Macrophages promote progression of spasmolytic polypeptide-expressing metaplasia after acute loss of parietal cells

Gastroenterology

Volumn 146, Issue 7, 2014, Pages

  Petersen, Christine P ^a,b   Weis, Victoria G ^a,b   Nam, Ki Taek ^b,c   Sousa, Josane F ^b   Fingleton, Barbara ^a   Goldenring, James R ^a,b,d  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VANDERBILT UNIVERSITY   (United States)

^c Yonsei University College of Medicine   (South Korea)

^d VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Acute Injury; CD68; Gastric Cancer; Immune Depletion

Indexed keywords

CLODRONIC ACID; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; GLUTATHIONE PEROXIDASE 2; RAG1 PROTEIN;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DISEASE COURSE; INFLAMMATION; INFLAMMATORY CELL; INNATE IMMUNITY; MACROPHAGE; METAPLASIA; MOUSE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; SPASMOLYTIC POLYPEPTIDE EXPRESSING METAPLASIA; STOMACH PARIETAL CELL; UPREGULATION;

ACUTE INJURY; CD68; GASTRIC CANCER; IMMUNE DEPLETION;

ADAPTIVE IMMUNITY; ANIMALS; ATROPHY; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; DISEASE MODELS, ANIMAL; GASTRITIS; GENE EXPRESSION REGULATION, NEOPLASTIC; GLUTATHIONE PEROXIDASE; HOMEODOMAIN PROTEINS; IMMUNITY, INNATE; INFLAMMATION MEDIATORS; INTERFERON-GAMMA; MACROPHAGES; MALE; METAPLASIA; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUCINS; NEUTROPHILS; PARIETAL CELLS, GASTRIC; PEPTIDES; PHENOTYPE; RNA, MESSENGER; STOMACH NEOPLASMS; UP-REGULATION;

EID: 84901228104     PISSN: 00165085     EISSN: 15280012     Source Type: Journal    
DOI: 10.1053/j.gastro.2014.02.007     Document Type: Article

References (56)

1. C. de Martel, J. Ferlay, and S. Franceschi et al. Global burden of cancers attributable to infections in 2008: a review and synthetic analysis Lancet Oncol 13 2012 607 615
2. M.J. Blaser, and J. Parsonnet Parasitism by the "slow" bacterium Helicobacter pylori leads to altered gastric homeostasis and neoplasia J Clin Invest 94 1994 4 8
3. K.T. Nam, H.J. Lee, and J.F. Sousa et al. Mature chief cells are cryptic progenitors for metaplasia in the stomach Gastroenterology 139 2010 2028 2037.e9
4. V.G. Weis, J.F. Sousa, and B.J. Lafleur et al. Heterogeneity in mouse spasmolytic polypeptide-expressing metaplasia lineages identifies markers of metaplastic progression Gut 62 2013 1270 1279
5. N. Yoshizawa, Y. Takenaka, and H. Yamaguchi et al. Emergence of spasmolytic polypeptide-expressing metaplasia in Mongolian gerbils infected with Helicobacter pylori Lab Invest 87 2007 1265 1276
6. K.T. Nam, H.J. Lee, and H. Mok et al. Amphiregulin-deficient mice develop spasmolytic polypeptide expressing metaplasia and intestinal metaplasia Gastroenterology 136 2009 1288 1296
7. J.R. Goldenring, K.T. Nam, and T.C. Wang et al. Spasmolytic polypeptide-expressing metaplasia and intestinal metaplasia: time for reevaluation of metaplasias and the origins of gastric cancer Gastroenterology 138 2010 2207 2210 2210.e1
8. A. Meining, A. Morgner, and S. Miehlke et al. Atrophy-metaplasia- dysplasia-carcinoma sequence in the stomach: a reality or merely an hypothesis? Best Pract Res Clin Gastroenterol 15 2001 983 998
9. H.M. El-Zimaity, H. Ota, and D.Y. Graham et al. Patterns of gastric atrophy in intestinal type gastric carcinoma Cancer 94 2002 1428 1436
10. J.R. Goldenring, G.S. Ray, and R.J. Coffey et al. Reversible drug-induced oxyntic atrophy in rats Gastroenterology 118 2000 1080 1093
11. S. Nomura, H. Yamaguchi, and M. Ogawa et al. Alterations in gastric mucosal lineages induced by acute oxyntic atrophy in wild-type and gastrin-deficient mice Am J Physiol Gastrointest Liver Physiol 288 2005 G362 G375
12. T.C. Wang, C.A. Dangler, and D. Chen et al. Synergistic interaction between hypergastrinemia and Helicobacter infection in a mouse model of gastric cancer Gastroenterology 118 2000 36 47
13. J. Houghton, C. Stoicov, and S. Nomura et al. Gastric cancer originating from bone marrow-derived cells Science 306 2004 1568 1571
14. C. Varon, P. Dubus, and F. Mazurier et al. Helicobacter pylori infection recruits bone marrow-derived cells that participate in gastric preneoplasia in mice Gastroenterology 142 2012 281 291
15. J.G. Fox, M. Blanco, and J.C. Murphy et al. Local and systemic immune responses in murine Helicobacter felis active chronic gastritis Infect Immun 61 1993 2309 2315
16. K.A. Roth, S.B. Kapadia, and S.M. Martin et al. Cellular immune responses are essential for the development of Helicobacter felis-associated gastric pathology J Immunol 163 1999 1490 1497
17. A. Chow, B.D. Brown, and M. Merad Studying the mononuclear phagocyte system in the molecular age Nat Rev Immunol 11 2011 788 798
18. Z. Liu, E.S. Demitrack, and T.M. Keeley et al. IFNgamma contributes to the development of gastric epithelial cell metaplasia in Huntingtin interacting protein 1 related (Hip1r)-deficient mice Lab Invest 92 2012 1045 1057
19. M.T. Silva When two is better than one: macrophages and neutrophils work in concert in innate immunity as complementary and cooperative partners of a myeloid phagocyte system J Leukoc Biol 87 2010 93 106
20. J.M. Daley, A.A. Thomay, and M.D. Connolly et al. Use of Ly6G-specific monoclonal antibody to deplete neutrophils in mice J Leukoc Biol 83 2008 64 70
21. D.A. Ferenbach, T.A. Sheldrake, and K. Dhaliwal et al. Macrophage/monocyte depletion by clodronate, but not diphtheria toxin, improves renal ischemia/reperfusion injury in mice Kidney Int 82 2012 928 933
22. M.J. van Amerongen, M.C. Harmsen, and N. van Rooijen et al. Macrophage depletion impairs wound healing and increases left ventricular remodeling after myocardial injury in mice Am J Pathol 170 2007 818 829
23. S.J. Jenkins, D. Ruckerl, and P.C. Cook et al. Local macrophage proliferation, rather than recruitment from the blood, is a signature of TH2 inflammation Science 332 2011 1284 1288
24. J.L. Stoger, M.J. Gijbels, and S. van der Velden et al. Distribution of macrophage polarization markers in human atherosclerosis Atherosclerosis 225 2012 461 468
25. M. Quiding-Jarbrink, S. Raghavan, and M. Sundquist Enhanced M1 macrophage polarization in human helicobacter pylori-associated atrophic gastritis and in vaccinated mice PLoS One 5 2010 e15018
26. P.J. Murray, and T.A. Wynn Protective and pathogenic functions of macrophage subsets Nat Rev Immunol 11 2011 723 737
27. F.A. Verreck, T. de Boer, and D.M. Langenberg et al. Phenotypic and functional profiling of human proinflammatory type-1 and anti-inflammatory type-2 macrophages in response to microbial antigens and IFN-gamma- and CD40L-mediated costimulation J Leukoc Biol 79 2006 285 293
28. M. Heusinkveld, and S.H. van der Burg Identification and manipulation of tumor associated macrophages in human cancers J Transl Med 9 2011 216
29. V. Bronte, and P. Zanovello Regulation of immune responses by L-arginine metabolism Nat Rev Immunol 5 2005 641 654
30. N.C. Chang, S.I. Hung, and K.Y. Hwa et al. A macrophage protein, Ym1, transiently expressed during inflammation is a novel mammalian lectin J Biol Chem 276 2001 17497 17506
31. M.G. Nair, I.J. Gallagher, and M.D. Taylor et al. Chitinase and Fizz family members are a generalized feature of nematode infection with selective upregulation of Ym1 and Fizz1 by antigen-presenting cells Infect Immun 73 2005 385 394
32. L.E. Smythies, K.B. Waites, and J.R. Lindsey et al. Helicobacter pylori-induced mucosal inflammation is Th1 mediated and exacerbated in IL-4, but not IFN-gamma, gene-deficient mice J Immunol 165 2000 1022 1029
33. P. Mombaerts, J. Iacomini, and R.S. Johnson et al. RAG-1-deficient mice have no mature B and T lymphocytes Cell 68 1992 869 877
34. B.J. Appelmelk, I. Simoons-Smit, and R. Negrini et al. Potential role of molecular mimicry between Helicobacter pylori lipopolysaccharide and host Lewis blood group antigens in autoimmunity Infect Immun 64 1996 2031 2040
35. S.P. Tu, M. Quante, and G. Bhagat et al. IFN-gamma inhibits gastric carcinogenesis by inducing epithelial cell autophagy and T-cell apoptosis Cancer Res 71 2011 4247 4259
36. W. Kang, S. Rathinavelu, and L.C. Samuelson et al. Interferon gamma induction of gastric mucous neck cell hypertrophy Lab Invest 85 2005 702 715
37. A. Mueller, D.S. Merrell, and J. Grimm et al. Profiling of microdissected gastric epithelial cells reveals a cell type-specific response to Helicobacter pylori infection Gastroenterology 127 2004 1446 1462
38. L.J. Syu, M. El-Zaatari, and K.A. Eaton et al. Transgenic expression of interferon-gamma in mouse stomach leads to inflammation, metaplasia, and dysplasia Am J Pathol 181 2012 2114 2125
39. R. Kozol, A. Domanowski, and R. Jaszewski et al. Neutrophil chemotaxis in gastric mucosa. A signal-to-response comparison Dig Dis Sci 36 1991 1277 1280
40. H.F. Ismail, J. Zhang, and R.G. Lynch et al. Role for complement in development of Helicobacter-induced gastritis in interleukin-10-deficient mice Infect Immun 71 2003 7140 7148
41. D.J. Evans Jr., D.G. Evans, and T. Takemura et al. Characterization of a Helicobacter pylori neutrophil-activating protein Infect Immun 63 1995 2213 2220
42. U.E. Mai, G.I. Perez-Perez, and L.M. Wahl et al. Soluble surface proteins from Helicobacter pylori activate monocytes/macrophages by lipopolysaccharide- independent mechanism J Clin Invest 87 1991 894 900
43. M.J. Blaser Hypotheses on the pathogenesis and natural history of Helicobacter pylori-induced inflammation Gastroenterology 102 1992 720 727
44. L.E. Wroblewski, R.M. Peek Jr., and K.T. Wilson Helicobacter pylori and gastric cancer: factors that modulate disease risk Clin Microbiol Rev 23 2010 713 739
45. D. Hashimoto, A. Chow, and C. Noizat et al. Tissue-resident macrophages self-maintain locally throughout adult life with minimal contribution from circulating monocytes Immunity 38 2013 792 804
46. H.U. Beuscher, C. Gunther, and M. Rollinghoff IL-1 beta is secreted by activated murine macrophages as biologically inactive precursor J Immunol 144 1990 2179 2183
47. I.L. Beales, and J. Calam Interleukin 1 beta and tumour necrosis factor alpha inhibit acid secretion in cultured rabbit parietal cells by multiple pathways Gut 42 1998 227 234
48. S. Tu, G. Bhagat, and G. Cui et al. Overexpression of interleukin-1beta induces gastric inflammation and cancer and mobilizes myeloid-derived suppressor cells in mice Cancer Cell 14 2008 408 419
49. R. Zaynagetdinov, T.P. Sherrill, and V.V. Polosukhin et al. A critical role for macrophages in promotion of urethane-induced lung carcinogenesis J Immunol 187 2011 5703 5711
50. H. Oshima, K. Hioki, and B.K. Popivanova et al. Prostaglandin E(2) signaling and bacterial infection recruit tumor-promoting macrophages to mouse gastric tumors Gastroenterology 140 2011 596 607.e7
51. H. Oshima, B.K. Popivanova, and K. Oguma et al. Activation of epidermal growth factor receptor signaling by the prostaglandin E(2) receptor EP4 pathway during gastric tumorigenesis Cancer Sci 102 2011 713 719
52. M. Fehlings, L. Drobbe, and V. Moos et al. Comparative analysis of the interaction of Helicobacter pylori with human dendritic cells, macrophages, and monocytes Infect Immun 80 2012 2724 2734
53. V.G. Weis, J.F. Sousa, and B.J. Lafleur et al. Heterogeneity in mouse spasmolytic polypeptide-expressing metaplasia lineages identifies markers of metaplastic progression Gut 62 2013 1270 1279
54. K.T. Nam, H.J. Lee, and H. Mok et al. Amphiregulin-deficient mice develop spasmolytic polypeptide expressing metaplasia and intestinal metaplasia Gastroenterology 136 2009 1288 1296
55. T.R. Jones, I.H. Kang, and D.B. Wheeler et al. CellProfiler Analyst: data exploration and analysis software for complex image-based screens BMC Bioinformatics 9 2008 482
56. C.M. Leys, S. Nomura, and B.J. LaFleur et al. Expression and prognostic significance of prothymosin-alpha and ERp57 in human gastric cancer Surgery 141 2007 41 50