Molecular Interaction of Protein-Pigment C-Phycocyanin with Bovine Serum Albumin in a Gomphosis Structure Inhibiting Amyloid Formation

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Molecular Interaction of Protein-Pigment C-Phycocyanin with Bovine Serum Albumin in a Gomphosis Structure Inhibiting Amyloid Formation International Journal of Molecular Sciences Article Molecular Interaction of Protein-Pigment C-Phycocyanin with Bovine Serum Albumin in a Gomphosis Structure Inhibiting Amyloid Formation Yi-Cong Luo and Pu Jing * Shanghai Food Safety and Engineering Technology Research Center, Bor S. Luh Food Safety Research Center, Key Lab of Urban Agriculture (South), School of Agriculture & Biology, Shanghai Jiao Tong University, Shanghai 200240, China; [email protected] * Correspondence: [email protected] Received: 29 August 2020; Accepted: 20 October 2020; Published: 2 November 2020 Abstract: Accumulation of amyloid fibrils in organisms accompanies many diseases. Natural extracts offer an alternative strategy to control the process with potentially fewer side effects. In this study, the inhibition of C-phycocyanin from Spirulina sp. on amyloid formation of bovine serum albumin (BSA) during a 21-day incubation was investigated using fluorescence and circular dichroism (CD), and mechanisms were explored via kinetic fitting and molecular docking. C-phycocyanin (0–50 µg/mL) hindered the amyloid formation process of BSA with increased half-lives (12.43–17.73 days) based on fluorescence intensity. A kinetic model was built and showed that the k1 decreased from 1.820 10 2 d 1 to 2.62 10 3 d 1 with the increase of C-phycocyanin, while k showed no changes, × − − × − − 2 indicating that the inhibition of BSA fibrillation by C-phycocyanin occurred in a spontaneous process instead of self-catalyzed one. CD results show that C-phycocyanin inhibited conformational conversion (α-helices and β-sheets) of BSA from day 6 to day 18. Molecular docking suggested that C-phycocyanin may hinder BSA fibrillation by hydrogen-bonding > 6 of 27 α-helices of BSA in a gomphosis-like structure, but the unblocked BSA α-helices might follow the self-catalytic process subsequently. Keywords: C-phycocyanin; blue food pigment; secondary interaction; fibrillation; non-covalent interaction 1. Introduction The process of aggregation and fibril formation called amyloid formation is widely found in proteins of organisms with unknown physiological functions. Accumulation of amyloid fibrils in organisms accompanies many diseases, such as Alzheimer’s, Parkinson’s, diabetes, prion diseases, etc. [1,2]. The mechanism of amyloid formation is still debated. Many different precursor proteins are involved in the fibrillation process; protein fibrillation is often accompanied by a decrease of α-helices and an increase of β-sheets [3]. Amyloid deposits have been under investigation in a number of pathological states, which then cause irreversible damage to the tissue [4], such as amyloid-β(Aβ) plaque deposits with neurofibrillary tangles containing tau proteins, which are the key pathognomonic manifestations of Alzheimer’s disease [5]. A range of small molecules (e.g., peptides and polyphenols) have been identified as impeding fibril formation. Peptides inhibitors or monomer binding-protein have been designed to block self-association and protein aggregation as a potential therapeutic target [6,7], although numerous phytochemicals such as polyphenols have been investigated to remodel mature amyloid fibrils to non-toxic aggregates [8,9]. A previous study showed that oral administration of the cyanobacteria Spriulina appeared to mediate effects. Spirulina exhibited a neuroprotective role against 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine Int. J. Mol. Sci. 2020, 21, 8207; doi:10.3390/ijms21218207 www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2020, 21, x 2 of 11 SpriulinaInt. J. Mol. Sci.appeared2020, 21, 8207to mediate effects. Spirulina exhibited a neuroprotective role against 1-methyl-4-2 of 11 phenyl-1,2,3,6-tetrahydropyridine neurotoxicity in a mice model of Parkinson’s disease. Spirulina may prevent memory dysfunction, possibly by lessening Aβ protein accumulation, reducing oxidativeneurotoxicity damage in a and mice mainly model augmenting of Parkinson’s the disease. catalase Spirulinaactivity inmay senescen preventce-accelerated memory dysfunction, mice [10]. Thepossibly pigment by lessening compound, Aβ protein namely accumulation, C-phycocyanin, reducing has been oxidative implicated damage in andprotec mainlytive benefits augmenting [11,12]. the C-phycocyanincatalase activity inaffected senescence-accelerated astrocytes-mediated mice [neuroprotection10]. The pigment against compound, oxidative namely brain C-phycocyanin, injury in astrocytehas been tissue implicated models in [11]. protective More recently, benefits C-phycocyanin [11,12]. C-phycocyanin from Spirulina affected was astrocytes-mediated found to inhibit α- synucleinneuroprotection and amyloid- againstβ oxidativefibril formation brain injury[13]. Molecular in astrocyte docking tissue studies models [14] [11]. showed More that recently, the phycocyaninC-phycocyanin interacted from Spirulina with thewas enzyme found β to-secretase, inhibit α -synucleinwhich catalyzes and amyloid- the proteolysisβ fibril of formation the amyloid [13]. precursorMolecular protein docking to studies form plaques. [14] showed that the phycocyanin interacted with the enzyme β-secretase, whichC-phycocyanin catalyzes the proteolysisis a homologous of the amyloid dimer precursor containing protein two to formidentical plaques. peptides and three chromophores,C-phycocyanin and is apractically homologous recognized dimer containing as a monomer, two identical which peptides can self-assemble and three chromophores,into trimer or hexamerand is practically in a solution recognized based on as concentration a monomer, [15]. which C-phycocyanin can self-assemble (Figure into 1a) trimer from Spirulina or hexamer sp. is in an a ediblesolution pigment based onprotein, concentration composing [15]. of C-phycocyanin α and β subunits. (Figure1 a)Three from tetrapyrroleSpirulina sp. chromophoreis an edible phycocyanobilinspigment protein, composing (Figure 1b) of areα andcovalentlyβ subunits. attached Three to tetrapyrrole the αβ monomer chromophore through phycocyanobilins three conserved cysteine(Figure1 b)residues are covalently [16]. attachedAdditionally, to the αβa monomervariety of through secondary three conservedinteractions cysteine occur residues between [16]. phycocyanobilinAdditionally, a variety and chromopeptide. of secondary interactions occur between phycocyanobilin and chromopeptide. (b) (a) (b) Figure 1. StructureStructure of C-phycocyanin ((aa)) andand phycocyanobilin phycocyanobilin (yellow) (yellow) with with its its secondary secondary interaction interaction of ofamino amino acid acid residues residues on the onα thesubunit α subunit (b). The (bα). andTheβ αsubunits and β subunits are colored are in colored pink and in blue, pink respectively. and blue, respectively. Bovine serum albumin (BSA) is a helical protein containing 583 amino acids, and is the most abundantBovine protein serum in albumin the circulatory (BSA) systemis a helical that isprotein involved containing in the transport 583 amino of drug acids, molecules. and is the BSA most can abundantspontaneously protein form in the fibers circulatory at pH = system7.4, with that the is increaseinvolved of inβ the-sheets transport [17]. of Therefore, drug molecules. BSA is oftenBSA canused spontaneously as a model of proteinform fibers fibrillation at pH = [ 187.4,–20 with]. In the this increase study, weof β aimed-sheets to [17]. investigate Therefore, the BSA inhibition is often of usedC-phycocyanin as a model fromof proteinSpirulina fibrillation sp. on the[18–20]. fibrillation In this ofstudy, BSA. we This aimed was to evaluated investigate using the fluorescenceinhibition of C-phycocyaninand circular dichroism from Spirulina analyses sp. andon the to fibrillation study the mechanismof BSA. This of was the evaluated secondary using interaction fluorescence using andmolecular circular docking. dichroism analyses and to study the mechanism of the secondary interaction using molecular docking. 2. Results 2. Results 2.1. Inhibitory Effect of C-phycocyanin on Formation of Amyloid Fibrils 2.1. InhibitoryFluorometric Effect and of C-phycocya CD assaysnin were on Formation applied to of evaluate Amyloid theFibrils process of amyloid formation [21,22]. The precipitates of insoluble protein fiber started being visually notable until day 18 and plenty were Fluorometric and CD assays were applied to evaluate the process of amyloid formation [21,22]. generated on day 21. The precipitates of insoluble protein fiber started being visually notable until day 18 and plenty were generated2.2. Fluorescence on day Intensity 21. and Kinetic Fitting Results 2.2. FluorescenceThe fluorescence Intensity intensity and Kinetic was Fitting positively Results associated with protein amyloid formation due to the characteristics of fluorescence, and showed in the linear range at low concentrations of BSA The fluorescence intensity was positively associated with protein amyloid formation due to the <~260 µM[23], where 5 µM of BSA was applied in the experiment. Figure2 shows that the fluorescence characteristics of fluorescence, and showed in the linear range at low concentrations of BSA <~260 intensity as an index of the degree of inhibitory effect on the amyloid formation of BSA was negatively µM [23], where 5 µM of BSA was applied in the experiment. Figure 2 shows that the fluorescence associated with an increasing dosage of C-phycocyanin (0.5–50 µg/mL), suggesting a potential Int. J. Mol. Sci. 2020, 21, x 3 of 11 intensity as an index of the degree of inhibitory effect on the amyloid formation of BSA was Int. J. Mol. Sci.
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