Micro/nanoscaled cellulose from coffee pods do not impact HT-29 cells while improving viability and endosomal compartment after C. jejuni CDT intoxication

Daniele Lopez, Giovanna Panza, Pietro Gobbi, Michele Guescini, Laura Valentini, Stefano Papa, Vieri Fusi, Eleonora Macedi, Daniele Paderni, Mariele Montanari, Barbara Canonico

Article ID: 6414
Vol 7, Issue 2, 2024

VIEWS - 880 (Abstract)

Abstract


The food industry progressively requires innovative and environmentally safe packaging materials with increased physical, mechanical, and barrier properties. Due to its unique properties, cellulose has several potential applications in the food industry as a packaging material, stabilizing agent, and functional food ingredient. A coffee pod is a filter of cellulosic, non-rigid, ready-made material containing ground portions and pressed coffee prepared in dedicated machines. In our study, we obtained, with homogenization and sonication, cellulose micro/nanoparticles from three different coffee pods. It is known that nanoparticulate systems can enter live cells and, if ingested, could exert alterations in gastrointestinal tract cells. Our work aims to investigate the response of HT-29 cells to cellulose nanoparticles from coffee pods. In particular, the subcellular effects between coffee-embedded nanocellulose (CENC) and cellulose nanoparticles (NC) were compared. Finally, we analysed the pathologic condition (Cytolethal Distending Toxin (CDT) from Campylobacter jejuni) on the same cells conditioned by NC and CENC. We evidenced that, for the cellular functional features analysed, NC and CENC pre-treatments do not worsen cell response to the C. jejuni CDT, also pointing out an improvement of the autophagic flux, particularly for CENC preconditioning.


Keywords


coffee embedded nanocellulose; nanocellulose; C. jejuni CDT; HT-29 intestinal cells; vacuolar compartment; biological improving responses; mitochondrial damage

Full Text:

PDF


References


Athinarayanan J, Periasamy VS, Alsaif MA, et al. Presence of nanosilica (E551) in commercial food products: TNF-mediated oxidative stress and altered cell cycle progression in human lung fibroblast cells. Cell Biology and Toxicology. 2014; 30(2): 89-100. doi: 10.1007/s10565-014-9271-8 Gómez HC, Serpa A, Velásquez-Cock J, et al. Vegetable nanocellulose in food science: A review. Food Hydrocolloids. 2016; 57: 178-186. doi: 10.1016/j.foodhyd.2016.01.023 Khare S, DeLoid GM, Molina RM, et al. Effects of ingested nanocellulose on intestinal microbiota and homeostasis in Wistar Han rats. NanoImpact. 2020; 18: 100216. doi: 10.1016/j.impact.2020.100216 Onyango C, Unbehend G, Lindhauer MG. Effect of cellulose-derivatives and emulsifiers on creep-recovery and crumb properties of gluten-free bread prepared from sorghum and gelatinised cassava starch. Food Research International. 2009; 42(8): 949-955. doi: 10.1016/j.foodres.2009.04.011 Pereda M, Amica G, Rácz I, et al. Structure and properties of nanocomposite films based on sodium caseinate and nanocellulose fibers. Journal of Food Engineering. 2011; 103(1): 76-83. doi: 10.1016/j.jfoodeng.2010.10.001 Boluk Y, Lahiji R, Zhao L, et al. Suspension viscosities and shape parameter of cellulose nanocrystals (CNC). Colloids and Surfaces A: Physicochemical and Engineering Aspects. 2011; 377(1-3): 297-303. doi: 10.1016/j.colsurfa.2011.01.003 Kalashnikova I, Bizot H, Cathala B, et al. New Pickering Emulsions Stabilized by Bacterial Cellulose Nanocrystals. Langmuir. 2011; 27(12): 7471-7479. doi: 10.1021/la200971f Zhao GH, Kapur N, Carlin B, et al. Characterisation of the interactive properties of microcrystalline cellulose-carboxymethyl cellulose hydrogels. International Journal of Pharmaceutics. 2011; 415(1-2): 95-101. doi: 10.1016/j.ijpharm.2011.05.054 Tang L, Huang B, Lu Q, et al. Ultrasonication-assisted manufacture of cellulose nanocrystals esterified with acetic acid. Bioresource Technology. 2013; 127: 100-105. doi: 10.1016/j.biortech.2012.09.133 Paunonen SV, Hong RY. The many faces of assumed similarity in perceptions of personality. Journal of Research in Personality. 2013; 47(6): 800-815. doi: 10.1016/j.jrp.2013.08.007 Alves JS, dos Reis KC, Menezes EGT, et al. Effect of cellulose nanocrystals and gelatin in corn starch plasticized films. Carbohydrate Polymers. 2015; 115: 215-222. doi: 10.1016/j.carbpol.2014.08.057 Nsor-Atindana J, Chen M, Goff HD, et al. Functionality and nutritional aspects of microcrystalline cellulose in food. Carbohydrate Polymers. 2017; 172: 159-174. doi: 10.1016/j.carbpol.2017.04.021 Robson AA. Tackling obesity: can food processing be a solution rather than a problem? Agro Food Industry Hi-Tech. 2012; 23(2): 10-11. Cao X, Zhang T, DeLoid GM, et al. Cytotoxicity and cellular proteome impact of cellulose nanocrystals using simulated digestion and an in vitro small intestinal epithelium cellular model. NanoImpact. 2020; 20: 100269. doi: 10.1016/j.impact.2020.100269 Li Q, Wu Y, Fang R, et al. Application of Nanocellulose as particle stabilizer in food Pickering emulsion: Scope, Merits and challenges. Trends in Food Science & Technology. 2021; 110: 573-583. doi: 10.1016/j.tifs.2021.02.027 DeLoid GM, Cao X, Molina RM, et al. Toxicological effects of ingested nanocellulose in in vitro intestinal epithelium and in vivo rat models. Environmental Science: Nano. 2019; 6(7): 2105-2115. doi: 10.1039/c9en00184k Karimian A, Parsian H, Majidinia M, et al. Nanocrystalline cellulose: Preparation, physicochemical properties, and applications in drug delivery systems. International Journal of Biological Macromolecules. 2019; 133: 850-859. doi: 10.1016/j.ijbiomac.2019.04.117 Lanfranchi M, Giannetto C, Dimitrova V. Evolutionary aspects of coffee consumers’ buying habits: Results of a sample survey. Bulgarian Journal of Agricultural Science. 2016; 22(5): 705-712. Abuabara L, Paucar-Caceres A, Burrowes-Cromwell T. Consumers’ values and behaviour in the Brazilian coffee-in-capsules market: promoting circular economy. International Journal of Production Research. 2019; 57(23): 7269-7288. doi: 10.1080/00207543.2019.1629664 Chen H, Xu L, Yu K, et al. Release of microplastics from disposable cups in daily use. Science of The Total Environment. 2023; 854: 158606. doi: 10.1016/j.scitotenv.2022.158606 Corlett D, Stock Phot A. Nanoplastic should be better understood. Nature Nanotechnology. 2019; 14(4): 299-299. doi: 10.1038/s41565-019-0437-7 Cox KD, Covernton GA, Davies HL, et al. Human Consumption of Microplastics. Environmental Science & Technology. 2019; 53(12): 7068-7074. doi: 10.1021/acs.est.9b01517 Zangmeister CD, Radney JG, Benkstein KD, et al. Common Single-Use Consumer Plastic Products Release Trillions of Sub-100 nm Nanoparticles per Liter into Water during Normal Use. Environmental Science & Technology. 2022; 56(9): 5448-5455. doi: 10.1021/acs.est.1c06768 Rodríguez-Fabià S, Torstensen J, Johansson L, et al. Hydrophobisation of lignocellulosic materials part I: physical modification. Cellulose. 2022; 29(10): 5375-5393. doi: 10.1007/s10570-022-04620-8 Torstensen J, Ottesen V, Rodríguez-Fabià S, et al. The influence of temperature on cellulose swelling at constant water density. Scientific Reports. 2022; 12(1). doi: 10.1038/s41598-022-22092-5 Dagnon KL, Shanmuganathan K, Weder C, et al. Water-Triggered Modulus Changes of Cellulose Nanofiber Nanocomposites with Hydrophobic Polymer Matrices. Macromolecules. 2012; 45(11): 4707-4715. doi: 10.1021/ma300463y Liu L, Kong F. The behavior of nanocellulose in gastrointestinal tract and its influence on food digestion. Journal of Food Engineering. 2021; 292: 110346. doi: 10.1016/j.jfoodeng.2020.110346 Salatin S, Yari Khosroushahi A. Overviews on the cellular uptake mechanism of polysaccharide colloidal nanoparticles. Journal of Cellular and Molecular Medicine. 2017; 21(9): 1668-1686. doi: 10.1111/jcmm.13110 Wang T, Bai J, Jiang X, et al. Cellular Uptake of Nanoparticles by Membrane Penetration: A Study Combining Confocal Microscopy with FTIR Spectroelectrochemistry. ACS Nano. 2012; 6(2): 1251-1259. doi: 10.1021/nn203892h Crater JS, Carrier RL. Barrier Properties of Gastrointestinal Mucus to Nanoparticle Transport. Macromolecular Bioscience. 2010; 10(12): 1473-1483. doi: 10.1002/mabi.201000137 Bergin IL, Witzmann FA. Nanoparticle toxicity by the gastrointestinal route: evidence and knowledge gaps. International Journal of Biomedical Nanoscience and Nanotechnology. 2013; 3(1/2): 163. doi: 10.1504/ijbnn.2013.054515 Suvarna V, Nair A, Mallya R, et al. Antimicrobial Nanomaterials for Food Packaging. Antibiotics. 2022; 11(6): 729. doi: 10.3390/antibiotics11060729 Bintsis T. Foodborne pathogens. AIMS Microbiology. 2017; 3(3): 529-563. doi: 10.3934/microbiol.2017.3.529 Canonico B, Cesarini E, Montanari M, et al. Rapamycin Re-Directs Lysosome Network, Stimulates ER-Remodeling, Involving Membrane CD317 and Affecting Exocytosis, in Campylobacter Jejuni-Lysate-Infected U937 Cells. International Journal of Molecular Sciences. 2020; 21(6): 2207. doi: 10.3390/ijms21062207 Pickett CL, Pesci EC, Cottle DL, et al. Prevalence of cytolethal distending toxin production in Campylobacter jejuni and relatedness of Campylobacter sp. cdtB gene. Infection and Immunity. 1996; 64(6): 2070-2078. doi: 10.1128/iai.64.6.2070-2078.1996 Lara-Tejero M, Galán JE. A Bacterial Toxin That Controls Cell Cycle Progression as a Deoxyribonuclease I-Like Protein. Science. 2000; 290(5490): 354-357. doi: 10.1126/science.290.5490.354 Zhang Y, Huang R, Jiang Y, et al. The role of bacteria and its derived biomaterials in cancer radiotherapy. Acta Pharmaceutica Sinica B. 2023; 13(10): 4149-4171. doi: 10.1016/j.apsb.2022.10.013 Canonico B, Campana R, Luchetti F, et al. Campylobacter jejuni cell lysates differently target mitochondria and lysosomes on HeLa cells. Apoptosis. 2014; 19(8): 1225-1242. doi: 10.1007/s10495-014-1005-0 Canonico B, Di Sario G, Cesarini E, et al. Monocyte Response to Different Campylobacter jejuni Lysates Involves Endoplasmic Reticulum Stress and the Lysosomal-Mitochondrial Axis: When Cell Death Is Better Than Cell Survival. Toxins. 2018; 10(6): 239. doi: 10.3390/toxins10060239 Jongsma MLM, Berlin I, Wijdeven RHM, et al. An ER-Associated Pathway Defines Endosomal Architecture for Controlled Cargo Transport. Cell. 2016; 166(1): 152-166. doi: 10.1016/j.cell.2016.05.078 Nasoni MG, Carloni S, Canonico B, et al. Melatonin reshapes the mitochondrial network and promotes intercellular mitochondrial transfer via tunneling nanotubes after ischemic‐like injury in hippocampal HT22 cells. Journal of Pineal Research. 2021; 71(1). doi: 10.1111/jpi.12747 Canonico B, Cangiotti M, Montanari M, et al. Characterization of a fluorescent 1,8-naphthalimide-functionalized PAMAM dendrimer and its Cu(ii) complexes as cytotoxic drugs: EPR and biological studies in myeloid tumor cells. Biological Chemistry. 2022; 403(3): 345-360. doi: 10.1515/hsz-2021-0388 Salucci S, Burattini S, Battistelli M, et al. Tyrosol prevents apoptosis in irradiated keratinocytes. Journal of Dermatological Science. 2015; 80(1): 61-68. doi: 10.1016/j.jdermsci.2015.07.002 Fiorani M, De Matteis R, Canonico B, et al. Temporal correlation of morphological and biochemical changes with the recruitment of different mechanisms of reactive oxygen species formation during human SW872 cell adipogenic differentiation. BioFactors. 2021; 47(5): 837-851. doi: 10.1002/biof.1769 Fusi V, Formica M, Giorgi L, et al. Preparation of heterocyclic compounds as fluorescent probes for detection in biological systems. Available online: https://ora.uniurb.it/handle/11576/2675836.2 (accessed on 5 January 2023). Canonico B, Giorgi L, Nasoni MG, et al. Synthesis and biological characterization of a new fluorescent probe for vesicular trafficking based on polyazamacrocycle derivative. Biological Chemistry. 2021; 402(10): 1225-1237. doi: 10.1515/hsz-2021-0204 Tayeb A, Amini E, Ghasemi S, et al. Cellulose Nanomaterials—Binding Properties and Applications: A Review. Molecules. 2018; 23(10): 2684. doi: 10.3390/molecules23102684 Roman M, Winter WT. Effect of Sulfate Groups from Sulfuric Acid Hydrolysis on the Thermal Degradation Behavior of Bacterial Cellulose. Biomacromolecules. 2004; 5(5): 1671-1677. doi: 10.1021/bm034519 Čolić M, Tomić S, Bekić M. Immunological aspects of nanocellulose. Immunology Letters. 2020; 222: 80-89. doi: 10.1016/j.imlet.2020.04.004 Pereira MM, Raposo NRB, Brayner R, et al. Cytotoxicity and expression of genes involved in the cellular stress response and apoptosis in mammalian fibroblast exposed to cotton cellulose nanofibers. Nanotechnology. 2013; 24(7): 075103. doi: 10.1088/0957-4484/24/7/075103 Oh JH, Lee JT, Yang ES, et al. The coffee diterpene kahweol induces apoptosis in human leukemia U937 cells through down-regulation of Akt phosphorylation and activation of JNK. Apoptosis. 2009; 14(11): 1378-1386. doi: 10.1007/s10495-009-0407-x Jabir NR, Islam MT, Tabrez S, et al. An insight towards anticancer potential of major coffee constituents. BioFactors. 2018; 44(4): 315-326. doi: 10.1002/biof.1437 Prasanthi JRP, Dasari B, Marwarha G, et al. Caffeine protects against oxidative stress and Alzheimer’s disease-like pathology in rabbit hippocampus induced by cholesterol-enriched diet. Free Radical Biology and Medicine. 2010; 49(7): 1212-1220. doi: 10.1016/j.freeradbiomed.2010.07.007 Ko J, Kim JY, Kim J, et al. Anti-oxidative and anti-adipogenic effects of caffeine in an in vitro model of Graves’ orbitopathy. Endocrine Journal. 2020; 67(4): 439-447. doi: 10.1507/endocrj.ej19-0521 Silvério A dos SD, Pereira RGFA, Duarte SM da S, et al. Coffee beverage reduces ROS production and does not affect the organism s response against Candida albicans. Revista de Ciências Farmacêutica Básica e Aplicadas—RCFBA. 2020; 41. doi: 10.4322/2179-443x.0684 Castaldo L, Toriello M, Sessa R, et al. Antioxidant and Anti-Inflammatory Activity of Coffee Brew Evaluated after Simulated Gastrointestinal Digestion. Nutrients. 2021; 13(12): 4368. doi: 10.3390/nu13124368 To EE, Erlich JR, Liong F, et al. Therapeutic Targeting of Endosome and Mitochondrial Reactive Oxygen Species Protects Mice from Influenza Virus Morbidity. Frontiers in Pharmacology. 2022; 13: 870156. doi: 10.3389/fphar.2022.870156 Zeng Q, Ma X, Song Y, et al. Targeting regulated cell death in tumor nanomedicines. Theranostics. 2022; 12(2): 817-841. doi: 10.7150/thno.67932 Amatori S, Ambrosi G, Borgogelli E, et al. Modulating the Sensor Response to Halide Using NBD-Based Azamacrocycles. Inorganic Chemistry. 2014; 53(9): 4560-4569. doi: 10.1021/ic5001649 Miękus N, Marszałek K, Podlacha M, et al. Health Benefits of Plant-Derived Sulfur Compounds, Glucosinolates, and Organosulfur Compounds. Molecules. 2020; 25(17): 3804. doi: 10.3390/molecules25173804 Xie J, Liao B, Tang RY. Functional Application of Sulfur-Containing Spice Compounds. Journal of Agricultural and Food Chemistry. 2020; 68(45): 12505-12526. doi: 10.1021/acs.jafc.0c05002 Cano-Marquina A, Tarín JJ, Cano A. The impact of coffee on health. Maturitas. 2013; 75(1): 7-21. doi: 10.1016/j.maturitas.2013.02.002 Montanari M, Guescini M, Gundogdu O, et al. Extracellular Vesicles from Campylobacter jejuni CDT-Treated Caco-2 Cells Inhibit Proliferation of Tumour Intestinal Caco-2 Cells and Myeloid U937 Cells: Detailing the Global Cell Response for Potential Application in Anti-Tumour Strategies. International Journal of Molecular Sciences. 2022; 24(1): 487. doi: 10.3390/ijms24010487 Hickey TE, Majam G, Guerry P. Intracellular Survival of Campylobacter jejuni in Human Monocytic Cells and Induction of Apoptotic Death by Cytholethal Distending Toxin. Infection and Immunity. 2005; 73(8): 5194-5197. doi: 10.1128/iai.73.8.5194-5197.2005 Alzheimer M, Svensson SL, König F, et al. A three-dimensional intestinal tissue model reveals factors and small regulatory RNAs important for colonization with Campylobacter jejuni. PLOS Pathogens. 2020; 16(2): e1008304. doi: 10.1371/journal.ppat.1008304 Martin OCB, Frisan T. Bacterial Genotoxin-Induced DNA Damage and Modulation of the Host Immune Microenvironment. Toxins. 2020; 12(2): 63. doi: 10.3390/toxins12020063 Balta I, Butucel E, Stef L, et al. Anti-Campylobacter Probiotics: Latest Mechanistic Insights. Foodborne Pathogens and Disease. 2022; 19(10): 693-703. doi: 10.1089/fpd.2022.0039 Athinarayanan J, Alshatwi AA, Subbarayan Periasamy V. Biocompatibility analysis of Borassus flabellifer biomass-derived nanofibrillated cellulose. Carbohydrate Polymers. 2020; 235: 115961. doi: 10.1016/j.carbpol.2020.115961 Ventura C, Pinto F, Lourenço AF, et al. On the toxicity of cellulose nanocrystals and nanofibrils in animal and cellular models. Cellulose. 2020; 27(10): 5509-5544. doi: 10.1007/s10570-020-03176-9 Wang X, Qiu Y, Wang M, et al. Endocytosis and Organelle Targeting of Nanomedicines in Cancer Therapy. International Journal of Nanomedicine. 2020; 15: 9447-9467. doi: 10.2147/ijn.s274289 López-Galilea I, De Peña MP, Cid C. Correlation of Selected Constituents with the Total Antioxidant Capacity of Coffee Beverages: Influence of the Brewing Procedure. Journal of Agricultural and Food Chemistry. 2007; 55(15): 6110-6117. doi: 10.1021/jf070779x Acidri R, Sawai Y, Sugimoto Y, et al. Phytochemical Profile and Antioxidant Capacity of Coffee Plant Organs Compared to Green and Roasted Coffee Beans. Antioxidants. 2020; 9(2): 93. doi: 10.3390/antiox9020093 Andueza S, Cid C, Cristina Nicoli M. Comparison of antioxidant and pro-oxidant activity in coffee beverages prepared with conventional and “Torrefacto” coffee. LWT—Food Science and Technology. 2004; 37(8): 893-897. doi: 10.1016/j.lwt.2004.04.004 Cui WQ, Wang ST, Pan D, et al. Caffeine and its main targets of colorectal cancer. World Journal of Gastrointestinal Oncology. 2020; 12(2): 149-172. doi: 10.4251/wjgo.v12.i2.149 Lee C. Antioxidant ability of caffeine and its metabolites based on the study of oxygen radical absorbing capacity and inhibition of LDL peroxidation. Clinica Chimica Acta. 2000; 295(1-2): 141-154. doi: 10.1016/S0009-8981(00)00201-1 Soares MJ, Sampaio GR, Guizellini GM, et al. Regular and decaffeinated espresso coffee capsules: Unravelling the bioaccessibility of phenolic compounds and their antioxidant properties in milk model system upon in vitro digestion. LWT. 2021; 135: 110255. doi: 10.1016/j.lwt.2020.110255 Filomeni G, De Zio D, Cecconi F. Oxidative stress and autophagy: the clash between damage and metabolic needs. Cell Death & Differentiation. 2014; 22(3): 377-388. doi: 10.1038/cdd.2014.150 Roosen DA, Cookson MR. LRRK2 at the interface of autophagosomes, endosomes and lysosomes. Molecular Neurodegeneration. 2016; 11(1). doi: 10.1186/s13024-016-0140-1 Farias-Pereira R, Park CS, Park Y. Mechanisms of action of coffee bioactive components on lipid metabolism. Food Science and Biotechnology. 2019; 28(5): 1287-1296. doi: 10.1007/s10068-019-00662-0 Al-Bari MdAA, Ito Y, Ahmed S, et al. Targeting Autophagy with Natural Products as a Potential Therapeutic Approach for Cancer. International Journal of Molecular Sciences. 2021; 22(18): 9807. doi: 10.3390/ijms22189807 Silva FAGS, Dourado F, Gama M, et al. Nanocellulose Bio-Based Composites for Food Packaging. Nanomaterials. 2020; 10(10): 2041. doi: 10.3390/nano10102041 Bhattacharya K, Kiliç G, Costa PM, Fadeel B. Cytotoxicity screening and cytokine profiling of nineteen nanomaterials enables hazard ranking and grouping based on inflammogenic potential. Nanotoxicology. 2017; 11(6): 809-826. doi: 10.1080/17435390.2017.1363309 Stoudmann N, Schmutz M, Hirsch C, et al. Human hazard potential of nanocellulose: quantitative insights from the literature. Nanotoxicology. 2020; 14(9): 1241-1257. doi: 10.1080/17435390.2020.1814440 Hiura TS, Li N, Kaplan R, et al. The Role of a Mitochondrial Pathway in the Induction of Apoptosis by Chemicals Extracted from Diesel Exhaust Particles. The Journal of Immunology. 2000; 165(5): 2703-2711. doi: 10.4049/jimmunol.165.5.2703 Teodoro JS, Simões AM, Duarte FV, et al. Assessment of the toxicity of silver nanoparticles in vitro: A mitochondrial perspective. Toxicology in Vitro. 2011; 25(3): 664-670. doi: 10.1016/j.tiv.2011.01.004



DOI: https://doi.org/10.24294/can.v7i2.6414

Refbacks

  • There are currently no refbacks.


Copyright (c) 2024 Daniele Lopez, Giovanna Panza, Pietro Gobbi, Michele Guescini, Laura Valentini, Stefano Papa, Vieri Fusi, Eleonora Macedi, Daniele Paderni, Mariele Montanari, Barbara Canonico

License URL: https://creativecommons.org/licenses/by/4.0/

This site is licensed under a Creative Commons Attribution 4.0 International License.