ADAM10 is required for SCF-induced mast cell migration

Cellular Immunology

Volumn 290, Issue 1, 2014, Pages 80-88

  Faber, Travis W ^a   Pullen, Nicholas A ^a   Fernando, Josephine F A ^a   Kolawole, Elizabeth Motunrayo ^a   McLeod, Jamie J A ^a   Taruselli, Marcela ^a   Williams, Kathryn L ^a   Rivera, Kevin O ^a   Barnstein, Brian O ^a   Conrad, Daniel H ^a   Ryan, John J ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

ADAM 10; Cytokine; Mast cell; Migration; Stem cell factor

Indexed keywords

ADAM10 ENDOPEPTIDASE; INTERLEUKIN 10; STEM CELL FACTOR; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL HYPERPLASIA; CELL MIGRATION; CELL PROLIFERATION; CELL SURFACE; CELL SURVIVAL; CELLULAR DISTRIBUTION; CONTROLLED STUDY; GENE DELETION; IMMUNOCOMPETENT CELL; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATORY DISEASE; MAST CELL; MICROENVIRONMENT; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE; TISSUE DISTRIBUTION;

ADAM-10; CYTOKINE; MAST CELL; MIGRATION; STEM CELL FACTOR;

ADAM PROTEINS; AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; CELL MOVEMENT; CELL PROLIFERATION; CELLS, CULTURED; HYPERPLASIA; INTERLEUKIN-10; MAST CELLS; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PERITONEUM; RNA INTERFERENCE; RNA, SMALL INTERFERING; STEM CELL FACTOR; T-LYMPHOCYTES; TRANSFORMING GROWTH FACTOR BETA;

EID: 84902504605     PISSN: 00088749     EISSN: 10902163     Source Type: Journal    
DOI: 10.1016/j.cellimm.2014.05.005     Document Type: Article

References (66)

1. Finkelman F.D. Anaphylaxis: lessons from mouse models. J. Allergy Clin. Immunol. 2007, 120:506-515. quiz 516-7.
2. Kalesnikoff J., Galli S.J. New developments in mast cell biology. Nat. Immunol. 2008, 9:1215-1223.
3. Metcalfe D.D., Peavy R.D., Gilfillan A.M. Mechanisms of mast cell signaling in anaphylaxis. J. Allergy Clin. Immunol. 2009, 124:639-646. quiz 647-8.
4. Halova I., Draberova L., Draber P. Mast cell chemotaxis - chemoattractants and signaling pathways. Front. Immunol. 2012, 3:119.
5. Galli S.J., Tsai M., Wershil B.K., Tam S.Y., Costa J.J. Regulation of mouse and human mast cell development, survival and function by stem cell factor, the ligand for the c-kit receptor. Int. Arch. Allergy Immunol. 1995, 107:51-53.
6. Kitamura Y., Oboki K., Ito A. Molecular mechanisms of mast cell development. Immunol. Allergy Clin. N. Am. 2006, 26:387-405. v.
7. Metcalfe D.D. Mast cells and mastocytosis. Blood 2008, 112:946-956.
8. Huang B., Lei Z., Zhang G.M., Li D., Song C., Li B., Liu Y., Yuan Y., Unkeless J., Xiong H., Feng Z.H. SCF-mediated mast cell infiltration and activation exacerbate the inflammation and immunosuppression in tumor microenvironment. Blood 2008, 112:1269-1279.
9. Caughey G.H. Mast cell proteases as protective and inflammatory mediators. Adv. Exp. Med. Biol. 2011, 716:212-234.
10. Shin K., Nigrovic P.A., Crish J., Boilard E., McNeil H.P., Larabee K.S., Adachi R., Gurish M.F., Gobezie R., Stevens R.L., Lee D.M. Mast cells contribute to autoimmune inflammatory arthritis via their tryptase/heparin complexes. J. Immunol. 2009, 182:647-656.
11. Piliponsky A.M., Chen C.C., Rios E.J., Treuting P.M., Lahiri A., Abrink M., Pejler G., Tsai M., Galli S.J. The chymase mouse mast cell protease 4 degrades TNF, limits inflammation, and promotes survival in a model of sepsis. Am. J. Pathol. 2012, 181:875-886.
12. Edwards D.R., Handsley M.M., Pennington C.J. The ADAM metalloproteinases. Mol. Aspects Med. 2008, 29:258-289.
13. Pruessmeyer J., Ludwig A. The good, the bad and the ugly substrates for ADAM10 and ADAM17 in brain pathology, inflammation and cancer. Semin. Cell Dev. Biol. 2009, 20:164-174.
14. Reiss K., Saftig P. The "a disintegrin and metalloprotease" (ADAM) family of sheddases: physiological and cellular functions. Semin. Cell Dev. Biol. 2009, 20:126-137.
15. Gibb D.R., Saleem S.J., Chaimowitz N.S., Mathews J., Conrad D.H. The emergence of ADAM10 as a regulator of lymphocyte development and autoimmunity. Mol. Immunol. 2011, 48:1319-1327.
16. Armanious H., Gelebart P., Anand M., Belch A., Lai R. Constitutive activation of metalloproteinase ADAM10 in mantle cell lymphoma promotes cell growth and activates the TNFalpha/NFkappaB pathway. Blood 2011, 117:6237-6246.
17. Chaimowitz N.S., Martin R.K., Cichy J., Gibb D.R., Patil P., Kang D.J., Farnsworth J., Butcher E.C., McCright B., Conrad D.H. A disintegrin and metalloproteinase 10 regulates antibody production and maintenance of lymphoid architecture. J. Immunol. 2011, 187:5114-5122.
18. D.H. Conrad, D.R. Gibb, and J. Sturgill, Regulation of the IgE response. F1000 Biol Rep 2 (2011).
19. Gibb D.R., El Shikh M., Kang D.J., Rowe W.J., El Sayed R., Cichy J., Yagita H., Tew J.G., Dempsey P.J., Crawford H.C., Conrad D.H. ADAM10 is essential for Notch2-dependent marginal zone B cell development and CD23 cleavage in vivo. J. Exp. Med. 2011, 207:623-635.
20. Gibb D.R., Saleem S.J., Kang D.J., Subler M.A., Conrad D.H. ADAM10 overexpression shifts lympho- and myelopoiesis by dysregulating site 2/site 3 cleavage products of Notch. J. Immunol. 2011, 186:4244-4252.
21. Hartmann D., de Strooper B., Serneels L., Craessaerts K., Herreman A., Annaert W., Umans L., Lubke T., Lena A., Illert K., von Figura, Saftig P. The disintegrin/metalloprotease ADAM 10 is essential for Notch signalling but not for alpha-secretase activity in fibroblasts. Hum. Mol. Genet. 2002, 11:2615-2624.
22. Mathews J.A., Ford J., Norton S., Kang D., Dellinger A., Gibb D.R., Ford A.Q., Massay H., Kepley C.L., Scherle P., Keegan A.D., Conrad D.H. A potential new target for asthma therapy: a disintegrin and metalloprotease 10 (ADAM10) involvement in murine experimental asthma. Allergy 2011, 66:1193-1200.
23. Mathews J.A., Gibb D.R., Chen B.H., Scherle P., Conrad D.H. CD23 Sheddase A disintegrin and metalloproteinase 10 (ADAM10) is also required for CD23 sorting into B cell-derived exosomes. J. Biol. Chem. 2010, 285:37531-37541.
24. Tian L., Wu X., Chi C., Han M., Xu T., Zhuang Y. ADAM10 is essential for proteolytic activation of Notch during thymocyte development. Int. Immunol. 2008, 20:1181-1187.
25. van Tetering G., van Diest P., Verlaan I., van der Wall E., Kopan R., Vooijs M. Metalloprotease ADAM10 is required for Notch1 site 2 cleavage. J. Biol. Chem. 2009, 284:31018-31027.
26. Weskamp G., Ford J.W., Sturgill J., Martin S., Docherty A.J., Swendeman S., Broadway N., Hartmann D., Saftig P., Umland S., Sehara-Fujisawa A., Black R.A., Ludwig A., Becherer J.D., Conrad D.H., Blobel C.P. ADAM10 is a principal 'sheddase' of the low-affinity immunoglobulin E receptor CD23. Nat. Immunol. 2006, 7:1293-1298.
27. Yoda M., Kimura T., Tohmonda T., Uchikawa S., Koba T., Takito J., Morioka H., Matsumoto M., Link D.C., Chiba K., Okada Y., Toyama Y., Horiuchi K. Dual functions of cell-autonomous and non-cell-autonomous ADAM10 activity in granulopoiesis. Blood 2011, 118:6939-6942.
28. Cruz A.C., Frank B.T., Edwards S.T., Dazin P.F., Peschon J.J., Fang K.C. Tumor necrosis factor-alpha-converting enzyme controls surface expression of c-Kit and survival of embryonic stem cell-derived mast cells. J. Biol. Chem. 2004, 279:5612-5620.
29. Edwards S.T., Cruz A.C., Donnelly S., Dazin P.F., Schulman E.S., Jones K.D., Wolters P.J., Hoopes C., Dolganov G.M., Fang K.C. C-Kit immunophenotyping and metalloproteinase expression profiles of mast cells in interstitial lung diseases. J. Pathol. 2005, 206:279-290.
30. Kawaguchi N., Horiuchi K., Becherer J.D., Toyama Y., Besmer P., Blobel C.P. Different ADAMs have distinct influences on Kit ligand processing: phorbol-ester-stimulated ectodomain shedding of Kitl1 by ADAM17 is reduced by ADAM19. J. Cell Sci. 2007, 120:943-952.
31. Fernando J., Faber T.W., Pullen N.A., Falanga Y.T., Kolawole E.M., Oskeritzian C.A., Barnstein B.O., Bandara G., Li G., Schwartz L.B., Spiegel S., Straus D.B., Conrad D.H., Bunting K.D., Ryan J.J. Genotype-dependent effects of TGF-beta1 on mast cell function: targeting the STAT5 pathway. J. Immunol. 2013, 191:4505-4513.
32. Ghildyal N., McNeil H.P., Stechschulte S., Austen K.F., Silberstein D., Gurish M.F., Somerville L.L., Stevens R.L. IL-10 induces transcription of the gene for mouse mast cell protease-1, a serine protease preferentially expressed in mucosal mast cells of Trichinella spiralis-infected mice. J. Immunol. 1992, 149:2123-2129.
33. Miller H.R., Wright S.H., Knight P.A., Thornton E.M. A novel function for transforming growth factor-beta1: upregulation of the expression and the IgE-independent extracellular release of a mucosal mast cell granule-specific beta-chymase, mouse mast cell protease-1. Blood 1999, 93:3473-3486.
34. Gruber B.L., Marchese M.J., Kew R.R. Transforming growth factor-beta 1 mediates mast cell chemotaxis. J. Immunol. 1994, 152:5860-5867.
35. Olsson N., Piek E., Sundstrom M., ten Dijke P., Nilsson G. Transforming growth factor-beta-mediated mast cell migration depends on mitogen-activated protein kinase activity. Cell. Signal. 2001, 13:483-490.
36. Olsson N., Piek E., ten Dijke P., Nilsson G. Human mast cell migration in response to members of the transforming growth factor-beta family. J. Leukoc. Biol. 2000, 67:350-356.
37. Macey M.R., Sturgill J.L., Morales J.K., Falanga Y.T., Morales J., Norton S.K., Yerram N., Shim H., Fernando J., Gifillan A.M., Gomez G., Schwartz L., Oskeritzian C., Spiegel S., Conrad D., Ryan J.J. IL-4 and TGF-beta 1 counterbalance one another while regulating mast cell homeostasis. J. Immunol. 2010, 184:4688-4695.
38. Pietrzak A., Misiak-Tloczek A., Brzezinska-Blaszczyk E. Interleukin (IL)-10 inhibits RANTES-, tumour necrosis factor (TNF)- and nerve growth factor (NGF)-induced mast cell migratory response but is not a mast cell chemoattractant. Immunol. Lett. 2009, 123:46-51.
39. Murphy G. The ADAMs: signalling scissors in the tumour microenvironment. Nat. Rev. Cancer 2008, 8:929-941.
40. Lantz C.S., Boesiger J., Song C.H., Mach N., Kobayashi T., Mulligan R.C., Nawa Y., Dranoff G., Galli S.J. Role for interleukin-3 in mast-cell and basophil development and in immunity to parasites. Nature 1998, 392:90-93.
41. Nakano K., Siar C.H., Tsujigiwa H., Nagatsuka H., Nagai N., Kawakami T. Notch signaling in benign and malignant ameloblastic neoplasms. Eur. J. Med. Res. 2008, 13:476-480.
42. Nakano N., Nishiyama C., Yagita H., Koyanagi A., Akiba H., Chiba S., Ogawa H., Okumura K. Notch signaling confers antigen-presenting cell functions on mast cells. J. Allergy Clin. Immunol. 2009, 123:74-81. e1.
43. Nakano N., Nishiyama C., Yagita H., Koyanagi A., Ogawa H., Okumura K. Notch1-mediated signaling induces MHC class II expression through activation of class II transactivator promoter III in mast cells. J. Biol. Chem. 2011, 286:12042-12048.
44. Sakata-Yanagimoto M., Sakai T., Miyake Y., Saito T.I., Maruyama H., Morishita Y., Nakagami-Yamaguchi E., Kumano K., Yagita H., Fukayama M., Ogawa S., Kurokawa M., Yasutomo K., Chiba S. Notch2 signaling is required for proper mast cell distribution and mucosal immunity in the intestine. Blood 2011, 117:128-134.
45. Nagano O., Murakami D., Hartmann D., De Strooper B., Saftig P., Iwatsubo T., Nakajima M., Shinohara M., Saya H. Cell-matrix interaction via CD44 is independently regulated by different metalloproteinases activated in response to extracellular Ca(2+) influx and PKC activation. J. Cell Biol. 2004, 165:893-902.
46. Takano H., Nakazawa S., Shirata N., Tamba S., Furuta K., Tsuchiya S., Morimoto K., Itano N., Irie A., Ichikawa A., Kimata K., Nakayama K., Sugimoto Y., Tanaka S. Involvement of CD44 in mast cell proliferation during terminal differentiation. Lab. Invest. 2009, 89:446-455.
47. Girodet P.O., Ozier A., Trian T., Begueret H., Ousova O., Vernejoux J.M., Chanez P., Marthan R., Berger P., Tunon de Lara J.M. Mast cell adhesion to bronchial smooth muscle in asthma specifically depends on CD51 and CD44 variant 6. Allergy 2010, 65:1004-1012.
48. Bissonnette E.Y., Enciso J.A., Befus A.D. TGF-beta1 inhibits the release of histamine and tumor necrosis factor-alpha from mast cells through an autocrine pathway. Am. J. Respir. Cell Mol. Biol. 1997, 16:275-282.
49. Broide D.H., Wasserman S.I., Alvaro-Gracia J., Zvaifler N.J., Firestein G.S. Transforming growth factor-beta 1 selectively inhibits IL-3-dependent mast cell proliferation without affecting mast cell function or differentiation. J. Immunol. 1989, 143:1591-1597.
50. Gomez G., Ramirez C.D., Rivera J., Patel M., Norozian F., Wright H.V., Kashyap M.V., Barnstein B.O., Fischer-Stenger K., Schwartz L.B., Kepley C.L., Ryan J.J. TGF-beta 1 inhibits mast cell Fc epsilon RI expression. J. Immunol. 2005, 174:5987-5993.
51. Kashyap M., Bailey D.P., Gomez G., Rivera J., Huff T.F., Ryan J.J. TGF-beta1 inhibits late-stage mast cell maturation. Exp. Hematol. 2005, 33:1281-1291.
52. Meade R., Askenase P.W., Geba G.P., Neddermann K., Jacoby R.O., Pasternak R.D. Transforming growth factor-beta 1 inhibits murine immediate and delayed type hypersensitivity. J. Immunol. 1992, 149:521-528.
53. Norozian F., Kashyap M., Ramirez C.D., Patel N., Kepley C.L., Barnstein B.O., Ryan J.J. TGFbeta1 induces mast cell apoptosis. Exp. Hematol. 2006, 34:579-587.
54. Toyota N., Hashimoto Y., Matsuo S., Iizuka H. Transforming growth factor beta 1 inhibits IL-3- and IL-4-dependent mouse connective tissue-type mast cell proliferation. Arch. Dermatol. Res. 1995, 287:198-201.
55. Zhao W., Gomez G., Yu S.H., Ryan J.J., Schwartz L.B. TGF-beta1 attenuates mediator release and de novo Kit expression by human skin mast cells through a Smad-dependent pathway. J. Immunol. 2008, 181:7263-7272.
56. Lin T.J., Befus A.D. Differential regulation of mast cell function by IL-10 and stem cell factor. J. Immunol. 1997, 159:4015-4023.
57. Marshall J.S., Leal-Berumen I., Nielsen L., Glibetic M., Jordana M. Interleukin (IL)-10 inhibits long-term IL-6 production but not preformed mediator release from rat peritoneal mast cells. J. Clin. Invest. 1996, 97:1122-1128.
58. Mirmonsef P., Shelburne C.P., Fitzhugh Yeatman C., Chong H.J., Ryan J.J. Inhibition of Kit expression by IL-4 and IL-10 in murine mast cells: role of STAT6 and phosphatidylinositol 3'-kinase. J. Immunol. 1999, 163:2530-2539.
59. Royer B., Varadaradjalou S., Saas P., Gabiot A.C., Kantelip B., Feger F., Guillosson J.J., Kantelip J.P., Arock M. Autocrine regulation of cord blood-derived human mast cell activation by IL-10. J. Allergy Clin. Immunol. 2001, 108:80-86.
60. Royer B., Varadaradjalou S., Saas P., Guillosson J.J., Kantelip J.P., Arock M. Inhibition of IgE-induced activation of human mast cells by IL-10. Clin. Exp. Allergy 2001, 31:694-704.
61. Shelburne C.P., Ryan J.J. The role of Th2 cytokines in mast cell homeostasis. Immunol. Rev. 2001, 179:82-93.
62. Speiran K., Bailey D.P., Fernando J., Macey M., Barnstein B., Kolawole M., Curley D., Watowich S.S., Murray P.J., Oskeritzian C., Ryan J.J. Endogenous suppression of mast cell development and survival by IL-4 and IL-10. J. Leukoc. Biol. 2009, 85:826-836.
63. Yeatman C.F., Jacobs-Helber S.M., Mirmonsef P., Gillespie S.R., Bouton L.A., Collins H.A., Sawyer S.T., Shelburne C.P., Ryan J.J. Combined stimulation with the T helper cell type 2 cytokines interleukin (IL)-4 and IL-10 induces mouse mast cell apoptosis. J. Exp. Med. 2000, 192:1093-1103.
64. Funaba M., Ikeda T., Murakami M., Ogawa K., Abe M. Up-regulation of mouse mast cell protease-6 gene by transforming growth factor-beta and activin in mast cell progenitors. Cell. Signal. 2005, 17:121-128.
65. Funaba M., Ikeda T., Murakami M., Ogawa K., Tsuchida K., Sugino H., Abe M. Transcriptional activation of mouse mast cell protease-7 by activin and transforming growth factor-beta is inhibited by microphthalmia-associated transcription factor. J. Biol. Chem. 2003, 278:52032-52041.
66. Gillespie S.R., DeMartino R.R., Zhu J., Chong H.J., Ramirez C., Shelburne C.P., Bouton L.A., Bailey D.P., Gharse A., Mirmonsef P., Odom S., Gomez G., Rivera J., Fischer-Stenger K., Ryan J.J. IL-10 inhibits Fc epsilon RI expression in mouse mast cells. J. Immunol. 2004, 172:3181-3188.