The DOI matches its Crossref record; 45 of the 47 references it cites were found in a registry or an index.
Seasonal modulation of the circadian time structure of circulating T and natural killer lymphocyte subsets from healthy subjects.
Open accessAbstract
A seasonal modulation of the circadian time structure of circulating T and natural killer (NK) lymphocyte subtypes was documented in five healthy men aged 24-36 yr. Venous blood was obtained every 4 h for 24 h from each subject in January, March, June, August, and November 1984. Three subjects were also studied in April and/or August and/or November 1983 for the T subsets only. Mononuclear cells were isolated on Ficoll-Paque gradient and aliquots were incubated with OKT3, OKT4, OKT8, or HNK-1 monoclonal antibodies for characterizing all, T, T helper, T suppressor-cytotoxic, and NK lymphocytes, respectively, under an epifluorescence microscope. An effect of both sampling time and study month was statistically validated (P less than 0.01) with both two-way analysis of variance and cosinor for the peripheral counts in total, pan-T, T helper, and NK lymphocytes (cells per cubic millimeter). Seasonal changes affected both the circadian patterns and the 24-h mean values. Thus the double amplitude (total extent of variation) of the circadian rhythm in circulating total, T and T helper lymphocytes varied between 0 in March (P greater than 0.30; no rhythm) and up to 46-68% of the 24-h-mean (M) in November, with acrophases (times of maximum, 0) localized in the first half of the night (P less than 0.001). Maximal values were found at 8:30 h for both T suppressor-cytotoxic and NK lymphocytes; a smaller second peak was also found at 20:30 h, and a 12-h rhythm was validated by cosinor (P less than 0.0001), with no patient change in waveform along the year scale. A circannual rhythm was statistically validated by cosinor for total (0 in November), pan-T (0 in March), T suppressor-cytotoxic (0 in December), and NK lymphocytes (0 in October). A rhythm with a period equal to 6 mo was found for circulating T helper cells with 0 occurring both in April and October. Seasonal variations in the incidence of several immunologically related diseases may correspond to an endogenous circannual time structure.
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“However, in light of the low-to-normal total CD4+ and CD8+ T-cells, this apparent decline could also be explained by the low point of normal T-cell circannual kinetics at the 2-year follow-up [44].”
From Immune reconstitution and clinical recovery following anti-CD28 antibody (TGN1412)-induced cytokine storm (2021) · cites this paper as [44]
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“Over 2 years, T-cell subsets displayed circannual kinetics [44, 45], especially noted in the CD25+/CD28+ subsets, incorporating Tregs.”
From Immune reconstitution and clinical recovery following anti-CD28 antibody (TGN1412)-induced cytokine storm (2021) · cites this paper as [44]
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Cites
Methods for cosinor-rhythmometry.
Nelson, W. E., Tong, Y. L., Lee, J. K., & Franz Halberg, A. (1979) · PubMed · Cited by 1,701
A differentiation antigen of human NK and K cells identified by a monoclonal antibody (HNK-1).
Abo, T., & Balch, C. M. (1981) · The Journal of Immunology · doi:10.4049/jimmunol.127.3.1024 · Cited by 1,407
Abo, T., Cooper, M. D., & Balch, C. M. (1982) · The Journal of Immunology · doi:10.4049/jimmunol.129.4.1752 · Cited by 323
Chronobiology in hematology and immunology
Haus, E. L., LAKATUA, D. J., Swoyer, J., & Sackett-Lundeen, L. L. (1983) · American Journal of Anatomy · doi:10.1002/aja.1001680406 · Cited by 303
Abo, T., Kawate, T., Itoh, K., & Kumagai, K. (1981) · The Journal of Immunology · doi:10.4049/jimmunol.126.4.1360 · Cited by 243
Ritz, J., Nadler, L. M., Bhan, A. K., Notis-McConarty, J., Pesando, J. M., & Schlossman, S. F. (1981) · Blood · doi:10.1182/blood.v58.3.648.648 · Cited by 223
Circadian variation of lymphocyte subpopulations: a study with monoclonal antibodies.
Ritchie, A. W. S., Oswald, I., Micklem, H. S., Boyd, J. E., Elton, R. A., Jazwinska, E. C., & James, K. (1983) · BMJ · doi:10.1136/bmj.286.6380.1773 · Cited by 192
Lanier, L. L., Engleman, E. G., Gatenby, P. A., Babcock, G. F., Warner, N. L., & Herzenberg, L. A. (1983) · Immunological Reviews · doi:10.1111/j.1600-065x.1983.tb01088.x · Cited by 161
Reinberg, A., Lagoguey, M., Cesselin, F., Touitou, Y., Legrand, J.-C., Delassalle, A., Antreassian, J., & Lagoguey, A. (1978) · Acta Endocrinologica · doi:10.1530/acta.0.0880417 · Cited by 126
Circadian and seasonal rhythms in α- and β-adrenergic receptors in the rat brain
Kafka, M. S., Wirz‐Justice, A., & Naber, D. (1981) · Brain Research · doi:10.1016/0006-8993(81)90373-5 · Cited by 118
Flagged first, then by citations
2 of the 47 references couldn’t be matched to a known paper.
Research works printed but not linked: 2
- [12]12. Schwab, R. G. 1971. Circannian testicular periodicity in the European starling in the absence of photoperiodic change. In Biochronometry. Proceedings of a Symposium at the National Acad- emy of Sciences USA.
- [17]17. evi, F., C. Canon, Y. Touitou, J. Sulon, M. Mechkouri, E. Demey-Ponsart, J. P. Touboul, J. M. Vannetzel, I. Mowzowicz, A. Reinberg, and G. Mathe. 1988. Circadian and circahemidian rhythms in circulating T lymphocyte subtypes and plasma concentrations of testosterone, total and free cortisol in five healthy men. Clin. Exp. Immunoe. In press.
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Items 101–104 of 104
Raschke, F. (2000) · Springer eBooks · doi:10.1007/978-3-642-59756-5_29
Paul, D. (2025) · Springer eBooks · doi:10.1007/978-3-032-08808-6_12 · Cited by 2
Clocking immunity: circadian modulation of NK cells and emerging timing perspectives
Liu, K., Lv, X., & Wen, W. (2026) · Frontiers in Immunology · doi:10.3389/fimmu.2026.1739723
Miao (1999) · doi:10.1002/(sici)1097-0215(19991029)83:3
Metadata
- Authors
- Lévi, F. A., Canon, C., Touitou, Y., Reinberg, A., & Mathé, G.
- Affiliations
- Centre National de la Recherche Scientifique (FR)
- Pitié-Salpêtrière Hospital (FR)
- ORCID
- Venue
- Journal of Clinical Investigation
- Published
- 1988-02-01
- Volume
- 81
- Issue
- 2
- Pages
- 407-413
- ISSN
- 0021-9738 (ISSN-L)
- PMC
- PMC329583
- OpenAlex
- W1964130172
- Cited by
- 104
- References
- 47
- Citations by year
- 2026: 1 · 2025: 1 · 2023: 2 · 2022: 2 · 2021: 1 · 2020: 1 · 2019: 4 · 2018: 1 · 2015: 1 · 2014: 4 · 2013: 4
- FWCI
- 3.51
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Clinical Investigation (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Immunology and Microbiology › Immunology › Immunotoxicology and immune responses
- Keywords
- circadian rhythm, seasonal variation, T cells, natural killer cells, T helper cells, suppressor/cytotoxic T cells, lymphocyte subsets, circannual rhythm, peripheral blood lymphocyte count, healthy men
- MeSH terms
- Adult, Antibodies, Monoclonal, Circadian Rhythm, Humans, Killer Cells, Natural, Leukocyte Count, Male, Seasons, T-Lymphocytes
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