The interplay between radioresistant Caco-2 cells and the immune system increases epithelial layer permeability and alters signaling protein spectrum

Frontiers in Immunology

Volumn 8, Issue MAR, 2017, Pages

  Morini, Jacopo ^a   Babini, Gabriele ^a   Barbieri, Sofia ^a   Baiocco, Giorgio ^a   Ottolenghi, Andrea ^a  

^a UNIVERSITY OF PAVIA   (Italy)

Author keywords

Caco 2 cells; Cytokines; Ionizing radiation; Peripheral blood mononuclear cells; Trans epithelial electrical resistance

Indexed keywords

AFADIN; CLAUDIN 1; CXCL1 CHEMOKINE; EPITHELIAL DERIVED NEUTROPHIL ACTIVATING FACTOR 78; GAMMA INTERFERON; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 15; INTERLEUKIN 4; INTERLEUKIN 5; MONOCYTE CHEMOTACTIC PROTEIN 3; OCCLUDIN; PEPTIDES AND PROTEINS; PROTEIN ZO1; PROTEIN ZO2; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; X LINKED INHIBITOR OF APOPTOSIS;

ARTICLE; CACO-2 CELL LINE; CELL PROLIFERATION; CELL VIABILITY ASSAY; CONTROLLED STUDY; CYTOKINE RELEASE; ELECTRIC RESISTANCE; HUMAN; HUMAN CELL; IMMUNITY; MEMBRANE PERMEABILITY; RADIATION DOSE; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

EID: 85017267392     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2017.00223     Document Type: Article

References (39)

1. Cunningham D, Atkin W, Lenz HJ, Lynch HT, Minsky B, Nordlinger B, et al. Colorectal cancer. Lancet (2010) 375:1030-47. doi: 10.1016/S0140-6736(10)60353-4
2. Mancuso M, Pasquali E, Leonardi S, Tanori M, Rebessi S, Di Majo V, et al. Oncogenic bystander radiation effects in patched heterozygous mouse cerebellum. Proc Natl Acad Sci U S A (2008) 105:12445-50. doi:10.1073/pnas.0804186105
3. Demaria S, Formenti SC. Can abscopal effects of local radiotherapy be predicted by modeling T cell trafficking? J Immunother cancer (2016) 4:29. doi:10.1186/s40425-016-0133-1
4. Trott KR, Doerr W, Facoetti A, Hopewell J, Langendijk J, Van Luijk P, et al. Biological mechanisms of normal tissue damage: importance for the design of NTCP models. Radiother Oncol (2012) 105:79-85. doi:10.1016/j.radonc.2012.05.008
5. Deiró de Carvalho A, de Souza W, Morgado-Díaz J. Morphological and molecular alterations at the junctional complex in irradiated human colon adenocarcinoma cells, Caco-2. Int J Radiat Biol (2006) 82:658-68. doi:10.1080/09553000600930095
6. Chlenski A, Ketels KV, Korovaitseva GI, Talamonti MS, Oyasu R, Scarpelli DG. Organization and expression of the human ZO-2 gene (tjp-2) in normal and neoplastic tissues. Biochim Biophys Acta (2000) 1493:319-24. doi:10.1016/S0167-4781(00)00185-8
7. Hewitt KJ, Agarwal R, Morin PJ. The claudin gene family: expression in normal and neoplastic tissues. BMC Cancer (2006) 6:186. doi:10.1186/1471-2407-6-186
8. Oliveira SS, Morgado-Díaz JA. Claudins: multifunctional players in epithelial tight junctions and their role in cancer. Cell Mol Life Sci (2007) 64:17-28. doi:10.1007/s00018-006-6314-1
9. Krämer F, White K, Kubbies M, Swisshelm K, Weber BHF. Genomic organization of claudin-1 and its assessment in hereditary and sporadic breast cancer. Hum Genet (2000) 107:249-56. doi:10.1007/s004390000375
10. Tokés A-M, Kulka J, Paku S, Szik A, Páska C, Novák PK, et al. Claudin-1,-3 and-4 proteins and mRNA expression in benign and malignant breast lesions: a research study. Breast Cancer Res (2005) 7:R296-305. doi:10.1186/bcr983
11. Resnick M, Konkin T, Routhier J, Sabo E, Pricolo V. Claudin-1 is a strong prognostic indicator in stage II colonic cancer: a tissue microarray study. Mod Pathol (2005) 18:511-8. doi:10.1038/modpathol.3800301
12. Somosy Z, Bognar G, Horvath G, Koteles GJ. Role of nitric oxide, cAMP and cGMP in the radiation induced changes of tight junctions in Madin-Darby canine kidney cells. Cell Mol Biol (Noisy-le-grand) (2003) 49:59-63.
13. Moyes SM, Killick EM, Morris JF, Kadhim MA, Hill MA, Carr KE. Changes produced by external radiation in parameters influencing intestinal permeability and microparticle uptake in vitro. Int J Radiat Biol (2008) 84:467-86. doi:10.1080/09553000802078388
14. Sambuy Y, Angelis ID, Ranaldi G, Scarino ML, Stammati A, Zucco F. The Caco-2 cell line as a model of the intestinal barrier: influence of cell and culture-related factors on Caco-2 cell functional characteristics. Cell Biol Toxicol (2005) 21:1-26. doi:10.1007/s10565-005-0085-6
15. Babini G, Bellinzona VE, Morini J, Baiocco G, Mariotti L, Unger K, et al. Mechanisms of the induction of apoptosis mediated by radiation-induced cytokine release. Radiat Prot Dosimetry (2015) 166:165-9. doi:10.1093/rpd/ncv133
16. Pellegrina CD, Perbellini O, Scupoli MT, Tomelleri C, Zanetti C, Zoccatelli G, et al. Effects of wheat germ agglutinin on human gastrointestinal epithelium: insights from an experimental model of immune/epithelial cell interaction. Toxicol Appl Pharmacol (2009) 237:146-53. doi:10.1016/j.taap.2009.03.012
17. Pozo-Rubio T, Mujico JR, Marcos A, Puertollano E, Nadal I, Sanz Y, et al. Immunostimulatory effect of faecal Bifidobacterium species of breast-fed and formula-fed infants in a peripheral blood mononuclear cell/Caco-2 co-culture system. Br J Nutr (2011) 106:1216-23. doi:10.1017/S0007114511001656
18. Parlesak A, Haller D, Brinz S, Baeuerlein A, Bode C. Modulation of cytokine release by differentiated CACO-2 cells in a compartmentalized coculture model with mononuclear leucocytes and nonpathogenic bacteria. Scand J Immunol (2004) 60:477-85. doi:10.1111/j.0300-9475.2004.01495.x
19. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods (1983) 65:55-63. doi:10.1016/0022-1759(83)90303-4
20. Suetens A, Moreels M, Quintens R, Soors E, Buset J, Chiriotti S, et al. Dose-and time-dependent gene expression alterations in prostate and colon cancer cells after in vitro exposure to carbon ion and X-irradiation. J Radiat Res (2015) 56(1):11-21. doi:10.1093/jrr/rru070
21. Shin HK, Kim M-S, Jeong J-H. Combination effect of nimotuzumab with radiation in colorectal cancer cells. J Korean Soc Ther Radiol Oncol (2010) 28:147. doi:10.3857/jkstro.2010.28.3.147
22. Derer A, Deloch L, Rubner Y, Fietkau R, Frey B, Gaipl US. Radio-immunotherapy-induced immunogenic cancer cells as basis for induction of systemic anti-tumor immune responses-pre-clinical evidence and ongoing clinical applications. Front Immunol (2015) 6:505. doi:10.3389/fimmu.2015.00505
23. Frey B, Gaipl US. Radio-immunotherapy: the focused beam expands. Lancet Oncol (2015) 16:742-3. doi:10.1016/S1470-2045(15)00055-8
24. Prise KM, O'Sullivan JM. Radiation-induced bystander signalling in cancer therapy. Nat Rev Cancer (2009) 9:351-60. doi:10.1038/nrc2603
25. Guertler A, Kraemer A, Roessler U, Hornhardt S, Kulka U, Moertl S, et al. The WST survival assay: an easy and reliable method to screen radiation-sensitive individuals. Radiat Prot Dosimetry (2010) 143:487-90. doi:10.1093/rpd/ncq515
26. Pellegrini P, Berghella AM, Del Beato T, Cicia S, Adorno D, Casciani CU. Disregulation in TH1 and TH2 subsets of CD4+ T cells in peripheral blood of colorectal cancer patients and involvement in cancer establishment and progression. Cancer Immunol Immunother (1996) 42:1-8. doi:10.1007/s002620050244
27. Durai R, Yang SY, Seifalian AM, Goldspink G, Winslet MC. Role of insulin-like growth factor binding protein-4 in prevention of colon cancer. World J Surg Oncol (2007) 5:128. doi:10.1186/1477-7819-5-128
28. Cohn L, Elias JA, Chupp GLA. Asthma: mechanisms of disease persistence and progression. Annu Rev Immunol (2004) 22:789-815. doi:10.1146/annurev.immunol.22.012703.104716
29. Ahdieh M, Vandenbos T, Youakim A. Lung epithelial barrier function and wound healing are decreased by IL-4 and IL-13 and enhanced by IFN-gamma. Am J Physiol Cell Physiol (2001) 281:C2029-38.
30. Ma TY, Iwamoto GK, Hoa NT, Akotia V, Pedram A, Boivin MA, et al. TNF-alpha-induced increase in intestinal epithelial tight junction permeability requires NF-kappa B activation. Am J Physiol Gastrointest Liver Physiol (2004) 286:G367-76. doi:10.1152/ajpgi.00173.2003
31. Nava P, Koch S, Laukoetter MG, Lee WY, Kolegraff K, Capaldo CT, et al. Interferon-γ regulates intestinal epithelial homeostasis through converging β-catenin signaling pathways. Immunity (2010) 32:392-402. doi:10.1016/j.immuni.2010.03.001
32. Kaiser GC, Polk DB. Tumor necrosis factor alpha regulates proliferation in a mouse intestinal cell line. Gastroenterology (1997) 112:1231-40. doi:10.1016/S0016-5085(97)70135-5
33. Ruemmele F, Gurbindo C, Mansour A, Marchand R, Levy E, Seidman E. Effects of interferon ? on growth, apoptosis, and MHC class II expression of immature rat intestinal crypt (IEC-6) cells. J Cell Physiol (1998) 126:120-6. doi:10.1002/(SICI)1097-4652(199807)176:1<120::AID-JCP14>3.0.CO;2-B
34. Youakim A, Ahdieh M. Interferon-gamma decreases barrier function in T84 cells by reducing ZO-1 levels and disrupting apical actin. Am J Physiol (1999) 276:G1279-88.
35. Oeckinghaus A, Hayden MS, Ghosh S. Crosstalk in NF-κB signaling pathways. Nat Immunol (2011) 12:695-708. doi:10.1038/ni.2065
36. Babini G, Morini J, Baiocco G, Mariotti L, Ottolenghi A. In vitro gamma-ray-induced inflammatory response is dominated by culturing conditions rather than radiation exposures. Sci Rep (2015) 5:9343. doi:10.1038/srep09343
37. Gu L, Zhu N, Zhang H, Durden DL, Feng Y, Zhou M. Regulation of XIAP translation and induction by MDM2 following irradiation. Cancer Cell (2009) 15:363-75. doi:10.1016/j.ccr.2009.03.002
38. Bai L, Smith DC, Wang S. Small-molecule SMAC mimetics as new cancer therapeutics. Pharmacol Ther (2014) 144:82-95. doi:10.1016/j.pharmthera.2014.05.007
39. Paulsen M, Ussat S, Jakob M, Scherer G, Lepenies I, Schütze S, et al. Interaction with XIAP prevents full caspase-3/-7 activation in proliferating human T lymphocytes. Eur J Immunol (2008) 38:1979-87. doi:10.1002/eji.200838211