Marine Microorganism Molecules as Potential Anti-Inflammatory Therapeutics
Abstract
:1. Introduction
2. The Link between the Inflammation and CIDs
2.1. Inflammatory Pathways
2.2. Therapeutic Strategies to Target Inflammation
Macro-Organisms | ||||||
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Organisms | Classification (Phylum) | Species | Type of Molecules | Molecules | Target/Mode of Action | Ref(s). |
Sponge | Porifera | Fasciospongia cavernosa | Terpene lactone | Cavernolide | TNF-α, NO, and PGE2 inhibition in RAW 264.7 cells | [19] |
Sponge | Porifera | Dysidea spp. | Sesquiterpene | Dysidotronic acid | TNF-α, IL-1, NO, PGE2 inhibition in RAW 264.7 cells | [20] |
Sponge | Porifera | Plakortis spp. | α-exomethylene-γ-lactone | Plakolide A | iNOS inhibition in RAW 264.7 cells | [21] |
Sponge | Porifera | Luffariella variabilis | Sesterterpene | Manoalide | Eicosanoids synthesis inhibition in human polymorphonuclear leukocytes | [22] |
Caribbean sponge | Porifera | Cacospongia linteiformis | Sesterterpene | Cyclolinteinone | iNOS and COX-2 inhibition in LPS-stimulated J774 macrophages | [23] |
Sponge | Porifera | Dysidea sp. and Petrosaspongia nigra | Merosesquiterpene & Sesterterpene | Bolinaquinone and petrosaspongiolide M | Protection against TNBS-induced colitis in BALB/c mice | [24] |
Sponge | Porifera | Petrosia spp. | Polyacetylenes | Petrocortyne D, Petrocortyne E, Petrocortyne F, Petrocortyne G, Petrocortyne H | Inhibition of PLA2 activity in K-562 cell line | [25] |
Sponge | Porifera | Petrosia spp. | Polyacetylenic alcohol | Petrocortyne A | TNF-α inhibition in LPS-activated RAW 264.7 and PMA/LPS-treated U937 cells and NO inhibition in LPS- or IFNγ-treated RAW 264.7 cells | [26] |
Sponge | Porifera | Theonella swinhoe | Steroid | Solomonsterol A | Reduction in arthritic score in anti-type II collagen antibody-induced arthritis murine model | [27] |
Sponge | Porifera | Geodia barretti | Alpha amino acids and derivatives | Barettin | TNF-α and IL-1β inhibition in LPS-stimulated THP-1 cells | [28] |
Sponge | Porifera | Geodia barretti | Alkaloids | 6-bromoindole derivatives geobarettin B, 6-bromoindole derivatives geobarettin C, 6-bromoindole alkaloids 6-bromoconicamin, barettin | IL-12 p40 inhibition and IL-10 increasing in dendritic cells | [29] |
Sponge | Porifera | Halichondria okadai | Alkaloid | Halichlorine | VCAM-1, ICAM-1, and E-selectin inhibition in LPS-stimulated aortic endothelial cells, inhibition of macrophage adhesion to cultured cell monolayers, an anti-inflammatory effect associated with NF-κB pathway | [30] |
Sponge | Porifera | Stylissa | Alkaloid | Pyrrole alkaloid (10Z)-debromohymenialdisine | IL-1β, IL-6, TNF-α, iNOS, COX-2, NO and PGE2 inhibition in co-cultures of LPS-stimulated Caco-2 and THP-1 cells | [31] |
Sponge | Porifera | Stylissa flabellata | Alkaloids | Stylissadine A, Stylissadine B | Antagonistic effect on P2X7 receptors in THP-1 cells | [32] |
Soft coral | Cnidaria | Sinularia dissecta | Diterpene | Seco-sethukarailin | Inhibition of pro-inflammatory cytokines in bone marrow-derived dendritic cells | [33] |
Soft coral | Cnidaria | Pseudopterogorgia elisabethae | Diterpenes | Pseudopterosin E, Pseudopterosin A | Reduction of PMA-induced mouse ear edema; PGE2 and LCT4 inhibition in zymosan-stimulated murine peritoneal macrophages | [34] |
Soft coral | Cnidaria | Sinularia gibberosa | Steroid | Gibberoketosterol | Inhibition of pro-inflammatory iNOS and COX-2 proteins in LPS-stimulated RAW264.7 cells | [35] |
Okinawan soft coral | Cnidaria | Sinularia spp. | Diterpenes | Norcembranolide and sinuleptolide | TNF-α and NO inhibition in LPS-stimulated RAW 264.7 cells | [36] |
Soft coral | Cnidaria | Sinularia lochmodes | Sesquiterpene | Lochmolins A, Lochmolins B | Inhibition of COX-2 expression in LPS-activated RAW 264.7 cells | [37] |
Lochmolins C | Inhibition of COX-2 expression in LPS-activated RAW 264.7 cells | [38] | ||||
Lochmolins D | Inhibition of COX-2 expression in LPS-activated RAW 264.7 cells | [37] | ||||
Soft coral | Cnidaria | Lemnalia cervicorni | Sesquiterpene | Lemnalol | Inhibition of iNOS and COX-2 expression in LPS-activated RAW 264.7 cells; inhibition of iNOS and COX-2 expression in carrageenan-activated rat paws | [39] |
Soft coral | Cnidaria | Lemnalia flava | Sesquiterpene | Flavalin A | iNOS and COX-2 inhibition in RAW 264.7 cells | [40] |
Soft coral | Cnidaria | Lobophytum crassum | Diterpenes | Crassumol E 1R,4R,2E,7E,11E-cembra-2,7,11-trien-4-ol | Inhibition of NF-κB activation in TNF-α-activated HepG2 cells | [41] |
Diterpenes | Lobocrasol A, Lobocrasol B | Inhibition of NF-κB activation in TNF-α-activated HepG2 cells | [42] | |||
Soft coral | Cnidaria | Scleronephthya gracillimum | Steroid | Sclerosteroid J | Inhibition of iNOS and COX-2 expression in LPS-activated RAW 264.7 cells | [43] |
Octocoral | Cnidaria | Pseudopterogorgia acerosa | Diterpene | Pseudopterane | Inhibition of NO, TNF-α, IL-1β and IFNγ-induced protein production in LPS-activated peritoneal macrophages | [44] |
Coral | Cnidaria | Rumphella antipathies (classification rhumphella antipathes Linnaeus 1758) | Sesquiterpene | Clovane compound 1 | Inhibition of superoxide anions generation and elastase release | [45] |
Sesquiterpene | Clovane compound 2 | Inhibition of elastase release in fMLP/CB-activated human neutrophils | [45] | |||
Sesquiterpene | Rumphellaone C | Inhibition of superoxide anion generation and elastase release in human neutrophils | [46] | |||
Sesquiterpene | Rumphellol A | Inhibition of superoxide generation and elastase release in human neutrophils | [47] | |||
Sesquiterpene | Rumpheloll B | |||||
Coral | Cnidaria | Briareum excavatum | Diterpene | Excavatolide B | Inhibition of iNOS expression in carrageenan-activated rat paws | [48] |
Coral | Cnidaria | Briareum excavatum | Diterpene | Excavatolide B | Inhibition of 12-O-tetradecanoylphorbol-13-acetate (TPA)-induced vascular permeability; inhibition of TPA-induced matrix metalloproteinase-9 expression in mouse skin; inhibition of IL-6 expression of LPS-activated mouse bone marrow-derived dendritic cells | [49] |
Anemone | Cnidaria | Zoanthus kuroshio | Alkaloid | 5α-iodozoanthenamine | Anti-inflammatory effect on—neutrophils, reduction of superoxide anion generation, and elastase by cells | [50] |
Anemone | Cnidaria | Zoanthus pulchellus | Alkaloids | 3-hydroxinorzoanthamine Norzoanthine Roanthamine | ROS and NO inhibition in LPS-stimulated BV-2 cells | [51] |
Starfish | Echinodermata | Marthasterias glacialis | Steroid | Ergosta-7,22-dien-3-ol | Inhibition of iNOS protein level in LPS-activated RAW 264.7 cells | [52] |
Starfish | Echinodermata | Astropecten polycanthus | Steroid | Steroid compound 5 | Inhibition of IL-12 p40, IL-6, and TNF-α production in LPS-activated mice bone marrow-derived dendritic cells | [53] |
Starfish | Echinodermata | Asterias amurensis | Fatty acid | Fatty acids | Inhibition of the expression of inflammatory genes via NF-κB and MAPK pathways in LPS-stimulated RAW 264.7 cells | [54] |
Starfish | Echinodermata | Marthasterias glacialis | Fatty acid | Cis 11-eicosenoic and cis 11,14 eicosadienoic acids | Inhibition of iNOS, COX-2, IκBα, and NF-κB gene expression in LPS-stimulated RAW 264.7 cells | [52] |
Starfish | Echinodermata | Protoreaster nodosus | Steroid | Oxygenated steroid derivatives | IL-12 p40, IL-6, and TNF-α inhibition in bone marrow-derived dendritic cells | [55] |
Starfish | Echinodermata | Protoreaster lincki | Steroids | Protolinckioside A, Protolinckioside B, Protolinckioside C, Protolinckioside D | Reduction of ROS formation and NO production in LPS-stimulated RAW 264.7 cells | [56] |
Starfish | Echinodermata | Anthenea aspera | Steroid | Anthenoside O | [57] | |
Starfish | Echinodermata | Pentaceraster regulus | Steroid | Pentareguloside C, Pentareguloside D, Pentareguloside E | Reduction of ROS formation and NO production in LPS-stimulated RAW 264.7 cells | [58] |
Starfish | Echinodermata | Acanthaster planci | Pyrrole oligoglycoside | Plancipyrroside A, Plancipyrroside B | Reduction of ROS formation and NO production in LPS-stimulated RAW 264.7 cells | [59] |
Starfish | Echinodermata | Asterina batheri | Pyrrole oligoglycoside | Astebatherioside B, Astebatherioside C, Astebatherioside D | IL-12 p40 inhibition in LPS-stimulated bone marrow-derived dendritic cells | [60] |
Sea cucumber | Echinodermata | Holothuria grisea | Protein | Lectin | Inhibition of neutrophil migration to the peritoneal cavity in carrageenan-activated rats; reduction of myeloperoxidase activity in carrageenan-activated rats | [61] |
Sea cucumber | Echinodermata | Apostichopus japonicus and Stichopus chloronotus | Sulfated polysaccharide | Fucosylated chondroitin sulfate | Reduction of neutrophil migration, inhibition of paw edema in carrageenan-induced paw edema in rats | [62] |
Sea cucumber | Echinodermata | Isostichopus badionotus | Sulfated polysaccharide | Fucosylated chondroitin sulfate | Suppression of TPA-mediated up-regulation of TNF-α, IL-6, NF-κB, iNOS, IL-10, IL-11, COX-2 and STAT3 genes in mouse ear tissue | [63] |
Sea cucumber | Echinodermata | Isostichopus badionotus | Sulfated polysaccharide | Fucoidan | Regulation of serum inflammatory cytokines (TNF-α, CRP, MIP-1, IL-1β, IL-6, and IL-10) and their mRNA expression, inactivation of JNK and IκB/NF-κB pathways | [64] |
Sea cucumber | Echinodermata | Holothuria albiventer and Cucumaria frondosa | Sulfated polysaccharide | Sulfated fucan/FCS | Suppression of TNF-α and IL-6 production | [65] |
Sea cucumber | Echinodermata | Holothuria tomasi | Triterpenes glycoside | Inhibition of IL-6, TNF-α levels in STZ-induced diabetic rats | [66] | |
Sea cucumber | Echinodermata | Pearsonothuria graeffei | Triterpenes glycoside | Holothurin A and Echinoside A | Inhibition of IL-1β, TNF-α, IL-6 and infiltration of macrophages in obese mice via p-ERK/cPLA2/COX-1 pathway and reduction of the PGE2 levels | [67] |
Sea cucumber | Echinodermata | Aspostichopus japonicus and Acaudina leucoprocta | Peptide | Oligopeptides | Downregulation of pro-inflammatory cytokines transcription, upregulation of anti-inflammatory cytokines, and inhibition of TLR4/MyD88/NF-κB signaling pathway | [68] |
Sea cucumber | Echinodermata | Cucumaria frondosa | Fatty acid | Eicosapentaenoic acid | Inhibition of TNF-α, IL-6, and MCP1 expression, attenuation of macrophage infiltration in the liver in mice, attenuation of the phosphorylation of NF-κB in RAW 264.7 cells | [69] |
Sea cucumber | Echinodermata | Cucumaria frondosa | Lipid | Frondanol | Reduction of inflammation-associated changes in the colon in mice, reduction of cytokine content at the protein and mRNA level | [70] |
Sea cucumber | Echinodermata | Cucumaria frondosa | Lipid | Sphingolipids | Inhibition of pro-inflammatory cytokines IL-1β, IL-6 TNF-α and increasing anti-inflammatory IL-10 via inhibition of phosphorylation of JNK and translocation of NF-κB | [71] |
Sea cucumber | Echinodermata | Cucumaria frondosa | Lipid | Frondaol A5 | Attenuation of circulating inflammatory cytokines and suppression of mRNA expression of inflammatory markers such as 5-LOX and FLAP | [72] |
Sea urchins | Echinodermata | Scaphechinus mirabilis | Dark red pigment | EchA | Attenuation of macrophage activation and infiltration (neutrophils), inhibition of TNF-α and IFNγ in bleomycin-induced scleroderma mouse model | [73] |
Sea urchins | Echinodermata | ? | Dark red pigment | EchA | Decreasing DIA, improvement of colon length and suppression of tissue damage, suppression of macrophage activation | [74] |
Sea urchins | Echinodermata | ? | Dark red pigment | EchA | TNF-α and NF-κB inhibition in Lewis rats | [75] |
Sea urchins | Echinodermata | Paracentrotus lividus | Dark red pigment | EchA | Potent stabilizing effect on the human red blood cells, suppression of the production of IL-6 and TNF-α in septic rats | [76] |
Sea urchins | Echinodermata | Scaphechinus mirabilis | Pigment | Spinochrome A | Reduction of chronic inflammation in cotton-pellet granuloma rat model | [77] |
Sea urchins | Echinodermata | Scaphechinus mirabilis | Pigment | Spinochrome B | [77] | |
Sea urchins | Echinodermata | Echinometra mathaei, diadema savignyi, tripneustes gratilla and Toxopneustes pileolus | Pigment | Spinochromes | TNF-α inhibition in J774 macrophages | [78] |
Sea urchins | Echinodermata | Echinometra mathaei, diadema savignyi, tripneustes gratilla and Toxopneustes pileolus | Pigment | EchA | ||
Sea urchins | Echinodermata | Strongylocentrotus droebachiensis | Peptide | Centrocin 1 (CEN1HC-Br) | IL-12 p40, IL-6, IL-1β and TNF-α inhibition in THP-1 cells | [79,80] |
Sea urchins | Echinodermata | Salmacis bicolor | Isochroman derived polyketide | Salmachroman | COX-2 and 5-LOX inhibition by using the 2, 7-dichlorofluorescein method | [81] |
Sea urchins | Echinodermata | Salmacis bicolor | Polyoxygenated furanocembranoid derivatives | Salmacembrane A Salmacembrane B | COX-1, COX-2, and 5-LOX inhibition by the 2, 7-dichlorofluorescein method | [82] |
Sea urchins | Echinodermata | Stomopneustes variolaris | Cembrane type of diterpene | 4-hydroxy-1-(16methoxyprop-16-en-15-yl)-8-methyl-21,22-dioxatricyclo[11.3.1.15,8]octadecane-3,19-dione | Inhibition of 5-LOX, COX-1 and COX-2 inhibition by the 2, 7-dichlorofluorescein method | [83] |
Sea urchins | Echinodermata | Stomopneustes variolaris | Macrocyclic lactone | Stomopneulactones D | COX-2, 5-LOX, iNOS inhibition in RAW 264.7 cells | [84] |
Sea urchins | Echinodermata | Brisaster latifrons | Sulfonic acid | (Z)-4-methylundeca-1,9-diene-6-sulfonic acid | Inhibition of proinflammatory cytokines by the inactivation of JNK/p38 MAPK and NF-kB pathways | [85] |
Sea urchins | Echinodermata | Hemicentrotus pulcherrimus and Diadema setosum | Lipid | Hp-s1 ganglioside | Inhibition of iNOS, COX-2, and cytokines, downregulation of the NF-κB and JNK/P38 MAPK signaling pathway | [86] |
Ascidian | Chordata | Aplidium orthium | Alkaloids | Alkaloid tubastrine, Orthidine A, Orthidine B, Orthidine C, Orthidine E, Orthidine F | Reduction of the superoxide synthesis in PMA-stimulated neutrophils in vitro and in in vivo models | [87] |
Ascidian | Chordata | Aplidium spp. | Alkaloids | Ascidiathiazone A, Ascidiathiazone B | Reduction of the superoxide production by PMA-stimulated neutrophils in vitro and in vivo in murine gout model | [88] |
Ascidian | Chordata | Pycnoclavella kottae | Alkaloid | Kottamide D | Reduction of superoxide synthesis by PMA and N-formylmethionyl-leucyl-phenylalanine (fMLP)-activated neutrophils in vitro | [89] |
Red algae | Rhodophyta | Gracilaria opuntia | Alkaloid | Azocinyl morpholinone | Inhibition of the carrageenan-induced paw edema | [90] |
Green algae | Chlorophyta | Enteromorpha prolifera | Chlorophyll | Pheophytin | Suppression of the production of superoxide anion in mouse macrophages | [91] |
Green algae | Chlorophyta | Ulva lactuca | Sterol | 3-0-B-D-glucopyranosil-stigmata-5,25,-dien sterol | Topical anti-inflammatory activity in mouse edema | [92] |
Green algae | Chlorophyta | Caulerpa racemosa | Alkaloid | Caulerpin//Sulfated polysaccharides | Inhibition of capsaicin-induced ear edema model and significant reduction of the number of recruited cells; reduction in neutrophil counts in the peritoneal cavity and paws of carrageenan-treated rats; reduction of edema volume in carrageenan and dextran-activated mouse paws | [93,94] |
Green algae | Chlorophyta | Enteromorpha prolifera | Chlorophyll | Pheophytin A | Significant suppression of TPA-induced inflammatory reactions such as edema formation in BALB/c mouse ears | [91] |
Green algae | Chlorophyta | Caulerpa mexicana | Sulfated polysaccharides | Sulfated polysaccharides | Reduction of edema volume and neutrophilic infiltration in carrageenan-activated raw paws; Reduction of edema volume in dextran and histamine-activated rat paws | [95] |
Green algae | Chlorophyta | Caulerpa cupressoids | Protein | Lectin | Reduction of leukocyte counts and myeloperoxidase activity in rat temporomandibular joint synovial lavage fluid in zymosan-activated rats | [96] |
Brown algae | Heterokontophyta | Ecklonia cava | Pholorotannin | Dieckol | Inhibition of NO, PGE2, and the expression of iNOS production in murine BV2 microglia | [97] |
Brown algae | Heterokontophyta | Undaria pinnatifida | Fatty acid | Ω-3 polyunsaturated fatty acids | Inhibition of the mouse ear inflammation induced by PMA | [98] |
Brown algae | Heterokontophyta | Laminaria japonica | Sulfated polysaccharide | Fucoidan | NO and IL-6 inhibition in Caco-2 cells | [99] |
Brown algae | Heterokontophyta | Fucus vesiculosus | Sulfated polysaccharide | Fucoidan | Reduction of NO, PGE2, TNF-α and IL-1β production in RAW 264.7 cells | [100] |
Microorganisms | ||||||
Organisms | Classification (Phylum) | Species | Type of Molecules | Molecules | Target/Mode of Action | Ref(s). |
Dinoflagellate (microalgae) | Dinoflagellata | Symbiodinium spp. | Amphoteric iminium | 6,6,6-tricyclic iminium ring and aryl sulfate moiety | Inhibition of the COX-2 activity in RAW 264.7 cells | [101] |
Haptophyte (microalgae) | Haptophyta | Isochrysis galbana | Galactolipids | Monogalactosyldiacylglycerols Digalactosyldiacylglycerol | Inhibition of the synthesis of TNF-α, IL-1β, IL-6, IL-17 in THP-1 cells | [102] |
Green microalgae | Chlorophyta | Chlorella vulgaris | Polyunsaturated fatty acid | Linoleic acid and α-linolenic | Inhibition of TNF-α, IL-6, PGE2, and NO production in RAW 264.7 cells | [103] |
Red microalgae | Rhodophyta | Porphyridium cruentum | Fatty acids | Fatty acids | Inhibition of superoxide anion production by peritoneal leukocytes primed with PMA | [104] |
Red microalgae | Rhodophyta | Porphyridium cruentum | Exopolysaccharide (EPS) | EPS | Inhibition of 77% of COX-2 in human keratinocytes and murine fibroblasts Balb/c-3T3 | [105] |
Pigment | Phycoerythrin | Inhibition of COX-2 in human keratinocytes and murine fibroblasts Balb/c-3T3 | [105] | |||
Cyanobacteria | Cyanobacteria | Spirulina subsalsa | Lipids (glycophospholipids, phospholipids) | Sulfoquinovosyl diacylglycerols, monogalactosylodiglycerides, cerebrosides; ceramides, phosphatidylcholines, phosphatidylethanolamines | Inhibitory effects on platelet-activating factor and thrombin-induced platelet aggregation | [106] |
Cyanobacteria | Cyanobacteria | Lyngbya majuscula | Malyngamide | Malyngamide F acetate | Inhibition of the NO production in RAW 264.7 cells | [107] |
Cyanobacteria | Cyanobacteria | Caldora sp. | Azirine | Dysidazirine carboxylic acid | Inhibition of the NO production by almost 50% at 50 µM in RAW 264.7 cells | [108] |
Fungi | Ascomycota | Chaetomium globosum QEN-14 | Alkaloid | Chaetoglobosin Fex | Inhibition of TNF-α and IL-6 production in LPS-activated RAW 264.7 cells | [109] |
Fungi | Ascomycota | Stachybotrys sp. HH1 ZSDS1F1-2 (isolated from a sponge from Xisha Island, China, in April 2012) | Xanthonne | Xanthone derivatives 3 (others), | Inhibition of COX-2 | [110] |
Xanthone derivatives 4 (others), | ||||||
Xanthone derivatives 11 (others) | ||||||
Fungi | Ascomycota | Aspergillus spp. | Diketopiperazine alkaloids | 5-prenyl-dihydrovariecolorin F | Inhibition of iNOS and COX-2 activity, reduction of NO and PGE2 levels in LPS-stimulated RAW 264.7 and BV2 cells | [111] |
Fungi | Ascomycota | Aspergillus spp. | Diketopiperazine alkaloids | 5-prenyl-dihydrorubrumazine A | ||
Fungi | Ascomycota | Aspergillus sp. SF-6354 | Polyketide | TMC-256C1 | NO and PGE2 inhibition in LPS-activated BV2 cells | [112] |
Fungi | Ascomycota | Aspergillus sp. SCSIO Ind09F01 | Polyketides | Diorcinol, Cordyol C, 3,7-dihydroxy-1,9-dimethyldibenzofuran | Inhibition of COX-2 (IC50 = 2.4–10.6 µM) | [113] |
Fungi | Ascomycota | Aspergillus sp. SF-5974 and Aspergillus sp. SF-5976 | Polyketides | Cladosporin 8-0-α-ribofuranoside, Cladosporin, Asperentin 6-O-methyl ether Cladosporin 8-O-methyl ether, 4′-hydroxyasperentin, 5′-hydroxyasperentin | Inhibition of NO and PGE2 expression, (IC50 = 20–65 µM) in LPS-activated microglial cells | [114] |
Fungi | Ascomycota | Aspergillus sp. SF-5044 | Polyketide | Asperlin | Inhibition of NO and PGE2 expression in LPS-activated murine macrophages | [115] |
Fungi | Ascomycota | Aspergillus sp. | Peptide | Aurantiamide acetate | Inhibition of NO and PGE2 expression in LPS-activated BV2 cells | [116] |
Fungi | Ascomycota | A.europaeus WZXY-SX-4-1 | Polyketides | Eurobenzophenone B, Euroxanthone A, 3-de-O-methylsulochrin, Yicathin B, Dermolutein, Methylemodin | Inhibition of NF-κB activation and NO expression in LPS-activated SW480 cells | [117] |
Fungi | Ascomycota | Aspergillus sp. ZLO-1b14 | Terpenes | Aspertetranone A, Aspertetranone B, Aspertetranone C, Aspertetranone D | Inhibition of IL-6 expression in LPS-activated RAW 264.7 cells | [118] |
Fungi | Ascomycota | A.sydowii J05B-7F-4 | Polyketide | Violaceol II, Cordyol E | Inhibition of NO (IC50 = 73 µM) expression in LPS-activated RAW 264.7 cells | [119] |
Fungi | Ascomycota | A.niger SCSIO Jcsw6F30 | Polyketides | Aurasperone F, Aurasperone C, Asperpyrone A | Inhibition of COX-2 expression (IC50 = 11.1, 4.2, and 6.4 µM for F, C, and A, respectively) in LPS-activated RAW 264.7 cells | [120] |
Fungi | Ascomycota | A. flocculosus 16D-1 | Alkaloids | Preussin C, Preussin D, Preussin E, Preussin F, Preussin G, Preussin H, Preussin I, Preussin J, Preussin K | Inhibition of IL-6 expression in LPS-activated THP-1 cells | [121] |
Fungi | Ascomycota | A.versicolor | Alkaloids | Asperversiamide B, Asperversiamide C, Asperversiamide F, Asperversiamide G | Inhibition of iNOS expression in LPS-activated RAW 264.7 cells | [122] |
Fungi | Ascomycota | A.terreus | Alkaloid | Luteoride E | Inhibition of NO in LPS-activated RAW 264.7 cells | [123] |
Fungi | Ascomycota | A.terreus | Terpene | Lovastatin | Inhibition of NO production in LPS-activated RAW 264.7 cells | [123] |
Fungi | Ascomycota | A.terreus CFCC 81836 | Terpene | Brasilanone A | Inhibition NO production in LPS-activated RAW 264.7 cells | [124] |
Fungi | Ascomycota | A.terreus CFCC 81836 | Terpene | Brasilanone E | [124] | |
Fungi | Ascomycota (phylum) | A.terreus | Polyketide | Versicolactone G | Inhibition of NO production (IC50 = 15.72 and 29.34 µM for G and A, respectively) in LPS-activated RAW 264.7 cells | [123] |
Fungi | Ascomycota | A.terreus | Polyketide | Territrem A | ||
Fungi | Ascomycota | A.terreus | Peptide | Methyl 3,4,5-trimethoxy-2-(2-(nicotinamido)benzamido)benzoate | Inhibition of NO production in LPS-activated RAW 264.7 cells | [123] |
Fungi | Ascomycota | A. terreus (isolated from the coral Sarcophyton subviride) | Aliphatic alcohol | (3E,7E)-4,8-dimethyl-undecane-3,7-diene-1,11-diol, 14α-hydroxyergosta-4,7,22-triene-3,6-dione | Inhibition of NO expression in LPS-activated RAW 264.7 cells | [123] |
Fungi | Ascomycota | Aspergillus sp. SCSIOW2 | Terpenes | Dihydrobipolaroxins B-D Dihydrobipolaroxin | NO inhibition in RAW 264.7 cells | [125] |
Fungi | Ascomycota | Eurotium sp., SF-5989 | Alkaloid | Neoechinulin B | Inhibition of NO production in amyloid-β 1-42-activated BV-2 cells | [126] |
Fungi | Ascomycota | Eurotium sp. SF-5989 | Polyketide | Flavoglaucin Isotecrahydroauroglaucin | Inhibition of NO and PGE2 expression in LPS-activated RAW 264.7 cells | [127] |
Fungi | Ascomycota | Eurotium spp. | Indolic alkaloid | Neoechinulin A | Reduction of NO and PGE2 production by inhibiting iNOS and COX-2 expression and reduced the production of IL-1β, TNF-α in LPS-stimulated RAW 264.7 cells | [126] |
Fungi | Ascomycota | Eurotium sp. SF-5989 | Alkaloid | Neocechinulin A | Inhibition of NO and PGE2 in LPS-stimulated RAW 264.7 macrophages | [126] |
Fungi | Ascomycota | E.amstelodami | Polyketide | Asperflavin | Inhibition of 4.6% and 55.9% of NO and PGE2 expression, respectively, in LPS-activated RAW 264.7 cells | [128] |
Fungi | Ascomycota | E.amstelodami | Polyketide | Questinol | Inhibition of 73% and 43.5% of NO and PGE2 expression, respectively, in LPS-stimulated RAW 264.7 cells | [129] |
Fungi | Ascomycota | Penicillium sp. SF-5859 (isolated from a sponge) | Polyketides | Curvularin, (11R,15S)-11-hydroxycurvularin, (11S,15S)-11-hydroxycurvularin, (11R,15S)-11-methoxycurvularin, (11S,15S)-11-methoxycurvularin, (10E,15S)-10,11-dehydrocurvularin, (10Z,15S)-10,11-dehydrocurvularin | Inhibition of NO and PGE2 expression (IC50 values ranging from 1.9 to 18.7 µM) in LPS-stimulated RAW 264.7 cells | [130] |
Fungi | Ascomycota | Graphostroma sp. MCCC 3A00421 | Terpene | Graphostromane F | Inhibition of NO in LPS-activated RAW 264.7 cells | [131] |
Fungi | Ascomycota | Graphostroma sp. MCCC 3A00421 | Terpene | Khusinol B | Inhibition of NO expression in LPS-activated RAW 264.7 cells | [132] |
Fungi | Ascomycota | P.chrysogenum SCSIO41001 | Alkaloid | Chrysamide C | Inhibition of IL-17 expression in mice T-cells | [133] |
Fungi | Ascomycota | Penicillium sp. SF-5295 | Alkaloid | Viridicaol | Inhibition of NO and PGE2 expression in LPS-activated RAW 264.7 and in LPS-activated BV2 cells | [134] |
Fungi Fungi | Ascomycota | Penicillium sp. | Alkaloids | Brevicompanine E, Brevicompanine H | Inhibition of NO production in LPS-activated RAW 264.7 cells | [135] |
Fungi | Ascomycota | Penicillium sp. SF-5995 | Alkaloid | Methylpenicinoline | Inhibition of NO, PGE2, iNOS and COX-2 expression in LPS-induced RAW 264.7 cells and BV2 microglia | [136] |
Fungi | Ascomycota | Penicillium sp. SF-5497 | Terpenes | 7-acetoxydehydroaustinol, Austinolide, 7-acetoxydehydroaustin, 11-hydroxyisoaustinone, 11-acetoxyisoaustinone | Inhibition of NO expression in LPS-activated BV-2 cells | [137] |
Fungi | Ascomycota | Penicillium sp. SF 6013 | Terpenes | 2E,4Z-tanzawaic acid D, Tanzawaicacids A, Tanzawaicacids E | Inhibition of NO expression in LPS-activated RAW 264.7 cells | [138] |
Fungi | Ascomycota | Penicillium sp. SF-5629 | Polyketide | Citrinin H1 | Inhibition of NO and prostaglandin E2 expression (IC50 = 8.1 and 8.0 µM) in LPS-activated BV2 cells | [139] |
Fungi | Ascomycota | Penicillium sp. SF-5292 | Polyketide | Penicillospirone | Inhibition of NO and PGE2 expression (with IC50 values of 21.9–27.6 µM) in LPS-activated RAW 264.7 and BV2 cells | [134] |
Fungi | Ascomycota | Penicillium sp. SF-5292 | Polyketide | Penicillinolide A | Inhibition of NO, PGE2, TNF-α, IL-1β, and IL-6 expression (IC50 = 20.47, 17.54, 8.63, 11.32, and 20.92 µM, respectively) in LPS-activated RAW 264.7 and BV2 cells | [140] |
Fungi | Ascomycota | Penicillium sp. J05B-3-F-1 | Hexylitaconic acid derivatives | Methyl 8 -hydroxy-3-methoxycarbonyl-2-methylenenonanoate, (3S)-Methyl 9-hydroxy-3-methoxycarbonyl-2-methylenenonanoate | Inhibition of pro-inflammatory cytokines and NO expression in LPS-activated RAW 264.7 cells | [141] |
Fungi | Ascomycota | P. atrovenetum | Terpene | Citreohybridonol | Anti-neuroinflammatory activity | [142] |
Fungi | Ascomycota | P.steckii 108YD142 | Terpenes | Tanzawaic acid Q, Tanzawaic acid A, Tanzawaic acid C, Tanzawaic acid D, Tanzawaic acid K | Inhibition of NO expression in LPS-activated RAW 264.7 cells | [143] |
Fungi | Ascomycota | P.paxililli | Polyketide | Pyrenocine A | Inhibition of TNF-α and PGE2 expression in LPS-activated RAW 264.7 cells | [144] |
Fungi | Ascomycota | P.thomii KMM 4667 | Terpene | Thomimarine E | Inhibition of 22.5% of NO production in LPS-activated RAW 264.7 cells | [145] |
Fungi | Ascomycota | P.thomii KMM 4667 | Polyketide | Guaiadiol A, 4,10,11 trihydroxyguaiane | Inhibition of 24.1% and 36.6% of NO production at 10 µM in LPS-activated RAW 264.7 cells | [145] |
Fungi | Ascomycota | P.citrinum SYP-F-2720 | Peptide | (S)-2-(2-hydroxypropanamido)benzoic acid | Reduction of the inflammation in xylene-induced mouse ear edema model | [146] |
Fungi | Ascomycota | Hypocreales sp. HLS-104 | Terpene | 1R,6R,7R,10S-10-hydroxy-4(5)-cadinen-3-one | Inhibition of NO expression in LPS-activated RAW 264.7 cells with Emax value of 26.46% at 1 µM | [147] |
Fungi | Ascomycota | Hypocreales sp. HLS-104 | Polyketide | (R)-5,6-dihydro-6-pentyl-2H-pyran-2-one | ||
Fungi | Ascomycota | F.heterosporum CNC-477 | Sesterpene polyol | Mangicol A | Inhibition of PMA-induced mouse ear edema assay | [148] |
Fungi | Ascomycota | F.heterosporum CNC-477 | Sesterpene polyol | Mangicol B | ||
Fungi | Basidiomycota | Chondrostereum sp. NTOU4196 | Sesquiterpenes | Chondroterpene A, Chondroterpene B, Chondroterpene H, Hirsutanol A, Chondrosterin A, Chondrosterin B | Inhibition of NO expression in LPS-activated BV-2 cells | [149] |
Fungi | Ascomycota | Pleosporales sp. | Terpenes | Pleosporallin A, Pleosporallin B, Pleosporallin C | Inhibition of IL-6 expression in LPS-activated RAW 264.7 cells | [150] |
Fungi | Ascomycota | Phoma sp. NTOU4195 | Polyketide | Phomaketides A-C, FR-111142 | Inhibition of NO expression (IC50 values ranging from 8.8 to 19.3 µM) in LPS-activated RAW 264.7 cells | [151] |
Fungi | Ascomycota | Stachybotrys chartarum 952 | Terpenes | Stachybotrysin C, Stachybonoid F, Stachybotylactone | Inhibition of NO expression in LPS-activated RAW 264.7 cells | [152] |
Fungi | Ascomycota | Leptosphaerulina chartarum 3608 | Polyketide | (4R,10S,4′S)-leptothalenone B | Inhibition of NO in LPS-activated RAW 264.7 cells (IC50 = 44.5 µM) | [153] |
Fungi | Ascomycota | Glimastix sp. ZSDS1-F11 | Polyketides | Expansol A, Expansol B, Expansol C, Expansol D, Expansol E, Expansol F | Inhibition of COX-1 (IC50 = 5.3, 16.2, 30.2, 41 and 56.8 µM, for A, B, C, E, F respectively) and COX-2 (IC50 = 3.1, 5.6, 3, 5.1, 3.2 and 3.7 µM, for A, B, C, D, E, F, respectively) | [154] |
Fungi | Ascomycota | Diaporthe sp. HLY-1 | Polyketide | Mycoepoxydiene | Inhibition of NO and TNF-α, IL-6, and IL-1β expression in LPS-activated macrophages | [155] |
Fungi | Ascomycota | Aspergillus violaceofuscus | Peptides | Violaceotide A, diketopiperazine dimer | Inhibition of IL-10 expression in LPS-activated THP1 cells | [156] |
Fungi | Ascomycota | Acremonium sp. | Peptide | Oxepinamide A | Inhibition of RTX-activated mouse ear edema assay | [157] |
Fungi | Ascomycota | Alternaria sp. | Peptide | Alternaramide | Inhibition NO and PGE2 expression in LPS-activated RAW 264.7 and BV2 cells | [158] |
Fungi | Ascomycota | Trichoderma citrinoviride (isolated from green alga Cladophora) | Sorbicillinoid | Trichodermanone C | Inhibitory effect on nitrite levels in LPS-activated J774A.1 macrophages | [159] |
Fungi | Ascomycota | Paraconiothyrium sp. VK-13 | Polyketide | 1-(2,5-dihydroxyphenyl)-3-hydroxybutan-1-one, 1-(2,5-dihydroxyphenyl)-2-buten-1-one | Inhibition of NO and PGE2 expression in LPS-activated RAW 264.7 cells (IC50 = 3.9–12.5 µM). | [160] |
Fungi | Basidiomycota | Cystobasidium larynges IV17-028 | Phenazine derivatives | 6-[1-(2-aminobenzoyloxy)ethyl]-1-phenazinecarboxylic acid, Saphenol, (R)-saphenic acid, Phenazine-1-carboxylic acid, 6-(1-hydroxyethyl)phenazine-1-carboxylic acid, 6-acetyl-phenazine-1-carboxylic acid | Inhibition of NO production in RAW 264.7 cells | [161] |
Fungi | Ascomycota | Penicillium sp JF-55 (polyketide) | Phenylpropanoid | Penstyrylpyrone | Inhibition of NO, PGE2, TNF-α, IL-1β in LPS-activated murine peritoneal macrophages | [162] |
Bacteria | Actinobacteria | Streptomyces spp. | Alkaloid | Actinoquinoline A | Inhibition of COX-1 and COX-2 | [163] |
Actinoquinoline B | ||||||
Bacteria | Actinobacteria | Streptomyces caniferus | Macrolide | Caniferolide A | Inhibition of NF-κB p65 translocation and pro-inflammatory cytokines expression in BV2 microglial cells | [164] |
Bacteria | Actinobacteria | Nocardiopsis sp. | Macrolide | Fijiolide A | Reduction of TNF-α-induced NF-κB in human embryonic kidney cells 293 (IC50 = 0.57 µM) | [165] |
Bacteria | Actinobacteria | Kocuria sp. strain AG5 | Exopolysaccharide | EPS5 | Inhibition of LOX-5 and COX-2 (IC50 = 15.39 ± 0.82 µg/mL and 28.06 ± 1.1 µg/mL, respectively) | [166] |
Bacteria | Bacillota | Bacillus subtilis B5 | Macrolactin derivative | 7,13-epoxyl-macrolactin A; 7-O-2′E-butenoyl macrolactin A | Inhibition of inducible nitric oxide synthase (iNOS), interleukin-1β (IL-1β), and interleukin-6 (IL-6) expression in LPS-stimulated RAW 264.7 macrophages | [167] |
3. Marine Microorganisms vs. Macro-Organisms: Who Are the Actual Producers of Metabolites?
4. Challenges and Future Directions
5. Conclusions
Author Contributions
Funding
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Lasalo, M.; Jauffrais, T.; Georgel, P.; Matsui, M. Marine Microorganism Molecules as Potential Anti-Inflammatory Therapeutics. Mar. Drugs 2024, 22, 405. https://doi.org/10.3390/md22090405
Lasalo M, Jauffrais T, Georgel P, Matsui M. Marine Microorganism Molecules as Potential Anti-Inflammatory Therapeutics. Marine Drugs. 2024; 22(9):405. https://doi.org/10.3390/md22090405
Chicago/Turabian StyleLasalo, Malia, Thierry Jauffrais, Philippe Georgel, and Mariko Matsui. 2024. "Marine Microorganism Molecules as Potential Anti-Inflammatory Therapeutics" Marine Drugs 22, no. 9: 405. https://doi.org/10.3390/md22090405