Updates from the intestinal front line: Autophagic weapons against inflammation and cancer

Cells

Volumn 1, Issue 3, 2012, Pages 535-557

  Madia, Federica ^a   Grossi, Valentina ^a   Peserico, Alessia ^a   Simone, Cristiano ^a,b  

^a Laboratorio Angela Valenti dei Fattori Genetici e Ambientali di Rischio Trombotico   (Italy)

^b UNIVERSITY OF BARI   (Italy)

Author keywords

Autophagy; Chemotherapy; Colorectal cancer; Inflammation; p38a

Indexed keywords

ACETYLSALICYLIC ACID; BAFILOMYCIN A1; BEVACIZUMAB; CASPASE RECRUITMENT DOMAIN PROTEIN 4; CETUXIMAB; CHLOROQUINE; CISPLATIN; FLUOROURACIL; FOLINIC ACID; HYPOXIA INDUCIBLE FACTOR; IRINOTECAN; OXALIPLATIN; SYNAPTOPHYSIN; VORINOSTAT;

ADAPTIVE IMMUNITY; AGING; APOPTOSIS; AUTOPHAGY; CLINICAL TRIAL (TOPIC); COLORECTAL CANCER; CROHN DISEASE; DISEASE PREDISPOSITION; ENTERITIS; GENETICS; HELICOBACTER INFECTION; HEREDITARY NONPOLYPOSIS COLORECTAL CANCER; HUMAN; IMMUNE SYSTEM; INFLAMMATION; NEOPLASM; NONHUMAN; OBESITY; OVARY CANCER; OXIDATIVE STRESS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; REVIEW; RISK FACTOR; ULCERATIVE COLITIS;

EID: 84905821501     PISSN: None     EISSN: 20734409     Source Type: Journal    
DOI: 10.3390/cells1030535     Document Type: Review

References (132)

1. Siegel, R.; Naishadham, D.; Jemal, A. Cancer statistics, 2012. CA Cancer J. Clin. 2012, 62, 10-29.
2. Ferlay, J.; Parkin, D.M.; Steliarova-Foucher, E. Estimates of cancer incidence and mortality in Europe in 2008. Eur. J. Cancer 2010, 46, 765-781.
3. Cunningham, D.; Atkin, W.; Lenz, H.J.; Lynch, H.T.; Minsky, B.; Nordlinger, B.; Starling, N. Colorectal cancer. Lancet 2010, 375, 1030-1047.
4. Migheli, F.; Migliore, L. Epigenetics of colorectal cancer. Clin. Genet. 2012, 81, 312-318.
5. Markowitz, S.D.; Bertagnolli, M.M. Molecular origins of cancer: Molecular basis of colorectal cancer. New Engl. J. Med. 2009, 361, 2449-60.
6. Leach, F.S.; Nicolaides, N.C.; Papadopoulos, N.; Liu, B.; Jen, J.; Parsons, R.; Peltomaki, P.; Sistonen, P.; Aaltonen, L.A.; Nystrom-Lahti, M.; et al. Mutations of a muts homolog in hereditary nonpolyposis colorectal cancer. Cell 1993, 75, 1215-1225.
7. Fishel, R.; Lescoe, M.K.; Rao, M.R.; Copeland, N.G.; Jenkins, N.A.; Garber, J.; Kane, M.; Kolodner, R. The human mutator gene homolog MSH2 and its association with hereditary nonpolyposis colon cancer. Cell 1993, 75, 1027-1038.
8. Bronner, C.E.; Baker, S.M.; Morrison, P.T.; Warren, G.; Smith, L.G.; Lescoe, M.K.; Kane, M.; Earabino, C.; Lipford, J.; Lindblom, A. Mutation in the DNA mismatch repair gene homologue hMLH1 is associated with hereditary non-polyposis colon cancer. Nature 1994, 368, 258-261.
9. Issa, J.P. CpG island methylator phenotype in cancer. Nat. Rev. Cancer 2004, 4, 988-993.
10. Kondo, Y.; Issa, J.P. Epigenetic changes in colorectal cancer. Cancer Metastasis Rev. 2004, 23, 29-39.
11. Nosho, K.; Irahara, N.; Shima, K.; Kure, S.; Kirkner, G.J.; Schernhammer, E.S.; Hazra, A.; Hunter, D.J.; Quackenbush, J.; Spiegelman, D. Comprehensive biostatistical analysis of CpG island methylator phenotype in colorectal cancer using a large population-based sample. PLoS One 2008, 3, e3698.
12. Howe, J.R.; Roth, S.; Ringold, J.C.; Summers, R.W.; Jarvinen, H.J.; Sistonen, P.; Tomlinson, I.P.; Houlston, R.S.; Bevan, S.; Mitros, F.A.; et al. Mutations in the SMAD4/DPC4 gene in juvenile polyposis. Science 1998, 280, 1086-1088.
13. Fearon, E.R.; Vogelstein, B. A genetic model for colorectal tumorigenesis. Cell 1990, 61, 759-767.
14. Kinzler, K.W.; Vogelstein, B. Lessons from hereditary colorectal cancer. Cell 1996, 87, 159-170.
15. Kinzler, K. W; Vogelstein, B. Life (and death) in a malignant tumour. Nature 1996, 379, 9-20.
16. National Cancer Institue Database. http://seer.cancer.gov/csr/1975_2009_pops09/ (accessed on 30 April 2012)
17. Gruber, S.B.; Ellis, N.A.; Scott, K.K.; Almog, R.; Kolachana, P.; Bonner, J.D.; Kirchhoff, T.; Tomsho, L.P.; Nafa, K.; Pierce, H.; et al. BLM heterozygosity and the risk of colorectal cancer. Science 2002, 297, 2013.
18. International Agency for Research on Caner. Fruit and Vegetables; Vainio, H., Bianchini, F., Eds.; International Agency for Research on Caner: Lyon, France, 2003.
19. Bianchini, F.; Kaaks, R.; Vainio, H. Overweight, obesity, and cancer risk. Lancet Oncol. 2002, 3, 565-574.
20. National Cancer Policy Board. Fulfilling the Potential of Cancer Prevention and Early Detection; Curry, S.J., Byers, T., Hewitt, M., Eds.; National Academies Press: Washington, DC, USA, 2003.
21. La Vecchia, C.; Gallus, S.; Talamini, R.; Decarli, A.; Negri, E.; Franceschi, S. Interaction between selected environmental factors and familial propensity for colon cancer. Eur. J. Cancer Prev. 1999, 8, 147-150.
22. Hall, E.H.; Crowe, S.E. Environmental and lifestyle influences on disorders of the large and small intestine: Implications for treatment. Dig. Dis. 2011, 29, 249-254.
23. Vannucci, L. To suppress to rescue? Changing the approach for recalling anticancer immune responses. Front. Biosci. (Schol. Ed.) 2010, 2, 1189-1197.
24. Blaut, M. Ecology and Physiology of the Intestinal Tract. Curr. Top. Microbiol. Immunol. 2011, doi: 10.1007/82_2011_192.
25. Possemiers, S.; Grootaert, C.; Vermeiren, J.; Gross, G.; Marzorati, M.; Verstraete, W.; Van de Wiele, T. The intestinal environment in health and disease-Recent insights on the potential of intestinal bacteria to influence human health. Curr. Pharm. Des. 2009, 15, 2051-2065.
26. Jackson, L.; Evers, B.M. Chronic inflammation and pathogenesis of GI and pancreatic cancers. Cancer Treat. Res. 2006, 130, 39-65.
27. Tlaskalova-Hogenova, H.; Farre-Castany, M.A.; Stepankova, R.; Kozakova, H.; Tuckova, L.; Funda, D.P.; Barot, R.; Cukrowska, B.; Sinkora, J.; Mandel, L.; et al. The gut as a lymphoepithelial organ: The role of intestinal epithelial cells in mucosal immunity. Folia Microbiol. (Praha) 1995, 40, 385-391.
28. Ullman, T.A.; Itzkowitz, S.H. Intestinal inflammation and cancer. Gastroenterology 2011, 140, 1807-1816.
29. Rutter, M.; Saunders, B.; Wilkinson, K.; Rumbles, S.; Schofield, G.; Kamm, M.; Williams, C.; Price, A.; Talbot, I.; Forbes, A. Severity of inflammation is a risk factor for colorectal neoplasia in ulcerative colitis. Gastroenterology 2004, 126, 451-459.
30. Waldner, M.J.; Neurath, M.F. Cytokines in colitis associated cancer: Potential drug targets? Inflamm. Allergy Drug. Targets 2008, 7, 187-194.
31. Popivanova, B.K.; Kitamura, K.; Wu, Y.; Kondo, T.; Kagaya, T.; Kaneko, S.; Oshima, M.; Fujii, C.; Mukaida, N. Blocking TNF-alpha in mice reduces colorectal carcinogenesis associated with chronic colitis. J. Clin. Invest. 2008, 118, 560-570.
32. Seo, G.S. The role of NF-kappaB in colon cancer. Korean J. Gastroenterol. 2011, 57, 3-7.
33. Agarwal, S.; Mayer, L. Gastrointestinal manifestations in primary immune disorders. Inflamm. Bowel Dis. 2009, 16, 703-711.
34. Marks, F.; Furstenberger, G.; Muller-Decker, K. Metabolic targets of cancer chemoprevention: Interruption of tumor development by inhibitors of arachidonic acid metabolism. Recent Res. Cancer 1999, 151, 45-67.
35. Kaur, J.; Sanyal, S.N. PI3-kinase/Wnt association mediates COX-2/PGE(2) pathway to inhibit apoptosis in early stages of colon carcinogenesis: Chemoprevention by diclofenac. Tumour Biol. 2010, 31, 623-631.
36. Cromer, W.E.; Mathis, J.M.; Granger, D.N.; Chaitanya, G.V.; Alexander, J.S. Role of the endothelium in inflammatory bowel diseases. World J. Gastroenterol. 2011, 17, 578-593.
37. Rogler, G.; Brand, K.; Vogl, D.; Page, S.; Hofmeister, R.; Andus, T.; Knuechel, R.; Baeuerle, P.A.; Scholmerich, J.; Gross, V. Nuclear factor kappaB is activated in macrophages and epithelial cells of inflamed intestinal mucosa. Gastroenterology 1998, 115, 357-369.
38. Nagendraprabhu, P.; Sudhandiran, G. Astaxanthin inhibits tumor invasion by decreasing extracellular matrix production and induces apoptosis in experimental rat colon carcinogenesis by modulating the expressions of ERK-2, NFkB and COX-2. Invest. New Drug. 2009, 29, 207-224.
39. Umesalma, S.; Sudhandiran, G. Differential inhibitory effects of the polyphenol ellagic acid on inflammatory mediators NF-kappaB, iNOS, COX-2, TNF-alpha, and IL-6 in 1,2-dimethylhydrazineinduced rat colon carcinogenesis. Basic Clin. Pharmacol. 2010, 107, 650-625.
40. Grivennikov, S.I.; Karin, M. Inflammation and oncogenesis: A vicious connection. Curr. Opin. Genet. Dev. 2009, 20, 5-71.
41. Grivennikov, S.I.; Karin, M. Dangerous liaisons: STAT3 and NF-kappaB collaboration and crosstalk in cancer. Cytokine Growth F.R. 2010, 21, 11-19.
42. Levine, B.; Mizushima, N.; Virgin, H.W. Autophagy in immunity and inflammation. Nature 2011, 469, 323-335.
43. Deretic, V.; Levine, B. Autophagy, immunity, and microbial adaptations. Cell Host Microbe 2009, 5, 527-549.
44. Levine, B.; Klionsky, D.J. Development by self-digestion: Molecular mechanisms and biological functions of autophagy. Dev. Cell 2004, 6, 463-477.
45. Levine, B.; Kroemer, G. Autophagy in the pathogenesis of disease. Cell 2008, 132, 27-42.
46. He, C.; Klionsky, D.J. Regulation mechanisms and signaling pathways of autophagy. Annu. Rev. Genet. 2009, 43, 67-93.
47. Sumpter, R., Jr.; Levine, B. Autophagy and innate immunity: triggering, targeting and tuning. Semin. Cell Dev. Biol. 2010, 21, 699-711.
48. Klionsky, D.J.; Abeliovich, H.; Agostinis, P.; Agrawal, D.K.; Aliev, G.; Askew, D.S.; Baba, M.; Baehrecke, E.H.; Bahr, B.A.; Ballabio, A.; et al. Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 2008, 4, 151-175.
49. Klionsky, D.J.; Baehrecke, E.H.; Brumell, J.H.; Chu, C.T.; Codogno, P.; Cuervo, A.M.; Debnath, J.; Deretic, V.; Elazar, Z.; Eskelinen, E.L.; et al. A comprehensive glossary of autophagy-related molecules and processes (2nd ed.). Autophagy 2011, 7, 1273-1294.
50. Hampe, J.; Franke, A.; Rosenstiel, P.; Till, A.; Teuber, M.; Huse, K.; Albrecht, M.; Mayr, G.; De La Vega, F.M.; Briggs, J.; et al. A genome-wide association scan of nonsynonymous SNPs identifies a susceptibility variant for Crohn disease in ATG16L1. Nat. Genet. 2007, 39, 207-211.
51. Kuballa, P.; Huett, A.; Rioux, J.D.; Daly, M.J.; Xavier, R.J. Impaired autophagy of an intracellular pathogen induced by a Crohn's disease associated ATG16L1 variant. PLoS One 2008, 3, e3391.
52. Cadwell, K.; Liu, J.Y.; Brown, S.L.; Miyoshi, H.; Loh, J.; Lennerz, J.K.; Kishi, C.; Kc, W.; Carrero, J.A.; Hunt, S.; et al. A key role for autophagy and the autophagy gene Atg16l1 in mouse and human intestinal Paneth cells. Nature 2008, 456, 259-263.
53. Kobayashi, K.S.; Chamaillard, M.; Ogura, Y.; Henegariu, O.; Inohara, N.; Nunez, G.; Flavell, R.A. Nod2-dependent regulation of innate and adaptive immunity in the intestinal tract. Science 2005, 307, 731-734.
54. Kabi, A.; Nickerson, K.P.; Homer, C.R.; McDonald, C. Digesting the genetics of inflammatory bowel disease: Insights from studies of autophagy risk genes. Inflamm. Bowel Dis. 2011, 18, 782-792.
55. Waterman, M.; Xu, W.; Stempak, J.M.; Milgrom, R.; Bernstein, C.N.; Griffiths, A.M.; Greenberg, G.R.; Steinhart, A.H.; Silverberg, M.S. Distinct and overlapping genetic loci in Crohn's disease and ulcerative colitis: Correlations with pathogenesis. Inflamm. Bowel Dis. 2011, 17, 1936-1942.
56. Parkes, M.; Barrett, J.C.; Prescott, N.J.; Tremelling, M.; Anderson, C.A.; Fisher, S.A.; Roberts, R.G.; Nimmo, E.R.; Cummings, F.R.; Soars, D.; et al. Sequence variants in the autophagy gene IRGM and multiple other replicating loci contribute to Crohn's disease susceptibility. Nat. Genet. 2007, 39, 830-832.
57. Rioux, J.D.; Xavier, R.J.; Taylor, K.D.; Silverberg, M.S.; Goyette, P.; Huett, A.; Green, T.; Kuballa, P.; Barmada, M.M.; Datta, L.W.; et al. Genome-wide association study identifies new susceptibility loci for Crohn disease and implicates autophagy in disease pathogenesis. Nat. Genet. 2007, 39, 596-604.
58. Pei, F.H.; Wang, Y.J.; Gao, S.L.; Liu, B.R.; Du, Y.J.; Liu, W.; Yu, H.Y.; Zhao, L.X.; Chi, B.R. Vitamin D receptor gene polymorphism and ulcerative colitis susceptibility in Han Chinese. J. Dig. Dis. 2011, 12, 90-98.
59. Naderi, N.; Farnood, A.; Habibi, M.; Derakhshan, F.; Balaii, H.; Motahari, Z.; Agah, M.R.; Firouzi, F.; Rad, M.G.; Aghazadeh, R.; et al. Association of vitamin D receptor gene polymorphisms in Iranian patients with inflammatory bowel disease. J. Gastroen. Hepatol. 2008, 23, 1816-1822.
60. Dresner-Pollak, R.; Ackerman, Z.; Eliakim, R.; Karban, A.; Chowers, Y.; Fidder, H.H. The BsmI vitamin D receptor gene polymorphism is associated with ulcerative colitis in Jewish Ashkenazi patients. Genet. Test. 2004, 8, 417-420.
61. Wang, T.T.; Dabbas, B.; Laperriere, D.; Bitton, A.J.; Soualhine, H.; Tavera-Mendoza, L.E.; Dionne, S.; Servant, M.J.; Bitton, A.; Seidman, E.G.; et al. Direct and indirect induction by 1,25-dihydroxyvitamin D3 of the NOD2/CARD15-defensin beta2 innate immune pathway defective in Crohn disease. J. Biol. Chem. 2010, 285, 2227-2231.
62. Groulx, J.-F.; Khalfaoui, T.; Benoit, Y.D.; Bernatchez, G.; Carrier, J.C.; Basora, N.; Beaulieu, J.-F. Autophagy is active in normal colon mucosa. Autophagy 2012, in press.
63. Mizushima, N.; Levine, B.; Cuervo, A.M.; Klionsky, D.J. Autophagy fights disease through cellular self-digestion. Nature 2008, 451, 1069-1075.
64. Liang, C.; Feng, P.; Ku, B.; Dotan, I.; Canaani, D.; Oh, B.H.; Jung, J.U. Autophagic and tumour suppressor activity of a novel Beclin1-binding protein UVRAG. Nat. Cell Biol. 2006, 8, 688-699.
65. Knaevelsrud, H.; Ahlquist, T.; Merok, M.A.; Nesbakken, A.; Stenmark, H.; Lothe, R.A.; Simonsen, A. UVRAG mutations associated with microsatellite unstable colon cancer do not affect autophagy. Autophagy 2010, 6, 863-870.
66. Kim, M.J.; Woo, S.J.; Yoon, C.H.; Lee, J.S.; An, S.; Choi, Y.H.; Hwang, S.G.; Yoon, G.; Lee, S.J. Involvement of autophagy in oncogenic K-Ras-induced malignant cell transformation. J. Biol. Chem. 2011, 286, 12924-12932.
67. Wei, H.; Wei, S.; Gan, B.; Peng, X.; Zou, W.; Guan, J.L. Suppression of autophagy by FIP200 deletion inhibits mammary tumorigenesis. Genes Dev. 2011, 25, 1510-1527.
68. Ogier-Denis, E.; Houri, J.J.; Bauvy, C.; Codogno, P. Guanine nucleotide exchange on heterotrimeric Gi3 protein controls autophagic sequestration in HT-29 cells. J. Biol. Chem. 1996, 271, 28593-28600.
69. Egan, D.; Kim, J.; Shaw, R.J.; Guan, K.L. The autophagy initiating kinase ULK1 is regulated via opposing phosphorylation by AMPK and mTOR. Autophagy 2011, 7, 643-644.
70. Diaz-Troya, S.; Perez-Perez, M.E.; Florencio, F.J.; Crespo, J.L. The role of TOR in autophagy regulation from yeast to plants and mammals. Autophagy 2008, 4, 851-865.
71. Habeeb, B.S.; Kitayama, J.; Nagawa, H. Adiponectin supports cell survival in glucose deprivation through enhancement of autophagic response in colorectal cancer cells. Cancer Sci. 2011, 102, 999-1006.
72. Ogier-Denis, E.; Pattingre, S.; El Benna, J.; Codogno, P. Erk1/2-dependent phosphorylation of Galpha-interacting protein stimulates its GTPase accelerating activity and autophagy in human colon cancer cells. J. Biol. Chem. 2000, 275, 39090-39095.
73. Galluzzi, L.; Vitale, I.; Abrams, J.M.; Alnemri, E.S.; Baehrecke, E.H.; Blagosklonny, M.V.; Dawson, T.M.; Dawson, V.L.; El-Deiry, W.S.; Fulda, S.; et al. Molecular definitions of cell death subroutines: Recommendations of the Nomenclature Committee on Cell Death 2012. Cell Death Differ. 2012, 19, 107-120.
74. Sato, K.; Tsuchihara, K.; Fujii, S.; Sugiyama, M.; Goya, T.; Atomi, Y.; Ueno, T.; Ochiai, A.; Esumi, H. Autophagy is activated in colorectal cancer cells and contributes to the tolerance to nutrient deprivation. Cancer Res. 2007, 67, 9677-9684.
75. Watson, A.J. An overview of apoptosis and the prevention of colorectal cancer. Crit. Rev. Oncol. Hemat. 2006, 57, 107-121.
76. Gao, C.; Cao, W.; Bao, L.; Zuo, W.; Xie, G.; Cai, T.; Fu, W.; Zhang, J.; Wu, W.; Zhang, X.; et al. Autophagy negatively regulates Wnt signalling by promoting Dishevelled degradation. Nat. Cell Biol. 2010, 12, 781-790.
77. Kutikhin, A.G. Role of NOD1/CARD4 and NOD2/CARD15 gene polymorphisms in cancer etiology. Hum. Immunol. 2011, 72, 55-68.
78. Tang, D.; Kang, R.; Cheh, C.W.; Livesey, K.M.; Liang, X.; Schapiro, N.E.; Benschop, R.; Sparvero, L.J.; Amoscato, A.A.; Tracey, K.J.; et al. HMGB1 release and redox regulates autophagy and apoptosis in cancer cells. Oncogene 2010 29, 5299-5310.
79. Livesey, K.; Kang, R.; Vernon, P.; Buchser, W.; Loughran, P.; Watkins, S.C.; Zhang, L.; Manfredi, J.J.; Zeh, H.J.; Li, L.; et al. p53/HMGB1 Complexes Regulate Autophagy and Apoptosis. Cancer Res. 2012, 72, 1996-2005.
80. Scherz-Shouval, R.; Weidberg, H.; Gonen, C.; Wilder, S.; Elazar, Z.; Oren, M. p53-dependent regulation of autophagy protein LC3 supports cancer cell survival under prolonged starvation. Proc. Natl. Acad. Sci. USA 2010, 107, 18511-18516.
81. Morselli, E.; Shen, S.; Ruckenstuhl, C.; Bauer, M.A.; Marino, G.; Galluzzi, L.; Criollo, A.; Michaud, M.; Maiuri, M.C.; Chano, T.; et al. p53 inhibits autophagy by interacting with the human ortholog of yeast Atg17, RB1CC1/FIP200. Cell Cycle 2011, 10, 2763-2769.
82. Kamp, D.W.; Shacter, E.; Weitzman, S.A. Chronic inflammation and cancer: The role of the mitochondria. Oncology (Williston Park) 2011, 25, 400-410,413.
83. Wang, S.; Mintz, A.; Mochizuki, K.; Dorsey, J.F.; Ackermann, J.M.; Alavi, A.; El-Deiry, W.S. Multimodality optical imaging and 18F-FDG uptake in wild-type p53-containing and p53-null human colon tumor xenografts. Cancer Biol. Ther. 2007, 6, 1649-1653.
84. Warburg, O. On the origin of cancer cells. Science 1956, 123, 309-314.
85. Diaz-Ruiz, R.; Rigoulet, M.; Devin, A. The Warburg and Crabtree effects: On the origin of cancer cell energy metabolism and of yeast glucose repression. Biochim. Biophys. Acta 2010, 1807, 568-576.
86. Elstrom, R.L.; Bauer, D.E.; Buzzai, M.; Karnauskas, R.; Harris, M.H.; Plas, D.R.; Zhuang, H.; Cinalli, R.M.; Alavi, A.; Rudin, C.M.; et al. Akt stimulates aerobic glycolysis in cancer cells. Cancer Res. 2004, 64, 3892-3899.
87. Rodriguez-Enriquez, S.; Vital-Gonzalez, P.A.; Flores-Rodriguez, F.L.; Marin-Hernandez, A.; Ruiz-Azuara, L.; Moreno-Sanchez, R. Control of cellular proliferation by modulation of oxidative phosphorylation in human and rodent fast-growing tumor cells. Toxicol. Appl. Pharm. 2006, 215, 208-217.
88. Guppy, M.; Leedman, P.; Zu, X.; Russell, V. Contribution by different fuels and metabolic pathways to the total ATP turnover of proliferating MCF-7 breast cancer cells. Biochem. J. 2002, 364, 309-315.
89. Pasdois, P.; Deveaud, C.; Voisin, P.; Bouchaud, V.; Rigoulet, M.; Beauvoit, B. Contribution of the phosphorylable complex I in the growth phase-dependent respiration of C6 glioma cells in vitro. J. Bioenerg. Biomembr. 2003, 35, 439-450.
90. Marino, G.; Kroemer, G. Ammonia: A diffusible factor released by proliferating cells that induces autophagy. Sci. Signal. 2010, 3, e19.
91. Matoba, S.; Kang, J.G.; Patino, W.D.; Wragg, A.; Boehm, M.; Gavrilova, O.; Hurley, P.J.; Bunz, F.; Hwang, P.M. p53 regulates mitochondrial respiration. Science 2006, 312, 1650-1653.
92. Ke, Q.; Costa, M. Hypoxia-inducible factor-1 (HIF-1). Mol. Pharmacol. 2006, 70, 1469-1480.
93. Semenza, G.L. Targeting HIF-1 for cancer therapy. Nat. Rev. Cancer 2003, 3, 721-732.
94. Cuenda, A.; Rousseau, S. p38 MAP-kinases pathway regulation, function and role in human diseases. Biochim. Biophys. Acta 2007, 1773, 1358-1375.
95. Zarubin, T.; Han, J. Activation and signaling of the p38 MAP kinase pathway. Cell Res. 2005, 15, 11-18.
96. Comes, F.; Matrone, A.; Lastella, P.; Nico, B.; Susca, F.C.; Bagnulo, R.; Ingravallo, G.; Modica, S.; Lo Sasso, G.; Moschetta, A.; et al. A novel cell type-specific role of p38alpha in the control of autophagy and cell death in colorectal cancer cells. Cell Death Differ. 2007, 14, 693-702.
97. Matrone, A.; Grossi, V.; Chiacchiera, F.; Fina, E.; Cappellari, M.; Caringella, A.M.; Di Naro, E.; Loverro, G.; Simone, C. p38alpha is required for ovarian cancer cell metabolism and survival. Int. J. Gynecol. Cancer 2010, 20, 203-211.
98. Chiacchiera, F.; Simone, C. Signal-dependent regulation of gene expression as a target for cancer treatment: inhibiting p38alpha in colorectal tumors. Cancer Lett. 2008, 265, 16-26.
99. Chiacchiera, F.; Simone, C. Inhibition of p38alpha unveils an AMPK-FoxO3A axis linking autophagy to cancer-specific metabolism. Autophagy 2009, 5, 1030-1033.
100. Chiacchiera, F.; Simone, C. The AMPK-FoxO3A axis as a target for cancer treatment. Cell Cycle 2010, 9, 1091-1096.
101. Chiacchiera, F.; Matrone, A.; Ferrari, E.; Ingravallo, G.; Lo Sasso, G.; Murzilli, S.; Petruzzelli, M.; Salvatore, L.; Moschetta, A.; Simone, C.; et al. p38alpha blockade inhibits colorectal cancer growth in vivo by inducing a switch from HIF1alpha-to FoxO-dependent transcription. Cell Death Differ. 2009, 16, 1203-1214.
102. Blouin, C.C.; Page, E.L.; Soucy, G.M.; Richard, D.E. Hypoxic gene activation by lipopolysaccharide in macrophages: Implication of hypoxia-inducible factor 1alpha. Blood 2004, 103, 1124-1130.
103. Hellwig-Burgel, T.; Stiehl, D.P.; Wagner, A.E.; Metzen, E.; Jelkmann, W. Review: Hypoxiainducible factor-1 (HIF-1): A novel transcription factor in immune reactions. J. Interferon Cytokine Res. 2005, 25, 297-310.
104. Kojima, H.; Gu, H.; Nomura, S.; Caldwell, C.C.; Kobata, T.; Carmeliet, P.; Semenza, G.L.; Sitkovsky, M.V. Abnormal B lymphocyte development and autoimmunity in hypoxia-inducible factor 1alpha-deficient chimeric mice. Proc. Natl. Acad. Sci. USA 2002, 99, 2170-2174.
105. Seglen, P.O.; Gordon, P.B. 3-Methyladenine: specific inhibitor of autophagic/lysosomal protein degradation in isolated rat hepatocytes. Proc. Natl. Acad. Sci. USA 1982, 79, 1889-1892.
106. Yamamoto, A.; Tagawa, Y.; Yoshimori, T.; Moriyama, Y.; Masaki, R.; Tashiro, Y. Bafilomycin A1 prevents maturation of autophagic vacuoles by inhibiting fusion between autophagosomes and lysosomes in rat hepatoma cell line, H-4-II-E cells. Cell Struct. Funct. 1998, 23, 33-42.
107. Klionsky, D.J.; Lazar, Z.; Seglen, P.O.; Rubinsztein, D.C. Does bafilomycin A1 block the fusion of autophagosomes with lysosomes? Autophagy 2008, 4, 849-950.
108. Shacka, J.J.; Klocke, B.J.; Roth, K.A. Autophagy, bafilomycin and cell death: The "a-B-cs" of plecomacrolide-induced neuroprotection. Autophagy 2006, 2, 228-230.
109. Petiot, A.; Ogier-Denis, E.; Blommaart, E.F.; Meijer, A.J.; Codogno, P. Distinct classes of phosphatidylinositol 3'-kinases are involved in signaling pathways that control macroautophagy in HT-29 cells. J. Biol. Chem. 2000, 275, 992-998.
110. Yang, Z.J.; Chee, C.E.; Huang, S.; Sinicrope, F. Autophagy modulation for cancer therapy. Cancer Biol. Ther. 2011, 11, 169-176.
111. Li, J.; Hou, N.; Faried, A.; Tsutsumi, S.; Kuwano, H. Inhibition of autophagy augments 5-fluorouracil chemotherapy in human colon cancer in vitro and in vivo model. Eur. J. Cancer 2010, 46, 1900-1909.
112. Xiong, H.Y.; Guo, X.L.; Bu, X.X.; Zhang, S.S.; Ma, N.N.; Song, J.R.; Hu, F.; Tao, S.F.; Sun, K.; Li, R.; et al. Autophagic cell death induced by 5-FU in Bax or PUMA deficient human colon cancer cell. Cancer Lett. 2010, 288, 68-74.
113. Carew, J.S.; Medina, E.C.; Esquivel, J.A., 2nd; Mahalingam, D.; Swords, R.; Kelly, K.; Zhang, H.; Huang, P.; Mita, A.C.; Mita, M.M.; et al. Autophagy inhibition enhances vorinostat-induced apoptosis via ubiquitinated protein accumulation. J. Cell Mol. Med. 2010, 14, 2448-2459.
114. Carew, J.S.; Espitia, C.M.; Esquivel, J.A., 2nd; Mahalingam, D.; Kelly, K.R.; Reddy, G.; Giles, F.J.; Nawrocki, S.T. Lucanthone is a novel inhibitor of autophagy that induces cathepsin D-mediated apoptosis. J. Biol. Chem. 2010, 286, 6602-6613.
115. Kondo, Y.; Kanzawa, T.; Sawaya, R.; Kondo, S. The role of autophagy in cancer development and response to therapy. Nat. Rev. Cancer 2005, 5, 726-734.
116. Boya, P.; Gonzalez-Polo, R.A.; Casares, N.; Perfettini, J.L.; Dessen, P.; Larochette, N.; Metivier, D.; Meley, D.; Souquere, S.; Yoshimori, T.; et al. Inhibition of macroautophagy triggers apoptosis. Mol. Cell Biol. 2005, 25, 1025-1040.
117. Psahoulia, F.H.; Moumtzi, S.; Roberts, M.L.; Sasazuki, T.; Shirasawa, S.; Pintzas, A. Quercetin mediates preferential degradation of oncogenic Ras and causes autophagy in Ha-RAStransformed human colon cells. Carcinogenesis 2007, 28, 1021-1031.
118. Yuk, J.M.; Shin, D.M.; Song, K.S.; Lim, K.; Kim, K.H.; Lee, S.H.; Kim, J.M.; Lee, J.S.; Paik, T.H.; Kim, J.S.; et al. Bacillus calmette-guerin cell wall cytoskeleton enhances colon cancer radiosensitivity through autophagy. Autophagy 2010, 6, 46-60.
119. Kauntz, H.; Bousserouel, S.; Gosse, F.; Raul, F. Silibinin triggers apoptotic signaling pathways and autophagic survival response in human colon adenocarcinoma cells and their derived metastatic cells. Apoptosis 2011, 16, 1042-1053.
120. Nakamura, Y.; Yogosawa, S.; Izutani, Y.; Watanabe, H.; Otsuji, E.; Sakai, T. A combination of indol-3-carbinol and genistein synergistically induces apoptosis in human colon cancer HT-29 cells by inhibiting Akt phosphorylation and progression of autophagy. Mol. Cancer 2009, 8, 100.
121. Villegas, I.; Sanchez-Fidalgo, S.; Alarcon de la Lastra, C. New mechanisms and therapeutic potential of curcumin for colorectal cancer. Mol. Nutr. Food Res. 2008, 52, 1040-1061.
122. Chiacchiera, F.; Simone, C. Signal-dependent control of autophagy-related gene expression. Methods Enzymol. 2009, 453, 305-324.
123. Fernandez de Mattos, S.; Villalonga, P.; Clardy, J.; Lam, E.W. FOXO3a mediates the cytotoxic effects of cisplatin in colon cancer cells. Mol. Cancer Ther. 2008, 7, 3237-3246.
124. Paillas, S.; Boissiere, F.; Bibeau, F.; Denouel, A.; Mollevi, C.; Causse, A.; Denis, V.; Vezzio-Vie, N.; Marzi, L.; Cortijo, C.; et al. Targeting the p38 MAPK pathway inhibits irinotecan resistance in colon adenocarcinoma. Cancer Res. 2011, 71, 1041-1049.
125. Bajbouj, K.; Poehlmann, A.; Kuester, D.; Drewes, T.; Haase, K.; Hartig, R.; Teller, A.; Kliche, S.; Walluscheck, D.; Ivanovska, J.; et al. Identification of phosphorylated p38 as a novel DAPK-interacting partner during TNFalpha-induced apoptosis in colorectal tumor cells. Am. J. Pathol. 2009, 175, 557-570.
126. Lee, M.R.; Dominguez, C. MAP kinase p38 inhibitors: Clinical results and an intimate look at their interactions with p38alpha protein. Curr. Med. Chem. 2005, 12, 2979-2994.
127. Yang, J.C.; Chien, C.T. A new approach for the prevention and treatment of Helicobacter pylori infection via upregulation of autophagy and downregulation of apoptosis. Autophagy 2009, 5, 413-414.
128. Barton, M.K. Daily aspirin reduces colorectal cancer incidence in patients with Lynch syndrome. CA-Cancer J. Clin. 2012, 62, 143-144.
129. Lee, C.S.; McNamara, D.; O'Morain, C.A. Aspirin as a chemoprevention agent for Colorectal cancer. Curr. Drug Metab. 2012, in press.
130. Bosetti, C.; Rosato, V.; Gallus, S.; Cuzick, J.; La Vecchia, C. Aspirin and cancer risk: A quantitative review to 2011. Ann. Oncol. 2012, 23, 403-415.
131. Kmietowicz, Z. Study finds possible role for aspirin as treatment for colon cancer. BMJ 2012, 344, e2988.
132. Din, F.V.; Valanciute, A.; Houde, V.P.; Zibrova, D.; Green, K.A.; Sakamoto, K.; Alessi, D.R.; Dunlop, M.G. Aspirin Inhibits mTOR Signaling, Activates AMP-Activated Protein Kinase, and Induces Autophagy in Colorectal Cancer Cells. Gastroenterology 2012, 142, 1504-1515.