Simulated microgravity disrupts intestinal homeostasis and increases colitis susceptibility

FASEB Journal

Volumn 29, Issue 8, 2015, Pages 3263-3273

  Li, Pingping ^a   Shi, Junxiu ^a   Zhang, Peng ^a   Wang, Ke ^a   Li, Jinglong ^b   Liu, Hongju ^a   Zhou, Yu ^a   Xu, Xi ^a   Hao, Jie ^a   Sun, Xiuyuan ^a   Pang, Xuewen ^a   Li, Yan ^a   Wu, Hounan ^c   Chen, Xiaoping ^a   Ge, Qing ^a  

^a PEKING UNIVERSITY HEALTH SCIENCE CENTER   (China)

^b Peking University Medical and Health Analytical Center Peking University Health Sciences Center Chinese Astronaut Research and Training Center ^*  (China)

^c SHAANXI NORMAL UNIVERSITY   (China)

Author keywords

IL 10; Microbiota; Neutrophil

Indexed keywords

ANTIBIOTIC AGENT; INTERLEUKIN 10; INTERLEUKIN 1BETA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COLITIS; CONTROLLED STUDY; CYTOKINE PRODUCTION; DEXTRAN SODIUM SULFATE-INDUCED COLITIS; DISEASE PREDISPOSITION; FEMALE; HOMEOSTASIS; INFLAMMATION; INNATE IMMUNITY; INTESTINE FLORA; MICROGRAVITY; MOUSE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; SIMULATION; SPACE; ANIMAL; C57BL MOUSE; DISEASE MODEL; INTESTINE; METABOLISM; PHYSIOLOGY; PROCEDURES; WEIGHTLESSNESS;

CANDIDATUS ARTHROMITUS SP. SFB-MOUSE; MUS;

ANIMALS; COLITIS; DISEASE MODELS, ANIMAL; DISEASE SUSCEPTIBILITY; FEMALE; HOMEOSTASIS; INFLAMMATION; INTERLEUKIN-10; INTERLEUKIN-1BETA; INTESTINES; MICE; MICE, INBRED C57BL; NEUTROPHILS; WEIGHTLESSNESS SIMULATION;

EID: 84940366725     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.15-271700     Document Type: Article

References (53)

1. Crucian, B. E., Stowe, R. P., Pierson, D. L., and Sams, C. F. (2008) Immune system dysregulation following short-vs long-duration spaceflight. Aviat. Space Environ. Med. 79, 835-843
2. Chakraborty, N., Gautam, A., Muhie, S., Miller, S. A., Jett, M., and Hammamieh, R. (2014) An integrated omics analysis: impact of microgravity on host response to lipopolysaccharide in vitro. BMC Genomics 15, 659
3. Girardi, C., De Pitta, C., Casara, S., Calura, E., Romualdi, C., Celotti, L., and Mognato, M. (2014) Integration analysis of microRNA and mRNA expression profiles in human peripheral blood lymphocytes cultured in modeled microgravity. Biomed. Res. Int. 2014, 296747
4. Guéguinou, N., Huin-Schohn, C., Bascove, M., Bueb, J. L., Tschirhart, E., Legrand-Frossi, C., and Frippiat, J. P. (2009) Could spaceflight-Associated immune system weakening preclude the expansion of human presence beyond Earth's orbit J. Leukoc. Biol. 86, 1027-1038
5. Kaur, I., Simons, E. R.,Castro, V. A.,MarkOtt,C., and Pierson,D.L. (2004) Changes in neutrophil functions in astronauts. Brain Behav. Immun. 18, 443-450
6. Stowe,R. P., Sams,C. F., Mehta, S. K.,Kaur, I., Jones,M.L., Feeback, D. L., and Pierson, D. L. (1999) Leukocyte subsets and neutrophil function after short-term spaceflight. J. Leukoc. Biol. 65, 179-186
7. Foster, J. S., Khodadad, C. L., Ahrendt, S. R., and Parrish, M. L. (2013) Impact of simulated microgravity on the normal developmental time line of an animal-bacteria symbiosis. Sci. Rep. 3, 1340
8. Kaur, I., Simons, E. R., Kapadia, A. S., Ott, C.M., and Pierson, D. L. (2008) Effect of spaceflight on ability of monocytes to respond to endotoxins of gram-negative bacteria. Clin. Vaccine Immunol. 15, 1523-1528
9. Crucian, B., Stowe,R.,Quiriarte, H., Pierson, D., and Sams,C. (2011) Monocyte phenotype and cytokine production profiles are dysregulated by short-duration spaceflight. Aviat. Space Environ. Med. 82, 857-862
10. Crucian, B., Stowe, R.,Mehta, S.,Uchakin, P.,Quiriarte,H., Pierson, D., and Sams,C. (2013) Immune systemdysregulationoccurs during short duration spaceflight on board the space shuttle. J. Clin. Immunol. 33, 456-465
11. Novoselova, E. G., Lunin, S. M., Khrenov, M. O., Parfenyuk, S. B., Novoselova, T. V., Shenkman, B. S., and Fesenko, E. E. (2014) Changes in immune cell signalling, apoptosis and stress response functions in mice returned from the BION-M1 mission in space. Immunobiology 220, 500-509
12. Pierson, D. L., Stowe, R. P., Phillips, T. M., Lugg, D. J., and Mehta, S. K. (2005) Epstein-Barr virus shedding by astronauts during space flight. Brain Behav. Immun. 19, 235-242
13. Stowe, R. P., Mehta, S. K., Ferrando, A. A., Feeback, D. L., and Pierson, D. L. (2001) Immune responses and latent herpesvirus reactivation in spaceflight. Aviat. Space Environ. Med. 72, 884-891
14. Crucian, B., and Sams, C. (2009) Immune system dysregulation during spaceflight: clinical risk for exploration-class missions. J. Leukoc. Biol. 86, 1017-1018
15. Klaus, D., Simske, S., Todd, P., and Stodieck, L. (1997) Investigation of space flight effects on Escherichia coli and a proposed model of underlying physical mechanisms. Microbiology 143, 449-455
16. Lynch, S. V., Brodie, E. L., and Matin, A. (2004) Role and regulation of sigma S in general resistance conferred by low-shear simulated microgravity in Escherichia coli. J. Bacteriol. 186, 8207-8212
17. Nickerson, C. A., Ott, C. M., Wilson, J. W., Ramamurthy, R., and Pierson, D. L. (2004)Microbial responses tomicrogravity and other low-shear environments. Microbiol. Mol. Biol. Rev. 68, 345-361
18. Arunasri,K.,Adil,M.,VenuCharan,K., Suvro,C.,HimabinduReddy, S., and Shivaji, S. (2013) Effect of simulated microgravity on E. coli K12 MG1655 growth and gene expression. PLoS ONE 8, e57860
19. Xiang, L., Qi, F., Dai, D., Li, C., and Jiang, Y. (2010) Simulated microgravity affects growth of Escherichia coli and recombinant beta-D-glucuronidase production. Appl. Biochem. Biotechnol. 162, 654-661
20. Ruby, E., Henderson, B., and McFall-Ngai, M. (2004)Microbiology. We get by with a little help from our (little) friends. Science 303, 1305-1307
21. Xu, J., and Gordon, J. I. (2003)Honor thy symbionts. Proc.Natl.Acad. Sci. USA 100, 10452-10459
22. McCarville, J. L., Clarke, S. T., Shastri, P., Liu, Y., Kalmokoff, M., Brooks,S.P., and Green-Johnson, J.M. (2013)Spaceflight influences both mucosal and peripheral cytokine production in PTN-Tg and wild type mice. PLoS ONE 8, e68961
23. Zhou, Y., Ni, H., Li, M., Sanzari, J. K., Diffenderfer, E. S., Lin, L., Kennedy, A. R., and Weissman, D. (2012) Effect of solar particle event radiation and hindlimb suspension on gastrointestinal tract bacterial translocation and immune activation. PLoS ONE 7, e44329
24. Sawyer, H. R., Moeller, C. L., Phillips, R. W., and Smirnov, K. L. (1992) Proliferation of jejunal mucosal cells in rats flown in space. J. Appl. Physiol. 73, 148S-150S
25. Bernstein, C. N., Wajda, A., and Blanchard, J. F. (2005) The clustering of other chronic inflammatory diseases in inflammatory bowel disease: a population-based study. Gastroenterology 129, 827-836
26. Huang,B. L., Chandra, S., and Shih,D.Q. (2012) Skin manifestations of inflammatory bowel disease. Front. Physiol. 3, 13
27. Xu,X.R.,Liu,C.Q.,Feng,B. S.,andLiu,Z. J.(2014)Dysregulationof mucosal immune response in pathogenesis of inflammatory bowel disease. World J. Gastroenterol. 20, 3255-3264
28. Wallace, K. L., Zheng, L. B., Kanazawa, Y., and Shih, D. Q. (2014) Immunopathology of inflammatory bowel disease. World J. Gastroenterol. 20, 6-21
29. Brazil, J. C., Louis, N. A., and Parkos, C. A. (2013) The role of polymorphonuclear leukocyte trafficking in the perpetuation of inflammation during inflammatory bowel disease. Inflamm. Bowel Dis. 19, 1556-1565
30. Neurath,M. F. (2014)Cytokines in inflammatory bowel disease. Nat. Rev. Immunol. 14, 329-342
31. Chapes, S. K.,Mastro, A. M., Sonnenfeld,G., and Berry,W.D. (1993) Antiorthostatic suspensionas amodel for the effects of spaceflight on the immune system. J. Leukoc. Biol. 54, 227-235
32. Zigmond, E., Varol, C., Farache, J., Elmaliah, E., Satpathy, A. T., Friedlander, G., Mack, M., Shpigel, N., Boneca, I. G., Murphy, K. M., Shakhar, G., Halpern, Z., and Jung, S. (2012) Ly6C hi monocytes in the inflamed colon give rise to proinflammatory effector cells and migratory antigen-presenting cells. Immunity 37, 1076-1090
33. Barman, M., Unold, D., Shifley, K., Amir, E., Hung, K., Bos, N., and Salzman, N. (2008) Enteric salmonellosis disrupts the microbial ecology of the murine gastrointestinal tract. Infect. Immun. 76, 907-915
34. Qiu, J., Guo, X., Chen, Z.M.,He, L., Sonnenberg,G. F., Artis, D., Fu, Y. X., and Zhou, L. (2013) Group 3 innate lymphoid cells inhibit Tcell-mediated intestinal inflammation through aryl hydrocarbon receptor signaling and regulation of microflora. Immunity 39, 386-399
35. Kelsen, J., Bartels, L. E., Dige, A., Hvas, C. L., Frings-Meuthen, P., Boehme, G., Thomsen,M. K., Fenger-Grøn, M., and Dahlerup, J. F. (2012) 21 Days head-down bed rest induces weakening of cellmediated immunity-Some spaceflight findings confirmed in a ground-based analog. Cytokine 59, 403-409
36. Xu,X., Tan, C., Li, P., Zhang, S., Pang, X.,Liu,H., Li,L., Sun, X., Zhang, Y., Wu, H., Chen, X., and Ge, Q. (2013) Changes of cytokines during a spaceflight analog-A 45-day head-down bed rest. PLoS ONE 8, e77401
37. Noor, S. O., Ridgway, K., Scovell, L., Kemsley, E. K., Lund, E. K., Jamieson, C., Johnson, I. T., and Narbad, A. (2010)Ulcerative colitis and irritable bowel patients exhibit distinct abnormalities of the gut microbiota. BMC Gastroenterol. 10, 134
38. Ivanov, I. I., and Honda, K. (2012) Intestinal commensalmicrobes as immune modulators. Cell Host Microbe 12, 496-508
39. Kabat, A. M., Srinivasan, N., and Maloy, K. J. (2014) Modulation of immune development and function by intestinal microbiota. Trends Immunol. 35, 507-517
40. Zenewicz, L. A., Yin, X.,Wang, G., Elinav, E.,Hao, L., Zhao, L., and Flavell, R. A. (2013) IL-22 deficiency alters colonic microbiota to be transmissible and colitogenic. J. Immunol. 190, 5306-5312
41. Devkota, S., Wang, Y., Musch, M. W., Leone, V., Fehlner-Peach, H., Nadimpalli, A., Antonopoulos, D. A., Jabri, B., and Chang, E. B. (2012) Dietary-fat-induced taurocholic acid promotes pathobiont expansion and colitis in Il10-/-mice. Nature 487, 104-108
42. Shih,V.F.,Cox, J.,Kljavin,N.M.,Dengler,H.S.,Reichelt,M.,Kumar, P., Rangell, L., Kolls, J. K., Diehl, L., Ouyang, W., and Ghilardi, N. (2014) Homeostatic IL-23 receptor signaling limits Th17 response through IL-22-mediated containment of commensal microbiota. Proc. Natl. Acad. Sci. USA 111, 13942-13947
43. Gaboriau-Routhiau,V.,Rakotobe, S., Lécuyer, E.,Mulder, I., Lan,A., Bridonneau, C., Rochet, V., Pisi, A., De Paepe,M., Brandi, G., Eberl, G., Snel, J., Kelly, D., and Cerf-Bensussan, N. (2009) The key role of segmented filamentous bacteria in the coordinated maturation of gut helper T cell responses. Immunity 31, 677-689
44. Ivanov, I. I., Atarashi, K.,Manel, N., Brodie, E. L., Shima, T., Karaoz, U., Wei, D.,Goldfarb, K. C., Santee, C. A., Lynch, S. V., Tanoue, T., Imaoka, A., Itoh, K., Takeda, K., Umesaki, Y., Honda, K., and Littman, D. R. (2009) Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 139, 485-498
45. Furusawa, Y.,Obata, Y., and Hase, K. (2014) Commensalmicrobiota regulates T cell fate decision in the gut. Semin. Immunopathol. 37, 17-25
46. Sanz, Y., and Moya-Pérez, A. (2014) Microbiota, inflammation and obesity. Adv. Exp. Med. Biol. 817, 291-317
47. Zigmond, E., Bernshtein, B., Friedlander, G.,Walker, C. R., Yona, S., Kim, K. W., Brenner,O., Krauthgamer, R., Varol, C.,Müller, W., and Jung, S. (2014) Macrophage-restricted interleukin-10 receptor deficiency, but not IL-10 deficiency, causes severe spontaneous colitis. Immunity 40, 720-733
48. Shouval, D. S., Biswas, A., Goettel, J. A., McCann, K., Conaway, E., Redhu,N. S.,Mascanfroni, I.D.,AlAdham, Z., Lavoie, S., Ibourk,M., Nguyen, D. D., Samsom, J. N., Escher, J. C., Somech, R.,Weiss, B., Beier, R., Conklin, L. S., Ebens, C. L., Santos, F. G., Ferreira, A. R., Sherlock, M., Bhan, A. K., Müller, W., Mora, J. R., Quintana, F. J., Klein, C., Muise, A. M., Horwitz, B. H., and Snapper, S. B. (2014) Interleukin-10 receptor signaling in innate immune cells regulates mucosal immune tolerance and anti-inflammatory macrophage function. Immunity 40, 706-719
49. Lukens, J. R., Gross, J. M., and Kanneganti, T. D. (2012) IL-1 family cytokines trigger sterile inflammatory disease. Front. Immunol. 3, 315
50. Masini,M.A., Albi,E., Barmo, C.,Bonfiglio, T., Bruni, L., Canesi, L., Cataldi, S., Curcio, F., D'Amora, M., Ferri, I., Goto, K., Kawano, F., Lazzarini, R., Loreti, E., Nakai, N.,Ohira, T., Ohira, Y., Palmero, S., Prato, P.,Ricci, F., Scarabelli, L., Shibaguchi,T., Spelat,R., Strollo, F., and Ambesi-Impiombato, F. S. (2012) The impact of long-term exposure to space environment on adult mammalian organisms: a study on mouse thyroid and testis. PLoS ONE 7, e35418
51. Schmitt, D. A., Schaffar, L., Taylor, G. R., Loftin, K. C., Schneider, V. S., Koebel, A., Abbal, M., Sonnenfeld, G., Lewis, D. E., Reuben, J. R., and Ferebee, R. (1996) Use of bed rest and head-down tilt to simulate spaceflight-induce immune system changes. J. Interferon Cytokine Res. 16, 151-157
52. Schmitt, D. A., Schwarzenberg, M., Tkaczuk, J., Hebrard, S., Brandenberger, G., Mauco, G., Cogoli-Greuter, M., and Abbal, M. (2000)Head-down tilt bed rest and immune responses. Pflugers Arch. 441 (2-3 Suppl) R79-R84
53. Fournier, B. M., and Parkos, C. A. (2012) The role of neutrophils during intestinal inflammation. Mucosal Immunol. 5, 354-366