Secretome profiling of oral squamous cell carcinoma-associated fibroblasts reveals organization and disassembly of extracellular matrix and collagen metabolic process signatures

Tumor Biology

Volumn 37, Issue 7, 2016, Pages 9045-9057

  Bagordakis, Elizabete ^a   Sawazaki Calone, Iris ^b   Macedo, Carolina Carneiro Soares ^a   Carnielli, Carolina M ^c   de Oliveira, Carine Ervolino ^a   Rodrigues, Priscila Campioni ^a   Rangel, Ana Lucia C A ^b   dos Santos, Jean Nunes ^d   Risteli, Juha ^e,f   Graner, Edgard ^a   Salo, Tuula ^e,f,g,h   Leme, Adriana Franco Paes ^c   Coletta, Ricardo D ^a  

^a UNIVERSITY OF CAMPINAS   (Brazil)

^b UNIVERSIDADE ESTADUAL DO OESTE DO PARANÁ   (Brazil)

^c CENTRO NACIONAL DE PESQUISA EM ENERGIA E MATERIAIS   (Brazil)

^d FEDERAL UNIVERSITY OF BAHIA   (Brazil)

^e UNIVERSITY OF OULU   (Finland)

^f OULU UNIVERSITY HOSPITAL   (Finland)

^g UNIVERSITY OF HELSINKI   (Finland)

^h HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

Author keywords

Cancer associated fibroblasts; Extracellular matrix; FNDC1; Secretome; SERPINE1; STC2; Type I collagen

Indexed keywords

COLLAGEN TYPE 1; FIBRONECTIN TYPE III DOMAIN CONTAINING 1; PROCOLLAGEN TYPE 3 AMINOPROPEPTIDE; PROTEIN; SECRETOME; SERPIN PEPTIDASE INHIBITOR TYPE 1; STANNIOCALCIN 2; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG; FNDC1 PROTEIN, HUMAN; GLYCOPROTEIN; PEPTIDE FRAGMENT; PLASMINOGEN ACTIVATOR INHIBITOR 1; PROCOLLAGEN; PROCOLLAGEN TYPE I N-TERMINAL PEPTIDE; SERPINE1 PROTEIN, HUMAN; SIGNAL PEPTIDE; STC2 PROTEIN, HUMAN; TUMOR PROTEIN;

ARTICLE; CANCER ASSOCIATED FIBROBLAST; CANCER PATIENT; CANCER PROGNOSIS; CANCER SURVIVAL; CLINICAL ARTICLE; COLLAGEN METABOLISM; CONTROLLED STUDY; DRUG TARGETING; ENZYME LINKED IMMUNOSORBENT ASSAY; EXTRACELLULAR MATRIX; FEMALE; FIBROBLAST; HUMAN; HUMAN CELL; HUMAN TISSUE; MALE; MASS SPECTROMETRY; MOUTH SQUAMOUS CELL CARCINOMA; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEOMICS; REAL TIME POLYMERASE CHAIN REACTION; STROMA; TUMOR MICROENVIRONMENT; CELL LINE; DISEASE FREE SURVIVAL; METABOLISM; MOUTH TUMOR; PATHOLOGY; PHYSIOLOGY; SQUAMOUS CELL CARCINOMA; TUMOR CELL LINE; UPREGULATION;

CARCINOMA, SQUAMOUS CELL; CELL LINE; CELL LINE, TUMOR; COLLAGEN TYPE I; DISEASE-FREE SURVIVAL; EXTRACELLULAR MATRIX; FEMALE; FIBROBLASTS; GLYCOPROTEINS; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MOUTH NEOPLASMS; NEOPLASM PROTEINS; PEPTIDE FRAGMENTS; PLASMINOGEN ACTIVATOR INHIBITOR 1; PROCOLLAGEN; TRANSFORMING GROWTH FACTOR BETA1; TUMOR MICROENVIRONMENT; UP-REGULATION;

EID: 84954314201     PISSN: 10104283     EISSN: 14230380     Source Type: Journal    
DOI: 10.1007/s13277-015-4629-y     Document Type: Article

References (55)

1. Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. 2015;136:E359–86.
2. Warnakulasuriya S. Living with oral cancer: epidemiology with particular reference to prevalence and life-style changes that influence survival. Oral Oncol. 2010;46:407–10.
3. Shah FD, Begum R, Vajaria BN, Patel KR, Patel JB, Shukla SN, et al. A review on salivary genomics and proteomics biomarkers in oral cancer. Indian J Clin Biochem. 2011;26:326–34.
4. Hanahan D, Coussens LM. Accessories to the crime: functions of cells recruited to the tumor microenvironment. Cancer Cell. 2012;21:309–22.
5. 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.
6. Curry JM, Sprandio J, Cognetti D, Luginbuhl A, Bar-ad V, Pribitkin E, et al. Tumor microenvironment in head and neck squamous cell carcinoma. Semin Oncol. 2014;41:217–34.
7. Gandellini P, Andriani F, Merlino G, D’Aiuto F, Roz L, Callari M. Complexity in the tumour microenvironment: cancer associated fibroblast gene expression patterns identify both common and unique features of tumour-stroma crosstalk across cancer types. Semin Cancer Biol. 2015.
8. Sobral LM, Bufalino A, Lopes MA, Graner E, Salo T, Coletta RD. Myofibroblasts in the stroma of oral cancer promote tumorigenesis via secretion of activin A. Oral Oncol. 2011;47:840–6.
9. Hinsley EE, Kumar S, Hunter KD, Whawell SA, Lambert DW. Endothelin-1 stimulates oral fibroblasts to promote oral cancer invasion. Life Sci. 2012;91:557–61.
10. Tommelein J, Verset L, Boterberg T, Demetter P, Bracke M, De Wever O. Cancer-associated fibroblasts connect metastasis-promoting communication in colorectal cancer. Front Oncol. 2015;5:63.
11. Kellermann MG, Sobral LM, da Silva SD, Zecchin KG, Graner E, Lopes MA, et al. Myofibroblasts in the stroma of oral squamous cell carcinoma are associated with poor prognosis. Histopathology. 2007;51:849–53.
12. Kawashiri S, Tanaka A, Noguchi N, Hase T, Nakaya H, Ohara T, 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.
13. Vered M, Dobriyan A, Dayan D, Yahalom R, Talmi YP, Bedrin L, 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.
14. Bello IO, Vered M, Dayan D, Dobriyan A, Yahalom R, Alanen K, et al. 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;47:33–8.
15. Marsh D, Suchak K, Moutasim KA, Vallath S, Hopper C, Jerjes W, et al. Stromal features are predictive of disease mortality in oral cancer patients. J Pathol. 2011;223:470–81.
16. Fujii N, Shomori K, Shiomi T, Nakabayashi M, Takeda C, Ryoke K, et al. Cancer-associated fibroblasts and CD163-positive macrophages in oral squamous cell carcinoma: their clinicopathological and prognostic significance. J Oral Pathol Med. 2012;41:444–51.
17. Ding L, Zhang Z, Shang D, Cheng J, Yuan H, Wu Y, et al. α-Smooth muscle actin-positive myofibroblasts, in association with epithelial-mesenchymal transition and lymphogenesis, is a critical prognostic parameter in patients with oral tongue squamous cell carcinoma. J Oral Pathol Med. 2014;43:335–43.
18. De Boeck A, Hendrix A, Maynard D, Van Bockstal M, Daniëls A, Pauwels P, et al. Differential secretome analysis of cancer-associated fibroblasts and bone marrow-derived precursors to identify microenvironmental regulators of colon cancer progression. Proteomics. 2013;13:379–88.
19. Chen SX, Xu XE, Wang XQ, Cui SJ, Xu LL, Jiang YH, et al. Identification of colonic fibroblast secretomes reveals secretory factors regulating colon cancer cell proliferation. J Proteomics. 2014;110:155–71.
20. Rasanen K, Sriswasdi S, Valiga A, Tang HY, Zhang G, Perego M, et al. Comparative secretome analysis of epithelial and mesenchymal subpopulations of head and neck squamous cell carcinoma identifies S100A4 as a potential therapeutic target. Mol Cell Proteomics. 2013;12:3778–92.
21. Ge S, Mao Y, Yi Y, Xie D, Chen Z, Xiao Z. Comparative proteomic analysis of secreted proteins from nasopharyngeal carcinoma-associated stromal fibroblasts and normal fibroblasts. Exp Ther Med. 2012;3:857–60.
22. Salo S, Bitu C, Merkku K, Nyberg P, Bello IO, Vuoristo J, et al. Human bone marrow mesenchymal stem cells induce collagen production and tongue cancer invasion. PLoS One. 2013;8:e77692.
23. Sobral LM, Zecchin KG, de Nascimento Aquino S, Lopes MA, Graner E, Coletta RD. Isolation and characterization of myofibroblast cell lines from oral squamous cell carcinoma. Oncol Rep. 2011;25:1013–20.
24. Sobral LM, Montan PF, Zecchin KG, Martelli-Junior H, Vargas PA, Graner E, et al. Smad7 blocks transforming growth factor-β1-induced gingival fibroblast-myofibroblast transition via inhibitory regulation of Smad2 and connective tissue growth factor. J Periodontol. 2011;82:642–51.
25. Sawazaki-Calone I, Rangel A, Bueno AG, Morais CF, Nagai HM, Kunz RP, et al. The prognostic value of histopathological grading systems in oral squamous cell carcinomas. Oral Dis. 2015;21:755–61.
26. Risteli L, Risteli J. Biochemical markers of bone metabolism. Ann Med. 1993;25:385–93.
27. Kellermann MG, Sobral LM, da Silva SD, Zecchin KG, Graner E, Lopes MA, 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.
28. Han Y, Zhang Y, Jia T, Sun Y. Molecular mechanism underlying the tumor-promoting functions of carcinoma-associated fibroblasts. Tumour Biol. 2015;36:1385–94.
29. Erickson HP. Irisin and FNDC5 in retrospect: an exercise hormone or a transmembrane receptor? Adipocyte. 2013;2:289–93.
30. Fain JN, Company JM, Booth FW, Laughlin MH, Padilla J, Jenkins NT, et al. Exercise training does not increase muscle FNDC5 protein or mRNA expression in pigs. Metabolism. 2013;62:1503–11.
31. Sung CO, Kim SC, Karnan S, Karube K, Shin HJ, Nam DH, et al. Genomic profiling combined with gene expression profiling in primary central nervous system lymphoma. Blood. 2011;117:1291–300.
32. Itoh T, Hayashi Y, Kanamaru T, Morita Y, Suzuki S, Wang W, et al. Clinical significance of urokinase-type plasminogen activator activity in hepatocellular carcinoma. J Gastroenterol Hepatol. 2000;15:422–30.
33. Zheng Q, Tang ZY, Xue Q, Shi DR, Song HY, Tang HB. Invasion and metastasis of hepatocellular carcinoma in relation to urokinase-type plasminogen activator, its receptor and inhibitor. J Cancer Res Clin Oncol. 2000;126:641–6.
34. Schmitt M, Harbeck N, Brünner N, Jänicke F, Meisner C, Mühlenweg B, et al. Cancer therapy trials employing level-of-evidence-1 disease forecast cancer biomarkers uPA and its inhibitor PAI-1. Expert Rev Mol Diagn. 2011;11:617–34.
35. Duffy MJ, McGowan PM, Harbeck N, Thomssen C, Schmitt M. uPA and PAI-1 as biomarkers in breast cancer: validated for clinical use in level-of-evidence-1 studies. Breast Cancer Res. 2014;16:428.
36. Look MP, van Putten WL, Duffy MJ, Harbeck N, Christensen IJ, Thomssen C, et al. Pooled analysis of prognostic impact of urokinase-type plasminogen activator and its inhibitor PAI-1 in 8377 breast cancer patients. J Natl Cancer Inst. 2002;94:116–28.
37. Harris L, Fritsche H, Mennel R, Norton L, Ravdin P, Taube S, et al. American society of clinical oncology update of recommendations for the use of tumor markers in breast cancer. J Clin Oncol. 2007;25:5287–312.
38. Roca C, Primo L, Valdembri D, Cividalli A, Declerck P, Carmeliet P, et al. Hyperthermia inhibits angiogenesis by a plasminogen activator inhibitor 1-dependent mechanism. Cancer Res. 2003;63:1500–7.
39. Bajou K, Masson V, Gerard RD, Schmitt PM, Albert V, Praus M, et al. The plasminogen activator inhibitor PAI-1 controls in vivo tumor vascularization by interaction with proteases, not vitronectin. Implications for antiangiogenic strategies. J Cell Biol. 2001;152:777–84.
40. Czekay RP, Loskutoff DJ. Plasminogen activator inhibitors regulate cell adhesion through a uPAR-dependent mechanism. J Cell Physiol. 2009;220:655–63.
41. Dhanda J, Triantafyllou A, Liloglou T, Kalirai H, Lloyd B, Hanlon R, et al. SERPINE1 and SMA expression at the invasive front predict extracapsular spread and survival in oral squamous cell carcinoma. Br J Cancer. 2014;111:2114–21.
42. Pedroza M, Le TT, Lewis K, Karmouty-Quintana H, To S, George AT, et al. STAT-3 contributes to pulmonary fibrosis through epithelial injury and fibroblast-myofibroblast differentiation. FASEB J. 2015 Aug 31.
43. Na SS, Aldonza MB, Sung HJ, Kim YI, Son YS, Cho S, et al. Stanniocalcin-2 (STC2): a potential lung cancer biomarker promotes lung cancer metastasis and progression. Biochim Biophys Acta. 1854;2015:668–76.
44. Wang Y, Gao Y, Cheng H, Yang G, Tan W. Stanniocalcin 2 promotes cell proliferation and cisplatin resistance in cervical cancer. Biochem Biophys Res Commun. 2015;466:362–8.
45. Hou J, Wang Z, Xu H, Yang L, Yu X, Yang Z, et al. Stanniocalicin 2 suppresses breast cancer cell migration and invasion via the PKC/claudin-1-mediated signaling. PLoS One. 2015;10:e0122179.
46. Bouras T, Southey MC, Chang AC, Reddel RR, Willhite D, Glynne R, et al. Stanniocalcin 2 is an estrogen-responsive gene coexpressed with the estrogen receptor in human breast cancer. Cancer Res. 2002;62:1289–95.
47. Ieta K, Tanaka F, Yokobori T, Kita Y, Haraguchi N, Mimori K, et al. Clinicopathological significance of stanniocalcin 2 gene expression in colorectal cancer. Int J Cancer. 2009;125:926–31.
48. Tamura K, Furihata M, Chung SY, Uemura M, Yoshioka H, Iiyama T, et al. Stanniocalcin 2 overexpression in castration-resistant prostate cancer and aggressive prostate cancer. Cancer Sci. 2009;100:914–9.
49. Law AY, Lai KP, Ip CK, Wong AS, Wagner GF, Wong CK. Epigenetic and HIF-1 regulation of stanniocalcin-2 expression in human cancer cells. Exp Cell Res. 2008;314:1823–30.
50. Law AY, Wong CK. Stanniocalcin-2 is a HIF-1 target gene that promotes cell proliferation in hypoxia. Exp Cell Res. 2010;316:466–76.
51. Chang AC, Jellinek DA, Reddel RR. Mammalian stanniocalcins and cancer. Endocrinol Relat Cancer. 2003;10:359–73.
52. Van Bockstal M, Lambein K, Van Gele M, De Vlieghere E, Limame R, Braems G, et al. Differential regulation of extracellular matrix protein expression in carcinoma-associated fibroblasts by TGF-β1 regulates cancer cell spreading but not adhesion. Oncoscience. 2014;1:634–48.
53. Kenny HA, Krausz T, Yamada SD, Lengyel E. Use of a novel 3D culture model to elucidate the role of mesothelial cells, fibroblasts and extra-cellular matrices on adhesion and invasion of ovarian cancer cells to the omentum. Int J Cancer. 2007;121:1463–72.
54. Tang D, Gao J, Wang S, Ye N, Chong Y, Huang Y, et al. Cancer-associated fibroblasts promote angiogenesis in gastric cancer through galectin-1 expression. Tumour Biol. 2015. doi:10.1007/s13277-015-3942-9.
55. Liu J, Liao S, Diop-Frimpong B, Chen W, Goel S, Naxerova K, et al. TGF-β blockade improves the distribution and efficacy of therapeutics in breast carcinoma by normalizing the tumor stroma. Proc Natl Acad Sci U S A. 2012;109:16618–23.