2005, Number 1
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Vet Mex 2005; 36 (1)
Reduction of total lymphocyte migration to the uterus during the fi rst days of pregnancy and pseudopregnancy of the rabbit (Oryctolagus cuniculus)
Zamora HVX, Villaseñor GH, Anzaldúa ASR, Pérez-Martínez M
Language: English/Spanish
References: 135
Page: 63-73
PDF size: 576.79 Kb.
ABSTRACT
The initiation of pregnancy is a transitional period during which very important changes in
sexual hormone levels are registered. These changes cause multiple morphologic changes in
the endometrium that are quite necessary for implantation to occur. The objective of the present
study was to evaluate the migration activity of total lymphocytes in the endometrium of
New Zealand breed, four months old, white female rabbits maintained in individual cages in
laboratory animal conditions with cycles of 12 hours light and 12 hours darkness, with feed
and water
ad libitum. With these animals three different groups were formed:
a) pregnant
animals on day 1, 2, 3, 4, 5 and 8;
b) animals in a pseudo-pregnant state on days 1, 2, 3, 4,
5 and 8 following the administration of 100 IU of human chorionic gonadotropin (hCG); and
c)
non pregnant animals (NP). The rabbits were slaughtered at different times according to the
experimental protocol through a lethal sodium pentobarbital intracardiac injection once the
rabbit were anesthetized. After the slaughter, fragments of both uterine horns were excised,
and fragments of uterine tissue were obtained, fi xed and processed by paraffi n inclusion to
perform histological cuts that were stained with hematoxylin-eosin (H & E) and Giemsa. Total
lymphocytes present in the luminal epithelial layer and lamina propia of the stroma of the
endometrium were counted. The number of total lymphocytes present in the rabbit endometrium
during days 1 to 5 and 8 of gestation and pseudo-gestation decreased (P ‹ 0.05) with
respect to the values found in non-pregnant, control females (NG). However, in the pseudopregnant
animals a decrease in the number of lymphocytes found on days 1 and 2 was more
evident than what was observed for these days in the pregnant rabbits. Day 8th was characterized
by presenting a smaller quantity of cells than the rest of the evaluated days. It is concluded
that during in the fi rst 8 days of gestation the number of lymphocytes present in the
rabbit endometrium decreases and that pseudo-pregnant rabbits present a similar condition.
REFERENCES
1.Hafez ES. Reproducción e inseminación artificial en animales. 6a ed. México: McGraw-Hill-Interamericana,1996.
2.Alvariño MR. Control de la Reproducción en el conejo.Madrid, España: Mundi- Prensa, 1993.
3.Lefevre B, Cailloi M. Relationship of oestrous behaviour with follicular growth and sex steroid concentration in the follicular fl uid in the domestic rabbit. Ann Biol Anim Bioch Biophys1978;18:1435-1441.
4.García X F. Fisiología de la reproducción en la coneja (Capitulo 2). En: Biología de la reproducción en la hembra del conejo doméstico. Universidad Politécnica de Valencia. Valencia, España 1991: 13-25.
5.Enkhuizen PJM, Van M. Distribution in size and number of ovarian follicles in the pregnant rabbit before and after revulation with hCG. Twelfth annual Conference of Australian Society for Reproductive Biology;1980; University of New England,1980.
6.Pla H, Baselga M, García F, Deltoro J. Categorías foliculares asociadas al comportamiento de monta en el conejo de carne: efectos sobre las estructuras uterinas. III Congreso Mundial de Cunicultura; 1984; Roma, Italia: Actas Vol. II 1984: 446-452.
7.Molina I, Pla M, García F. Poblaciones de folículos en función del comportamiento de monta en conejas:Utilización de un método simple para la medición de los folículos. ITEA 1986; 66: 21-26.
8.Holt JA. Regulation of progesterone production in the rabbit corpus luteum. Biol Reprod 1989;40:201-208.
9.Miller JB, Keyes PL. A mechanism for regression of the rabbit corpus luteum: uterine induced loss of luteal responsiveness to 17ß-estradiol. Biol Reprod 1976;15:511-518.
10.Browning J, Keyes FL, Wolfe R. Comparison of serum progesterone, 20-dihydroprogesterone and estradiol-17ß in pregnant and pseudo-pregnant rabbit: evidence
for post implantation recognition of pregnancy. Biol Reprod 1980;23:1014-1019. 11.Anzaldúa ASR, Peréz MM, Castro RJI. Variación en los índices de mitosis y apoptosis del epitelio uterino de la coneja durante los días previos a la implantación.
Téc Pecu Méx 2001;39:59-68.
12.Lessey BA, Arnold JT. Paracrine signaling in the endometrium integrins and the establishment of uterine receptivity. J Reprod Immunol 1998;39:105-116.
13.Yang YQ, Kudolo GB, Harper MJK. Binding of platelet activating factor to oviductal membranes during early pregnancy in the rabbit. J Lipid Med 1992;5:77-96.
14.Spinks NR, Ryan JP, O¨Neill C. Antagonists of embryo-derived platelet-activating factor act by inhibiting the ability of the mouse embryo to implant. J Reprod
15.Orozco C, Perkins T, Clarke FM. Platelet-activating factor induces the expression of early pregnancy factor in the female mice. J Reprod Fertil 1986;78:549-555.
16.Sueoka K, Dharmarajan AM, Myazaki T, Atlas SJ, Wallach EE. Platelet activating factor induced early pregnancy factor activity from the perfused rabbit ovary and oviduct. Am J Obstet Gynecol 1988;159:1580-1584.
17.Hansen PJ, Skopets B. Temporal relationship between progesterone and uterine lymphocyte-inhibitory activity in ewes. Vet Rec 1992;131:371-372.
18.Stephenson DJ, Hensen PJ. Induction by progesterone of immunosuppresive activity in utero secretions of ovariectomized ewes. Endocrinology 1999;129:3168-
19.Bailly A, Atger M, Atger P, Cerbón MA, Alison M, Vu Hai MT, et al. The rabbit uteroglobin gene. Structure and interaction with the progesterone receptor. J Biol
Chem 1983;258:10384-10389.
20.Gutierrez-Sagal R, Perez-Palacios G, Langley E, Pasapera AM, Castro I, Cerbon MA. Endometrial expression of progesterone receptor and uteroglobin genes during early pregnancy in the rabbit. Mol Reprod Dev 1993;34:244-249.
21.Wira CR, Sandoe CP. Sex steroid hormone regulation of IgA and IgG in rat uterine secretions. Nature 1977;268:534-536.
22.Díaz-Flores M, Baiza-Gutman LA, Hicks JJ. Los nuevos moduladores endometriales en el embarazo temprano. Gac Med Mex 1996;132:519-528.
23.Perez MM, Luna J, Mena R, Romano MC. Lymphocytes and T lymphocyte subsets are regionally distributed in the female goat reproductive tract: Infl uence of the stage of the oestrous cycle. Res Vet Sci 2002;72:115-121.
24.Kaushic C, Murdin AD, Under down BJ, Wira CR. Chlamidya trachomatis infection in the female reproductive tract of the rat: infl uence of progesterone on infectivity and immune response. Infect Immun 1998;66:893-895.
25.Parr MB, Parr EL. Mucosal immunity in the female and male reproductive tracts. In: Ogra J, Mestecky ME, Lamm W, Strober JR, Mc Ghee J B, editors.Handbook of Mucosal Immunology. New York:Academic Press. 1999:677-689.
26.Lee CS, Gogolin-Ewens K, Brandon MR. Identifi cation of a unique lymphocyte subpopulation in the sheep uterus. Immunology 1998;63:157-164.
27.Watson ED, Thompson RM. Lymphocyte subsets in the endometrium of genitally normal mares and mares suceptible to endometritis. Equine Vet J
28.Segerson E, Matterson P, Gunsett F. Endometrial T lymphocyte subset infi ltration during the ovineestrous cycle and early pregnancy. J Reprod Inmunol 1991;20:221-236.
29.Hussain AM. Bovine uterine defense mechanisms: a review J Vet Med B 1989; 36:641-651.
30.Cobb SP, Watson ED. Immunohistochemical study of immune cell in the bovine endometrium at different stages of oestrous cycle. Res Vet Sci 1995; 59:238-241.
31.Vander-Wielen AL, King GJ. Intraepithelial lymphocytes in the bovine uterus during the oestrous cycle and early pregnancy. J Reprod Fertil 1984;70:457-462.
32.Hussein AM, Newby TJ, Bourne FJ. Immunohisto chemical studies of the local immune system in the reproductive tract of the sow. J Reprod Immunol
33.Lavielle RE, Pérez MM, Hernández GR, Martínez MJJ. Cuantifi cación de células plasmáticas en cuello uterino de cerda, en fase folicular y lútea del ciclo
estral. Vet Méx 1994;25:29-31.
34.Bischof R, Brandon MR, Lee CS. Studies on the distribution of immune cell in the uteri of prepubertal and cyding gilts. J Reprod Inmunol 1994;26:1111-1129.
35.Lander-Chacin MF, Jansen PJ, Drost M. Effects of stage of the oestrus cycle and sterois treatment of uterine immunoglbulin content and polymorpho nuclear leukocytes in cattle. Theriogenology 1990;34:1169-1184.
36.Pérez MM, Mendoza GM, Mena LR, Romano PM.Linfocitos del útero de la cabra: Un estudio histológico e inmunohistoquímico por microscopía confocal. Memorias de la XI Reunión Nacional sobre Caprinocultura; 1996 octubre 16-18; Chapingo, México: octubre 16-18; México: Universidad Autónoma de Chapingo. 1996: 71-76.
37.Howe GR. Leukocytic response to spermatozoa in ligated segments of the rabbit vagina, uterus and oviduct. J Reprod Fertil 1967;13:563-566.
38.Dharmarajan AM, Yoshimura Y, Sueoka K, Atlas SJ, Dubin NH, Ewing- Zirkin BR, et al. Progesterone secretion by corpora lutea of the isolated perfused rabbit ovary during pseudopregnancy. Biol Reprod 1998;381:137-143.
39.Aragona P, Puzzolo D, Micali A, Ferreri G, Britti D. Morphological and Morphometric analysis on the rabbit connective goblet cells in different hormonal
conditions. Exp. Eye Res 1998; 66: 81-88.
40.Aluja, A.S. de. 2002. Consideraciones Éticas en la Experimentación Científi ca con animales y la Norma Oficial NOM-062-Z00-1999: “Especifi caciones técnicas para la producción, cuidado y uso de los animales de laboratorio”. Memorias V Congreso Nacional
Latinoamericano y del Caribe de Bioética, 21-24 de Noviembre 2001. Academia Nacional Mexicana de Bioética, Comisión Nacional de Bioética, México D.F.,México.
41.Aluja, A.S. de. Animales de Laboratorio y la Norma Oficial Mexicana (NOM-062-ZOO-1999). Gaceta Médica de México 2002;138:295-298.
42.Steel SR, Torrie HJ. Bioestadística, principios y procedimientos. Estadísticas no Paramétrica. 2ª ed. México: Mc Graw-Hill, 1988.
43.Hafez ESE. Reproducción e inseminación artificial en animales. 5a ed. México: Interamericana-Mc Graw-Hill; 1989.
44.Challis JRG, Davies IJ, Ryan KJ. The concentration of progesterone , estrone and 17ß estradiol in the plasma of pregnant rabbit. Endocrinology 1974;93:971-976.
45.Szekere-Bartho J, Barakonyi A, Par G, Polgar B,Palkovics T, Szereday L. Progesterone as an immunomodulatory molecule. Int Immunopharmacol 2001;1:1037-1048.
46.Moriyama I, Sugawa T. Progesterone facilitates implantation of xenogenic cultured cells in hamsteruterus. Endocrinology 1972;236:150-152.
47.Kimoto Y. A single human cell expresses all messenger ribonucleic acids: the arrow of time in a cell. Mol Gen Genet 1998;258:233-239.
48.Pasanen S, Ylikomi T, Palojoki E, Syvala H, Pelto-Huikko M, Touhimaa P. Progesterone receptor in chicken bursa of Fabricius and thymus: evidence for expression in
B-lymphocytes. Mol Cell Endocrinol 1998;141:119-128.
49.Szekeres-Bartho J, Reznikoff-Etievant MF, Varga P,Varga Z, Chaouat G. Lymphocytic progesterone receptors in human pregnancy. J Reprod Immunol
50.Szekeres-Bartho J, Szekeres GY, Debre P, Autran B, Chaouat G. Reactivity of lymphocytes to a progesterone receptor-specifi c monoclonal antibody. Cell Immunol 1990;125:273-283.
51.Shen XZ, Tsai MJ, Bullock DW, Woo SLC. Hormonal regulation of rabbit uteroglobin gene transcription.Endocrinology 1983;112:871-876.
52.Beato M, Beier R. Binding of progesterone to the proteins of uterine luminal fl uid. Identificaction of uteroglobins as the binding protein. Biochem Biophys Acta 1975;392:346-356.
53.Miele L. Antifl ammins, bioactive peptides derived from uteroglobin. Ann N Y Acad Sci 2000;923:128-140.
54.Moreno JJ. Antiflammin peptides in the regulation of infl ammatory response. Ann NY Acad Sci 2000;923:147-153.
55.Anzaldua SR, Camacho-Arroyo I, Cerbon MA.Histomorphological changes in the oviduct epithelium of the rabbit during early pregnancy. Anat Histol Embryol 2002;31:308-312.
Hafez ES. Reproducción e inseminación artificial en animales. 6a ed. México: McGraw-Hill-Interamericana,1996.
Alvariño MR. Control de la Reproducción en el conejo. Madrid, España: Mundi-Prensa, 1993.
Lefevre B, Cailloi M. Relationship of oestrous behaviour with follicular growth and sex steroid concentration in the follicular fluid in the domestic rabbit. Ann Biol Anim Bioch Biophys 1978;18:1435-1441.
García XF. Fisiología de la reproducción en la coneja (Capitulo 2). En: Biología de la reproducción en la hembra del conejo doméstico. Universidad Politécnica de Valencia. Valencia, España 1991: 13-25.
Enkhuizen PJM, Van M. Distribution in size and number of ovarian follicles in the pregnant rabbit before and after revulation with hCG. Twelfth annual Conference of Australian Society for Reproductive Biology; 1980; University of New England,1980.
Pla H, Baselga M, García F, Deltoro J. Categorías foliculares asociadas al comportamiento de monta en el conejo de carne: efectos sobre las estructuras uterinas. III Congreso Mundial de Cunicultura; 1984; Roma, Italia: Actas Vol. II 1984: 446-452.
Molina I, Pla M, García F. Poblaciones de folículos en función del comportamiento de monta en conejas: Utilización de un método simple para la medición de los folículos. ITEA 1986; 66: 21-26.
Holt JA. Regulation of progesterone production in the rabbit corpus luteum. Biol Reprod 1989;40:201-208.
Miller JB, Keyes PL. A mechanism for regression of the rabbit corpus luteum: uterine induced loss of luteal responsiveness to 17ß-estradiol. Biol Reprod 1976;15:511-518.
Browning J, Keyes FL, Wolfe R. Comparison of serum progesterone, 20α-dihydroprogesterone and estradiol-17ß in pregnant and pseudo-pregnant rabbit: evidence for post implantation recognition of pregnancy. Biol Reprod 1980;23:1014-1019.
Anzaldúa ASR, Peréz MM, Castro RJI. Variación en los índices de mitosis y apoptosis del epitelio uterino de la coneja durante los días previos a la implantación. Téc Pecu Méx 2001;39:59-68.
Lessey BA, Arnold JT. Paracrine signaling in the endometrium integrins and the establishment of uterine receptivity. J Reprod Immunol 1998;39:105-116.
Yang YQ, Kudolo GB, Harper MJK. Binding of platelet activating factor to oviductal membranes during early pregnancy in the rabbit. J Lipid Med 1992;5:77-96.
Spinks NR, Ryan JP, O¨Neill C. Antagonists of embryo-derived platelet-activating factor act by inhibiting the ability of the mouse embryo to implant. J Reprod Fertil 1990;88:241-248.
Orozco C, Perkins T, Clarke FM. Platelet-activating factor induces the expression of early pregnancy factor in the femalemice. J Reprod Fertil 1986;78:549-555.
Sueoka K, Dharmarajan AM, Myazaki T, Atlas SJ, Wallach EE. Platelet activating factor induced early pregnancy factor activity from the perfused rabbit ovary and oviduct. Am J Obstet Gynecol 1988;159:1580-1584.
Hansen PJ, Skopets B. Temporal relationship between progesterone and uterine lymphocyte-inhibitory activity in ewes. Vet Rec 1992;131:371-372.
Stephenson DJ, Hensen PJ. Induction by progesterone of immunosuppresive activity in utero secretions of ovariectomized ewes. Endocrinology 1999;129:3168-3178.
Bailly A, Atger M, Atger P, Cerbón MA, Alison M, Vu Hai MT, et al. The rabbit uteroglobin gene. Structure and interaction with the progesterone receptor. J Biol Chem 1983;258:10384-10389.
Gutierrez-Sagal R, Perez-Palacios G, Langley E, Pasapera AM, Castro I, Cerbon MA. Endometrial expression of progesterone receptor and uteroglobin genes during early pregnancy in the rabbit. Mol Reprod Dev 1993;34:244-249.
Wira CR, Sandoe CP. Sex steroid hormone regulation of IgA and IgG in rat uterine secretions. Nature 1977;268:534-536.
Díaz-Flores M, Baiza-Gutman LA, Hicks JJ. Los nuevos moduladores endometriales en el embarazo temprano. Gac Med Mex 1996;132:519-528.
Perez MM, Luna J, Mena R, Romano MC. Lymphocytes and T lymphocyte subsets are regionally distributed in the female goat reproductive tract: Influence of the stage of the oestrous cycle. Res Vet Sci 2002;72:115-121.
Kaushic C, Murdin AD, Under down BJ, Wira CR. Chlamidya trachomatis infection in the female reproductive tract of the rat: influence of progesterone on infectivity and immune response. Infect Immun 1998;66:893-895.
Parr MB, Parr EL. Mucosal immunity in the female and male reproductive tracts. In: Ogra J, Mestecky ME, Lamm W, Strober JR, Mc Ghee JB, editors. Handbook of Mucosal Immunology. New York: Academic Press. 1999:677-689.
Lee CS, Gogolin-Ewens K, Brandon MR. Identification of a unique lymphocyte subpopulation in the sheep uterus. Immunology 1998;63:157-164.
Watson ED, Thompson RM. Lymphocyte subsets in the endometrium of genitally normal mares and mares suceptible to endometritis. Equine Vet J 1996;28:106-110.
Segerson E, Matterson P, Gunsett F. Endometrial T lymphocyte subset infiltration during the ovineestrous cycle and early pregnancy. J Reprod Inmunol 1991;20:221-236.
Hussain AM. Bovine uterine defense mechanisms: a review J Vet Med B 1989; 36:641-651.
Cobb SP, Watson ED. Immunohistochemical study of immune cell in the bovine endometrium at different stages of oestrous cycle. Res Vet Sci 1995; 59:238-241.
Vander-Wielen AL, King GJ. Intraepithelial lymphocytes in the bovine uterus during the oestrous cycle and early pregnancy. J Reprod Fertil 1984;70:457-462.
Hussein AM, Newby TJ, Bourne FJ. Immunohisto chemical studies of the local immune system in the reproductive tract of the sow. J Reprod Immunol 1983;5:1-15.
Lavielle RE, Pérez MM, Hernández GR, Martínez MJJ. Cuantificación de células plasmáticas en cuello uterino de cerda, en fase folicular y lútea del ciclo estral. Vet Méx 1994;25:29-31.
Bischof R, Brandon MR, Lee CS. Studies on the distribution of immune cell in the uteri of prepubertal and cyding gilts. J Reprod Inmunol 1994;26:1111-1129.
Lander-Chacin MF, Jansen PJ, Drost M. Effects of stage of the oestrus cycle and sterois treatment of uterine immunoglbulin content and polymorpho nuclear leukocytes in cattle. Theriogenology 1990;34:1169-1184.
Pérez MM, Mendoza GM, Mena LR, Romano PM. Linfocitos del útero de la cabra: Un estudio histológico e inmunohistoquímico por microscopía confocal. Memorias de la XI Reunión Nacional sobre Caprinocultura; 1996 octubre 16-18; Chapingo, México: octubre 16-18; México: Universidad Autónoma de Chapingo. 1996: 71-76.
Howe GR. Leukocytic response to spermatozoa in ligated segments of the rabbit vagina, uterus and oviduct. J Reprod Fertil 1967;13:563-566.
Dharmarajan AM, Yoshimura Y, Sueoka K, Atlas SJ, Dubin NH, Ewing-Zirkin BR, et al. Progesterone secretion by corpora lutea of the isolated perfused rabbit ovary during pseudopregnancy. Biol Reprod 1998;381:137-143.
Aragona P, Puzzolo D, Micali A, Ferreri G, Britti D. Morphological and Morphometric analysis on the rabbit connective goblet cells in different hormonal conditions. Exp. Eye Res 1998; 66: 81-88.
Aluja, A.S. de. 2002. Consideraciones Éticas en la Experimentación Científica con animales y la Norma Oficial NOM-062-Z00-1999: “Especificaciones técnicas para la producción, cuidado y uso de los animales de laboratorio”. Memorias V Congreso Nacional Latinoamericano y del Caribe de Bioética, 21-24 de Noviembre 2001. Academia Nacional Mexicana de Bioética, Comisión Nacional de Bioética, México D.F.,México.
Aluja, A.S. de. Animales de Laboratorio y la Norma Oficial Mexicana (NOM-062-ZOO-1999). Gaceta Médica de México 2002;138:295-298.
Steel SR, Torrie HJ. Bioestadística, principios y procedimientos. Estadísticas no Paramétrica. 2ª ed. México: Mc Graw-Hill, 1988.
Hafez ESE. Reproducción e inseminación artificial en animales. 5a ed. México: Interamericana-Mc Graw-Hill; 1989.
Challis JRG, Davies IJ, Ryan KJ. The concentration of progesterone, estrone and 17ß estradiol in the plasma of pregnant rabbit. Endocrinology 1974;93:971-976.
Szekere-Bartho J, Barakonyi A, Par G, Polgar B, Palkovics T, Szereday L. Progesterone as an immunomodulatory molecule. Int Immunopharmacol 2001;1:1037-1048.
Moriyama I, Sugawa T. Progesterone facilitates implantation of xenogenic cultured cells in hamsteruterus. Endocrinology 1972;236:150-152.
Kimoto Y. A single human cell expresses all messenger ribonucleic acids: the arrow of time in a cell. Mol Gen Genet 1998;258:233-239.
Pasanen S, Ylikomi T, Palojoki E, Syvala H, Pelto-Huikko M, Touhimaa P. Progesterone receptor in chicken bursa of Fabricius and thymus: evidence for expression in B-lymphocytes. Mol Cell Endocrinol 1998;141:119-128.
Szekeres-Bartho J, Reznikoff-Etievant MF, Varga P,Varga Z, Chaouat G. Lymphocytic progesterone receptors in human pregnancy. J Reprod Immunol 1989;16:239-247.
Szekeres-Bartho J, Szekeres GY, Debre P, Autran B, Chaouat G. Reactivity of lymphocytes to a progesterone receptor-specific monoclonal antibody. Cell Immunol 1990;125:273-283.
Shen XZ, Tsai MJ, Bullock DW, Woo SLC. Hormonal regulation of rabbit uteroglobin gene transcription. Endocrinology 1983;112:871-876.
Beato M, Beier R. Binding of progesterone to the proteins of uterine luminal fluid. Identificaction of uteroglobins as the binding protein. Biochem Biophys Acta 1975;392:346-356.
Miele L. Antiflammins, bioactive peptides derived from uteroglobin. Ann NY Acad Sci 2000;923:128-140.
Moreno JJ. Antiflammin peptides in the regulation of inflammatory response. Ann NY Acad Sci 2000;923:147-153.
Anzaldua SR, Camacho-Arroyo I, Cerbon MA. Histomorphological changes in the oviduct epithelium of the rabbit during early pregnancy. Anat Histol Embryol 2002;31:308-312.
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