Inflammatory stimuli induce inhibitory S-nitrosylation of the deacetylase SIRT1 to increase acetylation and activation of p53 and p65

Science Signaling

Volumn 7, Issue 351, 2014, Pages

  Shinozaki, Shohei ^a,b   Chang, Kyungho ^a,c   Sakai, Michihiro ^a   Shimizu, Nobuyuki ^a   Yamada, Marina ^a   Tanaka, Tomokazu ^a   Nakazawa, Harumasa ^a   Ichinose, Fumito ^a   Yamada, Yoshitsugu ^c   Ishigami, Akihito ^d   Ito, Hideki ^d   Ouchi, Yasuyoshi ^c,e   Starr, Marlene E ^f   Saito, Hiroshi ^f   Shimokado, Kentaro ^b   Stamler, Jonathan S ^g   Kaneki, Masao ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

^d TOKYO METROPOLITAN INSTITUTE OF GERONTOLOGY   (Japan)

^e TORANOMON HOSPITAL   (Japan)

^f UNIVERSITY OF KENTUCKY   (United States)

^g CASE WESTERN RESERVE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; CYCLIC GMP; GLUTATHIONE DISULFIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; PROTEIN P53; TRANSCRIPTION FACTOR RELA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; NITROGEN; RELA PROTEIN, HUMAN; RELA PROTEIN, MOUSE; RELA PROTEIN, RAT; SIRT1 PROTEIN, HUMAN; SIRT1 PROTEIN, MOUSE; SIRT1 PROTEIN, RAT; SIRTUIN 1; TP53 PROTEIN, HUMAN;

ACETYLATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL DEATH; CONTROLLED STUDY; DEACETYLATION; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME INHIBITION; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; INFLAMMATION; MAMMAL CELL; MOUSE; NITROSYLATION; NONHUMAN; OXIDATIVE STRESS; PROTEIN MOTIF; RAT; AMINO ACID SEQUENCE; ANIMAL; C57BL MOUSE; CHEMISTRY; CHLOROCEBUS AETHIOPS; COS 1 CELL LINE; DISEASE MODEL; FISCHER 344 RAT; MALE; METABOLISM; MOLECULAR GENETICS; SEQUENCE HOMOLOGY;

ACETYLATION; AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; APOPTOSIS; CERCOPITHECUS AETHIOPS; COS CELLS; DISEASE MODELS, ANIMAL; HUMANS; INFLAMMATION; MALE; MICE; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; NF-KAPPA B; NITROGEN; OXIDATIVE STRESS; RATS; RATS, INBRED F344; SEQUENCE HOMOLOGY, AMINO ACID; SIRTUIN 1; TRANSCRIPTION FACTOR RELA; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84910624272     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2005375     Document Type: Article

References (102)

1. S. Di Marco, R. Mazroui, P. Dallaire, S. Chittur, S. A. Tenenbaum, D. Radzioch, A. Marette, I. E. Gallouzi, NF-κB-mediated MyoD decay during muscle wasting requires nitric oxide synthase mRNA stabilization, HuR protein, and nitric oxide release. Mol. Cell. Biol. 25, 6533-6545 (2005).
2. D. T. Hall, J. F. Ma, S. D. Marco, I. E. Gallouzi, Inducible nitric oxide synthase (iNOS) in muscle wasting syndrome, sarcopenia, and cachexia. Aging 3, 702-715 (2011).
3. D. Cai, M. Yuan, D. F. Frantz, P. A. Melendez, L. Hansen, J. Lee, S. E. Shoelson, Local and systemic insulin resistance resulting from hepatic activation of IKK-β and NF-κB. Nat. Med. 11, 183-190 (2005).
4. W. Duan, X. Zhu, B. Ladenheim, Q. S. Yu, Z. Guo, J. Oyler, R. G. Cutler, J. L Cadet, N. H. Greig, M. P. Mattson, p53 inhibitors preserve dopamine neurons and motor function in experimental parkinsonism. Ann. Neurol. 52, 597-606 (2002).
5. L Connelly, M. Palacios-Callender, C. Ameixa, S. Moncada, A. J. Hobbs, Biphasic regulation of NF-κB activity underlies the pro- and anti-inflammatory actions of nitric oxide. J. Immunol. 166, 3873-3881 (2001).
6. K. Katsuyama, M. Shichiri, F. Marumo, Y. Hirata, NO inhibits cytokine-induced iNOS expression and NF-κB activation by interfering with phosphorylation and degradation of κB-α. Arterioscler. Thromb. Vasc. Biol. 18, 1796-1802 (1998).
7. Z. T. Kelleher, A. Matsumoto, J. S. Stamler, H. E. Marshall, NOS2 regulation of NF-κB by S-nitrosylation of p65. J. Biol. Chem. 282, 30667-30672 (2007).
8. H. E. Marshall, J. S. Stamler, Inhibition of NF-κB by S-nitrosylation. Biochemistry 40, 1688-1693 (2001).
9. C. M. Schonhoff, M. C. Daou, S. N. Jones, C. A. Schiffer, A. H. Ross, Nitric oxide-mediated inhibition of Hdm2-p53 binding. Biochemistry 41, 13570-13574 (2002).
10. N. Shahani, A. Sawa, Nitric oxide signaling and nitrosative stress in neurons: Role for S-nitrosylation. Antioxid. Redox Signal. 14, 1493-1504 (2011).
11. S. Imai, C. M. Armstrong, M. Kaeberlein, L Guarente, Transcriptional silencing and longevity protein Sir2 is an NAD-dependent histone deacetylase. Nature 403, 795-800 (2000).
12. D. Moazed, Enzymatic activities of Sir2 and chromatin silencing. Curr. Opin. Cell Biol. 13, 232-238 (2001).
13. J. R. Delaney, G. L Sutphin, B. Duiken, S. Sim, J. R. Kim, B. Robison, J. Schleit, C. J. Murakami, D. Carr, E. H. An, E. Choi, A. Chou, M. Fletcher, M. Jelic, B. Liu, D. Lockshon, R. M. Moller, D. N. Pak, Q. Peng, Z. J. Peng, K. M. Pham, M. Sage, A. Solanky, K. K. Steffen, M. Tsuchiya, S. Tsuchiyama, S. Johnson, C. Raabe, Y. Suh, Z. Zhou, X. Liu, B. K. Kennedy, M. Kaeberlein, Sir2 deletion prevents lifespan extension in 32 long-lived mutants. Aging Cell 10, 1089-1091 (2011).
14. J. Chen, Y. Zhou, S. Mueller-Steiner, L F. Chen, H. Kwon, S. Yi, L Mucke, L Gan, SIRT1 protects against microglia-dependent amyloid-β toxicity through inhibiting NF-κB signaling. J. Biol. Chem. 280, 40364-40374 (2005).
15. E. Langley, M. Pearson, M. Faretta, U. M. Bauer, R. A. Frye, S. Minucci, P. G. Pelicci, T. Kouzarides, Human SIR2 deacetylates p53 and antagonizes PML/p53-induced cellular senescence. EMBO J. 21, 2383-2396 (2002).
16. J. Luo, A. Y. Nikolaev, S. Imai, D. Chen, F. Su, A. Shiloh, L. Guarente, W. Gu, Negative control of p53 by Sir2a promotes cell survival under stress. Cell 107, 137-148 (2001).
17. SIRT1 functions as an NAD-dependent p53 deacetylase. Cell 107, 149-159 (2001).
18. F. Yeung, J. E. Hoberg, C. S. Ramsey, M. D. Keller, D. R. Jones, R. A. Frye, M. W. Mayo, Modulation of NF-κB-dependent transcription and cell survival by the SIRT1 deacetylase. EMBO J. 23, 2369-2380 (2004).
19. A. S. Banks, N. Kon, C. Knight, M. Matsumoto, R. Gutiérrez-Juárez, L. Rossetti, W. Gu, D. Accili, SirT1 gain of function increases energy efficiency and prevents diabetes in mice. Cell. Metab. 8, 333-341 (2008).
20. G. Donmez, D. Wang, D. E. Cohen, L Guarente, SIRT1 suppresses β-amyloid production by activating the a-secretase gene ADAM10. Cell 142, 320-332 (2010).
21. D. Lee, A. L Goldberg, SIRT1 protein, by blocking the activities of transcription factors FoxOI and Fox03, inhibits muscle atrophy and promotes muscle growth. J. Biol. Chem. 288,30515-30526(2013).
22. R. H. Wang, H. S. Kim, C. Xiao, X Xu, O. Gavrilova, C. X Deng, Hepatic Sirtl deficiency in mice impairs mTorc2/Akt signaling and results in hyperglycemia, oxidative damage, and insulin resistance. J. Clin. Invest. 121, 4477-4490 (2011).
23. Y Li, S. Xu, A. Giles, K. Nakamura, J. W. Lee, X. Hou, G. Donmez, J. Li, Z. Luo, K. Walsh, L Guarente, M. Zang, Hepatic overexpression of SIRT1 in mice attenuates endoplasmic reticulum stress and insulin resistance in the liver. FASEB J. 25,1664-1679 (2011).
24. L Luu, F. F. Dai, K. J. Prentice, X Huang, A. B. Hardy, J. B. Hansen, Y Liu, J. W. Joseph, M. B. Wheeler, The loss of Sirtl in mouse pancreatic beta cells impairs insulin secretion by disrupting glucose sensing. Diabetologia 56, 2010-2020 (2013).
25. J. T. Rodgers, C. Lerin, W. Haas, S. P. Gygi, B. M. Spiegelman, P. Puigserver, Nutrient control of glucose homeostasis through a complex of PGC-1α and SIRT1. Nature 434, 113-118(2005).
26. A. Ito, Y. Kawaguchi, C. H. Lai, J. J. Kovacs, Y. Higashimoto, E. Appella, T. P. Yao, MDM2-HDAC1-mediated deacetylation of p53 is required for its degradation. EMBO J. 21, 6236-6245 (2002).
27. Y. Liu, P. W. Smith, D. R. Jones, Breast cancer metastasis suppressor 1 functions as a corepressor by enhancing histone deacetylase 1-mediated deacetylation of RelA/p65 and promoting apoptosis. Mol. Cell. Biol. 26, 8683-8696 (2006).
28. M. D. Kornberg, N. Sen, M. R. Hara, K. R. Juluri, J. V. Nguyen, A. M. Snowman, L Law, L D. Hester, S. H. Snyder, GAPDH mediates nitrosylation of nuclear proteins. Nat. Cell Boll. 12, 1094-1100 (2010).
29. M. H. Lee, M. H. Jang, E. K. Kim, S. W. Han, S. Y. Cho, C. J. Kim, Nitric oxide induces apoptosis in mouse C2C12 myoblast cells. J. Pharmacol. Sci. 97, 369-376 (2005).
30. U. K. Messmer, B. Brüne, Nitric oxide-induced apoptosis: p53-dependent and p53-independent signalling pathways. Biochem. J. 319, 299-305 (1996).
31. Q. W. Xie, Y. Kashiwabara, C. Nathan, Role of transcription factor NF-κB/Rel in induction of nitric oxide synthase. J. Biol. Chem. 269, 4705-4708 (1994).
32. R. A. Skidgel, X. P. Gao, V. Brovkovych, A. Rahman, D. Jho, S. Predescu, T. J. Standiford, A. B. Malik, Nitric oxide stimulates macrophage inflammatory protein-2 expression in sepsis. J. Immunol. 169, 2093-2101 (2002).
33. S. Cuzzocrea, P. K. Chatterjee, E. Mazzon, L Dugo, A. De Sarro, F. A. Van de Loo, A. P. Caputi, C. Thiemermann, Role of induced nitric oxide in the initiation of the inflammatory response after postischemic injury. Shock 18, 169-176 (2002).
34. C. Hierholzer, J. C. Kalff, T. R. Billiar, A. J. Bauer, D. J. Tweardy, B. G. Harbrecht, Induced nitric oxide promotes intestinal inflammation following hemorrhagic shock. Am. J. Physiol. Gastrointest. Liver Physiol. 286, G225-G233 (2004).
35. K. Katada, A. Bihari, A. Badhwar, N. Yoshida, T. Yoshikawa, R. F. Potter, G. Cepinskas, Hindlimb ischemia/reperfusion-induced remote injury to the small intestine: Role of inducible nitric-oxide synthase-derived nitric oxide. J. Pharmacol. Exp. Ther. 329, 919-927 (2009).
36. D. Cai, J. D. Frantz, N. E. Tawa Jr., P. A. Melendez, B. C. Oh, H. G. Lidov, P. O. Hasselgren, W. R. Frontera, J. Lee, D. J. Glass, S. E. Shoelson, IKKβ/NF-κB activation causes severe muscle wasting in mice. Cell 119, 285-298 (2004).
37. L. Chung, Y. C. Ng, Age-related alterations in expression of apoptosis regulatory proteins and heat shock proteins in rat skeletal muscle. Biochim. Biophys. Acta 1762, 103-109 (2006).
38. C. A. da Costa, C. Sunyach, E. Giaime, A. West, O. Corti, A. Brice, S. Safe, P. M. Abou-Sleiman, N. W. Wood, H. Takahashi, M. S. Goldberg, J. Shen, F. Checler, Transcriptional repression of p53 by parkin and impairment by mutations associated with autosomal recessive juvenile Parkinson's disease. Nat Cell Biol. 11, 1370-1375 (2009).
39. R. Dajani, S. Sanlioglu, Y. Zhang, Q. Li, M. M. Monick, E. Lazartigues, T. Eggleston, R. L Davisson, G. W. Hunninghake, J. F. Engelhardt, Pleiotropic functions of TNF-α determine distinct IKKβ-dependent hepatocellular fates in response to LPS. Am. J. Physiol. Gastrointest. Liver Physiol. 292, G242-G252 (2007).
40. R. Guler, M. L Olleros, D. Vesin, R. Parapanov, C. Vesin, S. Kantengwa, L Rubbia-Brandt, N. Mensi, A. Angelillo-Scherrer, E. Martinez-Soria, F. Tacchini-Cottier, I. Garcia, Inhibition of inducible nitric oxide synthase protects against liver injury induced by mycobacterial infection and endotoxins. J. Hepatol. 41, 773-781 (2004).
41. P. Hantraye, E. Brouillet, R. Ferrante, S. Palfi, R. Dolan, R. T. Matthews, M. F. Beal, Inhibition of neuronal nitric oxide synthase prevents MPTP-induced parkinsonism in baboons. Nat. Med. 2, 1017-1021 (1996).
42. G. T. Liberatore, V. Jackson-Lewis, S. Vukosavic, A. S. Mandir, M. Vila, W. G. McAuliffe, V. L. Dawson, T. M. Dawson, S. Przedborski, Inducible nitric oxide synthase stimulates dopaminergic neurodegeneration in the MPTP model of Parkinson disease. Nat. Med. 5, 1403-1409(1999).
43. T. H. Liu, E. K. Robinson, K. S. Helmer, S. D. West, A. A. Castaneda, L Chang, D. W. Mercer, Does upregulation of inducible nitric oxide synthase play a role in hepatic injury? Shock 18, 549-554 (2002).
44. I. Ogushi, Y. limuro, E. Seki, G. Son, T. Hirano, T. Hada, H. Tsutsui, K. Nakanishi, R. Morishita, Y. Kaneda, J. Fujimoto, Nuclear factor KB decoy oligodeoxynucleotides prevent endotoxin-induced fatal liver failure in a murine model. Hepatology 38,335-344 (2003).
45. S. Przedborski, V Jackson-Lewis, R. Yokoyama, T. Shibata, V L Dawson, T. M. Dawson, Role of neuronal nitric oxide in 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)-induced dopaminergic neurotoxicity. Proc. Natl. Acad. Sci. U.S.A. 93, 4565-4571 (1996).
46. T. Schäfer, C. Scheuer, K. Roemer, M. D. Menger, B. Vollmar, Inhibition of p53 protects liver tissue against endotoxin-induced apoptotic and necrotic cell death. FASEB J. 17, 660-667 (2003).
47. M. Schwarzkopf, D. Coletti, D. Sassoon, G. Marazzi, Muscle cachexia is regulated by a p53-PW1/Peg3-dependent pathway. Genes Dev. 20, 3440-3452 (2006).
48. M. Bar-Shai, E. Carmeli, A. Z. Reznick, The role of NF-κB in protein breakdown in immobilization, aging, and exercise: From basic processes to promotion of health. Ann. N. Y. Acad. Sci. 1057, 431-447 (2005).
49. M. Kaneki, N. Shimizu, D. Yamada, K. Chang, Nitrosative stress and pathogenesis of insulin resistance. Antioxid. Redox Signal. 9, 319-329 (2007).
50. P. C. Kuo, K. Y. Abe, R. A. Schroeder, Oxidative stress increases hepatocyte iNOS gene transcription and promoter activity. Biochem. Biophys. Res. Commun. 234, 289-292(1997).
51. T. Nakamura, S. A. Lipton, Molecular mechanisms of nitrosative stress-mediated protein misfolding in neurodegenerative diseases. Cell. Mol. Life Sci. 64, 1609-1620 (2007).
52. M. T. Forrester, M. W. Foster, J. S. Stamler, Assessment and application of the biotin switch technique for examining protein S-nitrosylation under conditions of pharmacologically induced oxidative stress. J. Biol. Chem. 282, 13977-13983 (2007).
53. T. Yasukawa, E. Tokunaga, H. Ota, H. Sugita, J. A. Martyn, M. Kaneki, S-nitrosylation-dependent inactivation of Akt/protein kinase B in insulin resistance. J. Biol. Chem. 280, 7511-7518(2005).
54. L Eklöw, P. Moldéus, S. Orrenius, Oxidation of glutathione during hydroperoxide metabolism. A study using isolated hepatocytes and the glutathione reductase inhibitor 1,3-bis(2-chloroethyl)-1-nitrosourea. Eur. J. Biochem. 138, 459-463 (1984).
55. S. R. Jaffrey, H. Erdjument-Bromage, C. D. Ferris, P. Tempst, S. H. Snyder, Protein S-nitrosylation: A physiological signal for neuronal nitric oxide. Nat. Cell Biol. 3,193-197 (2001).
56. B. Al-Ani, P. W. Hewett, S. Ahmed, M. Cudmore, T. Fujisawa, S. Ahmad, A. Ahmed, The release of nitric oxide from S-nitrosothiols promotes angiogenesis. PLOS One 1, e25 (2006).
57. S. Ratnayake, I. H. Dias, E. Lattman, H. R. Griffiths, Stabilising cysteinyl thiol oxidation and nitrosation for proteomic analysis. J. Proteomics 92, 160-170 (2013).
58. M. E. Conway, N. Yennawar, R. Wallin, L. B. Poole, S. M. Hutson, Identification of a peroxide-sensitive redox switch at the CXXC motif in the human mitochondrial branched chain aminotransferase. Biochemistry 41, 9070-9078 (2002).
59. S. Mohr, H. Hallak, A. de Boitte, E. G. Lapetina, B. Brune, Nitric oxide-induced S-glutathionylation and inactivation of glyceraldehyde-3-phosphate dehydrogenase. J. Biol. Chem. 274, 9427-9430 (1999).
60. L. K. Rogers, B. L. Leinweber, C. V. Smith, Detection of reversible protein thiol modifications in tissues. Anal. Biochem. 358, 171-184 (2006).
61. P. Kostka, J. K. Park, Fluorometric detection of S-nitrosothiols. Methods Enzymol. 301, 227-235(1999).
62. H. H. Al-Sa'doni, I. Y. Khan, L Poston, I. Fisher, A. Ferro, A novel family of S-nitrosothiols: Chemical synthesis and biological actions. Nitric Oxide 4, 550-560 (2000).
63. L P. Freedman, B. F. Luisi, Z. R. Korszun, R. Basavappa, P. B. Sigler, K. R. Yamamoto, The function and structure of the metal coordination sites within the glucocorticoid receptor DNA binding domain. Nature 334, 543-546 (1988).
64. H. Ota, E. Tokunaga, K. Chang, M. Hikasa, K. lijima, M. Eto, K. Kozaki, M. Akishita, Y. Ouchi, M. Kaneki, Sirtl inhibitor, Sirtinol, induces senescence-like growth arrest with attenuated Ras-MAPK signaling in human cancer cells. Oncogene 25, 176-185 (2006).
65. W. Gu, R. G. Roeder, Activation of p53 sequence-specific DNA binding by acetylation of the p53 C-terminal domain. Cell 90, 595-606 (1997).
66. M. T. Ronco, L Alvarez Mde, J. A. Monti, M. C. Carrillo, G. B. Pisani, M. C. Lugano, C. E. Carnovale, Role of nitric oxide increase on induced programmed cell death during early stages of rat liver regeneration. Biochim. Biophys. Acta 1690, 70-76 (2004).
67. Y. H. Wang, Y. G. Tsay, B. C. Tan, W. Y. Lo, S.-C. Lee, Identification and characterization of a novel p300-mediated p53 acetylation site, lysine 305. J. Biol. Chem. 278, 25568-25576 (2003).
68. B. Lima, M. T. Forrester, D. T. Hess, J. S. Stamler, S-nitrosylation in cardiovascular signaling. Circ. Res. 106, 633-646 (2010).
69. A. Schrammel, S. Behrends, K. Schmidt, D. Koesling, B. Mayer, Characterization of 1H-[1,2,4]oxadiazolo[4,3-a]quinoxalin-1-one as a heme-site inhibitor of nitric oxidesensitive guanylyl cyclase. Mol. Pharmacol. 50, 1-5 (1996).
70. N. Khan, M. Jeffers, S. Kumar, C. Hackett, F. Boldog, N. Khramtsov, X. Qian, E. Mills, S. C. Berghs, N. Carey, P. W. Finn, L S. Collins, A. Tumber, J. W. Ritchie, P. B. Jensen, H. S. Lichenstein, M. Sehested, Determination of the class and isoform selectivity of small-molecule histone deacetylase inhibitors. Biochem. J. 409, 581-589 (2008).
71. P. Ak, A. J. Levine, p53 and NF-κB: Different strategies for responding to stress lead to a functional antagonism. FASEB J. 24, 3643-3652 (2010).
72. C. R. Sunico, T. Nakamura, E. Rockenstein, M. Mante, A. Adame, S. F. Chan, T. F. Newmeyer, E. Masliah, N. Nakanishi, S. A. Lipton, S-Nitrosylation of parkin as a novel regulator of p53-mediated neuronal cell death in sporadic Parkinson's disease. Mol. Neurodegen. 8, 29 (2013).
73. 6-(1-lminoethyl)lysine: A selective inhibitor of inducible nitric oxide synthase. J. Med. Chem. 37, 3886-3888 (1994).
74. G. Williams, T. Brown, L. Becker, M. Prager, B. P. Giroir, Cytokine-induced expression of nitric oxide synthase in C2C12 skeletal muscle myocytes. Am. J. Physiol. 267, R1020-R1025 (1994).
75. R. Boer, W. R. Ulrich, T. Klein, B. Mirau, S. Haas, I. Baur, The inhibitory potency and selectivity of arginine substrate site nitric-oxide synthase inhibitors is solely determined by their affinity toward the different isoenzymes. Mol. Pharmacol. 58,1026-1034 (2000).
76. N. Gharavi, A. O. El-Kadi, Role of nitric oxide in downregulation of cytochrome P450 1a1 and NADPH: Quinone oxidoreductase 1 by tumor necrosis factor-α and lipopolysaccharide. J. Pharm. Sci. 96, 2795-2807 (2007).
77. M. Trøseid, T. K. Nestvold, K. Rudi, H. Thoresen, E. W. Nielsen, K. T. Lappegàrd, Plasma lipopolysaccharide is closely associated with glycemic control and abdominal obesity: Evidence from bariatric surgery. Diabetes Care 36, 3627-3632 (2013).
78. C. B. Forsyth, K. M. Shannon, J. H. Kordower, R. M. Voigt, M. Shaikh, J. A. Jaglin, J. D. Estes, H. B. Dodiya, A. Keshavarzian, Increased intestinal permeability correlates with sigmoid mucosa a-synuclein staining and endotoxin exposure markers in early Parkinson's disease. PLOS One 6, e28032 (2011).
79. P. Wiesner, S. H. Choi, F. Almazan, C. Benner, W. Huang, C. J. Diehl, A. Gonen, S. Butler, J. L. Witztum, C. K. Glass, Y. I. Miller, Low doses of lipopolysaccharide and minimally oxidized low-density lipoprotein cooperatively activate macrophages via nuclear factor κB and activator protein-1: Possible mechanism for acceleration of atherosclerosis by subclinical endotoxemia. Orc. Res. 107, 56-65 (2010).
80. A. Doyle, G. Zhang, E. A. Abdel Fattah, N. T. Eissa, Y. P. Li, Toll-like receptor 4 mediates lipopolysaccharide-induced muscle catabolism via coordinate activation of ubiquitin-proteasome and autophagy-lysosome pathways. FASEB J. 25,99-110 (2011).
81. M. E. Starr, H. Saito, Sepsis in old age: Review of human and animal studies. Aging Dis. 5, 126-136 (2014).
82. Y. Takaoka, S. Goto, T. Nakano, H. P. Tseng, S. M. Yang, S. Kawamoto, K. Ono, C. L. Chen, Glyceraldehyde-3-phosphate dehydrogenase (GAPDH) prevents lipopolysaccharide (LPS)-induced, sepsis-related severe acute lung injury in mice. Sci. Rep. 4, 5204(2014).
83. J. D. MacMicking, C. Nathan, G. Horn, N. Chartrain, D. S. Fletcher, M. Trumbauer, K. Stevens, Q. W. Xie, K. Sokol, N. Hutchinson, H. Chen, J. S. Mudget, Altered responses to bacterial infection and endotoxic shock in mice lacking inducible nitric oxide synthase. Cell 81, 641-650 (1995).
84. A. Ghosh, A. Roy, X. Liu, J. H. Kordower, E. J. Mufson, D. M. Hartley, S. Ghosh, R. L Mosley, H. E. Gendelman, K. Pahan, Selective inhibition of NF-κB activation prevents dopaminergic neuronal loss in a mouse model of Parkinson's disease. Proc. Natl. Acad. Sci. U.S.A. 104, 18754-18759 (2007).
85. L. Novikova, B. L. Garris, D. R. Garris, Y. S. Lau, Early signs of neuronal apoptosis in the substantia nigra pars compacta of the progressive neurodegenerative mouse 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine/probenecid model of Parkinson's disease. Neuroscience 140, 67-76 (2006).
86. M. Chalimoniuk, N. Lukacova, J. Marsala, J. Langfort, Alterations of the expression and activity of midbrain nitric oxide synthase and soluble guanylyl cyclase in 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-induced Parkinsonism in mice. Neuroscience 141, 1033-1046(2006).
87. M. Mitkovski, F. E. Padovan-Neto, R. Raisman-Vozari, L. Ginestet, C. A. da-Silva, E. A. Del-Bel, Investigations into potential extrasynaptic communication between the dopaminergic and nitrergic systems. Front. Physiol. 3, 372 (2012).
88. T. Gonzá-Hernández, M. Rodríguez, Compartimentai organization and chemical profile of dopaminergic and GABAergic neurons in the substantia nigra of the rat. J. Comp. Neurol. 421, 107-135 (2000).
89. D. S. Bredt, C. E. Glatt, P. M. Hwang, M. Fotuhi, T. M. Dawson, S. H. Snyder, Nitric oxide synthase protein and mRNA are discretely localized in neuronal populations of the mammalian CNS together with NADPH diaphorase. Neuron 7, 615-624 (1991).
90. A. J. Gow, Q. Chen, D. T. Hess, B. J. Day, H. Ischiropoulos, J. S. Stamler, Basal and stimulated protein S-nitrosylation in multiple cell types and tissues. J. Biol. Chem. 277, 9637-9640 (2002).
91. F. Murad, The nitric oxide-cyclic GMP signal transduction system for intracellular and intercellular communication. Recent Prog. Horm. Res. 49, 239-248 (1994).
92. T. Suda, T. Takahashi, P. Golstein, S. Nagata, Molecular cloning and expression of the Fas ligand, a novel member of the tumor necrosis factor family. Cell 75, 1169-1178 (1993).
93. S. L Dodd, B. Hain, S. M. Senf, A. R. Judge, Hsp27 inhibits IKKβ-induced NF-κB activity and skeletal muscle atrophy. FASEB J. 23, 3415-3423 (2009).
94. S. M. McCann, C. Mastronardi, A. de Laurentiis, V. Rettori, The nitric oxide theory of aging revisited. Ann. N. Y. Acad. Sci. 1057, 64-84 (2005).
95. T. Nakamura, S. Tu, M. W. Akhtar, C. R. Sunico, S. Okamoto, S. A. Lipton, Aberrant protein S-nitrosylation in neurodegenerative diseases. Neuron 78, 596-614 (2013).
96. L. Santhanam, H. K. Lim, H. K. Lim, V. Miriel, T. Brown, M. Patel, S. Balanson, S. Ryoo, M. Anderson, K. Irani, F. Khanday, L. Di Costanzo, D. Nyhan, J. M. Hare, D. W. Christianson, R. Rivers, A. Shoukas, D. E. Berkowitz, Inducible NO synthase-dependent S-nitrosylation and activation of arginasel contribute to age-related endothelial dysfunction. Circ. Res. 101, 692-702(2007).
97. V. A. Yakovlev, I. J. Barani, C. S. Rabender, S. M. Black, J. K. Leach, P. R. Graves, G. E. Kellogg, R. B. Mikkelsen, Tyrosine nitration of κBa: A novel mechanism for NF-κB activation. Biochemistry AG, 11671-11683 (2007).
98. Y. Zheng, S. E. Gardner, M. C. Clarke, Cell death, damage-associated molecular patterns, and sterile inflammation in cardiovascular disease. Arterioscler. Thromb. Vasc. Biol. 31, 2781-2786 (2011).
99. M. Yamada, K. Kida, W. Amutuhaire, F. Ichinose, M. Kaneki, Gene disruption of caspase-3 prevents MPTP-induced Parkinson's disease in mice. Biochem. Biophys. Res. Commun. 402, 312-318 (2010).
100. T. Kuncewicz, P. Balakrishnan, M. B. Snuggs, B. C. Kone, Specific association of nitric oxide synthase-2 with Rac isoforms in activated murine macrophages. Am. J. Physiol. Renal. Physiol. 281, F326-F336 (2001).
101. S. Shinozaki, C. S. Choi, N. Shimizu, M. Yamada, M. Kim, T. Zhang, G. Shiota, H. H. Dong, Y. B. Kim, M. Kaneki, Liver-specific inducible nitric-oxide synthase expression is sufficient to cause hepatic insulin resistance and mild hyperglycemia in mice. J. Biol. Chem. 286, 34959-34975 (2011).
102. J. Landry, A. Sutton, S. T. Tafrov, R. C. Heller, J. Stebbins, L Pillus, R. Sternglanz, The silencing protein SIR2 and its homologs are NAD-dependent protein deacetylases. Proc. Natl. Acad. Sci. U.S.A. 97, 5807-5811 (2000).