Exploring phospholipase C-coupled Ca2+ signalling networks using boolean modelling

G. Bhardwaj; C.P. Wells; R. Albert; D.B. van Rossum; R.L. Patterson

Exploring phospholipase C-coupled Ca²⁺ signalling networks using boolean modelling

Access Full Text

Exploring phospholipase C-coupled Ca²⁺ signalling networks using boolean modelling

Author(s): G. Bhardwaj ; C.P. Wells ; R. Albert ; D.B. van Rossum ; R.L. Patterson
DOI: 10.1049/iet-syb.2010.0019

For access to this article, please select a purchase option:

Buy article PDF

Buy Knowledge Pack

IET members benefit from discounts to all IET publications and free access to E&T Magazine. If you are an IET member, log in to your account and the discounts will automatically be applied.

Learn more about IET membership

Recommend Title Publication to library

IET Systems Biology — Recommend this title to your library

Thank you

Your recommendation has been sent to your librarian.

Author(s): G. Bhardwaj ^{1, 2, 3} ; C.P. Wells ¹ ; R. Albert ^{2, 4} ; D.B. van Rossum ^{1, 2} ; R.L. Patterson ^{2, 5}
- Affiliations: 1: Department of Biology, The Pennsylvania State University, University Park, USA
  2: Center for Computational Proteomics, The Pennsylvania State University, University Park, USA
  3: Department of Pharmacology, University of California, Davis, USA
  4: Department of Physics, The Pennsylvania State University, University Park, USA
  5: Department of Physiology and Membrane Biology, University of California, Davis, USA
Source: Volume 5, Issue 3, May 2011, p. 174 – 184
DOI: 10.1049/iet-syb.2010.0019 , Print ISSN 1751-8849, Online ISSN 1751-8857

Published

In this study, the authors explored the utility of a descriptive and predictive bionetwork model for phospholipase C-coupled calcium signalling pathways, built with non-kinetic experimental information. Boolean models generated from these data yield oscillatory activity patterns for both the endoplasmic reticulum resident inositol-1,4,5-trisphosphate receptor (IP₃R) and the plasma-membrane resident canonical transient receptor potential channel 3 (TRPC3). These results are specific as randomisation of the Boolean operators ablates oscillatory pattern formation. Furthermore, knock-out simulations of the IP₃R, TRPC3 and multiple other proteins recapitulate experimentally derived results. The potential of this approach can be observed by its ability to predict previously undescribed cellular phenotypes using in vitro experimental data. Indeed, our cellular analysis of the developmental and calcium-regulatory protein, DANGER1a, confirms the counter-intuitive predictions from our Boolean models in two highly relevant cellular models. Based on these results, the authors theorise that with sufficient legacy knowledge and/or computational biology predictions, Boolean networks can provide a robust method for predictive modelling of any biological system. [Includes supplementary material]

References

1. 1)
  - M.J. Berridge , P. Lipp , M.D. Bootman . The versatility and universality of calcium signalling. Nat. Rev. Mol. Cell Biol. , 1 , 11 - 21
2. 2)
  - H. Ando , A. Mizutani , H. Kiefer , D. Tsuzurugi , T. Michikawa , K. Mikoshiba . IRBIT suppresses IP3 receptor activity by competing with IP3 for the common binding site on the IP3 receptor. Mol. Cell , 6 , 795 - 806
3. 3)
  - Y. Tang . Simplification and analysis of models of calcium dynamics based on IP3-sensitive calcium channel kinetics. Biophys. J. , 1
4. 4)
  - C.L. Tu , W. Chang , D.D. Bikle . Phospholipase cgamma1 is required for activation of store-operated channels in human keratinocytes. J. Invest. Dermatol. , 1 , 187 - 197
5. 5)
  - R.L. Patterson , D. Boehning , S.H. Snyder . Inositol 1,4,5-trisphosphate receptors as signal integrators. Annu. Rev. Biochem. , 437 - 465
6. 6)
  - D. Liu , D.M. Umbach , S.D. Peddada , L. Li , P.W. Crockett , C.R. Weinberg . A random-periods model for expression of cell-cycle genes. Proc. Natl. Acad. Sci. USA , 19 , 7240 - 7245
7. 7)
  - C.A. Ross , S.K. Danoff , M.J. Schell , S.H. Snyder , A. Ullrich . Three additional inositol 1,4,5-trisphosphate receptors: molecular cloning and differential localization in brain and peripheral tissues. Proc. Natl. Acad. Sci. USA , 10 , 4265 - 4269
8. 8)
  - M.T. Miedel , Y. Rbaibi , C.J. Guerriero . Membrane traffic and turnover in TRP-ML1-deficient cells: a revised model for mucolipidosis type IV pathogenesis. J. Exp. Med. , 6 , 1477 - 1490
9. 9)
  - J.Y. Kim , W. Zeng , K. Kiselyov . Homer 1 mediates store- and inositol 1,4,5-trisphosphate receptor-dependent translocation and retrieval of TRPC3 to the plasma membrane. Biol. Chem. , 43 , 32540 - 32549
10. 10)
  - M. Trebak , N. Hempel , B.J. Wedel , J.T. Smyth , G.S. Bird , J.W. Putney . Negative regulation of TRPC3 channels by protein kinase C-mediated phosphorylation of serine 712. Mol. Pharmacol. , 2 , 558 - 563
11. 11)
  - J. Soboloff , M. Spassova , T. Hewavitharana . TRPC channels: integrators of multiple cellular signals. Handb Exp Pharmacol , 575 - 591
12. 12)
  - W. Zeng , D.O. Mak , Q. Li , D.M. Shin , J.K. Foskett , S. Muallem . A new mode of Ca2+ signaling by G protein-coupled receptors: gating of IP3 receptor Ca2+ release channels by Gbetagamma. Curr. Biol. , 10 , 872 - 876
13. 13)
  - S.E. Jordt , B.E. Ehrlich . TRP channels in disease. Subcell Biochem. , 253 - 271
14. 14)
  - R.H. Chow . Cadmium block of squid calcium currents. Macroscopic data and a kinetic model. J. Gen. Physiol. , 4 , 751 - 770
15. 15)
  - Y. Zhang , M.A. Hoon , J. Chandrashekar . Coding of sweet, bitter, and umami tastes: different receptor cells sharing similar signaling pathways. Cell , 3 , 293 - 301
16. 16)
  - M.R. Clark , K.S. Campbell , A. Kazlauskas . The B cell antigen receptor complex: association of Ig-alpha and Ig-beta with distinct cytoplasmic effectors. Science , 5079 , 123 - 126
17. 17)
  - A. Goldbeter . Computational approaches to cellular rhythms. Nature , 238 - 245
18. 18)
  - K. Venkatachalam , H.T. Ma , D.L. Ford , D.L. Gill . Expression of functional receptor-coupled TRPC3 channels in DT40 triple receptor InsP3 knockout cells. J. Biol. Chem. , 36 , 33980 - 33985
19. 19)
  - D.B. van Rossum , D. Oberdick , Y. Rbaibi . TRP_2, a Lipid/Trafficking domain that mediates diacylglycerol-induced vesicle fusion. J. Biol. Chem. , 49 , 34384 - 34392
20. 20)
  - G. Kervizic , L. Corcos . Dynamical modeling of the cholesterol regulatory pathway with Boolean networks. BMC Syst. Biol.
21. 21)
  - H.S. Li , X.Z. Xu , C. Montell . Activation of a TRPC3-dependent cation current through the neurotrophin BDNF. Neuron , 1 , 261 - 273
22. 22)
  - S. Patel , S.K. Joseph , A.P. Thomas . Molecular properties of inositol 1,4,5-trisphosphate receptors. Cell Calcium , 3 , 247 - 264
23. 23)
  - M.R. Maurya , S. Subramaniam . A kinetic model for calcium dynamics in RAW 264.7 cells: 2. Knockdown response and long-term response. Biophys. J. , 3 , 729 - 740
24. 24)
  - S.G. Rhee . Regulation of phosphoinositide-specific phospholipase C. Annu. Rev. Biochem. , 281 - 312
25. 25)
  - J.I. Bruce , T.J. Shuttleworth , D.R. Giovannucci , D.I. Yule . Phosphorylation of inositol 1,4,5-trisphosphate receptors in parotid acinar cells. A mechanism for the synergistic effects of cAMP on Ca2+ signaling. J. Biol. Chem. , 2 , 1340 - 1348
26. 26)
  - H. Streb , R.F. Irvine , M.J. Berridge , I. Schulz . Release of Ca2+ from a nonmitochondrial intracellular store in pancreatic acinar cells by inositol-1,4,5-trisphosphate. Nature , 5938 , 67 - 69
27. 27)
  - K. Venkatachalam , C. Montell . TRP channels. Annu. Rev. Biochem. , 387 - 417
28. 28)
  - N. Nikolaidis , D. Chalkia , D.N. Watkins . Ancient origin of the new developmental superfamily DANGER. PLoS ONE
29. 29)
  - A.P. Dawson . Calcium signalling: how do IP3 receptors work?. Curr. Biol. , 9 , R544 - R547
30. 30)
  - K. Kiselyov , A. Soyombo , S. Muallem . TRPpathies. J. Physiol. , 641 - 653
31. 31)
  - J.P. Yuan , K.I. Kiselyov , D.M. Shin . Homer binds TRPC family channels and is required for gating of TRPC1 by IP3-Receptors. Cell , 777 - 789
32. 32)
  - K. Venkatachalam , F. Zheng , D.L. Gill . Regulation of canonical transient receptor potential (TRPC) channel function by diacylglycerol and protein kinase C. J. Biol. Chem. , 31 , 29031 - 29040
33. 33)
  - T. Uchiyama , F. Yoshikawa , A. Hishida , T. Furuichi , K. Mikoshiba . A novel recombinant hyperaffinity inositol 1,4,5-trisphosphate (IP3) absorbent traps IP3, resulting in specific inhibition of IP3-mediated calcium signaling. J. Biol. Chem. , 10 , 8106 - 8113
34. 34)
  - L.P. Haynes , A.V. Tepikin , R.D. Burgoyne . Calcium binding protein 1 is an inhibitor of agonist-evoked, inositol 1,4,5-trisphophate-mediated calcium signalling. J. Biol. Chem. , 547 - 555
35. 35)
  - Y.X. Li . Equations for InsP3 receptor-mediated[Ca2+]i oscillations derived from a detailed kinetic model: a Hodgkin-Huxley like formalism. J. Theor. Biol. , 4
36. 36)
  - V. Ruiz-Velasco , S.R. Ikeda . A splice variant of the G protein beta 3-subunit implicated in disease states does not modulate ion channels. Physiol. Genomics , 2 , 85 - 95
37. 37)
  - D.M. Wittmann , J. Krumsiek , J. Saez-Rodriguez , D.A. Lauffenburger , S. Klamt , F.J. Theis . Transforming Boolean models to continuous models: methodology and application to T-cell receptor signaling. BMC Syst. Biol.
38. 38)
  - R.L. Patterson , D.B. van Rossum , A.I. Kaplin , R.K. Barrow , S.H. Snyder . Inositol 1,4,5-trisphosphate receptor/GAPDH complex augments Ca2+ release via locally derived NADH. Proc. Natl. Acad. Sci. USA , 5 , 1357 - 1359
39. 39)
  - M. Grimaldi , A. Favit , D.L. Alkon . cAMP-induced cytoskeleton rearrangement increases calcium transients through the enhancement of capacitative calcium entry. J. Biol. Chem. , 47 , 33557 - 33564
40. 40)
  - D.E. Clapham . TRP channels as cellular sensors. Nature , 6966 , 517 - 524
41. 41)
  - M.R. Maurya , S. Subramaniam . A kinetic model for calcium dynamics in RAW 264.7 cells: 1. Mechanisms, parameters, and subpopulational variability. Biophys. J. , 3 , 709 - 728
42. 42)
  - R.L. Patterson , D.B. van Rossum , D.L. Ford . Phospholipase C-gamma is required for agonist-induced Ca2+ entry. Cell , 4 , 529 - 541
43. 43)
  - D.P. Corey , J. Garcia-Anoveros , J.R. Holt . TRPA1 is a candidate for the mechanosensitive transduction channel of vertebrate hair cells. Nature , 7018 , 723 - 730
44. 44)
  - S.V. Straub , D.R. Giovannucci , J.I. Bruce , D.I. Yule . A role for phosphorylation of inositol 1,4,5-trisphosphate receptors in defining calcium signals induced by Peptide agonists in pancreatic acinar cells. J. Biol. Chem. , 35 , 31949 - 31956
45. 45)
  - R.L. Patterson , D.B. van Rossum , N. Nikolaidis , D.L. Gill , S.H. Snyder . Phospholipase C-gamma: diverse roles in receptor-mediated calcium signaling. Trends Biochem. Sci. , 12 , 688 - 697
46. 46)
  - P.J. Bartlett , K.W. Young , S.R. Nahorski , R.A. Challiss . Single cell analysis and temporal profiling of agonist-mediated inositol 1,4,5-trisphosphate, Ca2+, diacylglycerol, and protein kinase C signaling using fluorescent biosensors. J. Biol. Chem. , 23 , 21837 - 21846
47. 47)
  - M.J. Rebecchi , S.N. Pentyala . Structure, function, and control of phosphoinositide-specific phospholipase C. Physiol. Rev. , 4 , 1291 - 1335
48. 48)
  - V. Ruiz-Velasco , S.R. Ikeda . Multiple G-protein beta gamma combinations produce voltage-dependent inhibition of N-type calcium channels in rat superior cervical ganglion neurons. J. Neurosci. , 6 , 2183 - 2191
49. 49)
  - A. Tordai , R.A. Franklin , H. Patel , A.M. Gardner , G.L. Johnson , E.W. Gelfand . Cross-linking of surface IgM stimulates the Ras/Raf-1/MEK/MAPK cascade in human B lymphocytes. J. Biol. Chem. , 10 , 7538 - 7543
50. 50)
  - J.K. Acharya , K. Jalink , R.W. Hardy , V. Hartenstein , C.S. Zuker . InsP3 receptor is essential for growth and differentiation but not for vision in Drosophila. Neuron , 6 , 881 - 887
51. 51)
  - U.H. Kim , D. Fink , H.S. Kim . Nerve growth factor stimulates phosphorylation of phospholipase C-gamma in PC12 cells. J. Biol. Chem. , 3 , 1359 - 1362
52. 52)
  - C. Espinosa-Soto , P. Padilla-Longoria , E.R. varez-Buylla . A gene regulatory network model for cell-fate determination during arabidopsis thaliana flower development that is robust and recovers experimental gene expression profiles. Plant Cell , 11 , 2923 - 2939
53. 53)
  - R. Zhang , M.V. Shah , J. Yang . Network model of survival signaling in large granular lymphocyte leukemia. Proc. Natl. Acad. Sci. , 42 , 16308 - 16313
54. 54)
  - R. Albert . Scale-free networks in cell biology. J. Cell Sci. , 4947 - 4957
55. 55)
  - M.K. Jungnickel , H. Marrero , L. Birnbaumer , J.R. Lemos , H.M. Florman . Trp2 regulates entry of Ca2+ into mouse sperm triggered by egg ZP3. Nat. Cell Biol. , 5 , 499 - 502
56. 56)
  - R. Albert , H.G. Othmer . The topology of the regulatory interactions predicts the expression pattern of the segment polarity genes in Drosophila melanogaster. J. Theor. Biol. , 1 , 1 - 18
57. 57)
  - S. Shim , E.L. Goh , S. Ge . XTRPC1-dependent chemotropic guidance of neuronal growth cones. Nat. Neurosci. , 6 , 730 - 735
58. 58)
  - J. Thakar , M. Pilione , G. Kirimanjeswara , E.T. Harvill , R. Albert . Modeling systems-level regulation of host immune responses. PLoS Comput. Biol. , 6
59. 59)
  - D.B. van Rossum , R.L. Patterson , K.H. Cheung . Danger: a novel regulatory protein of IP3-receptor activity. J. Biol. Chem. , 37111 - 37116
60. 60)
  - D.H. Sharp , J. Reinitz . Prediction of mutant expression patterns using gene circuits. Biosystems , 79 - 90
61. 61)
  - M. Chaves , E.D. Sontag , R. Albert . Methods of robustness analysis for Boolean models of gene control networks. Syst. Biol. (Stevenage) , 4 , 154 - 167
62. 62)
  - G. von Dassow . The segment polarity network is a robust developmental module. Nature , 6792
63. 63)
  - C.D. Ferris , R.L. Huganir , S.H. Snyder . Calcium flux mediated by purified inositol 1,4,5-trisphosphate receptor in reconstituted lipid vesicles is allosterically regulated by adenine nucleotides. Proc. Natl. Acad. Sci. USA , 6 , 2147 - 2151
64. 64)
  - K. Tabuchi , M. Suzuki , A. Mizuno , A. Hara . Hearing impairment in TRPV4 knockout mice. Neurosci. Lett. , 3 , 304 - 308
65. 65)
  - T. Michikawa , J. Hirota , S. Kawano , Hiraoka . Calmodulin mediates calcium-dependent inactivation of the cerebellar type 1 inositol 1,4,5-trisphosphate receptor. Neuron , 4 , 799 - 808
66. 66)
  - K. Takei , R.M. Shin , T. Inoue , K. Kato , K. Mikoshiba . Regulation of nerve growth mediated by inositol 1,4,5-trisphosphate receptors in growth cones. Science , 5394 , 1705 - 1708
67. 67)
  - H. Jeong , Z.N. Oltvai , A.L. Barabasi . Prediction of protein essentiality based on genomic data. Complexus , 1 , 19 - 28
68. 68)
  - S. Li , S.M. Assmann , R. Albert . Predicting essential components of signal transduction networks: a dynamic model of guard cell abscisic acid signaling. PLoS Biol. , 10 , 1732 - 1748
69. 69)
  - M. Chaves , R. Albert , E.D. Sontag . Robustness and fragility of Boolean models for genetic regulatory networks. J. Theor. Biol. , 3 , 431 - 449
70. 70)
  - M.J. Alldred , J. Mulder-Rosi , S.E. Lingenfelter , G. Chen , B. Luscher . Distinct gamma2 subunit domains mediate clustering and synaptic function of postsynaptic GABAA receptors and gephyrin. J. Neurosci. , 3 , 594 - 603
71. 71)
  - D.O. Mak , S. McBride , J.K. Foskett . ATP regulation of type 1 inositol 1,4,5-trisphosphate receptor channel gating by allosteric tuning of Ca(2+) activation. J. Biol. Chem. , 32 , 22231 - 22237
72. 72)
  - U.S. Bhalla , R. Iyengar . Emergent properties of networks of biological signaling pathways. Science , 381 - 387
73. 73)
  - A.H. Sharp , S.H. Snyder , S.K. Nigam . Inositol 1,4,5-trisphosphate receptors. Localization in epithelial tissue. J. Biol. Chem. , 11 , 7444 - 7449
74. 74)
  - H. Ando , A. Mizutani , T. Matsu-ura , K. Mikoshiba . IRBIT, a novel inositol 1,4,5-trisphosphate (IP3] receptor-binding protein, is released from the IP3 receptor upon IP3 binding to the receptor. J. Biol. Chem. , 12 , 10602 - 10612
75. 75)
  - L. Missiaen , J.B. Parys , A.F. Weidema . The bell-shaped Ca2+ dependence of the inositol 1,4,5-trisphosphate-induced Ca2+ release is modulated by Ca2+/calmodulin. J. Biol. Chem. , 20 , 13748 - 13751
76. 76)
  - R.L. Patterson , D.B. van Rossum , R.K. Barrow , S.H. Snyder . RACK1 binds to inositol 1,4,5-trisphosphate receptors and mediates Ca2+ release. Proc. Natl. Acad. Sci. USA , 8 , 2328 - 2332
77. 77)
  - M.J. Berridge , M.D. Bootman , H.L. Roderick . Calcium signalling: dynamics, homeostasis and remodelling. Nat. Rev. Mol. Cell Biol. , 7 , 517 - 529
78. 78)
  - P. Pinton , C. Giorgi , R. Siviero , E. Zecchini , R. Rizzuto . Calcium and apoptosis: ER-mitochondria Ca2+ transfer in the control of apoptosis. Oncogene , 50 , 6407 - 6418
79. 79)
  - D. Boehning , R.L. Patterson , L. Sedaghat , N.O. Glebova , T. Kurosaki , S.H. Snyder . Cytochrome c binds to inositol(1, 4, 5) trisphosphate receptors, amplifying calcium-dependent apoptosis. Nat. Cell Biol. , 1051 - 1061
80. 80)
  - B.N. Kang , A.S. Ahmad , S. Saleem , R.L. Patterson . Death-associated protein kinase-mediated cell death modulated by interaction with DANGER. J. Neurosci. , 1 , 93 - 98
81. 81)
  - B.M. Rao , D.A. Lauffenburger , K.D. Wittrup . Integrating cell-level kinetic modeling into the design of engineered protein therapeutics. Nat. Biotech. , 2 , 191 - 194
82. 82)
  - Y. Li , Y.C. Jia , K. Cui , N. Li . Essential role of TRPC channels in the guidance of nerve growth cones by brain-derived neurotrophic factor. Nature , 7035 , 894 - 898

Login

Not registered yet?

Share

Tools

Login to add to favourites

Key

Exploring phospholipase C-coupled Ca²⁺ signalling networks using boolean modelling

Exploring phospholipase C-coupled Ca²⁺ signalling networks using boolean modelling

Buy article PDF

Buy Knowledge Pack

Thank you

References

Related content