Carcinoma cell hyaluronan as a "portable" cancerized prometastatic microenvironment

Cancer Research

Volumn 76, Issue 9, 2016, Pages 2507-2512

  Turley, Eva A ^a,b   Wood, David K ^c,d   McCarthy, James B ^d,e  

^a LONDON REGIONAL CANCER PROGRAM   (Canada)

^b WESTERN UNIVERSITY   (Canada)

^c University of Minnesota   (United States)

^d UNIVERSITY OF MINNESOTA   (United States)

^e UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; CELL PROTEIN; HERMES ANTIGEN; HYALURONIC ACID; PROTEIN RHAMM; UNCLASSIFIED DRUG;

CARCINOMA CELL; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; CIRCULATING TUMOR CELL; DEGRADATION KINETICS; ENZYME SYNTHESIS; EXTRACELLULAR MATRIX; HUMAN; METASTASIS; PRIMARY TUMOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; TUMOR MICROENVIRONMENT; ANIMAL; CARCINOMA; METABOLISM; PATHOLOGY; PHYSIOLOGY; TUMOR INVASION;

ANIMALS; CARCINOMA; HUMANS; HYALURONIC ACID; NEOPLASM INVASIVENESS; TUMOR MICROENVIRONMENT;

EID: 84969508713     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-15-3114     Document Type: Review

References (62)

1. Karousou E, D'AngeloML, Kouvidi K, Vigetti D, ViolaM, Nikitovic D, et al. Collagen VI and hyaluronan: the common role in breast cancer. Biomed Res Int 2014;2014:606458.
2. Schwertfeger KL, Cowman MK, Telmer PG, Turley EA, McCarthy JB. Hyaluronan, inflammation, and breast cancer progression. Front Immunol 2015;6:236.
3. Slevin M, Krupinski J, Gaffney J, Matou S, West D, Delisser H, et al. Hyaluronan-mediated angiogenesis in vascular disease: uncovering RHAMM and CD44 receptor signaling pathways. Matrix Biol 2007;26: 58-68.
4. Tolg C, McCarthy JB, Yazdani A, Turley EA. Hyaluronan and RHAMM in wound repair and the "cancerization" of stromal tissues. Biomed Res Int 2014;2014:103923.
5. Tammi RH, Passi AG, Rilla K, Karousou E, Vigetti D, Makkonen K, et al. Transcriptional and post-translational regulation of hyaluronan synthesis. FEBS J 2011;278:1419-28.
6. Evanko SP, Tammi MI, Tammi RH, Wight TN. Hyaluronan-dependent pericellular matrix. Adv Drug Deliv Rev 2007;59:1351-65.
7. Kusumoto T, Kodama J, Seki N, Nakamura K, Hongo A, Hiramatsu Y. Clinical significance of syndecan-1 and versican expression in human epithelial ovarian cancer. Oncol Rep 2010;23:917-25.
8. Voutilainen K, Anttila M, Sillanpaa S, Tammi R, Tammi M, Saarikoski S, et al. Versican in epithelial ovarian cancer: relation to hyaluronan, clinicopathologic factors and prognosis. Int J Cancer 2003;107:359-64.
9. Simpson MA, Wilson CM, Furcht LT, Spicer AP, Oegema TRJr, McCarthy JB. Manipulation of hyaluronan synthase expression in prostate adenocarcinoma cells alters pericellular matrix retention and adhesion to bone marrow endothelial cells. J Biol Chem 2002;277: 10050-7.
10. Pasonen-Seppanen S, Hyttinen JM, Rilla K, Jokela T, Noble PW, Tammi M, et al. Role of CD44 in the organization of keratinocyte pericellular hyaluronan. Histochem Cell Biol 2012;137:107-20.
11. Symonette CJ, Kaur Mann A, Tan XC, Tolg C, Ma J, Perera F, et al. Hyaluronan-phosphatidylethanolamine polymers form pericellular coats on keratinocytes and promote basal keratinocyte proliferation. Biomed Res Int 2014;2014:727459.
12. Murai T. Lipid Raft-mediated regulation of hyaluronan-CD44 interactions in inflammation and cancer. Front Immunol 2015;6:420.
13. Toole BP. Hyaluronan: from extracellular glue to pericellular cue. Nat Rev Cancer 2004;4:528-39.
14. Turley EA, Noble PW, Bourguignon LY. Signaling properties of hyaluronan receptors. J Biol Chem 2002;277:4589-92.
15. Cieply B, Koontz C, Frisch SM. CD44S-hyaluronan interactions protect cells resulting from EMT against anoikis. Matrix Biol 2015;48:55-65.
16. Veiseh M, Kwon DH, Borowsky AD, Tolg C, Leong HS, Lewis JD, et al. Cellular heterogeneity profiling by hyaluronan probes reveals an invasive but slow-growing breast tumor subset. Proc Natl Acad Sci U S A 2014;111: E1731-9.
17. Rilla K, Pasonen-Seppanen S, Deen AJ, Koistinen VV, Wojciechowski S, Oikari S, et al. Hyaluronan production enhances shedding of plasma membrane-derived microvesicles. Exp Cell Res 2013;319:2006-18.
18. Tian X, Azpurua J, Hine C, Vaidya A, Myakishev-RempelM, Ablaeva J, et al. High-molecular-mass hyaluronan mediates the cancer resistance of the naked mole rat. Nature 2013;499:346-9.
19. Benitez A, Yates TJ, Lopez LE, Cerwinka WH, Bakkar A, Lokeshwar VB. Targeting hyaluronidase for cancer therapy: antitumor activity of sulfated hyaluronic acid in prostate cancer cells. Cancer Res 2011;71:4085-95.
20. Cowman MK, Lee HG, Schwertfeger KL, McCarthy JB, Turley EA. The content and size of hyaluronan in biological fluids and tissues. Front Immunol 2015;6:261.
21. McAtee CO, Barycki JJ, Simpson MA. Emerging roles for hyaluronidase in cancer metastasis and therapy. Adv Cancer Res 2014;123:1-34.
22. Simpson MA, Lokeshwar VB. Hyaluronan and hyaluronidase in genitourinary tumors. Front Biosci 2008;13:5664-80.
23. Bharadwaj AG, Kovar JL, Loughman E, Elowsky C, Oakley GG, Simpson MA. Spontaneous metastasis of prostate cancer is promoted by excess hyaluronan synthesis and processing. Am J Pathol 2009;174:1027-36.
24. Keane M, Craig T, Alfoldi J, Berlin AM, Johnson J, Seluanov A, et al. The Naked Mole Rat Genome Resource: facilitating analyses of cancer and longevity-related adaptations. Bioinformatics 2014;30:3558-60.
25. Toole BP, Slomiany MG. Hyaluronan, CD44 and Emmprin: partners in cancer cell chemoresistance. Drug Resist Updat 2008;11:110-21.
26. Banerji S, Ni J, Wang SX, Clasper S, Su J, Tammi R, et al. LYVE-1, a new homologue of the CD44 glycoprotein, is a lymph-specific receptor for hyaluronan. J Cell Biol 1999;144:789-801.
27. Day AJ, Prestwich GD. Hyaluronan-binding proteins: tying up the giant. J Biol Chem 2002;277:4585-8.
28. Liu LK, Finzel BC. Fragment-based identification of an inducible binding site on cell surface receptor CD44 for the design of protein-carbohydrate interaction inhibitors. J Med Chem 2014;57:2714-25.
29. Toole BP, Slomiany MG. Hyaluronan: a constitutive regulator of chemoresistance and malignancy in cancer cells. Semin Cancer Biol 2008; 18:244-50.
30. Slomiany MG, Grass GD, Robertson AD, Yang XY,Maria BL, Beeson C, et al. Hyaluronan, CD44, and emmprin regulate lactate efflux and membrane localization of monocarboxylate transporters in human breast carcinoma cells. Cancer Res 2009;69:1293-301.
31. Slomiany MG, Dai L, Tolliver LB, Grass GD, Zeng Y, Toole BP. Inhibition of functional hyaluronan-CD44 interactions in CD133-positive primary human ovarian carcinoma cells by small hyaluronan oligosaccharides. Clin Cancer Res 2009;15:7593-601.
32. Wakamatsu Y, Sakamoto N, Oo HZ, Naito Y, Uraoka N, Anami K, et al. Expression of cancer stem cell markers ALDH1, CD44 and CD133 in primary tumor and lymph node metastasis of gastric cancer. Pathol Int 2012;62:112-9.
33. Yan Y, Zuo X, Wei D. Concise review: emerging role of CD44 in cancer stem cells: a promising biomarker and therapeutic target. Stem Cells TranslMed 2015;4:1033-43.
34. Greiner J, Ringhoffer M, TaniguchiM, Schmitt A, Kirchner D, Krahn G, et al. Receptor for hyaluronan acid-mediated motility (RHAMM) is a new immunogenic leukemia-associated antigen in acute and chronic myeloid leukemia. Exp Hematol 2002;30:1029-35.
35. Gurski LA, Xu X, Labrada LN, Nguyen NT, Xiao L, van Golen KL, et al. Hyaluronan (HA) interacting proteins RHAMM and hyaluronidase impact prostate cancer cell behavior and invadopodia formation in 3D HA-based hydrogels. PLoS One 2012;7:e50075.
36. Korkes F, de Castro MG, de Cassio Zequi S, Nardi L, Del Giglio A, de Lima Pompeo AC. Hyaluronan-mediated motility receptor (RHAMM) immunohistochemical expression and androgen deprivation in normal peritumoral, hyperplasic and neoplastic prostate tissue. BJU Int 2014;113:822-9.
37. Kouvidi K, Nikitovic D, Berdiaki A, Tzanakakis GN. Hyaluronan/RHAMM interactions in mesenchymal tumor pathogenesis: role of growth factors. Adv Cancer Res 2014;123:319-49.
38. Maxwell CA, Benitez J, Gomez-Baldo L, Osorio A, Bonifaci N, Fernandez-Ramires R, et al. Interplay between BRCA1 and RHAMM regulates epithelial apicobasal polarization and may influence risk of breast cancer. PLoS Biol 2011;9:e1001199.
39. Mohan P, Castellsague J, Jiang J, Allen K, Chen H, Nemirovsky O, et al. Genomic imbalance of HMMR/RHAMM regulates the sensitivity and response of malignant peripheral nerve sheath tumour cells to aurora kinase inhibition. Oncotarget 2013;4:80-93.
40. Tolg C, Poon R, Fodde R, Turley EA, Alman BA. Genetic deletion of receptor for hyaluronan-mediated motility (Rhamm) attenuates the formation of aggressive fibromatosis (desmoid tumor). Oncogene 2003;22:6873-82.
41. Man Y, Cao J, Jin S, Xu G, Pan B, Shang L, et al. Newly identified biomarkers for detecting circulating tumor cells in lung adenocarcinoma. Tohoku J Exp Med 2014;234:29-40.
42. Zlobec I, Terracciano L, Tornillo L, Gunthert U, Vuong T, Jass JR, et al. Role of RHAMM within the hierarchy of well-established prognostic factors in colorectal cancer. Gut 2008;57:1413-9.
43. Mantripragada KK, Spurlock G, Kluwe L, Chuzhanova N, Ferner RE, Frayling IM, et al. High-resolution DNA copy number profiling of malignant peripheral nerve sheath tumors using targeted microarraybased comparative genomic hybridization. Clin Cancer Res 2008;14: 1015-24.
44. Gutjahr JC, Greil R, Hartmann TN. The role of CD44 in the pathophysiology of chronic lymphocytic leukemia. Front Immunol 2015;6:177.
45. Rizzardi AE, Vogel RI, Koopmeiners JS, Forster CL, Marston LO, Rosener NK, et al. Elevated hyaluronan and hyaluronan-mediated motility receptor are associated with biochemical failure in patientswith intermediate-grade prostate tumors. Cancer 2014;120:1800-9.
46. Wang C, Thor AD, Moore DHII, Zhao Y, Kerschmann R, Stern R, et al. The overexpression of RHAMM, a hyaluronan-binding protein that regulates ras signaling, correlates with overexpression of mitogen-activated protein kinase and is a significant parameter in breast cancer progression. Clin Cancer Res 1998;4:567-76.
47. Koelzer VH, Huber B, Mele V, Iezzi G, Trippel M, Karamitopoulou E, et al. Expression of the hyaluronan-mediated motility receptor RHAMM in tumor budding cells identifies aggressive colorectal cancers. Hum Pathol 2015;46:1573-81.
48. Lompardia SL, Papademetrio DL, Mascaro M, Alvarez EM, Hajos SE. Human leukemic cell lines synthesize hyaluronan to avoid senescence and resist chemotherapy. Glycobiology 2013;23:1463-76.
49. Turley EA, Austen L, Vandeligt K, Clary C. Hyaluronan and a cell-associated hyaluronan binding protein regulate the locomotion of ras-transformed cells. J Cell Biol 1991;112:1041-7.
50. Silverman-Gavrila RV, Silverman-Gavrila LB, Bilal KH, Bendeck MP. Spectrin alpha is important for rear polarization of the microtubule organizing center during migration and spindle pole assembly during division of neointimal smooth muscle cells. Cytoskeleton 2015;72:157-70.
51. Smith TC, Fang Z, Luna EJ. Novel interactors and a role for supervillin in early cytokinesis. Cytoskeleton 2010;67:346-64.
52. Hatano H, Shigeishi H, Kudo Y, Higashikawa K, Tobiume K, Takata T, et al. RHAMM/ERK interaction induces proliferative activities of cementifying fibroma cells through a mechanism based on the CD44-EGFR. Lab Invest 2011;91:379-91.
53. Meier C, Spitschak A, Abshagen K, Gupta S, Mor JM, Wolkenhauer O, et al. Association of RHAMM with E2F1 promotes tumour cell extravasation by transcriptional up-regulation of fibronectin. J Pathol 2014;234:351-64.
54. Stangeland B, Mughal AA, Grieg Z, Sandberg CJ, Joel M, Nygard S, et al. Combined expressional analysis, bioinformatics and targeted proteomics identify new potential therapeutic targets in glioblastoma stem cells. Oncotarget 2015;6:26192-215.
55. Samuel SK, Hurta RA, Spearman MA, Wright JA, Turley EA, Greenberg AH. TGF-beta 1 stimulation of cell locomotion utilizes the hyaluronan receptor RHAMM and hyaluronan. J Cell Biol 1993;123:749-58.
56. Esguerra KV, Tolg C, Akentieva N, Price M, Cho CF, Lewis JD, et al. Identification, design and synthesis of tubulin-derived peptides as novel hyaluronan mimetic ligands for the receptor for hyaluronan-mediated motility (RHAMM/HMMR). Integr Biol 2015;7:1547-60.
57. TolgC,Hamilton SR, Zalinska E,McCulloch L, Amin R, Akentieva N, et al. A RHAMM mimetic peptide blocks hyaluronan signaling and reduces inflammation and fibrogenesis in excisional skin wounds. Am J Pathol 2012;181:1250-70.
58. Lokeshwar VB, Mirza S, Jordan A. Targeting hyaluronic acid family for cancer chemoprevention and therapy. Adv Cancer Res 2014;123:35-65.
59. Schmitt M, Schmitt A, Rojewski MT, Chen J, Giannopoulos K, Fei F, et al. RHAMM-R3 peptide vaccination in patients with acutemyeloid leukemia, myelodysplastic syndrome, and multiple myeloma elicits immunologic and clinical responses. Blood 2008;111:1357-65.
60. Yates TJ, Lopez LE, Lokeshwar SD, Ortiz N, Kallifatidis G, Jordan A, et al. Dietary supplement 4-methylumbelliferone: an effective chemopreventive and therapeutic agent for prostate cancer. J Natl Cancer Inst 2015;107:pii: djv085.
61. Yoshihara S, Kon A, Kudo D, Nakazawa H, Kakizaki I, Sasaki M, et al. A hyaluronan synthase suppressor, 4-methylumbelliferone, inhibits liver metastasis of melanoma cells. FEBS Lett 2005;579:2722-6.
62. Veiseh M, Leith SJ, Tolg C, Elhayek SS, Bahrami SB, Collis L, et al. Uncovering the dual role of RHAMM as an HA receptor and a regulator of CD44 expression in RHAMM-expressingmesenchymal progenitor cells. Front Cell Dev Biol 2015;3:63.