Attacking breast cancer at the preinvasion stage by targeting autophagy

Women's Health

Volumn 9, Issue 2, 2013, Pages 157-170

  Espina, Virginia ^a   Wysolmerski, John ^b   Edmiston, Kirsten ^c   Liotta, Lance A ^a  

^a GEORGE MASON UNIVERSITY   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c INOVA FAIRFAX HOSPITAL   (United States)

Author keywords

autophagy; breast; calcium; chemoprevention; chloroquine; DCIS; microenvironment; PMCA2; preinvasive; vitamin D

Indexed keywords

AUTOPHAGY PROTEIN 5; CALCITRIOL; CALCIUM; CHLOROQUINE; CYCLINE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; KI 67 ANTIGEN; MAMMALIAN TARGET OF RAPAMYCIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B;

ADJUVANT THERAPY; ANOIKIS; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; AUTOPHAGY; CALCIUM CELL LEVEL; CANCER CELL; CANCER RADIOTHERAPY; CANCER STEM CELL; CELL HYPOXIA; CELL PROLIFERATION; CELL SURVIVAL; DRUG DOSE COMPARISON; DRUG EFFICACY; DRUG SAFETY; DRUG TARGETING; HUMAN; IMMUNOHISTOCHEMISTRY; INTRADUCTAL CARCINOMA; MACROAUTOPHAGY; MASTECTOMY; METABOLIC STRESS; NONHUMAN; PARTIAL MASTECTOMY; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); REVIEW; TUMOR VOLUME;

AUTOPHAGY; BREAST NEOPLASMS; CARCINOMA IN SITU; CELL LINE, TUMOR; FEMALE; HUMANS; NEOPLASM STAGING; NEOPLASTIC STEM CELLS; STEM CELL NICHE;

EID: 84874865711     PISSN: 17455057     EISSN: 17455065     Source Type: Journal    
DOI: 10.2217/whe.13.5     Document Type: Review

References (94)

1. Sgroi DC. Preinvasive breast cancer. Ann. Rev. Pathol. 5, 193-221 (2010).
2. Boecker W. Preneoplasia of the Breast. Elsevier, Munich, Germany (2006).
3. Claus EB, Chu P, Howe CL et al. Pathobiologic findings in DCIS of the breast: morphologic features, angiogenesis, HER-2/neu and hormone receptors. Exp. Mol. Pathol. 70(3), 303-316 (2001).
4. Hu M, Yao J, Carroll DK et al. Regulation of in situ to invasive breast carcinoma transition. Cancer Cell 13(5), 394-406 (2008).
5. Page DL, Dupont WD, Rogers LW, Landenberger M. Intraductal carcinoma of the breast: follow-up after biopsy only. Cancer 49(4), 751-758 (1982).
6. Berman HK, Gauthier ML, Tlsty TD. Premalignant breast neoplasia: a paradigm of interlesional and intralesional molecular heterogeneity and its biological and clinical ramifications. Cancer Prev. Res. (Phila.) 3(5), 579-587 (2010).
7. Betsill WL Jr, Rosen PP, Lieberman PH, Robbins GF. Intraductal carcinoma. Longterm follow-up after treatment by biopsy alone. JAMA 239(18), 1863-1867 (1978).
8. Lagios MD. Heterogeneity of duct carcinoma in situ (DCIS): relationship of grade and subtype analysis to local recurrence and risk of invasive transformation. Cancer Lett. 90(1), 97-102 (1995).
9. Castro NP, Osorio CA, Torres C et al. Evidence that molecular changes in cells occur before morphological alterations during the progression of breast ductal carcinoma. Breast Cancer Res. 10(5), R87 (2008).
10. Collins LC, Tamimi RM, Baer HJ et al. Outcome of patients with ductal carcinoma in situ untreated after diagnostic biopsy: results from the Nurses' Health Study. Cancer 103(9), 1778-1784 (2005).
11. Espina V, Liotta LA. What is the malignant nature of human ductal carcinoma in situ? Nat. Rev. Cancer 11(1), 68-75 (2010).
12. Espina V, Mariani BD, Gallagher RI et al. Malignant precursor cells pre-exist in human breast DCIS and require autophagy for survival. PLoS ONE 5(4), e10240 (2010).
13. Ma XJ, Dahiya S, Richardson E, Erlander M, Sgroi DC. Gene expression profiling of the tumor microenvironment during breast cancer progression. Breast Cancer Res. 11(1), R7 (2009).
14. Ma XJ, Salunga R, Tuggle JT et al. Gene expression profiles of human breast cancer progression. Proc. Natl Acad. Sci. USA 100(10), 5974-5979 (2003).
15. Kelloff GJ, Sigman CC. Assessing intraepithelial neoplasia and drug safety in cancer-preventive drug development. Nat. Rev. Cancer 7(7), 508-518 (2007).
16. O'Shaughnessy JA, Kelloff GJ, Gordon GB et al. Treatment and prevention of intraepithelial neoplasia: an important target for accelerated new agent development. Clin. Cancer Res. 8(2), 314-346 (2002).
17. Dickson RB, Johnson MD, Maemura M, Low J. Anti-invasion drugs. Breast Cancer Res. Treat 38(1), 121-132 (1996).
18. Seton-Rogers S. Metastasis: opposing forces in invasion. Nat. Rev. Cancer 11(9), 624-625 (2011).
19. Bussolati G, Bongiovanni M, Cassoni P, Sapino A. Assessment of necrosis and hypoxia in ductal carcinoma in situ of the breast: basis for a new classification. Virchows Arch. 437(4), 360-364 (2000).
20. Tavassoli F. Intraductal proliferative lesions. In: Tumors of the Breast and Female Genital Organs. Tavassoli F, Devilee P (Eds). IARC-Press, Lyon, 63-73 (2003).
21. Liotta LA, Tryggvason K, Garbisa S et al. Metastatic potential correlates with enzymatic degradation of basement membrane collagen. Nature 284(5751), 67-68 (1980).
22. Mayr NA, Staples JJ, Robinson RA, Vanmetre JE, Hussey DH. Morphometric studies in intraductal breast carcinoma using computerized image analysis. Cancer 67(11), 2805-2812 (1991).
23. Pinder SE. Ductal carcinoma in situ (DCIS): pathological features, differential diagnosis, prognostic factors and specimen evaluation. Mod. Pathol. 23(Suppl. 2), S8-S13 (2010).
24. Lyng H, Sundfor K, Trope C, Rofstad EK. Oxygen tension and vascular density in human cervix carcinoma. Br. J. Cancer 74(10), 1559-1563 (1996).
25. Vaupel P, Kallinowski F, Okunieff P. Blood flow, oxygen and nutrient supply, and metabolic microenvironment of human tumors: a review. Cancer Res. 49(23), 6449-6465 (1989).
26. Boyer MJ, Barnard M, Hedley DW, Tannock IF. Regulation of intracellular pH in subpopulations of cells derived from spheroids and solid tumours. Br. J. Cancer 68(5), 890-897 (1993).
27. Tannock IF, Kopelyan I. Influence of glucose concentration on growth and formation of necrosis in spheroids derived from a human bladder cancer cell line. Cancer Res. 46(6), 3105-3110 (1986).
28. Hockel M, Vaupel P. Tumor hypoxia: definitions and current clinical, biologic, and molecular aspects. J. Natl Cancer Inst. 93(4), 266-276 (2001).
29. Pirnia F, Pawlak M, Thallinger GG et al. Novel functional profiling approach combining reverse phase protein microarrays and human 3-D ex vivo tissue cultures: expression of apoptosis-related proteins in human colon cancer. Proteomics 9(13), 3535-3548 (2009).
30. Bindra RS, Glazer PM. Genetic instability and the tumor microenvironment: towards the concept of microenvironment-induced mutagenesis. Mutat. Res. 569(1-2), 75-85 (2005).
31. Li CY, Little JB, Hu K et al. Persistent genetic instability in cancer cells induced by non-DNA-damaging stress exposures. Cancer Res. 61(2), 428-432 (2001).
32. Sendoel A, Kohler I, Fellmann C, Lowe SW, Hengartner MO. HIF-1 antagonizes p53-mediated apoptosis through a secreted neuronal tyrosinase. Nature 465(7298), 577-583 (2010).
33. Gatenby RA, Smallbone K, Maini PK et al. Cellular adaptations to hypoxia and acidosis during somatic evolution of breast cancer. Br. J. Cancer 97(5), 646-653 (2007).
34. Gauthier ML, Berman HK, Miller C et al. Abrogated response to cellular stress identifies DCIS associated with subsequent tumor events and defines basal-like breast tumors. Cancer Cell 12(5), 479-491 (2007).
35. Yu F, White SB, Zhao Q, Lee FS. HIF-1alpha binding to VHL is regulated by stimulussensitive proline hydroxylation. Proc. Natl Acad. Sci. USA 98(17), 9630-9635 (2001).
36. Mihaylova VT, Bindra RS, Yuan J et al. Decreased expression of the DNA mismatch repair gene Mlh1 under hypoxic stress in mammalian cells. Mol. Cell. Biol. 23(9), 3265-3273 (2003).
37. Young SD, Hill RP. Effects of reoxygenation on cells from hypoxic regions of solid tumors: anticancer drug sensitivity and metastatic potential. J. Natl Cancer Inst. 82(5), 371-380 (1990).
38. Young SD, Marshall RS, Hill RP. Hypoxia induces DNA overreplication and enhances metastatic potential of murine tumor cells. Proc. Natl Acad. Sci. USA 85(24), 9533-9537 (1988).
39. Cuvier C, Jang A, Hill RP. Exposure to hypoxia, glucose starvation and acidosis: effect on invasive capacity of murine tumor cells and correlation with cathepsin (L + B) secretion. Clin. Exp. Metastasis 15(1), 19-25 (1997).
40. Mathew R, Karantza-Wadsworth V, White E. Role of autophagy in cancer. Nat. Rev. Cancer 7(12), 961-967 (2007).
41. Gong C, Bauvy C, Tonelli G et al. Beclin 1 and autophagy are required for the tumorigenicity of breast cancer stem-like/progenitor cells. Oncogene doi:10.1038/onc.2012.252 (2012) (Epub ahead of print).
42. Guo JY, Chen HY, Mathew R et al. Activated Ras requires autophagy to maintain oxidative metabolism and tumorigenesis. Genes Dev. 25(5), 460-470 (2011).
43. Levine B, Mizushima N, Virgin HW. Autophagy in immunity and inflammation. Nature 469(7330), 323-335 (2011).
44. Rabinowitz JD, White E. Autophagy and metabolism. Science 330(6009), 1344-1348 (2010).
45. Klionsky DJ, Abeliovich H, Agostinis P et al. Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 4(2), 151-175 (2008).
46. Li H, Zhu R, Wang L et al. PIK3CA mutations mostly begin to develop in ductal carcinoma of the breast. Exp. Mol. Pathol. 88(1), 150-155 (2010).
47. Yu L, McPhee CK, Zheng L et al. Termination of autophagy and reformation of lysosomes regulated by mTOR. Nature 465(7300), 942-946 (2010).
48. Qu X, Zou Z, Sun Q et al. Autophagy genedependent clearance of apoptotic cells during embryonic development. Cell 128(5), 931-946 (2007).
49. Bellodi C, Lidonnici MR, Hamilton A et al. Targeting autophagy potentiates tyrosine kinase inhibitor-induced cell death in Philadelphia chromosome-positive cells, including primary CML stem cells. J. Clin. Invest. 119(5), 1109-1123 (2009).
50. Cook KL, Shajahan AN, Warri A et al. Glucose-regulated protein 78 controls cross-talk between apoptosis and autophagy to determine antiestrogen responsiveness. Cancer Res. 72(13), 3337-3349 (2012).
51. Schoenlein PV, Periyasamy-Thandavan S, Samaddar JS, Jackson WH, Barrett JT. Autophagy facilitates the progression of ERalpha-positive breast cancer cells to antiestrogen resistance. Autophagy 5(3), 400-403 (2009).
52. Vazquez-Martin A, Oliveras-Ferraros C, Menendez JA. Autophagy facilitates the development of breast cancer resistance to the anti-HER2 monoclonal antibody trastuzumab. PLoS ONE 4(7), e6251 (2009).
53. Fung C, Lock R, Gao S, Salas E, Debnath J. Induction of autophagy during extracellular matrix detachment promotes cell survival. Mol. Biol. Cell 19(3), 797-806 (2008).
54. Gao W, Ding WX, Stolz DB, Yin XM. Induction of macroautophagy by exogenously introduced calcium. Autophagy 4(6), 754-761 (2008).
55. Augustijns P, Geusens P, Verbeke N. Chloroquine levels in blood during chronic treatment of patients with rheumatoid arthritis. Eur. J. Clin. Pharmacol. 42(4), 429-433 (1992).
56. Ducharme J, Farinotti R. Clinical pharmacokinetics and metabolism of chloroquine. Focus on recent advancements. Clin. Pharmacokinet. 31(4), 257-274 (1996).
57. Rahim R, Strobl JS. Hydroxychloroquine, chloroquine, and all-trans retinoic acid regulate growth, survival, and histone acetylation in breast cancer cells. Anticancer Drugs 20(8), 736-745. (2009).
58. Savarino A, Lucia MB, Giordano F, Cauda R. Risks and benefits of chloroquine use in anticancer strategies. Lancet Oncol. 7(10), 792-793 (2006).
59. White E, DiPaola RS. The double-edged sword of autophagy modulation in cancer. Clin. Cancer Res. 15(17), 5308-5316 (2009).
60. Loehberg CR, Thompson T, Kastan MB et al. Ataxia telangiectasia-mutated and p53 are potential mediators of chloroquine-induced resistance to mammary carcinogenesis. Cancer Res. 67(24), 12026-12033 (2007).
61. Samaddar JS, Gaddy VT, Duplantier J et al. A role for macroautophagy in protection against 4-hydroxytamoxifen-induced cell death and the development of antiestrogen resistance. Mol. Cancer Ther. 7(9), 2977-2987 (2008).
62. Amaravadi RK, Yu D, Lum JJ et al. Autophagy inhibition enhances therapy-induced apoptosis in a Myc-induced model of lymphoma. J. Clin. Invest. 117(2), 326-336 (2007).
63. Maclean KH, Dorsey FC, Cleveland JL, Kastan MB. Targeting lysosomal degradation induces p53-dependent cell death and prevents cancer in mouse models of lymphomagenesis. J. Clin. Invest. 118(1), 79-88 (2008).
64. Ma XH, Piao S, Wang D et al. Measurements of tumor cell autophagy predict invasiveness, resistance to chemotherapy, and survival in melanoma. Clin. Cancer Res. 17(10), 3478-3489 (2011).
65. Maddodi N, Huang W, Havighurst T et al. Induction of autophagy and inhibition of melanoma growth in vitro and in vivo by hyperactivation of oncogenic BRAF. J. Invest. Dermatol. 130(6), 1657-1667 (2010).
66. Mirzoeva OK, Hann B, Hom YK et al. Autophagy suppression promotes apoptotic cell death in response to inhibition of the PI3K-mTOR pathway in pancreatic adenocarcinoma. J. Mol. Med. 89(9), 877-889 (2011).
67. Yang S, Wang X, Contino G et al. Pancreatic cancers require autophagy for tumor growth. Genes Dev. 25(7), 717-729 (2011).
68. Briceno E, Calderon A, Sotelo J. Institutional experience with chloroquine as an adjuvant to the therapy for glioblastoma multiforme. Surg. Neurol. 67(4), 388-391 (2007).
69. van Osdol W, Fujimori K, Weinstein JN. An analysis of monoclonal antibody distribution in microscopic tumor nodules: consequences of a 'binding site barrier'. Cancer Res. 51(18), 4776-4784 (1991).
70. Evans A, Pinder S, Wilson R et al. Ductal carcinoma in situ of the breast: correlation between mammographic and pathologic findings. AJR Am. J. Roentgenol. 162(6), 1307-1311 (1994).
71. Holland R, Hendriks JH, Vebeek AL, Mravunac M, Schuurmans Stekhoven JH. Extent, distribution, and mammographic/histological correlations of breast ductal carcinoma in situ. Lancet 335(8688), 519-522 (1990).
72. Hermann G, Keller RJ, Drossman S et al. Mammographic pattern of microcalcifications in the preoperative diagnosis of comedo ductal carcinoma in situ: histopathologic correlation. Can. Assoc. Radiol. J. 50(4), 235-240 (1999).
73. Foschini MP, Fornelli A, Peterse JL, Mignani S, Eusebi V. Microcalcifications in ductal carcinoma in situ of the breast: histochemical and immunohistochemical study. Hum. Pathol. 27(2), 178-183 (1996).
74. Lev-Toaff AS, Feig SA, Saitas VL, Finkel GC, Schwartz GF. Stability of malignant breast microcalcifications. Radiology 192(1), 153-156 (1994).
75. Berridge MJ, Bootman MD, Roderick HL. Calcium signalling: dynamics, homeostasis and remodelling. Nat. Rev. Mol. Cell Biol. 4(7), 517-529 (2003). Annu. Rev. Biochem. 56, 395-433 (1987).
76. VanHouten J, Sullivan C, Bazinet C et al. PMCA2 regulates apoptosis during mammary gland involution and predicts outcome in breast cancer. Proc. Natl Acad. Sci. USA 107(25), 11405-11410 (2010).
77. VanHouten JN, Neville MC, Wysolmerski JJ. The calcium-sensing receptor regulates plasma membrane calcium adenosine triphosphatase isoform 2 activity in mammary epithelial cells: a mechanism for calcium-regulated calcium transport into milk. Endocrinology 148(12), 5943-5954 (2007).
78. Brini M. Plasma membrane Ca(2+)-ATPase: from a housekeeping function to a versatile signaling role. Pflugers Arch. 457(3), 657-664 (2009).
79. Brini M, Carafoli E. Calcium pumps in health and disease. Physiol. Rev. 89(4), 1341-1378 (2009).
80. Faddy HM, Smart CE, Xu R et al. Localization of plasma membrane and secretory calcium pumps in the mammary gland. Biochem. Biophys. Res. Commun. 369(3), 977-981 (2008).
81. Reinhardt TA, Lippolis JD. Mammary gland involution is associated with rapid down regulation of major mammary Ca2+-ATPases. Biochem. Biophys. Res. Commun. 378(1), 99-102 (2009).
82. Watson CJ. Involution: apoptosis and tissue remodelling that convert the mammary gland from milk factory to a quiescent organ. Breast Cancer Res. 8(2), 203 (2006).
83. Monteith GR, McAndrew D, Faddy HM, Roberts-Thomson SJ. Calcium and cancer: targeting Ca2+ transport. Nat. Rev. Cancer 7(7), 519-530 (2007).
84. Roderick HL, Cook SJ. Ca2+ signalling checkpoints in cancer: remodelling Ca2+ for cancer cell proliferation and survival. Nat. Rev. Cancer 8(5), 361-375 (2008).
85. Cook SJ, Lockyer PJ. Recent advances in Ca(2+)-dependent Ras regulation and cell proliferation. Cell. Calcium 39(2), 101-112 (2006).
86. Lipskaia L, Lompre AM. Alteration in temporal kinetics of Ca2+ signaling and control of growth and proliferation. Biol. Cell 96(1), 55-68 (2004).
87. Santella L, Ercolano E, Nusco GA. The cell cycle: a new entry in the field of Ca2+ signaling. Cell. Mol. Life Sci. 62(21), 2405-2413 (2005).
88. Bikle D, Adams J, Christakos S. vitamin D: production, metabolism, mechanism of action and clinical requirements. In: Primer on the Metabolic Bone Diseases and Disorders of Mineral Metabolism. Rosen CJ (Ed.). American Society for Bone and Mineral Research, Washington, DC, USA, 141-149 (2008).
89. Bikle DD. Vitamin D metabolism and function in the skin. Mol. Cell. Endocrinol. 347(1-2), 80-89 (2011).
90. Welsh J. Vitamin D metabolism in mammary gland and breast cancer. Mol. Cell. Endocrinol. 347(1-2), 55-60 (2011).
91. Welsh J. Cellular and molecular effects of vitamin D on carcinogenesis. Arch. Biochem. Biophys. 523(1), 107-114 (2011).
92. Gordon PB, Holen I, Fosse M, Rotnes JS, Seglen PO. Dependence of hepatocytic autophagy on intracellularly sequestered calcium. J. Biol. Chem. 268(35), 26107-26112 (1993).
93. Jia W, Pua HH, Li Q J, He YW. Autophagy regulates endoplasmic reticulum homeostasis and calcium mobilization in T lymphocytes. J. Immunol. 186(3), 1564-1574 (2010).
94. ClinicalTrials.gov. Study of the Efficacy of Chloroquine in the Treatment of Ductal Carcinoma in Situ (The PINC Trial). http://clinicaltrials.gov/ct2/ show/NCT01023 477?term=NCT01023477&rank=1