Endocrine disruption in adolescence: Immunologic, hematologic and bone effects in monkeys

Toxicological Sciences

Volumn 82, Issue 2, 2004, Pages 598-607

  Golub, Mari S ^a   Hogrefe, Casey E ^b   Germann, Stacey L ^a,b   Jerome, Christopher P ^c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c SkeleTech Inc   (United States)

Author keywords

Bone mineral density; Diethylstilbestrol; Endocrine disruption; Female; Flow cytometry; Hematology; Methoxychlor; Puberty; Rhesus monkeys

Indexed keywords

ALBUMIN; AMINOTRANSFERASE; HEMOGLOBIN; LIPID; METHOXYCHLOR;

ALBUMIN BLOOD LEVEL; ANEMIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNE DISEASE; B LYMPHOCYTE; BLOOD CELL COUNT; BONE DISEASE; BONE GROWTH; BONE MASS; CHILD DEVELOPMENT; CONTROLLED STUDY; ENDOCRINE DISEASE; ENVIRONMENTAL EXPOSURE; ESTROGEN ACTIVITY; FEMALE; GENITAL SYSTEM; HEART DISEASE; HEMATOCRIT; HEMATOLOGIC DISEASE; HEMOGLOBIN DETERMINATION; IMMUNOLOGY; INFECTION; LYMPHOCYTE; NONHUMAN; OSTEOPOROSIS; RHESUS MONKEY; RISK ASSESSMENT;

AGING; ANIMALS; BLOOD CELL COUNT; BLOOD CHEMICAL ANALYSIS; BONE AND BONES; DENSITOMETRY, X-RAY; DIETHYLSTILBESTROL; ENDOCRINE SYSTEM DISEASES; ERYTHROCYTE COUNT; ESTROGENS, NON-STEROIDAL; FEMALE; FLOW CYTOMETRY; IMMUNITY; INSECTICIDES; LYMPHOCYTE COUNT; MACACA MULATTA; METHOXYCHLOR; ORGAN SIZE; PUBERTY;

MACACA MULATTA;

EID: 10044258452     PISSN: 10966080     EISSN: None     Source Type: Journal    
DOI: 10.1093/toxsci/kfh295     Document Type: Article

References (48)

1. Beard, J. L. (2000). Iron requirements in adolescent females. J. Nutr. 130, 440S-442S.
2. Bergstrom, E., Hernell, O., Lonnerdal, B., and Perrson, L. A. (1995). Sex differences in iron stores of adolescents: What is normal? J. Pediatr. Gastroenterol. Nutr. 20, 215-224.
3. Bonjour, J. P., Theintz, G., Buchs, B., Sloosman, D., and Rizzoli, R. (1991). Critical years and stages of puberty for spinal and femoral bone mass accumulation during adolescence. J. Clin. Endocrinol. Metab. 73, 555-563.
4. Carter, D. L., Shieh, T. M., Blosser, R. L., Chadwick, K. R., Margolick J. B., Hildreth, J. E., Clements, J. E., and Zink, M. C. (1999). CD56 identifies monocytes and not natural killer cells in rhesus macaques. Cytometry 37, 41-50.
5. Christiansen, C., and Riis, B. J. (1990). Five years with continuous combined oestrogen/progestogen therapy. Effects on calcium metabolism, lipoproteins, and bleeding pattern. Br. J. Obstet. Gynecol. 97, 1087-1092.
6. Cowan, L. D., Wallace, R. B., Barrett-Connor, E., Hunninghake, D., Pomreh, P., Wahl, P., and Heiss, G. (1982). Variations in clinical chemistry measures associated with oral contraceptive and estrogen use. J. Reprod. Med. 27, 275-282.
7. Djeu, J. (1995). Natural killer activity. In Methods in Immunotoxicology (G. Burleson, J. Dean, and A. Munson, Eds.), Vol. 1, pp. 437-449. Wiley-Liss, New York.
8. Erben, R. G., Raith, S., Eberle, J., and Stangassinger, M. (1998). Ovariectomy augments B lymphopoiesis and generation of monocyte-macrophage precursors in rat bone marrow. Am. J. Physiol. 274, E476-E483.
9. Erlandsson, M. C., Jonsson, C. A., Islander, U., OhIsson, C., and Carlsten, H. (2003). Oestrogen receptor specificity in oestradiol-mediated effects on B lymphopoiesis and immunoglobulin production in male mice. Immunology 108, 346-351.
10. Erlandsson, M. C., Jonsson, C. A., Lindberg, M. K., OhIsson, C., and Carlsten, H. (2002). Raloxifene- and estradiol-mediated effects on uterus, bone and B lymphocytes in mice. J. Endocrinol. 175, 319-327.
11. Gaido, K. W., Leonard, L. S., Maness, S. C., Hall, J. M., McDonnell, D. P., Saville, B., and Safe, S. (1999). Differential interaction of the methoxychlor metabolite 2,2-bis-(p hydroxyphenyl)-1,1,1-trichloroethane with estrogen receptors alpha and beta. Endocrinology 140, 5746-5753.
12. Gaido, K. W., Maness, S. C., McDonnell, D. P., Dehal, S. S., Kupfer, D., and Safe, S. (2000). Interaction of methoxychlor and related compounds with estrogen receptor alpha and beta, and androgen receptor: Structure-activity studies. Mol. Pharmacol. 58, 852-858.
13. Giavedoni, L. D., Velasquillo, M. C., Parodi, L. M., Hubbard, G. B., and Hodara, V. L. (2000). Cytokine expression, natural killer cell activation, and phenotypic changes in lymphoid cells from rhesus macaques during acute infection with pathogenic simian immunodeficiency virus. J. Virol. 74, 1648-1657.
14. Gilsanz, V., Roe, T., Mora, S., Costin, C., and Goodman, W. (1991). Changes in vertebral bone density in black girls and white girls during childhood and puberty. New. Engl. J. Med. 325, 1597-1600.
15. Goldman, J. M., Laws, S. C., Balchak, S. K., Cooper, R. L., and Kavlock, R. J. (2000). Endocrine-disrupting chemicals: Prepubertal exposures and effects on sexual maturation and thyroid activity in the female rat. A focus on the EDSTAC recommendations. Crit. Rev. Toxicol. 30, 135-196.
16. Golub, M., Germann, S., and Hogrefe, C. (2004). Endocrine disruption and cognitive function in adolescent female rhesus monkeys. Neurotoxicol. Teratol. 26, 799-809.
17. Golub, M., Hogrefe, C., Germann, S., Lasley, B., Natarajan, K., and Tarantal, A. F. (2003). Effects of exogenous estrogenic agents on pubertal growth and reproductive system maturation in female rhesus monkeys. Toxicol. Sci. 74, 103-113.
18. Gordon, C. L., Halton, J. M., Atkinson, S. A., and Webber, C. E. (1991). The contributions of growth and puberty to peak bone mass. Growth Dev. Aging 55, 157-162.
19. Gray, L. E., Jr. (1998). Tiered screening and testing strategy for xenoestrogens and antiandrogens. Toxicol. Lett. 102-103, 677-680.
20. Gray, L. J., Ostby, J., Ferrell, J., Rehnberg, C., Linder, R., Cooper, R., Goldman, J., Slott, V., and Laskey, J. (1989). A dose-response analysis of metboxychlor-induced alterations of reproductive development and function in the rat. Fundam. Appl. Toxicol. 12, 92-108.
21. Hendrickx, A., Benirschke, K., Thompson, R., Ahern, J., Lucas, W., and Oi, R. (1979). The effects of prenatal diethylstilbestrol (DES) exposure on the genitalia of pubertal Macaca mulatta. I. Female offspring. J. Reprod. Med. 22, 233-240.
22. Jacobsen, C. N., Aasted, B., Broe, M. K., and Petersen, J. L. (1993). Reactivities of 20 anti-human monoclonal antibodies with leucocytes from ten different animal species. Vet. Immunol. Immunopathol. 39, 461-466.
23. Jilka, R. L., Passeri, G., Girasole, G., Cooper, S., Abrams, J., Broxmeyer, H., and Manolagas, S. C. (1995). Estrogen loss upregulates hematopoiesis in the mouse: A mediating role of IL-6. Exp. Hematol. 23, 500-506.
24. Kincade, P. W., Medina, K. L., Payne, K. J., Rossi, M. I., Tudor, K. S., Yamashita, Y., and Kouro, T. (2000). Early B-lymphocyte precursors and their regulation by sex steroids. Immunol. Rev. 175, 128-137.
25. Kivinen, S., and Maenpaa, J. (1990). Effect of toremifene on clinical chemistry, hematology and hormone levels at different doses in healthy postmenopausal volunteers: Phase 1 Study. J. Steroid Biochem. 36, 217-220.
26. Lafont, B. A., Gloeckler, L., D'Hautcourt, J. L., Gut, J. P., and Aubertin, A. M. (2000). One-round determination of seven leukocyte subsets in rhesus macaque blood by flow cytometry. Cytometry 41, 193-202.
27. Lee, W.-W., Nam, K.-H., Terao, K., Adari, H., and Yoshikawa, Y. (2003). Age-related increase of peripheral CD4+ CD8+ double-positive T lymphocytes in cynomolgus monkeys: Longitudinal study in relation to thymic involution. Immunology 109, 217-225.
28. Manolagas, S. C., Bellido, T., and Jilka, R. L. (1995). Sex steroids, cytokines and the bone marrow: New concepts on the pathogenesis of osteoporosis. Ciba Found. Symp. 191, 187-196; discussion 197-202.
29. Marty, M. S., Crissman, J. W., and Carney, E. W. (1999). Evaluation of the EDSTAC female pubertal assay in CD rats using 17beta-estradiol, steroid biosynthesis inhibitors, and a thyroid inhibitor. Toxicol. Sci. 52, 269-277.
30. Monster, T. B., Janssen, W. M., de Jong, P. E., and de Jong-van den Berg, L. T. (2001). Oral contraceptive use and hormone replacement therapy are associated with microalbuminuria. Arch. Intern. Med. 161, 2000-2005.
31. Munn, D. H., Bree, A. G., Beall, A. C., Kaviani, M. D., Sabio, H., Schaub, R. G., Alpaugh, R. K., Weiner, L. M., and Goldman, S. J. (1996). Recombinant human macrophage colony-stimulating factor in nonhuman primates: Selective expansion of a CD16+ monocyte subset with phenotypic similarity to primate natural killer cells. Blood 88, 1215-1224.
32. O'Connor, J. C., Cook, J. C., Marty, M. S., Davis, L. G., Kaplan, A. M., and Carney, E. W. (2002). Evaluation of Tier I screening approaches for detecting endocrine-active compounds (EACs). Crit. Rev. Toxicol. 32, 521-549.
33. Perry, M. J., Samuels, A., Bird, D., and Tobias, J. H. (2000). Effects of high-dose estrogen on murine hematopoietic bone marrow precede those on osteogenesis. Am. J. Physiol. Endocrinol. Metab. 279, E1159-E1165.
34. Polatti, F., Perotti, F., Filippa, N., Gallina, D., and Nappi, R. E. (1995). Bone mass and long-term monophasic oral contraceptive treatment in young women. Contraception 51, 221-224.
35. Rappocciolo, G., Allan, J. S., Eichberg, J. W., and Chanh, T. C. (1992). A comparative study of natural killer cell activity, lymphoproliferation, and cell phenotypes in nonhuman primates. Vet. Pathol. 29, 53-59.
36. Register, T., Jayo, M., and Jerome, C. (1997). Oral contraceptive treatment inhibits the normal acquisition of bone mineral in skeletally immature young adult female monkeys. Osteoporos. Int. 7, 348-353.
37. Reimann, K. A., Waite, B. C., Lee-Parritz, D. E., Lin, W., Uchanska-Ziegler, B., O'Connell, M. J., and Letvin, N. L. (1994). Use of human leukocyte-specific monoclonal antibodies for clinically immunophenotyping lymphocytes of rhesus monkeys. Cytometry 17, 102-108.
38. Rudy, B. J., Wilson, C. M., Durako, S., Moscicki, A.-B., Muenz, L., and Douglas, S. D. (2002). Peripheral blood lymphocyte subsets in adolescents: A longitudinal analysis from the REACH project. Clin. Diagn. Lab. Immunol. 9, 959-965.
39. Schiele, F., Vincent-Viry, M., Fournier, B., Starck, M., and Siest, G. (1998). Biological effects of eleven combined oral contraceptives on serum triglycerides, gamma-glutamyltransferase, alkaline phosphatase, bilirubin and other biochemical variables. Clin. Chem. Lab. Med. 36, 871-878.
40. Slukvin, I. I., Watkins, D. I., and Golos, T. G. (2001). Phenotypic and functional characterization of rhesus monkey decidual lymphocytes: Rhesus decidual large granular lymphocytes express CD56 and have cytolytic activity. J. Reprod. Immunol. 50, 57-79.
41. Sodora, D. L., Douek, D. C., Silvestri, G., Montgomery, L., Rosenzweig, M., Igarashi, T., Bernacky, B., Johnson, R. P., Feinberg, M. B., Martin, M. A., et al. (2000). Quantification of thymic function by measuring T cell receptor excision circles within peripheral blood and lymphoid tissues in monkeys. Eur. J. Immunol. 30, 1145-1153.
42. Soekarjo, D. D., de Pee, S., Bloem, M. W., Tjiong, R., Yip, R., Schreurs, W. H., and Muhilal (2001). Socio-economic status and puberty are the main factors determining anaemia in adolescent girls and boys in East Java, Indonesia. Eur. J. Clin. Nutr. 55, 932-939.
43. Stoker, T. E., Parks, L. G., Gray, L. E., and Cooper, R. L. (2000). Endocrine-disrupting chemicals: Prepubertal exposures and effects on sexual maturation and thyroid function in the male rat. A focus on the EDSTAC recommendations. Endocrine Disrupter Screening and Testing Advisory Committee. Crit. Rev. Toxicol. 30, 197-252.
44. Theintz, G., Buchs, B., Rissoli, R., Slosman, D., Clavien, H., Sizonenko, P. C., and Bonjour, J. P. (1992). Longitudinal monitoring of bone mass accumulation in healthy adolescents: Evidence for a marked reduction after 16 years of age at the levels of lumbar spine and femoral neck in female subjects. J. Clin. Endocrinol. Metab. 75, 1060-1065.
45. Thoman, M. L. (1995). The pattern of T lymphocyte differentiation is altered during thymic involution. Mech. Ageing. Dev. 82, 155-170.
46. Utsuyama, M., Kanno, J., Inoue, T., and Hirokawa, K. (2002). Age/sex dependent and non-monotonous dose-response effect of diethylstilbestrol on the immune functions in mice. Toxicol. Lett. 135, 145-153.
47. Walden, C. E., Knopp, R. H., Johnson, J. L., Heiss, G., Wahl, P. W., and Hoover, J. J. (1986). Effect of estrogen/progestin potency on clinical chemistry measures. Am. J. Epidem. 123, 517-531.
48. Waters, K. M., Safe, S., and Gaido, K. W. (2001). Differential gene expression in response to methoxychlor and estradiol through ERalpha, ERbeta, and AR in reproductive tissues of female mice. Toxicol. Sci. 63, 47-56.