Tumor promoting effect of podoplanin-positive fibroblasts is mediated by enhanced RhoA activity

Biochemical and Biophysical Research Communications

Volumn 422, Issue 1, 2012, Pages 194-199

  Ito, Suguru ^a,b   Ishii, Genichiro ^b   Hoshino, Ayuko ^a,b   Hashimoto, Hiroko ^b   Neri, Shinya ^b   Kuwata, Takeshi ^b   Higashi, Morihiro ^c   Nagai, Kanji ^b   Ochiai, Atsushi ^a,b  

^a UNIVERSITY OF TOKYO   (Japan)

^b NATIONAL CANCER CENTER HOSPITAL EAST   (Japan)

^c SAITAMA MEDICAL UNIVERSITY   (Japan)

Author keywords

Fibroblast; Microenvironment; Podoplanin; RhoA

Indexed keywords

PODOPLANIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CANCER CELL CULTURE; CARCINOGENESIS; CELL FUNCTION; CONTROLLED STUDY; FEMALE; FIBROBLAST; HUMAN; HUMAN CELL; LUNG ADENOCARCINOMA; MOUSE; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; TUMOR GROWTH; TUMOR MICROENVIRONMENT; WILD TYPE;

ANIMALS; CELL LINE, TUMOR; CYTOPLASM; DOGS; FIBROBLASTS; HUMANS; MEMBRANE GLYCOPROTEINS; MICE; MUTATION; NEOPLASMS; PROTEIN STRUCTURE, TERTIARY; RHOA GTP-BINDING PROTEIN;

EID: 84861458063     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2012.04.158     Document Type: Article

References (30)

1. Bissell M.J., Radisky D. Putting tumours in context. Nat. Rev. Cancer 2001, 1:46-54.
2. Kalluri R., Zeisberg M. Fibroblasts in cancer. Nat. Rev. Cancer 2006, 6:392-401.
3. Tlsty T.D., Coussens L.M. Tumor stroma and regulation of cancer development. Annu. Rev. Pathol. 2006, 1:119-150.
4. Bremnes R.M., Dønnem T., Al-Saad S., Al-Shibli K., Andersen S., Sirera R., Camps C., Marinez I., Busund L.T. The role of tumor stroma in cancer progression and prognosis: emphasis on carcinoma-associated fibroblasts and non-small cell lung cancer. J. Thorac. Oncol. 2011, 6:209-217.
5. Orimo A., Gupta P.B., Sgroi D.C., Arenzana-Seisdedos F., Delaunay T., Naeem R., Carey V.J., Richardson A.L., Weinberg R.A. Stromal fibroblasts present in invasive human breast carcinomas promote tumor growth and angiogenesis through elevated SDF-1/CXCL12 secretion. Cell 2005, 121:335-348.
6. Pietras K., Pahler J., Bergers G., Hanahan D. Functions of paracrine PDGF signaling in the proangiogenic tumor stroma revealed by pharmacological targeting. PLoS Med. 2008, 5:e19.
7. Goetz J.G., Minguet S., Navarro-Lérida I., Lazcano J.J., Samaniego R., Calvo E., Tello M., Osteso-Ibáñez T., Pellinen T., Echarri A., Cerezo A., Klein-Szanto A.J., Garcia R., Keely P.J., Sánchez-Mateos P., Cukierman E., Del Pozo M.A. Biomechanical remodeling of the microenvironment by stromal caveolin-1 favors tumor invasion and metastasis. Cell 2011, 146:148-163.
8. Gaggioli C., Hooper S., Hidalgo-Carcedo C., Grosse R., Marshall J.F., Harrington K., Sahai E. Fibroblast-led collective invasion of carcinoma cells with differing roles for RhoGTPases in leading and following cells. Nat. Cell Biol. 2007, 12:1392-1400.
9. Kato Y., Fujita N., Kunita A., Sato S., Kaneko M., Osawa M., Tsuruo T. Molecular identification of aggrus/T1alpha as a platelet aggregation-inducing factor expressed in colorectal tumors. J. Biol. Chem. 2003, 278:51599-51605.
10. Kato Y., Kaneko M., Sata M., Fujita N., Tsuruo T., Osawa M. Enhanced expression of aggrus (T1alpha/podoplanin), a platelet-aggregation-inducing factor in lung squamous cell carcinoma. Tumour Biol. 2005, 26:195-200.
11. Kunita A., Kashima T.G., Morishita Y., Fukayama M., Kato Y., Tsuruo T., Fujita N. The platelet aggregation-inducing factor aggrus/podoplanin promotes pulmonary metastasis. Am. J. Pathol. 2007, 170:1337-1347.
12. Suzuki-Inoue K., Kato Y., Inoue O., Kaneko M.K., Mishima K., Yatomi Y., Yamazaki Y., Narimatsu H., Ozaki Y. Involvement of the snake toxin receptor CLEC-2, in podoplanin-mediated platelet activation, by cancer cells. J. Biol. Chem. 2007, 282:25993-26001.
13. Shimada Y., Ishii G., Nagai K., Atsumi N., Fujii S., Yamada A., Yamane Y., Hishida T., Nishimura M., Yoshida J., Ikeda N., Ochiai A. Expression of podoplanin, CD44, and p63 in squamous cell carcinoma of the lung. Cancer Sci. 2009, 100:2054-2059.
14. Martín-Villar E., Fernández-Muñoz B., Parsons M., Yurrita M.M., Megías D., Pérez-Gómez E., Jones G.E., Quintanilla M. Podoplanin associates with CD44 to promote directional cell migration. Mol. Biol. Cell 2010, 21:4387-4399.
15. Martin-Villar E., Megias D., Castel S., Yurrita M.M., Vilaro S., Quintanilla M. Podoplanin binds ERM proteins to activate RhoA and promote epithelial-mesenchymal transition. J. Cell Sci. 2006, 119:4541-4553.
16. Kawase A., Ishii G., Nagai K., Ito T., Nagano T., Murata Y., Hishida T., Nishimura M., Yoshida J., Suzuki K., Ochiai A. Podoplanin expression by cancer associated fibroblasts predicts poor prognosis of lung adenocarcinoma. Int. J. Cancer 2008, 123:1053-1059.
17. Ito M., Ishii G., Nagai K., Maeda R., Nakano Y., Ochiai A. Prognostic impact of cancer-associated stromal cells in stage I lung adenocarcinoma patients. Chest 2012, (Epub ahead of print).
18. Hoshino A., Ishii G., Ito T., Aoyagi K., Ohtaki Y., Nagai K., Sasaki H., Ochiai A. Podoplanin-positive fibroblasts enhance lung adenocarcinoma tumor formation: podoplanin in fibroblast functions for tumor progression. Cancer Res. 2011, 71:4769-4779.
19. Hoshino A., Chiba H., Nagai K., Ishii G., Ochiai A. Human vascular adventitial fibroblasts contain mesenchymal stem/progenitor cells. Biochem. Biophys. Res. Commun. 2008, 368:305-310.
20. Ishii G., Hashimoto H., Asada K., Ito T., Hoshino A., Fujii S., Kojima M., Kuwata T., Harigaya K., Nagai K., Ushijima T., Ochiai A. Fibroblasts associated with cancer cells keep enhanced migration activity after separation from cancer cells: a novel character of tumor educated fibroblasts. Int. J. Oncol. 2010, 37:317-325.
21. Schoppmann S.F., Berghoff A., Dinhof C., Jakesz R., Gnant M., Dubsky P., Jesch B., Heinzl H., Birner P. Podoplanin-expressing cancer-associated fibroblasts are associated with poor prognosis in invasive breast cancer. Breast Cancer Res. Treat. 2012, (Epub ahead of print).
22. Levental K.R., Yu H., Kass L., Lakins J.N., Egeblad M., Erler J.T., Fong S.F., Csiszar K., Giaccia A., Weninger W., Yamauchi M., Gasser D.L., Weaver V.M. Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 2009, 139(2009):891-906.
23. Friedl P., Gilmour D. Collective cell migration in morphogenesis, regeneration and cancer. Nat. Rev. Mol. Cell Biol. 2009, 10:445-457.
24. Provenzano P.P., Eliceiri K.W., Campbell J.M., Inman D.R., White J.G., Keely P.J. Collagen reorganization at the tumor-stromal interface facilitates local invasion. BMC Med. 2006, 4:38.
25. Takai Y., Sasaki T., Matozaki T. Small GTP-binding proteins. Physiol. Rev. 2001, 81:153-208.
26. Provenzano P.P., Inman D.R., Eliceiri K.W., Trier S.M., Keely P.J. Contact guidance mediated three-dimensional cell migration is regulated by Rho/ROCK-dependent matrix reorganization. Biophys. J. 2008, 95:5374-5384.
27. Goetz J.G., Minguet S., Navarro-Lérida I., Lazcano J.J., Samaniego R., Calvo E., Tello M., Osteso-Ibáñez T., Pellinen T., Echarri A., Cerezo A., Klein-Szanto A.J., Garcia R., Keely P.J., Sánchez-Mateos P., Cukierman E., Del Pozo M.A. Biomechanical remodeling of the microenvironment by stromal caveolin-1 favors tumor invasion and metastasis. Cell 2011, 146:148-163.
28. Mantovani A., Allavena P., Sica A., Balkwill F. Cancer-related inflammation. Nature 2008, 454:436-444.
29. Erez N., Truitt M., Olson P., Arron S.T., Hanahan D. Cancer-associated fibroblasts are activated in incipient neoplasia to orchestrate tumor-promoting inflammation in an NF-kappaB-dependent manner. Cancer Cell 2010, 17:135-147.
30. Chang Y.W., Bean R.R., Jakobi R. Targeting RhoA/Rho kinase and p21-activated kinase signaling to prevent cancer development and progression. Recent Pat. Anticancer Drug Discov. 2009, 4:110-124.