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Published in: Breast Cancer Research 1/2020

01-12-2020 | Breast Cancer | Research article

Extracellular vesicles from young women’s breast cancer patients drive increased invasion of non-malignant cells via the Focal Adhesion Kinase pathway: a proteomic approach

Authors: Kimberly R. Jordan, Jessica K. Hall, Troy Schedin, Michelle Borakove, Jenny J. Xian, Monika Dzieciatkowska, Traci R. Lyons, Pepper Schedin, Kirk C. Hansen, Virginia F. Borges

Published in: Breast Cancer Research | Issue 1/2020

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Abstract

Background

Extracellular vesicles (EVs) are small membrane particles that contribute to cancer progression and metastases by transporting biologically significant proteins and nucleic acids. They may also serve as biomarkers of various disease states or important therapeutic targets. Breast cancer EVs have the potential to change the behavior of other cells in their microenvironment. However, the proteomic content of EVs isolated from young women’s breast cancer patients and the mechanisms underlying the influence of EVs on tumor cell behavior have not yet been reported.

Methods

In our current translational studies, we compared the proteomic content of EVs isolated from invasive breast cancer cell lines and plasma samples from young women’s breast cancer (YWBC) patients and age-matched healthy donors using mass spectrometry. We analyzed the functionality of EVs in two dimensional tumor cell invasion assays and the gene expression changes in tumor cells after incubation with EVs.

Results

We found that treatment with EVs from both invasive breast cancer cell lines and plasma of YWBC patients altered the invasive properties of non-invasive breast cancer cells. Proteomics identified differences between EVs from YWBC patients and healthy donors that correlated with their altered function. Further, we identified gene expression changes in non-invasive breast cancer cells after treatment with EVs that implicate the Focal Adhesion Kinase (FAK) signaling pathway as a potential targetable pathway affected by breast cancer-derived EVs.

Conclusions

Our results suggest that the proteome of EVs from breast cancer patients reflects their functionality in tumor motility assays and may help elucidate the role of EVs in breast cancer progression.
Appendix
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Literature
1.
2.
go back to reference Gajdos C, Tartter PI, Bleiweiss IJ, Bodian C, Brower ST. Stage 0 to stage III breast cancer in young women. J Am Coll Surg. 2000;190(5):523–9.PubMedCrossRef Gajdos C, Tartter PI, Bleiweiss IJ, Bodian C, Brower ST. Stage 0 to stage III breast cancer in young women. J Am Coll Surg. 2000;190(5):523–9.PubMedCrossRef
3.
go back to reference Korde LA, Partridge AH, Esser M, Lewis S, Simha J, Johnson RH, Breast Cancer in Young Women: Research Priorities. A report of the young survival coalition research think tank meeting. J Adolesc Young Adult Oncol. 2015;4(1):34–43.PubMedCrossRef Korde LA, Partridge AH, Esser M, Lewis S, Simha J, Johnson RH, Breast Cancer in Young Women: Research Priorities. A report of the young survival coalition research think tank meeting. J Adolesc Young Adult Oncol. 2015;4(1):34–43.PubMedCrossRef
4.
go back to reference Yanez-Mo M, Siljander PR, Andreu Z, Zavec AB, Borras FE, Buzas EI, et al. Biological properties of extracellular vesicles and their physiological functions. J Extracell Vesicles. 2015;4:27066.PubMedCrossRef Yanez-Mo M, Siljander PR, Andreu Z, Zavec AB, Borras FE, Buzas EI, et al. Biological properties of extracellular vesicles and their physiological functions. J Extracell Vesicles. 2015;4:27066.PubMedCrossRef
5.
go back to reference Tkach M, Thery C. Communication by extracellular vesicles: where we are and where we need to go. Cell. 2016;164(6):1226–32.PubMedCrossRef Tkach M, Thery C. Communication by extracellular vesicles: where we are and where we need to go. Cell. 2016;164(6):1226–32.PubMedCrossRef
6.
go back to reference Taylor DD, Shah S. Methods of isolating extracellular vesicles impact down-stream analyses of their cargoes. Methods. 2015;87:3–10.PubMedCrossRef Taylor DD, Shah S. Methods of isolating extracellular vesicles impact down-stream analyses of their cargoes. Methods. 2015;87:3–10.PubMedCrossRef
7.
go back to reference Villagrasa A, Alvarez PJ, Osuna A, Garrido JM, Aranega A, Rodriguez-Serrano F. Exosomes derived from breast cancer cells, small Trojan horses? J Mammary Gland Biol Neoplasia. 2014;19(3–4):303–13.PubMedCrossRef Villagrasa A, Alvarez PJ, Osuna A, Garrido JM, Aranega A, Rodriguez-Serrano F. Exosomes derived from breast cancer cells, small Trojan horses? J Mammary Gland Biol Neoplasia. 2014;19(3–4):303–13.PubMedCrossRef
8.
go back to reference Becker A, Thakur BK, Weiss JM, Kim HS, Peinado H, Lyden D. Extracellular vesicles in cancer: cell-to-cell mediators of metastasis. Cancer Cell. 2016;30(6):836–48.PubMedPubMedCentralCrossRef Becker A, Thakur BK, Weiss JM, Kim HS, Peinado H, Lyden D. Extracellular vesicles in cancer: cell-to-cell mediators of metastasis. Cancer Cell. 2016;30(6):836–48.PubMedPubMedCentralCrossRef
9.
go back to reference Katsuda T, Kosaka N, Ochiya T. The roles of extracellular vesicles in cancer biology: toward the development of novel cancer biomarkers. Proteomics. 2014;14(4–5):412–25.PubMedCrossRef Katsuda T, Kosaka N, Ochiya T. The roles of extracellular vesicles in cancer biology: toward the development of novel cancer biomarkers. Proteomics. 2014;14(4–5):412–25.PubMedCrossRef
10.
11.
go back to reference Colombo M, Raposo G, Thery C. Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu Rev Cell Dev Biol. 2014;30:255–89.PubMedCrossRef Colombo M, Raposo G, Thery C. Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu Rev Cell Dev Biol. 2014;30:255–89.PubMedCrossRef
12.
go back to reference Peinado H, Lavotshkin S, Lyden D. The secreted factors responsible for pre-metastatic niche formation: old sayings and new thoughts. Semin Cancer Biol. 2011;21(2):139–46.PubMedCrossRef Peinado H, Lavotshkin S, Lyden D. The secreted factors responsible for pre-metastatic niche formation: old sayings and new thoughts. Semin Cancer Biol. 2011;21(2):139–46.PubMedCrossRef
13.
go back to reference Costa-Silva B, Aiello NM, Ocean AJ, Singh S, Zhang H, Thakur BK, et al. Pancreatic cancer exosomes initiate pre-metastatic niche formation in the liver. Nat Cell Biol. 2015;17(6):816–26.PubMedPubMedCentralCrossRef Costa-Silva B, Aiello NM, Ocean AJ, Singh S, Zhang H, Thakur BK, et al. Pancreatic cancer exosomes initiate pre-metastatic niche formation in the liver. Nat Cell Biol. 2015;17(6):816–26.PubMedPubMedCentralCrossRef
15.
go back to reference He M, Qin H, Poon TC, Sze SC, Ding X, Co NN, et al. Hepatocellular carcinoma-derived exosomes promote motility of immortalized hepatocyte through transfer of oncogenic proteins and RNAs. Carcinogenesis. 2015;36(9):1008–18.PubMedCrossRef He M, Qin H, Poon TC, Sze SC, Ding X, Co NN, et al. Hepatocellular carcinoma-derived exosomes promote motility of immortalized hepatocyte through transfer of oncogenic proteins and RNAs. Carcinogenesis. 2015;36(9):1008–18.PubMedCrossRef
16.
go back to reference Chan YK, Zhang H, Liu P, Tsao SW, Lung ML, Mak NK, et al. Proteomic analysis of exosomes from nasopharyngeal carcinoma cell identifies intercellular transfer of angiogenic proteins. Int J Cancer. 2015;137(8):1830–41.PubMedCrossRef Chan YK, Zhang H, Liu P, Tsao SW, Lung ML, Mak NK, et al. Proteomic analysis of exosomes from nasopharyngeal carcinoma cell identifies intercellular transfer of angiogenic proteins. Int J Cancer. 2015;137(8):1830–41.PubMedCrossRef
17.
go back to reference Marimpietri D, Petretto A, Raffaghello L, Pezzolo A, Gagliani C, Tacchetti C, et al. Proteome profiling of neuroblastoma-derived exosomes reveal the expression of proteins potentially involved in tumor progression. Plos One. 2013;8(9):e75054.PubMedPubMedCentralCrossRef Marimpietri D, Petretto A, Raffaghello L, Pezzolo A, Gagliani C, Tacchetti C, et al. Proteome profiling of neuroblastoma-derived exosomes reveal the expression of proteins potentially involved in tumor progression. Plos One. 2013;8(9):e75054.PubMedPubMedCentralCrossRef
18.
go back to reference Overbye A, Skotland T, Koehler CJ, Thiede B, Seierstad T, Berge V, et al. Identification of prostate cancer biomarkers in urinary exosomes. Oncotarget. 2015;6(30):30357–76.PubMedPubMedCentralCrossRef Overbye A, Skotland T, Koehler CJ, Thiede B, Seierstad T, Berge V, et al. Identification of prostate cancer biomarkers in urinary exosomes. Oncotarget. 2015;6(30):30357–76.PubMedPubMedCentralCrossRef
19.
go back to reference Szajnik M, Derbis M, Lach M, Patalas P, Michalak M, Drzewiecka H, et al. Exosomes in Plasma of Patients with Ovarian Carcinoma: Potential Biomarkers of Tumor Progression and Response to Therapy. Gynecol Obstet (Sunnyvale). 2013;Suppl 4:3. https://doi.org/10.3390/ijms21145066. Szajnik M, Derbis M, Lach M, Patalas P, Michalak M, Drzewiecka H, et al. Exosomes in Plasma of Patients with Ovarian Carcinoma: Potential Biomarkers of Tumor Progression and Response to Therapy. Gynecol Obstet (Sunnyvale). 2013;Suppl 4:3. https://​doi.​org/​10.​3390/​ijms21145066.
20.
go back to reference Redzic JS, Ung TH, Graner MW. Glioblastoma extracellular vesicles: reservoirs of potential biomarkers. Pharmgenomics Pers Med. 2014;7:65–77.PubMedPubMedCentral Redzic JS, Ung TH, Graner MW. Glioblastoma extracellular vesicles: reservoirs of potential biomarkers. Pharmgenomics Pers Med. 2014;7:65–77.PubMedPubMedCentral
21.
go back to reference Melo SA, Luecke LB, Kahlert C, Fernandez AF, Gammon ST, Kaye J, et al. Glypican-1 identifies cancer exosomes and detects early pancreatic cancer. Nature. 2015;523(7559):177–82.PubMedPubMedCentralCrossRef Melo SA, Luecke LB, Kahlert C, Fernandez AF, Gammon ST, Kaye J, et al. Glypican-1 identifies cancer exosomes and detects early pancreatic cancer. Nature. 2015;523(7559):177–82.PubMedPubMedCentralCrossRef
22.
go back to reference Matsumura T, Sugimachi K, Iinuma H, Takahashi Y, Kurashige J, Sawada G, et al. Exosomal microRNA in serum is a novel biomarker of recurrence in human colorectal cancer. Br J Cancer. 2015;113(2):275–81.PubMedPubMedCentralCrossRef Matsumura T, Sugimachi K, Iinuma H, Takahashi Y, Kurashige J, Sawada G, et al. Exosomal microRNA in serum is a novel biomarker of recurrence in human colorectal cancer. Br J Cancer. 2015;113(2):275–81.PubMedPubMedCentralCrossRef
23.
go back to reference Lane RE, Korbie D, Hill MM, Trau M. Extracellular vesicles as circulating cancer biomarkers: opportunities and challenges. Clin Transl Med. 2018;7(1):14.PubMedPubMedCentralCrossRef Lane RE, Korbie D, Hill MM, Trau M. Extracellular vesicles as circulating cancer biomarkers: opportunities and challenges. Clin Transl Med. 2018;7(1):14.PubMedPubMedCentralCrossRef
24.
go back to reference Haney MJ, Klyachko NL, Zhao Y, Gupta R, Plotnikova EG, He Z, et al. Exosomes as drug delivery vehicles for Parkinson’s disease therapy. J Control Release. 2015;207:18–30.PubMedPubMedCentralCrossRef Haney MJ, Klyachko NL, Zhao Y, Gupta R, Plotnikova EG, He Z, et al. Exosomes as drug delivery vehicles for Parkinson’s disease therapy. J Control Release. 2015;207:18–30.PubMedPubMedCentralCrossRef
26.
go back to reference Tran TH, Mattheolabakis G, Aldawsari H, Amiji M. Exosomes as nanocarriers for immunotherapy of cancer and inflammatory diseases. Clin Immunol. 2015;160(1):46–58.PubMedCrossRef Tran TH, Mattheolabakis G, Aldawsari H, Amiji M. Exosomes as nanocarriers for immunotherapy of cancer and inflammatory diseases. Clin Immunol. 2015;160(1):46–58.PubMedCrossRef
27.
go back to reference Pitt JM, Charrier M, Viaud S, Andre F, Besse B, Chaput N, et al. Dendritic cell-derived exosomes as immunotherapies in the fight against cancer. J Immunol. 2014;193(3):1006–11.PubMedCrossRef Pitt JM, Charrier M, Viaud S, Andre F, Besse B, Chaput N, et al. Dendritic cell-derived exosomes as immunotherapies in the fight against cancer. J Immunol. 2014;193(3):1006–11.PubMedCrossRef
28.
go back to reference Viaud S, Thery C, Ploix S, Tursz T, Lapierre V, Lantz O, et al. Dendritic cell-derived exosomes for cancer immunotherapy: what's next? Cancer Res. 2010;70(4):1281–5.PubMedCrossRef Viaud S, Thery C, Ploix S, Tursz T, Lapierre V, Lantz O, et al. Dendritic cell-derived exosomes for cancer immunotherapy: what's next? Cancer Res. 2010;70(4):1281–5.PubMedCrossRef
29.
go back to reference Sun YZ, Ruan JS, Jiang ZS, Wang L, Wang SM. Extracellular vesicles: a new perspective in tumor therapy. Biomed Res Int. 2018;2018:2687954.PubMedPubMedCentral Sun YZ, Ruan JS, Jiang ZS, Wang L, Wang SM. Extracellular vesicles: a new perspective in tumor therapy. Biomed Res Int. 2018;2018:2687954.PubMedPubMedCentral
30.
go back to reference Yu DD, Wu Y, Shen HY, Lv MM, Chen WX, Zhang XH, et al. Exosomes in development, metastasis and drug resistance of breast cancer. Cancer Sci. 2015;106(8):959–64.PubMedPubMedCentralCrossRef Yu DD, Wu Y, Shen HY, Lv MM, Chen WX, Zhang XH, et al. Exosomes in development, metastasis and drug resistance of breast cancer. Cancer Sci. 2015;106(8):959–64.PubMedPubMedCentralCrossRef
31.
go back to reference Lowry MC, Gallagher WM, O'Driscoll L. The role of exosomes in breast cancer. Clin Chem. 2015;61(12):1457–65.PubMedCrossRef Lowry MC, Gallagher WM, O'Driscoll L. The role of exosomes in breast cancer. Clin Chem. 2015;61(12):1457–65.PubMedCrossRef
32.
go back to reference Zhong Z, Rosenow M, Xiao N, Spetzler D. Profiling plasma extracellular vesicle by pluronic block-copolymer based enrichment method unveils features associated with breast cancer aggression, metastasis and invasion. J Extracell Vesicles. 2018;7(1):1458574.PubMedPubMedCentralCrossRef Zhong Z, Rosenow M, Xiao N, Spetzler D. Profiling plasma extracellular vesicle by pluronic block-copolymer based enrichment method unveils features associated with breast cancer aggression, metastasis and invasion. J Extracell Vesicles. 2018;7(1):1458574.PubMedPubMedCentralCrossRef
34.
go back to reference Frame MC, Patel H, Serrels B, Lietha D, Eck MJ. The FERM domain: organizing the structure and function of FAK. Nat Rev Mol Cell Biol. 2010;11(11):802–14.PubMedCrossRef Frame MC, Patel H, Serrels B, Lietha D, Eck MJ. The FERM domain: organizing the structure and function of FAK. Nat Rev Mol Cell Biol. 2010;11(11):802–14.PubMedCrossRef
35.
go back to reference Sood AK, Armaiz-Pena GN, Halder J, Nick AM, Stone RL, Hu W, et al. Adrenergic modulation of focal adhesion kinase protects human ovarian cancer cells from anoikis. J Clin Invest. 2010;120(5):1515–23.PubMedPubMedCentralCrossRef Sood AK, Armaiz-Pena GN, Halder J, Nick AM, Stone RL, Hu W, et al. Adrenergic modulation of focal adhesion kinase protects human ovarian cancer cells from anoikis. J Clin Invest. 2010;120(5):1515–23.PubMedPubMedCentralCrossRef
36.
go back to reference Golubovskaya VM, Zheng M, Zhang L, Li JL, Cance WG. The direct effect of focal adhesion kinase (FAK), dominant-negative FAK, FAK-CD and FAK siRNA on gene expression and human MCF-7 breast cancer cell tumorigenesis. BMC Cancer. 2009;9:280.PubMedPubMedCentralCrossRef Golubovskaya VM, Zheng M, Zhang L, Li JL, Cance WG. The direct effect of focal adhesion kinase (FAK), dominant-negative FAK, FAK-CD and FAK siRNA on gene expression and human MCF-7 breast cancer cell tumorigenesis. BMC Cancer. 2009;9:280.PubMedPubMedCentralCrossRef
39.
go back to reference Antonyak MA, Cerione RA. The distinct traits of extracellular vesicles generated by transformed cells. Small GTPases. 2016. p. 1–6. Antonyak MA, Cerione RA. The distinct traits of extracellular vesicles generated by transformed cells. Small GTPases. 2016. p. 1–6.
40.
go back to reference Antonyak MA, Cerione RA. The distinct traits of extracellular vesicles generated by transformed cells. Small GTPases. 2018;9(5):427–32. Antonyak MA, Cerione RA. The distinct traits of extracellular vesicles generated by transformed cells. Small GTPases. 2018;9(5):427–32.
41.
go back to reference Stensheim H, Moller B, van Dijk T, Fossa SD. Cause-specific survival for women diagnosed with cancer during pregnancy or lactation: a registry-based cohort study. J Clin Oncol. 2009;27(1):45–51.PubMedCrossRef Stensheim H, Moller B, van Dijk T, Fossa SD. Cause-specific survival for women diagnosed with cancer during pregnancy or lactation: a registry-based cohort study. J Clin Oncol. 2009;27(1):45–51.PubMedCrossRef
42.
go back to reference Lambe M, Hsieh C, Trichopoulos D, Ekbom A, Pavia M, Adami HO. Transient increase in the risk of breast cancer after giving birth. N Engl J Med. 1994;331(1):5–9.PubMedCrossRef Lambe M, Hsieh C, Trichopoulos D, Ekbom A, Pavia M, Adami HO. Transient increase in the risk of breast cancer after giving birth. N Engl J Med. 1994;331(1):5–9.PubMedCrossRef
43.
go back to reference Harris PA, Taylor R, Thielke R, Payne J, Gonzalez N, Conde JG. Research electronic data capture (REDCap)--a metadata-driven methodology and workflow process for providing translational research informatics support. J Biomed Inform. 2009;42(2):377–81.CrossRefPubMed Harris PA, Taylor R, Thielke R, Payne J, Gonzalez N, Conde JG. Research electronic data capture (REDCap)--a metadata-driven methodology and workflow process for providing translational research informatics support. J Biomed Inform. 2009;42(2):377–81.CrossRefPubMed
45.
go back to reference Cailleau R, Olive M, Cruciger QV. Long-term human breast carcinoma cell lines of metastatic origin: preliminary characterization. In Vitro. 1978;14(11):911–5.PubMedCrossRef Cailleau R, Olive M, Cruciger QV. Long-term human breast carcinoma cell lines of metastatic origin: preliminary characterization. In Vitro. 1978;14(11):911–5.PubMedCrossRef
46.
go back to reference Hu M, Yao J, Carroll DK, Weremowicz S, Chen H, Carrasco D, et al. Regulation of in situ to invasive breast carcinoma transition. Cancer Cell. 2008;13(5):394–406.PubMedPubMedCentralCrossRef Hu M, Yao J, Carroll DK, Weremowicz S, Chen H, Carrasco D, et al. Regulation of in situ to invasive breast carcinoma transition. Cancer Cell. 2008;13(5):394–406.PubMedPubMedCentralCrossRef
47.
go back to reference Lyons TR, O'Brien J, Borges VF, Conklin MW, Keely PJ, Eliceiri KW, et al. Postpartum mammary gland involution drives progression of ductal carcinoma in situ through collagen and COX-2. Nat Med. 2011;17(9):1109–15.PubMedPubMedCentralCrossRef Lyons TR, O'Brien J, Borges VF, Conklin MW, Keely PJ, Eliceiri KW, et al. Postpartum mammary gland involution drives progression of ductal carcinoma in situ through collagen and COX-2. Nat Med. 2011;17(9):1109–15.PubMedPubMedCentralCrossRef
48.
go back to reference Wisniewski JR, Zougman A, Nagaraj N, Mann M. Universal sample preparation method for proteome analysis. Nat Methods. 2009;6(5):359–62.PubMedCrossRef Wisniewski JR, Zougman A, Nagaraj N, Mann M. Universal sample preparation method for proteome analysis. Nat Methods. 2009;6(5):359–62.PubMedCrossRef
49.
go back to reference Wither MJ, Hansen KC, Reisz JA. Mass spectrometry-based bottom-up proteomics: sample preparation, LC-MS/MS analysis, and database query strategies. Curr Protoc Protein Sci. 2016;86:16 4 1–4 20.CrossRef Wither MJ, Hansen KC, Reisz JA. Mass spectrometry-based bottom-up proteomics: sample preparation, LC-MS/MS analysis, and database query strategies. Curr Protoc Protein Sci. 2016;86:16 4 1–4 20.CrossRef
50.
go back to reference Huang DW, Sherman BT, Lempicki RA. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 2009;37(1):1–13.CrossRef Huang DW, Sherman BT, Lempicki RA. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 2009;37(1):1–13.CrossRef
51.
go back to reference Huang DW, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 2009;4(1):44–57.CrossRef Huang DW, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 2009;4(1):44–57.CrossRef
52.
go back to reference Xia J, Wishart DS. MetPA: a web-based metabolomics tool for pathway analysis and visualization. Bioinformatics. 2010;26(18):2342–4.PubMedCrossRef Xia J, Wishart DS. MetPA: a web-based metabolomics tool for pathway analysis and visualization. Bioinformatics. 2010;26(18):2342–4.PubMedCrossRef
53.
go back to reference Fisher KE, Pop A, Koh W, Anthis NJ, Saunders WB, Davis GE. Tumor cell invasion of collagen matrices requires coordinate lipid agonist-induced G-protein and membrane-type matrix metalloproteinase-1-dependent signaling. Mol Cancer. 2006;5:69.PubMedPubMedCentralCrossRef Fisher KE, Pop A, Koh W, Anthis NJ, Saunders WB, Davis GE. Tumor cell invasion of collagen matrices requires coordinate lipid agonist-induced G-protein and membrane-type matrix metalloproteinase-1-dependent signaling. Mol Cancer. 2006;5:69.PubMedPubMedCentralCrossRef
54.
go back to reference Ponnusamy MP, Seshacharyulu P, Lakshmanan I, Vaz AP, Chugh S, Batra SK. Emerging role of mucins in epithelial to mesenchymal transition. Curr Cancer Drug Targets. 2013;13(9):945–56.PubMedPubMedCentralCrossRef Ponnusamy MP, Seshacharyulu P, Lakshmanan I, Vaz AP, Chugh S, Batra SK. Emerging role of mucins in epithelial to mesenchymal transition. Curr Cancer Drug Targets. 2013;13(9):945–56.PubMedPubMedCentralCrossRef
55.
go back to reference Miller FR, Santner SJ, Tait L, Dawson PJ. MCF10DCIS.com xenograft model of human comedo ductal carcinoma in situ. J Natl Cancer Inst. 2000;92(14):1185–6.PubMedCrossRef Miller FR, Santner SJ, Tait L, Dawson PJ. MCF10DCIS.com xenograft model of human comedo ductal carcinoma in situ. J Natl Cancer Inst. 2000;92(14):1185–6.PubMedCrossRef
56.
go back to reference Harris DA, Patel SH, Gucek M, Hendrix A, Westbroek W, Taraska JW. Exosomes released from breast cancer carcinomas stimulate cell movement. Plos One. 2015;10(3):e0117495.PubMedPubMedCentralCrossRef Harris DA, Patel SH, Gucek M, Hendrix A, Westbroek W, Taraska JW. Exosomes released from breast cancer carcinomas stimulate cell movement. Plos One. 2015;10(3):e0117495.PubMedPubMedCentralCrossRef
57.
go back to reference Zlotogorski-Hurvitz A, Dayan D, Chaushu G, Salo T, Vered M. Morphological and molecular features of oral fluid-derived exosomes: oral cancer patients versus healthy individuals. J Cancer Res Clin Oncol. 2016;142(1):101–10.PubMedCrossRef Zlotogorski-Hurvitz A, Dayan D, Chaushu G, Salo T, Vered M. Morphological and molecular features of oral fluid-derived exosomes: oral cancer patients versus healthy individuals. J Cancer Res Clin Oncol. 2016;142(1):101–10.PubMedCrossRef
58.
go back to reference Wang J, Zhou Y, Lu J, Sun Y, Xiao H, Liu M, et al. Combined detection of serum exosomal miR-21 and HOTAIR as diagnostic and prognostic biomarkers for laryngeal squamous cell carcinoma. Med Oncol. 2014;31(9):148.PubMedCrossRef Wang J, Zhou Y, Lu J, Sun Y, Xiao H, Liu M, et al. Combined detection of serum exosomal miR-21 and HOTAIR as diagnostic and prognostic biomarkers for laryngeal squamous cell carcinoma. Med Oncol. 2014;31(9):148.PubMedCrossRef
59.
go back to reference Burns G, Brooks K, Wildung M, Navakanitworakul R, Christenson LK, Spencer TE. Extracellular vesicles in luminal fluid of the ovine uterus. Plos One. 2014;9(3):e90913.PubMedPubMedCentralCrossRef Burns G, Brooks K, Wildung M, Navakanitworakul R, Christenson LK, Spencer TE. Extracellular vesicles in luminal fluid of the ovine uterus. Plos One. 2014;9(3):e90913.PubMedPubMedCentralCrossRef
60.
go back to reference Epple LM, Griffiths SG, Dechkovskaia AM, Dusto NL, White J, Ouellette RJ, et al. Medulloblastoma exosome proteomics yield functional roles for extracellular vesicles. Plos One. 2012;7(7):e42064.PubMedPubMedCentralCrossRef Epple LM, Griffiths SG, Dechkovskaia AM, Dusto NL, White J, Ouellette RJ, et al. Medulloblastoma exosome proteomics yield functional roles for extracellular vesicles. Plos One. 2012;7(7):e42064.PubMedPubMedCentralCrossRef
61.
go back to reference Higginbotham JN, Demory Beckler M, Gephart JD, Franklin JL, Bogatcheva G, Kremers GJ, et al. Amphiregulin exosomes increase cancer cell invasion. Curr Biol. 2011;21(9):779–86.PubMedPubMedCentralCrossRef Higginbotham JN, Demory Beckler M, Gephart JD, Franklin JL, Bogatcheva G, Kremers GJ, et al. Amphiregulin exosomes increase cancer cell invasion. Curr Biol. 2011;21(9):779–86.PubMedPubMedCentralCrossRef
62.
go back to reference Gangoda L, Boukouris S, Liem M, Kalra H, Mathivanan S. Extracellular vesicles including exosomes are mediators of signal transduction: are they protective or pathogenic? Proteomics. 2015;15(2–3):260–71.PubMedCrossRef Gangoda L, Boukouris S, Liem M, Kalra H, Mathivanan S. Extracellular vesicles including exosomes are mediators of signal transduction: are they protective or pathogenic? Proteomics. 2015;15(2–3):260–71.PubMedCrossRef
65.
go back to reference da Silva PL, do Amaral VC, Gabrielli V, Montt Guevara MM, Mannella P, Baracat EC, et al. Prolactin promotes breast cancer cell migration through actin cytoskeleton remodeling. Front Endocrinol (Lausanne). 2015;6:186.CrossRef da Silva PL, do Amaral VC, Gabrielli V, Montt Guevara MM, Mannella P, Baracat EC, et al. Prolactin promotes breast cancer cell migration through actin cytoskeleton remodeling. Front Endocrinol (Lausanne). 2015;6:186.CrossRef
66.
go back to reference Lin YT, Liang SM, Wu YJ, Wu YJ, Lu YJ, Jan YJ, et al. Cordycepin Suppresses Endothelial Cell Proliferation, Migration, Angiogenesis, and Tumor Growth by Regulating Focal Adhesion Kinase and p53. Cancers (Basel). 2019;11(2):168. Lin YT, Liang SM, Wu YJ, Wu YJ, Lu YJ, Jan YJ, et al. Cordycepin Suppresses Endothelial Cell Proliferation, Migration, Angiogenesis, and Tumor Growth by Regulating Focal Adhesion Kinase and p53. Cancers (Basel). 2019;11(2):168.
67.
go back to reference Slack-Davis JK, Martin KH, Tilghman RW, Iwanicki M, Ung EJ, Autry C, et al. Cellular characterization of a novel focal adhesion kinase inhibitor. J Biol Chem. 2007;282(20):14845–52.PubMedCrossRef Slack-Davis JK, Martin KH, Tilghman RW, Iwanicki M, Ung EJ, Autry C, et al. Cellular characterization of a novel focal adhesion kinase inhibitor. J Biol Chem. 2007;282(20):14845–52.PubMedCrossRef
68.
go back to reference Gorczynski RM, Erin N, Zhu F. Serum-derived exosomes from mice with highly metastatic breast cancer transfer increased metastatic capacity to a poorly metastatic tumor. Cancer Med. 2016;5(2):325–36.PubMedPubMedCentralCrossRef Gorczynski RM, Erin N, Zhu F. Serum-derived exosomes from mice with highly metastatic breast cancer transfer increased metastatic capacity to a poorly metastatic tumor. Cancer Med. 2016;5(2):325–36.PubMedPubMedCentralCrossRef
69.
go back to reference Lee JE, Moon PG, Cho YE, Kim YB, Kim IS, Park H, et al. Identification of EDIL3 on extracellular vesicles involved in breast cancer cell invasion. J Proteome. 2016;131:17–28.CrossRef Lee JE, Moon PG, Cho YE, Kim YB, Kim IS, Park H, et al. Identification of EDIL3 on extracellular vesicles involved in breast cancer cell invasion. J Proteome. 2016;131:17–28.CrossRef
70.
go back to reference Tian HM, Liu XH, Han W, Zhao LL, Yuan B, Yuan CJ. Differential expression of filamin A and its clinical significance in breast cancer. Oncol Lett. 2013;6(3):681–6.PubMedPubMedCentralCrossRef Tian HM, Liu XH, Han W, Zhao LL, Yuan B, Yuan CJ. Differential expression of filamin A and its clinical significance in breast cancer. Oncol Lett. 2013;6(3):681–6.PubMedPubMedCentralCrossRef
71.
go back to reference Jiang X, Yue J, Lu H, Campbell N, Yang Q, Lan S, et al. Inhibition of filamin-A reduces cancer metastatic potential. Int J Biol Sci. 2013;9(1):67–77.PubMedCrossRef Jiang X, Yue J, Lu H, Campbell N, Yang Q, Lan S, et al. Inhibition of filamin-A reduces cancer metastatic potential. Int J Biol Sci. 2013;9(1):67–77.PubMedCrossRef
72.
go back to reference O'Brien K, Rani S, Corcoran C, Wallace R, Hughes L, Friel AM, et al. Exosomes from triple-negative breast cancer cells can transfer phenotypic traits representing their cells of origin to secondary cells. Eur J Cancer. 2013;49(8):1845–59.PubMedCrossRef O'Brien K, Rani S, Corcoran C, Wallace R, Hughes L, Friel AM, et al. Exosomes from triple-negative breast cancer cells can transfer phenotypic traits representing their cells of origin to secondary cells. Eur J Cancer. 2013;49(8):1845–59.PubMedCrossRef
73.
74.
go back to reference Azmi AS, Bao B, Sarkar FH. Exosomes in cancer development, metastasis, and drug resistance: A comprehensive review. Cancer Metastasis Rev. 2013;32(3-4):623–42. Azmi AS, Bao B, Sarkar FH. Exosomes in cancer development, metastasis, and drug resistance: A comprehensive review. Cancer Metastasis Rev. 2013;32(3-4):623–42.
75.
go back to reference Samuel P, Fabbri M, Carter DRF. Mechanisms of drug resistance in cancer: the role of extracellular vesicles. Proteomics. 2017;17(23–24):1600375.CrossRef Samuel P, Fabbri M, Carter DRF. Mechanisms of drug resistance in cancer: the role of extracellular vesicles. Proteomics. 2017;17(23–24):1600375.CrossRef
76.
go back to reference Mukhopadhyay P, Chakraborty S, Ponnusamy MP, Lakshmanan I, Jain M, Batra SK. Mucins in the pathogenesis of breast cancer: implications in diagnosis, prognosis and therapy. Biochim Biophys Acta. 2011;1815(2):224–40.PubMedPubMedCentral Mukhopadhyay P, Chakraborty S, Ponnusamy MP, Lakshmanan I, Jain M, Batra SK. Mucins in the pathogenesis of breast cancer: implications in diagnosis, prognosis and therapy. Biochim Biophys Acta. 2011;1815(2):224–40.PubMedPubMedCentral
77.
go back to reference Park SA, Kim MJ, Park SY, Kim JS, Lim W, Nam JS, et al. TIMP-1 mediates TGF-beta-dependent crosstalk between hepatic stellate and cancer cells via FAK signaling. Sci Rep. 2015;5:16492.PubMedPubMedCentralCrossRef Park SA, Kim MJ, Park SY, Kim JS, Lim W, Nam JS, et al. TIMP-1 mediates TGF-beta-dependent crosstalk between hepatic stellate and cancer cells via FAK signaling. Sci Rep. 2015;5:16492.PubMedPubMedCentralCrossRef
79.
go back to reference Cufi S, Vazquez-Martin A, Oliveras-Ferraros C, Martin-Castillo B, Joven J, Menendez JA. Metformin against TGFbeta-induced epithelial-to-mesenchymal transition (EMT): from cancer stem cells to aging-associated fibrosis. Cell Cycle. 2010;9(22):4461–8.PubMedCrossRef Cufi S, Vazquez-Martin A, Oliveras-Ferraros C, Martin-Castillo B, Joven J, Menendez JA. Metformin against TGFbeta-induced epithelial-to-mesenchymal transition (EMT): from cancer stem cells to aging-associated fibrosis. Cell Cycle. 2010;9(22):4461–8.PubMedCrossRef
82.
go back to reference Lakshmanan I, Rachagani S, Hauke R, Krishn SR, Paknikar S, Seshacharyulu P, et al. MUC5AC interactions with integrin beta4 enhances the migration of lung cancer cells through FAK signaling. Oncogene. 2016;35(31):4112–21.PubMedPubMedCentralCrossRef Lakshmanan I, Rachagani S, Hauke R, Krishn SR, Paknikar S, Seshacharyulu P, et al. MUC5AC interactions with integrin beta4 enhances the migration of lung cancer cells through FAK signaling. Oncogene. 2016;35(31):4112–21.PubMedPubMedCentralCrossRef
83.
go back to reference Gao J, McConnell MJ, Yu B, Li J, Balko JM, Black EP, et al. MUC1 is a downstream target of STAT3 and regulates lung cancer cell survival and invasion. Int J Oncol. 2009;35(2):337–45.PubMed Gao J, McConnell MJ, Yu B, Li J, Balko JM, Black EP, et al. MUC1 is a downstream target of STAT3 and regulates lung cancer cell survival and invasion. Int J Oncol. 2009;35(2):337–45.PubMed
85.
go back to reference Thiery JP, Acloque H, Huang RY, Nieto MA. Epithelial-mesenchymal transitions in development and disease. Cell. 2009;139(5):871–90.PubMedCrossRef Thiery JP, Acloque H, Huang RY, Nieto MA. Epithelial-mesenchymal transitions in development and disease. Cell. 2009;139(5):871–90.PubMedCrossRef
87.
go back to reference Mitra SK, Schlaepfer DD. Integrin-regulated FAK-Src signaling in normal and cancer cells, Cuu Opin Cell Biol. 2006;18(5):516–23. Mitra SK, Schlaepfer DD. Integrin-regulated FAK-Src signaling in normal and cancer cells, Cuu Opin Cell Biol. 2006;18(5):516–23.
88.
go back to reference Dunn KB, Heffler M, Golubovskaya VM. Evolving therapies and FAK inhibitors for the treatment of cancer. Anti Cancer Agents Med Chem. 2010;10(10):722–34.CrossRef Dunn KB, Heffler M, Golubovskaya VM. Evolving therapies and FAK inhibitors for the treatment of cancer. Anti Cancer Agents Med Chem. 2010;10(10):722–34.CrossRef
Metadata
Title
Extracellular vesicles from young women’s breast cancer patients drive increased invasion of non-malignant cells via the Focal Adhesion Kinase pathway: a proteomic approach
Authors
Kimberly R. Jordan
Jessica K. Hall
Troy Schedin
Michelle Borakove
Jenny J. Xian
Monika Dzieciatkowska
Traci R. Lyons
Pepper Schedin
Kirk C. Hansen
Virginia F. Borges
Publication date
01-12-2020
Publisher
BioMed Central
Published in
Breast Cancer Research / Issue 1/2020
Electronic ISSN: 1465-542X
DOI
https://doi.org/10.1186/s13058-020-01363-x

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