Absence of microbiota (germ-free conditions) accelerates the atherosclerosis in apoe-deficient mice fed standard low cholesterol diet

Journal of Atherosclerosis and Thrombosis

Volumn 17, Issue 8, 2010, Pages 796-804

  Stepankova, Renata ^a   Tonar, Zbynek ^b,c   Bartova, Jirina ^c   Nedorost, Lukas ^c   Rossman, Pavel ^a   Poledne, Rudolf ^b   Schwarzer, Martin ^a   Tlaskalova Hogenova, Helena ^a  

^a INSTITUTE OF MICROBIOLOGY   (Czech Republic)

^b INSTITUTE FOR CLINICAL AND EXPERIMENTAL MEDICINE   (Czech Republic)

^c CHARLES UNIVERSITY   (Czech Republic)

Author keywords

Atherogenesis; Commensal bacteria; Germ free mice

Indexed keywords

APOLIPOPROTEIN E;

ABDOMINAL AORTA; ARTICLE; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; CHOLESTEROL DIET; DISEASE COURSE; FOAM CELL; HISTOLOGY; IMMUNOHISTOLOGY; INTESTINE FLORA; KNOCKOUT MOUSE; LIPID STORAGE; LOW FAT DIET; MACROPHAGE; MORPHOMETRICS; MOUSE; MOUSE STRAIN; NONHUMAN; SHAM FEEDING; THORACIC AORTA;

EID: 77956330642     PISSN: 13403478     EISSN: 18803873     Source Type: Journal    
DOI: 10.5551/jat.3285     Document Type: Article

References (43)

1. Ross R: Atherosclerosis: an inflammatory disease. N Engl J Med, 1999; 340: 115-126
2. Zang SH, Reddick RL, Piedrahita JA, Maeda N: Spontaneous hypercholesterolemia and arterial lesions in mice lacking apolipoprotein E. Science, 1992; 258: 468-471
3. Shi W, Brown MD, Wang X, Wong J, Kallmes DF, Matsumaotoa AH, Helm GA, Drake TA, Lusis AJ: Genetic background but not sizes of atherosclerotic lesions determine medial destruction in the aortic root of apolipoprotein E-deficient mice. Arterioscler Thromb Vas Biol, 2003; 23: 1901-1906
4. Meir KS, Leitersdorf E: Atherosclerosis in the apolipoprotein E-deficient mouse. Arterioscler Thromb Vas Biol, 2004; 24: 1006-1014
5. Zhou X: CD4+ T cells in atherosclerosis. Biomed Pharmacother, 2003; 57: 289-291
6. Beck JD, Offenbacher S, Williams R, Gibbs P, Garcia R: Periodontitis: a risk factor for coronary heart disease. Ann Periodontol, 1998; 3: 127-141
7. Wright SD, Burton Ch, Hernandez M, Hassing H, Montenegro J, Munt S, Patel S, Card DJ, Hermanowski-Vosadka, Brgström JD, Sparrow CP, Detmers PA, Chao YS: Infectious agents are not necessary for murine atherogenesis. J Exp Med, 2000; 191: 1437-1442
8. Stepankova R: Rearing of germ-free rats, mice, and rabbits. In: Immunology Methods Manual: Lefkovits I, Academic Press; London,:1537-1542, 1997
9. Fazzi P, Ciancaglini E, Soforza GR: Differential fluorescent staining method for detection of bacteria in blood cultures, cerebrospinal fluid and other clinical specimens. Eur J Clin Microbiol Infect Dis, 2002; 21: 373-378
10. Fox JG, Gorelick PL, Kullberg MC, Ge Z, Dewhirst FE, Ward JM: A novel urease-negative Helicobacter species associated with colitis and typhilis in IL-10- deficient mice. Inf Immun, 1999; 67: 1757-1762
11. Stepankova R, Powrie F, Kofronova O, Kozakova H, Hudcovic T, Hrncir T, Uhlig H, Read S, Rehakova Z, Benada O, Heczko P, Strus M, Bland P, Tlaskalova- Hogenova H: Segmented filamentous bacteria in a defined bacterial cocktail induce intestinal inflammation in SCID mice reconstituted with CD45high CD4+ T cells. Inflamm Bowel Dis, 2007; 13: 1202-1211
12. Saltzmann NH, de Jong H, Paterson Y, Harmsen HJM, Welling GW, Bos N: Analysis of 16S libraries of mouse gastrointestinal microflora reveals a large new group of mouse intestinal bacteria. Microbiology, 2002; 148: 3651-3660
13. Mantz W, Amann R, Ludwig W: Application of a suite of 16S rRNA -specific oligonucleotide probes designed to investigate bacteria of the phylum cytophago-flavobacterbacteroides in the natural environment. Microbiology, 1996; 142: 1097-1106
14. Amann RI, Binder BJ, Olson RJ, Chrisholm SW, Devereux R, Stahl DA: Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl Environ Microbiol, 1990; 56: 119-1925
15. Schuppler M, Lötzsch K, Waidmann M, Autenrieth B: An abubdance of Escherichia coli is harboured by the mucosaassociated bacterial flora of interleukin-2- deficient mice. nfect Immun, 2004; 72: 1983-1990
16. Franks AH, Harmsen HJ, Raangs GC, Jansen GJ, Schut F, Welling GW: Variations of bacterial populations in human feces measured by fluorescent in situ hybridization with group-specific 16S rRNA-targeted oligonucleotide probes. Appl Environ Microbiol, 1998; 64: 3336-3345
17. Snel J, Heinen PP, Blok HJ, Carman RJ, Ducan AJ, Allen PC, Collins MD: Comparison of 16rRNA sequences of segmented filamentous bacteria isolated from mice, rats and chickens and proposal of Candidatus arthromitus. Int J Syst Bacteriol, 1995; 45: 780-782
18. Kocova J: Overall staining of connective tissue and the muscular layer of vessels. Folia Morphologica, 1970; 3: 293-295
19. Stary HC: Natural history and histological classification of atherosclerotic lesions. Arterioscler Thromb Vasc Biol, 2000; 20: 1177-1178
20. Bobkova D, Tonar Z: Effect of long-term cholesterol diet on cholesterol concentration and development of atherosclerosis in homozygous apolipoprotein E-deficient mice. Acta Veterinaria Brno, 2005; 74: 501-507
21. Nachtigal P, Semecky V, Kopecky M: Application of stereological methods for the quantification of VCAM-1 and ICAM-1 expression in early stages of rabbit atherosclerosis. Path Res Prac, 2004; 200: 219-229
22. Howard CV, Reed MG: Unbiased Stereology: Three Dimensional Measurement in Microscopy. 1st ed. Royal Microscop Soc Handbook Series, Springer-Verlag NY, 41, 1998
23. Russ JC, Dehoff RT: Classical stereological measures: In: Practical Stereology. 2nd ed, JC Russ and RT Dehoff, Ed, Plenum Press NY, 44-54, 2001
24. Nakashima Y, Plump AS, Raines EW, Breslow JL, Ross R: ApoE-Deficient Mice Develop Lesions of All Phases of Atherosclerosis Throughout the Arterial Tree. Arterioscler Thromb, 1994; 14: 133-140
25. Yamazaki K, Honda T, Domon H, Okui T, Kajita K, Amanuma R, Kudoh C, Takashiba S, Kokeguchi S, Nishimura F, Kodama M, Aizawa Z, Oda H: Relationship of periodontal infection to serum antibody levels to periodontopathic bacteria and inflammatory markers in periodontitis patients with coronary disease. Clin Exp Immunol, 2007; 149: 445-452
26. Gibson FC, Hong C, Chou HH, Yumoto H, Chen J, Lien E, Wong J, Genco CA: Innate immune recognition of invasive bacteria accelerates atherosclerosis in apolipoprotein E-deficient mice. Circulation, 2004; 109: 2801-2806
27. Jiang HQ, Kushnir N, Thurnheer MC, Bos NA, Cebra JJ: Monoassociation of SCID mice with Helicobacter muridarum, but not four other enterics, provokes IBD upon receipt of T cells. Gastroenterology, 2002; 122: 1346-1354
28. Ley RE, Turnbaugh PJ, Klein S, Gordon JI: Microbial ecology: human gut microbes associated with obesity. Nature, 2006; 444: 1022-1023
29. King VL, Hatch NW, Chan HW, de Beer MC, de Beer FC, Tannock LR: A murine model of obesity with accelerated atherosclerosis. Br J Pharmacol, 2009; 156: 1067-1075
30. Naruszewicz M, Johansson ML, Zapolska-Downar D, Bukowska H: Effect of Lactobacillus plantarum 299v on cardiovascular disease risk factors in smokers. Am J Clin Nutr, 2002; 876: 1249-1255
31. Portugal LR, Goncalves JL, Fernandes LR, Silva HP, Arantes RM, Nicolo JR, Vieira LQ, Alvarez-Leite JI: Effect of Lactobacillus Delbrüeckii on cholesterol metabolism in germ-free mice and on atherogenesis in apolipoprotein E knock-out mice. Braz J Med Biol Res, 2006; 39: 629-635
32. Karlsson C, Ahrne S, Molin G, Berggren A, Palmquist I, Fredrikson GN, Jeppsson B: Probiotic therapy to men with incipient arteriosclerosis initiates increased bacterial diversity in colon: A randomized controlled trial. Atherosclerosis, on line Jun 18, 2009
33. Tlaskalova-Hogenova H, Stepankova R, Hudcovic T, Tuckova L, Cukrowska B, Lodinova-Zadnikova R, Kozakova H, Rossmann P, Bartova J, Sokol D, Funda DP, Borovska D, Rehakova Z, Sinkora J, Hofman J, Drastich P, Kokesova A: Commensal bacteria (normal microflora), mucosal immunity and chronic inflammatory and autoimmune diseases. Immunol Lett, 2004; 93: 97-108, Review
34. Sinkorova Z, Capkova J, Niederlová J, Stepankova R, Sinkora J: Commensal intestinal bacterial strains trigger ankylosing enthesopathy of the ankle in inbred B10.BR (H-2(k)) male mice. Hum Immunol, 2008; 69: 845-850
35. Hudcovic T, Stepankova R, Kozakova H, Hrncir T, Tlaskalova- Hogenova H: Effects of monocolonization with Escherichia coli strains O6K13 and Nissle 1917 on the development of experimentally induced acute and chronic intestinal inflammation in germ-free immunocompetent and immunodeficient mice. Folia Microbiol, 2007; 52: 618-626
36. Wen L, Ley RE, Volchkov PY, Stranges PB, Avanesyan L, Stonebraker AC, Hu C, Wong FS, Szot GL, Bluestone JA, Gordon JI, Chervonsky AV: Innate immunity and intestinal microbiota in the development of Type 1 diabetes. Nature, 2008; 455: 1109-1113
37. Kajiura T, Takeda T, Sakata S, Sakamoto M, Hashimoto M, Suzuki H, Suzuki M, Benno Y: Change of intestinal microbiota with elemental diet and its impact on therapeutic effects in a murine model of chronic colitis. Dig Dis Sci, 2009; 54: 1892-1900
38. De Palma G, Capilla A, Nadal I, Nova E, Pozo T, Varea V, Polanco I, Castillejo G, López A, Garrote JA, Calvo C, García-Novo MD, Cilleruelo ML, Ribes-Koninckx C, Palau F, Sanz Y: Interplay Between Human Leukocyte Antigen Genes and the Microbial Colonization Process of the Newborn Intestine. Curr Issues Mol Biol, 2009; 12: 1-10
39. Sheikh A, Strachan DP: The hygiene theory: fact or fiction? Curr Opin Otolaryngol Head Neck Surg, 2004; 12: 232-236
40. Hrncir T, Stepankova R, Kozakova H, Hudcovic T, Tlaskalova-Hogenova H: Gut microbiota and lipopolysaccharide content of the diet influence development of regulatory T cells: studies in germ-free mice. BMC Immunol, 2008; 9: 65-69
41. Schenkein HA, Berry CR, Purkall D, Burmeister JA, Brooks CN, Tew JG: Phosphorylcholine-dependent crossreactivity between dental plaque bacteria and oxidized low-density lipoproteins. Infect Immun, 2001; 69: 6612-6617
42. Wu D, Sharan C, Yang H, Goodwin SJ, Zhou L, Grabowski GA, Guo Z: Apolipoprotein E-deficient lipoproteins induce foam cell formation by downregulation of lysosomal hydrolases in macrophages. J Lipid Res, 2007; 48: 2571-2578
43. Galkina E, Kadl A, Sanders J, Varughese D, Sarembock IJ, Ley K: Lymphocyte recruitment into the aortic wall before and during development of atherosclerosis is partially L-selectin dependent. JEM, 2006; 203: 1273-1282