Podoplanin associates with cd44 to promote directional cell migration

Molecular Biology of the Cell

Volumn 21, Issue 24, 2010, Pages 4387-4399

  Martín Villar, Ester ^a   Fernández Munoz, Beatriz ^b,d   Parsons, Maddy ^a   Yurrita, Maria M ^b   Megías, Diego ^c   Pérez Gómez, Eduardo ^b   Jones, Gareth E ^a   Quintanilla, Miguel ^b  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^c Centro Nacional de Investigaciones Oncológicas   (Spain)

^d CENTRO DE BIOLOGÍA MOLECULAR SEVERO OCHOA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; CD44 ANTIBODY; HERMES ANTIGEN; HYALURONIC ACID; PODOPLANIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CARCINOMA CELL; CELL MEMBRANE; CELL MIGRATION; CELL MOTILITY; CELL SURFACE; CONTROLLED STUDY; CROSS LINKING; EPITHELIAL MESENCHYMAL TRANSITION; EPITHELIUM CELL; FLUORESCENCE LIFETIME IMAGING MICROSCOPY; FLUORESCENCE RESONANCE ENERGY TRANSFER; IMMUNOPRECIPITATION; IN VIVO STUDY; MICROSCOPY; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SKIN CARCINOGENESIS; SQUAMOUS CELL CARCINOMA; UPREGULATION;

ANIMALS; ANTIGENS, CD44; CARCINOMA, SQUAMOUS CELL; CELL ADHESION; CELL MOVEMENT; CELLS, CULTURED; EPITHELIAL-MESENCHYMAL TRANSITION; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMANS; HYALURONIC ACID; MEMBRANE GLYCOPROTEINS; MICE; MICROSCOPY, FLUORESCENCE; NEOPLASM INVASIVENESS; PROTEIN ISOFORMS; SKIN NEOPLASMS; UP-REGULATION;

EID: 78650452381     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E10-06-0489     Document Type: Article

References (51)

1. Akhurst, R. J., and Balmain, A. (1999). Genetic events and the role of TGF beta in epithelial tumour progression. J. Pathol. 187, 82-90.
2. Allen, W. E., Zicha, D., Ridley, A. J., and Jones, G. E. (1998). A role for Cdc42 in macrophage chemotaxis. J. Cell Biol. 141, 1147-1157.
3. Atsumi, N., Ishii, G., Kojima, M., Sanada, M., Fujii, S., and Ochiai, A. (2008). Podoplanin, a novel marker of tumor-initiating cells in human squamous cell carcinoma A431. Biochem. Biophys. Res. Commun. 373, 36-41.
4. Burns, P. A., Kemp, C. J., Gannon, J. V., Lane, D. P., Bremner, R., and Balmain, A. (1991). Loss of heterozygosity and mutational alterations of the p53 gene in skin tumours of interspecific hybrid mice. Oncogene 6, 2363-2369.
5. Camp, R. L., Kraus, T. A., and Pure, E. (1991). Variations in the cytoskeletal interaction and posttranslational modification of the CD44 homing receptor in macrophages. J. Cell Biol. 115, 1283-1292.
6. Chuang, W. Y., Yeh, C. J., Wu, Y. C., Chao, Y. K., Liu, Y. H., Tseng, C. K., Chang, H. K., Liu, H. P., and Hsueh, C. (2009). Tumor cell expression of podoplanin correlates with nodal metastasis in esophageal squamous cell carcinoma. Histol. Histopathol. 24, 1021-1027.
7. Clark, K., Pankov, R., Travis, M. A., Askari, J. A., Mould, A. P., Craig, S. E., Newham, P., Yamada, K. M., and Humphries, M. J. (2005). A specific alpha5beta1-integrin conformation promotes directional integrin translocation and fibronectin matrix formation. J. Cell Sci. 118, 291-300.
8. Colone, M., Calcabrini, A., Toccacieli, L., Bozzuto, G., Stringaro, A., Gentile, M., Cianfriglia, M., Ciervo, A., Caraglia, M., Budillon, A., Meo, G., Arancia, G., and Molinari, A. (2008). The multidrug transporter P-glycoprotein: A mediator of melanoma invasion? J. Invest. Dermatol. 128, 957-971.
9. Cueni, L.N., Chen, L., Zhang, H., Marino, D., Huggenberger, R., Alitalo, A., Bianchi, R., and Detmar, M. (2010). Podoplanin-Fc reduces lymphatic vessel formation in vitro and in vivo and causes disseminated intravascular coagulation when transgenically expressed in the skin. Blood. In press.
10. Cueni, L. N., and Detmar, M. (2009). Galectin-8 interacts with podoplanin and modulates lymphatic endothelial cell functions. Exp. Cell Res. 315, 1715-1723.
11. del Pozo, M. A., Alderson, N. B., Kiosses, W. B., Chiang, H. H., Anderson, R. G., and Schwartz, M. A. (2004). Integrins regulate Rac targeting by internalization of membrane domains. Science 303, 839-842.
12. Elbashir, S. M., Harborth, J., Lendeckel, W., Yalcin, A., Weber, K., and Tuschl, T. (2001). Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411, 494-498.
13. Friedl, P., and Wolf, K. (2003). Tumour-cell invasion and migration: Diversity and escape mechanisms. Nat. Rev. Cancer 3, 362-374.
14. Gandarillas, A., Scholl, F. G., Benito, N., Gamallo, C., and Quintanilla, M. (1997). Induction of PA2.26, a cell-surface antigen expressed by active fibroblasts, in mouse epidermal keratinocytes during carcinogenesis. Mol. Carcinog. 20, 10-18.
15. Hathcock, K. S., Hirano, H., Murakami, S., and Hodes, R. J. (1993). CD44 expression on activated B cells. Differential capacity for CD44-dependent binding to hyaluronic acid. J. Immunol. 151, 6712-6722.
16. Hirao, M., Sato, N., Kondo, T., Yonemura, S., Monden, M., Sasaki, T., Takai, Y., and Tsukita, S. (1996). Regulation mechanism of ERM (ezrin/radixin/ moesin) protein/plasma membrane association: Possible involvement of phosphatidylinositol turnover and Rho-dependent signaling pathway. J. Cell Biol. 135, 37-51.
17. Hudson, D. L., Speight, P. M., and Watt, F. M. (1996). Altered expression of CD44 isoforms in squamous-cell carcinomas and cell lines derived from them. Int. J. Cancer 66, 457-463.
18. Isacke, C. M., and Yarwood, H. (2002). The hyaluronan receptor, CD44. Int. J. Biochem. Cell Biol. 34, 718-721.
19. Jacobson, K., O'Dell, D., Holifield, B., Murphy, T. L., and August, J. T. (1984). Redistribution of a major cell surface glycoprotein during cell movement. J. Cell Biol. 99, 1613-1623.
20. Kato, Y., Kaneko, M. K., Kunita, A., Ito, H., Kameyama, A., Ogasawara, S., Matsuura, N., Hasegawa, Y., Suzuki-Inoue, K., Inoue, O., Ozaki, Y., and Narimatsu, H. (2008). Molecular analysis of the pathophysiological binding of the platelet aggregation-inducing factor podoplanin to the C-type lectin-like receptor CLEC-2. Cancer Sci. 99, 54-61.
21. Kunita, A., Kashima, T. G., Morishita, Y., Fukayama, M., Kato, Y., Tsuruo, T., and Fujita, N. (2007). The platelet aggregation-inducing factor aggrus/podoplanin promotes pulmonary metastasis. Am. J. Pathol. 170, 1337-1347.
22. Legg, J. W., and Isacke, C. M. (1998). Identification and functional analysis of the ezrin-binding site in the hyaluronan receptor, CD44. Curr. Biol. 8, 705-708.
23. Legg, J. W., Lewis, C. A., Parsons, M., Ng, T., and Isacke, C. M. (2002). A novel PKC-regulated mechanism controls CD44 ezrin association and directional cell motility. Nat. Cell Biol. 4, 399-407.
24. Marhaba, R., and Zoller, M. (2004). CD44 in cancer progression: Adhesion, migration and growth regulation. J. Mol. Histol. 35, 211-231.
25. Martin-Villar, E., Megias, D., Castel, S., Yurrita, M. M., Vilaro, S., and Quintanilla, M. (2006). Podoplanin binds ERM proteins to activate RhoA and promote epithelial-mesenchymal transition. J. Cell Sci. 119, 4541-4553.
26. Martin-Villar, E., Scholl, F. G., Gamallo, C., Yurrita, M. M., Munoz-Guerra, M., Cruces, J., and Quintanilla, M. (2005). Characterization of human PA2.26 antigen (T1alpha-2, podoplanin), a small membrane mucin induced in oral squamous cell carcinomas. Int. J. Cancer 113, 899-910.
27. Miletti-Gonzalez, K. E., Chen, S., Muthukumaran, N., Saglimbeni, G. N., Wu, X., Yang, J., Apolito, K., Shih, W. J., Hait, W. N., and Rodriguez-Rodriguez, L. (2005). The CD44 receptor interacts with P-glycoprotein to promote cell migration and invasion in cancer. Cancer Res. 65, 6660-6667.
28. Nagano, O., and Saya, H. (2004). Mechanism and biological significance of CD44 cleavage. Cancer Sci. 95, 930-935.
29. Nakazawa, Y., Sato, S., Naito, M., Kato, Y., Mishima, K., Arai, H., Tsuruo, T., and Fujita, N. (2008). Tetraspanin family member CD9 inhibits Aggrus/ podoplanin-induced platelet aggregation and suppresses pulmonary metastasis. Blood 112, 1730-1739.
30. Parsons, M., Messent, A. J., Humphries, J. D., Deakin, N. O., and Humphries, M. J. (2008). Quantification of integrin receptor agonism by fluorescence lifetime imaging. J. Cell Sci. 121, 265-271.
31. Peinado, H., Olmeda, D., and Cano, A. (2007). Snail, Zeb and bHLH factors in tumour progression: An alliance against the epithelial phenotype? Nat. Rev. Cancer 7, 415-428.
32. Perez-Gomez, E., Villa-Morales, M., Santos, J., Fernandez-Piqueras, J., Gamallo, C., Dotor, J., Bernabeu, C., and Quintanilla, M. (2007). A role for endoglin as a suppressor of malignancy during mouse skin carcinogenesis. Cancer Res. 67, 10268-10277.
33. Polyak, K., and Weinberg, R. A. (2009). Transitions between epithelial and mesenchymal states: Acquisition of malignant and stem cell traits. Nat. Rev. Cancer 9, 265-273.
34. Ponta, H., Sherman, L., and Herrlich, P. A. (2003). CD 44, from adhesion molecules to signalling regulators. Nat. Rev. Mol. Cell Biol. 4, 33-45.
35. Quintanilla, M., Ramirez, J. R., Perez-Gomez, E., Romero, D., Velasco, B., Letarte, M., Lopez-Novoa, J. M., and Bernabeu, C. (2003). Expression of the TGF-beta coreceptor endoglin in epidermal keratinocytes and its dual role in multistage mouse skin carcinogenesis. Oncogene 22, 5976-5985.
36. Ridley, A. J. (2001). Rho GTPases and cell migration. J. Cell Sci. 114, 2713-2722.
37. Roscic-Mrkic, B., Fischer, M., Leemann, C., Manrique, A., Gordon, C. J., Moore, J. P., Proudfoot, A. E., and Trkola, A. (2003). RANTES (CCL5) uses the proteoglycan CD44 as an auxiliary receptor to mediate cellular activation signals and HIV-1 enhancement. Blood 102, 1169-1177.
38. Scholl, F. G., Gamallo, C., and Quintanilla, M. (2000). Ectopic expression of PA2.26 antigen in epidermal keratinocytes leads to destabilization of adherens junctions and malignant progression. Lab. Invest. 80, 1749-1759.
39. Scholl, F.G., Gamallo, C., Vilaro, S., and Quintanilla, M. (1999). Identification of PA2.26 antigen as a novel cell-surface mucin-type glycoprotein that induces plasma membrane extensions and increased motility in keratinocytes. J. Cell Sci. 112 (Pt 24), 4601-4613.
40. Screaton, G. R., Bell, M. V., Jackson, D. G., Cornelis, F. B., Gerth, U., and Bell, J. I. (1992). Genomic structure of DNA encoding the lymphocyte homing receptor CD44 reveals at least 12 alternatively spliced exons. Proc. Natl. Acad. Sci. USA 89, 12160-12164.
41. Seveau, S., Eddy, R. J., Maxfield, F. R., and Pierini, L. M. (2001). Cytoskeletondependent membrane domain segregation during neutrophil polarization. Mol. Biol. Cell 12, 3550-3562.
42. Shimada, Y., Ishii, G., Nagai, K., Atsumi, N., Fujii, S., Yamada, A., Yamane, Y., Hishida, T., Nishimura, M., Yoshida, J., Ikeda, N., and Ochiai, A. (2009). Expression of podoplanin, CD44, and p63 in squamous cell carcinoma of the lung. Cancer Sci. 100, 2054-2059.
43. Skelton, T. P., Zeng, C., Nocks, A., and Stamenkovic, I. (1998). Glycosylation provides both stimulatory and inhibitory effects on cell surface and soluble CD44 binding to hyaluronan. J. Cell Biol. 140, 431-446.
44. Stoll, C., Baretton, G., Soost, F., Terpe, H. J., Domide, P., and Lohrs, U. (1999). Prognostic importance of the expression of CD44 splice variants in oral squamous cell carcinomas. Oral Oncol. 35, 484-489.
45. Thorne, R. F., Legg, J. W., and Isacke, C. M. (2004). The role of the CD44 transmembrane and cytoplasmic domains in co-ordinating adhesive and signalling events. J. Cell Sci. 117, 373-380.
46. Tzircotis, G., Thorne, R. F., and Isacke, C. M. (2005). Chemotaxis towards hyaluronan is dependent on CD44 expression and modulated by cell type variation in CD44-hyaluronan binding. J. Cell Sci. 118, 5119-5128.
47. Visvader, J. E., and Lindeman, G. J. (2008). Cancer stem cells in solid tumours: Accumulating evidence and unresolved questions. Nat. Rev. Cancer 8, 755-768.
48. Wicki, A., and Christofori, G. (2007). The potential role of podoplanin in tumour invasion. Br. J. Cancer 96, 1-5.
49. Wicki, A., Lehembre, F., Wick, N., Hantusch, B., Kerjaschki, D., and Christofori, G. (2006). Tumor invasion in the absence of epithelial-mesenchymal transition: Podoplanin-mediated remodeling of the actin cytoskeleton. Cancer Cell 9, 261-272.
50. Yonemura, S., Hirao, M., Doi, Y., Takahashi, N., Kondo, T., and Tsukita, S. (1998). Ezrin/radixin/moesin (ERM) proteins bind to a positively charged amino acid cluster in the juxta-membrane cytoplasmic domain of CD44, CD43, and ICAM-2. J. Cell Biol. 140, 885-895.
51. Yuan, P., Temam, S., El-Naggar, A., Zhou, X., Liu, D. D., Lee, J. J., and Mao, L. (2006). Overexpression of podoplanin in oral cancer and its association with poor clinical outcome. Cancer 107, 563-569.