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Flavonoids in Modulation of Cell Survival Signalling Pathways

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Flavonoids in Modulation of Cell Survival Signalling Pathways Genes Nutr (2014) 9:400 DOI 10.1007/s12263-014-0400-z REVIEW Flavonoids in modulation of cell survival signalling pathways Mohammad Lukman Mansuri • Priyanka Parihar • Isha Solanki • Mordhwaj S. Parihar Received: 13 December 2013 / Accepted: 18 March 2014 / Published online: 30 March 2014 Ó Springer-Verlag Berlin Heidelberg 2014 Abstract Flavonoids, a family of polyphenols, generally Introduction found in various fruits and vegetables, as well as in many plant beverages such as tea, pomegranate juice, raspberry, Flavonoids are a subclass of polyphenols, derived from blueberries, and red wine. Recently, studies on flavonoids plants secondary metabolism. They play important roles in have attracted scientific attention as a potential nutritional the plant biology and human health. Flavonoids have been strategy to prevent a broad range of chronic disorders. referred to as ‘‘nature’s biological response modifiers’’ Many studies suggest that consumption of these flavonoids because of the strong experimental evidence of their in sufficient amount plays neuroprotective, cardioprotec- inherent ability to modify the body’s reaction to allergens, tive, anti-inflammatory, and chemopreventive roles. While viruses, and carcinogens. They show anti-allergic, anti- there has been a major focus on the antioxidant properties, inflammatory, anti-microbial, and anti-cancer activities. there is an emerging view that flavonoids and their in vivo Evidences strongly support the contribution of flavonoids metabolites do not act only as conventional antioxidants in the prevention of cardiovascular diseases (Mursu et al. but may also exert modulatory actions on cellular system 2008), neurodegenerative diseases (Scalbert et al. 2005), through direct action on various signalling pathways. These coronary heart disease (Knekt et al. 2002), cancers (Bel- pathways include phosphoinositide 3-kinase, Akt/protein guise et al. 2007; Hazgui et al. 2008), and osteoporosis kinase B, mitogen-activated protein kinase, tyrosine kina- (Choi 2011). There is also a growing interest in the ses, and protein kinase C. Various inhibitory or stimulatory potential of flavonoids to improve memory, learning, and actions of flavonoids on these pathways greatly affect general cognitive ability (Spencer 2008). Many studies cellular functions by altering the phosphorylation state of have shown that this contribution is mainly due to the targeted molecules. In addition, flavonoids also modulate antioxidant power of particular flavonoids and flavonoid- various gene expressions through activation of various rich extracts (Chen et al. 2000; Rice-Evans 1995, 2001). transcription factors. Thus, the present review will bestow Flavonoids are characterized by possessing two or more a breathing overview regarding the prime role of flavonoids aromatic rings, each bearing at least one hydroxyl group and in modulation of survival signalling pathways at cellular connected with a carbon bridge (Clifford 2001). Depending system. on structural features, flavonoids can be subdivided into following subclasses; (1) flavones (e.g., apigenin, luteolin, Keywords Plant polyphenols Á Phosphoinositide and tangeretin), (2) flavonols (e.g., kaempferol, quercetin, 3-kinase Á Akt/protein kinase B Á Mitogen-activated protein myricetin, and rhamnazin), (3) isoflavones (e.g., daidzein, kinase Á Protein kinase C Á Cell survival genistein), (4) flavanones (e.g., hesperetin, naringenin, and eriodictyol), (5) flavonols (e.g., silibinin, taxifolin, and di- hydrokaempferol), (6) flavonols [e.g., (?)-catechin, (-)- epicatechin, epigallocatechin, and epigallocatechin gallate & M. L. Mansuri Á P. Parihar Á I. Solanki Á M. S. Parihar ( ) (EGCG)], (7) anthocyanidins (e.g., pelargonidin, cyanidin, School of Studies in Zoology and Biotechnology, Vikram University, Ujjain, MP, India delphinidin, and malvidin) (Vauzour 2012). The wide- e-mail: [email protected] spread distribution of flavonoids, their variety, and their 123 400 Page 2 of 9 Genes Nutr (2014) 9:400 in the pathogenesis of various diseases (Williams et al. 2004). Evidences are mounting to show that flavonoids and their metabolites may exert modulatory actions in cells through actions on protein kinase and lipid kinase signalling pathways. The signalling pathways which are targets of flavonoids include phosphatidylinositol-3 kinase (PI3K) (Choi 2011; Kyoung et al. 2010; Lin et al. 2012), protein kinase B (Akt/PKB) (Hwang and Yen 2009; Kyoung et al. 2010; Vauzour et al. 2007), protein kinase C (PKC) (Luo et al. 2012; Levites et al. 2002), and mitogen-activated protein kinase (MAPK) (Huang et al. 2007; Hwang and Yen 2009; Kyoung et al. 2010; Park et al. 2011; Vauzour et al. 2007) (Fig. 1). Inhibitory or stimulatory actions on these pathways by flavonoids greatly affect cellular functions by altering the phos- phorylation state of target molecules and by modulating gene expression (Table 1). In this review, we provide thorough overview of role of various flavonoids on dif- ferent cell survival signalling pathways. Signalling pathways targeted by flavonoids Fig. 1 Schematic representation of interaction of flavonoids with cell During the last decade, important advances have been made signalling pathways. As shown in figure, flavonoids activate various signalling pathways such as ERK, Akt/PKB, PI3K, and PKC to in our understanding of the molecular events underlying improve the cell survival. The symbol arrows show the activation, cellular responses to extracellular signals. The cell signalling and the symbol box drawings light up and horizontal show is a critically important mechanism for the multicellular deactivation of various signalling pathways. ERK extracellular organisms including human beings particularly for inflam- signal-regulated protein kinase; JNK c-Jun N-terminal kinase; PI3K phosphatidylinositol-3 kinase; PKC protein kinase C; Akt/PKB matory, cardiac, and neurological functions. In many dis- protein kinase B; ARE antioxidant response element; CREB cAMP eases, the signal transduction mechanisms responsible for response element-binding protein; Nrf2 nuclear factor (erythroid- inducing cell survival and apoptosis (cell death) have been derived 2)-like 2; PM plasma membrane identified. In recent years, there is much emphasis on the role of flavonoids in modulation of signalling pathways espe- relatively low toxicity compared to other active plant cially during various diseases (Fu et al. 2010; Hwang and metabolites (for instance alkaloids) had led to consumption Yen 2009; Kyoung et al. 2010; Rainey et al. 2008; Vauzour by human beings in significant quantities (Isaac et al. 2011). et al. 2007). Evidences indicate that cell signalling contin- The main dietary sources of flavonoids are fruits, vegeta- uously declines with ageing (Miyamoto et al. 2013; Naidoo bles, and plant-derived beverages such as tea, coffee, and et al. 2008) and these processes are subjected to alterations red wine. However, there is still a difficulty in determining during cardiovascular diseases, neurodegenerative diseases, the dose for the daily intake of flavonoids because of the etc. (Lakatta and Levy 2003a, b; Rice and Curran 1999). complexity of existence from various food sources and the Thus, there is a new emerging view to cure such diseases by occurrence of a large amount of flavonoids itself in nature. modulating the intracellular signalling pathways by use of The molecular actions of flavonoids are largely various natural compounds. It is for this reason that cell dependent on their bioavailability at the target tissue, and signalling pathways have come to be appreciated as attrac- now it has been clear that the concentrations of flavonoids tive targets for drug development. We discuss here the role of and their metabolite forms accumulated in vivo (Manal flavonoids in targeting various cell survival signalling et al. 2006) are lower than those recorded for small- pathways including PKC, MAPKs, and PI3K/Akt. molecule antioxidant nutrients such as ascorbic acid and a-tocopherol (Halliwell et al. 2005). There is a new emerging view that if flavonoids have any preventive or PKC pathway curative activity through their ingestion, this effect must involve not only their antioxidant potential, but also the Protein kinase C is an integral part in the cell signalling modulation of multiple cellular pathways that are crucial machinery. Members of this enzyme family play distinct 123 Genes Nutr (2014) 9:400 Page 3 of 9 400 Table 1 Showing cell signalling pathways targeted by different flavonoids. Shows the effect of flavonoids observed in various cell signalling pathways. The activation of ERK, Akt/PKB, PI3K, and PKC is important to improve the cell survival, and the down-regulation of P38 and JNK is preventing the apoptosis. The activation of signalling pathways is shown as up arrow (:) and down-regulation of signalling pathways by flavonoids is shown in down arrow (;) S. Flavonoids Activation Signalling Cell line Response References no. (:), pathways deactivation (;) 01 ECG ; P38 HaCaT keratinocytes, Prevent apoptosis, oxidative Choi et al. (2005), Huang EGCG ; endothelial, rat primary stress, and endothelial et al. (2007), Yang et al. hepatocytes, Chinese barrier dysfunction, as (2010), Hwang and Yen Quercetin ; hamster lung fibroblast neuroprotective, for (2009), Huang et al. (2013), Hesperetin ; (V79-4) cells, BV2 treatment of chronic pain Meottia et al. (2007), Park Luteolin ; microglial cells, neuronal and neuroinflammatory et al. (2011), Liu et al. Myricitrin ; cells diseases, improve cognitive (2012) function, and mitochondrial
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