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Mbalaviele, G. Role of Adenosine Diphosphate-Ribosylation in Bone Health. Encyclopedia. Available online: https://encyclopedia.pub/entry/19635 (accessed on 19 November 2024).
Mbalaviele G. Role of Adenosine Diphosphate-Ribosylation in Bone Health. Encyclopedia. Available at: https://encyclopedia.pub/entry/19635. Accessed November 19, 2024.
Mbalaviele, Gabriel. "Role of Adenosine Diphosphate-Ribosylation in Bone Health" Encyclopedia, https://encyclopedia.pub/entry/19635 (accessed November 19, 2024).
Mbalaviele, G. (2022, February 18). Role of Adenosine Diphosphate-Ribosylation in Bone Health. In Encyclopedia. https://encyclopedia.pub/entry/19635
Mbalaviele, Gabriel. "Role of Adenosine Diphosphate-Ribosylation in Bone Health." Encyclopedia. Web. 18 February, 2022.
Role of Adenosine Diphosphate-Ribosylation in Bone Health
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This entry is adapted from the peer-reviewed paper 10.3390/cells8101201

Adenosine diphosphate (ADP)-ribosylation is the transfer of ADP-ribose units from nicotinamide adenine dinucleotide (NAD+) to acceptor proteins. This post-translational modification (PTM) unavoidably alters protein functions and signaling networks, thereby impacting cell behaviors and tissue outcomes. As a ubiquitous mechanism, ADP-ribosylation affects multiple tissues, including bones, as abnormal ADP-ribosylation compromises bone development and remodeling.

ADP-ribosylation bone

1. Introduction

The transfer of adenosine diphosphate (ADP)-ribose unit(s) from nicotinamide adenine dinucleotide (NAD+) to acceptor proteins is known as ADP-ribosylation. This post-translational modification (PTM) unavoidably alters protein functions and signaling networks, thereby impacting cell behaviors and tissue outcomes. As a ubiquitous mechanism, ADP-ribosylation affects multiple tissues, including bones, as abnormal ADP-ribosylation compromises bone development and remodeling.

2. Osteoclast Differentiation

During development, the emerging ossification centers recruit myeloid progenitors where they undergo terminal differentiation into the osteoclasts, which resorb the mineralized matrix, an action that over time results in the formation of the bone marrow cavity [1][2][3]. Postnatally, the damaged or old bone matrix is sensed and removed by the osteoclasts, and is evenly replaced by the osteoblasts. Potential sensors of defective bone matrix components include the innate immune complex, NOD-like receptor family (NLR), pyrin domain containing 3 (NLRP3) inflammasome, which is activated by bone matrix degradation products and promotes osteoclast differentiation [4][5]. While bone marrow myeloid precursors (e.g., CD11blowCD115highCD117high-expressing cells) differentiate into the osteoclasts in homeostatic conditions, circulating monocytes are capable of forming osteoclasts or fusing with pre-existing multinucleated osteoclasts in pathological settings, such as inflammatory arthritis [6][7][8][9][10][11]. Osteoclast differentiation, activity, and survival depend on macrophage colony-stimulating factor (M-CSF) and receptor activator of NF-κB ligand (RANKL), whose expression and signaling outputs are regulated by various factors such as hormones (e.g., parathyroid hormone, estrogen, and 1,25α-dihydroxyvitamin D3) and pro-inflammatory cytokines, including those of the tumor necrosis factor (TNF) and interleukin-1 (IL-1) families [12][13][14][15]. For simplicity, osteoclast differentiation was considered, though other biological aspects of these cells, such as activity and survival, are occasionally described. M-CSF, RANKL, and the majority of osteoclast-regulating factors are mainly produced by cells of the osteoblast lineage, and immune cells (e.g., macrophages, T and B lymphocytes) though the osteoclasts themselves produce factors such as sphingosine-1-phosphate and Wnts, which act not only in autocrine manner, but also paracrine fashion, regulating the functions of neighboring cells such as the osteoblasts [16][17][18][19][20][21]. Osteoclast differentiation is driven by complex interactions among various transcription factors, including the nuclear factor of activated T cells cytoplasmic 1 (NFATc1), NF-κB, and c-Fos [22]. While the effects of PTMs such as phosphorylation, methylation, ubiquitination, and SUMOylation on transcriptional regulation and other key osteoclastogenic events have been extensively studied [23][24][25][26][27][28][29][30][31], only a few studies have investigated the role of ADP-ribosylation in osteoclast biology.

2.1. Role of ARTD1 in Osteoclast Differentiation

ARTD1 is the most studied member of the ARTD family in the skeleton. Early studies show that ARTD1 protein levels decline during in vitro osteoclast differentiation induced by RANKL, a response that correlates with increased expression of the a3 isoform of the V-ATPase subunit, tartrate-resistant acid phosphatase, and brain-type creatine kinase [32][33][34][35]. In agreement with the proposition that ARTD1 is a negative regulator of osteoclastogenesis, this protein binds to and represses the activity of the promoters of the aforementioned genes in the osteoclast precursors [32][33][34][35]. Follow up studies using engineered mice expressing uncleavable ARTD1 or Artd1-deficient mice, not only reinforce the anti-osteoclastogenic functions of ARTD1, but also shed light into the underlying mechanisms [36][37][38][39]. Novel insights include the demonstration that i) ARTD1 inhibits histone3lysine4 trimethylation (H3K4me3), histone marks of active chromatin, at the promoters of key osteoclastogenic factors such as B lymphocyte-induced maturation protein 1 (Blimp1), and ii) ARTD1 PARylates itself during osteoclast formation, a prerequisite modification that targets this protein for destruction through the proteasome pathway [39]. ARTD1 also inhibits H3K4me3 and H4 acetylation, thereby impeding the recruitment of the RelA subunit of NF-κB to the IL-1β promoter [37]. Progressive decline in ARTD1 levels also occurs during the differentiation of myotubes, which are multinucleated fibers that arise from the fusion of myoblasts [40]. The basis for the apparent inverse correlation between ARTD1 abundance and multinucleation is unclear, though it is tempting to speculate that the degradation of this enzyme, whose activity can deplete total intracellular NAD+ levels by 80% may be necessary to prevent energy collapse during the high energy-demanding differentiation process.
Mice lacking ARTD1 globally or selectively in myeloid cells indistinguishably exhibit a low bone mass phenotype associated with an increased number of the osteoclasts on bone surfaces (Wang et al., personal communication). Consistent with the view of osteoclast lineage autonomous actions of ARTD1, in vitro osteoclastogenesis from isolated mouse bone marrow cells is higher in Artd1 null cells compared to wild-type controls [37]. Potential ARTD1 substrates include the master regulators of osteoclast differentiation, NF-κB and NFATc1, which are PARylated by this enzyme in T cells and smooth muscle cells [41][42][43][44][45]. However, such interplay is unlikely in light of the recent study indicating that PARylated NF-κB and NFATc1 are undetectable in cells of the osteoclast lineage. Instead, ARTD1 consistently PARylates histone H2B among other proteins, and decreases the occupancy of H2B at the NFATc1 promoter, thereby inhibiting NFATc1 expression and restraining osteoclast differentiation (Wang et al., personal communication).
ARTD1 is cleaved at D214 into 89 kDa and 24 kDa fragments, presumably by caspase-7, in response to activation of the NLRP3 and NLR, CARD containing 4 (NLRC4) inflammasomes [39][46][47][48]. Consistent with its pro-inflammatory actions, loss of ARTD1 partially protects joints from destruction in the mouse model of collagen antibody-induced arthritis [49][50][51][52][53]. In line with the ability of ARTD1 and its cleaved fragments to activate signaling platforms such as the NF-κB pathway, knockin mice expressing uncleavable ARTD1 are resistant to ischemia/reperfusion-induced inflammation in intestine and kidney [36][41]. Unexpectedly, this ARTD1 mutant does not affect inflammatory outcomes induced by hyperactive NLRP3 inflammasome [38]. These conflicting results may be explained by the fact that ARTD1 actions are cell-context-dependent. Indeed, ARTD1 promotes NF-κB PARylation or activity in cultured smooth muscle cells, neuronal cells, and macrophages, while negatively regulating this transcription factor in lymphocytic leukemia cells [41][42][44][48]. Despite some gaps in our understanding of ARTD1 mechanisms of action, evidence overwhelmingly indicates that this enzyme negatively regulates osteoclast development (Figure 1).
Cells 08 01201 g002 550
Figure 1. Effects of ADP-ribosylation on osteoclast formation. ARTD1, ARTD5, and ARTD6 catalyze the attachment of ADP-ribose polymers from NAD+ to target proteins (PARylation), releasing nicotinamide (NAM) in the process; their actions lead to the inhibition of osteoclast differentiation. SIRT6 inhibits osteoclast development; however, the effects of its MARylating actions in this process are not clear because this enzyme also has deacetylase activity. Lysine deacetylation is coupled to NAD+ hydrolysis, yielding a deacetylated targeted protein, O-acetyl-ADP-ribose, and NAM. Ac, acetyl.

2.2. Role of ARTD5 and ARTD6 in Osteoclast Differentiation

ARTD5 (also known as PARP5A or tankyrase 1) and ARTD6 (also referred to as PARP5B or tankyrase 2) [54] are expressed by many cell types, including the osteoclast lineage [55][56][57][58]. ARTD5 and ARTD6 are implicated in a range of biological processes, including DNA repair, glucose homeostasis and energy expenditure, and skeletal metabolism (through their interactions with the adaptor protein SH3 domain-binding protein 2, SH3BP2 and AXIN 1/2) [55][59][60][61][62][63]. PARylation targets SH3BP2 for ubiquitination by the E3-ubiquitin ligase RNF46, and subsequently for degradation [55][64]. Missense mutations in SH3BP2 result in SH3BP2 that is stable, as it escapes the destructive actions of ARTD5 and ARTD6, and are associated with cherubism, a hereditary childhood-onset autoinflammatory disorder, whose severity regresses after puberty [65]. Focal facial bone lesions and deformities associated with the destruction of the jaws and dental complications characterize this disease [65]. Knockin mice expressing the most common disease-associated allele develop systemic inflammation (e.g., excessive TNF-α production) and bone loss due to massive osteoclast differentiation as a consequence of heightened sensitivity to M-CSF- and RANKL-induced signals; these events ultimately cumulate in hyperactivation of osteoclastogenic pathways such as Src, Syk, ERK1/2, and NFATc1 [55][56]. Conversely, Sh3bp2-deficient osteoclasts exhibit defective bone resorption in vitro [57]. Furthermore, pharmacological inhibition of ARTD5 and ARTD6, which results in SH3BP2 accumulation, promotes osteoclast differentiation in vitro and bone resorption in vivo [58][66], findings that are consistent with accelerated in vitro osteoclastogenesis of osteoclast precursors lacking both ARTD5 and ARTD6 [55]. A recent study suggests that oral bacteria produce pathogen-associated molecular patterns (PAMPs), which in conjunction with danger-associated molecular patterns (DAMPs) released during the remodeling of the jaws, provide tissue-restricted bone lesions in cherubism. Decreased jaw remodeling with age leading to attenuated levels of DAMPs may underlie the reported regression of this disorder over time in the affected patients [67]. Thus, ARTD5 and ARTD6 function as negative regulators of osteoclast differentiation (Figure 1).

3. Therapeutic Implications

ARTs are novel and promising targets for cancer therapies. Numerous studies have shown that various small-molecule inhibitors of ARTDs are efficacious against various cancers, including ovarian cancer, breast cancer, colon cancer, lung cancer, prostate cancer, hepatocellular carcinoma, osteosarcoma, and chordoma [68][69][70][71][72][73][74][75][76][77][78][79]. More importantly, the US Food and Drug Administration has approved three different ARTD inhibitors, olaparib, niraparib, and rucaparib for the treatment of BRCA1- or BRAC2-mutated ovarian cancers. Considering the crucial role that ARTDs play in the pathogenesis of acute tissue injury or periodontitis, some of these drugs may be indicated for the treatment of inflammatory osteolysis. However, pre-clinical evidence indicates that genetic or pharmacological inhibition of ARTD1 or ARTD5 and ARTD6 causes bone loss, a high-risk factor for fracture. Therefore, comprehensive translational studies may help understand the extent to which ARTD inhibitors may adversely affect the skeleton.

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Subjects: Agriculture, Dairy & Animal Science
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Gabriel Mbalaviele
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