Elucidating the mechanobiology of malignant brain tumors using a brain matrix-mimetic hyaluronic acid hydrogel platform

Biomaterials

Volumn 32, Issue 31, 2011, Pages 7913-7923

  Ananthanarayanan, Badriprasad ^a   Kim, Yushan ^a,b   Kumar, Sanjay ^a,b  

^a University of California   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Brain; Cell adhesion; ECM (extracellular matrix); Hyaluronic acid hyaluronan

Indexed keywords

ADHESIVE LIGANDS; ARG GLY ASPS; BRAIN PARENCHYMA; BRAIN SLICES; BRAIN TISSUE; BRAIN TUMORS; ECM (EXTRACELLULAR MATRIX); EXTRACELLULAR MATRICES; EXTRACELLULAR SPACE; FLAT SURFACES; FUNCTIONALIZED; GLIOBLASTOMA MULTIFORME; GLIOMA CELLS; HYALURONIC ACID HYDROGELS; HYALURONIC ACIDS; INDEPENDENT CONTROL; MATERIAL SYSTEMS; MECHANO-BIOLOGY; MODEL MATRICES; MORPHOLOGICAL PATTERNS; NANO-SCALE POROSITY; PHYSICAL STRUCTURES; RGD PEPTIDE; SCANNING ELECTRON MICROGRAPHS; SHEET-LIKE; SINGLE CELLS; STRESS FIBERS; THREE-DIMENSIONAL (3D); TUMOR CELLS; TUNABLE LIGANDS;

ADHESION; BIOMIMETICS; CELL ADHESION; CELLS; LIGANDS; MICROSTRUCTURE; ORGANIC ACIDS; PEPTIDES; SCANNING ELECTRON MICROSCOPY; STIFFNESS; THREE DIMENSIONAL; TUMORS;

HYDROGELS;

ACTIN; ARGINYLGLYCYLASPARTIC ACID; COLLAGEN; HYALURONIC ACID;

ANIMAL CELL; ARTICLE; BRAIN CANCER; BRAIN TISSUE; CELL ADHESION; CELL MOTILITY; CONTROLLED STUDY; EXTRACELLULAR MATRIX; EXTRACELLULAR SPACE; GLIOMA CELL; HUMAN; HUMAN CELL; HYDROGEL; NANOANALYSIS; NONHUMAN; POROSITY; PRIORITY JOURNAL; RAT; RIGIDITY; SCANNING ELECTRON MICROSCOPY; STRESS FIBER; SYNTHESIS; TUMOR GROWTH;

BIOMECHANICS; BIOMIMETIC MATERIALS; BRAIN NEOPLASMS; CELL ADHESION; CELL COUNT; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; CELL SHAPE; EXTRACELLULAR MATRIX; GLIOMA; HUMANS; HYALURONIC ACID; HYDROGELS; METHACRYLATES; MICROSCOPY, ELECTRON, SCANNING; NEOPLASM INVASIVENESS; OLIGOPEPTIDES; SPHEROIDS, CELLULAR;

EID: 80051821707     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2011.07.005     Document Type: Article

References (92)

1. Wen P.Y., Kesari S. Malignant gliomas in adults. N Engl J Med 2008, 359(5):492-507.
2. Nakada M., Nakada S., Demuth T., Tran N.L., Hoelzinger D.B., Berens M.E. Molecular targets of glioma invasion. Cell Mol Life Sci 2007, 64(4):458-478.
3. Furnari F.B., Fenton T., Bachoo R.M., Mukasa A., Stommel J.M., Stegh A., et al. Malignant astrocytic glioma: genetics, biology, and paths to treatment. Genes Dev 2007, 21(21):2683-2710.
4. Pàez-Ribes M., Allen E., Hudock J., Takeda T., Okuyama H., Viñals F., et al. Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis. Cancer Cell. 2009, 15(3):220-231.
5. Kunkel P., Ulbricht U., Bohlen P., Brockmann M.A., Fillbrandt R., Stavrou D., et al. Inhibition of glioma angiogenesis and growth in vivo by systemic treatment with a monoclonal antibody against vascular endothelial growth factor receptor-2. Cancer Res 2001, 61(18):6624-6628.
6. Bissell M.J., Radisky D. Putting tumours in context. Nat Rev Cancer 2001, 1(1):46-54.
7. Bellail A.C., Hunter S.B., Brat D.J., Tan C., Van Meir E.G. Microregional extracellular matrix heterogeneity in brain modulates glioma cell invasion. Int J Biochem Cell Biol 2004, 36(6):1046-1069.
8. Paganetti P.A., Caroni P., Schwab M.E. Glioblastoma infiltration into central nervous system tissue in vitro - involvement of a metalloprotease. J Cell Biol 1988, 107(6):2281-2291.
9. Bernstein J.J., Woodard C.A. Glioblastoma cells do not intravasate into blood-vessels. Neurosurgery 1995, 36(1):124-132.
10. Ruoslahti E. Brain extracellular matrix. Glycobiology 1996, 6(5):489-492.
11. Gladson C.L. The extracellular matrix of gliomas: modulation of cell function. J Neuropathol Exp Neurol 1999, 58(10):1029-1040.
12. Laurent T.C., Fraser J.R.E. Hyaluronan. FASEB J 1992, 6(7):2397-2404.
13. Toole B.P. Hyaluronan: from extracellular glue to pericellular cue. Nat Rev Cancer 2004, 4(7):528-539.
14. Delpech B., Maingonnat C., Girard N., Chauzy C., Maunoury R., Olivier A., et al. Hyaluronan and hyaluronectin in the extracellular matrix of human brain tumor stroma. Eur J Cancer 1993, 29A(7):1012-1017.
15. Koochekpour S., Pilkington G.J., Merzak A. Hyaluronic acid/CD44H interaction induces cell detachment and stimulates migration and invasion of human glioma cells in vitro. Int J Cancer 1995, 63(3):450-454.
16. Radotra B., McCormick D. Glioma invasion in vitro is mediated by CD44-hyaluronan interactions. J Pathol 1997, 181(4):434-438.
17. Hayen W., Goebeler M., Kumar S., Riessen R., Nehls V. Hyaluronan stimulates tumor cell migration by modulating the fibrin fiber architecture. J Cell Sci 1999, 112(13):2241-2251.
18. Giese A., Loo M.A., Rief M.D., Tran N., Berens M.E. Substrates for astrocytoma invasion. Neurosurgery 1995, 37(2):294-301.
19. Akiyama Y., Jung S., Salhia B., Lee S.P., Hubbard S., Taylor M., et al. Hyaluronate receptors mediating glioma cell migration and proliferation. J Neurooncol 2001, 53(2):115-127.
20. Okada H., Yoshida J., Sokabe M., Wakabayashi T., Hagiwara M. Suppression of CD44 expression decreases migration and invasion of human glioma cells. Int J Cancer 1996, 66(2):255-260.
21. Turley E.A., Noble P.W., Bourguignon L.Y.W. Signaling properties of hyaluronan receptors. J Biol Chem 2002, 277(7):4589-4592.
22. Xu Y., Stamenkovic I., Yu Q. CD44 attenuates activation of the Hippo signaling pathway and is a prime therapeutic target for glioblastoma. Cancer Res 2010, 70(6):2455-2464.
23. Ranuncolo S.M., Ladeda V., Specterman S., Varela M., Lastiri J., Morandi A., et al. CD44 expression in human gliomas. J Surg Oncol 2002, 79(1):30-36.
24. Ariza A., Lopez D., Mate J.L., Isamat M., Musulen E., Pujol M., et al. Role of CD44 in the invasiveness of glioblastoma multiforme and the noninvasiveness of meningioma - an immunohistochemistry study. Hum Pathol 1995, 26(10):1144-1147.
25. Bourguignon L.Y.W. Hyaluronan-mediated CD44 activation of RhoGTPase signaling and cytoskeleton function promotes tumor progression. Semin Cancer Biol 2008, 18(4):251-259.
26. Bourguignon L.Y.W., Singleton P.A., Zhu H.B., Diedrich F. Hyaluronan-mediated CD44 interaction with RhoGEF and Rho kinase promotes Grb2-associated binder-1 phosphorylation and phosphatidylinositol 3-kinase signaling leading to cytokine (Macrophage-Colony stimulating factor) production and breast tumor progression. J Biol Chem 2003, 278(32):29420-29434.
27. Tsatas D., Kanagasundaram V., Kaye A., Novak U. EGF receptor modifies cellular responses to hyaluronan in glioblastoma cell lines. J Clin Neurosci 2002, 9(3):282-288.
28. Bourguignon L.Y.W., Zhu H.B., Shao L.J., Chen Y.W. CD44 interaction with Tiam1 promotes Rac1 signaling and hyaluronic acid-mediated breast tumor cell migration. J Biol Chem 2000, 275(3):1829-1838.
29. Toole B.P., Trelstad R.L. Hyaluronate production and removal during corneal development in chick. Dev Biol 1971, 26(1):28.
30. Butcher D.T., Alliston T., Weaver V.M. A tense situation: forcing tumour progression. Nat Rev Cancer 2009, 9(2):108-122.
31. Kumar S., Weaver V. Mechanics, malignancy, and metastasis: the force journey of a tumor cell. Cancer Metastasis Rev 2009, 28(1):113-127.
32. Ulrich T.A., de Juan Pardo E.M., Kumar S. The mechanical rigidity of the extracellular matrix regulates the structure, motility, and proliferation of glioma cells. Cancer Res 2009, 69(10):4167-4174.
33. Sen S., Dong M.M., Kumar S. Isoform-specific contributions of alpha-actinin to glioma cell mechanobiology. PLoS One 2009, 4(12):e8427.
34. Beadle C., Assanah M.C., Monzo P., Vallee R., Rosenfeld S.S., Canoll P. The role of Myosin II in glioma invasion of the brain. Mol Biol Cell 2008, 19(8):3357-3368.
35. Ulrich T.A., Jain A., Tanner K., MacKay J.L., Kumar S. Probing cellular mechanobiology in three-dimensional culture with collagen-agarose matrices. Biomaterials 2010, 31(7):1875-1884.
36. Kaufman L.J., Brangwynne C.P., Kasza K.E., Filippidi E., Gordon V.D., Deisboeck T.S., et al. Glioma expansion in collagen I matrices: analyzing collagen concentration-dependent growth and motility patterns. Biophys J 2005, 89(1):635-650.
37. Hegedus B., Marga F., Jakab K., Sharpe-Timms K.L., Forgacs G. The interplay of cell-cell and cell-matrix interactions in the invasive properties of brain tumors. Biophys J 2006, 91(7):2708-2716.
38. Kim H.D., Guo T.W., Wu A.P., Wells A., Gertler F.B., Lauffenburger D.A. Epidermal Growth Factor-induced enhancement of glioblastoma cell migration in 3D arises from an intrinsic increase in speed but an extrinsic matrix- and proteolysis-dependent increase in persistence. Mol Biol Cell 2008, 19(10):4249-4259.
39. Pathak A., Kumar S. Biophysical regulation of tumor cell invasion: moving beyond matrix stiffness. Integr Biol (Camb) 2011, 3(4):267-278.
40. Gerecht S., Burdick J.A., Ferreira L.S., Townsend S.A., Langer R., Vunjak-Novakovic G. Hyaluronic acid hydrogel for controlled self-renewal and differentiation of human embryonic stem cells. Proc Natl Acad Sci U S A 2007, 104(27):11298-11303.
41. Baier Leach J., Bivens K.A., Patrick C.W., Schmidt C.E. Photocrosslinked hyaluronic acid hydrogels: natural, biodegradable tissue engineering scaffolds. Biotechnol Bioeng 2003, 82(5):578-589.
42. Masters K.S., Shah D.N., Leinwand L.A., Anseth K.S. Crosslinked hyaluronan scaffolds as a biologically active carrier for valvular interstitial cells. Biomaterials 2005, 26(15):2517-2525.
43. Campoccia D., Doherty P., Radice M., Brun P., Abatangelo G., Williams D.F. Semisynthetic resorbable materials from hyaluronan esterification. Biomaterials 1998, 19(23):2101-2127.
44. Wang T.-W., Spector M. Development of hyaluronic acid-based scaffolds for brain tissue engineering. Acta Biomater 2009, 5(7):2371-2384.
45. Lei Y., Gojgini S., Lam J., Segura T. The spreading, migration and proliferation of mouse mesenchymal stem cells cultured inside hyaluronic acid hydrogels. Biomaterials 2011, 32(1):39-47.
46. Burdick J.A., Prestwich G.D. Hyaluronic acid hydrogels for biomedical applications. Adv Mater 2011, 23(12):H41-H56.
47. Shu X.Z., Liu Y., Luo Y., Roberts M.C., Prestwich G.D. Disulfide cross-linked hyaluronan hydrogels. Biomacromolecules 2002, 3(6):1304-1311.
48. Young J.L., Engler A.J. Hydrogels with time-dependent material properties enhance cardiomyocyte differentiation in vitro. Biomaterials 2011, 32(4):1002-1009.
49. Jin S.G., Jeong Y.I., Jung S., Ryu H.H., Jin Y.H., Kim I.Y. The effect of hyaluronic acid on the invasiveness of malignant glioma cells: comparison of invasion potential at hyaluronic acid hydrogel and matrigel. J Korean Neurosurg Soc 2009, 46(5):472-478.
50. Coquerel B., Poyer F., Torossian F., Dulong V., Bellon G., Dubus I., et al. Elastin-derived peptides: matrikines critical for glioblastoma cell aggressiveness in a 3-D system. Glia 2009, 57(16):1716-1726.
51. Smeds K.A., Pfister-Serres A., Miki D., Dastgheib K., Inoue M., Hatchell D.L., et al. Photocrosslinkable polysaccharides for in situ hydrogel formation. J Biomed Mater Res 2001, 54(1):115-121.
52. Marklein R.A., Burdick J.A. Spatially controlled hydrogel mechanics to modulate stem cell interactions. Soft Matter 2010, 6(1):136.
53. Canal T., Peppas N.A. Correlation between mesh size and equilibrium degree of swelling of polymeric networks. J Biomed Mater Res 1989, 23(10):1183-1193.
54. Kelm J.M., Timmins N.E., Brown C.J., Fussenegger M., Nielsen L.K. Method for generation of homogeneous multicellular tumor spheroids applicable to a wide variety of cell types. Biotechnol Bioeng 2003, 83(2):173-180.
55. Elbert D.L., Pratt A.B., Lutolf M.P., Halstenberg S., Hubbell J.A. Protein delivery from materials formed by self-selective conjugate addition reactions. J Control Release 2001, 76(1-2):11-25.
56. Lutolf M.P., Hubbell J.A. Synthesis and physicochemical characterization of end-linked poly(ethylene glycol)-co-peptide hydrogels formed by Michael-type addition. Biomacromolecules 2003, 4(3):713-722.
57. Khetan S., Katz J.S., Burdick J.A. Sequential crosslinking to control cellular spreading in 3-dimensional hydrogels. Soft Matter 2009, 5(8):1601-1606.
58. Anseth K.S., Bowman C.N., Brannon-Peppas L. Mechanical properties of hydrogels and their experimental determination. Biomaterials 1996, 17(17):1647-1657.
59. Elkin B.S., Azeloglu E.U., Costa K.D., Morrison B. Mechanical heterogeneity of the rat hippocampus measured by atomic force microscope indentation. J Neurotrauma 2007, 24(5):812-822.
60. Christ A.F., Franze K., Gautier H., Moshayedi P., Fawcett J., Franklin R.J.M., et al. Mechanical difference between white and gray matter in the rat cerebellum measured by scanning force microscopy. J Biomech 2010, 43(15):2986-2992.
61. Cheng S., Clarke E.C., Bilston L.E. Rheological properties of the tissues of the central nervous system: a review. Med Eng Phys 2008, 30(10):1318-1337.
62. Segura T., Anderson B.C., Chung P.H., Webber R.E., Shull K.R., Shea L.D. Crosslinked hyaluronic acid hydrogels: a strategy to functionalize and pattern. Biomaterials 2005, 26(4):359-371.
63. Brigham M.D., Bick A., Lo E., Bendali A., Burdick J.A., Khademhosseini A. Mechanically robust and bioadhesive collagen and photocrosslinkable hyaluronic acid semi-interpenetrating networks. Tissue Eng Part A 2009, 15(7):1645-1653.
64. Eng D., Caplan M., Preul M., Panitch A. Hyaluronan scaffolds: a balance between backbone functionalization and bioactivity. Acta Biomater 2010, 6(7):2407-2414.
65. Collins M.N., Birkinshaw C. Investigation of the swelling behavior of crosslinked hyaluronic acid films and hydrogels produced using homogeneous reactions. J Appl Polym Sci 2008, 109(2):923-931.
66. Raeber G.P., Lutolf M.P., Hubbell J.A. Molecularly engineered PEG hydrogels: a novel model system for proteolytically mediated cell migration. Biophys J 2005, 89(2):1374-1388.
67. Bellamkonda R., Ranieri J.P., Bouche N., Aebischer P. Hydrogel-based 3-dimensional matrix for neural cells. J Biomed Mater Res 1995, 29(5):663-671.
68. Ghosh K., Shu X.Z., Mou R., Lombardi J., Prestwich G.D., Rafailovich M.H., et al. Rheological characterization of in situ cross-linkable hyaluronan hydrogels. Biomacromolecules 2005, 6(5):2857-2865.
69. Massia S.P., Hubbell J.A. An RGD spacing of 440nm is sufficient for integrin Alpha-V-Beta-3-mediated fibroblast spreading and 140nm for focal contact and stress fiber formation. J Cell Biol 1991, 114(5):1089-1100.
70. Rezania A., Johnson R., Lefkow A.R., Healy K.E. Bioactivation of metal oxide surfaces. 1. Surface characterization and cell response. Langmuir 1999, 15(20):6931-6939.
71. Maheshwari G., Brown G., Lauffenburger D.A., Wells A., Griffith L.G. Cell adhesion and motility depend on nanoscale RGD clustering. J Cell Sci 2000, 113(10):1677-1686.
72. Zaman M.H., Trapani L.M., Sieminski A.L., MacKellar D., Gong H., Kamm R.D., et al. Migration of tumor cells in 3D matrices is governed by matrix stiffness along with cell-matrix adhesion and proteolysis. Proc Natl Acad Sci U S A 2006, 103(29):10889-10894.
73. Lo C.M., Wang H.B., Dembo M., Wang Y.L. Cell movement is guided by the rigidity of the substrate. Biophys J 2000, 79(1):144-152.
74. Peyton S.R., Putnam A.J. Extracellular matrix rigidity governs smooth muscle cell motility in a biphasic fashion. J Cell Physiol 2005, 204(1):198-209.
75. Pathak A., Kumar S. From molecular signal activation to locomotion: an integrated, multiscale analysis of cell motility on defined matrices. PLoS One 2011, 6(3):e18423.
76. Chen C.S., Mrksich M., Huang S., Whitesides G.M., Ingber D.E. Geometric control of cell life and death. Science 1997, 276(5317):1425-1428.
77. Ulrich T.A., Lee T.G., Shon H.K., Moon D.W., Kumar S. Microscale mechanisms of agarose-induced disruption of collagen remodeling. Biomaterials 2011, 32(24):5633-5642.
78. Kakita A., Goldman J.E. Patterns and dynamics of SVZ cell migration in the postnatal forebrain: monitoring living progenitors in slice preparations. Neuron 1999, 23(3):461-472.
79. Thorne R.G., Nicholson C. In vivo diffusion analysis with quantum dots and dextrans predicts the width of brain extracellular space. Proc Natl Acad Sci U S A 2006, 103(14):5567-5572.
80. Seidlits S.K., Khaing Z.Z., Petersen R.R., Nickels J.D., Vanscoy J.E., Shear J.B., et al. The effects of hyaluronic acid hydrogels with tunable mechanical properties on neural progenitor cell differentiation. Biomaterials 2010, 31(14):3930-3940.
81. Ghosh K., Pan Z., Guan E., Ge S.R., Liu Y.J., Nakamura T., et al. Cell adaptation to a physiologically relevant ECM mimic with different viscoelastic properties. Biomaterials 2007, 28(4):671-679.
82. Unsgaard G., Rygh O.M., Selbekk T., Müller T.B., Kolstad F., Lindseth F., et al. Intra-operative 3D ultrasound in neurosurgery. Acta Neurochir (Wien) 2006, 148(3):235-253.
83. Y-l Yang, Motte S., Kaufman L.J. Pore size variable type I collagen gels and their interaction with glioma cells. Biomaterials 2010, 31(21):5678-5688.
84. Katsumi A., Orr A.W., Tzima E., Schwartz M.A. Integrins in mechanotransduction. J Biol Chem 2004, 279(13):12001-12004.
85. Knudson W., Loeser R.F. CD44 and integrin matrix receptors participate in cartilage homeostasis. Cell Mol Life Sci 2002, 59(1):36-44.
86. Knupfer M.M., Poppenborg H., Hotfilder M., Kuhnel K., Wolff J.E.A., Domula M. CD44 expression and hyaluronic acid binding of malignant glioma cells. Clin Exp Metastasis 1999, 17(1):71-76.
87. Novak U., Stylli S.S., Kaye A.H., Lepperdinger G. Hyaluronidase-2 overexpression accelerates intracerebral but not subcutaneous tumor formation of murine astrocytoma cells. Cancer Res 1999, 59(24):6246-6250.
88. David L., Dulong V., Le Cerf D., Chauzy C., Norris V., Delpech B., et al. Reticulated hyaluronan hydrogels: a model for examining cancer cell invasion in 3D. Matrix Biol 2004, 23(3):183-193.
89. Stern R. Hyaluronidases in cancer biology. Semin Cancer Biol 2008, 18(4):275-280.
90. Enegd B., King J.A.J., Stylli S., Paradiso L., Kaye A.H., Novak U. Overexpression of hyaluronan synthase-2 reduces the tumorigenic potential of glioma cells lacking hyaluronidase activity. Neurosurgery 2002, 50(6):1311-1318.
91. Becker L.C., Bergfeld W.F., Belsito D.V., Klaassen C.D., Marks J.G., Shank R.C., et al. Final report of the safety assessment of hyaluronic acid, potassium hyaluronate, and sodium hyaluronate. Int J Toxicol 2009, 28:5-67.
92. Liu Y.C., Shu X.Z., Prestwich G.D. Tumor engineering: orthotopic cancer models in mice using cell-loaded, injectable, cross-linked hyaluronan-derived hydrogels. Tissue Eng 2007, 13(5):1091-1101.