Identification of preferred substrate sequences for transglutaminase 1 - Development of a novel peptide that can efficiently detect cross-linking enzyme activity in the skin

FEBS Journal

Volumn 275, Issue 22, 2008, Pages 5667-5677

  Sugimura, Yoshiaki ^a   Hosono, Masayo ^a   Kitamura, Miyako ^a   Tsuda, Tatsuya ^b   Yamanishi, Kiyofumi ^b   Maki, Masatoshi ^a   Hitomi, Kiyotaka ^a  

^a NAGOYA UNIVERSITY   (Japan)

^b HYOGO COLLEGE OF MEDICINE   (Japan)

Author keywords

Epidermis; Keratinocyte; Phage display; Skin; Transglutaminase

Indexed keywords

GLUTATHIONE TRANSFERASE; HYBRID PROTEIN; PEPTIDE LIBRARY; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE;

AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; CROSS LINKING; ENZYME ACTIVITY; EPIDERMIS; HUMAN; HUMAN CELL; IN SITU HYBRIDIZATION; KERATINOCYTE; PHAGE DISPLAY; PRIORITY JOURNAL;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; ENZYMES; ISOENZYMES; MICE; PEPTIDE LIBRARY; PEPTIDES; SKIN; SUBSTRATE SPECIFICITY; TRANSGLUTAMINASES;

EID: 54849408758     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2008.06692.x     Document Type: Article

References (48)

1. Griffin M, Casadio R Bergamini CM (2002) Transglutaminases: nature's biological glues. Biochem J 368, 377 396.
2. Lorand L Graham RM (2003) Transglutaminases: crosslinking enzymes with pleiotropic functions. Nat Rev Mol Cell Biol 4, 140 156.
3. Ichinose A (2001) Physiopathology and regulation of factor XIII. Thromb Haemost 86, 57 65.
4. Fésüs L Piacentini M (2002) Transglutaminase 2: an enigmatic enzyme with diverse functions. Trends Biochem Sci 27, 534 539.
5. Fésüs L Szondy Z (2005) Transglutaminase 2 in the balance of cell death and survival. FEBS Lett 579, 3297 3302.
6. Telci D Griffin M (2006) Tissue transglutaminase (TG2) - a wound response enzyme. Front Biosci 11, 867 882.
7. Kim SY, Chung S-I Steinert PM (1995) Highly active soluble processed forms of the transglutaminase 1 enzyme in epidermal keratinocytes. J Biol Chem 270, 18026 18035.
8. Eckert RL, Sturniolo MT, Broome M, Ruse M Rorke E (2005) Transglutaminase function in epidermis. J Invest Dermatol 124, 481 492.
9. Hitomi K (2005) Transglutaminase in skin epidermis. Eur J Dermatol 15, 313 319.
10. Kalinin AE, Andrey VK Steinert PM (2002) Epithelial barrier function: assembly and structural features of the cornified envelop. Bioessays 24, 789 800.
11. Zeeuwen PL (2004) Epidermal differentiation: the role of proteases and their inhibitors. Eur J Cell Biol 83, 761 773.
12. Candi E, Schmidt R Melino G (2005) The cornified envelope: a model of cell death in the skin. Nat Rev Mol Cell Bio 6, 328 340.
13. Kim I-G, Gorman JJ, Park S-C, Chung S-I Steinert PM (1993) The deduced sequence of the novel protransglutaminase E (TGase3) of human and mouse. J Biol Chem 268, 12682 12690.
14. Kim S-Y, Chung S-I, Yoneda K Steinert PM (1995) Expression of transglutaminase 1 in human epidermis. J Invest Dermatol 104, 211 217.
15. Hitomi K, Horio Y, Ikura K, Yamanishi K Maki M (2001) Analysis of epidermal-type transglutaminase expression in mouse tissues and cell lines. Int J Biochem Cell Biol 33, 491 498.
16. Hitomi K, Presland RB, Nakayama T, Fleckman P, Dale BA Maki M (2003) Analysis of epidermal-type transglutaminase (transglutaminase 3) in human stratified epithelia and cultured keratinocytes using monoclonal antibodies. J Dermatol Sci 32, 95 103.
17. Candi E, Oddi S, Terrinoni A, Paradisi A, Ranalli M, Finazzi-Agro A Melino G (2001) Transglutaminase 5 cross-links loricrin, involucrin, and small proline-rich proteins in vitro. J Biol Chem 276, 35014 35023.
18. Candi E, Oddi S, Paradisi A, Terrinoni A, Ranalli M, Teofoli P, Citro G, Scarpato S, Puddu P Melino G (2002) Expression of transglutaminase 5 in normal and pathologic human epidermis. J Invest Dermatol 119, 670 677.
19. Steinert PM, Kim SY, Chung S-I Marekov LN (1996) The transglutaminase 1 enzyme is variably acylated by myristate and palmitate during differentiation in epidermal keratinocytes. J Biol Chem 271, 26242 26250.
20. Matsuki M, Yamashita F, Ishida-Yamamoto A, Yamada K, Kinoshita C, Fushiki S, Ueda E, Morishima Y, Tabata K, Yasuno H et al. (1998) Defective stratum corneum and early neonatal death in mice lacking the gene for transglutaminase 1. Proc Natl Acad Sci USA 95, 1044 1049.
21. Huber M, Rettler I, Bernasconi K, Frenk E, Lavrijsen SPM, Ponec M, Bon A, Lautenschlager S, Schorderet DF Hohl D (1995) Mutations of keratinocyte transglutaminase in lamellar ichthyosis. Science 267, 525 528.
22. Russell LJ, DiGiovanna JJ, Rogers GR, Steinert PM, Hashem N, Compton JG Bale SJ (1995) Mutations in the gene for transglutaminase 1 in autosomal recessive lamellar ichthyosis. Nat Genet 9, 279 283.
23. Huber M, Yee VC, Burri N, Vikerfors E, Lavrijsen APM, Paller AS Hohl D (1997) Consequences of seven novel mutations on the expression and structure of keratinocyte transglutaminase. J Biol Chem 272, 21018 21026.
24. Candi E, Melino G, Lahm A, Ceci R, Rossi A, Kim I-G, Ciani B Steinert PM (1998) Transglutaminase 1 mutations in lamellar ichthyosis. Loss of activity due to failure of activation by proteolytic processing. J Biol Chem 273, 13693 13702.
25. Akiyama M, Takizawa Y, Suzuki Y, Ishiko A, Matsuo I Shimizu H (2001) Compound heterozygous TGM1 mutations including a novel missense mutation L204Q in a mild form of lamellar ichthyosis. J Invest Dermatol 116, 992 995.
26. Jans R, Sturniolo MT Eckert R (2007) Localization of the TIG3 transglutaminase interaction domain and demonstration that the amino-terminal region is required for TIG3 function as a keratinocyte differentiation regulator. J Invest Dermatol 128, 517 529.
27. Esposito C Caputo I (2005) Mammalian transglutaminases: identification of substrates as a key to physiological function and physiological relevance. FEBS J 272, 615 631.
28. Facchiano AM, Facchiano A Facchiano F (2003) Active sequences collection (ASC) database: a new tool to assign functions to protein sequences. Nucleic Acids Res 31, 379 382.
29. Candi E, Melino G, Mei G, Tarcsa E, Chung S-I, Marekov LN Steinert PM (1995) Biochemical, structural, and transglutaminase substrate properties of human loricrin, the major epidermal cornified cell envelope protein. J Biol Chem 270, 26382 26390.
30. Steinert PM Marekov LN (1997) Direct evidence that involucrin is a major early isopeptide cross-linked component of the keratinocyte cornified cell envelope. J Biol Chem 272, 2021 2030.
31. Candi E, Tarcsa E, Idler WW, Kartasova T, Marekov LN Steinert PM (1999) Transglutaminase cross-linking properties of the small proline-rich 1 family of cornified cell envelope proteins. Integration with loricrin. J Biol Chem 274, 7226 7237.
32. Tarcsa E, Marekov LN, Andreoli J, Idler WW, Candi E, Chung S-I Steinert P (1997) The fate of trichohyalin: sequential post-translational modifications by peptidyl-arginine deiminase and transglutaminase. J Biol Chem 272, 27893 27901.
33. Sugimura Y, Hosono M, Wada F, Yoshimura T, Maki M Hitomi K (2006) Screening for the preferred substrate sequence of transglutaminase using a phage-displayed peptide library: identification of peptide substrates for TGase 2 and factor XIIIa. J Biol Chem 281, 17699 17706.
34. Hitomi K, Kitamura M Sugimura Y (2008) Preferred substrate sequences for transglutaminase 2: screening using a phage-displayed peptide library. Amino Acids, doi
35. Sugimura Y, Ueda H, Maki M Hitomi K (2007) Novel site-specific immobilization of a functional protein using a preferred substrate sequence for transglutaminase 2. J Biotechnol 131, 121 127.
36. Tarcsa E, Candi E, Kartasova T, Idler WW, Marekov LN Steinert PM (1998) Structural and transglutaminase substrate properties of the small proline-rich 2 family of cornified cell envelope proteins. J Biol Chem 273, 23297 23303.
37. Steinert PM, Candi E, Tarcsa E, Marecov LN, Sette M, Paci M, Ciani B, Guerrieri P Melino G (1999) Transglutaminase crosslinking and structural studies of the human small proline rich 3 protein. Cell Death Differ 6, 916 930.
38. Keresztessy Z, Csosz É, Hársfalvi J, Csomós K, Gray J, Lightowlers RN, Lakey JH, Balajthy Z Fésüs L (2006) Phage display selection of efficient glutamine-donor substrate peptides for transglutaminase 2. Protein Sci 15, 2466 2480.
39. Sollid LM (2002) Coeliac disease: dissecting a complex inflammatory disorder. Nat Rev Immunol 2, 647 655.
40. Hiiragi T, Sasaki H, Nagafuchi A, Sabe H, Shen SC, Matsuki M, Yamanishi K Tsukita S (1999) Transglutaminase type 1 and its cross-linking activity are concentrated at adherens junctions in simple epithelial cells. J Biol Chem 274, 34148 34154.
41. Iizuka R, Chiba K Ohmi-Imajoh S (2003) A novel approach for the detection of proteolytically activated transglutaminase 1 in epidermis using cleavage site-directed antibodies. J Invest Dermatol 121, 457 464.
42. Oji V, Oji ME, Adamini N, Walker T, Aufenvenne K, Raghunath M Traupe H (2006) Plasminogen activator inhibitor-2 is expressed in different types of congenital ichthyosis: in vivo evidence for its cross-linking into the cornified cell envelope by transglutaminase-1. Br J Dermatol 154, 860 867.
43. Furutani Y, Kato A, Notoya M, Ghoneim MA Hirose S (2001) A simple assay and histochemical localization of transglutaminase activity using a derivative of green fluorescent protein as substrate. J Histochem Cytochem 49, 247 258.
44. Sugimura Y, Yokoyma K, Nio N, Maki M Hitomi K (2008) Identification of preferred substrate sequences of microbial transglutaminase from Streptomyces mobaraensis using a phage-displayed peptide library. Arch Biophys Biochem 477, 379 383.
45. Pietroni V, Giorgi SD, Paradisi A, Ahvazi B, Candi E Melino G (2008) Inactive and highly active, proteolytically processed transglutaminase-5 in epithelial cells. J Invest Dermatol, doi
46. Hitomi K, Yamagiwa Y, Yamanishi K Maki M (2000) Characterization of human recombinant transglutaminase 1 purified from baculovirus-infected insect cells. Biosci Biotechnol Biochem 64, 2128 2137.
47. Hitomi K, Kanehiro S, Ikura K Maki M (1999) Characterization of recombinant mouse epidermal-type transglutaminase (TGase 3): regulation of its activity by proteolysis and guanine nucleotides. J Biochem (Tokyo) 125, 1048 1054.
48. Ikura K, Yokota H, Sasaki R Chiba H (1989) Amino acid sequence of guinea pig liver transglutaminase from its cDNA sequence. Biochemistry 28, 2344 2348.