Restoring specific lactobacilli levels decreases inflammation and muscle atrophy markers in an acute leukemia mouse model

PLoS ONE

Volumn 7, Issue 6, 2012, Pages

  Bindels, Laure B ^a   Beck, Raphaël ^a   Schakman, Olivier ^a   Martin, Jennifer C ^b   de Backer, Fabienne ^a   Sohet, Florence M ^a   Dewulf, Evelyne M ^a   Pachikian, Barbara D ^a   Neyrinck, Audrey M ^a   Thissen, Jean Paul ^a   Verrax, Julien ^a   Calderon, Pedro Buc ^a   Pot, Bruno ^c   Grangette, Corinne ^c   Cani, Patrice D ^a   Scott, Karen P ^b   Delzenne, Nathalie M ^a  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^b ROWETT RESEARCH INSTITUTE   (United Kingdom)

^c UNIV LILLE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ATROGIN 1; CATHEPSIN L; DNA 16S; GRANULOCYTE COLONY STIMULATING FACTOR; INTERLEUKIN 4; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; MUSCLE RING FINGER 1 PROTEIN;

ACUTE LEUKEMIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANOREXIA; ARTICLE; BODY FAT; CONTROLLED STUDY; FEMALE; GASTROCNEMIUS MUSCLE; INFLAMMATION; INTESTINE FLORA; LACTOBACILLUS; LACTOBACILLUS ACIDOPHILUS; LACTOBACILLUS ANIMALIS; LACTOBACILLUS GASSERI; LACTOBACILLUS JOHNSONII; LACTOBACILLUS MURINUS; LACTOBACILLUS REUTERI; MUSCLE ATROPHY; NONHUMAN; PROTEIN EXPRESSION; SUPPLEMENTATION; THERAPY EFFECT; TIBIALIS ANTERIOR MUSCLE;

ACUTE DISEASE; ANIMALS; CELLS, CULTURED; DIETARY SUPPLEMENTS; DISEASE MODELS, ANIMAL; FEMALE; FUSION PROTEINS, BCR-ABL; GASTROINTESTINAL TRACT; INFLAMMATION; INFLAMMATION MEDIATORS; LACTOBACILLUS; LEUKEMIA, EXPERIMENTAL; LIVER NEOPLASMS; METAGENOME; MICE; MICE, INBRED BALB C; MUSCULAR ATROPHY; PRECURSOR CELLS, B-LYMPHOID; SPLENIC NEOPLASMS;

LACTOBACILLUS; LACTOBACILLUS ACIDOPHILUS; LACTOBACILLUS ACIDOPHILUS NCFM; LACTOBACILLUS GASSERI; LACTOBACILLUS REUTERI; LACTOBACILLUS REUTERI 100-23; MUS;

EID: 84862993997     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0037971     Document Type: Article

References (52)

1. Tisdale MJ, (2009) Mechanisms of cancer cachexia. Physiol Rev 89: 381-410.
2. Tan BH, Fearon KC, (2008) Cachexia: prevalence and impact in medicine. Curr Opin Clin Nutr Metab Care 11: 400-407.
3. Dewys WD, Begg C, Lavin PT, Band PR, Bennett JM, et al. (1980) Prognostic effect of weight loss prior to chemotherapy in cancer patients. Eastern Cooperative Oncology Group. Am J Med 69: 491-497.
4. Moschovi M, Trimis G, Vounatsou M, Katsibardi K, Margeli A, et al. (2008) Serial plasma concentrations of PYY and ghrelin during chemotherapy in children with acute lymphoblastic leukemia. J Pediatr Hematol Oncol 30: 733-737.
5. Sessions J, (2007) Chronic myeloid leukemia in 2007. J Manag Care Pharm 13: 4-7.
6. Das SK, Eder S, Schauer S, Diwoky C, Temmel H, et al. (2011) Adipose triglyceride lipase contributes to cancer-associated cachexia. Science 333 233-238. science.1198973 [pii];10.1126/science.1198973 [doi].
7. Bodine SC, Latres E, Baumhueter S, Lai VK, Nunez L, et al. (2001) Identification of ubiquitin ligases required for skeletal muscle atrophy. Science 294: 1704-1708.
8. Gomes MD, Lecker SH, Jagoe RT, Navon A, Goldberg AL, (2001) Atrogin-1, a muscle-specific F-box protein highly expressed during muscle atrophy. Proc Natl Acad Sci U S A 98: 14440-14445.
9. Lecker SH, Jagoe RT, Gilbert A, Gomes M, Baracos V, et al. (2004) Multiple types of skeletal muscle atrophy involve a common program of changes in gene expression. FASEB J 18: 39-51.
10. Attaix D, Baracos VE, (2010) MAFbx/Atrogin-1 expression is a poor index of muscle proteolysis. Curr Opin Clin Nutr Metab Care 13: 223-224.
11. Clarke BA, Drujan D, Willis MS, Murphy LO, Corpina RA, et al. (2007) The E3 Ligase MuRF1 degrades myosin heavy chain protein in dexamethasone-treated skeletal muscle. Cell Metab 6 376-385. S1550-4131(07)00290-2 [pii];10.1016/j.cmet.2007.09.009 [doi].
12. Polge C, Heng AE, Jarzaguet M, Ventadour S, Claustre A, et al. (2011) Muscle actin is polyubiquitinylated in vitro and in vivo and targeted for breakdown by the E3 ligase MuRF1. FASEB J 25 3790-3802. fj.11-180968 [pii];10.1096/fj.11-180968 [doi].
13. Dobrowolny G, Aucello M, Rizzuto E, Beccafico S, Mammucari C, et al. (2008) Skeletal muscle is a primary target of SOD1G93A-mediated toxicity. Cell Metab 8: 425-436.
14. Round JL, Mazmanian SK, (2009) The gut microbiota shapes intestinal immune responses during health and disease. Nat Rev Immunol 9: 313-323.
15. Delzenne NM, Neyrinck AM, Backhed F, Cani PD, (2011) Targeting gut microbiota in obesity: effects of prebiotics and probiotics. Nat Rev Endocrinol 7 639-646. nrendo.2011.126 [pii];10.1038/nrendo.2011.126 [doi].
16. Clarke TB, Davis KM, Lysenko ES, Zhou AY, Yu Y, et al. (2010) Recognition of peptidoglycan from the microbiota by Nod1 enhances systemic innate immunity. Nat Med 16: 228-231.
17. Neish AS, (2009) Microbes in gastrointestinal health and disease. Gastroenterology 136: 65-80.
18. Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, et al. (2006) An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444: 1027-1031.
19. Backhed F, Ding H, Wang T, Hooper LV, Koh GY, et al. (2004) The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci U S A 101: 15718-15723.
20. Dewulf EM, Cani PD, Neyrinck AM, Possemiers S, Van HA, et al. (2011) Inulin-type fructans with prebiotic properties counteract GPR43 overexpression and PPARgamma-related adipogenesis in the white adipose tissue of high-fat diet-fed mice. J Nutr Biochem 22 712-722. S0955-2863(10)00148-8 [pii];10.1016/j.jnutbio.2010.05.009 [doi].
21. Backhed F, Manchester JK, Semenkovich CF, Gordon JI, (2007) Mechanisms underlying the resistance to diet-induced obesity in germ-free mice. Proc Natl Acad Sci U S A 104: 979-984.
22. Everard A, Lazarevic V, Derrien M, Girard M, Muccioli GM, et al. (2011) Responses of gut microbiota and glucose and lipid metabolism to prebiotics in genetic obese and diet-induced leptin-resistant mice. Diabetes 60 2775-2786. db11-0227 [pii];10.2337/db11-0227 [doi].
23. Spor A, Koren O, Ley R, (2011) Unravelling the effects of the environment and host genotype on the gut microbiome. Nat Rev Microbiol 9 279-290. nrmicro2540 [pii];10.1038/nrmicro2540 [doi].
24. Ren R, (2005) Mechanisms of BCR-ABL in the pathogenesis of chronic myelogenous leukaemia. Nat Rev Cancer 5: 172-183.
25. Fiskus W, Pranpat M, Bali P, Balasis M, Kumaraswamy S, et al. (2006) Combined effects of novel tyrosine kinase inhibitor AMN107 and histone deacetylase inhibitor LBH589 against Bcr-Abl-expressing human leukemia cells. Blood 108: 645-652.
26. Fiskus W, Pranpat M, Balasis M, Bali P, Estrella V, et al. (2006) Cotreatment with vorinostat (suberoylanilide hydroxamic acid) enhances activity of dasatinib (BMS-354825) against imatinib mesylate-sensitive or imatinib mesylate-resistant chronic myelogenous leukemia cells. Clin Cancer Res 12 5869-5878. 12/19/5869 [pii];10.1158/1078-0432.CCR-06-0980 [doi].
27. Muyzer G, de Waal EC, Uitterlinden AG, (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59: 695-700.
28. Delroisse JM, Boulvin AL, Parmentier I, Dauphin RD, Vandenbol M, et al. (2008) Quantification of Bifidobacterium spp. and Lactobacillus spp. in rat fecal samples by real-time PCR. Microbiol Res 163: 663-670.
29. R Development Core Team (2012) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0. R website. Available: http://www.R-project.org/. Accessed 2012 April.
30. Acharyya S, Butchbach ME, Sahenk Z, Wang H, Saji M, et al. (2005) Dystrophin glycoprotein complex dysfunction: a regulatory link between muscular dystrophy and cancer cachexia. Cancer Cell 8: 421-432.
31. Thomas CM, Versalovic J, (2010) Probiotics-host communication: Modulation of signaling pathways in the intestine. Gut Microbes 1: 148-163.
32. Louis P, Scott KP, Duncan SH, Flint HJ, (2007) Understanding the effects of diet on bacterial metabolism in the large intestine. J Appl Microbiol 102 1197-1208. JAM3322 [pii];10.1111/j.1365-2672.2007.03322.x [doi].
33. de Moreno de LeBlanc A, Dogi CA, Galdeano CM, Carmuega E, Weill R, et al. (2008) Effect of the administration of a fermented milk containing Lactobacillus casei DN-114001 on intestinal microbiota and gut associated immune cells of nursing mice and after weaning until immune maturity. BMC Immunol 9: 27.
34. Livingston M, Loach D, Wilson M, Tannock GW, Baird M, (2010) Gut commensal Lactobacillus reuteri 100-23 stimulates an immunoregulatory response. Immunol Cell Biol 88 99-102. icb200971 [pii];10.1038/icb.2009.71 [doi].
35. Trikha M, Corringham R, Klein B, Rossi JF, (2003) Targeted anti-interleukin-6 monoclonal antibody therapy for cancer: a review of the rationale and clinical evidence. Clin Cancer Res 9: 4653-4665.
36. Fernandez EM, Valenti V, Rockel C, Hermann C, Pot B, et al. (2011) Anti-inflammatory capacity of selected lactobacilli in experimental colitis is driven by NOD2-mediated recognition of a specific peptidoglycan-derived muropeptide. Gut 60 1050-1059. gut.2010.232918 [pii];10.1136/gut.2010.232918 [doi].
37. Altermann E, Russell WM, zcarate-Peril MA, Barrangou R, Buck BL, et al. (2005) Complete genome sequence of the probiotic lactic acid bacterium Lactobacillus acidophilus NCFM. Proc Natl Acad Sci U S A 102: 3906-3912.
38. Tilg H, Moschen AR, Kaser A, (2009) Obesity and the microbiota. Gastroenterology 136: 1476-1483.
39. Cani PD, Delzenne NM, (2009) The role of the gut microbiota in energy metabolism and metabolic disease. Curr Pharm Des 15: 1546-1558.
40. Madsen KL, Doyle JS, Jewell LD, Tavernini MM, Fedorak RN, (1999) Lactobacillus species prevents colitis in interleukin 10 gene-deficient mice. Gastroenterology 116: 1107-1114.
41. Crawford PA, Crowley JR, Sambandam N, Muegge BD, Costello EK, et al. (2009) Regulation of myocardial ketone body metabolism by the gut microbiota during nutrient deprivation. Proc Natl Acad Sci U S A 106: 11276-11281.
42. Karimi K, Inman MD, Bienenstock J, Forsythe P, (2009) Lactobacillus reuteri-induced regulatory T cells protect against an allergic airway response in mice. Am J Respir Crit Care Med 179 186-193. 200806-951OC [pii];10.1164/rccm.200806-951OC [doi].
43. Foligne B, Nutten S, Grangette C, Dennin V, Goudercourt D, et al. (2007) Correlation between in vitro and in vivo immunomodulatory properties of lactic acid bacteria. World J Gastroenterol 13: 236-243.
44. Yao Y, Li W, Kaplan MH, Chang CH, (2005) Interleukin (IL)-4 inhibits IL-10 to promote IL-12 production by dendritic cells. J Exp Med 201 1899-1903. jem.20050324 [pii];10.1084/jem.20050324 [doi].
45. Lagirand-Cantaloube J, Cornille K, Csibi A, Batonnet-Pichon S, Leibovitch MP, et al. (2009) Inhibition of atrogin-1/MAFbx mediated MyoD proteolysis prevents skeletal muscle atrophy in vivo. PLoS One 4 e4973. 10.1371/journal.pone.0004973 [doi].
46. Cong H, Sun L, Liu C, Tien P, (2011) Inhibition of atrogin-1/MAFbx expression by adenovirus-delivered small hairpin RNAs attenuates muscle atrophy in fasting mice. Hum Gene Ther 22 313-324. 10.1089/hum.2010.057 [doi].
47. Reed SA, Sandesara PB, Senf SM, Judge AR, (2012) Inhibition of FoxO transcriptional activity prevents muscle fiber atrophy during cachexia and induces hypertrophy. FASEB J 26 987-1000. fj.11-189977 [pii];10.1096/fj.11-189977 [doi].
48. Cani PD, Possemiers S, Van de WT, Guiot Y, Everard A, et al. (2009) Changes in gut microbiota control inflammation in obese mice through a mechanism involving GLP-2-driven improvement of gut permeability. Gut 58: 1091-1103.
49. Doyle A, Zhang G, bdel Fattah EA, Eissa NT, Li YP, (2011) Toll-like receptor 4 mediates lipopolysaccharide-induced muscle catabolism via coordinate activation of ubiquitin-proteasome and autophagy-lysosome pathways. FASEB J 25: 99-110.
50. Han DM, Zhang YQ, Bai QX, Chen XQ, (2007) Assay of AVP, CRP, and LPS in leukemia. Int J Lab Hematol 29: 185-189.
51. Aggarwal BB, Gehlot P, (2009) Inflammation and cancer: how friendly is the relationship for cancer patients? Curr Opin Pharmacol 9 351-369. S1471-4892(09)00090-3 [pii];10.1016/j.coph.2009.06.020 [doi].
52. Rollins BJ, (2006) Inflammatory chemokines in cancer growth and progression. Eur J Cancer 42 760-767. S0959-8049(06)00038-4 [pii];10.1016/j.ejca.2006.01.002 [doi].