Transglutaminase crosslinking and structural studies of the human small proline rich 3 protein

Cell Death and Differentiation

Volumn 6, Issue 9, 1999, Pages 916-930

  Steinert, Peter M ^a   Candi, Eleonora ^a,b   Tarcsa, Edit ^a   Marekov, Lyuben N ^a   Sette, Marco ^b   Paci, Maurizio ^b   Ciani, Barbara ^b   Guerrieri, Pietro ^b   Melino, Gerry ^b  

^a NATIONAL INSTITUTE OF ARTHRITIS AND MUSCULOSKELETAL AND SKIN DISEASES   (United States)

^b UNIVERSITY OF ROME TOR VERGATA   (Italy)

Author keywords

Barrier function; Cell envelope; Circular dichroism; Cross linking; Epithelia; Nuclear magnetic resonance; Skin; Small proline rich proteins; Transglutaminase

Indexed keywords

PROLINE; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE; RECOMBINANT PROTEIN; SYNTHETIC PEPTIDE; TRIFLUOROETHANOL; WATER;

AMINO ACID SEQUENCE; ARTICLE; CELL FUNCTION; CELL STRUCTURE; CIRCULAR DICHROISM; CROSS LINKING; HUMAN; HYDROGEN BOND; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN SECONDARY STRUCTURE; SQUAMOUS EPITHELIUM; TEMPERATURE;

EID: 0032831669     PISSN: 13509047     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.cdd.4400568     Document Type: Article

References (60)

1. Holbrook KA and Wolff K (1993) The structure and development of the skin. In: Dermatology in General Medicine. Fitzpatrick TB, Eisen AZ, Wolff K, Freedberg IM and Austen KF, (eds). McGraw-Hill, Inc., New York, pp 97-144
2. Polakowska RR and Haake AR (1994) The skin from a new perspective. Cell Death Differ. 1: 11-18
3. Melino G, De Laurenzi V, Catani MV, Terrinoni A, Ciani B, Candi E, Marekov LM and Steinert PM (1998) The cornified envelope: a model of cell death in the skin. In: Apoptosis: Biology, Mechanisms and Role in Disease. Kumar S (ed), Results Probl. Cell Differ. 24: 175-212
4. Reichert U, Michel S and Schmidt R (1993) The cornified envelope: A key structure of terminally differentiating keratinocytes. In Molecular Biology of the Skin. Darmon M and Blumenberg M (eds), Academic Press, Inc., New York, pp 107-150
5. Hohl D (1990) Cornified Cell envelope. Dermatologica 180: 201-211
6. Simon M (1994) The epidermal cornified envelope and its precursors. In: The Keratinocyte Handbook. Leigh IM, Lane EB and Watt FM (eds). Cambridge University Press, Cambridge, pp 275-292
7. Steinert PM (1995) A model for the hierarchical structure of the human epidermal cornified cell envelope. Cell Death Differ. 2: 33-40
8. Steinert PM and Marekov LN (1995) The proteins elafin, filaggrin, keratin intermediate filaments, loricrin, and small proline-rich proteins 1 and 2 are isodipeptide cross-linked components of the human epiderma cornified cell envelope. J. Biol. Chem. 270: 17702-17711
9. Steinert PM and Marekov LN (1997) Involucrin is an important early component in the assembly of the epidermal cornified cell envelope. J. Biol. Chem. 272: 2021-2030
10. Steinert PM, Kartasova T and Marekov LN (1998) Biochemical evidence that small proline-rich proteins and trichohyalin function in epithelia by modulation of the biomechanical properties of their cornified cell envelopes. J. B ol. Chem. 273: 11758-11769
11. Robinson NA, Lapic S, Welter JF and Eckert RL (1997) S100A11, S100A10, annexin I, desmosomal proteins, small proline-rich proteins, plasminogen activator inhibitor-2, and involucrin are components of the cornified envelope of cultured human epidermal keratinocytes. J. Biol. Chem. 272: 12035-12046
12. Jarnik M, Kartasova T, Steinert PM, Lichti U and Steven AC (1996) Differential expression and cell envelope incorporation of small proline-rich protein 1 in different cornified epithelia. J. Cell Sci. 109: 1381-1391
13. Jarnik M, Simon MN and Steven AC (1998) Cornified cell envelope assembly: a model based on electron microscopic determinations of thickness and projected density. J. Cell Sci. 111: 1051-1060
14. Candi E, Melino G, Mei G, Tarcsa E, Chung SI, 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
15. Nagy L, Thomazy VA, Saydak MM, Stein JP and Davis PJA (1997) The promoter of the mouse tissue transglutaminase gene directs tissue-specific, retinoid regulated and apoptosis-linked expression. Cell Death Differ. 4: 534-547
16. 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
17. Tarcsa E, Candi E, Kartasova T, Idler WW, Marekov LN and 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
18. Aeschlimann D, Koeller MK, Allen-Hoffmann BL and Mosher DF (1998) Isolation of a cDNA encoding a novel member of the transglutaminase gene family from human keratinocytes. Detection and identification of transglutaminase gene products based on reverse transcription-polymerase chain reaction with degenerate primers. J. Biol. Chem. 273: 3452-3460
19. Gibbs S, Fijneman R, Wiegant J, van Kessel AG, van de Putte P and Backendorf C (1993) Molecular characterization and evolution of the SPRR family of keratinocyte differentiation markers encoding small proline-rich proteins. Genomics 16: 630-637
20. Kartasova T, Darwiche N, Kohno Y, Koizumi H, Osada S, Huh N, Lichti U, Steinert PM and Kuroki T (1996) Sequence and expression patterns of mouse SPR1: Correlation of expression with epithelial function. J. Invest. Dermatol. 106: 294-304
21. Steinert PM, Candi E, Kartasova T and Marekov LN (1998) Small proline-rich proteins are cross-bridging proteins in the cornified cell envelopes of stratified squamous epithelia. J. Struct. Biol. 122: 76-85
22. Song H-J, Poy G, Darwiche N, Lichti U, Kuroki T, Kartasova T and Steinert PM (1999) Mouse Sprr2 genes: a clustered family of genes showing differential expression in epithelial tissues. Genomics 55: 28-42
23. Hohl D, de Viragh PA, Armiguet-Barras F, Gibbs S, Backendorf C and Huber M (1995) The small proline-rich proteins constitute a multigene family of differentially regulated cornified cell envelope precursor proteins. J. Invest. Dermatol. 106: 902-909
24. Austin SJ, Fujimoto W, Marvin KW, Vollberg TM, Lorand L and Jetten AM (1996) Cloning and regulation of cornifin beta, a new member of the cornifin/spr family. Suppression by retinoic acid receptor-selective retinoids. J. Biol. Chem. 271: 3737-3742
25. Fujimoto W, Nakanishi G, Arata J and Jetten AM (1997) Differential expression of human cornifin alpha and beta in squamous differentiating epithelial tissues and several skin lesions. J. Invest. Dermatol. 108: 200-204
26. Steinert PM, Chung S-I and Kim S-Y (1996) Inactive zymogen and highly active proteolytically processed membrane-bound forms of the transglutaminase 1 enzyme in human epidermal keratinocytes. Biochem. Biophys. Res. Commun. 221: 101-106
27. Birchbirchler PJ, Orr GR, Carter HA and Patterson MK (1977) Biochem. Res. Commun. 78: 1-7
28. Barry EL and Mosher DF (1990) Binding and degradation of blood coagulation factor XIII by cultured fibroblasts. J. Biol. Chem. 265: 9302-9307
29. Traupe H (1989) The Ichthyoses: A Guide to Clinical Diagnosis, Genetic Counseling and Therapy. Springer-Verlag, Heidelberg.
30. Matsuki M, Yamashita F, Ishida-Yamamoto A, Yamada K, Kinoshita C, Fushiki S, Ueda E, Morishima Y, Tabata K, Yasuno H, Hashida M, Iizuka H, Ikawa M, Okabe M, Kondoh G, Kinoshita T, Takeda J and Yamanishi K (1998) Defective stratum corneum and early neonatal death in mice lacking the gene for transglutaminase 1 (keratinocyte transglutaminase). Proc. Natl. Acad. Sci. USA 95:1044-1049
31. Isemura T, Asakura J, Shibata S, Iasemura S, Saitoh E and Sanada K (1983) Conformational study of the salivary proline-rich polypeptides. Int. J. Peptide Protein Res. 21: 281-287
32. Shibata S, Asakura J, Isemura T, Isemura S, Saitoh E and Sanada K (1984) Conformational study of the basic proline-rich polypeptides from human parotid saliva. Int. J. Peptide Protein Res. 23: 158-165
33. Raj PA, Edgerton M and Levine MJ. (1990) Salivary Histatin 5: dependence of sequence, chain length and helical conformation for candidacidal activity. J. Biol. Chem. 265: 3898-3905
34. Raj PA, Johnsson M, Levine MJ and Nancollas GH (1992) Salivary staherin: dependence of sequence, charge, hydrogen bonding potency, and helical conformation for adsorption to hydroxyapatite and inhibition of mineralization. J. Biol. Chem. 267: 5968-5976
35. Tanford C (1970) Theoretical models for the mechanism of denaturation. Adv. Prot. Chem. 24: 1-95
36. Darrell Fontenot J, Tiandra N, Bu D, Ho C, Montelaro RC and Finn OJ (1993) Biophysical characterization of one-, two-, and three-tandem repeats of human mucin (muc-1) protein core. Cancer Research 53: 5386-5394
37. Woody RW (1976) Studies of theoretical circular dichroism of polypeptides: contributions of beta turns. In: Blout ER, et al. (ed.). Peptides, polypeptides and proteins. New York, Wiley, pp. 338-350
38. Tatham AS, Drake AF and Shewry PR (1985) A conformational study of a glutamine-and proline-rich cereal seed protein C hordein. Biochem. J. 226: 557-562
39. Groß KH and Kalbitzer HR (1998) Distribution of chemical shifts in 1H nuclear magnetic resonance spectra of proteins. J. Magn. Reson. 76: 87-89
40. Urry DW (1997) Physical chemistry of biological free energy transduction as demonstrated by elastic protein-based polymers. J. Phys. Chem. 101: 11007-11028
41. Jimenez MA, Bruix M, Gonzalez C, Blanco FJ, Nieto JL, Herranz J and Rico M (1993) CD and 1H-NMR studies on the conformational properties of peptide fragments from the C-terminal domain of thermolysin. Eur J Biochem 211(3): 569-581
42. O'Neal KD, Chari MV, McDonald CH, Cook RG, Yuu-LeeL-Y, Morrissett JDand Shearer WT (1986) Multiple cis-trans conformers of the prolactin receptor proline-rich motif (PRM) peptide detected by reverse-phase HPLC, CD and NMR spectroscopy. Biochem. J. 315: 833-844
43. Dyson HJ, Rance M, Houghten RA and Wright PE (1998) Folding of immunogenic peptide fragments in water solution. J. Mol. Biol. 201: 161-200
44. Williamson MP (1993) Peptide structure determination by NMR. Methods Mol. Biol. 17: 69-85
45. Rose DR, Gierasch LM and Smith JA (1985) Turns in peptides and proteins. Adv. Prot. Chem. 37: 1-109
46. Wutrich K (1986) NMR of proteins and nucleic acids. John Wiley & Sons, New York.
47. Wilmot CM and Thornton JM (1988) Analysis and prediction of the different types of beta-turn in proteins. J. Mol. Biol. 205: 221-232
48. Chou PY and Fasman GD (1977) β-turns in proteins. J. Mol. Biol. 115:135-175
49. Fontenot JD, Mariappan SV, Catasti P, Domenech N, Finn OJ and Gupta G (1995) Structure of a tumor associated antigen containing a tandemly repeated immunodominant epitope. J. Biomol. Struct. Dyn. 13: 245-260
50. Leszczynski JF and Rose GD (1986) Loops in globular proteins: a novel category of secondary structure. Science 234: 849-855
51. Candi E, Melino G. Lahm A, Ceci R, Rossi A, Kim IG, Ciani B and 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
52. Kim H-C, Lewis MS, Gorman JJ, Park S-C, Girard JE, Folk JE and Chung S-I (1990) Protransglutaminase E from guinea pig skin. Isolation and partial characterization. J. Biol. Chem. 265: 21971-21978
53. Hohl D, Lichti U, Turner ML, Roop DR and Steinert PM (1991) Characterization of human loricrin. Structure and function of a new class of epidermal cell envelope proteins. J. Biol. Chem. 266: 6626-6636
54. Jeener J, Meier BH, Bachmann P and Ernst RR (1979) Investigation of exchange processes by two-dimensional NMR spectroscopy. J. Chem. Phys. 71: 4546-4553
55. Bax A and Davis DG (1985) Practical aspects of two-dimensional transverse NOE spectroscopy. J. Magn. Res. 63: 207-213
56. Griesinger C and Ernst RR (1987) Frequency offset effects and their elimination in NMR Rotating-Frame Cross-Relaxation spectroscopy. J. Magn. Reson. 75: 261-271
57. Brunger AT (1992) XPLOR, a system for crystallography and NMR. Yale University Press, New Haven, CT.
58. Nilges M, Clore GM and Gronenborn AM (1988) Determination of three-dimensional structures of proteins from interproton distance data by dynamical simulated annealing from a random array of atoms. Circumventing problems associated with folding. FEBS Lett. 229: 317-324
59. Nilges M, Gronenborn AM, Brunger AT and Clore GM (1998) Determination of three-dimensional structures of proteins by simulated annealing with interproton distance restraints. Application to crambin, potato carboxypeptidase inhibitor and barley serine proteinase inhibitor 2. Protein Eng. 2: 27-38
60. Kim S-Y, Kim I-G, Chung S-I and Steinert PM (1994) The structure of the transglutaminase 1 enzyme: deletion cloning reveals domains which regulate its specific activity and substrate specificity. J. Biol. Chem. 269: 27979-27986