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CELL DEATH IN THE OLFACTORY SYSTEM

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19 Contribution of Apoptosis to Physiologic

Remodeling of the Endocrine Pancreas and Pathophysiology of Diabetes

Nika N. Danial

1. INTRODUCTION

Homeostatic control of blood glucose levels is critically dependent on the balance of glucagon and insulin, two counteracting pancreatic hormones secreted by endocrine cells within the islets of Langerhans – alpha and beta cells, respectively. Elegant biochemical studies combined with metabolic flux analysis uncovered the unique ability of beta cells to sense blood glucose fluctuations and to fine tune insulin secretion accordingly.1 A high-capacity glucose transport system, a low-Km glucose phosphorylating activity catalyzed by glucokinase (GK), and the ability to channel the majority of glycolytically derived pyruvate to the mitochondrial tricarboxylic acid (TCA) cycle constitute essential metabolic design features that endow beta cells with a specialized secretory function.2 The increase in intracellular adenosine triphosphate (ATP)/adenosine diphosphate (ADP) ratio on mitochondrial metabolism of nutrients is among the metabolic coupling factors connecting fuel oxidation to insulin secretion. A rise in ATP/ADP ratio in turn leads to closure of ATP-sensitive K (KATP) channels at the plasma membrane, followed by membrane depolarization and influx of Ca2+ necessary for release of insulin granules.3 The two aspects of beta cell biology that contribute significantly to euglycemia are glucose dose responsiveness of insulin secretion and the remarkable plasticity of beta cell mass to meet insulin demand under physiologic and pathophysiologic nutrient stress.4,5 Beta cell mass is the net outcome of neogenesis (formation of new beta cells from non–beta cell precursors), replication of preexisting beta cells, beta cell size, and apoptosis.6 The integration of beta cell function and mass is further ensured through nutrient sensing pathways that concomitantly signal insulin secretion and modulate beta cell replication and survival.7,8 This chapter highlights the

apoptotic mechanisms operative in beta cells that influence the dynamic control of beta cell mass during the developmental remodeling of the endocrine pancreas and in the pathogenesis of diabetes.

2. APOPTOSIS IN PHYSIOLOGIC CONTROL

OF BETA CELL MASS

The transition from fetal to adult beta cell during physiologic remodeling of endocrine pancreas is heavily influenced by apoptosis. During fetal life in both rodents and humans, large and rapid expansion of beta cell mass is marked mainly by beta cell neogenesis, endowing the fetal pancreas with a suitable number of beta cells.9,10 Although beta cell mass continues to expand in neonates, the net beta cell mass remains unchanged because of a concomitant wave of apoptosis, which in rodents, occurs around the weaning period, and in humans, around the time of birth.11,12 Neonatal beta cell apoptosis is part of a physiologic program to remodel the endocrine pancreas4,12 and may further serve as a quality-control mechanism to select for a functional pool of beta cells with appropriate insulin secretion response to glucose.13,14,15 Persistent beta cell proliferation and apoptosis beyond the neonatal phase of pancreatic development was recently found in biopsies of newborns and children with hyperinsulinism and hypoglycemia of infancy,11 a metabolic disorder in which the lack of proper neonatal beta cell mass remodeling interferes with the fetal to adult beta cell transition, leading to retention of fetal beta cells incapable of eliciting an insulin secretory response that matches the level of glycemia.16 The molecular mechanisms controlling the change in apoptotic rate during fetal to neonatal beta cell transition are not fully understood. Direct correlations exist between the wave of apoptosis and expression

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pattern of multiple cell death/survival molecules in the developing pancreas. Notably, the antiapoptotic BCL-2 protein and the inhibitor of apoptosis protein survivin, which inhibits caspase-3 and -9,17 display high expression levels in fetal beta cells but are undetectable in the postnatal period.18,19 Furthermore, the neonatal wave of apoptosis is marked by high expression of the dephosphorylated, apoptotically active form of the BCL-2 family protein BAD.20,21,22 This is consistent with the observation that insulin-like growth factor (IGF) II, a known beta cell survival factor that targets BAD phosphorylation23 and stimulates beta cell survival,24 declines during neonatal pancreatic development.25,26,27 Of note, low levels of fetal IGF-II levels are associated with elevated beta cell apoptosis and gestational diabetes due to maternal diet low in proteins.28

In the adult, beta cell mass is linearly proportional to body weight29 and is under tight homeostatic control so that insulin secretion is proportional to insulin demand. Apoptosis influences the beta cell mass dynamics in the adult. For example, a 2.5-fold increase in beta cell mass during pregnancy30,31 is followed by rapid and efficient involution of beta cell mass postpartum because of a significant increase in apoptosis.32 Similarly, increase in beta cell function33,34 and mass35,36,37,38 during weight gain associated with obesity is an adaptive response to compensate for obesity-induced insulin resistance, a state in which liver and peripheral tissues such as muscle and fat become less sensitive to the action of this hormone and more insulin is needed to preserve euglycemia.39,40 In addition to increased proliferation and beta cell hypertrophy, attenuated apoptosis contributes to obesity-induced beta cell mass expansion.41,42,43 Studies are just beginning to unravel the functional relevance of the intrinsic and extrinsic pathways of apoptosis in beta cell mass adaptation. As such, genetic models have provided evidence that BAD36,44 and caspase-845 are but two apoptotic modulators of obesity-associated beta cell mass expansion. The importance of this homeostatic response of beta cell mass to insulin resistance is underscored by the fact that its insufficiency is associated with type 2 diabetes46,47,48,49 as detailed in the following sections.

3. CONTRIBUTION OF APOPTOSIS TO BETA CELL

MASS INADEQUACIES IN DIABETES

Loss of functional beta cell mass is central to the etiology of both type 1 and type 2 diabetes.35,50,51,52 Although the distinction between these two disease subtypes is based on differences in the nature of beta cell failure, the time of disease onset, and genetic predisposition,

accumulating evidence suggests that the common features between these two subtypes are more numerous than previously anticipated. Indeed, beta cell apoptosis is a common end point in both subtypes, which is further influenced by genetic and environmental factors. In type 1 diabetes (T1D), absolute insulin deficiency is due to the autoimmune-mediated loss of beta cells and the associated inflammatory immune response.52 In type 2 diabetes (T2D), beta cell apoptosis is induced by metabolic stress that accompanies chronic exposure to elevated levels of glucose and saturated fatty acids, oxidative stress, and endoplasmic reticulum (ER) stress because of accumulation of unfolded proteins.8,53,54,55 Recent studies also show that the damage inflicted by inflammatory cytokines is not unique to T1D; rather the metabolic stress imposed on beta cells in T2D leads to their secretion of inflammatory cytokines and subsequent cytotoxicity.56 The following sections review the beta cell defect and apoptotic stimuli in each diabetes subtype.

3.1. Beta cell death in the development of T1D

T1D is marked by autoimmune destruction of islet beta cells by cytotoxic T-lymphocytes (CTLs) that recognize beta cell–derived self-antigens. Progression of the type 1 disease follows a series of histopathologically defined stages that includes infiltration of lymphocytes in the area surrounding the islets of Langerhans, also known as insulitis, followed by production of inflammatory cytokines and fulminating immune attack.52 Permanent loss of functional beta cell mass is accompanied by blunted insulin secretion, glucose intolerance, and insulin dependency for life. Although characterization of the type 1 disease in humans has been limited to in vitro islet cultures and gene expression profiling of different disease stages, mouse models of the disease, especially the nonobese diabetic (NOD) mouse, as well as multiple T cell receptor TCR transgenic lines, have proved instructive in uncovering some of the molecular mechanisms underlying the breakdown of immune barrier and the cellular and molecular components of beta cell destruction.57 However, despite multiple common elements in disease progression, the extent to which modeling of the type 1 disease in rodents phenocopies that in humans is not fully understood.

Autoantigens in T1D consist of beta cell–derived peptides that are most likely encountered during the wave of neonatal beta cell apoptosis.58,59,60 Antigen presenting cells (APCs) such as macrophages and dendritic cells engulf apoptotic beta cells and process and present beta cell–derived peptides that include, but may not

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