Tumor cohesion and glioblastoma cell dispersal

Future Oncology

Volumn 9, Issue 8, 2013, Pages 1121-1132

  Foty, Ramsey A ^a  

^a ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

Author keywords

dispersal velocity; fibronectin matrix assembly; glioblastoma; integrin; matrix stiffness; tissue cohesion; tissue surface tensiometry; wetting

Indexed keywords

ALPHA5 INTEGRIN; ALPHA6 INTEGRIN; ALPHA9 BETA1 INTEGRIN; CADHERIN; DEXAMETHASONE; FIBRONECTIN; INTEGRIN; LAMININ; MYOSIN II; PROTEIN P53; TENASCIN; UNCLASSIFIED DRUG;

ADHERENT CELL; BRAIN TUMOR; CELL ADHESION; CELL MIGRATION; CELL MOTILITY; CELL SHAPE; ELASTICITY; EMBRYONAL TISSUE; ENDOTHELIUM CELL; GLIOBLASTOMA; GLIOMA CELL; HEART MUSCLE CONTRACTILITY; HUMAN; INTERCELLULAR SPACE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; REVIEW; SARCOMA CELL; STRESS FIBER; SURFACE TENSION; TISSUE LEVEL; TUMOR GROWTH; TUMOR MICROENVIRONMENT;

BRAIN NEOPLASMS; CELL ADHESION; CELL LINE, TUMOR; DISEASE-FREE SURVIVAL; EXTRACELLULAR MATRIX; GLIOBLASTOMA; HUMANS; INTEGRINS; MODELS, THEORETICAL; MOLECULAR TARGETED THERAPY; NEOPLASM RECURRENCE, LOCAL; NEOPLASM STAGING; PROGNOSIS;

EID: 84881301817     PISSN: 14796694     EISSN: 17448301     Source Type: Journal    
DOI: 10.2217/fon.13.66     Document Type: Review

References (81)

1. Dohrmann GJ, Farwell JR, Flannery JT. Glioblastoma multiforme in children. J. Neurosurg. 44 (4), 442-448 (1976).
2. Zada G, Bond AE, Wang YP, Giannotta SL, Deapen D. Incidence trends in the anatomic location of primary malignant brain tumors in the United States: 1992-2006. World Neurosurg. 77 (3-4), 518-524 (2012).
3. Verhaak RG, Hoadley KA, Purdom E et al. Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell 17 (1), 98-110 (2010).
4. Daumas-Duport C, Scheithauer B, O'Fallon J, Kelly P. Grading of astrocytomas. A simple and reproducible method. Cancer 62 (10), 2152-2165 (1988).
5. French LA, Galicich JH. The use of steroids for control of cerebral edema. Clin. Neurosurg. 10, 212-223 (1964).
6. Giese A, Westphal M. Glioma invasion in the central nervous system. Neurosurgery 39 (2), 235-250; discussion 250-232 (1996).
7. Thorne RG, Nicholson C. In vivo diffusion analysis with quantum dots and dextrans predicts the width of brain extracellular space. Proc. Natl Acad. Sci. USA 103 (14), 5567-5572 (2006).
8. Kwiatkowska A, Symons M. Signaling determinants of glioma cell invasion. Adv. Exp. Med. Biol. 986, 121-141 (2013).
9. Arismendi-Morillo G, Castellano A. Tumoral micro-blood vessels and vascular microenvironment in human astrocytic tumors. A transmission electron microscopy study. J. Neurooncol. 73 (3), 211-217 (2005).
10. Chamberlain MC, Cloughsey T, Reardon DA, Wen PY. A novel treatment for glioblastoma: Integrin inhibition. Expert Rev. Neurother. 12 (4), 421-435 (2012).
11. Yong RL, Lonser RR Surgery for glioblastoma multiforme: Striking a balance.World Neurosurg. 76 (6), 528-530 (2011).
12. Sanai N, Polley MY, Mcdermott MW, Parsa AT, Berger MS. An extent of resection threshold for newly diagnosed glioblastomas. J. Neurosurg. 115 (1), 3-8 (2011).
13. Markert J, Devita V, Hellman S, Rosenberg S. Glioblastoma Multiforme. Jones and Bartlett Publishers, MA, USA (2005).
14. Stupp R, Newlands E. New approaches for temozolomide therapy: Use in newly diagnosed glioma. Semin. Oncol. 28 (4 Suppl. 13), S19-S23 (2001).
15. Barker CA, Chang M, Chou JF et al. Radiotherapy and concomitant temozolomide may improve survival of elderly patients with glioblastoma. J. Neurooncol. 109 (2), 391-397 (2012).
16. Johnson DR, O'Neill BP. Glioblastoma survival in the United States before and during the temozolomide era. J. Neurooncol. 107 (2), 359-364 (2012).
17. Murat A, Migliavacca E, Gorlia T et al. Stem cell-related "self-renewal" signature and high epidermal growth factor receptor expression associated with resistance to concomitant chemoradiotherapy in glioblastoma. J. Clin. Oncol. 26 (18), 3015-3024 (2008).
18. Kunkel P, Ulbricht U, Bohlen P 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. 61 (18), 6624-6628 (2001).
19. Zuniga RM, Torcuator R, Jain R et al. Efficacy, safety and patterns of response and recurrence in patients with recurrent high-grade gliomas treated with bevacizumab plus irinotecan. J. Neurooncol. 91 (3), 329-336 (2009).
20. Paez-Ribes M, Allen E, Hudock J et al. Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis. Cancer Cell 15 (3), 220-231 (2009).
21. Desjardins A, Sampson JH. Avastin: More questions than answers. J. Neurosurg. 116 (2), 336-340; discussion 340 (2012).
22. Mcgirt MJ, Than KD, Weingart JD et al. Gliadel (BCNU) wafer plus concomitant temozolomide therapy after primary resection of glioblastoma multiforme. J. Neurosurg. 110 (3), 583-588 (2009).
23. De Bonis P, Anile C, Pompucci A et al. Safety and efficacy of gliadel wafers for newly diagnosed and recurrent glioblastoma. Acta Neurochir. 154 (8), 1371-1378 (2012).
24. Brandes AA, Tosoni A, Franceschi E, Reni M, Gatta G, Vecht C. Glioblastoma in adults. Crit. Rev. Oncol. Hematol. 67 (2), 139-152 (2008).
25. Wallner KE, Galicich JH, Krol G, Arbit E, Malkin MG. Patterns of failure following treatment for glioblastoma multiforme and anaplastic astrocytoma. Int. J. Radiat. Oncol. Biol. Phys. 16 (6), 1405-1409 (1989).
26. Clarke J, Butowski N, Chang S. Recent advances in therapy for glioblastoma. Arch. Neurol. 67 (3), 279-283 (2010).
27. Matsukado Y, Maccarty CS, Kernohan JW. The growth of glioblastoma multiforme (astrocytomas, grades 3 and 4) in neurosurgical practice. J. Neurosurg. 18, 636-644 (1961).
28. Sampetrean O, Saga I, Nakanishi M et al. Invasion precedes tumor mass formation in a malignant brain tumor model of genetically modified neural stem cells. Neoplasia 13 (9), 784-791 (2011).
29. Schnell O, Krebs B, Wagner E et al. Expression of integrin avb3 in gliomas correlates with tumor grade and is not restricted to tumor vasculature. Brain Pathol. 18 (3), 378-386 (2008).
30. Charles NA, Holland EC, Gilbertson R, Glass R, Kettenmann H. The brain tumor microenvironment. Glia 60 (3), 502-514 (2012).
31. Lathia JD, Gallagher J, Heddleston JM et al. Integrin a6 regulates glioblastoma stem cells. Cell Stem Cell 6 (5), 421-432 (2010).
32. Veeravalli KK, Ponnala S, Chetty C, Tsung AJ, Gujrati M, Rao JS. Integrin a9b1-mediated cell migration in glioblastoma via SSAT and Kir4.2 potassium channel pathway. Cell Signal. 24 (1), 272-281 (2012).
33. Martinkova E, Maglott A, Leger DY et al. a5b1 integrin antagonists reduce chemotherapy-induced premature senescence and facilitate apoptosis in human glioblastoma cells. Int. J. Cancer 127 (5), 1240-1248 (2010).
34. Tabatabai G, Weller M, Nabors B et al. Targeting integrins in malignant glioma. Targeted Oncol. 5 (3), 175-181 (2010).
35. Chintala SK, Sawaya R, Gokaslan ZL, Fuller G, Rao JS. Immunohistochemical localization of extracellular matrix proteins in human glioma, both in vivo and in vitro. Cancer Lett. 101 (1), 107-114 (1996).
36. Higuchi M, Ohnishi T, Arita N, Hiraga S, Hayakawa T. Expression of tenascin in human gliomas: Its relation to histological malignancy, tumor dedifferentiation and angiogenesis. Acta Neuropathol. 85 (5), 481-487 (1993).
37. Riemenschneider MJ, Mueller W, Betensky RA, Mohapatra G, Louis DN. In situ analysis of integrin and growth factor receptor signaling pathways in human glioblastomas suggests overlapping relationships with focal adhesion kinase activation. Am. J. Pathol. 167 (5), 1379-1387 (2005).
38. Wei KC, Huang CY, Chen PY et al. Evaluation of the prognostic value of CD44 in glioblastoma multiforme. Anticancer Res. 30 (1), 253-259 (2010).
39. Janouskova H, Maglott A, Leger DY et al. Integrin a5b1 plays a critical role in resistance to temozolomide by interfering with the p53 pathway in high-grade glioma. Cancer Res. 72 (14), 3463-3470 (2012).
40. Sengupta S, Nandi S, Hindi ES, Wainwright DA, Han Y, Lesniak MS. Short hairpin RNA-mediated fibronectin knockdown delays tumor growth in a mouse glioma model. Neoplasia 12 (10), 837-847 (2010).
41. Yamada S, Bu XY, Khankaldyyan V, Gonzales-Gomez I, McComb JG, Laug WE. Effect of the angiogenesis inhibitor cilengitide (EMD 121974) on glioblastoma growth in nude mice. Neurosurgery 59 (6), 1304-1312; discussion 1312 (2006).
42. Gilbert MR, Kuhn J, Lamborn KR et al. Cilengitide in patients with recurrent glioblastoma: The results of NABTC 03-02, a Phase II trial with measures of treatment delivery. J. Neurooncol. 106 (1), 147-153 (2012).
43. Nabors LB, Mikkelsen T, Hegi ME et al. A safety run-in and randomized Phase 2 study of cilengitide combined with chemoradiation for newly diagnosed glioblastoma (NABTT 0306). Cancer 118 (22), 5601-5607 (2012).
44. Foty RA, Corbett SA, Schwarzbauer JE, Steinberg MS. Dexamethasone up-regulates cadherin expression and cohesion of HT-1080 human fibrosarcoma cells. Cancer Res. 58 (16), 3586-3589 (1998).
45. Brenner KA, Corbett SA, Schwarzbauer JE. Regulation of fibronectin matrix assembly by activated Ras in transformed cells. Oncogene 19 (28), 3156-3163 (2000).
46. Foty RA, Forgacs G, Pfleger CM, Steinberg MS. Liquid properties of embryonic tissues: Measurement of interfacial tensions. Phys. Rev. Lett. 72 (14), 2298-2301 (1994).
47. Robinson EE, Zazzali KM, Corbett SA, Foty RA. a5b1 integrin mediates strong tissue cohesion. J. Cell Sci. 116 (Pt 2), 377-386 (2003).
48. Robinson EE, Foty RA, Corbett SA. Fibronectin matrix assembly regulates a5b1-mediated cell cohesion. Mol. Biol. Cell 15 (3), 973-981 (2004).
49. Jia D, Entersz I, Butler C, Foty RA. Fibronectin matrix-mediated cohesion suppresses invasion of prostate cancer cells. BMC Cancer 12, 94 (2012).
50. Sabari J, Lax D, Connors D et al. Fibronectin matrix assembly suppresses dispersal of glioblastoma cells. PLoS One 6 (9), e24810 (2011).
51. Steinberg MS. Adhesion in development: An historical overview. Dev. Biol. 180 (2), 377-388 (1996).
52. Foty RA, Pfleger CM, Forgacs G, Steinberg MS. Surface tensions of embryonic tissues predict their mutual envelopment behavior. Development 122 (5), 1611-1620 (1996).
53. Davies JT, Rideal EK. Interfacial Phenomena. Academic Press, NY, USA (1963).
54. Davis GS, Phillips HM, Steinberg MS. Germ-layer surface tensions and "tissue affinities" in Rana pipiens gastrulae: Quantitative measurements. Dev. Biol. 192 (2), 630-644 (1997).
55. Schotz EM, Burdine RD, Julicher F, Steinberg MS, Heisenberg CP, Foty RA. Quantitative differences in tissue surface tension influence zebrafish germ layer positioning. HFSP J. 2 (1), 42-56 (2008).
56. Schwarz MA, Zheng H, Legan S, Foty RA. Lung self-assembly is modulated by tissue surface tensions. Am. J. Respir. Cell Mol. Biol. 44 (5), 682-691 (2011).
57. Foty RA, Steinberg MS. The differential adhesion hypothesis: A direct evaluation. Dev. Biol. 278 (1), 255-263 (2005).
58. Foty RA, Steinberg MS. Measurement of tumor cell cohesion and suppression of invasion by E-or P-cadherin. Cancer Res. 57 (22), 5033-5036 (1997).
59. Winters BS, Shepard SR, Foty RA. Biophysical measurement of brain tumor cohesion. Int. J. Cancer 114 (3), 371-379 (2005).
60. Shafrin EG, Zisman WA. Constitutive relations in the wetting of low energy surfaces and the theory of the retraction method of preparing monolayers. J. Phys. Chem. 64 (5), 519-524 (1960).
61. Ryan PL, Foty RA, Kohn J, Steinberg MS. Tissue spreading on implantable substrates is a competitive outcome of cell-cell vs cell-substratum adhesivity. Proc. Natl Acad. Sci. USA 98 (8), 4323-4327 (2001).
62. Douezan S, Guevorkian K, Naouar R, Dufour S, Cuvelier D, Brochard-Wyart F. Spreading dynamics and wetting transition of cellular aggregates. Proc. Natl Acad. Sci. USA 108 (18), 7315-7320 (2011).
63. Utsuki S, Sato Y, Oka H, Tsuchiya B, Suzuki S, Fujii K. Relationship between the expression of E-, N-cadherins and b-catenin and tumor grade in astrocytomas. J. Neurooncol. 57 (3), 187-192 (2002).
64. Maret D, Gruzglin E, Sadr MS et al. Surface expression of precursor N-cadherin promotes tumor cell invasion. Neoplasia 12 (12), 1066-1080 (2010).
65. Cifarelli CP, Titus B, Yeoh HK. Cadherin-dependent adhesion of human U373MG glioblastoma cells promotes neurite outgrowth and increases migratory capacity. Laboratory investigation. J. Neurosurg. 114 (3), 663-669 (2011).
66. Tate CC, Garcia AJ, Laplaca MC. Plasma fibronectin is neuroprotective following traumatic brain injury. Exp. Neurol. 207 (1), 13-22 (2007).
67. Mckeown-Longo PJ, Mosher DF. Interaction of the 70,000-mol-wt amino-terminal fragment of fibronectin with the matrix-assembly receptor of fibroblasts. J. Cell Biol. 100 (2), 364-374 (1985).
68. Dimilla PA, Stone JA, Quinn JA, Albelda SM, Lauffenburger DA. Maximal migration of human smooth muscle cells on fibronectin and type IV collagen occurs at an intermediate attachment strength. J. Cell Biol. 122 (3), 729-737 (1993).
69. Lu P, Weaver VM, Werb Z. The extracellular matrix: A dynamic niche in cancer progression. J. Cell Biol. 196 (4), 395-406 (2012).
70. Paszek MJ, Zahir N, Johnson KR et al. Tensional homeostasis and the malignant phenotype. Cancer Cell 8 (3), 241-254 (2005).
71. Ulrich TA, De Juan Pardo EM, Kumar S. The mechanical rigidity of the extracellular matrix regulates the structure, motility, and proliferation of glioma cells. Cancer Res. 69 (10), 4167-4174 (2009).
72. Egeblad M, Rasch MG, Weaver VM. Dynamic interplay between the collagen scaffold and tumor evolution. Curr. Opin. Cell Biol. 22 (5), 697-706 (2010).
73. Pathak A, Kumar S. Biophysical regulation of tumor cell invasion: Moving beyond matrix stiffness. Integr. Biol. 3 (4), 267-278 (2011).
74. Pathak A, Kumar S. Independent regulation of tumor cell migration by matrix stiffness and confinement. Proc. Natl Acad. Sci. USA 109 (26), 10334-10339 (2012).
75. Wolf K, Wu YI, Liu Y et al. Multi-step pericellular proteolysis controls the transition from individual to collective cancer cell invasion. Nat. Cell Biol. 9 (8), 893-904 (2007).
76. Colbert MJ, Brochard-Wyart F, Fradin C, Dalnoki-Veress K. Squeezing and detachment of living cells. Biophys. J. 99 (11), 3555-3562 (2010).
77. Beadle C, Assanah MC, Monzo P, Vallee R, Rosenfeld SS, Canoll P. The role of myosin II in glioma invasion of the brain. Mol. Biol. Cell 19 (8), 3357-3368 (2008).
78. Kaal EC, Vecht CJ. The management of brain edema in brain tumors. Curr. Opin. Oncol. 16 (6), 593-600 (2004).
79. Manning ML, Foty RA, Steinberg MS, Schoetz EM. Coaction of intercellular adhesion and cortical tension specifies tissue surface tension. Proc. Natl Acad. Sci. USA 107 (28), 12517-12522 (2010).
80. Lin SH, Kleinberg LR. Carmustine wafers: Localized delivery of chemotherapeutic agents in CNS malignancies. Expert Rev. Anticancer Ther. 8 (3), 343-359 (2008).
81. Engler AJ, Sweeney HL, Discher DE, Schwarzbauer JE. Extracellular matrix elasticity directs stem cell differentiation. J. Musculoskelet. Neuronal Interact. 7 (4), 335 (2007).