Osteolytic bone metastasis is hampered by impinging on the interplay among autophagy, anoikis and ossification

Cell Death and Disease

Volumn 5, Issue 1, 2014, Pages e1005-

  Maroni, P ^a   Bendinelli, P ^b   Matteucci, E ^b   Locatelli, A ^b,c   Nakamura, T ^d   Scita, G ^b,c   Desiderio, M A ^b  

^a IRCCS ISTITUTO ORTOPEDICO GALEAZZI   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

^c FIRC INSTITUTE OF MOLECULAR ONCOLOGY   (Italy)

^d OSAKA UNIVERSITY   (Japan)

Author keywords

autophagy in metastasis; bone metastasis; HGF; NK4; Src

Indexed keywords

PROTEIN KINASE P60; SCATTER FACTOR; SCATTER FACTOR RECEPTOR;

ANIMAL; ANOIKIS; ARTICLE; AUTOPHAGY; BONE TUMOR; BREAST TUMOR; FEMALE; GENETICS; HETEROTOPIC OSSIFICATION; HUMAN; METABOLISM; METASTASIS; MOUSE; OSTEOLYSIS; PATHOLOGY; PATHOPHYSIOLOGY;

ANIMALS; ANOIKIS; AUTOPHAGY; BONE NEOPLASMS; BREAST NEOPLASMS; FEMALE; HEPATOCYTE GROWTH FACTOR; HUMANS; MICE; OSSIFICATION, HETEROTOPIC; OSTEOLYSIS; PROTO-ONCOGENE PROTEINS C-MET; PROTO-ONCOGENE PROTEINS PP60(C-SRC);

EID: 84906898054     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2013.465     Document Type: Article

References (49)

1. Psaila B, Lyden D. The metastatic niche: adapting to the foreign soil. Nat Rev Cancer 2009; 9: 285–293. DOI: 10.1038/nrc2621
2. Previdi S, Maroni P, Matteucci E, Broggini M, Bendinelli P, Desiderio MA. Interaction between human-breast cancer metastasis and bone microenvironment through activated hepatocyte growth factor/Met and β-catenin/Wnt pathways. Eur J Cancer 2010; 46: 1679–1691. DOI: 10.1016/j.ejca.2010.02.036
3. Matteucci E, Maroni P, Luzzati A, Perrucchini G, Bendinelli P, Desiderio MA. Bone metastatic process of breast cancer involves methylation state affecting E-cadherin expression through TAZ and WWOX nuclear effectors. Eur J Cancer 2013; 49: 231–244. DOI: 10.1016/j.ejca.2012.05.006
4. Zhang XH, Wang Q, Gerald W, Hudis L, Norton M, Smid JA et al. Latent bone metastasis in breast cancer tied to Src-dependent survival signals. Cancer Cell 2009; 16: 67–78. DOI: 10.1016/j.ccr.2009.05.017
5. Gherardi E, Birchmeier W, Birchmeier C, Vande Woude G. Targeting Met in cancer: rationale and progress. Nat Rev Cancer 2012; 12: 89–103. DOI: 10.1038/nrc3205
6. Bendinelli P, Maroni P, Matteucci E, Desiderio MA. Comparative role of acetylation along c-SRC/ETS1 signaling pathway in bone metastatic and invasive mammary cell phenotypes. Biochim Biophys Acta 2011; 1813: 1767–1776. DOI: 10.1016/j.bbamcr.2011.06.004
7. Matteucci E, Bendinelli P, Desiderio MA. Nuclear localization of active HGF receptor Met in aggressive MDA-MB231 breast carcinoma cells. Carcinogenesis 2009; 30: 937–945. DOI: 10.1093/carcin/bgp080
8. Barkan D, El Touny LH, Michalowski AM, Smith JA, Chu I, Davis AS et al. Metastatic growth from dormant cells induced by a Col-I-enriched fibrotic environment. Cancer Res 2010; 70: 5706–5716. DOI: 10.1158/0008-5472.CAN-09-2356
9. Araujo J, Logothetis C. Targeting Src in metastatic bone disease. Int J Cancer 2009; 124: 1–6. DOI: 10.1002/ijc.23998
10. Weilbaecher KN, Guise TA, McCauley LK. Cancer to bone: a fatal attraction. Nat Rev Cancer 2011; 11: 411–425. DOI: 10.1038/nrc3055
11. Buchheit CL, Rayavarapu RR, Schafer ZT. The regulation of cancer cell death and metabolism by extracellular matrix attachment. Semin Cell Dev Biol 2012; 23: 402–411. DOI: 10.1016/j.semcdb.2012.04.007
12. Lisanti MP, Martinez-Outschoorn UE, Chiavarina B, Pavlides S, Whitaker-Menezes D, Tsirigos A et al. Understanding the ‘lethal’ drivers of tumor–stroma co-evolution: emerging role(s) for hypoxia, oxidative stress and autophagy/mitophagy in the tumor microenvironment. Cancer Biol Ther 2010; 10: 537–542. DOI: 10.4161/cbt.10.6.13370
13. Roy S, Debnath J. Autophagy and tumorigenesis. Semin Immunopathol 2010; 32: 383–396. DOI: 10.1007/s00281-010-0213-0
14. White E. Deconvoluting the context-dependent role for autophagy in cancer. Nat Rev Cancer 2012; 12: 401–410. DOI: 10.1038/nrc3262
15. Suzuki Y, Sakai K, Ueki J, Xu Q, Nakamura T, Shimada H et al. Inhibition of Met/HGF receptor and angiogenesis by NK4 leads to suppression of tumor growth and migration in malignant pleural mesothelioma. Int J Cancer 2010; 127: 1948–1957. DOI: 10.1002/ijc.25197
16. Kishi Y, Kuba K, Nakamura T, Wen J, Suzuki Y, Mizuno S et al. Systemic NK4 gene therapy inhibits tumor growth and metastasis of melanoma and lung carcinoma in syngeneic mouse tumor models. Cancer Sci 2009; 100: 1351–1358. DOI: 10.1111/j.1349-7006.2009.01184.x
17. Kuba K, Matsumoto K, Date K, Shimura H, Tanaka M, Nakamura T. HGF/NK4, a four-kringle antagonist of hepatocyte growth factor, is an angiogenesis inhibitor that suppresses tumor growth and metastasis in mice. Cancer Res 2000; 60: 6737–6743.
18. Yue D, Wang Y, Ma P, Li Y-Y, Chen H, Wang P et al. Effects of transferred NK4 gene on proliferation, migration, invasion and apoptosis of human prostate cancer DU145 cells. Asian J Androl 2010; 12: 381–389. DOI: 10.1038/aja.2010.22
19. Choi J, Jung W, Koo JS. Expression of autophagy-related markers beclin-1, light chain 3A, light chain 3B and p62 according to the molecular subtype of breast cancer. Histopathology 2013; 62: 275–286. DOI: 10.1111/his.12002
20. Bjørkøy G, Lamark T, Johansen T. p62/SQSTM1: a missing link between protein aggregates and the autophagy machinery. Autophagy 2006; 2: 138–139. DOI: 10.4161/auto.2.2.2405
21. Huang WC, Xie Z, Konaka H, Sodek J, Zhau HE, Chung LWK. Human osteocalcin and bone sialoprotein mediating osteomimicry of prostate cancer cells: role of cAMP-dependent protein kinase A signaling pathway. Cancer Res 2005; 65: 2303–2313. DOI: 10.1158/0008-5472.CAN-04-3448
22. Bendinelli P, Maroni P, Matteucci E, Luzzati A, Perrucchini G, Desiderio MA. Hypoxia inducible factor-1 is activated by transcriptional co-activator with PDZ-binding motif (TAZ) versus WWdomain-containing oxidoreductase (WWOX) in hypoxic microenvironment of bone metastasis from breast cancer. Eur J Cancer 2013; 49: 2608–2618. DOI: 10.1016/j.ejca.2013.03.002
23. Maroni P, Matteucci E, Luzzati A, Perrucchini G, Bendinelli P, Desiderio MA. Nuclear co-localization and functional interaction of COX-2 and HIF-1α characterize bone metastasis of human breast carcinoma. Breast Cancer Res Treat 2011; 129: 433–450. DOI: 10.1007/s10549-010-1240-1
24. Whelan KA, Reginato MJ. Surviving without oxygen: hypoxia regulation of mammary morphogenesis and anoikis. Cell Cycle 2011; 10: 2287–2294. DOI: 10.4161/cc.10.14.16532
25. Maes H, Rubio N, Garg AD, Agostinis P. Autophagy: shaping the tumor microenvironment and therapeutic response. Trends Mol Med 2013; 19: 428–446. DOI: 10.1016/j.molmed.2013.04.005
26. Bendinelli P, Matteucci E, Maroni P, Desiderio MA. NF-kB activation, dependent on acetylation/deacetylation, contributes to HIF-1 activity and migration of bone metastatic breast carcinoma cells. Mol Cancer Res 2009; 7: 1328–1341. DOI: 10.1158/1541-7786.MCR-08-0548
27. Desiderio MA. Hepatocyte growth factor in invasive growth of carcinomas. Cell Mol Life Sci 2007; 64: 1341–1354. DOI: 10.1007/s00018-007-7050-x
28. Taddei ML, Giannoni E, Fiaschi T, Chiarugi P. Anoikis: an emerging hallmark in health and diseases. J Pathol 2012; 226: 380–393. DOI: 10.1002/path.3000
29. Chen K, Perez-Stable C, D’Ippolito G, Schiller PC, Roos BA, Howard GA. Human bone marrow-derived stem cell proliferation is inhibited by hepatocyte growth factor via increasing the cell cycle inhibitors p53, p21 and p27. Bone 2011; 49: 1194–1204. DOI: 10.1016/j.bone.2011.08.023
30. Soto AM, Sonnenschein C. The tissue organization field theory of cancer: A testable replacement for the somatic mutation theory. Bioassays 2011; 33: 332–340. DOI: 10.1002/bies.201100025
31. Valastyan S, Weinberg RA. Tumor metastasis: molecular insights and evolving paradigms. Cell 2011; 147: 275–292. DOI: 10.1016/j.cell.2011.09.024
32. Mizuno S, Nakamura T. HGF-MET cascade, a key target for inhibiting cancer metastasis: the impact of NK4 discovery on cancer biology and therapeutics. Int J Mol Sci 2013; 14: 888–919. DOI: 10.3390/ijms14010888
33. Wei L, Dai Q, Zhou Y, Zou M, Li Z, Lu N et al. Oroxylin A sensitizes non-small cell lung cancer cells to anoikis via glucose-deprivation-like mechanisms: c-Src and hexokinase II. Biochim Biophys Acta 2013; 1830: 3835–3845. DOI: 10.1016/j.bbagen.2013.03.009
34. Woolley JF, Corcoran A, Groeger G, Landry WD, Cotter TG. Redox-regulated growth factor survival signaling. Antioxid Redox Signal 2013 doi:10.1089/ars.2012.5028. DOI: 10.1089/ars.2012.5028
35. 87 of BimEL is phosphorylated by Akt and regulates BimEL apoptotic function. J Biol Chem 2006; 281: 813–823. DOI: 10.1074/jbc.M505546200
36. Ruppert SM, Li W, Zhang G, Carlson AL, Limaye A, Durum SK et al. The major isoforms of Bim contribute to distinct biological activities that govern the processes of autophagy and apoptosis in interleukin-7 dependent lymphocytes. Biochim Biophys Acta 2012; 1823: 1877–1893. DOI: 10.1016/j.bbamcr.2012.06.017
37. Giannoni E, Fiaschi T, Ramponi G, Chiarugi P. Redox regulation of anoikis resistance of metastatic prostate cancer cells: key role for Src and EGFR-mediated pro-survival signals. Oncogene 2009; 28: 2074–2086. DOI: 10.1038/onc.2009.77
38. Whelan KA, Caldwell SA, Shahriari KS, Jackson SR, Franchetti LD, Johannes GJ et al. Hypoxia suppression of Bim and Bmf blocks anoikis and luminal clearing during mammary morphogenesis. Mol Biol Cell 2010; 21: 3829–3837. DOI: 10.1091/mbc.e10-04-0353
39. Emaduddin M, Bicknell DC, Bodmer WF, Feller SM. Cell growth, global phosphotyrosine elevation, and c-Met phosphorylation through Src family kinases in colorectal cancer cells. Proc Natl Acad Sci USA 2008; 105: 2358–2362. DOI: 10.1073/pnas.0712176105
40. Kim JI, Lakshmikanthan V, Frilot N, Daaka Y. Prostaglandin E2 promotes lung cancer cell migration via EP4-betaArrestin1-c-Src signalosome. Mol Cancer Res 2010; 8: 569–577. DOI: 10.1158/1541-7786.MCR-09-0511
41. Rucci N, Recchia I, Angelucci A, Alamanou M, Del Fattore A, Fortunati D et al. Inhibition of protein kinase c-Src reduces the incidence of breast cancer metastasis and increases survival in mice: implications for therapy. J Pharmacol Exp Ther 2006; 318: 161–172. DOI: 10.1124/jpet.106.102004
42. Hu YL, Jahangiri A, De Lay M, Aghi MK. Hypoxia-induced tumor cell autophagy mediates resistance to anti-angiogenic therapy. Autophagy 2012; 8: 979–981. DOI: 10.4161/auto.20232
43. Karar J, Maity A. PI3K/AKT/mTOR pathway in angiogenesis. Front Mol Neurosci 2011; 4: 51. DOI: 10.3389/fnmol.2011.00051
44. Ponomarev V, Doubrovin M, Serganova I, Vider J, Shavrin A, Beresten T et al. A novel triple-modality reporter gene for whole-body fluorescent, bioluminescent, and nuclear noninvasive imaging. Eur J Nucl Med Mol Imag 2004; 31: 740–751. DOI: 10.1007/s00259-003-1441-5
45. Rice L, Lepler S, Pampo C, Siemann DW. Impact of the SRC inhibitor dasatinib on the metastatic phenotype of human prostate cancer cells. Clin Exp Metast 2012; 29: 133–142. DOI: 10.1007/s10585-011-9436-2
46. Jie JZ, Wang JW, Qu JG, Wang W, Hung T. Effects of adenoviral-mediated gene transduction of NK4 on proliferation, movement, and invasion of human colonic LS174T cancer cells in vitro. World J Gastroenterol 2006; 12: 3983–3988. DOI: 10.3748/wjg.v12.i25.3983
47. Bretland AJ, Lawry J, Sharrard RM. A study of death by anoikis in cultured epithelial cells. Cell Prolif 2001; 34: 199–210. DOI: 10.1046/j.1365-2184.2001.00198.x
48. Matteucci E, Castoldi R, Desiderio MA. Hepatocyte growth factor induces pro-apoptotic genes in HepG2 hepatoma but not in B16-F1 melanoma cells. J Cell Physiol 2001; 186: 387–396. DOI: 10.1002/1097-4652(2000)9999:9999<000::AID-JCP1033>3.0.CO;2-8
49. Maemondo M, Narumi K, Saijo Y, Usui K, Tahara M, Tazawa R et al. Targeting angiogenesis and HGF function using an adenoviral vector expressing the HGF antagonist NK4 for cancer therapy. Mol Ther 2002; 5: 177–185. DOI: 10.1006/mthe.2002.0533