Preferential production of G-CSF by a protein-like Lactobacillus rhamnosus GR-1 secretory factor through activating TLR2-dependent signaling events without activation of JNKs

BMC Microbiology

Volumn 15, Issue 1, 2015, Pages

  Meshkibaf, Shahab ^a   Fritz, Jörg ^b   Gottschalk, Marcelo ^c   Kim, Sung Ouk ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

Akt; ERKs; G CSF; Lactobacillus rhamnosus GR 1; Macrophage; NF B; TLR2

Indexed keywords

CXCL1 CHEMOKINE; CXCL11 CHEMOKINE; CXCL3 CHEMOKINE; CXCL9 CHEMOKINE; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GRANULOCYTE COLONY STIMULATING FACTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 5; PROTEIN KINASE B; RANTES; STRESS ACTIVATED PROTEIN KINASE; SYNAPTOPHYSIN; TOLL LIKE RECEPTOR 2; TUMOR NECROSIS FACTOR ALPHA; TLR2 PROTEIN, MOUSE; VIRULENCE FACTOR;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME ACTIVATION; FEMALE; GENE EXPRESSION; LACTOBACILLUS RHAMNOSUS; LACTOBACILLUS RHAMNOSUS GR 1; MALE; MOUSE; NONHUMAN; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN INDUCTION; SIGNAL TRANSDUCTION; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CELL CULTURE; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION PROFILING; IMMUNOLOGY; KNOCKOUT MOUSE; MACROPHAGE; METABOLISM; MICROBIOLOGY; POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CELLS, CULTURED; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; GENE EXPRESSION PROFILING; GRANULOCYTE COLONY-STIMULATING FACTOR; LACTOBACILLUS RHAMNOSUS; MACROPHAGES; MALE; MICE, INBRED C57BL; MICE, KNOCKOUT; POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 2; VIRULENCE FACTORS;

EID: 84945264362     PISSN: None     EISSN: 14712180     Source Type: Journal    
DOI: 10.1186/s12866-015-0578-2     Document Type: Article

References (95)

1. Klein M, Sanders ME, Duong T, Young HA. Probiotics: from bench to market. Ann N Y Acad Sci. 2010;1212 Suppl 1:E1-14.
2. Reid G, Younes JA, Van der Mei HC, Gloor GB, Knight R, Busscher HJ. Microbiota restoration: natural and supplemented recovery of human microbial communities. Nat Rev Microbiol. 2010;9(1):27-38.
3. Holzapfel WH, Haberer P, Snel J, Schillinger U, Huis in't Veld JH. Overview of gut flora and probiotics. Int J Food Microbiol. 1998;41(2):85-101.
4. Ravel J, Gajer P, Abdo Z, Schneider GM, Koenig SS, McCulle SL, et al. Vaginal microbiome of reproductive-age women. Proc Natl Acad Sci U S A. 2011;108 Suppl 1:4680-7.
5. Ashraf R, Shah NP. Immune system stimulation by probiotic microorganisms. Crit Rev Food Sci Nutr. 2014;54(7):938-56.
6. Lievin-Le Moal V, Servin AL. Anti-infective activities of lactobacillus strains in the human intestinal microbiota: from probiotics to gastrointestinal anti-infectious biotherapeutic agents. Clin Microbiol Rev. 2014;27(2):167-99.
7. Jensen H, Dromtorp SM, Axelsson L, Grimmer S. Immunomodulation of monocytes by probiotic and selected lactic Acid bacteria. Probiotics Antimicrob Proteins. 2015;7(1):14-23.
8. Vargas Garcia CE, Petrova M, Claes IJ, De Boeck I, Verhoeven TL, Dilissen E, et al. Piliation of Lactobacillus rhamnosus GG promotes adhesion, phagocytosis, and cytokine modulation in macrophages. Appl Environ Microbiol. 2015;81(6):2050-62.
9. Wu CT, Chen PJ, Lee YT, Ko JL, Lue KH. Effects of immunomodulatory supplementation with Lactobacillus rhamnosus on airway inflammation in a mouse asthma model. J Microbiol Immunol Infect. 2014.
10. Foster LM, Tompkins TA, Dahl WJ. A comprehensive post-market review of studies on a probiotic product containing Lactobacillus helveticus R0052 and Lactobacillus rhamnosus R0011. Benef Microbes. 2011;2(4):319-34.
11. Mileti E, Matteoli G, Iliev ID, Rescigno M. Comparison of the immunomodulatory properties of three probiotic strains of Lactobacilli using complex culture systems: prediction for in vivo efficacy. PLoS One. 2009;4(9), e7056.
12. Claes IJ, Lebeer S, Shen C, Verhoeven TL, Dilissen E, De Hertogh G, et al. Impact of lipoteichoic acid modification on the performance of the probiotic Lactobacillus rhamnosus GG in experimental colitis. Clin Exp Immunol. 2010;162(2):306-14.
13. Pena JA, Versalovic J. Lactobacillus rhamnosus GG decreases TNF-alpha production in lipopolysaccharide-activated murine macrophages by a contact-independent mechanism. Cell Microbiol. 2003;5(4):277-85.
14. Gosselink MP, Schouten WR, van Lieshout LM, Hop WC, Laman JD, Ruseler-van Embden JG. Delay of the first onset of pouchitis by oral intake of the probiotic strain Lactobacillus rhamnosus GG. Dis Colon Rectum. 2004;47(6):876-84.
15. Moon G, Myung SJ, Jeong JY, Yang SK, Cho YK, Lee SM, et al. Prophylactic effect of Lactobacillus GG in animal colitis and its effect on cytokine secretion and mucin gene expressions. Korean J Gastroenterol. 2004;43(4):234-45.
16. Yan F, Cao H, Cover TL, Whitehead R, Washington MK, Polk DB. Soluble proteins produced by probiotic bacteria regulate intestinal epithelial cell survival and growth. Gastroenterology. 2007;132(2):562-75.
17. Yan F, Polk DB. Probiotic bacterium prevents cytokine-induced apoptosis in intestinal epithelial cells. J Biol Chem. 2002;277(52):50959-65.
18. Yan F, Cao H, Cover TL, Washington MK, Shi Y, Liu L, et al. Colon-specific delivery of a probiotic-derived soluble protein ameliorates intestinal inflammation in mice through an EGFR-dependent mechanism. J Clin Invest. 2011;121(6):2242-53.
19. Reid G, Charbonneau D, Erb J, Kochanowski B, Beuerman D, Poehner R, et al. Oral use of Lactobacillus rhamnosus GR-1 and L. fermentum RC-14 significantly alters vaginal flora: randomized, placebo-controlled trial in 64 healthy women. FEMS Immunol Med Microbiol. 2003;35(2):131-4.
20. Gardiner GE, Heinemann C, Bruce AW, Beuerman D, Reid G. Persistence of Lactobacillus fermentum RC-14 and Lactobacillus rhamnosus GR-1 but not L. rhamnosus GG in the human vagina as demonstrated by randomly amplified polymorphic DNA. Clin Diagn Lab Immunol. 2002;9(1):92-6.
21. Marelli G, Papaleo E, Ferrari A. Lactobacilli for prevention of urogenital infections: a review. Eur Rev Med Pharmacol Sci. 2004;8(2):87-95.
22. Yeganegi M, Leung CG, Martins A, Kim SO, Reid G, Challis JR, et al. Lactobacillus rhamnosus GR-1-induced IL-10 production in human placental trophoblast cells involves activation of JAK/STAT and MAPK pathways. Reprod Sci. 2010;17(11):1043-51.
23. Yeganegi M, Leung CG, Martins A, Kim SO, Reid G, Challis JR, et al. Lactobacillus rhamnosus GR-1 stimulates colony-stimulating factor 3 (granulocyte) (CSF3) output in placental trophoblast cells in a fetal sex-dependent manner. Biol Reprod. 2011;84(1):18-25.
24. Karlsson M, Scherbak N, Khalaf H, Olsson PE, Jass J. Substances released from probiotic Lactobacillus rhamnosus GR-1 potentiate NF-kappaB activity in Escherichia coli-stimulated urinary bladder cells. FEMS Immunol Med Microbiol. 2012;66(2):147-56.
25. Karlsson M, Scherbak N, Reid G, Jass J. Lactobacillus rhamnosus GR-1 enhances NF-kappaB activation in Escherichia coli-stimulated urinary bladder cells through TLR4. BMC Microbiol. 2012;12:15.
26. Kim SO, Sheikh HI, Ha SD, Martins A, Reid G. G-CSF-mediated inhibition of JNK is a key mechanism for Lactobacillus rhamnosus-induced suppression of TNF production in macrophages. Cell Microbiol. 2006;8(12):1958-71.
27. Martins AJ, Colquhoun P, Reid G, Kim SO. Reduced expression of basal and probiotic-inducible G-CSF in intestinal mononuclear cells is associated with inflammatory bowel disease. Inflamm Bowel Dis. 2009;15(4):515-25.
28. Martins AJ, Spanton S, Sheikh HI, Kim SO. The anti-inflammatory role of granulocyte colony-stimulating factor in macrophage-dendritic cell crosstalk after Lactobacillus rhamnosus GR-1 exposure. J Leukoc Biol. 2011.
29. Lorea Baroja M, Kirjavainen PV, Hekmat S, Reid G. Anti-inflammatory effects of probiotic yogurt in inflammatory bowel disease patients. Clin Exp Immunol. 2007;149(3):470-9.
30. Sansonetti PJ. War and peace at mucosal surfaces. Nat Rev Immunol. 2004;4(12):953-64.
31. Iijima N, Thompson JM, Iwasaki A. Dendritic cells and macrophages in the genitourinary tract. Mucosal Immunol. 2008;1(6):451-9.
32. Plaza-Diaz J, Gomez-Llorente C, Fontana L, Gil A. Modulation of immunity and inflammatory gene expression in the gut, in inflammatory diseases of the gut and in the liver by probiotics. World J Gastroenterol. 2014;20(42):15632-49.
33. Macho Fernandez E, Valenti V, Rockel C, Hermann C, Pot B, Boneca IG, et al. Anti-inflammatory capacity of selected lactobacilli in experimental colitis is driven by NOD2-mediated recognition of a specific peptidoglycan-derived muropeptide. Gut. 2011;60(8):1050-9.
34. Grangette C, Nutten S, Palumbo E, Morath S, Hermann C, Dewulf J, et al. Enhanced antiinflammatory capacity of a Lactobacillus plantarum mutant synthesizing modified teichoic acids. Proc Natl Acad Sci U S A. 2005;102(29):10321-6.
35. Kim HG, Lee SY, Kim NR, Ko MY, Lee JM, Yi TH, et al. Inhibitory effects of Lactobacillus plantarum lipoteichoic acid (LTA) on Staphylococcus aureus LTA-induced tumor necrosis factor-alpha production. J Microbiol Biotechnol. 2008;18(6):1191-6.
36. Kaji R, Kiyoshima-Shibata J, Nagaoka M, Nanno M, Shida K. Bacterial teichoic acids reverse predominant IL-12 production induced by certain lactobacillus strains into predominant IL-10 production via TLR2-dependent ERK activation in macrophages. J Immunol. 2010;184(7):3505-13.
37. Yasuda E, Serata M, Sako T. Suppressive effect on activation of macrophages by Lactobacillus casei strain Shirota genes determining the synthesis of cell wall-associated polysaccharides. Appl Environ Microbiol. 2008;74(15):4746-55.
38. Konstantinov SR, Smidt H, de Vos WM, Bruijns SC, Singh SK, Valence F, et al. S layer protein A of Lactobacillus acidophilus NCFM regulates immature dendritic cell and T cell functions. Proc Natl Acad Sci U S A. 2008;105(49):19474-9.
39. Azcarate-Peril MA, Altermann E, Hoover-Fitzula RL, Cano RJ, Klaenhammer TR. Identification and inactivation of genetic loci involved with Lactobacillus acidophilus acid tolerance. Appl Environ Microbiol. 2004;70(9):5315-22.
40. Meijerink M, van Hemert S, Taverne N, Wels M, de Vos P, Bron PA, et al. Identification of genetic loci in Lactobacillus plantarum that modulate the immune response of dendritic cells using comparative genome hybridization. PLoS One. 2010;5(5), e10632.
41. Ganguli K, Collado MC, Rautava J, Lu L, Satokari R, von Ossowski I, et al. Lactobacillus rhamnosus GG and its SpaC pilus adhesin modulate inflammatory responsiveness and TLR-related gene expression in the fetal human gut. Pediatr Res. 2015;77(4):528-35.
42. Thomas CM, Hong T, van Pijkeren JP, Hemarajata P, Trinh DV, Hu W, et al. Histamine derived from probiotic Lactobacillus reuteri suppresses TNF via modulation of PKA and ERK signaling. PLoS One. 2012;7(2), e31951.
43. Hemarajata P, Gao C, Pflughoeft KJ, Thomas CM, Saulnier DM, Spinler JK, et al. Lactobacillus reuteri-specific immunoregulatory gene rsiR modulates histamine production and immunomodulation by Lactobacillus reuteri. J Bacteriol. 2013;195(24):5567-76.
44. Fitzpatrick LR, Small J, Hoerr RA, Bostwick EF, Maines L, Koltun WA. In vitro and in vivo effects of the probiotic Escherichia coli strain M-17: immunomodulation and attenuation of murine colitis. Br J Nutr. 2008;100(3):530-41.
45. Watanabe T, Nishio H, Tanigawa T, Yamagami H, Okazaki H, Watanabe K, et al. Probiotic Lactobacillus casei strain Shirota prevents indomethacin-induced small intestinal injury: involvement of lactic acid. Am J Physiol Gastrointest Liver Physiol. 2009;297(3):G506-13.
46. Hosoya T, Sakai F, Yamashita M, Shiozaki T, Endo T, Ukibe K, et al. Lactobacillus helveticus SBT2171 inhibits lymphocyte proliferation by regulation of the JNK signaling pathway. PLoS One. 2014;9(9), e108360.
47. Barreau F, Meinzer U, Chareyre F, Berrebi D, Niwa-Kawakita M, Dussaillant M, et al. CARD15/NOD2 is required for Peyer's patches homeostasis in mice. PLoS One. 2007;2(6), e523.
48. Ha SD, Park S, Han CY, Nguyen ML, Kim SO. Cellular adaptation to anthrax lethal toxin-induced mitochondrial cholesterol enrichment, hyperpolarization, and reactive oxygen species generation through downregulating MLN64 in macrophages. Mol Cell Biol. 2012;32(23):4846-60.
49. Svanborg Eden C, Hull R, Falkow S, Leffler H. Target cell specificity of wild-type E. coli and mutants and clones with genetically defined adhesins. Prog Food Nutr Sci. 1983;7(3-4):75-89.
50. Hashimoto M, Tawaratsumida K, Kariya H, Aoyama K, Tamura T, Suda Y. Lipoprotein is a predominant Toll-like receptor 2 ligand in Staphylococcus aureus cell wall components. Int Immunol. 2006;18(2):355-62.
51. Kao SJ, Lei HC, Kuo CT, Chang MS, Chen BC, Chang YC, et al. Lipoteichoic acid induces nuclear factor-kappaB activation and nitric oxide synthase expression via phosphatidylinositol 3-kinase, Akt, and p38 MAPK in RAW 264.7 macrophages. Immunology. 2005;115(3):366-74.
52. Schroder NW, Pfeil D, Opitz B, Michelsen KS, Amberger J, Zahringer U, et al. Activation of mitogen-activated protein kinases p42/44, p38, and stress-activated protein kinases in myelo-monocytic cells by Treponema lipoteichoic acid. J Biol Chem. 2001;276(13):9713-9.
53. Banerjee A, Gerondakis S. Coordinating TLR-activated signaling pathways in cells of the immune system. Immunol Cell Biol. 2007;85(6):420-4.
54. Gantner BN, Simmons RM, Canavera SJ, Akira S, Underhill DM. Collaborative induction of inflammatory responses by dectin-1 and Toll-like receptor 2. J Exp Med. 2003;197(9):1107-17.
55. Kagan JC. Signaling organelles of the innate immune system. Cell. 2012;151(6):1168-78.
56. Perea Velez M, Verhoeven TL, Draing C, Von Aulock S, Pfitzenmaier M, Geyer A, et al. Functional analysis of D-alanylation of lipoteichoic acid in the probiotic strain Lactobacillus rhamnosus GG. Appl Environ Microbiol. 2007;73(11):3595-604.
57. Travassos LH, Girardin SE, Philpott DJ, Blanot D, Nahori MA, Werts C, et al. Toll-like receptor 2-dependent bacterial sensing does not occur via peptidoglycan recognition. EMBO Rep. 2004;5(10):1000-6.
58. Inohara N, Ogura Y, Fontalba A, Gutierrez O, Pons F, Crespo J, et al. Host recognition of bacterial muramyl dipeptide mediated through NOD2. Implications for Crohn's disease. J Biol Chem. 2003;278(8):5509-12.
59. Chamaillard M, Girardin SE, Viala J, Philpott DJ. Nods, Nalps and Naip: intracellular regulators of bacterial-induced inflammation. Cell Microbiol. 2003;5(9):581-92.
60. Smits HH, Engering A, van der Kleij D, de Jong EC, Schipper K, van Capel TM, et al. Selective probiotic bacteria induce IL-10-producing regulatory T cells in vitro by modulating dendritic cell function through dendritic cell-specific intercellular adhesion molecule 3-grabbing nonintegrin. J Allergy Clin Immunol. 2005;115(6):1260-7.
61. van Hemert S, Meijerink M, Molenaar D, Bron PA, de Vos P, Kleerebezem M, et al. Identification of Lactobacillus plantarum genes modulating the cytokine response of human peripheral blood mononuclear cells. BMC Microbiol. 2010;10:293.
62. Lightfoot YL, Selle K, Yang T, Goh YJ, Sahay B, Zadeh M, et al. SIGNR3-dependent immune regulation by Lactobacillus acidophilus surface layer protein A in colitis. EMBO J. 2015;34(7):881-95.
63. Bermudez-Brito M, Munoz-Quezada S, Gomez-Llorente C, Matencio E, Bernal MJ, Romero F, et al. Cell-free culture supernatant of Bifidobacterium breve CNCM I-4035 decreases pro-inflammatory cytokines in human dendritic cells challenged with Salmonella typhi through TLR activation. PLoS One. 2013;8(3), e59370.
64. Bermudez-Brito M, Munoz-Quezada S, Gomez-Llorente C, Romero F, Gil A. Lactobacillus rhamnosus and its cell-free culture supernatant differentially modulate inflammatory biomarkers in Escherichia coli-challenged human dendritic cells. Br J Nutr. 2014;111(10):1727-37.
65. Messaoudi S, Manai M, Kergourlay G, Prevost H, Connil N, Chobert JM, et al. Lactobacillus salivarius: bacteriocin and probiotic activity. Food Microbiol. 2013;36(2):296-304.
66. Yue T, Pei J, Yuan Y. Purification and characterization of anti-Alicyclobacillus bacteriocin produced by Lactobacillus rhamnosus. J Food Prot. 2013;76(9):1575-81.
67. Li W, Yang S, Kim SO, Reid G, Challis JR, Bocking AD. Lipopolysaccharide-Induced Profiles of Cytokine, Chemokine, and Growth Factors Produced by Human Decidual Cells Are Altered by Lactobacillus rhamnosus GR-1 Supernatant. Reprod Sci. 2014;21(7):939-47.
68. Yang S, Li W, Challis JR, Reid G, Kim SO, Bocking AD. Probiotic Lactobacillus rhamnosus GR-1 supernatant prevents lipopolysaccharide-induced preterm birth and reduces inflammation in pregnant CD-1 mice. Am J Obstet Gynecol. 2014;211(1):44 e41-12.
69. Ono K, Han J. The p38 signal transduction pathway: activation and function. Cell Signal. 2000;12(1):1-13.
70. Kim JS, Kim KD, Na HS, Jeong SY, Park HR, Kim S, et al. Tumor necrosis factor-alpha and interleukin-1beta expression pathway induced by Streptococcus mutans in macrophage cell line RAW 264.7. Mol Oral Microbiol. 2012;27(3):149-59.
71. Shen J, Sakaida I, Uchida K, Terai S, Okita K. Leptin enhances TNF-alpha production via p38 and JNK MAPK in LPS-stimulated Kupffer cells. Life Sci. 2005;77(13):1502-15.
72. Kang JS, Yoon YD, Lee KH, Park SK, Kim HM. Costunolide inhibits interleukin-1beta expression by down-regulation of AP-1 and MAPK activity in LPS-stimulated RAW 264.7 cells. Biochem Biophys Res Commun. 2004;313(1):171-7.
73. Wang H, Brown J, Martin M. Glycogen synthase kinase 3: a point of convergence for the host inflammatory response. Cytokine. 2011;53(2):130-40.
74. Martin M, Rehani K, Jope RS, Michalek SM. Toll-like receptor-mediated cytokine production is differentially regulated by glycogen synthase kinase 3. Nat Immunol. 2005;6(8):777-84.
75. Bar-Yehuda S, Madi L, Barak D, Mittelman M, Ardon E, Ochaion A, et al. Agonists to the A3 adenosine receptor induce G-CSF production via NF-kappaB activation: a new class of myeloprotective agents. Exp Hematol. 2002;30(12):1390-8.
76. Wu MH, Lee YC, Tsai WJ, Yang WB, Chen YC, Chuang KA, et al. Characterized polysaccharides from black soybean induce granulocyte colony-stimulated factor gene expression in a phosphoinositide 3-kinase-dependent manner. Immunol Invest. 2010;40(1):39-61.
77. Chou YY, Gao JI, Chang SF, Chang PY, Lu SC. Rapamycin inhibits lipopolysaccharide induction of granulocyte-colony stimulating factor and inducible nitric oxide synthase expression in macrophages by reducing the levels of octamer-binding factor-2. FEBS J. 2011;278(1):85-96.
78. Chou YY, Lu SC. Inhibition by rapamycin of the lipoteichoic acid-induced granulocyte-colony stimulating factor expression in mouse macrophages. Arch Biochem Biophys. 2011;508(1):110-9.
79. Petnicki-Ocwieja T, Kern A. Mechanisms of Borrelia burgdorferi internalization and intracellular innate immune signaling. Front Cell Infect Microbiol. 2015;4:175.
80. Cervantes JL, Dunham-Ems SM, La Vake CJ, Petzke MM, Sahay B, Sellati TJ, et al. Phagosomal signaling by Borrelia burgdorferi in human monocytes involves Toll-like receptor (TLR) 2 and TLR8 cooperativity and TLR8-mediated induction of IFN-beta. Proc Natl Acad Sci U S A. 2011;108(9):3683-8.
81. Moratalla A, Gomez-Hurtado I, Moya-Perez A, Zapater P, Peiro G, Gonzalez-Navajas JM, et al. Bifidobacterium pseudocatenulatum CECT7765 promotes a TLR2-dependent anti-inflammatory response in intestinal lymphocytes from mice with cirrhosis. Eur J Nutr. 2015.
82. Mohamadzadeh M, Olson S, Kalina WV, Ruthel G, Demmin GL, Warfield KL, et al. Lactobacilli activate human dendritic cells that skew T cells toward T helper 1 polarization. Proc Natl Acad Sci U S A. 2005;102(8):2880-5.
83. Saber R, Zadeh M, Pakanati KC, Bere P, Klaenhammer T, Mohamadzadeh M. Lipoteichoic acid-deficient Lactobacillus acidophilus regulates downstream signals. Immunotherapy. 2011;3(3):337-47.
84. Carulli G. Effects of recombinant human granulocyte colony-stimulating factor administration on neutrophil phenotype and functions. Haematologica. 1997;82(5):606-16.
85. Bober LA, Grace MJ, Pugliese-Sivo C, Rojas-Triana A, Waters T, Sullivan LM, et al. The effect of GM-CSF and G-CSF on human neutrophil function. Immunopharmacology. 1995;29(2):111-9.
86. Weiss M, Gross-Weege W, Schneider M, Neidhardt H, Liebert S, Mirow N, et al. Enhancement of neutrophil function by in vivo filgrastim treatment for prophylaxis of sepsis in surgical intensive care patients. J Crit Care. 1995;10(1):21-6.
87. Meshkibaf S, William Gower M, Dekaban GA, Ouk Kim S. G-CSF preferentially supports the generation of gut-homing Gr-1high macrophages in M-CSF-treated bone marrow cells. J Leukoc Biol. 2014;96(4):549-61.
88. Rutella S, Bonanno G, Pierelli L, Mariotti A, Capoluongo E, Contemi AM, et al. Granulocyte colony-stimulating factor promotes the generation of regulatory DC through induction of IL-10 and IFN-alpha. Eur J Immunol. 2004;34(5):1291-302.
89. Rutella S, Danese S, Leone G. Tolerogenic dendritic cells: cytokine modulation comes of age. Blood. 2006;108(5):1435-40.
90. Rutella S, Zavala F, Danese S, Kared H, Leone G. Granulocyte colony-stimulating factor: a novel mediator of T cell tolerance. J Immunol. 2005;175(11):7085-91.
91. Gan XT, Ettinger G, Huang CX, Burton JP, Haist JV, Rajapurohitam V, et al. Probiotic administration attenuates myocardial hypertrophy and heart failure after myocardial infarction in the rat. Circ Heart Fail. 2014;7(3):491-9.
92. Lam V, Su J, Koprowski S, Hsu A, Tweddell JS, Rafiee P, et al. Intestinal microbiota determine severity of myocardial infarction in rats. FASEB J. 2012;26(4):1727-35.
93. Roberts AW. G-CSF: a key regulator of neutrophil production, but that's not all! Growth Factors. 2005;23(1):33-41.
94. Shimoji K, Yuasa S, Onizuka T, Hattori F, Tanaka T, Hara M, et al. G-CSF promotes the proliferation of developing cardiomyocytes in vivo and in derivation from ESCs and iPSCs. Cell Stem Cell. 2010;6(3):227-37.
95. Solaroglu I, Cahill J, Tsubokawa T, Beskonakli E, Zhang JH. Granulocyte colony-stimulating factor protects the brain against experimental stroke via inhibition of apoptosis and inflammation. Neurol Res. 2009;31(2):167-72.