CD117 Expression in fibroblasts-like stromal cells indicates unfavorable clinical outcomes in ovarian carcinoma patients

PLoS ONE

Volumn 9, Issue 11, 2014, Pages

  Huang, Ruixia ^a,b   Wu, Dan ^c   Yuan, Yuan ^d   Li, Xiaoran ^a,b   Holm, Ruth ^a   Trope, Claes G ^a,b   Nesland, Jahn M ^a,b   Suo, Zhenhe ^a,b  

^a OSLO UNIVERSITY HOSPITAL   (Norway)

^b UNIVERSITY OF OSLO   (Norway)

^c School of Medicine   (China)

^d CAPITAL MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

5' NUCLEOTIDASE; ALPHA SMOOTH MUSCLE ACTIN; SEPRASE; STEM CELL FACTOR RECEPTOR;

ADULT; AGED; ARTICLE; CANCER SURVIVAL; CONTROLLED STUDY; FEMALE; FIBROBLAST; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MAJOR CLINICAL STUDY; MESENCHYMAL STROMA CELL; OVARY CARCINOMA; OVERALL SURVIVAL; PROGRESSION FREE SURVIVAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; STROMA; STROMA CELL; TUMOR ASSOCIATED LEUKOCYTE; DISEASE FREE SURVIVAL; KAPLAN MEIER METHOD; MIDDLE AGED; OVARIAN NEOPLASMS; OVARY; PATHOLOGY; PROGNOSIS; VERY ELDERLY; YOUNG ADULT;

ADULT; AGED; AGED, 80 AND OVER; DISEASE-FREE SURVIVAL; FEMALE; FIBROBLASTS; HUMANS; KAPLAN-MEIER ESTIMATE; MIDDLE AGED; OVARIAN NEOPLASMS; OVARY; PROGNOSIS; PROTO-ONCOGENE PROTEINS C-KIT; STROMAL CELLS; YOUNG ADULT;

EID: 84915749670     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0112209     Document Type: Article

References (59)

1. Downs LS Jr, Judson PL, Argenta PA, Ghebre R, Geller MA, et al. (2008) A prospective randomized trial of thalidomide with topotecan compared with topotecan alone in women with recurrent epithelial ovarian carcinoma. Cancer 112: 331-339.
2. Guppy AE, Nathan PD, Rustin GJ (2005) Epithelial ovarian cancer: a review of current management. Clin Oncol (R Coll Radiol) 17: 399-411.
3. Ghesquiere B, Wong BW, Kuchnio A, Carmeliet P (2014) Metabolism of stromal and immune cells in health and disease. Nature 511: 167-176.
4. Liu ET (2007) Stromal effects in breast cancer. N Engl J Med 357: 2537-2538.
5. McMillin DW, Negri JM, Mitsiades CS (2013) The role of tumour-stromal interactions in modifying drug response: challenges and opportunities. Nature Reviews Drug Discovery 12: 217-228.
6. Kang Y (2013) Imaging signaling pathways and tumor-stromal interactions in cancer metastasis. Journal of Nuclear Medicine 54: 32-32.
7. Tod J, Jenei V, Thomas G, Fine D (2013) Tumor-stromal interactions in pancreatic cancer. Pancreatology 13: 1-7.
8. Pollack IF (2013) Tumor-Stromal Interactions in Medulloblastoma. New England Journal of Medicine 368: 1942-1943.
9. Albini A, Sporn MB (2007) The tumour microenvironment as a target for chemoprevention. Nat Rev Cancer 7: 139-147.
10. Zhang X, Kyo S, Nakamura M, Mizumoto Y, Maida Y, et al. (2014) Imatinib sensitizes endometrial cancer cells to cisplatin by targeting CD117-positive growth-competent cells. Cancer Lett 345: 106-114.
11. Adhikari AS, Agarwal N, Wood BM, Porretta C, Ruiz B, et al. (2010) CD117 and Stro-1 identify osteosarcoma tumor-initiating cells associated with metastasis and drug resistance. Cancer Res 70: 4602-4612.
12. Chen D, Zhang Y, Wang J, Chen J, Yang C, et al. (2013) MicroRNA-200c overexpression inhibits tumorigenicity and metastasis of CD117+CD44+ ovarian cancer stem cells by regulating epithelial-mesenchymal transition. J Ovarian Res 6: 50.
13. Cho KR, Shih Ie M (2009) Ovarian cancer. Annu Rev Pathol 4: 287-313.
14. Zivanovic O, Sima CS, Iasonos A, Hoskins WJ, Pingle PR, et al. (2010) The effect of primary cytoreduction on outcomes of patients with FIGO stage IIIC ovarian cancer stratified by the initial tumor burden in the upper abdomen cephalad to the greater omentum. Gynecol Oncol 116: 351-357.
15. Schmandt RE, Broaddus R, Lu KH, Shvartsman H, Thornton A, et al. (2003) Expression of c-ABL, c-KIT, and platelet-derived growth factor receptor-beta in ovarian serous carcinoma and normal ovarian surface epithelium. Cancer 98: 758-764.
16. Garrity MM, Gibbons SJ, Smyrk TC, Vanderwinden JM, Gomez-Pinilla PJ, et al. (2009) Diagnostic challenges of motility disorders: optimal detection of CD117+ interstitial cells of Cajal. Histopathology 54: 286-294.
17. Went PT, Dirnhofer S, Bundi M, Mirlacher M, Schraml P, et al. (2004) Prevalence of KIT expression in human tumors. J Clin Oncol 22: 4514-4522.
18. Ma D, Stence AA, Bossler AB, Hackman JR, Bellizzi AM (2013) Identification of KIT activating mutations in paediatric solitary mastocytoma. Histopathology 64: 218-225.
19. Gallegos I, Valdevenito JP, Miranda R, Fernandez C (2010) Immunohistochemistry expression of P53, Ki67, CD30, and CD117 and presence of clinical metastasis at diagnosis of testicular seminoma. Appl Immunohistochem Mol Morphol 19: 147-152.
20. de Silva CM, Reid R (2003) Gastrointestinal stromal tumors (GIST): C-kit mutations, CD117 expression, differential diagnosis and targeted cancer therapy with Imatinib. Pathol Oncol Res 9: 13-19.
21. Doyle LA, Hornick JL (2014) Gastrointestinal stromal tumours: from KIT to succinate dehydrogenase. Histopathology 64: 53-67.
22. Ismail RS, Cada M, Vanderhyden BC (1999) Transforming growth factor-beta regulates Kit ligand expression in rat ovarian surface epithelial cells. Oncogene 18: 4734-4741.
23. Kim DJ, Lee MH, Park TI, Bae HI (2006) Expression and mutational analysis of c-kit in ovarian surface epithelial tumors. J Korean Med Sci 21: 81-85.
24. Song N, Chen G, Zhang P, Liu M, He WX, et al. (2012) Diagnostic and clinical significance of KIT(CD117) expression in thymic epithelial tumors in China. Asian Pac J Cancer Prev 13: 2745-2748.
25. Petrini I, Zucali PA, Lee HS, Pineda MA, Meltzer PS, et al. (2010) Expression and mutational status of c-kit in thymic epithelial tumors. J Thorac Oncol 5: 1447-1453.
26. Kalluri R (2003) Basement membranes: structure, assembly and role in tumour angiogenesis. Nat Rev Cancer 3: 422-433.
27. Hanahan D, Weinberg RA (2000) The hallmarks of cancer. Cell 100: 57-70.
28. Tlsty TD, Coussens LM (2006) Tumor stroma and regulation of cancer development. Annu Rev Pathol 1: 119-150.
29. Cheng JD, Weiner LM (2003) Tumors and their microenvironments: tilling the soil. Commentary re: A. M. Scott et al., A Phase I dose-escalation study of sibrotuzumab in patients with advanced or metastatic fibroblast activation protein-positive cancer. Clin. Cancer Res., 9: 1639-1647, 2003.
30. Clin Cancer Res 9: 1590-1595.
31. Langley RR, Fidler IJ (2011) The seed and soil hypothesis revisited-the role of tumor-stroma interactions in metastasis to different organs. Int J Cancer 128: 2527-2535.
32. Chang HY, Chi JT, Dudoit S, Bondre C, van de Rijn M, et al. (2002) Diversity, topographic differentiation, and positional memory in human fibroblasts. Proc Natl Acad Sci U S A 99: 12877-12882.
33. Kalluri R, Zeisberg M (2006) Fibroblasts in cancer. Nat Rev Cancer 6: 392-401.
34. Brennen WN, Isaacs JT, Denmeade SR (2012) Rationale behind targeting fibroblast activation protein-expressing carcinoma-associated fibroblasts as a novel chemotherapeutic strategy. Mol Cancer Ther 11: 257-266.
35. Fearon DT (2014) The carcinoma-associated fibroblast expressing fibroblast activation protein and escape from immune surveillance. Cancer Immunol Res 2: 187-193.
36. Wang S, Ma N, Kawanishi S, Hiraku Y, Oikawa S, et al. (2014) Relationships of alpha-SMA-positive fibroblasts and SDF-1-positive tumor cells with neoangiogenesis in nasopharyngeal carcinoma. Biomed Res Int 2014: 507353.
37. Wu MH, Hong HC, Hong TM, Chiang WF, Jin YT, et al. (2011) Targeting galectin-1 in carcinoma-associated fibroblasts inhibits oral squamous cell carcinoma metastasis by downregulating MCP-1/CCL2 expression. Clin Cancer Res 17: 1306-1316.
38. in 't Anker PS, Noort WA, Scherjon SA, Kleijburg-van der Keur C, Kruisselbrink AB, et al. (2003) Mesenchymal stem cells in human secondtrimester bone marrow, liver, lung, and spleen exhibit a similar immunophenotype but a heterogeneous multilineage differentiation potential. Haematologica 88: 845-852.
39. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, et al. (1999) Multilineage potential of adult human mesenchymal stem cells. Science 284: 143-147.
40. Stagg J (2008) Mesenchymal stem cells in cancer. Stem Cell Rev 4: 119-124.
41. Lv FJ, Tuan RS, Cheung KM, Leung VY (2014) Concise review: the surface markers and identity of human mesenchymal stem cells. Stem Cells 32: 1408-1419.
42. Boxall SA, Jones E (2012) Markers for characterization of bone marrow multipotential stromal cells. Stem Cells Int 2012: 975871.
43. Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, et al. (2006) Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8: 315-317.
44. Potdar P, Sutar J (2010) Establishment and molecular characterization of mesenchymal stem cell lines derived from human visceral & subcutaneous adipose tissues. J Stem Cells Regen Med 6: 26-35.
45. Haniffa MA, Collin MP, Buckley CD, Dazzi F (2009) Mesenchymal stem cells: the fibroblasts' new clothes? Haematologica 94: 258-263.
46. Bae S, Park CW, Son HK, Ju HK, Paik D, et al. (2008) Fibroblast activation protein alpha identifies mesenchymal stromal cells from human bone marrow. Br J Haematol 142: 827-830.
47. Hung SC, Kuo PY, Chang CF, Chen TH, Ho LL (2006) Alpha-smooth muscle actin expression and structure integrity in chondrogenesis of human mesenchymal stem cells. Cell Tissue Res 324: 457-466.
48. Ljujic B, Milovanovic M, Volarevic V, Murray B, Bugarski D, et al. (2013) Human mesenchymal stem cells creating an immunosuppressive environment and promote breast cancer in mice. Scientific Reports 3.
49. Allard B, Turcotte M, Stagg J (2012) CD73-generated adenosine: orchestrating the tumor-stroma interplay to promote cancer growth. J Biomed Biotechnol 2012: 485156.
50. Synnestvedt K, Furuta GT, Comerford KM, Louis N, Karhausen J, et al. (2002) Ecto-59-nucleotidase (CD73) regulation by hypoxia-inducible factor-1 mediates permeability changes in intestinal epithelia. J Clin Invest 110: 993-1002.
51. Allard B, Turcotte M, Spring K, Pommey S, Royal I, et al. (2013) Anti-CD73 therapy impairs tumor angiogenesis. Int J Cancer 134: 1466-1473.
52. Chatterjee D, Tufa DM, Baehre H, Hass R, Schmidt RE, et al. (2014) Natural killer cells acquire CD73 expression upon exposure to mesenchymal stem cells. Blood 123: 594-595.
53. Sleeman JP, Thiery JP (2011) SnapShot: The epithelial-mesenchymal transition. Cell 145: 162 e161.
54. Thiery JP, Acloque H, Huang RY, Nieto MA (2009) Epithelial-mesenchymal transitions in development and disease. Cell 139: 871-890.
55. Thiery JP (2002) Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer 2: 442-454.
56. Xiong L, Wen Y, Miao X, Yang Z (2013) NT5E and FcGBP as key regulators of TGF-1-induced epithelial-mesenchymal transition (EMT) are associated with tumor progression and survival of patients with gallbladder cancer. Cell Tissue Res 355: 365-374.
57. Li O, Tormin A, Sundberg B, Hyllner J, Le Blanc K, et al. (2013) Human embryonic stem cell-derived mesenchymal stroma cells (hES-MSCs) engraft in vivo and support hematopoiesis without suppressing immune function: implications for off-the shelf ES-MSC therapies. PLoS One 8: e55319.
58. Park JS, Chang DY, Kim JH, Jung JH, Park J, et al. (2013) Retrovirus-mediated transduction of a cytosine deaminase gene preserves the stemness of mesenchymal stem cells. Exp Mol Med 45: e10.
59. Hermida-Gomez T, Fuentes-Boquete I, Gimeno-Longas MJ, Muinos-Lopez E, Diaz-Prado S, et al. (2010) Quantification of cells expressing mesenchymal stem cell markers in healthy and osteoarthritic synovial membranes. J Rheumatol 38: 339-349.