Multiscale Modeling of Glioblastoma Suggests that the Partial Disruption of Vessel/Cancer Stem Cell Crosstalk Can Promote Tumor Regression Without Increasing Invasiveness

IEEE Transactions on Biomedical Engineering

Volumn 64, Issue 3, 2017, Pages 538-548

  Yan, Huaming ^a   Romero Lopez, Monica ^a   Frieboes, Hermann B ^b   Hughes, Christopher C W ^c   Lowengrub, John S ^c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b University of Louisville   (United States)

^c University of California at Irvine   (United States)

Author keywords

Brain tumors; cancer stem cells; cancer therapies; feedback regulation; mathematical model

Indexed keywords

CELL ENGINEERING; CELLS; CROSSTALK; CYTOLOGY; DISEASES; ENDOTHELIAL CELLS; MATHEMATICAL MODELS; ONCOLOGY; PHYSIOLOGY; STEM CELLS;

ANTI-ANGIOGENIC THERAPY; BRAIN TUMORS; CANCER STEM CELLS; CANCER THERAPY; FEEDBACK REGULATION; MULTI-SCALE MODELING; VASCULAR ENDOTHELIAL CELLS; VASCULAR ENDOTHELIAL GROWTH FACTOR;

TUMORS;

VASCULOTROPIN; VASCULOTROPIN A;

ANGIOGENESIS; ANTIANGIOGENIC THERAPY; APOPTOSIS; ARTICLE; CANCER STEM CELL; CELL MOTION; CELL PROLIFERATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEEDBACK SYSTEM; GLIOBLASTOMA; HUMAN; HUMAN CELL; MATHEMATICAL MODEL; MITOSIS RATE; NUTRIENT CONCENTRATION; TUMOR GROWTH; TUMOR REGRESSION; TUMOR VOLUME; VASCULAR ENDOTHELIAL CELL; ANIMAL; BIOLOGICAL MODEL; CELL COMMUNICATION; CELL SURVIVAL; COMPUTER SIMULATION; ENDOTHELIUM CELL; METABOLISM; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY; PATHOPHYSIOLOGY; SIGNAL TRANSDUCTION; TUMOR INVASION;

ANIMALS; CELL COMMUNICATION; CELL PROLIFERATION; CELL SURVIVAL; COMPUTER SIMULATION; ENDOTHELIAL CELLS; GLIOBLASTOMA; HUMANS; MODELS, BIOLOGICAL; NEOPLASM INVASIVENESS; NEOPLASM REGRESSION, SPONTANEOUS; NEOPLASTIC STEM CELLS; NEOVASCULARIZATION, PATHOLOGIC; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 85013422768     PISSN: 00189294     EISSN: 15582531     Source Type: Journal    
DOI: 10.1109/TBME.2016.2615566     Document Type: Article

References (80)

1. T. R. Alves et al., "Glioblastoma cells: A heterogeneous and fatal tumor interacting with the parenchyma, " Life Sci., vol. 89, nos. 15/16, pp. 532-539, 2011.
2. A. R. Anderson andM. A. Chaplain, "Continuous and discrete mathematical models of tumor-induced angiogenesis, " Bull. Math. Biol., vol. 60, no. 5 pp. 857-899, 1998.
3. H. G. Augustin, "Tubes, branches, and pillars: The many ways of forming a new vasculature, " Circulation Res., vol. 89, no. 8, pp. 645-647, 2001.
4. J. M. Bailey et al., "Cancer metastasis facilitated by developmental pathways: Sonic hedgehog, Notch, and bone morphogenic proteins, " J. Cell Biochem., vol. 102, no. 4, pp. 829-839, 2007.
5. S. Bao et al., "Stem cell-like glioma cells promote tumor angiogenesis through vascular endothelial growth factor, " Cancer Res., vol. 66, no. 16, pp. 7843-7848, 2006.
6. N. S. Bayin et al., "Glioblastoma stem cells:Molecular characteristics and therapeutic implications, " World J. Stem Cells, vol. 6, no. 2, pp. 230-238, 2014.
7. E. L. Bearer et al., "Multiparameter computational modeling of tumor invasion, " Cancer Res., vol. 69, no. 10, pp. 4493-4501, 2009.
8. L. Bello et al., "Combinatorial administration of molecules that simultaneously inhibit angiogenesis and invasion leads to increased therapeutic efficacy inmousemodels of malignant glioma, " Clin. Cancer Res., vol. 10, no. 13, pp. 4527-4537, 2004.
9. R. Bonavia et al., "Heterogeneity maintenance in glioblastoma: A social network, " Cancer Res., vol. 71, no. 12, pp. 4055-4060, 2011.
10. E. Bullitt, et al., "Vessel tortuosity and brain tumor malignancy: A blinded study, " Acad. Radiol., vol. 12, no. 10, pp. 1232-1240, 2005.
11. C. Calabrese et al., "A perivascular niche for brain tumor stem cells, " Cancer Cell, vol. 11, no. 1, pp. 69-82, 2007.
12. O. Casanovas et al., "Drug resistance by evasion of antiangiogenic targeting of VEGF signaling in late-stage pancreatic islet tumors, " Cancer Cell, vol. 8, no. 4, pp. 299-309, 2005.
13. N. Charles et al., "Perivascular nitric oxide activates notch signaling and promotes stem-like character in PDGF-induced glioma cells, " Cell Stem Cell, vol. 6, no. 2, pp. 141-152, 2010.
14. R. Chen et al., "A hierarchy of self-renewing tumor-initiating cell types in glioblastoma, " Cancer Cell, vol. 17, no. 4, pp. 362-375, 2010.
15. L. Cheng et al., "Elevated invasive potential of glioblastoma stem cells, " Biochem. Biophys. Res. Commun., vol. 406, no. 4, pp. 643-648, 2011.
16. J. Clarke et al., "Recent advances in therapy for glioblastoma, " Arch. Neurol., vol. 67, no. 3, pp. 279-283, 2010.
17. V. Cristini et al., "Morphologic instability and cancer invasion, " Clin. Cancer Res., vol. 11, no. 19 Pt 1, pp. 6772-6779, 2005.
18. V. Cristini et al., "Nonlinear simulation of tumor growth, " J. Math. Biol., vol. 46, no. 3, pp. 191-224, 2003.
19. V. Cristini and J. S. Lowengrub, Multiscale Modeling of Cancer: An Integrated Experimental and Mathematical Modeling Approach. Cambridge, U.K.: Cambridge Univ. Press, 2010.
20. J. F. de Groot et al., "Tumor invasion after treatment of glioblastoma with bevacizumab: Radiographic and pathologic correlation in humans and mice, " Neuro Oncol., vol. 12, no. 3, pp. 233-42, 2010.
21. A. Dimberg, "The glioblastoma vasculature as a target for cancer therapy, " Biochem. Soc. Trans., vol. 42, no. 6, pp. 1647-1652, 2014.
22. C. E. Eyler et al., "Glioma stem cell proliferation and tumor growth are promoted by nitric oxide synthase-2, " Cell, vol. 146, no. 1, pp. 53-66, 2011.
23. C. E. Eyler and J. N. Rich, "Survival of the fittest: Cancer stem cells in therapeutic resistance and angiogenesis, " J. Clin. Oncol., vol. 26, no. 17, pp. 2839-2845, 2008.
24. X. Fan et al., "NOTCH pathway blockade depletes CD133-positive glioblastoma cells and inhibits growth of tumor neurospheres and xenografts, " Stem Cells, vol. 28, no. 1, pp. 5-16, 2010.
25. C. Folkins et al., "Anticancer therapies combining antiangiogenic and tumor cell cytotoxic effects reduce the tumor stem-like cell fraction in glioma xenograft tumors, " Cancer Res., vol. 67, no. 8, pp. 3560-3564, 2007.
26. C. Folkins et al., "Glioma tumor stem-like cells promote tumor angiogenesis and vasculogenesis via vascular endothelial growth factor and stromal-derived factor 1, " Cancer Res., vol. 69, no. 18, pp. 7243-7251, 2009.
27. J. Folkman, "Incipient angiogenesis, " J. Nat. Cancer Inst., vol. 92, no. 2, pp. 94-95, 2000.
28. H. B. Frieboes et al., "Three-dimensional multispecies nonlinear tumor growth-II: Tumor invasion and angiogenesis, " J. Theor. Biol., vol. 264, no. 4, pp. 1254-1278, 2010.
29. H. B. Frieboes et al., "Computer simulation of glioma growth and morphology, " Neuroimage, vol. 37 Suppl 1, pp. S59-S70, 2007.
30. E. M. Galan-Moya et al., "Secreted factors from brain endothelial cells maintain glioblastoma stem-like cell expansion through the mTOR pathway, " EMBO Rep., vol. 12, no. 5, pp. 470-476, 2011.
31. X. Gao et al., "Acute and fractionated irradiation differentially modulate glioma stem cell division kinetics, " Cancer Res., vol. 73, no. 5, pp. 1481-1490, 2013.
32. X. Gao et al., "A proposed quantitative index for assessing the potential contribution of reprogramming to cancer stem cell kinetics, " Stem Cells Int., vol. 2014, 2014, Art. no. 249309.
33. R. J. Gilbertson and J. N. Rich, "Making a tumours bed: Glioblastoma stem cells and the vascular niche, " Nat. Rev. Cancer, vol. 7, no. 10, pp. 733-736, 2007.
34. A. C. Girvan et al., "Glioblastoma treatment patterns, survival, and healthcare resource use in real-world clinical practice in the USA, " Drugs Context, vol. 4, 2015, Art. no. 212274.
35. C. A. Gregory et al., "TheWNT signaling inhibitor dickkopf-1 is required for reentry into the cell cycle of human adult stem cells from bone marrow, " J. Biol. Chem., vol. 278, no. 30, pp. 28067-28078, 2003.
36. H. Rieger, T. Fredrich, and M. Welter, "Physics of the tumor vasculature: Theory and experiment, " Eur. Phys. J. Plus, vol. 131, 2016, Art. no. 31.
37. N. Hartung et al., "Mathematical modeling of tumor growth andmetastatic spreading:Validation in tumor-bearingmice, " Cancer Res., vol. 74, no. 22, pp. 6397-6407, 2014.
38. M. A. Herve et al., "Overexpression of vascular endothelial growth factor 189 in breast cancer cells leads to delayed tumor uptake with dilated intratumoral vessels, " Amer. J. Pathol., vol. 172, no. 1, pp. 167-178, 2008.
39. J. Holash et al., "Vessel cooption, regression, and growth in tumors mediated by angiopoietins and VEGF, " Science, vol. 284, no. 5422, pp. 1994-1998, 1999.
40. K. E. Hovinga et al., "Inhibition of notch signaling in glioblastoma targets cancer stem cells via an endothelial cell intermediate, " Stem Cells, vol. 28, no. 6, pp. 1019-1029, 2010.
41. F. M. Iwamoto et al., Patterns of relapse and prognosis after bevacizumab failure in recurrent glioblastoma, " Neurology, vol. 73, no. 15, pp. 1200-1206, 2009.
42. R. K. Jain, "Molecular regulation of vessel maturation, " Nature Med., vol. 9, no. 6, pp. 685-693, 2003.
43. J. V. Joseph et al., "Hypoxia enhances migration and invasion in glioblastoma by promoting a mesenchymal shift mediated by theHIF1alpha-ZEB1 axis, " Cancer Lett., vol. 359, no. 1, pp. 107-116, 2015.
44. A. Klaus and W. Birchmeier, "Wnt signalling and its impact on development and cancer, " Nature Rev. Cancer, vol. 8, no. 5, pp. 387-398, 2008.
45. P. Kunkel 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., vol. 61, no. 18, pp. 6624-6628, 2001.
46. A. D. Lander et al., "Cell lineages and the logic of proliferative control, " PLOS Biol., vol. 7, no. 1, 2009, Art. no. 1000015.
47. W. Lederle et al., "Platelet-derived growth factor-B normalizes micromorphology and vessel function in vascular endothelial growth factor-A-induced squamous cell carcinomas, " Amer. J. Pathol., vol. 176, no. 2, pp. 981-994, 2010.
48. E. Lee et al., "Crosstalk between cancer cells and blood endothelial and lymphatic endothelial cells in tumour and organ microenvironment, " Expert Rev. Mol. Med., vol. 17, p. e3, 2015.
49. N. Lee et al., "A potential role for Dkk-1 in the pathogenesis of osteosarcoma predicts novel diagnostic and treatment strategies, " Brit. J. Cancer, vol. 97, no. 11, pp. 1552-1559, 2007.
50. Z. Li et al., "Hypoxia-inducible factors regulate tumorigenic capacity of glioma stem cells, " Cancer Cell, vol. 15, no. 6, pp. 501-513, 2009.
51. K. L. Ligon et al., "Olig2-regulated lineage-restricted pathway controls replication competence in neural stem cells and malignant glioma, " Neuron, vol. 53, no. 4, pp. 503-517, 2007.
52. S. J. Lunt et al., "Interstitial fluid pressure in tumors: Therapeutic barrier and biomarker of angiogenesis, " Future Oncol., vol. 4, no. 6, pp. 793-802, 2008.
53. S. R. McDougall et al., "Mathematical modelling of flow through vascular networks: Implications for tumour-induced angiogenesis and chemotherapy strategies, " Bull. Math. Biol., vol. 64, no. 4, pp. 673-702, 2002.
54. A. A. Merchant and W. Matsui, "Targeting Hedgehog-A cancer stem cell pathway, " Clin. Cancer Res., vol. 16, no. 12, pp. 3130-3140, 2010.
55. A. Minchenko et al., "Hypoxic stimulation of vascular endothelial growth factor expression in vitro and in vivo, " Lab Invest., vol. 71, no. 3, pp. 374-379, 1994.
56. N. Oka et al., "VEGF promotes tumorigenesis and angiogenesis of human glioblastoma stem cells, " Biochem. Biophys. Res. Commun., vol. 360, no. 3, pp. 553-559, 2007.
57. M. Paez-Ribes et al., "Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis, " Cancer Cell, vol. 15, no. 3, pp. 220-231, 2009.
58. K. Pham et al., "Predictions of tumour morphological stability and evaluation against experimental observations, " J. Roy. Soc. Interface, vol. 8, no. 54, pp. 16-29, 2011.
59. S. G. Piccirillo et al., "Bone morphogenetic proteins inhibit the tumorigenic potential of human brain tumour-initiating cells, " Nature, vol. 444, no. 7120, pp. 761-765, 2006.
60. F. Pistollato et al., "Intratumoral hypoxic gradient drives stem cells distribution and MGMT expression in glioblastoma, " Stem Cells, vol. 28, no. 5, pp. 851-862, 2010.
61. C. Raḿirez-Castillejo et al., "Pigment epithelium-derived factor is a niche signal for neural stem cell renewal, " Nature Neurosci., vol. 9, no. 3, pp. 331-339, 2006.
62. M. Robertson-Tessi et al., "Impact of metabolic heterogeneity on tumor growth, invasion, and treatment outcomes, " Cancer Res., vol. 75, no. 8, pp. 1567-1579, 2015.
63. A. Saaristo et al., "Adenoviral VEGF-C overexpression induces blood vessel enlargement, tortuosity, and leakiness but no sprouting angiogenesis in the skin or mucous membranes, " FASEB J., vol. 16, no. 9, pp. 1041-1049, 2002.
64. A. Sharma and A. Shiras, "Cancer stem cell-vascular endothelial cell interactions in glioblastoma, " Biochem. Biophys. Res. Commun., vol. 473, no. 3, pp. 688-692, 2016.
65. Q. Shen et al., "Endothelial cells stimulate self-renewal and expand neurogenesis of neural stem cells, " Science, vol. 304, no. 5675, pp. 1338-1340, 2004.
66. T. G. Simonsen et al., "High interstitial fluid pressure is associated with tumor-line specific vascular abnormalities in human melanoma xenografts, " PLOS ONE, vol. 7, no. 6, 2012, Art. no. 0040006.
67. A. Sottoriva et al., "Cancer stem cell tumor model reveals invasive morphology and increased phenotypical heterogeneity, " Cancer Res., vol. 70, no. 1, pp. 46-56, 2010.
68. G. Tabatabai and M. Weller, "Glioblastoma stem cells, " Cell Tissue Res., vol. 343, no. 3, pp. 459-465, 2011.
69. S. Takano et al., "Concentration of vascular endothelial growth factor in the serum and tumor tissue of brain tumor patients, " Cancer Res., vol. 56, no. 9, pp. 2185-2190, 1996.
70. M. Tavazoie et al., "A specialized vascular niche for adult neural stem cells, " Cell Stem Cell, vol. 3, no. 3, pp. 279-288, 2008.
71. E. Vlashi et al., "In vivo imaging, tracking, and targeting of cancer stem cells, " J. Nat. Cancer Inst., vol. 101, no. 5, pp. 350-359, 2009.
72. T. A. Wilson et al., "Glioblastoma multiforme: State of the art and future therapeutics, " Surg. Neurol. Int., vol. 5, p. 64, 2014.
73. S. M. Wise et al., "An adaptive multigrid algorithm for simulating solid tumor growth using mixture models, " Math. Comput. Model, vol. 53, nos. 1/2, pp. 1-20, 2011.
74. S. M. Wise et al., "Three-dimensional multispecies nonlinear tumor growth-I Model and numerical method, " J. Theor. Biol., vol. 253, no. 3, pp. 524-543, 2008.
75. X. Zhu et al., "Predicting simulation parameters of biological systems using a Gaussian process model, " Statist. Anal. Data Mining, vol. 5, no. 6, pp. 509-522, 2012.
76. G. N. Yan et al., "Endothelial cells promote stem-like phenotype of glioma cells through activating the Hedgehog pathway, " J. Pathol., vol. 234, no. 1, pp. 11-22, 2014.
77. J. Ye et al., "The cancer stem cell niche: Cross talk between cancer stem cells and their microenvironment, " Tumour Biol., vol. 35, no. 5, pp. 3945-3951, 2014.
78. H. Youssefpour et al., "Multispecies model of cell lineages and feedback control in solid tumors, " J. Theor. Biol., vol. 304, pp. 39-59, 2012.
79. Q. Zeng et al., "Crosstalk between tumor and endothelial cells promotes tumor angiogenesis by MAPK activation of Notch signaling, " Cancer Cell, vol. 8, no. 1, pp. 13-23, 2005.
80. T. S. Zhu et al., "Endothelial cells create a stem cell niche in glioblastoma by providing Notch ligands that nurture self-renewal of cancer stem-like cells, " Cancer Res., vol. 71, no. 18, pp. 6061-6072, 2011.