CCR2 and CD44 Promote Inflammatory Cell Recruitment during Fatty Liver Formation in a Lithogenic Diet Fed Mouse Model

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Egan, Charlotte E ^a   Daugherity, Erin K ^a   Rogers, Arlin B ^b   Abi Abdallah, Delbert S ^a   Denkers, Eric Y ^a   Maurer, Kirk J ^a  

^a Department of Obstetrics Gynecology   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; CD45 ANTIGEN; CHEMOKINE RECEPTOR CCR2; HERMES ANTIGEN; HYALURONIC ACID;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CD8+ T LYMPHOCYTE; CELL ACTIVATION; CONTROLLED STUDY; DIET; DISEASE PREDISPOSITION; DISEASE RESISTANCE; ENZYME BLOOD LEVEL; FATTY LIVER; FLOW CYTOMETRY; HEPATITIS; IMMUNOLOGICAL GENE; INFLAMMATORY CELL; LIPID STORAGE; LITHOGENIC DIET; LIVER FIBROSIS; LIVER HISTOLOGY; LIVER PROTECTION; MALE; MONOCYTE; MOUSE; MUTATOR GENE; NONALCOHOLIC FATTY LIVER; NONHUMAN; PHENOTYPE; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN SYNTHESIS INHIBITION; STELLATE CELL;

ANIMALS; ANTIGENS, CD11B; ANTIGENS, CD44; CD8-POSITIVE T-LYMPHOCYTES; CYTOKINES; DENDRITIC CELLS; DIET; DISEASE MODELS, ANIMAL; DISEASE SUSCEPTIBILITY; FATTY LIVER; FEEDING BEHAVIOR; HEPATIC STELLATE CELLS; HEPATITIS; HYALURONIC ACID; INFLAMMATION; INFLAMMATION MEDIATORS; LEUKOCYTES; LIPID METABOLISM; LIVER; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MONOCYTES; PHENOTYPE; RECEPTORS, CCR2;

MUS;

EID: 84878752311     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0065247     Document Type: Article

References (56)

1. Browning JD, Szczepaniak LS, Dobbins R, Nuremberg P, Horton JD, et al. (2004) Prevalence of hepatic steatosis in an urban population in the United States: impact of ethnicity. Hepatology 40: 1387-1395.
2. Williams CD, Stengel J, Asike MI, Torres DM, Shaw J, et al. (2011) Prevalence of Nonalcoholic Fatty Liver Disease and Nonalcoholic Steatohepatitis Among a Largely Middle-Aged Population Utilizing Ultrasound and Liver Biopsy: A Prospective Study. Gastroenterology 140: 124-131.
3. Torres DM, Harrison SA, (2008) Diagnosis and therapy of nonalcoholic steatohepatitis. Gastroenterology 134: 1682-1698.
4. Harmon RC, Tiniakos DG, Argo CK, (2011) Inflammation in nonalcoholic steatohepatitis. Expert Rev Gastroenterol Hepatol 5: 189-200.
5. Kamada Y, Kiso S, Yoshida Y, Chatani N, Kizu T, et al. (2011) Estrogen deficiency worsens steatohepatitis in mice fed high-fat and high-cholesterol diet. Am J Physiol Gastrointest Liver Physiol 301: G1031-1043.
6. Bertola A, Bonnafous S, Anty R, Patouraux S, Saint-Paul MC, et al. (2010) Hepatic expression patterns of inflammatory and immune response genes associated with obesity and NASH in morbidly obese patients. PLoS One 5: e13577.
7. Haukeland JW, Damas JK, Konopski Z, Loberg EM, Haaland T, et al. (2006) Systemic inflammation in nonalcoholic fatty liver disease is characterized by elevated levels of CCL2. J Hepatol 44: 1167-1174.
8. Tamura Y, Sugimoto M, Murayama T, Minami M, Nishikaze Y, et al. (2010) C-C chemokine receptor 2 inhibitor improves diet-induced development of insulin resistance and hepatic steatosis in mice. J Atheroscler Thromb 17: 219-228.
9. Tamura Y, Sugimoto M, Murayama T, Ueda Y, Kanamori H, et al. (2008) Inhibition of CCR2 ameliorates insulin resistance and hepatic steatosis in db/db mice. Arterioscler Thromb Vasc Biol 28: 2195-2201.
10. Daugherity EK, Balmus G, Al Saei A, Moore ES, Abi Abdallah D, et al. (2012) The DNA damage checkpoint protein ATM promotes hepatocellular apoptosis and fibrosis in a mouse model of non-alcoholic fatty liver disease. Cell Cycle 11: 1918-1928.
11. Serbina NV, Hohl TM, Cherny M, Pamer EG, (2009) Selective expansion of the monocytic lineage directed by bacterial infection. J Immunol 183: 1900-1910.
12. Woo J, Lu L, Rao AS, Li Y, Subbotin V, et al. (1994) Isolation, phenotype, and allostimulatory activity of mouse liver dendritic cells. Transplantation 58: 484-491.
13. Liao HX, Lee DM, Levesque MC, Haynes BF, (1995) N-terminal and central regions of the human CD44 extracellular domain participate in cell surface hyaluronan binding. J Immunol 155: 3938-3945.
14. Egan CE, Maurer KJ, Cohen SB, Mack M, Simpson KW, et al. (2011) Synergy between intraepithelial lymphocytes and lamina propria T cells drives intestinal inflammation during infection. Mucosal Immunol 4: 658-670.
15. Miura K, Yang L, van Rooijen N, Ohnishi H, Seki E, (2012) Hepatic recruitment of macrophages promotes nonalcoholic steatohepatitis through CCR2. American Journal of Physiology-Gastrointestinal and Liver Physiology 302: G1310-G1321.
16. McDonald B, McAvoy EF, Lam F, Gill V, de la Motte C, et al. (2008) Interaction of CD44 and hyaluronan is the dominant mechanism for neutrophil sequestration in inflamed liver sinusoids. J Exp Med 205: 915-927.
17. Gee K, Kryworuchko M, Kumar A, (2004) Recent advances in the regulation of CD44 expression and its role in inflammation and autoimmune diseases. Arch Immunol Ther Exp (Warsz) 52: 13-26.
18. Levesque MC, Haynes BF, (1997) Cytokine induction of the ability of human monocyte CD44 to bind hyaluronan is mediated primarily by TNF-alpha and is inhibited by IL-4 and IL-13. J Immunol 159: 6184-6194.
19. Maiti A, Maki G, Johnson P, (1998) TNF-alpha induction of CD44-mediated leukocyte adhesion by sulfation. Science 282: 941-943.
20. Bertola A, Deveaux V, Bonnafous S, Rousseau D, Anty R, et al. (2009) Elevated expression of osteopontin may be related to adipose tissue macrophage accumulation and liver steatosis in morbid obesity. Diabetes 58: 125-133.
21. Egan CE, Craven MD, Leng J, Mack M, Simpson KW, et al. (2009) CCR2-dependent intraepithelial lymphocytes mediate inflammatory gut pathology during Toxoplasma gondii infection. Mucosal Immunol 2: 527-535.
22. Le Y, Zhou Y, Iribarren P, Wang J, (2004) Chemokines and chemokine receptors: their manifold roles in homeostasis and disease. Cell Mol Immunol 1: 95-104.
23. Vanbervliet B, Homey B, Durand I, Massacrier C, Ait-Yahia S, et al. (2002) Sequential involvement of CCR2 and CCR6 ligands for immature dendritic cell recruitment: possible role at inflamed epithelial surfaces. Eur J Immunol 32: 231-242.
24. Kim CH, Johnston B, Butcher EC, (2002) Trafficking machinery of NKT cells: shared and differential chemokine receptor expression among V alpha 24(+)V beta 11(+) NKT cell subsets with distinct cytokine-producing capacity. Blood 100: 11-16.
25. Wolpe SD, Davatelis G, Sherry B, Beutler B, Hesse DG, et al. (1988) Macrophages secrete a novel heparin-binding protein with inflammatory and neutrophil chemokinetic properties. J Exp Med 167: 570-581.
26. Zaldivar MM, Pauels K, von Hundelshausen P, Berres ML, Schmitz P, et al. (2010) CXC chemokine ligand 4 (Cxcl4) is a platelet-derived mediator of experimental liver fibrosis. Hepatology 51: 1345-1353.
27. Kassel KM, Guo GL, Tawfik O, Luyendyk JP, (2010) Monocyte chemoattractant protein-1 deficiency does not affect steatosis or inflammation in livers of mice fed a methionine-choline-deficient diet. Lab Invest 90: 1794-1804.
28. Baeck C, Wehr A, Karlmark KR, Heymann F, Vucur M, et al. (2012) Pharmacological inhibition of the chemokine CCL2 (MCP-1) diminishes liver macrophage infiltration and steatohepatitis in chronic hepatic injury. Gut 61: 416-426.
29. Mbitikon-Kobo FM, Vocanson M, Michallet MC, Tomkowiak M, Cottalorda A, et al. (2009) Characterization of a CD44/CD122int memory CD8 T cell subset generated under sterile inflammatory conditions. J Immunol 182: 3846-3854.
30. Legras S, Levesque JP, Charrad R, Morimoto K, Le Bousse C, et al. (1997) CD44-mediated adhesiveness of human hematopoietic progenitors to hyaluronan is modulated by cytokines. Blood 89: 1905-1914.
31. Yamawaki H, Hirohata S, Miyoshi T, Takahashi K, Ogawa H, et al. (2009) Hyaluronan receptors involved in cytokine induction in monocytes. Glycobiology 19: 83-92.
32. Gee K, Lim W, Ma W, Nandan D, Diaz-Mitoma F, et al. (2002) Differential regulation of CD44 expression by lipopolysaccharide (LPS) and TNF-alpha in human monocytic cells: distinct involvement of c-Jun N-terminal kinase in LPS-induced CD44 expression. J Immunol 169: 5660-5672.
33. Levesque MC, Haynes BF, (2001) Activated T lymphocytes regulate hyaluronan binding to monocyte CD44 via production of IL-2 and IFN-gamma. J Immunol 166: 188-196.
34. Vicari AP, Vanbervliet B, Massacrier C, Chiodoni C, Vaure C, et al. (2004) In vivo manipulation of dendritic cell migration and activation to elicit antitumour immunity. Novartis Found Symp 256: 241-254; discussion 254-269.
35. Termeer C, Johannsen H, Braun T, Renkl A, Ahrens T, et al. (2001) The role of CD44 during CD40 ligand-induced dendritic cell clustering and maturation. J Leukoc Biol 70: 715-722.
36. Spruss A, Kanuri G, Wagnerberger S, Haub S, Bischoff SC, et al. (2009) Toll-like receptor 4 is involved in the development of fructose-induced hepatic steatosis in mice. Hepatology 50: 1094-1104.
37. Baffy G, (2009) Kupffer cells in non-alcoholic fatty liver disease: the emerging view. J Hepatol 51: 212-223.
38. Ibrahim J, Nguyen AH, Rehman A, Ochi A, Jamal M, et al. (2012) Dendritic cell populations with different concentrations of lipid regulate tolerance and immunity in mouse and human liver. Gastroenterology 143: 1061-1072.
39. Karlmark KR, Weiskirchen R, Zimmermann HW, Gassler N, Ginhoux F, et al. (2009) Hepatic recruitment of the inflammatory Gr1+ monocyte subset upon liver injury promotes hepatic fibrosis. Hepatology 50: 261-274.
40. Syn WK, Agboola KM, Swiderska M, Michelotti GA, Liaskou E, et al. (2012) NKT-associated hedgehog and osteopontin drive fibrogenesis in non-alcoholic fatty liver disease. Gut 61: 1323-1329.
41. Syn WK, Choi SS, Liaskou E, Karaca GF, Agboola KM, et al. (2011) Osteopontin is induced by hedgehog pathway activation and promotes fibrosis progression in nonalcoholic steatohepatitis. Hepatology 53: 106-115.
42. Sahai A, Malladi P, Melin-Aldana H, Green RM, Whitington PF, (2004) Upregulation of osteopontin expression is involved in the development of nonalcoholic steatohepatitis in a dietary murine model. Am J Physiol Gastrointest Liver Physiol 287: G264-273.
43. Egan CE, Cohen SB, Denkers EY (2011) Insights into inflammatory bowel disease using Toxoplasma gondii as an infectious trigger. Immunol Cell Biol.
44. Kang HS, Liao G, Degraff LM, Gerrish K, Bortner CD, et al. (2013) CD44 Plays a Critical Role in Regulating Diet-Induced Adipose Inflammation, Hepatic Steatosis, and Insulin Resistance. PLoS One 8: e58417.
45. Wang DQ, Carey MC, (2002) Susceptibility to murine cholesterol gallstone formation is not affected by partial disruption of the HDL receptor SR-BI. Biochim Biophys Acta 1583: 141-150.
46. Wang DQ, Zhang L, Wang HH, (2005) High cholesterol absorption efficiency and rapid biliary secretion of chylomicron remnant cholesterol enhance cholelithogenesis in gallstone-susceptible mice. Biochim Biophys Acta 1733: 90-99.
47. Wittenburg H, Lammert F, Wang DQ, Churchill GA, Li R, et al. (2002) Interacting QTLs for cholesterol gallstones and gallbladder mucin in AKR and SWR strains of mice. Physiol Genomics 8: 67-77.
48. Matsuzawa N, Takamura T, Kurita S, Misu H, Ota T, et al. (2007) Lipid-induced oxidative stress causes steatohepatitis in mice fed an atherogenic diet. Hepatology 46: 1392-1403.
49. Schreyer SA, Wilson DL, LeBoeuf RC, (1998) C57BL/6 mice fed high fat diets as models for diabetes-accelerated atherosclerosis. Atherosclerosis 136: 17-24.
50. Davies JP, Scott C, Oishi K, Liapis A, Ioannou YA, (2005) Inactivation of NPC1L1 causes multiple lipid transport defects and protects against diet-induced hypercholesterolemia. J Biol Chem 280: 12710-12720.
51. Moschetta A, Bookout AL, Mangelsdorf DJ, (2004) Prevention of cholesterol gallstone disease by FXR agonists in a mouse model. Nat Med 10: 1352-1358.
52. Uppal H, Zhai Y, Gangopadhyay A, Khadem S, Ren S, et al. (2008) Activation of liver X receptor sensitizes mice to gallbladder cholesterol crystallization. Hepatology 47: 1331-1342.
53. Amarapurkar DN, Patel ND, (2004) Clinical spectrum and natural history of non-alcoholic steatohepatitis with normal alanine aminotransferase values. Trop Gastroenterol 25: 130-134.
54. Charatcharoenwitthaya P, Lindor KD, Angulo P, (2012) The spontaneous course of liver enzymes and its correlation in nonalcoholic fatty liver disease. Dig Dis Sci 57: 1925-1931.
55. Mofrad P, Contos MJ, Haque M, Sargeant C, Fisher RA, et al. (2003) Clinical and histologic spectrum of nonalcoholic fatty liver disease associated with normal ALT values. Hepatology 37: 1286-1292.
56. Marra F, Gastaldelli A, Svegliati Baroni G, Tell G, Tiribelli C, (2008) Molecular basis and mechanisms of progression of non-alcoholic steatohepatitis. Trends Mol Med 14: 72-81.