Structures, organization, and function of reflectin proteins in dynamically tunable reflective cells

Journal of Biological Chemistry

Volumn 290, Issue 24, 2015, Pages 15238-15249

  DeMartini, Daniel G ^a   Izumi, Michi ^a   Weaver, Aaron T ^a   Pandolfi, Erica ^a   Morse, Daniel E ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MOLLUSCS; TISSUE;

CONSTRUCTIVE INTERFERENCE; DEPHOSPHORYLATIONS; SUB-CELLULAR; TISSUE SPECIFICITY; TISSUE SPECIFICS; TUNABILITIES;

PROTEINS;

ACETYLCHOLINE; CELL PROTEIN; REFLECTIN; UNCLASSIFIED DRUG; DNA; PRIMER DNA; PROTEIN;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL FUNCTION; CELLS BY BODY ANATOMY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; IRIDOCYTE; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DEPHOSPHORYLATION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; REFLECTIVE CELL; SKIN CELL; SQUID; TISSUE SPECIFICITY; ANIMAL; CHEMISTRY; CYTOLOGY; DECAPODIFORMES; IRIS; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHOSPHORYLATION; POLYMERASE CHAIN REACTION; PROTEIN CONFORMATION; SEQUENCE HOMOLOGY;

CEPHALOPODA;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; DECAPODIFORMES; DNA; DNA PRIMERS; IRIS; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; POLYMERASE CHAIN REACTION; PROTEIN CONFORMATION; PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84931281853     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.638254     Document Type: Article

References (42)

1. Land, M. F., and Fernald, R. D. (1992) The evolution of eyes. Annu. Rev. Neurosci. 15, 1-29
2. Arnold, J., and Young, R. (1974) Ultrastructure of squid photophore. I. Structure of the photogenic tissue. Biol. Bull. 147, 507-521
3. Ruby, E. G. (1996) Lessons from a cooperative, bacterial-animal association: the Vibrio fischeri-Euprymna scolopes light organ symbiosis. Annu. Rev. Microbiol. 50, 591-624
4. Mäthger, L. M., and Hanlon, R. T. (2007) Malleable skin coloration in cephalopods: selective reflectance, transmission and absorbance of light by chromatophores and iridophores. Cell Tissue Res. 329, 179-186
5. Hanlon, R. T., and Chiao, C. C., Mäthger, L. M., Barbosa, A., and Buresch, K. C., and Chubb, C. (2009) Cephalopod dynamic camouflage: bridging the continuum between background matching and disruptive coloration. Philos. Trans. R. Soc. Lond. B Biol. Sci. 364, 429-437
6. Boal, J., Shashar, N., Grable, M., Vaughan, K., Loew, E., and Hanlon, R. T. (2004) Behavioral evidence for intraspecific signaling with achromatic and polarized light by cuttlefish (Mollusca: Cephalopoda). Behaviour 141, 837-861
7. Hanlon, R. T., and Messenger, J. B. (1996) Cephalopod Behavior, pp. 31-45, 120-130, Cambridge University Press, Cambridge, UK
8. Denton, E. J., and Land, M. F. (1971) Mechanism of reflexion in silvery layers of fish and cephalopods. Proc. R Soc. Lond. B Biol. Sci. 178, 43-61
9. Brocco, S.L., and Cloney, R. A.(1980) Reflector cells inthe skin of Octopus dofleini. Cell Tissue Res. 205, 167-186
10. Crookes, W. J., Ding, L.-L., and Huang, Q. L., Kimbell, J. R., Horwitz, J., and McFall-Ngai, M. J. (2004) Reflectins: the unusual proteins of squid reflective tissues. Science 303, 235-238
11. Holt, A. L., and Sweeney, A. M., Johnsen, S., and Morse, D. E. (2011) A highly distributed Bragg stack with unique geometry provides effective camouflage for Loliginid squid eyes. J. R. Soc. Interface 8, 1386-1399
12. Cooper, K. M., and Hanlon, R. T., and Budelmann, B. U. (1990) Physiological color change in squid iridophores. II. Ultrastructural mechanisms in Lolliguncula brevis. Cell Tissue Res. 259, 15-24
13. Tao, A. R., and DeMartini, D. G., Izumi, M., Sweeney, A. M., and Holt, A. L., and Morse, D. E. (2010) The role of protein assembly in dynamically tunable bio-optical tissues. Biomaterials 31, 793-801
14. Izumi, M., and Sweeney, A. M., DeMartini, D. G., Weaver, J. C., and Powers, M. L., Tao, A., Silvas, T. V., Kramer, R. M., Crookes-Goodson, W. J., Mäthger, L. M., Naik, R. R., Hanlon, R. T., and Morse, D. E. (2010) Changes in reflectin protein phosphorylation are associated with dynamic iridescence in squid. J. R. Soc. Interface 7, 549-560
15. DeMartini, D. G., and Krogstad, D. V., and Morse, D. E. (2013) Membrane invaginations facilitate reversible water flux driving tunable iridescence in a dynamic biophotonic system. Proc. Natl. Acad. Sci. U.S.A. 110, 2552-2556
16. Cloney, R. A., and Brocco, S. L. (1983) Chromatophore organs, reflector cells, iridocytes and leucophores in cephalopods. Integr. Comp. Biol. 23, 581-592
17. Hanlon, R. T., and Cooper, K. M., Budelmann, B. U., and Pappas, T. C. (1990) Physiological color change in squid iridophores. I. Behavior, morphology and pharmacology in Lolliguncula brevis. Cell Tissue Res. 259, 3-14
18. Weiss, J. L., and Evans, N. A., Ahmed, T., Wrigley, J. D., Khan, S., Wright, C., Keen, J. N., Holzenburg, A., and Findlay, J. B. (2005) Methionine-rich repeat proteins: a family of membrane-associated proteins which contain unusual repeat regions. Biochim. Biophys. Acta 1668, 164-174
19. Rosenfeld, J., Capdevielle, J., Guillemot, J. C., and Ferrara, P. (1992) In-gel digestion of proteins for internal sequence analysis after one- or two-dimensional gel electrophoresis. Anal. Biochem. 203, 173-179
20. Hellman, U., Wernstedt, C., Góñez, J., and Heldin, C. H. (1995) Improvement of an "In-Gel" digestion procedure for the micropreparation of internal protein fragments for amino acid sequencing. Anal. Biochem. 224, 451-455
21. Bergersen, L. H., Storm-Mathisen, J., and Gundersen, V. (2008) Immunogold quantification of amino acids and proteins in complex subcellular compartments. Nat. Protoc. 3, 144-152
22. Claros, M.G., and von Heijne, G. (1994) TopPred II:animproved software for membrane protein structure predictions. Comput. Appl. Biosci. 10, 685-686
23. Wardill, T.J., Gonzalez-Bellido, P.T., Crook, R. J., and Hanlon, R.T. (2012) Neural control of tuneable skin iridescence in squid. Proc. Biol. Sci. 279, 4243-4252
24. Land, M. (1972) The physics and biology of animal reflectors. Prog. Biophys. Mol. Biol. 24, 75-106
25. Ghoshal, A., and DeMartini, D. G., Eck, E., and Morse, D. E. (2013) Optical parameters of the tunable Bragg reflectors in squid. J. R. Soc. Interface 10, 20130386
26. Barer, R., and Tkaczyk, S. (1954) Refractive index of concentrated protein solutions. Nature 173, 821-822
27. Zhao, H., and Brown, P. H., and Schuck, P. (2011) On the distribution of protein refractive index increments. Biophys. J. 100, 2309-2317
28. Horwitz, J. (2003) α-Crystallin. Exp. Eye Res. 76, 145-153
29. Ellis, R.J. (1979) The most abundant protein in the world. Trends Biochem. Sci. 4, 241-244
30. Mäthger, L. M., Senft, S. L., Gao, M., Karaveli, S., Bell, G. R. R., Zia, R., Kuzirian, A. M., Dennis, P. B., Crookes-Goodson, W.J., Naik, R. R., Kattawar, G. W., and Hanlon, R. T. (2013) Bright white scattering from protein spheres in color changing, flexible cuttlefish skin. Adv. Funct. Mater. 23, 3980-3989
31. DeMartini, D. G., Ghoshal, A., Pandolfi, E., Weaver, A. T., Baum, M., and Morse, D. E. (2013) Dynamic biophotonics: female squid exhibit sexually dimorphic tunable leucophores and iridocytes. J. Exp. Biol. 216, 3733-3741
32. Andouche, A., Bassaglia, Y., Baratte, S., and Bonnaud, L. (2013) Reflectin genes and development of iridophore patterns in Sepia officinalis embryos (Mollusca, Cephalopoda). Dev. Dyn. 242, 560-571.
33. Arnold, J. M. (1967) Organellogenesis of the cephalopod iridophore: cy-tomembranes in development. J. Ultrastruct. Res. 20, 410-421
34. Kramer, R. M., Crookes-Goodson, W. J., and Naik, R. R. (2007) The self-organizing properties of squid reflectin protein. Nat. Mater. 6, 533-538
35. Qin, G., and Dennis, P. B., Zhang, Y., Hu, X., Bressner, J. E., Sun, Z., Crookes-Goodson, W. J., Naik, R. R., Omenetto, F. G., and Kaplan, D. L. (2012) Recombinant reflectin-based optical materials. J. Polym. Sci. B Polym. Phys. 51, 254-264
36. Seago, A. E., Brady, P., Vigneron, J. P., and Schultz, T. D. (2009) Gold bugs and beyond: a review of iridescence and structural colour mechanisms in beetles (Coleoptera). J. R. Soc. Interface 6, S165-S184
37. Parker, A. R. (2000) 515 million years of structural colour. J. Opt. A Pure Appl. Opt. 2, 15-28
38. Mäthger, L. M., Land, M. F., and Siebeck, U. E., and Marshall, N. J. (2003) Rapid colour changes in multilayer reflecting stripes in the paradise whiptail, Pentapodus paradiseus. J. Exp. Biol. 206, 3607-3613
39. Vigneron, J. P., and Pasteels, J. M., Windsor, D. M., Vértesy, Z., Rassart, M., Seldrum, T., Dumont, J., Deparis, O., Lousse, V., Biró, L. P., Ertz, D., and Welch, V. (2007) Switchable reflector in the Panamanian tortoise beetle Charidotella egregia (Chrysomelidae: Cassidinae). Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 76, 031907
40. Walish, J., Kang, Y., Mickiewicz, R., and Thomas, E. (2009) Bioinspired electrochemically tunable block copolymer full color pixels. Adv. Mater. 21, 1-4
41. Fudouzi, H. (2011) Tunable structural color in organisms and photonic materials for design of bioinspired materials. Sci. Technol. Adv. Mater. 12, 064704
42. Engelman, D. M., and Steitz, T. A., and Goldman, A. (1986) Identifying non-polar transbilayer helices in amino acid sequences of membrane proteins. Annu. Rev. Biophys. Biophys. Chem. 15, 321-353