Parathyroid hormone-related protein inhibits nitrogen-containing bisphosphonate-induced apoptosis of human periodontal ligament fibroblasts by activating MKP1 phosphatase

References

• Bassett CA, Donath A, Macagno F, et al. Diphosphonates in the treatment of myositis ossificans. Lancet. 1969;2(7625):845.
   PubMed Web of Science ®Google Scholar
• Rogers MJ, Crockett JC, Coxon FP, et al. Biochemical and molecular mechanisms of action of bisphosphonates. Bone. 2011;49(1):34–41.
   PubMed Web of Science ®Google Scholar
• Lindsay R. Modeling the benefits of pamidronate in children with osteogenesis imperfecta. J Clin Invest. 2002;110(9):1239–1241.
   PubMed Web of Science ®Google Scholar
• Marx RE. Pamidronate (Aredia) and zoledronate (Zometa) induced avascular necrosis of the jaws: a growing epidemic. J Oral Maxillofac Surg. 2003;61(9):1115–1117.
   PubMed Web of Science ®Google Scholar
• Ruggiero SL, Dodson TB, Fantasia J, et al. American association of oral and maxillofacial surgeons. American association of oral and maxillofacial surgeons position paper on medication-related osteonecrosis of the jaw–2014 update. J Oral Maxillofac Surg. 2014;72(10)::1938–1956.
   Web of Science ®Google Scholar
• Ruggiero SL, Mehrotra B, Rosenberg TJ, et al. Osteonecrosis of the jaws associated with the use of bisphosphonates: a review of 63 cases. J Oral Maxillofac Surg. 2004;62(5):527–534.
   PubMed Web of Science ®Google Scholar
• Taniguchi N, Osaki M, Onuma K, et al. Bisphosphonate-induced reactive oxygen species inhibit proliferation and migration of oral fibroblasts: a pathogenesis of bisphosphonate-related osteonecrosis of the jaw. J Periodontol. 2020;91(7):947–955.
   PubMed Web of Science ®Google Scholar
• Lang M, Zhou Z, Shi L, et al. Influence of zoledronic acid on proliferation, migration, and apoptosis of vascular endothelial cells. Br J Oral Maxillofac Surg. 2016;54(8):889–893.
   PubMed Web of Science ®Google Scholar
• Ray P, Huang BW, Tsuji Y. Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cell Signal. 2012;24(5):981–990.
   PubMed Web of Science ®Google Scholar
• Almeida M, O’Brien CA. Basic biology of skeletal aging: role of stress response pathways. J Gerontol A Biol Sci Med Sci. 2013;68(10):1197–1208.
   PubMed Web of Science ®Google Scholar
• Haigis MC, Yankner BA. The Aging Stress Response. Mol Cell. 2010;40(2):333–344.
   PubMed Web of Science ®Google Scholar
• Martindale JL, Holbrook NJ. Cellular response to oxidative stress: signaling for suicide and survival. J Cell Physiol. 2002;192(1):1–15.
   PubMed Web of Science ®Google Scholar
• Janssen-Heininger YM, Mossman BT, Heintz NH, et al. van der Vliet A: redox-based regulation of signal transduction: principles, pitfalls, and promises. Free Radic Biol Med. 2008;45(1):1–17.
   PubMed Web of Science ®Google Scholar
• Ray PD, Huang BW, Tsuji Y. Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cell Signal. 2012;24(5):981–990.
   PubMed Web of Science ®Google Scholar
• Checa J, Aran JM. Reactive oxygen species: drivers of physiological and pathological processes. J Inflamm Res. 2020;13:1057–1073.
   PubMed Web of Science ®Google Scholar
• Haigis MC, Yankner BA. The aging stress response. Mol Cell. 2010;40(2):333–344.
   PubMed Web of Science ®Google Scholar
• Xiao L, Pimentel DR, Wang J, et al. Role of reactive oxygen species and NAD(P)H oxidase in alpha(1)-adrenoceptor signaling in adult rat cardiac myocytes. Am J Physiol Cell Physiol. 2002;282(4):C926–934.
   PubMed Web of Science ®Google Scholar
• Kim BY, Han MJ, Chung AS. Effects of reactive oxygen species on proliferation of Chinese hamster lung fibroblast (V79) cells. Free Radic Biol Med. 2001;30(6):686–698.
   PubMed Web of Science ®Google Scholar
• Wu Y, Yang Y, Yang P, et al. The osteogenic differentiation of PDLSCs is mediated through MEK/ERK and p38 MAPK signalling under hypoxia. Arch Oral Biol. 2013;58(10):1357–1368.
   PubMed Web of Science ®Google Scholar
• Almeida M, Han L, Ambrogini E, et al. Oxidative stress stimulates apoptosis and activates NF-kappaB in osteoblastic cells via a PKCbeta/p66shc signaling cascade: counter regulation by estrogens or androgens. Mol Endocrinol. 2010;24(10):2030–2037.
   PubMedGoogle Scholar
• Hao C, Wu X, Zhou R, et al. Downregulation of p66Shc can reduce oxidative stress and apoptosis in oxidative stress model of marginal cells of stria vascularis in Sprague Dawley rats. Drug Des Devel Ther. 2019;13:3199–3206.
   PubMed Web of Science ®Google Scholar
• Duan W, Yang Y, Yi W, et al. New role of JAK2/STAT3 signaling in endothelial cell oxidative stress injury and protective effect of melatonin. PLoS One. 2013;8(3):e57941.
   PubMed Web of Science ®Google Scholar
• Villanueva I, Alva-Sánchez C, Pacheco-Rosado J. The role of thyroid hormones as inductors of oxidative stress and neurodegeneration. Oxid Med Cell Longev. 2013;2013:218145.
   PubMed Web of Science ®Google Scholar
• Miao D, He B, Jiang Y, et al. Osteoblast-derived PTHrP is a potent endogenous bone anabolic agent that modifies the therapeutic efficacy of administered PTH 1-34. J Clin Invest. 2005;115(9):2402–2411.
   PubMed Web of Science ®Google Scholar
• McCauley LK, Martin TJ. Twenty-five years of PTHrP progress: from cancer hormone to multifunctional cytokine. J Bone Miner Res. 2012;27(6):1231–1239.
   PubMed Web of Science ®Google Scholar
• Esbrit P, Alcaraz MJ. Current perspectives on parathyroid hormone (PTH) and PTH-related protein (PTHrP) as bone anabolic therapies. Biochem Pharmacol. 2013;85(10):1417–1423.
   PubMed Web of Science ®Google Scholar
• Mahalingam CD, Sampathi BR, Sharma S, et al. MKP1-dependent PTH modulation of bone matrix mineralization in female mice is osteoblast maturation stage specific and involves P-ERK and P-p38 MAPKs. J Endocrinol. 2013;216(3):315–329.
   PubMed Web of Science ®Google Scholar
• Boutros T, Chevet E, Metrakos P. Mitogen-activated protein (MAP) kinase/MAP kinase phosphatase regulation: roles in cell growth, death, and cancer. Pharmacol Rev. 2008;60(3):261–310.
   PubMed Web of Science ®Google Scholar
• Kirk SG, Samavati L, Liu Y. MAP kinase phosphatase-1, a gatekeeper of the acute innate immune response. Life Sci. 2020;241:11715.
   Web of Science ®Google Scholar
• Ardura JA, Portal-Núñez S, Castelbón-Calvo I, et al. Parathyroid hormone-related protein protects osteoblastic cells from oxidative stress by activation of MKP1 phosphatase. J Cell Physiol. 2017;232(4):785–796.
   PubMed Web of Science ®Google Scholar
• Tai TW, Chen CY, Su FC, et al. Reactive oxygen species are required for zoledronic acid-induced apoptosis in osteoclast precursors and mature osteoclast-like cells. Sci Rep. 2017;7(1):44245.
   PubMedGoogle Scholar
• Trappanese DM, Sivilich S, Ets HK, et al. Regulation of mitogen-activated protein kinase by protein kinase C and mitogen-activated protein kinase phosphatase-1 in vascular smooth muscle. Am J Physiol Cell Physiol. 2016;310(11):C921–C930.
   PubMed Web of Science ®Google Scholar
• Chen Y, Wang H, Zhang R, et al. Microinjection of sanguinarine into the ventrolateral orbital cortex inhibits Mkp-1 and exerts an antidepressant-like effect in rats. Neurosci Lett. 2012;506(2):327–331.
   PubMed Web of Science ®Google Scholar
• Vogt A, Tamewitz A, Skoko J, et al. The benzo[c]phenanthridine alkaloid, sanguinaraine, is a selective, cell active inhibitor of mitogen-activated protein kinase phosphatase-1. J Biol Chem. 2005;280(19):19078–19086.
   PubMed Web of Science ®Google Scholar
• Conde De La Rosa L, Mh S, Te V, et al. Superoxide anions and hydrogen peroxide induce hepatocyte death by different mechanisms: involvement of JNK and ERK MAP kinases. J Hepatol. 2006;44(5):918–929.
   PubMed Web of Science ®Google Scholar
• Griffith CE, Zhang W, Wange RL. ZAP-70-dependent and -independent activation of Erk in Jurkat T cells. Differences in signaling induced by H2o2 and Cd3 cross-linking. J Biol Chem. 1998;273(17):10771–10776.
   PubMed Web of Science ®Google Scholar
• Lezcano V, Gentili C, De Boland AR. Role of PTHrP in human intestinal Caco-2 cell response to oxidative stress. Biochim Biophys Acta. 2013;1833(12):2834–2843.
   PubMed Web of Science ®Google Scholar
• De Colli M, Zara S, Di Giacomo V, et al. Nitric oxide-mediated cytotoxic effect induced by zoledronic acid treatment on human gingival fibroblasts. Clin Oral Investig. 2015;19:1269–1277.
   PubMed Web of Science ®Google Scholar
• Tai TW, Su FC, Chen CY, et al. Activation of p38 MAPK-regulated Bcl-xL signaling increases survival against zoledronic acid-induced apoptosis in osteoclast precursors. Bone. 2014;67:166–174.
   PubMed Web of Science ®Google Scholar
• Kang W, Jia Z, Tang D, et al. Fusobacterium nucleatum facilitates apoptosis, ROS generation, and inflammatory cytokine production by activating AKT/MAPK and NF-κB signaling pathways in human gingival fibroblasts. Oxid Med Cell Longev. 2019;2019:1681972.
   PubMed Web of Science ®Google Scholar
• Cagnol S, Chambard JC. ERK and cell death: mechanisms of ERK-induced cell death–apoptosis, autophagy and senescence. FEBS J. 2010;277(1):2–21.
   PubMed Web of Science ®Google Scholar
• Ichijo H, Nishida E, Irie K, et al. Induction of apoptosis by ASK1, a mammalian MAPKKK that activates SAPK/JNK and p38 signaling pathways. Science. 1997;275(5296):90–94.
   PubMed Web of Science ®Google Scholar
• Kim AH, Khursigara G, Sun X, et al. Akt phosphorylates and negatively regulates apoptosis signal-regulating kinase 1. Mol Cell Biol. 2001;21(3):893–901.
   PubMed Web of Science ®Google Scholar
• Meyer R, Schreckenberg R, Kretschmer F, et al. Parathyroid hormone-related protein (PTHrP) signal cascade modulates myocardial dysfunction in the pressure overloaded heart. Eur J Heart Fail. 2007;9(12):1156–1162.
   PubMed Web of Science ®Google Scholar
• Röthig A, Schreckenberg R, Weber K, et al. Effects of nicotine on PTHrP and PTHrP receptor expression in rat coronary endothelial cells. Cell Physiol Biochem. 2012;29(3–4):485–492.
   PubMedGoogle Scholar
• Franklin CC, Kraft AS. Conditional expression of the mitogen-activated protein kinase (MAPK) phosphatase MKP-1 preferentially inhibits p38 MAPK and stress-activated protein kinase in U937 cells. J Biol Chem. 1997;272(27):16917–16923.
   PubMed Web of Science ®Google Scholar
• Migliaccio E, Giorgio M, Mele S, et al. The p66shc adaptor protein controls oxidative stress response and life span in mammals. Nature. 1999;402(6759):309–313.
   PubMed Web of Science ®Google Scholar
• Giorgio M, Migliaccio E, Orsini F, et al. Electron transfer between cytochrome c and p66Shc generates reactive oxygen species that trigger mitochondrial apoptosis. Cell. 2005;122(2):221–233.
   PubMed Web of Science ®Google Scholar
• Orsini F, Migliaccio E, Moroni M, et al. The life span determinant p66Shc localizes to mitochondria where it associates with mitochondrial heat shock protein 70 and regulates trans-membrane potential. J Biol Chem. 2004;279(24):25689–25695.
   PubMed Web of Science ®Google Scholar
• Hu Y, Wang X, Zeng L, et al. ERK phosphorylates p66shcA on Ser36 and subsequently regulates p27kip1 expression via the Akt-FOXO3a pathway: implication of p27kip1 in cell response to oxidative stress. Mol Biol Cell. 2005;16(8):3705–3718.
   PubMed Web of Science ®Google Scholar
• Fa K, Yamamori T, Mattagajasingh I, et al. Rac1 leads to phosphorylation-dependent increase in stability of the p66shc adaptor protein: role in Rac1-induced oxidative stress. Mol Biol Cell. 2006;17(1):122–129.
   PubMed Web of Science ®Google Scholar