CD44 regulation of endothelial cell proliferation and apoptosis via modulation of CD31 and VE-cadherin expression

Journal of Biological Chemistry

Volumn 289, Issue 9, 2014, Pages 5357-5370

  Tsuneki, Masayuki ^a   Madri, Joseph A ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE ACTIVATION; MATRIX METALLOPROTEINASES; MICROVASCULAR ENDOTHELIAL CELLS; NUCLEAR LOCALIZATION; PATHOPHYSIOLOGICAL; PROLIFERATION AND APOPTOSIS; SIGNALING PATHWAYS; VASCULAR FUNCTIONS;

BIOLOGICAL MEMBRANES; CELL ADHESION; CELL DEATH; CELL PROLIFERATION; CHEMICAL ACTIVATION; GLYCOPROTEINS; MODULATION; PIGMENTS;

ENDOTHELIAL CELLS;

CD31 ANTIGEN; CELL ADHESION MOLECULE; CELL PROTEIN; EFFECTOR CASPASE; HERMES ANTIGEN; INITIATOR CASPASE; MATRIX METALLOPROTEINASE; PROTEIN YAP; SURVIVIN; UNCLASSIFIED DRUG; VASCULAR ENDOTHELIAL CADHERIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DENSITY; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; MICROVASCULAR ENDOTHELIAL CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

APOPTOSIS; CASPASE; CD31; CD44; CELL PROLIFERATION; ENDOTHELIAL CELL; SURVIVIN; VASCULAR BIOLOGY; WESTERN BLOTTING;

ANIMALS; ANTIGENS, CD; ANTIGENS, CD31; ANTIGENS, CD44; APOPTOSIS; CADHERINS; CELL ADHESION; CELL PROLIFERATION; CELLS, CULTURED; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION; INHIBITOR OF APOPTOSIS PROTEINS; MICE; MICE, KNOCKOUT; PROTEIN STRUCTURE, TERTIARY; PROTEIN-SERINE-THREONINE KINASES; REPRESSOR PROTEINS;

EID: 84896832536     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.529313     Document Type: Article

References (76)

1. Hiraga, T., Ito, S., and Nakamura, H. (2013) Cancer stem-like cell marker CD44 promotes bone metastases by enhancing tumorigenicity, cell motility, and hyaluronan production. Cancer Res. 73, 4112-4122
2. Tsuneki, M., Yamazaki, M., Maruyama, S., Cheng, J., and Saku, T. (2013) Podoplanin-mediated cell adhesion through extracellular matrix in oral squamous cell carcinoma. Lab. Invest. 93, 921-932
3. Kirschner, N., Haftek, M., Niessen, C. M., Behne, M. J., Furuse, M., Moll, I., and Brandner, J. M. (2011) CD44 regulates tight-junction assembly and barrier function. J. Invest. Dermatol. 131, 932-943
4. Cichy, J., and Puré, E. (2003) The liberation of CD44. J. Cell Biol. 161, 839-843 (Pubitemid 36718417)
5. Ladeda, V., Aguirre Ghiso, J. A., and Bal de Kier Joffé, E. (1998) Function and expression of CD44 during spreading, migration, and invasion of murine carcinoma cells. Exp. Cell Res. 242, 515-527 (Pubitemid 28359833)
6. Mellor, L., Knudson, C. B., Hida, D., Askew, E. B., and Knudson, W. (2013) Intracellular domain fragment of CD44 alters CD44 function in chondrocytes. J. Biol. Chem. 288, 25838-25850
7. Nagano, O., and Saya, H. (2004) Mechanism and biological significance of CD44 cleavage. Cancer Sci. 95, 930-935 (Pubitemid 40089583)
8. Chetty, C., Vanamala, S. K., Gondi, C. S., Dinh, D. H., Gujrati, M., and Rao, J. S. (2012) MMP-9 induces CD44 cleavage and CD44 mediated cell migration in glioblastoma xenograft cells. Cell. Signal. 24, 549-559
9. Seiki, M. (2002) The cell surface. The stage for matrix metalloproteinase regulation of migration. Curr. Opin. Cell Biol. 14, 624-632
10. Twarock, S., Tammi, M. I., Savani, R. C., and Fischer, J. W. (2010) Hyaluronan stabilizes focal adhesions, filopodia, and the proliferative phenotype in esophageal squamous carcinoma cells. J. Biol. Chem. 285, 23276-23284
11. Suwan, K., Choocheep, K., Hatano, S., Kongtawelert, P., Kimata, K., and Watanabe, H. (2009) Versican/PG-M assembles hyaluronan into extracellular matrix and inhibits CD44-mediated signaling toward premature senescence in embryonic fibroblasts. J. Biol. Chem. 284, 8596-8604
12. Bourguignon, L. Y., Peyrollier, K., Xia, W., and Gilad, E. (2008) Hyaluronan-CD44 interaction activates stem cell marker Nanog, Stat-3-mediated MDR1 gene expression, and ankyrin-regulated multidrug efflux in breast and ovarian tumor cells. J. Biol. Chem. 283, 17635-17651
13. Hertweck, M. K., Erdfelder, F., and Kreuzer, K. A. (2011) CD44 in hematological neoplasias. Ann. Hematol. 90, 493-508
14. Perez, A., Neskey, D. M., Wen, J., Pereira, L., Reategui, E. P., Goodwin, W. J., Carraway, K. L., and Franzmann, E. J. (2013) CD44 interacts with EGFR and promotes head and neck squamous cell carcinoma initiation and progression. Oral Oncol. 49, 306-313
15. Bourguignon, L. Y., Xia, W., and Wong, G. (2009) Hyaluronan-mediated CD44 interaction with p300 and SIRT1 regulates β-catenin signaling and NFκB-specific transcription activity leading to MDR1 and Bcl-xL gene expression and chemoresistance in breast tumor cells. J. Biol. Chem. 284, 2657-2671
16. Stamenkovic, I., and Yu, Q. (2010) Merlin, a "magic" linker between extracellular cues and intracellular signaling pathways that regulate cell motility, proliferation, and survival. Curr. Protein Pept. Sci. 11, 471-484
17. Singleton, P. A., Salgia, R., Moreno-Vinasco, L., Moitra, J., Sammani, S., Mirzapoiazova, T., and Garcia, J. G. (2007) CD44 regulates hepatocyte growth factor-mediated vascular integrity. Role of c-Met, Tiam1/Rac1, dynamin 2, and cortactin. J. Biol. Chem. 282, 30643-30657 (Pubitemid 350035212)
18. Singleton, P. A., Dudek, S. M., Ma, S. F., and Garcia, J. G. (2006) Transactivation of sphingosine 1-phosphate receptors is essential for vascular barrier regulation. Novel role for hyaluronan and CD44 receptor family. J. Biol. Chem. 281, 34381-34393 (Pubitemid 46036646)
19. Savani, R. C., Cao, G., Pooler, P. M., Zaman, A., Zhou, Z., and DeLisser, H. M. (2001) Differential involvement of the hyaluronan (HA) receptors CD44 and receptor for HA-mediated motility in endothelial cell function and angiogenesis. J. Biol. Chem. 276, 36770-36778
20. Flynn, K. M., Michaud, M., and Madri, J. A. (2013) CD44 deficiency contributes to enhanced experimental autoimmune encephalomyelitis.Arole in immune cells and vascular cells of the blood-brain barrier. Am. J. Pathol. 182, 1322-1336
21. Guan, H., Nagarkatti, P. S., and Nagarkatti, M. (2011) CD44 Reciprocally regulates the differentiation of encephalitogenic Th1/Th17 and Th2/regulatory T cells through epigenetic modulation involving DNA methylation of cytokine gene promoters, thereby controlling the development of experimental autoimmune encephalomyelitis. J. Immunol. 186, 6955-6964
22. Flynn, K. M., Michaud, M., Canosa, S., and Madri, J. A. (2013) CD44 regulates vascular endothelial barrier integrity via a PECAM-1 dependent mechanism. Angiogenesis 16, 689-705
23. Ilan, N., Mohsenin, A., Cheung, L., and Madri, J. A. (2001) PECAM-1 shedding during apoptosis generates a membrane-anchored truncated molecule with unique signaling characteristics. FASEB J. 15, 362-372 (Pubitemid 32141428)
24. Ilan, N., Mahooti, S., Rimm, D. L., and Madri, J. A. (1999) PECAM-1 (CD31) functions as a reservoir for and a modulator of tyrosine-phosphorylated β-catenin. J. Cell Sci. 112, 3005-3014 (Pubitemid 29465719)
25. Biswas, P., Zhang, J., Schoenfeld, J. D., Schoenfeld, D., Gratzinger, D., Canosa, S., and Madri, J. A. (2005) Identification of the regions of PECAM-1 involved in β- and γ-catenin associations. Biochem. Biophys. Res. Commun. 329, 1225-1233 (Pubitemid 40575641)
26. Zhang, J. J., Kelm, R. J., Biswas, P., Kashgarian, M., and Madri, J. A. (2007) PECAM-1 modulates thrombin-induced tissue factor expression on endothelial cells. J. Cell Physiol. 210, 527-537 (Pubitemid 44970427)
27. Biswas, P., Canosa, S., Schoenfeld, D., Schoenfeld, J., Li, P., Cheas, L. C., Zhang, J., Cordova, A., Sumpio, B., and Madri, J. A. (2006) PECAM-1 affects GSK-3β-mediated β-catenin phosphorylation and degradation. Am. J. Pathol. 169, 314-324
28. Gratzinger, D., Canosa, S., Engelhardt, B., and Madri, J. A. (2003) Platelet endothelial cell adhesion molecule-1 modulates endothelial cell motility through the small G-protein Rho. FASEB J. 17, 1458-1469 (Pubitemid 36935661)
29. Biswas, P., Canosa, S., Schoenfeld, J., Schoenfeld, D., Tucker, A., and Madri, J. A. (2003) PECAM-1 promotes β-catenin accumulation and stimulates endothelial cell proliferation. Biochem. Biophys. Res. Commun. 303, 212-218 (Pubitemid 36342277)
30. Graesser, D., Solowiej, A., Bruckner, M., Osterweil, E., Juedes, A., Davis, S., Ruddle, N. H., Engelhardt, B., and Madri, J. A. (2002) Altered vascular permeability and early onset of experimental autoimmune encephalomyelitis in PECAM-1-deficient mice. J. Clin. Invest. 109, 383-392 (Pubitemid 34141812)
31. Pinter, E., Barreuther, M., Lu, T., Imhof, B. A., and Madri, J. A. (1997) Platelet-endothelial cell adhesion molecule-1 (PECAM-1/CD31) tyrosine phosphorylation state changes during vasculogenesis in the murine conceptus. Am. J. Pathol. 150, 1523-1530 (Pubitemid 27193801)
32. Jijiwa, M., Demir, H., Gupta, S., Leung, C., Joshi, K., Orozco, N., Huang, T., Yildiz, V. O., Shibahara, I., de Jesus, J. A., Yong, W. H., Mischel, P. S., Fernandez, S., Kornblum, H. I., and Nakano, I. (2011) CD44v6 regulates growth of brain tumor stem cells partially through the AKT-mediated pathway. PLoS One 6, e24217
33. Feng, Y., Zou, Z., Gao, L., Zhang, X., Wang, T., Sun, H., Liu, Y., and Chen, X. (2012) Umbilical cord blood-derived stromal cells regulate megakaryocytic proliferation and migration through SDF-1/PECAM-1 pathway. Cell Biochem. Biophys. 64, 5-15
34. Fedorchenko, O., Stiefelhagen, M., Peer-Zada, A. A., Barthel, R., Mayer, P., Eckei, L., Breuer, A., Crispatzu, G., Rosen, N., Landwehr, T., Lilienthal, N., Möllmann, M., Montesinos-Rongen, M., Heukamp, L., Dürig, J., Hallek, M., Fingerle-Rowson, G., and Herling, M. (2013) CD44 regulates the apoptotic response and promotes disease development in chronic lymphocytic leukemia. Blood 121, 4126-4136
35. Rouschop, K. M., Claessen, N., Pals, S. T., Weening, J. J., and Florquin, S. (2006) CD44 disruption prevents degeneration of the capillary network in obstructive nephropathy via reduction of TGF-β1-induced apoptosis. J. Am. Soc. Nephrol. 17, 746-753
36. Hauptschein, R. S., Sloan, K. E., Torella, C., Moezzifard, R., Giel-Moloney, M., Zehetmeier, C., Unger, C., Ilag, L. L., and Jay, D. G. (2005) Functional proteomic screen identifies a modulating role for CD44 in death receptor-mediated apoptosis. Cancer Res. 65, 1887-1896 (Pubitemid 40478617)
37. Qian, H., Xia, L., Ling, P., Waxman, S., and Jing, Y. (2012) CD44 ligation with A3D8 antibody induces apoptosis in acute myeloid leukemia cells through binding to CD44s and clustering lipid rafts. Cancer Biol. Ther. 13, 1276-1283
38. Ghazi-Visser, L., Laman, J. D., Nagel, S., van Meurs, M., van Riel, D., Tzankov, A., Frank, S., Adams, H., Wolk, K., Terracciano, L., Melief, M. J., Sabat, R., and Günthert, U. (2013) CD44 variant isoforms control experimental autoimmune encephalomyelitis by affecting the lifespan of the pathogenic T cells. FASEB J. 27, 3683-3701
39. McKallip, R. J., Fisher, M., Gunthert, U., Szakal, A. K., Nagarkatti, P. S., and Nagarkatti, M. (2005) Role of CD44 and its v7 isoform in staphylococcal enterotoxin B-induced toxic shock. CD44 deficiency on hepatic mononuclear cells leads to reduced activation-induced apoptosis that results in increased liver damage. Infect. Immun. 73, 50-61 (Pubitemid 40041096)
40. McKallip, R. J., Do, Y., Fisher, M. T., Robertson, J. L., Nagarkatti, P. S., and Nagarkatti, M. (2002) Role of CD44 in activation-induced cell death. CD44-deficient mice exhibit enhanced T cell response to conventional and superantigens. Int. Immunol. 14, 1015-1026
41. Morishima, N., Nakanishi, K., Takenouchi, H., Shibata, T., and Yasuhiko, Y. (2002) An endoplasmic reticulum stress-specific caspase cascade in apoptosis. Cytochrome c-independent activation of caspase-9 by caspase-12. J. Biol. Chem. 277, 34287-34294
42. Bao, Y., Hata, Y., Ikeda, M., and Withanage, K. (2011) Mammalian Hippo pathway. From development to cancer and beyond. J. Biochem. 149, 361-379
43. Badouel, C., and McNeill, H. (2011) SnapShot. The hippo signaling pathway. Cell 145, 484-484.e1
44. Xu, Y., Stamenkovic, I., and Yu, Q. (2010) CD44 attenuates activation of the hippo signaling pathway and is a prime therapeutic target for glioblastoma. Cancer Res. 70, 2455-2464
45. Halder, G., and Johnson, R. L. (2011) Hippo signaling. Growth control and beyond. Development 138, 9-22
46. Li, W., Cooper, J., Karajannis, M. A., and Giancotti, F. G. (2012) Merlin. A tumour suppressor with functions at the cell cortex and in the nucleus. EMBO Rep. 13, 204-215
47. Bai, H., Zhang, N., Xu, Y., Chen, Q., Khan, M., Potter, J. J., Nayar, S. K., Cornish, T., Alpini, G., Bronk, S., Pan, D., and Anders, R. A. (2012) Yes-associated protein regulates the hepatic response after bile duct ligation. Hepatology 56, 1097-1107
48. Huang, J. M., Nagatomo, I., Suzuki, E., Mizuno, T., Kumagai, T., Berezov, A., Zhang, H., Karlan, B., Greene, M. I., and Wang, Q. (2013) YAP modifies cancer cell sensitivity to EGFR and survivin inhibitors and is negatively regulated by the non-receptor type protein tyrosine phosphatase 14. Oncogene 32, 2220-2229
49. Fan, R., Kim, N. G., and Gumbiner, B. M. (2013) Regulation of Hippo pathway by mitogenic growth factors via phosphoinositide 3-kinase and phosphoinositide-dependent kinase-1. Proc. Natl. Acad. Sci. U.S.A. 110, 2569-2574
50. Zhao, B., Wei, X., Li, W., Udan, R. S., Yang, Q., Kim, J., Xie, J., Ikenoue, T., Yu, J., Li, L., Zheng, P., Ye, K., Chinnaiyan, A., Halder, G., Lai, Z. C., and Guan, K. L. (2007) Inactivation of YAP oncoprotein by the Hippo pathway is involved in cell contact inhibition and tissue growth control. Genes Dev. 21, 2747-2761 (Pubitemid 350070721)
51. Chan, S. W., Lim, C. J., Chen, L., Chong, Y. F., Huang, C., Song, H., and Hong, W. (2011) The Hippo pathway in biological control and cancer development. J. Cell Physiol. 226, 928-939
52. Ramos, A., and Camargo, F. D. (2012) The Hippo signaling pathway and stem cell biology. Trends Cell Biol. 22, 339-346
53. Campbell, K. N., Wong, J. S., Gupta, R., Asanuma, K., Sudol, M., He, J. C., and Mundel, P. (2013) Yes-associated protein (YAP) promotes cell survival by inhibiting proapoptotic dendrin signaling. J. Biol. Chem. 288, 17057-17062
54. Hong, W., and Guan, K. L. (2012) The YAP and TAZ transcription co-activators. Key downstream effectors of the mammalian Hippo pathway. Semin. Cell Dev. Biol. 23, 785-793
55. Iurlaro, M., Demontis, F., Corada, M., Zanetta, L., Drake, C., Gariboldi, M., Peiro, S., Cano, A., Navarro, P., Cattelino, A., Tognin, S., Marchisio, P. C., and Dejana, E. (2004) VE-cadherin expression and clustering maintain low levels of survivin in endothelial cells. Am. J. Pathol. 165, 181-189 (Pubitemid 38821826)
56. Shin, S., Sung, B. J., Cho, Y. S., Kim, H. J., Ha, N. C., Hwang, J. I., Chung, C. W., Jung, Y. K., and Oh, B. H. (2001) An anti-apoptotic protein human survivin is a direct inhibitor of caspase-3 and -7. Biochemistry 40, 1117-1123 (Pubitemid 32108606)
57. Tamm, I., Wang, Y., Sausville, E., Scudiero, D. A., Vigna, N., Oltersdorf, T., and Reed, J. C. (1998) IAP-family protein survivin inhibits caspase activity and apoptosis induced by Fas (CD95), Bax, caspases, and anticancer drugs. Cancer Res. 58, 5315-5320 (Pubitemid 28551107)
58. Sun, G., and Irvine, K. D. (2013) Ajuba family proteins link JNK to Hippo signaling. Sci. Signal. 6, ra81
59. Das Thakur, M., Feng, Y., Jagannathan, R., Seppa, M. J., Skeath, J. B., and Longmore, G. D. (2010) Ajuba LIM proteins are negative regulators of the Hippo signaling pathway. Curr. Biol. 20, 657-662
60. Trochon, V., Mabilat, C., Bertrand, P., Legrand, Y., Smadja-Joffe, F., Soria, C., Delpech, B., and Lu, H. (1996) Evidence of involvement of CD44 in endothelial cell proliferation, migration and angiogenesis in vitro. Int. J. Cancer 66, 664-668 (Pubitemid 26197930)
61. Cao, G., Savani, R. C., Fehrenbach, M., Lyons, C., Zhang, L., Coukos, G., and Delisser, H. M. (2006) Involvement of endothelial CD44 during in vivo angiogenesis. Am. J. Pathol. 169, 325-336
62. Marhaba, R., and Zöller, M. (2004) CD44 in cancer progression. Adhesion, migration and growth regulation. J. Mol. Histol. 35, 211-231 (Pubitemid 40585308)
63. Cao, G., Fehrenbach, M. L., Williams, J. T., Finklestein, J. M., Zhu, J. X., and Delisser, H. M. (2009) Angiogenesis in platelet endothelial cell adhesion molecule-1-null mice. Am. J. Pathol. 175, 903-915
64. McClatchey, A. I., and Yap, A. S. (2012) Contact inhibition (of proliferation) redux. Curr. Opin. Cell Biol. 24, 685-694
65. Winkler, C. W., Foster, S. C., Matsumoto, S. G., Preston, M. A., Xing, R., Bebo, B. F., Banine, F., Berny-Lang, M. A., Itakura, A., McCarty, O. J., and Sherman, L. S. (2012) Hyaluronan anchored to activated CD44 on central nervous system vascular endothelial cells promotes lymphocyte extravasation in experimental autoimmune encephalomyelitis. J. Biol. Chem. 287, 33237-33251
66. Enciso, J. M., Gratzinger, D., Camenisch, T. D., Canosa, S., Pinter, E., and Madri, J. A. (2003) Elevated glucose inhibits VEGF-A-mediated endocardial cushion formation. Modulation by PECAM-1 and MMP-2. J. Cell Biol. 160, 605-615 (Pubitemid 36254398)
67. Ilan, N., Cheung, L., Miller, S., Mohsenin, A., Tucker, A., and Madri, J. A. (2001) Pecam-1 is a modulator of stat family member phosphorylation and localization. Lessons from a transgenic mouse. Dev. Biol. 232, 219-232 (Pubitemid 32250956)
68. Ilan, N., and Madri, J. A. (2003) PECAM-1. Old friend, new partners. Curr. Opin. Cell Biol. 15, 515-524 (Pubitemid 37176959)
69. Carrithers, M., Tandon, S., Canosa, S., Michaud, M., Graesser, D., and Madri, J. A. (2005) Enhanced susceptibility to endotoxic shock and impaired STAT3 signaling in CD31-deficient mice. Am. J. Pathol. 166, 185-196 (Pubitemid 40051671)
70. Zhang, L. S., Ma, H. W., Greyner, H. J., Zuo, W., and Mummert, M. E. (2010) Inhibition of cell proliferation by CD44. Akt is inactivated and EGR-1 is down-regulated. Cell Prolif. 43, 385-395
71. Riedl, S. J., and Shi, Y. (2004) Molecular mechanisms of caspase regulation during apoptosis. Nat. Rev. Mol. Cell Biol. 5, 897-907 (Pubitemid 39486541)
72. Boatright, K. M., and Salvesen, G. S. (2003) Mechanisms of caspase activation. Curr. Opin. Cell Biol. 15, 725-731 (Pubitemid 37492933)
73. Allan, L. A., and Clarke, P. R. (2009) Apoptosis and autophagy. Regulation of caspase-9 by phosphorylation. FEBS J. 276, 6063-6073
74. Sah, N. K., Khan, Z., Khan, G. J., and Bisen, P. S. (2006) Structural, functional and therapeutic biology of survivin. Cancer Lett. 244, 164-171 (Pubitemid 44485888)
75. Ilan, N., Cheung, L., Pinter, E., and Madri, J. A. (2000) Platelet-endothelial cell adhesion molecule-1 (CD31), a scaffolding molecule for selected catenin family members whose binding is mediated by different tyrosine and serine/threonine phosphorylation. J. Biol. Chem. 275, 21435-21443 (Pubitemid 30481846)
76. Wu, J., and Sheibani, N. (2003) Modulation of VE-cadherin and PECAM-1 mediated cell-cell adhesions by mitogen-activated protein kinases. J. Cell Biochem. 90, 121-137