The akt-nitric oxide-cGMP pathway contributes to nerve growth factor-mediated neurite outgrowth in apolipoprotein E knockout mice

Journal of Pharmacology and Experimental Therapeutics

Volumn 338, Issue 2, 2011, Pages 694-700

  Hashikawa Hobara, Narumi ^a   Hashikawa, Naoya ^a   Yutani, Chikao ^a   Zamami, Yoshito ^b   Jin, Xin ^b   Takatori, Shingo ^b   Mio, Mitsunobu ^c   Kawasaki, Hiromu ^b  

^a OKAYAMA UNIVERSITY OF SCIENCE   (Japan)

^b OKAYAMA UNIVERSITY   (Japan)

^c SHUJITSU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

8 BROMO CYCLIC GMP; APOLIPOPROTEIN E; CALCITONIN GENE RELATED PEPTIDE; CYCLIC GMP; MESSENGER RNA; N ACETYL S NITROSOPENICILLAMINE; NERVE GROWTH FACTOR; NERVE GROWTH FACTOR RECEPTOR; NITRIC OXIDE; NITROPRUSSIDE SODIUM; PROTEIN KINASE B;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; KNOCKOUT MOUSE; MALE; MESENTERIC ARTERY; MOUSE; NERVE FIBER GROWTH; NERVE REGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPINAL GANGLION; WILD TYPE;

ANIMALS; APOLIPOPROTEINS E; CALCITONIN GENE-RELATED PEPTIDE; CELLS, CULTURED; CYCLIC GMP; MALE; MICE; MICE, KNOCKOUT; NERVE GROWTH FACTOR; NEURAL PATHWAYS; NEURITES; NEUROGENESIS; NITRIC OXIDE; PAIN MEASUREMENT; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION;

EID: 79960548059     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.111.181487     Document Type: Article

References (31)

1. Akassoglou K (2005) Nerve growth factor-independent neuronal survival: a role for NO donors. Mol Pharmacol 68:952-955.
2. Boyles JK, Pitas RE, Wilson E, Mahley RW, and Taylor JM (1985) Apolipoprotein E associated with astrocytic glia of the central nervous system and with nonmyelinating glia of the peripheral nervous system. J Clin Invest 76:1501-1513. (Pubitemid 16193568)
3. Brunet A, Datta SR, and Greenberg ME (2001) Transcription-dependent and -independent control of neuronal survival by the PI3K-Akt signaling pathway. Curr Opin Neurobiol 11:297-305. (Pubitemid 32524094)
4. Crowder RJ and Freeman RS (1998) Phosphatidylinositol 3-kinase and Akt protein kinase are necessary and sufficient for the survival of nerve growth factordependent sympathetic neurons. J Neurosci 18:2933-2943. (Pubitemid 28163223)
5. Cunha TM, Roman-Campos D, Lotufo CM, Duarte HL, Souza GR, Verri WA Jr, Funez MI, Dias QM, Schivo IR, Domingues AC, et al. (2010) Morphine peripheral analgesia depends on activation of the PI3Kγ/AKT/nNOS/NO/KATP signaling pathway. Proc Natl Acad Sci USA 107:4442-4447.
6. Culmsee C, Gerling N, Landshamer S, Rickerts B, Duchstein HJ, Umezawa K, Klumpp S, and Krieglstein J (2005) Nitric oxide donors induce neurotrophin-like survival signaling and protect neurons against apoptosis. Mol Pharmacol 68:1006-1017. (Pubitemid 41345792)
7. Durham PL and Russo AF (2003) Stimulation of the calcitonin gene-related peptide enhancer by mitogen-activated protein kinases and repression by an antimigraine drug in trigeminal ganglia neurons. J Neurosci 23:807-815. (Pubitemid 36206171)
8. Eddy NB and Leimbach D (1953) Synthetic analgesics. II. Dithienylbutenyl- and dithienylbutylamines. J Pharmacol Exp Ther 107:385-393.
9. Freeland K, Liu YZ, and Latchman DS (2000) Distinct signalling pathways mediate the cAMP response element (CRE)-dependent activation of the calcitonin gene- related peptide gene promoter by cAMP and nerve growth factor. Biochem J 345:233-238. (Pubitemid 30077162)
10. Fullerton SM, Strittmatter WJ, and Matthew WD (1998) Peripheral sensory nerve defects in apolipoprotein E knockout mice. Exp Neurol 153:156-163. (Pubitemid 28452308)
11. Han G, Ma H, Chintala R, Miyake K, Fulton DJ, Barman SA, and White RE (2007) Nongenomic, endothelium-independent effects of estrogen on human coronary smooth muscle are mediated by type I (neuronal) NOS and PI3-kinase-Akt signaling. Am J Physiol Heart Circ Physiol 293:H314-H321. (Pubitemid 47105087)
12. Hobara N, Gessei-Tsutsumi N, Goda M, Takayama F, Akiyama S, Kurosaki Y, and Kawasaki H (2005) Long-term inhibition of angiotensin prevents reduction of periarterial innervation of calcitonin gene-related peptide (CGRP)-containing nerves in spontaneously hypertensive rats. Hypertens Res 28:465-474. (Pubitemid 41007462)
13. Hobara N, Goda M, Kitamura Y, Takayama F, and Kawasaki H (2006) Innervation and functional changes in mesenteric perivascular calcitonin gene-related peptideand neuropeptide Y-containing nerves following topical phenol treatment. Neuroscience 141:1087-1099. (Pubitemid 44066641)
14. Holtzman DM, Pitas RE, Kilbridge J, Nathan B, Mahley RW, Bu G, and Schwartz AL (1995) Low density lipoprotein receptor-related protein mediates apolipoprotein E-dependent neurite outgrowth in a central nervous system-derived neuronal cell line. Proc Natl Acad Sci USA 92:9480-9484.
15. Ignatius MJ, Gebicke-Härter PJ, Skene JH, Schilling JW, Weisgraber KH, Mahley RW, and Shooter EM (1986) Expression of apolipoprotein E during nerve degeneration and regeneration. Proc Natl Acad Sci USA 83:1125-1129. (Pubitemid 16086425)
16. Jones DM, Tucker BA, Rahimtula M, and Mearow KM (2003) The synergistic effects of NGF and IGF-1 on neurite growth in adult sensory neurons: convergence on the PI 3-kinase signaling pathway. J Neurochem 86:1116-1128. (Pubitemid 37022188)
17. Komagiri Y and Kitamura N (2003) Effect of intracellular dialysis of ATP on the hyperpolarization-activated cation current in rat dorsal root ganglion neurons. J Neurophysiol 90:2115-2122. (Pubitemid 37266482)
18. Kosacka J, Nowicki M, Kacza J, Borlak J, Engele J, and Spanel-Borowski K (2006) Adipocyte-derived angiopoietin-1 supports neurite outgrowth and synaptogenesis of sensory neurons. J Neurosci Res 83:1160-1169. (Pubitemid 43667999)
19. LeBlanc AC and Poduslo JF (1990) Regulation of apolipoprotein E gene expression after injury of the rat sciatic nerve. J Neurosci Res 25:162-171. (Pubitemid 20093966)
20. Lindsay RM and Harmar AJ (1989) Nerve growth factor regulates expression of neuropeptide genes in adult sensory neurons. Nature 337:362-364. (Pubitemid 19043498)
21. Masliah E, Mallory M, Veinbergs I, Miller A, and Samuel W (1996) Alterations in apolipoprotein E expression during aging and neurodegeneration. Prog Neurobiol 50:493-503. (Pubitemid 27032265)
22. Maysinger D, Holmes M, Han X, Epand RM, Pertens E, Foerster A, Barlas C, Holtzman DM, and Diamond J (2008) Ceramide is responsible for the failure of compensatory nerve sprouting in apolipoprotein E knock-out mice. J Neurosci 28:7891-7899.
23. Nathan BP, Barsukova AG, Shen F, McAsey M, and Struble RG (2004) Estrogen facilitates neurite extension via apolipoprotein E in cultured adult mouse cortical neurons. Endocrinology 145:3065-3073. (Pubitemid 38829971)
24. Nathan BP, Jiang Y, Wong GK, Shen F, Brewer GJ, and Struble RG (2002) Apolipoprotein E4 inhibits, and apolipoprotein E3 promotes neurite outgrowth in cultured adult mouse cortical neurons through the low-density lipoprotein receptorrelated protein. Brain Res 928:96-105. (Pubitemid 34159056)
25. Pola R, Gaetani E, Flex A, Aprahamian T, Proia AS, Bosch-Marcé M, Smith RC, and Pola P (2003) Peripheral nerve ischemia: apolipoprotein E deficiency results in impaired functional recovery and reduction of associated intraneural angiogenic response. Exp Neurol 184:264-273. (Pubitemid 37444036)
26. Qiu Z, Hyman BT, and Rebeck GW (2004) Apolipoprotein E receptors mediate neurite outgrowth through activation of p44/42 mitogen-activated protein kinase in primary neurons. J Biol Chem 279:34948-34956. (Pubitemid 39318131)
27. Sofroniew MV, Howe CL, and Mobley WC (2001) Nerve growth factor signaling, neuroprotection, and neural repair. Annu Rev Neurosci 24:1217-1281. (Pubitemid 32695259)
28. Stoll G, Meuller HW, Trapp BD, and Griffin JW (1989) Oligodendrocytes but not astrocytes express apolipoprotein E after injury of rat optic nerve. Glia 2:170-176.
29. Supowit SC, Zhao H, and DiPette DJ (2001) Nerve growth factor enhances calcitonin gene-related peptide expression in the spontaneously hypertensive rat. Hypertension 37:728-732. (Pubitemid 32199057)
30. Yamazaki M, Chiba K, and Mohri T (2005) Fundamental role of nitric oxide in neuritogenesis of PC12h cells. Br J Pharmacol 146:662-669. (Pubitemid 41573617)
31. Yao R and Cooper GM (1995) Requirement for phosphatidylinositol-3 kinase in the prevention of apoptosis by nerve growth factor. Science 267:2003-2006.