Doxycycline-Loaded Calcium Phosphate Nanoparticles with a Pectin Coat Can Ameliorate Lipopolysaccharide-Induced Neuroinflammation Via Enhancing AMPK

Altoé LS, Alves RS, Miranda LL, Sarandy MM, Bastos DS, Gonçalves-Santos E, Novaes RD, Gonçalves RV (2021) Doxycycline hyclate modulates antioxidant defenses, matrix metalloproteinases, and COX-2 activity accelerating skin wound healing by secondary intention in rats. Oxidative Medicine and Cellular Longevity 2021: 1–16

Ávila G, De Leonardis D, Grilli G, Lecchi C, Ceciliani F (2021) Anti-inflammatory activity of citrus pectin on chicken monocytes’ immune response. Vet Immunol Immunopathol 237:110269

Balducci C, Santamaria G, La Vitola P, Brandi E, Grandi F, Viscomi AR, Beeg M, Gobbi M, Salmona M, Ottonello S (2018) Doxycycline counteracts neuroinflammation restoring memory in Alzheimer’s disease mouse models. Neurobiol Aging 70:128–139

Bao H, Qu Q, Zhang W, Wang X, Fang J, Xue J, Liu Z, He S (2021) NRF2 exerts anti-inflammatory effects in LPS-induced gEECs by inhibiting the activation of the NF-κB. Mediators of inflammation 2021

Bevins RA, Besheer J (2006) Object recognition in rats and mice: a one-trial non-matching-to-sample learning task to study’recognition memory’. Nat Protoc 1(3):1306–1311

Bode C, Diedrich B, Muenster S, Hentschel V, Weisheit C, Rommelsheim K, Hoeft A, Meyer R, Boehm O, Knuefermann P (2014) Antibiotics regulate the immune response in both presence and absence of lipopolysaccharide through modulation of toll-like receptors, cytokine production and phagocytosis in vitro. Int Immunopharmacol 18(1):27–34

Chang C, Wang T, Hu Q, Zhou M, Xue J, Luo Y (2017) Pectin coating improves physicochemical properties of caseinate/zein nanoparticles as oral delivery vehicles for curcumin. Food Hydrocolloids 70:143–151

Colasanti A, Guo Q, Giannetti P, Wall MB, Newbould RD, Bishop C, Onega M, Nicholas R, Ciccarelli O, Muraro PA (2016) Hippocampal neuroinflammation, functional connectivity, and depressive symptoms in multiple sclerosis. Biol Psychiatry 80(1):62–72

Dasgupta B, Chhipa RR (2016) Evolving lessons on the complex role of AMPK in normal physiology and cancer. Trends Pharmacol Sci 37(3):192–206

Deacon RM, Rawlins JNP (2006) T-maze alternation in the rodent. Nat Protoc 1(1):7–12

Dong Y, Lagarde J, Xicota L, Corne H, Chantran Y, Chaigneau T, Crestani B, Bottlaender M, Potier MC, Aucouturier P (2018) Neutrophil hyperactivation correlates with Alzheimer’s disease progression. Ann Neurol 83(2):387–405

El-Habashy S, Eltaher H, Gaballah A, Mehanna R, El-Kamel AH (2021) Biomaterial-based nanocomposite for osteogenic repurposing of doxycycline. Int J Nanomed : 1103–1126

El-Habashy SE, El-Kamel AH, Essawy MM, Abdelfattah E-ZA, Eltaher HM (2021b) 3D printed bioinspired scaffolds integrating doxycycline nanoparticles: customizable implants for in vivo osteoregeneration. Int J Pharm 607:121002

El-Habashy SE, Eltaher HM, Gaballah A, Zaki EI, Mehanna RA, El-Kamel AH (2021c) Hybrid bioactive hydroxyapatite/polycaprolactone nanoparticles for enhanced osteogenesis. Mater Sci Engineering: C 119:111599

Fan K, Lin L, Ai Q, Wan J, Dai J, Liu G, Tang L, Yang Y, Ge P, Jiang R (2018) Lipopolysaccharide-induced dephosphorylation of AMPK-activated protein kinase potentiates inflammatory injury via repression of ULK1-dependent autophagy. Front Immunol 9:1464

Fuentes-Retamal S, Sandoval-Acuña C, Peredo-Silva L, Guzmán-Rivera D, Pavani M, Torrealba N, Truksa J, Castro-Castillo V, Catalán M, Kemmerling U (2020) Complex mitochondrial dysfunction induced by TPP+-Gentisic acid and mitochondrial translation inhibition by doxycycline evokes synergistic lethality in breast cancer cells. Cells 9(2): 407

Gárate I, Garcia-Bueno B, Madrigal JLM, Caso JR, Alou L, Gomez-Lus ML, Micó JA, Leza JC (2013) Stress-induced neuroinflammation: role of the toll-like receptor-4 pathway. Biol Psychiatry 73(1):32–43

Ghorbani S, Yong VW (2021) The extracellular matrix as modifier of neuroinflammation and remyelination in multiple sclerosis. Brain 144(7):1958–1973

Guerrero-Hue M, Rayego-Mateos S, Vázquez-Carballo C, Palomino-Antolín A, García-Caballero C, Opazo-Rios L, Morgado-Pascual JL, Herencia C, Mas S, Ortiz A (2020) Protective role of Nrf2 in renal disease. Antioxidants 10(1):39

Han JH, Lee YS, Im JH, Ham YW, Lee HP, Han SB, Hong JT (2019) Astaxanthin ameliorates lipopolysaccharide-induced neuroinflammation, oxidative stress and memory dysfunction through inactivation of the signal transducer and activator of transcription 3 pathway. Mar Drugs 17(2):123

Harland M, Torres S, Liu J, Wang X (2020) Neuronal mitochondria modulation of LPS-induced neuroinflammation. J Neurosci 40(8):1756–1765

Hosseini SM, Abbasalipourkabir R, Jalilian FA, Asl SS, Farmany A, Roshanaei G, Arabestani MR (2019) Doxycycline-encapsulated solid lipid nanoparticles as promising tool against Brucella melitensis enclosed in macrophage: a pharmacodynamics study on J774A. 1 cell line. Antimicrob Resist Infect Control 8(1):1–12

Jurcau A, Simion A (2021) Neuroinflammation in cerebral ischemia and ischemia/reperfusion injuries: from pathophysiology to therapeutic strategies. Int J Mol Sci 23(1):14

Kabel AM, Omar MS, Alhadhrami A, Alharthi SS, Alrobaian MM (2018) Linagliptin potentiates the effect of l-dopa on the behavioural, biochemical and immunohistochemical changes in experimentally-induced parkinsonism: role of toll-like receptor 4, TGF-β1, NF-κB and glucagon-like peptide 1. Physiol Behav 188:108–118

Kong M, Mao J, Luo B, Qin Z (2015) Role of transcriptional factor Nrf2 in the acute lung injury of mice. Int J Clin Exp Pathol 8(9):10929

Li Y, Liu T, Li Y, Han D, Hong J, Yang N, He J, Peng R, Mi X, Kuang C (2020) Baicalin ameliorates cognitive impairment and protects microglia from LPS-induced neuroinflammation via the SIRT1/HMGB1 pathway. Oxidative Medicine and Cellular Longevity 2020

Lin C-Y, Yao C-A (2020) Potential role of Nrf2 activators with dual antiviral and anti-inflammatory properties in the management of viral pneumonia. Infect Drug Resist : 1735–1741

Lv H, Liu Q, Wen Z, Feng H, Deng X, Ci X (2017) Xanthohumol ameliorates lipopolysaccharide (LPS)-induced acute lung injury via induction of AMPK/GSK3β-Nrf2 signal axis. Redox Biol 12:311–324

Moreira APB, Texeira TFS, Ferreira AB, Peluzio MdCG, Alfenas RdCG (2012) Influence of a high-fat diet on gut microbiota, intestinal permeability and metabolic endotoxaemia. Br J Nutr 108(5):801–809

Morita S, Furube E, Mannari T, Okuda H, Tatsumi K, Wanaka A, Miyata S (2016) Heterogeneous vascular permeability and alternative diffusion barrier in sensory circumventricular organs of adult mouse brain. Cell Tissue Res 363:497–511

Ni P, Fox JT (2019) Synthesis and appraisal of a hydroxyapatite/pectin hybrid material for zinc removal from water. RSC Adv 9(37):21095–21105

Nicastro N, Malpetti M, Mak E, Williams GB, Bevan-Jones WR, Carter SF, Passamonti L, Fryer TD, Hong YT, Aigbirhio FI (2020) Gray matter changes related to microglial activation in Alzheimer’s disease. Neurobiol Aging 94:236–242

Nishikimi M, Rao NA, Yagi K (1972) The occurrence of superoxide anion in the reaction of reduced phenazine methosulfate and molecular oxygen. Biochem Biophys Res Commun 46(2):849–854

Park BS, Song DH, Kim HM, Choi B-S, Lee H, Lee J-O (2009) The structural basis of lipopolysaccharide recognition by the TLR4–MD-2 complex. Nature 458(7242):1191–1195

Parvez MSA, Ohtsuki G (2022) Acute cerebellar inflammation and related ataxia: mechanisms and pathophysiology. Brain Sci 12(3):367

Patel A, Khande H, Periasamy H, Mokale S (2020) Immunomodulatory effect of doxycycline ameliorates systemic and pulmonary inflammation in a murine polymicrobial sepsis model. Inflammation 43:1035–1043

Peng X, Luo Z, He S, Zhang L, Li Y (2021) Blood-brain barrier disruption by lipopolysaccharide and sepsis-associated encephalopathy. Front Cell Infect Microbiol : 1083

Pulido-Salgado M, Vidal-Taboada JM, Barriga GG-D, Solà C, Saura J (2018) RNA-Seq transcriptomic profiling of primary murine microglia treated with LPS or LPS + IFNγ. Sci Rep 8(1):16096

Qujeq D, Tatar M, Feizi F, Parsian H, Halalkhor S (2013) Effect of Teucrium polium leaf extracts on AMPK level in isolated rat pancreases

Rahmani M, Álvarez SEN, Hernández EB (2022) The potential use of tetracyclines in neurodegenerative diseases and the role of nano-based drug delivery systems. Eur J Pharm Sci 175:106237

Rana A, Singh S, Deshmukh R, Kumar A (2020) Pharmacological potential of tocopherol and doxycycline against traumatic brain injury-induced cognitive/motor impairment in rats. Brain Injury 34(8):1039–1050

Ren Q, Ma M, Yang J, Nonaka R, Yamaguchi A, Ishikawa i, Kobayashi, Murayama, Hwang H, Saiki (2018) Soluble epoxide hydrolase plays a key role in the pathogenesis of Parkinson’s disease. Proc Natl Acad Sci 115(25):E5815–E5823

Rosi S, Ramirez-Amaya V, Vazdarjanova A, Worley PF, Barnes CA, Wenk GL (2005) Neuroinflammation alters the hippocampal pattern of behaviorally induced Arc expression. J Neurosci 25(3):723–731

Saito M, Saito M, Das BC (2019) Involvement of AMP-activated protein kinase in neuroinflammation and neurodegeneration in the adult and developing brain. Int J Dev Neurosci 77:48–59

Santa-Cecília FV, Leite CA, Del-Bel E, Raisman-Vozari R (2019) The neuroprotective effect of doxycycline on neurodegenerative diseases. Neurotox Res 35:981–986

Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 9(7):676–682

Shehata EM, Gowayed MA, El-Ganainy SO, Sheta E, Elnaggar YS, Abdallah OY (2022) Pectin coated nanostructured lipid carriers for targeted piperine delivery to hepatocellular carcinoma. Int J Pharm 619:121712

Silva Lagos L, Luu TV, De Haan B, Faas M, De Vos P (2022) TLR2 and TLR4 activity in monocytes and macrophages after exposure to Amoxicillin, ciprofloxacin, doxycycline and erythromycin. J Antimicrob Chemother 77(11):2972–2983

Stamouli E, Politis A (2016) Pro-inflammatory cytokines in Alzheimer’s disease. Psychiatrike = Psychiatriki. 27(4):264–275

Szandruk-Bender M, Wiatrak B, Szeląg A (2022) The risk of developing Alzheimer’s disease and Parkinson’s disease in patients with inflammatory bowel disease: a meta-analysis. J Clin Med 11(13):3704

Tadie J-M, Bae H-B, Deshane JS, Bell CP, Lazarowski ER, Chaplin DD, Thannickal VJ, Abraham E, Zmijewski JW (2012) Toll-like receptor 4 engagement inhibits adenosine 5′-monophosphate-activated protein kinase activation through a high mobility group box 1 protein-dependent mechanism. Mol Med 18:659–668

Takeda H, Yamaguchi T, Yano H, Tanaka J (2021) Microglial metabolic disturbances and neuroinflammation in cerebral infarction. J Pharmacol Sci 145(1):130–139

Yadav M, Parle M, Sharma N, Dhingra S, Raina N, Jindal DK (2017) Brain targeted oral delivery of doxycycline hydrochloride encapsulated tween 80 coated chitosan nanoparticles against ketamine induced psychosis: behavioral, biochemical, neurochemical and histological alterations in mice. Drug Delivery 24(1):1429–1440

Yan Z-q (2006) Regulation of TLR4 expression is a tale about tail. Am Heart Assoc 26:2582–2584

Younus H (2018) Therapeutic potentials of superoxide dismutase. Int J Health Sci 12(3):88

Yu J, Wang W-n, Matei N, Li X, Pang J-w, Mo J, Chen S-p, Tang J-p, Yan M, Zhang JH (2020) Ezetimibe attenuates oxidative stress and neuroinflammation via the AMPK/Nrf2/TXNIP pathway after MCAO in rats. Oxidative Medicine and Cellular Longevity 2020