The Perl Toolchain Summit needs more sponsors. If your company depends on Perl, please support this very important event.
   [1]The Journal of Biological Chemistry

   [2]Skip to main page content
     * [3]Home
     * [4]Current issue
     * [5]Archive
     * [6]Papers in Press
     * [7]Minireviews
     * [8]Classics
     * [9]Reflections
     * [10]Papers of the Week

   QUICK SEARCHAuthor: _________Keyword: ________________Year: ____Vol:
   ____Page: ____ GO Go[11][Advanced Search][12][Browse the Archive]
     * Institution: Univ Colorado - Denison Memorial Library
     * [13]Sign In

   Advertisement
   Advertisement
     * [14]F1000 papers in the JBC

 ¤1¤ Crystal Structure of Allophycocyanin from Red AlgaePorphyra yezoensis at
2.2- Resolution[15]* ¤1¤

    1. [16]Jin-Yu Liu,
    2. [17]Tao Jiang,
    3. [18]Ji-Ping Zhang and
    4. [19]Dong-Cai Liang[20]à

    1.


    From the National Laboratory of Biomacromolecules, Institute of
    Biophysics, Chinese Academy of Sciences, Chaoyang District, Beijing
    100101, China


   [21]Next Section

 ¤2¤ Abstract ¤2¤

   The crystal structure of allophycocyanin from red algae Porphyra
   yezoensis (APC-PY) at 2.2- resolution has been determined by the
   molecular replacement method. The crystal belongs to space group R32
   with cell parameters a = b = 105.3 , c = 189.4 , α = β = 90¡, γ =
   120¡. After several cycles of refinement using program X-PLOR and model
   building based on the electron density map, the crystallographic
   R-factor converged to 19.3% (R-free factor is 26.9%) in the range of
   10.0 to 2.2 . The r.m.s. deviations of bond length and angles are
   0.015  and 2.9¡, respectively.

   In the crystal, two APC-PY trimers associate face to face into a
   hexamer. The assembly of two trimers within the hexamer is similar to
   that of C-phycocyanin (C-PC) and R-phycoerythrin (R-PE) hexamers, but
   the assembly tightness of the two trimers to the hexamer is not so high
   as that in C-PC and R-PE hexamers.

   The chromophore-protein interactions and possible pathway of energy
   transfer were discussed. Phycocyanobilin 1α84 of APC-PY forms 5
   hydrogen bonds with 3 residues in subunit 2β of another monomer. In
   R-PE and C-PC, chromophore 1α84 only forms 1 hydrogen bond with 2β77
   residue in subunit 2β. This result may support and explain great
   spectrum difference exists between APC trimer and monomer.

   Phycobilisomes are large supramolecular aggregates attached to the
   stromal side of the thylakoid membrane in cyanobacteria, red algae, and
   cryptomonads. These supramolecular aggregates are light-harvesting
   protein pigment complexes that are composed of phycobiliproteins and
   linker proteins. Based on the absorption of visible light, the
   phycobiliproteins can be divided into three main groups: phycoerythrin
   (PE)^1 or phycoerythrocyanin (PEC), phycocyanin (PC), and
   allophycocyanin (APC). With the help of linker proteins,
   phycobiliproteins form the two distinct structural domains of
   phycobilisome, the core and the rods. The core, which is composed of
   three or more core cylinders associated by APC discs, is in proximity
   of the reaction centers, whereas the rods are attached on the core and
   are composed of PC discs in the middle and PE or PEC discs on the tip.
   Light energy is transferred from PE or PEC via PC to APC and finally to
   the reaction centers ([22]1).

   The crystal structures of several phycobiliproteins have been solved;
   among them, three are PEs ([23]2-4), three are C-phycocyanins (C-PCs)
   ([24]5-7), one is PEC:PEC from Mastigocladus laminosus ([25]8), and one
   is APC:APC from Spirulina platensis ([26]9). All these structures are
   very similar. The basic building block is an αβ monomer composed of α
   and β subunits (R-phycoerythrin (R-PE) and B-phycoerythrin (B-PE) have
   a third subunit γ in the center of the molecule); three αβ monomers are
   arranged around a 3-fold symmetry axis to form an (αβ)[3] trimer or two
   (αβ)[3] trimers, which are assembled face to face into an (αβ)[6]
   hexamer.

   The crystal structure of APC is very special compared with other
   phycobiliproteins. First, the spectrum difference between APC trimer
   and its monomer is very large. When APC monomers aggregate to trimer,
   the absorption spectrum has a 40-nm red shift; the CD spectrum also
   changes a great deal, and exiton interaction in the trimer of APC was
   suggested ([27]10), whereas the spectrum difference between C-PC
   monomer and its trimer is not so large as in APC, although phycocyanin
   has the same α84PCB and β84PCB as APC.

   Second, the functional unit of APC was thought to be a trimer, whereas
   the function unit of other phycobiliproteins were hexamer (αβ)[6] or
   (αβ)[6]γ. Brejc and co-workers solved the structure of APC-SP from blue
   alga S. platensis([28]9) in the unit cell of APC-SP crystal; two
   trimers are associated in a Òback to backÓ manner that might represent
   the assembly state of APC in nature. Red alga is higher than blue alga
   in evolution, so it would be interesting to know the packing of APC
   from red alga in the unit cell and in nature.

   Third, in PE and PC, the two trimeric discs are superimposed along a
   3-fold axis, but in PC and APC the two discs are connected
   perpendicularly. The pathway of energy transfer between PC and APC is
   still unknown.

   The red algae Porphyra yezoensis is an algae that exists widely in
   nature. Its phycobilisomes contain R-PE, C-PC, and APC. In this paper
   we report the crystal structure of APC from P. yezoensis (APC-PY) at
   2.2- resolution. The organization of APC trimers in the core cylinders
   of phycobiliproteins and the pathway of energy transfer were discussed.
   [29]Previous Section[30]Next Section

 ¤2¤ EXPERIMENTAL PROCEDURES ¤2¤

   Crystallization and data collection of APC-PY was reported earlier
   ([31]11). The crystals of APC-PY belong to space group R32 with
   parameters a = b = 105.3 , c = 189.4 , α = β = 90¡, and γ = 120¡.

   Molecular replacement using program AMoRe ([32]12) was carried out
   using the 2.3- structure of APC-SP as a model. Model cell parameters
   were a = b = c = 150.0 , α = β = γ = 90¡, integrate radius was 30 ,
   and rotation function calculation gave a rather high coefficient
   solution, α = 60.07, β = 3.06, γ = 88.03, Cc = 20.0. The orientations
   and positions of one αβ in the asymmetric unit were determined by the
   translation function with a high correlation coefficient of 66.9%. The
   R-factor in the range from 10 to 4  was 36.1%. After rigid-body
   refinement, R-factor dropped to 33.1%, and the correlation coefficient
   increased to 71.2%. The packing of molecules in the unit cell was
   reasonable.

   The structure was refined using X-PLOR ([33]13). The consensus sequence
   was used for the initial model building. Fourier transform and electron
   density were first calculated in the resolution range of 10  to 3.5 .
   Residues that could not be fitted into the electron density map were
   omitted from the phase calculation in the next refinement cycle. After
   several cycles of rigid body, positional refinement, and manual model
   adjustment, the R-factor dropped to 25.4%, and a 2Fo-Fc Fourier map
   looked quite good. Then the resolution was extended to 2.2 . After the
   chromophores were fitted in the map and followed by several cycles of
   positional refinement and model adjustment, the electron density
   improved further. At this stage almost all side chains were well
   defined except those on the surface. Residue exchanges were carried out
   at this stage according to the omit map. After several cycles of
   positional refinement and model adjustment, the R-factor was converged
   to 24.0%, the individual B-factors were then refined, and the R-factor
   dropped to 21.5%. 169 water molecules were added to the model according
   to the Fo-Fc and 2Fo-Fc maps, and the final R-factor of the model was
   19.3% (R-free factor was 26.9%) in the range of 10  to 2.2 .
   [34]Previous Section[35]Next Section

 ¤2¤ RESULTS AND DISCUSSION ¤2¤

 ¤5¤ Amino Acid Sequence ¤5¤

   Because the amino acid sequence of APC from P. yezoensis is still
   unknown, the following six APC amino acid sequences were used to get a
   consensus sequence for model building. Among these sequences, four are
   from cyanobacteria,Anabaena cylindrica ([36]14), Calotrix PCC7601
   ([37]15),Fischerella PCC7603 ([38]16), and SynechococcusPCC6301
   ([39]17), and two are from red algae, Aglaothamnion neglectum ([40]18)
   and Cyanidium caldarium ([41]19). The alignment of these six sequences
   is shown in Table[42]I.
   View this table:
     * [43]In this window
     * [44]In a new window

   Table I

   The sequence alignment of the APCs

 ¤5¤ Quality of the Model ¤5¤

   The final crystallographic R-factor for APC-PY model is 19.3%, in the
   range of 10.0  to 2.2 . The Luzzati plot gives a mean positional
   error of 0.26  ([45]20). The r.m.s. deviations of bond lengths and
   bond angles are 0.015  and 2.9¡, respectively. The quality of the
   final model is summarized in Table[46]II. The Ramachandran plot shows
   that all dihedral angles fall into most favored or allowed regions with
   the only exception of β77Thr (Fig. [47]1) ([48]21), which has a
   conserved unusual dihedral angle in all known phycobiliprotein
   structures. In APC-PY, the N atom of β77Thr forms a hydrogen bond with
   OD (the oxygen atom in the ring D of chromophore) oxygen atom of
   α84PCB. The electron density of this residue is well defined in APC-PY.
   The consensus amino acid sequence (Table [49]I) was used to build the
   initial model and later modified according to the electron density map.
   In the 2.3--resolution crystal structure of APC-SP ([50]9), 28
   residues were not well defined with 102 atoms of zero occupancy; these
   residues are α25 Asp, α35Glu, α36Arg, α49Glu, α50Arg, α53Lys, α54 Gln,
   α76 Tyr, α79 Asp, α120Lys, α127Glu, β2 Gln, β10Asn, β17Lys, β20 Asp,
   β25 Gln, β35Glu, β36Leu, β39Arg, β50Asn, β58Lys, β65 Asp, β68Arg,
   β116Lys, β117Glu, β131 Gln, β138Glu, β150Lys. The fit of these residues
   to our electron density map is better in APC-PY; most of them behave
   well at 1ς density level (Fig. [51]2); others behave well at 0.7ς
   density level except α76 in the loop, which has a density at 0.5ς
   density level.
   View this table:
     * [52]In this window
     * [53]In a new window

   Table II

   Parameters of refined APC-PY model
   [54]Figure 1
   View larger version:
     * [55]In this window
     * [56]In a new window

     * [57]Download as PowerPoint Slide

   Figure 1

   Ramachandran plot of the APC-PY residues. Glycine residues are marked
   as squares. Nonglycine residues are marked as crosses. β77 (277) is in
   an unusual region. PSI and PHI are dihedral angles ψ and φ.
   [58]Figure 2
   View larger version:
     * [59]In this window
     * [60]In a new window

     * [61]Download as PowerPoint Slide

   Figure 2

   Omit electron density map of residues β35Glu and β36Leu in APC-PY .

   Comparing the crystallographic sequences of the final model of APC-PY
   and APC-SP, there are 37 nonidentical residues, 25 in the α subunit and
   12 in the β subunit (Table [62]III). In comparison with other APC
   sequences, the 37 residues of APC-PY are more conserved than those of
   APC-SP. For example, α52Val and α61Gln of APC-PY are identical to other
   known sequences. The electron density of these two residues in APC-PY
   are well defined.
   View this table:
     * [63]In this window
     * [64]In a new window

   Table III

   Sequence comparison of APC-PY and APC-SP

 ¤5¤ Molecular Structure ¤5¤

   The asymmetric unit of APC-PY contains α and β subunit. The α subunit
   is composed of 160 residues, and the β subunit contains 161 residues.
   Three αβ monomers are arranged around a 3-fold axis to form a disc
   shaped (αβ)[3] trimer of 30  in thickness and 110  in diameter with a
   cave in the center. The α and β subunits in the αβ monomer have similar
   structures, with nine α-helices (X, Y, A, B, E, F, FÕ, G, H) separated
   by irregular loops (Fig.[65]3).
   [66]Figure 3
   View larger version:
     * [67]In this window
     * [68]In a new window

     * [69]Download as PowerPoint Slide

   Figure 3

   Ribbon representation of APC α subunit (a), APC β subunit (b).

   The three-dimensional structure of APC-PY α and β subunits are very
   similar to the known structure of APC-SP. The intersubunit interactions
   within the (αβ) monomer and the (αβ)[3] trimer are also very similar to
   these of APC-SP and other phycobiliproteins. In the (αβ) monomer of
   APC-PY, the ionic- and polar-interacting residues between the two
   subunits are α3 Ser-β3 Asp, α13 Asp-β94 Tyr, α13 Asp-β110Arg,
   α17Arg-β97 Tyr, α18 Tyr-β93Arg, β13 Asp-α93Arg, β13 Asp-α97 Tyr, β18
   Tyr-α89 Asp.

   In the APC-PY crystal, two trimers associate face to face into the
   (αβ)[6] hexamer through a crystallographic dyad perpendicular to the
   triad. There are three (αβ)[6]hexamers in a unit cell, locating at
   (0,0,0), (2/3, 1/3, 1/3), and (1/3, 2/3, 2/3) (Fig. [70]4 a). The
   assembly of two trimers in this hexamer is completely different from
   that of APC-SP. In APC-SP crystal, the two trimers are associated
   loosely through β subunits in a Òback to backÓ manner (Fig. [71]4 b) in
   the hexamer ([72]9), but in APC-PY crystal, the two trimers in the
   hexamer contact through α subunits, and the assembly of the two trimers
   is much tighter than that in APC-SP.
   [73]Figure 4
   View larger version:
     * [74]In this window
     * [75]In a new window

     * [76]Download as PowerPoint Slide

   Figure 4

   a, packing of APC-PY in the unit cell.b, packing of APC-SP in the unit
   cell.

   The assembly of the hexamer in the APC-PY crystal is similar to that of
   C-PC from Fremylla diplosiphon (C-PC-FR) and R-PE fromPolysiphonia
   urceolata (R-PE-PU) hexamers; two (αβ)[3] trimers associate face to
   face in the hexamer. The α subunits provide the contacting surface, and
   the two trimers fit complementarily in the hexamer.

   Despite the similarity in assembly in APC-PY, C-PC-FR, and R-PE-PU
   hexamers, the superposition of the C[α] atoms of APC-PY and C-PC-FR
   hexamers shows that the assembly of the two trimers in APC-PY hexamer
   is obviously looser than that in C-PC-FR and R-PE-PU hexamers. The
   calculated accessible areas between the trimers in C-PC-FR and R-PE-PU
   hexamers are about 5900 and 6900 ^2. In APC-PY hexamer, this value is
   about 3200 ^2, which is much bigger than that in APC-SP (600 ^2);
   thus, the APC-PY hexamer can be described as a Òloose hexamer.Ó The
   interactions between the trimers in APC-PY hexamer are different from
   those in C-PC-FR and R-PE-PU hexamers.

   First, the number of the residues involved in the interactions between
   the two trimers in APC-PY hexamer is smaller than that in C-PC-FR and
   R-PE-PU hexamers, indicating a weaker association. This is consistent
   with the calculated accessible areas between the two trimers in
   C-PC-FR, R-PE-PU, and APC-PY hexamers. The special polar network
   present in C-PC of Agmenellum quadruplaticum (C-PC-AQ), formed by
   residues 1β46 Asn-6α164 Asn-1α21 Asn-6α161 Glu-6α33 Glu-6α30 Arg
   ([77]6) is not conserved in APC-PY hexamer. In addition, the
   electrostatic interactions between 1α2Lys-6α23Glu, 1α17Arg-6α108 Asp,
   and 1α120Arg-4α174 C-terminal carboxyl group, which were suggested to
   be involved in the hexamer formation in C-PC-FR ([78]22), are also not
   present in APC-PY hexamer. Furthermore, the comparison of APC-PY with
   C-PC-FR and R-PE-PU reveals that all the conserved polar and ionic
   interactions between the two trimers in C-PC-FR and R-PE-PU hexamers
   are not present in APC-PY hexamer.

   Despite the above difference, the interactions that maintain APC-PY as
   a loose hexamer seem still to be the polar and charged interactions
   between the two trimers. In APC-PY hexamer, the polar and charged
   interactions are 1α25 Asp-6α37Arg, 1α22 Gly-6α26Arg, 1α25 Asp-6α161Glu,
   1α25 Asp-6α165 Tyr, and 1α28Lys-6α147 Asp. In APC-SP, only a few polar
   and charged interactions (<4 ) exist between the two trimers, such as
   1&#x3b2;65 Asp-6&#x3b2;131 Gln and 1&#x3b2;120AsnÐ6&#x3b2;120Asn, indicating a very loose
   packing.

   Second, in C-PC-FR and R-PE-PU hexamers, the trimer-trimer association
   is mediated almost exclusively by polar and charged residues ([79]6),
   but in the APC-PY hexamer, some hydrophobic residues are also involved,
   such as &#x3b1;21 Pro, &#x3b1;22 Gly, &#x3b1;104 Val, &#x3b1;164 Phe, &#x3b2;42 Ala, and &#x3b2;46 Ala.

 ¤5¤ Chromophores &#x3b1;84PCB and &#x3b2;84PCB ¤5¤

   In APC, two phycocyanobilins are covalently bound to cysteine residues
   at position &#x3b1;84 and &#x3b2;84 (Fig. [80]5). Both chromophores are well
   defined in APC-PY (Fig.[81]6). The geometry and protein environment of
   these two chromophores resemble those of APC-SP. The &#x3b1;84 PCB
   chromophores have a protein environment similar to that of &#x3b2;84PCB. The
   polar and ionic protein-chromophore interactions in &#x3b1;84PCB and &#x3b2;84PCB
   are shown in Table [82]IV.
   [83]Figure 5
   View larger version:
     * [84]In this window
     * [85]In a new window

     * [86]Download as PowerPoint Slide

   Figure 5

   Chemical structure of PCB .
   [87]Figure 6
   View larger version:
     * [88]In this window
     * [89]In a new window

     * [90]Download as PowerPoint Slide

   Figure 6

   The coincidence of chromophores in APC-PY with 2Fo-Fc electron density
   map &#x3b1;84PCB (a), &#x3b2;84PCB (b).
   View this table:
     * [91]In this window
     * [92]In a new window

   Table IV

   The polar and ionic protein-chromophore interactions in APC-PY ()

   Chromophores &#x3b1;84PCB and &#x3b2;84PCB have similar hydrophobic environment;
   there are three aromatic residues close to &#x3b1;84, such as &#x3b1;90 Tyr, &#x3b1;91
   Tyr, and &#x3b1;119 Tyr, and three close to &#x3b2;84, such as &#x3b2;90 Tyr, &#x3b2;91 Tyr,
   and &#x3b2;119 Tyr. In C-PC-FR, &#x3b1;90 and &#x3b1;91 are all Tyr, and &#x3b2;90 and &#x3b2;91 are
   all Ile. In R-PE-PU, &#x3b1;90 and &#x3b1;91 are His and Tyr, respectively, and &#x3b2;90
   and &#x3b2;91 are all Ile. But in all known APCs, &#x3b1;90, &#x3b1;91, &#x3b2;90, and &#x3b2;91 are
   all Tyr. So the microenvironment of &#x3b1;84 and &#x3b2;84 in APC-PY is similar to
   that in C-PC-FR and R-PE-PU, indicating that &#x3b1;84PCB and &#x3b2;84PCB have
   similar conformation and spectrum character. &#x3b2;90 Tyr and &#x3b2;91 Tyr
   stabilize the &#x3b2;84PCB ring D conformation, which may make PCB have
   different spectrum characteristics in APC and C-PC.

 ¤5¤ Energy Transfer ¤5¤

   There are 12 PCBs in APC-PY hexamer; the arrangement of these
   chromophores is shown in Fig.[93]7. The theory of shot-distance exiton
   interaction ([94]23) and long distance dipole-dipole resonance
   mechanism ([95]24) has been used to explain the energy transfer rate
   between chromophores.
   [96]Figure 7
   View larger version:
     * [97]In this window
     * [98]In a new window

     * [99]Download as PowerPoint Slide

   Figure 7

   The chromophores of APC-PY hexamer.

   Inside trimer of APC-PY, the distance between 1&#x3b2;84PCB and 2&#x3b2;84PCB in
   APC-PY is about 34  and that between 1&#x3b1;84PCB and 2&#x3b2;84PCB is about 21
   . These values are similar to those in C-PCs. The chromophores are too
   far away to have exiton interaction. It is also difficult to explain
   why exiton interaction exists in APC but not in C-PC. Our study of
   chromophore-protein interactions and comparison of microenvironments in
   R-PE-PU, C-PC-FR, and APC-PY show that almost all the
   chromophore-protein interactions exist within the same monomer (&#x3b1;&#x3b2;),
   the only exception being &#x3b1;84PEB in R-PE-PU, which forms a hydrogen bond
   with &#x3b2;77 Thr in another monomer. In C-PC-FR, the situation is the same
   as in R-PE-PU. However, it is different in APC-PY; its &#x3b1;84PCB forms
   five hydrogen bonds with the residues in other monomer, such as &#x3b1;84PCB
   O2B-2&#x3b2;62 Tyr OH, O1C-2&#x3b2;62 Tyr N, O1C-2&#x3b2;67 Thr OG1, O2C-2&#x3b2;67 Thr OG1,
   and OD-2&#x3b2;77 Thr N (see Table[100]IV). We believe this difference may
   explain why the spectrum of APC changes greatly when its monomers
   associate to trimer. In APC-SP, distances of &#x3b1;84PCB O2B-2&#x3b2;62 Tyr OH,
   O1C-2&#x3b2;62 Tyr N, O1C-2&#x3b2;67 Thr OG1, O2C-2&#x3b2;67 Thr OG1, and OD-2&#x3b2;77 Thr N
   are all within the distance of hydrogen bond formation. As we know, &#x3b2;62
   Tyr and &#x3b2;67 Thr are close to chromophore &#x3b2;84PCB and may control the
   conformation of chromophore and bridge between &#x3b1;84 PCB and &#x3b2;84 PCB to
   make the exiton interaction occur.

   The distances of chromophores between the two trimers in APC-PY hexamer
   are similar to those in C-PC-FR and R-PE-PU hexamers. Based on the
   1.9- resolution crystal structure, the possible pathway of energy
   transfer within and between the two trimers of R-PE-PU were discussed
   ([101]25). There are three pairs of short distance interactions between
   two trimers, such as 1&#x3b1;84 &#x2192; 4&#x3b1;84,1&#x3b1;140a &#x2192;6&#x3b2;155, and 1&#x3b2;155 &#x2192; 6&#x3b2;155.
   &#x3b1;84PEB is on the inner surface of R-PE-PU, and 1&#x3b1;84PEB &#x2192; 4&#x3b1;84PEB may be
   the dominant energy transfer pathway between the two trimers. Similar
   energy pathways (1&#x3b1;84PCB &#x2192; 4&#x3b1;84PCB) also exists in C-PC-FR hexamers
   ([102]26). In C-PC-FR, R-PE-PU, and APC-PY hexamers, the distances
   between 1&#x3b1;84 (C10 atom) and 4&#x3b1;84 (C10 atom) are 27.5, 28.7, and 30.3 ,
   respectively, which are comparable. Therefore, the distance between the
   two chromophores of APC-PY seems adequate for effective energy
   transfer.

   In addition to the energy pathway composed of chromophores, the
   aromatic pathway formed by aromatic residues may play an important role
   in energy transfer. The energy transfer from chromophores to aromatic
   residues vice versa can be explained by exiton interaction mechanism,
   because the distances between some chromophores and aromatic residues,
   such as &#x3b1;84PCB-&#x3b1;90 Tyr, &#x3b1;84PCB-&#x3b1;91 Tyr, &#x3b2;84PCB-&#x3b2;90 Tyr, &#x3b2;84PCB-&#x3b2;91 Tyr
   are very short (&#x223c;4 ). FšrsterÕs dipole-dipole resonance transfer can
   occur between different aromatic residues rather than between
   chromophores and aromatic residues, because the overlap integral
   between chromophore absorption (&#x3bb;[max] &#x2245; 650 nm for fluorescence
   spectrum) and aromatic residue emission (&#x3bb;[max] &#x2245; 300 nm for
   fluorescence spectrum and &#x3bb;[max] &#x2245; 400 nm for phosphorescence spectrum)
   is quite small. In APC-PY there are two areas abundant in aromatic
   residues as shown in Fig.[103]8. One is close to chromophore &#x3b1;84PCB and
   composed of &#x3b1;164 Phe, &#x3b1;165 Tyr, &#x3b1;166 Phe, &#x3b1;168 Tyr, &#x3b1;90 Tyr, &#x3b1;91 Tyr,
   &#x3b1;97 Tyr, &#x3b1;119 Tyr, and &#x3b2;18 Tyr. Another is close to chromophore &#x3b2;84 and
   composed of &#x3b2;165 Tyr, &#x3b2;166 Phe, &#x3b2;168 Tyr, &#x3b2;90 Tyr, &#x3b2;91 Tyr, &#x3b2;94 Tyr,
   &#x3b2;97 Tyr, &#x3b2;119 Tyr, and &#x3b1;18 Tyr. &#x3b1;164 Phe is involved in the hydrophobic
   interactions between the two trimers. The aromatic residues in the &#x3b1;
   subunit and the &#x3b2; subunit have high homology and similar locations.
   Other aromatic residues are on the periphery of the disc, such as &#x3b1;76
   Tyr, &#x3b1;60 Phe, &#x3b2;76 Tyr, &#x3b2;62 Tyr, &#x3b2;30 Tyr, &#x3b2;31 Phe, &#x3b1;30 Phe, and &#x3b2;81 Tyr;
   among them &#x3b1;76 Tyr and &#x3b2;62 Tyr may mediate the energy transfer between
   1&#x3b1;84PCB and 2&#x3b2;84PCB. Because PC and APC are connected perpendicularly
   in vivo, aromatic residues on the periphery may mediate the energy
   transfer from the chromophores of PC to those of APC.
   [104]Figure 8
   View larger version:
     * [105]In this window
     * [106]In a new window

     * [107]Download as PowerPoint Slide

   Figure 8

   The location of aromatic residues in APC-PY .

 ¤5¤ Functional Unit ¤5¤

   In the core cylinders of phycobilisomes, several APC trimers are close
   together, but the association manner of these APC trimers is still
   unknown. Based on dissociation experiments, it was suggested that
   allophycocyanin does not form hexamers ([108]27), because almost all
   the residues involved in the trimer-trimer aggregation in C-PC-AQ and
   C-PC-FR hexamers are not conserved in APC. Similar conclusions were
   reported later ([109]6, [110]9). In the APC-PY hexamer, all the
   interactions involved in the formation of C-PC-AQ and C-PC-FR hexamers
   and all the conserved polar and charged interactions in C-PC-FR and
   R-PE-PU hexamers are not present, but APC-PY can still associate face
   to face to form a hexamer, which is maintained by some polar and
   charged interactions, different from those in C-PC-FR and R-PE-PU.
   Because the distances of chromophores between the two trimers in this
   hexamer are also adequate for effective energy transfer, we assume that
   the loose hexamer may represent the basic unit of APC in physiological
   conditions. It is possible that linker proteins may help to stabilize
   the loose hexamers.
   [111]Previous Section[112]Next Section

 ¤2¤ ACKNOWLEDGEMENT ¤2¤

   We thank Professor Lu-Lu Gui, Institute of Biophysics, Chinese Academy
   of Sciences and Professor You-Shang Zhang, Institute of Biochemistry,
   Chinese Academy of Sciences for their support and concern.
   [113]Previous Section[114]Next Section

 ¤2¤ Footnotes ¤2¤

     * [115]&#x21b5;* This work was supported by Chinese Academy of Sciences
       (KJ85-04-40) and the National Natural Science Foundation of China
       (39630090).The costs of publication of this article were defrayed
       in part by the payment of page charges. The article must therefore
       be hereby marked ÒadvertisementÓ in accordance with 18 U.S.C.
       Section 1734 solely to indicate this fact.
     * [116]&#x21b5;à To whom correspondence should be addressed: National
       Laboratory of Biomacromolecules, Institute of Biophysics, Chinese
       Academy of Sciences, 15 Datun Rd., Chaoyang District, Beijing
       100101, China. Tel.: 86-10-64889867; Fax: 86-10-64889867;
       E-mail:dcliang{at}sun5.ibp.ac.cn.
     * Abbreviations:

        PE
                phycoerythrin

        APC
                allophycocyanin

        PC
                phycocyanin

        C-PC
                C-phycocyanin

        PEC
                phycoerythrocyanin

        APC-PY
                allophycocyanin from P. yezoensis

        APC-SP
                APC from S. platensis

        C-PC-AQ
                C-PC from A. quadruplaticum

        C-PC-FR
                C-PC from F. diplosiphon

        R-PE-PU
                R-PE from Polysiphonia urceolata

        PCB
                phycocyanobilin

        &#x3b1;
                1&#x3b2;, 2&#x3b1;, 2&#x3b2;, &#x2009;É 6&#x3b2; stand for the individual subunits of
                different monomers within the hexamer (according to
                Schirmer et al. ([117]6))

        r.m.s.
                root mean square

     *
          + Received December 16, 1998.
          + Revision received March 31, 1999.
     * The American Society for Biochemistry and Molecular Biology, Inc.

   [118]Previous Section

 ¤2¤ REFERENCES ¤2¤

    1. [119]&#x21b5;
         1. Glazer A. N.
       (1984) Biochim. Biophys. Acta 768:29Ð51.
    2. [120]&#x21b5;
         1. Ficner R.,
         2. Huber R.
       (1992) Eur. J. Biochem. 218:103Ð106.
       [121]Medline
    3. [122]&#x21b5;
         1. Ficner R.,
         2. Lobeck K.,
         3. Schimdt G.,
         4. Huber R.
       (1992) J. Mol. Biol. 228:935Ð950.
       [123]CrossRef[124]Medline
    4. [125]&#x21b5;
         1. Chang W. R.,
         2. Jiang T.,
         3. Wan Z. L.,
         4. Zhang J. P.,
         5. Yang Z. X.,
         6. Liang D. C.
       (1996) J. Mol. Biol. 262:721Ð731.
       [126]CrossRef[127]Medline
    5. [128]&#x21b5;
         1. Schirmer T.,
         2. Bode W.,
         3. Huber R.,
         4. Sidler W.,
         5. Zuber H.
       (1985) J. Mol. Biol. 184:257Ð277.
       [129]CrossRef[130]Medline[131]Web of Science
    6. [132]&#x21b5;
         1. Schirmer T.,
         2. Huber R.,
         3. Schneider M.,
         4. Bode W.,
         5. Miller M.,
         6. Hackert M. L.
       (1986) J. Mol. Biol. 188:651Ð676.
       [133]CrossRef[134]Medline
    7. [135]&#x21b5;
         1. Duerring M.,
         2. Schmidt G. B.,
         3. Huber R.
       (1991) J. Mol. Biol. 217:577Ð592.
       [136]CrossRef[137]Medline[138]Web of Science
    8. [139]&#x21b5;
         1. Duerring M.,
         2. Huber R.,
         3. Bode W.,
         4. Ruembeli R.,
         5. Zuber H.
       (1990) J. Mol. Biol. 211:633Ð644.
       [140]CrossRef[141]Medline[142]Web of Science
    9. [143]&#x21b5;
         1. Brejc K.,
         2. Ficner R.,
         3. Huber R.,
         4. Steinbacher S.
       (1995) J. Mol. Biol. 249:424Ð440.
       [144]CrossRef[145]Medline[146]Web of Science
   10. [147]&#x21b5;
         1. Csatorday K.,
         2. MacColl R.,
         3. Csizmadia V.
       (1984) Biochemistry 23:6466Ð6470.
       [148]CrossRef[149]Medline
   11. [150]&#x21b5;
         1. Liu J. Y.,
         2. Zhang J. P.,
         3. Wan Z. L.,
         4. Liang D. C.,
         5. Zhang J. P.,
         6. Wu H. J.
       (1998) Acta Crystallogr. Sec. D 54:662Ð664.
       [151]CrossRef[152]Medline
   12. [153]&#x21b5;
         1. Navaza J.
       (1994) Acta Crystallogr. Sec. A 50:157Ð163.
       [154]CrossRef[155]Web of Science
   13. [156]&#x21b5;
         1. BrŸnger A.
       (1990) XPLOR, Version 2.1 (Yale University, New Haven, CN).
   14. [157]&#x21b5;
         1. Minami Y.,
         2. Yamada F.,
         3. Hase T.,
         4. Matsubara H.,
         5. Murakami A.,
         6. Fujita Y.,
         7. Takao T.,
         8. Shimonishi T.
       (1985) FEBS Lett. 191:216Ð220.
       [158]CrossRef
   15. [159]&#x21b5;
         1. Houmard J.,
         2. Capuano V.,
         3. Coursin T.,
         4. Tandeau de Marsac N.
       (1988b) J. Bacteriol. 170:5515Ð5521.
   16. [160]&#x21b5;
         1. Sidler W.,
         2. Gysi J.,
         3. Isker E.,
         4. Zuber H.
       (1981) Hoppe-SeylerÕs Z. Physiol. Chem. 362:611Ð628.
       [161]Medline
   17. [162]&#x21b5;
         1. Houmard J.,
         2. Mazel D.,
         3. Moquet C.,
         4. Bryant D. A.,
         5. Tandeau de Marsac N.
       (1986) Mol. Gen. Genet. 205:404Ð410.
       [163]CrossRef[164]Medline
   18. [165]&#x21b5;
         1. Apt K. E.,
         2. Grossman A. R.
       (1993) Plant Mol. Biol. 21:27Ð38.
       [166]CrossRef[167]Medline
   19. [168]&#x21b5;
         1. Offner G. D.,
         2. Troxler R. F.
       (1983) J. Biol. Chem. 258:9931Ð9940.
       [169]Abstract/FREE Full Text
   20. [170]&#x21b5;
         1. Luzzati P. V.
       (1952) Acta Crystallogr. 5:802Ð810.
       [171]CrossRef
   21. [172]&#x21b5;
         1. Ramachandran G. N.,
         2. Sasisekharan V.
       (1968) Adv. Protein Chem. 23:283Ð291.
       [173]Medline
   22. [174]&#x21b5;
         1. Karshikov A.,
         2. Duerring M.,
         3. Huber R.
       (1991) Protein Eng. 4:681Ð690.
       [175]Abstract/FREE Full Text
   23. [176]&#x21b5;
         1. Dexter D. L.
       (1953) J. Chem. Phys. 21:836Ð850.
       [177]CrossRef
   24. [178]&#x21b5;
       Fšrster, T. (1965) in Modern Quantum Chemistry(Sinanoglu, O., ed)
       Part III, pp. 93Ð137, Academic Press, New York.
   25. [179]&#x21b5;
         1. Jiang T.,
         2. Zhang J. P.,
         3. Liang D. C.
       (1999) Proteins Struct. Funct. Genet. 34:224Ð231.
       [180]CrossRef[181]Medline
   26. [182]&#x21b5;
         1. Schirmer T.,
         2. Border W.,
         3. Huber R.
       (1987) J. Mol. Biol. 196:677Ð695.
       [183]CrossRef[184]Medline[185]Web of Science
   27. [186]&#x21b5;
         1. MacColl R.
       (1983) Arch. Biochem. Biophys. 223:24Ð32.
       [187]CrossRef[188]Medline

     * [189]Add to CiteULike CiteULike
     * [190]Add to Complore Complore
     * [191]Add to Connotea Connotea
     * [192]Add to Del.icio.us Del.icio.us
     * [193]Add to Digg Digg

   [194]What's this?
   [195]Ç Previous | [196]Next Article È[197]Table of Contents

 ¤3¤ This Article ¤3¤

    1. doi: 10.1074/jbc.274.24.16945 June 11, 1999 The Journal of
       Biological Chemistry, 274, 16945-16952.

    1. [198]AbstractFree
    2. È Full TextFree
    3. [199]Full Text (PDF)Free

 ¤4¤ Classifications ¤4¤

    1.
          + [200]PROTEIN CHEMISTRY AND STRUCTURE

 ¤4¤ Services ¤4¤

    1. [201]Email this article to a friend
    2. [202]Alert me when this article is cited
    3. [203]Alert me if a correction is posted
    4. [204]Alert me when eletters are published
    5. [205]Similar articles in this journal
    6. [206]Similar articles in Web of Science
    7. [207]Similar articles in PubMed
    8. [208]Download to citation manager
    9. [209]Request Permissions

 ¤4¤ Responses ¤4¤

    1. [210]Submit a Letter to the Editor

 ¤4¤ Citing Articles ¤4¤

    1. [211]Load citing article information
    2. [212]Citing articles via Web of Science
    3. [213]Citing articles via Google Scholar

 ¤4¤ Google Scholar ¤4¤

    1. [214]Articles by Liu, J.
    2. [215]Articles by Liang, D.
    3. [216]Search for related content

 ¤4¤ PubMed ¤4¤

    1. [217]PubMed citation
    2. [218]Articles by Liu, J.
    3. [219]Articles by Liang, D.
    4.

 ¤4¤ Related Content ¤4¤

    1. [220]Load related web page information

 ¤4¤ Social Bookmarking ¤4¤

    1.
          + [221]Add to CiteULike CiteULike
          + [222]Add to Complore Complore
          + [223]Add to Connotea Connotea
          + [224]Add to Del.icio.us Del.icio.us
          + [225]Add to Digg Digg
       [226]What's this?

 ¤3¤ Navigate This Article ¤3¤

    1. [227]Top
    2. [228]Abstract
    3. [229]EXPERIMENTAL PROCEDURES
    4. [230]RESULTS AND DISCUSSION
    5. [231]ACKNOWLEDGEMENT
    6. [232]Footnotes
    7. [233]REFERENCES

 ¤3¤ This Week's Issue ¤3¤

    1. [234]September 24, 2010, 285 (39)

    1. [235]Current Issue

    1. [236]Alert me to new issues of JBC

     * [237]Authors
     * [238]Submit
     * [239]Subscribers
     * [240]Editorial Board
     * [241]RSS and Email Alerts
     * [242]Article Statistics
     * [243]Teaching Tools
     * [244]Copyright Permissions
     * [245]Advertise
     * [246]Contact JBC

     * Advertisement
     * Advertisement

   Copyright © 2010 by [247]American Society for Biochemistry and
   Molecular Biology

   [248]Alternate route to the JBC: http://intl.jbc.org

   [249]Contact JBC | [250]Help Pages
     * [251]asbmb_today_logo
     * [252]jlr_logo
     * [253]mcp_logo

     * Print ISSN 0021-9258
     * Online ISSN 1083-351X

   Advertisement
   Advertisement
     * [254]ASBMB Membership: Find out what ASBMB can do for YOU!

References

   Visible links
   1. http://www.jbc.org/
   2. file://localhost/dev/paper.html#content-block
   3. http://www.jbc.org/
   4. http://www.jbc.org/content/current
   5. http://www.jbc.org/content/by/year
   6. http://www.jbc.org/content/early/recent/0
   7. http://www.jbc.org/content/by/section/Minireviews
   8. http://www.jbc.org/content/by/section/Classics
   9. http://www.jbc.org/content/by/section/Reflections
  10. http://www.jbc.org/potw
  11. http://www.jbc.org/search
  12. http://www.jbc.org/content/by/year
  13. http://www.jbc.org/login?uri=http%3A%2F%2Fwww.jbc.org%2Fcontent%2F274%2F24%2F16945.long
  14. http://www.jbc.org/cgi/adclick/?ad=21365&adclick=true&url=http%3A%2F%2Fwww.jbc.org%2Fcgi%2Fbrowserellinks
  15. file://localhost/dev/paper.html#fn-1
  16. http://www.jbc.org/search?author1=Jin-Yu+Liu&sortspec=date&submit=Submit
  17. http://www.jbc.org/search?author1=Tao+Jiang&sortspec=date&submit=Submit
  18. http://www.jbc.org/search?author1=Ji-Ping+Zhang&sortspec=date&submit=Submit
  19. http://www.jbc.org/search?author1=Dong-Cai+Liang&sortspec=date&submit=Submit
  20. file://localhost/dev/paper.html#fn-2
  21. file://localhost/dev/paper.html#sec-1
  22. file://localhost/dev/paper.html#ref-1
  23. file://localhost/dev/paper.html#ref-2
  24. file://localhost/dev/paper.html#ref-5
  25. file://localhost/dev/paper.html#ref-8
  26. file://localhost/dev/paper.html#ref-9
  27. file://localhost/dev/paper.html#ref-10
  28. file://localhost/dev/paper.html#ref-9
  29. file://localhost/dev/paper.html#abstract-1
  30. file://localhost/dev/paper.html#sec-2
  31. file://localhost/dev/paper.html#ref-11
  32. file://localhost/dev/paper.html#ref-12
  33. file://localhost/dev/paper.html#ref-13
  34. file://localhost/dev/paper.html#sec-1
  35. file://localhost/dev/paper.html#ack-1
  36. file://localhost/dev/paper.html#ref-14
  37. file://localhost/dev/paper.html#ref-15
  38. file://localhost/dev/paper.html#ref-16
  39. file://localhost/dev/paper.html#ref-17
  40. file://localhost/dev/paper.html#ref-18
  41. file://localhost/dev/paper.html#ref-19
  42. file://localhost/dev/paper.html#T1
  43. http://www.jbc.org/content/274/24/16945/T1.expansion.html
  44. http://www.jbc.org/content/274/24/16945/T1.expansion.html
  45. file://localhost/dev/paper.html#ref-20
  46. file://localhost/dev/paper.html#T2
  47. file://localhost/dev/paper.html#F1
  48. file://localhost/dev/paper.html#ref-21
  49. file://localhost/dev/paper.html#T1
  50. file://localhost/dev/paper.html#ref-9
  51. file://localhost/dev/paper.html#F2
  52. http://www.jbc.org/content/274/24/16945/T2.expansion.html
  53. http://www.jbc.org/content/274/24/16945/T2.expansion.html
  54. http://www.jbc.org/content/274/24/16945/F1.expansion.html
  55. http://www.jbc.org/content/274/24/16945/F1.expansion.html
  56. http://www.jbc.org/content/274/24/16945/F1.expansion.html
  57. http://www.jbc.org/powerpoint/274/24/16945/F1
  58. http://www.jbc.org/content/274/24/16945/F2.expansion.html
  59. http://www.jbc.org/content/274/24/16945/F2.expansion.html
  60. http://www.jbc.org/content/274/24/16945/F2.expansion.html
  61. http://www.jbc.org/powerpoint/274/24/16945/F2
  62. file://localhost/dev/paper.html#T3
  63. http://www.jbc.org/content/274/24/16945/T3.expansion.html
  64. http://www.jbc.org/content/274/24/16945/T3.expansion.html
  65. file://localhost/dev/paper.html#F3
  66. http://www.jbc.org/content/274/24/16945/F3.expansion.html
  67. http://www.jbc.org/content/274/24/16945/F3.expansion.html
  68. http://www.jbc.org/content/274/24/16945/F3.expansion.html
  69. http://www.jbc.org/powerpoint/274/24/16945/F3
  70. file://localhost/dev/paper.html#F4
  71. file://localhost/dev/paper.html#F4
  72. file://localhost/dev/paper.html#ref-9
  73. http://www.jbc.org/content/274/24/16945/F4.expansion.html
  74. http://www.jbc.org/content/274/24/16945/F4.expansion.html
  75. http://www.jbc.org/content/274/24/16945/F4.expansion.html
  76. http://www.jbc.org/powerpoint/274/24/16945/F4
  77. file://localhost/dev/paper.html#ref-6
  78. file://localhost/dev/paper.html#ref-22
  79. file://localhost/dev/paper.html#ref-6
  80. file://localhost/dev/paper.html#F5
  81. file://localhost/dev/paper.html#F6
  82. file://localhost/dev/paper.html#T4
  83. http://www.jbc.org/content/274/24/16945/F5.expansion.html
  84. http://www.jbc.org/content/274/24/16945/F5.expansion.html
  85. http://www.jbc.org/content/274/24/16945/F5.expansion.html
  86. http://www.jbc.org/powerpoint/274/24/16945/F5
  87. http://www.jbc.org/content/274/24/16945/F6.expansion.html
  88. http://www.jbc.org/content/274/24/16945/F6.expansion.html
  89. http://www.jbc.org/content/274/24/16945/F6.expansion.html
  90. http://www.jbc.org/powerpoint/274/24/16945/F6
  91. http://www.jbc.org/content/274/24/16945/T4.expansion.html
  92. http://www.jbc.org/content/274/24/16945/T4.expansion.html
  93. file://localhost/dev/paper.html#F7
  94. file://localhost/dev/paper.html#ref-23
  95. file://localhost/dev/paper.html#ref-24
  96. http://www.jbc.org/content/274/24/16945/F7.expansion.html
  97. http://www.jbc.org/content/274/24/16945/F7.expansion.html
  98. http://www.jbc.org/content/274/24/16945/F7.expansion.html
  99. http://www.jbc.org/powerpoint/274/24/16945/F7
 100. file://localhost/dev/paper.html#T4
 101. file://localhost/dev/paper.html#ref-25
 102. file://localhost/dev/paper.html#ref-26
 103. file://localhost/dev/paper.html#F8
 104. http://www.jbc.org/content/274/24/16945/F8.expansion.html
 105. http://www.jbc.org/content/274/24/16945/F8.expansion.html
 106. http://www.jbc.org/content/274/24/16945/F8.expansion.html
 107. http://www.jbc.org/powerpoint/274/24/16945/F8
 108. file://localhost/dev/paper.html#ref-27
 109. file://localhost/dev/paper.html#ref-6
 110. file://localhost/dev/paper.html#ref-9
 111. file://localhost/dev/paper.html#sec-2
 112. file://localhost/dev/paper.html#fn-group-1
 113. file://localhost/dev/paper.html#ack-1
 114. file://localhost/dev/paper.html#ref-list-1
 115. file://localhost/dev/paper.html#xref-fn-1-1
 116. file://localhost/dev/paper.html#xref-fn-2-1
 117. file://localhost/dev/paper.html#ref-6
 118. file://localhost/dev/paper.html#fn-group-1
 119. file://localhost/dev/paper.html#xref-ref-1-1
 120. file://localhost/dev/paper.html#xref-ref-2-1
 121. http://www.jbc.org/external-ref?access_num=8243457&link_type=MED
 122. file://localhost/dev/paper.html#xref-ref-2-1
 123. http://www.jbc.org/external-ref?access_num=10.1016/0022-2836(92)90876-L&link_type=DOI
 124. http://www.jbc.org/external-ref?access_num=1469725&link_type=MED
 125. file://localhost/dev/paper.html#xref-ref-2-1
 126. http://www.jbc.org/external-ref?access_num=10.1006/jmbi.1996.0547&link_type=DOI
 127. http://www.jbc.org/external-ref?access_num=8876649&link_type=MED
 128. file://localhost/dev/paper.html#xref-ref-5-1
 129. http://www.jbc.org/external-ref?access_num=10.1016/0022-2836(85)90379-1&link_type=DOI
 130. http://www.jbc.org/external-ref?access_num=3928897&link_type=MED
 131. http://www.jbc.org/external-ref?access_num=A1985AMS4300008&link_type=ISI
 132. file://localhost/dev/paper.html#xref-ref-5-1
 133. http://www.jbc.org/external-ref?access_num=10.1016/S0022-2836(86)80013-4&link_type=DOI
 134. http://www.jbc.org/external-ref?access_num=3090271&link_type=MED
 135. file://localhost/dev/paper.html#xref-ref-5-1
 136. http://www.jbc.org/external-ref?access_num=10.1016/0022-2836(91)90759-Y&link_type=DOI
 137. http://www.jbc.org/external-ref?access_num=1899708&link_type=MED
 138. http://www.jbc.org/external-ref?access_num=A1991EZ03400018&link_type=ISI
 139. file://localhost/dev/paper.html#xref-ref-8-1
 140. http://www.jbc.org/external-ref?access_num=10.1016/0022-2836(90)90270-V&link_type=DOI
 141. http://www.jbc.org/external-ref?access_num=2106585&link_type=MED
 142. http://www.jbc.org/external-ref?access_num=A1990CR81900010&link_type=ISI
 143. file://localhost/dev/paper.html#xref-ref-9-1
 144. http://www.jbc.org/external-ref?access_num=10.1006/jmbi.1995.0307&link_type=DOI
 145. http://www.jbc.org/external-ref?access_num=7783202&link_type=MED
 146. http://www.jbc.org/external-ref?access_num=A1995RB61600017&link_type=ISI
 147. file://localhost/dev/paper.html#xref-ref-10-1
 148. http://www.jbc.org/external-ref?access_num=10.1021/bi00321a029&link_type=DOI
 149. http://www.jbc.org/external-ref?access_num=6529563&link_type=MED
 150. file://localhost/dev/paper.html#xref-ref-11-1
 151. http://www.jbc.org/external-ref?access_num=10.1107/S0907444997017824&link_type=DOI
 152. http://www.jbc.org/external-ref?access_num=9761868&link_type=MED
 153. file://localhost/dev/paper.html#xref-ref-12-1
 154. http://www.jbc.org/external-ref?access_num=10.1107/S0108767393007597&link_type=DOI
 155. http://www.jbc.org/external-ref?access_num=A1994NG58500001&link_type=ISI
 156. file://localhost/dev/paper.html#xref-ref-13-1
 157. file://localhost/dev/paper.html#xref-ref-14-1
 158. http://www.jbc.org/external-ref?access_num=10.1016/0014-5793(85)80011-9&link_type=DOI
 159. file://localhost/dev/paper.html#xref-ref-15-1
 160. file://localhost/dev/paper.html#xref-ref-16-1
 161. http://www.jbc.org/external-ref?access_num=6792029&link_type=MED
 162. file://localhost/dev/paper.html#xref-ref-17-1
 163. http://www.jbc.org/external-ref?access_num=10.1007/BF00338074&link_type=DOI
 164. http://www.jbc.org/external-ref?access_num=3031427&link_type=MED
 165. file://localhost/dev/paper.html#xref-ref-18-1
 166. http://www.jbc.org/external-ref?access_num=10.1007/BF00039615&link_type=DOI
 167. http://www.jbc.org/external-ref?access_num=7678762&link_type=MED
 168. file://localhost/dev/paper.html#xref-ref-19-1
 169. http://www.jbc.org/cgi/ijlink?linkType=ABST&journalCode=jbc&resid=258/16/9931
 170. file://localhost/dev/paper.html#xref-ref-20-1
 171. http://www.jbc.org/external-ref?access_num=10.1107/S0365110X52002161&link_type=DOI
 172. file://localhost/dev/paper.html#xref-ref-21-1
 173. http://www.jbc.org/external-ref?access_num=4882249&link_type=MED
 174. file://localhost/dev/paper.html#xref-ref-22-1
 175. http://www.jbc.org/cgi/ijlink?linkType=ABST&journalCode=proeng&resid=4/6/681
 176. file://localhost/dev/paper.html#xref-ref-23-1
 177. http://www.jbc.org/external-ref?access_num=10.1063/1.1699044&link_type=DOI
 178. file://localhost/dev/paper.html#xref-ref-24-1
 179. file://localhost/dev/paper.html#xref-ref-25-1
 180. http://www.jbc.org/external-ref?access_num=10.1002/(SICI)1097-0134(19990201)34:2%3C224::AID-PROT8%3E3.0.CO;2-D&link_type=DOI
 181. http://www.jbc.org/external-ref?access_num=10022358&link_type=MED
 182. file://localhost/dev/paper.html#xref-ref-26-1
 183. http://www.jbc.org/external-ref?access_num=10.1016/0022-2836(87)90040-4&link_type=DOI
 184. http://www.jbc.org/external-ref?access_num=3119857&link_type=MED
 185. http://www.jbc.org/external-ref?access_num=A1987J731500018&link_type=ISI
 186. file://localhost/dev/paper.html#xref-ref-27-1
 187. http://www.jbc.org/external-ref?access_num=10.1016/0003-9861(83)90567-2&link_type=DOI
 188. http://www.jbc.org/external-ref?access_num=6407396&link_type=MED
 189. http://www.jbc.org/external-ref?tag_url=http://www.jbc.org/cgi/content/long/274/24/16945&title=Crystal%20Structure%20of%20Allophycocyanin%20from%20Red%20AlgaePorphyra%20yezoensis%20at%202.2-%C3%85%20Resolution+--+Liu%20et%20al.%20274%20%2824%29%3A%2016945+--+JBC&doi=10.1074/jbc.274.24.16945&link_type=CITEULIKE
 190. http://www.jbc.org/external-ref?tag_url=http://www.jbc.org/cgi/content/long/274/24/16945&title=Crystal%20Structure%20of%20Allophycocyanin%20from%20Red%20AlgaePorphyra%20yezoensis%20at%202.2-%C3%85%20Resolution+--+Liu%20et%20al.%20274%20%2824%29%3A%2016945+--+JBC&doi=10.1074/jbc.274.24.16945&link_type=COMPLORE
 191. http://www.jbc.org/external-ref?tag_url=http://www.jbc.org/cgi/content/long/274/24/16945&title=Crystal%20Structure%20of%20Allophycocyanin%20from%20Red%20AlgaePorphyra%20yezoensis%20at%202.2-%C3%85%20Resolution+--+Liu%20et%20al.%20274%20%2824%29%3A%2016945+--+JBC&doi=10.1074/jbc.274.24.16945&link_type=CONNOTEA
 192. http://www.jbc.org/external-ref?tag_url=http://www.jbc.org/cgi/content/long/274/24/16945&title=Crystal%20Structure%20of%20Allophycocyanin%20from%20Red%20AlgaePorphyra%20yezoensis%20at%202.2-%C3%85%20Resolution+--+Liu%20et%20al.%20274%20%2824%29%3A%2016945+--+JBC&doi=10.1074/jbc.274.24.16945&link_type=DEL_ICIO_US
 193. http://www.jbc.org/external-ref?tag_url=http://www.jbc.org/cgi/content/long/274/24/16945&title=Crystal%20Structure%20of%20Allophycocyanin%20from%20Red%20AlgaePorphyra%20yezoensis%20at%202.2-%C3%85%20Resolution+--+Liu%20et%20al.%20274%20%2824%29%3A%2016945+--+JBC&doi=10.1074/jbc.274.24.16945&link_type=DIGG
 194. http://www.jbc.org/help/social_bookmarks.dtl
 195. http://www.jbc.org/content/274/24/16940.short
 196. http://www.jbc.org/content/274/24/16953.short
 197. http://www.jbc.org/content/274/24.toc
 198. http://www.jbc.org/content/274/24/16945.abstract
 199. http://www.jbc.org/content/274/24/16945.full.pdf+html
 200. http://www.jbc.org/search?tocsectionid=PROTEIN+CHEMISTRY+AND+STRUCTURE&sortspec=date&submit=Submit
 201. http://www.jbc.org/email?gca=jbc;274/24/16945&current-view-path=/content/274/24/16945.long
 202. http://www.jbc.org/cgi/alerts/ctalert?alertType=citedby&addAlert=cited_by&cited_by_criteria_resid=jbc;274/24/16945&saveAlert=no&return-type=article&return_url=http://www.jbc.org/content/274/24/16945.long
 203. http://www.jbc.org/cgi/alerts/ctalert?alertType=correction&addAlert=correction&correction_criteria_value=274/24/16945&saveAlert=no&return-type=article&return_url=http://www.jbc.org/content/274/24/16945.long
 204. http://www.jbc.org/cgi/alerts/ctalert?alertType=eletter&addAlert=eletter&eletter_criteria_value=274/24/16945&saveAlert=no&return-type=article&return_url=http://www.jbc.org/content/274/24/16945.long
 205. http://www.jbc.org/search?qbe=jbc;274/24/16945&citation=Liu%20et%20al.%20274%20%2824%29:%2016945&submit=yes
 206. http://www.jbc.org/external-ref?access_num=jbc%3B274%2F24%2F16945&link_type=ISI_RELATEDRECORDS
 207. http://www.jbc.org/external-ref?access_num=10358042&link_type=MED_NBRS
 208. http://www.jbc.org/citmgr?gca=jbc;274/24/16945
 209. https://s100.copyright.com/AppDispatchServlet?publisherName=ASBMB&publication=jbc&title=Crystal%20Structure%20of%20Allophycocyanin%20from%20Red%20AlgaePorphyra%20yezoensis%20at%202.2-%C3%85%20Resolution&publicationDate=06/11/1999&author=Jin-Yu%20Liu,%20Tao%20Jiang,%20Ji-Ping%20Zhang,%20Dong-Cai%20Liang&startPage=16945&contentID=10.1074/jbc.274.24.16945&orderBeanReset=true&endPage=16952&volumeNum=274&issueNum=24
 210. http://www.jbc.org/letters/submit/jbc;274/24/16945
 211. http://www.jbc.org/content/274/24/16945.long?cited-by=yes&legid=jbc;274/24/16945#cited-by
 212. http://www.jbc.org/external-ref?access_num=jbc%3B274%2F24%2F16945&link_type=ISI_CITING
 213. http://www.jbc.org/external-ref?access_num=http://www.jbc.org/cgi/content/abstract/274/24/16945&link_type=GOOGLESCHOLAR
 214. http://scholar.google.com/scholar?q=%22author%3ALiu%20author%3AJ.%22
 215. http://scholar.google.com/scholar?q=%22author%3ALiang%20author%3AD.%22
 216. http://www.jbc.org/external-ref?access_num=http://www.jbc.org/cgi/content/abstract/274/24/16945&link_type=GOOGLESCHOLARRELATED
 217. http://www.jbc.org/external-ref?access_num=10358042&link_type=PUBMED
 218. http://www.jbc.org/external-ref?access_num=Liu%20J&link_type=AUTHORSEARCH
 219. http://www.jbc.org/external-ref?access_num=Liang%20D&link_type=AUTHORSEARCH
 220. http://www.jbc.org/content/274/24/16945.long?related-urls=yes&legid=jbc;274/24/16945#related-urls
 221. http://www.jbc.org/external-ref?tag_url=http://www.jbc.org/cgi/content/long/274/24/16945&title=Crystal%20Structure%20of%20Allophycocyanin%20from%20Red%20AlgaePorphyra%20yezoensis%20at%202.2-%C3%85%20Resolution+--+Liu%20et%20al.%20274%20%2824%29%3A%2016945+--+JBC&doi=10.1074/jbc.274.24.16945&link_type=CITEULIKE
 222. http://www.jbc.org/external-ref?tag_url=http://www.jbc.org/cgi/content/long/274/24/16945&title=Crystal%20Structure%20of%20Allophycocyanin%20from%20Red%20AlgaePorphyra%20yezoensis%20at%202.2-%C3%85%20Resolution+--+Liu%20et%20al.%20274%20%2824%29%3A%2016945+--+JBC&doi=10.1074/jbc.274.24.16945&link_type=COMPLORE
 223. http://www.jbc.org/external-ref?tag_url=http://www.jbc.org/cgi/content/long/274/24/16945&title=Crystal%20Structure%20of%20Allophycocyanin%20from%20Red%20AlgaePorphyra%20yezoensis%20at%202.2-%C3%85%20Resolution+--+Liu%20et%20al.%20274%20%2824%29%3A%2016945+--+JBC&doi=10.1074/jbc.274.24.16945&link_type=CONNOTEA
 224. http://www.jbc.org/external-ref?tag_url=http://www.jbc.org/cgi/content/long/274/24/16945&title=Crystal%20Structure%20of%20Allophycocyanin%20from%20Red%20AlgaePorphyra%20yezoensis%20at%202.2-%C3%85%20Resolution+--+Liu%20et%20al.%20274%20%2824%29%3A%2016945+--+JBC&doi=10.1074/jbc.274.24.16945&link_type=DEL_ICIO_US
 225. http://www.jbc.org/external-ref?tag_url=http://www.jbc.org/cgi/content/long/274/24/16945&title=Crystal%20Structure%20of%20Allophycocyanin%20from%20Red%20AlgaePorphyra%20yezoensis%20at%202.2-%C3%85%20Resolution+--+Liu%20et%20al.%20274%20%2824%29%3A%2016945+--+JBC&doi=10.1074/jbc.274.24.16945&link_type=DIGG
 226. http://www.jbc.org/help/social_bookmarks.dtl
 227. file://localhost/dev/paper.html#content-block
 228. file://localhost/dev/paper.html#abstract-1
 229. file://localhost/dev/paper.html#sec-1
 230. file://localhost/dev/paper.html#sec-2
 231. file://localhost/dev/paper.html#ack-1
 232. file://localhost/dev/paper.html#fn-group-1
 233. file://localhost/dev/paper.html#ref-list-1
 234. http://www.jbc.org/content/current
 235. http://www.jbc.org/content/current
 236. http://www.jbc.org/cgi/alerts/etoc
 237. http://www.jbc.org/misc/itoa.xhtml
 238. http://submit.jbc.org/
 239. http://www.jbc.org/subscriptions/
 240. http://submit.jbc.org/journals/jbc/forms/editors.dtl
 241. http://www.jbc.org/site/home/about/rss_alerts.xhtml
 242. http://www.jbc.org/site/home/about/article_stats.xhtml
 243. http://www.jbc.org/site/home/teaching_tools/
 244. http://www.jbc.org/site/misc/Copyright_Permission.xhtml
 245. http://www.asbmb.org/uploadedFiles/Publications/2009ASBMBJournalsMediaKit.pdf
 246. http://www.jbc.org/cgi/feedback
 247. http://www.asbmb.org/
 248. http://intl.jbc.org/
 249. http://www.jbc.org/cgi/feedback
 250. http://www.jbc.org/help/
 251. http://www.asbmb.org/page.aspx?id=218
 252. http://www.jlr.org/
 253. http://mcponline.org/
 254. http://www.jbc.org/cgi/adclick/?ad=21401&adclick=true&url=http%3A%2F%2Fwww.asbmb.org%2Fmembership

   Hidden links:
 255. http://www.jbc.org/entrez-links/10358042