Pyk2 is essential for astrocytes mobility following brain lesion

GLIA

Volumn 64, Issue 4, 2016, Pages 620-634

  Giralt, Albert ^a,b,c   Coura, Renata ^a,b,c   Girault, Jean Antoine ^a,b,c  

^a INSERM   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c INSTITUT DU FER À MOULIN   (France)

Author keywords

Actin polymerization; Filopodia; Gelsolin; Lamellipodia; Wound healing

Indexed keywords

ACTIN; FOCAL ADHESION KINASE 2; GELSOLIN; LATRUNCULIN B; PROTEIN KINASE C; RAC1 PROTEIN; TUMOR NECROSIS FACTOR ALPHA; NEUROPEPTIDE; PTK2B PROTEIN, MOUSE; RAC1 PROTEIN, MOUSE; TUMOR NECROSIS FACTOR;

ACTIN FILAMENT; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN DAMAGE; CELL MIGRATION; CELL MOTILITY; CELL STRUCTURE; CONTROLLED STUDY; DYNAMICS; ENZYME ACTIVITY; IN VITRO STUDY; IN VIVO CULTURE; LABORATORY; MOTOR CORTEX; MOUSE; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; WILD TYPE; WOUND; WOUND HEALING; ANIMAL; BRAIN INJURY; CELL CULTURE; CELL MOTION; DISEASE MODEL; ENZYMOLOGY; GENETICS; INJURIES; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; PHOSPHORYLATION; PHYSIOLOGY;

ACTINS; ANIMALS; ASTROCYTES; BRAIN INJURIES; CELL MOVEMENT; CELLS, CULTURED; DISEASE MODELS, ANIMAL; FOCAL ADHESION KINASE 2; GELSOLIN; MICE, KNOCKOUT; MOTOR CORTEX; NEUROPEPTIDES; PHOSPHORYLATION; PROTEIN KINASE C; RAC1 GTP-BINDING PROTEIN; TUMOR NECROSIS FACTOR-ALPHA; WOUND HEALING;

EID: 84958765684     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22952     Document Type: Article

References (76)

1. Aoto H, Sasaki H, Ishino M, Sasaki T. 2002. Nuclear translocation of cell adhesion kinase beta/proline-rich tyrosine kinase 2. Cell Struct Funct 27:47-61.
2. Aroeira RI, Sebastiao AM, Valente CA. 2015. BDNF, via truncated TrkB receptor, modulates GlyT1 and GlyT2 in astrocytes. Glia 63:2181-2197.
3. Avraham H, Park SY, Schinkmann K, Avraham S. 2000. RAFTK/Pyk2-mediated cellular signalling. Cell Signal 12:123-133.
4. Ben-Ze'ev A. 1997. Cytoskeletal and adhesion proteins as tumor suppressors. Curr Opin Cell Biol 9:99-108.
5. Benveniste EN, Sparacio SM, Bethea JR. 1989. Tumor necrosis factor-alpha enhances interferon-gamma-mediated class II antigen expression on astrocytes. J Neuroimmunol 25:209-219.
6. Buckbinder L, Crawford DT, Qi H, Ke HZ, Olson LM, Long KR, Bonnette PC, Baumann AP, Hambor JE, Grasser WA III, Pan LC, Owen TA, Luzzio MJ, Hulford CA, Gebhard DF, Paralkar VM, Simmons HA, Kath JC, Roberts WG, Smock SL, Guzman-Perez A, Brown TA, Li M 2007. Proline-rich tyrosine kinase 2 regulates osteoprogenitor cells and bone formation, and offers an anabolic treatment approach for osteoporosis. Proc Natl Acad Sci USA 104:10619-10624.
7. Bush TG, Puvanachandra N, Horner CH, Polito A, Ostenfeld T, Svendsen CN, Mucke L, Johnson MH, Sofroniew MV. 1999. Leukocyte infiltration, neuronal degeneration, and neurite outgrowth after ablation of scar-forming, reactive astrocytes in adult transgenic mice. Neuron 23:297-308.
8. Castilho RM, Squarize CH, Leelahavanichkul K, Zheng Y, Bugge T, Gutkind JS. 2010. Rac1 is required for epithelial stem cell function during dermal and oral mucosal wound healing but not for tissue homeostasis in mice. PLoS One 5:e10503.
9. Cazaubon S, Chaverot N, Romero IA, Girault JA, Adamson P, Strosberg AD, Couraud PO. 1997. Growth factor activity of endothelin-1 in primary astrocytes mediated by adhesion-dependent and -independent pathways. J Neurosci 17:6203-6212.
10. Chung CH, Fan J, Lee EY, Kang JS, Lee SJ, Pyagay PE, Khoury CC, Yeo TK, Khayat MF, Wang A, Chen S 2015. Effects of tumor necrosis factor-alpha on podocyte expression of monocyte chemoattractant protein-1 and in diabetic nephropathy. Nephron Extra 5:18.
11. Climent E, Sancho-Tello M, Minana R, Barettino D, Guerri C. 2000. Astrocytes in culture express the full-length Trk-B receptor and respond to brain derived neurotrophic factor by changing intracellular calcium levels: Effect of ethanol exposure in rats. Neurosci Lett 288:53-56.
12. Cowin AJ. 2005. Differential expression of F-actin in in utero fetal wounds. Eur J Dermatol 15:133-139.
13. Cowin AJ, Hatzirodos N, Teusner JT, Belford DA. 2003. Differential effect of wounding on actin and its associated proteins, paxillin and gelsolin, in fetal skin explants. J Invest Dermatol 120:1118-1129.
14. Deli MA, Descamps L, Dehouck MP, Cecchelli R, Joo F, Abraham CS, Torpier G. 1995. Exposure of tumor necrosis factor-alpha to luminal membrane of bovine brain capillary endothelial cells cocultured with astrocytes induces a delayed increase of permeability and cytoplasmic stress fiber formation of actin. J Neurosci Res 41:717-726.
15. Desai LP, Aryal AM, Ceacareanu B, Hassid A, Waters CM. 2004. RhoA and Rac1 are both required for efficient wound closure of airway epithelial cells. Am J Physiol Lung Cell Mol Physiol 287:L1134-L1144.
16. Du QS, Ren XR, Xie Y, Wang Q, Mei L, Xiong WC. 2001. Inhibition of PYK2-induced actin cytoskeleton reorganization, PYK2 autophosphorylation and focal adhesion targeting by FAK. J Cell Sci 114:2977-2987.
17. Gil-Henn H, Destaing O, Sims NA, Aoki K, Alles N, Neff L, Sanjay A, Bruzzaniti A, De Camilli P, Baron R, Schlessinger J 2007. Defective microtubule-dependent podosome organization in osteoclasts leads to increased bone density in Pyk2(-/-) mice. J Cell Biol 178:1053-1064.
18. Giralt A, Friedman HC, Caneda-Ferron B, Urban N, Moreno E, Rubio N, Blanco J, Peterson A, Canals JM, Alberch J. 2010. BDNF regulation under GFAP promoter provides engineered astrocytes as a new approach for long-term protection in Huntington's disease. Gene Ther 17:1294-1308.
19. Girault JA, Costa A, Derkinderen P, Studler JM, Toutant M. 1999. FAK and PYK2/CAKbeta in the nervous system: A link between neuronal activity, plasticity and survival? Trends Neurosci 22:257-263.
20. Goicoechea SM, Arneman D, Otey CA. 2008. The role of palladin in actin organization and cell motility. Eur J Cell Biol 87:517-525.
21. Goncalves AF, Dias NG, Moransard M, Correia R, Pereira JA, Witke W, Suter U, Relvas JB. 2010. Gelsolin is required for macrophage recruitment during remyelination of the peripheral nervous system. Glia 58:706-715.
22. Gott AL, Mallon BS, Paton A, Groome N, Rumsby MG. 1994. Rat brain glial cells in primary culture and subculture contain the delta, epsilon and zeta subspecies of protein kinase C as well as the conventional subspecies. Neurosci Lett 171:117-120.
23. Hampton DW, Rhodes KE, Zhao C, Franklin RJ, Fawcett JW. 2004. The responses of oligodendrocyte precursor cells, astrocytes and microglia to a cortical stab injury, in the brain. Neuroscience 127:813-820.
24. Holtje M, Hoffmann A, Hofmann F, Mucke C, Grosse G, Van RN, Kettenmann H, Just I, Ahnert-Hilger G. 2005. Role of Rho GTPase in astrocyte morphology and migratory response during in vitro wound healing. J Neurochem 95:1237-1248.
25. Huang Y, Lu W, Ali DW, Pelkey KA, Pitcher GM, Lu YM, Aoto H, Roder JC, Sasaki T, Salter MW, MacDonald JF 2001. CAKbeta/Pyk2 kinase is a signaling link for induction of long-term potentiation in CA1 hippocampus. Neuron 29:485-496.
26. Kaibuchi K, Kuroda S, Amano M. 1999. Regulation of the cytoskeleton and cell adhesion by the Rho family GTPases in mammalian cells. Annu Rev Biochem 68:459-486.
27. Kamen LA, Schlessinger J, Lowell CA. 2011. Pyk2 is required for neutrophil degranulation and host defense responses to bacterial infection. J Immunol 186:1656-1665.
28. Kinouchi R, Takeda M, Yang L, Wilhelmsson U, Lundkvist A, Pekny M, Chen DF. 2003. Robust neural integration from retinal transplants in mice deficient in GFAP and vimentin. Nat Neurosci 6:863-868.
29. Koppel AC, Kiss A, Hindes A, Burns CJ, Marmer BL, Goldberg G, Blumenberg M, Efimova T. 2014. Delayed skin wound repair in proline-rich protein tyrosine kinase 2 knockout mice. Am J Physiol Cell Physiol 306:C899-C909.
30. Kronenberg G, Gertz K, Baldinger T, Kirste I, Eckart S, Yildirim F, Ji S, Heuser I, Schrock H, Hortnagl H, Sohr R, Djoufack PC, Juttner R, Glass R, Przesdzing I, Kumar J, Freyer D, Hellweg R, Kettenmann H, Fink KB, Endres M 2010. Impact of actin filament stabilization on adult hippocampal and olfactory bulb neurogenesis. J Neurosci 30:3419-3431.
31. Kwon T, Kwon DY, Chun J, Kim JH, Kang SS. 2000. Akt protein kinase inhibits Rac1-GTP binding through phosphorylation at serine 71 of Rac1. J Biol Chem 275:423-428.
32. Lang D, Glukhov AV, Efimova T, Efimov IR. 2011. Role of Pyk2 in cardiac arrhythmogenesis. Am J Physiol Heart Circ Physiol 301:H975-H983.
33. Lev S, Moreno H, Martinez R, Canoll P, Peles E, Musacchio JM, Plowman GD, Rudy B, Schlessinger J. 1995. Protein tyrosine kinase PYK2 involved in Ca(2+)-induced regulation of ion channel and MAP kinase functions. Nature 376:737-745.
34. Liang CC, Park AY, Guan JL. 2007. In vitro scratch assay: A convenient and inexpensive method for analysis of cell migration in vitro. Nat Protoc 2:329-333.
35. Lieberman AP, Pitha PM, Shin HS, Shin ML. 1989. Production of tumor necrosis factor and other cytokines by astrocytes stimulated with lipopolysaccharide or a neurotropic virus. Proc Natl Acad Sci USA 86:6348-6352.
36. Lim Y, Lim ST, Tomar A, Gardel M, Bernard-Trifilo JA, Chen XL, Uryu SA, Canete-Soler R, Zhai J, Lin H, Schlaepfer WW, Nalbant P, Bokoch G, Ilic D, Waterman-Storer C, Schlaepfer DD 2008. PyK2 and FAK connections to p190Rho guanine nucleotide exchange factor regulate RhoA activity, focal adhesion formation, and cell motility. J Cell Biol 180:187-203.
37. Lipinski CA, Tran NL, Bay C, Kloss J, McDonough WS, Beaudry C, Berens ME, Loftus JC. 2003. Differential role of proline-rich tyrosine kinase 2 and focal adhesion kinase in determining glioblastoma migration and proliferation. Mol Cancer Res 1:323-332.
38. Lipinski CA, Tran NL, Menashi E, Rohl C, Kloss J, Bay RC, Berens ME, Loftus JC. 2005. The tyrosine kinase pyk2 promotes migration and invasion of glioma cells. Neoplasia 7:435-445.
39. Loftus JC, Yang Z, Kloss J, Dhruv H, Tran NL, Riggs DL. 2013. A novel interaction between Pyk2 and MAP4K4 is integrated with glioma cell migration. J Signal Transduct 2013:956580.
40. Lu M, Witke W, Kwiatkowski DJ, Kosik KS. 1997. Delayed retraction of filopodia in gelsolin null mice. J Cell Biol 138:1279-1287.
41. Mburu P, Romero MR, Hilton H, Parker A, Townsend S, Kikkawa Y, Brown SD. 2010. Gelsolin plays a role in the actin polymerization complex of hair cell stereocilia. PLoS One 5:e11627.
42. McGraw J, Hiebert GW, Steeves JD. 2001. Modulating astrogliosis after neurotrauma. J Neurosci Res 63:109-115.
43. Menegon A, Burgaya F, Baudot P, Dunlap DD, Girault JA, Valtorta F. 1999. FAK+ and PYK2/CAKbeta, two related tyrosine kinases highly expressed in the central nervous system: Similarities and differences in the expression pattern. Eur J Neurosci 11:3777-3788.
44. Meng XQ, Zheng KG, Yang Y, Jiang MX, Zhang YL, Sun QY, Li YL. 2006. Proline-rich tyrosine kinase2 is involved in F-actin organization during in vitro maturation of rat oocyte. Reproduction 132:859-867.
45. Mitsushima M, Takahashi H, Shishido T, Ueda K, Kioka N. 2006. Abl kinase interacts with and phosphorylates vinexin. FEBS Lett 580:4288-4295.
46. Muller G, Ayoub M, Storz P, Rennecke J, Fabbro D, Pfizenmaier K. 1995. PKC zeta is a molecular switch in signal transduction of TNF-alpha, bifunctionally regulated by ceramide and arachidonic acid. EMBO J 14:1961.
47. Murasawa S, Matsubara H, Mori Y, Masaki H, Tsutsumi Y, Shibasaki Y, Kitabayashi I, Tanaka Y, Fujiyama S, Koyama Y, Fujiyama A, Iba S, Iwasaka T 2000. Angiotensin II initiates tyrosine kinase Pyk2-dependent signalings leading to activation of Rac1-mediated c-Jun NH2-terminal kinase. J Biol Chem 275:26856-26863.
48. Nagaoka K, Udagawa T, Richter JD. 2012. CPEB-mediated ZO-1 mRNA localization is required for epithelial tight-junction assembly and cell polarity. Nat Commun 3:675.
49. Norris JG, Tang LP, Sparacio SM, Benveniste EN 1994. Signal transduction pathways mediating astrocyte IL-6 induction by IL-1 beta and tumor necrosis factor-alpha. J Immunol 152:841-850.
50. Okigaki M, Davis C, Falasca M, Harroch S, Felsenfeld DP, Sheetz MP, Schlessinger J. 2003. Pyk2 regulates multiple signaling events crucial for macrophage morphology and migration. Proc Natl Acad Sci USA 100:10740-10745.
51. Ovcharenko A, Granot G, Rokah OH, Park J, Shpilberg O, Raanani P. 2013. Enhanced adhesion/migration and induction of Pyk2 expression in K562 cells following imatinib exposure. Leuk Res 37:1729-1736.
52. Paulino VM, Yang Z, Kloss J, Ennis MJ, Armstrong BA, Loftus JC, Tran NL. 2010. TROY (TNFRSF19) is overexpressed in advanced glial tumors and promotes glioblastoma cell invasion via Pyk2-Rac1 signaling. Mol Cancer Res 8:1558-1567.
53. Pekny M, Nilsson M. 2005. Astrocyte activation and reactive gliosis. Glia 50:427-434.
54. Raponi E, Agenes F, Delphin C, Assard N, Baudier J, Legraverend C, Deloulme JC. 2007. S100B expression defines a state in which GFAP-expressing cells lose their neural stem cell potential and acquire a more mature developmental stage. Glia 55:165-177.
55. Ren XR, Du QS, Huang YZ, Ao SZ, Mei L, Xiong WC. 2001. Regulation of CDC42 GTPase by proline-rich tyrosine kinase 2 interacting with PSGAP, a novel pleckstrin homology and Src homology 3 domain containing rhoGAP protein. J Cell Biol 152:971-984.
56. Ridley AJ, Schwartz MA, Burridge K, Firtel RA, Ginsberg MH, Borisy G, Parsons JT, Horwitz AR. 2003. Cell migration: Integrating signals from front to back. Science 302:1704-1709.
57. Rose CR, Blum R, Pichler B, Lepier A, Kafitz KW, Konnerth A. 2003. Truncated TrkB-T1 mediates neurotrophin-evoked calcium signalling in glia cells. Nature 426:74-78.
58. Saadoun S, Papadopoulos MC, Watanabe H, Yan D, Manley GT, Verkman AS. 2005. Involvement of aquaporin-4 in astroglial cell migration and glial scar formation. J Cell Sci 118:5691-5698.
59. Santello M, Bezzi P, Volterra A. 2011. TNFalpha controls glutamatergic gliotransmission in the hippocampal dentate gyrus. Neuron 69:988-1001.
60. Sasaki H, Nagura K, Ishino M, Tobioka H, Kotani K, Sasaki T. 1995. Cloning and characterization of cell adhesion kinase beta, a novel protein-tyrosine kinase of the focal adhesion kinase subfamily. J Biol Chem 270:21206-21219.
61. Sholl DA. 1953. Dendritic organization in the neurons of the visual and motor cortices of the cat. J Anat 87:387-406.
62. Siciliano JC, Toutant M, Derkinderen P, Sasaki T, Girault JA. 1996. Differential regulation of proline-rich tyrosine kinase 2/cell adhesion kinase beta (PYK2/CAKbeta) and pp125(FAK) by glutamate and depolarization in rat hippocampus. J Biol Chem 271:28942-28946.
63. Sieg DJ, Ilic D, Jones KC, Damsky CH, Hunter T, Schlaepfer DD. 1998. Pyk2 and Src-family protein-tyrosine kinases compensate for the loss of FAK in fibronectin-stimulated signaling events but Pyk2 does not fully function to enhance FAK- cell migration. EMBO J 17:5933-5947.
64. Su Z, Yuan Y, Chen J, Cao L, Zhu Y, Gao L, Qiu Y, He C. 2009. Reactive astrocytes in glial scar attract olfactory ensheathing cells migration by secreted TNF-alpha in spinal cord lesion of rat. PLoS One 4:e8141.
65. Sullivan SM, Bjorkman ST, Miller SM, Colditz PB, Pow DV. 2010. Structural remodeling of gray matter astrocytes in the neonatal pig brain after hypoxia/ischemia. Glia 58:181-194.
66. Tchelingerian JL, Le SF, Jacque C. 1996. Identification and topography of neuronal cell populations expressing TNF alpha and IL-1 alpha in response to hippocampal lesion. J Neurosci Res 43:99-106.
67. Thompson CC, Ashcroft FJ, Patel S, Saraga G, Vimalachandran D, Prime W, Campbell F, Dodson A, Jenkins RE, Lemoine NR, Crnogorac-Jurcevic T, Yin HL, Costello E 2007. Pancreatic cancer cells overexpress gelsolin family-capping proteins, which contribute to their cell motility. Gut 56:95-106.
68. Tomar A, Schlaepfer DD. 2009. Focal adhesion kinase: Switching between GAPs and GEFs in the regulation of cell motility. Curr Opin Cell Biol 21:676-683.
69. Tomas M, Lazaro-Dieguez F, Duran JM, Marin P, Renau-Piqueras J, Egea G. 2003. Protective effects of lysophosphatidic acid (LPA) on chronic ethanol-induced injuries to the cytoskeleton and on glucose uptake in rat astrocytes. J Neurochem 87:220-229.
70. Wang K, Bekar LK, Furber K, Walz W. 2004. Vimentin-expressing proximal reactive astrocytes correlate with migration rather than proliferation following focal brain injury. Brain Res 1024:193-202.
71. Wang Q, Xie Y, Du QS, Wu XJ, Feng X, Mei L, McDonald JM, Xiong WC. 2003. Regulation of the formation of osteoclastic actin rings by proline-rich tyrosine kinase 2 interacting with gelsolin. J Cell Biol 160:565-575.
72. Witke W, Sharpe AH, Hartwig JH, Azuma T, Stossel TP, Kwiatkowski DJ. 1995. Hemostatic, inflammatory, and fibroblast responses are blunted in mice lacking gelsolin. Cell 81:41-51.
73. Yang CM, Lee IT, Hsu RC, Chi PL, Hsiao LD. 2013. NADPH oxidase/ROS-dependent PYK2 activation is involved in TNF-alpha-induced matrix metalloproteinase-9 expression in rat heart-derived H9c2 cells. Toxicol Appl Pharmacol 272:431-442.
74. Ying Z, Giachini FR, Tostes RC, Webb RC. 2009. PYK2/PDZ-RhoGEF links Ca2+ signaling to RhoA. Arterioscler Thromb Vasc Biol 29:1657-1663.
75. Yuan Z, Yao F, Hu Z, Sun S, Wu B. 2015. Quercetin inhibits the migration and proliferation of astrocytes in wound healing. Neuroreport 26:387-393.
76. Zhang QH, Li JC, Dong N, Tang LM, Zhu XM, Sheng ZY, Yao YM. 2013. Burn injury induces gelsolin expression and cleavage in the brain of mice. Neuroscience 228:60-72.