Insights into the role of components of the tumor microenvironment in oral carcinoma call for new therapeutic approaches

Experimental Cell Research

Volumn 325, Issue 2, 2014, Pages 58-64

  Salo, Tuula ^a,b,c   Vered, Marilena ^d,e   Bello, Ibrahim O ^f   Nyberg, Pia ^b   Bitu, Carolina Cavalcante ^a   Zlotogorski Hurvitz, Ayelet ^e,g   Dayan, Dan ^e  

^a UNIVERSITY OF OULU   (Finland)

^b OULU UNIVERSITY HOSPITAL   (Finland)

^c UNIVERSITY OF HELSINKI   (Finland)

^d SHEBA MEDICAL CENTER   (Israel)

^e TEL AVIV UNIVERSITY   (Israel)

^f KING SAUD UNIVERSITY   (Saudi Arabia)

^g RABIN MEDICAL CENTER   (Israel)

Author keywords

Antiangiogenesis; Carcinoma associated fibroblasts; Hypoxia; Inflammation; Oral cancer microenvironment; Oral cancer prognosis; Organotypic invasion assay; Proteases

Indexed keywords

CHEMOKINE; COLLAGEN FIBER; CYTOKINE; ENZYME; FIBRONECTIN; GROWTH FACTOR; PROTEINASE;

ANGIOGENESIS; CANCER CELL; CANCER GROWTH; CANCER PROGNOSIS; CANCER TISSUE; CARCINOMA ASSOCIATED FIBROBLAST; CARCINOMA ASSOCIATED INFLAMMATORY CELL; CELL HYPOXIA; DIAGNOSTIC APPROACH ROUTE; EXTRACELLULAR MATRIX; FIBROBLAST; HUMAN; IMMUNOCOMPETENT CELL; MOUTH CARCINOMA; OUTCOME ASSESSMENT; PHENOTYPE; PRIORITY JOURNAL; REVIEW; TUMOR INVASION; TUMOR MICROENVIRONMENT;

ANTIANGIOGENESIS; CARCINOMA ASSOCIATED FIBROBLASTS; HYPOXIA; INFLAMMATION; ORAL CANCER MICROENVIRONMENT; ORAL CANCER PROGNOSIS; ORGANOTYPIC INVASION ASSAY; PROTEASES;

ANIMALS; ANTINEOPLASTIC AGENTS; HUMANS; NEOPLASMS; TUMOR MICROENVIRONMENT;

EID: 84902841361     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2013.12.029     Document Type: Review

References (49)

1. Siegel R., Naishadham D., Jemal A. Cancer statistics, 2013. CA Cancer J. Clin. 2013, 63:11-30.
2. Coelho K.R. Challenges of the oral cancer burden in India. J. Cancer Epidemiol. 2012, 2012:701932.
3. Printz C. Radiation oncologists work to protect patients' oral health: in the process, researchers also make strides in treating head and neck cancers. Cancer 2012, 118:3223-3224.
4. Anneroth G., Batsakis J., Luna M. Review of the literature and a recommended system of malignancy grading in oral squamous cell carcinomas. Scand. J. Dent. Res. 1987, 95:229-249.
5. Bryne M., Koppang H.S., 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, 18:432-437.
6. Brandwein-Gensler M., Teixeira M.S., Lewis C.M., Lee B., Rolnitzky L., Hille J.J., Genden E., Urken M.L., Wang B.Y. Oral squamous cell carcinoma: histologic risk assessment, but not margin status, is strongly predictive of local disease-free and overall survival. Am. J. Surg. Pathol. 2005, 29:167-178.
7. Brandwein-Gensler M., Smith R.V., Wang B., Penner C., Theilken A., Broughel D., Schiff B., Owen R.P., Smith J., Sarta C., Hebert T., Nason R., Ramer M., DeLacure M., Hirsch D., Myssiorek D., Heller K., Prystowsky M., Schlecht N.F., Negassa A. Validation of the histologic risk model in a new cohort of patients with head and neck squamous cell carcinoma. Am. J. Surg. Pathol. 2010, 34:676-688.
8. Li Y., Bai S., Carroll W., Dayan D., Dort J.C., Heller K., Jour G., Lau H., Penner C., Prystowsky M., Rosenthal E., Schlecht N.F., Smith R.V., Urken M., Vered M., Wang B., Wenig B., Negassa A., Brandwein-Gensler M. Validation of the risk model: high-risk classification and tumor pattern of invasion predict outcome for patients with low-stage oral cavity squamous cell carcinoma. Head Neck Pathol. 2013, 7:211-223.
9. Almangush A., Bello I.O., Keski-Säntti H., Mäkinen L.K., Kauppila J.H., Pukkila M., Hagström J., Laranne J., Tommola S., Nieminen O., Soini Y., Kosma V.M., Koivunen P., Grenman R., Leivo I., Salo T. Depth of invasion, tumor budding, and worst pattern of invasion: prognostic indicators in early-stage oral tongue cancer. Head Neck 2013, 10.1002/hed.23380.
10. Madar S., Goldstein I., Rotter V. 'Cancer associated fibroblasts'-more than meets the eye. Trends Mol. Med. 2013, 19:447-453.
11. Bello I.O., Vered M., Dayan D., Dobriyan A., Yahalom R., Alanen K., Nieminen P., Kantola S., Läärä E., Salo T. Cancer-associated fibroblasts, a parameter of the tumor microenvironment, overcomes carcinoma-associated parameters in the prognosis of patients with mobile tongue cancer. Oral Oncol. 2011, 47:33-38.
12. 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.
13. Vered M., Dobriyan A., Dayan D., Yahalom R., Talmi Y.P., Bedrin L., Barshack I., Taicher S. Tumor-host histopathologic variables, stromal myofibroblasts and risk score, are significantly associated with recurrent disease in tongue cancer. Cancer Sci. 2010, 101:274-280.
14. Vered M., Dayan D., Yahalom R., Dobriyan A., Barshack I., Bello I.O., Kantola S., Salo T. Cancer-associated fibroblasts and epithelial-mesenchymal transition in metastatic oral tongue squamous cell carcinoma. Int. J. Cancer 2010, 127:1356-1362.
15. Kellermann M.G., Sobral L.M., da Silva S.D., Zecchin K.G., Graner E., Lopes M.A., Kowalski L.P., Coletta R.D. 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, 44:509-517.
16. Costea D.E., Johannessen A.C., Vintermyr O.K. Fibroblast control on epithelial differentiation is gradually lost during in vitro tumor progression. Differentiation 2005, 73:134-141.
17. Teppo S., Sundquist E., Vered M., Holappa H., Parkkisenniemi J., Rinaldi T., Lehenkari P., Grenman R., Dayan D., Risteli J., Salo T., Nyberg P. The hypoxic tumor microenvironment regulates invasion of aggressive oral carcinoma cells. Exp. Cell Res. 2013, 319:376-389.
18. Salo S., Bitu C., Merkku K., Nyberg P., Bello I.O., Vuoristo J., Sutinen M., Vähänikkilä H., Lehtonen S., Costea D.E., Kauppila J., Lehenkari P., Dayan D., Vered M., Risteli J., Salo T. Human bone marrow mesenchymal stem cells induce collagen production and tongue cancer invasion. PLoS One 2013, 8:e77692.
19. Dayan D., Salo T., Salo S., Nyberg P., Nurmenniemi S., Costea D.E., Vered M. Molecular crosstalk between cancer cells and tumor microenvironment components suggests potential targets for new therapeutic approaches in mobile tongue cancer. Cancer Med. 2012, 1:128-140.
20. Lim K.P., Cirillo N., Hassona Y., Wei W., Thurlow J.K., Cheong S.C., Pitiyage G., Parkinson E.K., Prime S.S. Fibroblast gene expression profile reflects the stage of tumour progression in oral squamous cell carcinoma. J. Pathol. 2011, 223:459-469.
21. Costea D.E., Hills A., Osman A.H., Thurlow J., Kalna G., Huang X., Pena Murillo C., Parajuli H., Suliman S., Kulasekara K.K., Johannessen A.C., Partridge M. Identification of two distinct carcinoma-associated fibroblast subtypes with differential tumor-promoting abilities in oral squamous cell carcinoma. Cancer Res. 2013, 73:3888-3901.
22. Mantovani A., Allavena P., Sica A., Balkwill F. Cancer-related inflammation. Nature 2008, 454:436-444.
23. Hanahan D., Coussens L.M. Accessories to the crime: functions of cells recruited to the tumor microenvironment. Cancer Cell 2012, 21:309-322.
24. Koontongkaew S. The tumor microenvironment contribution to development, growth, invasion and metastasis of head and neck squamous cell carcinomas. J. Cancer 2013, 4:66-83.
25. Fujii N., Shomori K., Shiomi T., Nakabayashi M., Takeda C., Ryoke K., Ito H. Cancer- associated fibroblasts and CD163-positive macrophages in oral squamous cell carcinoma: their clinicopathological and prognostic significance. J. Oral Pathol. Med. 2012, 41:444-451.
26. Zhou C., Liu J., Tang Y., Liang X. Inflammation linking EMT and cancer stem cells. Oral Oncol. 2012, 48:1068-1075.
27. Nyberg P., Xie L., Kalluri R. Endogenous inhibitors of angiogenesis. Cancer Res. 2005, 65:3967-3979.
28. Goetz J.G., Minguet S., Navarro-Lerida I., Lazcano J.J., Samaniego R., Calvo E., Tello M., Osteso-Ibanez T., Pellinen T., Echarri A., Cerezo A., Klein-Szanto A.J., Garcia R., Keely P.J., Sanchez-Mateos P., Cukierman E., Del Pozo M.A. Biomechanical remodeling of the microenvironment by stromal caveolin-1 favors tumor invasion and metastasis. Cell 2011, 146:148-163.
29. Harada T., Shinohara M., Nakamura S., Oka M. An immunohistochemical study of the extracellular matrix in oral squamous cell carcinoma and its association with invasive and metastatic potential. Virchows Arch 1994, 424:257-266.
30. Sudhakar A., Nyberg P., Keshamouni V.G., Mannam A.P., Li J., Sugimoto H., Cosgrove D., Kalluri R. Human alpha1 type IV collagen NC1 domain exhibits distinct antiangiogenic activity mediated by alpha1beta1 integrin. J. Clin Invest. 2005, 115:2801-2810.
31. Aikio M., Alahuhta I., Nurmenniemi S., Suojanen J., Palovuori R., Teppo S., Sorsa T., Lopez-Otin C., Pihlajaniemi T., Salo T., Heljasvaara R., Nyberg P. Arresten, a collagen-derived angiogenesis inhibitor, suppresses invasion of squamous cell carcinoma. PLoS One 2012, 7:e51044.
32. Folkman J. Antiangiogenesis in cancer therapy--endostatin and its mechanisms of action. Exp. Cell Res. 2006, 312:594-607.
33. Mishra M., Chandavarkar V., Naik V.V., Kale A.D. An immunohistochemical study of basement membrane heparan sulfate proteoglycan (perlecan) in oral epithelial dysplasia and squamous cell carcinoma. J. Oral Maxillofac. Pathol. 2013, 17:31-35.
34. Levental K.R., Yu H., Kass L., Lakins J.N., Egeblad M., Erler J.T., Fong S.F., Csiszar K., Giaccia A., Weninger W., Yamauchi M., Gasser D.L., Weaver V.M. Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 2009, 139:891-906.
35. Egeblad M., Rasch M.G., Weaver V.M. Dynamic interplay between the collagen scaffold and tumor evolution. Curr. Opin. Cell Biol. 2010, 22:697-706.
36. Kainulainen T., Grenman R., Oikarinen A., Greenspan D.S., Salo T. Distribution and synthesis of type VII collagen in oral squamous cell carcinoma. J. Oral Pathol. Med. 1997, 26:414-418.
37. Metwaly H., Maruyama S., Yamazaki M., Tsuneki M., Abe T., Jen K.Y., Cheng J., Saku T. Parenchymal-stromal switching for extracellular matrix production on invasion of oral squamous cell carcinoma. Hum. Pathol. 2012, 43:1973-1981.
38. Mendez E., Houck J.R., Doody D.R., Fan W., Lohavanichbutr P., Rue T.C., Yueh B., Futran N.D., Upton M.P., Farwell D.G., Heagerty P.J., Zhao L.P., Schwartz S.M., Chen C. A genetic expression profile associated with oral cancer identifies a group of patients at high risk of poor survival. Clin. Cancer Res. 2009, 15:1353-1361.
39. Kessenbrock K., Plaks V., Werb Z. Matrix metalloproteinases: regulators of the tumor microenvironment. Cell 2010, 141:52-67.
40. Korpi J.T., Kervinen V., Mäklin H., Väänänen A., Lahtinen M., Läärä E., Ristimäki A., Thomas G., Ylipalosaari M., Åstrom P., Lopez-Otin C., Sorsa T., Kantola S., Pirilä E., Salo T. Collagenase-2 (matrix metalloproteinase-8) plays a protective role in tongue cancer. Br. J. Cancer. 2008, 98:766-775.
41. Erler J.T., Bennewith K.L., Cox T.R., Lang G., Bird D., Koong A., Le Q.T., Giaccia A.J. Hypoxia-induced lysyl oxidase is a critical mediator of bone marrow cell recruitment to form the premetastatic niche. Cancer Cell 2009, 15:35-44.
42. Sorsa T., Tjäderhane L., Salo T. Matrix metalloproteinases (MMPs) in oral diseases. Oral Dis. 2004, 10:311-318.
43. Vilen S.T., Salo T., Sorsa T., Nyberg P. Fluctuating roles of matrix metalloproteinase-9 in oral squamous cell carcinoma. Sci. World J. 2013, 2013:920595.
44. Bitu C.C., Kauppila J.H., Bufalino A., Nurmenniemi S., Teppo S., Keinänen M., Vilen S.T., Lehenkari P., Nyberg P., Coletta R.D., Salo T. Cathepsin k is present in invasive oral tongue squamous cell carcinoma in vivo and in vitro. PLoS One 2013, 8:e70925.
45. Albini A., Sporn M.B. The tumour microenvironment as a target for chemoprevention. Nat. Rev. Cancer 2007, 7:139-147.
46. Sun Y., Campisi J., Higano C., Beer T.M., Porter P., Coleman I., True L., Nelson P.S. Treatment-induced damage to the tumor microenvironment promotes prostate cancer therapy resistance through WNT16B. Nat. Med. 2012, 18:1359-1368.
47. Junttila MR, de Sauvage FJ. Influence of tumour micro-environment heterogeneity on therapeutic response. Nature 2013, 501(7467):346-354. (Sep 19).
48. Zlotogorski A., Dayan A., Dayan D., Chaushu G., Salo T., Vered M. Nutraceuticals as new treatment approaches for oral cancer-I: Curcumin. Oral Oncol. 2013, 49:187-191.
49. Zlotogorski A., Dayan A., Dayan D., Chaushu G., Salo T., Vered M. Nutraceuticals as new treatment approaches for oral cancer: II. Green tea extracts and resveratrol. Oral Oncol. 2013, 49:502-506.