PDGF-BB and bFGF ameliorate radiation-induced intestinal progenitor/stem cell apoptosis via Akt/p53 signaling in mice

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 307, Issue 11, 2014, Pages G1033-G1043

  Liu, Zhihao ^a   Liu, Huiling ^a   Jiang, Jie ^a   Tan, Siwei ^a   Yang, Yidong ^a   Zhan, Yashi ^a   Wu, Bin ^a  

^a THE THIRD AFFILIATED HOSPITAL OF SUN YAT SEN UNIVERSITY   (China)

Author keywords

Akt; BFGF; Intestinal apoptosis; P53; PDGF BB

Indexed keywords

BASIC FIBROBLAST GROWTH FACTOR RECEPTOR; G PROTEIN COUPLED RECEPTOR; G PROTEIN COUPLED RECEPTOR 5; PERIFOSINE; PROTEIN KINASE B; PROTEIN P53; RADIOPROTECTIVE AGENT; RECOMBINANT BASIC FIBROBLAST GROWTH FACTOR RECEPTOR; RECOMBINANT PLATELET DERIVED GROWTH FACTOR BB; RECOMBINANT RECEPTOR; UNCLASSIFIED DRUG; FIBROBLAST GROWTH FACTOR 2; ONCOPROTEIN; PLATELET DERIVED GROWTH FACTOR B; PLATELET-DERIVED GROWTH FACTOR BB;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; CRYPT CELL; CYTOSOLIC FRACTION; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; IMMUNOHISTOCHEMISTRY; INTESTINAL STEM CELL; INTESTINE CRYPT; INTESTINE EPITHELIUM CELL; MOUSE; NICK END LABELING; NONHUMAN; PANETH CELL; PROTEIN EXPRESSION; RADIATION INJURY; RADIATION PROTECTION; SIGNAL TRANSDUCTION; SURVIVAL RATE; WESTERN BLOTTING; ANIMAL; DRUG EFFECTS; INTESTINE; PATHOLOGY; PHYSIOLOGY; RADIATION RESPONSE; STEM CELL;

ANIMALS; APOPTOSIS; FIBROBLAST GROWTH FACTOR 2; INTESTINES; MICE; ONCOGENE PROTEIN V-AKT; PROTO-ONCOGENE PROTEINS C-SIS; RADIATION-PROTECTIVE AGENTS; SIGNAL TRANSDUCTION; STEM CELLS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84913597130     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00151.2014     Document Type: Article

References (35)

1. Barker N, van Es JH, Kuipers J, Kujala P, van den Born M, Cozijnsen M, Haegebarth A, Korving J, Begthel H, Peters PJ, Clevers H. Identification of stem cells in small intestine and colon by marker gene LGR5. Nature449: 1003–1007, 2007.
2. Booth D, Potten CS. Protection against mucosal injury by growth factors and cytokines. J Natl Cancer Inst Monogr2001: 16–20, 2001.
3. Bouleau S, Pârvu-Ferecatu I, Rodriguez-Enfedaque A, Rincheval V, Grimal H, Mignotte B, Vayssiere JL, Renaud F. Fibroblast Growth Factor 1 inhibits p53-dependent apoptosis in PC12 cells. Apoptosis12: 1377–1387, 2007.
4. Ch’ang HJ, Maj JG, Paris F, Xing HR, Zhang J, Truman JP, Cardon-Cardo C, Haimovitz-Friedman A, Kolesnick R, Fuks Z. ATM regulates target switching to escalating doses of radiation in the intestines. Nat Med11: 484–490, 2005.
5. Clarke AR, Jones N, Pryde F, Adachi Y, Sansom OJ. 53BP1 deficiency in intestinal enterocytes does not alter the immediate response to ionizing radiation, but leads to increased nuclear area consistent with polyploidy. Oncogene26: 6349–6355, 2007.
6. Deng W, Wang DA, Gosmanova E, Johnson LR, Tigyi G. LPA protects intestinal epithelial cells from apoptosis by inhibiting the mitochondrial pathway. Am J Physiol Gastrointest Liver Physiol284: G821–G829, 2003.
7. Giannakis M, Stappenbeck TS, Mills JC, Leip DG, Lovett M, Clifton SW, Ippolito JE, Glasscock JI, Arumugam M, Brent MR, Gordon JI. Molecular properties of adult mouse gastric and intestinal epithelial progenitors in their niches. J Biol Chem281: 11292–11300, 2006.
8. Gulati AS, Ochsner SA, Henning SJ. Molecular properties of side population-sorted cells from mouse small intestine. Am J Physiol Gastro-intest Liver Physiol294: G286–G294, 2008.
9. Gu Q, Wang D, Wang X, Peng R, Liu J, Jiang T, Wang Z, Wang S, Deng H. Basic fibroblast growth factor inhibits radiation-induced apopto-sis of HUVECs. I. The PI3K/AKT pathway and induction of phosphory-lation of BAD. Radiat Res161: 692–702, 2004.
10. Houchen CW, George RJ, Sturmoski MA, Cohn SM. FGF-2 enhances intestinal stem cell survival and its expression is induced after radiation injury. Am J Physiol Gastrointest Liver Physiol276: G249–G258, 1999.
11. Houchen CW, Sturmoski MA, Anant S, Breyer RM, Stenson WF. Prosurvival and antiapoptotic effects of PGE2 in radiation injury are mediated by EP2 receptor in intestine. Am J Physiol Gastrointest Liver Physiol284: G490–G498, 2003.
12. Hua G, Thin TH, Feldman R, Haimovitz-Friedman A, Clevers H, Fuks Z, Kolesnick R. Crypt base columnar stem cells in small intestines of mice are radioresistant. Gastroenterology143: 1266–1276, 2012.
13. Ishizuka S, Martin K, Booth C, Potten CS, de Murcia G, Bürkle A, Kirkwood TB. Poly(ADP-ribose) polymerase-1 is a survival factor for radiation-exposed intestinal epithelial stem cells in vivo. Nucleic Acids Res31: 6198–6205, 2003.
14. Katoh M, Katoh M. FGF signaling network in the gastrointestinal tract (review). Int J Oncol29: 163–168, 2006.
15. Komarova EA, Kondratov RV, Wang K, Christov K, Golovkina TV, Goldblum JR, Gudkov AV. Dual effect of p53 on radiation sensitivity in vivo: p53 promotes hematopoietic injury, but protects from gastro-intes-tinal syndrome in mice. Oncogene23: 3265–3271, 2004.
16. Leibowitz BJ, Qiu W, Liu H, Cheng T, Zhang L, Yu J. Uncoupling p53 functions in radiation-induced intestinal damage via PUMA and p21. Mol Cancer Res9: 616–625, 2011.
17. Lennartsson J, Burovic F, Witek B, Jurek A, Heldin CH. Erk 5 is necessary for sustained PDGF-induced Akt phosphorylation and inhibition of apoptosis. Cell Signal22: 955–960, 2010.
18. Levine AJ, Feng Z, Mak TW, You H, Jin S. Coordination and communication between the p53 and IGF-1-AKT-TOR signal transduction pathways. Genes Dev20: 267–275, 2006.
19. Merritt AJ, Potten CS, Kemp CJ, Hickman JA, Balmain A, Lane DP, Hall PA. The role of p53 in spontaneous and radiation-induced apoptosis in the gastrointestinal tract of normal and p53-deficient mice. Cancer Res54: 614–617, 1994.
20. Neta R. Modulation of radiation damage by cytokines. Stem Cells 15, Suppl2: 87–94, 1997.
21. Paris F, Fuks Z, Kang A, Capodieci P, Juan G, Ehleiter D, Haimovitz-Friedman A, Cordon-Cardo C, Kolesnick R. Endothelial apoptosis as the primary lesion initiating intestinal radiation damage in mice. Science293: 293–297, 2001.
22. Qiu W, Carson-Walter EB, Liu H, Epperly M, Greenberger JS, Zambetti GP, Zhang L, Yu J. PUMA regulates intestinal progenitor cell radiosensitivity and gastrointestinal syndrome. Cell Stem Cell2: 576–883, 2008.
23. Sato T, Vries RG, Snippert HJ, van de Wetering M, Barker N, Stange DE, Van Es JH, Abo A, Kujala P, Peters PJ, Clevers H. Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature459: 262–265, 2009.
24. Sangiorgi E, Capecchi MR. Bmi1 is expressed in vivo in intestinal stem cells. Nat Genet40: 915–920, 2008.
25. Shaulian E, Resnitzky D, Shifman O, Blandino G, Amsterdam A, Yayon A, Oren M. Induction of Mdm2 and enhancement of cell survival by bFGF. Oncogene15: 2717–2725, 1997.
26. Son D, Na YR, Hwang ES, Seok SH. Platelet-derived growth factor-C (PDGF-C) induces anti-apoptotic effects on macrophages through Akt and Bad phosphorylation. J Biol Chem289: 6225–6235, 2014.
27. Stappenbeck TS, Mills JC, Gordon JI. Molecular features of adult mouse small intestinal epithelial progenitors. Proc Natl Acad Sci USA100: 1004–1009, 2006.
28. Villunger A, Michalak EM, Coultas L, Müllauer F, Böck G, Ausser-lechner MJ, Adams JM, Strasser A. p53- and drug-induced apoptotic responses mediated by BH3-only proteins puma and noxa. Science302: 1036–1038, 2003.
29. Wang P, Qiu W, Dudgeon C, Liu H, Huang C, Zambetti GP, Yu J, Zhang L. PUMA is directly activated by NF-kappaB and contributes to TNF-alpha-induced apoptosis. Cell Death Differ16: 1192–1202, 2009.
30. Wilkins HR, Ohneda K, Keku TO, D’Ercole AJ, Fuller CR, Williams KL, Lund PK. Reduction of spontaneous and irradiation-induced apopto-sis in small intestine of IGF-I transgenic mice. Am J Physiol Gastrointest Liver Physiol283: G457–G464, 2002.
31. Wu B, Qiu W, Wang P, Yu H, Cheng T, Zambetti GP, Zhang L, Yu J. p53 independent induction of PUMA mediates intestinal apoptosis in response to ischaemia-reperfusion. Gut56: 645–654, 2007.
32. Ye JY, Chan GC, Qiao L, Lian Q, Meng FY, Luo XQ, Khachigian LM, Ma M, Deng R, Chen JL, Chong BH, Yang M. Platelet-derived growth factor enhances platelet recovery in a murine model of radiation-induced thrombocytopenia and reduces apoptosis in megakaryocytes via its receptors and the PI3-k/Akt pathway. Haematologica95: 1745–1753, 2010.
33. Yonish-Rouach ERD, Lotem J, Sachs L, Kimchi A, Oren M. Wild-type p53 induces apoptosis of myeloid leukaemic cells that is inhibited by interleukin-6. Nature352: 345–347, 1991.
34. Yu J, Zhang L. The transcriptional targets of p53 in apoptosis control. Biochem Biophys Res Commun331: 851–858, 2005.
35. Zhu L, Gibson P, Currle DS, Tong Y, Richardson RJ, Bayazitov IT, Poppleton H, Zakharenko S, Ellison DW, Gilbertson RJ. Prominin 1 marks intestinal stem cells that are susceptible to neoplastic transformation. Nature457: 603–607, 2009.