Light-mediated kinetic control reveals the temporal effect of the Raf/MEK/ERK pathway in PC12 cell neurite outgrowth

PLoS ONE

Volumn 9, Issue 3, 2014, Pages

  Zhang, Kai ^a   Duan, Liting ^a   Ong, Qunxiang ^a   Lin, Ziliang ^a   Varman, Pooja Mahendra ^a   Sung, Kijung ^a   Cui, Bianxiao ^a  

^a STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; NERVE GROWTH FACTOR; RAF PROTEIN; CRY2 PROTEIN, RAT; CRYPTOCHROME; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE; RAF-1 PROTEIN, RAT;

3T3 CELL LINE; ANIMAL CELL; ARTICLE; BLUE LIGHT; CELL DIFFERENTIATION; CONTROLLED STUDY; ENZYME ACTIVATION; GENETIC TRANSFECTION; ILLUMINATION; IMMUNOFLUORESCENCE; NERVE FIBER GROWTH; NONHUMAN; PC12 CELL LINE; PHOTOSTIMULATION; PLASMID; PROTEIN PROTEIN INTERACTION; RAT; SIGNAL TRANSDUCTION; WESTERN BLOTTING; ANIMAL; CELL MEMBRANE; CHEMISTRY; DRUG EFFECTS; KINETICS; LIGHT; METABOLISM; MOUSE; NEURITE; PROTEIN TERTIARY STRUCTURE; PROTEIN TRANSPORT; RADIATION RESPONSE;

ANIMALS; CELL DIFFERENTIATION; CELL MEMBRANE; CRYPTOCHROMES; DOSE-RESPONSE RELATIONSHIP, RADIATION; ENZYME ACTIVATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; KINETICS; LIGHT; MAP KINASE KINASE KINASES; MAP KINASE SIGNALING SYSTEM; MICE; NERVE GROWTH FACTOR; NEURITES; NIH 3T3 CELLS; PC12 CELLS; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RAF KINASES; RATS;

EID: 84899716042     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0092917     Document Type: Article

References (63)

1. Fambrough D, McClure K, Kazlauskas A, Lander ES (1999) Diverse Signaling Pathways Activated by Growth Factor Receptors Induce Broadly Overlapping, Rather Than Independent, Sets of Genes. Cell 97: 727-741. (Pubitemid 29278047)
2. Brandman O, Meyer T (2008) Feedback Loops Shape Cellular Signals in Space and Time. Science 322: 390-395.
3. Marshall CJ (1995) Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation. Cell 80: 179-185.
4. Scott JD, Pawson T (2009) Cell signaling in space and time: where proteins come together and when they're apart. Science 326: 1220-1224.
5. Hoffmann A, Levchenko A, Scott ML, Baltimore D (2002) The IkappaB-NFkappaB signaling module: temporal control and selective gene activation. Science 298: 1241-1245. (Pubitemid 35285493)
6. Ren H, Zhang H (2010) Wnt signaling controls temporal identities of seam cells in Caenorhabditis elegans. Dev Biol 345: 144-155.
7. Zhang W, Liu HT (2002) MAPK signal pathways in the regulation of cell proliferation in mammalian cells. Cell Res 12: 9-18.
8. Widmann C, Gibson S, Jarpe MB, Johnson GL (1999) Mitogen-activated protein kinase: conservation of a three-kinase module from yeast to human. Physiol Rev 79: 143-180. (Pubitemid 29056951)
9. Ebisuya M, Kondoh K, Nishida E (2005) The duration, magnitude and compartmentalization of ERK MAP kinase activity: mechanisms for providing signaling specificity. J Cell Sci 118: 2997-3002. (Pubitemid 41149904)
10. Seedorf K (1995) Intracellular signaling by growth factors. Metabolism 44: 24-32.
11. Herbst KJ, Allen MD, Zhang J (2011) Spatiotemporally regulated protein kinase A activity is a critical regulator of growth factor-stimulated extracellular signal-regulated kinase signaling in PC12 cells. Mol Cell Biol 31: 4063-4075.
12. Ganesan A, Zhang J (2012) How cells process information: quantification of spatiotemporal signaling dynamics. Protein Sci 21: 918-928.
13. Manning BD, Cantley LC (2007) AKT/PKB signaling: Navigating downstream. Cell 129: 1261-1274. (Pubitemid 46962095)
14. Greene LA, Tischler AS (1976) Establishment of a Noradrenergic Clonal Line of Rat Adrenal Pheochromocytoma Cells Which Respond to Nerve Growth-Factor. Proceedings of the National Academy of Sciences of the United States of America 73: 2424-2428.
15. Segal RA (2003) Selectivity in neurotrophin signaling: theme and variations. Annu Rev Neurosci 26: 299-330.
16. Huff K, End D, Guroff G (1981) Nerve Growth Factor-Induced Alteration in the Response of Pc12 Pheochromocytoma Cells to Epidermal Growth-Factor. Journal of Cell Biology 88: 189-198. (Pubitemid 11174050)
17. Gotoh Y, Nishida E, Yamashita T, Hoshi M, Kawakami M, et al. (1990) Microtubule-Associated-Protein (Map) Kinase Activated by Nerve Growth-Factor and Epidermal Growth-Factor in Pc12 Cells - Identity with the Mitogen-Activated Map Kinase of Fibroblastic Cells. European Journal of Biochemistry 193: 661-669. (Pubitemid 20381695)
18. Wang L, Liang Z, Li G (2011) Rab22 controls NGF signaling and neurite outgrowth in PC12 cells. Mol Biol Cell 22: 3853-3860.
19. Liu J, Lamb D, Chou MM, Liu YJ, Li G (2007) Nerve growth factor-mediated neurite outgrowth via regulation of Rab5. Mol Biol Cell 18: 1375-1384. (Pubitemid 46626632)
20. Qiu MS, Green SH (1992) PC12 Cell Neuronal Differentiation Is Associated with Prolonged P21(Ras) Activity and Consequent Prolonged Erk Activity. Neuron 9: 705-717.
21. Vaudry D, Stork PJS, Lazarovici P, Eiden LE (2002) Signaling Pathways for PC12 Cell Differentiation: Making the Right Connections. Science 296: 1648-1649. (Pubitemid 34579153)
22. Sasagawa S, Ozaki Y, Fujita K, Kuroda S (2005) Prediction and validation of the distinct dynamics of transient and sustained ERK activation. Nat Cell Biol 7: 365-373. (Pubitemid 40533125)
23. Traverse S, Gomez N, Paterson H, Marshall C, Cohen P (1992) Sustained Activation of the Mitogen-Activated Protein (Map) Kinase Cascade May Be Required for Differentiation of Pc12 Cells - Comparison of the Effects of Nerve Growth-Factor and Epidermal Growth-Factor. Biochemical Journal 288: 351-355.
24. Herbst KJ, Allen MD, Zhang J (2011) Spatiotemporally Regulated Protein Kinase A Activity Is a Critical Regulator of Growth Factor-Stimulated Extracellular Signal-Regulated Kinase Signaling in PC12 Cells. Molecular and Cellular Biology 31: 4063-4075.
25. Chung J, Kubota H, Ozaki Y, Uda S, Kuroda S (2010) Timing-dependent actions of NGF required for cell differentiation. PLoS One 5: e9011.
26. New L, Li Y, Ge B, Zhong H, Mansbridge J, et al. (2001) SB203580 promotes EGF-stimulated early morphological differentiation in PC12 cell through activating ERK pathway. J Cell Biochem 83: 585-596. (Pubitemid 33055436)
27. Stanciu M, Wang Y, Kentor R, Burke N, Watkins S, et al. (2000) Persistent activation of ERK contributes to glutamate-induced oxidative toxicity in a neuronal cell line and primary cortical neuron cultures. J Biol Chem 275: 12200-12206. (Pubitemid 30237798)
28. Subramaniam S, Zirrgiebel U, von Bohlen Und Halbach O, Strelau J, Laliberte C, et al. (2004) ERK activation promotes neuronal degeneration predominantly through plasma membrane damage and independently of caspase-3. J Cell Biol 165: 357-369. (Pubitemid 38649911)
29. Cheung EC, Slack RS (2004) Emerging role for ERK as a key regulator of neuronal apoptosis. Sci STKE 2004: PE45.
30. Heasley LE, Johnson GL (1992) The beta-PDGF receptor induces neuronal differentiation of PC12 cells. Mol Biol Cell 3: 545-553. (Pubitemid 23079755)
31. Traverse S, Seedorf K, Paterson H, Marshall CJ, Cohen P, et al. (1994) EGF triggers neuronal differentiation of PC12 cells that overexpress the EGF receptor. Curr Biol 4: 694-701.
32. Nguyen TT, Scimeca JC, Filloux C, Peraldi P, Carpentier JL, et al. (1993) Co-regulation of the mitogen-activated protein kinase, extracellular signal-regulated kinase 1, and the 90-kDa ribosomal S6 kinase in PC12 cells. Distinct effects of the neurotrophic factor, nerve growth factor, and the mitogenic factor, epidermal growth factor. J Biol Chem 268: 9803-9810. (Pubitemid 23146043)
33. Avraham R, Yarden Y (2011) Feedback regulation of EGFR signalling: decision making by early and delayed loops. Nat Rev Mol Cell Biol 12: 104-117.
34. Ji Y, Lu Y, Yang F, Shen W, Tang TT, et al. (2010) Acute and gradual increases in BDNF concentration elicit distinct signaling and functions in neurons. Nat Neurosci 13: 302-309.
35. Pollock R, Clackson T (2002) Dimerizer-regulated gene expression. Curr Opin Biotechnol 13: 459-467. (Pubitemid 35379932)
36. Inoue T, Heo WD, Grimley JS, Wandless TJ, Meyer T (2005) An inducible translocation strategy to rapidly activate and inhibit small GTPase signaling pathways. Nat Methods 2: 415-418. (Pubitemid 40916559)
37. Castellano F, Chavrier P (2000) Inducible membrane recruitment of small GTP-binding proteins by rapamycin-based system in living cells. Methods Enzymol 325: 285-295.
38. Karginov AV, Ding F, Kota P, Dokholyan NV, Hahn KM (2010) Engineered allosteric activation of kinases in living cells. Nat Biotechnol 28: 743-747.
39. Karginov AV, Zou Y, Shirvanyants D, Kota P, Dokholyan NV, et al. (2010) Light Regulation of Protein Dimerization and Kinase Activity in Living Cells Using Photocaged Rapamycin and Engineered FKBP. J Am Chem Soc.
40. Gautier A, Deiters A, Chin JW (2011) Light-activated kinases enable temporal dissection of signaling networks in living cells. J Am Chem Soc 133: 2124-2127.
41. Harper SM, Neil LC, Gardner KH (2003) Structural basis of a phototropin light switch. Science 301: 1541-1544. (Pubitemid 37128547)
42. Wu YI, Frey D, Lungu OI, Jaehrig A, Schlichting I, et al. (2009) A genetically encoded photoactivatable Rac controls the motility of living cells. Nature 461: 104-108.
43. Strickland D, Lin Y, Wagner E, Hope CM, Zayner J, et al. (2012) TULIPs: tunable, light-controlled interacting protein tags for cell biology. Nat Methods 9: 379-384.
44. Strickland D, Yao X, Gawlak G, Rosen MK, Gardner KH, et al. (2010) Rationally improving LOV domain-based photoswitches. Nat Methods 7: 623-626.
45. Kennedy MJ, Hughes RM, Peteya LA, Schwartz JW, Ehlers MD, et al. (2010) Rapid blue-light-mediated induction of protein interactions in living cells. Nat Methods 7: 973-975.
46. Bugaj LJ, Choksi AT, Mesuda CK, Kane RS, Schaffer DV (2013) Optogenetic protein clustering and signaling activation in mammalian cells. Nat Methods 10: 249-252.
47. Levskaya A, Weiner OD, Lim WA, Voigt CA (2009) Spatiotemporal control of cell signalling using a light-switchable protein interaction. Nature 461: 997-1001.
48. Shimizu-Sato S, Huq E, Tepperman JM, Quail PH (2002) A light-switchable gene promoter system. Nat Biotechnol 20: 1041-1044.
49. Toettcher JE, Weiner OD, Lim WA (2013) Using optogenetics to interrogate the dynamic control of signal transmission by the Ras/Erk module. Cell 155: 1422-1434.
50. Wend S, Wagner HJ, Muller K, Zurbriggen MD, Weber W, et al. (2013) Optogenetic Control of Protein Kinase Activity in Mammalian Cells. ACS Synth Biol.
51. Chen X, Resh MD (2001) Activation of mitogen-activated protein kinase by membrane-targeted Raf chimeras is independent of raft localization. Journal of Biological Chemistry 276: 34617-34623.
52. Leevers SJ, Paterson HF, Marshall CJ (1994) Requirement for Ras in Raf activation is overcome by targeting Raf to the plasma membrane. Nature 369: 411-414. (Pubitemid 24184056)
53. Liu H, Yu X, Li K, Klejnot J, Yang H, et al. (2008) Photoexcited CRY2 Interacts with CIB1 to Regulate Transcription and Floral Initiation in Arabidopsis. Science 322: 1535-1539.
54. Lidke DS, Huang F, Post JN, Rieger B, Wilsbacher J, et al. (2010) ERK nuclear translocation is dimerization-independent but controlled by the rate of phosphorylation. J Biol Chem 285: 3092-3102.
55. Brunet A, Roux D, Lenormand P, Dowd S, Keyse S, et al. (1999) Nuclear translocation of p42/p44 mitogen-activated protein kinase is required for growth factor-induced gene expression and cell cycle entry. EMBO J 18: 664-674. (Pubitemid 29057251)
56. Chen RH, Sarnecki C, Blenis J (1992) Nuclear localization and regulation of erkand rsk-encoded protein kinases. Mol Cell Biol 12: 915-927.
57. Das KP, Freudenrich TM, Mundy WR (2004) Assessment of PC12 cell differentiation and neurite growth: a comparison of morphological and neurochemical measures. Neurotoxicol Teratol 26: 397-406. (Pubitemid 38534472)
58. Wood KW, Qi H, D'Arcangelo G, Armstrong RC, Roberts TM, et al. (1993) The cytoplasmic raf oncogene induces a neuronal phenotype in PC12 cells: a potential role for cellular raf kinases in neuronal growth factor signal transduction. Proc Natl Acad Sci U S A 90: 5016-5020. (Pubitemid 23182966)
59. Saito TH, Uda S, Tsuchiya T, Ozaki Y, Kuroda S (2013) Temporal decoding of MAP kinase and CREB phosphorylation by selective immediate early gene expression. PLoS One 8: e57037.
60. Watanabe K, Akimoto Y, Yugi K, Uda S, Chung J, et al. (2012) Latent process genes for cell differentiation are common decoders of neurite extension length. J Cell Sci 125: 2198-2211.
61. Kohn AD, Takeuchi F, Roth RA (1996) Akt, a pleckstrin homology domain containing kinase, is activated primarily by phosphorylation. J Biol Chem 271: 21920-21926. (Pubitemid 26303815)
62. Bryksin AV, Matsumura I (2010) Overlap extension PCR cloning: a simple and reliable way to create recombinant plasmids. Biotechniques 48: 463-465.
63. Meijering E, Jacob M, Sarria JC, Steiner P, Hirling H, et al. (2004) Design and validation of a tool for neurite tracing and analysis in fluorescence microscopy images. Cytometry A 58: 167-176. (Pubitemid 38509178)