Hypoxic and highly angiogenic Non-Tumor Tissues Surrounding Hepatocellular Carcinoma: The 'Niche' of endothelial progenitor cells

International Journal of Molecular Sciences

Volumn 11, Issue 8, 2010, Pages 2901-2909

  Yu, De Cai ^a   Chen, Jun ^a   Ding, Yi Tao ^a  

^a NANJING UNIVERSITY   (China)

Author keywords

Angiogenesis; Endothelial progenitor cells; Hepatocellular carcinoma; Liver cirrhosis

Indexed keywords

BASIC FIBROBLAST GROWTH FACTOR; CYCLOOXYGENASE 2; ENDOGLIN; ENDOSTATIN; GELATINASE B; HYPOXIA INDUCIBLE FACTOR 1ALPHA; INDUCIBLE NITRIC OXIDE SYNTHASE; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; TISSUE INHIBITOR OF METALLOPROTEINASE 2; TRANSFORMING GROWTH FACTOR BETA; VASCULOTROPIN A;

ANGIOGENESIS; CANCER RECURRENCE; CELL ACTIVATION; CELL DIFFERENTIATION; CELL HOMING; CELL MOTILITY; CHRONIC LIVER DISEASE; EPITHELIUM CELL; HUMAN; HYPOXEMIA; LIVER CELL CARCINOMA; LIVER CIRRHOSIS; LIVER RESECTION; METASTASIS; MICROVASCULARIZATION; NONHUMAN; PROTEIN EXPRESSION; REVIEW; STEM CELL; TISSUE MICROARRAY; TISSUE SECTION; TISSUE STRUCTURE; TUMOR VASCULARIZATION; ADULT STEM CELL; ANIMAL; CELL HYPOXIA; ENDOTHELIUM CELL; LIVER TUMOR; METABOLISM; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY; TUMOR MICROENVIRONMENT;

ADULT STEM CELLS; ANIMALS; CARCINOMA, HEPATOCELLULAR; CELL HYPOXIA; ENDOTHELIAL CELLS; HUMANS; LIVER NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; TUMOR MICROENVIRONMENT;

EID: 77957892417     PISSN: None     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms11082901     Document Type: Review

References (43)

1. Rafii, S.; Lyden, D. Therapeutic stem and progenitor cell transplantation for organ vascularization and regeneration. Nat. Med. 2003, 9, 702-712.
2. Asahara, T.; Masuda, H.; Takahashi, T.; Kalka, C.; Pastore, C.; Silver, M.; Kearne, M.; Magner, M.; Isner, J.M. Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circ. Res. 1999, 85, 221-228.
3. Lyden, D.; Hattori, K.; Dias, S.; Costa, C.; Blaikie, P.; Butros, L.; Chadburn, A.; Heissig, B.; Marks, W.; Witte, L.; Wu, Y.; Hicklin, D.; Zhu, Z.; Hackett, N.R.; Crystal, R.G.; Moore, M.A.; Hajjar, K.A.; Manova, K.; Benezra, R.; Rafii, S. Impaired recruitment of bone-marrow-derived endothelial and hematopoietic precursor cells blocks tumour angiogenesis and growth. Nat. Med. 2001, 7, 1194-1201.
4. Hilbe, W.; Dirnhofer, S.; Oberwasserlechner, F.; Schmid, T.; Gunsilius, E.; Hilbe, G.; Wöll, E.; Kähler, C.M. CD133 positive endothelial progenitor cells contribute to the tumour vasculature in non-small cell lung cancer. J. Clin. Pathol. 2004, 57, 965-969.
5. Dome, B.; Timar, J.; Dobos, J.; Meszaros, L.; Raso, E.; Paku, S.; Kenessey, I.; Ostoros, G.; Magyar, M.; Ladanyi, A.; Bogos, K.; Tovari, J. Identification and clinical significance of circulating endothelial progenitor cells in human non-small cell lung cancer. Cancer Res. 2006, 66, 7341-7347.
6. De Palma, M.; Venneri, M.A.; Roca, C.; Naldini, L. Targeting exogenous genes to tumour angiogenesis by transplantation of genetically modified hematopoietic stem cells. Nat. Med. 2003, 9, 789-795.
7. Beaudry, P.; Force, J.; Naumov, G.N.; Wang, A.; Baker, C.H.; Ryan, A.; Soker, S.; Johnson, B.E.; Folkman, J.; Heymach, J.V. Differential effects of vascular endothelial growth factor receptor-2 inhibitor ZD6474 on circulating endothelial progenitors and mature circulating endothelial cells.implications for use as a surrogate marker of antiangiogenic activity. Clin. Cancer Res. 2005, 11, 3514-3522.
8. Kuroi, K.; Toi, M. Circulating angiogenesis regulators in cancer patients. Int. J. Biol. Mark. 2001, 16, 5-26.
9. Yu, D.C.; Sun, X.T.; Qiu, Y.D.; Zhou, J.X.; Wu, Y.F.; Zhuang, L.Y.; Chen, J.; Ding, Y.T. Identification and clinical significance of mobilized endothelial progenitor cells in tumour vasculogenesis of hepatocellular carcinoma. Clin. Cancer Res. 2007, 13, 3814-3824.
10. Jin, H.; Aiyer, A.; Su, J.; Borgstrom, P.; Stupack, D.; Friedlander, M.; Varner, J. A homing mechanism for bone marrow-derived progenitor cell recruitment to the neovasculature. J. Clin. Invest. 2006, 116, 652-662.
11. Yao, Y.Z.; Pan, Y.M.; Chen, J.; Sun, X.T.; Qiu, Y.D.; Ding, Y.T. Endoglin (CD105) expression in angiogenesis of primary hepatocellular carcinoma.; analysis using tissue microarray and comparison with CD34 and VEGF. Ann. Clin. Lab. Sci. 2007, 37, 39-48.
12. Wang, G.L.; Semenza, G.L. General involvement of hypoxiainducible factor 1 in transcriptional response to hypoxia. Proc. Natl. Acad. Sci. USA 1993, 90, 4304-4308.
13. 2 tension. Proc. Natl. Acad. Sci. USA 1995, 92, 5510-5514.
14. Xie, H.; Song, J.; Liu, K.; Ji, H.; Shen, H.; Hu, S.; Yang, G.; Du, Y.; Zou, X.; Jin, H.; Yan, L.; Liu, J.; Fan, D. The expression of hypoxia-inducible factor-1alpha in hepatitis B virus-related hepatocellular carcinoma, correlation with patients' prognosis and hepatitis B virus X protein. Dig. Dis. Sci. 2008, 53, 3225-3233.
15. Wada, H.; Nagano, H.; Yamamoto, H.; Yang, Y.; Kondo, M.; Ota, H.; Nakamura, M.; Yoshioka, S.; Kato, H.; Damdinsuren, B.; Tang, D.; Marubashi, S.; Miyamoto, A.; Takeda, Y.; Umeshita, K.; Nakamori, S.; Sakon, M.; Dono, K.; Wakasa, K.; Monden, M. Expression pattern of angiogenic factors and prognosis after hepatic resection in hepatocellular carcinoma, importance of angiopoietin-2 and hypoxia-induced factor-1 alpha. Liver Int. 2006, 26, 414-423.
16. Yu, D.; Zhuang, L.; Sun, X.; Chen, J.; Yao, Y.; Meng, K.; Ding, Y. Particular distribution and expression pattern of endoglin (CD105) in the liver of patients with hepatocellular carcinoma. BMC Cancer 2007, 7, 122.
17. Mathonnet, M.; Descottes, B.; Valleix, D.; Labrousse, F.; Denizot, Y. VEGF in hepatocellular carcinoma and surrounding cirrhotic liver tissues. World J. Gastroenterol. 2006, 12, 830-831.
18. Deli, G.; Jin, CH.; Mu, R.; Yang, S.; Liang, Y.; Chen, D.; Makuuchi, M. Immunohistochemical assessment of angiogenesis in hepatocellular carcinoma and surrounding cirrhotic liver tissues. World J. Gastroenterol. 2005, 11, 960-963.
19. Guirouilh, J.; Le Bail, B.; Boussarie, L.; Balabaud, C.; Bioulac-Sage, P.; Desmouliere, A.; Schuppan, D.; Rosenbaum, J. Expression of hepatocyte growth factor in human hepatocellular carcinoma. J. Hepatol. 2001, 34, 78-83.
20. Rahman, M.A.; Dhar, D.K.; Yamaguchi, E.; Maruyama, S.; Sato, T.; Hayashi, H.; Ono, T.; Yamanoi, A.; Kohno, H.; Nagasue, N. Coexpression of inducible nitric oxide synthase and COX-2 in hepatocellular carcinoma and surrounding liver: Possible involvement of COX-2 in the angiogenesis of hepatitis C virus-positive cases. Clin. Cancer Res. 2001, 7, 1325-1332.
21. Zhu, X.D.; Zhang, J.B.; Zhuang, P.Y.; Zhu, H.G.; Zhang, W.; Xiong, Y.Q.; Wu, W.Z.; Wang, L.; Tang, Z.Y.; Sun, H.C. High expression of macrophage colony-stimulating factor in peritumoral liver tissue is associated with poor survival after curative resection of hepatocellular carcinoma. J. Clin. Oncol. 2008, 26, 2707-2716.
22. Liu, K.; He, X.; Lei, XZ.; Zhao, LS.; Tang, H.; Liu, L.; Lei, B.J. Pathomorphological study on location and distribution of Kupffer cells in hepatocellular carcinoma. World J. Gastroenterol. 2003, 9, 1946-1949.
23. Duff, S.E.; Li, C.; Garland, J.M.; Kumar, S. CD105 is important for angiogenesis: evidence and potential applications. FASEB J. 2003, 17, 984-992.
24. Beresford, M.J.; Harris, A.L.; Ah-See, M.; Daley, F.; Padhani, A.R.; Makris, A. The relationship of the neoangiogenic marker; endoglin; with response to neoadjuvant chemotherapy in breast cancer. Br. J. Cancer 2006, 95, 1683-1688.
25. Bodey, B.; Bodey, B., Jr.; Siegel, S.E.; Kaiser, H.E. Immunocytochemical detection of endoglin is indicative of angiogenesis in malignant melanoma. Anticancer Res. 1998, 18, 2701-2710.
26. Tanaka, F.; Otake, Y.; Yanagihara, K.; Kawano, Y.; Miyahara, R.; Li, M.; Yamada, T.; Hanaoka, N.; Inui, K.; Wada, H. Evaluation of angiogenesis in non-small cell lung cancer. Comparison between anti- CD34 antibody and anti-CD105 antibody. Clin. Cancer Res. 2001, 7, 3410-3415.
27. Li, C.; Gardy, R.; Seon, B.K.; Duff, S.E.; Abdalla, S.; Renehan, A.; O'Dwyer, S.T.; Haboubi, N.; Kumar, S. Both high intratumoral microvessel density determined using CD105 antibody and elevated plasma levels of CD105 in colorectal cancer patients correlate with poor prognosis. Br. J. Cancer 2003, 88, 1424-1431.
28. Ho, J.W.; Poon, R.T.; Sun, C.K.; Xue, W.C.; Fan, S.T. Clinicopathological and prognostic implications of endoglin (CD105) expression in hepatocellular carcinoma and its adjacent nontumorous liver. World J. Gastroenterol. 2005, 11, 176-181.
29. Ding, Y.T.; Kumar, S.; Yu, D.C. The role of endothelial progenitor cells in tumour vasculogenesis. Pathobiology 2008, 75, 265-273.
30. Bergers, G.; Benjamin, L.E. Tumorigenesis and the angiogenic switch. Nat. Rev. Cancer 2003, 3, 401-410.
31. Jeon, O.; Song, S.J.; Bhang, S.H.; Choi, C.Y.; Kim, M.J.; Kim, B.S. Additive effect of endothelial progenitor cell mobilization and bone marrow mononuclear cell transplantation on angiogenesis in mouse ischemic limbs. J. Biomed. Sci. 2007, 14, 323-330.
32. Fujiyama, S.; Amano, K.; Uehira, K.; Yoshida, M.; Nishiwaki, Y.; Nozawa, Y.; Jin, D.; Takai, S.; Miyazaki, M.; Egashira, K.; Imada, T.; Iwasaka, T.; Matsubara, H. Bone marrow monocyte lineage cells adhere on injured endothelium in a monocyte chemoattractant protein-1-dependent manner and accelerate reendothelialization as endothelial progenitor cells. Circ. Res. 2003, 93, 980-989.
33. Ho, J.W.; Pang, R.W.; Lau, C.; Sun, C.K.; Yu, W.C.; Fan, S.T.; Poon, R.T. Significance of circulating endothelial progenitor cells in hepatocellular carcinoma. Hepatology 2006, 44, 836-843.
34. Heissig, B.; Hattori, K.; Dias, S.; Friedrich, M.; Ferris, B.; Hackett, N.R.; Crystal, R.G.; Besmer, P.; Lyden, D.; Moore, M.A.; Werb, Z.; Rafii, S. Recruitment of stem and progenitor cells from the bone marrow niche requires MMP-9 mediated release of kit-ligand. Cell 2002, 109, 625-637.
35. Sherman, I.A.; Pappas, S.C.; Fisher, M.M. Hepatic microvascular changes associated with development of liver fibrosis and cirrhosis. Am. J. Physiol. 1990, 258, 460-465.
36. Akiyoshi, F.; Sata, M.; Suzuki, H.; Uchimura, Y.; Mitsuyama, K.; Matsuo, K.; Tanikawa, K. Serum vascular endothelial growth factor levels in various liver diseases. Dig. Dis. Sci. 1998, 43, 41-45.
37. Moon, E.J.; Jeong, C.H.; Jeong, J.W.; Kim, K.R.; Yu, D.Y.; Murakami, S.; Kim, C.W.; Kim, K.W. Hepatitis B virus X protein induces angiogenesis by stabilizing hypoxia-inducible factor-1alpha. FASEB J. 2004, 18, 382-384.
38. El-Assal, O.N.; Yamanoi, A.; Soda, Y.; Yamaguchi, M.; Igarashi, M.; Yamamoto, A.; Nabika, T.; Nagasue, N. Clinical significance of microvessel density and vascular endothelial growth factor expression in hepatocellular carcinoma and surrounding liver: possible involvement of vascular endothelial growth factor in the angiogenesis of cirrhotic liver. Hepatology 1998, 27, 1554-1562.
39. Liu, F.; Liu, Z.D.; Wu, N.; Cong, X.; Fei, R.; Chen, H.S.; Wei, L. Transplanted endothelial progenitor cells ameliorate carbon tetrachloride-induced liver cirrhosis in rats. Liver Transpl. 2009, 15, 1092-1100.
40. Nakamura, T.; Torimura, T.; Sakamoto, M.; Hashimoto, O.; Taniguchi, E.; Inoue, K.; Sakata, R.; Kumashiro, R.; Murohara, T.; Ueno, T.; Sata, M. Significance and therapeutic potential of endothelial progenitor cell transplantation in a cirrhotic liver rat model. Gastroenterology 2007, 133, 91-107.
41. Yu, D.; Chen, J.; Sun, X.; Zhuang, L.; Jiang, C.; Ding, Y. Mechanism of endothelial progenitor cell recruitment into neo-vessels in adjacent non-tumor tissues in hepatocellular carcinoma. BMC Cancer 2010, submitted.
42. Sieghart, W.; Fellner, S.; Reiberger, T.; Ulbrich, G.; Ferlitsch, A.; Wacheck, V.; Peck- Radosavljevic, M. Differential role of circulating endothelial progenitor cells in cirrhotic patients with or without hepatocellular carcinoma. Dig. Liver Dis. 2009, 41, 902-906.
43. Taniguchi, E.; Kin, M.; Torimura, T.; Nakamura, T.; Kumemura, H.; Hanada, S.; Hisamoto, T.; Yoshida, T.; Kawaguchi, T.; Baba, S.; Maeyama, M.; Koga, H.; Harada, M.; Kumashiro, R.; Ueno, T.; Mizuno, S.; Ikeda, H.; Imaizumi, T.; Murohara, T.; Sata, M. Endothelial progenitor cell transplantation improves the survival following liver injury in mice. Gastroenterology.2006, 130, 521-531.