Guanylate-binding protein 1 (GBP1) contributes to the immunity of human mesenchymal stromal cells against Toxoplasma gondii

Proceedings of the National Academy of Sciences of the United States of America

Volumn 114, Issue 6, 2017, Pages 1365-1370

  Qin, Aiping ^a,b   Lai, De Hua ^c   Liu, Qifa ^a   Huang, Weijun ^b,c   Wu, Ya Ping ^c   Chen, Xiaoyong ^b,c   Yan, Sunxing ^b,c   Xia, Huimin ^b   Hide, Geoff ^d   Lun, Zhao Rong ^c,d   Ayala, Francisco J ^e   Xiang, Andy Peng ^b,c  

^a SOUTHERN MEDICAL UNIVERSITY   (China)

^b SUN YAT SEN UNIVERSITY   (China)

^c SUN YAT SEN UNIVERSITY   (China)

^d UNIVERSITY OF SALFORD   (United Kingdom)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Human stem cells; In vitro cultivation; Innate immunity; Parasitic protozoan

Indexed keywords

GAMMA INTERFERON; GREEN FLUORESCENT PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN 1; INDOLEAMINE 2,3 DIOXYGENASE; UNCLASSIFIED DRUG; GBP1 PROTEIN, HUMAN; PHOTOPROTEIN;

ARTICLE; CELLULAR IMMUNITY; CONTROLLED STUDY; GENETIC TRANSFECTION; GROWTH INHIBITION; HELA CELL LINE; HOST RESISTANCE; HUMAN; HUMAN CELL; IN VITRO STUDY; INNATE IMMUNITY; MEMBRANE STRUCTURE; MESENCHYMAL STROMA CELL; NONHUMAN; PREPUCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SEQUENCE; SIGNAL TRANSDUCTION; SOMATIC CELL; TOXOPLASMA GONDII; WESTERN BLOTTING; ANIMAL; CELL CULTURE; CELL VACUOLE; CYTOLOGY; DRUG EFFECTS; FIBROBLAST; GENE EXPRESSION; GENETICS; HOST PARASITE INTERACTION; IMMUNOLOGY; MAMMALIAN EMBRYO; METABOLISM; MOUSE; PARASITOLOGY; PHYSIOLOGY; RNA INTERFERENCE; TOXOPLASMA;

ANIMALS; CELLS, CULTURED; EMBRYO, MAMMALIAN; FIBROBLASTS; GENE EXPRESSION; GTP-BINDING PROTEINS; HELA CELLS; HOST-PARASITE INTERACTIONS; HUMANS; INTERFERON-GAMMA; LUMINESCENT PROTEINS; MESENCHYMAL STROMAL CELLS; MICE; RNA INTERFERENCE; TOXOPLASMA; VACUOLES;

EID: 85011698062     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1619665114     Document Type: Article

References (53)

1. Balan A, et al. (2014) Mesenchymal stromal cells in the antimicrobial host response of hematopoietic stem cell recipients with graft-versus-host disease-friends or foes? Leukemia 28(10):1941-1948.
2. Auletta JJ, Deans RJ, Bartholomew AM (2012) Emerging roles for multipotent, bone marrow-derived stromal cells in host defense. Blood 119(8):1801-1809.
3. Paquet-Fifield S, et al. (2009) A role for pericytes as microenvironmental regulators of human skin tissue regeneration. J Clin Invest 119(9):2795-2806.
4. Krasnodembskaya A, et al. (2010) Antibacterial effect of human mesenchymal stem cells is mediated in part from secretion of the antimicrobial peptide LL-37. Stem Cells 28(12):2229-2238.
5. Németh K, et al. (2009) Bone marrow stromal cells attenuate sepsis via prostaglandin E(2)-dependent reprogramming of host macrophages to increase their interleukin-10 production. Nat Med 15(1):42-49.
6. Gonzalez-Rey E, et al. (2009) Human adult stem cells derived from adipose tissue protect against experimental colitis and sepsis. Gut 58(7):929-939.
7. Wong JH, et al. (2011) Antifungal action of human cathelicidin fragment (LL13-37) on Candida albicans. Peptides 32(10):1996-2002.
8. Gupta N, et al. (2012) Mesenchymal stem cells enhance survival and bacterial clearance in murine Escherichia coli pneumonia. Thorax 67(6):533-539.
9. Meisel R, et al. (2011) Human but not murine multipotent mesenchymal stromal cells exhibit broad-spectrum antimicrobial effector function mediated by indoleamine 2, 3- dioxygenase. Leukemia 25(4):648-654.
10. Hall SR, et al. (2013) Mesenchymal stromal cells improve survival during sepsis in the absence of heme oxygenase-1: The importance of neutrophils. Stem Cells 31(2):397-407.
11. Mei SH, et al. (2010) Mesenchymal stemcells reduce inflammation while enhancing bacterial clearance and improving survival in sepsis. Am J Respir Crit Care Med 182(8):1047-1057.
12. Yarovinsky F (2014) Innate immunity to Toxoplasma gondii infection. Nat Rev Immunol 14(2):109-121.
13. Suzuki Y, Orellana MA, Schreiber RD, Remington JS (1988) Interferon-gamma: The major mediator of resistance against Toxoplasma gondii. Science 240(4851):516-518.
14. Sturge CR, Yarovinsky F (2014) Complex immune cell interplay in the gamma interferon response during Toxoplasma gondii infection. Infect Immun 82(8):3090-3097.
15. Li Z, et al. (2012) Differences in iNOS and arginase expression and activity in the macrophages of rats are responsible for the resistance against T. gondii infection. PLoS One 7(4):e35834.
16. Murray HW, Juangbhanich CW, Nathan CF, Cohn ZA (1979) Macrophage oxygendependent antimicrobial activity. II. The role of oxygen intermediates. J Exp Med 150(4):950-964.
17. Howard JC, Hunn JP, Steinfeldt T (2011) The IRG protein-based resistance mechanism in mice and its relation to virulence in Toxoplasma gondii. Curr OpinMicrobiol 14(4):414-421.
18. Yamamoto M, et al. (2012) A cluster of interferon-γ-inducible p65 GTPases plays a critical role in host defense against Toxoplasma gondii. Immunity 37(2):302-313.
19. Kim BH, et al. (2011) A family of IFN-γ-inducible 65-kD GTPases protects against bacterial infection. Science 332(6030):717-721.
20. Murray HW, Teitelbaum RF (1992) L-Arginine-dependent reactive nitrogen intermediates and the antimicrobial effect of activated human mononuclear phagocytes. J Infect Dis 165(3):513-517.
21. Pfefferkorn ER (1984) Interferon gamma blocks the growth of Toxoplasma gondii in human fibroblasts by inducing the host cells to degrade tryptophan. Proc Natl Acad Sci USA 81(3):908-912.
22. Niedelman W, Sprokholt JK, Clough B, Frickel EM, Saeij JP (2013) Cell death of gamma interferon-stimulated human fibroblasts upon Toxoplasma gondii infection induces early parasite egress and limits parasite replication. Infect Immun 81(12):4341-4349.
23. Ribitsch I, et al. (2010) Basic science and clinical application of stem cells in veterinary medicine. Adv Biochem Eng Biotechnol 123:219-263.
24. Schmidt SK, et al. (2009) Antimicrobial and immunoregulatory properties of human tryptophan 2, 3-dioxygenase. Eur J Immunol 39(10):2755-2764.
25. Degrandi D, et al. (2013) Murine guanylate binding protein 2 (mGBP2) controls Toxoplasma gondii replication. Proc Natl Acad Sci USA 110(1):294-299.
26. Selleck EM, et al. (2013) Guanylate-binding protein 1 (Gbp1) contributes to cellautonomous immunity against Toxoplasma gondii. PLoS Pathog 9(4):e1003320.
27. Takács AC, Swierzy IJ, Lüder CG (2012) Interferon-γ restricts Toxoplasma gondii development in murine skeletal muscle cells via nitric oxide production and immunityrelated GTPases. PLoS One 7(9):e45440.
28. Dai W, Pan H, Kwok O, Dubey JP (1994) Human indoleamine 2, 3-dioxygenase inhibits Toxoplasma gondii growth in fibroblast cells. J Interferon Res 14(6):313-317.
29. Gazzinelli RT, Mendonça-Neto R, Lilue J, Howard J, Sher A (2014) Innate resistance against Toxoplasma gondii: An evolutionary tale of mice, cats, and men. Cell Host Microbe 15(2):132-138.
30. Zhao ZJ, et al. (2013) Lower expression of inducible nitric oxide synthase and higher expression of arginase in rat alveolar macrophages are linked to their susceptibility to Toxoplasma gondii infection. PLoS One 8(5):e63650.
31. Gao JM, et al. (2015) Investigation of infectivity of neonates and adults from different rat strains to Toxoplasma gondii Prugniaud shows both variation which correlates with iNOS and Arginase-1 activity and increased susceptibility of neonates to infection. Exp Parasitol 149:47-53.
32. Martens S, et al. (2005) Disruption of Toxoplasma gondii parasitophorous vacuoles by the mouse p47-resistance GTPases. PLoS Pathog 1(3):e24.
33. Bekpen C, et al. (2005) The interferon-inducible p47 (IRG) GTPases in vertebrates: Loss of the cell autonomous resistance mechanism in the human lineage. Genome Biol 6(11):R92.
34. Khaminets A, et al. (2010) Coordinated loading of IRG resistance GTPases on to the Toxoplasma gondii parasitophorous vacuole. Cell Microbiol 12(7):939-961.
35. Haldar AK, et al. (2013) IRG and GBP host resistance factors target aberrant, "non-self" vacuoles characterized by themissing of "self" IRGM proteins. PLoS Pathog 9(6):e1003414.
36. Meunier E, et al. (2015) Guanylate-binding proteins promote activation of the AIM2 inflammasome during infection with Francisella novicida. Nat Immunol 16(5):476-484.
37. Prakash B, Praefcke GJ, Renault L, Wittinghofer A, Herrmann C (2000) Structure of human guanylate-binding protein 1 representing a unique class of GTP-binding proteins. Nature 403(6769):567-571.
38. Li M, et al. (2011) Guanylate binding protein 1 is a novel effector of EGFR-driven invasion in glioblastoma. J Exp Med 208(13):2657-2673.
39. Naschberger E, et al. (2011) Increased expression of guanylate binding protein-1 in lesional skin of patients with cutaneous lupus erythematosus. Exp Dermatol 20(2):102-106.
40. Britzen-Laurent N, et al. (2013) GBP-1 acts as a tumor suppressor in colorectal cancer cells. Carcinogenesis 34(1):153-162.
41. Itsui Y, et al. (2009) Antiviral effects of the interferon-induced protein guanylate binding protein 1 and its interaction with the hepatitis C virus NS5B protein. Hepatology 50(6):1727-1737.
42. Degrandi D, et al. (2007) Extensive characterization of IFN-induced GTPases mGBP1 to mGBP10 involved in host defense. J Immunol 179(11):7729-7740.
43. Nantais DE, Schwemmle M, Stickney JT, Vestal DJ, Buss JE (1996) Prenylation of an interferon-gamma-induced GTP-binding protein: The human guanylate binding protein, huGBP1. J Leukoc Biol 60(3):423-431.
44. Haldar AK, et al. (2015) Ubiquitin systems mark pathogen-containing vacuoles as targets for host defense by guanylate binding proteins. Proc Natl Acad Sci USA 112(41):E5628-E5637.
45. Ohshima J, et al. (2014) Role of mouse and human autophagy proteins in IFN-γ-induced cell-Autonomous responses against Toxoplasma gondii. J Immunol 192(7): 3328-3335.
46. Lun ZR, et al. (2015) Cancer in the parasitic protozoans Trypanosoma brucei and Toxoplasma gondii. Proc Natl Acad Sci U S A 112(29):8835-8842.
47. Peng Y, et al. (2015) Mesenchymal stromal cells infusions improve refractory chronic graft versus host disease through an increase of CD5+ regulatory B cells producing interleukin 10. Leukemia 29(3):636-646.
48. Takahashi K, Yamanaka S (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126(4):663-676.
49. Liu J, et al. (2014) Islet-1 overexpression in human mesenchymal stem cells promotes vascularization throughmonocyte chemoattractant protein-3. Stem Cells 32(7):1843-1854.
50. Nishikawa Y, et al. (2003) Characterisation of Toxoplasma gondii engineered to express mouse interferon-gamma. Int J Parasitol 33(13):1525-1535.
51. Takashima Y, et al. (2008) Detection of the initial site of Toxoplasma gondii reactivation in brain tissue. Int J Parasitol 38(5):601-607.
52. Dominici M, et al. (2006) Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8(4):315-317.
53. Yan X, Ji Y, Liu X, Suo X (2015) Nitric oxide stimulates early egress of Toxoplasma gondii tachyzoites from Human foreskin fibroblast cells. Parasit Vectors 8(8):420.