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Abstract

A disintegrin and metalloproteinases (ADAMs) are a family of cell surface proteases that regulate diverse cellular functions, including cell adhesion, migration, cellular signaling, and proteolysis. Proteolytically active ADAMs are responsible for ectodomain shedding of membrane-associated proteins. ADAMs rapidly modulate key cell signaling pathways in response to changes in the extracellular environment (e.g., inflammation) and play a central role in coordinating intercellular communication within the local microenvironment. ADAM10 and ADAM17 are the most studied members of the ADAM family in the gastrointestinal tract. ADAMs regulate many cellular processes associated with intestinal development, cell fate specification, and the maintenance of intestinal stem cell/progenitor populations. Several signaling pathway molecules that undergo ectodomain shedding by ADAMs [e.g., ligands and receptors from epidermal growth factor receptor (EGFR)/ErbB and tumor necrosis factor α (TNFα) receptor (TNFR) families] help drive and control intestinal inflammation and injury/repair responses. Dysregulation of these processes through aberrant ADAM expression or sustained ADAM activity is linked to chronic inflammation, inflammation-associated cancer, and tumorigenesis.

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2016-02-10
2024-04-19
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Literature Cited

  1. Weber S, Saftig P. 1.  2012. Ectodomain shedding and ADAMs in development. Development 139:3693–709 [Google Scholar]
  2. Edwards DR, Handsley MM, Pennington CJ. 2.  2008. The ADAM metalloproteinases. Mol. Asp. Med. 29:258–89 [Google Scholar]
  3. Endres K, Fahrenholz F. 3.  2012. Regulation of α-secretase ADAM10 expression and activity. Exp. Brain Res. 217:343–52 [Google Scholar]
  4. Reiss K, Saftig P. 4.  2009. The “A disintegrin and metalloprotease” (ADAM) family of sheddases: physiological and cellular functions. Semin. Cell Dev. Biol. 20:126–37 [Google Scholar]
  5. Scheller J, Chalaris A, Garbers C, Rose-John S. 5.  2011. ADAM17: a molecular switch to control inflammation and tissue regeneration. Trends Immunol. 32:380–87 [Google Scholar]
  6. Khokha R, Murthy A, Weiss A. 6.  2013. Metalloproteinases and their natural inhibitors in inflammation and immunity. Nat. Rev. Immunol. 13:649–65 [Google Scholar]
  7. Cho C. 7.  2012. Testicular and epididymal ADAMs: expression and function during fertilization. Nat. Rev. Urol. 9:550–60 [Google Scholar]
  8. Adrain C, Zettl M, Christova Y, Taylor N, Freeman M. 8.  2012. Tumor necrosis factor signaling requires iRhom2 to promote trafficking and activation of TACE. Science 335:225–28 [Google Scholar]
  9. McIlwain DR, Lang PA, Maretzky T, Hamada K, Ohishi K. 9.  et al. 2012. iRhom2 regulation of TACE controls TNF-mediated protection against Listeria and responses to LPS. Science 335:229–32 [Google Scholar]
  10. Christova Y, Adrain C, Bambrough P, Ibrahim A, Freeman M. 10.  2013. Mammalian iRhoms have distinct physiological functions including an essential role in TACE regulation. EMBO Rep. 14:884–90 [Google Scholar]
  11. Maretzky T, McIlwain DR, Issuree PD, Li X, Malapeira J. 11.  et al. 2013. iRhom2 controls the substrate selectivity of stimulated ADAM17-dependent ectodomain shedding. PNAS 110:11433–38 [Google Scholar]
  12. Li X, Maretzky T, Weskamp G, Monette S, Qing X. 12.  et al. 2015. iRhoms 1 and 2 are essential upstream regulators of ADAM17-dependent EGFR signaling. PNAS 112:6080–85 [Google Scholar]
  13. Dornier E, Coumailleau F, Ottavi JF, Moretti J, Boucheix C. 13.  et al. 2012. TspanC8 tetraspanins regulate ADAM10/Kuzbanian trafficking and promote Notch activation in flies and mammals. J. Cell Biol. 199:481–96 [Google Scholar]
  14. Haining EJ, Yang J, Bailey RL, Khan K, Collier R. 14.  et al. 2012. The TspanC8 subgroup of tetraspanins interacts with A disintegrin and metalloprotease 10 (ADAM10) and regulates its maturation and cell surface expression. J. Biol. Chem. 287:39753–65 [Google Scholar]
  15. Prox J, Willenbrock M, Weber S, Lehmann T, Schmidt-Arras D. 15.  et al. 2012. Tetraspanin15 regulates cellular trafficking and activity of the ectodomain sheddase ADAM10. Cell Mol. Life Sci. 69:2919–32 [Google Scholar]
  16. Garbers C, Aparicio-Siegmund S, Rose-John S. 16.  2015. The IL-6/gp130/STAT3 signaling axis: recent advances towards specific inhibition. Curr. Opin Immunol. 34C:75–82 [Google Scholar]
  17. Janes PW, Saha N, Barton WA, Kolev MV, Wimmer-Kleikamp SH. 17.  et al. 2005. Adam meets Eph: An ADAM substrate recognition module acts as a molecular switch for ephrin cleavage in trans. Cell 123:291–304 [Google Scholar]
  18. Janes PW, Wimmer-Kleikamp SH, Frangakis AS, Treble K, Griesshaber B. 18.  et al. 2009. Cytoplasmic relaxation of active Eph controls ephrin shedding by ADAM10. PLOS Biol. 7:e1000215 [Google Scholar]
  19. Stoeck A, Keller S, Riedle S, Sanderson MP, Runz S. 19.  et al. 2006. A role for exosomes in the constitutive and stimulus-induced ectodomain cleavage of L1 and CD44. Biochem. J. 393:609–18 [Google Scholar]
  20. Shimoda M, Principe S, Jackson HW, Luga V, Fang H. 20.  et al. 2014. Loss of the Timp gene family is sufficient for the acquisition of the CAF-like cell state. Nat. Cell Biol. 16:889–901 [Google Scholar]
  21. Folgosa L, Zellner HB, El Shikh ME, Conrad DH. 21.  2013. Disturbed follicular architecture in B cell A disintegrin and metalloproteinase (ADAM)10 knockouts is mediated by compensatory increases in ADAM17 and TNF-α shedding. J. Immunol. 191:5951–58 [Google Scholar]
  22. Willems SH, Tape CJ, Stanley PL, Taylor NA, Mills IG. 22.  et al. 2010. Thiol isomerases negatively regulate the cellular shedding of ADAM17. Biochem. J. 428:439–50 [Google Scholar]
  23. Brew K, Nagase H. 23.  2010. The tissue inhibitors of metalloproteinases (TIMPs): an ancient family with structural and functional diversity. Biochim. Biophys. Acta 1803:55–71 [Google Scholar]
  24. Xu P, Derynck R. 24.  2010. Direct activation of TACE-mediated ectodomain shedding by p38 MAP kinase regulates EGF receptor–dependent cell proliferation. Mol. Cell 37:551–66 [Google Scholar]
  25. Xu P, Liu J, Sakaki-Yumoto M, Derynck R. 25.  2012. TACE activation by MAPK-mediated regulation of cell surface dimerization and TIMP3 association. Sci. Signal 5:ra34 [Google Scholar]
  26. Moss ML, Bomar M, Liu Q, Sage H, Dempsey P. 26.  et al. 2007. The ADAM10 prodomain is a specific inhibitor of ADAM10 proteolytic activity and inhibits cellular shedding events. J. Biol. Chem. 282:35712–21 [Google Scholar]
  27. Fridman JS, Caulder E, Hansbury M, Liu X, Yang G. 27.  et al. 2007. Selective inhibition of ADAM metalloproteases as a novel approach for modulating ErbB pathways in cancer. Clin. Cancer Res. 13:1892–902 [Google Scholar]
  28. Zhou BB, Peyton M, He B, Liu C, Girard L. 28.  et al. 2006. Targeting ADAM-mediated ligand cleavage to inhibit HER3 and EGFR pathways in non-small cell lung cancer. Cancer Cell 10:39–50 [Google Scholar]
  29. Murumkar PR, DasGupta S, Chandani SR, Giridhar R, Yadav MR. 29.  2010. Novel TACE inhibitors in drug discovery: a review of patented compounds. Expert Opin. Ther. Pat. 20:31–57 [Google Scholar]
  30. Tape CJ, Willems SH, Dombernowsky SL, Stanley PL, Fogarasi M. 30.  et al. 2011. Cross-domain inhibition of TACE ectodomain. PNAS 108:5578–83 [Google Scholar]
  31. Atapattu L, Saha N, Llerena C, Vail ME, Scott AM. 31.  et al. 2012. Antibodies binding the ADAM10 substrate recognition domain inhibit Eph function. J. Cell Sci. 125:6084–93 [Google Scholar]
  32. Tian H, Biehs B, Chiu C, Siebel CW, Wu Y. 32.  et al. 2015. Opposing activities of Notch and Wnt signaling regulate intestinal stem cells and gut homeostasis. Cell Rep. 11:33–42 [Google Scholar]
  33. Tran IT, Sandy AR, Carulli AJ, Ebens C, Chung J. 33.  et al. 2013. Blockade of individual Notch ligands and receptors controls graft-versus-host disease. J. Clin. Investig. 123:1590–604 [Google Scholar]
  34. VanDussen KL, Carulli AJ, Keeley TM, Patel SR, Puthoff BJ. 34.  et al. 2012. Notch signaling modulates proliferation and differentiation of intestinal crypt base columnar stem cells. Development 139:488–97 [Google Scholar]
  35. Huntzicker EG, Hotzel K, Choy L, Che L, Ross J. 35.  et al. 2015. Differential effects of targeting Notch receptors in a mouse model of liver cancer. Hepatology 61:942–52 [Google Scholar]
  36. Spence JR, Lauf R, Shroyer NF. 36.  2011. Vertebrate intestinal endoderm development. Dev. Dyn. 240:501–20 [Google Scholar]
  37. Zorn AM, Wells JM. 37.  2009. Vertebrate endoderm development and organ formation. Annu. Rev. Cell Dev. Biol. 25:221–51 [Google Scholar]
  38. Barker N. 38.  2014. Adult intestinal stem cells: critical drivers of epithelial homeostasis and regeneration. Nat. Rev. Mol. Cell Biol. 15:19–33 [Google Scholar]
  39. Clevers H. 39.  2013. The intestinal crypt, a prototype stem cell compartment. Cell 154:274–84 [Google Scholar]
  40. Clevers HC, Bevins CL. 40.  2013. Paneth cells: maestros of the small intestinal crypts. Annu. Rev. Physiol. 75:289–311 [Google Scholar]
  41. Sancho R, Cremona CA, Behrens A. 41.  2015. Stem cell and progenitor fate in the mammalian intestine: Notch and lateral inhibition in homeostasis and disease. EMBO Rep. 16:571–81 [Google Scholar]
  42. Fre S, Huyghe M, Mourikis P, Robine S, Louvard D, Artavanis-Tsakonas S. 42.  2005. Notch signals control the fate of immature progenitor cells in the intestine. Nature 435:964–68 [Google Scholar]
  43. Vooijs M, Ong CT, Hadland B, Huppert S, Liu Z. 43.  et al. 2007. Mapping the consequence of Notch1 proteolysis in vivo with NIP-CRE. Development 134:535–44 [Google Scholar]
  44. Kopinke D, Brailsford M, Shea JE, Leavitt R, Scaife CL, Murtaugh LC. 44.  2011. Lineage tracing reveals the dynamic contribution of Hes1+ cells to the developing and adult pancreas. Development 138:431–41 [Google Scholar]
  45. Carulli AJ, Keeley TM, Demitrack ES, Chung J, Maillard I, Samuelson LC. 45.  2015. Notch receptor regulation of intestinal stem cell homeostasis and crypt regeneration. Dev. Biol. 402:98–108 [Google Scholar]
  46. Riccio O, van Gijn ME, Bezdek AC, Pellegrinet L, van Es JH. 46.  et al. 2008. Loss of intestinal crypt progenitor cells owing to inactivation of both Notch1 and Notch2 is accompanied by derepression of CDK inhibitors p27Kip1 and p57Kip2. EMBO Rep. 9:377–83 [Google Scholar]
  47. Fre S, Pallavi SK, Huyghe M, Lae M, Janssen KP. 47.  et al. 2009. Notch and Wnt signals cooperatively control cell proliferation and tumorigenesis in the intestine. PNAS 106:6309–14 [Google Scholar]
  48. Pellegrinet L, Rodilla V, Liu Z, Chen S, Koch U. 48.  et al. 2011. Dll1- and Dll4-mediated Notch signaling are required for homeostasis of intestinal stem cells. Gastroenterology 140:1230–40.e7 [Google Scholar]
  49. Kim TH, Li F, Ferreiro-Neira I, Ho LL, Luyten A. 49.  et al. 2014. Broadly permissive intestinal chromatin underlies lateral inhibition and cell plasticity. Nature 506:511–15 [Google Scholar]
  50. Tsai YH, VanDussen KL, Sawey ET, Wade AW, Kasper C. 50.  et al. 2014. ADAM10 regulates Notch function in intestinal stem cells of mice. Gastroenterology 147:822–34.e13 [Google Scholar]
  51. Hartmann D, de Strooper B, Serneels L, Craessaerts K, Herreman A. 51.  et al. 2002. The disintegrin/metalloprotease ADAM 10 is essential for Notch signalling but not for α-secretase activity in fibroblasts. Hum. Mol. Genet. 11:2615–24 [Google Scholar]
  52. Groot AJ, Habets R, Yahyanejad S, Hodin CM, Reiss K. 52.  et al. 2014. Regulated proteolysis of NOTCH2 and NOTCH3 receptors by ADAM10 and presenilins. Mol. Cell. Biol. 34:2822–32 [Google Scholar]
  53. van Tetering G, van Diest P, Verlaan I, van der Wall E, Kopan R, Vooijs M. 53.  2009. Metalloprotease ADAM10 is required for Notch1 site 2 cleavage. J. Biol. Chem. 284:31018–27 [Google Scholar]
  54. Weber S, Niessen MT, Prox J, Lullmann-Rauch R, Schmitz A. 54.  et al. 2011. The disintegrin/metalloproteinase Adam10 is essential for epidermal integrity and Notch-mediated signaling. Development 138:495–505 [Google Scholar]
  55. Fre S, Hannezo E, Sale S, Huyghe M, Lafkas D. 55.  et al. 2011. Notch lineages and activity in intestinal stem cells determined by a new set of knock-in mice. PLOS ONE 6:e25785 [Google Scholar]
  56. Buczacki SJ, Zecchini HI, Nicholson AM, Russell R, Vermeulen L. 56.  et al. 2013. Intestinal label-retaining cells are secretory precursors expressing Lgr5. Nature 495:65–69 [Google Scholar]
  57. Montgomery RK, Carlone DL, Richmond CA, Farilla L, Kranendonk ME. 57.  et al. 2011. Mouse telomerase reverse transcriptase (mTert) expression marks slowly cycling intestinal stem cells. PNAS 108:179–84 [Google Scholar]
  58. Tian H, Biehs B, Warming S, Leong KG, Rangell L. 58.  et al. 2011. A reserve stem cell population in small intestine renders Lgr5-positive cells dispensable. Nature 478:255–59 [Google Scholar]
  59. van Es JH, Sato T, van de Wetering M, Lyubimova A, Nee AN. 59.  et al. 2012. Dll1+ secretory progenitor cells revert to stem cells upon crypt damage. Nat. Cell Biol. 14:1099–104 [Google Scholar]
  60. Sangiorgi E, Capecchi MR. 60.  2008. Bmi1 is expressed in vivo in intestinal stem cells. Nat. Genet. 40:915–20 [Google Scholar]
  61. Maretzky T, Reiss K, Ludwig A, Buchholz J, Scholz F. 61.  et al. 2005. ADAM10 mediates E-cadherin shedding and regulates epithelial cell-cell adhesion, migration, and β-catenin translocation. PNAS 102:9182–87 [Google Scholar]
  62. Maretzky T, Scholz F, Koten B, Proksch E, Saftig P, Reiss K. 62.  2008. ADAM10-mediated E-cadherin release is regulated by proinflammatory cytokines and modulates keratinocyte cohesion in eczematous dermatitis. J. Investig. Dermatol. 128:1737–46 [Google Scholar]
  63. Solanas G, Cortina C, Sevillano M, Batlle E. 63.  2011. Cleavage of E-cadherin by ADAM10 mediates epithelial cell sorting downstream of EphB signalling. Nat. Cell Biol. 13:1100–7 [Google Scholar]
  64. Merchant NB, Voskresensky I, Rogers CM, Lafleur B, Dempsey PJ. 64.  et al. 2008. TACE/ADAM-17: a component of the epidermal growth factor receptor axis and a promising therapeutic target in colorectal cancer. Clin. Cancer Res. 14:1182–91 [Google Scholar]
  65. Moss ML, Jin SL, Milla ME, Bickett DM, Burkhart W. 65.  et al. 1997. Cloning of a disintegrin metalloproteinase that processes precursor tumour-necrosis factor-α. Nature 385:733–36 [Google Scholar]
  66. Peschon JJ, Torrance DS, Stocking KL, Glaccum MB, Otten C. 66.  et al. 1998. TNF receptor–deficient mice reveal divergent roles for p55 and p75 in several models of inflammation. J. Immunol. 160:943–52 [Google Scholar]
  67. Peschon JJ, Slack JL, Reddy P, Stocking KL, Sunnarborg SW. 67.  et al. 1998. An essential role for ectodomain shedding in mammalian development. Science 282:1281–84 [Google Scholar]
  68. Winsauer C, Kruglov AA, Chashchina AA, Drutskaya MS, Nedospasov SA. 68.  2014. Cellular sources of pathogenic and protective TNF and experimental strategies based on utilization of TNF humanized mice. Cytokine Growth Factor Rev. 25:115–23 [Google Scholar]
  69. Sibilia M, Wagner EF. 69.  1995. Strain-dependent epithelial defects in mice lacking the EGF receptor. Science 269:234–38 [Google Scholar]
  70. Threadgill DW, Dlugosz AA, Hansen LA, Tennenbaum T, Lichti U. 70.  et al. 1995. Targeted disruption of mouse EGF receptor: effect of genetic background on mutant phenotype. Science 269:230–34 [Google Scholar]
  71. Miettinen PJ, Berger JE, Meneses J, Phung Y, Pedersen RA. 71.  et al. 1995. Epithelial immaturity and multiorgan failure in mice lacking epidermal growth factor receptor. Nature 376:337–41 [Google Scholar]
  72. Blobel CP, Carpenter G, Freeman M. 72.  2009. The role of protease activity in ErbB biology. Exp. Cell Res. 315:671–82 [Google Scholar]
  73. Sunnarborg SW, Hinkle CL, Stevenson M, Russell WE, Raska CS. 73.  et al. 2002. Tumor necrosis factor-α converting enzyme (TACE) regulates epidermal growth factor receptor ligand availability. J. Biol. Chem. 277:12838–45 [Google Scholar]
  74. Strunk KE, Amann V, Threadgill DW. 74.  2004. Phenotypic variation resulting from a deficiency of epidermal growth factor receptor in mice is caused by extensive genetic heterogeneity that can be genetically and molecularly partitioned. Genetics 167:1821–32 [Google Scholar]
  75. Gelling RW, Yan W, Al-Noori S, Pardini A, Morton GJ. 75.  et al. 2008. Deficiency of TNFα converting enzyme (TACE/ADAM17) causes a lean, hypermetabolic phenotype in mice. Endocrinology 149:6053–64 [Google Scholar]
  76. Li N, Boyd K, Dempsey PJ, Vignali DA. 76.  2007. Non–cell autonomous expression of TNF-α–converting enzyme ADAM17 is required for normal lymphocyte development. J. Immunol. 178:4214–21 [Google Scholar]
  77. Blaydon DC, Biancheri P, Di WL, Plagnol V, Cabral RM. 77.  et al. 2011. Inflammatory skin and bowel disease linked to ADAM17 deletion. N. Engl. J. Med. 365:1502–8 [Google Scholar]
  78. Franzke CW, Cobzaru C, Triantafyllopoulou A, Loffek S, Horiuchi K. 78.  et al. 2012. Epidermal ADAM17 maintains the skin barrier by regulating EGFR ligand–dependent terminal keratinocyte differentiation. J. Exp. Med. 209:1105–19 [Google Scholar]
  79. Brandl K, Sun L, Neppl C, Siggs OM, Le Gall SM. 79.  et al. 2010. MyD88 signaling in nonhematopoietic cells protects mice against induced colitis by regulating specific EGF receptor ligands. PNAS 107:19967–72 [Google Scholar]
  80. Chalaris A, Adam N, Sina C, Rosenstiel P, Lehmann-Koch J. 80.  et al. 2010. Critical role of the disintegrin metalloprotease ADAM17 for intestinal inflammation and regeneration in mice. J. Exp. Med. 207:1617–24 [Google Scholar]
  81. Yan F, Liu L, Dempsey PJ, Tsai YH, Raines EW. 81.  et al. 2013. A Lactobacillus rhamnosus GG–derived soluble protein, p40, stimulates ligand release from intestinal epithelial cells to transactivate epidermal growth factor receptor. J. Biol. Chem. 288:30742–51 [Google Scholar]
  82. Feng Y, Tsai YH, Xiao W, Ralls MW, Stoeck A. 82.  et al. 2015. Loss of ADAM17-mediated TNFα signaling in intestinal cells attenuates mucosal atrophy in a mouse model of parenteral nutrition. Mol. Cell. Biol. 35:3604–21 [Google Scholar]
  83. Lee D, Yu M, Lee E, Kim H, Yang Y. 83.  et al. 2009. Tumor-specific apoptosis caused by deletion of the ERBB3 pseudo-kinase in mouse intestinal epithelium. J. Clin. Investig. 119:2702–13 [Google Scholar]
  84. Rowland KJ, McMellen ME, Wakeman D, Wandu WS, Erwin CR, Warner BW. 84.  2012. Enterocyte expression of epidermal growth factor receptor is not required for intestinal adaptation in response to massive small bowel resection. J. Pediatr. Surg. 47:1748–53 [Google Scholar]
  85. Yan F, Cao H, Cover TL, Washington MK, Shi Y. 85.  et al. 2011. Colon-specific delivery of a probiotic-derived soluble protein ameliorates intestinal inflammation in mice through an EGFR-dependent mechanism. J. Clin. Investig. 121:2242–53 [Google Scholar]
  86. Zhang Y, Dube PE, Washington MK, Yan F, Polk DB. 86.  2012. ErbB2 and ErbB3 regulate recovery from dextran sulfate sodium–induced colitis by promoting mouse colon epithelial cell survival. Lab. Investig. 92:437–50 [Google Scholar]
  87. Frey MR, Polk DB. 87.  2014. ErbB receptors and their growth factor ligands in pediatric intestinal inflammation. Pediatr. Res. 75:127–32 [Google Scholar]
  88. Powell AE, Wang Y, Li Y, Poulin EJ, Means AL. 88.  et al. 2012. The pan-ErbB negative regulator Lrig1 is an intestinal stem cell marker that functions as a tumor suppressor. Cell 149:146–58 [Google Scholar]
  89. Wong VW, Stange DE, Page ME, Buczacki S, Wabik A. 89.  et al. 2012. Lrig1 controls intestinal stem-cell homeostasis by negative regulation of ErbB signalling. Nat. Cell Biol. 14:401–8 [Google Scholar]
  90. Horiuchi K, Kimura T, Miyamoto T, Takaishi H, Okada Y. 90.  et al. 2007. Cutting edge: TNF-α–converting enzyme (TACE/ADAM17) inactivation in mouse myeloid cells prevents lethality from endotoxin shock. J. Immunol. 179:2686–89 [Google Scholar]
  91. Saha A, Backert S, Hammond CE, Gooz M, Smolka AJ. 91.  2010. Helicobacter pylori CagL activates ADAM17 to induce repression of the gastric H, K-ATPase α subunit. Gastroenterology 139:239–48 [Google Scholar]
  92. Inoshima I, Inoshima N, Wilke GA, Powers ME, Frank KM. 92.  et al. 2011. A Staphylococcus aureus pore-forming toxin subverts the activity of ADAM10 to cause lethal infection in mice. Nat. Med. 17:1310–14 [Google Scholar]
  93. Wilke GA, Wardenburg JB. 93.  2010. Role of a disintegrin and metalloprotease 10 in Staphylococcus aureus α-hemolysin–mediated cellular injury. PNAS 107:13473–78 [Google Scholar]
  94. Sears CL, Geis AL, Housseau F. 94.  2014. Bacteroides fragilis subverts mucosal biology: from symbiont to colon carcinogenesis. J. Clin. Investig. 124:4166–72 [Google Scholar]
  95. Bonazzi M, Lecuit M, Cossart P. 95.  2009. Listeria monocytogenes internalin and E-cadherin: from bench to bedside. Cold Spring Harb. Perspect. Biol. 1:a003087 [Google Scholar]
  96. Naglich JG, Metherall JE, Russell DW, Eidels L. 96.  1992. Expression cloning of a diphtheria toxin receptor: identity with a heparin-binding EGF-like growth factor precursor. Cell 69:1051–61 [Google Scholar]
  97. Dube P, Punit S, Polk DB. 97.  2014. Redeeming an old foe: protective as well as pathophysiological roles for tumor necrosis factor in inflammatory bowel disease. Am. J. Physiol. Gastrointest. Liver Physiol. 308:G161–70 [Google Scholar]
  98. Leppkes M, Roulis M, Neurath MF, Kollias G, Becker C. 98.  2014. Pleiotropic functions of TNF-α in the regulation of the intestinal epithelial response to inflammation. Int. Immunol. 26:509–15 [Google Scholar]
  99. Brynskov J, Foegh P, Pedersen G, Ellervik C, Kirkegaard T. 99.  et al. 2002. Tumour necrosis factor α converting enzyme (TACE) activity in the colonic mucosa of patients with inflammatory bowel disease. Gut 51:37–43 [Google Scholar]
  100. Cesaro A, Abakar-Mahamat A, Brest P, Lassalle S, Selva E. 100.  et al. 2009. Differential expression and regulation of ADAM17 and TIMP3 in acute inflamed intestinal epithelia. Am. J. Physiol. Gastrointest. Liver Physiol. 296:G1332–43 [Google Scholar]
  101. Colon AL, Menchen LA, Hurtado O, De Cristobal J, Lizasoain I. 101.  et al. 2001. Implication of TNF-α convertase (TACE/ADAM17) in inducible nitric oxide synthase expression and inflammation in an experimental model of colitis. Cytokine 16:220–26 [Google Scholar]
  102. Forsyth CB, Banan A, Farhadi A, Fields JZ, Tang Y. 102.  et al. 2007. Regulation of oxidant-induced intestinal permeability by metalloprotease-dependent epidermal growth factor receptor signaling. J. Pharmacol. Exp. Ther. 321:84–97 [Google Scholar]
  103. Kirkegaard T, Pedersen G, Saermark T, Brynskov J. 103.  2004. Tumour necrosis factor-α converting enzyme (TACE) activity in human colonic epithelial cells. Clin. Exp. Immunol. 135:146–53 [Google Scholar]
  104. Franze E, Caruso R, Stolfi C, Sarra M, Cupi ML. 104.  et al. 2013. High expression of the “A Disintegrin And Metalloprotease” 19 (ADAM19), a sheddase for TNF-α in the mucosa of patients with inflammatory bowel diseases. Inflamm. Bowel Dis. 19:501–11 [Google Scholar]
  105. Egger B, Procaccino F, Lakshmanan J, Reinshagen M, Hoffmann P. 105.  et al. 1997. Mice lacking transforming growth factor α have an increased susceptibility to dextran sulfate-induced colitis. Gastroenterology 113:825–32 [Google Scholar]
  106. Egger B, Schmid SW, Naef M, Wildi S, Buchler MW. 106.  2000. Efficacy and safety of weight-adapted nadroparin calcium versus heparin sodium in prevention of clinically evident thromboembolic complications in 1,190 general surgical patients. Dig. Surg. 17:602–9 [Google Scholar]
  107. Frey MR, Edelblum KL, Mullane MT, Liang D, Polk DB. 107.  2009. The ErbB4 growth factor receptor is required for colon epithelial cell survival in the presence of TNF. Gastroenterology 136:217–26 [Google Scholar]
  108. Sahin U, Weskamp G, Kelly K, Zhou HM, Higashiyama S. 108.  et al. 2004. Distinct roles for ADAM10 and ADAM17 in ectodomain shedding of six EGFR ligands. J. Cell Biol. 164:769–79 [Google Scholar]
  109. Lu N, Wang L, Cao H, Liu L, Van Kaer L. 109.  et al. 2014. Activation of the epidermal growth factor receptor in macrophages regulates cytokine production and experimental colitis. J. Immunol. 192:1013–23 [Google Scholar]
  110. Neufert C, Becker C, Tureci O, Waldner MJ, Backert I. 110.  et al. 2013. Tumor fibroblast–derived epiregulin promotes growth of colitis-associated neoplasms through ERK. J. Clin. Investig. 123:1428–43 [Google Scholar]
  111. Hilliard VC, Frey MR, Dempsey PJ, Peek RM Jr, Polk DB. 111.  2011. TNF-α converting enzyme-mediated ErbB4 transactivation by TNF promotes colonic epithelial cell survival. Am. J. Physiol. Gastrointest. Liver Physiol. 301:G338–46 [Google Scholar]
  112. Rio C, Buxbaum JD, Peschon JJ, Corfas G. 112.  2000. Tumor necrosis factor-α–converting enzyme is required for cleavage of erbB4/HER4. J. Biol. Chem. 275:10379–87 [Google Scholar]
  113. Vecchi M, Rudolph-Owen LA, Brown CL, Dempsey PJ, Carpenter G. 113.  1998. Tyrosine phosphorylation and proteolysis: pervanadate-induced, metalloprotease-dependent cleavage of the ErbB-4 receptor and amphiregulin. J. Biol. Chem. 273:20589–95 [Google Scholar]
  114. Tsai Y-H, Feng Y, Wade AW, Teitelbaum DH, Dempsey PJ. 114.  2012. Intestinal cell responses in different injury/regeneration models are differentially dependent on ADAM17. Gastroenterology 142:S61 [Google Scholar]
  115. Demehri FR, Barrett M, Ralls MW, Miyasaka EA, Feng Y, Teitelbaum DH. 115.  2013. Intestinal epithelial cell apoptosis and loss of barrier function in the setting of altered microbiota with enteral nutrient deprivation. Front. Cell Infect. Microbiol. 3:105 [Google Scholar]
  116. Feng Y, Teitelbaum DH. 116.  2012. Epidermal growth factor/TNF-α transactivation modulates epithelial cell proliferation and apoptosis in a mouse model of parenteral nutrition. Am. J. Physiol. Gastrointest. Liver Physiol. 302:G236–49 [Google Scholar]
  117. Feng Y, Tsai YH, Teitelbaum DH, Dempsey PJ. 117.  2012. Intestinal epithelial cell responses to total parenteral nutrition (TPN) are under complex regulation by ADAM17. Gastroenterology 142:S167–68 [Google Scholar]
  118. Feng Y, Teitelbaum DH. 118.  2013. Tumour necrosis factor-α–induced loss of intestinal barrier function requires TNFR1 and TNFR2 signalling in a mouse model of total parenteral nutrition. J. Physiol. 591:3709–23 [Google Scholar]
  119. Roulis M, Armaka M, Manoloukos M, Apostolaki M, Kollias G. 119.  2011. Intestinal epithelial cells as producers but not targets of chronic TNF suffice to cause murine Crohn-like pathology. PNAS 108:5396–401 [Google Scholar]
  120. Stadnyk AW. 120.  2002. Intestinal epithelial cells as a source of inflammatory cytokines and chemokines. Can. J. Gastroenterol. 16:241–46 [Google Scholar]
  121. Xue X, Ramakrishnan S, Anderson E, Taylor M, Zimmermann EM. 121.  et al. 2013. Endothelial PAS domain protein 1 activates the inflammatory response in the intestinal epithelium to promote colitis in mice. Gastroenterology 145:831–41 [Google Scholar]
  122. McMahan RS, Riehle KJ, Fausto N, Campbell JS. 122.  2013. A disintegrin and metalloproteinase 17 regulates TNF and TNFR1 levels in inflammation and liver regeneration in mice. Am. J. Physiol. Gastrointest. Liver Physiol. 305:G25–34 [Google Scholar]
  123. Sanderson MP, Erickson SN, Gough PJ, Garton KJ, Wille PT. 123.  et al. 2005. ADAM10 mediates ectodomain shedding of the betacellulin precursor activated by p-aminophenylmercuric acetate and extracellular calcium influx. J. Biol. Chem. 280:1826–37 [Google Scholar]
  124. Coant N, Ben Mkaddem S, Pedruzzi E, Guichard C, Treton X. 124.  et al. 2010. NADPH oxidase 1 modulates WNT and NOTCH1 signaling to control the fate of proliferative progenitor cells in the colon. Mol. Cell. Biol. 30:2636–50 [Google Scholar]
  125. Zheng X, Tsuchiya K, Okamoto R, Iwasaki M, Kano Y. 125.  et al. 2011. Suppression of hath1 gene expression directly regulated by hes1 via Notch signaling is associated with goblet cell depletion in ulcerative colitis. Inflamm. Bowel. Dis. 17:2251–60 [Google Scholar]
  126. Gersemann M, Stange EF, Wehkamp J. 126.  2011. From intestinal stem cells to inflammatory bowel diseases. World J. Gastroenterol. 17:3198–203 [Google Scholar]
  127. Radtke F, MacDonald HR, Tacchini-Cottier F. 127.  2013. Regulation of innate and adaptive immunity by Notch. Nat. Rev. Immunol. 13:427–37 [Google Scholar]
  128. Xu H, Zhu J, Smith S, Foldi J, Zhao B. 128.  et al. 2012. Notch-RBP-J signaling regulates the transcription factor IRF8 to promote inflammatory macrophage polarization. Nat. Immunol. 13:642–50 [Google Scholar]
  129. Tsai YH, Rakshit R, Chung J, Maillard I, Dempsey PJ. 129.  2013. Myeloid-specific deletion of ADAM10 dramatically increases susceptibility to DSS-induced colitis. Gastroenterology 144:S308 [Google Scholar]
  130. Duffy MJ, McKiernan E, O'Donovan N, McGowan PM. 130.  2009. Role of ADAMs in cancer formation and progression. Clin. Cancer Res. 15:1140–44 [Google Scholar]
  131. Murphy G. 131.  2008. The ADAMs: signalling scissors in the tumour microenvironment. Nat. Rev. Cancer 8:929–41 [Google Scholar]
  132. Noah TK, Shroyer NF. 132.  2013. Notch in the intestine: regulation of homeostasis and pathogenesis. Annu. Rev. Physiol. 75:263–88 [Google Scholar]
  133. van Es JH, van Gijn ME, Riccio O, van den Born M, Vooijs M. 133.  et al. 2005. Notch/γ-secretase inhibition turns proliferative cells in intestinal crypts and adenomas into goblet cells. Nature 435:959–63 [Google Scholar]
  134. Peignon G, Durand A, Cacheux W, Ayrault O, Terris B. 134.  et al. 2011. Complex interplay between β-catenin signalling and Notch effectors in intestinal tumorigenesis. Gut 60:166–76 [Google Scholar]
  135. Tsai YH, Feng Y, Rakshit R, Fearon ER, Dempsey PJ. 135.  2013. Cell-autonomous ADAM10 signaling is required for adenoma initiation after APC mutation. Gastroenterology 144:S51–52 [Google Scholar]
  136. Chanrion M, Kuperstein I, Barriere C, El Marjou F, Cohen D. 136.  et al. 2014. Concomitant Notch activation and p53 deletion trigger epithelial-to-mesenchymal transition and metastasis in mouse gut. Nat. Commun. 5:5005 [Google Scholar]
  137. Sonoshita M, Itatani Y, Kakizaki F, Sakimura K, Terashima T. 137.  et al. 2015. Promotion of colorectal cancer invasion and metastasis through activation of NOTCH-DAB1-ABL-RHOGEF protein TRIO. Cancer Discov. 5:198–211 [Google Scholar]
  138. Lu J, Ye X, Fan F, Xia L, Bhattacharya R. 138.  et al. 2013. Endothelial cells promote the colorectal cancer stem cell phenotype through a soluble form of Jagged-1. Cancer Cell 23:171–85 [Google Scholar]
  139. Fiske WH, Threadgill D, Coffey RJ. 139.  2009. ERBBs in the gastrointestinal tract: recent progress and new perspectives. Exp. Cell Res. 315:583–601 [Google Scholar]
  140. Dong J, Opresko LK, Dempsey PJ, Lauffenburger DA, Coffey RJ, Wiley HS. 140.  1999. Metalloprotease-mediated ligand release regulates autocrine signaling through the epidermal growth factor receptor. PNAS 96:6235–40 [Google Scholar]
  141. Ardito CM, Gruner BM, Takeuchi KK, Lubeseder-Martellato C, Teichmann N. 141.  et al. 2012. EGF receptor is required for KRAS-induced pancreatic tumorigenesis. Cancer Cell. 22:304–17 [Google Scholar]
  142. Van Schaeybroeck S, Kalimutho M, Dunne PD, Carson R, Allen W. 142.  et al. 2014. ADAM17-dependent c-MET-STAT3 signaling mediates resistance to MEK inhibitors in KRAS mutant colorectal cancer. Cell Rep. 7:1940–55 [Google Scholar]
  143. Waldner MJ, Neurath MF. 143.  2014. Master regulator of intestinal disease: IL-6 in chronic inflammation and cancer development. Semin. Immunol. 26:75–79 [Google Scholar]
  144. Atreya R, Mudter J, Finotto S, Mullberg J, Jostock T. 144.  et al. 2000. Blockade of interleukin 6 trans signaling suppresses T-cell resistance against apoptosis in chronic intestinal inflammation: evidence in Crohn disease and experimental colitis in vivo. Nat. Med. 6:583–88 [Google Scholar]
  145. Becker C, Fantini MC, Schramm C, Lehr HA, Wirtz S. 145.  et al. 2004. TGF-β suppresses tumor progression in colon cancer by inhibition of IL-6 trans-signaling. Immunity 21:491–501 [Google Scholar]
  146. Matsumoto S, Hara T, Mitsuyama K, Yamamoto M, Tsuruta O. 146.  et al. 2010. Essential roles of IL-6 trans-signaling in colonic epithelial cells, induced by the IL-6/soluble-IL-6 receptor derived from lamina propria macrophages, on the development of colitis-associated premalignant cancer in a murine model. J. Immunol. 184:1543–51 [Google Scholar]
  147. Mitsuyama K, Matsumoto S, Rose-John S, Suzuki A, Hara T. 147.  et al. 2006. STAT3 activation via interleukin 6 trans-signalling contributes to ileitis in SAMP1/Yit mice. Gut 55:1263–69 [Google Scholar]
  148. Schlomann U, Koller G, Conrad C, Ferdous T, Golfi P. 148.  et al. 2015. ADAM8 as a drug target in pancreatic cancer. Nat. Commun. 6:6175 [Google Scholar]
  149. Sato T, Clevers H. 149.  2013. Growing self-organizing mini-guts from a single intestinal stem cell: mechanism and applications. Science 340:1190–94 [Google Scholar]
  150. Weber S, Wetzel S, Prox J, Lehmann T, Schneppenheim J. 150.  et al. 2013. Regulation of adult hematopoiesis by the a disintegrin and metalloproteinase 10 (ADAM10). Biochem. Biophys. Res. Commun. 442:234–41 [Google Scholar]
  151. Yoda M, Kimura T, Tohmonda T, Uchikawa S, Koba T. 151.  et al. 2011. Dual functions of cell-autonomous and non-cell-autonomous ADAM10 activity in granulopoiesis. Blood 118:6939–42 [Google Scholar]
  152. Faber TW, Pullen NA, Fernando JF, Kolawole EM, McLeod JJ. 152.  et al. 2014. ADAM10 is required for SCF-induced mast cell migration. Cell. Immunol. 290:80–88 [Google Scholar]
  153. Gibb DR, El Shikh M, Kang DJ, Rowe WJ, El Sayed R. 153.  et al. 2010. ADAM10 is essential for Notch2-dependent marginal zone B cell development and CD23 cleavage in vivo. J. Exp. Med. 207:623–35 [Google Scholar]
  154. Chaimowitz NS, Martin RK, Cichy J, Gibb DR, Patil P. 154.  et al. 2011. A disintegrin and metalloproteinase 10 regulates antibody production and maintenance of lymphoid architecture. J. Immunol. 187:5114–22 [Google Scholar]
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