Alpha-Helical Destabilization of the Bcl-2-BH4-Domain Peptide Abolishes Its Ability to Inhibit the IP3 Receptor

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Monaco, Giovanni ^a   Decrock, Elke ^b   Nuyts, Koen ^c   Wagner II, Larry E ^d   Luyten, Tomas ^a   Strelkov, Sergei V ^e   Missiaen, Ludwig ^a   De Borggraeve, Wim M ^c   Leybaert, Luc ^b   Yule, David I ^d   De Smedt, Humbert ^a   Parys, Jan B ^a   Bultynck, Geert ^a  

^a LABORATORY OF MOLECULAR AND CELLULAR SIGNALING   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

^c KULeuven   (Belgium)

^d UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

^e DEPARTMENT OF PHARMACEUTICAL AND PHARMACOLOGICAL SCIENCES   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; GLYCINE; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR; PROTEIN BCL 2; PROTEIN BCL 2 BH4; PROTEIN VARIANT; UNCLASSIFIED DRUG; VALINE;

ALPHA HELIX; AMINO ACID SUBSTITUTION; ANIMAL CELL; APOPTOSIS; ARTICLE; EMBRYO; MOUSE; NONHUMAN; PROTEIN CONFORMATION; PROTEIN DEPLETION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; WILD TYPE;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; APOPTOSIS; CALCIUM; CELL LINE, TUMOR; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; INOSITOL 1,4,5-TRISPHOSPHATE RECEPTORS; MICE; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; PERMEABILITY; PROTEIN STABILITY; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PROTO-ONCOGENE PROTEINS C-BCL-2;

EID: 84883417463     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0073386     Document Type: Article

References (55)

1. Grimm S, (2012) The ER-mitochondria interface: the social network of cell death. Biochim Biophys Acta 1823: 327-334. doi:10.1016/j.bbamcr.2011.11.018. PubMed: 22182703.
2. Rasola A, Bernardi P, (2011) Mitochondrial permeability transition in Ca2+-dependent apoptosis and necrosis. Cell Calcium 50: 222-233. doi:10.1016/j.ceca.2011.04.007. PubMed: 21601280.
3. Walter L, Hajnóczky G, (2005) Mitochondria and endoplasmic reticulum: the lethal interorganelle cross-talk. J Bioenerget Biomembr 37: 191-206. doi:10.1007/s10863-005-6600-x. PubMed: 16167176.
4. Rong Y, Distelhorst CW, (2008) Bcl-2 protein family members: versatile regulators of calcium signaling in cell survival and apoptosis. Annu Rev Physiol 70: 73-91. doi:10.1146/annurev.physiol.70.021507.105852. PubMed: 17680735.
5. Bender T, Martinou JC, (2013) Where killers meet--permeabilization of the outer mitochondrial membrane during apoptosis. Cold Spring Harbor Perspectives Biol 5: a011106. doi:10.1101/cshperspect.a011106. PubMed: 23284044.
6. Dremina ES, Sharov VS, Kumar K, Zaidi A, Michaelis EK, et al. (2004) Anti-apoptotic protein Bcl-2 interacts with and destabilizes the sarcoplasmic/endoplasmic reticulum Ca2+-ATPase (SERCA). Biochem J 383: 361-370. doi:10.1042/BJ20040187. PubMed: 15245329.
7. Dremina ES, Sharov VS, Schöneich C, (2012) Heat-shock proteins attenuate SERCA inactivation by the anti-apoptotic protein Bcl-2: possible implications for the ER Ca2+-mediated apoptosis. Biochem J 444: 127-139. doi:10.1042/BJ20111114. PubMed: 22360692.
8. Chami M, Prandini A, Campanella M, Pinton P, Szabadkai G, et al. (2004) Bcl-2 and Bax exert opposing effects on Ca2+ signaling, which do not depend on their putative pore-forming region. J Biol Chem 279: 54581-54589. doi:10.1074/jbc.M409663200. PubMed: 15485871.
9. Palmer AE, Jin C, Reed JC, Tsien RY, (2004) Bcl-2-mediated alterations in endoplasmic reticulum Ca2+ analyzed with an improved genetically encoded fluorescent sensor. Proc Natl Acad Sci U S A 101: 17404-17409. doi:10.1073/pnas.0408030101. PubMed: 15585581.
10. Oakes SA, Lin SS, Bassik MC, (2006) The control of endoplasmic reticulum-initiated apoptosis by the Bcl-2 family of proteins. Curr Mol Med 6: 99-109. doi:10.2174/156652406775574587. PubMed: 16472117.
11. Eckenrode EF, Yang J, Velmurugan GV, Foskett JK, White C, (2010) Apoptosis protection by Mcl-1 and Bcl-2 modulation of inositol 1,4,5-trisphosphate receptor-dependent Ca2+ signaling. J Biol Chem 285: 13678-13684. doi:10.1074/jbc.M109.096040. PubMed: 20189983.
12. Monaco G, Decrock E, Akl H, Ponsaerts R, Vervliet T, et al. (2012) Selective regulation of IP3-receptor-mediated Ca2+ signaling and apoptosis by the BH4 domain of Bcl-2 versus Bcl-Xl. Cell Death Differ 19: 295-309. doi:10.1038/cdd.2011.97. PubMed: 21818117.
13. Rong YP, Barr P, Yee VC, Distelhorst CW, (2009) Targeting Bcl-2 based on the interaction of its BH4 domain with the inositol 1,4,5-trisphosphate receptor. Biochim Biophys Acta 1793: 971-978. doi:10.1016/j.bbamcr.2008.10.015. PubMed: 19056433.
14. Rizzuto R, De Stefani D, Raffaello A, Mammucari C, (2012) Mitochondria as sensors and regulators of calcium signalling. Nat Rev Mol Cell Biol 13: 566-578. doi:10.1038/nrm3412. PubMed: 22850819.
15. Monaco G, Vervliet T, Akl H, Bultynck G, (2013) The selective BH4-domain biology of Bcl-2-family members: IP3Rs and beyond. Cell Mol Life Sci 70: 1171-1183. doi:10.1007/s00018-012-1118-y. PubMed: 22955373.
16. Akl H, Bultynck G, (2013) Altered Ca2+ signaling in cancer cells: proto-oncogenes and tumor suppressors targeting IP3 receptors. Biochim Biophys Acta 1835: 180-193. PubMed: 23232185.
17. Rong YP, Bultynck G, Aromolaran AS, Zhong F, Parys JB, et al. (2009) The BH4 domain of Bcl-2 inhibits ER calcium release and apoptosis by binding the regulatory and coupling domain of the IP3 receptor. Proc Natl Acad Sci U S A 106: 14397-14402. doi:10.1073/pnas.0907555106. PubMed: 19706527.
18. Hunter JJ, Bond BL, Parslow TG, (1996) Functional dissection of the human Bcl-2 protein: sequence requirements for inhibition of apoptosis. Mol Cell Biol 16: 877-883. PubMed: 8622689.
19. Huang DC, Adams JM, Cory S, (1998) The conserved N-terminal BH4 domain of Bcl-2 homologues is essential for inhibition of apoptosis and interaction with CED-4. EMBO J 17: 1029-1039. doi:10.1093/emboj/17.4.1029. PubMed: 9463381.
20. Reed JC, Zha H, Aime-Sempe C, Takayama S, Wang HG, (1996) Structure-function analysis of Bcl-2 family proteins. Regulators of programmed cell death. Adv Exp Med Biol 406: 99-112. doi:10.1007/978-1-4899-0274-0_10. PubMed: 8910675.
21. Petros AM, Medek A, Nettesheim DG, Kim DH, Yoon HS, et al. (2001) Solution structure of the antiapoptotic protein Bcl-2 Proceedings of the National Academy of Sciences of the United States of America 98: 3012-3017.
22. Lee LC, Hunter JJ, Mujeeb A, Turck C, Parslow TG, (1996) Evidence for alpha-helical conformation of an essential N-terminal region in the human Bcl-2 protein. J Biol Chem 271: 23284-23288. doi:10.1074/jbc.271.38.23284. PubMed: 8798527.
23. Lama D, Sankararamakrishnan R, (2010) Identification of core structural residues in the sequentially diverse and structurally homologous Bcl-2 family of proteins. Biochemistry 49: 2574-2584. doi:10.1021/bi100029k. PubMed: 20141168.
24. Kasri NN, Kocks SL, Verbert L, Hébert SS, Callewaert G, et al. (2006) Up-regulation of inositol 1,4,5-trisphosphate receptor type 1 is responsible for a decreased endoplasmic-reticulum Ca2+ content in presenilin double knockout cells. Cell Calcium 40: 41-51. doi:10.1016/j.ceca.2006.03.005. PubMed: 16675011.
25. De Vuyst E, De Bock M, Decrock E, Van Moorhem M, Naus C, et al. (2008) In situ bipolar electroporation for localized cell loading with reporter dyes and investigating gap junctional coupling. Biophys J 94: 469-479. doi:10.1529/biophysj.107.109470. PubMed: 17872956.
26. Bond SL, Bechberger JF, Khoo NK, Naus CC, (1994) Transfection of C6 glioma cells with connexin 32: the effects of expression of a nonendogenous gap junction protein. Cell Growth Differ 5: 179-186. PubMed: 8180131.
27. Wagner LE 2nd, Yule DI, (2012) Differential regulation of the InsP3 receptor type-1 and-2 single channel properties by InsP3, Ca2+ and ATP. J Physiol 590: 3245-3259. doi:10.1113/jphysiol.2012.228320. PubMed: 22547632.
28. Yin S, Ding F, Dokholyan NV, (2007) Eris: an automated estimator of protein stability. Nat Methods 4: 466-467. doi:10.1038/nmeth0607-466. PubMed: 17538626.
29. Roy A, Kucukural A, Zhang Y, (2010) I-TASSER: a unified platform for automated protein structure and function prediction. Nat Protoc 5: 725-738. doi:10.1038/nprot.2010.5. PubMed: 20360767.
30. Sreerama N, Woody RW, (1993) A self-consistent method for the analysis of protein secondary structure from circular dichroism. Anal Biochem 209: 32-44. doi:10.1006/abio.1993.1079. PubMed: 8465960.
31. Sreerama N, Woody RW, (2000) Estimation of protein secondary structure from circular dichroism spectra: comparison of CONTIN, SELCON, and CDSSTR methods with an expanded reference set. Anal Biochem 287: 252-260. doi:10.1006/abio.2000.4880. PubMed: 11112271.
32. Rong YP, Aromolaran AS, Bultynck G, Zhong F, Li X, et al. (2008) Targeting Bcl-2-IP3 receptor interaction to reverse Bcl-2's inhibition of apoptotic calcium signals. Mol Cell 31: 255-265. doi:10.1016/j.molcel.2008.06.014. PubMed: 18657507.
33. Decrock E, De Vuyst E, Vinken M, Van Moorhem M, Vranckx K, et al. (2009) Connexin 43 hemichannels contribute to the propagation of apoptotic cell death in a rat C6 glioma cell model. Cell Death Differ 16: 151-163. doi:10.1038/cdd.2008.138. PubMed: 18820645.34Decrock E, De Bock M, Wang N, Bol M, Gadicherla A, et al. (2013) Electroporation Loading Flash Photolysis Investigate Intra and Intercellular Ca 2+ signaling. Cold Spring Harbor Protocols. In press.
34. Decrock E, De Bock M, Wang N, Bol M, Gadicherla A, et al. (2013) Electroporation Loading Flash Photolysis Investigate Intra and Intercellular Ca 2+ signaling. Cold Spring Harbor Protocols. In press.
35. Betzenhauser MJ, Wagner LE 2nd, Park HS, Yule DI, (2009) ATP regulation of type-1 inositol 1,4,5-trisphosphate receptor activity does not require walker A-type ATP-binding motifs. J Biol Chem 284: 16156-16163. doi:10.1074/jbc.M109.006452. PubMed: 19386591.
36. Lyu PC, Wang PC, Liff MI, Kallenbach NR, (1991) Local effect of glycine substitution in a model helical peptide. J Am Chem Soc 113: 3568-3572. doi:10.1021/ja00009a052.
37. Pace CN, Scholtz JM, (1998) A helix propensity scale based on experimental studies of peptides and proteins. Biophys J 75: 422-427. doi:10.1016/S0006-3495(98)77529-0. PubMed: 9649402.
38. Corrêa DHA, Ramos CHI, (2009) The use of circular dichroism spectroscopy to study protein folding, form and function. Afr J Biochemistry Res 3: 164-173.
39. Greenfield NJ, (2006) Using circular dichroism spectra to estimate protein secondary structure. Nat Protoc 1: 2876-2890. PubMed: 17406547.
40. Yoshikawa F, Iwasaki H, Michikawa T, Furuichi T, Mikoshiba K, (1999) Trypsinized cerebellar inositol 1,4,5-trisphosphate receptor. Structural and functional coupling of cleaved ligand binding and channel domains. J Biol Chem 274: 316-327. doi:10.1074/jbc.274.1.316. PubMed: 9867846.
41. Stehno-Bittel L, Lückhoff A, Clapham DE, (1995) Calcium release from the nucleus by InsP3 receptor channels. Neuron 14: 163-167. doi:10.1016/0896-6273(95)90250-3. PubMed: 7530018.
42. Kruman I, Guo Q, Mattson MP, (1998) Calcium and reactive oxygen species mediate staurosporine-induced mitochondrial dysfunction and apoptosis in PC12 cells. J Neurosci Res 51: 293-308. doi:10.1002/(SICI)1097-4547(19980201)51:3. PubMed: 9486765.
43. Nutt LK, Chandra J, Pataer A, Fang B, Roth JA, et al. (2002) Bax-mediated Ca2+ mobilization promotes cytochrome c release during apoptosis. J Biol Chem 277: 20301-20308. doi:10.1074/jbc.M201604200. PubMed: 11909872.
44. Cantara S, Donnini S, Giachetti A, Thorpe PE, Ziche M, (2004) Exogenous BH4/Bcl-2 peptide reverts coronary endothelial cell apoptosis induced by oxidative stress. J Vasc Res 41: 202-207. doi:10.1159/000077408. PubMed: 15031604.
45. McDunn JE, Muenzer JT, Dunne B, Zhou A, Yuan K, et al. (2009) An anti-apoptotic peptide improves survival in lethal total body irradiation. Biochem Biophys Res Commun 382: 657-662. doi:10.1016/j.bbrc.2009.03.080. PubMed: 19303399.
46. Shimizu S, Konishi A, Kodama T, Tsujimoto Y, (2000) BH4 domain of antiapoptotic Bcl-2 family members closes voltage-dependent anion channel and inhibits apoptotic mitochondrial changes and cell death. Proc Natl Acad Sci U S A 97: 3100-3105. doi:10.1073/pnas.97.7.3100. PubMed: 10737788.
47. Jochim AL, Arora PS, (2009) Assessment of helical interfaces in protein-protein interactions. Mol Biosyst 5: 924-926. doi:10.1039/b903202a. PubMed: 19668855.
48. Guharoy M, Chakrabarti P, (2007) Secondary structure based analysis and classification of biological interfaces: identification of binding motifs in protein-protein interactions. Bioinformatics 23: 1909-1918. doi:10.1093/bioinformatics/btm274. PubMed: 17510165.
49. Khemtémourian L, Sani MA, Bathany K, Gröbner G, Dufourc EJ, (2006) Synthesis and secondary structure in membranes of the Bcl-2 anti-apoptotic domain BH4. J Pept Sci 12: 58-64. doi:10.1002/psc.686. PubMed: 15948141.
50. Sani MA, Castano S, Dufourc EJ, Gröbner G, (2008) Restriction of lipid motion in membranes triggered by β-sheet aggregation of the anti-apoptotic BH4 domain. FEBS J 275: 561-572. doi:10.1111/j.1742-4658.2007.06222.x. PubMed: 18199286.
51. Wang KR, Zhang BZ, Zhang W, Yan JX, Li J, et al. (2008) Antitumor effects, cell selectivity and structure-activity relationship of a novel antimicrobial peptide polybia-MPI. Peptides 29: 963-968. doi:10.1016/j.peptides.2008.01.015. PubMed: 18328599.
52. Sani MA, Loudet C, Gröbner G, Dufourc EJ, (2007) Pro-apoptotic Bax-alpha1 synthesis and evidence for beta-sheet to alpha-helix conformational change as triggered by negatively charged lipid membranes. J Pept Sci 13: 100-106. doi:10.1002/psc.803. PubMed: 17106904.
53. Monaco G, Vervliet T, Akl H, Bultynck G, (2013) The selective BH4-domain biology of Bcl-2-family members: IP3Rs and beyond. Cell Mol Life Sci 70: 1171-1183. doi:10.1007/s00018-012-1118-y. PubMed: 22955373.
54. Johanning GL, (2012) Stapled Peptides as Anti-Apoptotic Drugs. Chemotherapy 1: 1-3. doi:10.4236/mc.2012.11001.
55. Kawamoto SA, Coleska A, Ran X, Yi H, Yang CY, et al. (2012) Design of triazole-stapled BCL9 alpha-helical peptides to target the beta-catenin/B-cell CLL/lymphoma 9 (BCL9) protein-protein interaction. J Med Chem 55: 1137-1146. doi:10.1021/jm201125d. PubMed: 22196480.