Prostate stromal cell proteomics analysis discriminates normal from tumour reactive stromal phenotypes

Oncotarget

Volumn 7, Issue 15, 2016, Pages 20124-20139

  Webber, Jason P ^a   Spary, Lisa K ^a   Mason, Malcolm D ^a   Tabi, Zsuzsanna ^a   Brewis, Ian A ^b   Clayton, Aled ^a  

^a CARDIFF UNIVERSITY   (United Kingdom)

^b CARDIFF UNIVERSITY SCHOOL OF MEDICINE   (United Kingdom)

Author keywords

Angiogenesis; Cancer associated fibroblasts; Exosomes; Prostate cancer

Indexed keywords

ALDEHYDE DEHYDROGENASE; ALPHA SMOOTH MUSCLE ACTIN; BASP1 PROTEIN; CALD1 PROTEIN; CALU PROTEIN; CAVEOLIN 1; CYTOKERATIN; DESMIN; ION CHANNEL; TRANSFORMING GROWTH FACTOR BETA; TRANSGELIN; UNCLASSIFIED DRUG; VOLTAGE DEPENDENT ANION CHANNEL 1; PROTEOME; TUMOR MARKER;

ARTICLE; CANCER GROWTH; CANCER PATIENT; CARCINOGENESIS; CONTROLLED STUDY; CYTOSKELETON; ENDOTHELIUM CELL; EXOSOME; HUMAN; MYOFIBROBLAST; PHENOTYPE; PROSTATE CANCER; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEOMICS; STROMA CELL; CELL CULTURE; CELL DIFFERENTIATION; MALE; METABOLISM; PATHOLOGY; PROCEDURES; PROSTATE; PROSTATE TUMOR;

BIOMARKERS, TUMOR; CELL DIFFERENTIATION; CELLS, CULTURED; EXOSOMES; HUMANS; MALE; MYOFIBROBLASTS; PHENOTYPE; PROSTATE; PROSTATIC NEOPLASMS; PROTEOME; PROTEOMICS; STROMAL CELLS; TRANSFORMING GROWTH FACTOR BETA;

EID: 84964711886     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.7716     Document Type: Article

References (59)

1. Moorman AM, Vink R, Heijmans HJ, van der Palen J, Kouwenhoven EA. The prognostic value of tumour-stroma ratio in triple-negative breast cancer. Eur J Surg Oncol. 2012; 38:307-313.
2. Mesker WE, Liefers G-J, Junggeburt JMC, van Pelt GW, Alberici P, Kuppen PJK, Miranda NF, van Leeuwen KAM, Morreau H, Szuhai K, Tollenaar RAEM and Tanke HJ. Presence of a high amount of stroma and downregulation of SMAD4 predict for worse survival for stage I-II colon cancer patients. Cell Oncol. 2009; 31:169-178.
3. Yanagisawa N, Li R, Rowley D, Liu H, Kadmon D, Miles BJ, Wheeler TM, Ayala GE. Stromogenic prostatic carcinoma pattern (carcinomas with reactive stromal grade 3) in needle biopsies predicts biochemical recurrence-free survival in patients after radical prostatectomy. Hum Pathol. 2007; 38:1611-1620.
4. Tuxhorn JA, Ayala GE, Smith MJ, Smith VC, Dang TD, Rowley DR. Reactive Stroma in Human Prostate Cancer. Clin Cancer Res. 2002; 8:2912-2923.
5. Saigusa S, Toiyama Y, Tanaka K, Yokoe T, Okugawa Y, Fujikawa H, Matsusita K, Kawamura M, Inoue Y, Miki C, Kusunoki M. Cancer-associated fibroblasts correlate with poor prognosis in rectal cancer after chemoradiotherapy. Int J Oncol. 2011; 38:655-663.
6. Farmer P, Bonnefoi H, Anderle P, Cameron D, Wirapati P, Becette V, Andre S, Piccart M, Campone M, Brain E, MacGrogan G, Petit T, Jassem J, Bibeau F, Blot E, Bogaerts J, et al. A stroma-related gene signature predicts resistance to neoadjuvant chemotherapy in breast cancer. Nat Med. 2009; 15:68-74.
7. Kojima Y, Acar A, Eaton EN, Mellody KT, Scheel C, Ben-Porath I, Onder TT, Wang ZC, Richardson AL, Weinberg RA, Orimo A. Autocrine TGF-beta and stromal cell-derived factor-1 (SDF-1) signaling drives the evolution of tumorpromoting mammary stromal myofibroblasts. Proc Natl Acad Sci. 2010; 107:20009-20014.
8. Tuxhorn JA, McAlhany SJ, Yang F, Dang TD, Rowley DR. Inhibition of Transforming Growth Factor-β Activity Decreases Angiogenesis in a Human Prostate Cancerreactive Stroma Xenograft Model. Cancer Res. 2002; 62:6021-6025.
9. Orimo A, Gupta PB, Sgroi DC, Arenzana-Seisdedos F, Delaunay T, Naeem R, Carey VJ, Richardson AL, Weinberg RA. Stromal fibroblasts present in invasive human breast carcinomas promote tumor growth and angiogenesis through elevated SDF-1/CXCL12 secretion. Cell. 2005; 121:335-348.
10. Olumi AF, Grossfeld GD, Hayward SW, Carroll PR, Tlsty TD, Cunha GR. Carcinoma-associated Fibroblasts Direct Tumor Progression of Initiated Human Prostatic Epithelium. Cancer Res. 1999; 59:5002-5011.
11. Hu M, Peluffo G, Chen H, Gelman R, Schnitt S, Polyak K. Role of COX-2 in epithelial-stromal cell interactions and progression of ductal carcinoma in situ of the breast. Proc Natl Acad Sci U S A. 2009; 106:3372-3377.
12. Yang F, Tuxhorn JA, Ressler SJ, McAlhany SJ, Dang TD, Rowley DR. Stromal Expression of Connective Tissue Growth Factor Promotes Angiogenesis and Prostate Cancer Tumorigenesis. Cancer Research. 2005; 65:8887-8895.
13. Tomas D, Spajic B, Milosevic M, Demirovic A, Marusic Z, Kruslin B. Intensity of stromal changes predicts biochemical recurrence-free survival in prostatic carcinoma. Scand J Urol Nephrol. 2010; 44:284-290.
14. Rhim AD, Oberstein PE, Thomas DH, Mirek ET, Palermo CF, Sastra SA, Dekleva EN, Saunders T, Becerra CP, Tattersall IW, Westphalen CB, Kitajewski J, Fernandez-Barrena MG, Fernandez-Zapico ME, Iacobuzio-Donahue C, Olive KP, et al. Stromal Elements Act to Restrain, Rather Than Support, Pancreatic Ductal Adenocarcinoma. Cancer Cell. 2014; 25:735-747.
15. Özdemir BC, Pentcheva-Hoang T, Carstens JL, Zheng X, Wu C-C, Simpson TR, Laklai H, Sugimoto H, Kahlert C, Novitskiy SV, De Jesus-Acosta A, Sharma P, Heidari P, Mahmood U, Chin L, Moses HL, et al. Depletion of Carcinoma-Associated Fibroblasts and Fibrosis Induces Immunosuppression and Accelerates Pancreas Cancer with Reduced Survival. Cancer Cell. 2014; 25:719-734.
16. Kalluri R, Zeisberg M. Fibroblasts in cancer. Nat Rev Cancer. 2006; 6:392-401.
17. Karnoub AE, Dash AB, Vo AP, Sullivan A, Brooks MW, Bell GW, Richardson AL, Polyak K, Tubo R, Weinberg RA. Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nature. 2007; 449:557-563.
18. Kucerova L, Skolekova S, Matuskova M, Bohac M, Kozovska Z. Altered features and increased chemosensitivity of human breast cancer cells mediated by adipose tissue-derived mesenchymal stromal cells. BMC Cancer 2013; 13:535.
19. Hinz B, Phan S, Thannickal V, Galli A, Bochaton-Piallat M, Gabbiani G. The myofibroblast: one function, multiple origins. Am J Pathol. 2007; 170:1807-1816.
20. Hinz B, Phan SH, Thannickal VJ, Prunotto M, Desmoulière A, Varga J, De Wever O, Mareel M, Gabbiani G. Recent Developments in Myofibroblast Biology: Paradigms for Connective Tissue Remodeling. Am J Path. 2012; 180:1340-1355.
21. Maitland NJ. Carcinoma-derived exosomes modify microenvironment. Oncotarget. 2015; 6:1344-1345. doi: 10.18632/oncotarget.3182.
22. Webber J, Steadman R, Mason MD, Tabi Z, Clayton A. Cancer exosomes trigger fibroblast to myofibroblast differentiation. Cancer Res. 2010; 70:9621-9630.
23. Chowdhury R, Webber JP, Gurney M, Mason MD, Tabi Z, Clayton A. Cancer exosomes trigger mesenchymal stem cell differentiation into pro-angiogenic and pro-invasive myofibroblasts. Oncotarget. 2015; 6:715-31. doi: 10.18632/oncotarget.2711.
24. Gu J, Qian H, Shen L, Zhang X, Zhu W, Huang L, Yan Y, Mao F, Zhao C, Shi Y, Xu W. Gastric Cancer Exosomes Trigger Differentiation of Umbilical Cord Derived Mesenchymal Stem Cells to Carcinoma-Associated Fibroblasts through TGF-β/Smad Pathway. PLoS One. 2012; 7:e52465.
25. Cho JA, Park H, Lim EH, Lee KW. Exosomes from breast cancer cells can convert adipose tissue-derived mesenchymal stem cells into myofibroblast-like cells. Int J Oncol. 2012; 40:130-138.
26. Webber JP, Spary LK, Sanders AJ, Chowdhury R, Jiang WG, Steadman R, Wymant J, Jones AT, Kynaston H, Mason MD, Tabi Z, Clayton A. Differentiation of tumourpromoting stromal myofibroblasts by cancer exosomes. Oncogene. 2015; 34:290-302.
27. Brennan P, Shore AM, Clement M, Hewamana S, M C, Jones, Giles P, Fegan C, Pepper C, Brewis IA. Quantitative nuclear proteomics reveals new phenotypes altered in lymphoblastoid cells. Proteomics-Clinical Applications. 2009; 3:359-369.
28. Sexton K, Balharry D, Brennan P, McLaren J, Brewis IA, BéruBé K. Proteomic profiling of human respiratory epithelia by iTRAQ reveals biomarkers of exposure and harm by tobacco smoke components. Biomarkers. 2011; 16:567-576.
29. Dvorak HF. Tumors: Wounds That Do Not Heal-Redux. Cancer Immunology Research. 2015; 3:1-11.
30. Karagiannis GS, Poutahidis T, Erdman SE, Kirsch R, Riddell RH, Diamandis EP. Cancer-Associated Fibroblasts Drive the Progression of Metastasis through both Paracrine and Mechanical Pressure on Cancer Tissue. Molecular Cancer Research. 2012; 10:1403-1418.
31. Costea DE, Hills A, Osman AH, Thurlow J, Kalna G, Huang X, Pena Murillo C, Parajuli H, Suliman S, Kulasekara KK, Johannessen AC, Partridge M. Identification of Two Distinct Carcinoma-Associated Fibroblast Subtypes with Differential Tumor-Promoting Abilities in Oral Squamous Cell Carcinoma. Cancer Research. 2013; 73:3888-3901.
32. Franco OE, Jiang M, Strand DW, Peacock J, Fernandez S, Jackson RS, Revelo MP, Bhowmick NA, Hayward SW. Altered TGF-β Signaling in a Subpopulation of Human Stromal Cells Promotes Prostatic Carcinogenesis. Cancer Research. 2011; 71:1272-1281.
33. Cho JA, Park H, Lim EH, Kim KH, Choi JS, Lee JH, Shin JW, Lee KW. Exosomes from ovarian cancer cells induce adipose tissue-derived mesenchymal stem cells to acquire the physical and functional characteristics of tumor-supporting myofibroblasts. Gynecol Oncol. 2011; 123:379-386.
34. Hoshino A, Costa-Silva B, Shen T-L, Rodrigues G, Hashimoto A, Tesic Mark M, Molina H, Kohsaka S, Di Giannatale A, Ceder S, Singh S, Williams C, Soplop N, Uryu K, Pharmer L, King T, et al. Tumour exosome integrins determine organotropic metastasis. Nature. 2015; 527:329-335.
35. Duijvesz D, Luider T, Bangma CH, Jenster G. Exosomes as Biomarker Treasure Chests for Prostate Cancer. European Urology. 2011; 59:823-831.
36. Untergasser G, Gander R, Lilg C, Lepperdinger G, Plas E, Berger P. Profiling molecular targets of TGF-beta1 in prostate fibroblast-to-myofibroblast transdifferentiation. Mech Ageing Dev. 2005; 126:59-69.
37. Saffarini CM, McDonnell EV, Amin A, Spade DJ, Huse SM, Kostadinov S, Hall SJ, Boekelheide K. Maturation of the developing human fetal prostate in a rodent xenograft model. Prostate. 2013; 73:1761-1775.
38. Han S, Khuri FR, Roman J. Fibronectin stimulates nonsmall cell lung carcinoma cell growth through activation of Akt/mammalian target of rapamycin/S6 kinase and inactivation of LKB1/AMP-activated protein kinase signal pathways. Cancer Res. 2006; 66:315-323.
39. Korshunova I, Caroni P, Kolkova K, Berezin V, Bock E, Walmod PS. Characterization of BASP1-mediated neurite outgrowth. Journal of Neuroscience Research. 2008; 86:2201-2213.
40. Wiederkehr A, Staple J, Caroni P. The Motility-Associated Proteins GAP-43, MARCKS, and CAP-23 Share Unique Targeting and Surface Activity-Inducing Properties. Experimental Cell Research. 1997; 236:103-116.
41. Hartl M, Nist A, Khan MI, Valovka T, Bister K. Inhibition of Myc-induced cell transformation by brain acid-soluble protein 1 (BASP1). Proceedings of the National Academy of Sciences. 2009; 106:5604-5609.
42. Cojoc M, Peitzsch C, Kurth I, Trautmann F, Kunz-Schughart LA, Telegeev GD, Stakhovsky EA, Walker JR, Simin K, Lyle S, Fuessel S, Erdmann K, Wirth MP, Krause M, Baumann M, Dubrovska A. Aldehyde Dehydrogenase Is Regulated by β-Catenin/TCF and Promotes Radioresistance in Prostate Cancer Progenitor Cells. Cancer Research. 2015; 75:1482-1494.
43. Zhao L, Yu N, Guo T, Hou Y, Zeng Z, Yang X, Hu P, Tang X, Wang J, Liu M. Tissue Biomarkers for Prognosis of Prostate Cancer: A Systematic Review and Meta-analysis. Cancer Epidemiology Biomarkers & Prevention. 2014; 23:1047-1054.
44. Li T, Su Y, Mei Y, Leng Q, Leng B, Liu Z, Stass SA, Jiang F. ALDH1A1 is a marker for malignant prostate stem cells and predictor of prostate cancer patients/' outcome. Lab Invest. 2009; 90:234-244.
45. Li H-J, Reinhardt F, Herschman HR, Weinberg RA. Cancer-Stimulated Mesenchymal Stem Cells Create a Carcinoma Stem Cell Niche via Prostaglandin E2 Signaling. Cancer Discovery. 2012; 2:840-855.
46. Jester JV, Brown D, Pappa A, Vasiliou V. Myofibroblast differentiation modulates keratocyte crystallin protein expression, concentration, and cellular light scattering. Invest Ophthalmol Vis Sci. 2012; 53:770-778.
47. Zheng P, Wang Q, Teng J, Chen J. Calumenin and fibulin-1 on tumor metastasis: Implications for pharmacology. Pharmacol Res. 2015; 99:11-15.
48. Pedram A, Razandi M, Levin ER. Natriuretic Peptides Suppress Vascular Endothelial Cell Growth Factor Signaling to Angiogenesis. Endocrinology. 2001; 142:1578-1586.
49. Pin A-L, Houle F, Fournier P, Guillonneau M, Paquet ÉR, Simard MJ, Royal I, Huot J. Annexin-1-mediated Endothelial Cell Migration and Angiogenesis Are Regulated by Vascular Endothelial Growth Factor (VEGF)-induced Inhibition of miR-196a Expression. Journal of Biological Chemistry. 2012; 287:30541-30551.
50. Tomas D, Ulamec M, Hudolin T, Bulimbasic S, Belicza M, Kruslin B. Myofibroblastic stromal reaction and expression of tenascin-C and laminin in prostate adenocarcinoma. Prostate Cancer Prostatic Dis. 2006; 9:414-419.
51. Guido C, Whitaker-Menezes D, Capparelli C, Balliet R, Lin Z, Pestell RG, Howell A, Aquila S, Andò S, Martinez-Outschoorn U, Sotgia F, Lisanti MP. Metabolic reprogramming of cancer-associated fibroblasts by TGF-β drives tumor growth: Connecting TGF-β signaling with "Warburglike" cancer metabolism and L-lactate production. Cell Cycle. 2012; 11:3019-3035.
52. Lisanti MP, Martinez-Outschoorn UE, Sotgia F. Oncogenes induce the cancer-associated fibroblast phenotype: Metabolic symbiosis and "fibroblast addiction" are new therapeutic targets for drug discovery. Cell Cycle. 2013; 12:2723-2732.
53. Ayala G, Morello M, Frolov A, You S, Li R, Rosati F, Bartolucci G, Danza G, Adam RM, Thompson TC, Lisanti MP, Freeman MR, Di Vizio D. Loss of caveolin-1 in prostate cancer stroma correlates with reduced relapse-free survival and is functionally relevant to tumour progression. The Journal of Pathology. 2013; 231:77-87.
54. Pavlides S, Vera I, Gandara R, Sneddon S, Pestell RG, Mercier I, Martinez-Outschoorn UE, Whitaker-Menezes D, Howell A, Sotgia F, Lisanti MP. Warburg Meets Autophagy: Cancer-Associated Fibroblasts Accelerate Tumor Growth and Metastasis via Oxidative Stress, Mitophagy, and Aerobic Glycolysis. Antioxidants & Redox Signaling. 2011; 16:1264-1284.
55. Mitchell JP, Court J, Mason MD, Tabi Z, Clayton A. Increased exosome production from tumour cell cultures using the Integra CELLine Culture System. J Immunol Methods. 2008; 335:98-105.
56. Webber J, Stone TC, Katilius E, Smith BC, Gordon B, Mason MD, Tabi Z, Brewis IA, Clayton A. Proteomics Analysis of Cancer Exosomes Using a Novel Modified Aptamer-based Array (SOMAscan™) Platform. Mol Cell Proteomics. 2014; 13:1050-1064.
57. Welton JL, Khanna S, Giles PJ, Brennan P, Brewis IA, Staffurth J, Mason MD, Clayton A. Proteomic analysis of bladder cancer exosomes. Mol Cell Proteomics. 2010; 6:1324-1338.
58. Webber J, Clayton A. How pure are your vesicles? J Extracell Vesicles. 2013;19861
59. Shilov IV, Seymour SL, Patel AA, Loboda A, Tang WH, Keating SP, Hunter CL, Nuwaysir LM, Schaeffer DA. The Paragon Algorithm, a Next Generation Search Engine That Uses Sequence Temperature Values and Feature Probabilities to Identify Peptides from Tandem Mass Spectra. Molecular & Cellular Proteomics. 2007; 6:1638-1655.