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Apoptosis Physiology and Pathology: The Impact of Cell Death on Human Diseases and Therapies



Abstract:The heart is one of the most fascinating organs in living beings. It beats up to 100,000 times a day throughout the lifespan, without resting. The heart undergoes profound anatomical, biochemical, and functional changes during life, from hypoxemic fetal stages to a completely differentiated four-chambered cardiac muscle. In the middle, many biological events occur after and intersect with each other to regulate development, organ size, and, in some cases, regeneration. Several studies have defined the essential roles of the Hippo pathway in heart physiology through the regulation of apoptosis, autophagy, cell proliferation, and differentiation. This molecular route is composed of multiple components, some of which were recently discovered, and is highly interconnected with multiple known prosurvival pathways. The Hippo cascade is evolutionarily conserved among species, and in addition to its regulatory roles, it is involved in disease by drastically changing the heart phenotype and its function when its components are mutated, absent, or constitutively activated. In this review, we report some insights into the regulation of cardiac physiology and pathology by the Hippo pathway.Keywords: Hippo signaling; cardiac disease; cardiac physiology; YAP1; TAZ




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In a landmark review, Hanahan and Weinberg suggested that six essential alterations in cell physiology could underlie malignant cell growth [6]. These six alterations were described as the hallmarks of nearly all cancers and included, 1) self-sufficiency in growth signals, 2) insensitivity to growth inhibitory (antigrowth) signals, 3) evasion of programmed cell death (apoptosis), 4) limitless replicative potential, 5) sustained vascularity (angiogenesis), and 6) tissue invasion and metastasis. Genome instability, leading to increased mutability, was considered the essential enabling characteristic for manifesting the six hallmarks [6]. However, the mutation rate for most genes is low making it unlikely that the numerous pathogenic mutations found in cancer cells would occur sporadically within a normal human lifespan [7]. This then created another paradox. If mutations are such rare events, then how is it possible that cancer cells express so many different types and kinds of mutations?


The path from normal cell physiology to malignant behavior, where all major cancer hallmarks are expressed, is depicted in Figure 2 and is based on the evidence reviewed above. Any unspecific condition that damages a cell's oxidative phosphorylation, but is not severe enough to induce apoptosis, can potentially initiate the path to a malignant cancer. Some of the many unspecific conditions contributing to carcinogenesis can include inflammation, carcinogens, radiation (ionizing or ultraviolet), intermittent hypoxia, rare germline mutations, viral infections, and disruption of tissue morphogenetic fields. Any of these conditions can damage the structure and function of mitochondria thus activating a specific RTG response in the damaged cell. If the mitochondrial damage persists, the RTG response will persist. Uncorrected mitochondrial damage will require a continuous compensatory energy response involving substrate level phosphorylation in order to maintain the ΔG' ATP of approximately -56 kJ/mol for cell viability. Tumor progression is linked to a greater dependence on substrate level phosphorylation, which eventually becomes irreversible. As the integrity of the nuclear genome is dependent on the efficiency of mitochondrial energy production, the continued impairment of mitochondrial energy production will gradually undermine nuclear genome integrity leading to a mutator phenotype and a plethora of somatic mutations. Activation of oncogenes, inactivation of tumor suppressor genes, and aneuploidy will be the consequence of protracted mitochondrial dysfunction. These gene abnormalities will contribute further to mitochondrial dysfunction while also enhancing those energy pathways needed to up-regulate and sustain substrate level phosphorylation. The greater the dependency on substrate level phosphorylation over time the greater will be the degree of malignancy. Damage to the respiratory capacity of tissue myeloid cells can also produce invasive and metastatic properties according to the macrophage hypothesis of metastasis. This metabolic scenario can account for all major acquired characteristics of cancer to include the Warburg effect.


Targeted temperature management has historically been the focus of considerable HIBI research. It is a mainstay in the management of HIBI by mitigating secondary injury after CA [56]. At the cellular level, the beneficial effects of hypothermia are well documented. Cerebral metabolism is reduced by 5% to 10% per 1 C decrease in core body temperature. In addition, global carbon dioxide production and oxygen consumption are decreased proportionally to reductions in core body temperature [57]. By decreasing cerebral metabolism, hypothermia avoids excessive intracellular anaerobic metabolism, which leads to increased lactate production. Hypothermia also improves cerebral glucose use and allows available cellular energy stores to be used for necessary cellular functions in keeping with neuronal survival [56]. Additional benefits of hypothermia include prevention of apoptosis by decreasing proapoptotic mediators such as p53, tumor necrosis factor α, and caspase enzymes while increasing expression of antiapoptotic proteins such as Bcl-2 [56, 57]. Hypothermia also prevents mitochondrial dysfunction, a key pathway involved in the promotion of apoptosis by release of cytochrome c oxidase into the cellular cytoplasm [56]. Finally, hypothermia decreases inflammatory mediators such as the interleukin-1 family of cytokines [58] as well as chemotaxis of leukocytes into cerebral interstitial tissue [56], reduces excitotoxic neurotransmitter release (glutamate and glycine) [57], and decreases free radical production after HIBI [57]. Sustained hypothermia also has detrimental physiologic effects pertaining to immune suppression, hemoconcentration, coagulopathy, arrhythmias, electrolyte disturbances, and hemodynamic instability, which must be weighed against the possible benefits [56]. Furthermore, unintentional hypothermia can occur after CA, indicating possible severe damage to the key centers of thermoregulation, including the hypothalamus [56].


Liver involvement in severe Plasmodium falciparum infection is commonly a significant cause of morbidity and mortality among humans. The clinical presentation of jaundice often reflects a certain degree of liver damage. This study investigated the liver pathology of severe P. falciparum malaria as well as the regulation and occurrence of apoptosis in cellular components of formalin-fixed, paraffin-embedded liver tissues.


The severity of liver histopathology, occurrence of apoptosis and NF-κB p65 activation in P. falciparum malaria were associated with higher TB level. Significant correlations were found between NF-κB p65 expression and apoptosis in Kupffer cells and lymphocytes in the portal tracts.


Apoptotic changes occur in a variety of cellular systems and involve both physiologic and pathologic changes. While apoptotic change in the liver have not been documented in human malaria, changes have been reported in animal models during the erythrocytic stage in hepatocytes[7, 8] and during the hepatic stage in Kupffer cells[9]. This process of programmed cell death can be mediated by various stimuli, including hormones, cytokines, growth factors, bacterial or viral infections and the immune response[10]. Cell apoptosis is regulated via two major pathways: the intrinsic or mitochondrial pathway and the extrinsic or death-receptor pathway. Initiator caspases, such as caspase-8 or -9, play a regulatory role by activating downstream effector caspases, such as caspase-3, -6, or -7[11]. NF-κB has been shown to regulate the apoptotic program in various cell types, either as an up-regulating response or as an apoptosis blocker[12]. Evidence of NF-κB regulating apoptosis was found in the brain endothelial cells and intravascular lymphocytes in cerebral malaria[13]. However, no linkage between NF-κB and apoptosis has been reported in the livers of P. falciparum malaria patients. This study evaluated the liver pathology of severe P. falciparum malaria in association with total bilirubin (TB) level. The occurrence of apoptosis and its relation to a signaling molecule (NF-κB) in liver tissues was investigated.


The renin-angiotensin-aldosterone-vasopressin (antidiuretic hormone [ADH]) system causes a cascade of potentially deleterious long-term effects. Angiotensin II worsens heart failure by causing vasoconstriction, including efferent renal vasoconstriction, and by increasing aldosterone production, which enhances sodium reabsorption in the distal nephron and also causes myocardial and vascular collagen deposition and fibrosis. Angiotensin II increases norepinephrine release, stimulates release of vasopressin, and triggers apoptosis. Angiotensin II may be involved in vascular and myocardial hypertrophy, thus contributing to the remodeling of the heart and peripheral vasculature, potentially worsening HF. Aldosterone can be synthesized in the heart and vasculature independently of angiotensin II (perhaps mediated by corticotropin, nitric oxide, free radicals, and other stimuli) and may have deleterious effects in these organs. 2ff7e9595c


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