Carboxypeptidases in disease: Insights from peptidomic studies

Proteomics - Clinical Applications

Volumn 8, Issue 5-6, 2014, Pages 327-337

  Sapio, Matthew R ^a   Fricker, Lloyd D ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Carboxypeptidase; Metallopeptidase

Indexed keywords

AMINO ACID; CARBOXYPEPTIDASE; CARBOXYPEPTIDASE A6; CARBOXYPEPTIDASE H; CYTOSOLIC CARBOXYPEPTIDASE 1; TUBULIN; UNCLASSIFIED DRUG; PEPTIDE;

CARBOXY TERMINAL SEQUENCE; EPILEPSY; GENE MUTATION; MICROTUBULE; MOUSE; NERVE DEGENERATION; NONHUMAN; OBESITY; PEPTIDOMICS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; REVIEW; ANIMAL; DISEASES; HUMAN; METABOLISM; PROCEDURES; PROTEOMICS;

ANIMALS; CARBOXYPEPTIDASES; DISEASE; HUMANS; PEPTIDES; PROTEOMICS;

EID: 84902085363     PISSN: 18628346     EISSN: 18628354     Source Type: Journal    
DOI: 10.1002/prca.201300090     Document Type: Review

References (85)

1. Quesada, V., Ordonez, G. R., Sanchez, L. M., Puente, X. S. et al., The Degradome database: mammalian proteases and diseases of proteolysis. Nucleic Acids Res. 2009, 37, D239-D243.
2. Gomis-Ruth, F. X., Structure and mechanism of metallocarboxypeptidases. Crit. Rev. Biochem. Mol. Biol. 2008, 43, 319-345.
3. Lyons, P. J., Fricker, L. D., Carboxypeptidase O is a glycosylphosphatidylinositol-anchored intestinal peptidase with acidic amino acid specificity. J. Biol. Chem. 2011, 286, 39023-39032.
4. Reznik, S. E., Fricker, L. D., Carboxypeptidases from A to z: implications in embryonic development and Wnt binding. Cell. Mol. Life Sci. 2001, 58, 1790-1804.
5. Xin, X., Day, R., Dong, W., Lei, Y. et al., Identification of mouse CPX-2, a novel member of the metallocarboxypeptidase gene family: cDNA cloning, mRNA distribution, and protein expression and characterization. DNA Cell Biol. 1998, 17, 897-909.
6. He, G. P., Muise, A., Li, A. W., Ro, H. S., A eukaryotic transcriptional repressor with carboxypeptidase activity. Nature 1995, 378, 92-96.
7. Lei, Y., Xin, X., Morgan, D., Pintar, J. E. et al., Identification of mouse CPX-1, a novel member of the metallocarboxypeptidase gene family with highest similarity to CPX-2. DNA Cell Biol. 1999, 18, 175-185.
8. Harris, A., Morgan, J. I., Pecot, M., Soumare, A. et al., Regenerating motor neurons express Nna1, a novel ATP/GTP-binding protein related to zinc carboxypeptidases. Mol. Cell Neurosci. 2000, 16, 578-596.
9. Kalinina, E., Biswas, R., Berezniuk, I., Hermoso, A. et al., A novel subfamily of mouse cytosolic carboxypeptidases. FASEB J. 2007, 21, 836-850.
10. Wang, T., Morgan, J. I., The Purkinje cell degeneration (pcd) mouse: an unexpected molecular link between neuronal degeneration and regeneration. Brain Res. 2007, 1140, 26-40.
11. Rogowski, K., van Dijk, J., Magiera, M. M., Bosc, C. et al., A family of protein-deglutamylating enzymes associated with neurodegeneration. Cell 2010, 143, 564-578.
12. Berezniuk, I., Vu, H. T., Lyons, P. J., Sironi, J. J. et al., Cytosolic carboxypeptidase 1 is involved in processing alpha- and beta-tubulin. J. Biol. Chem. 2012, 287, 6503-6517.
13. Berezniuk, I., Lyons, P. J., Sironi, J. J., Xiao, H. et al., Cytosolic carboxypeptidase 5 removes alpha- and gamma-linked glutamates from tubulin. J. Biol. Chem. 2013, 288, 30445-30453.
14. Hsieh, J. M., Tsirulnikov, K., Sawaya, M. R., Magilnick, N. et al., Structures of aminoacylase 3 in complex with acetylated substrates. Proc. Natl. Acad. Sci. USA 2010, 107, 17962-17967.
15. Bitto, E., Bingman, C. A., Wesenberg, G. E., McCoy, J. G. et al., Structure of aspartoacylase, the brain enzyme impaired in Canavan disease. Proc. Natl. Acad. Sci. USA 2007, 104, 456-461.
16. Gardell, S. J., Craik, C. S., Clauser, E., Goldsmith, E. J. et al., A novel rat carboxypeptidase, CPA2: characterization, molecular cloning, and evolutionary implications on substrate specificity in the carboxypeptidase gene family. J. Biol. Chem. 1988, 263, 17828-17836.
17. Reynolds, D. S., Gurley, D. S., Austen, K. F., Cloning and characterization of the novel gene for mast-cell carboxypeptidase-A. J. Clin. Invest. 1992, 89, 273-282.
18. Lyons, P. J., Callaway, M. B., Fricker, L. D., Characterization of carboxypeptidase A6, an extracellular matrix peptidase. J. Biol. Chem. 2008, 283, 7054-7063.
19. Tanco, S., Zhang, X., Morano, C., Aviles, F. X. et al., Characterization of the substrate specificity of human carboxypeptidase A4 and implications for a role in extracellular peptide processing. J. Biol. Chem. 2010, 285, 18385-18396.
20. Lyons, P. J., Fricker, L. D., Substrate specificity of human carboxypeptidase A6. J. Biol. Chem. 2010, 285, 38234-38242.
21. Tanco, S., Lorenzo, J., Garcia-Pardo, J., Degroeve, S. et al., Proteome-derived peptide libraries to study the substrate specificity profiles of carboxypeptidases. Mol. Cell Proteomics 2013, 12, 2096-2110.
22. Coleman, D. L., Eicher, E. M., Fat (fat) and tubby (tub): two autosomal recessive mutations causing obesity syndromes in the mouse. J. Hered. 1990, 81, 424-427.
23. Naggert, J. K., Fricker, L. D., Varlamov, O., Nishina, P. M. et al., Hyperproinsulinaemia in obese fat/fat mice associated with a carboxypeptidase E mutation which reduces enzyme activity. Nat. Genet. 1995, 10, 135-142.
24. Fernandez-Gonzalez, A., La Spada, A. R., Treadaway, J., Higdon, J. C. et al., Purkinje cell degeneration (pcd) phenotypes caused by mutations in the axotomy-induced gene, Nna1. Science 2002, 295, 1904-1906.
25. Mullen, R. J., Eicher, E. M., Sidman, R. L., Purkinje cell degeneration, a new neurological mutation in the mouse. Proc. Natl. Acad. Sci. USA 1976, 73, 208-212.
26. Salzmann, A., Guipponi, M., Lyons, P. J., Fricker, L. D. et al., Carboxypeptidase A6 gene (CPA6) mutations in a recessive familial form of febrile seizures and temporal lobe epilepsy and in sporadic temporal lobe epilepsy. Hum. Mutat. 2012, 33, 124-135.
27. Sapio, M. R., Salzmann, A., Vessaz, M., Crespel, A. et al., Naturally occurring carboxypeptidase A6 mutations: effect on enzyme function and association with epilepsy. J. Biol. Chem. 2012, 287, 42900-42909.
28. Settle, S. H., Jr., Green, M. M., Burtis, K. C., The silver gene of Drosophila melanogaster encodes multiple carboxypeptidases similar to mammalian prohormone-processing enzymes. Proc. Natl. Acad. Sci. USA 1995, 92, 9470-9474.
29. Sidyelyeva, G., Baker, N. E., Fricker, L. D., Characterization of the molecular basis of the Drosophila mutations in carboxypeptidase D. Effect on enzyme activity and expression. J. Biol. Chem. 2006, 281, 13844-13852.
30. Sidyelyeva, G., Wegener, C., Schoenfeld, B. P., Bell, A. J. et al., Individual carboxypeptidase D domains have both redundant and unique functions in Drosophila development and behavior. Cell Mol. Life Sci. 2010, 67, 2991-3004.
31. Bouma, B. N., Meijers, J. C., New insights into factors affecting clot stability: a role for thrombin activatable fibrinolysis inhibitor (TAFI; plasma procarboxypeptidase B, plasma procarboxypeptidase U, procarboxypeptidase R). Semin. Hematol. 2004, 41, 13-19.
32. Mao, S. S., Holahan, M. A., Bailey, C., Wu, G. et al., Demonstration of enhanced endogenous fibrinolysis in thrombin activatable fibrinolysis inhibitor-deficient mice. Blood Coagul. Fibrin. 2005, 16, 407-415.
33. Boffa, M. B., TAFI and wound healing: closing a knowledge gap. J. Thromb. Haemost. 2003, 1, 2075-2077.
34. te Velde, E. A., Wagenaar, G. T., Reijerkerk, A., Roose-Girma, M. et al., Impaired healing of cutaneous wounds and colonic anastomoses in mice lacking thrombin-activatable fibrinolysis inhibitor. J. Thromb. Haemost. 2003, 1, 2087-2096.
35. Asai, S., Sato, T., Tada, T., Miyamoto, T. et al., Absence of procarboxypeptidase R induces complement-mediated lethal inflammation in lipopolysaccharide-primed mice. J. Immunol. 2004, 173, 4669-4674.
36. Schultz, G., Tedesco, M. M., Sho, E., Nishimura, T. et al., Enhanced abdominal aortic aneurysm formation in thrombin-activatable procarboxypeptidase B-deficient mice. Arterioscler. Thromb. Vasc. Biol. 2010, 30, 1363-1370.
37. Song, J. J., Hwang, I., Cho, K. H., Garcia, M. A. et al., Plasma carboxypeptidase B downregulates inflammatory responses in autoimmune arthritis. J. Clin. Invest. 2011, 121, 3517-3527.
38. Mueller-Ortiz, S. L., Wang, D., Morales, J. E., Li, L. et al., Targeted disruption of the gene encoding the murine small subunit of carboxypeptidase N (CPN1) causes susceptibility to C5a anaphylatoxin-mediated shock. J. Immunol. 2009, 182, 6533-6539.
39. Danzer, E., Layne, M. D., Auber, F., Shegu, S. et al., Gastroschisis in mice lacking aortic carboxypeptidase-like protein is associated with a defect in neuromuscular development of the eviscerated intestine. Pediatr. Res. 2010, 68, 23-28.
40. Zhang, L., Reidy, S. P., Bogachev, O., Hall, B. K. et al., Lactation defect with impaired secretory activation in AEBP1-null mice. PLoS One 2011, 6, e27795.
41. Bogachev, O., Majdalawieh, A., Pan, X., Zhang, L. et al., Adipocyte enhancer-binding protein 1 (AEBP1) (a novel macrophage proinflammatory mediator) overexpression promotes and ablation attenuates atherosclerosis in ApoE (-/-) and LDLR (-/-) mice. Mol. Med. 2011, 17, 1056-1064.
42. Matalon, R., Michals, K., Sebesta, D., Deanching, M. et al., Aspartoacylase deficiency and N-acetylaspartic aciduria in patients with Canavan disease. Am. J. Med. Genet. 1988, 29, 463-471.
43. Divry, P., Vianeyliaud, C., Gay, C., Macabeo, V. et al., N-acetylaspartic aciduria-report of 3 new cases in children with a neurological syndrome associating macrocephaly and leukodystrophy. J. Inherit. Metab. Dis. 1988, 11, 307-308.
44. Fricker, L. D., Snyder, S. H. Enkephalin convertase: purification and characterization of a specific enkephalin-synthesizing carboxypeptidase localized to adrenal chromaffin granules. Proc. Natl. Acad. Sci. USA 1982, 79, 3886-3890.
45. Fricker, L. D., Snyder, S. H., Purification and characterization of enkephalin convertase, an enkephalin-synthesizing carboxypeptidase. J. Biol. Chem. 1983, 258, 10950-10955.
46. Song, L., Fricker, L. D., Purification and characterization of carboxypeptidase D, a novel carboxypeptidase E-like enzyme, from bovine pituitary. J. Biol. Chem. 1995, 270, 25007-25013.
47. Varlamov, O., Fricker, L. D., Intracellular trafficking of metallocarboxypeptidase D in AtT-20 cells: localization to the trans-Golgi network and recycling from the cell surface. J. Cell Sci. 1998, 111 (Pt 7), 877-885.
48. Zhang, X., Che, F. Y., Berezniuk, I., Sonmez, K. et al., Peptidomics of Cpe(fat/fat) mouse brain regions: implications for neuropeptide processing. J. Neurochem. 2008, 107, 1596-1613.
49. Rodriguiz, R. M., Wilkins, J. J., Creson, T. K., Biswas, R. et al., Emergence of anxiety-like behaviours in depressive-like Cpefat/fat mice. Int. J. Neuropsychopharmacol. 2013, 16, 1623-1634.
50. Srinivasan, S., Bunch, D. O., Feng, Y., Rodriguiz, R. M. et al., Deficits in reproduction and pro-gonadotropin-releasing hormone processing in male Cpefat mice. Endocrinology 2004, 145, 2023-2034.
51. Woronowicz, A., Koshimizu, H., Chang, S. Y., Cawley, N. X. et al., Absence of carboxypeptidase E leads to adult hippocampal neuronal degeneration and memory deficits. Hippocampus 2008, 18, 1051-1063.
52. Cawley, N. X., Zhou, J. C., Hill, J. M., Abebe, D. et al., The carboxypeptidase E knockout mouse exhibits endocrinological and behavioral deficits. Endocrinology 2004, 145, 5807-5819.
53. Utsunomiya, N., Ohagi, S., Sanke, T., Tatsuta, H. et al., Organization of the human carboxypeptidase E gene and molecular scanning for mutations in Japanese subjects with NIDDM or obesity. Diabetologia 1998, 41, 701-705.
54. Chen, H., Jawahar, S., Qian, Y., Duong, Q. et al., Missense polymorphism in the human carboxypeptidase E gene alters enzymatic activity. Hum. Mutat. 2001, 18, 120-131.
55. Che, F. Y., Yan, L., Li, H., Mzhavia, N. et al., Identification of peptides from brain and pituitary of Cpe(fat)/Cpe(fat) mice. Proc. Natl. Acad. Sci. USA 2001, 98, 9971-9976.
56. Fricker, L. D., McKinzie, A. A., Sun, J., Curran, E. et al., Identification and characterization of proSAAS, a granin-like neuroendocrine peptide precursor that inhibits prohormone processing. J. Neurosci. 2000, 20, 639-648.
57. Mzhavia, N., Qian, Y., Feng, Y., Che, F. Y. et al., Processing of proSAAS in neuroendocrine cell lines. Biochem. J. 2002, 361, 67-76.
58. Wardman, J. H., Berezniuk, I., Di, S., Tasker, J. G. et al., ProSAAS-derived peptides are colocalized with neuropeptide Y and function as neuropeptides in the regulation of food intake. PLoS One 2011, 6, e28152.
59. Morgan, D. J., Wei, S., Gomes, I., Czyzyk, T. et al., The propeptide precursor proSAAS is involved in fetal neuropeptide processing and body weight regulation. J. Neurochem. 2010, 113, 1275-1284.
60. Wei, S., Feng, Y., Che, F. Y., Pan, H. et al., Obesity and diabetes in transgenic mice expressing proSAAS. J. Endocrinol. 2004, 180, 357-368.
61. Che, F. Y., Fricker, L. D., Quantitation of neuropeptides in Cpe(fat)/Cpe(fat) mice using differential isotopic tags and mass spectrometry. Anal. Chem. 2002, 74, 3190-3198.
62. Che, F. Y., Biswas, R., Fricker, L. D., Relative quantitation of peptides in wild-type and Cpe(fat/fat) mouse pituitary using stable isotopic tags and mass spectrometry. J. Mass Spectrom. 2005, 40, 227-237.
63. Lim, J., Berezniuk, I., Che, F. Y., Parikh, R. et al., Altered neuropeptide processing in prefrontal cortex of Cpe (fat/fat) mice: implications for neuropeptide discovery. J. Neurochem. 2006, 96, 1169-1181.
64. Fricker, L. D., Neuropeptidomics to study peptide processing in animal models of obesity. Endocrinology 2007, 148, 4185-4190.
65. Grandison, L., Guidotti, A., Stimulation of food intake by muscimol and beta endorphin. Neuropharmacology 1977, 16, 533-536.
66. Qu, D., Ludwig, D. S., Gammeltoft, S., Piper, M. et al., A role for melanin-concentrating hormone in the central regulation of feeding behaviour. Nature 1996, 380, 243-247.
67. Ollmann, M. M., Wilson, B. D., Yang, Y. K., Kerns, J. A. et al., Antagonism of central melanocortin receptors in vitro and in vivo by agouti-related protein. Science 1997, 278, 135-138.
68. Wei, S., Segura, S., Vendrell, J., Aviles, F. X. et al., Identification and characterization of three members of the human metallocarboxypeptidase gene family. J. Biol. Chem. 2002, 277, 14954-14964.
69. Fontenele-Neto, J. D., Kalinina, E., Feng, Y., Fricker, L. D., Identification and distribution of mouse carboxypeptidase A-6. Brain Res. Mol. Brain Res. 2005, 137, 132-142.
70. Song, L., Fricker, L. D., Cloning and expression of human carboxypeptidase Z, a novel metallocarboxypeptidase. J. Biol. Chem. 1997, 272, 10543-10550.
71. Novikova, E. G., Fricker, L. D., Purification and characterization of human metallocarboxypeptidase Z. Biochem. Biophys. Res. Commun. 1999, 256, 564-568.
72. Pizzuti, A., Calabrese, G., Bozzali, M., Telvi, L. et al., A peptidase gene in chromosome 8q is disrupted by a balanced translocation in a Duane syndrome patient. Invest. Ophthalmol. Vis. Sci. 2002, 43, 3609-3612.
73. Lyons, P. J., Ma, L. H., Baker, R., Fricker, L. D., Carboxypeptidase A6 in zebrafish development and implications for VIth cranial nerve pathfinding. PLoS One 2010, 5, e12967.
74. Wang, T., Parris, J., Li, L., Morgan, J. I., The carboxypeptidase-like substrate-binding site in Nna1 is essential for the rescue of the Purkinje cell degeneration (pcd) phenotype. Mol. Cell Neurosci. 2006, 33, 200-213.
75. Berezniuk, I., Sironi, J., Callaway, M. B., Castro, L. M. et al., CCP1/Nna1 functions in protein turnover in mouse brain: implications for cell death in Purkinje cell degeneration mice. FASEB J. 2010, 24, 1813-1823.
76. Beninga, J., Rock, K. L., Goldberg, A. L., Interferon-gamma can stimulate post-proteasomal trimming of the N terminus of an antigenic peptide by inducing leucine aminopeptidase. J. Biol. Chem. 1998, 273, 18734-18742.
77. Goldberg, A. L., Cascio, P., Saric, T., Rock, K. L., The importance of the proteasome and subsequent proteolytic steps in the generation of antigenic peptides. Mol. Immunol. 2002, 39, 147-164.
78. Saric, T., Graef, C. I., Goldberg, A. L., Pathway for degradation of peptides generated by proteasomes: a key role for thimet oligopeptidase and other metallopeptidases. J. Biol. Chem. 2004, 279, 46723-46732.
79. Reits, E., Neijssen, J., Herberts, C., Benckhuijsen, W. et al., A major role for TPPII in trimming proteasomal degradation products for MHC class I antigen presentation. Immunity 2004, 20, 495-506.
80. Berezniuk, I., Fricker, L. D., A defect in cytosolic carboxypeptidase 1 (Nna1) causes autophagy in Purkinje cell degeneration mouse brain. Autophagy 2010, 6, 558-559.
81. Berezniuk, I., Sironi, J. J., Wardman, J., Pasek, R. C. et al., Quantitative peptidomics of Purkinje cell degeneration mice. PLoS One 2013, 8, e60981.
82. Berman, Y., Mzhavia, N., Polonskaia, A., Devi, L. A., Impaired prohormone convertases in Cpe(fat)/Cpe(fat) mice. J. Biol. Chem. 2001, 276, 1466-1473.
83. Van Damme, P., Staes, A., Bronsoms, S., Helsens, K. et al., Complementary positional proteomics for screening substrates of endo- and exoproteases. Nat. Methods 2010, 7, 512-515.
84. O'Donoghue, A. J., Eroy-Reveles, A. A., Knudsen, G. M., Ingram, J. et al., Global identification of peptidase specificity by multiplex substrate profiling. Nat. Methods 2012, 9, 1095-1100.
85. Gomes, I., Aryal, D. K., Wardman, J. H., Gupta, A. et al., GPR171 is a hypothalamic G protein-coupled receptor for BigLEN, a neuropeptide involved in feeding. Proc. Natl. Acad. Sci. USA 2013, 110, 16211-16216.