Display options
Cite
Meloni BP, Mastaglia FL, Knuckey NW. Cationic Arginine-Rich Peptides (CARPs): A Novel Class of Neuroprotective Agents With a Multimodal Mechanism of Action. Front Neurol. 2020;11:108doi: 10.3389/fneur.2020.00108.
Meloni, B. P., Mastaglia, F. L., & Knuckey, N. W. (2020). Cationic Arginine-Rich Peptides (CARPs): A Novel Class of Neuroprotective Agents With a Multimodal Mechanism of Action. Frontiers in neurology, 11108. https://doi.org/10.3389/fneur.2020.00108
Meloni, Bruno P, et al. "Cationic Arginine-Rich Peptides (CARPs): A Novel Class of Neuroprotective Agents With a Multimodal Mechanism of Action." Frontiers in neurology vol. 11 (2020): 108. doi: https://doi.org/10.3389/fneur.2020.00108
Meloni BP, Mastaglia FL, Knuckey NW. Cationic Arginine-Rich Peptides (CARPs): A Novel Class of Neuroprotective Agents With a Multimodal Mechanism of Action. Front Neurol. 2020 Feb 25;11:108. doi: 10.3389/fneur.2020.00108. eCollection 2020. PMID: 32158425; PMCID: PMC7052017.
Copy Download .nbib Format: NLM
Share it on

Front Neurol. 2020 Feb 25;11:108. doi: 10.3389/fneur.2020.00108. eCollection 2020.

Cationic Arginine-Rich Peptides (CARPs): A Novel Class of Neuroprotective Agents With a Multimodal Mechanism of Action.

Frontiers in neurology

Bruno P Meloni, Frank L Mastaglia, Neville W Knuckey

Affiliations

  1. Department of Neurosurgery, QEII Medical Centre, Sir Charles Gairdner Hospital, Nedlands, WA, Australia.
  2. Perron Institute for Neurological and Translational Science, Nedlands, WA, Australia.
  3. Centre for Neuromuscular and Neurological Disorders, The University of Western Australia, Nedlands, WA, Australia.

PMID: 32158425 PMCID: PMC7052017 DOI: 10.3389/fneur.2020.00108

Abstract

There are virtually no clinically available neuroprotective drugs for the treatment of acute and chronic neurological disorders, hence there is an urgent need for the development of new neuroprotective molecules. Cationic arginine-rich peptides (CARPs) are an expanding and relatively novel class of compounds, which possess intrinsic neuroprotective properties. Intriguingly, CARPs possess a combination of biological properties unprecedented for a neuroprotective agent including the ability to traverse cell membranes and enter the CNS, antagonize calcium influx, target mitochondria, stabilize proteins, inhibit proteolytic enzymes, induce pro-survival signaling, scavenge toxic molecules, and reduce oxidative stress as well as, having a range of anti-inflammatory, analgesic, anti-microbial, and anti-cancer actions. CARPs have also been used as carrier molecules for the delivery of other putative neuroprotective agents across the blood-brain barrier and blood-spinal cord barrier. However, there is increasing evidence that the neuroprotective efficacy of many, if not all these other agents delivered using a cationic arginine-rich cell-penetrating peptide (CCPPs) carrier (e.g., TAT) may actually be mediated largely by the properties of the carrier molecule, with overall efficacy further enhanced according to the amino acid composition of the cargo peptide, in particular its arginine content. Therefore, in reviewing the neuroprotective mechanisms of action of CARPs we also consider studies using CCPPs fused to a putative neuroprotective peptide. We review the history of CARPs in neuroprotection and discuss in detail the intrinsic biological properties that may contribute to their cytoprotective effects and their usefulness as a broad-acting class of neuroprotective drugs.

Copyright © 2020 Meloni, Mastaglia and Knuckey.

Keywords: TAT; arginine; cationic arginine-rich peptides; cell-penetrating peptides; guanidinium head group; neuroprotection

References

  1. Biochem J. 1997 Jul 15;325 ( Pt 2):289-97 - PubMed
  2. J Neurotrauma. 2007 Jul;24(7):1093-107 - PubMed
  3. Brain Res. 2005 Aug 23;1054(1):1-8 - PubMed
  4. Neurodegener Dis. 2013;12(1):51-8 - PubMed
  5. Biochem Biophys Res Commun. 2011 Apr 15;407(3):501-6 - PubMed
  6. J Biol Chem. 2010 Jul 2;285(27):20675-82 - PubMed
  7. Brain Res. 2011 Mar 10;1378:137-43 - PubMed
  8. J Neurochem. 2007 Sep;102(6):1905-1917 - PubMed
  9. Nat Med. 2009 Dec;15(12):1399-406 - PubMed
  10. Nat Med. 2011 Jun 05;17(7):822-9 - PubMed
  11. Neurobiol Dis. 2010 May;38(2):266-72 - PubMed
  12. J Leukoc Biol. 2013 Jul;94(1):159-70 - PubMed
  13. Mol Neurobiol. 2016 Nov;53(9):5962-5970 - PubMed
  14. Neurosci Lett. 2005 Jun 24;381(3):305-8 - PubMed
  15. Int J Mol Sci. 2018 Sep 29;19(10): - PubMed
  16. J Cereb Blood Flow Metab. 2015 Jun;35(6):993-1004 - PubMed
  17. Cell Mol Life Sci. 2015 Feb;72(4):809-20 - PubMed
  18. J Neuroinflammation. 2015 Sep 17;12:172 - PubMed
  19. Mol Vis. 2009 Aug 05;15:1509-20 - PubMed
  20. Neuron. 2007 Feb 1;53(3):399-412 - PubMed
  21. Stroke. 2008 Sep;39(9):2544-53 - PubMed
  22. Biochim Biophys Acta. 2012 Jul;1818(7):1755-63 - PubMed
  23. Diabetes. 1998 Jul;47(7):1114-20 - PubMed
  24. Neuron. 2014 Sep 3;83(5):1144-58 - PubMed
  25. Peptides. 2018 Mar;101:135-144 - PubMed
  26. J Cereb Blood Flow Metab. 2019 Aug;39(8):1588-1601 - PubMed
  27. Nat Neurosci. 2014 Mar;17(3):471-80 - PubMed
  28. Acta Pharmacol Sin. 2003 Aug;24(8):746-50 - PubMed
  29. Future Med Chem. 2016;8(2):165-77 - PubMed
  30. AIDS Res Hum Retroviruses. 2001 Apr 10;17(6):475-86 - PubMed
  31. Neurochem Res. 2015 Jan;40(1):89-97 - PubMed
  32. J Neurosci. 2015 May 13;35(19):7349-64 - PubMed
  33. J Mol Neurosci. 2012 Sep;48(1):201-8 - PubMed
  34. Complement. 1988;5(3):153-62 - PubMed
  35. Food Chem Toxicol. 2018 May;115:315-328 - PubMed
  36. Mol Pain. 2012 Jul 24;8:54 - PubMed
  37. Neurochem Res. 2013 Oct;38(10):2095-104 - PubMed
  38. Brain Res. 2007 May 4;1144:146-55 - PubMed
  39. Proc Natl Acad Sci U S A. 2014 Jul 8;111(27):9971-6 - PubMed
  40. Biochem J. 1992 Jan 1;281 ( Pt 1):107-14 - PubMed
  41. Biopolymers. 2017 Sep;107(9): - PubMed
  42. Adv Drug Deliv Rev. 2008 Mar 1;60(4-5):452-72 - PubMed
  43. Sci Rep. 2017 Nov 24;7(1):16275 - PubMed
  44. Neurotox Res. 2009 Feb;15(2):123-6 - PubMed
  45. Cerebrovasc Dis. 2008;26(4):360-6 - PubMed
  46. Behav Brain Res. 2013 Jun 15;247:132-9 - PubMed
  47. Cell Mol Neurobiol. 2009 Feb;29(1):97-108 - PubMed
  48. Int J Nanomedicine. 2015 Aug 26;10:5423-34 - PubMed
  49. J Neurochem. 2007 Jul;102(1):65-76 - PubMed
  50. PLoS One. 2018 Jan 10;13(1):e0190449 - PubMed
  51. Mol Pharmacol. 2007 Jan;71(1):323-32 - PubMed
  52. Biosci Biotechnol Biochem. 2012;76(4):762-6 - PubMed
  53. Pain. 2018 May;159(5):849-863 - PubMed
  54. Neuroscience. 2010 Jun 30;168(2):523-30 - PubMed
  55. Proteomics. 2009 Jun;9(12):3257-67 - PubMed
  56. J Endocrinol. 2013 Sep 11;219(1):R13-35 - PubMed
  57. Free Radic Biol Med. 2014 Dec;77:239-48 - PubMed
  58. Neurocrit Care. 2006;4(1):25-31 - PubMed
  59. Anesthesiology. 2008 Jun;108(6):1071-80 - PubMed
  60. J Neurosci Res. 2013 Jun;91(6):799-807 - PubMed
  61. Clin Exp Pharmacol Physiol. 1998 Nov;25(11):908-12 - PubMed
  62. Mol Cell Neurosci. 2011 Apr;46(4):720-30 - PubMed
  63. J Neurosci. 2015 Nov 4;35(44):14727-39 - PubMed
  64. J Clin Invest. 2019 May 6;129(6):2390-2403 - PubMed
  65. Biochemistry. 2012 Jul 10;51(27):5531-9 - PubMed
  66. Eur J Pharmacol. 2016 Jun 5;780:166-73 - PubMed
  67. J Pharmacol Exp Ther. 2002 Jun;301(3):981-6 - PubMed
  68. Neuropharmacology. 2017 Oct;125:308-318 - PubMed
  69. Brain Res. 2010 Nov 11;1360:8-16 - PubMed
  70. Stroke. 2014 Oct;45(10):3089-91 - PubMed
  71. Exp Neurol. 2009 Jul;218(1):75-82 - PubMed
  72. Endocr J. 2009;56(4):609-17 - PubMed
  73. Nat Med. 2000 Jan;6(1):49-55 - PubMed
  74. J Mol Neurosci. 2008 Nov;36(1-3):270-8 - PubMed
  75. PLoS One. 2018 Mar 7;13(3):e0193884 - PubMed
  76. Brain Res. 2015 Oct 14;1623:30-8 - PubMed
  77. Cell Death Differ. 2019 Jan;26(2):260-275 - PubMed
  78. J Cereb Blood Flow Metab. 2015 May;35(5):739-42 - PubMed
  79. Arterioscler Thromb Vasc Biol. 1995 Mar;15(3):367-76 - PubMed
  80. Mol Cell Biochem. 2017 Feb;426(1-2):75-85 - PubMed
  81. Peptides. 2009 Jun;30(6):1153-7 - PubMed
  82. J Neurosci. 2006 Mar 29;26(13):3551-60 - PubMed
  83. J Neuropathol Exp Neurol. 2009 Sep;68(9):964-71 - PubMed
  84. J Cell Sci. 2005 Aug 1;118(Pt 15):3339-51 - PubMed
  85. Drug Deliv Transl Res. 2015 Jun;5(3):275-8 - PubMed
  86. Cell Physiol Biochem. 2017;44(1):388-400 - PubMed
  87. Peptides. 2002 Dec;23(12):2227-34 - PubMed
  88. J Immunol. 2005 May 1;174(9):5846-55 - PubMed
  89. PLoS One. 2011 Jan 17;6(1):e16259 - PubMed
  90. Neuropeptides. 2018 Feb;67:27-35 - PubMed
  91. J Biol Chem. 2011 Oct 28;286(43):37778-92 - PubMed
  92. J Pept Res. 2000 Nov;56(5):318-25 - PubMed
  93. Chem Pharm Bull (Tokyo). 2016;64(10):1431-1437 - PubMed
  94. J Neurosci Res. 2018 Nov;96(11):1816-1826 - PubMed
  95. J Mol Biol. 2016 Aug 14;428(16):3325-3336 - PubMed
  96. Neurobiol Dis. 2013 Jun;54:432-44 - PubMed
  97. J Neurochem. 2010 Jan;112(1):258-70 - PubMed
  98. J Neurosci. 2013 May 8;33(19):8185-201 - PubMed
  99. Stroke. 2001 Jan;32(1):168-74 - PubMed
  100. Nat Biotechnol. 1998 Mar;16(3):286-91 - PubMed
  101. Front Mol Neurosci. 2018 Sep 04;11:308 - PubMed
  102. J Neuropathol Exp Neurol. 2009 Jul;68(7):823-31 - PubMed
  103. J Control Release. 2007 Feb 12;117(2):148-62 - PubMed
  104. Biochem Biophys Res Commun. 1997 May 8;234(1):35-8 - PubMed
  105. Ann N Y Acad Sci. 2006 Jul;1070:531-4 - PubMed
  106. J Neurotrauma. 2009 Jan;26(1):121-9 - PubMed
  107. Int J Mol Sci. 2015 Nov 16;16(11):27391-400 - PubMed
  108. Front Physiol. 2015 Apr 10;6:115 - PubMed
  109. Sci Rep. 2017 Apr 21;7:46461 - PubMed
  110. Aging Cell. 2008 Mar;7(2):260-9 - PubMed
  111. Biochim Biophys Acta. 2012 Nov;1818(11):2669-78 - PubMed
  112. Brain Res. 1999 Aug 21;839(1):66-73 - PubMed
  113. Neurobiol Dis. 2019 Jan;121:17-33 - PubMed
  114. Biochimie. 2015 Sep;116:24-33 - PubMed
  115. Stroke. 2009 Feb;40(2):632-9 - PubMed
  116. Proc Natl Acad Sci U S A. 1989 Jul;86(14):5631-5 - PubMed
  117. Cell Signal. 2012 May;24(5):991-1001 - PubMed
  118. Cell Death Dis. 2015 Oct 22;6:e1939 - PubMed
  119. Biochem Biophys Res Commun. 2002 Jan 11;290(1):47-52 - PubMed
  120. J Mol Neurosci. 2017 Feb;61(2):235-246 - PubMed
  121. Exp Neurol. 2001 Jan;167(1):74-85 - PubMed
  122. Neuroscience. 2003;116(2):437-45 - PubMed
  123. J Neurotrauma. 2007 Jul;24(7):1108-18 - PubMed
  124. Biochim Biophys Acta. 2015 Feb;1848(2):593-602 - PubMed
  125. Sci Rep. 2016 Oct 07;6:34834 - PubMed
  126. FEBS J. 2016 Jun;283(11):2115-31 - PubMed
  127. J Exp Med. 2016 Nov 14;213(12):2655-2669 - PubMed
  128. Behav Brain Res. 2010 Dec 25;214(2):395-401 - PubMed
  129. J Mol Neurosci. 2017 Jan;61(1):42-51 - PubMed
  130. Neuropharmacology. 2006 Sep;51(3):497-505 - PubMed
  131. PLoS One. 2015 Nov 17;10(11):e0143038 - PubMed
  132. Ann Neurol. 2014 Mar;75(3):395-410 - PubMed
  133. Eur J Pharm Biopharm. 2009 May;72(1):219-25 - PubMed
  134. Cornea. 2010 Nov;29(11):1308-14 - PubMed
  135. Mol Pharm. 2010 Dec 6;7(6):2224-31 - PubMed
  136. Transl Neurosci. 2012 Mar;3(1):1-8 - PubMed
  137. FASEB J. 2017 Jun;31(6):2507-2519 - PubMed
  138. Chem Res Toxicol. 2016 Feb 15;29(2):227-34 - PubMed
  139. Stroke. 2006 Oct;37(10):2613-9 - PubMed
  140. Exp Eye Res. 2018 Dec;177:12-22 - PubMed
  141. Neuroscience. 2008 Mar 18;152(2):308-20 - PubMed
  142. J Neurosci. 2009 Nov 11;29(45):14057-65 - PubMed
  143. Biochemistry. 2003 Aug 5;42(30):8976-87 - PubMed
  144. Cell Death Differ. 2007 Feb;14(2):240-53 - PubMed
  145. EMBO Mol Med. 2017 May;9(5):703-715 - PubMed
  146. J Clin Invest. 2010 Oct;120(10):3480-92 - PubMed
  147. J Clin Pharmacol. 2017 Jun;57(6):770-776 - PubMed
  148. J Oleo Sci. 2011;60(10):537-44 - PubMed
  149. J Neurochem. 2011 Sep;118(6):1113-23 - PubMed
  150. Science. 1999 Sep 3;285(5433):1569-72 - PubMed
  151. Small. 2014 Apr 9;10(7):1250-4 - PubMed
  152. Biochemistry. 2005 Mar 29;44(12):4919-25 - PubMed
  153. FEBS Lett. 2000 Sep 15;481(2):131-6 - PubMed
  154. Biochem J. 2014 Jul 1;461(1):137-46 - PubMed
  155. Mol Neurobiol. 2016 Nov;53(9):6332-6341 - PubMed
  156. Br J Pharmacol. 2018 Jun;175(12):2244-2260 - PubMed
  157. J Biol Chem. 1994 Nov 18;269(46):29024-31 - PubMed
  158. J Neurochem. 2014 Jan;128(1):196-204 - PubMed
  159. Int J Environ Res Public Health. 2016 Sep 29;13(10): - PubMed
  160. J Med Chem. 2002 Aug 15;45(17):3612-8 - PubMed
  161. Front Neurosci. 2015 Feb 09;9:23 - PubMed
  162. Immunology. 2012 Sep;137(1):65-79 - PubMed
  163. J Biol Chem. 2006 Jun 23;281(25):17432-45 - PubMed
  164. J Neurosci Res. 2014 Jul;92(7):884-92 - PubMed
  165. Stroke. 2004 Jun;35(6):1506-18 - PubMed
  166. J Pharmacol Exp Ther. 2012 Jul;342(1):196-204 - PubMed
  167. J Biol Chem. 2001 Feb 2;276(5):3254-61 - PubMed
  168. J Neurochem. 2011 Apr;117(2):346-56 - PubMed
  169. Stroke Res Treat. 2016;2016:2372710 - PubMed
  170. Stroke. 2004 Jul;35(7):1738-43 - PubMed
  171. Cell Mol Life Sci. 2012 Jul;69(14):2315-25 - PubMed
  172. PLoS One. 2014 Mar 27;9(3):e92597 - PubMed
  173. PLoS One. 2015 Apr 09;10(4):e0119204 - PubMed
  174. J Neurochem. 2009 Feb;108(3):552-62 - PubMed
  175. Neurobiol Dis. 2012 Jun;46(3):710-21 - PubMed
  176. Neuroscience. 2010 May 5;167(2):490-500 - PubMed
  177. J Neurosci Res. 2009 Feb 15;87(3):677-82 - PubMed
  178. Int Immunol. 2006 Dec;18(12):1729-36 - PubMed
  179. Hippocampus. 2015 Jan;25(1):62-71 - PubMed
  180. PLoS One. 2015 Jun 25;10(6):e0130417 - PubMed
  181. J Cereb Blood Flow Metab. 2017 May;37(5):1820-1828 - PubMed
  182. J Neurosci. 2017 Jun 7;37(23):5648-5658 - PubMed
  183. Am J Physiol. 1999 Sep;277(3):H1007-13 - PubMed
  184. Eur J Biochem. 2000 Jun;267(11):3330-6 - PubMed
  185. J Alzheimers Dis. 2010;20 Suppl 2:S609-31 - PubMed
  186. AAPS J. 2006 Apr 21;8(2):E277-83 - PubMed
  187. Atherosclerosis. 2010 Jan;208(1):134-41 - PubMed
  188. Nat Med. 2010 Dec;16(12):1393-5 - PubMed
  189. J Neurochem. 2013 Mar;124(6):869-79 - PubMed
  190. J Pharmacol Exp Ther. 2006 Sep;318(3):956-65 - PubMed
  191. Neurochem Int. 2008 May;52(6):1256-65 - PubMed
  192. Neuroscientist. 2008 Oct;14(5):409-14 - PubMed
  193. J Biol Chem. 2011 Dec 23;286(51):43871-80 - PubMed
  194. PLoS One. 2012;7(4):e34504 - PubMed
  195. Mediators Inflamm. 2012;2012:318087 - PubMed
  196. Front Cell Neurosci. 2016 Mar 04;10:56 - PubMed
  197. Traffic. 2013 Nov;14(11):1182-91 - PubMed
  198. J Biol Chem. 2006 Jul 7;281(27):18317-26 - PubMed
  199. Sci Rep. 2016 Feb 22;6:21759 - PubMed
  200. Neurocrit Care. 2012 Apr;16(2):316-26 - PubMed
  201. Behav Brain Res. 2004 May 5;151(1-2):303-12 - PubMed
  202. J Neurosci. 2009 Jul 22;29(29):9330-43 - PubMed
  203. Cell. 2010 Jan 22;140(2):222-34 - PubMed
  204. Neuropharmacology. 2019 May 15;150:100-111 - PubMed
  205. Nature. 2015 Feb 19;518(7539):404-8 - PubMed
  206. PLoS One. 2009 Dec 07;4(12):e8191 - PubMed
  207. Stroke. 2000 Jun;31(6):1411-7 - PubMed
  208. Science. 2002 Oct 25;298(5594):846-50 - PubMed
  209. Expert Opin Drug Metab Toxicol. 2016 Aug;12(8):897-909 - PubMed
  210. Ann N Y Acad Sci. 1995 Sep 15;765:210-29 - PubMed
  211. J Biol Chem. 2002 Jan 25;277(4):2437-43 - PubMed
  212. Neurotherapeutics. 2019 Dec 12;: - PubMed
  213. J Pharmacol Sci. 2017 Jan;133(1):34-41 - PubMed
  214. J Cereb Blood Flow Metab. 2013 Dec;33(12):1937-43 - PubMed
  215. J Biol Chem. 1989 Nov 15;264(32):19318-26 - PubMed
  216. J Pharmacol Exp Ther. 1999 Feb;288(2):544-9 - PubMed
  217. J Neurochem. 2016 May;137(3):446-59 - PubMed
  218. Peptides. 2015 Jan;63:55-62 - PubMed
  219. Mol Neurobiol. 2017 Oct;54(8):6061-6073 - PubMed
  220. J Neurosci. 2008 Oct 15;28(42):10696-710 - PubMed
  221. J Biol Chem. 2003 Dec 5;278(49):48529-33 - PubMed
  222. Acta Neuropathol Commun. 2014 Aug 05;2:86 - PubMed
  223. Br J Pharmacol. 1998 Jul;124(5):905-10 - PubMed
  224. J Clin Invest. 2000 Aug;106(3):439-48 - PubMed
  225. Exp Cell Res. 2010 Jul 1;316(11):1773-83 - PubMed
  226. Biochim Biophys Acta Gen Subj. 2017 Aug;1861(8):1901-1912 - PubMed
  227. PLoS One. 2013;8(1):e54769 - PubMed
  228. Biochim Biophys Acta Mol Basis Dis. 2017 Mar;1863(3):654-662 - PubMed
  229. Front Neurol. 2017 Oct 16;8:556 - PubMed
  230. J Immunol Res. 2017;2017:8193932 - PubMed
  231. Fundam Clin Pharmacol. 1999;13(5):535-40 - PubMed
  232. Front Cell Neurosci. 2015 Jan 26;8:471 - PubMed
  233. J Cereb Blood Flow Metab. 2019 Nov;39(11):2233-2245 - PubMed
  234. Mol Ther. 2011 Oct;19(10):1849-57 - PubMed
  235. J Neuropathol Exp Neurol. 2019 May 1;78(5):426-435 - PubMed
  236. Biopolymers. 2011 Oct;95(10):722-31 - PubMed
  237. Biochem Soc Trans. 2014 Apr;42(2):425-32 - PubMed
  238. J Immunol. 2004 Mar 15;172(6):3758-65 - PubMed
  239. Brain Res. 1996 Nov 25;741(1-2):82-8 - PubMed
  240. J Neurosci. 2010 Jun 2;30(22):7575-86 - PubMed
  241. ChemMedChem. 2008 Dec;3(12):1848-52 - PubMed
  242. Free Radic Biol Med. 2016 Jul;96:89-98 - PubMed
  243. Neurosci Res. 2017 Jan;114:9-15 - PubMed
  244. Peptides. 2018 Jan;99:61-69 - PubMed
  245. Circulation. 2004 Apr 6;109(13):1660-7 - PubMed
  246. CNS Neurosci Ther. 2015 Apr;21(4):385-91 - PubMed
  247. J Neurol Neurophysiol. 2013 Apr;2014(Suppl 12):10 - PubMed
  248. Mar Drugs. 2017 Oct 13;15(10): - PubMed
  249. Exp Ther Med. 2019 May;17(5):4109-4115 - PubMed
  250. J Cereb Blood Flow Metab. 2005 Jun;25(6):694-712 - PubMed
  251. Proc Natl Acad Sci U S A. 2012 Feb 28;109(9):3317-22 - PubMed
  252. J Neurotrauma. 2010 Jun;27(6):1143-55 - PubMed
  253. Pharmacol Ther. 2015 Sep;153:36-54 - PubMed
  254. Proc Natl Acad Sci U S A. 2016 Oct 4;113(40):11324-11329 - PubMed
  255. Arch Biochem Biophys. 2003 Nov 1;419(1):31-40 - PubMed
  256. J Biol Chem. 2004 Aug 27;279(35):36788-94 - PubMed
  257. Nat Med. 2003 Sep;9(9):1180-6 - PubMed
  258. Free Radic Res. 2017 Mar;51(3):316-328 - PubMed
  259. Virology. 2003 Jul 20;312(1):196-203 - PubMed
  260. ACS Chem Neurosci. 2019 Jan 16;10(1):746-756 - PubMed
  261. Inflammation. 2014 Oct;37(5):1401-12 - PubMed
  262. J Pharmacol Exp Ther. 2001 Sep;298(3):1133-41 - PubMed
  263. Brain. 2006 Feb;129(Pt 2):465-79 - PubMed
  264. J Mol Biol. 2008 Dec 5;384(1):219-27 - PubMed
  265. Peptides. 2016 Jan;75:96-100 - PubMed
  266. Acta Biochim Biophys Sin (Shanghai). 2017 Jun 1;49(6):471-478 - PubMed
  267. Basic Res Cardiol. 2016 Jan;111(1):2 - PubMed
  268. Mol Pharmacol. 2011 Dec;80(6):1085-95 - PubMed
  269. PLoS One. 2015 Oct 14;10(10):e0139652 - PubMed
  270. Brain Behav Immun. 2010 Jul;24(5):812-21 - PubMed
  271. ACS Med Chem Lett. 2012 May 10;3(5):407-410 - PubMed
  272. Neuroscience. 2006 May 12;139(2):609-27 - PubMed
  273. Nat Med. 2008 Dec;14(12):1325-32 - PubMed
  274. Cerebrovasc Dis. 2010;29(6):564-70 - PubMed
  275. Biosci Biotechnol Biochem. 2019 Jun;83(6):1094-1101 - PubMed
  276. Front Mol Neurosci. 2017 Jan 23;10:1 - PubMed
  277. J Biol Chem. 2005 Feb 25;280(8):6561-9 - PubMed
  278. Mol Ther. 2011 Oct;19(10):1780-92 - PubMed
  279. J Phys Chem B. 2010 Oct 28;114(42):13426-38 - PubMed
  280. Atherosclerosis. 2014 Sep;236(1):133-41 - PubMed
  281. Bioorg Med Chem. 2018 Jun 1;26(10):2780-2787 - PubMed
  282. Lab Invest. 2010 Feb;90(2):156-67 - PubMed
  283. J Biol Chem. 2013 Jan 11;288(2):1079-87 - PubMed
  284. J Neurosci. 2004 Aug 4;24(31):6880-8 - PubMed
  285. Proc Natl Acad Sci U S A. 1996 Jun 11;93(12):6014-8 - PubMed
  286. Mol Brain. 2018 Feb 9;11(1):8 - PubMed
  287. J Neurochem. 2010 Jun;113(5):1307-18 - PubMed
  288. Hippocampus. 2018 Oct;28(10):724-734 - PubMed
  289. Biochem Biophys Res Commun. 2004 Aug 27;321(3):601-5 - PubMed
  290. J Thorac Cardiovasc Surg. 2003 Oct;126(4):1065-70 - PubMed
  291. Peptides. 2014 Jun;56:84-93 - PubMed
  292. J Biol Chem. 2015 Sep 4;290(36):22030-48 - PubMed
  293. Arthritis Rheum. 2010 Feb;62(2):441-51 - PubMed
  294. Exp Neurol. 2005 Mar;192(1):109-16 - PubMed
  295. J Neurotrauma. 2012 Sep;29(13):2332-41 - PubMed
  296. ACS Chem Neurosci. 2018 Jul 18;9(7):1566-1571 - PubMed
  297. Biochemistry. 2005 Jun 21;44(24):8898-907 - PubMed
  298. Circulation. 2000 Nov 21;102(21):2629-35 - PubMed
  299. J Cereb Blood Flow Metab. 2007 Apr;27(4):697-709 - PubMed
  300. Eur J Neurosci. 2010 Apr;31(7):1261-72 - PubMed
  301. Lancet Neurol. 2012 Nov;11(11):942-50 - PubMed
  302. Neuromolecular Med. 2017 Sep;19(2-3):271-285 - PubMed
  303. Channels (Austin). 2012 Jan-Feb;6(1):52-9 - PubMed
  304. J Mol Neurosci. 2012 Nov;48(3):526-40 - PubMed
  305. Elife. 2017 Jul 21;6: - PubMed
  306. Brain. 2012 Nov;135(Pt 11):3282-97 - PubMed
  307. Am J Physiol Heart Circ Physiol. 2001 Dec;281(6):H2612-8 - PubMed
  308. J Biol Chem. 2008 Jun 13;283(24):16752-61 - PubMed
  309. Cell. 2010 Aug 6;142(3):387-97 - PubMed
  310. Neurosci Lett. 2016 Aug 3;627:92-9 - PubMed
  311. Int J Mol Sci. 2011 Feb 08;12(2):1060-5 - PubMed
  312. Invest Ophthalmol Vis Sci. 2010 Feb;51(2):1198-207 - PubMed
  313. ASN Neuro. 2015 Sep 21;7(5): - PubMed
  314. Neurobiol Dis. 2016 May;89:101-11 - PubMed
  315. Cold Spring Harb Perspect Biol. 2009 Dec;1(6):a001651 - PubMed
  316. Neuropeptides. 2017 Feb;61:15-22 - PubMed
  317. Biochemistry. 2003 Jul 29;42(29):8663-70 - PubMed
  318. Eur J Pharmacol. 2016 Nov 15;791:213-220 - PubMed
  319. J Neurosci. 2013 May 1;33(18):7997-8008 - PubMed
  320. Biosci Biotechnol Biochem. 2011;75(8):1496-501 - PubMed
  321. Eur J Pharmacol. 2007 Mar 29;560(1):29-35 - PubMed
  322. Transl Neurosci. 2017 Nov 15;8:147-157 - PubMed
  323. Molecules. 2019 Jun 15;24(12): - PubMed
  324. J Neurotrauma. 2012 Jul 1;29(10):1941-59 - PubMed
  325. Exp Neurol. 2015 Nov;273:253-62 - PubMed
  326. Pharmacol Ther. 2018 Mar;183:160-176 - PubMed
  327. Cell Mol Neurobiol. 2014 Mar;34(2):173-81 - PubMed
  328. J Biol Chem. 1990 Mar 5;265(7):3763-71 - PubMed
  329. Cell Mol Life Sci. 2016 Sep;73(17):3221-47 - PubMed
  330. J Biol Chem. 2000 Nov 24;275(47):36741-9 - PubMed
  331. Stroke. 2011 Nov;42(11):3265-70 - PubMed
  332. Biochim Biophys Acta. 2014 Apr 4;1841(4):620-9 - PubMed
  333. Int J Mol Sci. 2017 Mar 21;18(3): - PubMed
  334. J Biol Chem. 2011 Feb 4;286(5):3839-50 - PubMed
  335. FASEB J. 2013 Feb;27(2):738-49 - PubMed
  336. Cell Immunol. 2012 Nov;280(1):22-35 - PubMed
  337. J Dent Res. 2017 Mar;96(3):254-260 - PubMed
  338. J Neurosci. 2014 May 7;34(19):6546-56 - PubMed
  339. Annu Rev Pharmacol Toxicol. 2016;56:511-33 - PubMed
  340. Brain Res. 2004 Nov 5;1026(1):151-6 - PubMed
  341. J Neurosci Res. 1999 Jul 15;57(2):280-9 - PubMed
  342. Brain Res. 2012 Dec 13;1489:140-8 - PubMed
  343. Chem Biol Drug Des. 2007 Aug;70(2):154-7 - PubMed
  344. PLoS One. 2013 Aug 09;8(8):e71650 - PubMed
  345. Neurochem Res. 2009 Nov;34(11):2008-21 - PubMed
  346. Naunyn Schmiedebergs Arch Pharmacol. 2002 Apr;365(4):269-76 - PubMed
  347. Proc Natl Acad Sci U S A. 2017 Apr 4;114(14):3750-3755 - PubMed
  348. Oncotarget. 2017 Jun 2;8(35):59929-59939 - PubMed
  349. BMC Neurosci. 2016 May 03;17(1):19 - PubMed
  350. Brain Res. 1996 Oct 14;736(1-2):280-6 - PubMed
  351. Mol Pharmacol. 2002 May;61(5):1081-8 - PubMed
  352. Antioxid Redox Signal. 2009 Sep;11(9):2095-104 - PubMed
  353. Proc Natl Acad Sci U S A. 1991 Jul 15;88(14):6368-71 - PubMed
  354. J Pharmacol Exp Ther. 2010 Jul;334(1):106-15 - PubMed
  355. Neuropharmacology. 2019 Jul 15;153:82-97 - PubMed
  356. Ann Clin Transl Neurol. 2017 Mar 09;4(4):246-265 - PubMed
  357. Neurochem Int. 2013 Nov;63(6):535-40 - PubMed
  358. Acc Chem Res. 2013 Apr 16;46(4):885-93 - PubMed
  359. Nature. 2012 Feb 29;483(7388):213-7 - PubMed
  360. Neurosci Lett. 1995 Jan 16;184(1):32-5 - PubMed
  361. Neurobiol Aging. 2010 Feb;31(2):203-14 - PubMed
  362. Mol Immunol. 2014 Feb;57(2):86-92 - PubMed
  363. Neurosci Lett. 2016 Aug 15;628:219-24 - PubMed
  364. Virology. 2003 Dec 5;317(1):84-94 - PubMed
  365. Neurosci Lett. 1998 Jul 10;250(3):185-8 - PubMed

Publication Types