Protein L-isoaspartyl methyltransferase repairs abnormal aspartyl residues accumulated in vivo in type-I collagen and restores cell migration

Experimental Cell Research

Volumn 293, Issue 1, 2004, Pages 96-105

  Lanthier, Julie ^a   Desrosiers, Richard R ^a  

^a UNIVERSITÉ DU QUÉBEC À MONTRÉAL   (Canada)

Author keywords

Aging; Collagen; Fibronectin; Integrin; L isoaspartyl residues; Migration; Protein L isoaspartyl methyltransferase

Indexed keywords

ASPARTIC ACID; ASPARTIC PROTEINASE; COLLAGEN TYPE 1; FIBRONECTIN; INTEGRIN; METHYLTRANSFERASE; PEPTIDE; PROTEIN DEXTRO ASPARTATE METHYLTRANSFERASE; RECOMBINANT PROTEIN;

AGING; ANIMAL; ANIMAL CELL; ARTICLE; CELL ADHESION; CELL ASSAY; CELL CULTURE; CELL DEATH; CELL MIGRATION; CELL MOTILITY; CELL MOTION; CHEMISTRY; COMPARATIVE STUDY; DROSOPHILA; ENZYME SPECIFICITY; EXTRACELLULAR MATRIX; GENETICS; HUMAN; IN VIVO STUDY; ISOLATION AND PURIFICATION; KIDNEY TUMOR; METABOLISM; NONHUMAN; PHYSIOLOGY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DETERMINATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; RAT STRAIN; STATISTICAL ANALYSIS; TIME; TUMOR CELL LINE;

EID: 0346690069     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yexcr.2003.10.003     Document Type: Article

References (48)

1. Huttenlocher A., Sandborg R.R., Horwitz A.F. Adhesion in cell migration. Curr. Opin. Cell Biol. 7:1995;697-706.
2. Giancotti F.G., Ruoslahti E. Integrin signaling. Science. 285:1999;1028-1032.
3. Parsons J.T., Martin K.H., Slack J.K., Taylor J.M., Weed S.A. Focal adhesion kinase: a regulator of focal adhesion dynamics and cell movement. Oncogene. 19:2000;5606-5613.
4. Staatz W.D., Fok K.F., Zutter M.M., Adams S.P., Rodriguez B.P., Santoro S.A. Identification of a tetrapeptide recognition sequence for the alpha 2 beta 1 integrin in collagen. J. Biol. Chem. 273:1991;25664-25672.
5. Akiyama S.K., Olden K., Yamada K.M. Fibronectin and integrins in invasion and metastasis. Cancer Metastasis Rev. 14:1995;173-189.
6. Pasqualini R., Koivunen E., Ruoslahti E.A. A peptide isolated from phage display libraries is a structural and functional mimic of an RGD-binding site on integrins. J. Cell Biol. 130:1995;1189-1196.
7. Shiokawa S., Yoshimura Y., Sawa H., Nagamatsu S., Hanashi H., Sakai K., Ando M., Nakamura Y. Functional role of arg-gly-asp (RGD)-binding sites on beta1 integrin in embryo implantation using mouse blastocysts and human decidua. Biol. Reprod. 60:1999;1468-1474.
8. Aswad D.W., Paranandi M.V., Schurter B.T. Isoaspartate in peptides and proteins: formation, significance, and analysis. J. Pharm. Biomed. Anal. 21:2000;1129-1136.
9. Lindner H., Helliger W. Age-dependent deamidation of asparagine residues in proteins. Exp. Gerontol. 36:2001;1551-1563.
10. Clarke S. Aging as war between chemical and biochemical processes: protein methylation and the recognition of age-damaged proteins for repair. Ageing Res. Rev. 2:2003;263-285.
11. Brennan T.V., Anderson J.W., Jia Z., Waygood E.B., Clarke S. Repair of spontaneously deamidated HPr phosphocarrier protein catalyzed by the L-isoaspartate-(D-aspartate)O-methyltransferase. J. Biol. Chem. 269:1994;24586-24595.
12. Johnson B.A., Langmack E.L., Aswad D.W. Partial repair of deamidation-damaged calmodulin by protein carboxyl methyltransferase. J. Biol. Chem. 262:1987;12283-12287.
13. Desrosiers R.R., Romanik E.A., O'Connor C.M. Selective carboxyl methylation of structurally altered calmodulins in Xenopus oocytes. J. Biol. Chem. 265:1990;21368-21374.
14. Najbauer J., Orpiszewski J., Aswad D.W. Molecular aging of tubulin: accumulation of isoaspartyl sites in vitro and in vivo. Biochemistry. 35:1996;5183-5190.
15. Lanthier J., Bouthillier A., Lapointe M., Demeule M., Beliveau R., Desrosiers R.R. Down-regulation of protein L-isoaspartyl methyltransferase in human epileptic hippocampus contributes to generation of damaged tubulin. J. Neurochem. 83:2002;581-591.
16. Paranandi M.V., Guzzetta A.W., Hancock W.S., Aswad D.W. Deamidation and isoaspartate formation during in vitro aging of recombinant tissue plasminogen activator. J. Biol. Chem. 269:1994;243-253.
17. Watanabe A., Takio K., Ihara Y. Deamidation and isoaspartate formation in smeared tau in paired helical filaments. Unusual properties of the microtubule-binding domain of tau. J. Biol. Chem. 274:1999;7368-7378.
18. Sandmeier E., Hunziker P., Kunz B., Sack R., Christen P. Spontaneous deamidation and isomerization of Asn108 in prion peptide 106-126 and in full-length prion protein. Biochem. Biophys. Res. Commun. 261:1999;578-583.
19. Shimizu T., Fukuda H., Murayama S., Izumiyama N., Shirasawa T. Isoaspartate formation at position 23 of amyloid beta peptide enhanced fibril formation and deposited onto senile plaques and vascular amyloids in Alzheimer's disease. J. Neurosci. Res. 70:2002;451-461.
20. Haley E.E., Corcoran B.J., Dorer F.E., Buchanan D.L. Beta-aspartyl peptides in enzymatic hydrolysates of protein. Biochemistry. 5:1966;3229-3235.
21. Bornstein P. Structure of alpha-1-CB8, a large cyanogen bromide produced fragment from the alpha-1 chain of rat collagen. The nature of a hydroxylamine-sensitive bond and composition of tryptic peptides. Biochemistry. 9:1970;2408-2421.
22. Cloos P.A., Fledelius C. Collagen fragments in urine derived from bone resorption are highly racemized and isomerized: a biological clock of protein aging with clinical potential. Biochem. J. 345:2000;473-480.
23. Fledelius C., Johnsen A.H., Cloos P.A., Bonde M., Qvist P. Characterization of urinary degradation products derived from type I collagen. Identification of a beta-isomerized Asp-Gly sequence within the C-terminal telopeptide (alpha1) region. J. Biol. Chem. 272:1997;9755-9763.
24. Brady J.D., Ju J., Robins S.P. Isoaspartyl bond formation within N-terminal sequences of collagen type I: implications for their use as markers of collagen degradation. Clin. Sci. (Lond). 96:1999;209-215.
25. Powell J.T., Vine N., Crossman M. On the accumulation of D-aspartate in elastin and other proteins of the ageing aorta. Atherosclerosis. 97:1992;201-208.
26. Weber D.J., McFadden P.N. Detection and characterization of a protein isoaspartyl methyltransferase which becomes trapped in the extracellular space during blood vessel injury. J. Protein Chem. 16:1997;257-267.
27. Weber D.J., McFadden P.N. Injury-induced enzymatic methylation of aging collagen in the extracellular matrix of blood vessels. J. Protein Chem. 16:1997;269-281.
28. Bornstein M.B. Reconstituted rat tail collagen used as substrate for time tissue cultures on coverslips in Maximow slides and roller tubes. Lab. Invest. 7:1958;134-139.
29. O'Connor M.B., Galus A., Hartenstine M., Magee M., Jackson F.R., O'Connor C.M. Structural organization and developmental expression of the protein isoaspartyl methyltransferase gene from Drosophila melanogaster. Insect Biochem. Mol. Biol. 27:1997;49-54.
30. Boivin D., Gingras D., Béliveau R. Purification and characterization of a membrane-bound protein carboxyl methyltransferase from rat kidney cortex. J. Biol. Chem. 268:1993;2610-2615.
31. Vuento M., Vaheri A. Purification of fibronectin from human plasma by affinity chromatography under non-denaturing conditions. Biochem. J. 183:1979;331-337.
32. Sakai K., Fujii T., Hayashi T. Cell-free formation of disulfide-bonded multimer from isolated plasma fibronectin in the presence of a low concentration of SH reagent under a physiological condition. J. Biochem. (Tokyo). 115:1994;415-421.
33. Lowenson J.D., Clarke S. Recognition of isomerized and racemized aspartyl residues in peptides by the protein L-isoaspartate (D-aspartate) O-methyltransferase. Aswad D.W. Deamidation and Isoaspartate Formation in Peptides and Proteins. 1995;55 CRC Press, Boca Raton.
34. Cloos P.A., Jensen A.L. Age-related de-phosphorylation of proteins in dentin: a biological tool for assessment of protein age. Biogerontology. 1:2000;341-356.
35. Collins M.J., Waite E.R., van Duin A.C. Predicting protein decomposition: the case of aspartic-acid racemization kinetics. Philos. Trans. R. Soc. Lond., B Biol. Sci. 354:1999;51-64.
36. Glanville R.W., Breitkreutz D., Meitinger M., Fietzek P.P. Completion of the amino acid sequence of the alpha 1 chain from type I calf skin collagen. Amino acid sequence of alpha 1(I)B8. Biochem. J. 215:1983;183-189.
37. Ruoslahti E. RGD and other recognition sequences for integrins. Annu. Rev. Cell Dev. Biol. 12:1996;697-715.
38. Newham P., Humphries M.J. Integrin adhesion receptors: structure, function and implications for biomedicine. Mol. Med. Today. 2:1996;304-313.
39. Shaub A. Unravelling the extracellular matrix. Nat. Cell Biol. 1:1999;E173-E175.
40. Chazin W.J., Kossiakoff A.A. The role of secondary and tertiary structures in intramolecular deamidation of proteins. Aswad D.W. Deamidation and Isoaspartate Formation in Peptides and Proteins. 1995;205 CRC Press, Boca Raton.
41. Aota S., Nomizu M., Yamada K.M. The short amino acid sequence Pro-His-Ser-Arg-Asn in human fibronectin enhances cell-adhesive function. J. Biol. Chem. 269:1994;24756-24761.
42. Wong J.Y., Weng Z., Moll S., Kim S., Brown C.T. Identification and validation of a novel cell-recognition site (KNEED) on the 8th type III domain of fibronectin. Biomaterials. 23:2002;3865-3870.
43. Xu Y., Gurusiddappa S., Rich R.L., Owens R.T., Keene D.R., Mayne R., Hook A., Hook M. Multiple binding sites in collagen type I for the integrins alpha1beta1 and alpha2beta1. J. Biol. Chem. 275:2000;38981-38989.
44. Reed M.J., Ferara N.S., Vernon R.B. Impaired migration, integrin function, and actin cytoskeletal organization in dermal fibroblasts from a subset of aged human donors. Mech. Ageing Dev. 122:2001;1203-1220.
45. Sandeman S.R., Allen M.C., Liu C., Faragher R.G., Lloyd A.W. Human keratocyte migration into collagen gels declines with in vitro ageing. Mech. Ageing Dev. 119:2000;149-157.
46. Paul R.G., Bailey A.J. The effect of advanced glycation end-product formation upon cell-matrix interactions. Int. J. Biochem. Cell Biol. 31:1999;653-660.
47. Verzijl N., DeGroot J., Oldehinkel E., Bank R.A., Thorpe S.R., Baynes J.W., Bayliss M.T., Bijlsma J.W., Lafeber F.P., Tekoppele J.M. Age-related accumulation of Maillard reaction products in human articular cartilage collagen. Biochem. J. 350:2000;381-387.
48. Monboisse J.C., Rittie L., Lamfarraj H., Garnotel R., Gillery P. In vitro glycoxidation alters the interactions between collagens and human polymorphonuclear leucocytes. Biochem. J. 350:2000;777-783.