Significance of myofibroblasts in oral squamous cell carcinoma

Journal of Oral Pathology and Medicine

Volumn 40, Issue 3, 2011, Pages 201-207

  Thode, Christenze ^a   Jørgensen, Trine G ^a   Dabelsteen, Erik ^a   Mackenzie, Ian ^b   Dabelsteen, Sally ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Leukoplakia; Oral cancer

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; TRANSFORMING GROWTH FACTOR BETA;

CANCER SURVIVAL; CELL DIFFERENTIATION; CELLULAR DISTRIBUTION; ELECTRON MICROSCOPY; EPITHELIAL MESENCHYMAL TRANSITION; HISTOLOGY; HUMAN; IMMUNOHISTOCHEMISTRY; MOUTH CARCINOMA; MYOFIBROBLAST; NONHUMAN; ORAL SQUAMOUS CELL CARCINOMA; PRIORITY JOURNAL; PROGNOSIS; REVIEW; SQUAMOUS CELL CARCINOMA; TONGUE CARCINOMA; TUMOR GROWTH;

ACTINS; CARCINOMA, SQUAMOUS CELL; CHEMOKINES; DISEASE PROGRESSION; ENDOTHELIAL CELLS; EXTRACELLULAR MATRIX PROTEINS; FIBROBLASTS; HUMANS; MOUTH NEOPLASMS; MYOFIBROBLASTS; PROGNOSIS; STROMAL CELLS; TUMOR MICROENVIRONMENT;

EID: 79951859622     PISSN: 09042512     EISSN: 16000714     Source Type: Journal    
DOI: 10.1111/j.1600-0714.2010.00999.x     Document Type: Review

References (75)

1. Braakhuis BJ, Tabor MP, Kummer JA, Leemans CR, Brakenhoff RH. A genetic explanation of Slaughter's concept of field cancerization: evidence and clinical implications. Cancer Res 2003; 63: 1727-30.
2. Califano J, Westra WH, Meininger G, Corio R, Koch WM, Sidransky D. Genetic progression and clonal relationship of recurrent premalignant head and neck lesions. Clin Cancer Res 2000; 6: 347-52.
3. Warnakulasuriya S, Reibel J, Bouquot J, Dabelsteen E. Oral epithelial dysplasia classification systems: predictive value, utility, weaknesses and scope for improvement. J Oral Pathol Med 2008; 37: 127-33.
4. Prehn RT. Do tumors grow because of the immune response of the host? Transplant Rev 1976; 28: 34-42.
5. Lazennec G, Richmond A. Chemokines and chemokine receptors: new insights into cancer-related inflammation. Trends Mol Med 2010; 16: 133-44.
6. Kalluri R, Zeisberg M. Fibroblasts in cancer. Nat Rev Cancer 2006; 6: 392-401.
7. Erez N, Truitt M, Olson P, Hanahan D. Cancer-associated fibroblasts are activated in incipient neoplasia to orchestrate tumor-promoting inflammation in an NF-kappaB-Dependent manner. Cancer Cell 2010; 17: 135-47.
8. Mueller L, Goumas FA, Affeldt M, et al. Stromal fibroblasts in colorectal liver metastases originate from resident fibroblasts and generate an inflammatory microenvironment. Am J Pathol 2007; 171: 1608-18.
9. Nielsen BS, Rank F, Illemann M, Lund LR, Dano K. Stromal cells associated with early invasive foci in human mammary ductal carcinoma in situ coexpress urokinase and urokinase receptor. Int J Cancer 2007; 120: 2086-95.
10. Mackenzie IC, Dabelsteen E. Connective tissue influences on the expression of epithelial cell-surface antigens. Cell Tissue Res 1987; 248: 137-41.
11. Phipps RP, Borrello MA, Blieden TM Fibroblast heterogeneity in the periodontium and other tissues. J Periodontal Res 1997; 32(1 Pt 2): 159-65.
12. Gron B, Stoltze K, Andersson A, Dabelsteen E. Oral fibroblasts produce more HGF and KGF than skin fibroblasts in response to co-culture with keratinocytes. APMIS 2002; 110: 892-8.
13. Lepekhin E, Gron B, Berezin V, Bock E, Dabelsteen E. Differences in motility pattern between human buccal fibroblasts and periodontal and skin fibroblasts. Eur J Oral Sci 2002; 110: 13-20.
14. Lekic PC, Pender N, McCulloch CA. Is fibroblast heterogeneity relevant to the health, diseases, and treatments of periodontal tissues? Crit Rev Oral Biol Med 1997; 8: 253-68.
15. McGettrick HM, Smith E, Filer A, et al. Fibroblasts from different sites may promote or inhibit recruitment of flowing lymphocytes by endothelial cells. Eur J Immunol 2009; 39: 113-25.
16. Gabbiani G. Modulation of fibroblastic cytoskeletal features during wound healing and fibrosis. Pathol Res Pract 1994; 190: 851-3.
17. Santos AM, Jung J, Aziz N, Kissil JL, Pure E. Targeting fibroblast activation protein inhibits tumor stromagenesis and growth in mice. J Clin Invest 2009; 119: 3613-25.
18. Chang HY, Sneddon JB, Alizadeh AA, et al. Gene expression signature of fibroblast serum response predicts human cancer progression: similarities between tumors and wounds. PLoS Biol 2004; 2: E7.
19. Gonda TA, Varro A, Wang TC, Tycko B. Molecular biology of cancer-associated fibroblasts: can these cells be targeted in anti-cancer therapy? Semin Cell Dev Biol 2010; 21: 2-10.
20. Anderberg C, Li H, Fredriksson L, et al. Paracrine signaling by platelet-derived growth factor-CC promotes tumor growth by recruitment of cancer-associated fibroblasts. Cancer Res 2009; 69: 369-78.
21. Sugimoto H, Mundel TM, Kieran MW, Kalluri R. Identification of fibroblast heterogeneity in the tumor microenvironment. Cancer Biol Ther 2006; 5: 1640-6.
22. Anderberg C, Pietras K. On the origin of cancer-associated fibroblasts. Cell Cycle 2009; 8: 1461-2.
23. De Wever O, Demetter P, Mareel M, Bracke M. Stromal myofibroblasts are drivers of invasive cancer growth. Int J Cancer 2008; 123: 2229-38.
24. Ronnov-Jessen L, Bissell MJ. Breast cancer by proxy: can the microenvironment be both the cause and consequence? Trends Mol Med 2009; 15: 5-13.
25. Ostman A, Augsten M. Cancer-associated fibroblasts and tumor growth - bystanders turning into key players. Curr Opin Genet Dev 2009; 19: 67-73.
26. Orimo A, Weinberg RA. Stromal fibroblasts in cancer: a novel tumor-promoting cell type. Cell Cycle 2006; 5: 1597-601.
27. Baglole CJ, Ray DM, Bernstein SH, et al. More than structural cells, fibroblasts create and orchestrate the tumor microenvironment. Immunol Invest 2006; 35: 297-325.
28. Xouri G, Christian S. Origin and function of tumor stroma fibroblasts. Semin Cell Dev Biol 2010; 21: 40-6.
29. Eyden B. The myofibroblast: a study of normal, reactive and neoplastic tissues, with an emphasis on ultrastructure. J Submicrosc Cytol Pathol 2007; 7-166.
30. 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.
31. Desmouliere A. Factors influencing myofibroblast differentiation during wound healing and fibrosis. Cell Biol Int 1995; 19: 471-6.
32. De Wever O, Mareel M. Role of tissue stroma in cancer cell invasion. J Pathol 2003; 200: 429-47.
33. Serini G, Gabbiani G. Mechanisms of myofibroblast activity and phenotypic modulation. Exp Cell Res 1999; 250: 273-83.
34. Hinz B, Phan SH, Thannickal VJ, Galli A, Bochaton-Piallat ML, Gabbiani G. The myofibroblast: one function, multiple origins. Am J Pathol 2007; 170: 1807-16.
35. McAnulty RJ. Fibroblasts and myofibroblasts: their source, function and role in disease. Int J Biochem Cell Biol 2007; 39: 666-71.
36. Barth PJ, Schenck zu ST, Ramaswamy A, Moll R. CD34+ fibrocytes, alpha-smooth muscle antigen-positive myofibroblasts, and CD117 expression in the stroma of invasive squamous cell carcinomas of the oral cavity, pharynx, and larynx. Virchows Arch 2004; 444: 231-4.
37. De Boeck A, Narine K, De Neve W, Mareel M, Bracke M, De Wever O. Resident and bone marrow-derived mesenchymal stem cells in head and neck squamous cell carcinoma. Oral Oncol 2010; 46: 336-42.
38. Werner S, Grose R. Regulation of wound healing by growth factors and cytokines. Physiol Rev 2003; 83: 835-70.
39. Toullec A, Gerald D, Despouy G, et al. Oxidative stress promotes myofibroblast differentiation and tumour spreading. EMBO Mol Med 2010; 2: 211-30.
40. Lewis MP, Lygoe KA, Nystrom ML, et al. Tumour-derived TGF-beta1 modulates myofibroblast differentiation and promotes HGF/SF-dependent invasion of squamous carcinoma cells. Br J Cancer 2004; 90: 822-32.
41. Hawinkels LJ, Verspaget HW, van der Reijden JJ, et al. Active TGF-beta1 correlates with myofibroblasts and malignancy in the colorectal adenoma-carcinoma sequence. Cancer Sci 2009; 100: 663-70.
42. Lygoe KA, Wall I, Stephens P, Lewis MP. Role of vitronectin and fibronectin receptors in oral mucosal and dermal myofibroblast differentiation. Biol Cell 2007; 99: 601-14.
43. Tejada ML, Yu L, Dong J, et al. Tumor-driven paracrine platelet-derived growth factor receptor alpha signaling is a key determinant of stromal cell recruitment in a model of human lung carcinoma. Clin Cancer Res 2006; 12: 2676-88.
44. Gutschalk CM, Herold-Mende CC, Fusenig NE, Mueller MM. Granulocyte colony-stimulating factor and granulocyte-macrophage colony-stimulating factor promote malignant growth of cells from head and neck squamous cell carcinomas in vivo. Cancer Res 2006; 66: 8026-36.
45. Daly AJ, McIlreavey L, Irwin CR. Regulation of HGF and SDF-1 expression by oral fibroblasts--implications for invasion of oral cancer. Oral Oncol 2008; 44: 646-51.
46. Karnoub AE, Dash AB, Vo AP, et al. Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nature 2007; 449: 557-63.
47. Rossi D, Zlotnik A. The biology of chemokines and their receptors. Annu Rev Immunol 2000; 18: 217-42.
48. Gibbs S, Ponec M. Intrinsic regulation of differentiation markers in human epidermis, hard palate and buccal mucosa. Arch Oral Biol 2000; 45: 149-58.
49. Hill MW, Mackenzie IC. The influence of differing connective tissue substrates on the maintenance of adult stratified squamous epithelia. Cell Tissue Res 1984; 237: 473-8.
50. Mackenzie IC, Hill MW. Maintenance of regionally specific patterns of cell proliferation and differentiation in transplanted skin and oral mucosa. Cell Tissue Res 1981; 219: 597-607.
51. De Wever O, Nguyen QD, Van HL, et al. Tenascin-C and SF/HGF produced by myofibroblasts in vitro provide convergent pro-invasive signals to human colon cancer cells through RhoA and Rac. FASEB J 2004; 18: 1016-8.
52. Matsumoto K, Horikoshi M, Rikimaru K, Enomoto S. A study of an in vitro model for invasion of oral squamous cell carcinoma. J Oral Pathol Med 1989; 18: 498-501.
53. Ronnov-Jessen L, Petersen OW. 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 1993; 68: 696-707.
54. Kellermann MG, Sobral LM, da Silva SD, et al. Mutual paracrine effects of oral squamous cell carcinoma cells and normal oral fibroblasts: induction of fibroblast to myofibroblast transdifferentiation and modulation of tumor cell proliferation. Oral Oncol 2008; 44: 509-17.
55. Jung DW, Che ZM, Kim J, et al. Tumor-stromal crosstalk in invasion of oral squamous cell carcinoma: a pivotal role of CCL7. Int J Cancer 2010; 127: 332-44.
56. Costea DE, Kulasekara K, Neppelberg E, Johannessen AC, Vintermyr OK. Species-specific fibroblasts required for triggering invasiveness of partially transformed oral keratinocytes. Am J Pathol 2006; 168: 1889-97.
57. Nielsen JD, Moeslund M, Wandall HH, Dabelsteen S. Influences of tumor stroma on the malignant phenotype. J Oral Pathol Med 2008; 37: 412-6.
58. Gaggioli C, Hooper S, Hidalgo-Carcedo C, et al. Fibroblast-led collective invasion of carcinoma cells with differing roles for RhoGTPases in leading and following cells. Nat Cell Biol 2007; 9: 1392-400.
59. Bissell MJ, Radisky DC, Rizki A, Weaver VM, Petersen OW. The organizing principle: microenvironmental influences in the normal and malignant breast. Differentiation 2002; 70: 537-46.
60. Costea DE, Johannessen AC, Vintermyr OK. Fibroblast control on epithelial differentiation is gradually lost during in vitro tumor progression. Differentiation 2005; 73: 134-41.
61. Vered M, Allon I, Buchner A, Dayan D. Stromal myofibroblasts accompany modifications in the epithelial phenotype of tongue dysplastic and malignant lesions. Cancer Microenviron 2009; 2: 49-57.
62. Etemad-Moghadam S, Khalili M, Tirgary F, Alaeddini M. Evaluation of myofibroblasts in oral epithelial dysplasia and squamous cell carcinoma. J Oral Pathol Med 2009; 38: 639-43.
63. Kellermann MG, Sobral LM, da Silva SD, et al. Myofibroblasts in the stroma of oral squamous cell carcinoma are associated with poor prognosis. Histopathology 2007; 51: 849-53.
64. Vered M, Dobriyan A, Dayan D, et al. Tumor-host histopathologic variables, stromal myofibroblasts and risk score, are significantly associated with recurrent disease in tongue cancer. Cancer Sci 2010; 101: 274-80.
65. Bryne M, Thrane PS, Dabelsteen E. Loss of expression of blood group antigen H is associated with cellular invasion and spread of oral squamous cell carcinomas. Cancer 1990; 66: 2118-23.
66. Bryne M, Koppang HS, Lilleng R, Stene T, Bang G, Dabelsteen E. New malignancy grading is a better prognostic indicator than Broders' grading in oral squamous cell carcinomas. J Oral Pathol Med 1989; 18: 432-7.
67. Wandall HH, Dabelsteen S, Sorensen JA, Krogdahl A, Mandel U, Dabelsteen E. Molecular basis for the presence of glycosylated onco-foetal fibronectin in oral carcinomas: the production of glycosylated onco-foetal fibronectin by carcinoma cells. Oral Oncol 2007; 43: 301-9.
68. Turley EA, Veiseh M, Radisky DC, Bissell MJ. Mechanisms of disease: epithelial-mesenchymal transition - does cellular plasticity fuel neoplastic progression? Nat Clin Pract Oncol 2008; 5: 280-90.
69. Vered M, Dayan D, Yahalom R, et al. Cancer-associated fibroblasts and epithelial-mesenchymal transition in metastatic oral tongue squamous cell carcinoma. Int J Cancer 2010; 127: 1356-62.
70. Martinez-Ferrer M, Afshar-Sherif AR, Uwamariya C, de CB, Davidson JM, Bhowmick NA. Dermal transforming growth factor-beta responsiveness mediates wound contraction and epithelial closure. Am J Pathol 2010; 176: 98-107.
71. Kawashiri S, Tanaka A, Noguchi N, et al. Significance of stromal desmoplasia and myofibroblast appearance at the invasive front in squamous cell carcinoma of the oral cavity. Head Neck 2009; 31: 1346-53.
72. Illemann M, Hansen U, Nielsen HJ, et al. Leading-edge myofibroblasts in human colon cancer express plasminogen activator inhibitor-1. Am J Clin Pathol 2004; 122: 256-65.
73. Offersen BV, Nielsen BS, Hoyer-Hansen G, et al. The myofibroblast is the predominant plasminogen activator inhibitor-1-expressing cell type in human breast carcinomas. Am J Pathol 2003; 163: 1887-99.
74. Lindberg P, Larsson A, Nielsen BS. Expression of plasminogen activator inhibitor-1, urokinase receptor and laminin gamma-2 chain is an early coordinated event in incipient oral squamous cell carcinoma. Int J Cancer 2006; 118: 2948-56.
75. Gao S, Krogdahl A, Sorensen JA, Kousted TM, Dabelsteen E, Andreasen PA. Overexpression of protease nexin-1 mRNA and protein in oral squamous cell carcinomas. Oral Oncol 2008; 44: 309-13.