Loss of Bace2 in zebrafish affects melanocyte migration and is distinct from Bace1 knock out phenotypes

Journal of Neurochemistry

Volumn 127, Issue 4, 2013, Pages 471-481

  Van Bebber, Frauke ^a   Hruscha, Alexander ^a   Willem, Michael ^a   Schmid, Bettina ^a,b   Haass, Christian ^a,b  

^a UNIVERSITY OF MUNICH   (Germany)

^b Germany 3 Munich Cluster for Systems Neurology   (Germany)

Author keywords

Alzheimer's disease; BACE; myelination; zebrafish

Indexed keywords

BETA SECRETASE 1; BETA SECRETASE 2; ZINC FINGER PROTEIN;

ARTICLE; BACE1 GENE; BACE2 GENE; CELL MIGRATION; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; ENZYME INHIBITION; GENE; GENE MUTATION; GENE SEQUENCE; GENE SILENCING; GENETIC ASSOCIATION; HOMOZYGOSITY; IN VIVO STUDY; MELANOCYTE; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PERIPHERAL NERVOUS SYSTEM; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEPLETION; PROTEIN FUNCTION; SEQUENCE ANALYSIS; ZEBRA FISH;

ALZHEIMER'S DISEASE; BACE; MYELINATION; ZEBRAFISH;

AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; ANIMALS, GENETICALLY MODIFIED; CELL MOVEMENT; GENE KNOCKOUT TECHNIQUES; LARVA; MELANOCYTES; MODELS, ANIMAL; MUTATION; PHENOTYPE; ZEBRAFISH; ZEBRAFISH PROTEINS;

DANIO RERIO;

EID: 84887031752     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.12198     Document Type: Article

References (59)

1. Bennett B. D., Babu-Khan S., Loeloff R., Louis J. C., Curran E., Citron M., and, Vassar R., (2000) Expression analysis of BACE2 in brain and peripheral tissues. J. Biol. Chem. 275, 20647-20651.
2. Brinkmann B. G., Agarwal A., Sereda M. W., et al,. (2008) Neuregulin-1/ErbB signaling serves distinct functions in myelination of the peripheral and central nervous system. Neuron 59, 581-595.
3. Cai J., Qi X., Kociok N., et al,. (2012) beta-Secretase (BACE1) inhibition causes retinal pathology by vascular dysregulation and accumulation of age pigment. EMBO Mol. Med. 9, 980-981.
4. Citron M., (2002a) Beta-secretase as a target for the treatment of Alzheimer's disease. J. Neurosci. Res. 70, 373-379.
5. Citron M., (2002b) Emerging Alzheimer's disease therapies: inhibition of beta-secretase. Neurobiol. Aging 23, 1017-1022.
6. Dominguez D., Tournoy J., Hartmann D., et al,. (2005) Phenotypic and biochemical analyses of BACE1- and BACE2-deficient mice. J. Biol. Chem. 280, 30797-30806.
7. Falls D. L., (2003) Neuregulins and the neuromuscular system: 10 years of answers and questions. J. Neurocytol. 32, 619-647.
8. Farzan M., Schnitzler C. E., Vasilieva N., Leung D., and, Choe H., (2000) BACE2, a beta -secretase homolog, cleaves at the beta site and within the amyloid-beta region of the amyloid-beta precursor protein. Proc. Natl Acad. Sci. U S A 97, 9712-9717.
9. Geling A., Steiner H., Willem M., Bally-Cuif L., and, Haass C., (2002) A gamma-secretase inhibitor blocks Notch signaling in vivo and causes a severe neurogenic phenotype in zebrafish. EMBO Rep. 3, 688-694.
10. Gilmour D. T., Maischein H. M., and, Nusslein-Volhard C., (2002) Migration and function of a glial subtype in the vertebrate peripheral nervous system. Neuron 34, 577-588.
11. Haass C., (2004) Take five-BACE and the gamma-secretase quartet conduct Alzheimer's amyloid beta-peptide generation. EMBO J. 23, 483-488.
12. Haass C., and, Selkoe D. J., (2007) Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer's amyloid beta-peptide. Nat. Rev. Mol. Cell Biol. 8, 101-112.
13. Hardy J., (2009) The amyloid hypothesis for Alzheimer's disease: a critical reappraisal. J. Neurochem. 110, 1129-1134.
14. Hardy J., and, Selkoe D. J., (2002) The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 297, 353-356.
15. Harrison S. M., Harper A. J., Hawkins J., et al,. (2003) BACE1 (beta-secretase) transgenic and knockout mice: identification of neurochemical deficits and behavioral changes. Mol. Cell. Neurosci. 24, 646-655.
16. Hitt B., Riordan S. M., Kukreja L., Eimer W. A., Rajapaksha T. W., and, Vassar R., (2012) beta-Site amyloid precursor protein (APP)-cleaving enzyme 1 (BACE1)-deficient mice exhibit a close homolog of L1 (CHL1) loss-of-function phenotype involving axon guidance defects. J. Biol. Chem. 287, 38408-38425.
17. Hu X., Hicks C. W., He W., Wong P., Macklin W. B., Trapp B. D., and, Yan R., (2006) Bace1 modulates myelination in the central and peripheral nervous system. Nat. Neurosci. 9, 1520-1525.
18. Hu X., He W., Diaconu C., Tang X., Kidd G. J., Macklin W. B., Trapp B. D., and, Yan R., (2008) Genetic deletion of BACE1 in mice affects remyelination of sciatic nerves. FASEB J. 22, 2970-2980.
19. Hu X., Zhou X., He W., Yang J., Xiong W., Wong P., Wilson C. G., and, Yan R., (2010) BACE1 deficiency causes altered neuronal activity and neurodegeneration. J. Neurosci. 30, 8819-8829.
20. Hussain I., Powell D., Howlett D. R., et al,. (1999) Identification of a novel aspartic protease (Asp 2) as beta-secretase. Mol. Cell. Neurosci. 14, 419-427.
21. Kelsh R. N., Brand M., Jiang Y. J., et al,. (1996) Zebrafish pigmentation mutations and the processes of neural crest development. Development 123, 369-389.
22. Kim D. Y., Carey B. W., Wang H., et al,. (2007) BACE1 regulates voltage-gated sodium channels and neuronal activity. Nat. Cell Biol. 9, 755-764.
23. Kim D. Y., Gersbacher M. T., Inquimbert P., and, Kovacs D. M., (2011) Reduced sodium channel Na(v)1.1 levels in BACE1-null mice. J. Biol. Chem. 286, 8106-8116.
24. Kimmel C. B., Ballard W. W., Kimmel S. R., Ullmann B., and, Schilling T. F., (1995) Stages of embryonic development of the zebrafish. Dev. Dyn. 203, 253-310.
25. Kitazume S., Tachida Y., Oka R., Shirotani K., Saido T. C., and, Hashimoto Y., (2001) Alzheimer's beta-secretase, beta-site amyloid precursor protein-cleaving enzyme, is responsible for cleavage secretion of a Golgi-resident sialyltransferase. Proc. Natl Acad. Sci. U S A 98, 13554-13559.
26. Kotani N., Kitazume S., Kamimura K., Takeo S., Aigaki T., Nakato H., and, Hashimoto Y., (2005) Characterization of Drosophila aspartic proteases that induce the secretion of a Golgi-resident transferase, heparan sulfate 6-O-sulfotransferase. J. Biochem. 137, 315-322.
27. Kuhn P. H., Koroniak K., Hogl S., et al,. (2012) Secretome protein enrichment identifies physiological BACE1 protease substrates in neurons. EMBO J. 31, 3157-3168.
28. La Marca R., Cerri F., Horiuchi K., et al,. (2011) TACE (ADAM17) inhibits Schwann cell myelination. Nat. Neurosci. 14, 857-865.
29. Laird F. M., Cai H., Savonenko A. V., et al,. (2005) BACE1, a major determinant of selective vulnerability of the brain to amyloid-beta amyloidogenesis, is essential for cognitive, emotional, and synaptic functions. J. Neurosci. 25, 11693-11709.
30. Lichtenthaler S. F., Dominguez D. I., Westmeyer G. G., Reiss K., Haass C., Saftig P., De Strooper B., and, Seed B., (2003) The cell adhesion protein P-selectin glycoprotein ligand-1 is a substrate for the aspartyl protease BACE1. J. Biol. Chem. 278, 48713-48719.
31. Lin X., Koelsch G., Wu S., Downs D., Dashti A., and, Tang J., (2000) Human aspartic protease memapsin 2 cleaves the beta-secretase site of beta-amyloid precursor protein. Proc. Natl Acad. Sci. U S A 97, 1456-1460.
32. Luo Y., Bolon B., Kahn S., et al,. (2001) Mice deficient in BACE1, the Alzheimer's beta-secretase, have normal phenotype and abolished beta-amyloid generation. Nat. Neurosci. 4, 231-232.
33. May P. C., Dean R. A., Lowe S. L., et al,. (2011) Robust central reduction of amyloid-beta in humans with an orally available, non-peptidic beta-secretase inhibitor. J. Neurosci. 31, 16507-16516.
34. Michailov G. V., Sereda M. W., Brinkmann B. G., et al,. (2004) Axonal neuregulin-1 regulates myelin sheath thickness. Science 304, 700-703.
35. Moussavi Nik S. H., Wilson L., Newman M., Croft K., Mori T. A., Musgrave I., and, Lardelli M., (2012) The BACE1-PSEN-AbetaPP regulatory axis has an ancient role in response to low oxygen/oxidative stress. J. Alzheimers Dis. 28, 515-530.
36. Munzel E. J., Schaefer K., Obirei B., et al,. (2012) Claudin k is specifically expressed in cells that form myelin during development of the nervous system and regeneration of the optic nerve in adult zebrafish. Glia 60, 253-270.
37. Ohno M., Sametsky E. A., Younkin L. H., Oakley H., Younkin S. G., Citron M., Vassar R., and, Disterhoft J. F., (2004) BACE1 deficiency rescues memory deficits and cholinergic dysfunction in a mouse model of Alzheimer's disease. Neuron 41, 27-33.
38. Perlin J. R., Lush M. E., Stephens W. Z., Piotrowski T., and, Talbot W. S., (2011) Neuronal neuregulin 1 type III directs Schwann cell migration. Development 138, 4639-4648.
39. Rajapaksha T. W., Eimer W. A., Bozza T. C., and, Vassar R., (2011) The Alzheimer's beta-secretase enzyme BACE1 is required for accurate axon guidance of olfactory sensory neurons and normal glomerulus formation in the olfactory bulb. Mol. Neurodegener. 6, 88.
40. Roberds S. L., Anderson J., Basi G., et al,. (2001) BACE knockout mice are healthy despite lacking the primary beta-secretase activity in brain: implications for Alzheimer's disease therapeutics. Hum. Mol. Genet. 10, 1317-1324.
41. Saunders A. J., Kim T. W., and, Tanzi R. E., (1999) BACE maps to chromosome 11 and a BACE homolog, BACE2, reside in the obligate down syndrome region of chromosome 21. Science, 286, 1255a.
42. Selkoe D. J., (2001) Alzheimer's disease: genes, proteins, and therapy. Physiol. Rev. 81, 741-766.
43. Sinha S., Anderson J. P., Barbour R., et al,. (1999) Purification and cloning of amyloid precursor protein beta-secretase from human brain. Nature 402, 537-540.
44. Stachel S. J., Coburn C. A., Steele T. G., et al,. (2004) Structure-based design of potent and selective cell-permeable inhibitors of human beta-secretase (BACE-1). J. Med. Chem. 47, 6447-6450.
45. Taveggia C., Zanazzi G., Petrylak A., et al,. (2005) Neuregulin-1 type III determines the ensheathment fate of axons. Neuron 47, 681-694.
46. Thisse B., and, Thisse C., (2004) Fast release clones: a high throughput expression analysis. ZFIN Direct Data Submission, .
47. Urnov F. D., Rebar E. J., Holmes M. C., Zhang H. S., and, Gregory P. D., (2010) Genome editing with engineered zinc finger nucleases. Nat. Rev. Genet. 11, 636-646.
48. Van Trump W. J., and, McHenry M. J., (2008) The morphology and mechanical sensitivity of lateral line receptors in zebrafish larvae (Danio rerio). J. Exp. Biol. 211, 2105-2115.
49. Vassar R., (2001) The beta-secretase, BACE: a prime drug target for Alzheimer's disease. J. Mol. Neurosci. 17, 157-170.
50. Vassar R., (2002) Beta-secretase (BACE) as a drug target for Alzheimer's disease. Adv. Drug Deliv. Rev. 54, 1589-1602.
51. Vassar R., and, Citron M., (2000) Abeta-generating enzymes: recent advances in beta- and gamma-secretase research. Neuron 27, 419-422.
52. Vassar R., Bennett B. D., Babu-Khan S., et al,. (1999) Beta-secretase cleavage of Alzheimer's amyloid precursor protein by the transmembrane aspartic protease BACE. Science 286, 735-741.
53. Velanac V., Unterbarnscheidt T., Hinrichs W., et al,. (2012) Bace1 processing of NRG1 type III produces a myelin-inducing signal but is not essential for the stimulation of myelination. Glia 60, 203-217.
54. Walter J., Fluhrer R., Hartung B., Willem M., Kaether C., Capell A., Lammich S., Multhaup G., and, Haass C., (2001) Phosphorylation regulates intracellular trafficking of beta-secretase. J. Biol. Chem. 276, 14634-14641.
55. Willem M., Garratt A. N., Novak B., et al,. (2006) Control of peripheral nerve myelination by the beta-secretase BACE1. Science 314, 664-666.
56. Wong H. K., Sakurai T., Oyama F., et al,. (2005) beta Subunits of voltage-gated sodium channels are novel substrates of beta-site amyloid precursor protein-cleaving enzyme (BACE1) and gamma-secretase. J. Biol. Chem. 280, 23009-23017.
57. Yan R., Bienkowski M. J., Shuck M. E., et al,. (1999) Membrane-anchored aspartyl protease with Alzheimer's disease beta-secretase activity. Nature 402, 533-537.
58. Zhao J., Fu Y., Yasvoina M., et al,. (2007) Beta-site amyloid precursor protein cleaving enzyme 1 levels become elevated in neurons around amyloid plaques: implications for Alzheimer's disease pathogenesis. J. Neurosci. 27, 3639-3649.
59. Zhou L., Barao S., Laga M., et al,. (2012) The neural cell adhesion molecules L1 and CHL1 are cleaved by BACE1 protease in vivo. J. Biol. Chem. 287, 25927-25940.