Transcriptional activation by NFκB increases perlecan/HSPG2 expression in the desmoplastic prostate tumor microenvironment

Journal of Cellular Biochemistry

Volumn 115, Issue 7, 2014, Pages 1322-1333

  Warren, Curtis R ^a   Grindel, Brian J ^a   Francis, Lewis ^b   Carson, Daniel D ^a,c   Farach Carson, Mary C ^a,d  

^a RICE UNIVERSITY   (United States)

^b SWANSEA UNIVERSITY   (United Kingdom)

^c UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^d Rice University   (United States)

Author keywords

CYTOKINES; GENE EXPRESSION; PERLECAN HSPG2; PROSTATE CANCER; TGF ; TNF

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PERLECAN; SYNAPTOTAGMIN I; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; DNA BINDING PROTEIN; PROTEOHEPARAN SULFATE; RELA PROTEIN, HUMAN; TRANSCRIPTION FACTOR RELA; TRANSFORMING GROWTH FACTOR BETA1;

ARTICLE; CANCER CELL; CONTROLLED STUDY; GENE; HSPG2 GENE; HUMAN; HUMAN TISSUE; PRIORITY JOURNAL; PROSTATE TUMOR; PROTEIN EXPRESSION; STROMA CELL; TUMOR MICROENVIRONMENT; ACTIVE TRANSPORT; BINDING SITE; BIOSYNTHESIS; CYTOLOGY; GENETICS; MALE; METABOLISM; PROMOTER REGION; PROSTATE; TRANSCRIPTION INITIATION; TUMOR CELL LINE;

ACTIVE TRANSPORT, CELL NUCLEUS; BINDING SITES; CELL LINE, TUMOR; DNA-BINDING PROTEINS; HEPARAN SULFATE PROTEOGLYCANS; HUMANS; MALE; PROMOTER REGIONS, GENETIC; PROSTATE; PROSTATIC NEOPLASMS; STROMAL CELLS; TRANSCRIPTION FACTOR RELA; TRANSCRIPTIONAL ACTIVATION; TRANSFORMING GROWTH FACTOR BETA1; TUMOR MICROENVIRONMENT; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84900027494     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.24788     Document Type: Article

References (49)

1. Andrades JA, Han B, Becerra J, Sorgente N, Hall FL, Nimni ME,. 1999. A recombinant human TGF-beta1 fusion protein with collagen-binding domain promotes migration, growth, and differentiation of bone marrow mesenchymal cells. Exp Cell Res 250: 485-498.
2. Behrens DT, Villone D, Koch M, Brunner G, Sorokin L, Robenek H, Bruckner-Tuderman L, Bruckner P, Hansen U,. 2012. The epidermal basement membrane is a composite of separate laminin- or collagen IV-containing networks connected by aggregated perlecan, but not by nidogens. J Biol Chem 287: 18700-18709.
3. Brown LF, Guidi AJ, Schnitt SJ, Van De Water L, Iruela-Arispe ML, Yeo TK, Tognazzi K, Dvorak HF,. 1999. Vascular stroma formation in carcinoma in situ, invasive carcinoma, and metastatic carcinoma of the breast. Clin Cancer Res 5: 1041-1056.
4. Brown AJ, Alicknavitch M, D'Souza SS, Daikoku T, Kirn-Safran CB, Marchetti D, Carson DD, Farach-Carson MC,. 2008. Heparanase expression and activity influences chondrogenic and osteogenic processes during endochondral bone formation. Bone 43: 689-689.
5. Bubendorf L, Schopfer A, Wagner U, Sauter G, Moch H, Willi N, Gasser TC, Mihatsch MJ,. 2000. Metastatic patterns of prostate cancer: An autopsy study of 1,589 patients. Hum Pathol 31: 578-583.
6. Byun CH, Koh JM, Kim DK, Park SI, Lee KU, Kim GS,. 2005. Alpha-lipoic acid inhibits TNF-alpha-induced apoptosis in human bone marrow stromal cells. J Bone Miner Res 20: 1125-1135.
7. Chen Y, Shi-Wen X, van Beek J, Kennedy L, McLeod M, Renzoni EA, Bou-Gharios G, Wilcox-Adelman S, Goetinck PF, Eastwood M, Black CM, Abraham DJ, Leask A,. 2005. Matrix contraction by dermal fibroblasts requires transforming growth factor-beta/activin-linked kinase 5, heparan sulfate-containing proteoglycans, and MEK/ERK: Insights into pathological scarring in chronic fibrotic disease. Am J Pathol 167: 1699-1711.
8. Chung SW, Miles FL, Sikes RA, Cooper CR, Farach-Carson MC, Ogunnaike BA,. 2009. Quantitative modeling and analysis of the transforming growth factor beta signaling pathway. Biophys J 96: 1733-1750.
9. Comito G, Giannoni E, Segura CP, Barcellos-de-Souza P, Raspollini MR, Baroni G, Lanciotti M, Serni S, Chiarugi P,. 2013. Cancer-associated fibroblasts and M2-polarized macrophages synergize during prostate carcinoma progression. Oncogene.
10. Coulson-Thomas VJ, Coulson-Thomas YM, Gesteira TF, de Paula CA, Mader AM, Waisberg J, Pinhal MA, Friedl A, Toma L, Nader HB,. 2011. Colorectal cancer desmoplastic reaction up-regulates collagen synthesis and restricts cancer cell invasion. Cell Tissue Res 346: 223-236.
11. D'Souza S, Yang W, Marchetti D, Muir C, Farach-Carson MC, Carson DD,. 2008. HIP/RPL29 antagonizes VEGF and FGF2 stimulated angiogenesis by interfering with HS-dependent responses. J Cell Biochem 105: 1183-1193.
12. Dakhova O, Ozen M, Creighton CJ, Li R, Ayala G, Rowley D, Ittmann M,. 2009. Global gene expression analysis of reactive stroma in prostate cancer. Clin Cancer Res 15: 3979-3989.
13. Dayyani F, Gallick GE, Logothetis CJ, Corn PG,. 2011. Novel therapies for metastatic castrate-resistant prostate cancer. J Natl Cancer Inst 103: 1665-1675.
14. DiPietro LA,. 1995. Wound healing: The role of the macrophage and other immune cells. Shock 4: 233-230.
15. Farach-Carson MC, Carson DD,. 2007. Perlecan-A multifunctional extracellular proteoglycan scaffold. Glycobiology 17: 897-905.
16. Farach-Carson MC, Warren CR, Harrington DA, Carson DD,. 2013. Border patrol: Insights into the unique role of perlecan/heparan sulfate proteoglycan 2 at cell and tissue borders. Matrix Biol.
17. Freire-de-Lima L, Gelfenbeyn K, Ding Y, Mandel U, Clausen H, Handa K, Hakomori SI,. 2011. Involvement of O-glycosylation defining oncofetal fibronectin in epithelial-mesenchymal transition process. Proc Natl Acad Sci USA 108: 17690-17695.
18. Iozzo RV, Pillarisetti J, Sharma B, Murdoch AD, Danielson KG, Uitto J, Mauviel A,. 1997. Structural and functional characterization of the human perlecan gene promoter. Transcriptional activation by transforming growth factor-beta via a nuclear factor 1-binding element. J Biol Chem 272: 5219-5228.
19. Jung M, Lord MS, Cheng B, Lyons JG, Alkhouri H, Hughes JM, McCarthy SJ, Iozzo RV, Whitelock JM,. 2013. Mast cells produce novel shorter forms of perlecan that contain functional endorepellin: A role in angiogenesis and wound healing. J Biol Chem 288: 3289-3304.
20. Kohyama T, Liu X, Wen FQ, Kobayashi T, Abe S, Rennard SI,. 2004. IL-4 and IL-13 induce chemotaxis of human foreskin fibroblasts, but not human fetal lung fibroblasts. Inflammation 28: 33-37.
21. Lagace R, Grimaud JA, Schurch W, Seemayer TA,. 1985. Myofibroblastic stromal reaction in carcinoma of the breast: variations of collagenous matrix and structural glycoproteins. Virchows Arch A Pathol Anat Histopathol 408: 49-59.
22. Murdoch AD, Dodge GR, Cohen I, Tuan RS, Iozzo RV,. 1992. Primary structure of the human heparan sulfate proteoglycan from basement membrane (HSPG2/perlecan). A chimeric molecule with multiple domains homologous to the low density lipoprotein receptor, laminin, neural cell adhesion molecules, and epidermal growth factor. J Biol Chem 267: 8544-8557.
23. Nakoshi Y, Hasegawa M, Sudo A, Yoshida T, Uchida A,. 2008. Regulation of tenascin-C expression by tumor necrosis factor-alpha in cultured human osteoarthritis chondrocytes. J Rheumatol 35: 147-152.
24. O'Connor JC, Farach-Carson MC, Schneider CJ, Carson DD,. 2007. Coculture with prostate cancer cells alters endoglin expression and attenuates transforming growth factor-beta signaling in reactive bone marrow stromal cells. Mol Cancer Res 5: 585-603.
25. Olumi AF, Grossfeld GD, Hayward SW, Carroll PR, Tlsty TD, Cunha GR,. 1999. Carcinoma-associated fibroblasts direct tumor progression of initiated human prostatic epithelium. Cancer Res 59: 5002-5011.
26. Postlethwaite AE, Seyer JM,. 1995. Identification of a chemotactic epitope in human transforming growth factor-beta 1 spanning amino acid residues 368-374. J Cell Physiol 164: 587-592.
27. Rodriguez Perez CE, Nie W, Sinnett-Smith J, Rozengurt E, Yoo J,. 2011. TNF-alpha potentiates lysophosphatidic acid-induced COX-2 expression via PKD in human colonic myofibroblasts. Am J Physiol Gastrointest Liver Physiol 300: G637-G646.
28. Roecklein BA, Torok-Storb B,. 1995. Functionally distinct human marrow stromal cell lines immortalized by transduction with the human papilloma virus E6/E7 genes. Blood 85: 997-1005.
29. Ronnov-Jessen L, Petersen OW,. 1993. Induction of alpha-smooth muscle actin by transforming growth factor-beta 1 in quiescent human breast gland fibroblasts. Implications for myofibroblast generation in breast neoplasia. Lab Invest 68: 696-707.
30. Sabit H, Tsuneyama K, Shimonishi T, Harada K, Cheng J, Ida H, Saku T, Saito K, Nakanuma Y,. 2001. Enhanced expression of basement-membrane-type heparan sulfate proteoglycan in tumor fibro-myxoid stroma of intrahepatic cholangiocarcinoma. Pathol Int 51: 248-256.
31. Savoré C, Zhang C, Muir C, Liu R, Wyrwa J, Shu J, Zhau HE, Chung LW, Carson DD, Farach-Carson MC,. 2005. Perlecan knockdown in metastatic prostate cancer cells reduces heparin-binding growth factor responses in vitro and tumor growth in vivo. Clin Exp Metastasis 22: 377-390.
32. Schafer M, Werner S,. 2008. Cancer as an overhealing wound: An old hypothesis revisited. Nat Rev Mol Cell Biol 9: 628-638.
33. Schmidt A, Lorkowski S, Seidler D, Breithardt G, Buddecke E,. 2006. TGF-beta1 generates a specific multicomponent extracellular matrix in human coronary SMC. Eur J Clin Invest 36: 473-482.
34. Schofield KP, Gallagher JT, David G,. 1999. Expression of proteoglycan core proteins in human bone marrow stroma. Biochem J 343 (Pt 3): 663-668.
35. Shaw A, Gipp J, Bushman W,. 2009. The Sonic Hedgehog pathway stimulates prostate tumor growth by paracrine signaling and recapitulates embryonic gene expression in tumor myofibroblasts. Oncogene 28: 4480-4490.
36. Siegbahn A, Hammacher A, Westermark B, Heldin CH,. 1990. Differential effects of the various isoforms of platelet-derived growth factor on chemotaxis of fibroblasts, monocytes, and granulocytes. J Clin Invest 85: 916-920.
37. Sumitomo M, Tachibana M, Nakashima J, Murai M, Miyajima A, Kimura F, Hayakawa M, Nakamura H,. 1999. An essential role for nuclear factor kappa B in preventing TNF-alpha-induced cell death in prostate cancer cells. J Urol 161: 674-679.
38. Terranova VP, Hujanen ES, Loeb DM, Martin GR, Thornburg L, Glushko V,. 1986. Use of a reconstituted basement membrane to measure cell invasiveness and select for highly invasive tumor cells. Proc Natl Acad Sci USA 83: 465-469.
39. Thalmann GN, Sikes RA, Wu TT, Degeorges A, Chang SM, Ozen M, Pathak S, Chung LW,. 2000. LNCaP progression model of human prostate cancer: Androgen-independence and osseous metastasis. Prostate 44 (2): 91-103.
40. Tuxhorn JA, Ayala GE, Smith MJ, Smith VC, Dang TD, Rowley DR,. 2002. Reactive stroma in human prostate cancer: Induction of myofibroblast phenotype and extracellular matrix remodeling. Clin Cancer Res 8: 2912-2923.
41. Wang K, Vishwanath P, Eichler GS, Al-Sebaei MO, Edgar CM, Einhorn TA, Smith TF, Gerstenfeld LC,. 2006. Analysis of fracture healing by large-scale transcriptional profile identified temporal relationships between metalloproteinase and ADAMTS mRNA expression. Matrix Biol 25: 271-281.
42. Webber MM, Trakul N, Thraves PS, Bello-DeOcampo D, Chu WW, Storto PD, Huard TK, Rhim JS, Williams DE,. 1999. A human prostatic stromal myofibroblast cell line WPMY-1: A model for stromal-epithelial interactions in prostatic neoplasia. Carcinogenesis 20: 1185-1192.
43. Yagi H, Soto-Gutierrez A, Navarro-Alvarez N, Nahmias Y, Goldwasser Y, Kitagawa Y, Tilles AW, Tompkins RG, Parekkadan B, Yarmush ML,. 2010. Reactive bone marrow stromal cells attenuate systemic inflammation via sTNFR1. Mol Ther 18: 1857-1864.
44. Yamazaki M, Cheng J, Hao N, Takagi R, Jimi S, Itabe H, Saku T,. 2004. Basement membrane-type heparan sulfate proteoglycan (perlecan) and low-density lipoprotein (LDL) are co-localized in granulation tissues: A possible pathogenesis of cholesterol granulomas in jaw cysts. J Oral Pathol Med 33: 177-184.
45. Yang WD, Gomes RR, Jr., Alicknavitch M, Farach-Carson MC, Carson DD,. 2005. Perlecan domain I promotes fibroblast growth factor 2 delivery in collagen I fibril scaffolds. Tissue Eng 11: 76-89.
46. Yang L, Pang Y, Moses HL,. 2010. TGF-beta and immune cells: An important regulatory axis in the tumor microenvironment and progression. Trends Immunol 31: 220-227.
47. Yurchenco PD, Smirnov S, Mathus T,. 2002. Analysis of basement membrane self-assembly and cellular interactions with native and recombinant glycoproteins. Methods Cell Biol 69: 111-144.
48. Zcharia E, Zilka R, Yaar A, Yacoby-Zeevi O, Zetser A, Metzger S, Sarid R, Naggi A, Casu B, Ilan N, Vlodavsky I, Abramovitch R,. 2005. Heparanase accelerates wound angiogenesis and wound healing in mouse and rat models. FASEB J 19: 211-221.
49. Zhau HE, Odero-Marah V, Lue HW, Nomura T, Wang R, Chu G, Liu ZR, Zhou BP, Huang WC, Chung LW,. 2008. Epithelial to mesenchymal transition (EMT) in human prostate cancer: Lessons learned from ARCaP model. Clin Exp Metastasis 25: 601-610.