Do natural antibodies compensate for humoral immunosenescence in tropical pythons?

Abstract

Summary 1.Ageing is frequently claimed to result in an age-dependent deterioration in immune function. 2. Our results, however, based on 30 known-aged water pythons (Liasis fuscus; age ranging from <1 to 18 years) immunized with keyhole limpet haemocyanin (KLH), demonstrate that agerelated changes in immune function may follow different and opposing pathways. 3. Python-specific humoral antibodies (SpAb) showed an age-dependent decrease in cross-reactivity to KLH, whereas natural antibodies (NAbs) ability to bind to this antigen increased with age. 4. Notably, when humoral SpAb and NAb titres were combined, no effect of age was detected in antibody cross-reactivity, strongly suggesting that NAbs may play a crucial role in maintaining immunocompetence during the ageing process.

Humoral immune responses are maintained with age in a long-lived ectotherm, the red-eared slider turtle

“…Thus, our turtles seem to have an increase in NAb, B-1-like immunity with age, but the specific, B-2-like response to LPS was not significantly impacted by age. While an increase in NAbs with age has been reported in mammals, birds and reptiles (Candore et al, 1997;Parmentier et ., 2004;Benatuil et al, 2008;Sparkman and Palacios, 2009;Ujvari and Madsen, 2011), studies in these same taxa have also reported a decrease in specific antibodies with age (Ujvari and Madsen, 2005;Lavoie, 2006;Frasca et al, 2008;Ujvari and Madsen, 2011). These studies on specific immune responses include a wide range of both T-dependent and T-independent antigens, including LPS.…”

“…This process can have important consequences for an organism; for example, an increase in mortality and morbidity in elderly humans is commonly attributed to a decrease in immune function (Dicarlo et al, 2009). However, the aging process does not affect every branch of the immune system in the same manner (Palacios et al, 2007;Ujvari and Madsen, 2011). This is highlighted in the humoral immune system, where it has been found in a number of taxa that specific antibody production decreases with age, while non-specific, polyreactive antibodies increase with age (Frasca et al, 2008).…”

“…These new assays, along with the ELISA that we have previously validated and the common practice of using blood smears to examine leukocyte populations, will allow us to gain a fuller understanding of humoral immune responses of sliders. A wide range of studies in a variety of vertebrate taxa, including mammals, birds and reptiles, have found that specific antibodies decrease with age while NAbs increase with age (Candore et al, 1997;Parmentier et al, 2004;Ujvari and Madsen, 2005;Lavoie, 2006;Benatuil et al, 2008;Frasca et al, 2008;Sparkman and Palacios, 2009;Ujvari and Madsen, 2011). This pattern, along with the typically slow and less-robust specific responses of reptiles, leads us to hypothesize that red-eared sliders utilize a predominantly NAbbased response, and thus would not show a deficit in humoral immune defenses with age.…”

“…In humans, this reduction in specific antibody responses has been viewed as a contributor to the rise in mortality and morbidity with increasing age and, although there is also an increase in NAbs with age in humans, they do not appear to be able to compensate for the loss of the specific antibodies (McGlauchlen and Vogel, 2003). Interestingly, the less-robust specific immune response of reptiles of all ages, combined with the increase in NAbs with age, may constitute an overall positive change in immune defense (Ujvari and Madsen, 2011). However, little is known about antibody production in reptiles beyond quantity.…”

“…This may force them to rely more heavily on NAbs to deal with pathogens. Thus, an increase in NAbs with age may be viewed as a positive change in immunity with age in reptiles (Ujvari and Madsen, 2011).…”