Remodeling of extracellular matrix by normal and tumor-associated fibroblasts promotes cervical cancer progression

BMC Cancer

Volumn 15, Issue 1, 2015, Pages

  Fullár, Alexandra ^a   Dudás, József ^b   Oláh, Lászlóné ^a   Hollósi, Péter ^a,c   Papp, Zoltán ^a   Sobel, Gábor ^a   Karászi, Katalin ^d   Paku, Sándor ^a,c   Baghy, Kornélia ^a   Kovalszky, Ilona ^a  

^a SEMMELWEIS UNIVERSITY   (Hungary)

^b INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^c INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^d UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Cancer associated fibroblasts; Cervical cancer; Extracellular matrix remodeling; Integrins; Laminin 1; Stromal fibroblasts

Indexed keywords

ALPHA6BETA4 INTEGRIN; FIBRONECTIN; GELATINASE A; GLYCOPROTEIN; INTEGRIN; LAMININ 1; LAMININ RECEPTOR; MATRILYSIN; MATRIX METALLOPROTEINASE; OSTEOPONTIN; TRANSFORMING GROWTH FACTOR BETA1; VITRONECTIN; ACTIN; LAMININ;

ADULT; AGED; ARTICLE; CANCER GROWTH; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CLINICAL ARTICLE; COCULTURE; CONTROLLED STUDY; EXTRACELLULAR MATRIX; FEMALE; FIBROBLAST; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; MIDDLE AGED; PROTEIN EXPRESSION; PROTEIN SECRETION; TUMOR CELL; UPREGULATION; UTERINE CERVIX CANCER; BASEMENT MEMBRANE; BIOSYNTHESIS; CARCINOGENESIS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY; TISSUE MICROARRAY; UTERINE CERVIX TUMOR;

ACTINS; ADULT; AGED; BASEMENT MEMBRANE; CARCINOGENESIS; CELL PROLIFERATION; COCULTURE TECHNIQUES; EXTRACELLULAR MATRIX; FEMALE; FIBROBLASTS; FIBRONECTINS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; INTEGRINS; LAMININ; MIDDLE AGED; TISSUE ARRAY ANALYSIS; TRANSFORMING GROWTH FACTOR BETA1; UTERINE CERVICAL NEOPLASMS;

EID: 84928566124     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/s12885-015-1272-3     Document Type: Article

References (54)

1. Allen M, Louise Jones J. Jekyll and Hyde: the role of the microenvironment on the progression of cancer. J Pathol. 2011;223(2):162-76.
2. Tomakidi P, Mirancea N, Fusenig NE, Herold-Mende C, Bosch FX, Breitkreutz D. Defects of basement membrane and hemidesmosome structure correlate with malignant phenotype and stromal interactions in HaCaT-Ras xenografts. Differentiation. 1999;64(5):263-75.
3. Liotta LA, Kohn EC. The microenvironment of the tumour-host interface. Nature. 2001;411(6835):375-9.
4. Park CC, Bissell MJ, Barcellos-Hoff MH. The influence of the microenvironment on the malignant phenotype. Mol Med Today. 2000;6(8):324-9.
5. Casey TM, Eneman J, Crocker A, White J, Tessitore J, Stanley M, et al. Cancer associated fibroblasts stimulated by transforming growth factor beta1 (TGF-beta 1) increase invasion rate of tumor cells: a population study. Breast Cancer Res Treat. 2008;110(1):39-49.
6. Murphy G, Nagase H. Progress in matrix metalloproteinase research. Mol Aspects Med. 2008;29(5):290-308.
7. Sato T, Ota T, Watanabe M, Imada K, Nomizu M, Ito A. Identification of an active site of EMMPRIN for the augmentation of matrix metalloproteinase-1 and-3 expression in a co-culture of human uterine cervical carcinoma cells and fibroblasts. Gynecol Oncol. 2009;114(2):337-42.
8. Sato T, Sakai T, Noguchi Y, Takita M, Hirakawa S, Ito A. Tumor-stromal cell contact promotes invasion of human uterine cervical carcinoma cells by augmenting the expression and activation of stromal matrix metalloproteinases. Gynecol Oncol. 2004;92(1):47-56.
9. Karvinen S, Kosma VM, Tammi MI, Tammi R. Hyaluronan, CD44 and versican in epidermal keratinocyte tumours. Br J Dermatol. 2003;148(1):86-94.
10. Hartmann-Petersen S, Tammi RH, Tammi MI, Kosma VM. Depletion of cell surface CD44 in nonmelanoma skin tumours is associated with increased expression of matrix metalloproteinase 7. Br J Dermatol. 2009;160(6):1251-7.
11. Boudreau N, Bissell MJ. Extracellular matrix signaling: integration of form and function in normal and malignant cells. Curr Opin Cell Biol. 1998;10(5):640-6.
12. Niu G, Chen X. Why integrin as a primary target for imaging and therapy. Theranostics. 2011;1:30-47.
13. Bachman KE, Park BH. Duel nature of TGF-beta signaling: tumor suppressor vs. tumor promoter. Curr Opin Oncol. 2005;17(1):49-54.
14. Massuto DA, Kneese EC, Johnson GA, Burghardt RC, Hooper RN, Ing NH, et al. Transforming growth factor beta (TGFB) signaling is activated during porcine implantation: proposed role for latency-associated peptide interactions with integrins at the conceptus-maternal interface. Reproduction. 2010;139(2):465-78.
15. Barcellos-Hoff MH, Park C, Wright EG. Radiation and the microenvironment - tumorigenesis and therapy. Nat Rev Cancer. 2005;5(11):867-75.
16. Heino J, Ignotz RA, Hemler ME, Crouse C, Massague J. Regulation of cell adhesion receptors by transforming growth factor-beta. Concomitant regulation of integrins that share a common beta 1 subunit. J Biol Chem. 1989;264(1):380-8.
17. Fule T, Csapo Z, Mathe M, Tatrai P, Laszlo V, Papp Z, et al. Prognostic significance of high-risk HPV status in advanced cervical cancers and pelvic lymph nodes. Gynecol Oncol. 2006;100(3):570-8.
18. Hazelbag S, Fleuren GJ, Baelde JJ, Schuuring E, Kenter GG, Gorter A. Cytokine profile of cervical cancer cells. Gynecol Oncol. 2001;83(2):235-43.
19. Baghy K, Dezso K, Laszlo V, Fullar A, Peterfia B, Paku S, et al. Ablation of the decorin gene enhances experimental hepatic fibrosis and impairs hepatic healing in mice. Lab Invest. 2011;91(3):439-51.
20. Fullar A, Kovalszky I, Bitsche M, Romani A, Schartinger VH, Sprinzl GM, et al. Tumor cell and carcinoma-associated fibroblast interaction regulates matrix metalloproteinases and their inhibitors in oral squamous cell carcinoma. Exp Cell Res. 2012;318(13):1517-27.
21. Peterfia B, Fule T, Baghy K, Szabadkai K, Fullar A, Dobos K, et al. Syndecan-1 enhances proliferation, migration and metastasis of HT-1080 cells in cooperation with syndecan-2. PLoS One. 2012;7(6):e39474.
22. Cao XC, Zhang WR, Cao WF, Liu BW, Zhang F, Zhao HM, et al. Aquaporin3 is required for FGF-2-induced migration of human breast cancers. PLoS One. 2013;8(2):e56735.
23. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976;72:248-54.
24. Dudas J, Bitsche M, Schartinger V, Falkeis C, Sprinzl GM, Riechelmann H. Fibroblasts produce brain-derived neurotrophic factor and induce mesenchymal transition of oral tumor cells. Oral Oncol. 2011;47(2):98-103.
25. Arumugam S, Jang YC, Chen-Jensen C, Gibran NS, Isik FF. Temporal activity of plasminogen activators and matrix metalloproteinases during cutaneous wound repair. Surgery. 1999;125(6):587-93.
26. Iozzo RV, Cohen I. Altered proteoglycan gene expression and the tumor stroma. Experientia. 1993;49(5):447-55.
27. Tomasek JJ, Gabbiani G, Hinz B, Chaponnier C, Brown RA. Myofibroblasts and mechano-regulation of connective tissue remodelling. Nat Rev Mol Cell Biol. 2002;3(5):349-63.
28. Imura J, Uchida Y, Nomoto K, Ichikawa K, Tomita S, Iijima T, et al. Laminin-5 is a biomarker of invasiveness in cervical adenocarcinoma. Diagn Pathol. 2012;7:105.
29. Horejs CM, Serio A, Purvis A, Gormley AJ, Bertazzo S, Poliniewicz A, et al. Biologically-active laminin-111 fragment that modulates the epithelial-to-mesenchymal transition in embryonic stem cells. Proc Natl Acad Sci U S A. 2014;111(16):5908-13.
30. Cress AE, Rabinovitz I, Zhu W, Nagle RB. The alpha 6 beta 1 and alpha 6 beta 4 integrins in human prostate cancer progression. Cancer Metastasis Rev. 1995;14(3):219-28.
31. Yanez-Mo M, Barreiro O, Gonzalo P, Batista A, Megias D, Genis L, et al. MT1-MMP collagenolytic activity is regulated through association with tetraspanin CD151 in primary endothelial cells. Blood. 2008;112(8):3217-26.
32. Sadej R, Grudowska A, Turczyk L, Kordek R, Romanska HM. CD151 in cancer progression and metastasis: a complex scenario. Lab Invest. 2014;94(1):41-51.
33. Fujita Y, Shiomi T, Yanagimoto S, Matsumoto H, Toyama Y, Okada Y. Tetraspanin CD151 is expressed in osteoarthritic cartilage and is involved in pericellular activation of pro-matrix metalloproteinase 7 in osteoarthritic chondrocytes. Arthritis Rheum. 2006;54(10):3233-43.
34. Maffini MV, Calabro JM, Soto AM, Sonnenschein C. Stromal regulation of neoplastic development: age-dependent normalization of neoplastic mammary cells by mammary stroma. Am J Pathol. 2005;167(5):1405-10.
35. Wipff PJ, Hinz B. Myofibroblasts work best under stress. J Bodyw Mov Ther. 2009;13(2):121-7.
36. Wu SH, Zhang J, Li Y, Li JM. [Expression of ETV5 and MMP-7 in early stage cervical squamous cell carcinoma and its role in lymphatic metastasis]. Ai zheng. 2006;25(3):315-9.
37. Kivi N, Ronty M, Tarkkanen J, Auvinen P, Auvinen E. Cell culture model predicts human disease: Altered expression of junction proteins and matrix metalloproteinases in cervical dysplasia. BMC Clin Pathol. 2012;12:9.
38. Ito TK, Ishii G, Chiba H, Ochiai A. The VEGF angiogenic switch of fibroblasts is regulated by MMP-7 from cancer cells. Oncogene. 2007;26(51):7194-203.
39. Clifford G, Franceschi S, Diaz M, Munoz N, Villa LL. Chapter 3: HPV type-distribution in women with and without cervical neoplastic diseases. Vaccine. 2006;24 Suppl 3:S3/26-34.
40. Abban CY, Meneses PI. Usage of heparan sulfate, integrins, and FAK in HPV16 infection. Virology. 2010;403(1):1-16.
41. Scheffer KD, Gawlitza A, Spoden GA, Zhang XA, Lambert C, Berditchevski F, et al. Tetraspanin CD151 mediates papillomavirus type 16 endocytosis. J Virol. 2013;87(6):3435-46.
42. Aksoy P, Abban CY, Kiyashka E, Qiang W, Meneses PI. HPV16 infection of HaCaTs is dependent on beta4 integrin, and alpha6 integrin processing. Virology. 2014;449:45-52.
43. Sterk LM, Geuijen CA, van den Berg JG, Claessen N, Weening JJ, Sonnenberg A. Association of the tetraspanin CD151 with the laminin-binding integrins alpha3beta1, alpha6beta1, alpha6beta4 and alpha7beta1 in cells in culture and in vivo. J Cell Sci. 2002;115(Pt 6):1161-73.
44. Nishiuchi R, Sanzen N, Nada S, Sumida Y, Wada Y, Okada M, et al. Potentiation of the ligand-binding activity of integrin alpha3beta1 via association with tetraspanin CD151. Proc Natl Acad Sci U S A. 2005;102(6):1939-44.
45. Hasegawa M, Furuya M, Kasuya Y, Nishiyama M, Sugiura T, Nikaido T, et al. CD151 dynamics in carcinoma-stroma interaction: integrin expression, adhesion strength and proteolytic activity. Lab Invest. 2007;87(9):882-92.
46. Zoller M. Tetraspanins: push and pull in suppressing and promoting metastasis. Nat Rev Cancer. 2009;9(1):40-55.
47. Bornstein P. Matricellular proteins: an overview. J Cell Commun Signaling. 2009;3(3-4):163-5.
48. John AS, Rothman VL, Tuszynski GP. Thrombospondin-1 (TSP-1) Stimulates Expression of Integrin alpha6 in Human Breast Carcinoma Cells: A Downstream Modulator of TSP-1-Induced Cellular Adhesion. J Oncol. 2010;2010:645376.
49. Decker S, van Valen F, Vischer P. Adhesion of osteosarcoma cells to the 70-kDa core region of thrombospondin-1 is mediated by the alpha 4 beta 1 integrin. Biochem Biophys Res Commun. 2002;293(1):86-92.
50. Sweetwyne MT, Murphy-Ullrich JE. Thrombospondin1 in tissue repair and fibrosis: TGF-beta-dependent and independent mechanisms. Matrix Biol. 2012;31(3):178-86.
51. Yang N, Mosher R, Seo S, Beebe D, Friedl A. Syndecan-1 in breast cancer stroma fibroblasts regulates extracellular matrix fiber organization and carcinoma cell motility. Am J Pathol. 2011;178(1):325-35.
52. Spaeth EL, Labaff AM, Toole BP, Klopp A, Andreeff M, Marini FC. Mesenchymal CD44 expression contributes to the acquisition of an activated fibroblast phenotype via TWIST activation in the tumor microenvironment. Cancer Res. 2013;73(17):5347-59.
53. Chetty C, Vanamala SK, Gondi CS, Dinh DH, Gujrati M, Rao JS. MMP-9 induces CD44 cleavage and CD44 mediated cell migration in glioblastoma xenograft cells. Cell Signal. 2012;24(2):549-59.
54. Ludbrook SB, Barry ST, Delves CJ, Horgan CM. The integrin alphavbeta3 is a receptor for the latency-associated peptides of transforming growth factors beta1 and beta3. Biochem J. 2003;369(Pt 2):311-8.