Serum Immune-Related Proteins are Differentially Expressed during Hibernation in the American Black Bear

Abstract

Hibernation is an adaptation to conserve energy in the face of extreme environmental conditions and low food availability that has risen in several animal phyla. This phenomenon is characterized by reduced metabolic rate (∼25% of the active basal metabolic rate in hibernating bears) and energy demand, while other physiological adjustments are far from clear. The profiling of the serum proteome of the American black bear (Ursus americanus) may reveal specific proteins that are differentially modulated by hibernation, and provide insight into the remarkable physiological adaptations that characterize ursid hibernation. In this study, we used differential gel electrophoresis (DIGE) analysis, liquid chromatography coupled to tandem mass spectrometry, and subsequent MASCOT analysis of the mass spectra to identify candidate proteins that are differentially expressed during hibernation in captive black bears. Seventy serum proteins were identified as changing by ±1.5 fold or more, out of which 34 proteins increased expression during hibernation. The majority of identified proteins are involved in immune system processes. These included α2-macroglobulin, complement components C1s and C4, immunoglobulin μ and J chains, clusterin, haptoglobin, C4b binding protein, kininogen 1, α2-HS-glycoprotein, and apoplipoproteins A-I and A-IV. Differential expression of a subset of these proteins identified by proteomic analysis was also confirmed by immunodetection. We propose that the observed serum protein changes contribute to the maintenance of the hibernation phenotype and health, including increased capacities for bone maintenance and wound healing during hibernation in bears.

Exploring the Bone Proteome to Help Explain Altered Bone Remodeling and Preservation of Bone Architecture and Strength in Hibernating Marmots

“…For example, we found that immunoglobulin heavy chain (a large polypeptide subunit of an antibody) was higher in bone samples in hibernating compared with active marmots. This is consistent with previous studies showing higher levels of immunoglobulin heavy chain in serum from hibernating compared with active bears (Chow et al 2013), which may possibly help explain bears' ability for wound healing during hibernation (Nishio et al 2009;Iaizzo et al 2012). Our finding is also consistent with increased numbers of B-lymphocytes in blood of hibernating 13-lined ground squirrels compared with active squirrels (Bouma et al 2013).…”

Transcriptomics in the wild: Hibernation physiology in free‐ranging dwarf lemurs

“…In a previous study with a captive colony of dwarf lemurs, we found another iron‐related gene, haptoglobin to show extreme levels of expression during Torpor relative to an active state (fold change of 7.22; Faherty, Villanueva‐Cañas, et al., ). This gene was also shown to be highly expressed during Torpor in other hibernating species (Chow, Donahue, Vaughan, McConkey, & Vijayan, ; Mominoki, ; Mominoki et al., ; Vermillion, Jagtap, Johnson, Griffin, & Andrews, ; Yan, ).…”

“…In a previous study with a captive colony of dwarf lemurs, we found another iron-related gene, haptoglobin to show extreme levels of expression during Torpor relative to an active state (fold change of 7.22 ;Faherty, Villanueva-Cañas, et al, 2016). This gene was also shown to be highly expressed during Torpor in other hibernating species (Chow, Donahue, Vaughan, McConkey, & Vijayan, 2013;Mominoki, 1998;Mominoki et al, 2005;Vermillion, Jagtap, Johnson, Griffin, & Andrews, 2015;Yan, 2006 (Utz & van Breukelen, 2013). Other studies have shown that rewarming rates for golden-mantled ground squirrels (Callospermophilus lateralis) can be nearly 1.5°C/min (Utz, Velickovska, Shmereva, & van Breukelen, 2007).…”

Blood clotting behavior is innately modulated in Ursus Americanus during early and late denning relative to summer months

“…One explanation, revealed in previous research on brown bears (Ursus arctos), is that bears have more and smaller platelets compared with humans (Fröbert et al, 2010). Interestingly, other studies have demonstrated seasonal changes that may suggest modulation, including previous work done by Chow et al (2013) and Sheikh et al (2003) describing differences in immune-related proteins including alpha 2 macroglobulins.…”