Serine protease activity of calnuc regulation by Zn2+ and G proteins

Journal of Biological Chemistry

Volumn 288, Issue 3, 2013, Pages 1762-1773

  Kanuru, Madhavi ^a   Raman, Rajeev ^b   Aradhyam, Gopala Krishna ^a  

^a INDIAN INSTITUTE OF TECHNOLOGY MADRAS   (India)

^b CENTRE FOR CELLULAR AND MOLECULAR BIOLOGY   (India)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE; BINDING PROTEINS; C-TERMINAL DOMAINS; C-TERMINAL REGIONS; CATALYTIC TRIAD; ENZYMATIC ACTIVITIES; ENZYME ACTIVE SITES; FREEFORMS; G PROTEIN; HIGH AFFINITY; MULTI DOMAINS; MULTIPLE FUNCTION; PROTEOLYTIC FUNCTIONS; SERINE PROTEASE; STRUCTURAL DOMAINS;

AMINO ACIDS; CALCIUM; ENZYME ACTIVITY;

PROTEINS;

ASPARTIC ACID; CALCIUM BINDING PROTEIN; CALCIUM ION; CALNUC PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; HISTIDINE; SERINE; SERINE PROTEINASE; UNCLASSIFIED DRUG; ZINC ION;

ALLOSTERISM; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; BINDING SITE; CARBOXY TERMINAL SEQUENCE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME CONFORMATION; PRIORITY JOURNAL; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION;

ALLOSTERIC REGULATION; ALLOSTERIC SITE; AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CALCIUM; CALCIUM-BINDING PROTEINS; CATALYTIC DOMAIN; DNA-BINDING PROTEINS; ESCHERICHIA COLI; GENE EXPRESSION; GTP-BINDING PROTEIN ALPHA SUBUNITS; HUMANS; KINETICS; MOLECULAR SEQUENCE DATA; NERVE TISSUE PROTEINS; PROTEIN BINDING; PROTEIN CONFORMATION; RECOMBINANT PROTEINS; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; SERINE ENDOPEPTIDASES; THERMODYNAMICS; ZINC;

EID: 84872691420     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.382846     Document Type: Article

References (43)

1. Kawasaki, H., Nakayama, S., and Kretsinger, R. H. (1998) Classification and evolution of EF-hand proteins. Biometals 11, 277-295 (Pubitemid 29121537)
2. Schaub, M. C., and Heizmann, C. W. (2008) Calcium, troponin, calmodulin, S100 proteins. From myocardial basics to new therapeutic strategies. Biochem. Biophys. Res. Commun. 369, 247-264 (Pubitemid 351381712)
3. Miura, K., Kurosawa, Y., and Kanai, Y. (1994) Calcium binding activity of nucleobindin mediated by an EF hand moiety. Biochem. Biophys. Res. Commun. 199, 1388-1393 (Pubitemid 24174812)
4. Miura, K., Titani, K., Kurosawa, Y., and Kanai, Y. (1992) Molecular cloning of nucleobindin, a novel DNA-binding protein that contains both a signal peptide and a leucine zipper structure. Biochem. Biophys. Res. Commun. 187, 375-380
5. Karabinos, A., Bhattacharya, D., Morys-Wortmann, C., Kroll, K., Hirschfeld, G., Kratzin, H. D., Barnikol-Watanabe, S., and Hilschmann, N. (1996) The divergent domains of the NEFA and nucleobindin proteins are derived from an EF-hand ancestor. Mol. Biol. Evol. 13, 990-998 (Pubitemid 26284915)
6. Karabinos, A., Bhattacharya, D., Kratzin, H. D., and Hilschmann, N. (1998) Origin of the NEFA and Nuc signal sequences. J. Mol. Evol. 46, 327-333 (Pubitemid 28090720)
7. Ballif, B. A., Mincek, N. V., Barratt, J. T., Wilson, M. L., and Simmons, D. L. (1996) Interaction of cyclooxygenases with an apoptosis-and autoimmunity-associated protein. Proc. Natl. Acad. Sci. USA 93, 5544-5549
8. Leclerc, P., Biarc, J., St-Onge, M., Gilbert, C., Dussault, A. A., Laflamme, C., and Pouliot, M. (2008) Nucleobindin co-localizes and associates with cyclooxygenase, COX-2, in human neutrophils. PLoS One. 3, e2229
9. Mochizuki, N., Hibi, M., Kanai, Y., and Insel, P. A. (1995) Interaction of the protein nucleobindin with G alpha i2, as revealed by the yeast two-hybrid system. FEBS Lett. 373, 155-158
10. Lin, P., Li, F., Zhang, Y. W., Huang, H., Tong, G., Farquhar, M. G., and Xu, H. (2007) Calnuc binds to Alzheimer's α-amyloid precursor protein and affects its biogenesis. J. Neurochem. 100, 1505-1514 (Pubitemid 46376215)
11. Lin, P., Yao, Y., Hofmeister, R., Tsien, R. Y., and Farquhar, M. G. (1999) Overexpression of calnuc (Nucleobindin) increases agonist and thapsigargin releaseable calcium storage in the Golgi. J. Cell Biol. 145, 279-289 (Pubitemid 29198301)
12. Kanai, Y., and Tanuma, S. (1992) Purification of a novel B cell growth and differentiation factor associated with lupus syndrome. Immunol. Lett. 32, 43-48
13. Kanai, Y., Miura, K., Uehara, T., Amagai, M., Takeda, O., Tanuma, S., and Kurosawa, Y. (1993) Natural occurrence of Nuc in the sera of autoimmune-prone MRL/lpr mice. Biochem. Biophys. Res. Commun. 196, 729-736 (Pubitemid 23337668)
14. Tsukumo, Y., Tomida, A., Kitahara, O., Nakamura, Y., Asada, S., Mori, K., and Tsuruo, T. (2007) Nucleobindin 1 controls the unfolded protein response by inhibiting ATF6 activation. J. Biol. Chem. 282, 29264-29272 (Pubitemid 350043383)
15. Valencia, C. A., Cotten, S. W., Duan, J., and Liu, R. (2008) Modulation of nucleobindin-1 and nucleobindin-2 by caspases. FEBS Lett. 582, 286-290
16. + binding protein Calnuc is a potential marker in colon cancer detection. Int. J. Oncol. 30, 1137-1144
17. Weiss, T. S., Chamberlain, C. E., Takeda, T., Lin, P., Hahn, K. M., and Farquhar, M. G. (2001) Gαi3 binding to calnuc on Golgi membranes in living cells monitored by fluorescence resonance energy transfer of green fluorescent protein fusion proteins. Proc. Natl. Acad. Sci. U. S. A. 98, 14961-14966 (Pubitemid 34013952)
18. Lin, P., Fischer, T., Lavoie, C., Huang, H., and Farquhar, M. G. (2009) Calnuc plays a role in dynamic distribution ofGαi but notGα subunits and modulates ACTH secretion in AtT-20 neuroendocrine secretory cells. Mol. Neurodegener. 4, 15
19. Kapoor, N., Gupta, R., Menon, S. T., Folta-Stogniew, E., Raleigh, D. P., and Sakmar, T. P. (2010) Nucleobindin 1 is a calcium-regulated guanine nucleotide dissociation inhibitor of Gαi1. J. Biol. Chem. 285, 31647-31660
20. Garcia-Marcos, M., Kietrsunthorn, P. S., Wang, H., Ghosh, P., and Farquhar, M. G. (2011) G protein binding sites on Calnuc (nucleobindin 1) and NUCB2 (nucleobindin 2) define a new class of Gαi-regulatory motifs. J. Biol. Chem. 286, 28138-28149
21. + versus Mg2α-calnuc adopts additional and unusual Ca2+-binding sites upon interaction with G-protein. FEBS J. 276, 2529-2546
22. Lowry, O. H., Rosenbrough, N. J., Farr, A. L., and Randall, R. J. (1951) Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193, 265-275
23. Fahmy, K., and Sakmar, T. P. (1993) Regulation of the rhodopsin-transducin interaction by a highly conserved carboxylic acid group. Biochemistry 32, 7229-7236 (Pubitemid 23223127)
24. Scatchard, G. (1949) The attractions of proteins for small molecules and ions. Ann. N.Y. Acad. Sci. 51, 660-672
25. Twining, S. S. (1984) Fluorescein isothiocyanate-labeled casein assay for proteolytic enzymes. Anal. Biochem. 143, 30-34 (Pubitemid 15157534)
26. McDonald, J. K., Ellis, S., and Reilly, T. J. (1966) Properties of dipeptidyl arylamidase I of the pituitary. J. Biol. Chem. 241, 1494-1501
27. Sarath, G., Dela Motte, R. S., and Wagner, W. (1989) Protease Assay: Methods in Proteolytic Enzymes. A Practical Approach, pp. 22-55, Oxford IRI Press, Oxford, UK
28. Tunlid, A., Rosén, S., Ek, B., and Rask, L. (1994) Purification and characterization of an extracellular serine protease from the nematode-trapping fungus. Arthrobotrys oligospora. Microbiology 140, 1687-1695 (Pubitemid 24231157)
29. Bergmeyer, H. U., Gawehn, K., and Grassl, M. (1974) Methods of Enzymatic Analysis, pp. 436-437, Academic Press Inc., New York
30. Taylor, E. L., Meriwether, B. P., and Park, J. H. (1963) The hydrolysis of p-nitrophenyl acetate catalyzed by 3-phosphoglyceraldehyde dehydrogenase crystallized from yeast. J. Biol. Chem. 238, 734-740
31. Aradhyam, G. K., Balivada, L. M., Kanuru, M., Vadivel, P., and Vidhya, B. S. (2010) Calnuc. Emerging roles in calcium signaling and human diseases. IUBMB Life 62, 436-446
32. Hooper, N. M. (1994) Families of zinc metalloproteases. FEBS Lett. 354, 1-6 (Pubitemid 24331694)
33. Carter, P., and Wells, J. A. (1988) Dissecting the catalytic triad of a serine protease. Nature 332, 564-568
34. Maret, W., and Li, Y. (2009) Coordination dynamics of zinc in proteins. Chem. Rev. 109, 4682-4707
35. Geiger, S. R., Böttcher, T., Sieber, S. A., and Cramer P. (2011) A conformational switch underlies ClpP protease function. Angew. Chem. Int. Ed. Engl. 50, 5749-5752
36. Ostermeier, M. (2009) Designing switchable enzymes. Curr. Opin. Struct. Biol. 19, 442-448
37. Guntas, G., Mansell, T. J., Kim, J. R., and Ostermeier, M. (2005) Directed evolution of protein switches and their application to the creation of ligand-binding proteins. Proc. Natl. Acad. Sci. U. S. A. 102, 11224-11229 (Pubitemid 41153802)
38. Abian, O., Neira, J. L., and Velazquez-Campoy, A. (2009) Thermodynamics of zinc binding to hepatitis C virus NS3 protease. A folding by binding event. Proteins 77, 624-636
39. Liang, J., Kim, J. R., Boock, J. T., Mansell, T. J., and Ostermeier M. (2007) Ligand binding and allostery can emerge simultaneously. Protein Sci. 16, 929-937 (Pubitemid 46683197)
40. Bauer, M. C., Nilsson, H., Thulin, E., Frohm, B., Malm, J., and Linse, S. (2008) Zn2α binding to human calbindin D28k and the role of histidine residues. Protein Sci. 17, 760-767 (Pubitemid 351480869)
41. Cuajungco, M. P., Fagét, K. Y., Huang, X., Tanzi, R. E., and Bush, A. I. (2000) Metal chelation as a potential therapy for Alzheimer's disease. Ann. N.Y. Acad. Sci. 920, 292-304 (Pubitemid 32056584)
42. Cuajungco, M. P., and Lees, G. J. (1997) Zinc metabolism in the brain. Relevance to human neurodegenerative disorders. Neurobiol. Dis. 4, 137-169 (Pubitemid 27465507)
43. Bleackley, M. R., and Macgillivray, R. T. (2011) Transition metal homeostasis. From yeast to human disease. Biometals 24, 785-809