Comparative Transcriptional Profiling of 3 Murine Models of SLE Nephritis Reveals Both Unique and Shared Regulatory Networks

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Bethunaickan, Ramalingam ^a   Berthier, Celine C ^b   Zhang, Weijia ^c   Kretzler, Matthias ^b   Davidson, Anne ^a  

^a FEINSTEIN INSTITUTE FOR MEDICAL RESEARCH   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATHEPSIN; CD68 ANTIGEN; CHEMOKINE RECEPTOR CCR2; CHEMOKINE RECEPTOR CCR5; CXCL16 CHEMOKINE; CYTOKINE; FC RECEPTOR; FORMYLPEPTIDE RECEPTOR; GAMMA INTERFERON INDUCIBLE PROTEIN 10; HLA DM ANTIGEN; INTERCELLULAR ADHESION MOLECULE 1; KIDNEY INJURY MOLECULE 1; LECTIN; MATRIX METALLOPROTEINASE 14; MONOCYTE CHEMOTACTIC PROTEIN 1; NEPHRIN; NEUTROPHIL GELATINASE ASSOCIATED LIPOCALIN; PROTEASOME; RANTES; STAT3 PROTEIN; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA1; VASCULAR CELL ADHESION MOLECULE 1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING SITE; CELL ACTIVATION; CELL AGGREGATION; CELL INFILTRATION; CELL LOSS; COMPLEMENT CLASSICAL PATHWAY; CONTROLLED STUDY; DENDRITIC CELL; ENDOTHELIUM CELL; ENZYME ACTIVATION; GENE CONTROL; GENE EXPRESSION PROFILING; GENETIC TRANSCRIPTION; HYPOXIA; LUPUS ERYTHEMATOSUS NEPHRITIS; LYMPHOID CELL; MACROPHAGE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMA CELL; PODOCYTE; PROTEIN BINDING; PROTEIN DEPLETION; SIGNAL TRANSDUCTION; T LYMPHOCYTE; TISSUE REGENERATION; ANIMAL; COMPARATIVE STUDY; COMPLEMENT ACTIVATION; DISEASE MODEL; FEMALE; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; MALE; METABOLISM; PATHOLOGY;

ANIMALS; COMPLEMENT ACTIVATION; DENDRITIC CELLS; DISEASE MODELS, ANIMAL; ENDOTHELIAL CELLS; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; LUPUS NEPHRITIS; MACROPHAGES; MALE; MICE; PLASMA CELLS; PODOCYTES; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

EID: 84886030609     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0077489     Document Type: Article

References (55)

1. Theofilopoulos AN, Dixon FJ, (1985) Murine models of systemic lupus erythematosus. Adv Immunol 37: 269-390.
2. Schiffer L, Kumpers P, Davalos-Misslitz AM, Haubitz M, Haller H, et al. (2009) B-cell-attracting chemokine CXCL13 as a marker of disease activity and renal involvement in systemic lupus erythematosus (SLE). Nephrol Dial Transplant 24: 3708-3712.
3. Singh RR, Saxena V, Zang S, Li L, Finkelman FD, et al. (2003) Differential contribution of IL-4 and STAT6 vs STAT4 to the development of lupus nephritis. J Immunol 170: 4818-4825.
4. Pisitkun P, Deane JA, Difilippantonio MJ, Tarasenko T, Satterthwaite AB, et al. (2006) Autoreactive B cell responses to RNA-related antigens due to TLR7 gene duplication. Science 312: 1669-1672.
5. Hang LM, Izui S, Dixon FJ, (1981) (NZW x BXSB)F1 hybrid. A model of acute lupus and coronary vascular disease with myocardial infarction. J Exp Med 154: 216-221.
6. Davidson A, Aranow C, (2010) Lupus nephritis: lessons from murine models. Nat Rev Rheumatol 6: 13-20.
7. Liu Z, Bethunaickan R, Huang W, Ramanujam M, Madaio MP, et al. (2011) IFN-{alpha} Confers Resistance of Systemic Lupus Erythematosus Nephritis to Therapy in NZB/W F1 Mice. J Immunol 187: 1506-1513.
8. Peterson KS, Huang JF, Zhu J, D'Agati V, Liu X, et al. (2004) Characterization of heterogeneity in the molecular pathogenesis of lupus nephritis from transcriptional profiles of laser-captured glomeruli. J Clin Invest 113: 1722-1733.
9. Giannico G, Fogo AB, (2013) Lupus nephritis: is the kidney biopsy currently necessary in the management of lupus nephritis? Clin J Am Soc Nephrol 8: 138-145.
10. Berthier CC, Bethunaickan R, Gonzalez-Rivera T, Nair V, Ramanujam M, et al. (2012) Cross-species transcriptional network analysis defines shared inflammatory responses in murine and human lupus nephritis. J Immunol 189: 988-1001.
11. Schiffer L, Bethunaickan R, Ramanujam M, Huang W, Schiffer M, et al. (2008) Activated renal macrophages are markers of disease onset and disease remission in lupus nephritis. J Immunol 180: 1938-1947.
12. Ramanujam M, Bethunaickan R, Huang W, Tao H, Madaio MP, et al. (2010) Selective blockade of BAFF for the prevention and treatment of systemic lupus erythematosus nephritis in NZM2410 mice. Arthritis Rheum 62: 1457-1468.
13. Bethunaickan R, Berthier CC, Ramanujam M, Sahu R, Zhang W, et al. (2011) A unique hybrid renal mononuclear phagocyte activation phenotype in murine systemic lupus erythematosus nephritis. J Immunol 186: 4994-5003.
14. Saeed AI, Bhagabati NK, Braisted JC, Liang W, Sharov V, et al. (2006) TM4 microarray software suite. Methods Enzymol 411: 134-193.
15. Kahn P, Ramanujam M, Bethunaickan R, Huang W, Tao H, et al. (2008) Prevention of murine antiphospholipid syndrome by BAFF blockade. Arthritis Rheum 58: 2824-2834.
16. Schiffer L, Sinha J, Wang X, Huang W, von Gersdorff G, et al. (2003) Short term administration of costimulatory blockade and cyclophosphamide induces remission of systemic lupus erythematosus nephritis in NZB/W F1 mice by a mechanism downstream of renal immune complex deposition. J Immunol 171: 489-497.
17. Hotta K, Sho M, Yamato I, Shimada K, Harada H, et al. (2011) Direct targeting of fibroblast growth factor-inducible 14 protein protects against renal ischemia reperfusion injury. Kidney Int 79: 179-188.
18. Matsuura K, Uesugi N, Hijiya N, Uchida T, Moriyama M, (2007) Upregulated expression of cardiac ankyrin-repeated protein in renal podocytes is associated with proteinuria severity in lupus nephritis. Hum Pathol 38: 410-419.
19. Fornoni A, Sageshima J, Wei C, Merscher-Gomez S, Aguillon-Prada R, et al. (2011) Rituximab targets podocytes in recurrent focal segmental glomerulosclerosis. Sci Transl Med 3: 85ra46.
20. Der SD, Zhou A, Williams BR, Silverman RH, (1998) Identification of genes differentially regulated by interferon alpha, beta, or gamma using oligonucleotide arrays. Proc Natl Acad Sci U S A 95: 15623-15628.
21. Baechler EC, Batliwalla FM, Karypis G, Gaffney PM, Ortmann WA, et al. (2003) Interferon-inducible gene expression signature in peripheral blood cells of patients with severe lupus. Proc Natl Acad Sci U S A 100: 2610-2615.
22. Liu J, Karypis G, Hippen KL, Vegoe AL, Ruiz P, et al. (2006) Genomic view of systemic autoimmunity in MRLlpr mice. Genes Immun 7: 156-168.
23. Karpurapu M, Wang X, Deng J, Park H, Xiao L, et al. (2011) Functional PU.1 in macrophages has a pivotal role in NF-kappaB activation and neutrophilic lung inflammation during endotoxemia. Blood 118: 5255-5266.
24. Huber R, Pietsch D, Panterodt T, Brand K, (2012) Regulation of C/EBPbeta and resulting functions in cells of the monocytic lineage. Cell Signal 24: 1287-1296.
25. Pedersen A, Skjong C, Shawlot W, (2005) Lim 1 is required for nephric duct extension and ureteric bud morphogenesis. Dev Biol 288: 571-581.
26. Chiang CK, Hsu SP, Wu CT, Huang JW, Cheng HT, et al. (2011) Endoplasmic reticulum stress implicated in the development of renal fibrosis. Mol Med 17: 1295-1305.
27. Wang Y, Barbacioru C, Hyland F, Xiao W, Hunkapiller KL, et al. (2006) Large scale real-time PCR validation on gene expression measurements from two commercial long-oligonucleotide microarrays. BMC Genomics 7: 59.
28. Gachon F, Olela FF, Schaad O, Descombes P, Schibler U, (2006) The circadian PAR-domain basic leucine zipper transcription factors DBP, TEF, and HLF modulate basal and inducible xenobiotic detoxification. Cell Metab 4: 25-36.
29. Matsui F, Meldrum KK, (2012) The role of the Janus kinase family/signal transducer and activator of transcription signaling pathway in fibrotic renal disease. J Surg Res 178: 339-345.
30. Lu LD, Stump KL, Wallace NH, Dobrzanski P, Serdikoff C, et al. (2011) Depletion of autoreactive plasma cells and treatment of lupus nephritis in mice using CEP-33779, a novel, orally active, selective inhibitor of JAK2. J Immunol 187: 3840-3853.
31. Ichii O, Otsuka S, Sasaki N, Yabuki A, Ohta H, et al. (2010) Local overexpression of interleukin-1 family, member 6 relates to the development of tubulointerstitial lesions. Lab Invest 90: 459-475.
32. Blumberg H, Dinh H, Trueblood ES, Pretorius J, Kugler D, et al. (2007) Opposing activities of two novel members of the IL-1 ligand family regulate skin inflammation. J Exp Med 204: 2603-2614.
33. Greter M, Lelios I, Pelczar P, Hoeffel G, Price J, et al. (2012) Stroma-derived interleukin-34 controls the development and maintenance of langerhans cells and the maintenance of microglia. Immunity 37: 1050-1060.
34. Wang Y, Szretter KJ, Vermi W, Gilfillan S, Rossini C, et al. (2012) IL-34 is a tissue-restricted ligand of CSF1R required for the development of Langerhans cells and microglia. Nat Immunol 13: 753-760.
35. Zykova SN, Tveita AA, Rekvig OP (2010) Renal Dnase1 enzyme activity and protein expression is selectively shut down in murine and human membranoproliferative lupus nephritis. PLoS One 5.
36. Fismen S, Mortensen ES, Rekvig OP, (2011) Nuclease deficiencies promote end-stage lupus nephritis but not nephritogenic autoimmunity in (NZB x NZW) F1 mice. Immunol Cell Biol 89: 90-99.
37. Kelkka T, Laurila JP, Sareila O, Olofsson P, Laukkanen MO, et al. (2012) Superoxide dismutase 3 limits collagen-induced arthritis in the absence of phagocyte oxidative burst. Mediators Inflamm 2012: 730469.
38. Richters L, Lange N, Renner R, Treiber N, Ghanem A, et al. (2011) Exercise-induced adaptations of cardiac redox homeostasis and remodeling in heterozygous SOD2-knockout mice. J Appl Physiol 111: 1431-1440.
39. Hill GS, Delahousse M, Nochy D, Remy P, Mignon F, et al. (2001) Predictive power of the second renal biopsy in lupus nephritis: significance of macrophages. Kidney Int 59: 304-316.
40. Hsieh C, Chang A, Brandt D, Guttikonda R, Utset TO, et al. (2011) Predicting outcomes of lupus nephritis with tubulointerstitial inflammation and scarring. Arthritis Care Res (Hoboken) 63: 865-874.
41. Villanueva E, Yalavarthi S, Berthier CC, Hodgin JB, Khandpur R, et al. (2011) Netting neutrophils induce endothelial damage, infiltrate tissues, and expose immunostimulatory molecules in systemic lupus erythematosus. J Immunol 187: 538-552.
42. Rerolle JP, Hertig A, Nguyen G, Sraer JD, Rondeau EP, (2000) Plasminogen activator inhibitor type 1 is a potential target in renal fibrogenesis. Kidney Int 58: 1841-1850.
43. Rinn JL, Rozowsky JS, Laurenzi IJ, Petersen PH, Zou K, et al. (2004) Major molecular differences between mammalian sexes are involved in drug metabolism and renal function. Dev Cell 6: 791-800.
44. Palm F, Nordquist L, (2011) Renal oxidative stress, oxygenation, and hypertension. Am J Physiol Regul Integr Comp Physiol 301: R1229-1241.
45. Martin-Martin N, Ryan G, McMorrow T, Ryan MP, (2010) Sirolimus and cyclosporine A alter barrier function in renal proximal tubular cells through stimulation of ERK1/2 signaling and claudin-1 expression. Am J Physiol Renal Physiol 298: F672-682.
46. Yasuda T, Saegusa C, Kamakura S, Sumimoto H, Fukuda M, (2012) Rab27 effector Slp2-a transports the apical signaling molecule podocalyxin to the apical surface of MDCK II cells and regulates claudin-2 expression. Mol Biol Cell 23: 3229-3239.
47. Jeong S, Ledee DR, Gordon GM, Itakura T, Patel N, et al. (2012) Interaction of clusterin and matrix metalloproteinase-9 and its implication for epithelial homeostasis and inflammation. Am J Pathol 180: 2028-2039.
48. Ueland JM, Gwira J, Liu ZX, Cantley LG, (2004) The chemokine KC regulates HGF-stimulated epithelial cell morphogenesis. Am J Physiol Renal Physiol 286: F581-589.
49. Chang A, Henderson SG, Brandt D, Liu N, Guttikonda R, et al. (2011) In situ B cell-mediated immune responses and tubulointerstitial inflammation in human lupus nephritis. J Immunol 186: 1849-1860.
50. Petrzilka S, Taraborrelli C, Cavadini G, Fontana A, Birchler T, (2009) Clock gene modulation by TNF-alpha depends on calcium and p38 MAP kinase signaling. J Biol Rhythms 24: 283-294.
51. Kon N, Hirota T, Kawamoto T, Kato Y, Tsubota T, et al. (2008) Activation of TGF-beta/activin signalling resets the circadian clock through rapid induction of Dec1 transcripts. Nat Cell Biol 10: 1463-1469.
52. Hashiramoto A, Yamane T, Tsumiyama K, Yoshida K, Komai K, et al. (2010) Mammalian clock gene Cryptochrome regulates arthritis via proinflammatory cytokine TNF-alpha. J Immunol 184: 1560-1565.
53. Liu N, Wang Y, Ashton-Rickardt PG, (2004) Serine protease inhibitor 2A inhibits caspase-independent cell death. FEBS Lett 569: 49-53.
54. Turgeon J, Haddad P, Dussault S, Groleau J, Maingrette F, et al. (2012) Protection against vascular aging in Nox2-deficient mice: Impact on endothelial progenitor cells and reparative neovascularization. Atherosclerosis 223: 122-129.
55. Jung GS, Kim MK, Jung YA, Kim HS, Park IS, et al. (2012) Clusterin attenuates the development of renal fibrosis. J Am Soc Nephrol 23: 73-85.