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María Marhuenda-Muñoz, S. Hurtado-Barroso, A. Tresserra-Rimbau, R. Lamuela-Raventós (2018)
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Mitochondria are highly dynamic organelles that are found in most eukaryotic organisms. It is broadly accepted that mitochondria originally evolved from prokaryotic bacteria, e.g. proteobacteria. The mitochondrion has its independent genome that encodes 37 genes, including 13 genes for oxidative phosphorylation. Accumulative evidence demonstrates that mitochondria are not only the powerhouse of the cells by supplying adenosine triphosphate, but also exert roles as signalling organelles in the cell fate and function. Numerous factors can affect mitochondria structurally and functionally. Carotenoids are a large group of fat-soluble pigments commonly found in our diets. Recently, much attention has been paid in carotenoids as dietary bioactives in mitochondrial structure and function in human health and disease, though the mechanistic research is limited. Here, we update the recent progress in mitochondrial functioning as signalling organelles in human health and disease, summarize the potential roles of carotenoids in regulation of mitochondrial redox homeostasis, biogenesis, and mitophagy, and discuss the possible approaches for future research in carotenoid regulation of mitochondrial function. Key words: β-carotene oxygenase 2; inflammation; mitochondrial DNA release; mitochondrial respiratory supercomplex; mito- chondrial signalling. Nowadays, mitochondria are recognized not only as the power- Introduction house of the cells by supplying adenosine triphosphate (ATP), but Mitochondria are highly specialized organelles that are found in also as signalling organelles in the cell fate and function (Myers and most eukaryotic organisms. Mitochondrial density differs by cell Slater, 1957; Bailis et al., 2019; Figure 1). Dysfunction of mitochon- types. For example, neutrophils and endothelial cells contain fewer drial is considered as a causial factor to the development of a series mitochondria, compared with the epithelial cells (Maianski et al., of chronic diseases, such as type 2 diabetes, obesity, cardiovascular 2004; Qian et al., 2005; Wilson et al., 2019). Red blood cells (or diseases, neurodegeneration, and some cancers (Kunej et al., 2007; erythrocytes) do not contain mitochondria (Zhang et al., 2011). Supale et al., 2013; Valero, 2014; Rigotto and Basso, 2019; Bianchi Evolutionally, it is broadly accepted that mitochondria were origin- et al., 2019). There are multiple factors causing dysfunctionality of ally derived from prokaryotic bacteria, e.g. proteobacteria (Youle, mitochondria, such as genetic mutation, environmental stimuli, life- 2019). The mitochondrion has its own independent genome that en- style, and eating behaviour in humans (Aon et al., 2016; Picard et al., codes 37 genes, including 13 genes for oxidative phosphorylation, 2016; Kramer and Bressan, 2018; Murphy and Hartley, 2018; Fang and the rest for building the machinery of the mitochondrial gene et al., 2019). Thus, prevention and/or protection of mitochondrial expression system (Chang et al., 1975; Taanman, 1999). Unlike nu- clear DNA, that comes from both parents, mitochondrial DNA is integrity and functionality are becoming a popular topic in the com- maternal inheritance in humans and most multicellular organisms munity, specifically during the pandemic of world-wide metabolic (Larsson and Clayton, 1995). diseases. © The Author(s) 2020. Published by Oxford University Press on behalf of Zhejiang University Press. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/ bync/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com Downloaded from https://academic.oup.com/fqs/article/4/3/115/5892227 by DeepDyve user on 03 November 2020 116 P. Lu et al., 2020, Vol. 4, No. 3 Figure 1. Mitochondria are not only the powerhouse of the cells by the synthesis of adenosine triphosphate (ATP), but also exert the roles in biogenesis and signalling. The mitochondrion has outer and inner membranes and the inter-membrane space. Inside the mitochondrial matrix, the tricarboxylic acid (TCA) cycle is carried out, producing reducing equivalents NADH and FADH2. They donate electrons to the electron transport chain, or the mitochondrial respiratory chain, resulting in generation of the cross-inner membrane proton gradient and subsequent production of ATP. The TCA cycle also synthesizes intermediate metabolites for biosynthesis of macromolecules, including fatty acids, nucleotides, heme, and others. Superoxide radicals, by-products of mitochondrial respiration, can be detoxified by mitochondrial superoxide dismutase (SOD2, or MnSOD) to H O , which then escape out of mitochondria. Accumulation of reactive oxygen 2 2 species (ROS) mainly superoxides within mitochondria may result in mitochondrial stress, leading to the release of mitochondrial DNA, cytochrome C, and apoptosis-inducing factor (AIF), and consequent inflammation and apoptosis. Mitochondria are also critical for calcikum singaling via buffering cellular calcium homeostasis. PDH, pyruvate dehydrogenase. Carotenoids are a large group of 40-carbon, fat-soluble pigments intermembrane space (IMS) and matrix. The outer membrane is commonly found in almost all higher plants, some microorganisms, permeable, whereas the inner membrane is highly selective and im- and a few marine products (Rodrigo-Baños et al., 2015; Galasso permeable (Hanstein and Hatefi, 1974). Thus, specific transport pro- et al., 2017; Rodriguez-Amaya, 2019; Balić and Mokos, 2019; teins are required for crossing the inner membrane of molecules, for Nedelec et al., 2019). Colourful carotenoids-containing foods are also example adenine nucleotide translocator (ANT) for ATP transport common in human diets. There is more than a dozen of carotenoids out of the matrix (Bauer et al., 1999). The mitochondrial matrix that have been identified in the human bloodstream, skin, macula, harbours the TCA (or Krebs) cycle, which utilizes pyruvate from the and other organs and tissues (Gimeno et al., 2001; Chacón-Ordóñez glycolysis to produce intermediate metabolites and reducing equiva- et al., 2019). It has been demonstrated that carotenoids are superb lents NADH and FADH2. These intermediate metabolites are used antioxidants exerting protective roles in human health (Rohrmann as essential molecules for biosynthetic pathways in cell metabolism. et al., 2004; Fiedor and Burda, 2014). On the other hand, circulatory NADH and FADH2 are the substrates of mitochondrial respira- carotenoid concentrations are tremendously lower in those groups tory complex I and complex II in the electron transport chain of of individuals with metabolic problems, such as type 2 diabetes and the inner mitochondrial membrane (Leverve et al., 2007). End prod- obesity (Polidori et al., 2000; Marhuenda-Muñoz et al., 2018). The ucts of the oxidative phosphorylation process include: 1. generation causality of low carotenoids under these disease conditions is still and maintenance of the mitochondrial membrane potential through controversial. In the past a couple of decades, some promising pro- pumping protons out to the IMS (through complexes I, III, and IV); gress has been made on better understanding how carotenoids alter 2. ATP production (through complex V); and 3. by-production of mitochondrial structure, metabolism, and function. Therefore, in this superoxide radicals (through complexes I, II, and III) (Raha et al., review, we will first look into the basic concepts of mitochondrial 2002; Kadenbach et al., 2010; Figures 1 and 2A ). Mitochondrial structure and function, followed by the possible effects of carotenoid superoxide dismutase (SOD2 or MnSOD) detoxifies superoxides metabolism on mitochondrial function in health and disease. At the to H O , which can then escape out of mitochondria (Keller et al., 2 2 end, we also discuss future pathways in the field of research. 1998; Buettner et al., 2006). The assembly of mitochondrial respiratory supercomplexes (SCs) has been characterized in the literature recently. The composition of Mitochondria as the Powerhouse—Brief SCs is complicated, including but not limited to SCs III +IV, III +IV , 2 2 2 Overview I +III , I +III +IV, I +III +IV (I +III +IV shown in Figure 2B, also see 2 2 2 2 2 The mitochondrion is a double-membrane-bound organelle. reviews (Qiu et al., 2013; Cogliati et al., 2016; Guo et al., 2017)). SCs These two membranes form two aqueous compartments, e.g. significantly increase the mitochondrial respiration efficiency and Downloaded from https://academic.oup.com/fqs/article/4/3/115/5892227 by DeepDyve user on 03 November 2020 Carotenoid metabolism, 2020, Vol. 4, No. 3 117 Figure 2. Mitochondrial inner membrane phospholipid bilayers and the respiratory chain. (A) The respiratory chain consists of five complexes (from I to V) embedded in the mitochondrial inner membrane phospholipid bilayers. (B) Diagram of the formation of supercomplex I+III +IV. Of note, complex III always show in the form of homodimer. decrease production of superoxides, compared with the traditional Oxidized mtDNAs translocation to the cytoplasm and binding to fluid ETC model (Figure 2A; Greggio et al., 2017; Lobo-Jarne et al., an NLRP3 inflammasome account for macrophage activation (Ilic 2018). The underlying mechanism by which SC formation remains et al., 2019). However, it is not clear whether the newly synthesized elusive. It would be interesting to explore whether and how the com- entire mtDNA strand or fragmented mtDNA plays the distinct roles position and oxidation status of phospholipids and embedding of in inflammation. Further investigation is also needed to explore the carotenoids alter the dynamics of SCs in health and disease. extent to which oxidized mtDNAs translocate out of mitochon- dria. The research provides a new direction towards a better under- standing of mitochondria as signalling organelle in mammals. Mitochondrial Signalling in Inflammation As illustrated in Figure 1, mitochondria are signalling organelles, as Carotenoid Metabolism evidenced by altering intermediate metabolites in the TCA cycle, cal- cium homeostasis, production of superoxides and ROS, and release The general structure of carotenoid is a 40-carbon polyene chain of a few apoptotic signal molecules, for example oxidized mitochon- with 9–11 double bonds, indicating high reducing potential. drial DNA (mtDNA). Please refer to the excellent reviews newly Carotenoids are fat-soluble pigments often found in colourful fruits, published in mitochondrial calcium homeostasis, oxidative stress, vegetables, egg yolks, and some marine products. They have long and TCA cycle as a biosynthetic hub (Susin et al., 1999; Li et al., been recognized as essential nutrients and important health benefi- 2000; McArthur et al., 2018). Here, we emphasize on the recent ad- cial compounds (Hammond and Renzi, 2013). There are two major vance in mtDNA signalling in immunity. subgroups of carotenoids: carotenes and xanthophylls (Hammond A recent study by Zhong et al. (2018) reported that macrophage and Renzi, 2013). Carotenes, also called pro-vitamin A carotenoids, mtDNA oxidation and release occurred when macrophage cells were such as α-carotene and β-carotene contain no oxygen atoms, which exposed to lipopolysaccharides (LPS) to mimic bacterial infection. are the major dietary sources of vitamin A. Differently, xanthophylls, Consequently, release of oxidized mtDNA resulted in Toll-like re- for example zeaxanthin, lutein, and astaxanthin, carry one or more ceptor 4 (TLR4) activation, which in turn triggered NACHT, LRR, oxygen atoms. Xanthophylls are more polarized than carotenes. The and PYD domains-containing protein 3 (NLRP3) inflammasome absorption of carotenoids is insufficient in humans (Brown et al., activation and subsequent interleukin 1 beta (IL-1β) production 1989). Although cooking process with other oils would increase the (Zhong et al., 2018). The study suggests that generation of high absorption efficiency, there are only ~10 % of dietary carotenoids levels of mitochondrial ROS is essential for oxidization of mtDNAs. that can be absorbed in the small intestine (Rubin et al., 2017). The Downloaded from https://academic.oup.com/fqs/article/4/3/115/5892227 by DeepDyve user on 03 November 2020 118 P. Lu et al., 2020, Vol. 4, No. 3 majority of dietary carotenoids are transported into the large intes- 2017; Guo et al., 2017). These animals had moderate inflammation tine, where they could be fermented by gut microbiota, and presum- and exhibited some characters of metabolic syndrome. The param- ably affect homeostasis of the gut microbiome (Lyu et al., 2018; Wu eters of metabolic disorders are also presented in human subjects et al., 2020). with BCO2 mutations (Vergara et al., 2017; Zhao et al., 2019). There are two carotenoid cleavage enzymes in mammals. Cytosolic Therefore, it would be an important topic for further discussion β-carotene oxygenase 1 (BCO1) catalyses carotenes only at the 15, and investigation of whether BCO2 functions solely as a carotenoid 15′ double bond site, yielding two molecules of retinal, whereas mito- metabolic enzyme or a possible structural protein in mitochondrial chondrial β-carotene oxygenase 2 (BCO2) cleaves almost all kinds of function. carotenoids at the 9, 10 and/or 9′, 10′ double bonds to yield various apocarotenoid products in the inner membrane of mitochondria Carotenoids in Mitochondrial Redox (Lindqvist et al., 2005; Amengual et al., 2013). Mutations and gen- Homeostasis etic polymorphism in BCO1 and BCO2 are associated with inherited diseases, resulting from vitamin A deficiency and/or carotenoid accu- Carotenoids have been claimed as superb antioxidants, due to the mulation in the plasma and/or other tissues (Amengual et al., 2013). ability to quench singlet oxygen and to scavenge other free radicals Distinct patterns of BCO2 expression could suggest that BCO2 that may prevent and treat a wide range of chronic diseases, such as protein could exert a role independent of carotenoid metabolism (Wu age-related macular degeneration (Meyers et al., 2014). The vast ma- et al., 2017). Using the single-cell transcriptomics technique, Voigt et al. jority of published studies demonstrated the measures of ROS and (2019) found a relative deficiency of BCO2 in the human retinal foveal other oxidative stress markers after the application of carotenoids cells, compared with BCO2 levels in peripheral retinal cells. They sug- in vitro and/or in vivo. How carotenoids affect mitochondrial redox gested that BCO2 deficiency may account for preferential accumulation levels at the organelle level is not clear. of carotenoids within the macula. By contrast, other studies disagree with BCO2 enzymatic activation in the human retina (Li et al., 2014; Mitochondrial Biogenesis and Mitophagy Babino et al., 2015). Interesting enough, a couple of most recent pub- lications from the models of the wild and domestic chicken presented Mitochondria are highly dynamic. The turnover rate of mitochon- that BCO2 protein expression could be genetically changed during the dria is tissue-specific, ranged from a couple of days to a couple of evolution of modern chickens and in poultry breeding (Fallahshahroudi weeks (Gottlieb and Gustafsson, 2011). Mitophagy, the selective et al., 2019; Qanbari et al., 2019). In these studies, they measured the mitochondrial autophagy process, eliminates damaged and/or BCO2 expression and carotenoid accumulation in the chicken gener- dysfunctional mitochondria, and also links to mitochondrial bio- ated from the cross-breeding to introgress the ancestral BCO2 allele genesis, a process of synthesis of new mitochondria (Gottlieb and into domestic White Leghorn chickens. They found that the derived Carreira, 2010). Mitochondria retain the ability to fuse and divide, haplotype was associated with suppression of BCO2 expression in skin, and to form the cellular mitochondrial network which is mechan- muscle, and adipose tissue, where more carotenoid accumulation oc- ically regulated by a number of genes involved in the processes of curs, whereas BCO2 expression in liver or duodenum was not different. fusion, fission, mitophagy, biogenesis, and spatial movement along We recently reported that deficiency of BCO2 caused hepatic microtubules in most eukaryotic cells in response to cellular energy mitochondrial hyperactivation, suppression of SOD2, elevation of demand, cell cycle, and other cellular and environmental stress con- ROS levels, and mitochondrial stress in laboratory mice (Wu et al., ditions (Aon et al., 2016; Fu et al., 2019; Figure 3). Figure 3. Mitochondrial dynamics in mammalian cells. Mitochondrial biogenesis is a process controlled by nuclear and mitochondrial encoded genes. Fusion requires mitochondrial dynamin-like GTPase (OPA1) at the inner mitochondrial membrane and mitofusin 1 (MFN1) and mitochondrial membrane and mitofusin 2 (MFN2) at the outer mitochondrial membrane to promote the fusion process of mitochondria. Mitochondrial fission is promoted by the formation of dynamin- related protein l (DRP1) helical oligomers that wrap around and scission the mitochondrial outer membrane. Mitochondrial fission 1 protein (Fis1) plays a minor role in the fission process. The mitochondrial fragmentation, caused by fission, is essential for mitophagy and/or mitochondrial apoptosis, resulting in release of mtDNA. Downloaded from https://academic.oup.com/fqs/article/4/3/115/5892227 by DeepDyve user on 03 November 2020 Carotenoid metabolism, 2020, Vol. 4, No. 3 119 Genes mediating mitochondrial dynamics have largely been identified and characterized in the past decades. Briefly, increases in mitochondrial mass and number are essential for cell growth, which could be archived by the enhanced mitochondrial biogen- esis. Mitochondrial biogenesis can be induced by nutrient depletion, oxidative stress, and other environmental factors (Ruegsegger et al., 2018). Mitochondrial biogenesis requires orchestrating regulation of nuclear and mitochondrial encoded gene expression (Dominy and Puigserver, 2013). Peroxisome proliferator-activated receptor gamma coactivator 1 alpha (PGC-1α), peroxisome proliferator-activated receptor gamma (PPARγ), and nuclear factor erythroid 2-related factor 1 and 2 (NRF1/2) are genes required in biogenesis (Wu et al., 1999; Lin et al., 2004; Pejznochova et al., 2010). Mitochondrial fu- sion requires mitochondrial dynamin-like GTPase (OPA1) at the inner mitochondrial membrane and mitofusin 1 (MFN1) and MFN2 Figure 4. AMP-activated protein kinase (AMPK) plays a central role in at the outer mitochondrial membrane to promote the fusion pro- carotenoid regulation of mitochondrial biogenesis and mitophagy After cess of mitochondria (Ishihara et al., 2004; Olichon et al., 2007). absorption, carotenoids (including intact molecules and apocarotenoids, Mitochondrial fission is promoted by the formation of dynamin- the cleavage metabolites by BCO1 and/or BCO2) directly and/or indirectly related protein l (DRP1) helical oligomers that wrap around and interact with and activate AMPK, which subsequently triggers downstream signalling pathways involved in mitophagy and biogenesis. BCO1, β-carotene scission the mitochondrial outer membrane (Varadi et al., 2004). oxygenase 1; BCO2, β-carotene oxygenase 2. Mitochondrial fission 1 protein (Fis1) plays a minor role in the fis- sion process (Lee et al., 2004). Recent research shows that DRP1 but subsequently triggers downstream signalling pathways involved in not dynamins is required for mitochondrial fission (Fonseca et al., mitophagy and biogenesis, such as Unc-51 like autophagy activating 2019). This mitochondrial fragmentation is essential for mitophagy kinase 1 (ULK1) and peroxisome proliferator-activated receptor and/or mitochondrial apoptosis, resulting in the release of mtDNA, gamma coactivator 1 alpha (PGC-1α) (Tang et al., 2011; Yu et al., cytochrome C, and AIF. Serine/threonine-protein kinase Unc-51 like 2013; Lin et al., 2014; Kim and Kim, 2019; Figure 4). autophagy activating kinase 1 (ULK1) is involved in mitophagy in response to stress, starvation, and even cell growth and development (Fonseca et al., 2019). This mitophagy recycling process is benefi- Concluding Remarks and Future Pathways of cial for mitochondrial dynamics (Twig and Shirihai, 2011). Fusion Carotenoid Research could limit mitophagy and apoptosis (Gunst et al., 2013). The mito- The role of carotenoids in mitochondrial biology attracts much at- chondrial respiratory activity, including ATP production and ROS tention because of the superb antioxidant properties and potentials generation, is not always associated with the status of mitochondrial in the regulation of mitochondrial and whole-body metabolism in dynamics, though mitochondrial fission generally links to high levels mammals. Unfortunately, there are many unknowns in the signifi- of superoxides, and declined efficiency of oxidative phosphorylation, cance of mitochondrial signalling driven by carotenoid metabolism. e.g. reduced ATP yield (Willems et al., 2015). Complex structures and hydrophobic characters determine that ca- rotenoid metabolic mechanism is complicated in humans. The in- tegration of the role of carotenoids in mitochondrial biology and Carotenoid Regulation of Mitochondrial metabolism is still in its infancy. There are several interesting topics Dynamics need to be addressed shortly. First, what is the exact mechanism by Although many black boxes exist regarding carotenoid regulation which carotenoids are up-token and integrated into the mitochon- of mitochondrial dynamics, much promising and interesting re- drial membrane? What carotenoids and how do they exert the roles search has been conducted in the application of pure carotenoids in membrane phospholipid dynamics and residual protein func- and/or whole foods rich in certain kinds of carotenoids in feeding tionality? Next, what is the difference in neuronal mitochondrial cell cultures and/or laboratory rodents. The von Lintig team has dynamics versus hepatic mitochondria in regard to carotenoid func- conducted extensive studies on the impacts of β-carotene, lutein, tion? The spatial dynamics of mitochondria in neuronal axons and and zeaxanthin on lipid metabolism and mitochondrial function dendrites could be distinct. Lastly, whether and how non-absorbed using the unique systemic knockout mice lacking BCO1, BCO2, or carotenoids in the gut role mitochondrial function in distal organs both genes (Amengual et al., 2011; Lobo et al., 2012; Palczewski and/or tissues, such as the gut-brain axis (Vishwanathan et al., 2013; et al., 2014). The results proved that the accumulation of caroten- Jeon et al., 2018). oids decreases whole-body respiration rates in those knockout mice (Palczewski et al., 2016). In vitro studies in HepG2 cells in culture Author Contributions suggest that carotenoids activate AMP-activated protein kinase (AMPK) (Liu et al., 2019). Nanjaiah and Vallikanan further dem- PL, SYW, LW, and DL conducted the literature review, prepared the figures, onstrated the direct binding of lutein in reduced and oxidized forms and wrote the draft of the manuscript. DL revised and proofed the manuscript. to AMPK in their computerized docking simulation work (Nanjaiah and Vallikannan, 2019). Acknowledgements We and others also reported that AMPK activation is critical for pure carotenoids- and/or zeaxanthin-rich wolfberry-induced mito- The authors thank Ms. Sandra Peterson for the technical support and labora- chondrial biogenesis and mitophagy in obesity. AMPK activation tory management. Downloaded from https://academic.oup.com/fqs/article/4/3/115/5892227 by DeepDyve user on 03 November 2020 120 P. Lu et al., 2020, Vol. 4, No. 3 plasma and low-density lipoproteins. Journal of Chromatography. B, Bio- Conflict of Interest medical Sciences and Applications, 758(2): 315–322. The authors declare no conflict of interest Gottlieb R. 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Food Quality and Safety – Oxford University Press
Published: Oct 22, 2020
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