The role of stromal fibroblasts in lung carcinogenesis: A target for chemoprevention?

International Journal of Cancer

Volumn 138, Issue 1, 2016, Pages 30-44

  Mahale, Jagdish ^a   Smagurauskaite, Gintare ^a   Brown, Karen ^a   Thomas, Anne ^a   Howells, Lynne M ^a  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

Author keywords

cancer associated fibroblasts; chemoprevention; co culture models; lung cancer

Indexed keywords

CAPECITABINE; CETUXIMAB; CISPLATIN; CRIZOTINIB; CURCUMIN; DASATINIB; EPIGALLOCATECHIN GALLATE; EPIRUBICIN; ERLOTINIB; GEFITINIB; IMATINIB; LOSARTAN; NILOTINIB; RAPAMYCIN; RILOTUMUMAB; SIBROTUZUMAB; SILTUXIMAB; SORAFENIB; STAT3 PROTEIN; ANTINEOPLASTIC AGENT;

ARTICLE; CANCER PREVENTION; CANCER RESISTANCE; CANCER STEM CELL; CELL EXPANSION; CELL FUNCTION; CELL INTERACTION; CHEMOPROPHYLAXIS; DRUG EFFECT; DRUG TARGETING; DRUG TREATMENT FAILURE; EPITHELIAL MESENCHYMAL TRANSITION; EXTRACELLULAR MATRIX; FIBROBLAST; HUMAN; LUNG CANCER; LUNG CARCINOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; STROMA CELL; TREATMENT PLANNING; TUMOR CELL; TUMOR MICROENVIRONMENT; TUMOR VOLUME; ANIMAL; CARCINOGENESIS; CELL COMMUNICATION; DRUG EFFECTS; DRUG RESISTANCE; GENETICS; LUNG NEOPLASMS; METABOLISM; MOLECULARLY TARGETED THERAPY; MORTALITY; PATHOLOGY; PROGNOSIS; SIGNAL TRANSDUCTION; STEM CELL;

ANIMALS; ANTINEOPLASTIC AGENTS; CARCINOGENESIS; CELL COMMUNICATION; CHEMOPREVENTION; DRUG RESISTANCE, NEOPLASM; EXTRACELLULAR MATRIX; FIBROBLASTS; HUMANS; LUNG NEOPLASMS; MOLECULAR TARGETED THERAPY; PROGNOSIS; SIGNAL TRANSDUCTION; STEM CELLS; STROMAL CELLS; TUMOR MICROENVIRONMENT;

EID: 84944274542     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.29447     Document Type: Article

References (97)

1. Bhowmick NA, Neilson EG, Moses HL., Stromal fibroblasts in cancer initiation and progression. Nature 2004; 432: 332-7.
2. Eberlein C, Rooney C, Ross SJ, et al., E-Cadherin and EpCAM expression by NSCLC tumour cells associate with normal fibroblast activation through a pathway initiated by integrin alphavbeta6 and maintained through TGFbeta signalling. Oncogene, in press.
3. El-Nikhely N, Larzabal L, Seeger W, et al., Tumor-stromal interactions in lung cancer: Novel candidate targets for therapeutic intervention. Expert Opin Investig Drugs 2012; 21: 1107-22.
4. Ruiz EJ, Oeztuerk-Winder F, Ventura JJ., A paracrine network regulates the cross-talk between human lung stem cells and the stroma. Nat Commun 2014; 5: 3175.
5. Chen WJ, Ho CC, Chang YL, et al., Cancer-associated fibroblasts regulate the plasticity of lung cancer stemness via paracrine signalling. Nat Commun 2014; 5: 3472.
6. Shintani Y, Abulaiti A, Kimura T, et al., Pulmonary fibroblasts induce epithelial mesenchymal transition and some characteristics of stem cells in non-small cell lung cancer. Ann Thorac Surg 2013; 96: 425-33.
7. Cirri P, Chiarugi P., Cancer associated fibroblasts: The dark side of the coin. Am J Cancer Res 2011; 1: 482-97.
8. Togo S, Polanska UM, Horimoto Y, et al., Carcinoma-associated fibroblasts are a promising therapeutic target. Cancers 2013; 5: 149-69.
9. Vicent S, Sayles LC, Vaka D, et al., Cross-species functional analysis of cancer-associated fibroblasts identifies a critical role for CLCF1 and IL-6 in non-small cell lung cancer in vivo. Cancer Res 2012; 72: 5744-56.
10. Karvonen HM, Lehtonen ST, Sormunen RT, et al., Lung cancer-associated myofibroblasts reveal distinctive ultrastructure and function. J Thorac Oncol 2014; 9: 664-74.
11. Horie M, Saito A, Mikami Y, et al., Characterization of human lung cancer-associated fibroblasts in three-dimensional in vitro co-culture model. Biochem Biophys Res Commun 2012; 423: 158-63.
12. Chaudhri VK, Salzler GG, Dick SA, et al., Metabolic alterations in lung cancer-associated fibroblasts correlated with increased glycolytic metabolism of the tumor. Mol Cancer Res 2013; 11: 579-92.
13. Calvo F, Ege N, Grande-Garcia A, et al., Mechanotransduction and YAP-dependent matrix remodelling is required for the generation and maintenance of cancer-associated fibroblasts. Nat Cell Biol 2013; 15: 637-46.
14. Maller O, DuFort CC, Weaver VM., YAP forces fibroblasts to feel the tension. Nat Cell Biol 2013; 15: 570-2.
15. Erez N, Truitt M, Olson P, et al., 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.
16. Duyverman AM, Steller EJ, Fukumura D, et al., Studying primary tumor-associated fibroblast involvement in cancer metastasis in mice. Nat Protoc 2012; 7: 756-62.
17. An J, Enomoto A, Weng L, et al., Significance of cancer-associated fibroblasts in the regulation of gene expression in the leading cells of invasive lung cancer. J Cancer Res Clin Oncol 2013; 139: 379-88.
18. Ridley AJ, Schwartz MA, Burridge K, et al., Cell migration: Integrating signals from front to back. Science 2003; 302: 1704-9.
19. Abulaiti A, Shintani Y, Funaki S, et al., Interaction between non-small-cell lung cancer cells and fibroblasts via enhancement of TGF-beta signaling by IL-6. Lung Cancer 2013; 82: 204-13.
20. Stankiewicz P, Sen P, Bhatt SS, et al., Genomic and genic deletions of the FOX gene cluster on 16q24.1 and inactivating mutations of FOXF1 cause alveolar capillary dysplasia and other malformations. Am J Hum Genet 2009; 84: 780-91.
21. Saito RA, Micke P, Paulsson J, et al., Forkhead box F1 regulates tumor-promoting properties of cancer-associated fibroblasts in lung cancer. Cancer Res 2010; 70: 2644-54.
22. Sanz-Moreno V, Gaggioli C, Yeo M, et al., ROCK and JAK1 signaling cooperate to control actomyosin contractility in tumor cells and stroma. Cancer Cell 2011; 20: 229-45.
23. Scott RW, Hooper S, Crighton D, et al., LIM kinases are required for invasive path generation by tumor and tumor-associated stromal cells. J Cell Biol 2010; 191: 169-85.
24. Karagiannis GS, Poutahidis T, Erdman SE, et al., Cancer-associated fibroblasts drive the progression of metastasis through both paracrine and mechanical pressure on cancer tissue. Mol Cancer Res 2012; 10: 1403-18.
25. Mazurov D, Barbashova L, Filatov A., Tetraspanin protein CD9 interacts with metalloprotease CD10 and enhances its release via exosomes. FEBS J 2013; 280: 1200-13.
26. Leithner K, Wohlkoenig C, Stacher E, et al., Hypoxia increases membrane metallo-endopeptidase expression in a novel lung cancer ex vivo model-role of tumor stroma cells. BMC Cancer 2014; 14: 40.
27. Nazareth MR, Broderick L, Simpson-Abelson MR, et al., Characterization of human lung tumor-associated fibroblasts and their ability to modulate the activtion of tumor-associated T cells. J Immunol 2007; 178: 5552-62.
28. Prasad S, Hogaboam CM, Jarai G., Deficient repair response of IPF fibroblasts in a co-culture model of epithelial injury and repair. Fibrogenesis Tissue Repair 2014; 7: 7.
29. Amann A, Zwierzina M, Gamerith G, et al., Development of an innovative 3D cell culture system to study tumour-stroma interactions in non-small cell lung cancer cells. PLoS One 2014; 9: E92511.
30. Xiao Y, Peiqin W, Tao J, et al., Fibroblasts weaken the anti-tumor effect of gefitinib on co-cultured non-small cell lung cancer cells. Chin Med J 2014; 127: 2091-96.
31. Kobayashi T, Kim H, Liu X, et al., Matrix metalloproteinase-9 activates TGF-beta and stimulates fibroblast contraction of collagen gels. Am J Physiol Lung Cell Mol Physiol 2014; 306: L1006-L10015.
32. Varzavand A, Drake JM, Svensson RU, et al., Integrin alpha3beta1 regulates tumor cell responses to stromal cells and can function to suppress prostate cancer metastatic colonization. Clin Exp Metastasis 2013; 30: 541-52.
33. Loubaki L, Hadj-Salem I, Fakhfakh R, et al., Co-culture of human bronchial fibroblasts and CD4+ T cells increases Th17 cytokine signature. PLoS One 2013; 8: E81983.
34. Conte E, Gili E, Fruciano M, et al., Human lung fibroblasts increase CD4(+)CD25(+)Foxp3(+) T cells in co-cultured CD4(+) lymphocytes. Cell Immunol 2013; 285: 55-61.
35. Choe C, Shin YS, Kim SH, et al., Tumor-stromal interactions with direct cell contacts enhance motility of non-small cell lung cancer cells through the hedgehog signaling pathway. Anticancer Res 2013; 33: 3715-23.
36. Kim SH, Choe C, Shin YS, et al., Human lung cancer-associated fibroblasts enhance motility of non-small cell lung cancer cells in co-culture. Anticancer Res 2013; 33: 2001-9.
37. Ruiz PA, Jarai G., Discoidin domain receptors regulate the migration of primary human lung fibroblasts through collagen matrices. Fibrogenesis Tissue Repair 2012; 5: 3.
38. Mishra DK, Sakamoto JH, Thrall MJ, et al., Human lung cancer cells grown in an ex vivo 3D lung model produce matrix metalloproteinases not produced in 2D culture. PLoS One 2012; 7: E45308.
39. Shieh AC, Rozansky HA, Hinz B, et al., Tumor cell invasion is promoted by interstitial flow-induced matrix priming by stromal fibroblasts. Cancer Res 2011; 71: 790-800.
40. Li Y, Jiang D, Liang J, et al., Severe lung fibrosis requires an invasive fibroblast phenotype regulated by hyaluronan and CD44. J Exp Med 2011; 208: 1459-71.
41. Asaithamby A, Hu B, Delgado O, et al., Irreparable complex DNA double-strand breaks induce chromosome breakage in organotypic three-dimensional human lung epithelial cell culture. Nucleic Acids Res 2011; 39: 5474-88.
42. Gaud G, Iochmann S, Guillon-Munos A, et al., TFPI-2 silencing increases tumour progression and promotes metalloproteinase 1 and 3 induction through tumour-stromal cell interactions. J Cell Mol Med 2011; 15: 196-208.
43. Kamio K, Liu XD, Sugiura H, et al., Statins inhibit matrix metalloproteinase release from human lung fibroblasts. Eur Respir J 2010; 35: 637-46.
44. Liu T, Lin B, Qin J., Carcinoma-associated fibroblasts promoted tumor spheroid invasion on a microfluidic 3D co-culture device. Lab Chip 2010; 10: 1671-7.
45. Navab R, Strumpf D, Bandarchi B, et al., Prognostic gene-expression signature of carcinoma-associated fibroblasts in non-small cell lung cancer. Proc Natl Acad Sci USA 2011; 108: 7160-5.
46. Vaira V, Fedele G, Pyne S, et al., Preclinical model of organotypic culture for pharmacodynamic profiling of human tumors. Proc Natl Acad Sci USA 2010; 107: 8352-6.
47. Fujita H, Ohuchida K, Mizumoto K, et al., Tumor-stromal interactions with direct cell contacts enhance proliferation of human pancreatic carcinoma cells. Cancer Sci 2009; 100: 2309-17.
48. Zhu S, Gladson CL, White KE, et al., Urokinase receptor mediates lung fibroblast attachment and migration toward provisional matrix proteins through interaction with multiple integrins. Am J Physiol Lung Cell Mol Physiol 2009; 297: L97-L108.
49. Wang W, Li Q, Yamada T, et al., Crosstalk to stromal fibroblasts induces resistance of lung cancer to epidermal growth factor receptor tyrosine kinase inhibitors. Clin Cancer Res 2009; 15: 6630-8.
50. Nakao M, Ishii G, Nagai K, et al., Prognostic significance of carbonic anhydrase IX expression by cancer-associated fibroblasts in lung adenocarcinoma. Cancer 2009; 115: 2732-43.
51. Martin MD, Fingleton B, Lynch CC, et al., Establishment and quantitative imaging of a 3D lung organotypic model of mammary tumor outgrowth. Clin Exp Metastasis 2008; 25: 877-85.
52. Maneva-Radicheva L, Ebert U, Dimoudis N, et al., Fibroblast remodeling of adsorbed collagen type IV is altered in contact with cancer cells. Histol Histopathol 2008; 23: 833-42.
53. Cekanova M, Masi T, Plummer HK, III, et al. Pulmonary fibroblasts stimulate the proliferation of cell lines from human lung adenocarcinomas. Anticancer Drugs 2006; 17: 771-81.
54. Vancheri C, Mastruzzo C, Trovato-Salinaro E, et al,. Interaction between human lung fibroblasts and T-lymphocytes prevents activation of CD4+ cells. Respir Res 2005; 6: 103.
55. Bartling B, Demling N, Silber RE, et al., Proliferative stimulus of lung fibroblasts on lung cancer cells is impaired by the receptor for advanced glycation end-products. Am J Respir Cell Mol Biol 2006; 34: 83-91.
56. Pechkovsky DV, Goldmann T, Ludwig C, et al., CCR2 and CXCR3 agonistic chemokines are differently expressed and regulated in human alveolar epithelial cells type II. Respir Res 2005; 6: 75.
57. Fromigue O, Louis K, Dayem M, et al., Gene expression profiling of normal human pulmonary fibroblasts following coculture with non-small-cell lung cancer cells reveals alterations related to matrix degradation, angiogenesis, cell growth and survival. Oncogene 2003; 22: 8487-97.
58. Pan T, Mason RJ, Westcott JY, et al., Rat alveolar type II cells inhibit lung fibroblast proliferation in vitro. Am J Respir Cell Mol Biol 2001; 25: 353-61.
59. Anderson IC, Mari SE, Broderick RJ, et al., The angiogenic factor interleukin 8 is induced in non-small cell lung cancer/pulmonary fibroblast cocultures. Cancer Res 2000; 60: 269-72.
60. Mari BP, Anderson IC, Mari SE, et al., Stromelysin-3 is induced in tumor/stroma cocultures and inactivated via a tumor-specific and basic fibroblast growth factor-dependent mechanism. J Biol Chem 1998; 273: 618-26.
61. Paulsson J, Micke P., Prognostic relevance of cancer-associated fibroblasts in human cancer. Semin Cancer Biol 2014; 25: 61-8.
62. Liao Y, Ni Y, He R, et al., Clinical implications of fibroblast activation protein-alpha in non-small cell lung cancer after curative resection: A new predictor for prognosis. J Cancer Res Clin Oncol 2013; 139: 1523-8.
63. Ito M, Ishii G, Nagai K, et al., Prognostic impact of cancer-associated stromal cells in patients with stage I lung adenocarcinoma. Chest 2012; 142: 151-8.
64. Kwak Y, Lee HE, Kim WH, et al., The clinical implication of cancer-associated microvasculature and fibroblast in advanced colorectal cancer patients with synchronous or metachronous metastases. PLoS One 2014; 9: E91811.
65. Kawase A, Ishii G, Nagai K, et al., Podoplanin expression by cancer associated fibroblasts predicts poor prognosis of lung adenocarcinoma. Int J Cancer 2008; 123: 1053-9.
66. Chen Y, Zou L, Zhang Y, et al., Transforming growth factor-beta1 and alpha-smooth muscle actin in stromal fibroblasts are associated with a poor prognosis in patients with clinical stage I-IIIA nonsmall cell lung cancer after curative resection. Tumour Biol 2014; 35: 6707-13.
67. Matsuwaki R, Ishii G, Zenke Y, et al., Immunophenotypic features of metastatic lymph node tumors to predict recurrence in N2 lung squamous cell carcinoma. Cancer Sci 2014; 105: 905-11.
68. Edlund K, Lindskog C, Saito A, et al., CD99 is a novel prognostic stromal marker in non-small cell lung cancer. Int J Cancer 2012; 131: 2264-73.
69. Kinoshita T, Ishii G, Hiraoka N, et al., Forkhead box P3 regulatory T cells coexisting with cancer associated fibroblasts are correlated with a poor outcome in lung adenocarcinoma. Cancer Sci 2013; 104: 409-15.
70. Yamada T, Takeuchi S, Kita K, et al., Hepatocyte growth factor induces resistance to anti-epidermal growth factor receptor antibody in lung cancer. J Thorac Oncol 2012; 7: 272-80.
71. Affolter A, Schmidtmann I, Mann WJ, et al., Cancer-associated fibroblasts do not respond to combined irradiation and kinase inhibitor treatment. Oncol Rep 2013; 29: 785-90.
72. Mink SR, Vashistha S, Zhang W, et al., Cancer-associated fibroblasts derived from EGFR-TKI-resistant tumors reverse EGFR pathway inhibition by EGFR-TKIs. Mol Cancer Res 2010; 8: 809-20.
73. Choi DY, You S, Jung JH, et al., Extracellular vesicles shed from gefitinib-resistant nonsmall cell lung cancer regulate the tumor microenvironment. Proteomics, in press.
74. Heigener DF, Reck M., Crizotinib. Recent Results Cancer Res Fortschritte der Krebsforschung Progres dans les recherches sur le cancer 2014; 201: 197-205.
75. Yamada T, Takeuchi S, Nakade J, et al., Paracrine receptor activation by microenvironment triggers bypass survival signals and ALK inhibitor resistance in EML4-ALK lung cancer cells. Clin Cancer Res 2012; 18: 3592-602.
76. Sonnenberg M, van der Kuip H, Haubeis S, et al., Highly variable response to cytotoxic chemotherapy in carcinoma-associated fibroblasts (CAFs) from lung and breast. BMC Cancer 2008; 8: 364.
77. Diop-Frimpong B, Chauhan VP, Krane S, et al., Losartan inhibits collagen I synthesis and improves the distribution and efficacy of nanotherapeutics in tumors. Proc Natl Acad Sci USA 2011; 108: 2909-14.
78. Kinoshita K, Nakagawa K, Hamada J, et al., Imatinib mesylate inhibits the proliferation-stimulating effect of human lung cancer-associated stromal fibroblasts on lung cancer cells. Int J Oncol 2010; 37: 869-77.
79. Haubeiss S, Schmid JO, Murdter TE, et al., Dasatinib reverses cancer-associated fibroblasts (CAFs) from primary lung carcinomas to a phenotype comparable to that of normal fibroblasts. Mol Cancer 2010; 9: 168.
80. Song L, Smith MA, Doshi P, et al., Antitumor efficacy of the anti-interleukin-6 (IL-6) antibody siltuximab in mouse xenograft models of lung cancer. J Thorac Oncol 2014; 9: 974-82.
81. Scott AM, Wiseman G, Welt S, et al., A Phase I dose-escalation study of sibrotuzumab in patients with advanced or metastatic fibroblast activation protein-positive cancer. Clin Cancer Res 2003; 9: 1639-47.
82. Iveson T, Donehower RC, Davidenko I, et al., Rilotumumab in combination with epirubicin, cisplatin, and capecitabine as first-line treatment for gastric or oesophagogastric junction adenocarcinoma: An open-label, dose de-escalation phase 1b study and a double-blind, randomised phase 2 study. Lancet Oncol, in press.
83. Mercier I, Camacho J, Titchen K, et al., Caveolin-1 and accelerated host aging in the breast tumor microenvironment: Chemoprevention with rapamycin, an mTOR inhibitor and anti-aging drug. Am J Pathol 2012; 181: 278-93.
84. Hsu YC, Chen MJ, Yu YM, et al., Suppression of TGF-beta1/SMAD pathway and extracellular matrix production in primary keloid fibroblasts by curcuminoids: Its potential therapeutic use in the chemoprevention of keloid. Arch Dermatol Res 2010; 302: 717-24.
85. Zhang D, Huang C, Yang C, et al., Bromme D. Antifibrotic effects of curcumin are associated with overexpression of cathepsins K and L in bleomycin treated mice and human fibroblasts. Respir Res 2011; 12: 154.
86. Chang JZ, Yang WH, Deng YT, et al., EGCG blocks TGFbeta1-induced CCN2 by suppressing JNK and p38 in buccal fibroblasts. Clin Oral Investig 2013; 17: 455-61.
87. Harada D, Takigawa N, Kiura K., The role of STAT3 in non-small cell lung cancer. Cancers 2014; 6: 708-22.
88. Song L, Rawal B, Nemeth JA, et al., JAK1 activates STAT3 activity in non-small-cell lung cancer cells and IL-6 neutralizing antibodies can suppress JAK1-STAT3 signaling. Mol Cancer Ther 2011; 10: 481-94.
89. Angevin E, Tabernero J, Elez E, et al., A phase I/II, multiple-dose, dose-escalation study of siltuximab, an anti-interleukin-6 monoclonal antibody, in patients with advanced solid tumors. Clin Cancer Res 2014; 20: 2192-204.
90. Hofheinz RD, al-Batran SE, Hartmann F, et al., Stromal antigen targeting by a humanised monoclonal antibody: An early phase II trial of sibrotuzumab in patients with metastatic colorectal cancer. Onkologie 2003; 26: 44-8.
91. Hu M, Che P, Han X, et al., Therapeutic targeting of Src kinase in myofibroblast differentiation and pulmonary fibrosis. J Pharmacol Exp Ther, in press.
92. Aljada A, Mousa SA., Metformin and neoplasia: Implications and indications. Pharmacol Ther 2012; 133: 108-15.
93. Park W, Amin AR, Chen ZG, et al., New perspectives of curcumin in cancer prevention. Cancer Prev Res 2013; 6: 387-400.
94. Singh BN, Shankar S, Srivastava RK., Green tea catechin, epigallocatechin-3-gallate (EGCG): Mechanisms, perspectives and clinical applications. Biochem Pharmacol 2011; 82: 1807-21.
95. Stolfi C, De Simone V, Pallone F, et al., Mechanisms of action of non-steroidal anti-inflammatory drugs (NSAIDs) and mesalazine in the chemoprevention of colorectal cancer. Int J Mol Sci 2013; 14: 17972-85.
96. Tanaka T, Shnimizu M, Moriwaki H., Cancer chemoprevention by carotenoids. Molecules 2012; 17: 3202-42.
97. Xiao H, Yang CS., Combination regimen with statins and NSAIDs: A promising strategy for cancer chemoprevention. Int J Cancer 2008; 123: 983-90.