Activation of p38-MAPK by CXCL4/CXCR3 axis contributes to p53-dependent intestinal apoptosis initiated by 5-fluorouracil

Cancer Biology and Therapy

Volumn 15, Issue 8, 2014, Pages 982-991

  Gao, Jing ^a   Gao, Jin ^a   Qian, Lan ^a   Wang, Xia ^a   Wu, Mingyuan ^a   Zhang, Yang ^a   Ye, Hao ^a   Zhu, Shunying ^a   Yu, Yan ^a   Han, Wei ^a  

^a SHANGHAI JIAO TONG UNIVERSITY   (China)

Author keywords

Apoptosis; Chemotherapy; CXCL4; Intestinal mucositis; p38; p53

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; CASPASE 3; CASPASE 8; CASPASE 9; CHEMOKINE RECEPTOR CXCR3; FLUOROURACIL; MITOGEN ACTIVATED PROTEIN KINASE P38; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY CXCL4; PROTEIN BAX; PROTEIN P53; UNCLASSIFIED DRUG; ALPHA CHEMOKINE; ANTINEOPLASTIC ANTIMETABOLITE; CASPASE; CXCL3 PROTEIN, MOUSE; NEUTRALIZING ANTIBODY; THROMBOCYTE FACTOR 4;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DIARRHEA; DISEASE SEVERITY; DOWN REGULATION; MALE; MOUSE; MUCOSA INFLAMMATION; NONHUMAN; PATHOGENESIS; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SINGLE DRUG DOSE; TISSUE REGENERATION; UPREGULATION; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; CHEMICALLY INDUCED; DRUG EFFECTS; ENZYME ACTIVATION; EPITHELIUM CELL; GENETIC TRANSCRIPTION; INTESTINE MUCOSA; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; RAT;

ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIMETABOLITES, ANTINEOPLASTIC; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; CASPASES; CHEMOKINES, CXC; DIARRHEA; ENZYME ACTIVATION; EPITHELIAL CELLS; FLUOROURACIL; INTESTINAL MUCOSA; MALE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; MUCOSITIS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PLATELET FACTOR 4; RATS; TRANSCRIPTION, GENETIC; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84905453824     PISSN: 15384047     EISSN: 15558576     Source Type: Journal    
DOI: 10.4161/cbt.29114     Document Type: Article

References (37)

1. Daniele B, Secondulfo M, De Vivo R, Pignata S, De Magistris L, Delrio P, Palaia R, Barletta E, Tambaro R, Carratù R. Effect of chemotherapy with 5-fluorouracil on intestinal permeability and absorption in patients with advanced colorectal cancer. J Clin Gastroenterol 2001; 32:228-30; http://dx.doi.org/10.1097/00004836-200103000-00010; PMID:11246350
2. Duncan M, Grant G. Oral and intestinal mucositis - causes and possible treatments. Aliment Pharmacol Ther 2003; 18:853-74; PMID:14616150; http://dx.doi.org/10.1046/j.1365-2036.2003.01784.x
3. Bowen JM, Gibson RJ, Cummins AG, Keefe DM. Intestinal mucositis: the role of the Bcl-2 family, p53 and caspases in chemotherapy-induced damage. Support Care Cancer 2006; 14:713-31; http://dx.doi.org/10.1007/s00520-005-0004-7; PMID:16453135
4. Anilkumar TV, Sarraf CE, Hunt T, Alison MR. The nature of cytotoxic drug-induced cell death in murine intestinal crypts. Br J Cancer 1992; 65:552-8; PMID:1562464; http://dx.doi.org/10.1038/bjc.1992.113
5. Pritchard DM, Potten CS, Hickman JA. The relationships between p53-dependent apoptosis, inhibition of proliferation, and 5-fluorouracil-induced histopathology in murine intestinal epithelia. Cancer Res 1998; 58:5453-65; PMID:9850079
6. Keefe DM, Brealey J, Goland GJ, Cummins AG. Chemotherapy for cancer causes apoptosis that precedes hypoplasia in crypts of the small intestine in humans. Gut 2000; 47:632-7; PMID:11034578; http://dx.doi.org/10.1136/gut.47.5. 632
7. Inomata A, Horii I, Suzuki K. 5-Fluorouracil-induced intestinal toxicity: what determines the severity of damage to murine intestinal crypt epithelia? Toxicol Lett 2002; 133:231-40; PMID:12119131; http://dx.doi.org/10.1016/S0378- 4274(02)00204-7
8. Kasper B, Petersen F. Molecular pathways of platelet factor 4/CXCL4 signaling. Eur J Cell Biol 2011; 90:521-6; http://dx.doi.org/10.1016/j.ejcb. 2010.12.002; PMID:21295372
9. Han ZC, Lu M, Li J, Defard M, Boval B, Schlegel N, Caen JP. Platelet factor 4 and other CXC chemokines support the survival of normal hematopoietic cells and reduce the chemosensitivity of cells to cytotoxic agents. Blood 1997; 89:2328-35; PMID:9116276
10. Watson JB, Getzler SB, Mosher DF. Platelet factor 4 modulates the mitogenic activity of basic fibroblast growth factor. J Clin Invest 1994; 94:261-8; http://dx.doi.org/10.1172/JCI117316; PMID:8040268
11. Han ZC, Bellucci S, Walz A, Baggiolini M, Caen JP. Negative regulation of human megakaryocytopoiesis by human platelet factor 4 (PF4) and connective tissue-activating peptide (CTAP-III). Int J Cell Cloning 1990; 8:253-9; http://dx.doi.org/10.1002/stem.5530080409; PMID:2401804
12. Srivastava K, Cockburn IA, Swaim A, Thompson LE, Tripathi A, Fletcher CA, Shirk EM, Sun H, Kowalska MA, Fox-Talbot K, et al. Platelet factor 4 mediates inflammation in experimental cerebral malaria. Cell Host Microbe 2008; 4:179-87; http://dx.doi.org/10.1016/j.chom.2008.07.003; PMID:18692777
13. Cervi D, Yip TT, Bhattacharya N, Podust VN, Peterson J, Abou-Slaybi A, Naumov GN, Bender E, Almog N, Italiano JE Jr., et al. Platelet-associated PF-4 as a biomarker of early tumor growth. Blood 2008; 111:1201-7; http://dx.doi.org/10.1182/blood-2007-04-084798; PMID:17914028
14. Lapchak PH, Ioannou A, Rani P, Lieberman LA, Yoshiya K, Kannan L, Dalle Lucca JJ, Kowalska MA, Tsokos GC. The role of platelet factor 4 in local and remote tissue damage in a mouse model of mesenteric ischemia/reperfusion injury. PLoS One 2012; 7:e39934; http://dx.doi.org/10.1371/journal.pone.0039934; PMID:22792197
15. Lammers KM, Lu R, Brownley J, Lu B, Gerard C, Thomas K, Rallabhandi P, Shea-Donohue T, Tamiz A, Alkan S, et al. Gliadin induces an increase in intestinal permeability and zonulin release by binding to the chemokine receptor CXCR3. Gastroenterology 2008; 135:194-204, e3; http://dx.doi.org/10.1053/j. gastro.2008.03.023; PMID:18485912
16. Han X, Wu Z, Di J, Pan Y, Zhang H, Du Y, Cheng Z, Jin Z, Wang Z, Zheng Q, et al. CXCL9 attenuated chemotherapy-induced intestinal mucositis by inhibiting proliferation and reducing apoptosis. Biomed Pharmacother 2011; 65:547-54; http://dx.doi.org/10.1016/j.biopha.2011.03.008; PMID:21775092
17. Lasagni L, Francalanci M, Annunziato F, Lazzeri E, Giannini S, Cosmi L, Sagrinati C, Mazzinghi B, Orlando C, Maggi E, et al. An alternatively spliced variant of CXCR3 mediates the inhibition of endothelial cell growth induced by IP-10, Mig, and I-TAC, and acts as functional receptor for platelet factor 4. J Exp Med 2003; 197:1537-49; http://dx.doi.org/10.1084/jem.20021897; PMID:12782716
18. Green LA, Petrusca D, Rajashekhar G, Gianaris T, Schweitzer KS, Wang L, Justice MJ, Petrache I, Clauss M. Cigarette smoke-induced CXCR3 receptor up-regulation mediates endothelial apoptosis. Am J Respir Cell Mol Biol 2012; 47:807-14; http://dx.doi.org/10.1165/rcmb.2012-0132OC; PMID:22936405
19. Bulavin DV, Saito S, Hollander MC, Sakaguchi K, Anderson CW, Appella E, Fornace AJ Jr. Phosphorylation of human p53 by p38 kinase coordinates N-terminal phosphorylation and apoptosis in response to UV radiation. EMBO J 1999; 18:6845-54; http://dx.doi.org/10.1093/emboj/18.23.6845; PMID:10581258
20. Pritchard DM, Watson AJ, Potten CS, Jackman AL, Hickman JA. Inhibition by uridine but not thymidine of p53-dependent intestinal apoptosis initiated by 5-fluorouracil: evidence for the involvement of RNA perturbation. Proc Natl Acad Sci U S A 1997; 94:1795-9; http://dx.doi.org/10.1073/pnas.94.5.1795; PMID:9050858
21. Wu ZQ, Han XD, Wang Y, Yuan KL, Jin ZM, Di JZ, Yan J, Pan Y, Zhang P, Huang XY, et al. Interleukin-1 receptor antagonist reduced apoptosis and attenuated intestinal mucositis in a 5-fluorouracil chemotherapy model in mice. Cancer Chemother Pharmacol 2011; 68:87-96; http://dx.doi.org/10.1007/s00280-010- 1451-5; PMID:20844880
22. Yasuda M, Kato S, Yamanaka N, Iimori M, Matsumoto K, Utsumi D, Kitahara Y, Amagase K, Horie S, Takeuchi K. 5-HT 3 receptor antagonists ameliorate 5-fluorouracil-induced intestinal mucositis by suppression of apoptosis in murine intestinal crypt cells. Br J Pharmacol 2013; 168:1388-400; http://dx.doi.org/10.1111/bph.12019; PMID:23072534
23. Korniejewska A, McKnight AJ, Johnson Z, Watson ML, Ward SG. Expression and agonist responsiveness of CXCR3 variants in human T lymphocytes. Immunology 2011; 132:503-15; http://dx.doi.org/10.1111/j.1365-2567.2010.03384.x; PMID:21255008
24. Shahabuddin S, Ji R, Wang P, Brailoiu E, Dun N, Yang Y, Aksoy MO, Kelsen SG. CXCR3 chemokine receptor-induced chemotaxis in human airway epithelial cells: role of p38 MAPK and PI3K signaling pathways. Am J Physiol Cell Physiol 2006; 291:C34-9; http://dx.doi.org/10.1152/ajpcell.00441.2005; PMID:16467404
25. Petrai I, Rombouts K, Lasagni L, Annunziato F, Cosmi L, Romanelli RG, Sagrinati C, Mazzinghi B, Pinzani M, Romagnani S, et al. Activation of p38(MAPK) mediates the angiostatic effect of the chemokine receptor CXCR3-B. Int J Biochem Cell Biol 2008; 40:1764-74; http://dx.doi.org/10.1016/j.biocel.2008.01. 008; PMID:18291705
26. Sidahmed AM, León AJ, Bosinger SE, Banner D, Danesh A, Cameron MJ, Kelvin DJ. CXCL10 contributes to p38-mediated apoptosis in primary T lymphocytes in vitro. Cytokine 2012; 59:433-41; http://dx.doi.org/10.1016/j. cyto.2012.05.002; PMID:22652417
27. Singh L, Arora SK, Bakshi DK, Majumdar S, Wig JD. Potential role of CXCL10 in the induction of cell injury and mitochondrial dysfunction. Int J Exp Pathol 2010; 91:210-23; http://dx.doi.org/10.1111/j.1365-2613.2009.00697.x; PMID:20041963
28. Sui Y, Potula R, Dhillon N, Pinson D, Li S, Nath A, Anderson C, Turchan J, Kolson D, Narayan O, et al. Neuronal apoptosis is mediated by CXCL10 overexpression in simian human immunodeficiency virus encephalitis. Am J Pathol 2004; 164:1557-66; http://dx.doi.org/10.1016/S0002-9440(10)63714-5; PMID:15111302
29. Feldman ED, Weinreich DM, Carroll NM, Burness ML, Feldman AL, Turner E, Xu H, Alexander HR Jr. Interferon gamma-inducible protein 10 selectively inhibits proliferation and induces apoptosis in endothelial cells. Ann Surg Oncol 2006; 13:125-33; http://dx.doi.org/10.1245/ASO.2006.03.038; PMID:16378159
30. Liang P, Cheng SH, Cheng CK, Lau KM, Lin SY, Chow EY, Chan NP, Ip RK, Wong RS, Ng MH. Platelet factor 4 induces cell apoptosis by inhibition of STAT3 via up-regulation of SOCS3 expression in multiple myeloma. Haematologica 2013; 98:288-95; http://dx.doi.org/10.3324/haematol.2012.065607; PMID:22929979
31. Zhang HM, Yuan J, Cheung P, Chau D, Wong BW, McManus BM, Yang D. Gamma interferon-inducible protein 10 induces HeLa cell apoptosis through a p53-dependent pathway initiated by suppression of human papillomavirus type 18 E6 and E7 expression. Mol Cell Biol 2005; 25:6247-58; http://dx.doi.org/10.1128/ MCB.25.14.6247-6258.2005; PMID:15988033
32. Ashkenazi A, Dixit VM. Death receptors: signaling and modulation. Science 1998; 281:1305-8; PMID:9721089; http://dx.doi.org/10.1126/science.281.5381.1305
33. Lacour S, Hammann A, Wotawa A, Corcos L, Solary E, Dimanche-Boitrel MT. Anticancer agents sensitize tumor cells to tumor necrosis factor-related apoptosis-inducing ligand-mediated caspase-8 activation and apoptosis. Cancer Res 2001; 61:1645-51; PMID:11245478
34. Nuñez G, Benedict MA, Hu Y, Inohara N. Caspases: the proteases of the apoptotic pathway. Oncogene 1998; 17:3237-45; http://dx.doi.org/10.1038/sj. onc.1202581; PMID:9916986
35. Pietsch EC, Sykes SM, McMahon SB, Murphy ME. The p53 family and programmed cell death. Oncogene 2008; 27:6507-21; http://dx.doi.org/10.1038/onc. 2008.315; PMID:18955976
36. Farrell CL, Bready JV, Rex KL, Chen JN, DiPalma CR, Whitcomb KL, Yin S, Hill DC, Wiemann B, Starnes CO, et al. Keratinocyte growth factor protects mice from chemotherapy and radiation-induced gastrointestinal injury and mortality. Cancer Res 1998; 58:933-9; PMID:9500453
37. Gibson RJ, Bowen JM, Inglis MR, Cummins AG, Keefe DM. Irinotecan causes severe small intestinal damage, as well as colonic damage, in the rat with implanted breast cancer. J Gastroenterol Hepatol 2003; 18:1095-100; PMID:12911669; http://dx.doi.org/10.1046/j.1440-1746.2003.03136.x