Carboxypeptidase-M is regulated by lipids and CSFs in macrophages and dendritic cells and expressed selectively in tissue granulomas and foam cells

Laboratory Investigation

Volumn 92, Issue 3, 2012, Pages 345-361

  Tsakiris, Ioannis ^a,b   Torocsik, Daniel ^a   Gyongyosi, Adrienn ^a   Dozsa, Aniko ^a   Szatmari, Istvan ^a   Szanto, Attila ^a   Soos, Gyorgyike ^a   Nemes, Zoltan ^a   Igali, Laszlo ^c   Marton, Ildiko ^b   Takats, Zoltan ^d   Nagy, Laszlo ^a   Dezso, Balazs ^a,b  

^a UNIVERSITY OF DEBRECEN   (Hungary)

^b UNIVERSITY OF DEBRECEN   (Hungary)

^c NORFOLK AND NORWICH UNIVERSITY HOSPITAL   (United Kingdom)

^d SEMMELWEIS UNIVERSITY   (Hungary)

Author keywords

carboxypeptidase M; epithelioid cell; granuloma; immunohistochemistry; lipid laden macrophage; qRT PCR

Indexed keywords

CARBOXYPEPTIDASE; CARBOXYPEPTIDASE M; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 4; LIPID; LOW DENSITY LIPOPROTEIN; MESSENGER RNA; UNCLASSIFIED DRUG; VERY LOW DENSITY LIPOPROTEIN;

ARTICLE; ASPIRATION PNEUMONIA; ATHEROSCLEROTIC PLAQUE; CELL DIFFERENTIATION; CELL MATURATION; CELL METABOLISM; CEREBROSPINAL FLUID; CONTROLLED STUDY; DENDRITIC CELL; DOWN REGULATION; ENZYME INDUCTION; ENZYME REGULATION; EPITHELIOID CELL; FOAM CELL; GENE EXPRESSION REGULATION; GRANULOMA; GRANULOMATOUS INFLAMMATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LIPID TRANSPORT; MACROPHAGE; MACROPHAGE ACTIVATION; MICROARRAY ANALYSIS; MONOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; TISSUE SECTION; TUBERCULOSIS; UPREGULATION; XANTHOMA;

BIOLOGICAL MARKERS; CELL DIFFERENTIATION; DENDRITIC CELLS; EPITHELIOID CELLS; FOAM CELLS; GPI-LINKED PROTEINS; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; GRANULOMA; HUMANS; IMMUNOHISTOCHEMISTRY; INTERLEUKIN-4; LIPID METABOLISM; METALLOENDOPEPTIDASES; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REAL-TIME POLYMERASE CHAIN REACTION; RNA, MESSENGER; TRANSCRIPTIONAL ACTIVATION; UP-REGULATION;

EID: 84857734407     PISSN: 00236837     EISSN: 15300307     Source Type: Journal    
DOI: 10.1038/labinvest.2011.168     Document Type: Article

References (54)

1. Kumar V, Abbas AK, Fausto N, Mitchell RN (eds). Robbins Basic Pathology; Granulomatous Inflammation, pp 56-57;
2. Delayed-Type Hypersensitivity, pp 128-130;
3. Maitra A, Fogo BA. Tuberculosis, pp 516-522, 8th edn. Saunders, Elsevier: Philadelphia, PA, 2007.
4. Asano M, Nakane A, Minagawa T. Endogenous gamma interferon is essential in granuloma formation induced by glycolipid-containing mycolic acid in mice. Infect Immun 1993;61:2872-2878. (Pubitemid 23182281)
5. Ulrichs T, Kaufmann SH. New insights into the function of granulomas in human tuberculosis. J Pathol 2006;208:261-269. (Pubitemid 43126118)
6. Aly S, Laskay T, Mages J, et al. Interferon-gamma-dependent mechanisms of mycobacteria-induced pulmonary immunopathology: the role of angiostasis and CXCR3-targeted chemokines for granuloma necrosis. J Pathol 2007;212:295-305. (Pubitemid 47010063)
7. Nagy B, Soós G, Nagy K, et al. Natural course of isolated pulmonary Langerhans' cell histiocytosis in a toddler. 3-year follow-up. Respiration 2008;75:215-220. (Pubitemid 351363879)
8. Skidgel RA, Davis RM, Tan F. Human carboxypeptidase M. Purification and characterization of a membrane-bound carboxypeptidase that cleaves peptide hormones. J Biol Chem 1989;264:2236-2241. (Pubitemid 19057698)
9. Skidgel RA, Õs EG. Cellular carboxypeptidases. Immunol Rev 1998;161:129-141.
10. Deiteren K, Hendriks D, Scharpe S, et al. Carboxypeptidase M: multiple alliances and unknown partners. Clin Chim Acta 2009; 399:24-39.
11. Majdalawieh A, Zhang L, Fuki IV, et al. Adipocyte enhancer-binding protein 1 is a potential novel atherogenic factor involved in macrophage cholesterol homeostasis and inflammation. Proc Natl Acad Sci USA 2006;103:2346-2351. (Pubitemid 43271672)
12. Fujiwara H, Higuchi T, Sato Y, et al. Regulation of human extravillous trophoblast function by membrane-bound peptidases. Biochim Biophys Acta 2005;1751:26-32. (Pubitemid 41033291)
13. Nagae A, Abe M, Becker RP, et al. High concentration of carboxypeptidase M in lungs: presence of the enzyme in alveolar type I cells. Am J Respir Cell Mol Biol 1993;9:221-229.
14. Tsakiris I, Soos G, Nemes Z, et al. The presence of carboxypeptidase-M in tumour cells signifies epidermal growth factor receptor expression in lung adenocarcinomas: the coexistence predicts a poor prognosis regardless of EGFR levels. J Cancer Res Clin Oncol 2008; 134:439-451. (Pubitemid 351322380)
15. Skidgel RA, McGwire GB, Li XY. Membrane anchoring and release of carboxypeptidase M: implications for extracellular hydrolysis of peptide hormones. Immunopharmacology 1996;32:48-52. (Pubitemid 26197967)
16. Zhang X, Tan F, Zhang Y, et al. Carboxypeptidase M and Kinin B1 receptor interact to facilitate efficient B1 signaling from B2 agonists. J Biol Chem 2008;283:7994-8004.
17. McGwire GB, Skidgel RA. Extracellular conversion of epidermal growth factor (EGF) to des-Arg53-EGF by carboxypeptidase M. J Biol Chem 1995;270:17154-17158.
18. Rehli M, Krause SW, Kreutz M, et al. Carboxypeptidase M is identical to the MAX.1 antigen and its expression is associated with monocyte to macrophage differentiation. J Biol Chem 1995;270: 15644-15649.
19. Krause SW, Rehli M, Andreesen R. Carboxypeptidase M as a marker of macrophage maturation. Immunol Rev 1998;161:119-127.
20. Rehli M, Krause SW, Andreesen R. The membrane-bound ectopeptidase CPM as a marker of macrophage maturation in vitro and in vivo. Adv Exp Med Biol 2000;477:205-216. (Pubitemid 32174007)
21. Ridley DS, Ridley MJ. Rationale for the histological spectrum of tuberculosis. A basis for classification. Pathology 1987;19:186-192. (Pubitemid 17094222)
22. Cardona PJ, LIatjos R, Gordillo S, et al. Evolution of granulomas in lungs of mice infected aerogenically with Mycobacterium tuberculosis. Scan J Immunol 2000;52:156-163. (Pubitemid 30649893)
23. Muller H, Kruger S. Immunohistochemical analysis of cell composition and in situ cytokine expression in HIV and non-HIV-associated tuberculous lymphadenitis. Immunobiology 1994;191:354-368. (Pubitemid 24331461)
24. Matsuura F, Yamashita S, Hirano K, et al. Activation of monocytes in vivo causes intracellular accumulation of lipoprotein-derived lipids and marked hypocholesterolemia-a possible pathogenesis of necrobiotic xanthogranuloma. Atherosclerosis 1999;142:355-365. (Pubitemid 29059494)
25. Szeliga J, Daniel DS, Yang CH, et al. Granulocyte-macrophage colony stimulating factor-mediated innate responses in tuberculosis. Tuberculosis 2008;88:7-20. (Pubitemid 350267359)
26. Douda DN, Famakovski N, Dell S, et al. SP-D counteracts GM-CSFmediated increase of granuloma formation by alveolar macrophages in lysinuric protein intolerance. Orphanet J Rare Dis 2009;4:29.
27. Ma Y, Gal A, Koss MN. The pathology of pulmonary sarcoidosis: update. Semin Diagn Pathol 2007;24:150-161. (Pubitemid 47238581)
28. Okabe T. Origin of epithelioid cells in sarcoid granuloma. Nippon Rinsho 2002;60:1714-1719.
29. Dezso B, Haas PG, Hamzavi F, et al. The mechanism of local tumor irradiation combined with interleukin 2 therapy in murine renal carcinoma: histological evaluation of pulmonary metastases. Clin Cancer Res 1996;2:1543-1552. (Pubitemid 126447448)
30. Gogolak P, Rethi B, Szatmari I, et al. Differentiation of CD1a-and CD1a+ monocyte-derived dendritic cells is biased by lipid environment and PPARgamma. Blood 2007;109:643-652.
31. Szanto A, Balint LB, Nagy ZS, et al. STAT6 transcription factor is a facilitator of the nuclear receptor PPARg-regulated gene expression in macrophages and dendritic cells. Immunity 2010;33:699-712.
32. Szatmari I, Goolak P, Im JS, et al. Activation of PPARgamma specifies a dendritic cell subtype capable of enhanced induction of iNKT cell expansion. Immunity 2004;21:95-106. (Pubitemid 38925270)
33. Gustafsson C, Mjö sberg J, Matussek A, et al. Gene expression profiling of human decidual macrophages: evidence for immunosuppressive phenotype. PLoS One 2008;3:e2078.
34. Szanto A, Benko S, Szatmari I, et al. Transcriptional regulation of human CYP27 integrates retinoid, peroxisome proliferator-activated receptor, and liver X receptor signaling in macrophages. Mol Cell Biol 2004;24:8154-8166. (Pubitemid 39167464)
35. Szatmari I, Torocsik D, Agostini M, et al. PPARg regulates the function of human dendritic cells primarily by altering lipid metabolism. Blood 2007;110:3271-3280. (Pubitemid 350106320)
36. Almeida PE, Silva AR, Maya-Monteiro CM, et al. Mycobacterium bovis bacillus Calmette-Gué rin infection induces TLR2-dependent peroxisome proliferator-activated receptor gamma expression and activation: functions in inflammation, lipid metabolism, and pathogenesis. J Immunol 2009;183:1337-1345.
37. Greenspan P, Mayer EP, Fowler SD. Nile red: a selective fluorescent stain for intracellular lipid droplets. J Cell Biol 1985;100: 965-973. (Pubitemid 15135357)
38. Szatmari I, Pap A, Ruhl R, et al. PPARgamma controls CD1d expression by turning on retionic acid synthesis in developing human dendritis cells. J Exp Med 2006;203:2351-2362. (Pubitemid 44498369)
39. Torocsik D, Barath M, Benko S, et al. Activation of liver X receptor sensitizes human dendritic cells to inflammatory stimuli. J Immunol 2010;184:5456-5465.
40. Marton IJ, Dezso B, Radics T, et al. Distribution of interleukin-2 receptor alpha-chain and cells expressing major histocompatibility complex class II antigen in chronic human periapical lesions. Oral Microbiol Immunol 1998;13:259-262. (Pubitemid 28348832)
41. Clemens DL, Horwitz MA. Characterisation of the Mycobacterium tuberculosis phagosome and evidence that phagosomal maturation is inhibited. J Exp Med 1995;181:257-270.
42. Fulton SA, Reba SM, Pai RK, et al. Inhibition of major histocompatibility complex II expression and antigen processing in murine alveolar macrophages by Mycobacterium bovis BCG and 19-kiloDalton mycobacterial lipoprotein. Infect Immun 2004;72:2101-2110. (Pubitemid 38419923)
43. Latchumanan VK, Balkhi MY, Sinha A, et al. Regulation of immune responses to Mycobacterium tuberculosis secretory antigens by dendritic cells. Tuberculosis 2005;85:377-383. (Pubitemid 41617392)
44. Yamauchi A, Dai S-Y, Nakagawa R, et al. Galectin-9 induces maturation of human monocyte-derived dendritic cells. Jpn J Clin Immunol 2005;28:381-388.
45. Beutler E, Grabowski GA. Gaucher disease. In: Scriver CR, Beaudet AL, Sly WS, Valle D (eds). The Metabolic and Molecular Basis of Inherited Disease, Vol. III, 8th edn. McGraw-Hill: New York, 2001, pp 3635-3668.
46. Boven LA, van Meurs M, Boot RG, et al. Gaucher cells demonstrate a distinct macrophage phenotype and resemble alternatively activated macrophages. Am J Clin Pathol 2004;122:359-369. (Pubitemid 39145540)
47. Tontonoz P, Nagy L, Alvarez JG, et al. PPARgamma promotes monocyte/macrophage differentiation and uptake of oxidized LDL. Cell 1998;93:241-252. (Pubitemid 28180857)
48. Dushkin MI, Khoshenko OM, Posokhova EN, et al. Agonist of PPARalpha, PPAR-gamma and inhibits the formation of foam cells from macrophages in mice with inflammation. Bull Exp Biol Med 2007;144: 713-716. (Pubitemid 351486653)
49. Rees AJ. Monocyte and macrophage biology: an overview. Semin Nephrol 2010;30:216-233.
50. Qian B-Z, Pollard JW. Macrophage diversity enhances tumor progression and metastasis. Cell 2010;141:39-51.
51. Marquez-Curtis L, Jalili A, Deiteren K, et al. Carboxypeptidase M expressed by human bone marrow cells cleaves the C-terminal lysine of SDF-1[alpha]: another player in hematopoietic stem/progenitor cell mobilization? Stem Cells 2008;26:1211-1220.
52. Paulson KE, Zhu S, Chen M, et al. Resident intimal dendritic cells accumulate lipid and contribute to the initiation of atherosclerosis. Circ Res 2010;106:383-390.
53. Klos A, Tenner AJ, Johswich KO, et al. The role of the anaphylatoxins in health and disease. Mol Immunol 2009;46:2753-2766.
54. Mount PF, Lane N, Venkatesan S, et al. Bradykinin stimulate endothelial cell fatty acid oxidation by CaMKK-dependent activation of AMPK. Atherosclerosis 2008;200:28-36.