Bone marrow and peripheral white blood cells number is affected by sleep deprivation in a murine experimental model
Abstract
Sleep deficit and related disorders are becoming increasingly prevalent in modern life and an extensive literature has documented that acute or chronic sleep deprivation can lead to several physiological consequences. Here, we evaluated the effects of sleep deprivation on hematopoietic composition of either bone marrow or peripheral blood. Mice were subjected to paradoxical sleep deprivation (PSD) for 72 h by modified multiple platform method, with or without an additional sleep recovery (SR) period of 10 days. PSD decreased total cellularity of the bone marrow and peripheral blood concomitantly. Subsequent analysis of cell composition showed that absolute number of hematopoietic stem/progenitor cells and colony‐forming units was decreased. Moreover, the absolute number of granulocytes and monocytes in bone marrow was reduced in PSD group. These alterations were paralleled by an accumulation of neutrophils and monocytes in peripheral blood. PSD also induced lymphopenia in the circulation. To the best of our knowledge, this is the first study that demonstrates the importance of sleep on the hematopoietic microenvironment and provides new insights into the relationship between sleep and the immune system. J. Cell. Physiol. 227: 361–366, 2012. © 2011 Wiley Periodicals, Inc.
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In patients with Epstein Barr virus-linked infectious mononucleosis, self-reported sleep duration was markedly increased and debilitating daytime sleepiness persisted over many years.
“In patients with an infectious illness linked to the Epstein Barr virus (EBV), such as infectious mononucleosis, self-reported sleep duration was markedly increased (349) and debilitating daytime sleepiness persisted over many years (218).”
From The Sleep-Immune Crosstalk in Health and Disease (2019) · cites this paper as [218]
Cites
Impact of sleep debt on metabolic and endocrine function
Spiegel, K., Leproult, R., & Van Cauter, E. (1999) · The Lancet · doi:10.1016/s0140-6736(99)01376-8 · Cited by 3,668 · see citing works
Signals from the Sympathetic Nervous System Regulate Hematopoietic Stem Cell Egress from Bone Marrow
Katayama, Y., Battista, M., Kao, W.-M., Hidalgo, A., Peired, A. J., Thomas, S. A., & Frenette, P. S. (2006) · Cell · doi:10.1016/j.cell.2005.10.041 · Cited by 1,412 · see citing works
Haematopoietic stem cell release is regulated by circadian oscillations
Méndez‐Ferrer, S., Lucas, D., Battista, M., & Frenette, P. S. (2008) · Nature · doi:10.1038/nature06685 · Cited by 1,310 · see citing works
Clues to the functions of mammalian sleep
Siegel, J. M. (2005) · Nature · doi:10.1038/nature04285 · Cited by 1,040 · see citing works
Effects of sleep and circadian rhythm on human circulating immune cells
Born, J., Lange, T., Hansen, K., Mölle, M., & Fehm, H. L. (1997) · The Journal of Immunology · doi:10.4049/jimmunol.158.9.4454 · Cited by 611 · see citing works
Sick and tired: does sleep have a vital role in the immune system?
Bryant, P. A., Trinder, J., & Curtis, N. (2004) · Nature Reviews Immunology · doi:10.1038/nri1369 · Cited by 551 · see citing works
Catecholamine-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
Partial night sleep deprivation reduces natural killer and celhdar immune responses in humans
Irwin, M., McClintick, J., Costlow, C., Fortner, M., White, J., & Gillin, J. C. (1996) · The FASEB Journal · doi:10.1096/fasebj.10.5.8621064 · Cited by 480 · see citing works
Cortisol and epinephrine control opposing circadian rhythms in T cell subsets
Dimitrov, S., Benedict, C., Heutling, D., Westermann, J., Born, J., & Lange, T. (2009) · Blood · doi:10.1182/blood-2008-11-190769 · Cited by 368 · see citing works
Effects of sleep and sleep loss on immunity and cytokines
Irwin, M. R. (2002) · Brain Behavior and Immunity · doi:10.1016/s0889-1591(02)00003-x · Cited by 366 · see citing works
Dinges, D. F., Douglas, S. D., Zaugg, L., Campbell, D. E., McMann, J. M., Whitehouse, W. G., Orne, E. C., Kapoor, S. C., Icaza, E., & Orne, M. T. (1994) · Journal of Clinical Investigation · doi:10.1172/jci117184 · Cited by 361 · see citing works
Sleep Enhances the Human Antibody Response to Hepatitis A Vaccination
Lange, T., Perras, B., Fehm, H. L., & Born, J. (2003) · Psychosomatic Medicine · doi:10.1097/01.psy.0000091382.61178.f1 · Cited by 351 · see citing works
Nakahata, T., & Ogawa, M. (1982) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.79.12.3843 · Cited by 309 · see citing works
Role of hippocampal oxidative stress in memory deficits induced by sleep deprivation in mice
Silva, R. H., Abílio, V. C., Takatsu, A. L., Kameda, S. R., Grassl, C., Chehin, A. B., Medrano, W. A., Calzavara, M. B., Registro, S., Andersen, M. L., et al. (2004) · Neuropharmacology · doi:10.1016/j.neuropharm.2003.11.032 · Cited by 307 · see citing works
Self-citationEpidemiological evidence for the links between sleep, circadian rhythms and metabolism
Gangwisch, J. E. (2009) · Obesity Reviews · doi:10.1111/j.1467-789x.2009.00663.x · Cited by 263 · see citing works
Andersen, M. L., Martins, P. J. F., D’Almeida, V., Bignotto, M., & Tufik, S. (2005) · Journal of Sleep Research · doi:10.1111/j.1365-2869.2004.00428.x · Cited by 246 · see citing works
Self-citationSleep deprivation and human immune function
Dinges, D. F., Douglas, S. D., Hamarman, S., Zaugg, L., & Kapoor, S. C. (1995) · Advances in Neuroimmunology · doi:10.1016/0960-5428(95)00002-j · Cited by 234 · see citing works
Engler, H., Bailey, M. T., Engler, A., & Sheridan, J. F. (2004) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2003.11.011 · Cited by 209 · see citing works
Does REM Sleep Deprivation Induce a Supersensitivity of Dopaminergic Receptors in the Rat Brain?
Tufik, S., Lindsey, C. J., & Carlini, E. A. (2008) · Pharmacology · doi:10.1159/000136753 · Cited by 209 · see citing works
Self-citationShift Work, Jet Lag, and Female Reproduction
Mahoney, M. M. (2010) · International Journal of Endocrinology · doi:10.1155/2010/813764 · Cited by 209 · see citing works
Lord, K. A., Abdollahi, A., Hoffman-Liebermann, B., & Liebermann, D. A. (1993) · Molecular and Cellular Biology · doi:10.1128/mcb.13.2.841 · Cited by 199 · see citing works
The relevance of sleep abnormalities to chronic inflammatory conditions
Ranjbaran, Z., Keefer, L., Stepanski, E. J., Farhadi, A., & Keshavarzian, A. (2007) · Inflammation Research · doi:10.1007/s00011-006-6067-1 · Cited by 191 · see citing works
Murine hematopoietic stem and progenitor cells: I. Enrichment and biologic characterization
Li, C., & Johnson, G. (1995) · Blood · doi:10.1182/blood.v85.6.1472.bloodjournal8561472 · Cited by 162 · see citing works
Alteration of sleep in rabbits by Staphylococcus aureus infection
Toth, L. A., & Krueger, J. M. (1988) · Infection and Immunity · doi:10.1128/iai.56.7.1785-1791.1988 · Cited by 159 · see citing works
Sleep and Host Defenses: A Review
Benca, R. M., & Quintáns, J. (1997) · SLEEP · doi:10.1093/sleep/20.11.1027 · Cited by 157 · see citing works
Nunes, G. P., Tufik, S., & Nóbrega, J. N. (1994) · Brain Research Bulletin · doi:10.1016/0361-9230(94)90018-3 · Cited by 128 · see citing works
Self-citationTelomere length and proliferation potential of hematopoietic stem cells
Lansdorp, P. M. (1995) · Journal of Cell Science · doi:10.1242/jcs.108.1.1 · Cited by 116 · see citing works
Sleep quality and motor vehicle crashes in adolescents.
Pizza, F., Contardi, S., Antognini, A. B., Zagoraiou, M., Borrotti, M., Mostacci, B., Mondini, S., & Cirignotta, F. (2010) · Journal of clinical sleep medicine : JCSM : official publication of the American Academy of Sleep Medicine · doi:10.5664/jcsm.27708 · Cited by 116 · see citing works
Alvarenga, T. A., Patti, C. L., Andersen, M. L., Silva, R. H., Calzavara, M. B., Lopez, G. B., Frussa‐Filho, R., & Tufik, S. (2008) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2008.07.013 · Cited by 96 · see citing works
Self-citationEffects of 48 hours sleep deprivation on human immune profile.
Öztürk, L., Pelin, Z., Karadeniz, D., Kaynak, H., Cakar, L., & Gözükırmızı, E. (1999) · PubMed · Cited by 86 · see citing works
Light-Mediated Perturbations of Circadian Timing and Cancer Risk: A Mechanistic Analysis
Reiter, R. J., Tan, D. X., Erren, T. C., Fuentes‐Broto, L., & Paredes, S. D. (2009) · Integrative Cancer Therapies · doi:10.1177/1534735409352026 · Cited by 74 · see citing works
Perry, J. C., D’Almeida, V., Souza, F. G., Schoorlemmer, G. H. M., Colombari, E., & Tufik, S. E. R. (2006) · Respiratory Physiology & Neurobiology · doi:10.1016/j.resp.2006.10.004 · Cited by 66 · see citing works
Self-citationZager, A., Andersen, M. L., Lima, M. M. S., Reksidler, A. B., Machado, R. B., & Tufik, S. (2009) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2009.03.005 · Cited by 63 · see citing works
Self-citationLancel, M., Crönlein, J., Müller-Preuss, P., & Holsboer, F. (1995) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1995.268.5.r1310 · Cited by 63 · see citing works
Dynamic norepinephrine alterations in bone marrow: evidence of functional innervation
Tang, Y., Shankar, R., Gamelli, R. L., & Jones, S. B. (1999) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(99)00032-6 · Cited by 55 · see citing works
Characterization of peripheral blood stem cells in mice
Yamamoto, Y., Yasumizu, R., Amou, Y., Watanabe, N., Nishio, N., Toki, J., Fukuhara, S., & Ikehara, S. (1996) · Blood · doi:10.1182/blood.v88.2.445.bloodjournal882445 · Cited by 47 · see citing works
A Reassessment of the Hyperphagia/Weight-Loss Paradox During Sleep Deprivation
Martins, P. J. F., D’Almeida, V., Nóbrega, J. N., & Tufik, S. (2006) · SLEEP · doi:10.1093/sleep/29.9.1233 · Cited by 47 · see citing works
Self-citationHipólide, D. C., Tufik, S., Raymond, R., & Nóbrega, J. N. (1998) · Neuroscience · doi:10.1016/s0306-4522(98)00067-0 · Cited by 45 · see citing works
Self-citationSleep changes induced by lipopolysaccharide in the rat are influenced by age
Schiffelholz, T., & Lancel, M. (2001) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.2001.280.2.r398 · Cited by 42 · see citing works
Ciriza, J., & García‐Ojeda, M. E. (2010) · Stem Cell Research & Therapy · doi:10.1186/scrt14 · Cited by 36 · see citing works
Increased plasma homocysteine levels in shift working bus drivers
Martins, P. J. F., D’Almeida, V., Vergani, N., Pérez, A. B. A., & Tufík, S. (2003) · Occupational and Environmental Medicine · doi:10.1136/oem.60.9.662 · Cited by 34 · see citing works
Catecholaminergic Regulation of Hematopoiesis in Mice
Maestroni, G. J. M. (1998) · Blood · doi:10.1182/blood.v92.8.2971 · Cited by 22 · see citing works
Burdach, S. E. G. (1991) · Klinische Pädiatrie · doi:10.1055/s-2007-1025445 · Cited by 11 · see citing works
Shoham, S., Ahokas, R. A., Blatteis, C. M., & Krueger, J. M. (1987) · Brain Research · doi:10.1016/0006-8993(87)90587-7 · Cited by 10 · see citing works
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Besedovsky, L., Lange, T., & Haack, M. (2019) · Physiological Reviews · doi:10.1152/physrev.00010.2018 · Cited by 1,479 · see citing works
“Other rodent studies found an increase in numbers of leukocytes and lymphocytes in the blood after normal sleep compared with forced wakefulness, whereas there were no changes in cell numbers in the lymph nodes, spleen, or bone marrow (171, 217, 596, 597).”
Liu, H., Huang, X., Li, Y., Xi, K., Han, Y., Mao, H., Ren, K., Wang, W., & Wu, Z. (2021) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2021.12.006 · Cited by 99 · see citing works
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De Lorenzo, B. H. P., de Oliveira Marchioro, L., Greco, C. R., & Suchecki, D. (2015) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2015.04.006 · Cited by 85 · see citing works
Chronically inadequate sleep results in abnormal bone formation and abnormal bone marrow in rats
Everson, C. A., Folley, A. E., & Toth, J. M. (2012) · Experimental Biology and Medicine · doi:10.1258/ebm.2012.012043 · Cited by 78 · see citing works
Oxidative stress, cancer, and sleep deprivation: is there a logical link in this association?
Noguti, J., Andersen, M. L., Cirelli, C., & Ribeiro, D. A. (2013) · Sleep And Breathing · doi:10.1007/s11325-012-0797-9 · Cited by 75 · see citing works
Chronic Sleep Restriction Impairs the Antitumor Immune Response in Mice
Lorenzo, B. H. P. D., Brito, R. R. N. E., Leal, T. P., Garcia, N. P., dos Santos, R. M. M., Alvares-Saraiva, A. M., Hurtado, E. C. P., dos Reis, T. C. B., & Palma, B. D. (2018) · NeuroImmunoModulation · doi:10.1159/000490352 · Cited by 58 · see citing works
Effect of sleep loss on pain—New conceptual and mechanistic avenues
Kourbanova, K., Alexandre, C., & Latrémolière, A. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.1009902 · Cited by 56 · see citing works
Jim, H., Evans, B., Jeong, J. M., Gonzalez, B. D., Johnston, L., Nelson, A. M., Kesler, S. R., Phillips, K. M., Barata, A., Pidala, J., et al. (2014) · Transplantation and Cellular Therapy · doi:10.1016/j.bbmt.2014.04.010 · Cited by 55 · see citing works
Sleep disruption impairs haematopoietic stem cell transplantation in mice
Rolls, A., Pang, W. W., Ibarra, I., Colas, D., Bonnavion, P., Korin, B., Heller, H. C., Weissman, I. L., & de Lecea, L. (2015) · Nature Communications · doi:10.1038/ncomms9516 · Cited by 48 · see citing works
Pellegrino, R., Sunaga, D. Y., Guindalini, C., Martins, R. C. S., Mazzotti, D. R., Wei, Z., Daye, Z. J., Andersen, M. L., & Tufik, S. (2012) · Physiological Genomics · doi:10.1152/physiolgenomics.00058.2012 · Cited by 42 · see citing works
Self-citationDedeepiya, V. D., Rao, Y. Y., Jayakrishnan, G. A., Parthiban, J., Subramani, B., Manjunath, S. R., Senthilkumar, R., & Abraham, S. J. (2012) · Bone Marrow Research · doi:10.1155/2012/787414 · Cited by 28 · see citing works
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Hahn, J. K., Günter, M., Schuhmacher, J., Bieber, K., Pöschel, S., Schütz, M., Engelhardt, B., Oster, H., Sina, C., Lange, T., et al. (2020) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2020.01.001 · Cited by 23 · see citing works
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Self-citationJim, H., Sutton, S. K., Majhail, N. S., Wood, W. A., Jacobsen, P. B., Wingard, J. R., Wu, J., Knight, J. M., Syrjala, K. L., & Lee, S. J. (2018) · Bone Marrow Transplantation · doi:10.1038/s41409-018-0138-0 · Cited by 16 · see citing works
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Sá-Nunes, A., Bizzarro, B., Egydio, F., Barros, M. S., Sesti-Costa, R., Soares, E. M., Pina, A., Russo, M., Faccioli, L. H., Tufik, S., et al. (2016) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2015.11.013 · Cited by 11 · see citing works
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Zhao, A. T., Holtzman, N. G., Golubić, M., & Pavletic, S. Z. (2024) · Transplantation and Cellular Therapy · doi:10.1016/j.jtct.2024.05.023 · Cited by 1 · see citing works
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Self-citation
- Authors
- Guariniello, L. D., Vicari, P., Lee, K. S., de Oliveira, A. C., & Tufik, S.
- Affiliations
- Universidade Federal de São Paulo (BR)
- Associação Fundo de Incentivo à Pesquisa (BR)
- Corresponding author
- Guariniello, Luciana Doria
- Venue
- Journal of Cellular Physiology
- Publisher
- Wiley
- Published
- 2011-10-24
- Volume
- 227
- Issue
- 1
- Pages
- 361-366
- ISSN
- 0021-9541 (ISSN-L)
- 1097-4652
- OpenAlex
- W2069388466
- Cited by
- 30
- References
- 44
- Citations by year
- 2024: 5 · 2022: 2 · 2021: 3 · 2020: 3 · 2019: 1 · 2018: 2 · 2017: 3 · 2015: 5 · 2014: 1 · 2013: 2 · 2012: 3
- FWCI
- 0.97
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Cellular Physiology (publishedVersion)
- PubMed (publishedVersion)
- UNIFESP Institutional Repository (Universidade Federal de São Paulo) (submittedVersion)
- Funders
- Fundação de Amparo à Pesquisa do Estado de São Paulo
- Conselho Nacional de Desenvolvimento Científico e Tecnológico
- Associação Fundo de Incentivo à Pesquisa
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Sleep and Work-Related Fatigue
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
- Keywords
- sleep deprivation, REM sleep deprivation, bone marrow, hematopoietic stem and progenitor cells, colony-forming units, granulocytes, monocytes, neutrophils, lymphopenia, sleep recovery, hematopoietic microenvironment, mice
- MeSH terms
- Animals, Bone Marrow Cells, Cell Separation, Disease Models, Animal, Flow Cytometry, Hematopoietic Stem Cells, Leukocyte Count, Leukocytes, Male, Mice, Inbred C57BL, Sleep Deprivation, Mice
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