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Hong, J.H.; Lee, D. UPS and Ca2+ Signaling. Encyclopedia. Available online: https://encyclopedia.pub/entry/23261 (accessed on 26 July 2024).
Hong JH, Lee D. UPS and Ca2+ Signaling. Encyclopedia. Available at: https://encyclopedia.pub/entry/23261. Accessed July 26, 2024.
Hong, Jeong Hee, Dongun Lee. "UPS and Ca2+ Signaling" Encyclopedia, https://encyclopedia.pub/entry/23261 (accessed July 26, 2024).
Hong, J.H., & Lee, D. (2022, May 24). UPS and Ca2+ Signaling. In Encyclopedia. https://encyclopedia.pub/entry/23261
Hong, Jeong Hee and Dongun Lee. "UPS and Ca2+ Signaling." Encyclopedia. Web. 24 May, 2022.
UPS and Ca2+ Signaling
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This entry is adapted from the peer-reviewed paper 10.3390/antiox11050997

The ubiquitin–proteasome system (UPS) is the main proteolytic pathway by which damaged target proteins are degraded after ubiquitination and the recruit of ubiquitinated proteins, thus regulating diverse physiological functions and the maintenance in various tissues and cells. The UPS and Ca2+ signaling are interconnected, since each affects the other. The interconnected nature of these signals plays a critical role in regulating cellular functions. 

UPS calcium ER stress ubiquitin proteasome

1. Introduction

The homeostatic maintenance of protein levels or elimination of misfolded or oxidized proteins requires essential quality control processes such as the ubiquitin–proteasome system (UPS) and autophagy [1][2][3][4]. The UPS regulates the intracellular protein levels and mediates the cell cycle modulation, DNA repair, transcription, and apoptosis [5]. Gradationally, the UPS begins with sequential ubiquitination to produce a poly-ubiquitin chain on the target protein [6][7] and is mediated by ubiquitin ligases E1, E2, and E3, which bind ubiquitin to the lysine residues of the target protein [6]. Poly-ubiquitinated proteins are recruited to the 26S proteasome and degraded through proteasome complexes, including the 19S and 20S proteasome [8][9]. The 19S proteasome, which is called the cap of the proteasome, detects poly-ubiquitinated proteins leading to the 20S proteasome, where poly-ubiquitinated proteins are deubiquitinated to recycle ubiquitin proteins [8]. The 20S proteasome, which is composed of α and β subunits, degrades poly-ubiquitinated target proteins [9].
The crosstalk between UPS and oxidative stress has been addressed bilaterally. It is known that inhibitors of UPS induce oxidative or endoplasmic reticulum (ER) stress [10], and protein oxidation through proteasome malfunction has been suggested as a major cause of human diseases such as Alzheimer’s disease (AD) [11], osteoarthritis [12], asthma [13], atherosclerosis [14], and chronic obstructive pulmonary disease [15]. In addition, the activity of UPS is increased by oxidative stress for the degradation of oxidized proteins, and extensive oxidation impairs the components of the UPS [16]. For example, the H2O2-induced protein carbonyl group, which is the indicator of protein oxidation, is increased by the treatment of proteasome inhibitor MG-132 [17].
The increase of an intracellular Ca2+ concentration ([Ca2+]i) is a messenger signal of oxidative pathways. Oxidative stress triggers an increase of [Ca2+]i through the ER membrane Ca2+ channels [18], and on the contrary, Ca2+ influx induces the generation of reactive oxygen species (ROS) [19]. Ca2+ signaling has been extensively studied for the past several decades. Briefly, [Ca2+]i is initiated through two pathways via the release of Ca2+ from intracellular stores by various extracellular stimuli and the influx of Ca2+ through plasma membrane-associated Ca2+ channels, including voltage-gated Ca2+ channels (VGCCs), ligand-gated Ca2+ channels (LGCCs), and Ca2+ ATPases [20]. Increased [Ca2+]i induces versatile and universal Ca2+ signaling to regulate various cellular physiological functions [21], including muscle contraction [22], the release of neurotransmitters [23], T-cell development [24], and fluid secretion [25].
The disruption of proteasome triggers an imbalance of human health and diseases occur [26][27][28][29]. A change of the signaling messenger Ca2+ is an essential process in various diseases, including oxidative stress. Thus, researchers suggest that the studies of basic mechanisms for the UPS with Ca2+ establish the foundation for the therapy of proteasome-associated diseases. In this entry, researchers will discuss the current advances in the roles of Ca2+-related proteins and the pathways of Ca2+ signaling in the UPS. Although Ca2+ signaling and the UPS have critical roles in other organisms, including plants [30][31][32][33] and yeast [34][35][36][37], this entry focuses on the mammalian UPS for relating to therapeutic potentials.

2. The Relationship between the UPS and Ca2+ Signaling

2.1. UPS-Mediated Degradation of Ca2+-Related Proteins

The UPS and Ca2+ signaling are interconnected, since each affects the other. The interconnected nature of these signals plays a critical role in regulating cellular functions. The UPS regulates Ca2+ signaling through the degradation of Ca2+-related proteins. Ca2+ channels and transporters are distributed on the membranes of intracellular organelles or the plasma membrane. In this section, researchers will discuss the relationship between these systems and how this affects protein degradation.
The endoplasmic reticulum (ER) is a major intracellular Ca2+ store. On the ER membrane, inositol 1,4,5-trisphosphate receptor (IP3R) releases Ca2+ to the cytosol via the binding of released IP3 from phosphatidylinositol 4,5-bisphosphate (PIP2) [38][39]. Generally, PIP2 is hydrolyzed to IP3 by phospholipase C (PLC), which is stimulated by the G-protein-coupled receptor, and IP3 subsequently activates IP3R to release ER Ca2+ [38][39]. Ubiquitin ligase ring finger protein 170 (RNF170), which has three membrane-spanning helices, is localized to the ER membrane and binds to IP3R [40]. Ubiquitin ligase RNF170-induced UPS downregulates IP3R in rat pancreas cells and CHO cells [41][42][43]. A deletion of endogenous RNF170 increased the expression of IP3R1 [40]. In other words, the knock-down of RNF170 inhibits IP3R ubiquitination and degradation [40]. In addition, reactive oxygen species are involved in the proteasome-associated degradation of IP3R. H2O2 treatment enhances the proteasome-induced degradation of IP3R in vascular smooth muscle cells [44]. The treatment of MG-132 recovers the H2O2-induced degradation of IP3Rs [44]. Other ER resident proteins: sarco-/endoplasmic reticulum Ca2+-ATPase (SERCAs) and ryanodine receptors (RyRs) are also degraded by the UPS [23][45]. SERCAs are family to the ER-localized P-type cation ATPase that transports cytosolic Ca2+ to the ER [46][47]. Inhibition of the UPS with MG-132 increases SERCA expression [23]. Type-2 RyR (RyR2), which contributes to cardiac excitation–contraction coupling, is degraded by the UPS [45]. In the simulated ischemia–reperfusion of mouse cardiomyocytes, RyR2 is degraded by the UPS following the activation of the Ca2+-dependent cysteine protease calpain, which is activated during ischemia/reperfusion [45]. Although the studies of the relationship between the UPS and intracellular organelle-releasing Ca2+ have been well-developed in the ER, it is meaningful to investigate the effect of the UPS on Ca2+ channels and transporters on other intracellular organelles, including the mitochondria and Golgi apparatus.
Regulatory channels of Ca2+ signaling, store-operated Ca2+ channels (SOCCs), are stimulated by changes in the Ca2+ store levels. When the concentration of ER Ca2+ is depleted, stromal interaction molecule (STIM) senses the depleted ER, elicits oligomerization, and forms a complex with the Orai channels to induce Ca2+ influx [48]. The overexpression of E3 ubiquitin ligase reduces the surface expression of STIM1, and the treatment with MG-132 increases the store-operated Ca2+ entry (SOCE), a Ca2+ homeostatic process to regulate cellular functions, by rescuing the STIM1 expression [49], whereas the inhibition of the proteasome degrades STIM1 and STIM2 through the complementary activation of autophagy [50]. To maintain the cellular activity by the degradation of proteins, autophagy and the UPS are known to communicate with each other [5]. If one is inhibited, the other is activated to degrade proteins [5]. Thus, the inhibition of the UPS complementally stimulates autophagic flux to maintain the [Ca2+]i level. 
The N-type Ca2+ channel voltage-gated calcium channel (CaV)2.2, which induces peripheral neuron neurotransmission [51], is degraded via the UPS to maintain the precise modulation of its expression [52][53]. For example, the overexpression of Parkin, which is an E3 ligase, decreases the current of CaV2.2 through proteasome-induced degradation [52], and proteasome inhibition through MG-132 increases the current of CaV2.2 [53]. The degradation of CaV2.2 is induced by the light chain of microtubule-associated protein B through ubiquitin-conjugating enzyme E2 L3 (UBE2L3)-mediated ubiquitination [54]. UBE2L3 is an E2-type ubiquitin ligase that is related to the occurrence of various diseases, including rheumatoid arthritis, celiac disease, and Crohn’s disease [55]. The β-subunit of CaV2.2 protects against the excessive degradation of CaV2.2 and even the formation of polyubiquitin chains but not from the binds of one to four ubiquitins [56][57]. CaV1.2 is expressed in the brain, cardiomyocytes, pancreas, adrenal medulla, and bladder smooth muscle [58] and specifically initiates cardiac excitation-contraction coupling [59] and triggers smooth muscle contractions [60]. Similar to CaV2.2, the β-subunit of CaV1.2 promotes the trafficking of CaV1.2 to the plasma membrane to avoid the UPS [61]. The aberrant splicing variant form of the CaV1.2 β-subunit increases the UPS-induced degradation of CaV1.2, which triggers cardiac hypertrophy [62]. Galectin-1 (Gal-1), which reduces the current density of CaV1.2 [63], induces the proteasome-induced degradation of CaV1.2 by disrupting the CaV1.2 β-subunit in HEK 293 cells [64]. Coupling between CaV1.2 and Gal-1 regulates the blood pressure, and Gal-1 deficiency triggers hypertension by activating CaV1.2 in spontaneously hypertensive rats [64]. In conclusion, adjustment of the UPS with the scope of the UPS to regulate Ca2+ signaling is proposed as a therapeutic strategy for Ca2+ channel-associated diseases, including cardiac hypertrophy and ischemia–reperfusion injury.

2.2. Ca2+ Signaling and Ca2+-Related Proteins Regulate UPS Acitivity

Ca2+ signaling regulates numerous cellular functions. In this section, researchers will elucidate Ca2+ signaling to regulate the UPS. For example, treatment with a Ca2+ ionophore (A23187) activates the proteasome within 10 min in ascidian and Xenopus eggs [65][66]. Increased proteasome activation is attenuated by the Ca2+-chelating agent 1,2-bis(o-aminophenoxy) ethane-N,N,N′,N′-tetra acetic acid (BAPTA)-AM [65][66]. Furthermore, A23187-induced Ca2+ increasingly activates the UPS to degrade the signaling proteins, including cyclooxygenase-1 and islet-brain1/JNK interacting protein 1 [67][68]. In neuronal membrane proteasome-inhibited neurons, Ca2+ signaling is dominantly attenuated [69]. Similarly, [Ca2+]i increases by the constitutive activation of the epithelial sodium channel, which induces the aggregation and activation of caspase-8 to inhibit the proteasome, and activated caspase-8 induces cellular apoptosis [70].
The ER is a major source of increased [Ca2+]i that regulates the UPS. Acute ER stress increases the degradation of the amyloid precursor protein, a diagnostic marker of AD [71]. In contrast, human islet amyloid polypeptide aggregation induces ER stress and subsequently impairs the UPS [72]. Aggravated oxidative stress and ER stress produce misfolded proteins in pancreatic β cells and subsequently impair the β-cell function [73]. In summary, the mechanisms by which Ca2+-related proteins regulate the UPS can be used to elucidate the interplay between Ca2+ signaling and the UPS with the scope of Ca2+ signaling to regulate the UPS and may provide dynamic tools for potential therapeutic applications.

2.2.1. Membrane-Bound Proteins and the UPS

Membrane-bound Ca2+ channels are categorized into various subfamilies. In this section, researchers will discuss the membrane-associated Ca2+ channels, which regulate the UPS. First, the UPS is regulated by Ca2+ signaling from intracellular organelles, including the mitochondria and ER. For example, the treatment with curcumin, which may have anticancer properties [74][75], induces a mitochondrial Ca2+ increase, which inhibits the UPS and induces severe vacuolation, which is a marker of paraptosis, along with apoptotic signals, including cellular shrinkage and the generation of apoptotic bodies [76]. Plasma membrane-bound VGCCs are categorized into several subtypes, including L-, N-, P/Q-, R-, and T-type channels [77]. The T-type Ca2+ channel inhibitor NNC 55-0396 blocks angiogenesis in human umbilical vein endothelial cells through hypoxia-inducible factor-1 (HIF-1) degradation [78]. Under hypoxic conditions, NNC 55-0396 treatment induces the ubiquitination of HIF-1 and subsequent UPS degradation [78]. Thus, modulation of the T-type Ca2+ channels and the subsequent UPS may have therapeutic potential in treating cancer by inhibiting angiogenesis. Transient receptor potential (TRP) channels are nonselective Ca2+ channels with various functions and subtypes [79][80] that also regulate the UPS. In oxidative stress induced by ultraviolet irradiation, TRP vanilloid (TRPV)1 is activated and induces an increase in the Ca2+ levels in human dermal fibroblasts [81]. The activation of TRPV1 induces the ubiquitination of nuclear factor erythroid 2-related factor 2 (Nrf2), which is a key factor in oxidative stress [81]. In addition, the overexpression of TRPV1 increases the ubiquitination of the epidermal growth factor receptor (EGFR) to reduce EGFR expression [82]. Another plasma membrane channel, the Ca2+-sensing receptor (CaSR), which maintains Ca2+ homeostasis, also induces proteasome-induced degradation [83]. CaSR inhibits the TGF-beta-dependent phosphorylation of Smad2, which increases its proliferative effect in human embryonic kidney (HEK) 293 cells [83]. The mechanisms by which Ca2+ channels and transporters are activated are diverse, and their roles in regulating ubiquitination and the UPS should be studied in further detail. Although the importance of Ca2+ channels and transporters is being magnified, the study of the UPS for Ca2+ channels and transporters is still attractive.

2.2.2. Cytosolic Ca2+-Binding Proteins and the UPS

Cytosolic Ca2+-binding proteins involved with the UPS have emerged in various studies. In this section, researchers will discuss the accumulating evidence of the role of Ca2+-binding/related proteins in the modulation of the UPS. The secondary messenger Ca2+ delivers signals through Ca2+-binding proteins, such as calmodulin (CaM) [84]. CaM is stimulated by the binding of Ca2+ and activates Ca2+/calmodulin-dependent protein kinases (CaMK) to regulate a variety of physiological functions, including smooth muscle contraction [85], the activation of phosphorylase kinase [86], and activation of the α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor [87]. In addition, CaM and CaMK regulate the UPS. E3 ligase, mahogunin ring finger 1 (MGRN1), and glycoprotein 78 (GP78) bind CaM under high [Ca2+]i, and the treatment with BAPTA attenuates the ubiquitination of MGRN1 and GP78 [88]. CaM bound to MGRN1 and GP78 activates the translocation of GP78 onto the ER membrane to induce ER-associated protein degradation [88]. In hippocampal neurons, the UPS induces an action potential that is inhibited by MG-132 [89]. The treatment with the Ca2+/calmodulin-dependent protein kinase II (CaMKII) inhibitor AIPII reduces the rate of protein degradation, while overexpression of the constitutively active form of CaMKII increases the protein degradation [89]. A recent study addressed a new T-type channel enhancer, ethyl-8-methyl-2,4-dioxo-2-(piperidin-1-yl)-2H-spiro[cyclopentane-1,3-imidazo [1,2-a]pyridin]-2-ene-3-carboxylate (SAK3), which has potential therapeutic effects against AD [90]. CaMKII is a scaffold protein that phosphorylates the proteasome subunit Rpt6 [91]. The administration of SAK3 increases CaMKII-Rpt6 signaling, which enhances the proteasome activity in dendritic cells [90]. In myotubules, the Ca2+ ionophore A23187 induces the UPS, while CaMKII inhibitors KN-62 and KN-93 dominantly attenuate the proteasome activity [92].
During muscle wasting caused by cachexia, the Ca2+-binding protein calpain induces Ca2+-dependent proteolysis and the breakdown of myofibrillar proteins [93]. The calpains activate ER-bound transcription factor 11 (TCF11)/Nrf1, which activates the 26S proteasome subunit genes [94]. Calpain-1 cleaves TCF11/Nrf1 to generate the active form, and the inhibition of calpain-1 slows down the degradation of TCF11/Nrf1 [94]. Another ER-related protein RNF122 interacts with Ca2+ to modulate the cyclophilin ligand (CAML) to stabilize RNF122, thus inhibiting the ubiquitination of RNF122 [91]. The lectin chaperone calreticulin, which maintains [Ca2+]i homeostasis, regulates the proteasome activity [95]. In calreticulin-deficient cells, the number of ubiquitinated proteins and proteasome activity are increased [95]. In addition, the Ca2+-binding protein S100, which regulates the tumor cell viability [96], interacts with the E3 ubiquitin ligase C-terminus of the Hsc70-interacting protein (CHIP) to inhibit ubiquitination and the proteasome system [97]. The current understanding of Ca2+ signaling and its associated proteins in the UPS is summarized in Table 1.
Table 1. The effect of Ca2+ signaling on the UPS.
Related Signaling Effect on UPS Details Ref
Mitochondrial
Ca2+ release		 Inhibition Curcumin inhibits the UPS to induce paraptosis. [76]
T-type
Ca2+ channel		 Inhibition NNC 55-0396 inhibits T-type Ca2+ channels to attenuate cancer angiogenesis. [78]
TRPV1 Activation Activation of TRPV1 induces the ubiquitination of Nrf2. [81]
Overexpressed TRPV1 increases the ubiquitination of EGFR to induce the UPS. [82]
CaSR Activation CaSR maintains Ca2+ homeostasis through the UPS. [83]
CaM Activation CaM induces the translocation of GP78 for ER-associated UPS. [88]
CaMKII Activation Phosphorylation of Rpt6 through CaMKII enhances the UPS. [90]
Calpain Activation Calpain-induced activation of Nrf1 stimulates the 26S proteasome subunit gene. [94]
CAML Inhibition CAML stabilizes RNF122. [91]
Calreticulin Inhibition Deficiency of calreticulin increases the UPS. [95]
S100 Inhibition Inhibition of the E3 ubiquitin ligase. [97]
Abbreviations: TRPV1, transient receptor potential vanilloid 1; CaSR, Ca2+-sensing receptor; CaM, calmodulin; CaMKII, Ca2+/calmodulin-dependent protein kinase II; CAML, Ca2+-modulating cyclophilin ligand; UPS, ubiquitin proteasome system; Nrf, nuclear factor erythroid 2-related factor; GP78, glycoprotein 78; RNF122, ring finger protein 122.

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Subjects: Biochemistry & Molecular Biology
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Jeong Hee Hong
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Dongun LEE
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