schwartz, L. B. (1984). Angiotensin I conversion by human and rat chymotryptic proteinases. J. Invest. Dermatol. 83, 336-339.
71. Woidacki, K., Popovic, M., Metz, M., Schumacher, A., Linzke, N., Teles, A., et al. (2013). Mast cells rescue implantation defects caused by c-kit deficiency. Cell Death Dis. 4, e462.
72. Wordinger, R. J., Jackson, F. L., and Morrill, A. (1986). Implantation, deciduoma formation and live births in mast cell-deficient mice (W/Wv). J. Reprod. Fertil. 77, 471-476.
73. Wordinger, R. J., Orr, E. L., Pace, K., Oakford, L., and Morrill, A. (1985). An assessment of mast-cell deficient mice (W/Wv) as a model system to study the role of histamine in implantation and deciduoma formation. J. Reprod. Fertil. 73, 451-456.
74. Zenclussen, A. C., Gerlof, K., Zenclussen, M. L., Ritschel, S., Zambon Bertoja, A., Fest, S., et al. (2006). Regulatory T cells induce a privileged tolerant microenvironment at the fetal-maternal interface. Eur. J. Immunol. 36, 82-94.