Short day lengths augment stress-induced leukocyte trafficking and stress-induced enhancement of skin immune function

Abstract

Environmental conditions influence the onset and severity of infection and disease. Stressful conditions during winter may weaken immune function and further compromise survival by means of hypothermia, starvation, or shock. To test the hypothesis that animals may use photoperiod to anticipate the onset of seasonal stressors and adjust immune function, we evaluated glucocorticoids and the distribution of blood leukocytes in Siberian hamsters (Phodopus sungorus) exposed to long day lengths (i.e., summer) or short day (SD) lengths (i.e., winter) at baseline and during acute stress. We also investigated the influence of photoperiod and acute stress on a delayed-type hypersensitivity response in the skin. SDs increased glucocorticoid concentrations and the absolute number of circulating blood leukocytes, lymphocytes, T cells, and natural killer cells at baseline in hamsters. During stressful challenges, it appears beneficial for immune cells to exit the blood and move to primary immune defense areas such as the skin, in preparation for potential injury or infection. Acute (2 h) restraint stress induced trafficking of lymphocytes and monocytes out of the blood. This trafficking occurred more rapidly in SDs compared to long days. Baseline delayed-type hypersensitivity responses were enhanced during SDs; this effect was augmented by acute stress and likely reflected more rapid redistribution of leukocytes out of the blood and into the skin. These results suggest that photoperiod may provide a useful cue by which stressors in the environment may be anticipated to adjust the repertoire of available immune cells and increase survival likelihood.

Winter day lengths enhance T lymphocyte phenotypes, inhibit cytokine responses, and attenuate behavioral symptoms of infection in laboratory rats

“…This enhancing effect of short photoperiods on T cells resembles that observed in reproductively photoperiodic rodents (e.g., Siberian hamsters; Bilbo et al, 2002a). In contrast to hamsters, the overall number of leukocytes in the blood did not differ in response to photoperiod, suggesting that increases in T-cell subtypes reflect a redistribution of investment in select cell phenotypes, rather than an omnibus effect on total leukocyte numbers.…”

“…For example, deer mice (Peromyscus maniculatus) exhibit increases in specific antibody production and lymphocyte antigen-responsiveness (Demas and Nelson, 1998a) following exposure to several weeks of short days; these changes in immune function occur in parallel with the cessation of reproductive activity (Desjardins et al, 1986). Siberian hamsters (Phodopus sungorus) also exhibit a host of changes in immune function following adaptation to short photoperiods: antibody production is decreased, but circulating leukocyte, T-cell and B-cell counts are greater, natural killer cell cytotoxicity is facilitated, and antigen-specific skin inflammatory responses are enhanced (Drazen et al, 2000;Bilbo et al, 2002a;Yellon at al., 1999). Short days also ameliorate the symptoms of bacterial infection: LPS-induced production of IL-1β, IL-6, and TNFα is lower in short days (Bilbo et al, 2002b;Prendergast et al, 2003a), and the magnitude and/or persistence of thermoregulatory, behavioral, emotional, and ponderal responses to infection are markedly attenuated (Bilbo et al, 2002b).…”

Pineal-dependent and -independent effects of photoperiod on immune function in Siberian hamsters (Phodopus sungorus)

“…Circulating lymphocyte concentrations (e.g., T cells, B cells) are greater in short days relative to long days (Bilbo et al, 2002a;Prendergast et al, 2004a;Yellon et al, 2005). In addition, more integrative measures of immune function such as T-cell-dependent skin inflammatory responses, which depend in part on specific leukocyte subtypes (i.e., CD44+ and CD62+ leukocytes), are greater in short days relative to long days (Dhabhar et al, 2000;Bilbo et al, 2002a;Prendergast et al, 2004a). Short days also ameliorate the acute-phase symptoms of bacterial infection in Siberian hamsters: LPS-induced IL-1β, IL-6, and TNF-α production are lower (Bilbo et al, 2002b;Prendergast et al, 2003a), and the magnitude and/or persistence of thermoregulatory (fever), behavioral (anorexia), emotional (anhedonia), and ponderal (cachexia) responses to simulated infection are attenuated (Bilbo et al, 2002b).…”

“…In Siberian hamsters, short days enhance natural killer cell cytolytic capacity and spontaneous blastogenesis in both whole blood lymphocytes and isolated lymphocytes (Yellon et al, 1999a). Circulating lymphocyte concentrations (e.g., T cells, B cells) are greater in short days relative to long days (Bilbo et al, 2002a;Prendergast et al, 2004a;Yellon et al, 2005). In addition, more integrative measures of immune function such as T-cell-dependent skin inflammatory responses, which depend in part on specific leukocyte subtypes (i.e., CD44+ and CD62+ leukocytes), are greater in short days relative to long days (Dhabhar et al, 2000;Bilbo et al, 2002a;Prendergast et al, 2004a).…”

Seasonal modulation of sickness behavior in free-living northwestern song sparrows (Melospiza melodia morphna)

“…The majority of studies examining seasonal variation of immunity have focused upon cellular and humoral components (Blom, 1994;Lochmiller et al, 1994;Demas and Nelson, 1996;Nelson and Demas, 1996;Zuk and Johnsen, 1998;Gonzalez et al, 1999;Moore and Siopes, 2000;Bilbo et al, 2002a;Møller et al, 2003;Nelson, 2004), while neglecting behavioral responses to infection. These behaviors are collectively referred to as sickness behaviors and include reduced activity, decreased food (anorexia) and water (adipsia) intake leading to weight loss, and a general decline in social activities and behavior (Hart, 1988).…”