Hyaluronan production enhances shedding of plasma membrane-derived microvesicles

Experimental Cell Research

Volumn 319, Issue 13, 2013, Pages 2006-2018

  Rilla, Kirsi ^a   Pasonen Seppänen, Sanna ^a   Deen, Ashik J ^a   Koistinen, Ville V T ^a   Wojciechowski, Sara ^a   Oikari, Sanna ^a   Kärnä, Riikka ^a   Bart, Genevieve ^a   Törrönen, Kari ^a   Tammi, Raija H ^a   Tammi, Markku I ^a  

^a UNIVERSITY OF EASTERN FINLAND   (Finland)

Author keywords

Extracellular matrix; Hyaluronan; Hyaluronan synthase; Microvesicle

Indexed keywords

COLLAGEN; HYALURONAN SYNTHASE 3; HYALURONIC ACID DERIVATIVE; UNCLASSIFIED DRUG;

ARTICLE; CARBOHYDRATE SYNTHESIS; CELL CULTURE; CELL ISOLATION; CELL MEMBRANE; CYST; EXTRACELLULAR MATRIX; FLOW CYTOMETRY; HUMAN; HUMAN CELL; MDCK CELL; MELANOMA CELL; MEMBRANE VESICLE; MICROVESICLE; MICROVILLUS; PRIORITY JOURNAL; PURIFICATION; SCANNING ELECTRON MICROSCOPY; SIGNAL TRANSDUCTION; TRANSMISSION ELECTRON MICROSCOPY; ULTRACENTRIFUGATION;

EID: 84879885842     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2013.05.021     Document Type: Article

References (46)

1. Tetta C., Ghigo E., Silengo L., Deregibus M.C., Camussi G. Extracellular vesicles as an emerging mechanism of cell-to-cell communication. Endocrine 2012, 10.1007/s12020-012-9839-0, (Epub ahead of print).
2. Taylor D.D., Gercel-Taylor C. Exosomes/microvesicles: mediators of cancer-associated immunosuppressive microenvironments. Semin. Immunopathol. 2011, 33:441-454.
3. Mincheva-Nilsson L., Baranov V. The role of placental exosomes in reproduction. Am. J. Reprod. Immunol. 2010, 63:520-533.
4. Webber J., Steadman R., Mason M.D., Tabi Z., Clayton A. Cancer exosomes trigger fibroblast to myofibroblast differentiation. Cancer Res. 2010, 70:9621-9630.
5. Camussi G., Deregibus M.C., Bruno S., Cantaluppi V., Biancone L. Exosomes/microvesicles as a mechanism of cell-to-cell communication. Kidney Int. 2010, 78:838-848.
6. Ardoin S.P., Shanahan J.C., Pisetsky D.S. The role of microparticles in inflammation and thrombosis. Scand. J. Immunol. 2007, 66:159-165.
7. Ratajczak J., Miekus K., Kucia M., Zhang J., Reca R., Dvorak P., Ratajczak M.Z. Embryonic stem cell-derived microvesicles reprogram hematopoietic progenitors: evidence for horizontal transfer of mRNA and protein delivery. Leukemia 2006, 20:847-856.
8. van Doormaal F.F., Kleinjan A., Di Nisio M., Buller H.R., Nieuwland R. Cell-derived microvesicles and cancer. Neth. J. Med. 2009, 67:266-273.
9. Iero M., Valenti R., Huber V., Filipazzi P., Parmiani G., Fais S., Rivoltini L. Tumour-released exosomes and their implications in cancer immunity. Cell Death Differ. 2008, 15:80-88.
10. Skog J., Wurdinger T., van Rijn S., Meijer D.H., Gainche L., Sena-Esteves M., Curry W.T., Carter B.S., Krichevsky A.M., Breakefield X.O. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat. Cell Biol. 2008, 10:1470-1476.
11. Kim H.K., Song K.S., Park Y.S., Kang Y.H., Lee Y.J., Lee K.R., Kim H.K., Ryu K.W., Bae J.M., Kim S. Elevated levels of circulating platelet microparticles, VEGF, IL-6 and RANTES in patients with gastric cancer: possible role of a metastasis predictor. Eur. J. Cancer 2003, 39:184-191.
12. Weigel P.H., DeAngelis P.L. Hyaluronan synthases: a decade-plus of novel glycosyltransferases. J. Biol. Chem. 2007, 282:36777-36781.
13. Kultti A., Rilla K., Tiihonen R., Spicer A.P., Tammi R.H., Tammi M.I. Hyaluronan synthesis induces microvillus-like cell surface protrusions. J. Biol. Chem. 2006, 281:15821-15828.
14. Kultti A., Kärnä R., Rilla K., Nurminen P., Koli E., Makkonen K.M., Si J., Tammi M.I., Tammi R.H. Methyl-beta-cyclodextrin suppresses hyaluronan synthesis by down-regulation of hyaluronan synthase 2 through inhibition of akt. J. Biol. Chem. 2010, 285:22901-22910.
15. Rilla K., Siiskonen H., Spicer A.P., Hyttinen J.M., Tammi M.I., Tammi R.H. Plasma membrane residence of hyaluronan synthase is coupled to its enzymatic activity. J. Biol. Chem. 2005, 280:31890-31897.
16. Bernanke D.H., Markwald R.R. Effects of hyaluronic acid on cardiac cushion tissue cells in collagen matrix cultures. Tex. Rep. Biol. Med. 1979, 39:271-285.
17. Bakkers J., Kramer C., Pothof J., Quaedvlieg N.E., Spaink H.P., Hammerschmidt M. Has2 is required upstream of Rac1 to govern dorsal migration of lateral cells during zebrafish gastrulation. Development 2004, 131:525-537.
18. Oliferenko S., Kaverina I., Small J.V., Huber L.A. Hyaluronic acid (HA) binding to CD44 activates Rac1 and induces lamellipodia outgrowth. J. Cell Biol. 2000, 148:1159-1164.
19. Welch D.R., Bisi J.E., Miller B.E., Conaway D., Seftor E.A., Yohem K.H., Gilmore L.B., Seftor R.E., Nakajima M., Hendrix M.J. Characterization of a highly invasive and spontaneously metastatic human malignant melanoma cell line. Int. J. Cancer 1991, 47:227-237.
20. Hjelle J.T., Golinska B.T., Waters D.C., Steidley K.R., McCarroll D.R., Dobbie J.W. Isolation and propagation in vitro of peritoneal mesothelial cells. Perit. Dial. Int. 1989, 9:341-347.
21. Rilla K., Pasonen-Seppänen S., Kärnä R., Karjalainen H.M., Törrönen K., Koistinen V., Tammi M.I., Tammi R.H., Teräväinen T., Manninen A. HAS3-induced accumulation of hyaluronan in 3D MDCK cultures results in mitotic spindle misorientation and disturbed organization of epithelium. Histochem. Cell Biol. 2012, 137:153-164.
22. Siiskonen H., Rilla K., Kärnä R., Bart G., Jing W., Haller M.F., Deangelis P.L., Tammi R.H., Tammi M.I. Hyaluronan in cytosol-microinjection-based probing of its existence and suggested functions. Glycobiology 2013, 23:222-231.
23. Rilla K., Tiihonen R., Kultti A., Tammi M., Tammi R. Pericellular hyaluronan coat visualized in live cells with a fluorescent probe is scaffolded by plasma membrane protrusions. J. Histochem. Cytochem. 2008, 56:901-910.
24. Hiltunen E.L., Anttila M., Kultti A., Ropponen K., Penttinen J., Yliskoski M., Kuronen A.T., Juhola M., Tammi R., Tammi M., Kosma V.M. Elevated hyaluronan concentration without hyaluronidase activation in malignant epithelial ovarian tumors. Cancer Res. 2002, 62:6410-6413.
25. Kubikova I., Konecna H., Sedo O., Zdrahal Z., Rehulka P., Hribkova H., Rehulkova H., Hampl A., Chmelik J., Dvorak P. Proteomic profiling of human embryonic stem cell-derived microvesicles reveals a risk of transfer of proteins of bovine and mouse origin. Cytotherapy 2009, 11:330-340. 1 p following 340.
26. Sarkar A., Mitra S., Mehta S., Raices R., Wewers M.D. Monocyte derived microvesicles deliver a cell death message via encapsulated caspase-1. PLoS One 2009, 4:e7140.
27. O'Brien L.E., Zegers M.M., Mostov K.E. Opinion: building epithelial architecture: insights from three-dimensional culture models. Nat. Rev. Mol. Cell Biol. 2002, 3:531-537.
28. Zegers M.M., O'Brien L.E., Yu W., Datta A., Mostov K.E. Epithelial polarity and tubulogenesis in vitro. Trends Cell Biol. 2003, 13:169-176.
29. Tammi R.H., Passi A.G., Rilla K., Karousou E., Vigetti D., Makkonen K., Tammi M.I. Transcriptional and post-translational regulation of hyaluronan synthesis. FEBS J. 2011.
30. Rilla K., Oikari S., Jokela T.A., Hyttinen J.M., Kärnä R., Tammi R.H., Tammi M.I. Hyaluronan synthase 1 (HAS1) requires higher cellular UDP-GlcNAc concentration than HAS2 and HAS3. J. Biol. Chem. 2013, 288:5973-5983.
31. Rilla K., Pasonen-Seppänen S., Rieppo J., Tammi M., Tammi R. The hyaluronan synthesis inhibitor 4-methylumbelliferone prevents keratinocyte activation and epidermal hyperproliferation induced by epidermal growth factor. J. Invest. Dermatol 2004, 123:708-714.
32. Guo Q., Xia B., Moshiach S., Xu C., Jiang Y., Chen Y., Sun Y., Lahti J.M., Zhang X.A. The microenvironmental determinants for kidney epithelial cyst morphogenesis. Eur. J. Cell Biol. 2008, 87:251-266.
33. Muralidharan-Chari V., Clancy J., Plou C., Romao M., Chavrier P., Raposo G., D'Souza-Schorey C. ARF6-regulated shedding of tumor cell-derived plasma membrane microvesicles. Curr. Biol. 2009, 19:1875-1885.
34. Del Conde I., Shrimpton C.N., Thiagarajan P., Lopez J.A. Tissue-factor-bearing microvesicles arise from lipid rafts and fuse with activated platelets to initiate coagulation. Blood 2005, 106:1604-1611.
35. Nykopp T.K., Rilla K., Sironen R., Tammi M.I., Tammi R.H., Hämäläinen K., Heikkinen A.M., Komulainen M., Kosma V.M., Anttila M. Expression of hyaluronan synthases (HAS1-3) and hyaluronidases (HYAL1-2) in serous ovarian carcinomas: inverse correlation between HYAL1 and hyaluronan content. BMC Cancer 2009, 9:143.
36. Nykopp T.K., Rilla K., Tammi M.I., Tammi R.H., Sironen R., Hämäläinen K., Kosma V.M., Heinonen S., Anttila M. Hyaluronan synthases (HAS1-3) and hyaluronidases (HYAL1-2) in the accumulation of hyaluronan in endometrioid endometrial carcinoma. BMC Cancer 2010, 10:512.
37. Okuda H., Kobayashi A., Xia B., Watabe M., Pai S.K., Hirota S., Xing F., Liu W., Pandey P.R., Fukuda K., Modur V., Ghosh A., Wilber A., Watabe K. Hyaluronan synthase HAS2 promotes tumor progression in bone by stimulating the interaction of breast cancer stem-like cells with macrophages and stromal cells. Cancer Res. 2012, 72:537-547.
38. Escrevente C., Keller S., Altevogt P., Costa J. Interaction and uptake of exosomes by ovarian cancer cells. BMC Cancer 2011, 11:108.
39. Deregibus M.C., Cantaluppi V., Calogero R., Lo Iacono M., Tetta C., Biancone L., Bruno S., Bussolati B., Camussi G. Endothelial progenitor cell derived microvesicles activate an angiogenic program in endothelial cells by a horizontal transfer of mRNA. Blood 2007, 110:2440-2448.
40. Choi K.Y., Jeon E.J., Yoon H.Y., Lee B.S., Na J.H., Min K.H., Kim S.Y., Myung S.J., Lee S., Chen X., Kwon I.C., Choi K., Jeong S.Y., Kim K., Park J.H. Theranostic nanoparticles based on PEGylated hyaluronic acid for the diagnosis, therapy and monitoring of colon cancer. Biomaterials 2012, 33:6186-6193.
41. Gwak S.J., Jung J.K., An S.S., Kim H.J., Oh J.S., Pennant W.A., Lee H.Y., Kong M.H., Kim K.N., Yoon D.H., Ha Y. Chitosan/TPP-hyaluronic acid nanoparticles: a new vehicle for gene delivery to the spinal cord. J. Biomater. Sci. Polym. Ed. 2011, (Epub ahead of print).
42. Dolo V., D'Ascenzo S., Violini S., Pompucci L., Festuccia C., Ginestra A., Vittorelli M.L., Canevari S., Pavan A. Matrix-degrading proteinases are shed in membrane vesicles by ovarian cancer cells in vivo and in vitro. Clin. Exp. Metastasis 1999, 17:131-140.
43. Keller S., Konig A.K., Marme F., Runz S., Wolterink S., Koensgen D., Mustea A., Sehouli J., Altevogt P. Systemic presence and tumor-growth promoting effect of ovarian carcinoma released exosomes. Cancer Lett. 2009, 278:73-81.
44. Al-Nedawi K., Meehan B., Micallef J., Lhotak V., May L., Guha A., Rak J. Intercellular transfer of the oncogenic receptor EGFRvIII by microvesicles derived from tumour cells. Nat. Cell Biol. 2008, 10:619-624.
45. Tammi R.H., Kultti A., Kosma V.M., Pirinen R., Auvinen P., Tammi M.I. Hyaluronan in human tumors: pathobiological and prognostic messages from cell-associated and stromal hyaluronan. Semin. Cancer Biol. 2008, 18:288-295.
46. Price R.D., Myers S., Leigh I.M., Navsaria H.A. The role of hyaluronic acid in wound healing: assessment of clinical evidence. Am. J. Clin. Dermatol. 2005, 6:393-402.