Radiation persistently promoted oxidative stress, activated mTOR via PI3K/Akt, and downregulated autophagy pathway in mouse intestine

International Journal of Biochemistry and Cell Biology

Volumn 57, Issue , 2014, Pages 167-176

  Datta, Kamal ^a,b   Suman, Shubhankar ^a,b   Fornace, Albert J ^a,b,c  

^a GEORGETOWN UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b GEORGETOWN UNIVERSITY   (United States)

^c KING ABDULAZIZ UNIVERSITY   (Saudi Arabia)

Author keywords

Autophagy; Intestine; Mitochondria; Oxidative stress; Radiation

Indexed keywords

MTOR PROTEIN, MOUSE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; TARGET OF RAPAMYCIN KINASE;

ANIMAL; AUTOPHAGY; C57BL MOUSE; DOWN REGULATION; EXPERIMENTAL RADIATION INJURY; FEMALE; INTESTINE; METABOLISM; MITOCHONDRION; MOUSE; OXIDATIVE STRESS; PHYSIOLOGY; RADIATION RESPONSE; SIGNAL TRANSDUCTION;

ANIMALS; AUTOPHAGY; DOWN-REGULATION; FEMALE; INTESTINES; MICE; MICE, INBRED C57BL; MITOCHONDRIA; OXIDATIVE STRESS; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; RADIATION INJURIES, EXPERIMENTAL; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES;

EID: 84964698545     PISSN: 13572725     EISSN: 18785875     Source Type: Journal    
DOI: 10.1016/j.biocel.2014.10.022     Document Type: Article

References (58)

1. Apel, A., Herr, I., Schwarz, H., Rodemann, H.P., Mayer, A., Blocked autophagy sensitizes resistant carcinoma cells to radiation therapy. Cancer Res 68 (2008), 1485–1494.
2. Bissonnette, R., Lee, M.J., Wang, E., The differentiation process of intestinal epithelial cells is associated with the appearance of statin, a non-proliferation-specific nuclear protein. J Cell Sci 95 (1990), 247–254.
3. Bjorkoy, G., Lamark, T., Pankiv, S., Overvatn, A., Brech, A., Johansen, T., Monitoring autophagic degradation of p62/SQSTM1. Methods Enzymol 452 (2009), 181–197.
4. Brenner, D.J., Doll, R., Goodhead, D.T., Hall, E.J., Land, C.E., Little, J.B., et al. Cancer risks attributable to low doses of ionizing radiation: assessing what we really know. Proc Natl Acad Sci U S A 100 (2003), 13761–13766.
5. Budina-Kolomets, A., Hontz, R.D., Pimkina, J., Murphy, M.E., A conserved domain in exon 2 coding for the human and murine ARF tumor suppressor protein is required for autophagy induction. Autophagy, 2013, 9.
6. Chen, Y., Klionsky, D.J., The regulation of autophagy – unanswered questions. J Cell Sci 124 (2011), 161–170.
7. Chen, Y.S., Song, H.X., Lu, Y., Li, X., Chen, T., Zhang, Y., et al. Autophagy inhibition contributes to radiation sensitization of esophageal squamous carcinoma cells. Dis Esophagus 24 (2011), 437–443.
8. Ciccia, F., Accardo-Palumbo, A., Rizzo, A., Guggino, G., Raimondo, S., Giardina, A., et al. Evidence that autophagy, but not the unfolded protein response, regulates the expression of IL-23 in the gut of patients with ankylosing spondylitis and subclinical gut inflammation. Ann Rheum Dis, 2013.
9. Clarke, R., Shajahan, A.N., Riggins, R.B., Cho, Y., Crawford, A., Xuan, J., et al. Gene network signaling in hormone responsiveness modifies apoptosis and autophagy in breast cancer cells. J Steroid Biochem Mol Biol 114 (2009), 8–20.
10. Codogno, P., Meijer, A.J., Autophagy: a potential link between obesity and insulin resistance. Cell Metab 11 (2010), 449–451.
11. Datta, K., Suman, S., Kallakury, B.V., Fornace, A.J.J., Exposure to heavy ion radiation induces persistent oxidative stress in mouse intestine. PLoS ONE, 7, 2012, e42224.
12. Datta, K., Hyduke, D.R., Suman, S., Moon, B.H., Johnson, M.D., Fornace, A.J.J., Exposure to ionizing radiation induced persistent gene expression changes in mouse mammary gland. Radiother Oncol, 7, 2012, 205.
13. Datta, K., Suman, S., Kallakury, B.V., Fornace, A.J.J., Heavy ion radiation exposure triggered higher intestinal tumor frequency and greater beta-catenin activation than gamma radiation in APC(Min/+) mice. PLoS ONE, 8, 2013, e59295.
14. Davidson, S.T., Any dose is too high. Environ Health Perspect, 113, 2005, A735.
15. Gilbert, E.S., Omohundro, E., Buchanan, J.A., Holter, N.A., Mortality of workers at the Hanford site: 1945–1986. Health Phys 64 (1993), 577–590.
16. Hauer-Jensen, M., Wang, J., Boerma, M., Fu, Q., Denham, J.W., Radiation damage to the gastrointestinal tract: mechanisms, diagnosis, and management. Curr Opin Support Palliat Care 1 (2007), 23–29.
17. He, S., Wang, C., Dong, H., Xia, F., Zhou, H., Jiang, X., et al. Immune-related GTPase M (IRGM1) regulates neuronal autophagy in a mouse model of stroke. Autophagy 8 (2012), 1621–1627.
18. He, G., Wang, Y., Pang, X., Zhang, B., Inhibition of autophagy induced by TSA sensitizes colon cancer cell to radiation. Tumour Biol 35 (2014), 1003–1011.
19. Henson, C., Chronic radiation proctitis: issues surrounding delayed bowel dysfunction post-pelvic radiotherapy and an update on medical treatment. Ther Adv Gastroenterol 3 (2010), 359–365.
20. Huigsloot, M., Tijdens, I.B., Mulder, G.J., van de Water, B., Differential regulation of doxorubicin-induced mitochondrial dysfunction and apoptosis by Bcl-2 in mammary adenocarcinoma (MTLn3) cells. J Biol Chem 277 (2002), 35869–35879.
21. Jo, Y.K., Kim, S.C., Park, I.J., Park, S.J., Jin, D.H., Hong, S.W., et al. Increased expression of ATG10 in colorectal cancer is associated with lymphovascular invasion and lymph node metastasis. PLoS ONE, 7, 2012, e52705.
22. Jung, C.H., Ro, S.H., Cao, J., Otto, N.M., Kim, D.H., mTOR regulation of autophagy. FEBS Lett 584 (2010), 1287–1295.
23. Kalvakolanu, D.V., Gade, P., IFNG and autophagy: a critical role for the ER-stress mediator ATF6 in controlling bacterial infections. Autophagy 8 (2012), 1673–1674.
24. Kim, G.J., Fiskum, G.M., Morgan, W.F., A role for mitochondrial dysfunction in perpetuating radiation-induced genomic instability. Cancer Res 66 (2006), 10377–10383.
25. Kongara, S., Karantza, V., The interplay between autophagy and ROS in tumorigenesis. Front Oncol, 2, 2012, 171.
26. Le Grand, J.N., Chakrama, F.Z., Seguin-Py, S., Fraichard, A., Delage-Mourroux, R., Jouvenot, M., et al. GABARAPL1 (GEC1): original or copycat?. Autophagy 7 (2011), 1098–1107.
27. Lee, J., Giordano, S., Zhang, J., Autophagy, mitochondria and oxidative stress: cross-talk and redox signalling. Biochem J 441 (2012), 523–540.
28. Li, S., Du, L., Zhang, L., Hu, Y., Xia, W., Wu, J., et al. Cathepsin B contributes to autophagy-related 7 (Atg7)-induced nod-like receptor 3 (NLRP3)-dependent proinflammatory response and aggravates lipotoxicity in rat insulinoma cell line. J Biol Chem 288 (2013), 30094–30104.
29. Liang, B., Kong, D., Liu, Y., Liang, N., He, M., Ma, S., et al. Autophagy inhibition plays the synergetic killing roles with radiation in the multi-drug resistant SKVCR ovarian cancer cells. Radiother Oncol, 7, 2012, 213.
30. Liang, N., Jia, L., Liu, Y., Liang, B., Kong, D., Yan, M., et al. ATM pathway is essential for ionizing radiation-induced autophagy. Cell Signal 25 (2013), 2530–2539.
31. Luciani, A., Villella, V.R., Esposito, S., Gavina, M., Russo, I., Silano, M., et al. Targeting autophagy as a novel strategy for facilitating the therapeutic action of potentiators on DeltaF508 cystic fibrosis transmembrane conductance regulator. Autophagy 8 (2012), 1657–1672.
32. Luo, C., Li, Y., Wang, H., Feng, Z., Li, Y., Long, J., et al. Mitochondrial accumulation under oxidative stress is due to defects in autophagy. J Cell Biochem 114 (2013), 212–219.
33. Macartney, K.K., Baumgart, D.C., Carding, S.R., Brubaker, J.O., Offit, P.A., Primary murine small intestinal epithelial cells, maintained in long-term culture, are susceptible to rotavirus infection. J Virol 74 (2000), 5597–5603.
34. Mizushima, N., Autophagy: process and function. Genes Dev 21 (2007), 2861–2873.
35. Ning, Y., Riggins, R.B., Mulla, J.E., Chung, H., Zwart, A., Clarke, R., IFNgamma restores breast cancer sensitivity to fulvestrant by regulating STAT1, IFN regulatory factor 1, NF-kappaB, BCL2 family members, and signaling to caspase-dependent apoptosis. Mol Cancer Ther 9 (2010), 1274–1285.
36. Patel, K.K., Stappenbeck, T.S., Autophagy and intestinal homeostasis. Annu Rev Physiol 75 (2013), 241–262.
37. Plotegher, N., Civiero, L., Neuronal autophagy, alpha-synuclein clearance, and LRRK2 regulation: a lost equilibrium in parkinsonian brain. J Neurosci 32 (2012), 14851–14853.
38. Preston, D.L., Shimizu, Y., Pierce, D.A., Suyama, A., Mabuchi, K., Studies of mortality of atomic bomb survivors. Report 13: solid cancer and noncancer disease mortality: 1950–1997. Radiat Res 160 (2003), 381–407.
39. Renna, M., Schaffner, C., Winslow, A.R., Menzies, F.M., Peden, A.A., Floto, R.A., et al. Autophagic substrate clearance requires activity of the syntaxin-5 SNARE complex. J Cell Sci 124 (2011), 469–482.
40. Ritz, B., Radiation exposure and cancer mortality in uranium processing workers. Epidemiology 10 (1999), 531–538.
41. Rubinsztein, D.C., Codogno, P., Levine, B., Autophagy modulation as a potential therapeutic target for diverse diseases. Nat Rev Drug Discov 11 (2012), 709–730.
42. Sallmyr, A., Fan, J., Datta, K., Kim, K.T., Grosu, D., Shapiro, P., et al. Internal tandem duplication of FLT3 (FLT3/ITD) induces increased ROS production, DNA damage, and misrepair: implications for poor prognosis in AML. Blood 111 (2008), 3173–3182.
43. Sarkar, S., Korolchuk, V.I., Renna, M., Imarisio, S., Fleming, A., Williams, A., et al. Complex inhibitory effects of nitric oxide on autophagy. Mol Cell 43 (2011), 19–32.
44. Shillingford, J.M., Piontek, K.B., Germino, G.G., Weimbs, T., Rapamycin ameliorates PKD resulting from conditional inactivation of Pkd1. J Am Soc Nephrol 21 (2010), 489–497.
45. Skaland, I., Janssen, E.A., Gudlaugsson, E., Klos, J., Kjellevold, K.H., Soiland, H., et al. Phosphohistone H3 expression has much stronger prognostic value than classical prognosticators in invasive lymph node-negative breast cancer patients less than 55 years of age. Mod Pathol 20 (2007), 1307–1315.
46. Slomovitz, B.M., Coleman, R.L., The PI3K/AKT/mTOR pathway as a therapeutic target in endometrial cancer. Clin Cancer Res 18 (2012), 5856–5864.
47. Sont, W.N., Zielinski, J.M., Ashmore, J.P., Jiang, H., Krewski, D., Fair, M.E., et al. First analysis of cancer incidence and occupational radiation exposure based on the National Dose Registry of Canada. Am J Epidemiol 153 (2001), 309–318.
48. Stacey, R., Green, J.T., Radiation-induced small bowel disease: latest developments and clinical guidance. Ther Adv Chronic Dis 5:1 (2014), 15–29.
49. Suman, S., Johnson, M.D., Fornace, A.J.J., Datta, K., Exposure to ionizing radiation causes long-term increase in serum estradiol and activation of PI3K-Akt signaling pathway in mouse mammary gland. Int J Radiat Oncol Biol Phys 84 (2012), 500–507.
50. Suman, S., Rodriguez, O.C., Winters, T.A., Fornace, A.J.J., Albanese, C., Datta, K., Therapeutic and space radiation exposure of mouse brain causes impaired DNA repair response and premature senescence by chronic oxidant production. Aging (Albany NY) 5 (2013), 607–622.
51. Thiagarajah, J.R., Gourmelon, P., Griffiths, N.M., Lebrun, F., Naftalin, R.J., Pedley, K.C., Radiation induced cytochrome c release causes loss of rat colonic fluid absorption by damage to crypts and pericryptal myofibroblasts. Gut 47 (2000), 675–684.
52. Wang, J., Kang, R., Huang, H., Xi, X., Wang, B., Wang, J., et al. Hepatitis C virus core protein activates autophagy through EIF2AK3 and ATF6 UPR pathway-mediated MAP1LC3B and ATG12 expression. Autophagy, 2014, 10.
53. Wu, W.K., Coffelt, S.B., Cho, C.H., Wang, X.J., Lee, C.W., Chan, F.K., et al. The autophagic paradox in cancer therapy. Oncogene 31 (2012), 939–953.
54. Xie, Z., Klionsky, D.J., Autophagosome formation: core machinery and adaptations. Nat Cell Biol 9 (2007), 1102–1109.
55. Xie, H., Hu, J., Pan, H., Lou, Y., Lv, P., Chen, Y., Adenovirus vector-mediated FAM176A overexpression induces cell death in human H1299 non-small cell lung cancer cells. BMB Rep 47 (2014), 104–109.
56. Zhang, Y., Yang, J.H., Activation of the PI3K/Akt pathway by oxidative stress mediates high glucose-induced increase of adipogenic differentiation in primary rat osteoblasts. J Cell Biochem 114 (2013), 2595–2602.
57. Zhang, Y., Wu, Y., Cheng, Y., Zhao, Z., Tashiro, S., Onodera, S., et al. Fas-mediated autophagy requires JNK activation in HeLa cells. Biochem Biophys Res Commun 377 (2008), 1205–1210.
58. Zhuang, W., Qin, Z., Liang, Z., The role of autophagy in sensitizing malignant glioma cells to radiation therapy. Acta Biochim Biophys Sin (Shanghai) 41 (2009), 341–351.