CharaCterization of a novel subtilisin-like protease myroicolsin from Deep sea bacterium Myroides profundi D25 and molecular insight into its collagenolytic mechanism

Journal of Biological Chemistry

Volumn 289, Issue 9, 2014, Pages 6041-6053

  Ran, Li Yuan ^a,b   Su, Hai Nan ^a,b   Zhou, Ming Yang ^a,b   Wang, Lei ^a,b   Chen, Xiu Lan ^a,b   Xie, Bin Bin ^a,b   Song, Xiao Yan ^a,b   Shi, Mei ^a,b   Qin, Qi Long ^a,b   Pang, Xiuhua ^a,b   Zhou, Bai Cheng ^b   Zhang, Yu Zhong ^a,b   Zhang, Xi Ying ^a,b  

^a SHANDONG UNIVERSITY   (China)

^b Marine Biotechnology Research Center   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMICAL ANALYSIS; BROAD SPECIFICITIES; COLLAGEN BINDING DOMAIN; COLLAGEN DEGRADATIONS; DEGRADATION MECHANISM; EXTRACELLULAR MATRICES; MARINE NITROGEN CYCLE; STRUCTURAL CHARACTERIZATION;

AMINO ACIDS; ATOMIC FORCE MICROSCOPY; BACTERIA; BIODEGRADATION; DEGRADATION; SCANNING ELECTRON MICROSCOPY;

COLLAGEN;

ARGININE; BACTERIAL PROTEIN; MYROICOLSIN; PROLINE; PROTEIN PRECURSOR; PROTEOGLYCAN; TELOPEPTIDE; UNCLASSIFIED DRUG;

ARTICLE; ATOMIC FORCE MICROSCOPY; CARBOXY TERMINAL SEQUENCE; COLLAGEN DEGRADATION; CONTROLLED STUDY; ENZYME SPECIFICITY; MARINE BACTERIUM; MOLECULAR CLONING; MYROIDES PROFUNDI; NITROGEN CYCLING; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN HYDROLYSIS; PROTEIN PURIFICATION; PROTEIN SECRETION; RESIDUE ANALYSIS; SCANNING ELECTRON MICROSCOPY; SEQUENCE ANALYSIS; STRUCTURE ANALYSIS;

BACTERIA; BIODEGRADATION; COLLAGEN; COLLAGENOLYTIC MECHANISM; DEEP SEA SEDIMENT; ENZYME MECHANISMS; NITROGEN CYCLING; SERINE PROTEASE; STRUCTURAL CHARACTERISTICS; SUBTILISIN-LIKE PROTEASE;

BACTERIAL PROTEINS; BASE SEQUENCE; COLLAGEN; FLAVOBACTERIACEAE; MOLECULAR SEQUENCE DATA; SEAWATER; SUBTILISIN; WATER MICROBIOLOGY;

EID: 84896807356     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.513861     Document Type: Article

References (56)

1. Aluwihare, L. I., Repeta, D. J., Pantoja, S., and Johnson, C. G. (2005) Two chemically distinct pools of organic nitrogen accumulate in the ocean. Science 308, 1007-1010 (Pubitemid 40664408)
2. Brunnegård, J., Grandel, S., Ståhl, H., Tengberg, A., and Hall, P. O. (2004) Nitrogen cycling in deep-sea sediments of the Porcupine Abyssal Plain, NE Atlantic. Prog. Oceanogr. 63, 159-181 (Pubitemid 40172026)
3. Sarkar, S., Pramanik, A., Mitra, A., and Mukherjee, J. (2010) Bioprocessing data for the production of marine enzymes. Mar. Drugs 8, 1323-1372
4. Exposito, J. Y., Valcourt, U., Cluzel, C., and Lethias, C. (2010) The fibrillar collagen family. Int. J. Mol. Sci. 11, 407-426
5. Prockop, D. J., and Kivirikko, K. I. (1995) Collagens. Molecular biology, diseases, and potentials for therapy. Annu. Rev. Biochem. 64, 403-434
6. Kadler, K. E., Baldock, C., Bella, J., and Boot-Handford, R. P. (2007) Collagens at a glance. J. Cell Sci. 120, 1955-1958 (Pubitemid 47009991)
7. Kadler, K. E., Holmes, D. F., Trotter, J. A., and Chapman, J. A. (1996) Collagen fibril formation. Biochem. J. 316, 1-11 (Pubitemid 26158194)
8. Brodsky, B., and Persikov, A. V. (2005) Molecular structure of the collagen triple helix. Adv. Protein Chem. 70, 301-339 (Pubitemid 40544786)
9. Orgel, J. P., Irving, T. C., Miller, A., and Wess, T. J. (2006) Microfibrillar structure of type I collagen in situ. Proc. Natl. Acad. Sci. U.S.A. 103, 9001-9005 (Pubitemid 43902523)
10. Scott, J. E., Orford, C. R., and Hughes, E. W. (1981) Proteoglycan-collagen arrangements in developing rat tail tendon. An electron microscopical and biochemical investigation. Biochem. J. 195, 573-581 (Pubitemid 11043887)
11. Rawlings, N. D., Barrett, A. J., and Bateman, A. (2010) MEROPS. The peptidase database. Nucleic Acids Res. 38, D227-D233
12. Kafienah, W., Brömme, D., Buttle, D. J., Croucher, L. J., and Hollander, A. P. (1998) Human cathepsin K cleaves native type I and II collagens at the N-terminal end of the triple helix. Biochem. J. 331, 727-732 (Pubitemid 28211893)
13. Eisen, A. Z., Henderson, K. O., Jeffrey, J. J., and Bradshaw, R. A. (1973) A collagenolytic protease from the hepatopancreas of the fiddler crab, Uca pugilator. Purification and properties. Biochemistry 12, 1814-1822
14. O'Farrell, T. J., Guo, R., Hasegawa, H., and Pourmotabbed, T. (2006) Matrix metalloproteinase-1 takes advantage of the induced fit mechanism to cleave the triple-helical type I collagen molecule. Biochemistry 45, 15411-15418 (Pubitemid 46032465)
15. Chung, L., Dinakarpandian, D., Yoshida, N., Lauer-Fields, J. L., Fields, G. B., Visse, R., and Nagase, H. (2004) Collagenase unwinds triple-helical collagen prior to peptide bond hydrolysis. EMBO J. 23, 3020-3030 (Pubitemid 39093596)
16. Tsu, C. A., Perona, J. J., Fletterick, R. J., and Craik, C. S. (1997) Structural basis for the broad substrate specificity of fiddler crab collagenolytic serine protease 1. Biochemistry 36, 5393-5401 (Pubitemid 27200035)
17. Visse, R., and Nagase, H. (2003) Matrix metalloproteinases and tissue inhibitors of metalloproteinases. Structure, function, and biochemistry. Circ. Res. 92, 827-839 (Pubitemid 36542523)
18. Perona, J. J., Tsu, C. A., Craik, C. S., and Fletterick, R. J. (1997) Crystal structure of an ecotin-collagenase complex suggests a model for recognition and cleavage of the collagen triple helix. Biochemistry 36, 5381-5392 (Pubitemid 27200034)
19. Huber, R., and Bode, W. (1978) Structural basis of the activation and action of trypsin. Acc. Chem. Res. 11, 114-122
20. Robinson, M. W., Corvo, I., Jones, P. M., George, A. M., Padula, M. P., To, J., Cancela, M., Rinaldi, G., Tort, J. F., Roche, L., and Dalton, J. P. (2011) Collagenolytic activities of the major secreted cathepsin L peptidases involved in the virulence of the helminth pathogen, Fasciola hepatica. PLoS Negl. Trop. Dis. 5, e1012
21. Takeuchi, H., Shibano, Y., Morihara, K., Fukushima, J., Inami, S., Keil, B., Gilles, A. M., Kawamoto, S., and Okuda, K. (1992) Structural gene and complete amino acid sequence of Vibrio alginolyticus collagenase. Biochem. J. 281, 703-708
22. Eckhard, U., Schönauer, E., Nüss, D., and Brandstetter, H. (2011) Structure of collagenase G reveals a chew-and-digest mechanism of bacterial collagenolysis. Nat. Struct. Mol. Biol. 18, 1109-1114
23. Yoshida, E., and Noda, H. (1965) Isolation and characterization of collagenases I and II from Clostridium histolyticum. Biochim. Biophys. Acta 105, 562-574
24. Gupta, R., Beg, Q. K., and Lorenz, P. (2002) Bacterial alkaline proteases. Molecular approaches and industrial applications. Appl. Microbiol. Biotechnol. 59, 15-32 (Pubitemid 34809671)
25. Okamoto, M., Yonejima, Y., Tsujimoto, Y., Suzuki, Y., and Watanabe, K. (2001) A thermostable collagenolytic protease with a very large molecular mass produced by thermophilic Bacillus sp. strain MO-1. Appl. Microbiol. Biotechnol. 57, 103-108 (Pubitemid 32938358)
26. Itoi, Y., Horinaka, M., Tsujimoto, Y., Matsui, H., and Watanabe, K. (2006) Characteristic features in the structure and collagen-binding ability of a thermophilic collagenolytic protease from the thermophile Geobacillus collagenovorans MO-1. J. Bacteriol. 188, 6572-6579 (Pubitemid 44412068)
27. Kim, H. K., Ha, Y. R., Yu, H. S., Kong, H. H., and Chung, D. I. (2003) Purification and characterization of a 33 kDa serine protease from Acanthamoeba lugdunensis KA/E2 isolated from a Korean keratitis patient. Korean J. Parasitol. 41, 189-196
28. Windhorst, S., Frank, E., Georgieva, D. N., Genov, N., Buck, F., Borowski, P., and Weber, W. (2002) The major extracellular protease of the nosocomial pathogen Stenotrophomonas maltophilia. Characterization of the protein and molecular clonning of the gene. J. Biol. Chem. 277, 11042-11049 (Pubitemid 34952862)
29. Kim, W. T., Kong, H. H., Ha, Y. R., Hong, Y. C., Jeong, H. J., Yu, H. S., and Chung, D. I. (2006) Comparison of specific activity and cytopathic effects of purified 33 kDa serine proteinase from Acanthamoeba strains with different degree of virulence. Korean J. Parasitol. 44, 321-330
30. Zhao, G. Y., Chen, X. L., Zhao, H. L., Xie, B. B., Zhou, B. C., and Zhang, Y. Z. (2008) Hydrolysis of insoluble collagen by deseasin MCP-01 from deep-sea Pseudoalteromonas sp. SM9913. Collagenolytic characters, collagen-binding ability of C-terminal polycystic kidney disease domain, and implication for its novel role in deep-sea sedimentary particulate organic nitrogen degradation. J. Biol. Chem. 283, 36100-36107
31. T. Appl. Microbiol. Biotechnol. 86, 589-598
32. Zhang, X. Y., Zhang, Y. J., Chen, X. L., Qin, Q. L., Zhao, D. L., Li, T. G., Dang, H. Y., and Zhang, Y. Z. (2008) Myroides profundi sp. nov., isolated from deep-sea sediment of the southern Okinawa Trough. FEMS Microbiol. Lett. 287, 108-112
33. Chen, X. L., Xie, B. B., Bian, F., Zhao, G. Y., Zhao, H. L., He, H. L., Zhou, B. C., and Zhang, Y. Z. (2009) Ecological function of myroilysin, a novel bacterial M12 metalloprotease with elastinolytic activity and a synergistic role in collagen hydrolysis, in biodegradation of deep-sea high-molecular-weight organic nitrogen. Appl. Environ. Microbiol. 75, 1838-1844
34. Sankar, S., Sekar, S., Mohan, R., Rani, S., Sundaraseelan, J., and Sastry, T. P. (2008) Preparation and partial characterization of collagen sheet from fish (Lates calcarifer) scales. Int. J. Biol. Macromol. 42, 6-9 (Pubitemid 350199686)
35. Worthington Biochemical Co. (1993) Worthington Enzyme Manual. Collagenase. Worthington Biochemical Co., Freehold, NJ
36. Abraham, L. D., and Breuil, C. (1996) Isolation and characterization of a subtilisin-like serine proteinase secreted by the sap-staining fungus Ophiostoma piceae. Enzyme Microb. Technol. 18, 133-140 (Pubitemid 26058696)
37. He, H. L., Chen, X. L., Li, J. W., Zhang, Y. Z., and Gao, P. J. (2004) Taste improvement of refrigerated meat treated with cold-adapted protease. Food Chem. 84, 307-311
38. Chen, X. L., Xie, B. B., Lu, J. T., He, H. L., and Zhang, Y. (2007) A novel type of subtilase from the psychrotolerant bacterium Pseudoalteromonas sp. SM9913. Catalytic and structural properties of deseasin MCP-01. Microbiology 153, 2116-2125
39. Maciver, B., McHale, R. H., Saul, D. J., and Bergquist, P. L. (1994) Cloning and sequencing of a serine proteinase gene from a thermophilic Bacillus species and its expression in Escherichia coli. Appl. Environ. Microbiol. 60, 3981-3988 (Pubitemid 24335849)
40. Liu, Y. G., and Whittier, R. F. (1995) Thermal asymmetric interlaced PCR. Automatable amplification and sequencing of insert end fragments from P1 and YAC clones for chromosome walking. Genomics 25, 674-681
41. Farndale, R. W., Buttle, D. J., and Barrett, A. J. (1986) Improved quantitation and discrimination of sulphated glycosaminoglycans by use of dimethylmethylene blue. Biochim. Biophys. Acta 883, 173-177 (Pubitemid 16027978)
42. Wang, Y. K., Zhao, G. Y., Li, Y., Chen, X. L., Xie, B. B., Su, H. N., Lv, Y. H., He, H. L., Liu, H., Hu, J., Zhou, B. C., and Zhang, Y. Z. (2010) Mechanistic insight into the function of the C-terminal PKD domain of the collagenolytic serine protease deseasin MCP-01 from deep sea Pseudoalteromonas sp. SM9913. Binding of the PKD domain to collagen results in collagen swelling but does not unwind the collagen triple helix. J. Biol. Chem. 285, 14285-14291
43. Nonaka, T., Fujihashi, M., Kita, A., Saeki, K., Ito, S., Horikoshi, K., and Miki, K. (2004) The crystal structure of an oxidatively stable subtilisin-like alkaline serine protease, KP-43, with a C-terminal β-barrel domain. J. Biol. Chem. 279, 47344-47351 (Pubitemid 39518391)
44. Eder, J., Rheinnecker, M., and Fersht, A. R. (1993) Folding of subtilisin BPN′. Role of the pro-sequence. J. Mol. Biol. 233, 293-304 (Pubitemid 23297598)
45. Orgel, J. P., Eid, A., Antipova, O., Bella, J., and Scott, J. E. (2009) Decorin core protein (decoron) shape complements collagen fibril surface structure and mediates its binding. PLoS One 4, e7028
46. Chen, Y. J., and Inouye, M. (2008) The intramolecular chaperone-mediated protein folding. Curr. Opin. Struct. Biol. 18, 765-770
47. Tanaka, S. I., Takeuchi, Y., Matsumura, H., Koga, Y., Takano, K., and Kanaya, S. (2008) Crystal structure of Tk-subtilisin folded without propeptide. Requirement of propeptide for acceleration of folding. FEBS Lett. 582, 3875-3878
48. Foophow, T., Tanaka, S., Angkawidjaja, C., Koga, Y., Takano, K., and Kanaya, S. (2010) Crystal structure of a subtilisin homologue, Tk-SP, from Thermococcus kodakaraensis. Requirement of a C-terminal β-Jelly Roll domain for hyperstability. J. Mol. Biol. 400, 865-877
49. Manka, S. W., Carafoli, F., Visse, R., Bihan, D., Raynal, N., Farndale, R. W., Murphy, G., Enghild, J. J., Hohenester, E., and Nagase, H. (2012) Structural insights into triple-helical collagen cleavage by matrix metalloproteinase 1. Proc. Natl. Acad. Sci. U.S.A. 109, 12461-12466
50. Knäuper, V., Cowell, S., Smith, B., López-Otin, C., O'Shea, M., Morris, H., Zardi, L., and Murphy, G. (1997) The role of the C-terminal domain of human collagenase-3 (MMP-13) in the activation of procollagenase-3, substrate specificity, and tissue inhibitor of metalloproteinase interaction. J. Biol. Chem. 272, 7608-7616 (Pubitemid 27137308)
51. Taddese, S., Jung, M. C., Ihling, C., Heinz, A., Neubert, R. H., and Schmelzer, C. E. (2010) MMP-12 catalytic domain recognizes and cleaves at multiple sites in human skin collagen type I and type III. Biochim. Biophys. Acta 1804, 731-739
52. Walton, R. S., Brand, D. D., and Czernuszka, J. T. (2010) Influence of telopeptides, fibrils and crosslinking on physicochemical properties of type I collagen films. J. Mater. Sci. Mater. Med. 21, 451-461
53. Panwar, P., Du, X., Sharma, V., Lamour, G., Castro, M., Li, H., and Brömme, D. (2013) Effects of cysteine proteases on the structural and mechanical properties of collagen fibers. J. Biol. Chem. 288, 5940-5950
54. Cowan, P. M., McGavin, S., and North, A. C. (1955) The polypeptide chain configuration of collagen. Nature 176, 1062-1064
55. Perona, J. J., and Craik, C. S. (1995) Structural basis of substrate specificity in the serine proteases. Protein Sci. 4, 337-360
56. Ballinger, M. D., Tom, J., and Wells, J. A. (1995) Designing subtilisin BPN′ to cleave substrates containing dibasic residues. Biochemistry 34, 13312-13319