Endoglin regulates cancer-stromal cell interactions in prostate tumors

Cancer Research

Volumn 71, Issue 10, 2011, Pages 3482-3493

  Romero, Diana ^a,d   O'Neill, Christine ^a   Terzic, Aleksandra ^a   Contois, Liangru ^a   Young, Kira ^a,b   Conley, Barbara A ^a   Bergan, Raymond C ^c   Brooks, Peter C ^a,b   Vary, Calvin P H ^a,b  

^a Maine Medical Center Research Institute   (United States)

^b UNIVERSITY OF MAINE   (United States)

^c NORTHWESTERN UNIVERSITY   (United States)

^d IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ENDOGLIN; SOMATOMEDIN BINDING PROTEIN 4;

ALLELE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CANCER MODEL; CARCINOGENESIS; CELL INFILTRATION; CELL INTERACTION; CELL MIGRATION; CELL STIMULATION; CELL VIABILITY; CONTROLLED STUDY; ENDOTHELIUM CELL; FIBROBLAST; GENE DELETION; HAPLOTYPE; HUMAN; HUMAN CELL; METASTASIS POTENTIAL; MOUSE; MOUSE STRAIN; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROSTATE ADENOCARCINOMA; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SECRETION; PROTEIN SYNTHESIS REGULATION; REGULATORY MECHANISM; STROMA CELL; TUMOR VASCULARIZATION;

ANIMALS; ANTIGENS, CD; FIBROBLASTS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; INSULIN-LIKE GROWTH FACTOR BINDING PROTEIN 4; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MICE; MICE, INBRED C57BL; NEOPLASM TRANSPLANTATION; PROSTATIC NEOPLASMS; RECEPTORS, CELL SURFACE; RNA, SMALL INTERFERING; STROMAL CELLS; TRANSFORMING GROWTH FACTOR BETA;

EID: 79956101964     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-10-2665     Document Type: Article

References (49)

1. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Thun MJ. Cancer statistics, 2009. CA Cancer J Clin 2009;59:225-49.
2. Kassouf W, Ismail HR, Aprikian AG, Chevalier S. Whole-mount prostate sections reveal differential endoglin expression in stromal, epithelial, and endothelial cells with the development of prostate cancer. Prostate Cancer Prostatic Dis 2004;7:105-10. (Pubitemid 38931431)
3. Josefsson A, Wikstrom P, Granfors T, Egevad L, Karlberg L, Stattin P, et al. Tumor size, vascular density and proliferation as prognostic markers in GS 6 and GS 7 prostate tumors in patients with long follow-up and non-curative treatment. Eur Urol 2005;48:577-83. (Pubitemid 41278582)
4. Liu Y, Jovanovic B, Pins M, Lee C, Bergan RC. Over expression of endoglin in human prostate cancer suppresses cell detachment, migration and invasion. Oncogene 2002;21:8272-81. (Pubitemid 35477867)
5. Craft CS, Romero D, Vary CP, Bergan RC. Endoglin inhibits prostate cancer motility via activation of the ALK2-Smad1 1 pathway. Oncogene . 2007;26:7240-50. (Pubitemid 350085322)
6. Romero D, Terzic A, Conley BA, Craft C, Jovanovic B, Bergan R, et al. Endoglin phosphorylation by ALK2 2 contributes to the regulation of prostate cancer cell migration. Carcinogenesis 2009;31:359-66.
7. Lakshman M, Huang X, Ananthanarayanan V, Jovanovic B, Liu Y, Craft CS, et al. Endoglin suppresses human prostate cancer metastasis. Clin Exp Metastasis 2011;28:39-53.
8. Orimo A, Weinberg RA. Stromal fibroblasts in cancer: a novel tumor-promoting cell type. Cell Cycle 2006;5:1597-601. (Pubitemid 44285243)
9. Joyce JA, Pollard JW. Microenvironmental regulation of metastasis. Nat Rev Cancer 2009;9:239-52.
10. Arthur HM, Ure J, Smith AJ, Renforth G, Wilson DI, Torsney E, et al. Endoglin, an ancillary TGFbeta receptor, is required for extraembryonic angiogenesis and plays a key role in heart development. Dev Biol 2000;217:42-53. (Pubitemid 30046798)
11. Gingrich JR, Barrios RJ, Morton RA, Boyce BF, DeMayo FJ, Finegold MJ, et al. Metastatic prostate cancer in a transgenic mouse. Cancer Res 1996;56:4096-102. (Pubitemid 26304996)
12. Greenberg NM, DeMayo F, Finegold MJ, Medina D, Tilley WD, Aspinall JO, et al. Prostate cancer in a transgenic mouse. Proc Natl Acad Sci U S A 1995;92:3439-43.
13. Shappell SB, Thomas GV, Roberts RL, Herbert R, Ittmann MM, Rubin MA, et al. Prostate pathology of genetically engineered mice: definitions and classification. The consensus report from the Bar Harbor meeting of the Mouse Models of Human Cancer Consortium Prostate Pathology Committee. Cancer Res 2004;64:2270-305.
14. Lakshman M, Xu L, Ananthanarayanan V, Cooper J, Takimoto CH, Helenowski I, et al. Dietary genistein inhibits metastasis of human prostate cancer in mice. Cancer Res 2008;68:2024-32. (Pubitemid 351416590)
15. Said N, Frierson HF Jr., Chernauskas D, Conaway M, Motamed K, Theodorescu D. The role of SPARC in the TRAMP model of prostate carcinogenesis and progression. Oncogene 2009;28:3487-98.
16. Mancini ML, Terzic A, Conley BA, Oxburgh LH, Nicola T, Vary CP. Endoglin plays distinct roles in vascular smooth muscle cell recruitment and regulation of arteriovenous identity during angiogenesis. Dev Dyn 2009;238:2479-93.
17. Bhowmick NA, Chytil A, Plieth D, Gorska AE, Dumont N, Shappell S, et al. TGF-beta signaling in fibroblasts modulates the oncogenic potential of adjacent epithelia. Science 2004;303:848-51. (Pubitemid 38174665)
18. Mouta-Bellum C, Kirov A, Miceli-Libby L, Mancini ML, Petrova TV, Liaw L, et al. Organ-specific lymphangiectasia, arrested lymphatic sprouting, and maturation defects resulting from gene-targeting of the PI3K regulatory isoforms p85alpha, p55alpha, and p50alpha. Dev Dyn 2009;238:2670-9.
19. Koleva RI, Conley BA, Romero D, Riley KS, Marto JA, Lux A, et al. Endoglin structure and function: determinants of endoglin phosphorylation by transforming growth factor-beta receptors. J Biol Chem 2006;281:25110-23. (Pubitemid 44401898)
20. Carter N, Nakamoto T, Hirai H, Hunter T. EphrinA1-induced cytoskeletal re-organization requires FAK and p130(cas). Nat Cell Biol 2002;4:565-73.
21. Akalu A, Roth JM, Caunt M, Policarpio D, Liebes L, Brooks PC. Inhibition of angiogenesis and tumor metastasis by targeting a matrix immobilized cryptic extracellular matrix epitope in laminin. Cancer Res 2007;67:4353-63. (Pubitemid 46815084)
22. Bernabeu C, Lopez-Novoa JM, Quintanilla M. The emerging role of TGF-beta superfamily coreceptors in cancer. Biochim Biophys Acta 2009;1792:954-73.
23. Kalluri R, Zeisberg M. Fibroblasts in cancer. Nat Rev Cancer 2006;6:392-401.
24. Faggin E, Puato M, Zardo L, Franch R, Millino C, Sarinella F, et al. Smooth muscle-specific SM22 protein is expressed in the adventitial cells of balloon-injured rabbit carotid artery. Arterioscler Thromb Vasc Biol 1999;19:1393-404. (Pubitemid 29263008)
25. Desmouliere A, Guyot C, Gabbiani G. The stroma reaction myofibroblast: a key player in the control of tumor cell behavior. Int J Dev Biol 2004;48:509-17. (Pubitemid 39360401)
26. Dull T, Zufferey R, Kelly M, Mandel RJ, Nguyen M, Trono D, et al. A third-generation lentivirus vector with a conditional packaging system. J Virol 1998;72:8463-71. (Pubitemid 28471781)
27. Shiio Y, Donohoe S, Yi EC, Goodlett DR, Aebersold R, Eisenman RN. Quantitative proteomic analysis of Myc oncoprotein function. EMBO J 2002;21:5088-96.
28. Coppock DL, Cina-Poppe D, Gilleran S. The quiescin Q6 gene (QSCN6) is a fusion of two ancient gene families: thioredoxin and ERV1. Genomics 1998;54:460-8. (Pubitemid 29036233)
29. Koyama N, Zhang J, Huqun , Miyazawa H, Tanaka T, Su X, et al. Identification of IGFBP-6 6 as an effector of the tumor suppressor activity of SEMA3B. Oncogene 2008;27:6581-9.
30. Dong Z, Nemeth JA, Cher ML, Palmer KC, Bright RC, Fridman R. Differential regulation of matrix metalloproteinase-9, tissue inhibitor of metalloproteinase-1 1 (TIMP-1) and TIMP-2 expression in cocultures of prostate cancer and stromal cells. Int J Cancer 2001;93:507-15.
31. Durai R, Davies M, Yang W, Yang SY, Seifalian A, Goldspink G, et al. Biology of insulin-like growth factor binding protein-4 4 and its role in cancer (review). Int J Oncol 2006;28:1317-25.
32. Tennant MK, Thrasher JB, Twomey PA, Birnbaum RS, Plymate SR. Insulin-like growth factor-binding proteins (IGFBP)-4, -5, and -6 6 in the benign and malignant human prostate: IGFBP-5 messenger ribonucleic acid localization differs from IGFBP-5 protein localization. J Clin Endocrinol Metab 1996;81:3783-92. (Pubitemid 26339954)
33. Pollak M. Insulin and insulin-like growth factor signalling in neoplasia. Nat Rev Cancer 2008;8:915-28.
34. Kawada M, Inoue H, Arakawa M, Ikeda D. Transforming growth factor-beta1 1 modulates tumor-stromal cell interactions of prostate cancer through insulin-like growth factor-I. Anticancer Res 2008;28:721-30. (Pubitemid 351578914)
35. Kawada M, Inoue H, Masuda T, Ikeda D. Insulin-like growth factor I secreted from prostate stromal cells mediates tumor-stromal cell interactions of prostate cancer. Cancer Res 2006;66:4419-25.
36. Kimura G, Kasuya J, Giannini S, Honda Y, Mohan S, Kawachi M, et al. Insulin-like growth factor (IGF) system components in human prostatic cancer cell-lines: LNCaP, DU145, and PC-3 3 cells. Int J Urol 1996;3:39-46. (Pubitemid 26082891)
37. Singh SV, Warin R, Xiao D, Powolny AA, Stan SD, Arlotti JA, et al. Sulforaphane inhibits prostate carcinogenesis and pulmonary metastasis in TRAMP mice in association with increased cytotoxicity of natural killer cells. Cancer Res 2009;69:2117-25.
38. Duwel A, Eleno N, Jerkic M, Arevalo M, Bolanos JP, Bernabeu C, et al. Reduced tumor growth and angiogenesis in endoglin-haploinsufficient mice. Tumour Biol 2007;28:1-8. (Pubitemid 46012460)
39. Perez-Gomez E, Villa-Morales M, Santos J, Fernandez-Piqueras J, Gamallo C, Dotor J, et al. A role for endoglin as a suppressor of malignancy during mouse skin carcinogenesis. Cancer Res 2007;67:10268-77. (Pubitemid 350070800)
40. Mishra PJ, Humeniuk R, Medina DJ, Alexe G, Mesirov JP, Ganesan S, et al. Carcinoma-associated fibroblast-like differentiation of human mesenchymal stem cells. Cancer Res 2008;68:4331-9.
41. Zeisberg EM, Potenta S, Xie L, Zeisberg M, Kalluri R. Discovery of endothelial to mesenchymal transition as a source for carcinoma-associated fibroblasts. Cancer Res 2007;67:10123-8. (Pubitemid 350070783)
42. Conley BA, Smith JD, Guerrero-Esteo M, Bernabeu C, Vary CP. Endoglin, a TGF-beta receptor-associated protein, is expressed by smooth muscle cells in human atherosclerotic plaques. Atherosclerosis 2000;153:323-35. (Pubitemid 32120331)
43. Hirschi KK, Rohovsky SA, D'Amore PA. PDGF, TGF-beta, and heterotypic cell-cell interactions mediate endothelial cell-induced recruitment of 10T1/2 cells and their differentiation to a smooth muscle fate. J Cell Biol 1998;141:805-14. (Pubitemid 28217923)
44. Ma X, Labinaz M, Goldstein J, Miller H, Keon WJ, Letarte M, et al. Endoglin is overexpressed after arterial injury and is required for transforming growth Factor-SS-induced inhibition of smooth muscle cell migration. Arterioscler Thromb Vasc Biol 2000;20:2546-52.
45. Mancini ML, Verdi JM, Conley BA, Nicola T, Spicer DB, Oxburgh LH, et al. Endoglin is required for myogenic differentiation potential of neural crest stem cells. Dev Biol 2007;308:520-33. (Pubitemid 47223119)
46. Verona EV, Elkahloun AG, Yang J, Bandyopadhyay A, Yeh IT, Sun LZ. Transforming growth factor-beta signaling in prostate stromal cells supports prostate carcinoma growth by up-regulating stromal genes related to tissue remodeling. Cancer Res 2007;67:5737-46. (Pubitemid 46985006)
47. Iwamura M, Sluss PM, Casamento JB, Cockett AT. Insulin-like growth factor I: action and receptor characterization in human prostate cancer cell lines. Prostate 1993;22:243-52. (Pubitemid 23184735)
48. Damon SE, Maddison L, Ware JL, Plymate SR. Overexpression of an inhibitory insulin-like growth factor binding protein (IGFBP), IGFBP-4, delays onset of prostate tumor formation. Endocrinology 1998;139:3456-64. (Pubitemid 28512302)
49. Barni T, Vannelli BG, Sadri R, Pupilli C, Ghiandi P, Rizzo M, et al. Insulin-like growth factor-I (IGF-I) and its binding protein IGFBP-4 4 in human prostatic hyperplastic tissue: gene expression and its cellular localization. J Clin Endocrinol Metab 1994;78:778-83. (Pubitemid 24083328)