LC3A-positive light microscopy detected patterns of autophagy and prognosis in operable breast carcinomas

American Journal of Pathology

Volumn 176, Issue 5, 2010, Pages 2477-2489

  Sivridis, Efthimios ^a   Koukourakis, Michael I ^a   Zois, Christos E ^a   Ledaki, Ioanna ^b   Ferguson, David J P ^b   Harris, Adrian L ^b   Gatter, Kevin C ^b   Giatromanolaki, Alexandra ^a  

^a DEMOCRITUS UNIVERSITY OF THRACE   (Greece)

^b JOHN RADCLIFFE HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ESTROGEN RECEPTOR; MICROTUBULE ASSOCIATED PROTEIN 1 LIGHT CHAIN 3; PROGESTERONE RECEPTOR; PROTEIN ANTIBODY; THAPSIGARGIN; UNCLASSIFIED DRUG;

ANOXIA; ARTICLE; AUTOPHAGY; BREAST CARCINOMA; CANCER CELL CULTURE; CANCER GRADING; CELL STRUCTURE; CELL VACUOLE; COLON TUMOR; CONTROLLED STUDY; CYTOPLASM; ELECTRON MICROSCOPY; EPITHELIUM TUMOR; FEMALE; GENE EXPRESSION; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MALE; MICROSCOPY; PRIORITY JOURNAL; PROGNOSIS; TUMOR VOLUME; XENOGRAFT;

EID: 77952040472     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.2353/ajpath.2010.090049     Document Type: Article

References (65)

1. Giatromanolaki A, Sivridis E, Koukourakis MI: Tumour angiogenesis: vascular growth and survival. APMIS 2004, 112:431-440
2. Jain RK: Molecular regulation of vessel maturation. Nat Med 2003, 9:685-693
3. Vaupel P, Thews O, Hoeckel M: Treatment resistance of solid tumors: role of hypoxia and anemia. Med Oncol 2001, 18:243-259
4. Harris AL: Hypoxia - a key regulatory factor in tumour growth. Nat Rev Cancer 2002, 2:38-47
5. Izuishi K, Kato K, Ogura T, Kinoshita T, Esumi H: Remarkable tolerance of tumor cells to nutrient deprivation: possible new biochemical target for cancer therapy. Cancer Res 2000, 60:6201-6207
6. Esumi H, Izuishi K, Kato K, Hashimoto K, Kurashima Y, Kishimoto A, Ogura T, Ozawa T: Hypoxia and nitric oxide treatment confer tolerance to glucose starvation in a 5.-AMP-activated protein kinase-dependent manner. J Biol Chem 2002, 277:32 791-798
7. Shintani T, Klionsky DJ: Autophagy in health and disease: a double-edged sword. Science 2004, 306:990-995
8. Mizushima N, Ohsumi Y, Yoshimori T: Autophagosome formation in mammalian cells. Cell Struct Funct 2002, 27:421-429
9. Yorimitsu T, Klionsky DJ: Autophagy: molecular machinery for self eating. Cell Death Differ 2005, 12:1542-1552
10. Locopo N, Fanelli M, Gasparini G: Clinical significance of angiogenic factors in breast cancer. Breast Cancer Res Treat 1998, 52:159-173
11. Giatromanolaki A, Harris AL: Tumour hypoxia, hypoxia signaling pathways and hypoxia inducible factor expression in human cancer. Anticancer Res 2001, 21:4317-4324
12. Koukourakis MI, Manolas C, Minopoulos G, Giatromanolaki A, Sivridis E: Angiogenesis relates to estrogen receptor negativity, c-erbB-2 overexpression and early relapse in node-negative ductal carcinoma of the breast. Int J Surg Pathol 2003, 11:29-34
13. Giatromanolaki A, Sivridis E, Simopoulos C, Polychronidis A, Gatter KC, Harris AL, Koukourakis MI: Differential assessment of angiogenic activity and of vascular survival ability (VSA) in breast cancer. Clin Exp Metastasis 2002, 19:673-679 (Pubitemid 36092262)
14. Airley RE, Mobasheri A: Hypoxic regulation of glucose transport, anaerobic metabolism and angiogenesis in cancer: novel pathways and targets for anticancer therapeutics. Chemotherapy 2007, 53:233-256
15. Koukourakis MI, Pitiakoudis M, Giatromanolaki A, Tsarouha A, Polychronidis A, Sivridis E, Simopoulos C: Oxygen and glucose consumption in gastrointestinal adenocarcinomas: correlation with markers of hypoxia, acidity and anaerobic glycolysis. Cancer Sci 2006, 97:1056-1060
16. Bursch W, Ellinger A, Gerner C, Fröhwein U, Schulte-Hermann R: Programmed cell death (PCD). Apoptosis, autophagic PCD, or others? Ann N Y Acad Sci 2000, 926:1-12
17. Viktorsson K, Lewensohn R, Zhivotovsky B: Apoptotic pathways and therapy resistance in human malignancies. Adv Cancer Res 2005, 94:143-196 (Pubitemid 41213078)
18. Martinet W, De Meyer GRY, Andries L, Herman AG, Kockx MM: In situ detection of starvation-induced autophagy. J Histochem Cytochem 2006, 54:85-96
19. Bhattacharyya TK, Buttler DG: Ultrastructure of the adrenocortical homologue in dexamethasone-treated eels. J Anat 1980, 130:323-332
20. Fedorko M: Effect of chloroquine on morphology of cytoplasmic granules in maturing human leukocytes - an ultrastructural study. J Clin Investigation 1967, 12:1932-1942
21. Hickman S, Neufeld EF: A hypothesis for I-cell disease: defective hydrolases that do not enter lysosomes. Biochem Biophys Res Comm 1972, 49:992-999
22. Zhong H, De Marzo AM, Laughner E, Lim M, Hilton DA, Zagzag D, Buechler P, Isaacs WB, Semenza GL, Simons JW: Overexpression of hypoxia-inducible factor 1alpha in common human cancers and their metastases. Cancer Res 1999, 59:5830-5835
23. Koong AC, Mehta VK, Le QT, Fisher GA, Terris DJ, Brown JM, Bastidas AJ, Vierra M: Pancreatic tumors show high levels of hypoxia. Int J Radiat Oncol Biol Phys 2000, 48:919-922
24. Buchler P, Reber HA, Lavey RS, Tomlinson J, Büchler MW, Friess H, Hines OJ: Tumor hypoxia correlates with metastatic tumor growth of pancreatic cancer in an orthotopic murine model. J Surg Res 2004, 120:295-303 (Pubitemid 38834199)
25. Kumar R, Vadlamudi RK, Adam L: Apoptosis in mammary gland and cancer. Endocr Relat Cancer 2000, 7:257-269
26. Fujii S, Mitsunaga S, Yamazaki M, Hasebe T, Ishii G, Kojima M, Kinoshita T, Ueno T, Esumi H, Ochiai A: Autophagy is activated in pancreatic cancer cells and correlates with poor patient outcome. Cancer Sci 2008, 99:1813-1819
27. He H, Dang Y, Dai F, Guo Z, Wu J, She X, Pei Y, Chen Y, Ling W, Wu C, Zhao S, Liu JO, Yu L: Post-translational modifications of three members of the human MAP1LC3 family and detection of a novel type of modification for MAP1LC3B. J Biol Chem 2003, 278:29278-29287
28. Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T, Kominami E, Ohsumi Y, Yoshimori T: LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 2000, 19:5720-5728
29. Muss HB, Thor AD, Berry DA, Kute T, Liu ET, Koerner F, Cirrincione CT, Budman DR, Wood WC, Barcos M, Henderson IC: c-erbB-2 expression and response to adjuvant therapy in women with nodepositive early breast cancer. N Engl J Med 1994, 330:1260-1266
30. Laemmli UK: Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227:680-685
31. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ: Protein measurement with the Folin phenol reagent. J Biol Chem 1951, 193:265-275
32. Li JL, Sainson RC, Shi W, Leek R, Harrington LS, Preusser M, Biswas S, Turley H, Heikamp E, Hainfellner JA, Harris AL: Delta-like 4 North ligand regulates tumor angiogenesis, improves tumor vascular function, and promotes tumor growth in vivo. Cancer Res 2007, 67:11244-11253
33. Ling YM, Shaw MH, Ayala C, Coppens I, Taylor GA, Ferguson DJP, Yap GS: Vacuolar and plasma membrane stripping and autophagic elimination of Toxoplasma gondii in primed effector macrophages. J Exp Med 2006, 203:2063-2071
34. Folkman J: What is the evidence that tumors are angiogenesis-dependent? J Natl Cancer Inst 1990, 82:4-6
35. Weinhouse S: The Warburg hypothesis fifty years later. Z Krebsforsch Klin Onkol Cancer Res Clin Oncol 1976, 87:115-126
36. DeBerardinis RJ, Lum JJ, Hatzivassiliou G, Thompson CG: The biology of cancer. Metabolic reprogramming fuels cell growth and proliferation. Cell Metab 2008, 7:11-20
37. Ganapathy V, Thangaraju M, Prasad PD: Nutrient transporters in cancer: relevance to Warburg hypothesis and beyond. Pharmacol Ther 2009, 121:29-40
38. Yen W-L, Klionsky DJ: Atg27 is a second transmembrane cycling protein. Autophagy 2007, 3:254-256
39. Blommaart EFC, Luiken JJFP, Meijer AJ: Autophagic proteolysis: control and specifity. Histochem J 1997, 29:365-385
40. Kissová I, Deffieu M, Manon S, Camougrand N: Uth1p is involved in the autophagic degradation of mitochondria. J Biol Chem 2004, 279:39068-39074
41. Mortimore GE, Poso AR: Intracellular protein catabolism and its control during nutrient deprivation and supply. Annu Rev Nutr 1987, 7:539-564
42. Martinet W, De Meyer GRY, Andries L, Herman AG, Kockx MM: Detection of autophagy in tissue by standard immunohistochemistry. Autophagy 2006, 2:55-57
43. Mizushima N: Methods for monitoring Autophagy. Int J Biochem Cell Biol 2004, 36:2491-2502
44. Motyl T, Gajkowska B, Zarzynska J, Gajewska M, Lamparska-Przybysz M: Apoptosis and autophagy in mammary gland remodelling and breast cancer chemotherapy. J Physiol Pharmacol 2006, 57[Supp 7]:17-32 (Pubitemid 46553587)
45. Reggiori F, Tucker KA, Stromhaug PE, Klionsky DJ: The Atg1-Atg13 complex regulates Atg9 and Atg23 retrieval transport from the preautophagosomal structure. Dev Cell 2004, 6:79-90
46. Webber JL, Young ARJ, Tooze SA: Atg9 trafficking in mammalian cells. Autophagy 2007, 3:54-56
47. He C, Klionsky DJ: Atg9 trafficking in autophagy-related pathways. Autophagy 2007, 3:271-274
48. Legakis JE, Yen Wei-Lien, Klionsky DJ: A cycling protein complex required for selective autophagy. Autophagy 2007, 3:422-432
49. Kuma A, Matsui M, Mizushima N: LC3, an autophagosome marker, can be incorporated into protein aggregates independent of autophagy. Caution in the interpretation of LC3 localization. Autophagy 2007, 3:323-328
50. Marx J: Autophagy: is it cancer's friend or foe? Science 2006, 312:1160-1161
51. Furuya D, Tsuji N, Yagihashi A, Watanabe N: Beclin 1 augmented cis-diamminedichloroplatinum induced apoptosis via enhancing caspase-9 activity. Exp Cell Res 2005, 307:26-40
52. Daniel F, Legrand A, Pessayre D, Vadrot N, Descatoire V, Bernuau D: Partial Beclin 1 silencing aggravates doxorubicin- and Fas-induced apoptosis in HepG2 cells. World J Gastroenterol 2006, 12:2895-2900
53. Ahn CH, Jeong EG, Lee JW, Kim SH, Yoo NJ, Lee SH: Expression of beclin-1, an autophagy-related protein, in gastric and colorectal cancers. APMIS 2007, 115:1344-1349
54. Baehrecke EH: Autophagy: dual roles in life and death? Nat Rev Mol Cell Biol 2005, 6:505-510
55. Edinger AL, Thompson CB: Death by design: apoptosis, necrosis and autophagy. Curr Opin Cell Biol 2004, 16:663-669
56. 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
57. Liang XH, Yu J, Brown K, Levine B: Beclin 1 contains a leucine-rich nuclear export signal that is required for its autophagy and tumor suppressor function. Cancer Res 2001, 61:3443-3449
58. Liang XH, Kleeman LK, Jiang HH, Gordon G, Goldman JE, Berry G, Herman B, Levine B: Protection against fatal Sindbis virus encephalitis by beclin, a novel Bcl-2-interecting protein. J Virol 1998, 72:8586-8596
59. Liang XH, Jackson S, Seaman M, Brown K, Kempkes B, Hibshoosh H, Levin B: Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature 1999, 402:672-676
60. Miracco C, Cosci E, Oliveri G, Luzi P, Pacenti L, Monciatti I, Mannucci S, De Nisi MC, Toscano M, Malagnino V, Falzarano SM, Pirtoli L, Tosi P: Protein and mRNA expression of autophagy gene Beclin 1 in human brain tumours. Int J Oncol 2007, 30:429-436
61. DiPaola RS, Dvorzhinski D, Thalasila A, Garikapaty V, Doram D, May M, Bray K, Mathew R, Beaudoin B, Karp C, Stein M, Foran DJ, White E: Therapeutic starvation and autophagy in prostate cancer: a new paradigm for targeting metabolism in cancer therapy. Prostate 2008, 68:1743-1752
62. Novikoff AB, Shin WY: Endoplasmic reticulum and autophagy in rat hepatocytes. Proc Natl Acad Sci U S A 1978, 75:5039-5042
63. Miyata S, Takemura G, Kawase Y, Li Y, Okada H, Maruyama R, Ushikoshi H, Esaki M, Kanamori H, Li L, Misao Y, Tezuka A, Toyo-Oka T, Minatoguchi S, Fujiwara T, Fujiwara H: Autophagic cardiomyocyte death in cardiomyopathic hamsters and its prevention by granulocyte colony-stimulating factor. Am J Pathol 2006, 168:386-397
64. Vincent RA Jr, Spicer SS: Giant dense bodies in fibroblasts cultured from beige mice with Chediak-Higashi syndrome. Am J Pathol 1981, 105:270-278
65. Klionsky DJ: The molecular machinery of autophagy. Unanswered questions J Cell Sci 2005, 118:7-18