A New Role of NAP1L1 in Megakaryocytes and Human Platelets
Abstract
:1. Introduction
2. Results
2.1. CD34+-Derived MKs and Freshly Isolated Human PLTs Express NAP1L1
2.2. NAP1L1 Directly Interacts with the Dihydrolipopolylysine-Residue Acetyltransferase Component of Pyruvate Dehydrogenase Complex (PDC-E2, ODP2)
2.3. NAP1L1 and PDC-E2 Show Dynamic Expression Changes When PLTs Are Exposed to Septic Conditions
2.4. Pyruvate Dehydrogenase Complex Activity Is Increased in PLTs during Sepsis
2.5. NAP1L1 Overexpression in MKs Induced Reduced Proplatelet Formation (PPF)
3. Discussion
4. Materials and Methods
4.1. Reagents and Antibodies
4.2. Septic Patients
4.3. PLT Isolation and Culture
4.4. CD34+-Derived MKs
4.5. RNA Isolation
4.6. Next Generation RNA-Sequencing
4.7. PCR Studies
4.8. Immunocytochemistry
4.9. Microscopy and Image Analysis
4.10. Protein Expression Studies
4.11. Co-Immunoprecipitation Studies
4.12. Mass Spectrometry
4.13. PDH Activity Assay
4.14. NAP1L1 In Vitro Transcription
4.15. NAP1L1 Transfection and Overexpression
4.16. Proplatelet Formation Assay
4.17. Statistical Analyses
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Acknowledgments
Conflicts of Interest
References
- Lichtman, M.A.; Chamberlain, J.K.; Simon, W.; Santillo, P.A. Parasinusoidal location of megakaryocytes in marrow: A determinant of platelet release. Am. J. Hematol. 1978, 4, 303–312. [Google Scholar] [CrossRef] [PubMed]
- Lefrancais, E.; Ortiz-Munoz, G.; Caudrillier, A.; Mallavia, B.; Liu, F.; Sayah, D.M.; Thornton, E.E.; Headley, M.B.; David, T.; Coughlin, S.R.; et al. The lung is a site of platelet biogenesis and a reservoir for haematopoietic progenitors. Nature 2017, 544, 105–109. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Patel, S.R.; Hartwig, J.H.; Italiano, J.E., Jr. The biogenesis of platelets from megakaryocyte proplatelets. J. Clin. Investig. 2005, 115, 3348–3354. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Machlus, K.R.; Italiano, J.E., Jr. The incredible journey: From megakaryocyte development to platelet formation. J. Cell Biol. 2013, 201, 785–796. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Machlus, K.R.; Thon, J.N.; Italiano, J.E., Jr. Interpreting the developmental dance of the megakaryocyte: A review of the cellular and molecular processes mediating platelet formation. Br. J. Haematol. 2014, 165, 227–336. [Google Scholar] [CrossRef]
- Campbell, R.A.; Franks, Z.; Bhatnagar, A.; Rowley, J.W.; Manne, B.K.; Supiano, M.A.; Schwertz, H.; Weyrich, A.S.; Rondina, M.T. Granzyme A in Human Platelets Regulates the Synthesis of Proinflammatory Cytokines by Monocytes in Aging. J. Immunol. 2018, 200, 295–304. [Google Scholar] [CrossRef] [Green Version]
- Campbell, R.A.; Schwertz, H.; Hottz, E.D.; Rowley, J.W.; Manne, B.K.; Washington, A.V.; Hunter-Mellado, R.; Tolley, N.D.; Christensen, M.; Eustes, A.S.; et al. Human megakaryocytes possess intrinsic anti-viral immunity through regulated induction of IFITM3. Blood 2019, 133, 2013–2026. [Google Scholar] [CrossRef]
- Middleton, E.A.; Rowley, J.W.; Campbell, R.A.; Grissom, C.K.; Brown, S.M.; Beesley, S.J.; Schwertz, H.; Kosaka, Y.; Manne, B.K.; Krauel, K.; et al. Sepsis alters the transcriptional and translational landscape of human and murine platelets. Blood 2019, 134, 911–923. [Google Scholar] [CrossRef]
- Junt, T.; Schulze, H.; Chen, Z.; Massberg, S.; Goerge, T.; Krueger, A.; Wagner, D.D.; Graf, T.; Italiano, J.E., Jr.; Shivdasani, R.A.; et al. Dynamic visualization of thrombopoiesis within bone marrow. Science 2007, 317, 1767–1770. [Google Scholar] [CrossRef] [Green Version]
- Patel, S.R.; Richardson, J.L.; Schulze, H.; Kahle, E.; Galjart, N.; Drabek, K.; Shivdasani, R.A.; Hartwig, J.H.; Italiano, J.E., Jr. Differential roles of microtubule assembly and sliding in proplatelet formation by megakaryocytes. Blood 2005, 106, 4076–4085. [Google Scholar] [CrossRef]
- Bender, M.; Thon, J.N.; Ehrlicher, A.J.; Wu, S.; Mazutis, L.; Deschmann, E.; Sola-Visner, M.; Italiano, J.E.; Hartwig, J.H. Microtubule sliding drives proplatelet elongation and is dependent on cytoplasmic dynein. Blood 2015, 125, 860–868. [Google Scholar] [CrossRef] [Green Version]
- Schmidt, H.; Carter, A.P. Review: Structure and mechanism of the dynein motor ATPase. Biopolymers 2016, 105, 557–567. [Google Scholar] [CrossRef]
- Koupenova, M.; Clancy, L.; Corkrey, H.A.; Freedman, J.E. Circulating Platelets as Mediators of Immunity, Inflammation, and Thrombosis. Circ. Res. 2018, 122, 337–351. [Google Scholar] [CrossRef]
- Semple, J.W.; Italiano, J.E., Jr.; Freedman, J. Platelets and the immune continuum. Nat. Rev. Immunol. 2011, 11, 264–274. [Google Scholar] [CrossRef]
- Weyrich, A.S.; Schwertz, H.; Kraiss, L.W.; Zimmerman, G.A. Protein synthesis by platelets: Historical and new perspectives. J. Thromb. Haemost. 2009, 7, 241–246. [Google Scholar] [CrossRef] [Green Version]
- Zimmerman, G.A.; Weyrich, A.S. Signal-dependent protein synthesis by activated platelets: New pathways to altered phenotype and function. Arter. Thromb. Vasc. Biol. 2008, 28, s17–s24. [Google Scholar] [CrossRef] [Green Version]
- Bhatlekar, S.; Basak, I.; Edelstein, L.C.; Campbell, R.A.; Lindsey, C.R.; Italiano, J.E., Jr.; Weyrich, A.S.; Rowley, J.W.; Rondina, M.T.; Sola-Visner, M.; et al. Anti-apoptotic BCL2L2 increases megakaryocyte proplatelet formation in cultures of human cord blood. Haematologica 2019, 104, 2075–2083. [Google Scholar] [CrossRef] [Green Version]
- Frey, C.; Koliopoulou, A.G.; Montenont, E.; Tolley, N.D.; Javan, H.; McKellar, S.H.; Drakos, S.G.; Selzman, C.H.; Rondina, M.T. Longitudinal assessment of the platelet transcriptome in advanced heart failure patients following mechanical unloading. Platelets 2020, 31, 952–959. [Google Scholar] [CrossRef]
- Rondina, M.; Voora, D.; Simon, L.; Schwertz, H.; Harper, J.; Lee, O.; Bhatlekar, S.; Li, Q.; Eustes, A.S.; Montenont, E.; et al. Longitudinal RNA-seq Analysis of the Repeatability of Gene Expression and Splicing in Human Platelets Identifies a Platelet SELP Splice QTL. Circ. Res. 2019, 126, 501–516. [Google Scholar] [CrossRef]
- Rowley, J.W.; Schwertz, H.; Weyrich, A.S. Platelet mRNA: The meaning behind the message. Curr. Opin. Hematol. 2012, 19, 385–391. [Google Scholar] [CrossRef]
- Weyrich, A.S.; Lindemann, S.; Tolley, N.D.; Kraiss, L.W.; Dixon, D.A.; Mahoney, T.M.; Prescott, S.M.; McIntyre, T.M.; Zimmerman, G.A. Change in protein phenotype without a nucleus: Translational control in platelets. Semin. Thromb. Hemost. 2004, 30, 493–500. [Google Scholar] [CrossRef] [PubMed]
- Rondina, M.T.; Schwertz, H.; Harris, E.S.; Kraemer, B.F.; Campbell, R.A.; Mackman, N.; Grissom, C.K.; Weyrich, A.S.; Zimmerman, G.A. The septic milieu triggers expression of spliced tissue factor mRNA in human platelets. J. Thromb. Haemost. 2011, 9, 748–758. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Denis, M.M.; Tolley, N.D.; Bunting, M.; Schwertz, H.; Jiang, H.; Lindemann, S.; Yost, C.C.; Rubner, F.J.; Albertine, K.H.; Swoboda, K.J.; et al. Escaping the nuclear confines: Signal-dependent pre-mRNA splicing in anucleate platelets. Cell 2005, 122, 379–391. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Schwertz, H.; Tolley, N.D.; Foulks, J.M.; Denis, M.M.; Risenmay, B.W.; Buerke, M.; Tilley, R.E.; Rondina, M.T.; Harris, E.M.; Kraiss, L.W.; et al. Signal-dependent splicing of tissue factor pre-mRNA modulates the thrombogenecity of human platelets. J. Exp. Med. 2006, 203, 2433–2440. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rowley, J.W.; Chappaz, S.; Corduan, A.; Chong, M.M.; Campbell, R.; Khoury, A.; Manne, B.K.; Wurtzel, J.G.; Michael, J.V.; Goldfinger, L.E.; et al. Dicer1-mediated miRNA processing shapes the mRNA profile and function of murine platelets. Blood 2016, 127, 1743–1751. [Google Scholar] [CrossRef] [Green Version]
- Schwertz, H.; Rowley, J.W.; Schumann, G.G.; Thorack, U.; Campbell, R.A.; Manne, B.K.; Zimmerman, G.A.; Weyrich, A.S.; Rondina, M.T. Endogenous LINE-1 (Long Interspersed Nuclear Element-1) Reverse Transcriptase Activity in Platelets Controls Translational Events Through RNA-DNA Hybrids. Arter. Thromb. Vasc. Biol. 2018, 38, 801–815. [Google Scholar] [CrossRef]
- Schwertz, H.; Rowley, J.W.; Tolley, N.D.; Campbell, R.A.; Weyrich, A.S. Assessing protein synthesis by platelets. Methods Mol. Biol. 2012, 788, 141–153. [Google Scholar]
- Schwertz, H.; Rowley, J.W.; Zimmerman, G.A.; Weyrich, A.S.; Rondina, M.T. Retinoic acid receptor-alpha regulates synthetic events in human platelets. J. Thromb. Haemost. 2017, 15, 2408–2418. [Google Scholar] [CrossRef] [Green Version]
- Ali, F.Y.; Davidson, S.J.; Moraes, L.A.; Traves, S.L.; Paul-Clark, M.; Bishop-Bailey, D.; Warner, T.D.; Mitchell, J.A. Role of nuclear receptor signaling in platelets: Antithrombotic effects of PPARbeta. FASEB J. 2006, 20, 326–328. [Google Scholar] [CrossRef]
- Ray, D.M.; Spinelli, S.L.; Pollock, S.J.; Murant, T.I.; O’Brien, J.J.; Blumberg, N.; Francis, C.W.; Taubman, M.B.; Phipps, R.P. Peroxisome proliferator-activated receptor gamma and retinoid X receptor transcription factors are released from activated human platelets and shed in microparticles. Thromb. Haemost. 2008, 99, 86–95. [Google Scholar]
- Rondina, M.T.; Freitag, M.; Pluthero, F.G.; Kahr, W.H.; Rowley, J.W.; Kraiss, L.W.; Franks, Z.; Zimmerman, G.A.; Weyrich, A.S.; Schwertz, H. Non-genomic activities of retinoic acid receptor alpha control actin cytoskeletal events in human platelets. J. Thromb. Haemost. 2016, 14, 1082–1094. [Google Scholar] [CrossRef] [Green Version]
- Cunin, P.; Bouslama, R.; Machlus, K.R.; Martinez-Bonet, M.; Lee, P.Y.; Wactor, A.; Nelson-Maney, N.; Morris, A.; Guo, L.; Weyrich, A.; et al. Megakaryocyte emperipolesis mediates membrane transfer from intracytoplasmic neutrophils to platelets. eLife 2019, 8, e44031. [Google Scholar] [CrossRef]
- Engelmann, B.; Massberg, S. Thrombosis as an intravascular effector of innate immunity. Nat Rev Immunol 2013, 13, 34–45. [Google Scholar] [CrossRef]
- Guo, L.; Rondina, M.T. The Era of Thromboinflammation: Platelets Are Dynamic Sensors and Effector Cells During Infectious Diseases. Front. Immunol. 2019, 10, 2204. [Google Scholar] [CrossRef] [Green Version]
- Garcia, C.; Compagnon, B.; Poette, M.; Gratacap, M.P.; Lapebie, F.X.; Voisin, S.; Minville, V.; Payrastre, B.; Vardon-Bounes, F.; Ribes, A. Platelet Versus Megakaryocyte: Who Is the Real Bandleader of Thromboinflammation in Sepsis? Cells 2022, 11, 1507. [Google Scholar] [CrossRef]
- D’Atri, L.P.; Rodriguez, C.S.; Miguel, C.P.; Pozner, R.G.; Ortiz Wilczynski, J.M.; Negrotto, S.; Carrera-Silva, E.A.; Heller, P.G.; Schattner, M. Activation of toll-like receptors 2 and 4 on CD34(+) cells increases human megakaryo/thrombopoiesis induced by thrombopoietin. J. Thromb. Haemost. 2019, 17, 2196–2210. [Google Scholar] [CrossRef]
- Rondina, M.T.; Carlisle, M.; Fraughton, T.; Brown, S.M.; Miller, R.R., 3rd; Harris, E.S.; Weyrich, A.S.; Zimmerman, G.A.; Supiano, M.A.; Grissom, C.K. Platelet-monocyte aggregate formation and mortality risk in older patients with severe sepsis and septic shock. J. Gerontol. Ser. A Biol. Sci. Med. Sci. 2015, 70, 225–231. [Google Scholar] [CrossRef] [Green Version]
- Venkata, C.; Kashyap, R.; Farmer, J.C.; Afessa, B. Thrombocytopenia in adult patients with sepsis: Incidence, risk factors, and its association with clinical outcome. J. Intensive Care 2013, 1, 9. [Google Scholar] [CrossRef]
- Yaguchi, A.; Lobo, F.L.; Vincent, J.L.; Pradier, O. Platelet function in sepsis. J. Thromb. Haemost. 2004, 2, 2096–2102. [Google Scholar] [CrossRef]
- Ishimi, Y.; Hirosumi, J.; Sato, W.; Sugasawa, K.; Yokota, S.; Hanaoka, F.; Yamada, M. Purification and initial characterization of a protein which facilitates assembly of nucleosome-like structure from mammalian cells. Eur. J. Biochem. 1984, 142, 431–439. [Google Scholar] [CrossRef]
- Zlatanova, J.; Seebart, C.; Tomschik, M. Nap1: Taking a closer look at a juggler protein of extraordinary skills. FASEB J. 2007, 21, 1294–1310. [Google Scholar] [CrossRef] [PubMed]
- Yan, Y.; Yin, P.; Gong, H.; Xue, Y.; Zhang, G.; Fang, B.; Chen, Z.; Li, Y.; Yang, C.; Huang, Z.; et al. Nucleosome Assembly Protein 1-Like 1 (Nap1l1) Regulates the Proliferation of Murine Induced Pluripotent Stem Cells. Cell Physiol. Biochem. 2016, 38, 340–350. [Google Scholar] [CrossRef] [PubMed]
- Okuwaki, M.; Kato, K.; Nagata, K. Functional characterization of human nucleosome assembly protein 1-like proteins as histone chaperones. Genes Cells 2010, 15, 13–27. [Google Scholar] [CrossRef] [PubMed]
- Yip, M.C.J.; Sedor, S.F.; Shao, S. Mechanism of client selection by the protein quality-control factor UBE2O. Nat. Struct. Mol. Biol. 2022, 29, 774–780. [Google Scholar] [CrossRef] [PubMed]
- Liang, X.; Tang, Z.; Zhang, Y.; Sun, Y.; Wang, J. NAP1L1 promotes the growth of colon cancer by activating HDGF/DDX5. Acta Biochim. Biophys. Sin. 2022. [Google Scholar] [CrossRef]
- Shen, B.; Zhu, W.; Liu, X.; Jiang, J. NAP1L1 Functions as a Novel Prognostic Biomarker Associated with Macrophages and Promotes Tumor Progression by Influencing the Wnt/beta-Catenin Pathway in Hepatocellular Carcinoma. Front. Genet. 2022, 13, 876253. [Google Scholar] [CrossRef]
- Xiaohua, Z.; Xie, Y.; Huang, W.; Chen, Z.; Guo, S. NAP1L1 promotes tumor proliferation through HDGF/C-JUN signaling in ovarian cancer. BMC Cancer 2022, 22, 339. [Google Scholar] [CrossRef]
- Gan, H.; Xu, X.; Bai, Y. Trametes robiniophila represses angiogenesis and tumor growth of lung cancer via strengthening let-7d-5p and targeting NAP1L1. Bioengineered 2022, 13, 6698–6710. [Google Scholar] [CrossRef]
- Rowley, J.W.; Oler, A.J.; Tolley, N.D.; Hunter, B.N.; Low, E.N.; Nix, D.A.; Yost, C.C.; Zimmerman, G.A.; Weyrich, A.S. Genome-wide RNA-seq analysis of human and mouse platelet transcriptomes. Blood 2011, 118, e101–e111. [Google Scholar] [CrossRef] [Green Version]
- De Boer, V.C.; Houten, S.M. A mitochondrial expatriate: Nuclear pyruvate dehydrogenase. Cell 2014, 158, 9–10. [Google Scholar] [CrossRef] [Green Version]
- Sutendra, G.; Kinnaird, A.; Dromparis, P.; Paulin, R.; Stenson, T.H.; Haromy, A.; Hashimoto, K.; Zhang, N.; Flaim, E.; Michelakis, E.D. A nuclear pyruvate dehydrogenase complex is important for the generation of acetyl-CoA and histone acetylation. Cell 2014, 158, 84–97. [Google Scholar] [CrossRef] [Green Version]
- Colapietro, F.; Lleo, A.; Generali, E. Antimitochondrial Antibodies: From Bench to Bedside. Clin. Rev. Allergy Immunol. 2022, 63, 166–177. [Google Scholar] [CrossRef]
- Mao, T.K.; Davis, P.A.; Odin, J.A.; Coppel, R.L.; Gershwin, M.E. Sidechain biology and the immunogenicity of PDC-E2, the major autoantigen of primary biliary cirrhosis. Hepatology 2004, 40, 1241–1248. [Google Scholar] [CrossRef] [Green Version]
- Park, Y.J.; Luger, K. Structure and function of nucleosome assembly proteins. Biochem. Cell Biol. 2006, 84, 549–558. [Google Scholar] [CrossRef]
- Park, Y.J.; Luger, K. The structure of nucleosome assembly protein 1. Proc. Natl. Acad. Sci. USA 2006, 103, 1248–1253. [Google Scholar] [CrossRef] [Green Version]
- Okada, M.; Hozumi, Y.; Ichimura, T.; Tanaka, T.; Hasegawa, H.; Yamamoto, M.; Takahashi, N.; Iseki, K.; Yagisawa, H.; Shinkawa, T.; et al. Interaction of nucleosome assembly proteins abolishes nuclear localization of DGKzeta by attenuating its association with importins. Exp. Cell Res. 2011, 317, 2853–2863. [Google Scholar] [CrossRef]
- Strub, A.; Lim, J.H.; Pfanner, N.; Voos, W. The mitochondrial protein import motor. Biol. Chem. 2000, 381, 943–949. [Google Scholar] [CrossRef]
- McCall, C.E.; Zhu, X.; Zabalawi, M.; Long, D.; Quinn, M.A.; Yoza, B.K.; Stacpoole, P.W.; Vachharajani, V. Sepsis, pyruvate, and mitochondria energy supply chain shortage. J. Leukoc. Biol. 2022. [Google Scholar] [CrossRef]
- Shimada, B.K.; Boyman, L.; Huang, W.; Zhu, J.; Yang, Y.; Chen, F.; Kane, M.A.; Yadava, N.; Zou, L.; Lederer, W.J.; et al. Pyruvate-Driven Oxidative Phosphorylation is Downregulated in Sepsis-Induced Cardiomyopathy: A Study of Mitochondrial Proteome. Shock 2022, 57, 553–564. [Google Scholar] [CrossRef]
- Schwertz, H.; Rowley, J.W.; Portier, I.; Middleton, E.A.; Tolley, N.D.; Campbell, R.A.; Eustes, A.S.; Chen, K.; Rondina, M.T. Human platelets display dysregulated sepsis-associated autophagy, induced by altered LC3 protein-protein interaction of the Vici-protein EPG5. Autophagy 2021, 18, 1534–1550. [Google Scholar] [CrossRef]
- Manne, B.K.; Bhatlekar, S.; Middleton, E.A.; Weyrich, A.S.; Borst, O.; Rondina, M.T. Phospho-inositide-dependent kinase 1 regulates signal dependent translation in megakaryocytes and platelets. J. Thromb. Haemost. 2020, 18, 1183–1196. [Google Scholar] [CrossRef] [PubMed]
- Montenont, E.; Bhatlekar, S.; Jacob, S.; Kosaka, Y.; Manne, B.K.; Lee, O.; Parra-Izquierdo, I.; Tugolukova, E.; Tolley, N.D.; Rondina, M.T.; et al. CRISPR-edited megakaryocytes for rapid screening of platelet gene functions. Blood Adv. 2021, 5, 2362–2374. [Google Scholar] [CrossRef] [PubMed]
- Pendaries, C.; Watson, S.P.; Spalton, J.C. Methods for genetic modification of megakaryocytes and platelets. Platelets 2007, 18, 393–408. [Google Scholar] [CrossRef]
- Koupenova, M.; Livada, A.C.; Morrell, C.N. Platelet and Megakaryocyte Roles in Innate and Adaptive Immunity. Circ. Res. 2022, 130, 288–308. [Google Scholar] [CrossRef] [PubMed]
- Lindemann, S.; McIntyre, T.M.; Prescott, S.M.; Zimmerman, G.A.; Weyrich, A.S. Platelet Signal-Dependent Protein Synthesis. In Platelet Function: Assessment, Diagnosis, and Treatment; Fitzgerald, D.J., Quinn, M., Eds.; The Humana Press Inc.: Totowa, NJ, USA, 2005; pp. 151–176. [Google Scholar]
- Schwertz, H.; Koster, S.; Kahr, W.H.; Michetti, N.; Kraemer, B.F.; Weitz, D.A.; Blaylock, R.C.; Kraiss, L.W.; Greinacher, A.; Zimmerman, G.A.; et al. Anucleate platelets generate progeny. Blood 2010, 115, 3801–3809. [Google Scholar] [CrossRef]
- Schwertz, H.; Rondina, M.T. Platelets and their Microparticles go hand in hand. Thromb. Res. 2018, 168, 164–165. [Google Scholar] [CrossRef]
- Qureshi, A.H.; Chaoji, V.; Maiguel, D.; Faridi, M.H.; Barth, C.J.; Salem, S.M.; Singhal, M.; Stoub, D.; Krastins, B.; Ogihara, M.; et al. Proteomic and phospho-proteomic profile of human platelets in basal, resting state: Insights into integrin signaling. PLoS ONE 2009, 4, e7627. [Google Scholar] [CrossRef] [Green Version]
- Bishop-Bailey, D. The platelet as a model system for the acute actions of nuclear receptors. Steroids 2010, 75, 570–575. [Google Scholar] [CrossRef]
- Osman, A.; Hitzler, W.E.; Ameur, A.; Provost, P. Differential Expression Analysis by RNA-Seq Reveals Perturbations in the Platelet mRNA Transcriptome Triggered by Pathogen Reduction Systems. PLoS ONE 2015, 10, e0133070. [Google Scholar] [CrossRef] [Green Version]
- Miller, K.E.; Heald, R. Glutamylation of Nap1 modulates histone H1 dynamics and chromosome condensation in Xenopus. J. Cell Biol. 2015, 209, 211–220. [Google Scholar] [CrossRef] [Green Version]
- Simon, H.U.; Mills, G.B.; Kozlowski, M.; Hogg, D.; Branch, D.; Ishimi, Y.; Siminovitch, K.A. Molecular characterization of hNRP, a cDNA encoding a human nucleosome-assembly-protein-I-related gene product involved in the induction of cell proliferation. Biochem. J. 1994, 297 Pt 2, 389–397. [Google Scholar] [CrossRef] [Green Version]
- Clark, J.; Alvarez, D.F.; Alexeyev, M.; King, J.A.; Huang, L.; Yoder, M.C.; Stevens, T. Regulatory role for nucleosome assembly protein-1 in the proliferative and vasculogenic phenotype of pulmonary endothelium. Am. J. Physiol. Lung. Cell Mol. Physiol. 2008, 294, L431–L439. [Google Scholar] [CrossRef]
- Regnard, C.; Desbruyeres, E.; Huet, J.C.; Beauvallet, C.; Pernollet, J.C.; Edde, B. Polyglutamylation of nucleosome assembly proteins. J. Biol. Chem. 2000, 275, 15969–15976. [Google Scholar] [CrossRef] [Green Version]
- Van Dijk, J.; Miro, J.; Strub, J.M.; Lacroix, B.; van Dorsselaer, A.; Edde, B.; Janke, C. Polyglutamylation is a post-translational modification with a broad range of substrates. J. Biol. Chem. 2008, 283, 3915–3922. [Google Scholar] [CrossRef] [Green Version]
- Ye, B.; Li, C.; Yang, Z.; Wang, Y.; Hao, J.; Wang, L.; Li, Y.; Du, Y.; Hao, L.; Liu, B.; et al. Cytosolic carboxypeptidase CCP6 is required for megakaryopoiesis by modulating Mad2 polyglutamylation. J. Exp. Med. 2014, 211, 2439–2454. [Google Scholar] [CrossRef] [Green Version]
- Matsuda, S.; Adachi, J.; Ihara, M.; Tanuma, N.; Shima, H.; Kakizuka, A.; Ikura, M.; Ikura, T.; Matsuda, T. Nuclear pyruvate kinase M2 complex serves as a transcriptional coactivator of arylhydrocarbon receptor. Nucleic Acids Res. 2016, 44, 636–647. [Google Scholar] [CrossRef] [Green Version]
- Chueh, F.Y.; Leong, K.F.; Cronk, R.J.; Venkitachalam, S.; Pabich, S.; Yu, C.L. Nuclear localization of pyruvate dehydrogenase complex-E2 (PDC-E2), a mitochondrial enzyme, and its role in signal transducer and activator of transcription 5 (STAT5)-dependent gene transcription. Cell Signal. 2011, 23, 1170–1178. [Google Scholar] [CrossRef] [Green Version]
- Thekkumkara, T.J.; Ho, L.; Wexler, I.D.; Pons, G.; Liu, T.C.; Patel, M.S. Nucleotide sequence of a cDNA for the dihydrolipoamide acetyltransferase component of human pyruvate dehydrogenase complex. FEBS Lett. 1988, 240, 45–48. [Google Scholar] [CrossRef] [Green Version]
- Wang, L.; Kaneko, S.; Kagaya, M.; Ohno, H.; Honda, M.; Kobayashi, K. Molecular cloning, and characterization and expression of dihydrolipoamide acetyltransferase component of murine pyruvate dehydrogenase complex in bile duct cancer cells. J. Gastroenterol. 2002, 37, 449–454. [Google Scholar] [CrossRef] [Green Version]
- Stelzl, U.; Worm, U.; Lalowski, M.; Haenig, C.; Brembeck, F.H.; Goehler, H.; Stroedicke, M.; Zenkner, M.; Schoenherr, A.; Koeppen, S.; et al. A human protein-protein interaction network: A resource for annotating the proteome. Cell 2005, 122, 957–968. [Google Scholar] [CrossRef] [Green Version]
- Arulkumaran, N.; Deutschman, C.S.; Pinsky, M.R.; Zuckerbraun, B.; Schumacker, P.T.; Gomez, H.; Gomez, A.; Murray, P.; Kellum, J.A.; Workgroup, A.X. Mitochondrial Function in Sepsis. Shock 2016, 45, 271–281. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nayler, W.G.; Panagiotopoulos, S.; Elz, J.S.; Daly, M.J. Calcium-mediated damage during post-ischaemic reperfusion. J. Mol. Cell Cardiol. 1988, 20 (Suppl. 2), 41–54. [Google Scholar] [CrossRef] [PubMed]
- Mao, L.; Sun, M.; Chen, Z.; Zeng, Z.; Wu, J.; Chen, Z.; Zhang, W.; Huang, Q. The Pyruvate Dehydrogenase Complex Mitigates LPS-Induced Endothelial Barrier Dysfunction by Metabolic Regulation. Shock 2022, 57, 308–317. [Google Scholar] [CrossRef] [PubMed]
- Zeng, Z.; Huang, Q.; Mao, L.; Wu, J.; An, S.; Chen, Z.; Zhang, W. The Pyruvate Dehydrogenase Complex in Sepsis: Metabolic Regulation and Targeted Therapy. Front. Nutr. 2021, 8, 783164. [Google Scholar] [CrossRef]
- Puskarich, M.A.; Kline, J.A.; Watts, J.A.; Shirey, K.; Hosler, J.; Jones, A.E. Early alterations in platelet mitochondrial function are associated with survival and organ failure in patients with septic shock. J. Crit. Care 2016, 31, 63–67. [Google Scholar] [CrossRef] [Green Version]
- Sjovall, F.; Morota, S.; Hansson, M.J.; Friberg, H.; Gnaiger, E.; Elmer, E. Temporal increase of platelet mitochondrial respiration is negatively associated with clinical outcome in patients with sepsis. Crit. Care 2010, 14, R214. [Google Scholar] [CrossRef] [Green Version]
- McCann, M.R.; McHugh, C.E.; Kirby, M.; Jennaro, T.S.; Jones, A.E.; Stringer, K.A.; Puskarich, M.A. A Multivariate Metabolomics Method for Estimating Platelet Mitochondrial Oxygen Consumption Rates in Patients with Sepsis. Metabolites 2020, 10, 139. [Google Scholar] [CrossRef] [Green Version]
- Bauer, N.C.; Doetsch, P.W.; Corbett, A.H. Mechanisms Regulating Protein Localization. Traffic 2015, 16, 1039–1061. [Google Scholar] [CrossRef] [Green Version]
- Munford, R.S. Severe sepsis and septic shock: The role of gram-negative bacteremia. Annu. Rev. Pathol. 2006, 1, 467–496. [Google Scholar] [CrossRef]
- Assinger, A.; Schrottmaier, W.C.; Salzmann, M.; Rayes, J. Platelets in Sepsis: An Update on Experimental Models and Clinical Data. Front. Immunol. 2019, 10, 1687. [Google Scholar] [CrossRef]
- Koyama, K.; Katayama, S.; Muronoi, T.; Tonai, K.; Goto, Y.; Koinuma, T.; Shima, J.; Nunomiya, S. Time course of immature platelet count and its relation to thrombocytopenia and mortality in patients with sepsis. PLoS ONE 2018, 13, e0192064. [Google Scholar] [CrossRef] [Green Version]
- Cataldo, L.M.; Zhang, Y.; Lu, J.; Ravid, K. Rat NAP1: cDNA cloning and upregulation by Mpl ligand. Gene 1999, 226, 355–364. [Google Scholar] [CrossRef]
- Dellinger, R.P.; Levy, M.M.; Carlet, J.M.; Bion, J.; Parker, M.M.; Jaeschke, R.; Reinhart, K.; Angus, D.C.; Brun-Buisson, C.; Beale, R.; et al. Surviving Sepsis Campaign: International guidelines for management of severe sepsis and septic shock: 2008. Crit. Care Med. 2008, 36, 296–327. [Google Scholar] [CrossRef] [Green Version]
- Kahr, W.H.; Hinckley, J.; Li, L.; Schwertz, H.; Christensen, H.; Rowley, J.W.; Pluthero, F.G.; Urban, D.; Fabbro, S.; Nixon, B.; et al. Mutations in NBEAL2, encoding a BEACH protein, cause gray platelet syndrome. Nat. Genet. 2011, 43, 738–740. [Google Scholar] [CrossRef]
- Jones, C.A.; London, N.R.; Chen, H.; Park, K.W.; Sauvaget, D.; Stockton, R.A.; Wythe, J.D.; Suh, W.; Larrieu-Lahargue, F.; Mukouyama, Y.S.; et al. Robo4 stabilizes the vascular network by inhibiting pathologic angiogenesis and endothelial hyperpermeability. Nat. Med. 2008, 14, 448–453. [Google Scholar] [CrossRef] [Green Version]
- Eng, J.K.; McCormack, A.L.; Yates, J.R. An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database. J. Am. Soc. Mass Spectrom. 1994, 5, 976–989. [Google Scholar] [CrossRef] [Green Version]
- Keller, A.; Nesvizhskii, A.I.; Kolker, E.; Aebersold, R. Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal. Chem. 2002, 74, 5383–5392. [Google Scholar] [CrossRef]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Freitag, M.; Schwertz, H. A New Role of NAP1L1 in Megakaryocytes and Human Platelets. Int. J. Mol. Sci. 2022, 23, 14694. https://doi.org/10.3390/ijms232314694
Freitag M, Schwertz H. A New Role of NAP1L1 in Megakaryocytes and Human Platelets. International Journal of Molecular Sciences. 2022; 23(23):14694. https://doi.org/10.3390/ijms232314694
Chicago/Turabian StyleFreitag, Martin, and Hansjörg Schwertz. 2022. "A New Role of NAP1L1 in Megakaryocytes and Human Platelets" International Journal of Molecular Sciences 23, no. 23: 14694. https://doi.org/10.3390/ijms232314694