Glycogen synthase kinase-3β inactivation is an intracellular marker and regulator for endotoxemic neutrophilia

详细信息    查看全文

• 作者：Tsan-Tzu Yang (1)
  Chia-Ling Chen (3)
  Wei-Chieh Lin (4)
  Yee-Shin Lin (1) (3) (5)
  Po-Chun Tseng (2)
  Chia-Yuan Hsieh (2)
  Yu-Hong Chen (1)
  Wei-Ching Huang (2)
  Cheng-Chieh Tsai (5) (6)
  Chi-Yun Wang (5)
  Chi-Chang Shieh (1) (2) (5) (7)
  Chiou-Feng Lin (1) (2) (3) (5)
  
• 关键词：Neutrophil ; Neutrophilia ; Apoptosis ; LPS ; Glycogen synthase kinase ; 3β ; Mcl ; 1 ; AKT ; p38 MAPK ; ROS
• 刊名：Journal of Molecular Medicine
• 出版年：2013
• 出版时间：February 2013
• 年：2013
• 卷：91
• 期：2
• 页码：207-217
• 全文大小：761KB
• 参考文献：1. Fialkow L, Fochesatto Filho L, Bozzetti MC, Milani AR, Rodrigues Filho EM, Ladniuk RM, Pierozan P, de Moura RM, Prolla JC, Vachon E et al (2006) Neutrophil apoptosis: a marker of disease severity in sepsis and sepsis-induced acute respiratory distress syndrome. Crit Care 10:R155 CrossRef
  2. Hoesel LM, Neff TA, Neff SB, Younger JG, Olle EW, Gao H, Pianko MJ, Bernacki KD, Sarma JV, Ward PA (2005) Harmful and protective roles of neutrophils in sepsis. Shock 24:40-7 CrossRef
  3. Hofman P (2004) Molecular regulation of neutrophil apoptosis and potential targets for therapeutic strategy against the inflammatory process. Curr Drug Targets Inflamm Allergy 3:1- CrossRef
  4. Fox S, Leitch AE, Duffin R, Haslett C, Rossi AG (2010) Neutrophil apoptosis: relevance to the innate immune response and inflammatory disease. J Innate Immun 2:216-27 CrossRef
  5. Brown KA, Brain SD, Pearson JD, Edgeworth JD, Lewis SM, Treacher DF (2006) Neutrophils in development of multiple organ failure in sepsis. Lancet 368:157-69 CrossRef
  6. Kobayashi SD, Voyich JM, Whitney AR, DeLeo FR (2005) Spontaneous neutrophil apoptosis and regulation of cell survival by granulocyte macrophage-colony stimulating factor. J Leukoc Biol 78:1408-418 CrossRef
  7. Klein JB, Rane MJ, Scherzer JA, Coxon PY, Kettritz R, Mathiesen JM, Buridi A, McLeish KR (2000) Granulocyte-macrophage colony-stimulating factor delays neutrophil constitutive apoptosis through phosphoinositide 3-kinase and extracellular signal-regulated kinase pathways. J Immunol 164:4286-291
  8. Derouet M, Thomas L, Cross A, Moots RJ, Edwards SW (2004) Granulocyte macrophage colony-stimulating factor signaling and proteasome inhibition delay neutrophil apoptosis by increasing the stability of Mcl-1. J Biol Chem 279:26915-6921 CrossRef
  9. Wardle DJ, Burgon J, Sabroe I, Bingle CD, Whyte MK, Renshaw SA (2011) Effective caspase inhibition blocks neutrophil apoptosis and reveals Mcl-1 as both a regulator and a target of neutrophil caspase activation. PLoS One 6:e15768 CrossRef
  10. Altenburg SP, Martins MA, Silva AR, Cordeiro RS, Castro-Faria-Neto HC (1997) LPS-induced blood neutrophilia is inhibited by alpha 1-adrenoceptor antagonists: a role for catecholamines. J Leukoc Biol 61:689-94
  11. Yoshimura A, Hara Y, Kaneko T, Kato I (1997) Secretion of IL-1 beta, TNF-alpha, IL-8 and IL-1ra by human polymorphonuclear leukocytes in response to lipopolysaccharides from periodontopathic bacteria. J Periodontal Res 32:279-86 CrossRef
  12. Smedman C, Gardlund B, Nihlmark K, Gille-Johnson P, Andersson J, Paulie S (2009) ELISpot analysis of LPS-stimulated leukocytes: human granulocytes selectively secrete IL-8, MIP-1beta and TNF-alpha. J Immunol Methods 346:1- CrossRef
  13. Maurer U, Charvet C, Wagman AS, Dejardin E, Green DR (2006) Glycogen synthase kinase-3 regulates mitochondrial outer membrane permeabilization and apoptosis by destabilization of MCL-1. Mol Cell 21:749-60 CrossRef
  14. Jope RS, Johnson GV (2004) The glamour and gloom of glycogen synthase kinase-3. Trends Biochem Sci 29:95-02 CrossRef
  15. Lin CF, Chen CL, Chiang CW, Jan MS, Huang WC, Lin YS (2007) GSK-3beta acts downstream of PP2A and the PI 3-kinase-Akt pathway, and upstream of caspase-2 in ceramide-induced mitochondrial apoptosis. J Cell Sci 120:2935-943 CrossRef
  16. Focosi D, Azzara A, Kast RE, Carulli G, Petrini M (2009) Lithium and hematology: established and proposed uses. J Leukoc Biol 85:20-8 CrossRef
  17. Thornton TM, Pedraza-Alva G, Deng B, Wood CD, Aronshtam A, Clements JL, Sabio G, Davis RJ, Matthews DE, Doble B et al (2008) Phosphorylation by p38 MAPK as an alternative pathway for GSK3beta inactivation. Science 320:667-70 CrossRef
  18. Witko-Sarsat V, Pederzoli-Ribeil M, Hirsch E, Sozzani S, Cassatella MA (2011) Regulating neutrophil apoptosis: new players enter the game. Trends Immunol 32:117-24 CrossRef
  19. Bikkavilli RK, Feigin ME, Malbon CC (2008) p38 mitogen-activated protein kinase regulates canonical Wnt-beta-catenin signaling by inactivation of GSK3beta. J Cell Sci 121:3598-607 CrossRef
  20. Emre Y, Hurtaud C, Nubel T, Criscuolo F, Ricquier D, Cassard-Doulcier AM (2007) Mitochondria contribute to LPS-induced MAPK activation via uncoupling protein UCP2 in macrophages. Biochem J 402:271-78 CrossRef
  21. Pan J, Chang Q, Wang X, Son Y, Zhang Z, Chen G, Luo J, Bi Y, Chen F, Shi X (2010) Reactive oxygen species-activated Akt/ASK1/p38 signaling pathway in nickel compound-induced apoptosis in BEAS 2B cells. Chem Res Toxicol 23:568-77 CrossRef
  22. Bracho F, Goldman S, Cairo MS (1998) Potential use of granulocyte colon-stimulating factor and granulocyte-macrophage colony-stimulating factor in neonates. Curr Opin Hematol 5:215-20 CrossRef
  23. Glowacka E, Banasik M, Lewkowicz P, Tchorzewski H (2002) The effect of LPS on neutrophils from patients with high risk of type 1 diabetes mellitus in relation to IL-8, IL-10 and IL-12 production and apoptosis in vitro. Scand J Immunol 55:210-17 CrossRef
  24. Bae HB, Zmijewski JW, Deshane JS, Zhi D, Thompson LC, Peterson CB, Chaplin DD, Abraham E (2012) Vitronectin inhibits neutrophil apoptosis through activation of integrin-associated signaling pathways. Am J Respir Cell Mol Biol 46:790-96 CrossRef
  25. Aomatsu K, Kato T, Fujita H, Hato F, Oshitani N, Kamata N, Tamura T, Arakawa T, Kitagawa S (2008) Toll-like receptor agonists stimulate human neutrophil migration via activation of mitogen-activated protein kinases. Immunology 123:171-80
  26. Kobayashi S, Lee SH, Meng XW, Mott JL, Bronk SF, Werneburg NW, Craig RW, Kaufmann SH, Gores GJ (2007) Serine 64 phosphorylation enhances the antiapoptotic function of Mcl-1. J Biol Chem 282:18407-8417 CrossRef
  27. Kodama Y, Taura K, Miura K, Schnabl B, Osawa Y, Brenner DA (2009) Antiapoptotic effect of c-Jun N-terminal Kinase-1 through Mcl-1 stabilization in TNF-induced hepatocyte apoptosis. Gastroenterology 136:1423-434 CrossRef
  28. Inoshita S, Takeda K, Hatai T, Terada Y, Sano M, Hata J, Umezawa A, Ichijo H (2002) Phosphorylation and inactivation of myeloid cell leukemia 1 by JNK in response to oxidative stress. J Biol Chem 277:43730-3734 CrossRef
  29. Thornton TM, Rincon M (2009) Non-classical p38 map kinase functions: cell cycle checkpoints and survival. Int J Biol Sci 5:44-1 CrossRef
  30. Leuenroth SJ, Grutkoski PS, Ayala A, Simms HH (2000) Suppression of PMN apoptosis by hypoxia is dependent on Mcl-1 and MAPK activity. Surgery 128:171-77 CrossRef
  31. Beurel E, Jope RS (2006) The paradoxical pro- and anti-apoptotic actions of GSK3 in the intrinsic and extrinsic apoptosis signaling pathways. Prog Neurobiol 79:173-89 CrossRef
  32. Xu Y, Loison F, Luo HR (2010) Neutrophil spontaneous death is mediated by down-regulation of autocrine signaling through GPCR, PI3Kgamma, ROS, and actin. Proc Natl Acad Sci U S A 107:2950-955 CrossRef
  33. Koay MA, Christman JW, Segal BH, Venkatakrishnan A, Blackwell TR, Holland SM, Blackwell TS (2001) Impaired pulmonary NF-kappaB activation in response to lipopolysaccharide in NADPH oxidase-deficient mice. Infect Immun 69:5991-996 CrossRef
  34. Asehnoune K, Strassheim D, Mitra S, Kim JY, Abraham E (2004) Involvement of reactive oxygen species in Toll-like receptor 4-dependent activation of NF-kappa B. J Immunol 172:2522-529
  35. Matsuzawa A, Ichijo H (2008) Redox control of cell fate by MAP kinase: physiological roles of ASK1-MAP kinase pathway in stress signaling. Biochim Biophys Acta 1780:1325-336 CrossRef
  36. Ajibade AA, Wang Q, Cui J, Zou J, Xia X, Wang M, Tong Y, Hui W, Liu D, Su B et al (2012) TAK1 negatively regulates NF-κB and p38 MAP kinase activation in Gr-1⁺CD11b⁺ neutrophils. Immunity 36:43-4 CrossRef
  37. Turrens JF (2003) Mitochondrial formation of reactive oxygen species. J Physiol 552:335-44 CrossRef
  38. West AP, Brodsky IE, Rahner C, Woo DK, Erdjument-Bromage H, Tempst P, Walsh MC, Choi Y, Shadel GS, Ghosh S (2011) TLR signalling augments macrophage bactericidal activity through mitochondrial ROS. Nature 472:476-80 CrossRef
  39. Savov JD, Brass DM, Lawson BL, McElvania-Tekippe E, Walker JK, Schwartz DA (2005) Toll-like receptor 4 antagonist (E5564) prevents the chronic airway response to inhaled lipopolysaccharide. Am J Physiol Lung Cell Mol Physiol 289:L329–L337 CrossRef
  40. Rincon M, Davis RJ (2009) Regulation of the immune response by stress-activated protein kinases. Immunol Rev 228:212-24 CrossRef
  
• 作者单位：Tsan-Tzu Yang (1)
  Chia-Ling Chen (3)
  Wei-Chieh Lin (4)
  Yee-Shin Lin (1) (3) (5)
  Po-Chun Tseng (2)
  Chia-Yuan Hsieh (2)
  Yu-Hong Chen (1)
  Wei-Ching Huang (2)
  Cheng-Chieh Tsai (5) (6)
  Chi-Yun Wang (5)
  Chi-Chang Shieh (1) (2) (5) (7)
  Chiou-Feng Lin (1) (2) (3) (5)
  
  1. Department of Microbiology and Immunology, College of Medicine, National Cheng Kung University, Tainan, Taiwan
  3. Center of Infectious Disease and Signaling Research, College of Medicine, National Cheng Kung University, Tainan, Taiwan
  4. Institute of Internal Medicine, College of Medicine, National Cheng Kung University, Tainan, Taiwan
  5. Institute of Basic Medical Sciences, College of Medicine, National Cheng Kung University, Tainan, Taiwan
  2. Institute of Clinical Medicine, College of Medicine, National Cheng Kung University, Tainan, Taiwan
  6. Department of Nursing, Chung Hwa University of Medical Technology, Tainan, Taiwan
  7. Institute of Pediatrics, College of Medicine, National Cheng Kung University, Tainan, Taiwan
  
• ISSN：1432-1440

文摘

Neutrophilia, defined as a large number of neutrophils in the circulating blood, is caused by increased differentiation and survival from activation-induced apoptosis. Regulation of apoptosis is essential for neutrophil homeostasis; however, the molecular signaling that regulates this process needs further investigation. Unlike TLR4 wild-type C3H/HeN mice, TLR4 mutated C3H/HeJ mice were insusceptible to LPS-induced blood neutrophilia. LPS prevented constitutive apoptosis in neutrophils and partly involved a blockade of the mitochondrial pathway including mitochondria transmembrane potential loss, myeloid cell leukemia sequence (Mcl) 1 degradation, and caspase-3 activation. In apoptotic neutrophils, glycogen synthase kinase (GSK)-3β was activated, and inhibiting GSK-3β decreased Mcl-1 degradation and apoptosis. LPS caused p38 MAPK-, JNK-, and PI3K/AKT-mediated Mcl-1 stabilization and prevented apoptosis, and LPS induced GSK-3β inactivation mainly through p38 MAPK and PI3K/AKT. Neutrophils in the neutrophilia showed increased GSK-3β inactivation and Mcl-1 stabilization accompanied by activation of p38 MAPK, JNK, and AKT. Notably, LPS-induced ROS generation can partly facilitate p38 MAPK/JNK/AKT activation to regulate GSK-3β-mediated Mcl-1 stability, apoptosis, and neutrophilia. These results demonstrate that the molecular basis of endotoxemic neutrophilia is through a direct action on neutrophils involving GSK-3β inactivation to prevent constitutive apoptosis.