Alterations induced by chronic stress in lymphocyte subsets of blood and primary and secondary immune organs of mice
Open accessAbstract
BACKGROUND: The immune system is particularly sensitive to stress. Although acute stress generally has positive effects, chronic stress typically provokes immunosuppression. The elucidation of the mechanisms involved in immunosuppression are of interest for the design of therapeutic approaches to avoid the appearance of stress disorders. This study aimed to investigate chronic stress-induced alterations on lymphocyte subset distribution and percentages. The experiments were performed with C57BL/6 mice subjected to chronic immobilization stress. RESULTS: Stress caused a marked increase in apoptosis inside the thymus, and a reduction in the total number of thymocytes. Furthermore, the proportion of immature thymocytes declined significantly suggesting that the increased apoptosis mainly affected cells of immature phenotype. In blood, the total number of lymphocytes diminished but not all lymphocyte populations showed the same tendency: while the relative proportion of B cells declined slightly, the relative proportion of circulating CD3+ cells, and particularly some T cell subsets showing an immature phenotype (CD3+PNA+), increased under stress. The spleen and lymph nodes show a marked reduction in cellularity, but the relative proportion of T cells increased, while no change or only a slight reduction was observed in the relative proportion of B cells. Similarly, the relative proportion of T cells increased in bone marrow. CONCLUSIONS: Detailed data on the alterations of lymphoid cell subsets occurring under immobilization stress, both in the bloodstream and in different lymphoid tissues, are obtained. In general, T cells are more affected than B cells and, in particular, a marked increase in the percentage of a subset of circulating PNA+CD3+ T cells is observed.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Reductions in perceived stress correlate with decreases in right basolateral amygdala gray matter density.
“Neurobiological studies have identified the amygdala as a crucial brain region in stress responses, with research showing that reductions in perceived stress correlate with decreases in right basolateral amygdala gray matter density [4,5,6,7].”
From Comprehensive review of chronic stress pathways and the efficacy of behavioral stress reduction programs (BSRPs) in managing diseases. (2024) · cites this paper as [4]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
An analysis of variance test for normality (complete samples)
SHAPIRO, S. S., & WILK, M. B. (1965) · Biometrika · doi:10.1093/biomet/52.3-4.591 · Cited by 23,480 · see citing works
McEwen, B. S. (2000) · Brain Research · doi:10.1016/s0006-8993(00)02950-4 · Cited by 1,827 · cited 1× · see citing works
“Acute stress generally has positive effects, while chronic stress typically provokes immunosuppression and diverse associated pathologies, including autoimmune diseases [22–28].”
BackgroundGlucocorticoids in T Cell Development and Function
Ashwell, J. D., Lu, F. W. M., & Vacchio, M. S. (2000) · Annual Review of Immunology · doi:10.1146/annurev.immunol.18.1.309 · Cited by 777 · cited 1× · see citing works
“This pathway, during which the cells undergo several phenotypic changes, involves the interplay of numerous molecules [7–15], and it is in fact completed by only a small percentage of thymocytes [16].”
BackgroundEffects of stress on immune cell distribution. Dynamics and hormonal mechanisms.
Dhabhar, F. S., Miller, A. H., McEwen, B. S., & Spencer, R. L. (1995) · The Journal of Immunology · doi:10.4049/jimmunol.154.10.5511 · Cited by 730 · cited 1× · see citing works
“Redistribution of leukocytes was also reported under acute stress by Dhabhar et al [21].”
BackgroundEnhancing versus suppressive effects of stress hormones on skin immune function
Dhabhar, F. S., & McEwen, B. S. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.3.1059 · Cited by 672 · cited 1× · see citing works
“Acute stress generally has positive effects, while chronic stress typically provokes immunosuppression and diverse associated pathologies, including autoimmune diseases [22–28].”
BackgroundScollay, R. G., Butcher, E. C., & Weissman, I. L. (1980) · European Journal of Immunology · doi:10.1002/eji.1830100310 · Cited by 555 · cited 1× · see citing works
“This pathway, during which the cells undergo several phenotypic changes, involves the interplay of numerous molecules [7–15], and it is in fact completed by only a small percentage of thymocytes [16].”
BackgroundCatecholamine-Induced Leukocytosis: Early Observations, Current Research, and Future Directions
Benschop, R. J., Rodriguez-Feuerhahn, M., & Schedlowski, M. (1996) · Brain Behavior and Immunity · doi:10.1006/brbi.1996.0009 · Cited by 521 · see citing works
The thymus selects the useful, neglects the useless and destroys the harmful
von Boehmer, H., Teh, H. S., & Kisielow, P. (1989) · Immunology Today · doi:10.1016/0167-5699(89)90307-1 · Cited by 372 · see citing works
Constitutive activation of NF‐κB and T‐cell leukemia/lymphoma in Notch3 transgenic mice
Bellavia, D., Campese, A. F., Alesse, E., Vacca, A., Felli, M. P., Balestri, A., Stoppacciaro, A., Tiveron, C., Tatangelo, L., Giovarelli, M., et al. (2000) · The EMBO Journal · doi:10.1093/emboj/19.13.3337 · Cited by 361 · cited 1× · see citing works
“This pathway, during which the cells undergo several phenotypic changes, involves the interplay of numerous molecules [7–15], and it is in fact completed by only a small percentage of thymocytes [16].”
BackgroundWeissman, I. L. (1967) · The Journal of Experimental Medicine · doi:10.1084/jem.126.2.291 · Cited by 347 · see citing works
Moraska, A. F., Terrence Deak, B., Spencer, R. L., Roth, D., & Fleshner, M. (2000) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.2000.279.4.r1321 · Cited by 325 · cited 1× · see citing works
“Acute stress generally has positive effects, while chronic stress typically provokes immunosuppression and diverse associated pathologies, including autoimmune diseases [22–28].”
BackgroundAyala, A., Herdon, C. D., Lehman, D. L., Ayala, C. A., & Ih, C. (1996) · Blood · doi:10.1182/blood.v87.10.4261.bloodjournal87104261 · Cited by 259 · cited 1× · see citing works
“The increase in apoptosis in the thymus under immobilization stress is in line with the results obtained in other studies [18,29].”
ResultDynamics of Early T Cells: Prothymocyte Migration and Proliferation in the Adult Mouse Thymus
Scollay, R. G., Smith, J., & Stauffer, V. K. (1986) · Immunological Reviews · doi:10.1111/j.1600-065x.1986.tb01487.x · Cited by 184 · cited 1× · see citing works
“In the most important T-cell maturation pathway, the intrathymic pathway, pre-T cells repopulate the thymus to become mature T cells [3–6].”
BackgroundLymphocyte Development from Stem Cells
Ikuta, K., Uchida, N., Friedman, J. S., & Weissman, I. L. (1992) · Annual Review of Immunology · doi:10.1146/annurev.iy.10.040192.003551 · Cited by 164 · cited 1× · see citing works
“Background Under normal conditions, the generation of the T-cell repertoire begins with the differentiation of precursor T cells (pre-T cells) in the fetal liver (during early embryogenesis) or bone marrow (during later embryogenesis and after birth [1,2].”
BackgroundStress, cytokine patterns and susceptibility to disease
Elenkov, I. J., & Chrousos, G. P. (1999) · Best Practice & Research Clinical Endocrinology & Metabolism · doi:10.1053/beem.1999.0045 · Cited by 128 · cited 1× · see citing works
“Acute stress generally has positive effects, while chronic stress typically provokes immunosuppression and diverse associated pathologies, including autoimmune diseases [22–28].”
BackgroundPhysiological responses of extrathymic T cells in the liver
Abo, T., Kawamura, T., & Watanabe, H. (2000) · Immunological Reviews · doi:10.1034/j.1600-0528.2002.017415.x · Cited by 127 · cited 1× · see citing works
“It has been reported previously that self-reactive forbidden clones, showing a higher resistance to apoptosis, arise under immunosuppression, differentiating via alternative thymic, hepatic and other pathways, and that stress play a role in the onset of several pathologies including autoimmune diseases [30–35].”
BackgroundMastorakos, G. P., & Ilias, Ι. (2000) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2000.tb06220.x · Cited by 116 · see citing works
Wu, W., Yamaura, T., Murakami, K., Murata, J., Matsumoto, K., Watanabe, H., & Saiki, I. (2000) · Life Sciences · doi:10.1016/s0024-3205(00)00506-3 · Cited by 116 · cited 1× · see citing works
“The immune system is particularly sensitive to stress, and specific effects of stress have been demonstrated by a number of studies [18–21].”
BackgroundMicroenvironmental regulation of T cell development in the thymus
Anderson, G., Harman, B. C., Hare, K. J., & Jenkinson, E. J. (2000) · Seminars in Immunology · doi:10.1006/smim.2000.0260 · Cited by 100 · cited 1× · see citing works
“In the most important T-cell maturation pathway, the intrathymic pathway, pre-T cells repopulate the thymus to become mature T cells [3–6].”
BackgroundPhysiological programmed cell death in thymocytes is induced by physical stress (exercise)
Concordet, J., & Ferry, A. (1993) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.1993.265.3.c626 · Cited by 95 · cited 1× · see citing works
“The increase in apoptosis in the thymus under immobilization stress is in line with the results obtained in other studies [18,29].”
ResultThe Immune System during Exposure to Extreme Physiologic Conditions
Pedersen, B. K., Kappel, M., Klokker, M., Nielsen, H. S., & Secher, N. H. (1994) · International Journal of Sports Medicine · doi:10.1055/s-2007-1021125 · Cited by 88 · cited 1× · see citing works
“Acute stress generally has positive effects, while chronic stress typically provokes immunosuppression and diverse associated pathologies, including autoimmune diseases [22–28].”
BackgroundDifferentiation and cell division in the mammalian thymus
Rothenberg, E. V., & Lugo, J. P. (1985) · Developmental Biology · doi:10.1016/0012-1606(85)90114-9 · Cited by 82 · cited 1× · see citing works
“In the most important T-cell maturation pathway, the intrathymic pathway, pre-T cells repopulate the thymus to become mature T cells [3–6].”
BackgroundEarly Ontogeny of Thymocytes in Pigs: Sequential Colonization of the Thymus by T Cell Progenitors
Šinkora, M., Šinkora, J., Šinkorová, Z., & Butler, J. E. (2000) · The Journal of Immunology · doi:10.4049/jimmunol.165.4.1832 · Cited by 75 · cited 1× · see citing works
“In the most important T-cell maturation pathway, the intrathymic pathway, pre-T cells repopulate the thymus to become mature T cells [3–6].”
BackgroundHuman intrathymic T cell differentiation.
Haynes, B. F., Denning, S. M., Le, P. T., & Singer, K. H. (1990) · PubMed · Cited by 74 · see citing works
Similarities and Differences between Extrathymic T Cells Residing in Mouse Liver and Intestine
Ohtsuka, K., Iiai, T., Watanabe, H., Tanaka, T. T., Miyasaka, M., Sato, K., Asakura, H., & Abo, T. (1994) · Cellular Immunology · doi:10.1006/cimm.1994.1005 · Cited by 70 · cited 1× · see citing works
“It has been reported previously that self-reactive forbidden clones, showing a higher resistance to apoptosis, arise under immunosuppression, differentiating via alternative thymic, hepatic and other pathways, and that stress play a role in the onset of several pathologies including autoimmune diseases [30–35].”
BackgroundStress, Affective Disorders, and Immune Function
Schindler, B. A. (1985) · Medical Clinics of North America · doi:10.1016/s0025-7125(16)31034-3 · Cited by 63 · cited 1× · see citing works
“Acute stress generally has positive effects, while chronic stress typically provokes immunosuppression and diverse associated pathologies, including autoimmune diseases [22–28].”
BackgroundThe Gtpase Rho Controls a P53-Dependent Survival Checkpoint during Thymopoiesis
Costello, P. S., Cleverley, S. C., Galandrini, R., Henning, S. W., & Cantrell, D. A. (2000) · The Journal of Experimental Medicine · doi:10.1084/jem.192.1.77 · Cited by 62 · cited 1× · see citing works
“This pathway, during which the cells undergo several phenotypic changes, involves the interplay of numerous molecules [7–15], and it is in fact completed by only a small percentage of thymocytes [16].”
BackgroundShimizu, S., Kawamura, Miyaji, Oya, Bannai, Yamamoto, Y., Weerasinghe, Halder, †↑, W., Hatakeyama, et al. (2000) · Scandinavian Journal of Immunology · doi:10.1046/j.1365-3083.2000.00695.x · Cited by 57 · cited 1× · see citing works
“It has been reported previously that self-reactive forbidden clones, showing a higher resistance to apoptosis, arise under immunosuppression, differentiating via alternative thymic, hepatic and other pathways, and that stress play a role in the onset of several pathologies including autoimmune diseases [30–35].”
BackgroundAberrant Development of Thymocytesin Mice Lacking Laminin‐2
Magner, W. J., Chang, A. C., Owens, J. W., Hong, M.-J. P., Brööks, A. G., & Coligan, J. E. (2000) · Journal of Immunology Research · doi:10.1155/2000/90943 · Cited by 42 · see citing works
Bödey, B., Bödey, B., Siegel, S. E., & Kaiser, H. E. (2000) · PubMed · Cited by 36 · see citing works
Zerrahn, J., Volkmann, A., Coles, M. C., Held, W., Lemonnier, F. A., & Raulet, D. H. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.20.11470 · Cited by 36 · see citing works
Moroda, T., Kawachi, Y., Iiai, T., Tsukahara, A., Suzuki, S., TADA, T., Watanabe, H., Hatakeyama, K., & Abo, T. (1997) · Immunology · doi:10.1046/j.1365-2567.1997.00222.x · Cited by 28 · cited 1× · see citing works
“It has been reported previously that self-reactive forbidden clones, showing a higher resistance to apoptosis, arise under immunosuppression, differentiating via alternative thymic, hepatic and other pathways, and that stress play a role in the onset of several pathologies including autoimmune diseases [30–35].”
BackgroundYuuki, H., Yoshikai, Y., Kishihara, K., Iwasaki, A., Matsuzaki, G., Takimoto, H., & Nomoto, K. (1990) · European Journal of Immunology · doi:10.1002/eji.1830200711 · Cited by 23 · see citing works
Geenen, V. G., Kecha, O., Brilot, F., Charlet-Renard, C., & Martens, H. (1999) · NeuroImmunoModulation · doi:10.1159/000026371 · Cited by 22 · cited 1× · see citing works
“This pathway, during which the cells undergo several phenotypic changes, involves the interplay of numerous molecules [7–15], and it is in fact completed by only a small percentage of thymocytes [16].”
BackgroundRegulation of pre-T-cell development
Möröy, T., & Karsunky, H. (2000) · Cellular and Molecular Life Sciences · doi:10.1007/pl00000737 · Cited by 18 · cited 1× · see citing works
“This pathway, during which the cells undergo several phenotypic changes, involves the interplay of numerous molecules [7–15], and it is in fact completed by only a small percentage of thymocytes [16].”
BackgroundLamontagne, L., Massicotte, E. M., & Pagé, C. (1997) · Immunology · doi:10.1111/j.1365-2567.1997.00402.x · Cited by 12 · see citing works
Lymphocyte Development From Stem Cells
Ikuta, K. (1992) · Annual Review of Immunology · doi:10.1146/annurev.immunol.10.1.759 · Cited by 9 · see citing works
Jacobs, H. (2000) · Seminars in Immunology · doi:10.1006/smim.2000.0262 · Cited by 5 · cited 1× · see citing works
“This pathway, during which the cells undergo several phenotypic changes, involves the interplay of numerous molecules [7–15], and it is in fact completed by only a small percentage of thymocytes [16].”
Background
Flagged first, then by citations
Cited by
Sorted by citations
Interpreting Stress Responses during Routine Toxicity Studies
Everds, N. E., Snyder, P. W., Bailey, K. L., Bolon, B. N., Creasy, D. M., Foley, G. L., Rosol, T. J., & Sellers, T. S. (2013) · Toxicologic Pathology · doi:10.1177/0192623312466452 · Cited by 338 · see citing works
“lymphocytes, with a minor component of redistribution (Dominguez-Gerpe and Rey-Mendez 2001; Herold, McPherson, and Reichardt 2006; Irwin 1994; Padgett and Glaser 2003).”
BackgroundKrüger, K., & Mooren, F. C. (2026) · PubMed · doi:10.22029/eir.2007.1629 · Cited by 137 · see citing works
Vitlic, A., Lord, J. M., & Phillips, A. C. (2014) · AGE · doi:10.1007/s11357-014-9631-6 · Cited by 123 · see citing works
Stressed to death: Implication of lymphocyte apoptosis for psychoneuroimmunology
Shi, Y., Devadas, S., Greeneltch, K. M., Yin, D., Mufson, R. A., & Zhou, J. (2003) · Brain Behavior and Immunity · doi:10.1016/s0889-1591(02)00062-4 · Cited by 88 · see citing works
Finnell, J. E., Lombard, C. M., Melson, M. N., Singh, N. P., Nagarkatti, M., Nagarkatti, P. S., Fadel, J. R., Wood, C. S., & Wood, S. K. (2016) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2016.08.019 · Cited by 86 · see citing works
“There is limited evidence to suggest that social stress can alter the expression of CD3+ (Dominguez-Gerpe and Rey-Mendez, 2001) and CD8+ (Stefanski and Engler, 1998) T-cells.”
Comprehensive Assessment and Mathematical Modeling of T Cell Population Dynamics and Homeostasis
Thomas‐Vaslin, V., Altes, H. K., de Boer, R. J., & Klatzmann, D. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.180.4.2240 · Cited by 86 · see citing works
“To deliver GCV continuously and avoid chronic stress by repeated mouse manipulation—which can induce thymic atrophy and severely affect T cell homeostasis (33), an osmotic pump was implanted in TK mice on day 0, by s.”
MethodEstruel‐Amades, S., Massot‐Cladera, M., Garcia-Cerdà, P., Pérez-Cano, F. J., Franch, À., Castell, M., & Camps‐Bossacoma, M. (2019) · Nutrients · doi:10.3390/nu11040783 · Cited by 74 · see citing works
Shchaslyvyi, A. Y., Antonenko, S. V., & Telegeev, G. D. (2024) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph21081077 · Cited by 73 · see citing works
Green Brazilian Propolis Action on Macrophages and Lymphoid Organs of Chronically Stressed Mice
Missima, F., & Sforcin, J. M. (2006) · Evidence-based Complementary and Alternative Medicine · doi:10.1093/ecam/nel112 · Cited by 62 · see citing works
Devalapalli, A. P., Lesher, A. P., Shieh, K., Solow, J. S., Everett, M. L., Edala, A. S., Whitt, P. B., Long, R. R., Newton, N. H., & Parker, W. (2006) · Scandinavian Journal of Immunology · doi:10.1111/j.1365-3083.2006.01785.x · Cited by 49 · see citing works
Effects of anxiety on TNF-α levels during psychological stress
Chandrashekara, S., Jayashree, K., Veeranna, H. B., Vadiraj, H. S., Ramesh, M. N., Shobha, A., Sarvanan, Y., & Vikram, Y. K. (2007) · Journal of Psychosomatic Research · doi:10.1016/j.jpsychores.2007.03.001 · Cited by 47 · see citing works
“The most frequently observed response is immune suppression, especially when the stress is chronic and persisting [1–3].”
BackgroundLi, Y., Jiang, W., Li, Z., Zhang, C., Huang, C. Y., Yang, J. J., Kong, G., & Li, Z. (2017) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2017.11.148 · Cited by 46 · see citing works
Missima, F., Pagliarone, A. C., Orsatti, C. L., Araújo, J. P., & Sforcin, J. M. (2010) · Phytotherapy Research · doi:10.1002/ptr.3142 · Cited by 43 · see citing works
“This procedure is easily performed and causes no physical pain to the animals (Domínguez-Gerpe and Rey-Méndez, 2001; Sforcin et al., 2007).”
BackgroundHernández, M. E., Martı́nez-Mota, L., Salinas, C., Márquez-Velasco, R., Hernández‐Chan, N. G., Morales‐Montor, J., Pérez-Tapia, M., Streber, M. L., Granados-Camacho, I., Becerril‐Villanueva, E., et al. (2013) · BioMed Research International · doi:10.1155/2013/868742 · Cited by 41 · see citing works
Herkenham, M. A., & Kigar, S. L. (2016) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2016.09.003 · Cited by 40 · see citing works
The effects of spaceflight and fracture healing on distant skeletal sites
Dadwal, U. C., Maupin, K. A., Zamarioli, A., Tucker, A., Harris, J. S., Fischer, J. P., Rytlewski, J. D., Scofield, D. C., Wininger, A. E., Bhatti, F., et al. (2019) · Scientific Reports · doi:10.1038/s41598-019-47695-3 · Cited by 40 · see citing works
Activation of p38 mitogen-activated protein kinase by norepinephrine in T-lineage cells
LaJevic, M. D., Suleiman, S., Cohen, R. L., & Chambers, D. A. (2010) · Immunology · doi:10.1111/j.1365-2567.2010.03354.x · Cited by 40 · see citing works
Higher Psychological and Psychovegetative Strain in Adolescents with Atypical Pigment Naevi
Trapp, M., Egger, J. W., Kapfhammer, H., Trapp, E.-M., Rohrer, P., Hörlesberger, N., Schwantzer, G., Komericki, P., Linder, M., Lvov, A. N., et al. (2015) · Acta Dermato Venereologica · doi:10.2340/00015555-1837 · Cited by 39 · see citing works
Ding, X., Zhao, X., Yang, T., Zhong, W., Fan, Q., Diao, J., Liu, Y., Chen, Y., Chen, J., & Lv, Z. (2014) · Evidence-based Complementary and Alternative Medicine · doi:10.1155/2014/605914 · Cited by 36 · see citing works
Chronic restraint stress modulates expression of genes in murine spleen
Yin, D., Zhang, Y., Stuart, C. A., Miao, J., Zhang, Y., Li, C., Zeng, X. R., Hanley, G., Moorman, J. P., Yao, Z., et al. (2006) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2006.05.004 · Cited by 35 · see citing works
“The proportion of CD4 and CD8 double positive thymocytes are more sensitive to stress, indicating that the increased apoptosis mainly impact cells of the immature phenotype (Dominguez-Gerpe and Rey-Mendez, 2001).”
BackgroundDifferential Effects of Physical and Psychological Stressors on Immune Functions of Rats
Oishi, K., Nishio, N., Konishi, K., Shimokawa, M., Okuda, T., Kuriyama, T., & Machida, K. (2003) · Stress · doi:10.1080/1025389031000101330 · Cited by 34 · see citing works
“The changes in the mitogeninduced lymphocyte proliferation response resulting from the psychological stressors might also be influenced by the stress-induced alterations in splenic lymphocyte subsets (Domı́nguez-Gerpe and Rey-Méndez, 2001).”
BackgroundThe effects of chronic stress on thymus innervation in the adult rat
Zivkovic, I. P., Rakin, A. K., Petrovic‐Djergovic, D., Miljković, B., & Mićić, M. (2005) · Acta Histochemica · doi:10.1016/j.acthis.2004.11.002 · Cited by 33 · see citing works
Song, M., Wang, C., Yang, H., Chen, Y., Feng, X., Li, B., & Fan, H. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2020.00680 · Cited by 30 · see citing works
Electroacupuncture suppresses surgical trauma stress-induced lymphocyte apoptosis in rats
Wang, J., Wang, Y., Yu, J. M., Cao, X.-D., & Wu, G.-C. (2005) · Neuroscience Letters · doi:10.1016/j.neulet.2005.03.068 · Cited by 29 · see citing works
“Researchesin several laboratories have shown that lymphopenia observed after exposure to stress in fact due to the induction of apoptosis [ 1 ,7,21].”
BackgroundEffects of lactoferrin on the immune response modified by the immobilization stress.
Zimecki, M., Artym, J., Chodaczek, G., Kocięba, M., & Kruzel, M. L. (2005) · PubMed · Cited by 28 · see citing works
Exposure to forced swim stress alters morphofunctional characteristics of the rat thymus
Zivkovic, I. P., Rakin, A. K., Petrovic‐Djergovic, D., Kosec, D. J., & Mićić, M. (2005) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2004.11.002 · Cited by 26 · see citing works
Zanos, P., Georgiou, P., Gonzalez, L. R., Hourani, S. M. O., Chen, Y., Kitchen, I., Kieffer, B. L., Winsky‐Sommerer, R., & Bailey, A. (2016) · The International Journal of Neuropsychopharmacology · doi:10.1093/ijnp/pyw011 · Cited by 26 · see citing works
“Twenty-four hours following the last behavioral test (ie, FST), mice were euthanized by 30-second exposure to CO2 followed by decapitation and spleen was weighed for peripheral assessment of stress (Kyo et al., 1999; Dominguez-Gerpe and Rey-Mendez, 2001).”
BackgroundMethodInfluentialSforcin, J. M. (2009) · Journal of ApiProduct and ApiMedical Science · doi:10.3896/ibra.4.01.1.05 · Cited by 23 · see citing works
Engler-Chiurazzi, E. B. (2024) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2024.1360242 · Cited by 24 · see citing works
Sarjan, H. N., & Yajurvedi, H. N. (2018) · Immunology Letters · doi:10.1016/j.imlet.2018.02.008 · Cited by 22 · see citing works
Lesher, A. P., Li, B., Whitt, P. B., Newton, N. H., Devalapalli, A. P., Shieh, K., Solow, J. S., & Parker, W. (2006) · Immunology and Cell Biology · doi:10.1111/j.1440-1711.2006.01440.x · Cited by 22 · see citing works
The Role of Toll-Like Receptor 9 in Chronic Stress-Induced Apoptosis in Macrophage
Xiang, Y., Yan, H. M., Zhou, J., Zhang, Q., Hanley, G., Caudle, Y., LeSage, G., Zhang, X., & Yin, D. (2015) · PLoS ONE · doi:10.1371/journal.pone.0123447 · Cited by 22 · see citing works
“Numerous studies have revealed that chronic stress leads to a decrease of thymocytes and splenocytes by a mechanism associated with stress-induced lymphocyte apoptosis [4, 5].”
BackgroundEstruel‐Amades, S., Ruíz-Iglesias, P., Périz, M., Franch, À., Pérez-Cano, F. J., Camps‐Bossacoma, M., & Castell, M. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2019.01491 · Cited by 21 · see citing works
“, 2018), which induce the downregulation of adhesion molecules producing lymphocyte demargination and release from reserve pools such as the spleen among other secondary lymphoid organs (Nielsen et al., 1997; Domínguez-Gerpe and Rey-Méndez, 2001; Krüger and Mooren, 2007; Krüger et al., 2008).”
BackgroundInnate and adaptive immune system consequences of post-traumatic stress disorder
Lauten, T. H., Natour, T., & Case, A. J. (2024) · Autonomic Neuroscience · doi:10.1016/j.autneu.2024.103159 · Cited by 21 · see citing works
“For example, when utilizing restraint stress, investigators observed reductions in the number of lymphocytes in the spleen and mesentery as well as levels of circulating antibodies after an immune challenge (Fukui et al., 1997; Domínguez-Gerpe and Rey-M ´ endez, 2001).”
Estrogen, the Peripheral Immune System and Major Depression – A Reproductive Lifespan Perspective
Engler-Chiurazzi, E. B., Chastain, W. H., Citron, K. K., Lambert, L. E., Kikkeri, D. N., & Shrestha, S. S. (2022) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.850623 · Cited by 20 · see citing works
Sarjan, H. N., & Yajurvedi, H. N. (2018) · Immunobiology · doi:10.1016/j.imbio.2018.09.007 · Cited by 20 · see citing works
Scientific and Regulatory Policy Committee Review
Fikes, J. D., Patrick, D. J., Francke, S., Frazier, K. S., Reindel, J. F., Romeike, A., Spaet, R. H., Tomlinson, L., & Schafer, K. A. (2015) · Toxicologic Pathology · doi:10.1177/0192623315596382 · Cited by 19 · see citing works
Sexual dimorphism during integrative endocrine and immune responses to ionizing radiation in mice
Burke, M., Wong, K., Talyansky, Y., Mhatre, S. D., Mitchell, C., Juran, C. M., Olson, M., Iyer, J. S., Puukila, S., Tahimic, C. G. T., et al. (2024) · Scientific Reports · doi:10.1038/s41598-023-33629-7 · Cited by 16 · see citing works
“Chronic physiological stress can influence thymus and spleen cellularity and weights 26 .”
BackgroundClipperton‐Allen, A. E., Ingrao, J. C., Ruggiero, L., Batista, L., Ovari, J., Hammermueller, J., Armstrong, J. N., Bienzle, D., Choleris, E., & Turner, P. V. (2015) · PubMed Central · Cited by 16 · see citing works
Stress Determined through Heart Rate Variability Predicts Immune Function
Hong, L., Wei, J., Yasin, Y., Wu, S. J., Barszczyk, A., Feng, Z., & Lee, K. (2019) · NeuroImmunoModulation · doi:10.1159/000500863 · Cited by 14 · see citing works
Duffy, H. B. D., & Roth, T. L. (2020) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2020.594244 · Cited by 14 · see citing works
Group B streptococcus toxic shock-like syndrome in a healthy woman: a case report.
Begley, J. S., & Barnes, R. C. (2007) · PubMed · Cited by 14 · see citing works
Sympathetic nervous system mediates surgical trauma stress-induced splenocyte apoptosis in rats
Wang, J., Sun, J., Yu, J. M., Cao, X.-D., Wang, Y., & Wu, G.-C. (2007) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2007.02.030 · Cited by 11 · see citing works
Ibrahim, A., Mahmoud, U. T., Khalil, N. S. A., Hussein, H. A., & Ali, M. M. (2017) · Journal of Veterinary Behavior · doi:10.1016/j.jveb.2017.10.011 · Cited by 10 · see citing works
On race, human variation, and who gets and dies of sepsis
Brinkworth, J. F., & Shaw, J. G. (2022) · American Journal of Biological Anthropology · doi:10.1002/ajpa.24527 · Cited by 9 · see citing works
“…white blood cells (B cells, T cells, and natural killer cells) drop, and cells produced often show altered cytotoxic and proliferative abilities (Dominguez-Gerpe & Rey-Mendez, 2001; Fleshner et al., 1989; Glaser et al., 1986; Irwin et al., 1990; Regnier & Kelley, 1981; Wyman et al., 2007).”
BackgroundDivyashree, S., Sarjan, H. N., & Yajurvedi, H. N. (2015) · Canadian Journal of Zoology · doi:10.1139/cjz-2015-0150 · Cited by 10 · see citing works
“2013), thymus (Dominguez-Gerpe and Rey-Méndez 2001; Zivkovic et al. 2005), and lymphnodes (Fukui et al.”
BackgroundEbokaiwe, A. P., Olasehinde, O., Chimezie, I. P., Ushang, O. R., Nvene, C., & Faith, E. (2023) · Biological Trace Element Research · doi:10.1007/s12011-023-03752-7 · Cited by 7 · see citing works
“Several investigators have used these endpoints to evaluate possible effects on immune function [46–48].”
Spleen tissue changes after restraint stress: effects of aerobic exercise training
Feriani, D. J., Sousa, A. S., Delbin, M. A., Ruberti, O. M., Crestani, C. C., & Rodrigues, B. (2021) · Stress · doi:10.1080/10253890.2021.1895112 · Cited by 7 · see citing works
“…morphology and immune cell subsets in the spleen, as well as to cause apoptosis of splenic lymphocytes (Cao et al., 2014; Dom ınguez-Gerpe & Rey-M endez, 2001; CONTACT Bruno Rodrigues prof.brodrigues@gmail.com Laboratory of Cardiovascular Investigation and Exercise (LICE), School of Physical…”
BackgroundOrekhova, N. A., & Modorov, M. V. (2016) · Stress · doi:10.1080/10253890.2016.1206883 · Cited by 6 · see citing works
“Other manifestations of the stress reaction include hypocellularity of the lymphoid tissue, the spleen in particular (Dominguez-Gerpe & Rcy-Mcmlez, 2001; Satoh et al., 2006), and our study also showed a decreased protein content and DNA/total protein ratio with increasing population size.”
BackgroundDoes caffeine reverse the EAC cell-induced immune suppression?
Mandal, A., & Poddar, M. K. (2007) · Journal of Pharmacy and Pharmacology · doi:10.1211/jpp.59.7.0013 · Cited by 6 · see citing works
“However, no significant change was observed in blood lymphocyte cytotoxicity under the present experimental condition (Figure 1B), possibly due to the alteration of T cell subsets in different compartments of the body under stressful condition (Lourdes & Manuel 2001).”
BackgroundZimecki, M., Artym, J., Kocięba, M., Zaczyńska, E., Kaleta‐Kuratewicz, K., Madej, J. P., Kuropka, P., Zambrowicz, A., & Bobak, Ł. (2025) · Frontiers in Bioscience-Landmark · doi:10.31083/fbl27949 · Cited by 4 · see citing works
“Generally, the T cell lym-phopoiesis during acute psychic stress is much more affected than that of B cells [9,12,13] and delayed type hypersensitivity reactions are preferentially inhibited in comparison to the humoral immune response [10,14–17].”
Таллерова, А. В., Коваленко, Л. П., Кузнецова, О. С., Дурнев, А. Д., & Середенин, С. Б. (2014) · Bulletin of Experimental Biology and Medicine · doi:10.1007/s10517-014-2343-1 · Cited by 4 · see citing works
Jongman, E. C., Rice, M., Campbell, A. J. D., Butler, K. L., & Hemsworth, P. H. (2016) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2016.10.015 · Cited by 4 · see citing works
Domínguez‐Gerpe, L. (2007) · Immunobiology · doi:10.1016/j.imbio.2007.04.005 · Cited by 4 · see citing works
Self-citationZhao, Q., Wang, J., Ma, F., Chen, Q., Liu, H., Yang, J., Chen, S., Tang, Y., Mi, S., Wang, L., et al. (2025) · Journal of Animal Science and Biotechnology/Journal of animal science and biotechnology · doi:10.1186/s40104-025-01184-y · Cited by 3 · see citing works
“The immune organs of pigs are the tissue structures that carry out the immune function of the pig’s body, including primary immune organs (bone marrow, thymus) and secondary immune organs (blood, spleen, lymph node) [47, 48].”
Cho, J., Bing, S. J., Kim, A., Herath, K. H. I. N. M., Ahn, G., & Jee, Y. (2019) · Molecular Biology Reports · doi:10.1007/s11033-019-04899-0 · Cited by 3 · see citing works
Zolotova, N. A., Цветков, И. С., Khochanskiy, D. N., Dzhalilova, D. S., Kosyreva, A. M., Mikhaylova, A. L., Михайлова, Л. П., & Makarova, O. V. (2020) · CLINICAL AND EXPERIMENTAL MORPHOLOGY · doi:10.31088/cem2020.9.4.50-64 · Cited by 4 · see citing works
Aghajani, M., Mahdavi, M. R. V., Najafabadi, M. K., Ghazanfari, T., Moradi, F., Golchoobian, R., Askari, H., Sanadgol, N., & Moghaddam, E. K. (2017) · NeuroImmunoModulation · doi:10.1159/000480732 · Cited by 4 · see citing works
Čulig, L., Kashyap, A., Kuribayashi, W., Claybourne, Q. C., & Beerman, I. (2025) · GeroScience · doi:10.1007/s11357-025-01793-5 · Cited by 2 · see citing works
“Lastly, T-cell function and repertoire decline with age in both mice and humans [17], while exposure to chronic stress increases their proportion in mouse blood [12].”
Harrison, M., Adebayo, J. O., Mills-Widemon, A., Ikuejamoye-Omotore, S. J., Estrada-Reyes, Z. M., Ogunade, I. M., Pech-Cervantes, A. A., Terrill, T. H., Siddique, A., & Ruíz-González, A. (2025) · Frontiers in Animal Science · doi:10.3389/fanim.2025.1631531 · Cited by 2 · see citing works
Immunity in Rodent Models of Stress
Hachenberg, S., Russo, S. J., & Cathomas, F. (2025) · Biological Psychiatry · doi:10.1016/j.biopsych.2025.11.007 · Cited by 2 · see citing works
de Amorim, G. A., Carvalho, N. S., & Pagliusi, M. (2026) · Brain Behavior and Immunity Integrative · doi:10.1016/j.bbii.2026.100176 · Cited by 2 · see citing works
Arifah, S., & Purwanti, O. S. (2008) · DOAJ (DOAJ: Directory of Open Access Journals) · doi:10.23917/bik.v1i3.3745 · Cited by 2 · see citing works
Vanroy, T., Catfolis, B., Verbrugghe, E., Verheyen, K., Lens, L., Strubbe, D., Pasmans, F., Martel, A., Croubels, S., Cherlet, M., et al. (2025) · Experimental Parasitology · doi:10.1016/j.exppara.2025.108999 · Cited by 1 · see citing works
A weight of evidence evaluation on the immunosuppressive potential of xylene
Morris‐Schaffer, K., Kocabaş, N. A., Hearon, S. E., Higgins, L. G., Dahlberg, S., Faulhammer, F., Freeman, E. L., Cubello, J., & Rooseboom, M. (2026) · Regulatory Toxicology and Pharmacology · doi:10.1016/j.yrtph.2026.106082 · Cited by 1 · see citing works
Prakash Babu, B., Hemalatha, B., & Henry, T. (2018) · Journal of Anatomical Society of India · doi:10.1016/j.jasi.2018.11.007 · Cited by 1 · see citing works
El‐Tahawy, N. F. G., & Ali, A. H. S. A. (2020) · The Egyptian Journal of Histology · doi:10.21608/ejh.2020.24673.1253 · Cited by 1 · see citing works
“This was in agreement with Domínguez-Gerpe and his co-worker[38] who proved that in general, T cells are more affected than B cells when exposed to stress.”
ResultPearse, G. (2017) · Molecular and integrative toxicology · doi:10.1007/978-3-319-47385-7_1 · Cited by 1 · see citing works
CIRCADIAN DISRUPTION AS A FACTOR OF IMPAIRED ADAPTIVE T-CELL IMMUNITY RESPONSE
Gevorkyan, A. R., Ippolitov, D., & Бочарова, Т. В. (2022) · PROBLEMS OF ENDOCRINE PATHOLOGY · doi:10.21856/j-pep.2022.1.10 · Cited by 1 · see citing works
Efeito da própolis sobre parâmetros imunológicos de camundongos Balb/c submetidos a estresse crônico
Missima, F. (2005) · Americanae (AECID Library) · Cited by 1 · see citing works
Normal Lymphocyte Subpopulation of the Spleen is Altered after Peripheral Nerve Injury in Mice
Yoo, J. H., Song, H.-K., Jeong, D. C., & Bae, D. H. (2007) · Korean Journal of Anesthesiology · doi:10.4097/kjae.2007.53.6.s42
The role of platelets in lymphocyte recruitment during liver inflamation
Robinson, J. A. (2016) · University of Birmingham Institutional Research Archive (University of Birmingham)
KOÇKAYA, M. (2017) · Atatürk Üniversitesi Veteriner Bilimleri Dergisi · doi:10.17094/ataunivbd.309769
Effect of classical conditioning over immature and mature B lymphocytes regulation
Bustos, H. R., Espinoza‐Navarro, O., & Castro, M. E. (2018) · Microscopy Research and Technique · doi:10.1002/jemt.23112
Taborda‐Barata, L. (2019) · Springer eBooks · doi:10.1007/978-3-030-30734-9_10
Chronic stress and ageing : effects on immune function
Vitlić, A. (2014) · University of Birmingham Institutional Research Archive (University of Birmingham)
Gonchar, D. I., Shmigol, T. A., Lyakhmun, D. N., Soloveva, A., Yankovskaya, S. K., Krendeleva, O. V., Vizgalina, V. D., Efimova, E. V., Ezdoglian, A. A., Kiseleva, N. M., et al. (2026) · Biomedicines · doi:10.3390/biomedicines14020356
Gou, X., Lei, Y., Yang, B., Zhou, W., Chen, X., Yan, K., Zhang, Q., Zheng, H., Deng, L., Guo, T., et al. (2026) · International Journal of Molecular Sciences · doi:10.3390/ijms27041919
“This immunosuppressive effect is also evident at the organ level: chronic restraint stress also causes structural alterations in the spleen, including expansion of the white pulp, degeneration of the red pulp, and reduced spleen index [14,15].”
Kranz, E. O., Bather, J. R., Feng, S., Zhang, X., Crump, A. A., Cole, S. W., & Cuevas, A. G. (2026) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2026.107945
Lafuse, W. P., & Rajaram, M. V. S. (2026) · Cells · doi:10.3390/cells15151356
“Chronic immobilization stress in mice induces thymic atrophy, reduces thymocyte numbers, and increases thymocyte apop-https://doi.org/10.3390/cells15151356 tosis, with immature thymocytes being particularly affected [57].”
InfluentialEfeito de leucotrienos sobre o estado de ativação de macrófagos de camundongos estressados
Nunes, G. A. (2005) · Americanae (AECID Library)
Missima, F. (2009) · Americanae (AECID Library)
- Authors
- Domínguez-Gerpe, L., & Rey-Méndez, M.
- Venue
- BMC Immunology
- Published
- 2001-07-31
- Volume
- 2
- Issue
- 1
- Pages
- 7-7
- ISSN
- 1471-2172 (ISSN-L)
- PMC
- PMC37547
- OpenAlex
- W1538345593
- Cited by
- 85
- References
- 37
- Citations by year
- 2026: 7 · 2025: 6 · 2024: 4 · 2023: 2 · 2022: 3 · 2021: 1 · 2020: 5 · 2019: 6 · 2018: 4 · 2017: 5 · 2016: 6 · 2015: 5 · 2014: 4 · 2013: 2
- FWCI
- 0.31
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- BMC Immunology (publishedVersion)
- PubMed Central (publishedVersion, other-oa)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Universidade de Santiago de Compostela
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Health Sciences › Medicine › Psychiatry and Mental health › Cancer, Stress, Anesthesia, and Immune Response
- Life Sciences › Immunology and Microbiology › Immunology › Immunotoxicology and immune responses
- Keywords
- chronic stress, restraint stress, immunosuppression, lymphocyte subsets, thymocyte apoptosis, thymus, T cell subsets, B cells, spleen, lymph nodes, bone marrow, lymphoid organs, stress disorders
- MeSH terms
- Animals, Blood Cells, Bone Marrow Cells, Immobilization, Lymph Nodes, Mice, Inbred C57BL, Spleen, Stress, Physiological, Thymus Gland, Lymphocyte Subsets, T-Lymphocyte Subsets, Mice
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
