How to escape the cancer attractor: Rationale and limitations of multi-target drugs

Seminars in Cancer Biology

Volumn 23, Issue 4, 2013, Pages 270-278

  Huang, Sui ^a,b   Kauffman, Stuart ^b,c  

^a INSTITUTE FOR SYSTEMS BIOLOGY   (United States)

^b UNIVERSITY OF CALGARY   (Canada)

^c UNIVERSITY OF VERMONT   (United States)

Author keywords

Cancer attractor; Epigenetic landscape; Gene regulatory network; Multi target therapy; Network dynamics

Indexed keywords

ANTINEOPLASTIC AGENT;

CANCER CELL; CANCER GROWTH; CANCER RESISTANCE; CELL SURVIVAL; COMPUTER MODEL; CONCEPTUAL FRAMEWORK; DRUG TARGETING; EPIGENETICS; GENE INTERACTION; GENE REGULATORY NETWORK; GENE SWITCHING; GENE TARGETING; GENETIC HETEROGENEITY; GENETIC STABILITY; HUMAN; MOLECULAR DYNAMICS; NONHUMAN; PHENOTYPIC PLASTICITY; REVIEW; SOMATIC MUTATION; STOCHASTIC MODEL; SYSTEMS BIOLOGY;

EID: 84881087888     PISSN: 1044579X     EISSN: 10963650     Source Type: Journal    
DOI: 10.1016/j.semcancer.2013.06.003     Document Type: Review

References (87)

1. Rosenzweig S.A. Acquired resistance to drugs targeting receptor tyrosine kinases. Biochem Pharmacol 2012, 8:1041-1048.
2. Mencher S.K., Wang L.G. Promiscuous drugs compared to selective drugs (promiscuity can be a virtue). BMC Clin Pharmacol 2005, 5:3.
3. Boran A.D., Iyengar R. Systems approaches to polypharmacology and drug discovery. Curr Opin Drug Discov Dev 2010, 1:297-309.
4. Maitland M.L., Hudoba C., Snider K.L., Ratain M.J. Analysis of the yield of phase II combination therapy trials in medical oncology. Clin Cancer Res 2010, 1:5296-5302.
5. Butcher E.C. Can cell systems biology rescue drug discovery?. Nat Rev Drug Discov 2005, 4:461-467.
6. Keith C.T., Borisy A.A., Stockwell B.R. Multicomponent therapeutics for networked systems. Nat Rev Drug Discov 2005, 4:71-78.
7. Hopkins A.L. Network pharmacology: the next paradigm in drug discovery. Nat Chem Biol 2008, 4:682-690.
8. Csermely P., Korcsmaros T., Kiss H.J., London G., Nussinov R. Structure and dynamics of molecular networks: a novel paradigm of drug discovery: a comprehensive review. Pharmacol Ther 2013, 13:333-408.
9. Huang S. Systems biology of stem cells: three useful perspectives to help overcome the paradigm of linear pathways. Philos Trans R Soc Lond B Biol Sci 2011, 36:2247-2259.
10. Huang S., Kauffman S. Complex gene regulatory networks - from structure to biological observables: cell fate determination. Encyclopedia of complexity and systems science 2009, 1180-1213. Springer. R.A. Meyers (Ed.).
11. Davidson E.H., Rast J.P., Oliveri P., Ransick A., Calestani C., Yuh C.H., et al. A genomic regulatory network for development. Science 2002, 29:1669-1678.
12. Cusick M.E., Klitgord N., Vidal M., Hill D.E. Interactome: gateway into systems biology. Hum Mol Genet 2005, 14(Spec No. 2):R171-R181.
13. Huang S. Rational drug discovery: what can we learn from regulatory networks?. Drug Discov Today 2002, 7:S163-S169.
14. Ramo P., Kesseli J., Yli-Harja O. Perturbation avalanches and criticality in gene regulatory networks. J Theor Biol 2006, 24:164-170.
15. Pierce G. Should we clean up the reputation of dirty drugs?. Can J Physiol Pharmacol 2012, 90:1333-1334.
16. Witt O., Lindemann R. HDAC inhibitors: magic bullets, dirty drugs or just another targeted therapy. Cancer Lett 2009, 28:123-124.
17. Machado F.S., Esper L., Dias A., Madan R., Gu Y., Hildeman D., et al. Native and aspirin-triggered lipoxins control innate immunity by inducing proteasomal degradation of TRAF6. J Exp Med 2008, 20:1077-1086.
18. Marimuthu S., Chivukula R.S., Alfonso L.F., Moridani M., Hagen F.K., Bhat G.J. Aspirin acetylates multiple cellular proteins in HCT-116 colon cancer cells: identification of novel targets. Int J Oncol 2011, 3:1273-1283.
19. Tegeder I., Pfeilschifter J., Geisslinger G. Cyclooxygenase-independent actions of cyclooxygenase inhibitors. FASEB J 2001, 1:2057-2072.
20. Esteller M. DNA methylation and cancer therapy: new developments and expectations. Curr Opin Oncol 2005, 1:55-60.
21. Ghoshal K., Bai S. DNA methyltransferases as targets for cancer therapy. Drugs Today 2007, 4:395-422.
22. Guo Y., Feng Y., Trivedi N.S., Huang S. Medusa structure of the gene regulatory network: dominance of transcription factors in cancer subtype classification. Exp Biol Med (Maywood) 2011, 23:628-636.
23. Huang S. On the intrinsic inevitability of cancer: from foetal to fatal attraction. Semin Cancer Biol 2011, 2:183-199.
24. Huang S., Ernberg I., Kauffman S. Cancer attractors: a systems view of tumors from a gene network dynamics and developmental perspective. Semin Cell Dev Biol 2009, 2:869-876.
25. Huang S. Non-genetic heterogeneity of cells in development: more than just noise. Development 2009, 13:3853-3862.
26. Altschuler S.J., Wu L.F. Cellular heterogeneity: do differences make a difference?. Cell 2010, 141:559-563.
27. Niepel M., Spencer S.L., Sorger P.K. Non-genetic cell-to-cell variability and the consequences for pharmacology. Curr Opin Chem Biol 2009, 1:556-561.
28. Dallas N.A., Xia L., Fan F., Gray M.J., Gaur P., van Buren G., et al. Chemoresistant colorectal cancer cells, the cancer stem cell phenotype, and increased sensitivity to insulin-like growth factor-I receptor inhibition. Cancer Res 2009, 69:1951-1957.
29. Tenbaum S.P., Ordonez-Moran P., Puig I., Chicote I., Arques O., Landolfi S., et al. Beta-catenin confers resistance to PI3K and AKT inhibitors and subverts FOXO3a to promote metastasis in colon cancer. Nat Med 2012, 1:892-901.
30. Jhawer M., Goel S., Wilson A.J., Montagna C., Ling Y.H., Byun D.S., et al. PIK3CA mutation/PTEN expression status predicts response of colon cancer cells to the epidermal growth factor receptor inhibitor cetuximab. Cancer Res 2008, 6:1953-1961.
31. La Rosee P., Deininger M.W. Resistance to imatinib: mutations and beyond. Semin Hematol 2010, 4:335-343.
32. Wilson T.R., Fridlyand J., Yan Y., Penuel E., Burton L., Chan E., et al. Widespread potential for growth-factor-driven resistance to anticancer kinase inhibitors. Nature 2012, 48:505-509.
33. Barouch-Bentov R., Sauer K. Mechanisms of drug resistance in kinases. Exp Opin Investig Drugs 2011, 2:153-208.
34. Sawyers C.L. The 2011 Gordon Wilson lecture: overcoming resistance to targeted cancer drugs. Trans Am Clin Climatol Assoc 2012, 123:114-123. discussion 23-5.
35. Tang J., Salama R., Gadgeel S.M., Sarkar F.H., Ahmad A. Erlotinib resistance in lung cancer: current progress and future perspectives. Front Pharmacol 2013, 4:15.
36. Galhardo R.S., Hastings P.J., Rosenberg S.M. Mutation as a stress response and the regulation of evolvability. Crit Rev Biochem Mol Biol 2007, 4:399-435.
37. Brock A., Chang H., Huang S. Non-genetic heterogeneity - a mutation-independent driving force for the somatic evolution of tumours. Nat Rev Genet 2009, 1:336-342.
38. Yang A.D., Fan F., Camp E.R., van Buren G., Liu W., Somcio R., et al. Chronic oxaliplatin resistance induces epithelial-to-mesenchymal transition in colorectal cancer cell lines. Clin Cancer Res 2006, 1:4147-4153.
39. Hu X., Ghisolfi L., Keates A.C., Zhang J., Xiang S., Lee D.K., et al. Induction of cancer cell stemness by chemotherapy. Cell Cycle 2012, 1:2691-2698.
40. Iyer R., Lehnert B.E. Low dose, low-LET ionizing radiation-induced radioadaptation and associated early responses in unirradiated cells. Mutat Res 2002, 50:1-9.
41. Lee G.Y., Shim J.S., Cho B., Jung J.Y., Lee D.S., Oh I.H. Stochastic acquisition of a stem cell-like state and drug tolerance in leukemia cells stressed by radiation. Int J Hematol 2011, 9:27-35.
42. Lambert G., Estevez-Salmeron L., Oh S., Liao D., Emerson B.M., Tlsty T.D., et al. An analogy between the evolution of drug resistance in bacterial communities and malignant tissues. Nat Rev Cancer 2011, 1:375-382.
43. Sun Y., Nelson P.S. Molecular pathways: involving microenvironment damage responses in cancer therapy resistance. Clin Cancer Res 2012, 1:4019-4025.
44. Landsberg J., Kohlmeyer J., Renn M., Bald T., Rogava M., Cron M., et al. Melanomas resist T-cell therapy through inflammation-induced reversible dedifferentiation. Nature 2012, 49:412-416.
45. Gilbert L.A., Hemann M.T. DNA damage-mediated induction of a chemoresistant niche. Cell 2010, 14:355-366.
46. Yildirim M.A., Goh K.I., Cusick M.E., Barabasi A.L., Vidal M. Drug-target network. Nat Biotechnol 2007, 2:1119-1126.
47. Huang S. The molecular and mathematical basis of Waddington's epigenetic landscape: a framework for post-Darwinian biology. Bioessays 2012, 3:149-155.
48. Huang S., Ingber D.E. Shape-dependent control of cell growth, differentiation, and apoptosis: switching between attractors in cell regulatory networks. Exp Cell Res 2000, 26:91-103.
49. Albert R., Jeong H., Barabasi A.L. Error and attack tolerance of complex networks. Nature 2000, 40:378-382.
50. Joy M.P., Brock A., Ingber D.E., Huang S. High-betweenness proteins in the yeast protein interaction network. J Biomed Biotechnol 2005, 200:96-103.
51. Iyer S., Killingback T., Sundaram B., Wang Z. Attack robustness and centrality of complex networks. PLoS ONE 2013, 8:e59613.
52. Coelho E.D., Arrais J.P., Oliveira J.L. From protein-protein interactions to rational drug design: are computational methods up to the challenge?. Curr Top Med Chem 2013, 13:602-618.
53. Zwaka T.P. Pluripotency network in embryonic stem cells: maybe Leibniz was right all along. Cell Stem Cell 2012, 1:441-442.
54. Aubin D. Forms of explanations in the catastrophe theory of René Thom: topology, morphogenesis, and structuralism. Growing explanations: historical perspective on the sciences of complexity 2004, 95-130. Duke University Press, Durham. M.N. Wise (Ed.).
55. Thomas R. Logical analysis of systems comprising feedback loops. J Theor Biol 1978, 7:631-656.
56. Delbrück M. Discussion Unités biologiques douées de continuité génétique Colloques Internationaux du Centre National de la Recherche Scientifique 1949, 33-35. CNRS, Paris.
57. Waddington C.H. Principles of embryology 1956, Allen & Unwin Ltd., London.
58. Monod J., Jacob F. Teleonomic mechanisms in cellular metabolism, growth, and differentiation. Cold Spring Harb Symp Quant Biol 1961, 2:389-401.
59. Kauffman S. Homeostasis and differentiation in random genetic control networks. Nature 1969, 22:177-178.
60. Bar-Yam Y., Epstein I.R. Response of complex networks to stimuli. Proc Natl Acad Sci USA 2004, 10:4341-4345.
61. Huang S. Reprogramming cell fates: reconciling rarity with robustness. Bioessays 2009, 3:546-560.
62. Huang S. Cell lineage determination in state space: a systems view brings flexibility to dogmatic canonical rules. PLoS Biol 2010, 8:e1000380.
63. Kashiwagi A., Urabe I., Kaneko K., Yomo T. Adaptive response of a gene network to environmental changes by fitness-induced attractor selection. PLoS ONE 2006, 1:e49.
64. Raj A., van Oudenaarden A. Nature, nurture, or chance: stochastic gene expression and its consequences. Cell 2008, 13:216-226.
65. Eldar A., Elowitz M.B. Functional roles for noise in genetic circuits. Nature 2010, 46:167-173.
66. Chang H.H., Hemberg M., Barahona M., Ingber D.E., Huang S. Transcriptome-wide noise controls lineage choice in mammalian progenitor cells. Nature 2008, 45:544-547.
67. Pina C., Fugazza C., Tipping A.J., Brown J., Soneji S., Teles J., et al. Inferring rules of lineage commitment in haematopoiesis. Nat Cell Biol 2012, 1:287-294.
68. Kauffman S. Differentiation of malignant to benign cells. J Theor Biol 1971, 3:429-451.
69. McCullough K.D., Coleman W.B., Ricketts S.L., Wilson J.W., Smith G.J., Grisham J.W. Plasticity of the neoplastic phenotype in vivo is regulated by epigenetic factors. Proc Natl Acad Sci USA 1998, 9:15333-15338.
70. Rubin H. What keeps cells in tissues behaving normally in the face of myriad mutations?. Bioessays 2006, 28:515-524.
71. Lang J.Y., Shi Y., Chin Y.E. Reprogramming cancer cells: back to the future. Oncogene 2013, 3:2247-2248.
72. Zhang X., Cruz F.D., Terry M., Remotti F., Matushansky I. Terminal differentiation and loss of tumorigenicity of human cancers via pluripotency-based reprogramming. Oncogene 2013, 3:2249-2260.
73. Aurell E., Sneppen K. Epigenetics as a first exit problem. Phys Rev Lett 2002, 88:048101.
74. Slack J.M.W. Timeline - Conrad Hal Waddington: the last renaissance biologist?. Nat Rev Genet 2002, 3:889-895.
75. Waddington C.H. The strategy of the genes 1957, Allen and Unwin, London.
76. Nicolis G., Prigogine I. Exploring complexity: an introduction 1989, W.H. Freeman & Company, San Francisco.
77. Zhou J.X., Aliyu M.D., Aurell E., Huang S. Quasi-potential landscape in complex multi-stable systems. J R Soc Interface 2012, 9:3539-3553.
78. Freidlin M., Wentzell A. Random perturbations of dynamical system 1984, Springer-Verlag, New York.
79. Paquette R.L., Koeffler H.P. Differentiation therapy. Hematol Oncol Clin North Am 1992, 6:687-706.
80. Nakamaki T., Sakashita A., Hino K., Suzuki K., Tomoyasu S., Tsuruoka N., et al. Difference in effects of interferon-alpha and interferon-gamma on the induction of differentiation of retinoic acid-treated acute myeloid leukemia cells in primary culture. Leukemia Res 1990, 1:785-794.
81. Kawamata H., Tachibana M., Fujimori T., Imai Y. Differentiation-inducing therapy for solid tumors. Curr Pharm Des 2006, 1:379-385.
82. Lee M.J., Ye A.S., Gardino A.K., Heijink A.M., Sorger P.K., MacBeath G., et al. Sequential application of anticancer drugs enhances cell death by rewiring apoptotic signaling networks. Cell 2012, 14:780-794.
83. Hampton T. "Promiscuous" anticancer drugs that hit multiple targets may thwart resistance. J Am Med Assoc 2004, 29:419-422.
84. Hashimshony T., Wagner F., Sher N., Yanai I. CEL-Seq: single-cell RNA-seq by multiplexed linear amplification. Cell Rep 2012, 2:666-673.
85. Kurimoto K., Yabuta Y., Ohinata Y., Saitou M. Global single-cell cDNA amplification to provide a template for representative high-density oligonucleotide microarray analysis. Nat Protoc 2007, 2:739-752.
86. Levsky J.M., Shenoy S.M., Pezo R.C., Singer R.H. Single-cell gene expression profiling. Science 2002, 29:836-840.
87. Technologies L. Using single-cell analysis to identify subpopulations. BioTechniques 2011, 5:278-279.