Endothelial cells decode VEGF-mediated Ca2+ signaling patterns to produce distinct functional responses

Science Signaling

Volumn 9, Issue 416, 2016, Pages

  Noren, David P ^a,b   Chou, Wesley H ^c   Lee, Sung Hoon ^d   Qutub, Amina A ^b   Warmflash, Aryeh ^b,c   Wagner, Daniel S ^c   Popel, Aleksander S ^a   Levchenko, Andre ^d  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Rice University   (United States)

^c RICE UNIVERSITY   (United States)

^d YALE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; MYOSIN LIGHT CHAIN KINASE; TRANSCRIPTION FACTOR NFAT; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 2; VASCULOTROPIN A; VEGFA PROTEIN, HUMAN; VEGFAA PROTEIN, ZEBRAFISH; ZEBRAFISH PROTEIN;

ANGIOGENESIS; ANIMAL EXPERIMENT; ARTICLE; CALCIUM SIGNALING; CELL CYCLE PROGRESSION; CELL DIVISION; CELL FUNCTION; CELL MIGRATION; CELL MOTILITY; CELL PROLIFERATION; CHEMOTAXIS; CONTROLLED STUDY; DISSOCIATION CONSTANT; ENDOTHELIUM CELL; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; UMBILICAL VEIN ENDOTHELIAL CELL; ZEBRA FISH; ANIMAL; CYTOLOGY; EMBRYOLOGY; METABOLISM; PHYSIOLOGY;

ANIMALS; CALCIUM SIGNALING; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MYOSIN-LIGHT-CHAIN KINASE; NEOVASCULARIZATION, PHYSIOLOGIC; NFATC TRANSCRIPTION FACTORS; VASCULAR ENDOTHELIAL GROWTH FACTOR A; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84959359746     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.aad3188     Document Type: Article

References (49)

1. R. Cheong, A. Rhee, C. J. Wang, I. Nemenman, A. Levchenko, Information transduction capacity of noisy biochemical signaling networks. Science 334, 354-358 (2011).
2. S. L. Spencer, S. Gaudet, J. G. Albeck, J. M. Burke, P. K. Sorger, Non-genetic origins of cell-to-cell variability in TRAIL-induced apoptosis. Nature 459, 428-432 (2009).
3. A. Samadani, J. Mettetal, A. Van Oudenaarden, Cellular asymmetry and individuality in directional sensing. Proc. Natl. Acad. Sci. U.S.A. 103, 11549-11554 (2006).
4. T. Rimchala, R. D. Kamm, D. A. Lauffenburger, Endothelial cell phenotypic behaviors cluster into dynamic state transition programs modulated by angiogenic and angiostatic cytokines. Integr. Biol. 5, 510-522 (2013).
5. H. Gerhardt, M. Golding, M. Fruttiger, C. Ruhrberg, A. Lundkvist, A. Abramsson, M. Jeltsch, C. Mitchell, K. Alitalo, D. Shima, C. Betsholtz, VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J. Cell Biol. 161, 1163-1177 (2003).
6. L. Lamalice, F. Houle, J. Huot, Phosphorylation of Tyr1214 within VEGFR-2 triggers the recruitment of Nck and activation of Fyn leading to SAPK2/p38 activation and endothelial cell migration in response to VEGF. J. Biol. Chem. 281, 34009-34020 (2006).
7. S. Rousseau, F. Houle, H. Kotanides, L. Witte, J. Waltenberger, J. Landry, J. Huot, Vascular endothelial growth factor (VEGF)-driven actin-based motility is mediated by VEGFR2 and requires concerted activation of stress-activated protein kinase 2 (SAPK2/p38) and geldanamycin-sensitive phosphorylation of focal adhesion kinase. J. Biol. Chem. 275, 10661-10672 (2000).
8. J. Waltenberger, L. Claesson-Welsh, A. Siegbahn, M. Shibuya, C.-H. Heldin, Different signal transduction properties of KDR and Flt1, two receptors for vascular endothelial growth factor. J. Biol. Chem. 269, 26988-26995 (1994).
9. E. C. Kohn, R. Alessandro, J. Spoonster, R. P. Wersto, L. A. Liotta, Angiogenesis: Role of calcium-mediated signal transduction. Proc. Natl. Acad. Sci. U.S.A. 92, 1307-1311 (1995).
10. G. E. Hardingham, S. Chawla, C. M. Johnson, H. Bading, Distinct functions of nuclear and cytoplasmic calcium in the control of gene expression. Nature 385, 260-265 (1997).
11. S. Antoniotti, A. F. Pla, S. Pregnolato, A. Mottola, D. Lovisolo, L. Munaron, Control of endothelial cell proliferation by calcium influx and arachidonic acid metabolism: A pharmacological approach. J. Cell. Physiol. 197, 370-378 (2003).
12. M. Faehling, J. Kroll, K. J. Föhr, G. Fellbrich, U. Mayr, G. Trischler, J. Waltenberger, Essential role of calcium in vascular endothelial growth factor A-induced signaling: Mechanism of the antiangiogenic effect of carboxyamidotriazole. FASEB J. 16, 1805-1807 (2002).
13. 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 calciumdependent apoptosis. Nat. Cell Biol. 5, 1051-1061 (2003).
14. M. Marhl, M. Gosak, M. Perc, E. Roux, Importance of cell variability for calcium signaling in rat airway myocytes. Biophys. Chem. 148, 42-50 (2010).
15. N. Nakamura, T. Yamazawa, Y. Okubo, M. Iino, Temporal switching and cell-to-cell variability in Ca2+ release activity in mammalian cells. Mol. Syst. Biol. 5, 247 (2009).
16. M. R. Maurya, S. Subramaniam, A kinetic model for calcium dynamics in RAW 264.7 cells: 1. Mechanisms, parameters, and subpopulational variability. Biophys. J. 93, 709-728 (2007).
17. S. Dragoni, U. Laforenza, E. Bonetti, F. Lodola, C. Bottino, R. Berra-Romani, G. Carlo Bongio, M. P. Cinelli, G. Guerra, P. Pedrazzoli, V. Rosti, F. Tanzi, F. Moccia, Vascular endothelial growth factor stimulates endothelial colony forming cells proliferation and tubulogenesis by inducing oscillations in intracellular Ca2+ concentration. Stem Cells 29, 1898-1907 (2011).
18. R. E. Dolmetsch, K. Xu, R. S. Lewis, Calcium oscillations increase the efficiency and specificity of gene expression. Nature 392, 933-936 (1998).
19. R. E. Dolmetsch, R. S. Lewis, C. C. Goodnow, J. I. Healy, Differential activation of transcription factors induced by Ca2+ response amplitude and duration. Nature 386, 855-858 (1997).
20. J. E. Purvis, G. Lahav, Encoding and decoding cellular information through signaling dynamics. Cell 152, 945-956 (2013).
21. G. L. Hernández, O. V. Volpert, M. A. Íñiguez, E. Lorenzo, S. Martínez-Martínez, R. Grau, M. Fresno, J. M. Redondo, Selective inhibition of vascular endothelial growth factor-mediated angiogenesis by cyclosporin a: Roles of the nuclear factor of activated T cells and cyclooxygenase 2. J. Exp. Med. 193, 607-620 (2001).
22. J. Dixelius, A.-K. Olsson, A. Thulin, C. Lee, I. Johansson, L. Claesson-Welsh, Minimal active domain and mechanism of action of the angiogenesis inhibitor histidine-rich glycoprotein. Cancer Res. 66, 2089-2097 (2006).
23. P. Rafiee, J. Heidemann, H. Ogawa, N. A. Johnson, P. J. Fisher, M. S. Li, M. F. Otterson, C. P. Johnson, D. G. Binion, Cyclosporin A differentially inhibits multiple steps in VEGF induced angiogenesis in human microvascular endothelial cells through altered intracellular signaling. Cell Commun. Signal. 2, 3 (2004).
24. L. C. Ewan, H. M. Jopling, H. Jia, S. Mittar, A. Bagherzadeh, G. J. Howell, J. H. Walker, I. C. Zachary, S. Ponnambalam, Intrinsic tyrosine kinase activity is required for vascular endothelial growth factor receptor 2 ubiquitination, sorting and degradation in endothelial cells. Traffic 7, 1270-1282 (2006).
25. B. K. Robbs, A. L. S. Cruz, M. B. F. Werneck, G. P. Mognol, J. P. B. Viola, Dual roles for NFAT transcription factor genes as oncogenes and tumor suppressors. Mol. Cell. Biol. 28, 7168-7181 (2008).
26. M. Buchholz, A. Schatz, M.Wagner, P. Michl, T. Linhart, G. Adler, T. M. Gress, V. Ellenrieder, Overexpression of c-myc in pancreatic cancer caused by ectopic activation of NFATc1 and the Ca2+/calcineurin signaling pathway. EMBO J. 25, 3714-3724 (2006).
27. J. J. Heit, A. A. Apelqvist, X. Gu, M. M. Winslow, J. R. Neilson, G. R. Crabtree, S. K. Kim, Calcineurin/NFAT signalling regulates pancreatic b-cell growth and function. Nature 443, 345-349 (2006).
28. A. Köenig, T. Linhart, K. Schlengemann, K. Reutlinger, J. Wegele, G. Adler, G. Singh, L. Hofmann, S. Kunsch, T. Büch, E. Schäfer, T.M.Gress, M. E. Fernandez-Zapico, V. Ellenrieder, NFAT-induced histone acetylation relay switch promotes c-Myc-dependent growth in pancreatic cancer cells. Gastroenterology 138, 1189-1199.e2 (2010).
29. G. Singh, S. K. Singh, A. König, K. Reutlinger, M. D. Nye, T. Adhikary, M. Eilers, T. M. Gress, M. E. Fernandez-Zapico, V. Ellenrieder, Sequential activation of NFAT and c-Myc transcription factors mediates the TGF-b switch from a suppressor to a promoter of cancer cell proliferation. J. Biol. Chem. 285, 27241-27250 (2010).
30. J. W. Neal, N. A. Clipstone, A constitutively active NFATc1 mutant induces a transformed phenotype in 3T3-L1 fibroblasts. J. Biol. Chem. 278, 17246-17254 (2003).
31. N. Yissachar, T. Sharar Fischler, A. A. Cohen, S. Reich-Zeliger, D. Russ, E. Shifrut, Z. Porat, N. Friedman, Dynamic response diversity of NFAT isoforms in individual living cells. Mol. Cell 49, 322-330 (2013).
32. S. Orrenius, B. Zhivotovsky, P. Nicotera, Regulation of cell death: The calcium-apoptosis link. Nat. Rev. Mol. Cell Biol. 4, 552-565 (2003).
33. T.-L. Chew, W. A. Wolf, P. J. Gallagher, F. Matsumura, R. L. Chisholm, A fluorescent resonant energy transfer-based biosensor reveals transient and regional myosin light chain kinase activation in lamella and cleavage furrows. J. Cell Biol. 156, 543-553 (2002).
34. I. Barkefors, S. Le Jan, L. Jakobsson, E. Hejll, G. Carlson, H. Johansson, J. Jarvius, J. W. Park, N. Li Jeon, J. Kreuger, Endothelial cell migration in stable gradients of vascular endothelial growth factor A and fibroblast growth factor 2: Effects on chemotaxis and chemokinesis. J. Biol. Chem. 283, 13905-13912 (2008).
35. R. Cheong, A. Levchenko, Oscillatory signaling processes: The how, the why and the where. Curr. Opin. Genet. Dev. 20, 665-669 (2010).
36. T. R. McKnight, F. E. Curry, Mechanisms of heterogeneous endothelial cytoplasmic calcium increases in venular microvessels. Microcirculation 9, 537-550 (2002).
37. S. N. Pagakis, F. E. Curry, Imaging of Ca2+ transients in endothelial cells of single perfused capillaries: Correlation of peak [Ca2+]i with sites of macromolecule leakage. Microcirculation 1, 213-230 (1994).
38. A. Shamloo, N. Ma, M.-m. Poo, L. L. Sohn, S. C. Heilshorn, Endothelial cell polarization and chemotaxis in a microfluidic device. Lab Chip 8, 1292-1299 (2008).
39. C. L. Stokes, D. A. Lauffenburger, S. K. Williams, Migration of individual microvessel endothelial cells: Stochastic model and parameter measurement. J. Cell Sci. 99, 419-430 (1991).
40. E. Isotani, G. Zhi, K. S. Lau, J. Huang, Y. Mizuno, A. Persechini, R. Geguchadze, K. E. Kamm, J. T. Stull, Real-time evaluation of myosin light chain kinase activation in smooth muscle tissues from a transgenic calmodulin-biosensor mouse. Proc. Natl. Acad. Sci. U.S.A. 101, 6279-6284 (2004).
41. L. H. Tay, O. Griesbeck, D. T. Yue, Live-cell transforms between Ca2+ transients and FRET responses for a troponin-C-based Ca2+ sensor. Biophys. J. 93, 4031-4040 (2007).
42. R. A. Tyson, D. B. A. Epstein, K. I. Anderson, T. Bretschneider, High resolution tracking of cell membrane dynamics in moving cells: An electrifying approach. Math. Model. Nat. Phenom. 5, 34-55 (2010).
43. C. A. Schneider, W. S. Rasband, K. W. Eliceiri, NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671-675 (2012).
44. S. Paliwal, P. A. Iglesias, K. Campbell, Z. Hilioti, A. Groisman, A. Levchenko, MAPKmediated bimodal gene expression and adaptive gradient sensing in yeast. Nature 446, 46-51 (2007).
45. M. A. Unger, H.-P. Chou, T. Thorsen, A. Scherer, S. R. Quake, Monolithic microfabricated valves and pumps by multilayer soft lithography. Science 288, 113-116 (2000).
46. A. Mata, A. J. Fleischman, S. Roy, Fabrication of multi-layer SU-8 microstructures. J. Micromech. Microeng. 16, 276-284 (2006).
47. T.-W. Chen, T. J. Wardill, Y. Sun, S. R. Pulver, S. L. Renninger, A. Baohan, E. R. Schreiter, R. A. Kerr, M. B. Orger, V. Jayaraman, L. L. Looger, K. Svoboda, D. S. Kim, Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499, 295-300 (2013).
48. E. Provost, J. Rhee, S. D. Leach, Viral 2A peptides allow expression of multiple proteins from a single ORF in transgenic zebrafish embryos. Genesis 45, 625-629 (2007).
49. K. Kawakami, A. Shima, N. Kawakami, Identification of a functional transposase of the Tol2 element, an Ac-like element from the Japanese medaka fish, and its transposition in the zebrafish germ lineage. Proc. Natl. Acad. Sci. U.S.A. 97, 11403-11408 (2000).