Skip to main content
SpringerLink
Log in

Tensegrity, Dynamic Networks, and Complex Systems Biology: Emergence in Structural and Information Networks Within Living Cells

  • Chapter
Complex Systems Science in Biomedicine

Abstract

The genomic revolution has led to the systematic characterization of all the genes of the genome and the proteins they encode. But we still do not fully understand how many cell behaviors are controlled, because many important biological properties of cells emerge at the whole-system level from the collective action of thousands of molecular components, which is orchestrated through specific regulatory interactions. In this chapter we present two distinct approaches based on the concept of molecular networks to understand two fundamental system properties of living cells: their ability to maintain their shape and mechanical stability, and their ability to express stable, discrete cell phenotypes and switch between them. We first describe how structural networks built using the principles of tensegrity architecture and computational models that incorporate these features can predict many of the complex mechanical behaviors that are exhibited by living mammalian cells. We then discuss how genome-wide biochemical signaling networks produce “attractor” states that may represent the stable cell phenotypes, such as growth, differentiation, and apoptosis, and which explain how cells can make discrete cell fate decisions in the presence of multiple conflicting signals. These network-based concepts help to bridge the apparent gap between emergent system features characteristic of living cells and the underlying molecular processes.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 259.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 329.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 329.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

7. References

  1. Aldana M, Cluzel P. 2003. A natural class of robust networks. Proc Natl Acad Sci USA 100:8710–8714.

    Article  PubMed  CAS  Google Scholar 

  2. Bar-Yam Y. 1997. Dynamics in complex systems. Studies in Nonlinearity. Perseus Publishing, Reading, MA.

    Google Scholar 

  3. Bogomolova EV. 2001. Isopropyl alcohol induced mycelium formation in lithobiontic black yeasts. Mikologiya i Fitopatologiya 35(4):24–28.

    CAS  Google Scholar 

  4. Burridge K, Chrzanowska-Wodnicka M. 1996. Focal adhesions, contractility, and signaling. Annu Rev Cell Dev Biol 12:463–518.

    Article  PubMed  CAS  Google Scholar 

  5. Cañadas P, Laurent VM, Oddou C, Isabey D, Wendling S. 2002. A cellular tensegrity model to analyse the structural viscoelasticity of the cytoskeleton. J Theor Biol 218:155–173.

    Article  PubMed  Google Scholar 

  6. Carpenter CL. 2000. Actin cytoskeleton and cell signaling. Crit Care Med 28(4 suppl):N94–N99.

    Article  PubMed  CAS  Google Scholar 

  7. Caspar DLD. 1980. Movement and self-control in protein assemblies. Biophys J 32:103–138.

    PubMed  CAS  Google Scholar 

  8. Chen CS, Alonso JL, Ostuni E, Whitesides GM, Ingber DE. 2003. Cell shape provides global control of focal adhesion assembly. Biochem Biophys Res Commun 307:355–361.

    Article  PubMed  CAS  Google Scholar 

  9. Chen CS, Ingber DE. 1999. Tensegrity and mechanoregulation: from skeleton to cytoskeleton. Osteoarthritis Cartilage 7:81–94.

    Article  PubMed  CAS  Google Scholar 

  10. Chen CS, Mrksich M, Huang S, Whitesides GM, Ingber DE. 1997. Geometric control of cell life and death. Science 276:1425–1428.

    Article  PubMed  CAS  Google Scholar 

  11. Chrzanowska-Wodnicka M, Burridge K. 1996. Rho-stimulated contractility drives the formation of stress fibers and focal adhesions. J Cell Biol 133:1403–1415.

    Article  PubMed  CAS  Google Scholar 

  12. Coffey DS. 1998. Self-organization, complexity and chaos: the new biology for medicine. Nature Med 4:882–885.

    Article  PubMed  CAS  Google Scholar 

  13. Collins SJ. 1987. The HL-60 promyelocytic leukemia cell line: proliferation, differentiation, and cellular oncogene expression. Blood 70:1233–1244.

    PubMed  CAS  Google Scholar 

  14. Das D, Pintucci G, Stern A. 2000. MAPK-dependent expression of p21(WAF) and p27(kip1) in PMA-induced differentiation of HL60 cells. FEBS Lett 472:50–52.

    Article  PubMed  CAS  Google Scholar 

  15. Delbrück M. 1949. Colloques Internationaux du CNRS. In Unités biologiques douées de continuité génétique. CNRS, Paris.

    Google Scholar 

  16. Dong C, Skalak R, Sung KL. 1991. Cytoplasmic rheology of passive neutrophils. Biorheol 28:557–567.

    CAS  Google Scholar 

  17. Evans E, Yeung A. 1989. Apparent viscosity and cortical tension of blood granulocytes determined by micropipet aspiration. Biophys J 56:151–160.

    Article  PubMed  CAS  Google Scholar 

  18. Fabry B, Maksym GN, Butler JP, Glogauer M, Navajas D, Fredberg JF. 2001. Scaling the microrheology of living cells. Phys Rev Lett 87:148102-1–148102-4.

    Article  CAS  Google Scholar 

  19. Farrell HM Jr, Qi PX, Brown EM, Cooke PH, Tunick MH, Wickham ED, Unruh JJ. 2002. Molten globule structures in milk proteins: implications for potential new structure-function relationships. J Dairy Sci 85:459–471.

    Article  PubMed  CAS  Google Scholar 

  20. Fox JJ, Hill CC. 2001. From topology to dynamics in biochemical networks. Chaos 11:809–815.

    Article  PubMed  CAS  Google Scholar 

  21. Fuller B. 1961. Tensegrity. Portfolio Artnews Annu 4:112–127.

    Google Scholar 

  22. Fung YC, Liu SQ. 1993. Elementary mechanics of the endothelium of blood vessels. ASME J Biomech Eng 115:1–12.

    CAS  Google Scholar 

  23. Geiger B, Bershadsky A. 2001. Assembly and mechanosensory function of focal contacts. Curr Opin Cell Biol 13:584–592.

    Article  PubMed  CAS  Google Scholar 

  24. Geiger B, Bershadsky A. 2002. Exploring the neighborhood: adhesion-coupled cell mechanosensors. Cell 110:139–142.

    Article  PubMed  CAS  Google Scholar 

  25. Gell-Mann M. 1994. The quark and the jaguar: adventures in the simple and the complex. Freeman, San Francisco.

    Google Scholar 

  26. Glass L, Hill C. 1998. Ordered and disordered dynamics in random networks. Europhys Lett 41:599–604.

    Article  CAS  Google Scholar 

  27. Goss RJ. 1967. The strategy of growth. In Control of cellular growth in the adult organism, pp. 3–27. Ed. H Teir, T Rytömaa T. Academic Press, London.

    Google Scholar 

  28. Howe AK, Aplin AE, Juliano RL. 2002. Anchorage-dependent ERK signaling-mechanisms and consequences. Curr Opin Genet Dev 12:30–35.

    Article  PubMed  CAS  Google Scholar 

  29. Huang S. 2000. The practical problems of post-genomic biology. Nature Biotechnol 18:471–472.

    Article  CAS  Google Scholar 

  30. Huang S. 2002. Regulation of cellular states in mammalian cells from a genome-wide view. In Gene regulation and metabolism: post-genomic computational approach, pp. 181–220. Ed. Collado-Vides J, Hofestädt R. MIT Press, Cambridge.

    Google Scholar 

  31. Huang S, Ingber DE. 2000. Shape-dependent control of cell growth, differentiation and apoptosis: switching between attractors in cell regulatory networks. Exp Cell Res 261:91–103.

    Article  PubMed  CAS  Google Scholar 

  32. Huang S, Chen SC, GM, Ingber DE. 1998. Cell-shape-dependent control of p27Kip and cell cycle progression in human capillary endothelial cells. Mol Biol Cell 9:3179–3193.

    PubMed  CAS  Google Scholar 

  33. Ingber DE, Jamieson JD. 1985. Cells as tensegrity strutures: architectural regulation of histodifferentiation by physical forces transduced over basement membrane. In Gene expression during normal and malignant differentiation, pp. 13–32. Ed. LC Anderson, CG Gahmberg, P Ekblom. Academic Press, Orlando, FL.

    Google Scholar 

  34. Ingber DE. 1991. Integrins as mechanochemical transducers. Curr Opin Cell Biol 3:841–848.

    Article  PubMed  CAS  Google Scholar 

  35. Ingber DE. 1993. Cellular tensegrity: defining new rules of biological design that govern the cytoskeleton. J Cell Sci 104:613–627.

    PubMed  Google Scholar 

  36. Ingber DE. 1993. The riddle of morphogenesis: a question of solution chemistry or molecular cell engineering? Cell 75:1249–1252.

    Article  PubMed  CAS  Google Scholar 

  37. Ingber DE. 1998. The architecture of life. Sci Am 278:48–57.

    Article  PubMed  CAS  Google Scholar 

  38. Ingber DE. 2000. The origin of cellular life. Bioessays 22(12):1160–1170.

    Article  PubMed  CAS  Google Scholar 

  39. Ingber DE. 2003. Tensegrity. I. Cell structure and hierarchical systems biology. J Cell Sci 116(Pt 7):1157–1173.

    Article  PubMed  CAS  Google Scholar 

  40. Ingber DE. 2003. Tensegrity. II. How structural networks influence cellular informationprocessing networks. J Cell Sci 116(Pt 8):1397–1408.

    Article  PubMed  CAS  Google Scholar 

  41. Jeong H, Mason SP, Barabasi AL, Oltvai ZN. 2001. Lethality and centrality in protein networks. Nature 411:41–42.

    Article  PubMed  CAS  Google Scholar 

  42. Kauffman SA. 1969. Metabolic stability and epigenesis in randomly constructed genetic nets. J Theor Biol 22:437–467.

    Article  PubMed  CAS  Google Scholar 

  43. Kauffman SA. 1993. The origins of order. Oxford UP, New York.

    Google Scholar 

  44. Kulyk WM, Hoffman LM. 1996. Ethanol exposure stimulates cartilage differentiation by embryonic limb mesenchyme cells. Exp Cell Res 223(2):290–300.

    Article  PubMed  CAS  Google Scholar 

  45. Lewontin RC. 2000. The triple helix: gene, organism, and environment. Harvard UP, Cambridge.

    Google Scholar 

  46. Maslov S, Sneppen K. 2002. Specificity and stability in topology of protein networks. Science 296:910–913.

    Article  PubMed  CAS  Google Scholar 

  47. Messing RO. 1993. Ethanol as an enhancer of neural differentiation. Alcohol Alcoholism 2(suppl.):289–293.

    CAS  Google Scholar 

  48. Monod J, Jacob F. 1961. General conclusions: teleonomic mechanisms in cellular metabolism, growth and differentiation. Cold Spring Harbor Symp Quant Biol 26:389–401.

    PubMed  CAS  Google Scholar 

  49. Morange M. 2001. The misunderstood gene. Harvard UP, Cambridge.

    Google Scholar 

  50. Ovadi J, Srere PA. 2000. Macromolecular compartmentation and channeling. Intl Rev Cytol 92:255–280.

    Google Scholar 

  51. Parker KK, Brock AL, Brangwynne C, Mannix RJ, Wang N, Ostuni E, Geisse NA, Adams JC, Whitesides GM, Ingber DE. 2002. Directional control of lamellipodia extension by constraining cell shape and orienting cell tractional forces. FASEB J 16(10):1195–1204.

    Article  PubMed  CAS  Google Scholar 

  52. Parker SB, Eichele G, Zhang P, Rawls A, Sands AT, Bradley A, Olson EN, Harper JW, Elledge SJ. 1995. p53-independent expression of p21Cip1 in muscle and other terminally differentiating cells. Science 267:1024–1027.

    Article  PubMed  CAS  Google Scholar 

  53. Rose SPR. 1998. Lifelines: biology beyond determinism. Oxford UP, Oxford.

    Google Scholar 

  54. Santana MA, Rosenstein Y. 2003. What it takes to become an effector T cell: the process, the cells involved, and the mechanisms. J Cell Physiol 195(3):392–401.

    Article  PubMed  CAS  Google Scholar 

  55. Schultz SG. 1996. Homeostasis, Humpty Dumpty, and integrative biology. News Physiol Sci 11:238–246.

    Google Scholar 

  56. Sherr CJ. 1994. G1 phase progression: cycling on. Cell 79:561–555.

    Article  Google Scholar 

  57. Spremulli EN, Dexter DL. 1984. Polar solvents: a novel class of antineoplastic agents. J Clin Oncol 2(3):227–241.

    PubMed  CAS  Google Scholar 

  58. Stamenovic D, Fredberg JJ, Wang N, Butler JP, Ingber DE. 1996. A microstructural approach to cytoskeletal mechanics based on tensegrity. J Theor Biol 181:125–136.

    Article  PubMed  CAS  Google Scholar 

  59. Stamenovic D, Liang Z, Chen J, Wang N. 2002. Effect of the cytoskeletal prestress on the mechanical impedance of cultured airway smooth muscle cells. J Appl Physiol 92:1443–1450.

    PubMed  Google Scholar 

  60. Stamenovic D, Ingber DE. 2002. Models of cytoskeletal mechanics and adherent cells. Biomech Modeling Mechanobiol 1:95–108.

    Article  CAS  Google Scholar 

  61. Steinman RA, Hoffman B, Iro A, Guillouf C, Liebermann DA, el-Houseini ME. 1994. Induction of p21 (WAF-1/CIP1) during differentiation. Oncogene 9:3389–3396.

    PubMed  CAS  Google Scholar 

  62. Strohman RC. 1997. The coming Kuhnian revolution in biology. Nature Biotechnol 15:194–200.

    Article  CAS  Google Scholar 

  63. Sultan C, Corless M, Skelton RE. 2001. The prestressability problem of tensegrity structures: some analytical solutions. Intl J Solids Struct 38:5223–5252.

    Article  Google Scholar 

  64. Sultan C, Stamenovic D, Ingber DE. 2004. A computational tensegrity model predicts dynamic rheological behaviors in living cells. Annu Biomed Eng 32:520–530.

    Article  Google Scholar 

  65. Volokh KY, Vilnay O, Belsky M. 2000. Tensegrity architecture explains linear stiffening and predicts softening of living cells. J Biomech 33:1543–1549.

    Article  PubMed  CAS  Google Scholar 

  66. Volokh KY, Vilnay O, Belsky M. 2002. Cell cytoskeleton and tensegrity. Biorheol 39:63–67.

    Google Scholar 

  67. Waddington CH. 1956. Principles of embryology. Allen & Unwin Ltd, London.

    Google Scholar 

  68. Waddington CH. 1940. Organisers and genes. Cambridge UP, Cambridge.

    Google Scholar 

  69. Wagenknecht T, Grassucci R, Radke GA, and Roche TE. 1991. Cryoelectron microscopy of mammalian pyruvate dehydrogenase complex. J Biol Chem 266:24650–24656.

    PubMed  CAS  Google Scholar 

  70. Wagner A. 2002. Estimating coarse gene network structure from large-scale gene perturbation data. Genome Res 12(2):309–315.

    Article  PubMed  CAS  Google Scholar 

  71. Weiss JN, Qu Z, Garfinkel A. 2003. Understanding biological complexity: lessons from the past. FASEB J 17:1–6.

    Article  PubMed  CAS  Google Scholar 

  72. Wendling S, Cañadas P, Oddou C, Meunier A. 2002. Interrelations between elastic energy and strain in a tensegrity model: contribution to the analysis of the mechanical response in living cells. Comput Meth Biomech Biomed Engin 5(1):1–6.

    Article  Google Scholar 

  73. Wendling S, Oddou C, Isabey D. 1999. Stiffening response of a cellular tensegrity model. J Theor Biol 96(3):309–325.

    Article  Google Scholar 

  74. Yu ZW, Quinn PJ. 1994. Dimethyl sulphoxide: a review of its applications in cell biology. Biosci Rep 14:259–281.

    Article  PubMed  CAS  Google Scholar 

  75. Zanotti G, Guerra C. 2003. Is tensegrity a unifying concept of protein folds? FEBS Lett 534:7–10.

    Article  PubMed  CAS  Google Scholar 

  76. Huang S, Eichler G, Bar-Yam Y, Ingber DE. 2005. Cell fates as high-dimensional attractor states of a complex gene regulatory network. Phys Rev Lett 94:128701.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Vascular Biology Program, Departments of Surgery and Pathology, Children’s Hospital and Harvard Medical School, Boston, Massachusetts

    Sui Huang, Cornel Sultan & Donald E. Ingber

Authors
  1. Sui Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Cornel Sultan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Donald E. Ingber
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Donald E. Ingber .

Editor information

Editors and Affiliations

  1. Harvard-MIT (HST) Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, East Bldg. 149, 13th Street, Charlestown, MA, 02129

    Thomas S. Deisboeck M.D. (Assistant Professor of Radiology (HMS, MGH, HST) and Director, Complex Biosystems Modeling Laboratory) (Assistant Professor of Radiology (HMS, MGH, HST) and Director, Complex Biosystems Modeling Laboratory)

  2. Dept. of Cardiothoracic Surgery, Drexel Univ. College of Medicine, 215 N. 15th Street, MS# 111, Philadelphia, PA, 19102-1192

    J. Yasha Kresh Ph.D., F.A.C.C. (Professor, Research Director, Professor of Medicine and Director) (Professor, Research Director, Professor of Medicine and Director)

  3. Cardiovascular Biophysics, Drexel Univ. College of Medicine, 215 N. 15th Street, MS# 111, Philadelphia, PA, 19102-1192

    J. Yasha Kresh Ph.D., F.A.C.C. (Professor, Research Director, Professor of Medicine and Director) (Professor, Research Director, Professor of Medicine and Director)

Rights and permissions

Reprints and permissions

Copyright information

© 2006 Springer Inc.

About this chapter

Cite this chapter

Huang, S., Sultan, C., Ingber, D.E. (2006). Tensegrity, Dynamic Networks, and Complex Systems Biology: Emergence in Structural and Information Networks Within Living Cells. In: Deisboeck, T.S., Kresh, J.Y. (eds) Complex Systems Science in Biomedicine. Topics in Biomedical Engineering International Book Series. Springer, Boston, MA. https://doi.org/10.1007/978-0-387-33532-2_11

Download citation

Publish with us

Policies and ethics

Search

Navigation