The N-terminal region of serum amyloid A3 protein activates NF-κB and up-regulates MUC2 mucin mRNA expression in mouse colonic epithelial cells

PLoS ONE

Volumn 12, Issue 7, 2017, Pages

  Tashiro, Manami ^a   Iwata, Ami ^a   Yamauchi, Marika ^a   Shimizu, Kaori ^a   Okada, Ayaka ^a   Ishiguro, Naotaka ^a   Inoshima, Yasuo ^a  

^a GIFU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

I KAPPA B KINASE ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; MESSENGER RNA; MUCIN 2; PROTEIN INHIBITOR; PROTEIN MD 2; RECOMBINANT PROTEIN; SERUM AMYLOID A; SERUM AMYLOID A1; SERUM AMYLOID A3; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; AMYLOID PROTEIN; CYTOKINE; MUC2 PROTEIN, MOUSE;

AMINO ACID ANALYSIS; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; COLON EPITHELIUM; CONTROLLED STUDY; CYTOKINE PRODUCTION; EPITHELIUM CELL; GENE EXPRESSION REGULATION; MOUSE; MUC2 GENE; NONHUMAN; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS; UPREGULATION; AMYLOIDOSIS; ANIMAL; CELL LINE; COLON; GENETICS; METABOLISM; NUCLEOTIDE SEQUENCE; SEQUENCE ALIGNMENT;

AMYLOIDOGENIC PROTEINS; AMYLOIDOSIS; ANIMALS; BASE SEQUENCE; CELL LINE; COLON; CYTOKINES; EPITHELIAL CELLS; MICE; MUCIN-2; NF-KAPPA B; RNA, MESSENGER; SEQUENCE ALIGNMENT; SERUM AMYLOID A PROTEIN; UP-REGULATION;

EID: 85025167183     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0181796     Document Type: Article

References (30)

1. Uhlar CM, Whitehead AS (1999) Serum amyloid A, the major vertebrate acute-phase reactant. Eur J Biochem 265: 501–23. PMID: 10504381
2. Obici L, Merlini G (2012) AA amyloidosis: basic knowledge, unmet needs and future treatments. Swiss Med Wkly 142: w13580. https://doi.org/10.4414/smw.2012.13580 PMID: 22653707
3. Hiratsuka S, Watanabe A, Sakurai Y, Akashi-Takamura S, Ishibashi S, Miyake K, et al. (2008) The S100A8-serum amyloid A3-TLR4 paracrine cascade establishes a pre-metastatic phase. Nat Cell Biol 10: 1349–55. PMID: 18820689
4. Meek RL, Benditt EP (1986) Amyloid A gene family expression in different mouse tissues. J Exp Med 164: 2006–17. PMID: 3783088
5. Reigstad CS, Lundén GÖ, Felin J, Bäckhed F (2009) Regulation of serum amyloid A3 (SAA3) in mouse colonic epithelium and adipose tissue by the intestinal microbiota. PLoS One 4: e5842. https://doi.org/10.1371/journal.pone.0005842 PMID: 19513118
6. de Beer MC, Yuan T, Kindy MS, Asztalos BF, Roheim PS, de Beer FC (1995) Characterization of constitutive human serum amyloid A protein (SAA4) as an apolipoprotein. J Lipid Res 36: 526–34. PMID: 7775864
7. Chiba T, Han CY, Vaisar T, Shimokado K, Kargi A, Chen MH, et al. (2009) Serum amyloid A3 does not contribute to circulating SAA levels. J Lipid Res 50: 1353–62. https://doi.org/10.1194/jlr.M900089-JLR200 PMID: 19286646
8. Shah C, Hari-Dass R, Raynes JG (2006) Serum amyloid A is an innate immune opsonin for Gram-negative bacteria. Blood 108: 1751–57. https://doi.org/10.1182/blood-2005-11-011932 PMID: 16735604
9. Eckhardt ERM, Witta J, Zhong J, Arsenescu R, Arsenescu V, Wang Y, Ghoshal S, et al. (2010) Intestinal epithelial serum amyloid A modulates bacterial growth in vitro and pro-inflammatory responses in mouse experimental colitis. BMC Gastroenterol 10: 133. https://doi.org/10.1186/1471-230X-10-133 PMID: 21067563
10. Shigemura H, Ishiguro N, Inoshima Y (2014) Up-regulation of MUC2 mucin expression by serum amyloid A3 protein in mouse colonic epithelial cells. J Vet Med Sci 76: 985–91. https://doi.org/10.1292/jvms.14-0007 PMID: 24694941
11. Dilly AK, Song X, Zeh HJ, Guo ZS, Lee YJ, Bartlett DL, Choudry HA (2015) Mitogen-activated protein kinase inhibition reduces mucin 2 production and mucinous tumor growth. Transl Res 166: 344–54. https://doi.org/10.1016/j.trsl.2015.03.004 PMID: 25890193
12. Cadera EJ, Wan F, Amin RH, Nolla H, Lenardo MJ, Schlissel MS (2009) NF-κB activity marks cells engaged in receptor editing. J Exp Med 206: 1803–16. https://doi.org/10.1084/jem.20082815 PMID: 19581408
13. Cash HL, Whitham CV, Behrendt CL, Hooper LV (2006) Symbiotic bacteria direct expression of an intestinal bactericidal lectin. Science 313: 1126–30. https://doi.org/10.1126/science.1127119 PMID: 16931762
14. Clarke LL, Gawenis LR, Bradford EM, Judd LM, Boyle KT, Simpson JE, et al. (2004) Abnormal Paneth cell granule dissolution and compromised resistance to bacterial colonization in the intestine of CF mice. Am J Physiol Gastrointest Liver Physiol 286: G1050–8. https://doi.org/10.1152/ajpgi.00393.2003 PMID: 14715526
15. Rahman A, Fahlgren A, Sundstedt C, Hammarström S, Danielsson Å, Hammarström ML (2010) Chronic colitis induces expression of β-defensins in murine intestinal epithelial cells. Clin Exp Immunol 163: 123–30. https://doi.org/10.1111/j.1365-2249.2010.04282.x PMID: 21039426
16. Wlodarska M, Willing B, Keeney KM, Menendez A, Bergstrom KS, Gill N, et al. (2011) Antibiotic treatment alters the colonic mucus layer and predisposes the host to exacerbated Citrobacter rodentium-induced colitis. Infect Immun 79: 1536–45. https://doi.org/10.1128/IAI.01104-10 PMID: 21321077
17. Yang YH, Morand EF, Getting SJ, Paul-Clark M, Liu DL, Yona S, et al. (2004) Modulation of inflammation and response to dexamethasone by Annexin 1 in antigen-induced arthritis. Arthritis Rheum 50: 976–84. https://doi.org/10.1002/art.20201 PMID: 15022342
18. Ayabe T, Satchell DP, Wilson CL, Parks WC, Selsted ME, Ouellette AJ (2000) Secretion of microbicidal α-defensins by intestinal Paneth cells in response to bacteria. Nat Immunol 1: 113–8. PMID: 11248802
19. Loonen LMP, Stolte EH, Jaklofsky MTJ, Meijerink M, Dekker J, van Baarlen P, et al. (2014) REG3γ-deficient mice have altered mucus distribution and increased mucosal inflammatory responses to the microbiota and enteric pathogens in the ileum. Mucosal Immunol 7: 939–47. PMID: 24345802
20. Yuan JS, Reed A, Chen F, Stewart CN Jr. (2006) Statistical analysis of real-time PCR data. BMC Bioin-formatics 7: 85. PMID: 16504059
21. Bottero V, Imbert V, Frelin C, Formento JL, Peyron JF (2003) Monitoring NF-κB transactivation potential via real-time PCR quantification of IκB-α gene expression. Mol Diagn 7: 187–94. PMID: 15068390
22. Deguchi A, Tomita T, Omori T, Komatsu A, Ohto U, Takahashi S, et al. (2013) Serum amyloid A3 binds MD-2 to activate p38 and NF-κB pathways in a MyD88-dependent manner. J Immunol 191: 1856–64. https://doi.org/10.4049/jimmunol.1201996 PMID: 23858030
23. Enss ML, Cornberg M, Wagner S, Gebert A, Henrichs M, Eisenblätter R, et al. (2000) Proinflammatory cytokines trigger MUC gene expression and mucin release in the intestinal cancer cell line LS180. Inflamm Res 49: 162–9. https://doi.org/10.1007/s000110050576 PMID: 10858016
24. Iwashita J, Sato Y, Sugaya H, Takahashi N, Sasaki H, Abe T (2003) mRNA of MUC2 is stimulated by IL-4, IL-13 or TNF-α through a mitogen-activated protein kinase pathway in human colon cancer cells. Immunol Cell Biol 81: 275–82. PMID: 12848848
25. Son DS, Roby KF, Terranova PF (2004) Tumor necrosis factor-α induces serum amyloid A3 in mouse granulosa cells. Endocrinology 145: 2245–52. https://doi.org/10.1210/en.2003-1261 PMID: 14749357
26. Mejías-Luque R, Peiró S, Vincent A, Van Seuningen I, de Bolós C (2008) IL-6 induces MUC4 expression through gp130/STAT3 pathway in gastric cancer cell lines. Biochim Biophys Acta 1783: 1728–36.
27. Fasshauer M, Klein J, Kralisch S, Klier M, Lossner U, Bluher M, et al. (2004) Serum amyloid A3 expression is stimulated by dexamethasone and interleukin-6 in 3T3-L1 adipocytes. J Endocrinol 183: 561–7. https://doi.org/10.1677/joe.1.05699 PMID: 15590982
28. Kasahara DI, Kim HY, Mathews JA, Verbout NG, Williams AS, Wurmbrand AP, et al. (2014) Pivotal role of IL-6 in the heperinflammatory responses to subacute ozone in adiponectin-deficient mice. Am J Physiol Lung Cell Mol Physiol 306: L508–20. https://doi.org/10.1152/ajplung.00235.2013 PMID: 24381131
29. Shimizu H, Yamamoto K (1994) NF-κB and C/EBP transcription factor families synergistically function in mouse serum amyloid A gene expression induced by inflammatory cytokines. Gene 149: 305–10. PMID: 7959007
30. Mack DR, McDonald TL, Larson MA, Wei S, Weber A (2003) The conserved TFLK motif of mammary-associated serum amyloid A3 is responsible for up-regulation of intestinal MUC3 mucin expression in vitro. Pediatr Res 53: 137–42. https://doi.org/10.1203/00006450-200301000-00023 PMID: 12508093