Targeting autophagy in cancer management-strategies and developments

Cancer Management and Research

Volumn 7, Issue , 2015, Pages 291-299

  Ozpolat, Bulent ^a   Benbrook, Doris M ^b  

^a UNIVERSITY OF TEXAS   (United States)

^b UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

Author keywords

Autophagy inhibition; Chemotherapy; Tumor microenvironment

Indexed keywords

BECLIN 1; BEVACIZUMAB; BORTEZOMIB; CAPECITABINE; CARBOPLATIN; CHLOROQUINE; CISPLATIN; DOCETAXEL; ERLOTINIB; ETOPOSIDE; GEMCITABINE; HYDROXYCHLOROQUINE; IMATINIB; MICROTUBULE ASSOCIATED PROTEIN; MICROTUBULE ASSOCIATED PROTEIN 1 LIGHT CHAIN 3; OXALIPLATIN; PACLITAXEL; RAPAMYCIN; SUNITINIB; TEMOZOLOMIDE; UNCLASSIFIED DRUG; VORINOSTAT;

ADVANCED CANCER; AUTOPHAGY; BREAST CANCER; CANCER INHIBITION; CANCER THERAPY; CELL SURVIVAL; COLORECTAL CANCER; DRUG RESPONSE; DRUG TARGETING; GLIOBLASTOMA; HUMAN; KIDNEY CANCER; LEUKEMIA; LUNG CANCER; METASTATIC MELANOMA; MULTIPLE MYELOMA; NONHUMAN; PANCREAS CANCER; PATIENT CARE; PROSTATE CANCER; PROTEIN EXPRESSION; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; SOLID TUMOR; TREATMENT OUTCOME; TUMOR MICROENVIRONMENT; TUMOR PROMOTION;

EID: 84941660367     PISSN: None     EISSN: 11791322     Source Type: Journal    
DOI: 10.2147/CMAR.S34859     Document Type: Review

References (75)

1. Yang Z, Klionsky DJ. Eaten alive: a history of macroautophagy. Nat Cell Biol. 2010;12(9):814-822.
2. Mizushima N, Yoshimori T, Ohsumi Y. The role of Atg proteins in autophagosome formation. Annu Rev Cell Dev Biol. 2011;27: 107-132.
3. Codogno P. Shining light on autophagy. Nat Rev Mol Cell Biol. 2014;15(3):153.
4. Rubinsztein DC, Shpilka T, Elazar Z. Mechanisms of autophagosome biogenesis. Curr Biol. 2012;22(1):R29-R34.
5. Li WW, Li J, Bao JK. Microautophagy: lesser-known self-eating. Cell Mol Life Sci. 2012;69(7):1125-1136.
6. Fortun J, Verrier JD, Go JC, Madorsky I, Dunn WA, Notterpek L. The formation of peripheral myelin protein 22 aggregates is hindered by the enhancement of autophagy and expression of cytoplasmic chaperones. Neurobiol Dis. 2007;25(2):252-265.
7. Ashrafi G, Schwarz TL. The pathways of mitophagy for quality control and clearance of mitochondria. Cell Death Differ. 2013;20(1):31-42.
8. Kondo Y, Kanzawa T, Sawaya R, Kondo S. The role of autophagy in cancer development and response to therapy. Nat Rev Cancer. 2005;5(9):726-734.
9. Kroemer G, Jäättelä M. Lysosomes and autophagy in cell death control. Nat Rev Cancer. 2005;5(11):886-897.
10. Levine B, Kroemer G. Autophagy in the pathogenesis of disease. Cell. 2008;132(1):27-42.
11. Terman A, Gustafsson B, Brunk UT. Autophagy, organelles and ageing. J Pathol. 2007;211(2):134-143.
12. Wu WK, Coffelt SB, Cho CH, et al. The autophagic paradox in cancer therapy. Oncogene. 2012;31(8):939-953.
13. Klionsky DJ, Abdalla FC, Abeliovich H, et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy. 2012;8(4):445-544.
14. Inoki K, Kim J, Guan KL. AMPK and mTOR in cellular energy homeostasis and drug targets. Annu Rev Pharmacol Toxicol. 2012;52: 381-400.
15. Lindmo K, Stenmark H. Regulation of membrane traffic by phosphoinositide 3-kinases. J Cell Sci. 2006;119(Pt 4):605-614.
16. Yoon YH, Cho KS, Hwang JJ, Lee SJ, Choi JA, Koh JY. Induction of lysosomal dilatation, arrested autophagy, and cell death by chloroquine in cultured ARPE-19 cells. Invest Ophthalmol Vis Sci. 2010;51(11): 6030-6037.
17. Popovic D, Dikic I. The molecular basis of selective autophagy. Biochemist. 2012;34:24-30.
18. Ye Y, Shibata Y, Kikkert M, van Voorden S, Wiertz E, Rapoport TA. Recruitment of the p97 ATPase and ubiquitin ligases to the site of retrotranslocation at the endoplasmic reticulum membrane. Proc Natl Acad Sci U S A. 2005;102(40):14132-14138.
19. Wooten MW, Geetha T, Babu JR, et al. Essential role of sequestosome 1/p62 in regulating accumulation of Lys63-ubiquitinated proteins. J Biol Chem. 2008;283(11):6783-6789.
20. Puissant A, Fenouille N, Auberger P. When autophagy meets cancer through p62/SQSTM1. Am J Cancer Res. 2012;2(4):397-413.
21. Spowart JE, Townsend KN, Huwait H, et al. The autophagy protein LC3A correlates with hypoxia and is a prognostic marker of patient survival in clear cell ovarian cancer. J Pathol. 2012;228(4):437-447.
22. Lazova R, Camp RL, Klump V, Siddiqui SF, Amaravadi RK, Pawelek JM. Punctate LC3B expression is a common feature of solid tumors and associated with proliferation, metastasis, and poor outcome. Clin Cancer Res. 2012;18(2):370-379.
23. Zois CE, Giatromanolaki A, Sivridis E, Papaiakovou M, Kainulainen H, Koukourakis MI. “Autophagic flux” in normal mouse tissues: focus on endogenous LC3A processing. Autophagy. 2011;7(11):1371-1378.
24. Giatromanolaki A, Koukourakis MI, Pouliliou S, et al. Overexpression of LC3A autophagy protein in follicular and diffuse large B-cell lymphomas. Hematol Oncol Stem Cell Ther. 2013;6(1):20-25.
25. Hanna RA, Quinsay MN, Orogo AM, Giang K, Rikka S, Gustafsson ÅB. Microtubule-associated protein 1 light chain 3 (LC3) interacts with Bnip3 protein to selectively remove endoplasmic reticulum and mitochondria via autophagy. J Biol Chem. 2012;287(23):19094-19104.
26. Kroemer G, Jäättelä M. Lysosomes and autophagy in cell death control. Nat Rev Cancer. 2005;5(11):886-897.
27. Ogier-Denis E, Codogno P. Autophagy: a barrier or an adaptive response to cancer. Biochim Biophys Acta. 2003;1603(2):113-128.
28. Scott RC, Juhász G, Neufeld TP. Direct induction of autophagy by Atg1 inhibits cell growth and induces apoptotic cell death. Curr Biol. 2007;17(1):1-11.
29. Dalby KN, Tekedereli I, Lopez-Berestein G, Ozpolat B. Targeting the prodeath and prosurvival functions of autophagy as novel therapeutic strategies in cancer. Autophagy. 2010;6(3):322-329.
30. Golstein P, Kroemer G. Cell death by necrosis: towards a molecular definition. Trends Biochem Sci. 2007;32(1):37-43.
31. Edinger AL, Thompson CB. Defective autophagy leads to cancer. Cancer Cell. 2003;4(6):422-424.
32. Tóth S, Nagy K, Pálfia Z, Réz G. Cellular autophagic capacity changes during azaserine-induced tumour progression in the rat pancreas. Up-regulation in all premalignant stages and down-regulation with loss of cycloheximide sensitivity of segregation along with malignant transformation. Cell Tissue Res. 2002;309(3):409-416.
33. Liang XH, Jackson S, Seaman M, et al. Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature. 1999;402(6762): 672-676.
34. Qu X, Yu J, Bhagat G, et al. Promotion of tumorigenesis by heterozygous disruption of the beclin 1 autophagy gene. J Clin Invest. 2003;112(12): 1809-1820.
35. Karantza-Wadsworth V, Patel S, Kravchuk O, et al. Autophagy mitigates metabolic stress and genome damage in mammary tumorigenesis. Genes Dev. 2007;21(13):1621-1635.
36. Saito H, Inazawa J, Saito S, et al. Detailed deletion mapping of chromosome 17q in ovarian and breast cancers: 2-cM region on 17q21.3 often and commonly deleted in tumors. Cancer Res. 1993;53(14): 3382-3385.
37. 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(8):3443-3449.
38. Gao X, Zacharek A, Salkowski A, et al. Loss of heterozygosity of the BRCA1 and other loci on chromosome 17q in human prostate cancer. Cancer Res. 1995;55(5):1002-1005.
39. Petiot A, Ogier-Denis E, Blommaart EF, Meijer AJ, 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(2):992-998.
40. Mizushima N. Methods for monitoring autophagy. Int J Biochem Cell Biol. 2004;36(12):2491-2502.
41. Pattingre S, Tassa A, Qu X, et al. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell. 2005;122(6):927-939.
42. Takacs-Vellai K, Vellai T, Puoti A, et al. Inactivation of the autophagy gene bec-1 triggers apoptotic cell death in C. elegans. Curr Biol. 2005; 15(16):1513-1517.
43. Arico S, Petiot A, Bauvy C, et al. The tumor suppressor PTEN positively regulates macroautophagy by inhibiting the phosphatidylinositol 3-kinase/protein kinase B pathway. J Biol Chem. 2001;276(38): 35243-35246.
44. Takeuchi H, Kondo Y, Fujiwara K, et al. Synergistic augmentation of rapamycin-induced autophagy in malignant glioma cells by phosphatidylinositol 3-kinase/protein kinase B inhibitors. Cancer Res. 2005; 65(8):3336-3346.
45. Pattingre S, Bauvy C, Codogno P. Amino acids interfere with the ERK1/2-dependent control of macroautophagy by controlling the activation of Raf-1 in human colon cancer HT-29 cells. J Biol Chem. 2003;278(19):16667-16674.
46. Fabre C, Carvalho G, Tasdemir E, et al. NF-kappaB inhibition sensitizes to starvation-induced cell death in high-risk myelodysplastic syndrome and acute myeloid leukemia. Oncogene. 2007;26(28):4071-4083.
47. Mavrakis M, Lippincott-Schwartz J, Stratakis CA, Bossis I. Depletion of type IA regulatory subunit (RIalpha) of protein kinase A (PKA) in mammalian cells and tissues activates mTOR and causes autophagic deficiency. Hum Mol Genet. 2006;15(19):2962-2971.
48. Crighton D, Wilkinson S, Ryan KM. DRAM links autophagy to p53 and programmed cell death. Autophagy. 2007;3(1):72-74.
49. Guo JY, Karsli-Uzunbas G, Mathew R, et al. Autophagy suppresses progression of K-ras-induced lung tumors to oncocytomas and maintains lipid homeostasis. Genes Dev. 2013;27(13):1447-1461.
50. Rouschop KM, Wouters BG. Regulation of autophagy through multiple independent hypoxic signaling pathways. Curr Mol Med. 2009;9(4):417-424.
51. Kanzawa T, Germano IM, Komata T, Ito H, Kondo Y, Kondo S. Role of autophagy in temozolomide-induced cytotoxicity for malignant glioma cells. Cell Death Differ. 2004;11(4):448-457.
52. Paglin S, Hollister T, Delohery T, et al. A novel response of cancer cells to radiation involves autophagy and formation of acidic vesicles. Cancer Res. 2001;61(2):439-444.
53. Boya P, González-Polo RA, Casares N, et al. Inhibition of macroautophagy triggers apoptosis. Mol Cell Biol. 2005;25(3):1025-1040.
54. Qadir MA, Kwok B, Dragowska WH, et al. Macroautophagy inhibition sensitizes tamoxifen-resistant breast cancer cells and enhances mitochondrial depolarization. Breast Cancer Res Treat. 2008;112(3): 389-403.
55. Carew JS, Nawrocki ST, Kahue CN, et al. Targeting autophagy augments the anticancer activity of the histone deacetylase inhibitor SAHA to overcome Bcr-Abl-mediated drug resistance. Blood. 2007;110(1): 313-322.
56. Amaravadi RK, Yu D, Lum JJ, et al. Autophagy inhibition enhances therapy-induced apoptosis in a Myc-induced model of lymphoma. J Clin Invest. 2007;117(2):326-336.
57. Apel A, Herr I, Schwarz H, Rodemann HP, Mayer A. Blocked autophagy sensitizes resistant carcinoma cells to radiation therapy. Cancer Res. 2008;68(5):1485-1494.
58. Abedin MJ, Wang D, McDonnell MA, Lehmann U, Kelekar A. Autophagy delays apoptotic death in breast cancer cells following DNA damage. Cell Death Differ. 2007;14(3):500-510.
59. Katayama M, Kawaguchi T, Berger MS, Pieper RO. DNA damaging agent-induced autophagy produces a cytoprotective adenosine triphosphate surge in malignant glioma cells. Cell Death Differ. 2007;14(3): 548-558.
60. Lu Z, Luo RZ, Lu Y, et al. The tumor suppressor gene ARHI regulates autophagy and tumor dormancy in human ovarian cancer cells. J Clin Invest. 2008;118(12):3917-3929.
61. Guo JY, Chen HY, Mathew R, et al. Activated Ras requires autophagy to maintain oxidative metabolism and tumorigenesis. Genes Dev. 2011;25(5):460-470.
62. Rangwala R, Leone R, Chang YC, et al. Phase I trial of hydroxychloroquine with dose-intense temozolomide in patients with advanced solid tumors and melanoma. Autophagy. 2014;10(8):1369-1379.
63. Mahalingam D, Mita M, Sarantopoulos J, et al. Combined autophagy and HDAC inhibition: a phase I safety, tolerability, pharmacokinetic, and pharmacodynamic analysis of hydroxychloroquine in combination with the HDAC inhibitor vorinostat in patients with advanced solid tumors. Autophagy. 2014;10(8):1403-1414.
64. Vogl DT, Stadtmauer EA, Tan KS, et al. Combined autophagy and proteasome inhibition: a phase 1 trial of hydroxychloroquine and bortezomib in patients with relapsed/refractory myeloma. Autophagy. 2014;10(8):1380-1390.
65. Rangwala R, Chang YC, Hu J, et al. Combined MTOR and autophagy inhibition: phase I trial of hydroxychloroquine and temsirolimus in patients with advanced solid tumors and melanoma. Autophagy. 2014;10(8):1391-1402.
66. Rosenfeld MR, Ye X, Supko JG, et al. A phase I/II trial of hydroxychloroquine in conjunction with radiation therapy and concurrent and adjuvant temozolomide in patients with newly diagnosed glioblastoma multiforme. Autophagy. 2014;10(8):1359-1368.
67. Sotelo J, Briceño E, López-González MA. Adding chloroquine to conventional treatment for glioblastoma multiforme: a randomized, double-blind, placebo-controlled trial. Ann Intern Med. 2006;144(5): 337-343.
68. Rojas-Puentes LL, Gonzalez-Pinedo M, Crismatt A, et al. Phase II randomized, double-blind, placebo-controlled study of whole-brain irradiation with concomitant chloroquine for brain metastases. Radiat Oncol. 2013;8:209.
69. Barnard RA, Wittenburg LA, Amaravadi RK, Gustafson DL, Thorburn A, Thamm DH. Phase I clinical trial and pharmacodynamic evaluation of combination hydroxychloroquine and doxorubicin treatment in pet dogs treated for spontaneously occurring lymphoma. Autophagy. 2014;10(8):1415-1425.
70. Jung CH, Ro SH, Cao J, Otto NM, Kim DH. mTOR regulation of autophagy. FEBS Lett. 2010;584(7):1287-1295.
71. Xie X, White EP, Mehnert JM. Coordinate autophagy and mTOR pathway inhibition enhances cell death in melanoma. PLoS One. 2013;8(1):e55096.
72. Akar U, Chaves-Reyez A, Barria M, et al. Silencing of Bcl-2 expression by small interfering RNA induces autophagic cell death in MCF-7 breast cancer cells. Autophagy. 2008;4(5):669-679.
73. Tekedereli I, Alpay SN, Akar U, et al. Therapeutic silencing of Bcl-2 by systemically administered siRNA nanotherapeutics inhibits tumor growth by autophagy and apoptosis and enhances the efficacy of chemotherapy in orthotopic xenograft models of ER (-) and ER (+) breast cancer. Mol Ther Nucleic Acids. 2013;2:e121.
74. Ozpolat B, Akar U, Mehta K, Lopez-Berestein G. PKC delta and tissue transglutaminase are novel inhibitors of autophagy in pancreatic cancer cells. Autophagy. 2007;3(5):480-483.
75. Wu WK, Sakamoto KM, Milani M, et al. Macroautophagy modulates cellular response to proteasome inhibitors in cancer therapy. Drug Resist Updat. 2010;13(3):87-92.