Optimization of murine small intestine leukocyte isolation for global immune phenotype analysis

Journal of Immunological Methods

Volumn 405, Issue , 2014, Pages 97-108

  Goodyear, Andrew W ^a   Kumar, Ajay ^a   Dow, Steven ^a   Ryan, Elizabeth P ^a  

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

Author keywords

Collagenase digestion; Flow cytometry; Global analysis; Isolation; Small intestine

Indexed keywords

CD11B ANTIGEN; CD3 ANTIGEN; CD45 ANTIGEN; CD5 ANTIGEN; CD8ALPHA ANTIGEN; CELL SURFACE MARKER; COLLAGENASE; DISPASE; GLYCOPROTEIN P 15095; REAGENT; SYNDECAN 1; T LYMPHOCYTE RECEPTOR; THERMOLYSIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL ASSAY; CELL ISOLATION; CELL POPULATION; CELL SURFACE; CELL VIABILITY; COST BENEFIT ANALYSIS; CULTURE MEDIUM; CULTURE OPTIMIZATION; ENZYME DEGRADATION; EPITHELIUM CELL; FEMALE; IMMUNOPHENOTYPING; INCUBATION TEMPERATURE; INCUBATION TIME; INTERDIGITATING CELL; INTESTINE CELL; LEUKOCYTE; MALE; MONOCYTE; MOUSE; NATURAL KILLER CELL; NONHUMAN; ORGAN WEIGHT; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; REPRODUCIBILITY; SMALL INTESTINE;

MURINAE; MUS;

COLLAGENASE DIGESTION; FLOW CYTOMETRY; GLOBAL ANALYSIS; ISOLATION; SMALL INTESTINE;

ANIMALS; ANTIGENS, CD; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL SEPARATION; CELL SURVIVAL; DENDRITIC CELLS; EPITHELIAL CELLS; FEMALE; IMMUNOPHENOTYPING; INTESTINAL MUCOSA; INTESTINE, SMALL; KILLER CELLS, NATURAL; LEUKOCYTES; MALE; MICE; MICE, 129 STRAIN; MICE, INBRED BALB C; MICE, INBRED ICR; MONOCYTES; REPRODUCIBILITY OF RESULTS;

EID: 84897419613     PISSN: 00221759     EISSN: 18727905     Source Type: Journal    
DOI: 10.1016/j.jim.2014.01.014     Document Type: Article

References (44)

1. Axis S. Isolation of Mouse Dendritic Cells from Tissues by a Mixer Technique (C21) 2013, (http://www.axis-shield-density-gradient-media.com/C21.pdf).
2. Bull D.M., Bookman M.A. Isolation and functional characterization of human intestinal mucosal lymphoid cells. J. Clin. Invest. 1977, 59:966-974.
3. Castro G.A., Roy S.A., Stockstill R.D. Trichinella spiralis: peroxidase activity in isolated cells from the rat intestine. Exp. Parasitol. 1974, 36:307-315.
4. Cebra J.J., Gearhart P.J., Kamat R., Robertson S.M., Tseng J. The secretory immunoglobulin a response in the gut. Biochem. Soc. Trans. 1977, 5:1565-1569.
5. Crofton R.W., Cochrane C., McClelland D.B. Preparation of lymphoid cells from small specimens of human gastrointestinal mucosa. Gut 1978, 19:898-906.
6. Davies M.D., Parrott D.M. Preparation and purification of lymphocytes from the epithelium and lamina propria of murine small intestine. Gut 1981, 22:481-488.
7. De Geus B., Van den Enden M., Coolen C., Nagelkerken L., Van der Heijden P., Rozing J. Phenotype of intraepithelial lymphocytes in euthymic and athymic mice: implications for differentiation of cells bearing a CD3-associated γδ T cell receptor. Eur. J. Immunol. 1990, 20:291-298.
8. Dillon S.B., MacDonald T.T. Isolation and function of mucosal lymphocytes in the mouse. Prog. Clin. Biol. Res. 1985, 181:381-385.
9. Ericsson A., Agace W. CCL25 enhances CD103-mediated lymphocyte adhesion to E-cadherin. Ann. N. Y. Acad. Sci. 2004, 1029:334-336.
10. + dendritic cells into the intestinal epithelium to sample bacterial antigens for presentation. Immunity 2013, 38:581-595.
11. Foureau D.M., Mielcarz D.W., Menard L.C., Schulthess J., Werts C., Vasseur V., Ryffel B., Kasper L.H., Buzoni-Gatel D. TLR9-dependent induction of intestinal α-defensins by Toxoplasma gondii. J. Immunol. 2010, 184:7022-7029.
12. + dendritic cells in the small intestine expresses TLR3, TLR7, and TLR9 and induces Th1 response and CTL activity. J. Immunol. 2011, 186:6287-6295.
13. Gautreaux M.D., Deitch E.A., Berg R.D. T lymphocytes in host defense against bacterial translocation from the gastrointestinal tract. Infect. Immun. 1994, 62:2874-2884.
14. Geem D., Medina-Contreras O., Kim W., Huang C.S., Denning T.L. Isolation and characterization of dendritic cells and macrophages from the mouse intestine. J. Vis. Exp. 2012, e4040.
15. Goodyear A., Jones A., Troyer R., Bielefeldt-Ohmann H., Dow S. Critical protective role for MCP-1 in Pneumonic Burkholderia mallei infection. J. Immunol. 2010, 184:1445-1454.
16. Goodyear A., Strange L., Rholl D.A., Silisouk J., Dance D.A., Schweizer H.P., Dow S. An improved selective culture medium enhances the isolation of Burkholderia pseudomallei from contaminated specimens. Am. J. Trop. Med. Hyg. 2013, 89:973-982.
17. Griffith M.E., Bodily H.L. Stability of antimycobacterial drugs in susceptibility testing. Antimicrob. Agents Chemother. 1992, 36:2398-2402.
18. Henderson A.J., Kumar A., Barnett B., Dow S.W., Ryan E.P. Consumption of rice bran increases mucosal immunoglobulin A concentrations and numbers of intestinal Lactobacillus spp. J. Med. Food 2012, 15:469-475.
19. Hook C.W., Brown S.I., Iwanij W., Nakanishi I. Characterization and inhibition of corneal collagenase. Invest. Ophthalmol. 1971, 10:496-503.
20. Hooper L.V., Littman D.R., Macpherson A.J. Interactions between the microbiota and the immune system. Science 2012, 336:1268-1273.
21. + dendritic cells in the regulation of tissue-selective T cell homing. J. Exp. Med. 2005, 202:1063-1073.
22. Kearsey J.A., Stadnyk A.W. Isolation and characterization of highly purified rat intestinal intraepithelial lymphocytes. J. Immunol. Methods 1996, 194:35-48.
23. Kumar A., Henderson A., Forster G.M., Goodyear A.W., Weir T.L., Leach J.E., Dow S.W., Ryan E.P. Dietary rice bran promotes resistance to Salmonella enterica serovar typhimurium colonization in mice. BMC Microbiol. 2012, 12:71.
24. Lee J.S., Oka K., Obara M., Nishimukai M., Yoo Y.C., Yamada K., Tsukahara T., Nakayama K., Hara H., Ishizuka S. Improved isolation methods for mucosal leukocytes from small and large intestines in rats. Biosci. Biotechnol. Biochem. 2009, 73:1732-1740.
25. Leventon G.S., Kulkarni S.S., Meistrich M.L., Newland J.R., Zander A.R. Isolation of murine small bowel intraepithelial lymphocytes. J. Immunol. Methods 1983, 63:35-44.
26. Lycke N. A sensitive method for the detection of specific antibody production in different isotypes from single lamina propria plasma cells. Scand. J. Immunol. 1986, 24:393-403.
27. Lyscom N., Brueton M.J. Intraepithelial, lamina propria and peyer's patch lymphocytes of the rat small intestine: isolation and characterization in terms of immunoglobulin markers and receptors for monoclonal antibodies. Immunology 1982, 45:775-783.
28. McShane P., Sutton R., Gray D.W., Morris P.J. Protease activity in pancreatic islet isolation by enzymatic digestion. Diabetes 1989, 38(Suppl. 1):126-128.
29. Nealon D.A., Henderson A.R. Stability of commonly used thiols and of human creatine kinase isoenzymes during storage at various temperature in various media. Clin. Chem. 1977, 23:816-829.
30. Okerman L., Van Hende J., De Zutter L. Stability of frozen stock solutions of β-lactam antibiotics, cephalosporins, tetracyclines and quinolones used in antibiotic residue screening and antibiotic susceptibility testing. Anal. Chim. Acta. 2007, 586:284-288.
31. Resendiz-Albor A.A., Esquivel R., Lopez-Revilla R., Verdin L., Moreno-Fierros L. Striking phenotypic and functional differences in lamina propria lymphocytes from the large and small intestine of mice. Life Sci. 2005, 76:2783-2803.
32. Roche Liberase Research Grade Purified Enzyme Blends 2013, vol. 6. (https://cssportal.roche.com/LFR_PublicDocs/ras/05401119001_en_06.pdf).
33. Ruiz V.E., Sachdev M., Zhang S., Wen S., Moss S.F. Isolating, immunophenotyping and ex vivo stimulation of CD4+ and CD8+ gastric lymphocytes during murine Helicobacter pylori infection. J. Immunol. Methods 2012, 384:157-163.
34. Salazar-Gonzalez R.M., Niess J.H., Zammit D.J., Ravindran R., Srinivasan A., Maxwell J.R., Stoklasek T., Yadav R., Williams I.R., Gu X., McCormick B.A., Pazos M.A., Vella A.T., Lefrancois L., Reinecker H.C., McSorley S.J. CCR6-mediated dendritic cell activation of pathogen-specific T cells in Peyer's patches. Immunity 2006, 24:623-632.
35. Sheridan B.S., Lefrancois L. Isolation of mouse lymphocytes from small intestine tissues. Curr. Protoc. Immunol. 2012, 99:3.19.1-3.19.11.
36. Sigma-Aldrich General Information about Sigma-Aldrich Collagenase Products 2013, vol. 2013. (http://www.sigmaaldrich.com/life-science/metabolomics/enzyme-explorer/l earning-center/collagenase-guide.html).
37. Suzuki H. Age-dependent changes in intraepithelial lymphocytes (IELs) of the small intestine, cecum, and colon from young adult to aged mice. Arch. Gerontol. Geriatr. 2012, 55:261-270.
38. Tagliabue A., Befus A.D., Clark D.A., Bienenstock J. Characteristics of natural killer cells in the murine intestinal epithelium and lamina propria. J. Exp. Med. 1982, 155:1785-1796.
39. Tseng J. Expression of immunoglobulin isotypes by lymphoid cells of mouse intestinal lamina propria. Cell. Immunol. 1982, 73:324-336.
40. Van der Heijden P.J., Stok W. Improved procedure for the isolation of functionally active lymphoid cells from the murine intestine. J. Immunol. Methods 1987, 103:161-167.
41. Veldhoen M., Brucklacher-Waldert V. Dietary influences on intestinal immunity. Nat. Rev. Immunol. 2012, 12:696-708.
42. Waidmann M., Allemand Y., Lehmann J., di Genaro S., Bucheler N., Hamann A., Autenrieth I.B. Microflora reactive IL-10 producing regulatory T cells are present in the colon of IL-2 deficient mice but lack efficacious inhibition of IFN-γ and TNF-α production. Gut 2002, 50:170-179.
43. Weigmann B., Tubbe I., Seidel D., Nicolaev A., Becker C., Neurath M.F. Isolation and subsequent analysis of murine lamina propria mononuclear cells from colonic tissue. Nat. Protoc. 2007, 2:2307-2311.
44. Ye Y., Yue M., Jin X., Chen S., Li Y. Isolation of murine small intestinal intraepithelial γδ T cells. Immunol. Invest. 2010, 39:661-673.