Angiogenin secretion from hepatoma cells activates hepatic stellate cells to amplify a self-sustained cycle promoting liver cancer

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Bárcena, Cristina ^a   Stefanovic, Milica ^a   Tutusaus, Anna ^a   Martinez Nieto, Guillermo A ^a   Martinez, Laura ^a   García Ruiz, Carmen ^a,b   De Mingo, Alvaro ^a   Caballeria, Juan ^b   Fernandez Checa, José C ^a,b,c   Marí, Montserrat ^a,b   Morales, Albert ^a,b  

^a INSTITUT D INVESTIGACIONS BIOMÈDIQUES AUGUST PI I SUNYER IDIBAPS   (Spain)

^b HOSPITAL CLÍNIC   (Spain)

^c UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENIN; PANCREATIC RIBONUCLEASE; TUMOR PROTEIN;

ANIMAL; CANCER TRANSPLANTATION; CARCINOMA, HEPATOCELLULAR; HEP-G2 CELL LINE; HEPATIC STELLATE CELL; HUMAN; LIVER NEOPLASMS, EXPERIMENTAL; METABOLISM; MOUSE; PATHOLOGY; SECRETION (PROCESS); XENOGRAFT;

ANIMALS; CARCINOMA, HEPATOCELLULAR; HEP G2 CELLS; HEPATIC STELLATE CELLS; HETEROGRAFTS; HUMANS; LIVER NEOPLASMS, EXPERIMENTAL; MICE; NEOPLASM PROTEINS; NEOPLASM TRANSPLANTATION; RIBONUCLEASE, PANCREATIC;

EID: 84923115956     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep07916     Document Type: Article

References (41)

1. Hanahan, D.&Coussens, L. M. Accessories to the crime: functions of cells recruited to the tumor microenvironment. Cancer Cell 21, 309-322 (2012).
2. Hernandez-Gea, V., Toffanin, S., Friedman, S. L.&Llovet, J. M. Role of the microenvironment in the pathogenesis and treatment of hepatocellular carcinoma. Gastroenterology 144, 512-527 (2013).
3. Schrader, J.&Iredale, J. P. The inflammatory microenvironment ofHCC-the plot becomes complex. J. Hepatol. 54, 853-855 (2011).
4. Friedman, S. L.Hepatic stellate cells: protean, multifunctional, and enigmatic cells of the liver. Physiol. Rev. 88, 125-172 (2008).
5. Friedman, S. L., Sheppard, D., Duffield, J. S.&Violette, S. Therapy for fibrotic diseases: nearing the starting line. Sci. Transl. Med. 5, 167sr161, doi:10.1126/ scitranslmed.3004700 (2013).
6. Ju, M. J. et al. Peritumoral activated hepatic stellate cells predict poor clinical outcome in hepatocellular carcinoma after curative resection. Am. J. Clin. Pathol. 131, 498-510 (2009).
7. Coulouarn, C. et al. Hepatocyte-stellate cell cross-talk in the liver engenders a permissive inflammatory microenvironment that drives progression in hepatocellular carcinoma. Cancer Res. 72, 2533-2542 (2012).
8. Fett, J. W. et al. Isolation and characterization of angiogenin, an angiogenic protein from human carcinoma cells. Biochemistry 24, 5480-5486 (1985).
9. Tsuji, T. et al. Angiogenin is translocated to the nucleus of HeLa cells and is involved in ribosomal RNA transcription and cell proliferation. Cancer Res. 65, 1352-1360 (2005).
10. Shimoyama, S.&Kaminishi, M. Angiogenin: its clinical implications in malignancy. Austral-As. J. Cancer. 1, 32-36 (2001).
11. Yoshioka, N.,Wang, L., Kishimoto, K., Tsuji, T.&Hu, G. F. A therapeutic target for prostate cancer based on angiogenin-stimulated angiogenesis and cancer cell proliferation. Proc. Natl. Acad. Sci. U. S. A. 103, 14519-14524 (2006).
12. Ibaragi, S. et al. Angiogenin-stimulated rRNA transcription is essential for initiation and survival of AKT-induced prostate intraepithelial neoplasia. Mol. Cancer Res. 7, 415-424 (2009).
13. Mas, V. R., Maluf, D. G., Archer, K. J., Yanek, K. C.&Fisher, R. A. Angiogenesis soluble factors as hepatocellular carcinoma noninvasive markers for monitoring hepatitis C virus cirrhotic patients awaiting liver transplantation. Transplantation 84, 1262-1271 (2007).
14. Hisai, H. et al. Increased expression of angiogenin in hepatocellular carcinoma in correlation with tumor vascularity. Clin. Cancer Res. 9, 4852-4859 (2003).
15. Weiner, H. L., Weiner, L. H.&Swain, J. L. Tissue distribution and developmental expression of the messenger RNA encoding angiogenin. Science 237, 280-282 (1987).
16. Li, S.&Hu, G. F. Emerging role of angiogenin in stress response and cell survival under adverse conditions. J. Cell Physiol. 227, 2822-2826 (2012).
17. Hu, G. F. Neomycin inhibits angiogenin-induced angiogenesis. Proc. Natl. Acad. Sci. U. S. A. 95, 9791-9795 (1998).
18. Ibaragi, S. et al. Neamine inhibits prostate cancer growth by suppressing angiogenin-mediated rRNA transcription. Clin. Cancer Res. 15, 1981-1988 (2009).
19. Hartmann, A. et al. Hypoxia-induced up-regulation of angiogenin in human malignant melanoma. Cancer Res. 59, 1578-1583 (1999).
20. Kishimoto, K. et al.Hypoxia-induced up-regulation of angiogenin, besides VEGF, is related to progression of oral cancer. Oral Oncol. 48, 1120-1127 (2012).
21. Verselis, S. J., Olson, K. A.&Fett, J. W. Regulation of angiogenin expression in human HepG2 hepatoma cells by mediators of the acute-phase response. Biochem. Biophys. Res. Commun. 259, 178-184 (1999).
22. Moles, A., Tarrats, N., Fernandez-Checa, J. C.&Mari, M. Cathepsins B and D drive hepatic stellate cell proliferation and promote their fibrogenic potential. Hepatology 49, 1297-1307 (2009).
23. Tarrats, N. et al. Critical role of tumor necrosis factor receptor 1, but not 2, in hepatic stellate cell proliferation, extracellular matrix remodeling, and liver fibrogenesis. Hepatology 54, 319-327 (2011).
24. Morales, A. et al. Pharmacological inhibition or small interfering RNA targeting acid ceramidase sensitizes hepatoma cells to chemotherapy and reduces tumor growth in vivo. Oncogene 26, 905-916 (2007).
25. Lluis, J. M. et al. GD3 synthase overexpression sensitizes hepatocarcinoma cells to hypoxia and reduces tumor growth by suppressing the cSrc/NF-kappaB survival pathway. PloS One 4, e8059, doi:10.1371/journal.pone.0008059 (2009).
26. Moles, A. et al. Acidic sphingomyelinase controls hepatic stellate cell activation and in vivo liver fibrogenesis. Am. J. Pathol. 177, 1214-1224 (2010).
27. Sancho-Bru, P. et al. Hepatocarcinoma cells stimulate the growth, migration and expression of pro-angiogenic genes in human hepatic stellate cells. Liver Int. 30, 31-41 (2010).
28. Amann, T. et al. Activated hepatic stellate cells promote tumorigenicity of hepatocellular carcinoma. Cancer Sci. 100, 646-653 (2009).
29. Dowling, P.&Clynes, M. Conditioned media from cell lines: a complementary model to clinical specimens for the discovery of disease-specific biomarkers. Proteomics 11, 794-804 (2011).
30. Kishimoto, K., Liu, S., Tsuji, T., Olson, K. A.&Hu, G. F. Endogenous angiogenin in endothelial cells is a general requirement for cell proliferation and angiogenesis. Oncogene 24, 445-456 (2005).
31. Chan, D. A. et al. Tumor vasculature is regulated by PHD2-mediated angiogenesis and bone marrow-derived cell recruitment. Cancer Cell 15, 527-538 (2009).
32. Shimoyama, S. et al. Increased angiogenin expression in pancreatic cancer is related to cancer aggressiveness. Cancer Res. 56, 2703-2706 (1996).
33. Zhao, J. et al. Neamine inhibits cell proliferation, migration, and invasion in H7402 human hepatoma cells. Saudi Med. J. 31, 1309-1314 (2010).
34. Ricciardolo, F. L. et al. Expression of vascular remodelling markers in relation to bradykinin receptors in asthma and COPD. Thorax 68, 803-811 (2013).
35. Ning, R. et al. Neamine induces neuroprotection after acute ischemic stroke in type one diabetic rats. Neuroscience 257, 76-85 (2014).
36. Chiarelli, F. et al. Serum angiogenin concentrations in young patients with diabetes mellitus. Eur. J. Clin. Invest. 32, 110-114 (2002).
37. Oikonomou, K. A. et al. Angiogenin, angiopoietin-1, angiopoietin-2, and endostatin serum levels in inflammatory bowel disease. Inflamm. Bowel Dis. 17, 963-970 (2011).
38. Miyake, M., Goodison, S., Lawton, A., Gomes-Giacoia, E.&Rosser, C. J. Angiogenin promotes tumoral growth and angiogenesis by regulating matrix metallopeptidase-2 expression via the ERK1/2 pathway. Oncogene, doi:10.1038/ onc.2014.2 (2014).
39. Kishimoto, K. et al. Neamine inhibits oral cancer progression by suppressing angiogenin-mediated angiogenesis and cancer cell proliferation. Anticancer Res. 34, 2113-2121 (2014).
40. Bottero, V. et al. Kaposi's sarcoma-associated herpesvirus-positive primary effusion lymphoma tumor formation in NOD/SCID mice is inhibited by neomycin and neamine blocking angiogenin's nuclear translocation. J. Virol. 87, 11806-11820 (2013).
41. Coulouarn, C.&Clement, B. Stellate cells and the development of liver cancer: therapeutic potential of targeting the stroma. J. Hepatol. 60, 1306-1309 (2014).