Pituitary Adenylate Cyclase-Activating Polypeptide (PACAP) impairs the regulation of apoptosis in megakaryocytes by activating NF-κB: A proteomic study

Molecular and Cellular Proteomics

Volumn 11, Issue 1, 2012, Pages

  Michele, Michela Di ^a   Peeters, Karen ^a   Loyen, Serena ^a   Thys, Chantel ^a   Waelkens, Etienne ^a   Overbergh, Lutgart ^a   Hoylaerts, Marc ^a   Van Geet, Christel ^a   Freson, Kathleen ^a  

^a UNIVERSITY HOSPITALS LEUVEN   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

HETERODIMER; HYPOPHYSIS ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE; I KAPPA B KINASE BETA; RNA; VASOACTIVE INTESTINAL POLYPEPTIDE RECEPTOR 1; CYCLIC AMP; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN;

ADULT; APOPTOSIS; ARTICLE; BIOINFORMATICS; CELL CYCLE; CONTROLLED STUDY; DATA ANALYSIS; DOWN REGULATION; DOWNSTREAM PROCESSING; DRUG MECHANISM; GEL ELECTROPHORESIS; GENE EXPRESSION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MALE; MEGAKARYOCYTE; META ANALYSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN PROCESSING; PROTEOMICS; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; THROMBOCYTE FUNCTION; TRANSCRIPTOMICS; UPREGULATION; CELL LINE; DRUG EFFECT; LEUKOCYTE; MASS SPECTROMETRY; METABOLISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ADULT; APOPTOSIS; CELL LINE; CYCLIC AMP; GENE EXPRESSION; HUMANS; LEUKOCYTES; MALE; MEGAKARYOCYTES; NF-KAPPA B; PITUITARY ADENYLATE CYCLASE-ACTIVATING POLYPEPTIDE; PROTEOMICS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

EID: 84856076396     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M111.007625     Document Type: Article

References (60)

1. Miyata, A., Arimura, A., Dahl, R. R., Minamino, N., Uehara, A., Jiang, L., Culler, M. D., and Coy, D. H. (1989) Isolation of a novel 38 residue-hypothalamic polypeptide which stimulates adenylate cyclase in pituitary cells. Biochem. Biophys. Res. Commun. 164, 567-574 (Pubitemid 19269770)
2. Vaudry, D., Gonzalez, B. J., Basille, M., Yon, L., Fournier, A., and Vaudry, H. (2000) Pituitary adenylate cyclase-activating polypeptide and its receptors: from structure to functions. Pharmacol. Rev. 52, 269-324 (Pubitemid 30368434)
3. Freson, K., Peeters, K., De Vos, R., Wittevrongel, C., Thys, C., Hoylaerts, M. F., Vermylen, J., and Van Geet, C. (2008) PACAP and its receptor VPAC1 regulate megakaryocyte maturation: therapeutic implications. Blood 111, 1885-1893 (Pubitemid 351451497)
4. Nam, C., Case, A. J., Hostager, B. S., and O'Dorisio, M. S. (2009) The role of vasoactive intestinal peptide (VIP) in megakaryocyte proliferation. J. Mol. Neurosci. 37, 160-167
5. Freson, K., Hashimoto, H., Thys, C., Wittevrongel, C., Danloy, S., Morita, Y., Shintani, N., Tomiyama, Y., Vermylen, J., Hoylaerts, M. F., Baba, A., and Van Geet, C. (2004) The pituitary adenylate cyclase-activating polypeptide is a physiological inhibitor of platelet activation. J. Clin. Invest. 113, 905-912 (Pubitemid 38544149)
6. Peeters, K., Stassen, J. M., Collen, D., Van Geet, C., and Freson, K. (2008) Emerging treatments for thrombocytopenia: increasing platelet production. Drug Discov. Today 13, 798-806
7. Unlü, M., Morgan, M. E., and Minden, J. S. (1997) Difference gel electrophoresis: a single gel method for detecting changes in protein extracts. Electrophoresis 18, 2071-2077 (Pubitemid 27501267)
8. Marouga, R., David, S., and Hawkins, E. (2005) The development of the DIGE system: 2D fluorescence difference gel analysis technology. Anal. Bioanal. Chem. 382, 669-678 (Pubitemid 40890994)
9. Alfonso, P., Núñez, A., Madoz-Gurpide, J., Lombardia, L., Sánchez, L., and Casal, J. I. (2005) Proteomic expression analysis of colorectal cancer by two-dimensional differential gel electrophoresis. Proteomics 5, 2602-2611 (Pubitemid 40966487)
10. Cicchillitti, L., Di Michele, M., Urbani, A., Ferlini, C., Donat, M. B., Scambia, G., and Rotilio, D. (2009) Comparative proteomic analysis of paclitaxel sensitive A2780 epithelial ovarian cancer cell line and its resistant counterpart A2780TC1 by 2D-DIGE: the role of ERp57. J. Proteome Res. 8, 1902-1912
11. Di Michele, M., Della Corte, A., Cicchillitti, L., Del Boccio, P., Urbani, A., Ferlini, C., Scambia, G., Donati, M. B., and Rotilio, D. (2009) A proteomic approach to paclitaxel chemoresistance in ovarian cancer cell lines. Biochim. Biophys. Acta 1794, 225-236
12. Benjamini, Y., and Hochberg, Y. (2000) On the adaptive control of the false discovery rate in multiple testing with independent statistics. J. Educ. Behav. Stat. 25, 60-83
13. Shevchenko, A., Wilm, M., Vorm, O., and Mann, M. (1996) Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68, 850-858
14. Elias, J. E., Haas, W., Faherty, B. K., and Gygi, S. P. (2005) Comparative evaluation of mass spectrometry platforms used in large-scale proteomics investigations. Nat. Methods 2, 667-675 (Pubitemid 41223093)
15. Gourlet, P., De Neef, P., Cnudde, J., Waelbroeck, M., and Robberecht, P. (1997) In vitro properties of a high affinity selective antagonist of the VIP1 receptor. Peptides 18, 1555-1560 (Pubitemid 28132998)
16. Yang, Y., Thannhauser, T. W., Li, L., and Zhang, S. (2007) Development of an integrated approach for evaluation of 2-D gel image analysis: impact of multiple proteins in single spots on comparative proteomics in conventional 2-D gel/MALDI workflow. Electrophoresis 28, 2080-2094
17. Sato-Kusubata, K., Yajima, Y., and Kawashima, S. (2000) Persistent activation of Gsalpha through limited proteolysis by calpain. Biochem. J. 347, 733-740 (Pubitemid 30260963)
18. Yu, Z., Luo, H., Fu, W., and Mattson, M. P. (1999) The endoplasmic reticulum stress-responsive protein GRP78 protects neurons against excitotoxicity and apoptosis: suppression of oxidative stress and stabilization of calcium homeostasis. Exp. Neurol. 155, 302-314 (Pubitemid 29124724)
19. Rocher, G., Letourneux, C., Lenormand, P., and Porteu, F. (2007) Inhibition of B56-containing protein phosphatase 2As by the early response gene IEX-1 leads to control of Akt activity. J. Biol. Chem. 282, 5468-5477 (Pubitemid 47093774)
20. Ma, X., Ren, X., Han, P., Hu, S., Wang, J., and Yin, J. (2010) SiRNA against Fabp5 induces 3T3-L1 cells apoptosis during adipocytic induction. Mol. Biol. Rep. 37, 4003-4011
21. Schamberger, C. J., Gerner, C., and Cerni, C. (2005) Caspase-9 plays a marginal role in serum starvation-induced apoptosis. Exp. Cell Res. 302, 115-128 (Pubitemid 39482373)
22. Pascal, V., Nathan, N. R., Claudio, E., Siebenlist, U., and Anderson, S. K. (2007) NF-kappa B p50/p65 affects the frequency of Ly49 gene expression by NK cells. J. Immunol. 179, 1751-1759
23. Fugman, D. A., Witte, D. P., Jones, C. L., Aronow, B. J., and Lieberman, M. A. (1990) In vitro establishment and characterization of a human megakaryoblastic cell line. Blood 75, 1252-1261 (Pubitemid 20107291)
24. Dorn, G. W., 2nd, and Davis, M. G. (1992) Differential megakaryocytic desensitization to platelet agonists. Am. J. Physiol. 263, C864-72
25. Yang, M., Khachigian, L. M., Hicks, C., Chesterman, C. N., and Chong, B. H. (1997) Identification of PDGF receptors on human megakaryocytes and megakaryocytic cell lines. Thromb. Haemost. 78, 892-896 (Pubitemid 27365590)
26. van der Vuurst, H., van Willigen, G., van Spronsen, A., Hendriks, M., Donath, J., and Akkerman, J. W. (1997) Signal transduction through trimeric G proteins in megakaryoblastic cell lines. Arterioscler. Thromb. Vasc. Biol. 17, 1830-1836 (Pubitemid 27424008)
27. Conran, N., and Hemming, F. W. (1999) Phorbol ester induces a transient increase in alpha 5 beta 1-mediated adhesion of the megakaryoblastic cell line CHRF 288-11. Platelets 10, 117-123 (Pubitemid 29182279)
28. den Dekker, E., Heemskerk, J. W., Gorter, G., van der Vuurst, H., Donath, J., Kroner, C., Mikoshiba, K., and Akkerman, J. W. (2002) Cyclic AMP raises intracellular Ca(2+) in human megakaryocytes independent of protein kinase A. Arterioscler. Thromb. Vasc. Biol. 22, 179-186 (Pubitemid 34076251)
29. Yang, M., Li, K., Ng, M. H., Yuen, P. M., Fok, T. F., Li, C. K., Hogg, P. J., and Chong, B. H. (2003) Thrombospondin-1 inhibits in vitro megakaryocytopoiesis via CD36. Thromb. Res. 109, 47-54 (Pubitemid 36385047)
30. Chui, C. M., Li, K., Yang, M., Chuen, C. K., Fok, T. F., Li, C. K., and Yuen, P. M. (2003) Platelet-derived growth factor up-regulates the expression of transcription factors NF-E2, GATA-1 and c-Fos in megakaryocytic cell lines. Cytokine 21, 51-64 (Pubitemid 36369391)
31. Fuhrken, P. G., Chen, C., Miller, W. M., and Papoutsakis, E. T. (2007) Comparative, genome-scale transcriptional analysis of CHRF-288-11 and primary human megakaryocytic cell cultures provides novel insights into lineage-specific differentiation. Exp. Hematol. 35, 476-489
32. Vaudry, D., Chen, Y., Ravni, A., Hamelink, C., Elkahloun, A. G., and Eiden, L. E. (2002) Analysis of the PC12 cell transcriptome after differentiation with pituitary adenylate cyclase-activating polypeptide (PACAP). J. Neurochem. 83, 1272-1284 (Pubitemid 35477467)
33. Grumolato, L., Elkahloun, A. G., Ghzili, H., Alexandre, D., Coulouarn, C., Yon, L., Salier, J. P., Eiden, L. E., Fournier, A., Vaudry, H., and Anouar, Y. (2003) Microarray and suppression subtractive hybridization analyses of gene expression in pheochromocytoma cells reveal pleiotropic effects of pituitary adenylate cyclase-activating polypeptide on cell proliferation, survival, and adhesion. Endocrinology 144, 2368-2379 (Pubitemid 36637089)
34. Ishido, M., and Masuo, Y. (2004) Transcriptome of pituitary adenylate cyclase-activating polypeptide-differentiated PC12 cells. Regul. Pep.t 123, 15-21 (Pubitemid 39424144)
35. Radley, J. M., and Haller, C. J. (1983) Fate of senescent megakaryocytes in the bone marrow. Br. J. Haematol. 53, 277-287 (Pubitemid 13171502)
36. Zauli, G., Vitale, M., Falcieri, E., Gibellini, D., Bassini, A., Celeghini, C., Columbaro, M., and Capitani, S. (1997) In vitro senescence and apoptotic cell death of human megakaryocytes. Blood 90, 2234-2243 (Pubitemid 27392707)
37. Falcieri, E., Bassini, A., Pierpaoli, S., Luchetti, F., Zamai, L., Vitale, M., Guidotti, L., and Zauli, G. (2000) Ultrastructural characterization of maturation, platelet release, and senescence of human cultured megakaryocytes. Anat. Rec. 258, 90-99 (Pubitemid 30030459)
38. De Botton, S., Sabri, S., Daugas, E., Zermati, Y., Guidotti, J. E., Hermine, O., Kroemer, G., Vainchenker, W., and Debili, N. (2002) Platelet formation is the consequence of caspase activation within megakaryocytes. Blood 100, 1310-1317 (Pubitemid 34864286)
39. Morison, I. M., Cramer Bordé, E. M., Cheesman, E. J., Cheong, P. L., Holyoake, A. J., Fichelson, S., Weeks, R. J., Lo, A., Davies, S. M., Wilbanks, S. M., Fagerlund, R. D., Ludgate, M. W., da Silva Tatley, F. M., Coker, M. S., Bockett, N. A., Hughes, G., Pippig, D. A., Smith, M. P., Capron, C., and Ledgerwood, E. C. (2008) A mutation of human cytochrome c enhances the intrinsic apoptotic pathway but causes only thrombocytopenia. Nat. Genet. 40, 387-389 (Pubitemid 351450877)
40. McDonnell, T. J., Deane, N., Platt, F. M., Nunez, G., Jaeger, U., McKearn, J. P., and Korsmeyer, S. J. (1989) bcl-2-immunoglobulin transgenic mice demonstrate extended B cell survival and follicular lymphoproliferation. Cell 57, 79-88 (Pubitemid 19098870)
41. Sentman, C. L., Shutter, J. R., Hockenbery, D., Kanagawa, O., and Korsmeyer, S. J. (1991) bcl-2 inhibits multiple forms of apoptosis but not negative selection in thymocytes. Cell 67, 879-888 (Pubitemid 121001502)
42. Ogilvy, S., Metcalf, D., Print, C. G., Bath, M. L., Harris, A. W., and Adams, J. M. (1999) Constitutive Bcl-2 expression throughout the hematopoietic compartment affects multiple lineages and enhances progenitor cell survival. Proc. Natl. Acad. Sci. U.S.A. 96, 14943-14948 (Pubitemid 30019744)
43. Bouillet, P., Metcalf, D., Huang, D. C., Tarlinton, D. M., Kay, T. W., Köntgen, F., Adams, J. M., and Strasser, A. (1999) Proapoptotic Bcl-2 relative Bim required for certain apoptotic responses, leukocyte homeostasis, and to preclude autoimmunity. Science 286, 1735-1738 (Pubitemid 129515880)
44. Lee, H. H., Dadgostar, H., Cheng, Q., Shu, J., and Cheng, G. (1999) NF-kappaB-mediated up-regulation of Bcl-x and Bfl-1/A1 is required for CD40 survival signaling in B lymphocytes. Proc. Natl. Acad. Sci. U.S.A. 96, 9136-9141 (Pubitemid 29374720)
45. Spinelli, S. L., Casey, A. E., Pollock, S. J., Gertz, J. M., McMillan, D. H., Narasipura, S. D., Mody, N. A., King, M. R., Maggirwar, S. B., Francis, C. W., Taubman, M. B., Blumberg, N., and Phipps, R. P. (2010) Platelets and megakaryocytes contain functional nuclear factor-kappaB. Arterioscler. Thromb. Vasc. Biol. 30, 591-598
46. Kim, K. W., Kim, S. H., Lee, E. Y., Kim, N. D., Kang, H. S., Kim, H. D., Chung, B. S., and Kang, C. D. (2001) Extracellular signal-regulated kinase/90-KDA ribosomal S6 kinase/nuclear factor-kappa B pathway mediates phorbol 12-myristate 13-acetate-induced megakaryocytic differentiation of K562 cells. J. Biol. Chem. 276, 13186-13191
47. Zhang, Y., Sun, S., Wang, Z., Thompson, A., Kaluzhny, Y., Zimmet, J., and Ravid, K. (2002) Signaling by the Mpl receptor involves IKK and NF-kappaB. J. Cell. Biochem. 85, 523-535 (Pubitemid 34465132)
48. Ahmad, N., Gupta, S., and Mukhtar, H. (2000) Green tea polyphenol epigallocatechin-3-gallate differentially modulates nuclear factor kappaB in cancer cells versus normal cells. Arch. Biochem. Biophys. 376, 338-346 (Pubitemid 30210882)
49. Estrov, Z., Shishodia, S., Faderl, S., Harris, D., Van, Q., Kantarjian, H. M., Talpaz, M., and Aggarwal, B. B. (2003) Resveratrol blocks interleukin-1beta-induced activation of the nuclear transcription factor NF-kappaB, inhibits proliferation, causes S-phase arrest, and induces apoptosis of acute myeloid leukemia cells. Blood 102, 987-995 (Pubitemid 36917794)
50. Chendil, D., Ranga, R. S., Meigooni, D., Sathishkumar, S., and Ahmed, M. M. (2004) Curcumin confers radiosensitizing effect in prostate cancer cell line PC-3. Oncogene 23, 1599-1607 (Pubitemid 38406523)
51. Shishodia, S., and Aggarwal, B. B. (2004) Guggulsterone inhibits NF-kappaB and IkappaBalpha kinase activation, suppresses expression of antiapoptotic gene products, and enhances apoptosis. J. Biol. Chem. 279, 47148-47158 (Pubitemid 39518371)
52. Chen, C., Fuhrken, P. G., Huang, L. T., Apostolidis, P., Wang, M., Paredes, C. J., Miller, W. M., and Papoutsakis, E. T. (2007) A systems-biology analysis of isogenic megakaryocytic and granulocytic cultures identifies new molecular components of megakaryocytic apoptosis. BMC Genomics 8, 384
53. Castorina, A., Tiralongo, A., Giunta, S., Carnazza, M. L., Rasi, G., and D'Agata, V. (2008) PACAP and VIP prevent apoptosis in schwannoma cells. Brain Res. 1241, 29-35
54. Brenneman, D. E., Phillips, T. M., Festoff, B. W., and Gozes, I. (1997) Identity of neurotrophic molecules released from astroglia by vasoactive intestinal peptide. Ann. N.Y. Acad. Sci. 814, 167-173
55. Villalba, M., Bockaert, J., and Journot, L. (1997) Pituitary adenylate cyclase-activating polypeptide (PACAP-38) protects cerebellar granule neurons from apoptosis by activating the mitogen-activated protein kinase (MAP kinase) pathway. J. Neurosci. 17, 83-90 (Pubitemid 27008852)
56. Lindholm, D., Skoglösa, Y., and Takei, N. (1998) Developmental regulation of pituitary adenylate cyclase activating polypeptide (PACAP) and its receptor 1 in rat brain: function of PACAP as a neurotrophic factor. Ann. N.Y. Acad. Sci. 865, 189-196 (Pubitemid 29047827)
57. Vaudry, D., Basille, M., Anouar, Y., Fournier, A., Vaudry, H., and Gonzalez, B. J. (1998) The neurotrophic activity of PACAP on rat cerebellar granule cells is associated with activation of the protein kinase A pathway and c-fos gene expression. Ann. N.Y. Acad. Sci. 865, 92-99 (Pubitemid 29047816)
58. Onoue, S., Endo, K., Ohshima, K., Yajima, T., and Kashimoto, K. (2002) The neuropeptide PACAP attenuates beta-amyloid (1-42)-induced toxicity in PC12 cells. Peptides 23, 1471-1478 (Pubitemid 35223015)
59. Vaudry, D., Pamantung, T. F., Basille, M., Rousselle, C., Fournier, A., Vaudry, H., Beauvillain, J. C., and Gonzalez, B. J. (2002) PACAP protects cerebellar granule neurons against oxidative stress-induced apoptosis. Eur. J. Neurosci. 15, 1451-1460 (Pubitemid 35477975)
60. Seaborn, T., Masmoudi-Kouli, O., Fournier, A., Vaudry, H., and Vaudry, D. (2011) Protective effects of pituitary adenylate cyclase-activating polypeptide (PACAP) against apoptosis. Current Pharm. Des. 17, 204-214