Transactivation of the receptor-tyrosine kinase ephrin receptor A2 is required for the low molecular weight hyaluronan-mediated angiogenesis that is implicated in tumor progression

Journal of Biological Chemistry

Volumn 289, Issue 35, 2014, Pages 24043-24058

  Lennon, Frances E ^a   Mirzapoiazova, Tamara ^a   Mambetsariev, Nurbek ^a   Mambetsariev, Bolot ^a   Salgia, Ravi ^a   Singleton, Patrick A ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BLOOD VESSELS; ENDOTHELIAL CELLS; ENZYMES; HYALURONIC ACID; MOLECULAR WEIGHT; SCAFFOLDS (BIOLOGY); TUMORS;

ANGIOGENESIS; ENDOTHELIAL-CELLS; EPHRINS; GROWTH POTENTIAL; HYALURONAN; LOW MOLECULAR WEIGHT; METASTATIC POTENTIAL; RECEPTOR-TYROSINE KINASE; TRANSACTIVATION; TUMOR PROGRESSIONS;

CHEMICAL ACTIVATION;

CD44V ANTIGEN; ENDOTHELIN 1; EPHRIN RECEPTOR A2; EPIDERMAL GROWTH FACTOR RECEPTOR 2; HYALURONIC ACID; LIPOSOME; PDZ PROTEIN; PROTEIN PATJ; PROTEIN TYROSINE KINASE; PROTEINASE ACTIVATED RECEPTOR; RHO GUANINE NUCLEOTIDE EXCHANGE FACTOR; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SCAFFOLD PROTEIN; UNCLASSIFIED DRUG; VASCULOTROPIN; VASCULOTROPIN RECEPTOR; EPHRIN A2;

ALTERNATIVE RNA SPLICING; ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING SITE; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME ACTIVATION; EXTRACELLULAR MATRIX; GENE SILENCING; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOPRECIPITATION; METASTASIS POTENTIAL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TRANSACTIVATION; TUMOR GROWTH; ANIMAL; C57BL MOUSE; CHEMISTRY; DISEASE COURSE; GENETICS; MOLECULAR WEIGHT; NEOPLASM; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; TRANSCRIPTION INITIATION; UMBILICAL VEIN ENDOTHELIAL CELL;

ANIMALS; DISEASE PROGRESSION; EPHRIN-A2; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; HYALURONIC ACID; MICE; MICE, INBRED C57BL; MOLECULAR WEIGHT; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; RECEPTOR PROTEIN-TYROSINE KINASES; TRANSCRIPTIONAL ACTIVATION;

EID: 84906861737     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.554766     Document Type: Article

References (75)

1. Stamenkovic, I., Amiot, M., Pesando, J. M., and Seed, B. (1989) A lymphocyte molecule implicated in lymph node homing is a member of the cartilage link protein family. Cell 56, 1057-1062 (Pubitemid 19091017)
2. Stoolman, L. M. (1989) Adhesion molecules controlling lymphocyte migration. Cell 56, 907-910
3. Puré, E., and Cuff, C. A. (2001) A crucial role for CD44 in inflammation. Trends Mol. Med. 7, 213-221 (Pubitemid 32822893)
4. Morrison, H., Sherman, L. S., Legg, J., Banine, F., Isacke, C., Haipek, C. A., Gutmann, D. H., Ponta, H., and Herrlich, P. (2001) The NF2 tumor suppressor gene product, merlin, mediates contact inhibition of growth through interactions with CD44. Genes Dev. 15, 968-980 (Pubitemid 32323547)
5. Ghatak, S., Misra, S., and Toole, B. P. (2005) Hyaluronan constitutively regulates ErbB2 phosphorylation and signaling complex formation in carcinoma cells. J. Biol. Chem. 280, 8875-8883 (Pubitemid 40409577)
6. Wang, S. J., and Bourguignon, L. Y. (2006) Hyaluronan and the interaction between CD44 and epidermal growth factor receptor in oncogenic signaling and chemotherapy resistance in head and neck cancer. Arch. Otolaryngol. Head Neck Surg. 132, 771-778 (Pubitemid 44086442)
7. Bourguignon, L. Y. (2008) Hyaluronan-mediated CD44 activation of RhoGTPase signaling and cytoskeleton function promotes tumor progression. Semin. Cancer Biol. 18, 251-259
8. 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)
9. Goodison, S., Urquidi, V., and Tarin, D. (1999) CD44 cell adhesion molecules. Mol. Pathol. 52, 189-196 (Pubitemid 29369203)
10. Turley, E. A., Noble, P. W., and Bourguignon, L. Y. (2002) Signaling properties of hyaluronan receptors. J. Biol. Chem. 277, 4589-4592 (Pubitemid 34968484)
11. Toole, B. P. (2004) Hyaluronan: from extracellular glue to pericellular cue. Nat. Rev. Cancer 4, 528-539
12. Nandi, A., Estess, P., and Siegelman, M. H. (2000) Hyaluronan anchoring and regulation on the surface of vascular endothelial cells is mediated through the functionally active form of CD44. J. Biol. Chem. 275, 14939-14948 (Pubitemid 30337210)
13. Cuff, C. A., Kothapalli, D., Azonobi, I., Chun, S., Zhang, Y., Belkin, R., Yeh, C., Secreto, A., Assoian, R. K., Rader, D. J., and Puré, E. (2001) The adhesion receptor CD44 promotes atherosclerosis by mediating inflammatory cell recruitment and vascular cell activation. J. Clin. Investig. 108, 1031-1040 (Pubitemid 32946077)
14. Slevin, M., Krupinski, J., Gaffney, J., Matou, S., West, D., Delisser, H., Savani, R. C., and Kumar, S. (2007) Hyaluronan-mediated angiogenesis in vascular disease: uncoveringRHAMMand CD44 receptor signaling pathways. Matrix Biol. 26, 58-68 (Pubitemid 46091650)
15. Termeer, C., Sleeman, J. P., and Simon, J. C. (2003) Hyaluronan: magic glue for the regulation of the immune response? Trends Immunol. 24, 112-114 (Pubitemid 36263092)
16. Dentener, M. A., Vernooy, J. H., Hendriks, S., and Wouters, E. F. (2005) Enhanced levels of hyaluronan in lungs of patients with COPD: relationship with lung function and local inflammation. Thorax 60, 114-119 (Pubitemid 40222892)
17. Lennon, F. E., and Singleton, P. A. (2011) Role of hyaluronan and hyaluronan-binding proteins in lung pathobiology. Am. J. Physiol. Lung Cell. Mol. Physiol. 301, L137-L147
18. Itano, N., Zhuo, L., and Kimata, K. (2008) Impact of the hyaluronan-rich tumor microenvironment on cancer initiation and progression. Cancer Sci. 99, 1720-1725
19. Sironen, R. K., Tammi, M., Tammi, R., Auvinen, P. K., Anttila, M., and Kosma, V. M. (2011) Hyaluronan in human malignancies. Exp. Cell Res. 317, 383-391
20. Brantley-Sieders, D. M., Fang, W. B., Hwang, Y., Hicks, D., and Chen, J. (2006) Ephrin-A1 facilitates mammary tumor metastasis through an angiogenesis-dependent mechanism mediated by EphA receptor and vascular endothelial growth factor in mice. Cancer Res. 66, 10315-10324 (Pubitemid 44799750)
21. Larson, J., Schomberg, S., Schroeder, W., and Carpenter, T.C. (2008) Endothelial EphA receptor stimulation increases lung vascular permeability. Am. J. Physiol. Lung Cell. Mol. Physiol. 295, L431-L439
22. Pasquale, E. B. (2008) Eph-ephrin bidirectional signaling in physiology and disease. Cell 133, 38-52
23. Wykosky, J., and Debinski, W. (2008) The EphA2 receptor and ephrinA1 ligand in solid tumors: function and therapeutic targeting. Mol. Cancer Res. 6, 1795-1806
24. Pasquale, E. B. (2005) Eph receptor signalling casts a wide net on cell behaviour. Nat. Rev. Mol. Cell Biol. 6, 462-475
25. Gusenbauer, S., Vlaicu, P., and Ullrich, A. (2013)HGFinduces novel EGFR functions involved in resistance formation to tyrosine kinase inhibitors. Oncogene 32, 3846-3856
26. Fang, W. B., Ireton, R. C., Zhuang, G., Takahashi, T., Reynolds, A., and Chen, J. (2008) Overexpression of EPHA2 receptor destabilizes adherens junctions via a RhoA-dependent mechanism. J. Cell Sci. 121, 358-368 (Pubitemid 351356707)
27. Flamme, I., Frölich, T., and Risau, W. (1997) Molecular mechanisms of vasculogenesis and embryonic angiogenesis. J. Cell. Physiol. 173, 206-210 (Pubitemid 27481131)
28. Arnold, F., and West, D. C. (1991) Angiogenesis in wound healing. Pharmacol. Ther. 52, 407-422
29. Shimizu, T., Hoshino, Y., Miyazaki, H., and Sato, E. (2012) Angiogenesis and microvasculature in the female reproductive organs: physiological and pathological implications. Curr. Pharm. Des. 18, 303-309
30. Folkman, J., Szabo, S., Stovroff, M., McNeil, P., Li, W., and Shing, Y. (1991) Duodenal ulcer: discovery of a new mechanism and development of angiogenic therapy that accelerates healing. Ann. Surg. 214, 414-425; discussion 426-417
31. Semerano, L., Clavel, G., Assier, E., Denys, A., and Boissier, M. C. (2011) Blood vessels, a potential therapeutic target in rheumatoid arthritis? Joint Bone Spine 78, 118-123
32. Leong, T. T., Fearon, U., and Veale, D. J. (2005) Angiogenesis in psoriasis and psoriatic arthritis: clues to disease pathogenesis. Curr. Rheumatol. Rep. 7, 325-329
33. Folkman, J. (1974) Tumor angiogensis: role in regulation of tumor growth. Symp. Soc. Dev. Biol. 30, 43-52
34. Hanahan, D., and Folkman, J. (1996) Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell 86, 353-364 (Pubitemid 26272076)
35. Calabro, A., Hascall, V. C., and Midura, R. J. (2000) Adaptation of FACE methodology for microanalysis of total hyaluronan and chondroitin sulfate composition from cartilage. Glycobiology 10, 283-293 (Pubitemid 30145200)
36. Lennon, F. E., Mirzapoiazova, T., Mambetsariev, B., Poroyko, V. A., Salgia, R., Moss, J., and Singleton, P. A. (2014) The μ-opioid receptor promotes opioid and growth factor-induced proliferation, migration, and epithelial mesenchymal transition (EMT) in human lung cancer. PLoS ONE 9, e91577
37. Arnaoutova, I., George, J., Kleinman, H. K., and Benton, G. (2009) The endothelial cell tube formation assay on basement membrane turns 20: state of the science and the art. Angiogenesis 12, 267-274
38. Singleton, P. A., Mirzapoiazova, T., Guo, Y., Sammani, S., Mambetsariev, N., Lennon, F. E., Moreno-Vinasco, L., and Garcia, J. G. (2010) High molecular weight hyaluronan is a novel inhibitor of pulmonary vascular leakiness. Am. J. Physiol. Lung Cell. Mol. Physiol. 299, L639-L651
39. Brandwijk, R. J., Mulder, W. J., Nicolay, K., Mayo, K. H., Thijssen, V. L., and Griffioen, A. W. (2007) Anginex-conjugated liposomes for targeting of angiogenic endothelial cells. Bioconjug. Chem. 18, 785-790 (Pubitemid 47010798)
40. Griffioen, A. W., van der Schaft, D. W., Barendsz-Janson, A. F., Cox, A., Struijker Boudier, H. A., Hillen, H. F., and Mayo, K. H. (2001) Anginex, a designed peptide that inhibits angiogenesis. Biochem. J. 354, 233-242 (Pubitemid 32209858)
41. West, D. C., Hampson, I. N., Arnold, F., and Kumar, S. (1985) Angiogenesis induced by degradation products of hyaluronic acid. Science 228, 1324-1326
42. Deed, R., Rooney, P., Kumar, P., Norton, J. D., Smith, J., Freemont, A. J., and Kumar, S. (1997) Early-response gene signalling is induced by angiogenic oligosaccharides of hyaluronan in endothelial cells. Inhibition by non-angiogenic, high molecular weight hyaluronan. Int. J. Cancer 71, 251-256 (Pubitemid 27252999)
43. Otrock, Z. K., Mahfouz, R. A., Makarem, J. A., and Shamseddine, A. I. (2007) Understanding the biology of angiogenesis: review of the most important molecular mechanisms. Blood Cells Mol. Dis. 39, 212-220 (Pubitemid 47126926)
44. Toole, B. P., Wight, T. N., and Tammi, M. I. (2002) Hyaluronan-cell interactions in cancer and vascular disease. J. Biol. Chem. 277, 4593-4596 (Pubitemid 34968485)
45. Slevin, M., Kumar, S., and Gaffney, J. (2002) Angiogenic oligosaccharides of hyaluronan induce multiple signaling pathways affecting vascular endothelial cell mitogenic and wound healing responses. J. Biol. Chem. 277, 41046-41059 (Pubitemid 35215695)
46. Bourguignon, L. Y., Wong, G., Earle, C., Krueger, K., and Spevak, C. C. (2010) Hyaluronan-CD44 interaction promotes c-Src-mediated twist signaling, microRNA-10b expression, and RhoA/RhoC up-regulation, leading to Rho-kinase-associated cytoskeleton activation and breast tumor cell invasion, J. Biol. Chem. 285, 36721-36735
47. Roskoski, R., Jr. (2005) Src kinase regulation by phosphorylation and dephosphorylation. Biochem. Biophys. Res. Commun. 331, 1-14
48. Hsieh, H. L., Lin, C. C., Chan, H. J., Yang, C. M., and Yang, C. M. (2012) c-Src-dependent EGF receptor transactivation contributes to ET-1-induced COX-2 expression in brain microvascular endothelial cells. J. Neuroinflammation 9, 152
49. Carpenter, T. C., Schroeder, W., Stenmark, K. R., and Schmidt, E. P. (2012) Eph-A2 promotes permeability and inflammatory responses to bleomycin-induced lung injury, Am. J. Respir. Cell Mol Biol. 46, 40-47
50. Fang, W. B., Brantley-Sieders, D. M., Hwang, Y., Ham, A. J., and Chen, J. (2008) Identification and functional analysis of phosphorylated tyrosine residues within EphA2 receptor-tyrosine kinase, J. Biol. Chem. 283, 16017-16026
51. Faoro, L., Singleton, P. A., Cervantes, G. M., Lennon, F. E., Choong, N. W., Kanteti, R., Ferguson, B. D., Husain, A. N., Tretiakova, M. S., Ramnath, N., Vokes, E. E., and Salgia, R. (2010) EphA2 mutation in lung squamous cell carcinoma promotes increased cell survival, cell invasion, focal adhesions, and mammalian target of rapamycin activation. J. Biol. Chem. 285, 18575-18585
52. Krupinski, J., Ethirajan, P., Font, M. A., Turu, M. M., Gaffney, J., Kumar, P., and Slevin, M. (2008) Changes in hyaluronan metabolism and RHAMM receptor expression accompany formation of complicated carotid lesions and may be pro-angiogenic mediators of intimal neovessel growth. Biomark. Insights 2, 361-367
53. Sáinz-Jaspeado, M., Huertas-Martinez, J., Lagares-Tena, L., Martin Liberal, J., Mateo-Lozano, S., de Alava, E., de Torres, C., Mora, J., Del Muro, X. G., and Tirado, O. M. (2013) EphA2-induced angiogenesis in ewing sarcoma cells works through bFGF production and is dependent on caveolin-1, PLoS ONE 8, e71449
54. Ernkvist, M., Luna Persson, N., Audebert, S., Lecine, P., Sinha, I., Liu, M., Schlueter, M., Horowitz, A., Aase, K., Weide, T., Borg, J. P., Majumdar, A., and Holmgren, L. (2009) The Amot/Patj/Syx signaling complex spatially controls RhoA GTPase activity in migrating endothelial cells. Blood 113, 244-253
55. Dings, R. P., Van Laar, E. S., Loren, M., Webber, J., Zhang, Y., Waters, S. J., Macdonald, J. R., and Mayo, K. H. (2010) Inhibiting tumor growth by targeting tumor vasculature with galectin-1 antagonist anginex conjugated to the cytotoxic acylfulvene, 6-hydroxylpropylacylfulvene. Bioconjug. Chem. 21, 20-27
56. Thijssen, V. L, Hulsmans, S., and Griffioen, A. W. (2008) The galectin profile of the endothelium: altered expression and localization in activated and tumor endothelial cells. Am. J. Pathol. 172, 545-553 (Pubitemid 351282039)
57. Hughes, C. S., Postovit, L. M., and Lajoie, G. A. (2010) Matrigel: a complex protein mixture required for optimal growth of cell culture. Proteomics 10, 1886-1890
58. Beauchamp, A., and Debinski, W. (2012) Ephs and ephrins in cancer: ephrin-A1 signalling. Semin. Cell Dev. Biol. 23, 109-115
59. 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)
60. Matou-Nasri, S., Gaffney, J., Kumar, S., and Slevin, M. (2009) Oligosaccharides of hyaluronan induce angiogenesis through distinct CD44- and RHAMM-mediated signalling pathways involving Cdc2 and γ-adducin. Int. J. Oncol. 35, 761-773
61. Cheng, N., Brantley, D. M., Liu, H., Lin, Q., Enriquez, M., Gale, N., Yancopoulos, G., Cerretti, D. P., Daniel, T. O., and Chen, J. (2002) Blockade of EphA receptor-tyrosine kinase activation inhibits vascular endothelial cell growth factor-induced angiogenesis. Mol. Cancer Res. 1, 2-11 (Pubitemid 36330206)
62. Zhou, N., Zhao, W. D., Liu, D. X., Liang, Y., Fang, W. G., Li, B., and Chen, Y. H. (2011) Inactivation of EphA2 promotes tight junction formation and impairs angiogenesis in brain endothelial cells. Microvasc. Res. 82, 113-121
63. Chan, B., and Sukhatme, V. P. (2009) Receptor-tyrosine kinase EphA2 mediates thrombin-induced upregulation of ICAM-1 in endothelial cells in vitro. Thromb. Res. 123, 745-752
64. Shin, K., Wang, Q., and Margolis, B. (2007) PATJ regulates directional migration of mammalian epithelial cells. EMBO Rep. 8, 158-164 (Pubitemid 46420844)
65. Whitehead, I., Kirk, H., and Kay, R. (1995) Retroviral transduction and oncogenic selection of a cDNA encoding Dbs, a homolog of the Dbl guanine nucleotide exchange factor. Oncogene 10, 713-721
66. Yamauchi, J., Hirasawa, A., Miyamoto, Y., Kokubu, H., Nishii, H., Okamoto, M., Sugawara, Y., Tsujimoto, G., and Itoh, H. (2002) Role of Dbl's big sister in the anti-mitogenic pathway from α1B-adrenergic receptor to c-Jun N-terminal kinase. Biochem. Biophys. Res. Commun. 296, 85-92 (Pubitemid 35002059)
67. Kostenko, E. V., Olabisi, O. O., Sahay, S., Rodriguez, P. L., and Whitehead, I. P. (2006) Ccpg1, a novel scaffold protein that regulates the activity of the Rho guanine nucleotide exchange factor Dbs. Mol. Cell. Biol. 26, 8964-8975 (Pubitemid 44851953)
68. Spindler, V., Schlegel, N., and Waschke, J. (2010) Role of GTPases in control of microvascular permeability. Cardiovasc. Res. 87, 243-253
69. Park, D., Kim, Y., Kim, H., Kim, K., Lee, Y. S., Choe, J., Hahn, J. H., Lee, H., Jeon, J., Choi, C., Kim, Y. M., and Jeoung, D. (2012) Hyaluronic acid promotes angiogenesis by inducing RHAMM-TGFβ receptor interaction via CD44-PKCδ. Mol. Cells 33, 563-574
70. Wang, Y. Z., Cao, M. L., Liu, Y. W., He, Y. Q., Yang, C. X., and Gao, F. (2011) CD44 mediates oligosaccharides of hyaluronan-induced proliferation, tube formation, and signal transduction in endothelial cells. Exp. Biol. Med. (Maywood) 236, 84-90
71. Olofsson, B., Porsch, H., and Heldin, P. (2014) Knock-down of CD44 regulates endothelial cell differentiation via NFκB-mediated chemokine production. PLoS ONE 9, e90921
72. Taylor, K. R., Yamasaki, K., Radek, K. A., Di Nardo, A., Goodarzi, H., Golenbock, D., Beutler, B., and Gallo, R. L. (2007) Recognition of hyaluronan released in sterile injury involves a unique receptor complex dependent on Toll-like receptor 4, CD44, and MD-2. J. Biol. Chem. 282, 18265-18275 (Pubitemid 47100227)
73. Taylor, K. R., Trowbridge, J. M., Rudisill, J. A., Termeer, C. C., Simon, J. C., and Gallo, R. L. (2004) Hyaluronan fragments stimulate endothelial recognition of injury through TLR4. J. Biol. Chem. 279, 17079-17084 (Pubitemid 38560463)
74. 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
75. Gao, F., Yang, C. X., Mo, W., Liu, Y. W., and He, Y. Q. (2008) Hyaluronan oligosaccharides are potential stimulators to angiogenesis via RHAMM mediated signal pathway in wound healing. Clin. Invest. Med. 31, E106-E116