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The maternal-neonatal neuro-immune interface: Are there long-term implications for inflammatory or stress-related disease?
Open accessAbstract
Inflammatory stimuli reliably elicit hypothalamic-pituitary-adrenal (HPA) activation, and it is now established that the immune and HPA systems are mutually regulatory and that their interactions partly determine stress effects on immune function. What has not been extensively investigated, however, is the interactive nature of the development of the endocrine and immune systems and whether this might alter predisposition to inflammatory disease or stress-related pathologies. Increasing attention is now being focused on the role of early life environments determining long-term predisposition to disease, and a role for the HPA axis in disease predisposition is emerging. Stress generally refers to the condition where coping with actual or perceived stimuli alters the homeostatic state of the organism. The classic stress response involves the activation of central and peripheral catecholamine systems and HPA responses. Increased glucocorticoid levels are thought to protect the organism, both by providing energy substrates to deal with immediate environmental demands and by blocking potentially harmful overreaction by the immune system and other stress-reactive systems (1). However, to avoid immunosuppression and degenerative pathologies associated with increased glucocorticoid levels, the HPA stress response must terminate efficiently once the environmental demands are removed (2). Consequently, disturbances in endocrine-immune interactions upset the normal regulatory homeostatic balance and alter susceptibility to a variety of disease states associated with immune dysregulation (3). The physiological impact of stress is variable across individuals, and susceptibility to stress apparently depends on attributes of the organism, such as genetic endowment and age, and experiential factors, such as previous stress experiences, and early life events (4, 5). Indeed, the endocrine and immune systems and the CNS all respond to environmental pressures during development, and the interactive nature of these systems suggests that alterations in one system could have developmental consequences for the others and potential long-term implications for disease vulnerability. Plasticity in most developing physiological systems is thought to be of adaptive importance, enabling an organism to better meet the demands of the environment in which it matures and will most likely reside. However, the short-term reorganization or re-setting of regulatory systems to deal with immediate demands may also have long-term consequences for normal physiological function, thereby predisposing an organism to pathology. This may particularly be the case when the environmental pressures differ between development and adulthood. A number of epidemiological studies have indicated that nutritional factors early in life have long-term implications for cardiovascular and metabolic disease in adulthood. Most data suggest that maternal nutrition and limited intrauterine growth are responsible for reorganizing metabolic regulation and results in metabolic and cardiovascular pathologies in adult life (6). The concept of “perinatal programming” is not new and has long been investigated in neuroendocrine development of both the adrenal and the gonadal axes (see review, ref. 7). Immune responses, too, are influenced by early life experiences, and it has been suggested that pathogen exposure during development is important for the developing immune repertoire and that too little activation may be associated with the development of allergy (8). Available data also indicate that there are long-term consequences following endocrine-immune interactions during the first week of life. Thus, the administration of steroids during antigen exposure alters the development of immune tolerance (9), and immune challenge during the first week of life is associated with altered endocrine development (10, 11). These data demonstrate the interactive nature of both the immune and the neuroendocrine systems during development and show that these interactions can alter both immune and endocrine function in the long term. Maternal factors represent some of the most salient environmental influences altering endocrine development (12–14). Indeed, there is an extensive literature detailing both prenatal and postnatal influences on the development of the HPA axis. It is also well established that immune factors passed in utero and also to the neonate via milk have a direct impact on the its immunocompetence (15, 16). However, evidence examining the neuro-immune interface and maternal factors is limited.
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“Animal models suggest that maternal care exerts a critical influence on the development of the stress response (6) and may alter the long-term predisposition to inflammation (7).”
From Childhood maltreatment predicts adult inflammation in a life-course study (2007) · cites this paper as [7]
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Liu, D., Diorio, J., Tannenbaum, B., Caldji, C., Francis, D., Freedman, A., Sharma, S., Pearson, D., Plotsky, P. M., & Meaney, M. J. (1997) · Science · doi:10.1126/science.277.5332.1659 · Cited by 3,170
Prenatal stress, glucocorticoids and the programming of the brain
Welberg, L. A. M., & Seckl, J. R. (2001) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2001.00601.x · Cited by 928
Chronic stress alters the immune response to influenza virus vaccine in older adults.
Kiecolt-Glaser, J. K., Glaser, R., Gravenstein, S., Malarkey, W. B., & Sheridan, J. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.7.3043 · Cited by 789
Cytokines and the Brain: Implications for Clinical Psychiatry
Kronfol, Z., & Remick, D. G. (2000) · American Journal of Psychiatry · doi:10.1176/appi.ajp.157.5.683 · Cited by 784
Adoption reverses the long-term impairment in glucocorticoid feedback induced by prenatal stress
Maccari, S., Piazza, P., Kabbaj, M., Barbazanges, A., Simon, H., & Moal, M. L. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-01-00110.1995 · Cited by 580
Effects of early adverse experiences on brain structure and function: clinical implications
Kaufman, J., Plotsky, P. M., Nemeroff, C. B., & Charney, D. S. (2000) · Biological Psychiatry · doi:10.1016/s0006-3223(00)00998-7 · Cited by 508
Urakubo, A., Jarskog, L. F., Lieberman, J. A., & Gilmore, J. H. (2001) · Schizophrenia Research · doi:10.1016/s0920-9964(00)00032-3 · Cited by 405
Give us this day our daily germs
Rook, G. A. W., & Stanford, J. L. (1998) · Immunology Today · doi:10.1016/s0167-5699(98)80008-x · Cited by 393
Shanks, N., Windle, R. J., Perks, P. A., Harbuz, M. S., Jessop, D. S., Ingram, C. D., & Lightman, S. L. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.090571897 · Cited by 374
Self-citationShanks, N., Larocque, S., & Meaney, M. (1995) · The Journal of Neuroscience · doi:10.1523/jneurosci.15-01-00376.1995 · Cited by 278
Self-citationBiondi, M., & Zannino, L.-G. (2010) · Psychotherapy and Psychosomatics · doi:10.1159/000289101 · Cited by 255
Mason, D. (1991) · Immunology Today · doi:10.1016/0167-5699(91)90158-p · Cited by 254
Multifactorial regulation of the hypothalamic-pituitary-adrenal axis during development
Rosenfeld, P., Suchecki, D., & Levine, S. (1992) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(05)80196-4 · Cited by 231
Give us this day our daily germs
Rook, G. A. W. (1998) · Immunology Today · doi:10.1016/s0167-5699(97)01204-8 · Cited by 202
The fetal origins of adult hypertension
Barker, D. J. P. (1992) · Journal of Hypertension · doi:10.1097/00004872-199212000-00004 · Cited by 186
Chronic stress alters the immune response to influenza virus vaccine in older adults
Kiecolt-Graser, J. (1996) · Medical Entomology and Zoology · Cited by 151
Prenatal Stress Depresses Immune Function in Rats
Kay, G., Tarcic, N., Poltyrev, T., & Weinstock, M. (1998) · Physiology & Behavior · doi:10.1016/s0031-9384(97)00456-3 · Cited by 149
Prenatal immune challenge alters the hypothalamic-pituitary-adrenocortical axis in adult rats.
Reul, J. M. H. M., Stec, I. S. M., Wiegers, G. J., Labeur, M. S., Linthorst, A. C. E., ARZT, E. S., & Holsboer, F. (1994) · Journal of Clinical Investigation · doi:10.1172/jci117272 · Cited by 142
Catalani, A., Casolini, P., Scaccianoce, S., Patacchioli, F. R., Spinozzi, P., & Angelucci, L. (2000) · Neuroscience · doi:10.1016/s0306-4522(00)00277-3 · Cited by 140
Stress and the Individual: Mechanisms Leading to Disease
McEwen, B. S. (1993) · Archives of Internal Medicine · doi:10.1001/archinte.1993.00410180039004 · Cited by 103
Early environmental programming hypothalamic-pituitary-adrenal responses to stress
Meaney, M. J., Tannenbaum, B. M., Francis, D. D., Bhatnagar, S., Shanks, N. M., Viau, V., O’Donnell, D., & Plotsky, P. M. (1994) · Seminars in Neuroscience · doi:10.1006/smns.1994.1032 · Cited by 96
Self-citationSobrian, S. K., Vaughn, V. T., Ashe, W. K., Markovic, B., DJURIĆ, V. J., & Janković, B. D. (1997) · Environmental Research · doi:10.1006/enrs.1997.3734 · Cited by 87
Bakker, J. M., Kavelaars, A., Kamphuis, P. J. G. H., Cobelens, P. M., van Vugt, H. H., van Bel, F., & Heijnen, C. J. (2000) · The Journal of Immunology · doi:10.4049/jimmunol.165.10.5932 · Cited by 85
Prenatal stress alters immune function in the offspring of rats
Klein, S. L., & Rager, D. R. (1995) · Developmental Psychobiology · doi:10.1002/dev.420280603 · Cited by 76
Kavelaars, A., van der Pompe, G., Bakker, J. M., van Hasselt, P. M., Cats, B. P., Visser, G. H. A., & Heijnen, C. J. (1999) · Pediatric Research · doi:10.1203/00006450-199903000-00003 · Cited by 71
Prenatal Influences on Neuroimmune Set Points in Infancy
Coe, C. L., & Lubach, G. R. (2000) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2000.tb05411.x · Cited by 61
Coe, C. L., & Crispen, H. R. (2000) · Health Psychology · doi:10.1037/0278-6133.19.6.554 · Cited by 54
Reyes, T. M., & Coe, C. L. (1997) · Brain Research · doi:10.1016/s0006-8993(97)00687-2 · Cited by 53
Maternal Deprivation and Early Weaning Modulate Experimental Allergic Encephalomyelitis in the Rat
Laban, O., Marković, B. M., Dimitrijević, M., & Janković, B. D. (1995) · Brain Behavior and Immunity · doi:10.1006/brbi.1995.1002 · Cited by 43
Alterations in the Pituitary–Adrenal Axis of Adult Mice Following Neonatal Exposure to Interleukin-1
del Rey, A., Furukawa, H., MONGE‐ARDITI, G., Kabiersch, A., Voigt, K., & Besedovsky, H. O. (1996) · Brain Behavior and Immunity · doi:10.1006/brbi.1996.0021 · Cited by 42
Influence of early life events on immune reactivity in adult mice
Neveu, P. J., Deleplanque, B., Puglisi‐Allegra, S., D'Amato, F. R., & Cabib, S. (1994) · Developmental Psychobiology · doi:10.1002/dev.420270403 · Cited by 40
Hilakivi-Clarke, L. A., Wright, A., & Lippman, M. E. (1993) · Physiology & Behavior · doi:10.1016/0031-9384(93)90104-n · Cited by 40
Experimental allergic encephalomyelitis in adult DA rats subjected to neonatal handling or gentling
Laban, O., Dimitrijević, M., von Hörsten, S., Marković, B. M., & Janković, B. D. (1995) · Brain Research · doi:10.1016/0006-8993(95)00106-z · Cited by 39
Susceptibility to adjuvant arthritis: relative importance of adrenal activity and bacterial flora
van de Langerijt, A. G. M., van Lent, P. L. E. M., Hermus, A. R. M. M., Sweep, F. C. G. J., Cools, A. R., & van den Berg, W. B. (1994) · Clinical & Experimental Immunology · doi:10.1111/j.1365-2249.1994.tb06575.x · Cited by 37
Saravia, F., Durant, S., Hasnaoui, A. E., Dardenne, M., & Homo‐Delarche, F. (1996) · Autoimmunity · doi:10.3109/08916939609001952 · Cited by 36
Short- and Long-Term Effects of Perinatal lnterleukin-1β-Application in Rats
Götz, F., Dörner, G., Malz, U., Rohde, W., Stahl, F., Poppe, I., Schulze, M., & Plagemann, A. (2008) · Neuroendocrinology · doi:10.1159/000126560 · Cited by 33
Gorczynski, R. M. (1992) · Brain Behavior and Immunity · doi:10.1016/0889-1591(92)90062-s · Cited by 29
Neonatal handling in eae‐susceptible rats altersNGFlevels and mast cell distribution in the brain
Manni, L., Micera, A., Pistillo, L., & Aloe, L. (1998) · International Journal of Developmental Neuroscience · doi:10.1016/s0736-5748(98)00003-3 · Cited by 25
Bhatnagar, S., Shanks, N. M., & Meaney, M. J. (1996) · Developmental Psychobiology · doi:10.1002/(sici)1098-2302(199603)29:2 · Cited by 23
Self-citationChalmers, J. P., Arnolda, L., Kapoor, V., Llewellyn‐Smith, I. J., Minson, J. B., & Pilowsky, P. M. (1992) · Journal of Hypertension · doi:10.1097/00004872-199212007-00003 · Cited by 23
Stress, the Hypothalamic-Pituitary-Adrenal Axis, and Immune Function
Stein, M., & Miller, A. H. (1993) · Advances in experimental medicine and biology · doi:10.1007/978-1-4615-2980-4_1 · Cited by 17
Sexual differentiation of neural circuitry in the neuroendocrine hypothalamus
Matsumoto, A., & Arai, Y. (1997) · Biomedical Reviews · doi:10.14748/bmr.v7.158 · Cited by 17
Long-Term Effects of Neuroendocrine–Immune Interactions during Early Development
O’Grady, M. P., & HALL, N. R. S. (1991) · Elsevier eBooks · doi:10.1016/b978-0-12-043780-1.50025-7 · Cited by 14
Dimitrijević, M., Marković, B. M., Laban, O., & Janković, B. D. (1995) · Journal of Neuroimmunology · doi:10.1016/0165-5728(94)00186-r · Cited by 3
Bailey (1999) · doi:10.1002/(sici)1098-2302(199909)35:2
Research works printed but not linked: 2
- 10.1001/archinte.153.18.2093 · DOI · Paper page
- 10.1046/j.1365-2826.2001.00601.x · DOI · Paper page
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Metadata
- Authors
- Shanks, N., & Lightman, S. L.
- Affiliations
- University of Bristol (GB)
- Corresponding author
- Shanks, Nola
- Venue
- Journal of Clinical Investigation
- Published
- 2001-12-01
- Volume
- 108
- Issue
- 11
- Pages
- 1567-1573
- ISSN
- 0021-9738 (ISSN-L)
- PMC
- PMC200999
- OpenAlex
- W2013929399
- Cited by
- 111
- References
- 45
- Citations by year
- 2024: 1 · 2023: 2 · 2022: 2 · 2021: 3 · 2020: 4 · 2019: 4 · 2018: 3 · 2017: 7 · 2016: 5 · 2015: 5 · 2014: 6 · 2013: 4 · 2012: 6
- FWCI
- 0.48
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Clinical Investigation (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Explore Bristol Research (publishedVersion)
- Bristol Research (University of Bristol) (submittedVersion)
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Maternal Mental Health During Pregnancy and Postpartum
- Keywords
- endocrine-immune interaction, hypothalamic-pituitary-adrenal axis, glucocorticoids, early life stress, developmental programming, disease susceptibility, immune dysregulation, maternal nutrition, fetal growth restriction, stress response, long-term health effects, stress-related disorders, developmental plasticity, glucocorticoid receptor
- MeSH terms
- Animals, Female, Fetus, Homeostasis, Humans, Hypothalamo-Hypophyseal System, Immune System, Inflammation, Pituitary-Adrenal System, Pregnancy, Pregnancy Complications, Stress, Physiological
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