Modeling putative therapeutic implications of exosome exchange between tumor and immune cells

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 40, 2014, Pages E4165-E4174

  Lu, Mingyang ^a   Huang, Bin ^a   Hanash, Samir M ^b   Onuchic, José N ^a   Ben Jacob, Eshel ^a,c  

^a RICE UNIVERSITY   (United States)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^c TEL AVIV UNIVERSITY   (Israel)

Author keywords

Cancer exosomes |; Cancer landscape |; Cancer therapy |; Computational modeling; Exosome communication|

Indexed keywords

ALGORITHM; ANIMAL; BIOLOGICAL MODEL; CELL COMMUNICATION; CYTOTOXIC T LYMPHOCYTE; DENDRITIC CELL; EXOSOME; GENETICS; HELPER CELL; HUMAN; IMMUNE SYSTEM; IMMUNITY; IMMUNOLOGY; METABOLISM; NATURAL KILLER CELL; NEOPLASM; PATHOLOGY; TUMOR MICROENVIRONMENT;

ALGORITHMS; ANIMALS; CELL COMMUNICATION; DENDRITIC CELLS; EXOSOMES; HUMANS; IMMUNE SYSTEM; IMMUNITY; KILLER CELLS, NATURAL; MODELS, IMMUNOLOGICAL; NEOPLASMS; T-LYMPHOCYTES, CYTOTOXIC; T-LYMPHOCYTES, HELPER-INDUCER; TUMOR MICROENVIRONMENT;

EID: 84907853282     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1416745111     Document Type: Article

References (72)

1. Schlom J (2012) Therapeutic cancer vaccines: Current status and moving forward. J Natl Cancer Inst 104(8):599-613.
2. Leach DR, Krummei MF, Allison JP (1996) Enhancement of antitumor immunity by CTLA-4 blockade. Science 271(5256):1734-1736.
3. Mougiakakos D, Choudhury A, Lladser A, Kiessling R, Johansson CC (2010) Advances in Cancer Research, eds Vande Woude GF, Klein G (Academic, New York), pp 57-117.
4. Sica A, Schioppa T, Mantovani A, Allavena P (2006) Tumour-associated macrophages are a distinct M2 polarised population promoting tumour progression: Potential targets of anti-cancer therapy. Eur J Cancer 42(6):717-727.
5. Bhatia A, Kumar Y (2011) Cancer-immune equilibrium: Questions unanswered. Cancer Microenviron 4(2):209-217.
6. Ben-Jacob E, Coffey DS, Levine H (2012) Bacterial survival strategies suggest rethinking cancer cooperativity. Trends Microbiol 20(9):403-410.
7. Vesely MD, Kershaw MH, Schreiber RD, Smyth MJ (2011) Natural innate and adaptive immunity to cancer. Annu Rev Immunol 29:235-271.
8. Igney FH, Krammer PH (2002) Immune escape of tumors: Apoptosis resistance and tumor counterattack. J Leukoc Biol 71 (6):907-920.
9. Hölzel M, Bovier A, Tüiting T (2013) Plasticity of tumour and immune cells: A source of heterogeneity and a cause for therapy resistance? Nat Rev Cancer 13(5):365-376.
10. Klimp AH, de Vries EGE, Scherphof GL, Daemen T (2002) A potential role of macrophage activation in the treatment of cancer. Crit Rev Oncol Hematol 44(2):143-161.
11. Smyth MJ, et al. (2000) Differential tumor surveillance by natural killer (NK) and NKT cells. J Exp Med 191(4):661-668.
12. Nagorsen D, Scheibenbogen C, Marincola FM, Letsch A, Keilholz U (2003) Natural T cell immunity against cancer. Clin Cancer Res 9(12):4296-4303.
13. Toes REM, Ossendorp F, Offringa R, Melief CJM (1999) CD4 T cells and their role in antitumor immune responses. J Exp Med 189(5):753-756.
14. Kuby J (1997) Immunology (Freeman, New York).
15. Banchereau J, Steinman RM (1998) Dendritic cells and the control of immunity. Nature 392(6673):245-252.
16. Barreira da Silva R, Münz C (2011) Natural killer cell activation by dendritic cells: Balancing inhibitory and activating signals. Cell Mol Life Sci 68(21):3505-3518.
17. Schroder K, Hertzog PJ, Ravasi T, Hume DA (2004) Interferon-γ: An overview of signals, mechanisms and functions. J Leukoc Biol 75(2):163-189.
18. Marusyk A, Almendro V, Polyak K (2012) Intra-tumour heterogeneity: A looking glass for cancer? Nat Rev Cancer 12(5):323-334.
19. Mueller MM, Fusenig NE (2004) Friends or foes: Bipolar effects of the tumour stroma in cancer. Nat Rev Cancer 4(11):839-849.
20. Holmes EC (1985) Immunology of tumor infiltrating lymphocytes. Ann Surg 201(2): 158-163.
21. Harper J, Sainson RCA (2014) Regulation of the anti-tumour immune response by cancer-associated fibroblasts. Semin Cancer Biol 25:69-77.
22. Vaupel P, Kallinowski F, Okunieff P (1989) Blood flow, oxygen and nutrient supply, and metabolic microenvironment of human tumors: A review. Cancer Res 49(23): 6449-6465.
23. Vaupel P, Kelleher DK, Höckel M (2001) Oxygen status of malignant tumors: Pathogenesis of hypoxia and significance for tumor therapy. Semin Oncol 28(2, Suppl 8): 29-35.
24. Munich S, Sobo-Vujanovic A, Buchser WJ, Beer-Stolz D, Vujanovic NL (2012) Dendritic cell exosomes directly kill tumor cells and activate natural killer cells via TNF superfamily ligands. Oncolmmunology 1(7): 1074-1083.
25. Marcus ME, Leonard JN (2013) FedExosomes: Engineering therapeutic biological nanoparticles that truly deliver. Pharmaceuticals (Basel) 6(5):659-680.
26. Février B, Raposo G (2004) Exosomes: Endosomal-derived vesicles shipping extracellular messages. Curr Opin Cell Biol 16(4):415-421.
27. Camussi G, et al. (2011) Exosome/microvesicle-mediated epigenetic reprogramming of cells. Am J Cancer Res 1(1):98-110.
28. Zhang H-G, Grizzle WE (2011) Exosomes and cancer: A newly described pathway of immune suppression. Clin Cancer Res 17(5):959-964.
29. Peinado H, et al. (2012) Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nat Med 18(6):883-891.
30. Viaud S, et al. (2009) Dendritic cell-derived exosomes promote natural killer cell activation and proliferation: A role for NKG2D ligands and IL-15Ralpha. PLoS ONE 4(3): e4942.
31. Matsumoto K, et al. (2004) Exosomes secreted from monocyte-derived dendritic cells support in vitro naive CD4+ T cell survival through NF-(K)B activation. Cell Immunol 231(1-2):20-29.
32. Hao S, et al. (2007) Mature dendritic cells pulsed with exosomes stimulate efficient cytotoxic T-lymphocyte responses and antitumour immunity. Immunology 120(1): 90-102.
33. Yu S, et al. (2007) Tumor exosomes inhibit differentiation of bone marrow dendritic cells. J Immunol 178(11):6867-6875.
34. Liu C, et al. (2006) Murine mammary carcinoma exosomes promote tumor growth by suppression of NK cell function. J Immunol 176(3):1375-1385.
35. Banasiak J, Chaplain MAJ, Miękisz J (2008) Multiscale Problems in the Life Sciences, eds Capasso V, Lachowicz M (Springer, Berlin).
36. Eftimie R, Bramson JL, Earn DJD (2011) Interactions between the immune system and cancer: A brief review of non-spatial mathematical models. Bull Math Biol 73(1):2-32.
37. Minelli A, Topputo F, Bernelli-Zazzera F (2011) Controlled drug delivery in cancer immunotherapy: Stability, optimization, and Monte Carlo analysis. SIAM J Appl Math 71:2229-2245.
38. Robertson-Tessi M, El-Kareh A, Goriely A (2012) A mathematical model of tumorimmune interactions. J Theor Biol 294:56-73.
39. Pappalardo F, Pennisi M, Ricupito A, Topputo F, Bellone M (2014) Induction of T-cell memory by a dendritic cell vaccine: A computational model. Bioinformatics 30(13): 1884-1891.
40. Wilkie KP, Hahnfeldt P (2013) Mathematical models of immune-induced cancer dormancy and the emergence of immune evasion. Interface Focus 3(4):20130010-20130010.
41. Rihan FA Abdel Rahman DH, Lakshmanan S, Alkhajeh AS (2014) A time delay model of tumour-immune system interactions: Global dynamics, parameter estimation, sensitivity analysis. Appl Math Comput 232:606-623.
42. Mehrian M, Asemani D, Arabameri A, Pourgholaminejad A, Hadjati J (2014) Modeling of tumor growth in dendritic cell-based immunotherapy using artificial neural networks. Comput Biol Chem 48:21-28.
43. Palsson S, et al. (2013) The development of a fully-integrated immune response model (FIRM) simulator of the immune response through integration of multiple subset models. BMC Syst Biol 7:95.
44. Lu M, et al. (2013) Tristability in cancer-associated microRNA-TF chimera toggle switch. J Phys Chem B 117(42):13164-13174.
45. Dunn GP, Bruce AT, Ikeda H, Old LJ, Schreiber RD (2002) Cancer immunoediting: From immunosurveillance to tumor escape. Nat Immunol 3(11):991-998.
46. Qu J-L, et al. (2009) Gastric cancer exosomes promote tumour cell proliferation through PI3K/Akt and MAPK/ERK activation. Dig Liver Dis 41 (12):875-880.
47. Gerosa F, et al. (2002) Reciprocal activating interaction between natural killer cells and dendritic cells. J Exp Med 195(3):327-333.
48. Vivier E, et al. (2011) Innate or adaptive immunity? The example of natural killer cells. Science 331 (6013):44-49.
49. Nelson BH (2010) CD20+ B cells: The other tumor-infiltrating lymphocytes. J Immunol 185(9):4977-4982.
50. Clayton A, Mitchell JP, Court J, Mason MD, Tabi Z (2007) Human tumor-derived exosomes selectively impair lymphocyte responses to interleukin-2. Cancer Res 67(15): 7458-7466.
51. Thomas DA, Massagué J (2005) TGF-beta directly targets cytotoxic T cell functions during tumor evasion of immune surveillance. Cancer Cell 8(5):369-380.
52. Hanke N, Alizadeh D, Katsanis E, Larmonier N (2013) Dendritic cell tumor killing activity and its potential applications in cancer immunotherapy. Crit Rev Immunol 33(1): 1-21.
53. Wolfers J, et al. (2001) Tumor-derived exosomes are a source of shared tumor rejection antigens for CTL cross-priming. Nat Med 7(3):297-303.
54. Menetrier-Caux C, et al. (1998) Inhibition of the differentiation of dendritic cells from CD34(+) progenitors by tumor cells: Role of interleukin-6 and macrophage colonystimulating factor. Blood 92(12):4778-4791.
55. Scarlett UK, et al. (2012) Ovarian cancer progression is controlled by phenotypic changes in dendritic cells. J Exp Med 209(3):495-506.
56. Wang J, Zhang K, Xu L, Wang E (2011) Quantifying the Waddington landscape and biological paths for development and differentiation. Proc Natl Acad Sci USA 108(20): 8257-8262.
57. Lu M, Onuchic J, Ben-Jacob E (2014) Construction of an effective landscape for multistate genetic switches. Phys Rev Lett 113(7):078102.
58. Formenti SC, Demaria S (2009) Systemic effects of local radiotherapy. Lancet Oncol 10(7):718-726.
59. Standish LJ, et al. (2008) Immune defects in breast cancer patients after radiotherapy. J Soc Integr Oncol 6(3):110-121.
60. Levy A, et al. (2013) Radiation therapy and immunotherapy: Implications for a combined cancer treatment. Crit Rev Oncol Hematol 85(3):278-287.
61. Gupta C, López JM, Ott W, Josic K, Bennett MR (2013) Transcriptional delay stabilizes bistable gene networks. Phys Rev Lett 111 (5):058104.
62. Lu M, Jolly MK, Levine H, Onuchic JN, Ben-Jacob E (2013) MicroRNA-based regulation of epithelial-hybrid-mesenchymal fate determination. Proc Natl Acad Sci USA 110(45): 18144-18149.
63. Li C, Wang J (2013) Quantifying cell fate decisions for differentiation and reprogramming of a human stem cell network: Landscape and biological paths. PLOS Comput Biol 9(8):e1003165.
64. Zhang B, Wolynes PG (2014) Stem cell differentiation as a many-body problem. Proc Natl Acad Sci USA 111 (28):10185-10190.
65. Huang S (2013) Hybrid T-helper cells: Stabilizing the moderate center in a polarized system. PLoS Biol 11(8):e1001632.
66. Maeurer MJ, et al. (1996) Tumor escape from immune recognition: Lethal recurrent melanoma in a patient associated with downregulation of the peptide transporter protein TAP-1 and loss of expression of the immunodominant MART-1/Melan-A antigen. J Clin Invest 98(7):1633-1641.
67. Uh S, et al. (1994) The effect of radiation therapy on immune function in patients with squamous cell lung carcinoma. Chest 105(1):132-137.
68. Quatromoni JG, Eruslanov E (2012) Tumor-associated macrophages: Function, phenotype, and link to prognosis in human lung cancer. Am J Transl Res 4(4):376-389.
69. Coventry BJ, et al. (2009) CRP identifies homeostatic immune oscillations in cancer patients: A potential treatment targeting tool? J Transi Med 7:102.
70. Heijer CD, Rheinboldt WC (1981) On steplength algorithms for a class of continuation methods. SIAM J Numer Anal 18:925-948.
71. Shampine LF, Thompson S (2001) Solving DDEs in MatLab. Appl Numer Math 37: 441-458.
72. Kloeden PE, Platen E (1992) Numerical Solution of Stochastic Differential Equations (Springer, Berlin).