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EMERGING TOPICS

Ecto-ADP-ribose Transferases: Cell-Surface Response to Local Tissue Injury

Anna Zolkiewska

Department of Biochemistry, Kansas State University, Manhattan, Kansas

zolkiea{at}ksu.edu

	Abstract

 
Ecto-ADP-ribose transferases (ecto-ARTs) catalyze the transfer of ADP-ribose from NAD⁺ to arginine residues in cell-surface proteins. Since the concentration of extracellular NAD⁺ is very low under normal physiological conditions but rises significantly upon tissue injury or membrane stress, it is postulated that the main role of ecto-ARTs is to ADP-ribosylate and regulate the function of certain membrane receptors in response to elevated levels of NAD⁺.

	Introduction

Top Introduction Ecto-ARTs Extracellular NAD+ levels and... Protein targets of ecto-ARTs How can ADP-ribosylation lead... Conclusions References

 
Nicotinamide adenine dinucleotide (NAD⁺) is not only a key coenzyme in oxidation/reduction reactions, but it is also an important signaling molecule (9). The signaling function of NAD⁺ is related to its ability to donate the ADP-ribose group. In enzyme-catalyzed reactions, the glycosidic bond between nicotinamide and the adjacent ribose in the NAD⁺ molecule is cleaved, and the ADP-ribose moiety is transferred to specific amino acids in proteins, or it reacts with the acetyl group derived from acetylated proteins. The latter reaction is catalyzed by the Sir2 family of NAD⁺-dependent protein deacetylases, or sirtuins (2, 11, 12). Sirtuin-mediated deacetylation of histones and several key transcription factors in the nucleus provides a link between metabolism, cell survival and differentiation, and longevity in metazoans (13, 21, 28). The former reaction—transfer of ADP-ribose to proteins—is catalyzed by enzymes known as ADP-ribose transferases (ARTs). Poly-ARTs (PARPs) catalyze the transfer of an initial ADP-ribose to glutamate residues in target proteins, as well as elongation and branching of poly(ADP-ribose) chains. PARPs operate in the nucleus of eukaryotic cells, where they are involved in DNA repair and apoptosis (5, 19, 71). In contrast, mono-ARTs catalyze the transfer of a single ADP-ribose group to proteins. The ART family includes many bacterial toxins (e.g., cholera, pertussis, diphtheria, and botulinum toxin; Refs. 4, 46, and 56), as well as much-less-characterized eukaryotic ARTs. This review is focused on mammalian ARTs, a unique group of enzymes with unusual properties and unexpected cellular localization, and their roles in tissue injury. The reader is also referred to recent excellent reviews that provide a more comprehensive discussion of the topic of mono-ADP-ribosylation (24, 82).

	Ecto-ARTs

Top Introduction Ecto-ARTs Extracellular NAD+ levels and... Protein targets of ecto-ARTs How can ADP-ribosylation lead... Conclusions References

 
ART1 was identified as the first mammalian mono-ART after protein purification from rabbit skeletal muscle and cDNA cloning (106). ART2, initially described in rat as RT6 alloantigen expressed on T lymphocytes, was later shown to be a mono-ART based on its sequence similarity to ART1 (50, 51, 78). Two isoforms of ART2 are expressed in mouse as a result of gene duplication; ART2 protein is not detected in humans due to premature stop codons in the human ART2 gene (36). Subsequently, three additional gene products related to ART1 and 2, namely ART3–5, were described in mouse and human (30, 49, 74). Interestingly, no ART-related genes have been identified in yeast, worm, fly, or plant genomes.

Among the five known ARTs, only ART1, 2, and 5 have the signature sequence R-S-EXE of arginine-specific mono-ARTs in their putative catalytic sites. Enzymes of this class catalyze a stereospecific transfer of the ADP-ribose moiety from ß-NAD⁺ to the guanidinium group of arginine residues to form an -anomeric ADP-ribosylarginine (FIGURE 1). ART3 and 4 lack the R-S-EXE motif, and it is not clear whether or not they are active ARTs (31). ART1, 2, and 5 show a rather restricted pattern of expression, with ART1 predominantly expressed in skeletal and cardiac muscle (31, 106), ART2 present in peripheral lymphoid tissues (31, 93), and ART5 being abundant in testis (30, 31).

View larger version (16K): [in this window] [in a new window]   FIGURE 1. Reaction catalyzed by arginine-specific ADP-ribose transferases ADP-ribose transferases (ARTs) catalyze stereospecific transfer of ADP-ribose from ß-NAD+ to arginine residues in proteins. The products of the reaction are -ADP-ribosylarginine and free nicotinamide.

	Extracellular NAD+ levels and tissue injury

Top Introduction Ecto-ARTs Extracellular NAD+ levels and... Protein targets of ecto-ARTs How can ADP-ribosylation lead... Conclusions References

 
Extracellular localization of ART1, 2, and 5 poses an intriguing question: is the concentration of NAD⁺ outside the cell high enough for the catalysis? The Michaelis-Menten constant (K_m) of ART1 for NAD⁺ was reported to be ~0.6 mM when ADP-ribose was transferred to free arginine (54) and ~0.1 mM when ADP-ribose was transferred to membrane proteins at the surface of ART1-transfected cells (26). Under normal physiological conditions, the concentration of free NAD⁺ in the extracellular compartment (in the plasma) is in the range of 0.1–0.3 µM (48). These concentrations are much lower than the K_m value of ART1 and, most likely, of the other two ARTs. It is expected, therefore, that the catalytic activities of ecto-ARTs are very low under these conditions. To attain significant activities, ecto-ARTs must experience much higher levels of NAD⁺. High concentrations of extracellular NAD⁺ can occur during local tissue injury, when the integrity of plasma membrane is compromised and NAD⁺ leaks out from damaged or dying cells.

There are several types of tissue or cell damage leading to elevated levels of extracellular nucleotides, including NAD⁺, that are particularly relevant to the topic of ecto-ADP-ribosylation. The most dramatic case of such damage involves cytolysis induced by infectious inflammatory processes. During this condition, NAD⁺ released from lysed cells serves as a substrate for ART2 in T cells present at the site of infection (52). On the other hand, various types of metabolic or mechanical stresses can trigger NAD⁺ efflux without cell lysis. "Chemical ischemia" induced by inhibition of glycolytic and oxidative metabolism leads to opening of unapposed connexin43 (Cx43) hemichannnels in astrocytes, HeLa cells, and 3T3 fibroblasts (14, 22, 23). These hemichannels have been shown to mediate NAD⁺ efflux from intact cells (14). Interestingly, Cx43 is abundantly expressed in cardiac muscle (95), where it may play a similar role in transporting NAD⁺ outside the cell and thus providing the substrate for muscle-specific ART1. Furthermore, a Cx43-independent mechanism has been implicated in the release of ATP (80), UTP (55), and NAD⁺ (79) from human osteoblastic (79, 80) or astrocytoma cells (55) subjected to mechanical stimuli by medium displacement. Recently it has been reported that electrical field stimulation of postganglionic nerve terminals results in the efflux not only of well-known factors such as ATP and norepinephrine but also of NAD⁺ (86). Finally, mechanical stress associated with stretching of neurons (29) or C2C12 muscle cells (15) seeded on flexible substratum made of silicone resulted in increased membrane permeability, as shown by the uptake of fluorescein-labeled dextran. Although the release of NAD⁺ was not directly measured in these experiments, the transiently formed membrane defects appeared large enough to permit the passage of NAD⁺.

Mechanical forces imposed on many tissues under physiological conditions lead to a loss of plasma membrane in constituent cells in vivo. Many of these disruptions are transient and do not lead to necrosis or apoptosis (66, 67). The levels of such "cell wounding" are the highest in skeletal and cardiac muscle. As these tissues constantly experience a certain degree of mechanical load, the amount of "wounded" cells has been reported to reach 5–30% under physiological conditions (20, 65). Microscopic "wounds" are usually repaired with the help of dysferlin, a member of the ferlin family (6, 25). The prevalence of membrane disruptions in muscle and the importance of the dysferlin-mediated repair mechanism is underscored by the fact that mutations in the dysferlin gene are associated with limb-girdle muscular dystrophy (type 2B) and Miyoshi myopathy (6, 25).

The ability of the plasma membrane of muscle cells to withstand a mechanical force and resist damage is severely compromised in the absence of dystrophin (53, 68, 77). Dystrophin is an intracellular component of the dystrophin-glycoprotein complex that provides a link between the actin cytoskeleton and the extracellular matrix (ECM) in muscle (27, 43). Mutations in the dystrophin gene and the loss of functional dystrophin protein in muscle are the primary cause of Duchenne muscular dystrophy in humans and in mdx mice, a mouse model of this disorder (40, 85). Dystrophin deficiency results in membrane lesions, causing chronic leakage of intracellular components, including cytosolic enzymes creatine kinase and pyruvate kinase, from myofibers and allowing influx of extracellular dyes such as procion red or Evans blue (37, 64, 88).

In conclusion, skeletal and cardiac muscle are constantly subjected to mechanical stress that may result in membrane injury and transient increase in membrane permeability. In the absence of dystrophin, myofibers are particularly prone to damage and plasma membrane leakiness is more sustained and severe. Since skeletal and cardiac muscle express high levels of ART1, it is conceivable that this ecto-ART experiences then a continuous supply of the substrate, extracellular NAD⁺, at the surface of damaged muscle fibers.

	Protein targets of ecto-ARTs

Top Introduction Ecto-ARTs Extracellular NAD+ levels and... Protein targets of ecto-ARTs How can ADP-ribosylation lead... Conclusions References

 
The list of proteins being modified by ADP-ribosylation by ecto-ARTs includes several soluble growth factors or peptides, as well as important cell-surface receptors involved in transmembrane signaling. Fibroblast growth factor-2 (44), platelet-derived growth factor BB (81), insulin-like growth factor (81), and -defensin-1 [an anti-microbial peptide (76)] were all reported to be ADP-ribosylated in vitro. Mass spectral analysis of endogenous -defensin-1 present in bronchoalveolar lavage fluid further indicated that -defensin-1 was ADP-ribosylated in vivo in smokers but not in nonsmokers (76).

In addition to ADP-ribosylating soluble factors, membrane-anchored ART1 and 2 can also modify extracellular domains of transmembrane proteins (61, 73, 98, 102). Two of these proteins have been characterized more thoroughly and will be discussed here in detail: the P2X7 purinoreceptor and cell-adhesion molecule ₇-integrin.

P2X7 is a cytolytic ATP receptor that mediates apoptotic cell death of T cells, macrophages, and dendritic cells (72). Recently, it has been shown that P2X7 is a direct target of ART2-mediated ADP-ribosylation at the surface of intact mouse T cells (83). ADP-ribosylation of the P2X7 receptor results in its activation, causing calcium flux, formation of large membrane pores, phosphatidylserine exposure, shedding of CD62L, cell shrinkage, and eventually T cell apoptosis (3, 35, 47, 60). Interestingly, the symptoms of NAD⁺-induced cell death are very similar to the symptoms generated by ATP, but the concentrations of NAD⁺ required for induction of cell death are much lower than the concentrations of ATP (83).

The exact mechanism of activation of the P2X7 receptor by ADP-ribosylation is currently unknown, but two different models have been proposed (83). First, ADP-ribose that is covalently attached to an arginine residue could function as a ligand for the adenosine binding site in the receptor. Second, ADP-ribosylation could activate the receptor via an allosteric mechanism. Regardless of the mechanism of activation of P2X7, ADP-ribosylation of the receptor is believed to play an important role in preventing undesirable activation and eliminating irrelevant and potentially autoreactive bystander T cells at the sites of infectious inflammatory reactions (83). Consistently, a lack of ART2 expression has been previously correlated with enhanced susceptibility to autoimmune diseases in several animal models (1, 33).

ART1 is the major ecto-ART of skeletal and cardiac muscle (31, 106). When mouse skeletal muscle cells are cultured in vitro, ART1 is undetectable in nondifferentiated, mononucleated myoblasts and is strongly upregulated in differentiated, multinucleated myotubes (106). After incubation of intact, differentiated mouse C2C12 myotubes with exogenous NAD⁺, ₇-integrin was identified as the key protein substrate for ART1 (104, 105). At micromolar concentrations of NAD⁺, ₇-integrin was practically the only protein undergoing ADP-ribosylation (104). At ~100 µM NAD⁺, additional proteins appeared to be ADP-ribosylated as well, but ₇-integrin still remained the predominant target of the ART1 enzyme (103, 105). The modification of ₇-integrin occurred within minutes after adding NAD⁺ to cells and reached the yield of at least 0.4 mol ADP-ribose/mol ₇-integrin (103, 105).

Integrins are transmembrane heterodimers composed of - and ß-subunits that bind to various components of the ECM (42). ₇-Integrin is expressed specifically in skeletal and cardiac muscle, forms a dimer with ß₁-integrin, and binds to laminin, an ECM protein (16, 97). Interestingly, in cytotoxic T cells that express high levels of ecto-ART activity, two other members of the integrin family, _L and ß₂ (forming the LFA-1 dimer), were also found to be ADP-ribosylated (70, 73). Thus in T cells, both subunits of the same _Lß₂ dimer may be ADP-ribosylated, whereas in the case of ₇ß₁-integrin, only the ₇-subunit undergoes modification and no ADP-ribosylation is associated with the ß₁-subunit.

₇-Integrin is composed of the NH₂-terminal "heavy" chain (X1 or X2 splice variant of ~100 kDa) and the COOH-terminal "light" chain (A or B splice variant of ~33 or ~38 kDa, respectively) (Ref. 16; see FIGURE 2). The two chains are connected by a disulfide bond and are separated upon reduction. ART1 modifies only the heavy chain and does not show any preference for the X1 or the X2 splice variant (103). The "light" chain of ₇-integrin, despite containing 121 amino acids that belong to the extracellular domain and include 6 Arg residues (amino acids 915–1035; FIGURE 2), is not ADP-ribosylated in intact cells. At low NAD⁺ concentrations (<10 µM), ADP-ribosylation takes place exclusively in the region of ₇-integrin between amino acids 605 and 914 (103, 105). This region contains 20 Arg residues, and it is not known which and how many of these residues are ADP-ribosylated (FIGURE 2). At higher NAD⁺ concentrations (75–100 µM), additional site(s) in the NH₂-terminal fragment of ₇-integrin between amino acids 34 and 604 are also modified (103, 105). It is obvious, however, that ADP-ribosylation of these additional site(s) is much less efficient, and most likely it is a consequence of a decreased specificity of ART1 at high NAD⁺ concentrations.

View larger version (95K): [in this window] [in a new window]   FIGURE 2. Amino acid sequence of mouse 7-integrin (the X2B isoform) The signal peptide is shown in italics, the transmembrane domain is underlined, amino acids 34–914 represent the "heavy" chain, and amino acids 915–1135 correspond to the "light" chain. The boxed fragment of the extracellular domain contains the major ADP-ribosylation site(s) by arginine-specific ecto-ART1. All arginine residues present in this fragment are highlighted. Arginines for which the distance from the membrane in the structural model of 7-integrin is smaller than the diameter of ART (see FIGURE 4B) are highlighted in magenta; these arginines are potential targets for ART1 at the surface of muscle cells. Arginines for which the distance from the membrane is predicted to exceed the diameter of an ART are highlighted in blue; these arginines are unlikely to serve as substrates for ART1 in intact cells.

	How can ADP-ribosylation lead to integrin activation?

Top Introduction Ecto-ARTs Extracellular NAD+ levels and... Protein targets of ecto-ARTs How can ADP-ribosylation lead... Conclusions References

 
Extracellular domains of integrins are composed of a globular NH₂-terminal head domain containing the ligand-binding site and two long, flexible stalks that connect to the transmembrane and cytoplasmic domains (101). Integrins can exist in several conformational states with different ligand-binding affinities (FIGURE 3). An "inactive" conformation, with the stalks of the heterodimer bent in the middle and the headpiece facing toward the membrane, has the lowest ligand-binding affinity. An "active" conformation, with straightened integrin stalks and an open headpiece, has the highest ligand-binding affinity. A body of evidence suggests that integrin straightening and induction of the high-affinity state is intrinsically coupled to the separation of the stalks, the transmembrane domains, and the cytoplasmic tails (84, 90). Integrin activation is achieved by shifting the equilibrium from the inactive to the active conformer (FIGURE 3). This transition is induced by ligand-binding events in the extracellular domains ("outside-in" signaling) or by protein-protein interactions mediated by the cytoplasmic tails ("inside-out" signaling) (58, 94).

View larger version (39K): [in this window] [in a new window]   FIGURE 3. Current model of integrin activation The integrin ßdimer can exist in a bent conformation, with a closed headpiece and a low ligand-binding affinity (left), or in an extended conformation, with an open headpiece and a high ligand-binding affinity (right). Induction of the extended conformation is accompanied by separation of the stalks, the transmembrane domains, and the cytoplasmic tails (84, 90).

_vß₃-Integrin is the only integrin for which the crystal structure of the entire extracellular domain is available (101). FIGURE 4A shows the structure of the _vß₃ dimer in a low-affinity conformation. The region of the _v-sub-unit corresponding to amino acids 605–914 in ₇-integrin is shown in cyan; the rest of _v-integrin is shown in green, and ß₃-integrin is shown in yellow. The fragment of mouse ₇-integrin between amino acids 605 and 914 contains the major ADP-ribosylation site(s), as discussed above. Interestingly, although this region is separated from the transmembrane domain by 121 amino acids of the "light chain" in the ₇ sequence (see FIGURE 2), it is adjacent to the membrane (FIGURE 4A). FIGURE 4B, LEFT depicts a structural model of this ₇ fragment (amino acids 605 and 914) next to the structure of rat ART2, the only available structure of a mammalian ecto-ART (69) (the molecular weights of mouse ART1 and rat ART2 are similar, and their sequence similarity is ~50%). The positions of all 20 Arg residues in the ₇-integrin structure are indicated. Interestingly, size comparison of the modeled ₇-integrin fragment and the structure of ART2 suggests that only 10 out of the total 20 Arg residues in ₇-integrin may be within the reach of ART at the cell surface (FIGURE 4B, RIGHT). Notably, a large cluster of Arg residues is located in the area that is predicted to be in close proximity to the membrane, in the lower portion of the integrin stalk. Membrane anchoring of ART1 via a flexible glycosylphosphatidylinositol tail may enable the enzyme to gain access to one or more of these residues and to catalyze the transfer of ADP-ribose from NAD⁺. Interestingly, a similar cluster of Arg residues is not detected in the _v-integrin, and this integrin, although being expressed in muscle cells, is not subject to ADP-ribosylation.

View larger version (42K): [in this window] [in a new window]   FIGURE 4. Localization of possible ADP-ribosylation sites within the predicted 7-integrin structure A: crystal structure of the extracellular domain of vß3-integrin in a bent, low-affinity conformation (PDB structure 1JV2). The v fragment between amino acids 568 and 845, corresponding to amino acids 605–914 in 7-integrin (based on sequence alignment using CLUSTAL W) is shown in cyan; the rest of v-integrin is shown in green, and ß3-integrin is shown in yellow. Notice that the v fragment extends to the end of the stalk region that is in close proximity to the membrane. B: predicted structure of 7-integrin fragment between amino acids 605 and 914, obtained by threading the 7 sequence onto the v structure using the Swiss-PdbViewer software and then submitted to the SWISS-MODEL server for refinement (left, grey). All 20 arginine residues are shown in cyan. The structure of rat ART2 enzyme (PDB structure 1OG3) is shown in the same scale (right, yellow). Amino acids R126, S147, and E189I at the catalytic site of ART2 are depicted in red; the COOH terminus (a site of glycosylphosphatidylinositol attachment), shown in blue, is facing the membrane. Notice that although the extracellular domains of integrins make a rigid transition into the transmembrane domains and the angle between the integrin stalk and the membrane is fixed and close to 90°, lipid anchoring of ARTs allows a large degree of flexibility at the protein-membrane interface, but it does not allow ART to reach beyond the membrane-proximal region of 7-integrin. The arginine residues within the 7 fragment that are separated from the membrane by a distance shorter than the diameter of ART2 and therefore may be accessible for the catalytic site of the enzyme are labeled; the same arginines are highlighted in magenta in FIGURE 2.

	Conclusions

Top Introduction Ecto-ARTs Extracellular NAD+ levels and... Protein targets of ecto-ARTs How can ADP-ribosylation lead... Conclusions References

 
Mammalian ecto-ARTs continue to pose many unanswered and fascinating questions. With the catalytic site located at the extracellular face of the membrane, with NAD⁺ serving as a donor of ADP-ribose, with important tissue-specific membrane receptors being the acceptors of ADP-ribose, and with functions of these receptors drastically changed after ADP-ribose attachment, the emerging view is that ecto-ARTs may help tissues to cope with local injuries. An unresolved issue that needs to be investigated in the future is whether the same proteins that are ADP-ribosylated ex vivo are also modified in vivo, after tissue damage and the leakage of intracellular NAD⁺ to the external milieu.

	References

Top Introduction Ecto-ARTs Extracellular NAD+ levels and... Protein targets of ecto-ARTs How can ADP-ribosylation lead... Conclusions References

 

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