Nitric oxide synthase mediates PC12 differentiation induced by the surface topography of nanostructured TiO2

Journal of Nanobiotechnology

Volumn 11, Issue 1, 2013, Pages

  Tamplenizza, Margherita ^a,b   Lenardi, Cristina ^a,b   Maffioli, Elisa ^a,b   Nonnis, Simona ^a,b   Negri, Armando ^a,b   Forti, Stefania ^a   Sogne, Elisa ^a,b   De Astis, Silvia ^a,b,c   Matteoli, Michela ^a,b,c   Schulte, Carsten ^a   Milani, Paolo ^a,b   Tedeschi, Gabriella ^a,b  

^a UNIVERSITY OF MILAN   (Italy)

^b Fondazione Filarete   (Italy)

^c Clinical and Research Center Humanitas   (Italy)

Author keywords

Nanostructured titanium oxide film; NOS; PC12; Tyrosine nitration

Indexed keywords

DIFFERENTIATION PROCESS; NANOSTRUCTURED TITANIUM; NITRIC-OXIDE SYNTHASE; NOS; PC12; SIGNAL-REGULATED KINASE; SUPERSONIC CLUSTER BEAM DEPOSITION; TYROSINE NITRATION;

AMINO ACIDS; CELL CULTURE; CELL PROLIFERATION; CELLS; ENZYME ACTIVITY; NANOTECHNOLOGY; NITRATION; NITRIC OXIDE; OXIDE FILMS; PROTEINS;

TITANIUM DIOXIDE;

CYTOSKELETON PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 3; NANOMATERIAL; NERVE GROWTH FACTOR; NITRIC OXIDE SYNTHASE; TITANIUM DIOXIDE;

ACTIN FILAMENT; ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL TYPE; CONTROLLED STUDY; HUMAN; HUMAN CELL; NEUROBLASTOMA; NITRATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PC12 CELL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; SURFACE PROPERTY; TOPOGRAPHY;

ANIMALS; BIOCOMPATIBLE MATERIALS; CELL DIFFERENTIATION; CELL PROLIFERATION; GENE EXPRESSION REGULATION; HUMANS; MECHANOTRANSDUCTION, CELLULAR; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; NERVE GROWTH FACTOR; NEURITES; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; PC12 CELLS; RATS; SURFACE PROPERTIES; TITANIUM; TYROSINE;

EID: 84885353705     PISSN: None     EISSN: 14773155     Source Type: Journal    
DOI: 10.1186/1477-3155-11-35     Document Type: Article

References (92)

1. Lutolf MP, Hubbell JA. Synthetic biomaterials as instructive extracellular microenvironments for morphogenesis in tissue engineering. Nat Biotechnol 2005, 23:47-55. 10.1038/nbt1055, 15637621.
2. Kleinman HK, Philp D, Hoffman MP. Role of the extracellular matrix in morphogenesis. Curr Opin Biotechnol 2003, 14:526-532. 10.1016/j.copbio.2003.08.002, 14580584.
3. Chen C, Jiang X. Microengineering the environment of mammalian cells in culture. MRS Bull 2005, 30:194-201.
4. Wheeldon I, Farhadi A, Bick AG, Jabbari E, Khademhosseini A. Nanoscale tissue engineering: spatial control over cell-materials interactions. Nanotechnology 2011, 22:212001. 10.1088/0957-4484/22/21/212001, 3155808, 21451238.
5. Abrams GA, Goodman SL, Nealey PF, Franco M, Murphy CJ. Nanoscale topography of the basement membrane underlying the corneal epithelium of the rhesus macaque. Cell Tissue Res 2000, 299:39-46. 10.1007/s004410050004, 10654068.
6. Dalby MJ, Riehle MO, Johnstone H, Affrossman S, Curtis AS. In vitro reaction of endothelial cells to polymer demixed nanotopography. Biomaterials 2002, 23:2945-2954. 10.1016/S0142-9612(01)00424-0, 12069336.
7. Andersson AS, Backhed F, Von Euler A, Richter-Dahlfors A, Sutherland D, Kasemo B. Nanoscale features influence epithelial cell morphology and cytokine production. Biomaterials 2003, 24:3427-3436. 10.1016/S0142-9612(03)00208-4, 12809771.
8. Thapa A, Webster TJ, Haberstroh KM. Polymers with nano-dimensional surface features enhance bladder smooth muscle cell adhesion. J Biomed Mater Res 2003, 67:1374-1383.
9. Dalby MJ, Gadegaard N, Riehle MO, Wilkinson CD, Curtis AS. Investigating filopodia sensing using arrays of defined nano-pits down to 35 nm diameter in size. Int J Biochem Cell Biol 2004, 36:2015-2025.
10. Dalby MJ, Riehle MO, Johnstone HJ, Affrossman S, Curtis AS. Polymer-demixed nanotopography: control of fibroblast spreading and proliferation. Tissue Eng 2002, 8:1099-1108. 10.1089/107632702320934191, 12542955.
11. Yim EKF, Darling EM, Kulangara K, Guilak F, Leong KW. Nanotopography-induced changes in focal adhesions, cytoskeletal organization, and mechanical properties of human mesenchymal stem cells. Biomaterials 2010, 31:1299-1306. 10.1016/j.biomaterials.2009.10.037, 2813896, 19879643.
12. Fan YW, Cui FZ, Hou S, Xu QY, Chen LN, Lee IS. Culture of neural cells on silicon wafers with nano-scale surface topograph. J Neurosci Methods 2002, 120:17-23. 10.1016/S0165-0270(02)00181-4, 12351203.
13. Ferrari A, Faraci P, Cecchini M, Beltram F. The effect of alternative neuronal differentiation pathways on PC12 cell adhesion and neurite alignment to nanogratings. Biomaterials 2010, 31:2565-2573. 10.1016/j.biomaterials.2009.12.010, 20035995.
14. Ferrari A, Cecchini M, Serresi M, Faraci P, Pisignano D, Beltram F. Neuronal polarity selection by topography-induced focal adhesion control. Biomaterials 2010, 31:4682-4694. 10.1016/j.biomaterials.2010.02.032, 20304485.
15. Foley AD, Grunwald EW, Nealey PF, Murphy CJ. Cooperative modulation of neuritogenesis by PC12 cells by topography and nerve growth factor. Biomaterials 2005, 26:3639-3644. 10.1016/j.biomaterials.2004.09.048, 15621254.
16. Schwarz US, Bischofs IB. Physical determinants of cell organization in soft media. Med Eng Phys 2005, 27:763-772. 10.1016/j.medengphy.2005.04.007, 15951217.
17. Huang C, Borchers CH, Schaller MD, Jacobson K. Phosphorylation of paxillin by p38MAPK is involved in the neurite extension of PC-12 cells. J Cell Biol 2004, 26:593-602.
18. Woo S, Gomez TM. Rac1 and RhoA promote neurite outgrowth through formation and stabilization of growth come point contacts. J Neurosci 2006, 27:730-742.
19. D'Arcandelo G, Halegoua S. A branched signaling pathway for nerve growth factor is revealed by Src-, Ras-, and Raf-mediated gene inductions. Mol Cell Biol 1993, 13:3146-3155. 359751, 8497245.
20. Klesse LJ, Meyers KA, Marshall CJ, Para LF. Nerve growth factor induces survival and differentiation through two distinct signaling cascades in PC12 cells. Oncogene 1999, 18:2055-2068. 10.1038/sj.onc.1202524, 10321730.
21. Rakhit S, Pyne S, Pyne NJ. Nerve growth factor stimulation of p42/p44 mitogen activated protein kinase in PC12 cells: Role of G(i/o), G protein -coupled receptor kinase 2, beta-arrestin I, and endocytic processing. Mol Pharmacol 2001, 60:63-70.
22. Waetzig V, Herdegen T. The concerted signaling of ERK1/2 and JNKs is essential for PC12 cell neuritogenesis and converges at the level of target proteins. Mol Cell Neurosci 2003, 24:238-249. 10.1016/S1044-7431(03)00126-X, 14550783.
23. Greene LA, Tischler AS. Establishment of noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc Natl Acad Sci USA 1976, 73:2424-2428. 10.1073/pnas.73.7.2424, 430592, 1065897.
24. Fujii DK, Massoglia SL, Savion N, Gospodarowicz D. Neurite outgrowth and protein synthesis by PC12 cells as a function of substratum and nerve growth factor. J Neurosci 1982, 2:1157-1175.
25. Lee JH, Lee HY, Kim HW. Adhesive proteins linked with focal adhesion kinase regulate neurite outgrowth of PC12 cells. Acta Biomater 2012, 8:165-172. 10.1016/j.actbio.2011.08.024, 21911085.
26. Aizawa M, Koyama S, Kimura K, Haruyama T, Yanagida Y, Kobatake E. Electrically stimulated modulation of cellular function in proliferation, differentiation, and gene expression. Electrochemistry 1999, 67:118-125.
27. Guo Y, Li M, Mylonakis A, Han J, MacDiarmid AG, Chen X, et al. Electroactive oligoaniline-containing self-assembled monolayers for tissue engineering applications. Biomacromolecules 2007, 8:3025-3034. 10.1021/bm070266z, 17845053.
28. Gerdin MJ, Eiden LE. Regulation of PC12 cell differentiation by cAMP signaling to ERK independent of PKA: do all the connections add up?. Sci STKE 2007, 382:pe15.
29. Peunova N, Enikolopov G. Nitric oxide triggers a switch to growth arrest during differentiation of neuronal cells. Nature 1995, 375:68-73. 10.1038/375068a0, 7536899.
30. Yamazaki M, Chiba K, Mohri T. Fundamental role of nitric oxide in neuritogenesis of PC12h cells. Br J Pharmacol 2005, 146:662-669. 10.1038/sj.bjp.0706370, 1751193, 16113690.
31. Lamour G, Journiac N, Souès S, Bonneau S, Nassoy P, Hamraoui A. Influence of surface energy distribution on neuritogenesis. Colloids Surf B: Biointerfaces 2009, 72:208-218. 10.1016/j.colsurfb.2009.04.006, 19419846.
32. Lamour G, Aftekhari-Bafrooei A, Borguet E, Souès A, Hamraoui A. Neuronal adhesion and differentiation driven by nanoscale surface free-energy gradients. Biomaterials 2010, 31:3762-3771. 10.1016/j.biomaterials.2010.01.099, 20149439.
33. Wegner K, Piseri P, Vahedi Tafreshi H, Milani P. Cluster beam deposition: a tool for nanoscale science and technology. J Phys D Appl Phys 2006, 39:R439-R459.
34. Carbone E, Marangi I, Zanardi A, Giorgetti L, Chierici E, Berlanda G, et al. Biocompatibility of cluster-assembled nanostructured TiO2 with primary and cancer cells. Biomaterials 2006, 27:3221-3229. 10.1016/j.biomaterials.2006.01.056, 16504283.
35. Bellicchi M, Erratico S, Razini P, Meregalli M, Cattaneo A, Jacchetti E, et al. Ex vivo expansion of human circulating myogenic progenitors on cluster-assembled nanostructured TiO2. Biomaterials 2010, 31:5385-5396. 10.1016/j.biomaterials.2010.03.021, 20398929.
36. Podestà A, Bongiorno G, Scopelliti PE, Bovio S, Milani P, Semprebon G, et al. Cluster-assembled nanostructured titanium oxide films with tailored wettability. J Phys Chem C 2009, 113:18264-18269.
37. Carbone R, De Marni M, Zanardi A, Vinati S, Barborini E, Fornasari L, et al. Characterization of cluster-assembled nanostructured titanium oxide coatings as substrates for protein arrays. Anal Biochem 2009, 394:7-12. 10.1016/j.ab.2009.07.005, 19589333.
38. Scopelliti PE, Borgonovo A, Indrieri M, Giorgetti L, Bongiorno G, Carbone R, et al. The effect of surface nanometre-scale morphology on protein adsorption. PLoS ONE 2010, 5:e11862. 10.1371/journal.pone.0011862, 2912332, 20686681.
39. Påhlman S, Ruusala AI, Abrahamsson L, Mattsson ME, Esscher T. Retinoic acid-induced differentiation of cultured human neuroblastoma cells: a comparison with phorbolester-induced differentiation. Cell Differ 1984, 14(2):135-144. 10.1016/0045-6039(84)90038-1, 6467378.
40. Jensen LM, Zhang Y, Shooter EM. Steady-state polypeptide modulations associated with nerve growth factor (NGF)-induced terminal differentiation and NGF deprivation-induced apoptosis in human neuroblastoma cells. J Biol Chem 1992, 267(27):19325-19333.
41. Jämsä A, Hasslund K, Cowburn RF, Bäckström A, Vasänge M. The retinoic acid and brain-derived neurotrophic factor differentiated SH-SY5Y cell line as a model for Alzheimer's disease-like tau phosphorylation. Biochem Biophys Res Commun 2004, 319(3):993-1000. 10.1016/j.bbrc.2004.05.075, 15184080.
42. Vahedi Tafreshi H, Piseri P, Benedek G, Milani P. The role of gas dynamics in operation conditions of a pulsed microplasma cluster source for nanostructured thin films deposition. J Nanosci Nanotechnol 2006, 6:1140-1149. 10.1166/jnn.2006.139, 16736779.
43. Piseri P, Vahedi Tafreshi H, Milani P. Manipulation of nanoparticles in supersonic beams for the production of nanostructured materials. Curr Opin Solid State Mater Sci 2004, 8:195-202.
44. Barborini E, Kholmanov IN, Conti AM, Piseri P, Vinati S, Milani P, et al. Supersonic cluster beam deposition of nanostructured titania. Eur Phys J D 2003, 24:277-282.
45. Verderio C, Coco S, Fumagalli G, Matteoli M. Spatial changes in calcium signaling during the establishment of neuronal polarity and synaptogenesis. J Cell Biol 1994, 126(6):1527-1536. 10.1083/jcb.126.6.1527, 2290961, 8089183.
46. Cappelletti G, Maggioni MG, Tedeschi G, Maci R. Protein Tyr nitration is triggered by nerve growth factor during neuronal differentiation of PC12 cells. Exp Cell Res 2003, 288:9-20. 10.1016/S0014-4827(03)00209-X, 12878155.
47. Barabasi AL, Stanley HE. Fractal concepts in surface growth 1995, New York: Cambridge University Press.
48. Caruso T, Lenardi C, Agostino RG, Amati M, Bongiorno G, Mazza T, Policicchio A, Formoso V, Maccallini E, Colavita E, Chiarello G, Finetti P, Šutara F, Skála T, Piseri P, Prince KC, Milani P. Electronic structure of cluster assembled nanostructured TiO2 by resonant photoemission at the Ti L2,3 edge. J Chem Phys 2008, 128:094704. 10.1063/1.2832321, 18331107.
49. Caruso T, Lenardi C, Mazza T, Policicchio A, Bongiorno G, Agostino RG, Chiarello G, Colavita E, Finetti P, Prince KC, Ducati C, Piseri P, Milani P. Photoemission investigations on nanostructured TiO2 grown by cluster assembling. Surf Sci 2007, 601:2688-2691.
50. Podestà A, Bongiorno G, Scopelliti PE, Bovio S, Milani P, Semprebon C, Mistura G. Cluster-assembled nanostructured titanium oxide films with tailored wettability. J Phys Chem 2009, 113:18264-18269.
51. Contestabile A, Ciani E. Role of nitric oxide in the regulation of neuronal proliferation, survival and differentiation. Neurochem Int 2004, 45:903-914. 10.1016/j.neuint.2004.03.021, 15312985.
52. Hindley S, Juurlink BH, Gysbers JW, Middlemiss PJ, Herman MA, Rathbone MP. Nitric oxide donors enhance neutrophin-induced neurite outgrowth through a cGMP-dependent mechanism. J Neurosci Res 1997, 45:427-439.
53. Yamazaki M, Chiba K, Mohri T, Hatanaka H. Cyclic GMP-dependent neurite outgrowth by genipin and nerve growth factor in PC12h cells. Eur J Pharmacol 2004, 488:35-43. 10.1016/j.ejphar.2004.02.009, 15044033.
54. Cappelletti G, Tedeschi G, Maggioni MG, Negri A, Nonnis S, Maci R. The nitration of τ protein in neurone-like PC12 cells. FEBS Lett 2004, 562:35-39. 10.1016/S0014-5793(04)00173-5, 15043998.
55. Nonnis S, Cappelletti G, Taverna F, Ronchi C, Ronchi S, Negri A, et al. Tau is endogenously nitrated in mouse brain: identification of a tyrosine residue modified in vivo by NO. Neurochem Res 2008, 33:518-525. 10.1007/s11064-007-9467-x, 17768677.
56. Tedeschi G, Cappelletti G, Nonnis S, Taverna F, Negri A, Ronchi C, et al. Tyrosine nitration is a novel post-translational modification occurring on the neuronal intermediate filament protein peripherin. Neurochem Res 2007, 32:433-441. 10.1007/s11064-006-9244-2, 17268851.
57. Oess S, Icking A, Fulton D, Govers R, Muller-Esterl W. Subcellular targeting and trafficking of nitric oxide synthases. Biochem J 2006, 396:401-409. 10.1042/BJ20060321, 1482820, 16722822.
58. Fostermann U, Boissel JP, Kleimert H. Expressional control of the" constitutive" isoforms of nitric oxide synthase (NOS I and NOS III). FASEB J 1998, 12:773-790.
59. Su Y, Kondrikov D, Block ER. Cytoskeletal regulation of nitric oxide synthase. Cell Biochem Biophys 2005, 43:439-449. 10.1385/CBB:43:3:439, 16244368.
60. Kondrikov D, Fonseca FV, Elms S, Fulton D, Black SM, Block ER, et al. β-Actin association with endothelial nitric-oxide synthase modulates nitric oxide and superoxide generation from the enzyme. J Biol Chem 2009, 285:4319-4327. 2836036, 19946124.
61. Liu Z, Cao J, Ma Q, Gao X, Ren J, Xue Y. GPS-YNO2: Computational prediction of tyrosine nitration sites in proteins. Mol Biosyst 2011, 7(4):1197-1204. 10.1039/c0mb00279h, 21258675.
62. Tedeschi G, Cappelletti G, Negri A, Pagliato L, Maggioni MG, Maci R, et al. Characterization of nitroproteome in neuron-like PC12 cells differentiated with nerve growth factor: identification of two nitration sites in α-tubulin. Proteomics 2005, 5:2422-2432. 10.1002/pmic.200401208, 15887183.
63. Cappelletti G, Maggioni MG, Ronchi C, Maci R, Tedeschi G. Protein tyrosine nitration is associated with cold- and drug- resistant microtubules in neuronal-like PC12 cells. Neurosci Lett 2006, 401:159-164. 10.1016/j.neulet.2006.03.009, 16567039.
64. Naoi M, Maruyama W, Shamoto-Nagai M, Akao Y, Tanaka M. Oxidative stress in mithocondria: decision to survival and death of neurons in neurodegenerative disorders. Mol Neurobiol 2005, 31:81-93. 10.1385/MN:31:1-3:081, 15953813.
65. Osen-Sand A, Catsicas M, Staple JK, Jones KA, Ayala G, Knowles J, Grenningloh G, Catsicas S. Inhibition of axonal growth by SNAP-25 antisense oligonucleotides in vitro and in vivo. Nature 1993, 364(6436):445-448. 10.1038/364445a0, 8332215.
66. Vaudry A, Stork PJS, Lazarovici P, Eiden L. Signaling pathways for PC12 cell differentiation: making the right connections. Science 2002, 296:1648-1649. 10.1126/science.1071552, 12040181.
67. Zhang Z, Tarone G, Turner DC. Expression of integrin alpha 1 beta 1 is regulated by nerve growth factor and dexamethasone in PC12 cells. Functional consequences for adhesion and neurite outgrowth. J Biol Chem 1993, 268:5557-5565.
68. Danker K, Mecahi N, Lucka L, Reutter W, Horstkorte R. The small GTPase ras is involved in growth factor-regulated expression of alpha1 integrin subunit in PC12 cells. Biol Chem 2001, 382:969-972.
69. Ivankovic-Dikic I, Gronroos E, Blaukat A, Barth BU, Dikic I. Pyk2 and FAK regulate neurite outgrowth induced by growth factors and integrins. Nat Cell Biol 2000, 2:574-581. 10.1038/35023515, 10980697.
70. Cucina A, Sterpetti AV, Pupelis G, Fragale A, Lepidi S, Cavallaro A, et al. Shear stress induces changes in the morphology and cytoskeleton organization of arterial endothelial cells. Eur J Vasc Endovasc Surg 1995, 9:86-92. 10.1016/S1078-5884(05)80230-8, 7664019.
71. Witteck A, Yao Y, Fechir M, Forstermann U, Kleinert H. Rho protein-mediated changes in the structure of the actin cytoskeleton regulate human inducible NO synthase gene expression. Exp Cell Res 2003, 287:106-115. 10.1016/S0014-4827(03)00129-0, 12799187.
72. Zeng C, Morrison AR. Disruption of the actin cytoskeleton regulates cytokine-induced iNOS expression. Am J Physiol Cell Physiol 2001, 281:C932-C940.
73. Hattori Y, Kasai K. Disruption of the actin cytoskeleton up-regulates iNOS expression in vascular smooth muscle cells. J Cardiovasc Pharmacol 2004, 43:209-213. 10.1097/00005344-200402000-00007, 14716207.
74. Marczin N, Jilling T, Papapetropoulos A, Go C, Catravas JD. Cytoskeleton-dependent activation of the inducible nitric oxide synthase in cultured aortic smooth muscle cells. Br J Pharmacol 1996, 118:1085-1094. 10.1111/j.1476-5381.1996.tb15510.x, 1909607, 8818330.
75. Ory S, Destaing O, Jurdic P. Microtubule dynamics differentially regulates Rho and Rac activity and triggers Rho-independent stress fiber formation in macrophage polykaryons. Eur J Cell Biol 2002, 81:351-362. 10.1078/0171-9335-00255, 12113476.
76. Jung HI, Shin I, Park YM, Kang KW, Ha KS. Colchicine activates actin polymerization by microtubule depolymerization. Mol Cells 1997, 7:431-437.
77. Kajstura J, Sowa G, Wronska D. Induction of DNA synthesis by microtubule depolymerization is mediated by actin filaments. Cytobios 1993, 76:67-74.
78. Zhang JS, Kraus WE, Turskey GA. Stretch-induced nitric oxide modulates mechanical properties of skeletal muscle cells. Am J Physiol Cell Physiol 2004, 287:C292-C299. 10.1152/ajpcell.00018.2004, 15044149.
79. Marechal G, Gailly P. Effects of nitric oxide on the contraction of skeletal muscle. Cell Mol Life Sci 1999, 55:1088-1102. 10.1007/s000180050359, 10442090.
80. Gupta SK, Vlahakis E. Integrin α9β1 mediates enhanced cell migration through nitric oxide synthase activity regulated by Src tyrosine kinase. J Cell Sci 2009, 122:2043-2054. 10.1242/jcs.041632, 2723157, 19470583.
81. Maa MC, Chang MY, Li J, Li YY, Hsieh MY, Yang CJ, et al. The iNOS/Src/FAK axis is critical in Toll-like receptor-mediated cell motility in macrophages. Biochim Biophys Acta 2011, 1813:136-147. 10.1016/j.bbamcr.2010.09.004, 20849883.
82. Miyamoto Y, Sakai R, Maeda C, Takata T, Ihara H, Tsuchiya Y, Watanabe Y. Nitric oxide promotes nicotine-triggered ERK signaling via redox reactions in PC12 cells. Nitric Oxide 2011, 23:344-349.
83. Yamazaki M, Chiba K, Mohri T, Hatanaka H. Activation of the mitogen-activated protein kinase cascade through nitric oxide synthesis as a mechanism of neuritogenenic effect of genipin in PC12h cells. J Neurochem 2001, 79:43-54.
84. Mancuso C, Capone C, Chairomonte Ranieri S, Fusco S, Calabrese V, et al. Bilirubin as an endogenous modulator of neurotrophin redox signaling. J Neurosc Res 2008, 86:2235-2249.
85. Schonhoff CM, Bulseco DA, Brancho DM, Parada LF, Ross AH. The RAs-ERK pathway is required for the induction of neuronal nitric oxide synthase in differentiating PC12 cells. J Neurochem 2001, 78:631-639. 10.1046/j.1471-4159.2001.00432.x, 11483666.
86. Kalisch BE, Demeris CS, Ishak M, Rylett RJ. Modulation of nerve growth factor-induced activation of MAP kinase in PC12 cells by inhibitors of nitric oxide synthase. J Neurochem 2003, 87:1321-1332. 10.1111/j.1471-4159.2003.02057.x, 14713289.
87. Nakata S, Tsutsui M, Shimokawa H, Tamura M, Tasaki H, et al. Vascular neuronal NO synthase is selectively upregulated by platelet-derived growth factor involvement of the MEK/ERK pathway. Arterioscler Thromb Vasc Biol 2005, 25:2502-2508. 10.1161/01.ATV.0000190663.88143.97, 16224055.
88. Chan SHH, Sun EYH, Chang AYW. Extracellular signal-regulated kinase 1/2 plays a pro-life role in experimental brain stem death via MAPK signal-interacting kinase at rostral ventriolateral medulla. J Biomed Sci 2010, 17:17. 10.1186/1423-0127-17-17, 2848001, 20226096.
89. Chrestensen CA, McMurry JL, Salerno JC. MAP kinases bind endothelial nitric oxide synthase. FEBS Open Bio 2012, 2:51-55. 3642102, 23650581.
90. Kumar VB, Viji RI, Kiran MS, Sudhakaran PR. Negative modulation of eNOS by laminin involving post-translational phosphorylation. J Cell Physiol 2009, 219:123-131. 10.1002/jcp.21659, 19097067.
91. Kan WH, Hsu JT, Ba ZS, Schwacha MG, Chen J, et al. P38 MAPK-dependent eNOS upregulation is critical for 17beta-estradiol-mediated cardioprotection following trauma-hemorrhage. Am J Physiol Heart Circ Physiol 2008, 294:H2627-H2636. 10.1152/ajpheart.91444.2007, 18408136.
92. Cragg CL, MacKinnon JC, Kalisch B. Nitric oxide sinthase inhibitors modulate nerve-growth-factor mediated activation of Akt. ISNR Cell Biol 2012, 2012(847974):11. doi:10.5402/2012/847974.