ADAM10 mediates N-cadherin ectodomain shedding during retinal ganglion cell differentiation in primary cultured retinal cells from the developing chick retina

Journal of Cellular Biochemistry

Volumn 114, Issue 4, 2013, Pages 942-954

  Paudel, Sharada ^a   Kim, Yeoun Hee ^a,b   Huh, Man Il ^a   Kim, Song Ja ^c   Chang, Yongmin ^a   Park, Young Jeung ^b   Lee, Kyoo Won ^b   Jung, Jae Chang ^a  

^a Kyungpook National University   (South Korea)

^b Cheil Eye Hospital   (South Korea)

^c Kongju National University   (South Korea)

Author keywords

ADAM10; DIFFERENTIATION; N CADHERIN; Pax6; RETINAL DEVELOPMENT; RETINAL GANGLION CELL (RGC)

Indexed keywords

ADAM10 ENDOPEPTIDASE; NERVE CELL ADHESION MOLECULE; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR PAX6;

ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; PHASE CONTRAST MICROSCOPY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; RETINA GANGLION CELL; RNA INTERFERENCE; WESTERN BLOTTING;

ADAM PROTEINS; ANIMALS; BLOTTING, WESTERN; CADHERINS; CELL DIFFERENTIATION; CELLS, CULTURED; CHICK EMBRYO; CHICKENS; CULTURE MEDIA, CONDITIONED; DIPEPTIDES; EYE PROTEINS; GENE EXPRESSION REGULATION; HOMEODOMAIN PROTEINS; HYDROXAMIC ACIDS; MICROSCOPY, PHASE-CONTRAST; NERVE TISSUE PROTEINS; NEURITES; PAIRED BOX TRANSCRIPTION FACTORS; PRIMARY CELL CULTURE; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; REPRESSOR PROTEINS; RETINA; RETINAL CONE PHOTORECEPTOR CELLS; RETINAL GANGLION CELLS; RNA, SMALL INTERFERING;

EID: 84874228253     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.24435     Document Type: Article

References (78)

1. Adler R,. 2000. A model of retinal cell differentiation in the chick embryo. Prog Retin Eye Res 19: 529-557.
2. Agathocleous M, Harris WA,. 2009. From progenitors to differentiated cells in the vertebrate retina. Annu Rev Cell Dev Biol 25: 45-69.
3. Ahmad I, Dooley CM, Polk DL,. 1997. Delta-1 is a regulator of neurogenesis in the vertebrate retina. Dev Biol 185: 92-103.
4. Alfandari D, McCusker C, Cousin H,. 2009. ADAM function in embryogenesis. Semin Cell Dev Biol 20: 153-163.
5. Andrews GL, Mastick GS,. 2003. R-cadherin is a Pax6-regulated, growth-promoting cue for pioneer axons. J Neurosci 23: 9873-9880.
6. Austin CP, Feldman DE, Ida JA, Jr., Cepko CL,. 1995. Vertebrate retinal ganglion cells are selected from competent progenitors by the action of Notch. Development 121: 3637-3650.
7. Bixby JL, Zhang R,. 1990. Purified N-cadherin is a potent substrate for the rapid induction of neurite outgrowth. J Cell Biol 110: 1253-1260.
8. 2+ influx and neurite growth in response to purified N-cadherin and laminin. J Cell Biol 127: 1461-1475.
9. Bozkulak EC, Weinmaster G,. 2009. Selective use of ADAM10 and ADAM17 in activation of Notch1 signaling. Mol Cell Biol 29: 5679-5695.
10. Canto-Soler MV, Huang H, Romero MS, Adler R,. 2008. Transcription factors CTCF and Pax6 are segregated to different cell types during retinal cell differentiation. Dev Dyn 237: 758-767.
11. Chen YY, Hehr CL, Atkinson-Leadbeater K, Hocking JC, McFarlane S,. 2007. Targeting of retinal axons requires the metalloproteinase ADAM10. J Neurosci 27: 8448-8456.
12. Chow RL, Altmann CR, Lang RA, Hemmati-Brivanlou A,. 1999. Pax6 induces ectopic eyes in a vertebrate. Development 126: 4213-4222.
13. Conroy WG, Ogden LF, Berg DK,. 2000. Cluster formation of alpha7-containing nicotinic receptors at interneuronal interfaces in cell culture. Neuropharmacology 39: 2699-2705.
14. Dallas DJ, Genever PG, Patton AJ, Millichip MI, McKie N, Skerry TM,. 1999. Localization of ADAM10 and Notch receptors in bone. Bone 25: 9-15.
15. Duffy MJ, McKiernan E, O'Donovan N, McGowan PM,. 2009. Role of ADAMs in cancer formation and progression. Clin Cancer Res 15: 1140-1144.
16. Edwards DR, Handsley MM, Pennington CJ,. 2008. The ADAM metalloproteinases. Mol Aspects Med 29: 258-289.
17. Engelkamp D, Rashbass P, Seawright A, van Heyningen V,. 1999. Role of Pax6 in development of the cerebellar system. Development 126: 3585-3596.
18. Escrevente C, Morais VA, Keller S, Soares CM, Altevogt P, Costa J,. 2008. Functional role of N-glycosylation from ADAM10 in processing, localization and activity of the enzyme. Biochim Biophys Acta 1780: 905-913.
19. Esteve P, Sandonis A, Cardozo M, Malapeira J, Ibanez C, Crespo I, Marcos S, Gonzalez-Garcia S, Toribio ML, Arribas J, Shimono A, Guerrero I, Bovolenta P,. 2011. SFRPs act as negative modulators of ADAM10 to regulate retinal neurogenesis. Nat Neurosci 14: 562-569.
20. Fanarraga ML, Avila J, Zabala JC,. 1999. Expression of unphosphorylated class III beta-tubulin isotype in neuroepithelial cells demonstrates neuroblast commitment and differentiation. Eur J Neurosci 11: 517-527.
21. Ferreiro-Galve S, Rodriguez-Moldes I, Anadon R, Candal E,. 2010. Patterns of cell proliferation and rod photoreceptor differentiation in shark retinas. J Chem Neuroanat 39: 1-14.
22. Ferreiro-Galve S, Rodriguez-Moldes I, Candal E,. 2011. Pax6 expression during retinogenesis in sharks: Comparison with markers of cell proliferation and neuronal differentiation. J Exp Zool B Mol Dev Evol 318: 91-108.
23. Glomski K, Monette S, Manova K, De Strooper B, Saftig P, Blobel CP,. 2011. Deletion of Adam10 in endothelial cells leads to defects in organ-specific vascular structures. Blood 118: 1163-1174.
24. Gotz M, Stoykova A, Gruss P,. 1998. Pax6 controls radial glia differentiation in the cerebral cortex. Neuron 21: 1031-1044.
25. Gumbiner BM,. 1996. Cell adhesion: The molecular basis of tissue architecture and morphogenesis. Cell 84: 345-357.
26. Hall RJ, Erickson CA,. 2003. ADAM 10: An active metalloprotease expressed during avian epithelial morphogenesis. Dev Biol 256: 146-159.
27. Hansen SM, Berezin V, Bock E,. 2008. Signaling mechanisms of neurite outgrowth induced by the cell adhesion molecules NCAM and N-cadherin. Cell Mol Life Sci 65: 3809-3821.
28. Henrique D, Hirsinger E, Adam J, Le Roux I, Pourquie O, Ish-Horowicz D, Lewis J,. 1997. Maintenance of neuroepithelial progenitor cells by Delta-Notch signalling in the embryonic chick retina. Curr Biol 7: 661-670.
29. Holst BD, Wang Y, Jones FS, Edelman GM,. 1997. A binding site for Pax proteins regulates expression of the gene for the neural cell adhesion molecule in the embryonic spinal cord. Proc Natl Acad Sci USA 94: 1465-1470.
30. Hsieh YW, Yang XJ,. 2009. Dynamic Pax6 expression during the neurogenic cell cycle influences proliferation and cell fate choices of retinal progenitors. Neural Dev 4: 32.
31. Huh MI, Lee YM, Seo SK, Kang BS, Chang Y, Lee YS, Fini ME, Kang SS, Jung JC,. 2007. Roles of MMP/TIMP in regulating matrix swelling and cell migration during chick corneal development. J Cell Biochem 101: 1222-1237.
32. Huntley GW,. 2002. Dynamic aspects of cadherin-mediated adhesion in synapse development and plasticity. Biol Cell 94: 335-344.
33. Inuzuka H, Miyatani S, Takeichi M,. 1991a. R-cadherin: A novel Ca(2+)-dependent cell-cell adhesion molecule expressed in the retina. Neuron 7: 69-79.
34. Inuzuka H, Redies C, Takeichi M,. 1991b. Differential expression of R- and N-cadherin in neural and mesodermal tissues during early chicken development. Development 113: 959-967.
35. Jorissen E, Prox J, Bernreuther C, Weber S, Schwanbeck R, Serneels L, Snellinx A, Craessaerts K, Thathiah A, Tesseur I, Bartsch U, Weskamp G, Blobel CP, Glatzel M, De Strooper B, Saftig P,. 2010. The disintegrin/metalloproteinase ADAM10 is essential for the establishment of the brain cortex. J Neurosci 30: 4833-4844.
36. Karkkainen I, Rybnikova E, Pelto-Huikko M, Huovila AP,. 2000. Metalloprotease-disintegrin (ADAM) genes are widely and differentially expressed in the adult CNS. Mol Cell Neurosci 15: 547-560.
37. Kim YH, Chang Y, Jung JC,. 2012. Staurosporine induces ganglion cell differentiation in part by stimulating urokinase-type plasminogen activator expression and activation in the developing chick retina. Biochem Biophys Res Commun 423: 67-72.
38. Kohutek ZA, diPierro CG, Redpath GT, Hussaini IM,. 2009. ADAM-10-mediated N-cadherin cleavage is protein kinase C-alpha dependent and promotes glioblastoma cell migration. J Neurosci 29: 4605-4615.
39. Lin J, Luo J, Redies C,. 2008. Differential expression of five members of the ADAM family in the developing chicken brain. Neuroscience 157: 360-375.
40. Liu X, Mizoguchi A, Takeichi M, Honda Y, Ide C,. 1997. Developmental changes in the subcellular localization of R-cadherin in chick retinal pigment epithelium. Histochem Cell Biol 108: 35-43.
41. Markus A, Yan X, Rolfs A, Luo J,. 2011. Quantitative and dynamic expression profile of premature and active forms of the regional ADAM proteins during chicken brain development. Cell Mol Biol Lett 16: 431-451.
42. Masai I, Lele Z, Yamaguchi M, Komori A, Nakata A, Nishiwaki Y, Wada H, Tanaka H, Nojima Y, Hammerschmidt M, Wilson SW, Okamoto H,. 2003. N-cadherin mediates retinal lamination, maintenance of forebrain compartments and patterning of retinal neurites. Development 130: 2479-2494.
43. Matsunaga M, Hatta K, Takeichi M,. 1988. Role of N-cadherin cell adhesion molecules in the histogenesis of neural retina. Neuron 1: 289-295.
44. McCulloch DR, Akl P, Samaratunga H, Herington AC, Odorico DM,. 2004. Expression of the disintegrin metalloprotease, ADAM-10, in prostate cancer and its regulation by dihydrotestosterone, insulin-like growth factor I, and epidermal growth factor in the prostate cancer cell model LNCaP. Clin Cancer Res 10: 314-323.
45. McCusker CD, Alfandari D,. 2009. Life after proteolysis: Exploring the signaling capabilities of classical cadherin cleavage fragments. Commun Integr Biol 2: 155-157.
46. Millichip MI, Dallas DJ, Wu E, Dale S, McKie N,. 1998. The metallo-disintegrin ADAM10 (MADM) from bovine kidney has type IV collagenase activity in vitro. Biochem Biophys Res Commun 245: 594-598.
47. Mu X, Klein WH,. 2004. A gene regulatory hierarchy for retinal ganglion cell specification and differentiation. Semin Cell Dev Biol 15: 115-123.
48. Nagano O, Murakami D, Hartmann D, De Strooper B, Saftig P, Iwatsubo T, Nakajima M, Shinohara M, Saya H,. 2004. 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 165: 893-902.
49. Nakagawa S, Takeichi M,. 1998. Neural crest emigration from the neural tube depends on regulated cadherin expression. Development 125: 2963-2971.
50. Oron-Karni V, Farhy C, Elgart M, Marquardt T, Remizova L, Yaron O, Xie Q, Cvekl A, Ashery-Padan R,. 2008. Dual requirement for Pax6 in retinal progenitor cells. Development 135: 4037-4047.
51. Paradies NE, Grunwald GB,. 1993. Purification and characterization of NCAD90, a soluble endogenous form of N-cadherin, which is generated by proteolysis during retinal development and retains adhesive and neurite-promoting function. J Neurosci Res 36: 33-45.
52. Philips GT, Stair CN, Young Lee H, Wroblewski E, Berberoglu MA, Brown NL, Mastick GS,. 2005. Precocious retinal neurons: Pax6 controls timing of differentiation and determination of cell type. Dev Biol 279: 308-321.
53. Pimentel B, Sanz C, Varela-Nieto I, Rapp UR, De Pablo F, de La Rosa EJ,. 2000. c-Raf regulates cell survival and retinal ganglion cell morphogenesis during neurogenesis. J Neurosci 20: 3254-3262.
54. Prada C, Puelles L, Genis-Galvez JM,. 1981. A golgi study on the early sequence of differentiation of ganglion cells in the chick embryo retina. Anat Embryol (Berl) 161: 305-317.
55. Puschel AW, Gruss P, Westerfield M,. 1992. Sequence and expression pattern of pax-6 are highly conserved between zebrafish and mice. Development 114: 643-651.
56. Radice GL, Rayburn H, Matsunami H, Knudsen KA, Takeichi M, Hynes RO,. 1997. Developmental defects in mouse embryos lacking N-cadherin. Dev Biol 181: 64-78.
57. 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.
58. Reiss K, Maretzky T, Ludwig A, Tousseyn T, de Strooper B, Hartmann D, Saftig P,. 2005. ADAM10 cleavage of N-cadherin and regulation of cell-cell adhesion and beta-catenin nuclear signalling. EMBO J 24: 742-752.
59. Riesenberg AN, Liu Z, Kopan R, Brown NL,. 2009. Rbpj cell autonomous regulation of retinal ganglion cell and cone photoreceptor fates in the mouse retina. J Neurosci 29: 12865-12877.
60. Rooke J, Pan D, Xu T, Rubin GM,. 1996. KUZ, a conserved metalloprotease-disintegrin protein with two roles in Drosophila neurogenesis. Science 273: 1227-1231.
61. Rosdahl JA, Mourton TL, Brady-Kalnay SM,. 2002. Protein kinase C delta (PKCdelta) is required for protein tyrosine phosphatase mu (PTPmu)-dependent neurite outgrowth. Mol Cell Neurosci 19: 292-306.
62. Rungger-Brandle E, Ripperger JA, Steiner K, Conti A, Stieger A, Soltanieh S, Rungger D,. 2010. Retinal patterning by Pax6-dependent cell adhesion molecules. Dev Neurobiol 70: 764-780.
63. Saga T, Scheurer D, Adler R,. 1996. Development and maintenance of outer segments by isolated chick embryo photoreceptor cells in culture. Invest Ophthalmol Vis Sci 37: 561-573.
64. Sahin U, Weskamp G, Kelly K, Zhou HM, Higashiyama S, Peschon J, Hartmann D, Saftig P, Blobel CP,. 2004. Distinct roles for ADAM10 and ADAM17 in ectodomain shedding of six EGFR ligands. J Cell Biol 164: 769-779.
65. Schulte D, Bumsted-O'Brien KM,. 2008. Molecular mechanisms of vertebrate retina development: Implications for ganglion cell and photoreceptor patterning. Brain Res 1192: 151-164.
66. Sebastian-Serrano A, Sandonis A, Cardozo M, Rodriguez-Tornos FM, Bovolenta P, Nieto M,. 2012. Pax6 expression in postmitotic neurons mediates the growth of axons in response to SFRP1. PLoS ONE 7: e31590.
67. Shaham O, Menuchin Y, Farhy C, Ashery-Padan R,. 2012. Pax6: A multi-level regulator of ocular development. Prog Retin Eye Res 31: 351-376.
68. Snow RL, Robson JA,. 1994. Ganglion cell neurogenesis, migration and early differentiation in the chick retina. Neuroscience 58: 399-409.
69. Stoykova A, Gotz M, Gruss P, Price J,. 1997. Pax6-dependent regulation of adhesive patterning, R-cadherin expression and boundary formation in developing forebrain. Development 124: 3765-3777.
70. Tanaka H, Yamashita T, Asada M, Mizutani S, Yoshikawa H, Tohyama M,. 2002. Cytoplasmic p21(Cip1/WAF1) regulates neurite remodeling by inhibiting Rho-kinase activity. J Cell Biol 158: 321-329.
71. Walther C, Gruss P,. 1991. Pax-6, a murine paired box gene, is expressed in the developing CNS. Development 113: 1435-1449.
72. Watanabe M, Rutishauser U, Silver J,. 1991. Formation of the retinal ganglion cell and optic fiber layers. J Neurobiol 22: 85-96.
73. White JM,. 2003. ADAMs: Modulators of cell-cell and cell-matrix interactions. Curr Opin Cell Biol 15: 598-606.
74. Wohrn JC, Puelles L, Nakagawa S, Takeichi M, Redies C,. 1998. Cadherin expression in the retina and retinofugal pathways of the chicken embryo. J Comp Neurol 396: 20-38.
75. Wolfsberg TG, Primakoff P, Myles DG, White JM,. 1995. ADAM, a novel family of membrane proteins containing A Disintegrin And Metalloprotease domain: Multipotential functions in cell-cell and cell-matrix interactions. J Cell Biol 131: 275-278.
76. Yamasaki T, Kawaji K, Ono K, Bito H, Hirano T, Osumi N, Kengaku M,. 2001. Pax6 regulates granule cell polarization during parallel fiber formation in the developing cerebellum. Development 128: 3133-3144.
77. Yan X, Lin J, Rolfs A, Luo J,. 2011. Differential expression of the ADAMs in developing chicken retina. Dev Growth Differ 53: 726-739.
78. Yang P, Baker KA, Hagg T,. 2006. The ADAMs family: Coordinators of nervous system development, plasticity and repair. Prog Neurobiol 79: 73-94.