Smad7 interrupts TGF-β signaling in intestinal macrophages and promotes inflammatory activation of these cells during necrotizing enterocolitis

Pediatric Research

Volumn 79, Issue 6, 2016, Pages 951-961

  MohanKumar, Krishnan ^a,b   Namachivayam, Kopperuncholan ^a,b   Chapalamadugu, Kalyan C ^c   Garzon, Steven A ^a   Premkumar, Muralidhar H ^d   Tipparaju, Srinivas M ^c   Maheshwari, Akhil ^a,b,c  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b UNIVERSITY OF SOUTH FLORIDA   (United States)

^c UNIVERSITY OF SOUTH FLORIDA   (United States)

^d BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

I KAPPA B KINASE BETA; SMAD7 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; I KAPPA B KINASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIPOPOLYSACCHARIDE; SMAD7 PROTEIN, HUMAN; SMAD7 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL LOAD; CELL ACTIVATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MACROPHAGE; MOUSE; NECROTIZING ENTEROCOLITIS; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TISSUE INJURY; TRANSCRIPTION INITIATION; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; INTESTINE; METABOLISM; RAW 264.7 CELL LINE;

ANIMALS; ENTEROCOLITIS, NECROTIZING; HUMANS; I-KAPPA B KINASE; INFLAMMATION; INTESTINES; LIPOPOLYSACCHARIDES; MACROPHAGES; MICE; MICE, INBRED C57BL; NF-KAPPA B; RAW 264.7 CELLS; SIGNAL TRANSDUCTION; SMAD7 PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

EID: 84976384384     PISSN: 00313998     EISSN: 15300447     Source Type: Journal    
DOI: 10.1038/pr.2016.18     Document Type: Article

References (39)

1. Neu J, Walker WA. Necrotizing enterocolitis. N Engl J Med 2011;364: 255-64.
2. Maheshwari A. Immunologic and hematological abnormalities in necrotizing enterocolitis. Clin Perinatol 2015;42:567-85.
3. Remon JI, Amin SC, Mehendale SR, et al. Depth of bacterial invasion in resected intestinal tissue predicts mortality in surgical necrotizing enterocolitis. J Perinatol 2015;35:755-62.
4. MohanKumar K, Kaza N, Jagadeeswaran R, et al. Gut mucosal injury in neonates is marked by macrophage infiltration in contrast to pleomorphic infiltrates in adult: evidence from an animal model. Am J Physiol Gastrointest Liver Physiol 2012;303:G93-102.
5. Ballance WA, Dahms BB, Shenker N, Kliegman RM. Pathology of neonatal necrotizing enterocolitis: a ten-year experience. J Pediatr 1990;117:S6-13.
6. Bain CC, Bravo-Blas A, Scott CL, et al. Constant replenishment from circulating monocytes maintains the macrophage pool in the intestine of adult mice. Nat Immunol 2014;15:929-37.
7. Smythies LE, Maheshwari A, Clements R, et al. Mucosal IL-8 and TGFbeta recruit blood monocytes: evidence for cross-Talk between the lamina propria stroma and myeloid cells. J Leukoc Biol 2006;80:492-9.
8. Smythies LE, Sellers M, Clements RH, et al. Human intestinal macrophages display profound inflammatory anergy despite avid phagocytic and bacteriocidal activity. J Clin Invest 2005;115:66-75.
9. Namachivayam K, Blanco CL, MohanKumar K, et al. Smad7 inhibits autocrine expression of TGF-?2 in intestinal epithelial cells in baboon necrotizing enterocolitis. Am J Physiol Gastrointest Liver Physiol 2013;304: G167-80.
10. Briones-Orta MA, Sosa-Garrocho M, Moreno-Alvarez P, Fonseca-Sanchez MA, Macias-Silva M. SnoN co-repressor binds and represses smad7 gene promoter. Biochem Biophys Res Commun 2006;341:889-94.
11. Maheshwari A, Kelly DR, Nicola T, et al. TGF-?2 suppresses macrophage cytokine production and mucosal inflammatory responses in the developing intestine. Gastroenterology 2011;140:242-53.
12. Namachivayam K, Blanco CL, Frost BL, et al. Preterm human milk contains a large pool of latent TGF-?, which can be activated by exogenous neuraminidase. Am J Physiol Gastrointest Liver Physiol 2013;304:G1055-65.
13. Power MR, Li B, Yamamoto M, Akira S, Lin TJ. A role of Toll-IL-1 receptor domain-containing adaptor-inducing IFN-beta in the host response to Pseudomonas aeruginosa lung infection in mice. J Immunol 2007;178:3170-6.
14. Ovcharenko I, Loots GG, Giardine BM, et al. Mulan: multiple-sequence local alignment and visualization for studying function and evolution. Genome Res 2005;15:184-94.
15. Aung HT, Schroder K, Himes SR, et al. LPS regulates proinflammatory gene expression in macrophages by altering histone deacetylase expression. FASEB J 2006;20:1315-27.
16. Bauge C, Attia J, Leclercq S, Pujol JP, Galera P, Boumediene K. Interleukin-1beta up-regulation of Smad7 via NF-kappaB activation in human chondrocytes. Arthritis Rheum 2008;58:221-6.
17. Sharma R, Hudak ML, Tepas JJ 3rd, et al. Impact of gestational age on the clinical presentation and surgical outcome of necrotizing enterocolitis. J Perinatol 2006;26:342-7.
18. Alex P, Zachos NC, Nguyen T, et al. Distinct cytokine patterns identified from multiplex profiles of murine DSS and TNBS-induced colitis. Inflamm Bowel Dis 2009;15:341-52.
19. Hsueh W, Caplan MS, Tan X, MacKendrick W, Gonzalez-Crussi F. Necrotizing enterocolitis of the newborn: pathogenetic concepts in perspective. Pediatr Dev Pathol 1998;1:2-16.
20. Hunter CJ, Singamsetty VK, Chokshi NK, et al. Enterobacter sakazakii enhances epithelial cell injury by inducing apoptosis in a rat model of necrotizing enterocolitis. J Infect Dis 2008;198:586-93.
21. Liu SX, Tian R, Baskind H, Hsueh W, De Plaen IG. Platelet-Activating factor induces the processing of nuclear factor-kappaB p105 into p50, which mediates acute bowel injury in mice. Am J Physiol Gastrointest Liver Physiol 2009;297:G76-81.
22. Maheshwari A, Christensen RD, Calhoun DA, Dimmitt RA, Lacson A. Circulating CXC-chemokine concentrations in a murine intestinal ischemia-reperfusion model. Fetal Pediatr Pathol 2004;23:145-57.
23. Walthall K, Cappon GD, Hurtt ME, Zoetis T. Postnatal development of the gastrointestinal system: a species comparison. Birth Defects Res B Dev Reprod Toxicol 2005;74:132-56.
24. Nanthakumar NN, Dai D, Meng D, Chaudry N, Newburg DS, Walker WA. Regulation of intestinal ontogeny: effect of glucocorticoids and luminal microbes on galactosyltransferase and trehalase induction in mice. Glycobiology 2005;15:221-32.
25. Jahchan NS, Luo K. SnoN in mammalian development, function and diseases. Curr Opin Pharmacol 2010;10:670-5.
26. Monteleone G, Pallone F, MacDonald TT. Smad7 in TGF-beta-mediated negative regulation of gut inflammation. Trends Immunol 2004;25: 513-7.
27. Yan X, Lin Z, Chen F, et al. Human BAMBI cooperates with Smad7 to inhibit transforming growth factor-beta signaling. J Biol Chem 2009;284: 30097-104.
28. Zhang S, Fei T, Zhang L, et al. Smad7 antagonizes transforming growth factor beta signaling in the nucleus by interfering with functional Smad-DNA complex formation. Mol Cell Biol 2007;27:4488-99.
29. Sasaki K, Ito T, Nishino N, Khochbin S, Yoshida M. Real-Time imaging of histone H4 hyperacetylation in living cells. Proc Natl Acad Sci USA 2009;106:16257-62.
30. Ausio J, van Holde KE. Histone hyperacetylation: its effects on nucleosome conformation and stability. Biochemistry 1986;25:1421-8.
31. Yang F, Tang E, Guan K, Wang CY. IKK beta plays an essential role in the phosphorylation of RelA/p65 on serine 536 induced by lipopolysaccharide. J Immunol 2003;170:5630-5.
32. Premkumar MH, Sule G, Nagamani SC, et al. Argininosuccinate lyase in enterocytes protects from development of necrotizing enterocolitis. Am J Physiol Gastrointest Liver Physiol 2014;307:G347-54.
33. Eliseev RA, Schwarz EM, Zuscik MJ, O'Keefe RJ, Drissi H, Rosier RN. Smad7 mediates inhibition of Saos2 osteosarcoma cell differentiation by NFkappaB. Exp Cell Res 2006;312:40-50.
34. Nakano H, Shindo M, Sakon S, et al. Differential regulation of IkappaB kinase alpha and beta by two upstream kinases, NF-kappaB-inducing kinase and mitogen-Activated protein kinase/ERK kinase kinase-1. Proc Natl Acad Sci USA 1998;95:3537-42.
35. Nolan T, Hands RE, Bustin SA. Quantification of mRNA using real-Time RT-PCR. Nat Protoc 2006;1:1559-82.
36. Xu D, Wang S, Liu W, Liu J, Feng X. A novel receptor activator of NF-kappaB (RANK) cytoplasmic motif plays an essential role in osteoclastogenesis by committing macrophages to the osteoclast lineage. J Biol Chem 2006;281:4678-90.
37. Namachivayam K, Coffing HP, Sankaranarayanan NV, et al. Transforming growth factor-'2 is sequestered in preterm human milk by chondroitin sulfate proteoglycans. Am J Physiol Gastrointest Liver Physiol 2015;309:G171-80.
38. Jiang C, Xuan Z, Zhao F, Zhang MQ. TRED: a transcriptional regulatory element database, new entries and other development. Nucleic Acids Res 2007;35:D137-40.
39. Massague J, Seoane J, Wotton D. Smad transcription factors. Genes Dev 2005;19:2783-810.