Competition through Dimerization between Antiapoptotic and Proapoptotic HS-1-Associated Protein X-1 (Hax-1)

Journal of Biological Chemistry

Volumn 289, Issue 6, 2014, Pages 3468-3477

  Koontz, Jason ^a   Kontrogianni Konstantopoulos, Aikaterini ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOPTOSIS; BCL-2 FAMILY PROTEINS; CELL DEATH; OXIDATIVE STRESS; PROTEIN-PROTEIN INTERACTIONS;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; APOPTOSIS; CARRIER PROTEINS; CELL SURVIVAL; HEK293 CELLS; HUMANS; HYDROGEN PEROXIDE; MUSCLE PROTEINS; MYOCARDIAL INFARCTION; MYOCARDIUM; OXIDANTS; PROTEIN MULTIMERIZATION; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84893659149     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.536151     Document Type: Article

References (45)

1. Grzybowska, E. A., Sarnowska, E., Konopinski, R., Wilczynska, A., Sarnowski, T. J., and Siedlecki, J. A. (2006) Identification and expression analysis of alternative splice variants of the rat Hax-1 gene. Gene 371, 84-92
2. Lees, D. M., Hart, I. R., and Marshall, J. F. (2008) Existence of multiple isoforms of HS1-Associated protein X-1 in murine and human tissues. J. Mol. Biol. 379, 645-655
3. Suzuki, Y., Demoliere, C., Kitamura, D., Takeshita, H., Deuschle, U., and Watanabe, T. (1997) HAX-1, a novel intracellular protein, localized on mitochondria, directly associates with HS1, a substrate of Src family tyrosine kinases. J. Immunol. 158, 2736-2744
4. Fadeel, B., and Grzybowska, E. (2009) HAX-1. A multifunctional protein with emerging roles in human disease. Biochim. Biophys. Acta 1790, 1139-1148
5. Jeyaraju, D. V., Cisbani, G., De Brito, O. M., Koonin, E. V., and Pellegrini, L. (2009) Hax1 lacks BH modules and is peripherally associated to heavy membranes. Implications for Omi/HtrA2 and PARL activity in the regulation of mitochondrial stress and apoptosis. Cell Death. Differ. 16, 1622-1629
6. Sharp, T. V., Wang, H. W., Koumi, A., Hollyman, D., Endo, Y., Ye, H., Du, M. Q., and Boshoff, C. (2002) K15 protein of Kaposi's sarcoma-Associated herpesvirus is latently expressed and binds to HAX-1, a protein with antiapoptotic function. J. Virol. 76, 802-816
7. Yedavalli, V. S., Shih, H. M., Chiang, Y. P., Lu, C. Y., Chang, L. Y., Chen, M. Y., Chuang, C. Y., Dayton, A. I., Jeang, K. T., and Huang, L. M. (2005) Human immunodeficiency virus type 1 Vpr interacts with antiapoptotic mitochondrial protein HAX-1. J. Virol. 79, 13735-13746
8. Han, Y., Chen, Y. S., Liu, Z., Bodyak, N., Rigor, D., Bisping, E., Pu, W. T., and Kang, P. M. (2006) Overexpression of HAX-1 protects cardiac myocytes from apoptosis through caspase-9 inhibition. Circ. Res. 99, 415-423
9. Vafiadaki, E., Sanoudou, D., Arvanitis, D. A., Catino, D. H., Kranias, E. G., and Kontrogianni-Konstantopoulos, A. (2007) Phospholamban interacts with HAX-1, a mitochondrial protein with anti-Apoptotic function. J. Mol. Biol. 367, 65-79
10. Mirmohammadsadegh, A., Tartler, U., Michel, G., Baer, A., Walz, M., Wolf, R., Ruzicka, T., and Hengge, U. R. (2003) HAX-1, identified by differential display reverse transcription polymerase chain reaction, is overexpressed in lesional psoriasis. J. Invest Dermatol. 120, 1045-1051
11. Trebinska, A., Rembiszewska, A., Ciosek, K., Ptaszynski, K., Rowinski, S., Kupryjanczyk, J., Siedlecki, J. A., and Grzybowska, E. A. (2010) HAX-1 overexpression, splicing and cellular localization in tumors. BMC Cancer 10, 76
12. Gallagher, A. R., Cedzich, A., Gretz, N., Somlo, S., and Witzgall, R. (2000) The polycystic kidney disease protein PKD2 interacts with Hax-1, a protein associated with the actin cytoskeleton. Proc. Natl. Acad. Sci. U.S.A. 97, 4017-4022
13. Ortiz, D. F., Moseley, J., Calderon, G., Swift, A. L., Li, S., and Arias, I. M. (2004) Identification of HAX-1 as a protein that binds bile salt export protein and regulates its abundance in the apical membrane of Madin-Darby canine kidney cells. J. Biol. Chem. 279, 32761-32770
14. Vafiadaki, E., Arvanitis, D. A., Pagakis, S. N., Papalouka, V., Sanoudou, D., Kontrogianni-Konstantopoulos, A., and Kranias, E. G. (2009) The antiapoptotic protein HAX-1 interacts with SERCA2 and regulates its protein levels to promote cell survival. Mol. Biol. Cell 20, 306-318
15. Lam, A. K., Galione, A., Lai, F. A., and Zissimopoulos, S. (2013) Hax-1 identified as a two-pore channel (TPC)-binding protein. FEBS Lett. 587, 3782-3786
16. Vafiadaki, E., Papalouka, V., Arvanitis, D. A., Kranias, E. G., and Sanoudou, D. (2009) The role of SERCA2a/PLN complex, Ca2-homeostasis, and anti-Apoptotic proteins in determining cell fate. Pflugers Arch. 457, 687-700
17. Zhao, W., Waggoner, J. R., Zhang, Z. G., Lam, C. K., Han, P., Qian, J., Schroder, P. M., Mitton, B., Kontrogianni-Konstantopoulos, A., Robia, S. L., and Kranias, E. G. (2009) The anti-Apoptotic protein HAX-1 is a regulator of cardiac function. Proc. Natl. Acad. Sci. U.S.A. 106, 20776-20781
18. Chao, J. R., Parganas, E., Boyd, K., Hong, C. Y., Opferman, J. T., and Ihle, J. N. (2008) Hax1-mediated processing of HtrA2 by Parl allows survival of lymphocytes and neurons. Nature 452, 98-102
19. Yap, S. V., Koontz, J. M., and Kontrogianni-Konstantopoulos, A. (2011) HAX-1. A family of apoptotic regulators in health and disease. J. Cell. Physiol. 226, 2752-2761
20. O'Shea, K. M., Khairallah, R. J., Sparagna, G. C., Xu, W., Hecker, P. A., Robillard-Frayne, I., Des Rosiers, C., Kristian, T., Murphy, R. C., Fiskum, G., and Stanley, W. C. (2009) Dietary omega-3 fatty acids alter cardiac mitochondrial phospholipid composition and delay Ca2-induced permeability transition. J. Mol. Cell Cardiol. 47, 819-827
21. Morgan, E. E., Chandler, M. P., Young, M. E., McElfresh, T. A., Kung, T. A., Rennison, J. H., Tserng, K. Y., Hoit, B. D., and Stanley, W. C. (2006) Dissociation between gene and protein expression of metabolic enzymes in a rodent model of heart failure. Eur. J. Heart Fail. 8, 687-693
22. Kontrogianni-Konstantopoulos, A., Jones, E. M., Van Rossum, D. B., and Bloch, R. J. (2003) Obscurin is a ligand for small ankyrin 1 in skeletal muscle. Mol. Biol. Cell 14, 1138-1148
23. Bowman, A. L., Catino, D. H., Strong, J. C., Randall, W. R., Kontrogianni-Konstantopoulos, A., and Bloch, R. J. (2008) The Rho-guanine nucleotide exchange factor domain of obscurin regulates assembly of titin at the Z-disk through interactions with Ran binding protein 9. Mol. Biol. Cell 19, 3782-3792
24. Thomas, P., and Smart, T. G. (2005) HEK293 cell line. A vehicle for the expression of recombinant proteins. J. Pharmacol. Toxicol. Methods 51, 187-200
25. Lytton, J., Westlin, M., and Hanley, M. R. (1991) Thapsigargin inhibits the sarcoplasmic or endoplasmic reticulum Ca-ATPase family of calcium pumps. J. Biol. Chem. 266, 17067-17071
26. Reed, P. W., and Lardy, H. A. (1972) A23187. A divalent cation ionophore. J. Biol. Chem. 247, 6970-6977
27. Kulkarni, G. V., and McCulloch, C. A. (1994) Serum deprivation induces apoptotic cell death in a subset of Balb/c 3T3 fibroblasts. J. Cell Sci. 107, 1169-1179
28. Stridh, H., Kimland, M., Jones, D. P., Orrenius, S., and Hampton, M. B. (1998) Cytochrome c release and caspase activation in hydrogen peroxideand tributyltin-induced apoptosis. FEBS Lett. 429, 351-355
29. Simmen, T. (2011) Hax-1. A regulator of calcium signaling and apoptosis progression with multiple roles in human disease. Expert. Opin. Ther. Targets 15, 741-751
30. Youle, R. J., and Strasser, A. (2008) The BCL-2 protein family. Opposing activities that mediate cell death. Nat. Rev. Mol. Cell Biol. 9, 47-59
31. O'Neill, J. W., Manion, M. K., Maguire, B., and Hockenbery, D. M. (2006) BCL-XL dimerization by three-dimensional domain swapping. J. Mol. Biol. 356, 367-381
32. Gross, A., McDonnell, J. M., and Korsmeyer, S. J. (1999) BCL-2 family members and the mitochondria in apoptosis. Genes Dev. 13, 1899-1911
33. Cheng, E. H., Wei, M. C., Weiler, S., Flavell, R. A., Mak, T. W., Lindsten, T., and Korsmeyer, S. J. (2001) BCL-2, BCL-X(L) sequester BH3 domain-only molecules preventing BAX-And BAK-mediated mitochondrial apoptosis. Mol. Cell 8, 705-711
34. Aouacheria, A., Rech de Laval, V., Combet, C., and Hardwick, J. M. (2013) Evolution of Bcl-2 homology motifs. Homology versus homoplasy. Trends Cell Biol. 23, 103-111
35. Lam, C. K., Zhao, W., Cai, W., Vafiadaki, E., Florea, S. M., Ren, X., Liu, Y., Robbins, N., Zhang, Z., Zhou, X., Jiang, M., Rubinstein, J., Jones, W. K., and Kranias, E. G. (2013) Novel role of HAX-1 in ischemic injury protection involvement of heat shock protein 90. Circ. Res. 112, 79-89
36. Yap, S. V., Vafiadaki, E., Strong, J., and Kontrogianni-Konstantopoulos, A. (2010) HAX-1. A multifaceted antiapoptotic protein localizing in the mitochondria and the sarcoplasmic reticulum of striated muscle cells. J. Mol. Cell Cardiol. 48, 1266-1279
37. Kim, R. (2005) Unknotting the roles of Bcl-2 and Bcl-xL in cell death. Biochem. Biophys. Res. Commun. 333, 336-343
38. Tao, W., Kurschner, C., and Morgan, J. I. (1998) Bcl-xS and Bad potentiate the death suppressing activities of Bcl-xL, Bcl-2, and A1 in yeast. J. Biol. Chem. 273, 23704-23708
39. Willimott, S., Merriam, T., and Wagner, S. D. (2011) Apoptosis induces Bcl-XS and cleaved Bcl-XL in chronic lymphocytic leukaemia. Biochem. Biophys. Res. Commun. 405, 480-485
40. Farrow, S. N., and Brown, R. (1996) New members of the Bcl-2 family and their protein partners. Curr. Opin. Genet. Dev. 6, 45-49
41. Michels, J., Kepp, O., Senovilla, L., Lissa, D., Castedo, M., Kroemer, G., and Galluzzi, L. (2013) Functions of BCL-X L at the interface between cell death and metabolism. Int. J. Cell Biol.
42. Lindenboim, L., Yuan, J., and Stein, R. (2000) Bcl-xS and Bax induce different apoptotic pathways in PC12 cells. Oncogene 19, 1783-1793
43. Esposti, M. D., Hatzinisiriou, I., McLennan, H., and Ralph, S. (1999) Bcl-2 and mitochondrial oxygen radicals. New approaches with reactive oxygen species-sensitive probes. J. Biol. Chem. 274, 29831-29837
44. Ouyang, Y. B., Carriedo, S. G., and Giffard, R. G. (2002) Effect of Bcl-x(L) overexpression on reactive oxygen species, intracellular calcium, and mitochondrial membrane potential following injury in astrocytes. Free Radic. Biol. Med. 33, 544-551
45. Yoshioka, H., Katsu, M., Sakata, H., Okami, N., Wakai, T., Kinouchi, H., and Chan, P. H. (2013) The role of PARL and HtrA2 in striatal neuronal injury after transient global cerebral ischemia. J. Cereb. Blood Flow Metab. 33, 1658-1665