Trophoblast phagocytic program: Roles in different placental systems

International Journal of Developmental Biology

Volumn 54, Issue 2-3, 2010, Pages 495-505

  Bevilacqua, Estela ^a   Hoshida, Mara Sandra ^a   Amarante Paffaro, Andrea ^b   Albieri Borges, Andrea ^c   Gomes, Sara Zago ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b FEDERAL UNIVERSITY OF ALFENAS   (Brazil)

^c STATE UNIVERSITY OF RIO DE JANEIRO   (Brazil)

Author keywords

Defense mechanism; Erythrophagocytosis; Phagocytosis; Placenta; Trophoblast

Indexed keywords

GAMMA INTERFERON; NITRIC OXIDE; REACTIVE OXYGEN METABOLITE;

ARTICLE; BLASTOCYST; DEFENSE MECHANISM; EMBRYO DEVELOPMENT; ENDOCYTOSIS; ERYTHROPHAGOCYTOSIS; HUMAN; IMMUNOMODULATION; INTERNALIZATION; MOTHER FETUS RELATIONSHIP; NIDATION; NONHUMAN; NUTRITION; OXIDATIVE STRESS; PHAGOCYTOSIS; PLACENTA DEVELOPMENT; PLACENTA FUNCTION; PRIORITY JOURNAL; PROTEIN SYNTHESIS; REPRODUCTION; SIGNAL TRANSDUCTION; TISSUE REGENERATION; TROPHOBLAST; ANIMAL; FEMALE; FETOMATERNAL TRANSFUSION; PHYSIOLOGY; PLACENTA; PREGNANCY; REVIEW;

ANIMALS; EMBRYO IMPLANTATION; FEMALE; MATERNAL-FETAL EXCHANGE; PHAGOCYTOSIS; PLACENTA; PLACENTATION; PREGNANCY; TROPHOBLASTS;

EID: 77950348827     PISSN: 02146282     EISSN: None     Source Type: Journal    
DOI: 10.1387/ijdb.082761eb     Document Type: Article

References (92)

1. ABRAHAMS, V.M. and MOR, G. (2005). Toll-like receptors and their role in the trophoblast. Placenta 26: 540-547.
2. AFONSO, S., ROMAGNANO, L. and BABIARZ, B. (1997). The expression and function of cystatin C and cathepsin B and cathepsin L during mouse embryo implantation and placentation. Development 124: 3415-3425.
3. AL-ABBASS, A.H. and SCHULTZ, R.L. (1966). Phagocytic activity of the rat placenta. J. Anat. 100: 349-359.
4. ALBIERI, A. and BEVILACQUA, E. (1996). Induction of erythrophagocytic activity in cultured mouse trophoblast cells by phorbol myristate acetate and all-transretinal. Placenta 17: 507-512.
5. ALBIERI, A., AMARANTE, A.M., GAGIOTI, S. and BEVILACQUA, E. (2001). In vitro behavior of post implanting and placental trophoblast cells during zymosan challenging and interferon-g stimulation. Placenta 22: A11.
6. ALBIERI, A., HOSHIDA, M.S., GAGIOTI, S.M., LEANZA, E.C., ABRAHAMSOHN, I., CROY, A., ASHKAR, A.A. and BEVILACQUA, E. (2005). Interferon-gamma alters the phagocytic activity of the mouse trophoblast. Reprod. Biol. Endocrinol. 3: 34.
7. ALBIERI, A., KIPNIS, T. and BEVILACQUA, E. (1999). Possible role of activated complement component C3 in phagocytic activity exhibited by the mouse trophoblast. Am. J. Reprod. Immunol. 41: 343-352.
8. ALEXANDER, C. M., HANSEL, E., BEHRENDSTEN, O., FLANDERS, M.L., KISHNANI, N.S., HAWKES, S.P. and WERB, Z. (1996). Expression and function of matrix metalloproteinases and their inhibitors at the maternalembryonic boundary during mouse embryo implantation. Development 122: 1723-1736.
9. AMARANTE-PAFFARO, A., QUEIROZ, G.S., CORREA, S.T., SPIRA, B., and BEVILACQUA, E. (2004). Phagocytosis as a potential mechanism for microbial defense of mouse placental trophoblast cells. Reproduction 128: 207-218.
10. ARKO-MENSAH, J., JULIÁN, E., SINGH, M. and FERNÁNDEZ, C. (2007). TLR2 but not TLR4 signalling is critically involved in the inhibition of IFN-gammainduced killing of mycobacteria by murine macrophages. Scand. J. Immunol. 65: 148-157.
11. ASSÉMAT, E., VINOT, S., GOFFLOT, F., LINSEL-NITSCHKE, P., ILLIEN, F., CHTELET, F., VERROUST, P., LOUVET-VALLÉE, S., RINNINGER, F. and KOZYRAKI, R. (2005). Expression and role of cubilin in the internalization of nutrients during the peri-implantation development of the rodent embryo. Biol. Reprod. 72: 1079-1086.
12. BABIOR, B.M. (2004). NADPH oxidase. Curr. Opin. Immunol. 16: 42-47.
13. BADWEY, J.A. and KARNOVSKY, M.L. (1980). Active oxygen species and the functions of phagocytic leukocytes. Ann. Rev. Biochem. 49: 695-726.
14. BAUMBACH, G.A., BARTLEY, N.G., KATTESH, H.G. and GODKIN, J.D. (1990). Immunolocalization and endocytosis of the uterine secretory protein, uteroferrin, in pre-implantation pig trophectoderm on day 11 of pregnancy. Anat. Embryol. 182: 563-568.
15. BEVILACQUA, E. and ABRAHAMSOHN, P.A. (1988). Ultrastructure of trophoblast giant cell transformation during invasive stage of implantation of the mouse embryo. J. Morphol. 198: 341-451.
16. BEVILACQUA, E. and ABRAHAMSOHN, P.A. (1989) Trophoblast invasion during implantation of the mouse embryo. Arch. Biol. Med. Exp. 22: 107-118.
17. BEVILACQUA, E. and ABRAHAMSOHN, P.A. (1994) Invasiveness of mouse trophoblastic cells in connective tissue. Acta Anat (Basel), 150: 246-252.
18. BRIGGS, R.T., KARNOVSKY, M.L. and KARNOVSKY, M.J. (1975). Cytochemical demonstration of hydrogen peroxide in polymorphonuclear leukocyte phagosomes. J. Cell. Biol. 64: 254-260.
19. BURROWS, T.D.; KING, A. and LOKE, Y.W. (1996). Trophoblast migration during human placental implantation. Human Reprod. Update 2: 307-321.
20. BURTON, G.J. (1982). Placental uptake of maternal erythrocytes-a comparative survey. Placenta 3: 407-434.
21. BURTON, G.J., WATSON, A.L., HEMPSTOCK, J., SKEPPER, J.N. and JAUNIAUX E. (2002). Uterine glands provide histiotrophic nutrition for the human fetus during the first trimester of pregnancy. J. Clin. Endocrinol. Metab. 87: 2954-2959.
22. CHOY, M.Y. and MANYONDA, I.T. (1998). The phagocytic activity of human first trimester extravillous trophoblast. Hum. Reprod. 13: 2941-2949.
23. CLINT, J.M., WAKELY, J. and OCKLEFORD, C.D. (1979). Differentiated regions of human placental cell surface associated with attachment of chorionic villi, phagocytosis of maternal erythrocytes and syncytiotrophoblast repair. Proc. R. Soc. Lond. B. Biol. Sci. 204: 345-353.
24. COHEN, M. and BISCHOF, P. (2007). Factors regulating trophoblast invasion. Gynecol. Obstet. Invest. 64: 126-130.
25. CONTRACTOR, S.F and KRAKAUER, K. (1976). Pinocytosis and intracellular digestion of 125I-labelled haemoglobin by trophoblastic cells in tissue culture in the presence and absence of serum. J. Cell Sci. 21: 595-607.
26. COOPMAN, P.J., DO, M.T., THOMPSON, E.W. and MUELLER, S.C. (1998). Phagocytosis of cross-linked gelatin matrix by human breast carcinoma cells correlates with their invasive capacity. Clin. Cancer Res. 4: 507-515.
27. DARNELL, J.E.JR., KERR, I.M. and STARK, G.R. (1994). Jak-STAT pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins. Science 264: 1415-1421.
28. DELGADO, M.A. and SANTOS-BUCH, C.A. (1978). Transplacental transmission and fetal parasitism of Trypanosoma cruzi in outbread white Swiss mice. Am. J. Trop. Med. Hyg. 27: 1108-1115.
29. DOYLE, S.E., O'CONNELL, R.M., MIRANDA, G.A., VAIDYA, S.A., CHOW, E.K., LIU, P.T., SUZUKI, S., SUZUKI, N., MODLIN, R.L., YEH, W.C., LANE, T.F. and CHENG, G. (2004) Toll-like receptors induce a phagocytic gene program through p38. J. Exp. Med. 199: 81-90.
30. DRAKE, B.L. and RODGER, J.C. (1987). Phagocytic properties of cultured murine trophoblast. Placenta 8: 129-134.
31. ENDERS, A.C. (1976). Anatomical aspects of implantation. J. Reprod. Fertil. Suppl. 25: 1-15.
32. ENDERS, A.C. and CARTER, A.M. (2006). Comparative placentation: some interesting modifications for histotrophic nutrition A Review. Placenta 27, Suppl A: S11-S16.
33. ENDERS, A.C. and NELSON, D.M. (1973). Pinocytotic activity of the uterus of the rat. Am. J. Anat. 138: 277-299.
34. ENDERS, A.C. and SCHLAFKE, S. (1969). Cytological aspects of trophoblastuterine interaction in early implantation. Am. J. Anat. 125: 1-29.
35. ENDERS, A.C., BLANKENSHIP, T.N., CONLEY, A.J. and JONES, C.J. (2006). Structure of the midterm placenta of the spotted hyena, Crocuta crocuta, with emphasis on the diverse hemophagous regions. Cells Tissues Organs 183: 141-155.
36. FERRO, E.A.V. and BEVILACQUA, E. (1994) Trophoblastic invasion of the uterine epithelium in Calomys callosus (Rodentia, Cricetidae). J. Morph. 221: 139-152.
37. FOLDES, J.J., SCHWARTZ, J. and KEHATY, T. (1973). Trophoblast and phagocytosis. I. In vitro phagocytosis by human cultured trophoblasts. Int. J. Fertil. 20: 228-230.
38. FRAULI M. and LUDWIG H. (1987). Demonstration of the ability of Hofbauer cells to phagocytose exogenous antibodies. Eur. J. Obstet. Gynecol. Reprod. Biol. 26: 135-144.
39. FUCHS, R. and ELLINGER, I. (2004). Endocytic and transcytotic processes in villous syncytiotrophoblast: role in nutrient transport to the human fetus. Traffic 5: 725-738.
40. GAGIOTI, S., COLEPICOLO, P. and BEVILACQUA, E. (1995). Post-implantation mouse embryos have the capability to generate and release reactive oxygen species. Reprod. Fertil. Dev. 7: 1111-1116.
41. GAGIOTI, S., SCAVONE, C. and BEVILACQUA, E. (2000). Participation of the mouse implanting trophoblast in nitric oxide production during pregnancy. Biol. Reprod. 62: 260-268.
42. GARDNER, R.L. (1975). Analysis of determination and differentiation in the early mammalian embryo using intraand interspecific chimeras. Symp. Soc. Dev. Biol. 33: 207-236.
43. GATTONI, A., PARLATO, A., VANGIERI, B., BRESCIANI, M. and DERNA, R. (2006). Interferon-gamma: biologic functions and HCV terapy (type I/II) (2 of 2 parts). Clin Ter. 157: 457-468.
44. GOMES, S.Z. and BEVILACQUA, E. (2008). NAD(P)H-oxidase expression in trophoblast cells. Placenta 29: 114.
45. GONÇALVES, C.R., ANTONIN, S.I., VIANNA-MORGANTE, A.M., MACHADOSANTELLI, G.M. and BEVILACQUA, E. (2003). Developmental changes in the ploidy of mouse implanting trophoblast cells in vitro. Histochem. Cell Biol., 119: 189-198.
46. GORETZSKI, L., SCHMITT, M., MANN, K., CALVETE, J., CHUCHOLOWSKI, N., KRAMER, M., GUNZLER, W., JANICKE, F. and GRAEFF, H. (1992). Effective activation of the proenzyme form of the urokinase-type plasminogen activator (prouPA) by the cysteine protease cathepsin L. FEBS Lett. 297: 112-118.
47. HARVEY, M.B., LECO, K.J., ARCELLANA-PANLILIO, M. Y., ZHANG, X., EDWARDS, D.R. and SCHULTZ, G.A. (1995). Proteinase expression in early mouse embryos is regulated by leukemia inhibitory factor and epidermal growth factor. Development 121: 1005-1014.
48. HATA, T., OHKAWA, K., TOMITA, M., and KISHINO, M. (1981). Phagocytosis of human cytotrophoblast cell invading into decidual tissue in early stage of gestation. Acta Obstet Gynaecol Jpn. 33: 537-544.
49. HEYNER, S., RAO, L.V., JARETT, L. and SMITH, R.M. (1989). Preimplantation mouse embryos internalize maternal insulin via receptor-mediated endocytosis: Pattern of uptake and functional correlations. Dev. Biol. 134: 48-58.
50. HOSHIDA, M.S., GORJÃO, R., LIMA, C., CURI, R., DAHER, S. and BEVILACQUA, E. (2007). Regulation of gene expression in mouse trophoblast cells by interferon-gamma. Placenta 28: 1059-1072.
51. HUBRECHT, A.A.W. (1889). Studies in mammalian embryology. I. The placentation of Erinaceus europaeus, with remarks on the phylogeny of the placenta. Q J Microsc Sci 30: 283-404.
52. JONES, C.J.P., ENDERS, A.C. and FAZLEABAS, A.T. (2001). Early implantation events in the baboon (Papio anubis) with special reference to the establishment of anchoring villi. Placenta 22: 440-456.
53. JOYCE, J.A. and HANAHAN, D. (2004). Multiple roles for cysteine cathepsins in cancer. Cell Cycle 3: 1516-1619.
54. KATZ, S. and ABRAHAMSOHN, P.A. (1987). Involution of the antimesometrial deciduas in the mouse (an ultrastructural study). Anat. Embryol. 176: 251-258.
55. KNOTH, M and LARSEN, JF. (1972). Ultrastructure of a human implantation site. Acta Obstet. Gynecol. Scand. 51: 385-393.
56. LAFUSE, W.P., ALVAREZ, G.R., CURRY, H.M. and ZWILLING, B.S. (2006). Mycobacterium tuberculosis and Mycobacterium avium inhibit IFN-gammainduced gene expression by TLR2-dependent and independent pathways. J Interferon Cytokine Res. 26: 548-561.
57. LEANZA, E.C., HOSHIDA, M.S., COSTA, A.F., FERNANDES, C.M., TEIXEIRA C.F.P. and BEVILACQUA, E. (2007). Signaling molecules involved in IFNgamma-inducible nitric oxide synthase expression in the mouse trophoblast. Am. J. Reprod. Immunol. 58: 537-546.
58. LEE, W., SODEK, J. and MCCULLOCH, C.A. (1996). Role of integrins in regulation of collagen phagocytosis by human fibroblasts. J. Cell Physiol. 168: 695-704.
59. LESLIE, R.G. and NIELSEN, C.H. (2004). The classical and alternative pathways of complement activation play distinct roles in spontaneous C3 fragment deposition and membrane attack complex (MAC) formation on human B lymphocytes. Immunology 111: 86-90.
60. LORENZON, A.R., ROCHA, C.R.R., VIEIRA, J.S., GOMES, S.Z. and BEVILACQUA E. (2008). Activation of NAD(P)H-oxidase and xanthine-oxidase and trophoblast reactive oxygen species production. Placenta 29: 115.
61. MA, Y., KRIKUN, G., ABRAHAMS, V.M., MOR, G., and GULLER S. (2007). Cell type-specific expression and function of toll-like receptors 2 and 4 in human placenta: implications in fetal infection. Placenta 28: 1024-1031.
62. MANYONDA, I.T. and CHOY, M.Y. (1999). Collagen phagocytosis by human extravillous trophoblast: potential role in trophoblastic invasion. J. Soc. Gynecol. Investig. 6: 158-166.
63. MATSUBARA, S., TAKIZAWA, T., YAMADA, T., MINAKAMI, H. and SATO, I. (2000). Phagocytosis of chorion laeve trophoblasts in patients with chorioamnionitis-associated preterm delivery: ultrastructural and enzyme-histochemical observations. Placenta 21: 273-279.
64. MESS, A. and CARTER, A.M. (2006). Evolutionary transformations of fetal membrane characters in Eutheria with special reference to Afrotheria. J. Exp. Zoolog. B. Mol. Dev. Evol. 306: 140-163.
65. MINAZAKI, C.K., GAGIOTI, S., ZAGO, D., TERRA, W., ARAUJO, V.C., OLIVEIRA, R.A. and BEVILACQUA, E. (2008). Acid phosphatase and cathepsin D are active expressed enzymes in the placenta of the cat. Res. Vet. Sci. 84: 326-334.
66. MURPHY, G., WARD, R., GAVRILOVIC, J. and ATKINSON S. (1992). Physiological mechanisms for metalloproteinase activation. Matrix Suppl 1: 224-230.
67. MYATT, L and CUI, X. (2004). Oxidative stress in the placenta. Histochem. Cell Biol. 122: 369-382.
68. NATHAN, C.F., MURRAY, H.W., WIEBE, M.E., and RUBIN, B.Y. (1983). Identification of interferonas the lymphokine that activates human macrophage oxidative metabolism and antimicrobial activity. J. Exp. Med. 158: 670-689
69. NERES, R., MARINHO, C.R.F., GONÇALVES, L.A., CATARINO, M.B. and PENHAGONÇALVES, C. (2008). Pregnancy outcome and placenta pathology in Plasmodium berghei ANKA infected mice reproduce the pathogenesis of severe malaria in pregnant women. PLoS ONE 3: e1608.
70. O'MAHONY, D.S., PHAM, U., IYER, R., HAWN, T.R. and LILES, W.C. (2008). Differential constitutive and cytokine-modulated expression of human Toll-like receptors in primary neutrophils, monocytes, and macrophages. Int. J. Med. Sci. 5:1-8.
71. PARKENING, T.A. (1976). An ultrastructural study of implantation in the golden hamster. II. Trophobalstic invasion and removal of the uterine epithelium. J. Anat. 122: 211-230.
72. PARR, M.B. and PARR, E.L. (1974). Uterine luminal epithelium: protrusions mediate endocytosis, not apocrine secretion, in the rat. Biol. Reprod. 11: 220-233.
73. PAVIA, C.S. (1983). Expression of the cell-mediated antimicrobial immunity by mouse trophoblast monolayers. J. Infect. Dis. 147: 1006-1010.
74. PETERS, T.J., ALBIERI, A., BEVILACQUA, E., CHAPMAN, B.M., CRANE, L.H., HAMLIN, G.P., SEIKI, M. and SOARES, M.J. (1999). Differentiation-dependent expression of gelatinase B/matrix metalloproteinase-9 in trophoblast cells. Cell Tissue Res. 295: 287-296.
75. RASSOULZADEGAN, M., ROSEN, B.S., GILLOT, I. and CUZIN, F. (2000). Phagocytosis reveals a reversible differentiated state early in the development of the mouse embryo. EMBO J. 19: 3295-3303.
76. RED-HORSE, K., ZHOU, Y., GENBACEV, O., PRAKOBPHOL, A., FOULK, R., MCMASTER, M. and FISHER, S.J. (2004). Trophoblast differentiation during embryo implantation and formation of the maternal-fetal interface. J. Clin. Invest. 114: 744-754.
77. ROCHA, C.R., LORENZON, A.R., VIEIRA, J.S., GOMES, S.Z. and BEVILACQUA E. (2007). superoxide anion production by trophoblast cells. Placenta 28: A.10.
78. SALMINEN, A., PAANANEN, R., VUOLTEENAHO, R., METSOLA, J., OJANIEMI, M., AUTIO-HARMAINEN, H. and HALLMAN, M. (2008). Maternal endotoxininduced preterm birth in mice: fetal responses in toll-like receptors, collectins, and cytokines. Pediatr Res. 63: 280-286.
79. SCHLESINGER, M. and KOREN, Z. (1967). Mouse trophoblast cells in tissue culture. Fertil. Steril. 18: 95-101.
80. SEAL, U.S., SINHA, A.A. and DOE, R.P. (1972). Placental iron transfer: relationship to placental anatomy and phylogeny of the mammals. Am. J. Anat. 134: 263-269.
81. SHILOH, M.U., MACMICKING, J.D., NICHOLSON, S., BRAUSE, J.E., POTTER, S., MARINO, M., FANG, F., DINAUER, M., and NATHAN, C. (1999). Phenotype of mice and macrophages deficient in both phagocyte oxidase and inducible nitric oxide synthase. Immunity 10: 29-38.
82. SIMMONS, D.G., FORTIER, A.L. and CROSS, J.C. (2007). Diverse subtypes and developmental origins of trophoblast giant cells in the mouse placenta. Dev Biol 304: 567-578.
83. SMITH, R.M., GARSIDE, W.T., AGHAYAN, M., SHI, C.Z., SHAH, N., JARETT, L. and HEYNER, S. (1993). Mouse preimplantation embryos exhibit receptormediated binding and transcytosis of maternal insulin-like growth factor I. Biol. Reprod. 49: 1-12.
84. STOFFEL, M.H., FRIESS, A.E. and HARTMANN, S.H. (2000). Ultrastructural evidence of transplacental transport of immunoglobulin G in bitches. J. Reprod. Fertil. 188: 315-326.
85. SWANSON, J.A. and HOPPE, A.D. (2004). The coordination of signaling during Fc receptor-mediated phagocytosis. J. Leukoc. Biol. 76: 1093-1103.
86. TEESALU, T., BLASI, F. and TALARICO, D. (1996). Embryo implantation in mouse: fetomaternal coordination in the pattern of expression of uPA, uPAR, PAI-1 and alpha 2MR/LRP genes. Mech. Dev. 56: 103-116.
87. UNDERHILL, D.M. and OZINSKY, A. (2002). Phagocytosis of microbes: Complexity in Action. Annu. Rev. Immunol. 20: 825-852.
88. VARANOU, A., WITHINGTON, S.L., LAKASING, L., WILLIAMSON, C., BURTON, G.J. and HEMBERGER, M. (2006). The importance of cysteine cathepsin proteases for placental development. J. Mo.l Med. 84: 305-317.
89. WANG, T., HAMANN, W. and HARTGE, R. (1983). Strucutural aspects of a placenta from a case of maternal acute lymphatic leukaemia. Placenta 4: 185-195.
90. WELSH, A.O. and ENDERS, A.C. (1985). Light and electron microscopic examination of the mature decidual cells of the rat with emphasis on the antimesometrial deciduas and its degeneration. Am. J. Anat. 172: 1-30.
91. WELSH, A.O. and ENDERS, A.C. (1991). Chorioallantoic placenta formation in the rat: I. Luminal epithelial cell death and extracellular matrix modifications in the mesometrial region of implantation chambers. Am. J. Anat. 192: 215-231.
92. ZYBINA, T.G. and ZYBINA, E.V. (2005). Cell reproduction and genome multiplication in the proliferative and invasive trophoblast cell populations of mammalian placenta. Cell Biol. Int. 29: 1071-1083.