Proteolysis Controls Endogenous Substance P Levels

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Mitchell, Andrew J ^a   Lone, Anna Mari ^b   Tinoco, Arthur D ^c   Saghatelian, Alan ^b  

^a HARVARD UNIVERSITY   (United States)

^b HARVARD UNIVERSITY   (United States)

^c UNIVERSITY OF PUERTO RICO   (Puerto Rico)

Author keywords

[No Author keywords available]

Indexed keywords

ILOMASTAT; SUBSTANCE P;

AMINO TERMINAL SEQUENCE; ANIMAL TISSUE; ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CELL LYSATE; CONTROLLED STUDY; MOUSE; NONHUMAN; PEPTIDOMICS; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DETERMINATION; SPINAL CORD;

AMINO ACID SEQUENCE; ANIMALS; ENZYME INHIBITORS; FEMALE; MASS SPECTROMETRY; METALLOPROTEASES; MICE; MICE, KNOCKOUT; PEPTIDE FRAGMENTS; PROTEOLYSIS; SPINAL CORD; SUBSTANCE P;

EID: 84880423718     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0068638     Document Type: Article

References (67)

1. Ribeiro-da-Silva A, Hokfelt T, (2000) Neuroanatomical localisation of substance P in the CNS and sensory neurons. Neuropeptides 34: 256-271.
2. Otsuka M, Yoshioka K, (1993) Neurotransmitter functions of mammalian tachykinins. Physiological Reviews 73: 229-308.
3. Hall ME, Stewart JM, (1983) Substance P and antinociception. Peptides 4: 31-35.
4. Hall ME, Stewart JM, (1983) Substance P and behavior: opposite effects of N-terminal and C-terminal fragments. Peptides 4: 763-768.
5. Yeomans D, Proudfit H, (1992) Antinociception induced by microinjection of substance P into the A7 catecholamine cell group in the rat. Neuroscience 49: 681-691.
6. Kolasinski SL, Haines KA, Siegel EL, Cronstein BN, Abramson SB, (1992) Neuropeptides and inflammation. A somatostatin analog as a selective antagonist of neutrophil activation by substance P. Arthritis & Rheumatism 35: 369-375.
7. Palmer J, Greenwood B, (1993) Regional content of enteric substance P and vasoactive intestinal peptide during intestinal inflammation in the parasitized ferret. Neuropeptides 25: 95-103.
8. Schlesinger K, Pelleymounter MA, Kamp J, Bader DL, Stewart JM, et al. (1986) Substance P facilitation of memory: effects in an appetitively motivated learning task. Behavioral and neural biology 45: 230-239.
9. Nagel JA, Welzl H, Bättig K, Huston JP, (1993) Facilitation of tunnel maze performance by systemic injection of the neurokinin substance P. Peptides. 14: 85-95.
10. Santangelo EM, Morato S, Mattioli R, (2001) Facilitatory effect of substance P on learning and memory in the inhibitory avoidance test for goldfish. Neuroscience letters 303: 137-139.
11. Berrettini WH, Rubinow DR, Nurnberger Jr JI, Simmons-Alling S, Post RM, et al. (1985) CSF substance P immunoreactivity in affective disorders. Biological psychiatry 20: 965-970.
12. Lieb K, Treffurth Y, Berger M, Fiebich BL, (2002) Substance p and affective disorders: new treatment opportunities by neurokinin 1 receptor antagonists? Neuropsychobiology 45: 2-6.
13. Shirayama Y, Mitsushio H, Takashima M, Ichikawa H, Takahashi K, (1996) Reduction of substance P after chronic antidepressants treatment in the striatum, substantia nigra and amygdala of the rat. Brain research 739: 70-78.
14. Kreeger JS, Larson AA, (1993) Substance P-(1-7), a substance P metabolite, inhibits withdrawal jumping in morphine-dependent mice. European journal of pharmacology 238: 111-115.
15. Kreeger JS, Larson AA, (1996) The substance P amino-terminal metabolite substance P (1-7), administered peripherally, prevents the development of acute morphine tolerance and attenuates the expression of withdrawal in mice. Journal of Pharmacology and Experimental Therapeutics 279: 662-667.
16. Nylander I, Sakurada T, Le Greves P, Terenius L, (1991) Levels of dynorphin peptides, substance P and CGRP in the spinal cord after subchronic administration of morphine in the rat. Neuropharmacology 30: 1219-1223.
17. Kang B-N, Jeong K-S, Park S-J, Kim S-H, Kim T-H, et al. (2001) Regulation of apoptosis by somatostatin and substance P in peritoneal macrophages. Regulatory peptides 101: 43-49.
18. Lallemend F, Lefebvre P, Hans G, Rigo J-m, Van de Water T, et al. (2003) Substance P protects spiral ganglion neurons from apoptosis via PKC-Ca2+-MAPK/ERK pathways. Journal of neurochemistry 87: 508-521.
19. Gerfen CR, McGinty J, Young WS, (1991) Dopamine differentially regulates dynorphin, substance P, and enkephalin expression in striatal neurons: in situ hybridization histochemical analysis. The Journal of neuroscience 11: 1016-1031.
20. Jessell T, Tsunoo A, Kanazawa I, Otsuka M, (1979) Substance P: depletion in the dorsal horn of rat spinal cord after section of the peripheral processes of primary sensory neurons. Brain research 168: 247-259.
21. Verge V, Richardson P, Wiesenfeld-Hallin Z, Hokfelt T, (1995) Differential influence of nerve growth factor on neuropeptide expression in vivo: a novel role in peptide suppression in adult sensory neurons. The Journal of neuroscience 15: 2081-2096.
22. Theriault E, Otsuka M, Jessell T, (1979) Capsaicin-evoked release of substance P from primary sensory neurons. Brain research 170: 209.
23. Marguet D, Baggio L, Kobayashi T, Bernard A-M, Pierres M, et al. (2000) Enhanced insulin secretion and improved glucose tolerance in mice lacking CD26. Proceedings of the National Academy of Sciences 97: 6874-6879.
24. Tinoco AD, Kim YG, Tagore DM, Wiwczar J, Lane WS, et al. (2011) A peptidomics strategy to elucidate the proteolytic pathways that inactivate Peptide hormones. Biochemistry 50: 2213.
25. Le Greves P, Nyberg F, Terenius L, Hökfelt T, (1985) Calcitonin gene-related peptide is a potent inhibitor of substance P degradation. European journal of pharmacology 115: 309-311.
26. Lee CM, Sandberg BE, Hanley MR, Iversen LL, (1981) Purification and Characterisation of a Membrane-Bound Substance-P-Degrading Enzyme from Human Brain. European Journal of Biochemistry 114: 315-327.
27. Blumberg S, Teichberg V, Charli J, Hersh L, McKelvy J, (1980) Cleavage of substance P to an N-terminal tetrapeptide and a C-terminal heptapeptide by a post-proline cleaving enzyme from bovine brain. Brain research 192: 477-486.
28. Bunnett N, Turner A, Hryszko J, Kobayashi R, Walsh J, (1988) Isolation of endopeptidase-24.11 (EC 3.4. 24.11, "phalinase" from the pig stomach. Hydrolysis of substance P, gastrin-releasing peptide 10,[Leu5] enkephalin, and [Met5] enkephalin. Gastroenterology 95: 952.
29. Diekmann O, Tschesche H, (1994) Degradation of kinins, angiotensins and substance P by polymorphonuclear matrix metalloproteinases MMP 8 and MMP 9. Brazilian journal of medical and biological research = Revista brasileira de pesquisas medicas e biologicas/Sociedade Brasileira de Biofisica [et al] 27: 1865.
30. Heymann E, Mentlein R, (1978) Liver dipeptidyl aminopeptidase IV hydrolyzes substance P. FEBS letters. 91: 360.
31. Karlsson K, Nyberg F, (1998) Purification of substance P endopeptidase (SPE) activity in human spinal cord and subsequent comparative studies with SPE in cerebrospinal fluid and with chymotrypsin. J Mol Recognit 11: 266-269.
32. Karlsson K, Nyberg F, (2000) Purification of Substance P endopeptidase activity in the rat ventral tegemental area with the Äkta-Purifier chromatographic system. Journal of Chromatography A 893: 107-113.
33. Yokosawa H, Endo S, Ogura Y, Ishii S-i, (1983) A new feature of angiotensin-converting enzyme in the brain: hydrolysis of substance P. Biochemical and biophysical research communications. 116: 735-742.
34. Zimmer A, Zimmer AM, Baffi J, Usdin T, Reynolds K, et al. (1998) Hypoalgesia in mice with a targeted deletion of the tachykinin 1 gene. Proceedings of the National Academy of Sciences 95: 2630-2635.
35. Lu B, Gerard NP, Kolakowski Jr LF, Bozza M, Zurakowski D, et al. (1995) Neutral endopeptidase modulation of septic shock. The Journal of experimental medicine 181: 2271-2275.
36. Kim YG, Lone AM, Nolte WM, Saghatelian A, (2012) Peptidomics approach to elucidate the proteolytic regulation of bioactive peptides. Proc Natl Acad Sci U S A 109: 8523-8527.
37. Tinoco AD, Tagore DM, Saghatelian A, (2010) Expanding the dipeptidyl peptidase 4-regulated peptidome via an optimized peptidomics platform. Journal of the American Chemical Society 132: 3819-3830.
38. Rawlings ND, Barrett AJ, Bateman A, (2012) MEROPS: the database of proteolytic enzymes, their substrates and inhibitors. Nucleic Acids Res 40: D343-350.
39. Ducret A, Van Oostveen I, Eng JK, Yates JR, Aebersold R, (1998) High throughput protein characterization by automated reverse-phase chromatography electrospray tandem mass spectrometry. Protein Science 7: 706-719.
40. Karlsson K, Eriksson U, Andrén P, Nyberg F, (1997) Purification and characterization of substance P endopeptidase activities in the rat spinal cord. Preparative biochemistry & biotechnology 27: 59-78.
41. Nyberg F, Le Greves P, Sundqvist C, Terenius L, (1984) Characterization of substance P(1-7) and (1-8) generating enzyme in human cerebrospinal fluid. Biochem Biophys Res Commun 125: 244-250.
42. Brou C, Logeat F, Gupta N, Bessia C, LeBail O, et al. (2000) A novel proteolytic cleavage involved in Notch signaling: the role of the disintegrin-metalloprotease TACE. Molecular cell 5: 207-216.
43. Sekar V, Hageman JH, (1979) Specificity of the serine protease inhibitor, phenylmethylsulfonyl fluoride. Biochemical and biophysical research communications 89: 474-478.
44. Siviter RJ, Nachman RJ, Dani MP, Keen JN, Shirras AD, et al. (2002) Peptidyl dipeptidases (Ance and Acer) of Drosophila melanogaster: major differences in the substrate specificity of two homologs of human angiotensin I-converting enzyme. Peptides 23: 2025-2034.
45. Bertenshaw GP, Turk BE, Hubbard SJ, Matters GL, Bylander JE, et al. (2001) Marked differences between metalloproteases meprin A and B in substrate and peptide bond specificity. Journal of Biological Chemistry 276: 13248-13255.
46. Skidgel RA, Engelbrecht S, Johnson AR, Erdös EG, (1984) Hydrolysis of substance P and neurotensin by converting enzyme and neutral endopeptidase. Peptides 5: 769-776.
47. Johnson GD, Stevenson T, Ahn K, (1999) Hydrolysis of Peptide Hormones by Endothelin-converting Enzyme-1 A COMPARISON WITH NEPRILYSIN. Journal of Biological Chemistry 274: 4053-4058.
48. Chow KM, Gakh O, Payne I, Juliano MA, Juliano L, et al. (2009) Mammalian Pitrilysin: Substrate Specificity and Mitochondrial Targeting†. Biochemistry 48: 2868-2877.
49. Kupershmidt I, Su QJ, Grewal A, Sundaresh S, Halperin I, et al. (2010) Ontology-based meta-analysis of global collections of high-throughput public data. PLoS One 5.
50. Lein ES, Hawrylycz MJ, Ao N, Ayres M, Bensinger A, et al. (2007) Genome-wide atlas of gene expression in the adult mouse brain. Nature 445: 168-176.
51. Scheer M, Grote A, Chang A, Schomburg I, Munaretto C, et al. (2011) BRENDA, the enzyme information system in 2011. NUCLEIC ACIDS RESEARCH 39: D670-D676.
52. Takayama J, Takaoka M, Yamamoto S, Nohara A, Ohkita M, et al. (2008) Actinonin, a meprin inhibitor, protects ischemic acute kidney injury in male but not in female rats. European journal of pharmacology 581: 157-163.
53. Oefner C, D'Arcy A, Hennig M, Winkler FK, Dale GE, (2000) Structure of human neutral endopeptidase (Neprilysin) complexed with phosphoramidon. Journal of molecular biology 296: 341-349.
54. Kukkola PJ, Savage P, Sakane Y, Berry JC, Bilci NA, et al. (1995) Differential structure-activity relationships of phosphoramidon analogues for inhibition of three metalloproteases: endothelin-converting enzyme, neutral endopeptidase, and angiotensin-converting enzyme. Journal of cardiovascular pharmacology 26: S65.
55. Grobelny D, Poncz L, Galardy RE, (1992) Inhibition of human skin fibroblast collagenase, thermolysin, and Pseudomonas aeruginosa elastase by peptide hydroxamic acids. Biochemistry 31: 7152-7154.
56. Whittaker M, Floyd CD, Brown P, Gearing AJH, (1999) Design and Therapeutic Application of Matrix Metalloproteinase Inhibitors. Chemical Reviews 99: 2735-2776.
57. Turk B, (2006) Targeting proteases: successes, failures and future prospects. Nature reviews Drug discovery 5: 785-799.
58. Kato T, Nakano T, Kojima K, Nagatsu T, Sakakibara S, (1980) Changes in prolyl endopeptidase during maturation of rat brain and hydrolysis of substance P by the purified enzyme. Journal of neurochemistry 35: 527-535.
59. Matsas R, Fulcher IS, Kenny AJ, Turner AJ, (1983) Substance P and [Leu] enkephalin are hydrolyzed by an enzyme in pig caudate synaptic membranes that is identical with the endopeptidase of kidney microvilli. Proceedings of the National Academy of Sciences 80: 3111-3115.
60. Nolte WM, Tagore DM, Lane WS, Saghatelian A, (2009) Peptidomics of prolyl endopeptidase in the central nervous system. Biochemistry 48: 11971-11981.
61. Sandberg BEB, Iversen LL, (1982) Substance P. Journal of medicinal chemistry. 25: 1009-1015.
62. Andren PE, Caprioli RM, (1995) In vivo metabolism of substance P in rat striatum utilizing microdialysis/liquid chromatography/micro-electrospray mass spectrometry. Journal of Mass Spectrometry 30: 817-824.
63. Keshishian H, Addona T, Burgess M, Mani DR, Shi X, et al. (2009) Quantification of cardiovascular biomarkers in patient plasma by targeted mass spectrometry and stable isotope dilution. Mol Cell Proteomics 8: 2339-2349.
64. Beaudry F, Vachon P, (2006) Determination of substance P in rat spinal cord by high-performance liquid chromatography electrospray quadrupole ion trap mass spectrometry. Biomedical Chromatography 20: 1344-1350.
65. Klohs J, Baeva N, Steinbrink J, Bourayou R, Boettcher C, et al. (2009) In vivo near-infrared fluorescence imaging of matrix metalloproteinase activity after cerebral ischemia. Journal of Cerebral Blood Flow & Metabolism 29: 1284-1292.
66. Saghatelian A, Jessani N, Joseph A, Humphrey M, Cravatt BF, (2004) Activity-based probes for the proteomic profiling of metalloproteases. Proceedings of the National Academy of Sciences of the United States of America 101: 10000-10005.
67. Kastin AJ (2006) Handbook of biologically active peptides. Amsterdam; Boston: Academic Press. xliii, 1595 p., 1540 p. of col. plates p.