Stalling the Course of Neurodegenerative Diseases: Could Cyanobacteria Constitute a New Approach toward Therapy?
Abstract
:1. Introduction
2. Cyanobacteria
3. Neurodegeneration
4. Cyanobacteria Potential against Neurodegenerative Diseases
4.1. Cyanobacteria against Alzheimer’s Disease
Strain | Compound/Extract | Effect | In Vitro Assays | In Vivo Assays | Reference |
---|---|---|---|---|---|
Anabaena flos-aquae NRC-525-17 | Anatoxin-a(s) (3) | AChE and BChE inhibition | AChE and BChE inhibition assay | [55] | |
Nostoc 78-12A | Nostocarboline (4) | BChE inhibition | AChE and BChE inhibition assay | [57] | |
Phormidium autumnale | SFE-EtOH extract | AChE and LOX inhibition. Antioxidant. | AChE inhibition assay. LOX inhibition assay. ORAC assay. | [60] | |
Anabaena variabilis | Methylene chloride/ methanol extract (Fraction 7) | AChE inhibition | AChE inhibition assay | [61] | |
Oscillatoria sancta | Methylene chloride/ methanol (1:1) extract | AChE inhibition | AChE inhibition assay | [62] | |
Nostoc sp. | Ethanolic Extract | AChE and BChE inhibition. Antioxidant. | AChE and BChE inhibition assay. DPPH assay. | [63] | |
Spirulina sp. | Phycocyanin | Inhibition of Aβ formation | Fluorimetric assay. Kinetic analysis. Circular dichroism analysis. | [65] | |
Spirulina sp. | Phycocyanin | Inhibition of Aβ40/42 amyloid fibrillation | Fibrillar and amorphous aggregation assays. Transmission electron microscopy imaging. | [66] | |
Symploca sp. | Tasiamide B (8) | BACE-1 inhibition | BACE-1 inhibition assay | [67] | |
Lyngbya sp. | Tasiamide F (9) | BACE-1 inhibition | BACE-1 inhibition assay | [69] | |
Leptolyngbya sp. N62DM | Phycocyanin | BACE-1 inhibition | Protein-complex interface identification | Caenorhabditis elegans CL4176 transgenic AD-model: Paralysis assay | [70] |
Lyngbya sp. A09DM | Phycoerythrin | BACE-1 inhibition | Surface plasmon resonance. Isothermal titration calorimetry. Enzyme activity by kinetic parameters. | Caenorhabditis elegans CL4176 transgenic AD-model: Thioflavin-T staining assay | [71] |
Spirulina platensis | Lipopolysaccharide | Downregulation of p-tau expression. Antioxidant. Anti-inflammatory. | Wistar albino rats exposed to nicotine: Biochemical assessments (Oxidative and inflammatory markers). RT-PCR. Western Blot (p-tau). | [78] | |
Spirulina maxima | 70% ethanol extract | AChE inhibition. Reduced Aβ, APP, and BACE-1 levels. BDNF/PI3K/Akt pathway activation. Antioxidant. Improved cognition. | ICR mice injected with Aβ1–42: Passive Avoidance Test. Morris WaterMaze Test. Biochemical Analysis (Aβ1–42, GSH, BDNF, AChE). Western Blot. | [72] | |
Aphanizomenon flos-aquae | KlamExtra® | Reduced Aβ, APP and BACE-1 levels. Anti-inflammatory and anti-gliosis. Improved metabolic parameters. Protection of neuronal morphology and synapses. | High-Fat Diet C57BL/6J mice: Metabolic parameters analysis. Western Blot (IR, Akt, PSEN-1, BACE-1, PSD-95, synaptophysin, TNF-α, GFAP, IL-10, TREM-2). Histopathology and Immunohistochemistry (GFAP, TREM-2, Aβ). Thioflavin T staining. TUNEL assay. | [73] | |
Spirulina platensis | Diet supplementation | Decreased Aβ1–42, APP, BACE-1, p-tau, and p-GSK levels. Anti-inflammatory. Improved microbiota dysbiosis. Improved metabolic parameters. Improved locomotor and cognitive function. | High-Fat Diet C57BL/6J mice: Barnes Maze test. Morris Water Maze test. ELISA (Aβ1–42, TNF-α, IL-1β, IL-6, LPS). RT-PCR. Western Blot (APP, BACE-1, p-tau, p-GSK, IBA-1). Microbial diversity analysis. GC (SCFAs). | [79] | |
cf. Symploca sp. | Santacruzamate A (11) | Anti-apoptotic. Anti-UPR and ER stress. Improvement of the mitochondrial fission pathway. Modulation of KDELR and Mia40-ALR. Memory improvement. | PC12 cells: Cell viability and apoptosis assays. Electrophysiological recordings. Immunoblot analyses. Measurement of mitochondrial permeability transition pore. Opening and mitochondrial membrane potentials. | APPswe/PS1dE9 mice: Open-Field test. Morris Water Maze test. RT-PCR (Mia40, KDEL). | [80] |
Spirulina platensis | Diet supplementation (tablets) | Protection of neuronal morphology. Reduction in Aβ accumulation. Improvement of metabolic parameters. Antioxidant. Anti-inflammatory. | Wistar rats treated with AlCl3: TBARS assay. GSH content assay. Total thiol content assay. TAC assay. GPx, GST, SOD activity assay. Lipid profile determination. ELISA (TNF-α). Histology. Immunofluorescence (Aβ). | [82] | |
Spirulina platensis | S. platensis- loaded niosome | Protection of neuronal morphology. Restored levels of AChE and ACh. Gene modulation. Recognition and working memory improvement. | Wistar rats treated with AlCl3: Novel object recognition test. Y-maze test. TAC assay. MDA assay. AChE assay. Histology. HPLC (ACh, NE, 5HT, DA, DOPAC). qPCR (Bax, Bcl-2, AChE, MAO). | [83] | |
Spirulina platensis | Enzyme Digested Phycocyanin (EDPC) | Cognitive function improvement. Gene modulation. | Male Slc:ddY SPF mice injected with Aβ25–35: Y Maze test. DNA microarray. | [85] | |
Spirulina platensis | Phycocyanin | Gene and miRNA modulation. Anti-inflammatory. Anti-apoptotic. Memory improvement. | Male C57BL/6 mice injected with oligomeric Aβ1–42: Eight-arm radial maze. RT-PCR (caspase-3, caspase-9, miR-335). Western Blot (HDAC3, Bcl-2, Bax, IL-6, IL-1β). Immunohistochemistry (Bcl-2, Bax). Immunofluorescence (BDNF, HDAC3). | [86] | |
Spirulina platensis | Phycocyanin | AChE inhibition. ChAT activity increase. Gene modulation. Increased PI3K/Akt pathway. Anti-inflammatory. Memory improvement. | Female Wistar Rats injected with STZ: Morris Water Maze. Memory consolidation test. Novel object recognition test. Open field test. AChE and ChAT activity assays. ELISA (TNF-α, NF-kB p56, Bcl-2, Bax, BDNF, IGF-1). qRT-PCR (IRS-1, INS, PI3K, Akt, PTEN). | [87] | |
Spirulina maxima | 70% ethanolic extract (SM70EE) pills | Memory and vocabulary improvement. | Randomized, double-blind, and placebo- controlled clinical trial. Visual learning, visual working memory, and verbal learning tests. | [88] | |
Spirulina platensis | Dietary supplementation | Improved cognitive function. Improved metabolic status. | Randomized, double-blind, and placebo. -controlled clinical trial. Mini-mental state exam. ELISA (hs-CRP, Insulin). Biochemical analysis (NO, TAC, GSH, MDA, FPG, lipid profile). | [89] |
4.2. Cyanobacteria against Parkinson’s Disease
Strain | Compound/Extract | Effect | In Vitro Assays | In Vivo Assays | Reference |
---|---|---|---|---|---|
Spirulina sp. | Phycocyanin | Inhibition of A53Tα-synuclein amyloid fibrillation | Fibrillar and amorphous aggregation assays. Transmission electron microscopy imaging. | [66] | |
Spirulina platensis | Phycocyanin | Reduction in α-synuclein inclusions. Gene modulation. Antioxidant. Improved proteostasis. | BY4741 Yeast transformed with p42FAL-αsyn-GFP: Spot assay. Fluorescence microscopy. Western Blot (α-syn). Flow cytometry. TBARS assay. CAT activity. Total thiols assay. qRT-PCR (SOD1, SOD2, HAP4, LHS1, HRD1, GSH1, GLR1, RPN4, ATG8). | [93] | |
Spirulina platensis | Phycocyanin derived peptides (MHLWAAK, MAQAAEYYR, MDYYFEER) | Improved locomotion. Neuronal protection. Antioxidant. Anti-apoptosis. Gene modulation. | MPTP-induced parkinsonism in transgenic zebrafish: Fluorescence Microscopy. Behavioral tests. Fluorescence ROS determination. Biochemical analysis (SOD, CAT, GSH-Px, CO, AChE). Acridine orange staining. qRT-PCR. | [98] | |
Spirulina maxima | Diet supplementation | Protection of DA and HVA content. Blockage of lipid peroxidation. | MPTP-induced parkinsonism in male C-57 rats: HPLC (DA, HVA, 5-HIAA, 5-HT). TBARS Assay. | [95] | |
Spirulina maxima | Diet supplementation | Improved locomotion. Recovery of mitochondrial activity. Protection of DA, DOPAC, and HVA levels. Antioxidant. | 6-OHDA-induced parkinsonism in male Wistar rats: Turn-behavior test. Closed-field test. Cylinder test. Fluorescence ROS determination. Griess reaction. TBARS assay. MTT assay. HPLC (DA, DOPAC, HVA). | [96] | |
Spirulina fusiform | Aqueous freeze-dried extract suspended in olive oil | Improved behavior and locomotion. Protection of DA levels. Antioxidant. | 6-OHDA-induced parkinsonism in male Wistar albino rats: Amphetamine- and Apomorphine -induced rotations. Locomotor activity. Rota rod. TBARS assay. Reduced glutathione content assay. HPLC (DA). | [97] | |
Spirulina platensis | Methanolic extract | Increased lifespan and locomotion. Antioxidant. Protection of DA content. | Drosophila Melanogaster exposed to FeSO4: Total phenol Content. DPPH radical scavenging activity. Survival rate. Negative Geotaxis assay. Lipid Peroxidation Assay. DA content assay. | [100] | |
Spirulina platensis | Diet supplementation | Increased lifespan and locomotion. Antioxidant. Reduced cellular stress. | DJ-1βΔ93 Drosophila Melanogaster exposed to paraquat: Survival assay. Locomotor assay. PCR (HSP70). SOD and CAT enzymatic assays. Immunostaining (Hsp70 and JNK). | [101] | |
Spirulina platensis | Polysaccharide | Increased TH and DAT expression. Antioxidant. | MPTP-induced parkinsonism in male C57BL/6J mice: Immunohistochemistry and RT-PCR (TH, DAT). SOD and GSH-Px assays. | [103] | |
Spirulina platensis | Protein-rich fraction (SPF) | Improved behavior. Protection of DA and DOPAC levels. Increased TH and DAT expression. Reduced iNOS, COX-2, and GFAP expression. Antioxidant. | 6-OHDA-induced hemiparkinsonism in male Wistar rats: Apomorphine-induced rotational test. Open-field test. Forced swim test. HPLC (DA, DOPAC). Griess Reaction. TBARS assay. Immunohistochemistry (TH, DAT, iNOS, GFAP, COX-2) | [104] | |
Spirulina platensis | 10% (w/v) aqueous extract | Improved behavior. Protection of DA and DOPAC levels. Protection of TH and DAT expression. Decreased iNOS and COX-2. Antioxidant. | 6-OHDA-induced parkinsonism in male Wistar rats: Apomorphine-induced rotational test. HPLC (DA, DOPAC). Griess Reaction. TBARS assay. Immunohistochemistry (TH, DAT, iNOS, COX-2). | [105] | |
Spirulina | Diet supplementation | Increase in TH+ and NeuN+ neurons. Anti-inflammatory. | F344 rats treated with AAV9α-synuclein: Immunohistochemistry (TH, α-synuclein, OX-6, NeuN). Stereology. Western Blot (CX3CR1). | [106] | |
Spirulina | Diet supplementation | Recovery of striatal dopamine innervation. Increased TH+ fibers. Anti-inflammatory. | 6-OHDA-induced parkinsonism in F344 male rats: Immunohistochemistry (TH, OX-6, Iba1, GFAP). Cell counting. | [107] |
4.3. Cyanobacteria against Multiple Sclerosis
Strain | Compound/Extract | Effect | In Vitro Assays | In Vivo Assays | Reference |
---|---|---|---|---|---|
Spirulina platensis | Phycocyanin | Decreased the mean cumulative score. Neuronal Morphology Protection. Antioxidant. Anti-inflammatory. Treg induction. | PBMCs: RT-PCR (TGF-β, IL-10, CD25, Foxp3). Flow cytometry (CD4, CD25, CD69). | EAE induction in male Lewis rats: MDA assay. PP assay. TOP assay. AOPP assay. FRAP assay. Transmission electron microscopy studies. | [112] |
Spirulina platensis | Phycocyanin | Improvement in disease onset and locomotion. Neuronal Morphology Protection. Antioxidant. Anti-inflammatory. | EAE induction in male Lewis rats and female C57BL/6 mice: Rotarod test. MDA assay. PP assay. FRA assay. Transmission electron microscopy studies. ELISA (IL-17, IL-6, IFN-γ). | [113] | |
Spirulina platensis | Phycocyanin | Improvement in disease onset. Antioxidant. Anti-inflammatory. Anti-demyelination. Neuronal Protection. Gene Modulation. | EAE induction in C57BL/6 mice: Immunohistochemistry (CD3, Mac-3, APP). Morphometric Analysis. MDA assay. PP assay. SOD, CAT, and GSH assays. IL-17 quantification. RT-PCR. Microarray Analysis. | [114] | |
Spirulina platensis | Phycocyanobilin (12) | Improvement in disease onset. Anti-inflammatory. Antioxidant. Anti-apoptosis. Gene modulation. | Human SHSY5Y cells: RT-PCR. Gene expression profile analysis. | EAE induction in C57BL/6 mice: ELISA (IL-17, IL-6, IFN-γ). Transmission electron microscopy. Immunohistochemistry (caspase-3, CD11). | [115] |
Spirulina | Phycocyanobilin (12) | Improvement in disease onset. Anti-inflammatory. Anti-demyelination. Neuronal protection. Gene modulation. | TMBP-GFP cells: Proliferation assay. Fluoresce microscopy. | EAE induction in C57BL/6 mice: Immunohistochemistry (CD3, Mac-3, APP, TPPP/p25, Olig2). Morphometric analysis. ELISA (IL-17A, IL-6, and IL-10). qPCR. Flow cytometry. | [116] |
4.4. Cyanobacteria against Amyotrophic Lateral Sclerosis
Strain | Compound/Extract | Effect | In Vitro Assays | In Vivo Assays | Reference |
---|---|---|---|---|---|
Oscillatoria planktothrix sp. | LPS-like molecule VB3323 | TLR4 antagonist. Improved motor function tests. Anti-inflammatory and anti-gliosis. Neuroprotection. | Purified microglial cells: Immunocytochemistry (CD11b). Immunoblotting (CD68). Live cell imaging (GFP) Motor neurons/glia co-culture: ELISA (TNF-α, IL-1β and IL-6). Motor neurons/glia coculture and purified motor neurons: Motor Neuron Viability Assay (SMI32). | Wobbler Mice: Paw abnormality and grip strength test. Immunohistochemistry (GFAP, CD11, and TNF-α). | [121] |
Spirulina | Diet supplementation | Maintenance of extension reflex. Anti-inflammatory. Neuroprotection against motor neuron degeneration. | SOD1G93A mice: Weight and measurement. Extension Reflex test. Ribonuclease Protection Assay (IL-1α, IL-1β, IL-6, TNF-α). Immunohistochemistry (Fluoro-Jade, GFAP) | [124] |
4.5. Cyanobacteria against Huntington’s Disease
Strain | Compound/Extract | Effect | In Vitro Assays | In Vivo Assays | Reference |
---|---|---|---|---|---|
Leptolyngbya sp. N62DM | Phycocyanin | Anti-polyQ aggregation. Antioxidant. Increased lifespan. | DPPH assay. FRAP assay. SRSA assay. R-Power assay. | N2 Caenorhabditis elegans: Life span assay. Pharyngeal pumping and locomotion assays. DCFH-DA fluorescence staining. Stress resistance assay. DAF-16::GFP localization Caenorhabditis elegans AM141: PolyQ aggregation assay. Paraquat sensitivity assay. Life span assay. DAF-16::GFP localization | [30] |
Nostoc sphaeroides | Chemically derived oligosaccharides (NOS-HCA, NOS-TFA) | Improved chemosensory behavior. Improved lifespan. Antioxidant. Gene modulation. | ABTS assay. DPPH assay. | N2 Caenorhabditis elegans: Oxidative survival assay. Lifespan assay. qPCR. Caenorhabditis elegans HA759: Oxidative survival assay. Chemosensory behavior assay. Lifespan assay. qPCR (gst-4, ctl-2, hsp-6, and hsp-6). | [129] |
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Ramos, V.; Reis, M.; Ferreira, L.; Silva, A.M.; Ferraz, R.; Vieira, M.; Vasconcelos, V.; Martins, R. Stalling the Course of Neurodegenerative Diseases: Could Cyanobacteria Constitute a New Approach toward Therapy? Biomolecules 2023, 13, 1444. https://doi.org/10.3390/biom13101444
Ramos V, Reis M, Ferreira L, Silva AM, Ferraz R, Vieira M, Vasconcelos V, Martins R. Stalling the Course of Neurodegenerative Diseases: Could Cyanobacteria Constitute a New Approach toward Therapy? Biomolecules. 2023; 13(10):1444. https://doi.org/10.3390/biom13101444
Chicago/Turabian StyleRamos, Vitória, Mariana Reis, Leonor Ferreira, Ana Margarida Silva, Ricardo Ferraz, Mónica Vieira, Vitor Vasconcelos, and Rosário Martins. 2023. "Stalling the Course of Neurodegenerative Diseases: Could Cyanobacteria Constitute a New Approach toward Therapy?" Biomolecules 13, no. 10: 1444. https://doi.org/10.3390/biom13101444