Abstract
As the embryo develops, multiple cellular events of division, differentiation, migration, and invasion occur. Cells are formed at specific locations and migrate along different axes to various destinations, by acquiring diverse types of molecular machineries and processes. One such process is the epithelial-to-mesenchymal transition (EMT), in which epithelial cells with highly ordered shapes and contacts transform into mesenchyme in order to start migration. Consequently, these separated cells react to intracellular and extracellular signals to travel through different microenvironments along stereotypical, long-distance migratory routes to their precise homing targets. Different types of proteases are necessary to execute such complex events. One excellent system to evaluate cell movements during embryonic development is the population of neural crest cells. These unique cells are initially formed as part of the neural epithelium, but then they undergo a dramatic EMT after which they extensively migrate and differentiate into various fates including craniofacial skeleton, skin pigments, and peripheral nerves. In this review, we will discuss the central roles of proteases, mainly the family of matrix metalloproteases, in facilitating neural crest cell migration, and propose an integrative model to suggest the orchestrated action of two such proteases in these developmental events.
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References
Kalcheim C, Burstyn-Cohen, T (2005) Early stages of neural crest ontogeny: formation and regulation of cell delamination. Int J Dev Biol 49:105-116
Le Douarin NM, Kalcheim C (1999) The Neural Crest. 2nd edn. Cambridge University Press, Cambridge.
Barembaum M, Bronner-Fraser M (2005) Early steps in neural crest specification. Semin Cell Dev Biol 16:642-646
Erickson CA, Reedy MV (1998) Neural Crest Development: The Interplay between Morphogenesis and Cell Differentiation. Curr Top Dev Bio 40:177-209
Kulesa PM, Gammill LS (2010) Neural crest migration: Patterns, phases and signals. Dev Biol 344:566-568
Bronner-Fraser M (1993) Neural crest cell migration in the developing embryo. Trends Cell Biol 3:392-397
McKinney MC, Stark DA, Teddy J et al (2011) Neural crest cell communication involves an exchange of cytoplasmic material through cellular bridges revealed by photoconversion of KikGR. Dev Dyn 240:1391-1401
Teddy JM, Kulesa PM (2004) In vivo evidence for short- and long-range cell communication in cranial neural crest cells. Development 131:6141-6151
Nichols DH (1986) Formation and distribution of neural crest mesenchyme to the first pharyngeal arch region of the mouse embryo. Am J Anat 176:221-231
Sadler TW (2006) Langman’s medical embryology. 10th edn. Lippincott Williams & Wilkins, Philadelphia, p 67-87
Trainor A (2005) Specification of neural crest cell formation and migration in mouse embryos. Semin Cell Dev Biol 16:683-693
Sauka-Spengler T, Bronner-Fraser M (2006) Development and evolution of the migratory neural crest: a gene regulatory perspective. Curr Opin Genet Dev 16:360-366
Taylor KM, LaBonne C (2007) Modulating the activity of neural crest regulatory factors. Curr Opin Genet Dev 17:326-331
Raible DW (2006) Development of the neural crest: achieving specificity in regulatory pathways. Curr Opin Cell Biol 18:698-703
Kirby ML, Waldo KL (1995) Neural Crest and Cardiovascular Patterning. Circ Res 77:211-215
Acloque H, Adams MS, Fishwick K et al (2009) Epithelial-mesenchymal transitions: the importance of changing cell state in development and disease. J Clin Invest 119: 1438-1449
Badner JA, Sieber WK, Garver KL et al (1990) A genetic study of Hirschsprung disease. Am J Hum Genet 46:568-580
Cobourne MT (2004) The complex genetics of cleft lip and palate. Eur J Orthod. 26:7-16
Farlie PG, McKeown SJ, Newgreen DF (2004) The neural crest: basic biology and clinical relationships in the craniofacial and enteric nervous systems. Birth Defects Res C Embryo Today 72:173-189
Read AP, Newton VE (1997) Waardenburg syndrome. J Med Genet 34:656-665
Morales AV, Barbas JA, Nieto MA (2005) How to become neural crest: From segregation to delamination. Semin Cell Dev Biol 16:655-662
Sela-Donenfeld D, Kalcheim C (2000) Inhibition of noggin expression in the dorsal neural tube by somitogenesis: a mechanism for coordinating the timing of neural crest emigration. Development 127:4845-4854
Sela-Donenfeld D, Kalcheim C (1999) Regulation of the onset of neural crest migration by coordinated activity of BMP4 and Noggin in the dorsal neural tube. Development 126:4749-4762
Martinez-Morales PL, Diez del Corral R, Olivera-Martinez I ,et al (2011) FGF and retinoic acid activity gradients control the timing of neural crest cell emigration in the trunk. J Cell Biol 194:489-503
Kerosuo L, Bronner-Fraser M (2012) What is bad in cancer is good in the embryo: importance of EMT in neural crest development. Semin Cell Dev Biol 23: 320-332
Duband JL, Monier F, Delannet M et al (1995) Epithelium-mesenchyme transition during neural crest development. Acta Anat (Basel). 154:63-78
Lu P, Weaver VM, Werb Z (2012) The extracellular matrix: A dynamic niche in cancer progression. J Cell Bio 196:395-406
Mott JD, Werb Z (2004) Regulation of matrix biology by matrix metalloproteinases. Curr Opin Cell Biol 16:558-564
Henderson DJ, Copp AJ (1997) Role of the extracellular matrix in neural crest cell migration. J Anat 191:507-515
Perris R (1997) The extracellular matrix in neural crest-cell migration. Trends Neurosci 20:23-31
Perris R, Perissinotto D (2000) Role of the extracellular matrix during neural crest cell migration. Mech Dev 95:3-21
Klar A, Baldassare M, Jessell TM (1992) F-spondin: A gene expressed at high levels in the floor plate encodes a secreted protein that promotes neural cell adhesion and neurite extension. Cell 69:95-110
Lawler J (2000) The functions of thrombospondin-1 and-2. Curr Opin Cell Biol 12:634-640
Tucker RP, Hagios C, Chiquet-Ehrismann R, et al (1999) Thrombospondin-1 and neural crest cell migration. Dev Dyn 214:312-322
Debby-Brafman A, Burstyn-Cohen T, Klar A et al (1999) F-Spondin, Expressed in Somite Regions Avoided by Neural Crest Cells, Mediates Inhibition of Distinct Somite Domains to Neural Crest Migration. Neuron 22:475-488
Strobl-Mazzulla PH, Bronner M.E. (2012) Epithelial to mesenchymal transition: New and old insights from the classical neural crest model. Semin Cancer Biol 22:411-416
Chu YS, Eder O, Thomas WA, et al (2006) Prototypical Type I E-cadherin and Type II Cadherin-7 Mediate Very Distinct Adhesiveness through Their Extracellular Domains. J Biol Chem 281:2901-2910
Pla P, Moore R, Morali OG et al (2001) Cadherins in neural crest cell development and transformation. J Cell Physiol 189:121-132
Taneyhill LA (2008) To adhere or not to adhere: The role of Cadherins in neural crest cell development. Cell Adh Mig 2:223-230
McKeown SJ, Wallace AS, Anderson RB (2013) Expression and function of cell adhesion molecules during neural crest migration. Dev Biol 373:244-257
Nakagawa S, Takeichi M (1995) Neural crest cell-cell adhesion controlled by sequential and subpopulation-specific expression of novel cadherins. Development 121:1321-1332
Coles EG, Taneyhill LA, Bronner-Fraser M (2007) A critical role for Cadherin6B in regulating avian neural crest emigration. Dev Biol 312:533-544
Nakagawa S, Takeichi M (1998) Neural crest emigration from the neural tube depends on regulated cadherin expression. Development 125:2963-2971
Park KS, Gumbiner BM, (2010) Cadherin 6B induces BMP signaling and de-epithelialization during the epithelial mesenchymal transition of the neural crest. Development 137:2691-2701
Coles, EG, Gammill LS, Miner JH et al (2006) Abnormalities in neural crest cell migration in laminin ±5 mutant mice. Dev Biol 289:218-228
Duband JL, Thiery JP (1987) Distribution of laminin and collagens during avian neural crest development. Development 101:461-478
Kil SH, Lallier T, Bronner-Fraser M (1996) Inhibition of cranial neural crest adhesion in vitro and migration in vivo using integrin antisense oligonucleotides. Dev Biol 179:91-101
Groblewska M, Siewko M, Mroczko B et al. (2012) The role of matrix metalloproteinases (MMPs) and their inhibitors (TIMPs) in the development of esophageal cancer. Folia Histochem Cytobiol 50:12-19
Sternlicht MD, Werb Z (2001) How Matrix metalloproteinases regulate cell Behavior. Annu Rev Cell Dev Biol 17:463-516
Nagase H, Woessner JF (1999) Matrix Metalloproteinases. J Biol Chem 274:21491-21494
Overall CM, Tam E, McQuibban GA et al (2000) Domain Interactions in the Gelatinase A.TIMP-2.MT1-MMP Activation Complex: the ectodomain of the 44-kda form of membrane type-1 matrix metalloproteinase does not modulate gelatinase a activation. J Biol Chem 275:39497-39506
Stöcker W, Grams F, Reinemer P et al (1995) The metzincins — Topological and sequential relations between the astacins, adamalysins, serralysins, and matrixins (collagenases) define a super family of zinc-peptidases. Protein Sci 4:823-840
Sternlicht MD, Bissell MJ, Werb Z (2000) The matrix metalloproteinase stromelysin-1 acts as a natural mammary tumor promoter. Oncogene 19:1102-1113
Nelson AR, Fingleton B, Rothenberg ML et al (2000) Matrix Metalloproteinases: Biologic Activity and Clinical Implications. J Clin Oncol 18:1135-1149
Bauvois B (2012) New facets of matrix metalloproteinases MMP-2 and MMP-9 as cell surface transducers: Outside-in signaling and relationship to tumor progression. Biochim Biophys Acta 1825:29-36
Egeblad M, Werb Z (2002) New functions for the matrix metalloproteinases in cancer progression. Nat Rev Cancer 2:161-174
Cauwe B, Opdenakker G (2010) Intracellular substrate cleavage: a novel dimension in the biochemistry, biology and pathology of matrix metalloproteinases. Crit Rev Biochem Mol Biol 45:351-423
Mannello F, Medda V (2012) Nuclear localization of Matrix metalloproteinases. Prog Histochem Cytochem 47:27-58
Berezney R (1992) The Nuclear Matrix: Structure, Function and DNA Replication. In, Bittar E (ed) : Advances in Molecular and Cell Biology. Elsevier, Amsterdam p. 37
Nelson WG, Pienta KJ, Barrack ER et al (1986) The role of the nuclear matrix in the organization and function of DNA. Annu Rev Biophys Biophys Chem 15:457-475
Yeghiazaryan M, Zybura-Broda K, Cabaj A et al (2012) Fine-structural distribution of MMP-2 and MMP-9 activities in the rat skeletal muscle upon training: a study by high-resolution in situ zymography. Histochem Cell Biol 138:75-87
Sbai O, Ould-Yahoui A, Ferhat L et al (2010) Differential vesicular distribution and trafficking of MMP-2, MMP-9, and their inhibitors in astrocytes. Glia 58:344-366
Eguchi T, Kubota S, Kawata K (2008) Novel Transcription Factor-Like Function of Human Matrix Metalloproteinase 3 Regulating the CTGF/CCN2 Gene. Mol Cell Biol 28: 2391-2413
Boudreau N, Myers C, Bissell MJ (1995) From laminin to lamin: regulation of tissue-specific gene expression by the ECM. Trends Cell Biol 5:1-4
Lohi J, Wilson CL, Roby JD et al (2001) Epilysin, a Novel Human Matrix Metalloproteinase (MMP-28) Expressed in Testis and Keratinocytes and in Response to Injury. J Biol Chem 276:10134-10144
Visse R, Nagase H. (2003) Matrix metalloproteinases and tissue inhibitors of metalloproteinases: structure, function, and biochemistry. Circ Res 92:827-839
Bourboulia D, Stetler-Stevenson WG (2010) Matrix metalloproteinases (MMPs) and tissue inhibitors of metalloproteinases (TIMPs): Positive and negative regulators in tumor cell adhesion. Semin Cancer Biol 20:161-168
Duong TD, Erickson CA (2004) MMP-2 plays an essential role in producing epithelial-mesenchymal transformations in the avian embryo. Dev Dyn 229:42-53
Cai DH, Vollberg TM. Hahn-Dantona, E. et al (2000) MMP-2 expression during early avian cardiac and neural crest morphogenesis. Anat Rec 259:168-179
Monsonego-Ornan E, Kosonovsky J, Bar A et al (2012) Matrix metalloproteinase 9/gelatinase B is required for neural crest cell migration. Dev Biol 364:162-177
Giambernardi TA, Sakaguchi AY, Gluhak J et al (2001) Neutrophil collagenase (MMP-8) is expressed during early development in neural crest cells as well as in adult melanoma cells. Matrix Biol 20:577-587
Harrison M.,Abu-Elmagd M, Grocott T et al (2004) Matrix metalloproteinase genes in Xenopus development. Dev Dyn 231:214-220
Morris-Wiman J, Burch H, Basco E (2000) Temporospatial distribution of matrix metalloproteinase and tissue inhibitors of matrix metalloproteinases during murine secondary palate morphogenesis. Anat Embryol 202:129-141
Blavier L., Lazaryev A, Groffen J et al., (2001) TGF-beta3-induced palatogenesis requires matrix metalloproteinases. Mol Biol Cell 12:1457-1466
Goldberg M, Septier D, Bourd K et al., (2003) Immunohistochemical localization of MMP-2, MMP-9, TIMP-1, and TIMP-2 in the forming rat incisor. Connect Tissue Res 44:143-153
Reponen P, Sahlberg C, Huhtala P et al (1992) Molecular cloning of murine 72-kDa type IV collagenase and its expression during mouse development. J Biol Chem 267:7856-7862
Robbins JR, McGuire PG, Wehrle-Haller B et al (1999) Diminished Matrix Metalloproteinase 2 (MMP-2) in Ectomesenchyme-Derived Tissues of the Patch Mutant Mouse: Regulation of MMP-2 by PDGF and Effects on Mesenchymal Cell Migration. Dev Biol 212:255-263
Martignetti JA, Aqeel AA, Sewairi WA et al (2001) Mutation of the matrix metalloproteinase 2 gene (MMP2) causes a multicentric osteolysis and arthritis syndrome. Nat Genet 28: 261-265
Al Aqeel, A, Al Sewairi W, Edress B et al., (2000) Inherited multicentric osteolysis with arthritis: A variant resembling Torg syndrome in a Saudi family. Am J Med Genet 93:11-18
Al-Mayouf SM, Majeed M, Hugosson C et al (2000) New form of idiopathic osteolysis: Nodulosis, arthropathy and osteolysis (NAO) syndrome. Am J Med Genet 93:5-10
Itoh T, Ikeda T, Gomi H et al (1997) Unaltered secretion of beta-amyloid precursor protein in gelatinase A (matrix metalloproteinase 2)-deficient mice. J Biol Chem 272:22389-22392
Mosig RA, Dowling O, DiFeo A et al (2007) Loss of MMP-2 disrupts skeletal and craniofacial development and results in decreased bone mineralization, joint erosion and defects in osteoblast and osteoclast growth. Hum Mol Genet 16:1113-1123
Vu TH, Shipley JM, Bergers G et al (1998) MMP-9/Gelatinase B Is a Key Regulator of Growth Plate Angiogenesis and Apoptosis of Hypertrophic Chondrocytes. Cell 93:411-422
Letra A, da Silva RA, Menezes R et al (2007) Studies with MMP9 gene promoter polymorphism and nonsyndromic cleft lip and palate. Am J Med Genet 143: 89-91
Chin JR, Werb Z (1997) Matrix metalloproteinases regulate morphogenesis, migration and remodeling of epithelium, tongue skeletal muscle and cartilage in the mandibular arch. Development 124:1519-1530
Werb Z, Chin JR (1998) Extracellular Matrix Remodeling during Morphogenesis. Ann N Y Acad Sci 857:110-118
Collins JM, Ramamoorthy K, Silveira AD et al (2005) Expression of matrix metalloproteinase genes in the rat intramembranous bone during postnatal growth and upon mechanical stresses. J Biomech 38:485-492
Achong R, Nishimura I, Ramachandran H et al (2003) Membrane Type (MT)1-Matrix Metalloproteinase (MMP) and MMP-2 Expression in Ligature-Induced Periodontitis in the Rat. J Periodont 74:494-500
Holmbeck K, Bianco P, Caterina J et al (1999) MT1-MMP-Deficient Mice Develop Dwarfism, Osteopenia, Arthritis, and Connective Tissue Disease due to Inadequate Collagen Turnover. Cell 99:81-92
Zhou Z, Apte SS, Soininen R et al (2000) Impaired endochondral ossification and angiogenesis in mice deficient in membrane-type matrix metalloproteinase I. Proc Natl Acad Sci USA 97:4052-4057
Singh GD, Moxham BJ (1996) Mesenchymal Cell Activity during 5-fluoro-2-deoxyuridine-Induced Cleft Palate Formation in the Rat. Cleft Palate Craniofac J 33:395-399
Shi J, Son MY, Yamada S et al (2008) Membrane-type MMPs enable extracellular matrix permissiveness and mesenchymal cell proliferation during embryogenesis. Dev Biol 313:196-209
Letra A, Silva RA, Menezes R et al (2007) MMP gene polymorphisms as contributors for cleft lip/palate: Association with MMP3 but not MMP1. Arch Oral Biol 52:954-960
Morris-Wiman J, Du Y, Brinkley L (1999) Occurrence and temporal variation in matrix metalloproteinases and their inhibitors during murine secondary palatal morphogenesis. J Craniofac Genet Dev Biol 19:201-212
Anderson RB, Newgreen DF, Young HM (2006) Neural crest and the development of the enteric nervous system. Adv Exp Med Biol 589:181-196
Kuo BR, Erickson CA (2010) Regional differences in neural crest morphogenesis. Cell Adh Mig 4:567-585
Anderson RB (2010) Matrix metalloproteinase-2 is involved in the migration and network formation of enteric neural crest-derived cells. Int J Dev Biol 54:63-69
Cai DH, Brauer PR (2002) Synthetic matrix metalloproteinase inhibitor decreases early cardiac neural crest migration in chicken embryos. Dev Dyn 224: 441-449
Tomlinson ML, Guan P, Morris RJ et al (2009) A Chemical Genomic Approach Identifies Matrix Metalloproteinases as Playing an Essential and Specific Role in Xenopus Melanophore Migration. Chem Biol 16:93-104
Levin JI, Chen J, Du M et al (2001) The discovery of anthranilic acid-Based MMP inhibitors. Part 2: SAR of the 5-position and P11 groups. Bioorg Med Chem Lett 11:2189-2192
Coyle RC, Latimer A, Jessen JR (2008) Membrane-type 1 matrix metalloproteinase regulates cell migration during zebrafish gastrulation: Evidence for an interaction with non-canonical Wnt signaling. Exp Cell Res 314:2150-2162
Hillegass JM, Villano CM, Cooper KR et al (2008) Glucocorticoids Alter Craniofacial Development and Increase Expression and Activity of Matrix Metalloproteinases in Developing Zebrafish (Danio rerio). Toxicol Sci 102:413-424
Hillegass JM, Villano CM, Cooper KR, et al (2007) Matrix Metalloproteinase-13 Is Required for Zebra fish (Danio rerio) Development and Is a Target for Glucocorticoids. Toxico Sci 100:168-179
Bonventre JA, White LA, Cooper KR (2012) Craniofacial abnormalities and altered wnt and mmp mRNA expression in zebrafish embryos exposed to gasoline oxygenates ETBE and TAME. Aquat Toxicol 120-121:45-53
Murphy D, Diaz Ba, Bromann PA et al (2011) A Src-Tks5 Pathway Is Required for Neural Crest Cell Migration during Embryonic Development. PLoS ONE 6:e22499. doi:10.1371/journal.pone.0022499
van Boxtel AL, Gansner JM, Hakvoort HWJ et al (2011) Lysyl oxidase-like 3b is critical for cartilage maturation during zebrafish craniofacial development. Matrix Biol 30:178-187
Moro E, Tomanin R, Friso A, et al (2010) A novel functional role of iduronate-2-sulfatase in zebrafish early development. Matrix Biol 29:43-50
Cantemir V, Cai DH, Reedy MV et al (2004) Tissue inhibitor of metalloproteinase-2 (TIMP-2) expression during cardiac neural crest cell migration and its role in proMMP-2 activation. Dev Dyn 231:709-719
Brauer PR and Cai DH (2002) Expression of tissue inhibitor of metalloproteinases (TIMPs) during early cardiac development. Mech Dev 113:175-179
Pickard B, Damjanovski S (2004) Overexpression of the tissue inhibitor of metalloproteinase-3 during Xenopus embryogenesis affects head and axial tissue formation. Cell Res 14:389-399
Werb Z, Vu TH, Rinkenberger JL et al (1999) Matrix-degrading proteases and angiogenesis during development and tumor formation. APMIS 107:11-18
Sugiura Y, Shimada H, Seeger RC et al (1998) Matrix Metalloproteinases-2 and −9 Are Expressed in Human Neuroblastoma: Contribution of Stromal Cells to Their Production and Correlation with Metastasis. Cancer Res 58:2209-2216
Sakakibara M, Koizumi S, Saikawa Y et al (1999) Membrane-type matrix metalloproteinase-1 expression and activation of gelatinase A as prognostic markers in advanced pediatric neuroblastoma. Cancer 85:231-239
Spurbeck WW, Ng CYC, Vanin EF et al (2003) Retroviral vector-producer cell-mediated in vivo gene transfer of TIMP-3 restricts angiogenesis and neuroblastoma growth in mice. Cancer Gene Ther 10:161-167
Papi A, Ferreri AM, Rocchi P et al (2010) Epigenetic Modifiers as Anticancer Drugs: Effectiveness of Valproic Acid in Neural Crest-derived Tumor Cells. Anticancer Res 30:535-540
Karafiat V, Dvorakova M, Krejci E et al (2005) Transcription factor c-Myb is involved in the regulation of the epithelial-mesenchymal transition in the avian neural crest. Cell Mol Life Sci 62:2516-25
Bailey CM, Morrison JA, Kulesa PM (2012) Melanoma revives an embryonic migration program to promote plasticity and invasion. Pigment Cell & Melanoma Res 25:573-283
Bailey CM, Morrison JA, Kulesa PM (2008) Molecular analysis of neural crest migration. Phil Trans R Soci B Biol Sci 363:1349-1362
Przybylo JA, Radisky DC (2007) Matrix metalloproteinase-induced epithelial-mesenchymal transition: tumor progression at Snail’s pace. Int J Biochem Cell Biol 39:1082-1088
Cano A, Perez-Moreno MA, Rodrigo I et al (2000) The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat Cell Biol 2:76-83
Nieto MA (2002) The snail superfamily of zinc-finger transcription factors. Nat Rev Mol Cell Biol 3:155-166
Munshi HG, Stack MS (2006) Reciprocal interactions between adhesion receptor signaling and MMP regulation. Cancer Metastasis Rev 25:45-56
Miyoshi A, Kitajima Y, Kido S et al (2005) Snail accelerates cancer invasion by upregulating MMP expression and is associated with poor prognosis of hepatocellular carcinoma. Br J Cancer 92:252-258
Radisky DC, Levy DD, Littlepage LE et al (2005) Rac1b and reactive oxygen species mediate MMP-3-induced EMT and genomic instability. Nature 436:123-127
Reiss K, Saftig P (2009) The “a disintegrin and metalloprotease” (ADAM) family of sheddases: physiological and cellular functions. Semin Cell Dev Biol 20:126-137
Edwards DR, Handsley MM, Pennington CJ (2008) The ADAM metalloproteinases. Mol Aspects Med 29:258-289
Puente XS, Lopez-Otin C (2004) A genomic analysis of rat proteases and protease inhibitors. Genome Res 14:609-622
Weber S, Saftig P (2012) Ectodomain shedding and ADAMs in development. Development 139:3693-3709
Alfandari D, McCusker C, Cousin H (2009) ADAM function in embryogenesis. Semin Cell Dev Biol 20:153-163
Becherer JD, Blobel CP (2003) Biochemical properties and functions of membrane-anchored metalloprotease-disintegrin proteins (ADAMs). Curr Top Dev Biol 54: 101-123
Andersson ER, Sandberg R, Lendahl U (2011) Notch signaling: simplicity in design, versatility in function. Development 138:3593-3612.
Ferber EC, Kajita M, Wadlow A et al (2008) A role for the cleaved cytoplasmic domain of E-cadherin in the nucleus. J Biol Chem 283:12691-12700
Maretzky T, Reiss K, Ludwig A et al (2005) ADAM10 mediates E-cadherin shedding and regulates epithelial cell-cell adhesion, migration, and beta-catenin translocation. Proc Natl Acad Sci USA 102:9182-9187
Reiss K, Maretzky T, Ludwig A et al (2005) ADAM10 cleavage of N-cadherin and regulation of cell-cell adhesion and beta-catenin nuclear signalling. EMBO J 24: 742-752.
Shoval I, Ludwig A, Kalcheim C (2007) Antagonistic roles of full-length N-cadherin and its soluble BMP cleavage product in neural crest delamination. Development 134:491-501
McCusker C, Cousin H, Neuner R et a (2009) Extracellular cleavage of cadherin-11 by ADAM metalloproteases is essential for Xenopus cranial neural crest cell migration. Mol Biol Cell 20:78-89
Hall RJ, Erickson CA (2003) ADAM 10: an active metalloprotease expressed during avian epithelial morphogenesis. Dev Biol 256:146-159
Lin J, Luo J, Redies C (2010) Molecular characterization and expression analysis of ADAM12 during chicken embryonic development. Dev Growth Differ 52:757-769
Lin J, Yan X, Markus A et al (2010) Expression of seven members of the ADAM family in developing chicken spinal cord. Dev Dyn 239:1246-1254
Alfandari D, Wolfsberg TG, White JM et al (1997) ADAM 13: A Novel ADAM Expressed in Somitic Mesoderm and Neural Crest Cells during Xenopus laevis Development. Dev Biol 182:314-330
Cai H, Kratzschmar J, Alfandari D et al (1998) Neural crest-specific and general expression of distinct metalloprotease-disintegrins in early Xenopus laevis development. Dev Biol 204:508-524
Hartmann D, de Strooper B, Serneels L et al (2002) The disintegrin/metalloprotease ADAM 10 is essential for Notch signalling but not for alpha-secretase activity in fibroblasts. Hum Mol Genet 11:2615-2624
Uemura K, Kihara T, Kuzuya A et al (2006) Characterization of sequential N-cadherin cleavage by ADAM10 and PS1. Neurosci Lett 402:278-283
Fortini ME (2002) Gamma-secretase-mediated proteolysis in cell-surface-receptor signalling. Nat Rev Mol Cell Biol 3:673-684
Marambaud P, Wen PH, Dutt A et al (2003) A CBP binding transcriptional repressor produced by the PS1/epsilon-cleavage of N-cadherin is inhibited by PS1 FAD mutations. Cell 114:635-645
Neuner R, Cousin H, McCusker C et al (2009) Xenopus ADAM19 is involved in neural, neural crest and muscle development. Mech Dev 126:240-255
Wei S, Xu G, Bridges LC et al (2010) ADAM13 Induces Cranial Neural Crest by Cleaving Class B Ephrins and Regulating Wnt Signaling. Dev Cell 19:345-352
Cousin H, Abbruzzese G, McCusker C et al (2012) ADAM13 function is required in the 3 dimensional context of the embryo during cranial neural crest cell migration in Xenopus laevis. Dev Biol 368:335-344
Cousin Hln, Abbruzzese G, Kerdavid E et al (2011) Translocation of the Cytoplasmic Domain of ADAM13 to the Nucleus Is Essential for Calpain8-a Expression and Cranial Neural Crest Cell Migration. Dev Cell 20:256-263
Valinsky JE, Le Douarin NM (1985) Production of plasminogen activator by migrating cephalic neural crest cells. Embo J 4:1403-1406
Agrawal M, Brauer PR (1996) Urokinase-type plasminogen activator regulates cranial neural crest cell migration in vitro. Dev Dyn 207:281-290
Murphy G, Stanton H, Cowell S et al (1999) Mechanisms for pro matrix metalloproteinase activation. APMIS 107:38-44
González-Cuevas J, Bueno-Topete M, Armendariz-Borunda J (2006) Urokinase plasminogen activator stimulates function of active forms of stromelysin and gelatinases (MMP-2 and MMP-9) in cirrhotic tissue. J Gastroenterol Hepatol 21:1544-1554
Kim K, Lee YA, Choi H et al (2012) Implication of MMP-9 and urokinase plasminogen activator (uPA) in the activation of pro-matrix metalloproteinase (MMP)-13. Rheumatol Int 32:3069-3075
Wee Yong V, Forsyth PA, Bell R et al (1998) Matrix metalloproteinases and diseases of the CNS. Trends Neurosci 21:75-80
Arscott WT, LaBauve AE, May V et al (2008) Suppression of neuroblastoma growth by dipeptidyl peptidase IV: relevance of chemokine regulation and caspase activation. Oncogene 28:479-491
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We are grateful to Dr. Yuval Peretz for his assistance in the graphical illustrations.
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Bar, A., Shoval, I., Monsonego-Ornan, E., Sela-Donenfeld, D. (2014). The Role of Proteases in Embryonic Neural Crest Cells. In: Dhalla, N., Chakraborti, S. (eds) Role of Proteases in Cellular Dysfunction. Advances in Biochemistry in Health and Disease, vol 8. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-9099-9_6
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