An Lck-cre transgene accelerates autoantibody production and lupus development in (NZB × NZW)F1 mice

Lupus

Volumn 25, Issue 2, 2016, Pages 137-154

  Nelson, R K ^a   Gould, K A ^a  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

(NZB NZW)F1 mice; autoantibodies; cre toxicity; lupus; T cell apoptosis

Indexed keywords

AUTOANTIBODY; CELL NUCLEUS ANTIGEN; CRE RECOMBINASE; PROTEIN KINASE LCK; ANTIGEN ANTIBODY COMPLEX; INTEGRASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY PRODUCTION; APOPTOSIS; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; DISEASE COURSE; FEMALE; LUPUS VULGARIS; MALE; MOUSE; NEPHRITIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRANSGENE; ALLELE; ANIMAL; ANTIGEN ANTIBODY COMPLEX; BIOSYNTHESIS; DISEASE MODEL; GENETICS; IMMUNOLOGY; LUPUS ERYTHEMATOSUS NEPHRITIS; METABOLISM; NEW ZEALAND BLACK MOUSE; PATHOLOGY; SEQUENCE ANALYSIS; T LYMPHOCYTE; TRANSGENIC MOUSE;

ALLELES; ANIMALS; ANTIGEN-ANTIBODY COMPLEX; APOPTOSIS; AUTOANTIBODIES; DISEASE MODELS, ANIMAL; FEMALE; INTEGRASES; LUPUS NEPHRITIS; MALE; MICE; MICE, INBRED NZB; MICE, TRANSGENIC; SEQUENCE ANALYSIS; T-LYMPHOCYTES; TRANSGENES;

EID: 84954202079     PISSN: 09612033     EISSN: 14770962     Source Type: Journal    
DOI: 10.1177/0961203315603139     Document Type: Article

References (54)

1. Dhir V, Singh AP, Aggarwal A, Naik S, Misra R,. Increased T-lymphocyte apoptosis in lupus correlates with disease activity and may be responsible for reduced T cell frequency: a cross-sectional and longitudinal study. Lupus 2009; 18: 785-791.
2. Funauchi M, Sugiyama M, SukYoo B, et al. A possible role of apoptosis for regulating autoreactive responses in systemic lupus erythematosus. Lupus 2001; 10: 284-288.
3. Grondal G, Traustadottir KH, Kristjansdottir H, et al. Increased T-lymphocyte apoptosis/necrosis and IL-10 producing cells in patients and their spouses in Icelandic systemic lupus erythematosus multicase families. Lupus 2002; 11: 435-442.
4. Perniok A, Wedekind F, Herrmann M, Specker C, Schneider M,. High levels of circulating early apoptic peripheral blood mononuclear cells in systemic lupus erythematosus. Lupus 1998; 7: 113-118.
5. Wang H, Xu J, Ji X, et al. The abnormal apoptosis of T cell subsets and possible involvement of IL-10 in systemic lupus erythematosus. Cell Immunol 2005; 235: 117-121.
6. Trebeden-Negre H, Weill B, Fournier C, Batteux F,. B cell apoptosis accelerates the onset of murine lupus. Eur J Immunol 2003; 33: 1603-1612.
7. Licht R, Dieker JWC, Jacobs CWM, Tax WJM, Berden JHM,. Decreased phagocytosis of apoptotic cells in diseased SLE mice. J Autoimmun 2004; 22: 139-145.
8. Herrmann M, Voll RE, Zoller OM, Hagenhofer M, Ponner BB, Kalden JR,. Impaired phagocytosis of apoptotic cell material by monocyte-derived macrophages from patients with systemic lupus erythematosus. Arthritis Rheum 1998; 41: 1241-1250.
9. Potter PK, Cortes-Hernandez J, Quartier P, Botto M, Walport MJ,. Lupus-prone mice have an abnormal response to thioglycolate and an impaired clearance of apoptotic cells. J Immunol 2003; 170: 3223-3232.
10. Denny MF, Chandaroy P, Killen PD, et al. Accelerated macrophage apoptosis induces autoantibody formation and organ damage in systemic lupus erythematosus. J Immunol 2006; 176: 2095-2104.
11. Dieker JW, van der Vlag J, Berden JH,. Deranged removal of apoptotic cells: its role in the genesis of lupus. Nephrol Dial Transplant 2004; 19: 282-285.
12. Rodriguez-Manzanet R, Sanjuan MA, Wu HY, et al. T and B cell hyperactivity and autoimmunity associated with niche-specific defects in apoptotic body clearance in TIM-4-deficient mice. Proc Natl Acad Sci USA 2010; 107: 8706-8711.
13. Shao X, Yang R, Yan M, et al. Inducible expression of kallikrein in renal tubular cells protects mice against spontaneous lupus nephritis. Arthritis Rheum 2013; 65: 780-791.
14. Hwang SH, Lee H, Yamamoto M, et al. B cell TLR7 expression drives anti-RNA autoantibody production and exacerbates disease in systemic lupus erythematosus-prone mice. J Immunol 2012; 189: 5786-5796.
15. Teichmann LL, Ols ML, Kashgarian M, Reizis B, Kaplan DH, Shlomchik MJ,. Dendritic cells in lupus are not required for activation of T and B cells but promote their expansion, resulting in tissue damage. Immunity 2010; 33: 967-978.
16. Loonstra A, Vooijs M, Beverloo HB, et al. Growth inhibition and DNA damage induced by Cre recombinase in mammalian cells. Proc Natl Acad Sci USA 2001; 98: 9209-9214.
17. Silver DP, Livingston DM,. Self-excising retroviral vectors encoding the Cre recombinase overcome Cre-mediated cellular toxicity. Mol Cell 2001; 8: 233-243.
18. Janbandhu VC, Moik D, Fassler R,. Cre recombinase induces DNA damage and tetraploidy in the absence of loxP sites. Cell Cycle 2014; 13: 462-470.
19. Schmidt EE, Taylor DS, Prigge JR, Barnett S, Capecchi MR,. Illegitimate Cre-dependent chromosome rearrangements in transgenic mouse spermatids. Proc Natl Acad Sci USA 2000; 97: 13702-13707.
20. Higashi AY, Ikawa T, Muramatsu M, et al. Direct hematological toxicity and illegitimate chromosomal recombination caused by the systemic activation of CreERT2. J Immunol 2009; 182: 5633-5640.
21. Jeannotte L, Aubin J, Bourque S, Lemieux M, Montaron S, Provencher St-Pierre A,. Unsuspected effects of a lung-specific Cre deleter mouse line. Genesis 2011; 49: 152-159.
22. Naiche LA, Papaioannou VE,. Cre activity causes widespread apoptosis and lethal anemia during embryonic development. Genesis 2007; 45: 768-775.
23. Zheng B, Sage M, Sheppeard EA, Jurecic V, Bradley A,. Engineering mouse chromosomes with Cre-loxP: range, efficiency, and somatic applications. Mol Cell Biol 2000; 20: 648-655.
24. Semprini S, Troup TJ, Kotelevtseva N, et al. Cryptic loxP sites in mammalian genomes: genome-wide distribution and relevance for the efficiency of BAC/PAC recombineering techniques. Nucleic Acids Res 2007; 35: 1402-1410.
25. Thyagarajan B, Guimaraes MJ, Groth AC, Calos MP,. Mammalian genomes contain active recombinase recognition sites. Gene 2000; 244: 47-54.
26. Ramirez-Solis R, Liu P, Bradley A,. Chromosome engineering in mice. Nature 1995; 378: 720-724.
27. Lee JY, Ristow M, Lin X, White MF, Magnuson MA, Hennighausen L,. RIP-Cre revisited, evidence for impairments of pancreatic beta-cell function. J Biol Chem 2006; 281: 2649-2653.
28. Guo F, Cancelas JA, Hildeman D, Williams DA, Zheng Y,. Rac GTPase isoforms Rac1 and Rac2 play a redundant and crucial role in T cell development. Blood 2008; 112: 1767-1775.
29. Gubbels Bupp MR, Edwards B, Guo C, et al. T cells require Foxo1 to populate the peripheral lymphoid organs. Eur J Immunol 2009; 39: 2991-2999.
30. Stephensen CB, Borowsky AD, Lloyd KC,. Disruption of Rxra gene in thymocytes and T lymphocytes modestly alters lymphocyte frequencies, proliferation, survival and T helper type 1/type 2 balance. Immunology 2007; 121: 484-498.
31. Hennet T, Hagen FK, Tabak LA, Marth JD,. T cell-specific deletion of a polypeptide N-acetylgalactosaminyl-transferase gene by site-directed recombination. Proc Natl Acad Sci USA 1995; 92: 12070-12074.
32. Bynoté KK, Hackenberg JM, Korach KS, Lubahn DB, Lane PH, Gould KA,. Estrogen receptor-alpha deficiency attenuates autoimmune disease in (NZB x NZW)F1 mice. Genes Immun 2008; 9: 137-152.
33. Dupont S, Krust A, Gansmuller A, Dierich A, Chambon P, Mark M,. Effect of single and compound knockouts of estrogen receptors alpha (ERalpha) and beta (ERbeta) on mouse reproductive phenotypes. Development 2000; 127: 4277-4291.
34. Hewitt SC, O'Brien JE, Jameson JL, Kissling GE, Korach KS,. Selective disruption of ER{alpha} DNA-binding activity alters uterine responsiveness to estradiol. Mol Endocrinol 2009; 23: 2111-2116.
35. Lubahn DB, Moyer JS, Golding TS, Couse JF, Korach KS, Smithies O,. Alteration of reproductive function but not prenatal sexual development after insertional disruption of the mouse estrogen receptor gene. Proc Natl Acad Sci U S A 1993; 90: 11162-11166.
36. Mohan C, Adams S, Stanik V, Datta SK,. Nucleosome: a major immunogen for pathogenic autoantibody-inducing T cells of lupus. J Exp Med 1993; 177: 1367-1381.
37. Burlingame RW, Rubin RL,. Subnucleosome structures as substrates in enzyme-linked immunosorbent assays. J Immunol Methods 1990; 134: 187-199.
38. Drake CG, Babcock SK, Palmer E, Kotzin BL,. Genetic analysis of the NZB contribution to lupus-like autoimmune disease in (NZB x NZW)F1 mice. Proc Natl Acad Sci U S A 1994; 91: 4062-4066.
39. Drake CG, Rozzo SJ, Hirschfeld HF, Smarnworawong NP, Palmer E, Kotzin BL,. Analysis of the New Zealand Black contribution to lupus-like renal disease. Multiple genes that operate in a threshold manner. J Immunol 1995; 154: 2441-2447.
40. Rozzo SJ, Vyse TJ, Drake CG, Kotzin BL,. Effect of genetic background on the contribution of New Zealand black loci to autoimmune lupus nephritis. Proc Natl Acad Sci USA 1996; 93: 15164-15168.
41. Vyse TJ, Morel L, Tanner FJ, Wakeland EK, Kotzin BL,. Backcross analysis of genes linked to autoantibody production in New Zealand White mice. J Immunol 1996; 157: 2719-2727.
42. Kotzin BL, Palmer E,. The contribution of NZW genes to lupus-like disease in (NZB x NZW)F1 mice. J Exp Med 1987; 165: 1237-1251.
43. Shi J, Petrie HT,. Activation kinetics and off-target effects of thymus-initiated cre transgenes. PLoS ONE 2012; 7: e46590.
44. Orban PC, Chui D, Marth JD,. Tissue- and site-specific DNA recombination in transgenic mice. Proc Natl Acad Sci U S A 1992; 89: 6861-6865.
45. Cao Y, Li H, Liu H, Zhang M, Hua Z, Ji H, et al. LKB1 regulates TCR-mediated PLCgamma1 activation and thymocyte positive selection. EMBO J 2011; 30: 2083-2093.
46. Gupta A, Hunt CR, Pandita RK, et al. T cell-specific deletion of Mof blocks their differentiation and results in genomic instability in mice. Mutagenesis 2013; 28: 263-270.
47. Reiss C, Haneke T, Volker HU, et al. Conditional inactivation of MLH1 in thymic and naive T cells in mice leads to a limited incidence of lymphoblastic T cell lymphomas. Leuk Lymphoma 2010; 51: 1875-1886.
48. Bassi C, Xavier D, Palomino G, et al. Efficiency of the DNA repair and polymorphisms of the XRCC1, XRCC3 and XRCC4 DNA repair genes in systemic lupus erythematosus. Lupus 2008; 17: 988-995.
49. Li Y, Choi PS, Casey SC, Felsher DW,. Activation of cre recombinase alone can induce complete tumor regression. PLoS One 2014; 9: e107589.
50. Chung SH, Seki K, Choi BI, et al. CXC chemokine receptor 4 expressed in T cells plays an important role in the development of collagen-induced arthritis. Arthritis Res Ther 2010; 12: R188.
51. Gaidarenko O, Xu Y,. Transcription activity is required for p53-dependent tumor suppression. Oncogene 2009; 28: 4397-4401.
52. Liu Y, Johnson SM, Fedoriw Y, et al. Expression of p16(INK4a) prevents cancer and promotes aging in lymphocytes. Blood 2011; 117: 3257-3267.
53. Wong WF, Nakazato M, Watanabe T, et al. Over-expression of Runx1 transcription factor impairs the development of thymocytes from the double-negative to double-positive stages. Immunology 2010; 130: 243-253.
54. Chang HC, Han L, Jabeen R, Carotta S, Nutt SL, Kaplan MH,. PU.1 regulates TCR expression by modulating GATA-3 activity. J Immunol 2009; 183: 4887-4894.