Chicory; Gut microbiota; Hormone assay; In vitro apoptosis; In vitro pro-inflammatory cytokines; Transcriptomics; Food Science; Nutrition and Dietetics
Abstract :
[en] Industrial chicory has been the subject of numerous studies, most of which provide clinical observations on its health effects. Whether it is the roasted root, the flour obtained from the roots or the different classes of molecules that enter into the composition of this plant, understanding the molecular mechanisms of action on the human organism remains incomplete. In this study, we were interested in three molecules or classes of molecules present in chicory root: fructose, chlorogenic acids, and sesquiterpene lactones. We conducted experiments on the murine model and performed a nutrigenomic analysis, a metabolic hormone assay and a gut microbiota analysis, associated with in vitro observations for different responses. We have highlighted a large number of effects of all these classes of molecules that suggest a pro-apoptotic activity, an anti-inflammatory, antimicrobial, antioxidant, hypolipidemic and hypoglycemic effect and also an important role in appetite regulation. A significant prebiotic activity was also identified. Fructose seems to be the most involved in these activities, contributing to approximately 83% of recorded responses, but the other classes of tested molecules have shown a specific role for these different effects, with an estimated contribution of 23–24%.
Disciplines :
Food science
Author, co-author :
Pouille, Céline L.; UMR Transfrontalière BioEcoAgro N◦1158, Univ. Lille, INRAE, Univ. Liège, UPJV, JUNIA, Univ. Artois, Univ. Littoral Côte d’Opale, ICV, SFR Condorcet FR CNRS 3417—Institut Charles Viollette, Villeneuve d’Ascq, France ; Joint Laboratory CHIC41H, University of Lille-Florimond-Desprez, Villeneuve d’Ascq, France
Ouaza, Souad; UMR Transfrontalière BioEcoAgro N◦1158, Univ. Lille, INRAE, Univ. Liège, UPJV, JUNIA, Univ. Artois, Univ. Littoral Côte d’Opale, ICV, SFR Condorcet FR CNRS 3417—Institut Charles Viollette, Villeneuve d’Ascq, France ; Joint Laboratory CHIC41H, University of Lille-Florimond-Desprez, Villeneuve d’Ascq, France
Roels, Elise ; UMR Transfrontalière BioEcoAgro N◦1158, Univ. Lille, INRAE, Univ. Liège, UPJV, JUNIA, Univ. Artois, Univ. Littoral Côte d’Opale, ICV, SFR Condorcet FR CNRS 3417—Institut Charles Viollette, Villeneuve d’Ascq, France ; Joint Laboratory CHIC41H, University of Lille-Florimond-Desprez, Villeneuve d’Ascq, France
Behra, Josette; UMR Transfrontalière BioEcoAgro N◦1158, Univ. Lille, INRAE, Univ. Liège, UPJV, JUNIA, Univ. Artois, Univ. Littoral Côte d’Opale, ICV, SFR Condorcet FR CNRS 3417—Institut Charles Viollette, Villeneuve d’Ascq, France
Tourret, Melissa; UMR Transfrontalière BioEcoAgro N◦1158, Univ. Lille, INRAE, Univ. Liège, UPJV, JUNIA, Univ. Artois, Univ. Littoral Côte d’Opale, ICV, SFR Condorcet FR CNRS 3417—Institut Charles Viollette, Villeneuve d’Ascq, France
Molinié, Roland ; UMR Transfontalière BioEcoAgro N◦1158, Univ. Lille, INRAE, Univ. Liège, UPJV, JUNIA, Univ. Artois, Univ. Littoral Côte d’Opale, ICV, SFR Condorcet FR CNRS 3417—BIOlogie des Plantes et Innovation (BIOPI), Amiens, France
Fontaine, Jean-Xavier ; UMR Transfontalière BioEcoAgro N◦1158, Univ. Lille, INRAE, Univ. Liège, UPJV, JUNIA, Univ. Artois, Univ. Littoral Côte d’Opale, ICV, SFR Condorcet FR CNRS 3417—BIOlogie des Plantes et Innovation (BIOPI), Amiens, France
Mathiron, David ; Plateforme Analytique UFR des Sciences, UPJV, Bâtiment Serres-Transfert Rue Dallery-Passage du Sourire d’Avril, Amiens, France
Gagneul, David ; UMR Transfrontalière BioEcoAgro N◦1158, Univ. Lille, INRAE, Univ. Liège, UPJV, JUNIA, Univ. Artois, Univ. Littoral Côte d’Opale, ICV, SFR Condorcet FR CNRS 3417—Institut Charles Viollette, Villeneuve d’Ascq, France ; Joint Laboratory CHIC41H, University of Lille-Florimond-Desprez, Villeneuve d’Ascq, France
Taminiau, Bernard ; Université de Liège - ULiège > Fundamental and Applied Research for Animals and Health (FARAH) > FARAH: Santé publique vétérinaire
Daube, Georges ; Université de Liège - ULiège > Fundamental and Applied Research for Animals and Health (FARAH) > FARAH: Santé publique vétérinaire
Funding: This work has been supported by the Région des Hauts-de-France via ALIBIOTECH Institutional Review Board Statement: The study was conducted according to the Directive 2010/63/ EEC for the protection of animals used for fine scientists and in accordance with Law 2012-10 (2012)B.T., J.-X.F., D.M. and R.M.; Writing—Original Draft Preparation, A.L.-D. and C.L.P.; Writing—Review and R.M.; Formal analysis, C.L.P., A.L.-D., E.R., S.O., B.T., M.T. and D.M.; Validation, S.O.; Data and Editing, B.C., C.R., J.-L.H., B.T., G.D., J.B., R.M., D.G. and D.M.; Supervision, R.R., G.D., J.-L.H., curation, B.T., J.-X.F., D.M. and R.M.; Writing—Original Draft Preparation, A.L.-D. and C.L.P.; Writ-D.G. and C.R.; Project administration, C.R.; Funding acquisition, C.R. and J.-L.H. All authors have ing—Review and Editing, B.C., C.R., J.-L.H., B.T., G.D., J.B., R.M., D.G. and D.M.; Supervision, R.R., read and agreed to the published version of the manuscript. G.D., J.-L.H., D.G. and C.R.; Project administration, C.R.; Funding acquisition, C.R. and J.-L.H. All Funding: This work has been supported by the Région des Hauts-de-France via ALIBIOTECHThis work has been supported by the R?gion des Hauts-de-France via ALIBIOTECH CPER/FEDER 2016?2021 and FEDER for CHIC41H 2019?2021 programs.
Perović, J.; Tumbas Šaponjac, V.; Kojić, J.; Krulj, J.; Moreno, D.A.; García-Viguera, C.; Bodroža-Solarov, M.; Ilić, N. Chicory (Cichorium intybus L.) as a food ingredient—Nutritional composition, bioactivity, safety, and health claims: A review. Food Chem. 2021, 336, 127676. [CrossRef] [PubMed]
Pouille, C.L.; Jegou, D.; Dugardin, C.; Cudennec, B.; Ravallec, R.; Hance, P.; Rambaud, C.; Hilbert, J.L.; Lucau-Danila, A. Chicory root flour—A functional food with potential multiple health benefits evaluated in a mice model. J. Funct. Foods 2020, 74, 104174. [CrossRef]
Reimer, R.A.; Soto-Vaca, A.; Nicolucci, A.C.; Mayengbam, S.; Park, H.; Madsen, K.L.; Menon, R.; Vaughan, E.E. Effect of chicory inulin-type fructan–containing snack bars on the human gut microbiota in low dietary fiber consumers in a randomized crossover trial. Am. J. Clin. Nutr. 2020, 111, 1286–1296. [CrossRef]
EFSA Panel on Nutrition, Novel Foods and Food Allergens (NDA). Frutalose®, a mixture of fructans obtained from enzymatic hydrolysis of chicory inulin, and normal defecation: Evaluation of a health claim pursuant to Article 13 of Regulation (EC) No 1924/2006. EFSA J. 2021, 19, e06775. [CrossRef]
Ferrare, K.; Bidel, L.P.; Awwad, A.; Poucheret, P.; Cazals, G.; Lazennec, F.; Azay-Milhau, J.; Tournier, M.; Lajoix, A.D.; Tousch, D. Increase in insulin sensitivity by the association of chicoric acid and chlorogenic acid contained in a natural chicoric acid extract (NCRAE) of chicory (Cichorium intybus L.) for an antidiabetic effect. J. Ethnopharmacol. 2018, 215, 241–248. [CrossRef] [PubMed]
Epure, A.; Pârvu, A.E.; Vlase, L.; Benedec, D.; Hanganu, D.; Gheldiu, A.M.; Toma, V.A.; Oniga, I. Phytochemical profile, antioxidant, cardioprotective and nephroprotective activity of romanian chicory extract. Plants 2021, 10, 64. [CrossRef] [PubMed]
Bernard, G.; Alves Dos Santos, H.A.D.; Etienne, A.; Samaillie, J.; Neut, C.; Sahpaz, S.; Hilbert, J.L.; Gagneul, D.; Jullian, N.; Tahrioui, A.; et al. MeJA elicitation of chicory hairy roots promotes efficient increase of 3,5-diCQA accumulation, a potent antioxidant and antibacterial molecule. Antibiotics 2020, 9, 659. [CrossRef]
Peña-Espinoza, M.; Williams, A.R.; Thamsborg, S.M.; Simonsen, H.T.; Enemark, H.L. Anthelmintic effects of forage chicory (Cichorium intybus) against free-living and parasitic stages of Cooperia oncophora. Vet. Parasitol. 2017, 243, 204–207. [CrossRef]
Peña-Espinoza, M.; Valente, A.H.; Bornancin, L.; Simonsen, H.T.; Thamsborg, S.M.; Williams, A.R.; López-Muñoz, R. Anthelmintic and metabolomic analyses of chicory (Cichorium intybus) identify an industrial by-product with potent in vitro antinematodal activity. Vet. Parasitol. 2020, 280, 109088. [CrossRef]
Valente, A.H.; de Roode, M.; Ernst, M.; Peña-Espinoza, M.; Bornancin, L.; Bonde, C.S.; Martínez-Valladares, M.; Ramünke, S.; Krücken, J.; Simonsen, H.T.; et al. Identification of compounds responsible for the anthelmintic effects of chicory (Cichorium intybus) by molecular networking and bio-guided fractionation. Int. J. Parasitol. Drugs Drug Resist. 2021, 15, 105–114. [CrossRef]
Karadeniz, F.; Oh, J.H.; Kong, C.-S. Sesquiterpene lactones: A review of biological activities. J. Life Sci. 2021, 31, 430–441. [CrossRef]
Abbas, Z.K.; Saggu, S.; Sakeran, M.I.; Zidan, N.; Rehman, H.; Ansari, A.A. Phytochemical, antioxidant and mineral composition of hydroalcoholic extract of chicory (Cichorium intybus L.) leaves. Saudi J. Biol. Sci. 2015, 22, 322–326. [CrossRef] [PubMed]
Hoste, H.; Jackson, F.; Athanasiadou, S.; Thamsborg, S.M.; Hoskin, S.O. The effects of tannin-rich plants on parasitic nematodes in ruminants. Trends Parasitol. 2006, 22, 253–261. [CrossRef] [PubMed]
Tchoumtchoua, J.; Mathiron, D.; Pontarin, N.; Gagneul, D.; van Bohemen, A.-I.; Otogo N’nang, E.; Mesnard, F.; Petit, E.; Fontaine, J.-X.; Molinié, R.; et al. Phenolic profiling of flax highlights contrasting patterns in winter and spring varieties. Molecules 2019, 24, 4303. [CrossRef] [PubMed]
Deborde, C.; Fontaine, J.-X.; Jacob, D.; Botana, A.; Nicaise, V.; Richard-Forget, F.; Lecomte, S.; Decourtil, C.; Hamade, K.; Mesnard, F.; et al. Optimizing 1D 1H-NMR profiling of plant samples for high throughput analysis: Extract preparation, standardization, automation and spectra processing. Metabolomics 2019, 15, 28. [CrossRef] [PubMed]
Jacob, D.; Deborde, C.; Lefebvre, M.; Maucourt, M.; Moing, A. NMRProcFlow: A graphical and interactive tool dedicated to 1D spectra processing for NMR-based metabolomics. Metabolomics 2017, 13, 36. [CrossRef] [PubMed]
Fouré, M.; Dugardin, C.; Foligné, B.; Hance, P.; Cadalen, T.; Delcourt, A.; Taminiau, B.; Daube, G.; Ravallec, R.; Cudennec, B.; et al. Chicory roots for prebiotics and appetite regulation: A pilot study in mice. J. Agric. Food Chem. 2018, 66, 6439–6449. [CrossRef]
Willeman, H. Contribution à la Recherche des Composés Impliqués dans L’amertume de la Racine de Chicorée: Approches Métabolomique et Sensorielle de L’influence de la Torréfaction. Ph.D. Thesis, University of Lille, Lille, France, 2016. Available online: https://www.theses.fr/2016LIL10222 (accessed on 21 January 2022).
Obafemi, C.A.; Sulaimon, T.O.; Akinpelu, D.A.; Olugbade, T.A. Antimicrobial activity of extracts and a germacranolidetype sesquiterpene lactone from Tithonia diversifolia leaf extract. Afr. J. Biotechnol. 2006, 5, 1254–1258. [CrossRef]
Passos, C.P.; Costa, R.M.; Ferreira, S.S.; Lopes, G.R.; Cruz, M.T.; Coimbra, M.A. Role of coffee caffeine and chlorogenic acids adsorption to polysaccharides with impact on brew immunomodulation effects. Foods 2021, 10, 378. [CrossRef]
Rognes, T.; Flouri, T.; Nichols, B.; Quince, C.; Mahé, F. VSEARCH: A versatile open source tool for metagenomics. Peer J. 2016, 4, e2584. [CrossRef] [PubMed]
Gérard, A.; El-Hajjaji, S.; Burteau, S.; Fall, P.A.; Pirard, B.; Taminiau, B.; Daube, G.; Sindic, M. Study of the microbial diversity of a panel of Belgian artisanal cheeses associated with challenge studies for Listeria monocytogenes. Food Microbiol. 2021, 100, 103861. [CrossRef] [PubMed]
Ma, X.; Tian, X.; Huang, X.; Yan, F.; Qiao, D. Resveratrol-induced mitochondrial dysfunction and apoptosis are associated with Ca2+ and mCICR-mediated MPT activation in HepG2 cells. Mol. Cell. Biochem. 2007, 302, 99–109. [CrossRef] [PubMed]
Aruoma, O.I.; Halliwell, B.; Hoey, B.M.; Butler, J. The antioxidant action of N-acetylcysteine: Its reaction with hydrogen peroxide, hydroxyl radical, superoxide, and hypochlorous acid. Free Radical Biol. Med. 1989, 6, 593–597. [CrossRef]
Halliwell, B.; Gutteridge, J.M.; Aruoma, O.I. The deoxyribose method: A simple “test-tube” assay for determination of rate constants for reactions of hydroxyl radicals. Anal. Biochem. 1987, 165, 215–219. [CrossRef]
Heurtier, V.; Owens, N.; Gonzalez, I.; Mueller, F.; Proux, C.; Mornico, D.; Clerc, P.; Dubois, A.; Navarro, P. The molecular logic of Nanog-induced self-renewal in mouse embryonic stem cells. Nat. Commun. 2019, 10, 1109. [CrossRef]
Gong, S.; Li, Q.; Jeter, C.R.; Fan, Q.; Tang, D.G.; Liu, B. Regulation of NANOG in cancer cells. Mol. Carcinog. 2015, 54, 679–687. [CrossRef]
Gawlik-Rzemieniewska, N.; Bednarek, I. The role of NANOG transcriptional factor in the development of malignant phenotype of cancer cells. Cancer Biol. Ther. 2016, 17, 1–10. [CrossRef]
Santaliz-Ruiz, L.E.; Xie, X.; Old, M.; Teknos, T.N.; Pan, Q. Emerging role of nanog in tumorigenesis and cancer stem cells. Int. J. Cancer 2014, 135, 2741–2748. [CrossRef]
O’Leary, V.B.; Smida, J.; Buske, F.A.; Carrascosa, L.G.; Azimzadeh, O.; Maugg, D.; Hain, S.; Tapio, S.; Heidenreich, W.; Kerr, J.; et al. PARTICLE triplexes cluster in the tumor suppressor WWOX and may extend throughout the human genome. Sci. Rep. 2017, 7, 7163. [CrossRef] [PubMed]
Delbridge, A.R.D.; Valente, L.J.; Strasser, A. The role of the apoptotic machinery in tumor suppression. Cold Spring Harbor Perspect. Biol. 2012, 4, a008789. [CrossRef] [PubMed]
Finsterbusch, F.; Ravindranathan, R.; Dereli, I.; Stanzione, M.; Tränkner, D.; Tóth, A. Alignment of homologous chromosomes and effective repair of programmed DNA double-strand breaks during mouse meiosis require the minichromosome maintenance domain containing 2 (MCMDC2) protein. PLoS Genet. 2016, 12, e1006393. [CrossRef]
Parr, C.; Jiang, W.G. Metastasis suppressor 1 (MTSS1) demonstrates prognostic value and anti-metastatic properties in breast cancer. Eur. J. Cancer 2009, 45, 1673–1683. [CrossRef] [PubMed]
Du, P.; Ye, L.; Yang, Y.; Jiang, W.G. The tumour suppressive role of metastasis suppressor-1, MTSS1, in human kidney cancer, a possible connection with the SHH pathway. J. Exp. Ther. Oncol. 2012, 10, 91–99.
Wang, X.X.; Liu, B.B.; Wu, X.; Su, D.; Zhu, Z.; Fu, L. Loss of leucine zipper putative tumor suppressor 1 (LZTS1) expression contributes to lymph node metastasis of breast invasive micropapillary carcinoma. Pathol. Oncol. Res. 2015, 21, 1021–1026. [CrossRef]
Shi, Z.; Li, Z.; Li, Z.J.; Cheng, K.; Du, Y.; Fu, H.; Khuri, F.R. Cables1 controls p21/Cip1 protein stability by antagonizing proteasome subunit alpha type 3. Oncogene 2015, 34, 2538–2545. [CrossRef]
Murakami, T.; Takano, R.; Takeo, S.; Taniguchi, R.; Ogawa, K.; Ohashi, E.; Tsurimoto, T. Stable interaction between the human proliferating cell nuclear antigen loader complex Ctf18-replication factor C (RFC) and DNA polymerase ɛ is mediated by the cohesion-specific subunits, Ctf18, Dcc1, and Ctf8. J. Biol. Chem. 2010, 285, 34608–34615. [CrossRef]
Saleem, M.; Abbas, K.; Naseer, F.; Ahmad, M.; Syed, N.H.; Javed, F.; Hussain, K.; Asima, S. Anticancer activity of n-hexane extract of Cichorium intybus on lymphoblastic leukemia cells (Jurkat cells). Afr. J. Plant Sci. 2014, 8, 315–319. [CrossRef]
Mehrandish, R.; Awsat Mellati, A.; Rahimipour, A.; Dehghan Nayeri, N. Anti-cancer activity of methanol extracts of Cichorium intybus on human breast cancer SKBR3 cell line. Razavi Int. J. Med. 2016, 5, 1–4. [CrossRef]
Narayana, S.V.; Carson, M.; el-Kabbani, O.; Kilpatrick, J.M.; Moore, D.; Chen, X.; Bugg, C.E.; Volanakis, J.E.; DeLucas, L.J. Structure of human factor D. A complement system protein at 2.0 A resolution. J. Mol. Biol. 1994, 235, 695–708. [CrossRef]
Ripoll, C.; Schmidt, B.M.; Ilic, N.; Poulev, A.; Dey, M.; Kurmukov, A.G.; Raskin, I. Anti-inflammatory effects of a sesquiterpene lactone extract from chicory (Cichorium intybus L.) roots. Nat. Prod. Commun. 2007, 2, 1934578X0700200. [CrossRef]
Matos, M.S.; Anastácio, J.D.; Allwood, J.W.; Carregosa, D.; Marques, D.; Sungurtas, J.; McDougall, G.J.; Menezes, R.; Matias, A.A.; Stewart, D.; et al. Assessing the intestinal permeability and anti-inflammatory potential of sesquiterpene lactones from chicory. Nutrients 2020, 12, 3547. [CrossRef]
Meo, S.A.; Al-Asiri, S.A.; Mahesar, A.L.; Ansari, M.J. Role of honey in modern medicine. Saudi J. Biol. Sci. 2017, 24, 975–978. [CrossRef]
Nowrouzi, P.; Mazani, M.; Rezagholizadeh, L.; Banaei, S. Mechanism and clinical aspects of the effects of chicory on diabetes. Asian J. Res. Med. Pharm. Sci. 2017, 1, 1–11. [CrossRef]
Nishimura, M.; Ohkawara, T.; Kanayama, T.; Kitagawa, K.; Nishimura, H.; Nishihira, J. Effects of the extract from roasted chicory (Cichorium intybus L.) root containing inulin-type fructans on blood glucose, lipid metabolism, and fecal properties. J. Tradit. Complement. Med. 2015, 5, 161–167. [CrossRef] [PubMed]
Minneé, E.; Waghorn, G.; Lee, J.; Clark, C. Including chicory or plantain in a perennial ryegrass/white clover-based diet of dairy cattle in late lactation: Feed intake, milk production and rumen digestion. Anim. Feed Sci. Technol. 2017, 227, 52–61. [CrossRef]
Niderkorn, V.; Martin, C.; Bernard, M.; le Morvan, A.; Rochette, Y.; Baumont, R. Effect of increasing the proportion of chicory in forage-based diets on intake and digestion by sheep. Animal 2019, 13, 718–726. [CrossRef] [PubMed]
Khoobani, M.; Hasheminezhad, S.H.; Javandel, F.; Nosrati, M.; Seidavi, A.; Kadim, I.T.; Laudadio, V.; Tufarelli, V. Effects of dietary chicory (Chicorium intybus L.) and probiotic blend as natural feed additives on performance traits, blood biochemistry, and gut microbiota of broiler chickens. Antibiotics 2019, 9, 5. [CrossRef] [PubMed]
Plump, A.S.; Azrolan, N.; Odaka, H.; Wu, L.; Jiang, X.; Tall, A.; Eisenberg, S.; Breslow, J.L. ApoA-I knockout mice: Characterization of HDL metabolism in homozygotes and identification of a post-RNA mechanism of apoA-I up-regulation in heterozygotes. J. Lipid Res. 1997, 38, 1033–1047. [CrossRef]
Vanhooren, J.C.T.; Fransen, M.; Bethune, B.; Baumgart, E.; Baes, M.; Torrekens, S.; Leuven, F.; Mannaerts, G.P.; Veldhoven, P.P. Rat Pristanoyl-CoA Oxidase. cDNA Cloning and recognition of its C-Terminal (SQL) by the peroxisomal-targeting signal 1 receptor. Eur. J. Biochem. 1996, 239, 302–309. [CrossRef]
Aoki, J.; Inoue, A.; Okudaira, S. Two pathways for lysophosphatidic acid production. Biochim. Biophys. Acta Mol. Cell Biol. Lipids 2008, 1781, 513–518. [CrossRef]
Chen, C.; Wang, H.; Chen, B.; Chen, D.; Lu, C.; Li, H.; Qian, Y.; Tan, Y.; Weng, H.; Cai, L. Pex11a deficiency causes dyslipidaemia and obesity in mice. J. Cell. Mol. Med. 2018, 23, 2020–2031. [CrossRef]
Weng, H.; Ji, X.; Naito, Y.; Endo, K.; Ma, X.; Takahashi, R.; Shen, C.; Hirokawa, G.; Fukushima, Y.; Iwai, N. Pex11α deficiency impairs peroxisome elongation and division and contributes to nonalcoholic fatty liver in mice. Am. J. Physiol. Endocrinol. Metab. 2013, 304, E187–E196. [CrossRef]
Joshi, A.; Rajput, S.; Wang, C.; Ma, J.; Cao, D. Murine aldo-keto reductase family 1 subfamily B: Identification of AKR1B8 as an ortholog of human AKR1B10. Biol. Chem. 2010, 391, 1371–1378. [CrossRef] [PubMed]
Zoöller, I.; Meixner, M.; Hartmann, D.; Bussow, H.; Meyer, R.; Gieselmann, V.; Eckhardt, M. Absence of 2-hydroxylated sphingolipids is compatible with normal neural development but causes late-onset axon and myelin sheath degeneration. J. Neurosci. 2008, 28, 9741–9754. [CrossRef] [PubMed]
Garman, S.C.; Garboczi, D.N. The molecular defect leading to Fabry disease: Structure of human α-galactosidase. J. Mol. Biol. 2004, 337, 319–335. [CrossRef] [PubMed]
Prolo, P.; Wong, M.L.; Licinio, J. Leptin. Int. J. Biochem. Cell Biol. 1998, 30, 1285–1290. [CrossRef]
van Wijk, R.; van Solinge, W.W. The energy-less red blood cell is lost: Erythrocyte enzyme abnormalities of glycolysis. Blood 2005, 106, 4034–4042. [CrossRef]
Wang, L.; Tong, X.; Gu, F.; Zhang, L.; Chen, W.; Cheng, X.; Xie, L.; Chang, Y.; Zhang, H. The KLF14 transcription factor regulates hepatic gluconeogenesis in mice. J. Biol. Chem. 2017, 292, 21631–21642. [CrossRef]
Erejuwa, O.O.; Sulaiman, S.A.; Wahab, M.S.A. Fructose might contribute to the hypoglycemic effect of honey. Molecules 2012, 17, 1900–1915. [CrossRef]
Jin, T. Mechanisms underlying proglucagon gene expression. J. Endocrinol. 2008, 198, 17–28. [CrossRef]
Cai, T.; Chen, X.; Wang, R.; Xu, H.; You, Y.; Zhang, T.; Lan, M.S.; Notkins, A.L. Expression of insulinoma-associated 2 (INSM2) in pancreatic islet cells is regulated by the transcription factors Ngn3 and NeuroD1. Endocrinology 2011, 152, 1961–1969. [CrossRef]
Seino, Y.; Fukushima, M.; Yabe, D. GIP and GLP-1, the two incretin hormones: Similarities and differences. J. Diabetes Investig. 2010, 1, 8–23. [CrossRef] [PubMed]
Lepczyński, A.; Herosimczyk, A.; Ożgo, M.; Barszcz, M.; Taciak, M.; Skomiał, J. Modification of ileal proteome in growing pigs by dietary supplementation with inulin or dried chicory root. J. Anim. Feed Sci. 2019, 28, 177–186. [CrossRef]
Matsuoka, Y.; Li, X.; Bennett, V. Adducin: Structure, function and regulation. Cell. Mol. Life Sci. 2000, 57, 884–895. [CrossRef] [PubMed]
Kiang, K.M.Y.; Leung, G.K.K. A review on adducin from functional to pathological mechanisms: Future direction in cancer. BioMed Res. Int. 2018, 2018, 3465929. [CrossRef] [PubMed]
McClard, C.K.; Kochukov, M.Y.; Herman, I.; Liu, Z.; Eblimit, A.; Moayedi, Y.; Ortiz-Guzman, J.; Colchado, D.; Pekarek, B.; Panneerselvam, S.; et al. POU6f1 mediates neuropeptide-dependent plasticity in the adult brain. J. Neurosci. 2018, 38, 1443–1461. [CrossRef]
Berkemeier, L.R.; Winslow, J.W.; Kaplan, D.R.; Nikolics, K.; Goeddel, D.V.; Rosenthal, A. Neurotrophin-5: A novel neurotrophic factor that activates trk and trkB. Neuron 1991, 7, 857–866. [CrossRef]
Liebl, D.J.; Mbiene, J.P.; Parada, L.F. NT4/5 mutant mice have deficiency in gustatory papillae and taste bud formation. Dev. Biol. 1999, 213, 378–389. [CrossRef]
Moretti, P.; Levenson, J.M.; Battaglia, F.; Atkinson, R.; Teague, R.; Antalffy, B.; Armstrong, D.; Arancio, O.; Sweatt, J.D.; Zoghbi, H.Y. Learning and memory and synaptic plasticity are impaired in a mouse model of Rett syndrome. J. Neurosci. 2006, 26, 319–327. [CrossRef]
Schlager, M.A.; Kapitein, L.C.; Grigoriev, I.; Burzynski, G.M.; Wulf, P.S.; Keijzer, N.; de Graaff, E.; Fukuda, M.; Shepherd, I.T.; Akhmanova, A.; et al. Pericentrosomal targeting of Rab6 secretory vesicles by bicaudal-D-related protein 1 (BICDR-1) regulates neuritogenesis. EMBO J. 2010, 29, 1637–1651. [CrossRef]
Peeters, P.J.; Baker, A.; Goris, I.; Daneels, G.; Verhasselt, P.; Luyten, W.H.; Geysen, J.J.; Kass, S.U.; Moechars, D.W. Sensory deficits in mice hypomorphic for a mammalian homologue of unc-53. Dev. Brain Res. 2004, 150, 89–101. [CrossRef]
Seco, C.Z.; Oonk, A.M.; Domínguez-Ruiz, M.; Draaisma, J.M.; Gandía, M.; Oostrik, J.; Neveling, K.; Kunst, H.P.; Hoefsloot, L.H.; del Castillo, I.; et al. Progressive hearing loss and vestibular dysfunction caused by a homozygous nonsense mutation in CLIC5. Eur. J. Hum. Genet. 2014, 23, 189–194. [CrossRef] [PubMed]
Shirokova, E.; Raguse, J.D.; Meyerhof, W.; Krautwurst, D. The human vomeronasal type-1 receptor family—Detection of volatiles and cAMP signaling in HeLa/Olf cells. FASEB J. 2008, 22, 1416–1425. [CrossRef] [PubMed]
Basch, M.L.; Bronner-Fraser, M.; García-Castro, M.I. Specification of the neural crest occurs during gastrulation and requires Pax7. Nature 2006, 441, 218–222. [CrossRef] [PubMed]
Barman, A.; Assmann, A.; Richter, S.; Soch, J.; Schütze, H.; Wüstenberg, T.; Deibele, A.; Klein, M.; Richter, A.; Behnisch, G.; et al. Genetic variation of the RASGRF1 regulatory region affects human hippocampus-dependent memory. Front. Hum. Neurosci. 2014, 8, 260. [CrossRef] [PubMed]
Niu, S.; Shingle, D.L.; Garbarino-Pico, E.; Kojima, S.; Gilbert, M.; Green, C.B. The circadian deadenylase nocturnin is necessary for stabilization of the iNOS mRNA in mice. PLoS ONE 2011, 6, e26954. [CrossRef]
Payant, M.A.; Chee, M.J. Neural mechanisms underlying the role of fructose in overfeeding. Neurosci. Biobehav. Rev. 2021, 128, 346–357. [CrossRef]
Wijlens, A.; Mars, M.; Dull, D.; de Graaf, K. Short term effect of chicory root fibre on appetite ratings and energy intake. Appetite 2013, 71, 490. [CrossRef]
Crean, D.; Bellwon, P.; Aschauer, L.; Limonciel, A.; Moenks, K.; Hewitt, P.; Schmidt, T.; Herrgen, K.; Dekant, W.; Lukas, A.; et al. Development of an in vitro renal epithelial disease state model for xenobiotic toxicity testing. Toxicol. Vitr. 2015, 30, 128–137. [CrossRef]
Capasso, M.; Bhamrah, M.K.; Henley, T.; Boyd, R.S.; Langlais, C.; Cain, K.; Dinsdale, D.; Pulford, K.; Khan, M.; Musset, B.; et al. HVCN1 modulates BCR signal strength via regulation of BCR-dependent generation of reactive oxygen species. Nat. Immunol. 2010, 11, 265–272. [CrossRef] [PubMed]
Zhou, S.G.; Wang, P.; Pi, R.B.; Gao, J.; Fu, J.J.; Fang, J.; Qin, J.; Zhang, H.J.; Li, R.F.; Chen, S.R.; et al. Reduced expression of GSTM2 and increased oxidative stress in spontaneously hypertensive rat. Mol. Cell. Biochem. 2008, 309, 99–107. [CrossRef] [PubMed]
Tornio, A.; Backman, J.T. Cytochrome P450 in pharmacogenetics: An update. Adv. Pharmacol. 2018, 83, 3–32. [CrossRef] [PubMed]
Jasim, R.S. Antioxidant, antimicrobial activities and phytochemical constituents of Cichorium intybus L. Aerial Parts. Int. J. Bot. 2018, 14, 24–29. [CrossRef]
Turnbaugh, P.J.; Bäckhed, F.; Fulton, L.; Gordon, J.I. Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host Microbe 2008, 3, 213–223. [CrossRef]
Wen, L.; Ley, R.E.; Volchkov, P.Y.; Stranges, P.B.; Avanesyan, L.; Stonebraker, A.C.; Hu, C.; Wong, F.S.; Szot, G.L.; Bluestone, J.A.; et al. Innate immunity and intestinal microbiota in the development of Type 1 diabetes. Nature 2008, 455, 1109–1113. [CrossRef]
Braak, H.; de Vos, R.A.; Bohl, J.; del Tredici, K. Gastric α-synuclein immunoreactive inclusions in Meissner’s and Auerbach’s plexuses in cases staged for Parkinson’s disease-related brain pathology. Neurosci. Lett. 2006, 396, 67–72. [CrossRef]
Jin, M.; Li, J.; Liu, F.; Lyu, N.; Wang, K.; Wang, L.; Liang, S.; Tao, H.; Zhu, B.; Alkasir, R. Analysis of the gut microflora in patients with Parkinson’s disease. Front. Neurosci. 2019, 13, 1184. [CrossRef]
Trzeciak, P.; Herbet, M. Role of the Intestinal microbiome, intestinal barrier and psychobiotics in depression. Nutrients 2021, 13, 927. [CrossRef]
Sarkar, A.; Lehto, S.M.; Harty, S.; Dinan, T.G.; Cryan, J.F.; Burnet, P.W. Psychobiotics and the manipulation of bacteria–gut–brain signals. Trends Neurosci. 2016, 39, 763–781. [CrossRef]
Medlock, G.L.; Carey, M.A.; McDuffie, D.G.; Mundy, M.B.; Giallourou, N.; Swann, J.R.; Kolling, G.L.; Papin, J.A. Inferring metabolic mechanisms of interaction within a defined gut microbiota. Cell Syst. 2018, 7, 245–257.e7. [CrossRef]
Ignacio, A.; Fernandes-Terra, F.; Watanabe, I.; Basso, P.J.; Câmara, N. Role of the microbiome in intestinal barrier function and immune defense. In Microbiome and Metabolome in Diagnosis, Therapy, and Other Strategic Applications, 1st ed.; Faintuch, J., Faintuch, S., Eds.; Academic Press: Boston, MA, USA, 2019; pp. 127–138. [CrossRef]
Clavel, T.; Lepage, P.; Charrier, C. The family Coriobacteriaceae. In The Prokaryotes, 1st ed.; Rosenberg, E., DeLong, E.F., Lory, S., Stackebrandt, E., Thompson, F., Eds.; Springer: Berlin/Heidelberg, Germany, 2014; pp. 201–238. [CrossRef]
Kim, H.N.; Joo, E.J.; Cheong, H.S.; Kim, Y.; Kim, H.L.; Shin, H.; Chang, Y.; Ryu, S. Gut microbiota and risk of persistent nonalcoholic fatty liver diseases. J. Clin. Med. 2019, 8, 1089. [CrossRef] [PubMed]
Liu, G.; Zhao, Q.; Wei, H. Characteristics of intestinal bacteria with fatty liver diseases and cirrhosis. Ann. Hepatol. 2019, 18, 796–803. [CrossRef]
Ruuskanen, M.O.; Åberg, F.; Männistö, V.; Havulinna, A.S.; Méric, G.; Liu, Y.; Loomba, R.; Vázquez-Baeza, Y.; Tripathi, A.; Valsta, L.M.; et al. Links between gut microbiome composition and fatty liver disease in a large population sample. Gut Microbes 2021, 13, 1–22. [CrossRef] [PubMed]
Maki, K.A.; Burke, L.A.; Calik, M.W.; Watanabe-Chailland, M.; Sweeney, D.; Romick-Rosendale, L.E.; Green, S.J.; Fink, A.M. Sleep fragmentation increases blood pressure and is associated with alterations in the gut microbiome and fecal metabolome in rats. Physiol. Genom. 2020, 52, 280–292. [CrossRef]
Kaakoush, N.O. Insights into the role of Erysipelotrichaceae in the human host. Front. Cell. Infect. Microbiol. 2015, 5, 84. [CrossRef]
Dinh, D.M.; Volpe, G.E.; Duffalo, C.; Bhalchandra, S.; Tai, A.K.; Kane, A.V.; Wanke, C.A.; Ward, H.D. Intestinal microbiota, microbial translocation, and systemic inflammation in chronic HIV infection. J. Infect. Dis. 2015, 211, 19–27. [CrossRef]
Bernard, G.; Gagneul, D.; Alves Dos Santos, H.; Etienne, A.; Hilbert, J.L.; Rambaud, C. Efficient genome editing using CRISPR/Cas9 technology in chicory. Int. J. Mol. Sci. 2019, 20, 1155. [CrossRef]