Tripodal tris-tacn and tris-dpa platforms for assembling phosphate-templated trimetallic centers

Article abstract of DOI:10.1021/ja108212v

Multidentate tripodal ligands, N(CH₂-m-C₆H ₄-CH₂tacn)₃ (L1) and N(CH₂-o-C ₆H₄-CH₂N(CH₂py)₂) ₃ (L2), have been devised for assembling high-nuclearity metal clusters. By using the same tripodal platform with different ligand appendages, either triazacyclononanes or dipicolylamines, and functionalizing either the ortho or the meta positions on the tris(xylyl) linker arms, discrete trimetal phosphate units of relevance to phosphate-metabolizing trimetallic centers in biology were prepared. Four such compounds, [(Cu^IICl) ₃(HPO₄)L1](PF₆) (1), [(Cu^IICl) ₃(HAsO₄)L1](PF₆) (2), Na₂[Mn ^III₆Mn^II₂(H₂O) ₂(HPO₄)₆(PO₄)₄(L1) ₂] (3), and [Co^II₃(H₂PO ₄)Cl₂(MeCN)L2](PF₆)₃ (4), all containing three metal centers bound to a central phosphate or arsenate unit bridging oxygen atoms, have been synthesized and structurally characterized. These results demonstrate the propensity of this novel tripodal ligand platform, in the presence of phosphate or arsenate, to assemble {M₃(EO ₄)} units and thus structurally mimic trimetallic active sites of proteins involved in phosphate metabolism. Reactivity studies reveal that the tricopper complex 1 is more efficient than monocopper analogues in catalyzing the hydrolysis of 4-nitrophenyl phosphate.

Full text of DOI:10.1021/ja108212v

Published on Web 11/22/2010
Tripodal Tris-tacn and Tris-dpa Platforms for Assembling
Phosphate-Templated Trimetallic Centers
Rui Cao, Peter Mu¨ller, and Stephen J. Lippard*
Department of Chemistry, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, United States
Received September 11, 2010; E-mail: lippard@mit.edu
Scheme 1
Abstract: Multidentate tripodal ligands, N(CH2-m-C6H4-CH2tacn)3
(L1) and N(CH2-o-C6H4-CH2N(CH2py)2)3 (L2), have been devised
for assembling high-nuclearity metal clusters. By using the same
tripodal platform with different ligand appendages, either triaza-
cyclononanes or dipicolylamines, and functionalizing either the ortho
or the meta positions on the tris(xylyl) linker arms, discrete trimetal
phosphate units of relevance to phosphate-metabolizing tri-
metallic centers in biology were prepared. Four such com-
pounds, [(CuIICl)3(HPO4)L1](PF6) (1), [(CuIICl)3(HAsO4)L1](PF6)
(2), Na2[MnIII6MnII2(H2O)2(HPO4)6(PO4)4(L1)2] (3), and [CoII3(H2PO4)-
Cl2(MeCN)L2](PF6)3 (4), all containing three metal centers bound
to a central phosphate or arsenate unit bridging oxygen atoms,
reveals an M3 site bridged by the {PO4} unit, with each metal
have been synthesized and structurally characterized. These
connected to one of the three O atoms of the phosphate and a
results demonstrate the propensity of this novel tripodal ligand
nucleophilic water molecule below the M3 plane.13
platform, in the presence of phosphate or arsenate, to assemble
Many artificial phosphates/nucleases have been developed for
{M3(EO4)} units and thus structurally mimic trimetallic active sites
applications in biotechnology and medicine, and multiple metal ions
of proteins involved in phosphate metabolism. Reactivity studies
in a single molecule can endow unique activity.25-30 Despite such
reveal that the tricopper complex 1 is more efficient than
achievements, however, no discrete structural model having a
monocopper analogues in catalyzing the hydrolysis of 4-nitro-
trimetallic center linked by a phosphate group within a single ligand
phenyl phosphate.
framework to mimic the protein {M3(PO4)} cores is available, to
our knowledge.7,13 We report here a tripodal platform in which
ligand arms at either the meta or ortho positions of a tris(xylyl)
Metalloproteins containing three metal ions at their active sites
perform a variety of important biological functions,1 including the
four-electron reduction of dioxygen to water by laccase and other
multicopper oxidases,2-5 the hydrolysis of phosphoric acid
monoesters,6,7 phospholipids,8,9 nucleotides,10,11 and inorganic
pyrophosphate12,13 by enzymes having a diverse array of divalent
metal ions, and the mediation of electron transfer by 3(4)Fe-4S-
containing proteins.14,15 Phosphoric acid derivatives, including
phosphates, also play a dominant role in biology,16 including
metabolic energy storage as adenosine triphosphate and energy
generation by metal phosphate (MHPO4) chelates.17-19 Phosphate
mono- and diesters are important structural components of lipids
and macromolecules of the genome, and protein function is widely
regulated by reversible phosphorylation of amino acid side chains.
Many enzymes required for phosphate metabolism contain a
trimetallic active site.1 Such trimetallic centers in P1 nuclease,10,11
alkaline phosphatases,6,20,21 phospholipase C,8,9 and inorganic
pyrophosphatases12,13 are responsible for cleavage of phosphate
P-O bonds; the trimetallic centers in PhoU proteins are involved
in inorganic phosphate uptake and regulation.22,23 In addition, some
proteins, like T5 flap endonuclease, have only two divalent metal
ions bound in the active site in the absence of phosphates but bind
a third metal ion in the presence of substrates,24 which implies a
weak association constant for the third metal and a templating effect
of phosphate substrates in the protein active site. The use of three
metal ions to hydrolyze phosphates is believed to anchor and orient
them in a position best suited for bond cleavage. As shown in
Scheme 1 (left), the X-ray structure of a family II pyrophosphatase
scaffold can each bind one metal ion with phosphate or arsenate to
self-assemble the desired core. The resulting structures have a
tetrahedral anion binding to each metal through one of three facial
oxygen atoms, similar to the coordination observed in protein active
sites (Scheme 1, right). Four such complexes with different metal
ions, ligand arms, and arm positions have been obtained, and all
were structurally characterized, indicating the versatility of this
tripodal platform. Moreover, reactivity studies reveal that the
hydrolysis of 4-nitrophenyl phosphate is accelerated by the tricopper
complex 1, which is catalytically more efficient than its monocopper
analogues.
In the course of developing multidentate ligands to coordinate
trimetallic clusters, we found that a tribenzylamine scaffold provides
the appropriate platform to draw three ligand arms together at the
requisite spacing to accommodate a trimetal phosphate core.
Crystallographic studies of a prototypical tripodal ligand backbone
of this kind, N(CH2-p-C6H4-CONH2)3 (Figure 1), the syntheses and
properties of which are supplied in the Supporting Information,
indicated that three symmetric ligand arms connected via para
positions produce a flattened structure lacking the preorganized
ligand environment suitable for assembling a trimetallic cluster.
However, the structure revealed that ligand arms at the meta or
ortho positions would produce the desired geometric configuration.
We therefore placed three 1,4,7-triazacyclononane (tacn) ligand
arms at the meta positions of the tribenzylamine platform, and this
effort gave the novel tris-tacn tripodal cluster-forming ligand,
N(CH2-m-C6H4-CH2tacn)3 (L1) (syntheses and details in the Sup-
porting Information). The choice of tacn ligand arms was based
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10.1021/ja108212v  2010 American Chemical Society

C O M M U N I C A T I O N S
The molecular structure of 1 demonstrates that the tacn-based
tripodal ligand N(CH2-m-C6H4-CH2tacn)3 (L1) can bind three metal
centers to afford the {(CuCl)3(HPO4)}+ core in the presence of
phosphate ion. Although, as shown in Figure 1, the ligand arms at
the meta positions of the tribenzylamine linker can have either an
upward or a downward orientation, the templating effect of the
phosphate group selects the former to afford the desired trimetallic
core. This conclusion is supported by studies of the ligand precursor
N(CH2-m-C6H4-CH2Br)3, in which the three bromomethyl arms
adopt a downward orientation in the solid state (Figure S2,
Supporting Information). Presumably, this geometric configuration
is thermodynamically more stable prior to introduction of the
phosphate anion to form 1.
The arsenic analogue of 1 was also synthesized and structurally
characterized. Replacement of HPO42- with HAsO42- in the reaction
of L1 and CuCl2, followed by addition of PF6 anion, gave small
Figure 1. Ball-and-stick representation of the X-ray structure of a tripodal
ligand model N(CH2-p-C6H4-CONH2)3. The C, O, N, and H atoms are
depicted in black, red, light blue, and light pink, respectively. The upward
and downward meta positions and downward ortho position are labeled.
-
crystalline cubes of [(CuIICl)3(HAsO4)L1](PF6) (2). The structure
matches that of the phosphate analogue (Figure S5, Supporting
Information), in which a {(CuCl)3(HAsO4)}+ core is coordinated
by L1 with each Cu(II) bound to three N atoms of a tacn-based
ligand arm. The monocationic cluster has C3 symmetry, and its
on the well-known facial coordination and high binding affinity of
this unit for most transition metals.31-33 Although ligands with
two, three, or four tacn moieties linked by a phenyl group have
been reported previously, in no case was a discrete trinuclear metal
complex formed having a central phosphate bridge.34-40
-
charge is balanced by a PF6 counterion. The As-O distances
(As1-O1 1.576(8) Å, As1-O2 1.623(17) Å) are longer than the
P-O distances (P1-O1 ) 1.516(2) Å, P1-O2 ) 1.585(5) Å), a
result consistent with the larger ionic radius of As(V) vs P(V).
2-
Reaction of L1 with CuCl2 in the presence of HPO4 under
ambient conditions gave a clear blue solution after filtration.
Addition of NH4(PF6) to this clear solution and subsequent
evaporation in air afforded crystalline prisms of [(CuIICl)3-
(HPO4)L1](PF6) (1). Complex 1 crystallizes in the trigonal space
Reaction of ligand L1 with the dinuclear manganese complex
[MnIII2(µ-O)(µ-OAc)2(bpy)2Cl2] in the presence of HPO4 gave
2-
Na2[MnIII6MnII (H2O)2(HPO4)6(PO4)4(L1)2] (3) as red crystalline
2
prisms. Crystallographic studies revealed a remarkable octaman-
ganese cluster flanked by two symmetry-equivalent L1 ligands and
overall Ci site symmetry (Figure 3). Alternatively, the structure of
3 can be described as a dimer of two symmetry-equivalent
j
group R3, with the monocationic cluster having a crystallographi-
cally required C3 axis passing through the tetrahedral phosphate
(O2 and P1) and nitrogen (N1) atoms (Figure 2). Each of the three
symmetric ligand arms of L1 coordinates one Cu(II) atom using
three N atoms of the tacn moiety, and the three Cu atoms are
bridged by the phosphate group with each Cu connected to one of
the three facial oxygen atoms. A terminal chloride ligand on each
Cu completes the coordination sphere and results in a distorted
square-pyramidal geometry with the tertiary nitrogen atom (N2) at
the apex (Cu1-N2, 2.256(3) Å). The fourth, uncoordinated oxygen
atom (O2) of the phosphate is protonated, as revealed by the longer
P1-O2 bond distance of 1.585(5) Å compared to P1-O1 )
1.516(2) Å. Monoprotonation of O2 is further confirmed by charge
trimetallic [MnIII3(HPO4)3(PO4)2L1]3- units, hereafter {Mn3L1}3-
,
connected by two additional Mn atoms. In each {Mn3L1}3- unit,
three manganese atoms are each coordinated by one tacn-based
ligand arm through its three nitrogen atoms and additionally linked
by a phosphate group (P1). The resulting {Mn3(PO4)}6+ core is
thus stabilized within the tripodal framework of ligand L1. The
ligand arms in 3 are directed in the upward orientation, thereby
resembling the geometric configuration observed in the structures
of 1 and 2.
-
In each {Mn3L1}3- unit, Mn1 has a terminal monodentate
phosphate group (P2) and an aqua ligand to complete a six-
coordinate, octahedral environment. The Mn2 and Mn3 atoms are
each linked to the Mn4 atom through a bidentate bridging phosphate
group (P4 and P3, respectively) and another such group (P5 and
P5, respectively) that also uses one of its coordinated oxygen atoms
to bridge to a third Mn atom. The Mn4 atom additionally binds to
a fourth oxygen atom supplied by the P1 phosphate. The binding
pattern of the resulting inorganic {Mn8(HPO4)6(PO4)4}2- core is
also depicted in Figure 3. A crystallographically imposed inversion
center is located at the midpoint of the Mn4-Mn4 vector.
balance, with one PF6 counterion per trimetallic cluster being
located both in the X-ray structure and by elemental analysis.
The three Mn atoms in the {Mn3L1}3- unit are all in the +3
oxidation state, as established by a bond valence sum (BVS)
analysis as well as the existence of a Jahn-Teller elongation axis,
typical of high-spin d4 Mn(III) ions. The central Mn4 atoms,
however, have a d5 Mn(II) electronic configuration (BVS ) 2.05),
Mn(II) probably forming by disproportionation of Mn(III). Careful
examination of the phosphate groups indicated the presence of six
HPO42- and four PO43- units. Taken together, these considerations
Figure 2. Thermal ellipsoid plot (50% probability) of the X-ray structure
of complex 1. The C3 axis passes through O2, P1, and N1 atoms. Hydrogen
atoms are omitted for clarity.
establish the formula as [MnIII6MnII (H2O)2(HPO4)6(PO4)4(L1)2]2-
,
2
with two Na+ counterions.
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C O M M U N I C A T I O N S
resulting trimetallic cluster [CoII (H2PO4)Cl2(MeCN)L2]3+ is charge-
3
-
balanced by three PF6 ions that were also located in the X-ray
structure.
The structures of 1-4 represent the first examples in which a
trimetal phosphate/arsenate unit is stabilized in a discrete ligand
environment. As such, they serve as structural mimics of trimetal
phosphate enzyme active sites.7,13 The occurrence of this unit in
diverse complexes illustrates the value of using the new trinucleating
ligands in conjunction with bridging tetrahedral anions like
phosphate or arsenate.
In order to examine the potential for such complexes to serve
as metallohydrolase catalysts, we studied the hydrolysis of
4-nitrophenyl phosphate in the presence of the tricopper(II)
complex 1. As deduced by a high-resolution ESI-MS measure-
ment (Figure S9, Supporting Information), the monocationic
cluster 1 stays intact upon dissolution. This hydrolytic reaction
produces inorganic phosphate and 4-nitrophenol, which can be
readily detected spectroscopically by its strong electronic
absorption at ∼400 nm).41,42 Kinetic studies revealed that the
hydrolysis of 4-nitrophenyl phosphate is accelerated by 1 (Figure
S10, Supporting Information). We also investigated this hydro-
lysis reaction using the mononuclear copper tacn complex
[Cu(tacn)Cl2], which structurally resembles a single ligand arm
of 1. The observed hydrolysis rate for 1 is 12 times greater than
that of [Cu(tacn)Cl2] at equimolar copper concentrations, which
suggests that the three copper atoms in close proximity may work
together with greater efficiency than mononuclear copper species
in catalyzing the hydrolysis of 4-nitrophenyl phosphate.
In conclusion, by using tripodal ligand N(CH2-m-C6H4-CH2tacn)3
(L1) or N(CH2-o-C6H4-CH2N(CH2py)2)3 (L2), trimetal phosphate or
arsenate units that mimic natural sites in phosphate-metabolizing
enzymes were accessed in discrete molecular systems. Four com-
pounds, all containing such a trimetallic core, were prepared and
structurally characterized: [(CuIICl)3(HPO4)L1](PF6) (1), [(CuIICl)3-
(HAsO4)L1](PF6) (2), Na2[MnIII6MnII (H2O)2(HPO4)6(PO4)4(L1)2] (3),
Figure 3. Thermal ellipsoid plot (30% probability) of the {Mn3L1}3-
omitting some atoms of the P2, P3, P4, and P5 phosphate groups,
,
2
and [CoII (H2PO4)Cl2(MeCN)L2](PF6)3 (4). In all four compounds,
3
subunit of complex
3 (top). Ball-and-stick representation of the
three metal ions are each bound by one arm of the tripodal ligand
through three N atoms and further linked by a tetrahedral phosphate,
protonated phosphate, or protonated arsenate group. The resulting
structures reprise features of the phosphate-bridged trimetallic active
sites in several proteins involved in phosphate metabolism.7,13 Complex
1 catalyzes the hydrolysis of 4-nitrophenyl phosphate with a greater
efficiency than its mononuclear Cu(II) tacn analogue, a result sug-
{Mn8(HPO4)6(PO4)4}2- core cluster of 3 (bottom). In the bottom part,
the ligand backbone of L1 is omitted. The Mn, P, O, and N atoms are
shown in purple, orange, red, and blue, respectively.
A related trinucleating ligand based on the same tribenzylamine
platform has been prepared. As noted from the structure of N(CH2-
p-C6H4-CONH2)3, ligand arms at the ortho positions can also give
rise to a preorganized environment capable of forming a trimetallic
center. We therefore prepared N(CH2-o-C6H4-CH2N(CH2py)2)3 (L2),
in which three dipicolylamine (dpa) ligand arms were appended to
ortho positions in the tribenzylamine platform. The synthesis and
details are available in the Supporting Information. Reaction of L2
-
and CoCl2 in the presence of H2PO4 gave a clear pink-purple
solution. Addition of NH4(PF6) to the reaction solution and vapor
diffusion using diethyl ether at room temperature afforded crystal-
line purple prisms of [CoII (H2PO4)Cl2(MeCN)L2](PF6)3 (4). In 4,
3
three Co(II) atoms, the oxidation states of which are supported by
a BVS calculation (Supporting Information), are each bound by
one L2 dpa ligand appendage through three N atoms and
-
linked by a central H2PO4 group (Figure 4). Co1 has a trigonal
bipyramidal coordination sphere with a terminal Cl ligand at the
apex trans to the tertiary nitrogen atom (N2). Co2 and Co3 are
further bridged by a Cl- ligand (Cl2). Co2 also has trigonal
bipyramidal stereochemistry, with Cl2 at the apex trans to the
tertiary nitrogen atom (N5), whereas Co3 is six-coordinate, with a
terminal MeCN ligand trans to the tertiary nitrogen atom (N8). The
Figure 4. Thermal ellipsoid plot (50% probability) of the X-ray structure
of 4.
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C O M M U N I C A T I O N S
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Acknowledgment. This work was supported by a grant from
the Camille and Henry Dreyfus Foundation. We thank Dr. William
H. Armstrong for helpful discussions. This paper is dedicated to
Prof. Dr. Karl Wieghardt on the occasion of his retirement.
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Supporting Information Available: Complete synthesis and char-
acterization of the tripodal model complex N(CH2-p-C6H4-CONH2)3,
tripodal ligands L1 and L2, and metal complexes 1-4; hydrolysis
studies of 4-nitrophenyl phosphate; Schemes S1-S3, Tables S1-S8,
and Figures S1-S10; X-ray data as CIF files for N(CH2-p-C6H4-
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CONH2)3, N(CH2-m-C6H4-CH2Br)3, N(CH2-o-C6H4-CH2OH)3, [MnIII
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