A magnetic protein biocompass

Nature Materials

Volumn 15, Issue 2, 2016, Pages 217-226

  Qin, Siying ^a   Yin, Hang ^a   Yang, Celi ^a   Dou, Yunfeng ^a   Liu, Zhongmin ^b   Zhang, Peng ^c   Yu, He ^a   Huang, Yulong ^d   Feng, Jing ^c   Hao, Junfeng ^c   Hao, Jia ^a   Deng, Lizong ^c   Yan, Xiyun ^c   Dong, Xiaoli ^d   Zhao, Zhongxian ^d   Jiang, Taijiao ^c   Wang, Hong Wei ^b   Luo, Shu Jin ^a   Xie, Can ^a  

^a PEKING UNIVERSITY   (China)

^b Tsinghua University   (China)

^c INSTITUTE OF BIOPHYSICS   (China)

^d INSTITUTE OF PHYSICS   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; BIOMAGNETISM; MAGNETIC FIELDS; PROTEINS;

BIOPHYSICAL METHODS; CRYPTOCHROMES; IRON BASED SYSTEM; MAGNETORECEPTION; MAGNETORECEPTOR; MULTIMERIC; PROTEIN COMPLEXES;

MAGNETISM;

ANTIBODY; BIOMATERIAL; IRON SULFUR PROTEIN; MESSENGER RNA;

ANIMAL; BIOPHYSICS; CHEMICAL STRUCTURE; COMPUTER SIMULATION; DROSOPHILA MELANOGASTER; ELECTRON MICROSCOPY; GENE EXPRESSION REGULATION; GENETICS; GENOME-WIDE ASSOCIATION STUDY; MAGNETISM; METABOLISM; MUTAGENESIS; PIGEONS AND DOVES; PROTEIN CONFORMATION; PROTEIN TRANSPORT; RETINA;

ANIMALS; ANTIBODIES; BIOCOMPATIBLE MATERIALS; BIOPHYSICS; COLUMBIDAE; COMPUTER SIMULATION; DROSOPHILA MELANOGASTER; GENE EXPRESSION REGULATION; GENOME-WIDE ASSOCIATION STUDY; IRON-SULFUR PROTEINS; MAGNETICS; MICROSCOPY, ELECTRON; MODELS, MOLECULAR; MUTAGENESIS; PROTEIN CONFORMATION; PROTEIN TRANSPORT; RETINA; RNA, MESSENGER;

EID: 84955490921     PISSN: 14761122     EISSN: 14764660     Source Type: Journal    
DOI: 10.1038/nmat4484     Document Type: Article

References (65)

1. Wiltschko, R. & Wiltschko, W. Magnetic Orientation in Animals (Springer, 1995).
2. Wiltschko, W. & Wiltschko, R. Magnetic orientation and magnetoreception in birds and other animals. J. Comp. Physiol. 191, 675-693 (2005).
3. Zhan, S., Merlin, C., Boore, J. L. & Reppert, S. M. The monarch butterfly genome yields insights into long-distance migration. Cell 147, 1171-1185 (2011).
4. Quinn, T. Evidence for celestial and magnetic compass orientation in lake migrating sockeye salmon fry. J. Comp. Physiol. 137, 243-248 (1980).
5. Cain, S. D., Boles, L. C., Wang, J. H. & Lohmann, K. J. Magnetic orientation and navigation in marine turtles, lobsters, and molluscs: Concepts and conundrums. Integr. Comp. Biol. 45, 539-546 (2005).
6. Boles, L. C. & Lohmann, K. J. True navigation and magnetic maps in spiny lobsters. Nature 421, 60-63 (2003).
7. Wang, Y., Pan, Y., Parsons, S., Walker, M. & Zhang, S. Bats respond to polarity of a magnetic field. Proc. Biol. Sci. 274, 2901-2905 (2007).
8. Nemec, P., Altmann, J., Marhold, S., Burda, H. & Oelschlager, H. H. Neuroanatomy of magnetoreception: The superior colliculus involved in magnetic orientation in a mammal. Science 294, 366-368 (2001).
9. Marhold, S., Wiltschko, W. & Burda, H. A magnetic polarity compass for direction finding in a subterranean mammal. Naturwissenschaften 84, 421-423 (1997).
10. O'Neill, P. Magnetoreception and baroreception in birds. Dev. Growth Differ. 55, 188-197 (2013).
11. Pavlova, G. A., Glantz, R. M. & Dennis Willows, A. O. Responses to magnetic stimuli recorded in peripheral nerves in the marine nudibranch mollusk Tritonia diomedea. J. Comp. Physiol. 197, 979-986 (2011).
12. Jacklyn, P. M. & Munro, U. Evidence for the use of magnetic cues in mound construction by the termite Amitermes meridionalis (Isoptera : Termitinae). Aust. J. Zool. 50, 357-368 (2002).
13. Westby, G.W. & Partridge, K. J. Human homing: Still no evidence despite geomagnetic controls. J. Exp. Biol. 120, 325-331 (1986).
14. Baker, R. R. Human Navigation and the Sixth Sense (Hodder and Stoughton, 1981).
15. Thoss, F., Bartsch, B., Fritzsche, B., Tellschaft, D. & Thoss, M. The magnetic field sensitivity of the human visual system shows resonance and compass characteristic. J. Comp. Physiol. 186, 1007-1010 (2000).
16. Johnsen, S. & Lohmann, K. J. Magnetoreception in animals. Phys. Today 61, 29-35 (March, 2008).
17. Schulten, K. & Weller, A. Exploring fast electron transfer processes by magnetic fields. Biophys. J. 24, 295-305 (1978).
18. Schulten, K. & Windemuth, A. in Biophysical effects of Steady Magnetic Fields (eds Maret, G., Kiepenheuen, J. & Boccara, N.) 99-106 (Springer, 1986).
19. Mohseni, M., Omar, Y., Engel, G. S. & Plenio, M. B. in Quantum effects in Biology (eds Solov'yov, I. S., Ritz, T., Schulten, K. & Hore, P. J.) Ch. 10, 218-236 (Cambridge Univ. Press, 2014).
20. Ritz, T., Adem, S. & Schulten, K. A model for photoreceptor-based magnetoreception in birds. Biophys. J. 78, 707-718 (2000).
21. Solov'yov, I. A. & Schulten, K. Magnetoreception through cryptochrome may involve superoxide. Biophys. J. 96, 4804-4813 (2009).
22. Solov'yov, I. A., Mouritsen, H. & Schulten, K. Acuity of a cryptochrome and vision-based magnetoreception system in birds. Biophys. J. 99, 40-49 (2010).
23. Cai, J. & Plenio, M. B. Chemical compass model for avian magnetoreception as a quantum coherent device. Phys. Rev. Lett. 111, 230503 (2013).
24. Rodgers, C. T. & Hore, P. J. Chemical magnetoreception in birds: The radical pair mechanism. Proc. Natl Acad. Sci. USA 106, 353-360 (2009).
25. Maeda, K. et al. Chemical compass model of avian magnetoreception. Nature 453, 387-390 (2008).
26. Moller, A., Sagasser, S., Wiltschko, W. & Schierwater, B. Retinal cryptochrome in a migratory passerine bird: A possible transducer for the avian magnetic compass. Naturwissenschaften 91, 585-588 (2004).
27. Mouritsen, H. & Ritz, T. Magnetoreception and its use in bird navigation. Curr. Opin. Neurobiol. 15, 406-414 (2005).
28. Ritz, T., Thalau, P., Phillips, J. B., Wiltschko, R. & Wiltschko, W. Resonance effects indicate a radical-pair mechanism for avian magnetic compass. Nature 429, 177-180 (2004).
29. Mouritsen, H. & Hore, P. J. The magnetic retina: Light-dependent and trigeminal magnetoreception in migratory birds. Curr. Opin. Neurobiol. 22, 343-352 (2012).
30. Gegear, R. J., Casselman, A., Waddell, S. & Reppert, S. M. Cryptochrome mediates light-dependent magnetosensitivity in Drosophila. Nature 454, 1014-1018 (2008).
31. Gegear, R. J., Foley, L. E., Casselman, A. & Reppert, S. M. Animal cryptochromes mediate magnetoreception by an unconventional photochemical mechanism. Nature 463, 804-807 (2010).
32. Fleissner, G. et al. Ultrastructural analysis of a putative magnetoreceptor in the beak of homing pigeons. J. Comp. Neurol. 458, 350-360 (2003).
33. Fleissner, G., Stahl, B., Thalau, P., Falkenberg, G. & Fleissner, G. A novel concept of Fe-mineral-based magnetoreception: Histological and physicochemical data from the upper beak of homing pigeons. Naturwissenschaften 94, 631-642 (2007).
34. Falkenberg, G. et al. Avian magnetoreception: Elaborate iron mineral containing dendrites in the upper beak seem to be a common feature of birds. PLoS ONE 5, e9231 (2010).
35. Hanzlik, M. et al. Superparamagnetic magnetite in the upper beak tissue of homing pigeons. Biometals 13, 325-331 (2000).
36. Kirschvink, J. L. & Gould, J. L. Biogenic magnetite as a basis for magnetic field detection in animals. Biosystems 13, 181-201 (1981).
37. Eder, S. H. et al. Magnetic characterization of isolated candidate vertebrate magnetoreceptor cells. Proc. Natl Acad. Sci. USA 109, 12022-12027 (2012).
38. Cadiou, H. & McNaughton, P. A. Avian magnetite-based magnetoreception: A physiologist's perspective. J. R. Soc. Interface 7, S193-205 (2010).
39. Mann, S., Sparks, N. H., Walker, M. M. & Kirschvink, J. L. Ultrastructure, morphology and organization of biogenic magnetite from sockeye salmon, Oncorhynchus nerka: Implications for magnetoreception. J. Exp. Biol. 140, 35-49 (1988).
40. Treiber, C. D. et al. Clusters of iron-rich cells in the upper beak of pigeons are macrophages not magnetosensitive neurons. Nature 484, 367-370 (2012).
41. Lohmann, K. J., Lohmann, C. M. & Putman, N. F. Magnetic maps in animals: Nature's GPS. J. Exp. Biol. 210, 3697-3705 (2007).
42. Yoshii, T., Todo, T., Wulbeck, C., Stanewsky, R. & Helfrich-Forster, C. Cryptochrome is present in the compound eyes and a subset of Drosophila's clock neurons. J. Comp. Neurol. 508, 952-966 (2008).
43. Ceriani, M. F. et al. Light-dependent sequestration of TIMELESS by CRYPTOCHROME. Science 285, 553-556 (1999).
44. Mandilaras, K. & Missirlis, F. Genes for iron metabolism influence circadian rhythms in Drosophila melanogaster. Metallomics 4, 928-936 (2012).
45. Chaves, I. et al. The cryptochromes: Blue light photoreceptors in plants and animals. Annu. Rev. Plant Biol. 62, 335-364 (2011).
46. Zhu, H. et al. Cryptochromes define a novel circadian clock mechanism in monarch butterflies that may underlie sun compass navigation. PLoS Biol. 6, e4 (2008).
47. Yoshii, T., Ahmad, M. & Helfrich-Forster, C. Cryptochrome mediates light-dependent magnetosensitivity of Drosophila's circadian clock. PLoS Biol. 7, e1000086 (2009).
48. Solov'yov, I. A. & Greiner, W. Micromagnetic insight into a magnetoreceptor in birds: Existence of magnetic field amplifiers in the beak. Phys. Rev. E 80, 041919 (2009).
49. Bilder, P.W., Ding, H. & Newcomer, M. E. Crystal structure of the ancient, Fe-S scaffold IscA reveals a novel protein fold. Biochemistry 43, 133-139 (2004).
50. Zoltowski, B. D. et al. Structure of full-length Drosophila cryptochrome. Nature 480, 396-399 (2011).
51. Watari, R. et al. Light-dependent structural change of chicken retinal Cryptochrome4. J. Biol. Chem. 287, 42634-42641 (2012).
52. Mouritsen, H. et al. Cryptochromes and neuronal-activity markers colocalize in the retina of migratory birds during magnetic orientation. Proc. Natl Acad. Sci. USA 101, 14294-14299 (2004).
53. Schrödinger, E.What Is Life? with Mind and Matter and Autobiographical Sketches (Cambridge Univ. Press, 1967).
54. Jia, C. J. et al. Large-scale synthesis of single-crystalline iron oxide magnetic nanorings. J. Am. Chem. Soc. 130, 16968-16977 (2008).
55. Cao, C. et al. Magnetic characterization of noninteracting, randomly oriented, nanometer-scale ferrimagnetic particles. J. Geophys. Res. 115, B07103 (2010).
56. Ashburner, M. et al. Gene ontology: Tool for the unification of biology. The Gene Ontology Consortium. Nature Genet. 25, 25-29 (2000).
57. Chintapalli, V. R., Wang, J. & Dow, J. A. Using Fly Atlas to identify better Drosophila melanogaster models of human disease. Nature Genet. 39, 715-720 (2007).
58. Schultz, J., Milpetz, F., Bork, P. & Ponting, C. P. SMART, a simple modular architecture research tool: Identification of signaling domains. Proc. Natl Acad. Sci. USA 95, 5857-5864 (1998).
59. Nishida, N. et al. Activation of leukocyte b2 integrins by conversion from bent to extended conformations. Immunity 25, 583-594 (2006).
60. Steven, J., Ludtke, P. R. B. & Chiu, W. EMAN: Semiautomated software for high-resolution single-particle reconstructions. J. Struct. Biol. 128, 82-97 (1999).
61. van Heel, M., Harauz, G., Orlova, E. V., Schmidt, R. & Schatz, M. A new generation of the IMAGIC image processing system. J. Struct. Biol. 116, 17-24 (1996).
62. Saxton, W. O. & Baumeister, W. The correlation averaging of a regularly arranged bacterial cell envelope protein. J. Microsc. 127, 127-138 (1982).
63. Kelley, L. A. & Sternberg, M. J. Protein structure prediction on the Web: A case study using the Phyre server. Nature Protoc. 4, 363-371 (2009).
64. Fan, K. et al. Magnetoferritin nanoparticles for targeting and visualizing tumour tissues. Nature Nanotech. 7, 459-464 (2012).
65. Galvez, N. et al. Comparative structural and chemical studies of ferritin cores with gradual removal of their iron contents. J. Am. Chem. Soc. 130, 8062-8068 (2008).