Normalization of the ovarian cancer microenvironment by SPARC

Molecular Cancer Research

Volumn 5, Issue 10, 2007, Pages 1015-1030

  Said, Neveen ^a   Socha, Matthew J ^a   Olearczyk, Jeffrey J ^a   Elmarakby, Ahmed A ^a   Imig, John D ^a   Motamed, Kouros ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

8 ISOPROSTANE; CHEMOATTRACTANT; GELATINASE A; GELATINASE B; INTEGRIN; INTERLEUKIN 6; MATRIX METALLOPROTEINASE; OSTEONECTIN; VASCULOTROPIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASCITES; ASCITES FLUID; CANCER INFILTRATION; CANCER INVASION; CARCINOGENICITY; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; FEEDBACK SYSTEM; FEMALE; GENETIC TRANSCRIPTION; MACROPHAGE ACTIVATION; MOUSE; NONHUMAN; OVARY CANCER; PRIORITY JOURNAL;

ANIMALS; ASCITIC FLUID; CARCINOMA; CELL ADHESION; CELL PROLIFERATION; CELL SURVIVAL; CHEMOKINE CCL2; DINOPROST; FEMALE; INFLAMMATION; INTEGRINS; INTERLEUKIN-6; METALLOENDOPEPTIDASES; MICE; MICE, MUTANT STRAINS; OSTEONECTIN; OVARIAN NEOPLASMS; PERITONEAL NEOPLASMS; TISSUE INHIBITOR OF METALLOPROTEINASES; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

MUS;

EID: 35948982192     PISSN: 15417786     EISSN: None     Source Type: Journal    
DOI: 10.1158/1541-7786.MCR-07-0001     Document Type: Article

References (85)

1. Kohn EC, Travers LA, Kassis J, Broome U, Klominek J. Malignant effusions are sources of fibronectin and other promigratory and proinvasive components. Diagn Cytopathol 2005;33:300-8.
2. Kassis J, Klominek J, Kohn EC. Tumor microenvironment: what can effusions teach us? Diagn Cytopathol 2005;33:316-9.
3. Mukherjee TM, Swift JG, Henderson DW. Freeze-fracture study of intercellular junctions in benign and malignant mesothelial cells in effusions and a comparison with those seen in pleural mesotheliomas (solid tumour). J Submicrosc Cytol Pathol 1988;20:195-208.
4. Fiegl M, Massoner A, Haun M, et al. Sensitive detection of tumour cells in effusions by combining cytology and fluorescence in situ hybridisation (FISH). Br J Cancer 2004;91:558-63.
5. Fiegl M, Haun M, Massoner A, et al. Combination of cytology, fluorescence in situ hybridization for aneuploidy, and reverse-transcriptase polymerase chain reaction for human mammaglobin/mammaglobin B expression improves diagnosis of malignant effusions. J Clin Oncol 2004;22:474-83.
6. Chou CH, Wei LH, Kuo ML, et al. Up-regulation of interleukin-6 in human ovarian cancer cell via a Gi/PI3K-Akt/NF-κB pathway by lysophosphatidic acid, an ovarian cancer-activating factor. Carcinogenesis 2005;26:45-52.
7. Fang X, Yu S, Bast RC, et al. Mechanisms for lysophosphatidic acid-induced cytokine production in ovarian cancer cells. J Biol Chem 2004;279:9653-61.
8. Bian D, Mahanivong C, Yu J, et al. The G12/13-RhoA signaling pathway contributes to efficient lysophosphatidic acid-stimulated cell migration. Oncogene 2006;25:2234-44.
9. Ren J, Xiao YJ, Singh LS, et al. Lysophosphatidic acid is constitutively produced by human peritoneal mesothelial cells and enhances adhesion, migration, and invasion of ovarian cancer cells. Cancer Res 2006;66:3006-14.
10. Yamada T, Sato K, Komachi M, et al. Lysophosphatidic acid (LPA) in malignant ascites stimulates motility of human pancreatic cancer cells through LPA1. J Biol Chem 2004;279:6595-605.
11. Kobayashi H. Suppression of urokinase expression and tumor metastasis by bikunin overexpression [mini-review]. Hum Cell 2001;14:233-6.
12. Fishman DA, Bafetti LM, Stack MS. Membrane-type matrix metalloproteinase expression and matrix metalloproteinase-2 activation in primary human ovarian epithelial carcinoma cells. Invasion Metastasis 1996;16:150-9.
13. Liotta LA, Kohn EC. Stromal therapy: the next step in ovarian cancer treatment. J Natl Cancer Inst 2002;94:1113-4.
14. Chu CS, Woo EY, Toll AJ, et al. Tumor-associated macrophages as a source of functional dendritic cells in ovarian cancer patients. Clin Immunol 2002;102:291-301.
15. Zavadova E, Loercher A, Verstovsek S, Verschraegen CF, Micksche M, Freedman RS. The role of macrophages in antitumor defense of patients with ovarian cancer. Hematol Oncol Clin North Am 1999;13:135-44.
16. Brekken RA, Sage EH. SPARC, a matricellular protein: at the crossroads of cell-matrix communication. Matrix Biol 2001;19:816-27.
17. Framson PE, Sage EH. SPARC and tumor growth: where the seed meets the soil? J Cell Biochem 2004;92:679-90.
18. Brekken RA, Sage EH. SPARC, a matricellular protein: at the crossroads of cell-matrix. Matrix Biol 2000;19:569-80.
19. Brekken RA, Puolakkainen P, Graves DC, Workman G, Lubkin SR, Sage EH. Enhanced growth of tumors in SPARC null mice is associated with changes in the ECM. J Clin Invest 2003;111:487-95.
20. Chlenski A, Liu S, Crawford SE, et al. SPARC is a key Schwannian-derived inhibitor controlling neuroblastoma tumor angiogenesis. Cancer Res 2002;62:7357-63.
21. Ledda F, Bravo AI, Adris S, Bover L, Mordoh J, Podhajcer OL. The expression of the secreted protein acidic and rich in cysteine (SPARC) is associated with the neoplastic progression of human melanoma. J Invest Dermatol 1997;108:210-214.
22. De S, Chen J, Narizhneva NV, et al. Molecular pathway for cancer metastasis to bone. J Biol Chem 2003;278:39044-50.
23. Chlenski A, Liu S, Guerrero LJ, et al. SPARC expression is associated with impaired tumor growth, inhibited angiogenesis and changes in the extracellular matrix. Int J Cancer 2006;118:310-6.
24. Sangaletti S, Stoppacciaro A, Guiducci C, Torrisi MR, Colombo MP. Leukocyte, rather than tumor-produced SPARC, determines stroma and collagen type IV deposition in mammary carcinoma. J Exp Med 2003;198:1475-85.
25. Said N, Motamed K. Absence of host-secreted protein acidic and rich in cysteine (SPARC) augments peritoneal ovarian carcinomatosis. Am J Pathol 2005;167:1739-52.
26. Yiu GK, Chan WY, Ng SW, et al. SPARC (secreted protein acidic and rich in cysteine) induces apoptosis in ovarian cancer cells. Am J Pathol 2001;159:609-22.
27. Said NA, Najwer I, Socha MJ, et al. SPARC inhibits LPA-mediated mesothelial-ovarian cancer cell crosstalk. Neoplasia 2007;9:23-35.
28. Said N, Najwer I, Motamed K. Secreted protein acidic and rich in cysteine (SPARC) inhibits integrin-mediated adhesion and growth factor-dependent survival signaling in ovarian cancer. Am J Pathol 2007;170:1054-63.
29. Gilles C, Bassuk JA, Pulyaeva H, Sage EH, Foidart JM, Thompson EW. SPARC/osteonectin induces matrix metalloproteinase 2 activation in human breast cancer cell lines. Cancer Res 1998;58:5529-36.
30. Koblinski JE, Kaplan-Singer BR, VanOsdol SJ, et al. Endogenous osteonectin/SPARC/BM-40 expression inhibits MDA-MB-231 breast cancer cell metastasis. Cancer Res 2005;65:7370-7.
31. Puolakkainen PA, Brekken RA, Muneer S, Sage EH. Enhanced growth of pancreatic tumors in SPARC-null mice is associated with decreased deposition of extracellular matrix and reduced tumor cell apoptosis. Mol Cancer Res 2004;2:215-24.
32. Chlenski A, Guerrero LJ, Yang Q, et al. SPARC enhances tumor stroma formation and prevents fibroblast activation. Oncogene 2007;26:4513-22.
33. Chlenski A, Liu S, Baker LJ, et al. Neuroblastoma angiogenesis is inhibited with a folded synthetic molecule corresponding to the epidermal growth factor-like module of the follistatin domain of SPARC. Cancer Res 2004;64:7420-5.
34. Koukourakis MI, Giatromanolaki A, Brekken RA, et al. Enhanced expression of SPARC/osteonectin in the tumor-associated stroma of non-small cell lung cancer is correlated with markers of hypoxia/acidity and with poor prognosis of patients. Cancer Res 2003;63:5376-80.
35. Chen J, De S, Brainard J, Byzova TV. Metastatic properties of prostate cancer cells are controlled by VEGF. Cell Commun Adhes 2004;11:1-11.
36. De S, Razorenova O, McCabe NP, O'Toole T, Qin J, Byzova TV. VEGF-integrin interplay controls tumor growth and vascularization. Proc Natl Acad Sci U S A 2005;102:7589-94.
37. Byzova TV, Goldman CK, Pampori N, et al. A mechanism for modulation of cellular responses to VEGF: activation of the integrins. Mol Cell 2000;6:851-60.
38. Zhang L, Yang N, Park JW, et al. Tumor-derived vascular endothelial growth factor up-regulates angiopoietin-2 in host endothelium and destabilizes host vasculature, supporting angiogenesis in ovarian cancer. Cancer Res 2003;63:3403-12.
39. Zhang L, Yang N, Garcia JR, et al. Generation of a syngeneic mouse model to study the effects of vascular endothelial growth factor in ovarian carcinoma. Am J Pathol 2002;161:2295-309.
40. Taverna S, Ghersi G, Ginestra A, et al. Shedding of membrane vesicles mediates fibroblast growth factor-2 release from cells. J Biol Chem 2003;278:51911-9.
41. Belotti D, Paganoni P, Manenti L, et al. Matrix metalloproteinases (MMP9 and MMP2) induce the release of vascular endothelial growth factor (VEGF) by ovarian carcinoma cells: implications for ascites formation. Cancer Res 2003;63:5224-9.
42. Graves LE, Ariztia EV, Navari JR, Matzel HJ, Stack MS, Fishman DA. Proinvasive properties of ovarian cancer ascites-derived membrane vesicles. Cancer Res 2004;64:7045-9.
43. Huang S, Van Arsdall M, Tedjarati S, et al. Contributions of stromal metalloproteinase-9 to angiogenesis and growth of human ovarian carcinoma in mice. J Natl Cancer Inst 2002;94:1134-42.
44. Janat-Amsbury MM, Yockman JW, Anderson ML, Kieback DG, Kim SW. Comparison of ID8 MOSE and VEGF-modified ID8 cell lines in an immunocompetent animal model for human ovarian cancer. Anticancer Res 2006;26:2785-9.
45. Davidson B, Goldberg I, Gotlieb WH, et al. Coordinated expression of integrin subunits, matrix metalloproteinases (MMP), angiogenic genes and Ets transcription factors in advanced-stage ovarian carcinoma: a possible activation pathway? Cancer Metastasis Rev 2003;22:103-15.
46. Davidson B, Goldberg I, Gotlieb WH, et al. The prognostic value of metalloproteinases and angiogenic factors in ovarian carcinoma. Mol Cell Endocrinol 2002;187:39-45.
47. Boyce EA, Kohn EC. Ovarian cancer in the proteomics era: diagnosis, prognosis, and therapeutics targets. Int J Gynecol Cancer 2005;15 Suppl 3:266-73.
48. Lessan K, Aguiar DJ, Oegema T, Siebenson L, Skubitz AP. CD44 and β1 integrin mediate ovarian carcinoma cell adhesion to peritoneal mesothelial cells. Am J Pathol 1999;154:1525-37.
49. Cannistra SA, Kansas GS, Niloff J, DeFranzo B, Kim Y, Ottensmeier C. Binding of ovarian cancer cells to peritoneal mesothelium in vitro is partly mediated by CD44H. Cancer Res 1993;53:3830-8.
50. Strobel T, Cannistra SA. β1-integrins partly mediate binding of ovarian cancer cells to peritoneal mesothelium in vitro. Gynecol Oncol 1999;73:362-7.
51. Byzova TV, Kim W, Midura RJ, Plow EF. Activation of integrin α(V)β(3) regulates cell adhesion and migration to bone sialoprotein. Exp Cell Res 2000;254:299-308.
52. Byzova T. Integrins in bone recognition and metastasis. J Musculoskelet Neuronal Interact 2004;4:374.
53. Costanzo ES, Lutgendorf SK, Sood AK, Anderson B, Sorosky J, Lubaroff DM. Psychosocial factors and interleukin-6 among women with advanced ovarian cancer. Cancer 2005;104:305-13.
54. Kryczek I, Grybos M, Karabon L, Klimczak A, Lange A. IL-6 production in ovarian carcinoma is associated with histiotype and biological characteristics of the tumour and influences local immunity. Br J Cancer 2000;82:621-8.
55. Yao V, Platell C, Hall JC. Peritoneal mesothelial cells produce inflammatory related cytokines. ANZ J Surg 2004;74:997-1002.
56. Laird AD, Vajkoczy P, Shawver LK, et al. SU6668 is a potent antiangiogenic and antitumor agent that induces regression of established tumors. Cancer Res 2000;60:4152-60.
57. Byzova TV, Plow EF. Activation of αvβ3 on vascular cells controls recognition of prothrombin. J Cell Biol 1998;143:2081-92.
58. Yabushita H, Shimazu M, Noguchi M, et al. Vascular endothelial growth factor activating matrix metalloproteinase in ascitic fluid during peritoneal dissemination of ovarian cancer. Oncol Rep 2003;10:89-95.
59. Wang FQ, So J, Reierstad S, Fishman DA. Vascular endothelial growth factor-regulated ovarian cancer invasion and migration involves expression and activation of matrix metalloproteinases. Int J Cancer 2006;118:879-88.
60. Stefanidakis M, Koivunen E. Cell-surface association between matrix metalloproteinases and integrins: role of the complexes in leukocyte migration and cancer progression. Blood 2006;108:1441-50.
61. Ahmed N, Riley C, Oliva K, Stutt E, Rice GE, Quinn MA. Integrin-linked kinase expression increases with ovarian tumour grade and is sustained by peritoneal tumour fluid. J Pathol 2003;201:229-37.
62. Ahmed N, Pansino F, Clyde R, et al. Overexpression of α(v)β6 integrin in serous epithelial ovarian cancer regulates extracellular matrix degradation via the plasminogen activation cascade. Carcinogenesis 2002;23:237-44.
63. Curran S, Murray GI. Matrix metalloproteinases: molecular aspects of their roles in tumour invasion and metastasis. Eur J Cancer 2000;36:1621-30.
64. Xu Y, Gaudette DC, Boynton JD, et al. Characterization of an ovarian cancer activating factor in ascites from ovarian cancer patients. Clin Cancer Res 1995;1:1223-32.
65. Huang MC, Lee HY, Yeh CC, Kong Y, Zaloudek CJ, Goetzl EJ. Induction of protein growth factor systems in the ovaries of transgenic mice overexpressing human type 2 lysophosphatidic acid G protein-coupled receptor (LPA2). Oncogene 2004;23:122-9.
66. Symowicz J, Adley BP, Woo MMM, Auersperg N, Hudson LG, Stack MS. Cyclooxygenase-2 functions as a downstream mediator of lysophosphatidic acid to promote aggressive behavior in ovarian carcinoma cells. Cancer Res 2005;65:2234-42.
67. Fishman DA, Liu Y, Ellerbroek SM, Stack MS. Lysophosphatidic acid promotes matrix metalloproteinase (MMP) activation and MMP-dependent invasion in ovarian cancer cells. Cancer Res 2001;61:3194-9.
68. Sakai T, de la Pena JM, Mosher DF. Synergism among lysophosphatidic acid, h1A integrins, and epidermal growth factor or platelet-derived growth factor in mediation of cell migration. J Biol Chem 1999;274:15480-6.
69. Milliken D, Scotton C, Raju S, Balkwill F, Wilson J. Analysis of chemokines and chemokine receptor expression in ovarian cancer ascites. Clin Cancer Res 2002;8:1108-14.
70. Murdoch C, Lewis CE. Macrophage migration and gene expression in response to tumor hypoxia. Int J Cancer 2005;117:701-8.
71. Duyndam MC, Hilhorst MC, Schluper HM, et al. Vascular endothelial growth factor-165 overexpression stimulates angiogenesis and induces cyst formation and macrophage infiltration in human ovarian cancer xenografts. Am J Pathol 2002;160:537-48.
72. Gabrilovich D, Ishida T, Oyama T, et al. Vascular endothelial growth factor inhibits the development of dendritic cells and dramatically affects the differentiation of multiple hematopoietic lineages in vivo. Blood 1998;92:4150-66.
73. Menetrier-Caux C, Montmain G, Dieu MC, et al. Inhibition of the differentiation of dendritic cells from CD34(+) progenitors by tumor cells: role of interleukin-6 and macrophage colony-stimulating factor. Blood 1998;92:4778-91.
74. Brault S, Gobeil F, Jr., Fortier A, et al. Lysophosphatidic acid induces endothelial cell death by modulating the redox environment. Am J Physiol Regul Integr Comp Physiol 2007;292:R1174-83.
75. Siess W. Platelet interaction with bioactive lipids formed by mild oxidation of low-density lipoprotein. Pathophysiol Haemost Thromb 2006;35:292-304.
76. Rask K, Zhu Y, Wang W, Hedin L, Sundfeldt K. Ovarian epithelial cancer: a role for PGE2 synthesis and signalling in malignant transformation and progression. Mol Cancer 2006;5:62.
77. Sengupta S, Xiao YJ, Xu Y. A novel laminin-induced LPA autocrine loop in the migration of ovarian cancer cells. FASEB J 2003;17:1570-2.
78. Kim KS, Sengupta S, Berk M, et al. Hypoxia enhances lysophosphatidic acid responsiveness in ovarian cancer cells and lysophosphatidic acid induces ovarian tumor metastasis in vivo. Cancer Res 2006;66:7983-90.
79. Savani RC, Zhou Z, Arguiri E, et al. Bleomycin-induced pulmonary injury in mice deficient in SPARC. Am J Physiol Lung Cell Mol Physiol 2000;279:L743-750.
80. Raines EW, Lane TF, Iruela-Arispe ML, Ross R, Sage EH. The extracellular glycoprotein SPARC interacts with platelet-derived growth factor (PDGF)-AB and -BB and inhibits the binding of PDGF to its receptors. Proc Natl Acad Sci U S A 1992;89:1281-5.
81. Motamed K, Blake DJ, Angello JC, et al. Fibroblast growth factor receptor-1 mediates the inhibition of endothelial cell proliferation and the promotion of skeletal myoblast differentiation by SPARC: a role for protein kinase A. J Cell Biochem 2003;90:408-23.
82. Kupprion C, Motamed K, Sage EH. SPARC (BM-40, osteonectin) inhibits the mitogenic effect of vascular endothelial growth factor on microvascular endothelial cells. J Biol Chem 1998;273:29635-40.
83. Roby KF, Taylor CC, Sweetwood JP, et al. Development of a syngeneic mouse model for events related to ovarian cancer. Carcinogenesis 2000;21:585-91.
84. Muller J, Yoshida T. Interaction of murine peritoneal leukocytes and mesothelial cells: in vitro model system to survey cellular events on serosal membranes during inflammation. Clin Immunol Immunopathol 1995;75:231-8.
85. Groothuis PG, Koks CAM, de Goeij AFPM, Dunselman GAJ, Arends JW, Evers JLH. Adhesion of human endometrial fragments to peritoneum in vitro. Fertil Steril 1999;71:1119-24.