Differential effects on light chain amyloid formation depend on mutations and type of glycosaminoglycans

Journal of Biological Chemistry

Volumn 290, Issue 8, 2015, Pages 4953-4965

  Blancas Mejía, Luis M ^a   Hammernik, Jared ^b   Marin Argany, Marta ^a   Ramirez Alvarado, Marina ^a  

^a MAYO GRADUATE SCHOOL   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALUMINUM; GLYCOPROTEINS;

AMYLOID FORMATION; AMYLOIDOGENICITY; BIOLOGICALLY RELEVANT MOLECULES; CHONDROITIN SULFATES; DIFFERENTIAL EFFECT; GLYCOSAMINOGLYCANS; HEPARAN SULFATES; PROPERTIES OF AL;

PROTEINS;

AMYLOID; CHONDROITIN 4 SULFATE; GLYCOSAMINOGLYCAN; HEPARAN SULFATE; AMYLOID PROTEIN; CHONDROITIN SULFATE; IMMUNOGLOBULIN KAPPA CHAIN;

ARTICLE; CELL AGGREGATION; CHEMICAL STRUCTURE; CONTROLLED STUDY; GEL PERMEATION CHROMATOGRAPHY; IN VITRO STUDY; IN VIVO STUDY; MUTATIONAL ANALYSIS; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FOLDING; SIGNAL TRANSDUCTION; THERMODYNAMICS; WILD TYPE; AMINO ACID SUBSTITUTION; AMYLOIDOSIS; CHEMISTRY; GENETICS; HUMAN; METABOLISM; MISSENSE MUTATION; PROTEINOSIS;

AMINO ACID SUBSTITUTION; AMYLOIDOGENIC PROTEINS; AMYLOIDOSIS; CHONDROITIN SULFATES; HEPARITIN SULFATE; HUMANS; IMMUNOGLOBULIN KAPPA-CHAINS; MUTATION, MISSENSE; PROTEIN AGGREGATION, PATHOLOGICAL;

EID: 84929105231     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.615401     Document Type: Article

References (50)

1. Merlini, G., and Stone, M.J. (2006) Dangerous small B-cell clones. Blood 108, 2520-2530
2. Kumar, S. K., Dispenzieri, A., Lacy, M. Q., Hayman, S. R., Buadi, F. K., Zeldenrust, S. R., Tan, T., Sinha, S., Leung, N., Kyle, R.A., Rajkumar, S. V., and Gertz, M.A. (2011) Changes in serum-free light chain rather than intact monoclonal immunoglobulin levels predicts outcome following therapy in primary amyloidosis. Am. J. Hematol. 86, 251-255
3. Blancas-Mejía, L. M., and Ramirez-Alvarado, M. (2013) Systemic amyloidoses. Annu. Rev. Biochem. 82, 745-774
4. Abraham, R.S., Geyer, S. M., Price-Troska, T. L., Allmer, C., Kyle, R.A., Gertz, M.A., and Fonseca, R. (2003) Immunoglobulin light chain variable (V) region genes influence clinical presentation and outcome in light chain-associated amyloidosis (AL). Blood 101, 3801-3808
5. Janeway, C.A. (2001) How the immune system works to protect the host from infection: a personal view. Proc. Natl. Acad. Sci. U.S.A. 98, 7461-7468
6. Dispenzieri, A., Gertz, M.A., and Buadi, F. (2012) What do I need to know about immunoglobulin light chain (AL) amyloidosis? Blood Rev. 26, 137-154
7. Falk, R. H. (2005) Diagnosis and Management of the cardiac amyloidoses. Circulation 112, 2047-2060
8. Dubrey, S. W., Cha, K., Anderson, J., Chamarthi, B., Reisinger, J., Skinner, M., and Falk, R. H. (1998) The clinical features of immunoglobulin lightchain (AL) amyloidosis with heart involvement. QJM 91, 141-157
9. Kyle, R.A., and Gertz, M.A. (1995) Primary systemic amyloidosis: clinical and laboratory features in 474 cases. Semin. Hematol. 32, 45-59
10. Randles, E. G., Thompson, J.R., Martin, D.J., and Ramirez-Alvarado, M. (2009) Structural alterations within native amyloidogenic immunoglobulin light chains. J. Mol. Biol. 389, 199-210
11. Wall, J.S., Gupta, V., Wilkerson, M., Schell, M., Loris, R., Adams, P., Solomon, A., Stevens, F., and Dealwis, C. (2004) Structural basis of light chain amyloidogenicity: comparison of the thermodynamic properties, fibrillogenic potential and tertiary structural features of fourV6 proteins. J. Mol. Recognit. 17, 323-331
12. Pokkuluri, P. R., Gu, M., Cai, X., Raffen, R., Stevens, F.J., and Schiffer, M. (2002) Factors contributing to decreased protein stability when aspartic acid residues are in α-sheet regions. Protein Sci. 11, 1687-1694
13. Hernández-Santoyo, A., del Pozo Yauner, L., Fuentes-Silva, D., Ortiz, E., Rudiño-Piñera, E., Sánchez-López, R., Horjales, E., Becerril, B., and Rodríguez-Romero, A. (2010)Asingle mutation at the sheet switch region results in conformational changes favoring6 light-chain fibrillogenesis. J. Mol. Biol. 396, 280-292
14. Schormann, N., Murrell, J.R., Liepnieks, J.J., and Benson, M.D. (1995) Tertiary structure of an amyloid immunoglobulin light chain protein: a proposed model for amyloid fibril formation. Proc. Natl. Acad. Sci. U.S.A. 92, 9490-9494
15. Hurle, M.R., Helms, L.R., Li, L., Chan, W., and Wetzel, R. (1994)Arole for destabilizing amino acid replacements in light-chain amyloidosis. Proc. Natl. Acad. Sci. U.S.A. 91, 5446-5450
16. Wall, J., Schell, M., Murphy, C., Hrncic, R., Stevens, F.J., and Solomon, A. (1999) Thermodynamic instability of human 6 light chains: correlation with fibrillogenicity. Biochemistry 38, 14101-14108
17. Wetzel, R. (1997) Domain stability in immunoglobulin light chain deposition disorders. Adv. Protein Chem. 50, 183-242
18. Poshusta, T. L., Katoh, N., Gertz, M.A., Dispenzieri, A., and Ramirez-Alvarado, M. (2013) Thermal stability threshold for amyloid formation in light chain amyloidosis. Int. J. Mol. Sci. 14, 22604-22617
19. Buxbaum, J. N., and Linke, R. P. (2012) A molecular history of the amyloidoses. J. Mol. Biol. 421, 142-159
20. Stevens, F.J., and Kisilevsky, R. (2000) Immunoglobulin light chains, glycosaminoglycans, and amyloid. Cell. Mol. Life Sci. 57, 441-449
21. Bishop, J.R., Schuksz, M., and Esko, J.D. (2007) Heparan sulphate proteoglycans fine-tune mammalian physiology. Nature 446, 1030-1037
22. Shi, X., and Zaia, J. (2009) Organ-specific heparan sulfate structural phenotypes. J. Biol. Chem. 284, 11806-11814
23. Varki, A. (2006) Nothing in glycobiology makes sense, except in the light of evolution. Cell 126, 841-845
24. Bosman, F. T., and Stamenkovic, I. (2003) Functional structure and composition of the extracellular matrix. J. Pathol. 200, 423-428
25. Nelson, S. R., Lyon, M., Gallagher, J.T., Johnson, E.A., and Pepys, M.B. (1991) Isolation and characterization of the integral glycosaminoglycan constituents of human amyloid A and monoclonal light-chain amyloid fibrils. Biochem. J. 275, 67-73
26. Ohishi, H., Skinner, M., Sato-Araki, N., Okuyama, T., Gejyo, F., Kimura, A., Cohen, A. S., and Schmid, K. (1990) Glycosaminoglycans of the hemodialysis-associated carpal synovial amyloid and of amyloid-rich tissues and fibrils of heart, liver, and spleen. Clin. Chem. 36, 88-91
27. Jiang, X., Myatt, E., Lykos, P., and Stevens, F.J. (1997) Interaction between glycosaminoglycans and immunoglobulin light chains. Biochemistry 36, 13187-13194
28. Trinkaus-Randall, V., Walsh, M.T., Steeves, S., Monis, G., Connors, L. H., and Skinner, M. (2005) Cellular response of cardiac fibroblasts to amyloidogenic light chains. Am. J. Pathol. 166, 197-208
29. Martin, D.J., and Ramirez-Alvarado, M. (2011) Glycosaminoglycans promote fibril formation by amyloidogenic immunoglobulin light chains through a transient interaction. Biophys. Chem. 158, 81-89
30. Ren, R., Hong, Z., Gong, H., Laporte, K., Skinner, M., Seldin, D.C., Costello, C. E., Connors, L. H., and Trinkaus-Randall, V. (2010) Role of glycosaminoglycan sulfation in the formation of immunoglobulin light chain amyloid oligomers and fibrils. J. Biol. Chem. 285, 37672-37682
31. McLaughlin, R.W., De Stigter, J. K., Sikkink, L.A., Baden, E.M., and Ramirez-Alvarado, M. (2006) The effects of sodium sulfate, glycosaminoglycans, and Congo red on the structure, stability, and amyloid formation of an immunoglobulin light-chain protein. Protein Sci. 15, 1710-1722
32. Baden, E.M., Randles, E. G., Aboagye, A. K., Thompson, J.R., and Ramirez-Alvarado, M. (2008) Structural insights into the role of mutations in amyloidogenesis. J. Biol. Chem. 283, 30950-30956
33. Blancas-Mejía, L. M., Tischer, A., Thompson, J.R., Tai, J., Wang, L., Auton, M., and Ramirez-Alvarado, M. (2014) Kinetic control in protein folding for light chain amyloidosis and the differential effects of somatic mutations. J. Mol. Biol. 426, 347-361
34. Baden, E.M., Owen, B.A., Peterson, F. C., Volkman, B. F., Ramirez-Alvarado, M., and Thompson, J.R. (2008) Altered dimer interface decreases stability in an amyloidogenic protein. J. Biol. Chem. 283, 15853-15860
35. Sikkink, L.A., and Ramirez-Alvarado, M. (2008) Salts enhance both protein stability and amyloid formation of an immunoglobulin light chain. Biophys. Chem. 135, 25-31
36. DiCostanzo, A.C., Thompson, J.R., Peterson, F. C., Volkman, B. F., and Ramirez-Alvarado, M. (2012) Tyrosine residues mediate fibril formation in a dynamic light chain dimer interface. J. Biol. Chem. 287, 27997-28006
37. Peterson, F. C., Baden, E.M., Owen, B.A., Volkman, B. F., and Ramirez-Alvarado, M. (2010) A single mutation promotes amyloidogenicity through a highly promiscuous dimer interface. Structure 18, 563-570
38. Martin, D.J., and Ramirez-Alvarado, M. (2010) Comparison of amyloid fibril formation by two closely related immunoglobulin light chain variable domains. Amyloid 17, 129-136
39. Sreerama, N., Manning, M. C., Powers, M. E., Zhang, J.-X., Goldenberg, D. P., and Woody, R.W. (1999) Tyrosine, phenylalanine, and disulfide contributions to the circular dichroism of proteins: circular dichroism spectra of wild-type and mutant bovine pancreatic trypsin inhibitor. Biochemistry 38, 10814-10822
40. Albinsson, B., and Norden, B. (1992) Excited-state properties of the indole chromophore: electronic transition moment directions from linear dichroism measurements: effect of methyl and methoxy substituents. J. Phys. Chem. 96, 6204-6212
41. Hu, D., Qin, Z., Xue, B., Fink, A. L., and Uversky, V. N. (2008) Effect of methionine oxidation on the structural properties, conformational stability, and aggregation of immunoglobulin light chain LEN. Biochemistry 47, 8665-8677
42. Souillac, P. O., Uversky, V. N., Millett, I. S., Khurana, R., Doniach, S., and Fink, A. L. (2002) Effect of association state and conformational stability on the kinetics of immunoglobulin light chain amyloid fibril formation at physiological pH.J. Biol. Chem. 277, 12657-12665
43. Souillac, P. O., Uversky, V. N., and Fink, A. L. (2003) Structural transformations of oligomeric intermediates in the fibrillation of the immunoglobulin light chain LEN. Biochemistry 42, 8094-8104
44. Khurana, R., Gillespie, J.R., Talapatra, A., Minert, L. J., Ionescu-Zanetti, C., Millett, I., and Fink, A. L. (2001) Partially folded intermediates as critical precursors of light chain amyloid fibrils and amorphous aggregates. Biochemistry 40, 3525-3535
45. Souillac, P. O., Uversky, V. N., Millett, I. S., Khurana, R., Doniach, S., and Fink, A. L. (2002) Elucidation of the molecular mechanism during the early events in immunoglobulin light chain amyloid fibrillation: evidence for an off-pathway oligomer at acidic pH.J. Biol. Chem. 277, 12666-12679
46. Blancas-Mejia, L. M., Tellez, L.A., del Pozo-Yauner, L., Becerril, B., Sanchez-Ruiz, J.M., and Fernandez-Velasco, D.A. (2009) Thermodynamic and kinetic characterization of a germ line human 6 light-chain protein: the relation between unfolding and fibrillogenesis. J. Mol. Biol. 386, 1153-1166
47. Fauerbach, J.A., Yushchenko, D.A., Shahmoradian, S.H., Chiu, W., Jovin, T. M., and Jares-Erijman, E.A. (2012) Supramolecular non-amyloid intermediates in the early stages of α-synuclein aggregation. Biophys. J. 102, 1127-1136
48. Seyrek, E., and Dubin, P. (2010) Glycosaminoglycans as polyelectrolytes. Adv. Colloid Interface Sci. 158, 119-129
49. Guerrero-Muñoz, M.J., Castillo-Carranza, D.L., and Kayed, R. (2014) Therapeutic approaches against common structural features of toxic oligomers shared by multiple amyloidogenic proteins. Biochem. Pharmacol. 88, 468-478
50. Aguilera, J.J., Zhang, F., Beaudet, J.M., Linhardt, R.J., and Colón, W. (2014) Divergent effect of glycosaminoglycans on the in vitro aggregation of serum amyloid A. Biochimie 104, 70-80