A critical tryptophan and Ca2+ in activation and catalysis of TPPI, the enzyme deficient in classic late-infantile neuronal ceroid lipofuscinosis

PLoS ONE

Volumn 5, Issue 8, 2010, Pages

  Kuizon, Salomon ^a   Dimaiuta, Kathleen ^a   Walus, Marius ^a   Jenkins, Edmund C ^a   Kuizon, Marisol ^a   Kida, Elizabeth ^a   Golabek, Adam A ^a   Espinoza, Daniel O ^a   Pullarkat, Raju K ^a   Junaid, Mohammed A ^a  

^a NEW YORK STATE INSTITUTE FOR BASIC RESEARCH IN DEVELOPMENTAL DISABILITIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINOPEPTIDASE; CALCIUM ION; N BROMOSUCCINIMIDE; TRIPEPTIDYL AMINOPEPTIDASE I; TRYPTOPHAN; UNCLASSIFIED DRUG; CALCIUM; DIPEPTIDYL PEPTIDASE; ENZYME INHIBITOR; ENZYME PRECURSOR; INDOLE DERIVATIVE; SERINE PROTEINASE; TRIPEPTIDYL PEPTIDASE I; TRIPEPTIDYL-PEPTIDASE 1;

ANIMAL CELL; ARTICLE; CATALYSIS; CELLULAR DISTRIBUTION; CHO CELL; CONCENTRATION RESPONSE; CONTROLLED STUDY; COW; ENZYME ACTIVITY; LYSOSOME; NEURONAL CEROID LIPOFUSCINOSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN TERTIARY STRUCTURE; SITE DIRECTED MUTAGENESIS; STRUCTURE ACTIVITY RELATION; ANIMAL; BIOCATALYSIS; CHEMICAL STRUCTURE; CHEMISTRY; CRICETULUS; ENZYME ACTIVATION; ENZYMOLOGY; GENETICS; HAMSTER; HUMAN; METABOLISM; MUTATION; OXIDATION REDUCTION REACTION; PROTEIN CONFORMATION; PROTEIN TRANSPORT;

MAMMALIA;

AMINOPEPTIDASES; ANIMALS; BASE SEQUENCE; BIOCATALYSIS; BROMOSUCCINIMIDE; CALCIUM; CHO CELLS; CRICETINAE; CRICETULUS; DIPEPTIDYL-PEPTIDASES AND TRIPEPTIDYL-PEPTIDASES; ENZYME ACTIVATION; ENZYME INHIBITORS; ENZYME PRECURSORS; HUMANS; INDOLES; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; MUTATION; NEURONAL CEROID-LIPOFUSCINOSES; OXIDATION-REDUCTION; PROTEIN CONFORMATION; PROTEIN TRANSPORT; SERINE PROTEASES; TRYPTOPHAN;

EID: 77957783943     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0011929     Document Type: Article

References (54)

1. Junaid MA, Pullarkat RK (2001) Biochemistry of neuronal ceroid lipofuscinosis. Adv Genet 45: 93-106.
2. Mole SE (2004) The genetic spectrum of human neuronal ceroid-lipofuscinoses. Brain Pathol 14(1): 70-76.
3. Golabek AA, Kida E (2006) Tripeptidyl-peptidase I in health and disease. Biol Chem 387(8): 1091-1099.
4. Zeman W, Donahue S, Dyken P, Green J (1970) Leukodystrophies and poliodystrophies. In: Vinken PJ, Bruyn GW, editors. Handbook of Clinical Neurology. Amsterdam: Elsevier Science Volume 10: 588-679.
5. Boustany R-M (1996) Neurodystrophies and Neurolipidoses. In: Moser HW, editor. Handbook of Clinical Neurology. Amsterdam: Elsevier Science Volume 22 (66): 671-700.
6. Mole SE, Williams RE, Goebel HH (2005) Correlations between genotype, ultrastructural morphology and clinical phenotype in the neuronal ceroid lipofuscinosis. Neurogenetics 6(3): 107-126.
7. Sleat DE, Donnelly RJ, Lackland H, Liu C-G, Sohar I, et al. (1997) Association of mutations in a lysosomal protein with classical late-infantile neuronal ceroid lipofuscinosis. Science 277: 1802-1805.
8. Vines DJ, Warburton MJ (1999) Classical late infantile neuronal ceroid lipofuscinosis fibroblasts are deficient in lysosomal tripeptidyl peptidase I. FEBS Lett 443: 131-135.
9. Rawlings ND, Barrett AJ (1999) Tripeptidyl-peptidase I is apparently the CLN2 protein absent in classical late-infantile neuronal ceroid lipofuscinosis. Biochim Biophys Acta 1429: 496-500.
10. Sleat DE, El-Banna M, Sohar I, Kim KH, Dobrenis K, et al. (2008) Residual levels of tripeptidyl-peptidase I activity dramatically ameliorate disease in late-infantile neuronal ceroid lipofuscinosis. Mol Genet Metab 94(2): 222-233.
11. Elleder M, Dvorakova L, Stolnaja L, Vlaskova H, Hulkova H, et al. (2008) Atypical CLN2 with later onset and prolonged course: a neuropathologic study showing different sensitivity of neuronal subpopulations to TPP1 deficiency. Acta Neuropathol 116(1): 119-124.
12. Junaid MA, Sklower Brooks S, Wisniewski KE, Pullarkat RKA novel assay for lysosomal pepstatin-insensitive proteinase and its application for the diagnosis of late-infantile neuronal ceroid lipofuscinosis, Clin Chim Acta 281(1999): 169-176.
13. Sohar I, Sleat DE, Jadot M, Lobel P (1999) Biochemical characterization of a lysosomal protease deficient in classical late infantile neuronal ceroid lipofuscinosis (LINCL) and development of an enzyme-based assay for diagnosis and exclusion of LINCL in human specimens and animal models. J Neurochem 73(2): 700-711.
14. Kurachi Y, Oka A, Mizuguchi M, Ohkoshi Y, Sasaki M, et al. (2000) Rapid immunologic diagnosis of classic late infantile neuronal ceroid lipofuscinosis. Neurology 54(8): 1676-1680.
15. Young EP, Winchester BG, Peter Logan W, Wheeler RB, Lake BD (2000) Exclusion of late infantile neuronal ceroid lipofuscinosis (LINCL) in a fetus by assay of tripeptidyl peptidase I in chorionic villi. Prenat Diagn 20(4): 337-339.
16. Zhong NA, Wisniewski KE, Ju W, Moroziewicz DN, Jurkiewicz A, et al. (2000) Molecular diagnosis of and carrier screening for the neuronal ceroid lipofuscinosis. Genet Test 4(3): 243-248.
17. Kleijer WJ, van Diggelen OP, Keulemans JL, Losekoot M, Garritsen VH, et al. (2001) First-trimester diagnosis of late-infantile neuronal ceroid lipofuscinosis (LINCL) by tripeptidyl peptidase I assay and CLN2 mutation analysis. Prenat Diagn 21(2): 99-101.
18. Passini MA, Dodge JC, Bu J, Yang W, Zhao Q, et al. (2006) Intracranial delivery of CLN2 reduces brain pathology in a mouse model of classical late infantile neuronal ceroid lipofuscinosis. J Neurosci 26(5): 1334-1342.
19. Chang M, Cooper JD, Sleat DE, Cheng SH, Dodge JC, et al. (2008) Intraventricular enzyme replacement improves disease phenotypes in a mouse model of late infantile neuronal ceroid lipofuscinosis. Mol Ther 16(4): 649-656.
20. Worgall S, Sondhi D, Hackett NR, Kosofsky B, Kekatpure MV, et al. (2008) Treatment of late infantile neuronal ceroid lipofuscinosis by CNS administration of a serotype 2 adeno-associated virus expressing CLN2 cDNA. Hum Gene Ther 19(5): 463-474.
21. Junaid MA, Clark GM, Pullarkat RK (1999) A lysosomal pepstatin-insensitive proteinase as a novel biomarker for breast cancer. Int J Biol Markers 15(2): 129-134.
22. Altorjay A, Paal B, Sohar N, Kiss J, Szanto I, et al. (2005) Metabolic changes in the lower esophageal sphincter influencing the result of anti-reflux surgical interventions in chronic gastroesophageal reflux disease. World J Gastroentero 11(37): 5751-5756.
23. Tsukamoto T, Iida J, Dobashi Y, Furukawa T, Konishi F (2006) Overexpression in colorectal carcinoma of two lysosomal enzymes, CLN2 and CLN1, involved in neuronal ceroid lipofuscinosis. Cancer 106(7): 1489-1497.
24. Junaid MA, Pullarkat RKIncreased brain lysosomal pepstatin-insensitive proteinase activity in patients with neurodegenerative diseases. Neurosci Lett 264: 157-160.
25. Mitchison HM, Bernard DJ, Greene NDE, Cooper JD, Junaid MA, et al. (1999) Targeted disruption of the Cln3 gene provides a mouse model for Batten disease, The Batten Mouse Model Consortium (corrected). Neurobiol Dis 6: 321-334.
26. Liu C-G, Sleat DE, Donnelly RJ, Lobel P (1998) Structural organization and sequence of CLN2, the defective gene in classical late infantile neuronal ceroid lipofuscinosis. Genomics 50: 206-212.
27. Lin L, Sohar I, Lackland H, Lobel P (2001) The human CLN2 protein/tripeptidyl-peptidase I is a serine protease that autoactivates at acidic pH. J Biol Chem 276(3): 2249-2255.
28. Wujek P, Kida E, Walus M, Wisniewski KE, Golabek AA (2004) N-glycosylation is crucial for folding, trafficking, and stability of human tripeptidyl-peptidase I. J Biol Chem 279(13): 12827-12839.
29. Golabek A A, Kida E, Walus M, Wujek P, Mehta P, et al. (2003) Biosynthesis, glycosylation, and enzymatic processing in vivo of human tripeptidyl-peptidase I. J Biol Chem 278: 7135-7145.
30. Golabek AA, Dolzhanskaya N, Walus M, Wisniewski KE, Kida E (2008) Prosegment of tripeptidyl peptidase I is a potent, slow-binding inhibitor of its cognate enzyme. J Biol Chem 283(24): 16497-16504.
31. Tsiakas K, Steinfeld R, Storch S, Ezaki J, Lukacs Z, et al. (2004) Mutation of the glycosylated asparagine residue 286 in human CLN2 protein results in loss of enzymatic activity. Glycobiology 14(4): 1C-5C.
32. Pal A, Kraetzner R, Gruene T, Grapp M, Schreiber K, et al. (2009) Structure of tripeptidyl-peptidase I provides insight into the molecular basis of late infantile neuronal ceroid lipofuscinosis. J Biol Chem 284(6): 3976-3984.
33. Guhaniyogi J, Sohar I, Das K, Stock AM, Lobel PCrystal structure and autoactivation pathway of the precursor form of human tripeptidyl-peptidase 1, the enzyme deficient in late infantile ceroid lipofuscinosis. J Biol Chem 284(6): 3985-3997.
34. Rawlings ND, Morton FR, Kok CY, Kong J, Barrett AJ (2008) MEROPS: the peptidase database. Nucleic Acids Res 36: D320-D325.
35. Tian Y, Sohar I, Taylor JW, Lobel P (2006) Determination of the substrate specificity of tripeptidyl-peptidase I using combinatorial peptide libraries and development of improved fluorogenic substrates. J Biol Chem 281(10): 6559-6572.
36. Ezaki J, Takeda-Ezaki M, Oda K, Kominami E (2000) Characterization of endopeptidase activity of tripeptidyl peptidase-I/CLN2 protein which is deficient in classical late infantile neuronal ceroid lipofuscinosis. Biochem Biophys Res Commun 268(3): 904-908.
37. Junaid MA, Wu G, Pullarkat RK (2000) Purification and characterization of bovine brain lysosomal pepstatin-insensitive proteinase, the gene product deficient in the human late-infantile neuronal ceroid lipofuscinosis. J Neurochem 74: 287-294.
38. Autefage H, Albinet V, Garcia V, Berges H, Nicolau ML, et al. (2009) Lysosomal serine protease CLN2 regulates tumor necrosis factor-alpha-mediated apoptosis in a Bid-dependent manner. J Biol Chem 284(17): 11507-11516.
39. Palmer DN, Fearnley IM, Walker JE, Hall NA, Lake BD, et al. (1992) Mitochondrial ATP synthase subunit c storage in the ceroid-lipofuscinoses (Batten disease). Am J Med Genet 42(4): 561-567.
40. Elleder M, Sokolova J, Hrebicek M (1997) Follow-up study of subunit c of mitochondrial ATP synthase (SCMAS) in Batten disease and in unrelated lysosomal disorders. Acta Neuropathol 93: 379-390.
41. Lundblad RL (2005) The chemical modification of tryptophan. Chemical reagents for protein modification. Florida: CRC Press. pp. 247-268. 3rd edition.
42. Freisheim JH, Huennekens FM (1969) Effect of N-bromosuccinimide on dihydrofolate reductase. Biochemistry 8(6): 2271-2276.
43. Sleat DE, Sohar I, Pullarkat PS, Lobel P, Pullarkat RK (1998) Specific alterations in levels of mannose 6-phosphorylated glycoproteins in different neuronal ceroid lipofuscinosis. Biochem J 334: 547-551.
44. Pohlmann R, Boeker MW, von Figura K (1995) The two mannose 6-phosphate receptors transport distinct complements of lysosomal proteins. J Biol Chem 270(45): 27311-27318.
45. Cohen FE, Kelly JW (2003) Therapeutic approaches to protein-misfolding diseases. Nature 426: 905-909.
46. Kida E, Golabek AA, Walus M, Wujek P, Kaczmarski W, et al. Distribution of tripeptidyl peptidase I in human tissues under normal and pathological conditions. J Neuropathol Exp Neurol 60: 280-292.
47. Ramachandran LK, Witkop B (1967) N-Bromosuccinimide cleavage of peptides. Meth Enzymol 11: 283.
48. Ippolito JA, Alexander RS, Christianson DW (1990) Hydrogen bond stereochemistry in protein structure and function. J Mol Biol 215(3): 457-471.
49. Vey M, Schafer W, Berghofer S, Klenk H-D, Garten W (1994) Maturation of the trans-Golgi network protease furin: compartmentalization of propeptide removal, substrate cleavage, and COOH-terminal truncation. J Cell Biol 127(6 Pt 2): 1829-1842.
50. Zhou Y, Lindberg I (1994) Enzymatic properties of carboxyl-terminally truncated prohormone convertase 1 (PC1/SPC3) and evidence for autocatalytic conversion. J Biol Chem 269(28): 18408-18413.
51. Gallagher T, Bryan P, Gilliland GL (1993) Calcium-independent subtilisin by design. Proteins 16(2): 205-213.
52. Walus M, Kida E, Wisniewski KE, Golabek AA (2005) Ser475, Glu272, Asp276, Asp327, and Asp360 are involved in catalytic activity of human tripeptidyl-peptidase I. FEBS Lett 579(6): 1383-1388.
53. Vines DJ, Warburton MJ (1998) Purification and characterisation of a tripeptidyl aminopeptidase I from rat spleen. Biochim Biophys Acta 1384(2): 233-242.
54. Lowry OH, Rosenbrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193: 265-275.