Hyaluronan: A modulator of the tumor microenvironment

Cancer Letters

Volumn 375, Issue 1, 2016, Pages 20-30

  Chanmee, Theerawut ^a   Ontong, Pawared ^a   Itano, Naoki ^a  

^a KYOTO SANGYO UNIVERSITY   (Japan)

Author keywords

Cancer stem cell; Epithelial mesenchymal transition; Hyaluronan; Stromal cells; Tumor microenvironment

Indexed keywords

GROWTH FACTOR; HYALURONIC ACID;

CANCER GROWTH; CANCER PATIENT; CANCER PROGNOSIS; CANCER STEM CELL; CELL FUNCTION; CELL INTERACTION; CELL INVASION; CELL PROLIFERATION; ENDOTHELIUM CELL; EXTRACELLULAR MATRIX; FIBROBLAST; HUMAN; IMMUNOCOMPETENT CELL; INFLAMMATORY CELL; INTRACELLULAR SPACE; NONHUMAN; PRIORITY JOURNAL; SHORT SURVEY; STEM CELL NICHE; STROMA CELL; TUMOR CELL; TUMOR MICROENVIRONMENT; ANIMAL; EPITHELIAL MESENCHYMAL TRANSITION; IMMUNOLOGY; IMMUNOMODULATION; MACROPHAGE; METABOLISM; NEOPLASM; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY; PHYSIOLOGY;

ANIMALS; EPITHELIAL-MESENCHYMAL TRANSITION; HUMANS; HYALURONIC ACID; IMMUNOMODULATION; MACROPHAGES; NEOPLASMS; NEOPLASTIC STEM CELLS; NEOVASCULARIZATION, PATHOLOGIC; STEM CELL NICHE; TUMOR MICROENVIRONMENT;

EID: 84960088583     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2016.02.031     Document Type: Review

References (148)

1. Quail D.F., Joyce J.A. Microenvironmental regulation of tumor progression and metastasis. Nat. Med 2013, 19:1423-1437.
2. Hanahan D., Coussens L.M. Accessories to the crime: functions of cells recruited to the tumor microenvironment. Cancer Cell 2012, 21:309-322.
3. Whiteside T.L. The tumor microenvironment and its role in promoting tumor growth. Oncogene 2008, 27:5904-5912.
4. McAllister S.S., Weinberg R.A. The tumour-induced systemic environment as a critical regulator of cancer progression and metastasis. Nat. Cell Biol 2014, 16:717-727.
5. Gorter A., Zijlmans H.J., van Gent H., Trimbos J.B., Fleuren G.J., Jordanova E.S. Versican expression is associated with tumor-infiltrating CD8-positive T cells and infiltration depth in cervical cancer. Mod. Pathol 2010, 23:1605-1615.
6. Koyama H., Hibi T., Isogai Z., Yoneda M., Fujimori M., Amano J., et al. Hyperproduction of hyaluronan in neu-induced mammary tumor accelerates angiogenesis through stromal cell recruitment: possible involvement of versican/PG-M. Am. J. Pathol 2007, 170:1086-1099.
7. Levental K.R., Yu H., Kass L., Lakins J.N., Egeblad M., Erler J.T., et al. Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 2009, 139:891-906.
8. Chiquet-Ehrismann R., Chiquet M. Tenascins: regulation and putative functions during pathological stress. J. Pathol 2003, 200:488-499.
9. Chieppa M., Bianchi G., Doni A., Del Prete A., Sironi M., Laskarin G., et al. Cross-linking of the mannose receptor on monocyte-derived dendritic cells activates an anti-inflammatory immunosuppressive program. J. Immunol 2003, 171:4552-4560.
10. Wight T.N. Versican: a versatile extracellular matrix proteoglycan in cell biology. Curr. Opin. Cell Biol 2002, 14:617-623.
11. Ames J.J., Contois L., Caron J.M., Tweedie E., Yang X., Friesel R., et al. Identification of an endogenously generated cryptic collagen epitope (XL313) that may selectively regulate angiogenesis by an integrin-YAP mechano-transduction pathway. J. Biol. Chem 2016, 291:2731-2750.
12. Toole B.P. Hyaluronan: from extracellular glue to pericellular cue. Nat. Rev. Cancer 2004, 4:528-539.
13. Heldin P., Basu K., Olofsson B., Porsch H., Kozlova I., Kahata K. Deregulation of hyaluronan synthesis, degradation and binding promotes breast cancer. J. Biochem 2013, 154:395-408.
14. Slevin M., Kumar S., Gaffney J. Angiogenic oligosaccharides of hyaluronan induce multiple signaling pathways affecting vascular endothelial cell mitogenic and wound healing responses. J. Biol. Chem 2002, 277:41046-41059.
15. West D.C., Kumar S. The effect of hyaluronate and its oligosaccharides on endothelial cell proliferation and monolayer integrity. Exp. Cell Res 1989, 183:179-196.
16. Bollyky P.L., Lord J.D., Masewicz S.A., Evanko S.P., Buckner J.H., Wight T.N., et al. Cutting edge: high molecular weight hyaluronan promotes the suppressive effects of CD4+CD25+ regulatory T cells. J. Immunol 2007, 179:744-747.
17. Weigel P.H., Hascall V.C., Tammi M. Hyaluronan synthases. J. Biol. Chem 1997, 272:13997-14000.
18. Csoka A.B., Scherer S.W., Stern R. Expression analysis of six paralogous human hyaluronidase genes clustered on chromosomes 3p21 and 7q31. Genomics 1999, 60:356-361.
19. + exchanger (NHE1) creates acidic microenvironments leading to hyaluronidase-2 and cathepsin B activation and breast tumor cell invasion. J. Biol. Chem 2004, 279:26991-27007.
20. Csoka A.B., Frost G.I., Stern R. The six hyaluronidase-like genes in the human and mouse genomes. Matrix Biol 2001, 20:499-508.
21. Yoshida H., Nagaoka A., Kusaka-Kikushima A., Tobiishi M., Kawabata K., Sayo T., et al. KIAA1199, a deafness gene of unknown function, is a new hyaluronan binding protein involved in hyaluronan depolymerization. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:5612-5617.
22. Abe S., Usami S., Nakamura Y. Mutations in the gene encoding KIAA1199 protein, an inner-ear protein expressed in Deiters' cells and the fibrocytes, as the cause of nonsyndromic hearing loss. J. Hum. Genet 2003, 48:564-570.
23. Auvinen P., Tammi R., Parkkinen J., Tammi M., Agren U., Johansson R., et al. Hyaluronan in peritumoral stroma and malignant cells associates with breast cancer spreading and predicts survival. Am. J. Pathol 2000, 156:529-536.
24. Josefsson A., Adamo H., Hammarsten P., Granfors T., Stattin P., Egevad L., et al. Prostate cancer increases hyaluronan in surrounding nonmalignant stroma, and this response is associated with tumor growth and an unfavorable outcome. Am. J. Pathol 2011, 179:1961-1968.
25. Lipponen P., Aaltomaa S., Tammi R., Tammi M., Agren U., Kosma V.M. High stromal hyaluronan level is associated with poor differentiation and metastasis in prostate cancer. Eur. J. Cancer 2001, 37:849-856.
26. Anttila M.A., Tammi R.H., Tammi M.I., Syrjanen K.J., Saarikoski S.V., Kosma V.M. High levels of stromal hyaluronan predict poor disease outcome in epithelial ovarian cancer. Cancer Res 2000, 60:150-155.
27. Pirinen R., Tammi R., Tammi M., Hirvikoski P., Parkkinen J.J., Johansson R., et al. Prognostic value of hyaluronan expression in non-small-cell lung cancer: increased stromal expression indicates unfavorable outcome in patients with adenocarcinoma. Int. J. Cancer 2001, 95:12-17.
28. Kosunen A., Ropponen K., Kellokoski J., Pukkila M., Virtaniemi J., Valtonen H., et al. Reduced expression of hyaluronan is a strong indicator of poor survival in oral squamous cell carcinoma. Oral Oncol 2004, 40:257-263.
29. Karjalainen J.M., Tammi R.H., Tammi M.I., Eskelinen M.J., Agren U.M., Parkkinen J.J., et al. Reduced level of CD44 and hyaluronan associated with unfavorable prognosis in clinical stage I cutaneous melanoma. Am. J. Pathol 2000, 157:957-965.
30. Itano N., Sawai T., Atsumi F., Miyaishi O., Taniguchi S., Kannagi R., et al. Selective expression and functional characteristics of three mammalian hyaluronan synthases in oncogenic malignant transformation. J. Biol. Chem 2004, 279:18679-18687.
31. Auvinen P., Rilla K., Tumelius R., Tammi M., Sironen R., Soini Y., et al. Hyaluronan synthases (HAS1-3) in stromal and malignant cells correlate with breast cancer grade and predict patient survival. Breast Cancer Res. Treat 2014, 143:277-286.
32. Adamia S., Reiman T., Crainie M., Mant M.J., Belch A.R., Pilarski L.M. Intronic splicing of hyaluronan synthase 1 (HAS1): a biologically relevant indicator of poor outcome in multiple myeloma. Blood 2005, 105:4836-4844.
33. Itano N., Sawai T., Miyaishi O., Kimata K. Relationship between hyaluronan production and metastatic potential of mouse mammary carcinoma cells. Cancer Res 1999, 59:2499-2504.
34. Liu N., Gao F., Han Z., Xu X., Underhill C.B., Zhang L. Hyaluronan synthase 3 overexpression promotes the growth of TSU prostate cancer cells. Cancer Res 2001, 61:5207-5214.
35. Kosaki R., Watanabe K., Yamaguchi Y. Overproduction of hyaluronan by expression of the hyaluronan synthase Has2 enhances anchorage-independent growth and tumorigenicity. Cancer Res 1999, 59:1141-1145.
36. Kobayashi N., Miyoshi S., Mikami T., Koyama H., Kitazawa M., Takeoka M., et al. Hyaluronan deficiency in tumor stroma impairs macrophage trafficking and tumor neovascularization. Cancer Res 2010, 70:7073-7083.
37. Bernert B., Porsch H., Heldin P. Hyaluronan synthase 2 (HAS2) promotes breast cancer cell invasion by suppression of tissue metalloproteinase inhibitor 1 (TIMP-1). J. Biol. Chem 2011, 286:42349-42359.
38. Shuster S., Frost G.I., Csoka A.B., Formby B., Stern R. Hyaluronidase reduces human breast cancer xenografts in SCID mice. Int. J. Cancer 2002, 102:192-197.
39. Schmaus A., Klusmeier S., Rothley M., Dimmler A., Sipos B., Faller G., et al. Accumulation of small hyaluronan oligosaccharides in tumour interstitial fluid correlates with lymphatic invasion and lymph node metastasis. Br. J. Cancer 2014, 111:559-567.
40. Stern R., Asari A.A., Sugahara K.N. Hyaluronan fragments: an information-rich system. Eur. J. Cell Biol 2006, 85:699-715.
41. Sugahara K.N., Murai T., Nishinakamura H., Kawashima H., Saya H., Miyasaka M. Hyaluronan oligosaccharides induce CD44 cleavage and promote cell migration in CD44-expressing tumor cells. J. Biol. Chem 2003, 278:32259-32265.
42. Voelcker V., Gebhardt C., Averbeck M., Saalbach A., Wolf V., Weih F., et al. Hyaluronan fragments induce cytokine and metalloprotease upregulation in human melanoma cells in part by signalling via TLR4. Exp. Dermatol 2008, 17:100-107.
43. Bourguignon L.Y., Wong G., Earle C.A., Xia W. Interaction of low molecular weight hyaluronan with CD44 and toll-like receptors promotes the actin filament-associated protein 110-actin binding and MyD88-NFkappaB signaling leading to proinflammatory cytokine/chemokine production and breast tumor invasion. Cytoskeleton (Hoboken) 2011, 68:671-693.
44. Schwertfeger K.L., Cowman M.K., Telmer P.G., Turley E.A., McCarthy J.B. Hyaluronan, inflammation, and breast cancer progression. Front. Immunol 2015, 6:236.
45. Liu D., Pearlman E., Diaconu E., Guo K., Mori H., Haqqi T., et al. Expression of hyaluronidase by tumor cells induces angiogenesis in vivo. Proc. Natl. Acad. Sci. U.S.A. 1996, 93:7832-7837.
46. Lokeshwar V.B., Young M.J., Goudarzi G., Iida N., Yudin A.I., Cherr G.N., et al. Identification of bladder tumor-derived hyaluronidase: its similarity to HYAL1. Cancer Res 1999, 59:4464-4470.
47. Posey J.T., Soloway M.S., Ekici S., Sofer M., Civantos F., Duncan R.C., et al. Evaluation of the prognostic potential of hyaluronic acid and hyaluronidase (HYAL1) for prostate cancer. Cancer Res 2003, 63:2638-2644.
48. Delpech B., Laquerriere A., Maingonnat C., Bertrand P., Freger P. Hyaluronidase is more elevated in human brain metastases than in primary brain tumours. Anticancer Res 2002, 22:2423-2427.
49. Victor R., Chauzy C., Girard N., Gioanni J., d'Anjou J., Stora De Novion H., et al. Human breast-cancer metastasis formation in a nude-mouse model: studies of hyaluronidase, hyaluronan and hyaluronan-binding sites in metastatic cells. Int. J. Cancer 1999, 82:77-83.
50. Kuscu C., Evensen N., Kim D., Hu Y.J., Zucker S., Cao J. Transcriptional and epigenetic regulation of KIAA1199 gene expression in human breast cancer. PLoS ONE 2012, 7:e44661.
51. Michishita E., Garces G., Barrett J.C., Horikawa I. Upregulation of the KIAA1199 gene is associated with cellular mortality. Cancer Lett 2006, 239:71-77.
52. Birkenkamp-Demtroder K., Maghnouj A., Mansilla F., Thorsen K., Andersen C.L., Oster B., et al. Repression of KIAA1199 attenuates Wnt-signalling and decreases the proliferation of colon cancer cells. Br. J. Cancer 2011, 105:552-561.
53. Frost G.I., Mohapatra G., Wong T.M., Csoka A.B., Gray J.W., Stern R. HYAL1LUCA-1, a candidate tumor suppressor gene on chromosome 3p21.3, is inactivated in head and neck squamous cell carcinomas by aberrant splicing of pre-mRNA. Oncogene 2000, 19:870-877.
54. Nykopp T.K., Pasonen-Seppanen S., Tammi M.I., Tammi R.H., Kosma V.M., Anttila M., et al. Decreased hyaluronidase 1 expression is associated with early disease recurrence in human endometrial cancer. Gynecol. Oncol 2015, 137:152-159.
55. Cheng X.B., Sato N., Kohi S., Yamaguchi K. Prognostic impact of hyaluronan and its regulators in pancreatic ductal adenocarcinoma. PLoS ONE 2013, 8:e80765.
56. Kultti A., Zhao C., Singha N.C., Zimmerman S., Osgood R.J., Symons R., et al. Accumulation of extracellular hyaluronan by hyaluronan synthase 3 promotes tumor growth and modulates the pancreatic cancer microenvironment. Biomed Res. Int 2014, 2014:817613.
57. Noy R., Pollard J.W. Tumor-associated macrophages: from mechanisms to therapy. Immunity 2014, 41:49-61.
58. Qian B.Z., Pollard J.W. Macrophage diversity enhances tumor progression and metastasis. Cell 2010, 141:39-51.
59. Ohtaki Y., Ishii G., Nagai K., Ashimine S., Kuwata T., Hishida T., et al. Stromal macrophage expressing CD204 is associated with tumor aggressiveness in lung adenocarcinoma. J. Thorac. Oncol 2010, 5:1507-1515.
60. Zhang Q.W., Liu L., Gong C.Y., Shi H.S., Zeng Y.H., Wang X.Z., et al. Prognostic significance of tumor-associated macrophages in solid tumor: a meta-analysis of the literature. PLoS ONE 2012, 7:e50946.
61. Forssell J., Oberg A., Henriksson M.L., Stenling R., Jung A., Palmqvist R. High macrophage infiltration along the tumor front correlates with improved survival in colon cancer. Clin. Cancer Res 2007, 13:1472-1479.
62. Shimura S., Yang G., Ebara S., Wheeler T.M., Frolov A., Thompson T.C. Reduced infiltration of tumor-associated macrophages in human prostate cancer: association with cancer progression. Cancer Res 2000, 60:5857-5861.
63. Tan S.Y., Fan Y., Luo H.S., Shen Z.X., Guo Y., Zhao L.J. Prognostic significance of cell infiltrations of immunosurveillance in colorectal cancer. World J. Gastroenterol 2005, 11:1210-1214.
64. Kuang D.M., Wu Y., Chen N., Cheng J., Zhuang S.M., Zheng L. Tumor-derived hyaluronan induces formation of immunosuppressive macrophages through transient early activation of monocytes. Blood 2007, 110:587-595.
65. Wynn T.A., Chawla A., Pollard J.W. Macrophage biology in development, homeostasis and disease. Nature 2013, 496:445-455.
66. Kim S., Takahashi H., Lin W.W., Descargues P., Grivennikov S., Kim Y., et al. Carcinoma-produced factors activate myeloid cells through TLR2 to stimulate metastasis. Nature 2009, 457:102-106.
67. Tiainen S., Tumelius R., Rilla K., Hamalainen K., Tammi M., Tammi R., et al. High numbers of macrophages, especially M2-like (CD163-positive), correlate with hyaluronan accumulation and poor outcome in breast cancer. Histopathology 2015, 66:873-883.
68. Selbi W., de la Motte C.A., Hascall V.C., Day A.J., Bowen T., Phillips A.O. Characterization of hyaluronan cable structure and function in renal proximal tubular epithelial cells. Kidney Int 2006, 70:1287-1295.
69. de la Motte C.A., Hascall V.C., Drazba J., Bandyopadhyay S.K., Strong S.A. Mononuclear leukocytes bind to specific hyaluronan structures on colon mucosal smooth muscle cells treated with polyinosinic acid:polycytidylic acid: inter-alpha-trypsin inhibitor is crucial to structure and function. Am. J. Pathol 2003, 163:121-133.
70. Scheibner K.A., Lutz M.A., Boodoo S., Fenton M.J., Powell J.D., Horton M.R. Hyaluronan fragments act as an endogenous danger signal by engaging TLR2. J. Immunol 2006, 177:1272-1281.
71. Jiang D., Liang J., Li Y., Noble P.W. The role of Toll-like receptors in non-infectious lung injury. Cell Res 2006, 16:693-701.
72. Ruffell B., Coussens L.M. Macrophages and therapeutic resistance in cancer. Cancer Cell 2015, 27:462-472.
73. del Fresno C., Otero K., Gomez-Garcia L., Gonzalez-Leon M.C., Soler-Ranger L., Fuentes-Prior P., et al. Tumor cells deactivate human monocytes by up-regulating IL-1 receptor associated kinase-M expression via CD44 and TLR4. J. Immunol 2005, 174:3032-3040.
74. Madar S., Goldstein I., Rotter V. 'Cancer associated fibroblasts' - more than meets the eye. Trends Mol. Med 2013, 19:447-453.
75. Karagiannis G.S., Poutahidis T., Erdman S.E., Kirsch R., Riddell R.H., Diamandis E.P. Cancer-associated fibroblasts drive the progression of metastasis through both paracrine and mechanical pressure on cancer tissue. Mol. Cancer Res 2012, 10:1403-1418.
76. Parsonage G., Filer A.D., Haworth O., Nash G.B., Rainger G.E., Salmon M., et al. A stromal address code defined by fibroblasts. Trends Immunol 2005, 26:150-156.
77. Vong S., Kalluri R. The role of stromal myofibroblast and extracellular matrix in tumor angiogenesis. Genes Cancer 2011, 2:1139-1145.
78. Ohlund D., Elyada E., Tuveson D. Fibroblast heterogeneity in the cancer wound. J. Exp. Med 2014, 211:1503-1523.
79. Grugan K.D., Miller C.G., Yao Y., Michaylira C.Z., Ohashi S., Klein-Szanto A.J., et al. Fibroblast-secreted hepatocyte growth factor plays a functional role in esophageal squamous cell carcinoma invasion. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:11026-11031.
80. Tsuyada A., Chow A., Wu J., Somlo G., Chu P., Loera S., et al. CCL2 mediates cross-talk between cancer cells and stromal fibroblasts that regulates breast cancer stem cells. Cancer Res 2012, 72:2768-2779.
81. Ueno T., Toi M., Saji H., Muta M., Bando H., Kuroi K., et al. Significance of macrophage chemoattractant protein-1 in macrophage recruitment, angiogenesis, and survival in human breast cancer. Clin. Cancer Res 2000, 6:3282-3289.
82. Ito T.K., Ishii G., Chiba H., Ochiai A. The VEGF angiogenic switch of fibroblasts is regulated by MMP-7 from cancer cells. Oncogene 2007, 26:7194-7203.
83. Chang P.H., Hwang-Verslues W.W., Chang Y.C., Chen C.C., Hsiao M., Jeng Y.M., et al. Activation of Robo1 signaling of breast cancer cells by Slit2 from stromal fibroblast restrains tumorigenesis via blocking PI3K/Akt/beta-catenin pathway. Cancer Res 2012, 72:4652-4661.
84. Cadamuro M., Nardo G., Indraccolo S., Dall'olmo L., Sambado L., Moserle L., et al. Platelet-derived growth factor-D and Rho GTPases regulate recruitment of cancer-associated fibroblasts in cholangiocarcinoma. Hepatology 2013, 58:1042-1053.
85. Postlethwaite A.E., Keski-Oja J., Moses H.L., Kang A.H. Stimulation of the chemotactic migration of human fibroblasts by transforming growth factor beta. J. Exp. Med 1987, 165:251-256.
86. Li Y., Jiang D., Liang J., Meltzer E.B., Gray A., Miura R., et al. Severe lung fibrosis requires an invasive fibroblast phenotype regulated by hyaluronan and CD44. J. Exp. Med 2011, 208:1459-1471.
87. Tolg C., Telmer P., Turley E. Specific sizes of hyaluronan oligosaccharides stimulate fibroblast migration and excisional wound repair. PLoS ONE 2014, 9:e88479.
88. Tolg C., Hamilton S.R., Nakrieko K.A., Kooshesh F., Walton P., McCarthy J.B., et al. Rhamm-/- fibroblasts are defective in CD44-mediated ERK1,2 motogenic signaling, leading to defective skin wound repair. J. Cell Biol 2006, 175:1017-1028.
89. Midgley A.C., Rogers M., Hallett M.B., Clayton A., Bowen T., Phillips A.O., et al. Transforming growth factor-beta1 (TGF-beta1)-stimulated fibroblast to myofibroblast differentiation is mediated by hyaluronan (HA)-facilitated epidermal growth factor receptor (EGFR) and CD44 co-localization in lipid rafts. J. Biol. Chem 2013, 288:14824-14838.
90. Quante M., Tu S.P., Tomita H., Gonda T., Wang S.S., Takashi S., et al. Bone marrow-derived myofibroblasts contribute to the mesenchymal stem cell niche and promote tumor growth. Cancer Cell 2011, 19:257-272.
91. Spaeth E.L., Labaff A.M., Toole B.P., Klopp A., Andreeff M., Marini F.C. Mesenchymal CD44 expression contributes to the acquisition of an activated fibroblast phenotype via TWIST activation in the tumor microenvironment. Cancer Res 2013, 73:5347-5359.
92. Zoltan-Jones A., Huang L., Ghatak S., Toole B.P. Elevated hyaluronan production induces mesenchymal and transformed properties in epithelial cells. J. Biol. Chem 2003, 278:45801-45810.
93. Chanmee T., Ontong P., Mochizuki N., Kongtawelert P., Konno K., Itano N. Excessive hyaluronan production promotes acquisition of cancer stem cell signatures through the coordinated regulation of Twist and the transforming growth factor beta (TGF-beta)-Snail signaling axis. J. Biol. Chem 2014, 289:26038-26056.
94. Weis S.M., Cheresh D.A. Tumor angiogenesis: molecular pathways and therapeutic targets. Nat. Med 2011, 17:1359-1370.
95. Chung A.S., Lee J., Ferrara N. Targeting the tumour vasculature: insights from physiological angiogenesis. Nat. Rev. Cancer 2010, 10:505-514.
96. Davis G.E., Senger D.R. Endothelial extracellular matrix: biosynthesis, remodeling, and functions during vascular morphogenesis and neovessel stabilization. Circ. Res 2005, 97:1093-1107.
97. Montesano R., Kumar S., Orci L., Pepper M.S. Synergistic effect of hyaluronan oligosaccharides and vascular endothelial growth factor on angiogenesis in vitro. Lab. Invest 1996, 75:249-262.
98. Slevin M., Krupinski J., Kumar S., Gaffney J. Angiogenic oligosaccharides of hyaluronan induce protein tyrosine kinase activity in endothelial cells and activate a cytoplasmic signal transduction pathway resulting in proliferation. Lab. Invest 1998, 78:987-1003.
99. Lennon F.E., Mirzapoiazova T., Mambetsariev N., Mambetsariev B., Salgia R., Singleton P.A. 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. J. Biol. Chem 2014, 289:24043-24058.
100. Olofsson B., Porsch H., Heldin P. Knock-down of CD44 regulates endothelial cell differentiation via NFkappaB-mediated chemokine production. PLoS ONE 2014, 9:e90921.
101. Savani R.C., Cao G., Pooler P.M., Zaman A., Zhou Z., DeLisser H.M. Differential involvement of the hyaluronan (HA) receptors CD44 and receptor for HA-mediated motility in endothelial cell function and angiogenesis. J. Biol. Chem 2001, 276:36770-36778.
102. Matou-Nasri S., Gaffney J., Kumar S., Slevin M. Oligosaccharides of hyaluronan induce angiogenesis through distinct CD44 and RHAMM-mediated signalling pathways involving Cdc2 and gamma-adducin. Int. J. Oncol 2009, 35:761-773.
103. Fuchs K., Hippe A., Schmaus A., Homey B., Sleeman J.P., Orian-Rousseau V. Opposing effects of high- and low-molecular weight hyaluronan on CXCL12-induced CXCR4 signaling depend on CD44. Cell Death Dis 2013, 4:e819.
104. Ariffin A.B., Forde P.F., Jahangeer S., Soden D.M., Hinchion J. Releasing pressure in tumors: what do we know so far and where do we go from here? A review. Cancer Res 2014, 74:2655-2662.
105. Less J.R., Posner M.C., Boucher Y., Borochovitz D., Wolmark N., Jain R.K. Interstitial hypertension in human breast and colorectal tumors. Cancer Res 1992, 52:6371-6374.
106. Curti B.D., Urba W.J., Alvord W.G., Janik J.E., Smith J.W., Madara K., et al. Interstitial pressure of subcutaneous nodules in melanoma and lymphoma patients: changes during treatment. Cancer Res 1993, 53:2204-2207.
107. Gutmann R., Leunig M., Feyh J., Goetz A.E., Messmer K., Kastenbauer E., et al. Interstitial hypertension in head and neck tumors in patients: correlation with tumor size. Cancer Res 1992, 52:1993-1995.
108. Provenzano P.P., Hingorani S.R. Hyaluronan, fluid pressure, and stromal resistance in pancreas cancer. Br. J. Cancer 2013, 108:1-8.
109. Provenzano P.P., Cuevas C., Chang A.E., Goel V.K., Von Hoff D.D., Hingorani S.R. Enzymatic targeting of the stroma ablates physical barriers to treatment of pancreatic ductal adenocarcinoma. Cancer Cell 2012, 21:418-429.
110. Thompson C.B., Shepard H.M., O'Connor P.M., Kadhim S., Jiang P., Osgood R.J., et al. Enzymatic depletion of tumor hyaluronan induces antitumor responses in preclinical animal models. Mol. Cancer Ther 2010, 9:3052-3064.
111. Jacobetz M.A., Chan D.S., Neesse A., Bapiro T.E., Cook N., Frese K.K., et al. Hyaluronan impairs vascular function and drug delivery in a mouse model of pancreatic cancer. Gut 2013, 62:112-120.
112. Yang J., Weinberg R.A. Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev. Cell 2008, 14:818-829.
113. Xu J., Lamouille S., Derynck R. TGF-beta-induced epithelial to mesenchymal transition. Cell Res 2009, 19:156-172.
114. Lamouille S., Xu J., Derynck R. Molecular mechanisms of epithelial-mesenchymal transition. Nat. Rev. Mol. Cell Biol 2014, 15:178-196.
115. Puisieux A., Brabletz T., Caramel J. Oncogenic roles of EMT-inducing transcription factors. Nat. Cell Biol 2014, 16:488-494.
116. Zhang Y., Thant A.A., Machida K., Ichigotani Y., Naito Y., Hiraiwa Y., et al. Hyaluronan-CD44s signaling regulates matrix metalloproteinase-2 secretion in a human lung carcinoma cell line QG90. Cancer Res 2002, 62:3962-3965.
117. Ghatak S., Misra S., Toole B.P. Hyaluronan constitutively regulates ErbB2 phosphorylation and signaling complex formation in carcinoma cells. J. Biol. Chem 2005, 280:8875-8883.
118. DeSouza L.V., Matta A., Karim Z., Mukherjee J., Wang X.S., Krakovska O., et al. Role of moesin in hyaluronan induced cell migration in glioblastoma multiforme. Mol. Cancer 2013, 12:74.
119. El-Haibi C.P., Bell G.W., Zhang J., Collmann A.Y., Wood D., Scherber C.M., et al. Critical role for lysyl oxidase in mesenchymal stem cell-driven breast cancer malignancy. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:17460-17465.
120. Porsch H., Bernert B., Mehic M., Theocharis A.D., Heldin C.H., Heldin P. Efficient TGFbeta-induced epithelial-mesenchymal transition depends on hyaluronan synthase HAS2. Oncogene 2013, 32:4355-4365.
121. Conacci-Sorrell M., Simcha I., Ben-Yedidia T., Blechman J., Savagner P., Ben-Ze'ev A. Autoregulation of E-cadherin expression by cadherin-cadherin interactions: the roles of beta-catenin signaling, Slug, and MAPK. J. Cell Biol 2003, 163:847-857.
122. Onder T.T., Gupta P.B., Mani S.A., Yang J., Lander E.S., Weinberg R.A. Loss of E-cadherin promotes metastasis via multiple downstream transcriptional pathways. Cancer Res 2008, 68:3645-3654.
123. 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, 579:2722-2726.
124. Arai E., Nishida Y., Wasa J., Urakawa H., Zhuo L., Kimata K., et al. Inhibition of hyaluronan retention by 4-methylumbelliferone suppresses osteosarcoma cells in vitro and lung metastasis in vivo. Br. J. Cancer 2011, 105:1839-1849.
125. Draffin J.E., McFarlane S., Hill A., Johnston P.G., Waugh D.J. CD44 potentiates the adherence of metastatic prostate and breast cancer cells to bone marrow endothelial cells. Cancer Res 2004, 64:5702-5711.
126. Hiraga T., Ito S., Nakamura H. Cancer stem-like cell marker CD44 promotes bone metastases by enhancing tumorigenicity, cell motility, and hyaluronan production. Cancer Res 2013, 73:4112-4122.
127. Desai B., Rogers M.J., Chellaiah M.A. Mechanisms of osteopontin and CD44 as metastatic principles in prostate cancer cells. Mol. Cancer 2007, 6:18.
128. Ouhtit A., Abd Elmageed Z.Y., Abdraboh M.E., Lioe T.F., Raj M.H. In vivo evidence for the role of CD44s in promoting breast cancer metastasis to the liver. Am. J. Pathol 2007, 171:2033-2039.
129. Weber G.F., Bronson R.T., Ilagan J., Cantor H., Schmits R., Mak T.W. Absence of the CD44 gene prevents sarcoma metastasis. Cancer Res 2002, 62:2281-2286.
130. Qu C., Rilla K., Tammi R., Tammi M., Kroger H., Lammi M.J. Extensive CD44-dependent hyaluronan coats on human bone marrow-derived mesenchymal stem cells produced by hyaluronan synthases HAS1, HAS2 and HAS3. Int. J. Biochem. Cell Biol 2014, 48:45-54.
131. Goncharova V., Serobyan N., Iizuka S., Schraufstatter I., de Ridder A., Povaliy T., et al. Hyaluronan expressed by the hematopoietic microenvironment is required for bone marrow hematopoiesis. J. Biol. Chem 2012, 287:25419-25433.
132. Valent P., Bonnet D., De Maria R., Lapidot T., Copland M., Melo J.V., et al. Cancer stem cell definitions and terminology: the devil is in the details. Nat. Rev. Cancer 2012, 12:767-775.
133. Alison M.R., Lin W.R., Lim S.M., Nicholson L.J. Cancer stem cells: in the line of fire. Cancer Treat. Rev 2012, 38:589-598.
134. Kreso A., Dick J.E. Evolution of the cancer stem cell model. Cell Stem Cell 2014, 14:275-291.
135. Lu H., Clauser K.R., Tam W.L., Frose J., Ye X., Eaton E.N., et al. A breast cancer stem cell niche supported by juxtacrine signalling from monocytes and macrophages. Nat. Cell Biol 2014, 16:1105-1117.
136. Reya T., Clevers H. Wnt signalling in stem cells and cancer. Nature 2005, 434:843-850.
137. Visvader J.E., Lindeman G.J. Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat. Rev. Cancer 2008, 8:755-768.
138. Okuda H., Kobayashi A., Xia B., Watabe M., Pai S.K., Hirota S., et al. Hyaluronan synthase HAS2 promotes tumor progression in bone by stimulating the interaction of breast cancer stem-like cells with macrophages and stromal cells. Cancer Res 2012, 72:537-547.
139. Bourguignon L.Y., Wong G., Earle C., Chen L. Hyaluronan-CD44v3 interaction with Oct4-Sox2-Nanog promotes miR-302 expression leading to self-renewal, clonal formation, and cisplatin resistance in cancer stem cells from head and neck squamous cell carcinoma. J. Biol. Chem 2012, 287:32800-32824.
140. Bourguignon L.Y., Peyrollier K., Xia W., Gilad E. 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 2008, 283:17635-17651.
141. Shigeishi H., Biddle A., Gammon L., Emich H., Rodini C.O., Gemenetzidis E., et al. Maintenance of stem cell self-renewal in head and neck cancers requires actions of GSK3beta influenced by CD44 and RHAMM. Stem Cells 2013, 31:2073-2083.
142. Mani S.A., Guo W., Liao M.J., Eaton E.N., Ayyanan A., Zhou A.Y., et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008, 133:704-715.
143. Guo W., Keckesova Z., Donaher J.L., Shibue T., Tischler V., Reinhardt F., et al. Slug and Sox9 cooperatively determine the mammary stem cell state. Cell 2012, 148:1015-1028.
144. Bourguignon L.Y., Spevak C.C., Wong G., Xia W., Gilad E. Hyaluronan-CD44 interaction with protein kinase C(epsilon) promotes oncogenic signaling by the stem cell marker Nanog and the production of microRNA-21, leading to down-regulation of the tumor suppressor protein PDCD4, anti-apoptosis, and chemotherapy resistance in breast tumor cells. J. Biol. Chem 2009, 284:26533-26546.
145. Tamada M., Nagano O., Tateyama S., Ohmura M., Yae T., Ishimoto T., et al. Modulation of glucose metabolism by CD44 contributes to antioxidant status and drug resistance in cancer cells. Cancer Res 2012, 72:1438-1448.
146. Ishimoto T., Nagano O., Yae T., Tamada M., Motohara T., Oshima H., et al. CD44 variant regulates redox status in cancer cells by stabilizing the xCT subunit of system xc(-) and thereby promotes tumor growth. Cancer Cell 2011, 19:387-400.
147. Ye J., Wu H., Wu Y., Wang C., Zhang H., Shi X., et al. High molecular weight hyaluronan decreases oxidative DNA damage induced by EDTA in human corneal epithelial cells. Eye (Lond.) 2012, 26:1012-1020.
148. Grishko V., Xu M., Ho R., Mates A., Watson S., Kim J.T., et al. Effects of hyaluronic acid on mitochondrial function and mitochondria-driven apoptosis following oxidative stress in human chondrocytes. J. Biol. Chem 2009, 284:9132-9139.