Macrophage colony-stimulating factor (CSF1) controls monocyte production and maturation and the steady-state size of the liver in pigs

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 311, Issue 3, 2016, Pages G533-G547

  Sauter, Kristin A ^a   Waddell, Lindsey A ^a   Lisowski, Zofia M ^a   Young, Rachel ^a   Lefevre, Lucas ^a   Davis, Gemma M ^a   Clohisey, Sara M ^a   McCulloch, Mary ^a   Magowan, Elizabeth ^b   Mabbott, Neil A ^a   Summers, Kim M ^a   Hume, David A ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b AGRI FOOD AND BIOSCIENCES INSTITUTE   (United Kingdom)

Author keywords

CD163; Hepatosplenomegaly; Hepatostat; M CSF; Macrophages

Indexed keywords

BILE ACID; BILIRUBIN; CD163 ANTIGEN; COLONY STIMULATING FACTOR 1; COLONY STIMULATING FACTOR 1 FC; INTERLEUKIN 1; INTERLEUKIN 6; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; ANTIBODY; CYTOCHROME P450; LEUKOCYTE ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE MARROW; CELL DIFFERENTIATION; CELL INFILTRATION; CELL MATURATION; CELL PROLIFERATION; CONTROLLED STUDY; FEEDBACK SYSTEM; FEMALE; HEPATOSPLENOMEGALY; LIVER CELL; LIVER REGENERATION; LIVER SIZE; LIVER WEIGHT; MACROPHAGE; MALE; MONOCYTE; MONOCYTOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPLEEN WEIGHT; ANIMAL; GENE EXPRESSION REGULATION; GENETICS; LIVER; METABOLISM; MONONUCLEAR CELL; PHYSIOLOGY; PIG;

ANIMALS; ANTIBODIES; ANTIGENS, CD; CYTOCHROME P-450 ENZYME SYSTEM; FEMALE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; LEUKOCYTES, MONONUCLEAR; LIVER; MACROPHAGE COLONY-STIMULATING FACTOR; MALE; MONOCYTES; SWINE;

EID: 84986626395     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00116.2016     Document Type: Article

References (52)

1. Alikhan MA, Jones CV, Williams TM, Beckhouse AG, Fletcher AL, Kett MM, Sakkal S, Samuel CS, Ramsay RG, Deane JA, Wells CA, Little MH, Hume DA, Ricardo SD. Colony-stimulating factor-1 promotes kidney growth and repair via alteration of macrophage responses. Am J Pathol 179: 1243-1256, 2011
2. Alison MR, Lin WR. Hepatocyte turnover and regeneration: virtually a virtuoso performance. Hepatology 53: 1393-1396, 2011
3. Bailey M, Haverson K, Inman C, Harris C, Jones P, Corfield G, Miller B, Stokes C. The development of the mucosal immune system preand post-weaning: balancing regulatory and effector function. Proc Nutr Soc 64: 451-457, 2005
4. Bartocci A, Mastrogiannis DS, Migliorati G, Stockert RJ, Wolkoff AW, Stanley ER. Macrophages specifically regulate the concentration of their own growth factor in the circulation. Proc Natl Acad Sci USA 84: 6179-6183, 1987
5. Boissonneault V, Filali M, Lessard M, Relton J, Wong G, Rivest S. Powerful beneficial effects of macrophage colony-stimulating factor on beta-amyloid deposition and cognitive impairment in Alzheimer’s disease. Brain 132: 1078-1092, 2009
6. Cenci S, Weitzmann MN, Gentile MA, Aisa MC, Pacifici R. M-CSF neutralization and egr-1 deficiency prevent ovariectomy-induced bone loss. J Clin Invest 105: 1279-1287, 2000
7. Chazaud B. Macrophages: supportive cells for tissue repair and regeneration. Immunobiology 219: 172-178, 2014
8. Chen BP, Kuziel WA, Lane TE. Lack of CCR2 results in increased mortality and impaired leukocyte activation and trafficking following infection of the central nervous system with a neurotropic coronavirus. J Immunol 167: 4585-4592, 2001
9. Chitu V, Stanley ER. Colony-stimulating factor-1 in immunity and inflammation. Curr Opin Immunol 18: 39-48, 2006
10. Chow A, Huggins M, Ahmed J, Hashimoto D, Lucas D, Kunisaki Y, Pinho S, Leboeuf M, Noizat C, van Rooijen N, Tanaka M, Zhao Z.J, Bergman A, Merad M, Frenette PS. CD169() macrophages provide a niche promoting erythropoiesis under homeostasis and stress. Nat Med 19: 429-436, 2013
11. Cole DJ, Sanda MG, Yang JC, Schwartzentruber DJ, Weber J, Ettinghausen SE, Pockaj BA, Kim HI, Levin RD, Pogrebniak HW, Balkissoon J, Fenton RM, DeBarge LR, Kaye J, Rosenberg SA, Parkinson DR. Phase I trial of recombinant human macrophage colonystimulating factor administered by continuous intravenous infusion in patients with metastatic cancer. J Natl Cancer Inst 86: 39-45, 1994
12. Dai XM, Ryan GR, Hapel AJ, Dominguez MG, Russell RG, Kapp S, Sylvestre V, Stanley ER. Targeted disruption of the mouse colonystimulating factor 1 receptor gene results in osteopetrosis, mononuclear phagocyte deficiency, increased primitive progenitor cell frequencies, and reproductive defects. Blood 99: 111-120, 2002
13. Dixon JE, Allan JE, Doherty PC, Hume DA. Immunohistochemical analysis of the involvement of F4/80 and Ia-positive macrophages in mouse liver infected with lymphocytic choriomeningitis virus. J Leukoc Biol 40: 617-628, 1986
14. Duan X, Nauwynck HJ, Pensaert MB. Effects of origin and state of differentiation and activation of monocytes/macrophages on their susceptibility to porcine reproductive and respiratory syndrome virus (PRRSV). Arch Virol 142: 2483-2497, 1997
15. Elsegood CL, Chan CW, Degli-Esposti MA, Wikstrom ME, Domenichini A, Lazarus K, van Rooijen N, Ganss R, Olynyk JK, Yeoh GC. Kupffer cell-monocyte communication is essential for initiating murine liver progenitor cell-mediated liver regeneration. Hepatology 62: 1272-1284, 2015
16. Fairbairn L, Kapetanovic R, Beraldi D, Sester DP, Tuggle CK, Archibald AL, Hume DA. Comparative analysis of monocyte subsets in the pig. J Immunol 190: 6389-6396, 2013
17. Fairbairn L, Kapetanovic R, Sester DP, Hume DA. The mononuclear phagocyte system of the pig as a model for understanding human innate immunity and disease. J Leukoc Biol 89: 855-871, 2011
18. Freeman TC, Ivens A, Baillie JK, Beraldi D, Barnett MW, Dorward D, Downing A, Fairbairn L, Kapetanovic R, Raza S, Tomoiu A, Alberio R, Wu C, Su AI, Summers KM, Tuggle CK, Archibald AL, Hume DA. A gene expression atlas of the domestic pig. BMC Biol 10: 90, 2012
19. Gougelet A, Torre C, Veber P, Sartor C, Bachelot L, Denechaud PD, Godard C, Moldes M, Burnol AF, Dubuquoy C, Terris B, Guillonneau F, Ye T, Schwarz M, Braeuning A, Perret C, Colnot S. T-cell factor 4 and beta-catenin chromatin occupancies pattern zonal liver metabolism in mice. Hepatology 59: 2344-2357, 2014
20. Gow DJ, Garceau V, Kapetanovic R, Sester DP, Fici GJ, Shelly JA, Wilson TL, Hume DA. Cloning and expression of porcine Colony Stimulating Factor-1 (CSF-1) and Colony Stimulating Factor-1 Receptor (CSF-1R) and analysis of the species specificity of stimulation by CSF-1 and Interleukin 34. Cytokine 60: 793-805, 2012
21. Gow DJ, Sauter KA, Pridans C, Moffat L, Sehgal A, Stutchfield BM, Raza S, Beard PM, Tsai YT, Bainbridge G, Boner PL, Fici G, Garcia-Tapia D, Martin RA, Oliphant T, Shelly JA, Tiwari R, Wilson TL, Smith LB, Mabbott NA, Hume DA. Characterisation of a novel Fc conjugate of macrophage colony-stimulating factor. Mol Ther 22: 1580-1592, 2014
22. Heymann F, Tacke F. Immunology in the liver - from homeostasis to disease. Nat Rev Gastroenterol Hepatol 13: 88-110, 2016
23. Hume DA, MacDonald KP. Therapeutic applications of macrophage colony-stimulating factor-1 (CSF-1) and antagonists of CSF-1 receptor (CSF-1R) signaling. Blood 119: 1810-1820, 2012
24. Hume DA, Pavli P, Donahue RE, Fidler IJ. The effect of human recombinant macrophage colony-stimulating factor (CSF-1) on the murine mononuclear phagocyte system in vivo. J Immunol 141: 3405-3409, 1988
25. Hume DA, Weidemann MJ. Role and regulation of glucose metabolism in proliferating cells. J Natl Cancer Inst 62: 3-8, 1979
26. Huynh D, Akcora D, Malaterre J, Chan CK, Dai XM, Bertoncello I, Stanley ER, Ramsay RG. CSF-1 receptor-dependent colon development, homeostasis and inflammatory stress response. PLoS One 8: e56951, 2013
27. Jaeschke H. Mechanisms of Liver Injury. II. Mechanisms of neutrophilinduced liver cell injury during hepatic ischemia-reperfusion and other acute inflammatory conditions. Am J Physiol Gastrointest Liver Physiol 290: G1083-G1088, 2006
28. Jakubowski AA, Bajorin DF, Templeton MA, Chapman PB, Cody BV, Thaler H, Tao Y, Filippa DA, Williams L, Sherman ML, Garnick MB, Houghton AN. Phase I study of continuous-infusion recombinant macrophage colony-stimulating factor in patients with metastatic melanoma. Clin Cancer Res 2: 295-302, 1996
29. Kapetanovic R, Fairbairn L, Beraldi D, Sester DP, Archibald AL, Tuggle CK, Hume DA. Pig bone marrow-derived macrophages resemble human macrophages in their response to bacterial lipopolysaccharide. J Immunol 188: 3382-3394, 2012
30. Kapetanovic R, Fairbairn L, Downing A, Beraldi D, Sester DP, Freeman TC, Tuggle CK, Archibald AL, Hume DA. The impact of breed and tissue compartment on the response of pig macrophages to lipopolysaccharide. BMC Genomics 14: 581, 2013
31. Korkosz M, Bukowska-Strakova K, Sadis S, Grodzicki T, Siedlar M. Monoclonal antibodies against macrophage colony-stimulating factor diminish the number of circulating intermediate and nonclassical (CD14()CD16()/CD14()CD16()) monocytes in rheumatoid arthritis patient. Blood 119: 5329-5330, 2012
32. Lee KC, Palacios Jimenez C, Alibhai H, Chang YM, Leckie PJ, Baker LA, Stanzani G, Priestnall SL, Mookerjee RP, Jalan R, Davies NA. A reproducible, clinically relevant, intensively managed, pig model of acute liver failure for testing of therapies aimed to prolong survival. Liver Int 33: 544-551, 2013
33. MacDonald KP, Palmer JS, Cronau S, Seppanen E, Olver S, Raffelt NC, Kuns R, Pettit AR, Clouston A, Wainwright B, Branstetter D, Smith J, Paxton RJ, Cerretti DP, Bonham L, Hill GR, Hume DA. An antibody against the colony-stimulating factor 1 receptor depletes the resident subset of monocytes and tissueand tumor-associated macrophages but does not inhibit inflammation. Blood 116: 3955-3963, 2010
34. Michalopoulos GK. Advances in liver regeneration. Expert Rev Gastroenterol Hepatol 8: 897-907, 2014
35. Michalopoulos GK. Liver regeneration after partial hepatectomy: critical analysis of mechanistic dilemmas. Am J Pathol 176: 2-13, 2010
36. Michalopoulos GK. Principles of liver regeneration and growth homeostasis. Compr Physiol 3: 485-513, 2013
37. Mitrasinovic OM, Vincent VA, Simsek D, Murphy GM Jr. Macrophage colony stimulating factor promotes phagocytosis by murine microglia. Neurosci Lett 344: 185-188, 2003
38. Moeser AJ, Klok CV, Ryan KA, Wooten JG, Little D, Cook VL, Blikslager AT. Stress signaling pathways activated by weaning mediate intestinal dysfunction in the pig. Am J Physiol Gastrointest Liver Physiol 292: G173-G181, 2007
39. Moffat L, Rothwell L, Garcia-Morales C, Sauter KA, Kapetanovic R, Gow DJ, Hume DA. Development and characterisation of monoclonal antibodies reactive with porcine CSF1R (CD115). Dev Comp Immunol 47: 123-128, 2014
40. Nehra D, Fallon EM, Puder M. The prevention and treatment of intestinal failure-associated liver disease in neonates and children. Surg Clin North Am 91: 543-563, 2011
41. Newsome PN, Henderson NC, Nelson LJ, Dabos C, Filippi C, Bellamy C, Howie F, Clutton RE, King T, Lee A, Hayes PC, Plevris JN. Development of an invasively monitored porcine model of acetaminophen-induced acute liver failure. BMC Gastroenterol 10: 34, 2010
42. Pohl CS, Medland JE, Moeser AJ. Early-life stress origins of gastrointestinal disease: animal models, intestinal pathophysiology, and translational implications. Am J Physiol Gastrointest Liver Physiol 309: G927-G941, 2015
43. Pollard JW. Trophic macrophages in development and disease. Nat Rev Immunol 9: 259-270, 2009
44. Sauter KA, Pridans C, Sehgal A, Bain CC, Scott C, Moffat L, Rojo R, Stutchfield BM, Davies CL, Donaldson DS, Renault K, McColl BW, Mowat AM, Serrels A, Frame MC, Mabbott NA, Hume DA. The MacBlue binary transgene (csf1r-gal4VP16/UAS-ECFP) provides a novel marker for visualisation of subsets of monocytes, macrophages and dendritic cells and responsiveness to CSF1 administration. PLoS One 9: e105429, 2014
45. Sauter KA, Pridans C, Sehgal A, Tsai YT, Bradford BM, Raza S, Moffat L, Gow DJ, Beard PM, Mabbott NA, Smith LB, Hume DA. Pleiotropic effects of extended blockade of CSF1R signaling in adult mice. J Leukoc Biol 96: 265-274, 2014
46. Stutchfield BM, Antoine DJ, Mackinnon AC, Gow DJ, Bain CC, Hawley CA, Hughes M, Francis B, Wojtacha D, Man TY, Dear JW, Devey LR, Mowat AM, Pollard JW, Park BK, Jenkins SJ, Simpson KJ, Hume DA, Wigmore SJ, Forbes SJ. CSF1 restores innate immunity after liver injury in mice and serum levels indicate outcomes of patients with acute liver failure. Gastroenterology 149: 1896-1909.e14, 2015
47. Thomas JA, Pope C, Wojtacha D, Robson AJ, Gordon-Walker TT, Hartland S, Ramachandran P, Van Deemter M, Hume DA, Iredale JP, Forbes SJ. Macrophage therapy for murine liver fibrosis recruits host effector cells improving fibrosis, regeneration, and function. Hepatology 53: 2003-2015, 2011
48. Torre C, Perret C, Colnot S. Molecular determinants of liver zonation. Prog Mol Biol Transl Sci 97: 127-150, 2010
49. Tsou CL, Peters W, Si Y, Slaymaker S, Aslanian AM, Weisberg SP, Mack M, Charo IF. Critical roles for CCR2 and MCP-3 in monocyte mobilization from bone marrow and recruitment to inflammatory sites. J Clin Invest 117: 902-909, 2007
50. Visser JJ, Bom-van Noorloos AA, Meijer S, Hoitsma HF. Serum total bile acids monitoring after experimental orthotopic liver transplantation. J Surg Res 36: 147-153, 1984
51. Yona S, Kim KW, Wolf Y, Mildner A, Varol D, Breker M, StraussAyali D, Viukov S, Guilliams M, Misharin A, Hume DA, Perlman H, Malissen B, Zelzer E, Jung S. Fate mapping reveals origins and dynamics of monocytes and tissue macrophages under homeostasis. Immunity 38: 79-91, 2013
52. Zhang J, Babic A. Regulation of the MET oncogene: molecular mechanisms. Carcinogenesis 2016