Vital role of protein kinase C-related kinase in the formation and stability of neurites during hypoxia

Journal of Neurochemistry

Volumn 113, Issue 2, 2010, Pages 432-446

  Thauerer, Bettina ^a   Zur Nedden, Stephanie ^a,b   Baier Bitterlich, Gabriele ^a  

^a INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^b UNIVERSITY OF WARWICK   (United Kingdom)

Author keywords

Cerebellar granule neurons; Guanosine; Hypoxia; Neuroprotection; Pheochromocytoma cells; Protein kinase C related kinase 1

Indexed keywords

F ACTIN; GUANOSINE; NERVE GROWTH FACTOR; NEUROMODULIN; NEUROTROPHIN; PHOSPHOTRANSFERASE; PROTEIN KINASE C RELATED KINASE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL HYPOXIA; CELL VIABILITY; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; CYTOSKELETON; NERVE CELL; NERVE FIBER GROWTH; NEURITE; NEUROPROTECTION; NONHUMAN; PHEOCHROMOCYTOMA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION;

ANIMALS; ANIMALS, NEWBORN; CELL DEATH; CELL HYPOXIA; CELL SURVIVAL; CELLS, CULTURED; CEREBELLUM; DRUG INTERACTIONS; GAP-43 PROTEIN; GUANOSINE; NERVE GROWTH FACTOR; NEURITES; NEURONS; ONCOGENE PROTEIN V-AKT; PROTEIN KINASE C; RATS; RATS, SPRAGUE-DAWLEY; RNA, SMALL INTERFERING; TRANSFECTION;

EID: 77949745284     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2010.06624.x     Document Type: Article

References (64)

1. Arslan G., Kull B. Fredholm B. B. (1999) Signaling via A2A adenosine receptor in four PC12 cell clones. Naunyn Schmiedebergs Arch. Pharmacol. 359, 28 32.
2. Benowitz L. I., Shashoua V. E. Yoon M. G. (1981) Specific changes in rapidly transported proteins during regeneration of the goldfish optic nerve. J. Neurosci. 1, 300 307.
3. Berger R. Garnier Y. (1999) Pathophysiology of perinatal brain damage. Brain Res. Brain Res. Rev. 30, 107 134.
4. Bito H., Furuyashiki T., Ishihara H., Shibasaki Y., Ohashi K., Mizuno K., Maekawa M., Ishizaki T. Narumiya S. (2000) A critical role for a Rho-associated kinase, p160ROCK, in determining axon outgrowth in mammalian CNS neurons. Neuron 26, 431 441.
5. Bocklinger K., Tomaselli B., Heftberger V., Podhraski V., Bandtlow C. Baier-Bitterlich G. (2004) Purine nucleosides support the neurite outgrowth of primary rat cerebellar granule cells after hypoxia. Eur. J. Cell Biol. 83, 51 54.
6. Boksa P. El-Khodor B. F. (2003) Birth insult interacts with stress at adulthood to alter dopaminergic function in animal models: possible implications for schizophrenia and other disorders. Neurosci. Biobehav. Rev. 27, 91 101.
7. Chen P., Goldberg D. E., Kolb B., Lanser M. Benowitz L. I. (2002) Inosine induces axonal rewiring and improves behavioral outcome after stroke. Proc. Natl Acad. Sci. USA 99, 9031 9036.
8. Ciccarelli R., Di Iorio P., D'Alimonte I., Giuliani P., Florio T., Caciagli F., Middlemiss P. J. Rathbone M. P. (2000) Cultured astrocyte proliferation induced by extracellular guanosine involves endogenous adenosine and is raised by the co-presence of microglia. Glia 29, 202 211.
9. Costello B., Meymandi A. Freeman J. A. (1990) Factors influencing GAP-43 gene expression in PC12 pheochromocytoma cells. J. Neurosci. 10, 1398 1406.
10. D'Alimonte I., Flati V., D'Auro M. et al. (2007) Guanosine inhibits CD40 receptor expression and function induced by cytokines and beta amyloid in mouse microglia cells. J. Immunol. 178, 720 731.
11. Davis S., Vanhoutte P., Pages C., Caboche J. Laroche S. (2000) The MAPK/ERK cascade targets both Elk-1 and cAMP response element-binding protein to control long-term potentiation-dependent gene expression in the dentate gyrus in vivo. J. Neurosci. 20, 4563 4572.
12. El-Khodor B. F. Boksa P. (2000) Transient birth hypoxia increases behavioral responses to repeated stress in the adult rat. Behav. Brain Res. 107, 171 175.
13. Fredholm B. B. (2007) Adenosine, an endogenous distress signal, modulates tissue damage and repair. Cell Death Differ. 14, 1315 1323.
14. Gartner A., Collin L. Lalli G. (2006) Nucleofection of primary neurons. Methods Enzymol. 406, 374 388.
15. Govek E. E., Newey S. E. Van Aelst L. (2005) The role of the Rho GTPases in neuronal development. Genes Dev. 19, 1 49.
16. Greene L. A. Tischler A. S. (1976) Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc. Natl Acad. Sci. USA 73, 2424 2428.
17. Gudi T., Chen J. C., Casteel D. E., Seasholtz T. M., Boss G. R. Pilz R. B. (2002) cGMP-dependent protein kinase inhibits serum-response element-dependent transcription by inhibiting rho activation and functions. J. Biol. Chem. 277, 37382 37393.
18. Gysbers J. W. Rathbone M. P. (1996) Neurite outgrowth in PC12 cells is enhanced by guanosine through both cAMP-dependent and -independent mechanisms. Neurosci. Lett. 220, 175 178.
19. Hatten M. E. (1985) Neuronal regulation of astroglial morphology and proliferation in vitro. J. Cell Biol. 100, 384 396.
20. Hatten M. E., Alder J., Zimmerman K. Heintz N. (1997) Genes involved in cerebellar cell specification and differentiation. Curr. Opin. Neurobiol. 7, 40 47.
21. Heftberger V., Tomaselli B., Podhraski V. Baier-Bitterlich G. (2005) Purine Nucleoside Mediated Protection of Primary Cerebellar Granule Cells after Hypoxic Insult. Nova Science Publishers, Inc, New York.
22. Hide I., Padgett W. L., Jacobson K. A. Daly J. W. (1992) A2A adenosine receptors from rat striatum and rat pheochromocytoma PC12 cells: characterization with radioligand binding and by activation of adenylate cyclase. Mol. Pharmacol. 41, 352 359.
23. Hirose M., Ishizaki T., Watanabe N., Uehata M., Kranenburg O., Moolenaar W. H., Matsumura F., Maekawa M., Bito H. Narumiya S. (1998) Molecular dissection of the Rho-associated protein kinase (p160ROCK)-regulated neurite remodeling in neuroblastoma N1E-115 cells. J. Cell Biol. 141, 1625 1636.
24. Horn A. P., Gerhardt D., Geyer A. B., Valentim L., Cimarosti H., Tavares A., Horn F., Lenz G. Salbego C. (2005) Cellular death in hippocampus in response to PI3K pathway inhibition and oxygen and glucose deprivation. Neurochem. Res. 30, 355 361.
25. Irwin N., Chao S., Goritchenko L., Horiuchi A., Greengard P., Nairn A. C. Benowitz L. I. (2002) Nerve growth factor controls GAP-43 mRNA stability via the phosphoprotein ARPP-19. Proc. Natl Acad. Sci. USA 99, 12427 12431.
26. Ishizaki T., Uehata M., Tamechika I., Keel J., Nonomura K., Maekawa M. Narumiya S. (2000) Pharmacological properties of Y-27632, a specific inhibitor of rho-associated kinases. Mol. Pharmacol. 57, 976 983.
27. Kobayashi S. Millhorn D. E. (1999) Stimulation of expression for the adenosine A2A receptor gene by hypoxia in PC12 cells. A potential role in cell protection. J. Biol. Chem. 274, 20358 20365.
28. Kobayashi S., Conforti L., Pun R. Y. Millhorn D. E. (1998) Adenosine modulates hypoxia-induced responses in rat PC12 cells via the A2A receptor. J. Physiol. 508 (Pt 1 95 107.
29. Kuhar S. G., Feng L., Vidan S., Ross M. E., Hatten M. E. Heintz N. (1993) Changing patterns of gene expression define four stages of cerebellar granule neuron differentiation. Development 117, 97 104.
30. Love S. (2003) Apoptosis and brain ischaemia. Prog. Neuropsychopharmacol. Biol. Psychiatry 27, 267 282.
31. Lu Y. Settleman J. (1999) The Drosophila Pkn protein kinase is a Rho/Rac effector target required for dorsal closure during embryogenesis. Genes Dev. 13, 1168 1180.
32. Mellor H. Parker P. J. (1998) The extended protein kinase C superfamily. Biochem. J. 332 (Pt 2 281 292.
33. Mishra R., Gupta S. K., Meiri K. F., Fong M., Thostrup P., Juncker D. Mani S. (2008) GAP-43 is key to mitotic spindle control and centrosome-based polarization in neurons. Cell Cycle 7, 348 357.
34. Modha R., Campbell L. J., Nietlispach D., Buhecha H. R., Owen D. Mott H. R. (2008) The Rac1 polybasic region is required for interaction with its effector PRK1. J. Biol. Chem. 283, 1492 1500.
35. Mukai H. (2003) The structure and function of PKN, a protein kinase having a catalytic domain homologous to that of PKC. J. Biochem. (Tokyo) 133, 17 27.
36. Mukai H., Miyahara M., Sunakawa H., Shibata H., Toshimori M., Kitagawa M., Shimakawa M., Takanaga H. Ono Y. (1996) Translocation of PKN from the cytosol to the nucleus induced by stresses. Proc. Natl Acad. Sci. USA 93, 10195 10199.
37. Neary J. T., Rathbone M. P., Cattabeni F., Abbracchio M. P. Burnstock G. (1996) Trophic actions of extracellular nucleotides and nucleosides on glial and neuronal cells. Trends Neurosci. 19, 13 18.
38. Nusser N., Gosmanova E., Zheng Y. Tigyi G. (2002) Nerve growth factor signals through TrkA, phosphatidylinositol 3-kinase, and Rac1 to inactivate RhoA during the initiation of neuronal differentiation of PC12 cells. J. Biol. Chem. 277, 35840 35846.
39. O'Driscoll C. M. Gorman A. M. (2005) Hypoxia induces neurite outgrowth in PC12 cells that is mediated through adenosine A2A receptors. Neuroscience 131, 321 329.
40. Oleskovicz S. P., Martins W. C., Leal R. B. Tasca C. I. (2008) Mechanism of guanosine-induced neuroprotection in rat hippocampal slices submitted to oxygen-glucose deprivation. Neurochem. Int. 52, 411 418.
41. Perrone-Bizzozero N. I., Finklestein S. P. Benowitz L. I. (1986) Synthesis of a growth-associated protein by embryonic rat cerebrocortical neurons in vitro. J. Neurosci. 6, 3721 3730.
42. Perrone-Bizzozero N. I., Cansino V. V. Kohn D. T. (1993) Posttranscriptional regulation of GAP-43 gene expression in PC12 cells through protein kinase C-dependent stabilization of the mRNA. J. Cell Biol. 120, 1263 1270.
43. van der Ploeg I., Ahlberg S., Parkinson F. E., Olsson R. A. Fredholm B. B. (1996) Functional characterization of adenosine A2 receptors in Jurkat cells and PC12 cells using adenosine receptor agonists. Naunyn Schmiedebergs Arch. Pharmacol. 353, 250 260.
44. Podhraski V., Tomaselli B. Baier-Bitterlich G. (2005) Adenosine receptor expression in PC12-cells during normoxic and hypoxic conditions. J. Neurochem. Suppl. 2, 210 266.
45. Rathbone M. P., Middlemiss P., Andrew C., Caciagli F., Ciccarelli R., Di Iorio P. Huang R. (1998) The trophic effects of purines and purinergic signaling in pathologic reactions of astrocytes. Alzheimer Dis. Assoc. Disord. 12 (Suppl. 2 S36 S45.
46. Schmidt A. P., Lara D. R. Souza D. O. (2007) Proposal of a guanine-based purinergic system in the mammalian central nervous system. Pharmacol. Ther. 116, 401 416.
47. Seta K. A., Spicer Z., Yuan Y., Lu G. Millhorn D. E. (2002) Responding to hypoxia: lessons from a model cell line. Sci. STKE 2002, RE11.
48. Sitkovsky M. V., Kjaergaard J., Lukashev D. Ohta A. (2008) Hypoxia-adenosinergic immunosuppression: tumor protection by T regulatory cells and cancerous tissue hypoxia. Clin. Cancer Res. 14, 5947 5952.
49. Skene J. H. (1989) Axonal growth-associated proteins. Annu. Rev. Neurosci. 12, 127 156.
50. Snipes G. J., Costello B., McGuire C. B., Mayes B. N., Bock S. S., Norden J. J. Freeman J. A. (1987) Regulation of specific neuronal and nonneuronal proteins during development and following injury in the rat central nervous system. Prog. Brain Res. 71, 155 175.
51. Sun W., Vincent S., Settleman J. Johnson G. L. (2000) MEK kinase 2 binds and activates protein kinase C-related kinase 2. Bifurcation of kinase regulatory pathways at the level of an MAPK kinase kinase. J. Biol. Chem. 275, 24421 24428.
52. Takahashi M., Mukai H., Toshimori M., Miyamoto M. Ono Y. (1998) Proteolytic activation of PKN by caspase-3 or related protease during apoptosis. Proc. Natl Acad. Sci. USA 95, 11566 11571.
53. Thangnipon W., Kingsbury A., Webb M. Balazs R. (1983) Observations on rat cerebellar cells in vitro: influence of substratum, potassium concentration and relationship between neurones and astrocytes. Brain Res. 313, 177 189.
54. Tomaselli B., Podhraski V., Böck G. Baier-Bitterlich G. (2005a) Early cellular responses of purine nucleoside-mediated protection of hypoxia-induced injuries of neuronal PC12 cells. Am. J. Biochem. Biotechnol. 2, 161 167.
55. Tomaselli B., Podhraski V., Heftberger V., Bock G. Baier-Bitterlich G. (2005b) Purine nucleoside-mediated protection of chemical hypoxia-induced neuronal injuries involves p42/44 MAPK activation. Neurochem. Int. 46, 513 521.
56. Tomaselli B., Nedden S. Z., Podhraski V. Baier-Bitterlich G. (2008) p42/44 MAPK is an essential effector for purine nucleoside-mediated neuroprotection of hypoxic PC12 cells and primary cerebellar granule neurons. Mol. Cell. Neurosci. 38, 559 568.
57. Torbett N. E., Casamassima A. Parker P. J. (2003) Hyperosmotic-induced protein kinase N 1 activation in a vesicular compartment is dependent upon Rac1 and 3-phosphoinositide-dependent kinase 1. J. Biol. Chem. 278, 32344 32351.
58. Traversa U., Bombi G., Camaioni E., Macchiarulo A., Costantino G., Palmieri C., Caciagli F. Pellicciari R. (2003) Rat brain guanosine binding site. Biological studies and pseudo-receptor construction. Bioorg. Med. Chem. 11, 5417 5425.
59. Uemura Y., Miller J. M., Matson W. R. Beal M. F. (1991) Neurochemical analysis of focal ischemia in rats. Stroke 22, 1548 1553.
60. Velier J. J., Ellison J. A., Kikly K. K., Spera P. A., Barone F. C. Feuerstein G. Z. (1999) Caspase-8 and caspase-3 are expressed by different populations of cortical neurons undergoing delayed cell death after focal stroke in the rat. J. Neurosci. 19, 5932 5941.
61. Vincent S. Settleman J. (1997) The PRK2 kinase is a potential effector target of both Rho and Rac GTPases and regulates actin cytoskeletal organization. Mol. Cell. Biol. 17, 2247 2256.
62. Zetterstrom T., Vernet L., Ungerstedt U., Tossman U., Jonzon B. Fredholm B. B. (1982) Purine levels in the intact rat brain. Studies with an implanted perfused hollow fibre. Neurosci. Lett. 29, 111 115.
63. Zhu W. H., Conforti L., Czyzyk-Krzeska M. F. Millhorn D. E. (1996) Membrane depolarization in PC-12 cells during hypoxia is regulated by an O2-sensitive K+ current. Am. J. Physiol. 271, C658 C665.
64. Zur Nedden S., Tomaselli B. Baier-Bitterlich G. (2008) HIF-1 alpha is an essential effector for purine nucleoside-mediated neuroprotection against hypoxia in PC12 cells and primary cerebellar granule neurons. J. Neurochem. 105, 1901 1914.