Matrix metalloproteinase dependent cleavage of cell adhesion molecules in the pathogenesis of CNS dysfunction with HIV and methamphetamine

Current HIV Research

Volumn 10, Issue 5, 2012, Pages 384-391

  Conant, Katherine ^a   Lim, Seung T ^a   Randall, Brad ^a   Maguire Zeiss, Kathleen A ^a  

^a GEORGETOWN UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Adhesion; Cell adhesion molecule (CAM); Matrix metalloproteinase (MMP); Methamphetamine; Microglial cell; Neuron; Synapse

Indexed keywords

CELL ADHESION MOLECULE; INTEGRIN; MATRIX METALLOPROTEINASE; METHAMPHETAMINE;

ARTICLE; CELL ACTIVATION; CELL DIVISION; CENTRAL NERVOUS SYSTEM DISEASE; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; MICROGLIA; NONHUMAN; PATHOGENESIS;

ANIMALS; CELL ADHESION; CELL ADHESION MOLECULES; CENTRAL NERVOUS SYSTEM DISEASES; CENTRAL NERVOUS SYSTEM STIMULANTS; HIV INFECTIONS; HUMANS; INFLAMMATION; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; METHAMPHETAMINE; MICE; MICROGLIA; NEURONAL PLASTICITY; RATS; SUBSTANCE-RELATED DISORDERS;

EID: 84866337826     PISSN: 1570162X     EISSN: 18734251     Source Type: Journal    
DOI: 10.2174/157016212802138733     Document Type: Article

References (130)

1. Handsley MM, Cross J., Gavrilovic J, Edwards DR. The Matrix Met-aletal/et-alloproteinases and Their Inhibitors. In: Gottschall PE and Conant K, ed. Matrix Metalloproteinases in the Central Nervous System. Vol.1. London: Imperial College Press, 2005: 3-16.
2. Puente XS, Sanchez LM, Overall CM, Lopez-Otin C. Human and mouse proteases: a comparative genomic approach. Nature reviews 2003; 4: 544-558.
3. Knox JD, Boreham DR, Walker JA, et al. Mapping of the metalloproteinase gene matrilysin (MMP7) to human chromosome 11q21-->q22. Cytogenet Cell Genet 1996; 72: 179-182.
4. Pendas AM, Balbin M, Llano E, et al. Structural analysis and promoter characterization of the human collagenase-3 gene (MMP13). Genomics 1997; 40: 222-233.
5. Gu Z, Kaul M, Yan B, et al. S-nitrosylation of matrix metalloproteinases: signaling pathway to neuronal cell death. Science 2002; 297: 1186-1190.
6. Clutterbuck AL, Asplin KE, Harris P, et al. Targeting matrix metalloproteinases in inflammatory conditions. Curr Drug Targets 2009; 10: 1245-1254.
7. Kohutek ZA, diPierro CG, Redpath GT, Hussaini IM. ADAM-10-mediated N-cadherin cleavage is protein kinase C-alpha dependent and promotes glioblastoma cell migration. J Neurosci 2009; 29: 4605-4615.
8. Matrisian LM. The matrix-degrading metalloproteinases. Bioessays 1992; 14: 455-463.
9. McCawley LJ, Matrisian LM. Matrix metalloproteinases: they're not just for matrix anymore! Curr Opin Cell Biol 2001; 13: 534-540.
10. Yong VW, Power C, Forsyth P, Edwards DR. Metalloproteinases in biology and pathology of the nervous system. Nat Rev Neurosci 2001; 2: 502-511.
11. Ding JY, Kreipke CW, Schafer P, et al. Synapse loss regulated by matrix metalloproteinases in traumatic brain injury is associated with hypoxia inducible factor-1alpha expression. Brain Res 2009; 1268: 125-134.
12. Sbai O, Ferhat L, Bernard A, et al. Vesicular trafficking and secretion of matrix metalloproteinases-2, -9 and tissue inhibitor of metalloproteinases-1 in neuronal cells. Mol Cell Neurosci 2008; 39: 549-568.
13. Kean MJ, Williams KC, Skalski M, et al. VAMP3, syntaxin-13 and SNAP23 are involved in secretion of matrix metalloproteinases, degradation of the extracellular matrix and cell invasion. J Cell Sci 2009; 122: 4089-4098.
14. Salles FJ, Strickland S. Localization and regulation of the tissue plasminogen activator-plasmin system in the hippocampus. J Neurosci 2002; 22: 2125-2134.
15. Gottschall PE SJ, and Zimmerman DR. Substrates for Metalloendopeptidases in the Central Nervous System. In: Gottschall PE and Conant K, ed. Matrix Metalloproteinases in the Central Nervous System Vol. 1. London: Imperial College Press, 2005: 87-118.
16. Boire A, Covic L, Agarwal A, et al. PAR1 is a matrix metalloprotease-1 receptor that promotes invasion and tumorigenesis of breast cancer cells. Cell 2005; 120: 303-313.
17. Yang Y, Estrada EY, Thompson JF, et al. Matrix metalloproteinase-mediated disruption of tight junction proteins in cerebral vessels is reversed by synthetic matrix metalloproteinase inhibitor in focal ischemia in rat. J Cereb Blood Flow Metab 2007; 27: 697-709.
18. Buhler LA, Samara R, Guzman E, et al. Matrix metalloproteinase-7 facilitates immune access to the CNS in experimental autoimmune encephalomyelitis. BMC Neuroscience 2009; 10: 17.
19. Brundula V, Rewcastle NB, Metz LM, et al. Targeting leukocyte MMPs and transmigration: minocycline as a potential therapy for multiple sclerosis. Brain 2002; 125: 1297-1308.
20. Ghorpade A, Persidskaia R, Suryadevara R, et al. Mononuclear phagocyte differentiation, activation, and viral infection regulate matrix metalloproteinase expression: implications for human immunodeficiency virus type 1-associated dementia. J Virol 2001; 75: 6572-6583.
21. Conant K, McArthur JC, Griffin DE, et al. Cerebrospinal fluid levels of MMP-2, 7, and 9 are elevated in association with human immunodeficiency virus dementia. Ann Neurol 1999; 46: 391-398.
22. Sporer B, Paul R, Koedel U, et al. Presence of matrix metalloproteinase-9 activity in the cerebrospinal fluid of human immunodeficiency virus-infected patients. J Infect Dis 1998; 178: 854-857.
23. Conant K, St Hillaire C, Anderson C et al. Human immunodeficiency virus type 1 Tat and methamphetamine affect the release and activation of matrix-degrading proteinases. J Neurovirol 2004;10:21-28.
24. Louboutin JP, Reyes BA, Agrawal L, et al. HIV-1 gp120 upregulates matrix metalloproteinases and their inhibitors in a rat model of HIV encephalopathy. Eur J Neurosci 2011; 34: 2015-2023.
25. Misse D, Esteve PO, Renneboog B, et al. HIV-1 glycoprotein 120 induces the MMP-9 cytopathogenic factor production that is abolished by inhibition of the p38 mitogen-activated protein kinase signaling pathway. Blood 2001; 98: 541-547.
26. Lafrenie RM, Wahl LM, Epstein JS, et al. HIV-1-Tat modulates the function of monocytes and alters their interactions with microvessel endothelial cells. A mechanism of HIV pathogenesis. J Immunol 1996; 156: 1638-1645.
27. Mizoguchi H, Yamada K, Nabeshima T. Neuropsychotoxicity of abused drugs: involvement of matrix metalloproteinase-2 and -9 and tissue inhibitor of matrix metalloproteinase-2 in methamphetamine-induced behavioral sensitization and reward in rodents. J Pharmacol Sci 2008; 106: 9-14.
28. Liu Y, Brown S, Shaikh J, et al. Relationship between methamphetamine exposure and matrix metalloproteinase 9 expression. Neuroreport 2008; 19: 1407-1409.
29. Conant K, Lonskaya I, Szklarczyk A, et al. Methamphetamineassociated cleavage of the synaptic adhesion molecule intercellular adhesion molecule-5. J Neurochem 2011; 118: 521-532
30. Cozzi NV, Sievert MK, Shulgin AT, et al. Inhibition of plasma membrane monoamine transporters by beta-ketoamphetamines. Eur J Pharmacol 1999; 381: 63-69.
31. Sulzer D, Sonders MS, Poulsen NW, Galli A. Mechanisms of neurotransmitter release by amphetamines: a review. Prog Neurobiol 2005; 75: 406-433.
32. Mark KA, Quinton MS, Russek SJ, Yamamoto BK. Dynamic changes in vesicular glutamate transporter 1 function and expression related to methamphetamine-induced glutamate release. J Neurosci 2007; 27: 6823-6831.
33. Spiegel A, Shivtiel S, Kalinkovich A, et al. Catecholaminergic neurotransmitters regulate migration and repopulation of immature human CD34+ cells through Wnt signaling. Nat Immunol 2007; 8: 1123-1131.
34. Speidl WS, Toller WG, Kaun C, et al. Catecholamines potentiate LPS-induced expression of MMP-1 and MMP-9 in human monocytes and in the human monocytic cell line U937: possible implications for peri-operative plaque instability. Faseb J 2004; 18: 603-605.
35. Takemoto Y, Yoshiyama M, Takeuchi K, et al. Increased JNK, AP-1 and NF-kappa B DNA binding activities in isoproterenolinduced cardiac remodeling. J Mol Cell Cardiol 1999; 31: 2017-2030.
36. Guillaumond F, Becquet D, Bosler O, Francois-Bellan AM. Adrenergic inducibility of AP-1 binding in the rat pineal gland depends on prior photoperiod. J Neurochem 2002; 83: 157-166.
37. Conant K, Wang Y, Szklarczyk A, et al. Matrix metalloproteinasedependent shedding of intercellular adhesion molecule-5 occurs with long-term potentiation. Neuroscience 2010; 166: 508-521.
38. Vawter MP, Usen N, Thatcher L, et al. Characterization of human cleaved N-CAM and association with schizophrenia. Exp Neurol 2001; 172: 29-46.
39. Guo H, Tong N, Turner T et al. Release of the neuronal glycoprotein ICAM-5 in serum after hypoxic-ischemic injury. Ann Neurol 2000; 48: 590-602.
40. Eugenin EA, Gamss R, Buckner C, et al. Shedding of PECAM-1 during HIV infection: a potential role for soluble PECAM-1 in the pathogenesis of NeuroAIDS. J Leukoc Biol 2006; 79: 444-452.
41. Lindsberg PJ, Launes J, Tian L, et al. Release of soluble ICAM-5, a neuronal adhesion molecule, in acute encephalitis. Neurology 2002; 58: 446-451.
42. Marambaud P, Wen PH, Dutt A, et al. A CBP binding transcriptional repressor produced by the PS1/epsilon-cleavage of N-cadherin is inhibited by PS1 FAD mutations. Cell 2003; 114: 635-645.
43. Sakamoto Y, Ogita H, Hirota T, et al. Interaction of integrin alpha(v)beta3 with nectin. Implication in cross-talk between cellmatrix and cell-cell junctions. J Biol Chem 2006; 281: 19631-19644.
44. Gahmberg CG, Tian L, Ning L, Nyman-Huttunen H. ICAM-5-a novel two-facetted adhesion molecule in the mammalian brain. Immunol Lett 2008; 117: 131-135.
45. Marciano DK, Denda S, Reichardt LF. Methods for identifying novel integrin ligands. Methods in enzymology 2007; 426: 223-237.
46. Mechtersheimer S, Gutwein P, Agmon-Levin N, et al. Ectodomain shedding of L1 adhesion molecule promotes cell migration by autocrine binding to integrins. J Cell Biol 2001; 155: 661-673.
47. Colton CA, Wilcock DM. Assessing activation states in microglia. CNS Neurol Disord Drug Targets 2010;9: 174-191.
48. Jayadev S, Nesser NK, Hopkins S, et al. Transcription factor p53 influences microglial activation phenotype. Glia 2011; 59: 1402-1413.
49. Campbell JH, Burdo TH, Autissier P, et al. Minocycline inhibition of monocyte activation correlates with neuronal protection in SIV NeuroAIDS. PLoS One 2011; 6: e18688.
50. Zink MC, Uhrlaub J, DeWitt J, et al. Neuroprotective and antihuman immunodeficiency virus activity of minocycline. Jama 2005; 293: 2003-2011.
51. Garden GA. Microglia in human immunodeficiency virusassociated neurodegeneration. Glia 2002; 40: 240-251.
52. Gray F, Adle-Biassette H, Brion F, et al. Neuronal apoptosis in human immunodeficiency virus infection. J Neurovirol 2000; 6 Suppl 1: S38-S43.
53. Kuhn DM, Francescutti-Verbeem DM, Thomas DM. Dopamine quinones activate microglia and induce a neurotoxic gene expression profile: relationship to methamphetamine-induced nerve ending damage. Ann N Y Acad Sci 2006; 1074: 31-41.
54. Cadet JL, Sheng P, Ali S, et al. Attenuation of methamphetamineinduced neurotoxicity in copper/zinc superoxide dismutase transgenic mice. J Neurochem 1994; 62: 380-383.
55. Kim YS, Choi DH, Block ML, et al. A pivotal role of matrix metalloproteinase-3 activity in dopaminergic neuronal degeneration via microglial activation. Faseb J 2007; 21: 179-187.
56. Hamill CE, Caudle WM, Richardson JR, et al. Exacerbation of dopaminergic terminal damage in a mouse model of Parkinson's disease by the G-protein-coupled receptor protease-activated receptor 1. Mol Pharmacol 2007; 72: 653-664.
57. Hanisch UK, Kettenmann H. Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci 2007; 10: 1387-1394.
58. Woo MS, Park JS, Choi IY, et al. Inhibition of MMP-3 or -9 suppresses lipopolysaccharide-induced expression of proinflammatory cytokines and iNOS in microglia. J Neurochem 2008; 106: 770-780.
59. Kim HS, Suh YH. Minocycline and neurodegenerative diseases. Behav Brain Res 2009; 196: 168-179.
60. Duivenvoorden WC, Hirte HW, Singh G. Use of tetracycline as an inhibitor of matrix metalloproteinase activity secreted by human bone-metastasizing cancer cells. Invasion & metastasis 1997; 17: 312-322.
61. Milner R, Campbell IL. The extracellular matrix and cytokines regulate microglial integrin expression and activation. J Immunol 2003; 170: 3850-3858.
62. Gao HM, Zhou H, Zhang F, et al. HMGB1 acts on microglia Mac1 to mediate chronic neuroinflammation that drives progressive neurodegeneration. J Neurosci 2011; 31: 1081-1092.
63. Zhang D, Hu X, Qian L, et al. Microglial MAC1 receptor and PI3K are essential in mediating beta-amyloid peptide-induced microglial activation and subsequent neurotoxicity. J Neuroinflammation 2011; 8: 3.
64. Mizuno T, Yoshihara Y, Kagamiyama H, et al. Neuronal adhesion molecule telencephalin induces rapid cell spreading of microglia. Brain Res 1999; 849: 58-66.
65. Milner R, Crocker SJ, Hung S, et al. Fibronectin- and vitronectininduced microglial activation and matrix metalloproteinase-9 expression is mediated by integrins alpha5beta1 and alphavbeta5. J Immunol 2007; 178: 8158-8167.
66. Milner R, Campbell IL. The integrin family of cell adhesion molecules has multiple functions within the CNS. J Neurosci Res 2002; 69: 286-291.
67. Milward EA, Fitzsimmons C, Szklarczyk A, Conant K. The matrix metalloproteinases and CNS plasticity: an overview. J Neuroimmunol 2007; 187: 9-19.
68. Michaluk P, Kolodziej L, Mioduszewska B, et al. Betadystroglycan as a target for MMP-9, in response to enhanced neuronal activity. J Biol Chem 2007; 282: 16036-16041.
69. Pauly T, Ratliff M, Pietrowski E, et al. Activity-dependent shedding of the NMDA receptor glycine binding site by matrix metalloproteinase 3: a PUTATIVE mechanism of postsynaptic plasticity. PLoS One 2008; 3: e2681.
70. Nagy V, Bozdagi O, Matynia A, et al. Matrix metalloproteinase-9 is required for hippocampal late-phase long-term potentiation and memory. J Neurosci 2006; 26: 1923-1934.
71. Bilousova TV, Rusakov DA, Ethell DW, Ethell IM. Matrix metalloproteinase-7 disrupts dendritic spines in hippocampal neurons through NMDA receptor activation. J Neurochem 2006; 97: 44-56.
72. Wang XB, Bozdagi O, Nikitczuk JS, et al. Extracellular proteolysis by matrix metalloproteinase-9 drives dendritic spine enlargement and long-term potentiation coordinately. Proc Natl Acad Sci USA 2008; 105: 19520-19525.
73. Nagy V, Bozdagi O, Matynia A, et al. Matrix metalloproteinase-9 is required for hippocampal late-phase long-term potentiation and memory. J Neurosci 2006; 26: 1923-1934.
74. Meighan SE, Meighan PC, Choudhury P, et al. Effects of extracellular matrix-degrading proteases matrix metalloproteinases 3 and 9 on spatial learning and synaptic plasticity. J Neurochem 2006; 96: 1227-1241.
75. Tian L, Stefanidakis M, Ning L, et al. Activation of NMDA receptors promotes dendritic spine development through MMPmediated ICAM-5 cleavage. J Cell Biol 2007; 178: 687-700.
76. Meighan PC, Meighan SE, Davis CJ, et al. Effects of matrix metalloproteinase inhibition on short- and long-term plasticity of schaffer collateral/CA1 synapses. J Neurochem 2007; 102: 2085-2096.
77. Mizoguchi H, Yamada K, Mouri A, et al. Role of matrix metalloproteinase and tissue inhibitor of MMP in methamphetamine-induced behavioral sensitization and reward: implications for dopamine receptor down-regulation and dopamine release. J Neurochem 2007; 102: 1548-1560.
78. Brown TE, Forquer MR, Cocking DL, et al. Role of matrix metalloproteinases in the acquisition and reconsolidation of cocaine-induced conditioned place preference. Learning & memory (Cold Spring Harbor, N.Y. 2007; 14: 214-223.
79. Brown TE, Forquer MR, Harding JW, et al. Increase in matrix metalloproteinase-9 levels in the rat medial prefrontal cortex after cocaine reinstatement of conditioned place preference. Synapse 2008; 62: 886-889.
80. Maiya R, Zhou Y, Norris EH, et al. Tissue plasminogen activator modulates the cellular and behavioral response to cocaine. Proc Natl Acad Sci USA 2009; 106: 1983-1988.
81. Sfakianos MK, Eisman A, Gourley SL, et al. Inhibition of Rho via Arg and p190RhoGAP in the postnatal mouse hippocampus regulates dendritic spine maturation, synapse and dendrite stability, and behavior. J Neurosci 2007; 27: 10982-10992.
82. Szklarczyk A, Conant K, Owens DF, et al. Matrix metalloproteinase-7 modulates synaptic vesicle recycling and induces atrophy of neuronal synapses. Neuroscience 2007; 149: 87-98.
83. Masliah E, Heaton RK, Marcotte TD, et al. Dendritic injury is a pathological substrate for human immunodeficiency virus-related cognitive disorders. HNRC Group. The HIV Neurobehavioral Research Center. Ann Neurol 1997; 2: 963-972.
84. Langford D, Adame A, Grigorian A, et al. Patterns of selective neuronal damage in methamphetamine-user AIDS patients. J Acquir Immune Defic Syndr 2003; 34: 467-474.
85. Valentijn AJ, Zouq N, Gilmore AP. Anoikis. Biochem Soc Trans 2004; 32: 421-425.
86. Vitolo D, Paradiso P, Uccini S, et al. Expression of adhesion molecules and extracellular matrix proteins in glioblastomas: relation to angiogenesis and spread. Histopathology 1996; 28: 521-528.
87. Tsakadze NL, Sithu SD, Sen U, et al. Tumor necrosis factor-alphaconverting enzyme (TACE/ADAM-17) mediates the ectodomain cleavage of intercellular adhesion molecule-1 (ICAM-1). J Biol Chem 2006; 281: 3157-3164.
88. Lyons PD, Benveniste EN. Cleavage of membrane-associated ICAM-1 from astrocytes: involvement of a metalloprotease. Glia 1998; 22: 103-112.
89. Clark WM, Lauten JD, Lessov N, et al. Time course of ICAM-1 expression and leukocyte subset infiltration in rat forebrain ischemia. Molecular and chemical neuropathology / sponsored by the International Society for Neurochemistry and the World Federation of Neurology and research groups on neurochemistry and cerebrospinal fluid 1995; 26: 213-230.
90. Satoh J, Kastrukoff LF, Kim SU. Cytokine-induced expression of intercellular adhesion molecule-1 (ICAM-1) in cultured human oligodendrocytes and astrocytes. J Neuropathol Exp Neurol 1991; 50: 215-226.
91. Rutishauser U, Acheson A, Hall AK, et al. The neural cell adhesion molecule (NCAM) as a regulator of cell-cell interactions. Science 1988; 240: 53-57.
92. Bhat S, Silberberg DH. Developmental expression of neural cell adhesion molecules of oligodendrocytes in vivo and in culture. J Neurochem 1988; 50: 1830-1838.
93. Wang Y, Neumann H. Alleviation of neurotoxicity by microglial human Siglec-11. J Neurosci; 30: 3482-3488.
94. Hinkle CL, Diestel S, Lieberman J, Maness PF. Metalloproteaseinduced ectodomain shedding of neural cell adhesion molecule (NCAM). J Neurobiol 2006; 66: 1378-1395.
95. Niquet J, Jorquera I, Ben-Ari Y, Represa A. NCAM immunoreactivity on mossy fibers and reactive astrocytes in the hippocampus of epileptic rats. Brain Res 1993; 626: 106-116.
96. Gutwein P, Stoeck A, Riedle S, et al. Cleavage of L1 in exosomes and apoptotic membrane vesicles released from ovarian carcinoma cells. Clin Cancer Res 2005; 11: 2492-2501.
97. Maretzky T, Schulte M, Ludwig A, et al. L1 is sequentially processed by two differently activated metalloproteases and presenilin/gamma-secretase and regulates neural cell adhesion, cell migration, and neurite outgrowth. Mol Cell Biol 2005; 25: 9040-9053.
98. Nolte C, Moos M, Schachner M. Immunolocalization of the neural cell adhesion molecule L1 in epithelia of rodents. Cell Tissue Res 1999; 298: 261-273.
99. Itoh K, Sakurai Y, Asou H, Umeda M. Differential expression of alternatively spliced neural cell adhesion molecule L1 isoforms during oligodendrocyte maturation. J Neurosci Res 2000; 60: 579-586.
100. Guaiquil V, Swendeman S, Yoshida T, et al. ADAM9 is involved in pathological retinal neovascularization. Mol Cell Biol 2009; 29: 2694-2703.
101. Wassmer SC, Moxon CA, Taylor T, et al. Vascular endothelial cells cultured from patients with cerebral or uncomplicated malaria exhibit differential reactivity to TNF. Cellular Microbiology 2011; 13: 198-209.
102. Peterson JW, Bo L, Mork S, et al. VCAM-1-positive microglia target oligodendrocytes at the border of multiple sclerosis lesions. J Neuropathol Exp Neurol 2002; 61: 539-546.
103. Birdsall HH, Lane C, Ramser MN, Anderson DC. Induction of VCAM-1 and ICAM-1 on human neural cells and mechanisms of mononuclear leukocyte adherence. J Immunol 1992; 148: 2717-2723.
104. Kaluza J, Krupinski J, Kumar P, et al. VCAM-1 expression on reactive and tumour astrocytes. Folia Histochem Cytobiol 1994; 32(1): 17-20.
105. Reiss K, Maretzky T, Ludwig A, et al. ADAM10 cleavage of Ncadherin and regulation of cell-cell adhesion and beta-catenin nuclear signalling. Embo J 2005; 24: 742-752.
106. Payne HR, Hemperly JJ, Lemmon V. N-cadherin expression and function in cultured oligodendrocytes. Brain Res Dev Brain Res 1996; 97: 9-15.
107. Neugebauer KM, Tomaselli KJ, Lilien J, Reichardt LF. N-cadherin, NCAM, and integrins promote retinal neurite outgrowth on astrocytes in vitro. J Cell Biol 1988; 107: 1177-1187.
108. Williams H, Johnson JL, Jackson CL, et al. MMP-7 mediates cleavage of N-cadherin and promotes smooth muscle cell apoptosis. Cardiovascular research 2010; 87: 137-146.
109. Maretzky T, Reiss K, Ludwig A, et al. ADAM10 mediates Ecadherin shedding and regulates epithelial cell-cell adhesion, migration, and beta-catenin translocation. Proc Natl Acad Sci USA 2005; 102: 9182-9187.
110. Lee KH, Choi EY, Hyun MS, et al. Association of extracellular cleavage of E-cadherin mediated by MMP-7 with HGF-induced in vitro invasion in human stomach cancer cells. European surgical research. Eur Surg Res 2007; 39(4): 208-215.
111. Najy AJ, Day KC, Day ML. The ectodomain shedding of Ecadherin by ADAM15 supports ErbB receptor activation. J Biol Chem 2008; 283: 18393-18401.
112. Maretzky T, Scholz F, Koten B, et al. ADAM10-mediated Ecadherin release is regulated by proinflammatory cytokines and modulates keratinocyte cohesion in eczematous dermatitis. J Invest Dermatol 2008; 128: 1737-1746.
113. Mizuhara E, Minaki Y, Nakatani T, et al. Purkinje cells originate from cerebellar ventricular zone progenitors positive for Neph3 and E-cadherin. Developmental biology 2010; 338: 202-214.
114. Abbruscato TJ, Davis TP. Protein expression of brain endothelial cell E-cadherin after hypoxia/aglycemia: influence of astrocyte contact. Brain Res 1999; 842: 277-286.
115. Ichikawa Y, Ishikawa T, Momiyama N, et al. Matrilysin (MMP-7) degrades VE-cadherin and accelerates accumulation of beta-catenin in the nucleus of human umbilical vein endothelial cells. Oncology reports 2006; 15: 311-315.
116. Kim J, Lilliehook C, Dudak A. Activity-dependent alpha-cleavage of nectin-1 is mediated by a disintegrin and metalloprotease 10 (ADAM10). J Biol Chem 2010; 285: 22919-22926.
117. Kim DY, Ingano LA, Kovacs DM. Nectin-1alpha, an immunoglobulin-like receptor involved in the formation of synapses, is a substrate for presenilin/gamma-secretase-like cleavage. J Biol Chem 2002; 277: 49976-49981.
118. Mizoguchi A, Nakanishi H, Kimura K, et al. Nectin: an adhesion molecule involved in formation of synapses. J Cell Biol 2002; 156: 555-565.
119. Su G, Blaine SA, Qiao D, Friedl A. Membrane type 1 matrix metalloproteinase-mediated stromal syndecan-1 shedding stimulates breast carcinoma cell proliferation. Cancer Res 2008; 68: 9558-9565.
120. Hayashida K, Stahl PD, Park PW. Syndecan-1 ectodomain shedding is regulated by the small GTPase Rab5. J Biol Chem 2008; 283: 35435-35444
121. Li Q, Park PW, Wilson CL, Parks WC. Matrilysin shedding of syndecan-1 regulates chemokine mobilization and transepithelial efflux of neutrophils in acute lung injury. Cell 2002; 111: 635-646.
122. Chen P, Abacherli LE, Nadler ST, et al. MMP7 shedding of syndecan-1 facilitates re-epithelialization by affecting alpha(2)beta(1) integrin activation. PLoS One 2009; 4: e6565.
123. Brule S, Charnaux N, Sutton A, et al. The shedding of syndecan-4 and syndecan-1 from HeLa cells and human primary macrophages is accelerated by SDF-1/CXCL12 and mediated by the matrix metalloproteinase-9. Glycobiology 2006; 16: 488-501.
124. Murakami K, Namikawa K, Shimizu T, et al. Nerve injury induces the expression of EXT2, a glycosyltransferase required for heparin sulfate synthesis. Neuroscience 2006; 141: 1961-1969.
125. Properzi F, Lin R, Kwok J, et al. Heparan sulphate proteoglycans in glia and in the normal and injured CNS: expression of sulphotransferases and changes in sulphation. Eur J Neurosci 2008; 27: 593-604.
126. Ohnishi H, Kobayashi H, Okazawa H, et al. Ectodomain shedding of SHPS-1 and its role in regulation of cell migration. J Biol Chem 2004; 279: 27878-27887.
127. Comu S, Weng W, Olinsky S, et al. The murine P84 neural adhesion molecule is SHPS-1, a member of the phosphatasebinding protein family. J Neurosci 1997; 17: 8702-8710.
128. Kusakari S, Ohnishi H, Jin FJ, et al. Trans-endocytosis of CD47 and SHPS-1 and its role in regulation of the CD47-SHPS-1 system. J Cell Sci 2008; 121: 1213-1223.
129. Tomizawa T, Kaneko Y, Kaneko Y, et al. Resistance to experimental autoimmune encephalomyelitis and impaired T cell priming by dendritic cells in Src homology 2 domain-containing protein tyrosine phosphatase substrate-1 mutant mice. J Immunol 2007; 179: 869-877.
130. Johansen ML, Brown EJ. Dual regulation of SIRPalpha phosphorylation by integrins and CD47. J Biol Chem 2007; 282: 24219-24230.