Effects of Insulin-Like Growth Factor Administration and Bone Marrow Transplantation on Thymopoiesis in Aged Mice 1
Abstract
There has been considerable interest in using hormone replacement therapy to rejuvenate the involuted thymus during aging. GH and insulin-like growth factor-I (IGF-I), a mediator of GH actions, have been of particular interest because of their thymopoietic effects and the fact that their serum concentrations decline during aging. However, treatment of aging rodents with either GH or IGF-I does not restore thymus cellularity to levels present in young animals, suggesting that additional defects might limit the magnitude of their effects. In particular, deficiencies have been reported to accumulate in the bone marrow T cell precursor compartment during aging. In view of this, 18-month-old mice were administered either recombinant IGF-I, bone marrow cells from young mice, or a combination of IGF-I and young bone marrow cells. Thymus cellularity in the latter group of mice was significantly higher than in animals treated with hormone or bone marrow transplantation alone, suggesting that optimal therapies for restoring thymus cellularity must address both endocrine and hematopoietic defects that accumulate during aging. Results from in vitro studies using fetal thymic organ cultures suggest that IGF-I acts by potentiating thymic colonization by bone marrow T cell precursors and/or that the hormone affects some other event soon after thymus colonization.
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Thymus size is increased in old mice given either growth hormone or IGF-1.
“numerous studies (42) have shown that thymus size is increased in old mice administered either hormone (101, 103).”
From Causes, consequences, and reversal of immune system aging (2013) · cites this paper as [101]
Growth hormone and IGF-1 bind to receptors expressed on thymocytes and thymic epithelial cells.
“GH and IGF-1 bind to receptors expressed on thymocytes (101) and thymic epithelial cells (102)”
From Causes, consequences, and reversal of immune system aging (2013) · cites this paper as [101]
Cites
The aging immune system: primer and prospectus
Miller, R. A. (1996) · Science · doi:10.1126/science.273.5271.70 · Cited by 1,165 · see citing works
Prolactin and Growth Hormone in the Regulation of the Immune System
Gala, R. R. (1991) · Experimental Biology and Medicine · doi:10.3181/00379727-198-43286b · Cited by 318 · see citing works
Clark, R. (1997) · Endocrine Reviews · doi:10.1210/edrv.18.2.0296 · Cited by 314 · see citing works
Self-citationGH3 pituitary adenoma cells can reverse thymic aging in rats.
Kelley, K. W., Brief, S., Westly, H. J., NOVAKOFSKI, J. E., Bechtel, P. J., Simon, J. R., & Walker, E. (1986) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.83.15.5663 · Cited by 279 · see citing works
Insulin-like growth factor-1 stimulation of lymphopoiesis.
CLARK, R. G., Strasser, J. E., McCabe, S., Robbins, K., & Jardieu, P. M. (1993) · Journal of Clinical Investigation · doi:10.1172/jci116621 · Cited by 171 · see citing works
Self-citationAspinall, R. (1997) · The Journal of Immunology · doi:10.4049/jimmunol.158.7.3037 · Cited by 163 · see citing works
Donskoy, E., & Goldschneider, I. (1992) · The Journal of Immunology · doi:10.4049/jimmunol.148.6.1604 · Cited by 162 · see citing works
Differential effects of growth hormone and prolactin on murine T cell development and function.
Murphy, W. J., Durum, S. K., & Longo, D. (1993) · The Journal of Experimental Medicine · doi:10.1084/jem.178.1.231 · Cited by 132 · see citing works
Murphy, W. J., Durum, S. K., & Longo, D. (1992) · The Journal of Immunology · doi:10.4049/jimmunol.149.12.3851 · Cited by 127 · see citing works
Age-Related Decrease in Mouse T Cell Progenitors
Tyan, M. L. (1977) · The Journal of Immunology · doi:10.4049/jimmunol.118.3.846 · Cited by 113 · see citing works
Repopulation of the atrophied thymus in diabetic rats by insulin-like growth factor I.
Binz, K., Joller, P. W., Froesch, P., Binz, H., Zapf, J., & Froesch, E. R. (1990) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.87.10.3690 · Cited by 106 · see citing works
CLARK, R. G. (1997) · Endocrine Reviews · doi:10.1210/er.18.2.157 · Cited by 104 · see citing works
Self-citationThymic stem cells in mouse bone marrow
Antica, M., Wu, L., Shortman, K., & Scollay, R. G. (1994) · Blood · doi:10.1182/blood.v84.1.111.111 · Cited by 104 · see citing works
Jardieu, P. M., CLARK, R. G., Mortensen, D. L., & Dorshkind, K. A. (1994) · The Journal of Immunology · doi:10.4049/jimmunol.152.9.4320 · Cited by 100 · see citing works
Self-citationTwo rare populations of mouse Thy-1lo bone marrow cells repopulate the thymus.
Spangrude, G. J., Müller‐Sieburg, C. E., Heimfeld, S., & Weissman, I. L. (1988) · The Journal of Experimental Medicine · doi:10.1084/jem.167.5.1671 · Cited by 92 · see citing works
Murphy, W. J., Durum, S. K., & Longo, D. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.10.4481 · Cited by 92 · see citing works
Effects of growth hormone and prolactin immune development and function
Murphy, W. J., Rui, H., & Longo, D. L. (1995) · Life Sciences · doi:10.1016/0024-3205(95)00237-z · Cited by 90 · see citing works
In vivo effects of growth hormone on thymus function in aging mice
Goya, R. G., Gagnerault, M. C., Leite‐de‐Moraes, M., Savino, W., & Dardenne, M. (1992) · Brain Behavior and Immunity · doi:10.1016/0889-1591(92)90033-k · Cited by 90 · see citing works
Pituitary hormones modulate cell–cell interactions between thymocytes and thymic epithelial cells
Coelho, V. D. M., Villa‐Verde, D. M. S., Dardenne, M., & Savino, W. (1997) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(97)00031-3 · Cited by 85 · see citing works
Insulin-like growth factors and their binding proteins
Rutanen, E., & Pekonen, F. (1990) · European Journal of Endocrinology · doi:10.1530/acta.0.1230007 · Cited by 85 · see citing works
Shores, E. W., van Ewijk, W., & Singer, A. (1994) · International Immunology · doi:10.1093/intimm/6.9.1393 · Cited by 79 · see citing works
Telford, N. A., Hogan, A., Franz, C. R., & Schultz, G. A. (1990) · Molecular Reproduction and Development · doi:10.1002/mrd.1080270202 · Cited by 77 · see citing works
LeRoith, D., Yanowski, J., Kaldjian, E. P., Jaffe, E. S., LeRoith, T., Purdue, K., Cooper, B., Pyle, R. S., & Adler, W. H. (1996) · Endocrinology · doi:10.1210/endo.137.3.8603576 · Cited by 75 · see citing works
Age-related changes in the capacity of bone marrow cells to differentiate in thymic organ cultures
Eren, R., Zharhary, D., Abel, L., & Globerson, A. (1988) · Cellular Immunology · doi:10.1016/0008-8749(88)90315-2 · Cited by 64 · see citing works
Kooijman, R., Scholtens, L. E., Rijkers, G. T., & ZEGERS, B. J. M. (1995) · Journal of Endocrinology · doi:10.1677/joe.0.1470203 · Cited by 64 · see citing works
Effects of growth hormone on thymocyte development from progenitor cells in the bone marrow
Knyszynski, A., Adler-Kunin, S., & Globerson, A. (1992) · Brain Behavior and Immunity · doi:10.1016/0889-1591(92)90032-j · Cited by 63 · see citing works
Primary B cell development is impaired in mice with defects of the pituitary/thyroid axis
Montecino‐Rodriguez, E., CLARK, R. G., Powell-Braxton, L., & Dorshkind, K. A. (1997) · The Journal of Immunology · doi:10.4049/jimmunol.159.6.2712 · Cited by 62 · see citing works
Self-citationBeschorner, W. E., Divic, J., PULIDO, H., Yao, X., KENWORTHY, P., & BRUCE, G. (1991) · Transplantation · doi:10.1097/00007890-199111000-00024 · Cited by 62 · see citing works
D'Costa, A. P., Ingram, R. L., LENHAM, J. E., & Sonntag, W. E. (1993) · PubMed · Cited by 55 · see citing works
Li, Y. M., Brunke, D. L., Dantzer, R., & Kelley, K. W. (1992) · Endocrinology · doi:10.1210/endo.130.5.1572290 · Cited by 54 · see citing works
Verland, S., & Gammeltoft, S. (1989) · Molecular and Cellular Endocrinology · doi:10.1016/0303-7207(89)90211-6 · Cited by 51 · see citing works
Murphy, W. J., Durum, S. K., Anver, M. R., Frazier, M. G., & Longo, D. L. (1992) · Brain Behavior and Immunity · doi:10.1016/0889-1591(92)90034-l · Cited by 42 · see citing works
Tsarfaty, G., Longo, D., & Murphy, W. J. (1994) · PubMed · Cited by 39 · see citing works
Thymic Involution in Aging Prospects for Correction
Hadden, J. W., Malec, P., Coto, J. A., & Hadden, E. M. (1992) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1992.tb27458.x · Cited by 36 · see citing works
Quantitative analysis of bone marrow thymic progenitors in young and aged mice
Eren, R., Globerson, A., Abel, L., & Zharhary, D. (1990) · Cellular Immunology · doi:10.1016/0008-8749(90)90129-f · Cited by 36 · see citing works
Lesley, J., Trotter, J., Schulte, R. J., & Hyman, R. (1990) · Cellular Immunology · doi:10.1016/0008-8749(90)90007-e · Cited by 33 · see citing works
Thymocyte progenitors in ageing
Globerson, A. (1994) · Immunology Letters · doi:10.1016/0165-2478(94)00059-x · Cited by 21 · see citing works
Effect of bovine growth hormone administration on the pattern of thymic involution in mice.
Bar‐Dayan, Y., & Small, M. (1994) · PubMed · Cited by 21 · see citing works
Thymic stem cells in mouse bone marrow
Antica, M., Wu, L., Shortman, K., et al. (1994) · Blood · doi:10.1182/blood.v84.1.111.bloodjournal841111 · Cited by 15 · see citing works
Human Growth Hormone and Aging
Mahmud, K. (2003) · New England Journal of Medicine · doi:10.1056/nejmc030764 · Cited by 12 · see citing works
Thymocyte development in vitro: implications for studies of ageing and thymic involution
Montecino‐Rodriguez, E., & Dorshkind, K. A. (1997) · Mechanisms of Ageing and Development · doi:10.1016/s0047-6374(96)01818-0 · Cited by 6 · see citing works
Self-citationNeuroendocrinology and ageing.
O'Neill, P. (1992) · PubMed · Cited by 4 · see citing works
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Cited by
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Pawelec, G. (2002) · Frontiers in bioscience · doi:10.2741/a831 · Cited by 368 · see citing works
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Globerson, A., & Effros, R. B. (2000) · Immunology Today · doi:10.1016/s0167-5699(00)01714-x · Cited by 309 · see citing works
Smith, T. J. (2010) · Pharmacological Reviews · doi:10.1124/pr.109.002469 · Cited by 269 · see citing works
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Napolitano, L. A., Schmidt, D. K., Gotway, M. B., Ameli, N., Filbert, E. L., Ng, M. M., Clor, J. L., Epling, L., Sinclair, E., Baum, P. D., et al. (2008) · Journal of Clinical Investigation · doi:10.1172/jci32830 · Cited by 176 · see citing works
Napolitano, L. A., Lo, J. C.-M., Gotway, M. B., Mulligan, K. M., Barbour, J. D., Schmidt, D. K., Grant, R. M., Halvorsen, R. A., Schambelan, M., & McCune, J. M. (2002) · AIDS · doi:10.1097/00002030-200205240-00003 · Cited by 153 · see citing works
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Pawelec, G. (1999) · Frontiers in bioscience · doi:10.2741/pawelec · Cited by 138 · see citing works
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Min, H., Montecino‐Rodriguez, E., & Dorshkind, K. (2005) · Immunological Reviews · doi:10.1111/j.0105-2896.2005.00263.x · Cited by 96 · see citing works
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Min, H., Montecino‐Rodriguez, E., & Dorshkind, K. A. (2005) · Clinical Immunology · doi:10.1016/j.clim.2005.08.015 · Cited by 71 · see citing works
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Wils, E., & Cornelissen, J. J. (2004) · Blood Reviews · doi:10.1016/j.blre.2004.04.001 · Cited by 44 · see citing works
Growth hormone in T-lymphocyte thymic and postthymic development: A study in HIV-infected children
Viganò, M., Saresella, M., Trabattoni, D., Giacomet, V., di Natale, B., Merlo, M., Venuto, A., Villa, M. L., Vanzulli, S., Ferrante, P., et al. (2004) · The Journal of Pediatrics · doi:10.1016/j.jpeds.2004.06.027 · Cited by 35 · see citing works
Thymic Hypoplasia in Japanese Black Calves with Stillbirth/Perinatal Weak Calf Syndrome
Takasu, M., Shirota, K., Yasunori, O. H. B. A., NISHII, N., MURASE, T., MIYAZAWA, K., & KITAGAWA, H. (2008) · Journal of Veterinary Medical Science · doi:10.1292/jvms.70.1173 · Cited by 23 · see citing works
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Fahy, G. M. (2003) · Rejuvenation Research · doi:10.1089/109454503322733063 · Cited by 23 · see citing works
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Chappel, S. C. (1999) · Journal of Acquired Immune Deficiency Syndromes & Human Retrovirology · doi:10.1097/00042560-199904150-00003 · Cited by 19 · see citing works
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Immunity to infections following hematopoietic cell transplantation
Brown, J. W., Weissman, I. L., & Shizuru, J. A. (2001) · Current Opinion in Immunology · doi:10.1016/s0952-7915(00)00240-5 · Cited by 11 · see citing works
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Linton, P., Lustgarten, J., & Thoman, M. L. (2006) · Clinical and Applied Immunology Reviews · doi:10.1016/j.cair.2006.06.001 · Cited by 10 · see citing works
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Savino, W., Smaniotto, S., & Dardenne, M. (2005) · Advances in experimental medicine and biology · doi:10.1007/0-387-26274-1_7 · Cited by 4 · see citing works
Goffinet, L., Mottet, M., Kermani, H., Renard-Charlet, C., Geenen, V. G., & Martens, H. (2011) · Immunology Endocrine & Metabolic Agents - Medicinal Chemistry · doi:10.2174/187152211794519421 · Cited by 3 · see citing works
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Arsenijévic, Y. (2005) · Springer eBooks · doi:10.1007/0-387-26274-1_15 · Cited by 1 · see citing works
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- Authors
- Montecino-Rodriguez, E., Clark, R., & Dorshkind, K.
- Venue
- Endocrinology
- Publisher
- The Endocrine Society
- Published
- 1998-10
- Volume
- 139
- Issue
- 10
- Pages
- 4120-4126
- ISSN
- 0013-7227 (ISSN-L)
- 1945-7170
- OpenAlex
- W4251460696
- Cited by
- 36
- References
- 40
- Citations by year
- 2018: 1 · 2013: 1
- FWCI
- 0.48
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Endocrinology (publishedVersion)
- Funders
- National Institutes of Health
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Growth Hormone and Insulin-like Growth Factors
- Health Sciences › Medicine › Hematology › Hematopoietic Stem Cell Transplantation
- Keywords
- insulin-like growth factor I, thymopoiesis, thymus aging, bone marrow transplantation, thymus cellularity, T cell precursors, growth hormone, hormone replacement therapy, thymic organ culture, aged mice
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