Interconnected network motifs control podocyte morphology and kidney function

Science Signaling

Volumn 7, Issue 311, 2014, Pages

  Azeloglu, Evren U ^a   Hardy, Simon V ^a,c   Eungdamrong, Narat John ^a,d   Chen, Yibang ^a   Jayaraman, Gomathi ^a   Chuang, Peter Y ^a   Fang, Wei ^a   Xiong, Huabao ^a   Neves, Susana R ^a   Jain, Mohit R ^b   Li, Hong ^b   Ma'Ayan, Avi ^a   Gordon, Ronald E ^a   He, John Cijiang ^a   Iyengar, Ravi ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b The State University of New Jersey   (United States)

^c UNIVERSITÉ LAVAL   (Canada)

^d NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; CELLS, CULTURED; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; CYCLIC AMP-DEPENDENT PROTEIN KINASES; GENE EXPRESSION; GENE REGULATORY NETWORKS; IMMUNOBLOTTING; KIDNEY; KIDNEY DISEASES; MALE; MEMBRANE PROTEINS; MICE; MICROFILAMENT PROTEINS; MICROSCOPY, ELECTRON; PODOCYTES; PROTEOMICS; PUROMYCIN; RATS; RATS, SPRAGUE-DAWLEY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

EID: 84894250245     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2004621     Document Type: Article

References (93)

1. K. Tryggvason, J. Wartiovaara, How does the kidney filter plasma? Physiology 20, 96-101 (2005).
2. B. Haraldsson, J. Nyström, W. M. Deen, Properties of the glomerular barrier and mechanisms of proteinuria. Physiol. Rev. 88, 451-487 (2008).
3. R. Lannigan, R. Kark, V. E. Pollak, The effect of a single intravenous injection of aminonucleoside of puromycin on the rat kidney: A light- and electron-microscope study. J. Pathol. Bacteriol. 83, 357-362 (1962).
4. U. S. Bhalla, P. T. Ram, R. Iyengar, MAP kinase phosphatase as a locus of flexibility in a mitogen-activated protein kinase signaling network. Science 297, 1018- 1023 (2002).
5. A. Becskei, B. B. Kaufmann, A. van Oudenaarden, Contributions of low molecule number and chromosomal positioning to stochastic gene expression. Nat. Genet. 37, 937-944 (2005).
6. F. J. Isaacs, J. Hasty, C. R. Cantor, J. J. Collins, Prediction and measurement of an autoregulatory genetic module. Proc. Natl. Acad. Sci. U.S.A. 100, 7714-7719 (2003).
7. U. Alon, Network motifs: Theory and experimental approaches. Nat. Rev. Genet. 8, 450-461 (2007).
8. K. Tanaka, G. J. Augustine, A positive feedback signal transduction loop determines timing of cerebellar long-term depression. Neuron 59, 608-620 (2008).
9. W. Xiong, J. E. Ferrell Jr., A positive-feedback-based bistable 'memory module' that governs a cell fate decision. Nature 426, 460-465 (2003).
10. Y. Yang, D. Atasoy, H. H. Su, S. M. Sternson, Hunger states switch a flip-flop memory circuit via a synaptic AMPK-dependent positive feedback loop. Cell 146, 992-1003 (2011).
11. T. C. Lu, Z. Wang, X. Feng, P. Chuang, W. Fang, Y. Chen, S. Neves, A. Maayan, H. Xiong, Y. Liu, R. Iyengar, P. E. Klotman, J. C. He, Retinoic acid utilizes CREB and USF1 in a transcriptional feed-forward loop in order to stimulate MKP1 expression in human immunodeficiency virus-infected podocytes. Mol. Cell. Biol. 28, 5785-5794 (2008).
12. J. Hu, J. Qian, O. Borisov, S. Pan, Y. Li, T. Liu, L. Deng, K. Wannemacher, M. Kurnellas, C. Patterson, S. Elkabes, H. Li, Optimized proteomic analysis of a mouse model of cerebellar dysfunction using amine-specific isobaric tags. Proteomics 6, 4321-4334 (2006).
13. D. R. Shaw, Searching the Mouse Genome Informatics (MGI) resources for information on mouse biology from genotype to phenotype. Curr. Protoc. Bioinformatics Chapter 1, Unit1.7 (2009).
14. A. Lachmann, A. Ma'ayan, KEA: Kinase enrichment analysis. Bioinformatics 25, 684-686 (2009).
15. E.Y. Chen, H. Xu, S. Gordonov,M.P. Lim, M. H. Perkins, A. Ma'ayan, Expression2Kinases: mRNA profiling linked to multiple upstream regulatory layers. Bioinformatics 28, 105-111 (2012).
16. S. I. Berger, J. M. Posner, A. Ma 'ayan, Genes2Networks: Connecting lists of gene symbols using mammalian protein interactions databases. BMC Bioinformatics 8, 372 (2007).
17. J. C. He, T. C. Lu, M. Fleet, M. Sunamoto, M. Husain, W. Fang, S. Neves, Y. Chen, S. Shankland, R. Iyengar, P. E. Klotman, Retinoic acid inhibits HIV-1-induced podocyte proliferation through the cAMP pathway. J. Am. Soc. Nephrol. 18, 93-102 (2007).
18. K. Asanuma, E. Yanagida-Asanuma, C. Faul, Y. Tomino, K. Kim, P. Mundel, Synaptopodin orchestrates actin organization and cell motility via regulation of RhoA signalling. Nat. Cell Biol. 8, 485-491 (2006).
19. P. Mundel, H. W. Heid, T. M. Mundel, M. Krüger, J. Reiser, W. Kriz, Synaptopodin: An actin-associated protein in telencephalic dendrites and renal podocytes. J. Cell Biol. 139, 193-204 (1997).
20. A. J. Shaywitz, M. E. Greenberg, CREB: A stimulus-induced transcription factor activated by a diverse array of extracellular signals. Annu. Rev. Biochem. 68, 821-861 (1999).
21. M. Deak, A. D. Clifton, L. M. Lucocq, D. R. Alessi, Mitogen- and stress-activated protein kinase-1 (MSK1) is directly activated by MAPK and SAPK2/p38, and may mediate activation of CREB. EMBO J. 17, 4426-4441 (1998).
22. X. Chen, J. C. Dai, S. A. Orellana, E. M. Greenfield, Endogenous protein kinase inhibitor γ terminates immediate-early gene expression induced by cAMP-dependent protein kinase (PKA) signaling: Termination depends on PKA inactivation rather than PKA export from the nucleus. J. Biol. Chem. 280, 2700-2707 (2005).
23. D. Ekholm, P. Belfrage, V. Manganiello, E. Degerman, Protein kinase A-dependent activation of PDE4 (cAMP-specific cyclic nucleotide phosphodiesterase) in cultured bovine vascular smooth muscle cells. Biochim. Biophys. Acta 1356, 64-70 (1997).
24. T. Murata, Petri nets: Properties, analysis and applications. Proc. IEEE 77, 541-580 (1989).
25. L. R. Castro, N. Gervasi, E. Guiot, L. Cavellini, V. O. Nikolaev, D. Paupardin-Tritsch, P. Vincent, Type 4 phosphodiesterase plays different integrating roles in different cellular domains in pyramidal cortical neurons. J. Neurosci. 30, 6143-6151 (2010).
26. S. R. Neves, P. Tsokas, A. Sarkar, E. A. Grace, P. Rangamani, S. M. Taubenfeld, C. M. Alberini, J. C. Schaff, R. D. Blitzer, I. I. Moraru, R. Iyengar, Cell shape and negative links in regulatory motifs together control spatial information flow in signaling networks. Cell 133, 666-680 (2008).
27. P. T. Ram, Overexpression of tightly regulated proteins: Protein phosphatase 2A overexpression in NIH 3T3 cells. Methods Enzymol. 345, 551-555 (2002).
28. C. Blanco-Aparicio, J. Torres, R. Pulido, A novel regulatory mechanism of MAP kinases activation and nuclear translocation mediated by PKA and the PTP-SL tyrosine phosphatase. J. Cell Biol. 147, 1129-1136 (1999).
29. R. Pulido, A. Zúñiga, A. Ullrich, PTP-SL and STEP protein tyrosine phosphatases regulate the activation of the extracellular signal-regulated kinases ERK1 and ERK2 by association through a kinase interaction motif. EMBO J. 17, 7337-7350 (1998).
30. S. Paul, A. C. Nairn, P. Wang, P. J. Lombroso, NMDA-mediated activation of the tyrosine phosphatase STEP regulates the duration of ERK signaling. Nat. Neurosci. 6, 34-42 (2003).
31. K. M. Walton, R. P. Rehfuss, J. C. Chrivia, J. E. Lochner, R. H. Goodman, A dominant repressor of cyclic adenosine 3′,5′-monophosphate (cAMP)-regulated enhancer-binding protein activity inhibits the cAMP-mediated induction of the somatostatin promoter in vivo. Mol. Endocrinol. 6, 647-655 (1992).
32. S. Mangan, S. Itzkovitz, A. Zaslaver, U. Alon, The incoherent feed-forward loop accelerates the response-time of the gal system of Escherichia coli. J. Mol. Biol. 356, 1073-1081 (2006).
33. N. Papeta, Z. Zheng, E. A. Schon, S. Brosel, M. M. Altintas, S. H. Nasr, J. Reiser, V. D. D'Agati, A. G. Gharavi, Prkdc participates in mitochondrial genome maintenance and prevents Adriamycin-induced nephropathy in mice. J. Clin. Invest. 120, 4055-4064 (2010).
34. R. Verma, B. Wharram, I. Kovari, R. Kunkel, D. Nihalani, K. K. Wary, R. C. Wiggins, P. Killen, L. B. Holzman, Fyn binds to and phosphorylates the kidney slit diaphragm component Nephrin. J. Biol. Chem. 278, 20716-20723 (2003).
35. C. M. Alberini, Transcription factors in long-term memory and synaptic plasticity. Physiol. Rev. 89, 121-145 (2009).
36. J. Y. Altarejos, M. Montminy, CREB and the CRTC co-activators: Sensors for hormonal and metabolic signals. Nat. Rev. Mol. Cell Biol. 12, 141-151 (2011).
37. U. S. Bhalla, R. Iyengar, Emergent properties of networks of biological signaling pathways. Science 283, 381-387 (1999).
38. G. Weng, U. S. Bhalla, R. Iyengar, Complexity in biological signaling systems. Science 284, 92-96 (1999).
39. H. Wichterle, I. Lieberam, J. A. Porter, T. M. Jessell, Directed differentiation of embryonic stem cells into motor neurons. Cell 110, 385-397 (2002).
40. R. T. Premont, J. Inglese, R. J. Lefkowitz, Protein kinases that phosphorylate activated G protein-coupled receptors. FASEB J. 9, 175-182 (1995).
41. H. Sun, C. H. Charles, L. F. Lau, N. K. Tonks, MKP-1 (3CH134), an immediate early gene product, is a dual specificity phosphatase that dephosphorylates MAP kinase in vivo. Cell 75, 487-493 (1993).
42. H. Husdan, A. Rapoport, Estimation of creatinine by the Jaffe reaction. A comparison of three methods. Clin. Chem. 14, 222-238 (1968).
43. M. R. Jain, Q. Li, T. Liu, J. Rinaggio, A. Ketkar, V. Tournier, K. Madura, S. Elkabes, H. Li, Proteomic identification of immunoproteasome accumulation in formalin-fixed rodent spinal cords with experimental autoimmune encephalomyelitis. J. Proteome Res. 11, 1791-1803 (2012).
44. M. R. Jain, T. Liu, J. Hu, M. Darfler, V. Fitzhugh, J. Rinaggio, H. Li, Quantitative proteomic analysis of formalin fixed paraffin embedded oral HPV lesions from HIV patients. Open Proteomics J. 1, 40-45 (2008).
45. A. I. Nesvizhskii, A. Keller, E. Kolker, R. Aebersold, A statistical model for identifying proteins by tandem mass spectrometry. Anal. Chem. 75, 4646-4658 (2003).
46. A. I. Su, T. Wiltshire, S. Batalov, H. Lapp, K. A. Ching, D. Block, J. Zhang, R. Soden, M. Hayakawa, G. Kreiman, M. P. Cooke, J. R. Walker, J. B. Hogenesch, A gene atlas of the mouse and human protein-encoding transcriptomes. Proc. Natl. Acad. Sci. U.S.A. 101, 6062-6067 (2004).
47. -ΔΔCT method. Methods 25, 402-408 (2001).
48. H. Liu, R. G. Sadygov, J. R. Yates III, A model for random sampling and estimation of relative protein abundance in shotgun proteomics. Anal. Chem. 76, 4193-4201 (2004).
49. C. Rohr, W. Marwan, M. Heiner, Snoopy - A unifying Petri net framework to investigate biomolecular networks. Bioinformatics 26, 974-975 (2010).
50. R. David, H. Alla, Discrete, Continuous, and Hybrid Petri Nets (Springer, Heidelberg, ed. 2, 2010), p. 554.
51. S. Hardy, R. Iyengar, in Modeling in Systems Biology (Springer, London, 2011), vol. 16, pp. 225-251.
52. R. Heinrich, B. G. Neel, T. A. Rapoport, Mathematical models of protein kinase signal transduction. Mol. Cell 9, 957-970 (2002).
53. 2 by p42 microtubule-associated protein 2 kinase and protein kinase C. J. Biol. Chem. 268, 1960-1964 (1993).
54. J. S. Sanghera, H. B. Paddon, S. A. Bader, S. L. Pelech, Purification and characterization of a maturation-activated myelin basic protein kinase from sea star oocytes. J. Biol. Chem. 265, 52-57 (1990).
55. A. Takai, G. Mieskes, Inhibitory effect of okadaic acid on the p-nitrophenyl phosphate phosphatase activity of protein phosphatases. Biochem. J. 275, 233-239 (1991).
56. M. D. Pato, C. Sutherland, S. J. Winder, M. P. Walsh, Smooth-muscle caldesmon phosphatase is SMP-I, a type 2A protein phosphatase. Biochem. J. 293, 35-41 (1993).
57. J. G. Foulkes, S. J. Strada, P. J. F. Henderson, P. Cohen, A kinetic analysis of the effects of inhibitor-1 and inhibitor-2 on the activity of protein phosphatase-1. Eur. J. Biochem. 132, 309-313 (1983).
58. C. H. Charles, H. Sun, L. F. Lau, N. K. Tonks, The growth factor-inducible immediate-early gene 3CH134 encodes a protein-tyrosine- phosphatase. Proc. Natl. Acad. Sci. U.S.A. 90, 5292-5296 (1993).
59. MAPK-dependent phosphorylation. Science 286, 2514-2517 (1999).
60. S. P. Collins, M. D. Uhler, Characterization of PKIγ, a novel isoform of the protein kinase inhibitor of cAMP-dependent protein kinase. J. Biol. Chem. 272, 18169-18178 (1997).
61. T. Force, J. V. Bonventre, G. Heidecker, U. Rapp, J. Avruch, J. M. Kyriakis, Enzymatic characteristics of the c-Raf-1 protein kinase. Proc. Natl. Acad. Sci. U.S.A. 91, 1270-1274 (1994).
62. R. Seger, N. G. Ahn, J. Posada, E. S. Munar, A. M. Jensen, J. A. Cooper, M. H. Cobb, E. G. Krebs, Purification and characterization of mitogen-activated protein kinase activator(s) from epidermal growth factor-stimulated A431 cells. J. Biol. Chem. 267, 14373-14381 (1992).
63. mapk by MAP kinase kinase. FEBS Lett. 306, 17-22 (1992).
64. G. B. Bolger, S. Erdogan, R. E. Jones, K. Loughney, G. Scotland, R. Hoffmann, I.Wilkinson, C. Farrell, M. D. Houslay, Characterization of five different proteins produced by alternatively spliced mRNAs from the human cAMP-specific phosphodiesterase PDE4D gene. Biochem. J. 328, 539-548 (1997).
65. 2-terminal UCR regions. J. Biol. Chem. 275, 16609-16617 (2000).
66. S. Paul, G. L. Snyder, H. Yokakura, M. R. Picciotto, A. C. Nairn, P. J. Lombroso, The dopamine/D1 receptor mediates the phosphorylation and inactivation of the protein tyrosine phosphatase STEP via a PKA-dependent pathway. J. Neurosci. 20, 5630-5638 (2000).
67. K. Nika, H. Hyunh, S. Williams, S. Paul, N. Bottini, K. Taskén, P. J. Lombroso, T. Mustelin, Haematopoietic protein tyrosine phosphatase (HePTP) phosphorylation by cAMP-dependent protein kinase in T-cells: Dynamics and subcellular location. Biochem. J. 378, 335-342 (2004).
68. B. Zhou, Z. X. Wang, Y. Zhao, D. L. Brautigan, Z. Y. Zhang, The specificity of extracellular signal-regulated kinase 2 dephosphorylation by protein phosphatases. J. Biol. Chem. 277, 31818-31825 (2002).
69. C. Sette, M. Conti, Phosphorylation and activation of a cAMP-specific phosphodiesterase by the cAMP-dependent protein kinase. Involvement of serine 54 in the enzyme activation. J. Biol. Chem. 271, 16526-16534 (1996).
70. P. Hasler, J. J. Moore, G. M. Kammer, Human T lymphocyte cAMP-dependent protein kinase: Subcellular distributions and activity ranges of type I and type II isozymes. FASEB J. 6, 2735- 2741 (1992).
71. S. B. Smith, H. D. White, J. B. Siegel, E. G. Krebs, Cyclic AMP-dependent protein kinase I: Cyclic nucleotide binding, structural changes, and release of the catalytic subunits. Proc. Natl. Acad. Sci. U.S.A. 78, 1591-1595 (1981).
72. D. Ogreid, S. O. Døskeland, The kinetics of association of cyclic AMP to the two types of binding sites associated with protein kinase II from bovine myocardium. FEBS Lett. 129, 287-292 (1981).
73. H. Rehmann, F. Schwede, S. O. Døskeland, A. Wittinghofer, J. L. Bos, Ligand-mediated activation of the cAMP-responsive guanine nucleotide exchange factor Epac. J. Biol. Chem. 278, 38548-38556 (2003).
74. T. Brinkmann, O. Daumke, U. Herbrand, D. Kühlmann, P. Stege, M. R. Ahmadian, A. Wittinghofer, Rap-specific GTPase activating protein follows an alternative mechanism. J. Biol. Chem. 277, 12525-12531 (2002).
75. H. B. Kuiperij, J. de Rooij, H. Rehmann, M. van Triest, A. Wittinghofer, J. L. Bos, F. J. Zwartkruis, Characterisation of PDZ-GEFs, a family of guanine nucleotide exchange factors specific for Rap1 and Rap2. Biochim. Biophys. Acta 1593, 141-149 (2003).
76. A. Kraemer, T. Brinkmann, I. Plettner, R. Goody, A. Wittinghofer, Fluorescently labelled guanine nucleotide binding proteins to analyse elementary steps of GAP-catalysed reactions. J. Mol. Biol. 324, 763-774 (2002).
77. C. W. Dessauer, T. T. Scully, A. G. Gilman, Interactions of forskolin and ATP with the cytosolic domains of mammalian adenylyl cyclase. J. Biol. Chem. 272, 22272-22277 (1997).
78. C. M. Kim, S. B. Dion, J. L. Benovic, Mechanism of β-adrenergic receptor kinase activation by G proteins. J. Biol. Chem. 268, 15412-15418 (1993).
79. 2 adrenergic receptor. Evidence for ligand-specific conformational changes. J. Biol. Chem. 270, 28268-28275 (1995).
80. s vesicles. J. Biol. Chem. 261, 1656-1664 (1986).
81. i in Sf9 insect cell membranes. J. Biol. Chem. 277, 922-931 (2002).
82. sα in Escherichia coli. Purification and properties of two forms of the protein. J. Biol. Chem. 264, 409-418 (1989).
83. 2-adrenergic receptors with mutations of the proposed G protein-coupled receptor kinase phosphorylation sites. J. Biol. Chem. 273, 7637-7642 (1998).
84. M. Costa, M. Marchi, F. Cardarelli, A. Roy, F. Beltram, L. Maffei, G. M. Ratto, Dynamic regulation of ERK2 nuclear translocation and mobility in living cells. J. Cell Sci. 119, 4952-4963 (2006).
85. A. Fujioka, K. Terai, R. E. Itoh, K. Aoki, T. Nakamura, S. Kuroda, E. Nishida, M. Matsuda, Dynamics of the Ras/ERK MAPK cascade as monitored by fluorescent probes. J. Biol. Chem. 281, 8917-8926 (2006).
86. M. Hagiwara, P. Brindle, A. Harootunian, R. Armstrong, J. Rivier, W. Vale, R. Tsien, M. R. Montminy, Coupling of hormonal stimulation and transcription via the cyclic AMP-responsive factor CREB is rate limited by nuclear entry of protein kinase A. Mol. Cell. Biol. 13, 4852-4859 (1993).
87. B. M. Mayr, G. Canettieri, M. R. Montminy, Distinct effects of cAMP and mitogenic signals on CREB-binding protein recruitment impart specificity to target gene activation via CREB. Proc. Natl. Acad. Sci. U.S.A. 98, 10936-10941 (2001).
88. I. H. Pang, P. C. Sternweis, Purification of unique α subunits of GTP-binding regulatory proteins (G proteins) by affinity chromatography with immobilized βγ subunits. J. Biol. Chem. 265, 18707- 18712 (1990).
89. S. R. Post, R. Hilal-Dandan, K. Urasawa, L. L. Brunton, P. A. Insel, Quantification of signalling components and amplification in the β-adrenergic-receptor -adenylate cyclase pathway in isolated adult rat ventricular myocytes. Biochem. J. 311, 75- 80 (1995).
90. S. S. Taylor, J. A. Buechler, W. Yonemoto, Camp-dependent protein kinase: Framework for a diverse family of regulatory enzymes. Annu. Rev. Biochem. 59, 971-1005 (1990).
91. S. Storm, J. Cleveland, U. Rapp, Expression of raf family proto-oncogenes in normal mouse tissues. Oncogene 5, 345 -351 (1990).
92. C. V. Carman, T. Som, C. M. Kim, J. L. Benovic, Binding and phosphorylation of tubulin by G protein-coupled receptor kinases. J. Biol. Chem. 273, 20308-20316 (1998).
93. Y. Ohba, N. Mochizuki, K. Matsuo, S. Yamashita, M. Nakaya, Y. Hashimoto, M. Hamaguchi, T. Kurata, K. Nagashima, M. Matsuda, Rap2 as a slowly responding molecular switch in the Rap1 signaling cascade. Mol. Cell. Biol. 20, 6074-6083 (2000).