Oncogenic epithelial cell-derived exosomes containing Rac1 and PAK2 induce angiogenesis in recipient endothelial cells

Oncotarget

Volumn 7, Issue 15, 2016, Pages 19709-19722

  Gopal, Shashi K ^a   Greening, David W ^a   Hanssen, Eric G ^b   Zhu, Hong Jian ^c   Simpson, Richard J ^a   Mathias, Rommel A ^a  

^a LA TROBE UNIVERSITY   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Angiogenesis; Epithelial mesenchymal transition; Exosome; Extracellular vesicle; Tumour microenvironment

Indexed keywords

P21 ACTIVATED KINASE 2; RAC1 PROTEIN; RAS PROTEIN; Y BOX BINDING PROTEIN 1; P21 ACTIVATED KINASE;

ANGIOGENESIS; ARTICLE; CELL COMMUNICATION; CELL MOTILITY; CONTROLLED STUDY; EPITHELIUM CELL; EXOSOME; HUMAN; HUMAN CELL; MOLECULAR DYNAMICS; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEOMICS; UMBILICAL VEIN ENDOTHELIAL CELL; ANIMAL; CELL LINE; CELL MOTION; CELL TRANSFORMATION; DOG; ENDOTHELIUM CELL; EPITHELIAL MESENCHYMAL TRANSITION; MDCK CELL LINE; METABOLISM; NEOVASCULARIZATION (PATHOLOGY); PROCEDURES;

ANIMALS; CELL LINE; CELL MOVEMENT; CELL TRANSFORMATION, NEOPLASTIC; DOGS; ENDOTHELIAL CELLS; EPITHELIAL CELLS; EPITHELIAL-MESENCHYMAL TRANSITION; EXOSOMES; HUMANS; MADIN DARBY CANINE KIDNEY CELLS; NEOVASCULARIZATION, PATHOLOGIC; P21-ACTIVATED KINASES; PROTEOMICS; RAC1 GTP-BINDING PROTEIN;

EID: 84964780772     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.7573     Document Type: Article

References (48)

1. Albini A, Sporn MB. The tumour microenvironment as a target for chemoprevention. Nature reviews Cancer. 2007; 7:139-147.
2. Berx G, Raspe E, Christofori G, Thiery JP, Sleeman JP. Pre-EMTing metastasis? Recapitulation of morphogenetic processes in cancer. Clinical & experimental metastasis. 2007; 24:587-597.
3. Jing Y, Han Z, Zhang S, Liu Y, Wei L. Epithelial-Mesenchymal Transition in tumor microenvironment. Cell & bioscience. 2011; 1:29.
4. Ungefroren H, Sebens S, Seidl D, Lehnert H, Hass R. Interaction of tumor cells with the microenvironment. Cell communication and signaling: CCS. 2011; 9:18.
5. Lamouille S, Xu J, Derynck R. Molecular mechanisms of epithelial-mesenchymal transition. Nature reviews Molecular cell biology. 2014; 15:178-196.
6. Yang J, Weinberg RA. Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Developmental cell. 2008; 14:818-829.
7. Thiery JP. Epithelial-mesenchymal transitions in tumour progression. Nature reviews Cancer. 2002; 2:442-454.
8. Weis SM, Cheresh DA. Tumor angiogenesis: molecular pathways and therapeutic targets. Nature medicine. 2011; 17:1359-1370.
9. Hendrix MJ, Seftor EA, Hess AR, Seftor RE. Vasculogenic mimicry and tumour-cell plasticity: lessons from melanoma. Nature reviews Cancer. 2003; 3:411-421.
10. Psaila B, Lyden D. The metastatic niche: adapting the foreign soil. Nature reviews Cancer. 2009; 9:285-293.
11. Carmeliet P, Jain RK. Molecular mechanisms and clinical applications of angiogenesis. Nature. 2011; 473:298-307.
12. Greening DW, Gopal SK, Mathias RA, Liu L, Sheng J, Zhu HJ, Simpson RJ. Emerging roles of exosomes during epithelial-mesenchymal transition and cancer progression. Seminars in cell & developmental biology. 2015; 40:60-71
13. Kahlert C, Kalluri R. Exosomes in tumor microenvironment influence cancer progression and metastasis. Journal of molecular medicine. 2013; 91:431-437.
14. Mineo M, Garfield SH, Taverna S, Flugy A, De Leo G, Alessandro R, Kohn EC. Exosomes released by K562 chronic myeloid leukemia cells promote angiogenesis in a Src-dependent fashion. Angiogenesis. 2012; 15:33-45.
15. Sheldon H, Heikamp E, Turley H, Dragovic R, Thomas P, Oon CE, Leek R, Edelmann M, Kessler B, Sainson RC, Sargent I, Li JL, Harris AL. New mechanism for Notch signaling to endothelium at a distance by Deltalike 4 incorporation into exosomes. Blood. 2010; 116:2385-2394.
16. Umezu T, Ohyashiki K, Kuroda M, Ohyashiki JH. Leukemia cell to endothelial cell communication via exosomal miRNAs. Oncogene. 2013; 32:2747-2755.
17. Zhang B, Wu X, Zhang X, Sun Y, Yan Y, Shi H, Zhu Y, Wu L, Pan Z, Zhu W, Qian H, Xu W. Human umbilical cord mesenchymal stem cell exosomes enhance angiogenesis through the Wnt4/beta-catenin pathway. Stem cells translational medicine. 2015; 4:513-522.
18. Sharghi-Namini S, Tan E, Ong LL, Ge R, Asada HH. Dll4-containing exosomes induce capillary sprout retraction in a 3D microenvironment. Scientific reports. 2014; 4:4031.
19. Chen YS, Mathias RA, Mathivanan S, Kapp EA, Moritz RL, Zhu HJ, Simpson RJ. Proteomics profiling of Madin-Darby canine kidney plasma membranes reveals Wnt-5a involvement during oncogenic H-Ras/TGF-beta-mediated epithelial-mesenchymal transition. Molecular & cellular proteomics. 2011; 10:M110 001131.
20. Mathias RA, Chen YS, Wang B, Ji H, Kapp EA, Moritz RL, Zhu HJ, Simpson RJ. Extracellular remodelling during oncogenic Ras-induced epithelial-mesenchymal transition facilitates MDCK cell migration. Journal of proteome research. 2010; 9:1007-1019.
21. Mathias RA, Wang B, Ji H, Kapp EA, Moritz RL, Zhu HJ, Simpson RJ. Secretome-based proteomic profiling of Rastransformed MDCK cells reveals extracellular modulators of epithelial-mesenchymal transition. Journal of proteome research. 2009; 8:2827-2837.
22. Tauro BJ, Mathias RA, Greening DW, Gopal SK, Ji H, Kapp EA, Coleman BM, Hill AF, Kusebauch U, Hallows JL, Shteynberg D, Moritz RL, Zhu HJ, et al. Oncogenic H-ras reprograms Madin-Darby canine kidney (MDCK) cell-derived exosomal proteins following epithelialmesenchymal transition. Molecular & cellular proteomics. 2013; 12:2148-2159.
23. Gopal SK, Greening DW, Mathias RA, Ji H, Rai A, Chen M, Zhu HJ, Simpson RJ. YBX1/YB-1 induces partial EMT and tumourigenicity through secretion of angiogenic factors into the extracellular microenvironment. Oncotarget. 2015; 6:13718-13730. doi: 10.18632/oncotarget.3764.
24. Ji H, Greening DW, Barnes TW, Lim JW, Tauro BJ, Rai A, Xu R, Adda C, Mathivanan S, Zhao W, Xue Y, Xu T, Zhu HJ, et al. Proteome profiling of exosomes derived from human primary and metastatic colorectal cancer cells reveal differential expression of key metastatic factors and signal transduction components. Proteomics. 2013; 13:1672-1686.
25. Licciulli S, Maksimoska J, Zhou C, Troutman S, Kota S, Liu Q, Duron S, Campbell D, Chernoff J, Field J, Marmorstein R, Kissil JL. FRAX597, a small molecule inhibitor of the p21-activated kinases, inhibits tumorigenesis of neurofibromatosis type 2 (NF2)-associated Schwannomas. The Journal of biological chemistry. 2013; 288:29105-29114.
26. Murray BW, Guo C, Piraino J, Westwick JK, Zhang C, Lamerdin J, Dagostino E, Knighton D, Loi CM, Zager M, Kraynov E, Popoff I, Christensen JG, et al. Smallmolecule p21-activated kinase inhibitor PF-3758309 is a potent inhibitor of oncogenic signaling and tumor growth. Proceedings of the National Academy of Sciences of the United States of America. 2010; 107:9446-9451.
27. Peinado H, Lavotshkin S, Lyden D. The secreted factors responsible for pre-metastatic niche formation: old sayings and new thoughts. Seminars in cancer biology. 2011; 21:139-146.
28. Soker S, Takashima S, Miao HQ, Neufeld G, Klagsbrun M. Neuropilin-1 is expressed by endothelial and tumor cells as an isoform-specific receptor for vascular endothelial growth factor. Cell. 1998; 92:735-745.
29. Maden CH, Gomes J, Schwarz Q, Davidson K, Tinker A, Ruhrberg C. NRP1 and NRP2 cooperate to regulate gangliogenesis, axon guidance and target innervation in the sympathetic nervous system. Developmental biology. 2012; 369:277-285.
30. Rollin S, Lemieux C, Maliba R, Favier J, Villeneuve LR, Allen BG, Soker S, Bazan NG, Merhi Y, Sirois MG. VEGF-mediated endothelial P-selectin translocation: role of VEGF receptors and endogenous PAF synthesis. Blood. 2004; 103:3789-3797.
31. Bernatchez PN, Rollin S, Soker S, Sirois MG. Relative effects of VEGF-A and VEGF-C on endothelial cell proliferation, migration and PAF synthesis: Role of neuropilin-1. Journal of cellular biochemistry. 2002; 85:629-639.
32. Favier B, Alam A, Barron P, Bonnin J, Laboudie P, Fons P, Mandron M, Herault JP, Neufeld G, Savi P, Herbert JM, Bono F. Neuropilin-2 interacts with VEGFR-2 and VEGFR-3 and promotes human endothelial cell survival and migration. Blood. 2006; 108:1243-1250.
33. Olsson AK, Dimberg A, Kreuger J, Claesson-Welsh L. VEGF receptor signalling-in control of vascular function. Nature reviews Molecular cell biology. 2006; 7:359-371.
34. Fryer BH, Field J. Rho, Rac, Pak and angiogenesis: old roles and newly identified responsibilities in endothelial cells. Cancer letters. 2005; 229:13-23.
35. Bayless KJ, Davis GE. The Cdc42 and Rac1 GTPases are required for capillary lumen formation in three-dimensional extracellular matrices. Journal of cell science. 2002; 115:1123-1136.
36. Koh W, Mahan RD, Davis GE. Cdc42-and Rac1-mediated endothelial lumen formation requires Pak2, Pak4 and Par3, and PKC-dependent signaling. Journal of cell science. 2008; 121:989-1001.
37. Radu M, Lyle K, Hoeflich KP, Villamar-Cruz O, Koeppen H, Chernoff J. p21-Activated Kinase 2 Regulates Endothelial Development and Function through the Bmk1/Erk5 Pathway. Molecular and cellular biology. 2015; 35:3990-4005.
38. Greening DW, Xu R, Ji H, Tauro BJ, Simpson RJ. A protocol for exosome isolation and characterization: evaluation of ultracentrifugation, density-gradient separation, and immunoaffinity capture methods. Methods in molecular biology. 2015; 1295:179-209.
39. Xu R, Greening DW, Rai A, Ji H, Simpson RJ. Highlypurified exosomes and shed microvesicles isolated from the human colon cancer cell line LIM1863 by sequential centrifugal ultrafiltration are biochemically and functionally distinct. Methods. 2015; 87:11-25.
40. Tauro BJ, Greening DW, Mathias RA, Ji H, Mathivanan S, Scott AM, Simpson RJ. Comparison of ultracentrifugation, density gradient separation, and immunoaffinity capture methods for isolating human colon cancer cell line LIM1863-derived exosomes. Methods. 2012; 56:293-304.
41. Sokolova V, Ludwig AK, Hornung S, Rotan O, Horn PA, Epple M, Giebel B. Characterisation of exosomes derived from human cells by nanoparticle tracking analysis and scanning electron microscopy. Colloids and surfaces B, Biointerfaces. 2011; 87:146-150.
42. Williams TF, Mirando AC, Wilkinson B, Francklyn CS, Lounsbury KM. Secreted Threonyl-tRNA synthetase stimulates endothelial cell migration and angiogenesis. Scientific reports. 2013; 3:1317.
43. Kaafarani I, Fernandez-Sauze S, Berenguer C, Chinot O, Delfino C, Dussert C, Metellus P, Boudouresque F, Mabrouk K, Grisoli F, Figarella-Branger D, Martin PM, Ouafik L. Targeting adrenomedullin receptors with systemic delivery of neutralizing antibodies inhibits tumor angiogenesis and suppresses growth of human tumor xenografts in mice. FASEB journal. 2009; 23:3424-3435.
44. Cox J, Mann M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nature biotechnology. 2008; 26:1367-1372.
45. Cox J, Matic I, Hilger M, Nagaraj N, Selbach M, Olsen JV, Mann M. A practical guide to the MaxQuant computational platform for SILAC-based quantitative proteomics. Nature protocols. 2009; 4:698-705.
46. Cox J, Neuhauser N, Michalski A, Scheltema RA, Olsen JV, Mann M. Andromeda: a peptide search engine integrated into the MaxQuant environment. Journal of proteome research. 2011; 10:1794-1805.
47. Luber CA, Cox J, Lauterbach H, Fancke B, Selbach M, Tschopp J, Akira S, Wiegand M, Hochrein H, O'Keeffe M, Mann M. Quantitative proteomics reveals subset-specific viral recognition in dendritic cells. Immunity. 2010; 32:279-289.
48. Takano A, Ishikawa N, Nishino R, Masuda K, Yasui W, Inai K, Nishimura H, Ito H, Nakayama H, Miyagi Y, Tsuchiya E, Kohno N, Nakamura Y, et al. Identification of nectin-4 oncoprotein as a diagnostic and therapeutic target for lung cancer. Cancer research. 2009; 69:6694-6703.