Hypoxia after liver surgery imposes an aggressive cancer stem cell phenotype on residual tumor cells

Annals of Surgery

Volumn 259, Issue 4, 2014, Pages 750-759

  Govaert, Klaas M ^a   Emmink, Benjamin L ^a   Nijkamp, Maarten W ^a   Cheung, Zing J ^a   Steller, Ernst J A ^a   Fatrai, Szabolcs ^a   De Bruijn, Menno T ^a   Kranenburg, Onno ^a   Borel Rinkes, Inne H M ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

Cancer stem cell; colorectal; hypoxia; hypoxia activated prodrugs; inflammation; liver metastases; surgery; tirapazamine

Indexed keywords

TIRAPAZAMINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; CANCER CELL CULTURE; CANCER CHEMOTHERAPY; CANCER GROWTH; CANCER RECURRENCE; CANCER RESISTANCE; CANCER STEM CELL; CANCER SURVIVAL; CELL CLONE; CELL DIFFERENTIATION; CELL HYPOXIA; CELL INVASION; CLONOGENESIS; COLORECTAL CANCER; CONTROLLED STUDY; HEMATOPOIETIC STEM CELL; HUMAN; HYPOXIA; IMMUNOCOMPETENT CELL; IN VITRO STUDY; LIVER METASTASIS; LIVER SURGERY; MALE; METASTASIS POTENTIAL; METASTATIC COLORECTAL CANCER; MICROMETASTASIS; MINIMAL RESIDUAL DISEASE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RADIOFREQUENCY ABLATION; REPERFUSION INJURY;

ANIMALS; ANOXIA; ANTINEOPLASTIC AGENTS; BLOTTING, WESTERN; CATHETER ABLATION; CELL LINE, TUMOR; COLORECTAL NEOPLASMS; FLOW CYTOMETRY; HEMATOPOIETIC STEM CELLS; HEPATECTOMY; HUMANS; IMMUNOHISTOCHEMISTRY; LIVER NEOPLASMS, EXPERIMENTAL; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED NOD; MICE, NUDE; MICE, SCID; NEOPLASM INVASIVENESS; NEOPLASM MICROMETASTASIS; NEOPLASM RECURRENCE, LOCAL; NEOPLASM, RESIDUAL; NEOPLASTIC STEM CELLS; PHENOTYPE; POSTOPERATIVE COMPLICATIONS; REAL-TIME POLYMERASE CHAIN REACTION; REPERFUSION INJURY; TRIAZINES; TUMOR MARKERS, BIOLOGICAL;

EID: 84895920615     PISSN: 00034932     EISSN: 15281140     Source Type: Journal    
DOI: 10.1097/SLA.0b013e318295c160     Document Type: Article

References (64)

1. Jones FS, Rous P. On the cause of the localization of secondary tumors at points of injury. J ExpMed. 1914;20:404-412.
2. Demicheli R, Retsky MW, Hrushesky WJ, et al. The effects of surgery on tumor growth: A century of investigations. Ann Oncol. 2008;19:1821-1828.
3. Nijkamp MW, Van Der Bilt JD, De Bruijn MT, et al. Accelerated perinecrotic outgrowth of colorectal liver metastases following radiofrequency ablation is a hypoxia-driven phenomenon. Ann Surg. 2009;249:814-823.
4. Fisher B, Fisher ER. Experimental studies of factors influencing hepatic metastases. III. Effect of surgical trauma with special reference to liver injury. Ann Surg. 1959;150:731-744.
5. Van Der Bilt JD, Kranenburg O, Nijkamp MW, et al. Ischemia/reperfusion accelerates the outgrowth of hepatic micrometastases in a highly standardized murine model. Hepatology. 2005;42:165-175.
6. Daenen LG, Roodhart JM, Van AM, et al. Chemotherapy enhances metastasis formation via VEGFR-1-expressing endothelial cells. Cancer Res. 2011;71:6976-6985.
7. Van Den Brenk HA, Kelly H. Stimulation of growth of metastases by local x-irradiation in kidney and liver. Br J Cancer. 1973;28:349-353.
8. Nijkamp MW, Van Der Bilt JD, Snoeren N, et al. Prolonged portal triad clamping during liver surgery for colorectal liver metastases is associated with decreased time to hepatic tumour recurrence. Eur J Surg Oncol. 2010;36: 182-188.
9. Van Der Bij GJ, Oosterling SJ, Beelen RH, et al. The perioperative period is an underutilized window of therapeutic opportunity in patients with colorectal cancer. Ann Surg. 2009;249:727-734.
10. Van Der Bilt JD, Kranenburg O, Verheem A, et al. Selective portal clamping to minimize hepatic ischaemia-reperfusion damage and avoid accelerated outgrowth of experimental colorectal liver metastases. Br J Surg. 2006;93:1015-1022.
11. Van Der Bilt JD, Soeters ME, Duyverman AM, et al. Perinecrotic hypoxia contributes to ischemia/reperfusion-accelerated outgrowth of colorectal micrometastases. Am J Pathol. 2007;170:1379-1388.
12. NijkampMW, Hoogwater FJ, Steller EJ, et al. CD95 is a key mediator of invasion and accelerated outgrowth of mouse colorectal liver metastases following radiofrequency ablation. J Hepatol. 2010;53:1069-1077.
13. Bertout JA, Patel SA, Simon MC. The impact of O2 availability on human cancer. Nat Rev Cancer. 2008;8:967-975.
14. Klampfer L. Cytokines, inflammation and colon cancer. Curr Cancer Drug Targets. 2011;11:451-464.
15. Semenza GL. Hypoxia-inducible factors: Mediators of cancer progression and targets for cancer therapy. Trends Pharmacol Sci. 2012;33:207-214.
16. Shiao SL, Ganesan AP, Rugo HS, et al. Immune microenvironments in solid tumors: New targets for therapy. Genes Dev. 2011;25:2559-2572.
17. LydenD,Hattori K, Dias S, et al. Impaired recruitment of bone-marrow-derived endothelial and hematopoietic precursor cells blocks tumor angiogenesis and growth. Nat Med. 2001;7:1194-1201.
18. Langenberg MH, Nijkamp MW, Roodhart JM, et al. Liver surgery induces an immediate mobilization of progenitor cells in liver cancer patients: A potential role for G-CSF. Cancer Biol Ther. 2010;9:743-748.
19. Imtiyaz HZ, Simon MC. Hypoxia-inducible factors as essential regulators of inflammation. Curr Top Microbiol Immunol. 2010; 345:105-120.
20. Taylor CT. Interdependent roles for hypoxia inducible factor and nuclear factorkappaB in hypoxic inflammation. J Physiol. 2008;586:4055-4059.
21. Taylor CT, Cummins EP. The role of NF-kappaB in hypoxia-induced gene expression. Ann N Y Acad Sci. 2009;1177:178-184.
22. Emmink BL, Van Houdt WJ, Vries RG, et al. Differentiated human colorectal cancer cells protect tumor-initiating cells from irinotecan. Gastroenterology. 2011;141:269-278.
23. Steller EJ, Ritsma L, Raats DA, et al. The death receptor CD95 activates the cofilin pathway to stimulate tumour cell invasion. EMBO Rep. 2011;12: 931-937.
24. Nijkamp MW, Borren A, Govaert KM, et al. Radiofrequency ablation of colorectal liver metastases induces an inflammatory response in distant hepatic metastases but not in local accelerated outgrowth. J SurgOncol. 2010;101:551-556.
25. De Sousa E Melo F, Colak S, Buikhuisen J, et al. Methylation of cancer-stemcell-associated Wnt target genes predicts poor prognosis in colorectal cancer patients. Cell Stem Cell. 2011; 9:476-485.
26. Merlos-Suarez A, Barriga FM, Jung P, et al. The intestinal stem cell signature identifies colorectal cancer stem cells and predicts disease relapse. Cell Stem Cell. 2011;8:511-524.
27. Charafe-Jauffret E, Ginestier C, Iovino F, et al. Aldehyde dehydrogenase 1-positive cancer stem cells mediate metastasis and poor clinical outcome in inflammatory breast cancer. Clin Cancer Res. 2010;16:45-55.
28. Deng S, Yang X, Lassus H, et al. Distinct expression levels and patterns of stem cell marker, aldehyde dehydrogenase isoform 1 (ALDH1), in human epithelial cancers. PLoS One. 2010;5:e10277.
29. Shenoy A, Butterworth E, Huang EH. ALDH as a marker for enriching tumorigenic human colonic stem cells. Methods Mol Biol. 2012;916: 373-385.
30. Shenoy AK, Fisher RC, Butterworth EA, et al. Transition from colitis to cancer: High Wnt activity sustains the tumor-initiating potential of colon cancer stem cell precursors. Cancer Res. 2012;72:5091-5100.
31. Weng D, Penzner JH, Song B, et al. Metastasis is an early event in mouse mammary carcinomas and is associated with cells bearing stem cell markers. Breast Cancer Res. 2012;14:R18.
32. Chen MS,WoodwardWA, Behbod F, et al.Wnt/beta-catenin mediates radiation resistance of Sca1+ progenitors in an immortalized mammary gland cell line. J Cell Sci. 2007;120:468-477.
33. Xin L, Lawson DA, Witte ON. The Sca-1 cell surface marker enriches for a prostate-regenerating cell subpopulation that can initiate prostate tumorigenesis. Proc Natl Acad Sci USA. 2005;102:6942-6947.
34. Batts TD, Machado HL, Zhang Y, et al. Stem cell antigen-1 (Sca-1) regulates mammary tumor development and cell migration. PLoS One. 2011;6: E27841.
35. Upadhyay G,YinY,YuanH, et al. Stem cell antigen-1 enhances tumorigenicity by disruption of growth differentiation factor-10 (GDF10)-dependent TGFbeta signaling. Proc Natl Acad Sci USA. 2011;108:7820-7825.
36. Mulholland DJ, Xin L, Morim A, et al. Lin-Sca-1+CD49fhigh stem/progenitors are tumor-initiating cells in the Pten-null prostate cancer model. Cancer Res. 2009;69:8555-8562.
37. Grange C, Lanzardo S, Cavallo F, et al. Sca-1 identifies the tumor-initiating cells in mammary tumors of BALB-neuT transgenic mice. Neoplasia. 2008; 10:1433-1443.
38. Kruger JA, Kaplan CD, Luo Y, et al. Characterization of stem cell-like cancer cells in immune-competent mice. Blood. 2006;108:3906-3912.
39. Eyler CE, Rich JN. Survival of the fittest: Cancer stem cells in therapeutic resistance and angiogenesis. J Clin Oncol. 2008;26:2839-2845.
40. Eyler CE, Foo WC, LaFiura KM, et al. Brain cancer stem cells display preferential sensitivity to Akt inhibition. Stem Cells. 2008;26:3027-3036.
41. Wilson WR, Hay MP. Targeting hypoxia in cancer therapy. Nat Rev Cancer. 2011;11:393-410.
42. Govaert KM, Nijkamp MW, Emmink BL, et al. Effects of tirapazamine on experimental colorectal liver metastases after radiofrequency ablation. Br J Surg. 2012;99:567-575.
43. Mulier S, Ni Y, Jamart J, et al. Local recurrence after hepatic radiofrequency coagulation: Multivariatemeta-analysis and reviewof contributing factors. Ann Surg. 2005;242:158-171.
44. Wong SL,Mangu PB, ChotiMA, et al. American Society of Clinical Oncology 2009 clinical evidence review on radiofrequency ablation of hepatic metastases from colorectal cancer. J Clin Oncol. 2010;28:493-508.
45. Nanko M, Shimada H, Yamaoka H, et al. Micrometastatic colorectal cancer lesions in the liver. Surg Today. 1998;28:707-713.
46. Yokoyama N, Shirai Y, Ajioka Y, et al. Immunohistochemically detected hepatic micrometastases predict a high risk of intrahepatic recurrence after resection of colorectal carcinoma liver metastases. Cancer. 2002;94:1642-1647.
47. Conzelmann M, Linnemann U, Berger MR. Detection of disseminated tumour cells in the liver of cancer patients. Eur J Surg Oncol. 2005;31:977-985.
48. Heddleston JM, Li Z, Lathia JD, et al. Hypoxia inducible factors in cancer stem cells. Br J Cancer. 2010;102:789-795.
49. Visvader JE, Lindeman GJ. Cancer stem cells in solid tumours: Accumulating evidence and unresolved questions. Nat Rev Cancer. 2008;8:755-768.
50. Harrison LE, Koneru B, Baramipour P, et al. Locoregional recurrences are frequent after radiofrequency ablation for hepatocellular carcinoma. J AmColl Surg. 2003;197:759-764.
51. Tezuka M, Hayashi K, Kubota K, et al. Growth rate of locally recurrent hepatocellular carcinoma after transcatheter arterial chemoembolization: Comparing the growth rate of locally recurrent tumor with that of primary hepatocellular carcinoma. Dig Dis Sci. 2007;52:783-788.
52. Kubota K, Ina H, Okada Y, et al. Growth rate of primary single hepatocellular carcinoma: Determining optimal screening interval with contrast enhanced computed tomography. Dig Dis Sci. 2003;48:581-586.
53. Rhee TK, Young JY, Larson AC, et al. Effect of transcatheter arterial embolization on levels of hypoxia-inducible factor-1alpha in rabbit VX2 liver tumors. J Vasc Interv Radiol. 2007;18:639-645.
54. Virmani S, Rhee TK, Ryu RK, et al. Comparison of hypoxia-inducible factor-1alpha expression before and after transcatheter arterial embolization in rabbit VX2 liver tumors. J Vasc Interv Radiol. 2008;19:1483-1489.
55. Keith B, Simon MC. Hypoxia-inducible factors, stem cells, and cancer. Cell. 2007;129:465-472.
56. Todaro M, Alea MP, Di Stefano AB et al. Colon cancer stem cells dictate tumor growth and resist cell death by production of interleukin-4. Cell Stem Cell. 2007;1:389-402.
57. Dean M, Fojo T, Bates S. Tumour stem cells and drug resistance. Nat Rev Cancer. 2005;5:275-284.
58. Brown JM. The hypoxic cell: A target for selective cancer therapy - eighteenth Bruce F. Cain Memorial Award lecture. Cancer Res. 1999;59:5863-5870.
59. Wang J, Biedermann KA, Brown JM. Repair of DNA and chromosome breaks in cells exposed to SR 4233 under hypoxia or to ionizing radiation. Cancer Res. 1992;52:4473-4477.
60. Zeman EM, Brown JM, LemmonMJ, et al. SR-4233: A new bioreductive agent with high selective toxicity for hypoxic mammalian cells. Int J Radiat Oncol Biol Phys. 1986;12:1239-1242.
61. Todaro M, Alea MP, Di Stefano AB, et al. Colon cancer stem cells dictate tumor growth and resist cell death by production of interleukin-4. Cell Stem Cell. 2007;1:389-402.
62. Dylla SJ, Beviglia L, Park IK, et al. Colorectal cancer stem cells are enriched in xenogeneic tumors following chemotherapy. PLoS One. 2008;3: E2428.
63. Zhang J, Cao J, Weng Q, et al. Suppression of hypoxia-inducible factor 1alpha (HIF-1alpha) by tirapazamine is dependent on eIF2alpha phosphorylation rather than the mTORC1/4E-BP1 pathway. PLoS One. 2010;5:e13910.
64. Lencioni R, De Baere T, Burrel M, et al. Transcatheter treatment of hepatocellular carcinoma with Doxorubicin-loaded DC Bead (DEBDOX): Technical recommendations. Cardiovasc Intervent Radiol. 2012;35:980-985.