Increased Oxidative Stress and NLRP3 Inflammasome Activation May Drive “Cytokine Storms” in Aging, Type 2 Diabetes, Cardiovascular Disease, Obesity and Hypertension in Persons with SARS-CoV-2 Infections

James P. Bennett, Jr.

Neurodegeneration Therapeutics, Inc.

Charlottesville, VA 22901

Correspondence:

James P. Bennett, Jr. M.D. Ph.D.

Neurodegeneration Therapeutics, Inc.

3050A Berkmar Drive

Charlottesville, VA 22901-3450

PH: (434) 529-6457

FAX: (434) 529-6458

jpb8u@icloud.com

www.NDTherapeutics.org

Abstract

Infections with SARS-CoV-2 virus result in symptoms of a syndrome now referred to as COVID-19 that have increased morbidity and mortality (M&M) in aged persons, particularly those with underlying medical conditions such as obesity, type 2 diabetes mellitus (T2DM), cardiovascular disease/atherosclerosis, and hypertension (HTN). Much of this increased M&M appears to arise from “cytokine storms”, overproduction of toxic cytokines that are part of the normal immune response. Because these underlying medical conditions are associated with increased oxidative stress (O.S.) and NLRP3 inflammasome activation, infection with SARS-CoV-2 virus may trigger a toxic feed-forward “cytokine storm”.

In this paper I review the recent data concerning how increased O.S. (overproduction of oxidative/nitrative species) and NLRP3 activation are associated with all of these conditions that can yield increased M&M in SARS-CoV-2 infections. Recently, adverse interactions of SARS-CoV-2 proteins with mitochondrial machinery have been described. Both may result in damage to mitochondrial DNA (mtDNA), a recognized activator of NLRP3 inflammasome.

Mitochondrial dysfunction leading to O.S. and NLRP3 inflammasome activation should now be considered as pathophysiological events producing cytokine storms with increased M&M in SARS-CoV-2 infection of older persons with chronic medical conditions. Anti-oxidant chemicals can be safely administered to humans and/or experimental animals, leading to reduction of O.S. Inhibitors of NLRP3 inflammasome are also known. Antioxidants and NLRP3 inflammasome inhibitors may thus comprise part of a combinatorial approach to SARS-CoV-2 infections and may prevent cytokine storms in susceptible persons. (233 words)

Introduction

Exposure to the highly infectious SARS-CoV-2 virus has resulted in an international pandemic in only a few months. While some infected persons (generally young) have minimal or no symptoms, older individuals (1, 2), particularly those with chronic medical conditions such as cardiovascular disease/atherosclerosis, T2DM, hypertension (HTN) or obesity can develop multiple organ failure and death. To date, over 140,000 persons in the United States alone have died from SARS-CoV-2 infection since January, 2020.

O.S. is a biochemical state that results from production of oxidative species, particularly free radicals (molecules with unpaired electrons), in greater abundance than can be detoxified by endogenous anti-oxidative systems. Most free radicals are believed to originate from electrons that inappropriately leave the electron transport chain (ETC) of mitochondria and reduce nearby molecules. Superimposed infection with SARS-CoV-2 and resulting mitochondrial damage in the setting of baseline impaired mitochondrial function in older persons with chronic medical diseases may further activate NLRP3 inflammasomes and lead to deadly “cytokine storms” (1, 3-5).

The inflammasome is a multiprotein complex that is an important part of the innate immunity system (6). Inflammasomes recruit pro-caspase 1 via an adapter molecule known as ASC (apoptosis-associated speck-like protein containing a caspase recruitment domain (CARD)). Active caspase 1 cleaves pro-interleukin 1-beta (pro-IL-1) and pro-interleukin 18 (pro-IL-18) into mature IL-1and mature IL-18, respectively. Activated inflammasomes also initiate a form of cell death known as pyroptosis that is mediated by gasdermin D (GSDMD), which forms pores in the plasma membrane of cells.

Several inflammasomes have been described, including NLRP3, NLRP1, AIM2 and NLRC4 (6). NLRP3 is among the best characterized and most studied, and consists of the sensor molecule NLRP3 (contains a pyrin domain, PYD), the adaptor protein ASC (contains PYD and CARD domains) and pro-caspase 1 (contains CARD domain). Upon activation, the NLRP3 inflammasome consists of a NLRP3 protein-ASC-pro-caspase 1 complex.

Although it remains unclear why clinical outcomes are so varied, two potential unifying and interacting mechanisms are increased oxidative stress (O.S.) and NLRP3 inflammasome activation. O.S. has been shown to be present in aging (7-154), T2DM (7, 10, 19, 34-36, 48, 54, 56, 98, 112, 119, 121, 127, 130, 138, 155-279), hypertension (16, 21, 26, 34, 48, 52, 96, 98, 101, 107, 113, 114, 116-118, 120-122, 135, 160, 187, 189, 201, 206, 225, 254, 267, 271, 273, 275, 280-381), cardiovascular disease/atherosclerosis (9, 10, 29, 34, 35, 42, 44, 48-50, 62, 71, 97, 102, 103, 110, 114, 116-118, 120, 121, 156, 165, 169, 180, 183, 189, 195, 197, 199, 201, 205, 213, 220, 223-226, 232, 233, 241, 280-282, 284, 285, 289-291, 293-295, 297, 305, 307, 309, 311-313, 315, 318, 319, 321, 322, 324, 325, 327, 330, 333, 335, 339, 340, 342, 343, 348-350, 352, 355, 382-404) and obesity (19, 35, 36, 42, 44, 48, 49, 53, 56, 67, 69, 122, 137, 155, 156, 160, 164, 165, 169, 185, 186, 188, 189, 197, 200, 206, 216, 224, 225, 227, 228, 231, 232, 234, 242, 254, 266, 267, 272, 298, 324, 325, 340, 368, 370, 373, 383, 387, 388, 392, 393, 395, 397, 399-402, 405-470).

NLRP3 inflammasome activation has also been demonstrated in aging (“inflammaging”) (1, 22, 32, 62, 72, 78, 79, 84, 106, 117, 134, 137, 471-593), T2DM (156, 192, 214, 237, 246-248, 255, 267, 476, 492, 493, 496, 497, 508, 512, 526, 533, 538, 539, 594-718), hypertension (1, 5, 117, 267, 369, 373, 374, 485, 538, 561, 646, 698, 714, 719-823), cardiovascular disease/atherosclerosis (3, 62, 117, 137, 156, 391, 403, 492, 494, 496, 498, 501, 507, 512, 544, 545, 552, 553, 609, 611, 619, 634, 645, 647, 651, 661, 665, 683, 684, 687, 692, 695, 708, 719, 721, 727, 728, 730, 732, 736, 741, 744, 748, 752, 753, 759, 764, 765, 824-890) and obesity (3, 137, 156, 267, 373, 425, 431, 442, 444, 452, 460, 461, 483, 493, 496, 508, 510, 538, 539, 598, 599, 601, 603, 620, 623, 626, 627, 631-634, 636, 639-641, 643, 647, 651, 654, 661, 662, 664, 669, 672, 677, 678, 683, 688, 692, 696, 697, 699, 703, 707, 708, 733, 736, 739, 742, 747, 826, 829, 834, 842, 856, 857, 860, 869, 891-941).

Mitochondria are abundant organelles that are believed to have originated from endosymbiosis by early Archea of proto-bacteria containing metallo-proteins that could detoxify molecular oxygen. This “symbiosis” hypothesis of mitochondrial origin, while remaining controversial, has received extensive genetic and molecular biochemical support since first championed by Lynn Margulis (942-946).

Mitochondria are found in all terrestrial animals, almost all eukaryotic cells and metabolize chemical potential energy-containing substrates, ultimately derived from solar photons, to generate through the ETC a gradient of protons used to synthesize adenosine triphosphate (ATP), a universal energy currency. This process of electrons moving down the ETC linked to ATP production is known as oxidative phosphorylation (O.P.).

The mitochondrial ETC normally has very high efficiency, in the range of 98% or higher. But the efficiency is not 100%, with the net result that under basal conditions 6-8 liters of superoxide gas (O2*) are formed every 24 hrs in the course of O.P. and ATP production. At an efficiency of 98%, about 2.82 moles of “extra” ATP equivalent in electrons are injected into the ETC to meet the average 24 hr. needs of a 70 kg person (a 70 kg person needs ~70 kg ATP/24 hrs. = 138 moles ATP/24 hrs.). These 2.82 moles of “excess” ATP equivalent would require ~4.25X1024 electrons injected into and subsequently leaking from the ETC under normal coupling (~2.5 electrons/ATP molecule). If all leaked electrons form superoxide (O2*) and no electrons are scavenged, this would yield 7.05 moles of O2* gas, or about 179 liters of O2* gas assuming ideal behavior, 37 degrees C, 1 atmosphere pressure. That there are only 6-8 liters of O2* gas formed in 24 hrs. indicates that normally there is extensive scavenging of electrons leaking from the ETC in spite of an abundance of electrophilic molecular oxygen in the mitochondrial matrix.

O2* gas, formed in the mitochondrial matrix, is negatively charged and thus does not pass readily across the lipid-rich mitochondrial inner membrane (I.M.). What O2* gas is formed is rapidly dismutated to hydrogen peroxide by superoxide dismutase (SOD) enzymes. Genetic ablation of the mitochondrial isomer of SOD (SOD2, located mainly in mitochondrial matrix) is embryonic lethal, which indicates the essential role of SOD2 to remove mitochondrially generated O2* gas. Any O2* gas escaping to the cell cytoplasm or generated in compartments other than mitochondria is dismutated to hydrogen peroxide by SOD1, the cytosolic SOD, which may also be located in the mitochondrial inter-membrane space (I.M.S.) between the inner and outer mitochondrial membranes. In both cases, formed hydrogen peroxide is removed by catalase enzymes, which convert hydrogen peroxide to water and oxygen. In this manner, oxygen from O2* gas is “recycled” back to mitochondria. Other important ROS/RNS-scavenging enzymes include thioredoxins and peroxyredoxins.

Free electrons leaking from the ETC are scavenged ultimately by glutathione, which normally exists in the reduced form and serves as a cofactor for several enzymes that remove hydrogen peroxide (i.e. catalase) and other oxidants. During its use as a cofactor, glutathione is oxidized to a disulfide that then is reduced/recycled to sulfhydryl (reduced) glutathione by the actions of glutathione reductase. Both mitochondria and cell cytoplasm contain high levels of reduced glutathione and the enzymes needed for its renewal.

Nitric oxide (NO) is a free radical gas used extensively in multiple signaling systems, is a vasodilator in many vascular beds and is synthesized by mitochondria through controversial mechanisms. NO can non-enzymatically combine with O2* to form peroxynitrite anion (ONOO), which is “trapped” in mitochondrial matrix by its negative charge, can nitrosylate tyrosine residues on proteins and can decompose spontaneously to yield the very reactive hydroxyl free radical (OH*) that is one of the most powerful oxidants known. OH* can also be formed non-enzymatically by the “Fenton reaction” between hydrogen peroxide and unbound ferrous ion (Fe+2) and is believed to oxidize the first molecule it comes into contact with. “Reactive nitrogen species” (RNS) such as NO* and ONOO represent an additional component of damage to macromolecules both within and external to mitochondria and should be considered as contributory along with “reactive oxygen species” (ROS).

Under normal conditions little oxidative stress exists, as most escaping electrons are scavenged (see above) and ROS/RNS, which are mainly but not exclusively formed in mitochondria, are chemically detoxified. However, ROS/RNS are not removed completely and gradually can cause accumulated oxidative/nitrative damage to multiple cellular constituents, including DNA, RNA, proteins and certain lipids of cells. Mitochondrial DNA (mtDNA), a separate circular genome ~16kb in size, maternally inherited and found normally as multiple copies in each mitochondrial matrix, has limited protein protection (in contrast to histones and nuclear genomic DNA) and capacity to repair damage from ROS/RNS. Thus, mtDNA is a target of ROS/RNS, is damaged ~10-fold during aging compared to nuclear genomic DNA, and is a noted activator of the NLRP3 inflammasome (516, 532, 590, 612, 680, 704, 729, 732, 740, 822, 874, 907, 947-956).

SARS-CoV-2 Virus and Mitochondria

Anand and Tikoo, who published their review in 2013 (957), discuss how viruses other than CoV2 can alter mitochondrial function. Singh, et al (2), recently reported that viral RNA of SARS-CoV-2 virus, which is similar to viral RNA of SARS-CoV1 virus, may localize in mitochondria leading to “hijacking” of mitochondria, and that viral proteins may alter mitochondrial functions and mitochondrial involvement in innate immunity.

Mitochondria should be considered as potential targets of infection by several viruses, including SARS-CoV-2. In addition, mitochondrial damage leading to oxidative stress is a recognized activator of the NLRP3 inflammasome (62, 78, 79, 134, 137, 192, 214, 267, 391, 431, 486, 488, 492, 516, 529, 532, 534, 554, 555, 572, 589, 590, 593, 595-597, 612, 615, 620, 648, 661, 675, 680, 684, 689, 699, 704, 708, 709, 711, 715, 728, 729, 732, 740, 744, 751, 752, 757, 766, 767, 783, 785, 805, 807, 819, 822, 864, 865, 869, 874, 878, 907, 923, 925, 926, 929, 932, 937, 948-956, 958-1000), which has been described as over-activated in aging, hypertension, obesity, cardiovascular disease and T2DM (see above).

Assessing Oxidative Stress in Humans

Animal and human tissues and cells have been shown to accumulate oxidative damage to nucleic acids such as DNA and RNA, leading to the adducts 8-hydroxy-deoxy guanosine (8-OHdG, DNA) and 8-hydroxy guanosine (8-OHG, RNA), respectively, among many others. These oxidative nucleic acid derivatives can lead to DNA copying errors, or RNA translation errors. These oxidative nucleic acid derivatives are more common in mitochondrial DNA (mtDNA) and mitochondrial RNA (mtRNA), presumably reflecting both the physical proximity of mtDNA and mtRNA to ROS/RNS formed by the ETC, limited protein protection of mtDNA and reduced capacity in mitochondria to repair such damages. ROS/RNS damage to proteins is conveniently assayed by protein carbonyl or nitrotyrosine content, and ROS/RNS damage to lipids is conveniently assayed by hydroxynonenal (HNE) content.

Because the human brain disproportionately uses metabolic fuels and oxygen (2-3% of body weight, 20-25% of total metabolic fuel and oxygen consumption), it is particularly damaged by ROS during the lifespan. Brain oxidative stress may underlie reduced brain energy transformation during aging and onset of neurodegenerative diseases. Brain oxidative stress may underlie the encephalopathy associated with SARS-CoV-2 infection that is increasingly reported (1001-1011).

What Is(Are) the Origin(s) of O.S. Damage and NLRP3 Inflammasome Activation in Aging and Chronic Medical Conditions?

There is likely no single answer to this question. If mitochondrial symbiosis survived evolutionary pressure due to favorable protection from molecular oxygen (a toxic “by-product” of photosynthesis) and survival of the “oxygen holocaust” (this is a controversial argument), then O.S. can be viewed as an inevitable consequence of respiring in an oxygen environment. By this argument, the chronic medical conditions discussed simply accelerate a process (O.S.) that would normally appear and lead to bioenergetic decline and ultimate death of the organism’s cells.

However, that may be too simplistic, and one should consider mechanisms operative that could both lead to O.S. and how O.S. results in inflammasome activation. In terms of O.S., one needs to consider that electrons are quantum entities flowing through the electron transport chain (E.T.C.), with both wave and particle properties depending on what kind of measurement is made. In mitochondria, the location of electrons in the E.T.C. is relatively defined, as is the speed of transit through the E.T.C.. Both of these properties defy the Heisenberg uncertainty principle, until one realizes that mitochondria are more properly regarded as macroscopic entities, far larger than the “Planck” size where the uncertainty principle is applicable.

Also, the concept of decoherence (loss of pure quantum behavior) (1012) may apply as electrons flow in a more macroscopic mitochondrial entity. Mitochondria may even convert electrons into a form of superconductivity, changing the electrons from fermions (particles with unique quantum states) into bosons that have identical quantum states. Normally superconductivity is found only at extremely low temperatures, so this idea must be regarded as very speculative.

Independently of how one views the physics of electron flow within mitochondria, the “bottom line” is that this electron flow is coupled (through as yet unclear mechanisms) to pumping of protons across the mitochondrial inner membrane (I.M.) into the inter-membrane space (I.M.S.). Mitochondria thus create a proton electrochemical gradient across the I.M.S./I.M. that is a form of potential energy and is used to convert ADP (adenosine diphosphate) into ATP (adenosine triphosphate) through the nanomotor enzyme ATP synthase (aka Complex V) by forcing a high-energy phosphorus-oxygen bond to be created.

Mitochondria can “leak” electrons at many locations. Under normal circumstances, electron flows through the Fe-sulfur complexes of Complex 1 at the beginning of the E.T.C. terminate in the reduction of ubiquinone (coenzyme Q10) to ubiquinol. At this juncture, electron flow to ubiquinone must compete thermodynamically with flow to molecular oxygen, which is energetically much more favorable. The reduction of ubiquinone is likely favored by having a very abundant concentration of ubiquinone relative to that of molecular oxygen at that location in Complex I. However, some electron leakage likely occurs at this point.

Further electron transfer from ubiquinol to the heme in oxidized cytochrome c protein in Complex III likely occurs within the restricted confines of the macromolecular assembly of Complexes I, III and IV recently described in mitochondria from several species’ tissues. Access to molecular oxygen again is likely physically restricted, even though reduction of molecular oxygen to water is more thermodynamically favored. Likely some electron leakage takes place here as well. The reduction of molecular oxygen to water finally occurs at Complex IV (aka cytochrome c oxidase), following re-oxidation of cytochrome c, with regulated electron flow from cytochrome c through the iron and copper complexes within complex IV to oxygen.

Proton pumping (protons are also quantum entities) occurs at Complexes I, III and IV. If the coupling between electron flow in the E.T.C. and proton pumping is reduced, and/or if the relative leak of protons across the I.M. increases, then more electrons/unit time will need to flow through the E.T.C. to maintain the proton gradient and support adequate ATP synthesis. This will likely increase the absolute amount of electron leakage from the E.T.C. and potentially increase O.S.

Electron flow rates through the E.T.C. may also be reduced. Electrons appear to utilize “quantum tunneling” to reduce activation energy barriers to flow through E.T.C. proteins (1013). If this mechanism of quantum tunneling becomes impaired, then rates of ATP synthesis may be reduced with the need for increased electron flow through the E.T.C., leading to more electron leakage and increased O.S.

Quantum tunneling sites on E.T.C. proteins may be damaged in two non-exclusive ways. First, previously normal proteins, particularly in assembled Complex I where tunneling has been most extensively studied, may be damaged by ROS/RNS generated over time. Second, most E.T.C. proteins, particularly those believed to be involved in electron transport, are coded by the nuclear genome and imported into mitochondria. They may be damaged at the level of cytosolic mRNA and defectively translated, damaged as cytosolic proteins after translation and prior to importation into mitochondria, or damaged after mitochondrial importation and assembly into E.T.C. Complexes.

How increased O.S. arises in the chronic medical conditions of aging, T2DM, HTN, cardiovascular disease and obesity remains to be determined. Whether increased O.S. in these conditions is causal or simply correlative is also not clear at this time. Likely, O.S. arises due to various combinations of mechanisms discussed above, in addition to mechanisms not discussed or not yet known.

How might O.S. lead to inflammasome activation? The likely culprit (and there are potentially many culprits) is mtDNA damaged by ROS/RNS and released by damaged mitochondria, either spontaneously or by means of mitochondrial autophagy (mitophagy). Such damaged mtDNA’s can not only drive mitophagy but can, through unknown mechanisms, activate inflammasomes, particularly the NLRP3 inflammasome most intensively studied (516, 532, 590, 612, 680, 704, 729, 732, 740, 822, 874, 907, 947-956). Inflammasome inhibitors are also known, some of which have been administered to humans (6).

Use of Antioxidants in Humans to Reduce Oxidative Stress

While there are dozens of known antioxidant molecules, both man-made and naturally occurring, relatively few combine mitochondrial matrix localization and successful administration to homo sapiens or animal models of human diseases. Those meeting both criteria include active molecules attached to triphenylphosphonium backbones, such as MitoQ10 (1014) and pramipexole isomers (1015, 1016). N-acetylcysteine, while not concentrated into mitochondria, can function as a glutathione repleting agent and exerts antioxidative effects. It has also been administered to humans (1017).

Conclusions

Oxidative Stress (O.S) arises mainly from mitochondria when production rates of reactive oxygen species (R.O.S.) and reactive nitrogen species (R.N.S.) exceed scavenging rates. O.S. damages mitochondrial components, specifically mtDNA, which can activate inflammasomes and lead to cytokine storms. Infection with SARS-CoV-2 virus, producing symptoms known as COVID-19, is itself toxic to mitochondria and can trigger cytokine storms in older subjects who have additional medical conditions such as T2DM, HTN, obesity and cardiovascular disease. A unifying mechanism is the increased O.S. and inflammasome activation in older persons with any of these additional chronic medical diseases, combined with SARS-CoV-2 infection.

If correct, this mechanism dictates therapy of SARS-CoV-2 infection in persons with any of the co-morbid conditions known to increase morbidity and mortality. A combinatorial therapeutic approach would consist of the early co-administration of mitochondrially targeted antioxidant and inflammasome inhibitor.

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