Morphological relationships and leukocyte influence on steroid production in the epigonal organ-ovary complex of the skate, Leucoraja erinacea

Journal of Morphology

Volumn 269, Issue 5, 2008, Pages 620-629

  Lutton, B V ^a   Callard, I P ^b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b Boston University   (United States)

Author keywords

Elasmobranch; Immunology; Reproduction

Indexed keywords

ELASMOBRANCHII; LEUCORAJA ERINACEA;

ESTROGEN; TESTOSTERONE;

ANIMAL; ARTICLE; CAPILLARY; CELL CULTURE; COCULTURE; CULTURE MEDIUM; CYTOLOGY; ELECTRIC FISH; FEMALE; HISTOLOGY; IMMUNOLOGY; LEUKOCYTE; METABOLISM; OVARY FOLLICLE; VASCULARIZATION;

ANIMALS; CAPILLARIES; CELLS, CULTURED; COCULTURE TECHNIQUES; CULTURE MEDIA, CONDITIONED; ESTROGENS; FEMALE; LEUKOCYTES; OVARIAN FOLLICLE; SKATES (FISH); TESTOSTERONE;

EID: 47949105387     PISSN: 03622525     EISSN: 10974687     Source Type: Journal    
DOI: 10.1002/jmor.10614     Document Type: Article

References (61)

1. Adashi EY. 1992. The potential relevance of cytokines to ovarian physiology. J Steroid Biochem Mol Biol 43:439-444.
2. Andreuccetti P, Iodice M, Prisco M, Gualtieri R. 1999. Intercellular bridges between granulosa cells and the oocyte in the elasmobranch, Raya asterias. Anat Rec 255:180-187.
3. Arnold JE. 2005. Hematology of the sandbar shark, Carcharhinus plumbeus: Standardization of complete blood count techniques for elasmobranchs. Vet Clin Pathol 34:115-123.
4. Barua A, Yoshimura Y. 1999. Effects of aging and sex steroids on the localization of T cell subsets in the ovary of chicken, Gallus domesticus. Gen Comp Endocrinol 114:28-35.
5. Benten WP, Stephan C, Wunderlich F. 2002. B cells express intracellular but not surface receptors for testosterone and estradiol. Steroids 67:647-654.
6. Bird S, Zou J, Wang T, Munday B, Cunningham C, Secombes CJ. 2002. Evolution of interleukin-1β. Cytokine Growth Factor Rev 13:483-502.
7. Bourguiba S, Chater S, Delalande C, Benahmed M, Carreau S. 2003. Regulation of aromatase gene expression in purified germ cells of adult male rats: Effects of transforming growth factor β, tumor necrosis factor α, and cyclic adenosine 37prime;,5′-monosphosphate. Biol Reprod 69:592-601.
8. Brannstrom M, Mayrhofer G, Robertson SA. 1993. Localization of leukocyte subsets in the rat ovary during the periovulatory period. Biol Reprod 48:277-286.
9. Breucker H. 1978. Macrophages, a normal component in seasonally involuting testes of the swan, Cygnus olor. Cell Tissue Res 193:463-471.
10. Brozman M, Jakubovsky J. 1989. The red pulp of the human spleen. Structural basis of blood filtration. Z Mikrosk Anat Forsch 103:316-328.
11. Bukulmez O, Arici A. 2000. Leukocytes in ovarian function. Hum Reprod Update 6:1-15.
12. Castro A, Castro O, Troncoso JL, Kohen P, Simon C, Vega M, Devoto L. 1998. Luteal leukocytes are modulators of the steroidogenic process of human mid-luteal cells. Hum Reprod 13:1584-1589.
13. Darbon JM, Oury F, Laredo J, Bayard F. 1989. Tumor necrosis factor-α inhibits follicle-stimulating hormone-induced differentiation in cultured rat granulosa cells. Biochem Biophys Res Commun 163:1038-1046.
14. Dooley H, Flajnik MF. 2005. Shark immunity bites back: Affinity maturation and memory response in the nurse shark, Ginglymostoma cirratum. Eur J Immunol 35:936-945.
15. Emoto N, Baird A. 1988. The effect of tumor necrosis factor/cachectin on follicle-stimulating hormone-induced aromatase activity in cultured rat granulosa cells. Biochem Biophys Res Commun 153:792-798.
16. Engel KB. 2008. The regulation and toxicology of spermatogenesis. Boston University: Boston, MA. pp. 421.
17. Fange R, Pulsford A. 1983. Structural studies on lymphomyeloid tissues of the dogfish, Scyliorhinus canicula L. Cell Tissue Res 230:337-351.
18. Ghersevich S, Isomaa V, Vihko P. 2001. Cytokine regulation of the expression of estrogenic biosynthetic enzymes in cultured rat granulosa cells. Mol Cell Endocrinol 172:21-30.
19. Ghiara G, Taddei C. 1966. Cytological and ultrastructural data on a special type of basophil constituents of the cytoplasm of follicular cells and ovarian ovocytes of reptiles. Boll Soc Ital Biol Sper 42:784-788.
20. Gottschall PE, Uehara A, Hoffmann ST, Arimura A. 1987. Interleukin-1 inhibits follicle stimulating hormone-induced differentiation in rat granulosa cells in vitro. Biochem Biophys Res Commun 149:502-509.
21. Greve JW, Gouma DJ, Buurman WA. 1989. Bile acids inhibit endotoxin-induced release of tumor necrosis factor by monocytes: An in vitro study. Hepatol 10:454-458.
22. Hales KH, Diemer T, Ginde S, Shankar BK, Roberts M, Bosmann HB, Hales DB. 2000. Diametric effects of bacterial endotoxin lipopolysaccharide on adrenal and Leydig cell steroidogenic acute regulatory protein. Endocrinol 141:4000-4012.
23. Hamlett WC, Jezior M, Spieler R. 1999. Ultrastructural analysis of folliculogenesis in the ovary of the yellow spotted stingray, Urolophus jamaicensis. Ann Anat 181:159-172.
24. Hurwitz A, Hernandez ER, Payne DW, Dharmarajan AM, Adashi EY. 1992. Interleukin-1 is both morphogenic and cytotoxic to cultured rat ovarian cells: Obligatory role for heterologous, contact-independent cell-cell interaction. Endocrinol 131:1643-1649.
25. Kasson BG, Gorospe WC. 1989. Effects of interleukins 1, 2, and 3 on follicle stimulating hormone-induced differentiation of granulosa cells. Mol Cell Endocrinol 62:103-111.
26. Koehler KF, Helguero LA, Haldosen LA, Warner M, Gustafsson JA. 2005. Reflections on the discovery and significance of estrogen receptor β. Endocr Rev 26:465-478.
27. Koob TJ, Callard IP. 1999. Reproductive endocrinology of female elasmobranchs: Lessons from the little skate (Raja erinacea) and spiny dogfish (Squalus acanthias). J Exp Zool 284:557-574.
28. Lamote I, Meyer E, De Ketelaere A, Duchateau L, Burvenich C. 2006. Expression of the estrogen receptor in blood neutrophils of dairy cows during the periparturient period. Theriogenology 65:1082-1098.
29. Lisby S, Hauser C. 2002. Transcriptional regulation of tumor necrosis factor-α in keratinocytes mediated by interleukin-1β and tumor necrosis factor-α. Exp Dermatol 11:592-598.
30. Lister A, Van Der Kraak G. 2002. Modulation of goldfish testicular testosterone production in vitro by tumor necrosis factor α, interleukin-1β, and macrophage conditioned media. J Exp Zool 292:477-486.
31. Lutton BV, Callard IP. 2006. Evolution of reproductive-immune interactions. Int Comp Biol 46:1060-1069.
32. Lutton BV, Callard IP. 2007. Effects of reproductive activity and sex hormones on apoptosis in the epigonal organ of the skate (Leucoraja erinacea). Gen Comp Endocrinol 154:75-84.
33. Lutton BV, Callard IP. 2008. Influence of reproductive activity, sex steroids, and seasonality on epigonal organ cellular proliferation in the skate (Leucoraja erinacea). Gen Comp Endocrinol 155:116-125.
34. Macdiarmid F, Wang D, Duncan LJ, Purohit A, Ghilchick MW, Reed MJ. 1994. Stimulation of aromatase activity in breast fibroblasts by tumor necrosis factor α. Mol Cell Endocrinol 106:17-21.
35. Marcinkiewicz JL, Krishna A, Cheung CM, Terranova PF. 1994. Oocytic tumor necrosis factor α: Localization in the neonatal ovary and throughout follicular development in the adult rat. Biol Reprod 50:1251-1260.
36. Maxwell MH. 1985. Heterophilic leucocytes are the predominant granulocytes in the ovary and ultimobranchial glands of the adult fowl. Res Vet Sci 39:119-121.
37. Miracle AL, Anderson MK, Litman RT, Walsh CJ, Luer CA, Rothenberg EV, Litman GW. 2001. Complex expression patterns of lymphocyte-specific genes during the development of cartilaginous fish implicate unique lymphoid tissues in generating an immune repertoire. Int Immunol 13:567-580.
38. Pacifici R, Rifas L, McCracken R, Vered I, McMurtry C, Avioli LV, Peck WA. 1989. Ovarian steroid treatment blocks a postmenopausal increase in blood monocyte interleukin 1 release. Proc Natl Acad Sci USA 86:2398-2402.
39. Pasanen S, Ylikomi T, Palojoki E, Syvala H, Pelto-Huikko M, Tuohimaa P. 1998. Progesterone receptor in chicken bursa of Fabricius and thymus: Evidence for expression in B-lymphocytes. Mol Cell Endocrinol 141:119-128.
40. Patino R, Xia Z, Gale WL, Wu C, Maule AG, Chang X. 2000. Novel transcripts of the estrogen receptor α gene in channel catfish. Gen Comp Endocrinol 120:314-325.
41. Piferrer FC, Callard GV. 1995. Inhibition of deoxyribonucleic acid synthesis during premeiotic stages of spermatogenesis by a factor from testis-associated lymphomyeloid tissue in the dogfish shark (Squalus acanthias). Biol Reprod 53:390-398.
42. Pioli PA, Weaver LK, Schaefer TM, Wright JA, Wira CR, Guyre PM. 2006. Lipopolysaccharide-induced IL-1 β production by human uterine macrophages up-regulates uterine epithelial cell expression of human β-defensin 2. J Immunol 176:6647-6655.
43. Pitzel L, Jarry H, Wuttke W. 1993. Effects and interactions of prostaglandin F2 α, oxytocin, and cytokines on steroidogenesis of porcine luteal cells. Endocrinol 132:751-756.
44. Polan ML, Loukides J, Nelson P, Carding S, Diamond M, Walsh A, Bottomly K. 1989. Progesterone and estradiol modulate interleukin-1 β messenger ribonucleic acid levels in cultured human peripheral monocytes. J Clin Endocrinol Metab 69:1200-1206.
45. Presnell JK, Schreibman MP. 1997. Humason's Animal Tissue Techniques. Baltimore: Johns Hopkins Press. 572 p.
46. Prisco M, Romano M, Ricchiari L, Limatola E, Andreuccetti P. 2002. An ultrastructural study on the vitellogenesis in the spotted ray, Torpedo marmorata. Gen Comp Endocrinol 128:171-179.
47. Purohit A, Singh A, Ghilchik MW, Reed MJ. 1999. Inhibition of tumor necrosis factor α-stimulated aromatase activity by microtubule-stabilizing agents, paclitaxel and 2-methoxyestradiol. Biochem Biophys Res Commun 261:214-217.
48. Rivier C, Vale W. 1989. In the rat, interleukin-1 α acts at the level of the brain and the gonads to interfere with gonadotropin and sex steroid secretion. Endocrinology 124:2105-2109.
49. Roby KF, Terranova PF. 1988. Tumor necrosis factor α alters follicular steroidogenesis in vitro. Endocrinology 123:2952-2964.
50. Sancho-Tello M, Perez-Roger I, Imakawa K, Tilzer L, Terranova PF. 1992. Expression of tumor necrosis factor-α in the rat ovary. Endocrinology 130:1359-1364.
51. Sar M, Lubahn DB, French FS, Wilson EM. 1990. Immunohistochemical localization of the androgen receptor in rat and human tissues. Endocrinology 127:3180-3186.
52. Singh A, Purohit A, Duncan LJ, Mokbel K, Ghilchik MW, Reed MJ. 1997. Control of aromatase activity in breast tumours: The role of the immune system. J Steroid Biochem Mol Biol 61:185-192.
53. Slater CH, Schreck CB. 1993. Testosterone alters the immune response of chinook salmon, Oncorhynchus tshawytscha. Gen Comp Endocrinol 89:291-298.
54. Spicer LJ, Alpizar E. 1994. Effects of cytokines on FSH-induced estradiol production by bovine granulosa cells in vitro: Dependence on size of follicle. Domest Anim Endocrinol 11:25-34.
55. Sullivan WP, Smith DF, Beito TG, Krco CJ, Toft DO. 1988. Hormone-dependent processing of the avian progesterone receptor. J Cell Biochem 36:103-119.
56. Turnbull AV, Rivier C. 1997. Inhibition of gonadotropin-induced testosterone secretion by the intracerebroventricular injection of interleukin-1 β in the male rat. Endocrinol 138:1008-1013.
57. Verburg-van Kemenade BML, Engelsma MY, Huising MO, Kwang J, Muiswinkel WB van, Saeij JPJ, Metz JR. 2001. Crosstalk between the neuro-endocrine and immune system in teleosts. In: Goos HJTh, Rastogi RK, Vaudry H, Pierantoni R, editors. Perspective in Comparative Endocrinology: Unity and Diversity. Monduzzi editore 14th International Congress of Comparative Endocrinology. pp 359-367.
58. Veldhuis JD, Garmey JC, Urban RJ, Demers LM, Aggarwal BB. 1991. Ovarian actions of tumor necrosis factor-α (TNF α): Pleiotropic effects of TNF α on differentiated functions of untransformed swine granulosa cells. Endocrinol 129:641-648.
59. Withanage GS, Sasai K, Fukata T, Miyamoto T, Lillehoj HS, Baba E. 2003. Increased lymphocyte subpopulations and macrophages in the ovaries and oviducts of laying hens infected with Salmonella enterica serovar Enteritidis. Avian Pathol 32:583-590.
60. Zapata AG. 1981. Ultrastructure of elasmobranch lymphoid tissue. II. Leydig's and epigonal organs. Dev Comp Immunol 5:43-52.
61. Zapata AG, Amemiya CT. 2000. Phylogeny of lower vertebrates and their immunological structures. Curr Top Microbiol Immunol 248:67-107.