896
Views
0
CrossRef citations to date
0
Altmetric
Research Paper

Using a human colonoid-derived monolayer to study bacteriophage translocation

, , , , , , , & ORCID Icon show all
Article: 2331520 | Received 21 Jan 2024, Accepted 13 Mar 2024, Published online: 22 Mar 2024

References

  • Turner D, Shkoporov AN, Lood C, Millard AD, Dutilh BE, Alfenas-Zerbini P, van Zyl LJ, Aziz RK, Oksanen HM, Poranen MM. et al. Abolishment of morphology-based taxa and change to binomial species names: 2022 taxonomy update of the ICTV bacterial viruses subcommittee. Arch Virol. 2023;168(2):74. doi:10.1007/s00705-022-05694-2.
  • Dion MB, Oechslin F, Moineau S. Phage diversity, genomics and phylogeny. Nat Rev Microbiol. 2020;18(3):125–18. doi:10.1038/s41579-019-0311-5.
  • Sausset R, Petit MA, Gaboriau-Routhiau V, De Paepe M. New insights into intestinal phages. Mucosal Immunol. 2020;13(2):205–215. doi:10.1038/s41385-019-0250-5.
  • Shkoporov AN, Hill C. Bacteriophages of the human gut: the “known unknown” of the microbiome. Cell Host Microbe. 2019;25(2):195–209. doi:10.1016/j.chom.2019.01.017.
  • Federici S, Nobs SP, Elinav E. Phages and their potential to modulate the microbiome and immunity. Cell Mol Immunol. 2021;18(4):889–904. doi:10.1038/s41423-020-00532-4.
  • O’Boyle CJ, MacFie J, Mitchell CJ, Johnstone D, Sagar PM, Sedman PC. Microbiology of bacterial translocation in humans. Gut. 1998;42(1):29–35. doi:10.1136/gut.42.1.29.
  • Sedman PC, Macfle J, Sagar P, Mitchell CJ, May J, Mancey-Jones B, Johnstone D. The prevalence of gut translocation in humans. Gastroenterology. 1994;107(3):643–649. doi:10.1016/0016-5085(94)90110-4.
  • Stehle JR Jr., Leng X, Kitzman DW, Nicklas BJ, Kritchevsky SB, High KP. Lipopolysaccharide-binding protein, a surrogate marker of microbial translocation, is associated with physical function in healthy older adults. J Gerontol A Biol Sci Med Sci. 2012;67(11):1212–1218. doi:10.1093/gerona/gls178.
  • Zhou X, Li J, Guo J, Geng B, Ji W, Zhao Q, Li J, Liu X, Liu J, Guo Z. et al. Gut-dependent microbial translocation induces inflammation and cardiovascular events after ST-elevation myocardial infarction. Microbiome. 2018;6(1):66. doi:10.1186/s40168-018-0441-4.
  • Górski A, Ważna E, DÄbrowska B-W, DÄbrowska K, Å?witaå?a-JeleÅ? K, Miä?dzybrodzki R. Bacteriophage translocation. FEMS Immunol Med Microbiol. 2006;46(3):313–319. doi:10.1111/j.1574-695X.2006.00044.x.
  • Brown-Jaque M, Muniesa M, Navarro FJSR. Bacteriophages in clinical samples can interfere with microbiological diagnostic tools. Sci Rep. 2016;6(1):1–8. doi:10.1038/srep33000.
  • Nguyen S, Baker K, Padman BS, Patwa R, Dunstan RA, Weston TA, Schlosser K, Bailey B, Lithgow T, Lazarou M. et al. Bacteriophage transcytosis provides a mechanism to cross epithelial cell layers. mBio. 2017;8(6):10–128. doi:10.1128/mBio.01874-17.
  • Bichet MC, Chin WH, Richards W, Lin Y-W, Avellaneda-Franco L, Hernandez CA, Oddo A, Chernyavskiy O, Hilsenstein V, Neild A. et al. Bacteriophage uptake by mammalian cell layers represents a potential sink that may impact phage therapy. iScience. 2021;24(4):102287. doi:10.1016/j.isci.2021.102287.
  • van Klinken BJ-W, Oussoren E, Weenink J-J, Strous GJ, Büller HA, Dekker J, Einerhand AWC. The human intestinal cell lines caco-2 and LS174T as models to study cell-type specific mucin expression. Glycoconj J. 1996;13(5):757–768. doi:10.1007/BF00702340.
  • Hartmann P, Seebauer CT, Schnabl B. Alcoholic liver disease: the gut microbiome and liver cross talk. Alcohol Clin Exp Res. 2015;39(5):763–775. doi:10.1111/acer.12704.
  • Linares R, Francés R, Gutiérrez A, Juanola O. Bacterial translocation as inflammatory Driver in Crohn’s disease. Front Cell Dev Biol. 2021;9:703310. doi:10.3389/fcell.2021.703310.
  • Almeida J, Galhenage S, Yu J, Kurtovic J, Riordan SM. Gut flora and bacterial translocation in chronic liver disease. World J Gastroenterol. 2006;12(10):1493–1502. doi:10.3748/wjg.v12.i10.1493.
  • Chen D, Le TH, Shahidipour H, Read SA, Ahlenstiel G. The role of gut-derived microbial antigens on liver fibrosis initiation and progression. Cells. 2019;8(11):1324. doi:10.3390/cells8111324.
  • Ahmad R, Sorrell MF, Batra SK, Dhawan P, Singh AB. Gut permeability and mucosal inflammation: bad, good or context dependent. Mucosal Immunol. 2017;10(2):307–317. doi:10.1038/mi.2016.128.
  • Paone P, Cani PD. Mucus barrier, mucins and gut microbiota: the expected slimy partners? Gut. 2020;69(12):2232–2243. doi:10.1136/gutjnl-2020-322260.
  • Schooley RT, Biswas B, Gill JJ, Hernandez-Morales A, Lancaster J, Lessor L, Barr JJ, Reed SL, Rohwer F, Benler S. et al. Development and use of personalized bacteriophage-based therapeutic cocktails to treat a patient with a disseminated resistant acinetobacter baumannii infection. Antimicrob Agents Chemother. 2017;61(10):e00954–00917. doi:10.1128/AAC.00954-17.
  • Jault P, Leclerc T, Jennes S, Pirnay JP, Que Y-A, Resch G, Rousseau AF, Ravat F, Carsin H, Le Floch R. et al. Efficacy and tolerability of a cocktail of bacteriophages to treat burn wounds infected by Pseudomonas aeruginosa (PhagoBurn): a randomised, controlled, double-blind phase 1/2 trial. Lancet Infect Dis. 2019;19(1):35–45. doi:10.1016/S1473-3099(18)30482-1.
  • Bruttin A, Brussow H. Human volunteers receiving Escherichia coli phage T4 orally: a safety test of phage therapy. Antimicrob Agents Chemother. 2005;49(7):2874–2878. doi:10.1128/AAC.49.7.2874-2878.2005.
  • Aslam S, Lampley E, Wooten D, Karris M, Benson C, Strathdee S, Schooley RT. Lessons learned from the first 10 consecutive cases of intravenous bacteriophage therapy to treat multidrug-resistant bacterial infections at a single center in the United States. Open Forum Infect Dis. 2020;7(9):ofaa389. doi:10.1093/ofid/ofaa389.
  • Sarker SA, Sultana S, Reuteler G, Moine D, Descombes P, Charton F, Bourdin G, McCallin S, Ngom-Bru C, Neville T. et al. Oral phage therapy of acute bacterial diarrhea with two coliphage preparations: a randomized trial in children from Bangladesh. EBioMedicine. 2016;4:124–137. doi:10.1016/j.ebiom.2015.12.023.
  • Dedrick RM, Smith BE, Cristinziano M, Freeman KG, Jacobs-Sera D, Belessis Y, Whitney Brown A, Cohen KA, Davidson RM, van Duin D. et al. Phage therapy of mycobacterium infections: compassionate use of phages in 20 patients with drug-resistant mycobacterial disease. Clin Infect Dis. 2022;76(1):103–112. doi:10.1093/cid/ciac453.
  • Petrovic Fabijan A, Lin RCY, Ho J, Maddocks S, Ben Zakour NL, Iredell JR, Khalid A, Venturini C, Chard R, Morales S. et al. Safety of bacteriophage therapy in severe staphylococcus aureus infection. Nat Microbiol. 2020;5(3):465–472. doi:10.1038/s41564-019-0634-z.
  • Monsur KA, Rahman MA, Huq F, Islam MN, Northrup RS, Hirschhorn N. Effect of massive doses of bacteriophage on excretion of vibrios, duration of diarrhoea and output of stools in acute cases of cholera. Bull World Health Organ 42, 723–732 (1970). 5
  • Van Belleghem JD, Clement F, Merabishvili M, Lavigne R, Vaneechoutte M. Pro- and anti-inflammatory responses of peripheral blood mononuclear cells induced by Staphylococcus aureus and Pseudomonas aeruginosa phages. Sci Rep. 2017;7(1):8004. doi:10.1038/s41598-017-08336-9.
  • Gogokhia L, Buhrke K, Bell R, Hoffman B, Brown DG, Hanke-Gogokhia C, Ajami NJ, Wong MC, Ghazaryan A, Valentine JF. et al. Expansion of bacteriophages is linked to aggravated intestinal inflammation and colitis. Cell Host Microbe. 2019;25(2):285–299.e8. doi:10.1016/j.chom.2019.01.008.
  • Sweere JM, Van Belleghem JD, Ishak H, Bach MS, Popescu M, Sunkari V, Kaber G, Manasherob R, Suh GA, Cao X. et al. Bacteriophage trigger antiviral immunity and prevent clearance of bacterial infection. Science. 2019;363(6434):eaat9691. doi:10.1126/science.aat9691.
  • Clokie M, Kropinski A. Bacteriophages methods and protocols, volume 1: isolation, characterization, and Interactions, (Humana Totowa, NJ). Methods Mol Biol. 2009;1:69–81. doi:10.1007/978-1-60327-164-6.
  • Venturini C, Ben Zakour NL, Bowring B, Morales S, Cole R, Kovach Z, Branston S, Kettle E, Thomson N, Iredell JR. et al. Fine capsule variation affects bacteriophage susceptibility in Klebsiella pneumoniae ST258. FASEB J. 2020;34(8):10801–10817. doi:10.1096/fj.201902735R.
  • Yu Q, Wang Z, Li P, Yang Q. The effect of various absorption enhancers on tight junction in the human intestinal caco-2 cell line. Drug Dev Ind Pharm. 2013;39(4):587–592. doi:10.3109/03639045.2012.692376.
  • Elamin E, Masclee A, Troost F, Pieters H-J, Keszthelyi D, Aleksa K, Dekker J, Jonkers D. Ethanol impairs intestinal barrier function in humans through mitogen activated protein kinase signaling: a combined in vivo and in vitro approach. PloS One. 2014;9(9):e107421. doi:10.1371/journal.pone.0107421.
  • Meroni M, Paolini E, Longo M, Piciotti R, Tria G, Fargion S, Fracanzani AL, Dongiovanni P. Recreating gut-liver axis during NAFLD onset by using a caco-2/HepG2 co-culture system. Metab Target Organ Damage. 2022;2(4):1–14. doi:10.20517/mtod.2021.19.
  • Xu P, Elamin E, Elizalde M, Bours PPHA, Pierik MJ, Masclee AAM, Jonkers DMAE. Modulation of intestinal epithelial permeability by plasma from patients with Crohn’s disease in a Three-dimensional Cell Culture Model. Sci Rep. 2019;9(1):2030. doi:10.1038/s41598-018-38322-8.
  • Al-Sadi RM, Ma TY. IL-1β causes an increase in intestinal epithelial tight junction permeability. J Immunol. 2007;178(7):4641–4649. doi:10.4049/jimmunol.178.7.4641.
  • Suzuki T, Yoshinaga N, Tanabe S. Interleukin-6 (IL-6) regulates claudin-2 expression and tight junction permeability in intestinal epithelium. J Biol Chem. 2011;286(36):31263–31271. doi:10.1074/jbc.M111.238147.
  • In JG, Foulke-Abel J, Clarke E, Kovbasnjuk O. Human colonoid monolayers to study interactions between pathogens, commensals, and Host intestinal epithelium. J Vis Exp. 2019;(146):e59357. doi:10.3791/59357-v.
  • Miyoshi H, Stappenbeck TS. In vitro expansion and genetic modification of gastrointestinal stem cells in spheroid culture. Nat Protoc. 2013;8(12):2471–2482. doi:10.1038/nprot.2013.153.
  • Sato T. et al. Long-term expansion of epithelial organoids from human colon, adenoma, adenocarcinoma, and Barrett’s epithelium. Gastroenterology. 2011;141:1762–1772. doi:10.1053/j.gastro.2011.07.050.
  • Co JY, Margalef-Català M, Li X, Mah AT, Kuo CJ, Monack DM, Amieva MR. Controlling epithelial polarity: a human enteroid Model for host-pathogen interactions. Cell Rep. 2019;26(9):2509–2520.e4. doi:10.1016/j.celrep.2019.01.108.
  • Almeida GMF, Laanto E, Ashrafi R, Sundberg L-R, Martiny JBH. Bacteriophage adherence to mucus mediates preventive protection against pathogenic bacteria. mBio. 2019;10(6):e01984–01919. doi:10.1128/mBio.01984-19.
  • Lourenco M, Chaffringeon L, Lamy-Besnier Q, Pédron T, Campagne P, Eberl C, Bérard M, Stecher B, Debarbieux L, De Sordi L. et al. The spatial heterogeneity of the gut limits predation and fosters coexistence of bacteria and bacteriophages. Cell Host Microbe. 2020;28(3):390–401.e5. doi:10.1016/j.chom.2020.06.002.
  • Sinnecker H, Ramaker K, Frey A. Coating with luminal gut-constituents alters adherence of nanoparticles to intestinal epithelial cells. Beilstein J Nanotechnol. 2014;5:2308–2315. doi:10.3762/bjnano.5.239.
  • Johansson MEV, Larsson JMH, Hansson GC. The two mucus layers of colon are organized by the MUC2 mucin, whereas the outer layer is a legislator of host–microbial interactions. Proc Natl Acad Sci USA. 2011;108(supplement_1):4659–4665. doi:10.1073/pnas.1006451107.
  • Navabi N, McGuckin MA, Lindén SK, Foligne B. Gastrointestinal cell lines form polarized epithelia with an Adherent Mucus Layer when cultured in semi-wet interfaces with mechanical stimulation. PloS One. 2013;8(7):e68761. doi:10.1371/journal.pone.0068761.
  • Keely S, Feighery, L., Campion, D P., O’Brien, L., Brayden, D J., Baird, A W. Chloride-led disruption of the intestinal mucous Layer impedes Salmonella invasion: evidence for an ‘Enteric Tear’ mechanism. Cell Physiol Biochem. 2011;28(4):743–752. doi:10.1159/000335768.
  • Wang X, Wang N, Yuan L, Li N, Wang J, Yang X. Exploring tight junction alteration using double fluorescent probe combination of lanthanide complex with gold nanoclusters. Sci Rep. 2016;6(1):32218. doi:10.1038/srep32218.
  • Bibbò S, Dore MP, Cammarota G. Response to: comment on “gut microbiota as a Driver of inflammation in nonalcoholic fatty liver disease”. Mediators Inflamm. 2018;2018:1–2. doi:10.1155/2018/7328057.
  • Sender R, Fuchs S, Milo R. Revised estimates for the Number of Human and Bacteria Cells in the body. PLoS Biol. 2016;14(8):e1002533. doi:10.1371/journal.pbio.1002533.
  • Gregory AC, Zablocki O, Howell A, Bolduc B, Sullivan MB. The human gut virome database. Cell host & microbe 2019;28(5):655910.
  • Mendes BG, Duan Y, Schnabl B. Immune response of an oral Enterococcus faecalis phage cocktail in a mouse model of ethanol-induced liver disease. Viruses. 2022;14(3):490. doi:10.3390/v14030490.
  • Dhungana G, Nepal R, Regmi M, Malla R. Pharmacokinetics and pharmacodynamics of a novel virulent klebsiella phage Kp_Pokalde_002 in a mouse Model. Front Cell Infect Microbiol. 2021;11:684704. doi:10.3389/fcimb.2021.684704.
  • Gorski A, Miedzybrodzki R, Jonczyk-Matysiak E, Kniotek M, Letkiewicz S. Therapeutic phages as modulators of the immune response: practical implications. Clin Infect Dis. 2023;77(Supplement_5):S433–S439. doi:10.1093/cid/ciad483.
  • Porayath C, Salim A, Palillam Veedu A, Babu P, Nair B, Madhavan A, Pal S. Characterization of the bacteriophages binding to human matrix molecules. Int J Biol Macromol. 2018;110:608–615. doi:10.1016/j.ijbiomac.2017.12.052.
  • Joeris T, Müller-Luda K, Agace WW, Mowat AM. Diversity and functions of intestinal mononuclear phagocytes. Mucosal Immunol. 2017;10(4):845–864. doi:10.1038/mi.2017.22.
  • Dosh RH, Jordan-Mahy N, Sammon C, Le Maitre CL. Long-term in vitro 3D hydrogel co-culture model of inflammatory bowel disease. Sci Rep. 2019;9(1):1812. doi:10.1038/s41598-019-38524-8.
  • Dean P, Quitard S, Bulmer DM, Roe AJ, Kenny B. Cultured enterocytes internalise bacteria across their basolateral surface for, pathogen-inhibitable, trafficking to the apical compartment. Sci Rep. 2015;5(1):17359. doi:10.1038/srep17359.
  • Pelaseyed T, Bergström JH, Gustafsson JK, Ermund A, Birchenough GMH, Schütte A, van der Post S, Svensson F, Rodríguez‐Piñeiro AM, Nyström EEL. et al. The mucus and mucins of the goblet cells and enterocytes provide the first defense line of the gastrointestinal tract and interact with the immune system. Immunol Rev. 2014;260(1):8–20. doi:10.1111/imr.12182.
  • Javitt G, Calvo MLG, Albert L, Reznik N, Ilani T, Diskin R, Fass D. Intestinal gel-forming mucins polymerize by disulfide-mediated dimerization of D3 domains. J Mol Biol. 2019;431(19):3740–3752. doi:10.1016/j.jmb.2019.07.018.
  • Atuma C, Strugala V, Allen A, Holm L. The adherent gastrointestinal mucus gel layer: thickness and physical state in vivo. Am J Physiol Gastrointest Liver Physiol. 2001;280(5):G922–G929. doi:10.1152/ajpgi.2001.280.5.G922.
  • Birchenough GM, Nystrom EE, Johansson ME, Hansson GC. A sentinel goblet cell guards the colonic crypt by triggering Nlrp6-dependent Muc2 secretion. Science. 2016;352(6293):1535–1542. doi:10.1126/science.aaf7419.
  • Yin H, Li J, Huang H, Wang Y, Qian X, Ren J, Xue F, Dai J, Tang F. Microencapsulated phages show prolonged stability in gastrointestinal environments and high therapeutic efficiency to treat Escherichia coli O157: H7 infection. Vet Res. 2021;52(1):118. doi:10.1186/s13567-021-00991-1.
  • Hartmann P, Chen P, Wang HJ, Wang L, McCole DF, Brandl K, Stärkel P, Belzer C, Hellerbrand C, Tsukamoto H. et al. Deficiency of intestinal mucin-2 ameliorates experimental alcoholic liver disease in mice. Hepatology. 2013;58(1):108–119. doi:10.1002/hep.26321.
  • Melis M, Tang XH, Mai K, Gudas LJ, Trasino SE. Fenretinide Reduces Intestinal Mucin-2-Positive Goblet Cells in Chronic Alcohol Abuse. Pharmacology. 2022;107(7–8):406–416. doi:10.1159/000524386.
  • Qin X, Deitch EA. Dissolution of lipids from mucus: a possible mechanism for prompt disruption of gut barrier function by alcohol. Toxicol Lett. 2015;232(2):356–362. doi:10.1016/j.toxlet.2014.11.027.
  • Benoit B, Bruno J, Kayal F, Estienne M, Debard C, Ducroc R, Plaisancié P. Saturated and unsaturated fatty acids differently modulate colonic goblet cells in vitro and in rat pups. J Nutr. 2015;145(8):1754–1762. doi:10.3945/jn.115.211441.
  • Filippello A, Di Mauro S, Scamporrino A, Torrisi SA, Leggio GM, Di Pino A, Scicali R, Di Marco M, Malaguarnera R, Purrello F. et al. Molecular effects of chronic exposure to Palmitate in intestinal organoids: a new Model to study obesity and diabetes. Int J Mol Sci. 2022;23(14):7751. doi:10.3390/ijms23147751.
  • Enss ML, Cornberg M, Wagner S, Gebert A, Henrichs M, Eisenblätter R, Beil W, Kownatzki R, Hedrich HJ. Proinflammatory cytokines trigger MUC gene expression and mucin release in the intestinal cancer cell line LS180. Inflamm Res. 2000;49(4):162–169. doi:10.1007/s000110050576.
  • Sun J, Shen X, Li Y, Guo Z, Zhu W, Zuo L, Zhao J, Gu L, Gong J, Li J. et al. Therapeutic potential to modify the mucus barrier in inflammatory bowel disease. Nutrients. 2016;8(1):44. doi:10.3390/nu8010044.
  • Nandhra GK, Chaichanavichkij P, Birch M, Scott SM. Gastrointestinal Transit Times in Health as determined using ingestible capsule systems: a systematic review. J Clin Med. 2023;12(16):5272. doi:10.3390/jcm12165272.
  • VanDussen KL, Marinshaw JM, Shaikh N, Miyoshi H, Moon C, Tarr PI, Ciorba MA, Stappenbeck TS. Development of an enhanced human gastrointestinal epithelial culture system to facilitate patient-based assays. Gut. 2015;64(6):911–920. doi:10.1136/gutjnl-2013-306651.