A comparison of DNA compaction by arginine and lysine peptides: A physical basis for arginine rich protamines

Biochemistry

Volumn 52, Issue 17, 2013, Pages 3000-3009

  Derouchey, Jason ^a   Hoover, Brandon ^b   Rau, Donald C ^b  

^a UNIVERSITY OF KENTUCKY   (United States)

^b EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE PEPTIDES; DNA CONDENSATION; EQUILIBRIUM SPACING; INTERHELICAL DISTANCE; OSMOTIC STRESS TECHNIQUES; OXIDIZING SPECIES; POSITIVELY CHARGED PEPTIDES; SHORT-RANGE REPULSION;

ARGININE; COMPACTION; PEPTIDES; POLYPEPTIDES;

DNA;

ARGININE; DNA; LYSINE; ORNITHINE; PROTAMINE;

ARTICLE; COMPARATIVE STUDY; DNA DAMAGE; OSMOTIC STRESS; PRIORITY JOURNAL; PROTEIN BINDING; RADIATION SCATTERING; SPERM;

ARGININE; DNA; LYSINE; NUCLEIC ACID CONFORMATION; PEPTIDES; PROTAMINES; SCATTERING, RADIATION;

EID: 84877011320     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi4001408     Document Type: Article

References (49)

1. Johnson, J. E. and Chiu, W. (2007) DNA packaging and delivery machines in tailed bacteriophages Curr. Opin. Struct. Biol. 17, 237-243
2. Nurmemmedov, E., Castelnovo, M., Catalano, C. E., and Evilevitch, A. (2007) Biophysics of viral infectivity: Matching genome length with capsid size Q. Rev. Biophys. 40, 327-356
3. Blanc, N. S., Senn, A., Leforestier, A., Livolant, F., and Dubochet, J. (2001) DNA in human and stallion spermatozoa forms local hexagonal packing with twist and many defects J. Struct. Biol. 134, 76-81
4. Hud, N. V., Allen, M. J., Downing, K. H., Lee, J., and Balhorn, R. (1993) Identification of the elemental packing unit of DNA in mammalian sperm cells by atomic force microscopy Biochem. Biophys. Res. Commun. 193, 1347-1354
5. Brewer, L. (2011) Deciphering the structure of DNA toroids Integr. Biol. 3, 540-547
6. DeRouchey, J. E. and Rau, D. C. (2011) Role of amino acid insertions on intermolecular forces between arginine peptide condensed DNA helices: Implications for protamine-DNA packaging in sperm J. Biol. Chem. 286, 41985-41992
7. Rau, D. C. and Parsegian, V. A. (1992) Direct measurement of the intermolecular forces between counterion-condensed DNA double helices: Evidence for long-range attractive hydration forces Biophys. J. 61, 246-259
8. Toma, A. C., de Frutos, M., Livolant, F., and Raspaud, E. (2009) DNA Condensed by Protamine: A "Short" or "Long" Polycation Behavior Biomacromolecules 10, 2129-2134
9. Braun, R. E. (2001) Packaging paternal chromosomes with protamine Nat. Genet. 28, 10-12
10. Carrell, D. T., Emery, B. R., and Hammoud, S. (2008) The aetiology of sperm protamine abnormalities and their potential impact on the sperm epigenome Int. J. Androl. 31, 537-545
11. Gonzalez-Marin, C., Gosalvez, J., and Roy, R. (2012) Types, causes, detection and repair of DNA fragmentation in animal and human sperm cells Int. J. Mol. Sci. 13, 14026-14052
12. Muratori, M., Marchiani, S., Maggi, M., Forti, G., and Baldi, E. (2006) Origin and biological significance of DNA fragmentation in human spermatozoa Front. Biosci. 11, 1491-1499
13. Miller, D., Brinkworth, M., and Iles, D. (2010) Paternal DNA packaging in spermatozoa: More than the sum of its parts? DNA, histones, protamines and epigenetics Reproduction 139, 287-301
14. Oliva, R. (2006) Protamines and male infertility Hum. Reprod. Update 12, 417-435
15. Aitken, R. J. and De Iuliis, G. N. (2010) On the possible origins of DNA damage in human spermatozoa Mol. Hum. Reprod. 16, 3-13
16. Bloomfield, V. A. (1997) DNA condensation by multivalent cations Biopolymers 44, 269-282
17. DeRouchey, J., Netz, R. R., and Radler, J. O. (2005) Structural investigations of DNA-polycation complexes Eur. Phys. J. E: Soft Matter Biol. Phys. 16, 17-28
18. DeRouchey, J., Parsegian, V. A., and Rau, D. C. (2010) Cation charge dependence of the forces driving DNA assembly Biophys. J. 99, 2608-2615
19. Pelta, J., Livolant, F., and Sikorav, J. L. (1996) DNA aggregation induced by polyamines and cobalthexammine J. Biol. Chem. 271, 5656-5662
20. Raspaud, E., de la Cruz, M. O., Sikorav, J. L., and Livolant, F. (1998) Precipitation of DNA by polyamines: A polyelectrolyte behavior Biophys. J. 74, 381-393
21. Raspaud, E., Durand, D., and Livolant, F. (2005) Interhelical spacing in liquid crystalline spermine and spermidine-DNA precipitates Biophys. J. 88, 392-403
22. Rau, D. C. and Parsegian, V. A. (1992) Direct measurement of temperature-dependent solvation forces between DNA double helices Biophys. J. 61, 260-271
23. Schellman, J. A. and Parthasarathy, N. (1984) X-ray diffraction studies in cation-collapsed DNA J. Mol. Biol. 175, 313-329
24. Todd, B. A., Parsegian, V. A., Shirahata, A., Thomas, T. J., and Rau, D. C. (2008) Attractive forces between cation condensed DNA double helices Biophys. J. 94, 4775-4782
25. DeRouchey, J. E. and Rau, D. C. (2011) Salt effects on condensed protamine-DNA assemblies: Anion binding and weakening of attraction J. Phys. Chem. B 115, 11888-11894
26. Yang, J. and Rau, D. C. (2005) Incomplete ion dissociation underlies the weakened attraction between DNA helices at high spermidine concentrations Biophys. J. 89, 1932-1940
27. Lewis, J. D., Song, Y., de Jong, M. E., Bagha, S. M., and Ausio, J. (2003) A walk though vertebrate and invertebrate protamines Chromosoma 111, 473-482
28. Queralt, R., Adroer, R., Oliva, R., Winkfein, R. J., Retief, J. D., and Dixon, G. H. (1995) Evolution of protamine P1 genes in mammals J. Mol. Evol. 40, 601-607
29. Leikin, S., Parsegian, V. A., Rau, D. C., and Rand, R. P. (1993) Hydration Forces Annu. Rev. Phys. Chem. 44, 369-395
30. Parsegian, V. A., Rand, R. P., Fuller, N. L., and Rau, D. C. (1986) Osmotic-Stress for the Direct Measurement of Intermolecular Forces Methods Enzymol. 127, 400-416
31. Stanley, C. and Rau, D. C. (2011) Evidence for water structuring forces between surfaces Curr. Opin. Colloids Interface Sci. 16, 551-556
32. Kornyshev, A. A., Lee, D. J., Leikin, S., and Wynveen, A. (2007) Structure and interactions of biological helices Rev. Mod. Phys. 79, 943-996
33. Hud, N. V., Milanovich, F. P., and Balhorn, R. (1994) Evidence of novel secondary structure in DNA-bound protamine is revealed by raman-spectroscopy Biochemistry 33, 7528-7535
34. McGhee, J. D., Wood, W. I., Dolan, M., Engel, J. D., and Felsenfeld, G. (1981) A 200 base pair region at the 5′ end of the chicken adult β-globin gene is accessible to nuclease digestion Cell 27, 45-55
35. Korolev, N., Berezhnoy, N. V., Eom, K. D., Tam, J. P., and Nordenskiold, L. (2009) A universal description for the experimental behavior of salt-(in)dependent oligocation-induced DNA condensation Nucleic Acids Res. 37, 7137-7150
36. Nayvelt, I., Thomas, T., and Thomas, T. J. (2007) Mechanistic differences in DNA nanoparticle formation in the presence of oligolysines and poly- l -lysine Biomacromolecules 8, 477-484
37. Suwalsky, M. and Traub, W. (1972) A comparative X-ray study of nucleoprotamine and DNA complexes with polylysine and polyarginine Biopolymers 11, 2223-2231
38. Balhorn, R. (2007) The protamine family of sperm nuclear proteins Genome Biol. 8, 227.1-227.8
39. Lewis, J. D., Saperas, N., Song, Y., Zamora, M. J., Chiva, M., and Ausio, J. (2004) Histone H1 and the origin of protamines Proc. Natl. Acad. Sci. U.S.A. 101, 4148-4152
40. Mascotti, D. P. and Lohman, T. M. (1993) Thermodynamics of single-stranded RNA and DNA interactions with oligolysines containing tryptophan. Effects of base composition Biochemistry 32, 10568-10579
41. Mascotti, D. P. and Lohman, T. M. (1997) Thermodynamics of oligoarginines binding to RNA and DNA Biochemistry 36, 7272-7279
42. Leng, M. and Felsenfeld, G. (1966) The preferential interactions of polylysine and polyarginine with specific base sequences in DNA Proc. Natl. Acad. Sci. U.S.A. 56, 1325-1332
43. Kawashima, S. and Ando, T. (1978) Interaction of basic oligo- l -amino acids with deoxyribonucleic acids. Oligo- l -arginines of various chain lengths and herring sperm DNA J. Biochem. 84, 343-350
44. Kawashima, S., Inoue, S., and Ando, T. (1969) Interaction of basic oligo- l -amino acids with deoxyribonucleic acid. Oligo- l -ornithines of various chain lengths and herring sperm DNA Biochim. Biophys. Acta 186, 145-157
45. Vijayanathan, V., Lyall, J., Thomas, T., Shirahata, A., and Thomas, T. J. (2005) Ionic, structural, and temperature effects on DNA nanoparticles formed by natural and synthetic polyamines Biomacromolecules 6, 1097-1103
46. Brewer, L., Corzett, M., Lau, E. Y., and Balhorn, R. (2003) Dynamics of protamine 1 binding to single DNA molecules J. Biol. Chem. 278, 42403-42408
47. Cherstvy, A. G., Kornyshev, A. A., and Leikin, S. (2004) Torsional deformation of double helix in interaction and aggregation of DNA J. Phys. Chem. B 108, 6508-6518
48. Kornyshev, A. A. and Leikin, S. (1998) Electrostatic interaction between helical macromolecules in dense aggregates: An impetus for DNA poly- and mesomorphism Proc. Natl. Acad. Sci. U.S.A. 95, 13579-13584
49. Kornyshev, A. A. and Leikin, S. (1999) Electrostatic zipper motif for DNA aggregation Phys. Rev. Lett. 82, 4138-4141