Investigating the Proximate Causes of Defective Antibody Production in the Aged Immune System

In the open access paper linked below, researchers outline the proximate cause for one aspect of the characteristic decline in immune function that accompanies aging, in this case the failure to produce sufficient numbers of antibodies in response to the presence of pathogens. Along the way they find an approach that can partially reverse this degeneration, though it remains far from clear as to nature of the root causes and how those root causes lead to the proximate cause.

The progressive failure of the immune system is an important component of age-related frailty, and the more that can be done to turn it back, the better. Here the focus is on humoral immunity and specifically the generation of antibodies by B cells. Portions of the immune system are responsible for digesting the component parts of pathogens such as viruses and microbes, breaking them down into antigens, then presenting those antigens to the antibody manufacturing process. Antibodies are proteins constructed to match and bind to those antigens, let loose in vast numbers so that they can either flag the matching pathogens for destruction by other parts of the immune system, or directly interfere in some vital machinery essential to the pathogen's activities.

It is well known that the aged immune system produces an ever smaller output of antibodies when challenged. This is a part of the reason why vaccinations become ineffective in the elderly, for example. It is worth keeping an eye on research efforts to explain and potentially reverse this decline, but bear in mind that the immune system is enormously complex. Talking about even one narrow portion of the whole - manufacturing antibodies in this case - means considering the roles of many different cell types, mechanisms within cells, and an intricate chain of activities leading from the arrival of a pathogen to matching antibody production, wherein imbalance or failure at any point leads to a worse outcome. You should probably click through and take a look at the diagram that accompanies the abstract before reading on:

Defective TFH Cell Function and Increased TFR Cells Contribute to Defective Antibody Production in Aging

The extent of humoral immunity, or immunity provided by antibodies, decreases with age in both mice and humans. This decrease in humoral immunity translates into increased frequency and severity of infectious diseases in aged individuals. Furthermore, vaccination of the elderly provides inadequate protection against most infectious diseases, leaving these individuals vulnerable to a number of diseases.

The production of antibodies results from a complex interaction of B cells with T follicular helper (TFH) cells in the germinal center (GC) reaction. After differentiation, TFH cells migrate to the B cell follicle and provide help to B cells via costimulation and cytokine production. Mice lacking TFH cells, or their key effector molecules, have severely defective antibody production in response to T-dependent antigens.

T follicular regulatory (TFR) cells are a recently defined specialized subset of effector T regulatory cells (Tregs) that inhibit antibody production. TFR cells originate from natural Tregs in contrast to TFH cells, which develop from naive CD4+ T cell precursors. Programmed cell death protein-1 (PD-1) expression on TFR cells limits both the differentiation and effector function of TFR cells. How TFR cells exert their suppressive effects is not yet clear.

We have demonstrated that the ratio of TFH/TFR cells is an important factor in humoral immunity and that this ratio dictates the magnitude of antibody responses. Therefore, successful humoral immunity is a delicate balance between stimulatory TFH cells and inhibitory TFR cells and not simply a result of the total number of TFH cells. TFR cells appear to be specialized in their suppression of the GC reaction because non-TFR Tregs do not have the same suppressive capacity. We demonstrate an increase in the ratio of inhibitory T follicular regulatory (TFR) cells to stimulatory T follicular helper (TFH) cells in aged mice. We find increases in both TFH and TFR cells, with a proportionally greater increase in TFR cells. Aged TFH and TFR cells are phenotypically distinct from those in young mice, exhibiting increased programmed cell death protein-1 expression but decreased ICOS expression. Aged TFH cells exhibit defective antigen-specific responses, and programmed cell death protein-ligand 1 blockade can partially rescue TFH cell function. In contrast, young and aged TFR cells have similar suppressive capacity on a per-cell basis in vitro and in vivo.

Together, our studies provide insights into mechanisms for defective antibody production in aging. We find an over-representation of functionally competent suppressive TFR cells in aged mice, most likely resulting from enhanced differentiation of TFR cells. However, expansion of memory TFR cells may also contribute. In addition, we find that TFH cells are generated following immunization of aged mice, but these aged TFH cells fail to elicit strong antigen-specific B cell responses in vivo. Aged TFH cells express higher levels of PD-1 and PD-1 blockade can improve TFH cell function. Thus, the substantial increase in fully suppressive TFR cells, combined with the decrease in antigen-specific responses of TFH cells, results in a significant defect in antibody production in aged mice. Although other mechanisms, such as defects in clonality and/or naive T or B cell numbers also may contribute, our data point to alterations in TFH cell activity and TFR cell proportions as being a key mechanism that impairs antibody production in aging. Therefore, approaches that downmodulate TFR cells may provide a strategy for improving humoral immune responses in the elderly.

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