Tilt/Asymmetry in Nitrosyl Metalloporphyrin Complexes: The Cobalt Case

Full text of DOI:10.1021/ic971109j

382
Inorg. Chem. 1998, 37, 382-383
Tilt/Asymmetry in Nitrosyl Metalloporphyrin Complexes: The Cobalt Case
Mary K. Ellison and W. Robert Scheidt*
Department of Chemistry and Biochemistry, University of Notre Dame, Notre Dame, Indiana 46556
ReceiVed August 29, 1997
The nature of nitric oxide (NO) ligation in hemes has received
renewed interest because of the recognition of NO participation
in a wide variety of biological functions.1 We recently found, in
two crystalline polymorphs of the five-coordinate iron nitrosyl
derivative [Fe(OEP)(NO)],2,3 that the FeN5 coordination group
shows substantial deviation from expected axial symmetry. The
deviations are a significant off-axis tilt of the Fe-N(NO) bond
vector and an asymmetry in the equatorial Fe-Np bond distances.
Reasons for the off-axis tilt are not immediately obvious. The
equatorial asymmetry pattern is that the two Fe-Np bonds closest
to the tilted Fe-N(NO) axial vector are effectively identical but
significantly shorter than the other two Fe-Np bonds, which are
also effectively equal. Since one of these structure determinations
was carried out to extremely high resolution and a similar tilting/
asymmetry pattern is also present in the structure of a related
complex,4 the equatorial asymmetry appears to be the result of
subtle bonding effects correlated with the off-axis tilt. Moreover,
there are hints of similar deviations from axial symmetry in
previous structures of five-coordinate (porphinato)iron(II) ni-
trosyls. However, in these previous structure determinations,5
disorder has limited the accuracy of the result. These observations
strongly suggest that tilt/asymmetry in the coordination group is
a hitherto unrecognized, fundamental property in (porphinato)-
iron(II) nitrosyl systems.
Figure 1. ORTEP diagram of [Co(OEP)NO] (50% probability ellipsoids).
The labeling scheme is used in all diagrams and tables that are found in
the Supporting Information. The direction of the 2.2° Co-N(NO) vector
tilt from the normal to the porphyrin plane is between N(2) and N(3).
Individual values of the four Co-Np bonds are shown. The standard
uncertainty for each value is 0.0008 Å.
approach has been to investigate different metalloporphyrin
derivatives containing a bent nitrosyl group. Cobalt porphyrins
are one such class and are especially interesting since they contain
2
one additional electron in the critical dz -π*(NO) molecular
While the need for a better understanding of the interaction of
nitric oxide with metalloporphyrins is evident, there is also a
similar need with other diatomic ligand interactions in heme
proteins and iron porphyrins. A particular point of interest is
the apparent asymmetric binding of CO in the heme proteins that
is described as the “tilting” and/or “bending” of the CO group
with respect to the heme plane. This binding mode has been
regarded as the basis for the significant difference in CO affinity
between iron porphyrins and the O2-binding hemoproteins.
Although there remains significant controversy about just how
distorted the Fe-C-O linkage is,6 a variety of mechanisms for
explaining this distortion has been offered. The traditional
explanation offered has been steric effects in the ligand binding
pocket.7 Recent work emphasized the importance of electrostatic
interactions in the distal pocket,8 or the proximal histidine residue,9
or coupling of the FeCO tilting/bending mode10 in controlling
the distortion. Since the iron nitrosyl results3 offered evidence
that a structural distortion of a strongly bonding axial ligand can
be a stable one and the distortion supported only by bonding
effects, we have attempted to further characterize the effect. One
orbital. It is precisely this MO that must play an important role
if the axial distortion is the result of bonding effects.11 We report
in this communication the structure determination of [Co(OEP)-
(NO)], which has been carried out to high resolution.13
(6) The experimental results cited below have given a wide range of apparent
Fe-C-O angles: (a) Kuriyan, J.; Wilz, S.; Karplus, M.; Petsko, G. A.
J. Mol. Biol. 1986, 192, 133. (b) Teng, T.-Y.; Sˇrajer, V.; Moffat, K.
Nat. Struct. Biol. 1994, 1, 701. (c) Cheng, X.; Schoenborn, B. P. J. Mol.
Biol. 1991, 220, 381. (d) Moore, J. N.; Hansen, P. A.; Hochstrasser, R.
M. Proc. Natl. Acad. Sci. U.S.A. 1988, 85, 5062. (e) Ormos, P.;
Braunstein, D.; Frauenfelder, H.; Hong, M. K.; Lim, S.-L.; Sauke, T.
B.; Young, R. D. Proc. Natl. Acad. Sci. U.S.A. 1988, 85, 8492. (f) Lim,
M.; Jackson, T. A.; Anfinrud, P. A. Science 1995, 269, 962. (g) Ivanov,
D.; Sage, J. T.; Keim, M.; Powell, J. R.; Asher, S. A.; Champion, P. A.
J. Am. Chem. Soc. 1994, 116, 4139. (h) Quillan, M. L.; Arduini, R. M.;
Olson, J. S.; Phillips, G. N., Jr. J. Mol. Biol. 1993, 234, 140. (i)
Schlichting, I.; Berendzen, J.; Phillips, G. N., Jr.; Sweet, R. M. Nature
1994, 371, 808.
(7) Jameson, G. B.; Ibers, J. A. In Bioinorganic Chemistry; Bertini, I., Gray,
H. B., Lippard, S., Valentine, J. S., Eds.; University Science Books: Mill
Valley, CA, 1994; Chapter 4.
(8) (a) Balasubramanian, S.; Lambright, D. G.; Boxer S. G. Proc. Natl. Acad.
Sci. U.S.A. 1993, 90, 4718. (b) Braunstein, D. P.; Chu, K.; Egeberg, K.
D.; Frauenfelder, H.; Mourant, J. D.; Nienhaus, G. U.; Ormos, P.; Sligar,
S. G.; Springer, B. A.; Young, R. D. Biophys. J. 1993, 65, 2447. (c) Li,
T.; Quillin, M. L.; Phillips, G. N., Jr.; Olson, J. S. Biochemistry 1994,
33, 1433. (d) Springer, B. A.; Sligar, S. G.; Olson, J. S.; Phillips, G. N.,
Jr. Chem. ReV. 1994, 94, 699.
* To whom correspondence should be addressed: fax, (219) 631-4044;
e-mail, Scheidt.1@ND.edu.
(1) Stamler, J. S.; Singel, S. J.; Loscalzo, J. Science 1992, 258, 1898. Traylor,
T. G.; Sharma, V. J. Biochemistry 1992, 31, 2847.
(2) Abbreviations: Porph, a generalized porphyrin dianion; OEP, the dianion
of octaethylporphyrin; OETAP, the dianion of octaethyltetraazaporphyrin;
Np, porphyrinato nitrogen.
(3) Ellison, M. K.; Scheidt, W. R. J. Am. Chem. Soc. 1997, 119, 7404.
(4) Bohle, D. S.; Debrunner, P.; Fitzgerald, J.; Hansert, B.; Hung, C.-H.;
Thompson, A. J. J. Chem. Soc., Chem. Commun. 1997, 91.
(5) (a) Scheidt, W. R.; Frisse, M. E. J. Am. Chem. Soc. 1975, 97, 17. (b)
Bohle, D. S.; Hung, C.-H. J. Am. Chem. Soc. 1995, 117, 9584. Nasri,
H.; Haller, K. J.; Wang, Y.; Huynh, B. H.; Scheidt, W. R. Inorg. Chem.
1992, 31, 3459.
(9) Jewsbury, P.; Yamamoto, S.; Minato, T.; Saito, M.; Kitagawa, T. J. Phys.
Chem. 1995, 99, 12677.
(10) Ghosh, A.; Bocian, D. F. J. Phys. Chem. 1996, 100, 6363.
(11) Hoffmann et al.12 have predicted that bent nitrosyl ligands should display
an off-axis movement of the nitrosyl nitrogen atom leading to a tilt.
However, the direction predicted for the {MNO}8 complexes considered
is opposite to that observed in the iron system. To our knowledge, the
study of Hoffmann et al.12 is the only theoretical study to have addressed
this point and no one has dealt with the equatorial asymmetry seen for
the iron systems.
S0020-1669(97)01109-9 CCC: $15.00 © 1998 American Chemical Society
Published on Web 01/16/1998

Communications
Inorganic Chemistry, Vol. 37, No. 3, 1998 383
Table 1. Bonding Parameters for [M(Porph)NO] Complexes
b,f
M-Np
complex
M-N-Oa
∆Mb,c
M-N(NO)b
N-Ob
orientationa,d
tilta,e
short
long
ref
[Fe(OEP)NO] (P1h)
[Fe(OEP)NO] (P21/c)
[Fe(OETAP)NO] (P1h)
[Co(OEP)NO] (P1h)
142.74(8)
144.4(2)
143.7(4)
122.70(8)
0.27
0.29
0.31
0.16
1.7307(7)
1.722(2)
1.721(4)
1.8444(9)
1.1677(11)
1.167(3)
1.155(5)
40.2
37.9
39.6
45.0
8.2
6.5
7.6
2.2
1.999(1)
1.991(3)
1.924(2)
1.977(1)
2.020(4)
2.016(1)
1.940(2)
1.992(3)
3
3
4
1.1642(13)
this work
a Value in degrees. b Value in angstroms. c Metal atom displacement from 24-atom mean plane. d Dihedral angle of M-N-O and Np -M-
N(NO) planes. e Deviation from normal to porphyrin plane. f Estimated standard deviations calculated for two averaged values.
Crystalline [Co(OEP)(NO)]14 has a nitrosyl stretching frequency
at 1677 cm-1 (KBr pellet); the solution values are 1676 cm-1 in
CHCl3 and 1670 cm-1 in CH2Cl2. The crystal structure deter-
mination15 shows that the molecule is completely ordered, unlike
the previously reported systems.16,17 The derived results for the
determination have the high precision and low standard uncertain-
ties that are expected given the extensive, high-angle data
measured. Figure 1 displays an ORTEP drawing of the [Co-
(OEP)(NO)] molecule. The Co-Np bond distance average of
1.984(8) Å, the axial Co-N(NO) distance of 1.8444(9) Å, the
Co-N-O angle of 122.70(8)°, and the 0.16 Å displacement of
the cobalt atom from the mean plane are values that are consistent
with those found for previous cobalt nitrosyls.16,17 As shown in
Figure S1 (Supporting Information), a formal diagram of the
porphinato core in the [Co(OEP)(NO)] molecule, the core is
almost exactly planar. Also shown in Figure S1 are the averaged
bond distances and angles18 for the chemically unique classes in
the core. None of the averaged values warrant further comment.
A comparison of the structure of [Co(OEP)(NO)] with the five-
coordinate iron(II) analogues (Table 1) shows the major differ-
ences: the Co-N-O angle is ∼21° smaller, the displacement of
the cobalt atom from the porphinato plane is about half that of
the iron atom, and the axial Co-N(NO) distance is about 0.12 Å
larger. Figure S2 (Supporting Information) shows the arrange-
ment of the pairs of [Co(OEP)(NO)] molecules that form weak
dimers in the solid state.
Shown in Figure 1 is the orientation of the tilted nitric oxide
ligand with respect to the porphyrin axis system; the tilt of the
Co-N(NO) vector is between the pair of short Co-Np bonds,
i.e., N(2) and N(3). Importantly, the highly precise and ordered
structure of [Co(OEP)(NO)] permits a detailed comparison with
the unusual structural features of the two polymorphs of [Fe-
(OEP)(NO)]3 and that of [Fe(OETAP)(NO)].4 These features are
the interesting deviations from axial symmetry displayed by all
three iron species. Table 1 gives values for a number of
parameters in the four structures. Like the iron derivatives, [Co-
(OEP)(NO)] displays an off-axis tilt of the M-N(NO) bond vector
and the same pattern of asymmetric distortions in the equatorial
MN4 plane. However, the tilt value of 2.2° is substantially smaller
than the values observed in the iron species, where the tilt of the
Fe-N(NO) vector is 6.5 or 8.2°.19 Despite the smaller value of
the axial tilt, the same asymmetric pattern of equatorial M-Np
bond distances remains. Since crystals of [Co(OEP)(NO)] and
the second form of [Fe(OEP)(NO)] are isomorphous, the fact that
different tilt angles are seen in the two structures buttresses our
earlier conclusion that the tilt results from bonding effects rather
than crystal packing. Indeed, the closest nonbonded O‚‚‚H contact
is opposite to that expected given the direction of the tilt.20
These cobalt results further suggest that there is a correlation
between the value of the tilt and the equatorial distance asym-
metry. Clearly the effect is subtle and will require careful
theoretical calculations for complete understanding. That the
addition of an electron in the axial dz2-π*(NO) molecular orbital
plays an apparent, strong role in the tilt/asymmetry should provide
an important constraint for theoretical studies. A final issue is
the question of whether the tilt/asymmetry structural features now
seen for four nitrosyl complexes are a general phenomenon in
axially ligated metalloporphyrin species. If so, what types of axial
ligand or ligands are required? Conclusive results will almost
certainly require new structure determinations to provide the
needed high-quality diffraction data. Searches for such systems
are now underway.
(12) Hoffmann, R.; Chen, M. L.; Elian, M.; Rossi, A. R.; Mingos, D. M. P.
Inorg. Chem. 1974, 13, 2666.
(13) It is to be noted that nitrosylcobalt porphyrin derivatives have been used
to probe hemoprotein structure and function. See, for example: (a)
Yonetani, T.; Yamamoto, H.; Erman, J. E.; Leigh, J. S., Jr.; Reed, G. H.
J. Biol. Chem. 1972, 247, 2447. (b) Hori, H.; Ikeda-Saito, M.; Leigh, J.
S., Jr.; Yonetani, T. Biochemistry 1982, 21, 1431. (c) Yu, N.-Y.;
Thompson, H. M.; Mizyukami, H.; Gersonde, K. Eur. J. Biochem. 1986,
159, 129. (d) Dierks, E. A.; Hu, S.; Vogel, K. M.; Yu, A. E.; Spiro, T.
G.; Burstyn, J. N. J. Am. Chem. Soc. 1997, 119, 7316.
(14) [Co(OEP)NO] was prepared from 10 mg of Co(OEP) dissolved in dry
chloroform solution (∼5 mL) and several drops of pyridine in a narrow
Schlenk tube. Purified NO was then bubbled through the solution. Single
crystals were obtained by liquid diffusion using methanol (distilled over
Mg) as the nonsolvent. Earlier preparations of [Co(OEP)NO] have been
reported: Fujita, E.; Chang, C. K.; Fajer, J. J. Am. Chem. Soc. 1985,
107, 7665. Groombridge, C. J.; Larkworthy, L. F.; Mason, J. Inorg. Chem.
1993, 32, 379.
Acknowledgment. We thank the National Institutes of Health
for support under Grants GM-38401 and RR-06709.
(15) A dark purple, rectangular block crystal of [Co(OEP)NO] (0.40 × 0.30
× 0.10 mm3) was used for the structure determination. Data collection
was carried out on an Enraf-Nonius FAST area-detector diffractometer
with a Mo rotating-anode source (λh ) 0.710 73 Å) using our methods
for small-molecule X-ray data collection (Scheidt, W. R.; Turowska-
Tyrk, I. Inorg. Chem. 1994, 33, 1314). Data collections were performed
at 130(2) K. Complete crystallographic details are given in the Supporting
Information (Table S1). The structure was solved using SHELXS-86
(Sheldrick, G. M. Acta Crystallogr. 1990, A46, 467). The structure was
refined against F2 with the program SHELXL-93 (Sheldrick, G. M. J.
Appl. Crystallogr., in press). Hydrogen atoms were idealized with the
standard SHELXL-93 idealization methods. A modified (Karaulov, A.
I. School of Chemistry and Applied Chemistry, University of Wales,
College of Cardiff, Cardiff CF1 3TB, U.K. Personal communication)
version of the absorption correction program DIFABS (Walker, N. P.;
Stuart, D. Acta Crystallogr., Sect. A 1983, A39, 158) was applied.
(16) Scheidt, W. R.; Hoard, J. L. J. Am. Chem. Soc. 1973, 95, 8289.
(17) Richter-Addo, G. B.; Hodge, S. J.; Yi, G.-B.; Khan, M. A.; Ma, T.;
Caemelbecke, E. V.; Guo, N.; Kadish, K. M. Inorg. Chem. 1996, 35,
6530-6538; 1997, 36, 2696.
Supporting Information Available: Tables S1-S6, giving complete
crystallographic details, atomic coordinates, complete bond distances and
angles, anisotropic temperature factors, and fixed hydrogen atom positions,
and Figures S1-S3, presenting additional structural diagrams (14 pages).
The X-ray crystallographic file, in CIF format, is available. Ordering
and Internet access information is given on any current masthead page.
IC971109J
(18) The number in parentheses following each averaged value is the estimated
standard deviation calculated on the assumption that all averaged values
are drawn from the same population.
(19) The main component of uncertainty in the tilt angles is the uncertainty
in defining the mean plane of the porphyrin core. We estimate this at
∼0.5°.
(20) A detailed examination of crystal packing distances shows no significantly
short distances involving the nitrosyl ligand. An illustration showing the
immediate environment of the NO is given in the Supporting Information.