Silencing of S100A4, a metastasis-associated protein, in endothelial cells inhibits tumor angiogenesis and growth

Angiogenesis

Volumn 17, Issue 1, 2014, Pages 17-26

  Ochiya, Takahiro ^a   Takenaga, Keizo ^b   Endo, Hideya ^c  

^a NATIONAL CANCER CENTER RESEARCH INSTITUTE   (Japan)

^b SHIMANE UNIVERSITY   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

Author keywords

Angiogenesis; Endothelial cells; S100A4; siRNA; Therapy; Tumor

Indexed keywords

CALVASCULIN; SMALL INTERFERING RNA;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CANCER INHIBITION; CONTROLLED STUDY; DOWN REGULATION; ENDOTHELIUM CELL; GENE EXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; IN VITRO STUDY; MALE; MOLECULARLY TARGETED THERAPY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN FUNCTION; TUMOR VASCULARIZATION; TUMOR XENOGRAFT; UPREGULATION;

MURINAE;

ANIMALS; CELL LINE, TUMOR; GENE SILENCING; HETEROGRAFTS; HUMANS; MALE; MICE; MICE, NUDE; NEOPLASM METASTASIS; NEOPLASM PROTEINS; NEOPLASM TRANSPLANTATION; NEOVASCULARIZATION, PATHOLOGIC; PROSTATIC NEOPLASMS; S100 PROTEINS;

EID: 84892813886     PISSN: 09696970     EISSN: 15737209     Source Type: Journal    
DOI: 10.1007/s10456-013-9372-7     Document Type: Article

References (48)

1. +-binding protein family. Genes Dev 3:1086-1093
2. Davies BR, O'Donnell M, Durkan GC, Rudland PS, Barraclough R, Neal DE et al (2002) Expression of S100A4 protein is associated with metastasis and reduced survival in human bladder cancer. J Pathol 196:292-299
3. Platt-Higgins AM, Renshaw CA, West CR, Winstanley JH, De Silva Rudland S, Barraclough R et al (2000) Comparison of the metastasis-inducing protein S100A4 (p9ka) with other prognostic markers in human breast cancer. Int J Cancer 89:198-208
4. Rosty C, Ueki T, Argani P, Jansen M, Yeo CJ, Cameron JL et al (2002) Overexpression of S100A4 in pancreatic ductal adenocarcinomas is associated with poor differentiation and DNA hypomethylation. Am J Pathol 160:45-50
5. Rudland PS, Platt-Higgins A, Renshaw C, West CR, Winstanley JH, Robertson L et al (2000) Prognostic significance of the metastasis-inducing protein S100A4 (p9Ka) in human breast cancer. Cancer Res 60:1595-1603
6. Takenaga K, Nakanishi H, Wada K, Suzuki M, Matsuzaki O, Matsuura A et al (1997) Increased expression of S100A4, a metastasis-associated gene, in human colorectal adenocarcinomas. Clin Cancer Res 3:2309-2316
7. Yonemura Y, Endou Y, Kimura K, Fushida S, Bandou E, Taniguchi K et al (2000) Inverse expression of S100A4 and E-cadherin is associated with metastatic potential in gastric cancer. Clin Cancer Res 6:4234-4242
8. Lukanidin E, Georgiev G (1996) Metastasis-related mts1 gene. In: Günthert U, Birchmeier W (eds) Current topics in microbiology and immunology: attempts to understand metastasis formation, vol 213/II. Springer, Berlin, pp 171-195
9. Ambartsumian NS, Grigorian MS, Larsen IF, Karlstrøm O, Sidenius N, Rygaard J et al (1996) Metastasis of mammary carcinomas in GRS/A hybrid mice transgenic for the mts1 gene. Oncogene 13:1621-1630
10. Davies MP, Rudland PS, Robertson L, Parry EW, Jolicoeur P, Barraclough R (1996) Expression of the calcium-binding protein S100A4 (p9Ka) in MMTV-neu transgenic mice induces metastasis of mammary tumours. Oncogene 13:1631-1637
11. Barraclough R (1998) Calcium-binding protein S100A4 in health and disease. Biochim Biophys Acta 1998(1448):190-199
12. Grum-Schwensen B, Klingelhofer J, Berg CH, El-Naaman C, Grigorian M, Lukanidin E et al (2005) Suppression of tumor development and metastasis formation in mice lacking the S100A4(mts1) gene. Cancer Res 65:3772-3780
13. Hua J, Chen D, Fu H, Zhang R, Shen W, Liu S et al (2010) Short hairpin RNA-mediated inhibition of S100A4 promotes apoptosis and suppresses proliferation of BGC823 gastric cancer cells in vitro and in vivo. Cancer Lett 292:41-47
14. Zhang G, Li M, Jin J, Bai Y, Yang C (2011) Knockdown of S100A4 decreases tumorigenesis and metastasis in osteosarcoma cells by repression of matrix metalloproteinase-9. Asian Pac J Cancer Prev 12:2075-2080
15. Takenaga K, Nygren J, Zelenina M, Ohira M, Iuchi T, Lukanidin E, Sjöquist M, Kozlova EN (2007) Modified expression of Mts1/S100A4 protein in C6 glioma cells or surrounding astrocytes affects migration of tumor cells in vitro and in vivo. Neurobiol Dis 25:455-463
16. Saleem M, Kweon MH, Johnson JJ, Adhami VM, Elcheva I, Khan N et al (2006) S100A4 accelerates tumorigenesis and invasion of human prostate cancer through the transcriptional regulation of matrix metalloproteinase 9. Proc Natl Acad Sci USA 103:14825-14830
17. Li N, Song MM, Chen XH, Liu LH, Li FS (2012) S100A4 siRNA inhibits human pancreatic cancer cell invasion in vitro. Biomed Environ Sci 25:465-470
18. Chen D, Zheng XF, Yang ZY, Liu DX, Zhang GY, Jiao XL, Zhao H (2012) S100A4 silencing blocks invasive ability of esophageal squamous cell carcinoma cells. World J Gastroenterol 18:915-922
19. Ambartsumian N, Klingelhöfer J, Grigorian M, Christensen C, Kriajevska M, Tulchinsky E et al (2001) The metastasis-associated Mts1(S100A4) protein could act as an angiogenic factor. Oncogene 20:4685-4695
20. Schmidt-Hansen B, Ornås D, Grigorian M, Klingelhöfer J, Tulchinsky E, Lukanidin E et al (2004) Extracellular S100A4(mts1) stimulates invasive growth of mouse endothelial cells and modulates MMP-13 matrix metalloproteinase activity. Oncogene 23:5487-5495
21. Schmidt-Hansen B, Klingelhöfer J, Grum-Schwensen B, Christensen A, Andresen S, Kruse C, Hansen T et al (2004) Functional significance of metastasis-inducing S100A4(Mts1) in tumor-stroma interplay. J Biol Chem 279:24498-24504
22. Endo H, Takenaga K, Kanno T, Satoh H, Mori S (2002) Methionine aminopeptidase 2 is a new target for the metastasis-associated protein, S100A4. J Biol Chem 277:26396-26402
23. Takenaga K, Nakamura Y, Sakiyama S, Hasegawa Y, Sato K, Endo H (1994) Binding of pEL98 protein, an S100-related calcium-binding protein, to nonmuscle tropomyosin. J Cell Biol 124:757-768
24. Yanai N, Satoh T, Obinata M (1991) Endothelial cells create a hematopoietic inductive microenvironment preferential to erythropoiesis in the mouse spleen. Cell Struct Funct 16:87-93
25. Namba K, Abe M, Saito S, Satake M, Ohmoto T, Watanabe T, Sato Y (2000) Indispensable role of the transcription factor PEBP2/CBF in angiogenic activity of a murine endothelial cell MSS31. Oncogene 19:106-114
26. Takahashi T, Yamaguchi S, Chida K, Shibuya M (2001) A single autophosphorylation site on KDR/Flk-1 is essential for VEGF-A-dependent activation of PLC-gamma and DNA synthesis in vascular endothelial cells. EMBO J 20:2768-2778
27. Takeshita F, Minakuchi Y, Nagahara S, Honma K, Sasaki H, Hirai K et al (2005) Efficient delivery of small interfering RNA to bone-metastatic tumors by using atelocollagen in vivo. Proc Natl Acad Sci USA 102:12177-12182
28. Fidler IJ (1973) Selection of successive tumour lines for metastasis. Nat New Biol 1242:148-149
29. Taniguchi S, Kawano T, Kakunaga T, Baba T (1986) Differences in expression of a variant actin between low and high metastatic B16 melanoma. J Biol Chem 261:6100-6106
30. Takenaga K, Nakamura Y, Endo H, Sakiyama S (1994) Involvement of S100-related calcium-binding protein pEL98 (or mts1) in cell motility and tumor cell invasion. Jpn J Cancer Res 85:831-839
31. Bussolino F, Di Renzo MF, Ziche M, Bocchietto E, Olivero M, Naldini L et al (1992) Hepatocyte growth factor is a potent angiogenic factor which stimulates endothelial cell motility and growth. J Cell Biol 119:629-641
32. Saadoun S, Papadopoulos MC, Hara-Chikuma M, Verkman AS (2005) Impairment of angiogenesis and cell migration by targeted aquaporin-1 gene disruption. Nature 434:786-792
33. Antoine M, Wirz W, Tag CG, Gressner AM, Wycislo M, Müller R et al (2006) Fibroblast growth factor 16 and 18 are expressed in human cardiovascular tissues and induce on endothelial cells migration but not proliferation. Biochem Biophys Res Commun 346:224-233
34. Mu H, Ohashi R, Yan S, Chai H, Yang H, Lin P et al (2006) Adipokine resistin promotes in vitro angiogenesis of human endothelial cells. Cardiovasc Res 70:146-157
35. Izumi Y, Kim-Mitsuyama S, Yoshiyama M, Omura T, Shiota M, Matsuzawa A et al (2005) Important role of apoptosis signal-regulating kinase 1 in ischemia-induced angiogenesis. Arterioscler Thromb Vasc Biol 25:1877-1883
36. Jurisic G, Iolyeva M, Proulx ST, Halin C, Detmar M (2010) Thymus cell antigen 1 (Thy1, CD90) is expressed by lymphatic vessels and mediates cell adhesion to lymphatic endothelium. Exp Cell Res 316:2982-2992
37. Maiese K, Hou J, Chong ZZ, Shang YC (2009) A fork in the path: developing therapeutic inroads with FoxO proteins. Oxid Med Cell Longev 2:119-129
38. Backen AC, Cole CL, Lau SC, Clamp AR, McVey R, Gallagher JT et al (2007) Heparan sulphate synthetic and editing enzymes in ovarian cancer. Br J Cancer 96:1544-1548
39. Spurbeck WW, Ng CY, Strom TS, Vanin EF, Davidoff AM (2002) Enforced expression of tissue inhibitor of matrix metalloproteinase-3 affects functional capillary morphogenesis and inhibits tumor growth in a murine tumor model. Blood 100:3361-3368
40. Lee S, Bui Nguyen TM, Kovalenko D, Adhikari N, Grindle S, Polster SP et al (2010) Sprouty1 inhibits angiogenesis in association with up-regulation of p21 and p27. Mol Cell Biochem 338:255-261
41. Iruela-Arispe ML, Lombardo M, Krutzsch HC, Lawler J, Roberts DD (1999) Inhibition of angiogenesis by thrombospondin-1 is mediated by 2 independent regions within the type 1 repeats. Circulation 100:1423-1431
42. Cabrita MA, Christofori G (2008) Sprouty proteins, masterminds of receptor tyrosine kinase signaling. Angiogenesis 11:53-62
43. Honma K, Iwao-Koizumi K, Takeshita F, Yamamoto Y, Yoshida T, Nishio K et al (2008) RPN2 gene confers docetaxel resistance in breast cancer. Nat Med 14:939-948
44. Ochiya T, Takahama Y, Nagahara S, Sumita Y, Hisada A, Itoh H et al (1999) New delivery system for plasmid DNA in vivo using atelocollagen as a carrier material: the minipellet. Nat Med 5:707-710
45. Hayashi Y, Edwards NA, Proescholdt MA, Oldfield EH, Merrill MJ (2007) Regulation and function of aquaporin-1 in glioma cells. Neoplasia 9:777-787
46. Loreto C, Galanti C, Almeida LE, Leonardi R, Pannone G, Musumeci G et al (2012) Expression and localization of aquaporin-1 in temporomandibular joint disc with internal derangement. J Oral Pathol Med 41:642-647
47. Horcajadas JA, Mínguez P, Dopazo J, Esteban FJ, Domínguez F, Giudice LC et al (2008) Controlled ovarian stimulation induces a functional genomic delay of the endometrium with potential clinical implications. J Clin Endocrinol Metab 93:4500-4510
48. Sonvilla G, Allerstorfer S, Stättner S, Karner J, Klimpfinger M, Fischer H et al (2008) FGF18 in colorectal tumour cells: autocrine and paracrine effects. Carcinogenesis 29:15-24