Alterations in the phenotype and function of immune cells in ovariectomy-induced osteopenic mice

Human Reproduction

Volumn 21, Issue 4, 2006, Pages 880-887

  García Pérez, Miguel A ^a   Noguera, I ^b   Hermenegildo, C ^a,b   Martinez Romero A ^b   Tarin J J ^b   Cano, A ^b  

^a HOSPITAL CLÍNICO UNIVERSITARIO   (Spain)

^b UNIVERSITY OF VALENCIA   (Spain)

Author keywords

Bone metabolism; Estrogen deficiency; Immune system; Mouse; Ovariectomy

Indexed keywords

ALKALINE PHOSPHATASE BONE ISOENZYME; CD11B ANTIGEN; CD19 ANTIGEN; CD3 ANTIGEN; CD4 ANTIGEN; CD51 ANTIGEN; CD61 ANTIGEN; CD8 ANTIGEN; ESTROGEN; GAMMA INTERFERON; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 6; OSTEOCLAST DIFFERENTIATION FACTOR; TRANSCRIPTION FACTOR RUNX1;

ALKALINE PHOSPHATASE BLOOD LEVEL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; B LYMPHOCYTE; BONE DEVELOPMENT; BONE MARROW; BONE TURNOVER; CELL FUNCTION; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVITY; ESTROGEN DEFICIENCY; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION; IMMUNE SYSTEM; IMMUNOCOMPETENT CELL; MOUSE; NONHUMAN; OSTEOCLAST; OSTEOPENIA; OVARIECTOMY; PHENOTYPIC VARIATION; PROTEIN BLOOD LEVEL; SPLEEN; T LYMPHOCYTE;

ANIMALIA;

EID: 33645292570     PISSN: 02681161     EISSN: 14602350     Source Type: Journal    
DOI: 10.1093/humrep/dei413     Document Type: Article

References (49)

1. Aloisi AM, Muscettola M and Lupo C (2001) Effects of gonadectomy and pain on interferon-gamma production in splenocytes of male and female rats. Brain Behav Immun 15,266-272.
2. Anderson DM, Maraskovsky E, Billingsley WL, Dougall WC, Tometsko ME, Roux ER, Teepe MC, DuBose RF, Cosman D and Galibert L (1997) A homologue of the TNF receptor and its ligand enhance T-cell growth and dendritic-cell function. Nature 390,175-179.
3. Arron JR and Choi Y (2000) Bone versus immune system. Nature 408,535-536.
4. Barr IG, Khalid BA, Pearce P, Toh BH, Bartlett PF, Scollay RG and Funder JW (1982) Dihydrotestosterone and estradiol deplete corticosensitive thymocytes lacking in receptors for these hormones. J Immunol 128,2825-2828.
5. Bellido T, Girasole G, Passeri G, Yu XP, Mocharla H, Jilka RL, Notides A and Manolagas SC (1993) Demonstration of estrogen and vitamin D receptors in bone marrow-derived stromal cells: Up-regulation of the estrogen receptor by 1,25-dihydroxyvitamin-D3. Endocrinology 133,553-562.
6. Bonnelye E, Kung V, Laplace C, Galson DL and Aubin JE (2002) Estrogen receptor-related receptor alpha impinges on the estrogen axis in bone: potential function in osteoporosis. Endocrinology 143,3658-3670.
7. Cenci S, Weitzmann MN, Roggia C, Namba N, Novack D, Woodring J and Pacifici R (2000) Estrogen deficiency induces bone loss by enhancing T-cell production of TNF-alpha. J Clin Invest 106,1229-1237.
8. Cenci S, Toraldo G, Weitzmann MN, Roggia C, Gao Y, Qian WP, Sierra O and Pacifici R (2003) Estrogen deficiency induces bone loss by increasing T cell proliferation and lifespan through IFN-gamma-induced class II transactivator. Proc Natl Acad Sci USA 100,10405-10410.
9. Dao MA, Hannum CH, Kohn DB and Nolta JA (1997) FLT3 ligand preserves the ability of human CD34+ progenitors to sustain long-term hematopoiesis in immune-deficient mice after ex vivo retroviral-mediated transduction. Blood 89,446-456.
10. Eghbali-Fatourechi G, Khosla S, Sanyal A, Boyle WJ, Lacey DL and Riggs BL (2003) Role of RANK ligand in mediating increased bone resorption in early postmenopausal women. J Clin Invest 111,1221-1230.
11. Erben RG, Harti G and Graf H (1998a) Ovariectomy does not alter CD4+/ CD8+ ratio in peripheral blood T-lymphocytes in the rat. Horm Metab Res 30,50-54.
12. Erben RG, Raith S, Eberle J and Stangassinger M (1998b) Ovariectomy augments B lymphopoiesis and generation of monocyte-macrophage precursors in rat bone marrow. Am J Physiol 274,E476-E483.
13. Gevers EF, Loveridge N and Robinson IC (2002) Bone marrow adipocytes: A neglected target tissue for growth hormone. Endocrinology 143,4065-4073.
14. Gowen M and Mundy GR (1986) Actions of recombinant interleukin 1, interleukin 2, and interferon-gamma on bone resorption in vitro. J Immunol 136,2478-2482.
15. Igarashi H, Kouro T, Yokota T, Comp PC and Kincade PW (2001) Age and stage dependency of estrogen receptor expression by lymphocyte precursors. Proc Natl Acad Sci USA 98,15131-15136.
16. Jilka RL (1998) Cytokines, bone remodeling, and estrogen deficiency: A 1998 update. Bone 23,75-81.
17. Jilka RL, Takahashi K, Munshi M, Williams DC, Roberson PK and Manolagas SC (1998) Loss of estrogen upregulates osteoblastogenesis in the murine bone marrow. Evidence for autonomy from factors released during bone resorption. J Clin Invest 101,1942-1950.
18. Josien R, Wong BR, Li HL, Steinman RM and Choi Y (1999) TRANCE, a TNF family member, is differentially expressed on T cell subsets and induces cytokine production in dendritic cells. J Immunol 162,2562-2568.
19. Karpuzoglu-Sahin E, Hissong BD and Ansar AS (2001) Interferon-gamma levels are upregulated by 17-beta-estradiol and diethylstilbestrol. J Reprod Immunol 52,113-127.
20. Key LL Jr, Rodriguiz RM, Willi SM, Wright NM, Hatcher HC, Eyre DR, Cure JK, Griffin PP and Ries WL (1995) Long-term treatment of osteopetrosis with recombinant human interferon gamma. N Engl J Med 332,1594-1599.
21. Kimble RB, Matayoshi AB, Vannice JL, Kung VT, Williams C and Pacifici R (1995) Simultaneous block of interleukin-1 and tumor necrosis factor is required to completely prevent bone loss in the early postovariectomy period. Endocrinology 136,3054-3061.
22. Komi J and Lassila O (2000) Nonsteroidal anti-estrogens inhibit the functional differentiation of human monocyte-derived dendritic cells. Blood 95,2875-2882.
23. Kong YY, Feige U, Sarosi I et al. (1999) Activated T cells regulate bone loss and joint destruction in adjuvant arthritis through osteoprotegerin ligand. Nature 402,304-309.
24. Kumru S, Godekmerdan A and Yilmaz B (2004) Immune effects of surgical menopause and estrogen replacement therapy in peri-menopausal women. J Reprod Immunol 63,31-38.
25. Lacey DL, Timms E, Tan HL et al. (1998) Osteoprotegerin ligand is a cytokine that regulates osteoclast differentiation and activation. Cell 93,165-176.
26. Lau KH, Onishi T, Wergedal JE, Singer FR and Baylink DJ (1987) Characterization and assay of tartrate-resistant acid phosphatase activity in serum: Potential use to assess bone resorption. Clin Chem 33,458-462.
27. Lee SW, Kwak HB, Chung WJ, Cheong H, Kim HH and Lee ZH (2003) Participation of protein kinase C beta in osteoclast differentiation and function. Bone 32,217-227.
28. Maret A, Coudert JD, Garidou L et al. (2003) Estradiol enhances primary antigen-specific CD4 T cell responses and Th1 development in vivo. Essential role of estrogen receptor alpha expression in hematopoietic cells. Eur J Immunol 33,512-521.
29. Masuzawa T, Miyaura C, Onoe Y, Kusano K, Ohta H, Nozawa S and Suda T (1994) Estrogen deficiency stimulates B lymphopoiesis in mouse bone marrow. J Clin Invest 94,1090-1097.
30. Minisola S, Pacitti MT, Ombricolo E, Costa G, Scarda A, Palombo E and Rosso R (1998) Bone turnover and its relationship with bone mineral density in pre- and postmenopausal women with or without fractures. Maturitas 29,265-270.
31. Miyaura C, Onoe Y, Inada M, Maki K, Ikuta K, Ito M and Suda T (1997) Increased B-lymphopoiesis by interleukin 7 induces bone loss in mice with intact ovarian function: Similarity to estrogen deficiency. Proc Natl Acad Sci USA 94,9360-9365.
32. Miyazaki T, Matsunaga T, Miyazaki S, Hokari S and Komoda T (2004) Changes in receptor activator of nuclear factor-kappaB, and its ligand, osteoprotegerin, bone-type alkaline phosphatase, and tartrate-resistant acid phosphatase in ovariectomized rats. J Cell Biochem 93,503-512.
33. Olsen NJ and Kovacs WJ (1996) Gonadal steroids and immunity. Endocr Rev 17,369-384.
34. Pei W, Bellows CG, Elsubeihi ES and Heersche JN (2003) Effect of ovariectomy on dexamethasone- and progesterone-dependent osteoprogenitors in vertebral and femoral rat bone cell populations. Bone 33,822-830.
35. Richman C, Kutilek S, Miyakoshi N, Srivastava AK, Beamer WG, Donahue LR, Rosen CJ, Wergedal JE, Baylink DJ and Mohan S (2001) Postnatal and pubertal skeletal changes contribute predominantly to the differences in peak bone density between C3H/HeJ and C57BL/6J mice. J Bone Miner Res 16,386-397.
36. Riggs BL, Khosla S and Melton LJ III (1998) A unitary model for involutional osteoporosis: Estrogen deficiency causes both type I and type II osteoporosis in postmenopausal women and contributes to bone loss in aging men. J Bone Miner Res 13,763-773.
37. Roggia C, Gao Y, Cenci S, Weitzmann MN, Toraldo G, Isaia G and Pacifici R (2001) Up-regulation of TNF-producing T cells in the bone marrow: A key mechanism by which estrogen deficiency induces bone loss in vivo. Proc Natl Acad Sci USA 98,13960-13965.
38. Safadi FF, Dissanayake IR, Goodman GG, Jago RA, Baker AE, Bowman AR, Sass DA, Popoff SN and Epstein S (2000) Influence of estrogen deficiency and replacement on T-cell populations in rat lymphoid tissues and organs. Endocrine 12,81-88.
39. Sakakura Y, Shide N, Tsuruga E, Irie K and Yajima T (2001) Effects of running exercise on the mandible and tibia of ovariectomized rats. J Bone Miner Metab 19,159-167.
40. Sato T, Shibata T, Ikeda K and Watanabe K (2001) Generation of bone-resorbing osteoclasts from B220+ cells: Its role in accelerated osteoclastogenesis due to estrogen deficiency. J Bone Miner Res 16,2215-2221.
41. Sun D, Krishnan A, Zaman K, Lawrence R, Bhattacharya A and Fernandes G (2003) Dietary n-3 fatty acids decrease osteoclastogenesis and loss of bone mass in ovariectomized mice. J Bone Miner Res 18,1206-1216.
42. Takahashi M, Kushida K, Hoshino H, Miura M, Ohishi T and Inoue T (1997) Comparison of bone and total alkaline phosphatase activity on bone turnover during menopause and in patients with established osteoporosis. Clin Endocrinol (Oxf) 47,177-183.
43. Takayanagi H, Ogasawara K, Hida S et al. (2000) T-cell-mediated regulation of osteoclastogenesis by signalling cross-talk between RANKL and IFN-gamma. Nature 408,600-605.
44. Tanizawa T, Yamaguchi A, Uchiyama Y et al. (2000) Reduction in bone formation and elevated bone resorption in ovariectomized rats with special reference to acute inflammation. Bone 26,43-53.
45. Teitelbaum SL (2004) Postmenopausal osteoporosis, T cells, and immune dysfunction. Proc Natl Acad Sci USA 101,16711-16712.
46. Teng YT, Nguyen H, Gao X, Kong YY, Gorczynski RM, Singh B, Ellen RP and Penninger JM (2000) Functional human T-cell immunity and osteoprotegerin ligand control alveolar bone destruction in periodontal infection. J Clin Invest 106,R59-R67.
47. Theill LE, Boyle WJ and Penninger JM (2002) RANK-L and RANK: T cells, bone loss, and mammalian evolution. Annu Rev Immunol 20,795-823.
48. Weaver CM, Peacock M, Martin BR, McCabe GP, Zhao J, Smith DL and Wastney ME (1997) Quantification of biochemical markers of bone turnover by kinetic measures of bone formation and resorption in young healthy females. J Bone Miner Res 12,1714-1720.
49. Yang JH, Chen CD, Wu MY, Chao KH, Yang YS and Ho HN (2000) Hormone replacement therapy reverses the decrease in natural killer cytotoxicity but does not reverse the decreases in the T-cell subpopulation or interferon-gamma production in postmenopausal women. Fertil Steril 74,261-267.