An organotypic slice model for ex vivo study of neural, immune, and microbial interactions of mouse intestine

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 310, Issue 4, 2016, Pages G240-G248

  Schwerdtfeger, Luke A ^a   Ryan, Elizabeth P ^a   Tobet, Stuart A ^a,b  

^a Department of Environmental and Radiological Health Sciences   (United States)

^b Engineering Research Center and Hydraulics Laboratory   (United States)

Author keywords

Contraction; Enteric; Gut; Microbiome; Neuroimmune

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DEATH; CELL PROLIFERATION; COLON; COMMENSAL; CONTROLLED STUDY; EX VIVO STUDY; FEMALE; ILEUM; IMMUNOCOMPETENCE; IMMUNOREACTIVITY; INTERSTITIAL CELL OF CAJAL; INTESTINAL TISSUE; INTESTINE CELL; INTESTINE FLORA; INTESTINE MOTILITY; JEJUNUM; MALE; MICROBIOME; MICROENVIRONMENT; MICROVILLUS; MOUSE; NONHUMAN; ORGANISMAL INTERACTION; PEYER PATCH; PRIORITY JOURNAL; SMALL INTESTINE; SMOOTH MUSCLE CONTRACTION; TIME-LAPSE VIDEO MICROSCOPY; TISSUE SLICE; ANIMAL; BIOLOGICAL MODEL; C57BL MOUSE; DRUG EFFECTS; IMMUNOLOGY; INNERVATION; INTESTINE; INTESTINE MUCOSA; MICROBIOLOGY; MICROFLORA; MUSCLE CONTRACTION; ORGAN CULTURE TECHNIQUE; PHYSIOLOGY; SMOOTH MUSCLE; ULTRASTRUCTURE;

ANTIINFECTIVE AGENT; CALCIUM CHANNEL BLOCKING AGENT; NICARDIPINE;

ANIMALS; ANTI-BACTERIAL AGENTS; CALCIUM CHANNEL BLOCKERS; CELL PROLIFERATION; ENTEROCYTES; FEMALE; INTESTINAL MUCOSA; INTESTINES; MALE; MICE; MICE, INBRED C57BL; MICROBIOTA; MODELS, BIOLOGICAL; MUSCLE CONTRACTION; MUSCLE, SMOOTH; NICARDIPINE; ORGAN CULTURE TECHNIQUES; PEYER'S PATCHES;

EID: 84958534361     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00299.2015     Document Type: Article

References (40)

1. Asano M, Yamamoto T, Tsuruta T, Nishimura N, Sonoyama K. Dual labeling with 5-bromo-2=-deoxyuridine and 5-ethynyl-2=-deoxyuridine for estimation of cell migration rate in the small intestinal epithelium. Dev Growth Differ 57: 68–73, 2015.
2. Carlone DL, Breault DT. Tales from the crypt: the expanding role of slow cycling intestinal stem cells. Cell Stem Cell 10: 2–4, 2012.
3. Cheng H, Bjerknes M. Cell production in mouse intestinal epithelium measured by stathmokinetic flow cytometry and Coulter particle counting. Anat Rec 207: 427–434, 1983.
4. Davis AM, Seney ML, Walker HJ, Tobet SA. Differential colocalization of Islet-1 and estrogen receptor alpha in the murine preoptic area and hypothalamus during development. Endocrinology 145: 360–366, 2004.
5. de Almada CN, Martinez RC, Sant’ana AS. Characterization of the intestinal microbiota and its interaction with probiotics and health impacts. Appl Microbiol Biotechnol 99: 4175–4199, 2015.
6. de Graaf IA, Olinga P, de Jager MH, Merema MT, de Kanter R, Van de Kerkhof EG, Groothuis GM. Preparation and incubation of precisioncut liver and intestinal slices for application in drug metabolism and toxicity studies. Nat Protoc 5: 1540–1551, 2010.
7. de Kanter R, Tuin A, van de Kerkhof E, Martignoni M, Draaisma AL, Jager MH, de Graaf IA, Meijer DKF, Groothuis GM. A new technique for preparing precision-cut slices from small intestine and colon for drug biotransformation studies. J Pharmacol Toxicol Methods 51: 65–72, 2005.
8. De Filippis D, Esposito G, Cirillo C, Cipriano M, De Winter BY, Scuderi C, Sarnelli G, Cuomo R, Steardo L, De Man JG, Luvone T. Cannabidiol reduces intestinal inflammation through the control of neuroimmune axis. PLoS One 6: e28159, 2011.
9. Fan YY, Davidson LA, Callaway ES, Wright GA, Safe S, Chapkin RS. A bioassay to measure energy metabolism in mouse colonic crypts, organoids and sorted stem cells. Am J Physiol Gastrointest Liver Physiol 309: G1–G9, 2015.
10. Feng G, Mellor RH, Bernstein M, Keller-Peck C, Nguyen QT, Nerbonne JM, Lichtman JW, Sanes JR. Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 28: 41–51, 2000.
11. Forsythe P, Kunze WA. Voices from within; gut microbes and the CNS. Cell Mol Life Sci 2013: 55–69, 2013.
12. Frahm KA, Clay CM, Tobet SA. Characterization of an ovarian slice model in vitro to view ovulation (Abstract). Biol Reprod 83: 66, 2010.
13. Frahm KA, Tobet SA. Development of the blood-brain barrier within the paraventricular nucleus of the hypothalamus: influence of fetal glucocorticoid excess. Brain Struct Funct 220: 2225–2234, 2014.
14. Furness JB. The Enteric Nervous System. Malden, MA: Blackwell, 2006.
15. Furness JB, Costa M. The Enteric Nervous System. Edinburgh: Churchill Livingstone, 1987.
16. Gracz AD, Magness ST. Defining hierarchies of stemness in the intestine: evidence from biomarkers and regulatory pathways. Am J Physiol Gastrointest Liver Physiol 307: G260–G273, 2014.
17. Grasa L, Abecia L, Forcén R, Castro M, de Jalón JA, Latorre E, Alcalde AI, Murillo MD. Antibiotic-induced depletion of murine microbiota induces mild inflammation and changes in toll-like receptor patterns and intestinal motility. Microb Ecol 70: 835–848, 2015.
18. Groothuis GM, de Graff IA. Precision-cut intestinal slices as in vitro tool for studies on drug metabolism. Curr Drug Metab 14: 112–119, 2013.
19. He G, Shankar RA, Chzhan M, Samouilov A, Kuppusamy P, Zweier JL. Noninvasive measurement of anatomic structure and intraluminal oxygenation in the gastrointestinal tract of living mice with spatial and spectral EPR imaging. Proc Natl Acad Sci USA 96: 4586–4591, 1999.
20. Hennig GW, Spencer NJ, Jokela-Willis S, Bayguinov PO, Lee HT, Ritchie LA, Ward SM, Smith TK, Sanders KM. ICC-MY coordinate smooth muscle electrical and mechanical activity in the murine small intestine. Neurogastroenterol Motil 22: e138–e151, 2010.
21. Huizinga JD, Chen JH, Zhu YF, Pawelka A, McGinn RJ, Bardakjian BL, Parsons SP, Kunze WA, Wu RY, Berik P, Khoshdel A, Chen S, Yin S, Zhang Q, Yu Y, Gao Q, Li K, Hu X, Zarate N, Collins P, Pistilli M, Ma J, Zhang R, Chen D. The origin of segmentation motor activity in the intestine. Nat Commun 5: 3326, 2014.
22. Jung C, Hugot JP, Barreau F. Peyer’s patches: the immune sensors of the intestine. Int J Inflam 2010: 823710, 2010.
23. Kabouridis PS, Lasrado R, McCallum S, Chng SH, Snippert HJ, Clevers H, Pettersson S, Pachnis V. Microbiota controls the homeostasis of glial cells in the gut lamina propria. Neuron 85: 289–295, 2015.
24. Kim HJ, Ingber DE. Gut-on-a-Chip microenvironment induces human intestinal cells to undergo villus differentiation. Integr Biol (Camb) 5: 1130–1140, 2013.
25. Knoll JG, Wolfe CA, Tobet SA. Estrogen modulates neuronal movements within the developing preoptic area-anterior hypothalamus. Eur J Neurosci 26: 1091–1099, 2007.
26. Khoshdel A, Verdu EF, Kunze W, McLean P, Bergonzelli G, Huizinga JD. Bifidobacterium longum NCC3001 inhibits AH neuron excitability. Neurogastroenterol Motil 25: e478–e484, 2013.
27. Li C, Liu B, Tong W, Zhang L, Jiang Y. Dissociation, culture and morphologic changes of interstitial cells of Cajal in vitro. World J Gastroenterol 11: 2838–2840, 2005.
28. Muller PA, Koscsó B, Rajani GM, Stevanovic K, Berres ML, Hashimoto D, Mortha A, Leboeuf M, Li XM, Mucida D, Stanley ER, Dahan S, Margolis KG, Gershon MD, Merad M, Bogunovic M. Crosstalk between muscularis macrophages and enteric neurons regulates gastrointestinal motility. Cell 158: 300–313, 2014.
29. Navratil AM, Knoll JG, Whitesell JD, Tobet SA, Clay CM. Neuroendocrine plasticity in the anterior pituitary: gonadotropin-releasing hormone- mediated movement in vitro and in vivo. Endocrinology 148: 1736–1744, 2007.
30. Punyadarsaniya D, Winter C, Mork AK, Amiri M, Naim HY, Rautenschlein S, Herrler G. Precision-cut intestinal slices as a culture system to analyze the infection of differentiated intestinal epithelial cells by avian influenza viruses. J Virol Methods 212: 71–75, 2015.
31. Sanders KM, Ward SM, Koh SD. Interstitial cells: regulators of smooth muscle function. Physiol Rev 94: 859–907, 2014.
32. Sang Q, Young HM. Chemical coding of neurons in the myenteric plexus and external muscle of the small and large intestine of the mouse. Cell Tissue Res 284: 39–53, 1996.
33. Takaki M. Gut pacemaker cells: the interstitial cells of Cajal (ICC). J Smooth Muscle Res 39: 137–161, 2003.
34. Tobet SA, Walker HJ, Seney ML, Yu KW. Viewing cell movements in the developing neuroendocrine brain. Integr Comp Biol 43: 794–801, 2003.
35. Van Midwoud PM, Merema MT, Verpoorte E, Groothuis GM. A microfluidic approach for in vitro assessment of interorgan interactions in drug metabolism using intestinal and liver slices. Lab Chip 10: 2778–2786, 2010.
36. Van Nassauw L, Wu M, de Jonge F, Adriaensen D, Timmermans JP. Cytoplasmic, but not nuclear, expression of the neuronal nuclei (NeuN) antibody is an exclusive feature of Dogiel type II neurons in the guinea-pig gastrointestinal tract. Histochem Cell Biol 124: 369–377, 2005.
37. Vidal M, Morris R, Grosveld F, Spanopoulou E. Tissue-specific control elements of the Thy-1 gene. EMBO J 9: 833–840, 1990.
38. Weiland GA, Oswald RE. The mechanism of binding of dihydropyridine calcium channel blockers to rat brain membranes. J Biol Chem 260: 8456–8464, 1984.
39. Williams K, Koyama T, Schulz D, Kaluza GL, Pautler RG, Weisbrodt N, Conner ME. Use of fluoroscopy to study in vivo motility in mouse pups. J Pediatr Gastroenterol Nutr 52: 679–685, 2011.
40. 2+ conductance in interstitial cells of Cajal of the murine small intestine. Am J Physiol Cell Physiol 306: C705–C713, 2014.