Disseminated tumor cells persist in the bone marrow of breast cancer patients through sustained activation of the unfolded protein response

Cancer Research

Volumn 75, Issue 24, 2015, Pages 5367-5377

  Bartkowiak, Kai ^a   Kwiatkowski, Marcel ^a   Buck, Friedrich ^a   Gorges, Tobias M ^a   Nilse, Lars ^b   Assmann, Volker ^a   Andreas, Antje ^a   Müller, Volkmar ^a   Wikman, Harriet ^a   Riethdorf, Sabine ^a   Schlüter, Hartmut ^a   Pantel, Klaus ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; GLUCOSE 6 PHOSPHATE DEHYDROGENASE; GLUCOSE REGULATED PROTEIN 78; GLUCOSE REGULATED PROTEIN 94; HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA UPREGULATED PROTEIN 1; INDUCIBLE NITRIC OXIDE SYNTHASE; PEPTIDES AND PROTEINS; PROTEIN DISULFIDE ISOMERASE; UNCLASSIFIED DRUG; VIMENTIN; VOLTAGE DEPENDENT ANION CHANNEL 2;

ARTICLE; BONE MARROW METASTASIS; BREAST CANCER; CARCINOGENESIS; CELL PROLIFERATION; CELL STRESS; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; DOWN REGULATION; ENZYME INDUCTION; EX VIVO STUDY; HUMAN; HUMAN CELL; HUMAN TISSUE; MAJOR CLINICAL STUDY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; UNFOLDED PROTEIN RESPONSE; UPREGULATION; ADAPTATION; BONE MARROW; BREAST TUMOR; CANCER STEM CELL; CELL HYPOXIA; CELL LINE; FEMALE; IMMUNOHISTOCHEMISTRY; METABOLISM; PATHOLOGY; PHYSIOLOGY; TISSUE MICROARRAY; WESTERN BLOTTING;

ADAPTATION, PHYSIOLOGICAL; BLOTTING, WESTERN; BONE MARROW; BREAST NEOPLASMS; CELL HYPOXIA; CELL LINE; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; NEOPLASTIC STEM CELLS; TISSUE ARRAY ANALYSIS; UNFOLDED PROTEIN RESPONSE;

EID: 84955454424     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-14-3728     Document Type: Article

References (42)

1. Pantel K, Alix-Panabieres C. Bone marrow as a reservoir for disseminated tumor cells: a special source for liquid biopsy in cancer patients. Bonekey Rep 2014;3:584.
2. Parmar K, Mauch P, Vergilio JA, Sackstein R, Down JD. Distribution of hematopoietic stem cells in the bone marrow according to regional hypoxia. Proc Natl Acad Sci U S A 2007;104:5431-6.
3. Shiozawa Y, Pedersen EA, Havens AM, Jung Y, Mishra A, Joseph J, et al. Human prostate cancer metastases target the hematopoietic stem cell niche to establish footholds in mouse bone marrow. J Clin Invest 2011;121: 1298-312.
4. Spencer JA, Ferraro F, Roussakis E, Klein A, Wu J, Runnels JM, et al. Direct measurement of local oxygen concentration in the bone marrow of live animals. Nature 2014;508:269-73.
5. Braun S, Vogl FD, Naume B, Janni W, Osborne MP, Coombes RC, et al. A pooled analysis of bone marrow micrometastasis in breast cancer. N Engl J Med 2005;353:793-802.
6. Janni W, Vogl FD, Wiedswang G, Synnestvedt M, Fehm T, Juckstock J, et al. Persistenceofdisseminatedtumor cells in the bone marrow ofbreast cancer patients predicts increased risk for relapse - a European pooled analysis. Clin Cancer Res 2011;17:2967-76.
7. Braun S, Kentenich C, Janni W, Hepp F, de Waal J, Willgeroth F, et al. Lack of effect of adjuvant chemotherapy on the elimination of single dormant tumor cells in bone marrow of high-risk breast cancer patients. J Clin Oncol 2000;18:80-6.
8. Tam WL, Weinberg RA. The epigenetics of epithelial-mesenchymal plasticity in cancer. Nat Med 2013;19:1438-49.
9. Ameri K, Luong R, Zhang H, Powell AA, Montgomery KD, Espinosa I, et al. Circulating tumour cells demonstrate an altered response to hypoxia and an aggressive phenotype. Br J Cancer 2010;102:561-9.
10. Bristow RG, Hill RP. Hypoxia and metabolism. Hypoxia, DNA repair and genetic instability. Nat Rev Cancer 2008;8:180-92.
11. Bartkowiak K, Effenberger KE, Harder S, Andreas A, Buck F, Peter-Katalinic J, et al. Discovery of a novel unfolded protein response phenotype of cancer stem/progenitor cells from the bone marrow of breast cancer patients. J Proteome Res 2010;9:3158-68.
12. Pantel K, Brakenhoff RH. Dissecting the metastatic cascade. Nat Rev Cancer 2004;4:448-56.
13. Wouters BG, Koritzinsky M. Hypoxia signalling through mTOR and the unfolded protein response in cancer. Nat Rev Cancer 2008;8:851-64.
14. Lee AS. Glucose-regulated proteins in cancer: molecular mechanisms and therapeutic potential. Nat Rev Cancer 2014;14:263-76.
15. Bennett HL, Fleming JT, O'Prey J, Ryan KM, Leung HY. Androgens modulate autophagy and cell deathvia regulation of the endoplasmic reticulum chaperone glucose-regulated protein 78/BiP in prostate cancer cells. Cell Death Dis 2010;1:e72.
16. Tan SS, Ahmad I, Bennett HL, Singh L, Nixon C, Seywright M, et al. GRP78 up-regulation is associated with androgen receptor status, Hsp70-Hsp90 client proteins and castrate-resistant prostate cancer. J Pathol 2011;223: 81-7.
17. Korkaya H, Wicha MS. Breastcancer stem cells: we've got them surrounded. Clin Cancer Res 2013;19:511-3.
18. Lehtinen L, Vainio P, Wikman H, Reemts J, Hilvo M, Issa R, et al. 15-Hydroxyprostaglandin dehydrogenase associates with poor prognosis in breast cancer, induces epithelial-mesenchymal transition, and promotes cell migration in cultured breast cancer cells. J Pathol 2012;226:674-86.
19. Wrage M, Ruosaari S, Eijk PP, Kaifi JT, Hollmen J, Yekebas EF, et al. Genomic profiles associated with early micrometastasis in lung cancer: relevance of 4q deletion. Clin Cancer Res 2009;15:1566-74.
20. Putz E, Witter K, Offner S, Stosiek P, Zippelius A, Johnson J, et al. Phenotypic characteristics of cell lines derived from disseminated cancer cells in bone marrow of patients with solid epithelial tumors: establishment of working models for human micrometastases. Cancer Res 1999; 59:241-8.
21. Pantel K, Dickmanns A, Zippelius A, Klein C, Shi J, Hoechtlen-Vollmar W, et al. Establishment of micrometastatic carcinoma cell lines: a novel source of tumor cell vaccines. J Natl Cancer Inst 1995;87:1162-8.
22. Dittmar T, Husemann A, Schewe Y, Nofer JR, Niggemann B, Zanker KS, et al. Induction of cancer cell migration by epidermal growth factor is initiated by specific phosphorylation of tyrosine 1248 of c-erbB-2 receptor via EGFR. FASEB J 2002;16:1823-5.
23. Grabinski N, Bartkowiak K, Grupp K, Brandt B, Pantel K, Jucker M. Distinct functional roles of Akt isoforms for proliferation, survival, migration and EGF-mediated signalling in lung cancer derived disseminated tumor cells. Cell Signal 2011;23:1952-60.
24. Balz LM, Bartkowiak K, Andreas A, Pantel K, Niggemann B, Zanker KS, et al. The interplay of HER2/HER3/PI3K and EGFR/HER2/PLC-gamma1 signalling in breast cancer cell migration and dissemination. J Pathol 2012;227: 234-44.
25. Bartkowiak K, Wieczorek M, Buck F, Harder S, Moldenhauer J, Effenberger KE, et al. Two-dimensional differential gel electrophoresis of a cell line derived from a breast cancer micrometastasis revealed a stem/progenitor cell protein profile. J Proteome Res 2009;8:2004-14.
26. Yuan Y, Hilliard G, Ferguson T, Millhorn DE. Cobalt inhibits the interaction between hypoxia-inducible factor-alpha and von Hippel-Lindau protein by direct binding to hypoxia-inducible factor-alpha. J Biol Chem 2003;278:15911-6.
27. Ni M, Zhou H, Wey S, Baumeister P, Lee AS. Regulation of PERK signaling and leukemic cell survival by anovel cytosolic isoform of the UPR regulator GRP78/Bi P. PLoS ONE 2009;4:e6868.
28. Braun S, Pantel K, Muller P, Janni W, Hepp F, Kentenich CR, et al. Cytokeratin-positive cells in the bone marrow and survival of patients with stage I, II, or III breast cancer. N Engl J Med 2000;342:525-33.
29. Yu M, Bardia A, Wittner BS, Stott SL, Smas ME, Ting DT, et al. Circulating breast tumor cells exhibit dynamic changes in epithelial and mesenchymal composition. Science 2013;339:580-4.
30. Baird SD, Turcotte M, Korneluk RG, Holcik M. Searching for IRES. RNA 2006;12:1755-85.
31. Anderson P, Kedersha N. RNA granules: post-transcriptional and epigenetic modulators of gene expression. Nat Rev Mol Cell Biol 2009;10:430-6.
32. Anderson P, Kedersha N. RNA granules. J Cell Biol 2006;172:803-8.
33. Quaresma AJ, Bressan GC, Gava LM, Lanza DC, Ramos CH, Kobarg J. Human hnRNP Q re-localizes to cytoplasmic granules upon PMA, thapsi-gargin, arsenite and heat-shock treatments. Exp Cell Res 2009;315:968-80.
34. Felig P, Marliss E, Owen OE, Cahill GF Jr. Blood glucose and cluconeogenesis in fasting man. Arch Intern Med 1969;123:293-8.
35. Tennant DA, Duran RV, Gottlieb E. Targeting metabolic transformation for cancer therapy. Nat Rev Cancer 2010;10:267-77.
36. Lin AY, Maniotis AJ, Valyi-Nagy K, Majumdar D, Setty S, Kadkol S, et al. Distinguishing fibrovascular septa from vasculogenic mimicry patterns. Arch Pathol Lab Med 2005;129:884-92.
37. Shirakawa K, Tsuda H, Heike Y, Kato K, Asada R, Inomata M, et al. Absence of endothelial cells, central necrosis, and fibrosis are associated with aggressive inflammatory breast cancer. Cancer Res 2001;61:445-51.
38. Shirakawa K, Wakasugi H, Heike Y, Watanabe I, Yamada S, Saito K, et al. Vasculogenic mimicry and pseudo-comedo formation in breast cancer. Int J Cancer 2002;99:821-8.
39. Hillen F, Griffioen AW. Tumour vascularization: sprouting angiogenesis and beyond. Cancer Metastasis Rev 2007;26:489-502.
40. Ping YF, Bian XW. Consice review: contribution of cancer stem cells to neovascularization. Stem Cells 2011;29:888-94.
41. Fan YL, Zheng M, Tang YL, Liang XH. A new perspective of vasculogenic mimicry: EMT and cancer stem cells (Review). Oncol Lett 2013;6:1174-80.
42. Nombela-Arrieta C, Pivarnik G, Winkel B, Canty KJ, Harley B, Mahoney JE, et al. Quantitative imaging of haematopoietic stem and progenitor cell localization and hypoxic status in the bone marrow microenvironment. Nat Cell Biol 2013;15:533-43.