Journal of the American Chemical Society
Page 4 of 9
with proteins,43 the bdhꢀZnꢀT122Hferritin system repreꢀ
(10) Sakai, F.; Yang, G.; Weiss, M. S.; Liu, Y.; Chen, G.; Jiang, M.
Nat. Commun. 2014, 5, 4634.
(11) Brodin, J. D.; Ambroggio, X. I.; Tang, C.; Parent, K. N.; Baker,
T. S.; Tezcan, F. A. Nat. Chem. 2012, 4, 375.
(12) Furukawa, H.; Cordova, K. E.; O'Keeffe, M.; Yaghi, O. M. Sciꢀ
ence 2013, 341, 1230444.
(13) Jones, J. T. A.; Hasell, T.; Wu, X.; Bacsa, J.; Jelfs, K. E.;
Schmidtmann, M.; Chong, S. Y.; Adams, D. J.; Trewin, A.; Schiffꢀ
man, F.; Cora, F.; Slater, B.; Steiner, A.; Day, G. M.; Cooper, A. I.
Nature 2011, 474, 367.
(14) Farha, O. K.; Özgür Yazaydın, A.; Eryazici, I.; Malliakas, C. D.;
Hauser, B. G.; Kanatzidis, M. G.; Nguyen, S. T.; Snurr, R. Q.; Hupp,
J. T. Nat. Chem. 2010, 2, 944.
(15) Peplow, M. Nature 2015, 520, 148.
(16) Chui, S. S.ꢀY.; Lo, S. M.ꢀF.; Charmant, J. P. H.; Orpen, A. G.;
Williams, I. D. Science 1999, 283, 1148.
(17) Li, J. R.; Sculley, J.; Zhou, H. C. Chem. Rev. 2012, 112, 869.
(18) Liu, J.; Chen, L.; Cui, H.; Zhang, J.; Zhang, L.; Su, C. Y. Chem.
Soc. Rev. 2014, 43, 6011.
(19) Horike, S.; Shimomura, S.; Kitagawa, S. Nat. Chem. 2009, 1,
695.
(20)Yoon, M.; Srirambalaji, R.; Kim, K. Chem. Rev. 2011, 112, 1196.
(21) Sumida, K.; Rogow, D. L.; Mason, J. A.; McDonald, T. M.;
Bloch, E. D.; Herm, Z. R.; Bae, T. H.; Long, J. R. Chem. Rev. 2012,
112, 724.
(22) Horcajada, P.; Gref, R.; Baati, T.; Allan, P. K.; Maurin, G.; Couꢀ
vreur, P.; Ferey, G.; Morris, R. E.; Serre, C. Chem. Rev. 2012, 112,
1232.
(23) Wang, Z.; Cohen, S. M. Chem. Rev. 2009, 38, 1315.
(24) Eddaoudi, M.; Kim, J.; Rosi, N.; Vodak, D.; Wachter, J.;
O'Keeffe, M.; Yaghi, O. M. Science 2002, 295, 469.
(25) Ockwig, N. W.; DelgadoꢀFriedrichs, O.; O'Keeffe, M.; Yaghi, O.
M. Acc. Chem. Res. 2005, 38, 176.
(26) Toussaint, L.; Bertrand, L.; Hue, L.; Crichton, R. R.; Declercq, J.
P. J. Mol. Biol. 2007, 365, 440.
(27) Huard, D. J.; Kane, K. M.; Tezcan, F. A. Nat. Chem. Biol 2013,
9, 169.
1
2
3
4
5
6
7
8
sents the first example of a ternary proteinꢀmetalꢀorganic
crystalline framework where each component is an inteꢀ
gral part of the construction. The bcc arrangement preꢀ
sents a relatively high packing density for a spherical
building block (packing factor = 0.68), yet the ferritin
hubs themselves are hollow, thus producing a highly
porous framework with a solvent content of 67%. As a
result, bdhꢀZnꢀT122Hferritin crystals are highly permeable
to solutes, allowing the ferritin hubs to perform their
native enzymatic activity within the lattice, which is the
oxidation of soluble Fe2+ into crystalline Fe3+ꢀoxide
mineral (Figure S4). This in crystallo enzymatic activity
creates the future opportunity to template crystalline
inorganic materials in 3D with nanoscopic precision,
particularly if the stability of the frameworks can be imꢀ
proved. More generally, the bdhꢀZnꢀT122Hferritin crystals
introduce a new class of hybrid materials that combine
the chemical and structural versatility of metal ions, orꢀ
ganic linkers and protein building blocks in a modular
fashion.
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50
51
52
53
54
55
56
57
58
59
60
Supporting Information. Supporting Materials and Methꢀ
ods, Supporting Figures S1ꢀS4, and Supporting Table 1.
This material is available free of charge via the Internet at
Corresponding Author
Author Contributions
‡These authors contributed equally to the work.
(28) Li, H.; Eddaoudi, M.; O'Keeffe, M.; Yaghi, O. M. Nature 1999,
402, 276.
(29) Barthelet, K.; Marrot, J.; Riou, D.; Ferey, G. Angew. Chem. Int.
Ed. Engl. 2002, 41, 281.
(30) Santambrogio, P.; Pinto, P.; Levi, S.; Cozzi, A.; Rovida, E.; Alꢀ
bertini, A.; Artymiuk, P.; Harrison, P. M.; Arosio, P. Biochem. J.
1997, 322, 461.
(31) Lawson, D. M.; Artymiuk, P. J.; Yewdall, S. J.; Smith, J. M.;
Livingstone, J. C.; Treffry, A.; Luzzago, A.; Levi, S.; Arosio, P.;
Cesareni, G.; Thomas, C. D., Shaw, W. V.; Harrison, P. M. Nature
1991, 349, 541.
ACKNOWLEDGMENT
We thank C. Moore, A. Rheingold, M. Denny, H. Fei, D.
Puerta, and S. Cohen for helpful discussions. This work
was supported by the US Department of Energy (DOE)
(Division of Materials Sciences, Office of Basic Energy
Sciences, Award DEꢀFG02ꢀ10ER46677 to F.A.T.). Crystalꢀ
lographic data were collected at SSRL, supported by the
DOE, Offices of Basic Energy Sciences and Biological and
Environmental Research, as well as by the NIH. Coordinate
and structure factor files were deposited into the Protein
Data Bank under accession numbers 5CMQ and 5CMR.
(32) Liu, L.; Konstas, K.; Hill, M. R.; Telfer, S. G. J. Am. Chem. Soc.
2013, 135, 17731.
(33) Grams, F.; Reinemer, P.; Powers, J. C.; Kleine, T.; Pieper, M.;
Tschesche, H.; Huber, R.; Bode, W. Eur. J. Biochem. 1995, 228, 830.
(34) Puerta, D. T.; Cohen, S. M. Inorg. Chem. 2002, 41, 5075.
(35) Schulze Wischeler, J.; Innocenti, A.; Vullo, D.; Agrawal, A.;
Cohen, S. M.; Heine, A.; Supuran, C. T.; Klebe, G. ChemMedChem
2010, 5, 1609.
(36) Jani, M.; Tordai, H.; Trexler, M.; Banyai, L.; Patthy, L. Bioꢀ
chimie 2005, 87, 385.
(37)Radford, R. J.; Tezcan, F. A. J. Am. Chem. Soc. 2009, 131, 9136.
(38) Radford, R. J.; Nguyen, P. C.; Ditri, T. B.; Figueroa, J. S.;
Tezcan, F. A. Inorg. Chem. 2010, 49, 4362.
(39) Radford, R. J.; Nguyen, P. C.; Tezcan, F. A. Inorg. Chem. 2010,
49, 7106.
(40) Radford, R. J.; Lawrenz, M.; Nguyen, P. C.; McCammon, J. A.;
Tezcan, F. A. Chem. Commun. 2011, 47, 313.
(41) Burazerovic, S.; Gradinaru, J.; Pierron, J.; Ward, T. R. Angew.
Chem. Int. Ed. Engl. 2007, 119, 5606.
(42) Broomell, C. C.; Birkedal, H.; Oliveira, C. L. P.; Pedersen, J. S.;
Gertenbach, J.ꢀA.; Young, M.; Douglas, T. Soft matter 2010, 6, 3167.
(43) Jung, S.; Kim, Y.; Kim, S.ꢀJ.; Kwon, T.ꢀH.; Huh, S.; Park, S.
REFERENCES
(1) Moulton, B.; Zaworotko, M. J. Chem. Rev. 2001, 101, 1629.
(2) Desiraju, G. R. Angew. Chem. Int. Ed. Engl. 2007, 46, 8342.
(3) Hollingsworth, M. D. Science 2002, 295, 2410.
(4) Dandekar, P.; Kuvadia, Z. B.; Doherty, M. F. Annu. Rev. Mater.
Res. 2013, 43, 359.
(5) Margolin, A. L.; Navia, M. A. Angew. Chem. Int. Ed. Engl. 2001,
40, 2204.
(6) Ueno, T. Chem. Eur. J. 2013, 19, 9096.
(7) Cooper, D. R.; Boczek, T.; Grelewska, K.; Pinkowska, M.; Siꢀ
korska, M.; Zawadzki, M.; Derewenda, Z. Acta Crystallogr., Sect. D:
Biol. Crystallogr. 2007, 63, 636.
(8) Derewenda, Z. S. Acta Crystallogr., Sect. D: Biol. Crystallogr.
2010, 66, 604.
(9) Lanci, C. J.; MacDermaid, C. M.; Kang, S. G.; Acharya, R.;
North, B.; Yang, X.; Qiu, X. J.; DeGrado, W. F.; Saven, J. G. Proc.
Natl. Acad. Sci. U.S.A. 2012, 109, 7304.
Chem.
Commun.
2011,
47,
2904.
4
ACS Paragon Plus Environment