Ecteinascidin-743 drug resistance in sarcoma cells: Transcriptional and cellular alterations

Biochemical Pharmacology

Volumn 66, Issue 12, 2003, Pages 2381-2395

  Shao, Li ^a,b   Kasanov, Jeremy ^a   Hornicek, Francis J ^a   Morii, Takeshi ^a,c   Fondren, Gertrude ^a   Weissbach, Lawrence ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b CENTRE FOR ADDICTION AND MENTAL HEALTH   (Canada)

^c KEIO UNIVERSITY   (Japan)

Author keywords

Chemotherapy; Chondrosarcoma; Collagen; Drug resistance; Ecteinascidin 743; Extracellular matrix

Indexed keywords

ANTINEOPLASTIC AGENT; CARRIER PROTEIN; CELL PROTEIN; COLLAGEN TYPE 1; COLLAGEN TYPE 4; GELATIN; GLYCOPROTEIN P; MESSENGER RNA; MULTIDRUG RESISTANCE PROTEIN 1; TRABECTEDIN;

AMINO ACID SEQUENCE; ARTICLE; CANCER CELL CULTURE; CELL ADHESION; CELL MIGRATION; CHONDROSARCOMA; CONCENTRATION RESPONSE; CONTROLLED STUDY; CULTURE MEDIUM; CYTOARCHITECTURE; CYTOSKELETON; DRUG CYTOTOXICITY; FLUORESCENCE ANALYSIS; HUMAN; HUMAN CELL; MOLECULAR BIOLOGY; MOLECULAR WEIGHT; MULTIDRUG RESISTANCE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RNA ANALYSIS; SARCOMA CELL; STAINING;

EID: 0344082200     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bcp.2003.08.033     Document Type: Article

References (97)

1. Demetri G.D. ET-743: the US experience in sarcomas of soft tissues. Anticancer Drugs. 13:2002;S7-S9.
2. Delaloge S., Yovine A., Taamma A., Riofrio M., Brain E., Raymond E., Cottu P., Goldwasser F., Jimeno J., Misset J.L., Marty M., Cvitkovic E. Ecteinascidin-743: a marine-derived compound in advanced, pretreated sarcoma patients - preliminary evidence of activity. J. Clin. Oncol. 19:2001;1248-1255.
3. Ryan D.P., Supko J.G., Eder J.P., Seiden M.V., Demetri G., Lynch T.J., Fischman A.J., Davis J., Jimeno J., Clark J.W. Phase I and pharmacokinetic study of Ecteinascidin 743 administered as a 72-hr continuous intravenous infusion in patients with solid malignancies. Clin. Cancer Res. 7:2001;231-242.
4. Aune G.J., Furuta T., Pommier Y. Ecteinascidin 743: a novel anticancer drug with a unique mechanism of action. Anticancer Drugs. 13:2002;545-555.
5. Takebayashi Y., Goldwasser F., Urasaki Y., Kohlhagen G., Pommier Y. Ecteinascidin 743 induces protein-linked DNA breaks in human colon carcinoma HCT116 cells and is cytotoxic independently of topoisomerase I expression. Clin. Cancer Res. 7:2001;185-191.
6. Jin S., Gorfajn B., Faircloth G., Scotto K.W. Ecteinascidin 743, a transcription-targeted chemotherapeutic that inhibits MDR1 activation. Proc. Natl. Acad. Sci. U.S.A. 97:2000;6775-6779.
7. Minuzzo M., Marchini S., Broggini M., Faircloth G., D'Incalci M., Mantovani R. Interference of transcriptional activation by the antineoplastic drug Ecteinascidin-743. Proc. Natl. Acad. Sci. U.S.A. 97:2000;6780-6784.
8. Friedman D., Hu Z., Kolb A., Gorfajn B., Scotto K.W. Ecteinascidin-743 inhibits activated but not constitutive transcription. Cancer Res. 62:2002;3377-3381.
9. Damia G., Silvestri S., Carrassa L., Filiberti L., Faircloth G.T., Liberi G., Foiani M., D'Incalci M. Unique pattern of ET-743 activity in different cellular systems with defined deficiencies in DNA-repair pathways. Int. J. Cancer. 92:2001;583-588.
10. Erba E., Bergamaschi D., Bassano L., Damia G., Ronzoni S., Faircloth G.T., D'Incalci M. Ecteinascidin-743 (ET-743), a natural marine compound, with a unique mechanism of action. Eur. J. Cancer. 37:2001;97-105.
11. Takebayashi Y., Pourquier P., Zimonjic D.B., Nakayama K., Emmert S., Ueda T., Urasaki Y., Kanzaki A., Akiyama S.-I., Popescu N., Kraemer K.H., Pommier Y. Antiproliferative activity of Ecteinascidin 743 is dependent upon transcription-coupled nucleotide-excision repair. Nat. Med. 7:2001;961-966.
12. Gottesman M.M., Fojo T., Bates S.E. Multidrug resistance in cancer: role of ATP-dependent transporters. Nat. Cancer Rev. 2:2002;48-58.
13. Mankin H.J., Cantley K.P., Lippiello L., Schiller A.L., Campbell C.J. The biology of human chondrosarcoma. Description of the cases, grading and biochemical analyses. J. Bone Joint Surg. 62A:1980;160-176.
14. Mankin H.J., Cantley K.P., Schiller A.L., Lipiello L. The biology of human chondrosarcoma. Variation in chemical composition among types and subtypes of benign and malignant cartilage tumors. J. Bone Joint Surg. 62-A:1980;176-188.
15. Unni K.K. Cartilaginous lesions of bone. J. Orthop. Sci. 6:2001;457-472.
16. Lee F.Y., Mankin H.J., Fondren G., Gebhardt M.C., Springfield D.S., Rosenberg A.E., Jennings L.C. Chondrosarcoma of bone: an assessment of outcome. J. Bone Joint Surg. 81-A:1999;326-338.
17. Fiorenza F., Abudu A., Grimer R.J., Carter S.R., Tillman R.M., Ayoub K., Mangham D.C., Davies A.M. Risk factors for survival and local control in chondrosarcoma of bone. J. Bone Joint Surg. Br. 84-B:2002;93-99.
18. Li W.W., Takahashi N., Jhanwar S., Cordon-Cardo C., Elisseyeff Y., Jimeno J., Faircloth G., Bertino J.R. Sensitivity of soft tissue sarcoma cell lines to chemotherapeutic agents: identification of Ecteinascidin-743 as a potent cytotoxic agent. Clin Cancer Res. 7:2001;2908-2911.
19. Morioka H., Weissbach L., Vogel T., Nielsen G.P., Faircloth G.T., Shao L., Hornicek F.J. Antiangiogenesis treatment combined with chemotherapy produces tumor necrosis. Clin. Cancer Res. 9:2003;1211-1217.
20. Malinin T.I., Hornicek F.J. Response of human chondrocytes cultures in vitro to human somatropin, triiodothyronine, and thyroxine. Transplant. Proc. 29:1997;2037-2039.
21. Gillies R.J., Didier N., Denton M. Determination of cell number in monolayer cultures. Anal. Biochem. 159:1986;109-113.
22. Beck W.T., Mueller T.J., Tanzer L.R. Altered surface membrane glycoproteins in vinca alkaloid-resistant human leukemic lymphoblasts. Cancer Res. 39:1979;2070-2076.
23. Davey R.A., Longhurst T.J., Davey M.W., Belov L., Harvie R.M., Hancox D., Wheeler H. Drug resistance mechanisms and MRP expression in response to epirubicin treatment in a human leukaemia cell line. Leuk. Res. 19:1995;275-282.
24. r 190,000 multidrug resistance protein, MRP, with monoclonal antibodies. Cancer Res. 54:1994;5788-5792.
25. Hipfner D.R., Almquist K.C., Stride B.D., Deeley R.G., Cole S.P.C. Location of a protease-hypersensitive region in the multidrug resistance protein (MRP) by mapping of the epitope of MRP-specific monoclonal antibody QCRL-1. Cancer Res. 56:1996;3307-3314.
26. Rehn M., Veikkola T., Kukk-Vldre E., Nakamura H., Ilmonen M., Lombardo C., Pihlajaniemi T., Alitalo K., Vuori K. Interaction of endostatin with integrins implicated in angiogenesis. Proc. Natl. Acad. Sci. U.S.A. 98:2001;1024-1029.
27. Cos S., Fernandez R., Guezmes A., Sanchez-Barcelo E.J. Influence of melatonin on invasive and metastatic properties of MCF-7 human breast cancer cells. Cancer Res. 58:1998;4383-4390.
28. López J.M., Imperial S., Valderrama R., Navarro S. An improved Bradford assay for collagen proteins. Clin. Chim. Acta. 220:1993;91-100.
29. Stefanovic B., Schnabl B., Brenner D.A. Inhibition of collagen α1(I) expression by the 5′ stem-loop as a molecular decoy. J. Biol. Chem. 277:2002;18229-18237.
30. Tromp G., Kuivaniemi H., Stacey A., Shikata H., Baldwin C.T., Jaenisch R., Prockop D.J. Structure of a full-length cDNA clone for the prepro alpha 1(I) chain of human type I procollagen. Biochem. J. 253:1988;919-922.
31. Kleiner D.E., Stetler-Stevenson W.G. Quantitative zymography: detection of picogram quantities of gelatinases. Anal. Biochem. 218:1994;325-329.
32. Hawkes SP, Li H, Taniguchi GT. Zymography and reverse zymography for detecting MMPs, and TIMPs. In: Clark L, editor. Methods in Molecular Biology: Matrix Metalloproteinase Protocols, vol. 151. Totawa, NJ: Humana Press; 2001. p. 239-410.
33. Murphy G., Crabbe T. Gelatinases A and B. Meth. Enzymol. 248:1995;470-484.
34. Hutton J.J., Tappel A.L., Udenfriend S. Cofactor and substrate requirements of collagen proline hydroxylase. Arch. Biochem. 118:1967;231-240.
35. Hata R.-I., Senoo H. L-Ascorbic acid 2-phosphate stimulates collagen accumulation, cell proliferation, and formation of a three-dimensional tissuelike substance by skin fibroblasts. J. Cell Physiol. 138:1989;8-16.
36. Kurata S., Senoo H., Hata R. Transcriptional activation of type I collagen genes by ascorbic acid 2-phosphate in human skin fibroblasts and its failure in cells from a patient with α2(I)-chain-defective Ehlers-Danlos syndrome. Exp. Cell Res. 206:1993;63-71.
37. Smith A.R., Visioli F., Hagen T.M. Vitamin C matters: increased oxidative stress in cultured human aortic endothelial cells without supplemental ascorbic acid. FASEB J. 16:2002;1102-1104.
38. Peterkofsky B., Kalwinsky D., Assad R. A substance in L-929 cell extracts which replaces the ascorbate requirement for prolyl hydroxylase in a tritium release assay for reducing cofactor; correlation of its concentration with the extent of ascorbate-independent proline hydroxylation and the level of prolyl hydroxylase activity in these cells. Arch. Biochem. Biophys. 199:1980;362-373.
39. Chu M.-L., de Wet W., Bernard M., Ramirez F. Fine structural analysis of the human pro-α1(I) collagen gene. J. Biol. Chem. 260:1985;2315-2320.
40. Takahashi N., Li W., Banerjee D., Guan Y., Wada-Takahashi Y., Brennan M.F., Chou T.-C., Scotto K.W., Bertino J.R. Sequence-dependent synergistic cytotoxicity of Ecteinascidin-743 and paclitaxel in human breast cancer cell lines in vitro and in vivo. Cancer Res. 62:2002;6909-6915.
41. Stephenson J. Cancer studies explore targeted therapy, researchers seek new prevention strategies. JAMA. 287:2002;3063-3067.
42. De Pas T., Curigliano G., Masci G., Catania C., Comandone A., Boni C., Tucci A., Pagani O., Marrocco E., de Braud F. Phase I study of 12-day prolonged infusion of high-dose ifosfamide and doxorubicin as first-line chemotherapy in adult patients with advanced soft tissue sarcomas. Ann. Oncol. 13:2002;161-166.
43. Wyman J.J., Hornstein A.M., Meitner P.A., Mak S., Verdier P., Block J.A., Pan J., Terek R.M. Multidrug resistance-1 and P-glycoprotein in human chondrosarcoma cell lines: expression correlates with decreased intracellular doxorubicin and in vitro chemoresistance. J. Orthop. Res. 17:1999;935-940.
44. Erba E., Bergamaschi D., Bassano L., Di Liberti G., Muradore I., Vignati S., Faircloth G., Jimeno J., D'Incalci M. Isolation and characterization of an IGROV-1 human ovarian cancer cell line made resistant to Ecteinascidin-743 (ET-743). Br. J. Cancer. 82:2000;1732-1739.
45. Kanzaki A., Takebayashi Y., Ren X.-Q., Miyashita H., Mori S., Akiyama S.-i., Pommier Y. Overcoming multidrug drug resistance in P-glycoprotein/MDR1- overexpressing cell lines by Ecteinascidin 743. Mol. Cancer Ther. 1:2002;1327-1334.
46. Ridley A.J. Rho family proteins: coordinating cell responses. Trends Cell. Biol. 11:2001;471-477.
47. Kobayashi T., Okada F., Fujii N., Tomita N., Ito S., Tazawa H., Aoyama T., Choi S.K., Shibata T., Fujita H., Hosokawa M. Thymosin-β4 regulates motility and metastasis of malignant mouse fibrosarcoma cells. Am. J. Pathol. 160:2002;869-882.
48. Otto A.M., Muller C.S., Huff T., Hannappel E. Chemotherapeutic drugs change actin skeleton organization and the expression of beta-thymosins in human breast cancer cells. J. Cancer Res. Clin. Oncol. 128:2002;247-256.
49. García-Rocha M., García-Gravalos M.D., Avila J. Characterization of antimitotic products from marine organisms that disorganise the microtubule network: Ecteinascidin 743, isohomohalichondrin-B and LL-15. Br. J. Cancer. 73:1996;875-883.
50. Puchner M.J.A., Giese A. Tamoxifen-resistant glioma-cell sub-populations are characterized by increased migration and proliferation. Int. J. Cancer. 86:2000;468-473.
51. Shain K.H., Dalton W.S. Cell adhesion is a key determinant in de novo multidrug resistance: new targets for the prevention of acquired MDR. Mol. Cancer Ther. 1:2001;69-78.
52. Prockop D.J., Kivirikko K.I. Collagens: molecular biology, diseases, and potentials for therapy. Annu. Rev. Biochem. 64:1995;403-434.
53. Terraz C., Brideau G., Ronco P., Rossert J. A combination of cis-acting elements is required to activate the pro-α1(I) collagen promoter in tendon fibroblasts of transgenic mice. J. Biol. Chem. 277:2002;19019-19026.
54. Sado Y., Kagawa M., Naito I., Ueki Y., Seki T., Momota R., Oohashi T., Ninomiya Y. Organization and expression of basement membrane collagen IV genes and their roles in human disorders. J. Biochem. 123:1998;767-776.
55. Di Lullo G.A., Sweeney S.M., Körkkö J., Ala-Kokko L., San Antonio J.D. Mapping the ligand-binding sites and disease-associated mutations on the most abundant protein in the human, type I collagen. J. Biol. Chem. 277:2002;4223-4231.
56. 1. Cell. 101:2000;47-56.
57. fak in human platelets stimulated by collagen. J. Biol. Chem. 276:2001;3167-3174.
58. 1 recognize the same specific amino acid sequence, GFOGER, in native (triple-helical) collagens. J. Biol. Chem. 275:2000;35-40.
59. 1 integrin down-regulates ICAM-1 expression and ICAM-1-dependent adhesion of lung cancer cells through focal adhesion kinase. Cancer Res. 61:2001;2022-2030.
60. Xu U., Rodriguez D., Petitclerc E., Kim J.J., Hangai M., Yuen S.M., Davis G.E., Brooks P.C. Proteolytic exposure of a cryptic site within collagen type IV is required for angiogenesis and tumor growth in vivo. J. Cell. Biol. 154:2001;1069-1079.
61. Ikeda K., Wang L.-H., Torres R., Zhao H., Olaso E., Eng F.J., Labrador P., Klein R., Lovett D., Yancopoulos G.D., Friedman S.L., Lin H.C. Discoidin domain receptor 2 interacts with Src and Shc following its activation by type I collagen. J. Biol. Chem. 277:2002;19206-19212.
62. Toth M., Sako Y., Ninomiya Y., Fridman R. Biosynthesis of α2(IV) and α1(IV) chains of collagen IV and interactions with matrix metalloproteinase-9. J. Cell. Physiol. 180:1999;131-139.
63. Nieto N., Friedman S.L., Cederbaum A.I. Cytochrome P450 2E1-derived reactive oxygen species mediate paracrine stimulation of collagen I protein synthesis by hepatic stellate cells. J. Biol. Chem. 277:2002;9853-9864.
64. Sun W., Hou F., Panchenko M.P., Smith B.D. A member of the Y-box protein family interacts with an upstream element on the α1(I) collagen gene. Matrix Biol. 20:2001;527-541.
65. 9 myoblasts. FEBS Lett. 513:2002;282-288.
66. Lai C.-F., Cheng S.-L. Signal transductions induced by bone morphogenetic protein-2 and transforming growth factor-β in normal human osteoblastic cells. J. Biol. Chem. 277:2002;15514-15522.
67. Stefanovic B., Hellerbrand C., Holcik M., Briendl M., Aliebhaber S., Brenner D.A. Posttranscriptional regulation of collagen α1(I) mRNA in hepatic stellate cells. Mol. Cell. Biol. 17:1997;5201-5209.
68. Ingber D., Folkman J. Inhibition of angiogenesis through modulation of collagen metabolism. Lab. Invest. 59:1988;44-51.
69. DeClerck Y.A. Interactions between tumour cells and stromal cells and proteolytic modification of the extracellular matrix by metalloproteinases in cancer. Eur. J. Cancer. 36:2000;1258-1268.
70. Hegerfeldt Y., Tusch M., Bröcker E.-B., Friedl P. Collective cell movement in primary melanoma explants: plasticity of cell-cell interaction, β1-integrin function, and migration strategies. Cancer Res. 62:2002;2125-2130.
71. Dahlman T., Lammerts E., Bergström D., Franzén Å., Westermark K., Heldin N.-E., Rubin K. Collagen type I expression in experimental anaplastic thyroid carcinoma: regulation and relevance for tumorigenicity. Int. J. Cancer. 98:2002;186-192.
72. Dvorak H.F. Tumors: wounds that do not heal. Similarities between tumor stroma generation and wound healing. N. Engl. J. Med. 315:1986;1650-1659.
73. Tannock I.F., Lee C.M., Tunggal J.K., Cowan D.S.M., Egorin M.J. Limited penetration of anticancer drugs through tumor tissue: a potential cause of resistance of solid tumors to chemotherapy. Clin. Cancer Res. 8:2002;878-884.
74. Netti P.A., Berk D.A., Swartz M.A., Grodzinsky A.J., Jain R.K. Role of extracellular matrix assembly in interstitial transport in solid tumors. Cancer Res. 60:2000;2497-2503.
75. Pogány G., Timár F., Oláh J., Harisi R., Polony G., Paku S., Bocsi J., Jeney A., Laurie G.W. Role of the basement membrane in tumor cell dormancy and cytotoxic resistance. Lab. Invest. 60:2001;274-281.
76. Sethi T., Rintoul R.C., Moore S.M., MacKinnon A.C., Salter D., Choo C., Chilvers E.R., Dransfield I., Donnelly S.C., Strieter R., Haslett C. Extracellular matrix proteins protect small cell lung cancer cells against apoptosis: a mechanism for small cell lung cancer growth and drug resistance in vivo. Nat. Med. 5:1999;662-668.
77. Lindahl G.E., Chambers R.C., Papakrivopoulou J., Dawson S.J., Jacobsen M.C., Bishop J.E., Laurent G.J. Activation of fibroblast procollagen α1(I) transcription by mechanical strain is transforming growth factor-β- dependent and involves increased binding of CCAAT-binding factor (CBF/NF-Y) at the proximal promoter. J. Biol. Chem. 277:2002;6153-6161.
78. Gaidarova S., Jiménez S.A. Inhibition of basal and transforming growth factor-β-induced stumulation of COL1A1 transcription by the DNA intercalators, mitoxantrone and WP631, in cultured human dermal fibroblasts. J. Biol. Chem. 277:2002;38737-38745.
79. Greenwel P., Inagaki Y., Hu W., Walsh M., Ramirez F. Sp1 is required for the early response of β2(I) collagen to transforming growth factor-α1. J. Biol. Chem. 272:1997;19738-19745.
80. Pessah M., Prunier C., Marais J., Ferrand N., Mazars A., Lallemand F., Gauthier J.M., Atfi A. c-Jun interacts with the corepressor TG-interacting factor (TGIF) to suppress Smad2 transcriptional activity. Proc. Natl. Acad. Sci. U.S.A. 98:2001;6198-6203.
81. Greenwel P., Tanaka S., Penkov D., Zhang W., Olive M., Moll J., Vinson C., Di Liberto M., Ramirez R. Tumor necrosis factor alpha inhibits type I collagen synthesis through repressive CCAAT/enhancer-binding proteins. Mol. Cell. Biol. 20:2000;912-918.
82. Geiser A.G., Busam K.J., Kim S.J., Lafyatis R., O'Reilly M.A., Webbink R., Roberts A.B., Sporn M.B. Regulation of the transforming growth factor-β1 and -β3 promoters by transcription factor Sp1. Gene. 129:1993;223-228.
83. Nehls M.C., Brenner D.A., Gruss H.J., Dierbach H., Mertelsmann R., Herrmann F. Mithramycin selectively inhibits collagen-alpha 1(I) gene expression in human fibroblasts. J. Clin. Invest. 92:1993;2916-2921.
84. Verrecchia F., Rossert J., Mauviel A. Blocking Sp1 transcription factor broadly inhibits extracellular matrix gene expression in vitro and in vivo: implications for the treatment of tissue fibrosis. J. Invest. Dermatol. 116:2001;755-763.
85. Zaucke F., Dinser R., Maurer P., Paulsson M. Cartilage oligomeric matrix protein (COMP) and collagen IX are sensitive markers for the differentiation state of articular primary chondrocytes. Biochem. J. 358:2001;17-24.
86. Oshima O., Haraki T., Kakuta S., Kumura Y., Nagumo M. Expression of collagen species in a cartilaginous tumor derived from a human osteogenic sarcoma. Calcif. Tissue Int. 54:1994;516-520.
87. Söderström M., Böhling T., Ekfors T., Nelimarkka L., Aro H.T., Vuorio E. Molecular profiling of human chondrosarcomas for matrix production and cancer markers. Int. J. Cancer. 100:2002;144-151.
88. Ueda Y., Oda Y., Tsuchiya H., Tomita K., Nakanishi I. Immunohistological study on collagenous proteins of benign and malignant human cartilaginous tumours of bone. Virchows Arch. A Pathol. Anat. 417:1990;291-297.
89. Aigner T., Müller S., Neureiter D., Illstrup D.M., Kirchner T., Björnsson J. Prognostic relevance of cell biologic and biochemical features in conventional chondrosarcomas. Cancer. 94:2002;2273-2281.
90. Aigner T., Loos S., Müller S., Sandell L.J., Unni K.K., Kirchner T. Cell differentiation and matrix gene expression in mesenchymal chondrosarcomas. Am. J. Pathol. 156:2000;1327-1335.
91. Chano T., Okabe H., Saeki Y., Ishizawa M., Matsumoto K., Hukuda S. Characterization of a newly established human chondrosarcoma cell line, CD-OKB. Virchows Arch. 435:1998;529-534.
92. Kunisada T., Miyazaki M., Mihara K., Gao C., Kawai A., Inoue H., Namba M. A new human chondrosarcoma cell line (OUMS-27) that maintains chondrocytic differentiation. Int. J. Cancer. 77:1998;854-859.
93. Aigner T., Dertinger S., Vornehm S.I., Dudhia J., von der Mar K., Kirchner T. Phenotypic diversity of neoplastic chondroctyes and extracellular matrix gene expression in cartilaginous neoplasms. Am. J. Pathol. 150:1997;2133-2141.
94. Takigawa M., Pan H.-O., Kinoshita A., Tajima K., Takano Y. Establishment from a human chondrosarcoma of a new immortal cell line with high tumorigenicity in vivo, which is able to form proteoglycan-rich cartilage-like nodules and to respond to insulin in vitro. Int. J. Cancer. 48:1991;717-725.
95. Reif S., Lang A., Lindquist J.N., Yata Y., Gabele E., Scanga A., Brenner D.A., Rippe R.A. The role of focal adhesion kinase-phosphatidylinositol 3-kinase-Akt signaling in hepatic stellate cell proliferation and type I collagen expression. J. Biol. Chem. 278:2003;8083-8090.
96. Inagaki Y., Nemoto T., Nakao A., ten Dijke P., Kobayashi K., Takehara K., Greenwel P. Interaction between GC box binding factors and Smad proteins modulates cell lineage-specific α2(I) collagen gene transcription. J. Biol. Chem. 276:2001;16573-16579.
97. Demers L.M., Costa L., Lipton A. Biochemical markers and skeletal metastases. Cancer. 88:2000;2919-2926.