Golden Retriever dogs with neuronal ceroid lipofuscinosis have a two-base-pair deletion and frameshift in CLN5

Molecular Genetics and Metabolism

Volumn 115, Issue 2-3, 2015, Pages 101-109

  Gilliam, D ^a   Kolicheski, A ^a   Johnson, G S ^a   Mhlanga Mutangadura, T ^a   Taylor, J F ^a   Schnabel, R D ^a   Katz, M L ^b  

^a UNIVERSITY OF MISSOURI   (United States)

^b University of Missouri   (United States)

Author keywords

Batten disease; Canine model; CLN5 mutation; Lysosomal storage disease; Neurodegeneration; Neuronal ceroid lipofuscinosis; Whole genome sequence

Indexed keywords

AGGRESSION; ALLELE; ANIMAL TISSUE; ANXIETY; ARTICLE; ATAXIA; BRAIN CELL; BRAIN CORTEX; CANINE MODEL; CEREBELLUM; CIRCLING BEHAVIOR; CLN5 GENE; CONTROLLED STUDY; FRAMESHIFT MUTATION; GENE; GENE DELETION; GOLDEN RETRIEVER; HETEROZYGOTE; HOMOZYGOTE; INDEL MUTATION; MISSENSE MUTATION; NEURONAL CEROID LIPOFUSCINOSIS; NONHUMAN; ONSET AGE; PRIORITY JOURNAL; PURKINJE CELL; RETINA; STOP CODON; TONIC CLONIC SEIZURE; TREMOR; VISUAL IMPAIRMENT; ANIMAL; DNA SEQUENCE; DOG; DOG DISEASE; GENETICS; NUCLEOTIDE SEQUENCE; VETERINARY;

CANIS FAMILIARIS;

MEMBRANE PROTEIN;

ANIMALS; BASE SEQUENCE; DOG DISEASES; DOGS; FRAMESHIFT MUTATION; HOMOZYGOTE; MEMBRANE PROTEINS; NEURONAL CEROID-LIPOFUSCINOSES; SEQUENCE ANALYSIS, DNA; SEQUENCE DELETION;

EID: 84930180000     PISSN: 10967192     EISSN: 10967206     Source Type: Journal    
DOI: 10.1016/j.ymgme.2015.04.001     Document Type: Article

References (54)

1. Haltia M., Goebel H.H. The neuronal ceroid-lipofuscinoses: a historical introduction. Biochim. Biophys. Acta 2013 Nov, 1832(11):1795-1800. (Epub 2012 Aug 29). 10.1016/j.bbadis.2012.08.012.
2. Anderson G.W., Goebel H.H., Simonati A. Human pathology in NCL. Biochim. Biophys. Acta 2013 Nov, 1832(11):1807-1826. (Epub 2012 Nov 29). 10.1016/j.bbadis.2012.11.014.
3. Mink J.W., Augustine E.F., Adams H.R., Marshall F.J., Kwon J.M. Genetic basis and phenotypic correlations of the neuronal ceroid lipofusinoses. J. Child Neurol. 2013 Sep, 28(9):1101-1105. (Epub 2013 Jul 9). 10.1177/0883073813494268.
4. Vesa J., Hellsten E., Verkruyse L.A., Camp L.A., Rapola J., Santavuori P., Hofmann S.L., Peltonen L. Mutations in the palmitoyl protein thioesterase gene causing infantile neuronal ceroid lipofuscinosis. Nature 1995 Aug 17, 376(6541):584-587.
5. The International Batten Disease Consortium Isolation of a novel gene underlying Batten disease, CLN3. The International Batten Disease Consortium. Cell 1995 Sep 22, 82(6):949-957.
6. Cotman S.L., Karaa A., Staropoli J.F., Sims K.B. Neuronal ceroid lipofuscinosis: impact of recent genetic advances and expansion of the clinicopathologic spectrum. Curr. Neurol. Neurosci. Rep. 2013 Aug, 13(8):366. 10.1007/s11910-013-0366-z.
7. Berkovic S.F., Carpenter S., Andermann F., Andermann E., Wolfe L.S. Kufs' disease: a critical reappraisal. Brain 1988 Feb, 111(Pt 1):27-62.
8. Williams RE. Appendix 1: NCL incidence and prevalence data. In:The Neuronal Ceroid Lipofuscinoses (Batten Disease) 2nd edition. Oxford University Press 2011 SE Mole, RE Williams, and HH Goebel editors.
9. Bond M., Holthaus S.M., Tammen I., Tear G., Russell C. Use of model organisms for the study of neuronal ceroid lipofuscinosis. Biochim. Biophys. Acta 2013 Nov, 1832(11):1842-1865. 10.1016/j.bbadis.2013.01.009.
10. Sanders D.N., Farias F.H., Johnson G.S., Chiang V., Cook J.R., O'Brien D.P., Hofmann S.L., Lu J.Y., Katz M.L. A mutation in canine PPT1 causes early onset neuronal ceroid lipofuscinosis in a Dachshund. Mol. Genet. Metab. 2010 Aug, 100(4):349-356. (Epub 2010 Apr 24). 10.1016/j.ymgme.2010.04.009.
11. Awano T., Katz M.L., O'Brien D.P., Sohar I., Lobel P., Coates J.R., Khan S., Johnson G.C., Giger U., Johnson G.S. A frame shift mutation in canine TPP1 (the ortholog of human CLN2) in a juvenile Dachshund with neuronal ceroid lipofuscinosis. Mol. Genet. Metab. 2006 Nov, 89(3):254-260. 10.1016/j.ymgme.2006.02.016.
12. Melville S.A., Wilson C.L., Chiang C.S., Studdert V.P., Lingaas F., Wilton A.N. A mutation in canine CLN5 causes neuronal ceroid lipofuscinosis in Border Collie dogs. Genomics 2005 Sep, 86(3):287-294. 10.1016/j.ygeno.2005.06.005.
13. Katz M.L., Farias F.H., Sanders D.N., Zeng R., Khan S., Johnson G.S., O'Brien D.P. A missense mutation in canine CLN6 in an Australian shepherd with neuronal ceroid lipofuscinosis. J. Biomed. Biotechnol. 2011, 2011:198042. (Epub 2010 Dec 22). 10.1155/2011/198042.
14. Guo J., Brien DP O., Mhlanga-Mutangadura T., Olby N.J., Taylor J.F., Schnabel R.D., Katz M.L., Johnson G.S. A rare homozygous MFSD8 single-base-pair deletion and frameshift in the whole genome sequence of a Chinese Crested dog with neuronal ceroid lipofuscinosis. BMC Vet. Res. 2015 Jan 3, 10(1):960. (Epub ahead of print). 10.1186/s12917-014-0181-z.
15. Katz M.L., Khan S., Awano T., Shahid S.A., Siakotos A.N., Johnson G.S. A mutation in the CLN8 gene in English Setter dogs with neuronal ceroid-lipofuscinosis. Biochem. Biophys. Res. Commun. 2005 Feb 11, 327(2):541-547. 10.1016/j.bbrc.2004.12.038.
16. Guo J., Johnson G.S., Brown H.A., Provencher M.L., da Costa R.C., Mhlanga-Mutangadura T., Taylor J.F., Schnabel R.D., O'Brien D.P., Katz M.L. A CLN8 nonsense mutation in the whole genome sequence of a mixed breed dog with neuronal ceroid lipofuscinosis and Australian Shepherd ancestry. Mol. Genet. Metab. 2014 Aug, 112(4):302-309. (Epub 2014 Jun 4). 10.1016/j.ymgme.2014.05.014.
17. Awano T., Katz M.L., O'Brien D.P., Taylor J.F., Evans J., Khan S., Sohar I., Lobel P., Johnson G.S. A mutation in the cathepsin D gene (CTSD) in American Bulldogs with neuronal ceroid lipofuscinosis. Mol. Genet. Metab. 2006 Apr, 87(4):341-348. 10.1016/j.ymgme.2005.11.005.
18. Farias F.H., Zeng R., Johnson G.S., Wininger F.A., Taylor J.F., Schnabel R.D., McKay S.D., Sanders D.N., Lohi H., Seppälä E.H., Wade C.M., Lindblad-Toh K., O'Brien D.P., Katz M.L. A truncating mutation in ATP13A2 is responsible for adult-onset neuronal ceroid lipofuscinosis in Tibetan terriers. Neurobiol. Dis. 2011 Jun, 42(3):468-474. 10.1016/j.nbd.2011.02.009.
19. Wöhlke A., Philipp U., Bock P., Beineke A., Lichtner P., Meitinger T., Distl O. A one base pair deletion in the canine ATP13A2 gene causes exon skipping and late-onset neuronal ceroid lipofuscinosis in the Tibetan terrier. PLoS Genet. 2011 Oct, 7(10):e1002304. 10.1371/journal.pgen.1002304.
20. Abitbol M., Thibaud J.L., Olby N.J., Hitte C., Puech J.P., Maurer M., Pilot-Storck F., Hédan B., Dréano S., Brahimi S., Delattre D., André C., Gray F., Delisle F., Caillaud C., Bernex F., Panthier J.J., Aubin-Houzelstein G., Blot S., Tiret L. A canine Arylsulfatase G (ARSG) mutation leading to a sulfatase deficiency is associated with neuronal ceroid lipofuscinosis. Proc. Natl. Acad. Sci. U. S. A. 2010 Aug 17, 107(33):14775-14780.
21. Kowalewski B., Lamanna W.C., Lawrence R., Damme M., Stroobants S., Padva M., Kalus I., Frese M.A., Lubke T., Lullmann-Rauch R., D'Hooge R., Esko J.D., Dierks T. Arylsulfatase G inactivation causes loss of heparan sulfate 3-O-sulfatase activity and mucopolysaccharidosis in mice. Proceedings of the National Academy of Sciences of the United States of America 2012 Jun 26, 109(26):10310-10315. 10.1073/pnas.1202071109.
22. Kowalewski B., Lubke T., Kollmann K., Braulke T., Reinheckel T., Dierks T., Damme M. Molecular characterization of arylsulfatase G: expression, processing, glycosylation, transport, and activity. J. Biol. Chem. 2014 Oct 3, 289(40):27992-28005. 10.1074/jbc.M114.584144.
23. Studdert V.P., Mitten R.W. Clinical features of ceroid lipofuscinosis in Border Collie dogs. Aust. Vet. J. 1991 Apr, 68(4):137-140.
24. Mizukami K., Kawamichi T., Koie H., Tamura S., Matsunaga S., Imamoto S., Saito M., Hasegawa D., Matsuki N., Tamahara S., Sato S., Yabuki A., Chang H.S., Yamato O. Neuronal ceroid lipofuscinosis in Border Collie dogs in Japan: clinical and molecular epidemiological study (2000-2011). Sci. World J. 2012, 2012:383174. 10.1100/2012/383174.
25. Kluth S., Eckardt J., Distl O. Selection response to DNA testing for canine ceroid lipofuscinosis in Tibetan terriers. Vet. J. 2014 Sep, 201(3):433-434. 10.1016/j.tvjl.2014.05.029.
26. Evans J., Katz M.L., Levesque D., Shelton G.D., de Lahunta A., O'Brien D. A variant form of neuronal ceroid lipofuscinosis in American bulldogs. J. Vet. Intern. Med. 2005 Jan-Feb, 19(1):44-51. 10.1111/j.1939-1676.2005.tb02657.x.
27. Vuillemenot B.R., Kennedy D., Cooper J.D., Wong A.M., Sri S., Doeleman T., Katz M.L., Coates J.R., Johnson G.C., Reed R.P., Adams E.L., Butt M.T., Musson D.G., Henshaw J., Keve S., Cahayag R., Tsuruda L.S., O'Neill C.A. Nonclinical evaluation of CNS-administered TPP1 enzyme replacement in canine CLN2 neuronal ceroid lipofuscinosis. Mol. Genet. Metab. 2015, 114(2):281-293.
28. Katz M.L., Coates J.R., Sibigtroth C.M., Taylor J.D., Carpentier M., Young W.M., Wininger F.A., Kennedy D., Vuillemenot B.R., O'Neill C.A. Enzyme replacement therapy attenuates disease progression in a canine model of late-infantile neuronal ceroid lipofuscinosis (CLN2 disease). J. Neurosci. Res. 2014 Nov, 92(11):1591-1598. 10.1002/jnr.23423.
29. Whiting R.E., Narfström K., Yao G., Pearce J.W., Coates J.R., Castaner L.J., Jensen C.A., Dougherty B.N., Vuillemenot B.R., Kennedy D., O'Neill C.A., Katz M.L. Enzyme replacement therapy delays pupillary light reflex deficits in a canine model of late infantile neuronal ceroid lipofuscinosis. Exp. Eye Res. 2014 Aug, 125:164-172.
30. Sofroniew M.V., Vinters H.V. Astrocytes: biology and pathology. Acta Neuropathol. 2010, 119:7-35.
31. Wininger F.A., Zeng R., Johnson G.S., Katz M.L., Johnson G.C., Bush W.W., Jarboe J.M., Coates J.R. Degenerative myelopathy in a Bernese Mountain Dog with a novel SOD1 missense mutation. J. Vet. Intern. Med. 2011, 25:1166-1170. 10.1111/j.1939-1676.2011.0760.x.
32. Zimin A.V., Marçais G., Puiu D., Roberts M., Salzberg S.L., Yorke J.A. The MaSuRCA genome assembler. Bioinformatics 2013 Nov 1, 29(21):2669-2677. (Epub 2013 Aug 29). 10.1093/bioinformatics/btt476.
33. Swofford R., Mauceli E., Moghadam B.T., Greka A., Alföldi J., Abouelleil A., Aftuck L., Bessette D., Berlin A., Brown A., Gearin G., Lui A., Macdonald J.P., Priest M., Shea T., Turner-Maier J., Zimmer A., Lander E.S., di Palma F., Lindblad-Toh K., Grabherr M.G. An improved canine genome and a comprehensive catalogue of coding genes and non-coding transcripts. PLoS ONE 2014 Mar 13, 9(3):e91172. (eCollection 2014). 10.1371/journal.pone.0091172.
34. Livak K.J. Allelic discrimination using fluorogenic probes and the 5' nuclease assay. Genet. Anal. 1999, 14:143-149. 10.1016/S1050-3862(98)00019-9.
35. Katz M.L., Sanders D.A., Sanders D.N., Hansen E.A., Johnson G.S. Assessment of plasma carnitine concentrations in relation to ceroid lipofuscinosis in Tibetan Terriers. Am. J. Vet. Res. 2002 Jun, 63(6):890-895. 10.2460/ajvr.2002.63.890.
36. Savukoski M., Klockars T., Holmberg V., Santavuori P., Lander E.S., Peltonen L. CLN5, a novel gene encoding a putative transmembrane protein mutated in Finnish variant late infantile neuronal ceroid lipofuscinosis. Nat. Genet. 1998 Jul, 19(3):286-288. 10.1038/975.
37. Kopra O., Vesa J., von Schantz C., Manninen T., Minye H., Fabritius A.L., Rapola J., van Diggelen O.P., Saarela J., Jalanko A., Peltonen L. A mouse model for Finnish variant late infantile neuronal ceroid lipofuscinosis, CLN5, reveals neuropathology associated with early aging. Hum. Mol. Genet. 2004 Dec 1, 13(23):2893-2906. (Epub 2004 Sep 30). 10.1093/hmg/ddh312.
38. Houweling P.J., Cavanagh J.A., Palmer D.N., Frugier T., Mitchell N.L., Windsor P.A., Raadsma H.W., Tammen I. Neuronal ceroid lipofuscinosis in Devon cattle is caused by a single base duplication (c.662dupG) in the bovine CLN5 gene. Biochim. Biophys. Acta 2006 Oct, 1762(10):890-897. (Epub 2006 Jul 25). 10.1016/j.bbadis.2006.07.008.
39. Frugier T., Mitchell N.L., Tammen I., Houweling P.J., Arthur D.G., Kay G.W., van Diggelen O.P., Jolly R.D., Palmer D.N. A new large animal model of CLN5 neuronal ceroid lipofuscinosis in Borderdale sheep is caused by a nucleotide substitution at a consensus splice site (c.571+1G>A) leading to excision of exon 3. Neurobiol. Dis. 2008 Feb, 29(2):306-315. (Epub 2007 Sep 29). 10.1016/j.nbd.2007.09.006.
40. Vesa J., Chin M.H., Oelgeschläger K., Isosomppi J., DellAngelica E.C., Jalanko A., Peltonen L. Neuronal ceroid lipofuscinoses are connected at molecular level: interaction of CLN5 protein with CLN2 and CLN3. Mol. Biol. Cell 2002 Jul, 13(7):2410-2420.
41. Schmiedt M.L., Bessa C., Heine C., Ribeiro M.G., Jalanko A., Kyttala A. The neuronal ceroid lipofuscinosis protein CLN5: new insights into cellular maturation, transport, and consequences of mutations. Hum. Mutat. 2010 Mar, 31(3):356-365. 10.1002/humu.21195.
42. Petersen T.N., Brunak S., von Heijne G., Nielsen H. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat. Methods 2011, 8:785-786. 10.1038/nmeth.1701.
43. Isosomppi J., Vesa J., Jalanko A., Peltonen L. Lysosomal localization of the neuronal ceroid lipofuscinosis CLN5 protein. Hum. Mol. Genet. 2002 Apr 15, 11(8):885-891. 10.1093/hmg/11.8.885.
44. Holmberg V., Jalanko A., Isosomppi J., Fabritius A.L., Peltonen L., Kopra O. The mouse ortholog of the neuronal ceroid lipofuscinosis CLN5 gene encodes a soluble lysosomal glycoprotein expressed in the developing brain. Neurobiol. Dis. 2004 Jun, 16(1):29-40. 10.1016/j.nbd.2003.12.019.
45. Moharir A., Peck S.H., Budden T., Lee S.Y. The role of N-glycosylation in folding, trafficking, and functionality of lysosomal protein CLN5. PLoS ONE 2013 Sep 10, 8(9):e74299. (eCollection 2013). 10.1371/journal.pone.0074299.
46. Larkin H., Ribeiro M.G., Lavoie C. Topology and membrane anchoring of the lysosomal storage disease-related protein CLN5. Hum. Mutat. 2013 Dec, 34(12):1688-1697. (Epub 2013 Oct 10). 10.1002/humu.22443.
47. Santavuori P., Rapola J., Nuutila A., Raininko R., Lappi M., Launes J., Herva R., Sainio K. The spectrum of Jansky-Bielschowsky disease. Neuropediatrics 1991 May, 22(2):92-96.
48. Kousi M., Lehesjoki A.E., Mole S.E. Update of the mutation spectrum and clinical correlations of over 360 mutations in eight genes that underlie the neuronal ceroid lipofuscinoses. Hum. Mutat. 2012 Jan, 33(1):42-63. 10.1002/humu.21624.
49. Cannelli N., Nardocci N., Cassandrini D., Morbin M., Aiello C., Bugiani M., Criscuolo L., Zara F., Striano P., Granata T., Bertini E., Simonati A., Santorelli F.M. Revelation of a novel CLN5 mutation in early juvenile neuronal ceroid lipofuscinosis. Neuropediatrics 2007 Feb, 38(1):46-49. 10.1055/s-2007-981449.
50. Xin W., Mullen T.E., Kiely R., Min J., Feng X., Cao Y., O'Malley L., Shen Y., Chu-Shore C., Mole S.E., Goebel H.H., Sims K. CLN5 mutations are frequent in juvenile and late-onset non-Finnish patients with NCL. Neurology 2010 Feb 16, 74(7):565-571. 10.1212/WNL.0b013e3181cff70d.
51. Mancini C., Nassani S., Guo Y., Chen Y., Giorgio E., Brussino A., Di Gregorio E., Cavalieri S., Lo Buono N., Funaro A., Pizio N.R., Nmezi B., Kyttala A., Santorelli F.M., Padiath Q.S., Hakonarson H., Zhang H., Brusco A. Adult-onset autosomal recessive ataxia associated with neuronal ceroid lipofuscinosis type 5 gene (CLN5) mutations. J. Neurol. 2015 Jan, 262(1):173-178. (Epub 2014 Oct 31). 10.1007/s00415-014-7553-y.
52. von Schantz C., Kielar C., Hansen S.N., Pontikis C.C., Alexander N.A., Kopra O., Jalanko A., Cooper J.D. Progressive thalamocortical neuron loss in Cln5 deficient mice: distinct effects in Finnish variant late infantile NCL. Neurobiol. Dis. 2009 May, 34(2):308-319. 10.1016/j.nbd.2009.02.001.
53. Schmiedt M.L., Blom T., Blom T., Kopra O., Wong A., von Schantz-Fant C., Ikonen E., Kuronen M., Jauhiainen M., Cooper J.D., Jalanko A. Cln5-deficiency in mice leads to microglial activation, defective myelination and changes in lipid metabolism. Neurobiol. Dis. 2012 Apr, 46(1):19-29. (Epub 2011 Dec 13. d). 10.1016/j.nbd.2011.12.009.
54. Hughes S.M., Hope K.M., Xu J.B., Mitchell N.L., Palmer D.N. Inhibition of storage pathology in prenatal CLN5-deficient sheep neural cultures by lentiviral gene therapy. Neurobiol. Dis. 2014 Feb, 62:543-550. (Epub 2013 Nov 19. PMID:24269732). 10.1016/j.nbd.2013.11.011.