Inhibition of PACAP activity by a receptor antagonist results in changes in cell cycle and apoptotic proteins in chick neuroblasts

Journal of Molecular Neuroscience

Volumn 27, Issue 1, 2005, Pages 107-123

  Erhardt, Nola M ^a   Haines, Lee R ^a   Pearson, Terry W ^a   Sherwood, Nancy M ^a  

^a UNIVERSITY OF VICTORIA   (Canada)

Author keywords

Cell cycle; Differentiation; Flow cytometry; ICAT; Neuroblasts; PACAP; Proteomics; Receptor

Indexed keywords

CELL CYCLE PROTEIN; HYPOPHYSIS ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE; PROTEIN PCAP6 38; RECEPTOR BLOCKING AGENT; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BIOGENESIS; BRAIN MITOCHONDRION; CELL ACTIVITY; CELL CYCLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CHICKEN; CONTROLLED STUDY; FLOW CYTOMETRY; HUMAN; NEUROBLAST; NONHUMAN; PROTEIN ANALYSIS; RECEPTOR BLOCKING; RIBOSOME; TRANSLATION REGULATION;

EID: 23444433920     PISSN: 08958696     EISSN: None     Source Type: Journal    
DOI: 10.1385/JMN:27:1:107     Document Type: Article

References (85)

1. Ahlemeyer B., Fischer D., Kissel T., and Krieglstein J. (2000) Staurosporine-induced apoptosis in cultured chick embryonic neurons is reduced by polyethylenimine of low molecular weight used as a coating substrate. Neurosci. Res. 37, 245-253.
2. Alpini G., Baiocchi L., Glaser S., Ueno Y., Marzioni M., Francis H., et al. (2002) Ursodeoxycholate and tauroursodeoxycholate inhibit cholangiocyte growth and secretion of BDL rats through activation of PKC alpha. Hepatology 35, 1041-1052.
3. Arakura N., Hayama M., Hondo T., Matsuzawa K., Akamatsu T., and Ota H. (2001) Histone H3 mRNA in situ hybridization for identifying proliferating cells in human pancreas, with special reference to the ductal system. Histochem. J. 33, 183-191.
4. Bazar L., Harris V., Sunitha I., Hartmann D., and Avigan M. (1995) Atransactivator of c-mycis coordinately regulated with the proto-oncogene during cellular growth. Oncogene 10, 2229-2238.
5. Bettuzzi S., Scorcioni F., Astancolle S., Davilla P., Scaltriti M., and Corti A. (2002) Clusterin (SGP-2) transient overexpression decreases proliferation rate of SV40-immortalized human prostate epithelial cells by slowing down cell cycle progression. Oncogene 21, 4328-4334.
6. Bevort M. and Leffers H. (2000) Down regulation of ribosomal protein mRNAs during neuronal differentiation of human NTERA2 cells. Differentiation 66, 81-92.
7. Boon K., Caron H. N., van Asperen R., Valenttijn L., Hermus M.- C., van Sluis P., et al. (2001) N-myc enhances the expression of a large set of genes functioning in ribosome biogenesis and protein synthesis. EMBO J. 20, 1383-1393.
8. Brewer G. J., Torricelli J. R., Evege E. K., and Price P. J. (1993) Optimized survival of hippocampal neurons in B27-supplemented Neurobasal™, a new serum-free medium combination. J. Neurosci. Res. 35, 567-576.
9. Bruce J. L., Price B. D., Coleman N., and Calderwood S. K. (1993) Oxidant injury rapidly activates the heat shock transciption factor but fails to increase levels of heatshock proteins. Cancer Res. 53, 12-15.
10. Cabart P., Kalousek I., and Jandova D. (1991) Expresssion of chromosomal protein HMG-1 in transformed and normal human cells. Haematologia 24, 71-75.
11. Carr M. C., Schlussel R. N., Peters C. R., Uchida T., Mandell J., and Freeman M. R. (1995) Expression of cell growth regulated genes in the fetal kidney: relevance to in utero obstruction. J. Urol. 154, 242-246.
12. Chen J.-Y., Dzik J., Edgecombe G. D., Ramsköld L., and Zhou G.-Q. (1995) Apossible early Cambrian chordate. Nature 377, 720-722.
13. Chen T. H., Brody J. R., Romantsev F. E., Yu J. G., Kayler A. E., Voneiff E., etal. (1996) Structure of pp32, an acidic nuclear protein which inhibits oncogene-induced formation of transformed foci. Mol. Biol. Cell. 7, 2045-2056.
14. Clynen E., De Loof A., and Schoofs L. (2003) The use of peptidomics in endocrine research. Gen. Comp. Endocrinol. 132, 1-9.
15. Dang C. V. (1999) c-myc target genes involved in cell growth, apoptosis and metabolism. Mol. Cell. Biol. 19, 1-11.
16. Dawson G. (2000) Mechanisms of apoptosis in embryonic cortical neurons (E6 and E7) in culture involved lipid signalling, protein phosphorylation and caspase activation. Int. J. Dev. Neurosci. 18, 247-257.
17. Delva P., Lechi A., Pastori C., Degan M., Sheiban I., Montesi G., et al. (2002) Collagen I and III mRNA gene expression and cell growth potential of skin fibroblasts in patients with essential hypertension. J. Hypertens. 20, 1393-1399.
18. Dhavan R. and Tsai L.- H. (2001) A decade of Cdk5. Mol. Cell. Biol. 2, 749-759.
19. DiCicco-Bloom E., Deutsch P., Maltzman J., Zhang J., Pintar J., Zheng J., et al. (2000) Autocrine expression and ontogene tic functions of the PACAP ligand/receptor system during sympathetic development. Dev Biol. 219, 197-213.
20. D'Souza S. M. and Brown I. R. (1998) Constitutive expression of heat shock proteins Hsp90, Hsc70, Hsp70 and Hsp60 in neural and non-neural tissues of the rat during post-natal development. Cell Stress Chaperon. 3, 188-199.
21. Duncan R., Collins I., Tomonaga T., Zhang T., and Levens D. (1996) A unique transactivation sequence motif is found in the carboxyl-terminal domain of the single-strand-binding protein FBP. Mol. Cell. Biol. 16, 2274-2282.
22. Erhardt N. M. and Sherwood N. M. (2004) PACAP maintains cell cycling and inhibits apoptosis in chick neuroblasts. Mol. Cell. Endocrinol. 221, 121-134.
23. Erhardt N. M., Fradinger E. A., Cervini L. A., Rivier J. E., and Sherwood N. M. (2001) Early expression of pituitary adenylate cyclase- activatingpolypeptide and activation of its receptor in chick neuroblasts. Endocrinology 142, 1616-1625.
24. Pages C., Nolo R., Huttunen H. J., Eskelinen E.-L., and Rauvala H. (2000) Regulation of cell migration by amphoterin. J. Cell Sci. 113, 611-620.
25. Futcher B., Latter G. I., Monardo P., McLaughlin C. S., and Garrels J. I. (1999) A sampling of the yeast proteome. Mol. Cell. Biol. 19, 7357-7768.
26. Galaviz-Hernandez C., Stagg C., de Ridder G., Tanaka T. S., Ko M. S., Schlessinger D., and Nagaraja R. (2003) Plac8 and Plac9, novel placental-enriched genes identified through microarray analysis. Gene 309, 81-89.
27. Gomez G., Lee H. M., He Q., Englander E. W., Uchida T., and Greeley G. H. J. (2001) Acute pancreatitis signals activation of apoptosis-associated and survival genes in mice. Exp. Biol. Med. 226, 692-700.
28. Gozes I. and Furman S. (2003) VIP and drug design. Curr. Pharm. Des. 9, 483-494.
29. Gygi S. P., Rist B., Gerber S. A., Turecek F., Gelb M. H., and Aebersold R. (1999a) Quantitative analysis of complex protein mixtures using isotope-coded affinity tags. Nat. Biotechnol. 17, 994-999.
30. Gygi S. P., Rist B., Giffin T. J., Eng J., and Aebersold R. (2002) Proteome analysis of low-abundance proteins using multidimensional chromatography and isotope-coded affinity tags. J. Proteome Res. 1, 47-54.
31. Gygi S. P., Rochon Y., Franza B. R., and Aebersold R. (1999b) Correlation between protein and mRNA abundance in yeast. Mol. Cell. Biol. 19, 1720-1730.
32. Handwerger S. and Aronow B. (2003) Dynamic changes in gene expression during human trophoblast differentiation. Recent Prog. Horm. Res. 58, 263-281.
33. Henchcliffe C. and Burke R. E. (1997) Increased expression of cyclin-dependent kinase 5 in induced apoptotic neuronal death in rat substantia nigra. Neurosci. Lett. 230, 41-44.
34. Hölzl H., Kapelari B., Kellerman J., Seemüller E., Sümegi M., Udvardy A., et al. (2000) The regulatory complex of Drosophila melanogaster 26S proteasomes: subunit composition and localization of a deubiquitylating enzyme. J.Cell Biol. 150, 119-129.
35. Howard K. M., Burke L. C., Mailhos C., Pizzey A., Gilbert C. S., Lawson D. W., et al. (1993) Cell cycle arrest of proliferating neuronal cells by serum deprivation can result in either apoptosis or differentiation. J. Neurochem. 60, 1783-1791.
36. Hoyle C. H. V. (1998) Neuropeptide families: evolutionary perspectives. Regul. Pept. 73, 1-33.
37. Irwin N., Baekelandt V., Goritchenko L., and Benowitz L. (1997) Identification of two proteins that bind to a pyrimidine-rich sequence in the 3′-untranslated region of GAP-43 mRNA. Nucleic Acids Res. 25, 1281-1288.
38. Jaffredo T., Vandenbunder B., and Dieterlen-Lièvere F. (1989) In situ study of c-myc protein expression during avian development. Development 105, 679-695.
39. Jiang X., Kim H.-E., Shu H., Zhao Y., Zhang H., Kofron J., et al. (2003) Distinctive roles of PHAP proteins and prothymosin-alpha in a death regulatory pathway. Science 299, 223-226.
40. Johnson K. R., Disney J. E., Wyatt C. R., and Reeves R. (1990) Expression of messenger RNA encoding mammalian chromosomal proteins HMG-1 and HMG-Y during cellular proliferation. Exp. Cell. Res. 187, 69-76.
41. Kinoshita A., Wanibuchi H., Morimura K., Wei M., Shen J., Imaoka S., et al. (2003) Phenobarbital at low dose exerts hormesis inrat hepatocarcinogenesis by reducing oxidative DNA damage, altering cell proliferation, apoptosis and gene expression. Carcinogenesis 24, 1389-1399.
42. Kuniyasu H., Chihara Y., and Takahashi T. (2003) Co-expression of receptor for advanced glycation end products and the ligand amphoterin associates closely with metastasis of colorectal cancer. Oncol. Rep. 10, 445-448.
43. Laburthe M., Couvineau A., and Nicole P. (2003) Molecular pharmacology and structure-function analysis of PACAP/VIP receptors, in Pituitary Adenylate Cyclase-Activating Polypeptide, Vaudry H. and Arimura, A., (eds.), Kluywer Academic Publishers Group, Dordrecht, The Netherlands, pp. 69-94.
44. Lee K. Y., Helbing C. C., Choi K. S., Johnston R. N., and Wang J. H. (1997) Neuronal Cdc2-like kinase (Nclk) binds and phosphorylates the retinoblastoma protein. J. Biol. Chem. 272, 5622-5626.
45. Lew J. and Wang J. H. (1995) Neuronal cdc2-like kinase. Trends Biochem. Sci. 20, 33-37.
46. 1-R) isoforms. J. Neurosci. Res. 53, 651-662.
47. Marzluff W. E and Pandey N. B. (1988) Multiple regulatory steps control histone concentrations. Trends Biol. Sci. 13, 49-52.
48. Mateyak M. K., Obaya A. J., Adachi S., and Sedivy J. M. (1997) Phenotypes of c-myc-deficient rat fibroblasts isolated by targeted homologous recombination. Cell Growth Differ. 8, 1039-1048.
49. McRory J. and Sherwood N. (1997) Two protochordate genes encode pituitary adenylate cyclase-activating polypeptide and related family members. Endocrinology 138, 2380-2390.
50. Merrick W. C. (1992) Mechanism and regulation of eukaryotic protein synthesis. Micobiol. Rev. 56, 291-315.
51. Moorthamer M. and Bhabatosh C. (1999) Identification of ribosomal protein L34 as a novel Cdk5 inhibitor. Biochem. Biophys. Res. Commun. 255, 631-638.
52. Muller S., Scaffidi P., Degryse B., Bonaldi T., Ronfani L., Agresti A., et al. (2001) The double life of HMGB1 chromatin protein: architectural factor and extracellular signal. EMBO J. 20, 4337-4340.
53. Nagao T., Ishida Y., and Kondo Y. (1996) Determination of S-phase cells by in situ hybridization for histone H3 mRNA in hepatocellular carcinoma: correlation with histologic grade and other cell proliferation markers. Mod. Pathol. 9, 99-104.
54. Nicot A. and DiCicco-Bloom E (2001) Regulation of neuroblast mitosis by PACAP receptor isoform expression. Proc. Natl. Acad. Sci. U. S. A. 98, 4658-4763.
55. Patton W. F. (2002) Detection technologies in proteome analysis. J. Chromatogr. B. Analyt. Technol. Biomed. Life Sci. 771, 3-31.
56. Schumm M. A., Castellanos D. A., Frydel B. R., and Sagen J. (2002) Enhanced viability and neuronal differentiation of neural progenitors by chromaffin cell co-culture. Dev. Brain Res. 137, 115-125.
57. Schwartzman R. A. and Cidlowski J. A. (1993) Apoptosis: the biochemistry and molecular biology of programmed cell death. Endocr. Rev. 14, 133-151.
58. Seyedin S. M., Pehrson J. R., and Cole R. D. (1981) Loss of chromosomal high mobility group proteins HMG1 and HMG2 when mouse neuroblastoma and Friend erythroleukemia cells become committed to differentiation. Biochemistry 78, 5988-5992.
59. Shankar S. L., O'Guin K., Cammer M., McMorris F. A., Stitt T. N., Basch R. S., et al. (2003) The growth arrestspecific gene product Gas6 promotes the survival of human oligodendrocytes via a phosphatidylinositol 3-kinase-dependent pathway. J. Neurosci. 23, 4208-4218.
60. Sherwood N. M., Krueckl S. L., and McRory J. R. (2000) The origin and function of the PACAP/glucagon superfamily. Endocr. Rev. 21, 619-670.
61. Shi Y. (2001) A structural view of mitochondria-mediated apoptosis. Nat. Struct. Biol. 8, 394-401.
62. Shiio Y., Donohoe S., Eugene C.-Y., Goodlett D. R., Aebersold R., and Eisenman R. N. (2002) Quantitative proteomic analysis of Myconcoprotein function. EMBO J. 21, 5088-5096.
63. Shin-ichi Y., Hideki Y., Takashi Y., and Kubota H. (2001) Cytosolic chaperonin-containing T-complex polypeptide 1 changes the content of a particular subunit species concomitmant with substrate binding and folding activities during the cycle. Eur. J. Biochem. 268, 4664-4673.
64. Shioda S., Zhou C.-J. I., Ohtaki H., and Yada T. (2003) PACAP receptor signaling, in Pituitary Adenylate Cyclase-Activating Polypeptide, Vaudry H., and Arimura, A., eds., Kluywer Academic Publishers Group, Dordrecht, The Netherlands, pp. 95-124.
65. Shirvan A., Ziv I., Zilkh-Falb R., Machlyn T., Barzilai A., and Melamed E. (1998) Expression of cell cycle-related genes during neuronal apoptosis: is there a distinct pattern? Neurochem. Res. 23, 767-777.
66. Skoulakis E. M. and David R. L. (1998) 14-3-3 proteins in neuronal development and function. Mol. Neurobiol. 16, 269-284.
67. Smith D. S., and Tsai L.-H. (2002) Cdk5 behind the wheel: a role in trafficking and transport? Trends Cell Biol. 12, 28-36.
68. Song C., Wang Q., and Li C. C. H. (2003) ATPase activity of p97 valosin-containing protein (VCP). D2 mediates the major enzyme activity, and D1 contributes to the heat-induced activity. J. Biol. Chem. 278, 3648-3655.
69. Stenger A. M., Garre M. L., Andreussi L., Cama A., Callea F., Brisigotti M., et al. (1992) Expression of histone H3 cell cycle-related gene vimentin and myc genes in pediatric brain tumors. A preliminary analysis showing the different malignant cell growth potential. Mol. Brain Res. 13, 273-275.
70. Stryer L. (1988) Biochemistry, 3rd ed., W. H. Freeman and Company, New York.
71. Tabakoff B., Bhave S. V., and Hoffman P. L. (2003) Selective breeding, quantitative traitlocus analysis, and gene arrays identify candidate genes for complex drug-related behaviors. J. Neurosci. 23, 4491-4498.
72. Tabuchi A., Funaji K., Nakatsubo J., Fukuchi M., Tsuchiya T., and Tsuda M. (2003) Inactivation of aconitase during the apoptosis of mouse cerebellar granule neurons induced by a deprivation of membrane depolarization. J. Neurosci. Res. 71, 504-515.
73. Tang D. and Wang J. H. (1996) Cyclin-dependent kinase 5 (Cdk5) and neuron-specific Cdk5 activators. Prog. Cell Cycle Res. 2, 205-216.
74. Thompson E. B. (1998) The many roles of c-myc in apoptosis. Annu. Rev. Physiol. 60, 575-600.
75. Tsai L.-H., Delalle I., Caviness V. R., Jr., Chae T., and Harlow E. (1994) p35 is a neural-specific regulatory subunit of cyclin-dependent kinase 5. Nature 371, 419-423.
76. Udtha M., Lee S. J., Alam R., Coombes K., and Huff V. (2003) Upregulation of c-MYC in WT-1-mutanttumors: assessment of WT1 putative transcriptional targets using cDNA microarray expression profiling of genetically defined Wilms' tumors. Oncogene 22, 3821-3826.
77. Vaudry D., Chen Y., Ravni A., Hamelink C., Elkahloun A., and Eiden E. (2002) Analysis of the PC12 transcriptome after differentiation with pituitary adenylate cyclase-activating polypeptide (PACAP). J. Neurochem. 83, 1272-1284
78. Villa P., Miehe M., Sensenbrenner M., and Pettman B. (1994) Synthesis of specific proteins in trophic factor-deprived neurons undergoing apoptosis. J. Neurochem. 62, 1468-1475.
79. Weisner D. A. and Dawson G. (1996) Staurosporine induces programmed cell death in embryonic neurons and activation of the ceramide pathway. J. Neurochem. 66, 1418-1425.
80. Won K.-A., Schumaker R. J., Farr G. W., Horwich A. L., and Reed S. I. (1998) Maturation of human cyclin E requires the function of the eukaryotic chaperonin CCT. Mol. Cell. Biol. 18, 7584-7589.
81. Yaffe M. B. (2002) How do 14-3-3 proteins work? Gatekeeper phophorylation and the molecular anvil hypothesis. FEBS Lett. 513, 53-57.
82. Yamamura J.-I., Takada Y., Goto M., Kumegawa M., and Aoe S. (1999) High mobility group-like protein inbovine milk stimulates the proliferation of osteoblastic MC3T3-E1 cells. Biochem. Biophys. Res. Commun. 261, 113-117.
83. Yokoyama Y, Ozawa S., Seyama Y, Maniki H., Hayashi Y, Kaji K., et al. (1997) Enhancement of apoptosis in developing chick neural retina cells by basic fibroblast growth factor. J. Neurochem. 68, 2212-2215.
84. Zha J., Harada H., Yang E., Jockei J., and Korsmeyer J. (1996) Serine phosphorylation of death agonist BAD in response to survival factor results in binding to 14-3-3 not Bcl-XL. Cell Tissue Res. 87, 619-628.
85. Zhang Q., Ahuja H. S., Zakeri Z., and Wolgemuth D. J. (1997) Cyclin-dependent kinase 5 is associated with a apoptotic cell death during development and tissue remodeling. Dev. Biol. 183, 222-233.