PACAP enhances axon outgrowth in cultured hippocampal neurons to a comparable extent as BDNF

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  Ogata, Katsuya ^a   Shintani, Norihito ^a   Hayata Takano, Atsuko ^b   Kamo, Toshihiko ^a   Higashi, Shintaro ^a   Seiriki, Kaoru ^a   Momosaki, Hisae ^a   Vaudry, David ^c,d   Vaudry, Hubert ^c,d   Galas, Ludovic ^d   Kasai, Atsushi ^a   Nagayasu, Kazuki ^a   Nakazawa, Takanobu ^a   Hashimoto, Ryota ^b,e   Ago, Yukio ^a   Matsuda, Toshio ^a,b   Baba, Akemichi ^f   Hashimoto, Hitoshi ^a,b  

^a OSAKA UNIVERSITY   (Japan)

^b Molecular Research Center for Children's Mental Development   (Japan)

^c UNIVERSITÉ DE ROUEN   (France)

^d UNIVERSITY OF ROUEN   (France)

^e OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^f HYOGO COLLEGE OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; DUAL SPECIFICITY PHOSPHATASE 2; HYPOPHYSIS ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE; K 252A; ADCYAP1 PROTEIN, MOUSE; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; HYPOPHYSIS ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE RECEPTOR 1; VASOACTIVE INTESTINAL POLYPEPTIDE; VASOACTIVE INTESTINAL POLYPEPTIDE RECEPTOR 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL COUNT; CELL STRUCTURE; CONTROLLED STUDY; DENDRITE; FEMALE; FETUS; HIPPOCAMPAL NEURONAL CULTURE; IN VITRO STUDY; NERVE CELL INHIBITION; NERVE FIBER GROWTH; NERVOUS SYSTEM PARAMETERS; NONHUMAN; PROTEIN ANALYSIS; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SOMATIC CELL; ANIMAL; AXON; CELL CULTURE; HIPPOCAMPUS; INSTITUTE FOR CANCER RESEARCH MOUSE; METABOLISM; MOUSE; NERVE CELL; NERVE CELL PLASTICITY; PHYSIOLOGY;

ANIMALS; AXONS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELLS, CULTURED; HIPPOCAMPUS; MICE; MICE, INBRED ICR; NEURONAL PLASTICITY; NEURONS; PITUITARY ADENYLATE CYCLASE-ACTIVATING POLYPEPTIDE; RECEPTOR, TRKB; RECEPTORS, PITUITARY ADENYLATE CYCLASE-ACTIVATING POLYPEPTIDE, TYPE I; RECEPTORS, VASOACTIVE INTESTINAL PEPTIDE, TYPE II; SIGNAL TRANSDUCTION; VASOACTIVE INTESTINAL PEPTIDE;

EID: 84961288459     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0120526     Document Type: Article

References (60)

1. Vaudry D, Falluel-Morel A, Bourgault S, Basille M, Burel D,Wurtz O, et al. Pituitary adenylate cyclase-activating polypeptide and its receptors: 20 years after the discovery. Pharmacol Rev. 2009; 61: 283-357. doi: 10.1124/pr.109.001370 PMID: 19805477
2. Jaworski DM, Proctor MD. Developmental regulation of pituitary adenylate cyclase-activating polypeptide and PAC(1) receptor mRNA expression in the rat central nervous system. Brain Res Dev Brain Res. 2000; 120: 27-39. PMID: 10727727
3. Roberto M, Scuri R, Brunelli M. Differential effects of PACAP-38 on synaptic responses in rat hippocampal CA1 region. Learn Mem. 2001; 8: 265-271. PMID: 11584073
4. Matsuyama S, Matsumoto A, Hashimoto H, Shintani N, Baba A. Impaired long-term potentiation in vivo in the dentate gyrus of pituitary adenylate cyclase-activating polypeptide (PACAP) or PACAP type 1 receptor-mutant mice. Neuroreport 2003; 14: 2095-2098. PMID: 14600504
5. MacDonald JF, Jackson MF, Beazely MA. G protein-coupled receptors control NMDARs and metaplasticity in the hippocampus. Biochim Biophys Acta. 2007; 1768: 941-951. PMID: 17261268
6. Hammack SE, Cheung J, Rhodes KM, Schutz KC, Falls WA, Braas KM, et al. Chronic stress increases pituitary adenylate cyclase-activating peptide (PACAP) and brain-derived neurotrophic factor (BDNF) mRNA expression in the bed nucleus of the stria terminalis (BNST): roles for PACAP in anxiety-like behavior. Psychoneuroendocrinology 2009; 34: 833-843. doi: 10.1016/j.psyneuen.2008.12.013 PMID: 19181454
7. Hashimoto H, Shintani N, Tanida M, Hayata A, Hashimoto R, Baba A. PACAP is implicated in the stress axes. Curr Pharm Des. 2011; 17: 985-989. PMID: 21524255
8. Tsukiyama N, Saida Y, Kakuda M, Shintani N, Hayata A, Morita Y, et al. PACAP centrally mediates emotional stress-induced corticosterone responses in mice. Stress 2011; 14: 368-375. doi: 10.3109/10253890.2010.544345 PMID: 21438773
9. Smith CB, Eiden LE. Is PACAP the major neurotransmitter for stress transduction at the adrenomedullary synapse? J Mol Neurosci. 2012; 48: 403-412. PMID: 22610912
10. Reglodi D, Kiss P, Szabadfi K, Atlasz T, Gabriel R, Horvath G, et al. PACAP is an endogenous protective factor-insights from PACAP-deficient mice. J Mol Neurosci. 2012; 48: 482-492. PMID: 22528455
11. Ohtaki H, Nakamachi T, Dohi K, Aizawa Y, Takaki A, Hodoyama K, et al. Pituitary adenylate cyclaseactivating polypeptide (PACAP) decreases ischemic neuronal cell death in association with IL-6. Proc Natl Acad Sci U S A 2006; 103: 7488-7493. PMID: 16651528
12. Szabadfi K, Atlasz T, Kiss P, Danyadi B, Tamas A, Helyes Z, et al. Mice deficient in pituitary adenylate cyclase activating polypeptide (PACAP) are more susceptible to retinal ischemic injury in vivo. Neurotox Res. 2012; 21: 41-48. doi: 10.1007/s12640-011-9254-y PMID: 21717232
13. Ago Y, Yoneyama M, Ishihama T, Kataoka S, Kawada K, Tanaka T, et al. Role of endogenous pituitary adenylate cyclase-activating polypeptide in adult hippocampal neurogenesis. Neuroscience 2011; 172: 554-561. doi: 10.1016/j.neuroscience.2010.10.044 PMID: 20974227
14. Park H, Poo MM. Neurotrophin regulation of neural circuit development and function. Nat Rev Neurosci. 2013; 14: 7-23. doi: 10.1038/nrn3379 PMID: 23254191
15. Pego JM, Morgado P, Pinto LG, Cerqueira JJ, Almeida OF, Sousa N. Dissociation of the morphological correlates of stress-induced anxiety and fear. Eur J Neurosci. 2008; 27: 1503-1516. doi: 10.1111/j.1460-9568.2008.06112.x PMID: 18336570
16. Hammack SE, Roman CW, Lezak KR, Kocho-Shellenberg M, Grimmig B, Falls WA, et al. Roles for pituitary adenylate cyclase-activating peptide (PACAP) expression and signaling in the bed nucleus of the stria terminalis (BNST) in mediating the behavioral consequences of chronic stress. J Mol Neurosci. 2010; 42: 327-340. doi: 10.1007/s12031-010-9364-7 PMID: 20405238
17. Ishihama T, Ago Y, Shintani N, Hashimoto H, Baba A, Takuma K, et al. Environmental factors during early developmental period influence psychobehavioral abnormalities in adult PACAP-deficient mice. Behav Brain Res. 2010; 209: 274-280. doi: 10.1016/j.bbr.2010.02.009 PMID: 20144662
18. Sakai Y, Hashimoto H, Shintani N, Tomimoto S, Tanaka K, Ichibori A, et al. Involvement of p38 MAP kinase pathway in the synergistic activation of PACAP mRNA expression by NGF and PACAP in PC12h cells. Biochem Biophys Res Commun. 2001; 285: 656-661. PMID: 11453643
19. Watanabe K, Akimoto Y, Yugi K, Uda S, Chung J, Nakamuta S, et al. Latent process genes for cell differentiation are common decoders of neurite extension length. J Cell Sci. 2012; 125: 2198-2211. doi: 10.1242/jcs.097709 PMID: 22344266
20. Monaghan TK, Mackenzie CJ, Plevin R, Lutz EM. PACAP-38 induces neuronal differentiation of human SH-SY5Y neuroblastoma cells via cAMP-mediated activation of ERK and p38 MAP kinases. J Neurochem. 2008; 104: 74-88. PMID: 17995938
21. Cazillis M, Gonzalez BJ, Billardon C, Lombet A, Fraichard A, Samarut J, et al. VIP and PACAP induce selective neuronal differentiation of mouse embryonic stem cells. Eur J Neurosci. 2004; 19: 798-808. PMID: 15009127
22. Lu N, DiCicco-Bloom E. Pituitary adenylate cyclase-activating polypeptide is an autocrine inhibitor of mitosis in cultured cortical precursor cells. Proc Natl Acad Sci U S A 1997; 94: 3357-3362. PMID: 9096398
23. Gonzalez BJ, Basille M, Vaudry D, Fournier A, Vaudry H. Pituitary adenylate cyclase-activating polypeptide promotes cell survival and neurite outgrowth in rat cerebellar neuroblasts. Neuroscience 1997; 78: 419-430. PMID: 9145799
24. Nielsen KM, Chaverra M, Hapner SJ, Nelson BR, Todd V, Zigmond RE, et al. PACAP promotes sensory neuron differentiation: blockade by neurotrophic factors. Mol Cell Neurosci. 2004; 25: 629-641. PMID: 15080892
25. Shi GX, Jin L, Andres DA. Pituitary adenylate cyclase-activating polypeptide 38-mediated Rin activation requires Src and contributes to the regulation of HSP27 signaling during neuronal differentiation. Mol Cell Biol. 2008; 28: 4940-4951. doi: 10.1128/MCB.02193-07 PMID: 18541665
26. Ravni A, Vaudry D, Gerdin MJ, Eiden MV, Falluel-Morel A, Gonzalez BJ, et al. A cAMP-dependent, protein kinase A-independent signaling pathway mediating neuritogenesis through Egr1 in PC12 cells. Mol Pharmacol. 2008; 73: 1688-1708. doi: 10.1124/mol.107.044792 PMID: 18362103
27. Drahushuk K, Connell TD, Higgins D. Pituitary adenylate cyclase-activating polypeptide and vasoactive intestinal peptide inhibit dendritic growth in cultured sympathetic neurons. J Neurosci. 2002; 22: 6560-6569. PMID: 12151535
28. Kambe Y, Miyata A. Role of mitochondrial activation in PACAP dependent neurite outgrowth. J Mol Neurosci. 2012; 48: 550-557. PMID: 22460784
29. Lazarovici P, Cohen G, Arien-Zakay H, Chen J, Zhang C, Chopp M, et al. Multimodal neuroprotection induced by PACAP38 in oxygen-glucose deprivation and middle cerebral artery occlusion stroke models. J Mol Neurosci. 2012; 48: 526-540. PMID: 22678884
30. Henle F, Fischer C, Meyer DK, Leemhuis J. Vasoactive intestinal peptide and PACAP38 control N-methyl-D-aspartic acid-induced dendrite motility by modifying the activities of Rho GTPases and phosphatidylinositol 3-kinases. J Biol Chem. 2006; 281: 24955-24969. PMID: 16803895
31. Yamada K, Matsuzaki S, Hattori T, Kuwahara R, Taniguchi M, Hashimoto H, et al. Increased stathmin1 expression in the dentate gyrus of mice causes abnormal axonal arborizations. PLoS One 2010; 5: e8596. doi: 10.1371/journal.pone.0008596 PMID: 20062533
32. Caceres A, Ye B, Dotti CG. Neuronal polarity: demarcation, growth and commitment. Curr Opin Cell Biol. 2012; 24: 547-553. doi: 10.1016/j.ceb.2012.05.011 PMID: 22726583
33. Dotti CG, Sullivan CA, Banker GA. The establishment of polarity by hippocampal neurons in culture. J Neurosci. 1988; 8: 1454-1468. PMID: 3282038
34. Patel MN, McNamara JO. Selective enhancement of axonal branching of cultured dentate gyrus neurons by neurotrophic factors. Neuroscience 1995; 69: 763-770. PMID: 8596646
35. Labelle C, Leclerc N. Exogenous BDNF, NT-3 and NT-4 differentially regulate neurite outgrowth in cultured hippocampal neurons. Brain Res Dev Brain Res. 2000; 123: 1-11. PMID: 11020545
36. Ji Y, Pang PT, Feng L, Lu B. Cyclic AMP controls BDNF-induced TrkB phosphorylation and dendritic spine formation in mature hippocampal neurons. Nat Neurosci. 2005; 8: 164-172. PMID: 15665879
37. Tajiri M, Hayata-Takano A, Seiriki K, Ogata K, Hazama K, Shintani N, et al. Serotonin 5-HT(7) receptor blockade reverses behavioral abnormalities in PACAP-deficient mice and receptor activation promotes neurite extension in primary embryonic hippocampal neurons: therapeutic implications for psychiatric disorders. J Mol Neurosci. 2012; 48: 473-481. PMID: 22843252
38. Yacoubian TA, Lo DC. Truncated and full-length TrkB receptors regulate distinct modes of dendritic growth. Nat Neurosci. 2000; 3: 342-349. PMID: 10725923
39. Yaka R, He DY, Phamluong K, Ron D. Pituitary adenylate cyclase-activating polypeptide (PACAP(1-38)) enhances N-methyl-D-aspartate receptor function and brain-derived neurotrophic factor expression via RACK1. J Biol Chem. 2003; 278: 9630-9638. PMID: 12524444
40. Lee FS, Rajagopal R, Kim AH, Chang PC, Chao MV. Activation of Trk neurotrophin receptor signaling by pituitary adenylate cyclase-activating polypeptides. J Biol Chem. 2002; 277: 9096-9102. PMID: 11784714
41. ZinkM, Otto C, Zorner B, Zacher C, Schutz G, Henn FA, et al. Reduced expression of brain-derived neurotrophic factor in mice deficient for pituitary adenylate cyclase activating polypeptide type-I-receptor. Neurosci Lett. 2004; 360: 106-108. PMID: 15082190
42. Dong YX, Fukuchi M, Inoue M, Takasaki I, Tabuchi A, Wu CF, et al. Pituitary adenylate cyclase-activating polypeptide (PACAP) is an upstream regulator of prodynorphin mRNA expression in neurons. Neurosci Lett. 2010; 484: 174-177. doi: 10.1016/j.neulet.2010.08.044 PMID: 20728507
43. Sakai Y, Hashimoto H, Shintani N, Katoh H, Negishi M, Kawaguchi C, et al. PACAP activates Rac1 and synergizes with NGF to activate ERK1/2, thereby inducing neurite outgrowth in PC12 cells. Brain Res Mol Brain Res. 2004; 123: 18-26. PMID: 15046862
44. Hashimoto H, Hagihara N, Koga K, Yamamoto K, Shintani N, Tomimoto S, et al. Synergistic induction of pituitary adenylate cyclase-activating polypeptide (PACAP) gene expression by nerve growth factor and PACAP in PC12 cells. J Neurochem. 2000; 74: 501-507. PMID: 10646500
45. Otto C, Kovalchuk Y, Wolfer DP, Gass P, Martin M, Zuschratter W, et al. Impairment of mossy fiber long-term potentiation and associative learning in pituitary adenylate cyclase activating polypeptide type I receptor-deficient mice. J Neurosci. 2001; 21: 5520-5527. PMID: 11466423
46. Hashimoto H, Shintani N, Nishino A, Okabe M, Ikawa M, Matsuyama S, et al. Mice with markedly reduced PACAP (PAC(1)) receptor expression by targeted deletion of the signal peptide. J Neurochem. 2000; 75: 1810-1817. PMID: 11032869
47. Hashimoto H, Shintani N, Tanaka K,Mori W, HiroseM, Matsuda T, et al. Altered psychomotor behaviors in mice lacking pituitary adenylate cyclase-activating polypeptide (PACAP). Proc Natl Acad Sci U S A 2001; 98: 13355-13360. PMID: 11687615
48. Hashimoto H, Hashimoto R, Shintani N, Tanaka K, Yamamoto A, Hatanaka M, et al. Depression-like behavior in the forced swimming test in PACAP-deficient mice: amelioration by the atypical antipsychotic risperidone. J Neurochem. 2009; 110: 595-602. doi: 10.1111/j.1471-4159.2009.06168.x PMID: 19457081
49. Hazama K, Hayata-Takano A, Uetsuki K, Kasai A, Encho N, Shintani N, et al. Increased Behavioral and Neuronal Responses to a Hallucinogenic Drug in PACAP Heterozygous Mutant Mice. PLoS One 2014; 9: e89153. doi: 10.1371/journal.pone.0089153 PMID: 24586556
50. Tanaka K, Shintani N, Hashimoto H, Kawagishi N, Ago Y, Matsuda T, et al. Psychostimulant-induced attenuation of hyperactivity and prepulse inhibition deficits in Adcyap1-deficient mice. J Neurosci. 2006; 26: 5091-5097. PMID: 16687500
51. Gaszner B, Kormos V, Kozicz T, Hashimoto H, Reglodi D, Helyes Z. The behavioral phenotype of pituitary adenylate-cyclase activating polypeptide-deficient mice in anxiety and depression tests is accompanied by blunted c-Fos expression in the bed nucleus of the stria terminalis, central projecting Edinger-Westphal nucleus, ventral lateral septum, and dorsal raphe nucleus. Neuroscience 2012; 202: 283-299. doi: 10.1016/j.neuroscience.2011.11.046 PMID: 22178610
52. Hattori S, Takao K, Tanda K, Toyama K, Shintani N, Baba A, et al. Comprehensive behavioral analysis of pituitary adenylate cyclase-activating polypeptide (PACAP) knockout mice. Front Behav Neurosci. 2012; 6: 58. doi: 10.3389/fnbeh.2012.00058 PMID: 23060763
53. Hashimoto R, Hashimoto H, Shintani N, Chiba S, Hattori S, Okada T, et al. Pituitary adenylate cyclaseactivating polypeptide is associated with schizophrenia. Mol Psychiatry 2007; 12: 1026-1032. PMID: 17387318
54. Freson K, Hashimoto H, Thys C, Wittevrongel C, Danloy S, Morita Y, et al. The pituitary adenylate cy-clase-activating polypeptide is a physiological inhibitor of platelet activation. J Clin Invest. 2004; 113: 905-912. PMID: 15067323
55. Vacic V, McCarthy S, Malhotra D, Murray F, Chou HH, Peoples A, et al. Duplications of the neuropeptide receptor gene VIPR2 confer significant risk for schizophrenia. Nature 2011; 471: 499-503. doi: 10.1038/nature09884 PMID: 21346763
56. Ressler KJ, Mercer KB, Bradley B, Jovanovic T, Mahan A, Kerley K, et al. Post-traumatic stress disorder is associated with PACAP and the PAC1 receptor. Nature 2011; 470: 492-497. doi: 10.1038/nature09856 PMID: 21350482
57. Selemon LD, Goldman-Rakic PS. The reduced neuropil hypothesis: a circuit based model of schizophrenia. Biol Psychiatry 1999; 45: 17-25. PMID: 9894571
58. Sala C, Segal M. Dendritic spines: the locus of structural and functional plasticity. Physiol Rev. 2014; 94: 141-188. doi: 10.1152/physrev.00012.2013 PMID: 24382885
59. Hattori T, Baba K, Matsuzaki S, Honda A, Miyoshi K, Inoue K, et al. A novel DISC1-interacting partner DISC1-Binding Zinc-finger protein: implication in the modulation of DISC1-dependent neurite outgrowth. Mol Psychiatry 2007; 12: 398-407. PMID: 17389905
60. Cheng MC, Chuang YA, Lu CL, Chen YJ, Luu SU, Li JM, et al. Genetic and functional analyses of early growth response (EGR) family genes in schizophrenia. Prog Neuropsychopharmacol Biol Psychiatry 2012; 39: 149-155. doi: 10.1016/j.pnpbp.2012.06.004 PMID: 22691714