Dysregulation of cellular energetics in Gulf War Illness

Abstract:

Gulf War Illness (GWI) is estimated to have affected about one third of the Veterans who participated in the first Persian Gulf War. The symptoms of GWI include chronic neurologic impairments, chronic fatigue syndrome, as well as fibromyalgia and immune system disorders, collectively referred to as chronic multi-symptom illness. Thirty years after the war, we still do not have an effective treatment for GWI. It is necessary to understand the molecular basis of the symptoms of GWI in order to develop appropriate therapeutic strategies. Cellular energetics are critical to the maintenance of cellular homeostasis, a process that is highly dependent on intact mitochondrial function and there is significant evidence from both human studies and animal models that mitochondrial impairments may lead to GWI symptoms.

The available clinical and pre-clinical data suggest that agents that improve mitochondrial function have the potential to restore cellular energetics and treat GWI. To date, the experiments conducted in animal models of GWI have mainly focused on neurobehavioral aspects of the illness. Additional studies to address the fundamental biological processes that trigger the dysregulation of cellular energetics in GWI are warranted to better understand the underlying pathology and to develop new treatment methods. This review highlights studies related to mitochondrial dysfunction observed in both GW veterans and in animal models of GWI.

Source: Raju RP, Terry AV. Dysregulation of cellular energetics in Gulf War Illness. Toxicology. 2021 Aug 10:152894. doi: 10.1016/j.tox.2021.152894. Epub ahead of print. PMID: 34389359. https://pubmed.ncbi.nlm.nih.gov/34389359/

Radiation exposure and mitochondrial insufficiency in chronic fatigue and immune dysfunction syndrome

Abstract:

Chronic fatigue and Immune Dysfunction Syndrome (CFIDS) is a heterogeneous disease that may be promoted by various environmental stressors, including viral infection, toxin uptake, and ionizing radiation exposure. Previous studies have identified mitochondrial dysfunction in CFIDS patients, including modulation of mitochondrial respiratory chain activity, deletions in the mitochondrial genome, and upregulation of reactive oxygen species (ROS). This paper focuses on radiation effects and hypothesizes that CFIDS is primarily caused by stressor-induced mitochondrial metabolic insufficiency, which results in decreased energy production and anabolic metabolites required for normal cellular metabolism. Furthermore, tissues neighbouring or distant from directly perturbed tissues compensate for this dysfunction, which causes symptoms associated with CFIDS.

This hypothesis is justified by reviewing the links between radiation exposure and CFIDS, cancer, immune dysfunction, and induction of oxidative stress. Moreover, the relevance of mitochondria in cellular responses to radiation and metabolism are discussed and putative mitochondrial biomarkers for CFIDS are introduced. Implications for diagnosis are then described, including a potential urine assay and PCR test for mitochondrial genome mutations. Finally, future research needs are offered with an emphasis on where rapid progress may be made to assist the afflicted.

Source: Rusin A, Li M, Cocchetto A, Seymour C, Mothersill C. Radiation exposure and mitochondrial insufficiency in chronic fatigue and immune dysfunction syndrome. Med Hypotheses. 2021 Jul 27;154:110647. doi: 10.1016/j.mehy.2021.110647. Epub ahead of print. PMID: 34358921. https://pubmed.ncbi.nlm.nih.gov/34358921/

Bioenergetic and Proteomic Profiling of Immune Cells in Myalgic Encephalomyelitis/Chronic Fatigue Syndrome Patients: An Exploratory Study

Abstract:

Myalgic encephalomyelitis/chronic fatigue syndrome (ME/CFS) is a heterogeneous, debilitating, and complex disease. Along with disabling fatigue, ME/CFS presents an array of other core symptoms, including autonomic nervous system (ANS) dysfunction, sustained inflammation, altered energy metabolism, and mitochondrial dysfunction. Here, we evaluated patients’ symptomatology and the mitochondrial metabolic parameters in peripheral blood mononuclear cells (PBMCs) and plasma from a clinically well-characterised cohort of six ME/CFS patients compared to age- and gender-matched controls.

We performed a comprehensive cellular assessment using bioenergetics (extracellular flux analysis) and protein profiles (quantitative mass spectrometry-based proteomics) together with self-reported symptom measures of fatigue, ANS dysfunction, and overall physical and mental well-being. This ME/CFS cohort presented with severe fatigue, which correlated with the severity of ANS dysfunction and overall physical well-being.

PBMCs from ME/CFS patients showed significantly lower mitochondrial coupling efficiency. They exhibited proteome alterations, including altered mitochondrial metabolism, centred on pyruvate dehydrogenase and coenzyme A metabolism, leading to a decreased capacity to provide adequate intracellular ATP levels. Overall, these results indicate that PBMCs from ME/CFS patients have a decreased ability to fulfill their cellular energy demands.

Source: Fernandez-Guerra P, Gonzalez-Ebsen AC, Boonen SE, Courraud J, Gregersen N, Mehlsen J, Palmfeldt J, Olsen RKJ, Brinth LS. Bioenergetic and Proteomic Profiling of Immune Cells in Myalgic Encephalomyelitis/Chronic Fatigue Syndrome Patients: An Exploratory Study. Biomolecules. 2021 Jun 29;11(7):961. doi: 10.3390/biom11070961. PMID: 34209852. https://pubmed.ncbi.nlm.nih.gov/34209852/

Editorial: The Pathogenesis of Long-Term Neuropsychiatric COVID-19 and the Role of Microglia, Mitochondria, and Persistent Neuroinflammation: A Hypothesis

Abstract:

Persistent comorbidities occur in patients who initially recover from acute coronavirus disease 2019 (COVID-19) due to infection with severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). ‘Long COVID’ involves the central nervous system (CNS), resulting in neuropsychiatric symptoms and signs, including cognitive impairment or ‘brain fog’ and chronic fatigue syndrome. There are similarities in these persistent complications between SARS-CoV-2 and the Ebola, Zika, and influenza A viruses. Normal CNS neuronal mitochondrial function requires high oxygen levels for oxidative phosphorylation and ATP production. Recent studies have shown that the SARS-CoV-2 virus can hijack mitochondrial function. Persistent changes in cognitive functioning have also been reported with other viral infections. SARS-CoV-2 infection may result in long-term effects on immune processes within the CNS by causing microglial dysfunction. This short opinion aims to discuss the hypothesis that the pathogenesis of long-term neuropsychiatric COVID-19 involves microglia, mitochondria, and persistent neuroinflammation.

Source: Stefano GB, Büttiker P, Weissenberger S, Martin A, Ptacek R, Kream RM. Editorial: The Pathogenesis of Long-Term Neuropsychiatric COVID-19 and the Role of Microglia, Mitochondria, and Persistent Neuroinflammation: A Hypothesis. Med Sci Monit. 2021 May 10;27:e933015. doi: 10.12659/MSM.933015. PMID: 34016942. https://pubmed.ncbi.nlm.nih.gov/34016942/

Dysregulated Provision of Oxidisable Substrates to the Mitochondria in ME/CFS Lymphoblasts

Abstract:

Although understanding of the biomedical basis of Myalgic Encephalomyelitis/Chronic Fatigue Syndrome (ME/CFS) is growing, the underlying pathological mechanisms remain uncertain. We recently reported a reduction in the proportion of basal oxygen consumption due to ATP synthesis by Complex V in ME/CFS patient-derived lymphoblast cell lines, suggesting mitochondrial respiratory inefficiency. This was accompanied by elevated respiratory capacity, elevated mammalian target of rapamycin complex 1 (mTORC1) signaling activity and elevated expression of enzymes involved in the TCA cycle, fatty acid β-oxidation and mitochondrial transport. These and other observations led us to hypothesise the dysregulation of pathways providing the mitochondria with oxidisable substrates.

In our current study, we aimed to revisit this hypothesis by applying a combination of whole-cell transcriptomics, proteomics and energy stress signaling activity measures using subsets of up to 34 ME/CFS and 31 healthy control lymphoblast cell lines from our growing library. While levels of glycolytic enzymes were unchanged in accordance with our previous observations of unaltered glycolytic rates, the whole-cell proteomes of ME/CFS lymphoblasts contained elevated levels of enzymes involved in the TCA cycle (p = 1.03 × 10-4), the pentose phosphate pathway (p = 0.034, G6PD p = 5.5 × 10-4), mitochondrial fatty acid β-oxidation (p = 9.2 × 10-3), and degradation of amino acids including glutamine/glutamate (GLS p = 0.034, GLUD1 p = 0.048, GOT2 p = 0.026), branched-chain amino acids (BCKDHA p = 0.028, BCKDHB p = 0.031) and essential amino acids (FAH p = 0.036, GCDH p = 0.006). The activity of the major cellular energy stress sensor, AMPK, was elevated but the increase did not reach statistical significance. The results suggest that ME/CFS metabolism is dysregulated such that alternatives to glycolysis are more heavily utilised than in controls to provide the mitochondria with oxidisable substrates.

Source: Missailidis D, Sanislav O, Allan CY, Smith PK, Annesley SJ, Fisher PR. Dysregulated Provision of Oxidisable Substrates to the Mitochondria in ME/CFS Lymphoblasts. Int J Mol Sci. 2021 Feb 19;22(4):2046. doi: 10.3390/ijms22042046. PMID: 33669532; PMCID: PMC7921983. https://www.mdpi.com/1422-0067/22/4/2046/htm (Full text)

Role of mitochondria, oxidative stress and the response to antioxidants in myalgic encephalomyelitis/chronic fatigue syndrome: a possible approach to SARS-CoV-2 ‘long-haulers’?

Abstract:

A significant number of SARS-CoV-2 (COVID-19) pandemic patients have developed chronic symptoms lasting weeks or months which are very similar to those described for myalgic encephalomyelitis/chronic fatigue syndrome. This paper reviews the current literature and understanding of the role that mitochondria, oxidative stress and antioxidants may play in the understanding of the pathophysiology and treatment of chronic fatigue. It describes what is known about the dysfunctional pathways which can develop in mitochondria and their relationship to chronic fatigue. It also reviews what is known about oxidative stress and how this can be related to the pathophysiology of fatigue, as well as examining the potential for specific therapy directed at mitochondria for the treatment of chronic fatigue in the form of antioxidants. This review identifies areas which require urgent, further research in order to fully elucidate the clinical and therapeutic potential of these approaches.

Source: Wood E, Hall KH, Tate W. Role of mitochondria, oxidative stress and the response to antioxidants in myalgic encephalomyelitis/chronic fatigue syndrome: a possible approach to SARS-CoV-2 ‘long-haulers’? Chronic Dis Transl Med. 2020 Nov 21. doi: 10.1016/j.cdtm.2020.11.002. Epub ahead of print. PMID: 33251031; PMCID: PMC7680046.  https://pubmed.ncbi.nlm.nih.gov/33251031/

A systematic review of mitochondrial abnormalities in myalgic encephalomyelitis/chronic fatigue syndrome/systemic exertion intolerance disease

Abstract:

Background: Patients with Myalgic Encephalomyelitis/Chronic Fatigue Syndrome (ME/CFS) or Systemic Exertion Intolerance Disease (SEID) present with a constellation of symptoms including debilitating fatigue that is unrelieved by rest. The pathomechanisms underlying this illness are not fully understood and the search for a biomarker continues, mitochondrial aberrations have been suggested as a possible candidate. The aim of this systematic review is to collate and appraise current literature on mitochondrial changes in ME/CFS/SEID patients compared to healthy controls.

Methods: Embase, PubMed, Scopus and Medline (EBSCO host) were systematically searched for articles assessing mitochondrial changes in ME/CFS/SEID patients compared to healthy controls published between January 1995 and February 2020. The list of articles was further refined using specific inclusion and exclusion criteria. Quality and bias were measured using the Joanna Briggs Institute Critical Appraisal Checklist for Case Control Studies.

Results: Nineteen studies were included in this review. The included studies investigated mitochondrial structural and functional differences in ME/CFS/SEID patients compared with healthy controls. Outcomes addressed by the papers include changes in mitochondrial structure, deoxyribonucleic acid/ribonucleic acid, respiratory function, metabolites, and coenzymes.

Conclusion: Based on the included articles in the review it is difficult to establish the role of mitochondria in the pathomechanisms of ME/CFS/SEID due to inconsistencies across the studies. Future well-designed studies using the same ME/CFS/SEID diagnostic criteria and analysis methods are required to determine possible mitochondrial involvement in the pathomechanisms of ME/CFS/SEID.

Source: Holden S, Maksoud R, Eaton-Fitch N, Cabanas H, Staines D, Marshall-Gradisnik S. A systematic review of mitochondrial abnormalities in myalgic encephalomyelitis/chronic fatigue syndrome/systemic exertion intolerance disease. J Transl Med. 2020;18(1):290. Published 2020 Jul 29. doi:10.1186/s12967-020-02452-3 https://translational-medicine.biomedcentral.com/articles/10.1186/s12967-020-02452-3 (Full text)

Mitochondria and Immunity in Chronic Fatigue Syndrome

Abstract:

It is widely accepted that the pathophysiology and treatment of myalgic encephalomyelitis/chronic fatigue syndrome (ME/CFS) could be considerably improved. The heterogeneity of ME/CFS and the confusion over its classification have undoubtedly contributed to this, although this would seem a consequence of the complexity of the array of ME/CFS presentations and high levels of diverse comorbidities.

This article reviews the biological underpinnings of ME/CFS presentations, including the interacting roles of the gut microbiome/permeability, endogenous opioidergic system, immune cell mitochondria, autonomic nervous system, microRNA-155, viral infection/re-awakening and leptin as well as melatonin and the circadian rhythm. This details not only relevant pathophysiological processes and treatment options, but also highlights future research directions.

Due to the complexity of interacting systems in ME/CFS pathophysiology, clarification as to its biological underpinnings is likely to considerably contribute to the understanding and treatment of other complex and poorly managed conditions, including fibromyalgia, depression, migraine, and dementia. The gut and immune cell mitochondria are proposed to be two important hubs that interact with the circadian rhythm in driving ME/CFS pathophysiology.

Source: Anderson G, Maes M. Mitochondria and immunity in chronic fatigue syndrome [published online ahead of print, 2020 May 26]. Prog Neuropsychopharmacol Biol Psychiatry. 2020;109976. doi:10.1016/j.pnpbp.2020.109976 https://pubmed.ncbi.nlm.nih.gov/32470498/

For ME/CFS patients, viral immunities come at a devastating, lifelong cost

Press Release: EurekAlert

Mylagic encephalomyelitis/chronic fatigue syndrome (ME/CFS) is a disabling and complex illness. Affected persons often cannot pursue ordinary activities — physical or mental — because of an incapacitating loss of energy and other symptoms, and may find themselves confined to bed or house-bound for years.

Anyone can develop ME/CFS, though it most commonly afflicts people between the ages of 40 and 60; women more often than men. In nearly every case, ME/CFS begins after a sequence of severe environmental exposures, injuries or infections. Until relatively recently, the utter mystery and complexity of ME/CFS persuaded some that it was not a “real” condition. In 2015, the National Academy of Medicine declared ME/CFS to be a serious, chronic, complex and systemic disease.

In a new study, to be published in the May 1, 2020 print edition of https://www.immunohorizons.org/content/4/4/201 ImmunoHorizons, a team of researchers at University of California San Diego School of Medicine and three German universities describe an underlying biological basis for ME/CFS, one that illustrates how efforts by the body to boost immune system protections can come at physiological cost elsewhere.

“These findings are important because they show for the first time that there is an antiviral activity in the serum of patients with ME/CFS that is tightly associated with an activity that fragments the mitochondrial network and decreases cellular energy (ATP) production,” said Robert Naviaux, MD, PhD, professor of medicine, pediatrics and pathology at UC San Diego School of Medicine.

Naviaux is co-senior author of the study with Bhupesh K. Prusty, PhD, a scientist in the Department of Microbiology and Institute for Virology and Immunobiology at Julius Maximilians University in Würzburg, Germany.

“This provides an explanation for the common observation that ME/CFS patients often report a sharp decrease in the number of colds and other viral infections they experience after they developed the disease. Our work also helps us understand the long-known, but poorly understood link of ME/CFS to past infections with Human Herpes Virus-6 (HHV-6) or HHV-7,” said Naviaux.

More than 90 percent of people are exposed to HHV-6 by three years of age. The virus DNA can insert itself into a chromosome and remain latent in just a few cells for years, silently being copied each time the cell divides. For most people, this causes no problem.

“However, we found that exposure to new metabolic or environmental chemical stresses caused cells with an integrated copy of HHV-6 to secrete an activity that warned neighboring cells of the threat,” said Naviaux. “The secreted activity not only protected neighboring and distant cells from new RNA and DNA virus infections, but also fragmented the mitochondrial network and lowered their intracellular ATP reserve capacity. Cells without an integrated copy of HHV-6 did not secrete the antiviral activity.

“Our results show that cellular bioenergetic fatigue and cellular defense are two sides to the same coin in ME/CFS. When energy is used for cellular defense, it is not available for normal cell functions like growth, repair, neuroendocrine and autonomic nervous system functions.”

The findings further illuminate a concept called cell danger response theory, which Naviaux and colleagues have been investigating for years. CDR theory posits that chronic disease is the consequence of the natural healing cycle becoming blocked by disruptions at the metabolic and cellular levels. In this case, persons with ME/CFS obtained protections against certain kinds of infections, but at a cost of fragmenting mitochondrial function. Persistence of fragmented mitochondria and the associated abnormalities in cell signaling block normal healing and recovery, and can lead to a lifetime of illness.

Mitochondria are organelles in cells that break down nutrients to create a fuel called adenosine triphosphate (ATP), the primary energy carrier in all living organisms. ATP provides the energy used to drive many cellular processes, including muscle contractions, nerve impulses and chemical synthesis.

“This paper will be a paradigm shift in our understanding of potential infectious causes behind ME/CFS. Human herpesvirus 6 and HHV-7 have long been thought to play a role in this disease, but there was hardly any causative mechanism known before,” said senior co-author Prusty.

“For the first time, we show that even a few HHV-6 infected or reactivated cells can drive a powerful metabolic and mitochondrial remodeling response that can push even the non-virus containing cells towards a hypometabolic (abnormally low metabolic) state. Hypometabolic cells are resistant to other viral infections and to many environmental stresses, but this comes at the cost of severe symptoms and suffering for patients with ME/CFS.”

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Co-authors include: Philipp Schreiner, Stephanie Lamer and Andreas Schlosser, Julius-Maximilians University, Germany; Thomas Harrer, University of Erlangen-Nuremberg; and Carmen Scheibenbogen, Charite-Universitatsmedizin Berlin.

Metabolic Dysfunction in Myalgic Encephalomyelitis/Chronic Fatigue Syndrome Not Due to Anti-mitochondrial Antibodies

Abstract:

Metabolic profiling studies have recently indicated dysfunctional mitochondria in myalgic encephalomyelitis/chronic fatigue syndrome (ME/CFS). This includes an impaired function of pyruvate dehydrogenase complex (PDC), possibly driven by serum factor(s), which leads to inadequate adenosine triphosphate generation and excessive lactate accumulation. A reminiscent energy blockade is likely to occur in primary biliary cholangitis (PBC), caused by anti-PDC autoantibodies, as recently proposed. PBC is associated with fatigue and post-exertional malaise, also signifying ME/CFS. We herein have investigated whether ME/CFS patients have autoreactive antibodies that could interfere with mitochondrial function.

We found that only 1 of 161 examined ME/CFS patients was positive for anti-PDC, while all PBC patients (15/15) presented significant IgM, IgG, and IgA anti-PDC reactivity, as previously shown. None of fibromyalgia patients (0/14), multiple sclerosis patients (0/29), and healthy blood donors (0/44) controls showed reactivities. Anti-mitochondrial autoantibodies (inner and outer membrane) were negative in ME/CFS cohort. Anti-cardiolipin antibody levels in patients did not differ significantly from healthy blood donors.

In conclusion, the impaired mitochondrial/metabolic dysfunction, observed in ME/CFS, cannot be explained by presence of circulating autoantibodies against the tested mitochondrial epitopes.

Copyright © 2020 Nilsson, Palmer, Apostolou, Gottfries, Rizwan, Dahle and Rosén.

Source: Nilsson I, Palmer J, Apostolou E, Gottfries CG, Rizwan M, Dahle C, Rosén A. Metabolic Dysfunction in Myalgic Encephalomyelitis/Chronic Fatigue Syndrome Not Due to Anti-mitochondrial Antibodies. Front Med (Lausanne). 2020 Mar 31;7:108. doi: 10.3389/fmed.2020.00108. eCollection 2020. https://www.frontiersin.org/articles/10.3389/fmed.2020.00108/full (Full text)