Early Mucosal Sensing of SIV Infection by Paneth Cells Induces IL-1β Production and Initiates Gut Epithelial Disruption

PLoS Pathogens

Volumn 10, Issue 8, 2014, Pages

  Hirao, Lauren A ^a   Grishina, Irina ^a   Bourry, Olivier ^a   Hu, William K ^a   Somrit, Monsicha ^b   Sankaran Walters, Sumathi ^a   Gaulke, Chris A ^a   Fenton, Anne N ^a   Li, Jay A ^a   Crawford, Robert W ^a   Chuang, Frank ^a   Tarara, Ross ^c   Marco, Maria L ^b   Bäumler, Andreas J ^a   Cheng, Holland ^b   Dandekar, Satya ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD163 ANTIGEN; CD206 ANTIGEN; CD68 ANTIGEN; CHEMOKINE RECEPTOR CXCR4; CLAUDIN 1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 17; INTERLEUKIN 1BETA; LIPOPOLYSACCHARIDE; LYMPHOCYTE ANTIGEN; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; MESSENGER RNA; PROTEIN ZO1; STROMAL CELL DERIVED FACTOR 1; TIGHT JUNCTION PROTEIN; UNCLASSIFIED DRUG; VIRUS RNA;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD SAMPLING; CD4+ T LYMPHOCYTE; CELL MEMBRANE PERMEABILITY; CELL REGENERATION; CONTROLLED STUDY; DIAGNOSTIC TEST; DOWN REGULATION; EPITHELIAL TIGHT JUNCTION REPAIR; FLOW CYTOMETRY; GENE DOSAGE; GENE EXPRESSION; IMMUNE RESPONSE; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOLOGY; INFLAMMATION; INTESTINE EPITHELIUM; INTESTINE MUCOSA; INTRACELLULAR SIGNALING; LACTOBACILLUS PLANTARUM; LIMULUS AMEBOCYTE ASSAY; MALE; MEMBRANE BIOLOGY; MICROARRAY ANALYSIS; NONHUMAN; PANETH CELL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RHESUS MONKEY; RNA EXTRACTION; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; TRANSEPITHELIAL ELECTRICAL RESISTANCE; TRANSMISSION ELECTRON MICROSCOPY; VIRUS CELL INTERACTION; VIRUS LOAD; ANIMAL; BIOSYNTHESIS; DNA MICROARRAY; FLUORESCENT ANTIBODY TECHNIQUE; HOST PARASITE INTERACTION; IMMUNOHISTOCHEMISTRY; IMMUNOLOGY; METABOLISM; TIGHT JUNCTION; ULTRASTRUCTURE; VIROLOGY;

ANIMALS; FLUORESCENT ANTIBODY TECHNIQUE; HOST-PARASITE INTERACTIONS; IMMUNOHISTOCHEMISTRY; INTERLEUKIN-1BETA; INTESTINAL MUCOSA; MACACA MULATTA; MALE; MICROSCOPY, ELECTRON, TRANSMISSION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PANETH CELLS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; TIGHT JUNCTIONS; VIRAL LOAD;

EID: 84930974237     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004311     Document Type: Article

References (53)

1. Gaulke CA, Porter M, Han YH, Sankaran-Walters S, Grishina I, et al. (2014) Intestinal Epithelial Barrier Disruption through Altered Mucosal MicroRNA Expression in Human Immunodeficiency Virus and Simian Immunodeficiency Virus Infections. J Virol 88: 6268–6280.
2. Brenchley JM, Price DA, Schacker TW, Asher TE, Silvestri G, et al. (2006) Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat Med 12: 1365–1371.
3. Estes JD, Harris LD, Klatt NR, Tabb B, Pittaluga S, et al. (2010) Damaged intestinal epithelial integrity linked to microbial translocation in pathogenic simian immunodeficiency virus infections. PLoS Pathog 6: e1001052.
4. McHardy IH, Li X, Tong M, Ruegger P, Jacobs J, et al. (2013) HIV Infection is associated with compositional and functional shifts in the rectal mucosal microbiota. Microbiome 1: 26.
5. Lozupone CA, Li M, Campbell TB, Flores SC, Linderman D, et al. (2013) Alterations in the gut microbiota associated with HIV-1 infection. Cell Host Microbe 14: 329–339.
6. Gori A, Tincati C, Rizzardini G, Torti C, Quirino T, et al. (2008) Early impairment of gut function and gut flora supporting a role for alteration of gastrointestinal mucosa in human immunodeficiency virus pathogenesis. J Clin Microbiol 46: 757–758.
7. Gordon MA, Walsh AL, Chaponda M, Soko D, Mbvwinji M, et al. (2001) Bacteraemia and mortality among adult medical admissions in Malawi–predominance of non-typhi salmonellae and Streptococcus pneumoniae. J Infect 42: 44–49.
8. Hunt PW, Martin JN, Sinclair E, Bredt B, Hagos E, et al. (2003) T cell activation is associated with lower CD4+ T cell gains in human immunodeficiency virus-infected patients with sustained viral suppression during antiretroviral therapy. J Infect Dis 187: 1534–1543.
9. Guadalupe M, Sankaran S, George MD, Reay E, Verhoeven D, et al. (2006) Viral suppression and immune restoration in the gastrointestinal mucosa of human immunodeficiency virus type 1-infected patients initiating therapy during primary or chronic infection. J Virol 80: 8236–8247.
10. Moir S, Chun TW, Fauci AS, (2011) Pathogenic mechanisms of HIV disease. Annu Rev Pathol 6: 223–248.
11. Heise C, Vogel P, Miller CJ, Halsted CH, Dandekar S, (1993) Simian immunodeficiency virus infection of the gastrointestinal tract of rhesus macaques. Functional, pathological, and morphological changes. Am J Pathol 142: 1759–1771.
12. Heise C, Miller CJ, Lackner A, Dandekar S, (1994) Primary acute simian immunodeficiency virus infection of intestinal lymphoid tissue is associated with gastrointestinal dysfunction. J Infect Dis 169: 1116–1120.
13. Sankaran S, George MD, Reay E, Guadalupe M, Flamm J, et al. (2008) Rapid onset of intestinal epithelial barrier dysfunction in primary human immunodeficiency virus infection is driven by an imbalance between immune response and mucosal repair and regeneration. J Virol 82: 538–545.
14. Li Q, Estes JD, Duan L, Jessurun J, Pambuccian S, et al. (2008) Simian immunodeficiency virus-induced intestinal cell apoptosis is the underlying mechanism of the regenerative enteropathy of early infection. J Infect Dis 197: 420–429.
15. Guadalupe M, Reay E, Sankaran S, Prindiville T, Flamm J, et al. (2003) Severe CD4+ T-cell depletion in gut lymphoid tissue during primary human immunodeficiency virus type 1 infection and substantial delay in restoration following highly active antiretroviral therapy. J Virol 77: 11708–11717.
16. Dandekar S, George MD, Baumler AJ, (2010) Th17 cells, HIV and the gut mucosal barrier. Curr Opin HIV AIDS 5: 173–178.
17. Raffatellu M, Santos RL, Verhoeven DE, George MD, Wilson RP, et al. (2008) Simian immunodeficiency virus-induced mucosal interleukin-17 deficiency promotes Salmonella dissemination from the gut. Nat Med 14: 421–428.
18. Brenchley JM, Paiardini M, Knox KS, Asher AI, Cervasi B, et al. (2008) Differential Th17 CD4 T-cell depletion in pathogenic and nonpathogenic lentiviral infections. Blood 112: 2826–2835.
19. Peterson LW, Artis D, (2014) Intestinal epithelial cells: regulators of barrier function and immune homeostasis. Nat Rev Immunol 14: 141–153.
20. Bevins CL, Salzman NH, (2011) Paneth cells, antimicrobial peptides and maintenance of intestinal homeostasis. Nat Rev Microbiol 9: 356–368.
21. Zaragoza MM, Sankaran-Walters S, Canfield DR, Hung JK, Martinez E, et al. (2011) Persistence of gut mucosal innate immune defenses by enteric alpha-defensin expression in the simian immunodeficiency virus model of AIDS. J Immunol 186: 1589–1597.
22. Hand TW, Dos Santos LM, Bouladoux N, Molloy MJ, Pagan AJ, et al. Acute gastrointestinal infection induces long-lived microbiota-specific T cell responses. Science 337: 1553–1556.
23. Lamkanfi M, Kanneganti TD, Franchi L, Nunez G, (2007) Caspase-1 inflammasomes in infection and inflammation. J Leukoc Biol 82: 220–225.
24. Arnolds KL, Spencer JV, CXCR4: A virus's best friend? Infect Genet Evol 25C: 146–156.
25. Esplugues E, Huber S, Gagliani N, Hauser AE, Town T, et al. (2011) Control of TH17 cells occurs in the small intestine. Nature 475: 514–518.
26. Cogswell JP, Godlevski MM, Wisely GB, Clay WC, Leesnitzer LM, et al. (1994) NF-kappa B regulates IL-1 beta transcription through a consensus NF-kappa B binding site and a nonconsensus CRE-like site. J Immunol 153: 712–723.
27. Pontillo A, Silva LT, Oshiro TM, Finazzo C, Crovella S, et al. (2012) HIV-1 induces NALP3-inflammasome expression and interleukin-1beta secretion in dendritic cells from healthy individuals but not from HIV-positive patients. AIDS 26: 11–18.
28. Jacquelin B, Mayau V, Targat B, Liovat AS, Kunkel D, et al. (2009) Nonpathogenic SIV infection of African green monkeys induces a strong but rapidly controlled type I IFN response. J Clin Invest 119: 3544–3555.
29. Malleret B, Maneglier B, Karlsson I, Lebon P, Nascimbeni M, et al. (2008) Primary infection with simian immunodeficiency virus: plasmacytoid dendritic cell homing to lymph nodes, type I interferon, and immune suppression. Blood 112: 4598–4608.
30. Bosinger SE, Hosiawa KA, Cameron MJ, Persad D, Ran L, et al. (2004) Gene expression profiling of host response in models of acute HIV infection. J Immunol 173: 6858–6863.
31. Kurashima Y, Goto Y, Kiyono H, (2013) Mucosal innate immune cells regulate both gut homeostasis and intestinal inflammation. Eur J Immunol 43: 3108–3115.
32. McGettrick AF, O'Neill LA, (2013) NLRP3 and IL-1beta in macrophages as critical regulators of metabolic diseases. Diabetes Obes Metab 15 (Suppl 3) 19–25.
33. Suzuki T, (2013) Regulation of intestinal epithelial permeability by tight junctions. Cell Mol Life Sci 70: 631–659.
34. Al-Sadi RM, Ma TY, (2007) IL-1beta causes an increase in intestinal epithelial tight junction permeability. J Immunol 178: 4641–4649.
35. Al-Sadi R, Ye D, Dokladny K, Ma TY, (2008) Mechanism of IL-1beta-induced increase in intestinal epithelial tight junction permeability. J Immunol 180: 5653–5661.
36. Al-Sadi R, Ye D, Said HM, Ma TY, (2010) IL-1beta-induced increase in intestinal epithelial tight junction permeability is mediated by MEKK-1 activation of canonical NF-kappaB pathway. Am J Pathol 177: 2310–2322.
37. Wang F, Graham WV, Wang Y, Witkowski ED, Schwarz BT, et al. (2005) Interferon-gamma and tumor necrosis factor-alpha synergize to induce intestinal epithelial barrier dysfunction by up-regulating myosin light chain kinase expression. Am J Pathol 166: 409–419.
38. Nazli A, Chan O, Dobson-Belaire WN, Ouellet M, Tremblay MJ, et al. (2010) Exposure to HIV-1 directly impairs mucosal epithelial barrier integrity allowing microbial translocation. PLoS Pathog 6: e1000852.
39. Duchmann R, Kaiser I, Hermann E, Mayet W, Ewe K, et al. (1995) Tolerance exists towards resident intestinal flora but is broken in active inflammatory bowel disease (IBD). Clin Exp Immunol 102: 448–455.
40. Nagy LH, Grishina I, Macal M, Hirao LA, Hu WK, et al. (2013) Chronic HIV infection enhances the responsiveness of antigen presenting cells to commensal Lactobacillus. PLoS One 8: e72789.
41. Gekonge B, Giri MS, Kossenkov AV, Nebozyhn M, Yousef M, et al. (2012) Constitutive gene expression in monocytes from chronic HIV-1 infection overlaps with acute Toll-like receptor induced monocyte activation profiles. PLoS One 7: e41153.
42. Hernandez JC, Stevenson M, Latz E, Urcuqui-Inchima S, (2012) HIV type 1 infection up-regulates TLR2 and TLR4 expression and function in vivo and in vitro. AIDS Res Hum Retroviruses 28: 1313–1328.
43. Heggelund L, Muller F, Lien E, Yndestad A, Ueland T, et al. (2004) Increased expression of toll-like receptor 2 on monocytes in HIV infection: possible roles in inflammation and viral replication. Clin Infect Dis 39: 264–269.
44. Karczewski J, Troost FJ, Konings I, Dekker J, Kleerebezem M, et al. (2010) Regulation of human epithelial tight junction proteins by Lactobacillus plantarum in vivo and protective effects on the epithelial barrier. Am J Physiol Gastrointest Liver Physiol 298: G851–859.
45. Anderson RC, Cookson AL, McNabb WC, Park Z, McCann MJ, et al. (2010) Lactobacillus plantarum MB452 enhances the function of the intestinal barrier by increasing the expression levels of genes involved in tight junction formation. BMC Microbiol 10: 316.
46. Liu Z, Shen T, Zhang P, Ma Y, Qin H, (2011) Lactobacillus plantarum surface layer adhesive protein protects intestinal epithelial cells against tight junction injury induced by enteropathogenic Escherichia coli. Mol Biol Rep 38: 3471–3480.
47. van Baarlen P, Troost FJ, van Hemert S, van der Meer C, de Vos WM, et al. (2009) Differential NF-kappaB pathways induction by Lactobacillus plantarum in the duodenum of healthy humans correlating with immune tolerance. Proc Natl Acad Sci U S A 106: 2371–2376.
48. Petrof EO, Claud EC, Sun J, Abramova T, Guo Y, et al. (2009) Bacteria-free solution derived from Lactobacillus plantarum inhibits multiple NF-kappaB pathways and inhibits proteasome function. Inflamm Bowel Dis 15: 1537–1547.
49. Klatt NR, Canary LA, Sun X, Vinton CL, Funderburg NT, et al. (2013) Probiotic/prebiotic supplementation of antiretrovirals improves gastrointestinal immunity in SIV-infected macaques. J Clin Invest 123: 903–907.
50. Gori A, Rizzardini G, Van't Land B, Amor KB, van Schaik J, et al. (2011) Specific prebiotics modulate gut microbiota and immune activation in HAART-naive HIV-infected adults: results of the “COPA” pilot randomized trial. Mucosal Immunol 4: 554–563.
51. Shulzhenko N, Morgun A, Hsiao W, Battle M, Yao M, et al. (2011) Crosstalk between B lymphocytes, microbiota and the intestinal epithelium governs immunity versus metabolism in the gut. Nat Med 17: 1585–1593.
52. Verhoeven D, George MD, Hu W, Dang AT, Smit-McBride Z, et al. (2014) Enhanced innate antiviral gene expression, IFN-alpha, and cytolytic responses are predictive of mucosal immune recovery during simian immunodeficiency virus infection. J Immunol 192: 3308–3318.
53. Macal M, Sankaran S, Chun TW, Reay E, Flamm J, et al. (2008) Effective CD4+ T-cell restoration in gut-associated lymphoid tissue of HIV-infected patients is associated with enhanced Th17 cells and polyfunctional HIV-specific T-cell responses. Mucosal Immunol 1: 475–488.